A catalogue of putative HIV-1 protease host cell substrates

Biological Chemistry

Volumn 393, Issue 9, 2012, Pages 915-931

  Impens, Francis ^a,b   Timmerman, Evy ^a,b   Staes, An ^a,b   Moens, Kathleen ^a,b   Ariën, Kevin K ^c   Verhasselt, Bruno ^c   Vandekerckhove, Joël ^a,b   Gevaert, Kris ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c GHENT UNIVERSITY HOSPITAL   (Belgium)

Author keywords

AIDS; COFRADIC; Positional proteomics; Protease degradomics; Protein neo N termini; Subsite cooperativity

Indexed keywords

HUMAN IMMUNODEFICIENCY VIRUS PROTEINASE; PROTEOME;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; CONFERENCE PAPER; ENZYME SPECIFICITY; ENZYME SUBSTRATE; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN MOTIF; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEOMICS; SEQUENCE ANALYSIS; UNINDEXED SEQUENCE;

AMINO ACID SEQUENCE; HIV PROTEASE; HIV-1; HUMANS; JURKAT CELLS; SUBSTRATE SPECIFICITY;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84869483961     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/hsz-2012-0168     Document Type: Conference Paper

References (44)

1. Barsnes, H., Vizcaino, J.A., Eidhammer, I., and Martens, L. (2009). PRIDE Converter: making proteomics data-sharing easy. Nat. Biotechnol. 27, 598-599.
2. Beck, Z.Q., Hervio, L., Dawson, P.E., Elder, J.H., and Madison, E.L. (2000). Identifi cation of effi ciently cleaved substrates for HIV-1 protease using a phage display library and use in inhibitor development. Virology 274, 391-401.
3. Beck, Z.Q., Morris, G.M., and Elder, J.H. (2002). Defi ning HIV-1 protease substrate selectivity. Curr. Drug Targets Infect. Disord. 2, 37-50.
4. Becker-Pauly, C., Barre, O., Schilling, O., Auf dem Keller, U., Ohler, A., Broder, C., Schutte, A., Kappelhoff, R., Stocker, W., and Overall, C.M. (2011). Proteomic analyses reveal an acidic prime side specifi city for the astacin metalloprotease family refl ected by physiological substrates. Mol. Cell Proteomics 10, M111.009233.
5. Castello, A., Franco, D., Moral-Lopez, P., Berlanga, J.J., Alvarez, E., Wimmer, E., and Carrasco, L. (2009). HIV- 1 protease inhibits Cap- and poly(A)-dependent translation upon eIF4GI and PABP cleavage. PLoS One 4, e7997.
6. Colaert, N., Helsens, K., Martens, L., Vandekerckhove, J., and Gevaert, K. (2009). Improved visualization of protein consensus sequences by iceLogo. Nat. Methods 6, 786-787.
7. Demon, D., Van Damme, P., Vanden Berghe, T., Deceuninck, A., Van Durme, J., Verspurten, J., Helsens, K., Impens, F., Wejda, M., Schymkowitz, J., et al. (2009). Proteome-wide substrate analysis indicates substrate exclusion as a mechanism to generate caspase-7 versus caspase-3 specifi city. Mol. Cell Proteomics 8, 2700-2714.
8. Drag, M. and Salvesen, G.S. (2010). Emerging principles in proteasebased drug discovery. Nat. Rev. Drug Discov. 9, 690-701.
9. Freed, E.O. (2001). HIV-1 replication. Somat. Cell Mol. Genet. 26, 13-33.
10. Fu, W., Sanders-Beer, B.E., Katz, K.S., Maglott, D.R., Pruitt, K.D., and Ptak, R.G. (2009). Human immunodefi ciency virus type 1, human protein interaction database at NCBI. Nucleic Acids Res. 37, D417-422.
11. Fuller-Pace, F.V. and Moore, H.C. (2011). RNA helicases p68 and p72: multifunctional proteins with important implications for cancer development. Future Oncol. 7, 239-251.
12. Gevaert, K., Goethals, M., Martens, L., Van Damme, J., Staes, A., Thomas, G.R., and Vandekerckhove, J. (2003). Exploring proteomes and analyzing protein processing by mass spectrometric identifi cation of sorted N-terminal peptides. Nat. Biotechnol. 21, 566-569.
