Role of nucleotide binding and GTPase domain dimerization in dynamin-like myxovirus resistance protein a for GTPase activation and antiviral activity

Journal of Biological Chemistry

Volumn 290, Issue 20, 2015, Pages 12779-12792

  Dick, Alexej ^a,b   Graf, Laura ^c,d   Olal, Daniel ^a   Von Der Malsburg, Alexander ^c,f   Gao, Song ^e   Kochs, Georg ^c,d   Daumke, Oliver ^a,b  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

^c UNIVERSITY OF FREIBURG   (Germany)

^d UNIVERSITY OF FREIBURG   (Germany)

^e SUN YAT SEN UNIVERSITY CANCER CENTER   (China)

^f MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANES; CHEMICAL ACTIVATION; CYTOLOGY; DIMERIZATION; HYDROLYSIS; MOBILE SECURITY; NUCLEOTIDES; PROTEINS; SELF ASSEMBLY;

DYNAMIC REDISTRIBUTION; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM MEMBRANES; HUMAN IMMUNODEFICIENCY VIRUS; INTRACELLULAR DYNAMICS; NUCLEOCAPSID PROTEINS; NUCLEOTIDE HYDROLYSIS; PROTEIN CONCENTRATIONS;

VIRUSES;

DYNAMIN; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATE; MYXOVIRUS RESISTANCE PROTEIN A; NUCLEOCAPSID PROTEIN; NUCLEOTIDE; MX1 PROTEIN, HUMAN; MYXOVIRUS RESISTANCE PROTEIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ANTIVIRAL ACTIVITY; ARTICLE; CATALYSIS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DIMERIZATION; ENDOPLASMIC RETICULUM MEMBRANE; ENZYME ACTIVATION; HUMAN; HUMAN CELL; HYDROLYSIS; INFLUENZA VIRUS; LA CROSSE VIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; THOGOTO VIRUS; CELL LINE; ENDOPLASMIC RETICULUM; GENETICS; INTRACELLULAR MEMBRANE; METABOLISM; ORTHOMYXOVIRIDAE; PHYSIOLOGY; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE; THOGOTOVIRUS;

HUMAN IMMUNODEFICIENCY VIRUS; LA CROSSE VIRUS; ORTHOMYXOVIRIDAE; THOGOTO VIRUS;

CELL LINE; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; GTP PHOSPHOHYDROLASES; HUMANS; HYDROLYSIS; INTRACELLULAR MEMBRANES; LA CROSSE VIRUS; MYXOVIRUS RESISTANCE PROTEINS; NUCLEOCAPSID PROTEINS; ORTHOMYXOVIRIDAE; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; THOGOTOVIRUS;

EID: 84929379426     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.650325     Document Type: Article

References (58)

