JNK1/2 regulates ER-mitochondrial Ca2+ cross-talk during IL-1β-mediated cell death in RINm5F and human primary β-cells

Molecular Biology of the Cell

Volumn 24, Issue 12, 2013, Pages 2058-2071

  Verma, Gaurav ^a   Bhatia, Himanshi ^a   Datta, Malabika ^a  

^a CSIR INSTITUTE OF GENOMICS AND INTEGRATIVE BIOLOGY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM ION; INSULIN; INTERLEUKIN 1BETA; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; MITOGEN ACTIVATED PROTEIN KINASE P38; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE 1;

APOPTOSIS; ARTICLE; CALCIUM TRANSPORT; CELL DEATH; CELL ORGANELLE; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; INSULIN RELEASE; MITOCHONDRIAL MEMBRANE POTENTIAL; MOLECULAR INTERACTION; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN DEPLETION; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ADENOSINE TRIPHOSPHATE; ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CALCIUM; CELL LINE, TUMOR; CELLS, CULTURED; ENDOPLASMIC RETICULUM; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; INSULIN-SECRETING CELLS; INTERLEUKIN-1BETA; MACROCYCLIC COMPOUNDS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICROSCOPY, FLUORESCENCE; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; MITOGEN-ACTIVATED PROTEIN KINASE 8; MITOGEN-ACTIVATED PROTEIN KINASE 9; MODELS, BIOLOGICAL; OXAZOLES; PERMEABILITY; RATS; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE;

EID: 84879591081     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E12-12-0885     Document Type: Article

References (55)

