BAG3, a host cochaperone, facilitates Varicella-zoster virus replication

Journal of Virology

Volumn 81, Issue 14, 2007, Pages 7491-7503

  Kyratsous, Christos A ^a   Silverstein, Saul J ^a  

^a Columbia University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANSAMYCIN DERIVATIVE; CHAPERONE; HEAT SHOCK COGNATE PROTEIN 70; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; PROTEIN BAG3; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ARTICLE; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; VARICELLA ZOSTER VIRUS; VIRUS CELL INTERACTION; VIRUS REPLICATION; VIRUS TRANSCRIPTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; BASE SEQUENCE; BENZOQUINONES; CELL LINE; CYTOPLASM; DNA PRIMERS; HERPESVIRUS 3, HUMAN; HSP70 HEAT-SHOCK PROTEINS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; HYDROLYSIS; LACTAMS, MACROCYCLIC; OPEN READING FRAMES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; VIRUS REPLICATION;

HUMAN HERPESVIRUS 3;

EID: 34447265496     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00442-07     Document Type: Article

References (81)

1. Antoku, K., R. S. Maser, W. J. Scully, Jr., S. M. Delach, and D. E. Johnson. 2001. Isolation of Bcl-2 binding proteins that exhibit homology with BAG-1 and suppressor of death domains protein. Biochem. Biophys. Res. Commun. 286:1003-1010.
2. Arvin, A. M. 1996. Varicella-zoster virus. Clin. Microbiol. Rev. 9:361-381.
3. Arvin, A. M. 1996. Varicella-zoster virus: overview and clinical manifestations. Semin. Dermatol. 15:4-7.
4. Bimston, D., J. Song, D. Winchester, S. Takayama, J. C. Reed, and R. I. Morimoto. 1998. BAG-1, a negative regulator of Hsp70 chaperone activity, uncouples nucleotide hydrolysis from substrate release. EMBO J. 17:6871-6878.
5. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
6. Brummelkamp, T. R., R. Bernards, and R. Agami. 2002. Stable suppression of tumorigenicity by virus-mediated RNA interference. Cancer Cell 2:243-247.
7. Burch, A. D., and S. K. Weller. 2005. Herpes simplex virus type 1 DNA polymerase requires the mammalian chaperone Hsp90 for proper localization to the nucleus. J. Virol. 79:10740-10749.
8. Burch, A. D., and S. K. Weller. 2004. Nuclear sequestration of cellular chaperone and proteasomal machinery during herpes simplex virus type 1 infection. J. Virol. 78:7175-7185.
9. Burkham, J., D. M. Coen, and S. K. Weller. 1998. ND10 protein PML is recruited to herpes simplex virus type 1 prereplicative sites and replication compartments in the presence of viral DNA polymerase. J. Virol. 72:10100-10107.
10. Campbell, K. S., K. P. Mullane, I. A. Aksoy, H. Stubdal, J. Zalvide, J. M. Pipas, P. A. Silver, T. M. Roberts, B. S. Schaffhausen, and J. A. DeCaprio. 1997. DnaJ/hsp40 chaperone domain of SV40 large T antigen promotes efficient viral DNA replication. Genes Dev. 11:1098-1110.
11. Cohen, J. I., T. Krogmann, L. Pesnicak, and M. A. Ali. 2007. Absence or overexpression of the varicella-zoster virus (VZV) ORF29 latency-associated protein impairs late gene expression and reduces VZV latency in a rodent model. J. Virol. 81:1586-1591.
12. Cohen, J. I., and S. E. Straus. 1996. Varicella-zoster virus and its replication, p. 2525-2545. In B. N. Fields, D. M. Knipe, and P. M. Howley (ed.), Fields virology. Lippincott-Raven Publishers, Philadelphia, PA.
13. Cohrs, R. J., M. Barbour, and D. H. Gilden. 1996. Varicella-zoster virus (VZV) transcription during latency in human ganglia: detection of transcripts mapping to genes 21, 29, 62, and 63 in a cDNA library enriched for VZV RNA. J. Virol. 70:2789-2796.
