A transmembrane domain-containing surface protein from Toxoplasma gondii augments replication in activated immune cells and establishment of a chronic infection

Infection and Immunity

Volumn 77, Issue 9, 2009, Pages 3731-3739

  Pollard, Angela M ^a   Skariah, Sini ^a,b   Mordue, Dana G ^a,b   Knoll, Laura J ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b NEW YORK MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE ANTIGEN; MEMBRANE PROTEIN; NITRIC OXIDE; POLYPEPTIDE; SAG1 ANTIGEN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRADYZOITE; CELL DIVISION; CHRONIC DISEASE; CONTROLLED STUDY; DENDRITIC CELL; DOWN REGULATION; FEMALE; GENE; GENE INSERTION; GENETIC COMPLEMENTATION; IMMUNOCOMPETENT CELL; IMMUNOFLUORESCENCE; INFECTION; ISOLATION PROCEDURE; MACROPHAGE; MACROPHAGE ACTIVATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; TACHYZOITE; TGME49 1111670 GENE; TOXOPLASMA GONDII; TOXOPLASMOSIS; WESTERN BLOTTING;

ANIMALS; CELLS, CULTURED; FEMALE; HUMANS; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; MICE, INBRED C57BL; PROTOZOAN PROTEINS; TOXOPLASMA; TOXOPLASMOSIS, ANIMAL;

EID: 69049101205     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00450-09     Document Type: Article

References (40)