1. Verhelst, J., Hulpiau, P., and Saelens, X. (2013) Mx proteins: antiviral gatekeepers that restrain the uninvited. Microbiol. Mol. Biol. Rev. 77, 551-566
2. Haller, O., Staeheli, P., Schwemmle, M., and Kochs, G. (2015) Mx GTPases: dynamin-like antiviral machines of innate immunity. Trends Microbiol. 23, 154-163
3. Haller, O., and Kochs, G. (2011) Human MxA protein: an interferon-induced dynamin-like GTPase with broad antiviral activity. J. Interferon Cytokine Res. 31, 79-87
4. Netherton, C. L., Simpson, J., Haller, O., Wileman, T. E., Takamatsu, H. H., Monaghan, P., and Taylor, G. (2009) Inhibition of a large double-stranded DNA virus by MxA protein. J. Virol. 83, 2310-2320
5. Gordien, E., Rosmorduc, O., Peltekian, C., Garreau, F., Bréchot, C., and Kremsdorf, D. (2001) Inhibition of hepatitis B virus replication by the interferon-inducible MxA protein. J. Virol. 75, 2684-2691
6. Liu, Z., Pan, Q., Ding, S., Qian, J., Xu, F., Zhou, J., Cen, S., Guo, F., and Liang, C. (2013) The interferon-inducible MxB protein inhibits HIV-1 infection. Cell Host Microbe 14, 398-410
7. Goujon, C., Moncorgé, O., Bauby, H., Doyle, T., Ward, C. C., Schaller, T., Hué, S., Barclay, W. S., Schulz, R., and Malim, M. H. (2013) Human MX2 is an interferon-induced post-entry inhibitor of HIV-1 infection. Nature 502, 559-562
8. Kane, M., Yadav, S. S., Bitzegeio, J., Kutluay, S. B., Zang, T., Wilson, S. J., Schoggins, J. W., Rice, C. M., Yamashita, M., Hatziioannou, T., and Bieniasz, P. D. (2013) MX2 is an interferon-induced inhibitor of HIV-1 infection. Nature 502, 563-566
9. Busnadiego, I., Kane, M., Rihn, S. J., Preugschas, H. F., Hughes, J., Blanco-Melo, D., Strouvelle, V. P., Zang, T. M., Willett, B. J., Boutell, C., Bieniasz, P. D., and Wilson, S. J. (2014) Host and viral determinants of Mx2 antiretroviral activity. J. Virol. 88, 7738-7752
10. Accola, M. A., Huang, B., Al Masri, A., and McNiven, M. A. (2002) The antiviral dynamin family member, MxA, tubulates lipids and localizes to the smooth endoplasmic reticulum. J. Biol. Chem. 277, 21829-21835
11. Kochs, G., Haener, M., Aebi, U., and Haller, O. (2002) Self-assembly of human MxA GTPase into highly ordered dynamin-like oligomers. J. Biol. Chem. 277, 14172-14176
12. von der Malsburg, A., Abutbul-Ionita, I., Haller, O., Kochs, G., and Danino, D. (2011) Stalk domain of the dynamin-like MxA GTPase protein mediates membrane binding and liposome tubulation via the unstructured L4 loop. J. Biol. Chem. 286, 37858-37865
13. Stertz, S., Reichelt, M., Krijnse-Locker, J., Mackenzie, J., Simpson, J. C., Haller, O., and Kochs, G. (2006) Interferon-induced, antiviral human MxA protein localizes to a distinct subcompartment of the smooth endoplasmic reticulum. J. Interferon Cytokine Res. 26, 650-660
14. Reichelt, M., Stertz, S., Krijnse-Locker, J., Haller, O., and Kochs, G. (2004) Missorting of LaCrosse virus nucleocapsid protein by the interferon-induced MxA GTPase involves smooth ER membranes. Traffic 5, 772-784
15. Turan, K., Mibayashi, M., Sugiyama, K., Saito, S., Numajiri, A., and Nagata, K. (2004) Nuclear MxA proteins form a complex with influenza virus NP and inhibit the transcription of the engineered influenza virus genome. Nucleic Acids Res. 32, 643-652
16. Kochs, G., and Haller, O. (1999) Interferon-induced human MxA GTPase blocks nuclear import of Thogoto virus nucleocapsids. Proc. Natl. Acad. Sci. U.S.A. 96, 2082-2086
17. Kochs, G., Janzen, C., Hohenberg, H., and Haller, O. (2002) Antivirally active MxA protein sequesters La Crosse virus nucleocapsid protein into perinuclear complexes. Proc. Natl. Acad. Sci. U.S.A. 99, 3153-3158
18. Gao, S., von der Malsburg, A., Paeschke, S., Behlke, J., Haller, O., Kochs, G., and Daumke, O. (2010) Structural basis of oligomerization in the stalk region of dynamin-like MxA. Nature 465, 502-506
19. Gao, S., von der Malsburg, A., Dick, A., Faelber, K., Schröder, G. F., Haller, O., Kochs, G., and Daumke, O. (2011) Structure of myxovirus resistance protein a reveals intra-and intermolecular domain interactions required for the antiviral function. Immunity 35, 514-525
