Host immune response to Cryptosporidium parvum infection

Experimental Parasitology

Volumn 126, Issue 3, 2010, Pages 304-309

  Petry, Franz ^a   Jakobi, Vera ^a   Tessema, Tesfaye S ^a  

^a UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

Author keywords

Apicomplexa; Cryptosporidium parvum; Immune response

Indexed keywords

BETA DEFENSIN 2; GAMMA INTERFERON; IMMUNOGLOBULIN A ANTIBODY; INTERLEUKIN 12; INTERLEUKIN 18; INTERLEUKIN 4; INTERLEUKIN 5; MANNAN BINDING LECTIN; NITRIC OXIDE; COMPLEMENT; CYTOKINE; PROTOZOON ANTIBODY;

ADAPTIVE IMMUNITY; ANTIBODY PRODUCTION; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; COMPLEMENT SYSTEM; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM PARVUM; DENDRITIC CELL; FOOD CONTAMINATION; HELPER CELL; HOST PARASITE INTERACTION; HUMAN; IMMUNE DEFICIENCY; IMMUNE RESPONSE; INNATE IMMUNITY; INTERFERON PRODUCTION; INTESTINE EPITHELIUM CELL; NATURAL KILLER CELL; NONHUMAN; PARASITE TRANSMISSION; PHAGOCYTE; PRIORITY JOURNAL; REVIEW; TH2 CELL; AIDS RELATED COMPLEX; ANIMAL; BIOSYNTHESIS; DISEASE MODEL; IMMUNOCOMPETENCE; IMMUNOCOMPROMISED PATIENT; IMMUNOLOGY; INTESTINE MUCOSA; MOUSE; PARASITOLOGY; T LYMPHOCYTE;

ADAPTIVE IMMUNITY; AIDS-RELATED OPPORTUNISTIC INFECTIONS; ANIMALS; ANTIBODIES, PROTOZOAN; B-LYMPHOCYTES; COMPLEMENT SYSTEM PROTEINS; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM PARVUM; CYTOKINES; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; HUMANS; IMMUNITY, INNATE; IMMUNOCOMPETENCE; IMMUNOCOMPROMISED HOST; INTESTINAL MUCOSA; KILLER CELLS, NATURAL; MICE; NITRIC OXIDE; PHAGOCYTES; T-LYMPHOCYTES;

ANIMALIA; APICOMPLEXA; CRYPTOSPORIDIUM; CRYPTOSPORIDIUM HOMINIS; CRYPTOSPORIDIUM PARVUM; PROTOZOA;

EID: 77956249827     PISSN: 00144894     EISSN: 10902449     Source Type: Journal    
DOI: 10.1016/j.exppara.2010.05.022     Document Type: Review

References (87)

