Strong viremia control in vaccinated macaques does not prevent gradual Th17 cell loss from central memory

Vaccine

Volumn 29, Issue 35, 2011, Pages 6017-6028

  Demberg, Thorsten ^a   Ettinger, Amelia C ^a   Aladi, Stanley ^a   McKinnon, Katherine ^a   Kuddo, Thea ^b   Venzon, David ^c   Patterson, L Jean ^a   Phillips, Terry M ^b   Robert Guroff, Marjorie ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b NATIONAL INSTITUTE OF BIOMEDICAL IMAGING AND BIOENGINEERING   (United States)

^c Biostatistics and Data Management Section   (United States)

Author keywords

Chronic immune activation; Microbial translocation; Simian human immunodeficiency virus; Tc17 cells; Th17 cells; Vaccine

Indexed keywords

CHEMOKINE RECEPTOR CCR6; GAMMA INTERFERON; KI 67 ANTIGEN; PROTEIN INHIBITOR OF ACTIVATED STAT; VIRUS ENVELOPE PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CELL LOSS; CONTROLLED STUDY; ERYTHROCYTE PRESERVATION; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MACACA; NONHUMAN; NUCLEOTIDE SEQUENCE; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETROSPECTIVE STUDY; TH17 CELL; VIREMIA;

AIDS VACCINES; ANIMALS; HIV INFECTIONS; HIV-1; IMMUNOLOGIC MEMORY; MACACA MULATTA; SAIDS VACCINES; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; TH17 CELLS; VACCINATION; VIREMIA;

EID: 79960707966     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2011.06.032     Document Type: Article

References (86)

