IRG and GBP Host Resistance Factors Target Aberrant, "Non-self" Vacuoles Characterized by the Missing of "Self" IRGM Proteins

PLoS Pathogens

Volumn 9, Issue 6, 2013, Pages

  Haldar, Arun K ^a   Saka, Hector A ^a   Piro, Anthony S ^a   Da Dunn, Joen ^a   Henry, Stanley C ^b,c   Taylor, Gregory A ^b,c   Frickel, Eva M ^d   Valdivia, Raphael H ^a   Coers, Jörn ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c DURHAM VA MEDICAL CENTER   (United States)

^d NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FAT DROPLET; GAMMA INTERFERON; GREEN FLUORESCENT PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE TRIPHOSPHATASE; IMMUNITY RELATED GTPASE 1; IMMUNITY RELATED GTPASE 3; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIGEN RECOGNITION; ARTICLE; CELL VACUOLE; CHLAMYDIA TRACHOMATIS; CONTROLLED STUDY; FLOW CYTOMETRY; GENETIC TRANSFECTION; HOST RESISTANCE; HUMAN; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; MOUSE; NONHUMAN; OLIGOMERIZATION; PROTEIN ASSEMBLY; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; TOXOPLASMA GONDII;

ANIMALS; CELL LINE; CHLAMYDIA INFECTIONS; CHLAMYDIA TRACHOMATIS; GTP PHOSPHOHYDROLASES; GTP-BINDING PROTEINS; IMMUNITY, INNATE; MICE; MICE, KNOCKOUT; TOXOPLASMA; TOXOPLASMOSIS; VACUOLES;

BACTERIA (MICROORGANISMS); CHLAMYDIA TRACHOMATIS; PROTOZOA; TOXOPLASMA GONDII;

EID: 84879547102     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003414     Document Type: Article

References (46)

