Overexpression of the nuclear factor-κB subunit c-Rel protects against human islet cell death in vitro

American Journal of Physiology - Endocrinology and Metabolism

Volumn 297, Issue 5, 2009, Pages

  Mokhtari, Dariush ^a   Barbu, Andreea ^a   Mehmeti, Ilir ^b   Vercamer, Chantal ^c   Welsh, Nils ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c INSTITUT DE BIOLOGIE DE LILLE   (France)

Author keywords

cell apoptosis; Bcl X L; Caspase 3; Heat shock protein 72; Ribosomal protein S3

Indexed keywords

CASPASE 3; HEAT SHOCK PROTEIN 72; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN P105; PROTEIN P50; PROTEIN P52; RIBOSOMAL PROTEIN S3; RIBOSOME PROTEIN; SYNAPTOTAGMIN I; TRANSCRIPTION FACTOR REL; TRANSCRIPTION FACTOR RELB; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DEATH; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; MOUSE; NONHUMAN; PANCREAS ISLET CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; RAT;

ADENOVIRIDAE; ANIMALS; APOPTOSIS REGULATORY PROTEINS; BLOTTING, WESTERN; CELL DEATH; CELL SURVIVAL; COLORING AGENTS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; FEMALE; GENE EXPRESSION; GENETIC VECTORS; HUMANS; ISLETS OF LANGERHANS; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; MICROSCOPY, CONFOCAL; NF-KAPPA B; NUCLEAR PROTEINS; PERFUSION; PROTEIN SUBUNITS; RATS; RATS, SPRAGUE-DAWLEY; TETRAZOLIUM SALTS; THIAZOLES; TRANSDUCTION, GENETIC;

EID: 70350455734     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00212.2009     Document Type: Article

References (52)

