Hydroxyoctadecadienoic acids regulate apoptosis in human THP-1 cells in a PPARγ-dependent manner

Lipids

Volumn 49, Issue 12, 2014, Pages 1181-1192

  Vangaveti, Venkat N ^a   Shashidhar, Venkatesh M ^a   Rush, Catherine ^a   Malabu, Usman H ^a   Rasalam, Roy R ^a   Collier, Fiona ^b   Baune, Bernhard T ^c   Kennedy, Richard L ^b  

^a JAMES COOK UNIVERSITY   (Australia)

^b DEAKIN UNIVERSITY   (Australia)

^c UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Apoptosis; Macrophages; Monocytes; Oxidized lipids

Indexed keywords

13 HYDROXYOCTADECADIENOIC ACID; 2 CHLORO 5 NITRO N (4 PYRIDYL)BENZAMIDE; 9 HYDROXYOCTADECADIENOIC ACID; CAMPTOTHECIN; CASPASE 3; CASPASE 7; CASPASE INHIBITOR; DNA; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 132; LINOLEIC ACID; LINOLENIC ACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; ROSIGLITAZONE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; UNSATURATED FATTY ACID; 13-HYDROXY-9,11-OCTADECADIENOIC ACID; 2,4 THIAZOLIDINEDIONE DERIVATIVE; 9-HYDROXY-10,12-OCTADECADIENOIC ACID; CELL CYCLE PROTEIN; CONJUGATED LINOLEIC ACID; FABP4 PROTEIN, HUMAN; FATTY ACID BINDING PROTEIN; G2A RECEPTOR; HYDROXYOCTADECADIENOIC ACID;

APOPTOSIS; ARTICLE; ATHEROSCLEROSIS; CELL ADHESION; CELL COUNT; CELL VIABILITY; CONTROLLED STUDY; DNA FRAGMENTATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MACROPHAGE; MONOCYTE; PATHOGENESIS; AGONISTS; CELL LINE; CELL SURVIVAL; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; SIGNAL TRANSDUCTION;

ALPHA-LINOLENIC ACID; APOPTOSIS; CASPASE 3; CASPASE 7; CELL CYCLE PROTEINS; CELL LINE; CELL SURVIVAL; DNA FRAGMENTATION; FATTY ACID-BINDING PROTEINS; FATTY ACIDS, UNSATURATED; GENE EXPRESSION REGULATION; HUMANS; LINOLEIC ACID; LINOLEIC ACIDS; LINOLEIC ACIDS, CONJUGATED; MONOCYTES; PPAR GAMMA; RECEPTORS, G-PROTEIN-COUPLED; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; THIAZOLIDINEDIONES;

EID: 84922086230     PISSN: 00244201     EISSN: 15589307     Source Type: Journal    
DOI: 10.1007/s11745-014-3954-z     Document Type: Article

References (60)

