Pax4 is not essential for beta-cell differentiation in zebrafish embryos but modulates alpha-cell generation by repressing arx gene expression

BMC Developmental Biology

Volumn 12, Issue 1, 2012, Pages

  Djiotsa, Joachim ^a   Verbruggen, Vincianne ^a   Giacomotto, Jean ^b   Ishibashi, Minaka ^b   Manning, Elisabeth ^b   Rinkwitz, Silke ^b   Manfroid, Isabelle ^a   Voz, Marianne L ^a   Peers, Bernard ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Arx; Development; Glucagon; Insulin; mRNA export; Pancreas; Pax4; Zebrafish

Indexed keywords

ARX PROTEIN, ZEBRAFISH; HOMEODOMAIN PROTEIN; MESSENGER RNA; MORPHOLINO OLIGONUCLEOTIDE; PAIRED BOX TRANSCRIPTION FACTOR; PAX4 PROTEIN, ZEBRAFISH; TRANSCRIPTION FACTOR; ZEBRAFISH PROTEIN;

ANIMAL; ANIMAL EMBRYO; ARTICLE; BIOSYNTHESIS; CELL DIFFERENTIATION; CYTOLOGY; DRUG EFFECT; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; METABOLISM; PANCREAS; PANCREAS ISLET ALPHA CELL; PANCREAS ISLET BETA CELL; PRENATAL DEVELOPMENT; RNA SPLICING; ZEBRA FISH;

ANIMALS; CELL DIFFERENTIATION; EMBRYO, NONMAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCKDOWN TECHNIQUES; GLUCAGON-SECRETING CELLS; HOMEODOMAIN PROTEINS; INSULIN-SECRETING CELLS; MORPHOLINOS; PAIRED BOX TRANSCRIPTION FACTORS; PANCREAS; RNA SPLICING; RNA, MESSENGER; TRANSCRIPTION FACTORS; ZEBRAFISH; ZEBRAFISH PROTEINS;

MLCS; MLOWN;

EID: 84870988178     PISSN: None     EISSN: 1471213X     Source Type: Journal    
DOI: 10.1186/1471-213X-12-37     Document Type: Article

References (42)