20. Rennie, M. L., McKelvie, S. A., Bulloch, E. M., and Kingston, R. L. (2014) Transient dimerization of duman MxA promotes GTP hydrolysis, resulting in a mechanical power stroke. Structure 22, 1433-1445
21. Mitchell, P. S., Patzina, C., Emerman, M., Haller, O., Malik, H. S., and Kochs, G. (2012) Evolution-guided identification of antiviral specificity determinants in the broadly acting interferon-induced innate immunity factor MxA. Cell Host Microbe 12, 598-604
22. Patzina, C., Haller, O., and Kochs, G. (2014) Structural requirements for the antiviral activity of the human MxA protein against Thogoto and influenza A virus. J. Biol. Chem. 289, 6020-6027
23. Staeheli, P., Pitossi, F., and Pavlovic, J. (1993) Mx proteins: GTPases with antiviral activity. Trends Cell Biol. 3, 268-272
24. Gasper, R., Meyer, S., Gotthardt, K., Sirajuddin, M., and Wittinghofer, A. (2009) It takes two to tango: regulation ofGproteins by dimerization. Nat. Rev. Mol. Cell Biol. 10, 423-429
25. Chappie, J. S., Acharya, S., Leonard, M., Schmid, S. L., and Dyda, F. (2010) G domain dimerization controls dynamin's assembly-stimulated GTPase activity. Nature 465, 435-440
26. Wenger, J., Klinglmayr, E., Fröhlich, C., Eibl, C., Gimeno, A., Hessenberger, M., Puehringer, S., Daumke, O., and Goettig, P. (2013) Functional mapping of human dynamin-1-like GTPase domain based on x-ray structure analyses. PLoS One 8, e71835
27. Haller, O., Gao, S., von der Malsburg, A., Daumke, O., and Kochs, G. (2010) Dynamin-like MxA GTPase: structural insights into oligomerization and implications for antiviral activity. J. Biol. Chem. 285, 28419-28424
28. Chappie, J. S., Mears, J. A., Fang, S., Leonard, M., Schmid, S. L., Milligan, R. A., Hinshaw, J. E., and Dyda, F. (2011) A pseudoatomic model of the dynamin polymer identifies a hydrolysis-dependent powerstroke. Cell 147, 209-222
29. Arnold, K., Bordoli, L., Kopp, J., and Schwede, T. (2006) The SWISSMODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22, 195-201
30. DeLano, W. L. (2010) The PyMOL Molecular Graphics System, Version 1.3, Schrödinger, LLC, New York
31. Kochs, G., Weber, F., Gruber, S., Delvendahl, A., Leitz, C., and Haller, O. (2000) Thogoto virus matrix protein is encoded by a spliced mRNA. J. Virol. 74, 10785-10789
32. Thompson, W. H., Kalfayan, B., and Anslow, R. O. (1965) Isolation of California encephalitis group virus from a fatal human illness. Am. J. Epidemiol. 81, 245-253
33. Dittmann, J., Stertz, S., Grimm, D., Steel, J., García-Sastre, A., Haller, O., and Kochs, G. (2008) Influenza A virus strains differ in sensitivity to the antiviral action of Mx-GTPase. J. Virol. 82, 3624-3631
34. Lutz, A., Dyall, J., Olivo, P. D., and Pekosz, A. (2005) Virus-inducible reporter genes as a tool for detecting and quantifying influenza A virus replication. J. Virol. Methods 126, 13-20
35. Kochs, G., and Haller, O. (1999) GTP-bound human MxA protein interacts with the nucleocapsids of Thogoto virus (Orthomyxoviridae). J. Biol. Chem. 274, 4370-4376
36. Flohr, F., Schneider-Schaulies, S., Haller, O., and Kochs, G. (1999) The central interactive region of human MxA GTPase is involved in GTPase activation and interaction with viral target structures. FEBS Lett. 463, 24-28
37. Pitossi, F., Blank, A., Schröder, A., Schwarz, A., Hüssi, P., Schwemmle, M., Pavlovic, J., and Staeheli, P. (1993) A functional GTP-binding motif is necessary for antiviral activity of Mx proteins. J. Virol. 67, 6726-6732
38. Ponten, A., Sick, C., Weeber, M., Haller, O., and Kochs, G. (1997) Dominant-negative mutants of human MxA protein: domains in the carboxyl-terminal moiety are important for oligomerization and antiviral activity. J. Virol. 71, 2591-2599
39. Herskovits, J. S., Burgess, C. C., Obar, R. A., and Vallee, R. B. (1993) Effects of mutant rat dynamin on endocytosis. J. Cell Biol. 122, 565-578
40. Damke, H., Baba, T., Warnock, D. E., and Schmid, S. L. (1994) Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J. Cell Biol. 127, 915-934
