Evaluation of selected binding domains for the analysis of ubiquitinated proteomes

Journal of the American Society for Mass Spectrometry

Volumn 24, Issue 8, 2013, Pages 1214-1223

  Nakayasu, Ernesto S ^a   Ansong, Charles ^a   Brown, Joseph N ^a   Yang, Feng ^a   Lopez Ferrer, Daniel ^a,b   Qian, Wei Jun ^a   Smith, Richard D ^a   Adkins, Joshua N ^a  

^a PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

^b Caprion Proteomics US   (United States)

Author keywords

Affinity purification; Mass spectrometry; Post translation modification; Proteomics; Ubiquitination

Indexed keywords

AFFINITY PURIFICATION; BACTERIAL PATHOGENS; POST-TRANSLATION MODIFICATION; POST-TRANSLATIONAL MODIFICATIONS; PROTEOMICS; UBIQUITINATED PROTEINS; UBIQUITINATION; WESTERN-BLOT ANALYSIS;

AMINO ACIDS; ANTIGEN-ANTIBODY REACTIONS; ENZYME ACTIVITY; MASS SPECTROMETRY; MOLECULAR BIOLOGY; MONOCLONAL ANTIBODIES; PURIFICATION;

PROTEINS;

AMINO TERMINAL TELOPEPTIDE; LYSINE; MONOCLONAL ANTIBODY; PROTEIN DSK2; PROTEOME; UBIQUILIN 1; UBIQUITIN; UBIQUITINATED PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; BINDING AFFINITY; CONTROLLED STUDY; ENZYME ACTIVITY; MOLECULAR EVOLUTION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION; PROTEOMICS; REVIEW; UBIQUITINATION;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, MONOCLONAL; BLOTTING, WESTERN; CELL CYCLE PROTEINS; CELL LINE; CHROMATOGRAPHY, AFFINITY; ELECTROPHORESIS, POLYACRYLAMIDE GEL; HYDROLYSIS; IMMUNOCHEMISTRY; INDICATORS AND REAGENTS; INFLAMMATION; MACROPHAGES; MICE; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEOME; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; UBIQUITINATED PROTEINS; UBIQUITINS;

EID: 84880767172     PISSN: 10440305     EISSN: 18791123     Source Type: Journal    
DOI: 10.1007/s13361-013-0619-8     Document Type: Review

References (59)

