Antiviral therapy during primary simian immunodeficiency virus infection fails to prevent acute loss of CD4+ T cells in gut mucosa but enhances their rapid restoration through central memory T cells

Journal of Virology

Volumn 82, Issue 8, 2008, Pages 4016-4027

  Verhoeven, David ^a   Sankaran, Sumathi ^a   Silvey, Melanie ^a   Dandekar, Satya ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIRETROVIRUS AGENT; EMTRICITABINE; GAMMA INTERFERON; INTERLEUKIN 2; TENOFOVIR; ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; MEMBRANE ANTIGEN; VIRUS RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN IMMUNODEFICIENCY VIRUS; INFLAMMATION; INTESTINE LYMPHATIC TISSUE; INTESTINE MUCOSA; LYMPHOCYTE PROLIFERATION; MACACA; MALE; MEMORY T LYMPHOCYTE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; SIMIAN IMMUNODEFICIENCY VIRUS; VIRUS INFECTION; VIRUS LOAD; VIRUS REPLICATION; ANIMAL; BIOSYNTHESIS; BLOOD; FLOW CYTOMETRY; IMMUNOLOGICAL MEMORY; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; MONKEY DISEASE; T LYMPHOCYTE SUBPOPULATION; VIROLOGY;

ANIMALIA; HUMAN IMMUNODEFICIENCY VIRUS; MACACA; SIMIAN IMMUNODEFICIENCY VIRUS;

ANIMALS; ANTI-HIV AGENTS; ANTIGENS, SURFACE; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; FLOW CYTOMETRY; IMMUNE TOLERANCE; IMMUNOLOGIC MEMORY; INTERFERON TYPE II; INTERLEUKIN-2; INTESTINAL MUCOSA; MACACA MULATTA; MALE; RNA, VIRAL; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; T-LYMPHOCYTE SUBSETS; VIRAL LOAD;

EID: 41949101136     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02164-07     Document Type: Article

References (73)

1. Abel, K., D. M. Rocke, B. Chohan, L. Fritts, and C. J. Miller. 2005. Temporal and anatomic relationship between virus replication and cytokine gene expression after vaginal simian immunodeficiency virus infection. J. Virol. 79:12164-12172.
2. Agace, W. W., A. I. Roberts, L. Wu, C. Greineder, E. C. Ebert, and C. M. Parker. 2000. Human intestinal lamina propria and intraepithelial lymphocytes express receptors specific for chemokines induced by inflammation. Eur. J. Immunol. 30:819-826.
3. + lymphocyte IL-2 expression is associated with early treatment with highly active antiretroviral therapy. Clin. Immunol. 121:191-197.
4. + T cells are predominantly distributed among six phenotypically and functionally distinct subsets. J. Immunol. 175:5765-5773.
5. Betts, M. R., B. Exley, D. A. Price, A. Bansal, Z. T. Camacho, V. Teaberry, S. M. West, D. R. Ambrozak, G. Tomaras, M. Roederer, J. M. Kilby, J. Tartaglia, R. Belshe, F. Gao, D. C. Douek, K. J. Weinhold, R. A. Koup, P. Goepfert, and G. Ferrari. 2005. Characterization of functional and phenotypic changes in anti-Gag vaccine-induced T cell responses and their role in protection after HIV-1 infection. Proc. Natl. Acad. Sci. USA 102:4512-4517.
6. + T cells. Blood 107:4781-4789.
7. Biancotto, A., J. C. Grivel, S. J. Iglehart, C. Vanpouille, A. Lisco, S. F. Sieg, R. Debernardo, K. Garate, B. Rodriguez, L. B. Margolis, and M. M. Lederman. 2007. Abnormal activation and cytokine spectra in lymph nodes of people chronically infected with HIV-1. Blood 109:4272-4279.
8. Bostik, P., E. S. Noble, A. E. Mayne, L. Gargano, F. Villinger, and A. A. Ansari. 2006. Central memory CD4 T cells are the predominant cell subset resistant to anergy in SIV disease resistant sooty mangabeys. AIDS 20:181-188.