41. Sundborger, A. C., Fang, S., Heymann, J. A., Ray, P., Chappie, J. S., and Hinshaw, J. E. (2014) A dynamin mutant defines a superconstricted prefission state. Cell Rep. 8, 734-742
42. Marks, B., Stowell, M. H., Vallis, Y., Mills, I. G., Gibson, A., Hopkins, C. R., and McMahon, H. T. (2001) GTPase activity of dynamin and resulting conformation change are essential for endocytosis. Nature 410, 231-235
43. Song, B. D., Leonard, M., and Schmid, S. L. (2004) Dynamin GTPase domain mutants that differentially affect GTP binding, GTP hydrolysis, and clathrin-mediated endocytosis. J. Biol. Chem. 279, 40431-40436
44. Egea, P. F., Shan, S. O., Napetschnig, J., Savage, D. F., Walter, P., and Stroud, R. M. (2004) Substrate twinning activates the signal recognition particle and its receptor. Nature 427, 215-221
45. Shan, S. O., Stroud, R. M., and Walter, P. (2004) Mechanism of association and reciprocal activation of two GTPases. PLoS Biol. 2, e320
46. Shan, S. O., and Walter, P. (2005) Molecular crosstalk between the nucleotide specificity determinant of the SRP GTPase and the SRP receptor. Biochemistry 44, 6214-6222
47. Frese, M., Kochs, G., Meier-Dieter, U., Siebler, J., and Haller, O. (1995) Human MxA protein inhibits tick-borne Thogoto virus but not Dhori virus. J. Virol. 69, 3904-3909
48. Pavlovic, J., Arzet, H. A., Hefti, H. P., Frese, M., Rost, D., Ernst, B., Kolb, E., Staeheli, P., and Haller, O. (1995) Enhanced virus resistance of transgenic mice expressing the human MxA protein. J. Virol. 69, 4506-4510
49. Maines, T. R., Lu, X. H., Erb, S. M., Edwards, L., Guarner, J., Greer, P. W., Nguyen, D. C., Szretter, K. J., Chen, L. M., Thawatsupha, P., Chittaganpitch, M., Waicharoen, S., Nguyen, D. T., Nguyen, T., Nguyen, H. H., et al. (2005) Avian influenza (H5N1) viruses isolated from humans in Asia in 2004 exhibit increased virulence in mammals. J. Virol. 79, 11788-11800
50. Duc, T. T., Farnir, F., Michaux, C., Desmecht, D., and Cornet, A. (2012) Detection of new biallelic polymorphisms in the human MxA gene. Mol. Biol. Rep. 39, 8533-8538
51. Ghosh, A., Praefcke, G. J., Renault, L., Wittinghofer, A., and Herrmann, C. (2006) How guanylate-binding proteins achieve assembly-stimulated processive cleavage of GTP to GMP. Nature 440, 101-104
52. Melén, K., Ronni, T., Broni, B., Krug, R. M., von Bonsdorff, C. H., and Julkunen, I. (1992) Interferon-induced Mx proteins form oligomers and contain a putative leucine zipper. J. Biol. Chem. 267, 25898-25907
53. Di Paolo, C., Hefti, H. P., Meli, M., Landis, H., and Pavlovic, J. (1999) Intramolecular backfolding of the carboxyl-terminal end of MxA protein is a prerequisite for its oligomerization. J. Biol. Chem. 274, 32071-32078
54. Schmidt, G., Lenzen, C., Simon, I., Deuter, R., Cool, R. H., Goody, R. S., and Wittinghofer, A. (1996) Biochemical and biological consequences of changing the specificity of p21ras from guanosine to xanthosine nucleotides. Oncogene 12, 87-96
55. Cool, R. H., Schmidt, G., Lenzen, C. U., Prinz, H., Vogt, D., and Wittinghofer, A. (1999) The Ras mutant D119N is both dominant negative and activated. Mol. Cell. Biol. 19, 6297-6305
56. Steegmaier, M., Oorschot, V., Klumperman, J., and Scheller, R. H. (2000) Syntaxin 17 is abundant in steroidogenic cells and implicated in smooth endoplasmic reticulum membrane dynamics. Mol. Biol. Cell 11, 2719-2731
57. Tazi-Ahnini, R., di Giovine, F. S., McDonagh, A. J., Messenger, A. G., Amadou, C., Cox, A., Duff, G. W., and Cork, M. J. (2000) Structure and polymorphism of the human gene for the interferon-induced p78 protein (MX1): evidence of association with alopecia areata in the Down syndrome region. Hum. Genet. 106, 639-645
58. Everitt, A. R., Clare, S., Pertel, T., John, S. P., Wash, R. S., Smith, S. E., Chin, C. R., Feeley, E. M., Sims, J. S., Adams, D. J., Wise, H. M., Kane, L., Goulding, D., Digard, P., Anttila, V., et al. (2012) IFITM3 restricts the morbidity and mortality associated with influenza. Nature 484, 519-523