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Palatogenez: Sekonder damak gelişiminde Sonic hedgehog (Shh) sinyalinin rolü

Yıl 2022, Cilt: 12 Sayı: 2, 367 - 374, 30.06.2022
https://doi.org/10.31832/smj.1061944

Öz

Palatogenez, malfonksiyonları yeni doğanda en sık görülen embriyonik gelişimsel anomalilerden biri olan konjenital yarık damağa yol açan, karmaşık ve kusursuz olarak dengelenmiş bir süreçtir. Çok sayıda sinyal yolakları ve transkripsiyon faktörleri palatal çıkıntıların gelişimi ile ilişkilidir. Bu makalenin amacı, sekonder damak gelişiminde kritik rol oynayan en önemli sinyal yolaklarından biri olan Sonic hedgehog (Shh) sinyal yolağı hakkında derleme yapmaktır. Bu çalışma, sekonder damak gelişimi sırasında oluşan karşılıklı epitelyal-mezenkimal etkileşimlerde Hedgehog sinyal yolağı üyelerinin ekspresyon modellerini ve Shh sinyalinin rolünü genel olarak değerlendirmektedir.

Kaynakça

  • 1- Bush JO, Jiang R. Palatogenesis: morphogenetic and molecular mechanisms of secondary palate development. Development. 2012; 139(2):231-243. doi: 10.1242/dev.067082.
  • 2- Gritli-Linde A. Molecular control of secondary palate development. Dev Biol. 2007; 301(2):309–326. doi: 10.1016/j.ydbio.2006.07.042.
  • 3- Lan Y, Xu J, Jiang R. Cellular and molecular mechanisms of palatogenesis. Curr Top Dev Biol. 2015; 115:59–84. doi: 10.1016/bs.ctdb.2015.07.002.
  • 4- McMahon AP, Ingham PW, Tabin CJ. Developmental roles and clinical significance of hedgehog signaling. Curr Top Dev Biol. 2003; 53:1–114. doi: 10.1016/s0070-2153(03)53002-2.
  • 5- Cobourne MT, Green JBA. Hedgehog Signalling in Development of the Secondary Palate. Front Oral Biol. 2012;16:52–59. doi: 10.1159/000337543.
  • 6- Briscoe J, Thérond PP. The mechanisms of hedgehog signaling and its roles in development and disease. Nat Rev Mol Cell Biol. 2013; 14(7):416–429. doi: 10.1038/nrm3598.
  • 7- Xavier MG, Seppala M, Barrell W, Birjandi AA, Geoghegan F, Cobourne M. Hedgehog receptor function during craniofacial development. Dev Biol. 2016; 415(2):198–215. doi: 10.1016/j.ydbio.2016.02.009.
  • 8- Allen BL, Tenzen T, McMahon AP. The Hedgehog- binding proteins Gas1 and Cdo cooperate to positively regulate Shh signaling during mouse development. Genes Dev. 2007; 21(10):1244–1257. doi: 10.1101/gad.1543607.
  • 9- Martinelli DC, Fan CM. Gas1 extends the range of Hedgehog action by facilitating its signaling. Genes Dev. 2007; 21(10):1231–1243. doi: 10.1101/gad.1546307.
  • 10- Seppala M, Depew MJ, Martinelli DC, Fan CM, Sharpe PT, Cobourne MT. Gas1 is a modifier for holoprosencephaly and genetically interacts with Sonic hedgehog. J Clin Invest. 2007; 117(6):1575–1584. doi: 10.1172/JCI32032.
  • 11- Tenzen T, Allen BL, Cole F, Kang JS, Krauss RS, McMahon AP. The cell surface membrane proteins Cdo and Boc are components and targets of the Hedgehog signaling pathway and feedback network in mice. Dev Cell. 2006; 10(5):647–656. doi: 10.1016/j.devcel.2006.04.004.
  • 12- Lee RT, Zhao Z, Ingham PW. Hedgehog signalling. Development. 2016;143(3):367–372. doi: 10.1242/dev.120154.
  • 13- Cobourne MT, Sharpe PT. Sonic hedgehog signaling and the developing tooth. Curr Top Dev Biol. 2005; 65:255–287. doi: 10.1016/S0070-2153(04)65010-1.
  • 14- Casali A, Struhl G. Reading the Hedgehog morphogen gradient by measuring the ratio of bound to unbound Patched protein. Nature. 2004; 431(7004):76–80. doi: 10.1038/nature02835.
  • 15- Chen Y, Struhl G. Dual roles for patched in sequestering and transducing Hedgehog. Cell. 1996; 87(3):553–563. doi: 10.1016/s0092-8674(00)81374-4.
