Aging of the human innate immune system in HIV infection

Current Opinion in Immunology

Volumn 29, Issue 1, 2014, Pages 127-136

  Zapata, Heidi J ^a   Shaw, Albert C ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIRETROVIRUS AGENT; ESTROGEN; TELOMERASE; TESTOSTERONE; TOLL LIKE RECEPTOR;

AGE DISTRIBUTION; AGING; BACTERIAL TRANSLOCATION; CD4+ T LYMPHOCYTE; CELLULAR SECRETION; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; DENDRITIC CELL; DISEASE ASSOCIATION; DISEASE DURATION; DNA DAMAGE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; INNATE IMMUNITY; MONOCYTE; PATTERN RECOGNITION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; REVIEW; IMMUNOLOGY; INFLAMMATION;

AGING; DENDRITIC CELLS; HIV INFECTIONS; HUMANS; IMMUNITY, INNATE; INFLAMMATION; TOLL-LIKE RECEPTORS;

EID: 84903612373     PISSN: 09527915     EISSN: 18790372     Source Type: Journal    
DOI: 10.1016/j.coi.2014.06.007     Document Type: Review

References (109)

1. Samji H., Cescon A., Hogg R.S., Modur S.P., Althoff K.N., Buchacz K., Burchell A.N., Cohen M., Gebo K.A., Gill M.J., et al. Closing the gap: increases in life expectancy among treated HIV-positive individuals in the United States and Canada. PLoS One 2013, 8:e81355.
2. Antiretroviral Therapy Cohort C Life expectancy of individuals on combination antiretroviral therapy in high-income countries: a collaborative analysis of 14 cohort studies. Lancet 2008, 372:293-299.
3. Luther V.P., Wilkin A.M. HIV infection in older adults. Clin Geriatr Med 2007, 23:567-583. vii.
4. High K.P., Brennan-Ing M., Clifford D.B., Cohen M.H., Currier J., Deeks S.G., Deren S., Effros R.B., Gebo K., Goronzy J.J., et al. HIV and aging: state of knowledge and areas of critical need for research. A report to the NIH Office of AIDS Research by the HIV and Aging Working Group. J Acquir Immune Defic Syndr 2012, 60(Suppl. 1):S1-S18.
5. Effros R.B., Fletcher C.V., Gebo K., Halter J.B., Hazzard W.R., Horne F.M., Huebner R.E., Janoff E.N., Justice A.C., Kuritzkes D., et al. Aging and infectious diseases: workshop on HIV infection and aging: what is known and future research directions. Clin Infect Dis 2008, 47:542-553.
6. Keating S.M., Jacobs E.S., Norris P.J. Soluble mediators of inflammation in HIV and their implications for therapeutics and vaccine development. Cytokine Growth Factor Rev 2012, 23:193-206.
7. Armah K.A., McGinnis K., Baker J., Gibert C., Butt A.A., Bryant K.J., Goetz M., Tracy R., Oursler K.K., Rimland D., et al. HIV status, burden of comorbid disease, and biomarkers of inflammation, altered coagulation, and monocyte activation. Clin Infect Dis 2012, 55:126-136.
8. Kuller L.H., Tracy R., Belloso W., De Wit S., Drummond F., Lane H.C., Ledergerber B., Lundgren J., Neuhaus J., Nixon D., et al. Inflammatory and coagulation biomarkers and mortality in patients with HIV infection. PLoS Med 2008, 5:e203.
9. Kamat A., Misra V., Cassol E., Ancuta P., Yan Z., Li C., Morgello S., Gabuzda D. A plasma biomarker signature of immune activation in HIV patients on antiretroviral therapy. PLoS One 2012, 7:e30881.
10. Krishnan S., Wilson E.M., Sheikh V., Rupert A., Mendoza D., Yang J., Lempicki R., Migueles S.A., Sereti I. Evidence for innate immune system activation in HIV type 1-infected elite controllers. J Infect Dis 2014, 209:931-939.
