Differential Th17 CD4 T-cell depletion in pathogenic and nonpathogenic lentiviral infections

Blood

Volumn 112, Issue 7, 2008, Pages 2826-2835

  Brenchley, Jason M ^a,h   Paiardini, Mirko ^b   Knox, Kenneth S ^c,d   Asher, Ava I ^a   Cervasi, Barbara ^b   Asher, Tedi E ^a   Scheinberg, Phillip ^a   Price, David A ^a,e   Hage, Chadi A ^c,d   Kholi, Lisa M ^c   Khoruts, Alexander ^f   Frank, Ian ^b   Else, James ^g   Schacker, Timothy ^f   Silvestri, Guido ^b   Douek, Daniel C ^a,h  

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

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c INDIANA UNIVERSITY   (United States)

^d RICHARD L ROUDEBUSH VETERANS AFFAIRS MEDICAL CENTER   (United States)

^e CARDIFF UNIVERSITY SCHOOL OF MEDICINE   (United Kingdom)

^f UNIVERSITY OF MINNESOTA   (United States)

^g EMORY UNIVERSITY   (United States)

^h VRC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ARTICLE; CD4+ T LYMPHOCYTE; CELL MATURATION; CERCOCEBUS; CLINICAL ARTICLE; CONTROLLED STUDY; GASTROINTESTINAL TRACT; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HUMAN TISSUE; LUNG LAVAGE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RETROVIRUS INFECTION; SIMIAN IMMUNODEFICIENCY VIRUS; T CELL DEPLETION; TH17 CELL; ANIMAL; CELL DIFFERENTIATION; HELPER CELL; IMMUNOLOGY; LYMPHOCYTE DEPLETION; PATHOLOGY; TH1 CELL; VIROLOGY;

BACTERIAL ANTIGEN; EPITOPE; FUNGUS ANTIGEN;

ANIMALS; ANTIGENS, BACTERIAL; ANTIGENS, FUNGAL; BRONCHOALVEOLAR LAVAGE; CELL DIFFERENTIATION; CERCOCEBUS ATYS; EPITOPES; GASTROINTESTINAL TRACT; HIV INFECTIONS; HUMANS; LENTIVIRUS INFECTIONS; LYMPHOCYTE DEPLETION; PHENOTYPE; SIMIAN IMMUNODEFICIENCY VIRUS; T-LYMPHOCYTES, HELPER-INDUCER; TH1 CELLS;

EID: 53449093632     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2008-05-159301     Document Type: Article

References (53)

