Effects of rosiglitazone on gene expression in subcutaneous adipose tissue in highly active antiretroviral therapy-associated lipodystrophy

American Journal of Physiology - Endocrinology and Metabolism

Volumn 286, Issue 6 49-6, 2004, Pages

  Sutinen, Jussi ^a   Kannisto, Katja ^c   Korsheninnikova, Elena ^b   Fisher, Rachel M ^c   Ehrenborg, Ewa ^c   Nyman, Tuulikki ^b   Virkamäki, Antii ^b   Funahashi, Tohru ^d   Matsuzawa, Yuji ^d   Vidal, Hubert ^e   Hamsten, Anders ^c   Yki Järvinen, Hannele ^a,c  

^a HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^b MINERVA FOUNDATION INSTITUTE FOR MEDICAL RESEARCH   (Finland)

^c KAROLINSKA INSTITUTE   (Sweden)

^d OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^e INSERM   (France)

Author keywords

Adiponectin; Human immunodeficiency virus; Liver fat; Real time polymerase chain reaction

Indexed keywords

ABACAVIR; ADIPONECTIN; AMPRENAVIR; ANTIRETROVIRUS AGENT; CARRIER PROTEIN; CD45 ANTIGEN; DIDANOSINE; FATTY ACID TRANSPORT PROTEIN 1; FATTY ACID TRANSPORT PROTEIN 4; GLUCOSE TRANSPORTER 1; GLUCOSE TRANSPORTER 4; INDINAVIR; INSULIN; INTERLEUKIN 6; LIPID BINDING PROTEIN; LIPOPROTEIN LIPASE; LONG CHAIN FATTY ACID COENZYME A LIGASE; LOPINAVIR; MESSENGER RNA; NELFINAVIR; NEVIRAPINE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; RITONAVIR; ROSIGLITAZONE; STAVUDINE; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; UNCLASSIFIED DRUG; ZALCITABINE; ZIDOVUDINE;

ARTICLE; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; DOUBLE BLIND PROCEDURE; DRUG EFFECT; FATTY ACID METABOLISM; GENE EXPRESSION; GLUCOSE TRANSPORT; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HUMAN TISSUE; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIPODYSTROPHY; LIPOGENESIS; LIVER; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROGNOSIS; RANDOMIZED CONTROLLED TRIAL; REAL TIME POLYMERASE CHAIN REACTION; SUBCUTANEOUS FAT;

ADIPONECTIN; ADIPOSE TISSUE; ANTIRETROVIRAL THERAPY, HIGHLY ACTIVE; BODY COMPOSITION; FATTY ACIDS; GENE EXPRESSION; HIV-ASSOCIATED LIPODYSTROPHY SYNDROME; HUMANS; HYPOGLYCEMIC AGENTS; INSULIN RESISTANCE; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LIVER; PROTEINS; SUBCUTANEOUS TISSUE; THIAZOLIDINEDIONES;

EID: 2442641811     PISSN: 01931849     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpendo.00490.2003     Document Type: Article

References (65)