11. Leng S.X., Tian X., Matteini A., Li H., Hughes J., Jain A., Walston J.D., Fedarko N.S. IL-6-independent association of elevated serum neopterin levels with prevalent frailty in community-dwelling older adults. Age Ageing 2011, 40:475-481.
12. Shaw A.C., Goldstein D.R., Montgomery R.R. Age-dependent dysregulation of innate immunity. Nat Rev Immunol 2013, 13:875-887.
13. Salvioli S., Capri M., Valensin S., Tieri P., Monti D., Ottaviani E., Franceschi C. Inflamm-aging, cytokines and aging: state of the art, new hypotheses on the role of mitochondria and new perspectives from systems biology. Curr Pharm Des 2006, 12:3161-3171.
14. Franceschi C., Valensin S., Bonafe M., Paolisso G., Yashin A.I., Monti D., De Benedictis G. The network and the remodeling theories of aging: historical background and new perspectives. Exp Gerontol 2000, 35:879-896.
15. Hearps A.C., Maisa A., Cheng W.J., Angelovich T.A., Lichtfuss G.F., Palmer C.S., Landay A.L., Jaworowski A., Crowe S.M. HIV infection induces age-related changes to monocytes and innate immune activation in young men that persist despite combination antiretroviral therapy. AIDS 2012, 26:843-853.
16. Hearps A.C., Martin G.E., Angelovich T.A., Cheng W.J., Maisa A., Landay A.L., Jaworowski A., Crowe S.M. Aging is associated with chronic innate immune activation and dysregulation of monocyte phenotype and function. Aging Cell 2012, 11:867-875.
17. Seidler S., Zimmermann H.W., Bartneck M., Trautwein C., Tacke F. Age-dependent alterations of monocyte subsets and monocyte-related chemokine pathways in healthy adults. BMC Immunol 2010, 11:30.
18. Nyugen J., Agrawal S., Gollapudi S., Gupta S. Impaired functions of peripheral blood monocyte subpopulations in aged humans. J Clin Immunol 2010, 30:806-813.
19. Martin G.E., Gouillou M., Hearps A.C., Angelovich T.A., Cheng A.C., Lynch F., Cheng W.J., Paukovics G., Palmer C.S., Novak R.M., et al. Age-associated changes in monocyte and innate immune activation markers occur more rapidly in HIV infected women. PLoS One 2013, 8:e55279.
20. van Duin D., Mohanty S., Thomas V., Ginter S., Montgomery R.R., Fikrig E., Allore H.G., Medzhitov R., Shaw A.C. Age-associated defect in human TLR-1/2 function. J Immunol 2007, 178:970-975.
21. van Duin D., Allore H.G., Mohanty S., Ginter S., Newman F.K., Belshe R.B., Medzhitov R., Shaw A.C. Prevaccine determination of the expression of costimulatory B7 molecules in activated monocytes predicts influenza vaccine responses in young and older adults. J Infect Dis 2007, 195:1590-1597.
22. Qian F., Wang X., Zhang L., Chen S., Piecychna M., Allore H., Bockenstedt L., Malawista S., Bucala R., Shaw A.C., et al. Age-associated elevation in TLR5 leads to increased inflammatory responses in the elderly. Aging Cell 2012, 11:104-110.
23. Chang J.J., Lacas A., Lindsay R.J., Doyle E.H., Axten K.L., Pereyra F., Rosenberg E.S., Walker B.D., Allen T.M., Altfeld M. Differential regulation of toll-like receptor pathways in acute and chronic HIV-1 infection. AIDS 2012, 26:533-541.
24. Heggelund L., Muller F., Lien E., Yndestad A., Ueland T., Kristiansen K.I., Espevik T., Aukrust P., Froland S.S. Increased expression of toll-like receptor 2 on monocytes in HIV infection: possible roles in inflammation and viral replication. Clin Infect Dis 2004, 39:264-269.
25. Della Bella S., Bierti L., Presicce P., Arienti R., Valenti M., Saresella M., Vergani C., Villa M.L. Peripheral blood dendritic cells and monocytes are differently regulated in the elderly. Clin Immunol 2007, 122:220-228.