1. Abdelli S, Bonny C (2012). JNK3 maintains expression of the insulin receptor substrate 2 (IRS2) in insulin-secreting cells: Functional consequences for insulin signaling. PLoS One 7, e35997.
2. Abdelli S, Puyal J, Bielmann C, Buchillier V, Abderrahmani A, Clarke PG, Beckmann JS, Bonny C (2009). JNK3 is abundant in insulin-secreting cells and protects against cytokine-induced apoptosis. Diabetologia 52, 1871-1880.
3. Bonny C, Oberson A, Steinmann M, Schorderet DF, Nicod P, Waeber G (2000). IB1 reduces cytokine-induced apoptosis of insulin-secreting cells. J Biol Chem 275, 16466-16472. (Pubitemid 30398867)
4. Bradford PG, Maglich JM, Kirkwood KL (2000). IL-1 beta increases type 1 inositol trisphosphate receptor expression and IL-6 secretory capacity in osteoblastic cell cultures. Mol Cell Biol Res Commun 3, 73-75. (Pubitemid 30252131)
5. Cardozo AK, Ortis F, Storling J, Feng YM, Rasschaert J, Tonnesen M, Van EF, Mandrup-Poulsen T, Herchuelz A, Eizirik DL (2005). Cytokines downregulate the sarcoendoplasmic reticulum pump Ca2+ ATPase 2b and deplete endoplasmic reticulum Ca2+, leading to induction of endoplasmic reticulum stress in pancreatic beta-cells. Diabetes 54, 452-461.
6. Chen L, Koh DS, Hille B (2003). Dynamics of calcium clearance in mouse pancreatic beta-cells. Diabetes 52, 1723-1731. (Pubitemid 36792463)
7. Collier JJ, Burke SJ, Eisenhauer ME, Lu D, Sapp RC, Frydman CJ, Campagna SR (2011). Pancreatic beta-cell death in response to pro-inflammatory cytokines is distinct from genuine apoptosis. PLoS One 6, e22485.
8. Corbett JA, McDaniel ML (1994). Reversibility of interleukin-1 beta-induced islet destruction and dysfunction by the inhibition of nitric oxide synthase. Biochem J 299, 719-724.
9. Corbett JA, Wang JL, Hughes JH, Wolf BA, Sweetland MA, Lancaster JR Jr, McDaniel ML (1992). Nitric oxide and cyclic GMP formation induced by interleukin 1 beta in islets of Langerhans. Evidence for an effector role of nitric oxide in islet dysfunction. Biochem J 287, 229-235.
10. Csordas G, Renken C, Varnai P, Walter L, Weaver D, Buttle KF, Balla T, Mannella CA, Hajnóczky G (2006). Structural and functional features and significance of the physical linkage between ER and mitochondria. J Cell Biol 174, 915-921. (Pubitemid 44455180)
11. Csordas G, Varnai P, Golenar T, Roy S, Purkins G, Schneider TG, Balla T, Hajnóczky G (2010). Imaging interorganelle contacts and local calcium dynamics at the ER-mitochondrial interface. Mol Cell 39, 121-132.
12. Davis RJ (2000). Signal transduction by the JNK group of MAP kinases. Cell 103, 239-252.
13. de Brito OM, Scorrano L (2010). An intimate liaison: Spatial organization of the endoplasmic reticulum-mitochondria relationship. EMBO J 29, 2715-2723.
14. Deniaud A, Sharaf el dein O, Maillier E, Poncet D, Kroemer G, Lemaire C, Brenner C (2008). Endoplasmic reticulum stress induces calcium-dependent permeability transition, mitochondrial outer membrane permeabilization and apoptosis. Oncogene 27, 285-299.
15. Dula SB, Jecmenica M, Wu R, Jahanshahi P, Verrilli GM, Carter JD, Brayman KL, Nunemaker CS (2010). Evidence that low-grade systemic inflammation can induce islet dysfunction as measured by impaired calcium handling. Cell Calcium 48, 133-142.
16. Filippin L, Magalhaes PJ, Di BG, Colella M, Pozzan T (2003). Stable interactions between mitochondria and endoplasmic reticulum allow rapid accumulation of calcium in a subpopulation of mitochondria. J Biol Chem 278, 39224-39234. (Pubitemid 37221826)
17. Giorgi C, De SD, Bononi A, Rizzuto R, Pinton P (2009). Structural and functional link between the mitochondrial network and the endoplasmic reticulum. Int J Biochem Cell Biol 41, 1817-1827.
18. Green DR, Kroemer G (2004). The pathophysiology of mitochondrial cell death. Science 305, 626-629. (Pubitemid 39006738)
19. Grunnet LG, Aikin R, Tonnesen MF, Paraskevas S, Blaabjerg L, Storling J, Rosenberg L, Billestrup N, Maysinger D, Mandrup-Poulsen T (2009). Proinflammatory cytokines activate the intrinsic apoptotic pathway in beta-cells. Diabetes 58, 1807-1815.
