The polyomavirus BK agnoprotein co-localizes with lipid droplets

Virology

Volumn 399, Issue 2, 2010, Pages 322-331

  Unterstab, Gunhild ^a   Gosert, Rainer ^a   Leuenberger, David ^a   Lorentz, Pascal ^b   Rinaldo, Christine H ^c   Hirsch, Hans H ^a,d  

^a UNIVERSITY OF BASEL   (Switzerland)

^b UNIVERSITY OF BASEL   (Switzerland)

^c UNIVERSITY HOSPITAL OF NORTH NORWAY   (Norway)

^d UNIVERSITY HOSPITAL BASEL   (Switzerland)

Author keywords

Accessory protein; Agnoprotein; BK virus; CLSM; Deconvolution; Infection; Lipid droplets; Polyomavirus; Transfection

Indexed keywords

AGNOPROTEIN; ALANINE; ASPARTIC ACID; ENHANCED GREEN FLUORESCENT PROTEIN; FAT DROPLET; SERINE;

ARTICLE; BK VIRUS; CELL STRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GENE MUTATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HYDROPHOBICITY; IN VITRO STUDY; KIDNEY TUBULE EPITHELIUM; PRIORITY JOURNAL; PROTEIN DENATURATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; VERO CELL; VIRUS CORE; VIRUS REPLICATION;

AMINO ACID SEQUENCE; ANIMALS; BK VIRUS; CELL NUCLEUS; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; CYTOPLASM; HUMANS; LIPIDS; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; MUTATION; PHOSPHORYLATION; PROTEIN STRUCTURE, SECONDARY; VERO CELLS; VIRAL REGULATORY AND ACCESSORY PROTEINS;

BK POLYOMAVIRUS; POLYOMAVIRUS; UTA;

EID: 77249139943     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2010.01.011     Document Type: Article

References (48)

