Smooth muscle-specific expression of calcium-independent phospholipase A2β (iPLA2β) participates in the initiation and early progression of vascular inflammation and neointima formation

Journal of Biological Chemistry

Volumn 287, Issue 29, 2012, Pages 24739-24753

  Liu, Shu ^a   Xie, Zhongwen ^a   Zhao, Qingwei ^a   Pang, Huan ^a   Turk, John ^b   Calderon, Lindsay ^a   Su, Wen ^a   Zhao, Guogang ^a   Xu, Haifei ^a   Gong, Ming C ^a   Guo, Zhenheng ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN II; ANTISENSE OLIGONUCLEOTIDES; ARACHIDONIC ACIDS; CARDIO-VASCULAR DISEASE; CAROTID ARTERY; NEOINTIMA FORMATION; NORDIHYDROGUAIARETIC ACID; PHOSPHOLIPASE A; PROINFLAMMATORY CYTOKINES; SMOOTH MUSCLE CELLS; SMOOTH MUSCLES; THERAPEUTIC TARGETS; TRANSGENIC MICE; VASCULAR SMOOTH MUSCLE CELLS;

CELLS; ENZYME INHIBITION; IMMUNOLOGY; MUSCLE;

PLANTS (BOTANY);

ANGIOTENSIN II; ANTISENSE OLIGODEOXYNUCLEOTIDE; ARACHIDONATE 12 LIPOXYGENASE; ARACHIDONATE 15 LIPOXYGENASE; ARACHIDONIC ACID; BROMOENOL LACTONE; CALCIUM INDEPENDENT PHOSPHOLIPASE A2; CALCIUM INDEPENDENT PHOSPHOLIPASE A2 BETA; INTERLEUKIN 6; LUTEOLIN; MESSENGER RNA; NORDIHYDROGUAIARETIC ACID; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CAROTID ARTERY LIGATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE COURSE; ENZYME ACTIVITY; ENZYME INHIBITION; GENE DELETION; MACROPHAGE MIGRATION; MALE; MOUSE; NEOINTIMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SMOOTH MUSCLE; SMOOTH MUSCLE FIBER; TUNICA MEDIA; VASCULITIS;

ANGIOTENSIN II; ANIMALS; BLOTTING, WESTERN; CALCIUM; CAROTID ARTERIES; CELLS, CULTURED; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MUSCLE, SMOOTH, VASCULAR; NEOINTIMA; OLIGONUCLEOTIDES, ANTISENSE; PHOSPHOLIPASES A2, CALCIUM-INDEPENDENT; POLYMERASE CHAIN REACTION; PROMOTER REGIONS, GENETIC; RABBITS; RATS; RATS, SPRAGUE-DAWLEY;

MUS MUSCULUS;

EID: 84863808523     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.340216     Document Type: Article

References (51)

