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Immune System Modulation by Helminth Infections: Potential Impact on HIV Transmission and Disease Progression

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How Helminths Alter Immunity to Infection

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 828))

Abstract

The co-prevalence of helminth and HIV-1 infections in sub-Saharan Africa has fueled the suspicion that helminth infections constitute an important factor contributing to the high HIV prevalence in this region. Furthermore, it has been hypothesized that anti-helminthic treatment of co-infected HIV-positive patients is a potentially cost effective public health measurement that delays HIV disease progression and thus eligibility to antiretroviral therapy. Here we review the scientific data on the interaction between different helminth species and HIV on an epidemiological level and address pathogenic mechanisms that have been hypothesized to increase HIV susceptibility or rate of disease progression in helminth-HIV co-infected patients. We first focus on the basic concepts of HIV transmission, pathogenesis and then aim to consolidate the available data from human cohort studies, animal models and in vitro experiments to provide a coherent overview on the current state of knowledge in this field.

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References

  1. Sharp PM, Hahn BH (2011) Origins of HIV and the AIDS pandemic. Cold Spring Harb Perspect Med 1(1):a006841 (Cold Spring Harbor Laboratory Press)

    PubMed  PubMed Central  Google Scholar 

  2. Keele BF, Van Heuverswyn F, Li Y, Bailes E, Takehisa J, Santiago ML et al (2006) Chimpanzee reservoirs of pandemic and nonpandemic HIV-1. Science 313(5786):523–536

    PubMed  CAS  PubMed Central  Google Scholar 

  3. Chen Z, Telfier P, Gettie A, Reed P, Zhang L, Ho DD et al (1996) Genetic characterization of new West African simian immunodeficiency virus SIVsm: geographic clustering of household-derived SIV strains with human immunodeficiency virus type 2 subtypes and genetically diverse viruses from a single feral sooty mangabey troop. J Virol 70(6):3617–3627

    PubMed  CAS  PubMed Central  Google Scholar 

  4. Gao F, Yue L, White AT, Pappas PG, Barchue J, Hanson AP et al (1992) Human infection by genetically diverse SIVSM-related HIV-2 in west Africa. Nature 358(6386):495–499

    PubMed  CAS  Google Scholar 

  5. Hirsch VM, Olmsted RA, Murphey-Corb M, Purcell RH, Johnson PR (1989) An African primate lentivirus (SIVsm) closely related to HIV-2. Nature 339(6223):389–392

    PubMed  CAS  Google Scholar 

  6. Plantier J-C, Leoz M, Dickerson JE, De Oliveira F, Cordonnier F, Lemée V et al (2009) A new human immunodeficiency virus derived from gorillas. Nat Med 15(8):871–872

    PubMed  CAS  Google Scholar 

  7. Korber B, Muldoon M, Theiler J, Gao F, Gupta R, Lapedes A et al (2000) Timing the ancestor of the HIV-1 pandemic strains. Science 288(5472):1789–1796

    PubMed  CAS  Google Scholar 

  8. Worobey M, Gemmel M, Teuwen DE, Haselkorn T, Kunstman K, Bunce M et al (2008) Direct evidence of extensive diversity of HIV-1 in Kinshasa by 1960. Nature 455(7213):661–664

    PubMed  CAS  PubMed Central  Google Scholar 

  9. Barré-Sinoussi F, Chermann JC, Rey F, Nugeyre MT, Chamaret S, Gruest J et al (1983) Isolation of a T-lymphotropic retrovirus from a patient at risk for acquired immune deficiency syndrome (AIDS). Rev Invest Clin 56(2):126–129

    Google Scholar 

  10. Gallo RC, Sarin PS, Gelmann EP, Robert-Guroff M, Richardson E, Kalyanaraman VS et al (1983) Isolation of human T-cell leukemia virus in acquired immune deficiency syndrome (AIDS). Science 220(4599):865–867

    PubMed  CAS  Google Scholar 

  11. UNAIDS (2012) Global report: UNAIDS report on the global AIDS epidemic, pp 8–33

    Google Scholar 

  12. Cohen MS, Chen YQ, McCauley M, Gamble T, Hosseinipour MC, Kumarasamy N et al (2011) Prevention of HIV-1 infection with early antiretroviral therapy. N Engl J Med 365(6):493–505 (NIH Public Access)

    PubMed  CAS  PubMed Central  Google Scholar 

  13. Hanson S, Hanson C (2008) HIV control in low-income countries in sub-Saharan Africa: are the right things done? Glob Health Action 1:1–8

    Google Scholar 

  14. Moir S, Chun T-W, Fauci AS (2011) Pathogenic mechanisms of HIV disease. Annu Rev Pathol 6:223–248

    PubMed  CAS  Google Scholar 

  15. Merlin R (2012) Viral dynamics and immune response in acute infection and their impact on viral set-point. AIDS vaccine confernce. AIDS vaccine conference, Boston

    Google Scholar 

  16. Koup RA, Safrit JT, Cao Y, Andrews CA, McLeod G, Borkowsky W et al (1994) Temporal association of cellular immune responses with the initial control of viremia in primary human immunodeficiency virus type 1 syndrome. J Virol 68(7):4650–4655

