Table of Contents Author Guidelines Submit a Manuscript
PPAR Research
Volume 2009, Article ID 607902, 8 pages
http://dx.doi.org/10.1155/2009/607902
Review Article

HIV-1 Infection and the PPAR -Dependent Control of Adipose Tissue Physiology

1Department of Biochemistry and Molecular Biology and Institute of Biomedicine, University of Barcelona, 08028 Barcelona, Spain
2CIBER Fisiopatología de la Obesidad y Nutrición, Instituto de Salud Carlos III, 08028 Barcelona, Spain
3Department of Internal Medicine, Hospital de la Santa Creu i Sant Pau, 08025 Barcelona, Spain

Received 5 May 2008; Accepted 23 July 2008

Academic Editor: Jacqueline Capeau

Copyright © 2009 Marta Giralt et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. S. Grinspoon and A. Carr, “Cardiovascular risk and body-fat abnormalities in HIV-infected adults,” The New England Journal of Medicine, vol. 352, no. 1, pp. 48–62, 2005. View at Publisher · View at Google Scholar
  2. E. D. Rosen, C. J. Walkey, P. Puigserver, and B. M. Spiegelman, “Transcriptional regulation of adipogenesis,” Genes & Development, vol. 14, no. 11, pp. 1293–1307, 2000. View at Google Scholar
  3. M.-L. Gougeon, L. Pénicaud, B. Fromenty, P. Leclercq, J.-P. Viard, and J. Capeau, “Adipocytes targets and actors in the pathogenesis of HIV-associated lipodystrophy and metabolic alterations,” Antiviral Therapy, vol. 9, no. 2, pp. 161–177, 2004. View at Google Scholar
  4. F. Villarroya, P. Domingo, and M. Giralt, “Lipodystrophy in HIV 1-infected patients: lessons for obesity research,” International Journal of Obesity, vol. 31, no. 12, pp. 1763–1776, 2007. View at Publisher · View at Google Scholar
  5. A. Carr, K. Samaras, D. J. Chisholm, and D. A. Cooper, “Pathogenesis of HIV-1-protease inhibitor-associated peripheral lipodystrophy, hyperlipidaemia, and insulin resistance,” The Lancet, vol. 351, no. 9119, pp. 1881–1883, 1998. View at Publisher · View at Google Scholar
  6. D. Nolan, M. John, and S. Mallal, “Antiretoviral therapy and the lipodystrophy syndrome, part 2: concepts in aetiopathogenesis,” Antiviral Therapy, vol. 6, no. 3, pp. 145–160, 2001. View at Google Scholar
  7. P. W. G. Mallon, P. Unemori, R. Sedwell et al., “In vivo, nucleoside reverse-transcriptase inhibitors alter expression of both mitochondrial and lipid metabolism genes in the absence of depletion of mitochondrial DNA,” Journal of Infectious Diseases, vol. 191, no. 10, pp. 1686–1696, 2005. View at Publisher · View at Google Scholar
  8. J. Miller, A. Carr, S. Emery et al., “HIV lipodystrophy: prevalence, severity and correlates of risk in Australia,” HIV Medicine, vol. 4, no. 3, pp. 293–301, 2003. View at Publisher · View at Google Scholar
  9. D. P. Kotler, J. Wang, and R. N. Pierson Jr., “Body composition studies in patients with the acquired immunodeficiency syndrome,” American Journal of Clinical Nutrition, vol. 42, no. 6, pp. 1255–1265, 1985. View at Google Scholar
  10. M. Ott, B. Lembcke, H. Fischer et al., “Early changes of body composition in human immunodeficiency virus-infected patients: tetrapolar body impedance analysis indicates significant malnutrition,” American Journal of Clinical Nutrition, vol. 57, no. 1, pp. 15–19, 1993. View at Google Scholar