1. Abrahamsen M.S., Lancto C.A., Walcheck B., Layton W., Jutila M.A. Localization of α/β and γ/δ T lymphocytes in Cryptosporidium parvum-infected tissues in naive and immune calves. Infection and Immunity 1997, 65:2428-2433.
2. Aguirre S.A., Mason P.H., Perryman L.E. Susceptibility of major histocompatibility complex (MHC) class I- and MHC class II-deficient mice to Cryptosporidium parvum infection. Infection and Immunity 1994, 62:697-699.
3. + αβ+IL-4+ lymphocytes in gut-associated lymphoid tissue during resolution of infection. Journal of Immunology 1998, 161:1891-1900.
4. Appay V., Zaunders J.J., Papagno L., Sutton J., Jaramillo A., Waters A., Easterbrook P., Grey P., Smith D., McMichael A.J., Cooper D.A., Rowland-Jones S.L., Kelleher A.D. Characterization of CD4(+) CTLs ex vivo. Journal of Immunology 2002, 168:5954-5958.
5. Auray G., Lacroix-Lamande S., Mancassola R., Dimier-Poisson I., Laurent F. Involvement of intestinal epithelial cells in dendritic cell recruitment during C. parvum infection. Microbes and Infection 2007, 9:574-582.
6. Barakat F.M., McDonald V., Di Santo J.P., Korbel D.S. Roles for NK cells and an NK cell-independent source of intestinal gamma interferon for innate immunity to Cryptosporidium parvum infection. Infection and Immunity 2009, 77:5044-5049.
7. Barakat F.M., McDonald V., Foster G.R., Tovey M.G., Korbel D.S. Cryptosporidium parvum infection rapidly induces a protective innate immune response involving type I interferon. Journal of Infectious Diseases 2009, 200:1548-1555.
8. Brombacher F., Kastelein R.A., Alber G. Novel IL-12 family members shed light on the orchestration of Th1 responses. Trends in Immunology 2003, 24:207-212.
9. Brown D.M., Dilzer A.M., Meents D.L., Swain S.L. CD4 T cell-mediated protection from lethal influenza: perforin and antibody-mediated mechanisms give a one-two punch. Journal of Immunology 2006, 177:2888-2898.
10. Campbell L.D., Stewart J.N., Mead J.R. Susceptibility to Cryptosporidium parvum infections in cytokine- and chemokine-receptor knockout mice. Journal of Parasitology 2002, 88:1014-1016.
11. Carmolli M., Duggal P., Haque R., Lindow J., Mondal D., Petri W.A., Mourningstar P., Larsson C.J., Sreenivasan M., Khan S., Kirkpatrick B.D. Deficient serum mannose-binding lectin levels and MBL2 polymorphisms increase the risk of single and recurrent Cryptosporidium infections in young children. Journal of Infectious Diseases 2009, 200:1540-1547.
12. Chardes T., Buzoni-Gatel D., Lepage A., Bernard F., Bout D. Toxoplasma gondii oral infection induces specific cytotoxic CD8 α/β+ Thy-1+ gut intraepithelial lymphocytes, lytic for parasite-infected enterocytes. Journal of Immunology 1994, 153:4596-4603.
13. Chen W., Harp J.A., Harmsen A.G. Cryptosporidium parvum infection in gene-targeted B cell-deficient mice. Journal of Parasitology 2003, 89:391-393.
14. + cells and gamma interferon in resolution of established Cryptosporidium parvum infection in mice. Infection and Immunity 1993, 61:3928-3932.
15. Chen W., Harp J.A., Harmsen A.G., Havell E.A. Gamma interferon functions in resistance to Cryptosporidium parvum infection in severe combined immunodeficient mice. Infection and Immunity 1993, 61:3548-3551.
16. Clavel A., Arnal A.C., Sánchez E.C., Cuesta J., Letona S., Amiguet J.A., Castillo F.J., Varea M., Gómez-Lus R. Respiratory cryptosporidiosis: case series and review of the literature. Infection 1996, 24:341-346.
17. Cozon G., Biron F., Jeannin M., Cannella D., Revillard J.P. Secretory IgA antibodies to Cryptosporidium parvum in AIDS patients with chronic cryptosporidiosis. Journal of Infectious Diseases 1994, 169:696-699.