13. Ghesquiere, B., Goethals, M., Van Damme, J., Staes, A., Timmerman, E., Vandekerckhove, J., and Gevaert, K. (2006). Improved tandem mass spectrometric characterization of 3-nitrotyrosine sites in peptides. Rapid Commun. Mass Spectrom. 20, 2885-2893.
14. Helsens, K., Colaert, N., Barsnes, H., Muth, T., Flikka, K., Staes, A., Timmerman, E., Wortelkamp, S., Sickmann, A., Vandekerckhove, J., et al. (2010). ms-lims, a simple yet powerful open source laboratory information management system for MS-driven proteomics. Proteomics 10, 1261-1264.
15. Impens, F., Colaert, N., Helsens, K., Ghesquiere, B., Timmerman, E., De Bock, P.J., Chain, B.M., Vandekerckhove, J., and Gevaert, K. (2010a). A quantitative proteomics design for systematic identifi cation of protease cleavage events. Mol. Cell Proteomics 9, 2327-2333.
16. Impens, F., Colaert, N., Helsens, K., Plasman, K., Van Damme, P., Vandekerckhove, J., and Gevaert, K. (2010b). MS-driven protease substrate degradomics. Proteomics 10, 1284-1296.
17. Jacob, R.J. and Cramer, R. (2006). PIGOK: linking protein identity to gene ontology and function. J. Proteome Res. 5, 3429-3432.
18. Jager, S., Cimermancic, P., Gulbahce, N., Johnson, J.R., McGovern, K.E., Clarke, S.C., Shales, M., Mercenne, G., Pache, L., Li, K., et al. (2012). Global landscape of HIV-human protein complexes. Nature 481, 365-370.
19. Jensen, L.J., Kuhn, M., Stark, M., Chaffron, S., Creevey, C., Muller, J., Doerks, T., Julien, P., Roth, A., Simonovic, M., et al. (2009). STRING 8 - a global view on proteins and their functional interactions in 630 organisms. Nucleic Acids Res. 37, D412-416.
20. Kall, L., Storey, J.D., MacCoss, M.J., and Noble, W.S. (2008). Assigning signifi cance to peptides identifi ed by tandem mass spectrometry using decoy databases. J. Proteome Res. 7, 29-34.
21. Kohl, N.E., Emini, E.A., Schleif, W.A., Davis, L.J., Heimbach, J.C., Dixon, R.A., Scolnick, E.M., and Sigal, I.S. (1988). Active human immunodefi ciency virus protease is required for viral infectivity. Proc. Natl. Acad. Sci. USA 85, 4686-4690.
22. Lee, S.K., Potempa, M., Kolli, M., Ozen, A., Schiffer, C., and Swanstrom, R. (2012). Context surrounding processing sites is crucial in determining cleavage rate of a subset of the processing sites in the HIV-1 Gag and Gag-Pro-Pol precursors by the viral protease. J. Biol. Chem. 287, 13279-13290.
23. Liu, H., Sadygov, R.G., and Yates, J.R. 3rd. (2004). A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal. Chem. 76, 4193-4201.
24. Lopez-Otin, C. and Overall, C.M. (2002). Protease degradomics: a new challenge for proteomics. Nat. Rev. Mol. Cell Biol. 3, 509-519.
25. Naji, S., Ambrus, G., Cimermancic, P., Reyes, J.R., Johnson, J.R., Filbrandt, R., Huber, M.D., Vesely, P., Krogan, N.J., Yates, J.R., 3rd, et al. (2012). Host cell interactome of HIV-1 Rev includes RNA helicases involved in multiple facets of virus production. Mol. Cell Proteomics 11, M111.015313.
26. Ng, N.M., Pike, R.N., and Boyd, S.E. (2009). Subsite cooperativity in protease specifi city. Biol. Chem. 390, 401-407.
27. Nie, Z., Phenix, B.N., Lum, J.J., Alam, A., Lynch, D.H., Beckett, B., Krammer, P.H., Sekaly, R.P., and Badley, A.D. (2002). HIV-1 protease processes procaspase 8 to cause mitochondrial release of cytochrome c, caspase cleavage and nuclear fragmentation. Cell Death Differ. 9, 1172-1184.
28. Nie, Z., Bren, G.D., Vlahakis, S.R., Schimnich, A.A., Brenchley, J.M., Trushin, S.A., Warren, S., Schnepple, D.J., Kovacs, C.M., Loutfy, M.R., et al. (2007). Human immunodefi ciency virus type 1 protease cleaves procaspase 8 in vivo. J. Virol. 81, 6947-6956.
