Cleavage preference distinguishes the two-component NS2B-NS3 serine proteinases of Dengue and West Nile viruses

Biochemical Journal

Volumn 401, Issue 3, 2007, Pages 743-752

  Shiryaev, Sergey A ^a   Kozlov, Igor A ^b   Ratnikov, Boris I ^a   Smith, Jeffrey W ^a   Lebl, Michal ^b   Strongin, Alex Y ^a  

^a BURNHAM INSTITUTE   (United States)

^b ILLUMINA INC   (United States)

Author keywords

Dengue fever virus; Flavivirus; NS2B NS3; Peptide cleavage assay; Polyprotein precursor processing; West Nile virus

Indexed keywords

AMINO ACIDS; ENZYME INHIBITION; MEDICAL PROBLEMS; SUBSTRATES; SYNTHESIS (CHEMICAL); VIRUSES;

DENGUE FEVER VIRUS; FLAVIVIRUS; PEPTIDE CLEAVAGE ASSAY; POLYPROTEIN PRECURSOR PROCESSING; WEST NILE VIRUS;

ENZYMES;

AMINO ACID DERIVATIVE; BIOTIN; GLYCINE; SERINE PROTEINASE; VIRUS ENZYME;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DENGUE VIRUS; ENZYME SPECIFICITY; MOLECULAR RECOGNITION; NONHUMAN; NUCLEOTIDE SEQUENCE; PEPTIDE SYNTHESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; SEQUENCE ANALYSIS; WEST NILE FLAVIVIRUS;

BINDING SITES; DENGUE VIRUS; MUTATION; RNA HELICASES; SERINE ENDOPEPTIDASES; SUBSTRATE SPECIFICITY; VIRAL NONSTRUCTURAL PROTEINS; WEST NILE VIRUS;

DENGUE VIRUS; FLAVIVIRUS; WEST NILE VIRUS;

EID: 33846883704     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20061136     Document Type: Article

References (50)