9. + T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J. Exp. Med. 200:749-759.
10. Campbell, J. J., K. E. Murphy, E. J. Kunkel, C. E. Brightling, D. Soler, Z. Shen, J. Boisvert, H. B. Greenberg, M. A. Vierra, S. B. Goodman, M. C. Genovese, A. J. Wardlaw, E. C. Butcher, and L. Wu. 2001. CCR7 expression and memory T cell diversity in humans. J. Immunol. 166:877-884.
11. Centlivre, M., M. Sala, S. Wain-Hobson, and B. Berkhout. 2007. In HIV-1 pathogenesis the die is cast during primary infection. AIDS 21:1-11.
12. Dandekar, S. 2007. Pathogenesis of HIV in the gastrointestinal tract. Curr. HIV Res. AIDS Rep. 4:10-15.
13. Durier, C., C. Capitant, A. S. Lascaux, C. Goujard, E. Oksenhendler, I. Poizot-Martin, J. P. Viard, L. Weiss, E. Netzer, J. F. Delfraissy, J. P. Aboulker, and Y. Levy. 2007. Long-term effects of intermittent interleukin-2 therapy in chronic HIV-infected patients (ANRS 048-079 trials). AIDS 21: 1887-1897.
14. Fritsch, R. D., X. Shen, G. P. Sims, K. S. Hathcock, R. J. Hodes, and P. E. Lipsky. 2005. Stepwise differentiation of CD4 memory T cells defined by expression of CCR7 and CD27. J. Immunol. 175:6489-6497.
15. + T cells with reduced apoptotic susceptibility in rhesus macaques that control virus replication after challenge with pathogenic SIVmac239. J. Immunol. 179:4732-4740.
16. + T-cell restoration and enhanced gene expression regulating mucosal repair and regeneration. J. Virol. 79:2709-2719.
17. George, M. D., S. Sankaran, E. Reay, A. C. Gelli, and S. Dandekar. 2003. High-throughput gene expression profiling indicates dysregulation of intestinal cell cycle mediators and growth factors during primary simian immunodeficiency virus infection. Virology 312:84-94.
18. George, M. D., D. Verhoeven, Z. McBride, and S. Dandekar. 2006. Gene expression profiling of gut mucosa and mesenteric lymph nodes in simian immunodeficiency virus-infected macaques with divergent disease course. J. Med. Primatol. 35:261-269.
19. + T cell recovery during suppressive antiretroviral therapy: association of immune activation, T cell maturation markers, and cellular HIV-1 DNA. J. Infect. Dis. 194:29-37.
20. + T cells in AIDS-free simian immunodeficiency virus-infected sooty mangabeys. J. Immunol. 179:3026-3034.
21. + T-cell depletion in gut lymphoid tissue during primary human immunodeficiency virus type 1 infection and substantial delay in restoration following highly active antiretroviral therapy. J. Virol. 77:11708-11717.
22. Guadalupe, M., S. Sankaran, M. D. George, E. Reay, D. Verhoeven, B. L. Shacklett, J. Flamm, J. Wegelin, T. Prindiville, and S. Dandekar. 2006. Viral suppression and immune restoration in the gastrointestinal mucosa of human immunodeficiency virus type 1-infected patients initiating therapy during primary or chronic infection. J. Virol. 80:8236-8247.
23. Harari, A., V. Dutoit, C. Cellerai, P. A. Bart, R. A. Du Pasquier, and G. Pantaleo. 2006. Functional signatures of protective antiviral T-cell immunity in human virus infections. Immunol. Rev. 211:236-254.
24. Hirsch, V. M., and J. D. Lifson. 2000. Simian immunodeficiency virus infection of monkeys as a model system for the study of AIDS pathogenesis, treatment, and prevention. Adv. Pharmacol. 49:437-477.
25. Hofmann-Lehmann, R., R. K. Swenerton, V. Liska, C. M. Leutenegger, H. Lutz, H. M. McClure, and R. M. Ruprecht. 2000. Sensitive and robust one-tube real-time reverse transcriptase-polymerase chain reaction to quantify SIV RNA load: comparison of one- versus two-enzyme systems. AIDS Res. Hum. Retrovir. 16:1247-1257.
