Endocrine pancreas development in zebrafish

Cell Cycle

Volumn 10, Issue 20, 2011, Pages 3466-3472

  Tehrani, Zahra ^a   Lin, Shuo ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Development; Endocrine; Insulin; Islet; Pancreas; Zebrafish; cell

Indexed keywords

CELL MATURATION; DIABETES MELLITUS; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; GASTRULATION; NONHUMAN; ORGANOGENESIS; PANCREAS ISLET; PANCREAS ISLET BETA CELL; REVIEW; SIGNAL TRANSDUCTION; ZEBRA FISH;

DANIO RERIO;

EID: 80055118585     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.10.20.17764     Document Type: Review

References (81)

1. Edlund H. Pancreatic organogenesis-developmental mechanisms and implications for therapy. Nat Rev Genet 2002; 3:524-32; PMID:12094230; DOI:10.1038/nrg841.
2. Kumar M, Melton D. Pancreas specification: a budding question. Curr Opin Genet Dev 2003; 13:401-7; PMID:12888014; DOI:10.1016/S0959-437X(03)00089-3.
3. Murtaugh LC, Melton DA. Genes, signals and lineages in pancreas development. Annu Rev Cell Dev Biol 2003; 19:71-89; PMID:14570564; DOI:10.1146/ annurev.cellbio.19.111301.144752.
4. Bell GI, Polonsky KS. Diabetes mellitus and genetically programmed defects in beta-cell function. Nature 2001; 414:788-91; PMID:11742410; DOI:10.1038/414788a.
5. Mi QS, He HZ, Dong Z, Isales C, Zhou L. microRNA deficiency in pancreatic islet cells exacerbates streptozotocin-induced murine autoimmune diabetes. Cell Cycle 2010; 9:3127-9; PMID:20699654; DOI:10.4161/cc.9.15.12596.
6. Gunasekaran U, Gannon M. Type 2 diabetes and the aging pancreatic Beta cell. Aging (Albany NY); 3:565- 75.
7. Kuhlow D, Florian S, von Figura G, Weimer S, Schulz N, Petzke KJ, et al. Telomerase deficiency impairs glucose metabolism and insulin secretion. Aging (Albany NY); 2:650-8.
8. Lee SH, Itkin-Ansari P, Levine F. CENP-A, a protein required for chromosome segregation in mitosis, declines with age in islet but not exocrine cells. Aging (Albany NY); 2:785-90.
9. Zhou Q, Melton DA. Pathways to new beta cells. Cold Spring Harb Symp Quant Biol 2008; 73:175-81; PMID:19478324; DOI:10.1101/sqb.2008.72.002.
10. Kroon E, Martinson LA, Kadoya K, Bang AG, Kelly OG, Eliazer S, et al. Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo. Nat Biotechnol 2008; 26:443-52; PMID:18288110; DOI:10.1038/ nbt1393.
11. D'Amour KA, Bang AG, Eliazer S, Kelly OG, Agulnick AD, Smart NG, et al. Production of pancreatic hormone- expressing endocrine cells from human embryonic stem cells. Nat Biotechnol 2006; 24:1392-401; PMID:17053790; DOI:10.1038/nbt1259.
12. D'Amour KA, Agulnick AD, Eliazer S, Kelly OG, Kroon E, Baetge EE. Efficient differentiation of human embryonic stem cells to definitive endoderm. Nat Biotechnol 2005; 23:1534-41; PMID:16258519; DOI:10.1038/nbt1163.
13. Zon LI, Peterson RT. In vivo drug discovery in the zebrafish. Nat Rev Drug Discov 2005; 4:35-44; PMID:15688071; DOI:10.1038/nrd1606.
14. Driever W, Solnica-Krezel L, Schier AF, Neuhauss SC, Malicki J, Stemple DL, et al. A genetic screen for mutations affecting embryogenesis in zebrafish. Development 1996; 123:37-46; PMID:9007227.
15. Pichler FB, Laurenson S, Williams LC, Dodd A, Copp BR, Love DR. Chemical discovery and global gene expression analysis in zebrafish. Nat Biotechnol 2003; 21:879-83; PMID:12894204; DOI:10.1038/nbt852.
