Sonic Hedgehog (Shh) and Fluoride

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Sonic Hedgehog (Shh) and Fluoride

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August 20, 2013

Since the late 1990s, it has been known that the Sonic Hedgehog gene (Shh) controls tooth growth and morphogenesis (Dassule et al, 2000).

Shh is a thyroid-hormone (TH)-responsive gene.

Shh and Dental Fluorosis

Shh and Dental Fluorosis

Although fluoride and dental fluorosis (DF) have been studied for over 80 years, dental researchers continue to claim that the mechanisms leading to DF are not yet fully understood.
For 20 years we have investigated the literature on this matter and have come to the conclusion that DF is caused by disturbances in thyroid hormone metabolism - that DF is a visual sign that TH metabolism and regulated pathways have been disturbed at a time crucial for development.

To strengthen our case, we have searched worldwide for any research documenting the effects of fluoride on Shh, and more specifically, Shh's role in DF.

We were astonished to discover that no studies on Shh and dental fluorosis (DF) were found in major medical literature databases such as PubMed or SciFinder.

It appeared that no one had yet recognized the importance of investigating this connection.

Today (thanks to Jirong), we found the first studies on the effects of fluoride on Shh in DF. They were found in the Chinese literature. Two papers on the subject had been published, one in 2007 and one in 2012.

As we had expected - the studies show that fluoride affects the expression of Shh.

UPDATE: Shh pathways involve Gq/11 and deiodinase 3 (DIO3) (Ostasov e al., 2020; Adachi et al., 2019; El-Zaatari et al., 2010; Aw et al, 2014; Luongo et al., 2014; Castellone et al, 2015).

PFPC Canada

Shh & Dental Fluorosis

Chen L, Wang Y, Yang W, Tian M - "Effects of different selenium levels on tooth germ development in fluorosis rats" Journal of Oral Science Research 5:417-419, 422 (2012) PFPC Library
Objective: To investigate the effects of different selenium levels on the development of dental germs in rats with fluorosis and to explore the underlying molecular mechanisms.

Methods: Sixty male Sprague-Dawley (SD) rats were randomly divided into six groups. The control group was fed a normal diet and given distilled water. The fluoride group was fed a normal diet but given distilled water containing 45 mg/L fluoride (F−). The four fluoride + selenium groups were fed a fluoride-containing diet along with varying selenium levels: 1.37 mg/kg (Group 1), 1.6 mg/kg (Group 2), 2.3 mg/kg (Group 3), and 4 mg/kg (Group 4). At the end of the experiment, all rats were sacrificed, and incisor specimens were collected. Immunohistochemistry was performed to detect the expression of Smad3 and Shh in secretory ameloblasts.

Results: Positive expression of Smad3 and Shh was observed in secretory ameloblasts of the control group. In the fluoride group, the expression of Smad3 and Shh was significantly reduced compared to the control group. The fluoride + selenium groups showed stronger expression of Smad3 and Shh compared to the fluoride-only group, with the most pronounced effect observed in the 2.3 mg/kg selenium group (Group 3).

Conclusion: Selenium may antagonize the adverse effects of fluoride on dental germ development, possibly by modulating the expression of key signal transduction factors Smad3 and Shh. The optimal selenium dosage for mitigating fluoride-induced disruptions in dental germ development was found to be 2.3 mg/kg.
Liu H, Wang O, Zhu F, Luo PP, Liu TL, Wei XL, Wang LL - "Effect of fluorosis on the expression of Shh in rat incisors" Beijing Journal of Stomatology 15(4) (2007) PFPC Library
目的 研究过量氟对大鼠切牙Shh(Sonic Hedgehog)表达的影响,从分子水平探讨氟斑牙的发病机制.方法 20只Wistar大鼠随机分为2组:对照组(饮用蒸馏水)和实验组(饮用100 mg/L氟化水),复制氟斑牙动物模型,8周末处死动物,获取切牙标本,免疫组化染色观察Shh在大鼠切牙的表达定位及在对照组与实验组切牙表达的变化.结果 Shh在分泌期成釉细胞、成牙本质阳性表达.实验组Shh的表达明显弱于对照组,差异有显著性(P<.01).结论 过量氟可能通过抑制Shh的表达,从而影响牙齿发育的启动和随后的细胞分化,导致釉质发育障碍.

Objective: To investigate the effect of excessive fluoride on Sonic Hedgehog (Shh) expression in rat incisors and to explore the molecular mechanisms underlying the pathogenesis of dental fluorosis.

Methods: Twenty Wistar rats were randomly assigned to two groups: a control group (receiving distilled water) and an experimental group (receiving 100 mg/L fluoride in drinking water) to establish an animal model of dental fluorosis. After 8 weeks, the rats were sacrificed, and incisor specimens were collected. Immunohistochemical staining was performed to localize and quantify Shh expression in the incisor tissues, and expression changes between the control and experimental groups were compared.

Results: Shh was expressed in secretory ameloblasts and odontoblasts. In the experimental group, Shh expression was significantly reduced compared to the control group, with the difference being statistically significant (P < 0.01).

Conclusions: Excessive fluoride may inhibit Shh expression, thereby disrupting the initiation of tooth development and subsequent cell differentiation, ultimately leading to enamel developmental disorders.

SEE ALSO - smad3

Luo Pingping, Wang Qiang, Liu Hui - "Excessive fluoride during the development of rat incisor smad3 expression" Practical Stomatology, 3:377-379 (2007) PFPC Library


Shh & Thyroid Hormone | Deiodinase

Desouza LA, Sathanoori M, Kapoor R, Rajadhyaksha N, Gonzalez LE, Kottmann AH, Tole S, Vaidya VA - "Thyroid hormone regulates the expression of the sonic hedgehog signaling pathway in the embryonic and adult Mammalian brain" Endocrinology 152(5):1989-2000 (2011)
https://academic.oup.com/endo/article/1 ... 89/2457119

Dentice M - "Hedgehog-mediated regulation of thyroid hormone action through iodothyronine deiodinases" Expert Opin Ther Targets 15(4):493-504 (2011)
https://www.tandfonline.com/doi/full/10 ... 011.553607


Shh & Tooth Development

Dassule HR, Lewis P, Bei M, Maas R, McMahon AP - "Sonic hedgehog regulates growth and morphogenesis of the tooth" Development 127(22):4775-85 (2000)
http://dev.biologists.org/content/127/22/4775.long

Gritli-Linde A, Bei M, Mass R,et al. - "Shh signaling within the dental epithelium is necessary for cell proliferation, growth and polarization" Development 129(23):5323 (2002)
https://journals.biologists.com/dev/art ... thelium-is

Hardcastle Z, Hui CC, Sharpe PT - "The Shh signalling pathway in early tooth development" Cell Mol Biol (Noisy-le-grand) 45(5):567-78 (1999) PMID: 10512189.
https://pubmed.ncbi.nlm.nih.gov/10512189/

Zhang Lu, Sun Zhijun, Wang Zhifeng, Hua Fang, Zhang Qi, Chen Zhi - "Expression of Shh and Its Recepters mRNA in the Late Tooth Development of Murine Lower Incisor" Journal of Wuhan University: Medical Edition 4:419-421 (2004) PFPC Library
Objective: To investigate the temporal and spatial expression of Shh and its receptors Ptc1、Ptc2 mRNA in the late tooth development of murine lower incisor and to discuss its role in cyto diff erentiation.Methods: The embryonic mouse mandibles of late incisor development(E18.5~P 1.5 ) were obtained and 5μm serial sections were made. DIG labeling RNA probes of Shh,Ptc1 and Ptc2 were generated by in vitro transcription from Shh、Ptc1、Ptc2 cDNA template. The expression pattern of Shh,Ptc1 and Ptc2 mRNA was analyzed by means of in situ hybridization. Results: The expression pattern of Shh and Ptc2 was similar. In the late tooth development,they were expressed in the inner dental epithelium and stratum intermedium of the incisor labial side. Ptc1 mRNA was expressed in the inner dental epithelium and stratum intermedium as well as the odontoblast. Conclusion: In the late incisor development,Shh might participate in the ameloblast and odontoblast differentiation as a paracrine or autocrine signaling molecule.

