The Toxoplasma pseudokinase ROP5 forms complexes with ROP18 and ROP17 kinases that synergize to control acute virulence in mice

Cell Host and Microbe

Volumn 15, Issue 5, 2014, Pages 537-550

  Etheridge, Ronald D ^a   Alaganan, Aditi ^a   Tang, Keliang ^a   Lou, Hua Jane ^b   Turk, Benjamin E ^b   Sibley, L David ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYME; GUANOSINE TRIPHOSPHATASE; RHOPTRY SECRETED KINASE 17; RHOPTRY SECRETED KINASE 18; RHOPTRY SECRETED KINASE 5; THREONINE; UNCLASSIFIED DRUG; VIRULENCE FACTOR; PROTEIN BINDING; PROTEIN SERINE THREONINE KINASE; PROTOZOAL PROTEIN;

ARTICLE; CELL VACUOLE; CHEMICAL ANALYSIS; ENZYME ACTIVITY; HOST RESISTANCE; INNATE IMMUNITY; MACROPHAGE; MOUSE; NONHUMAN; PARASITE CLEARANCE; PARASITE SURVIVAL; PARASITE VIRULENCE; PRIORITY JOURNAL; PROTEIN PURIFICATION; TOXOPLASMA GONDII; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; ENZYMOLOGY; GENETICS; HOST PARASITE INTERACTION; HUMAN; METABOLISM; MOLECULAR GENETICS; PARASITOLOGY; PATHOGENICITY; SEQUENCE ALIGNMENT; TOXOPLASMA; TOXOPLASMOSIS; VIRULENCE;

AMINO ACID SEQUENCE; ANIMALS; GTP PHOSPHOHYDROLASES; HOST-PARASITE INTERACTIONS; HUMANS; MICE; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; PROTOZOAN PROTEINS; SEQUENCE ALIGNMENT; TOXOPLASMA; TOXOPLASMOSIS; VIRULENCE;

EID: 84901029147     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2014.04.002     Document Type: Article

References (41)

