Toxoplasma gondii cyclophilin 18-mediated production of nitric oxide induces bradyzoite conversion in a CCR5-dependent manner

Infection and Immunity

Volumn 77, Issue 9, 2009, Pages 3686-3695

  Ibrahim, Hany M ^a,b   Bannai, Hiroshi ^a   Xuan, Xuenan ^a   Nishikawa, Yoshifumi ^a  

^a OBIHIRO UNIVERSITY OF AGRICULTURE AND VETERINARY MEDICINE   (Japan)

^b Menoufia University   (Egypt)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR5; CYCLOPHILIN; CYCLOPHILIN 18; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 6; NITRIC OXIDE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRADYZOITE; CONTROLLED STUDY; FEMALE; GROWTH INHIBITION; IMMUNOMODULATION; MACROPHAGE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; TOXOPLASMA GONDII;

ANIMALS; CYCLOPHILINS; FEMALE; INTERLEUKIN-12 SUBUNIT P40; INTERLEUKIN-6; MICE; MICE, INBRED C57BL; NITRIC OXIDE; PROTOZOAN PROTEINS; RECEPTORS, CCR5; TOXOPLASMA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 69049093908     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00361-09     Document Type: Article

References (63)

1. Aliberti, J., C. Reis e Sousa, M. Schito, S. Hieny, T. Wells, G. B. Huffnage, and A. Sher.2000. CCR5 provides a signal for microbial induced production of IL-12 by CD8α+ dendritic cells. Nat. Immunol. 1:83-87.
2. Aliberti, J., J. G. Valenzuela, V. B. Carruthers, S. Hieny, J. Andersen, H. Charest, C. Reis e Sousa, A. Fairlamb, J. M. Ribeiro, and A. Sher.2003. Molecular mimicry of a CCR5 binding-domain in the microbial activation of dendritic cells. Nat. Immunol. 4:485-490.
3. Bastos, K. R., R. Barboza, L. Sardinha, M. Russo, J. M. Alvarez, and M. R. Lima.2007. Role of endogenous IFN-gamma in macrophage programming induced by IL-12 and IL-18. J. Interf. Cytok. Res. 27:399-410.
4. Bell, A., P. Monaghan, and A. P. Page.2006. Peptidyl-prolyl cis-trans isomerases (immunophilins) and their roles in parasite biochemistry, host-parasite interaction and antiparasitic drug action. Int. J. Parasitol. 36:261-276.
5. Bohne, W., J. Heesemann, and U. Gross.1993. Induction of bradyzoite-specific Toxoplasma gondii antigens in gamma interferon-treated mouse macrophages. Infect. Immun. 61:1141-1145.
6. Bohne, W., J. Heesemann, and U. Gross.1994. Reduced replication of Toxoplasma gondii is necessary for induction of bradyzoite-specific antigens: a possible role for nitric oxide in triggering stage conversion. Infect. Immun. 62:1761-1767.
7. Cai, G., R. Kastelein, and C. A. Hunter.2000. Interleukin-18 (IL-18) enhances innate IL-12-mediated resistance to Toxoplasma gondii. Infect. Immun. 68:6932-6938.
8. Cai, G., T. Radzanowski, E. N. Villegas, R. Kastelein, and C. A. Hunter. 2000. Identification of STAT4-dependent and independent mechanisms of resistance to Toxoplasma gondii. J. Immunol. 165:2619-2627.
9. Chai, Z., B. Sarcevic, A. Mawson, and B. H. Toh.2001. SET-related cell division autoantigen-1 (CDA1) arrests cell growth. J. Biol. Chem. 276:33665-33674.
10. Cleary, M. D., U. Singh, I. J. Blader, J. L. Brewer, and J. C. Boothroyd.2002. Toxoplasma gondii asexual development: identification of developmentally regulated genes and distinct patterns of gene expression. Eukaryot. Cell 1:329-340.
11. da Fonseca Ferreira da Silva, M., H. S. Barbosa, U. Gross, and C. G. Lüder. 2008. Stress-related and spontaneous stage differentiation of Toxoplasma gondii. Mol. Biosyst. 4:824-834.
