Regulation of innate immune functions by guanylate-binding proteins

International Journal of Medical Microbiology

Volumn 308, Issue 1, 2018, Pages 237-245

  Praefcke, Gerrit J K ^a,b  

^a PAUL EHRLICH INSTITUT   (Germany)

^b UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Autophagy; Guanylate binding proteins; Immunity related GTPase; Inflammasome; Interferon inducible GTPase; Intracellular pathogens

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE TRIPHOSPHATASE; INFLAMMASOME; INTERFERON;

CELL DESTRUCTION; CELL VACUOLE; CELLULAR DISTRIBUTION; HUMAN; IMMUNOREGULATION; INNATE IMMUNITY; NONHUMAN; OLIGOMERIZATION; OUTER MEMBRANE; PROTEIN STRUCTURE; PROTOZOON; REVIEW; ANIMAL; AUTOPHAGY; CHEMISTRY; CYTOPLASM; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PARASITOLOGY; PHYSIOLOGY; VIROLOGY;

ANIMALS; AUTOPHAGY; CYTOPLASM; GTP PHOSPHOHYDROLASES; GTP-BINDING PROTEINS; HUMANS; IMMUNITY, INNATE; INFLAMMASOMES; INTERFERONS; VACUOLES;

EID: 85034772396     PISSN: 14384221     EISSN: 16180607     Source Type: Journal    
DOI: 10.1016/j.ijmm.2017.10.013     Document Type: Review

References (150)

1. Abdullah, N., Balakumari, M., Sau, A.K., Dimerization and its role in GMP formation by human guanylate binding proteins. Biophys. J. 99:7 (2010), 2235–2244.
2. Abella, G., Pena, R.N., Nogareda, C., Armengol, R., Vidal, A., Moradell, L., Tarancon, V., Novell, E., Estany, J., Fraile, L., A WUR SNP is associated with European Porcine Reproductive and Respiratory Virus Syndrome resistance and growth performance in pigs. Res. Vet. Sci. 104 (2016), 117–122.
3. Al-Zeer, M.A., Al-Younes, H.M., Braun, P.R., Zerrahn, J., Meyer, T.F., IFN-gamma-inducible Irga6 mediates host resistance against Chlamydia trachomatis via autophagy. PLoS One, 4(2), 2009, e4588.
4. Al-Zeer, M.A., Al-Younes, H.M., Lauster, D., Abu Lubad, M., Meyer, T.F., Autophagy restricts Chlamydia trachomatis growth in human macrophages via IFNG-inducible guanylate binding proteins. Autophagy 9:1 (2013), 50–62.
5. Alaganan, A., Fentress, S.J., Tang, K., Wang, Q., Sibley, L.D., Toxoplasma GRA7 effector increases turnover of immunity-related GTPases and contributes to acute virulence in the mouse. Proc. Natl. Acad. Sci. U. S. A. 111:3 (2014), 1126–1131.
6. Anderson, S.L., Carton, J.M., Lou, J., Xing, L., Rubin, B.Y., Interferon-induced guanylate binding protein-1 (GBP-1) mediates an antiviral effect against vesicular stomatitis virus and encephalomyocarditis virus. Virology 256:1 (1999), 8–14.
7. Balasubramanian, S., Messmer-Blust, A.F., Jeyaratnam, J.A., Vestal, D.J., Role of GTP binding, isoprenylation, and the C-terminal α-helices in the inhibition of cell spreading by the interferon-induced GTPase, mouse guanylate-binding protein-2. J. Interferon Cytokine Res. 31:3 (2011), 291–298.
8. Behnke, M.S., Fentress, S.J., Mashayekhi, M., Li, L.X., Taylor, G.A., Sibley, L.D., The polymorphic pseudokinase ROP5 controls virulence in Toxoplasma gondii by regulating the active kinase ROP18. PLoS Pathog., 8(11), 2012, e1002992.
9. Bekpen, C., Hunn, J.P., Rohde, C., Parvanova, I., Guethlein, L., Dunn, D.M., Glowalla, E., Leptin, M., 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(11), 2005, R92.
10. Bekpen, C., Marques-Bonet, T., Alkan, C., Antonacci, F., Leogrande, M.B., Ventura, M., Kidd, J.M., Siswara, P., Howard, J.C., Eichler, E.E., Death and resurrection of the human IRGM gene. PLoS Genet., 5(3), 2009, e1000403.
11. Biering, S.B., Choi, J., Halstrom, R.A., Brown, H.M., Beatty, W.L., Lee, S., McCune, B.T., Dominici, E., Williams, L.E., Orchard, R.C., Wilen, C.B., Yamamoto, M., Coers, J., Taylor, G.A., Hwang, S., Viral replication complexes are targeted by LC3-Guided interferon-Inducible GTPases. Cell Host Microbe 22:1 (2017), 74–85 (e7).
12. Boddicker, N., Waide, E.H., Rowland, R.R.R., Lunney, J.K., Garrick, D.J., Reecy, J.M., Dekkers, J.C.M., Evidence for a major QTL associated with host response to porcine reproductive and respiratory syndrome virus challenge. J. Anim. Sci. 90:6 (2012), 1733–1746.
13. Boehm, U., Guethlein, L., Klamp, T., Ozbek, K., Schaub, A., Futterer, A., Pfeffer, K., Howard, J.C., Two families of GTPases dominate the complex cellular response to IFN-gamma. J. Immunol. 161:12 (1998), 6715–6723.
14. Britzen-Laurent, N., Bauer, M., Berton, V., Fischer, N., Syguda, A., Reipschläger, S., Naschberger, E., Herrmann, C., Stürzl, M., Intracellular trafficking of guanylate-binding proteins is regulated by heterodimerization in a hierarchical manner. PLoS One, 5(12), 2010, e14246.
15. Britzen-Laurent, N., Herrmann, C., Naschberger, E., Croner, R.S., Stürzl, M., Pathophysiological role of guanylate-binding proteins in gastrointestinal diseases. World J. Gastroenterol. 22:28 (2016), 6434–6443.