26. Panda A., Qian F., Mohanty S., van Duin D., Newman F.K., Zhang L., Chen S., Towle V., Belshe R.B., Fikrig E., et al. Age-associated decrease in TLR function in primary human dendritic cells predicts influenza vaccine response. J Immunol 2010, 184:2518-2527.
27. Jing Y., Shaheen E., Drake R.R., Chen N., Gravenstein S., Deng Y. Aging is associated with a numerical and functional decline in plasmacytoid dendritic cells, whereas myeloid dendritic cells are relatively unaltered in human peripheral blood. Hum Immunol 2009, 70:777-784.
28. Garbe K., Bratke K., Wagner S., Virchow J.C., Lommatzsch M. Plasmacytoid dendritic cells and their Toll-like receptor 9 expression selectively decrease with age. Hum Immunol 2012, 73:493-497.
29. Canaday D.H., Amponsah N.A., Jones L., Tisch D.J., Hornick T.R., Ramachandra L. Influenza-induced production of interferon-alpha is defective in geriatric individuals. J Clin Immunol 2010, 30:373-383.
30. Sridharan A., Esposo M., Kaushal K., Tay J., Osann K., Agrawal S., Gupta S., Agrawal A. Age-associated impaired plasmacytoid dendritic cell functions lead to decreased CD4 and CD8 T cell immunity. Age (Dordr) 2011, 33:363-376.
31. Agrawal A., Agrawal S., Cao J.N., Su H., Osann K., Gupta S. Altered innate immune functioning of dendritic cells in elderly humans: a role of phosphoinositide 3-kinase-signaling pathway. J Immunol 2007, 178:6912-6922.
32. Agrawal A., Tay J., Ton S., Agrawal S., Gupta S. Increased reactivity of dendritic cells from aged subjects to self-antigen, the human DNA. J Immunol 2009, 182:1138-1145.
33. Qian F., Wang X., Zhang L., Lin A., Zhao H., Fikrig E., Montgomery R.R. Impaired interferon signaling in dendritic cells from older donors infected in vitro with West Nile virus. J Infect Dis 2011, 203:1415-1424.
34. Frleta D., Ochoa C.E., Kramer H.B., Khan S.A., Stacey A.R., Borrow P., Kessler B.M., Haynes B.F., Bhardwaj N. HIV-1 infection-induced apoptotic microparticles inhibit human DCs via CD44. J Clin Invest 2012, 122:4685-4697.
35. Sabado R.L., O'Brien M., Subedi A., Qin L., Hu N., Taylor E., Dibben O., Stacey A., Fellay J., Shianna K.V., et al. Evidence of dysregulation of dendritic cells in primary HIV infection. Blood 2010, 116:3839-3852.
36. Huang J., Yang Y., Al-Mozaini M., Burke P.S., Beamon J., Carrington M.F., Seiss K., Rychert J., Rosenberg E.S., Lichterfeld M., et al. Dendritic cell dysfunction during primary HIV-1 infection. J Infect Dis 2011, 204:1557-1562.
37. Miller E.A., Spadaccia M.R., O'Brien M.P., Rolnitzky L., Sabado R., Manches O., Frleta D., Bhardwaj N. Plasma factors during chronic HIV-1 infection impair IL-12 secretion by myeloid dendritic cells via a virus-independent pathway. J Acquir Immune Defic Syndr 2012, 61:535-544.
38. Buisson S., Benlahrech A., Gazzard B., Gotch F., Kelleher P., Patterson S. Monocyte-derived dendritic cells from HIV type 1-infected individuals show reduced ability to stimulate T cells and have altered production of interleukin (IL)-12 and IL-10. J Infect Dis 2009, 199:1862-1871.
39. Fan Z., Huang X.L., Kalinski P., Young S., Rinaldo C.R. Dendritic cell function during chronic hepatitis C virus and human immunodeficiency virus type 1 infection. Clin Vaccine Immunol 2007, 14:1127-1137.
40. Blanchet F.P., Moris A., Nikolic D.S., Lehmann M., Cardinaud S., Stalder R., Garcia E., Dinkins C., Leuba F., Wu L., et al. Human immunodeficiency virus-1 inhibition of immunoamphisomes in dendritic cells impairs early innate and adaptive immune responses. Immunity 2010, 32:654-669.