1. Arioglu E, Duncan-Morin J, Sebring N, Rother KI, Gottlieb N, Lieberman J, Herion D, Kleiner DE, Reynolds J, Premkumar A, Sumner AE, Hoofnagle J, Reitman ML, and Taylor SI. Efficacy and safety of troglitazone in the treatment of lipodystrophy syndromes. Ann Intern Med 133: 263-274, 2000.
2. Berg AH, Combs TP, Du X, Brownlee M, and Scherer PE. The adipocyte-secreted protein Acrp30 enhances hepatic insulin action. Nat Med 7: 947-953, 2001.
3. Berg AH, Combs TP, and Scherer PE. ACRP30/adiponectin: an adipokine regulating glucose and lipid metabolism. Trends Endocrinol Metab 13: 84-89, 2002.
4. Berger J and Moller DE. The mechanisms of action of PPARs. Annu Rev Med 53: 409-435, 2002.
5. Berger J, Tanen M, Elbrecht A, Hermanowski-Vosatka A, Moller DE, Wright SD, and Thieringer R. Peroxisome proliferator-activated receptor-gamma ligands inhibit adipocyte 11beta-hydroxysteroid dehydrogenase type 1 expression and activity. J Biol Chem 276: 12629-12635, 2001.
6. Boelsterli UA and Bedoucha M. Toxicological consequences of altered peroxisome proliferator-activated receptor gamma (PPARgamma) expression in the liver: insights from models of obesity and type 2 diabetes. Biochem Pharmacol 63: 1-10, 2002.
7. Burant CF, Sreenan S, Hirano K, Tai TA, Lohmiller J, Lukens J, Davidson NO, Ross S, and Graves RA. Troglitazone action is independent of adipose tissue. J Clin Invest 100: 2900-2908, 1997.
8. Caron M, Auclair M, Vigouroux C, Glorian M, Forest C, and Capeau J. The HIV protease inhibitor indinavir impairs sterol regulatory element-binding protein-1 intranuclear localization, inhibits preadipocyte differentiation, and induces insulin resistance. Diabetes 50: 1378-1388, 2001.
9. Carr A and Cooper DA. Adverse effects of antiretroviral therapy. Lancet 356: 1423-1430, 2000.
10. Cavaillon JM. Cytokines and macrophages. Biomed Pharmacother 48: 445-453, 1994.
11. Chao L, Marcus-Samuels B, Mason MM, Moitra J, Vinson C, Arioglu E, Gavrilova O, and Reitman ML. Adipose tissue is required for the antidiabetic, but not for the hypolipidemic, effect of thiazolidinediones. J Clin Invest 106: 1221-1228, 2000.
12. Combs TP, Berg AH, Obici S, Scherer PE, and Rossetti L. Endogenous glucose production is inhibited by the adipose-derived protein Acrp30. J Clin Invest 108: 1875-1881, 2001.
13. Combs TP, Wagner JA, Berger J, Doebber T, Wang WJ, Zhang BB, Tanen M, Berg AH, O'Rahilly S, Savage DB, Chatterjee K, Weiss S, Larson PJ, Gottesdiener KM, Gertz BJ, Charron MJ, Scherer PE, and Moller DE. Induction of adipocyte complement-related protein of 30 kilodaltons by PPARgamma agonists: a potential mechanism of insulin sensitization. Endocrinology 143: 998-1007, 2002.
14. Coppack SW. Pro-inflammatory cytokines and adipose tissue. Proc Nutr Soc 60: 349-356, 2001.
15. Dube MP, Stein JH, Aberg JA, Fichtenbaum CJ, Gerber JG, Tashima KT, Henry WK, Currier JS, Sprecher D, and Glesby MJ. Guidelines for the evaluation and management of dyslipidemia in human immunodeficiency virus (HIV)-infected adults receiving antiretroviral therapy: recommendations of the HIV Medical Association of the Infectious Disease Society of America and the Adult AIDS Clinical Trials Group. Clin Infect Dis 37: 613-627, 2003.
16. Dunaif A, Scott D, Finegood D, Quintana B, and Whitcomb R. The insulin-sensitizing agent troglitazone improves metabolic and reproductive abnormalities in the polycystic ovary syndrome. J Clin Endocrinol Metab 81: 3299-3306, 1996.
17. Ehrmann DA, Schneider DJ, Sobel BE, Cavaghan MK, Imperial J, Rosenfield RL, and Polonsky KS. Troglitazone improves defects in insulin action, insulin secretion, ovarian steroidogenesis, and fibrinolysis in women with polycystic ovary syndrome. J Clin Endocrinol Metab 82: 2108-2116, 1997.
18. El-Kebbi IM, Roser S, and Pollet RJ. Regulation of glucose transport by pioglitazone in cultured muscle cells. Metabolism 43: 953-958, 1994.
