Abstract
During the past decade, our laboratory has carried out a series of studies analyzing the effects of autonomic nervous system (ANS) activity on HIV- 1 pathogenesis (Cole et al., 1998). These studies were motivated by natural history studies showing accelerated HIV disease progression in gay men who had socially inhibited personality characteristics (Cole et al., 1996, 2003). Previous developmental studies have suggested that socially inhibited individuals show elevated levels of ANS activity (Block, 1957; Buck et al., 1974; Cole et al., 1999b; Miller et al., 1999), providing a potential neurobiological basis for differential HIV disease progression. In a subsequent cohort study of 54 HIV-positive gay men with early- to mid-stage infection (no AIDS, and CD4+ T cell levels > 200/mm3), we found that socially inhibited individuals did indeed show elevated levels of ANS activity. ANS activity was measured across a range of end-organ responses including palmar skin conductance, blood pressure, heart rate interbeat interval, finger pulse amplitude, and peripheral pulse transit time (time from heart beat to subsequent finger pulse peak) (Fig. 9.1). Baseline autonomic activity and reactivity to a series of physical, psychological, and social stimuli was found to be stable over time. Individuals showing constitutively high levels of ANS activity also showed elevated plasma viral load (Fig. 9.1) and impaired suppression of viremia and CD4+ T-lymphocyte recovery after the onset of combination antiretroviral therapy (Cole et al., 2001, 2003).
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References
Agy, M.B., Acker, R.L., Sherbert, C.H., and Katze, M.G. (1995). Interferon treatment inhibits virus replication in HIV-1-and SIV-infected CD4+ T-cell lines by distinct mechanisms: Evidence for decreased stability and aberrant processing of HIV-1 proteins. Virology 214(2):379–386.
Antoni, M.H. (2003). Stress management effects on psychological, endocrinological, and immune functioning in men with HIV infection: Empirical support for a psychoneuroimmunological model. Stress 6(3):173–188.
Baca-Regen, L., Heinzinger, N., Stevenson, M., and Gendelman, H.E. (1994). Alpha interferon-induced antiretroviral activities: restriction of viral nucleic acid synthesis and progeny virion production in human immunodeficiency virus type 1-infected monocytes. J. Virol. 68(11):7559–7565.
Badou, A., Bennasser, Y., Moreau, M., Leclerc, C., Benkirane, M., and Bahraoui, E. (2000). Tat protein of human immunodeficiency virus type 1 induces interleukin-10 in human peripheral blood monocytes: Implication of protein kinase C-dependent pathway. J. Virol. 74(22):10551–10562.
Bleul, C.C., Farzan, M., Choe, H., Parolin, C., Clark-Lewis, I., Sodroski, J., and Springer, T.A. (1996). The lymphocyte chemoattractant SDF-1 is a ligand for LESTR/fusin and blocks HIV-1 entry. Nature 382(6594):829–833.
Block, J. (1957). A study of affective responsiveness in a lie-detection situation. J. Abnorm. Psychol. 55(1):11–15.
Buck, R., Miller, R.E., and Caul, W.F. (1974). Sex, personality, and physiological variables in the communication of affect via facial expression. J. Pers. Soc. Psychol. 30(4):587–596.
Capitanio, J.P., Mendoza, S.P., Lerche, N.W., and Mason, W.A. (1998). Social stress results in altered glucocorticoid regulation and shorter survival in simian acquired immune deficiency syndrome. Proc. Natl. Acad. Sci. U.S.A. 95(8):4714–4719.
Castrillon, P.O., Cardinali, D.P., Arce, A., Cutrera, R.A., and Esquifino, A.I. (2000). Interferon-gamma release in sympathetically denervated rat submaxillary lymph nodes. Neuroimmunomodulation 8(4):197–202.
Chun, T.W., Davey, R.T., Jr., Ostrowski, M., Shawn Justement, J., Engel, D., Mullins, J.I., and Fauci, A.S. (2000). Relationship between pre-existing viral reservoirs and the re-emergence of plasma viremia after discontinuation of highly active anti-retroviral therapy. Nat. Med. 6(7):757–761.
Cole, S.W., and Kemeny, M.E. (1997). Psychobiology of HIV infection. Crit. Rev. Neurobiol. 11(4):289–321.
Cole, S., and Kemeny, M.E. (2001). Psychosocial Influences on the Progression of HIV Infection. In R. Ader, D.L. Felten, and N. Cohen (eds.), Psychoneuroimmunology, 3rd ed.,Vol. 2. San Diego: Academic Press. 538–612.
Cole, S.W., Kemeny, M.E., Taylor, S.E., Visscher, B.R., and Fahey, J.L. (1996). Accelerated course of human immunodeficiency virus infection in gay men who conceal their homosexual identity. Psychosom. Med. 58(3):219–231.