1. Haase A.T. Perils at mucosal front lines for HIV and SIV and their hosts. Nat Rev Immunol 2005, 5(10):783-792.
2. Miller C.J., Li Q., Abel K., Kim E.Y., Ma Z.M., Wietgrefe S., et al. Propagation and dissemination of infection after vaginal transmission of simian immunodeficiency virus. J Virol 2005, 79(14):9217-9227.
3. Ling B., Mohan M., Lackner A.A., Green L.C., Marx P.A., Doyle L.A., et al. The large intestine as a major reservoir for simian immunodeficiency virus in macaques with long-term, nonprogressing infection. J Infect Dis 2010, 202(12):1846-1854.
4. Mattapallil J.J., Douek D.C., Hill B., Nishimura Y., Martin M., Roederer M. Massive infection and loss of memory CD4+ T cells in multiple tissues during acute SIV infection. Nature 2005, 434(7037):1093-1097.
5. Brenchley J.M., Douek D.C. HIV infection and the gastrointestinal immune system. Mucosal Immunol 2008, 1(1):23-30.
6. Brenchley J.M., Schacker T.W., Ruff L.E., Price D.A., Taylor J.H., Beilman G.J., et al. CD4+ T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J Exp Med 2004, 200(6):749-759.
7. Gordon S.N., Klatt N.R., Bosinger S.E., Brenchley J.M., Milush J.M., Engram J.C., et al. Severe depletion of mucosal CD4+ T cells in AIDS-free simian immunodeficiency virus-infected sooty mangabeys. J Immunol 2007, 179(5):3026-3034.
8. Bello G., Velasco-de-Castro C.A., Bongertz V., Rodrigues C.A., Giacoia-Gripp C.B., Pilotto J.H., et al. Immune activation and antibody responses in non-progressing elite controller individuals infected with HIV-1. J Med Virol 2009, 81(10):1681-1690.
9. Loke P., Favre D., Hunt P.W., Leung J.M., Kanwar B., Martin J.N., et al. Correlating cellular and molecular signatures of mucosal immunity that distinguish HIV controllers from noncontrollers. Blood 2010, 115(15):e20-32.
10. Vollbrecht T., Brackmann H., Henrich N., Roeling J., Seybold U., Bogner J.R., et al. Impact of changes in antigen level on CD38/PD-1 co-expression on HIV-specific CD8 T cells in chronic, untreated HIV-1 infection. J Med Virol 2010, 82(3):358-370.
11. Nazli A., Chan O., Dobson-Belaire W.N., Ouellet M., Tremblay M.J., Gray-Owen S.D., et al. Exposure to HIV-1 directly impairs mucosal epithelial barrier integrity allowing microbial translocation. PLoS Pathog 2010, 6(4):e1000852.
12. 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(12):1365-1371.
13. Klatt N.R., Harris L.D., Vinton C.L., Sung H., Briant J.A., Tabb B., et al. Compromised gastrointestinal integrity in pigtail macaques is associated with increased microbial translocation, immune activation, and IL-17 production in the absence of SIV infection. Mucosal Immunol 2010, 3(4):387-398.
14. Marchetti G., Bellistri G.M., Borghi E., Tincati C., Ferramosca S., La Francesca M., et al. Microbial translocation is associated with sustained failure in CD4+ T-cell reconstitution in HIV-infected patients on long-term highly active antiretroviral therapy. AIDS 2008, 22(15):2035-2038.
15. Troseid M., Nowak P., Nystrom J., Lindkvist A., Abdurahman S., Sonnerborg A. Elevated plasma levels of lipopolysaccharide and high mobility group box-1 protein are associated with high viral load in HIV-1 infection: reduction by 2-year antiretroviral therapy. AIDS 2010, 24(11):1733-1737.
16. Crome S.Q., Wang A.Y., Levings M.K. Translational mini-review series on Th17 cells: function and regulation of human T helper 17 cells in health and disease. Clin Exp Immunol 2010, 159(2):109-119.
17. Damsker J.M., Hansen A.M., Caspi R.R. Th1 and Th17 cells: adversaries and collaborators. Ann N Y Acad Sci 2010, 1183:211-221.
18. Hashimoto M., Hirota K., Yoshitomi H., Maeda S., Teradaira S., Akizuki S., et al. Complement drives Th17 cell differentiation and triggers autoimmune arthritis. J Exp Med 2010, 207(6):1135-1143.
