Current topics in HIV pathogenesis, part 2: Inflammation drives a Warburg-like effect on the metabolism of HIV-infected subjects

Cytokine and Growth Factor Reviews

Volumn 28, Issue , 2016, Pages 1-10

  Aounallah, Mouna ^a   Dagenais Lussier, Xavier ^a   El Far, Mohamed ^b   Mehraj, Vikram ^c   Jenabian, Mohammad Ali ^d   Routy, Jean Pierre ^c   van Grevenynghe, Julien ^a  

^a INRS INSTITUT ARMAND FRAPPIER   (Canada)

^b CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^c MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^d UNIVERSITÉ DU QUÉBEC À MONTRÉAL   (Canada)

Author keywords

HIV 1; Inflammasome; Inflammation; Innate immunity; Metabolism

Indexed keywords

CRYOPYRIN; INDOLEAMINE 2,3 DIOXYGENASE; INDOLEAMINE 2,3 DIOXYGENASE 1; INFLAMMASOME; UNCLASSIFIED DRUG;

BACTERIAL TRANSLOCATION; CD4+ T LYMPHOCYTE; CHRONIC INFLAMMATION; DISEASE ASSOCIATION; DISEASE COURSE; DYSBIOSIS; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOCOMPETENT CELL; INFLAMMATION; INFLAMMATORY CELL; INNATE IMMUNITY; INTESTINE INJURY; LIPID METABOLISM; LYMPHOCYTE DEPLETION; METABOLIC SYNDROME X; METABOLISM; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SHORT SURVEY; VIRUS PATHOGENESIS; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGY; PATHOLOGY; QUALITY OF LIFE; VIROLOGY;

CD4-POSITIVE T-LYMPHOCYTES; HIV INFECTIONS; HIV-1; HUMANS; IMMUNITY, INNATE; INFLAMMATION; QUALITY OF LIFE;

EID: 84956688757     PISSN: 13596101     EISSN: 18790305     Source Type: Journal    
DOI: 10.1016/j.cytogfr.2016.01.001     Document Type: Short Survey

References (100)

