Simian immunodeficiency virus-induced alterations in monocyte production of tumor necrosis factor alpha contribute to reduced immune activation in sooty mangabeys

Journal of Virology

Volumn 86, Issue 14, 2012, Pages 7605-7615

  Mir, Kiran D ^a,b   Bosinger, Steven E ^b   Gasper, Melanie ^a   Ho, On ^c   Else, James G ^b,d   Brenchley, Jason M ^e   Kelvin, David J ^f   Silvestri, Guido ^b,d   Hu, Shiu Lok ^c   Sodora, Donald L ^a  

^a SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^b EMORY UNIVERSITY   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^f UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 6; INTERLEUKIN 8; LIPOPOLYSACCHARIDE; LIPOTEICHOIC ACID; MESSENGER RNA; SINGLE STRANDED RNA; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD8+ T LYMPHOCYTE; CERCOCEBUS; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOSE RESPONSE; EX VIVO STUDY; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOSTIMULATION; IMMUNOSUPPRESSIVE TREATMENT; IN VITRO STUDY; INFECTION CONTROL; LYMPHOCYTE ACTIVATION; MONOCYTE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; RESPIRATORY BURST; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN VIRUS;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CERCOCEBUS ATYS; HIV-1; HUMANS; INTERLEUKIN-10; LIPOPOLYSACCHARIDES; LYMPHOCYTE ACTIVATION; MONOCYTES; PHAGOCYTOSIS; PHYTOHEMAGGLUTININS; RNA, MESSENGER; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; TEICHOIC ACIDS; TOLL-LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR-ALPHA; VIRAL LOAD;

ANIMALIA; HUMAN IMMUNODEFICIENCY VIRUS 1; MACACA; SIMIAE; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 84863764742     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.06813-11     Document Type: Article

References (55)