1. Edlund H: Pancreatic organogenesis–developmental mechanisms and implications for therapy. Nat Rev Genet 2002, 3(7):524–532.
2. Murtaugh LC: Pancreas and beta-cell development: from the actual to the possible. Development 2007, 134(3):427–438.
3. Jensen J: Gene regulatory factors in pancreatic development. Dev Dyn 2004, 229(1):176–200.
4. Offield MF, Jetton TL, Labosky PA, Ray M, Stein RW, Magnuson MA, Hogan BL, Wright CV: PDX-1 is required for pancreatic outgrowth and differentiation of the rostral duodenum. Development 1996, 122(3):983–995.
5. Kawaguchi Y, Cooper B, Gannon M, Ray M, MacDonald RJ, Wright CV: The role of the transcriptional regulator Ptf1a in converting intestinal to pancreatic progenitors. Nat Genet 2002, 32(1):128–134.
6. Jonsson J, Carlsson L, Edlund T, Edlund H: Insulin-promoter-factor 1 is required for pancreas development in mice. Nature 1994, 371(6498):606–609.
7. Naya FJ, Huang HP, Qiu Y, Mutoh H, DeMayo FJ, Leiter AB, Tsai MJ: Diabetes, defective pancreatic morphogenesis, and abnormal enteroendocrine differentiation in BETA2/neuroD-deficient mice. Genes Dev 1997, 11(18):2323–2334.
8. Gradwohl G, Dierich A, LeMeur M, Guillemot F: neurogenin3 is required for the development of the four endocrine cell lineages of the pancreas. Proc Natl Acad Sci USA 2000, 97(4):1607–1611.
9. Sussel L, Kalamaras J, Hartigan-O'Connor DJ, Meneses JJ, Pedersen RA, Rubenstein JL, German MS: Mice lacking the homeodomain transcription factor Nkx2.2 have diabetes due to arrested differentiation of pancreatic beta cells. Development 1998, 125(12):2213–2221.
10. Sosa-Pineda B, Chowdhury K, Torres M, Oliver G, Gruss P: The Pax4 gene is essential for differentiation of insulin-producing beta cells in the mammalian pancreas. Nature 1997, 386(6623):399–402.
11. Sander M, Sussel L, Conners J, Scheel D, Kalamaras J, Dela Cruz F, Schwitzgebel V, Hayes-Jordan A, German M: Homeobox gene Nkx6.1 lies downstream of Nkx2.2 in the major pathway of beta-cell formation in the pancreas. Development 2000, 127(24):5533–5540.
12. Collombat P, Mansouri A, Hecksher-Sorensen J, Serup P, Krull J, Gradwohl G, Gruss P: Opposing actions of Arx and Pax4 in endocrine pancreas development. Genes Dev 2003, 17(20):2591–2603.
13. Verbruggen V, Ek O, Georlette D, Delporte F, Von Berg V, Detry N, Biemar F, Coutinho P, Martial JA, Voz ML, et al: The Pax6b homeodomain is dispensable for pancreatic endocrine cell differentiation in zebrafish. J Biol Chem 2010, 285(18):13863–13873.
14. Heller RS, Stoffers DA, Liu A, Schedl A, Crenshaw EB 3rd, Madsen OD, Serup P: The role of Brn4/Pou3f4 and Pax6 in forming the pancreatic glucagon cell identity. Dev Biol 2004, 268(1):123–134.
15. Wang J, Elghazi L, Parker SE, Kizilocak H, Asano M, Sussel L, Sosa-Pineda B: The concerted activities of Pax4 and Nkx2.2 are essential to initiate pancreatic beta-cell differentiation. Dev Biol 2004, 266(1):178–189.
16. Greenwood AL, Li S, Jones K, Melton DA: Notch signaling reveals developmental plasticity of Pax4(+) pancreatic endocrine progenitors and shunts them to a duct fate. Mech Dev 2007, 124(2):97–107.
17. Sosa-Pineda B: The gene Pax4 is an essential regulator of pancreatic beta-cell development. Mol Cells 2004, 18(3):289–294.
18. Smith SB, Ee HC, Conners JR, German MS: Paired-homeodomain transcription factor PAX4 acts as a transcriptional repressor in early pancreatic development. Mol Cell Biol 1999, 19(12):8272–8280.
19. Collombat P, Xu X, Ravassard P, Sosa-Pineda B, Dussaud S, Billestrup N, Madsen OD, Serup P, Heimberg H, Mansouri A: The ectopic expression of Pax4 in the mouse pancreas converts progenitor cells into alpha and subsequently beta cells. Cell 2009, 138(3):449–462.
20. Brun T, Franklin I, St-Onge L, Biason-Lauber A, Schoenle EJ, Wollheim CB, Gauthier BR: The diabetes-linked transcription factor PAX4 promotes {beta}-cell proliferation and survival in rat and human islets. J Cell Biol 2004, 167(6):1123–1135.
