Serum response factor expression is enriched in pancreatic β cells and regulates insulin gene expression

FASEB Journal

Volumn 25, Issue 8, 2011, Pages 2592-2603

  Sarkar, Aloke ^a   Zhang, Mao ^a   Liu, Shi He ^a   Sarkar, Swapna ^a   Brunicardi, F Charles ^a   Berger, David H ^a   Belaguli, Narasimhaswamy S ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Knock in; LacZ; Pdx 1

Indexed keywords

BETA GALACTOSIDASE; GLUCOSE; INSULIN; REGULATOR PROTEIN; SERUM RESPONSE FACTOR; TRANSCRIPTION FACTOR PDX 1;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; GENE ACTIVATION; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; INSULIN RELEASE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT;

ANIMALS; BASE SEQUENCE; BINDING SITES; CELL LINE; CELL NUCLEUS; CYTOPLASM; GENE EXPRESSION REGULATION; GLUCOSE; HOMEODOMAIN PROTEINS; INSULIN; INSULIN-SECRETING CELLS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, FLUORESCENCE; PROMOTER REGIONS, GENETIC; RATS; RNA, SMALL INTERFERING; SERUM RESPONSE FACTOR; TRANS-ACTIVATORS; TRANSFECTION;

ANIMALIA; MURINAE; RATTUS;

EID: 80051691457     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.10-173757     Document Type: Article

References (50)

