Regulation of intrahepatic biliary duct morphogenesis by Claudin 15-like b

Developmental Biology

Volumn 361, Issue 1, 2012, Pages 68-78

  Cheung, Isla D ^a   Bagnat, Michel ^a,e   Ma, Taylur P ^b   Datta, Anirban ^a   Evason, Kimberley ^a,c   Moore, John C ^d   Lawson, Nathan D ^d   Mostov, Keith E ^a   Moens, Cecilia B ^b   Stainier, Didier Y R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Fred Hutchinson Cancer Research Center   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^e DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Biliary cells; Biliary duct morphogenesis; Biliary duct remodeling; Cholestasis; Claudin; Liver development; Tight junctions; Zebrafish

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BILE DUCT MALFORMATION; CELL POLARITY; CLAUDIN 15 LIKE B GENE; CONTROLLED STUDY; EPITHELIUM CELL; GENE; GENE EXPRESSION; INTRAHEPATIC BILE DUCT; LIVER CELL; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; TIGHT JUNCTION; ZEBRA FISH;

DANIO RERIO;

EID: 83055176400     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2011.10.004     Document Type: Article

References (59)

1. Alexander J., Stainier D.Y., Yelon D. Screening mosaic F1 females for mutations affecting zebrafish heart induction and patterning. Dev. Genet. 1998, 22:288-299.
2. Alrefai W.A., Gill R.K. Bile acid transporters: structure, function, regulation and pathophysiological implications. Pharm. Res. 2007, 24:1803-1823.
3. Antoniou A., Raynaud P., Cordi S., Zong Y., Tronche F., Stanger B.Z., Jacquemin P., Pierreux C.E., Clotman F., Lemaigre F.P. Intrahepatic bile ducts develop according to a new mode of tubulogenesis regulated by the transcription factor SOX9. Gastroenterology 2009, 136:2325-2333.
4. Baala L., Hadj-Rabia S., Hamel-Teillac D., Hadchouel M., Prost C., Leal S.M., Jacquemin E., Sefiani A., De Prost Y., Courtois G., Munnich A., Lyonnet S., Vabres P. Homozygosity mapping of a locus for a novel syndromic ichthyosis to chromosome 3q27-q28. J. Invest. Dermatol. 2002, 119:70-76.
5. Bagnat M., Cheung I.D., Mostov K.E., Stainier D.Y. Genetic control of single lumen formation in the zebrafish gut. Nat. Cell Biol. 2007, 9:954-960.
6. Battle M.A., Konopka G., Parviz F., Gaggl A.L., Yang C., Sladek F.M., Duncan S.A. Hepatocyte nuclear factor 4alpha orchestrates expression of cell adhesion proteins during the epithelial transformation of the developing liver. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:8419-8424.
7. Beis D., Bartman T., Jin S.W., Scott I.C., D'Amico L.A., Ober E.A., Verkade H., Frantsve J., Field H.A., Wehman A., Baier H., Tallafuss A., Bally-Cuif L., Chen J.N., Stainier D.Y., Jungblut B. Genetic and cellular analyses of zebrafish atrioventricular cushion and valve development. Development 2005, 132:4193-4204.
8. Bryant D.M., Datta A., Rodriguez-Fraticelli A.E., Peranen J., Martin-Belmonte F., Mostov K.E. A molecular network for de novo generation of the apical surface and lumen. Nat. Cell Biol. 2010, 12:1035-1045.
9. Carlton V.E., Harris B.Z., Puffenberger E.G., Batta A.K., Knisely A.S., Robinson D.L., Strauss K.A., Shneider B.L., Lim W.A., Salen G., Morton D.H., Bull L.N. Complex inheritance of familial hypercholanemia with associated mutations in TJP2 and BAAT. Nat. Genet. 2003, 34:91-96.
10. Carlton V.E., Pawlikowska L., Bull L.N. Molecular basis of intrahepatic cholestasis. Ann. Med. 2004, 36:606-617.