21. Collombat P, Hecksher-Sorensen J, Broccoli V, Krull J, Ponte I, Mundiger T, Smith J, Gruss P, Serup P, Mansouri A: The simultaneous loss of Arx and Pax4 genes promotes a somatostatin-producing cell fate specification at the expense of the alpha- and beta-cell lineages in the mouse endocrine pancreas. Development 2005, 132(13):2969–2980.
22. Manousaki T, Feiner N, Begemann G, Meyer A, Kuraku S: Co-orthology of Pax4 and Pax6 to the fly eyeless gene: molecular phylogenetic, comparative genomic, and embryological analyses. Evol Dev 2011, 13(5):448–459.
23. Miura H, Yanazawa M, Kato K, Kitamura K: Expression of a novel aristaless related homeobox gene 'Arx' in the vertebrate telencephalon, diencephalon and floor plate. Mech Dev 1997, 65(1–2):99–109.
24. Binot AC, Manfroid I, Flasse L, Winandy M, Motte P, Martial JA, Peers B, Voz ML: Nkx6.1 and nkx6.2 regulate alpha- and beta-cell formation in zebrafish by acting on pancreatic endocrine progenitor cells. Dev Biol 2010, 340(2):397–407.
25. Mavropoulos A, Devos N, Biemar F, Zecchin E, Argenton F, Edlund H, Motte P, Martial JA, Peers B: sox4b is a key player of pancreatic alpha cell differentiation in zebrafish. Dev Biol 2005, 285(1):211–223.
26. Navratilova P, Fredman D, Hawkins TA, Turner K, Lenhard B, Becker TS: Systematic human/zebrafish comparative identification of cis-regulatory activity around vertebrate developmental transcription factor genes. Dev Biol 2009, 327(2):526–540.
27. Courtney M, Pfeifer A, Al-Hasani K, Gjernes E, Vieira A, Ben-Othman N, Collombat P: In vivo conversion of adult alpha-cells into beta-like cells: a new research avenue in the context of type 1 diabetes. Diabetes Obes Metab 2011, 13(Suppl 1):47–52.
28. Galy V, Gadal O, Fromont-Racine M, Romano A, Jacquier A, Nehrbass U: Nuclear retention of unspliced mRNAs in yeast is mediated by perinuclear Mlp1. Cell 2004, 116(1):63–73.
29. Rutz B, Seraphin B: A dual role for BBP/ScSF1 in nuclear pre-mRNA retention and splicing. EMBO J 2000, 19(8):1873–1886.
30. Naye F, Voz ML, Detry N, Hammerschmidt M, Peers B, Manfroid I: Essential roles of zebrafish bmp2a, fgf10, and fgf24 in the specification of the ventral pancreas. Mol Biol Cell 2012, 23(5):945–954.
31. Smith SB, Watada H, Scheel DW, Mrejen C, German MS: Autoregulation and maturity onset diabetes of the young transcription factors control the human PAX4 promoter. J Biol Chem 2000, 275(47):36910–36919.
32. Wendik B, Maier E, Meyer D: Zebrafish mnx genes in endocrine and exocrine pancreas formation. Dev Biol 2004, 268(2):372–383.
33. Dalgin G, Ward AB, le Hao T, Beattie CE, Nechiporuk A, Prince VE: Zebrafish mnx1 controls cell fate choice in the developing endocrine pancreas. Development 2011, 138(21):4597–4608.
34. Westerfield M: The zebrafish book. A guide for the laboratory use of zebrafish (danio rerio). 4th edition. Eugene: Univ. of Oregon Press; 1995.
35. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF: Stages of embryonic development of the zebrafish. Dev Dyn 1995, 203(3):253–310.
36. Hauptmann G, Gerster T: Two-color whole-mount in situ hybridization to vertebrate and Drosophila embryos. Trends Genet 1994, 10(8):266.
37. Cheesman SE, Layden MJ, Von Ohlen T, Doe CQ, Eisen JS: Zebrafish and fly Nkx6 proteins have similar CNS expression patterns and regulate motoneuron formation. Development 2004, 131(21):5221–5232.
38. Korzh V, Sleptsova I, Liao J, He J, Gong Z: Expression of zebrafish bHLH genes ngn1 and nrd defines distinct stages of neural differentiation. Dev Dyn 1998, 213(1):92–104.
39. Argenton F, Zecchin E, Bortolussi M: Early appearance of pancreatic hormone-expressing cells in the zebrafish embryo. Mech Dev 1999, 87(1–2):217–221.
40. Milewski WM, Duguay SJ, Chan SJ, Steiner DF: Conservation of PDX-1 structure, function, and expression in zebrafish. Endocrinology 1998, 139(3):1440–1449.
41. Pauls S, Zecchin E, Tiso N, Bortolussi M, Argenton F: Function and regulation of zebrafish nkx2.2a during development of pancreatic islet and ducts. Dev Biol 2007, 304(2):875–890.
42. Korzh V, Edlund T, Thor S: Zebrafish primary neurons initiate expression of the LIM homeodomain protein Isl-1 at the end of gastrulation. Development 1993, 118(2):417–425.