林媛;吴补领;陆群 Shh在大鼠牙胚发育过程中的表达 [期刊论文] -临床口腔医学杂志2004(04) doi:10.3969/j.issn.1003-1634.2004.04.004
Lin Y, Wu BL, Lu Q - "Expression of Shh during the development of rat tooth germs" J Clin Stomato (04) (2004) doi:10.3969/j.issn.1003-1634.2004.04.004.

陈智;张露;王志峰 Shh及其受体Ptc1、Ptc2在鼠帽状期磨牙的基因表达 [期刊论文] -中华口腔医学杂志2003(02)
Chen Z, Zhang L, Wang ZF - "Gene expression of Shh and its receptors Ptc1 and Ptc2 in mouse molars at the cap stage" Chin J Stomatol (02) (2003)

杜娟;刘淑红;范文红 Sonic hedgehog在小鼠胚胎颌面部的表达 [期刊论文] -北京口腔医学2005(01)
Du J, Liu SH, Fan WH - "Expression of Sonic Hedgehog in the craniofacial region of mouse embryos" Beijing J Stomatol (01) 2005
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Sonic Hedgehog - SHH and T3

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Ostasov P, Tuma J, Pitule P, Moravec J, Houdek Z, Vozeh F, Kralickova M, Cendelin J, Babuska Vm - "Sonic Hedgehog and Triiodothyronine Pathway Interact in Mouse Embryonic Neural Stem Cells" Int J Mol Sci 21(10):3672 (2020)
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7279276/
Abstract

Neural stem cells are fundamental to development of the central nervous system (CNS)-as well as its plasticity and regeneration-and represent a potential tool for neuro transplantation therapy and research. This study is focused on examination of the proliferation dynamic and fate of embryonic neural stem cells (eNSCs) under differentiating conditions. In this work, we analyzed eNSCs differentiating alone and in the presence of sonic hedgehog (SHH) or triiodothyronine (T3) which play an important role in the development of the CNS. We found that inhibition of the SHH pathway and activation of the T3 pathway increased cellular health and survival of differentiating eNSCs. In addition, T3 was able to increase the expression of the gene for the receptor smoothened (Smo), which is part of the SHH signaling cascade, while SHH increased the expression of the T3 receptor beta gene (Thrb). This might be the reason why the combination of SHH and T3 increased the expression of the thyroxine 5-deiodinase type III gene (Dio3), which inhibits T3 activity, which in turn affects cellular health and proliferation activity of eNSCs.
Desouza LA, Sathanoori M, Kapoor R, Rajadhyaksha N, Gonzalez LE, Kottmann AH, Tole S, Vaidya VA - "Thyroid hormone regulates the expression of the sonic hedgehog signaling pathway in the embryonic and adult Mammalian brain" Endocrinology 152(5):1989-2000 (2011) doi: 10.1210/en.2010-1396
https://pmc.ncbi.nlm.nih.gov/articles/PMC3179409/
Abstract

Thyroid hormone is important for development and plasticity in the immature and adult mammalian brain. Several thyroid hormone-responsive genes are regulated during specific developmental time windows, with relatively few influenced across the lifespan. We provide novel evidence that thyroid hormone regulates expression of the key developmental morphogen sonic hedgehog (Shh), and its coreceptors patched (Ptc) and smoothened (Smo), in the early embryonic and adult forebrain. Maternal hypo- and hyperthyroidism bidirectionally influenced Shh mRNA in embryonic forebrain signaling centers at stages before fetal thyroid hormone synthesis. Further, Smo and Ptc expression were significantly decreased in the forebrain of embryos derived from hypothyroid dams. Adult-onset thyroid hormone perturbations also regulated expression of the Shh pathway bidirectionally, with a significant induction of Shh, Ptc, and Smo after hyperthyroidism and a decline in Smo expression in the hypothyroid brain. Short-term T₃ administration resulted in a significant induction of cortical Shh mRNA expression and also enhanced reporter gene expression in Shh(+/LacZ) mice. Further, acute T₃ treatment of cortical neuronal cultures resulted in a rapid and significant increase in Shh mRNA, suggesting direct effects. Chromatin immunoprecipitation assays performed on adult neocortex indicated enhanced histone acetylation at the Shh promoter after acute T₃ administration, providing further support that Shh is a thyroid hormone-responsive gene. Our results indicate that maternal and adult-onset perturbations of euthyroid status cause robust and region-specific changes in the Shh pathway in the embryonic and adult forebrain, implicating Shh as a possible mechanistic link for specific neurodevelopmental effects of thyroid hormone.
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Re: Shh and Gq/11

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Shh acts via Gq/11 pathways

Adachi C, Kakinuma N, Jo SH, Ishii T, Arai Y, Arai S, Kitaguchi T, Takeda S, Inoue T - "Sonic hedgehog enhances calcium oscillations in hippocampal astrocytes" J Biol Chem 294(44):16034-16048 (2019) doi: 10.1074/jbc.RA119.007883
https://pubmed.ncbi.nlm.nih.gov/31506300/
Abstract

Sonic hedgehog (SHH) is important for organogenesis during development. Recent studies have indicated that SHH is also involved in the proliferation and transformation of astrocytes to the reactive phenotype. However, the mechanisms underlying these are unknown. Involvement of SHH signaling in calcium (Ca) signaling has not been extensively studied. Here, we report that SHH and Smoothened agonist (SAG), an activator of the signaling receptor Smoothened (SMO) in the SHH pathway, activate Ca oscillations in cultured murine hippocampal astrocytes. The response was rapid, on a minute time scale, indicating a noncanonical pathway activity. Pertussis toxin blocked the SAG effect, indicating an involvement of a Gi coupled to SMO. Depletion of extracellular ATP by apyrase, an ATP-degrading enzyme, inhibited the SAG-mediated activation of Ca oscillations. These results indicate that SAG increases extracellular ATP levels by activating ATP release from astrocytes, resulting in Ca oscillation activation. We hypothesize that SHH activates SMO-coupled Gi in astrocytes, causing ATP release and activation of Gq/11-coupled P2 receptors on the same cell or surrounding astrocytes. Transcription factor activities are often modulated by Ca patterns; therefore, SHH signaling may trigger changes in astrocytes by activating Ca oscillations. This enhancement of Ca oscillations by SHH signaling may occur in astrocytes in the brain in vivo because we also observed it in hippocampal brain slices. In summary, SHH and SAG enhance Ca oscillations in hippocampal astrocytes, Gi mediates SAG-induced Ca oscillations downstream of SMO, and ATP-permeable channels may promote the ATP release that activates Ca oscillations in astrocytes.
El-Zaatari M, Zavros Y, Tessier A, Waghray M, Lentz S, Gumucio D, Todisco A, Merchant JL - "Intracellular calcium release and protein kinase C activation stimulate sonic hedgehog gene expression during gastric acid secretion" Gastroenterology 139(6):2061-2071.e2 (2010). doi: 10.1053/j.gastro.2010.08.047
https://linkinghub.elsevier.com/retriev ... 10)01297-7
Abstract

Background & aims: Hypochlorhydria during Helicobacter pylori infection inhibits gastric Sonic Hedgehog (Shh) expression. We investigated whether acid-secretory mechanisms regulate Shh gene expression through intracellular calcium (Ca2(+)(i))-dependent protein kinase C (PKC) or cyclic adenosine monophosphate (cAMP)-dependent protein kinase A (PKA) activation.