1. A. Alaganan, S.J. Fentress, K. Tang, Q. Wang, and L.D. Sibley Toxoplasma GRA7 effector increases turnover of immunity-related GTPases and contributes to acute virulence in the mouse Proc. Natl. Acad. Sci. USA 111 2014 1126 1131
2. M.S. Behnke, A. Khan, J.C. Wootton, J.P. Dubey, K. Tang, and L.D. Sibley Virulence differences in Toxoplasma mediated by amplification of a family of polymorphic pseudokinases Proc. Natl. Acad. Sci. USA 108 2011 9631 9636
3. M.S. Behnke, S.J. Fentress, M. Mashayekhi, L.X. Li, G.A. Taylor, and L.D. Sibley The polymorphic pseudokinase ROP5 controls virulence in Toxoplasma gondii by regulating the active kinase ROP18 PLoS Pathog. 8 2012 e1002992
4. P.J. Bradley, C. Ward, S.J. Cheng, D.L. Alexander, S. Coller, G.H. Coombs, J.D. Dunn, D.J. Ferguson, S.J. Sanderson, J.M. Wastling, and J.C. Boothroyd Proteomic analysis of rhoptry organelles reveals many novel constituents for host-parasite interactions in Toxoplasma gondii J. Biol. Chem. 280 2005 34245 34258
5. D. Degrandi, E. Kravets, C. Konermann, C. Beuter-Gunia, V. Klümpers, S. Lahme, E. Wischmann, A.K. Mausberg, S. Beer-Hammer, and K. Pfeffer Murine guanylate binding protein 2 (mGBP2) controls Toxoplasma gondii replication Proc. Natl. Acad. Sci. USA 110 2013 294 299
6. J.P. Dubey Toxoplasmosis of animals and humans 2010 CRC Press Boca Raton
7. J.D. Dunn, S. Ravindran, S.K. Kim, and J.C. Boothroyd The Toxoplasma gondii dense granule protein GRA7 is phosphorylated upon invasion and forms an unexpected association with the rhoptry proteins ROP2 and ROP4 Infect. Immun. 76 2008 5853 5861
8. S.J. Fentress, and L.D. Sibley The secreted kinase ROP18 defends Toxoplasma's border Bioessays 33 2011 693 700
9. S.J. Fentress, M.S. Behnke, I.R. Dunay, M. Mashayekhi, L.M. Rommereim, B.A. Fox, D.J. Bzik, G.A. Taylor, B.E. Turk, and C.F. Lichti et al. Phosphorylation of immunity-related GTPases by a Toxoplasma gondii-secreted kinase promotes macrophage survival and virulence Cell Host Microbe 8 2010 484 495
10. M.C. Fleckenstein, M.L. Reese, S. Könen-Waisman, J.C. Boothroyd, J.C. Howard, and T. Steinfeldt A Toxoplasma gondii pseudokinase inhibits host IRG resistance proteins PLoS Biol. 10 2012 e1001358
11. S. Håkansson, A.J. Charron, and L.D. Sibley Toxoplasma evacuoles: a two-step process of secretion and fusion forms the parasitophorous vacuole EMBO J. 20 2001 3132 3144
12. A.K. Haldar, H.A. Saka, A.S. Piro, J.D. Dunn, S.C. Henry, G.A. Taylor, E.M. Frickel, R.H. Valdivia, and J. Coers IRG and GBP host resistance factors target aberrant, "non-self" vacuoles characterized by the missing of "self" IRGM proteins PLoS Pathog. 9 2013 e1003414
13. S.K. Hanks, and T. Hunter Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification FASEB J. 9 1995 576 596
14. J.C. Howard, J.P. Hunn, and T. Steinfeldt The IRG protein-based resistance mechanism in mice and its relation to virulence in Toxoplasma gondii Curr. Opin. Microbiol. 14 2011 414 421
15. C.A. Hunter, and L.D. Sibley Modulation of innate immunity by Toxoplasma gondii virulence effectors Nat. Rev. Microbiol. 10 2012 766 778
16. A. Khaminets, J.P. Hunn, S. Könen-Waisman, Y.O. Zhao, D. Preukschat, J. Coers, J.P. Boyle, Y.C. Ong, J.C. Boothroyd, G. Reichmann, and J.C. Howard Coordinated loading of IRG resistance GTPases on to the Toxoplasma gondii parasitophorous vacuole Cell. Microbiol. 12 2010 939 961
17. A. Khan, S. Taylor, C. Su, A.J. Mackey, J. Boyle, R.H. Cole, D. Glover, K. Tang, I.T. Paulsen, and M. Berriman et al. Composite genome map and recombination parameters derived from three archetypal lineages of Toxoplasma gondii Nucleic Acids Res. 33 2005 2980 2992
18. B.H. Kim, A.R. Shenoy, P. Kumar, C.J. Bradfield, and J.D. MacMicking IFN-inducible GTPases in host cell defense Cell Host Microbe 12 2012 432 444
19. J.D. MacMicking Interferon-inducible effector mechanisms in cell-autonomous immunity Nat. Rev. Immunol. 12 2012 367 382
20. J.D. MacMicking, C. Nathan, G. Hom, N. Chartrain, D.S. Fletcher, M. Trumbauer, K. Stevens, Q.W. Xie, K. Sokol, and N. Hutchinson et al. Altered responses to bacterial infection and endotoxic shock in mice lacking inducible nitric oxide synthase Cell 81 1995 641 650
21. S.F. Parmley, S. Yang, G. Harth, L.D. Sibley, A. Sucharczuk, and J.S. Remington Molecular characterization of a 65-kilodalton Toxoplasma gondii antigen expressed abundantly in the matrix of tissue cysts Mol. Biochem. Parasitol. 66 1994 283 296
