sox9b is a key regulator of pancreaticobiliary ductal system development

PLoS Genetics

Volumn 8, Issue 6, 2012, Pages

  Delous, Marion ^a   Yin, Chunyue ^a   Shin, Donghun ^a,e   Ninov, Nikolay ^a   Debrito Carten, Juliana ^b,c   Pan, Luyuan ^d   Ma, Taylur P ^d   Farber, Steven A ^b,c   Moens, Cecilia B ^d   Stainier, Didier Y R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c GEOPHYSICAL LABORATORY   (United States)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^e UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NOTCH RECEPTOR; TRANSCRIPTION FACTOR SOX9; TRANSCRIPTION FACTOR SOX9B; UNCLASSIFIED DRUG; SOX9B PROTEIN, ZEBRAFISH; ZEBRAFISH PROTEIN;

ALLELE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL FATE; CONTROLLED STUDY; CYST; DIGESTIVE SYSTEM; EMBRYO; HOMOZYGOSITY; INTRAHEPATIC BILE DUCT; INTRAHEPATIC CHOLESTASIS; JUVENILE ANIMAL; LARVAL STAGE; LIVER CELL; LIVER FIBROSIS; MORPHOGENESIS; NONHUMAN; NONSENSE MUTATION; ORGANOGENESIS; PANCREAS DISEASE; PANCREATICOBILIARY DUCTAL SYSTEM; PHENOTYPE; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; ZEBRA FISH; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIVER; METABOLISM; PANCREAS; PRENATAL DEVELOPMENT; STOP CODON;

DANIO RERIO; MAMMALIA; MUS;

ANIMALS; BILE DUCTS, INTRAHEPATIC; CODON, NONSENSE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LIVER; MORPHOGENESIS; PANCREAS; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; SOX9 TRANSCRIPTION FACTOR; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84864029149     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002754     Document Type: Article

References (54)