Methods: We blocked Hedgehog signaling by transgenically overexpressing a secreted form of the Hedgehog interacting protein-1, a natural inhibitor of hedgehog ligands, which induced hypochlorhydria. Gadolinium, ethylene glycol-bis(β-aminoethyl ether)-N,N,N',N'-tetraacetic acid (EGTA) + 1,2-bis(2-aminophenoxy)ethane-N,N,N',N'-tetraacetic acid (BAPTA), PKC-overexpressing adenoviruses, and PKC inhibitors were used to modulate Ca(2+)(i)-release, PKC activity, and Shh gene expression in primary gastric cell, organ, and AGS cell line cultures. PKA hyperactivity was induced in the H(+)/K(+)-β-cholera-toxin-overexpressing mice.

Results: Mice that expressed secreted hedgehog-interacting protein-1 had lower levels of gastric acid (hypochlorhydria), reduced production of somatostatin, and increased gastrin gene expression. Hypochlorhydria in these mice repressed Shh gene expression, similar to the levels obtained with omeprazole treatment of wild-type mice. However, Shh expression also was repressed in the hyperchlorhydric H(+)/K(+)-β-cholera-toxin model with increased cAMP, suggesting that the regulation of Shh was not solely acid-dependent, but pertained to specific acid-stimulatory signaling pathways. Based on previous reports that Ca(2+)(i) release also stimulates acid secretion in parietal cells, we showed that gadolinium-, thapsigargin-, and carbachol-mediated release of Ca(2+)(i) induced Shh expression. Ca(2+)-chelation with BAPTA + EGTA reduced Shh expression. Overexpression of PKC-α, -β, and -δ (but not PKC-ϵ) induced an Shh gene expression. In addition, phorbol esters induced a Shh-regulated reporter gene.

Conclusions: Secretagogues that stimulate gastric acid secretion induce Shh gene expression through increased Ca(2+)(i)-release and PKC activation. Shh might be the ligand transducing changes in gastric acidity to the regulation of G-cell secretion of gastrin.
Castellone MD, Laukkanen MO, Teramoto H, Bellelli R, Alì G, Fontanini G, Santoro M, Gutkind JS - "Cross talk between the bombesin neuropeptide receptor and Sonic hedgehog pathways in small cell lung carcinoma" Oncogene 34(13):1679-87 (2015). doi: 10.1038/onc.2014.104
https://pubmed.ncbi.nlm.nih.gov/24747971/
Small cell lung carcinoma (SCLC) often features the upregulation of the Sonic hedgehog (Shh) pathway leading to activation of Gli transcription factors. SCLC cells secrete bombesin (BBS)-like neuropeptides that act as autocrine growth factors. Here, we show that SCLC tumor samples feature co-expression of Shh and BBS-cognate receptor (gastrin-releasing peptide receptor (GRPR)). We also demonstrate that BBS activates Gli in SCLC cells, which is crucial for BBS-mediated SCLC proliferation, because cyclopamine, an inhibitor of the Shh pathway, hampered the BBS-mediated effects. BBS binding to GRPR stimulated Gli through its downstream Gαq and Gα₁₂/₁₃ GTPases, and consistently, other Gαq and Gα₁₃ coupled receptors (such as muscarinic receptor, m1, and thrombin receptor, PAR-1) and constitutively active GαqQL and Gα₁₂/₁₃QL mutants stimulated Gli. By using cells null for Gαq and Gα₁₂/₁₃, we demonstrate that these G proteins are strictly necessary for Gli activation by BBS. Moreover, by using constitutively active Rho small G-protein (Rho QL) as well as its inhibitor, C3 toxin, we show that Rho mediates G-protein-coupled receptor (GPCR)-, Gαq- and Gα₁₂/₁₃-dependent Gli stimulation. At the molecular level, BBS caused a significant increase in Shh gene transcription and protein secretion that was dependent on BBS-induced GPCR/Gαq-₁₂/₁₃/Rho mediated activation of nuclear factor κB (NFκB), which can stimulate a NF-κB response element in the Shh gene promoter. Our data identify a novel molecular network acting in SCLC linking autocrine BBS and Shh circuitries and suggest Shh inhibitors as novel therapeutic strategies against this aggressive cancer type.
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Re: Shh and fluoride | More Fluorosis Studies

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Zhao L, Yu Y, Zhu Z, et al, - "Expressions of protein and mRNA relevant to hedgehog signaling pathway in liver of fluorosis rats" Chinese Journal of Public Health 31(9): 1162-1166 (2015) doi: 10.11847/zgggws2015-31-09-16

Zhao L, Yu Y, Deng C - "Expression of sonic hedgehog signaling pathway and its inhibition by cyclopamine in rat liver with chronic fluorosis" Chinese Journal of Pathology 43(12):814-9 (2014)
https://pubmed.ncbi.nlm.nih.gov/25623978/
Objective: To investigate the expression of sonic hedgehog (Shh) signaling pathway in liver fluorosis and to explore related mechanism.

Methods: To establish animal model, 48 normal SD rats (aged 4-5 weeks) were randomly divided into 4 groups (12 each): control group, fluoriosis group, blocking group and blocking control group. After 6 months, the blocking group and blocking control group were injected intraperitoneally once every 2 days for 3 times with 10 mg/kg cyclopamine or dimethysulfoxide, respectively. Rats were sacrificed at the end of the experiment and the fluoride content in urine and liver function was determined. The expression of Shh and Gli1 protein and mRNA in hepatocytes was detected by immunohistochemistry and real-time fluorescence quantitative PCR, respectively.

Results: The fluoride contents in the urine and the incidence of dental fluorosis increased in the fluoride and blocking control groups as compared with those in the control group, but decreased in the blocking group compared with those of the fluoride and blocking control group. Compared with the control group, the titers of aspartate transaminase (AST) and alanine transaminase (ALT) significantly increased, while the activity of total protein and albumin decreased in the fluoride and blocking control groups. Compared with the fluoride and blocking control groups, the activity of the ALT slightly declined and the AST, total protein and albumin slightly increased in the blocking group. Histologically, the cells were disorganized and swollen with cytoplasmic clearing (balloon cells), compared with the control group. The expression of Shh and Gli1 significantly increased in all but the control group. Compared with the fluoride and blocking control groups, the expression of Shh and Gli1 declined in the blocking group.