18. Crabb J.H. Antibody-based immunotherapy of cryptosporidiosis. Opportunistic Protozoa in Humans 1998, 121-149. Academic Press, San Diego. S. Tzipori (Ed.).
19. Current W.L., Garcia L.S. Cryptosporidiosis. Clinical and Microbiological Reviews 1991, 4:325-358.
20. Ehigiator H.N., McNair N., Mead J.R. Cryptosporidium parvum: The contribution of Th1-inducing pathways to the resolution of infection in mice. Experimental Parasitology 2007, 115:107-113.
21. Ehigiator H.N., Romagnoli P., Borgelt K., Fernandez M., McNair N., Secor W.E., Mead J.R. Mucosal cytokine and antigen-specific responses to Cryptosporidium parvum in IL-12p40 KO mice. Parasite Immunology 2005, 27:17-28.
22. + TH1- and TH2-cell-secreted cytokines in cryptosporidiosis. Folia Parasitologica. Praha 1993, 40:307-311.
23. Flanigan T., Whalen C., Turner J., Soave R., Toerner J., Havlir D., Kotler D. Cryptosporidium infection and CD4 counts. Annals of Internal Medicine 1992, 116:840-842.
24. Fritz J.H., Ferrero R.L., Philpott D.J., Girardin S.E. Nod-like proteins in immunity, inflammation and disease. Nature Immunology 2006, 7:1250-1257.
25. Gookin J.L., Chiang S., Allen J., Armstrong M.U., Stauffer S.H., Finnegan C., Murtaugh M.P. NF-kappaB-mediated expression of iNOS promotes epithelial defense against infection by Cryptosporidium parvum in neonatal piglets. American Journal of Physiology - Gastrointestinal and Liver Physiology 2006, 290:G164-G174.
26. Gookin J.L., Duckett L.L., Armstrong M.U., Stauffer S.H., Finnegan C.P., Murtaugh M.P., Argenzio R.A. Nitric oxide synthase stimulates prostaglandin synthesis and barrier function in C. parvum-infected porcine ileum. American Journal of Physiology - Gastrointestinal and Liver Physiology 2004, 287:G571-G581.
27. + cells in response to Cryptosporidium parvum antigen. Journal of Parasitology 1994, 80:67-72.
28. Hayward A.R., Cosyns M., Jones M., Ponnuraj E.M. Marrow-Derived CD40-positive cells are required for mice to clear Cryptosporidium parvum infection. Infection and Immunity 2001, 69:1630-1634.
29. Heine J., Moon H.W., Woodmansee D.B. Persistent Cryptosporidium infection in congenitally athymic (nude) mice. Infection and Immunity 1984, 43:856-859.
30. Hershberg R.M., Mayer L.F. Antigen processing and presentation by intestinal epithelial cells-polarity and complexity. Immunology Today 2000, 21:123-128.
31. Hill B.D., Blewett D.A., Dawson A.M., Wright S. Analysis of the kinetics, isotype and specificity of serum and coproantibody in lambs infected with Cryptosporidium parvum. Research in Veterinary Science 1990, 48:76-81.
32. Huang D.S., Lopez M.C., Wang J.Y., Martinez F., Watson R.R. Alterations of the mucosal immune system due to Cryptosporidium parvum infection in normal mice. Cellular Immunology 1996, 173:176-182.
33. Huang K., Yang S. Inhibitory effect of selenium on Cryptosporidium parvum infection in vitro and in vivo. Biological Trace Element Research 2002, 90:261-272.
34. Jakobi V., Petry F. Humoral immune response in interleukin-12 and interferon-γ deficient mice after infection with Cryptosporidium parvum. Parasite Immunology 2008, 30:151-161.
35. Jellison E.R., Kim S.K., Welsh R.M. Cutting edge: MHC class II-restricted killing in vivo during viral infection. Journal of Immunology 2005, 174:614-618.
36. Jenkins M.C., O'Brien C., Trout J., Guidry A., Fayer R. Hyperimmune bovine colostrum specific for recombinant Cryptosporidium parvum antigen confers partial protection against cryptosporidiosis in immunosuppressed adult mice. Vaccine 1999, 17:2453-2460.
37. Kapel N., Benhamou Y., Buraud M., Magne D., Opolon P., Gobert J.G. Kinetics of mucosal ileal γ-interferon response during cryptosporidiosis in immunocompetent neonatal mice. Parasitology Research 1996, 82:664-667.
