Regulatory Cells and Immunosuppressive Cytokines: 
      Parasite-Derived Factors  Induce Immune Polarization

Ouaissi, Ali

doi:https://doi.org/10.1155/2007/94971

BioMed Research International

On this page

Abstract References Copyright Related Articles

Special Issue

Immunology and Molecular Biology of Protozoan Infections

View this Special Issue

Review Article | Open Access

Volume 2007 | Article ID 094971 | https://doi.org/10.1155/2007/94971

Regulatory Cells and Immunosuppressive Cytokines: Parasite-Derived Factors Induce Immune Polarization

Ali Ouaissi¹

Academic Editor: Abdelali Haoudi

Received27 Nov 2006

Accepted19 Mar 2007

Published21 May 2007

Abstract

Parasitic infections are prevalent in both tropical and subtropical areas. Most of the affected and/or exposed populations are living in developing countries where control measures are lacking or inadequately applied. Although significant progress has been made in our understanding of the immune response to parasites, no definitive step has yet been successfully done in terms of operational vaccines against parasitic diseases. Evidence accumulated during the past few years suggests that the pathology observed during parasitic infections is in part due to deregulation of normal components of the immune system, mainly cytokines, antibodies, and immune effector cell populations. A large number of studies that illustrate how parasites can modify the host immune system for their own benefit have been reported in both metazoan and protozoan parasites. The first line of defense against foreign organisms is barrier tissue such as skin, humoral factors, for instance the complement system and pentraxin, which upon activation of the complement cascade facilitate pathogen recognition by cells of innate immunity such as macrophages and DC. However, all the major groups of parasites studied have been shown to contain and/or to release factors, which interfere with both arms of the host immune system. Even some astonishing observations relate to the production by some parasites of orthologues of mammalian cytokines. Furthermore, chronic parasitic infections have led to the immunosuppressive environment that correlates with increased levels of myeloid and T suppressor cells that may limit the success of immunotherapeutic strategies based on vaccination. This minireview briefly analyzes some of the current data related to the regulatory cells and molecules derived from parasites that affect cellular function and contribute to the polarization of the immune response of the host. Special attention is given to some of the data from our laboratory illustrating the role of immunomodulatory factors released by protozoan parasites, in the induction and perpetuation of chronic disease.