  11. F. Visnegarwala, S. S. Raghavan, C. M. Mullin et al., “Sex differences in the associations of HIV disease characteristics and body composition in antiretroviral-naive persons,” American Journal of Clinical Nutrition, vol. 82, no. 4, pp. 850–856, 2005. View at Google Scholar
  12. C. Grunfeld, D. P. Kotler, R. Hamadeh, A. Tierney, J. Wang, and R. N. Pierson Jr., “Hypertriglyceridemia in acquired immunodeficiency syndrome,” The American Journal of Medicine, vol. 86, no. 1, pp. 27–31, 1989. View at Publisher · View at Google Scholar
  13. M. D. Peck, E. Mantero-Atienza, M. J. Miguez-Burbano et al., “The esterified plasma fatty acid profile is altered in early HIV-1 infection,” Lipids, vol. 28, no. 7, pp. 593–597, 1993. View at Publisher · View at Google Scholar
  14. M. van der Valk, P. Reiss, F. C. van Leth et al., “Highly active antiretroviral therapy-induced lipodystrophy has minor effects on human immunodeficiency virus-induced changes in lipolysis, but normalizes resting energy expenditure,” The Journal of Clinical Endocrinology & Metabolism, vol. 87, no. 11, pp. 5066–5071, 2002. View at Publisher · View at Google Scholar
  15. A. Balasubramanyam, H. Mersmann, F. Jahoor et al., “Effects of transgenic expression of HIV-1 Vpr on lipid and energy metabolism in mice,” American Journal of Physiology, vol. 292, no. 1, pp. E40–E48, 2007. View at Publisher · View at Google Scholar
  16. A. J. Vidal-Puig, R. V. Considine, M. Jimenez-Liñan et al., “Peroxisome proliferator-activated receptor gene expression in human tissues. Effects of obesity, weight loss, and regulation by insulin and glucocorticoids,” The Journal of Clinical Investigation, vol. 99, no. 10, pp. 2416–2422, 1997. View at Publisher · View at Google Scholar
  17. M. Ricote, A. C. Li, T. M. Willson, C. J. Kelly, and C. K. Glass, “The peroxisome proliferator-activated receptor-γ is a negative regulator of macrophage activation,” Nature, vol. 391, no. 6662, pp. 79–82, 1998. View at Publisher · View at Google Scholar
  18. N. Marx, T. Bourcier, G. K. Sukhova, P. Libby, and J. Plutzky, “PPARγ activation in human endothelial cells increases plasminogen activator inhibitor type-1 expression: PPARγ as a potential mediator in vascular disease,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 19, no. 3, pp. 546–551, 1999. View at Google Scholar
  19. E. Hu, J. B. Kim, P. Sarraf, and B. M. Spiegelman, “Inhibition of adipogenesis through MAP kinase-mediated phosphorylation of PPARγ,” Science, vol. 274, no. 5295, pp. 2100–2103, 1996. View at Publisher · View at Google Scholar
  20. D. Yamashita, T. Yamaguchi, M. Shimizu, N. Nakata, F. Hirose, and T. Osumi, “The transactivating function of peroxisome proliferator-activated receptor γ is negatively regulated by SUMO conjugation in the amino-terminal domain,” Genes to Cells, vol. 9, no. 11, pp. 1017–1029, 2004. View at Publisher · View at Google Scholar
  21. E. Powell, P. Kuhn, and W. Xu, “Nuclear receptor cofactors in PPARγ-mediated adipogenesis and adipocyte energy metabolism,” PPAR Research, vol. 2007, Article ID 53843, 11 pages, 2007. View at Publisher · View at Google Scholar
  22. N. J. McKenna and B. W. O'Malley, “Combinatorial control of gene expression by nuclear receptors and coregulators,” Cell, vol. 108, no. 4, pp. 465–474, 2002. View at Publisher · View at Google Scholar
  23. P. Puigserver, Z. Wu, C. W. Park, R. Graves, M. Wright, and B. M. Spiegelman, “A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis,” Cell, vol. 92, no. 6, pp. 829–839, 1998. View at Publisher · View at Google Scholar