1. Schwartz, S. M., deBlois, D., and O'Brien, E. R. (1995) The intima. Soil for atherosclerosis and restenosis. Circ. Res. 77, 445-465
2. Ross, R. (1999) Atherosclerosis is an inflammatory disease. Am. Heart J. 138, S419-S420
3. Libby, P. (2002) Inflammation in atherosclerosis. Nature 420, 868-874
4. Costa, M. A., and Simon, D. I. (2005) Molecular basis of restenosis and drug-eluting stents. Circulation 111, 2257-2273 (Pubitemid 40632443)
5. Glass, C. K., and Witztum, J. L. (2001) Atherosclerosis. The road ahead. Cell 104, 503-516
6. Owens, G. K., Kumar, M. S., and Wamhoff, B. R. (2004) Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol. Rev. 84, 767-801 (Pubitemid 38823766)
7. Schober, A., and Weber, C. (2005) Mechanisms of monocyte recruitment in vascular repair after injury. Antioxid. Redox. Signal. 7, 1249-1257 (Pubitemid 41232521)
8. Doran, A. C., Meller, N., and McNamara, C. A. (2008) Role of smooth muscle cells in the initiation and early progression of atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 28, 812-819 (Pubitemid 351544093)
9. Raines, E. W., and Ferri, N. (2005) Thematic review series. The immune system and atherogenesis. Cytokines affecting endothelial and smooth muscle cells in vascular disease. J. Lipid Res. 46, 1081-1092 (Pubitemid 43109823)
10. 2. J. Biol. Chem. 269, 13057-13060
11. 2. Mechanism-based discrimination between calcium-dependent and -independent phospholipases A2. J. Biol. Chem. 266, 7227-7232
12. 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, S63-S68
13. 2+-independent phospholipase A2. Prog. Nucleic Acids Res. Mol. Biol. 67, 1-33
14. Murakami, M., Taketomi, Y., Miki, Y., Sato, H., Hirabayashi, T., and Yamamoto, K. (2011) Recent progress in phospholipaseA2 research. From cells to animals to humans. Prog. Lipid Res. 50, 152-192
15. Natarajan, R., and Nadler, J. L. (2004) Lipid inflammatory mediators in diabetic vascular disease. Arterioscler. Thromb. Vasc. Biol. 24, 1542-1548 (Pubitemid 39180875)
16. Xie, Z., Gong, M. C., Su, W., Turk, J., and Guo, Z. (2007) Group VIA phospholipase A2 (iPLA2β) 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 (Pubitemid 47372835)
17. 2 in thrombin-induced arachidonic acid release and growth in vascular smooth muscle cells. J. Biol. Chem. 278, 43831-43837
18. Smani, T., Zakharov, S. I., Csutora, P., Leno, E., Trepakova, E. S., and Bolotina, V. M. (2004) A novel mechanism for the store-operated calcium influx pathway. Nat. Cell Biol. 6, 113-120 (Pubitemid 38425710)
19. 2+ sensitization of contraction in vascular smooth muscle. J. Biol. Chem. 278, 1856-1863
20. 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
21. 2 (iPLA2) β, and not iPLA2γ, as the mediator of arginine vasopressin-induced arachidonic acid release in A-10 smooth muscle cells. Enantioselective mechanism-based discrimination of mammalian iPLA2s. J. Biol. Chem. 277, 32807-32814
22. 8]vasopressin is largely mediated by calcium-independent phospholipase A2. J. Biol. Chem. 268, 20713-20716
23. 2&beta. J. Biol. Chem. 283, 33975-33987
24. Xie, Z., Liu, D., Liu, S., Calderon, L., Zhao, G., Turk, J., and Guo, Z. (2011) Identification of a cAMP-response element in the regulator of G-protein signaling-2 (RGS2) promoter as a key cis-regulatory element for RGS2 transcriptional regulation by angiotensin II in cultured vascular smooth muscles. J. Biol. Chem. 286, 44646-44658
25. Bao, S., Miller, D. J., Ma, Z., Wohltmann, M., Eng, G., Ramanadham, S., Moley, K., and Turk, J. (2004) Male mice that do not express group VIA phospholipase A2 produce spermatozoa with impaired motility and have greatly reduced fertility. J. Biol. Chem. 279, 38194-38200 (Pubitemid 39295966)
26. Kallmeier, R. C., Somasundaram, C., and Babij, P. (1995) A novel smooth muscle-specific enhancer regulates transcription of the smooth muscle myosin heavy chain gene in vascular smooth muscle cells. J. Biol. Chem. 270, 30949-30957 (Pubitemid 26012179)
27. Kumar, A., and Lindner, V. (1997) Remodeling with neointima formation in the mouse carotid artery after cessation of blood flow. Arterioscler. Thromb. Vasc. Biol. 17, 2238-2244 (Pubitemid 28057127)
28. Villa, A. E., Guzman, L. A., Poptic, E. J., Labhasetwar, V., D'Souza, S., Farrell, C. L., Plow, E. F., Levy, R. J., DiCorleto, P. E., and Topol, E. J. (1995) Effects of antisense c-Myb oligonucleotides on vascular smooth muscle cell proliferation and response to vessel wall injury. Circ. Res. 76, 505-513
