Three-dimensional structure of a monomeric form of a retroviral protease

Journal of Molecular Biology

Volumn 333, Issue 4, 2003, Pages 771-780

  Veverka, V áclav ^a,c   Bauerová, Helena ^b   Zábranský, Aleš ^b   Lang, Jan ^a   Ruml, Tomáš ^a,b   Pichová, Iva ^b   Hrabal, Richard ^a  

^a INSTITUTE OF CHEMICAL TECHNOLOGY   (Czech Republic)

^b INSTITUTE OF ORGANIC CHEMISTRY AND BIOCHEMISTRY   (Czech Republic)

^c UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

M PMV; Monomer; NMR spectroscopy; Protein structure; Retroviral protease

Indexed keywords

ALANINE; ASPARAGINE; CYSTEINE; MONOMER; MUTANT PROTEIN; PROTEINASE; VIRUS ENZYME;

ARTICLE; CYTOPLASM; ENZYME STRUCTURE; MASON PFIZER MONKEY VIRUS; MOLECULAR WEIGHT; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OXIDATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN MOTIF; RETROVIRUS; VIRUS CAPSID;

MASON-PFIZER MONKEY VIRUS; PAPAYA MOSAIC VIRUS;

EID: 0142011069     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2003.08.049     Document Type: Article

References (46)

