Emerging themes in IFN-γ-induced macrophage immunity by the p47 and p65 GTPase families

Immunobiology

Volumn 212, Issue 9-10, 2008, Pages 771-784

  Shenoy, Avinash R ^a   Kim, Bae Hoon ^a   Choi, Han Pil ^a   Matsuzawa, Takeshi ^a   Tiwari, Sangeeta ^a   MacMicking, John D ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Autophagy; GBP; GTPase; IFN ; Macrophage; p47 IRG; Phagosome

Indexed keywords

GAMMA INTERFERON; GUANOSINE TRIPHOSPHATASE; P65 PROTEIN; PROTEIN P47; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ANTIBIOTIC RESISTANCE; ARTICLE; BIOCHEMISTRY; CELLULAR IMMUNITY; CHLAMYDIA TRACHOMATIS; EFFECTOR CELL; GENE EXPRESSION; GENOME; HOST RESISTANCE; HUMAN; INFECTION; INNATE IMMUNITY; LEISHMANIA MAJOR; LISTERIA MONOCYTOGENES; MACROPHAGE; MYCOBACTERIUM AVIUM; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; SALMONELLA TYPHIMURIUM; TOXOPLASMA GONDII; TRYPANOSOMA CRUZI; VERTEBRATE;

EID: 37049020693     PISSN: 01712985     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.imbio.2007.09.018     Document Type: Article

References (93)

1. Anderson S.L., Carton J.M., Lou J., Xing L., and Rubin B.Y. Interferon-induced guanylate binding protein-1 (GBP-1) mediates an antiviral effect against vesicular stomatitis virus and encephalomyocarditis virus. Virology 256 (1999) 8-14
2. 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
3. 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. USA 103 (2006) 14,092-14,097
4. 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
5. Briken V., Ruffner H., Schultz U., Schwarz A., Reis L.F., Strehlow I., Decker T., and Staeheli P. Interferon regulatory factor 1 is required for mouse Gbp gene activation by gamma interferon. Mol. Cell Biol. 15 (1995) 975-982
6. 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
7. 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
8. Carter C.C., Gorbacheva V.Y., and Vestal D.J. Inhibition of VSV and EMCV replication by the interferon-induced GTPase, mGBP-2: differential requirement for wild-type GTP binding domain. Arch. Virol. 150 (2005) 1213-1220
9. Chekmenev D.S., Haid C., and Kel A.E. P-Match: transcription factor binding site search by combining patterns and weight matrices. Nucleic Acids Res. 33 (2005) W432-W437
10. 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
11. 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
12. Colonno R.J., and Pang R.H. Induction of unique mRNAs by human interferons. J. Biol. Chem. 257 (1982) 9234-9237
13. Do C.B., Mahabhashyam M.S., Brudno M., and Batzoglou S. ProbCons: probabilistic consistency-based multiple sequence alignment. Genome Res. 15 (2005) 330-340
14. Doyle S., Vaidya S., O'Connell R., Dadgostar H., Dempsey P., Wu T., Rao G., Sun R., Haberland M., Modlin R., and Cheng G. IRF3 mediates a TLR3/TLR4-specific antiviral gene program. Immunity 17 (2002) 251-263
15. 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
16. Finbloom D.S., Hoover D.L., and Wahl L.M. The characteristics of binding of human recombinant interferon-gamma to its receptor on human monocytes and human monocyte-like cell lines. J. Immunol. 135 (1985) 300-305
17. Frank S.A. Immunology and Evolution of Infectious Disease (2002), Princeton University Press, Princeton, NJ
18. 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
19. 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
20. Ghosh A., Praefcke G.J., Renault L., Wittinghofer A., and Herrmann C. How guanylate-binding proteins achieve assembly-stimulated processive cleavage of GTP to GMP. Nature 440 (2006) 101-104