References

R. M. Maizels and M. Yazdanbakhsh, “Immune regulation by helminth parasites: cellular and molecular mechanisms,” Nature Reviews Immunology, vol. 3, no. 9, pp. 733–744, 2003.
View at: Publisher Site | Google Scholar
D. van der Kleij and M. Yazdanbakhsh, “Control of inflammatory diseases by pathogens: lipids and the immune system,” European Journal of Immunology, vol. 33, no. 11, pp. 2953–2963, 2003.
View at: Publisher Site | Google Scholar
M. Wills-Karp, J. Santeliz, and C. L. Karp, “The germless theory of allergic disease: revisiting the hygiene hypothesis,” Nature Reviews Immunology, vol. 1, no. 1, pp. 69–75, 2001.
View at: Publisher Site | Google Scholar
M. Yazdanbakhsh, P. G. Kremsner, and R. Van Ree, “Allergy, parasites, and the hygiene hypothesis,” Science, vol. 296, no. 5567, pp. 490–494, 2002.
View at: Publisher Site | Google Scholar
S. Imai and K. Fujita, “Molecules of parasites as immunomodulatory drugs,” Current Topics in Medicinal Chemistry, vol. 4, no. 5, pp. 539–552, 2004.
View at: Publisher Site | Google Scholar
D. Mason and F. Powrie, “Control of immune pathology by regulatory T cells,” Current Opinion in Immunology, vol. 10, no. 6, pp. 649–655, 1998.
View at: Publisher Site | Google Scholar
S. Sakaguchi, “Animal models of autoimmunity and their relevance to human diseases,” Current Opinion in Immunology, vol. 12, no. 6, pp. 684–690, 2000.
View at: Publisher Site | Google Scholar
E. M. Shevach, “Suppressor T cells: rebirth, function and homeostasis,” Current Biology, vol. 10, no. 15, pp. R572–R575, 2000.
View at: Publisher Site | Google Scholar
K. J. Maloy and F. Powrie, “Regulatory T cells in the control of immune pathology,” Nature Immunology, vol. 2, no. 9, pp. 816–822, 2001.
View at: Publisher Site | Google Scholar
J. A. Bluestone and A. K. Abbas, “Natural versus adaptive regulatory T cells,” Nature Reviews Immunology, vol. 3, no. 3, pp. 253–257, 2003.
View at: Publisher Site | Google Scholar
A. O'Garra and P. Vieira, “Regulatory T cells and mechanisms of immune system control,” Nature Medicine, vol. 10, no. 8, pp. 801–805, 2004.
View at: Publisher Site | Google Scholar
K. H. G. Mills, “Regulatory T cells: friend or foe in immunity to infection?” Nature Reviews Immunology, vol. 4, no. 11, pp. 841–855, 2004.
View at: Publisher Site | Google Scholar
Y. Belkaid, R. B. Blank, and I. Suffia, “Natural regulatory T cells and parasites: a common quest for host homeostasis,” Immunological Reviews, vol. 212, no. 1, pp. 287–300, 2006.
View at: Publisher Site | Google Scholar
A. Haque, A. Capron, A. Ouaissi et al., “Immune unresponsiveness and its possible relation to filarial disease,” Contributions to Microbiology and Immunology, vol. 7, pp. 9–21, 1983.
View at: Google Scholar
I. Petralanda, L. Yarzabal, and W. F. Piessens, “Parasite antigens are present in breast milk of women infected with Onchocerca volvulus,” American Journal of Tropical Medicine and Hygiene, vol. 38, no. 2, pp. 372–379, 1988.
View at: Google Scholar
M. A. Ouaissi, J. P. Dessaint, J. Cornette, I. Desmoutis, and A. Capron, “Induction of non-specific human suppressor cells in vitro by defined Onchocerca volvulus antigens,” Clinical and Experimental Immunology, vol. 53, no. 3, pp. 634–644, 1983.
View at: Google Scholar
A. Doetze, J. Satoguina, G. Burchard 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- $ß$ but not by a $T_{h} 1$ to $T_{h} 2$ shift,” International Immunology, vol. 12, no. 5, pp. 623–630, 2000.
View at: Publisher Site | Google Scholar