26. Kannanganat, S., C. Ibegbu, L. Chennareddi, H. L. Robinson, and R. R. Amara. 2007. Multiple-cytokine-producing antiviral CD4 T cells are functionally superior to single-cytokine-producing cells. J. Virol. 81:8468-8476.
27. + T cells and this effect overrides its ability to stimulate virus expression. Proc. Natl. Acad. Sci. USA 92:10985-10989.
28. + T cells during peripheral differentiation. Eur. J. Immunol. 34:3370-3378.
29. Lanzavecchia, A., and F. Sallusto. 2000. Dynamics of T lymphocyte responses: intermediates, effectors, and memory cells. Science 290:92-97.
30. Lanzavecchia, A., and F. Sallusto. 2005. Understanding the generation and function of memory T cell subsets. Curr. Opin. Immunol. 17:219-229.
31. + cells in HIV-infected and uninfected individuals. J. Immunol. 177:5145-5154.
32. + central memory T cells and survival in vaccinated SIV-challenged monkeys. Science 312:1530-1533.
33. Letvin, N. L., S. S. Rao, V. Dang, A. P. Buzby, B. Korioth-Schmitz, D. Dombagoda, J. G. Parvani, R. H. Clarke, L. Bar, K. R. Carlson, P. A. Kozlowski, V. M. Hirsch, J. R. Mascola, and G. J. Nabel. 2007. No evidence for consistent virus-specific immunity in simian immunodeficiency virus-exposed, uninfected rhesus monkeys. J. Virol. 81:12368-12374.
34. Leutenegger, C. M., J. Higgins, T. B. Matthews, A. F. Tarantal, P. A. Luciw, N. C. Pedersen, and T. W. North. 2001. Real-time TaqMan PCR as a specific and more sensitive alternative to the branched-chain DNA assay for quantitation of simian immunodeficiency virus RNA. AIDS Res. Hum. Retrovir. 17:243-251.
35. + T cells. Nature 434:1148-1152.
36. + T cells in gut-associated lymphoid tissues in SIVmac239-infected rhesus macaques, but not resistance to rechallenge. J. Med. Primatol. 32:201-210.
37. Lifson, J. D., J. L. Rossio, R. Arnaout, L. Li, T. L. Parks, D. K. Schneider, R. F. Kiser, V. J. Coalter, G. Walsh, R. J. Imming, B. Fisher, B. M. Flynn, N. Bischofberger, M. Piatak, Jr., V. M. Hirsch, M. A. Nowak, and D. Wodarz. 2000. Containment of simian immunodeficiency virus infection: cellular immune responses and protection from rechallenge following transient postinoculation antiretroviral treatment. J. Virol. 74:2584-2593.
38. Ling, B., R. S. Veazey, M. Hart, A. A. Lackner, M. Kuroda, B. Pahar, and P. A. Marx. 2007. Early restoration of mucosal CD4 memory CCR5 T cells in the gut of SIV-infected rhesus predicts long term non-progression. AIDS 21:2377-2385.
39. Martinez-Marino, B., S. Shiboski, F. M. Hecht, J. O. Kahn, and J. A. Levy. 2004. Interleukin-2 therapy restores CD8 cell non-cytotoxic anti-HIV responses in primary infection subjects receiving HAART. AIDS 18:1991-1999.
40. Marzo, A. L., H. Yaquita, and L. Lefrançois. 2007. Cutting edge: migration to nonlymphoid tissues results in functional conversion of central to effector memory CD8 T cells. J. Immunol. 179:36-40.
41. + T cells in multiple tissues during acute SIV infection. Nature 434:1093-1097.
42. Mattapallil, J. J., D. C. Douek, A. Buckler-White, D. Montefiori, N. L. Letvin, G. J. Nabel, and M. Roederer. 2006. Vaccination preserves CD4 memory T cells during acute simian immunodeficiency virus challenge. J. Exp. Med. 203:1533-1541.
