New and Old World hantaviruses differentially utilize host cytoskeletal components during their life cycles

Virology

Volumn 374, Issue 1, 2008, Pages 138-150

  Ramanathan, Harish N ^a   Jonsson, Colleen B ^b  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b Drug Discovery Division   (United States)

Author keywords

Cytoskeleton; ERGIC; Hantavirus; Nucleocapsid protein; Trafficking

Indexed keywords

ACTIN FILAMENT; ANDES VIRUS; ANIMAL CELL; ARTICLE; BLACK CREEK CANAL VIRUS; CONTROLLED STUDY; CYTOSKELETON; HANTAVIRUS; HOST PATHOGEN INTERACTION; LIFE CYCLE; MICROTUBULE ASSEMBLY; NONHUMAN; PRIORITY JOURNAL; PROTEIN TRANSPORT; SEOUL VIRUS; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS INFECTION; VIRUS REPLICATION; VIRUS SURVIVAL;

ACTINS; ANIMALS; CERCOPITHECUS AETHIOPS; CYTOSKELETON; ENDOPLASMIC RETICULUM; GOLGI APPARATUS; HANTAVIRUS; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; MICROTUBULES; NUCLEOCAPSID PROTEINS; VERO CELLS;

ANDES VIRUS; BLACK CREEK CANAL VIRUS; HANTAVIRUS; SEOUL VIRUS;

EID: 41649095179     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2007.12.030     Document Type: Article

References (51)

