Molecular basis of Trypanosoma cruzi and Leishmania interaction with their host(s): Exploitation of immune and defense mechanisms by the parasite leading to persistence and chronicity, features reminiscent of immune system evasion strategies in cancer diseases

Archivum Immunologiae et Therapiae Experimentalis

Volumn 53, Issue 2, 2005, Pages 102-114

  Ouaissi, Ali ^a   Ouaissi, Mehdi ^b  

^a INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

^b HÔPITAL SAINTE MARGUERITE   (France)

Author keywords

Cancer cells; Immunoregulation; Trypanosomatids; Virulence factors

Indexed keywords

VIRULENCE FACTOR;

CANCER IMMUNOLOGY; CELL ACTIVATION; CELLULAR IMMUNITY; CYTOKINE RELEASE; DEFENSE MECHANISM; HOST CELL; HOST PARASITE INTERACTION; HUMORAL IMMUNITY; IMMUNE SYSTEM; IMMUNOREGULATION; LEISHMANIA; NONHUMAN; PARASITE IMMUNITY; REVIEW; TRYPANOSOMA CRUZI;

ANIMALS; ANTIGENS, PROTOZOAN; APOPTOSIS; CHAGAS DISEASE; COMPLEMENT SYSTEM PROTEINS; CYTOKINES; HOST-PARASITE RELATIONS; HUMANS; LEISHMANIA; LEISHMANIASIS; LYMPHOCYTE ACTIVATION; MODELS, IMMUNOLOGICAL; NEOPLASMS; NITRIC OXIDE; TRYPANOSOMA CRUZI;

EID: 23044488575     PISSN: 0004069X     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (92)

