Group X secretory phospholipase a2 regulates insulin secretion through a cyclooxygenase-2-dependent mechanism

Journal of Biological Chemistry

Volumn 289, Issue 40, 2014, Pages 27410-27417

  Shridas, Preetha ^a   Zahoor, Lubna ^a   Forrest, Kathy J ^a   Layne, Joseph D ^a   Webb, Nancy R ^a  

^a UNIVERSITY OF KENTUCKY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASCORBIC ACID; CELLS; GLUCOSE; INSULIN; MAMMALS; PHOSPHOLIPIDS; PHYSIOLOGY;

BETA CELL FUNCTIONS; GLUCOSE-STIMULATED INSULIN SECRETIONS; INSULIN-PRODUCING CELLS; MEMBRANE PHOSPHOLIPIDS; PANCREATIC BETA CELLS; PLASMA INSULIN LEVELS; RECEPTOR ANTAGONISTS; SECRETORY PHOSPHOLIPASE;

CYTOLOGY;

ARACHIDONIC ACID; CYCLIC AMP; CYCLOOXYGENASE 2; GLUCOSE; GROUP X SECRETORY PHOSPHOLIPASE A2; INSULIN; N (2 CYCLOHEXYLOXY 4 NITROPHENYL)METHANESULFONAMIDE; N [(5 BROMO 2 METHOXYPHENYL)SULFONYL] 3 [2 (2 NAPHTHYLMETHYL)PHENYL]ACRYLAMIDE; PHOSPHOLIPASE A2 GROUP X; PROSTAGLANDIN E2; SECRETORY PHOSPHOLIPASE A2; UNCLASSIFIED DRUG; PTGS2 PROTEIN, MOUSE;

AGE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ISOLATION; CONTROLLED STUDY; ENZYME ACTIVITY; EX VIVO STUDY; GENE OVEREXPRESSION; GLUCOSE TOLERANCE; IN VITRO STUDY; IN VIVO STUDY; INSULIN BLOOD LEVEL; INSULIN RELEASE; MALE; MIN6 CELL LINE; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PANCREAS ISLET CELL FUNCTION; PROSTAGLANDIN SYNTHESIS; REGULATORY MECHANISM; ANIMAL; C57BL MOUSE; ENZYMOLOGY; GENETICS; KNOCKOUT MOUSE; METABOLISM; PANCREAS ISLET; SECRETION (PROCESS);

ANIMALS; CYCLOOXYGENASE 2; DINOPROSTONE; GLUCOSE; GROUP X PHOSPHOLIPASES A2; INSULIN; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT;

EID: 84907487966     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.591735     Document Type: Article

References (49)