  24. I. Tzameli, H. Fang, M. Ollero et al., “Regulated production of a peroxisome proliferator-activated receptor-? ligand during an early phase of adipocyte differentiation in 3T3-L1 adipocytes,” The Journal of Biological Chemistry, vol. 279, no. 34, pp. 36093–36102, 2004. View at Publisher · View at Google Scholar
  25. B. M. Forman, P. Tontonoz, J. Chen, R. P. Brun, B. M. Spiegelman, and R. M. Evans, “15-deoxy-Δ12,14-prostaglandin J2 is a ligand for the adipocyte determination factor PPARγ,” Cell, vol. 83, no. 5, pp. 803–812, 1995. View at Publisher · View at Google Scholar
  26. J. M. Lehmann, L. B. Moore, T. A. Smith-Oliver, W. O. Wilkison, T. M. Willson, and S. A. Kliewer, “An antidiabetic thiazolidinedione is a high affinity ligand for peroxisome proliferator-activated receptor γ (PPARγ),” The Journal of Biological Chemistry, vol. 270, no. 22, pp. 12953–12956, 1995. View at Publisher · View at Google Scholar
  27. J. M. Olefsky and A. R. Saltiel, “PPARγ and the treatment of insulin resistance,” Trends in Endocrinology and Metabolism, vol. 11, no. 9, pp. 362–368, 2000. View at Publisher · View at Google Scholar
  28. C. Knouff and J. Auwerx, “Peroxisome proliferator-activated receptor-γ calls for activation in moderation: lessons from genetics and pharmacology,” Endocrine Reviews, vol. 25, no. 6, pp. 899–918, 2004. View at Publisher · View at Google Scholar
  29. R. F. Kletzien, S. D. Clarke, and R. G. Ulrich, “Enhancement of adipocyte differentiation by an insulin-sensitizing agent,” Molecular Pharmacology, vol. 41, no. 2, pp. 393–398, 1992. View at Google Scholar
  30. P. Tontonoz, E. Hu, and B. M. Spiegelman, “Stimulation of adipogenesis in fibroblasts by PPARγ2, a lipid-activated transcription factor,” Cell, vol. 79, no. 7, pp. 1147–1156, 1994. View at Publisher · View at Google Scholar
  31. Y. Barak, M. C. Nelson, E. S. Ong et al., “PPAR? is required for placental, cardiac, and adipose tissue development,” Molecular Cell, vol. 4, no. 4, pp. 585–595, 1999. View at Publisher · View at Google Scholar
  32. E. D. Rosen, P. Sarraf, A. E. Troy et al., “PPAR? is required for the differentiation of adipose tissue in vivo and in vitro,” Molecular Cell, vol. 4, no. 4, pp. 611–617, 1999. View at Publisher · View at Google Scholar
  33. W. He, Y. Barak, A. Hevener et al., “Adipose-specific peroxisome proliferator-activated receptor ? knockout causes insulin resistance in fat and liver but not in muscle,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 26, pp. 15712–15717, 2003. View at Publisher · View at Google Scholar
  34. K. Schoonjans, J. Peinado-Onsurbe, A.-M. Lefebvre et al., “PPARa and PPAR? activators direct a distinct tissue-specific transcriptional response via a PPRE in the lipoprotein lipase gene,” The EMBO Journal, vol. 15, no. 19, pp. 5336–5348, 1996. View at Google Scholar
  35. P. Tontonoz, E. Hu, R. A. Graves, A. I. Budavari, and B. M. Spiegelman, “mPPARγ2: tissue-specific regulator of an adipocyte enhancer,” Genes & Development, vol. 8, no. 10, pp. 1224–1234, 1994. View at Publisher · View at Google Scholar
  36. P. Tontonoz, E. Hu, J. Devine, E. G. Beale, and B. M. Spiegelman, “PPARγ2 regulates adipose expression of the phosphoenolpyruvate carboxykinase gene,” Molecular and Cellular Biology, vol. 15, no. 1, pp. 351–357, 1995. View at Google Scholar