41. Lehmann C., Jung N., Forster K., Koch N., Leifeld L., Fischer J., Mauss S., Drebber U., Steffen H.M., Romerio F., et al. Longitudinal analysis of distribution and function of plasmacytoid dendritic cells in peripheral blood and gut mucosa of HIV infected patients. J Infect Dis 2014, 209:940-949.
42. Lehmann C., Lafferty M., Garzino-Demo A., Jung N., Hartmann P., Fatkenheuer G., Wolf J.S., van Lunzen J., Romerio F. Plasmacytoid dendritic cells accumulate and secrete interferon alpha in lymph nodes of HIV-1 patients. PLoS One 2010, 5:e11110.
43. Shodell M., Siegal F.P. Circulating, interferon-producing plasmacytoid dendritic cells decline during human ageing. Scand J Immunol 2002, 56:518-521.
44. Kamga I., Kahi S., Develioglu L., Lichtner M., Maranon C., Deveau C., Meyer L., Goujard C., Lebon P., Sinet M., et al. Type I interferon production is profoundly and transiently impaired in primary HIV-1 infection. J Infect Dis 2005, 192:303-310.
45. Tilton J.C., Manion M.M., Luskin M.R., Johnson A.J., Patamawenu A.A., Hallahan C.W., Cogliano-Shutta N.A., Mican J.M., Davey R.T., Kottilil S., et al. Human immunodeficiency virus viremia induces plasmacytoid dendritic cell activation in vivo and diminished alpha interferon production in vitro. J Virol 2008, 82:3997-4006.
46. Reitano K.N., Kottilil S., Gille C.M., Zhang X., Yan M., O'Shea M.A., Roby G., Hallahan C.W., Yang J., Lempicki R.A., et al. Defective plasmacytoid dendritic cell-NK cell cross-talk in HIV infection. AIDS Res Hum Retroviruses 2009, 25:1029-1037.
47. Martinelli E., Cicala C., Van Ryk D., Goode D.J., Macleod K., Arthos J., Fauci A.S. HIV-1 gp120 inhibits TLR9-mediated activation and IFN-{alpha} secretion in plasmacytoid dendritic cells. Proc Natl Acad Sci USA 2007, 104:3396-3401.
48. von Sydow M., Sonnerborg A., Gaines H., Strannegard O. Interferon-alpha and tumor necrosis factor-alpha in serum of patients in various stages of HIV-1 infection. AIDS Res Hum Retroviruses 1991, 7:375-380.
49. O'Brien M., Manches O., Sabado R.L., Baranda S.J., Wang Y., Marie I., Rolnitzky L., Markowitz M., Margolis D.M., Levy D., et al. Spatiotemporal trafficking of HIV in human plasmacytoid dendritic cells defines a persistently IFN-alpha-producing and partially matured phenotype. J Clin Invest 2011, 121:1088-1101.
50. Beignon A.S., McKenna K., Skoberne M., Manches O., DaSilva I., Kavanagh D.G., Larsson M., Gorelick R.J., Lifson J.D., Bhardwaj N. Endocytosis of HIV-1 activates plasmacytoid dendritic cells via Toll-like receptor-viral RNA interactions. J Clin Invest 2005, 115:3265-3275.
51. Meier A., Alter G., Frahm N., Sidhu H., Li B., Bagchi A., Teigen N., Streeck H., Stellbrink H.J., Hellman J., et al. MyD88-dependent immune activation mediated by human immunodeficiency virus type 1-encoded Toll-like receptor ligands. J Virol 2007, 81:8180-8191.
52. Heil F., Hemmi H., Hochrein H., Ampenberger F., Kirschning C., Akira S., Lipford G., Wagner H., Bauer S. Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science 2004, 303:1526-1529.
53. Hatano H., Strain M.C., Scherzer R., Bacchetti P., Wentworth D., Hoh R., Martin J.N., McCune J.M., Neaton J.D., Tracy R.P., et al. Increase in 2-long terminal repeat circles and decrease in D-dimer after raltegravir intensification in patients with treated HIV infection: a randomized, placebo-controlled trial. J Infect Dis 2013, 208:1436-1442.