J. Satoguina, M. Mempel, J. Larbi et al., “Antigen-specific T regulatory-1 cells are associated with immunosuppression in a chronic helminth infection (onchocerciasis),” Microbes and Infection, vol. 4, no. 13, pp. 1291–1300, 2002.
View at: Publisher Site | Google Scholar
C. Asseman, S. Mauze, M. W. Leach, R. L. Coffman, and F. Powrie, “An essential role for interleukin 10 in the function of regulatory T cells that inhibit intestinal inflammation,” The Journal of Experimental Medicine, vol. 190, no. 7, pp. 995–1004, 1999.
View at: Publisher Site | Google Scholar
S. Read, V. Malmström, and F. Powrie, “Cytotoxic T lymphocyte-associated antigen 4 plays an essential role in the function of $CD 25^{+} CD 4^{+}$ regulatory cells that control intestinal inflammation,” The Journal of Experimental Medicine, vol. 192, no. 2, pp. 295–302, 2000.
View at: Publisher Site | Google Scholar
A. M. Thornton and E. M. Shevach, “ $CD 4^{+} CD 25^{+}$ immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production,” The Journal of Experimental Medicine, vol. 188, no. 2, pp. 287–296, 1998.
View at: Publisher Site | Google Scholar
C. A. Piccirillo, J. J. Letterio, A. M. Thornton et al., “ $CD 4^{+} CD 25^{+}$ regulatory T cells can mediate suppressor function in the absence of transforming growth factor $ß$ 1 production and responsiveness,” The Journal of Experimental Medicine, vol. 196, no. 2, pp. 237–246, 2002.
View at: Publisher Site | Google Scholar
E. M. Shevach, “ $CD 4^{+} CD 25^{+}$ suppressor T cells: more questions than answers,” Nature Reviews Immunology, vol. 2, no. 6, pp. 389–400, 2002.
View at: Google Scholar
D. Buzoni-Gatel, H. Debbabi, F. J. D. Mennechet et al., “Murine ileitis after intracellular parasite infection is controlled by TGF- $ß$ -producing intraepithelial lymphocytes,” Gastroenterology, vol. 120, no. 4, pp. 914–924, 2001.
View at: Publisher Site | Google Scholar
M. D. Taylor, L. LeGoff, A. Harris, E. Malone, J. E. Allen, and R. M. Maizels, “Removal of regulatory T cell activity reverses hyporesponsiveness and leads to filarial parasite clearance in vivo,” The Journal of Immunology, vol. 174, no. 8, pp. 4924–4933, 2005.
View at: Google Scholar
Z. Su, M. Segura, K. Morgan, J. C. Loredo-Osti, and M. M. Stevenson, “Impairment of protective immunity to blood-stage malaria by concurrent nematode infection,” Infection and Immunity, vol. 73, no. 6, pp. 3531–3539, 2005.
View at: Publisher Site | Google Scholar
J. L. Grogan, P. G. Kremsner, A. M. Deelder, and M. Yazdanbakhsh, “Antigen-specific proliferation and interferon- $γ$ and interleukin-5 production are down-regulated during Schistosoma haematobium infection,” The Journal of Infectious Diseases, vol. 177, no. 5, pp. 1433–1437, 1998.
View at: Google Scholar
A. S. McKee and E. J. Pearce, “ $CD 25^{+} CD 4^{+}$ cells contribute to $T_{h} 2$ polarization during helminth infection by suppressing $T_{h} 1$ response development,” The Journal of Immunology, vol. 173, no. 2, pp. 1224–1231, 2004.
View at: Google Scholar
M. Hesse, C. A. Piccirillo, Y. Belkaid et al., “The pathogenesis of schistosomiasis is controlled by cooperating IL-10-producing innate effector and regulatory T cells,” The Journal of Immunology, vol. 172, no. 5, pp. 3157–3166, 2004.
View at: Google Scholar
I. J. Suffia, S. K. Reckling, C. A. Piccirillo, R. S. Goldszmid, and Y. Belkaid, “Infected site-restricted Fox $p 3^{+}$ natural regulatory T cells are specific for microbial antigens,” The Journal of Experimental Medicine, vol. 203, no. 3, pp. 777–788, 2006.