  • 16- Dessaud E, Yang LL, Hill K, Cox B, Ulloa F, Ribeiro A, et al. Interpretation of the Sonic hedgehog morphogen gradient by a temporal adaptation mechanism. Nature. 2007; 450(7170):717–720. doi: 10.1038/nature06347.
  • 17- Rice R, Connor E, Rice DPC. Expression patterns of Hedgehog signalling pathway members during mouse palate development. Gene Expr Patterns. 2006; 6(2):206-212. doi: 10.1016/j.modgep.2005.06.005.
  • 18- Hu D, Helms JA. The role of sonic hedgehog in normal and abnormal craniofacial morphogenesis. Development. 1999; 126(21):4873-4884.
  • 19- Schachter KA , Krauss RS. Murine models of holoprosencephaly. Curr Top Dev Biol. 2008; 84:139-170. doi: 10.1016/S0070-2153(08)00603-0.
  • 20- Roessler E, Belloni E, Gaudenz K, Jay P, Berta P, Scherer SW, et al. Mutations in the human Sonic hedgehog gene cause holoprosencephaly. Nat Genet. 1996; 14(3): 357–360. doi: 10.1038/ng1196-357.
  • 21- Echelard Y, Epstein DJ, St-Jacques B, Shen L, Mohler J, McMahon JA, et al. Sonic Hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell. 1993; 75(7): 1417– 1430. doi: 10.1016/0092-8674(93)90627-3.
  • 22- Jiang J, Hui CC. Hedgehog signaling in development and cancer. Developmental cell. 2008; 15(6):801–812. doi: 10.1016/j.devcel.2008.11.010.
  • 23- Hanna A, Shevde LA. Hedgehog signaling: modulation of cancer properies and tumor mircroenvironment. Mol Cancer. 2016; 15:24. doi: 10.1186/s12943-016-0509-3.
  • 24- Jeong J, Mao J, Tenzen T, Kottmann AH, McMahon AP. Hedgehog signaling in the neural crest cells regulates the patterning and growth of facial primordia. Genes Dev. 2004; 18(8):937-951. doi: 10.1101/gad.1190304.
  • 25- Pantalacci S, Prochazka J, Martin A, Rothova M, Lambert A, Bernard L, et al. Patterning of palatal rugae through sequential addition reveals an anterior/ posterior boundary in palatal development. BMC Dev Biol. 2008; 8:116. doi: 10.1186/1471-213X-8-116.
  • 26- Welsh IC, O'Brien TP. Signaling integration in the rugae growth zone directs sequential SHH signaling center formation during the rostral outgrowth of the palate. Dev Biol. 2009; 336(1):53–67. doi: 10.1016/j.ydbio.2009.09.028.
  • 27- Economou AD, Ohazama A, Porntaveetus T, Sharpe PT, Kondo S, Basson MA, et al. Periodic stripe formation by a Turing mechanism operating at growth zones in the mammalian palate. Nat Genet. 2012; 44(3):348–351. doi: 10.1038/ng.1090.
  • 28- Baek JA, Lan Y, Liu H, Maltby KM, Mishina Y, Jiang R. Bmpr1a signaling plays critical roles in palatal shelf growth and palatal bone formation. Developmental biology. 2011; 350(5):520–531. doi: 10.1016/j.ydbio.2010.12.028.
  • 29- Zhou J, Gao Y, Lan Y, Jia S, Jiang R. Pax9 regulates a molecular network involving Bmp4, Fgf10, Shh signaling and the Osr2 transcription factor to control palate morphogenesis. Development. 2013; 140(23):4709–4718. doi: 10.1242/dev.099028.
  • 30- Rice R, Spencer-Dene B, Connor EC, Gritli-Linde A, McMahon AP, Dickson C, et al. Disruption of Fgf10/Fgfr2bcoordinated epithelial-mesenchymal interactions causes cleft palate. J Clin Invest. 2004; 113(12):1692-1700. doi: 10.1172/JCI20384.
  • 31- Lan Y, Jiang R. Sonic hedgehog signaling regulates reciprocal epithelial-mesenchymal interactions controlling palatal outgrowth. Development. 2009; 136(8):1387-1396. doi: 10.1242/dev.028167.
  • 32- Zhang Z, Song Y, Zhao X, Zhang X, Fermin C, Chen Y. Rescue of cleft palate in Msx1-deficient mice by transgenic Bmp4 reveals a network of BMP and Shh signaling in the regulation of mammalian palatogenesis. Development. 2002; 129(17):4135-4146.
