Cleavage targets and the D-arginine-based inhibitors of the West Nile virus NS3 processing proteinase

Biochemical Journal

Volumn 393, Issue 2, 2006, Pages 503-511

  Shiryaev, Sergey A ^a   Ratnikov, Boris I ^a   Chekanov, Alexei V ^a   Sikora, Sergey ^a   Rozanov, Dmitri V ^a   Godzik, Adam ^a   Wang, Jun ^a   Smith, Jeffrey W ^a   Huang, Ziwei ^a   Lindberg, Iris ^b   Samuel, Melanie A ^c   Diamond, Michael S ^c   Strongin, Alex Y ^a  

^a BURNHAM INSTITUTE   (United States)

^b LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Dengue virus; Flavivirus; Furin; Peptide inhibitor; Proteinase; West Nile virus

Indexed keywords

BIOCHEMISTRY; NEUROLOGY; SUBSTRATES;

CLEAVAGE TARGETS; DENGUE VIRUS; FURIN; PEPTIDE INHIBITORS;

PROTEINS;

ALPHA 1 ANTITRYPSIN; APROTININ; CATHEPSIN B; COMPLEMENTARY DNA; DEXTRO ARGININE; FURIN; MYELIN BASIC PROTEIN; NONSTRUCTURAL PROTEIN 3; NS3 PROTEINASE; PROTEINASE; PROTEINASE INHIBITOR; SYNTHETIC PEPTIDE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; DNA SEQUENCE; DRUG TARGETING; ENZYME ACTIVITY; ENZYME INHIBITION; HOST CELL; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOUSE; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PEPTIDE SYNTHESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; SOLID PHASE SYNTHESIS; SUPERIOR CERVICAL GANGLION; SYMPATHETIC NERVE; WEST NILE FLAVIVIRUS;

AMINO ACID SEQUENCE; ANIMALS; ARGININE; CELLS, CULTURED; CONSERVED SEQUENCE; FURIN; MICE; MOLECULAR SEQUENCE DATA; MYELIN SHEATH; NEURONS; PEPTIDES; PROTEASE INHIBITORS; RNA HELICASES; SEQUENCE HOMOLOGY, AMINO ACID; SERINE ENDOPEPTIDASES; SERPINS; SUBSTRATE SPECIFICITY; VIRAL NONSTRUCTURAL PROTEINS; WEST NILE VIRUS;

ANIMALIA; DENGUE VIRUS; FLAVIVIRUS; WEST NILE VIRUS;

EID: 30744452734     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20051374     Document Type: Article

References (48)