1. Abel K, et al. 2003. Simian-human immunodeficiency virus SHIV89.6-induced protection against intravaginal challenge with pathogenic SIVmac239 is independent of the route of immunization and is associated with a combination of cytotoxic T-lymphocyte and alpha interferon responses. J. Virol. 77:3099-3118.
2. Beaumier CM, et al. 2009. CD4 downregulation by memory CD4+ T cells in vivo renders African green monkeys resistant to progressive SIVagm infection. Nat. Med. 15:879-885.
3. Biggs BA, Hewish M, Kent S, Hayes K, Crowe SM. 1995. HIV-1 infection of human macrophages impairs phagocytosis and killing of Toxoplasma gondii. J. Immunol. 154:6132-6139.
4. Böhmer RH, Trinkle LS, Staneck JL. 1992. Dose effects of LPS on neutrophils in a whole blood flow cytometric assay of phagocytosis and oxidative burst. Cytometry 13:525-531.
5. Bosinger SE, et al. 2009. Global genomic analysis reveals rapid control of a robust innate response in SIV-infected sooty mangabeys. J. Clin. Invest. 119:3556-3572.
6. Bravo-Cuellar A, Nowacki W, Vuillier F, de Saint-Martin J, Orbach-Arbouys S. 1992. The bactericidal capacity of peripheral blood monocytes from HIV positive patients may collapse very soon after the infection. Immunol. Lett. 31:297-299.
7. Brenchley JM, et al. 2008. Differential Th17 CD4 T-cell depletion in pathogenic and nonpathogenic lentiviral infections. Blood 112:2826-2835.
8. Brenchley JM, Price DA, Douek DC. 2006. HIV disease: fallout from a mucosal catastrophe? Nat. Immunol. 7:235-239.
9. Brenchley JM, et al. 2006. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat. Med. 12:1365-1371.
10. Brunialti MK, Kallas EG, Freudenberg M, Galanos C, Salomao R. 2002. Influence of EDTA and heparin on lipopolysaccharide binding and cell activation, evaluated at single-cell level in whole blood. Cytometry 50:14-18.
11. Chantry D, Turner M, Abney E, Feldmann M. 1989. Modulation of cytokine production by transforming growth factor-beta. J. Immunol. 142:4295-4300.
12. Cross AS, et al. 2001. Active immunization with a detoxified Escherichia coli J5 lipopolysaccharide group B meningococcal outer membrane protein complex vaccine protects animals from experimental sepsis. J. Infect. Dis. 183:1079-1086.
13. Durudas A, et al. 2009. Elevated levels of innate immune modulators in lymph nodes and blood are associated with more-rapid disease progression in simian immunodeficiency virus-infected monkeys. J. Virol. 83: 12229-12240.
14. Estes JD, et al. 2008. Early resolution of acute immune activation and induction of PD-1 in SIV-infected sooty mangabeys distinguishes nonpathogenic from pathogenic infection in rhesus macaques. J. Immunol. 180:6798-6807.
15. Fidder HH, Hommes DW. 2010. Anti-TNF and Crohn's disease: when should we start? Curr. Drug Targets 11:143-147.
16. Giorgi JV, et al. 1999. Shorter survival in advanced human immunodeficiency virus type 1 infection is more closely associated with T lymphocyte activation than with plasma virus burden or virus chemokine coreceptor usage. J. Infect. Dis. 179:859-870.
17. Giorgi JV, et al. 2002. Predictive value of immunologic and virologic markers after long or short duration of HIV-1 infection. J. Acquir. Immune Defic. Syndr. 29:346-355.
18. Harris LD, et al. 2010. 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. 84:7886-7891.
19. Heinzelmann M, Mercer-Jones MA, Flodgaard H, Miller FN. 1998. Heparin-binding protein (CAP37) is internalized in monocytes and increases LPS-induced monocyte activation. J. Immunol. 160:5530-5536.
20. Ho O, et al. 2009. Pathogenic infection of Macaca nemestrina with a CCR5-tropic subtype-C simian-human immunodeficiency virus. Retrovirology 6:65.
21. Hober D, et al. 1989. Production of tumour necrosis factor-alpha (TNFalpha) and interleukin-1 (IL-1) in patients with AIDS. Enhanced level of TNF-alpha is related to a higher cytotoxic activity. Clin. Exp. Immunol. 78:329-333.
22. Jacquelin B, et al. 2009. Nonpathogenic SIV infection of African green monkeys induces a strong but rapidly controlled type I IFN response. J. Clin. Invest. 119:3544-3555.
23. Jin J, Chang Y, Wei W. 2010. Clinical application and evaluation of anti-TNF-alpha agents for the treatment of rheumatoid arthritis. Acta Pharmacol. Sin. 31:1133-1140.
24. Klatt NR, et al. 2010. 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. 3:387-398.
25. Kollias G, Douni E, Kassiotis G, Kontoyiannis D. 1999. The function of tumour necrosis factor and receptors in models of multi-organ inflammation, rheumatoid arthritis, multiple sclerosis and inflammatory bowel disease. Ann. Rheum. Dis. 58(Suppl 1):I32-I39.
26. Lederer S, et al. 2009. Transcriptional profiling in pathogenic and nonpathogenic SIV infections reveals significant distinctions in kinetics and tissue compartmentalization. PLoS Pathog. 5:e1000296. doi:10.1371/ journal.ppat.1000296.