Cole, S.W., Kemeny, M.E., and Taylor, S.E. (1997). Social identity and physical health: accelerated HIV progression in rejection-sensitive gay men. J. Pers. Soc. Psychol. 72(2):320–335.
Cole, S.W., Korin, Y.D., Fahey, J.L., and Zack, J.A. (1998). Norepinephrine accelerates HIV replication via protein kinase A-dependent effects on cytokine production. J. Immunol. 161(2):610–616.
Cole, S.W., Jamieson, B.D., and Zack, J.A. (1999a). cAMP up-regulates cell surface expression of lymphocyte CXCR4: implications for chemotaxis and HIV-1 infection. J. Immunol. 162(3):1392–1400.
Cole, S.W., Kemeny, M.E., Weitzman, O.B., Schoen, M., and Anton, P.A. (1999b). Socially inhibited individuals show heightened DTH response during intense social engagement. Brain Behav. Immun. 13(2):187–200.
Cole, S.W., Naliboff, B.D., Kemeny, M.E., Griswold, M.P., Fahey, J.L., and Zack, J.A. (2001). Impaired response to HAART in HIV-infected individuals with high autonomic nervous system activity. Proc. Natl. Acad. Sci. U.S.A. 98(22):12695–12700.
Cole, S.W., Kemeny, M.E., Fahey, J.L., Zack, J.A., and Naliboff, B.D. (2003). Psychological risk factors for HIV pathogenesis: mediation by the autonomic nervous system. Biol. Psychiatry 54(12):1444–1456.
Davey, R.T., Jr., Bhat, N., Yoder, C., Chun, T.W., Metcalf, J.A., Dewar, R., Natarajan, V., Lempicki, R.A., Adelsberger, J.W., Miller, K.D., Kovacs, J.A., Polis, M.A., Walker, R.E., Falloon, J., Masur, H., Gee, D., Baseler, M., Dimitrov, D.S., Fauci, A.S., and Lane, H.C. (1999). HIV-1 and T cell dynamics after interruption of highly active antiretroviral therapy (HAART) in patients with a history of sustained viral suppression. Proc. Natl. Acad. Sci. U.S.A. 96(26):15109–15114.
Downing, J.E., and Miyan, J.A. (2000). Neural immunoregulation: emerging roles for nerves in immune homeostasis and disease. Immunol. Today 21(6):281–289.
Embretson, J., Zupancic, M., Ribas, J.L., Burke, A., Racz, P., Tenner-Racz, K., and Haase, A.T. (1993). Massive covert infection of helper T lymphocytes and macrophages by HIV during the incubation period of AIDS. Nature 362(6418): 359–362.
Felten, S.Y., and Olschowka, J. (1987). Noradrenergic sympathetic innervation of the spleen: II. Tyrosine hydroxylase (TH)-positive nerve terminals form synaptic-like contacts on lymphocytes in the splenic white pulp. J. Neurosci. Res. 18(1): 37–48.
Felten, D.L., Livnat, S., Felten, S.Y., Carlson, S.L., Bellinger, D.L., and Yeh, P. (1984). Sympathetic innervation of lymph nodes in mice. Brain Res. Bull. 13(6):693–699.
Felten, D.L., Felten, S.Y., Bellinger, D.L., Carlson, S.L., Ackerman, K.D., Madden, K.S., Olschowki, J.A., and Livnat, S. (1987). Noradrenergic sympathetic neural interactions with the immune system: Structure and function. Immunol. Rev. 100: 225–260.
Fink, T., and Weihe, E. (1988). Multiple neuropeptides in nerves supplying mammalian lymph nodes: messenger candidates for sensory and autonomic neuroimmunomodulation? Neurosci. Lett. 90(1–2):39–44.
Finnegan, A., Roebuck, K.A., Nakai, B.E., Gu, D.S., Rabbi, M.F., Song, S., and Landay, A.L. (1996). IL-10 cooperates with TNF-alpha to activate HIV-1 from latently and acutely infected cells of monocyte/macrophage lineage. J. Immunol. 156(2):841–851.
Finzi, D., Hermankova, M., Pierson, T., Carruth, L.M., Buck, C., Chaisson, R.E., Quinn, T.C., Chadwick, K., Margolick, J., Brookmeyer, R., Gallant, J., Markowitz, M., Ho, D.D., Richman, D.D., and Siliciano, R.F. (1997). Identification of a reservoir for HIV-1 in patients on highly active antiretroviral therapy. Science 278(5341):1295–1300.
Jamieson, B.D., and Zack, J.A. (1998). In vivo pathogenesis of a human immunodeficiency virus type 1 reporter virus. J. Virol. 72(8):6520–6526.
Kelley, S.P., Moynihan, J.A., Stevens, S.Y., Grota, L.J., and Felten, D.L. (2003). Sympathetic nerve destruction in spleen in murine AIDS. Brain Behav. Immun. 17(2): 94–109.
