Group VIA PLA 2 (iPLA 2β) is activated upstream of p38 mitogen-activated protein kinase (MAPK) in pancreatic islet β-cell signaling

Journal of Biological Chemistry

Volumn 287, Issue 8, 2012, Pages 5528-5541

  Song, Haowei ^a   Wohltmann, Mary ^a   Tan, Min ^a   Bao, Shunzhong ^a   Ladenson, Jack H ^a   Turk, John ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARACHIDONIC ACIDS; CELL APOPTOSIS; CELL SIGNALING; CERAMIDES; CLOSTRIDIUM DIFFICILE; D-GLUCOSE; EXPRESSION LEVELS; FORSKOLIN; FUNCTIONAL RESPONSE; G PROTEIN; GLUCOSE-STIMULATED INSULIN SECRETIONS; INSULIN SECRETION; INSULINOMA CELLS; ISOFORMS; KINASE ACTIVATION; OVER-EXPRESSION; P38 MAPK; P38 MITOGEN-ACTIVATED PROTEIN KINASE; PANCREATIC ISLET; PHOSPHOLIPASE A; RHO FAMILY; SIGNALING EVENTS; THAPSIGARGINS;

AMIDES; CELL DEATH; CHEMICAL ACTIVATION; GLUCOSE; MAMMALS; PHOSPHORYLATION; PHYSIOLOGY;

INSULIN;

4 (4 FLUOROPHENYL) 2 (4 NITROPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ARACHIDONIC ACID; BROMOENOL LACTONE; CERAMIDE; CLOSTRIDIUM DIFFICILE TOXIN B; FORSKOLIN; GLUCOSE; GROUP VIA PHOSPHOLIPASE A2 BETA; INSULIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHOLIPASE A2; RHO FACTOR; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; THAPSIGARGIN; UNCLASSIFIED DRUG; 6 (BROMOMETHYLENE)TETRAHYDRO 3 (1 NAPHTHALENEYL) 2H PYRAN 2 ONE; 6-(BROMOMETHYLENE)TETRAHYDRO-3-(1-NAPHTHALENEYL)-2H-PYRAN-2-ONE; IMIDAZOLE DERIVATIVE; NAPHTHALENE DERIVATIVE; PHOSPHOLIPASE A2 GROUP VI; PLA2G6 PROTEIN, MOUSE; PYRONE DERIVATIVE; RHO GUANINE NUCLEOTIDE BINDING PROTEIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL FUNCTION; CELL STIMULATION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; INSULIN RELEASE; INTRACELLULAR SIGNALING; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; ANIMAL; CYTOLOGY; DOSE RESPONSE; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; GENE EXPRESSION REGULATION; MALE; METABOLISM; PHOSPHORYLATION; SECRETION (PROCESS); SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANIMALS; APOPTOSIS; ARACHIDONIC ACID; CELL LINE, TUMOR; CERAMIDES; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUCOSE; GROUP VI PHOSPHOLIPASES A2; IMIDAZOLES; INSULIN; INSULIN-SECRETING CELLS; MALE; MICE; NAPHTHALENES; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PYRONES; RATS; RHO GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION; THAPSIGARGIN;

EID: 84857323260     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.285114     Document Type: Article

References (107)