16. Carlow, D.A., Marth, J., Clark-Lewis, I., Teh, H.S., 1995 Isolation of a gene encoding a developmentally regulated T cell-specific protein with a guanine nucleotide triphosphate-binding motif. J. Immunol. 154:4 (1995), 1724–1734.
17. Carter, C.C., Gorbacheva, V.Y., 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. 150:6 (2005), 1213–1220.
18. Chauhan, S., Mandell, M.A., Deretic, V., Mechanism of action of the tuberculosis and Crohn disease risk factor IRGM in autophagy. Autophagy 12:2 (2016), 429–431.
19. Cheng, Y.S., Colonno, R.J., Yin, F.H., Interferon induction of fibroblast proteins with guanylate binding activity. J. Biol. Chem. 258:12 (1983), 7746–7750.
20. Cheng, Y.S., Patterson, C.E., Staeheli, P., Interferon-induced guanylate-binding proteins lack an N(T)KXD consensus motif and bind GMP in addition to GDP and GTP. Mol. Cell. Biol. 11:9 (1991), 4717–4725.
21. Choi, J., Park, S., Biering, S.B., Selleck, E., Liu, C.Y., Zhang, X., Fujita, N., Saitoh, T., Akira, S., Yoshimori, T., Sibley, L.D., Hwang, S., Virgin, H.W., The parasitophorous vacuole membrane of Toxoplasma gondii is targeted for disruption by ubiquitin-like conjugation systems of autophagy. Immunity 40:6 (2014), 924–935.
22. Clough, B., Frickel, E.-M., The toxoplasma parasitophorous vacuole: an evolving host-Parasite frontier. Trends Parasitol. 33:6 (2017), 473–488.
23. Coers, J., Gondek, D.C., Olive, A.J., Rohlfing, A., Taylor, G.A., Starnbach, M.N., Compensatory T cell responses in IRG-deficient mice prevent sustained Chlamydia trachomatis infections. PLoS Pathog., 7(6), 2011, e1001346.
24. Darnell, J.E., Kerr, I.M., Stark, G.R., Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 264:5164 (1994), 1415–1421.
25. Daumke, O., Praefcke, G.J.K., Invited review: mechanisms of GTP hydrolysis and conformational transitions in the dynamin superfamily. Biopolymers 105:8 (2016), 580–593.
26. Degrandi, D., Konermann, C., Beuter-Gunia, C., Kresse, A., Würthner, J., Kurig, S., Beer, S., Pfeffer, K., 2007 Extensive characterization of IFN-induced GTPases mGBP1 to mGBP10 involved in host defense. J. Immunol. 179:11 (2007), 7729–7740.
27. Degrandi, D., Kravets, E., Konermann, C., Beuter-Gunia, C., Klümpers, V., Lahme, S., Wischmann, E., Mausberg, A.K., Beer-Hammer, S., Pfeffer, K., Murine guanylate binding protein 2 (mGBP2) controls Toxoplasma gondii replication. Proc. Natl. Acad. Sci. U. S. A. 110:1 (2013), 294–299.
28. Etheridge, R.D., Alaganan, A., Tang, K., Lou, H.J., Turk, B.E., Sibley, L.D., The Toxoplasma pseudokinase ROP5 forms complexes with ROP18 and ROP17 kinases that synergize to control acute virulence in mice. Cell Host Microbe 15:5 (2014), 537–550.
29. Ewald, S.E., Chavarria-Smith, J., Boothroyd, J.C., NLRP1 is an inflammasome sensor for Toxoplasma gondii. Infect. Immun. 82:1 (2014), 460–468.
30. Feeley, E.M., Pilla-Moffett, D.M., Zwack, E.E., Piro, A.S., Finethy, R., Kolb, J.P., Martinez, J., Brodsky, I.E., Coers, J., Galectin-3 directs antimicrobial guanylate binding proteins to vacuoles furnished with bacterial secretion systems. Proc. Natl. Acad. Sci. U. S. A. 114:9 (2017), E1698–E1706.
31. Fellenberg, F., Hartmann, T.B., Dummer, R., Usener, D., Schadendorf, D., Eichmuller, S., GBP-5 splicing variants: new guanylate-binding proteins with tumor-associated expression and antigenicity. J. Invest. Dermatol. 122:6 (2004), 1510–1517.
32. Feng, C.G., Weksberg, D.C., Taylor, G.A., Sher, A., Goodell, M.A., The p47 GTPase Lrg-47(Irgm1) links host defense and hematopoietic stem cell proliferation. Cell Stem Cell 2:1 (2008), 83–89.
33. Feng, J., Cao, Z., Wang, L., Wan, Y., Peng, N., Wang, Q., Chen, X., Zhou, Y., Zhu, Y., Inducible GBP5 mediates the antiviral response via interferon-Related pathways during influenza a virus infection. J. Innate Immun. 9:4 (2017), 419–435.
34. 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., Townsend, R.R., Qiu, W., Hui, R., Beatty, W.L., Sibley, L.D., Phosphorylation of immunity-related GTPases by a Toxoplasma gondii-secreted kinase promotes macrophage survival and virulence. Cell Host Microbe 8:6 (2010), 484–495.
35. Fiegl, D., Kägebein, D., Liebler-Tenorio, E.M., Weisser, T., Sens, M., Gutjahr, M., Knittler, M.R., 2013 Amphisomal route of MHC class I cross-presentation in bacteria-infected dendritic cells. J. Immunol. 190:6 (2013), 2791–2806.
36. Finethy, R., Jorgensen, I., Haldar, A.K., Zoete de, M.R., Strowig, T., Flavell, R.A., Yamamoto, M., Nagarajan, U.M., Miao, E.A., Coers, J., Guanylate binding proteins enable rapid activation of canonical and noncanonical inflammasomes in Chlamydia-infected macrophages. Infect. Immun. 83:12 (2015), 4740–4749.