Conclusions: The overexpression and cyclopamine inhibition of the Shh signaling pathway are closely related to the content of fluoride in the liver. The Shh signaling pathway plays an important role in the pathogenesis of liver injury caused by fluorosis, suggesting a preventive and therapeutic target of the disease.
Zhao L, Yu Y, Deng C - "Protein and mRNA expression of Shh, Smo and Gli1 and inhibition by cyclopamine in hepatocytes of rats with chronic fluorosis" Toxicol Lett 225(2):318-24 (2014). doi: 10.1016/j.toxlet.2013.12.022
Abstract

In order to investigate the Sonic hedgehog (Shh) signaling pathway and the effect of cyclopamine in rat hepatocytes with chronic fluorosis, 48 Wistar rats were randomly divided into 4 groups. The control group was provided with tap water in which the fluorine concentration was <1mg/L, while the remaining three groups were provided with water containing sodium fluoride (NaF) at a concentration of 50mg/L. After 6 months, the blocking and blocking control groups were injected intraperitoneally once every 2 days for 6 days with 10mg/kg cyclopamine or dimethyl sulfoxide, respectively. The urinary and skeletal fluoride contents were determined by the ion selective electrode method. Levels of aspartate transaminase (AST), alanine transaminase (ALT), total protein (TP) and albumin (Alb) in the serum were determined by using autobiochemical machine. Histological changes in liver tissue were evaluated with Hematoxylin & Eeosin (H&E) staining using light microscopy. The protein and mRNA expression of Shh, Smo and Gli1 in hepatocytes of experimental animals was determined by immunohistochemistry (IHC), Western blotting (Wb) and Real-time quantitative PCR (RT-qPCR). Fluoride content of the urine and bone was increased in the fluorosis and blocking groups compared to those in the control group (P<0.05), while fluoride content in the blocking group was decreased compared to the fluorosis and blocking control groups (P<0.05). The expression of Shh, Smo and Gli1 at the mRNA and protein levels was significantly increased in hepatocytes from the fluorosis and blocking control groups compared with the control group, and expression in the blocking group was lower than that of the fluorosis and blocking control groups. The difference between any two groups was considered to be statistically significant (P<0.05). Taken together, our study indicates that the expression of Shh, Smo and Gli1 at the protein and mRNA level in hepatocytes of rats with chronic fluorosis can be increased by fluoride and may be inhibited by cyclopamine and that the Shh signaling pathway plays an important role in the liver pathogenesis caused by fluorosis.
Zhu Zhijian, Yu Yanni, Tao Xin, Deng Chaonan - "Role of Hh signaling pathway in fluoride-induced primary chondrocyte damage in rats" Chinese Journal of Public Health 5:574-578 (2015) PFPC Library
Objective: To investigate the roles of sonic hedgehog (Shh), smoothened (Smo), and bone morphogenetic protein-2 (BMP-2) in fluoride-induced primary chondrocyte damage in rats in vitro.

Methods: The primary chondrocytes were obtained from one-week-old healthy Sprague-Dawley rats with a mechanical-enzyme digestion method and identified with immunohistochemical cells. They were then divided into a control group and 5, 10, 20, and 40 mg/L sodium fluoride (NaF) exposure groups. After 48 hours of treatment, the viability of the cells was determined with the methyl thiazolyl tetrazolium test (MTT); the expressions of protein and mRNA of Smo, Shh, and BMP-2 were detected with Western blot and reverse transcription-polymerase chain reaction (RT-PCR), and apoptosis was detected with flow cytometry.

Results: Compared with the control group, the vitality of the cells exposed to NaF of 5 and 10 mg/L significantly increased (113.33 ± 11.74% and 127.25 ± 10.24%, P < 0.05) but decreased significantly for the cells exposed to NaF of 40 mg/L (73.91 ± 9.94%, P < 0.05). The protein and mRNA expressions of Shh, Smo, and BMP-2 increased along with the increment of fluorine concentration. The apoptosis rate of the cells with 40 mg/L NaF exposure was 11.13 ± 1.20%, significantly higher than that of the control group (P < 0.05).

Conclusion: Fluoride can activate the hedgehog (Hh) signaling pathway, and both the Hh signaling pathway and apoptosis may play roles in the pathogenesis of cartilage damage in fluorosis.
Zhu ZJ, Yu YN, Chen R - "Role of Hedgehog signaling pathway on cartilage tissue damage in chronic fluorosis rats" Chin J Public Health. 34(2):241-245 (2018) doi:10.11847/zgggws1115085shu.PFPC Library
Objective:
To investigate the role of the Hedgehog (Hh) signaling pathway in cartilage tissue damage in rats with chronic fluorosis.

Methods:
Thirty-six healthy Sprague-Dawley (SD) rats were randomly assigned to three groups (6 males and 6 females in each group): a control group (supplied with drinking water containing sodium fluoride [NaF] < 1 mg/L) and two fluorosis groups (supplied with drinking water containing NaF at concentrations of 5 mg/L and 50 mg/L, respectively). After six months of treatment, fluoride content in urine and bone was measured using a fluoride-ion selective electrode method. Histological changes in cartilage tissues were observed under a light microscope following hematoxylin and eosin (HE) staining. Protein components of the Hh signaling pathway, including Sonic Hedgehog (Shh), Smoothened (Smo), and Bone Morphogenetic Protein-2 (BMP-2), as well as apoptosis-regulating proteins B-cell lymphoma/leukemia-2 (Bcl-2) and Bcl-2-associated X protein (Bax), were detected using immunohistochemistry staining and Western blot analysis.

Results:
The fluoride content in urine (3.66 ± 0.43 mg/L and 8.05 ± 0.60 mg/L) and bone (402.38 ± 33.77 mg/kg and 935.12 ± 49.60 mg/kg) of rats in the low- and high-dose fluoride groups were significantly higher than those in the control group (P < 0.05 for all). Histological examination revealed thinning of the metaphyseal cartilage in the stifles, a decreased number of chondrocytes, and features consistent with sclerotic skeletal fluorosis in the fluoride-treated groups. Compared to the control group, the low- and high-dose fluoride groups showed significantly increased protein expression of Shh (0.86 ± 0.09 and 1.11 ± 0.15), Smo (0.92 ± 0.11 and 1.17 ± 0.14), BMP-2 (1.02 ± 0.14 and 1.13 ± 0.12), and Bax (0.91 ± 0.14 and 0.92 ± 0.11), with a concomitant decrease in Bcl-2 expression (0.78 ± 0.03 and 0.57 ± 0.09) (P < 0.05 for all).

Conclusion:
The activation of the Hedgehog signaling pathway and excessive expression of its downstream target genes may play a key role in the pathogenesis of chondrocyte damage in chronic fluorosis in rats.
Zhang Jiejing - "Effects of Hh signaling pathway on cartilage damage in rats with fluorosis" Chinese Journal of Control of Endemic Diseases1:25-27 (2016) PFPC Library
Objective: To investigate the effect of Hedgehog (Hh) signaling pathway on cartilage damage in rats with fluorosis.

Methods: Sixty healthy Wistar rats were selected and divided into the control group (tap water), low fluorine group (10 mg/L sodium fluoride solution), and high fluorine group (50 mg/L sodium fluoride solution) based on the random number table method. Rats' cartilage cell activity and apoptosis rate were recorded under different strengths of fluoride poison. Chondrocytes Alto speed hedgehog protein (Shh) and Indian hedgehog (IHH), a transmembrane protein (SMO), transmembrane protein receptor (PTCH1), nuclear transcription factor protein Gli1, Gli2, and Gli3 mRNA and protein expression levels of the three groups were compared.

Results: The activity of chondrocytes in the control group, low fluoride group, and high fluoride group were (100 ± 0)%, (116.48 ± 10.27)%, and (76.25 ± 11.38)%, respectively. The apoptosis rate was (4.15 ± 0.78)%, (3.02 ± 0.71)%, and (9.58 ± 1.14)%, respectively. The cartilage expression of Shh, Ihh, Smo, Gli1, Gli2 mRNA, and protein expression of Shh, Ihh, Smo, Ptch1, Gli1, Gli2 in the control, low fluorosis, and high fluorosis group increased in turn, but Gli3 mRNA was gradually decreased (P < 0.05). Smo, Ptch1, Gli1, Gli2, Gli3, and Hh were involved in the activity of cartilage injury in rats.
Deng Chaonan, Zhang Ying, Xu Lin, Zhao Lina, Linghuyan, Yu Yanni - "Expressions of Ihh, Shh and Smo mRNA and protein in rats' bone exposed to different doses of fluoride and the significance" Chinese Journal of Endemic Diseases" Issue 09 (2020)
https://www.airitilibrary.com/Publicati ... z202009003
Objective:
To investigate the changes in the expression of Hedgehog-related factors (Ihh, Shh, and Smo) in the bone of rats with chronic fluorosis and to explore their significance in bone formation.

