Diabetes-induced oxidative stress is mediated by Ca2+- independent phospholipase A2 in neutrophils

Journal of Immunology

Volumn 184, Issue 3, 2010, Pages 1507-1515

  Ayilavarapu, Srinivas ^a   Kantarci, Alpdogan ^a   Fredman, Gabrielle ^a   Turkoglu, Oya ^a   Omori, Kazuhiro ^b   Liu, Hongsheng ^a   Iwata, Tomoyuki ^a   Yagi, Motohiko ^c   Hasturk, Hatice ^a   Van Dyke, Thomas E ^a  

^a BOSTON UNIVERSITY   (United States)

^b OKAYAMA UNIVERSITY   (Japan)

^c NIHON UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ARACHIDONIC ACID; BROMOENOL LACTONE; CALCIUM ION; FORMYLMETHIONYLLEUCYLPHENYLALANINE; PHOSPHOLIPASE A2; PROTEIN S100B; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SMALL INTERFERING RNA; SUPEROXIDE; CALCIUM; PHOSPHATIDATE PHOSPHATASE; PHOSPHOLIPASE A2 GROUP VI; PLA2G6 PROTEIN, HUMAN; PROTEIN KINASE C;

ADULT; ARTICLE; CELL ISOLATION; CELL STRAIN HL 60; CONTROLLED STUDY; DIABETES MELLITUS; ENZYME ACTIVITY; FEMALE; GENE SILENCING; HUMAN; HUMAN CELL; HYPERGLYCEMIA; IN VITRO STUDY; MAJOR CLINICAL STUDY; MALE; NEUTROPHIL; OXIDATIVE STRESS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; WESTERN BLOTTING; BLOOD; DRUG ANTAGONISM; ENZYMOLOGY; GENE TARGETING; GENETICS; IMMUNOLOGY; INSULIN DEPENDENT DIABETES MELLITUS; METABOLISM; MIDDLE AGED; NON INSULIN DEPENDENT DIABETES MELLITUS; PHYSIOLOGY; SIGNAL TRANSDUCTION; UPREGULATION;

ADULT; CALCIUM; DIABETES MELLITUS, TYPE 1; DIABETES MELLITUS, TYPE 2; FEMALE; GENE TARGETING; GROUP VI PHOSPHOLIPASES A2; HL-60 CELLS; HUMANS; MALE; MIDDLE AGED; NEUTROPHILS; OXIDATIVE STRESS; PHOSPHATIDATE PHOSPHATASE; PROTEIN KINASE C; SIGNAL TRANSDUCTION; SUPEROXIDES; UP-REGULATION;

EID: 77949322314     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0901219     Document Type: Article

References (38)

