Members of the large Maf transcription family regulate insulin gene transcription in islet β cells

Molecular and Cellular Biology

Volumn 23, Issue 17, 2003, Pages 6049-6062

  Matsuoka, Taka Aki ^a   Zhao, Li ^a   Artner, Isabella ^a   Jarrett, Harry W ^c   Friedman, David ^b   Means, Anna ^b   Stein, Roland ^a,b  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; GENE PRODUCT; GLUCOSE; INSULIN; PROTEIN RIPE3B1; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR MAF; UNCLASSIFIED DRUG;

ACINAR CELL; AFFINITY CHROMATOGRAPHY; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CELL FUNCTION; CHROMATIN; CONTROLLED STUDY; DNA BINDING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; NUCLEOTIDE SEQUENCE; PANCREAS ISLET BETA CELL; PEPTIDE MAPPING; PH MEASUREMENT; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TANDEM MASS SPECTROMETRY; TRANSCRIPTION REGULATION; TWO DIMENSIONAL GEL ELECTROPHORESIS;

AMINO ACID SEQUENCE; ANIMALS; AVIAN PROTEINS; BINDING SITES; CELLS, CULTURED; DNA-BINDING PROTEINS; ENHANCER ELEMENTS (GENETICS); GENE EXPRESSION REGULATION; HOMEODOMAIN PROTEINS; HUMANS; HYDROGEN-ION CONCENTRATION; INSULIN; ISLETS OF LANGERHANS; LECTINS, C-TYPE; MACROMOLECULAR SUBSTANCES; MAF TRANSCRIPTION FACTORS, LARGE; MAFB TRANSCRIPTION FACTOR; MASS SPECTROMETRY; MICE; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; NUCLEAR PROTEINS; ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-MAF; SEQUENCE HOMOLOGY, AMINO ACID; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 0041970072     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.17.6049-6062.2003     Document Type: Article

References (82)

1. Ahlgren, U., J. Jonsson, L. Jonsson, K. Simu, H. Edlund. 1998. Beta-cell-specific inactivation of the mouse Ipf1/Pdx1 gene results in loss of the beta-cell phenotype and maturity onset diabetes. Genes Dev. 12:1763-1768.
2. Aronheim, A., H. Ohlsson, C. W. Park, T. Edlund, and M. D. Walker. 1991. Distribution and characterization of helix-loop-helix enhancer-binding proteins from pancreatic beta cells and lymphocytes. Nucleic Acids Res. 19:3893-3899.
3. Benkhelifa, S., S. Provot, O. Lecoq, C. Pouponnot, G. Calothy, and M. P. Felder-Schmittbuhl. 1998. mafA, a novel member of the maf proto-oncogene family, displays developmental regulation and mitogenic capacity in avian neuroretina cells. Oncogene 17:247-254.
4. Benkhelifa, S., S, Provot, E. Nabais, A. Eychene, G. Calothy, and M. P. Felder-Schmittbuhl. 2001. Phosphorylation of MafA is essential for its transcriptional and biological properties. Mol. Cell. Biol. 14:4441-4452.
5. Blank, V., and N. C. Andrews. 1997. The Maf transcription factors: regulators of differentiation. Trends Biochem. Sci. 22:437-441.
6. Bretherton-Watt, D., N. Gore, and D. S. W. Boam. 1996. Insulin upstream factor 1 and a novel ubiquitous factor bind to the human islet amyloid polypeptide/amylin gene promoter. Biochem. J. 313:495-502.
7. , Carty, M. D., J. S. Lillquist, M. Peshavaria, R. Stein, and W. C. Soeller. 1997. Identification of cis- and trans-active factors regulating islet amyloid polypeptide expression in pancreatic β cells. J. Biol. Chem. 272:11986-11993.
8. Civil, A., S. T. van Genesen, and N. H. Lubsen. 2002. c-Maf, the γD-crystallin Maf-responsive element and growth factor regulation. Nucleic Acids Res. 30:975-982.