1. Raynaud P, Carpentier R, Antoniou A, Lemaigre FP, (2011) Biliary differentiation and bile duct morphogenesis in development and disease. Int J Biochem Cell Biol 43: 245-256.
2. Spence JR, Lange AW, Lin SC, Kaestner KH, Lowy AM, et al. (2009) Sox17 regulates organ lineage segregation of ventral foregut progenitor cells. Dev Cell 17: 62-74.
3. Zong Y, Stanger BZ, (2011) Molecular mechanisms of bile duct development. Int J Biochem Cell Biol 43: 257-264.
4. Geisler F, Nagl F, Mazur PK, Lee M, Zimber-Strobl U, et al. (2008) Liver-specific inactivation of Notch2, but not Notch1, compromises intrahepatic bile duct development in mice. Hepatology 48: 607-616.
5. Kodama Y, Hijikata M, Kageyama R, Shimotohno K, Chiba T, (2004) The role of notch signaling in the development of intrahepatic bile ducts. Gastroenterology 127: 1775-1786.
6. Lozier J, McCright B, Gridley T, (2008) Notch signaling regulates bile duct morphogenesis in mice. PLoS ONE 3: e1851 doi:10.1371/journal.pone.0001851.
7. McCright B, Lozier J, Gridley T, (2002) A mouse model of Alagille syndrome: Notch2 as a genetic modifier of Jag1 haploinsufficiency. Development 129: 1075-1082.
8. Tchorz JS, Kinter J, Muller M, Tornillo L, Heim MH, et al. (2009) Notch2 signaling promotes biliary epithelial cell fate specification and tubulogenesis during bile duct development in mice. Hepatology 50: 871-879.
9. Zong Y, Panikkar A, Xu J, Antoniou A, Raynaud P, et al. (2009) Notch signaling controls liver development by regulating biliary differentiation. Development 136: 1727-1739.
10. Clotman F, Lannoy VJ, Reber M, Cereghini S, Cassiman D, et al. (2002) The onecut transcription factor HNF6 is required for normal development of the biliary tract. Development 129: 1819-1828.
11. Coffinier C, Gresh L, Fiette L, Tronche F, Schutz G, et al. (2002) Bile system morphogenesis defects and liver dysfunction upon targeted deletion of HNF1beta. Development 129: 1829-1838.
12. Hunter MP, Wilson CM, Jiang X, Cong R, Vasavada H, et al. (2007) The homeobox gene Hhex is essential for proper hepatoblast differentiation and bile duct morphogenesis. Dev Biol 308: 355-367.
13. Maestro MA, Boj SF, Luco RF, Pierreux CE, Cabedo J, et al. (2003) Hnf6 and Tcf2 (MODY5) are linked in a gene network operating in a precursor cell domain of the embryonic pancreas. Human Molecular Genetics 12: 3307-3314.
14. Pierreux CE, Poll AV, Kemp CR, Clotman F, Maestro MA, et al. (2006) The transcription factor hepatocyte nuclear factor-6 controls the development of pancreatic ducts in the mouse. Gastroenterology 130: 532-541.
15. Dong PD, Munson CA, Norton W, Crosnier C, Pan X, et al. (2007) Fgf10 regulates hepatopancreatic ductal system patterning and differentiation. Nat Genet 39: 397-402.
16. Chung WS, Shin CH, Stainier DY, (2008) Bmp2 signaling regulates the hepatic versus pancreatic fate decision. Dev Cell 15: 738-748.
17. Shin D, Lee Y, Poss KD, Stainier DY, (2011) Restriction of hepatic competence by Fgf signaling. Development 138: 1339-1348.
18. Field HA, Dong PD, Beis D, Stainier DY, (2003) Formation of the digestive system in zebrafish. II. Pancreas morphogenesis. Dev Biol 261: 197-208.
19. Ober EA, Verkade H, Field HA, Stainier DY, (2006) Mesodermal Wnt2b signalling positively regulates liver specification. Nature 442: 688-691.
20. Lorent K, Yeo SY, Oda T, Chandrasekharappa S, Chitnis A, et al. (2004) Inhibition of Jagged-mediated Notch signaling disrupts zebrafish biliary development and generates multi-organ defects compatible with an Alagille syndrome phenocopy. Development 131: 5753-5766.
21. Lorent K, Moore JC, Siekmann AF, Lawson N, Pack M, (2010) Reiterative use of the notch signal during zebrafish intrahepatic biliary development. Dev Dyn 239: 855-864.
22. Pauls S, Zecchin E, Tiso N, Bortolussi M, Argenton F, (2007) Function and regulation of zebrafish nkx2.2a during development of pancreatic islet and ducts. Dev Biol 304: 875-890.
23. Antoniou A, Raynaud P, Cordi S, Zong Y, Tronche F, et al. (2009) Intrahepatic bile ducts develop according to a new mode of tubulogenesis regulated by the transcription factor SOX9. Gastroenterology 136: 2325-2333.
24. Furuyama K, Kawaguchi Y, Akiyama H, Horiguchi M, Kodama S, et al. (2011) Continuous cell supply from a Sox9-expressing progenitor zone in adult liver, exocrine pancreas and intestine. Nat Genet 43: 34-41.
25. Seymour PA, Freude KK, Tran MN, Mayes EE, Jensen J, et al. (2007) SOX9 is required for maintenance of the pancreatic progenitor cell pool. Proc Natl Acad Sci U S A 104: 1865-1870.
26. Wagner T, Wirth J, Meyer J, Zabel B, Held M, et al. (1994) Autosomal sex reversal and campomelic dysplasia are caused by mutations in and around the SRY-related gene SOX9. Cell 79: 1111-1120.
27. Foster JW, Dominguez-Steglich MA, Guioli S, Kwok C, Weller PA, et al. (1994) Campomelic dysplasia and autosomal sex reversal caused by mutations in an SRY-related gene. Nature 372: 525-530.