1. Kahn, S. E., Hull, R. L., and Utzschneider, K. M. (2006) Mechanisms linking obesity to insulin resistance and type 2 diabetes. Nature 444, 840-846
2. Prentki, M., and Nolan, C.J. (2006) Islet ß cell failure in type 2 diabetes. J. Clin. Invest 116, 1802-1812
3. Ramanadham, S., Bohrer, A., Mueller, M., Jett, P., Gross, R. W., and Turk, J. (1993) Mass spectrometric identification and quantitation of arachidonate-containing phospholipids in pancreatic islets: Prominence of plasmenylethanolamine molecular species. Biochemistry 32, 5339-5351
4. Jones, P. M., and Persaud, S. J. (1993) Arachidonic acid as a second messenger in glucose-induced insulin secretion from pancreatic ß-cells. J. Endocrinol. 137, 7-14
5. Persaud, S. J., Muller, D., Belin, V. D., Kitsou-Mylona, I., Asare-Anane, H., Papadimitriou, A., Burns, C. J., Huang, G. C., Amiel, S. A., and Jones, P. M. (2007) The role of arachidonic acid and its metabolites in insulin secretion from human islets of langerhans. Diabetes 56, 197-203
6. Keane, D., and Newsholme, P. (2008) Saturated and unsaturated (including arachidonic acid) non-esterified fatty acid modulation of insulin secretion from pancreatic beta-cells. Biochem. Soc. Trans. 36, 955-958
7. Landt, M., Easom, R. A., Colca, J. R., Wolf, B. A., Turk, J., Mills, L. A., and McDaniel, M. L. (1992) Parallel effects of arachidonic acid on insulin secretion, calmodulin-dependent protein kinase activity and protein kinase C activity in pancreatic islets. Cell calcium 13, 163-172
8. Metz, S. A. (1988) Exogenous arachidonic acid promotes insulin release from intact or permeabilized rat islets by dual mechanisms. Putative activation of Ca2+ mobilization and protein kinase C. Diabetes 37, 1453-1469
9. Meng, Z. X., Sun, J. X., Ling, J. J., Lv, J. H., Zhu, D. Y., Chen, Q., Sun, Y. J., and Han, X. (2006) Prostaglandin E2 regulates Foxo activity via the Akt pathway: implications for pancreatic islet beta cell dysfunction. Diabetologia 49, 2959-2968
10. Meng, Z., Lv, J., Luo, Y., Lin, Y., Zhu, Y., Nie, J., Yang, T., Sun, Y., and Han, X. (2009) Forkhead box O1/pancreatic and duodenal homeobox 1 intracellular translocation is regulated by c-Jun N-terminal kinase and involved in prostaglandin E2-induced pancreatic ß-cell dysfunction. Endocrinology 150, 5284-5293
11. Tran, P. O. T., Gleason, C. E., Poitout, V., and Robertson, R. P. (1999) Prostaglandin E2 mediates inhibition of insulin secretion by interleuldn-1ß.J. Biol. Chem. 274, 31245-31248
12. Luo, P., and Wang, M.-H. (2011) Eicosanoids, ß-cell function, and diabetes. Prostaglandins Other Lipid Mediat. 95, 1-10
13. Kimple, M. E., Keller, M. P., Rabaglia, M. R., Pasker, R. L., Truchan, N. A., Neuman, J. C., Brar, H. K., and Attie, A. D. (2013) The prostaglandin E2 receptor, EP3, is induced in diabetic islets and negatively regulates glucose-and hormone-stimulated insulin secretion. Diabetes 62, 1904-1912
14. Coleman, R. A., Smith, W. L., and Narumiya, S. (1994) International Union of Pharmacology classification of prostanoid receptors: properties, distribution, and structure of the receptors and their subtypes. Pharmacol. Rev. 46, 205-229
15. Tran, P. O. T., Gleason, C. E., and Robertson, R. P. (2002) Inhibition of interleukin-1ß-induced COX-2 and EP3 gene expression by sodium salicylate enhances pancreatic islet ß-cell function. Diabetes 51, 1772-1778
16. Smyth, E. M., Grosser, T., Wang, M., Yu, Y., and FitzGerald, G. A. (2009) Prostanoids in health and disease. J. Lipid Res. 50, S423-S428
17. Yajima, H., Komatsu, M., Schermerhorn, T., Aizawa, T., Kaneko, T., Nagai, M., Sharp, G. W., and Hashizume, K. (1999) cAMP enhances insulin secretion by an action on the ATP-sensitive K+ channel-independent pathway of glucose signaling in rat pancreatic islets. Diabetes 48, 1006-1012
18. Dubois, R. N., Abramson, S.B., Crofford, L., Gupta, R. A., Simon, L. S., Van De Putte, L. B., and Lipsky, P. E. (1998) Cyclooxygenase in biology and disease. FASEB J. 12, 1063-1073