  37. Y. Olswang, H. Cohen, O. Papo et al., “A mutation in the peroxisome proliferator-activated receptor ?-binding site in the gene for the cytosolic form of phosphoenolpyruvate carboxykinase reduces adipose tissue size and fat content in mice,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 2, pp. 625–630, 2002. View at Publisher · View at Google Scholar
  38. Z. Wu, Y. Xie, R. F. Morrison, N. L. R. Bucher, and S. R. Farmer, “PPARγ induces the insulin-dependent glucose transporter GLUT4 in the absence of C/EBPα during the conversion of 3T3 fibroblasts into adipocytes,” The Journal of Clinical Investigation, vol. 101, no. 1, pp. 22–32, 1998. View at Publisher · View at Google Scholar
  39. E. Hondares, O. Mora, P. Yubero et al., “Thiazolidinediones and rexinoids induce peroxisome proliferator-activated receptor-coactivator (PGC)-1a gene transcription: an autoregulatory loop controls PGC-1a expression in adipocytes via peroxisome proliferator-activated receptor-? coactivation,” Endocrinology, vol. 147, no. 6, pp. 2829–2838, 2006. View at Publisher · View at Google Scholar
  40. L. Wilson-Fritch, A. Burkart, G. Bell et al., “Mitochondrial biogenesis and remodeling during adipogenesis and in response to the insulin sensitizer rosiglitazone,” Molecular and Cellular Biology, vol. 23, no. 3, pp. 1085–1094, 2003. View at Publisher · View at Google Scholar
  41. S. M. Rangwala and M. A. Lazar, “Peroxisome proliferator-activated receptor γ in diabetes and metabolism,” Trends in Pharmacological Sciences, vol. 25, no. 6, pp. 331–336, 2004. View at Publisher · View at Google Scholar
  42. R. K. Semple, V. K. K. Chatterjee, and S. O'Rahilly, “PPARγ and human metabolic disease,” The Journal of Clinical Investigation, vol. 116, no. 3, pp. 581–589, 2006. View at Publisher · View at Google Scholar
  43. I. Barroso, M. Gurnell, V. E. F. Crowley et al., “Dominant negative mutations in human PPAR? associated with severe insulin resistance, diabetes mellitus and hypertension,” Nature, vol. 402, no. 6764, pp. 880–883, 1999. View at Publisher · View at Google Scholar
  44. D. B. Savage, G. D. Tan, C. L. Acerini et al., “Human metabolic syndrome resulting from dominant-negative mutations in the nuclear receptor peroxisome proliferator-activated receptor-?,” Diabetes, vol. 52, no. 4, pp. 910–917, 2003. View at Publisher · View at Google Scholar
  45. L. A. Moraes, L. Piqueras, and D. Bishop-Bailey, “Peroxisome proliferator-activated receptors and inflammation,” Pharmacology & Therapeutics, vol. 110, no. 3, pp. 371–385, 2006. View at Publisher · View at Google Scholar
  46. P. Tontonoz, L. Nagy, J. G. A. Alvarez, V. A. Thomazy, and R. M. Evans, “PPARγ promotes monocyte/macrophage differentiation and uptake of oxidized LDL,” Cell, vol. 93, no. 2, pp. 241–252, 1998. View at Publisher · View at Google Scholar
  47. A. Chawla, Y. Barak, L. Nagy, D. Liao, P. Tontonoz, and R. M. Evans, “PPAR-γ dependent and independent effects on macrophage-gene expression in lipid metabolism and inflammation,” Nature Medicine, vol. 7, no. 1, pp. 48–52, 2001. View at Publisher · View at Google Scholar
  48. K. J. Moore, E. D. Rosen, M. L. Fitzgerald et al., “The role of PPAR-? in macrophage differentiation and cholesterol uptake,” Nature Medicine, vol. 7, no. 1, pp. 41–47, 2001. View at Publisher · View at Google Scholar