View at: Publisher Site | Google Scholar
Y. Belkaid, K. F. Hoffmann, S. Mendez et al., “The role of interleukin (IL)-10 in the persistence of Leishmania major in the skin after healing and the therapeutic potential of anti-IL-10 receptor antibody for sterile cure,” The Journal of Experimental Medicine, vol. 194, no. 10, pp. 1497–1506, 2001.
View at: Publisher Site | Google Scholar
L. I. Terrazas, K. L. Walsh, D. Piskorska, E. McGuire, and D. A. Harn Jr., “The schistosome oligosaccharide lacto- $N$ -neotetraose expands $Gr 1^{+}$ cells that secrete anti-inflammatory cytokines and inhibit proliferation of naive $CD 4^{+}$ cells: a potential mechanism for immune polarization in helminth infections,” The Journal of Immunology, vol. 167, no. 9, pp. 5294–5303, 2001.
View at: Google Scholar
M.-B. Voisin, D. Buzoni-Gatel, D. Bout, and F. Velge-Roussel, “Both expansion of regulatory $Gr 1^{+}$ $CD 11 b^{+}$ myeloid cells and anergy of T lymphocytes participate in hyporesponsiveness of the lung-associated immune system during acute toxoplasmosis,” Infection and Immunity, vol. 72, no. 9, pp. 5487–5492, 2004.
View at: Publisher Site | Google Scholar
O. Goñi, P. Alcaide, and M. Fresno, “Immunosuppression during acute Trypanosoma cruzi infection: involvement of Ly6G $(Gr 1^{+}) CD 11 b^{+}$ immature myeloid suppressor cells,” International Immunology, vol. 14, no. 10, pp. 1125–1134, 2002.
View at: Google Scholar
J. S. Stamler, D. J. Singel, and J. Loscalzo, “Biochemistry of nitric oxide and its redox-activated forms,” Science, vol. 258, no. 5090, pp. 1898–1902, 1992.
View at: Publisher Site | Google Scholar
S. L. James, “Role of nitric oxide in parasitic infections,” Microbiological Reviews, vol. 59, no. 4, pp. 533–547, 1995.
View at: Google Scholar
S. Hayashi, C. C. Chan, R. Gazzinelli, and F. G. Roberge, “Contribution of nitric oxide to the host parasite equilibrium in toxoplasmosis,” The Journal of Immunology, vol. 156, no. 4, pp. 1476–1481, 1996.
View at: Google Scholar
I. A. Abrahamsohn and R. L. Coffman, “Cytokine and nitric oxide regulation of the immunosuppression in Trypanosoma cruzi infection,” The Journal of Immunology, vol. 155, no. 8, pp. 3955–3963, 1995.
View at: Google Scholar
K. Fehsel, K.-D. Kroncke, K. L. Meyer, H. Huber, V. Wahn, and V. Kolb-Bachofen, “Nitric oxide induces apoptosis in mouse thymocytes,” The Journal of Immunology, vol. 155, no. 6, pp. 2858–2865, 1995.
View at: Google Scholar
J. E. Albina, S. Cui, R. B. Mateo, and J. S. Reichner, “Nitric oxide-mediated apoptosis in murine peritoneal macrophages,” The Journal of Immunology, vol. 150, no. 11, pp. 5080–5085, 1993.
View at: Google Scholar
R.-H. Chang, M.-H. Lin Feng, W.-H. Liu, and M.-Z. Lai, “Nitric oxide increased interleukin-4 expression in T lymphocytes,” Immunology, vol. 90, no. 3, pp. 364–369, 1997.
View at: Publisher Site | Google Scholar
L. Soong and R. L. Tarleton, “Trypanosoma cruzi infection suppresses nuclear factors that bind to specific sites on the interleukin-2 enhancer,” European Journal of Immunology, vol. 24, no. 1, pp. 16–23, 1994.
View at: Publisher Site | Google Scholar
A. Mizoguchi and A. K. Bhan, “A case for regulatory B cells,” The Journal of Immunology, vol. 176, no. 2, pp. 705–710, 2006.
View at: Google Scholar
P. Velupillai and D. A. Harn, “Oligosaccharide-specific induction of interleukin 10 production by $B 220^{+}$ cells from schistosome-infected mice: a mechanism for regulation of $CD 4^{+}$ T-cell subsets,” Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 1, pp. 18–22, 1994.
