Detection of ubiquitin-proteasome enzymatic activities in cells: Application of activity-based probes to inhibitor development

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1823, Issue 11, 2012, Pages 2029-2037

  Kramer, Holger B ^a   Nicholson, Benjamin ^c   Kessler, Benedikt M ^b   Altun, Mikael ^d  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c Progenra Inc   (United States)

^d KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Active site directed molecular probe; Deubiquitinating enzyme; Proteomics; Small molecular inhibitor; Ubiquitin; Ubiquitin specific protease

Indexed keywords

DEUBIQUITYLATING ENZYME; PHOSPHATASE; PROTEASOME; UBIQUITIN; UBIQUITIN CONJUGATING ENZYME; UNCLASSIFIED DRUG;

CELL ACTIVATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME INHIBITOR COMPLEX; ENZYME SPECIFICITY; MASS SPECTROMETRY; MOLECULAR PROBE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; REVIEW;

ANIMALS; DRUG DESIGN; HUMANS; MOLECULAR PROBES; PROTEASOME ENDOPEPTIDASE COMPLEX; UBIQUITIN;

EID: 84866992804     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2012.05.014     Document Type: Review

References (85)

1. Ciechanover A. The ubiquitin-proteasome pathway: on protein death and cell life. EMBO J. 1998, 17:7151-7160.
2. Amerik A.Y., Hochstrasser M. Mechanism and function of deubiquitinating enzymes. Biochim. Biophys. Acta, Mol. Cell Res. 2004, 1695:189-207.
3. Glickman M.H., Ciechanover A. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol. Rev. 2002, 82:373-428.
4. Rock K.L., Gramm C., Rothstein L., Clark K., Stein R., Dick L., Hwang D., Goldberg A.L. Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell 1994, 78:761-771.
5. Schwartz A.L., Ciechanover A. Targeting proteins for destruction by the ubiquitin system: implications for human pathobiology. Annu. Rev. Pharmacol. Toxicol. 2009, 49:73-96.
6. Lecker S.H., Goldberg A.L., Mitch W.E. Protein degradation by the ubiquitin-proteasome pathway in normal and disease states. J. Am. Soc. Nephrol. 2006, 17:1807-1819.
7. Hemelaar J., Galardy P.J., Borodovsky A., Kessler B.M., Ploegh H.L., Ovaa H. Chemistry-based functional proteomics: mechanism-based activity-profiling tools for ubiquitin and ubiquitin-like specific proteases. J. Proteome Res. 2004, 3:268-276.
8. Kessler B.M. Putting proteomics on target: activity-based profiling of ubiquitin and ubiquitin-like processing enzymes. Expert Rev. Proteomics 2006, 3:213-221.
9. Ovaa H. Active-site directed probes to report enzymatic action in the ubiquitin proteasome system. Nat. Rev. Cancer 2007, 7:613-620.
10. Verdoes M., Florea B.I., Van Der Marel G.A., Overkleeft H.S. Chemical tools to study the proteasome. Eur. J. Org. Chem. 2009, 3301-3313.
11. de Bettignies G., Coux O. Proteasome inhibitors: dozens of molecules and still counting. Biochimie 2010, 92:1530-1545.
12. Bogyo M., Shin S., McMaster J.S., Ploegh H.L. Substrate binding and sequence preference of the proteasome revealed by active-site-directed affinity probes. Chem. Biol. 1998, 5:307-320.
13. Heinemeyer W., Fischer M., Krimmer T., Stachon U., Wolf D.H. The active sites of the eukaryotic 20S proteasome and their involvement in subunit precursor processing. J. Biol. Chem. 1997, 272:25200-25209.
14. Griffin T.A., Nandi D., Cruz M., Fehling H.J., Van Kaer L., Monaco J.J., Colbert R.A. Immunoproteasome assembly: cooperative incorporation of interferon γ (IFN-γ)-inducible subunits. J. Exp. Med. 1998, 187:97-104.
15. Murata S., Sasaki K., Kishimoto T., Niwa S.I., Hayashi H., Takahama Y., Tanaka K. Regulation of CD8+ T cell development by thymus-specific proteasomes. Science 2007, 316:1349-1353.