11. Clotman F., Jacquemin P., Plumb-Rudewiez N., Pierreux C.E., Van der Smissen P., Dietz H.C., Courtoy P.J., Rousseau G.G., Lemaigre F.P. Control of liver cell fate decision by a gradient of TGF beta signaling modulated by Onecut transcription factors. Genes Dev. 2005, 19:1849-1854.
12. Clotman F., Lannoy V.J., Reber M., Cereghini S., Cassiman D., Jacquemin P., Roskams T., Rousseau G.G., Lemaigre F.P. The onecut transcription factor HNF6 is required for normal development of the biliary tract. Development 2002, 129:1819-1828.
13. Coffinier C., Gresh L., Fiette L., Tronche F., Schutz G., Babinet C., Pontoglio M., Yaniv M., Barra J. Bile system morphogenesis defects and liver dysfunction upon targeted deletion of HNF1beta. Development 2002, 129:1829-1838.
14. Cui S., Capecci L.M., Matthews R.P. Disruption of planar cell polarity activity leads to developmental biliary defects. Dev. Biol. 2011, 351:229-241.
15. Cullinane A.R., Straatman-Iwanowska A., Zaucker A., Wakabayashi Y., Bruce C.K., Luo G., Rahman F., Gurakan F., Utine E., Ozkan T.B., Denecke J., Vukovic J., Di Rocco M., Mandel H., Cangul H., Matthews R.P., Thomas S.G., Rappoport J.Z., Arias I.M., Wolburg H., Knisely A.S., Kelly D.A., Muller F., Maher E.R., Gissen P. Mutations in VIPAR cause an arthrogryposis, renal dysfunction and cholestasis syndrome phenotype with defects in epithelial polarization. Nat. Genet. 2010, 42:303-312.
16. Cullinane A.R., Straatman-Iwanowska A., Zaucker A., Wakabayashi Y., Bruce C.K., Luo G., Rahman F., Gurakan F., Utine E., Ozkan T.B., Denecke J., Vukovic J., Di Rocco M., Mandel H., Cangul H., Matthews R.P., Thomas S.G., Rappoport J.Z., Arias I.M., Wolburg H., Knisely A.S., Kelly D.A., Muller F., Maher E.R., Gissen P. Mutations in VIPAR cause an arthrogryposis, renal dysfunction and cholestasis syndrome phenotype with defects in epithelial polarization. Nat. Genet. 2010, 42:303-312.
17. Curado S., Ober E.A., Walsh S., Cortes-Hernandez P., Verkade H., Koehler C.M., Stainier D.Y. The mitochondrial import gene tomm22 is specifically required for hepatocyte survival and provides a liver regeneration model. Dis. Model. Mech. 2010, 3:486-495.
18. Farber S.A., Pack M., Ho S.Y., Johnson I.D., Wagner D.S., Dosch R., Mullins M.C., Hendrickson H.S., Hendrickson E.K., Halpern M.E. Genetic analysis of digestive physiology using fluorescent phospholipid reporters. Science 2001, 292:1385-1388.
19. Gatmaitan Z.C., Arias I.M. ATP-dependent transport systems in the canalicular membrane of the hepatocyte. Physiol. Rev. 1995, 75:261-275.
20. Gerloff T., Stieger B., Hagenbuch B., Madon J., Landmann L., Roth J., Hofmann A.F., Meier P.J. The sister of P-glycoprotein represents the canalicular bile salt export pump of mammalian liver. J. Biol. Chem. 1998, 273:10046-10050.
21. Gunzel D., Stuiver M., Kausalya P.J., Haisch L., Krug S.M., Rosenthal R., Meij I.C., Hunziker W., Fromm M., Muller D. Claudin-10 exists in six alternatively spliced isoforms that exhibit distinct localization and function. J. Cell Sci. 2009, 122:1507-1517.
22. Haas P., Gilmour D. Chemokine signaling mediates self-organizing tissue migration in the zebrafish lateral line. Dev. Cell 2006, 10:673-680.
23. Hadj-Rabia S., Baala L., Vabres P., Hamel-Teillac D., Jacquemin E., Fabre M., Lyonnet S., De Prost Y., Munnich A., Hadchouel M., Smahi A. Claudin-1 gene mutations in neonatal sclerosing cholangitis associated with ichthyosis: a tight junction disease. Gastroenterology 2004, 127:1386-1390.