1. Ammirante M, Rosati A, Gentilella A, Festa M, Petrella A, Marzullo L, Pascale M, Belisario MA, Leone A, Turco MC. The activity of hsp90 alpha promoter is regulated by NF-kappa B transcription factors. Oncogene 27: 1175-1178, 2008. (Pubitemid 351253180)
2. Ankarcrona M, Dypbukt JM, Brune B, Nicotera P. Interleukin-1 β-induced nitric oxide production activates apoptosis in pancreatic RINm5F cells. Exp Cell Res 213: 172-177, 1994. (Pubitemid 2101572)
3. Barbu A, Akusjärvi G, Welsh N. Adenoviral induced islet cell cytotoxicity is not counteracted by Bcl-2 overexpression. Mol Med 8: 733-741, 2002. (Pubitemid 36337500)
4. Barbu AR, Akusjarvi G, Welsh N. Adenoviral-mediated transduction of human pancreatic islets: importance of adenoviral genome for cell viability and association with a deficient antiviral response. Endocrinology 146: 2406-2414, 2005. (Pubitemid 40577528)
5. Barbu AR, Bodin B, Welsh M, Jansson L, Welsh N. A perfusion protocol for highly efficient transduction of intact pancreatic islets of Langerhans. Diabetologia 49: 2388-2391, 2006. (Pubitemid 44359100)
6. Barbu A, Welsh N, Saldeen J. Cytokine-induced apoptosis and necrosis are preceded by disruption of the mitochondrial membrane potential [Deltapsi(m)] in pancreatic RIN-5AH cells: prevention by Bcl-2. Mol Cell Endocrinol 190: 75-82, 2002. (Pubitemid 34462053)
7. Beere HM. Death versus survival: functional interaction between the apoptotic and stress-inducible heat shock protein pathways. J Clin Invest 115: 2633-2639, 2005.
8. Borg LAH, Cagliero E, Sandler S, Welsh N, Eizirik DL. Interleukin-1β increases the activity of superoxide dismutase in rat pancreatic islets. Endocrinology 130: 2851-2857, 1992.
9. Cardo AK, Heimberg H, Heremans Y, Leeman R, Kutlu B, Kruhoffer M, Orntoft T, Eizirik DL. A comprehensive analysis of cytokine-induced and nuclear factor-kappa B-dependent genes in primary rat pancreatic β-cells. J Biol Chem 276: 48879-48886, 2001. (Pubitemid 37370587)
10. Choi SH, Kim SY, An JJ, Lee SH, Kim DW, Ryu HJ, Lee NI, Yeo SI, Jang SH, Won MH, Kang TC, Kwon HJ, Cho SW, Kim J, Lee KS, Park J, Eum WS, Choi SY. Human PEP-1-ribosomal protein S3 protects against UV-induced skin cell death. FEBS Lett 580: 6755-6762, 2006.
11. Cimmino A, Calin GA, Fabbri M, Iorio MV, Ferracin M, Shimizu M, Wojcik SE, Aqeilan RI, Zupo S, Dono M, Rassenti L, Alder H, Volinia S, Liu CG, Kipps TJ, Negrini M, Croce CM. miR-15 and miR-16 induce apoptosis by targeting BCL2. Proc Natl Acad Sci USA 102: 13944-13949, 2005. (Pubitemid 41377683)
12. Eizirik DL, Cagliero E, Björklund A, Welsh N. Interleukin-1β induces the expression of an isoform of nitric oxide synthase in insulin-producing cells, which is similar to that observed in activated macrophages. FEBS Lett 308: 249-252, 1992.
13. Eizirik DL, Flodström M, Karlsen EA, Welsh N. The harmony of the spheres: inducible nitric oxide synthase and related genes in pancreatic β cells. Diabetologia 39: 875-890, 1996. (Pubitemid 26249106)
14. Eizirik DL, Sandler S, Welsh N, Cetkovic-Cvrlje M, Nieman A, Geller DA, Pipeleers DG, Bendtzen K, Hellerström C. Cytokines suppress human islet function irrespective of their effects on nitric oxide generation. J Clin Invest 93: 1968-1974, 1994.
15. Eldor R, Yeffet A, Baum K, Doviner V, Amar D, Ben-Neriah Y, Christofori G, Peled A, Carel JC, Boitard C, Klein T, Serup P, Eizirik DL, Melloul D. Conditional and specific NF-kappaB blockade protects pancreatic β cells from diabetogenic agents. Proc Natl Acad Sci USA 103: 5072-5077, 2006.
16. Flodström M, Welsh N, Eizirik DL. Cytokines activate the nuclear factor kB (NF-κB) and induces nitric oxide production in human pancreatic islets. FEBS Lett 385: 4-6, 1996. (Pubitemid 126334541)
17. Ghobrial IM, Witzig TE, Adjeji AA. Targeting apoptosis pathways in cancer therapy. CA Cancer J Clin 55: 178-194, 2005. (Pubitemid 40826487)
