Inhibition of Simian Virus 40 replication by targeting the molecular chaperone function and ATPase activity of T antigen

Virus Research

Volumn 141, Issue 1, 2009, Pages 71-80

  Wright, Christine M ^a   Seguin, Sandlin P ^a   Fewell, Sheara W ^a   Zhang, Haijiang ^b   Ishwad, Chandra ^d   Vats, Abhay ^d   Lingwood, Clifford A ^e   Wipf, Peter ^a   Fanning, Ellen ^b,c   Pipas, James M ^a   Brodsky, Jeffrey L ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b VANDERBILT UNIVERSITY   (United States)

^c VANDERBILT INGRAM CANCER CENTER   (United States)

^d CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^e UNIVERSITY OF TORONTO   (Canada)

Author keywords

BK virus; Dihydropyrimidine; Heat shock protein; Hsp70; J domain; SV40

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CHAPERONE; HEAT SHOCK PROTEIN 70; MAL2 11B; PROTEIN INHIBITOR; PROTEIN TAG; UNCLASSIFIED DRUG; VIRUS T ANTIGEN;

ANIMAL CELL; ARTICLE; CELL CULTURE; CONTROLLED STUDY; DNA REPLICATION; IN VITRO STUDY; KIDNEY CELL; MOLECULAR LIBRARY; NONHUMAN; PRIORITY JOURNAL; SIMIAN VIRUS 40; VIRUS CULTURE; VIRUS LOAD; VIRUS REPLICATION;

ADENOSINE TRIPHOSPHATASES; ANTIGENS, VIRAL, TUMOR; CELL LINE; DOWN-REGULATION; HSP70 HEAT-SHOCK PROTEINS; HUMANS; SIMIAN VIRUS 40; SMALL MOLECULE LIBRARIES; VIRAL PROTEINS; VIRUS REPLICATION;

BK POLYOMAVIRUS; JC POLYOMAVIRUS; POLYOMAVIRUS; SIMIAN VIRUS 40;

EID: 61449200234     PISSN: 01681702     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.virusres.2008.12.018     Document Type: Article

References (82)