1. Mahler, R. J., and Adler, M. L. (1999) Type 2 diabetes mellitus. Update on diagnosis, pathophysiology, and treatment. J. Clin. Endocr. Metab. 84, 1165-1171
2. Hossain, P., Kawar, B., and El Nahas, M. (2007) Obesity and diabetes in the developing world.Agrowing challenge. N. Engl. J. Med. 356, 213-215
3. Hotamisligil, G. S., Shargill, N. S., and Spiegelman, B. M. (1993) Adipose expression of tumor necrosis factor-α. Direct role in obesity-linked insulin resistance. Science 259, 87-91
4. Ogden, C. L., Carroll, M. D., Curtin, L. R., Lamb, M. M., and Flegal, K. M. (2010) Prevalence of high body mass index in US children and adolescents. JAMA 303, 242-249
5. Laing, S. P., Swerdlow, A. J., Slater, S. D., Burden, A. C., Morris, A., Waugh, N. R., Gatling, W., Bingley, P. J., and Patterson, C. C. (2003) Mortality from heart disease in a cohort of 23,000 patients with insulin-treated diabetes. Diabetologia 46, 760-765
6. Shulman GI. (2000) Cellular mechanisms of insulin resistance. J. Clin. Invest. 106, 171-176
7. Kahn B. (1998) Type 2 diabetes: When insulin secretion fails to compensate for insulin resistance. Cell 92, 593-596
8. Gerich, J. E. (1998) The genetic basis of type 2 diabetes mellitus. Impaired insulin secretion versus impaired insulin sensitivity. Endocr. Rev. 19, 491-503
9. Weyer, C., Bogardus, C., Mott, D. M., and Pratley, R. E. (1999) The natural history of insulin secretory dysfunction and insulin resistance in the pathogenesis of type 2 diabetes mellitus. J. Clin. Invest. 104, 787-794
10. Klöppel, G., Löhr, M., Habich, K., Oberholzer, M., and Heitz, P. U. (1985) Islet pathology and the pathogenesis of type 1 and type 2 diabetes mellitus revisited. Surv. Synth. Pathol. Res. 4, 110-125
11. Stefan, Y., Orci, L., Malaisse-Lagae, F., Perrelet, A., Patel, Y., and Unger, R. H. (1982) Quantitation of endocrine cell content in the pancreas of nondiabetic and diabetic humans. Diabetes 31, 694-700
12. Butler, A. E., Janson, J., Bonner-Weir, S., Ritzel, R., Rizza, R. A., and Butler, P. C. (2003) Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes 52, 102-110
13. Oyadomari, S., Araki, E., and Mori, M. (2002) Endoplasmic reticulum stress-mediated apoptosis in pancreatic beta-cells. Apoptosis 7, 335-345
14. Araki, E., Oyadomari, S., and Mori, M. (2003) Impact of endoplasmic reticulum stress pathway on pancreatic beta cells and diabetes mellitus. Exp. Biol. Med. 228, 1213-1217
15. Ashcroft, S. J. (1980) Glucoreceptor mechanisms and the control of insulin release and biosynthesis. Diabetologia 18, 5-15
16. Meglasson, M. D., and Matschinsky, F. M. (1986) Pancreatic islet glucose metabolism and the regulation of insulin secretion. Diabetes Metab. Rev. 2, 163-214
17. Garvey, W. T. (1992) Glucose transport and NIDDM. Diabetes Care 15, 396-417
18. Matschinsky, F. M. (1990) Glucokinase as glucose sensor and metabolic signal generator in pancreatic beta cells and hepatocytes. Diabetes 39, 647-652
19. +channels in pancreatic β-cells. Nature 311, 271-273
20. + channels in rat pancreatic β-cells is modulated by ADP. FEBS Lett. 208, 63-66
21. Ghosh, A., Ronner, P., Cheong, E., Khalid, P., and Matschinsky, F. M. (1991) The role of ATP and free ADP in metabolic coupling during fuel-stimulated insulin release from islet β-cells in the isolated perfused rat pancreas. J. Biol. Chem. 266, 22887-22892
22. 2+ concentration in pancreatic beta cells. J. Biol. Chem. 262, 5448-5454
23. 2+ entry. Diabetes 41, 662-670
24. Easom RA. (1999) CaM kinase II. A protein kinase with extraordinary talents germane to insulin exocytosis. Diabetes 48, 675-684
25. 2+ stores and plasma membrane ion channels. Curr. Opin. Endocrinol. Diabetes Obes. 4, 262-271
26. 2+ influx in the electrically excitable pancreatic beta cell. J. Biol. Chem. 274, 20197-20205
27. 2 and protein kinase C-dependent phosphorylation of the α-subunit. J. Biol. Chem. 274, 2000-2008
28. Brown, L. J., MacDonald, M. J., Lehn, D. A., and Moran, S. M. (1994) Sequence of rat mitochondrial glycerol-3-phosphate dehydrogenase cDNA. Evidence for EF-hand calcium-binding domains. J. Biol. Chem. 269, 14363-14366