1. Hershko, A.; Ciechanover, A.: The ubiquitin system. Annu. Rev. Biochem. 67, 425-479 (1998)
2. Welchman, R.L.; Gordon, C.; Mayer, R.J.: Ubiquitin and ubiquitin-like proteins as multifunctional signals. Nat. Rev. Mol. Cell Biol. 6, 599-609 (2005)
3. Kim, W.; Bennett, E.J.; Huttlin, E.L.; Guo, A.; Li, J.; Possemato, A.; Sowa, M.E.; Rad, R.; Rush, J.; Comb, M.J.; Harper, J.W.; Gygi, S.P.: Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol. Cell. 44, 325-340 (2011)
4. Wagner, S.A.; Beli, P.; Weinert, B.T.; Nielsen, M.L.; Cox, J.; Mann, M.; Choudhary, C.: A proteome-wide, quantitative survey of in vivo ubiquitylation sites reveals widespread regulatory roles. Mol. Cell. Proteomics. 10, M111 013284 (2011)
5. Udeshi, N.D.; Mani, D.R.; Eisenhaure, T.; Mertins, P.; Jaffe, J.D.; Clauser, K.R.; Hacohen, N.; Carr, S.A.: Methods for quantification of in vivo changes in protein ubiquitination following proteasome and deubiquitinase inhibition. Mol. Cell. Proteomics. 11, 148-159 (2012)
6. Komander, D.; Clague, M.J.; Urbe, S.: Breaking the chains: Structure and function of the deubiquitinases. Nat. Rev. Mol. Cell Biol. 10, 550-563 (2009)
7. Love, K.R.; Catic, A.; Schlieker, C.; Ploegh, H.L.: Mechanisms, biology and inhibitors of deubiquitinating enzymes. Nat. Chem. Biol. 3, 697-705 (2007)
8. Xu, P.; Duong, D.M.; Seyfried, N.T.; Cheng, D.; Xie, Y.; Robert, J.; Rush, J.; Hochstrasser, M.; Finley, D.; Peng, J.: Quantitative proteomics reveals the function of unconventional ubiquitin chains in proteasomal degradation. Cell 137, 133-145 (2009)
9. Newton, K.; Matsumoto, M.L.; Wertz, I.E.; Kirkpatrick, D.S.; Lill, J.R.; Tan, J.; Dugger, D.; Gordon, N.; Sidhu, S.S.; Fellouse, F.A.; Komuves, L.; French, D.M.; Ferrando, R.E.; Lam, C.; Compaan, D.; Yu, C.; Bosanac, I.; Hymowitz, S.G.; Kelley, R.F.; Dixit, V.M.: Ubiquitin chain editing revealed by polyubiquitin linkage-specific antibodies. Cell 134, 668-678 (2008)
10. Xiong, Y.; Qiu, F.; Piao, W.; Song, C.; Wahl, L.M.; Medvedev, A.E.: Endotoxin tolerance impairs IL-1 receptor-associated kinase (IRAK) 4 and TGF-beta-activated kinase 1 activation, K63-linked polyubiquitination and assembly of IRAK1, TNF receptor-associated factor 6, and IkappaB kinase gamma and increases A20 expression. J. Biol. Chem. 286, 7905-7916 (2011)
11. Matsumoto, M.L.; Wickliffe, K.E.; Dong, K.C.; Yu, C.; Bosanac, I.; Bustos, D.; Phu, L.; Kirkpatrick, D.S.; Hymowitz, S.G.; Rape, M.; Kelley, R.F.; Dixit, V.M.: K11-linked polyubiquitination in cell cycle control revealed by a K11 linkage-specific antibody. Mol. Cell. 39, 477-484 (2010)
12. Singer, A.U.; Rohde, J.R.; Lam, R.; Skarina, T.; Kagan, O.; Dileo, R.; Chirgadze, N.Y.; Cuff, M.E.; Joachimiak, A.; Tyers, M.; Sansonetti, P.J.; Parsot, C.; Savchenko, A.: Structure of the Shigella T3SS effector IpaH defines a new class of E3 ubiquitin ligases. Nat. Struct. Mol. Biol. 15, 1293-1301 (2008)
13. Hicks, S.W.; Galan, J.E.: Hijacking the host ubiquitin pathway: Structural strategies of bacterial E3 ubiquitin ligases. Curr. Opin. Microbiol. 13, 41-46 (2010)
14. Wu, B.; Skarina, T.; Yee, A.; Jobin, M.C.; Dileo, R.; Semesi, A.; Fares, C.; Lemak, A.; Coombes, B.K.; Arrowsmith, C.H.; Singer, A.U.; Savchenko, A.: NleG Type 3 effectors from enterohaemorrhagic Escherichia coli are U-Box E3 ubiquitin ligases. PLoS Pathog. 6, e1000960 (2010)