19. Fonseca V, Rosenstock J, Patwardhan R, and Salzman A. Effect of metformin and rosiglitazone combination therapy in patients with type 2 diabetes mellitus: a randomized controlled trial. JAMA 283: 1695-1702, 2000.
20. Fruebis J, Tsao TS, Javorschi S, Ebbets-Reed D, Erickson MR, Yen FT, Bihain BE, and Lodish HF. Proteolytic cleavage product of 30-kDa adipocyte complement-related protein increases fatty acid oxidation in muscle and causes weight loss in mice. Proc Natl Acad Sci USA 98: 2005-2010, 2001.
21. Galli M, Cozzi-Lepri A, Ridolfo AL, Gervasoni C, Ravasio L, Corsico L, Gianelli E, Vaccarezza M, Vullo V, Cargnel A, Minoli L, Coronado O, Giacometti A, Antinori A, Antonucci G, d'Arminio MA, and Moroni M. Incidence of adipose tissue alterations in first-line antiretroviral therapy: the LipolCoNa Study. Arch Intern Med 162: 2621-2628, 2002.
22. Garg A. Lipodystrophies. Am J Med 108: 143-152, 2000.
23. Gustafson B, Jack MM, Cushman SW, and Smith U. Adiponectin gene activation by thiazolidinediones requires PPAR gamma 2, but not C/EBP alpha-evidence for differential regulation of the aP2 and adiponectin genes. Biochem Biophys Res Commun 308: 933-939, 2003.
24. Hadigan C, Borgonha S, Rabe J, Young V, and Grinspoon S. Increased rates of lipolysis among human immunodeficiency virus-infected men receiving highly active antiretroviral therapy. Metabolism 51: 1143-1147, 2002.
25. Hadigan C, Meigs JB, Corcoran C, Rietschel P, Piecuch S, Basgoz N, Davis B, Sax P, Stanley T, Wilson PW, D'Agostino RB, and Grinspoon S. Metabolic abnormalities and cardiovascular disease risk factors in adults with human immunodeficiency virus infection and lipodystrophy. Clin Infect Dis 32: 130-139, 2001.
26. Haffner SM, Greenberg AS, Weston WM, Chen H, Williams K, and Freed MI. Effect of rosiglitazone treatment on nontraditional markers of cardiovascular disease in patients with type 2 diabetes mellitus. Circulation 106: 679-684, 2002.
27. Hirose H, Kawai T, Yamamoto Y, Taniyama M, Tomita M, Matsubara K, Okazaki Y, Ishii T, Oguma Y, Takei I, and Saruta T. Effects of pioglitazone on metabolic parameters, body fat distribution, and serum adiponectin levels in Japanese male patients with type 2 diabetes. Metabolism 51: 314-317, 2002.
28. Iwaki M, Matsuda M, Maeda N, Funahashi T, Matsuzawa Y, Makishima M, and Shimomura I. Induction of adiponectin, a fat-derived antidiabetic and antiatherogenic factor, by nuclear receptors. Diabetes 52: 1655-1663, 2003.
29. Kannisto K, Sutinen J, Korsheninnikova E, Fisher RM, Ehrenborg E, Gertow K, Virkamäki A, Nyman T, Vidal H, Hamsten A, and YkiJärvinen H. Expression of adipogenic transcription factors, peroxisome proliferator-activated receptor gamma co-activator 1, IL-6 and CD45 in subcutaneous adipose tissue in lipodystrophy associated with highly active antiretroviral therapy. AIDS 17: 1753-1762, 2003.
30. Koutnikova H and Auwerx J. Regulation of adipocyte differentiation. Ann Med 33: 556-561, 2001.
31. Lebovitz HE, Dole JF, Patwardhan R, Rappaport EB, and Freed MI. Rosiglitazone monotherapy is effective in patients with type 2 diabetes. J Clin Endocrinol Metab 86: 280-288, 2001.
32. Maeda N, Shimomura I, Kishida K, Nishizawa H, Matsuda M, Nagaretani H, Furuyama N, Kondo H, Takahashi M, Arita Y, Komuro R, Ouchi N, Kihara S, Tochino Y, Okutomi K, Horie M, Takeda S, Aoyama T, Funahashi T, and Matsuzawa Y. Diet-induced insulin resistance in mice lacking adiponectin/ACRP30. Nat Med 8: 731-737, 2002.
33. Maeda N, Takahashi M, Funahashi T, Kihara S, Nishizawa H, Kishida K, Nagaretani H, Matsuda M, Komuro R, Ouchi N, Kuriyama H, Hotta K, Nakamura T, Shimomura I, and Matsuzawa Y. PPARgamma ligands increase expression and plasma concentrations of adiponectin, an adipose-derived protein. Diabetes 50: 2094-2099, 2001.
34. Mayerson AB, Hundal RS, Dufour S, Lehon V, Befroy D, Cline GW, Enocksson S, Inzucchi SE, Shulman GI, and Petersen KF. The effects of rosiglitazone on insulin sensitivity, lipolysis, and hepatic and skeletal muscle triglyceride content in patients with type 2 diabetes. Diabetes 51: 797-802, 2002.