14. Cohrs, R. J., M. B. Barbour, R. Mahalingam, M. Wellish, and D. H. Gilden. 1995. Varicella-zoster virus (VZV) transcription during latency in human ganglia: prevalence of VZV gene 21 transcripts in latently infected human ganglia. J. Virol. 69:2674-2678.
15. Cohrs, R. J., D. H. Gilden, P. R. Kinchington, E. Grinfeld, and P. G. Kennedy. 2003. Varicella-zoster virus gene 66 transcription and translation in latently infected human ganglia. J. Virol. 77:6660-6665.
16. Cohrs, R. J., K. Srock, M. B. Barbour, G. Owens, R. Mahalingam, M. E. Devlin, M. Wellish, and D. H. Gilden. 1994. Varicella-zoster virus (VZV) transcription during latency in human ganglia: construction of a cDNA library from latently infected human trigeminal ganglia and detection of a VZV transcript. J. Virol. 68:7900-7908.
17. Cole, N. L., and C. Grose. 2003. Membrane fusion mediated by herpesvirus glycoproteins: the paradigm of varicella-zoster virus. Rev. Med. Virol. 13: 207-222.
18. Cory, S., D. C. Huang, and J. M. Adams. 2003. The Bcl-2 family: roles in cell survival and oncogenesis. Oncogene 22:8590-3607.
19. Croen, K. D., J. M. Ostrove, L. J. Dragovic, and S. E. Straus. 1988. Patterns of gene expression and sites of latency in human nerve ganglia are different for varicella-zoster and herpes simplex viruses. Proc. Natl. Acad. Sci. USA 85:9773-9777.
20. Dai-Ju, J. Q., L. Li, L. A. Johnson, and R. M. Sandri-Goldin. 2006. ICP27 interacts with the C-terminal domain of RNA polymerase II and facilitates its recruitment to herpes simplex virus 1 transcription sites, where it undergoes proteasomal degradation during infection. J. Virol. 80:3567-3581.
21. de Bruyn Kops, A., and D. M. Knipe. 1994. Preexisting nuclear architecture defines the intranuclear location of herpesvirus DNA replication structures. J. Virol. 68:3512-3526.
22. Doong, H., K. Rizzo, S. Fang, V. Kulpa, A. M. Weissman, and E. C. Kohn. 2003. CAIR-1/BAG-3 abrogates heat shock protein-70 chaperone complex-mediated protein degradation: accumulation of poly-ubiquitinated Hsp90 client proteins. J. Biol. Chem. 278:28490-28500.
23. Doong, H., A. Vrailas, and E. C. Kohn. 2002. What's in the 'BAG'? - A functional domain analysis of the BAG-family proteins. Cancer Lett. 188: 25-32.
24. El Karen, A., A. J. Murphy, T. Fichter, A. Efstratiadis, and S. Silverstein. 1985. "Transactivation" control signals in the promoter of the herpesvirus thymidine kinase gene. Proc. Natl. Acad. Sci. USA 82:1002-1006.
25. Ellis, R. J., and F. U. Hartl. 1996. Protein folding in the cell: competing models of chaperonin function. FASEB J. 10:20-26.
26. Everett, R. D., and G. G. Maul. 1994. HSV-1 IE protein Vmw110 causes redistribution of PML. EMBO J. 13:5062-5069.
27. Feldman, D. E., and J. Frydman. 2000. Protein folding in vivo: the importance of molecular chaperones. Curr. Opin. Struct. Biol. 10:26-33.
28. Georgopoulos, C. P., R. W. Hendrix, S. R. Casjens, and A. D. Kaiser. 1973. Host participation in bacteriophage lambda head assembly. J. Mol. Biol. 76:45-60.
29. Giraldo, R., and R. Diaz-Orejas. 2001. Similarities between the DNA replication initiators of gram-negative bacteria plasmids (RepA) and eukaryotes (Orc4p)/archaea (Cdc6p). Proc. Natl. Acad. Sci. USA 98:4938-4943.
30. Gong, D., and J. E. Ferrell, Jr. 2004. Picking a winner: new mechanistic insights into the design of effective siRNAs. Trends Biotechnol. 22:451-454.