12. Darwich, L., G. Coma, R. Peña, R. Bellido, E. J. Blanco, J. A. Este, F. E. Borras, B. Clotet, L. Ruiz, A. Rosell, F. Andreo, R. M. Parkhouse, and M. Bofill.2008. Secretion of interferon-gamma by human macrophages demonstrated at the single-cell level after costimulation with interleukin (IL)-12 plus IL-18. Immunology 126:386-393.
13. Dautu, G., B. Munyaka, G. Carmen, G. Zhang, Y. Omata, X. Xuenan, and M. Igarashi.2007. Toxoplasma gondii: DNA vaccination with genes encoding antigens MIC2, M2AP, AMA1 and BAG1 and evaluation of their immunogenic potential. Exp. Parasitol. 116:273-282.
14. Denkers, E. Y.2003. From cells to signaling cascades: manipulation of innate immunity by Toxoplasma gondii. FEMS Immunol. Med. Microbiol. 39:193-203.
15. 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.
16. Drapier, J. C., and J. B. Hibbs, Jr.1988. Differentiation of murine macrophages to express nonspecific cytotoxicity for tumor cells results in L-arginine-dependent inhibition of mitochondrial iron-sulfur enzymes in the macrophage effector cells. J. Immunol. 140:2829-2838.
17. Dubey, J. P.1994. Toxoplasmosis. J. Am. Vet. Med. Assoc. 205:1593-1598.
18. Dubey, J. P.1998. Re-examination of resistance of Toxoplasma gondii tachyzoites and bradyzoites to pepsin and trypsin digestion. Parasitology 116:43-50.
19. Dubey, J. P., D. S. Lindsay, and C. A. Speer.1998. Structures of Toxoplasma gondii tachyzoites, bradyzoites, and sporozoites and biology and development of tissue cysts. Clin. Microbiol. Rev. 11:267-299.
20. Eaton, M. S., L. M. Weiss, and K. Kim.2006. Cyclic nucleotide kinases and tachyzoite-bradyzoite transition in Toxoplasma gondii. Int. J. Parasitol. 36:107-114.
21. Ferguson, D. J.2004. Use of molecular and ultrastructural markers to evaluate stage conversion of Toxoplasma gondii in both the intermediate and definitive host. Int. J. Parasitol. 34:347-360.
22. Fultz, M. J., S. A. Barber, C. W. Dieffenbach, and S. N. Vogel.1993. Induction of IFN-gamma in macrophages by lipopolysaccharide. Int. Immunol. 5:1383-1392.
23. Gamo, K., S. Kiryu-Seo, H. Konishi, S. Aoki, K. Matsushima, K. Wada, and H. Kiyama.2008. G-protein-coupled receptor screen reveals a role for chemokine receptor CCR5 in suppressing microglial neurotoxicity. J. Neurosci. 28:11980-11988.
24. Gazzinelli, R. T., F. T. Hakim, S. Hieny, G. M. Shearer, and A. Sher.1991. Synergistic role of CD4+ and CD8+ T lymphocytes in IFN-γ production and protective immunity induced by an attenuated T. gondii vaccine. J. Immunol. 146:286-292.
25. Gazzinelli, R. T., I. Eltoum, T. A. Wynn, and A. Sher.1993. Acute cerebral toxoplasmosis is induced by in vivo neutralization of TNF-α and correlates with the down-regulated expression of inducible nitric oxide synthase and other markers of macrophage activation. J. Immunol. 151:3672-3681.
26. Gazzinelli, R. T., S. Hieny, T. A. Wynn, S. Wolf, and A. Sher.1993. Interleukin 12 is required for the T-lymphocyte-independent induction of interferon gamma by an intracellular parasite and induces resistance in T-cell-deficient hosts. Proc. Natl. Acad. Sci. USA 90:6115-6119.
27. High, K. P., K. A. Joiner, and R. E. Handschumacher.1994. Isolation, cDNA sequences, and biochemical characterization of the major cyclosporin-binding proteins of Toxoplasma gondii. J. Biol. Chem. 269:9105-9112.
28. Hunter, C. A., C. S. Subauste, V. H. Van Cleave, and J. S. Remington.1994. Production of gamma interferon by natural killer cells from Toxoplasma gondii-infected SCID mice: regulation by interleukin-10, interleukin-12, and tumor necrosis factor alpha. Infect. Immun. 62:2818-2824.
29. Hunter, C. A., C. W. Roberts, M. Murray, and J. Alexander.1992. Detection of cytokine mRNA in the brains of mice with toxoplasmic encephalitis. Parasite Immunol. 14:405-413.