Methods:
Thirty-six healthy Sprague-Dawley (SD) rats (body weight 100-120 g) were randomly assigned to three groups (n=12 per group, 6 males and 6 females) using a random digits table. The control group was given tap water (NaF < 1 mg/L), while the experimental groups received sodium fluoride (NaF) in their drinking water at concentrations of 5 mg/L (low-dose fluoride group) and 50 mg/L (high-dose fluoride group) to establish a chronic fluorosis model. After six months, 24-hour urine samples were collected, and the femoral metaphysis was harvested. Urine fluoride and bone fluoride concentrations were measured using a fluoride ion-selective electrode method. Bone tissues were stained with hematoxylin-eosin (HE) and observed under a light microscope. Serum bone alkaline phosphatase (BALP) was measured using an enzyme-linked immunosorbent assay (ELISA). The mRNA and protein expression levels of Ihh, Shh, and Smo in bone tissue were analyzed by real-time PCR and immunohistochemistry (IHC).

Results:
Urine fluoride, bone fluoride, and serum BALP levels increased progressively in the control, low-dose, and high-dose fluoride groups. The following significant differences were observed (P < 0.05):

Urine fluoride: (1.37 ± 0.44), (5.96 ± 0.56), (7.60 ± 0.61) mg/L.
Bone fluoride: (306.04 ± 12.58), (652.91 ± 51.83), (1,094.11 ± 126.34) mg/kg.
Serum BALP: (27.78 ± 4.09), (46.59 ± 5.75), (57.45 ± 3.99) U/L.
Bone sclerosis was observed in the low- and high-dose fluoride groups under light microscopy. The mRNA expression of Ihh, Shh, and Smo in the high-dose fluoride group (1.39 ± 0.36, 0.56 ± 0.23, 0.40 ± 0.15, respectively) was significantly higher than in the control and low-dose fluoride groups (Ihh: 0.73 ± 0.19, 0.92 ± 0.34; Shh: 0.19 ± 0.04, 0.36 ± 0.16; Smo: 0.14 ± 0.04, 0.24 ± 0.13; P < 0.05). The Shh mRNA expression in the low-dose fluoride group was also significantly higher than that of the control group (P < 0.05).

At the protein level, the expression of Ihh and Smo in the high-dose fluoride group (138.89 ± 3.72, 149.29 ± 7.63, respectively) was significantly higher than in the control (127.39 ± 2.69, 134.81 ± 3.53) and low-dose fluoride groups (129.64 ± 12.62, 139.07 ± 9.30; P < 0.05). Protein levels of Ihh and Smo were also higher in the low-dose fluoride group compared to the control group (P < 0.05). Similarly, Shh protein expression in the high-dose fluoride group (141.26 ± 7.49) was significantly higher than in the control group (130.96 ± 11.10, P < 0.05).

Conclusion:

Chronic fluorosis induces changes in the expression of Hedgehog signaling pathway-related factors (Ihh, Shh, and Smo) in bone tissue. These changes suggest that fluoride activates the Hedgehog signaling pathway, which in turn affects bone formation. This may provide new insights into the molecular mechanisms underlying fluoride-induced bone alterations.
Bcl-2 is a downstream target gene for Shh. The following study by Yang et al. found that high amounts of fluoride downregulated Bcl-2 in ameloblast-like LS8 cells. It is further noteworthy that both retinoic acid and dexamethasone were used to induce maturation of mouse ameloblast-like LS8 cells, as this strongly implicates T3 (triiodothyronine) in the process.

Yang T, Zhang Y, Li Y, Hao Y, Zhou M, Dong N, Duan X - "High amounts of fluoride induce apoptosis/cell death in matured ameloblast-like LS8 cells by downregulating Bcl-2" Arch Oral Biol 58(9):1165-73 (2013). doi: 10.1016/j.archoralbio.2013.03.016
https://www.sciencedirect.com/science/a ... 6913001106
Abstract
Objective: Excessive fluoride intake during enamel formation may result in enamel fluorosis and apoptosis is regarded to be involved in the process by an unclear mechanism. We hypothesize that excessive fluoride might cause apoptosis in the ameloblasts and fluoride-induced apoptosis varies with the maturation stages of ameloblasts.

Methods: We set up an in vitro differentiation model of ameloblasts by using retinoic acid (RA) and dexamethasone (DEX) to induce the maturation of mouse ameloblast-like LS8 cells.

Results: The mRNA and protein levels of two enamel matrix proteins and two enamel proteinases were downregulated and upregulated, respectively, in the RA/DEX induced cells, indicating RA/DEX induced cells possessed the characteristics of matured ameloblasts. The strengthened endocytosis function and decreased intracellular pH value inside RA/DEX treated ameloblasts confirmed the maturation inducing effect of RA/DEX on ameloblasts. Excessive fluoride inhibited cell proliferation of ameloblasts within 72h. High amounts of fluoride also induced more apoptosis/dead cells and reduced the expression of Bcl-2, but to a different degree in the non-induced cells and RA/DEX induced cells.

Conclusions: We inferred that high doses of fluoride may easily target the transitional/early maturation ameloblasts and cause apoptosis or cell death. Bcl-2 might be involved in this process.
Wang Y, Zhang X, Zhao Z, Xu H - "Preliminary Analysis of MicroRNAs Expression Profiling in MC3T3-E1 Cells Exposed to Fluoride" Biol Trace Elem Res 176(2):367-373 (2017). doi: 10.1007/s12011-016-0833-x.
https://link.springer.com/article/10.10 ... 016-0833-x
"The Wnt, insulin, TGF-beta, hedgehog, VEGF, and notch pathways in osteoblasts were those mainly affected by fluoride treatment."
Abstract

Overexposure to fluoride from environmental sources can cause serious public health problems. Disrupted osteoblast function and impaired bone formation were found to be associated with excessive fluoride exposure. A massive analysis of microRNAs (miRNAs) was used to figure out the possible pathways in which fluoride affects osteoblast function. MC3T3-E1 cells were treated with 8 mg/L of fluorine for 7 days. Total RNA of cells was extracted, and their integrity and purity were tested. RNA samples were analyzed by using miRNA array, including miRNA labeling, hybridization, scanning, and expression data analysis to compare the profiling of miRNA expression between control and fluoride-treated group. Transcriptome analysis console and enrichment analysis calculated by miRSystem were used to predict target genes and collect miRNAs pathway maps. Forty-five upregulated and 31 downregulated miRNAs expression were found in the fluoride-treated group, and most of the verified miRNAs were mature. The KEGG pathway enrichment analysis searched out 36 pathways that scored more than 0.1. These pathways mainly included intracellular signaling, cytokines, metabolism, and cytoskeleton-related pathways. Among them, the Wnt, insulin, TGF-beta, hedgehog, VEGF, and notch pathways in osteoblasts were those mainly affected by fluoride treatment. These results have shown a number of higher level systemic pathways activated by overexposure of fluoride in osteoblastic cells and verified that fluoride affected the molecular crosstalk in the osteoblasts.
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Re: Shh and fluoride | More on G proteins

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Pusapati GV, Kong JH, Patel BB, Gouti M, Sagner A, Sircar R, Luchetti G, Ingham PW, Briscoe J, Rohatgi R - "G protein-coupled receptors control the sensitivity of cells to the morphogen Sonic Hedgehog" Sci Signal 11(516):eaao5749 (2016). doi: 10.1126/scisignal.aao5749
https://pubmed.ncbi.nlm.nih.gov/29438014/
Abstract