  • 33- Han J, Mayo J, Xu X, Li J, Bringas P, Maas RL, et al. Indirect modulation of Shh signaling by Dlx5 affects the oral-nasal patterning of palate and rescues cleft palate in Msx1-null mice. Development. 2009; 136(24):4225-4233. doi: 10.1242/dev.036723.
  • 34- Francavilla C, Rigbolt KT, Emdal KB, Carraro G, Vernet E, Bekker-Jensen DB, et al. Functional proteomics defines the molecular switch underlying FGF receptor trafficking and cellular outputs. Molecular cell. 2013; 51(6):707–722. doi: 10.1016/j.molcel.2013.08.002.
  • 35- Xu J, Liu H, Lan Y, Aronow BJ, Kalinichenko VV, Jiang R. A Shh-Foxf-Fgf18-Shh Molecular Circuit Regulating Palate Development. PLoS Genet. 2016; 12(1): e1005769. doi: 10.1371/journal.pgen.1005769.
  • 36- Olsen SK, Li JY, Bromleigh C, Eliseenkova AV, Ibrahimi OA, Lao Z, et al. Structural basis by which alternative splicing modulates the organizer activity of FGF8 in the brain. Genes Dev. 2006; 20(2):185–198. doi: 10.1101/gad.1365406.
  • 37- Brown A, Adam LE, Blundell TL. The crystal structure of fibroblast growth factor 18 (FGF18). Protein cell. 2014; 5(5):343–347. doi: 10.1007/s13238-014-0033-4.
  • 38- Mahlappu M, Ormestad M, Enerbäck S, Carlsson P. The forkhead transcription factor Foxf1 is required for differentiation of extraembryonic and lateral plate mesoderm. Development. 2001; 128(12):155-166.
  • 39- Wang T, Tamakoshi T, Uezato T, Shu F, Kanzaki-Kato N, Fu Y, et al. Forkhead transcription factor Foxf2 (LUN)-deficient mice exhibit abnormal development of secondary palate. Dev Biol. 2003; 259(1):83-94. doi: 10.1016/s0012-1606(03)00176-3.
  • 40- Lan Y, Ovitt CE, Cho ES, Maltby KM, Wang Q, Jiang R. Odd-skipped related 2 (Osr2) encodes a key intrinsic regulator of secondary palate growth and morphogenesis. Development. 2004; 131(13):3207-3216. doi: 10.1242/dev.01175.
  • 41- Gao Y, Lan Y, Ovitt CE, Jiang R. Functional equivalence of the zinc finger transcription factors Osr1 and Osr2 in mouse development. Dev Biol. 2009; 328(2):200-209. doi: 10.1016/j.ydbio.2009.01.008.
  • 42- Sasaki Y, O’Kane S, Dixon J, Dixon MJ, Ferguson MW. Temporal and spatial expression of Pax9 and Sonic hedgehog during development of normal mouse palates and cleft palates in TGF-βeta3 null embryos. Arch Oral Biol. 2007; 52(3):260–267. doi: 10.1016/j.archoralbio.2006.09.012.
  • 43- Lin C, Fisher AV, Yin Y, Maruyama T, Veith GM, Dhandha M, et al. The inductive role of Wnt- β-catenin signaling in the formation of oral apparatus. Dev Biol. 2011; 356(1):40–50. doi: 10.1016/j.ydbio.2011.05.002.
  • 44- Yang T, Jia Z, Bryant-Pike W, Chandrasekhar A, Murray JC, Fritzsch B, et al. Analysis of PRICKLE1 in human cleft palate and mouse development demonstrates rare and common variants involved in human malformations. Mol Genet Genomic Med. 2014; 2(2):138–151. doi: 10.1002/mgg3.53.
  • 45- El Shahawy M, Reibring CG, Hallberg K, Neben CL, Marangoni P, Harfe BD, et al .Sonic hedgehog signaling is required for Cyp26 expression during embryonic development. Int J Mol Sci. 2019; 20(9):2275. doi: 10.3390/ijms20092275.
  • 46- Duester G. Retinoic acid synthesis and signaling during early organogenesis. Cell. 2008; 134(6):921–931. doi: 10.1016/j.cell.2008.09.002.
  • 47- Rhinn M, Dollé P. Retinoic acid signalling during development. Development. 2012; 139(5):843–858. doi: 10.1242/dev.065938.
  • 48- Ikemi N, Kawata M, Yasuda M. All-trans-retinoic acid-induced variant patterns of palatal rugae in CRJ: Sd rat fetuses and their potential as indicators for teratogenesis. Reprod Toxicol. 1995; 9(4):369–377. doi: 10.1016/0890-6238(95)00024-5.