  49. A. Chawla, W. A. Boisvert, C.-H. Lee et al., “A PPAR?-LXR-ABCA1 pathway in macrophages is involved in cholesterol efflux and atherogenesis,” Molecular Cell, vol. 7, no. 1, pp. 161–171, 2001. View at Publisher · View at Google Scholar
  50. S. E. Shoelson, J. Lee, and A. B. Goldfine, “Inflammation and insulin resistance,” The Journal of Clinical Investigation, vol. 116, no. 7, pp. 1793–1801, 2006. View at Publisher · View at Google Scholar
  51. J. I. Odegaard, R. R. Ricardo-Gonzalez, M. H. Goforth et al., “Macrophage-specific PPAR? controls alternative activation and improves insulin resistance,” Nature, vol. 447, no. 7148, pp. 1116–1120, 2007. View at Publisher · View at Google Scholar
  52. A. M. Sharma and B. Staels, “Peroxisome proliferator-activated receptor γ and adipose tissue—understanding obesity-related changes in regulation of lipid and glucose metabolism,” The Journal of Clinical Endocrinology & Metabolism, vol. 92, no. 2, pp. 386–395, 2007. View at Publisher · View at Google Scholar
  53. M. Giralt, P. Domingo, J. P. Guallar et al., “HIV-1 infection alters gene expression in adipose tissue, which contributes to HIV-1/HAART-associated lipodystrophy,” Antiviral Therapy, vol. 11, no. 6, pp. 729–740, 2006. View at Google Scholar
  54. J.-P. Bastard, M. Caron, H. Vidal et al., “Association between altered expression of adipogenic factor SREBP1 in lipoatrophic adipose tissue from HIV-1-infected patients and abnormal adipocyte differentiation and insulin resistance,” The Lancet, vol. 359, no. 9311, pp. 1026–1031, 2002. View at Publisher · View at Google Scholar
  55. C. S. Pace, A. M. Martin, E. L. Hammond, C. D. Mamotte, D. A. Nolan, and S. A. Mallal, “Mitochondrial proliferation, DNA depletion and adipocyte differentiation in subcutaneous adipose tissue of HIV-positive HAART recipients,” Antiviral Therapy, vol. 8, no. 4, pp. 323–331, 2003. View at Google Scholar
  56. J. K. Min, P. Leclercq, E. Lanoy et al., “A 6-month interruption of antiretroviral therapy improves adipose tissue function in HIV-infected patients: the ANRS EP29 Lipostop Study,” Antiviral Therapy, vol. 12, no. 8, pp. 1273–1283, 2007. View at Google Scholar
  57. S. Caspar-Bauguil, B. Cousin, A. Galinier et al., “Adipose tissues as an ancestral immune organ: site-specific change in obesity,” FEBS Letters, vol. 579, no. 17, pp. 3487–3492, 2005. View at Publisher · View at Google Scholar
  58. H. Wu, S. Ghosh, X. D. Perrard et al., “T-cell accumulation and regulated on activation, normal T cell expressed and secreted upregulation in adipose tissue in obesity,” Circulation, vol. 115, no. 8, pp. 1029–1038, 2007. View at Publisher · View at Google Scholar
  59. U. Hazan, I. A. Romero, R. Cancello et al., “Human adipose cells express CD4, CXCR4, and CCR5 receptors: a new target cell type for the immunodeficiency virus-1?” The FASEB Journal, vol. 16, no. 10, pp. 1254–1256, 2002. View at Publisher · View at Google Scholar
  60. N. Dupin, M. Buffet, A.-G. Marcelin et al., “HIV and antiretroviral drug distribution in plasma and fat tissue of HIV-infected patients with lipodystrophy,” AIDS, vol. 16, no. 18, pp. 2419–2424, 2002. View at Publisher · View at Google Scholar
  61. S. Munier, A. Borjabad, M. Lemaire, V. Mariot, and U. Hazan, “In vitro infection of human primary adipose cells with HIV-1: a reassessment,” AIDS, vol. 17, no. 17, pp. 2537–2539, 2003. View at Publisher · View at Google Scholar