29. MacDonald MJ. (1995) Feasibility of a mitochondrial pyruvate-malate shuttle in pancreatic islets. Further implication of cytosolic NADPH in insulin secretion. J. Biol. Chem. 270, 20051-20058
30. Eto, K., Tsubamoto, Y., Terauchi, Y., Sugiyama, T., Kishimoto, T., Takahashi, N., Yamauchi, N., Kubota, N., Murayama, S., Aizawa, T., Akanuma, Y., Aizawa, S., Kasai, H., Yazaki, Y., and Kadowaki, T. (1999) Role of NADH shuttle system in glucose-induced activation of mitochondrial metabolism and insulin secretion. Science 283, 981-985
31. Ravier, M. A., Eto, K., Jonkers, F. C., Nenquin, M., Kadowaki, T., and Henquin, J. C. (2000) The oscillatory behavior of pancreatic islets from mice with mitochondrial glycerol-3-phosphate dehydrogenase knockout. J. Biol. Chem. 275, 1587-1593
32. Wollheim, C. B. (2000) Beta cell mitochondria in the regulation of insulin secretion. A new culprit in type II diabetes. Diabetologia 43, 265-277
33. + channels in beta cells. Endocrinology 140, 2252-2257
34. + channel-independent pathway of glucose signaling in rat pancreatic islets. Diabetes 48, 1006-1012
35. Seino, S., and Shibasaki, T. (2005) PKA-dependent and PKA-independent pathways for cAMP-regulated exocytosis. Physiol. Rev. 85, 1303-1342
36. 2+, cAMP, and phospholipid- derived messengers in coupling mechanisms of insulin secretion. Physiol. Rev. 67, 1185-1248
37. 2 activity in pancreatic islets is calcium-dependent and stimulated by glucose. Cell Calcium 3, 43-54
38. 2 in glucose stimulated pancreatic islets. Biochem. Biophys. Res. Commun. 120, 820-827
39. Metz, S. A. (1991) The pancreatic islet as Rubik's cube. Is phospholipid hydrolysis a piece of the puzzle? Diabetes 40, 1565-1573
40. + permeability without diminution by exogenous arachidonic acid. Biochem. Pharm. 53, 1077-1086
41. 2 and its potential regulation of islet function. Int. J. Pancreatol. 27, 1-11
42. 2 results in insufficient insulin secretion and impaired glucose tolerance. Mol Endocrinol. 19, 504-515
43. McDonald, P., Veluthakal, R., Kaur, H., and Kowluru, A. (2007) Biologically active lipids promote trafficking and membrane association of Rac1 in insulin-secreting INS 832/13 cells. Am. J. Physiol. Cell. Physiol. 292, C1216-C1220
44. Poitout, V. (2008) Phospholipid hydrolysis and insulin secretion. A step toward solving the Rubik's cube. Am. J. Physiol. Endocrinol. Metab. 294, E214-E216
45. 2+ mobilization by arachidonic acid. Comparison with myoinositol 1,4,5-triphosphate in isolated pancreatic islets. J. Biol. Chem. 261, 3501-3511
46. Wolf, B. A., Pasquale, S. M., and Turk, J. (1991) Free fatty acid accumulation in secretagogue-stimulated pancreatic islets and effects of arachidonate on depolarization-induced insulin secretion. Biochemistry 30, 6372-6379
47. Turk, J., Mueller, M., Bohrer, A., and Ramanadham, S. (1992) Arachidonic acid metabolism in isolated pancreatic islets VI. Carbohydrate insulin secretagogues must be metabolized to induce eicosanoid release. Biochim. Biophys. Acta 1125, 280-291
48. Ramanadham, S., Gross, R., and Turk, J. (1992) Arachidonic acid induces an increase in cytosolic calcium concentration in single pancreatic islet beta cells. Biochem. Biophys. Res. Commun. 184, 647-653
49. Ramanadham, S., Gross, R. W., Han, X., and Turk, J. (1993) Inhibition of arachidonate release by secretagogue-stimulated pancreatic islets suppresses both insulin secretion and the rise in beta cell cytosolic calcium concentration. Biochemistry 32, 337-346
50. 2 activity selective for hydrolysis of arachidonate which is stimulated by ATP and specifically localized to islet beta cells. Biochemistry 32, 327-336
51. 2from clonal insulin-secreting HIT cells and rat pancreatic islets. A possible molecular component of the beta cell fuel sensor. Biochemistry 33, 7442-7452
52. 2 enzyme in clonal insulinoma cell lines. Biochim. Biophys. Acta 1344, 153-164
53. 2enzyme that contains a repeated structural motif homologous to the integral membrane protein binding domain of ankyrin. J. Biol. Chem. 272, 11118-11127
54. 2 gene on chromosome 22q13.1. J. Biol. Chem. 274, 9607-9616