    PubMed  CAS  PubMed Central  Google Scholar 

  17. Borrow P, Lewicki H, Hahn BH, Shaw GM, Oldstone MB (1994) Virus-specific CD8+ cytotoxic T-lymphocyte activity associated with control of viremia in primary human immunodeficiency virus type 1 infection. J Virol 68(9):6103–6110

    PubMed  CAS  PubMed Central  Google Scholar 

  18. Ogg GS, Jin X, Bonhoeffer S, Dunbar RP, Nowak MA, Monard S et al (1998) Quantitation of HIV-1-specific cytotoxic T lymphocytes and plasma load of viral RNA. Science 279(5359):2103–2106

    PubMed  CAS  Google Scholar 

  19. Jin X, Bauer DE, Tuttleton SE, Lewin S, Gettie A, Blanchard J et al (1999) Dramatic rise in plasma viremia after CD8+ T cell depletion in simian immunodeficiency virus-infected macaques. J Exp Med 189(6):991–998

    PubMed  CAS  PubMed Central  Google Scholar 

  20. Schmitz JE, Kuroda MJ, Santra S, Sasseville VG, Simon MA, Lifton MA et al (1999) Control of viremia in simian immunodeficiency virus infection by CD8+ lymphocytes. Science 283(5403):857–860

    PubMed  CAS  Google Scholar 

  21. Mellors JW, Rinaldo CR, Gupta P, White RM, Todd JA, Kingsley LA (1996) Prognosis in HIV-1 infection predicted by the quantity of virus in plasma. Science 272(5265):1167–1170

    PubMed  CAS  Google Scholar 

  22. Altfeld M, Addo MM, Rosenberg ES, Hecht FM, Lee PK, Vogel M et al (2003) Influence of HLA-B57 on clinical presentation and viral control during acute HIV-1 infection. AIDS 17(18):2581–2591

    PubMed  CAS  Google Scholar 

  23. Kiepiela P, Leslie AJ, Honeyborne I, Ramduth D, Thobakgale C, Chetty S et al (2004) Dominant influence of HLA-B in mediating the potential co-evolution of HIV and HLA. Nature 432(7018):769–775

    PubMed  CAS  Google Scholar 

  24. Kiepiela P, Ngumbela K, Thobakgale C, Ramduth D, Honeyborne I, Moodley E et al (2007) CD8+ T-cell responses to different HIV proteins have discordant associations with viral load. Nat Med 13(1):46–53 (Nature Publishing Group)

    PubMed  CAS  Google Scholar 

  25. Geldmacher C, Currier JR, Herrmann E, Haule A, Kuta E, McCutchan F et al (2007) CD8 T-cell recognition of multiple epitopes within specific Gag regions is associated with maintenance of a low steady-state viremia in human immunodeficiency virus type 1-seropositive patients. J Virol 81(5):2440–2448

    PubMed  CAS  PubMed Central  Google Scholar 

  26. Edwards BH, Bansal A, Sabbaj S, Bakari J, Mulligan MJ, Goepfert PA (2002) Magnitude of functional CD8+ T-cell responses to the gag protein of human immunodeficiency virus type 1 correlates inversely with viral load in plasma. J Virol 76(5):2298–2305

    PubMed  CAS  PubMed Central  Google Scholar 

  27. Gray RH, Wawer MJ, Brookmeyer R, Sewankambo NK, Serwadda D, Wabwire-Mangen F et al (2001) Probability of HIV-1 transmission per coital act in monogamous, heterosexual, HIV-1-discordant couples in Rakai, Uganda. Lancet 357(9263):1149–1153

    PubMed  CAS  Google Scholar 

  28. Madigan N (2004) New H.I.V. Infection found in sex-film industry. New York Times

    Google Scholar 

  29. Pilcher CD, Tien HC, Eron JJ, Vernazza PL, Leu S-Y, Stewart PW et al (2004) Brief but efficient: acute HIV infection and the sexual transmission of HIV. J Infect Dis 189(10):1785–1792

    PubMed  Google Scholar 

  30. Sheth PM, Danesh A, Sheung A, Rebbapragada A, Shahabi K, Kovacs C et al (2006) Disproportionately high semen shedding of HIV is associated with compartmentalized cytomegalovirus reactivation. J Infect Dis 193(1):45–48

    PubMed  Google Scholar 

  31. Cohen MS, Hoffman IF, Royce RA, Kazembe P, Dyer JR, Daly CC (1997) et al Reduction of concentration of HIV-1 in semen after treatment of urethritis: implications for prevention of sexual transmission of HIV-1. AIDSCAP Malawi Research Group. Lancet 349(9069):1868–1873

    PubMed  CAS  Google Scholar 

  32. Kaul R, Pettengell C, Sheth PM, Sunderji S, Biringer A, MacDonald K et al (2008) The genital tract immune milieu: an important determinant of HIV susceptibility and secondary transmission. J Reprod Immunol 77(1):32–40

    PubMed  CAS  Google Scholar 

  33. Arthos J, Cicala C, Martinelli E, Macleod K, Van Ryk D, Wei D et al (2008) HIV-1 envelope protein binds to and signals through integrin alpha4beta7, the gut mucosal homing receptor for peripheral T cells. Nat Immunol 9(3):301–309