1. Kuhn H, Belkner J, Wiesner R, Schewe T, Lankin VZ, Tikhaze AK (1992) Structure elucidation of oxygenated lipids in human atherosclerotic lesions. Eicosanoids 5:17-22
2. Jira W, Spiteller G, Carson W, Schramm A (1998) Strong increase in hydroxy fatty acids derived from linoleic acid in human low density lipoproteins of atherosclerotic patients. Chem Phys Lipids 91:1-11
3. Waddington E, Sienuarine K, Puddey I, Croft K (2001) Identification and quantitation of unique fatty acid oxidation products in human atherosclerotic plaque using high-performance liquid chromatography. Anal Biochem 292:234-244
4. Kuhn H, Belkner J, Zaiss S, Fahrenklemper T, Wohlfeil S (1994) Involvement of 15-lipoxygenase in early stages of atherogenesis. J Exp Med 179:1903-1911
5. Jostarndt K, Gellert N, Rubic T, Weber C, Kuhn H, Johansen B, Hrboticky N, Neuzil J (2002) Dissociation of apoptosis induction and CD36 upregulation by enzymatically modified low-density lipoprotein in monocytic cells. Biochem Biophys Res Commun 290:988-993
6. Vangaveti V, Baune BT, Kennedy RL (2010) Hydroxyoctadecadienoic acids: novel regulators of macrophage differentiation and atherogenesis. Ther Adv Endocrinol Metab 1:51-60
7. Brinckmann R, Kuhn H (1997) Regulation of 15-lipoxygenase expression by cytokines. Adv Exp Med Biol 400B:599-604
8. Waddington EI, Croft KD, Sienuarine K, Latham B, Puddey IB (2003) Fatty acid oxidation products in human atherosclerotic plaque: an analysis of clinical and histopathological correlates. Atherosclerosis 167:111-120
9. Upston JM, Neuzil J, Witting PK, Alleva R, Stocker R (1997) Oxidation of free fatty acids in low density lipoprotein by 15-lipoxygenase stimulates nonenzymic, alpha-tocopherol-mediated peroxidation of cholesteryl esters. J Biol Chem 272:30067-30074
10. Nagy L, Tontonoz P, Alvarez JG, Chen H, Evans RM (1998) Oxidized LDL regulates macrophage gene expression through ligand activation of PPARgamma. Cell 93:229-240
11. Han KH, Chang MK, Boullier A, Green SR, Li A, Glass CK, Quehenberger O (2000) Oxidized LDL reduces monocyte CCR2 expression through pathways involving peroxisome proliferator-activated receptor gamma. J Clin Invest 106:793-802
12. Ricote M, Welch JS, Glass CK (2000) Regulation of macrophage gene expression by the peroxisome proliferator-activated receptor-gamma. Horm Res 54:275-280
13. Inoue M, Itoh H, Tanaka T, Chun TH, Doi K, Fukunaga Y, Sawada N, Yamshita J, Masatsugu K, Saito T, Sakaguchi S, Sone M, Yamahara K, Yurugi T, Nakao K (2001) Oxidized LDL regulates vascular endothelial growth factor expression in human macrophages and endothelial cells through activation of peroxisome proliferator-activated receptor-gamma. Arterioscler Thromb Vasc Biol 21:560-566
14. Fu Y, Luo N, Lopes-Virella MF, Garvey WT (2002) The adipocyte lipid binding protein (ALBP/aP2) gene facilitates foam cell formation in human THP-1 macrophages. Atherosclerosis 165:259-269
15. Barbier O, Torra IP, Duguay Y, Blanquart C, Fruchart JC, Glineur C, Staels B (2002) Pleiotropic actions of peroxisome proliferator-activated receptors in lipid metabolism and atherosclerosis. Arterioscler Thromb Vasc Biol 22:717-726
16. Tabas I (2005) Consequences and therapeutic implications of macrophage apoptosis in atherosclerosis: the importance of lesion stage and phagocytic efficiency. Arterioscler Thromb Vasc Biol 25:2255-2264