16. Berkers C.R., Verdoes M., Lichtman E., Fiebiger E., Kessler B.M., Anderson K.C., Ploegh H.L., Ovaa H., Galardy P.J. Activity probe for in vivo profiling of the specificity of proteasome inhibitor bortezomib. Nat. Methods 2005, 2:357-362.
17. Sin N., Kyung B.K., Elofsson M., Meng L., Auth H., Kwok B.H.B., Crews C.M. Total synthesis of the potent proteasome inhibitor epoxomicin: a useful tool for understanding proteasome biology. Bioorg. Med. Chem. Lett. 1999, 9:2283-2288.
18. Kessler B.M., Tortorella D., Altun M., Kisselev A.F., Fiebiger E., Hekking B.G., Ploegh H.L., Overkleeft H.S. Extended peptide-based inhibitors efficiently target the proteasome and reveal overlapping specificities of the catalytic β-subunits. Chem. Biol. 2001, 8:913-929.
19. Berkers C.R., Van Leeuwen F.W.B., Groothuis T.A., Peperzak V., Van Tilburg E.W., Borst J., Neefjes J.J., Ovaa H. Profiling proteasome activity in tissue with fluorescent probes. Mol. Pharm. 2007, 4:739-748.
20. Verdoes M., Florea B.I., Menendez-Benito V., Maynard C.J., Witte M.D., van der Linden W.A., van den Nieuwendijk A.M.C.H., Hofmann T., Berkers C.R., van Leeuwen F.W.B., Groothuis T.A., Leeuwenburgh M.A., Ovaa H., Neefjes J.J., Filippov D.V., van der Marel G.A., Dantuma N.P., Overkleeft H.S. A fluorescent broad-spectrum proteasome inhibitor for labeling proteasomes in vitro and in vivo. Chem. Biol. 2006, 13:1217-1226.
21. Greenbaum D., Medzihradszky K.F., Burlingame A., Bogyo M. Epoxide electrophiles as activity-dependent cysteine protease profiling and discovery tools. Chem. Biol. 2000, 7:569-581.
22. Ovaa H., Van Swieten P.F., Kessler B.M., Leeuwenburgh M.A., Fiebiger E., Van den Nieuwendijk A.M.C.H., Galardy P.J., Van der Marel G.A., Ploegh H.L., Overkleeft H.S. Chemistry in living cells: detection of active proteasomes by a two-step labeling strategy. Angew. Chem. Int. Ed. 2003, 42:3626-3629.
23. Saxon E., Bertozzi C.R. Cell surface engineering by a modified Staudinger reaction. Science 2000, 287:2007-2010.
24. Tornoe C.W., Christensen C., Meldal M. Peptidotriazoles on solid phase: [1,2,3]-triazoles by regiospecific copper(I)-catalyzed 1,3-dipolar cycloadditions of terminal alkynes to azides. J. Org. Chem. 2002, 67:3057-3064.
25. Rostovtsev V.V., Green L.G., Fokin V.V., Sharpless K.B. A stepwise huisgen cycloaddition process: copper(I)-catalyzed regioselective "ligation" of azides and terminal alkynes. Angew. Chem. Int. Ed. 2002, 41:2596-2599.
26. Hasegawa M., Kinoshita K., Nishimura C., Matsumura U., Shionyu M., Ikeda S.i., Mizukami T. Affinity labeling of the proteasome by a belactosin A derived inhibitor. Bioorg. Med. Chem. Lett. 2008, 18:5668-5671.
27. Borodovsky A., Ovaa H., Kolli N., Gan-Erdene T., Wilkinson K.D., Ploegh H.L., Kessler B.M. Chemistry-based functional proteomics reveals novel members of the deubiquitinating enzyme family. Chem. Biol. 2002, 9:1149-1159.
28. Borodovsky A., Kessler B.M., Casagrande R., Overkleeft H.S., Wilkinson K.D., Ploegh H.L. A novel active site-directed probe specific for deubiquitylating enzymes reveals proteasome association of USP14. EMBO J. 2001, 20:5187-5196.