16. Ober EA, Field HA, Stainier DY. From endoderm formation to liver and pancreas development in zebrafish. Mech Dev 2003; 120:5-18; PMID:12490292; DOI:10.1016/S0925-4773(02)00327-1.
17. Field HA, Dong PD, Beis D, Stainier DY. Formation of the digestive system in zebrafish. II. Pancreas morphogenesis. Dev Biol 2003; 261:197- 208; PMID:12941629; DOI:10.1016/S0012- 1606(03)00308-7.
18. Li Z, Wen C, Peng J, Korzh V, Gong Z. Generation of living color transgenic zebrafish to trace somatostatinexpressing cells and endocrine pancreas organization. Differentiation 2009; 77:128-34; PMID:19281772; DOI:10.1016/j.diff.2008.09.014.
19. Wang Y, Rovira M, Yusuff S, Parsons MJ. Genetic inducible fate mapping in larval zebrafish reveals origins of adult insulin-producing beta-cells. Development 2011; 138:609-17; PMID:21208992; DOI:10.1242/ dev.059097.
20. Hesselson D, Anderson RM, Beinat M, Stainier DY. Distinct populations of quiescent and proliferative pancreatic beta-cells identified by HOTcre mediated labeling. Proc Natl Acad Sci USA 2009; 106:14896-901; PMID:19706417; DOI:10.1073/pnas.0906348106.
21. Bagnat M, Cheung ID, Mostov KE, Stainier DY. Genetic control of single lumen formation in the zebrafish gut. Nat Cell Biol 2007; 9:954-60; PMID:17632505; DOI:10.1038/ncb1621.
22. Wallace KN, Pack M. Unique and conserved aspects of gut development in zebrafish. Dev Biol 2003; 255:12-29; PMID:12618131; DOI:10.1016/S0012- 1606(02)00034-9.
23. Warga RM, Nusslein-Volhard C. Origin and development of the zebrafish endoderm. Development 1999; 126:827-38; PMID:9895329.
24. Kikuchi Y, Agathon A, Alexander J, Thisse C, Waldron S, Yelon D, et al. casanova encodes a novel Sox-related protein necessary and sufficient for early endoderm formation in zebrafish. Genes Dev 2001; 15:1493-505; PMID:11410530; DOI:10.1101/gad.892301.
25. Alexander J, Stainier DY. A molecular pathway leading to endoderm formation in zebrafish. Curr Biol 1999; 9:1147-57; PMID:10531029; DOI:10.1016/S0960- 9822(00)80016-0.
26. Poulain M, Furthauer M, Thisse B, Thisse C, Lepage T. Zebrafish endoderm formation is regulated by combinatorial Nodal, FGF and BMP signalling. Development 2006; 133:2189-200; PMID:16672336; DOI:10.1242/dev.02387.
27. Tiso N, Moro E, Argenton F. Zebrafish pancreas development. Mol Cell Endocrinol 2009.
28. Ward AB, Warga RM, Prince VE. Origin of the zebrafish endocrine and exocrine pancreas. Dev Dyn 2007; 236:1558-69; PMID:17474119; DOI:10.1002/ dvdy.21168.
29. Kondo M. Bone morphogenetic proteins in the early development of zebrafish. FEBS J 2007; 274:2960-7; PMID:17521339; DOI:10.1111/j.1742- 4658.2007.05838.x.
30. Tiso N, Filippi A, Pauls S, Bortolussi M, Argenton F. BMP signalling regulates anteroposterior endoderm patterning in zebrafish. Mech Dev 2002; 118:29-37; PMID:12351167; DOI:10.1016/S0925- 4773(02)00252-6.
31. Tucker JA, Mintzer KA, Mullins MC. The BMP signaling gradient patterns dorsoventral tissues in a temporally progressive manner along the anteroposterior axis. Dev Cell 2008; 14:108-19; PMID:18194657; DOI:10.1016/j.devcel.2007.11.004.
32. Chung WS, Andersson O, Row R, Kimelman D, Stainier DY. Suppression of Alk8-mediated Bmp signaling cell-autonomously induces pancreatic {beta}- cells in zebrafish. Proc Natl Acad Sci USA 2009.
33. Tehrani Z, Lin S. Antagonistic interactions of hedgehog, Bmp and retinoic acid signals control zebrafish endocrine pancreas development. Development 2011; 138:631-40; PMID:21228001; DOI:10.1242/ dev.050450.
