Cyclooxygenase-2 dependent metabolism of 20-hete increases adiposity and adipocyte enlargement in mesenchymal stem cell-derived adipocytes

Journal of Lipid Research

Volumn 54, Issue 3, 2013, Pages 786-793

  Kim, Dong Hyun ^a   Puri, Nitin ^b   Sodhi, Komal ^b   Falck, John R ^c   Abraham, Nader G ^a   Shapiro, Joseph ^a   Schwartzman, Michal L ^d  

^a MARSHALL UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MEDICAL COLLEGE OF OHIO   (United States)

^c UNIVERSITY OF TEXAS AT DALLAS   (United States)

^d NEW YORK MEDICAL COLLEGE   (United States)

Author keywords

Adipogenesis; Arachidonic acid; Mesenchymal stem cells

Indexed keywords

20 HYDROXY PROSTAGLANDIN E2; 20 HYDROXYICOSATETRAENOIC ACID; BETA CATENIN; CYCLOOXYGENASE 2; CYTOCHROME P450; CYTOCHROME P450 4A11; CYTOCHROME P450 4F2; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROSTAGLANDIN E2 DERIVATIVE; UNCLASSIFIED DRUG;

ADIPOCYTE; ADIPOGENESIS; ARTICLE; CELL DIFFERENTIATION; CELL ENLARGEMENT; CONCENTRATION RESPONSE; CONTROLLED STUDY; FATTY ACID METABOLISM; HUMAN; HUMAN CELL; HYPERTROPHY; INFLAMMATION; LIPID STORAGE; MESENCHYMAL STEM CELL; OBESITY; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION;

ADIPOCYTES; ADIPOSITY; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELLS, CULTURED; CYCLOOXYGENASE 2; HUMANS; HYDROXYEICOSATETRAENOIC ACIDS; MESENCHYMAL STROMAL CELLS; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84874025141     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M033894     Document Type: Article

References (47)