19. Sorli, C. H., Zhang, H.-J., Armstrong, M. B., Rajotte, R. V., Maclouf, J., and Robertson, R. P. (1998) Basal expression of cyclooxygenase-2 and nuclear factor-interleukin 6 are dominant and coordinately regulated by interleukin 1 in the pancreatic islet. Proc. Natl. Acad. Sci. U.S.A. 95, 1788 -1793
20. Fujita, H., Kakei, M., Fujishima, H., Morii, T., Yamada, Y., Qi, Z., and Breyer, M. D. (2007) Effect of selective cyclooxygenase-2 (COX-2) inhibitor treatment on glucose-stimulated insulin secretion in C57BL/6 mice. Biochem. Biophys. Res. Commun. 363, 37-43
21. Persaud, S. J., Burns, C. J., Belin, V. D., and Jones, P. M. (2004) Glucoseinduced regulation of COX-2 expression in human islets of Langerhans. Diabetes 53, S190-S192
22. Dennis, E. A., Cao, J., Hsu, Y.-H., Magrioti, V., and Kokotos, G. (2011) Phospholipase A2 Enzymes: Physical structure, biological function, disease implication, chemical inhibition, and therapeutic intervention. Chemical Reviews 111, 6130-6185
23. Chen, M., Yang, Z., Naji, A., and Wolf, B. A. (1996) Identification of calcium-dependent phospholipase A2 isoforms in human and rat pancreatic islets and insulin secreting beta-cell lines. Endocrinology 137, 2901-2909
24. Juhl, K., Høy, M., Olsen, H. L., Bokvist, K., Efanov, A. M., Hoffmann, E. K., and Gromada, J. (2003) cPLA2α-evoked formation of arachidonic acid and lysophospholipids is required for exocytosis in mouse pancreatic betacells. Am. J. Physiol. Endocrinol. Metab. 285, E73-E81
25. Jones, P. M., Burns, C. J., Belin, V. D., Roderigo-Milne, H. M., and Persaud, S. J. (2004) The role of cytosolic phospholipase A2 in insulin secretion. Diabetes 53, 5172-5178
26. Bao, S., Song, H., Wohltmann, M., Ramanadham, S., Jin, W., Bohrer, A., and Turk, J. (2006) Insulin secretory responses and phospholipid composition of pancreatic islets from mice that do not express group VIA Phospholipase A2 and effects of metabolic stress on glucose homeostasis. J. Biol. Chem. 281, 20958-20973
27. Song, K., Zhang, X., Zhao, C., Ang, N. T., and Ma, Z. A. (2005) Inhibition of Ca2 + -independent phospholipase A2 results in insufficient insulin secretion and impaired glucose tolerance. Mol. Endocrinol. 19, 504-515
28. Lambeau, G., and Gelb, M. H. (2008) Biochemistry and physiology of mammalian secreted phospholipases A2. Annu. Rev. Biochem. 77, 495-520
29. 2 Hydrolysis of Low-Density Lipoprotein Results in Spontaneous Particle Aggregation and Promotes Macrophage Foam Cell Formation. Arterioscler. Thromb. Vase. Biol. 24, 762-767
30. Shridas, P., Bailey, W. M., Gizard, F., Oslund, R. C., Gelb, M. H., Bruemmer, D., and Webb, N. R. (2010) Group X secretory phospholipase A2 negatively regulates ABCA1 and ABCG1 expression and cholesterol efflux in macrophages. Arterioscler. Thromb. Vasc. Biol. 30, 2014-2021
31. Shridas, P., Bailey, W. M., Boyanovsky, B. B., Oslund, R. C., Gelb, M. H., and Webb, N.R. (2010) Group X secretory phospholipase A2 regulates the expression of steroidogenic acute regulatory protein (StAR) in mouse adrenals. J. Biol. Chem. 285, 20031-20039
32. Degousee, N., Ghomashchi, F., Stefanski, E., Singer, A., Smart, B. P., Borregaard, N., Reithmeier, R., Lindsay, T. F., Lichtenberger, C., Reinisch, W., Lambeau, G., Arm, J., Tischfield, J., Gelb, M. H., and Rubin, B. B. (2002) Groups IV, V, and X phospholipases A2s in human neutrophils: role in eicosanoid production and gram-negative bacterial phospholipid hydrolysis. J. Biol. Chem. 277, 5061-5073
33. Morioka, Y., Ikeda, M., Saiga, A., Fujii, N., Ishimoto, Y., Arita, H., and Hanasaki, K. (2000) Potential role of group X secretory phospholipase A(2) in cyclooxygenase-2-dependent PGE(2) formation during colon tumorigenesis. FEBS Lett. 487, 262-266
34. Robertson, R. P., Tsai, P., Little, S. A., Zhang, H. J., and Walseth, T. F. (1987) Receptor-mediated adenylate cyclase-coupled mechanism for PGE2 inhibition of insulin secretion in HIT cells. Diabetes 36, 1047-1053