The morphogen Sonic Hedgehog (SHH) patterns tissues during development by directing cell fates in a concentration-dependent manner. The SHH signal is transmitted across the membrane of target cells by the heptahelical transmembrane protein Smoothened (SMO), which activates the GLI family of transcription factors through a mechanism that is undefined in vertebrates. Using CRISPR-edited null alleles and small-molecule inhibitors, we systematically analyzed the epistatic interactions between SMO and three proteins implicated in SMO signaling: the heterotrimeric G protein subunit GαS, the G protein-coupled receptor kinase 2 (GRK2), and the GαS-coupled receptor GPR161. Our experiments uncovered a signaling mechanism that modifies the sensitivity of target cells to SHH and consequently changes the shape of the SHH dose-response curve. In both fibroblasts and spinal neural progenitors, the loss of GPR161, previously implicated as an inhibitor of basal SHH signaling, increased the sensitivity of target cells across the entire spectrum of SHH concentrations. Even in cells lacking GPR161, GRK2 was required for SHH signaling, and Gαs, which promotes the activation of protein Kinase A (PKA), antagonized SHH signaling. We propose that the sensitivity of target cells to Hedgehog morphogens, and the consequent effects on gene expression and differentiation outcomes, can be controlled by signals from G protein-coupled receptors that converge on Gαs and PKA.
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Re: Shh and fluoride | MAPK and DIO3

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Aw DK, Sinha RA, Tan HC, Loh LM, Salvatore D, Yen PM - "Studies of molecular mechanisms associated with increased deiodinase 3 expression in a case of consumptive hypothyroidism" J Clin Endocrinol Metab 99(11):3965-71 (2014). doi: 10.1210/jc.2013-3408
https://academic.oup.com/jcem/article/9 ... 65/2836372
Consumptive hypothyroidism (CH) is a rare form of hypothyroidism due to increased catabolic activity of type 3 iodothyronine deiodinase (DIO3) that can occur in large tumors. Patients with CH typically present with markedly increased requirements for exogenous thyroid hormone and resolution after removal of the source of ectopic DIO3. DIO3 is encoded by DIO3, an imprinted gene expressed on the paternal allele that is located in a DIO3/delta-like 1 homolog (DLK1) gene locus regulated by a common control region, intergenic differentially methylated region (IGDMR). Because DIO3 is an imprinted gene, loss of imprinting at the IGDMR is thought to play a role in its increased expression; however, the molecular mechanism for DIO3 in CH currently is not known.

Objective:
The aim of the study was to determine the molecular mechanism for CH in an adult patient.

Setting:
The study was conducted in the Department of Endocrinology of a tertiary care center in Singapore.

Patient:
We report the case of an adult Asian female patient with a large intrathoracic fibrous tumor and severe hypothyroidism that resolved after tumor resection.

Results:
The patient's tumor expressed increased levels of DIO3 and DLK1 mRNA and protein levels. Methylation-specific PCR of the IGDMR showed similar hypomethylation in placenta, thyroid, leukocytes, and tumor. Western blotting showed activation of sonic hedgehog (SHH) and MAPK signaling pathways that can increase DIO3 and DLK1 expression.

Conclusions:
Loss of imprinting did not account for overexpression of DIO3 in the patient's tumor. Instead SHH and MAPK/ERK pathway activation was associated with systemic thyroid hormone catabolism and growth of the tumor. These findings raise the possibility that other tumors that have increased SHH and MAPK/ERK signaling also may have intratumor or systemic effects on thyroid hormone function.
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Re: Shh and fluoride | Glioma & Other cancers | DIO3

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Note: Gli1, Gli2, and Gli3 regulate the transcription of SHH target genes.

Luongo C, Ambrosio R, Salzano S, Dlugosz AA, Missero C, Dentice M - "The sonic hedgehog-induced type 3 deiodinase facilitates tumorigenesis of basal cell carcinoma by reducing Gli2 inactivation" Endocrinology 155(6):2077-88 (2014). doi: 10.1210/en.2013-2108
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5393316/
Thyroid hormone (TH) is an important regulator of growth, development, and metabolism. Most of the active TH T3 is generated by peripheral TH metabolism mediated by the iodothyronine deiodinases. Type 3 deiodinase (D3) inactivates T3 via specific deiodination reactions. It is an oncofetal protein frequently expressed in neoplastic tissues and is a direct target of the sonic hedgehog (Shh) pathway in basal cell carcinomas (BCCs). However, the molecular mechanisms triggered by T3 in BCC are still mostly unrevealed. Here, we demonstrate that D3 action is critical in the proliferation and survival of BCC cells. D3 depletion or T3 treatment induce apoptosis of BCC cells and attenuate Shh signaling. This is achieved through a direct impairment of Gli2 protein stability by T3. T3 induces protein kinase A, which in turn destabilizes Gli2 protein via its C-terminal degron. Finally, in a mouse model of BCC, T3-topical treatment significantly reduces tumor growth. These results demonstrate the existence of a previously unrecognized cross talk between TH and Gli2 oncogene, providing functional and mechanistic evidence of the involvement of TH metabolism in Shh-induced cancer. TH-mediated Gli2 inactivation would be beneficial for therapeutically purposes, because the inhibition of Shh-Gli2 signaling is an attractive target for several anticancer drugs, currently in clinical trials.
SEE: viewtopic.php?f=97&t=5078

Romitti M, Wajner SM, Ceolin L, Ferreira CV, Ribeiro RV, Rohenkohl HC, Weber Sde S, Lopez PL, Fuziwara CS, Kimura ET, Maia AL - "MAPK and SHH pathways modulate type 3 deiodinase expression in papillary thyroid carcinoma" Endocr Relat Cancer. 23(3):135-46 (2016). doi: 10.1530/ERC-15-0162.
Abstract

Type 3 deiodinase (DIO3, D3) is reactivated in human neoplasias. Increased D3 levels in papillary thyroid carcinoma (PTC) have been associated with tumor size and metastatic disease. The objective of this study is to investigate the signaling pathways involved in DIO3 upregulation in PTC. Experiments were performed in human PTC cell lines (K1 and TPC-1 cells) or tumor samples. DIO3 mRNA and activity were evaluated by real-time PCR and ion-exchange column chromatography respectively. Western blot analysis was used to determine the levels of D3 protein. DIO3 gene silencing was performed via siRNA transfection. DIO3 mRNA levels and activity were readily detected in K1 (BRAF(V6) (0) (0E)) and, at lower levels, in TPC-1 (RET/PTC1) cells (P<0.007 and P=0.02 respectively). Similarly, DIO3 mRNA levels were higher in PTC samples harboring the BRAF(V600E) mutation as compared with those with RET/PTC1 rearrangement or negative for these mutations (P<0.001). Specific inhibition of BRAF oncogene (PLX4032, 3 μM), MEK (U0126, 10-20 μM) or p38 (SB203580, 10-20 μM) signaling was associated with decreases in DIO3 expression in K1 and TPC-1 cells. Additionally, the blockage of the sonic hedgehog (SHH) pathway by cyclopamine (10 μM) resulted in markedly decreases in DIO3 mRNA levels. Interestingly, siRNA-mediated DIO3 silencing induced decreases on cyclin D1 expression and partial G1 phase cell cycle arrest, thereby downregulating cell proliferation. In conclusion, sustained activation of the MAPK and SHH pathways modulate the levels of DIO3 expression in PTC. Importantly, DIO3 silencing was associated with decreases in cell proliferation, thus suggesting a D3 role in tumor growth and aggressiveness.
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Sonic Hedgehog (Shh) and Gli1: more