20. Gurzov EN, Ortis F, Cunha DA, Gosset G, Li M, Cardozo AK, Eizirik DL (2009). Signaling by IL-1beta+IFN-gamma and ER stress converge on DP5/Hrk activation: A novel mechanism for pancreatic beta-cell apoptosis. Cell Death Differ 16, 1539-1550.
21. Hajnóczky G, Csordás G, Das S, Garcia-Perez C, Saotome M, Sinha RS, Yi M (2006). Mitochondrial calcium signalling and cell death: Approaches for assessing the role of mitochondrial Ca2+ uptake in apoptosis. Cell Calcium 40, 553-560. (Pubitemid 44660721)
22. Kim EK, Kwon KB, Song MY, Han MJ, Lee JH, Lee YR, Lee JH, Ryu DG, Park BH, Park JW (2007). Flavonoids protect against cytokine-induced pancreatic beta-cell damage through suppression of nuclear factor kappaB activation. Pancreas 35, e1-e9.
23. Kim J, Xu M, Xo R, Mates A, Wilson GL, Pearsall AW, Grishko V (2010). Mitochondrial DNA damage is involved in apoptosis caused by pro-inflammatory cytokines in human OA chondrocytes. Osteoarthritis Cartilage 18, 424-432.
24. Kirichok Y, Krapivinsky G, Clapham DE (2004). The mitochondrial calcium uniporter is a highly selective ion channel. Nature 427, 360-364. (Pubitemid 38133664)
25. Kornmann B, Walter P (2010). ERMES-mediated ER-mitochondria contacts: Molecular hubs for the regulation of mitochondrial biology. J Cell Sci 123, 1389-1393.
26. Larsen CM, Faulenbach M, Vaag A, Volund A, Ehses JA, Seifert B, Mandrup-Poulsen T, Donath MY (2007). Interleukin-1-receptor antagonist in type 2 diabetes mellitus. N Engl J Med 356, 1517-1526. (Pubitemid 46588416)
27. Lee B, Laychock SG (2000). Regulation of inositol trisphosphate receptor isoform expression in glucose-desensitized rat pancreatic islets: Role of cyclic adenosine 3',5'-monophosphate and calcium. Endocrinology 141, 1394-402. (Pubitemid 32269107)
28. Maedler K, Sergeev P, Ris F, Oberholzer J, Joller-Jemelka HI, Spinas GA, Kaiser N, Halban PA, Donath MY (2002). Glucose-induced beta cell production of IL-1beta contributes to glucotoxicity in human pancreatic islets. J Clin Invest 110, 851-860.
29. Maedler K, Storling J, Sturis J, Zuellig RA, Spinas GA, Arkhammar PO, Mandrup-Poulsen T, Donath MY (2004). Glucose-and interleukin-1beta-induced beta-cell apoptosis requires Ca2 +influx and extracellular signal-regulated kinase (ERK) 1/2 activation and is prevented by a sulfonylurea receptor 1/inwardly rectifying K+ channel 6.2 (SUR/Kir6.2) selective potassium channel opener in human islets. Diabetes 53, 1706-1713. (Pubitemid 38857028)
30. Major CD, Wolf BA (2001). Interleukin-1beta stimulation of c-Jun NH(2)-terminal kinase activity in insulin-secreting cells: Evidence for cytoplasmic restriction. Diabetes 50, 2721-2728. (Pubitemid 33733122)
31. Marchetti P, Bugliani M, Lupi R, Marselli L, Masini M, Boggi U, Filipponi F, Weir GC, Eizirik DL, Cnop M (2007). The endoplasmic reticulum in pancreatic beta cells of type 2 diabetes patients. Diabetologia 50, 2486-2494. (Pubitemid 350060637)
32. Marchi S, Marinello M, Bononi A, Bonora M, Giorgi C, Rimessi A, Pinton P (2012). Selective modulation of subtype III IP3R by Akt regulates ER Ca2+ release and apoptosis. Cell Death Dis 3, e304.
33. Mbaya E et al. (2010). Calcium signalling-dependent mitochondrial dysfunction and bioenergetics regulation in respiratory chain complex II deficiency. Cell Death Differ 17, 1855-1866.
34. Mokhtari D, Myers JW, Welsh N (2008). MAPK kinase kinase-1 is essential for cytokine-induced c-Jun NH2-terminal kinase and nuclear factor-kappaB activation in human pancreatic islet cells. Diabetes 57, 1896-1904.
35. Nakatani Y et al. (2005). Involvement of endoplasmic reticulum stress in insulin resistance and diabetes. J Biol Chem 280, 847-851. (Pubitemid 40165054)
36. Pfaffl MW (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29, e45.
37. Pirot P, Ortis F, Cnop M, Ma Y, Hendershot LM, Eizirik DL, Cardozo AK (2007). Transcriptional regulation of the endoplasmic reticulum stress gene chop in pancreatic insulin-producing cells. Diabetes 56, 1069-1077. (Pubitemid 46540305)