37. Finethy, R., Luoma, S., Orench-Rivera, N., Feeley, E.M., Haldar, A.K., Yamamoto, M., Kanneganti, T.-D., Kuehn, M.J., Coers, J., Inflammasome activation by bacterial outer membrane vesicles requires guanylate binding proteins. mBio, 8(5), 2017.
38. Fleckenstein, M.C., Reese, M.L., Könen-Waisman, S., Boothroyd, J.C., Howard, J.C., Steinfeldt, T., A Toxoplasma gondii pseudokinase inhibits host IRG resistance proteins. PLoS Biol., 10(7), 2012, e1001358.
39. Foltz, C., Napolitano, A., Khan, R., Clough, B., Hirst, E.M., Frickel, E.-M., TRIM21 is critical for survival of Toxoplasma gondii infection and localises to GBP-positive parasite vacuoles. Sci. Rep., 7(1), 2017, 5209.
40. Fox, B.A., Gigley, J.P., Bzik, D.J., Toxoplasma gondii lacks the enzymes required for de novo arginine biosynthesis and arginine starvation triggers cyst formation. Int. J. Parasitol. 34:3 (2004), 323–331.
41. Fres, J.M., Müller, S., Praefcke, G.J.K., Purification of the CaaX-modified, dynamin-related large GTPase hGBP1 by coexpression with farnesyltransferase. J. Lipid Res. 51:8 (2010), 2454–2459.
42. Ghosh, A., Uthaiah, R., Howard, J., Herrmann, C., Wolf, E., Crystal structure of IIGP1: a paradigm for interferon-inducible p47 resistance GTPases. Mol. Cell 15:5 (2004), 727–739.
43. Ghosh, A., Praefcke, G.J.K., Renault, L., Wittinghofer, A., Herrmann, C., How guanylate-binding proteins achieve assembly-stimulated processive cleavage of GTP to GMP. Nature 440:7080 (2006), 101–104.
44. Gilly, M., Wall, R., 1992 The IRG-47 gene is IFN-gamma induced in B cells and encodes a protein with GTP-binding motifs. J. Immunol. 148:10 (1992), 3275–3281.
45. Gorfu, G., Cirelli, K.M., Melo, M.B., Mayer-Barber, K., Crown, D., Koller, B.H., Masters, S., Sher, A., Leppla, S.H., Moayeri, M., Saeij, J.P.J., Grigg, M.E., Dual role for inflammasome sensors NLRP1 and NLRP3 in murine resistance to Toxoplasma gondii. mBio, 5(1), 2014.
46. Guenzi, E., Topolt, K., Cornali, E., Lubeseder-Martellato, C., Jorg, A., Matzen, K., Zietz, C., Kremmer, E., Nappi, F., Schwemmle, M., Hohenadl, C., Barillari, G., Tschachler, E., Monini, P., Ensoli, B., Sturzl, M., The helical domain of GBP-1 mediates the inhibition of endothelial cell proliferation by inflammatory cytokines. EMBO J. 20:20 (2001), 5568–5577.
47. Haldar, A.K., Saka, H.A., Piro, A.S., Dunn, J.D., Henry, S.C., Taylor, G.A., Frickel, E.M., Valdivia, R.H., Coers, J., IRG and GBP host resistance factors target aberrant, non-self vacuoles characterized by the missing of self IRGM proteins. PLoS Pathog., 9(6), 2013, e1003414.
48. Haldar, A.K., Piro, A.S., Pilla, D.M., Yamamoto, M., Coers, J., The E2-like conjugation enzyme Atg3 promotes binding of IRG and Gbp proteins to Chlamydia- and Toxoplasma-containing vacuoles and host resistance. PLoS One, 9(1), 2014, e86684.
49. Haldar, A.K., Foltz, C., Finethy, R., Piro, A.S., Feeley, E.M., Pilla-Moffett, D.M., Komatsu, M., Frickel, E.-M., Coers, J., Ubiquitin systems mark pathogen-containing vacuoles as targets for host defense by guanylate binding proteins. Proc. Natl. Acad. Sci. U. S. A. 112:41 (2015), E5628–37.
50. Haldar, A.K., Piro, A.S., Finethy, R., Espenschied, S.T., Brown, H.E., Giebel, A.M., Frickel, E.-M., Nelson, D.E., Coers, J., Chlamydia trachomatis is resistant to inclusion ubiquitination and associated host defense in gamma interferon-Primed human epithelial cells. mBio, 7(6), 2016.
51. Haller, O., Staeheli, P., Schwemmle, M., Kochs, G., Mx GTPases: dynamin-like antiviral machines of innate immunity. Trends Microbiol. 23:3 (2015), 154–163.
52. Hermanns, T., Müller, U.B., Könen-Waisman, S., Howard, J.C., Steinfeldt, T., The Toxoplasma gondii rhoptry protein ROP18 is an Irga6-specific kinase and regulated by the dense granule protein GRA7. Cell. Microbiol. 18:2 (2016), 244–259.
53. Howard, J.C., Hunn, J.P., Steinfeldt, T., The IRG protein-based resistance mechanism in mice and its relation to virulence in Toxoplasma gondii. Curr. Opin. Microbiol. 14:4 (2011), 414–421.
54. Hu, J., Rapoport, T.A., Fusion of the endoplasmic reticulum by membrane-bound GTPases. Semin. Cell Dev. Biol. 60 (2016), 105–111.
55. Hunn, J.P., Koenen-Waisman, S., Papic, N., Schroeder, N., Pawlowski, N., Lange, R., Kaiser, F., Zerrahn, J., Martens, S., Howard, J.C., Regulatory interactions between IRG resistance GTPases in the cellular response to Toxoplasma gondii. EMBO J. 27:19 (2008), 2495–2509.
56. Ince, S., Kutsch, M., Shydlovskyi, S., Herrmann, C., The human guanylate-binding proteins hGBP-1 and hGBP-5 cycle between monomers and dimers only. FEBS J. 284:14 (2017), 2284–2301.
