Affinity proteomics to study endogenous protein complexes: Pointers, pitfalls, preferences and perspectives

BioTechniques

Volumn 58, Issue 3, 2015, Pages 103-119

  Lacava, John ^a,b   Molloy, Kelly R ^a   Taylor, Martin S ^c   Domanski, Michal ^a,d   Chait, Brian T ^a   Rout, Michael P ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d AARHUS UNIVERSITY   (Denmark)

Author keywords

Affinity; Interactomics; Protein complex; Protein purification; Proteomics

Indexed keywords

AFFINITY CAPTURE TECHNIQUE; AFFINITY PROTEOMICS; ARTICLE; CELL BREAKAGE; CRYSTALLOGRAPHY; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC PROCEDURES; HUMAN; MASS SPECTROMETRY; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROCESS OPTIMIZATION; PROTEIN BINDING; PROTEIN COMPLEX; PROTEIN EXTRACTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEOMICS; STAINING; TRANSGENE; WESTERN BLOTTING; AFFINITY CHROMATOGRAPHY; CHEMISTRY; ISOLATION AND PURIFICATION; PROCEDURES;

MULTIPROTEIN COMPLEX; PROTEIN; PROTEIN BINDING;

CHROMATOGRAPHY, AFFINITY; HUMANS; MASS SPECTROMETRY; MULTIPROTEIN COMPLEXES; PROTEIN BINDING; PROTEINS; PROTEOMICS;

EID: 84924404035     PISSN: 07366205     EISSN: 19409818     Source Type: Journal    
DOI: 10.2144/000114262     Document Type: Article

References (170)