29. Guo, Z., Su, W., Allen, S., Pang, H., Daugherty, A., Smart, E., and Gong, M. C. (2005) COX-2 up-regulation and vascular smooth muscle contractile hyper-reactivity in spontaneous diabetic db/db mice. Cardiovasc. Res. 67, 723-735 (Pubitemid 41033368)
30. Pang, H., Guo, Z., Su, W., Xie, Z., Eto, M., and Gong, M. C. (2005) RhoARho kinase pathway mediates thrombin- and U-46619-induced phosphorylation of a myosin phosphatase inhibitor, CPI-17, in vascular smooth muscle cells. Am. J. Physiol. Cell Physiol. 289, C352-C360 (Pubitemid 41014837)
31. Pang, H., Guo, Z., Xie, Z., Su, W., and Gong, M. C. (2006) Divergent kinase signaling mediates agonist-induced phosphorylation of phosphatase inhibitory proteins PHI-1 and CPI-17 in vascular smooth muscle cells. Am. J. Physiol. Cell Physiol 290, C892-C899
32. Xie, Z., Su, W., Guo, Z., Pang, H., Post, S. R., and Gong, M. C. (2006) Up-regulation of CPI-17 phosphorylation in diabetic vasculature and high glucose cultured vascular smooth muscle cells. Cardiovasc. Res. 69, 491-501 (Pubitemid 43098805)
33. Su, W., Guo, Z., Randall, D. C., Cassis, L., Brown, D. R., and Gong, M. C. (2008) Hypertension and disrupted blood pressure circadian rhythm in type 2 diabetic db/db mice. Am. J. Physiol. Heart Circ. Physiol. 295, H1634-H1641
34. 2 family members possessing triacylglycerol lipase and acylglycerol transacylase activities. J. Biol. Chem. 279, 48968-48975
35. 2by generating a diffusible bromomethyl keto acid that alkylates cysteine thiols. Biochemistry 45, 1061-1073
36. Harmon, K. J., Couper, L. L., and Lindner, V. (2000) Strain-dependent vascular remodeling phenotypes in inbred mice. Am. J. Pathol. 156, 1741-1748 (Pubitemid 30646711)
37. Stec, D. E., Morimoto, S., and Sigmund, C. D. (2001) Vectors for high level expression of cDNAs controlled by tissue-specific promoters in transgenic mice. BioTechniques 31, 256-260 (Pubitemid 32747577)
38. Kumar, A., Hoover, J. L., Simmons, C. A., Lindner, V., and Shebuski, R. J. (1997) Remodeling and neointimal formation in the carotid artery of normal and P-selectin-deficient mice. Circulation 96, 4333-4342 (Pubitemid 28007463)
39. Rectenwald, J. E., Moldawer, L. L., Huber, T. S., Seeger, J. M., and Ozaki, C. K. (2000) Direct evidence for cytokine involvement in neointimal hyperplasia. Circulation 102, 1697-1702
40. Balsinde, J., and Dennis, E. A. (1997) Function and inhibition of intracellular calcium-independent phospholipase A2. J. Biol. Chem. 272, 16069-16072 (Pubitemid 27276415)
41. 2 in cell growth and signaling. Biochem. Pharmacol. 76, 1059-1067
42. 2 isoforms by TNF-α and IL-1β in adult rat ventricular myocytes. Am. J. Physiol. 275, H1462-H1472
43. 2 expression by sterol availability. Biochim. Biophys. Acta 1684, 29-37
44. 2 expression. A role for regulation by SREBP-1. J. Biol. Chem. 285, 6693-6705
45. Zhou, R. H., Pesant, S., Cohn, H. I., and Eckhart, A. D. (2008) Enhanced sterol response element-binding protein in postintervention restenotic blood vessels plays an important role in vascular smooth muscle proliferation. Life Sci. 82, 174-181
46. Wolf, M. J., Wang, J., Turk, J., and Gross, R. W. (1997) Depletion of intracellular calcium stores activates smooth muscle cell calcium-independent phospholipase A2. A novel mechanism underlying arachidonic acid mobilization. J. Biol. Chem. 272, 1522-1526 (Pubitemid 27043230)
47. Natarajan, R., Reddy, M. A., Malik, K. U., Fatima, S., and Khan, B. V. (2001) Signaling mechanisms of nuclear factor-κB-mediated activation of inflammatory genes by 13-hydroperoxyoctadecadienoic acid in cultured vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 21, 1408-1413 (Pubitemid 34219800)
48. Dwarakanath, R. S., Sahar, S., Reddy, M. A., Castanotto, D., Rossi, J. J., and Natarajan, R. (2004) Regulation of monocyte chemoattractant protein-1 by the oxidized lipid, 13-hydroperoxyoctadecadienoic acid, in vascular smooth muscle cells via nuclear factor-κB (NF-κB). J. Mol. Cell. Cardiol. 36, 585-595 (Pubitemid 38469949)
49. Chava, K. R., Karpurapu, M., Wang, D., Bhanoori, M., Kundumani-Sridharan, V., Zhang, Q., Ichiki, T., Glasgow, W. C., and Rao, G. N. (2009) CREB-mediated IL-6 expression is required for 15(S)-hydroxyeicosatetraenoic acid-induced vascular smooth muscle cell migration. Arterioscler. Thromb. Vasc. Biol. 29, 809-815
50. Walev, I., Klein, J., Husmann, M., Valeva, A., Strauch, S., Wirtz, H., Weichel, O., and Bhakdi, S. (2000) Potassium regulates IL-1β processing via calcium-independent phospholipase A2. J. Immunol. 164, 5120-5124 (Pubitemid 30305186)
51. 2β is dispensable in inflammasome activation and its inhibition by bromoenol lactone. J. Innate Immun. 1, 607-617