Evidence of contribution of iPLA2β-mediated events during islet β-cell apoptosis due to proinflammatory cytokines suggests a role for iPLA2β in T1D development

Endocrinology (United States)

Volumn 155, Issue 9, 2014, Pages 3352-3364

  Lei, Xiaoyong ^a,d   Bone, Robert N ^b,d   Ali, Tomader ^a,d   Zhang, Sheng ^e   Bohrer, Alan ^e   Tse, Hubert M ^c,d   Bidasee, Keshore R ^f   Ramanadham, Sasanka ^a,d  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b University of Alabama at Birmingham   (United States)

^c University of Alabama at Birmingham   (United States)

^d UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^e WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM INDEPENDENT PHOSPHOLIPASE A2; CALCIUM INDEPENDENT PHOSPHOLIPASE A2 BETA; CASPASE 3; CERAMIDE; GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; LYSOPHOSPHATIDYLCHOLINE; SPHINGOMYELIN PHOSPHODIESTERASE; SPHINGOMYELINASE 2; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; UNCLASSIFIED DRUG; CYTOKINE; PHOSPHOLIPASE A2 GROUP VI; PLA2G6 PROTEIN, HUMAN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL DEATH; CHEMOTAXIS; CONTROLLED STUDY; DISEASE COURSE; DISEASE EXACERBATION; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; FEMALE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; INSULIN DEPENDENT DIABETES MELLITUS; MALE; MITOCHONDRIAL MEMBRANE; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PROTEIN EXPRESSION; ANIMAL; CYTOLOGY; ENZYMOLOGY; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; PANCREAS ISLET; PATHOPHYSIOLOGY;

ADULT; ANIMALS; APOPTOSIS; CYTOKINES; DIABETES MELLITUS, TYPE 1; ENDOPLASMIC RETICULUM STRESS; FEMALE; GROUP VI PHOSPHOLIPASES A2; HUMANS; INTERFERON-GAMMA; INTERLEUKIN-1BETA; ISLETS OF LANGERHANS; MALE; MICE; MICE, KNOCKOUT; STEROL REGULATORY ELEMENT BINDING PROTEIN 1;

EID: 84907053922     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2013-2134     Document Type: Article

References (65)