1. Shore, P., and Sharrocks, A. D. (1995) The MADS-box family of transcription factors. Eur. J. Biochem. 229, 1-13
2. Li, S., Czubryt, M. P., McAnally, J., Bassel-Duby, R., Richardson, J. A., Wiebel, F. F., Nordheim, A., and Olson, E. N. (2005) Requirement for serum response factor for skeletal muscle Growth and maturation revealed by tissue-specific gene deletion in mice. Proc. Natl. Acad. Sci. U. S. A. 102, 1082-1087 (Pubitemid 40170729)
3. Miano, J. M. (2003) Serum response factor: toggling between disparate programs of gene expression. J. Mol. Cell. Cardiol. 35, 577-593
4. Niu, Z., Yu, W., Zhang, S. X., Barron, M., Belaguli, N. S., Schneider, M. D., Parmacek, M., Nordheim, A., and Schwartz, R. J. (2005) Conditional mutagenesis of the murine serum response factor gene blocks cardiogenesis and the transcription of downstream gene targets. J. Biol. Chem. 280, 32531-32538 (Pubitemid 41361867)
5. Schratt, G., Weinhold, B., Lundberg, A. S., Schuck, S., Berger, J., Schwarz, H., Weinberg, R. A., Ruther, U., and Nordheim, A. (2001) Serum response factor is required for immediate-early gene activation yet is dispensable for proliferation of embryonic Stem cells. Mol. Cell. Biol. 21, 2933-2943 (Pubitemid 32244935)
6. Norman, C., Runswick, M., Pollock, R., and Treisman, R. (1988) Isolation and properties of cDNA clones encoding SRF, a transcription factor that binds to the c-fos serum response element. Cell 55, 989-1003 (Pubitemid 19020052)
7. Boxer, L. M., Prywes, R., Roeder, R. G., and Kedes, L. (1989) The sarcomeric actin CArG-binding factor is indistinguishable from the c-fos serum response factor. Mol. Cell. Biol. 9, 515-522 (Pubitemid 19038856)
8. Hautmann, M. B., Madsen, C. S., Mack, C. P., and Owens, G. K. (1998) Substitution of the degenerate smooth muscle (SM) alpha-actin CC(A/T-rich)6GG elements with c-fos serum response elements results in increased basal expression but relaxed SM cell specificity and reduced angiotensin II inducibility. J. Biol. Chem. 273, 8398-8406 (Pubitemid 28168901)
9. Taylor, M., Treisman, R., Garrett, N., and Mohun, T. (1989) Muscle-specific (CArG) and serum-responsive (SRE) promoter elements are functionally interchangeable in Xenopus embryos and mouse fibroblasts. Development 106, 67-78 (Pubitemid 19150671)
10. Buchwalter, G., Gross, C., and Wasylyk, B. (2004) Ets ternary complex transcription factors. Gene 324, 1-14 (Pubitemid 38030321)
11. Treisman, R., and Ammerer, G. (1992) The SRF and MCM1 transcription factors. Curr. Opin. Genet. Dev. 2, 221-226
12. Belaguli, N. S., Sepulveda, J. L., Nigam, V., Charron, F., Nemer, M., and Schwartz, R. J. (2000) Cardiac tissue enriched factors serum response factor and GATA-4 are mutual coregulators. Mol. Cell. Biol. 20, 7550-7558
13. Cen, B., Selvaraj, A., and Prywes, R. (2004) Myocardin/MKL family of SRF coactivators: key regulators of immediate early and muscle specific gene expression. J. Cell. Biochem. 93, 74-82
14. Chen, C. Y., and Schwartz, R. J. (1996) Recruitment of the tinman homolog Nkx-2.5 by serum response factor activates cardiac alpha-actin gene transcription. Mol. Cell. Biol. 16, 6372-6384 (Pubitemid 26360996)
15. Groisman, R., Masutani, H., Leibovitch, M. P., Robin, P., Soudant, I., Trouche, D., and Harel-Bellan, A. (1996) Physical interaction between the mitogen-responsive serum response factor and myogenic basic-helix-loop-helix proteins. J. Biol. Chem. 271, 5258-5264 (Pubitemid 26075022)
16. Wang, D., Chang, P. S., Wang, Z., Sutherland, L., Richardson, J. A., Small, E., Krieg, P. A., and Olson, E. N. (2001) Activation of cardiac gene expression by myocardin, a transcriptional cofactor for serum response factor. Cell 105, 851-862 (Pubitemid 32635087)
17. Iyer, D., Chang, D., Marx, J., Wei, L., Olson, E. N., Parmacek, M. S., Balasubramanyam, A., and Schwartz, R. J. (2006) Serum response factor MADS box serine-162 phosphorylation switches proliferation and myogenic gene programs. Proc. Natl. Acad. Sci. U. S. A. 103, 4516-4521