1. Mosmann TR, Cherwinski H, Bond MW, Giedlin MA. Coffman RL. Two types of murine helper T cell clone: I. Definition according to profiles of lymphokine activities and secreted proteins. J Immunol. 1986;136:2348-2357.
2. Aggarwal S, Ghilardi N, Xie MH, de Sauvage FJ, Gurney AL. Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17. J Biol Chem. 2003; 278:1910-1914.
3. Langrish CL, Chen Y, Blumenschein WM, et al. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med. 2005;201:233-240.
4. Harrington LE, Hatton RD, Mangan PR, et al. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol. 2005;6:1123-1132.
5. Park H, Li Z, Yang XO, et al. Adistinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol. 2005;6:1133-1141.
6. Steinman L. A brief history of T(H)17, the first major revision in the T(H)1/T(H)2 hypothesis of T cell-mediated tissue damage. Nat Med. 2007;13: 139-145.
7. Kao CY, Chen Y, Thai P, et al. IL-17 markedly upregulates beta-defensin-2 expression in human airway epithelium via JAK and NF-kappaB signaling pathways. J Immunol. 2004;173:3482-3491.
8. Liang SC, Tan XY, Luxenberg DP, et al. Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. J Exp Med. 2006;203: 2271-2279.
9. Kolls JK, Linden A. Interleukin-17 family members and inflammation. Immunity. 2004;21:467-476.
10. Huang W, Na L, Fidel PL, Schwarzenberger P. Requirement of interleukin-17A for systemic anti-Candida albicans host defense in mice. J Infect Dis. 2004;190:624-631.
11. Chung DR, Kasper DL, Panzo RJ, et al. CD4+T cells mediate abscess formation in intra-abdominal sepsis by an IL-17-dependent mechanism. J Immunol. 2003;170:1958-1963.
12. Rohn TA, Jennings GT, Hernandez M, et al. Vaccination against IL-17 suppresses autoimmune arthritis and encephalomyelitis. EurJ Immunol. 2006;36:2857-2867.
13. Sonderegger I, Rohn TA, Kurrer MO, et al. Neutralization of IL-17 by active vaccination inhibits IL-23-dependent autoimmune myocarditis. Eur J Immunol. 2006;36:2849-2856.
14. Samoilova EB, Horton JL, Hilliard B, Liu TS, Chen Y. IL-6-deficient mice are resistant to experimental autoimmune encephalomyelitis: roles of IL-6 in the activation and differentiation of autoreactive T cells. J Immunol. 1998;161:6480-6486.
15. Acosta-Rodriguez EV, Rivino L, Geginat J, et al. Surface phenotype and antigenic specificity of human interleukin 17-producing T helper memory cells. Nat Immunol. 2007;8:639-646.
16. Annunziato F, Cosmi L, Santarlasci V, et al. Phenotypic and functional features of human Th17 cells. J Exp Med. 2007;204:1849-1861.
17. 2+CCR5-phenotype. J Immunol. 2007;178: 7525-7529.
18. Stein TP, Koerner B, Schluter MD, et al. Weight loss, the gut and the inflammatory response in aids patients. Cytokine. 1997;9:143-147.
19. Brenchley JM, Price DA, Schacker TW, et al. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med. 2006;12:1365-1371.
20. Anselmi A, Vendrame D, Rampon O, Giaquinto C, Zanchetta M, De Rossi A. Immune reconstitution in human immunodeficiency virus type 1-infected children with different virological responses to anti-retroviral therapy. Clin Exp Immunol. 2007;150:442-450.
21. Cecchinato V, Trindale C, Laurence A, et al. Altered balance between Th17 and Th1 cells at mucosal sites predicts AIDS progression in simian immunodeficienty virus-infected macaques. Mucosal Immunol. 2008;1:279-288.
22. Balagopal A, Philp FH, Astemborski J, et al. Human immunodeficiency virus-related microbial translocation and progression of hepatitis C. Gastroenterology. 2008;135:226-233.
23. Twigg HL, Soliman DM, Day RB, et al. Lymphocytic alveolitis, bronchoalveolar lavage viral load, and outcome in human immunodeficiency virus infection. Am J Respir Crit Care Med. 1999;159: 1439-1444,
24. Pitcher CJ, Quittner C, Peterson DM, et al. HIV-1 - specific CD4+ T cells are detectable in most individuals with active HIV-1 infection, but decline with prolonged viral suppression. Nat Med. 1999; 5:518-525.
25. Brenchley JM, Hill BJ, Ambrozak DR, et al. T-cell subsets that harbor human immunodeficiency virus (HIV) in vivo: implications for HIV pathogenesis. J Virol. 2004;78:1160-1168.
26. Douek DC, Betts MR, Brenchley JM, et al. A novel approach to the analysis of specificity, clonality, and frequency of HIV-specific T cell responses reveals a potential mechanism for control of viral escape. J Immunol. 2002;168:3099-3104.
27. Douek DC, Brenchley JM, Betts MR, et al. HIV preferentially infects HIV-specific CD4+ T-cells. Nature. 2002;417:95-98.
28. Scheinberg P, Melenhorst JJ, Hill BJ, et al. The clonal composition of human CD4+CD25 + Foxp3+ cells determined by a comprehensive DNA-based multiplex PCR for TCRB gene rearrangements. J Immunol Methods. 2007;321:107-120.
