Epoxyeicosatrienoic acid agonist regulates human mesenchymal stem cell-derived adipocytes through activation of HO-1-pAKT signaling and a decrease in PPARγ

Stem Cells and Development

Volumn 19, Issue 12, 2010, Pages 1863-1873

  Kim, Dong Hyun ^a   Vanella, Luca ^a   Inoue, Kazuyoshi ^b   Burgess, Angela ^a   Gotlinger, Katherine ^b   Manthati, Vijaya Lingam ^c   Koduru, Sreenivasulu Reddy ^c   Zeldin, Darryl C ^d   Falck, John R ^c   Schwartzman, Michal L ^b   Abraham, Nader G ^a  

^a MEDICAL COLLEGE OF OHIO   (United States)

^b NEW YORK MEDICAL COLLEGE   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^d NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

12 (3 HEXYLUREIDO)DODEC ENOIC ACID; ACTIVATED LEUKOCYTE CELL ADHESION MOLECULE; ADIPONECTIN; AGENTS AFFECTING LIPID METABOLISM; CCAAT ENHANCER BINDING PROTEIN ALPHA; ENDOGLIN; EPOXYICOSATRIENOIC ACID; FATTY ACID SYNTHASE; HEME OXYGENASE 1; LY 2940002; MESOPORPHYRIN TIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROTEIN KINASE B; THY 1 ANTIGEN; UNCLASSIFIED DRUG;

ADIPOCYTE; ADIPOGENESIS; ARTICLE; CELL DIFFERENTIATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFECT; ENZYME ACTIVITY; ENZYME INHIBITION; GLUCOSE TRANSPORT; HUMAN; HUMAN CELL; LIPID STORAGE; MESENCHYMAL STEM CELL; PRIORITY JOURNAL;

8,11,14-EICOSATRIENOIC ACID; ADIPOCYTES; ADIPOGENESIS; ADIPONECTIN; ARACHIDONIC ACID; CCAAT-ENHANCER-BINDING PROTEINS; CHROMONES; CYTOCHROME P-450 ENZYME SYSTEM; EPOXIDE HYDROLASES; FATTY ACID SYNTHETASE COMPLEX; FATTY ACIDS, MONOUNSATURATED; GLUCOSE; HEME OXYGENASE-1; HUMANS; HYDROXYEICOSATETRAENOIC ACIDS; LIPIDS; MESENCHYMAL STEM CELLS; METALLOPORPHYRINS; MORPHOLINES; PPAR GAMMA; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION;

EID: 78649703778     PISSN: 15473287     EISSN: None     Source Type: Journal    
DOI: 10.1089/scd.2010.0098     Document Type: Article

References (52)