1. Kumar Y, Valdivia RH, (2009) Leading a sheltered life: intracellular pathogens and maintenance of vacuolar compartments. Cell Host Microbe 5: 593-601.
2. Shahnazari S, Brumell JH, (2011) Mechanisms and consequences of bacterial targeting by the autophagy pathway. Curr Opin Microbiol 14: 68-75.
3. MacMicking JD, (2012) Interferon-inducible effector mechanisms in cell-autonomous immunity. Nat Rev Immunol 12: 367-382.
4. Schroder K, Hertzog PJ, Ravasi T, Hume DA, (2004) Interferon-gamma: an overview of signals, mechanisms and functions. J Leukoc Biol 75: 163-189.
5. Zhang SY, Boisson-Dupuis S, Chapgier A, Yang K, Bustamante J, et al. (2008) Inborn errors of interferon (IFN)-mediated immunity in humans: insights into the respective roles of IFN-alpha/beta, IFN-gamma, and IFN-lambda in host defense. Immunol Rev 226: 29-40.
6. Howard JC, Hunn JP, Steinfeldt T, (2011) The IRG protein-based resistance mechanism in mice and its relation to virulence in Toxoplasma gondii. Curr Opin Microbiol 14: 414-421.
7. Ling YM, Shaw MH, Ayala C, Coppens I, Taylor GA, et al. (2006) Vacuolar and plasma membrane stripping and autophagic elimination of Toxoplasma gondii in primed effector macrophages. J Exp Med 203: 2063-2071.
8. Gutierrez MG, Master SS, Singh SB, Taylor GA, Colombo MI, et al. (2004) Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 119: 753-766.
9. Singh SB, Davis AS, Taylor GA, Deretic V, (2006) Human IRGM induces autophagy to eliminate intracellular mycobacteria. Science 313: 1438-1441.
10. Singh SB, Ornatowski W, Vergne I, Naylor J, Delgado M, et al. (2010) Human IRGM regulates autophagy and cell-autonomous immunity functions through mitochondria. Nat Cell Biol 12: 1154-1165.
11. Butcher BA, Greene RI, Henry SC, Annecharico KL, Weinberg JB, et al. (2005) p47 GTPases regulate Toxoplasma gondii survival in activated macrophages. Infect Immun 73: 3278-3286.
12. Martens S, Sabel K, Lange R, Uthaiah R, Wolf E, et al. (2004) Mechanisms regulating the positioning of mouse p47 resistance GTPases LRG-47 and IIGP1 on cellular membranes: retargeting to plasma membrane induced by phagocytosis. J Immunol 173: 2594-2606.
13. Tiwari S, Choi HP, Matsuzawa T, Pypaert M, MacMicking JD, (2009) Targeting of the GTPase Irgm1 to the phagosomal membrane via PtdIns(3,4)P(2) and PtdIns(3,4,5)P(3) promotes immunity to mycobacteria. Nat Immunol 10: 907-917.
14. Melzer T, Duffy A, Weiss LM, Halonen SK, (2008) The gamma interferon (IFN-gamma)-inducible GTP-binding protein IGTP is necessary for toxoplasma vacuolar disruption and induces parasite egression in IFN-gamma-stimulated astrocytes. Infect Immun 76: 4883-4894.
15. Papic N, Hunn JP, Pawlowski N, Zerrahn J, Howard JC, (2008) Inactive and active states of the interferon-inducible resistance GTPase, Irga6, in vivo. J Biol Chem 283: 32143-32151.
16. Hunn JP, Koenen-Waisman S, Papic N, Schroeder N, Pawlowski N, et al. (2008) Regulatory interactions between IRG resistance GTPases in the cellular response to Toxoplasma gondii. EMBO J 27: 2495-2509.
17. Conrad C, Gerlich DW, (2010) Automated microscopy for high-content RNAi screening. J Cell Biol 188: 453-461.
18. Baird GS, Zacharias DA, Tsien RY, (2000) Biochemistry, mutagenesis, and oligomerization of DsRed, a red fluorescent protein from coral. Proc Natl Acad Sci U S A 97: 11984-11989.
19. Sacchetti A, Subramaniam V, Jovin TM, Alberti S, (2002) Oligomerization of DsRed is required for the generation of a functional red fluorescent chromophore. FEBS Lett 525: 13-19.
20. Roth JF, (2000) The yeast Ty virus-like particles. Yeast 16: 785-795.
21. Fang Y, Wu N, Gan X, Yan W, Morrell JC, et al. (2007) Higher-order oligomerization targets plasma membrane proteins and HIV gag to exosomes. PLoS Biol 5: e158.
22. Henry SC, Daniell XG, Burroughs AR, Indaram M, Howell DN, et al. (2009) Balance of Irgm protein activities determines IFN-gamma-induced host defense. J Leukoc Biol 85: 877-885.
23. Martens S, Parvanova I, Zerrahn J, Griffiths G, Schell G, et al. (2005) Disruption of Toxoplasma gondii parasitophorous vacuoles by the mouse p47-resistance GTPases. PLoS Pathog 1: e24.
24. Khaminets A, Hunn JP, Konen-Waisman S, Zhao YO, Preukschat D, et al. (2010) Coordinated loading of IRG resistance GTPases on to the Toxoplasma gondii parasitophorous vacuole. Cell Microbiol 12: 939-961.
