Evolutionary constraints on chaperone-mediated folding provide an antiviral approach refractory to development of drug resistance

Genes and Development

Volumn 21, Issue 2, 2007, Pages 195-205

  Geller, Ron ^a   Vignuzzi, Marco ^b   Andino, Raul ^b   Frydman, Judith ^a  

^a STANFORD UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Antiviral; Drug resistance; Evolution; Hsp90; Picornavirus; Protein folding

Indexed keywords

17 ALLYLAMINO 17 DEMETHOXYGELDANAMYCIN; CAPSID PROTEIN; CHAPERONE; GELDANAMYCIN; HEAT SHOCK PROTEIN 90; HEAT SHOCK PROTEIN 90 INHIBITOR; VIRUS PROTEIN; VIRUS RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; COXSACKIE VIRUS; DOSE RESPONSE; DRUG MECHANISM; FEMALE; HUMAN; HUMAN CELL; MALE; MOLECULAR EVOLUTION; MOUSE; NONHUMAN; PICORNAVIRUS; POLIOMYELITIS VIRUS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEIN PROCESSING; PROTEIN TARGETING; RHINOVIRUS; RNA VIRUS; VIRUS CAPSID; VIRUS INHIBITION; VIRUS REPLICATION;

ANIMALS; ANTIVIRAL AGENTS; BENZOQUINONES; CAPSID PROTEINS; CELL LINE; CERCOPITHECUS AETHIOPS; DRUG RESISTANCE, VIRAL; EVOLUTION, MOLECULAR; FEMALE; FIBROBLASTS; HELA CELLS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; LACTAMS, MACROCYCLIC; MALE; MICE; MICE, TRANSGENIC; PICORNAVIRIDAE; PICORNAVIRIDAE INFECTIONS; PROTEIN FOLDING; VERO CELLS; VIRUS REPLICATION;

ANIMALIA; COXSACKIEVIRUS; MIRIDAE; PICORNAVIRIDAE; POLIOVIRUS; RHINOVIRUS; RNA VIRUSES;

EID: 33846471075     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1505307     Document Type: Article

References (56)