    PubMed  CAS  Google Scholar 

  34. Cicala C, Martinelli E, McNally JP, Goode DJ, Gopaul R, Hiatt J et al (2009) The integrin alpha4beta7 forms a complex with cell-surface CD4 and defines a T-cell subset that is highly susceptible to infection by HIV-1. Proc Natl Acad Sci U S A 106(49):20877–20882

    PubMed  CAS  PubMed Central  Google Scholar 

  35. Zolla-Pazner S, deCamp AC, Cardozo T, Karasavvas N, Gottardo R, Williams C et al (2013) Analysis of V2 antibody responses induced in vaccinees in the ALVAC/AIDSVAX HIV-1 vaccine efficacy trial. PLoS One 8(1):e53629

    PubMed  CAS  PubMed Central  Google Scholar 

  36. Liao H-X, Bonsignori M, Alam SM, McLellan JS, Tomaras GD, Moody MA et al (2013) Vaccine induction of antibodies against a structurally heterogeneous site of immune pressure within HIV-1 envelope protein variable regions 1 and 2. Immunity 38(1):176–186

    PubMed  CAS  PubMed Central  Google Scholar 

  37. Haynes BF, Gilbert PB, McElrath MJ, Zolla-Pazner S, Tomaras GD, Alam SM et al (2012) Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N Engl J Med 366(14):1275–1286

    PubMed  CAS  PubMed Central  Google Scholar 

  38. Hladik F, Sakchalathorn P, Ballweber L, Lentz G, Fialkow M, Eschenbach D et al (2007) Initial events in establishing vaginal entry and infection by human immunodeficiency virus type-1. Immunity 26(2):257–270

    PubMed  CAS  PubMed Central  Google Scholar 

  39. Maier R, Bartolomé-Rodríguez MM, Moulon C, Weltzien HU, Meyerhans A (2000) Kinetics of CXCR4 and CCR5 up-regulation and human immunodeficiency virus expansion after antigenic stimulation of primary CD4+ T lymphocytes. Blood 96(5):1853–1856

    PubMed  CAS  Google Scholar 

  40. Zhang Z, Schuler T, Zupancic M, Wietgrefe S, Staskus KA, Reimann KA et al (1999) Sexual transmission and propagation of SIV and HIV in resting and activated CD4+ T cells. Science 286(5443):1353–1357

    PubMed  CAS  Google Scholar 

  41. Jaspan HB, Liebenberg L, Hanekom W, Burgers W, Coetzee D, Williamson A-L et al (2011) Immune activation in the female genital tract during HIV infection predicts mucosal CD4 depletion and HIV shedding. J Infect Dis 204(10):1550–1556

    PubMed  CAS  PubMed Central  Google Scholar 

  42. Zhang Z, Wietgrefe SW, Li Q, Shore MD, Duan L, Reilly C et al (2004) Roles of substrate availability and infection of resting and activated CD4+ T cells in transmission and acute simian immunodeficiency virus infection. Proc Natl Acad Sci U S A 101(15):5640–5645

    PubMed  CAS  PubMed Central  Google Scholar 

  43. Li Q, Duan L, Estes JD, Ma Z-M, Rourke T, Wang Y et al (2005) Peak SIV replication in resting memory CD4+ T cells depletes gut lamina propria CD4+ T cells. Nature 434(7037):1148–1152

    PubMed  CAS  Google Scholar 

  44. Brenchley JM, Schacker TW, Ruff LE, Price DA, Taylor JH, Beilman GJ et al (2004) CD4+ T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J Exp Med 200(6):749–759

    PubMed  CAS  PubMed Central  Google Scholar 

  45. Mattapallil JJ, Douek DC, Hill B, Nishimura Y, Martin M, Roederer M (2005) Massive infection and loss of memory CD4+ T cells in multiple tissues during acute SIV infection. Nature 434(7037):1093–1097

    PubMed  CAS  Google Scholar 

  46. Veazey RS, DeMaria M, Chalifoux LV, Shvetz DE, Pauley DR, Knight HL et al (1998) Gastrointestinal tract as a major site of CD4+ T cell depletion and viral replication in SIV infection. Science 280(5362):427–431

    PubMed  CAS  Google Scholar 

  47. Mehandru S, Poles MA, Tenner-Racz K, Horowitz A, Hurley A, Hogan C et al (2004) Primary HIV-1 infection is associated with preferential depletion of CD4+ T lymphocytes from effector sites in the gastrointestinal tract. J Exp Med 200(6):761–770

    PubMed  CAS  PubMed Central  Google Scholar 

  48. Geldmacher C, Koup RA (2012) Pathogen-specific T cell depletion and reactivation of opportunistic pathogens in HIV infection. Trends Immunol 33(5):207–214 (Elsevier Ltd)

    PubMed  CAS  PubMed Central  Google Scholar 

  49. Grossman Z, Meier-Schellersheim M, Paul WE, Picker LJ (2006) Pathogenesis of HIV infection: what the virus spares is as important as what it destroys. Nat Med 12(3):289–295

    PubMed  CAS  Google Scholar 

  50. Okoye AA, Rohankhedkar M, Abana C, Pattenn A, Reyes M, Pexton C et al (2012) Naive T cells are dispensable for memory CD4+ T cell homeostasis in progressive simian immunodeficiency virus infection. J Exp Med 209(4):641–651