1. Frezza C., Mauro C. The metabolic challenges of immune cells in health and disease. Front. Immunol. 2015, 6:293.
2. Li H.B., Jin C., Chen Y., Flavell R.A. Inflammasome activation and metabolic disease progression. Cytokine Growth Factor Rev. 2014, 25:699-706.
3. Hotamisligil G.S., Erbay E. Nutrient sensing and inflammation in metabolic diseases. Nat. Rev. Immunol. 2008, 8:923-934.
4. Kumar H., Kawai T., Akira S. Pathogen recognition by the innate immune system. Int. Rev. Immunol. 2011, 30:16-34.
5. Martinon F. Dangerous liaisons: mitochondrial DNA meets the NLRP3 inflammasome. Immunity 2012, 36:313-315.
6. Wegiel B., Larsen R., Gallo D., Chin B.Y., Harris C., Mannam P., et al. Macrophages sense and kill bacteria through carbon monoxide-dependent inflammasome activation. J. Clin. Investig. 2014, 124:4926-4940.
7. Lamkanfi M., Dixit V.M. The inflammasomes. PLoS Pathog. 2009, 5:e1000510.
8. Mariathasan S., Monack D.M. Inflammasome adaptors and sensors: intracellular regulators of infection and inflammation. Nat. Rev. Immunol. 2007, 7:31-40.
9. McGettrick A.F., O'Neill L.A. NLRP3 and IL-1beta in macrophages as critical regulators of metabolic diseases. Diabetes Obesity Metabol. 2013, 15(Suppl. (3)):19-25.
10. McGettrick A.F., O'Neill L.A. How metabolism generates signals during innate immunity and inflammation. J. Biol. Chem. 2013, 288:22893-22898.
11. Norata G.D., Caligiuri G., Chavakis T., Matarese G., Netea M.G., Nicoletti A., et al. The cellular and molecular basis of translational immunometabolism. Immunity 2015, 43:421-434.
12. Palsson-McDermott E.M., O'Neill L.A. The Warburg effect then and now: from cancer to inflammatory diseases. BioEssays: News Rev. Mol. Cell. Dev. Biol. 2013, 35:965-973.
13. Popa C., Netea M.G., van Riel P.L., van der Meer J.W., Stalenhoef A.F. The role of TNF-alpha in chronic inflammatory conditions, intermediary metabolism, and cardiovascular risk. J. Lipid Res. 2007, 48:751-762.
14. K.R. Feingold, C. Grunfeld, 2000. The effect of inflammation and infection on lipids and lipoproteins. In: L.J. De Groot, P. Beck-Peccoz, G. Chrousos, K. Dungan, A. Grossman, J.M. Hershman, et al., (Eds.) Endotext, South Dartmouth (MA).
15. Zorzi F., Calabrese E., Monteleone G. Pathogenic aspects and therapeutic avenues of intestinal fibrosis in Crohn's disease. Clin. Sci. (Lond.) 2015, 129:1107-1113.
16. de Zoete M.R., Palm N.W., Zhu S., Flavell R.A. Inflammasomes 2014, 6:a016287. Cold Spring Harbor Perspectives in Biology.
17. Franchi L., Eigenbrod T., Munoz-Planillo R., Nunez G. The inflammasome: a caspase-1-activation platform that regulates immune responses and disease pathogenesis. Nat. Immunol. 2009, 10:241-247.
18. Haneklaus M., O'Neill L.A. NLRP3 at the interface of metabolism and inflammation. Immunol. Rev. 2015, 265:53-62.
19. Fracchia K.M., Walsh C.M. Metabolic mysteries of the inflammatory response: T cell polarization and plasticity. Int. Rev. Immunol. 2015, 34:3-18.
20. Martinez-Outschoorn U.E., Curry J.M., Ko Y.H., Lin Z., Tuluc M., Cognetti D., et al. Oncogenes and inflammation rewire host energy metabolism in the tumor microenvironment: RAS and NFkappaB target stromal MCT4. Cell Cycle 2013, 12:2580-2597.
21. Peng B., Liu F., Han R., Luo G., Cathopoulis T., Lu K., et al. Dynamic metabolic change is indicative of inflammation-induced transformation of hepatic cells. Int. J. Biochem. Cell Biol. 2015, 66:45-58.
22. Vaughan R.A., Garcia-Smith R., Trujillo K.A., Bisoffi M. Tumor necrosis factor alpha increases aerobic glycolysis and reduces oxidative metabolism in prostate epithelial cells. Prostate 2013, 73:1538-1546.
23. Wen H., Ting J.P., O'Neill L.A. A role for the NLRP3 inflammasome in metabolic diseases-did Warburg miss inflammation. Nat. Immunol. 2012, 13:352-357.
24. Conley L.J., Bush T.J., Rupert A.W., Sereti I., Patel P., Brooks J.T., et al. Obesity is associated with greater inflammation and monocyte activation among HIV-infected adults receiving antiretroviral therapy. AIDS 2015, 29:2201-2207.
