CREB mediates the insulinotropic and anti-apoptotic effects of GLP-1 signaling in adult mouse β-cells

Molecular Metabolism

Volumn 3, Issue 8, 2014, Pages 803-812

  Shin, Soona ^a   Le Lay, John ^a   Everett, Logan J ^a   Gupta, Rana ^a   Rafiq, Kiran ^a   Kaestner, Klaus H ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Apoptosis; CAMP signaling; Conditional gene ablation; CREB; Leucine zipper transcription factor; P21

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR 1A; GLUCAGON LIKE PEPTIDE 1;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CDKN1A GENE; CELL METABOLISM; CELL VOLUME; CONTROLLED STUDY; FEMALE; GENE DELETION; GENE OVEREXPRESSION; GLUCOSE HOMEOSTASIS; INSULIN LIKE ACTIVITY; INSULIN RELEASE; MALE; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

EID: 84908208784     PISSN: None     EISSN: 22128778     Source Type: Journal    
DOI: 10.1016/j.molmet.2014.08.001     Document Type: Article

References (59)

1. Mayr B., Montminy M. Transcriptional regulation by the phosphorylation-dependent factor CREB. Nature Reviews Molecular Cell Biology 2001, 2(8):599-609.
2. Oetjen E., et al. Distinct properties of the cAMP-responsive element of the rat insulin I gene. The Journal of Biological Chemistry 1994, 269(43):27036-27044.
3. Miller C.P., Lin J.C., Habener J.F. Transcription of the rat glucagon gene by the cyclic AMP response element-binding protein CREB is modulated by adjacent CREB-associated proteins. Molecular and Cellular Biology 1993, 13(11):7080-7090.
4. Schwaninger M., et al. Membrane depolarization and calcium influx induce glucagon gene transcription in pancreatic islet cells through the cyclic AMP-responsive element. The Journal of Biological Chemistry 1993, 268(7):5168-5177.
5. Montminy M.R., Bilezikjian L.M. Binding of a nuclear protein to the cyclic-AMP response element of the somatostatin gene. Nature 1987, 328(6126):175-178.
6. Novials A., et al. Mutation at position -132 in the islet amyloid polypeptide (IAPP) gene promoter enhances basal transcriptional activity through a new CRE-like binding site. Diabetologia 2004, 47(7):1167-1174.
7. Sarkar S.A., et al. Dominant negative mutant forms of the cAMP response element binding protein induce apoptosis and decrease the anti-apoptotic action of growth factors in human islets. Diabetologia 2007, 50(8):1649-1659.
8. Kim M.J., et al. Exendin-4 induction of cyclin D1 expression in INS-1 beta-cells: involvement of cAMP-responsive element. Journal of Endocrinology 2006, 188(3):623-633.
9. Velmurugan K., et al. Antiapoptotic actions of exendin-4 against hypoxia and cytokines are augmented by CREB. Endocrinology 2012, 153(3):1116-1128.
10. Klinger S., et al. Increasing GLP-1-induced beta-cell proliferation by silencing the negative regulators of signaling cAMP response element modulator-alpha and DUSP14. Diabetes 2008, 57(3):584-593.
11. Skoglund G., Hussain M.A., Holz G.G. Glucagon-like peptide 1 stimulates insulin gene promoter activity by protein kinase A-independent activation of the rat insulin I gene cAMP response element. Diabetes 2000, 49(7):1156-1164.
12. Sonoda N., et al. Beta-Arrestin-1 mediates glucagon-like peptide-1 signaling to insulin secretion in cultured pancreatic beta cells. Proceedings of the National Academy of Sciences of the United States of America 2008, 105(18):6614-6619.
13. Yabe D., Seino Y. Two incretin hormones GLP-1 and GIP: comparison of their actions in insulin secretion and beta cell preservation. Progress in Biophysics & Molecular Biology 2011, 107(2):248-256.
14. Garber A.J., Spann S.J. An overview of incretin clinical trials. The Journal of Family Practice 2008, 57(9 Suppl.):S10-S18.
15. Li Y., et al. Glucagon-like peptide-1 receptor signaling modulates beta cell apoptosis. The Journal of Biological Chemistry 2003, 278(1):471-478.