9. Cordes, S. P., and G. S. Barsh. 1994. The mouse segmentation gene kr encodes a novel basic domain-leucine zipper transcription factor. Cell 79:1025-1034.
10. Cordle, S. R., E. Henderson, H. Masuoka, P. A. Weil, and R. Stein. 1991. Pancreatic β-cell-type-specific transcription of the insulin gene is mediated by basic helix-loop-helix DNA-binding proteins. Mol. Cell. Biol. 11:1734-1738.
11. De Wit, L., A. D. van Mansfeld, H. A. van Teeffelen, C. J. Lips, and J. W. Hoppener. 1993. Strong promoter activity of human and rat islet amyloid polypeptide/amylin gene constructs in mouse beta cells (βTC3). Biochem. Biophys. Res. Commun. 192:840-848.
12. Dumonteil, E., B. Laser, I. Constant, and J. Philippe. 1998. Differential regulation of the glucagon and insulin I gene promoters by the basic helix-loop-helix transcription factors E47 and BETA2. J. Biol. Chem. 273:19945-19954.
13. Edlund, H. 2002. Pancreatic organogenesis-developmental mechanisms and implications for therapy. Nat. Rev. Genet. 3:524-532.
14. Efrat, S., S. Linde, H. Kofod, D. Spector, M. Delannoy, S. Grant, D. Hanahan, and S. Baekkeskov. 1988. Beta-cell lines derived from transgenic mice expressing a hybrid insulin gene-oncogene. Proc. Natl. Acad. Sci. USA 85:9037-9041.
15. Gadgil, H., and H. W. Jarrett HW. 2002. Oligonucleotide trapping method for purification of transcription factors. J. Chromatogr. A 966(1-2):99-110.
16. Gannon, M., and C. V. E. Wright. 1999. Endoderm patterning and organogenesis, p. 583-615. In Sally Moody (ed.), Cell lineage and fate determination. Academic Press, Inc., San Diego, Calif.
17. German, M. S., M. A. Blanar, C. Nelson, L. G. Moss, and W. J. Rutter. 1991. Two related helix-loop-helix proteins participate in separate cell-specific complexes that bind the insulin enhancer. Mol. Endocrinol. 5:292-299.
18. German, M. S., L. G. Moss, J. Wang, and W. J. Rutter. 1992. The insulin and islet amyloid polypeptide genes contain similar cell-specific promoter elements that bind identical beta-cell nuclear complexes. Mol. Cell. Biol. 12:1777-1788.
19. Gerrish, K., M. A. Cissell, and R. Stein. 2001. The role of hepatic nuclear factor 1α and PDX-1 in transcriptional regulation of the pdx-1 gene. J. Biol. Chem. 276:47775-47784.
20. Hamaguchi, K., and E. H. Leiter. 1990. Comparison of cytokine effects on mouse pancreatic alpha-cell and beta-cell lines: viability, secretory function, and MHC antigen expression. Diabetes 39:415-425.
21. Jonsson, J., L. Carlsson, T. Edlund, and H. Edlund. 1994. Insulin-promoter-factor 1 is required for pancreas development in mice. Nature 371:606-609.
22. Kataoka, K., S. I. Han, S. Shioda, M. Hirai, M. Nishizawa, and H. Handa. 2002. MafA is a glucose-regulated and pancreatic beta-cell-specific transcriptional activator for the insulin gene. J. Biol. Chem. 277:49903-49910.
23. Kawauchi, S., S. Takahashi, O. Nakajima, H. Ogino, M. Morita, M. Nishizawa, K. Yasuda, and M. Yamamoto M. 1999. Regulation of lens fiber cell differentiation by transcription factor c-Maf. J. Biol. Chem. 274:19254-19260.
24. Kelly, L. M., U. Englmeier, I. Lafon, M. H. Sieweke, and T. Graf. 2000. MafB is an inducer of monocytic differentiation. EMBO J. 19:1987-1997.
25. Kerppola, T. K., and T. Curran. 1994. A conserved region adjacent to the basic domain is required for recognition of an extended DNA binding site by Maf/Nrl family proteins. Oncogene 9:3149-3158.
