CD4+ T cells mediate mucosal and systemic immune responses to experimental hookworm infection

Parasite Immunology

Volumn 32, Issue 6, 2010, Pages 406-413

  Dondji, B ^a,c   Sun, T ^a   Bungiro, R D ^b   Vermeire, J J ^a   Harrison, L M ^a   Bifulco, C ^a,d   Cappello, M ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BROWN UNIVERSITY   (United States)

^c CENTRAL WASHINGTON UNIVERSITY   (United States)

^d PROVIDENCE PORTLAND MEDICAL CENTER   (United States)

Author keywords

Ancylostoma ceylanicum; Anemia; CD4+ T cells; Hookworm; Nematode

Indexed keywords

CD4 IMMUNOGLOBULIN; IMMUNOGLOBULIN G;

ANCYLOSTOMA CEYLANICUM; ANEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; HOOKWORM INFECTION; HUMORAL IMMUNITY; IMMUNE RESPONSE; INTESTINE FLORA; MUCOSAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; T CELL DEPLETION;

ANCYLOSTOMA; ANCYLOSTOMIASIS; ANEMIA; ANIMALS; ANTIBODIES, HELMINTH; ANTIBODIES, MONOCLONAL; CD4-POSITIVE T-LYMPHOCYTES; CRICETINAE; IMMUNITY, MUCOSAL; INTESTINES; LYMPHOCYTE DEPLETION; MESOCRICETUS;

ANCYLOSTOMA; ANCYLOSTOMA CEYLANICUM; ANCYLOSTOMATOIDEA; ANIMALIA; CRICETINAE; MESOCRICETUS AURATUS; MURINAE;

EID: 77952245064     PISSN: 01419838     EISSN: 13653024     Source Type: Journal    
DOI: 10.1111/j.1365-3024.2010.01204.x     Document Type: Article

References (48)

