Multiple regions in dengue virus capsid protein contribute to nuclear localization during virus infection

Journal of General Virology

Volumn 89, Issue 5, 2008, Pages 1254-1264

  Sangiambut, Sutha ^a   Keelapang, Poonsook ^b   Aaskov, John ^c   Puttikhunt, Chunya ^a   Kasinrerk, Watchara ^a,d   Malasit, Prida ^a,e   Sittisombut, Nopporn ^a,b  

^a NATIONAL SCIENCE AND TECHNOLOGY DEVELOPMENT AGENCY   (Thailand)

^b Faculty of Medicine Chiang Mai University   (Thailand)

^c QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

^d CHIANG MAI UNIVERSITY   (Thailand)

^e MAHIDOL UNIVERSITY   (Thailand)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; CAPSID PROTEIN; PROTEIN C;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CELL LINE; CONTROLLED STUDY; CORRELATION ANALYSIS; DENGUE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; MOSQUITO; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN LOCALIZATION; VERO CELL; VIROGENESIS; VIRUS LATENCY; VIRUS MUTANT; VIRUS REPLICATION; ANIMAL; CELL NUCLEUS; CERCOPITHECUS; CHEMICAL STRUCTURE; CHEMISTRY; DENGUE VIRUS; FLUORESCENCE MICROSCOPY; GENETICS; METABOLISM; PHYSIOLOGY; SITE DIRECTED MUTAGENESIS; SWINE;

DENGUE VIRUS; MIRIDAE;

AMINO ACID SUBSTITUTION; ANIMALS; CAPSID PROTEINS; CELL LINE; CELL NUCLEUS; CERCOPITHECUS AETHIOPS; CULICIDAE; DENGUE VIRUS; MICROSCOPY, FLUORESCENCE; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; SWINE; VIRUS REPLICATION;

EID: 44649173963     PISSN: 00221317     EISSN: None     Source Type: Journal    
DOI: 10.1099/vir.0.83264-0     Document Type: Article

References (50)