25. Galvan-Pena S., O'Neill L.A. Metabolic reprograming in macrophage polarization. Front. Immunol. 2014, 5:420.
26. Kelly B., O'Neill L.A. Metabolic reprogramming in macrophages and dendritic cells in innate immunity. Cell Res. 2015, 25:771-784.
27. Mills E.L., O'Neill L.A. Reprogramming mitochondrial metabolism in macrophages as an anti-inflammatory signal. Eur. J. Immunol. 2015.
28. O'Neill L.A., Pearce E.J. Immunometabolism governs dendritic cell and macrophage function. J. Exp. Med. 2015.
29. Zhu L., Zhao Q., Yang T., Ding W., Zhao Y. Cellular metabolism and macrophage functional polarization. Int. Rev. Immunol. 2015, 34:82-100.
30. Hsu P.P., Sabatini D.M. Cancer cell metabolism: Warburg and beyond. Cell 2008, 134:703-707.
31. Pouyssegur J., Dayan F., Mazure N.M. Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature 2006, 441:437-443.
32. Tannahill G.M., Curtis A.M., Adamik J., Palsson-McDermott E.M., McGettrick A.F., Goel G., et al. Succinate is an inflammatory signal that induces IL-1beta through HIF-1alpha. Nature 2013, 496:238-242.
33. Wu W., Zhao S. Metabolic changes in cancer: beyond the Warburg effect. Acta Biochim. Biophys. Sin. 2013, 45:18-26.
34. Pontillo A., Carvalho M.S., Kamada A.J., Moura R., Schindler H.C., Duarte A.J., et al. Susceptibility to Mycobacterium tuberculosis infection in HIV-positive patients is associated with CARD8 genetic variant. J. Acquir. Immune Defic. Syndr. 2013, 63:147-151.
35. Pontillo A., Oshiro T.M., Girardelli M., Kamada A.J., Crovella S., Duarte A.J. Polymorphisms in inflammasome' genes and susceptibility to HIV-1 infection. J. Acquir. Immune Defic. Syndr. 2012, 59:121-125.
36. Zhang Q., Fan H.W., Zhang J.Z., Wang Y.M., Xing H.J. NLRP3 rs35829419 polymorphism is associated with increased susceptibility to multiple diseases in humans. Genet. Mol. Res.: GMR 2015, 14:13968-13980.
37. Biancotto A., Grivel J.C., Iglehart S.J., Vanpouille C., Lisco A., Sieg S.F., et al. Abnormal activation and cytokine spectra in lymph nodes of people chronically infected with HIV-1. Blood 2007, 109:4272-4279.
38. Breen E.C. Pro- and anti-inflammatory cytokines in human immunodeficiency virus infection and acquired immunodeficiency syndrome. Pharmacol. Therap. 2002, 95:295-304.
39. Decrion A.Z., Dichamp I., Varin A., Herbein G. HIV and inflammation. Curr. HIV Res. 2005, 3:243-259.
40. Chattergoon M.A., Latanich R., Quinn J., Winter M.E., Buckheit R.W., Blankson J.N., et al. HIV and HCV activate the inflammasome in monocytes and macrophages via endosomal Toll-like receptors without induction of type 1 interferon. PLoS Pathog. 2014, 10:e1004082.
41. Guo H., Gao J., Taxman D.J., Ting J.P., Su L. HIV-1 infection induces interleukin-1beta production via TLR8 protein-dependent and NLRP3 inflammasome mechanisms in human monocytes. J. Biol. Chem. 2014, 289:21716-21726.
42. Pontillo A., Santillo B.T., Duarte A.J., Oshiro T.M. Differential inflammasome expression and IL-1beta secretion in monocyte-derived dendritic cells differentiated with IL-4 or IFN-alpha. AIDS Res. Ther. 2013, 10:35.
43. Doitsh G., Galloway N.L., Geng X., Yang Z., Monroe K.M., Zepeda O., et al. Cell death by pyroptosis drives CD4 T-cell depletion in HIV-1 infection. Nature 2014, 505:509-514.
44. Galloway N.L., Doitsh G., Monroe K.M., Yang Z., Munoz-Arias I., Levy D.N., et al. Cell-to-cell transmission of HIV-1 is required to trigger pyroptotic death of lymphoid-tissue-derived CD4T cells. Cell Rep. 2015, 12:1555-1563.
45. Haque S., Lan X., Wen H., Lederman R., Chawla A., Attia M., et al. HIV promotes NLRP3 inflammasome complex activation in murine HIV-associated nephropathy. Am. J. Pathol. 2015.
46. Walsh J.G., Reinke S.N., Mamik M.K., McKenzie B.A., Maingat F., Branton W.G., et al. Rapid inflammasome activation in microglia contributes to brain disease in HIV/AIDS. Retrovirology 2014, 11:35.
47. Tedla N., Palladinetti P., Kelly M., Kumar R.K., DiGirolamo N., Chattophadhay U., et al. Chemokines and T lymphocyte recruitment to lymph nodes in HIV infection. Am. J. Pathol. 1996, 148:1367-1373.