18. Wang, Z., Wang, D. Z., Hockemeyer, D., McAnally, J., Nordheim, A., and Olson, E. N. (2004) Myocardin and ternary complex factors compete for SRF to control smooth muscle gene expression. Nature 428, 185-189 (Pubitemid 38374315)
19. Arsenian, S., Weinhold, B., Oelgeschlager, M., Ruther, U., and Nordheim, A. (1998) Serum response factor is essential for mesoderm formation during mouse embryogenesis. EMBO J. 17, 6289-6299 (Pubitemid 28497801)
20. Belaguli, N. S., Schildmeyer, L. A., and Schwartz, R. J. (1997) Organization and myogenic restricted expression of the murine serum response factor gene. A role for autoregulation. J. Biol. Chem. 272, 18222-18231 (Pubitemid 27306410)
21. Croissant, J. D., Kim, J. H., Eichele, G., Goering, L., Lough, J., Prywes, R., and Schwartz, R. J. (1996) Avian serum response factor expression restricted primarily to muscle cell lineages is required for alpha-actin gene transcription. Dev. Biol. 177, 250-264 (Pubitemid 26252496)
22. Baker, D. L., Dave, V., Reed, T., Misra, S., Periasamy, M. (1998) A novel E box/AT-rich element is required for muscle-specific expression of the sarcoplasmic reticulum Ca2+-ATPase (SERCA2) gene. Nucleic Acids Res. 26, 1092-1098 (Pubitemid 28291667)
23. 2+ exchanger gene. J. Biol. Chem. 274, 12819-12826
24. Rene, C., Taulan, M., Iral, F., Doudement, J., L'Honore, A., Gerbon, C., Demaille, J., Claustres, M., and Romey, M. C. (2005) Binding of serum response factor to cystic fibrosis transmembrane conductance regulator CArG-like elements, as a new potential CFTR transcriptional regulation pathway. Nucleic Acids Res. 33, 5271-5290
25. Nilsson, M., Dahlman-Wright, K., Karelmo, C., Ebeling, M., Gustafsson, J. A., and Steffensen, K. R. (2007) Elk1 and SRF transcription factors convey basal transcription and mediate glucose response via their binding sites in the human LXRB gene promoter. Nucleic Acids Res. 35, 4858-4868 (Pubitemid 47260296)
26. Contreras, J. L., Bilbao, G., Smyth, C. A., Jiang, X. L., Eckhoff, D. E., Jenkins, S. M., Thomas, F. T., Curiel, D. T., and Thomas, J. M. (2001) Cytoprotection of pancreatic islets before and soon after transplantation by gene transfer of the anti-apoptotic Bcl-2 gene. Transplantation 71, 1015-1023 (Pubitemid 32448812)
27. Gurzov, E. N., Ortis, F., Bakiri, L., Wagner, E. F., and Eizirik, D. L. (2008) JunB inhibits ER stress and apoptosis in pancreatic beta cells. PLoS One 3, e3030
28. Schratt, G., Philippar, U., Hockemeyer, D., Schwarz, H., Alberti, S., and Nordheim, A. (2004) SRF regulates Bcl-2 expression and promotes cell survival during murine embryonic development. EMBO J. 23, 1834-1844 (Pubitemid 38649646)
29. Selvaraj, A., and Prywes, R. (2004) Expression profiling of serum inducible genes identifies a subset of SRF target genes that are MKL dependent. BMC Mol. Biol. 5, 13
30. Miralles, F., Hebrard, S., Lamotte, L., Durel, B., Gilgenkrantz, H., Li, Z., Daegelen, D., Tuil, D., and Joshi, R. L. (2006) Conditional inactivation of the murine serum response factor in the pancreas leads to severe pancreatitis. Lab. Invest. 86, 1020-1036 (Pubitemid 44423067)
31. Barron, M. R., Belaguli, N. S., Zhang, S. X., Trinh, M., Iyer, D., Merlo, X., Lough, J. W., Parmacek, M. S., Bruneau, B. G., and Schwartz, R. J. (2005) Serum response factor, an enriched cardiac mesoderm obligatory factor, is a downstream gene target for Tbx genes. J. Biol. Chem. 280, 11816-11828 (Pubitemid 40418496)
32. Belaguli, N. S., Zhou, W., Trinh, T. H., Majesky, M. W., and Schwartz, R. J. (1999) Dominant negative murine serum response factor: alternative splicing within the activation domain inhibits transactivation of serum response factor binding targets. Mol. Cell. Biol. 19, 4582-4591 (Pubitemid 29289496)
33. Johansen, F. E., and Prywes, R. (1993) Identification of transcriptional activation and inhibitory domains in serum response factor (SRF) by using GAL4-SRF constructs. Mol. Cell. Biol. 13, 4640-4647