1. Hayes, C. G. (2001) West Nile virus: Uganda, 1937, to New York City, 1999. Ann. N.Y. Acad. Sci. 951, 25-37
2. van der Meulen, K. M., Pensaert, M. B. and Nauwynck, H. J. (2005) West Nile virus in the vertebrate world. Arch. Virol. 150, 637-657
3. Brinton, M. A. (2002) The molecular biology of West Nile Virus: a new invader of the western hemisphere. Annu. Rev. Microbiol. 56, 371-402
4. Stadler, K., Allison, S. L., Schalich, J. and Heinz, F. X. (1997) Proteolytic activation of tick-borne encephalitis virus by furin. J. Virol. 71, 8475-8481
5. Thomas, G. (2002) Furin at the cutting edge: from protein traffic to embryogenesis and disease. Nat. Rev. Mol. Cell Biol. 3, 753-766
6. 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
7. Clum, S., Ebner, K. E. and Padmanabhan, R. (1997) Cotranslational 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. Jan, L. R., Yang, C. S., Trent, D. W., Falgout, B. and Lai, C. J. (1995) Processing of Japanese encephalitis virus non-structural proteins: NS2B-NS3 complex and heterologous proteases. J. Gen. Virol. 76, 573-580
10. Lobigs, M. (1993) Flavivirus premembrane protein cleavage and spike heterodimer secretion require the function of the viral proteinase NS3. Proc. Natl. Acad. Sci. U.S.A. 90, 6218-6222
11. 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
12. 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
13. 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
14. 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
15. Droll, D. A., Krishna Murthy, H. M. and Chambers, T. J. (2000) Yellow fever virus NS2B-NS3 protease: charged-to-alanine mutagenesis and deletion analysis define regions important for protease complex formation and function. Virology 275, 335-347
16. 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
17. 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
18. 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
19. Murthy, H. M., Clum, S. and Padmanabhan, R. (1999) Dengue virus NS3 serine protease: crystal structure and insights into interaction of the active site with substrates by molecular modeling and structural analysis of mutational effects. J. Biol. Chem. 274, 5573-5580
20. 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
21. 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 tetra- and octa-peptide substrate libraries. J. Biol. Chem. 280, 28766-28774
22. 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
23. 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
24. Easton, R. M., Deckwerth, T. L., Parsadanian, A. S. and Johnson, Jr, E. M. (1997) Analysis of the mechanism of loss of trophic factor dependence associated with neuronal maturation: a phenotype indistinguishable from Bax deletion. J. Neurosci. 17, 9656-9666
25. Diamond, M. S., Sitati, E. M., Friend, L. D., Higgs, S., Shrestha, B. and Engle, M. (2003) A critical role for induced IgM in the protection against West Nile virus infection. J. Exp. Med. 198, 1853-1862
26. Sikora, S. and Godzik, A. (2004) Combination of multiple alignment analysis and surface mapping paves a way for a detailed pathway reconstruction - the case of VHL (von Hippel-Lindau) protein and angiogenesis regulatory pathway. Protein Sci. 13, 786-796
27. Henrich, S., Cameron, A., Bourenkov, G. P., Kiefersauer, R., Huber, R., Lindberg, I., Bode, W. and Than, M. E. (2003) The crystal structure of the proprotein processing proteinase furin explains its stringent specificity. Nat. Struct. Biol. 10, 520-526
28. Collier, R. J. and Young, J. A. (2003) Anthrax toxin. Annu. Rev. Cell Dev. Biol. 19, 45-70
29. 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
30. Wong, S. J., Boyle, R. H., Demarest, V. L., Woodmansee, A. N., Kramer, L. D., Li, H., Drebot, M., Koski, R. A., Fikrig, E., Martin, D. A. and Shi, P. Y. (2003) Immunoassay targeting nonstructural protein 5 to differentiate West Nile virus infection from dengue and St. Louis encephalitis virus infections and from flavivirus vaccination. J. Clin. Microbiol. 41, 4217-4223
31. Golubkov, V. S., Boyd, S., Savinov, A. Y., Chekanov, A. V., Osterman, A. L., Remade, A., Rozanov, D. V., Doxsey, S. J. and Strongin, A. Y. (2005) Membrane type-1 matrix metalloproteinase (MT1-MMP) exhibits an important intracellular cleavage function and causes chromosome instability. J. Biol. Chem. 280, 25079-25086
32. Boyd, S. E., Pike, R. N., Rudy, G. B., Whisstock, J. C. and Garcia de la Banda, M. (2005) Pops: a computational tool for modeling and predicting protease specificity. J. Bioinform. Comput. Biol. 3, 551-585
33. Chernoff, G. F. (1981) Shiverer: an autosomal recessive mutant mouse with myelin deficiency. J. Hered. 72, 128
34. Lutton, J. D., Winston, R. and Rodman, T. C. (2004) Multiple sclerosis: etiological mechanisms and future directions. Exp. Biol. Med. 229, 12-20
35. Pedraza, L. (1997) Nuclear transport of myelin basic protein. J. Neurosci. Res. 50, 258-264
36. Seiwa, C., Kojima-Aikawa, K., Matsumoto, I. and Asou, H. (2002) CNS myelinogenesis in vitro: myelin basic protein deficient shiverer oligodendrocytes. J. Neurosci. Res. 69, 305-317
37. Cameron, A., Appel, J., Houghten, R. A. and Lindberg, I. (2000) Polyarginines are potent furin inhibitors. J. Biol. Chem. 275, 36741-36749
38. Jean, F., Stella, K., Thomas, L., Liu, G., Xiang, Y., Reason, A. J. and Thomas, G. (1998) α1-Antitrypsin Portland, a bioengineered serpin highly selective for furin: application as an antipathogenic agent. Proc. Natl. Acad. Sci. U.S.A. 95, 7293-7298
39. Murthy, H. M., Judge, K., DeLucas, L. and Padmanabhan, R. (2000) Crystal structure of Dengue virus NS3 protease in complex with a Bowman-Birk inhibitor: implications for flaviviral polyprotein processing and drug design. J. Mol. Biol. 301, 759-767
40. Henrich, S., Lindberg, I., Bode, W. and Than, M. E. (2005) Proprotein convertase models based on the crystal structures of furin and kexin: explanation of their specificity. J. Mol. Biol. 345, 211-227
41. Comellas-Bigler, M., Maskos, K., Huber, R., Oyama, H., Oda, K. and Bode, W. (2004) 1.2 Å crystal structure of the serine carboxyl proteinase pro-kumamolisin; structure of an intact pro-subtilase. Structure 12, 1313-1323
42. Gallagher, T., Gilliland, G., Wang, L. and Bryan, P. (1995) The prosegment-subtilisin BPN' complex: crystal structure of a specific 'foldase'. Structure 3, 907-914
43. Tangrea, M. A., Alexander, P., Bryan, P. N., Eisenstein, E., Toedt, J. and Orban, J. (2001) Stability and global fold of the mouse prohormone convertase 1 pro-domain. Biochemistry 40, 5488-5495
44. Marie-Claire, C., Ruffet, E., Beaumont, A. and Roques, B. P. (1999) The prosequence of thermolysin acts as an intramolecular chaperone when expressed in trans with the mature sequence in Escherichia coli. J. Mol. Biol. 285, 1911-1915
45. Almog, O., Gallagher, T., Tordova, M., Hoskins, J., Bryan, P. and Gilliland, G. L. (1998) Crystal structure of calcium-independent subtilisin BPN' with restored thermal stability folded without the prodomain. Proteins 31, 21-32
46. Ruvinov, S., Wang, L., Ruan, B., Almog, O., Gilliland, G. L., Eisenstein, E. and Bryan, P. N. (1997) Engineering the independent folding of the subtilisin BPN' prodomain: analysis of two-state folding versus protein stability. Biochemistry 36, 10414-10421
47. Wang, L., Ruvinov, S., Strausberg, S., Gallagher, D. T., Gilliland, G. and Bryan, P. N. (1995) Prodomain mutations at the subtilisin interface: correlation of binding energy and the rate of catalyzed folding. Biochemistry 34, 15415-15420
48. Bryan, P., Wang, L., Hoskins, J., Ruvinov, S., Strausberg, S., Alexander, P., Almog, O., Gilliland, G. and Gallagher, T. (1995) Catalysis of a protein folding reaction: mechanistic implications of the 2.0 Å structure of the subtilisin-prodomain complex. Biochemistry 34, 10310-10318