Hantaviral proteins: Structure, functions, and role in hantavirus infection

Frontiers in Microbiology

Volumn 6, Issue NOV, 2015, Pages

  Muyangwa, Musalwa ^a   Martynova, Ekaterina V ^a   Khaiboullina, Svetlana F ^a,b   Morzunov, Sergey P ^c   Rizvanov, Albert A ^a  

^a KAZAN FEDERAL UNIVERSITY   (Russian Federation)

^b Nevada Center for Dermatology   (United States)

^c UNIVERSITY OF NEVADA SCHOOL OF MEDICINE   (United States)

Author keywords

Glycoprotein; Hantavirus; MxA protein; Nucleocapsid protein; Reassortment

Indexed keywords

BETA INTERFERON; HANTAVIRAL PROTEIN; INTERFERON; INTERFERON REGULATORY FACTOR 1; INTERFERON REGULATORY FACTOR 3; INTERFERON REGULATORY FACTOR 7; INTERFERON REGULATORY FACTOR 9; MYXOVIRUS RESISTANCE PROTEIN A; PROTEIN KINASE R; RANTES; RIBONUCLEOPROTEIN; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 3; UNCLASSIFIED DRUG; VASCULOTROPIN; VIRUS GLYCOPROTEIN; VIRUS NUCLEOPROTEIN; VIRUS PROTEIN;

ANTIVIRAL ACTIVITY; GENETIC REASSORTMENT; HANTAVIRUS CARDIOPULMONARY SYNDROME; HANTAVIRUS INFECTION; HEMORRHAGIC FEVER WITH RENAL SYNDROME; HUMAN; INNATE IMMUNITY; LIFE CYCLE; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; PROTEIN STRUCTURE; REVIEW; RIFT VALLEY FEVER VIRUS; TRANSCRIPTION REGULATION; VIRUS GENOME; VIRUS REPLICATION; VIRUS VIRULENCE;

EID: 84949761183     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.01326     Document Type: Review

References (79)