54. Chun T.W., Fauci A.S. Viral persistence in HIV infection: much known, much to learn. J Infect Dis 2013, 208:1356-1358.
55. Mureith M.W., Chang J.J., Lifson J.D., Ndung'u T., Altfeld M. Exposure to HIV-1-encoded Toll-like receptor 8 ligands enhances monocyte response to microbial encoded Toll-like receptor 2/4 ligands. AIDS 2010, 24:1841-1848.
56. Lester R.T., Yao X.D., Ball T.B., McKinnon L.R., Omange W.R., Kaul R., Wachihi C., Jaoko W., Rosenthal K.L., Plummer F.A. HIV-1 RNA dysregulates the natural TLR response to subclinical endotoxemia in Kenyan female sex-workers. PLoS One 2009, 4:e5644.
57. Nazli A., Kafka J.K., Ferreira V.H., Anipindi V., Mueller K., Osborne B.J., Dizzell S., Chauvin S., Mian M.F., Ouellet M., et al. HIV-1 gp120 induces TLR2- and TLR4-mediated innate immune activation in human female genital epithelium. J Immunol 2013, 191:4246-4258.
58. Brenchley J.M., Price D.A., Douek D.C. HIV disease: fallout from a mucosal catastrophe?. Nat Immunol 2006, 7:235-239.
59. Sandler N.G., Douek D.C. Microbial translocation in HIV infection: causes, consequences and treatment opportunities. Nat Rev Microbiol 2012, 10:655-666.
60. Brenchley J.M., Price D.A., Schacker T.W., Asher T.E., Silvestri G., Rao S., Kazzaz Z., Bornstein E., Lambotte O., Altmann D., et al. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 2006, 12:1365-1371.
61. Klatt N.R., Funderburg N.T., Brenchley J.M. Microbial translocation, immune activation, and HIV disease. Trends Microbiol 2013, 21:6-13.
62. Jiang W., Lederman M.M., Hunt P., Sieg S.F., Haley K., Rodriguez B., Landay A., Martin J., Sinclair E., Asher A.I., et al. Plasma levels of bacterial DNA correlate with immune activation and the magnitude of immune restoration in persons with antiretroviral-treated HIV infection. J Infect Dis 2009, 199:1177-1185.
63. Merlini E., Bai F., Bellistri G.M., Tincati C., d'Arminio Monforte A., Marchetti G. Evidence for polymicrobic flora translocating in peripheral blood of HIV-infected patients with poor immune response to antiretroviral therapy. PLoS One 2011, 6:e18580.
64. Ellis C.L., Ma Z.M., Mann S.K., Li C.S., Wu J., Knight T.H., Yotter T., Hayes T.L., Maniar A.H., Troia-Cancio P.V., et al. Molecular characterization of stool microbiota in HIV-infected subjects by panbacterial and order-level 16S ribosomal DNA (rDNA) quantification and correlations with immune activation. J Acquir Immune Defic Syndr 2011, 57:363-370.
65. Dillon S.M., Lee E.J., Kotter C.V., Austin G.L., Dong Z., Hecht D.K., Gianella S., Siewe B., Smith D.M., Landay A.L., et al. An altered intestinal mucosal microbiome in HIV-1 infection is associated with mucosal and systemic immune activation and endotoxemia. Mucosal Immunol 2014, 10.1038/mi.2013.116.
66. Stehle J.R., Leng X., Kitzman D.W., Nicklas B.J., Kritchevsky S.B., High K.P. Lipopolysaccharide-binding protein, a surrogate marker of microbial translocation, is associated with physical function in healthy older adults. J Gerontol A Biol Sci Med Sci 2012, 67:1212-1218.
67. Limaye A.P., Kirby K.A., Rubenfeld G.D., Leisenring W.M., Bulger E.M., Neff M.J., Gibran N.S., Huang M.L., Santo Hayes T.K., Corey L., et al. Cytomegalovirus reactivation in critically ill immunocompetent patients. JAMA 2008, 300:413-422.