29. Ovaa H., Kessler B.M., Rolan U., Ploegh H.L., Masucci M.G. Activity-based ubiquitin-specific protease (USP), profiling of virus-infected and malignant human cells. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:2253-2258.
30. Hemelaar J., Borodovsky A., Kessler B.M., Reverter D., Cook J., Kolli N., Gan-Erdene T., Wilkinson K.D., Gill G., Lima C.D., Ploegh H.L., Ovaa H. Specific and covalent targeting of conjugating and deconjugating enzymes of ubiquitin-like proteins. Mol. Cell. Biol. 2004, 24:84-95.
31. Rolan U., Kobzeva V., Gasparjan N., Ovaa H., Winberg G., Kisseljov F., Masucci M.G. Activity profiling of deubiquitinating enzymes in cervical carcinoma biopsies and cell lines. Mol. Carcinog. 2006, 45:260-269.
32. Gredmark S., Schlieker C., Quesada V., Spooner E., Ploegh H.L. A functional ubiquitin-specific protease embedded in the large tegument protein (ORF64) of murine gammaherpesvirus 68 is active during the course of infection. J. Virol. 2007, 81:10300-10309.
33. Gredmark-Russ S., Isaacson M.K., Kattenhorn L., Cheung E.J., Watson N., Ploegh H.L. A gammaherpesvirus ubiquitin-specific protease is involved in the establishment of murine gammaherpesvirus 68 infection. J. Virol. 2009, 83:10644-10652.
34. Kattenhorn L.M., Korbel G.A., Kessler B.M., Spooner E., Ploegh H.L. A deubiquitinating enzyme encoded by HSV-1 belongs to a family of cysteine proteases that is conserved across the family Herpesviridae. Mol. Cell 2005, 19:547-557.
35. Wang J., Loveland A.N., Kattenhorn L.M., Ploegh H.L., Gibson W. High-molecular-weight protein (pUL48) of human cytomegalovirus is a competent deubiquitinating protease: mutant viruses altered in its active-site cysteine or histidine are viable. J. Virol. 2006, 80:6003-6012.
36. White R.R., Miyata S., Papa E., Spooner E., Gounaris K., Selkirk M.E., Artavanis-Tsakonas K. Characterisation of the trichinella spiralis deubiquitinating enzyme, TsUCH37, an evolutionarily conserved proteasome interaction partner. PLoS Negl. Trop. Dis. 2011, 5.
37. Artavanis-Tsakonas K., Misaghi S., Comeaux C.A., Catic A., Spooner E., Duraisingh M.T., Ploegh H.L. Identification by functional proteomics of a deubiquitinating/deNeddylating enzyme in Plasmodium falciparum. Mol. Microbiol. 2006, 61:1187-1195.
38. Catic A., Misaghi S., Korbel G.A., Ploegh H.L. ElaD, a deubiquitinating protease expressed by E. coli. PLoS One 2007, 2.
39. Misaghi S., Balsara Z.R., Catic A., Spooner E., Ploegh H.L., Starnbach M.N. Chlamydia trachomatis-derived deubiquitinating enzymes in mammalian cells during infection. Mol. Microbiol. 2006, 61:142-150.
40. Edelmann M.J., Kessler B.M. Ubiquitin and ubiquitin-like specific proteases targeted by infectious pathogens: emerging patterns and molecular principles. Biochim. Biophys. Acta, Mol. Basis Dis. 2008, 1782:809-816.
41. Isaacson M.K., Ploegh H.L. Ubiquitination, ubiquitin-like modifiers, and deubiquitination in viral infection. Cell Host Microbe 2009, 5:559-570.
42. Rytkanen A., Holden D.W. Bacterial interference of ubiquitination and deubiquitination. Cell Host Microbe 2007, 1:13-22.
43. Randow F., Lehner P.J. Viral avoidance and exploitation of the ubiquitin system. Nat. Cell Biol. 2009, 11:527-534.
44. Misaghi S., Galardy P.J., Meester W.J.N., Ovaa H., Ploegh H.L., Gaudet R. Structure of the ubiquitin hydrolase UCH-L3 complexed with a suicide substrate. J. Biol. Chem. 2005, 280:1512-1520.