1. Alff, P. J., Gavrilovskaya, I. N., Gorbunova, E., Endriss, K., Chong, Y., Geimonen, E., et al. (2006). The pathogenic NY-1 Hantavirus G1 cytoplasmic tail inhibits RIG-I-and TBK-1-directed interferon responses. J. Virol. 80, 9676-9686. doi: 10.1128/JVI.00508-506
2. Alff, P. J., Sen, N., Gorbunova, E., Gavrilovskaya, I. N., and Mackow, E. R. (2008). The NY-1 Hantavirus Gn cytoplasmic tail coprecipitates TRAF3 and inhibits cellular interferon responses by disrupting TBK1-TRAF3 complex formation. J. Virol. 82, 9115-9122. doi: 10.1128/JVI.00290-08
3. Amada, T., Yoshimatsu, K., Yasuda, S. P., Shimizu, K., Koma, T., Hayashimoto, N., et al. (2013). Rapid, whole blood diagnostic test for detecting anti-Hantavirus antibody in rats. J. Virol. Methods 193, 42-49. doi: 10.1016/j.jviromet.2013.04.021
4. Baigent, S. J., Zhang, G., Fray, M. D., Flick-Smith, H., Goodbourn, S., and Mccauley, J. W. (2002). Inhibition of beta interferon transcription by noncytopathogenic bovine viral diarrhea virus is through an interferon regulatory factor 3-dependent mechanism. J. Virol. 76, 8979-8988. doi: 10.1128/JVI.76.18.8979-8988.2002
5. Battisti, A. J., Chu, Y. K., Chipman, P. R., Kaufmann, B., Jonsson, C. B., and Rossmann, M. G. (2011). Structural studies of Hantaan virus. J. Virol. 85, 835-841. doi: 10.1128/JVI.01847-10
6. Beaty, B. J., Holterman, M., Tabachnick, W., Shope, R. E., Rozhon, E. J., and Bishop, D. H. (1981). Molecular basis of bunyavirus transmission by mosquitoes: role of the middle-sized RNA segment. Science 211, 1433-1435. doi: 10.1126/science.6781068
7. Beaty, B. J., Sundin, D. R., Chandler, L. J., and Bishop, D. H. (1985). Evolution of bunyaviruses by genome reassortment in dually infected mosquitoes (Aedes triseriatus). Science 230, 548-550. doi: 10.1126/science.4048949
8. Beierle, E. A., Strande, L. F., and Chen, M. K. (2002). VEGF upregulates Bcl-2 expression and is associated with decreased apoptosis in neuroblastoma cells. J. Pediatr. Surg. 37, 467-471. doi: 10.1053/jpsu.2002.30868
9. Chandler, L. J., Hogge, G., Endres, M., Jacoby, D. R., Nathanson, N., and Beaty, B. J. (1991). Reassortment of la crosse and tahyna bunyaviruses in Aedes triseriatus mosquitoes. Virus Res. 20, 181-191. doi: 10.1016/0168-1702(91)90108-8
10. Cimica, V., Dalrymple, N. A., Roth, E., Nasonov, A., and Mackow, E. R. (2014). An innate immunity-regulating virulence determinant is uniquely encoded by the Andes virus nucleocapsid protein. MBio 5:e01088-13. doi: 10.1128/mBio.01088-13
11. Deyde, V. M., Rizvanov, A. A., Chase, J., Otteson, E. W., and St. Jeor, S. C. (2005). Interactions and trafficking of andes and sin nombre Hantavirus glycoproteins G1 and G2. Virology 331, 307-315. doi: 10.1016/j.virol.2004.11.003
12. Elliott, R. M. (1990). Molecular biology of the Bunyaviridae. J. Gen. Virol. 71(Pt 3), 501-522. doi: 10.1099/0022-1317-71-3-501
13. Elliott, R. M., Bouloy, M., Calisher, C. H., Goldbach, R., Moyer, J. T., Nichol, S. T., et al. (2000). "Bunyaviridae". in Virus Taxonomy: The Classification and Nomenclature of Viruses, eds M. H. V. Van Regenmortel, C. M. Fauquet, D. H. L. Bishop, E. B. Carsten, M. K. Estes, S. M. Lemon, et al. (San Diego, CA: Academic Press), 599-621.
14. Enria, D. A., Briggiler, A. M., Pini, N., and Levis, S. (2001). Clinical manifestations of New World Hantaviruses. Curr. Top. Microbiol. Immunol. 256, 117-134. doi: 10.1007/978-3-642-56753-7_7