    PubMed  CAS  PubMed Central  Google Scholar 

  51. Okoye A, Meier-Schellersheim M, Brenchley JM, Hagen SI, Walker JM, Rohankhedkar M et al (2007) Progressive CD4+ central memory T cell decline results in CD4+ effector memory insufficiency and overt disease in chronic SIV infection. J Exp Med 204(9):2171–2185

    PubMed  CAS  PubMed Central  Google Scholar 

  52. Hazenberg MD, Otto SA, Van-Benthem BHB, Roos MTL, Coutinho RA, Lange JMA et al (2003) Persistent immune activation in HIV-1 infection is associated with progression to AIDS. AIDS 17(13):1881–1888

    PubMed  Google Scholar 

  53. Sachsenberg N, Perelson AS, Yerly S, Schockmel GA, Leduc D, Hirschel B et al (1998) Turnover of CD4+ and CD8+ T lymphocytes in HIV-1 infection as measured by Ki-67 antigen. J Exp Med 187(8):1295–1303

    PubMed  CAS  PubMed Central  Google Scholar 

  54. Ribeiro RM, Mohri H, Ho DD, Perelson AS (2002) In vivo dynamics of T cell activation, proliferation, and death in HIV-1 infection: why are CD4+ but not CD8+ T cells depleted? Proc Natl Acad Sci U S A 99(24):15572–15577

    PubMed  CAS  PubMed Central  Google Scholar 

  55. Banda NK, Bernier J, Kurahara DK, Kurrle R, Haigwood N, Sekaly RP et al (1992) Crosslinking CD4 by human immunodeficiency virus gp120 primes T cells for activation-induced apoptosis. J Exp Med 176(4):1099–1106

    PubMed  CAS  Google Scholar 

  56. Groux H, Torpier G, Monté D, Mouton Y, Capron A, Ameisen JC (1992) Activation-induced death by apoptosis in CD4+ T cells from human immunodeficiency virus-infected asymptomatic individuals. J Exp Med 175(2):331–340

    PubMed  CAS  Google Scholar 

  57. Doitsh G, Cavrois M, Lassen KG, Zepeda O, Yang Z, Santiago ML et al (2010) Abortive HIV infection mediates CD4 T cell depletion and inflammation in human lymphoid tissue. Cell 143(5):789–801 (Elsevier Ltd)

    PubMed  CAS  PubMed Central  Google Scholar 

  58. Cooper A, García M, Petrovas C, Yamamoto T, Koup RA, Nabel GJ (2013) HIV-1 causes CD4 cell death through DNA-dependent protein kinase during viral integration. Nature 498(7454):376–379

    PubMed  CAS  Google Scholar 

  59. Ascher MS, Sheppard HW (1988) AIDS as immune system activation: a model for pathogenesis. Clin Exp Immunol 73(2):165–167

    PubMed  CAS  PubMed Central  Google Scholar 

  60. Giorgi JV, Hultin LE, McKeating JA, Johnson TD, Owens B, Jacobson LP 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(4):859–870

    PubMed  CAS  Google Scholar 

  61. Giorgi JV, Lyles RH, Matud JL, Yamashita TE, Mellors JW, Hultin LE 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(4):346–355

    PubMed  Google Scholar 

  62. Hazenberg MD, Stuart JWTC, Otto SA, Borleffs JCC, Charles AB, Boucher CAB et al (2000) 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) T-cell division in human immunodeficiency virus. Blood 95(1):249–255

    PubMed  CAS  Google Scholar 

  63. Hunt PW, Martin JN, Sinclair E, Bredt B, Hagos E, Lampiris H et al (2003) T cell activation is associated with lower CD4+ T cell gains in human immunodeficiency virus-infected patients with sustained viral suppression during antiretroviral therapy. J Infect Dis 187(10):1534–1543

    PubMed  CAS  Google Scholar 

  64. Liu Z, Cumberland WG, Hultin LE, Prince HE, Detels R, Giorgi JV (1997) Elevated CD38 antigen expression on CD8+ T cells is a stronger marker for the risk of chronic HIV disease progression to AIDS and death in the Multicenter AIDS Cohort Study than CD4+ cell count, soluble immune activation markers, or combinations of HLA-DR. J Acquir Immune Defic Syndr Hum Retrovirol 16(2):83–92

    PubMed  CAS  Google Scholar 

  65. Sandler NG, Wand H, Roque A, Law M, Nason MC, Nixon DE et al (2011) Plasma levels of soluble CD14 independently predict mortality in HIV infection. J Infect Dis 203(6):780–790

    PubMed  CAS  PubMed Central  Google Scholar 

  66. Smith MZ, Bastidas S, Karrer U, Oxenius A (2013) Impact of antigen specificity on CD4+ T cell activation in chronic HIV-1 infection. BMC Infect Dis 13:100

    PubMed  CAS  PubMed Central  Google Scholar 

  67. Querec TD, Akondy RS, Lee EK, Cao W, Nakaya HI, Teuwen D et al (2009) Systems biology approach predicts immunogenicity of the yellow fever vaccine in humans. Nat Immunol 10(1):116–125

    PubMed  CAS  PubMed Central  Google Scholar 

  68. Brenchley JM, Price DA, Schacker TW, Asher TE, Silvestri G, Rao S et al (2006) Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 12(12):1365–1371