15. Rytkonen, A.; Poh, J.; Garmendia, J.; Boyle, C.; Thompson, A.; Liu, M.; Freemont, P.; Hinton, J.C.; Holden, D.W.: SseL, a Salmonella deubiquitinase required for macrophage killing and virulence. Proc. Natl. Acad. Sci. U. S. A. 104, 3502-3507 (2007)
16. Catic, A.; Misaghi, S.; Korbel, G.A.; Ploegh, H.L.: ElaD, a Deubiquitinating protease expressed by E coli. PloS One 2, e381 (2007)
17. Peng, J.; Schwartz, D.; Elias, J.E.; Thoreen, C.C.; Cheng, D.; Marsischky, G.; Roelofs, J.; Finley, D.; Gygi, S.P.: A proteomics approach to understanding protein ubiquitination. Nat. Biotechnol. 21, 921-926 (2003)
18. Crinelli, R.; Bianchi, M.; Menotta, M.; Carloni, E.; Giacomini, E.; Pennati, M.; Magnani, M.: Ubiquitin over-expression promotes E6AP autodegradation and reactivation of the p53/MDM2 pathway in HeLa cells. Mol. Cell. Biochem. 318, 129-145 (2008)
19. Matsumoto, M.; Hatakeyama, S.; Oyamada, K.; Oda, Y.; Nishimura, T.; Nakayama, K.I.: Large-scale analysis of the human ubiquitin-related proteome. Proteomics 5, 4145-4151 (2005)
20. Vasilescu, J.; Smith, J.C.; Ethier, M.; Figeys, D.: Proteomic analysis of ubiquitinated proteins from human MCF-7 breast cancer cells by immunoaffinity purification and mass spectrometry. J. Proteome. Res. 4, 2192-2200 (2005)
21. Xu, G.; Paige, J.S.; Jaffrey, S.R.: Global analysis of lysine ubiquitination by ubiquitin remnant immunoaffinity profiling. Nat. Biotechnol. 28, 868-873 (2010)
22. Wagner, S.A.; Beli, P.; Weinert, B.T.; Scholz, C.; Kelstrup, C.D.; Young, C.; Nielsen, M.L.; Olsen, J.V.; Brakebusch, C.; Choudhary, C.: Proteomic analyses reveal divergent ubiquitylation site patterns in murine tissues. Mol. Cell. Proteomics: MCP 11, 1578-1585 (2012)
23. Bustos, D.; Bakalarski, C.E.; Yang, Y.; Peng, J.; Kirkpatrick, D.S.: Characterizing ubiquitination sites by peptide-based immunoaffinity enrichment. Mol. Cell. Proteomics: MCP 11, 1529-1540 (2012)
24. Grabbe, C.; Dikic, I.: Functional roles of ubiquitin-like domain (ULD) and ubiquitin-binding domain (UBD) containing proteins. Chem. Rev. 109, 1481-1494 (2009)
25. Hurley, J.H.; Lee, S.; Prag, G.: Ubiquitin-binding domains. Biochem. J. 399, 361-372 (2006)
26. Raasi, S.; Varadan, R.; Fushman, D.; Pickart, C.M.: Diverse polyubiquitin interaction properties of ubiquitin-associated domains. Nat. Struct. Mol. Biol. 12, 708-714 (2005)
27. Hjerpe, R.; Aillet, F.; Lopitz-Otsoa, F.; Lang, V.; England, P.; Rodriguez, M.S.: Efficient protection and isolation of ubiquitylated proteins using tandem ubiquitin-binding entities. EMBO Rep 10, 1250-1258 (2009)
28. Shi, Y.; Chan, D.W.; Jung, S.Y.; Malovannaya, A.; Wang, Y.; Qin, J.: A data set of human endogenous protein ubiquitination sites. Mol. Cell Proteomics 10, M110 002089 (2011)
29. Lopitz-Otsoa, F.; Rodriguez-Suarez, E.; Aillet, F.; Casado-Vela, J.; Lang, V.; Matthiesen, R.; Elortza, F.; Rodriguez, M.S.: Integrative analysis of the ubiquitin proteome isolated using Tandem Ubiquitin Binding Entities (TUBEs). J. Proteomics 65, 2998-3014 (2012)
30. Shi, Y.; Xu, P.; Qin, J.: Ubiquitinated proteome: Ready for global. Mol. Cell Proteomics 10, R110 006882 (2011)