1. Tisch R, McDevitt H. Insulin-dependent diabetes mellitus. Cell. 1996;85:291-297.
2. Rabinovitch A, Suarez-Pinzon WL. Cytokines and their roles in pancreatic islet beta-cell destruction and insulin-dependent diabetes mellitus. Biochem Pharmacol. 1998;55:1139-1149.
3. Mandrup-Poulsen T. Beta-cell apoptosis: stimuli and signaling. Diabetes. 2001;50:S58-S63.
4. -/-mice reveals a role for transla-tional control in secretory cell survival. Mol Cell. 2001;7:1153-1163.
5. Oyadomari S, Araki E, Mori M. Endoplasmic reticulum stress-mediated apoptosis in pancreatic beta-cells. Apoptosis. 2002;7:335-345.
6. Kroncke K-D, Brenner H-H, Rodriguez M-L, Etzkorn K, Noack EA, Kolb H, et al. Pancreatic islet cells are highly susceptible towards the cytotoxic effects of chemically generated nitric oxide. Biochimic Biophys Acta. 1993;1182:221-229.
7. Mandrup-Poulsen T. Theroleofinterleukin-1 in the pathogenesis of IDDM. Diabetologia. 1996;39:1005-1029.
8. Akerfeldt MC, Howes J, Chan JY, et al. Cytokine-induced beta-cell death is independent of endoplasmic reticulum stress signaling. Diabetes. 2008;57:3034-3044.
9. Eizirik DL, Cardozo AK, Cnop M. The role for endoplasmic reticulum stress in diabetes mellitus. Endocr Rev. 2008;29:42-61.
10. Kacheva S, Lenzen S, Gurgul-Convey E. Differential effects of proinflammatory cytokines on cell death and ER stress in insulin-secreting INS1E cells and the involvement of nitric oxide. Cytokine. 2011;55:195-201.
11. 2+release through the c-Jun N-terminal kinase pathway. Mol Cell Biochem. 2009;324: 183-190.
12. Weber SM, Chambers KT, Bensch KG, Scarim AL, Corbett JA. PPARgamma ligands induce ER stress in pancreatic beta-cells: ER stress activation results in attenuation of cytokine signaling. Am J Physiol Endocrinol Metab. 2004;287:E1171-E1177.
13. Zhong J, Rao X, Xu JF, Yang P, Wang CY. The role of endoplasmic reticulum stress in autoimmune-mediated beta-cell destruction in type 1 diabetes. Exp Diabetes Res. 2012;2012:238980.
14. 2expression: a role for regulation by SREBP-1. JBiol Chem. 2010;285: 6693-6705.
15. 2participates in ER stress-induced INS-1 insulinoma cell apoptosis by promoting ceramide generation via hydrolysis of sphingomyelins by neutral sphingomyelinase. Biochemistry. 2007;46:10170-10185.
16. 2beta)-mediated ceramide generation plays a key role in the cross-talk between the endoplasmic reticulum (ER) and mitochondria during ER stress-induced insulin-secreting cell apoptosis. J Biol Chem. 2008;283:34819-34832.
17. 2beta. Biochemistry. 2004;43:918-930.
18. 2/3 expression provides evidence for its impact on β-cell apoptosis and autophagy. Islets. 2013;5:29-44.
19. 2/3 in human pancreatic islet β-cell apoptosis. Am J Physiol Endocrinol Metab. 2012;303: E1386-E1395.
20. 2: homeo-static phospholipases with significant potential as targets for novel therapeutics. Curr Drug Targets. 2008;9:683-697.
21. Ramanadham S, Bohrer A, Gross RW, Turk J. Mass spectrometric characterization of arachidonate-containing plasmalogens in human pancreatic islets and in rat islet beta-cells and subcellular membranes. Biochemistry. 1993;32:13499-13509.
22. 2in neutrophils. J Immunol. 2010; 184:1507-1515.
23. 2activation in the response to ischemia. Am J Physiol. 2011;300:H326-H334.
24. 2beta in high glucose-induced activation of RhoA, Rho kinase, and CPI-17 in cultured vascular smooth muscle cells and vascular smooth muscle hypercontractility in diabetic animals. J Biol Chem. 2010;285:8628-8638.
25. Heitmeier MR, Kelly CB, Ensor NJ, et al. Role of cyclooxygenase-2 in cytokine-induced beta-cell dysfunction and damage by isolated rat and human islets. J Biol Chem. 2004;279:53145-53151.
26. Hindlycke H, Lu T, Welsh N. Cytokine-induced human islet cell death in vitro correlates with a persistently high phosphorylation of STAT-1, but not with NF-κB activation. Biochem Biophys Res Commun. 2012;418:845-850.
27. Cardozo AK, Proost P, Gysemans C, Chen MC, Mathieu C, Eizirik DL. IL-1beta and IFN-gamma induce the expression of diverse chemokines and IL-15 in human and rat pancreatic islet cells, and in islets from pre-diabetic NOD mice. Diabetologia. 2003;46:255-266.
28. Heitmeier MR, Scarim AL, Corbett JA. Interferon-gamma increases the sensitivity of islets of Langerhans for inducible nitric-oxide synthase expression induced by interleukin 1. J Biol Chem. 1997;272: 13697-13704.
29. Corbett JA, Kwon G, Marino MH, et al. Tyrosine kinase inhibitors prevent cytokine-induced expression of iNOS and COX-2 by human islets. Am J Physiol. 1996;270:C1581-C1587.
30. Corbett JA, Sweetland MA, Wang JL, Lancaster JR Jr, McDaniel ML. Nitric oxide mediates cytokine-induced inhibition of insulin secretion by human islets of Langerhans. Proc Natl Acad Sci USA. 1993;90:1731-1735.
31. Burgess A, Vigneron S, Brioudes E, Labbé JC, Lorca T, Castro A. Loss of human Greatwall results in G2 arrest and multiple mitotic defects due to deregulation of the cyclin B-Cdc2/PP2A balance. Proc Natl Acad Sci USA. 2010;107:12564-12569.
32. 2gamma, as the mediator of arginine vasopressin-induced ar-achidonic acid release in A-10 smooth muscle cells. Enantioselective mechanism-based discrimination of mammalian iPLA2s. J Biol Chem. 2002;277:32807-32814.