1. Alexander, J., and C. A. Hunter. 1998. Immunoregulation during toxoplasmosis. Chem. Immunol. 70:81-102.
2. Aline, F., D. Bout, and I. Dimier-Poisson. 2002. Dendritic cells as effector cells: gamma interferon activation of murine dendritic cells triggers oxygen-dependent inhibition of Toxoplasma gondii replication. Infect. Immun. 70: 2368-2374.
3. Bliss, S. K., Y. Zang, and E. Y. Denkers. 1999. Murine neutrophil stimulation by Toxoplasma gondii antigen drives high level production of IFN-γ independent IL-12. J. Immunol. 163:2081-2088.
4. Boothroyd, J. C., A. Hehl, L. J. Knoll, and I. D. Manger. 1998. The surface of Toxoplasma: more or less. Int. J. Parasitol. 28:3-9.
5. Chao, C. C., W. R. Anderson, S. Hu, G. Gekker, A. Martella, and P. K. Peterson. 1993. Activated microglia inhibit multiplication of Toxoplasma gondii via a nitric oxide mechanism. Clin. Immunol. Immunopathol. 67:178-183.
6. Denkers, E. Y., and B. A. Butcher. 2005. Sabotage and exploitation in macrophages parasitized by intracellular protozoans. Trends Parasitol. 21:35-41.
7. Denkers, E. Y., and R. T. Gazzinelli. 1998. Regulation and function of T-cell-mediated immunity during Toxoplasma gondii infection. Clin. Microbiol. Rev. 11:569-588.
8. Donald, R. G., and D. S. Roos. 1993. Stable molecular transformation of Toxoplasma gondii: a selectable dihydrofolate reductase-thymidylate synthase marker based on drug-resistance mutations in malaria. Proc. Natl. Acad. Sci. USA 90:11703-11707.
9. Dubey, J. P. 1994. Toxoplasmosis. J. Am. Vet. Med. Assoc. 205:1593-1598.
10. Dubey, J. P. 1998. Advances in the life cycle of Toxoplasma. Int. J. Parasitol. 28:1019-1024.
11. Frankel, M. B., D. G. Mordue, and L. J. Knoll. 2007. Discovery of parasite virulence genes reveals a unique regulator of chromosome condensation 1 ortholog critical for efficient nuclear trafficking. Proc. Natl. Acad. Sci. USA 104:10181-10186.
12. Gazzinelli, R. T., S. Hieny, T. Wynn, S. Wolf, and A. Sher. 1993. IL-12 is required for the T-cell independent induction of IFN-γ by an intracellular parasite and induces resistance in T-cell deficient hosts. Proc. Natl. Acad. Sci. USA 90:6115-6119.
13. 125I]iodonaphthalene-1-azide. Eukaryot. Cell 5:1622-1634.
14. Grimwood, J., and J. E. Smith. 1996. Toxoplasma gondii: the role of parasite surface and secreted proteins in host cell invasion. Int. J. Parasitol. 26:169-173.
15. Inaba, K., W. J. Swiggard, R. M. Steinman, N. Romani, and G. Schuler. 2003. Isolation of dendritic cells. p. 3.7.1-3.7.15. In J. E. Coligan, A. M. Krusibeck, D. H. Margulies, E. M. Shevach, and W. Strobe (ed.), Current protocols in immunology. John Wiley & Sons, Indianapolis, IN.
16. Jung, C., C. Y.-F. Lee, and M. E. Grigg. 2004. The SRS superfamily of Toxoplasma surface proteins. Int. J. Parasitol. 34:285-296.
17. Kim, S.-K., A. Karasov, and J. C. Boothroyd. 2007. Bradyzoite-specific surface antigen SRS9 plays a role in maintaining Toxoplasma gondii persistence in the brain and in host control of parasite replication in the intestine. Infect. Immun. 75:1626-1634.
18. Lambert, H., N. Hitziger, I. Dellacasa, M. Svensson, and A. Barragan. 2006. Induction of dendritic cell migration upon Toxoplasma gondii infection potentates parasite dissemination. Cell. Microbiol. 8:1611-1623.
19. Lekutis, C., D. J. P. Ferguson, M. E. Grigg, M. Camps, and J. C. Boothroyd. 2001. Surface antigens of Toxoplasma gondii: variations on a theme. Int. J. Parasitol. 31:1285-1292.
20. Liu, C.-H., Y. Fan, A. Dias, L. Esper, R. A. Corn, A. Bafica, F. S. Machado, and J. Aliberti. 2006. Cutting edge: dendritic cells are essential for in vivo IL-12 production and development of resistance against Toxoplasma gondii infection in mice. J. Immunol. 177:31-35.
21. Lüder, C. G., M. Algner, C. Lang, N. Bleicher, and U. Gross. 2003. Reduced expression of the inducible nitric oxide synthase after infection with Toxoplasma gondii facilitates parasite replication in activated murine macrophages. Int. J. Parasitol. 33:833-844.
22. Luft, B. J., Y. Naot, F. G. Araujo, E. B. Stinson, and J. S. Remington. 1983. Primary and reactivated Toxoplasma infection in patients with cardiac transplants. Ann. Intern. Med. 99:27-31.
23. Martens, S., I. Parvanova, J. Zerrahn, G. Griffiths, G. Shell, G. Reichmann, and J. C. Howard. 2005. Disruption of Toxoplasma gondii parasitophorous vacuoles by the mouse p47-resistance GTPases. PLoS Pathog. 1:e24.
24. McKee, A. S., F. Dzierszinski, M. Boes, D. S. Roos, and E. J. Pearce. 2004. Functional inactivation of immature dendritic cells by the intracellular parasite Toxoplasma gondii. J. Immunol. 173:2632-2640.
25. Mineo, J. R., and L. H. Kasper. 1994. Attachment of Toxoplasma gondii to host cells involves major surface protein, SAG-1 (P30). Exp. Parasitol. 79:11-20.
26. Mordue, D. G., C. F. Scott-Weathers, C. M. Tobin, and L. J. Knoll. 2007. A patatin-like protein protects Toxoplasma gondii from degradation in activated macrophages. Mol. Microbiol. 63:482-496.
27. Mordue, D. G., and L. D. Sibley. 2003. A novel population of Gr-1+-activated macrophages induced during acute toxoplasmosis. J. Leukoc. Biol. 74:1015-1025.
28. Pollard, A. M., K. N. Onatolu, L. Hiller, K. Haldar, and L. J. Knoll. 2008. Highly polymorphic family of glycosylphosphatidylinositol- anchored surface antigens with evidence of developmental regulation in Toxoplasma gondii. Infect. Immun. 76:103-110.
29. Porter, S. B., and M. Sande. 1992. Toxoplasmosis of the central nervous system in the acquired immunodeficiency syndrome. N. Engl. J. Med. 327:1643-1648.
30. Remington, J. S., R. McLeond, and G. Desmonts. 1990. Toxoplasmosis, p. 89-195. In J. S. Remington and J. O. Klein (ed.), Infectious diseases of the fetus and newborn. WB Saunders Co., Philadelphia, PA.
31. Rozenfeld, C., R. Martinez, S. Seabra, C. Sant'anna, J. G. Goncalves, M. Bozza, V. Moura-Neto, and W. De Souza. 2005. Toxoplasma gondii prevents neuron degeneration by interferon-γ-activated microglia in a mechanism involving inhibition of inducible nitric oxide synthase and transforming growth factor-β1 production by infected microglia. Am. J. Pathol. 167:1021-1031.
32. Scharton-Kersten, T. M., T. A. Wynn, E. Y. Denkers, S. Bala, L. Showe, E. Grunvald, S. Hieny, R. T. Gazzinelli, and A. Sher. 1996. In the absence of endogenous IFN-γ mice develop unimpaired IL-12 responses to Toxoplasma gondii while failing to control acute infection. J. Immunol. 157:4045-4054.
33. Scharton-Kersten, T. M., G. Yap, J. Magram, and A. Sher. 1997. Inducible nitric oxide is essential for host control of persistent but not acute infection of intracellular pathogen, Toxoplasma gondii. J. Exp. Med. 185:1261-1273.
34. Seabra, S. H., W. de Sousa, and R. A. Damatta. 2002. Toxoplasma gondii partially inhibits nitric oxide production of activated murine macrophages. Exp. Parasitol. 100:62-70.
35. Soldati, D., and J. C. Boothroyd. 1995. A selector of transcription initiation in the protozoan parasite Toxoplasma gondii. Mol. Cell. Biol. 15:18-93.
36. Suzuki, Y., M. A. Orellana, R. D. Schreiber, and J. S. Remington. 1988. Interferon-γ: the major mediator of resistance against Toxoplasma gondii. Science 240:516-518.
37. Wichroski, M. J., J. A. Melton, C. G. Donahue, R. K. Tweten, and G. E. Ward. 2002. Clostridium septicum alpha-toxin is active against the parasitic protozoan Toxoplasma gondii and targets members of the SAG family of glycosylphosphatidylinositol-anchored surface proteins. Infect. Immun. 70:4353-4361.
38. Wong, S. Y., and J. S. Remington. 1993. Biology of Toxoplasma gondii. AIDS 7:299-316.
39. Yap, G. S., and A. Sher. 1999. Cell-mediated immunity to Toxoplasma gondii: initiation, regulation, and effector function. Immunobiology 201:240-247.
40. Zhao, Y., D. J. P. Ferguson, D. C. Wilson, J. C. Howard, L. D. Sibley, and G. S. Yap. 2009. Virulent Toxoplasma gondii evade immunity-related GTPase-mediated parasite vacuole disruption within primed macrophages. J. Immunol. 182:3775-3781.