45. Hu M., Li P., Li M., Li W., Yao T., Wu J.W., Gu W., Cohen R.E., Shi Y. Crystal structure of a UBP-family deubiquitinating enzyme in isolation and in complex with ubiquitin aldehyde. Cell 2002, 111:1041-1054.
46. Hu M., Li P., Song L., Jeffrey P.D., Chenova T.A., Wilkinson K.D., Cohen R.E., Shi Y. Structure and mechanisms of the proteasome-associated deubiquitinating enzyme USP14. EMBO J. 2005, 24:3747-3756.
47. Johnston S.C., Riddle S.M., Cohen R.E., Hill C.P. Structural basis for the specificity of ubiquitin C-terminal hydrolases. EMBO J. 1999, 18:3877-3887.
48. Akutsu M., Ye Y., Virdee S., Chin J.W., Komander D. Molecular basis for ubiquitin and ISG15 cross-reactivity in viral ovarian tumor domains. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:2228-2233.
49. Capodagli G.C., McKercher M.A., Baker E.A., Masters E.M., Brunzelle J.S., Pegan S.D. Structural analysis of a viral ovarian tumor domain protease from the Crimean-Congo hemorrhagic fever virus in complex with covalently bonded ubiquitin. J. Virol. 2011, 85:3621-3630.
50. James T.W., Frias-Staheli N., Bacik J.P., Levingston Macleod J.M., Khajehpour M., GarcÃa-Sastre A., Mark B.L. Structural basis for the removal of ubiquitin and interferon-stimulated gene 15 by a viral ovarian tumor domain-containing protease. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:2222-2227.
51. Altun M., Kramer H.B., Willems L.I., McDermott J.L., Leach C.A., Goldenberg S.J., Kumar K.G.S., Konietzny R., Fischer R., Kogan E., MacKeen M.M., McGouran J., Khoronenkova S.V., Parsons J.L., Dianov G.L., Nicholson B., Kessler B.M. Activity-based chemical proteomics accelerates inhibitor development for deubiquitylating enzymes. Chem. Biol. 2011, 18:1401-1412.
52. Love K.R., Pandya R.K., Spooner E., Ploegh H.L. Ubiquitin C-terminal electrophiles are activity-based probes for identification and mechanistic study of ubiquitin conjugating machinery. ACS Chem. Biol. 2009, 4:275-287.
53. Bogyo M. Screening for selective small molecule inhibitors of the proteasome using activity-based probes. Methods Enzymol. 2005, 399:609-622.
54. Greenbaum D.C., Arnold W.D., Lu F., Hayrapetian L., Baruch A., Krumrine J., Toba S., Chehade K., Brömme D., Kuntz I.D., Bogyo M. Small molecule affinity fingerprinting: a tool for enzyme family subclassification, target identification, and inhibitor design. Chem. Biol. 2002, 9:1085-1094.
55. Leung D., Hardouin C., Boger D.L., Cravatt B.F. Discovering potent and selective reversible inhibitors of enzymes in complex proteomes. Nat. Biotechnol. 2003, 21:687-691.
56. Kapuria V., Peterson L.F., Showalter H.D.H., Kirchhoff P.D., Talpaz M., Donato N.J. Protein cross-linking as a novel mechanism of action of a ubiquitin-activating enzyme inhibitor with anti-tumor activity. Biochem. Pharmacol. 2011, 82:341-349.
57. Altun M., Galardy P.J., Shringarpure R., Hideshima T., LeBlanc R., Anderson K.C., Ploegh H.L., Kessler B.M. Effects of PS-341 on the activity and composition of proteasomes in multiple myeloma cells. Cancer Res. 2005, 65:7896-7901.