1. Sonigo P., Barker C., Hunter E., Wain-Hobson S. Nucleotide sequence of Mason-Pfizer monkey virus: an immunosuppressive D-type retrovirus. Cell. 45:1986;375-385.
2. Zabransky A., Andreansky M., Hruskova-Heidingsfeldova O., Havlicek V., Hunter E., Ruml T., Pichova I. Three active forms of aspartic proteinase from Mason-Pfizer monkey virus. Virology. 245:1998;250-256.
3. Hruskova-Heidingsfeldova O., Andreansky M., Fabry M., Blaha I., Strop P., Hunter E. Cloning, bacterial expression, and characterization of the Mason-Pfizer monkey virus proteinase. J. Biol. Chem. 270:1995;15053-15058.
4. Vogt V.M. Proteolytic processing and particle maturation. Curr. Top. Microbiol. Immunol. 214:1996;95-131.
5. Wlodawer A., Gustchina A. Structural and biochemical studies of retroviral proteases. Biochim. Biophys. Acta. 1477:2000;16-34.
6. Strisovsky K., Tessmer U., Langner J., Konvalinka J., Krausslich H.G. Systematic mutational analysis of the active-site threonine of HIV-1 proteinase: rethinking the "fireman's grip" hypothesis. Protein Sci. 9:2000;1631-1641.
7. Todd M.J., Semo N., Freire E. The structural stability of the HIV-1 protease. J. Mol. Biol. 283:1998;475-488.
8. Louis J.M., Clore G.M., Gronenborn A.M. Autoprocessing of HIV-1 protease is tightly coupled to protein folding [In Process Citation]. Nature Struct. Biol. 6:1999;868-875.
9. Schatz G.W., Reinking J., Zippin J., Nicholson L.K., Vogt V.M. Importance of the N-terminus of Rous sarcoma virus protease for structure and enzymatic function. J. Virol. 75:2001;4761-4770.
10. Ishima R., Ghirlando R., Tozser J., Gronenborn A.M., Torchia D.A., Louis J.M. Folded monomer of HIV-1 protease. J. Biol. Chem. 276:2001;49110-49116.
11. Karlstrom A.R., Levine R.L. Copper inhibits the protease from human immunodeficiency virus 1 by both cysteine-dependent and cysteine-independent mechanisms. Proc. Natl Acad. Sci. USA. 88:1991;5552-5556.
12. Karlstrom A.R., Shames B.D., Levine R.L. Reactivity of cysteine residues in the protease from human immunodeficiency virus: identification of a surface-exposed region which affects enzyme function. Arch. Biochem. Biophys. 304:1993;163-169.
13. Meek T.D., Dayton B.D., Metcalf B.W., Dreyer G.B., Strickler J.E., Gorniak J.G., et al. Human immunodeficiency virus 1 protease expressed in Escherichia coli behaves as a dimeric aspartic protease. Proc. Natl Acad. Sci. USA. 86:1989;1841-1845.
14. Davis D.A., Dorsey K., Wingfield P.T., Stahl S.J., Kaufman J., Fales H.M., Levine R.L. Regulation of HIV-1 protease activity through cysteine modification. Biochemistry. 35:1996;2482-2488.
15. Davis D.A., Yusa K., Gillim L.A., Newcomb F.M., Mitsuya H., Yarchoan R. Conserved cysteines of the human immunodeficiency virus type 1 protease are involved in regulation of polyprotein processing and viral maturation of immature virions. J. Virol. 73:1999;1156-1164.
16. Davis D.A., Newcomb F.M., Moskovitz J., Wingfield P.T., Stahl S.J., Kaufman J., et al. HIV-2 protease is inactivated after oxidation at the dimer interface and activity can be partly restored with methionine sulphoxide reductase. Biochem. J. 346 Pt 2:2000;305-311.
17. Campbell S., Oshima M., Mirro J., Nagashima K., Rein A. Reversal by dithiothreitol treatment of the block in murine leukemia virus maturation induced by disulfide cross-liniking. J. Virol. 76:2002;10050-10055.
18. Davis D.A., Brown C.A., Newcomb F.M., Boja E.S., Fales H.M., Kaufman J., et al. Reversible oxidative modification as a mechanism for regulating retroviral protease dimerization and activation. J. Virol. 77:2003;3319-3325.
19. Laco G.S., Schalk-Hihi C., Lubkowski J., Morris G., Zdanov A., Olson A., et al. Crystal structures of the inactive D30N mutant of feline immunodeficiency virus protease complexed with a substrate and an inhibitor. Biochemistry. 36:1997;10696-10708.
20. Prabu-Jeyabalan M., Nalivaika E., Schiffer C.A. How does a symmetric dimer recognize an asymmetric substrate? A substrate complex of HIV-1 protease. J. Mol. Biol. 301:2000;1207-1220.
21. Veverka V., Bauerova H., Zabransky A., Pichova I., Hrabal R. Backbone resonance assignment of protease from Mason-Pfizer monkey virus. J. Biomol. NMR. 20:2001;291-292.
22. Nilges M., Macias M.J., O'Donoghue S.I., Oschkinat H. Automated NOESY interpretation with ambiguous distance restraints: the defined NMR solution structure of the pleckstrin homology domain from b-spectrin. J. Mol. Biol. 269:1997;408-422.