1. Abrahamshon I. A. and Coffman R. L. (1995): Cytokine and nitric oxide regulation of the immunosuppression in Trypanosoma cruzi infection. J. Immunol., 155, 3955-3963.
2. Aga E., Katschinski M. D., Zandbergen G. V., Laufs H., Hansen B., Muller K., Solbach W. and Laskay T. (2002): Inhibition of the spontaneous apoptosis of neutrophil granulocytes by the intracellular parasite Leishmania major. J. Immunol., 169, 898-905.
3. Allaoui A., Francois C., Zemzoumi K. Guilvard E. and Ouaissi A. (1999): In vitro and in vivo decreased infectivity and alteration of metacyclogenesis process of Trypanosoma cruzi carrying a targeted deletion of a Tc52 protein encoding allele. Mol. Microbiol., 32, 1273-1286.
4. Ameisen J. C., Idziorek T., Billaut-Multo O., Loyens M., Yissier J. P., Potentier A. and Ouaissi A. (1996): Apoptosis in a unicellular eukaryote (Trypanosoma cruzi): implications for the evolutionary origin and role of programmed cell death in the control of cell proliferation, differentiation and survival. Parasitol. Today, 12, 49.
5. Araujo-Jorge T. C., Lage M. J. F., Rivera M. T., Carlier Y. and Van Leuven F. (1992): Trypanosoma cruzi: enhanced alpha-macroglobin levels correlate with the resistance of BALB/cj mice to acute infection. Parasitol. Res., 78, 215-221.
6. Arend W. P., Malyak M., Smith M. F. Jr., Whisenand T. D., Slack J. L., Sims J. E., Giri J. G. and Dower S. K. (1994): Binding of IL-1alpha, IL-1beta, and IL-1 receptor antagonist by soluble IL-1 receptors and levels of soluble IL-1 receptors in synovial fluids. J. Immunol., 153, 4766-4774.
7. Barros H.C., Da Silva S., Verbisck N. V., Araguth M. F., Tedesco R. C., Procopio D. O. and Mortara R. A. (1996): Release of membrane-bound trails by Trypanosoma cruzi amastigotes onto modified surfaces and mammalian cells. J. Eukaryot. Microbiol., 43, 275-285.
8. Bast R. C., Klein S., Inbar M. et al. (1983): Tumor cell membrane vesicles block T cell mediated cytotoxicity and TS1 suppressor cells. Fed. Proc., 42, 1081-1087.
9. Bohme M. W., Evans D. A., Miles M. A. and Holborow E. J. (1986): Occurrence of autoantibodies to intermediate filament proteins in human visceral leishmaniasis and their induction by experimental polyclonal B-cell activation. Immunology, 59, 583-588.
10. Borges M., Cordeiro da Silva A. C., Sereno D. and Ouaissi A. (2003): Peptide-based analysis of the amino acid sequence important to the immunoregulatory function of Trypanosoma cruzi Tc52 virulence factor. Immunology, 109, 147-155.
11. Borges M., Guilvard E., Cordeiro da Silva A., Vergnes B., Zemzoumi K. and Ouaissi A. (2001): Endogenous Trypanosoma cruzi Tc52 protein expression upregulates the growth of murine macrophages and fibroblasts and cytokine gene expression. Immunol. Lett., 78, 127-134.
12. Brener Z. (1980): Immunity to Trypanosoma cruzi. Adv. Parasitol., 18, 247-292.
13. Buates S. and Matlashewski G. (2001): General suppression of macrophage gene expression during Leishmania donovani infection. J. Immunol., 166, 3416-3422.
14. Bunn-Moreno M. M., Madeira E. D., Miller K., Menezes J. A. and Campos-Neto A. (1985): Hypergammaglobulinaemia in Leishmania donovani infected hamsters: possible association with a polyclonal activator of B cells and with suppression of T cell function. Clin. Exp. Immunol., 59, 427-434.
15. Campos M. A., Almeida I. C., Takeuchi O., Akira S., Valente E. P., Procopio D. O., Travassos L. R., Smith J. A., Golenbock D. T. and Gazzinelli R. T. (2001): Activation of Toll-like receptor-2 by glycosylphosphatidylinositol anchors from a protozoan parasite. J. Immunol., 167, 416-423.
16. Capron A. and Dessaint J. P. (1989): Molecular basis of host-parasite relationship: towards the definition of protective antigens. Immunl. Rev., 112, 27-48.
17. Carvalho E. M., Bacellar O., Barral A., Badaro R. and Johnson W. D. Jr. (1989): Antigen-specific immunosuppression in visceral leishmaniasis is cell mediated. J. Clin. Invest., 83, 860-864.
18. Chang R. H., Feng M. H., Liu W. H. and Lai M. Z. (1997): Nitric oxide increased interleukin-4 expression in T lymphocytes. Immunology, 90, 364-369.