1. Salem HK and C Thiemermann. (2010). Stem Cells 28:585-596. Review.
2. Song H, MJ Cha, BW Song, IK Kim, W Chang, S Lim, EJ Choi, O Ham, SY Lee, N Chung, Y Jang and KC Hwang. (2010). Reactive oxygen species inhibit adhesion of mesenchymal stem cells implanted into ischemic myocardium via interference of focal adhesion complex. Stem Cells 28:555-563.
3. Bai XC, D Lu, J Bai, H Zheng, ZY Ke, XM Li and SQ Luo. (2004). Oxidative stress inhibits osteoblastic differentiation of bone cells by ERK and NF-kappaB. Biochem Biophys Res Commun 314:197-207.
4. Sambuceti G, S Morbelli, L Vanella, C Kusmic, C Marini, M Massollo, C Augeri, M Corselli, C Ghersi, B Chiavarina, LF Rodella, A L' Abbate, G Drummond, NG Abraham and F Frassoni. (2009). Diabetes impairs the vascular recruitment of normal stem cells by oxidant damage; reversed by increases in pAMPK, heme oxygenase-1 and adiponectin. Stem Cells 27:399-407.
5. Wellen KE and GS Hotamisligil. (2003). Obesity-induced inflammatory changes in adipose tissue. J Clin Invest 112: 1785-1788.
6. Houstis N, ED Rosen and ES Lander. (2006). Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature 440:944-948.
7. Vanella L, DH Kim, D Asprinio, S Peterson, I Barbagallo, A Vanella, D Goldstein, S Ikehara and N Abraham. (2009). HO-1 expression increases mesenchymal stem cell-derived osteoblast and decrease adipocyte lineages. Bone 46:236-243.
8. Verda L, DA Kim, S Ikehara, L Statkute, D Bronesky, Y Petrenko, Y Oyama, X He, C Link, NN Vahanian and RK Burt. (2008). Hematopoietic mixed chimerism derived from allogeneic embryonic stem cells prevents autoimmune diabetes mellitus in NOD mice. Stem Cells 26:381-386.
9. Abraham NG, M Li, L Vanella, SJ Peterson, S Ikehara and D Asprinio. (2008). Bone marrow stem cell transplant into intra-bone cavity prevents type 2 diabetes: role of heme oxygenase-adiponectin. J Autoimmun 30:128-135.
10. Abraham NG. (1991). Molecular regulation\biological role of heme in hematopoiesis. Blood Rev 5:19-28.
11. Iwaki M, M Matsuda, N Maeda, T Funahashi, Y Matsuzawa, M Makishima and I Shimomura. (2003). Induction of adi-ponectin, a fat-derived antidiabetic and antiatherogenic factor, by nuclear receptors. Diabetes 52:1655-1663.
12. Kusmic C, A L'Abbate, G Sambuceti, G Drummond, C Barsanti, M Matteucci, J Cao, F Piccolomini, J Cheng and NG Abraham. (2010). Improved myocardial perfusion in chronic diabetic mice by the up-regulation of pLKB1 and AMPK signaling. J Cell Biochem 109:1033-1044.
13. Li C and JF Keaney, Jr. (2010). AMP-activated protein kinase: a stress-responsive kinase with implications for cardiovascular disease. Curr Opin Pharmacol 10:111-115. Review.
14. Walsh K. (2009). Adipokines, myokines and cardiovascular disease. Circ J 73:13-18.
15. Kim DH, AP Burgess, M Li, PL Tsenovoy, F Addabbo, JA McClung, N Puri and NG Abraham. (2008). Heme oxygenase-mediated increases in adiponectin decrease fat content and inflammatory cytokines, tumor necrosis factor-alpha and interleukin-6 in Zucker rats and reduce adipo-genesis in human mesenchymal stem cells. J Pharmacol Exp Ther 325:833-840.
16. Li M, DH Kim, PL Tsenovoy, SJ Peterson, R Rezzani, LF Rodella, WS Aronow, S Ikehara and NG Abraham. (2008). Treatment of obese diabetic mice with a heme oxygenase inducer reduces visceral and subcutaneous adiposity, increases adiponectin levels, and improves insulin sensitivity and glucose tolerance. Diabetes 57:1526-1535.
17. Nicolai A, M Li, DH Kim, SJ Peterson, L Vanella, V Positano, A Gastaldelli, R Rezzani, LF Rodella, G Drummond, C Kusmic, A L'Abbate, A Kappas and NG Abraham. (2009). Heme oxygenase-1 induction remodels adipose tissue and improves insulin sensitivity in obesity-induced diabetic rats. Hypertension 53:508-515.