29. Nie, Z., Bren, G.D., Rizza, S.A., and Badley, A.D. (2008). HIV protease cleavage of procaspase 8 is necessary for death of HIVinfected cells. Open Virol. J. 2, 1-7.
30. Ong, S.E., Blagoev, B., Kratchmarova, I., Kristensen, D.B., Steen, H., Pandey, A., and Mann, M. (2002). Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell Proteomics 1, 376-386.
31. Ozen, A., Haliloglu, T., and Schiffer, C.A. (2011). Dynamics of preferential substrate recognition in HIV-1 protease: redefi ning the substrate envelope. J. Mol. Biol. 410, 726-744.
32. Prabu-Jeyabalan, M., Nalivaika, E., and Schiffer, C.A. (2002). Substrate shape determines specifi city of recognition for HIV-1 protease: analysis of crystal structures of six substrate complexes. Structure 10, 369-381.
33. Ridky, T.W., Cameron, C.E., Cameron, J., Leis, J., Copeland, T., Wlodawer, A., Weber, I.T. and Harrison, R.W. (1996). Human immunodefi ciency virus, type 1 protease substrate specifi city is limited by interactions between substrate amino acids bound in adjacent enzyme subsites. J. Biol. Chem. 271, 4709-4717.
34. Schilling, O. and Overall, C.M. (2008). Proteome-derived, databasesearchable peptide libraries for identifying protease cleavage sites. Nat. Biotechnol. 26, 685-694.
35. Shoeman, R.L., Honer, B., Stoller, T.J., Kesselmeier, C., Miedel, M.C., Traub, P., and Graves, M.C. (1990). Human immunodefi ciency virus type 1 protease cleaves the intermediate fi lament proteins vimentin, desmin, and glial fi brillary acidic protein. Proc. Natl. Acad. Sci. USA 87, 6336-6340.
36. Staes, A., Van Damme, P., Helsens, K., Demol, H., Vandekerckhove, J., and Gevaert, K. (2008). Improved recovery of proteome-informative, protein N-terminal peptides by combined fractional diagonal chromatography (COFRADIC). Proteomics 8, 1362-1370.
37. Staes, A., Impens, F., Van Damme, P., Ruttens, B., Goethals, M., Demol, H., Timmerman, E., Vandekerckhove, J., and Gevaert, K. (2011). Selecting protein N-terminal peptides by combined fractional diagonal chromatography. Nat. Protoc. 6, 1130-1141.
38. Tomasselli, A.G., Hui, J.O., Adams, L., Chosay, J., Lowery, D., Greenberg, B., Yem, A., Deibel, M.R., Zurcher-Neely, H., and Heinrikson, R.L. (1991). Actin, troponin C, Alzheimer amyloid precursor protein and pro-interleukin 1 beta as substrates of the protease from human immunodefi ciency virus. J. Biol. Chem. 266, 14548-14553.
39. Tozser, J. and Oroszlan, S. (2003). Proteolytic events of HIV-1 replication as targets for therapeutic intervention. Curr. Pharm. Des. 9, 1803-1815.
40. Tozser, J., Bagossi, P., Weber, I.T., Louis, J.M., Copeland, T.D., and Oroszlan, S. (1997). Studies on the symmetry and sequence context dependence of the HIV-1 proteinase specifi city. J. Biol. Chem. 272, 16807-16814.
41. Van Damme, P., Martens, L., Van Damme, J., Hugelier, K., Staes, A., Vandekerckhove, J., and Gevaert, K. (2005). Caspase-specifi c and nonspecifi c in vivo protein processing during Fas-induced apoptosis. Nat. Methods 2, 771-777.
42. Van Damme, P., Impens, F., Vandekerckhove, J., and Gevaert, K. (2008). Protein processing characterized by a gel-free proteomics approach. Methods Mol. Biol. 484, 245-262.
43. Van Damme, P., Maurer-Stroh, S., Plasman, K., Van Durme, J., Colaert, N., Timmerman, E., De Bock, P.J., Goethals, M., Rousseau, F., Schymkowitz, J., et al. (2009). Analysis of protein processing by N-terminal proteomics reveals novel speciesspecifi c substrate determinants of granzyme B orthologs. Mol. Cell Proteomics 8, 258-272.
44. Wondrak, E.M., Louis, J.M., and Oroszlan, S. (1991). The effect of salt on the Michaelis Menten constant of the HIV-1 protease correlates with the Hofmeister series. FEBS Lett. 280, 344-346.