Development of chemical inhibitors of the SARS coronavirus: Viral helicase as a potential target

Biochemical Pharmacology

Volumn 84, Issue 10, 2012, Pages 1351-1358

  Keum, Young Sam ^a   Jeong, Yong Joo ^b  

^a Dongguk University   (South Korea)

^b Kookmin University   (South Korea)

Author keywords

Coronavirus; Myricetin; nsP13; Scutellarein; Severe acute respiratory syndrome (SARS)

Indexed keywords

HELICASE; MYRICETIN; NUCLEIC ACID; SCUTELLAREIN; UNCLASSIFIED DRUG; VIRAL HELICASE;

ENZYME ACTIVITY; ENZYME BINDING; ENZYME INHIBITION; ENZYME KINETICS; HYDROLYSIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SARS CORONAVIRUS; SEVERE ACUTE RESPIRATORY SYNDROME;

ANTIVIRAL AGENTS; APIGENIN; DNA HELICASES; DNA, VIRAL; FLAVONOIDS; HUMANS; HYDROLYSIS; METHYLTRANSFERASES; NUCLEOSIDE-TRIPHOSPHATASE; SARS VIRUS; SEVERE ACUTE RESPIRATORY SYNDROME;

EID: 84867854189     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2012.08.012     Document Type: Review

References (80)