34. Krauss S, Concordet JP, Ingham PW. A functionally conserved homolog of the Drosophila segment polarity gene hh is expressed in tissues with polarizing activity in zebrafish embryos. Cell 1993; 75:1431-44; PMID:8269519; DOI:10.1016/0092-8674(93)90628- 4.
35. Chung WS, Stainier DY. Intra-endodermal interactions are required for pancreatic beta cell induction. Dev Cell 2008; 14:582-93; PMID:18410733; DOI:10.1016/j. devcel.2008.02.012.
36. diIorio PJ, Moss JB, Sbrogna JL, Karlstrom RO, Moss LG. Sonic hedgehog is required early in pancreatic islet development. Dev Biol 2002; 244:75-84; PMID:11900460; DOI:10.1006/dbio.2002.0573.
37. Roy S, Qiao T, Wolff C, Ingham PW. Hedgehog signaling pathway is essential for pancreas specification in the zebrafish embryo. Curr Biol 2001; 11:1358-63; PMID:11553330; DOI:10.1016/S0960- 9822(01)00402-X.
38. Hebrok M, Kim SK, Melton DA. Notochord repression of endodermal Sonic hedgehog permits pancreas development. Genes Dev 1998; 12:1705-13; PMID:9620856; DOI:10.1101/gad.12.11.1705.
39. Kim SK, Melton DA. Pancreas development is promoted by cyclopamine, a hedgehog signaling inhibitor. Proc Natl Acad Sci USA 1998; 95:13036-41; PMID:9789036; DOI:10.1073/pnas.95.22.13036.
40. Lau J, Kawahira H, Hebrok M. Hedgehog signaling in pancreas development and disease. Cell Mol Life Sci 2006; 63:642-52; PMID:16465449; DOI:10.1007/ s00018-005-5357-z.
41. Stafford D, White RJ, Kinkel MD, Linville A, Schilling TF, Prince VE. Retinoids signal directly to zebrafish endoderm to specify insulin-expressing beta-cells. Development 2006; 133:949-56; PMID:16452093; DOI:10.1242/dev.02263.
42. Stafford D, Prince VE. Retinoic acid signaling is required for a critical early step in zebrafish pancreatic development. Curr Biol 2002; 12:1215-20; PMID:12176331; DOI:10.1016/S0960-9822(02)00929-6.
43. Borowiak M, Maehr R, Chen S, Chen AE, Tang W, Fox JL, et al. Small molecules efficiently direct endodermal differentiation of mouse and human embryonic stem cells. Cell Stem Cell 2009; 4:348-58; PMID:19341624; DOI:10.1016/j.stem.2009.01.014.
44. Song J, Kim HJ, Gong Z, Liu NA, Lin S. Vhnf1 acts downstream of Bmp, Fgf and RA signals to regulate endocrine beta cell development in zebrafish. Dev Biol 2007; 303:561-75; PMID:17217944; DOI:10.1016/j. ydbio.2006.11.040.
45. Martín M, Gallego-Llamas J, Ribes V, Kedinger M, Niederreither K, Chambon P, et al. Dorsal pancreas agenesis in retinoic acid-deficient Raldh2 mutant mice. Dev Biol 2005; 284:399-411; PMID:16026781; DOI:10.1016/j.ydbio. 2005.05.035.
46. Molotkov A, Molotkova N, Duester G. Retinoic acid generated by Raldh2 in mesoderm is required for mouse dorsal endodermal pancreas development. Dev Dyn 2005; 232:950-7; PMID:15739227; DOI:10.1002/dvdy.20256.
47. Stafford D, Hornbruch A, Mueller PR, Prince VE. A conserved role for retinoid signaling in vertebrate pancreas development. Dev Genes Evol 2004; 214:432-41; PMID:15322880; DOI:10.1007/s00427-004-0420-6.
48. Kinkel MD, Sefton EM, Kikuchi Y, Mizoguchi T, Ward AB, Prince VE. Cyp26 enzymes function in endoderm to regulate pancreatic field size. Proc Natl Acad Sci USA 2009; 106:7864-9; PMID:19416885; DOI:10.1073/pnas.0813108106.
49. Kinkel MD, Eames SC, Alonzo MR, Prince VE. Cdx4 is required in the endoderm to localize the pancreas and limit beta-cell number. Development 2008; 135:919- 29; PMID:18234725; DOI:10.1242/dev.010660.