View at: Publisher Site | Google Scholar
V. Gillan, R. A. Lawrence, and E. Devaney, “B cells play a regulatory role in mice infected with the L3 of Brugia pahangi,” International Immunology, vol. 17, no. 4, pp. 373–382, 2005.
View at: Publisher Site | Google Scholar
C. Mauri, D. Gray, N. Mushtaq, and M. Londei, “Prevention of arthritis by interleukin 10-producing B cells,” The Journal of Experimental Medicine, vol. 197, no. 4, pp. 489–501, 2003.
View at: Publisher Site | Google Scholar
G. A. DosReis and M. A. Barcinski, “Apoptosis and parasitism: from the parasite to the host immune response,” Advances in Parasitology, vol. 49, pp. 133–161, 2001.
View at: Publisher Site | Google Scholar
G. A. DosReis, M. E. F. Fonseca, and M. F. Lopes, “Programmed T-cell death in experimental Chagas disease,” Parasitology Today, vol. 11, no. 10, pp. 390–394, 1995.
View at: Publisher Site | Google Scholar
J. Zhang, Z. A. Andrade, Z.-X. Yu et al., “Apoptosis in a canine model of acute Chagasic myocarditis,” Journal of Molecular and Cellular Cardiology, vol. 31, no. 3, pp. 581–596, 1999.
View at: Publisher Site | Google Scholar
M. F. Lopes and G. A. DosReis, “Trypanosoma cruzi-induced immunosuppression: selective triggering of $CD 4^{+}$ T-cell death by the T-cell receptor-CD3 pathway and not by the CD69 or Ly-6 activation pathway,” Infection and Immunity, vol. 64, no. 5, pp. 1559–1564, 1996.
View at: Google Scholar
G. A. Martins, S. B. Petkova, F. S. Machado et al., “Fas-FasL interaction modulates nitric oxide production in Trypanosoma cruzi-infected mice,” Immunology, vol. 103, no. 1, pp. 122–129, 2001.
View at: Publisher Site | Google Scholar
M. S. Leguizamón, E. Mocetti, H. G. Rivello, P. Argibay, and O. Campetella, “Trans-sialidase from Trypanosoma cruzi induces apoptosis in cells from the immune system in vivo,” The Journal of Infectious Diseases, vol. 180, no. 4, pp. 1398–1402, 1999.
View at: Publisher Site | Google Scholar
J. Mucci, A. Hidalgo, E. Mocetti, P. F. Argibay, M. S. Leguizamón, and O. Campetella, “Thymocyte depletion in Trypanosoma cruzi infection is mediated by trans-sialidase-induced apoptosis on nurse cells complex,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 6, pp. 3896–3901, 2002.
View at: Publisher Site | Google Scholar
C. G. Freire-de-Lima, M. P. Nunes, S. Corte-Real et al., “Proapoptotic activity of a Trypanosoma cruzi ceramide-containing glycolipid turned on in host macrophages by IFN- $?$ ,” The Journal of Immunology, vol. 161, no. 9, pp. 4909–4916, 1998.
View at: Google Scholar
C. G. Freire-de-Lima, D. O. Nascimento, M. B. P. Soares et al., “Uptake of apoptotic cells drives the growth of a pathogenic trypanosome in macrophages,” Nature, vol. 403, no. 6766, pp. 199–203, 2000.
View at: Publisher Site | Google Scholar
H. Nishimura and T. Honjo, “PD-1: an inhibitory immunoreceptor involved in peripheral tolerance,” Trends in Immunology, vol. 22, no. 5, pp. 265–268, 2001.
View at: Publisher Site | Google Scholar
Y. Agata, A. Kawasaki, H. Nishimura et al., “Expression of the PD-1 antigen on the surface of stimulated mouse T and B lymphocytes,” International Immunology, vol. 8, no. 5, pp. 765–772, 1996.
View at: Publisher Site | Google Scholar
Y. Iwai, S. Terawaki, M. Ikegawa, T. Okazaki, and T. Honjo, “PD-1 inhibits antiviral immunity at the effector phase in the liver,” The Journal of Experimental Medicine, vol. 198, no. 1, pp. 39–50, 2003.
View at: Publisher Site | Google Scholar