    PubMed  CAS  Google Scholar 

  69. Bosinger SE, Li Q, Gordon SN, Klatt NR, Duan L, Xu L et al (2009) Global genomic analysis reveals rapid control of a robust innate response in SIV-infected sooty mangabeys. J Clin Invest 119(12):3556–3572

    PubMed  CAS  PubMed Central  Google Scholar 

  70. Jacquelin B, Mayau V, Targat B, Liovat A-S, Kunkel D, Petitjean G et al (2009) Nonpathogenic SIV infection of African green monkeys induces a strong but rapidly controlled type I IFN response. J Clin Invest 119(12):3544–3555

    PubMed  CAS  PubMed Central  Google Scholar 

  71. Manches O, Bhardwaj N (2009) Resolution of immune activation defines nonpathogenic SIV infection. J Clin Invest 119(12):3512–3515 (American Society for Clinical Investigation)

    PubMed  CAS  PubMed Central  Google Scholar 

  72. Bentwich Z, Kalinkovich A, Weisman Z (1995) Immune activation is a dominant factor in the pathogenesis of African AIDS. Immunol Today 16(4):187–191

    PubMed  CAS  Google Scholar 

  73. Secor WE (2012) The effects of schistosomiasis on HIV/AIDS infection, progression and transmission. Curr Opin HIV AIDS 7(3):254–259

    PubMed  CAS  Google Scholar 

  74. Mbabazi PS, Andan O, Fitzgerald DW, Chitsulo L, Engels D, Downs JA (2011) Examining the relationship between urogenital schistosomiasis and HIV infection. PLoS Negl Trop Dis 5(12):e1396

    PubMed  PubMed Central  Google Scholar 

  75. Kjetland EF, Ndhlovu PD, Gomo E, Mduluza T, Midzi N, Gwanzura L et al (2006) Association between genital schistosomiasis and HIV in rural Zimbabwean women. AIDS 20(4):593–600

    PubMed  Google Scholar 

  76. Downs JA, Mguta C, Kaatano GM, Mitchell KB, Bang H, Simplice H et al (2011) Urogenital schistosomiasis in women of reproductive age in Tanzania’s Lake Victoria region. Am J Trop Med Hyg 84(3):364–369

    PubMed  PubMed Central  Google Scholar 

  77. Siddappa NB, Hemashettar G, Shanmuganathan V, Semenya AA, Sweeney ED, Paul KS et al (2011) Schistosoma mansoni enhances host susceptibility to mucosal but not intravenous challenge by R5 Clade C SHIV. PLoS Negl Trop Dis 5(8):e1270

    PubMed  PubMed Central  Google Scholar 

  78. Chenine A-L, Shai-Kobiler E, Steele LN, Ong H, Augostini P, Song R et al (2008) Acute Schistosoma mansoni infection increases susceptibility to systemic SHIV clade C infection in rhesus macaques after mucosal virus exposure. PLoS Negl Trop Dis 2(7):e265

    PubMed  PubMed Central  Google Scholar 

  79. Chenine AL, Siddappa NB, Kramer VG, Sciaranghella G, Rasmussen RA, Lee SJ et al (2010) Relative transmissibility of an R5 clade C simian-human immunodeficiency virus across different mucosae in macaques parallels the relative risks of sexual HIV-1 transmission in humans via different routes. J Infect Dis 201(8):1155–1163

    PubMed  CAS  PubMed Central  Google Scholar 

  80. McElroy MD, Elrefaei M, Jones N, Ssali F, Mugyenyi P, Barugahare B et al (2005) Coinfection with Schistosoma mansoni is associated with decreased HIV-specific cytolysis and increased IL-10 production. J Immunol 174(8):5119–5123

    PubMed  CAS  Google Scholar 

  81. Kallestrup P, Zinyama R, Gomo E, Butterworth AE, Mudenge B, Dam GJ van et al (2005) Schistosomiasis and HIV-1 infection in rural Zimbabwe: effect of treatment of schistosomiasis on CD4 cell count and plasma HIV-1 RNA load. J Infect Dis 192(11):1956–1961

    PubMed  CAS  Google Scholar 

  82. Lawn SD, Karanja DM, Mwinzia P, Andove J, Colley DG, Folks TM et al (2000) The effect of treatment of schistosomiasis on blood plasma HIV-1 RNA concentration in coinfected individuals. AIDS 14(16):2437–2443

    PubMed  CAS  Google Scholar 

  83. Brown M, Kizza M, Watera C, Quigley MA, Rowland S, Hughes P et al (2004) Helminth infection is not associated with faster progression of HIV disease in coinfected adults in Uganda. J Infect Dis 190(10):1869–1879

    PubMed  Google Scholar 

  84. Brown M, Mawa PA, Joseph S, Bukusuba J, Watera C, Whitworth JAG et al (2005) Treatment of Schistosoma mansoni infection increases helminth-specific type 2 cytokine responses and HIV-1 loads in coinfected Ugandan adults. J Infect Dis 191(10):1648–1657

    PubMed  CAS  Google Scholar 

  85. Karanja DM, Colley DG, Nahlen BL, Ouma JH, Secor WE (1997) Studies on schistosomiasis in western Kenya: I. Evidence for immune-facilitated excretion of schistosome eggs from patients with Schistosoma mansoni and human immunodeficiency virus coinfections. Am J Trop Med Hyg 56(5):515–521