1. Wierusz-Wysocka, B., H.Wysocki, H. Siekierka, A. Wykretowicz, A. Szczepanik, and R. Klimas. 1987. Evidence of polymorphonuclear neutrophils (PMN) activation in patients with insulin-dependent diabetes mellitus. J. Leukoc. Biol. 42: 519-523.
2. Hand, W. L., D. L. Hand, and Y. Vasquez. 2007. Increased polymorphonuclear leukocyte respiratory burst function in type 2 diabetes. Diabetes Res. Clin. Pract. 76: 44-50.
3. Gupta, A., A. K. Tripathi, R. L. Tripathi, S. V. Madhu, and B. D. Banerjee. 2007. Advanced glycosylated end products-mediated activation of polymorphonuclear neutrophils in diabetes mellitus and associated oxidative stress. Indian J. Biochem. Biophys. 44: 373-378.
4. Omori, K., T. Ohira, Y. Uchida, S. Ayilavarapu, E. L. Batista Jr., M. Yagi, T. Iwata, H. Liu, H. Hasturk, A. Kantarci, and T. E. Van Dyke. 2008. Priming of neutrophil oxidative burst in diabetes requires preassembly of the NADPH oxidase. J. Leukoc. Biol. 84: 292-301.
5. Karima, M., A. Kantarci, T. Ohira, H. Hasturk, V. L. Jones, B. H. Nam, A. Malabanan, P. C. Trackman, J. A. Badwey, and T. E. Van Dyke. 2005. Enhanced superoxide release and elevated protein kinase C activity in neutrophils from diabetic patients: association with periodontitis. J. Leukoc. Biol. 78: 862-870.
6. Gyurko, R., C. C. Siqueira, N. Caldon, L. Gao, A. Kantarci, and T. E. Van Dyke. 2006. Chronic hyperglycemia predisposes to exaggerated inflammatory response and leukocyte dysfunction in Akita mice. J. Immunol. 177: 7250-7256. (Pubitemid 44715094)
7. Ding, Y., A. Kantarci, H. Hasturk, P. C. Trackman, A. Malabanan, and T. E. Van Dyke. 2007. Activation of RAGE induces elevated O2- generation by mononuclear phagocytes in diabetes. J. Leukoc. Biol. 81: 520-527.
8. Sheppard, F. R., M. R. Kelher, E. E. Moore, N. J. McLaughlin, A. Banerjee, and C. C. Silliman. 2005. Structural organization of the neutrophil NADPH oxidase: phosphorylation and translocation during priming and activation. J. Leukoc. Biol. 78: 1025-1042.
9. Burg, N. D., and M. H. Pillinger. 2001. The neutrophil: function and regulation in innate and humoral immunity. Clin. Immunol. 99: 7-17.
10. Dana, R., H. L. Malech, and R. Levy. 1994. The requirement for phospholipase A2 for activation of the assembled NADPH oxidase in human neutrophils. Biochem. J. 297: 217-223. (Pubitemid 2023784)
11. Shmelzer, Z., N. Haddad, E. Admon, I. Pessach, T. L. Leto, Z. Eitan-Hazan, M. Hershfinkel, and R. Levy. 2003. Unique targeting of cytosolic phospholipase A2 to plasma membranes mediated by the NADPH oxidase in phagocytes. J. Cell Biol. 162: 683-692. (Pubitemid 37022945)
12. Henderson, L. M., J. B. Chappell, and O. T. Jones. 1989. Superoxide generation is inhibited by phospholipase A2 inhibitors. Role for phospholipase A2 in the activation of the NADPH oxidase. Biochem. J. 264: 249-255.
13. Balsinde, J., M. V. Winstead, and E. A. Dennis. 2002. Phospholipase A(2) regulation of arachidonic acid mobilization. FEBS Lett. 531: 2-6.
14. Balsinde, J., and M. A. Balboa. 2005. Cellular regulation and proposed biological functions of group VIA calcium-independent phospholipase A2 in activated cells. Cell. Signal. 17: 1052-1062.
15. Schaloske, R. H., and E. A. Dennis. 2006. The phospholipase A2 superfamily and its group numbering system. Biochim. Biophys. Acta 1761: 1246-1259.
16. Gilroy, D. W., J. Newson, P. Sawmynaden, D. A. Willoughby, and J. D. Croxtall. 2004. A novel role for phospholipase A2 isoforms in the checkpoint control of acute inflammation. FASEB J. 18: 489-498.
17. Rubin, B. B., G. P. Downey, A. Koh, N. Degousee, F. Ghomashchi, L. Nallan, E. Stefanski, D. W. Harkin, C. Sun, B. P. Smart, et al. 2005. Cytosolic phospholipase A2-α is necessary for platelet-activating factor biosynthesis, efficient neutrophil-mediated bacterial killing, and the innate immune response to pulmonary infection: cPLA2-α does not regulate neutrophil NADPH oxidase activity. J. Biol. Chem. 280: 7519-7529.
18. Tithof, P. K., M. Peters-Golden, and P. E. Ganey. 1998. Distinct phospholipases A2 regulate the release of arachidonic acid for eicosanoid production and superoxide anion generation in neutrophils. J. Immunol. 160: 953-960.
19. Wong, R. K. M., A. I. Pettit, P. A. Quinn, S. C. Jennings, J. E. Davies, and L. L. Ng. 2003. Advanced glycation end products stimulate an enhanced neutrophil respiratory burst mediated through the activation of cytosolic phospholipase A2 and generation of arachidonic Acid. Circulation 108: 1858-1864.
20. Expert Committee on the Diagnosis and Classification of Diabetes Mellitus. 2000. Report of the Expert Committee on the Diagnosis and Classification of Diabetes Mellitus. Diabetes Care 23(Suppl 1): S4-S19.