1. A. Berger, C. Drosten, H.W. Doerr, M. Sturmer, and W. Preiser Severe acute respiratory syndrome (SARS) - paradigm of an emerging viral infection J Clin Virol 29 2004 13 22
2. J.S. Peiris, K.Y. Yuen, A.D. Osterhaus, and K. Stohr The severe acute respiratory syndrome N Engl J Med 349 2003 2431 2441
3. M.A. Marra, S.J. Jones, C.R. Astell, R.A. Holt, A. Brooks-Wilson, and Y.S. Butterfield The Genome sequence of the SARS-associated coronavirus Science 300 2003 1399 1404
4. P.A. Rota, M.S. Oberste, S.S. Monroe, W.A. Nix, R. Campagnoli, and J.P. Icenogle Characterization of a novel coronavirus associated with severe acute respiratory syndrome Science 300 2003 1394 1399
5. Severe acute respiratory syndrome (SARS): over 100 days into the outbreak. Wkly Epidemiol Rec 2003;78:217-20.
6. V. Thiel, K.A. Ivanov, A. Putics, T. Hertzig, B. Schelle, and S. Bayer Mechanisms and enzymes involved in SARS coronavirus genome expression J Gen Virol 84 2003 2305 2315
7. SARS Investigation Team from DMERI; SGH Strategies adopted and lessons learnt during the severe acute respiratory syndrome crisis in Singapore Rev Med Virol 15 2005 57 70
8. T.M. Lohman, and K.P. Bjornson Mechanisms of helicase-catalyzed DNA unwinding Annual Review of Biochemistry 65 1996 169 214
9. S.S. Patel, and I. Donmez Mechanisms of helicases J Biol Chem 281 2006 18265 18268
10. S.S. Patel, and K.M. Picha Structure and function of hexameric helicases Annu Rev Biochem 69 2000 651 697 2000
11. M. Abdel-Monem, and H. Hoffmann-Berling Enzymic unwinding of DNA. 1. Purification and characterization of a DNA-dependent ATPase from Escherichia coli Eur J Biochem 65 1976 431 440
12. A. Kornberg DNA replication Biochimica et Biophysica Acta 951 1988 235 239
13. X. Veaute, S. Delmas, M. Selva, J. Jeusset, E. Le Cam, and I. Matic UvrD helicase, unlike Rep helicase, dismantles RecA nucleoprotein filaments in Escherichia coli EMBO J 24 2005 180 189
14. E. Jankowsky, C.H. Gross, S. Shuman, and A.M. Pyle Active disruption of an RNA-protein interaction by a DExH/D RNA helicase Science 291 2001 121 125
15. A. Saha, J. Wittmeyer, and B.R. Cairns Chromatin remodelling: the industrial revolution of DNA around histones Nat Rev Mol Cell Biol 7 2006 437 447
16. N.A. Ellis DNA helicases in inherited human disorders Curr Opin Genet Dev 7 1997 354 363
17. N.A. Ellis, J. Groden, T.Z. Ye, J. Straughen, D.J. Lennon, and S. Ciocci The Bloom's syndrome gene product is homologous to RecQ helicases Cell 83 1995 655 666
18. C.E. Yu, J. Oshima, Y.H. Fu, E.M. Wijsman, F. Hisama, and R. Alisch Positional cloning of the Werner's syndrome gene Science 272 1996 258 262
19. T.M. Lohman, E.J. Tomko, and C.G. Wu Non-hexameric DNA helicases and translocases: mechanisms and regulation Nat Rev Mol Cell Biol 9 2008 391 401
20. M.R. Singleton, M.S. Dillingham, and D.B. Wigley Structure and mechanism of helicases and nucleic acid translocases Annu Rev Biochem 76 2007 23 50
21. A.E. Gorbalenya, and E.V. Koonin Helicases: amino acidsequence comparisons and structure-function relationships Curr Opin Struct Biol 3 1993 419 429
22. A. Bernini, O. Spiga, V. Venditti, F. Prischi, L. Bracci, and J. Huang Tertiary structure prediction of SARS coronavirus helicase Biochem Biophys Res Commun 343 2006 1101 1104
23. M. Hoffmann, K. Eitner, M. von Grotthuss, L. Rychlewski, E. Banachowicz, and T. Grabarkiewicz Three dimensional model of severe acute respiratory syndrome coronavirus helicase ATPase catalytic domain and molecular design of severe acute respiratory syndrome coronavirus helicase inhibitors J Comput Aided Mol Des 20 2006 305 319
24. E.J. Snijder, P.J. Bredenbeek, J.C. Dobbe, V. Thiel, J. Ziebuhr, and L.L. Poon Unique and conserved features of genome and proteome of SARS-coronavirus, an early split-off from the coronavirus group 2 lineage J Mol Biol 331 2003 991 1004
25. K.J. Jang, N.R. Lee, W.S. Yeo, Y.J. Jeong, and D.E. Kim Isolation of inhibitory RNA aptamers against severe acute respiratory syndrome (SARS) coronavirus NTPase/Helicase Biochem Biophys Res Commun 366 2008 738 744
26. C. Lee, J.M. Lee, N.R. Lee, B.S. Jin, K.J. Jang, and D.E. Kim Aryl diketoacids (ADK) selectively inhibit duplex DNA-unwinding activity of SARS coronavirus NTPase/helicase Bioorg Med Chem Lett 19 2009 1636 1638
27. C. Lee, J.M. Lee, N.R. Lee, D.E. Kim, Y.J. Jeong, and Y. Chong Investigation of the pharmacophore space of severe acute respiratory syndrome coronavirus (SARS-CoV) NTPase/helicase by dihydroxychromone derivatives Bioorg Med Chem Lett 19 2009 4538 4541
28. N.R. Lee, H.M. Kwon, K. Park, S. Oh, Y.J. Jeong, and D.E. Kim Cooperative translocation enhances the unwinding of duplex DNA by SARS coronavirus helicase nsP13 Nucleic Acids Res 38 2010 7626 7636