1. Burkhardt J.K., Echeverri C.J., Nilsson T., and Vallee R.B. Overexpression of the dynamitin (p50) subunit of the dynactin complex disrupts dynein-dependent maintenance of membrane organelle distribution. J. Cell Biol. 139 (1997) 469-484
2. Carvalho Z.G., De Matos A.P., and Rodrigues-Pousada C. Association of African swine fever virus with the cytoskeleton. Virus Res. 11 (1988) 175-192
3. Chen M., Goorha R., and Murti K.G. Interaction of frog virus 3 with the cytomatrix. IV. Phosphorylation of vimentin precedes the reorganization of intermediate filaments around the virus assembly sites. J. Gen. Virol. 67 (1986) 915-922
4. Chung D.H., Sun Y., Parker W.B., Arterburn J.B., Bartolucci A., and Jonsson C.B. Ribavirin reveals a lethal threshold of allowable mutation frequency for Hantaan virus. J. Virol. 81 (2007) 11722-11729
5. Cordo S.M., and Candurra N.A. Intermediate filament integrity is required for Junin virus replication. Virus Res. 97 (2003) 47-55
6. Damm E.M., Pelkmans L., Kartenbeck J., Mezzacasa A., Kurzchalia T., and Helenius A. Clathrin- and caveolin-1-independent endocytosis: entry of simian virus 40 into cells devoid of caveolae. J. Cell Biol. 168 (2005) 477-488
7. Gahmberg N., Kuismanen E., Keranen S., and Pettersson R.F. Uukuniemi virus glycoproteins accumulate in and cause morphological changes of the Golgi complex in the absence of virus maturation. J. Virol. 57 (1986) 899-906
8. Gavrilovskaya I.N., Brown E.J., Ginsberg M.H., and Mackow E.R. Cellular entry of hantaviruses which cause hemorrhagic fever with renal syndrome is mediated by beta3 integrins. J. Virol. 73 (1999) 3951-3959
9. Gavrilovskaya I.N., Shepley M., Shaw R., Ginsberg M.H., and Mackow E.R. Beta3 integrins mediate the cellular entry of hantaviruses that cause respiratory failure. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 7074-7079
10. Goldsmith C.S., Elliott L.H., Peters C.J., and Zaki S.R. Ultrastructural characteristics of Sin Nombre virus, causative agent of hantavirus pulmonary syndrome. Arch. Virol. 140 (1995) 2107-2122
11. Jantti J., Hilden P., Ronka H., Makiranta V., Keranen S., and Kuismanen E. Immunocytochemical analysis of Uukuniemi virus budding compartments: role of the intermediate compartment and the Golgi stack in virus maturation. J. Virol. 71 (1997) 1162-1172
12. Jin M., Park J., Lee S., Park B., Shin J., Song K.J., Ahn T.I., Hwang S.Y., Ahn B.Y., and Ahn K. Hantaan virus enters cells by clathrin-dependent receptor-mediated endocytosis. Virology 294 (2002) 60-69
13. Jonsson C.B., and Schmaljohn C.S. Replication of hantaviruses. Curr. Top. Microbiol. Immunol. 256 (2001) 15-32
14. Kariwa H., Tanabe H., Mizutani T., Kon Y., Lokugamage K., Lokugamage N., Iwasa M.A., Hagiya T., Araki K., Yoshimatsu K., Arikawa J., and Takashima I. Synthesis of Seoul virus RNA and structural proteins in cultured cells. Arch. Virol. 148 (2003) 1671-1685
15. Kaukinen P., Kumar V., Tulimaki K., Engelhardt P., Vaheri A., and Plyusnin A. Oligomerization of hantavirus N protein: C-terminal alpha-helices interact to form a shared hydrophobic space. J. Virol. 78 (2004) 13669-13677
16. Kaukinen P., Vaheri A., and Plyusnin A. Hantavirus nucleocapsid protein: a multifunctional molecule with both housekeeping and ambassadorial duties. Arch. Virol. 150 (2005) 1693-1713
17. Kuismanen E. Posttranslational processing of Uukuniemi virus glycoproteins G1 and G2. J. Virol. 51 (1984) 806-812
18. Kukkonen S.K., Vaheri A., and Plyusnin A. Tula hantavirus L protein is a 250 kDa perinuclear membrane-associated protein. J. Gen. Virol. 85 (2004) 1181-1189
19. Lake J.A., Carr J., Feng F., Mundy L., Burrell C., and Li P. The role of Vif during HIV-1 infection: interaction with novel host cellular factors. J. Clin. Virol. 26 (2003) 143-152
20. Lee H.W., and Cho H.J. Electron microscope appearance of Hantaan virus, the causative agent of Korean haemorrhagic fever. Lancet 1 (1981) 1070-1072
21. Matsuoka Y., Chen S.Y., and Compans R.W. Bunyavirus protein transport and assembly. Curr. Top. Microbiol. Immunol. 169 (1991) 161-179
22. Matsuoka Y., Ihara T., Bishop D.H., and Compans R.W. Intracellular accumulation of Punta Toro virus glycoproteins expressed from cloned cDNA. Virology 167 (1988) 251-260
23. Moolenaar R.L., Breiman R.F., and Peters C.J. Hantavirus pulmonary syndrome. Semin. Respir. Infect. 12 (1997) 31-39
24. Moolenaar R.L., Dalton C., Lipman H.B., Umland E.T., Gallaher M., Duchin J.S., Chapman L., Zaki S.R., Ksiazek T.G., Rollin P.E., et al. Clinical features that differentiate hantavirus pulmonary syndrome from three other acute respiratory illnesses. Clin. Infect. Dis 21 (1995) 643-649
25. Murti K.G., Goorha R., and Klymkowsky M.W. A functional role for intermediate filaments in the formation of frog virus 3 assembly sites. Virology 162 (1988) 264-269
26. Nedellec P., Vicart P., Laurent-Winter C., Martinat C., Prevost M.C., and Brahic M. Interaction of Theiler's virus with intermediate filaments of infected cells. J. Virol. 72 (1998) 9553-9560