21. Gilly M., Damore M.A., and Wall R. A promoter ISRE and dual 5′ YY1 motifs control IFN-gamma induction of the IRG-47 G-protein gene. Gene 179 (1996) 237-244
22. Gorbacheva V.Y., Lindner D., Sen G.C., and Vestal D.J. The interferon (IFN)-induced GTPase, mGBP-2. Role in IFN-gamma-induced murine fibroblast proliferation. J. Biol. Chem. 277 (2002) 6080-6087
23. Gutierrez M.G., Master S.S., Singh S.B., Taylor G.A., Colombo M.I., and Deretic V. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 119 (2004) 753-766
24. 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
25. Han B.H., Park D.J., Lim R.W., Im J.H., and Kim H.D. Cloning, expression, and characterization of a novel guanylate-binding protein, GBP3 in murine erythroid progenitor cells. Biochim. Biophys. Acta 19 (1998) 373-386
26. Hemmi H., Takeuchi O., Sato S., Yamamoto M., Kaisho T., Sanjo H., Kawai T., Hoshino K., Takeda K., and Akira S. The roles of two IkappaB kinase-related kinases in lipopolysaccharide and double stranded RNA signaling and viral infection. J. Exp. Med. 199 (2004) 1641-1650
27. Henikoff S., and Henikoff J.G. Automated assembly of protein blocks for database searching. Nucleic Acids Res. 19 (1991) 6565-6572
28. Honda K., and Taniguchi T. IRFs: master regulators of signalling by Toll-like receptors and cytosolic pattern-recognition receptors. Nat. Rev. Immunol. 6 (2006) 644-658
29. Itsui Y., Sakamoto N., Kurosaki M., Kanazawa N., Tanabe Y., Koyama T., Takeda Y., Nakagawa M., Kakinuma S., Sekine Y., Maekawa S., Enomoto N., and Watanabe M. Expressional screening of interferon-stimulated genes for antiviral activity against hepatitis C virus replication. J. Viral Hepat. 13 (2006) 690-700
30. Kaiser F., Kaufmann S.H., and Zerrahn J. IIGP, a member of the IFN inducible and microbial defense mediating 47 kDa GTPase family, interacts with the microtubule binding protein hook3. J. Cell Sci. 117 (2004) 1747-1756
31. Kumar S., Tamura K., and Nei M. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform. 5 (2004) 150-163
32. Kunzelmann S., Praefcke G.J., and Herrmann C. Nucleotide binding and self-stimulated GTPase activity of human guanylate-binding protein 1 (hGBP1). Methods Enzymol. 404 (2005) 512-527
33. Lapaque N., Takeuchi O., Corrales F., Akira S., Moriyon I., Howard J.C., and Gorvel J.P. Differential inductions of TNF-alpha and IGTP, IIGP by structurally diverse classic and non-classic lipopolysaccharides. Cell Microbiol. 8 (2006) 401-413
34. Lew D.J., Decker T., Strehlow I., and Darnell J.E. Overlapping elements in the guanylate-binding protein gene promoter mediate transcriptional induction by alpha and gamma interferons. Mol. Cell Biol. 11 (1991) 182-191
35. Lieberman L.A., Banica M., Reiner S.L., and Hunter C.A. STAT1 plays a critical role in the regulation of antimicrobial effector mechanisms, but not in the development of Th1-type responses during toxoplasmosis. J. Immunol. 172 (2004) 457-463
36. 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
37. MacMicking J.D. IFN-inducible GTPases and immunity to intracellular pathogens. Trends Immunol. 25 (2004) 601-609
38. MacMicking J.D. Immune control of phagosomal bacteria by p47 GTPases. Curr. Opin. Microbiol. 8 (2005) 74-82
39. MacMicking J., Xie Q.W., and Nathan C. Nitric oxide and macrophage function. Annu. Rev. Immunol. 15 (1997) 323-350
40. 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
41. Martens S., and Howard J. The interferon-inducible GTPases. Annu. Rev. Cell Dev. Biol. 22 (2006) 559-589
42. 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
43. 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 Pathog. 1 (2005) e24