    PubMed  CAS  Google Scholar 

  86. Doenhoff MJ (1998) Granulomatous inflammation and the transmission of infection: schistosomiasis—and TB too? Immunol Today 19(10):462–467

    PubMed  CAS  Google Scholar 

  87. Davies SJ, Grogan JL, Blank RB, Lim KC, Locksley RM, McKerrow JH (2001) Modulation of blood fluke development in the liver by hepatic CD4+ lymphocytes. Science 294(5545):1358–1361

    PubMed  CAS  Google Scholar 

  88. Kjetland EF, Kurewa EN, Ndhlovu PD, Midzi N, Gwanzura L, Mason PR et al (2008) Female genital schistosomiasis—a differential diagnosis to sexually transmitted disease: genital itch and vaginal discharge as indicators of genital Schistosoma haematobium morbidity in a cross-sectional study in endemic rural Zimbabwe. Trop Med Int Health 13(12):1509–1517

    PubMed  Google Scholar 

  89. Ndeffo Mbah ML, Kjetland EF, Atkins KE, Poolman EM, Orenstein EW, Meyers LA et al (2013) Cost-effectiveness of a community-based intervention for reducing the transmission of Schistosoma haematobium and HIV in Africa. Proc Natl Acad Sci U S A 110(19):7952–7957

    PubMed  CAS  PubMed Central  Google Scholar 

  90. Webb EL, Ekii AO, Pala P (2012) Epidemiology and immunology of helminth-HIV interactions. Curr Opin HIV AIDS 7(3):245–253

    PubMed  CAS  Google Scholar 

  91. Walson JL, Herrin BR, John-Stewart G (2009) Deworming helminth co-infected individuals for delaying HIV disease progression. Cochrane Database Syst Rev (3):CD006419

    Google Scholar 

  92. Alexander PE, De P (2009) HIV-1 and intestinal helminth review update: updating a Cochrane review and building the case for treatment and has the time come to test and treat? Parasite Immunol 31(6):283–286

    PubMed  CAS  Google Scholar 

  93. Modjarrad K, Vermund SH (2010) Effect of treating co-infections on HIV-1 viral load: a systematic review. Lancet Infect Dis 10(7):455–463

    PubMed  PubMed Central  Google Scholar 

  94. Webb EL, Kyosiimire-Lugemwa J, Kizito D, Nkurunziza P, Lule S, Muhangi L et al (2012) The effect of anthelmintic treatment during pregnancy on HIV plasma viral load: results from a randomized, double-blind, placebo-controlled trial in Uganda. J Acquir Immune Defic Syndr 60(3):307–313

    PubMed  CAS  PubMed Central  Google Scholar 

  95. Sangaré LR, Herrin BR, John-Stewart G, Walson JL (2011) Species-specific treatment effects of helminth/HIV-1 co-infection: a systematic review and meta-analysis. Parasitology 138(12):1546–1558

    PubMed  PubMed Central  Google Scholar 

  96. Walson J, Singa B, Sangaré L, Naulikha J, Piper B, Richardson B et al (2012) Empiric deworming to delay HIV disease progression in adults with HIV who are ineligible for initiation of antiretroviral treatment (the HEAT study): a multi-site, randomised trial. Lancet Infect Dis 12(12):925–932

    PubMed  Google Scholar 

  97. Card CM, McLaren PJ, Wachihi C, Kimani J, Plummer FA, Fowke KR (2009) Decreased immune activation in resistance to HIV-1 infection is associated with an elevated frequency of CD4+CD25+FOXP3+ regulatory T cells. J Infect Dis 199(9):1318–1322 (Oxford University Press)

    PubMed  Google Scholar 

  98. Koning FA, Otto SA, Hazenberg MD, Dekker L, Prins M, Miedema F et al (2005) Low-level CD4+ T cell activation is associated with low susceptibility to HIV-1 infection. J Immunol 175:6117–6122

    PubMed  CAS  Google Scholar 

  99. Bégaud E, Chartier L, Marechal V, Ipero J, Léal J, Versmisse P et al (2006) Reduced CD4 T cell activation and in vitro susceptibility to HIV-1 infection in exposed uninfected Central Africans. Retrovirology 3:35

    PubMed  PubMed Central  Google Scholar 

  100. Vatakis DN, Bristol G, Wilkinson TA, Chow SA, Zack JA (2007) Immediate activation fails to rescue efficient human immunodeficiency virus replication in quiescent CD4+ T cells. J Virol 81(7):3574–3582

    PubMed  CAS  PubMed Central  Google Scholar 

  101. Kalinkovich A, Weisman Z, Greenberg Z, Nahmias J, Eitan S, Stein M et al (1998) Decreased CD4 and increased CD8 counts with T cell activation is associated with chronic helminth infection. Clin Exp Immunol 114(3):414–421

    PubMed  CAS  PubMed Central  Google Scholar 

  102. Kalinkovich A, Borkow G, Weisman Z, Tsimanis A, Stein M, Bentwich Z (2001) Increased CCR5 and CXCR4 expression in Ethiopians living in Israel: environmental and constitutive factors. Clin Immunol 100(1):107–117