1. Chambers, T. J. and Diamond, M. S. (2003) Pathogenesis of flavivirus encephalitis. Adv. Virus Res. 60, 273-342
2. Samuel, C. E. (2002) Host genetic variability and West Nile virus susceptibility. Proc. Natl. Acad. Sci. U.S.A. 99, 11555-11557
3. Mukhopadhyay, S., Kuhn, R. J. and Rossmann, M. G. (2005) A structural perspective of the flavivirus life cycle. Nat. Rev. Microbiol. 3, 13-22
4. Chambers, T. J., Droll, D. A., Tang, Y., Liang, Y., Ganesh, V. K., Murthy, K. H. and Nickells, M. (2005) Yellow fever virus NS2B-NS3 protease: characterization of charged-to-alanine mutant and revertant viruses and analysis of polyprotein-cleavage activities. J. Gen. Virol. 86, 1403-1413
5. Chambers, T. J., Nestorowicz, A., Amberg, S. M. and Rice, C. M. (1993) Mutagenesis of the yellow fever virus NS2B protein: effects on proteolytic processing, NS2B-NS3 complex formation, and viral replication. J. Virol. 67, 6797-6807
6. Chappell, K. J., Nall, T. A., Stoermer, M. J., Fang, N. X., Tyndall, J. D., Fairlie, D. P. and Young, P. R. (2005) Site-directed mutagenesis and kinetic studies of the West Nile Virus NS3 protease identify key enzyme-substrate interactions. J. Biol. Chem. 280, 2896-2903
7. Clum, S., Ebner, K. E. and Padmanabhan, R. (1997) Co-translational membrane insertion of the serine proteinase precursor NS2B-NS3(Pro) of dengue virus type 2 is required for efficient in vitro processing and is mediated through the hydrophobic regions of NS2B. J. Biol. Chem. 272, 30715-30723
8. Falgout, B., Miller, R. H. and Lai, C. J. (1993) Deletion analysis of dengue virus type 4 nonstructural protein NS2B: identification of a domain required for NS2B-NS3 protease activity. J. Virol. 67, 2034-2042
9. Falgout, B., Pethel, M., Zhang, Y. M. and Lai, C. J. (1991) Both nonstructural proteins NS2B and NS3 are required for the proteolytic processing of Dengue virus nonstructural proteins. J. Virol. 65, 2467-2475
10. Keelapang, P., Sriburi, R., Supasa, S., Panyadee, N., Songjaeng, A., Jairungsri, A., Puttikhunt, C., Kasinrerk, W., Malasit, P. and Sittisombut, N. (2004) Alterations of pr-M cleavage and virus export in pr-M junction chimeric Dengue viruses. J. Virol. 78, 2367-2381
11. Lin, C., Pragai, B. M., Grakoui, A., Xu, J. and Rice, C. M. (1994) Hepatitis C virus NS3 serine proteinase: trans-cleavage requirements and processing kinetics. J. Virol. 68, 8147-8157
12. Preugschat, F., Yao, C. W. and Strauss, J. H. (1990) In vitro processing of Dengue virus type 2 nonstructural proteins NS2A, NS2B, and NS3. J. Virol. 64, 4364-4374
13. Shafee, N. and AbuBakar, S. (2003) Dengue virus type 2 NS3 protease and NS2B-NS3 protease precursor induce apoptosis. J. Gen. Virol. 84, 2191-2195
14. Stadler, K., Allison, S. L., Schalich, J. and Heinz, F. X. (1997) Proteolytic activation of tick-borne encephalitis virus by furin. J. Viral. 71, 8475-8481
15. Stocks, C. E. and Lobigs, M. (1998) Signal peptidase cleavage at the flavivirus C-prM junction: dependence on the viral NS2B-3 protease for efficient processing requires determinants in C, the signal peptide, and prM. J. Virol. 72, 2141-2149
16. Yamshchikov, V. F. and Compans, R. W. (1994) Processing of the intracellular form of the West Nile virus capsid protein by the viral NS2B-NS3 protease: an in vitro study. J. Virol. 68, 5765-5771
17. Yamshchikov, V. F., Trent, D. W. and Compans, R. W. (1997) Upregulation of signalase processing and induction of prM-E secretion by the flavivirus NS2B-NS3 protease: roles of protease components. J. Virol. 71, 4364-4371
18. Yusof, R., Clum, S., Wetzel, M., Murthy, H. M. and Padmanabhan, R. (2000) Purified NS2B/NS3 serine protease of Dengue virus type 2 exhibits cofactor NS2B dependence for cleavage of substrates with dibasic amino acids in vitro. J. Biol. Chem. 275, 9963-9969
19. Cahour, A., Falgout, B. and Lai, C. J. (1992) Cleavage of the Dengue virus polyprotein at the NS3/NS4A and NS4B/NS5 junctions is mediated by viral protease NS2B-NS3, whereas NS4A/NS4B may be processed by a cellular protease. J. Virol. 66, 1535-1542
20. Yon, C., Teramoto, T., Mueller, N., Phelan, J., Ganesh, V K., Murthy, K. H. and Padmanabhan, R. (2005) Modulation of the nucleoside triphosphatase/RNA helicase and 5′-RNA triphosphatase activities of Dengue virus type 2 nonstructural protein 3 (NS3) by interaction with NS5, the RNA-dependent RNA polymerase. J. Biol. Chem. 280, 27412-27419
21. Kang, L. W., Cho, H. S., Cha, S. S., Chung, K. M., Back, S. H., Jang, S. K. and Oh, B. H. (1998) Crystallization and preliminary X-ray crystallographic analysis of the helicase domain of hepatitis C virus NS3 protein. Acta Crystallogr. Sect. D Biol. Crystallogr. 54, 121-123
22. Mackintosh, S. G., Lu, J. Z., Jordan, J. B., Harrison, M. K., Sikora, B., Sharma, S. D., Cameron, C. E., Raney, K. D. and Sakon, J. (2006) Structural and biological identification of residues on the surface of NS3 helicase required for optimal replication of the hepatitis C virus. J. Biol. Chem. 281, 3528-3535
23. Tai, C. L., Pan, W. C., Liaw, S. H., Yang, U. C., Hwang, L. H. and Chen, D. S. (2001) Structure-based mutational analysis of the hepatitis C virus NS3 helicase. J. Virol. 75, 8289-8297
24. Nall, T. A., Chappell, K. J., Stoermer, M. J., Fang, N. X., Tyndall, J. D., Young, P. R. and Fairlie, D. P. (2004) Enzymatic characterization and homology model of a catalytically active recombinant West Nile virus NS3 protease. J. Biol. Chem. 279, 48535-48542