1. Aberham, C., Weber, S., and Phares, W. 1996. Spontaneous mutations in the human immunodeficiency virus type 1 gag gene that affect viral replication in the presence of cyclosporins. J. Virol. 70: 3536-3544.
2. Ali, M.M., Roe, S.M., Vaughan, C.K., Meyer, P., Panaretou, B., Piper, P.W., Prodromou, C., and Pearl, L.H. 2006. Crystal structure of an Hsp90-nucleotide-p23/Sba1 closed chaperone complex. Nature 440: 1013-1017.
3. Andino, R., Rieckhof, G.E., Achacoso, P.L., and Baltimore, D. 1993. Poliovirus RNA synthesis utilizes an RNP complex formed around the 5′-end of viral RNA. EMBO J. 12: 3587-3598.
4. Ansardi, D.C., Porter, D.C., and Morrow, C.D. 1991. Coinfection with recombinant vaccinia viruses expressing poliovirus P1 and P3 proteins results in polyprotein processing and formation of empty capsid structures. J. Virol. 65: 2088-2092.
5. Basavappa, R., Syed, R., Flore, O., Icenogle, J.P., Filman, D.J., and Hogle, J.M. 1994. Role and mechanism of the maturation cleavage of VP0 in poliovirus assembly: Structure of the empty capsid assembly intermediate at 2.9 Å resolution. Protein Sci. 3: 1651-1669.
6. Basha, W., Kitagawa, R., Uhara, M., Imazu, H., Uechi, K., and Tanaka, J. 2005. Geldanamycin, a potent and specific inhibitor of Hsp90, inhibits gene expression and replication of human cytomegalovirus. Antivir. Chem. Chemother. 16: 135-146.
7. Borkovich, K.A., Farrelly, F.W., Finkelstein, D.B., Taulien, J., and Lindquist, S. 1989. hsp82 is an essential protein that is required in higher concentrations for growth of cells at higher temperatures. Mol. Cell. Biol. 9: 3919-3930.
8. Braakman, I. and van Anken, E. 2000. Folding of viral envelope glycoproteins in the endoplasmic reticulum. Traffic 1: 533-539.
9. Bucci, M., Roviezzo, F., Cicala, C., Sessa, W.C., and Cirino, G. 2000. Geldanamycin, an inhibitor of heat shock protein 90 (Hsp90) mediated signal transduction has anti-inflammatory effects and interacts with glucocorticoid receptor in vivo. Br. J. Pharmacol. 131: 13-16.
10. Burch, A.D. and Weller, S.K. 2005. Herpes simplex virus type 1 DNA polymerase requires the mammalian chaperone hsp90 for proper localization to the nucleus. J. Virol. 79: 10740-10749.
11. Committee on Development of a Polio Antiviral and Its Potential Role in Global Poliomyelitis Eradication. 2006. Exploring the Role of Antiviral Drugs in the Eradication of Polio. The National Academies Press, Washington, DC. http:// www.nap.edu/catalog/11599.html.
12. Crotty, S., Hix, L., Sigal, L.J., and Andino, R. 2002. Poliovirus pathogenesis in a new poliovirus receptor transgenic mouse model: Age-dependent paralysis and a mucosal route of infection. J. Gen. Virol. 83: 1707-1720.
13. Crotty, S., Saleh, M.C., Gitlin, L., Beske, O., and Andino, R. 2004. The poliovirus replication machinery can escape inhibition by an antiviral drug that targets a host cell protein. J. Virol. 78: 3378-3386.
14. Crowder, S. and Kirkegaard, K. 2005. Trans-dominant inhibition of RNA viral replication can slow growth of drug-resistant viruses. Nat. Genet. 37: 701-709.
15. Cuconati, A., Molla, A., and Wimmer, E. 1998. Brefeldin A inhibits cell-free, de novo synthesis of poliovirus. J. Virol. 72: 6456-6464.
16. Dai, C. and Whitesell, L. 2005. HSP90: A rising star on the horizon of anticancer targets. Future Oncol. 1: 529-540.
17. Doedens, J., Maynell, L.A., Klymkowsky, M.W., and Kirkegaard, K. 1994. Secretory pathway function, but not cytoskeletal integrity, is required in poliovirus infection. Arch. Virol. Suppl. 9: 159-172.
18. Domingo, E. and Holland, J.J. 1997. RNA virus mutations and fitness for survival. Annu. Rev. Microbiol. 51: 151-178.
19. Drake, J.W. 1999. The distribution of rates of spontaneous mutation over viruses, prokaryotes, and eukaryotes. Ann. N. Y. Acad. Sci. 870: 100-107.
20. Elena, S.F., Carrasco, P., Daros, J.A., and Sanjuan, R. 2006. Mechanisms of genetic robustness in RNA viruses. EMBO Rep. 7: 168-173.
21. Fields, B.N., Knipe, D.M., Howley, P.M., and Griffin, D.E. 2001. Fields' virology. Lippincott Williams & Wilkins, Philadelphia.
22. Frydman, J. 2001. Folding of newly translated proteins in vivo: The role of molecular chaperones. Annu. Rev. Biochem. 70: 603-647.
23. Gitlin, L., Karelsky, S., and Andino, R. 2002. Short interfering RNA confers intracellular antiviral immunity in human cells. Nature 418: 430-434.
24. Haas, A.L. and Rose, I.A. 1981. Hemin inhibits ATP-dependent ubiquitin-dependent proteolysis: Role of hemin in regulating ubiquitin conjugate degradation. Proc. Natl. Acad. Sci. 78: 6845-6848.
25. Herold, J. and Andino, R. 2000. Poliovirus requires a precise 5′ end for efficient positive-strand RNA synthesis. J. Virol. 74: 6394-6400.
26. Hogle, J.M. 2002. Poliovirus cell entry: Common structural themes in viral cell entry pathways. Annu. Rev. Microbiol. 56: 677-702.
27. Hong, S., Choi, G., Park, S., Chung, A.S., Hunter, E., and Rhee, S.S. 2001. Type D retrovirus Gag polyprotein interacts with the cytosolic chaperonin TRiC. J. Virol. 75: 2526-2534.