19. Kamada N., Hisamatsu T., Honda H., Kobayashi T., Chinen H., Takayama T., et al. TL1A produced by lamina propria macrophages induces Th1 and Th17 immune responses in cooperation with IL-23 in patients with Crohn's disease. Inflamm Bowel Dis 2010, 16(4):568-575.
20. Wu H.J., Ivanov I.I., Darce J., Hattori K., Shima T., Umesaki Y., et al. Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity 2010, 32(6):815-827.
21. Zhao Y., Balato A., Fishelevich R., Chapoval A., Mann D.L., Gaspari A.A. Th17/Tc17 infiltration and associated cytokine gene expression in elicitation phase of allergic contact dermatitis. Br J Dermatol 2009, 161(6):1301-1306.
22. Kuang D.M., Peng C., Zhao Q., Wu Y., Zhu L.Y., Wang J., et al. Tumor-activated monocytes promote expansion of IL-17-producing CD8+ T cells in hepatocellular carcinoma patients. J Immunol 2010, 185(3):1544-1549.
23. Hamada H., Garcia-Hernandez Mde L., Reome J.B., Misra S.K., Strutt T.M., McKinstry K.K., et al. Tc17, a unique subset of CD8 T cells that can protect against lethal influenza challenge. J Immunol 2009, 182(6):3469-3481.
24. Fenoglio D., Poggi A., Catellani S., Battaglia F., Ferrera A., Setti M., et al. Vdelta1 T lymphocytes producing IFN-gamma and IL-17 are expanded in HIV-1-infected patients and respond to Candida albicans. Blood 2009, 113(26):6611-6618.
25. Xu S., Han Y., Xu X., Bao Y., Zhang M., Cao X. IL-17A-producing gammadeltaT cells promote CTL responses against Listeria monocytogenes infection by enhancing dendritic cell cross-presentation. J Immunol 2010, 185(10):5879-5887.
26. Cua D.J., Tato C.M. Innate IL-17-producing cells: the sentinels of the immune system. Nat Rev Immunol 2010, 10(7):479-489.
27. Annunziato F., Cosmi L., Liotta F., Maggi E., Romagnani S. The phenotype of human Th17 cells and their precursors, the cytokines that mediate their differentiation and the role of Th17 cells in inflammation. Int Immunol 2008, 20(11):1361-1368.
28. de Jong E., Suddason T., Lord G.M. Translational mini-review series on Th17 cells: development of mouse and human T helper 17 cells. Clin Exp Immunol 2010, 159(2):148-158.
29. Romagnani S., Maggi E., Liotta F., Cosmi L., Annunziato F. Properties and origin of human Th17 cells. Mol Immunol 2009, 47(1):3-7.
30. Torchinsky M.B., Blander J.M. T helper 17 cells: discovery, function, and physiological trigger. Cell Mol Life Sci 2010, 67(9):1407-1421.
31. Klatt N.R., Brenchley J.M. Th17 cell dynamics in HIV infection. Curr Opin HIV AIDS 2010, 5(2):135-140.
32. Ndhlovu L.C., Chapman J.M., Jha A.R., Snyder-Cappione J.E., Pagan M., Leal F.E., et al. Suppression of HIV-1 plasma viral load below detection preserves IL-17 producing T cells in HIV-1 infection. Aids 2008, 22(8):990-992.
33. Maek A.N.W., Buranapraditkun S., Klaewsongkram J., Ruxrungtham K. Increased interleukin-17 production both in helper T cell subset Th17 and CD4-negative T cells in human immunodeficiency virus infection. Viral Immunol 2007, 20(1):66-75.
34. Dodon M.D., Li Z., Hamaia S., Gazzolo L. Tax protein of human T-cell leukaemia virus type 1 induces interleukin 17 gene expression in T cells. J Gen Virol 2004, 85(Pt 7):1921-1932.
35. Brenchley J.M., Paiardini M., Knox K.S., Asher A.I., Cervasi B., Asher T.E., et al. Differential Th17 CD4 T-cell depletion in pathogenic and nonpathogenic lentiviral infections. Blood 2008, 112(7):2826-2835.
36. Hunt P.W. Th17, gut, and HIV: therapeutic implications. Curr Opin HIV AIDS 2010, 5(2):189-193.
37. Prendergast A., Prado J.G., Kang Y.H., Chen F., Riddell L.A., Luzzi G., et al. HIV-1 infection is characterized by profound depletion of CD161+ Th17 cells and gradual decline in regulatory T cells. AIDS 2010, 24(4):491-502.