1. Amberg, S. M. & Rice, C. M. (1999). Mutagenesis of the NS2B-NS3-mediated cleavage site in the flavivirus capsid protein demonstrates a requirement for coordinated processing. J Virol 73, 8083-8094.
2. Amberg, S. M., Nestorowicz, D., McCourt, D. W. & Rice, C. M. (1994). NS2B-3 proteinase-mediated processing in the yellow fever virus structural region: in vitro and in vivo studies. J Virol 68, 3794-3802.
3. Andersen, J. S., Lam, Y. W., Leung, A. K., Ong, S. E., Lyon, C. E., Lamond, A. I. & Mann, M. (2005). Nucleolar proteome dynamics. Nature 433, 77-83.
4. Avirutnan, P., Malasit, P., Selinger, B., Bhakdi, S. & Husmann, M. (1998). Dengue virus infection of human endothelial cells leads to chemokine production, complement activation, and apoptosis. I Immunol 161, 6338-6346.
5. Boisvert, F. M., Van Koningsbruggen, S., Navascues, J. & Lamond, A. L. (2007). The multifunctional nucleolus. Nat Rev Mol Cell Biol 8, 574-585.
6. Brooks, A. J., Johansson, M., John, A. V., Xu, Y., Jans, D. A. & Vasudevan, S. G. (2002). The interdomain region of dengue NS5 protein that binds to the viral helicase NS3 contains independently functional importin beta 1 and importin alpha/beta-recognized nuclear localization signals. J Biol Chem 277, 36399-36407.
7. Bui, M., Myers, J. E. & Whittaker, G. R. (2002). Nucleo-cytoplasmic localization of influenza virus nucleoprotein depends on cell density and phosphorylation. Virus Res 84, 37-44.
8. Bulich, R. & Aaskov, J. G. (1992). Nuclear localization of dengue 2 virus core protein detected with monoclonal antibodies. J Gen Virol 73, 2999-3003.
9. de Madrid, A. T. & Porterfield, J. S. (1969). A simple micro-culture method for the study of group B arboviruses. Bull World Health Organ 40, 113-121.
10. Dingwall, C. & Laskey, R. A. (1991). Nuclear targeting sequences: a consensus? Trends Biochem Sci 16, 478-481.
11. Görlich, D. & Kutay, U. (1999). Transport between the cell nucleus and the cytoplasm. Annu Rev Cell Dev Biol 15, 607-660.
12. Grieger, J. C., Snowdy, S. & Samulski, R. J. (2006). Separate basic region motifs within the adeno-associated virus capsid proteins are essential for infectivity and assembly. J Virol 80, 5199-5210.
13. Helt, A. M. & Harris, E. (2005). S-phase-dependent enhancement of dengue virus replication in mosquito cells, but not in human cells. J Virol 79, 13218-13230.
14. Henchal, E. A., Gentry, M. K., McCown, J. M. & Brandt, W. E. (1982). Dengue virus-specific and flavivirus group determinants identified with monoclonal antibodies by indirect immunofluorescence. Am J Trop Med Hyg 31, 830-836.
15. Hiscox, J. A. (2007). RNA viruses: hijacking the dynamic nucleolus. Nat Rev Microbiol 5, 119-127.
16. Hogarth, C. A., Calanni, S., Jans, D. & Loveland, K. (2006). Importin α mRNAs have distinct expression profiles during spermatogenesis. Dev Dyn 235, 253-262.
17. Igarashi, A. (1978). Isolation of Singh's Aedes albopictus cell clone sensitive to dengue and chikungunya viruses. J Gen Virol 40, 531-544.
18. Jans, D. A. Xiao, C. Y. & Lam, M. H. (2000). Nuclear targeting signal recognition: a key control point in nuclear transport? Bioessays 22, 532-544.
19. Keelapang, P., Sriburi, R., Supasa, S., Punyadee, N., Songjaeng, A., Jairungsri, A., Puttikhunt, C., Kasinrerk, W., Malasit, P. & Sittisombut, N. (2004). Alterations of pr-M cleavage and virus export in pr-M junction chimeric dengue viruses. J Virol 78, 2367-2381.
20. Khromykh. A. A. & Westaway, E. G. (1996). RNA binding properties of core protein of the flavivirus Kunjin. Arch Virol 141, 685-699.
21. Kohler, M., Speck, C., Christiansen, M., Bischoff, F. R., Prehn, S., Haller, H., Gorlich, D. & Hartmann, E. (1999). Evidence for distinct substrate specificities of importin α family members in nuclear protein import. Mol Cell Biol 19, 7782-7791.
22. Lee, C., Hodgins, D., Calvert, J. G., Welch, S. W., Jolie, R. & Yoo, D. (2006). Mutations within the nuclear localization signal of the porcine reproductive and respiratory syndrome virus nucleocapsid protein attenuate virus replication. Virology 346, 238-250.
23. Li, J., Lim, S. P., Beer, D., Patel, V., Wen, D., Tumanut, C., Tully, D., Williams, J. A., Jiricek, J. & other authors (2005). Functional profiling of recombinant NS3 proteases from all four serotypes of dengue virus using tetrapeptide and octapeptide substrate libraries. J Biol Chem 280, 28766-28774.
24. Lindenbach, B. D. & Rice, C. M. (2001). Flaviviridae: the viruses and their replication. In Fields Virology, 4th edn, vol. 1, pp. 991-1041. Edited by D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman & S. E. Straus. Philadelphia, PA: Lippincott Williams & Wilkins.
25. Llorian, M., Beullens, M., Lesage, B., Nicolaescu, E., Beke, L., Landuyt, W., Ortiz, J. M. & Bollen, M. (2005). Nucleocytoplasmic shuttling of the splicing factor SIPP1. J Biol Chem 280, 38862-38869.
26. Lobigs, M. (1993). Flavivirus premembrane protein cleavage and spike heterodimer secretion require the function of the viral proteinase NS3. Proc Natl Acad Sci U S A 90, 6218-6222.