15. Estrada, D. F., Boudreaux, D. M., Zhong, D., St. Jeor, S. C., and De Guzman, R. N. (2009). The Hantavirus glycoprotein G1 tail contains dual CCHC-type classical zinc fingers. J. Biol. Chem. 284, 8654-8660. doi: 10.1074/jbc. M808081200
16. Estrada, D. F., Conner, M., Jeor, S. C., and Guzman, R. N. (2011). The structure of the Hantavirus zinc finger domain is conserved and represents the only natively folded region of the gn cytoplasmic tail. Front. Microbiol. 2:251. doi: 10.3389/fmicb.2011.00251
17. Estrada, D. F., and De Guzman, R. N. (2011). Structural characterization of the crimean-congo hemorrhagic fever virus Gn tail provides insight into virus assembly. J. Biol. Chem. 286, 21678-21686. doi: 10.1074/jbc. M110.216515
18. Finlay, B. B., and McFadden, G. (2006). Anti-immunology: evasion of the host immune system by bacterial and viral pathogens. Cell 124, 767-782. doi: 10.1016/j.cell.2006.01.034
19. Gavrilovskaya, I. N., Shepley, M., Shaw, R., Ginsberg, M. H., and Mackow, E. R. (1998). beta3 Integrins mediate the cellular entry of Hantaviruses that cause respiratory failure. Proc. Natl. Acad. Sci. U.S.A. 95, 7074-7079. doi: 10.1073/pnas.95.12.7074
20. Geimonen, E., Neff, S., Raymond, T., Kocer, S. S., Gavrilovskaya, I. N., and Mackow, E. R. (2002). Pathogenic and nonpathogenic Hantaviruses differentially regulate endothelial cell responses. Proc. Natl. Acad. Sci. U.S.A. 99, 13837-13842. doi: 10.1073/pnas.192298899
21. Gil, J., and Esteban, M. (2000). Induction of apoptosis by the dsRNA-dependent protein kinase (PKR): mechanism of action. Apoptosis 5, 107-114. doi: 10.1023/A:1009664109241
22. Goodbourn, S., Didcock, L., and Randall, R. E. (2000). Interferons: cell signalling, immune modulation, antiviral response and virus countermeasures. J. Gen. Virol. 81, 2341-2364. doi: 10.1099/0022-1317-81-10-2341
23. Haller, O., and Kochs, G. (2002). Interferon-induced mx proteins: dynamin-like GTPases with antiviral activity. Traffic 3, 710-717. doi: 10.1034/j.1600-0854.2002.31003.x
24. Henderson, W. W., Monroe, M. C., St. Jeor, S. C., Thayer, W. P., Rowe, J. E., Peters, C. J., et al. (1995). Naturally occurring Sin Nombre virus genetic reassortants. Virology 214, 602-610. doi: 10.1006/viro.1995.0071
25. Hepojoki, J., Strandin, T., Lankinen, H., and Vaheri, A. (2012). Hantavirus structure-molecular interactions behind the scene. J. Gen. Virol. 93, 1631-1644. doi: 10.1099/vir.0.042218-10
26. Hepojoki, J., Vaheri, A., and Strandin, T. (2014). The fundamental role of endothelial cells in Hantavirus pathogenesis. Front. Microbiol. 5:727. doi: 10.3389/fmicb.2014.00727
27. Horisberger, M. A., Wathelet, M., Szpirer, J., Szpirer, C., Islam, Q., Levan, G., et al. (1988). cDNA cloning and assignment to chromosome 21 of IFI-78K gene, the human equivalent of murine Mx gene. Somat. Cell Mol. Genet. 14, 123-131. doi: 10.1007/BF01534397
28. Huiskonen, J. T., Hepojoki, J., Laurinmaki, P., Vaheri, A., Lankinen, H., Butcher, S. J., et al. (2010). Electron cryotomography of Tula Hantavirus suggests a unique assembly paradigm for enveloped viruses. J. Virol. 84, 4889-4897.
29. Jonsson, C. B., Figueiredo, L. T., and Vapalahti, O. (2010). A global perspective on Hantavirus ecology, epidemiology, and disease. Clin. Microbiol. Rev. 23, 412-441. doi: 10.1128/CMR.00062-09
30. Kanerva, M., Melen, K., Vaheri, A., and Julkunen, I. (1996). Inhibition of Puumala and Tula Hantaviruses in Vero cells by MxA protein. Virology 224, 55-62. doi: 10.1006/viro.1996.0506