44. Mascie-Taylor C.G., and Karim E. The burden of chronic disease. Science 302 (2003) 1921-1922
45. McCaffrey R.L., Fawcett P., O'Riordan M., Lee K.D., Havell E.A., Brown P.O., and Portnoy D.A. A specific gene expression program triggered by Gram-positive bacteria in the cytosol. Proc. Natl. Acad. Sci. USA 101 (2004) 11,386-11,391
46. Modiano N., Lu Y.E., and Cresswell P. Golgi targeting of human guanylate-binding protein-1 requires nucleotide binding, isoprenylation, and an IFN-gamma-inducible cofactor. Proc. Natl. Acad. Sci. USA 102 (2005) 8680-8685
47. Nantais D.E., Schwemmle M., Stickney J.T., Vestal D.J., and Buss J.E. Prenylation of an interferon-gamma-induced GTP-binding protein: the human guanylate binding protein, huGBP1. J. Leukoc. Biol. 60 (1996) 423-431
48. Naschberger E., Werner T., Vicente A.B., Guenzi E., Topolt K., Leubert R., Lubeseder-Martellato C., Nelson P.J., and Sturzl M. Nuclear factor-kappaB motif and interferon-alpha-stimulated response element co-operate in the activation of guanylate-binding protein-1 expression by inflammatory cytokines in endothelial cells. Biochem. J. 379 (2004) 409-420
49. Nathan C.F., Murray H.W., Wiebe M.E., and Rubin B.Y. Identification of interferon-gamma as the lymphokine that activates human macrophage oxidative metabolism and antimicrobial activity. J. Exp. Med. 158 (1983) 670-689
50. Nathan C.F., Prendergast T.J., Wiebe M.E., Stanley E.R., Platzer E., Remold H.G., Welte K., Rubin B.Y., and Murray H.W. Activation of human macrophages. Comparison of other cytokines with interferon-gamma. J. Exp. Med. 160 (1984) 600-605
51. Nathan C., and Shiloh M.U. Reactive oxygen and nitrogen intermediates and the relationship between mammalian hosts and microbial pathogens. Proc. Natl. Acad. Sci. USA 97 (2000) 8841-8848
52. 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. USA 102 (2005) 10,658-10,663
53. Neun R., Richter M.F., Staeheli P., and Schwemmle M. GTPase properties of the interferon-induced human guanylate-binding protein 2. FEBS Lett. 390 (1996) 69-72
54. Nguyen T.T., Hu Y., Widney D.P., Mar R.A., and Smith J.B. Murine GBP-5, a new member of the murine guanylate-binding protein family, is coordinately regulated with other GBPs in vivo and in vitro. J. Interferon Cytokine Res. 22 (2002) 899-909
55. Ni Z., Karaskov E., Yu T., Callaghan S.M., Der S., Park D.S., Xu Z., Pattenden S.G., and Bremner R. Apical role for BRG1 in cytokine-induced promoter assembly. Proc. Natl. Acad. Sci. USA 102 (2005) 14,611-14,616
56. Notredame C., Higgins D.G., and Heringa J. T-Coffee: a novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 302 (2000) 205-217
57. Olszewski M.A., Gray J., and Vestal D.J. In silico genomic analysis of the human and murine guanylate-binding protein (GBP) gene clusters. J. Interferon Cytokine Res. 26 (2006) 328-352
58. Pace J.L., Russell S.W., Schreiber R.D., Altman A., and Katz D.H. Macrophage activation: priming activity from a T-cell hybridoma is attributable to interferon-gamma. Proc. Natl. Acad. Sci. USA 80 (1983) 3782-3786
59. Pattenden S.G., Klose R., Karaskov E., and Bremner R. Interferon-gamma-induced chromatin remodeling at the CIITA locus is BRG1 dependent. EMBO J. 21 (2002) 1978-1986
60. Praefcke G.J., Kloep S., Benscheid U., Lilie H., Prakash B., and Herrmann C. Identification of residues in the human guanylate-binding protein 1 critical for nucleotide binding and cooperative GTP hydrolysis. J. Mol. Biol. 344 (2004) 257-269
61. Prakash B., Praefcke G.J., Renault L., Wittinghofer A., and Herrmann C. Structure of human guanylate-binding protein 1 representing a unique class of GTP-binding proteins. Nature 403 (2000) 567-571