31. Grenert, J. P., W. P. Sullivan, P. Fadden, T. A. Haystead, J. Clark, E. Mimnaugh, H. Krutzsch, H. J. Ochel, T. W. Schulte, E. Sausville, L. M. Neckers, and D. O. Toft. 1997. The amino-terminal domain of heat shock protein 90 (hsp90) that binds geldanamycin is an ATP/ADP switch domain that regulates hsp90 conformation. J. Biol. Chem. 272:23843-23850.
32. Grinfeld, E., and P. G. Kennedy. 2004. Translation of varicella-zoster virus genes during human ganglionic latency. Virus Genes 29:317-319.
33. Grose, C., and P. A. Brunel. 1978. Varicella-zoster virus: isolation and propagation in human melanoma cells at 36 and 32 degrees C. Infect. Immun. 19:199-203.
34. Hershko, A., and A. Ciechanover. 1998. The ubiquitin system. Annu. Rev. Biochem. 67:425-479.
35. Hohfeld, J., and S. Jentsch. 1997. GrpE-like regulation of the hsc70 chaperone by the anti-apoptotic protein BAG-1. EMBO J. 16:6209-6216.
36. Jagla, B., N. Aulner, P. D. Kelly, D. Song, A. Volchuk, A. Zatorski, D. Shum, T. Mayer, D. A. De Angelis, O. Ouerfelli, U. Rutishauser, and J. E. Rothman. 2005. Sequence characteristics of functional siRNAs. RNA 11:864-872.
37. Kennedy, P. G., E. Grinfeld, and J. E. Bell. 2000. Varicella-zoster virus gene expression in latently infected and explanted human ganglia. J. Virol. 74: 11893-11898.
38. Kinchington, P. R., K. Fite, and S. E. Turse. 2000. Nuclear accumulation of 1E62, the varicella-zoster virus (VZV) major transcriptional regulatory protein, is inhibited by phosphorylation mediated by the VZV open reading frame 66 protein kinase. J. Virol. 74:2265-2277.
39. Kinchington, P. R., G. Inchauspe, J. H. Subak-Sharpe, F. Robey, J. Hay, and W. T. Ruyechan. 1988. Identification and characterization of a varicella-zoster virus DNA-binding protein by using antisera directed against a predicted synthetic oligopeptide. J. Virol. 62:802-809.
40. Knipe, D. M., D. Senechek, S. A. Rice, and J. L. Smith. 1987. Stages in the nuclear association of the herpes simplex virus transcriptional activator protein ICP4. J. Virol. 61:276-284.
41. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
42. Lee, J. H., T. Takahashi, N. Yasuhara, J. Inazawa, S. Kamada, and Y. Tsujimoto. 1999. Bis, a Bcl-2-binding protein that synergizes with Bcl-2 in preventing cell death. Oncogene 18:6183-6190.
43. Li, Y. H., P. Z. Tao, Y. Z. Liu, and J. D. Jiang. 2004. Geldanamycin, a ligand of heat shock protein 90, inhibits the replication of herpes simplex virus type 1 in vitro. Antimicrob. Agents Chemother. 48:867-872.
44. Liberek, K., C. Georgopoulos, and M. Zylicz. 1988. Role of the Escherichia coli DnaK and DnaJ heat shock proteins in the initiation of bacteriophage lambda DNA replication. Proc. Natl. Acad. Sci. USA 85:6632-6636.
45. Liberek, K., J. Marszalek, D. Ang, C. Georgopoulos, and M. Zylicz. 1991. Escherichia coli DnaJ and GrpE heat shock proteins jointly stimulate ATPase activity of DnaK. Proc. Natl. Acad. Sci. USA 88:2874-2878.
46. Liu, J. S., S. R. Kuo, A. M. Makhov, D. M. Cyr, J. D. Griffith, T. R. Broker, and L. T. Chow. 1998. Human Hsp70 and Hsp40 chaperone proteins facilitate human papillomavirus-11 E1 protein binding to the origin and stimulate cell-free DNA replication. J. Biol. Chem. 273:30704-30712.