28. Piper K, Ball SG, Keeling JW, Mansoor S, Wilson DI, et al. (2002) Novel SOX9 expression during human pancreas development correlates to abnormalities in Campomelic dysplasia. Mech Dev 116: 223-226.
29. Bi W, Huang W, Whitworth DJ, Deng JM, Zhang Z, et al. (2001) Haploinsufficiency of Sox9 results in defective cartilage primordia and premature skeletal mineralization. Proc Natl Acad Sci U S A 98: 6698-6703.
30. Yan YL, Willoughby J, Liu D, Crump JG, Wilson C, et al. (2005) A pair of Sox: distinct and overlapping functions of zebrafish sox9 co-orthologs in craniofacial and pectoral fin development. Development 132: 1069-1083.
31. Yan YL, Miller CT, Nissen RM, Singer A, Liu D, et al. (2002) A zebrafish sox9 gene required for cartilage morphogenesis. Development 129: 5065-5079.
32. Crosnier C, Vargesson N, Gschmeissner S, Ariza-McNaughton L, Morrison A, et al. (2005) Delta-Notch signalling controls commitment to a secretory fate in the zebrafish intestine. Development 132: 1093-1104.
33. Shin D, Weidinger G, Moon RT, Stainier DY, Intrinsic and extrinsic modifiers of the regulative capacity of the developing liver. Mech Dev 128: 525-535.
34. Ninov N, Borius M, Stainier DY, (2012) Different levels of Notch signaling regulate quiescence, renewal and differentiation in pancreatic endocrine progenitors. Development 139: 1557-1567.
35. Parsons MJ, Pisharath H, Yusuff S, Moore JC, Siekmann AF, et al. (2009) Notch-responsive cells initiate the secondary transition in larval zebrafish pancreas. Mech Dev 126: 898-912.
36. Obholzer N, Wolfson S, Trapani JG, Mo W, Nechiporuk A, et al. (2008) Vesicular glutamate transporter 3 is required for synaptic transmission in zebrafish hair cells. J Neurosci 28: 2110-2118.
37. Cheung ID, Bagnat M, Ma TP, Datta A, Evason K, et al. (2011) Regulation of intrahepatic biliary duct morphogenesis by Claudin 15-like b. Dev Biol.
38. Gerloff T, Stieger B, Hagenbuch B, Madon J, Landmann L, et al. (1998) The sister of P-glycoprotein represents the canalicular bile salt export pump of mammalian liver. J Biol Chem 273: 10046-10050.
39. Sakaguchi TF, Sadler KC, Crosnier C, Stainier DY, (2008) Endothelial signals modulate hepatocyte apicobasal polarization in zebrafish. Curr Biol 18: 1565-1571.
40. Carten JD, Bradford MK, Farber S, (2011) Visualizing digestive organ morphology and function using differential fatty acid metabolism in live zebrafish. Dev Biol.
41. Hofmann JJ, Zovein AC, Koh H, Radtke F, Weinmaster G, et al. (2010) Jagged1 in the portal vein mesenchyme regulates intrahepatic bile duct development: insights into Alagille syndrome. Development 137: 4061-4072.
42. Geling A, Steiner H, Willem M, Bally-Cuif L, Haass C, (2002) A gamma-secretase inhibitor blocks Notch signaling in vivo and causes a severe neurogenic phenotype in zebrafish. EMBO Rep 3: 688-694.
43. Scheer N, Groth A, Hans S, Campos-Ortega JA, (2001) An instructive function for Notch in promoting gliogenesis in the zebrafish retina. Development 128: 1099-1107.
44. Li X, Zhao X, Fang Y, Jiang X, Duong T, et al. (1998) Generation of destabilized green fluorescent protein as a transcription reporter. J Biol Chem 273: 34970-34975.
45. Alexander J, Stainier DY, (1999) A molecular pathway leading to endoderm formation in zebrafish. Curr Biol 9: 1147-1157.
46. Hesselson D, Anderson RM, Beinat M, Stainier DY, (2009) Distinct populations of quiescent and proliferative pancreatic beta-cells identified by HOTcre mediated labeling. Proc Natl Acad Sci U S A 106: 14896-14901.
47. Carpentier R, Suner RE, van Hul N, Kopp JL, Beaudry JB, et al. Embryonic ductal plate cells give rise to cholangiocytes, periportal hepatocytes, and adult liver progenitor cells. Gastroenterology 141: 1432-1438 1438e 1431-1434.
48. Furuyama K, Kawaguchi Y, Akiyama H, Horiguchi M, Kodama S, et al. (2010) Continuous cell supply from a Sox9-expressing progenitor zone in adult liver, exocrine pancreas and intestine. Nat Genet 43: 34-41.
49. Galan-Gomez E, Sanchez EB, Arias-Castro S, Cardesa-Garcia JJ, (2007) Intrauterine growth retardation, duodenal and extrahepatic biliary atresia, hypoplastic pancreas and other intestinal anomalies: further evidence of the Martinez-Frias syndrome. Eur J Med Genet 50: 144-148.
50. Chappell L, Gorman S, Campbell F, Ellard S, Rice G, et al. (2008) A further example of a distinctive autosomal recessive syndrome comprising neonatal diabetes mellitus, intestinal atresias and gall bladder agenesis. Am J Med Genet A 146A: 1713-1717.
51. Kwok C, Weller PA, Guioli S, Foster JW, Mansour S, et al. (1995) Mutations in SOX9, the gene responsible for Campomelic dysplasia and autosomal sex reversal. Am J Hum Genet 57: 1028-1036.
52. Westerfield M, (2000) The Zebrafish Book: A Guide for the Laboratory Use of Zebrafish (Danio rerio).
53. Obholzer RJ, Nouraei SA, Ahmed J, Kadhim MR, Sandhu GS, (2008) An approach to the management of paroxysmal laryngospasm. J Laryngol Otol 122: 57-60.
54. Alexander J, Stainier DY, Yelon D, (1998) Screening mosaic F1 females for mutations affecting zebrafish heart induction and patterning. Dev Genet 22: 288-299.