35. Newgard, C. B., and McGarry, J. D. (1995) Metabolic coupling factors in pancreatic beta-cell signal transduction. Annu. Rev. Biochem. 64, 689 -719
36. Ramanadham, S., Ma, Z., Arita, H., Zhang, S., and Turk, J. (1998) Type IB secretory phospholipase A2 is contained in insulin secretory granules of pancreatic islet beta-cells and is co-secreted with insulin from glucosestimulated islets. Biochim. Biophys. Acta 1390, 301-312
37. Ishida-Oku, M., Iwase, M., Sonoki, K., Sasaki, N., Imoto, H., and Uchizono, Y. (2010) Expression of secretory phospholipase A2 in insulitis of human transplanted pancreas and its insulinotropic effect on isolated rat islets. Islets 2, 274-277
38. Labonté, E. D., Kirby, R. J., Schildmeyer, N. M., Cannon, A. M., Huggins, K. W., and Hui, D. Y. (2006) Group IB phospholipase A2-mediated lysophospholipid absorption directly contributes to postprandial hyperglycemia. Diabetes 55, 935-941
39. Kennedy, B. P., Payette, P., Mudgett, J., Vadas, P., Pruzanski, W., Kwan, M., Tang, C., Rancourt, D. E., and Cromlish, W. A. (1995) A natural disruption of the secretory group II phospholipase A2 gene in inbred mouse strains. J. Biol. Chem. 270, 22378-22385
40. Murakami, M., Taketomi, Y., Mild, Y., Sato, H., Hirabayashi, T., and Yamamoto, K. (2011) Recent progress in phospholipase A(2) research: from cells to animals to humans. Prog. Lipid Res. 50, 152-192
41. Mounier, C. M., Ghomashchi, F., Lindsay, M. R., James, S., Singer, A. G., Parton, R. G., and Gelb, M. H. (2004) Arachidonic acid release from mammalian cells transfected with human groups IIA and X secreted phospholipase A(2) occurs predominantly during the secretory process and with the involvement of cytosolic phospholipase A(2)-α. J. Biol. Chem. 279, 25024-25038
42. Ohtsuki, M., Taketomi, Y., Arata, S., Masuda, S., Ishikawa, Y., Ishii, T., Takanezawa, Y., Aoki, J., Arai, H., Yamamoto, K., Kudo, I., and Murakami, M. (2006) Transgenic expression of group V, but not group X, secreted phospholipase A2 in mice leads to neonatal lethality because of lung dysfunction. J Biol. Chem. 281, 36420-36433
43. Li, X., Shridas, P., Forrest, K., Bailey, W., and Webb, N. R. (2010) Group X secretory phospholipase A2 negatively regulates adipogenesis in murine models. FASEB J. 24, 4313-4324
44. Fryirs, M., Barter, P. J., and Rye, K. A. (2009) Cholesterol metabolism and pancreatic beta-cell function. Curr. Opin. Lipidol. 20, 159-164
45. Kruit, J. K., Wijesekara, N., Westwell-Roper, C., Vanmierlo, T., de Haan, W., Bhattacharjee, A., Tang, R., Wellington, C. L., LütJohann, D., Johnson, J. D., Brunham, L. R., Verchere, C. B., and Hayden, M. R. (2012) Loss of both ABCA1 and ABCG1 results in increased disturbances in islet sterol homeostasis, inflammation, and impaired beta-cell function. Diabetes 61, 659-664
46. Cupillard, L., Koumanov, K., Mattéi, M.-G., Lazdunski, M., and Lambeau, G. (1997) Cloning, chromosomal mapping, and expression of a novel human secretory phospholipase A2.J. Biol. Chem. 272, 15745-15752
47. Jemel, I., Ii, H., Oslund, R. C., Payré, C., Dabert-Gay, A.-S., Douguet, D., Chargui, K., Scarzello, S., Gelb, M. H., and Lambeau, G. (2011) Group X secreted phospholipase A2 proenzyme is matured by a furin-like proprotein convertase and releases arachidonic acid inside of human HEK293 cells.J. Biol. Chem. 286, 36509-36521
48. Smeekens, S. P., Montag, A. G., Thomas, G., Albiges-Rizo, C., Carroll, R., Benig, M., Phillips, L. A., Martin, S., Ohagi, S., and Gardner, P. (1992) Proinsulin processing by the subtilisin-related proprotein convertases furin, PC2, and PC3. Proc. Natl. Acad. Sci. U.S.A. 89, 8822-8826
49. Bennett, D. L., Bailyes, E. M., Nielsen, E., Guest, P. C., Rutherford, N. G., Arden, S. D., and Hutton, J. C. (1992) Identification of the type 2 proinsulin processing endopeptidase as PC2, a member of the eukaryote subtilisin family. J. Biol. Chem. 267, 15229-15236