29. J.A. Tanner, B.J. Zheng, J. Zhou, R.M. Watt, J.Q. Jiang, and K.L. Wong The adamantane-derived bananins are potent inhibitors of the helicase activities and replication of SARS coronavirus Chem Biol 12 2005 303 311
30. J.A. Tanner, R.M. Watt, Y.B. Chai, L.Y. Lu, M.C. Lin, and J.S. Peiris The severe acute respiratory syndrome (SARS) coronavirus NTPase/helicase belongs to a distinct class of 5′ to 3′ viral helicases J Biol Chem 278 2003 39578 39582
31. C.G. Lee, and J. Hurwitz A new RNA helicase isolated from HeLa cells that catalytically translocates in the 3′ to 5′ direction J Biol Chem 267 1992 4398 4407
32. G.W. Rogers Jr., N.J. Richter, and W.C. Merrick Biochemical and kinetic characterization of the RNA helicase activity of eukaryotic initiation factor 4A J Biol Chem 274 1999 12236 12244
33. K.A. Ivanov, V. Thiel, J.C. Dobbe, Y. van der Meer, E.J. Snijder, and J. Ziebuhr Multiple enzymatic activities associated with severe acute respiratory syndrome coronavirus helicase J Virol 78 2004 5619 5632
34. P.S. Pang, E. Jankowsky, P.J. Planet, and A.M. Pyle The hepatitis C viral NS3 protein is a processive DNA helicase with cofactor enhanced RNA unwinding EMBO J 21 2002 1168 1176
35. Y.J. Jeong, M.K. Levin, and S.S. Patel The DNA-unwinding mechanism of the ring helicase of bacteriophage T7 Proc Natl Acad Sci USA 101 2004 7264 7269
36. J.A. Ali, and T.M. Lohman Kinetic measurement of the step size of DNA unwinding by Escherichia coli UvrD helicase Science 275 1997 377 380
37. M.K. Levin, Y.H. Wang, and S.S. Patel The functional interaction of the hepatitis C virus helicase molecules is responsible for unwinding processivity J Biol Chem 279 2004 26005 26012
38. E. Jankowsky, C.H. Gross, S. Shuman, and A.M. Pyle The DExH protein NPH-II is a processive and directional motor for unwinding RNA Nature 403 2000 447 451
39. A.O. Adedeji, B. Marchand, A.J. Te Velthuis, E.J. Snijder, S. Weiss, and R.L. Eoff Mechanism of nucleic acid unwinding by SARS-CoV helicase PLoS One 7 2012 e36521
40. B. Nanduri, A.K. Byrd, R.L. Eoff, A.J. Tackett, and K.D. Raney Pre-steady-state DNA unwinding by bacteriophage T4 Dda helicase reveals a monomeric molecular motor Proc Natl Acad Sci USA 99 2002 14722 14727
41. H.Q. Xu, E. Deprez, A.H. Zhang, P. Tauc, M.M. Ladjimi, and J.C. Brochon The Escherichia coli RecQ helicase functions as a monomer J Biol Chem 278 2003 34925 34933
42. W. Cheng, J. Hsieh, K.M. Brendza, and T.M. Lohman E. coli Rep oligomers are required to initiate DNA unwinding in vitro J Mol Biol 310 2001 327 350
43. C.J. Fischer, N.K. Maluf, and T.M. Lohman Mechanism of ATP-dependent translocation of E. coli UvrD monomers along single-stranded DNA J Mol Biol 344 2004 1287 1309
44. A. Niedziela-Majka, M.A. Chesnik, E.J. Tomko, and T.M. Lohman Bacillus stearothermophilus PcrA monomer is a single-stranded DNA translocase but not a processive helicase in vitro J Biol Chem 282 2007 27076 27085
45. J.A. Ali, N.K. Maluf, and T.M. Lohman An oligomeric form of E. coli UvrD is required for optimal helicase activity J Mol Biol 293 1999 815 834
46. N.K. Maluf, C.J. Fischer, and T.M. Lohman A dimer of Escherichia coli UvrD is the active form of the helicase in vitro J Mol Biol 325 2003 913 935
47. Y. Yang, S.X. Dou, H. Ren, P.Y. Wang, X.D. Zhang, and M. Qian Evidence for a functional dimeric form of the PcrA helicase in DNA unwinding Nucleic Acids Res 36 2008 1976 1989
48. N.M. Stano, Y.J. Jeong, I. Donmez, P. Tummalapalli, M.K. Levin, and S.S. Patel DNA synthesis provides the driving force to accelerate DNA unwinding by a helicase Nature 435 2005 370 373
49. D.E. Kim, M. Narayan, and S.S. Patel T7 DNA helicase: a molecular motor that processively and unidirectionally translocates along single-stranded DNA J Mol Biol 321 2002 807 819
50. A.K. Byrd, and K.D. Raney Increasing the length of the single-stranded overhang enhances unwinding of duplex DNA by bacteriophage T4 Dda helicase Biochemistry 44 2005 12990 12997
51. M.R. Singleton, M.R. Sawaya, T. Ellenberger, and D.B. Wigley Crystal structure of T7 gene 4 ring helicase indicates a mechanism for sequential hydrolysis of nucleotides Cell 101 2000 589 600
52. J.P. Abrahams, A.G. Leslie, R. Lutter, and J.E. Walker Structure at 2.8 A resolution of F1-ATPase from bovine heart mitochondria Nature 370 1994 621 628
53. M.M. Hingorani, M.T. Washington, K.C. Moore, and S.S. Patel The dTTPase mechanism of T7 DNA helicase resembles the binding change mechanism of the F1-ATPase Proc Natl Acad Sci USA 94 1997 5012 5017
54. M.S. Dillingham, D.B. Wigley, and M.R. Webb Demonstration of unidirectional single-stranded DNA translocation by PcrA helicase: measurement of step size and translocation speed Biochemistry 39 2000 205 212
55. P. Soultanas, M.S. Dillingham, P. Wiley, M.R. Webb, and D.B. Wigley Uncoupling DNA translocation and helicase activity in PcrA: direct evidence for an active mechanism EMBO J 19 2000 3799 3810
