Toxoplasma polymorphic effectors determine macrophage polarization and intestinal inflammation

Cell Host and Microbe

Volumn 9, Issue 6, 2011, Pages 472-483

  Jensen, Kirk D C ^a,d   Wang, Yiding ^a,b   Wojno, Elia D Tait ^c   Shastri, Anjali J ^d   Hu, Kenneth ^a   Cornel, Lara ^a,b   Boedec, Erwan ^a,e   Ong, Yi Ching ^d   Chien, Yueh Hsiu ^d   Hunter, Christopher A ^c   Boothroyd, John C ^d   Saeij, Jeroen P J ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b WAGENINGEN UNIVERSITY   (Netherlands)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d STANFORD UNIVERSITY   (United States)

^e UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GRANULE ANTIGEN 15; PLASMA PROTEIN; RHOPTRY PROTEIN 16; UNCLASSIFIED DRUG;

ARTICLE; CELL ACTIVATION; DNA POLYMORPHISM; GENE CONTROL; GENE EXPRESSION; HOST RESISTANCE; ILEITIS; MACROPHAGE; POLARIZATION; PRIORITY JOURNAL; TOXOPLASMA; TOXOPLASMOSIS;

ANIMALS; CELL LINE; FEMALE; HUMANS; INTESTINES; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; MICE, INBRED C57BL; PROTOZOAN PROTEINS; SPECIES SPECIFICITY; TOXOPLASMA; TOXOPLASMOSIS;

MUS; TOXOPLASMA; TOXOPLASMA GONDII;

EID: 79958695985     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2011.04.015     Document Type: Article

References (42)