58. Richardson P.G., Barlogie B., Berenson J., Singhal S., Jagannath S., Irwin D., Rajkumar S.V., Srkalovic G., Alsina M., Alexanian R., Siegel D., Orlowski R.Z., Kuter D., Limentani S.A., Lee S., Hideshima T., Esseltine D.L., Kauffman M., Adams J., Schenkein D.P., Anderson K.C. A phase 2 study of Bortezomib in relapsed, refractory myeloma. N. Engl. J. Med. 2003, 348:2609-2617.
59. Chauhan D., Catley L., Li G., Podar K., Hideshima T., Velankar M., Mitsiades C., Mitsiades N., Yasui H., Letai A., Ovaa H., Berkers C., Nicholson B., Chao T.H., Neuteboom S.T.C., Richardson P., Palladino M.A., Anderson K.C. A novel orally active proteasome inhibitor induces apoptosis in multiple myeloma cells with mechanisms distinct from Bortezomib. Cancer Cell 2005, 8:407-419.
60. Crawford L.J.A., Walker B., Ovaa H., Chauhan D., Anderson K.C., Morris T.C.M., Irvine A.E. Comparative selectivity and specificity of the proteasome inhibitors BzLLLCOCHO, PS-341, and MG-132. Cancer Res. 2006, 66:6379-6386.
61. Ho Y.K., Bargagna-Mohan P., Wehenkel M., Mohan R., Kim K.B. LMP2-specific inhibitors: chemical genetic tools for proteasome biology. Chem. Biol. 2007, 14:419-430.
62. Kapuria V., Peterson L.F., Fang D., Bornmann W.G., Talpaz M., Donato N.J. Deubiquitinase inhibition by small-molecule WP1130 triggers aggresome formation and tumor cell apoptosis. Cancer Res. 2010, 70:9265-9276.
63. Nicholson B., Suresh Kumar K.G. The multifaceted roles of USP7: new therapeutic opportunities. Cell Biochem. Biophys. 2011, 60:61-68.
64. Parsons J.L., Dianova I.I., Khoronenkova S.V., Edelmann M.J., Kessler B.M., Dianov G.L. USP47 is a deubiquitylating enzyme that regulates base excision repair by controlling steady-state levels of DNA polymerase beta. Mol. Cell 2011, 41:609-615.
65. Reverdy C., Conrath S., Lopez R., Planquette C., Atmanene C., Collura V., Harpon J., Battaglia V., Vivat V., Sippl W., Colland F. Discovery of specific inhibitors of human USP7/HAUSP deubiquitinating enzyme. Chem. Biol. 2012, 19:467-477.
66. D'Arcy P., Brnjic S., Olofsson M.H., Fryknas M., Lindsten K., De Cesare M., Perego P., Sadeghi B., Hassan M., Larsson R., Linder S. Inhibition of proteasome deubiquitinating activity as a new cancer therapy. Nat. Med. 2011.
67. Ratia K., Pegan S., Takayama J., Sleeman K., Coughlin M., Baliji S., Chaudhuri R., Fu W., Prabhakar B.S., Johnson M.E., Baker S.C., Ghosh A.K., Mesecar A.D. A noncovalent class of papain-like protease/deubiquitinase inhibitors blocks SARS virus replication. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:16119-16124.
68. Patricelli M.P., Szardenings A.K., Liyanage M., Nomanbhoy T.K., Wu M., Weissig H., Aban A., Chun D., Tanner S., Kozarich J.W. Functional interrogation of the kinome using nucleotide acyl phosphates. Biochemistry 2007, 46:350-358.
69. Liu Y., Shreder K.R., Gai W., Corral S., Ferris D.K., Rosenblum J.S. Wortmannin, a widely used phosphoinositide 3-kinase inhibitor, also potently inhibits mammalian polo-like kinase. Chem. Biol. 2005, 12:99-107.
70. Yee M.C., Fas S.C., Stohlmeyer M.M., Wandless T.J., Cimprich K.A. A cell-permeable, activity-based probe for protein and lipid kinases. J. Biol. Chem. 2005, 280:29053-29059.
71. Liu Y., Jiang N., Wu J., Dai W., Rosenblum J.S. Polo-like kinases inhibited by Wortmannin: labeling site and downstream effects. J. Biol. Chem. 2007, 282:2505-2511.