57. Itsui, Y., Sakamoto, N., Kakinuma, S., Nakagawa, M., Sekine-Osajima, Y., Tasaka-Fujita, M., Nishimura-Sakurai, Y., Suda, G., Karakama, Y., Mishima, K., Yamamoto, M., Watanabe, T., Ueyama, M., Funaoka, Y., Azuma, S., Watanabe, M., Antiviral effects of the interferon-induced protein guanylate binding protein 1 and its interaction with the hepatitis C virus NS5B protein. Hepatology 50:6 (2009), 1727–1737.
58. Johnston, A.C., Piro, A., Clough, B., Siew, M., Virreira Winter, S., Coers, J., Frickel, E.-M., Human GBP1 does not localize to pathogen vacuoles but restricts Toxoplasma gondii. Cell. Microbiol. 18:8 (2016), 1056–1064.
59. Jutras, I., Houde, M., Currier, N., Boulais, J., Duclos, S., LaBoissiere, S., Bonneil, E., Kearney, P., Thibault, P., Paramithiotis, E., Hugo, P., Desjardins, M., Modulation of the phagosome proteome by interferon-gamma. Mol. Cell. Proteomics 7:4 (2008), 697–715.
60. Khaminets, A., Hunn, J.P., Konen-Waisman, S., Zhao, Y.O., Preukschat, D., Coers, J., Boyle, J.P., Ong, Y.C., Boothroyd, J.C., Reichmann, G., Howard, J.C., Coordinated loading of IRG resistance GTPases on to the Toxoplasma gondii parasitophorous vacuole. Cell. Microbiol. 12:7 (2010), 939–961.
61. Kim, B.-H., Shenoy, A.R., Kumar, P., Das, R., Tiwari, S., MacMicking, J.D., A family of IFN- −Inducible 65-kD GTPases protects against bacterial infection. Science 332:6030 (2011), 717–721.
62. Kim, B.-H., Chee, J.D., Bradfield, C.J., Park, E.-S., Kumar, P., MacMicking, J.D., Interferon-induced guanylate-binding proteins in inflammasome activation and host defense. Nat. Immunol. 17:5 (2016), 481–489.
63. King, K.Y., Baldridge, M.T., Weksberg, D.C., Chambers, S.M., Lukov, G.L., Wu, S., Boles, N.C., Jung, S.Y., Qin, J., Liu, D., Songyang, Z., Eissa, N.T., Taylor, G.A., Goodell, M.A., Irgm1 protects hematopoietic stem cells by negative regulation of IFN signaling. Blood 118:6 (2011), 1525–1533.
64. Koltes, J.E., Fritz-Waters, E., Eisley, C.J., Choi, I., Bao, H., Kommadath, A., Serão, N.V.L., Boddicker, N.J., Abrams, S.M., Schroyen, M., Loyd, H., Tuggle, C.K., Plastow, G.S., Guan, L., Stothard, P., Lunney, J.K., Liu, P., Carpenter, S., Rowland, R.R.R., Dekkers, J.C.M., Reecy, J.M., Identification of a putative quantitative trait nucleotide in guanylate binding protein 5 for host response to PRRS virus infection. BMC Genomics, 16, 2015, 412.
65. Kommadath, A., Bao, H., Choi, I., Reecy, J.M., Koltes, J.E., Fritz-Waters, E., Eisley, C.J., Grant, J.R., Rowland, R.R.R., Tuggle, C.K., Dekkers, J.C.M., Lunney, J.K., Le Guan, L., Stothard, P., Plastow, G.S., Genetic architecture of gene expression underlying variation in host response to porcine reproductive and respiratory syndrome virus infection. Sci. Rep., 7, 2017, 46203.
66. Krapp, C., Hotter, D., Gawanbacht, A., McLaren, P.J., Kluge, S.F., Stürzel, C.M., Mack, K., Reith, E., Engelhart, S., Ciuffi, A., Hornung, V., Sauter, D., Telenti, A., Kirchhoff, F., Guanylate binding protein (GBP) 5 is an interferon-Inducible inhibitor of HIV-1 infectivity. Cell Host Microbe 19:4 (2016), 504–514.
67. Kravets, E., Degrandi, D., Weidtkamp-Peters, S., Ries, B., Konermann, C., Felekyan, S., Dargazanli, J.M., Praefcke, G.J.K., Seidel, C.A.M., Schmitt, L., Smits, S.H.J., Pfeffer, K., The GTPase activity of murine guanylate-binding protein 2 (mGBP2) controls the intracellular localization and recruitment to the parasitophorous vacuole of Toxoplasma gondii. J. Biol. Chem. 287:33 (2012), 27452–27466.
68. Kravets, E., Degrandi, D., Ma, Q., Peulen, T.-O., Klümpers, V., Felekyan, S., Kühnemuth, R., Weidtkamp-Peters, S., Am Seidel, C., Pfeffer, K., Guanylate binding proteins directly attack Toxoplasma gondii via supramolecular complexes. eLife, 2016, 5.
69. Kresse, A., Konermann, C., Degrandi, D., Beuter-Gunia, C., Wuerthner, J., Pfeffer, K., Beer, S., Analyses of murine GBP homology clusters based on in silico, in vitro and in vivo studies. BMC Genomics, 9, 2008, 158.
70. Kunzelmann, S., Praefcke, G.J.K., Herrmann, C., Transient kinetic investigation of GTP hydrolysis catalyzed by interferon-gamma-induced hGBP1 (human guanylate binding protein 1). J. Biol. Chem. 281:39 (2006), 28627–28635.
71. Lafuse, W.P., Brown, D., Castle, L., 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. Leukoc. Biol. 57:3 (1995), 477–483.
72. Lee, Y., Sasai, M., Ma, J.S., Sakaguchi, N., Ohshima, J., Bando, H., Saitoh, T., Akira, S., Yamamoto, M., P62 plays a specific role in interferon-γ-Induced presentation of a toxoplasma vacuolar antigen. Cell Rep. 13:2 (2015), 223–233.
