Control of IFN-γ-mediated host resistance to intracellular pathogens by immunity-related GTPases (p47 GTPases)

Microbes and Infection

Volumn 9, Issue 14-15, 2007, Pages 1644-1651

  Taylor, Gregory A ^a   Feng, Carl G ^b   Sher, Alan ^b  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

GTPase; Innate immunity; Interferon

Indexed keywords

GAMMA INTERFERON; GUANOSINE TRIPHOSPHATASE; IMMUNITY RELATED GUANOSINE TRIPHOSPHATASE; PROTEIN P47; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL VACUOLE; CYTOKINE RELEASE; GENETIC CONSERVATION; HEMATOPOIESIS; HOST CELL; HOST RESISTANCE; HUMAN; IMMUNITY; INFECTION; INFECTION SENSITIVITY; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTOZOON; REGULATORY MECHANISM;

ANIMALS; BACTERIA; BACTERIAL INFECTIONS; GTP PHOSPHOHYDROLASES; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, NATURAL; INTERFERON TYPE II; MACROPHAGES; MICE; MICE, KNOCKOUT; PROTOZOA; PROTOZOAN INFECTIONS;

MUS; PROTOZOA;

EID: 36749064729     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2007.09.004     Document Type: Article

References (40)

1. Boehm U., Klamp T., Groot M., and Howard J.C. Cellular responses to interferon-gamma. Annu. Rev. Immunol. 15 (1997) 749-795
2. Stark G.R., Kerr I.M., Williams B.R., Silverman R.H., and Schreiber R.D. How cells respond to interferons. Annu. Rev. Biochem. 67 (1998) 227-264
3. Ehrt S., Schnappinger D., Bekiranov S., Drenkow J., Shi S., Gingeras T.R., Gaasterland T., Schoolnik G., and Nathan C. Reprogramming of the macrophage transcriptome in response to interferon-gamma and Mycobacterium tuberculosis: signaling roles of nitric oxide synthase-2 and phagocyte oxidase. J. Exp. Med. 194 (2001) 1123-1140
4. Martens S., and Howard J. The interferon-inducible GTPases. Annu. Rev. Cell Dev. Biol. 22 (2006) 559-589
5. MacMicking J.D. Immune control of phagosomal bacteria by p47 GTPases. Curr. Opin. Microbiol. 8 (2005) 74-82
6. MacMicking J.D. IFN-inducible GTPases and immunity to intracellular pathogens. Trends Immunol. 25 (2004) 601-609
7. Taylor G.A., Feng C.G., and Sher A. p47 GTPases: regulators of immunity to intracellular pathogens. Nat. Rev. Immunol. 4 (2004) 100-109
8. Bekpen C., Hunn J.P., Rohde C., Parvanova I., Guethlein L., Dunn D.M., Glowalla E., Leptin M., and Howard J.C. The interferon-inducible p47 (IRG) GTPases in vertebrates: loss of the cell autonomous resistance mechanism in the human lineage. Genome Biol. 6 (2005) R92
9. Singh S.B., Davis A.S., Taylor G.A., and Deretic V. Human IRGM induces autophagy to eliminate intracellular mycobacteria. Science 313 (2006) 1438-1441
10. Sorace J.M., Johnson R.J., Howard D.L., and Drysdale B.E. Identification of an endotoxin and IFN-inducible cDNA: possible identification of a novel protein family. J. Leukocyte Biol. 58 (1995) 477-484
11. Boehm U., Guethlein L., Klamp T., Ozbek K., Schaub A., Futterer A., Pfeffer K., and Howard J.C. Two families of GTPases dominate the complex cellular response to IFN-gamma. J Immunol. 161 (1998) 6715-6723
12. Taylor G.A., Jeffers M., Largaespada D.A., Jenkins N.A., Copeland N.G., and Woude G.F. Identification of a novel GTPase, the inducibly expressed GTPase, that accumulates in response to interferon gamma. J. Biol. Chem. 271 (1996) 20399-20405