19. Chess Q., Acosta A. M., Sethi J. K. and Santos-Buch C. A. (1983): Reversible acquisition of a host cell surface membrane antigen by Trypanosoma cruzi. Infect. Immun., 40, 299-302.
20. Chuenkova M. V., Furnari F. B., Cavenee W. K. and Pereira M. A. (2001): Trypanosoma cruzi trans-sialidase: a potent specific survival factor for human Schwann cells by means of phosphatidylinositol 3-kinase/Akt signaling. Proc. Natl. Acad. Sci. USA, 98, 9936-9941.
21. Chuenkova M. V. and Pereira M. A. (2000): A trypanosomal protein synergizes with the cytokines ciliary neurotrophic factor and leukemia inhibitory factor to prevent apoptosis of neuronal cells. Mol. Biol. Cell, 11, 1487-1498.
22. Cohen E. P. (1980): Antigenic modulation and down regulation- their similarities suggest they may have a common origin. Cancer Biochem. Biophys., 4, 237-243.
23. Cordeiro-Da-Silva A., Borges M. C., Guilvard E. and Ouaissi A. (2001): Dual role of the Leishmania major ribosomal protein S3a homologue in regulation of T- and B-cell activation. Infect. Immun., 69, 6588-6596.
24. Cordeiro-da-Silva A., Cardoso L., Arujo N., Castro H., Tomas A., Rodrigues M., Cabral M., Vergnes B., Sereno D. and Ouaissi A. (2003): Identification of antibodies to Leishmania silent information regulatory 2 (SIR2) protein homologue during canine natural infections: pathological implications. Immunol. Lett., 86, 155-162.
25. Curtin J. F. and Cotter T. G. (2003): Live and let die: regulatory mechanisms in Fas-mediated apoptosis. Cell Signal, 15, 983-992.
26. Da Silva A., Espinoza A. G., Taibi A., Ouaissi A. and Minoprio P. (1998): A 24,000 MW Trypanosoma cruzi antigen is a B-cell activator. Immunology, 94, 189-196.
27. Dinarello C. A. (1993): Modalities for reducing interleukin-1 activity in disease. Trends Pharmacol. Sci., 14, 155-159.
28. Dinarello C. A. and Wolff S. M. (1993): The role of interleukin-1 in disease. N. Engl. J. Med., 328, 106-113.
29. Ding L. and Shevach E. M. (1992): IL-10 inhibits mitogen-induced T cell proliferation by selectively inhibiting macrophage costimulatory function. J. Immunol., 148, 3133-3139.
30. Edbrook M. R., Parker D., McVey J. H., Riley J. H., Sorenson G. D., Pettengill O. S. and Craig R. K. (1985): Expression of the human calcitonin/CGRP gene in lung and thyroid cancer. EMBO J., 4, 715-724.
31. Fernandez-Gomez R., Esteban S., Gomez-Corvera R., Zoulika K. and Ouaissi A. (1998): Trypanosoma cruzi: Tc52 released protein-induced increased expression of nitric oxide and nitric oxide production by macrophages. J. Immunol., 160, 3471-3479.
32. Ferreira S. H. (1993): The role of interleukins and nitric oxide in the mediation of inflammatory pain and its control by peripheral analgesics. Drugs, 46 (suppl. 1), 1-9.
33. Fiorentino D. F., Zlotnik A., Vieira P., Mosmann T. R., Howard M., Moore K. W. and O'Garra A. (1991): IL-10 acts on the antigen-presenting cell to inhibit cytokine production by Th1. J. Immunol., 146, 3444-3451.
34. Fischer E., Ouaissi M. A., Velge P., Cornette J. and Kazatchkine M. D. (1988): gp 58/68, a parasite component that contributes to the escape of the trypomastigote form of T. cruzi from damage by the human alternative complement pathway. Immunology, 65, 299-303.
35. Fuhram S. A. and Joiner K. A. (1989): Complement evasion by parasites. Exp. Parasitol., 68, 474-481.
36. Garzón E., Borges M. C., Cordeiro-da-Silva A., Nacife V., Meirelles Mde N., Guilvard E., Bosseno M. F., Guevara A. G., Breniere S. F. and Ouaissi A. (2003): Trypanosoma cruzi carrying a targeted deletion of a Tc52 protein-encoding allele elicits attenuated Chagas' disease in mice. Immunol. Lett., 89, 67-80.
37. Grimaldi G. Jr. and Tesh R. B. (1993): Leishmaniases of the New World: current concepts and implications for future research. Clin. Microbiol. Rev., 6, 230-250.
38. Hall B. F. and Joiner K. A. (1991): Strategies of obligate intracellular parasites for evading host defences. Parasitol. Today, 12, A22-A27.