1. Hung, W. W., T. J. Hsieh, T. Lin, P. C. Chou, P. J. Hsiao, K. D. Lin, and S. J. Shin. 2011. Blockade of the renin-angiotensin system ameliorates apelin production in 3T3-L1 adipocytes. Cardiovasc. Drugs Ther. 25 : 3-12.
2. Matsushita, K., Y. Wu, Y. Okamoto, R. E. Pratt, and V. J. Dzau. 2006. Local renin angiotensin expression regulates human mesenchymal stem cell differentiation to adipocytes. Hypertension. 48 : 1095-1102.
3. Sodhi, K., N. Puri, K. Inoue, J. R. Falck, M. L. Schwartzman, and N. G. Abraham. 2012. EET agonist prevents adiposity and vascular dysfunction in rats fed a high fat diet via a decrease in Bach 1 and an increase in HO-1 levels. Prostaglandins Other Lipid Mediat. 98 : 133-142.
4. Allende-Vigo, M. Z. 2012. Adipocytes and cardiometabolic risk. Am. J. Ther. 19 : 294-299.
5. Espiritu, D. J., and T. Mazzone. 2008. Oxidative stress regulates adipocyte apolipoprotein E and suppresses its expression in obesity. Diabetes. 57 : 2992-2998.
6. Kim, D. H., A. P. Burgess, M. Li, P. L. Tsenovoy, F. Addabbo, J. A. McClung, N. Puri, and N. G. Abraham. 2008. Heme oxygenasemediated increases in adiponectin decrease fat content and infl ammatory cytokines, tumor necrosis factor-alpha and interleukin-6 in Zucker rats and reduce adipogenesis in human mesenchymal stem cells. J. Pharmacol. Exp. Ther. 325 : 833-840.
7. Puri, N., K. Sodhi, M. Haarstad, D. H. Kim, S. Bohinc, E. Foglio, G. Favero, and N. G. Abraham. 2012. Heme induced oxidative stress attenuates sirtuin1 and enhances adipogenesis in mesenchymal stem cells and mouse pre-adipocytes. J. Cell. Biochem. 113 : 1926-1935.
8. Chu, X., L. Xu, K. Nishimura, M. Jisaka, T. Nagaya, F. Shono, and K. Yokota. 2009. Suppression of adipogenesis program in cultured preadipocytes transfected stably with cyclooxygenase isoforms. Biochim. Biophys. Acta. 1791 : 273-280.
9. Sodhi, K., C. C. Wu, J. Cheng, K. Gotlinger, K. Inoue, M. Goli, J. R. Falck, N. G. Abraham, and M. L. Schwartzman. 2010. CYP4A2-induced hypertension is 20-hydroxyeicosatetraenoic acid-and angiotensin II-dependent. Hypertension. 56 : 871-878.
10. Moreno, C., K. G. Maier, K. M. Hoagland, M. Yu, and R. J. Roman. 2001. Abnormal pressure-natriuresis in hypertension: role of cytochrome P450 metabolites of arachidonic acid. Am. J. Hypertens. 14 : 90S-97S.
11. Miyata, N., and R. J. Roman. 2005. Role of 20-hydroxyeicosatetraenoic acid (20-HETE) in vascular system. J. Smooth Muscle Res. 41 : 175-193.
12. Dunn, K. M., M. Renic, A. K. Flasch, D. R. Harder, J. Falck, and R. J. Roman. 2008. Elevated production of 20-HETE in the cerebral vasculature contributes to severity of ischemic stroke and oxidative stress in spontaneously hypertensive rats. Am. J. Physiol. Heart Circ. Physiol. 295 : H2455-H2465.
13. Park, F., W. E. Sweeney, Jr., G. Jia, T. Akbulut, B. Mueller, J. R. Falck, S. Birudaraju, R. J. Roman, and E. D. Avner. 2009. Chronic blockade of 20-HETE synthesis reduces polycystic kidney disease in an orthologous rat model of ARPKD. Am. J. Physiol. Renal Physiol. 296 : F575-F582.
14. Minuz, P., H. Jiang, C. Fava, L. Turolo, S. Tacconelli, M. Ricci, P. Patrignani, A. Morganti, A. Lechi, and J. C. McGiff. 2008. Altered release of cytochrome p450 metabolites of arachidonic acid in renovascular disease. Hypertension. 51 : 1379-1385.
15. Laffer, C. L., M. Laniado-Schwartzman, A. Nasjletti, and F. Elijovich. 2004. 20-HETE and circulating insulin in essential hypertension with obesity. Hypertension. 43 : 388-392.
16. Williams, J. M., S. Murphy, M. Burke, and R. J. Roman. 2010. 20-hydroxyeicosatetraeonic acid: a new target for the treatment of hypertension. J. Cardiovasc. Pharmacol. 56 : 336-344.
17. Lasker, J. M., W. B. Chen, I. Wolf, B. P. Bloswick, P. D. Wilson, and P. K. Powell. 2000. Formation of 20-hydroxyeicosatetraenoic acid, a vasoactive and natriuretic eicosanoid, in human kidney. Role of Cyp4F2 and Cyp4A11. J. Biol. Chem. 275 : 4118-4126.