31. Manzano, C.; Abraham, Z.; Lopez-Torrejon, G.; Del Pozo, J.C.: Identification of ubiquitinated proteins in Arabidopsis. Plant Mol. Biol. 68, 145-158 (2008)
32. Mayor, T.; Graumann, J.; Bryan, J.; MacCoss, M.J.; Deshaies, R.J.: Quantitative profiling of ubiquitylated proteins reveals proteasome substrates and the substrate repertoire influenced by the Rpn10 receptor pathway. Mol. Cell Proteomics 6, 1885-1895 (2007)
33. Livesay, E.A.; Tang, K.; Taylor, B.K.; Buschbach, M.A.; Hopkins, D.F.; LaMarche, B.L.; Zhao, R.; Shen, Y.; Orton, D.J.; Moore, R.J.; Kelly, R.T.; Udseth, H.R.; Smith, R.D.: Fully automated four-column capillary LC-MS system for maximizing throughput in proteomic analyses. Anal. Chem. 80, 294-302 (2008)
34. Eng, J.K.; McCormack, A.L.; Yates III, J.R.: An approach to correlate MS/MS data to amino acid sequences in a protein database. J. Am. Soc. Mass. Spectrom 5, 976-989 (1994)
35. Lopez-Ferrer, D.; Martinez-Bartolome, S.; Villar, M.; Campillos, M.; Martin-Maroto, F.; Vazquez, J.: Statistical model for large-scale peptide identification in databases from tandem mass spectra using SEQUEST. Anal. Chem. 76, 6853-6860 (2004)
36. Lopez-Ferrer, D.; Petritis, K.; Hixson, K.K.; Heibeck, T.H.; Moore, R.J.; Belov, M.E.; Camp 2nd, D.G.; Smith, R.D.: Application of pressurized solvents for ultrafast trypsin hydrolysis in proteomics: Proteomics on the fly. J. Proteome. Res. 7, 3276-3281 (2008)
37. Franco, M.; Seyfried, N.T.; Brand, A.H.; Peng, J.; Mayor, U.: A novel strategy to isolate ubiquitin conjugates reveals wide role for ubiquitination during neural development. Mol. Cell. Proteomics 10, M110 002188 (2011)
38. Nielsen, M.L.; Vermeulen, M.; Bonaldi, T.; Cox, J.; Moroder, L.; Mann, M.: Iodoacetamide-induced artifact mimics ubiquitination in mass spectrometry. Nat. Methods 5, 459-460 (2008)
39. Polpitiya, A.D.; Qian, W.J.; Jaitly, N.; Petyuk, V.A.; Adkins, J.N.; Camp 2nd, D.G.; Anderson, G.A.; Smith, R.D.: DAnTE: A statistical tool for quantitative analysis of -omics data. Bioinformatics 24, 1556-1558 (2008)
40. Donaldson, K.M.; Yin, H.; Gekakis, N.; Supek, F.; Joazeiro, C.A.: Ubiquitin signals protein trafficking via interaction with a novel ubiquitin binding domain in the membrane fusion regulator, Vps9p. Curr. Biol. 13, 258-262 (2003)
41. Kamitani, T.; Kito, K.; Fukuda-Kamitani, T.; Yeh, E.T.: Targeting of NEDD8 and its conjugates for proteasomal degradation by NUB1. J. Biol. Chem. 276, 46655-46660 (2001)
42. Kang, Y.; Chen, X.; Lary, J.W.; Cole, J.L.; Walters, K.J.: Defining how ubiquitin receptors hHR23a and S5a bind polyubiquitin. J. Mol. Biol. 369, 168-176 (2007)
43. Kirkin, V.; Lamark, T.; Sou, Y.S.; Bjorkoy, G.; Nunn, J.L.; Bruun, J.A.; Shvets, E.; McEwan, D.G.; Clausen, T.H.; Wild, P.; Bilusic, I.; Theurillat, J.P.; Overvatn, A.; Ishii, T.; Elazar, Z.; Komatsu, M.; Dikic, I.; Johansen, T.: A role for NBR1 in autophagosomal degradation of ubiquitinated substrates. Mol. Cell 33, 505-516 (2009)
44. Lim, P.J.; Danner, R.; Liang, J.; Doong, H.; Harman, C.; Srinivasan, D.; Rothenberg, C.; Wang, H.; Ye, Y.; Fang, S.; Monteiro, M.J.: Ubiquilin and p97/VCP bind erasin, forming a complex involved in ERAD. J. Cell Biol. 187, 201-217 (2009)