73. Lew, D.J., Decker, T., Strehlow, I., Darnell, J.E., Overlapping elements in the guanylate-binding protein gene promoter mediate transcriptional induction by alpha and gamma interferons. Mol. Cell. Biol. 11:1 (1991), 182–191.
74. Li, G., Zhang, J., Sun, Y., Wang, H., Wang, Y., The evolutionarily dynamic IFN-inducible GTPase proteins play conserved immune functions in vertebrates and cephalochordates. Mol. Biol. Evol. 26:7 (2009), 1619–1630.
75. Li, L.-F., Yu, J., Li, Y., Wang, J., Li, S., Zhang, L., Xia, S.-L., Yang, Q., Wang, X., Yu, S., Luo, Y., Sun, Y., Zhu, Y., Munir, M., Qiu, H.-J., Guanylate-Binding protein 1, an interferon-Induced GTPase, exerts an antiviral activity against classical swine fever virus depending on its GTPase activity. J. Virol. 90:9 (2016), 4412–4426.
76. Lilue, J., Müller, U.B., Steinfeldt, T., Howard, J.C., Reciprocal virulence and resistance polymorphism in the relationship between Toxoplasma gondii and the house mouse. eLife, 2, 2013, e01298.
77. Lindenberg, V., Mölleken, K., Kravets, E., Stallmann, S., Hegemann, J.H., Degrandi, D., Pfeffer, K., Broad recruitment of mGBP family members to Chlamydia trachomatis inclusions. PLoS One, 12(9), 2017, e0185273.
78. MacMicking, J.D., Interferon-inducible effector mechanisms in cell-autonomous immunity. Nature reviews. Immunology 12:5 (2012), 367–382.
79. Man, S.M., Karki, R., Sasai, M., Place, D.E., Kesavardhana, S., Temirov, J., Frase, S., Zhu, Q., Malireddi, R.K.S., Kuriakose, T., Peters, J.L., Neale, G., Brown, S.A., Yamamoto, M., Kanneganti, T.-D., IRGB10 liberates bacterial ligands for sensing by the AIM2 and caspase-11-NLRP3 inflammasomes. Cell 167:2 (2016), 382–396 (e17).
80. Maric-Biresev, J., Hunn, J.P., Krut, O., Helms, J.B., Martens, S., Howard, J.C., Loss of the interferon-γ-inducible regulatory immunity-related GTPase (IRG), Irgm1, causes activation of effector IRG proteins on lysosomes, damaging lysosomal function and predicting the dramatic susceptibility of Irgm1-deficient mice to infection. BMC Biol., 14, 2016, 33.
81. Martens, S., Sabel, K., Lange, R., Uthaiah, R., Wolf, E., 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. 173:4 (2004), 2594–2606.
82. McNew, J.A., Sondermann, H., Lee, T., Stern, M., Brandizzi, F., GTP-dependent membrane fusion. Annu. Rev. Cell Dev. Biol. 29 (2013), 529–550.
83. Meunier, E., Broz, P., Interferon-induced guanylate-binding proteins promote cytosolic lipopolysaccharide detection by caspase-11. DNA Cell Biol. 34:1 (2015), 1–5.
84. Meunier, E., Broz, P., Interferon-inducible GTPases in cell autonomous and innate immunity. Cell. Microbiol. 18:2 (2016), 168–180.
85. Meunier, E., Dick, M.S., Dreier, R.F., Schürmann, N., Kenzelmann Broz, D., Warming, S., Roose-Girma, M., Bumann, D., Kayagaki, N., Takeda, K., Yamamoto, M., Broz, P., Caspase-11 activation requires lysis of pathogen-containing vacuoles by IFN-induced GTPases. Nature 509:7500 (2014), 366–370.
86. Modiano, N., Lu, Y.E., Cresswell, P., Golgi targeting of human guanylate-binding protein-1 requires nucleotide binding, isoprenylation, and an IFN-gamma-inducible cofactor. Proc. Natl. Acad. Sci. U. S. A. 102:24 (2005), 8680–8685.
87. Mordue, D.G., Desai, N., Dustin, M., Sibley, L.D., Invasion by Toxoplasma gondii establishes a moving junction that selectively excludes host cell plasma membrane proteins on the basis of their membrane anchoring. J. Exp. Med. 190:12 (1999), 1783–1792.
88. Nantais, D.E., Schwemmle, M., Stickney, J.T., Vestal, D.J., Buss, J.E., Prenylation of an interferon-gamma-induced GTP-binding protein: the human guanylate binding protein, huGBP1. J. Leukoc. Biol. 60:3 (1996), 423–431.
89. Naschberger, E., Geißdörfer, W., Bogdan, C., Tripal, P., Kremmer, E., Stürzl, M., Britzen-Laurent, N., Processing and secretion of guanylate binding protein-1 depend on inflammatory caspase activity. J. Cell. Mol. Med. 21:9 (2017), 1954–1966.
90. Neun, R., Richter, M.F., Staeheli, P., Schwemmle, M., GTPase properties of the interferon-induced human guanylate-binding protein 2. FEBS Lett. 390:1 (1996), 69–72.
91. Niedelman, W., Gold, D.A., Rosowski, E.E., Sprokholt, J.K., Lim, D., Farid Arenas, A., Melo, M.B., Spooner, E., Yaffe, M.B., Saeij, J.P.J., The rhoptry proteins ROP18 and ROP5 mediate Toxoplasma gondii evasion of the murine, but not the human, interferon-gamma response. PLoS Pathog., 8(6), 2012, e1002784.
92. Niedelman, W., Sprokholt, J.K., Clough, B., Frickel, E.-M., Saeij, J.P.J., Cell death of gamma interferon-stimulated human fibroblasts upon Toxoplasma gondii infection induces early parasite egress and limits parasite replication. Infect. Immun. 81:12 (2013), 4341–4349.
93. Niu, P., Shabir, N., Khatun, A., Seo, B.-J., Gu, S., Lee, S.-M., Lim, S.-K., Kim, K.-S., Kim, W.-I., Effect of polymorphisms in the GBP1, Mx1 and CD163 genes on host responses to PRRSV infection in pigs. Vet. Microbiol. 182 (2016), 187–195.