31. Kang, W., Huang, C., Bai, X., Yang, W., and Li, G. (2002). [A preliminary genetic reassortment between Hantaan virus and Seoul virus strains]. Zhonghua Liu Xing Bing Xue Za Zhi 23, 46-49.
32. Khaiboullina, S. F., Netski, D. M., Krumpe, P., and St. Jeor, S. C. (2000). Effects of tumor necrosis factor alpha on Sin Nombre virus infection in vitro. J. Virol. 74, 11966-11971. doi: 10.1128/JVI.74.24.11966-11971.2000
33. Khaiboullina, S. F., Rizvanov, A. A., Deyde, V. M., and St. Jeor, S. C. (2005). Andes virus stimulates interferon-inducible MxA protein expression in endothelial cells. J. Med. Virol. 75, 267-275. doi: 10.1002/jmv.20266
34. Khaiboullina, S. F., Rizvanov, A. A., Otteson, E., Miyazato, A., Maciejewski, J., and St. Jeor, S. (2004). Regulation of cellular gene expression in endothelial cells by sin nombre and prospect hill viruses. Viral Immunol. 17, 234-251. doi: 10.1089/0882824041310504
35. 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. doi: 10.1073/pnas.052430399
36. Krautkramer, E., Zeier, M., and Plyusnin, A. (2013). Hantavirus infection: an emerging infectious disease causing acute renal failure. Kidney Int. 83, 23-27. doi: 10.1038/ki.2012.360
37. Kumar, A., Yang, Y. L., Flati, V., Der, S., Kadereit, S., Deb, A., et al. (1997). Deficient cytokine signaling in mouse embryo fibroblasts with a targeted deletion in the PKR gene: role of IRF-1 and NF-kappaB. EMBO J. 16, 406-416. doi: 10.1093/emboj/16.2.406
38. Li, D., Schmaljohn, A. L., Anderson, K., and Schmaljohn, C. S. (1995). Complete nucleotide sequences of the M and S segments of two Hantavirus isolates from California: evidence for reassortment in nature among viruses related to Hantavirus pulmonary syndrome. Virology 206, 973-983. doi: 10.1006/viro.1995.1020
39. Lyles, D. S. (2013). Assembly and budding of negative-strand RNA viruses. Adv. Virus Res. 85, 57-90. doi: 10.1016/B978-0-12-408116-1.00003-3
40. Mackow, E. R., Dalrymple, N. A., Cimica, V., Matthys, V., Gorbunova, E., and Gavrilovskaya, I. (2014). Hantavirus interferon regulation and virulence determinants. Virus Res. 187, 65-71. doi: 10.1016/j.virusres.2013.12.041
41. Macneil, A., Nichol, S. T., and Spiropoulou, C. F. (2011). Hantavirus pulmonary syndrome. Virus Res. 162, 138-147. doi: 10.1016/j.virusres.2011.09.017
42. Matthys, V., Gorbunova, E. E., Gavrilovskaya, I. N., Pepini, T., and Mackow, E. R. (2011). The C-terminal 42 residues of the Tula virus Gn protein regulate interferon induction. J. Virol. 85, 4752-4760. doi: 10.1128/JVI.01945-10
43. Matthys, V. S., Cimica, V., Dalrymple, N. A., Glennon, N. B., Bianco, C., and Mackow, E. R. (2014). Hantavirus GnT elements mediate TRAF3 binding and inhibit RIG-I/TBK1-directed beta interferon transcription by blocking IRF3 phosphorylation. J. Virol. 88, 2246-2259. doi: 10.1128/JVI.02647-13
44. Melchjorsen, J., and Paludan, S. R. (2003). Induction of RANTES/CCL5 by herpes simplex virus is regulated by nuclear factor kappa B and interferon regulatory factor 3. J. Gen. Virol. 84, 2491-2495. doi: 10.1099/vir.0.19159-0
45. Mir, M. A., Duran, W. A., Hjelle, B. L., Ye, C., and Panganiban, A. T. (2008). Storage of cellular 5' mRNA caps in P bodies for viral cap-snatching. Proc. Natl. Acad. Sci. U.S.A. 105, 19294-19299. doi: 10.1073/pnas.0807211105
46. Mir, M. A., and Panganiban, A. T. (2004). Trimeric Hantavirus nucleocapsid protein binds specifically to the viral RNA panhandle. J. Virol. 78, 8281-8288. doi: 10.1128/JVI.78.15.8281-8288.2004