26. Kim, J. I., T. Li, I. C. Ho, M. J. Grusby, and L. H. Glimcher. 1999. Requirement for the c-Maf transcription factor in crystallin gene regulation and lens development. Proc. Natl. Acad. Sci. USA 96:3781-3785.
27. Kulkarni, R. N., J. C. Bruning, J. N. Winnay, C. Postic, M. A. Magnuson, and C. R. Kahn. 1998. Tissue-specific knockout of the insulin receptor in the pancreatic β cells creates an insulin secretory defect similar to that in type 2 diabetes. Cell 96:329-339.
28. Kumar, R. S. Chen, D. Scheurer, Q. L. Wang, E. Duh, C. H. Sung, A. Rehemtulla, A. Swaroop, R. Adler, and D. J. Zack. 1996. The bZIP transcription factor Nrl stimulates rhodopsin promoter activity in primary retinal cell cultures. J. Biol. Chem. 271:29612-29618.
29. Kushner, J. A., J. Ye, M. Schubert, D. J. Burks, M. A. Dow, C. L. Flint, S. Dutta, C. V. Wright, M. R. Montminy, and M. F. White. 2002. Pdx1 restores beta cell function in Irs2 knockout mice. J. Clin. Investig. 109:1193-1201.
30. Leibiger, I. B., B. Leibiger, and P. O, Berggren. 2002. Insulin feedback action on pancreatic beta-cell function. FEBS Lett. 532:1-6.
31. Leibiger, I. B., B. Leibiger, T. Moede, and P. O. Berggren. 1998. Exocytosis of insulin promotes insulin gene transcription via the insulin receptor/PI-3 kinase/p70 s6 kinase and CaM kinase pathways. Mol. Cell 1:933-938.
32. Malecki, M. T., U. S. Jhala, A. Antanellis, L. Fields, T. Orban, M. Saad, A. Doria, J. H. Warram, M. Montminy, and A. S. Krolewski. 1999. Mutations in NeuroD1/BETA2 are associated with the development of type 2 diabetes mellitus. Nat. Genet. 23:323-328.
33. Manzanares, M., S. Cordes, L. Ariza-McNaughton, V. Sadl, K. Maruthainar, G. Barsh, and R. Krumlauf. 1999. Conserved and distinct roles of kreisler in regulation of the paralogous Hoxa3 and Hoxb3 genes. Development 126:759-769.
34. Martin, C. C., L. J. Bischof, B. Bergman, L. A. Hornbuckle, C. Hilliker, C. Frigeri, D. Wahl, C. A. Svitek, R. Wong, J. K. Goldman, J. K. Oeser, F. Lepretre, P. Froguel, R. M. O'Brien, and J. C. Hutton. 2001. Cloning and characterization of the human and rat islet-specific glucose-6-phosphatase catalytic subunit-related protein (IGRP) genes. J. Biol. Chem. 276:25197-25207.
35. Mathis, D., L. Vence, and C. Benoist. 2001. Beta-cell death during progression to diabetes. Nature 414:792-798.
36. Matsuoka, T., L. Zhao, and R. Stein. 2001. The DNA binding activity of the RIPE3b1 transcription factor of the insulin gene appears to be influenced by tyrosine phosphorylation. J. Biol. Chem. 276:22071-22076.
37. Melloul, D., S. Marshak, and E. Cerasi. 2002. Regulation of insulin gene transcription. Diabetologia 45:309-326.
38. Miyazaki, J., K. Araki, E. Yamato, H. Ikegami, T. Asano, Y. Shibasaki, Y. Oka, and K. Yamamura. 1990. Establishment of a pancreatic beta cell line that retains glucose-inducible insulin secretion: special reference to expression of glucose transporter isoforms. Endocrinology 127:126-132.
39. Moates, J. M., S. Nanda, M. A. Cissell, M. J. Tsai, and R. Stein. 2003. BETA2 activates transcription from the upstream glucokinase gene promoter in islet beta-cells and gut endocrine cells. Diabetes 52:403-408.