94. Nordmann, A., Wixler, L., Boergeling, Y., Wixler, V., Ludwig, S., A new splice variant of the human guanylate-binding protein 3 mediates anti-influenza activity through inhibition of viral transcription and replication. FASEB J. 26:3 (2012), 1290–1300.
95. Obar, R.A., Collins, C.A., Hammarback, J.A., Shpetner, H.S., Vallee, R.B., Molecular cloning of the microtubule-associated mechanochemical enzyme dynamin reveals homology with a new family of GTP-binding proteins. Nature 347:6290 (1990), 256–261.
96. Ohshima, J., Lee, Y., Sasai, M., Saitoh, T., Su Ma, J., Kamiyama, N., Matsuura, Y., Pann-Ghill, S., Hayashi, M., Ebisu, S., Takeda, K., Akira, S., Yamamoto, M., Role of mouse and human autophagy proteins in IFN-γ-induced cell-autonomous responses against Toxoplasma gondii. J. Immunol. 192:7 (2014), 3328–3335.
97. Ohshima, J., Sasai, M., Liu, J., Yamashita, K., Ma, J.S., Lee, Y., Bando, H., Howard, J.C., Ebisu, S., Hayashi, M., Takeda, K., Standley, D.M., Frickel, E.-M., Yamamoto, M., RabGDIα is a negative regulator of interferon-γ-inducible GTPase-dependent cell-autonomous immunity to Toxoplasma gondii. Proc. Natl. Acad. Sci. U. S. A. 112:33 (2015), E4581–90.
98. Olszewski, M.A., Gray, J., Vestal, D.J., In silico genomic analysis of the human and murine guanylate-binding protein (GBP) gene clusters. J. Interferon Cytokine Res. 26:5 (2006), 328–352.
99. Ostler, N., Britzen-Laurent, N., Liebl, A., Naschberger, E., Lochnit, G., Ostler, M., Forster, F., Kunzelmann, P., Ince, S., Supper, V., Praefcke, G.J.K., Schubert, D.W., Stockinger, H., Herrmann, C., Stürzl, M., Gamma interferon-induced guanylate binding protein 1 is a novel actin cytoskeleton remodeling factor. Mol. Cell. Biol. 34:2 (2014), 196–209.
100. Pan, W., Zuo, X., Feng, T., Shi, X., Dai, J., Guanylate-binding protein 1 participates in cellular antiviral response to dengue virus. Virol. J., 9, 2012, 292.
101. Pandita, E., Rajan, S., Rahman, S., Mullick, R., Das, S., Sau, A.K., Tetrameric assembly of hGBP1 is crucial for both stimulated GMP formation and antiviral activity. Biochem. J. 473:12 (2016), 1745–1757.
102. Papic, N., Hunn, J.P., Pawlowski, N., Zerrahn, J., Howard, J.C., Inactive and active states of the interferon-inducible resistance GTPase, Irga6, in vivo. J. Biol. Chem. 283:46 (2008), 32143–32151.
103. Pawlowski, N., Khaminets, A., Hunn, J.P., Papic, N., Schmidt, A., Uthaiah, R.C., Lange, R., Vopper, G., Martens, S., Wolf, E., Howard, J.C., The activation mechanism of Irga6, an interferon-inducible GTPase contributing to mouse resistance against Toxoplasma gondii. BMC Biol., 9, 2011, 7.
104. Pfefferkorn, E.R., Rebhun, S., Eckel, M., Characterization of an indoleamine 2,3-dioxygenase induced by gamma-interferon in cultured human fibroblasts. J. Interferon Res. 6:3 (1986), 267–279.
105. Pfefferkorn, E.R., Interferon gamma blocks the growth of Toxoplasma gondii in human fibroblasts by inducing the host cells to degrade tryptophan. Proc. Natl. Acad. Sci. U. S. A. 81:3 (1984), 908–912.
106. Pilla, D.M., Hagar, J.A., Haldar, A.K., Mason, A.K., Degrandi, D., Pfeffer, K., Ernst, R.K., Yamamoto, M., Miao, E.A., Coers, J., Guanylate binding proteins promote caspase-11-dependent pyroptosis in response to cytoplasmic LPS. Proc. Natl. Acad. Sci. U. S. A. 111:16 (2014), 6046–6051.
107. Pilla-Moffett, D., Barber, M.F., Taylor, G.A., Coers, J., Interferon-Inducible GTPases in host resistance, inflammation and disease. J. Mol. Biol. 428:17 (2016), 3495–3513.
108. Platanias, L.C., Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat. Rev. Immunol. 5:5 (2005), 375–386.
109. Praefcke, G.J.K., McMahon, H.T., The dynamin superfamily: universal membrane tubulation and fission molecules?. Nat. Rev. Mol. Cell Biol. 5:2 (2004), 133–147.
110. Praefcke, G.J.K., Geyer, M., Schwemmle, M., Robert Kalbitzer, H., Herrmann, C., Nucleotide-binding characteristics of human guanylate-binding protein 1 (hGBP1) and identification of the third GTP-binding motif. J. Mol. Biol. 292:2 (1999), 321–332.
111. Praefcke, G.J.K., Kloep, S., Benscheid, U., Lilie, H., Prakash, B., Herrmann, C., Identification of residues in the human guanylate-binding protein 1 critical for nucleotide binding and cooperative GTP hydrolysis. J. Mol. Biol. 344:1 (2004), 257–269.
112. Prakash, B., Praefcke, G.J.K., Renault, L., Wittinghofer, A., Herrmann, C., Structure of human guanylate-binding protein 1 representing a unique class of GTP-binding proteins. Nature 403:6769 (2000), 567–571.
113. Prakash, B., Renault, L., Praefcke, G.J.K., Herrmann, C., Wittinghofer, A., Triphosphate structure of guanylate-binding protein 1 and implications for nucleotide binding and GTPase mechanism. EMBO J. 19:17 (2000), 4555–4564.