38. Kelly P., Jack D.L., Naeem A., Mandanda B., Pollok R.C., Klein N.J., Turner M.W., Farthing M.J. Mannose-binding lectin is a component of innate mucosal defense against Cryptosporidium parvum in AIDS. Gastroenterology 2000, 119:1236-1242.
39. Kirkpatrick B.D., Huston C.D., Wagner D., Noel F., Rouzier P., Pape J.W., Bois G., Larsson C.J., Alston W.K., Tenney K., Powden C., O'Neill J.P., Sears C.L. Serum mannose-binding lectin deficiency is associated with cryptosporidiosis in young Haitian children. Clinical Infectious Diseases 2006, 43:289-294.
40. Kuhls T.L., Greenfield R.A., Mosier D.A., Crawford D.L., Joyce W.A. Cryptosporidiosis in adult and neonatal mice with severe combined immunodeficiency. Journal of Comparative Pathology 1992, 106:399-410.
41. Lacroix S., Mancassola R., Naciri M., Laurent F. Cryptosporidium parvum-specific mucosal immune response in C57BL/6 neonatal and gamma interferon-deficient mice. role of tumor necrosis factor alpha in protection. Infection and Immunity 2001, 69:1635-1642.
42. Lacroix-Lamande S., Mancassola R., Naciri M., Laurent F. Role of gamma interferon in chemokine expression in the ileum of mice and in a murine intestinal epithelial cell line after Cryptosporidium parvum infection. Infection and Immunity 2002, 70:2090-2099.
43. Lean I.S., Lacroix-Lamande S., Laurent F., McDonald V. Role of tumor necrosis factor alpha in development of immunity against Cryptosporidium parvum infection. Infection and Immunity 2006, 74:4379-4382.
44. Lean I.S., McDonald V., Pollok R.C. The role of cytokines in the pathogenesis of Cryptosporidium infection. Current Opinion in Infectious Diseases 2002, 15:229-234.
45. Leitch G.J., He Q. Reactive nitrogen and oxygen species ameliorate experimental cryptosporidiosis in the neonatal BALB/c mouse model. Infection and Immunity 1999, 67:5885-5891.
46. Leitch G.J., He Q. Arginine-derived nitric oxide reduces fecal oocyst shedding in nude mice infected with Cryptosporidium parvum. Infection and Immunity 1994, 62:5173-5176.
47. Loos M., Clas F. Antibody-independent killing of gram-negative bacteria via the classical pathway of complement. Immunology Letters 1987, 14:203-208.
48. Magalhaes J.G., Tattoli I., Girardin S.E. The intestinal epithelial barrier: how to distinguish between the microbial flora and pathogens. Seminars in Immunology 2007, 19:106-115.
49. Maillot C., Gargala G., Delaunay A., Ducrotte P., Brasseur P., Ballet J.J., Favennec L. Cryptosporidium parvum infection stimulates the secretion of TGF-β, IL-8 and RANTES by Caco-2 cell line. Parasitology Research 2000, 86:947-949.
50. McDonald S.A.C., O'Grady J.E., Bajaj-Elliott M., Notley C.A., Alexander J., Brombacher F., McDonald V. Protection against the early acute phase of Cryptosporidium parvum infection conferred by interleukin-4-induced expression of T helper 1 cytokines. Journal of Infectious Diseases 2004, 190:1019-1025.
51. McDonald V. Host cell-mediated responses to infection with Cryptosporidium. Parasite Immunology 2000, 22:597-604.
52. McDonald V., Bancroft G.J. Mechanisms of innate and acquired resistance to Cryptosporidium parvum infection in SCID mice. Parasite Immunology 1994, 16:315-320.
53. McDonald V., Deer R., Uni S., Iseki M., Bancroft G.J. Immune responses to Cryptosporidium muris and Cryptosporidium parvum in adult immunocompetent or immunocompromised (nude and SCID) mice. Infection and Immunity 1992, 60:3325-3331.
54. McDonald V., Pollok R.C., Dhaliwal W., Naik S., Farthing M.J., Bajaj-Elliott M. A potential role for interleukin-18 in inhibition of the development of Cryptosporidium parvum. Clinical and Experimental Immunology 2006, 145:555-562.