34. Liu, S. H., Ma, J. T., Yueh, A. Y., Lees-Miller, S. P., Anderson, C. W., and Ng, S. Y. (1993) The carboxyl-terminal transactivation domain of human serum response factor contains DNAactivated protein kinase phosphorylation sites. J. Biol. Chem. 268, 21147-21154 (Pubitemid 23292301)
35. Sun, K., Battle, M. A., Misra, R. P., and Duncan, S. A. (2009) Hepatocyte expression of serum response factor is essential for liver function, hepatocyte proliferation and survival, and postnatal body growth in mice. Hepatology 49, 1645-1654
36. Lu, M., Seufert, J., and Habener, J. F. (1997) Pancreatic beta-cell-specific repression of insulin gene transcription by CCAAT/enhancer-binding protein beta. Inhibitory interactions with basic helix-loop-helix transcription factor E47. J. Biol. Chem. 272, 28349-28359 (Pubitemid 27517780)
37. Pino, M. F., Ye, D. Z., Linning, K. D., Green, C. D., Wicksteed, B., Poitout, V., and Olson, L. K. (2005) Elevated glucose attenuates human insulin gene promoter activity in INS-1 pancreatic beta-cells via reduced nuclear factor binding to the A5/core and Z element. Mol. Endocrinol. 19, 1343-1360 (Pubitemid 40594129)
38. Sharma, A., Olson, L. K., Robertson, R. P., and Stein, R. (1995) The reduction of insulin gene transcription in HIT-T15 beta cells chronically exposed to high glucose concentration is associated with the loss of RIPE3b1 and STF-1 transcription factor expression. Mol. Endocrinol. 9, 1127-1134
39. Andrali, S. S., Sampley, M. L., Vanderford, N. L., and Ozcan, S. (2008) Glucose regulation of insulin gene expression in pancreatic beta-cells. Biochem. J. 415, 1-10
40. Kaneto, H., Miyatsuka, T., Kawamori, D., Yamamoto, K., Kato, K., Shiraiwa, T., Katakami, N., Yamasaki, Y., Matsuhisa, M., and Matsuoka, T. A. (2008) PDX-1 and MafA play a crucial role in pancreatic beta-cell differentiation and maintenance of mature beta-cell function. Endocr. J. 55, 235-252 (Pubitemid 351670948)
41. Crowe, D. T., and Tsai, M. J. (1989) Mutagenesis of the rat insulin II 5′-flanking region defines sequences important for expression in HIT cells. Mol. Cell Biol. 9, 1784-1789 (Pubitemid 19095220)
42. Karlsson, O., Edlund, T., Moss, J. B., Rutter, W. J., and Walker, M. D. (1987) A mutational analysis of the insulin gene transcription control region: expression in beta cells is dependent on two related sequences within the enhancer. Proc. Natl. Acad. Sci. U. S. A. 84, 8819-8823
43. Zhang, S. X., Garcia-Gras, E., Wycuff, D. R., Marriot, S. J., Kadeer, N., Yu, W., Olson, E. N., Garry, D. J., Parmacek, M. S., and Schwartz, R. J. (2005) Identification of direct serumresponse factor gene targets during Me2SO-induced P19 cardiac cell differentiation. J. Biol. Chem. 280, 19115-19126 (Pubitemid 41379618)
44. Miano, J. M., Long, X., and Fujiwara, K. (2007) Serum response factor: master regulator of the actin cytoskeleton and contractile apparatus. Am. J. Physiol. Cell Physiol. 292, C70-C81 (Pubitemid 46115122)
45. Bernal-Mizrachi, E., Wice, B., Inoue, H., and Permutt, M. A. (2000) Activation of serum response factor in the depolarization induction of Egr-1 transcription in pancreatic islet beta-cells. J. Biol. Chem. 275, 25681-25689
46. Treisman, R. (1992) The serum response element. Trends Biochem. Sci. 17, 423-426
47. Chen, Y., and Tye, B. K. (1995) The yeast Mcm1 protein is regulated posttranscriptionally by the flux of glycolysis. Mol. Cell. Biol. 15, 4631-4639
48. Escalante, R., Moreno, N., and Sastre, L. (2003) Dictyostelium discoideum developmentally regulated genes whose expression is dependent on MADS box transcription factor SrfA. Eukaryot. Cell 2, 1327-1335 (Pubitemid 38047240)
49. Black, B. L., and Olson, E. N. (1998) Transcriptional control of muscle development by myocyte enhancer factor-2 (MEF2) proteins. Annu. Rev. Cell Dev. Biol. 14, 167-196 (Pubitemid 29001453)
50. Wang, Z., and Thurmond, D. C. (2009) Mechanisms of biphasic insulin-granule exocytosis - roles of the cytoskeleton, small GTPases, and SNARE proteins. J. Cell Sci. 122, 893-903