30. Hunter, C. A., C. W. Roberts, and J. Alexander.1992. Kinetics of cytokine mRNA production in the brains of mice with progressive toxoplasmic encephalitis. Eur. J. Immunol. 22:2317-2322.
31. James, S. L.1995. Role of nitric oxide in parasitic infections. Microbiol. Rev. 59:533-547.
32. Khan, I. A., J. D. Schwartzman, T. Matsuura, and L. H. Kasper.1997. A dichotomous role for nitric oxide during acute Toxoplasma gondii infection in mice. Proc. Natl. Acad. Sci. USA 94:13955-13960.
33. Khan, I. A., S. Y. Thomas, M. M. Moretto, F. S. Lee, S. A. Islam, C. Combe, J. D. Schwartzman, and A. D. Luster.2006. CCR5 is essential for NK cell trafficking and host survival following Toxoplasma gondii infection. PLoS Pathog. 2:e49.
34. Kolb, H., and V. Kolb-Bachofen.1992. Nitric oxide: a pathogenetic factor in autoimmunity. Immunol. Today 13:157-160.
35. Langermans, J. A. M., M. E. B. van der Hulst, P. H. Nibbering, P. S. Hiemstra, L. Fransen, and R. van Furth.1992. IFN-γ induced L-arginine dependent toxoplasmastatic activity in murine peritoneal macrophages is mediated by endogenous tumor necrosis factor alpha. J. Immunol. 148:568-574.
36. Li, L., B. P. Brunk, J. C. Kissinger, D. Pape, K. Tang, R. H. Cole, J. Martin, T. Wylie, M. Dante, S. J. Fogarty, D. K. Howe, P. A. Liberator, C. Diaz, J. Anderson, M. White, M. E. Jerome, E. A. Johnson, J. A. Radke, C. J. Stoeckert, Jr., R. H. Waterston, S. W. Clifton, D. S. Roos, and L. D. Sibley.2003. Gene discovery in the Apicomplexa as revealed by EST sequencing and assembly of a comparative gene database. Genome Res. 13:443-454.
37. Liew, F. Y., and F. E. G. Cox.1991. Nonspecific defence mechanism: the role of nitric oxide. Immunol. Today 12:A17-A21.
38. Luft, B. J., and J. S. Remington.1992. Toxoplasmic encephalitis in AIDS. Clin. Infect. Dis. 15:211-222.
39. Manger, I. D., H. Adrian, S. Parmley, L. D. Sibley, M. Marra, L. Hillier, R. Waterston, and J. C. Boothroyd.1998. Expressed sequence tag analysis of the bradyzoite stage of Toxoplasma gondii: identification of developmentally regulated genes. Infect. Immun. 66:1632-1637.
40. Mun, H. S., F. Aosai, K. Norose, L. X. Piao, H. Fang, S. Akira, and A. Yano. 2005. Toll-like receptor 4 mediates tolerance in macrophages stimulated with Toxoplasma gondii-derived heat shock protein 70. Infect. Immun. 73:4634-4642.
41. Navia, B. A., C. K. Petito, J. W. Gold, E. S. Cho, B. D. Jordan, and R. W. Price.1986. Cerebral toxoplasmosis complicating the acquired immune de-ficiency syndrome: clinical and neuropathological findings in 27 patients. Ann. Neurol. 19:224-238.
42. Nishikawa, Y., H. Zhang, H. M. Ibrahim, F. Ui, A. Ogiso, and X. Xuan.2008. Construction of Toxoplasma gondii bradyzoite expressing the green fluorescent protein. Parasitol. Int. 57:219-222.
43. Nishikawa, Y., X. Xuenan, L. Makala, O. Vielemeyer, K. A. Joiner, and H. Nagasawa.2003. Characterisation of Toxoplasma gondii engineered to express mouse interferon-gamma. Int. J. Parasitol. 33:1525-1535.
44. Radke, J. R., M. S. Behnke, A. J. Mackey, J. B. Radke, D. S. Roos, and M. W. White.2005. The transcriptome of Toxoplasma gondii. BMC Biol. 3:26.
45. Radke, J. R., R. G. Donald, A. Eibs, M. E. Jerome, M. S. Behnke, P. Liberator, and M. W. White.2006. Changes in the expression of human cell division autoantigen-1 influence Toxoplasma gondii growth and development. PLoS Pathog. 2:e105.