24. Her G.M., Chiang C.C., Chen W.Y., Wu J.L. In vivo studies of liver-type fatty acid binding protein (L-FABP) gene expression in liver of transgenic zebrafish (Danio rerio). FEBS Lett. 2003, 538:125-133.
25. Horne-Badovinac S., Lin D., Waldron S., Schwarz M., Mbamalu G., Pawson T., Jan Y., Stainier D.Y., Abdelilah-Seyfried S. Positional cloning of heart and soul reveals multiple roles for PKC lambda in zebrafish organogenesis. Curr. Biol. 2001, 11:1492-1502.
26. Ke Z., Kondrichin I., Gong Z., Korzh V. Combined activity of the two Gli2 genes of zebrafish play a major role in Hedgehog signaling during zebrafish neurodevelopment. Mol. Cell. Neurosci. 2008, 37:388-401.
27. Kubota K., Furuse M., Sasaki H., Sonoda N., Fujita K., Nagafuchi A., Tsukita S. Ca(2+)-independent cell-adhesion activity of claudins, a family of integral membrane proteins localized at tight junctions. Curr. Biol. 1999, 9:1035-1038.
28. Lamps L.W. Hepatic granulomas, with an emphasis on infectious causes. Adv. Anat. Pathol. 2008, 15:309-318.
29. Lee N.P., Luk J.M. Hepatic tight junctions: from viral entry to cancer metastasis. World J. Gastroenterol. 2010, 16:289-295.
30. Lemaigre F.P. Molecular mechanisms of biliary development. Prog. Mol. Biol. Transl. Sci. 2010, 97:103-126.
31. Loh Y.H., Christoffels A., Brenner S., Hunziker W., Venkatesh B. Extensive expansion of the claudin gene family in the teleost fish, Fugu rubripes. Genome Res. 2004, 14:1248-1257.
32. Lorent K., Moore J.C., Siekmann A.F., Lawson N., Pack M. Reiterative use of the notch signal during zebrafish intrahepatic biliary development. Dev. Dyn. 2010, 239:855-864.
33. Lorent K., Yeo S.Y., Oda T., Chandrasekharappa S., Chitnis A., Matthews R.P., Pack M. Inhibition of Jagged-mediated Notch signaling disrupts zebrafish biliary development and generates multi-organ defects compatible with an Alagille syndrome phenocopy. Development 2004, 131:5753-5766.
34. Matthews R.P., Lorent K., Pack M. Transcription factor onecut3 regulates intrahepatic biliary development in zebrafish. Dev. Dyn. 2008, 237:124-131.
35. Matthews R.P., Lorent K., Russo P., Pack M. The zebrafish onecut gene hnf-6 functions in an evolutionarily conserved genetic pathway that regulates vertebrate biliary development. Dev. Biol. 2004, 274:245-259.
36. Matthews R.P., Plumb-Rudewiez N., Lorent K., Gissen P., Johnson C.A., Lemaigre F., Pack M. Zebrafish vps33b, an ortholog of the gene responsible for human arthrogryposis-renal dysfunction-cholestasis syndrome, regulates biliary development downstream of the onecut transcription factor hnf6. Development 2005, 132:5295-5306.
37. Montesano R., Friend D.S., Perrelet A., Orci L. In vivo assembly of tight junctions in fetal rat liver. J. Cell Biol. 1975, 67:310-319.
38. Morris A.P., Tawil A., Berkova Z., Wible L., Smith C.W., Cunningham S.A. Junctional Adhesion Molecules (JAMs) are differentially expressed in fibroblasts and co-localize with ZO-1 to adherens-like junctions. Cell Commun. Adhes. 2006, 13:233-247.
39. Nemeth Z., Szasz A.M., Tatrai P., Nemeth J., Gyorffy H., Somoracz A., Szijarto A., Kupcsulik P., Kiss A., Schaff Z. Claudin-1, -2, -3, -4, -7, -8, and -10 protein expression in biliary tract cancers. J. Histochem. Cytochem. 2009, 57:113-121.
40. Parsons M.J., Pisharath H., Yusuff S., Moore J.C., Siekmann A.F., Lawson N., Leach S.D. Notch-responsive cells initiate the secondary transition in larval zebrafish pancreas. Mech. Dev. 2009, 126:898-912.