16. Wang Q., Brubaker P.L. Glucagon-like peptide-1 treatment delays the onset of diabetes in 8 week-old db/db mice. Diabetologia 2002, 45(9):1263-1273.
17. Rudolph D., et al. Impaired fetal T cell development and perinatal lethality in mice lacking the cAMP response element binding protein. Proceedings of the National Academy of Sciences of the United States of America 1998, 95(8):4481-4486.
18. Jhala U.S., et al. cAMP promotes pancreatic beta-cell survival via CREB-mediated induction of IRS2. Genes & Development 2003, 17(13):1575-1580.
19. Inada A., et al. Overexpression of inducible cyclic AMP early repressor inhibits transactivation of genes and cell proliferation in pancreatic beta cells. Molecular and Cellular Biology 2004, 24(7):2831-2841.
20. Ahn S., et al. Adominant-negative inhibitor of CREB reveals that it is a general mediator of stimulus-dependent transcription of c-fos. Molecular and Cellular Biology 1998, 18(2):967-977.
21. Copeland N.G., Jenkins N.A., Court D.L. Recombineering: a powerful new tool for mouse functional genomics. Nature Reviews Genetics 2001, 2(10):769-779.
22. Holzenberger M., et al. Cre-mediated germline mosaicism: a method allowing rapid generation of several alleles of a target gene. Nucleic Acids Research 2000, 28(21):E92.
23. Gu G., Dubauskaite J., Melton D.A. Direct evidence for the pancreatic lineage: NGN3+ cells are islet progenitors and are distinct from duct progenitors. Development 2002, 129(10):2447-2457.
24. Heiser P.W., et al. Stabilization of beta-catenin impacts pancreas growth. Development 2006, 133(10):2023-2032.
25. Scharp D.W., et al. The use of ficoll in the preparation of viable islets of langerhans from the rat pancreas. Transplantation 1973, 16(6):686-689.
26. Cornu M., et al. Glucagon-like peptide-1 protects beta-cells against apoptosis by increasing the activity of an IGF-2/IGF-1 receptor autocrine loop. Diabetes 2009, 58(8):1816-1825.
27. Mohanty S., et al. Overexpression of IRS2 in isolated pancreatic islets causes proliferation and protects human beta-cells from hyperglycemia-induced apoptosis. Experimental Cell Research 2005, 303(1):68-78.
28. Rieck S., et al. The transcriptional response of the islet to pregnancy in mice. Molecular Endocrinology 2009, 23(10):1702-1712.
29. Tuteja G., et al. Cis-regulatory modules in the mammalian liver: composition depends on strength of Foxa2 consensus site. Nucleic Acids Research 2008, 36(12):4149-4157.
30. Le Lay J., et al. CRTC2 (TORC2) contributes to the transcriptional response to fasting in the liver but is not required for the maintenance of glucose homeostasis. Cell Metabolism 2009, 10(1):55-62.
31. Heinz S., et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Molecular Cell 2010, 38(4):576-589.
32. Bramswig N.C., et al. Epigenomic plasticity enables human pancreatic alpha to beta cell reprogramming. The Journal of Clinical Investigation 2013, 123(3):1275-1284.
33. Langmead B., et al. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biology 2009, 10(3):R25.
34. Grant G.R., et al. Comparative analysis of RNA-Seq alignment algorithms and the RNA-Seq unified mapper (RUM). Bioinformatics 2011, 27(18):2518-2528.
35. Lee D., Le Lay J., Kaestner K.H. The transcription factor CREB has no non-redundant functions in hepatic glucose metabolism in mice. Diabetologia 2014, 57(6):1242-1248.
36. Hummler E., et al. Targeted mutation of the CREB gene: compensation within the CREB/ATF family of transcription factors. Proceedings of the National Academy of Sciences of the United States of America 1994, 91(12):5647-5651.
37. Valverde O., et al. Modulation of anxiety-like behavior and morphine dependence in CREB-deficient mice. Neuropsychopharmacology 2004, 29(6):1122-1133.
38. Blendy J.A., et al. Targeting of the CREB gene leads to up-regulation of a novel CREB mRNA isoform. EMBO Journal 1996, 15(5):1098-1106.