17. Secchiero P, Corallini F, Pandolfi A, Consoli A, Candido R, Fabris B, Celeghini C, Capitani S, Zauli G (2006) An increased osteoprotegerin serum release characterizes the early onset of diabetes mellitus and may contribute to endothelial cell dysfunction. Am J Pathol 169:2236-2244
18. Stoneman V, Braganza D, Figg N, Mercer J, Lang R, Goddard M, Bennett M (2007) Monocyte/macrophage suppression in CD11b diphtheria toxin receptor transgenic mice differentially affects atherogenesis and established plaques. Circ Res 100:884-893
19. Ait-Oufella H, Pouresmail V, Simon T, Blanc-Brude O, Kinugawa K, Merval R, Offenstadt G, Leseche G, Cohen PL, Tedgui A, Mallat Z (2008) Defective mer receptor tyrosine kinase signaling in bone marrow cells promotes apoptotic cell accumulation and accelerates atherosclerosis. Arterioscler Thromb Vasc Biol 28:1429-1431
20. Thorp E, Cui D, Schrijvers DM, Kuriakose G, Tabas I (2008) Mertk receptor mutation reduces efferocytosis efficiency and promotes apoptotic cell accumulation and plaque necrosis in atherosclerotic lesions of apoe-/- mice. Arterioscler Thromb Vasc Biol 28:1421-1428
21. Thorp E, Li Y, Bao L, Yao PM, Kuriakose G, Rong J, Fisher EA, Tabas I, Thorp E, Li Y, Bao L, Yao PM, Kuriakose G, Rong J, Fisher EA, Tabas I (2009) Brief report: increased apoptosis in advanced atherosclerotic lesions of Apoe-/- mice lacking macrophage Bcl-2. Arterioscler Thromb Vasc Biol 29:169-172
22. Carpenter KLH, Challis IR, Arends MJ (2003) Mildly oxidised LDL induces more macrophage death than moderately oxidised LDL: roles of peroxidation, lipoprotein-associated phospholipase A2 and PPARgamma. FEBS Lett 553:145-150
23. Lizard G, Lemaire S, Monier S, Gueldry S, Néel D, Gambert P (1997) Induction of apoptosis and of interleukin-1β secretion by 7β-hydroxycholesterol and 7-ketocholesterol: partial inhibition by Bcl-2 overexpression. FEBS Lett 419:276-280
24. Rusinol AE, Thewke D, Liu J, Freeman N, Panini SR, Sinensky MS (2004) AKT/protein kinase B regulation of BCL family members during oxysterol-induced apoptosis. J Biol Chem 279:1392-1399
25. Hampel JKA, Brownrigg LM, Vignarajah D, Croft KD, Dharmarajan AM, Bentel JM, Puddey IB, Yeap BB (2006) Differential modulation of cell cycle, apoptosis and PPARgamma2 gene expression by PPARgamma agonists ciglitazone and 9-hydroxyoctadecadienoic acid in monocytic cells. Prostaglandins Leukot Essent Fatty Acids 74:283-293
26. Obinata H, Izumi T, Obinata H, Izumi T (2009) G2A as a receptor for oxidized free fatty acids. Prostaglandins Other Lipid Mediat 89:66-72
27. Yin H, Chu A, Li W, Wang B, Shelton F, Otero F, Nguyen DG, Caldwell JS, Chen YA, Yin H, Chu A, Li W, Wang B, Shelton F, Otero F, Nguyen DG, Caldwell JS, Chen YA (2009) Lipid G protein-coupled receptor ligand identification using beta-arrestin PathHunter assay. J Biol Chem 284:12328-12338
28. Vangaveti V, Shashidhar V, Jarrod G, Baune BT, Kennedy RL (2010) Free fatty acid receptors: emerging targets for treatment of diabetes and its complications. Ther Adv Endocrinol Metab 1:165-175
29. Rikitake Y, K-i Hirata, Yamashita T, Iwai K, Kobayashi S, Itoh H, Ozaki M, Ejiri J, Shiomi M, Inoue N, Kawashima S, Yokoyama M (2002) Expression of G2A, a receptor for lysophosphatidylcholine, by macrophages in murine, rabbit, and human atherosclerotic plaques. Arterioscler Thromb Vasc Biol 22:2049-2053
30. Bolick DT, Whetzel AM, Skaflen M, Deem TL, Lee J, Hedrick CC (2007) Absence of the G protein-coupled receptor G2A in mice promotes monocyte/endothelial interactions in aorta. Circ Res 100:572-580 (see comment)