47. Lium, E. K., C. A. Panagiotidis, X. Wen, and S. Silverstein. 1996. Repression of the alpha0 gene by ICP4 during a productive herpes simplex virus infection. J. Virol. 70:3488-3496.
48. Lungu, O., P. W. Annunziato, A. Gershon, S. M. Staugaitis, D. Josefson, P. LaRussa, and S. J. Silverstein. 1995. Reactivated and latent varicella-zoster virus in human dorsal root ganglia. Proc. Natl. Acad. Sci. USA 92:10980-10984.
49. Lungu, O., C. A. Panagiotidis, P. W. Annunziato, A. A. Gershon, and S. J. Silverstein. 1998. Aberrant intracellular localization of varicella-zoster virus regulatory proteins during latency. Proc. Natl. Acad. Sci. USA 95:7080-7085.
50. Macgregor, P. F., C. Abate, and T. Curran. 1990. Direct cloning of leucine zipper proteins: Jun binds cooperatively to the CRE with CRE-BP1. Oncogene 5:451-458.
51. Margolis, B., and R. Young. 1994. Screening lambda expression libraries with antibody and protein probed, p. 1-14. In D. M. Glover and B. D. Hames (ed.), DNA cloning: a practical approach, 2nd ed. IRL Press, Oxford University Press, Oxford, United Kingdom.
52. Markowitz, D., S. Goff, and A. Bank. 1988. A safe packaging line for gene transfer: separating viral genes on two different plasmids. J. Virol. 62:1120-1124.
53. McClellan, A. J., and J. Frydman. 2001. Molecular chaperones and the art of recognizing a lost cause. Nat. Cell Biol. 3:E51-E53.
54. McClellan, A. J., S. Tam, D. Kaganovich, and J. Frydman. 2005. Protein quality control: chaperones culling corrupt conformations. Nat. Cell Biol. 7:736-741.
55. McKnight, S. L., and R. Kingsbury. 1982. Transcriptional control signals of a eukaryotic protein-coding gene. Science 217:316-324.
56. Meier, J. L., R. P. Holman, K. D. Croen, J. E. Smialek, and S. E. Straus. 1993. Varicella-zoster virus transcription in human trigeminal ganglia. Virology 193:193-200.
57. Neckers, L., and K. Neckers. 2005. Heat-shock protein 90 inhibitors as novel cancer chemotherapeutics - an update. Expert. Opin. Emerg. Drugs 10:137-149.
58. Neckers, L., T. W. Schulte, and E. Mimnaugh. 1999. Geldanamycin as a potential anti-cancer agent: its molecular target and biochemical activity. Investig. New Drugs 17:361-373.
59. Ng, P., D. T. Cummings, C. M. Evelegh, and F. L. Graham. 2000. Yeast recombinase FLP functions effectively in human cells for construction of adenovirus vectors. BioTechniques 29:524-526, 528.
60. Nishioka, Y., and S. Silverstein. 1977. Degradation of cellular mRNA during infection by herpes simplex virus. Proc. Natl. Acad. Sci. USA 74:2370-2374.
61. Panagiotidis, C. A., and S. J. Silverstein. 1995. pALEX, a dual-tag prokaryotic expression vector for the purification of full-length proteins. Gene 164:45-47.
62. Prodromou, C., S. M. Roe, R. O'Brien, J. E. Ladbury, P. W. Piper, and L. H. Pearl. 1997. Identification and structural characterization of the ATP/ADP-binding site in the Hsp90 molecular chaperone. Cell 90:65-75.
63. Quinlan, M. P., L. B. Chen, and D. M. Knipe. 1984. The intranuclear location of a herpes simplex virus DNA-binding protein is determined by the status of viral DNA replication. Cell 36:857-868.
64. Reynolds, A., D. Leake, Q. Boese, S. Scaringe, W. S. Marshall, and A. Khvorova. 2004. Rational siRNA design for RNA interference. Nat. Biotechnol. 22:326-330.
65. Schneider, C., L. Sepp-Lorenzino, E. Nimmesgern, O. Ouerfelli, S. Danishefsky, N. Rosen, and F. U. Hartl. 1996. Pharmacologic shifting of a balance between protein refolding and degradation mediated by Hsp90. Proc. Natl. Acad. Sci. USA 93:14536-14541.