43. + T helper cells repopulate the intestine early following antiretroviral therapy of simian immunodeficiency virus-infected rhesus macaques but exhibit a decreased potential to produce interleukin-2. J. Virol. 73:6661-6669.
44. McGowan, I., J. Elliott, M. Fuerst, P. Taing, J. Boscardin, M. Poles, and P. Anton. 2004. Increased HIV-1 mucosal replication is associated with generalized mucosal cytokine activation. J. Acquir. Immune Defic. Syndr. 37: 1228-1236.
45. Mehandru, S., and S. Dandekar. 2008. Role of the gastrointestinal tract in establishing infection in primates and humans. Curr. Opin. HIV AIDS 3:22-27.
46. Mehandru, S., M. A. Poles, K. Tenner-Racz, P. Jean-Pierre, V. Manuelli, P. Lopez, A. Shet, A. Low, H. Mohri, D. Boden, P. Racz, and M. Markowitz. 2006. Lack of mucosal immune reconstitution during prolonged treatment of acute and early HIV-1 infection. PLoS Med. 3:e484.
47. Mehandru, S., M. A. Poles, K. Tenner-Racz, V. Manuelli, P. Jean-Pierre, P. Lopez, A. Shet, A. Low, H. Mohri, D. Boden, P. Racz, and M. Markowitz. 2007. Mechanisms of gastrointestinal CD4+ T cell depletion during acute and early HIV-1 infection. J. Virol. 81:599-612.
48. + T cell dynamics during primary simian immunodeficiency virus infection in macaques: relationship of effector cell differentiation with the extent of viral replication. J. Immunol. 174:6898-6908.
49. Nicholson, J. K., S. W. Browning, R. L. Hengel, E. Lew, L. E. Gallagher, D. Rimland, and J. S. MeDougal. 2001. CCR5 and CXCR4 expression on memory and naive T cells in HIV-1 infection and response to highly active antiretroviral therapy. J. Acquir. Immune Defic. Syndr. 27:105-115.
50. Nilsson, J., S. Kinloch-de-Loes, A. Granath, A. Sönnerborg, L. E. Goh, and J. Andersson. 2007. Early immune activation in gut-associated and peripheral lymphoid tissue during acute HIV infection. AIDS 21:5.
51. Nowak, M. A., A. L. Lloyd, G. M. Vasquez, T. A. Wiltrout, L. M. Wahl, N. Bischofberger, J. Williams, A. Kinter, A. S. Fauci, V. M. Hirsch, and J. D. Lifson. 1997. Viral dynamics of primary viremia and antiretroviral therapy in simian immunodeficiency virus infection. J. Virol. 71:7518-7525.
52. + effector memory insufficiency and overt disease in chronic SIV infection. J. Exp. Med. 204: 2171-2185.
53. + T cells is not predictive of simian immunodeficiency virus virulence. J. Immunol. 179:3035-3046.
54. Peretz, Y., M. L. Ndongala, S. Boulet, M. R. Boulassel, D. Rouleau, P. Cote, D. Longpre, J. P. Routy, J. Falutz, C. Tremblay, C. M. Tsoukas, R. P. Sekaly, and N. F. Bernard. 2007. Functional T cell subsets contribute differentially to HIV peptide-specific responses within infected individuals: correlation of these functional T cell subsets with markers of disease progression. Clin. Immunol. 124:57-68.
55. Picker, L. 2006. Immunopathogenesis of acute AIDS virus infection. Curr. Opin. Immunol. 18:399-405.
56. Picker, L. J., E. F. Reed-Inderbitzin, S. I. Hagen, J. B. Edgar, S. G. Hansen, A. Legasse, S. Planer, M. Piatak, Jr., J. D. Lifson, V. C. Maino, M. K. Axthelm, and F. Villinger. 2006. IL-15 induces CD4 effector memory T cell production and tissue emigration in nonhuman primates. J. Clin. Investig. 116:1514-1524.
57. Pitcher, C. J., S. I. Hagen, J. M. Walker, R. Lum, B. L. Mitchell, V. C. Maino, M, K. Axthelm, and L. J. Picker. 2002. Development and homeostasis of T cell memory in rhesus macaque. J. Immunol. 168:29-43.