1. Ahuja D., Saenz-Robles M.T., and Pipas J.M. SV40 large T antigen targets multiple cellular pathways to elicit cellular transformation. Oncogene 24 52 (2005) 7729-7745
2. Ali S.H., Chandraker A., and DeCaprio J.A. Inhibition of Simian virus 40 large T antigen helicase activity by fluoroquinolones. Antivir. Ther. 12 1 (2007) 1-6
3. Ali S.H., and DeCaprio J.A. Cellular transformation by SV40 large T antigen: interaction with host proteins. Semin. Cancer Biol. 11 1 (2001) 15-23
4. Allander T., Andreasson K., Gupta S., Bjerkner A., Bogdanovic G., Persson M.A., Dalianis T., Ramqvist T., and Andersson B. Identification of a third human polyomavirus. J. Virol. 81 8 (2007) 4130-4136
5. Andrei G., Snoeck R., Vandeputte M., and De Clercq E. Activities of various compounds against murine and primate polyomaviruses. Antimicrob. Agents Chemother. 41 3 (1997) 587-593
6. Arunkumar A.I., Klimovich V., Jiang X., Ott R.D., Mizoue L., Fanning E., and Chazin W.J. Insights into hRPA32 C-terminal domain-mediated assembly of the simian virus 40 replisome. Nat. Struct. Mol. Biol. 12 4 (2005) 332-339
7. Barbanti-Brodano G., Martini F., De Mattei M., Lazzarin L., Corallini A., and Tognon M. BK and JC human polyomaviruses and simian virus 40: natural history of infection in humans, experimental oncogenicity, and association with human tumors. Adv. Virus Res. 50 (1998) 69-99
8. Beck J., and Nassal M. Efficient Hsp90-independent in vitro activation by Hsc70 and Hsp40 of duck hepatitis B virus reverse transcriptase, an assumed Hsp90 client protein. J. Biol. Chem. 278 38 (2003) 36128-36138
9. Becker J., Walter W., Yan W., and Craig E.A. Functional interaction of cytosolic hsp70 and a DnaJ-related protein, Ydj1p, in protein translocation in vivo. Mol. Cell. Biol. 16 8 (1996) 4378-4386
10. Bista B.R., Ishwad C., Wadowsky R.M., Manna P., Randhawa P.S., Gupta G., Adhikari M., Tyagi R., Gasper G., and Vats A. Development of a loop-mediated isothermal amplification assay for rapid detection of BK virus. J. Clin. Microbiol. 45 5 (2007) 1581-1587
11. Borowiec J.A., and Hurwitz J. Localized melting and structural changes in the SV40 origin of replication induced by T-antigen. EMBO J. 7 10 (1988) 3149-3158
12. Brodsky J.L., and Pipas J.M. Polyomavirus T antigens: molecular chaperones for multiprotein complexes. J. Virol. 72 7 (1998) 5329-5334
13. Campbell K.S., Mullane K.P., Aksoy I.A., Stubdal H., Zalvide J., Pipas J.M., Silver P.A., Roberts T.M., Schaffhausen B.S., and DeCaprio J.A. DnaJ/hsp40 chaperone domain of SV40 large T antigen promotes efficient viral DNA replication. Genes Dev. 11 9 (1997) 1098-1110
14. Cantalupo P., Doering A., Sullivan C.S., Pal A., Peden K.W., Lewis A.M., and Pipas J.M. Complete nucleotide sequence of polyomavirus SA12. J. Virol. 79 20 (2005) 13094-13104
15. Cantalupo P., Saenz-Robles M.T., and Pipas J.M. Expression of SV40 large T antigen in baculovirus systems and purification by immunoaffinity chromatography. Methods Enzymol. 306 (1999) 297-307
16. Carbone M., Rudzinski J., and Bocchetta M. High throughput testing of the SV40 Large T antigen binding to cellular p53 identifies putative drugs for the treatment of SV40-related cancers. Virology 315 2 (2003) 409-414
17. Castellino A.M., Cantalupo P., Marks I.M., Vartikar J.V., Peden K.W., and Pipas J.M. trans-Dominant and non-trans-dominant mutant simian virus 40 large T antigens show distinct responses to ATP. J. Virol. 71 10 (1997) 7549-7559
18. Chromy L.R., Oltman A., Estes P.A., and Garcea R.L. Chaperone-mediated in vitro disassembly of polyoma- and papillomaviruses. J. Virol. 80 10 (2006) 5086-5091
19. Clark R., Peden K., Pipas J.M., Nathans D., and Tjian R. Biochemical activities of T-antigen proteins encoded by simian virus 40 A gene deletion mutants. Mol. Cell. Biol. 3 2 (1983) 220-228
20. Cole C.N., Tornow J., Clark R., and Tjian R. Properties of the simian virus 40 (SV40) large T antigens encoded by SV40 mutants with deletions in gene A. J. Virol. 57 2 (1986) 539-546
21. Collins B.S., and Pipas J.M. T antigens encoded by replication-defective simian virus 40 mutants dl1135 and 5080. J. Biol. Chem. 270 25 (1995) 15377-15384