38. Nigam P., Kwa S., Velu V., Amara R.R. Loss of IL-17-producing CD8 T cells during late chronic stage of pathogenic simian immunodeficiency virus infection. J Immunol 2011, 186(2):745-753.
39. Demberg T., Florese R.H., Heath M.J., Larsen K., Kalisz I., Kalyanaraman V.S., et al. A replication-competent adenovirus-human immunodeficiency virus (Ad-HIV) tat and Ad-HIV env priming/Tat and envelope protein boosting regimen elicits enhanced protective efficacy against simian/human immunodeficiency virus SHIV89.6P challenge in rhesus macaques. J Virol 2007, 81(7):3414-3427.
40. Malkevitch N.V., Patterson L.J., Aldrich M.K., Wu Y., Venzon D., Florese R.H., et al. Durable protection of rhesus macaques immunized with a replicating adenovirus-SIV multigene prime/protein boost vaccine regimen against a second SIVmac251 rectal challenge: role of SIV-specific CD8+ T cell responses. Virology 2006, 353(1):83-98.
41. Patterson L.J., Beal J., Demberg T., Florese R.H., Malkevich N., Venzon D., et al. Replicating adenovirus HIV/SIV recombinant priming alone or in combination with a gp140 protein boost results in significant control of viremia following a SHIV89.6P challenge in Mamu-A*01 negative rhesus macaques. Virology 2008, 374(2):322-337.
42. Patterson L.J., Daltabuit-Test M., Xiao P., Zhao J., Hu W., Wille-Reece U., et al. Rapid SIV Env-specific mucosal and serum antibody induction augments cellular immunity in protecting immunized, elite-controller macaques against high dose heterologous SIV challenge. Virology 2011, 411(1):87-102.
43. Patterson L.J., Malkevitch N., Venzon D., Pinczewski J., Gomez-Roman V.R., Wang L., et al. Protection against mucosal simian immunodeficiency virus SIV(mac251) challenge by using replicating adenovirus-SIV multigene vaccine priming and subunit boosting. J Virol 2004, 78(5):2212-2221.
44. Lubeck M.D., Natuk R., Myagkikh M., Kalyan N., Aldrich K., Sinangil F., et al. Long-term protection of chimpanzees against high-dose HIV-1 challenge induced by immunization. Nat Med 1997, 3(6):651-658.
45. Tseng C.-P., Cheng J.-C., Tseng C.-C., Wang C., Chen Y.-L., Chiu D.T.-Y., et al. Broad-range ribosomal RNA real-time PCR after removal of DNA from reagents: melting profiles for clinically important bacteria. Clin Chem 2003, 49:306-309.
46. Farrelly V., Rainey F.A., Stackebrandt E. Effect of genome size and rrn gene copy number on PCR amplification of 16S rRNA genes from a mixture of bacterial species. Appl Environ Microbiol 1995, 61:2798-2801.
47. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001, 29(9):e45.
48. Kaur A., Hale C.L., Ramanujan S., Jain R.K., Johnson R.P. Differential dynamics of CD4(+) and CD8(+) T-lymphocyte proliferation and activation in acute simian immunodeficiency virus infection. J Virol 2000, 74(18):8413-8424.
49. Kader M., Wang X., Piatak M., Lifson J., Roederer M., Veazey R., et al. Alpha4(+)beta7(hi)CD4(+) memory T cells harbor most Th-17 cells and are preferentially infected during acute SIV infection. Mucosal Immunol 2009, 2(5):439-449.
50. Kader M., Bixler S., Piatak M., Lifson J., Mattapallil J.J. Anti-retroviral therapy fails to restore the severe Th-17: Tc-17 imbalance observed in peripheral blood during simian immunodeficiency virus infection. J Med Primatol 2009, 38(Suppl 1):32-38.
51. Jiang W., Lederman M.M., Hunt P., Sieg S.F., Haley K., Rodriguez B., 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(8):1177-1185.
52. El Hed A., Khaitan A., Kozhaya L., Manel N., Daskalakis D., Borkowsky W., et al. Susceptibility of human Th17 cells to human immunodeficiency virus and their perturbation during infection. J Infect Dis 2010, 201(6):843-854.