Palatogenesis: The role of Sonic hedgehog (Shh) signaling in the secondary palate development

Yıl 2022, Cilt: 12 Sayı: 2, 367 - 374, 30.06.2022
https://doi.org/10.31832/smj.1061944

Öz

Palatogenesis is a complicated and precisely balanced process in which malfunctions induce congenital cleft palate, one of the most common embryonic developmental anomaly seen in newborns. Multiple signaling pathways and transcription factors have been implicated in palatal shelves development. The purpose of this article is to review one of the most important signaling pathways that plays a critical role in secondary palate development, namely Sonic hedgehog (Shh) signaling pathway. It includes an overview of the expression patterns of members of the Hedgehog signaling pathway and the role of Shh signaling in the reciprocal epithelial-mesenchymal interactions during secondary palate development.

Kaynakça

  • 1- Bush JO, Jiang R. Palatogenesis: morphogenetic and molecular mechanisms of secondary palate development. Development. 2012; 139(2):231-243. doi: 10.1242/dev.067082.
  • 2- Gritli-Linde A. Molecular control of secondary palate development. Dev Biol. 2007; 301(2):309–326. doi: 10.1016/j.ydbio.2006.07.042.
  • 3- Lan Y, Xu J, Jiang R. Cellular and molecular mechanisms of palatogenesis. Curr Top Dev Biol. 2015; 115:59–84. doi: 10.1016/bs.ctdb.2015.07.002.
  • 4- McMahon AP, Ingham PW, Tabin CJ. Developmental roles and clinical significance of hedgehog signaling. Curr Top Dev Biol. 2003; 53:1–114. doi: 10.1016/s0070-2153(03)53002-2.
  • 5- Cobourne MT, Green JBA. Hedgehog Signalling in Development of the Secondary Palate. Front Oral Biol. 2012;16:52–59. doi: 10.1159/000337543.
  • 6- Briscoe J, Thérond PP. The mechanisms of hedgehog signaling and its roles in development and disease. Nat Rev Mol Cell Biol. 2013; 14(7):416–429. doi: 10.1038/nrm3598.
  • 7- Xavier MG, Seppala M, Barrell W, Birjandi AA, Geoghegan F, Cobourne M. Hedgehog receptor function during craniofacial development. Dev Biol. 2016; 415(2):198–215. doi: 10.1016/j.ydbio.2016.02.009.
  • 8- Allen BL, Tenzen T, McMahon AP. The Hedgehog- binding proteins Gas1 and Cdo cooperate to positively regulate Shh signaling during mouse development. Genes Dev. 2007; 21(10):1244–1257. doi: 10.1101/gad.1543607.
  • 9- Martinelli DC, Fan CM. Gas1 extends the range of Hedgehog action by facilitating its signaling. Genes Dev. 2007; 21(10):1231–1243. doi: 10.1101/gad.1546307.
  • 10- Seppala M, Depew MJ, Martinelli DC, Fan CM, Sharpe PT, Cobourne MT. Gas1 is a modifier for holoprosencephaly and genetically interacts with Sonic hedgehog. J Clin Invest. 2007; 117(6):1575–1584. doi: 10.1172/JCI32032.
  • 11- Tenzen T, Allen BL, Cole F, Kang JS, Krauss RS, McMahon AP. The cell surface membrane proteins Cdo and Boc are components and targets of the Hedgehog signaling pathway and feedback network in mice. Dev Cell. 2006; 10(5):647–656. doi: 10.1016/j.devcel.2006.04.004.