22. L. Peixoto, F. Chen, O.S. Harb, P.H. Davis, D.P. Beiting, C.S. Brownback, D. Ouloguem, and D.S. Roos Integrative genomic approaches highlight a family of parasite-specific kinases that regulate host responses Cell Host Microbe 8 2010 208 218
23. J.D. Pollock, D.A. Williams, M.A. Gifford, L.L. Li, X. Du, J. Fisherman, S.H. Orkin, C.M. Doerschuk, and M.C. Dinauer Mouse model of X-linked chronic granulomatous disease, an inherited defect in phagocyte superoxide production Nat. Genet. 9 1995 202 209
24. O. Puig, F. Caspary, G. Rigaut, B. Rutz, E. Bouveret, E. Bragado-Nilsson, M. Wilm, and B. Séraphin The tandem affinity purification (TAP) method: a general procedure of protein complex purification Methods 24 2001 218 229
25. M.L. Reese, and J.C. Boothroyd A helical membrane-binding domain targets the Toxoplasma ROP2 family to the parasitophorous vacuole Traffic 10 2009 1458 1470
26. M.L. Reese, and J.C. Boothroyd A conserved non-canonical motif in the pseudoactive site of the ROP5 pseudokinase domain mediates its effect on Toxoplasma virulence J. Biol. Chem. 286 2011 29366 29375
27. M.L. Reese, G.M. Zeiner, J.P. Saeij, J.C. Boothroyd, and J.P. Boyle Polymorphic family of injected pseudokinases is paramount in Toxoplasma virulence Proc. Natl. Acad. Sci. USA 108 2011 9625 9630
28. J.P.J. Saeij, J.P. Boyle, S. Coller, S. Taylor, L.D. Sibley, E.T. Brooke-Powell, J.W. Ajioka, and J.C. Boothroyd Polymorphic secreted kinases are key virulence factors in toxoplasmosis Science 314 2006 1780 1783
29. E.M. Selleck, S.J. Fentress, W.L. Beatty, D. Degrandi, K. Pfeffer, H.W. Virgin 4th, J.D. Macmicking, and L.D. Sibley Guanylate-binding protein 1 (Gbp1) contributes to cell-autonomous immunity against Toxoplasma gondii PLoS Pathog. 9 2013 e1003320
30. L.D. Sibley, and J.W. Ajioka Population structure of Toxoplasma gondii: clonal expansion driven by infrequent recombination and selective sweeps Annu. Rev. Microbiol. 62 2008 329 351
31. T. Steinfeldt, S. Könen-Waisman, L. Tong, N. Pawlowski, T. Lamkemeyer, L.D. Sibley, J.P. Hunn, and J.C. Howard Phosphorylation of mouse immunity-related GTPase (IRG) resistance proteins is an evasion strategy for virulent Toxoplasma gondii PLoS Biol. 8 2010 e1000576
32. C. Su, D.K. Howe, J.P. Dubey, J.W. Ajioka, and L.D. Sibley Identification of quantitative trait loci controlling acute virulence in Toxoplasma gondii Proc. Natl. Acad. Sci. USA 99 2002 10753 10758
33. G.A. Taylor, C.M. Collazo, G.S. Yap, K. Nguyen, T.A. Gregorio, L.S. Taylor, B. Eagleson, L. Secrest, E.A. Southon, and S.W. Reid et al. Pathogen-specific loss of host resistance in mice lacking the IFN-gamma-inducible gene IGTP Proc. Natl. Acad. Sci. USA 97 2000 751 755
34. S. Taylor, A. Barragan, C. Su, B. Fux, S.J. Fentress, K. Tang, W.L. Beatty, H.E. Hajj, M. Jerome, and M.S. Behnke et al. A secreted serine-threonine kinase determines virulence in the eukaryotic pathogen Toxoplasma gondii Science 314 2006 1776 1780
35. G.A. Taylor, C.G. Feng, and A. Sher Control of IFN-gamma-mediated host resistance to intracellular pathogens by immunity-related GTPases (p47 GTPases) Microbes Infect. 9 2007 1644 1651
36. B.E. Turk, J.E. Hutti, and L.C. Cantley Determining protein kinase substrate specificity by parallel solution-phase assay of large numbers of peptide substrates Nat. Protoc. 1 2006 375 379
37. N.F.J. van Poppel, J. Welagen, R.F.J.J. Duisters, A.N. Vermeulen, and D. Schaap Tight control of transcription in Toxoplasma gondii using an alternative tet repressor Int. J. Parasitol. 36 2006 443 452
38. M. Yamamoto, J.S. Ma, C. Mueller, N. Kamiyama, H. Saiga, E. Kubo, T. Kimura, T. Okamoto, M. Okuyama, and H. Kayama et al. ATF6beta is a host cellular target of the Toxoplasma gondii virulence factor ROP18 J. Exp. Med. 208 2011 1533 1546
39. M. Yamamoto, M. Okuyama, J.S. Ma, T. Kimura, N. Kamiyama, H. Saiga, J. Ohshima, M. Sasai, H. Kayama, and T. Okamoto et al. A cluster of interferon-γ-inducible p65 GTPases plays a critical role in host defense against Toxoplasma gondii Immunity 37 2012 302 313
40. G.S. Yap, and A. Sher Effector cells of both nonhemopoietic and hemopoietic origin are required for interferon (IFN)-gamma- and tumor necrosis factor (TNF)-alpha-dependent host resistance to the intracellular pathogen, Toxoplasma gondii J. Exp. Med. 189 1999 1083 1092
41. Y. Zhao, D.J. Ferguson, D.C. Wilson, J.C. Howard, L.D. Sibley, and G.S. Yap Virulent Toxoplasma gondii evade immunity-related GTPase-mediated parasite vacuole disruption within primed macrophages J. Immunol. 182 2009 3775 3781