40. Mosselman, S., J. W. Hoppener, L. de Wit, W. Soeller, C. J. Lips, and H. S. Jansz. 1990. IAPP/amylin gene transcriptional control region: evidence for negative regulation. FEBS Lett. 271:33-36.
41. Muta, M., Y. Kamachi, A. Yoshimoto, Y. Higashi, and H. Kondoh. 2002. Distinct roles of SOX2, Pax6, and Maf transcription factors in the regulation of lens-specific δ1-crystallin enhancer. Genes Cells 7:791-805.
42. Naya, F. J., C. M. M. Stellrecht, and M.-J. Tsai. 1995. Tissue-specific regulation of the insulin gene by a novel basic helix-loop-helix transcription factor. Genes Dev. 9:1009-1019.
43. Naya, F. J., H.-P. Huang, Y. Qiu, H. Mouth, F. J. DeMayo, A. B. Leiter, and M.-J. Tsai. 1997. Diabetes, defective pancreatic morphogenesis, and abnormal enteroendocrine differentiation in BETA2/NeuroD-deficient mice. Genes Dev. 11:2323-2334.
44. Offield, M. F., T. L. Jetton, R. Stein, T. Labosky, M. Ray, M. Magnuson, B. Hogan, and C. V. E. Wright. 1996. PDX-1 is required for development of the pancreas and differentiation of the rostral duodenum. Development 122:983-995.
45. Ogino, H., and K. Yasuda. Induction of lens differentiation by activation of a bZIP transcription factor, L-Maf. Science 280:115-158.
46. Ohlsson, H., K. Karlsson, and T. Edlund. 1993. IPF-1, a homeodomain-containing transactivator of the insulin gene. EMBO J. 12:4251-4259.
47. Olbrot, M., J. Rud, L. G. Moss, and A. Sharma. 2002. Identification of β-cell-specific insulin gene transcription factor RIPE3b1 as mammalian MafA. Proc. Natl. Acad. Sci. USA 99:6737-6742.
48. Peers, B., J. Leonard, S. Sharma, G. Teitelman, and M. R. Montminy. 1994. Insulin expression in pancreatic islet cells relies on cooperative interactions between the helix loop helix factor E47 and the homeobox factor STF-1. Mol. Endocrinol. 8:1798-1806.
49. Peshavaria, M., L. Gamer, E. Henderson, G. Teitelman, C. V. E. Wright, and R. Stein. 1994. XIHbox 8, an endoderm-specific Xenopus homeodomain protein, is closely related to a mammalian insulin gene transcription factor. Mol. Endocrinol. 8:806-816.
50. Petersen, H. V., P. Serup, J. Leonard, B. K. Michelsen, and O. D. Madsen. 1994. Transcriptional regulation of the human insulin gene is dependent of the homeodomain proteins STF1/IPF1 acting through the CT boxes. Proc. Natl. Acad. Sci. USA 91:10465-10469.
51. Peyton, M., L. Moss, and M.-J. Tsai. 1994. Two distinct class A helix-loop-helix transcription factors, E2A and BETA1, form separate DNA-binding complexes on the insulin E-box. J. Biol. Chem. 269:25936-25941.
52. Planque, N., L. Leconte, F. M. Coquelle, S. Benkhelifa, P. Martin, M. P. Felder-Schmittbuhl, and S. Saule. 2001. Interaction of Maf transcription factors with Pax-6 results in synergistic activation of the glucagon promoter. J. Biol. Chem. 276:35751-35760.
53. Rehemtulla, A., R. Warwar, R. Kumar, X. Ji, D. J. Zack, and A. Swaroop. 1996. The basic motif-leucine zipper transcription factor Nrl can positively regulate rhodopsin gene expression. Proc. Natl. Acad. Sci. USA 93:191-195.
54. Reza, H. M., H. Ogino, and K. Yasuda. 2002. L-Maf, a downstream target of Pax6, is essential for chick lens development. Mech. Dev. 116:61-73.