50. Kinkel MD, Prince VE. On the diabetic menu: zebrafish as a model for pancreas development and function. Bioessays 2009; 31:139-52; PMID:19204986; DOI:10.1002/bies.200800123.
51. Mizoguchi T, Verkade H, Heath JK, Kuroiwa A, Kikuchi Y. Sdf1/Cxcr4 signaling controls the dorsal migration of endodermal cells during zebrafish gastrulation. Development 2008; 135:2521-9; PMID:18579679; DOI:10.1242/dev. 020107.
52. Nair S, Schilling TF. Chemokine signaling controls endodermal migration during zebrafish gastrulation. Science 2008; 322:89-92; PMID:18719251; DOI:10.1126/science.1160038.
53. Matsui T, Raya A, Kawakami Y, Callol-Massot C, Capdevila J, Rodriguez-Esteban C, et al. Noncanonical Wnt signaling regulates midline convergence of organ primordia during zebrafish development. Genes Dev 2005; 19:164-75; PMID:15630025; DOI:10.1101/ gad.1253605.
54. Kim HJ, Schleiffarth JR, Jessurun J, Sumanas S, Petryk A, Lin S, et al. Wnt5 signaling in vertebrate pancreas development. BMC Biol 2005; 3:23; PMID:16246260; DOI:10.1186/1741-7007-3-23.
55. Biemar F, Argenton F, Schmidtke R, Epperlein S, Peers B, Driever W. Pancreas development in zebrafish: early dispersed appearance of endocrine hormone expressing cells and their convergence to form the definitive islet. Dev Biol 2001; 230:189-203; PMID:11161572; DOI:10.1006/dbio.2000.0103.
56. Gu G, Dubauskaite J, Melton DA. Direct evidence for the pancreatic lineage: NGN3+ cells are islet progenitors and are distinct from duct progenitors. Development 2002; 129:2447-57; PMID:11973276.
57. Huang H, Liu N, Lin S. Pdx-1 knockdown reduces insulin promoter activity in zebrafish. Genesis 2001; 30:134-6; PMID:11477691; DOI:10.1002/ gene.1048.
58. Yee NS, Yusuff S, Pack M. Zebrafish pdx1 morphant displays defects in pancreas development and digestive organ chirality, and potentially identifies a multipotent pancreas progenitor cell. Genesis 2001; 30:137-40; PMID:11477692; DOI:10.1002/gene.1049.
59. Jonsson J, Carlsson L, Edlund T, Edlund H. Insulinpromoter- factor 1 is required for pancreas development in mice. Nature 1994; 371:606-9; PMID:7935793; DOI:10.1038/371606a0.
60. Offield MF, Jetton TL, Labosky PA, Ray M, Stein RW, Magnuson MA, et al. PDX-1 is required for pancreatic outgrowth and differentiation of the rostral duodenum. Development 1996; 122:983-95; PMID:8631275.
61. Ahlgren U, Jonsson J, Edlund H. The morphogenesis of the pancreatic mesenchyme is uncoupled from that of the pancreatic epithelium in IPF1/PDX1- deficient mice. Development 1996; 122:1409-16; PMID:8625829.
62. Fujitani Y, Fujitani S, Boyer DF, Gannon M, Kawaguchi Y, Ray M, et al. Targeted deletion of a cis-regulatory region reveals differential gene dosage requirements for Pdx1 in foregut organ differentiation and pancreas formation. Genes Dev 2006; 20:253-66; PMID:16418487; DOI:10.1101/gad.1360106.
63. Zhou Q, Brown J, Kanarek A, Rajagopal J, Melton DA. In vivo reprogramming of adult pancreatic exocrine cells to beta-cells. Nature 2008; 455:627-32; PMID:18754011; DOI:10.1038/nature07314.
64. Oliver-Krasinski JM, Stoffers DA. On the origin of the beta cell. Genes Dev 2008; 22:1998-2021; PMID:18676806; DOI:10.1101/gad.1670808.
65. Zecchin E, Filippi A, Biemar F, Tiso N, Pauls S, Ellertsdottir E, et al. Distinct delta and jagged genes control sequential segregation of pancreatic cell types from precursor pools in zebrafish. Dev Biol 2007; 301:192-204; PMID:17059815; DOI:10.1016/j. ydbio.2006.09.041.