33. Siskind LJ, Kolesnick RN, Colombini M. Ceramide forms channels in mitochondrial outer membranes at physiologically relevant concentrations. Mitochondrion. 2006;6:118-125.
34. Desagher S, Osen-Sand A, Nichols A, et al. Bid-induced conformational change of Bax is responsible for mitochondrial cytochrome c release during apoptosis. J Cell Biol. 1999;144:891-901.
35. 2produce spermatozoa with impaired motility and have greatly reduced fertility. J Biol Chem. 2004;279:38194-38200.
36. 2beta-null mice. Am J Physiol Endocrinol Metab. 2008;294:E217-E229.
37. van Belle TL, Coppieters KT, von Herrath MG. Type 1 diabetes: etiology, immunology, and therapeutic strategies. Physiol Rev. 2011;91:79-118.
38. Tse HM, Milton MJ, Schreiner S, Profozich JL, Trucco M, Piganelli JD. Disruption of innate-mediated proinflammatory cytokine and reactive oxygen species third signal leads to antigen-specific hypo-responsiveness. JImmunol. 2007;178:908-917.
39. Tse HM, Milton MJ, Piganelli JD. Mechanistic analysis of the immunomodulatory effects of a catalytic antioxidant on antigen-presenting cells: implication for their use in targeting oxidation-reduction reactions in innate immunity. Free Radic Biol Med. 2004;36: 233-247.
40. Padgett LE, Broniowska KA, Hansen PA, Corbett JA, Tse HM. The role of reactive oxygen species and proinflammatory cytokines in type 1 diabetes pathogenesis. Ann NY Acad Sci. 2013;1281:16-35.
41. Mandrup-Poulsen T. Beta cell death and protection. Ann NY Acad Sci. 2003;1005:32-42.
42. Harding HP, Zhang Y, Ron D. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature. 1999;397:271-274.
43. Reddy RK, Mao C, Baumeister P, Austin RC, Kaufman RJ, Lee AS. Endoplasmic reticulum chaperone protein GRP78 protects cells from apoptosis induced by topoisomerase inhibitors: role of ATP binding site in suppression of caspase-7 activation. J Biol Chem. 2003;278:20915-20924.
44. 2activity selective for hydrolysis of arachidonate which is stimulated by adenosine triphosphate and is specifically localized to islet beta-cells. Biochemistry. 1993;32:327-336.
45. Tersey SA, Nishiki Y, Templin AT, et al. Islet β-cell endoplasmic reticulum stress precedes the onset of type 1 diabetes in the nonobese diabetic mouse model. Diabetes. 2012;61:818-827.
46. 2/3): candidate drug for preventing beta-cell apoptosis and diabetes. PloS one. 2013;8:e71748.
47. Duchen MR. Mitochondria and calcium: from cell signalling to cell death. J Physiol. 2000;529 Pt 1:57-68.
48. Boslem E, Meikle PJ, Biden TJ. Roles of ceramide and sphingolipids in pancreatic β-cell function and dysfunction. Islets. 2012;4:177-187.
49. Hannun YA. Functions of ceramide in coordinating cellular responses to stress. Science. 1996;274:1855-1859.
50. Shimabukuro M, Higa M, Zhou YT, Wang MY, Newgard CB, Unger RH. Lipoapoptosis in beta-cells of obese prediabetic fa/fa rats. Role of serine palmitoyltransferase overexpression. J Biol Chem. 1998;273:32487-32490.
51. Memon RA, Holleran WM, Moser AH, et al. Endotoxin and cytokines increase hepatic sphingolipid biosynthesis and produce lipoproteins enriched in ceramides and sphingomyelin. Arterioscler Thromb Vasc Biol. 1998;18:1257-1265.
52. Kaplan M, Aviram M, Hayek T. Oxidative stress and macrophage foam cell formation during diabetes mellitus-induced atherogenesis: role of insulin therapy. Pharmacol Ther. 2012;136:175-185.
53. Wang H, Kouri G, Wollheim CB. ER stress and SREBP-1 activation are implicated in beta-cell glucolipotoxicity. J Cell Sci. 2005;118: 3905-3915.
54. 2expression by sterol availability. Biochim Biophys Acta. 2004;1684:29-37.
55. Grankvist K, Marklund SL, Täljedal IB. CuZn-superoxide dismu-tase, Mn-superoxide dismutase, catalase and glutathione peroxidase in pancreatic islets and other tissues in the mouse. Biochem J. 1981;199:393-398.
56. Wang M, Crager M, Pugazhenthi S. Modulation of apoptosis pathways by oxidative stress and autophagy in β-cells. Exp Diabetes Res. 2012;2012:647914.
57. Zhao F, Wang Q. The protective effect of peroxiredoxin II on oxidative stress induced apoptosis in pancreatic β-cells. Cell Biosci. 2012;2:22.
58. Rutkute K, Asmis RH, Nikolova-Karakashian MN. Regulation of neutral sphingomyelinase-2 by GSH: a new insight to the role of oxidative stress in aging-associated inflammation. J Lipid Res. 2007;48:2443-2452.
59. 2beta) and its role in beta-cell programmed cell death. Biochimie. 2010;92:627-637.
60. Murakami K, Kondo T, Ohtsuka Y, Fujiwara Y, Shimada M, Kawakami Y. Impairment of glutathione metabolism in erythrocytes from patients with diabetes mellitus. Metabolism. 1989;38: 753-758.
61. 2in L929 cells. FEBS Lett. 2001;507:151-156.
62. Lauber K, Bohn E, Kröber SM, et al. Apoptotic cells induce migration of phagocytes via caspase-3-mediated release of a lipid attraction signal. Cell. 2003;113:717-730.
63. Peter C, Waibel M, Keppeler H, et al. Release of lysophospholipid 'find-me' signals during apoptosis requires the ATP-binding cassette transporter A1. Autoimmunity. 2012;45:568-573.
64. Peter C, Waibel M, Radu CG, et al. Migration to apoptotic "find-me" signals is mediated via the phagocyte receptor G2A. J Biol Chem. 2008;283:5296-5305.
65. Weaver JR, Holman TR, Imai Y, Jadhav A, Kenyon V, Maloney DJ, et al. Integration of pro-inflammatory cytokines, 12-lipoxygenase and NOX-1 in pancreatic islet beta cell dysfunction. Mol Cell Endocrinol. 2012;358:88-95.