48. Schacker T.W., Nguyen P.L., Beilman G.J., Wolinsky S., Larson M., Reilly C., et al. Collagen deposition in HIV-1 infected lymphatic tissues and T cell homeostasis. J. Clin. Investig. 2002, 110:1133-1139.
49. Smith A.J., Toledo C.M., Wietgrefe S.W., Duan L., Schacker T.W., Reilly C.S., et al. The immunosuppressive role of IL-32 in lymphatic tissue during HIV-1 infection. J. Immunol. 2011, 186:6576-6584.
50. Fichtenbaum C.J. Inflammatory markers associated with coronary heart disease in persons with HIV infection. Curr. Infect. Dis. Rep. 2011, 13:94-101.
51. Liang H., Duan Z., Li D., Li D., Wang Z., Ren L., et al. Higher levels of circulating monocyte-platelet aggregates are correlated with viremia and increased sCD163 levels in HIV-1 infection. Cell. Mol. Immunol. 2015, 12:435-443.
52. Miller E.A., Gopal R., Valdes V., Berger J.S., Bhardwaj N., O'Brien M.P. Soluble CD40 ligand contributes to dendritic cell-mediated T-cell dysfunction in HIV-1 infection. AIDS 2015, 29:1287-1296.
53. Somsouk M., Estes J.D., Deleage C., Dunham R.M., Albright R., Inadomi J.M., et al. Gut epithelial barrier and systemic inflammation during chronic HIV infection. AIDS 2015, 29:43-51.
54. Gruys E., Toussaint M.J., Niewold T.A., Koopmans S.J. Acute phase reaction and acute phase proteins. J. Zhejiang Univ. Sci. B 2005, 6:1045-1056.
55. Brenchley J.M., Price D.A., Schacker T.W., Asher T.E., Silvestri G., Rao S., et al. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat. Med. 2006, 12:1365-1371.
56. Ancuta P., Kamat A., Kunstman K.J., Kim E.Y., Autissier P., Wurcel A., et al. Microbial translocation is associated with increased monocyte activation and dementia in AIDS patients. PloS One 2008, 3:e2516.
57. Johnson A.R., Milner J.J., Makowski L. The inflammation highway: metabolism accelerates inflammatory traffic in obesity. Immunol. Rev. 2012, 249:218-238.
58. Jenabian M.A., Mehraj V., Costiniuk C.T., Vyboh K., Kema I., Rollet K., et al. Influence of Hepatitis C Virus (HCV) sustained virological response on immunosuppressive Tryptophan catabolism in ART-treated HIV/HCV co-infected patients. J. Acquir. Immune Defic. Syndr. 2015.
59. Estes J.D., Wietgrefe S., Schacker T., Southern P., Beilman G., Reilly C., et al. Simian immunodeficiency virus-induced lymphatic tissue fibrosis is mediated by transforming growth factor beta 1-positive regulatory T cells and begins in early infection. J. Infect. Dis. 2007, 195:551-561.
60. Hamlyn E., Fidler S., Stohr W., Cooper D.A., Tambussi G., Schechter M., et al. Interleukin-6 and D-dimer levels at seroconversion as predictors of HIV-1 disease progression. AIDS 2014, 28:869-874.
61. Jenabian M.A., El-Far M., Vyboh K., Kema I., Costiniuk C.T., Thomas R., et al. Immunosuppressive Tryptophan catabolism and gut mucosal dysfunction following early HIV infection. J. Infect. Dis. 2015, 212:355-366.
62. Liovat A.S., Rey-Cuille M.A., Lecuroux C., Jacquelin B., Girault I., Petitjean G., et al. Acute plasma biomarkers of T cell activation set-point levels and of disease progression in HIV-1 infection. PloS One 2012, 7:e46143.
63. Dagenais-Lussier X., Mouna A., Routy J.P., Tremblay C., Sekaly R.P., El-Far M., et al. Current topics in HIV-1 pathogenesis: the emergence of deregulated immuno-metabolism in HIV-infected subjects. Cytokine Growth Factor Rev. 2015.
64. Calza L., Magistrelli E., Danese I., Colangeli V., Borderi M., Bon I., et al. Changes in serum markers of inflammation and endothelial activation in HIV-infected antiretroviral naive patients starting a treatment with abacavir-lamivudine or tenofovir-emtricitabine plus efavirenz. Curr. HIV Res. 2016, 14:61-70.
65. Jong E., Louw S., van Gorp E.C., Meijers J.C., ten Cate H., Jacobson B.F. The effect of initiating combined antiretroviral therapy on endothelial cell activation and coagulation markers in South African HIV-infected individuals. Thromb. Haemost. 2010, 104:1228-1234.
66. Kim C.J., McKinnon L.R., Kovacs C., Kandel G., Huibner S., Chege D., et al. Mucosal Th17 cell function is altered during HIV infection and is an independent predictor of systemic immune activation. J. Immunol. 2013, 191:2164-2173.