55. Ring, B. Z., S. P. Cordes, P. A. Overbeek, and G. S. Barsh. 2000. Regulation of mouse lens fiber cell development and differentiation by the Maf gene. Development 127:307-317.
56. Sadl, V., F. Jin, J. Yu, S. Cui, D. Holmyard, S. Quaggin, G. Barsh, and S. Cordes. 2002. The mouse Kreisler (Krml1/MafB) segmentation gene is required for differentiation of glomerular visceral epithelial cells. Dev. Biol. 249:16-29.
57. Sakai, M., J. Imaki, K. Yoshida, A. Ogata, Y. Matsushima-Hibaya, Y. Kuboki, M. Nishizawa, and S. Nishi. 1997. Rat maf related genes: specific expression in chondrocytes, lens, and spinal cord. Oncogene 14:745-750.
58. Sakai, M., M. S. Serria, H. Ikeda, K. Yoshida, J. Imaki, and S. Nishi. 2001. Regulation of c-maf gene expression by Pax6 in cultured cells. Nucleic Acids Res. 29:1228-1237.
59. Samaras, S. E., L. Zhao, A. Means, E. Henderson, T. A. Matsuoka, and R. Stein. 2003. The islet β-cell-enriched RIPE3b1/Maf transcription factor regulates pdx-1 expression. J. Biol. Chem. 278:12263-12270.
60. Sander, M., and M. S. German. 1997. The beta cell transcription factors and development of the pancreas. J. Mol. Med. 75:327-340.
61. Sander, M., A. Neubuser, J. Kalamaras, H. C. Ee, G. R. Martin, and M. S. German. 1997. Genetic analysis reveals that PAX6 is required for normal transcription of pancreatic hormone genes and islet development. Gene Dev. 11:1662-1673.
62. Sander, M., L. Sussel, J. Conners, D. Scheel, J. Kalamaras, F. Dela Cruz, V. Schwitzgebel, A. Hayes-Jordan, and M. German. 2000. Homeobox gene Nkx6.1 lies downstream of Nkx2.2 in the major pathway of beta-cell formation in the pancreas. Development 127:5533-5540.
63. Schreiber, E., P. Matthias, M. M. Muller, and W. Schaffner. 1989. Eukaryotic expression vectors for the analysis of mutant proteins. Nucleic Acids Res. 17:6418.
64. Serup, P., J. Jensen, F. G. Andersen, M. C. Jorgensen, N. Blume, J. J. Holst, and O. D. Madsen. 1996. Induction of insulin and islet amyloid polypeptide production in pancreatic islet glucagonoma cells by insulin promoter factor 1. Proc. Natl. Acad. Sci. USA 93:9015-9020.
65. Shieh, S.-Y., and M.-J. Tsai. 1991. Cell-specific and ubiquitous factors are responsible for the enhancer activity of the rat insulin II gene. J. Biol. Chem. 266:16708-16714.
66. Shieh, S.-Y., M. M. Stellrecht, and M.-J. Tsai. 1995. Molecular characterization of the rat insulin enhancer-binding complex 3b2. J. Biol. Chem. 270:21503-21508.
67. Stein, R. 2001. Insulin gene transcription: the factors involved in cell-type-specific and glucose-regulated expression in islet β cells are also essential during pancreatic development, p. 25-78. In A. Cherrington and J. Jefferson (ed.), Handbook of physiology, vol. II. American Physiology Society, Washington, D.C.
68. Stoffers, D. A., J. Ferrer, W. L. Clarke, and J. F. Habener. 1997. Early-onset type-II diabetes mellitus (MODY4) linked to IPF1. Nat. Genet. 17:138-139.
69. Stoffers, D. A., N. T. Zinkin, V. Stanojevic, W. L. Clarke, and J. F. Habener. 1997. Pancreatic agenesis attributable to a single nucleotide deletion in the human IPF1 gene coding sequence. Nat. Genet. 15:106-110.