55. 2) in fatty acid incorporation, phospholipid remodeling, lysophosphatidylcholine generation, and secretagogue-induced arachidonic acid release in pancreatic islets and insulinoma cells. J. Biol. Chem. 274, 13915-13927
56. 2β) in β-cells. Can J. Physiol. Pharmacol. 82, 824-832
57. Kienesberger, P. C., Oberer, M., Lass, A., and Zechner, R. (2009) Mammalian patatin domain-containing proteins. A family with diverse lipolytic activities involved in multiple biological functions. J. Lipid Res. 50, (suppl.) S63-S68
58. 2β. J. Biol. Chem. 276, 13198-13208
59. 2β transcript. Biochemistry 42, 13929-13940
60. 2 expression on phospholipid content and composition, insulin secretion, and proliferation of INS-1 insulinoma cells. J. Biol. Chem. 281, 187-198
61. 2 and effects of metabolic stress on glucose homeostasis. J. Biol. Chem. 281, 20958-20973
62. 2β-null mice. Am. J. Physiol. Endocrinol. Metab. 294, E217-E229
63. 2. A novel mechanism underlying arachidonic acid release. J. Biol. Chem. 272, 1522-1526
64. 2+ concentration. Endocrinology 139, 4073-4085
65. 2β) in endoplasmic reticulum stress-induced apoptosis in insulinoma cells. Biochemistry 43, 918-930
66. 2. J. Biol. Chem. 282, 27100-27114
67. -/- mice. J. Biol. Chem. 283, 33975-33987
68. 2β) in beta cells include tyrosine phosphorylation and increased association with calnexin. J. Biol. Chem. 285, 33843-33857
69. 2-mediated repair of mitochondrial membrane peroxidation. Endocrinology 151, 3038-3048
70. 2 localizes in and protects mitochondria during apoptotic induction by staurosporine. J. Biol. Chem. 281, 22275-22288
71. 2 participates in ER stress-induced INS-1 insulinoma cell apoptosis by promoting ceramide generation via hydrolysis of sphingomyelins by neutral sphingomyelinase. Biochemistry 46, 10170-10185
72. 2β)- 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. 283, 34819-34832
73. Ron, D., and Walter, P. (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 8, 519-529
74. Ma, Y., Brewer, J. W., Diehl, J. A., and Hendershot, L. M. (2002) Two distinct stress signaling pathways converge upon the CHOP promoter during the mammalian unfolded protein response. J. Mol. Biol. 318, 1351-1365
75. Harding, H. P., Zhang, Y., Bertolotti, A., Zeng, H., and Ron, D. (2000) Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol. Cell 5, 897-904
76. Rao, R. V., Ellerby, H. M., and Bredesen, D. E. (2004) Coupling endoplasmic reticulum stress to the cell death program. Cell Death Differ. 11, 372-380
77. Cargnello, M., and Roux, P. P. (2011) Activation and function of the MAPKs and their substrates, the MAPK-activated protein kinases. Microbiol. Mol. Biol. Rev. 75, 50-83
78. Hsu, F. F., and Turk, J. (2002) Characterization of ceramides by low energy collisional-activated dissociation tandem mass spectrometry with negative-ion electrospray ionization. J. Am. Soc. Mass Spectrom. 13, 558-570
79. Hsu, F. F., Turk, J., Stewart, M. E., and Downing, D. T. (2002) Structural studies on ceramides as lithiated adducts by low energy collisional-activated dissociation tandem mass spectrometry with electrospray ionization. J. Am. Soc. Mass Spectrom. 13, 680-695
80. 2γ) exhibit relative resistance to obesity and metabolic abnormalities induced by a Western diet. Am. J. Physiol. Endocrinol. Metab. 298, E1097-E1114
81. Bordin, S., and Whitfield, D. (2003) Cutting edge. Proliferating fibroblasts respond to collagenous C1q with phosphorylation of p38 mitogen-activated protein kinase and apoptotic features. J. Immunol. 170, 667-671
82. Song, H., Ramanadham, S., Bao, S., Hsu, F. F., and Turk, J. (2006) A bromoenol lactone suicide substrate inactivates Group VIA phospholipase A2 by generating a diffusible bromomethyl ketoacid that alkylates cysteine thiols. Biochemistry 45, 1061-1073
83. 2. J. Biol. Chem. 266, 7227-7232
84. 2. J. Med. Chem. 36, 95-100
85. Khaled, A. R., Moor, A. N., Li, A., Kim, K., Ferris, D. K., Muegge, K., Fisher, R. J., Fliegel, L., and Durum, S. K. (2001) Trophic factor withdrawal. p38 mitogen-activated protein kinase activates NHE1, which induces intracellular alkalinization. Mol. Cell. Biol. 21, 7545-7557