68. Stowe R.P., Kozlova E.V., Yetman D.L., Walling D.M., Goodwin J.S., Glaser R. Chronic herpesvirus reactivation occurs in aging. Exp Gerontol 2007, 42:563-570.
69. Roberts E.T., Haan M.N., Dowd J.B., Aiello A.E. Cytomegalovirus antibody levels, inflammation, and mortality among elderly Latinos over 9 years of follow-up. Am J Epidemiol 2010, 172:363-371.
70. Bartlett D.B., Firth C.M., Phillips A.C., Moss P., Baylis D., Syddall H., Sayer A.A., Cooper C., Lord J.M. The age-related increase in low-grade systemic inflammation (Inflammaging) is not driven by cytomegalovirus infection. Aging Cell 2012, 11:912-915.
71. Deayton J.R., Prof Sabin C.A., Johnson M.A., Emery V.C., Wilson P., Griffiths P.D. Importance of cytomegalovirus viraemia in risk of disease progression and death in HIV-infected patients receiving highly active antiretroviral therapy. Lancet 2004, 363:2116-2121.
72. Coppe J.P., Desprez P.Y., Krtolica A., Campisi J. The senescence-associated secretory phenotype: the dark side of tumor suppression. Annu Rev Pathol 2010, 5:99-118.
73. Coppe J.P., Patil C.K., Rodier F., Sun Y., Munoz D.P., Goldstein J., Nelson P.S., Desprez P.Y., Campisi J. Senescence-associated secretory phenotypes reveal cell-nonautonomous functions of oncogenic RAS and the p53 tumor suppressor. PLoS Biol 2008, 6:2853-2868.
74. Jylhava J., Jylha M., Lehtimaki T., Hervonen A., Hurme M. Circulating cell-free DNA is associated with mortality and inflammatory markers in nonagenarians: the Vitality 90+ Study. Exp Gerontol 2012, 47:372-378.
75. Jylhava J., Nevalainen T., Marttila S., Jylha M., Hervonen A., Hurme M. Characterization of the role of distinct plasma cell-free DNA species in age-associated inflammation and frailty. Aging Cell 2013, 12:388-397.
76. Pinti M., Cevenini E., Nasi M., De Biasi S., Salvioli S., Monti D., Benatti S., Gibellini L., Cotichini R., Stazi M.A., et al. Circulating mitochondrial DNA increases with age and is a familiar trait: implications for "inflamm-aging". Eur J Immunol 2014, 44:1552-1562.
77. Iyer S.S., Pulskens W.P., Sadler J.J., Butter L.M., Teske G.J., Ulland T.K., Eisenbarth S.C., Florquin S., Flavell R.A., Leemans J.C., et al. Necrotic cells trigger a sterile inflammatory response through the Nlrp3 inflammasome. Proc Natl Acad Sci USA 2009, 106:20388-20393.
78. Li H., Ambade A., Re F. Cutting edge: necrosis activates the NLRP3 inflammasome. J Immunol 2009, 183:1528-1532.
79. Imaeda A.B., Watanabe A., Sohail M.A., Mahmood S., Mohamadnejad M., Sutterwala F.S., Flavell R.A., Mehal W.Z. Acetaminophen-induced hepatotoxicity in mice is dependent on Tlr9 and the Nalp3 inflammasome. J Clin Invest 2009, 119:305-314.
80. Doitsh G., Galloway N.L., Geng X., Yang Z., Monroe K.M., Zepeda O., Hunt P.W., Hatano H., Sowinski S., Munoz-Arias I., et al. Cell death by pyroptosis drives CD4 T-cell depletion in HIV-1 infection. Nature 2014, 505:509-514.
81. Ray A., Prefontaine K.E., Ray P. Down-modulation of interleukin-6 gene expression by 17 beta-estradiol in the absence of high affinity DNA binding by the estrogen receptor. J Biol Chem 1994, 269:12940-12946.