25. Al-Zeer MA, Al-Younes HM, Braun PR, Zerrahn J, Meyer TF, (2009) IFN-gamma-inducible Irga6 mediates host resistance against Chlamydia trachomatis via autophagy. PLoS One 4: e4588.
26. Bougneres L, Helft J, Tiwari S, Vargas P, Chang BH, et al. (2009) A role for lipid bodies in the cross-presentation of phagocytosed antigens by MHC class I in dendritic cells. Immunity 31: 232-244.
27. Traver MK, Henry SC, Cantillana V, Oliver T, Hunn JP, et al. (2011) Immunity-related gtpase M (IRGM) proteins influence the localization of guanylate-binding protein 2 (GBP2) by modulating macroautophagy. J Biol Chem 286 (35) (): 30471-80.
28. Praefcke GJ, Kloep S, Benscheid U, Lilie H, Prakash B, et al. (2004) Identification of residues in the human guanylate-binding protein 1 critical for nucleotide binding and cooperative GTP hydrolysis. J Mol Biol 344: 257-269.
29. Kim BH, Shenoy AR, Kumar P, Das R, Tiwari S, et al. (2011) A family of IFN-gamma-inducible 65-kD GTPases protects against bacterial infection. Science 332: 717-721.
30. Ichimura Y, Komatsu M, (2010) Selective degradation of p62 by autophagy. Semin Immunopathol 32: 431-436.
31. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, et al. (2012) Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 8: 445-544.
32. Degrandi D, Konermann C, Beuter-Gunia C, Kresse A, Wurthner J, et al. (2007) Extensive characterization of IFN-induced GTPases mGBP1 to mGBP10 involved in host defense. J Immunol 179: 7729-7740.
33. Virreira Winter S, Niedelman W, Jensen KD, Rosowski EE, Julien L, et al. (2011) Determinants of GBP recruitment to Toxoplasma gondii vacuoles and the parasitic factors that control it. PLoS One 6: e24434.
34. Karre K, Ljunggren HG, Piontek G, Kiessling R, (1986) Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy. Nature 319: 675-678.
35. Kiessling V, Wan C, Tamm LK, (2009) Domain coupling in asymmetric lipid bilayers. Biochim Biophys Acta 1788: 64-71.
36. Britzen-Laurent N, Bauer M, Berton V, Fischer N, Syguda A, et al. (2010) Intracellular trafficking of guanylate-binding proteins is regulated by heterodimerization in a hierarchical manner. PLoS One 5: e14246.
37. Prakash B, Praefcke GJ, Renault L, Wittinghofer A, Herrmann C, (2000) Structure of human guanylate-binding protein 1 representing a unique class of GTP-binding proteins. Nature 403: 567-571.
38. Yamamoto M, Okuyama M, Ma JS, Kimura T, Kamiyama N, et al. (2012) A Cluster of Interferon-gamma-Inducible p65 GTPases Plays a Critical Role in Host Defense against Toxoplasma gondii. Immunity 37: 302-313.
39. Coers J, Bernstein-Hanley I, Grotsky D, Parvanova I, Howard JC, et al. (2008) Chlamydia muridarum evades growth restriction by the IFN-gamma-inducible host resistance factor Irgb10. J Immunol 180: 6237-6245.
40. Coers J, Gondek DC, Olive AJ, Rohlfing A, Taylor GA, et al. (2011) Compensatory T Cell Responses in IRG-Deficient Mice Prevent Sustained Chlamydia trachomatis Infections. PLoS Pathog 7: e1001346.
41. Coers J, Vance RE, Fontana MF, Dietrich WF, (2007) Restriction of Legionella pneumophila growth in macrophages requires the concerted action of cytokine and Naip5/Ipaf signalling pathways. Cell Microbiol 9: 2344-2357.
42. Wang Y, Kahane S, Cutcliffe LT, Skilton RJ, Lambden PR, et al. (2011) Development of a transformation system for Chlamydia trachomatis: restoration of glycogen biosynthesis by acquisition of a plasmid shuttle vector. PLoS Pathog 7: e1002258.
43. Kim SK, Karasov A, Boothroyd JC, (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.
44. Cocchiaro JL, Kumar Y, Fischer ER, Hackstadt T, Valdivia RH, (2008) Cytoplasmic lipid droplets are translocated into the lumen of the Chlamydia trachomatis parasitophorous vacuole. Proc Natl Acad Sci U S A 105: 9379-9384.
45. Taylor GA, Jeffers M, Largaespada DA, Jenkins NA, Copeland NG, et al. (1996) Identification of a novel GTPase, the inducibly expressed GTPase, that accumulates in response to interferon gamma. J Biol Chem 271: 20399-20405.
46. Scidmore MA, Hackstadt T, (2001) Mammalian 14-3-3beta associates with the Chlamydia trachomatis inclusion membrane via its interaction with IncG. Mol Microbiol 39: 1638-1650.