    PubMed  CAS  Google Scholar 

  103. Chachage M, Podola L, Clowes P, Nsojo A, Bauer A, Mgaya O et al (2014) Helminth-associated systemic immune activation and HIV co-receptor expression: response to Albendazole/Praziquantel treatment. PLoS Negl Trop Dis 8(3):e2755

    Google Scholar 

  104. Canary LA, Vinton CL, Morcock DR, Pierce JB, Estes JD, Brenchley JM et al (2013) Rate of AIDS progression is associated with gastrointestinal dysfunction in simian immunodeficiency virus-infected pigtail macaques. J Immunol 190(6):2959–2965

    PubMed  CAS  PubMed Central  Google Scholar 

  105. Marchetti G, Tincati C, Silvestri G (2013) Microbial translocation in the pathogenesis of HIV infection and AIDS. Clin Microbiol Rev 26(1):2–18

    PubMed  CAS  PubMed Central  Google Scholar 

  106. Estes JD, Harris LD, Klatt NR, Tabb B, Pittaluga S, Paiardini M et al (2010) Damaged intestinal epithelial integrity linked to microbial translocation in pathogenic simian immunodeficiency virus infections. PLoS Pathog 6(8):e1001052

    PubMed  PubMed Central  Google Scholar 

  107. Raffatellu M, Santos RL, Verhoeven DE, George MD, Wilson RP, Winter SE et al (2008) Simian immunodeficiency virus-induced mucosal interleukin-17 deficiency promotes Salmonella dissemination from the gut. Nat Med 14(4):421–428

    PubMed  CAS  PubMed Central  Google Scholar 

  108. Cecchinato V, Franchini G (2010) Th17 cells in pathogenic simian immunodeficiency virus infection of macaques. Curr Opin HIV AIDS 5(2):141–145

    PubMed  PubMed Central  Google Scholar 

  109. Acosta-Rodriguez EV, Rivino L, Geginat J, Jarrossay D, Gattorno M, Lanzavecchia A et al (2007) Surface phenotype and antigenic specificity of human interleukin 17-producing T helper memory cells. Nat Immunol 8(6):639–646

    PubMed  CAS  Google Scholar 

  110. Annunziato F, Cosmi L, Santarlasci V, Maggi L, Liotta F, Mazzinghi B et al (2007) Phenotypic and functional features of human Th17 cells. J Exp Med 204(8):1849–1861

    PubMed  CAS  PubMed Central  Google Scholar 

  111. Brenchley JM, Price DA, Douek DC (2006) HIV disease: fallout from a mucosal catastrophe? Nat Immunol 7(3):235–239

    PubMed  CAS  Google Scholar 

  112. Onguru D, Liang Y, Griffith Q, Nikolajczyk B, Mwinzi P, Ganley-Leal L (2011) Human schistosomiasis is associated with endotoxemia and Toll-like receptor 2- and 4-bearing B cells. Am J Trop Med Hyg 84(2):321–324

    PubMed  CAS  PubMed Central  Google Scholar 

  113. George PJ, Anuradha R, Kumar NP, Kumaraswami V, Nutman TB, Babu S (2012) Evidence of microbial translocation associated with perturbations in T cell and antigen-presenting cell homeostasis in hookworm infections. PLoS Negl Trop Dis 6(10):e1830

    PubMed  PubMed Central  Google Scholar 

  114. Broadhurst MJ, Ardeshir A, Kanwar B, Mirpuri J, Gundra UM, Leung JM et al (2012) Therapeutic helminth infection of macaques with idiopathic chronic diarrhea alters the inflammatory signature and mucosal microbiota of the colon. PLoS Pathog 8(11):e1003000

    PubMed  CAS  PubMed Central  Google Scholar 

  115. Brown KN, Trichel A, Barratt-Boyes SM (2007) Parallel loss of myeloid and plasmacytoid dendritic cells from blood and lymphoid tissue in simian AIDS. J Immunol 178(11):6958–6967

    PubMed  CAS  Google Scholar 

  116. Brown KN, Wijewardana V, Liu X, Barratt-Boyes SM (2009) Rapid influx and death of plasmacytoid dendritic cells in lymph nodes mediate depletion in acute simian immunodeficiency virus infection. PLoS Pathog 5(5):e1000413

    PubMed  PubMed Central  Google Scholar 

  117. Champagne P, Ogg GS, King AS, Knabenhans C, Ellefsen K, Nobile M et al (2001) Skewed maturation of memory HIV-specific CD8 T lymphocytes. Nature 410(6824):106–111

    PubMed  CAS  Google Scholar 

  118. Maizels RM, Yazdanbakhsh M (2003) Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat Rev Immunol 3(9):733–744

    PubMed  CAS  Google Scholar 

  119. Maizels RM, Hewitson JP, Smith KA (2012) Susceptibility and immunity to helminth parasites. Curr Opin Immunol 24(4):459–466

    PubMed  CAS  PubMed Central  Google Scholar 

  120. Horsnell WGC, Cutler AJ, Hoving JC, Hoving CJ, Mearns H, Myburgh E et al (2007) Delayed goblet cell hyperplasia, acetylcholine receptor expression, and worm expulsion in SMC-specific IL-4Ralpha-deficient mice. PLoS Pathog 3(1):e1