72. Liu Y., Wu J., Weissig H., Betancort J.M., Gai W.Z., Leventhal P.S., Patricelli M.P., Samii B., Szardenings A.K., Shreder K.R., Kozarich J.W. Design and synthesis of AX4697, a bisindolylmaleimide exo-affinity probe that labels protein kinase C alpha and beta. Bioorg. Med. Chem. Lett. 2008, 18:5955-5958.
73. Kalesh K.A., Sim D.S.B., Wang J., Liu K., Lin Q., Yao S.Q. Small molecule probes that target Abl kinase. Chem. Commun. 2010, 46:1118-1120.
74. Fischer J.J., Graebner O.Y., Dalhoff C., Michaelis S., Schrey A.K., Ungewiss J., Andrich K., Jeske D., Kroll F., Glinski M., Sefkow M., Dreger M., Koester H. Comprehensive identification of staurosporine-binding kinases in the hepatocyte cell line HepG2 using capture compound mass spectrometry (CCMS). J. Proteome Res. 2010, 9:806-817.
75. Shi H., Cheng X., Sze S.K., Yao S.Q. Proteome profiling reveals potential cellular targets of staurosporine using a clickable cell-permeable probe. Chem. Commun. 2011, 47:11306-11308.
76. Lo L.C., Chiang Y.L., Kuo C.H., Liao H.K., Chen Y.J., Lin J.J. Study of the preferred modification sites of the quinone methide intermediate resulting from the latent trapping device of the activity probes for hydrolases. Biochem. Biophys. Res. Commun. 2004, 326:30-35.
77. Lo L.C., Pang T.L., Kuo C.H., Chiang Y.L., Wang H.Y., Lin J.J. Design and synthesis of class-selective activity probes for protein tyrosine phosphatases. J. Proteome Res. 2002, 1:35-40.
78. Zhu Q., Huang X., Chen G.Y.J., Yao S.Q. Activity-based fluorescent probes that target phosphatases. Tetrahedron Lett. 2003, 44:2669-2672.
79. Kumar S., Zhou B., Liang F., Wang W.Q., Huang Z., Zhang Z.Y. Activity-based probes for protein tyrosine phosphatases. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:7943-7948.
80. Kalesh K.A., Tan L.P., Lu K., Gao L., Wang J., Yao S.Q. Peptide-based activity-based probes (ABPs) for target-specific profiling of protein tyrosine phosphatases (PTPs). Chem. Commun. 2010, 46:589-591.
81. Kumar S., Zhou B., Liang F., Yang H., Wang W.Q., Zhang Z.Y. Global analysis of protein tyrosine phosphatase activity with ultra-sensitive fluorescent probes. J. Proteome Res. 2006, 5:1898-1905.
82. Liu S., Zhou B., Yang H., He Y., Jiang Z.X., Kumar S., Wu L., Zhang Z.Y. Aryl vinyl sulfonates and sulfones as active site-directed and mechanism-based probes for protein tyrosine phosphatases. J. Am. Chem. Soc. 2008, 130:8251-8260.
83. Hu M., Li L., Wu H., Su Y., Yang P.Y., Uttamchandani M., Xu Q.H., Yao S.Q. Multicolor, one- and two-photon imaging of enzymatic activities in live cells with fluorescently quenched activity-based probes (qABPs). J. Am. Chem. Soc. 2011, 133:12009-12020.
84. Shreder K.R., Liu Y., Nomanhboy T., Fuller S.R., Wong M.S., Gai W.Z., Wu J., Leventhal P.S., Lill J.R., Corral S. Design and synthesis of AX7574: a microcystin-derived, fluorescent probe for serine/threonine phosphatases. Bioconjug. Chem. 2004, 15:790-798.
85. Patricelli M.P., Nomanbhoy T.K., Wu J., Brown H., Zhou D., Zhang J., Jagannathan S., Aban A., Okerberg E., Herring C., Nordin B., Weissig H., Yang Q., Lee J.D., Gray N.S., Kozarich J.W. In situ kinase profiling reveals functionally relevant properties of native kinases. Chem. Biol. 2011, 18:699-710.