1. Barba G., Harper F., Harada T., Kohara M., Goulinet S., Matsuura Y., Eder G., Schaff Z., Chapman M.J., Miyamura T., and Brechot C. Hepatitis C virus core protein shows a cytoplasmic localization and associates to cellular lipid storage droplets. Proc. Natl. Acad. Sci. U.S.A. 94 4 (1997) 1200-1205
2. Brasaemle D.L., and Wolins N.E. Isolation of lipid droplets from cells by density gradient centrifugation. Curr. Protoc. Cell Biol. (2006) Chapter 3, Unit 3 15
3. Brasaemle D.L., Dolios G., Shapiro L., and Wang R. Proteomic analysis of proteins associated with lipid droplets of basal and lipolytically stimulated 3T3-L1 adipocytes. J. Biol. Chem. 279 45 (2004) 46835-46842
4. Chesters P.M., Heritage J., and McCance D.J. Persistence of DNA sequences of BK virus and JC virus in normal human tissues and in diseased tissues. J. Infect. Dis. 147 4 (1983) 676-684
5. Darbinyan A., Siddiqui K.M., Slonina D., Darbinian N., Amini S., White M.K., and Khalili K. Role of JC virus agnoprotein in DNA repair. J. Virol. 78 16 (2004) 8593-8600
6. De Clercq E. Antivirals and antiviral strategies. Nat. Rev. Microbiol. 2 9 (2004) 704-720
7. Dorries K., and ter Meulen V. Progressive multifocal leucoencephalopathy: detection of papovavirus JC in kidney tissue. J. Med. Virol. 11 4 (1983) 307-317
8. Dropulic L.K., and Jones R.J. Polyomavirus BK infection in blood and marrow transplant recipients. Bone Marrow Transplant. 41 1 (2008) 11-18
9. Egli A., Infanti L., Dumoulin A., Buser A., Samaridis J., Stebler C., Gosert R., and Hirsch H.H. Prevalence of Polyomavirus BK and JC Infection and Replication in 400 Healthy Blood Donors. J. Infect. Dis. 199 (2009) 837-846
10. Englert C., Hou X., Maheswaran S., Bennett P., Ngwu C., Re G.G., Garvin A.J., Rosner M.R., and Haber D.A. WT1 suppresses synthesis of the epidermal growth factor receptor and induces apoptosis. EMBO J. 14 19 (1995) 4662-4675
11. Gardner S.D., Field A.M., Coleman D.V., and Hulme B. New human papovavirus (B.K.) isolated from urine after renal transplantation. Lancet 1 7712 (1971) 1253-1257
12. Gosert R., Rinaldo C.H., Funk G.A., Egli A., Ramos E., Drachenberg C.B., and Hirsch H.H. Polyomavirus BK with rearranged noncoding control region emerge in vivo in renal transplant patients and increase viral replication and cytopathology. J. Exp. Med. 205 4 (2008) 841-852
13. Grinde B., Gayorfar M., and Rinaldo C.H. Impact of a polyomavirus (BKV) infection on mRNA expression in human endothelial cells. Virus Res. 123 1 (2007) 86-94
14. Guo Y., Walther T.C., Rao M., Stuurman N., Goshima G., Terayama K., Wong J.S., Vale R.D., Walter P., and Farese R.V. Functional genomic screen reveals genes involved in lipid-droplet formation and utilization. Nature 453 7195 (2008) 657-661
15. Hope R.G., and McLauchlan J. Sequence motifs required for lipid droplet association and protein stability are unique to the hepatitis C virus core protein. J. Gen. Virol. 81 Pt. 8 (2000) 1913-1925
16. Hope R.G., Murphy D.J., and McLauchlan J. The domains required to direct core proteins of hepatitis C virus and GB virus-B to lipid droplets share common features with plant oleosin proteins. J. Biol. Chem. 277 6 (2002) 4261-4270
17. Ishola Jr. D.A., Post J.A., van Timmeren M.M., Bakker S.J., Goldschmeding R., Koomans H.A., Braam B., and Joles J.A. Albumin-bound fatty acids induce mitochondrial oxidant stress and impair antioxidant responses in proximal tubular cells. Kidney Int. 70 4 (2006) 724-731
18. Jay G., Nomura S., Anderson C.W., and Khoury G. Identification of the SV40 agnogene product: a DNA binding protein. Nature 291 5813 (1981) 346-349
19. Jiang M., Abend J.R., Johnson S.F., and Imperiale M.J. The role of polyomaviruses in human disease. Virology 384 2 (2009) 266-273
20. Johannessen M., Myhre M.R., Dragset M., Tummler C., and Moens U. Phosphorylation of human polyomavirus BK agnoprotein at Ser-11 is mediated by PKC and has an important regulative function. Virology 379 1 (2008) 97-109
21. Khanna N., Elzi L., Mueller N.J., Garzoni C., Cavassini M., Fux C.A., Vernazza P., Bernasconi E., Battegay M., Hirsch H.H., and for the Swiss HIV Cohort Study. Incidence and outcome of progressive multifocal leukoencephalopathy in 20 years of the Swiss HIV Cohort Study. Clin. Infect. Dis. 48 (2009) 1459-1466
22. Khemici V., Poljak L., Luisi B.F., and Carpousis A.J. The RNase E of Escherichia coli is a membrane-binding protein. Mol. Microbiol. 70 4 (2008) 799-813
23. Knowles W.A., Pipkin P., Andrews N., Vyse A., Minor P., Brown D.W., and Miller E. Population-based study of antibody to the human polyomaviruses BKV and JCV and the simian polyomavirus SV40. J. Med. Virol. 71 1 (2003) 115-123
24. Kumar Y., Cocchiaro J., and Valdivia R.H. The obligate intracellular pathogen Chlamydia trachomatis targets host lipid droplets. Curr. Biol. 16 16 (2006) 1646-1651