22. Cory A.H., Owen T.C., Barltrop J.A., and Cory J.G. Use of an aqueous soluble tetrazolium/formazan assay for cell growth assays in culture. Cancer Commun. 3 7 (1991) 207-212
23. Craig E.A., Huang P., Aron R., and Andrew A. The diverse roles of J-proteins, the obligate Hsp70 co-chaperone. Rev. Physiol. Biochem. Pharmacol. 156 (2006) 1-21
24. Cripe T.P., Delos S.E., Estes P.A., and Garcea R.L. In vivo and in vitro association of hsc70 with polyomavirus capsid proteins. J. Virol. 69 12 (1995) 7807-7813
25. Cyr D.M., Lu X., and Douglas M.G. Regulation of Hsp70 function by a eukaryotic DnaJ homolog. J. Biol. Chem. 267 29 (1992) 20927-20931
26. De Clercq E., and Holy A. Case History: Acyclic nucleoside phosphonates: a key class of antiviral drugs. Nat. Rev. Drug Discov. 4 11 (2005) 928-940
27. Eash S., Manley K., Gasparovic M., Querbes W., and Atwood W.J. The human polyomaviruses. Cell. Mol. Life Sci. 63 7-8 (2006) 865-876
28. Farasati N.A., Shapiro R., Vats A., and Randhawa P. Effect of leflunomide and cidofovir on replication of BK virus in an in vitro culture system. Transplantation 79 1 (2005) 116-118
29. Farber J.M., Peden K.W., and Nathans D. trans-Dominant defective mutants of simian virus 40 T antigen. J. Virol. 61 2 (1987) 436-445
30. Fendrick J.L., and Hallick L.M. Optimal conditions for titration of SV40 by the plaque assay method. J. Virol. Methods 7 2 (1983) 93-102
31. Feng H., Shuda M., Chang Y., and Moore P.S. Clonal integration of a polyomavirus in human merkel cell carcinoma. Science 319 (2008) 1096-1100
32. Fewell S.W., Pipas J.M., and Brodsky J.L. Mutagenesis of a functional chimeric gene in yeast identifies mutations in the simian virus 40 large T antigen J domain. Proc. Natl. Acad. Sci. USA 99 4 (2002) 2002-2007
33. Fewell S.W., Smith C.M., Lyon M.A., Dumitrescu T.P., Wipf P., Day B.W., and Brodsky J.L. Small molecule modulators of endogenous and co-chaperone-stimulated Hsp70 ATPase activity. J. Biol. Chem. 279 49 (2004) 51131-51140
34. Gassler C.S., Buchberger A., Laufen T., Mayer M.P., Schroder H., Valencia A., and Bukau B. Mutations in the DnaK chaperone affecting interaction with the DnaJ cochaperone. Proc. Natl. Acad. Sci. USA 95 26 (1998) 15229-15234
35. Gaynor A.M., Nissen M.D., Whiley D.M., Mackay I.M., Lambert S.B., Wu G., Brennan D.C., Storch G.A., Sloots T.P., and Wang D. Identification of a novel polyomavirus from patients with acute respiratory tract infections. PLoS Pathog. 3 5 (2007) 595-604
36. Glotzer J.B., Saltik M., Chiocca S., Michou A.I., Moseley P., and Cotten M. Activation of heat-shock response by an adenovirus is essential for virus replication. Nature 407 6801 (2000) 207-211
37. Gluzman Y., and Ahrens B. SV40 early mutants that are defective for viral DNA synthesis but competent for transformation of cultured rat and simian cells. Virology 123 1 (1982) 78-92
38. Goeckeler J.L., Stephens A., Lee P., Caplan A.J., and Brodsky J.L. Overexpression of yeast Hsp110 homolog Sse1p suppresses ydj1-151 thermosensitivity and restores Hsp90-dependent activity. Mol. Biol. Cell. 13 8 (2002) 2760-2770
39. Gorczynska E., Turkiewicz D., Rybka K., Toporski J., Kalwak K., Dyla A., Szczyra Z., and Chybicka A. Incidence, clinical outcome, and management of virus-induced hemorrhagic cystitis in children and adolescents after allogeneic hematopoietic cell transplantation. Biol. Blood Marrow Transplant. 11 10 (2005) 797-804
40. Harlow E., Crawford L.V., Pim D.C., and Williamson N.M. Monoclonal antibodies specific for simian virus 40 tumor antigens. J. Virol. 39 3 (1981) 861-869
41. Hennessy F., Nicoll W.S., Zimmermann R., Cheetham M.E., and Blatch G.L. Not all J domains are created equal: implications for the specificity of Hsp40-Hsp70 interactions. Protein Sci. 14 7 (2005) 1697-1709
42. Hymes L.C., and Warshaw B.L. Polyomavirus (BK) in pediatric renal transplants: evaluation of viremic patients with and without BK associated nephritis. Pediatr. Transplant. 10 8 (2006) 920-922