13. Gilly M., and Wall R. The IRG-47HSP!gene is IFN-gamma induced in B cells and encodes a protein with GTP-binding motifs. J. Immunol. 148 (1992) 3275-3281
14. Carlow D.A., Marth J., Clark-Lewis I., and Teh H.S. Isolation of a gene encoding a developmentally regulated T cell-specific protein with a guanine nucleotide triphosphate-binding motif. J. Immunol. 154 (1995) 1724-1734
15. Lafuse W.P., Brown D., Castle L., and Zwilling B.S. Cloning and characterization of a novel cDNA that is IFN-gamma-induced in mouse peritoneal macrophages and encodes a putative GTP-binding protein. J. Leukocyte Biol. 57 (1995) 477-483
16. Bernstein-Hanley I., Coers J., Balsara Z.R., Taylor G.A., Starnbach M.N., and Dietrich W.F. The p47 GTPases Igtp and Irgb10 map to the Chlamydia trachomatis susceptibility locus Ctrq-3 and mediate cellular resistance in mice. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 14092-14097
17. Taylor G.A., Collazo C.M., Yap G.S., Nguyen K., Gregorio T.A., Taylor L.S., Eagleson B., Secrest L., Southon E.A., Reid S.W., Tessarollo L., Bray M., McVicar D.W., Komschlies K.L., Young H.A., Biron C.A., Sher A., and Vande Woude G.F. Pathogen-specific loss of host resistance in mice lacking the IFN-gamma-inducible gene IGTP. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 751-755
18. Collazo C.M., Yap G.S., Sempowski G.D., Lusby K.C., Tessarollo L., Woude G.F., Sher A., and Taylor G.A. Inactivation of LRG-47 and IRG-47 reveals a family of interferon gamma-inducible genes with essential, pathogen-specific roles in resistance to infection. J. Exp. Med. 194 (2001) 181-188
19. Zerrahn J., Schaible U.E., Brinkmann V., Guhlich U., and Kaufmann S.H. The IFN-inducible Golgi- and endoplasmic reticulum- associated 47-kDa GTPase IIGP is transiently expressed during listeriosis. J. Immunol. 168 (2002) 3428-3436
20. MacMicking J.D., Taylor G.A., and McKinney J.D. Immune control of tuberculosis by IFN-gamma-inducible LRG-47. Science 302 (2003) 654-659
21. Gavrilescu L.C., Butcher B.A., Del Rio L., Taylor G.A., and Denkers E.Y. STAT1 is essential for antimicrobial effector function but dispensable for gamma interferon production during Toxoplasma gondii infection. Infect. Immun. 72 (2004) 1257-1264
22. Collazo C.M., Yap G.S., Hieny S., Caspar P., Feng C.G., Taylor G.A., and Sher A. The function of gamma interferon-inducible GTP-binding protein IGTP in host resistance to Toxoplasma gondii is Stat1 dependent and requires expression in both hematopoietic and nonhematopoietic cellular compartments. Infect. Immun. 70 (2002) 6933-6939
23. Carlow D.A., Teh S.J., and Teh H.S. Specific antiviral activity demonstrated by TGTP, a member of a new family of interferon-induced GTPases. J. Immunol. 161 (1998) 2348-2355
24. Marks B., Stowell M.H., Vallis Y., Mills I.G., Gibson A., Hopkins C.R., and McMahon H.T. GTPase activity of dynamin and resulting conformation change are essential for endocytosis. Nature 410 (2001) 231-235
25. Taylor G.A., Stauber R., Rulong S., Hudson E., Pei V., Pavlakis G.N., Resau J.H., and Vande Woude G.F. The inducibly expressed GTPase localizes to the endoplasmic reticulum, independently of GTP binding. J. Biol. Chem. 272 (1997) 10639-10645