53. Lim H.W., Lee J., Hillsamer P., Kim C.H. Human Th17 cells share major trafficking receptors with both polarized effector T cells and FOXP3+ regulatory T cells. J Immunol 2008, 180(1):122-129.
54. Miller Sanders C., Cruse J.M., Lewis R.E. Toll-like receptor and chemokine receptor expression in HIV-infected T lymphocyte subsets. Exp Mol Pathol 2010, 88(1):26-31.
55. Potzl J., Botteron C., Tausch E., Pedre X., Mueller A.M., Mannel D.N., et al. Tracing functional antigen-specific CCR6 Th17 cells after vaccination. PLoS One 2008, 3(8):e2951.
56. Yamazaki T., Yang X.O., Chung Y., Fukunaga A., Nurieva R., Pappu B., et al. CCR6 regulates the migration of inflammatory and regulatory T cells. J Immunol 2008, 181(12):8391-8401.
57. Ciccone E.J., Greenwald J.H., Lee P.I., Biancotto A., Read S.W., Yao M.A., et al. CD4+ T cells, including Th17 and cycling subsets, are intact in the gut mucosa of HIV-1-infected long-term nonprogressors. J Virol 2011, 85(12):5880-5888.
58. Redd A.D., Gray R.H., Quinn T.C. Is microbial translocation a cause or consequence of HIV disease progression?. J Infect Dis 2011, 203:744-745.
59. Leinert C., Stahl-Hennig C., Ecker A., Schneider T., Fuchs D., Sauermann U., et al. Microbial translocation in simian immunodeficiency virus (SIV)-infected rhesus monkeys (Macaca mulatta). J Med Primatol 2010, 39(4):243-251.
60. Brenchley J.M., Douek D.C. The mucosal barrier and immune activation in HIV pathogenesis. Curr Opin HIV AIDS 2008, 3(3):356-361.
61. Pandrea I.V., Gautam R., Ribeiro R.M., Brenchley J.M., Butler I.F., Pattison M., et al. Acute loss of intestinal CD4+ T cells is not predictive of simian immunodeficiency virus virulence. J Immunol 2007, 179(5):3035-3046.
62. Paiardini M. Th17 cells in natural SIV hosts. Curr Opin HIV AIDS 2010, 5(2):166-172.
63. Bennett-Guerrero E., Barclay G.R., Weng P.L., Bodian C.A., Feierman D.E., Vela-Cantos F., et al. Endotoxin-neutralizing capacity of serum from cardiac surgical patients. J Cardiothorac Vasc Anesth 2001, 15(4):451-454.
64. Simon J.K., Wahid R., Maciel M., Picking W.L., Kotloff K.L., Levine M.M., et al. Antigen-specific B memory cell responses to lipopolysaccharide (LPS) and invasion plasmid antigen (Ipa) B elicited in volunteers vaccinated with live-attenuated Shigella flexneri 2a vaccine candidates. Vaccine 2009, 27(4):565-572.
65. Nelson J.W., Butler S.L., Brown P.H., Greening A.P., Govan J.R. Serum IgG and sputum IgA antibody to core lipopolysaccharide antigen from Pseudomonas cepacia in patients with cystic fibrosis. J Med Microbiol 1993, 39(1):39-47.
66. Redd A.D., Dabitao D., Bream J.H., Charvat B., Laeyendecker O., Kiwanuka N., et al. Microbial translocation, the innate cytokine response, and HIV-1 disease progression in Africa. Proc Natl Acad Sci USA 2009, 106(16):6718-6723.
67. Lim A., Amini A., D'Orsogna L., Rajasuriar R., Kramski M., Lewin S.R., Purcell D., Price P., French M.A. Antibody and B cell responses may control circulating lipopolysaccharide in patients with HIV infection. AIDS 2011, doi:10.1097/QAD.0b013e328348a789.
68. Leligdowicz A., Feldmann J., Jaye A., Cotten M., Dong T., McMichael A., et al. Direct relationship between virus load and systemic immune activation in HIV-2 infection. J Infect Dis 2010, 201(1):114-122.
69. Redd A.D., Eaton K.P., Kong X., Laeyendecker O., Lutalo T., Wawer M.J., et al. C-reactive protein levels increase during HIV-1 disease progression in Rakai, Uganda, despite the absence of microbial translocation. J Acquir Immune Defic Syndr 2010, 54(5):556-559.
70. Tuaillon E., Al Tabaa Y., Baillat V., Segondy M., Picot M.C., Reynes J., et al. Close association of CD8+/CD38 bright with HIV-1 replication and complex relationship with CD4+ T-cell count. Cytometry B Clin Cytom 2009, 76B(4):249-260.
