Incomplete recovery of pneumococcal CD4 T cell immunity after initiation of antiretroviral therapy in HIV-infected Malawian adults

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Sepako, Enoch ^a,b   Glennie, Sarah J ^a,e   Jambo, Kondwani C ^a,b   Mzinza, David ^a   Iwajomo, Oluwadamilola H ^a,d,e   Banda, Dominic ^a   Van Oosterhout, Joep J ^c   Williams, Neil A ^e   Gordon, Stephen B ^b   Heyderman, Robert S ^a  

^a UNIVERSITY OF MALAWI   (Malawi)

^b LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

^c DIGNITAS INTERNATIONAL   (Malawi)

^d UNIVERSITY OF TORONTO   (Canada)

^e UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIRETROVIRUS AGENT; CD40 LIGAND; CYTOKINE; EFAVIRENZ; EFAVIRENZ PLUS LAMIVUDINE PLUS STAVUDINE; GAMMA INTERFERON; INTERLEUKIN 2; LAMIVUDINE PLUS NEVIRAPINE PLUS STAVUDINE; LAMIVUDINE PLUS NEVIRAPINE PLUS ZIDOVUDINE; PNEUMOLYSIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; T LYMPHOCYTE RECEPTOR;

ADULT; ANTIGEN EXPRESSION; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL STRAIN; BACTERIUM ISOLATION; BACTERIUM MUTANT; CD4+ T LYMPHOCYTE; CELL PROLIFERATION ASSAY; CELLULAR IMMUNITY; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSPOT ASSAY; FEMALE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HUMAN TISSUE; IMMUNOASSAY; INTRACELLULAR CYTOKINE ASSAY; LYMPHOCYTE PROLIFERATION; MALE; NASOPHARYNGEAL SWAB; NONHUMAN; PNEUMOCOCCAL INFECTION; PROTEIN EXPRESSION; RISK ASSESSMENT; STREPTOCOCCUS PNEUMONIAE; THROAT CULTURE; TREATMENT DURATION; CD4 LYMPHOCYTE COUNT; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HIV INFECTIONS; IMMUNOLOGY; IMMUNOPHENOTYPING; LYMPHOCYTE ACTIVATION; MALAWI; METABOLISM; MIDDLE AGED; MIXED INFECTION; PHENOTYPE; T LYMPHOCYTE SUBPOPULATION; VIROLOGY; VIRUS LOAD;

ADULT; ANTIRETROVIRAL THERAPY, HIGHLY ACTIVE; CD4 LYMPHOCYTE COUNT; CD4-POSITIVE T-LYMPHOCYTES; CD40 LIGAND; COINFECTION; FEMALE; HIV INFECTIONS; HUMANS; IMMUNOPHENOTYPING; INTERFERON-GAMMA; LYMPHOCYTE ACTIVATION; MALAWI; MALE; MIDDLE AGED; PHENOTYPE; PNEUMOCOCCAL INFECTIONS; STREPTOCOCCUS PNEUMONIAE; T-CELL ANTIGEN RECEPTOR SPECIFICITY; T-LYMPHOCYTE SUBSETS; VIRAL LOAD;

EID: 84903519454     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0100640     Document Type: Article

References (44)