55. Mead J.R., Arrowood M.J., Healey M.C., Sidwell R.W. Cryptosporidial infections in SCID mice reconstituted with human or murine lymphocytes. Journal of Protozoology 1991, 38:59S-61S.
56. Mead J.R., You X. Susceptibility differences to Cryptosporidium parvum infection in two strains of gamma interferon knockout mice. Journal of Parasitology 1998, 84:1045-1048.
57. Mosmann T.R., Cherwinski H., Bond M.W., Giedlin M.A., Coffman R.L. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. Journal of Immunology 1986, 136:2348-2357.
58. Nakanishi K., Yoshimoto T., Tsutsui H., Okamura H. Interleukin-18 regulates both Th1 and Th2 responses. Annual Review of Immunology 2001, 19:423-474.
59. Nathan C., Shiloh M.U. Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proceedings of the National Academy of Sciences 2000, 97:8841-8848.
60. Nikiforow S., Bottomly K., Miller G., Munz C. Cytolytic CD4(+)-T-cell clones reactive to EBNA1 inhibit Epstein-Barr virus-induced B-cell proliferation. Journal of Virology 2003, 77:12088-12104.
61. Okazawa A., Kanai T., Nakamaru K., Sato T., Inoue N., Ogata H., Iwao Y., Ikeda M., Kawamura T., Makita S., Uraushihara K., Okamoto R., Yamazaki M., Kurimoto M., Ishii H., Watanabe M., Hibi T. Human intestinal epithelial cell-derived interleukin (IL)-18, along with IL-2, IL-7 and IL-15, is a potent synergistic factor for the proliferation of intraepithelial lymphocytes. Clinical and Experimental Immunology 2004, 136:269-276.
62. Pasquali P., Fayer R., Zarlenga D., Canals A., Marez T., Gomez Munoz M.T., Almeria S., Gasbarre L.C. Recombinant bovine interleukin-12 stimulates a gut immune response but does not provide resistance to Cryptosporidium parvum infection in neonatal calves. Veterinary Parasitology 2006, 135:259-268.
63. Peeters J.E., Villacorta I., Vanopdenbosch E., Vandergheynst D., Naciri M., Ares Mazas E., Yvore P. Cryptosporidium parvum in calves: kinetics and immunoblot analysis of specific serum and local antibody responses (immunoglobulin A [IgA], IgG, and IgM) after natural and experimental infections. Infection and Immunity 1992, 60:2309-2316.
64. Perryman L.E., Kapil S.J., Jones M.L., Hunt E.L. Protection of calves against cryptosporidiosis with immune bovine colostrum induced by a Cryptosporidium parvum recombinant protein. Vaccine 1999, 17:2142-2149.
65. Perryman L.E., Mason P.H., Chrisp C.E. Effect of spleen cell populations on resolution of Cryptosporidium parvum infection in SCID mice. Infection and Immunity 1994, 62:1474-1477.
66. Petry F., Jakobi V., Wagner S., Tessema T.S., Thiel S., Loos M. Binding and activation of human and mouse complement by Cryptosporidium parvum (Apicomplexa) and susceptibility of C1q- and MBL-deficient mice to infection. Molecular Immunology 2008, 45:3392-3400.
67. Petry F., Loos M. Bacteria and complement. The Human Complement System in Health and Disease 1998, 375-392. Marcel Dekker Inc., New York. J.E. Volanakis, M.M. Frank (Eds.).
68. Pollok R.C., Farthing M.J., Bajaj-Elliott M., Sanderson I.R., McDonald V. Interferon gamma induces enterocyte resistance against infection by the intracellular pathogen Cryptosporidium parvum. Gastroenterology 2001, 120:99-107.
69. Reperant J.M., Naciri M., Iochmann S., Tilley M., Bout D.T. Major antigens of Cryptosporidium parvum recognised by serum antibodies from different infected animal species and man. Veterinary Parasitology 1994, 55:1-13.
70. Robinson P., Okhuysen P.C., Chappell C.L., Lewis D.E., Shahab I., Janecki A., White A.C. Expression of tumor necrosis factor alpha and interleukin 1β in jejuna of volunteers after experimental challenge with Cryptosporidium parvum correlates with exposure but not with symptoms. Infection and Immunity 2001, 69:1172-1174.