70. St-Onge, L., B. Sosa-Pineda, K. Chowdhury, A. Mansouri, and P. Gruss. 1997. Pax6 is required for differentiation of glucagon-producing α-cells in mouse pancreas. Nature 387:406-409.
71. Swift, G. H., Y. Liu, S. D. Rose, L. J. Bischof, S. Steelman, A. M. Buchberg, C. V. Wright, and R. J. MacDonald. 1998. An endocrine-exocrine switch in the activity of the pancreatic homeodomain protein PDX1 through formation of a trimeric complex with PBX1b and MRG1 (MEIS2). Mol. Cell. Biol. 18:5109-5120.
72. Taylor, S. I. 1999. Deconstructing type 2 diabetes. Cell 97:9-12.
73. Vinson, C., M. Myakishev, A. Acharya, A. A. Mir, J. R. Moll, and M. Bonovich. 2002. Classification of human B-ZIP proteins based on dimerization properties. Mol. Cell. Biol. 22:6321-6335.
74. Waeber, G., N. Thompson, P. Nicod, and C. Bonny. 1996. Transcriptional activation of the GLUT2 gene by the IPF-1/STF-1/IDX-1 homeobox factor. Mol. Endocrinol. 10:1327-1334.
75. Watada, H., Y. Kajimoto, H. Kaneto, T. Matsuoka, Y. Fujitani, J. Miyazaki, and Y. Yamasaki. 1996. Involvement of the homeodomain-containing transcription factor PDX-1 in islet amyloid polypeptide gene transcription. Biochem. Biophys. Res. Commun. 229:746-751.
76. Watada, H., Y. Kajimoto, J. Miyagwa, T. Hanafusa, K. Hamaguchi, T. Matsuoka, K. Yamamoto, Y. Matsuzawa, R. Kawamori, and Y. Yamasaki. 1996. PDX-1 induces insulin and glucokinase gene expression in αTC1 clone 6 cells in the presence of betacellulin. Diabetes 45:1826-1831.
77. Watada, H., Y. Umayahara, T. Matsuoka, H. Kaneto, Y. Fujitani, T. Kamada, R. Kawamori, and Y. Yamasaki. 1996. The human glucokinase gene β-cell-type promoter: an essential role of insulin promoter factor 1/PDX-1 in its activation in HIT-T15 cells. Diabetes 45:1478-1488.
78. Whelan, J., S. R. Cordle, E. Henderson, P. A. Weil, and R. Stein. 1990. Identification of a pancreatic β-cell insulin gene transcription factor that binds to and appears to activate cell-type-specific expression: its possible relationship to other cellular factors that bind to a common insulin gene sequence. Mol. Cell. Biol. 10:1564-1572.
79. Withers, D. J., D. J. Burks, D. J., H. H. Towery, S. L. Altamuro, C. L. Flint, and M. F. White. 1999. Irs-2 coordinates Igf-1 receptor-mediated β-cell development and peripheral insulin signalling. Nat. Genet. 23:32-40.
80. Wu, K.-L., M. Peshavaria, M. Gannon, E. Henderson, M. F. Offield, E. Henderson, M. Ray, A. Marks, L. W. Gamer, C. V. E. Wright, and R. Stein. 1997. HNF3β is involved in pancreatic β-cell-specific transcription of the pdx-1 gene. Mol. Cell. Biol. 17:6002-6013.
81. Yasuda, T., Y. Kajimoto, Y. Fujitani, H. Watada, S. Yamamoto, T. Watarai, Y. Umayahara, M. Matsuhisa, S. Gorogawa, Y. Kuwayama, Y. Tano, Y. Yamasaki, and M. Hori. 2002. PAX6 mutation as a genetic factor common to aniridia and glucose intolerance. Diabetes 51:224-230.
82. Zhao, L., M. A. Cissell, E. Henderson, R. Colbran, and R. Stein. 2000. The RIPE3b1 activator of the insulin gene is composed of a protein(s) of approximately 43 kDa, whose DNA binding activity is inhibited by protein phosphatase treatment. J. Biol. Chem. 275:10532-10537.