26. Uthaiah R.C., Praefcke G.J., Howard J.C., and Herrmann C. IIGP1, an interferon-gamma-inducible 47-kDa GTPase of the mouse, showing cooperative enzymatic activity and GTP-dependent multimerization. J. Biol. Chem. 278 (2003) 29336-29343
27. Ghosh A., Uthaiah R., Howard J., Herrmann C., and Wolf E. Crystal structure of IIGP1: a paradigm for interferon-inducible p47 resistance GTPases. Mol. Cell 15 (2004) 727-739
28. Wennerberg K., Rossman K.L., and Der C.J. The Ras superfamily at a glance. J. Cell Sci. 118 (2005) 843-846
29. Martens S., Sabel K., Lange R., Uthaiah R., Wolf E., and Howard J.C. 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 (2004) 2594-2606
30. Butcher B.A., Greene R.I., Henry S.C., Annecharico K.L., Weinberg J.B., Denkers E.Y., Sher A., and Taylor G.A. p47 GTPases regulate Toxoplasma gondii survival in activated macrophages. Infect. Immun. 73 (2005) 3278-3286
31. Martens S., Parvanova I., Zerrahn J., Griffiths G., Schell G., Reichmann G., and Howard J.C. Disruption of Toxoplasma gondii parasitophorous vacuoles by the mouse p47-resistance GTPases. PLoS Pathogens 1 (2005) e24
32. Ling Y.M., Shaw M.H., Ayala C., Coppens I., Taylor G.A., Ferguson D.J., and Yap G.S. Vacuolar and plasma membrane stripping and autophagic elimination of Toxoplasma gondii in primed effector macrophages. J. Exp. Med. 203 (2006) 2063-2071
33. Luft B.J., and Remington J.S. Toxoplasmic encephalitis in AIDS. Clin. Infect. Dis. 15 (1992) 211-222
34. Sibley L.D. Toxoplasma gondii: perfecting an intracellular life style. Traffic 4 (2003) 581-586
35. Halonen S.K., Taylor G.A., and Weiss L.M. Gamma interferon-induced inhibition of Toxoplasma gondii in astrocytes is mediated by IGTP. Infect. Immun. 69 (2001) 5573-5576
36. Santiago H.C., Feng C.G., Bafica A., Roffe E., Arantes R.M., Cheever A., Taylor G., Vierira L.Q., Aliberti J., Gazzinelli R.T., and Sher A. Mice deficient in LRG-47 display enhanced susceptibility to Trypanosoma cruzi infection associated with defective hemopoiesis and intracellular control of parasite growth. J. Immunol. 175 (2005) 8165-8172
37. Nelson D.E., Virok D.P., Wood H., Roshick C., Johnson R.M., Whitmire W.M., Crane D.D., Steele-Mortimer O., Kari L., McClarty G., and Caldwell H.D. Chlamydial IFN-gamma immune evasion is linked to host infection tropism. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 10658-10663
38. Hackstadt T., Scidmore M.A., and Rockey D.D. Lipid metabolism in Chlamydia trachomatis-infected cells: directed trafficking of Golgi-derived sphingolipids to the chlamydial inclusion. Proc. Natl. Acad. Sci. U.S.A. 92 (1995) 4877-4881
39. Feng C.G., Collazo-Custodio C.M., Eckhaus M., Hieny S., Belkaid Y., Elkins K., Jankovic D., Taylor G.A., and Sher A. Mice deficient in LRG-47 display increased susceptibility to mycobacterial infection associated with the induction of lymphopenia. J. Immunol. 172 (2004) 1163-1168
40. Zhang H.M., Yuan J., Cheung P., Luo H., Yanagawa B., Chau D., Stephan-Tozy N., Wong B.W., Zhang J., Wilson J.E., McManus B.M., and Yang D. Overexpression of interferon-gamma-inducible GTPase inhibits coxsackievirus B3-induced apoptosis through the activation of the phosphatidylinositol 3-kinase/Akt pathway and inhibition of viral replication. J. Biol. Chem. 278 (2003) 33011-33019