18. Hägerkvist R, Sandler S, Mokhtari D, Welsh N. Amelioration of diabetes by imatinib mesylate (Gleevec): role of β-cell NF-kappaB activation and anti-apoptotic preconditioning. FASEB J 21: 618-628, 2007. (Pubitemid 46213508)
19. Hammar EB, Irminger JC, Rickenbach K, Parnaud G, Ribaux P, Bosco D, Rouiller DG, Halban PA. Activation of NF-kappaB by extracellular matrix is involved in spreading and glucose-stimulated insulin secretion of pancreatic β cells. J Biol Chem 280: 30630-30637, 2005. (Pubitemid 41216249)
20. Huang YH, Wu JY, Zhang Y, Wu MX. Synergistic and opposing regulation of the stress-responsive gene IEX-1 by p53, c-Myc, and multiple NF-κB/rel complexes. Oncogene 21: 6819-6828, 2002. (Pubitemid 35221924)
21. Hwang IK, Yoo KY, Kim DW, Kim SY, Park JH, Ryoo ZY, Kim J, Choi SY, Won MH. Ischemia-induced ribosomal protein S3 expressional changes and the neuroprotective effect against experimental cerebral ischemic damage. J Neurosci Res 86: 1823-1835, 2008.
22. Ingelsson E, Saldeen J, Welsh N. Islet expression of perforin, FAS/ APO-1 and interleukin-1 converting enzyme (ICE) in non-obese diabetic (NOD) mice. Immunol Lett 63: 125-129, 1998. (Pubitemid 28522297)
23. Jang CY, Lee JY, Kim J. RpS3, a DNA repair endonuclease and ribosomal protein, is involved in apoptosis. FEBS Lett 560: 81-85, 2004. (Pubitemid 38264297)
24. John NE, Andersen HU, Fey SJ, Larsen PM, Roepstorff P, Larsen MR, Pociot F, Karlsen AE, Nerup J, Green IC, Mandrup-Poulsen T. Cytokine- or chemically derived nitric oxide alters the expression of proteins detected by two-dimentsional gel electrophoresis in neonatal rat islets of Langerhans. Diabetes 49: 1819-1829, 2000.
25. Karin M, Cao Y, Greten FR, Li ZW. NF-kappaB in cancer: from innocent bystander to major culprit. Nat Rev Cancer 2: 301-310, 2002. (Pubitemid 37328783)
26. Kassardjian A, Kreydiyyeh SI. JNK modulates the effect of caspases and NF-kappaB in the TNF-alpha-induced down-regulation of Na+/K+ATPase in HepG2 cells. J Cell Physiol 216: 615-620, 2008.
27. Kim S, Millet I, Kim HS, Kim JY, Han MS, Lee MK, Kim KW, Sherwin RS, Karin M, Lee MS. NF-kappa B prevents β cell death and autoimmune diabetes in NOD mice. Proc Natl Acad Sci USA 104: 1913-1918, 2007.
28. Kretz-Remy C, Bates EE, Arrigo AP. Amino acid analogs activate NF-kappaB through redox-dependent IkappaB-alpha degradation by the proteasome without apparent IkappaB-alpha phosphorylation. Consequence on HIV-1 long terminal repeat activation. J Biol Chem 273: 3180-3191, 1998. (Pubitemid 28109726)
29. Kucharczak J, Simmons MJ, Fan Y, Gélinas C. To be, or not to be: NF-κB is the answer-role of Rel/NF-κB in the regulation of apoptosis. Oncogene 2: 8961-8982, 2003. (Pubitemid 38121698)
30. Lavrovsky Y, Schwartzman ML, Abraham NG. Novel regulatory sites of the human heme oxygenase-1 promoter region. Biochem Biophys Res Commun 196: 336-341, 1993. (Pubitemid 23309512)
31. Liuwantara D, Elliot M, Smith MW, Yam AO, Walters SN, Marino E, McShea A, Grey ST. Nuclear factor-κB regulates β-cell death: a critical role for A20 in β-cell protection. Diabetes 55: 2491-2501, 2006. (Pubitemid 44871149)
32. Mauricio D, Mandrup-Poulsen T. Apoptosis and the pathogenesis of IDDM: a question of life and death. Diabetes 47: 1537-1543, 1998. (Pubitemid 28445339)
33. Norlin S, Ahlgren U, Edlund H. Nuclear Factor-κB activity in β-cells is required for glucose-stimulated insulin secretion. Diabetes 54: 125-131, 2005. (Pubitemid 40105103)
34. Ortis F, Pirot P, Naamane N, Kreins AY, Rasschaert J, Moore F, Théâtre E, Verhaeghe C, Magnusson NE, Chariot A, Orntoft TF, Eizirik DL. Induction of nuclear factor-kappaB and its downstream genes by TNF-alpha and IL-1β has a pro-apoptotic role in pancreatic β cells. Diabetologia 51: 1213-1225, 2008.
35. Pomerantz JL, Baltimore D. Two pathways to NF-kappaB. Mol Cell 10: 41-45, 2002.