39. Hand P. H., Nuti M., Colcher D. and Schlom J. (1983): Definition of antigenic heterogeneity and modulation among human mammary carcinoma cell populations using monoclonal antibodies to tumor-associated antigens. Cancer Res., 43, 728-735.
40. Hayashi S., Chan C. C., Gazzinelli R. and Roberge F. G. (1996): Contribution of nitric oxide to the host parasite equilibrium in toxoplasmosis. J. Immunol., 156, 1476-1481.
41. Hermoso T., Fishelson Z., Becker S. I., Hirschberg K. and Jaffe C. L. (1991): Leishmanial protein kinases phosphorylate components of the complement system. EMBO J., 10, 4061-4067.
42. Hill J. R., Corbett J. A., Kwon G., Marshall C. A. and McDaniel M. L. (1996): Nitric oxide regulates interleukin 1 bioactivity released from murine macrophages. J. Biol. Chem., 271, 22672-22678.
43. Höppener J. W., Steebergh P. H., Slebos R. J., Visser A., Lips C. J., Jansz H. S., Bechet J. M., Lenoir G. M., Born W., Haller-Brem S. et al. (1987): Expression of the second calcitonin/calcitonin gene-related peptide gene in Ewing sarcoma cell lines. J. Clin. Endocrinol. Meta., 64, 809-817.
44. James S. L. (1995): Role of nitric oxide in parasitic infections. Microbiol. Rev., 59, 533-547.
45. Joiner K. Rimoldi M. T. Kipnis T. et al. (1987): Trypomastigotes of Trypanosoma cruzi produce molecules which accelerate the decay of complement C3 convertases. Complement, 4, 175 (abstract).
46. Kahn S. J. and Wleklinski M. (1997): The surface glycoproteins of Trypanosoma cruzi encode a superfamily of variant T cell epitopes. J. Immunol., 159, 4444-4451.
47. Kedzierski L., Montgomery J., Bullen D., Curtis J., Gardiner E., Jimenez-Ruiz A. and Handman E. (2004): A leucin-rich repeat motif of Leishmania parasite surface antigen 2 binds to macrophages through the complement receptor 3. J. Immunol., 172, 4902-4906.
48. Kwan W. C., McMaster W. R., Wong N. and Reiner N. E. (1992): Inhibition of expression of major histocompatibility class II molecules in macrophages infected with Leishmania donovani occurs at the level of gene transcription via a cyclic AMP-independent mechanism. Infect. Immun., 60, 2115-2120.
49. Leblanc B., Parodi A. L., Lagadic M. Hurtrel M. and Jobit C. (1991): Immunocytochemistry of thyroid tumors. Vet. Pathol., 28, 370-380.
50. Leguizamon M. S., Mocetti E., Garcia Rivello H., Argibay P. and Campetella O. (1999): Trans-sialidase from Trypanosoma cruzi induces apoptosis in cells from the immune system in vivo. J. Infect. Dis., 180, 1398-1402.
51. Liew F. Y. (1995): Interactions between cytokines and nitric oxide. Adv. Neuroimmunol., 5, 201-209.
52. Mirjalili A., Alimohammadian M. H. and Madani R. (2003): Presence of immunoglobulin on the surface of lesion-derived amastigotes of Leishmania major as a tool for isolation of amastigote stage from BALB/c mice. Iranian Biomed. J., 7, 155-160.
53. Moncayo A. (1993): Chagas' disease. Eleventh Programme Report WHO, Geneva, pp 67-75.
54. Monti P., Leone B. E., Zerbi A., Balzano G., Cainarca S., Sordi V., Pontillo M., Mercalli A., Di Carlo V., Allavena P. and Piemonti L. (2004): Tumor-derived MUC1 mucins interact with differentiating monocytes and induce IL-10highIL-121ow regulatory dendritic cell. J. Immunol., 172, 7341-7349.
55. Moore K. J. and Mallashewski G. (1994): Intracellular infection by Leishmania donovani inhibits macrophage apoptosis. J. Immunol., 152, 2930-2937.
56. Munoz-Fernandez M., Fernandez M. A. and Fresno M. (1992): Activation of human macrophages for the killing of intracellular Trypanosoma cruzi by TNF-alpha and IFN-gamma through a nitric oxide-dependent mechanism. Immunol. Lett., 33, 35-40.
57. Murray H. W. (1988): Interferon-gamma, the activated macrophage and host defence against microbial challenge. Ann. Intern. Med., 108, 595-608.
58. Nandan D., Yi T., Lopez M., Lai C. and Reiner N. E. (2002): Leishmania EF-1alpha activates the Src homology domain containing tyrosine phosphatase SHP-1 leading to macrophage deactivation. J. Biol. Chem., 277, 50190-50197.