66. Short, J. M., J. M. Fernandez, J. A. Sorge, and W. D. Huse. 1988. Lambda ZAP: a bacteriophage lambda expression vector with in vivo excision properties. Nucleic Acids Res. 16:7583-7600.
67. Skolnik, E. Y., B. Margolis, M. Mohammadi, E. Lowenstein, R. Fischer, A. Drepps, A. Ullrich, and J. Schlessinger. 1991. Cloning of PI3 kinase-associated p85 utilizing a novel method for expression/cloning of target proteins for receptor tyrosine kinases. Cell 65:83-90.
68. Smith, D. B., and K. S. Johnson. 1988. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene 67:31-40.
69. Sondermann, H., C. Scbeufler, C. Schneider, J. Hohfeld, F. U. Hartl, and I. Moarefi. 2001. Structure of a Bag/Hsc70 complex: convergent functional evolution of Hsp70 nucleotide exchange factors. Science 291:1553-1557.
70. Stallings, C. L., G. J. Duigou, A. A. Gershon, M. D. Gershon, and S. J. Silverstein. 2006. The cellular localization pattern of varicella-zoster virus ORF29p is influenced by proteasome-mediated degradation. J. Virol. 80: 1497-1512.
71. Stallings, C. L., and S. Silverstein. 2005. Dissection of a novel nuclear localization signal in open reading frame 29 of varicella-zoster virus. J. Virol. 79:13070-13081.
72. Straus, S. E., H. S. Aulakh, W. T. Ruyechan, J. Hay, T. A. Casey, G. F. Vande Woude, J. Owens, and H. A. Smith. 1981. Structure of varicella-zoster virus DNA. J. Virol. 40:516-525.
73. Sullivan, W., B. Stensgard, G. Caucutt, B. Bartha, N. McMahon, E. S. Alnemri, G. Litwack, and D. Toft. 1997. Nucleotides and two functional states of hsp90. J. Biol. Chem. 272:8007-8012.
74. Takayama, S., D. N. Bimston, S. Matsuzawa, B. C. Freeman, C. Aime-Sempe, Z. Xie, R. I. Morimoto, and J. C. Reed. 1997. BAG-1 modulates the chaperone activity of Hsp70/Hsc70. EMBO J. 16:4887-4896.
75. Takayama, S., and J. C. Reed. 2001. Molecular chaperone targeting and regulation by BAG family proteins. Nat. Cell Biol. 3:E237-E241.
76. Takayama, S., Z. Xie, and J. C. Reed. 1999. An evolutionarily conserved family of Hsp70/Hsc70 molecular chaperone regulators. J. Biol. Chem. 274:781-786.
77. Tzanck, A. 1947. Le cytodiagnostic immediat en dermatologie. Bull. Soc. Fr. Dermatol. Symp. 7:68.
78. Whitesell, L., E. G. Mimnaugh, B. De Costa, C. E. Myers, and L. M. Neckers. 1994. Inhibition of heat shock protein HSP90-pp60v-src heteroprotein complex formation by benzoquinone ansamycins: essential role for stress proteins in oncogenic transformation. Proc. Natl. Acad. Sci. USA 91:8324-8328.
79. Yee, J. K., A. Miyanohara, P. LaPorte, K. Bouic, J. C. Burns, and T. Friedmann. 1994. A general method for the generation of high-titer, pantropic retroviral vectors: highly efficient infection of primary hepatocytes. Proc. Natl. Acad. Sci. USA 91:9564-9568.
80. Yochem, J., H. Uchida, M. Sunshine, H. Saito, C. P. Georgopoulos, and M. Feiss. 1978. Genetic analysis of two genes, dnaJ and dnaK, necessary for Escherichia coli and bacteriophage lambda DNA replication. Mol. Gen. Genet. 164:9-14.
81. Zylicz, M., D. Ang, K. Liberek, and C. Georgopoulos. 1989. Initiation of lambda DNA replication with purified host- and bacteriophage-encoded proteins: the role of the dnaK, dnaJ and grpE heat shock proteins. EMBO J. 8:1601-1608.