25. Leuenberger D., Andresen P.A., Gosert R., Binggeli S., Strom E.H., Bodaghi S., Rinaldo C.H., and Hirsch H.H. Human polyomavirus type 1 (BK virus) agnoprotein is abundantly expressed but immunologically ignored. Clin. Vaccine Immunol. 14 8 (2007) 959-968
26. Linstedt A.D., and Hauri H.P. Giantin, a novel conserved Golgi membrane protein containing a cytoplasmic domain of at least 350 kDa. Mol. Biol. Cell 4 7 (1993) 679-693
27. Liu P., Bartz R., Zehmer J.K., Ying Y.S., Zhu M., Serrero G., and Anderson R.G. Rab-regulated interaction of early endosomes with lipid droplets. Biochim. Biophys. Acta 1773 6 (2007) 784-793
28. Miyanari Y., Atsuzawa K., Usuda N., Watashi K., Hishiki T., Zayas M., Bartenschlager R., Wakita T., Hijikata M., and Shimotohno K. The lipid droplet is an important organelle for hepatitis C virus production. Nat. Cell Biol. 9 9 (2007) 1089-1097
29. Moriyama T., and Sorokin A. Repression of BK virus infection of human renal proximal tubular epithelial cells by pravastatin. Transplantation 85 9 (2008) 1311-1317
30. Myhre M.R., Olsen G.H., Gosert R., Hirsch H.H., and Rinaldo C.H. Clinical polyomavirus BK variants with agnogene deletion are non-functional but rescued by trans-complementation. Virology (2010) (Electronic publication ahead of print)
31. Nast C.C., and Cohen A.H. Renal cholesterol granulomas: identification and morphological pattern of development. Histopathology 9 11 (1985) 1195-1204
32. Ostermeyer A.G., Ramcharan L.T., Zeng Y., Lublin D.M., and Brown D.A. Role of the hydrophobic domain in targeting caveolin-1 to lipid droplets. J. Cell Biol. 164 1 (2004) 69-78
33. Padgett B.L., Walker D.L., ZuRhein G.M., Eckroade R.J., and Dessel B.H. Cultivation of papova-like virus from human brain with progressive multifocal leucoencephalopathy. Lancet 1 7712 (1971) 1257-1260
34. Ramos E., Drachenberg C.B., Wali R., and Hirsch H.H. The decade of polyomavirus BK-associated nephropathy: state of affairs. Transplantation 87 5 (2009) 621-630
35. Rinaldo C.H., and Hirsch H.H. Antivirals for the treatment of polyomavirus BK replication. Expert Rev. Anti. Infect. Ther. 5 1 (2007) 105-115
36. Rinaldo C.H., Traavik T., and Hey A. The agnogene of the human polyomavirus BK is expressed. J. Virol. 72 7 (1998) 6233-6236
37. Rust R.C., Landmann L., Gosert R., Tang B.L., Hong W., Hauri H.P., Egger D., and Bienz K. Cellular COPII proteins are involved in production of the vesicles that form the poliovirus replication complex. J. Virol. 75 20 (2001) 9808-9818
38. Safak M., Barrucco R., Darbinyan A., Okada Y., Nagashima K., and Khalili K. Interaction of JC virus agno protein with T antigen modulates transcription and replication of the viral genome in glial cells. J. Virol. 75 3 (2001) 1476-1486
39. Schweizer A., Fransen J.A., Bachi T., Ginsel L., and Hauri H.P. Identification, by a monoclonal antibody, of a 53-kD protein associated with a tubulo-vesicular compartment at the cis-side of the Golgi apparatus. J. Cell Biol. 107 5 (1988) 1643-1653
40. Schweizer A., Ericsson M., Bachi T., Griffiths G., and Hauri H.P. Characterization of a novel 63 kDa membrane protein. Implications for the organization of the ER-to-Golgi pathway. J. Cell Sci. 104 (1993) 671-683
41. Shishido-Hara Y., Ichinose S., Higuchi K., Hara Y., and Yasui K. Major and minor capsid proteins of human polyomavirus JC cooperatively accumulate to nuclear domain 10 for assembly into virions. J. Virol. 78 18 (2004) 9890-9903
42. Subramanian V., Garcia A., Sekowski A., and Brasaemle D.L. Hydrophobic sequences target and anchor perilipin A to lipid droplets. J. Lipid Res. 45 11 (2004) 1983-1991
43. Suzuki T., Okada Y., Semba S., Orba Y., Yamanouchi S., Endo S., Tanaka S., Fujita T., Kuroda S., Nagashima K., and Sawa H. Identification of FEZ1 as a protein that interacts with JC virus agnoprotein and microtubules: role of agnoprotein-induced dissociation of FEZ1 from microtubules in viral propagation. J. Biol. Chem. 280 26 (2005) 24948-24956
44. Urahama Y., Ohsaki Y., Fujita Y., Maruyama S., Yuzawa Y., Matsuo S., and Fujimoto T. Lipid droplet-associated proteins protect renal tubular cells from fatty acid-induced apoptosis. Am. J. Pathol. 173 5 (2008) 1286-1294
45. van Kuppeveld F.J., Hoenderop J.G., Smeets R.L., Willems P.H., Dijkman H.B., Galama J.M., and Melchers W.J. Coxsackievirus protein 2B modifies endoplasmic reticulum membrane and plasma membrane permeability and facilitates virus release. EMBO J. 16 12 (1997) 3519-3532
46. Welte M.A. Proteins under new management: lipid droplets deliver. Trends Cell Biol. 17 8 (2007) 363-369
47. White M.K., and Khalili K. Expression of JC virus regulatory proteins in human cancer: potential mechanisms for tumourigenesis. Eur. J. Cancer 41 16 (2005) 2537-2548
48. Zehmer J.K., Huang Y., Peng G., Pu J., Anderson R.G., and Liu P. A role for lipid droplets in inter-membrane lipid traffic. Proteomics 9 4 (2009) 914-921