38. Pita I, Jelaso AM, Ide CF (1999). IL-1beta increases intracellular calcium through an IL-1 type 1 receptor mediated mechanism in C6 astrocytic cells. Int J Dev Neurosci 17, 813-820. (Pubitemid 29488559)
39. Pizzo P, Pozzan T (2007). Mitochondria-endoplasmic reticulum choreography: Structure and signaling dynamics. Trends Cell Biol 17, 511-517. (Pubitemid 47562768)
40. Rapizzi E, Pinton P, Szabadkai G, Wieckowski MR, Vandecasteele G, Baird G, Tuft RA, Fogarty KE, Rizzuto R (2002). Recombinant expression of the voltage-dependent anion channel enhances the transfer of Ca2+ microdomains to mitochondria. J Cell Biol 159, 613-624.
41. Rizvi F, Heimann T, Herrnreiter A, O'Brien WJ (2011). Mitochondrial dysfunction links ceramide activated HRK expression and cell death. PLoS One 6, e18137.
42. Rizzuto R et al. (2009). Ca(2+) transfer from the ER to mitochondria: When, how and why. Biochim Biophys Acta 1787, 1342-1351.
43. Rizzuto R, Pinton P, Carrington W, Fay FS, Fogarty KE, Lifshitz LM, Tuft RA, Pozzan T (1998). Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses. Science 280, 1763-1766. (Pubitemid 28283502)
44. Storling J, Zaitsev SV, Kapelioukh IL, Karlsen AE, Billestrup N, Berggren PO, Mandrup-Poulsen T (2005). Calcium has a permissive role in interleukin-1beta-induced c-jun N-terminal kinase activation in insulin-secreting cells. Endocrinology 146, 3026-3036. (Pubitemid 41002810)
45. Tait SW, Green DR (2010). Mitochondria and cell death: Outer membrane permeabilization and beyond. Nat Rev Mol Cell Biol 11, 621-632.
46. Thomas HE, Darwiche R, Corbett JA, Kay TW (2002). Interleukin-1 plus gamma-interferon-induced pancreatic beta-cell dysfunction is mediated by beta-cell nitric oxide production. Diabetes 51, 311-316. (Pubitemid 34764785)
47. Thomas HE, Irawaty W, Darwiche R, Brodnicki TC, Santamaria P, Allison J, Kay TW (2004). IL-1 receptor deficiency slows progression to diabetes in the NOD mouse. Diabetes 53, 113-121. (Pubitemid 38044705)
48. Urano F, Wang X, Bertolotti A, Zhang Y, Chung P, Harding HP, Ron D (2000). Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287, 664-666. (Pubitemid 30070916)
49. Veluthakal R, Palanivel R, Zhao Y, McDonald P, Gruber S, Kowluru A (2005). Ceramide induces mitochondrial abnormalities in insulin-secreting INS-1 cells: Potential mechanisms underlying ceramide-mediated metabolic dysfunction of the beta cell. Apoptosis 10, 841-850. (Pubitemid 41187082)
50. Verma G, Datta M (2010). IL-1beta induces ER stress in a JNK dependent manner that determines cell death in human pancreatic epithelial MIA PaCa-2 cells. Apoptosis 15, 864-876.
51. Wang HJ, Guay G, Pogan L, Sauve R, Nabi IR (2000). Calcium regulates the association between mitochondria and a smooth subdomain of the endoplasmic reticulum. J Cell Biol 150, 1489-1498.
52. Wang X, Su B, Siedlak SL, Moreira PI, Fujioka H, Wang Y, Casadesus G, Zhu X (2008). Amyloid-beta overproduction causes abnormal mitochondrial dynamics via differential modulation of mitochondrial fission/fusion proteins. Proc Natl Acad Sci USA 105, 19318-19323.
53. Welsh N, Cnop M, Kharroubi I, Bugliani M, Lupi R, Marchetti P, Eizirik DL (2005). Is there a role for locally produced interleukin-1 in the deleterious effects of high glucose or the type 2 diabetes milieu to human pancreatic islets. Diabetes 54, 3238-3244. (Pubitemid 43334380)
54. Yasuhara R, Miyamoto Y, Akaike T, Akuta T, Nakamura M, Takami M, Morimura N, Yasu K, Kamijo R (2005). Interleukin-1beta induces death in chondrocyte-like ATDC5 cells through mitochondrial dysfunction and energy depletion in a reactive nitrogen and oxygen species-dependent manner. Biochem J 389, 315-323. (Pubitemid 41021134)
55. Zhao G, Adebiyi A, Blaskova E, Xi Q, Jaggar JH (2008). Type 1 inositol 1,4,5-trisphosphate receptors mediate UTP-induced cation currents, Ca2+ signals, and vasoconstriction in cerebral arteries. Am J Physiol Cell Physiol 295, C1376-C1384. (Pubitemid 352790341)