S. C. Liang, R. J. Greenwald, Y. E. Latchman et al., “PD-L1 and PD-L2 have distinct roles in regulating host immunity to cutaneous leishmaniasis,” European Journal of Immunology, vol. 36, no. 1, pp. 58–64, 2005.
View at: Publisher Site | Google Scholar
D. G. Colley, L. E. Sasser, and A. M. Reed, “PD- $L 2^{+}$ dendritic cells and PD- $1^{+}$ $CD 4^{+}$ T cells in schistosomiasis correlate with morbidity,” Parasite Immunology, vol. 27, no. 1-2, pp. 45–53, 2005.
View at: Publisher Site | Google Scholar
A. Sala and G. Folco, “Neutrophils, endothelial cells, and cysteinyl leukotrienes: a new approach to neutrophil-dependent inflammation?” Biochemical and Biophysical Research Communications, vol. 283, no. 5, pp. 1003–1006, 2001.
View at: Publisher Site | Google Scholar
S. Kilfeather, “5-lipoxygenase inhibitors for the treatment of COPD,” Chest, vol. 121, 5 supplement, pp. 197S–200S, 2002.
View at: Publisher Site | Google Scholar
M. J. McConville and M. A. J. Ferguson, “The structure, biosynthesis and function of glycosylated phosphatidylinositols in the parasitic protozoa and higher eukaryotes,” The Biochemical Journal, vol. 294, part 2, pp. 305–324, 1993.
View at: Google Scholar
J. C. Carreira, C. Jones, R. Wait, J. O. Previato, and L. Mendonça-Previato, “Structural variation in the glycoinositolphospholipids of different strains of Trypanosoma cruzi,” Glycoconjugate Journal, vol. 13, no. 6, pp. 955–966, 1996.
View at: Publisher Site | Google Scholar
N. A. Gomes, J. O. Previato, B. Zingales, L. Mendonça-Previato, and G. A. DosReis, “Down-regulation of T lymphocyte activation in vitro and in vivo induced by glycoinositolphospholipids from Trypanosoma cruzi: assignment of the T cell-suppressive determinant to the ceramide domain,” The Journal of Immunology, vol. 156, no. 2, pp. 628–635, 1996.
View at: Google Scholar
C. Brodskyn, J. Patricio, R. Oliveira et al., “Glycoinositolphospholipids from Trypanosoma cruzi interfere with macrophages and dendritic cell responses,” Infection and Immunity, vol. 70, no. 7, pp. 3736–3743, 2002.
View at: Publisher Site | Google Scholar
S. S. Goldberg, M. N. Cordeiro, A. A. Silva Pereira, and M. L. Mares Guia, “Release of lipopolysaccharide (LPS) from cell surface of Trypanosoma cruzi by EDTA,” International Journal for Parasitology, vol. 13, no. 1, pp. 11–18, 1983.
View at: Google Scholar
M. A. S. Campos, I. C. Almeida, O. Takeuchi et al., “Activation of toll-like receptor-2 by glycosylphosphatidylinositol anchors from a protozoan parasite,” The Journal of Immunology, vol. 167, no. 1, pp. 416–423, 2001.
View at: Google Scholar
F. Leyva-Cobián, I. M. Outschoorn, E. Carrasco-Marín, and C. Alvarez-Domínguez, “The consequences of the intracellular retention of pathogen-derived T-cell-independent antigens on protein presentation to T cells,” Clinical Immunology and Immunopathology, vol. 85, no. 1, pp. 1–15, 1997.
View at: Publisher Site | Google Scholar
P. Velupillai, W. E. Secor, A. M. Horauf, and D. A. Harn, “B-1 cell $(CD 5^{+} B 220^{+})$ outgrowth in murine schistosomiasis is genetically restricted and is largely due to activation by polylactosamine sugars,” The Journal of Immunology, vol. 158, no. 1, pp. 338–344, 1997.
View at: Google Scholar
C. A. M. Bento, M. B. Melo, J. O. Previato, L. Mendonça-Previato, and L. M. T. Peçanha, “Glycoinositolphospholipids purified from Trypanosoma cruzi stimulate Ig production in vitro,” The Journal of Immunology, vol. 157, no. 11, pp. 4996–5001, 1996.
View at: Google Scholar