1. Bierly, A.L., Shufesky, W.J., Sukhumavasi, W., Morelli, A.E., and Denkers, E.Y. (2008). Dendritic cells expressing plasmacytoid marker PDCA-1 are Trojan horses during Toxoplasma gondii infection. J. Immunol. 181, 8485-8491.
2. Biswas, S.K., and Mantovani, A. (2010). Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat. Immunol. 11, 889-896.
3. Boothroyd, J.C., and Grigg, M.E. (2002). Population biology of Toxoplasma gondii and its relevance to human infection: do different strains cause different disease? Curr. Opin. Microbiol. 5, 438-442.
4. Cook, T., Roos, D., Morada, M., Zhu, G., Keithly, J.S., Feagin, J.E., Wu, G., and Yarlett, N. (2007). Divergent polyamine metabolism in the Apicomplexa. Microbiology 153, 1123-1130. (Pubitemid 46605810)
5. Corraliza, I.M., Campo, M.L., Soler, G., and Modolell, M. (1994). Determination of arginase activity in macrophages: a micromethod. J. Immunol. Methods 174, 231-235. (Pubitemid 24297154)
6. Dunay, I.R., Damatta, R.A., Fux, B., Presti, R., Greco, S., Colonna, M., and Sibley, L.D. (2008). Gr1(+) inflammatory monocytes are required for mucosal resistance to the pathogen Toxoplasma gondii. Immunity 29, 306-317.
7. El Kasmi, K.C., Qualls, J.E., Pesce, J.T., Smith, A.M., Thompson, R.W., Henao-Tamayo, M., Basaraba, R.J., Konig, T., Schleicher, U., Koo, M.S., et al. (2008). Toll-like receptor-induced arginase 1 in macrophages thwarts effective immunity against intracellular pathogens. Nat. Immunol. 9, 1399-1406.
8. Fentress, S.J., Behnke, M.S., Dunay, I.R., Mashayekhi, M., Rommereim, L.M., Fox, B.A., Bzik, D.J., Taylor, G.A., Turk, B.E., Lichti, C.F., et al. (2010). Phosphorylation of immunity-related GTPases by a Toxoplasma gondii-secreted kinase promotes macrophage survival and virulence. Cell Host Microbe 8, 484-495.
9. Gazzinelli, R.T., Wysocka, M., Hieny, S., Scharton-Kersten, T., Cheever, A., Kuhn, R., Muller, W., Trinchieri, G., and Sher, A. (1996). In the absence of endogenous IL-10, mice acutely infected with Toxoplasma gondii succumb to a lethal immune response dependent on CD4+ T cells and accompanied by overproduction of IL-12, IFN-gamma and TNF- alpha. J. Immunol. 157, 798-805.
10. Gordon, S. (2003). Alternative activation of macrophages. Nat. Rev. Immunol. 3, 23-35.
11. Grigg, M.E., Ganatra, J., Boothroyd, J.C., and Margolis, T.P. (2001). Unusual abundance of atypical strains associated with human ocular toxoplasmosis. J. Infect. Dis. 184, 633-639.
12. Iniesta, V., Gomez-Nieto, L.C., and Corraliza, I. (2001). The inhibition of arginase by N(omega)-hydroxy-l-arginine controls the growth of Leishmania inside macrophages. J. Exp. Med. 193, 777-784.
13. John, B., Harris, T.H., Tait, E.D., Wilson, E.H., Gregg, B., Ng, L.G., Mrass, P., Roos, D.S., Dzierszinski, F., Weninger, W., and Hunter, C.A. (2009). Dynamic Imaging of CD8(+) T cells and dendritic cells during infection with Toxoplasma gondii. PLoS Pathog. 5, e1000505. 10.1371/journal.ppat.1000505.
14. Liesenfeld, O., Kosek, J., Remington, J.S., and Suzuki, Y. (1996). Association of CD4+T cell-dependent, interferon-gamma-mediatednecrosis of thesmall intestine with genetic susceptibility of mice to peroral infection with Toxoplasma gondii. J. Exp. Med. 184, 597-607.
15. Martinez, F.O., Gordon, S., Locati, M., and Mantovani, A. (2006). Transcriptional profilingof thehumanmonocyte-to-macrophage differentiationandpolarization: new molecules and patterns of gene expression. J. Immunol. 177, 7303-7311. (Pubitemid 44715100)
16. Martinez, F.O., Helming, L., and Gordon, S. (2009). Alternative activation of macrophages: an immunologic functional perspective. Annu. Rev. Immunol. 27, 451-483.
17. Medzhitov, R., and Horng, T. (2009). Transcriptional control of the inflammatory response. Nat. Rev. Immunol. 9, 692-703.
18. Mills, C.D., Kincaid, K., Alt, J.M., Heilman, M.J., and Hill, A.M. (2000). M-1/M-2 macrophages and the Th1/Th2 paradigm. J. Immunol. 164, 6166-6173. (Pubitemid 30408793)
19. Mordue, D.G., Monroy, F., La Regina, M., Dinarello, C.A., and Sibley, L.D. (2001). Acute toxoplasmosis leads to lethal overproduction of Th1 cytokines. J. Immunol. 167, 4574-4584. (Pubitemid 32954337)
20. Mordue, D.G., and Sibley, L.D. (2003). A novel population of Gr-1+-activated macrophages induced during acute toxoplasmosis. J. Leukoc. Biol. 74, 1015-1025.
21. Munoz, M., Heimesaat, M.M., Danker, K., Struck, D., Lohmann, U., Plickert, R., Bereswill, S., Fischer, A., Dunay, I.R., Wolk, K., et al. (2009). Interleukin (IL)-23 mediates Toxoplasma gondii-induced immunopathology in the gut via matrix-metalloproteinase-2 and IL-22 but independent of IL-17. J. Exp. Med. 206, 3047-3059.
22. Odegaard, J.I., Ricardo-Gonzalez, R.R., Goforth, M.H., Morel, C.R., Subramanian, V., Mukundan, L., Eagle, A.R., Vats, D., Brombacher, F., Ferrante, A.W., and Chawla, A. (2007). Macrophage-specific PPARgamma controls alternative activation and improves insulin resistance. Nature 447, 1116-1120. (Pubitemid 47014427)