21. Smani, T., S. I. Zakharov, P. Csutora, E. Leno, E. S. Trepakova, and V. M. Bolotina. 2004. A novel mechanism for the store-operated calcium influx pathway. Nat. Cell Biol. 6: 113-120.
22. Csutora, P., V. Zarayskiy, K. Peter, F. Monje, T. Smani, S. I. Zakharov, D. Litvinov, and V. M. Bolotina. 2006. Activation mechanism for CRAC current and store-operated Ca2+ entry: calcium influx factor and Ca2+-independent phospholipase A2beta-mediated pathway. J. Biol. Chem. 281: 34926-34935.
23. Fuentes, L., R. Pérez, M. L. Nieto, J. Balsinde, and M. A. Balboa. 2003. Bromoenol lactone promotes cell death by a mechanism involving phosphatidate phosphohydrolase-1 rather than calcium-independent phospholipase A2. J. Biol. Chem. 278: 44683-44690.
24. Dewas, C., M. Fay, M. A. Gougerot-Pocidalo, and J. El-Benna. 2000. The mitogen-activated protein kinase extracellular signal-regulated kinase 1/2 pathway is involved in formyl-methionyl-leucyl-phenylalanine-induced p47phox phosphorylation in human neutrophils. J. Immunol. 165: 5238-5244.
25. Dang, P. M., A. Fontayne, J. Hakim, J. El Benna, and A. Périanin. 2001. Protein kinase C zeta phosphorylates a subset of selective sites of the NADPH oxidase component p47phox and participates in formyl peptide-mediated neutrophil respiratory burst. J. Immunol. 166: 1206-1213.
26. Ohira, T., Q. Zhan, Q. Ge, T. VanDyke, and J. A. Badwey. 2003. Protein phosphorylation in neutrophils monitored with phosphospecific antibodies. J. Immunol. Methods 281: 79-94. (Pubitemid 37324572)
27. Ding, Y., A. Kantarci, J. A. Badwey, H. Hasturk, A. Malabanan, and T. E. Van Dyke. 2007. Phosphorylation of pleckstrin increases proinflammatory cytokine secretion by mononuclear phagocytes in diabetes mellitus. J. Immunol. 179: 647-654. (Pubitemid 46986583)
28. Hazen, S. L., L. A. Zupan, R. H. Weiss, D. P. Getman, and R. W. Gross. 1991. Suicide inhibition of canine myocardial cytosolic calcium-independent phospholipase A2. Mechanism-based discrimination between calcium-dependent and -independent phospholipases A2. J. Biol. Chem. 266: 7227-7232.
29. Dana, R., T. L. Leto, H. L. Malech, and R. Levy. 1998. Essential requirement of cytosolic phospholipase A2 for activation of the phagocyte NADPH oxidase. J. Biol. Chem. 273: 441-445.
30. Jenkins, C.M., M. J.Wolf, D. J.Mancuso, and R.W. Gross. 2001. Identification of the calmodulin-binding domain of recombinant calcium-independent phospholipase A2beta. implications for structure and function. J. Biol. Chem. 276: 7129-7135.
31. Balsinde, J., and E. A. Dennis. 1996. Distinct roles in signal transduction for each of the phospholipase A2 enzymes present in P388D1 macrophages. J. Biol. Chem. 271: 6758-6765.
32. Underwood, K. W., C. Song, R. W. Kriz, X. J. Chang, J. L. Knopf, and L.-L. Lin. 1998. A novel calcium-independent phospholipase A2, cPLA2-γ, that is prenylated and contains homology to cPLA2. J. Biol. Chem. 273: 21926-21932.
33. Mollapour, E., D. C. Linch, and P. J. Roberts. 2001. Activation and priming of neutrophil nicotinamide adenine dinucleotide phosphate oxidase and phospholipase A(2) are dissociated by inhibitors of the kinases p42(ERK2) and p38(SAPK) and by methyl arachidonyl fluorophosphonate, the dual inhibitor of cytosolic and calcium-independent phospholipase A(2). Blood 97: 2469-2477.
34. Henderson, L. M., and J. B. Chappell. 1992. The NADPH-oxidase-associated H+ channel is opened by arachidonate. Biochem. J. 283: 171-175.
35. Serezani, C. H., J. Chung, M. N. Ballinger, B. B. Moore, D. M. Aronoff, and M. Peters- Golden. 2007. Prostaglandin E2 suppresses bacterial killing in alveolar macrophages by inhibiting NADPH oxidase. Am. J. Respir. Cell Mol. Biol. 37: 562-570.
36. O'Dowd, Y. M., J. El-Benna, A. Perianin, and P. Newsholme. 2004. Inhibition of formyl-methionyl-leucyl-phenylalanine-stimulated respiratory burst in human neutrophils by adrenaline: inhibition of Phospholipase A2 activity but not p47phox phosphorylation and translocation. Biochem. Pharmacol. 67: 183-190.
37. Bauldry, S. A., and R. E. Wooten. 1997. Induction of cytosolic phospholipase A2 activity by phosphatidic acid and diglycerides in permeabilized human neutrophils: interrelationship between phospholipases D and A2. Biochem. J. 322: 353-363.
38. Magalhães, M. A., F. Zhu, H. Sarantis, S. D. Gray-Owen, R. P. Ellen, and M. Glogauer. 2007. Expression and translocation of fluorescent-tagged p21-activated kinase-binding domain and PH domain of protein kinase B during murine neutrophil chemotaxis. J. Leukoc. Biol. 82: 559-566.