71. Rohlman V.C., Kuhls T.L., Mosier D.A., Crawford D.L., Greenfield R.A. Cryptosporidium parvum infection after abrogation of natural killer cell activity in normal and severe combined immunodeficiency mice. Journal of Parasitology 1993, 79:295-297.
72. Seydel K.B., Zhang T., Champion G.A., Fichtenbaum C., Swanson P.E., Tzipori S., Griffiths J.K., Stanley S.L. Cryptosporidium parvum infection of human intestinal xenografts in SCID mice induces production of human tumor necrosis factor alpha and interleukin-8. Infection and Immunity 1998, 66:2379-2382.
73. Singh I., Theodos C., Li W., Tzipori S. Kinetics of Cryptosporidium parvum-specific cytokine responses in healing and nonhealing murine models of C. parvum infection. Parasitology Research 2005, 97:309-317.
74. Smith L.M., Bonafonte M.T., Campbell L.D., Mead J.R. Exogenous interleukin-12 (IL-12) exacerbates Cryptosporidium parvum infection in gamma interferon knockout mice. Experimental Parasitology 2001, 98:123-133.
75. Smith L.M., Bonafonte M.T., Mead J.R. Cytokine expression and specific lymphocyte proliferation in two strains of Cryptosporidium parvum-infected gamma-interferon knockout mice. Journal of Parasitology 2000, 86:300-307.
76. Takeuchi D., Jones V.C., Kobayashi M., Suzuki F. Cooperative role of macrophages and neutrophils in host antiprotozoan resistance in mice acutely infected with Cryptosporidium parvum. Infection and Immunity 2008, 76:3657-3663.
77. Tessema T.S., Schwamb B., Lochner M., Forster I., Jakobi V., Petry F. Dynamics of gut mucosal and systemic Th1/Th2 cytokine responses in interferon-γ and interleukin-12p40 knock out mice during primary and challenge Cryptosporidium parvum infection. Immunobiology 2009, 214:454-466.
78. + T lymphocytes in protective immunity. Journal of Immunology 1991, 147:1014-1022.
79. Ungar B.L., Soave R., Fayer R., Nash T.E. Enzyme immunoassay detection of immunoglobulin M and G antibodies to Cryptosporidium in immunocompetent and immunocompromised persons. Journal of Infectious Diseases 1986, 153:570-578.
80. Urban J.F., Fayer R., Chen S.J., Gause W.C., Gately M.K., Finkelman F.D. IL-12 protects immunocompetent and immunodeficient neonatal mice against infection with Cryptosporidium parvum. Journal of Immunology 1996, 156:263-268.
81. Wagner S., Lynch N.J., Walter W., Schwaeble W.J., Loos M. Differential expression of the murine mannose-binding lectins A and C in lymphoid and nonlymphoid organs and tissues. Journal of Immunology 2003, 170:1462-1465.
82. Wang H.C., Dann S.M., Okhuysen P.C., Lewis D.E., Chappell C.L., Adler D.G., White A.C. High levels of CXCL10 are produced by intestinal epithelial cells in AIDS patients with active cryptosporidiosis but not after reconstitution of immunity. Infection and Immunity 2007, 75:481-487.
83. White A.C., Cron S.G., Chappell C.L. Paromomycin in cryptosporidiosis. Clinical Infectious Diseases 2001, 32:1516-1517.
84. Williams R.O., Burden D.J. Measurement of class specific antibody against cryptosporidium in serum and faeces from experimentally infected calves. Research in Veterinary Science 1987, 43:264-265.
85. Wyatt C.R., Brackett E.J., Savidge J. Evidence for the emergence of a type-1-like immune response in intestinal mucosa of calves recovering from cryptosporidiosis. Journal of Parasitology 2001, 87:90-95.
86. Yassien N.A., Khalifa E.A., el-Nouby K.A. Role of anti-oxidant preparation (oxi-guard) on Cryptosporidium parvum infection in albino mice. Journal of Egyptian Society of Parasitology 2001, 31:95-106.
87. Zaalouk T.K., Bajaj-Elliott M., George J.T., McDonald V. Differential regulation of β-defensin gene expression during Cryptosporidium parvum infection. Infection and Immunity 2004, 72:2772-2779.