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Deng CN, Zhang Y, Xu L, Zhao LN, Linghu Y, Yu YN - "Change and relationship between Gli1 and β-catenin on rats' bone formation with chronic fluorosis" Zhonghua Bing Li Xue Za Zhi 49(2):168-173 (2020) Chinese. doi: 10.3760/cma.j.issn.0529-5807.2020.02.012
https://pubmed.ncbi.nlm.nih.gov/32074731/
Abstract in English

Objective: To investigate the change and association of glioma-associated oncogene homolog 1 (Gli1) and β-catenin on bone formation in rats with chronic fluorosis which were inhibited by cyclopamine (Cycl). Methods: Forty-eight Sprague-Dawley rats were evenly divided to four groups, including control, F, F+Cycl and F+DMSO groups. The control group were fed with tap water (NaF<1 ppm). The F, F+Cycl and F+DMSO groups were exposed to NaF (50 ppm) in drinking water as the chronic fluorosis model. Then the rats in F+Cycl or F+DMSO groups were injected by Cycl or DMSO after 6 months, respectively. Urine fluoride concentration was detected using fluorine ion selective electrode. The enzyme-linked immunosorbent assay (ELISA) was used to detect bone alkaline phosphatase (BALP). Bone tissues were stained with hematoxylin-eosin. The mRNA and protein expression of Gli1 and β-catenin in bone tissue were detected using real-time PCR, immunohistochemistry and Western blot. Results: Compared with the controls, the urine fluoride concentration and the width and volume of bone trabeculae were increased in the F, F+Cycl and F+DMSO groups, but no statistical difference among the 3 fluorosis groups. The concentration of BALP was increased in the F group and decreased in F+Cycl group (P<0.05). The expression of Gli1 and β-catenin mRNA and protein was higher in the F and F+Cycl groups than controls, but lower in the F+Cycl group than in the F group. There was positive correlation between the expression of Gli1 and β-catenin (r=0.476, P<0.05). The expression of Gli1 and β-catenin was also associated with BALP concentration and volume of bone trabeculae, respectively (r(1)=0.457, r(2)=0.466, r(3)=0.581, r(4)=0.554, respectively, P<0.05 for all). Conclusions: The expression of Gli1 can be inhibited by Cycl. It may be involved in the bone formation of rats with chronic fluorosis. It may also affect the expression of β-catenin, which is an osteogenesis factor.
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Sonic Hedgehog (Shh) and Autism

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Al-Ayadhi LY - "Relationship between Sonic hedgehog protein, brain-derived neurotrophic factor and oxidative stress in autism spectrum disorders" Neurochemical Research 37(2):394-400 (2012)
https://doi.org/10.1007/s11064-011-0624-x
Case-control serum study reporting higher SHH in autistic children (mild and severe) versus controls, reduced BDNF in mild ASD, and links to oxidative-stress measures.

Bashir S, Halepoto DM, Al-Ayadhi L - "Serum level of desert hedgehog protein in autism spectrum disorder: preliminary results" Medical Principles and Practice 23(1):14-17 (2014)
https://doi.org/10.1159/000354295
Case-control serum study reporting lower desert hedgehog (Dhh) levels in autism versus controls (ELISA), with no significant association between Dhh and CARS severity score.

Bashir S, Zeina R, Muhammad D, Al-Ayadhi L - "Role of hedgehog protein family members in autistic children" Neurology, Psychiatry and Brain Research 20(3):63-67 (2014)
https://doi.org/10.1016/j.npbr.2014.06.002
The data indicated that autistic children had higher serum levels of Shh (P = 0.001), Ihh (P = 0.001) and lower level of Dhh (P = 0.003) than those of normal controls. Moreover, serum levels of Shh had significant positive correlations with Dhh (P < 0.002).
Conclusions: This study suggests that higher levels of Shh, Ihh and lower Dhh levels may play a role in the pathophysiology of autism.


Ghanizadeh A - "Malondialdehyde, Bcl-2, superoxide dismutase and glutathione peroxidase may mediate the association of sonic hedgehog protein and oxidative stress in autism" Neurochemical Research 37(4):899-901 (2012)
https://doi.org/10.1007/s11064-011-0667-z
Short review/comment proposing that SHH may relate to oxidative stress in autism via markers including malondialdehyde, Bcl-2, SOD, and glutathione peroxidase.

Gozal E, Jagadapillai R, Cai J, Barnes GN – “Potential crosstalk between sonic hedgehog-WNT signaling and neurovascular molecules: Implications for blood-brain barrier integrity in autism spectrum disorder” J Neurochem 159(1):15-28 (2021)
https://doi.org/10.1111/jnc.15460
This paper explores how dysregulation of the sonic hedgehog (Shh) and WNT signaling pathways may interact with neurovascular factors to alter blood-brain barrier (BBB) function in autism spectrum disorder. The authors propose that impaired Shh-WNT crosstalk compromises endothelial and astrocytic interactions essential for BBB maintenance, contributing to neuroinflammation and aberrant neuronal connectivity characteristic of ASD.
Abstract

Autism Spectrum Disorder (ASD) is a neurodevelopmental disease originating from combined genetic and environmental factors. Post-mortem human studies and some animal ASD models have shown brain neuroinflammation, oxidative stress, and changes in blood-brain barrier (BBB) integrity. However, the signaling pathways leading to these inflammatory findings and vascular alterations are currently unclear. The BBB plays a critical role in controlling brain homeostasis and immune response. Its dysfunction can result from developmental genetic abnormalities or neuroinflammatory processes. In this review, we explore the role of the Sonic Hedgehog/Wingless-related integration site (Shh/Wnt) pathways in neurodevelopment, neuroinflammation, and BBB development. The balance between Wnt-β-catenin and Shh pathways controls angiogenesis, barriergenesis, neurodevelopment, central nervous system (CNS) morphogenesis, and neuronal guidance. These interactions are critical to maintain BBB function in the mature CNS to prevent the influx of pathogens and inflammatory cells. Genetic mutations of key components of these pathways have been identified in ASD patients and animal models, which correlate with the severity of ASD symptoms. Disruption of the Shh/Wnt crosstalk may therefore compromise BBB development and function. In turn, impaired Shh signaling and glial activation may cause neuroinflammation that could disrupt the BBB. Elucidating how ASD-related mutations of Shh/Wnt signaling could cause BBB leaks and neuroinflammation will contribute to our understanding of the role of their interactions in ASD pathophysiology. These observations may provide novel targeted therapeutic strategies to prevent or alleviate ASD symptoms while preserving normal developmental processes.
Halepoto DM, Bashir S, Zeina R, Al-Ayadhi LY - "Correlation Between Hedgehog (Hh) Protein Family and Brain-Derived Neurotrophic Factor (BDNF) in Autism Spectrum Disorder (ASD)" Journal of the College of Physicians and Surgeons Pakistan 25(12):882-885 (2015)
Observational comparative study reporting higher serum SHH and IHH in autistic subjects than controls and reporting correlations among SHH, IHH, BDNF, and severity strata, without significant relationships to CARS, age, or gender.

Rahi S, Gupta R, Sharma A, Mehan S - "Smo-Shh signaling activator purmorphamine ameliorates neurobehavioral, molecular, and morphological alterations in an intracerebroventricular propionic acid-induced experimental model of autism" Human and Experimental Toxicology 40(11):1880-1898 (2021)
https://doi.org/10.1177/09603271211013456
Animal-model intervention study testing the SMO-SHH agonist purmorphamine in an intracerebroventricular propionic-acid autism model, reporting improvements across neurobehavioral and molecular endpoints (as described in the abstract).