18. Peterson SJ, G Drummond, KD Hyun, M Li, AL Kruger, S Ikehara and NG Abraham. (2008). L-4F treatment reduces adiposity, increases adiponectin levels and improves insulin sensitivity in obese mice. J Lipid Res 49:1658-1669.
19. Peterson SJ, DH Kim, M Li, V Positano, L Vanella, LF Rodella, F Piccolomini, N Puri, A Gastaldelli, C Kusmic, A L'Abbate and NG Abraham. (2009). The L-4F mimetic peptide prevents insulin resistance through increased levels of HO-1, pAMPK, and pAKT in obese mice. J Lipid Res 50:1293-1304.
20. Sodhi K, K Inoue, K Gotlinger, M Canestraro, L Vanella, DH Kim, VL Manthati, SR Koduru, JR Falck, ML Schwartzman and NG Abraham. (2009). Epoxyeicosatrienoic acid agonist rescues the metabolic syndrome phenotype of HO-2-null mice. J Pharmacol Exp Ther 331:906-916.
21. Sacerdoti D, M Bolognesi, PM Di, A Gatta, JC McGiff, ML Schwartzman and NG Abraham. (2006). Rat mesenteric arterial dilator response to 11,12-epoxyeicosatrienoic acid is mediated by activating heme oxygenase. Am J Physiol Heart Circ Physiol 291:H1999-H2002.
22. Sacerdoti D, C Colombrita, PM Di, ML Schwartzman, M Bolognesi, JR Falck, A Gatta and NG Abraham. (2007). 11,12-Epoxyeicosatrienoic acid stimulates heme-oxygenase-1 in endothelial cells. Prostaglandins Other Lipid Mediat 82:155-161.
23. Zeldin DC. (2001). Epoxygenase pathways of arachidonic acid metabolism. J Biol Chem 276:36059-36062.
24. Campbell WB and JR Falck. (2007). Arachidonic acid metabolites as endothelium-derived hyperpolarizing factors. Hypertension 49:590-596.
25. Abraham NG, E Feldman, JR Falck, JD Lutton and ML Schwartzman. (1991). Modulation of erythropoiesis by novel human bone marrow cytochrome P450-dependent metabolites of arachidonic acid. Blood 78:1461-1466.
26. Grimm S and PA Baeuerle. (1993). The inducible transcription factor NF-kappa B: structure-function relationship of its protein subunits. Biochem J 290 (Pt 2):297-308.
27. Burns KD, J Capdevila, S Wei, MD Breyer, T Homma and RC Harris. (1995). Role of cytochrome P-450 epoxygenase metabolites in EGF signaling in renal proximal tubule. Am J Physiol 269:C831-C840.
28. Tavian D and R Colombo. (2007). Improved cytochemical method for detecting Jordans' bodies in neutral lipid storage diseases. J Clin Pathol 60:956-958.
29. Seubert J, B Yang, JA Bradbury, J Graves, LM Degraff, S Gabel, R Gooch, J Foley, J Newman, L Mao, HA Rockman, BD Hammock, E Murphy and DC Zeldin. (2004). Enhanced postischemic functional recovery in CYP2J2 transgenic hearts involves mitochondrial ATP-sensitive K\+ channels and p42=p44 MAPK pathway. Circ Res 95:506-514.
30. Falck JR, R Kodela, R Manne, KR Atcha, N Puli, N Dubasi, VL Manthati, JH Capdevila, XY Yi, DH Goldman, C Mor-isseau, BD Hammock and WB Campbell. (2009). 14,15-Epoxyeicosa-5,8,11-trienoic acid (14,15-EET) surrogates containing epoxide bioisosteres: influence upon vascular relaxation and soluble epoxide hydrolase inhibition. J Med Chem 52:5069-5075.
31. Sacerdoti D, NG Abraham, AO Oyekan, L Yang, A Gatta and JC McGiff. (2004). Role of the heme oxygenases in abnormalities of the mesenteric circulation in cirrhotic rats. J Pharmacol Exp Ther 308:636-643.
32. Gutterman DD. (2002). Vascular dysfunction in hypergly-cemia: is protein kinase C the culprit? Circ Res 90:5-7.
33. Imig JD. (2005). Epoxide hydrolase and epoxygenase metabolites as therapeutic targets for renal diseases. Am J Physiol Renal Physiol 289:F496-F503.
34. Barbagallo I, A Vanella, SJ Peterson, DH Kim, D Tibullo, C Giallongo, L Vanella, N Parrinello, GA Palumbo, F Di Rai-mond, NG Abraham and D Asprinio. (2010). Over expression of heme oxygenase-1 increases human osteoblast stem cell differentiation. J Bone Miner Metab 28:276-288.
35. Spector AA and AW Norris. (2007). Action of epoxyeicosa-trienoic acids on cellular function. Am J Physiol Cell Physiol 292:C996-C1012.