1. Roque, A.C.A. and C.R. Lowe. 2008. Affinity chromatography: history, perspectives, limitations and prospects. Methods Mol Biol. 421:1-21.
2. Urh, M., D. Simpson, and K. Zhao. 2009. Affinity Chromatography: General Methods. Methods Enzymol. 463:417-438.
3. Dunham, W.H., M. Mullin, and A.-C. Gingras. 2012. Affinity-purification coupled to mass spectrometry: basic principles and strategies. Proteomics 12:1576-1590.
4. Oeffinger, M. 2012. Two steps forward-one step back: Advances in affinity purification mass spectrometry of macromolecular complexes. Proteomics 12:1591-1608.
5. Jeong, J.S., L. Jiang, E. Albino, J. Marrero, H.S. Rho, J. Hu, S. Hu, C. Vera, et al. 2012. Rapid identification of monospecific monoclonal antibodies using a human proteome microarray. Mol Cell Proteomics 11:O111.016253.
6. Kurosawa, N., M. Yoshioka, R. Fujimoto, F. Yamagishi, and M. Isobe. 2012. Rapid production of antigen-specific monoclonal antibodies from a variety of animals. BMC Biol. 10:80.
7. Fridy, P.C., Y. Li, S. Keegan, M.K. Thompson, I. Nudelman, J.F. Scheid, M. Oeffinger, M.C. Nussenzweig, et al. 2014. A robust pipeline for rapid production of versatile nanobody repertoires. Nat. Methods 11:1253-1260.
8. Couchman, J.R. 2009. Commercial antibodies: the good, bad, and really ugly. J. Histochem. Cytochem. 57:7-8.
9. Wadman, M. 2013. NIH mulls rules for validating key results. Nature 500:14-16.
10. Johnson, M., and H. Pan. 2014. Antibody Quality. Mater Methods 4:572.
11. Bradbury, A. and A. Plückthun. 2015. Reproducibility: Standardize antibodies used in research. Nature 518:27-29.
12. Tomecki, R., M.S. Kristiansen, S. Lykke-Andersen, A. Chlebowski, K.M. Larsen, R.J. Szczesny, K. Drazkowska, A. Pastula, et al. 2010. The human core exosome interacts with differentially localized processive RNases: hDros. Inf. Serv.3 and hDros. Inf. Serv.3L. EMBO J. 29:2342-2357.
13. Domanski, M., K. Molloy, H. Jiang, B.T. Chait, M.P. Rout, T.H. Jensen, and J. LaCava. 2012. Improved methodology for the affinity isolation of human protein complexes expressed at near endogenous levels. Biotechniques 0:1-6.
14. Stadler, C., E. Rexhepaj, V.R. Singan, R.F. Murphy, R. Pepperkok, M. Uhlen, J.C. Simpson, and E. Lundberg. 2013. Immunofluorescence and fluorescent-protein tagging show high correlation for protein localization in mammalian cells. Nat. Methods 10:315-323.
15. Gibson, T.J., M. Seiler, and R.A. Veitia. 2013. The transience of transient overexpression. Nat. Methods 10:715-721.
16. Jarvik, J.W. and C.A. Telmer. 1998. Epitope tagging. Annu. Rev. Genet. 32:601-618.
17. Terpe, K. 2003. Overview of tag protein fusions: from molecular and biochemical fundamentals to commercial systems. Appl. Microbiol. Biotechnol. 60:523-533.
18. Lichty, J.J., J.L. Malecki, H.D. Agnew, D.J. Michelson-Horowitz, and S. Tan. 2005. Comparison of affinity tags for protein purification. Protein Expr. Purif. 41:98-105.
19. Li, Y. 2011. The tandem affinity purification technology: an overview. Biotechnol. Lett. 33:1487-1499.
20. Palmer, E. and T. Freeman. 2004. Investigation into the use of C-and N-terminal GFP fusion proteins for subcellular localization studies using reverse transfection microarrays. Comp. Funct. Genomics 5:342-353.
21. Tasaki, T., S.M. Sriram, K.S. Park, and Y.T. Kwon. 2012. The N-End rule pathway. Annu. Rev. Biochem. 81:261-289.
22. Beach, N.M., S.M. Smith, S. Ramamoorthy, and X.J. Meng. 2011. Chimeric porcine circoviruses (PCV) containing amino acid epitope tags in the C terminus of the capsid gene are infectious and elicit both anti-epitope tag antibodies and anti-PCV type 2 neutralizing antibodies in pigs. J. Virol. 85:4591-4595.
23. Teterina, N.L., C. Lauber, K.S. Jensen, E.A. Levenson, A.E. Gorbalenya, and E. Ehrenfeld. 2011. Identification of tolerated insertion sites in poliovirus non-structural proteins. Virology 409:1-11.
24. Remenyi, R., H. Qi, S.-Y. Su, Z. Chen, N.C. Wu, V. Arumugaswami, S. Truong, V. Chu, et al. 2014. A comprehensive functional map of the hepatitis C virus genome provides a resource for probing viral proteins. MBio. 5:e01469-14.
25. Taylor, M.S., J. LaCava, P. Mita, K.R. Molloy, C.R.L. Huang, D. Li, E.M. Adney, H. Jiang, et al. 2013. Affinity proteomics reveals human host factors implicated in discrete stages of LINE-1 retrotransposition. Cell 155:1034-1048.
26. Chen, X., J.L. Zaro, and W.-C. Shen. 2013. Fusion protein linkers: Property, design and functionality. Adv. Drug Deliv. Rev. 65:1357-1369.
27. Waugh, D.S. 2011. An overview of enzymatic reagents for the removal of affinity tags. Protein Expr. Purif. 80:283-293.
28. Lindmark, R., K. Thorén-Tolling, and J. Sjöquist. 1983. Binding of immunoglobulins to protein A and immunoglobulin levels in mammalian sera. J. Immunol. Methods 62:1-13.