62. Prakash B., Renault L., Praefcke G.J., Herrmann C., and Wittinghofer A. Triphosphate structure of guanylate-binding protein 1 and implications for nucleotide binding and GTPase mechanism. EMBO J. 19 (2000) 4555-4564
63. Sabeti P.C., Schaffner S.F., Fry B., Lohmueller J., Varilly P., Shamovsky O., Palma A., Mikkelsen T.S., Altshuler D., and Lander E.S. Positive natural selection in the human lineage. Science 312 (2006) 1614-1620
64. Santiago H.C., Feng C.G., Bafica A., Roffe E., Arantes R.M., Cheever A., Taylor G., Vieira 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
65. Scheffzek K., and Ahmadian M.R. GTPase activating proteins: structural and functional insights 18 years after discovery. Cell Mol. Life Sci. 62 (2005) 3014-3038
66. Schneider T.D., and Stephens R.M. Sequence logos: a new way to display consensus sequences. Nucl. Acids Res. 18 (1990) 6097-6100
67. Schroder K., Sweet M.J., and Hume D.A. Signal integration between IFNgamma and TLR signalling pathways in macrophages. Immunobiology 211 (2006) 511-524
68. Schwemmle M., and Staeheli P. The interferon-induced 67-kDa guanylate-binding protein (hGBP1) is a GTPase that converts GTP to GMP. J. Biol. Chem. 269 (1994) 11,299-11,305
69. Shi S., Nathan C., Schnappinger D., Drenkow J., Fuortes M., Block E., Ding A., Gingeras T.R., Schoolnik G., Akira S., Takeda K., and Ehrt S. MyD88 primes macrophages for full-scale activation by interferon-gamma yet mediates few responses to Mycobacterium tuberculosis. J. Exp. Med. 198 (2003) 987-997
70. Shotland Y., Kramer H., and Groisman E.A. The Salmonella SpiC protein targets the mammalian Hook3 protein function to alter cellular trafficking. Mol. Microbiol. 49 (2003) 1565-1576
71. 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
72. Skamene E., Schurr E., and Gros P. Infection genomics: Nramp1 as a major determinant for natural resistance to intracellular infections. Ann. Rev. Med. 49 (1998) 275-287
73. Snyder M., He W., and Zhang J.J. The DNA replication factor MCM5 is essential for Stat1-mediated transcriptional activation. Proc. Natl. Acad. Sci. USA 102 (2005) 14,444-14,539
74. 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. Leukoc. Biol. 58 (1995) 477-484
75. Sprang S.R. G proteins, effectors and GAPs: structure and mechanism. Curr. Opin. Struct. Biol. 7 (1997) 849-856
76. Sun D., and Ding A. MyD88-mediated stabilization of interferon-gamma-induced cytokine and chemokine mRNA. Nat. Immunol. 7 (2006) 375-381
77. Taylor G.A., Jeffers M., Largaespada D.A., Jenkins N.A., Copel 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. 23 (1996) 20,399-20,405
78. 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) 10,639-10,645
79. 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. USA 97 (2000) 751-755
80. Taylor G.A., Feng C.G., and Sher A. p47 GTPases: regulators of immunity to intracellular pathogens. Nat. Rev. Immunol. 4 (2004) 100-109
81. tenOever B.R., Ng S.-L., Chua M.A., McWhirter S.M., Garcia-Sastre A., and Maniatis T. Multiple functions of the IKK-related kinase IKKε in interferon-mediated antiviral activity. Science 315 (2007) 1274-1278
82. 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) 29,336-29,343
83. Varinou L., Ramsauer K., Karaghiosoff M., Kolbe T., Pfeffer K., Muller M., and Decker T. Phosphorylation of the Stat1 transactivation domain is required for full-fledged IFN-gamma-dependent innate immunity. Immunity 19 (2003) 793-802