114. Qin, A., Lai, D.-H., Liu, Q., Huang, W., Wu, Y.-P., Chen, X., Yan, S., Xia, H., Hide, G., Lun, Z.-R., Ayala, F.J., Xiang, A.P., Guanylate-binding protein 1 (GBP1) contributes to the immunity of human mesenchymal stromal cells against Toxoplasma gondii. Proc. Natl. Acad. Sci. U. S. A. 114:6 (2017), 1365–1370.
115. Scharton-Kersten, T.M., Yap, G., Magram, J., Sher, A., Inducible nitric oxide is essential for host control of persistent but not acute infection with the intracellular pathogen Toxoplasma gondii. J. Exp. Med. 185:7 (1997), 1261–1273.
116. Schnoor, M., Betanzos, A., Weber, D.A., Parkos, C.A., Guanylate-binding protein-1 is expressed at tight junctions of intestinal epithelial cells in response to interferon-gamma and regulates barrier function through effects on apoptosis. Mucosal Immunol. 2:1 (2009), 33–42.
117. Schroyen, M., Eisley, C., Koltes, J.E., Fritz-Waters, E., Choi, I., Plastow, G.S., Guan, L., Stothard, P., Bao, H., Kommadath, A., Reecy, J.M., Lunney, J.K., Rowland, R.R.R., Dekkers, J.C.M., Tuggle, C.K., Bioinformatic analyses in early host response to Porcine Reproductive and Respiratory Syndrome virus (PRRSV) reveals pathway differences between pigs with alternate genotypes for a major host response QTL. BMC Genomics, 17, 2016, 196.
118. Schulte, K., Pawlowski, N., Faelber, K., Fröhlich, C., Howard, J., Daumke, O., The immunity-related GTPase Irga6 dimerizes in a parallel head-to-head fashion. BMC Biol., 14, 2016, 14.
119. Schwemmle, M., Staeheli, P., The interferon-induced 67-kDa guanylate-binding protein (hGBP1) is a GTPase that converts GTP to GMP. J. Biol. Chem. 269:15 (1994), 11299–11305.
120. Selleck, E.M., Fentress, S.J., Beatty, W.L., Degrandi, D., Pfeffer, K., Virgin, H.W., MacMicking, J.D., Sibley, L.D., Guanylate-binding protein 1 (Gbp1) contributes to cell-autonomous immunity against Toxoplasma gondii. PLoS Pathog., 9(4), 2013, e1003320.
121. Shenoy, A.R., Wellington, D.A., Kumar, P., Kassa, H., Booth, C.J., Cresswell, P., MacMicking, J.D., GBP5 promotes NLRP3 inflammasome assembly and immunity in mammals. Science 336:6080 (2012), 481–485.
122. Shydlovskyi, S., Zienert, A.Y., Ince, S., Dovengerds, C., Hohendahl, A., Dargazanli, J.M., Blum, A., Günther, S.D., Kladt, N., Stürzl, M., Schauss, A.C., Kutsch, M., Roux, A., Praefcke, G.J.K., Herrmann, C., Nucleotide-dependent farnesyl switch orchestrates polymerization and membrane binding of human guanylate-binding protein 1. Proc. Natl. Acad. Sci. U. S. A. 114:28 (2017), E5559–E5568.
123. Sorace, J.M., Johnson, R.J., Howard, D.L., Drysdale, B.E., Identification of an endotoxin and IFN-inducible cDNA: possible identification of a novel protein family. J. Leukoc. Biol. 58:4 (1995), 477–484.
124. Steinfeldt, T., Könen-Waisman, S., Tong, L., Pawlowski, N., Lamkemeyer, T., Sibley, L.D., Hunn, J.P., Howard, J.C., Phosphorylation of mouse immunity-related GTPase (IRG) resistance proteins is an evasion strategy for virulent Toxoplasma gondii. PLoS Biol., 8(12), 2010, e1000576.
125. Stickney, J.T., Buss, J.E., Murine guanylate-binding protein: incomplete geranylgeranyl isoprenoid modification of an interferon-gamma-inducible guanosine triphosphate-binding protein. Mol. Biol. Cell 11:7 (2000), 2191–2200.
126. Syguda, A., Bauer, M., Benscheid, U., Ostler, N., Naschberger, E., Ince, S., Stürzl, M., Herrmann, C., Tetramerization of human guanylate-binding protein 1 is mediated by coiled-coil formation of the C-terminal α-helices. FEBS J. 279:14 (2012), 2544–2554.
127. Syguda, A., Kerstan, A., Ladnorg, T., Stüben, F., Wöll, C., Herrmann, C., Immobilization of biotinylated hGBP1 in a defined orientation on surfaces is crucial for uniform interaction with analyte proteins and catalytic activity. Langmuir 28:15 (2012), 6411–6418.
128. Taylor, G.A., Jeffers, M., Largaespada, D.A., Jenkins, N.A., Copeland, N.G., Vande Woude, G.F., Identification of a novel GTPase, the inducibly expressed GTPase, that accumulates in response to interferon gamma. J. Biol. Chem. 271:34 (1996), 20399–20405.
129. 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., 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. 97:2 (2000), 751–755.
130. Thurston, T.L.M., Wandel, M.P., Muhlinen, N., von Foeglein, A., Randow, F., Galectin 8 targets damaged vesicles for autophagy to defend cells against bacterial invasion. Nature 482:7385 (2012), 414–418.
131. Tietzel, I., El-Haibi, C., Carabeo, R.A., Human guanylate binding proteins potentiate the anti-chlamydia effects of interferon-gamma. PLoS One, 4(8), 2009, e6499.
132. Traver, M.K., Henry, S.C., Cantillana, V., Oliver, T., Hunn, J.P., Howard, J.C., Beer, S., Pfeffer, K., Coers, J., Taylor, G.A., Immunity-related GTPase M (IRGM) proteins influence the localization of guanylate-binding protein 2 (GBP2) by modulating macroautophagy. J. Biol. Chem. 286:35 (2011), 30471–30480.