58. Poonia, B., S. Nelson, G. J. Bagby, and R. S. Veazey. 2006. Intestinal lymphocyte subsets and turnover are affected by chronic alcohol consumption: implications for SIV/HIV infection. J. Acquir. Immune Defic. Syndr. 41:537-547.
59. Poonia, B., L. Walter, J. Dufour, R. Harrison, P. A. Marx, and R. S. Veazey. 2006. Cyclic changes in the vaginal epithelium of normal rhesus macaques. J. Endocrinol. 190:829-835.
60. + T cell responses. J. Exp. Med. 204:1405-1416.
61. Sankaran, S., M. Guadalupe, E. Reay, M. D. George, J. Flamm, T. Prindiville, and S. Dandekar. 2005. Gut mucosal T cell responses and gene expression correlate with protection against disease in long-term HIV-1-infected nonprogressors. Proc. Natl. Acad. Sci. USA 102:9860-9865.
62. Schaefer, T. M., C. L. Fuller, S. Basu, B. A. Fallert, S. L. Poveda, S. K. Sanghavi, Y. K. Choi, D. E. Kirschner, E. Feingold, and T. A. Reinhart. 2000. Increased expression of interferon-inducible genes in macaque lung tissues during simian immunodeficiency virus infection. Microbes Infect. 8:1839-1850.
63. + T cells to gut-associated lymphoid tissue during chronic infection. J. Virol. 77:5621-5631.
64. Shkoda, A., P. A. Ruiz, H. Daniel, S. C. Kim, G. Rogler, R. B. Sartor, and D. Haller. 2007. Interleukin-10 blocked endoplasmic reticulum stress in intestinal epithelial cells: impact on chronic inflammation. Gastroenterology 132: 190-207.
65. Smith, M. S., L. Foresman, G. J. Lopez, J. Tsay, D. Wodara, J. D. Lifson, A. Page, C. Wang, Z. Li, I. Adany, S. Buch, N. Bischofberger, and O. Narayan. 2000. Lasting effects of transient postinoculation tenofovir [9-R-(2-Phosphonomethoxypropyl)adenine] treatment on SHIV(KU2) infection of rhesus macaques. Virology 277:306-315.
66. Smythies, L. E., A. Maheshwari, R. Clements, D. Eckhoff, L. Novak, H. L. Vu, L. M. Mosteller-Barnum, M. Sellers, and P. D. Smith. 2006. Mucosal IL-8 and TGF-beta recruit blood monocytes: evidence for cross-talk between the lamina propria stroma and myeloid cells. J. Leukoc. Biol. 80:492-499.
67. + memory T cells reveals early branched pathways of T cell differentiation in humans. Proc. Natl. Acad. Sci. USA 102:7916-7921.
68. Stone, J. D., C. C. Heise, C. J. Miller, C. H. Halsted, and S. Dandekar. 1994. Development of malabsorption and nutritional complications in simian immunodeficiency virus-infected rhesus macaques. AIDS 8:1245-1256.
69. Sturm, A., and A. U. Dignass. 2002. Modulation of gastrointestinal wound repair and inflammation by phospholipids. Biochim. Biophys. Acta 1582: 282-288.
70. + T cells in lymphoid tissues during simian immunodeficiency virus infection. J. Virol. 74:11001-11007.
71. + T-cell restoration during antiretroviral therapy. J. Med. Primatol. 36:219-227.
72. + T lymphocytes during primary human immunodeficiency virus type 1 infection: regulation by interleukin (IL)-2, IL-15, and Bcl-2. J. Infect. Dis. 187:1735-1747.
73. Zimmerli, S. C., A. Harari, C. Cellerai, F. Vallelian, P. A. Bart, and G. Pantaleo. 2005. HIV-1-specific IFN-gamma/IL-2-secreting CD8 T cells support CD4-independent proliferation of HIV-1-specific CD8 T cells. Proc. Natl. Acad. Sci. USA 102:7239-7244.