45. Long, J.; Gallagher, T.R.; Cavey, J.R.; Sheppard, P.W.; Ralston, S.H.; Layfield, R.; Searle, M.S.: Ubiquitin recognition by the ubiquitin-associated domain of p62 involves a novel conformational switch. J. Biol. Chem. 283, 5427-5440 (2008)
46. Prag, G.; Misra, S.; Jones, E.A.; Ghirlando, R.; Davies, B.A.; Horazdovsky, B.F.; Hurley, J.H.: Mechanism of ubiquitin recognition by the CUE domain of Vps9p. Cell 113, 609-620 (2003)
47. Zhang, D.; Chen, T.; Ziv, I.; Rosenzweig, R.; Matiuhin, Y.; Bronner, V.; Glickman, M.H.; Fushman, D.: Together, Rpn10 and Dsk2 can serve as a polyubiquitin chain-length sensor. Mol. Cell 36, 1018-1033 (2009)
48. Zhang, D.; Raasi, S.; Fushman, D.: Affinity makes the difference: Nonselective interaction of the UBA domain of Ubiquilin-1 with monomeric ubiquitin and polyubiquitin chains. J. Mol. Biol. 377, 162-180 (2008)
49. Zhang, N.; Wang, Q.; Ehlinger, A.; Randles, L.; Lary, J.W.; Kang, Y.; Haririnia, A.; Storaska, A.J.; Cole, J.L.; Fushman, D.; Walters, K.J.: Structure of the s5a:k48-linked diubiquitin complex and its interactions with rpn13. Mol. Cell 35, 280-290 (2009)
50. Isogai, S.; Morimoto, D.; Arita, K.; Unzai, S.; Tenno, T.; Hasegawa, J.; Sou, Y.S.; Komatsu, M.; Tanaka, K.; Shirakawa, M.; Tochio, H.: Crystal Structure of the Ubiquitin-associated (UBA) Domain of p62 and Its Interaction with Ubiquitin. J. Biol. Chem. 286, 31864-31874 (2011)
51. Paul, F.E.; Hosp, F.; Selbach, M.: Analyzing protein-protein interactions by quantitative mass spectrometry. Methods 54, 387-395 (2011)
52. Lichty, J.J.; Malecki, J.L.; Agnew, H.D.; Michelson-Horowitz, D.J.; Tan, S.: Comparison of affinity tags for protein purification. Protein Expr. Purif. 41, 98-105 (2005)
53. Perkins, D.J.; Qureshi, N.; Vogel, S.N.: A Toll-like receptor-responsive kinase, protein kinase R, is inactivated in endotoxin tolerance through differential K63/K48 ubiquitination. MBio 1 (2010)
54. Cannon, J.; Nakasone, M.; Fushman, D.; Fenselau, C.: Proteomic identification and analysis of K63-linked ubiquitin conjugates. Anal. Chem. 84, 10121-10128 (2012)
55. Kirkpatrick, D.S.; Weldon, S.F.; Tsaprailis, G.; Liebler, D.C.; Gandolfi, A.J.: Proteomic identification of ubiquitinated proteins from human cells expressing His-tagged ubiquitin. Proteomics 5, 2104-2111 (2005)
56. Haley, B.; Paunesku, T.; Protic, M.; Woloschak, G.E.: Response of heterogeneous ribonuclear proteins (hnRNP) to ionising radiation and their involvement in DNA damage repair. Int. J. Radiat. Biol. 85, 643-655 (2009)
57. Kraft, C.; Deplazes, A.; Sohrmann, M.; Peter, M.: Mature ribosomes are selectively degraded upon starvation by an autophagy pathway requiring the Ubp3p/Bre5p ubiquitin protease. Nat. Cell Biol. 10, 602-610 (2008)
58. Yoshida, M.; Yoshida, K.; Kozlov, G.; Lim, N.S.; De Crescenzo, G.; Pang, Z.; Berlanga, J.J.; Kahvejian, A.; Gehring, K.; Wing, S.S.; Sonenberg, N.: Poly(A) binding protein (PABP) homeostasis is mediated by the stability of its inhibitor, Paip2. EMBO J. 25, 1934-1944 (2006)
59. Kaiser, S.E.; Riley, B.E.; Shaler, T.A.; Trevino, R.S.; Becker, C.H.; Schulman, H.; Kopito, R.R.: Protein standard absolute quantification (PSAQ) method for the measurement of cellular ubiquitin pools. Nat Methods 8, 691-696 (2011)