  62. T. Maurin, C. Saillan-Barreau, B. Cousin, L. Casteilla, A. Doglio, and L. Pénicaud, “Tumor necrosis factor-α stimulates HIV-1 production in primary culture of human adipocytes,” Experimental Cell Research, vol. 304, no. 2, pp. 544–551, 2005. View at Publisher · View at Google Scholar
  63. J. A. Johnson, J. B. Albu, E. S. Engelson et al., “Increased systemic and adipose tissue cytokines in patients with HIV-associated lipodystrophy,” American Journal of Physiology, vol. 286, no. 2, pp. E261–E271, 2004. View at Publisher · View at Google Scholar
  64. R. A. Hegele, “Lessons from human mutations in PPARγ,” International Journal of Obesity, vol. 29, supplement 1, pp. S31–S35, 2005. View at Publisher · View at Google Scholar
  65. K. G. Murti, P. S. Brown, L. Ratner, and J. V. Garcia, “Highly localized tracks of human immunodeficiency virus type 1 Nef in the nucleus of cells of a human CD4+ T-cell line,” Proceedings of the National Academy of Sciences of the United States of America, vol. 90, no. 24, pp. 11895–11899, 1993. View at Publisher · View at Google Scholar
  66. K. Otake, S. Omoto, T. Yamamoto et al., “HIV-1 Nef protein in the nucleus influences adipogenesis as well as viral transcription through the peroxisome proliferator-activated receptors,” AIDS, vol. 18, no. 2, pp. 189–198, 2004. View at Publisher · View at Google Scholar
  67. S. Shrivastav, T. Kino, T. Cunningham et al., “Human immunodeficiency virus (HIV)-1 viral protein R suppresses transcriptional activity of peroxisome proliferator-activated receptor ? and inhibits adipocyte differentiation: implications for HIV-associated lipodystrophy,” Molecular Endocrinology, vol. 22, no. 2, pp. 234–247, 2008. View at Publisher · View at Google Scholar
  68. P. Henklein, K. Bruns, M. P. Sherman et al., “Functional and structural characterization of synthetic HIV-1 Vpr that transduces cells, localizes to the nucleus, and induces G2 cell cycle arrest,” The Journal of Biological Chemistry, vol. 275, no. 41, pp. 32016–32026, 2000. View at Publisher · View at Google Scholar
  69. D. N. Levy, Y. Refaeli, R. R. MacGregor, and D. B. Weiner, “Serum Vpr regulates productive infection and latency of human immunodeficiency virus type 1,” Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 23, pp. 10873–10877, 1994. View at Publisher · View at Google Scholar
  70. D. A. Sarruf, I. Iankova, A. Abella, S. Assou, S. Miard, and L. Fajas, “Cyclin D3 promotes adipogenesis through activation of peroxisome proliferator-activated receptor γ,” Molecular and Cellular Biology, vol. 25, no. 22, pp. 9985–9995, 2005. View at Publisher · View at Google Scholar
  71. A. Abella, P. Dubus, M. Malumbres et al., “Cdk4 promotes adipogenesis through PPAR? activation,” Cell Metabolism, vol. 2, no. 4, pp. 239–249, 2005. View at Publisher · View at Google Scholar
  72. L. Fajas, R. L. Landsberg, Y. Huss-Garcia, C. Sardet, J. A. Lees, and J. Auwerx, “E2Fs regulate adipocyte differentiation,” Developmental Cell, vol. 3, no. 1, pp. 39–49, 2002. View at Publisher · View at Google Scholar
  73. C. Ambrosino, C. Palmieri, A. Puca et al., “Physical and functional interaction of HIV-1 Tat with E2F-4, a transcriptional regulator of mammalian cell cycle,” The Journal of Biological Chemistry, vol. 277, no. 35, pp. 31448–31458, 2002. View at Publisher · View at Google Scholar