35. McTernan PG, Harte AL, Anderson LA, Green A, Smith SA, Holder JC, Barnett AH, Eggo MC, and Kumar S. Insulin and rosiglitazone regulation of lipolysis and lipogenesis in human adipose tissue in vitro. Diabetes 51: 1493-1498, 2002.
36. Miles J, Classcock R, Aikens J, Gerich J, and Haymond N. A microfluorometric method for the determination of free fatty acids in plasma. J Lipid Res 24: 96-99, 1983.
37. Miyazaki Y, Glass L, Triplitt C, Matsuda M, Cusi K, Mahankali A, Mahankali S, Mandarino LJ, and DeFronzo RA. Effect of rosiglitazone on glucose and non-esterified fatty acid metabolism in Type II diabetic patients. Diabetologia 44: 2210-2219, 2001.
38. Motoshima H, Wu X, Sinha MK, Hardy VE, Rosato EL, Barbot DJ, Rosato FE, and Goldstein BJ. Differential regulation of adiponectin secretion from cultured human omental and subcutaneous adipocytes: effects of insulin and rosiglitazone. J Clin Endocrinol Metab 87: 5662-5667, 2002.
39. Nugent C, Prins JB, Whitehead JP, Savage D, Wentworth JM, Chatterjee VK, and O'Rahilly S. Potentiation of glucose uptake in 3T3-L1 adipocytes by PPAR gamma agonists is maintained in cells expressing a PPAR gamma dominant-negative mutant: evidence for selectivity in the downstream responses to PPAR gamma activation. Mol Endocrinol 15: 1729-1738, 2001.
40. Ouchi N, Kihara S, Funahashi T, Nakamura T, Nishida M, Kumada M, Okamoto Y, Ohashi K, Nagaretani H, Kishida K, Nishizawa H, Maeda N, Kobayashi H, Hiraoka H, and Matsuzawa Y. Reciprocal association of C-reactive protein with adiponectin in blood stream and adipose tissue. Circulation 107: 671-674, 2003.
41. Palella FJJ, Delaney KM, Moorman AC, Loveless MO, Fuhrer J, Satten GA, Aschman DJ, and Holmberg SD. Declining morbidity and mortality among patients with advanced human immunodeficiency virus infection. HIV Outpatient Study Investigators. N Engl J Med 338: 853-860, 1998.
42. Raskin P, Rappaport EB, Cole ST, Yan Y, Patwardhan R, and Freed MI. Rosiglitazone short-term monotherapy lowers fasting and post-prandial glucose in patients with type II diabetes. Diabetologia 43: 278-284, 2000.
43. Razeghi P, Young ME, Alcorn JL, Moravec CS, Frazier OH, and Taegtmeyer H. Metabolic gene expression in fetal and failing human heart. Circulation 104: 2923-2931, 2001.
44. Rieusset J, Auwerx J, and Vidal H. Regulation of gene expression by activation of the peroxisome proliferator-activated receptor gamma with rosiglitazone (BRL 49653) in human adipocytes. Biochem Biophys Res Commun 265: 265-271, 1999.
45. Roche R, Poizot-Martin 1, Yazidi CM, Compe E, Gastaut JA, Torresani J, and Planells R. Effects of antiretroviral drug combinations on the differentiation of adipocytes. AIDS 16: 13-20, 2002.
46. Schoonjans K, Peinado-Onsurbe J, Lefebvre AM, Heyman RA, Briggs M, Deeb S, Staels B, and Auwerx J. PPARalpha and PPARgamma activators direct a distinct tissue-specific transcriptional response via a PPRE in the lipoprotein lipase gene. EMBO J 15: 5336-5348, 1996.
47. Schultz DR and Arnold PI. Properties of four acute phase proteins: C-reactive protein, serum amyloid A protein, alpha 1-acid glycoprotein, and fibrinogen. Semin Arthritis Rheum 20: 129-147, 1990.
48. Seppälä-Lindroos A, Vehkavaara S, Häkkinen AM, Goto T, Westerbacka J, Sovijärvi A, Halavaara J, and Yki-Järvinen H. Fat accumulation in the liver is associated with defects in insulin suppression of glucose production and serum free fatty acids independent of obesity in normal men. J Clin Endocrinol Metab 87: 3023-3028, 2002.
49. Sigrist S, Bedoucha M, and Boelsterli UA. Down-regulation by troglitazone of hepatic tumor necrosis factor-alpha and interleukin-6 mRNA expression in a murine model of non-insulin-dependent diabetes. Biochem Pharmacol 60: 67-75, 2000.
50. Spiegelman BM. PPAR-gamma: adipogenic regulator and thiazolidinedione receptor. Diabetes 47: 507-514, 1998.