18. Ishizuka, T., J. Cheng, H. Singh, M. D. Vitto, V. L. Manthati, J. R. Falck, and M. Laniado-Schwartzman. 2008. 20-Hydroxyeicosatetraenoic acid stimulates nuclear factor-kappaB activation and the production of infl ammatory cytokines in human endothelial cells. J. Pharmacol. Exp. Ther. 324 : 103-110.
19. Singh, H., J. Cheng, H. Deng, R. Kemp, T. Ishizuka, A. Nasjletti, and M. L. Schwartzman. 2007. Vascular cytochrome P450 4A ex-pression and 20-hydroxyeicosatetraenoic acid synthesis contribute to endothelial dysfunction in androgen-induced hypertension. Hypertension. 50 : 123-129.
20. Cheng, J., J. S. Ou, H. Singh, J. R. Falck, D. Narsimhaswamy, K. A. Pritchard, Jr., and M. L. Schwartzman. 2008. 20-hydroxyeicosatetraenoic acid causes endothelial dysfunction via eNOS uncoupling. Am. J. Physiol. Heart Circ. Physiol. 294 : H1018-H1026.
21. Brownlee, M. 2001. Biochemistry and molecular cell biology of diabetic complications. Nature. 414 : 813-820.
22. Ueno, T., and K. Fujimori. 2011. Novel suppression mechanism operating in early phase of adipogenesis by positive feedback loop for enhancement of cyclooxygenase-2 expression through prostaglandin F2alpha receptor mediated activation of MEK/ERK-CREB cascade. FEBS J. 278 : 2901-2912.
23. Fujimori, K., and F. Amano. 2011. Niacin promotes adipogenesis by reducing production of anti-adipogenic PGF2alpha through suppression of C/EBPbeta-activated COX-2 expression. Prostaglandins Other Lipid Mediat. 94 : 96-103.
24. Xie, Y., X. Kang, W. E. Ackerman, M. A. Belury, C. Koster, B. H. Rovin, M. B. Landon, and D. A. Kniss. 2006. Differentiationdependent regulation of the cyclooxygenase cascade during adipogenesis suggests a complex role for prostaglandins. Diabetes Obes. Metab. 8 : 83-93.
25. Salem, H. K. and C. Thiemermann. 2010. Mesenchymal stromal cells: current understanding and clinical status. Stem Cells. 28: 585-596.
26. Nicolai, A., M. Li, D. H. Kim, S. J. Peterson, L. Vanella, V. Positano, A. Gastaldelli, R. Rezzani, L. F. Rodella, G. Drummond, et al. 2009. Heme oxygenase-1 induction remodels adipose tissue and improves insulin sensitivity in obesity-induced diabetic rats. Hypertension. 53 : 508-515.
27. Vanella, L., D. H. Kim, K. Sodhi, I. Barbagallo, A. P. Burgess, J. R. Falck, M. L. Schwartzman, and N. G. Abraham. 2011. Crosstalk between EET and HO-1 downregulates Bach1 and adipogenic marker expression in mesenchymal stem cell derived adipocytes. Prostaglandins Other Lipid Mediat. 96 : 54-62.
28. Kim, D. H., L. Vanella, K. Inoue, A. Burgess, K. Gotlinger, V. L. Manthati, S. R. Koduru, D. C. Zeldin, J. R. Falck, M. L. Schwartzman, et al. 2010. Epoxyeicosatrienoic acid agonist regulates human mesenchymal stem cell-derived adipocytes through activation of HO-1-pAKT signaling and a decrease in PPARgamma. Stem Cells Dev. 19 : 1863-1873.
29. Tsai, I. J., K. D. Croft, I. B. Puddey, L. J. Beilin, and A. Barden. 2011. 20-Hydroxyeicosatetraenoic acid synthesis is increased in human neutrophils and platelets by angiotensin II and endothelin-1. Am. J. Physiol. Heart Circ. Physiol. 300 : H1194-H1200.
30. Schwartzman, M. L., J. R. Falck, P. Yadagiri, and B. Escalante. 1989. Metabolism of 20-hydroxyeicosatetraenoic acid by cyclooxygenase. Formation and identifi cation of novel endothelium-dependent vasoconstrictor metabolites. J. Biol. Chem. 264 : 11658-11662.
31. Abraham, N. G., E. Feldman, J. R. Falck, J. D. Lutton, and M. L. Schwartzman. 1991. Modulation of erythropoiesis by novel human bone marrow cytochrome P450-dependent metabolites of arachidonic acid. Blood. 78 : 1461-1466.
32. Lin, F., A. Rios, J. R. Falck, Y. Belosludtsev, and M. L. Schwartzman. 1995. 20-Hydroxyeicosatetraenoic acid is formed in response to EGF and is a mitogen in rat proximal tubule. Am. J. Physiol. 269 : F806-F816.