27. Nichol, S.T.,, 2001. Bunyaviruses p. 1603-1633. In Fields virology. D.M. Knipe, P.M. Howley, D.E. Griffin, R.A. Lamb, M.A. Martin, B. Roizman, and S.E. Straus (ed.) In "Fields virology", Vol. 2, pp. 1603-1633. 2 vols. Lippincott Williams & Wilkins, Philadelphia, Pa.
28. Novoa R.R., Calderita G., Arranz R., Fontana J., Granzow H., and Risco C. Virus factories: associations of cell organelles for viral replication and morphogenesis. Biol. Cell 97 (2005) 147-172
29. Pelkmans L., and Helenius A. Insider information: what viruses tell us about endocytosis. Curr. Opin. Cell Biol. 15 (2003) 414-422
30. Pelkmans L., Kartenbeck J., and Helenius A. Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat. Cell Biol. 3 (2001) 473-483
31. Penningroth S.M., Cheung A., Bouchard P., Gagnon C., and Bardin C.W. Dynein ATPase is inhibited selectively in vitro by erythro-9-[3-2-(hydroxynonyl)]adenine. Biochem. Biophys. Res. Commun. 104 (1982) 234-240
32. Pensiero M.N., Jennings G.B., Schmaljohn C.S., and Hay J. Expression of the Hantaan virus M genome segment by using a vaccinia virus recombinant. J. Virol. 62 (1988) 696-702
33. Qualmann B., Kessels M.M., and Kelly R.B. Molecular links between endocytosis and the actin cytoskeleton. J. Cell Biol. 150 (2000) F111-F116
34. Ramanathan H.N., Chung D.H., Plane S.J., Sztul E., Chu Y.K., Guttieri M.C., McDowell M., Ali G., and Jonsson C.B. Dynein-dependent transport of the Hantaan virus nucleocapsid protein to the endoplasmic reticulum-Golgi intermediate compartment. J. Virol. 81 (2007) 8634-8647
35. Ravkov E.V., and Compans R.W. Hantavirus nucleocapsid protein is expressed as a membrane-associated protein in the perinuclear region. J. Virol. 75 (2001) 1808-1815
36. Ravkov E.V., Nichol S.T., and Compans R.W. Polarized entry and release in epithelial cells of Black Creek Canal virus, a New World hantavirus. J. Virol. 71 (1997) 1147-1154
37. Ravkov E.V., Nichol S.T., Peters C.J., and Compans R.W. Role of actin microfilaments in Black Creek Canal virus morphogenesis. J. Virol. 72 (1998) 2865-2870
38. Reichelt M., Stertz S., Krijnse-Locker J., Haller O., and Kochs G. Missorting of LaCrosse virus nucleocapsid protein by the interferon-induced MxA GTPase involves smooth ER membranes. Traffic 5 (2004) 772-784
39. Rowe R.K., and Pekosz A. Bidirectional virus secretion and nonciliated cell tropism following Andes virus infection of primary airway epithelial cell cultures. J. Virol. 80 (2006) 1087-1097
40. Salanueva I.J., Novoa R.R., Cabezas P., Lopez-Iglesias C., Carrascosa J.L., Elliott R.M., and Risco C. Polymorphism and structural maturation of Bunyamwera virus in Golgi and post-Golgi compartments. J. Virol. 77 (2003) 1368-1381
41. Schmaljohn C.S., Hasty S.E., Harrison S.A., and Dalrymple J.M. Characterization of Hantaan virions, the prototype virus of hemorrhagic fever with renal syndrome. J. Infect. Dis. 148 (1983) 1005-1012
42. Schmaljohn C.S., Hasty S.E., Rasmussen L., and Dalrymple J.M. Hantaan virus replication: effects of monensin, tunicamycin and endoglycosidases on the structural glycoproteins. J. Gen. Virol. 67 (1986) 707-717
43. Schmaljohn, C. S., and Hooper, J. W., 2001. Bunyaviridae: the viruses and their replication, p. 1581-1633. In Fields virology D.M. Knipe, P.M. Howley, D.E. Griffin, R.A. Lamb, M.A. Martin, B. Roizman, and S.E. Straus (ed.). In "Fields virology", Vol. 2, pp. 1581-1633. 2 vols. Lippincott Williams & Wilkins, Philadelphia, Pa.
44. Schmaljohn, C.S., and Nichol, S.T.,, 2007. Bunyaviridae. In "Fields virology" (D.M. Knipe, P.M. Howley, D.E. Griffin, R.A. Lamb, M.A. Martin, R.B., and S.S.E., Eds.), Vol. 2, pp. 1741-1789. 2vols. Lippincott Williams & Wilkins, Philadelphia.
45. Sieczkarski S.B., and Whittaker G.R. Dissecting virus entry via endocytosis. J. Gen. Virol. 83 (2002) 1535-1545
46. Spiropoulou C.F. Hantavirus maturation. Current Topics in Microbiology and Immunology 256 (2001) 33-46
47. Stefanovic S., Windsor M., Nagata K.I., Inagaki M., and Wileman T. Vimentin rearrangement during African swine fever virus infection involves retrograde transport along microtubules and phosphorylation of vimentin by calcium calmodulin kinase II. J. Virol. 79 (2005) 11766-11775
48. Sun Y., Chung D.H., Chu Y.K., Jonsson C.B., and Parker W.B. Activity of ribavirin against Hantaan virus correlates with production of ribavirin-5'-triphosphate, not with inhibition of IMP dehydrogenase. Antimicrob. Agents Chemother. 51 (2007) 84-88
49. Wang S., Zang L., Feng M., Liang Z., Zheng S., Zhang L., Jiang Z., and Chen D. Transmission electron microscopic study of the hemorrhagic spots in patients with epidemic hemorrhagic fever in the early stage. Ultrastruct. Pathol. 21 (1997) 281-287
50. Wasmoen T.L., Kakach L.T., and Collett M.S. Rift Valley fever virus M segment: cellular localization of M segment-encoded proteins. Virology 166 (1988) 275-280
51. Zaki S.R., Greer P.W., Coffield L.M., Goldsmith C.S., Nolte K.B., Foucar K., Feddersen R.M., Zumwalt R.E., Miller G.L., Khan A.S., et al. Hantavirus pulmonary syndrome. Pathogenesis of an emerging infectious disease. Am. J. Pathol. 146 (1995) 552-579