59. Nitz N., Gomes C., de Cassia Rosa A., D'Souza-Ault M. R., Moreno F., Lauria-Pires L., Nascimento R. J. and Teixeira A. R. (2004): Heritable integration of kDNA minicircle sequences from Trypanosoma cruzi into the avian genome: insights into human Chagas' disease. Cell, 118, 175-186.
60. Norris K. A. (1998): Stable transfection of Trypanosoma cruzi epimastigotes with the trypomastigote-specific complement regulatory protein cDNA confers complement resistance. Infect. Immun., 66, 2460-2465.
61. Norris K. A., Bradt B., Cooper N. R. and So, M. (1991): Characterization of a Trypanosoma cruzi C3 binding protein with functional and genetic similarities to the complement regulatory protein, decay-accelerating factor. J. Immunol., 147, 2240-2247.
62. Norris K. A., Harth G. and So M. (1989): Purification of a Trypanosoma cruzi membrane glycoprotein which elicits lytic antibodies. Infect. Immun., 57, 2372-2377.
63. Norris K. A. and Schrimpf J. E. (1994): Biochemical analysis of the membrane and soluble forms of the complement regulatory protein of Trypanosoma cruzi. Infect. Immun., 62, 236-243.
64. Ouaissi A., Aguirre T., Plumas-Marty B., Piras M., Schoneck R., Gras-Masse H., Taibi A., Loyens M., Tartar A., Capron A. et al. (1992): Cloning and sequencing of a 24-kDa Trypanosoma cruzi specific antigen released in association with membrane vesicles and defined by a monoclonal antibody. Biol. Cell, 75, 11-17.
65. Ouaissi A., Guevara-Espinoza A., Chabe F., Gomez-Corvera R. and Taibi A. (1995): A novel and basic mechanism of immunosuppression in Chagas' disease: Trypanosoma cruzi releases in vitro and in vivo a protein which induces T cells unresponsiveness through specific interaction with cysteine and glutathione. Immunol. Lett., 48, 221-224.
66. Ouaissi A., Guilvard E., Delneste Y., Caron G., Magistrelli G., Herbault N., Thieblemont N. and Jeannin P. (2002): The Trypanosoma cruzi Tc52-released protein induces human dendritic cell maturation, signals via Toll-like receptor 2, and confers protection against lethal infection. J. Immunol., 168, 6366-6374.
67. Ouaissi A., Ouaissi M. and Sereno D. (2002): Glutathione S-transferases and related proteins from pathogenic human parasites behave as immunomodulatory factors. Immunol. Lett., 81, 159-164.
68. Ouaissi M. A., Afchain D., Capron A. and Grimaud J. A. (1984): Fibronectin receptors on Trypanosoma cruzi trypomastigotes and their biological function. Nature, 308, 380-382.
69. Ouaissi M. A., Cornette J., Afchain D., Capron A., Gras-Masse H. and Tartar A. (1986): Trypanosoma cruzi infection inhibited by peptides modeled from a fibronectin cell attachment domain. Science, 234, 603-607.
70. Ouaissi M. A., Da Silva A. C., Guevara A. G., Borges M. and Guilvard E. (2001): Trypanosoma crazf-induced host immune system dysfunction: a rational for parasite immunosuppressive factor(s) encoding gene targeting. J. Biomed. Biotechnol., 1, 11-17.
71. Ouaissi M. A., Dubremetz J. F., Kusnierz J. P., Cornette J., Loyens M., Taibi A., Marty B., Velge P., Rizvi F. and Capron A. (1990): Trypanosoma cruzi: differential expression and distribution of an 85-kDa polypeptide epitope by in vitro developmental stages. Exp. Parasitol., 71, 207-217.
72. Petray P., Rottenberg M. E., Grinstein S. and Orn A. (1994): Release of nitric oxide during the experimental infection with Trypanosoma cruzi. Parasite Immunol., 16, 193-199.
73. Pham B. N., Prin L., Gosset D., Hatron P. Y., Devulder B., Capron A. and Dessaint J. P. (1989): T lymphocyte activation in systemic lupus erythematous analysed by proliferative response to nucleoplasmic proteins on nitrocellulose immunoblots. Clin. Exp. Immunol., 77, 168-174.
74. Pinelli E., Rutten V. P., Bruysters M., Moore P. F. and Ruitenberg E. J. (1999): Compensation for decreased expression of B7 molecules on Leishmania infantum-infected canine macrophages results in restoration of parasite-specific T-cell proliferation and gamma interferon production. Infect. Immun., 67, 237-243.