36. Rabson AB, Weissmann D. From microarray to bedside: targeting NF-kappaB for therapy of lymphomas. Clin Cancer Res 11: 2-6, 2005.
37. Sakar SA, Kutlu B, Velmuruga K, Kizaka-Kondoh S, Lee CE, Wong R, Valentine A, Davidson HW, Hutton JC, Pugazhenthi S. Cytokine-mediated induction of anti-apoptotic genes that are linked to nuclear factor kappa-βB (NF-βB) signaling in human islets and in a mouse β cell line. Diabetologia 52: 1092-1101, 2009.
38. Saldeen J. Cytokines induce both necrosis and apoptosis via a common Bcl-2-inhibitable pathway in rat insulin-producing cells. Endocrinology 141: 2003-2010, 2000. (Pubitemid 32274349)
39. Saldeen J, Jaffrézou JP, Welsh N. The acid sphingomyelinase inhibitor SR33557 counteracts TNF-α-mediated potentiation of IL-1β induced NF-κB activation in the insulin-producing cell line RINm5F. Autoimmunity 32: 241-254, 2000. (Pubitemid 32043779)
40. Saldeen J, Welsh N. Interleukin-1β induced activation of NF-κB in insulin producing RINm5F cells is prevented by the protease inhibitor tosyl-lysine chloromethyl ketone. Biochem Biophys Res Commun 203: 149-155, 1994. (Pubitemid 2124629)
41. Schumann DM, Maedler K, Franklin I, Konrad D, Størling J, Böni- Schnetzler M, Gjinovci A, Kurrer MO, Gauthier BR, Bosco D, Andres A, Berney T, Greter M, Becher B, Chervonsky AV, Halban PA, Mandrup-Poulsen T, Wollheim CB, Donath MY. The Fas pathway is involved in pancreatic β cell secretory function. Proc Natl Acad Sci USA 104: 2861-2866, 2007. (Pubitemid 46327970)
42. Strandell E, Buschard K, Saldeen J, Welsh N. Interleukin-1β induces the expression of HSP70, heme oxygenase and Mn-SOD in FACS-purified rat islet β-cells, but not in α-cells. Immunol Lett 48: 145-148, 1995. (Pubitemid 3011949)
43. Thomas HE, Angstetra E, Fernandes RV, Mariana L, Irawaty W, Jamieson EL, Dudek NL, Kay TW. Perturbations in nuclear factor-kappaB or c-Jun N-terminal kinase pathways in pancreatic β cells confer susceptibility to cytokine-induced cell death. Immunol Cell Biol 84: 20-27, 2006.
44. Varfolomeev E, Vucic D. (Un)expected roles of c-IAPs in apoptotic and NFkappaB signaling pathways. Cell Cycle 7: 1511-1521, 2008. (Pubitemid 351881313)
45. Wan F, Anderson DE, Barnitz RA, Snow A, Bidere N, Zheng L, Hegde V, Lam LT, Staudt LM, Levens D, Deutsch WA, Lenardo MJ. Ribosomal protein S3: a KH domain subunit in NF-kappaB complexes that mediates selective gene regulation. Cell 131: 927-939, 2007. (Pubitemid 350138085)
46. Welsh N, Eizirik DL, Bendtzen K, Sandler S. Interleukin-1 β-induced nitric oxide production in isolated rat pancreatic islets requires gene transcription and may lead to inhibition of the Krebs cycle enzyme aconitase. Endocrinology 129: 3167-3173, 1991.
47. Welsh N, Eizirik DL, Sandler S. Nitric oxide and pancreatic β-cell destruction in insulin dependent diabetes mellitus: don't take NO for an answer. Autoimmunity 18: 285-290, 1994. (Pubitemid 24350977)
48. Welsh N, Welsh M, Lindquist S, Eizirik D, Bendtzen K, Sandler S. Interleukin-1β increases the biosynthesis of the heat shock protein hsp-70 and decreases the biosynthesis of five specific proteins in rat pancreatic islets. Autoimmunity 9: 33-40, 1991.
49. Welsh N, Sandler S. Protective action by hemin against interleukin-1β induced inhibition of rat pancreatic islet function. Mol Cell Endocrinol 103: 109-114, 1994. (Pubitemid 24195552)
50. Wollheim CB, Meda P, Halban PA. Isolation of pancreatic islets and primary culture of the intact microorgans or of dispersed islet cells. Methods Enzymol 192: 188-223, 1990.
51. Xiao C, Ghosh S. NF-kappaB, an evolutionarily conserved mediator of immune and inflammatory responses. Adv Exp Med Biol 560: 41-45, 2005. (Pubitemid 43759173)
52. Xiao G, Harhaj EW, Sun SC. NF-kappaB-inducing kinase regulates the processing of NF-kappaB2 p100. Mol Cell 7: 401-409, 2001. (Pubitemid 32206507)