1. Geiger SM, Massara CL, Bethony J, Soboslay PT Correa-Oliveira R. Cellular responses and cytokine production in post-treatment hookworm patients from an endemic area in Brazil. Clin Exp Immunol 2004 136 : 334 340.
2. Onyemelukwe GC Musa BO. T-lymphocyte subsets in patients with hookworm infection in Zaria, Nigeria. Afr J Med Med Sci 2001 30 : 255 259.
3. Borkow G, Teicher C Bentwich Z. Helminth-HIV coinfection: should we deworm? PLoS Negl Trop Dis 2007 1 : e160.
4. Walson JL. Treatment of helminth co-infection in individuals with HIV-1: a systematic review of the literature. PLoS Negl Trop Dis 2007 1 : e102.
5. Cooper PJ, Chico M, Sandoval C, et al. Human infection with Ascaris lumbricoides is associated with suppression of the interleukin-2 response to recombinant cholera toxin B subunit following vaccination with the live oral cholera vaccine CVD 103-HgR. Infect Immun 2001 69 : 1574 1580.
6. Dondji B, Bungiro RD, Harrison LM, et al. Role for nitric oxide in hookworm-associated immune suppression. Infect Immun 2008 76 : 2560 2567.
7. Jenson JS, O'Connor R, Osborne J Devaney E. Infection with Brugia microfilariae induces apoptosis of CD4(+) T lymphocytes: a mechanism of immune unresponsiveness in filariasis. Eur J Immunol 2002 32 : 858 867.
8. Geiger SM, Caldas IR, Mc Glone BE, et al. Stage-specific immune responses in human Necator americanus infection. Parasite Immunol 2007 29 : 347 358.
9. Bancroft AJ, Grencis RK, Else KJ Devaney E. The role of CD4 cells in protective immunity to Brugia pahangi. Parasite Immunol 1994 16 : 385 387.
10. Koyama K, Tamauchi H Ito Y. The role of CD4+ and CD8+ T cells in protective immunity to the murine nematode parasite Trichuris muris. Parasite Immunol 1995 17 : 161 165.
11. Vickery AC, Vincent AL, Sodeman WA, Jr. Effect of immune reconstitution on resistance to Brugia pahangi in congenitally athymic nude mice. J Parasitol 1983 69 : 478 485.
12. Doetze A, Satoguina J, Burchard G, et al. Antigen-specific cellular hyporesponsiveness in a chronic human helminth infection is mediated by T(h)3/T(r)1-type cytokines IL-10 and transforming growth factor-beta but not by a T(h)1 to T(h)2 shift. Int Immunol 2000 12 : 623 630.
13. McKee AS Pearce EJ. CD25+CD4+ cells contribute to Th2 polarization during helminth infection by suppressing Th1 response development. J Immunol 2004 173 : 1224 1231.
14. Beiting DP, Gagliardo LF, Hesse M, Bliss SK, Meskill D Appleton JA. Coordinated control of immunity to muscle stage Trichinella spiralis by IL-10, regulatory T cells, and TGF-beta. J Immunol 2007 178 : 1039 1047.
15. Taylor MD, LeGoff L, Harris A, Malone E, Allen JE Maizels RM. Removal of regulatory T cell activity reverses hyporesponsiveness and leads to filarial parasite clearance in vivo. J Immunol 2005 174 : 4924 4933.
16. Held MR, Bungiro RD, Harrison LM, Hamza I Cappello M. Dietary iron content mediates hookworm pathogenesis in vivo. Infect Immun 2006 74 : 289 295.
17. Bungiro RD, Jr., Greene J, Kruglov E Cappello M. Mitigation of hookworm disease by immunization with soluble extracts of Ancylostoma ceylanicum. J Infect Dis 2001 183 : 1380 1387.
18. DuChateau BK, Jensen JR, England DM, Callister SM, Lovrich SD Schell RF. Macrophages and enriched populations of T lymphocytes interact synergistically for the induction of severe, destructive Lyme arthritis. Infect Immun 1997 65 : 2829 2836.
19. DuChateau BK, Munson EL, England DM, et al. Macrophages interact with enriched populations of distinct T lymphocyte subsets for the induction of severe destructive Lyme arthritis. J Leukoc Biol 1999 65 : 162 170.
20. Bungiro RD, Jr., Sun T, Harrison LM, Shoemaker CB Cappello M. Mucosal antibody responses in experimental hookworm infection. Parasite Immunol 2008 30 : 293 303.
21. Bungiro RD, Jr., Solis CV, Harrison LM Cappello M. Purification and molecular cloning of and immunization with Ancylostoma ceylanicum excretory-secretory protein 2, an immunoreactive protein produced by adult hookworms. Infect Immun 2004 72 : 2203 2213.
22. Bungiro RD, Harrison LM Cappello M. Ancylostoma ceylanicum excretory/secretory protein 1: purification and molecular cloning of a major secretory protein from adult hookworms. Mol Biochem Parasitol 2002 119 : 147 151.
23. Cox FE Liew EY. Centrefold: T-cell subsets and cytokines in parasitic infections. Parasitol Today 1992 8 : 371 374.
24. Scott P Kaufmann SH. The role of T-cell subsets and cytokines in the regulation of infection. Immunol Today 1991 12 : 346 348.