1. Greenwood B (1999) The epidemiology of pneumococcal infection in children in the developing world. Philos Trans R Soc Lond B Biol Sci 354: 777-785.
2. O'Brien KL, Wolfson LJ, Watt JP, Henkle E, Deloria-Knoll M, et al. (2009) Burden of disease caused by Streptococcus pneumoniae in children younger than 5 years: global estimates. Lancet 374: 893-902.
3. McEllistrem MC, Mendelsohn AB, Pass MA, Elliott JA, Whitney CG, et al. (2002) Recurrent invasive pneumococcal disease in individuals with human immunodeficiency virus infection. J Infect Dis 185: 1364-1368. (Pubitemid 34439149)
4. Klugman KP, Madhi SA, Feldman C (2007) HIV and pneumococcal disease. Curr Opin Infect Dis 20: 11-15. (Pubitemid 46052121)
5. Gordon SB, Chaponda M, Walsh AL, Whitty CJ, Gordon MA, et al. (2002) Pneumococcal disease in HIV-infected Malawian adults: acute mortality and long-term survival. AIDS 16: 1409-1417. (Pubitemid 34722073)
6. Pido-Lopez J, Kwok WW, Mitchell TJ, Heyderman RS, Williams NA (2011) Acquisition of pneumococci specific effector and regulatory Cd4+ T cells localising within human upper respiratory-tract mucosal lymphoid tissue. PLoS Pathog 7: e1002396.
7. Basset A, Thompson CM, Hollingshead SK, Briles DE, Ades EW, et al. (2007) Antibody-independent, CD4+ T-cell-dependent protection against pneumococcal colonization elicited by intranasal immunization with purified pneumococcal proteins. Infect Immun 75: 5460-5464. (Pubitemid 350033635)
8. Rapola S, Jantti V, Haikala R, Syrjanen R, Carlone GM, et al. (2000) Natural development of antibodies to pneumococcal surface protein A, pneumococcal surface adhesin A, and pneumolysin in relation to pneumococcal carriage and acute otitis media. J Infect Dis 182: 1146-1152.
9. Zhang Q, Bagrade L, Bernatoniene J, Clarke E, Paton JC, et al. (2007) Low CD4 T cell immunity to pneumolysin is associated with nasopharyngeal carriage of pneumococci in children. J Infect Dis 195: 1194-1202. (Pubitemid 46543453)
10. Mureithi MW, Finn A, Ota MO, Zhang Q, Davenport V, et al. (2009) T cell memory response to pneumococcal protein antigens in an area of high pneumococcal carriage and disease. J Infect Dis 200: 783-793.
11. Glennie SJ, Sepako E, Mzinza D, Harawa V, Miles DJ, et al. (2011) Impaired CD4 T cell memory response to Streptococcus pneumoniae precedes CD4 T cell depletion in HIV-infected Malawian adults. PLoS One 6: e25610.
12. Iwajomo OH, Finn A, Moons P, Nkhata R, Sepako E, et al. (2011) Deteriorating pneumococcal-specific B-cell memory in minimally symptomatic African children with HIV infection. J Infect Dis 204: 534-543.
13. Knox KS, Vinton C, Hage CA, Kohli LM, Twigg HL 3rd, et al. (2010) Reconstitution of CD4 T cells in bronchoalveolar lavage fluid after initiation of highly active antiretroviral therapy. J Virol 84: 9010-9018.
14. Wilkinson KA, Seldon R, Meintjes G, Rangaka MX, Hanekom WA, et al. (2009) Dissection of regenerating T-Cell responses against tuberculosis in HIV-infected adults sensitized by Mycobacterium tuberculosis. Am J Respir Crit Care Med 180: 674-683.
15. Nunes MC, von Gottberg A, de Gouveia L, Cohen C, Kuwanda L, et al. (2011) Persistent high burden of invasive pneumococcal disease in South African HIV-infected adults in the era of an antiretroviral treatment program. PLoS One 6: e27929.
16. Heffernan RT, Barrett NL, Gallagher KM, Hadler JL, Harrison LH, et al. (2005) Declining incidence of invasive Streptococcus pneumoniae infections among persons with AIDS in an era of highly active antiretroviral therapy, 1995-2000. J Infect Dis 191: 2038-2045. (Pubitemid 40800574)
17. Glennie SJ, Banda D, Gould K, Hinds J, Kamngona A, et al. (2013) Defective pneumococcal-specific Th1 responses in HIV-infected adults precedes a loss of control of pneumococcal colonization. Clin Infect Dis 56: 291-299.
18. O'Brien KL, Nohynek H (2003) Report from a WHO Working Group: standard method for detecting upper respiratory carriage of Streptococcus pneumoniae. Pediatr Infect Dis J 22: e1-11.
19. Berry AM, Ogunniyi AD, Miller DC, Paton JC (1999) Comparative virulence of Streptococcus pneumoniae strains with insertion-duplication, point, and deletion mutations in the pneumolysin gene. Infect Immun 67: 981-985. (Pubitemid 29059247)
20. Chattopadhyay PK, Yu J, Roederer M (2006) Live-cell assay to detect antigen-specific CD4+ T-cell responses by CD154 expression. Nat Protoc 1: 1-6.
21. Jambo KC, Sepako E, Fullerton DG, Mzinza D, Glennie S, et al. (2011) Bronchoalveolar CD4+ T cell responses to respiratory antigens are impaired in HIV-infected adults. Thorax 66: 375-382.
22. Sallusto F, Lenig D, Forster R, Lipp M, Lanzavecchia A (1999) Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401: 708-712.
23. Cao W, Jamieson BD, Hultin LE, Hultin PM, Detels R (2009) Regulatory T cell expansion and immune activation during untreated HIV type 1 infection are associated with disease progression. AIDS Res Hum Retroviruses 25: 183-191.