Rahi S, Mehan S – “Understanding Abnormal SMO-SHH Signaling in Autism Spectrum Disorder: Potential Drug Target and Therapeutic Goals” Cell Mol Neurobiol 42(4):931-953 (2022)
https://doi.org/10.1007/s10571-020-01010-1
This review examines dysregulation of the sonic hedgehog (SHH) pathway, focusing on Smoothened (SMO) receptor abnormalities in autism spectrum disorder. It highlights how altered SHH-SMO-Gli signaling affects neurogenesis, synaptogenesis, and oxidative stress pathways. The authors identify SMO as a therapeutic target, suggesting that pharmacological modulation of SHH signaling could restore neuronal differentiation and improve behavioral outcomes in ASD.
Abstract

Autism is a multifactorial neurodevelopmental condition; it demonstrates some main characteristics, such as impaired social relationships and increased repetitive behavior. The initiation of autism spectrum disorder is mostly triggered during brain development by the deregulation of signaling pathways. Sonic hedgehog (SHH) signaling is one such mechanism that influences neurogenesis and neural processes during the development of the central nervous system. SMO-SHH signaling is also an important part of a broad variety of neurological processes, including neuronal cell differentiation, proliferation, and survival. Dysregulation of SMO-SHH signaling leads to many physiological changes that lead to neurological disorders such as ASD and contribute to cognitive decline. The aberrant downregulation of SMO-SHH signals contributes to the proteolytic cleavage of GLI (glioma-associated homolog) into GLI3 (repressor), which increases oxidative stress, neuronal excitotoxicity, neuroinflammation, and apoptosis by suppressing target gene expression. We outlined in this review that SMO-SHH deregulation plays a crucial role in the pathogenesis of autism and addresses the current status of SMO-SHH pathway modulators. Additionally, a greater understanding of the SHH signaling pathway is an effort to improve successful treatment for autism and other neurological disorders.
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Sonic Hedgehog (Shh) and Thyroid Hormone (T3)

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Desouza LA, Sathanoori M, Kapoor R, Rajadhyaksha N, Gonzalez LE, Kottmann AH, Tole S, Vaidya VA - "Thyroid hormone regulates the expression of the sonic hedgehog signaling pathway in the embryonic and adult mammalian brain" Endocrinology 152(5):1989-2000 (2011)
https://doi.org/10.1210/en.2010-1396
Maternal hypo- and hyperthyroidism bidirectionally altered Shh mRNA in embryonic forebrain; in adults, T3 increased Shh mRNA in multiple regions, and acute T3 increased Shh mRNA in vivo and in cortical neuron cultures, with promoter histone acetylation changes consistent with TH-responsive regulation.
Abstract:

Thyroid hormone is important for development and plasticity in the immature and adult mammalian brain. Several thyroid hormone-responsive genes are regulated during specific developmental time windows, with relatively few influenced across the lifespan. We provide novel evidence that thyroid hormone regulates expression of the key developmental morphogen sonic hedgehog (Shh), and its coreceptors patched (Ptc) and smoothened (Smo), in the early embryonic and adult forebrain. Maternal hypo- and hyperthyroidism bidirectionally influenced Shh mRNA in embryonic forebrain signaling centers at stages before fetal thyroid hormone synthesis. Further, Smo and Ptc expression were significantly decreased in the forebrain of embryos derived from hypothyroid dams. Adult-onset thyroid hormone perturbations also regulated expression of the Shh pathway bidirectionally, with a significant induction of Shh, Ptc, and Smo after hyperthyroidism and a decline in Smo expression in the hypothyroid brain. Short-term T3 administration resulted in a significant induction of cortical Shh mRNA expression and also enhanced reporter gene expression in Shh+/LacZ mice. Further, acute T3 treatment of cortical neuronal cultures resulted in a rapid and significant increase in Shh mRNA, suggesting direct effects. Chromatin immunoprecipitation assays performed on adult neocortex indicated enhanced histone acetylation at the Shh promoter after acute T3 administration, providing further support that Shh is a thyroid hormone-responsive gene. Our results indicate that maternal and adult-onset perturbations of euthyroid status cause robust and region-specific changes in the Shh pathway in the embryonic and adult forebrain, implicating Shh as a possible mechanistic link for specific neurodevelopmental effects of thyroid hormone.
Hasebe T, Kajita M, Fu L, Shi YB, Ishizuya-Oka A - "Thyroid hormone-induced sonic hedgehog signal up-regulates its own pathway in a paracrine manner in the Xenopus laevis intestine during metamorphosis" Developmental Dynamics 241(2):403-414 (2012)
https://doi.org/10.1002/dvdy.23723
During Xenopus intestinal metamorphosis, Shh is described as directly induced by thyroid hormone at the transcription level as an early remodeling event; the study also reports TH induction of pathway components and identifies Gli2 as a direct TH response gene under protein synthesis inhibition.
Abstract

Background: During Xenopus laevis metamorphosis, Sonic hedgehog (Shh) is directly induced by thyroid hormone (TH) at the transcription level as one of the earliest events in intestinal remodeling. However, the regulation of other components of this signaling pathway remains to be analyzed. Here, we analyzed the spatiotemporal expression of Patched (Ptc)-1, Smoothened (Smo), Gli1, Gli2, and Gli3 during natural and TH-induced intestinal remodeling. Results: We show that all of the genes examined are transiently up-regulated in the mesenchymal tissues during intestinal metamorphosis. Conclusions: Interestingly, in the presence of protein synthesis inhibitors, Gli2 but not the others was induced by TH, suggesting that Gli2 is a direct TH response gene, while the others are likely indirect ones. Furthermore, we demonstrate by the organ culture experiment that overexpression of Shh enhances the expression of Ptc-1, Smo, and Glis even in the absence of TH, indicating that Shh regulates its own pathway components during intestinal remodeling.
NOTE: TH can switch Shh on, and Shh can then amplify its own pathway.

Ishizuya-Oka A, Ueda S, Inokuchi T, Amano T, Damjanovski S, Stolow M, Shi YB - "Thyroid hormone-induced expression of sonic hedgehog correlates with adult epithelial development during remodeling of the Xenopus stomach and intestine" Differentiation 69(1):27-37 (2001)
https://doi.org/10.1046/j.1432-0436.2001.690103.x
Shh is reported as an early thyroid hormone response gene in Xenopus intestine; the abstract states Shh expression is induced by thyroid hormone in an organ-autonomous manner and correlates with adult epithelial primordia proliferation and differentiation during metamorphic remodeling.
Abstract

Sonic hedgehog (Shh) was isolated from the Xenopus laevis intestine as an early thyroid hormone (TH) response gene. To investigate possible roles of TH-upregulated expression of Shh during metamorphosis, we raised a polyclonal antibody against Xenopus Shh and immunohistochemically examined the relationship between Shh expression and the larval-to-adult intestinal remodeling at the cellular level. Our results indicate that the epithelial-specific expression of Shh in the intestine spatiotemporally correlates well with active proliferation and/or initial differentiation of the secondary (adult) epithelial primordia that originate from stem cells, but not with apoptosis of the primary (larval) epithelium. Given the similar transformations of the stomach during metamorphosis, we also analyzed Shh expression in this organ and found similar correlations in the stomach, although the position of the adult epithelial primordia and their final differentiation in the stomach are different from those in the intestine. Furthermore, we show here that Shh expression is organ-autonomously induced by TH and its correlation with the adult epithelial development is reproduced in vitro in both the intestine and the stomach. More importantly, addition of recombinant Shh protein to the culture medium results in developmental anomalies of both organs. However, differentiation of the adult epithelium is more severely inhibited by exogenous Shh in the intestine than in the stomach. These results suggest that TH-upregulated expression of Shh plays important roles in the postembryonic gastrointestinal remodeling, but its roles are at least partially different between the intestine and the stomach.
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