47. Pavlovic, J., Schroder, A., Blank, A., Pitossi, F., and Staeheli, P. (1993). Mx proteins: GTPases involved in the interferon-induced antiviral state. Ciba Found. Symp. 176, 233-243; discussion 243-237.
48. Pensiero, M. N., and Hay, J. (1992). The Hantaan virus M-segment glycoproteins G1 and G2 can be expressed independently. J. Virol. 66, 1907-1914.
49. Pettersson, R. F., and Melin, L. (1996). "Synthesis, assembly and intracellular transport of Bunyaviridae membrane proteins". in The Bunyaviridae, 1st Edn, ed. R. M. Elliott (New York, NY: Plenum Press), 159-188. doi: 10.1007/978-1-4899-1364-7_7
50. Pidgeon, G. P., Barr, M. P., Harmey, J. H., Foley, D. A., and Bouchier-Hayes, D. J. (2001). Vascular endothelial growth factor (VEGF) upregulates BCL-2 and inhibits apoptosis in human and murine mammary adenocarcinoma cells. Br. J. Cancer 85, 273-278. doi: 10.1054/bjoc.2001.1876
51. Plyusnin, A., Cheng, Y., Lehvaslaiho, H., and Vaheri, A. (1996). Unique and conserved features of Tula Hantavirus M gene encoding envelope glycoproteins G1 and G2. Virus Genes 12, 257-263. doi: 10.1007/BF00284646
52. Plyusnin, A., and Morzunov, S. P. (2001). Virus evolution and genetic diversity of Hantaviruses and their rodent hosts. Curr. Top. Microbiol. Immunol 256, 47-75. doi: 10.1007/978-3-642-56753-7_4
53. Plyusnin, A., Vapalahti, O., Lankinen, H., Lehvaslaiho, H., Apekina, N., Myasnikov, Y., et al. (1994). Tula virus: a newly detected Hantavirus carried by European common voles. J. Virol. 68, 7833-7839.
54. Ravkov, E. V., Nichol, S. T., Peters, C. J., and Compans, R. W. (1998). Role of actin microfilaments in Black creek canal virus morphogenesis. J. Virol. 72, 2865-2870.
55. Reich, N. C. (2002). Nuclear/cytoplasmic localization of IRFs in response to viral infection or interferon stimulation. J. Interferon Cytokine Res. 22, 103-109. doi: 10.1089/107999002753452719
56. Rizvanov, A. A., Khaiboullina, S. F., and St. Jeor, S. (2004). Development of reassortant viruses between pathogenic Hantavirus strains. Virology 327, 225-232. doi: 10.1016/j.virol.2004.07.012
57. Rodriguez, L. L., Owens, J. H., Peters, C. J., and Nichol, S. T. (1998). Genetic reassortment among viruses causing Hantavirus pulmonary syndrome. Virology 242, 99-106. doi: 10.1006/viro.1997.8990
58. Ruusala, A., Persson, R., Schmaljohn, C. S., and Pettersson, R. F. (1992). Coexpression of the membrane glycoproteins G1 and G2 of Hantaan virus is required for targeting to the Golgi complex. Virology 186, 53-64. doi: 10.1016/0042-6822(92)90060-3
59. Sall, A. A., de, A Zanotto, P. M., Zeller, H. G., Digoutte, J. P., Thiongane, Y., and Bouloy, M. (1997). Variability of the NS(S) protein among Rift Valley fever virus isolates. J. Gen. Virol. 78(Pt 11), 2853-2858. doi: 10.1099/0022-1317-78-11-2853
60. Schall, T. J., Bacon, K., Toy, K. J., and Goeddel, D. V. (1990). Selective attraction of monocytes and T lymphocytes of the memory phenotype by cytokine RANTES. Nature 347, 669-671. doi: 10.1038/347669a0
61. Schmaljohn, C., and Hjelle, B. (1997). Hantaviruses: a global disease problem. Emerg. Infect. Dis 3, 95-104. doi: 10.3201/eid0302.970202
62. Scmaljohn, C. S., and Hopper, J. W. (2001). "Bunyaviridae: the viruses and their replication". in Fields Virology, eds D. M. Knipe, P. M. Howley, and B. N. Fields (Philadelphia, PA: Lippincott Williams & Wilkins), 1581-1602.