23. Ong, Y.C., Reese, M.L., and Boothroyd, J.C. (2010). Toxoplasma rhoptry protein 16 (ROP16) subverts host function by direct tyrosine phosphorylation of STAT6. J. Biol. Chem. 285, 28731-28740.
24. Pesce, J.T., Ramalingam, T.R., Mentink-Kane, M.M., Wilson, M.S., El Kasmi, K.C., Smith, A.M., Thompson, R.W., Cheever, A.W., Murray, P.J., and Wynn, T.A. (2009). Arginase-1-expressing macrophages suppress Th2 cytokine-driven inflammation and fibrosis. PLoS Pathog. 5, e1000371. 10.1371/journal. ppat.1000371.
25. Reese, M.L., Zeiner, G.M., Saeij, J.P., Boothroyd, J.C., and Boyle, J.P. (2011). Polymorphic family of injected pseudokinases is paramount in Toxoplasma virulence. Proc. Natl. Acad. Sci. USA. Published online March 21, 2011.
26. Roach, J.C., Glusman, G., Rowen, L., Kaur, A., Purcell, M.K., Smith, K.D., Hood, L.E., and Aderem, A. (2005). The evolution of vertebrate Toll-like receptors. Proc. Natl. Acad. Sci. USA 102, 9577-9582.
27. Robben, P.M., Mordue, D.G., Truscott, S.M., Takeda, K., Akira, S., and Sibley, L.D. (2004). Production of IL-12 by macrophages infected with Toxoplasma gondii depends on the parasite genotype. J. Immunol. 172, 3686-3694. (Pubitemid 38337952)
28. Roberts, C.W., Ferguson, D.J., Jebbari, H., Satoskar, A., Bluethmann, H., and Alexander, J. (1996). Different roles for interleukin-4 during the course of Toxoplasma gondii infection. Infect. Immun. 64, 897-904.
29. Rosowski, E.E., Lu, D., Julien, L., Rodda, L., Gaiser, R.A., Jensen, K.D., and Saeij, J.P. (2011). Strain-specific activation of the NF-kappaB pathway by GRA15, a novel Toxoplasma gondii dense granule protein. J. Exp. Med. 208, 195-212.
30. Saeij, J.P., Boyle, J.P., Coller, S., Taylor, S., Sibley, L.D., Brooke-Powell, E.T., Ajioka, J.W., and Boothroyd, J.C. (2006). Polymorphic secreted kinases are key virulence factors in toxoplasmosis. Science 314, 1780-1783. (Pubitemid 44969090)
31. Saeij, J.P., Coller, S., Boyle, J.P., Jerome, M.E., White, M.W., and Boothroyd, J.C. (2007). Toxoplasma co-opts host gene expression by injection of a polymorphic kinase homologue. Nature 445, 324-327. (Pubitemid 46122820)
32. Scharton-Kersten, T.M., Yap, G., Magram, J., and Sher, A. (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.
33. Schroder, A.J., Pavlidis, P., Arimura, A., Capece, D., and Rothman, P.B. (2002). Cutting edge: STAT6 serves as a positive and negative regulator of gene expression in IL-4-stimulated B lymphocytes. J. Immunol. 168, 996-1000. (Pubitemid 34094461)
34. Shen, Z., Reznikoff, G., Dranoff, G., and Rock, K.L. (1997). Cloned dendritic cells can present exogenous antigens on both MHC class I and class II molecules. J. Immunol. 158, 2723-2730. (Pubitemid 127470530)
35. Sibley, L.D., and Ajioka, J.W. (2008). Population structure of Toxoplasma gondii: clonal expansion driven by infrequent recombination and selective sweeps. Annu. Rev. Microbiol. 62, 329-351.
36. Steinfeldt, T., Konen-Waisman, S., Tong, L., Pawlowski, N., Lamkemeyer, T., Sibley, L.D., Hunn, J.P., and Howard, J.C. (2010). Phosphorylation of mouse immunity-related GTPase (IRG) resistance proteins is an evasion strategy for virulent Toxoplasma gondii. PLoS Biol. 8, e1000576. 10.1371/journal.pbio. 1000576.
37. Stumhofer, J.S., Laurence, A., Wilson, E.H., Huang, E., Tato, C.M., Johnson, L.M., Villarino, A.V., Huang, Q., Yoshimura, A., Sehy, D., et al. (2006). Interleukin 27 negatively regulates the development of interleukin 17-producing T helper cells during chronic inflammation of the central nervous system. Nat. Immunol. 7, 937-945.
38. Suzuki, Y., and Joh, K. (1994). Effect of the strain of Toxoplasma gondii on the development of toxoplasmic encephalitis in mice treated with antibody to interferon- gamma. Parasitol. Res. 80, 125-130.
39. Tait, E.D., Jordan, K.A., Dupont, C.D., Harris, T.H., Gregg, B., Wilson, E.H., Pepper, M., Dzierszinski, F., Roos, D.S., and Hunter, C.A. (2010). Virulence of Toxoplasma gondii is associated with distinct dendritic cell responses and reduced numbers of activated CD8+ T cells. J. Immunol. 185, 1502-1512.
40. Taylor, S., Barragan, A., Su, C., Fux, B., Fentress, S.J., Tang, K., Beatty, W.L., Hajj, H.E., Jerome, M., Behnke, M.S., et al. (2006). A secreted serine-threonine kinase determines virulence in the eukaryotic pathogen Toxoplasma gondii. Science 314, 1776-1780. (Pubitemid 44969089)
41. Yarovinsky, F., Zhang, D., Andersen, J.F., Bannenberg, G.L., Serhan, C.N., Hayden, M.S., Hieny, S., Sutterwala, F.S., Flavell, R.A., Ghosh, S., and Sher, A. (2005). TLR11 activation of dendritic cells by a protozoan profilin-like protein. Science 308, 1626-1629. (Pubitemid 40807512)
42. Zimmermann, S., Murray, P.J., Heeg, K., and Dalpke, A.H. (2006). Induction of suppressor of cytokine signaling-1 by Toxoplasma gondii contributes to immune evasion in macrophages by blocking IFN-gamma signaling. J. Immunol. 176, 1840-1847. (Pubitemid 43134329)