46. Scanga, C. A., J. Aliberti, D. Jankovic, F. Tilloy, S. Bennouna, E. Y. Denkers, R. Medzhitov, and A. Sher.2002. MyD88 is required for resistance to Toxoplasma gondii infection and regulates parasite-induced IL-12 production by dendritic cells. J. Immunol. 168:5997-6001.
47. 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 with the intracellular pathogen Toxoplasma gondii. J. Exp. Med. 185:1261-1273.
48. 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.
49. Schlüter, D., M. Deckert-Schlüter, E. Lorenz, T. Meyer, M. Röllinghoff, and C. Bogdan.1999. Inhibition of inducible nitric oxide synthase exacerbates chronic cerebral toxoplasmosis in Toxoplasma gondii-susceptible C57BL/6 mice but does not reactivate the latent disease in T. gondii-resistant BALB/c mice. J. Immunol. 162:3512-3518.
50. Sibley, L. D., L. B. Adams, Y. Fukotomi, and J. L. Krahenbuhl.1991. Tumor necrosis factor alpha triggers antitoxoplasmal activity of IFN-gamma primed macrophages. J. Immunol. 147:2340-2345.
51. Silva, N. M., W. L. Tafuri, J. I. Alvarez-Leite, J. R. Mineo, and R. T. Gazzinelli.2002. Toxoplasma gondii: in vivo expression of BAG-5 and cyst formation is independent of TNF p55 receptor and inducible nitric oxide synthase functions. Microbes Infect. 4:261-270.
52. Soête, M., and J. F. Dubremetz.1996. Toxoplasma gondii: kinetics of stage-specific protein expression during tachyzoite-bradyzoite conversion in vitro. Curr. Top. Microbiol. Immunol. 219:76-80.
53. Soête, M., B. Fortier, D. Camus, and J. F. Dubremetz.1993. Toxoplasma gondii: kinetics of bradyzoite-tachyzoite interconversion in vitro. Exp. Parasitol. 76:259-264.
54. Soête, M., D. Camus, and J. F. Dubremetz.1994. Experimental induction of bradyzoite-specific antigen expression and cyst formation by the RH strain of Toxoplasma gondii in vitro. Exp. Parasitol. 78:361-370.
55. Sullivan, W. J. J., J. Narasimhan, M. M. Bhatti, and R. C. Wek.2004. Parasite-specific eIF2 (eukaryotic initiation factor-2) kinase required for stress-induced translation control. Biochem. J. 380:523-531.
56. Suzuki, Y., F. K. Conley, and J. S. Remington.1990. Treatment of toxoplasmic encephalitis in mice with recombinant gamma interferon. Infect. Immun. 58:3050-3055.
57. 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.
58. Tomavo, S., and J. C. Boothroyd.1995. Interconnection between organellar functions, development and drug resistance in the protozoan parasite, Toxoplasma gondii. Int. J. Parasitol. 25:1293-1299.
59. Tuo, W., R. Fetterer, M. Jenkins, and J. P. Dubey.2005. Identification and characterization of Neospora caninum cyclophilin that elicits gamma interferon production. Infect. Immun. 73:5093-5100.
60. Ueno, A., G. Dautu, B. Munyaka, G. Carmen, Y. Kobayashi, and M. Igarashi. 2009. Toxoplasma gondii: identification and characterization of bradyzoite-specific deoxyribose phosphate aldolase-like gene (TgDPA). Exp. Parasitol. 121:55-63.
61. Vercesi, A. E., C. O. Rodrigues, S. A. Uyemura, L. Zhong, and S. N. Moreno. 1998. Respiration and oxidative phosphorylation in the apicomplexan parasite Toxoplasma gondii. J. Biol. Chem. 273:31040-31047.
62. Yarovinsky, F., D. Zhang, J. F. Andersen, G. L. Bannenberg, C. N. Serhan, M. S. Hayden, S. Hieny, F. S. Sutterwala, R. A. Flavell, S. Ghosh, and A. Sher.2005. TLR11 activation of dendritic cells by a protozoan profilin-like protein. Science 308:1626-1629.
63. Yarovinsky, F., J. F. Andersen, L. R. King, P. Caspar, J. Aliberti, H. Golding, and A. Sher.2004. Structural determinants of the anti-HIV activity of a CCR5 antagonist derived from Toxoplasma gondii. J. Biol. Chem. 279:53635-53642.