71. Mueller Y.M., Do D.H., Boyer J.D., Kader M., Mattapallil J.J., Lewis M.G., et al. CD8+ cell depletion of SHIV89.6P-infected macaques induces CD4+ T cell proliferation that contributes to increased viral loads. J Immunol 2009, 183(8):5006-5012.
72. Okoye A., Meier-Schellersheim M., Brenchley J.M., Hagen S.I., Walker J.M., Rohankhedkar M., et al. Progressive CD4+ central memory T cell decline results in CD4+ effector memory insufficiency and overt disease in chronic SIV infection. J Exp Med 2007, 204(9):2171-2185.
73. Chattopadhyay P.K., Roederer M. Good cell, bad cell: flow cytometry reveals T-cell subsets important in HIV disease. Cytometry A 2010, 77(7):614-622.
74. Manrique M., Kozlowski P.A., Cobo-Molinos A., Wang S.W., Wilson R.L., Montefiori D.C., et al. Long-term control of simian immunodeficiency Virus mac251 viremia to undetectable levels in half of infected female rhesus macaques nasally vaccinated with simian immunodeficiency virus DNA/recombinant modified vaccinia virus Ankara. J Immunol 2011, 186(6):3581-3593.
75. Roberts L., Passmore J.A., Williamson C., Little F., Bebell L.M., Mlisana K., et al. Plasma cytokine levels during acute HIV-1 infection predict HIV disease progression. AIDS 2010, 24(6):819-831.
76. Raffatellu M., Santos R.L., Verhoeven D.E., George M.D., Wilson R.P., Winter S.E., et al. Simian immunodeficiency virus-induced mucosal interleukin-17 deficiency promotes Salmonella dissemination from the gut. Nat Med 2008, 14(4):421-428.
77. Fitzgerald-Bocarsly P., Jacobs E.S. Plasmacytoid dendritic cells in HIV infection: striking a delicate balance. J Leukoc Biol 2010, 87(4):609-620.
78. Swiecki M., Colonna M. Unraveling the functions of plasmacytoid dendritic cells during viral infections, autoimmunity, and tolerance. Immunol Rev 2010, 234(1):142-162.
79. Harris L.D., Tabb B., Sodora D.L., Paiardini M., Klatt N.R., Douek D.C., et al. Downregulation of robust acute type I interferon responses distinguishes nonpathogenic simian immunodeficiency virus (SIV) infection of natural hosts from pathogenic SIV infection of rhesus macaques. J Virol 2010, 84(15):7886-7891.
80. Haller O., Staeheli P., Kochs G. Protective role of interferon-induced Mx GTPases against influenza viruses. Rev Sci Technol 2009, 28(1):219-231.
81. Nyman T.A., Tolo H., Parkkinen J., Kalkkinen N. Identification of nine interferon-alpha subtypes produced by Sendai virus-induced human peripheral blood leucocytes. Biochem J 1998, 329(Pt 2):295-302.
82. Easlick J., Szubin R., Lantz S., Baumgarth N., Abel K. The early interferon alpha subtype response in infant macaques infected orally with SIV. J Acquir Immune Defic Syndr 2010, 55(1):14-28.
83. Zhang Y., Lou B., Lal R.B., Gettie A., Marx P.A., Moore J.P. Use of inhibitors to evaluate coreceptor usage by simian and simian/human immunodeficiency viruses and human immunodeficiency virus type 2 in primary cells. J Virol 2000, 74(15):6893-6910.
84. Hofmann-Lehmann R., Williams A.L., Swenerton R.K., Li P.L., Rasmussen R.A., Chenine A.L., et al. Quantitation of simian cytokine and beta-chemokine mRNAs, using real-time reverse transcriptase-polymerase chain reaction: variations in expression during chronic primate lentivirus infection. AIDS Res Hum Retroviruses 2002, 18(9):627-639.
85. Hardstedt M., Finnegan C.P., Kirchhof N., Hyland K.A., Wijkstrom M., Murtaugh M.P., et al. Post-transplant upregulation of chemokine messenger RNA in non-human primate recipients of intraportal pig islet xenografts. Xenotransplantation 2005, 12(4):293-302.
86. Medeiros M., Sharma V.K., Ding R., Yamaji K., Li B., Muthukumar T., et al. Optimization of RNA yield, purity and mRNA copy number by treatment of urine cell pellets with RNAlater. J Immunol Methods 2003, 279(1-2):135-142.