67. Lederman M.M., Calabrese L., Funderburg N.T., Clagett B., Medvik K., Bonilla H., et al. Immunologic failure despite suppressive antiretroviral therapy is related to activation and turnover of memory CD4 cells. J. Infect. Dis. 2011, 204:1217-1226.
68. Castley A., Berry C., French M., Fernandez S., Krueger R., Nolan D. Elevated plasma soluble CD14 and skewed CD16+ monocyte distribution persist despite normalisation of soluble CD163 and CXCL10 by effective HIV therapy: a changing paradigm for routine HIV laboratory monitoring?. PloS One 2014, 9:e115226.
69. Piroth L., Moinot L., Yeni P., Avettand-Fenoel V., Reynes J., Girard P.M., et al. Immunity, inflammation and reservoir in patients at an early stage of HIV infection on intermittent ART (ANRS 141 TIPI Trial). J. Antimicrob. Chemother. 2015.
70. Byakwaga H., Boum Y., 2nd Huang Y., Muzoora C., Kembabazi A., Weiser S.D., et al. The kynurenine pathway of tryptophan catabolism, CD4+ T-cell recovery, and mortality among HIV-infected Ugandans initiating antiretroviral therapy. J. Infect. Dis. 2014, 210:383-391.
71. Favre D., Mold J., Hunt P.W., Kanwar B., Loke P., Seu L., et al. Tryptophan catabolism by indoleamine 2,3-dioxygenase 1 alters the balance of TH17 to regulatory T cells in HIV disease. Sci. Transl. Med. 2010, 2:32ra6.
72. Jenabian M.A., Patel M., Kema I., Kanagaratham C., Radzioch D., Thebault P., et al. Distinct tryptophan catabolism and Th17/Treg balance in HIV progressors and elite controllers. PloS One 2013, 8:e78146.
73. Jenabian M.A., Patel M., Kema I., Vyboh K., Kanagaratham C., Radzioch D., et al. Soluble CD40-ligand (sCD40L, sCD154) plays an immunosuppressive role via regulatory T cell expansion in HIV infection. Clin. Exp. Immunol. 2014, 178:102-111.
74. Gaardbo J.C., Trosied M., Stiksrud B., Midttun O., Ueland P.M., Ullum H., et al. Increased Tryptophan catabolism is associated with increased frequency of CD161+ Tc17/MAIT cells and lower CD4+ T-cell count in HIV-1 infected patients on cART after 2 years of follow-up. J. Acquir. Immune Defic. Syndr. 2015, 70:228-235.
75. Glavan T.W., Gaulke C.A., Hirao L.A., Sankaran-Walters S., Dandekar S. SIV-infection-driven changes of pattern recognition receptor expression in mesenteric lymph nodes and gut microbiota dysbiosis. J. Med. Primatol. 2015, 44:241-252.
76. Glavan T.W., Gaulke C.A., Santos Rocha C., Sankaran-Walters S., Hirao L.A., Raffatellu M., et al. Gut immune dysfunction through impaired innate pattern recognition receptor expression and gut microbiota dysbiosis in chronic SIV infection. Mucosal Immunol. 2015.
77. Nowak P., Troseid M., Avershina E., Barqasho B., Neogi U., Holm K., et al. Gut microbiota diversity predicts immune status in HIV-1 infection. AIDS 2015, 29:2409-2418.
78. Vujkovic-Cvijin I., Dunham R.M., Iwai S., Maher M.C., Albright R.G., Broadhurst M.J., et al. Dysbiosis of the gut microbiota is associated with HIV disease progression and tryptophan catabolism. Sci. Transl. Med. 2013, 5:193ra91.
79. Borges A.H., O'Connor J.L., Phillips A.N., Baker J.V., Vjecha M.J., Losso M.H., et al. Factors associated with D-dimer levels in HIV-infected individuals. PloS One 2014, 9:e90978.
80. Borges A.H., O'Connor J.L., Phillips A.N., Ronsholt F.F., Pett S., Vjecha M.J., et al. Factors associated with plasma IL-6 levels during HIV infection. J. Infect. Dis. 2015, 212:585-595.
81. Pedersen K.K., Pedersen M., Troseid M., Gaardbo J.C., Lund T.T., Thomsen C., et al. Microbial translocation in HIV infection is associated with dyslipidemia, insulin resistance, and risk of myocardial infarction. J. Acquir. Immune Defic. Syndr. 2013, 64:425-433.
82. Zidar D.A., Juchnowski S., Ferrari B., Clagett B., Pilch-Cooper H.A., Rose S., et al. Oxidized LDL levels are increased in HIV infection and may drive monocyte activation. J. Acquir. Immune Defic. Syndr. 2015, 69:154-160.