25. Brinkworth, R. I., Fairlie, D. P., Leung, D. and Young, P. R. (1999) Homology model of the dengue 2 virus NS3 protease: putative interactions with both substrate and NS2B cofactor. J. Gen. Virol. 80, 1167-1177
26. Leung, D., Schroder, K., White, H., Fang, N. X., Stoermer, M. J., Abbenante, G., Martin, J. L., Young, P. R. and Fairlie, D. P. (2001) Activity of recombinant Dengue 2 virus NS3 protease in the presence of a truncated NS2B co-factor, small peptide substrates, and inhibitors. J. Biol. Chem. 276, 45762-45771
27. Niyomrattanakit, P, Winoyanuwattikun, P., Chanprapaph, S., Angsutnanasombat, C., Panyim, S. and Katzenmeier, G. (2004) Identification of residues in the Dengue virus type 2 NS2B cofactor that are critical for NS3 protease activation. J. Virol. 78, 13708-13716
28. Beasley, D. W. (2005) Recent advances in the molecular biology of West Nile virus. Curr. Mol. Med. 5, 835-850
29. Shiryaev, S. A., Ratnikov, B. I., Chekanov, A. V., Sikora, S., Rozanov, D. V., Godzik, A., Wang, J., Smith, J. W., Huang, Z., Lindberg, I. et al. (2006) Cleavage targets and the D-arginine-based inhibitors of the West Nile virus NS3 processing proteinase. Biochem. J. 393, 503-511
30. Kacprzak, M. M., Peinado, J. R., Than, M. E., Appel, J., Henrich, S., Lipkind, G., Houghten, R. A., Bode, W. and Lindberg, I. (2004) Inhibition of furin by polyarginine-containing peptides: nanomolar inhibition by nona-D-arginine. J. Biol. Chem. 279, 36788-36794
31. Lebl, M. (1999) New technique for high-throughput synthesis. Bioorg. Med. Chem. Lett. 9, 1305-1310
32. Lebl, M. and Hachmann, J. (2005) High-throughput peptide synthesis. Methods Mol. Biol. 298, 167-194
33. Hachmann, J. and Lebl, M. (2006) Alternative to piperidine in Fmoc solid-phase synthesis. J. Comb. Chem. 8, 149
34. Fischer, R., Mader, O., Jung, G. and Brock, R. (2003) Extending the applicability of carboxyfluorescein in solid-phase synthesis. Bioconjugate Chem. 14, 653-660
35. King, D. S., Fields, C. G. and Fields, G. B. (1990) A cleavage method which minimizes side reactions following Fmoc solid phase peptide synthesis. Int. J. Pept. Protein Res. 36, 255-266
36. Wu, C. F., Wang, S. H., Sun, C. M., Hu, S. T. and Syu, W. J. (2003) Activation of dengue protease autocleavage at the NS2B-NS3 junction by recombinant NS3 and GST-NS2B fusion proteins. J. Virol. Methods 114, 45-54
37. Li, J., Lim, S. P., Beer, D., Patel, V., Wen, D., Tumanut, C., Tully, D. C., Williams, J. A., Jiricek, J., Priestle, J. P. et al. (2005) Functional profiling of recombinant NS3 proteases from all four serotypes of dengue virus using tetrapeptide and octapeptide substrate libraries. J. Biol. Chem. 280, 28766-28774
38. Niyomrattanakit, P., Yahorava, S., Mutule, I., Mutulis, F., Petrovska, R., Prusis, P., Katzenmeier, G. and Wikberg, J. E. (2006) Probing the substrate specificity of the Dengue virus type 2 NS3 serine protease by using internally quenched fluorescent peptides. Biocnem. J. 397, 203-211
39. Hachmann, J. and Lebl, M. (2006) Search for optimal coupling reagent in multiple peptide synthesizer. Biopolymers 84, 340-347
40. Lebl, M., Pokorny, V. and Krchnak, V. (2005) Simple tools for resin distribution. J. Comb. Chem. 7, 42-45
41. Kozlov, I. A., Melnyk, P. C., Zhao, C., Hachmann, J. P., Shevchenko, V., Srinivasan, A., Barker, D. L. and Lebl, M. (2006) A method for rapid protease substrate evaluation and optimization. Comb. Chem. High Throughput Screen. 9, 481-487
42. Thomas, G. (2002) Furin at the cutting edge: from protein traffic to embryogenesis and disease. Nat. Rev. Mol. Cell. Biol. 3, 753-766
43. Elshuber, S., Allison, S. L., Heinz, F. X. and Mandl, C. W. (2003) Cleavage of protein prM is necessary for infection of BHK-21 cells by tick-borne encephalitis virus. J. Gen. Virol. 84, 183-191
44. Seidah, N. G. (2006) Unexpected similarity between the cytosolic West Nile virus NS3 and the secretory furin-like serine proteinases. Biochem. J. 393, e1-e3
45. Hayes, C. G. (2001) West Nile virus: Uganda, 1937, to New York City, 1999. Ann. NY Acad. Sci. 951, 25-37
46. Erbel, P., Schiering, N., D'Arcy, A., Renatus, M., Kroemer, M., Lim, S. P., Yin, Z., Keller, T. H., Vasudevan, S. G. and Hommel, U. (2006) Structural basis for the activation of flaviviral NS3 proteases from dengue and West Nile virus. Nat. Struct. Mol. Biol. 13, 372-373
47. Melino, S., Fucito, S., Campagna, A., Wrubl, F., Gamarnik, A., Cicero, D. O. and Paci, M. (2006) The active essential CFNS3d protein complex. FEBS J. 273, 3650-3662
48. Khumthong, R., Angsuthanasombat, C., Panyim, S. and Katzenmeier, G. (2002) In vitro determination of dengue virus type 2 NS2B-NS3 protease activity with fluorescent peptide substrates. J. Biochem. Mol. Biol. 35, 206-212
49. Khumthong, R., Niyomrattanakit, P., Chanprapaph, S., Angsuthanasombat, C., Panyim, S. and Katzenmeier, G. (2003) Steady-state cleavage kinetics for dengue virus type 2 NS2B-NS3(pro) serine protease with synthetic peptides. Protein Pept. Lett. 10, 19-26
50. Lin, C., Chambers, T. J. and Rice, C. M. (1993) Mutagenesis of conserved residues at the yellow fever virus 3/4A and 4B/5 dibasic cleavage sites: effects on cleavage efficiency and polyprotein processing. Virology 192, 596-604