56. S.S. Velankar, P. Soultanas, M.S. Dillingham, H.S. Subramanya, and D.B. Wigley Crystal structures of complexes of PcrA DNA helicase with a DNA substrate indicate an inchworm mechanism Cell 97 1999 75 84
57. M.M. Hingorani, and S.S. Patel Interactions of bacteriophage T7 DNA primase/helicase protein with single-stranded and double-stranded DNAs Biochemistry 32 1993 12478 12487
58. Y.J. Jeong, D.E. Kim, and S.S. Patel Kinetic pathway of dTTP hydrolysis by hexameric T7 helicase-primase in the absence of DNA J Biol Chem 277 2002 43778 43784
59. E.M. Bautista, K.S. Faaberg, D. Mickelson, and E.D. McGruder Functional properties of the predicted helicase of porcine reproductive and respiratory syndrome virus Virology 298 2002 258 270
60. K.A. Morgenstern, J.A. Landro, K. Hsiao, C. Lin, Y. Gu, and M.S.S. Su Polynucleotide modulation of the protease, nucleoside triphosphatase, and helicase activities of a hepatitis C virus NS3-NS4A complex isolated from transfected COS cells J Virol 71 1997 3767 3775
61. F. Preugschat, D.R. Averett, B.E. Clarke, and D.J.T. Porter A steady-state and pre-steady-state kinetic analysis of the NTPase activity associated with the hepatitis C virus NS3 helicase domain J Biol Chem 271 1996 24449 24457
62. M. Bisaillon, J. Bergeron, and G. Lemay Characterization of the nucleoside triphosphate phosphohydrolase and helicase activities of the reovirus lambda1 protein J Biol Chem 272 1997 18298 18303
63. M. Bisaillon, and G. Lemay Characterization of the reovirus lambda1 protein RNA 5′-triphosphatase activity J Biol Chem 272 1997 29954 29957
64. Y.I. Li, T.W. Shih, Y.H. Hsu, Y.T. Han, Y.L. Huang, and M. Meng The helicase-like domain of plant potexvirus replicase participates in formation of RNA 5′ cap structure by exhibiting RNA 5′-triphosphatase activity J Virol 75 2001 12114 12120
65. G. Kadare, and A.L. Haenni Virus-encoded RNA helicases J Virol 71 1997 2583 2590
66. N.R. Lee, A.R. Lee, B. Lee, D-E. Kim, and Y-J. Jeong ATP hydrolysis analysis of severe acute respiratory syndrome (SARS) coronavirus helicase Korean Chem Soc 30 8 2009 1724 1728
67. P. Soultanas, M.S. Dillingham, S.S. Velankar, and D.B. Wigley DNA binding mediates conformational changes and metal ion coordination in the active site of PcrA helicase J Mol Biol 290 1999 137 148
68. K. Arai, and A. Kornberg Mechanism of dnaB protein action. II. ATP hydrolysis by dnaB protein dependent on single- or double-stranded DNA J Biol Chem 256 1981 5253 5259
69. S.S. Patel, A.H. Rosenberg, F.W. Studier, and K.A. Johnson Large scale purification and biochemical characterization of T7 primase/helicase proteins. evidence for homodimer and heterodimer formation J Biol Chem 267 1992 15013 15021
70. M.T. Washington, A.H. Rosenberg, K. Griffin, F.W. Studier, and S.S. Patel Biochemical analysis of mutant T7 primase/helicase proteins defective in DNA binding, nucleotide hydrolysis, and the coupling of hydrolysis with DNA unwinding J Biol Chem 271 1996 26825 26834
71. L.J. Stockman, R. Bellamy, and P. Garner SARS: systematic review of treatment effects PLoS Med 3 2006 e343
72. J. Cinatl Jr., M. Michaelis, G. Hoever, W. Preiser, and H.W. Doerr Development of antiviral therapy for severe acute respiratory syndrome Antiviral Res 66 2005 81 97
73. M.S. Yu, J. Lee, J.M. Lee, Y. Kim, Y.W. Chin, and J.G. Jee Identification of myricetin and scutellarein as novel chemical inhibitors of the SARS coronavirus helicase, nsP13 Bioorg Med Chem Lett 22 2012 4049 4054
74. R.J. Williams, J.P. Spencer, and C. Rice-Evans Flavonoids: antioxidants or signalling molecules Free Radic Biol Med 36 2004 838 849
75. S. Hassfjell, and M.W. Brechbiel The development of the alpha-particle emitting radionuclides 212Bi and 213Bi, and their decay chain related radionuclides, for therapeutic applications Chem Rev 101 2001 2019 2036
76. N. Yang, J.A. Tanner, B.J. Zheng, R.M. Watt, M.L. He, and L.Y. Lu Bismuth complexes inhibit the SARS coronavirus Angew Chem Int Ed Engl 46 2007 6464 6468
77. N. Yang, J.A. Tanner, Z. Wang, J.D. Huang, B.J. Zheng, and N. Zhu Inhibition of SARS coronavirus helicase by bismuth complexes Chem Commun (Camb) 2007 4413 4415
78. A.L. Totura, and R.S. Baric SARS coronavirus pathogenesis: host innate immune responses and viral antagonism of interferon Curr Opin Virol 2 2012 264 275
79. C.K. Wong, C.W. Lam, A.K. Wu, W.K. Ip, N.L. Lee, and I.H. Chan Plasma inflammatory cytokines and chemokines in severe acute respiratory syndrome Clin Exp Immunol 136 2004 95 103
80. S.L. Smits, A. de Lang, J.M. van den Brand, L.M. Leijten, I.W.F. van, and M.J. Eijkemans Exacerbated innate host response to SARS-CoV in aged non-human primates PLoS Pathog 6 2010 e1000756