D. Piedrafita, L. Proudfoot, A. V. Nikolaev et al., “Regulation of macrophage IL-12 synthesis by Leishmania phosphoglycans,” European Journal of Immunology, vol. 29, no. 1, pp. 235–244, 1999.
View at: Publisher Site | Google Scholar
A. Ouaissi, M. A. Ouaissi, and D. Sereno, “Glutathione $S$ -transferases and related proteins from pathogenic human parasites behave as immunomodulatory factors,” Immunology Letters, vol. 81, no. 3, pp. 159–164, 2002.
View at: Publisher Site | Google Scholar
A. Sommer, R. Rickert, P. Fischer, H. Steinhart, R. D. Walter, and E. Liebau, “A dominant role for extracellular glutathione $S$ -transferase from Onchocerca volvulus is the production of prostaglandin $D_{2}$ ,” Infection and Immunity, vol. 71, no. 6, pp. 3603–3606, 2003.
View at: Publisher Site | Google Scholar
A. Ouaissi, A. Guevara-Espinoza, F. Chabé, R. Gomez-Corvera, and A. Taibi, “A novel and basic mechanism of immunosuppression in Chagas' disease: Trypanosoma cruzi releases in vitro and in vivo a protein which induces T cell unresponsiveness through specific interaction with cysteine and glutathione,” Immunology Letters, vol. 48, no. 3, pp. 221–224, 1995.
View at: Publisher Site | Google Scholar
R. Fernandez-Gomez, S. Esteban, R. Gomez-Corvera, K. Zoulika, and A. Ouaissi, “Trypanosoma cruzi: Tc52 released protein-induced increased expression of nitric oxide synthase and nitric oxide production by macrophages,” The Journal of Immunology, vol. 160, no. 7, pp. 3471–3479, 1998.
View at: Google Scholar
M. Borges, E. Guilvard, A. Cordeiro da Silva, B. Vergnes, K. Zemzoumi, and A. Ouaissi, “Endogenous Trypanosoma cruzi Tc52 protein expression upregulates the growth of murine macrophages and fibroblasts and cytokine gene expression,” Immunology Letters, vol. 78, no. 3, pp. 127–134, 2001.
View at: Publisher Site | Google Scholar
M. C. Borges, A. Cordeiro da Silva, D. Sereno, and A. Ouaissi, “Peptide-based analysis of the amino acid sequence important to the immunoregulatory function of Trypanosoma cruzi Tc52 virulence factor,” Immunology, vol. 109, no. 1, pp. 147–155, 2003.
View at: Publisher Site | Google Scholar
A. Allaoui, C. François, K. Zemzoumi, E. Guilvard, and A. Ouaissi, “Intracellular growth and metacyclogenesis defects in Trypanosoma cruzi carrying a targeted deletion of a Tc52 protein-encoding allele,” Molecular Microbiology, vol. 32, no. 6, pp. 1273–1286, 1999.
View at: Publisher Site | Google Scholar
E. Garzón, M. C. Borges, A. Cordeiro-da-Silva et al., “Trypanosoma cruzi carrying a targeted deletion of a Tc52 protein-encoding allele elicits attenuated Chagas' disease in mice,” Immunology Letters, vol. 89, no. 1, pp. 67–80, 2003.
View at: Publisher Site | Google Scholar
L. Ding and E. M. Shevach, “IL-10 inhibits mitogen-induced T cell proliferation by selectively inhibiting macrophage costimulatory function,” The Journal of Immunology, vol. 148, no. 10, pp. 3133–3139, 1992.
View at: Google Scholar
D. F. Fiorentino, A. Zlotnik, P. Vieira et al., “IL-10 acts on the antigen-presenting cell to inhibit cytokine production by $T_{h} 1$ cells,” The Journal of Immunology, vol. 146, no. 10, pp. 3444–3451, 1991.
View at: Google Scholar
A. H. Ding, C. F. Nathan, and D. J. Stuehr, “Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages: comparison of activating cytokines and evidence for independent production,” The Journal of Immunology, vol. 141, no. 7, pp. 2407–2412, 1988.
View at: Google Scholar