25. Urban JF, Jr., Schopf L, Morris SC, et al. Stat6 signaling promotes protective immunity against Trichinella spiralis through a mast cell- and T cell-dependent mechanism. J Immunol 2000 164 : 2046 2052.
26. Grencis RK, Lee TD Wakelin D. Adoptive transfer of immunity to Trichinella spiralis in mice: generation of effective cells by different life cycle stages. Int J Parasitol 1985 15 : 195 202.
27. Grencis RK, Riedlinger J Wakelin D. L3T4-positive T lymphoblasts are responsible for transfer of immunity to Trichinella spiralis in mice. Immunology 1985 56 : 213 218. (Pubitemid 15231394)
28. Riedlinger J, Grencis RK Wakelin D. Antigen-specific T-cell lines transfer protective immunity against Trichinella spiralis in vivo. Immunology 1986 58 : 57 61.
29. Phillips SM, Lin JJ, Galal N, Tung AS, Linette GP Perrin PJ. Resistance in murine schistosomiasis is contingent on activated IL-2 receptor-bearing L3T4+ lymphocytes, negatively regulated by Lyt-2+ cells, and uninfluenced by the presence of IL-4. J Immunol 1991 146 : 1335 1340.
30. Katona IM, Urban JF, Jr. Finkelman FD. The role of L3T4+ and Lyt-2+ T cells in the IgE response and immunity to Nippostrongylus brasiliensis. J Immunol 1988 140 : 3206 3211.
31. Katona IM, Urban JF Jr, Kang SS, Paul WE Finkelman FD. IL-4 requirements for the generation of secondary in vivo IgE responses. J Immunol 1991 146 : 4215 4221.
32. Garside P Behnke JM. Ancylostoma ceylanicum in the hamster: observations on the host-parasite relationship during primary infection. Parasitology 1989 98 (Pt 2 283 289.
33. Garside P, Behnke JM Rose RA. The immune response of male DSN hamsters to a primary infection with Ancylostoma ceylanicum. J Helminthol 1989 63 : 251 260.
34. Chowdhury AB Schad GA. Ancylostoma ceylanicum: a parasite of man in Calcutta and environs. Am J Trop Med Hyg 1972 21 : 300 301.
35. Areekul S, Radomyos P Viravan C. Experimental infection of Ancylostoma ceylanicum in man. J Med Assoc Thai 1970 53 : 190 194.
36. Velasquez CC Cabrera BC. Ancylostoma ceylanicum (Looss, 1911) in a Filipino woman. J Parasitol 1968 54 : 430 431.
37. Yoshida Y, Okamoto K Chiu JK. Ancylostoma ceylanicum infection in dogs, cats, and man in Taiwan. Am J Trop Med Hyg 1968 17 : 378 381.
38. Suss G, Eichmann K, Kury E, Linke A Langhorne J. Roles of CD4- and CD8-bearing T lymphocytes in the immune response to the erythrocytic stages of Plasmodium chabaudi. Infect Immun 1988 56 : 3081 3088.
39. Lim LC, England DM, Glowacki NJ, DuChateau BK Schell RF. Involvement of CD4+ T lymphocytes in induction of severe destructive Lyme arthritis in inbred LSH hamsters. Infect Immun 1995 63 : 4818 4825.
40. Mendez S, Valenzuela JG, Wu W Hotez PJ. Host cytokine production, lymphoproliferation, and antibody responses during the course of Ancylostoma ceylanicum infection in the Golden Syrian hamster. Infect Immun 2005 73 : 3402 3407.
41. Ekkens MJ, Liu Z, Liu Q, et al. The role of OX40 ligand interactions in the development of the Th2 response to the gastrointestinal nematode parasite Heligmosomoides polygyrus. J Immunol 2003 170 : 384 393.
42. Bungiro RD, Jr. Cappello M. Detection of excretory/secretory coproantigens in experimental hookworm infection. Am J Trop Med Hyg 2005 73 : 915 920.
43. Chu D, Bungiro RD, Ibanez M, et al. Molecular characterization of Ancylostoma ceylanicum Kunitz-type serine protease inhibitor: evidence for a role in hookworm-associated growth delay. Infect Immun 2004 72 : 2214 2221.
44. Mendez S, Zhan B, Goud G, et al. Effect of combining the larval antigens Ancylostoma secreted protein 2 (ASP-2) and metalloprotease 1 (MTP-1) in protecting hamsters against hookworm infection and disease caused by Ancylostoma ceylanicum. Vaccine 2005 23 : 3123 3130.
45. Hotez PJ, Molyneux DH, Fenwick A, et al. Control of neglected tropical diseases. N Engl J Med 2007 357 : 1018 1027.
46. Bundy D, Sher A Michael E. Good worms or bad worms: do worm infections affect the epidemiological patterns of other diseases? Parasitol Today 2000 16 : 273 274.
47. Walson JL, Otieno PA, Mbuchi M, et al. Albendazole treatment of HIV-1 and helminth co-infection: a randomized, double-blind, placebo-controlled trial. AIDS 2008 22 : 1601 1609.
48. Bachur TP, Vale JM, Coelho IC, Queiroz TR Chaves Cde S. Enteric parasitic infections in HIV/AIDS patients before and after the highly active antiretroviral therapy. Braz J Infect Dis 2008 12 : 115 122.