    PubMed  PubMed Central  Google Scholar 

  121. Barner M, Mohrs M, Brombacher F, Kopf M (1998) Differences between IL-4R alpha-deficient and IL-4-deficient mice reveal a role for IL-13 in the regulation of Th2 responses. Curr Biol 8(11):669–672

    PubMed  CAS  Google Scholar 

  122. Urban JF, Noben-Trauth N, Donaldson DD, Madden KB, Morris SC, Collins M et al (1998) IL-13, IL-4Ralpha, and Stat6 are required for the expulsion of the gastrointestinal nematode parasite Nippostrongylus brasiliensis. Immunity 8(2):255–264

    PubMed  CAS  Google Scholar 

  123. Gaze S, McSorley HJ, Daveson J, Jones D, Bethony JM, Oliveira LM et al (2012) Characterising the mucosal and systemic immune responses to experimental human hookworm infection. PLoS Pathog 8(2):e1002520

    PubMed  CAS  PubMed Central  Google Scholar 

  124. Maggi E, Mazzetti M, Ravina A, Annunziato F, de Carli M, Piccinni MP et al (1994) Ability of HIV to promote a TH1 to TH0 shift and to replicate preferentially in TH2 and TH0 cells. Science 265(5169):244–248

    PubMed  CAS  Google Scholar 

  125. Mikovits JA, Taub DD, Turcovski-Corrales SM, Ruscetti FW (1998) Similar levels of human immunodeficiency virus type 1 replication in human TH1 and TH2 clones. J Virol 72(6):5231–5238

    PubMed  CAS  PubMed Central  Google Scholar 

  126. Vicenzi E, Bordignon PP, Biswas P, Brambilla A, Bovolenta C, Cota M et al (1999) Envelope-dependent restriction of human immunodeficiency virus type 1 spreading in CD4+ T lymphocytes: R5 but not X4 viruses replicate in the absence of T-cell receptor restimulation. J Virol 73(9):7515–7523

    PubMed  CAS  PubMed Central  Google Scholar 

  127. Accornero P, Radrizzani M, Delia D, Gerosa F, Kurrle R, Colombo MP (1997) Differential susceptibility to HIV-GP120-sensitized apoptosis in CD4+ T-cell clones with different T-helper phenotypes: role of CD95/CD95L interactions. Blood 89(2):558–569

    PubMed  CAS  Google Scholar 

  128. Klein SA, Dobmeyer JM, Dobmeyer TS, Pape M, Ottmann OG, Helm EB et al (1997) Demonstration of the Th1 to Th2 cytokine shift during the course of HIV-1 infection using cytoplasmic cytokine detection on single cell level by flow cytometry. AIDS 11(9):1111–1118

    PubMed  CAS  Google Scholar 

  129. Gopinath R, Ostrowski M, Justement SJ, Fauci AS, Nutman TB (2000) Filarial infections increase susceptibility to human immunodeficiency virus infection in peripheral blood mononuclear cells in vitro. J Infect Dis 182(6):1804–1808

    PubMed  CAS  Google Scholar 

  130. Mwinzi PN, Karanja DM, Colley DG, Orago AS, Secor WE (2001) Cellular immune responses of schistosomiasis patients are altered by human immunodeficiency virus type 1 coinfection. J Infect Dis 184(4):488–496

    PubMed  CAS  Google Scholar 

  131. Mkhize-Kwitshana ZL, Taylor M, Jooste P, Mabaso ML, Walzl G (2011) The influence of different helminth infection phenotypes on immune responses against HIV in co-infected adults in South Africa. BMC Infect Dis 11(1):273 (BioMed Central Ltd)

    PubMed  CAS  PubMed Central  Google Scholar 

  132. Bava AJ, Troncoso AR (2009) Strongyloides stercoralis hyperinfection in a patient with AIDS. J Int Assoc 8(4):235–238 (Physicians AIDS Care (Chic))

    Google Scholar 

  133. Jaka H, Koy M, Egan JP, Meda JR, Mirambo M, Mazigo HD et al (2013) Strongyloides stercoralis infection presenting as an unusual cause of massive upper gastrointestinal bleeding in an immunosuppressed patient: a case report. Trop Doct 43(1):46–48

    PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Cellular Immunology, National Institute for Medical Research-Mbeya Medical Research Centre (NIMR-MMRC), Hospital Hill road, Mbeya, Tanzania

    Dr. (PhD) Mkunde Chachage PhD, BSc(Hons), Bsc

  2. Division of Infectious Diseases and Tropical Medicine, Medical center of the University of Munish (LMU), 80799, Munich, Germany

    Dr. rer. nat. Christof Geldmacher

  3. German Center for Infection Research (DZIF), partner site Munich, Germany

    Dr. rer. nat. Christof Geldmacher

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  1. Dr. (PhD) Mkunde Chachage PhD, BSc(Hons), Bsc
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  2. Dr. rer. nat. Christof Geldmacher
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Correspondence to Mkunde Chachage PhD, BSc(Hons), Bsc .

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  1. Division of Immunology/IIDM, University of Cape Town, Cape Town, South Africa

    William Horsnell

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Chachage, M., Geldmacher, C. (2014). Immune System Modulation by Helminth Infections: Potential Impact on HIV Transmission and Disease Progression. In: Horsnell, W. (eds) How Helminths Alter Immunity to Infection. Advances in Experimental Medicine and Biology, vol 828. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-1489-0_6

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