82. Pottratz S.T., Bellido T., Mocharla H., Crabb D., Manolagas S.C. 17 beta-Estradiol inhibits expression of human interleukin-6 promoter-reporter constructs by a receptor-dependent mechanism. J Clin Invest 1994, 93:944-950.
83. Abu-Taha M., Rius C., Hermenegildo C., Noguera I., Cerda-Nicolas J.M., Issekutz A.C., Jose P.J., Cortijo J., Morcillo E.J., Sanz M.J. Menopause and ovariectomy cause a low grade of systemic inflammation that may be prevented by chronic treatment with low doses of estrogen or losartan. J Immunol 2009, 183:1393-1402.
84. Gordon C.M., LeBoff M.S., Glowacki J. Adrenal and gonadal steroids inhibit IL-6 secretion by human marrow cells. Cytokine 2001, 16:178-186.
85. Maggio M., Basaria S., Ble A., Lauretani F., Bandinelli S., Ceda G.P., Valenti G., Ling S.M., Ferrucci L. Correlation between testosterone and the inflammatory marker soluble interleukin-6 receptor in older men. J Clin Endocrinol Metab 2006, 91:345-347.
86. Yang B.C., Liu C.W., Chen Y.C., Yu C.K. Exogenous dehydroepiandrosterone modified the expression of T helper-related cytokines in NZB/NZW F1 mice. Immunol Invest 1998, 27:291-302.
87. Monroe A.K., Dobs A.S., Palella F.J., Kingsley L.A., Witt M.D., Brown T.T. Morning free and total testosterone in HIV-infected men: implications for the assessment of hypogonadism. AIDS Res Ther 2014, 11:6.
88. Tchkonia T., Morbeck D.E., Von Zglinicki T., Van Deursen J., Lustgarten J., Scrable H., Khosla S., Jensen M.D., Kirkland J.L. Fat tissue, aging, and cellular senescence. Aging Cell 2010, 9:667-684.
89. Morin C.L., Pagliassotti M.J., Windmiller D., Eckel R.H. Adipose tissue-derived tumor necrosis factor-alpha activity is elevated in older rats. J Gerontol A Biol Sci Med Sci 1997, 52:B190-B195.
90. Wu D., Ren Z., Pae M., Guo W., Cui X., Merrill A.H., Meydani S.N. Aging up-regulates expression of inflammatory mediators in mouse adipose tissue. J Immunol 2007, 179:4829-4839.
91. Starr M.E., Evers B.M., Saito H. Age-associated increase in cytokine production during systemic inflammation: adipose tissue as a major source of IL-6. J Gerontol A Biol Sci Med Sci 2009, 64:723-730.
92. Cartier A., Cote M., Lemieux I., Perusse L., Tremblay A., Bouchard C., Despres J.P. Age-related differences in inflammatory markers in men: contribution of visceral adiposity. Metabolism 2009, 58:1452-1458.
93. Stenholm S., Koster A., Alley D.E., Visser M., Maggio M., Harris T.B., Egan J.M., Bandinelli S., Guralnik J.M., Ferrucci L. Adipocytokines and the metabolic syndrome among older persons with and without obesity: the InCHIANTI study. Clin Endocrinol (Oxf) 2010, 73:55-65.
94. Pou K.M., Massaro J.M., Hoffmann U., Vasan R.S., Maurovich-Horvat P., Larson M.G., Keaney J.F., Meigs J.B., Lipinska I., Kathiresan S., et al. Visceral and subcutaneous adipose tissue volumes are cross-sectionally related to markers of inflammation and oxidative stress: the Framingham Heart Study. Circulation 2007, 116:1234-1241.
95. Koethe J.R., Hulgan T., Niswender K. Adipose tissue and immune function: a review of evidence relevant to HIV infection. J Infect Dis 2013, 208:1194-1201.
96. Walker U.A., Bickel M., Lutke Volksbeck S.I., Ketelsen U.P., Schofer H., Setzer B., Venhoff N., Rickerts V., Staszewski S. Evidence of nucleoside analogue reverse transcriptase inhibitor-associated genetic and structural defects of mitochondria in adipose tissue of HIV-infected patients. J Acquir Immune Defic Syndr 2002, 29:117-121.