39. Dobrian A.D., et al. Dipeptidyl peptidase IV inhibitor sitagliptin reduces local inflammation in adipose tissue and in pancreatic islets of obese mice. American Journal of Physiology. Endocrinology and Metabolism 2011, 300(2):E410-E421.
40. Donath M.Y., et al. Islet inflammation impairs the pancreatic beta-cell in type 2 diabetes. Physiology 2009, 24:325-331.
41. Ferdaoussi M., et al. Exendin-4 protects beta-cells from interleukin-1 beta-induced apoptosis by interfering with the c-Jun NH2-terminal kinase pathway. Diabetes 2008, 57(5):1205-1215.
42. Natalicchio A., et al. Exendin-4 prevents c-Jun N-terminal protein kinase activation by tumor necrosis factor-alpha (TNFalpha) and inhibits TNFalpha-induced apoptosis in insulin-secreting cells. Endocrinology 2010, 151(5):2019-2029.
43. Huo J.X., Metz S.A., Li G.D. p53-independent induction of p21(waf1/cip1) contributes to the activation of caspases in GTP-depletion-induced apoptosis of insulin-secreting cells. Cell Death & Differentiation 2004, 11(1):99-109.
44. Kaneto H., et al. Oxidative stress induces p21 expression in pancreatic islet cells: possible implication in beta-cell dysfunction. Diabetologia 1999, 42(9):1093-1097.
45. Yamada T., et al. WFS1-deficiency increases endoplasmic reticulum stress, impairs cell cycle progression and triggers the apoptotic pathway specifically in pancreatic beta-cells. Human Molecular Genetics 2006, 15(10):1600-1609.
46. Zhang S., et al. Induction of apoptosis by human amylin in RINm5F islet beta-cells is associated with enhanced expression of p53 and p21WAF1/CIP1. FEBS Letters 1999, 455(3):315-320.
47. Hussain M.A., et al. Increased pancreatic beta-cell proliferation mediated by CREB binding protein gene activation. Molecular and Cellular Biology 2006, 26(20):7747-7759.
48. Kudo K., et al. Aselective increase in phosphorylation of cyclic AMP response element-binding protein in hippocampal CA1 region of male, but not female, rats following contextual fear and passive avoidance conditioning. Brain Research 2004, 1024(1-2):233-243.
49. Lin Y., et al. Sex differences in the effects of acute and chronic stress and recovery after long-term stress on stress-related brain regions of rats. Cerebral Cortex 2009, 19(9):1978-1989.
50. Mogi K., et al. Sex difference in the response of melanin-concentrating hormone neurons in the lateral hypothalamic area to glucose, as revealed by the expression of phosphorylated cyclic adenosine 3',5'-monophosphate response element-binding protein. Endocrinology 2005, 146(8):3325-3333.
51. Hai T., Curran T. Cross-family dimerization of transcription factors Fos/Jun and ATF/CREB alters DNA binding specificity. Proceedings of the National Academy of Sciences of the United States of America 1991, 88(9):3720-3724.
52. Ryseck R.P., Bravo R. c-JUN, JUN B, and JUN D differ in their binding affinities to AP-1 and CRE consensus sequences: effect of FOS proteins. Oncogene 1991, 6(4):533-542.
53. Sassone-Corsi P. Transcription factors responsive to cAMP. Annual Review of Cell and Developmental Biology 1995, 11:355-377.
54. Molina C.A., et al. Inducibility and negative autoregulation of CREM: an alternative promoter directs the expression of ICER, an early response repressor. Cell 1993, 75(5):875-886.
55. Stehle J.H., et al. Adrenergic signals direct rhythmic expression of transcriptional repressor CREM in the pineal gland. Nature 1993, 365(6444):314-320.
56. Seino S., et al. Roles of cAMP signalling in insulin granule exocytosis. Diabetes Obesity and Metabolism 2009, 11(Suppl.4):180-188.
57. Melnikova V.O., et al. CREB inhibits AP-2alpha expression to regulate the malignant phenotype of melanoma. PLoS One 2010, 5(8):e12452.
58. Pellegrini M., et al. Expression profile of CREB knockdown in myeloid leukemia cells. BMC Cancer 2008, 8:264.
59. Du J., et al. HIF-1alpha deletion partially rescues defects of hematopoietic stem cell quiescence caused by Cited2 deficiency. Blood 2012, 119(12):2789-2798.