31. Bolick DT, Skaflen MD, Johnson LE, Kwon SC, Howatt D, Daugherty A, Ravichandran KS, Hedrick CC, Bolick DT, Skaflen MD, Johnson LE, Kwon S-C, Howatt D, Daugherty A, Ravichandran KS, Hedrick CC (2009) G2A deficiency in mice promotes macrophage activation and atherosclerosis. Circ Res 104:318-327
32. Parks BW, Gambill GP, Lusis AJ, Kabarowski JHS (2005) Loss of G2A promotes macrophage accumulation in atherosclerotic lesions of low density lipoprotein receptor-deficient mice. J Lipid Res 46:1405-1415
33. Parks BW, Lusis AJ, Kabarowski JHS (2006) Loss of the lysophosphatidylcholine effector, G2A, ameliorates aortic atherosclerosis in low-density lipoprotein receptor knockout mice. Arterioscler Thromb Vasc Biol 26:2703-2709
34. Parks BW, Srivastava R, Yu S, Kabarowski JH, Parks BW, Srivastava R, Yu S, Kabarowski JHS (2009) ApoE-dependent modulation of HDL and atherosclerosis by G2A in LDL receptor-deficient mice independent of bone marrow-derived cells. Arterioscler Thromb Vasc Biol 29:539-547
35. Tsuchiya S, Kobayashi Y, Goto Y, Okumura H, Nakae S, Konno T, Tada K (1982) Induction of maturation in cultured human monocytic leukemia cells by a phorbol diester. Cancer Res 42:1530-1536
36. Baird SK, Hampton MB, Gieseg SP (2004) Oxidized LDL triggers phosphatidylserine exposure in human monocyte cell lines by both caspase-dependent and -independent mechanisms. FEBS Lett 578:169-174
37. Rutherford LD, Gieseg SP (2012) 7-ketocholesterol is not cytotoxic to U937 cells when incorporated into acetylated low density lipoprotein. Lipids 47:239-247
38. Wintergerst ES, Jelk J, Rahner C, Asmis R (2000) Apoptosis induced by oxidized low density lipoprotein in human monocyte-derived macrophages involves CD36 and activation of caspase-3. Eur J biochem/FEBS 267:6050-6059
39. Salvayre R, Auge N, Benoist H, Negre-Salvayre A, Salvayre R, Auge N, Benoist H, Negre-Salvayre A (2002) Oxidized low-density lipoprotein-induced apoptosis. Biochim Biophys Acta 1585:213-221
40. Hundal RS, Gomez-Munoz A, Kong JY, Salh BS, Marotta A, Duronio V, Steinbrecher UP, Hundal RS, Gomez-Munoz A, Kong JY, Salh BS, Marotta A, Duronio V, Steinbrecher UP (2003) Oxidized low density lipoprotein inhibits macrophage apoptosis by blocking ceramide generation, thereby maintaining protein kinase B activation and Bcl-XL levels. J Biol Chem 278:24399-24408
41. Namgaladze D, Kollas A, Brune B, Namgaladze D, Kollas A, Brune B (2008) Oxidized LDL attenuates apoptosis in monocytic cells by activating ERK signaling. J Lipid Res 49:58-65
42. Chen JH, Riazy M, Smith EM, Proud CG, Steinbrecher UP, Duronio V, Chen JH, Riazy M, Smith EM, Proud CG, Steinbrecher UP, Duronio V (2009) Oxidized LDL-mediated macrophage survival involves elongation factor-2 kinase. Arterioscler Thromb Vasc Biol 29:92-98
43. Vicca S, Hennequin C, Nguyen-Khoa T, Massy ZA, Descamps-Latscha B, Drueke TB, Lacour B (2000) Caspase-dependent apoptosis in THP-1 cells exposed to oxidized low-density lipoproteins. Biochem Biophys Res Commun 273:948-954
44. Boullier A, Li Y, Quehenberger O, Palinski W, Tabas I, Witztum JL, Miller YI, Boullier A, Li Y, Quehenberger O, Palinski W, Tabas I, Witztum JL, Miller YI (2006) Minimally oxidized LDL offsets the apoptotic effects of extensively oxidized LDL and free cholesterol in macrophages. Arterioscler Thromb Vasc Biol 26:1169-1176