23. Cornilescu G., Delaglio F., Bax A. Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR. 13:1999;289-302.
24. Miller M., Jaskolski M., Rao J.K.M., Leis J., Wlodawer A. Crystal structure of a retroviral protease proves relationship to aspartic protease family. Nature. 337:1989;576-579.
25. Yamazaki T., Hinck A.P., Wang Y.X., Nicholson L.K., Torchia D.A., Wingfield P.T., et al. Three-dimensional solution structure of the HIV-1 protease complexed with DMP323, a novel cyclic urea-type inhibitor, determined by nuclear magnetic resonance spectroscopy. Protein Sci. 5:1996;495-506.
26. Louis J.M., Ishima R., Nesheiwat I., Pannell L.K., Lynch S.M., Torchia D.A., Gronenborn A.M. Revisiting monomeric HIV-1 protease. Characterization and redesign for improved properties. J. Biol. Chem. 278:2003;6085-6092.
27. Nicholson L.K., Yamazaki T., Torchia D.A., Grzesiek S., Bax A., Stahl S.J., et al. Flexibility and function in HIV-1 protease. Nature Struct. Biol. 2:1995;274-280.
28. Holzman T.F., Kohlbrenner W.E., Weigl D., Rittenhouse J., Kempf D., Erickson J. Inhibitor stabilization of human immunodeficiency virus type-2 proteinase dimer formation. J. Biol. Chem. 266:1991;19217-19220.
29. Grant S.K., Deckman I.C., Culp J.S., Minnich M.D., Brooks I.S., Hensley P., et al. Use of protein unfolding studies to determine the conformational and dimeric stabilities of HIV-1 and SIV proteases. Biochemistry. 31:1992;9491-9501.
30. Wondrak E.M., Nashed N.T., Haber M.T., Jerina D.M., Louis J.M. A transient precursor of the HIV-1 protease. Isolation, characterization, and kinetics of maturation. J. Biol. Chem. 271:1996;4477-4481.
31. Wondrak E.M., Louis J.M. Influence of flanking sequences on the dimer stability of human immunodeficiency virus type 1 protease. Biochemistry. 35:1996;12957-12962.
32. Ishima R., Freedberg D.I., Wang Y.X., Louis J.M., Torchia D.A. Flap opening and dimer-interface flexibility in the free and inhibitor-bound HIV protease, and their implications for function. Struct. Fold. Des. 7:1999;1047-1055.
33. Parker S.D., Hunter E. Activation of the Mason-Pfizer monkey virus protease within immature capsids in vitro. Proc. Natl Acad. Sci. USA. 98:2001;14631-14636.
34. Rhee S.S., Hunter E. Amino acid substitutions within the matrix protein of type D retroviruses affect assembly, transport and membrane association of a capsid. EMBO J. 10:1991;535-546.
35. Rhee S.S., Hunter E. A single amino acid substitutiton within the matrix protein of a type D retrovirus converts its morphogenesis to that of a type C retrovirus. Cell. 63:1990;77-86.
36. Sommerfelt M.A., Petteway S.R., Dreyer G.B., Hunter E. Effect of retroviral proteinase inhibitors on Mason-Pfizer monkey virus maturation and transmembrane glycoprotein cleavage. J. Virol. 66:1992;4220-4227.
37. Andreansky M., Hunter E. Phagemid pSIT permits efficient in vitro mutagenesis and tightly controlled expression in E. coli. Biotechniques. 16:1994;626-628. 630-633.
38. Delaglio F., Grzesiek S., Vuister G.W., Zhu G., Pfeifer J., Bax A. NMRPipe: a multidimensional spectral processing system based on Unix pipes. J. Biomol. NMR. 6:1995;277-293.
39. Johnson B.A., Blevins R.A. A computer program for visualization and analysis of NMR data. J. Biomol. NMR. 4:1994;603-614.
40. Lipari G., Szabo A. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 2. Analysis of experimental results. J. Am. Chem. Soc. 104:1982;4559-4570.
41. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallog. D. Biol. Crystallog. 54 (Pt 5):1998;905-921.
42. Koradi R., Billeter M., Wuthrich K. Molmol: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14:1996;51-55.
43. Laskowski R.A., Rullmann J.A.C., MacArthur M.W., Kaptein R., Thornton J.M. Aqua and Procheck-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR. 8:1996;477-486.
44. Laue T.M., Shah B.D., Ridgeway T.M., Pelletier S.L. Analytical Ultracentrifugation in Biochemistry and Polymer Science. 1992;The Royal Society of Chemistry, Cambridge. pp 90-125.
45. Wlodawer A., Miller M., Jaskolski M., Sathyanarayana B.K., Baldwin E., Weber I.T., et al. Conserved folding in retroviral proteases: crystal structure of a synthetic HIV-1 protease. Science. 245:1989;616-621.
46. Shindyalov I.N., Bourne P.E. Protein structure alignment by incremental combinatorial extension (CE) of the optimal path. Protein Eng. 11:1998;739-747.