J. M. Sternberg and N. A. Mabbott, “Nitric oxide-mediated suppression of T cell responses during Trypanosoma brucei infection: soluble trypanosome products and interferon- $γ$ are synergistic inducers of nitric oxide synthase,” European Journal of Immunology, vol. 26, no. 3, pp. 539–543, 1996.
View at: Publisher Site | Google Scholar
W. Wang, K. Keller, and K. Chadee, “Entamoeba histolytica modulates the nitric oxide synthase gene and nitric oxide production by macrophages for cytotoxicity against amoebae and tumour cells,” Immunology, vol. 83, no. 4, pp. 601–610, 1994.
View at: Google Scholar
A. Ouaissi, E. Guilvard, Y. Delneste et al., “The Trypanosoma cruzi Tc52-released protein induces human dendritic cell maturation, signals via Toll-like receptor 2, and confers protection against lethal infection,” The Journal of Immunology, vol. 168, no. 12, pp. 6366–6374, 2002.
View at: Google Scholar
G. Gorelik, G. Cremaschi, E. Borda, and L. Sterin-Borda, “Trypanosoma cruzi antigens down-regulate T lymphocyte proliferation by muscarinic cholinergic receptor-dependent release of PGE2,” Acta Physiologica Pharmacologica et Therapeutica Latinoamericana, vol. 48, no. 3, pp. 115–123, 1998.
View at: Google Scholar
F. Kierszenbaum, J. L. de Diego, M. Fresno, and M. B. Sztein, “Inhibitory effects of the Trypanosoma cruzi membrane glycoprotein AGC10 on the expression of IL-2 receptor chains and secretion of cytokines by subpopulations of activated human T lymphocytes,” European Journal of Immunology, vol. 29, no. 5, pp. 1684–1691, 1999.
View at: Publisher Site | Google Scholar
A. Cordeiro da Silva, A. G. Espinoza, A. Taibi, A. Ouaissi, and P. Minoprio, “A 24000 MW Trypanosoma cruzi antigen is a B-cell activator,” Immunology, vol. 94, no. 2, pp. 189–196, 1998.
View at: Publisher Site | Google Scholar
A. Cordeiro da Silva, M. C. Borges, E. Guilvard, and A. Ouaissi, “Dual role of the Leishmania major ribosomal protein S3a homologue in regulation of T- and B-cell activation,” Infection and Immunity, vol. 69, no. 11, pp. 6588–6596, 2001.
View at: Publisher Site | Google Scholar
A. R. Macintyre, J. B. Dixon, J. S. Bleakley, and J. R. Green, “Echinococcus granulosus: assays for hydatid immunoregulatory factors using established lymphoid cell lines,” Parasite Immunology, vol. 22, no. 10, pp. 475–485, 2000.
View at: Publisher Site | Google Scholar
R. K. Grencis and G. M. Entwistle, “Production of an interferon- $γ$ homologue by an intestinal nematode: functionally significant or interesting artefact?” Parasitology, vol. 115, supplement, pp. S101–S106, 1997.
View at: Publisher Site | Google Scholar
X. Zang, P. Taylor, J. M. Wang et al., “Homologues of human macrophage migration inhibitory factor from a parasitic nematode: gene cloning, protein activity, and crystal structure,” The Journal of Biological Chemistry, vol. 277, no. 46, pp. 44261–44267, 2002.
View at: Publisher Site | Google Scholar
J. Aliberti, J. G. Valenzuela, V. B. Carruthers et al., “Molecular mimicry of a ${CCR}_{5}$ binding-domain in the microbial activation of dendritic cells,” Nature Immunology, vol. 4, no. 5, pp. 485–490, 2003.
View at: Publisher Site | Google Scholar
A. Wang and D. M. McKay, “Immune modulation by a high molecular weight fraction from the rat tapeworm Hymenolepis diminuta,” Parasitology, vol. 130, no. 5, pp. 575–585, 2005.
View at: Publisher Site | Google Scholar

Copyright

Copyright © 2007 Ali Ouaissi. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

PDF Download Citation Order printed copies

Views

423

Downloads

965

Citations