133. Tripal, P., Bauer, M., Naschberger, E., Mortinger, T., Hohenadl, C., Cornali, E., Thurau, M., Sturzl, M., Unique features of different members of the human guanylate-binding protein family. J. Interferon Cytokine Res. 27:1 (2007), 44–52.
134. Trost, M., English, L., Lemieux, S., Courcelles, M., Desjardins, M., Thibault, P., The phagosomal proteome in interferon-gamma-activated macrophages. Immunity 30:1 (2009), 143–154.
135. Tyrkalska, S.D., Candel, S., Angosto, D., Gómez-Abellán, V., Martín-Sánchez, F., García-Moreno, D., Zapata-Pérez, R., Sánchez-Ferrer, Á., Sepulcre, M.P., Pelegrín, P., Mulero, V., Neutrophils mediate Salmonella Typhimurium clearance through the GBP4 inflammasome-dependent production of prostaglandins. Nat. Commun., 7, 2016, 12077.
136. Uthaiah, R.C., Praefcke, G.J.K., Howard, J.C., Herrmann, C., IIGP1, an interferon-gamma-inducible 47-kDa GTPase of the mouse, showing cooperative enzymatic activity and GTP-dependent multimerization. J. Biol. Chem. 278:31 (2003), 29336–29343.
137. Vöpel, T., Kunzelmann, S., Herrmann, C., Nucleotide dependent cysteine reactivity of hGBP1 uncovers a domain movement during GTP hydrolysis. FEBS Lett. 583:12 (2009), 1923–1927.
138. Vöpel, T., Syguda, A., Britzen-Laurent, N., Kunzelmann, S., Lüdemann, M.-B., Dovengerds, C., Stürzl, M., Herrmann, C., Mechanism of GTPase-activity-induced self-assembly of human guanylate binding protein 1. J. Mol. Biol. 400:1 (2010), 63–70.
139. Vöpel, T., Hengstenberg, C.S., Peulen, T.-O., Ajaj, Y., Seidel, C.A.M., Herrmann, C., Klare, J.P., Triphosphate induced dimerization of human guanylate binding protein 1 involves association of the C-terminal helices: a joint double electron–electron resonance and FRET study. Biochemistry 53:28 (2014), 4590–4600.
140. Vestal, D.J., Gorbacheva, V.Y., Sen, G.C., Different subcellular localizations for the related interferon-induced GTPases, MuGBP-1 and MuGBP-2: implications for different functions?. Journal Interferon Cytokine Res. 20:11 (2000), 991–1000.
141. Virreira Winter, S., Niedelman, W., Jensen, K.D., Rosowski, E.E., Julien, L., Spooner, E., Caradonna, K., Burleigh, B.A., Saeij, J.P.J., Ploegh, H.L., Frickel, E.-M., Determinants of GBP recruitment to Toxoplasma gondii vacuoles and the parasitic factors that control it. PLoS One, 6(9), 2011, e24434.
142. Wallet, P., Benaoudia, S., Mosnier, A., Lagrange, B., Martin, A., Lindgren, H., Golovliov, I., Michal, F., Basso, P., Djebali, S., Provost, A., Allatif, O., Meunier, E., Broz, P., Yamamoto, M., Py, B.F., Faudry, E., Sjöstedt, A., Henry, T., IFN-γ extends the immune functions of Guanylate Binding Proteins to inflammasome-independent antibacterial activities during Francisella novicida infection. PLoS Pathog., 13(10), 2017, e1006630.
143. Wandel, M.P., Pathe, C., Werner, E.I., Ellison, C.J., Boyle, K.B., Malsburg, A., von der Rohde, J., Randow, F., GBPs inhibit motility of shigella flexneri but are targeted for degradation by the bacterial ubiquitin ligase IpaH9. 8. Cell Host Microbe 22:4 (2017), 507–518 (e5).
144. Wehner, M., Herrmann, C., Biochemical properties of the human guanylate binding protein 5 and a tumor-specific truncated splice variant. FEBS J. 277:7 (2010), 1597–1605.
145. Wehner, M., Kunzelmann, S., Herrmann, C., The guanine cap of human guanylate-binding protein 1 is responsible for dimerization and self-activation of GTP hydrolysis. FEBS J. 279:2 (2012), 203–210.
146. Yamamoto, M., Okuyama, M., Ma, J.S., Kimura, T., Kamiyama, N., Saiga, H., Ohshima, J., Sasai, M., Kayama, H., Okamoto, T., Huang, D.C.S., Soldati-Favre, D., Horie, K., Takeda, J., Takeda, K., A cluster of interferon-γ-inducible p65 GTPases plays a critical role in host defense against Toxoplasma gondii. Immunity 37:2 (2012), 302–313.
147. Yarovinsky, F., Innate immunity to Toxoplasma gondii infection. Nature reviews. Immunology 14:2 (2014), 109–121.
148. Zhao, Z., Fux, B., Goodwin, M., Dunay, I.R., Strong, D., Miller, B.C., Cadwell, K., Delgado, M.A., Ponpuak, M., Green, K.G., Schmidt, R.E., Mizushima, N., Deretic, V., Sibley, L.D., Virgin, H.W., Autophagosome-independent essential function for the autophagy protein Atg5 in cellular immunity to intracellular pathogens. Cell Host Microbe 4:5 (2008), 458–469.
149. Zhao, Y.O., Khaminets, A., Hunn, J.P., Howard, J.C., Disruption of the Toxoplasma gondii parasitophorous vacuole by IFNgamma-inducible immunity-related GTPases (IRG proteins) triggers necrotic cell death. PLoS Pathog., 5(2), 2009, e1000288.
150. Zou, Z., Meng, Z., Ma, C., Liang, D., Sun, R., Lan, K., Guanylate-Binding protein 1 inhibits nuclear delivery of kaposi's sarcoma-associated herpesvirus virions by disrupting formation of actin filament. J. Virol., 91(16), 2017.