  • 12- Lee RT, Zhao Z, Ingham PW. Hedgehog signalling. Development. 2016;143(3):367–372. doi: 10.1242/dev.120154.
  • 13- Cobourne MT, Sharpe PT. Sonic hedgehog signaling and the developing tooth. Curr Top Dev Biol. 2005; 65:255–287. doi: 10.1016/S0070-2153(04)65010-1.
  • 14- Casali A, Struhl G. Reading the Hedgehog morphogen gradient by measuring the ratio of bound to unbound Patched protein. Nature. 2004; 431(7004):76–80. doi: 10.1038/nature02835.
  • 15- Chen Y, Struhl G. Dual roles for patched in sequestering and transducing Hedgehog. Cell. 1996; 87(3):553–563. doi: 10.1016/s0092-8674(00)81374-4.
  • 16- Dessaud E, Yang LL, Hill K, Cox B, Ulloa F, Ribeiro A, et al. Interpretation of the Sonic hedgehog morphogen gradient by a temporal adaptation mechanism. Nature. 2007; 450(7170):717–720. doi: 10.1038/nature06347.
  • 17- Rice R, Connor E, Rice DPC. Expression patterns of Hedgehog signalling pathway members during mouse palate development. Gene Expr Patterns. 2006; 6(2):206-212. doi: 10.1016/j.modgep.2005.06.005.
  • 18- Hu D, Helms JA. The role of sonic hedgehog in normal and abnormal craniofacial morphogenesis. Development. 1999; 126(21):4873-4884.
  • 19- Schachter KA , Krauss RS. Murine models of holoprosencephaly. Curr Top Dev Biol. 2008; 84:139-170. doi: 10.1016/S0070-2153(08)00603-0.
  • 20- Roessler E, Belloni E, Gaudenz K, Jay P, Berta P, Scherer SW, et al. Mutations in the human Sonic hedgehog gene cause holoprosencephaly. Nat Genet. 1996; 14(3): 357–360. doi: 10.1038/ng1196-357.
  • 21- Echelard Y, Epstein DJ, St-Jacques B, Shen L, Mohler J, McMahon JA, et al. Sonic Hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell. 1993; 75(7): 1417– 1430. doi: 10.1016/0092-8674(93)90627-3.
  • 22- Jiang J, Hui CC. Hedgehog signaling in development and cancer. Developmental cell. 2008; 15(6):801–812. doi: 10.1016/j.devcel.2008.11.010.
  • 23- Hanna A, Shevde LA. Hedgehog signaling: modulation of cancer properies and tumor mircroenvironment. Mol Cancer. 2016; 15:24. doi: 10.1186/s12943-016-0509-3.
  • 24- Jeong J, Mao J, Tenzen T, Kottmann AH, McMahon AP. Hedgehog signaling in the neural crest cells regulates the patterning and growth of facial primordia. Genes Dev. 2004; 18(8):937-951. doi: 10.1101/gad.1190304.
  • 25- Pantalacci S, Prochazka J, Martin A, Rothova M, Lambert A, Bernard L, et al. Patterning of palatal rugae through sequential addition reveals an anterior/ posterior boundary in palatal development. BMC Dev Biol. 2008; 8:116. doi: 10.1186/1471-213X-8-116.
  • 26- Welsh IC, O'Brien TP. Signaling integration in the rugae growth zone directs sequential SHH signaling center formation during the rostral outgrowth of the palate. Dev Biol. 2009; 336(1):53–67. doi: 10.1016/j.ydbio.2009.09.028.