86. 2s. J. Biol. Chem. 277, 32807-32814
87. 2β) participates in angiotensin II-induced transcriptional up-regulation of regulator of G-protein signaling-2 in vascular smooth muscle cells. J. Biol. Chem. 282, 25278-25289
88. 2β 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. 285, 8628-8638
89. 2 and 12/15-Lipoxygenase to Rac and Cdc42 activation. J. Biol. Chem. 282, 33405-33411
90. Zhang, S., Han, J., Sells, M. A., Chernoff, J., Knaus, U. G., Ulevitch, R. J., and Bokoch, G. M. (1995) Rho family GTPases regulate p38 mitogen-activated protein kinase through the downstream mediator Pak1. J. Biol. Chem. 270, 23934-23936
91. Bagrodia, S., Dérijard, B., Davis, R. J., and Cerione, R. A. (1995) Cdc42 and PAK-mediated signaling leads to Jun kinase and p38 mitogen-activated protein kinase activation. J. Biol. Chem. 270, 27995-27998
92. Tibbles, L. A., Ing, Y. L., Kiefer, F., Chan, J., Iscove, N., Woodgett, J. R., and Lassam, N. J. (1996) MLK-3 activates the SAPK/JNK and p38/RK pathways via SEK1 and MKK3/6. EMBO J. 15, 7026-7035
93. Martin, G. A., Bollag, G., McCormick, F., and Abo, A. (1995) A novel serine kinase activated by rac1/CDC42Hs-dependent autophosphorylation is related to PAK65 and STE20. EMBO J. 14, 1970-1978
94. Manser, E., Leung, T., Salihuddin, H., Zhao, Z. S., and Lim, L. (1994) A brain serine/threonine protein kinase activated by Cdc42 and Rac1. Nature 367, 40-46
95. Just, I., Selzer, J., Wilm, M., von Eichel-Streiber, C., Mann, M., and Aktories, K. (1995) Glucosylation of Rho proteins by Clostridium difficile toxin B. Nature 375, 500-503
96. Cheng, H., Kartenbeck, J., Kabsch, K., Mao, X., Marqués, M., and Alonso, A. (2002) Stress kinase p38 mediates EGFR transactivation by hyperosmolar concentrations of sorbitol. J. Cell. Physiol. 192, 234-243
97. Jacobson, D. A., Weber, C. R., Bao, S., Turk, J., and Philipson, L. H. (2007) Modulation of the pancreatic islet beta-cell-delayed rectifier potassium channel Kv2.1 by the polyunsaturated fatty acid arachidonate. J. Biol. Chem. 282, 7442-7449
98. Jacobson, D. A., Kuznetsov, A., Lopez, J. P., Kash, S., Ammälä, C. E., and Philipson, L. H. (2007) Kv2.1 ablation alters glucose-induced islet electrical activity, enhancing insulin secretion. Cell Metab. 6, 229-235
99. Hii, C. S., Huang, Z. H., Bilney, A., Costabile, M., Murray, A. W., Rathjen, D. A., Der, C. J., and Ferrante, A. (1998) Stimulation of p38 phosphorylation and activity by arachidonic Acid in HeLa Cells, HL60 promyelocytic leukemic cells, and human neutrophils. Stimulation of p38 phosphorylation and activity by arachidonic acid in HeLa cells, HL60 promyelocytic leukemic cells, and human neutrophils. Evidence for cell type-specific activation of mitogen-activated protein kinases. J. Biol. Chem. 273, 19277-19282
100. Talukdar, I., Szeszel-Fedorowicz, W., and Salati, L. M. (2005) Arachidonic acid inhibits the insulin induction of glucose-6-phosphate dehydrogenase via p38 MAP kinase. J. Biol. Chem. 280, 40660-40667
101. Park, K. S., Mohapatra, D. P., Misonou, H., and Trimmer, J. S. (2006) Graded regulation of the Kv2.1 potassium channel by variable phosphorylation. Science 313, 976-979
102. Tiran, Z., Peretz, A., Attali, B., and Elson, A. (2003) Phosphorylation-dependent regulation of Kv2.1 channel activity at tyrosine 124 by Src and by protein-tyrosine phosphatase ε. J. Biol. Chem. 278, 17509-17514
103. Redman, P. T., He, K., Hartnett, K. A., Jefferson, B. S., Hu, L., Rosenberg, P. A., Levitan, E. S., and Aizenman, E. (2007) Apoptotic surge of potassium currents is mediated by p38 phosphorylation of Kv2.1. Proc. Natl. Acad. Sci. U.S.A. 104, 3568-3573
104. 2 expression. A role for regulation by SREBP-1. J. Biol. Chem. 285, 6693-6705
105. Zarubin, T., and Han, J. (2005) Activation and signaling of the p38 MAP kinase pathway. Cell Res. 15, 11-18
106. 2β regulates virus-induced inducible nitric-oxide synthase expression by macrophages. J. Biol. Chem. 280, 28162-28168
107. 2 activates p38 MAPK signaling pathways during cytostasis in prostate cancer cells. Biochem. Pharmacol. 79, 1727-1735