27. McMichael AJ, Borrow P, Tomaras GD, Goonetilleke N, Haynes BF. 2010. The immune response during acute HIV-1 infection: clues for vaccine development. Nat. Rev. Immunol. 10:11-23.
28. Meier A, et al. 2007. MyD88-dependent immune activation mediated by human immunodeficiency virus type 1-encoded Toll-like receptor ligands. J. Virol. 81:8180-8191.
29. Meythaler M, et al. 2009. Differential CD4+ T-lymphocyte apoptosis and bystander T-cell activation in rhesus macaques and sooty mangabeys during acute simian immunodeficiency virus infection. J. Virol. 83:572-583.
30. Milush JM, et al. 2011. Lack of clinical AIDS in SIV-infected sooty mangabeys with significant CD4+ T cell loss is associated with double-negative T cells. J. Clin. Invest. 121:1-9.
31. Milush JM, et al. 2007. Virally induced CD4+ T cell depletion is not sufficient to induce AIDS in a natural host. J. Immunol. 179:3047-3056.
32. Milush JM, et al. 2007. Mucosal innate immune response associated with a timely humoral immune response and slower disease progression after oral transmission of simian immunodeficiency virus to rhesus macaques. J. Virol. 81:6175-6186.
33. Mir KD, Gasper M, Sundaravaradan V, Sodora DL. 2011. SIV infection in natural hosts: resolution of immune activation during the acute-tochronic transition phase. Microbes Infect. 13:14-24.
34. Munford RS. 2005. Detoxifying endotoxin: time, place and person. J. Endotoxin Res. 11:69-84.
35. National Research Council. 1996. Guide for the care and use of laboratory animals, 8th ed. National Academy Press, Washington, DC.
36. Nguyen BY, Reveille JD. 2009. Rheumatic manifestations associated with HIV in the highly active antiretroviral therapy era. Curr. Opin. Rheumatol. 21:404-410.
37. Orendi JM, et al. 1998. Activation and cell cycle antigens in CD4+ and CD8+ T cells correlate with plasma human immunodeficiency virus (HIV-1) RNA level in HIV-1 infection. J. Infect. Dis. 178:1279-1287.
38. Pandrea I, Apetrei C. 2010. Where the wild things are: pathogenesis of SIV infection in African nonhuman primate hosts. Curr. HIV/AIDS Rep. 7:28-36.
39. Pandrea I, Sodora DL, Silvestri G, Apetrei C. 2008. Into the wild: simian immunodeficiency virus (SIV) infection in natural hosts. Trends Immunol. 29:419-428.
40. Porter SB. 1997. Current status of clinical trials with anti-TNF. Chest 112:339S-341S.
41. Pos O, Stevenhagen A, Meenhorst PL, Kroon FP, Van Furth R. 1992. Impaired phagocytosis of Staphylococcus aureus by granulocytes and monocytes of AIDS patients. Clin. Exp. Immunol. 88:23-28.
42. Reddy MM, Sorrell SJ, Lange M, Grieco MH. 1988. Tumor necrosis factor and HIV P24 antigen levels in serum of HIV-infected populations. J. Acquir. Immune Defic. Syndr. 1:436-440.
43. Saukkonen K, et al. 1990. The role of cytokines in the generation of inflammation and tissue damage in experimental gram-positive meningitis. J. Exp. Med. 171:439-448.
44. Schindler M, et al. 2006. Nef-mediated suppression of T cell activation was lost in a lentiviral lineage that gave rise to HIV-1. Cell 125:1055-1067.
45. Shale MJ, et al. 2010. Review article: chronic viral infection in the antitumour necrosis factor therapy era in inflammatory bowel disease. Aliment. Pharmacol. Ther. 31:20-34.
46. Silvestri G. 2005. Naturally SIV-infected sooty mangabeys: are we closer to understanding why they do not develop AIDS? J. Med. Primatol. 34: 243-252.
47. Silvestri G, et al. 2003. Nonpathogenic SIV infection of sooty mangabeys is characterized by limited bystander immunopathology despite chronic high-level viremia. Immunity 18:441-452.
48. Sodora DL, et al. 2009. Toward an AIDS vaccine: lessons from natural simian immunodeficiency virus infections of African nonhuman primate hosts. Nat. Med. 15:861-865.
49. Sodora DL, Silvestri G. 2008. Immune activation and AIDS pathogenesis. AIDS 22:439-446.
50. Strieter RM, Kunkel SL, Bone RC. 1993. Role of tumor necrosis factoralpha in disease states and inflammation. Crit. Care Med. 21:S447-S463.
51. Taaffe J, et al. 2010. A five-year longitudinal analysis of sooty mangabeys naturally infected with simian immunodeficiency virus reveals a slow but progressive decline in CD4+ T-cell count whose magnitude is not predicted by viral load or immune activation. J. Virol. 84:5476-5484.
52. Wan Y, et al. 2009. Interleukin-1 receptor-associated kinase 2 is critical for lipopolysaccharide-mediated post-transcriptional control. J. Biol. Chem. 284:10367-10375.
53. Wertheim JO, Worobey M. 2009. Dating the age of the SIV lineages that gave rise to HIV-1 and HIV-2. PLoS Comput. Biol. 5:e1000377. doi: 10.1371/journal.pcbi.1000377.
54. Williams KC, Burdo TH. 2009. HIV and SIV infection: the role of cellular restriction and immune responses in viral replication and pathogenesis. APMIS 117:400-412.
55. Worobey M, et al. 2010. Island biogeography reveals the deep history of SIV. Science 329:1487.