  • 27- Economou AD, Ohazama A, Porntaveetus T, Sharpe PT, Kondo S, Basson MA, et al. Periodic stripe formation by a Turing mechanism operating at growth zones in the mammalian palate. Nat Genet. 2012; 44(3):348–351. doi: 10.1038/ng.1090.
  • 28- Baek JA, Lan Y, Liu H, Maltby KM, Mishina Y, Jiang R. Bmpr1a signaling plays critical roles in palatal shelf growth and palatal bone formation. Developmental biology. 2011; 350(5):520–531. doi: 10.1016/j.ydbio.2010.12.028.
  • 29- Zhou J, Gao Y, Lan Y, Jia S, Jiang R. Pax9 regulates a molecular network involving Bmp4, Fgf10, Shh signaling and the Osr2 transcription factor to control palate morphogenesis. Development. 2013; 140(23):4709–4718. doi: 10.1242/dev.099028.
  • 30- Rice R, Spencer-Dene B, Connor EC, Gritli-Linde A, McMahon AP, Dickson C, et al. Disruption of Fgf10/Fgfr2bcoordinated epithelial-mesenchymal interactions causes cleft palate. J Clin Invest. 2004; 113(12):1692-1700. doi: 10.1172/JCI20384.
  • 31- Lan Y, Jiang R. Sonic hedgehog signaling regulates reciprocal epithelial-mesenchymal interactions controlling palatal outgrowth. Development. 2009; 136(8):1387-1396. doi: 10.1242/dev.028167.
  • 32- Zhang Z, Song Y, Zhao X, Zhang X, Fermin C, Chen Y. Rescue of cleft palate in Msx1-deficient mice by transgenic Bmp4 reveals a network of BMP and Shh signaling in the regulation of mammalian palatogenesis. Development. 2002; 129(17):4135-4146.
  • 33- Han J, Mayo J, Xu X, Li J, Bringas P, Maas RL, et al. Indirect modulation of Shh signaling by Dlx5 affects the oral-nasal patterning of palate and rescues cleft palate in Msx1-null mice. Development. 2009; 136(24):4225-4233. doi: 10.1242/dev.036723.
  • 34- Francavilla C, Rigbolt KT, Emdal KB, Carraro G, Vernet E, Bekker-Jensen DB, et al. Functional proteomics defines the molecular switch underlying FGF receptor trafficking and cellular outputs. Molecular cell. 2013; 51(6):707–722. doi: 10.1016/j.molcel.2013.08.002.
  • 35- Xu J, Liu H, Lan Y, Aronow BJ, Kalinichenko VV, Jiang R. A Shh-Foxf-Fgf18-Shh Molecular Circuit Regulating Palate Development. PLoS Genet. 2016; 12(1): e1005769. doi: 10.1371/journal.pgen.1005769.
  • 36- Olsen SK, Li JY, Bromleigh C, Eliseenkova AV, Ibrahimi OA, Lao Z, et al. Structural basis by which alternative splicing modulates the organizer activity of FGF8 in the brain. Genes Dev. 2006; 20(2):185–198. doi: 10.1101/gad.1365406.
  • 37- Brown A, Adam LE, Blundell TL. The crystal structure of fibroblast growth factor 18 (FGF18). Protein cell. 2014; 5(5):343–347. doi: 10.1007/s13238-014-0033-4.
  • 38- Mahlappu M, Ormestad M, Enerbäck S, Carlsson P. The forkhead transcription factor Foxf1 is required for differentiation of extraembryonic and lateral plate mesoderm. Development. 2001; 128(12):155-166.