28. Hu, J. and Anselmo, D. 2000. In vitro reconstitution of a functional duck hepatitis B virus reverse transcriptase: Posttranslational activation by Hsp90. J. Virol. 74: 11447-11455.
29. Hu, J., Toft, D.O., and Seeger, C. 1997. Hepadnavirus assembly and reverse transcription require a multi-component chaperone complex which is incorporated into nucleocapsids. EMBO J. 16: 59-68.
30. Hung, J.J., Chung, C.S., and Chang, W. 2002. Molecular chaperone Hsp90 is important for vaccinia virus growth in cells. J. Virol. 76: 1379-1390.
31. Irurzun, A., Perez, L., and Carrasco, L. 1992. Involvement of membrane traffic in the replication of poliovirus genomes: Effects of brefeldin A. Virology 191: 166-175.
32. Janin, Y.L. 2005. Heat shock protein 90 inhibitors. A text book example of medicinal chemistry? J. Med. Chem. 48: 7503-7512.
33. Kamal, A., Thao, L., Sensintaffar, J., Zhang, L., Boehm, M.F., Fritz, L.C., and Burrows, F.J. 2003. A high-affinity conformation of Hsp90 confers tumour selectivity on Hsp90 inhibitors. Nature 425: 407-410.
34. Kampmueller, K.M. and Miller, D.J. 2005. The cellular chaperone heat shock protein 90 facilitates Flock House virus RNA replication in Drosophila cells. J. Virol. 79: 6827-6837.
35. Kerner, M.J., Naylor, D.J., Ishihama, Y., Maier, T., Chang, H.C., Stines, A.P., Georgopoulos, C., Frishman, D., Hayer-Hartl, M., Mann, M., et al. 2005. Proteome-wide analysis of chaperonin-dependent protein folding in Escherichia coli. Cell 122: 209-220.
36. Klump, W.M., Bergmann, I., Muller, B.C., Ameis, D., and Kandolf, R. 1990. Complete nucleotide sequence of infectious Coxsackievirus B3 cDNA: Two initial 5′ uridine residues are regained during plus-strand RNA synthesis. J. Virol. 64: 1573-1583.
37. Li, Y.H., Tao, P.Z., Liu, Y.Z., and Jiang, J.D. 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.
38. Macejak, D.G. and Sarnow, P. 1992. Association of heat shock protein 70 with enterovirus capsid precursor P1 in infected human cells. J. Virol. 66: 1520-1527.
39. Mayer, M.P. 2005. Recruitment of Hsp70 chaperones: A crucial part of viral survival strategies. Rev. Physiol. Biochem. Pharmacol. 153: 1-46.
40. Maynell, L.A., Kirkegaard, K., and Klymkowsky, M.W. 1992. Inhibition of poliovirus RNA synthesis by brefeldin A. J. Virol. 66: 1985-1994.
41. Melnick, J.L., Crowther, D., and Barrera-Oro, J. 1961. Rapid development of drug-resistant mutants of poliovirus. Science 134: 557.
42. Murata, T., Goshima, F., Koshizuka, T., Takakuwa, H., and Nishiyama, Y. 2001. A single amino acid substitution in the ICP27 protein of herpes simplex virus type 1 is responsible for its resistance to leptomycin B. J. Virol. 75: 1039-1043.
43. Okamoto, T., Nishimura, Y., Ichimura, T., Suzuki, K., Miyamura, T., Suzuki, T., Moriishi, K., and Matsuura, Y. 2006. Hepatitis C virus RNA replication is regulated by FKBP8 and Hsp90. EMBO J. 25: 5015-5025.
44. Pfeiffer, J.K. and Kirkegaard, K. 2003. A single mutation in poliovirus RNA-dependent RNA polymerase confers resistance to mutagenic nucleotide analogs via increased fidelity. Proc. Natl. Acad. Sci. 100: 7289-7294.
45. Picard, D. 2002. Heat-shock protein 90, a chaperone for folding and regulation. Cell. Mol. Life Sci. 59: 1640-1648.
46. Pillay, D. and Zambon, M. 1998. Antiviral drug resistance. BMJ 317: 660-662.
47. Pratt, W.B. and Toft, D.O. 2003. Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery. Exp. Biol. Med. (Maywood) 228: 111-133.
48. Prodromou, C. and Pearl, L.H. 2003. Structure and functional relationships of Hsp90. Curr. Cancer Drug Targets 3: 301-323.
49. Riggs, D.L., Cox, M.B., Cheung-Flynn, J., Prapapanich, V., Carrigan, P.E., and Smith, D.F. 2004. Functional specificity of co-chaperone interactions with Hsp90 client proteins. Crit. Rev. Biochem. Mol. Biol. 39: 279-295.
50. Sarafianos, S.G., Das, K., Hughes, S.H., and Arnold, E. 2004. Taking aim at a moving target: Designing drugs to inhibit drug-resistant HIV-1 reverse transcriptases. Curr. Opin. Struct. Biol. 14: 716-730.
51. Vignuzzi, M., Stone, J.K., Arnold, J.J., Cameron, C.E., and Andino, R. 2006. Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population. Nature 439: 344-348.
52. Waza, M., Adachi, H., Katsuno, M., Minamiyama, M., Sang, C., Tanaka, F., Inukai, A., Doyu, M., and Sobue, G. 2005. 17-AAG, an Hsp90 inhibitor, ameliorates polyglutamine-mediated motor neuron degeneration. Nat. Med. 11: 1088-1095.
53. Wegele, H., Muller, L., and Buchner, J. 2004. Hsp70 and Hsp90 - A relay team for protein folding. Rev. Physiol. Biochem. Pharmacol. 151: 1-44.
54. Whitesell, L. and Lindquist, S.L. 2005. HSP90 and the chaperoning of cancer. Nat. Rev. Cancer 5: 761-772.
55. Young, J.C., Moarefi, I., and Hartl, F.U. 2001. Hsp90: A specialized but essential protein-folding tool. J. Cell Biol. 154: 267-273.
56. Young, J.C., Agashe, V.R., Siegers, K., and Hartl, F.U. 2004. Pathways of chaperone-mediated protein folding in the cytosol. Nat. Rev. Mol. Cell Biol. 5: 781-791.