27. Ma, L., Jones, C. T., Groesch, T. D., Kuhn, R. J. & Post, C. B. (2004). Solution structure of dengue virus capsid protein reveals another fold. Proc Natl Acad Sci U S A 101, 3414-3419.
28. Marg, A., Shan, Y., Meyer, T., Meissner, T., Brandenburg, M. & Vinkemeier, U. (2004). Nucleocytoplasmic shuttling by nucleoporins Nup153 and Nup214 and CRM1-dependent nuclear export control the subcellular distribution of latent Stat1. J Cell Biol 165, 823-833.
29. Marianneau, P., Cardona, A., Edelman, L., Deubel, V. & Desprès, P. (1997). Dengue virus replication in human cells activates NF-κB which in turn induces apoptotic cell death. J Virol 71, 3244-3249.
30. Markoff, L., Falgout, B. & Chang, A. (1997). A conserved internal hydrophobic domain mediates the stable membrane integration of the dengue virus capsid protein. Virology 233, 105-117.
31. Melén, K., Kinnunen, L., Fagerlund, R., Ikonen, N., Twu, K. Y., Krug, R. M. & Julkunen, I. (2007). Nuclear and nucleolar targeting of influenza A virus NS1 protein: striking differences between different virus subtypes. J Virol 81, 5995-6006.
32. Mizrachy, L., Dabush, D., Levy, Y., Aloni, R., Altman, A. & Gafni, Y. (2004). Cloning and characterization of the tomato karyopherin α 1 gene promoter. Dev Growth Differ 46, 515-522.
33. Mizuno, T., Okamoto, T., Yokoi, M., Izumi, M., Kobayashi, A., Hachiya, T., Tamai, K., Inoue, T. & Hanaoka, F. (1996). Identification of the nuclear localization signal of mouse DNA primase: nuclear transport of p46 subunit is facilitated by interaction with p54 subunit. J Cell Sci 109, 2627-2636.
34. Mori, Y., Okabayashi, T., Yamashita, T., Zhao, Z. Wakita, T., Yasui, K., Hasebe, F., Tadano, M., Konishi, E. & Matsuura, Y. (2005). Nuclear localization of Japanese encephalitis virus core protein enhances viral replication. J Virol 79, 3448-3458.
35. Nachury, M. V., Ryder, U. W., Lamond, A. I. & Weis, K. (1998). Cloning and characterization of two hSPP1γ, a tissue-specific nuclear transport factor. Proc Natl Acad Sci U S A 95, 582-587.
36. Ng, M. L., Tan, S. H. & Chu, J. J. (2001). Transport and budding at two distinct sites of visible nucleocapsids of West Nile (Sarafend) virus. J Med Virol 65, 758-764.
37. Niyomrattanakit, P., Yahorava, S., Mutule, I., Mutulis, F., Petrovska, R., Prusis, P., Katzenmeier, G. & Wikberg, J. E. (2006). Probing the substrate specificity of the dengue virus type 2 NS3 serine protease by using internally quenched fluorescent peptides. Biochem J 397, 203-211.
38. Oh, W., Yang, M. R., Lee, E. W., Park, K. M., Pyo, S., Yang, J. S., Lee, H. W. & Song, J. (2006). Jab1 mediates cytoplasmic localization and degradation of West Nile virus capsid protein. J Biol Chem 281, 30166-30174.
39. Pemberton, L. F. & Paschal, B. M. (2005). Mechanisms of receptor-mediated nuclear import and nuclear export. Traffic 6, 187-198.
40. Puttikhunt C., Kasinrerk, W., Srisa-ad, S., Duangchinda, T., Silakate, W., Moonsom, S., Sittisombut, N. & Malasit, P. (2003). Production of anti-dengue NS1 monoclonal antibodies by DNA immunization. J Virol Methods 109, 55-61.
41. Reed, M. L., Dove, B. K., Jackson, R. M., Collins, R., Brooks, G. & Hiscox, J. A. (2006). Delineation and modeling of a nucleolar retention signal in the coronavirus nucleocapsid protein. Traffic 7, 833-848.
42. Sriburi, R., Keelapang, P., Duangchinda, T., Pruksakorn, S., Maneekarn, N., Malasit, P. & Sittisombut N. (2001). Construction of infectious dengue 2 virus cDNA clones using high copy number plasmid. J Virol Methods 92, 71-82.
43. Tadano, M., Makino, Y., Fukunaga, T., Okuno, Y. & Fukai, K. (1989). Detection of dengue 4 virus core protein in the nucleus. I. A monoclonal antibody to dengue 4 virus reacts with the antigen in the nucleus and cytoplasm. J Gen Virol 70, 1409-1415.
44. Tao, T., Lan, J., Presley, J. F., Sweezey, N. B. & Kaplan, F. (2004). Nucleocytoplasmic shuttling of Ig12 is developmentally regulated in fetal lung. Am J Respir Cell Mol Biol 30, 350-359.
45. Uchil, P. D., Kumar, A. V. & Satchidanandam, V. (2006). Nuclear localization of flavivirus RNA synthesis in infected cells. J Virol 80, 5451-5464.
46. Wang, Y., Geer, L. Y., Chappey, C., Kans, J. A. & Bryant S. H. (2000). Cn3D: sequence and structure views for Entrez. Trends Biochem Sci 23, 300-302.
47. Wang, S. H., Syu, W.-J., Hiuang, K. J., Lei, H. Y., Yao, C. W., King, C. C. & Hu, S. T. (2002). Intracellular localization and determination of a nuclear localization signal of the core protein of dengue virus. J Gen Virol 83, 3093-3102.
48. Wang, S. H., Syu, W. J. & Hu, S. T. (2004). identification of the homotypic interaction domain of the core protein of dengue virus type 2. J Gen Virol 85, 2307-2314.
49. Westaway, E. G. (1966). Assessment and application of a cell line from pig kidney for plaque assay and neutralization tests with twelve group B aboviruses. Am J Epidemiol 84, 439-456.
50. Westaway, E. G., Khromykh, A. A., Kenney, M. T., Mackenzie, J. M. & Jones, M. K. (1997). Proteins C and NS4B of the flavivirus Kunjin translocate independently into the nucleus. Virology 234, 31-41.