24. Darrah PA, Patel DT, De Luca PM, Lindsay RW, Davey DF, et al. (2007) Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat Med 13: 843-850. (Pubitemid 47038186)
25. Brenchley JM, Knox KS, Asher AI, Price DA, Kohli LM, et al. (2008) High frequencies of polyfunctional HIV-specific T cells are associated with preservation of mucosal CD4 T cells in bronchoalveolar lavage. Mucosal Immunol 1: 49-58.
26. Sutherland JS, Young JM, Peterson KL, Sanneh B, Whittle HC, et al. (2010) Polyfunctional CD4(+) and CD8(+) T cell responses to tuberculosis antigens in HIV-1-infected patients before and after anti-retroviral treatment. J Immunol 184: 6537-6544.
27. Van Braeckel E, Desombere I, Clement F, Vandekerckhove L, Verhofstede C, et al. (2013) Polyfunctional CD4(+) T cell responses in HIV-1-infected viral controllers compared with those in healthy recipients of an adjuvanted polyprotein HIV-1 vaccine. Vaccine 31: 3739-3746.
28. Betts MR, Nason MC, West SM, De Rosa SC, Migueles SA, et al. (2006) HIV nonprogressors preferentially maintain highly functional HIV-specific CD8+ T cells. Blood 107: 4781-4789. (Pubitemid 43882629)
29. Kalsdorf B, Scriba TJ, Wood K, Day CL, Dheda K, et al. (2009) HIV-1 infection impairs the bronchoalveolar T-cell response to mycobacteria. Am J Respir Crit Care Med 180: 1262-1270.
30. Dworkin MS, Ward JW, Hanson DL, Jones JL, Kaplan JE (2001) Pneumococcal disease among human immunodeficiency virus-infected persons: incidence, risk factors, and impact of vaccination. Clin Infect Dis 32: 794-800. (Pubitemid 32221939)
31. Gilks CF, Ojoo SA, Ojoo JC, Brindle RJ, Paul J, et al. (1996) Invasive pneumococcal disease in a cohort of predominantly HIV-1 infected female sexworkers in Nairobi, Kenya. Lancet 347: 718-723. (Pubitemid 26085646)
32. Malley R, Henneke P, Morse SC, Cieslewicz MJ, Lipsitch M, et al. (2003) Recognition of pneumolysin by Toll-like receptor 4 confers resistance to pneumococcal infection. Proc Natl Acad Sci U S A 100: 1966-1971. (Pubitemid 36254557)
33. Amdahl BM, Rubins JB, Daley CL, Gilks CF, Hopewell PC, et al. (1995) Impaired natural immunity to pneumolysin during human immunodeficiency virus infection in the United States and Africa. Am J Respir Crit Care Med 152: 2000-2004.
34. Jambo KC, Sepako E, Glennie SJ, Mzinza D, Williams NA, et al. (2012) Naturally-acquired influenza-specific CD4+ T-cell proliferative responses are impaired in HIV-infected African adults. PLoS One 7: e38628.
35. French N, Nakiyingi J, Carpenter LM, Lugada E, Watera C, et al. (2000) 23-valent pneumococcal polysaccharide vaccine in HIV-1-infected Ugandan adults: double-blind, randomised and placebo controlled trial. Lancet 355: 2106-2111. (Pubitemid 30364659)
36. WHO (2008d) 23-valent pneumococcal polysaccharide vaccine:WHO position paper. 373-384 p.
37. French N, Gordon SB, Mwalukomo T, White SA, Mwafulirwa G, et al. (2010) A trial of a 7-valent pneumococcal conjugate vaccine in HIV-infected adults. N Engl J Med 362: 812-822.
38. Lange CG, Valdez H, Medvik K, Asaad R, Lederman MM (2002) CD4+ T-lymphocyte nadir and the effect of highly active antiretroviral therapy on phenotypic and functional immune restoration in HIV-1 infection. Clin Immunol 102: 154-161. (Pubitemid 34171514)
39. French M, Keane N, McKinnon E, Phung S, Price P (2007) Susceptibility to opportunistic infections in HIV-infected patients with increased CD4 T-cell counts on antiretroviral therapy may be predicted by markers of dysfunctional effector memory CD4 T cells and B cells. HIV Med 8: 148-155.
40. Sieg SF, Mitchem JB, Bazdar DA, Lederman MM (2002) Close link between CD4 + and CD8 + T cell proliferation defects in patients with human immunodeficiency virus disease and relationship to extended periods of CD4+lymphopenia. J Infect Dis 185: 1401-1416.
41. Lederman HM, Williams PL, Wu JW, Evans TG, Cohn SE, et al. (2003) Incomplete immune reconstitution after initiation of highly active antiretroviral therapy in human immunodeficiency virus-infected patients with severe CD4+cell depletion. J Infect Dis 188: 1794-1803. (Pubitemid 38064863)
42. Forbes EK, Sander C, Ronan EO, McShane H, Hill AV, et al. (2008) Multifunctional, high-level cytokine-producing Th1 cells in the lung, but not spleen, correlate with protection against Mycobacterium tuberculosis aerosol challenge in mice. J Immunol 181: 4955-4964.
43. Abel B, Tameris M, Mansoor N, Gelderbloem S, Hughes J, et al. (2010) The novel tuberculosis vaccine, AERAS-402, induces robust and polyfunctional CD4+ and CD8+ T cells in adults. Am J Respir Crit Care Med 181: 1407-1417.
44. Beveridge NE, Price DA, Casazza JP, Pathan AA, Sander CR, et al. (2007) Immunisation with BCG and recombinant MVA85A induces long-lasting, polyfunctional Mycobacterium tuberculosis-specific CD4+ memory T lymphocyte populations. Eur J Immunol 37: 3089-3100. (Pubitemid 350131288)