63. Severson, W., Partin, L., Schmaljohn, C. S., and Jonsson, C. B. (1999). Characterization of the Hantaan nucleocapsid protein-ribonucleic acid interaction. J. Biol. Chem. 274, 33732-33739. doi: 10.1074/jbc.274.47.33732
64. Severson, W. E., Xu, X., and Jonsson, C. B. (2001). cis-Acting signals in encapsidation of Hantaan virus S-segment viral genomic RNA by its N protein. J. Virol. 75, 2646-2652. doi: 10.1128/JVI.75.6.2646-2652.2001
65. Shi, X., and Elliott, R. M. (2002). Golgi localization of Hantaan virus glycoproteins requires coexpression of G1 and G2. Virology 300, 31-38. doi: 10.1006/viro.2002.1414
66. Spiropoulou, C. F. (2013). "Hantavirus maturation". in Hantaviruses, eds C. S. Scmaljohn and S. T. Nichol (Berlin: Springer Science & Business Media), 33-44.
67. Spiropoulou, C. F., Goldsmith, C. S., Shoemaker, T. R., Peters, C. J., and Compans, R. W. (2003). Sin Nombre virus glycoprotein trafficking. Virology 308, 48-63. doi: 10.1016/S0042-6822(02)00092-2
68. Sundstrom, J. B., Mcmullan, L. K., Spiropoulou, C. F., Hooper, W. C., Ansari, A. A., Peters, C. J., et al. (2001). Hantavirus infection induces the expression of RANTES and IP-10 without causing increased permeability in human lung microvascular endothelial cells. J. Virol. 75, 6070-6085. doi: 10.1128/JVI.75.13.6070-6085.2001
69. Urquidi, V., and Bishop, D. H. (1992). Non-random reassortment between the tripartite RNA genomes of La Crosse and snowshoe hare viruses. J. Gen. Virol. 73(Pt 9), 2255-2265. doi: 10.1099/0022-1317-73-9-2255
70. Vapalahti, O., Kallio-Kokko, H., Narvanen, A., Julkunen, I., Lundkvist, A., Plyusnin, A., et al. (1995). Human B-cell epitopes of Puumala virus nucleocapsid protein, the major antigen in early serological response. J. Med. Virol. 46, 293-303. doi: 10.1002/jmv.1890460402
71. Wang, Z., and Mir, M. A. (2015). Andes virus nucleocapsid protein interrupts protein kinase R dimerization to counteract host interference in viral protein synthesis. J. Virol. 89, 1628-1639. doi: 10.1128/JVI.02347-14
72. Webster, R. G., and Laver, W. G. (1971). Antigenic variation in influenza virus. Biology and chemistry. Prog. Med. Virol. 13, 271-338.
73. Welsch, S., Muller, B., and Krausslich, H. G. (2007). More than one door-Budding of enveloped viruses through cellular membranes. FEBS Lett. 581, 2089-2097. doi: 10.1016/j.febslet.2007.03.060
74. Yamauchi, Y., and Helenius, A. (2013). Virus entry at a glance. J. Cell Sci. 126, 1289-1295. doi: 10.1242/jcs.119685
75. Yoneyama, M., and Fujita, T. (2007). Function of RIG-I-like receptors in antiviral innate immunity. J. Biol. Chem. 282, 15315-15318. doi: 10.1074/jbc. R700007200
76. Yoshimatsu, K., and Arikawa, J. (2014). Serological diagnosis with recombinant N antigen for Hantavirus infection. Virus Res. 187, 77-83. doi: 10.1016/j.virusres.2013.12.040
77. Young, J. F., and Palese, P. (1979). Evolution of human influenza A viruses in nature: recombination contributes to genetic variation of H1N1 strains. Proc. Natl. Acad. Sci. U.S.A. 76, 6547-6551. doi: 10.1073/pnas.76.12.6547
78. Zaki, S. R., Greer, P. W., Coffield, L. M., Goldsmith, C. S., Nolte, K. B., Foucar, K., et al. (1995). Hantavirus pulmonary syndrome. Pathogenesis of an emerging infectious disease. Am. J. Pathol. 146, 552-579.
79. Zhang, X. L., Wang, X. H., and Liu, C. Z. (1987). [Detection of viral antigens in various organs in 14 fatal cases of epidemic hemorrhagic fever]. Zhonghua Nei Ke Za Zhi 26, 461-463, 509-410