45. Lee G, Elwood F, McNally J, Weiszmann J, Lindstrom M, Amaral K, Nakamura M, Miao S, Cao P, Learned RM (2002) T0070907, a selective ligand for peroxisome proliferator-activated receptor γ, functions as an antagonist of biochemical and cellular activities. J Biol Chem 277:19649-19657
46. Itoh T, Fairall L, Amin K, Inaba Y, Szanto A, Balint BL, Nagy L, Yamamoto K, Schwabe JWR (2008) Structural basis for the activation of PPARgamma by oxidized fatty acids. Nat Struct Mol Biol 15:924-931
47. Straus DS, Pascual G, Li M, Welch JS, Ricote M, Hsiang CH, Sengchanthalangsy LL, Ghosh G, Glass CK (2000) 15-deoxy-delta 12,14-prostaglandin J2 inhibits multiple steps in the NF-kappa B signaling pathway. Proc Natl Acad Sci USA 97:4844-4849
48. Castrillo A, Mojena M, Hortelano S, Bosca L (2001) Peroxisome proliferator-activated receptor-gamma-independent inhibition of macrophage activation by the non-thiazolidinedione agonist L-796,449. Comparison with the effects of 15-deoxy-delta(12,14)-prostaglandin J(2). J Biol Chem 276:34082-34088
49. Clay CE, Monjazeb A, Thorburn J, Chilton FH, High KP (2002) 15-Deoxy-delta12,14-prostaglandin J2-induced apoptosis does not require PPARgamma in breast cancer cells. J Lipid Res 43:1818-1828
50. Azuma Y, Watanabe K, Date M, Daito M, Ohura K, Azuma Y, Watanabe K, Date M, Daito M, Ohura K (2004) Induction of proliferation by 15-deoxy-delta12,14-prostaglandin J2 and the precursors in monocytic leukemia U937. Pharmacology 71:181-191
51. Wittwer J, Hersberger M (2007) The two faces of the 15-lipoxygenase in atherosclerosis. Prostaglandins Leukot Essent Fatty Acids 77:67-77
52. Kongkaneramit L, Sarisuta N, Azad N, Lu Y, Iyer AK, Wang L, Rojanasakul Y (2008) Dependence of reactive oxygen species and FLICE inhibitory protein on lipofectamine-induced apoptosis in human lung epithelial cells. J Pharmacol Exp Ther 325:969-977
53. Kiefer K, Clement J, Garidel P, Peschka-Suss R (2004) Transfection efficiency and cytotoxicity of nonviral gene transfer reagents in human smooth muscle and endothelial cells. Pharm Res 21:1009-1017
54. Yamano S, Dai J, Moursi AM (2010) Comparison of transfection efficiency of nonviral gene transfer reagents. Mol Biotechnol 46:287-300
55. Hattori T, Obinata H, Ogawa A, Kishi M, Tatei K, Ishikawa O, Izumi T, Hattori T, Obinata H, Ogawa A, Kishi M, Tatei K, Ishikawa O, Izumi T (2008) G2A plays proinflammatory roles in human keratinocytes under oxidative stress as a receptor for 9-hydroxyoctadecadienoic acid. J Invest Dermatol 128:1123-1133
56. Lin P, Ye RD (2003) The lysophospholipid receptor G2A activates a specific combination of G proteins and promotes apoptosis. J Biol Chem 278:14379-14386
57. Xie S, Lee YF, Kim E, Chen LM, Ni J, Fang LY, Liu S, Lin SJ, Abe J, Berk B, Ho FM, Chang C, Xie S, Lee Y-F, Kim E, Chen L-M, Ni J, Fang L-Y, Liu S, Lin S-J, Abe J-I, Berk B, Ho F-M, Chang C (2009) TR4 nuclear receptor functions as a fatty acid sensor to modulate CD36 expression and foam cell formation. Proc Natl Acad Sci USA 106:13353-13358
58. Patwardhan AM, Scotland PE, Akopian AN, Hargreaves KM (2009) Activation of TRPV1 in the spinal cord by oxidized linoleic acid metabolites contributes to inflammatory hyperalgesia. Proc Natl Acad Sci USA 106:18820-18824
59. Patwardhan AM, Akopian AN, Ruparel NB, Diogenes A, Weintraub ST, Uhlson C, Murphy RC, Hargreaves KM (2010) Heat generates oxidized linoleic acid metabolites that activate TRPV1 and produce pain in rodents. J Clin Invest 120:1617-1626
60. Zhao L, Funk CD (2004) Lipoxygenase pathways in atherogenesis. Trends Cardiovasc Med 14:191-195