29. Li Q, Estes JD, Duan L, et al. Simian immunodeficiency virus-induced intestinal cell apoptosis is the underlying mechanism of the regenerative enteropathy of early infection. J Infect Dis. 2008; 197:420-429.
30. Kotler DP. Characterization of intestinal disease associated with human immunodeficiency virus infection and response to antiretroviral therapy. J Infect Dis. 1999;179(Suppl 3):454-456.
31. Bjarnason I, Sharpstone DR, Francis N, et al. Intestinal inflammation, ileal structure and function in HIV. AIDS. 1996;10:1385-1391.
32. Brenchley JM, SchackerTW, Ruff LE, et al. CD4+ T-cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J Exp Med. 2004;200:749-759.
33. Mehandru S, Poles MA, Tenner-Racz K, et al. Primary HIV-1 infection is associated with preferential depletion of CD4+ T lymphocytes from effector sites in the gastrointestinal tract. J Exp Med. 2004;200:761-770.
34. Guadalupe M, Reay E, Sankaran S, et al. Severe CD4+ 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. 2003;77:11708-11717.
35. Critchfield JW, Lemongello D, Walker DH, et al. Multifunctional human immunodeficiency virus (HIV) gag-specific CD8+ T-cell responses in rectal mucosa and peripheral blood mononuclear cells during chronic HIVtype 1 infection. J Virol. 2007;81:5460-5471.
36. Shacklett BL, Cox CA, Sandberg JK, Stollman NH, Jacobson MA, Nixon DF. Trafficking of human immunodeficiency vims type 1-specific CD8+ T cells to gut-associated lymphoid tissue during chronic infection. J Virol. 2003;77:5621-5631.
37. Mehandru S, Poles MA, Tenner-Racz K, et al. Mechanisms of gastrointestinal CD4+ T-cell depletion during acute and early human immunodeficiency virus type 1 Infection. J Virol. 2007;81: 599-612.
38. Brenchley JM, Knox KK, Asher Al, et al. High frequencies of polyfunctional HIV-specificT cells are associated with preservation of mucosal CD4T cells in bronchoalveolar lavage. Mucosal Immunol. 2008;1:49-58.
39. Appay V, Rowland-Jones SL. Premature ageing of the immune system: the cause of AIDS? Trends Immunol. 2002;23:580-585.
40. Appay V, Zaunders JJ, Papagno L, et al. Characterization of CD4(+) CTLs ex vivo. J Immunol. 2002;168:5954-5958.
41. Brenchley JM, Ruff LE, Casazza JP, Koup RA, Price DA, Douek DC. Preferential infection shortens the life span of human immunodeficiency virus-specific CD4+ T cells in vivo. J Virol. 2006; 80:6801-6809.
42. Betts MR, Nason MC, West SM, et al. HlV nonprogressors preferentially maintain highly functional HIV-specific CD8+ T-cells. Blood. 2006; 107:4781-4789.
43. Silvestri G, Sodora DL, Koup RA, et al. Nonpathogenic SIV infection of sooty mangabeys is characterized by limited bystander immunopathology despite chronic high-level viremia. Immunity. 2003;18:441-452.
44. Gordon SN, Klatt NR, Bosinger SE, et al. Severe depletion of mucosal CD4+ T cells in AIDS-free simian immunodeficiency virus-infected sooty mangabeys. J Immunol. 2007;179:3026-3034.
45. Rodriguez B, Sethi AK, Cheruvu VK, etal. Predictive value of plasma HIV RNA level on rate of CD4T-cell decline in untreated HIV infection. JAMA. 2006;296:1498-1506.
46. Sharpstone D, Neild P, Crane R, et al. Small intestinal transit, absorption, and permeability in patients with AIDS with and without diarrhoea. Gut. 1999;45:70-76.
47. Lane HC, Masur H, Edgar LC, Whalen G, Rook AH, Fauci AS. Abnormalities of B-cell activation and immunoregulation in patients with the acquired immunodeficiency syndrome. N Engl JMed. 1983;309:453-458.
48. Hellerstein M, Hanley MB, Cesar D, et al. Directly measured kinetics of circulating T lymphocytes in normal and HIV-1-infected humans. Nat Med. 1999;5:83-89.
49. Hazenberg MD, Stuart JW, Otto SA, et al. T-cell division in human immunodeficiency virus (HIV)-1 infection is mainly due to immune activation: a longitudinal analysis in patients before and during highly active antiretroviral therapy (HAART). Blood. 2000;95:249-255.
50. Valdez H, Lederman MM. Cytokines and cytokine therapies in HIV infection. AIDS Clin Rev. 1997: 187-228.
51. Fahey JL. Cytokines, plasma immune activation markers, and clinically relevant surrogate markers in human immunodeficiency virus infection. Clin Diagn Lab Immunol. 1998;5:597-603.
52. Milner J, Brenchley JM, Laurence A, et al. Impaired Th17 cell differentiation in subjects with autosomal dominant hyper-IgE syndrome. Nature. 2008;452:773-776.
53. Denning TL, Wang YC, Patel SR, Williams IR, Pulendran B. Lamina propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses. Nat Immunol. 2007;8:1086-1094.