43. Jiang X., Klimovich V., Arunkumar A.I., Hysinger E.B., Wang Y., Ott R.D., Guler G.D., Weiner B., Chazin W.J., and Fanning E. Structural mechanism of RPA loading on DNA during activation of a simple pre-replication complex. EMBO J. 25 23 (2006) 5516-5526
44. Kim H.Y., Ahn B.Y., and Cho Y. Structural basis for the inactivation of retinoblastoma tumor suppressor by SV40 large T antigen. EMBO J. 20 1-2 (2001) 295-304
45. Li D., Zhao R., Lilyestrom W., Gai D., Zhang R., DeCaprio J.A., Fanning E., Jochimiak A., Szakonyi G., and Chen X.S. Structure of the replicative helicase of the oncoprotein SV40 large tumour antigen. Nature 423 6939 (2003) 512-518
46. Li J.J., Peden K.W., Dixon R.A., and Kelly T. Functional organization of the simian virus 40 origin of DNA replication. Mol. Cell. Biol. 6 4 (1986) 1117-1128
47. Lin B.Y., Makhov A.M., Griffith J.D., Broker T.R., and Chow L.T. Chaperone proteins abrogate inhibition of the human papillomavirus (HPV) E1 replicative helicase by the HPV E2 protein. Mol. Cell. Biol. 22 18 (2002) 6592-6604
48. Maga G., Stucki M., Spadari S., and Hubscher U. DNA polymerase switching: I. Replication factor C displaces DNA polymerase alpha prior to PCNA loading. J. Mol. Biol. 295 4 (2000) 791-801
49. Mastrangelo I.A., Hough P.V., Wall J.S., Dodson M., Dean F.B., and Hurwitz J. ATP-dependent assembly of double hexamers of SV40 T antigen at the viral origin of DNA replication. Nature 338 6217 (1989) 658-662
50. Matsumoto T., Eki T., and Hurwitz J. Studies on the initiation and elongation reactions in the simian virus 40 DNA replication system. Proc. Natl. Acad. Sci. USA 87 24 (1990) 9712-9716
51. Mayer M.P. Recruitment of Hsp70 chaperones: a crucial part of viral survival strategies. Rev. Physiol. Biochem. Pharmacol. 153 (2005) 1-46
52. McClellan A.J., and Brodsky J.L. Mutation of the ATP-binding pocket of SSA1 indicates that a functional interaction between Ssa1p and Ydj1p is required for post-translational translocation into the yeast endoplasmic reticulum. Genetics 156 2 (2000) 501-512
53. Minguez J.M., Kim S.Y., Giuliano K.A., Balachandran R., Madiraju C., Day B.W., and Curran D.P. Synthesis and biological assessment of simplified analogues of the potent microtubule stabilizer (+)-discodermolide. Bioorg. Med. Chem. 11 15 (2003) 3335-3357
54. Mossi R., Keller R.C., Ferrari E., and Hubscher U. DNA polymerase switching: II. Replication factor C abrogates primer synthesis by DNA polymerase alpha at a critical length. J. Mol. Biol. 295 4 (2000) 803-814
55. Nadeau K., Nadler S.G., Saulnier M., Tepper M.A., and Walsh C.T. Quantitation of the interaction of the immunosuppressant deoxyspergualin and analogs with Hsc70 and Hsp90. Biochemistry 33 9 (1994) 2561-2567
56. Nylandsted J., Rohde M., Brand K., Bastholm L., Elling F., and Jaattela M. Selective depletion of heat shock protein 70 (Hsp70) activates a tumor-specific death program that is independent of caspases and bypasses Bcl-2. Proc. Natl. Acad. Sci. USA 97 14 (2000) 7871-7876
57. Peden K.W., and Pipas J.M. Simian virus 40 mutants with amino-acid substitutions near the amino terminus of large T antigen. Virus Genes 6 2 (1992) 107-118
58. Pipas J.M., and Levine A.J. Role of T antigen interactions with p53 in tumorigenesis. Semin. Cancer Biol. 11 1 (2001) 23-30
59. Portolani M., Pietrosemoli P., Cermelli C., Mannini-Palenzona A., Grossi M.P., Paolini L., and Barbanti-Brodano G. Suppression of BK virus replication and cytopathic effect by inhibitors of prokaryotic DNA gyrase. Antivir. Res. 9 3 (1988) 205-218
60. Poulin D.L., and DeCaprio J.A. Is there a role for SV40 in human cancer?. J. Clin. Oncol. 24 26 (2006) 4356-4365
61. Ramakers C., Ruijter J.M., Deprez R.H., and Moorman A.F. Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci. Lett. 339 1 (2003) 62-66
62. Rodina A., Vilenchik M., Moulick K., Aguirre J., Kim J., Chiang A., Litz J., Clement C.C., Kang Y., She Y., Wu N., Felts S., Wipf P., Massague J., Jiang X., Brodsky J.L., Krystal G.W., and Chiosis G. Selective compounds define Hsp90 as a major inhibitor of apoptosis in small-cell lung cancer. Nat. Chem. Biol. 3 8 (2007) 498-507