36. Imig JD. (2006). Cardiovascular therapeutic aspects of soluble epoxide hydrolase inhibitors. Cardiovasc Drug Rev 24:169-188.
37. Ohtoshi K, H Kaneto, K Node, Y Nakamura, T Shiraiwa, M Matsuhisa and Y Yamasaki. (2005). Association of soluble epoxide hydrolase gene polymorphism with insulin resistance in type 2 diabetic patients. Biochem Biophys Res Commun 331:347-350.
38. Bodiga S, R Zhang, DE Jacobs, BT Larsen, A Tampo, VL Manthati, WM Kwok, DC Zeldin, JR Falck, DD Gutterman, ER Jacobs and MM Medhora. (2009). Protective actions of epoxyeicosatrienoic acid: dual targeting of cardiovascular PI3K and KATP channels. J Mol Cell Cardiol 46:978-988.
39. Larsen BT, DD Gutterman, A Sato, K Toyama, WB Campbell, DC Zeldin, VL Manthati, JR Falck and H Miura. (2008). Hydrogen peroxide inhibits cytochrome p450 epoxygenases: interaction between two endothelium-derived hyperpolar-izing factors. Circ Res 102:59-67.
40. Dhanasekaran A, R Al-Saghir, B Lopez, D Zhu, DD Gut-terman, ER Jacobs and M Medhora. (2006). Protective effects of epoxyeicosatrienoic acids on human endothelial cells from the pulmonary and coronary vasculature. Am J Physiol Heart Circ Physiol 291:H517-H531.
41. Asija A, S Peterson, DE Stec and NG Abraham. (2007). Targeting endothelial cells with heme oxygenase-1 gene using VE-cadherin promoter attenuates hyperglycemia-mediated cell injury and apoptosis. Antioxid Redox Signal 12:2065-2074.
42. Olszanecki R, R Rezzani, S Omura, DE Stec, L Rodella, FT Botros, AI Goodman, G Drummond and NG Abraham. (2007). Genetic suppression of HO-1 exacerbates renal damage: reversed by an increase in the antiapoptotic signaling pathway. Am J Physiol Renal Physiol 292:F148-F157.
43. Di Noia MA, DS Van, F Palmieri, LM Yang, S Quan, AI Goodman and NG Abraham. (2006). Heme oxygenase-1 enhances renal mitochondrial transport carriers and cyto-chrome C oxidase activity in experimental diabetes. J Biol Chem 281:15687-15693.
44. Turkseven S, G Drummond, R Rezzani, L Rodella, S Quan, S Ikehara and NG Abraham. (2007). Impact of silencing HO-2 on EC-SOD and the mitochondrial signaling pathway. J Cell Biochem 100:815-823.
45. Murgia M, JT Elbenhardt, M Cusinato, M Garcia, EA Richter and S Schiaffino. (2009). Multiple signalling pathways redundantly control GLUT4 gene transcription in skeletal muscle. J Physiol 587:4319-4327.
46. Habets DD, WA Coumans, HM El, E Zarrinpashneh, L Bertrand, B Viollet, B Kiens, TE Jensen, EA Richter, A Bonen, JF Glatz and JJ Luiken. (2009). Crucial role for LKB1 to AMPKalpha2 axis in the regulation of CD36-mediated long-chain fatty acid uptake into cardiomyocytes. Biochim Biophys Acta 1791:212-219.
47. Buhl ES, N Jessen, R Pold, T Ledet, A Flyvbjerg, SB Ped-ersen, O Pedersen, O Schmitz and S Lund. (2002). Long-term AICAR administration reduces metabolic disturbances and lowers blood pressure in rats displaying features of the insulin resistance syndrome. Diabetes 51:2199-2206.
48. Ross SE, N Hemati, KA Longo, CN Bennett, PC Lucas, RL Erickson and OA MacDougald. (2000). Inhibition of adipo-genesis by Wnt signaling. Science 289:950-953.
49. Elmarakby AA and JD Imig. (2010). Obesity is the major contributor to vascular dysfunction and inflammation in high fat diet hypertensive rats. Clin Sci (Lond) 118:291-301.
50. Moustaid N and HS Sul. (1991). Regulation of expression of the fatty acid synthase gene in 3T3-L1 cells by differentiation and triiodothyronine. J Biol Chem 266:18550-18554.
51. Li K, L Li, GY Yang, H Liu, SB Li and G Boden. (2009). Effect of shRNA-mediated adiponectin=Acrp30 down-regulation on insulin signaling and glucose uptake in the 3T3-L1 adi-pocytes. J Endocrinol Invest 33:96-102.
52. Funaki M, P Randhawa and PA Janmey. (2004). Separation of insulin signaling into distinct GLUT4 translocation and activation steps. Mol Cell Biol 24:7567-7577.