75. Pitti R. M., Marsters S. A., Lawrence D. A., Roy M., Kischkel F. C., Dowd P., Huang A., Donahue C. J., Sherwood S. W., Baldwin D. T., Godowski P. J., Wood W. I., Gurney A. L., Hillan K. J., Cohen R. L., Goddard A. D., Botstein D. and Ashkenazi A. (1998): Genomic amplification of a decoy receptor for Fas ligand in lung and colon cancer. Nature, 396, 699-703.
76. Poutsiaka D. D., Taylor D. D. and Levy E. M. and Black P. H. (1985): Inhibition of recombinant interferon-gamma-induced 1a antigen expression by shed B16 F10 melanoma cell membrane vesicles. J. Immunol., 134, 145-150.
77. Probst P., Skeiky Y. A., Sleeves M., Gervassi A., Grabstein K. H. and Reed S. G. (1997): A Leishmania protein that modulates interleukin (IL)-12, IL-10 and tumor necrosis factor-alpha production and expression of B7-1 in human monocyte-derived antigen-presenting cells. Eur. J. Immunol., 27, 2634-2642.
78. Proudfoot L., Nikolaev A. V., Feng G. J., Wei W. Q., Ferguson M. A., Brimacombe J. S. and Liew F. Y. (1996): Regulation of the expression of nitric oxide synthase and leishmanicidal activity by glycoconjugates of Leishmania lipophosphoglycan in murine macrophages. Proc. Natl. Acad. Sci. USA, 93, 10984-10989.
79. Raz A., Goldman A., Yuli I. et al. (1978): Isolation of plasma membrane fragments and vesicles from ascites fluid of lymphoma-bearing mice and their possible role in the escape mechanism of tumors from host immune rejection. Cancer Immunol. Immunother., 4, 53-62.
80. Requena J. M., Alonso C. and Soto M. (2000): Evolutionary conserved proteins as prominent immunogens during Leishmania infections. Parasitol. Today, 16, 246-250.
81. Roth J. A., Osborne B. A. and Ames R. S. (1983): Immunoregulatory factors derived from human tumors. II. Partial purification and further immunobiochemical characterization of a human sarcoma-derived immunosuppressive factor expressing HLA-DR and immunoglobulin-related determinants. J. Immunol., 130, 303-308.
82. Soong L. and Tarleton R. L. (1994): Trypanosoma cruzi infection suppresses nuclear factors that bind to specific sites on the interleukin-2 enhancer. Eur. J. Immunol., 24, 16-22.
83. Sternberg J. M. and Mabbott N. A. (1996): Nitric oxide-mediated suppression of T cell responses during Trypanosoma brucei infection: soluble trypanosome products and interferon-gamma are synergistic inducers of nitric oxide synthase. Eur. J. Immunol., 26, 539-543.
84. Takami H., Shikata J., Kakudo K. and Ito K. (1990): Calcitonin gene-related peptide in patients with endocrin tumors. J. Surg. Oncol., 43, 28-32.
85. Takami H., Shikata J., Ozaki O., Mimura T. and Ito K. (1991): Measurement of plasma calcitonin gene-related peptide (CGRP) level in patients with thyroid disease. Nippon Geka Gakkai Zasshi, 91, 401-406.
86. Takle G. B. and Snary D. (1993): South American Trypanosomiasis (Chagas' disease). In Warren K. S (ed.): Immunology and Molecular Biology of Parasitic Infections. Third Edition. Blackwell Scientific Publications, Inc., 213-236.
87. Unanue E. R. and Allen P. M. (1987): The basis of the immunoregulatory role of macrophages and other accessory cells. Science, 236, 551-557.
88. Wang F., Millet I., Bottomly K. and Vignery A. (1992): Calcitonin gene-related peptide inhibits interleukin 2 production by murine T lymphocytes. J. Biol. Biochem., 267, 21052-21057.
89. Wang H., Xie X., Lu W. G., Ye D. F., Chen H. Z., Li X. and Cheng Q. (2004): Ovarian carcinoma cells inhibit T cell proliferation: suppression of IL-2 receptor beta and gamma expression and their JAK-STAT signalling pathway. Life Sci., 74, 1739-1749.
90. Wyler D. J., Sypek J. P. and McDonald J. A. (1985): In vitro parasite-monocyte interactions in human leishmaniasis: possible role of fibronectin in parasite attachment. Infect. Immun., 49, 305-311.
91. Yahiaoui B., Taibi A. and Ouaissi A. (1996): A Leishmania major protein with extensive homology to silent information regulator 2 of Saccharomyces cerevisiae. Gene, 169, 115-118.
92. Zemzoumi K., Guilvard E., Sereno D., Preto A., Benlemlih M., Da Silva A. C., Lemesre J. L. and Ouaissi A. (1999): Cloning of a Leishmania major gene encoding for an antigen with extensive homology to ribosomal protein S3a. Gene, 240, 57-65.