Korth, M.J., Taylor, M.D., and Katze, M.G. (1998). Interferon inhibits the replication of HIV-1, SIV, and SHIV chimeric viruses by distinct mechanisms. Virology 247(2):265–273.
Madden, K.S., Felten, S.Y., Felten, D.L., and Bellinger, D.L. (1995a). Sympathetic nervous system—immune system interactions in young and old Fischer 344 rats. Ann. N.Y. Acad. Sci. 771:523–534.
Madden, K.S., Sanders, V.M., and Felten, D.L. (1995b). Catecholamine influences and sympathetic neural modulation of immune responsiveness. Annu. Rev. Pharmacol. Toxicol. 35:417–448.
Miller, G.E., Cohen, S., Rabin, B.S., Skoner, D.P., and Doyle, W.J. (1999). Personality and tonic cardiovascular, neuroendocrine, and immune parameters. Brain Behav. Immun. 13(2):109–123.
Miller, L.E., Justen, H.P., Scholmerich, J., and Straub, R.H. (2000). The loss of sympathetic nerve fibers in the synovial tissue of patients with rheumatoid arthritis is accompanied by increased norepinephrine release from synovial macrophages. FASEB J. 14(13):2097–2107.
Oberlin, E., Amara, A., Bachelerie, F., Bessia, C., Virelizier, J.L., Arenzana-Seisdedos, F., Schwartz, O., Heard, J.M., Clark-Lewis, I., Legler, D.F., Loetscher, M., Baggiolini, M., and Moser, B. (1996). The CXC chemokine SDF-1 is the ligand for LESTR/fusin and prevents infection by T-cell-line-adapted HIV-1. Nature 382(6594):833–835.
Panel on Clinical Practices for Treatment of HIV Infection. (2004). Guidelines for the Use of Antiretroviral Agents in HIV-1 Infected Adults and Adolescents. Washington, DC: U.S. Department of Health and Human Services, p. 115.
Pantaleo, G., Graziosi, C., Demarest, J.F., Butini, L., Montroni, M., Fox, C.H., Orenstein, J.M., Kotler, D.P., and Fauci, A.S. (1993). HIV infection is active and progressive in lymphoid tissue during the clinically latent stage of disease. Nature 362(6418):355–358.
Pitha, P.M. (1994). Multiple effects of interferon on the replication of human immunodeficiency virus type 1. Antiviral Res. 24(2–3):205–219.
Ramratnam, B., Mittler, J.E., Zhang, L., Boden, D., Hurley, A., Fang, F., Macken, C.A., Perelson, A.S., Markowitz, M., and Ho, D.D. (2000). The decay of the latent reservoir of replication-competent HIV-1 is inversely correlated with the extent of residual viral replication during prolonged anti-retroviral therapy. Nat. Med. 6(1):82–85.
Sapolsky, R.M. (1998). Why Zebras Don’t Get Ulcers: An Updated Guide To Stress, Stress Related Diseases, and Coping. New York: W.H. Freeman.
Sharkey, M.E., Teo, I., Greenough, T., Sharova, N., Luzuriaga, K., Sullivan, J.L., Bucy, R.P., Kostrikis, L.G., Haase, A., Veryard, C., Davaro, R.E., Cheeseman, S.H., Daly, J.S., Bova, C., Ellison, R.T., 3rd, Mady, B., Lai, K.K., Moyle, G., Nelson, M., Gazzard, B., Shaunak, S., and Stevenson, M. (2000). Persistence of episomal HIV-1 infection intermediates in patients on highly active anti-retroviral therapy. Nat. Med. 6(1):76–81.
Sloan, E.K., Tarara, R.P., Capitanio, J.P., and Cole, S.W. (2006). Enhanced SIV replication adjacent to catechnolaminergic varicosities in primate lymph nodes. Journal of Virology. 80(9):4326–4335.
Stebbing, J., Gazzard, B., and Douek, D.C. (2004). Where does HIV live? N. Engl. J. Med. 350(18):1872–1880.
Weiner, H. (1992). Perturbing the Organism: The Biology of Stressful Experience. Chicago: University of Chicago Press.
Weissman, D., Poli, G., and Fauci, A.S. (1995). IL-10 synergizes with multiple cytokines in enhancing HIV production in cells of monocytic lineage. J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 9(5):442–449.
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Sloan, E.K., Collado-Hidalgo, A., Cole, S.W. (2006). Autonomic Nervous System Influences on HIV Pathogenesis. In: Welsh, C.J., Meagher, M.W., Sternberg, E.M. (eds) Neural and Neuroendocrine Mechanisms in Host Defense and Autoimmunity. Springer, Boston, MA. https://doi.org/10.1007/978-0-387-48334-4_9
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DOI: https://doi.org/10.1007/978-0-387-48334-4_9
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