97. Morse C.G., Voss J.G., Rakocevic G., McLaughlin M., Vinton C.L., Huber C., Hu X., Yang J., Huang da W., Logun C., et al. HIV infection and antiretroviral therapy have divergent effects on mitochondria in adipose tissue. J Infect Dis 2012, 205:1778-1787.
98. Cherry C.L., Gahan M.E., McArthur J.C., Lewin S.R., Hoy J.F., Wesselingh S.L. Exposure to dideoxynucleosides is reflected in lowered mitochondrial DNA in subcutaneous fat. J Acquir Immune Defic Syndr 2002, 30:271-277.
99. Nolan D., Hammond E., Martin A., Taylor L., Herrmann S., McKinnon E., Metcalf C., Latham B., Mallal S. Mitochondrial DNA depletion and morphologic changes in adipocytes associated with nucleoside reverse transcriptase inhibitor therapy. AIDS 2003, 17:1329-1338.
100. Perez-Matute P., Perez-Martinez L., Blanco J.R., Oteo J.A. Role of mitochondria in HIV infection and associated metabolic disorders: focus on nonalcoholic fatty liver disease and lipodystrophy syndrome. Oxid Med Cell Longev 2013, 2013:493413.
101. Payne B.A., Wilson I.J., Hateley C.A., Horvath R., Santibanez-Koref M., Samuels D.C., Price D.A., Chinnery P.F. Mitochondrial aging is accelerated by anti-retroviral therapy through the clonal expansion of mtDNA mutations. Nat Genet 2011, 43:806-810.
102. Bua E., Johnson J., Herbst A., Delong B., McKenzie D., Salamat S., Aiken J.M. Mitochondrial DNA-deletion mutations accumulate intracellularly to detrimental levels in aged human skeletal muscle fibers. Am J Hum Genet 2006, 79:469-480.
103. McComsey G.A., Daar E.S., O'Riordan M., Collier A.C., Kosmiski L., Santana J.L., Fichtenbaum C.J., Fink H., Sax P.E., Libutti D.E., et al. Changes in fat mitochondrial DNA and function in subjects randomized to abacavir-lamivudine or tenofovir DF-emtricitabine with atazanavir-ritonavir or efavirenz: AIDS Clinical Trials Group study A5224s, substudy of A5202. J Infect Dis 2013, 207:604-611.
104. Payne B.A., Hollingsworth K.G., Baxter J., Wilkins E., Lee V., Price D.A., Trenell M., Chinnery P.F. In vivo mitochondrial function in HIV-infected persons treated with contemporary anti-retroviral therapy: a magnetic resonance spectroscopy study. PLoS One 2014, 9:e84678.
105. Peng Y., Mian I.S., Lue N.F. Analysis of telomerase processivity: mechanistic similarity to HIV-1 reverse transcriptase and role in telomere maintenance. Mol Cell 2001, 7:1201-1211.
106. Leeansyah E., Cameron P.U., Solomon A., Tennakoon S., Velayudham P., Gouillou M., Spelman T., Hearps A., Fairley C., Smit de V., et al. Inhibition of telomerase activity by human immunodeficiency virus (HIV) nucleos(t)ide reverse transcriptase inhibitors: a potential factor contributing to HIV-associated accelerated aging. J Infect Dis 2013, 207:1157-1165.
107. Hukezalie K.R., Thumati N.R., Cote H.C., Wong J.M. In vitro and ex vivo inhibition of human telomerase by anti-HIV nucleoside reverse transcriptase inhibitors (NRTIs) but not by non-NRTIs. PLoS One 2012, 7:e47505.
108. Wang X., Singh S., Jung H.Y., Yang G., Jun S., Sastry K.J., Park J.I. HIV-1 Vpr protein inhibits telomerase activity via the EDD-DDB1-VPRBP E3 ligase complex. J Biol Chem 2013, 288:15474-15480.
109. Dock J.N., Effros R.B. Role of CD8 T cell replicative senescence in human aging and in HIV-mediated immunosenescence. Aging Dis 2011, 2:382-397.