  • 39- Wang T, Tamakoshi T, Uezato T, Shu F, Kanzaki-Kato N, Fu Y, et al. Forkhead transcription factor Foxf2 (LUN)-deficient mice exhibit abnormal development of secondary palate. Dev Biol. 2003; 259(1):83-94. doi: 10.1016/s0012-1606(03)00176-3.
  • 40- Lan Y, Ovitt CE, Cho ES, Maltby KM, Wang Q, Jiang R. Odd-skipped related 2 (Osr2) encodes a key intrinsic regulator of secondary palate growth and morphogenesis. Development. 2004; 131(13):3207-3216. doi: 10.1242/dev.01175.
  • 41- Gao Y, Lan Y, Ovitt CE, Jiang R. Functional equivalence of the zinc finger transcription factors Osr1 and Osr2 in mouse development. Dev Biol. 2009; 328(2):200-209. doi: 10.1016/j.ydbio.2009.01.008.
  • 42- Sasaki Y, O’Kane S, Dixon J, Dixon MJ, Ferguson MW. Temporal and spatial expression of Pax9 and Sonic hedgehog during development of normal mouse palates and cleft palates in TGF-βeta3 null embryos. Arch Oral Biol. 2007; 52(3):260–267. doi: 10.1016/j.archoralbio.2006.09.012.
  • 43- Lin C, Fisher AV, Yin Y, Maruyama T, Veith GM, Dhandha M, et al. The inductive role of Wnt- β-catenin signaling in the formation of oral apparatus. Dev Biol. 2011; 356(1):40–50. doi: 10.1016/j.ydbio.2011.05.002.
  • 44- Yang T, Jia Z, Bryant-Pike W, Chandrasekhar A, Murray JC, Fritzsch B, et al. Analysis of PRICKLE1 in human cleft palate and mouse development demonstrates rare and common variants involved in human malformations. Mol Genet Genomic Med. 2014; 2(2):138–151. doi: 10.1002/mgg3.53.
  • 45- El Shahawy M, Reibring CG, Hallberg K, Neben CL, Marangoni P, Harfe BD, et al .Sonic hedgehog signaling is required for Cyp26 expression during embryonic development. Int J Mol Sci. 2019; 20(9):2275. doi: 10.3390/ijms20092275.
  • 46- Duester G. Retinoic acid synthesis and signaling during early organogenesis. Cell. 2008; 134(6):921–931. doi: 10.1016/j.cell.2008.09.002.
  • 47- Rhinn M, Dollé P. Retinoic acid signalling during development. Development. 2012; 139(5):843–858. doi: 10.1242/dev.065938.
  • 48- Ikemi N, Kawata M, Yasuda M. All-trans-retinoic acid-induced variant patterns of palatal rugae in CRJ: Sd rat fetuses and their potential as indicators for teratogenesis. Reprod Toxicol. 1995; 9(4):369–377. doi: 10.1016/0890-6238(95)00024-5.
Toplam 48 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Sağlık Kurumları Yönetimi
Bölüm Makaleler
Yazarlar

Reem Al-towaitee 0000-0001-6573-6869

Elvan Şahin 0000-0001-8585-9903

Yayımlanma Tarihi 30 Haziran 2022
Gönderilme Tarihi 23 Ocak 2022
Yayımlandığı Sayı Yıl 2022 Cilt: 12 Sayı: 2

Kaynak Göster

AMA Al-towaitee R, Şahin E. Palatogenesis: The role of Sonic hedgehog (Shh) signaling in the secondary palate development. Sakarya Tıp Dergisi. Haziran 2022;12(2):367-374. doi:10.31832/smj.1061944

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