63. Safak M., and Khalili K. An overview: human polyomavirus JC virus and its associated disorders. J. Neurovirol. 9 (2003) 3-9
64. Sawai E.T., and Butel J.S. Association of a cellular heat shock protein with simian virus 40 large T antigen in transformed cells. J. Virol. 63 9 (1989) 3961-3973
65. Sawai E.T., Rasmussen G., and Butel J.S. Construction of SV40 deletion mutants and delimitation of the binding domain for heat shock protein to the amino terminus of large T-antigen. Virus Res. 31 3 (1994) 367-378
66. Smelkova N.V., and Borowiec J.A. Dimerization of simian virus 40 T-antigen hexamers activates T-antigen DNA helicase activity. J. Virol. 71 11 (1997) 8766-8773
67. Sock E., Enderich J., and Wegner M. The J domain of papovaviral large tumor antigen is required for synergistic interaction with the POU-domain protein Tst-1/Oct6/SCIP. Mol. Cell. Biol. 19 4 (1999) 2455-2464
68. Srinivasan A., McClellan A.J., Vartikar J., Marks I., Cantalupo P., Li Y., Whyte P., Rundell K., Brodsky J.L., and Pipas J.M. The amino-terminal transforming region of simian virus 40 large T and small t antigens functions as a J domain. Mol. Cell. Biol. 17 8 (1997) 4761-4773
69. Suh W.C., Burkholder W.F., Lu C.Z., Zhao X., Gottesman M.E., and Gross C.A. Interaction of the Hsp70 molecular chaperone, DnaK, with its cochaperone DnaJ. Proc. Natl. Acad. Sci. USA 95 26 (1998) 15223-15228
70. Sullivan C.S., Cantalupo P., and Pipas J.M. The molecular chaperone activity of simian virus 40 large T antigen is required to disrupt Rb-E2F family complexes by an ATP-dependent mechanism. Mol. Cell. Biol. 20 17 (2000) 6233-6243
71. Sullivan C.S., and Pipas J.M. T antigens of simian virus 40: molecular chaperones for viral replication and tumorigenesis. Microbiol. Mol. Biol. Rev. 66 2 (2002) 179-202
72. Taneja P., Gu J., Peng R., Carrick R., Uchiumi F., Ott R.D., Gustafson E., Podust V.N., and Fanning E. A dominant-negative mutant of human DNA helicase B blocks the onset of chromosome DNA replication. J. Biol. Chem. 277 43 (2002) 40853-40861
73. Tanguy Le Gac N., and Boehmer P.E. Activation of the herpes simplex virus type-1 origin-binding protein (UL9) by heat shock proteins. J. Biol. Chem. 277 7 (2002) 5660-5666
74. Tremblay J.D., Sachsenmeier K.F., and Pipas J.M. Propagation of wild-type and mutant SV40. Methods Mol. Biol. 165 (2001) 1-7
75. Valle M., Chen X., Donate L.E., Fanning E., and Carazo J.M. Structural basis for the cooperative assembly of large T antigen on the origin of replication. J. Mol. Biol. 357 (2006) 1295-1305
76. Vats A., Randhawa P.S., and Shapiro R. Diagnosis and treatment of BK virus-associated transplant nephropathy. Adv. Exp. Med. Biol. 577 (2006) 213-227
77. Weisshart K., Bradley M.K., Weiner B.M., Schneider C., Moarefi I., Fanning E., and Arthur A.K. An N-terminal deletion mutant of simian virus 40 (SV40) large T antigen oligomerizes incorrectly on SV40 DNA but retains the ability to bind to DNA polymerase alpha and replicate SV40 DNA in vitro. J. Virol. 70 6 (1996) 3509-3516
78. Whetstone H., and Lingwood C. 3′Sulfogalactolipid binding specifically inhibits Hsp70 ATPase activity in vitro. Biochemistry 42 6 (2003) 1611-1617
79. Wright C., Chovatiya R., Jameson N., Turner D., Zhu G., Werner S., Huryn D., Pipas J., Day B., Wipf P., and Brodsky J. Pyrimidinone-peptoid hybrid molecules with distinct effects on molecular chaperone function and cell proliferation. Bioorg. Med. Chem. 16 (2008) 3291-3301
80. Youker R.T., Walsh P., Beilharz T., Lithgow T., and Brodsky J.L. Distinct roles for the Hsp40 and Hsp90 molecular chaperones during cystic fibrosis transmembrane conductance regulator degradation in yeast. Mol. Biol. Cell. 15 11 (2004) 4787-4797
81. Yuzhakov A., Kelman Z., Hurwitz J., and O'Donnell M. Multiple competition reactions for RPA order the assembly of the DNA polymerase delta holoenzyme. EMBO J. 18 21 (1999) 6189-6199
82. Ziegler K., Bui T., Frisque R.J., Grandinetti A., and Nerurkar V.R. A rapid in vitro polyomavirus DNA replication assay. J. Virol. Methods 122 1 (2004) 123-127