66. Apelqvist A, Li H, Sommer L, Beatus P, Anderson DJ, Honjo T, et al. Notch signalling controls pancreatic cell differentiation. Nature 1999; 400:877-81; PMID:10476967; DOI:10.1038/23716.
67. Jensen J, Pedersen EE, Galante P, Hald J, Heller RS, Ishibashi M, et al. Control of endodermal endocrine development by Hes-1. Nat Genet 2000; 24:36-44; PMID:10615124; DOI:10.1038/71657.
68. Esni F, Ghosh B, Biankin AV, Lin JW, Albert MA, Yu X, et al. Notch inhibits Ptf1 function and acinar cell differentiation in developing mouse and zebrafish pancreas. Development 2004; 131:4213-24; PMID:15280211; DOI:10.1242/dev.01280.
69. 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; 213:92- 104; PMID:9733104; DOI:10.1002/(SICI)1097- 0177(199809)213: 1〈92::AID-AJA9〉3.0.CO;2-T
70. Anderson KR, Torres CA, Solomon K, Becker TC, Newgard CB, Wright CV, et al. Cooperative transcriptional regulation of the essential pancreatic islet gene NeuroD1 (beta2) by Nkx2.2 and neurogenin 3. J Biol Chem 2009; 284:31236-48; PMID:19759004; DOI:10.1074/jbc.M109.048694.
71. Murtaugh LC. Pancreas and beta-cell development: from the actual to the possible. Development 2007; 134:427-38; PMID:17185316; DOI:10.1242/ dev.02770.
72. Manfroid I, Delporte F, Baudhuin A, Motte P, Neumann CJ, Voz ML, et al. Reciprocal endodermmesoderm interactions mediated by fgf24 and fgf10 govern pancreas development. Development 2007.
73. Zecchin E, Mavropoulos A, Devos N, Filippi A, Tiso N, Meyer D, et al. Evolutionary conserved role of ptf1a in the specification of exocrine pancreatic fates. Dev Biol 2004; 268:174-84; PMID:15031114; DOI:10.1016/j.ydbio.2003.12. 016.
74. Lin JW, Biankin AV, Horb ME, Ghosh B, Prasad NB, Yee NS, et al. Differential requirement for ptf1a in endocrine and exocrine lineages of developing zebrafish pancreas. Dev Biol 2004; 274:491-503; PMID:15570689; DOI:10.1016/j.ydbio.2004.07.001.
75. Krapp A, Knofler M, Frutiger S, Hughes GJ, Hagenbuchle O, Wellauer PK. The p48 DNA-binding subunit of transcription factor PTF1 is a new exocrine pancreas-specific basic helix-loop-helix protein. EMBO J 1996; 15:4317-29; PMID:8861960.
76. 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; 32:128-34; PMID:12185368; DOI:10.1038/ng959.
77. Krapp A, Knofler M, Ledermann B, Burki K, Berney C, Zoerkler N, et al. The bHLH protein PTF1-p48 is essential for the formation of the exocrine and the correct spatial organization of the endocrine pancreas. Genes Dev 1998; 12:3752-63; PMID:9851981; DOI:10.1101/gad.12.23.3752.
78. Dong PD, Provost E, Leach SD, Stainier DY. Graded levels of Ptf1a differentially regulate endocrine and exocrine fates in the developing pancreas. Genes Dev 2008; 22:1445-50; PMID:18519637; DOI:10.1101/ gad.1663208.
79. Hesselson D, Anderson RM, Stainier DY. Suppression of Ptf1a activity induces acinar-to-endocrine conversion. Curr Biol 2011; 21:712-7; PMID:21497092; DOI:10.1016/j.cub.2011.03.041.
80. Tiso N, Moro E, Argenton F. Zebrafish pancreas development. Mol Cell Endocrinol 2009; 312:24-30; PMID:19477220; DOI:10.1016/j.mce.2009.04.018.
81. Parsons MJ, Pisharath H, Yusuff S, Moore JC, Siekmann AF, Lawson N, et al. Notch-responsive cells initiate the secondary transition in larval zebrafish pancreas. Mech Dev 2009; 126:898-912; PMID:19595765; DOI:10.1016/j.mod.2009.07. 002.