84. Venter J.C., Adams M.D., Myers E.W., Li P.W., Mural R.J., Sutton G.G., Smith H.O., Yandell M., Evans C.A., Holt R.A., Gocayne J.D., Amanatides P., Ballew R.M., Huson D.H., Wortman J.R., Zhang Q., Kodira C.D., Zheng X.H., Chen L., Skupski M., Subramanian G., Thomas P.D., Zhang J., Gabor Miklos G.L., Nelson C., Broder S., Clark A.G., Nadeau J., McKusick V.A., Zinder N., Levine A.J., Roberts R.J., Simon M., Slayman C., Hunkapiller M., Bolanos R., Delcher A., Dew I., Fasulo D., Flanigan M., Florea L., Halpern A., Hannenhalli S., Kravitz S., Levy S., Mobarry C., Reinert K., Remington K., Abu-Threideh J., Beasley E., Biddick K., Bonazzi V., Brandon R., Cargill M., Chandramouliswaran I., Charlab R., Chaturvedi K., Deng Z., Di Francesco V., Dunn P., Eilbeck K., Evangelista C., Gabrielian A.E., Gan W., Ge W., Gong F., Gu Z., Guan P., Heiman T.J., Higgins M.E., Ji R.R., Ke Z., Ketchum K.A., Lai Z., Lei Y., Li Z., Li J., Liang Y., Lin X., Lu F., Merkulov G.V., Milshina N., Moore H.M., Naik A.K., Narayan V.A., Neelam B., Nusskern D., Rusch D.B., Salzberg S., Shao W., Shue B., Sun J., Wang Z., Wang A., Wang X., Wang J., Wei M., Wides R., Xiao C., Yan C., et al. The sequence of the human genome. Science 291 (2001) 1304-1351
85. Vestal D.J. The guanylate-binding proteins (GBPs): proinflammatory cytokine-induced members of the dynamin superfamily with unique GTPase activity. J. Interferon Cytokine Res. 25 (2005) 435-443
86. Vestal D.J., Gorbacheva V.Y., and Sen G.C. Different subcellular localizations for the related interferon-induced GTPases, MuGBP-1 and MuGBP-2: implications for different functions?. J. Interferon Cytokine Res. 20 (2000) 991-1000
87. Vetter I.R., and Wittinghofer A. The guanine nucleotide-binding switch in three dimensions. Science 294 (2001) 1299-1304
88. Waterston R.H., Lindblad-Toh K., Birney E., Rogers J., Abril J.F., Agarwal P., Agarwala R., Ainscough R., Alexandersson M., An P., Antonarakis S.E., Attwood J., Baertsch R., Bailey J., Barlow K., Beck S., Berry E., Birren B., Bloom T., Bork P., Botcherby M., Bray N., Brent M.R., Brown D.G., Brown S.D., Bult C., Burton J., Butler J., Campbell R.D., Carninci P., Cawley S., Chiaromonte F., Chinwalla A.T., Church D.M., Clamp M., Clee C., Collins F.S., Cook L.L., Copley R.R., Coulson A., Couronne O., Cuff J., Curwen V., Cutts T., Daly M., David R., Davies J., Delehaunty K.D., Deri J., Dermitzakis E.T., Dewey C., Dickens N.J., Diekhans M., Dodge S., Dubchak I., Dunn D.M., Eddy S.R., Elnitski L., Emes R.D., Eswara P., Eyras E., Felsenfeld A., Fewell G.A., Flicek P., Foley K., Frankel W.N., Fulton L.A., Fulton R.S., Furey T.S., Gage D., Gibbs R.A., Glusman G., Gnerre S., Goldman N., Goodstadt L., Grafham D., Graves T.A., Green E.D., Gregory S., Guigo R., Guyer M., Hardison R.C., Haussler D., Hayashizaki Y., Hillier L.W., Hinrichs A., Hlavina W., Holzer T., Hsu F., Hua A., Hubbard T., Hunt A., Jackson I., Jaffe D.B., Johnson L.S., Jones M., Jones T.A., Joy A., Kamal M., Karlsson E.K., et al. Initial sequencing and comparative analysis of the mouse genome. Nature 420 (2002) 520-562
89. Weighardt H., Jusek G., Mages J., Lang R., Hoebe K., Beutler B., and Holzmann B. Identification of a TLR4- and TRIF-dependent activation program of dendritic cells. Eur. J. Immunol. 34 (2004) 558-564
90. Yamaguchi T., Omatsu N., Omukae A., and Osumi T. Analysis of interaction partners for perilipin and ADRP on lipid droplets. Mol. Cell. Biochem. 284 (2006) 167-173
91. Yates R.M., Hermetter A., Taylor G.A., and Russell D.G. Macrophage activation downregulates the degradative capacity of the phagosome. Traffic 8 (2007) 241-250
92. 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
93. 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) 33,011-33,019