33. Muthalif, M. M., I. F. Benter, N. Karzoun, S. Fatima, J. Harper, M. R. Uddin, and K. U. Malik. 1998. 20-Hydroxyeicosatetraenoic acid mediates calcium/calmodulin-dependent protein kinase IIinduced mitogen-activated protein kinase activation in vascular smooth muscle cells. Proc. Natl. Acad. Sci. USA. 95 : 12701-12706.
34. Jiang, M., A. Mezentsev, R. Kemp, K. Byun, J. R. Falck, J. M. Miano, A. Nasjletti, N. G. Abraham, and M. Laniado-Schwartzman. 2004. Smooth muscle-specifi c expression of CYP4A1 induces endothelial sprouting in renal arterial microvessels. Circ. Res. 94 : 167-174.
35. Chen, P., M. Guo, D. Wygle, P. A. Edwards, J. R. Falck, R. J. Roman, and A. G. Scicli. 2005. Inhibitors of cytochrome P450 4A suppress angiogenic responses. Am. J. Pathol. 166 : 615-624.
36. Stec, D. E., K. P. Gannon, J. S. Beaird, and H. A. Drummond. 2007. 20-Hydroxyeicosatetraenoic acid (20-HETE) stimulates migration of vascular smooth muscle cells. Cell. Physiol. Biochem. 19 : 121-128.
37. Wu, C. C., and M. L. Schwartzman. 2011. The role of 20-HETE in androgen-mediated hypertension. Prostaglandins Other Lipid Mediat. 96 : 45-53.
38. Inazumi, T., N. Shirata, K. Morimoto, H. Takano, E. Segi-Nishida, and Y. Sugimoto. 2011. Prostaglandin E(2)-EP4 signaling suppresses adipocyte differentiation in mouse embryonic fi broblasts via an autocrine mechanism. J. Lipid Res. 52 : 1500-1508.
39. Cao, J., S. J. Peterson, K. Sodhi, L. Vanella, I. Barbagallo, L. F. Rodella, M. L. Schwartzman, N. G. Abraham, and A. Kappas. 2012. Heme oxygenase gene targeting to adipocytes attenuates adiposity and vascular dysfunction in mice fed a high-fat diet. Hypertension. 60 : 467-475.
40. Fang, X., J. S. Dillon, S. Hu, S. D. Harmon, J. Yao, S. Anjaiah, J. R. Falck, and A. A. Spector. 2007. 20-carboxy-arachidonic acid is a dual activator of peroxisome proliferator-activated receptors alpha and gamma. Prostaglandins Other Lipid Mediat. 82 : 175-184.
41. Cowart, L. A., S. Wei, M. H. Hsu, E. F. Johnson, M. U. Krishna, J. R. Falck, and J. H. Capdevila. 2002. The CYP4A isoforms hydroxylate epoxyeicosatrienoic acids to form high affi nity peroxisome proliferator- activated receptor ligands. J. Biol. Chem. 277 : 35105-35112.
42. Theken, K. N., Y. Deng, R. N. Schuck, A. Oni-Orisan, T. M. Miller, M. A. Kannon, S. M. Poloyac, and C. R. Lee. 2012. Enalapril reverses high-fat diet-induced alterations in cytochrome P450-mediated eicosanoid metabolism. Am. J. Physiol. Endocrinol. Metab. 302 : E500-E509.
43. Tsai, I. J., K. D. Croft, T. A. Mori, J. R. Falck, L. J. Beilin, I. B. Puddey, and A. E. Barden. 2009. 20-HETE and F2-isoprostanes in the metabolic syndrome: the effect of weight reduction. Free Radic. Biol. Med. 46 : 263-270.
44. Ward, N. C., J. M. Hodgson, I. B. Puddey, L. J. Beilin, and K. D. Croft. 2006. 20-Hydroxyeicosatetraenoic acid is not associated with circulating insulin in lean to overweight humans. Diabetes Res. Clin. Pract. 74 : 197-200.
45. Ward, N. C., J. Rivera, J. Hodgson, I. B. Puddey, L. J. Beilin, J. R. Falck, and K. D. Croft. 2004. Urinary 20-hydroxyeicosatetraenoic acid is associated with endothelial dysfunction in humans. Circulation. 110 : 438-443.
46. Ward, N. C., I. B. Puddey, J. M. Hodgson, L. J. Beilin, and K. D. Croft. 2005. Urinary 20-hydroxyeicosatetraenoic acid excretion is associated with oxidative stress in hypertensive subjects. Free Radic. Biol. Med. 38 : 1032-1036.
47. Issan, Y., E. Hochhauser, A. Guo, K. H. Gotlinger, R. Kornowski, D. Leshem-Lev, E. Lev, E. Porat, E. Snir, C. I. Thompson, N. G. Abraham, M. Laniado-Schwartzman. 2013. Elevated level of pro-infl ammatory eicosanoids and EPC dysfunction in diabetic patients with cardiac ischemia. Prostaglandins Other Lipid Mediat. In press.