  74. S. Amini, K. Khalili, and B. E. Sawaya, “Effect of HIV-1 Vpr on cell cycle regulators,” DNA and Cell Biology, vol. 23, no. 4, pp. 249–260, 2004. View at Publisher · View at Google Scholar
  75. B. Y. Zhou and J. J. He, “Proliferation inhibition of astrocytes, neurons, and non-glial cells by intracellularly expressed human immunodeficiency virus type 1 (HIV-1) Tat protein,” Neuroscience Letters, vol. 359, no. 3, pp. 155–158, 2004. View at Publisher · View at Google Scholar
  76. G. Marzio, M. Tyagi, M. I. Gutierrez, and M. Giacca, “HIV-1 Tat transactivator recruits p300 and CREB-binding protein histone acetyltransferases to the viral promoter,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 23, pp. 13519–13524, 1998. View at Publisher · View at Google Scholar
  77. T. Kino, A. Gragerov, O. Slobodskaya, M. Tsopanomichalou, G. P. Chrousos, and G. N. Pavlakis, “Human immunodeficiency virus type 1 (HIV-1) accessory protein Vpr induces transcription of the HIV-1 and glucocorticoid-responsive promoters by binding directly to p300/CBP coactivators,” Journal of Virology, vol. 76, no. 19, pp. 9724–9734, 2002. View at Publisher · View at Google Scholar
  78. V. Desai-Yajnik, E. Hadzic, P. Modlinger, S. Malhotra, G. Gechlik, and H. H. Samuels, “Interactions of thyroid hormone receptor with the human immunodeficiency virus type 1 (HIV-1) long terminal repeat and the HIV-1 Tat transactivator,” Journal of Virology, vol. 69, no. 8, pp. 5103–5112, 1995. View at Google Scholar
  79. J. A. A. Ladias, “Convergence of multiple nuclear receptor signaling pathways onto the long terminal repeat of human immunodeficiency virus-1,” The Journal of Biological Chemistry, vol. 269, no. 8, pp. 5944–5951, 1994. View at Google Scholar
  80. I. Issemann and S. Green, “Activation of a member of the steroid hormone receptor superfamily by peroxisome proliferators,” Nature, vol. 347, no. 6294, pp. 645–650, 1990. View at Publisher · View at Google Scholar
  81. M. M. Hayes, B. R. Lane, S. R. King, D. M. Markovitz, and M. J. Coffey, “Peroxisome proliferator-activated receptor γ agonists inhibit HIV-1 replication in macrophages by transcriptional and post-transcriptional effects,” The Journal of Biological Chemistry, vol. 277, no. 19, pp. 16913–16919, 2002. View at Publisher · View at Google Scholar
  82. S. M. Wahl, T. Greenwell-Wild, G. Peng, G. Ma, J. M. Orenstein, and N. Vázquez, “Viral and host cofactors facilitate HIV-1 replication in macrophages,” Journal of Leukocyte Biology, vol. 74, no. 5, pp. 726–735, 2003. View at Publisher · View at Google Scholar
  83. P. R. Skolnik, M. F. Rabbi, J.-M. Mathys, and A. S. Greenberg, “Stimulation of peroxisome proliferator-activated receptors α and γ blocks HIV-1 replication and TNFα production in acutely infected primary blood cells, chronically infected U1 cells, and alveolar macrophages from HIV-infected subjects,” Journal of Acquired Immune Deficiency Syndromes, vol. 31, no. 1, pp. 1–10, 2002. View at Google Scholar
  84. R. Potula, S. H. Ramirez, B. Knipe et al., “Peroxisome proliferator-receptor ? agonist suppresses HIV-1 replication by inhibition of the nuclear factor ?B in vitro and in an animal model of HIV-1 encephalitis,” Journal of NeuroVirology, vol. 12, supplement 1, p. 66, 2006. View at Google Scholar