83. Falasca K., Manigrasso M.R., Racciatti D., Zingariello P., Dalessandro M., Ucciferri C., et al. Associations between hypertriglyceridemia and serum ghrelin, adiponectin, and IL-18 levels in HIV-infected patients. Ann. Clin. Lab. Sci. 2006, 36:59-66.
84. Iannello A., Samarani S., Debbeche O., Tremblay C., Toma E., Boulassel M.R., et al. Role of interleukin-18 in the development and pathogenesis of AIDS. AIDS Rev. 2009, 11:115-125.
85. Yearley J.H., Xia D., Pearson C.B., Carville A., Shannon R.P., Mansfield K.G. Interleukin-18 predicts atherosclerosis progression in SIV-infected and uninfected rhesus monkeys (Macaca mulatta) on a high-fat/high-cholesterol diet. Lab. Investig. J. Tech. Methods Pathol. 2009, 89:657-667.
86. Maisa A., Hearps A.C., Angelovich T.A., Pereira C.F., Zhou J., Shi M.D., et al. Monocytes from HIV-infected individuals show impaired cholesterol efflux and increased foam cell formation after transendothelial migration. AIDS 2015, 29:1445-1457.
87. Jones A.G., Hattersley A.T. The clinical utility of C-peptide measurement in the care of patients with diabetes. Diabet. Med.: J. Br. Diabet. Assoc. 2013, 30:803-817.
88. Limone P., Biglino A., Valle M., Degioanni M., Paola Servato M., Berardi C., et al. Insulin resistance in HIV-infected patients: relationship with pro-inflammatory cytokines released by peripheral leukocytes. J. Infect. 2003, 47:52-58.
89. Palmer C.S., Anzinger J.J., Zhou J., Gouillou M., Landay A., Jaworowski A., et al. Glucose transporter 1-expressing proinflammatory monocytes are elevated in combination antiretroviral therapy-treated and untreated HIV+ subjects. J. Immunol. 2014, 193:5595-5603.
90. Brabers N.A., Nottet H.S. Role of the pro-inflammatory cytokines TNF-alpha and IL-1beta in HIV-associated dementia. Eur. J. Clin. Invest. 2006, 36:447-458.
91. Pais T.F., Figueiredo C., Peixoto R., Braz M.H., Chatterjee S. Necrotic neurons enhance microglial neurotoxicity through induction of glutaminase by a MyD88-dependent pathway. J. Neuroinflam. 2008, 5:43.
92. Williams R., Yao H., Peng F., Yang Y., Bethel-Brown C., Buch S. Cooperative induction of CXCL10 involves NADPH oxidase: Implications for HIV dementia. Glia 2010, 58:611-621.
93. Palios J., Kadoglou N.P., Lampropoulos S. The pathophysiology of HIV-/HAART-related metabolic syndrome leading to cardiovascular disorders: the emerging role of adipokines. Exp. Diabetes Res. 2012, 2012:103063.
94. Paula A.A., Falcao M.C., Pacheco A.G. Metabolic syndrome in HIV-infected individuals: underlying mechanisms and epidemiological aspects. AIDS Res. Ther. 2013, 10:32.
95. Hurwitz B.E., Klimas N.G., Llabre M.M., Maher K.J., Skyler J.S., Bilsker M.S., et al. HIV, metabolic syndrome X, inflammation, oxidative stress, and coronary heart disease risk: role of protease inhibitor exposure. Cardiovasc. Toxicol. 2004, 4:303-316.
96. Lagathu C., Eustace B., Prot M., Frantz D., Gu Y., Bastard J.P., et al. Some HIV antiretrovirals increase oxidative stress and alter chemokine, cytokine or adiponectin production in human adipocytes and macrophages. Antivir. Ther. 2007, 12:489-500.
97. Bastard J.P., Fellahi S., Couffignal C., Raffi F., Gras G., Hardel L., et al. Increased systemic immune activation and inflammatory profile of long-term HIV-infected ART-controlled patients is related to personal factors, but not to markers of HIV infection severity. J. Antimicrob. Chemother. 2015, 70:1816-1824.
98. Deeks S.G. HIV infection, inflammation, immunosenescence, and aging. Ann. Rev. Med. 2011, 62:141-155.
99. Langkilde A., Petersen J., Henriksen J.H., Jensen F.K., Gerstoft J., Eugen-Olsen J., et al. Leptin, IL-6, and suPAR reflect distinct inflammatory changes associated with adiposity, lipodystrophy and low muscle mass in HIV-infected patients and controls. Immun. Ageing: I & A 2015, 12:9.
100. Tenorio A.R., Zheng Y., Bosch R.J., Krishnan S., Rodriguez B., Hunt P.W., et al. Soluble markers of inflammation and coagulation but not T-cell activation predict non-AIDS-defining morbid events during suppressive antiretroviral treatment. J. Infect. Dis. 2014, 210:1248-1259.