41. Parviz F., Matullo C., Garrison W.D., Savatski L., Adamson J.W., Ning G., Kaestner K.H., Rossi J.M., Zaret K.S., Duncan S.A. Hepatocyte nuclear factor 4alpha controls the development of a hepatic epithelium and liver morphogenesis. Nat. Genet. 2003, 34:292-296.
42. Sakaguchi T.F., Sadler K.C., Crosnier C., Stainier D.Y. Endothelial signals modulate hepatocyte apicobasal polarization in zebrafish. Curr. Biol. 2008, 18:1565-1571.
43. Saxena R., Theise N. Canals of Hering: recent insights and current knowledge. Semin. Liver Dis. 2004, 24:43-48.
44. Shin K., Fogg V.C., Margolis B. Tight junctions and cell polarity. Annu. Rev. Cell Dev. Biol. 2006, 22:207-235.
45. Si-Tayeb K., Lemaigre F.P., Duncan S.A. Organogenesis and development of the liver. Dev. Cell 2010, 18:175-189.
46. Son S., Kojima T., Decaens C., Yamaguchi H., Ito T., Imamura M., Murata M., Tanaka S., Chiba H., Hirata K., Sawada N. Knockdown of tight junction protein claudin-2 prevents bile canalicular formation in WIF-B9 cells. Histochem. Cell Biol. 2009, 131:411-424.
47. Stainier D.Y., Weinstein B.M., Detrich H.W., Zon L.I., Fishman M.C. Cloche, an early acting zebrafish gene, is required by both the endothelial and hematopoietic lineages. Development 1995, 121:3141-3150.
48. Sun Z., Hopkins N. vhnf1, the MODY5 and familial GCKD-associated gene, regulates regional specification of the zebrafish gut, pronephros, and hindbrain. Genes Dev. 2001, 15:3217-3229.
49. Swaim L.E., Connolly L.E., Volkman H.E., Humbert O., Bom D.E., Ramakrishnan L. Mycobacterium marinum infection of adult zebrafish causes caseating granulomatous tuberculosis and is moderated by adaptive immunity. Infect. Immun. 2006, 74:6108-6117.
50. Theard D., Steiner M., Kalicharan D., Hoekstra D., van Ijzendoorn S.C. Cell polarity development and protein trafficking in hepatocytes lacking E-cadherin/beta-catenin-based adherens junctions. Mol. Biol. Cell 2007, 18:2313-2321.
51. Thermes V., Grabher C., Ristoratore F., Bourrat F., Choulika A., Wittbrodt J., Joly J.S. I-SceI meganuclease mediates highly efficient transgenesis in fish. Mech. Dev. 2002, 118:91-98.
52. Tsukita S., Furuse M., Itoh M. Multifunctional strands in tight junctions. Nat. Rev. Mol. Cell Biol. 2001, 2:285-293.
53. Van Itallie C.M., Anderson J.M. Claudins and epithelial paracellular transport. Annu. Rev. Physiol. 2006, 68:403-429.
54. Van Itallie C.M., Rogan S., Yu A., Vidal L.S., Holmes J., Anderson J.M. Two splice variants of claudin-10 in the kidney create paracellular pores with different ion selectivities. Am. J. Physiol. Renal Physiol. 2006, 291:F1288-F1299.
55. Vroman B., LaRusso N.F. Development and characterization of polarized primary cultures of rat intrahepatic bile duct epithelial cells. Lab. Invest. 1996, 74:303-313.
56. Wakabayashi Y., Dutt P., Lippincott-Schwartz J., Arias I.M. Rab11a and myosin Vb are required for bile canalicular formation in WIF-B9 cells. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:15087-15092.
57. Westerfield M. The zebrafish book a guide for the laboratory use of zebrafish Danio (Brachydanio) rerio 2000, ZFIN, Eugene, Or. 4th ed.
58. Yeh T.H., Krauland L., Singh V., Zou B., Devaraj P., Stolz D.B., Franks J., Monga S.P., Sasatomi E., Behari J. Liver-specific beta-catenin knockout mice have bile canalicular abnormalities, bile secretory defect, and intrahepatic cholestasis. Hepatology 2010, 52:1410-1419.
59. Zong Y., Panikkar A., Xu J., Antoniou A., Raynaud P., Lemaigre F., Stanger B.Z. Notch signaling controls liver development by regulating biliary differentiation. Development 2009, 136:1727-1739.