51. Sutinen J, Häkkinen AM, Westerbacka J, Seppälä-Lindroos A, Vehkavaara S, Halavaara J, Järvinen A, Ristola M, and Yki-Järvinen H. Increased fat accumulation in the liver in HIV-infected patients with antiretroviral therapy-associated lipodystrophy. AIDS 16: 2183-2193, 2002.
52. Sutinen J, Häkkinen AM, Westerhacka J, Seppäiä-Lindroos A, Vehkavaara S, Halavaara J, Järvinen A, Ristola M, and Yki-Järvinen H. Rosiglitazone in the treatment of HAART-associated lipodystrophy-a randomized double-blind placebo-controlled study. Antiviral Ther 8: 199-207, 2003.
53. Sutinen J, Korsheninnikova E, Funahashi T, Matsuzawa Y, Nyman T, and Yki-Järvinen H. Circulating concentration of adiponectin and its expression in subcutaneous adipose tissue in patients with highly active antiretroviral therapy-associated lipodystrophy. J Clin Endocrinol Metab 88: 1907-1910, 2003.
54. Tiikkainen M, Tamminen M, Häkkinen AM, Bergholm R, Vehkavaara S, Halavaara J, Teramo K, Rissanen A, and Yki-Järvinen H. Liver-fat accumulation and insulin resistance in obese women with previous gestational diabetes. Obes Res 10: 859-867, 2002.
55. Van der Valk M, Gisolf EH, Reiss P, Wit FW, Japour A, Weverling GJ, and Danner SA. Increased risk of lipodystrophy when nucleoside analogue reverse transcriptase inhibitors are included with protease inhibitors in the treatment of HIV-1 infection. AIDS 15: 847-855, 2001.
56. Van der Valk M, Kastelein JJ, Murphy RL, van Leth F, Katlama C, Horban A, Glesby M, Behrens G, Clotet B, Stellato RK, Molhuizen HO, and Reiss P. Nevirapine-containing antiretroviral therapy in HIV-1 infected patients results in an anti-atherogenic lipid profile. AIDS 15: 2407-2414, 2001.
57. Wanke CA, Falutz JM, Shevitz A, Phair JP, and Kotler DP. Clinical evaluation and management of metabolic and morphologic abnormalities associated with human immunodeficiency virus. Clin Infect Dis 34: 248-259, 2002.
58. Wu Z, Xie Y, Morrison RF, Bucher NL, and Farmer SR. PPARgamma induces the insulin-dependent glucose transporter GLUT4 in the absence of C/EBPalpha during the conversion of 3T3 fibroblasts into adipocytes. J Clin Invest 101: 22-32, 1998.
59. Yamauchi T, Kamon J, Minokoshi Y, Ito Y, Waki H, Uchida S, Yamashita S, Noda M, Kita S, Ueki K, Eto K, Akanuma Y, Froguel P, Foufelle F, Ferre P, Carling D, Kimura S, Nagai R, Kahn BB, and Kadowaki T. Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase. Nat Med 11: 1288-1295, 2002.
60. Yamauchi T, Kamon J, Waki H, Terauchi Y, Kubota N, Hara K, Mori Y, Ide T, Murakami K, Tsuboyama-Kasaoka N, Ezaki O, Akanuma Y, Gavrilova O, Vinson C, Reitman ML, Kagechika H, Shudo K, Yoda M, Nakano Y, Tobe K, Nagai R, Kimura S, Tomita M, Froguel P, and Kadowaki T. The fat-derived hormone adiponectin reverses insulin resistance associated with both lipoatrophy and obesity. Nat Med 7: 941-946, 2001.
61. Yang WS, Jeng CY, Wu TJ, Tanaka S, Funahashi T, Matsuzawa Y, Wang JP, Chen CL, Tai TY, and Chuang LM. Synthetic peroxisome proliferator-activated receptor-gamma agonist, rosiglitazone, increases plasma levels of adiponectin in type 2 diabetic patients. Diabetes Care 25: 376-380, 2002.
62. Ye JM, Frangioudakis G, Iglesias MA, Furler SM, Ellis B, Dzamko N, Cooney GJ, and Kraegen EW. Prior thiazolidinedione treatment preserves insulin sensitivity in normal rats during acute fatty acid elevation: role of the liver. Endocrinology 143: 4527-4535, 2002.
63. Yeni PG, Hammer SM, Carpenter CC, Cooper DA, Fischl MA, Gatell JM, Gazzard BG, Hirsch MS, Jacobsen DM, Katzenstein DA, Montaner JS, Richman DD, Saag MS, Schechter M, Schooley RT, Thompson MA, Vella S, and Volberding PA. Antiretroviral treatment for adult HIV infection in 2002: updated recommendations of the International AIDS Society-USA Panel. JAMA 288: 222-235, 2002.
64. Yki-Järvinen H. Action of insulin on glucose metabolism in vivo. Baillieres Clin Endocrinol Metab 7: 903-927, 1993.
65. Yonemitsu S, Nishimura H, Shintani M, Inoue R, Yamamoto Y, Masuzaki H, Ogawa Y, Hosoda K, Inoue G, Hayashi T, and Nakao K. Troglitazone induces GLUT4 translocation in L6 myotubes. Diabetes 50: 1093-1101, 2001.