29. Moks, T., L. Abrahmsén, B. Nilsson, U. Hellman, J. Sjöquist, and M. Uhlén. 1986. Staphylococcal protein A consists of five IgG-binding domains. Eur. J. Biochem. 156:637-643.
30. Ljungberg, U.K., B. Jansson, U. Niss, R. Nilsson, B.E.B. Sandberg, and B. Nilsson. 1993. The interaction between different domains of staphylococcal protein A and human polyclonal IgG, IgA, IgM and F(ab’)2: Separation of affinity from specificity. Mol. Immunol. 30:1279-1285.
31. Brown, N.L., S.P. Bottomley, M.D. Scawen, and M.G. Gore. 1998. A study of the interactions between an IgG-binding domain based on the B domain of staphylococcal protein A and rabbit IgG. Mol Biotechnol. 10:9-16.
32. Jansson, B., M. Uhlén, and P.A. Nygren. 1998. All individual domains of staphylococcal protein A show Fab binding. FEMS Immunol. Med. Microbiol. 20:69-78.
33. LaCava, J., N. Chandramouli, H. Jiang, and M.P. Rout. 2013. Improved Native Isolation of Endogenous Protein A-Tagged Protein Complexes. Biotechniques 54:213-216.
34. Rigaut, G., A. Shevchenko, B. Rutz, M. Wilm, M. Mann, and B. Seraphin. 1999. A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol. 17:1030-1032.
35. Nilsson, B., T. Moks, B. Jansson, L. Abrahmsén, A. Elmblad, E. Holmgren, C. Henrichson, T.A. Jones, and M. Uhlén. 1987. A synthetic IgG-binding domain based on staphylococcal protein A. Protein Eng. 1:107-113.
36. Uhlén, M., B. Guss, B. Nilsson, S. Gatenbeck, L. Philipson, and M. Lindberg. 1984. Complete Sequence of the Staphylococcal Gene Encoding Protein-a -a Gene Evolved Through Multiple Duplications. J. Biol. Chem. 259:1695-1702.
37. Aitchison, J.D., M.P. Rout, M. Marelli, G. Blobel, and R.W. Wozniak. 1995. Two novel related yeast nucleoporins Nup170p and Nup157p: complementation with the vertebrate homologue Nup155p and functional interactions with the yeast nuclear pore-membrane protein Pom152p. J. Cell Biol. 131:1133-1148.
38. Deisenhofer, J. 1981. Crystallographic refinement and atomic models of a human Fc fragment and its complex with fragment B of protein A from Staphylococcus aureus at 2.9-and 2.8-Å resolution. Biochemistry 20:2361-2370.
39. Tashiro, M., R. Tejero, D.E. Zimmerman, B. Celda, B. Nilsson, and G.T. Montelione. 1997. High-resolution solution NMR structure of the Z domain of staphylococcal protein A. J. Mol. Biol. 272:573-590.
40. Bürckstümmer, T., K.L. Bennett, A. Preradovic, G. Schutze, O. Hantschel, G. Superti-Furga, and A. Bauch. 2006. An efficient tandem affinity purification procedure for interaction proteomics in mammalian cells. Nat. Methods 3:1013-1019.
41. DeLano, W.L., M.H. Ultsch, A.M. de Vos, and J.A. Wells. 2000. Convergent solutions to binding at a protein-protein interface. Science 287:1279-1283.
42. Strambio-de-Castillia, C., J. Tetenbaum-Novatt, B.S. Imai, B.T. Chait, and M.P. Rout. 2005. A method for the rapid and efficient elution of native affinity-purified protein A tagged complexes. J. Proteome Res. 4:2250-2256.
43. Tillib, S.V. 2011. “Camel nanoantibody” is an efficient tool for research, diagnostics and therapy. Mol Biol (Mosk). 45:77-85.
44. Cristea, I.M., R. Williams, B. Chait, and M. Rout. 2005. Fluorescent proteins as proteomic probes. Mol. Cell. Proteomics 4:1933-1941.
45. Hopp, T., K. Prickett, V. Price, R. Libby, C. March, D. Cerretti, D. Urdal, and P. Conlon. 1988. A short polypeptide marker sequence useful for recombinant protein identification and purification. Nat Biotechnol. 6:1204-1210.
46. Brizzard, B.L., R.G. Chubet, and D.L. Vizard. 1994. Immunoaffinity purification of FLAG epitope-tagged bacterial alkaline phosphatase using a novel monoclonal antibody and peptide elution. Biotechniques 16:730-735.
47. Firsov, D., L. Schild, I. Gautschi, A.M. Merillat, E. Schneeberger, and B.C. Rossier. 1996. Cell surface expression of the epithelial Na channel and a mutant causing Liddle syndrome: A quantitative approach. Proc. Natl. Acad. Sci. USA 93:15370-15375.
48. Wegner, G.J., H.J. Lee, and R.M. Corn. 2002. Characterization and optimization of peptide arrays for the study of epitope-antibody interactions using surface plasmon resonance imaging. Anal. Chem. 74:5161-5168.
49. Hernan, R., K. Heuermann, and B. Brizzard. 2000. Multiple epitope tagging of expressed proteins for enhanced detection. Biotechniques 28:789-793.
50. Zhang, L., R. Hernan, and B. Brizzard. 2001. Multiple tandem epitope tagging for enhanced detection of protein expressed in mammalian cells. Mol. Biotechnol. 19:313-321.
51. Scheiner Bobis, G. 2009. Gene expression in yeast. In Encyclopedia of Life Sciences, (John Wiley & Sons, Ltd).
52. Petracek, M.E. and M.S. Longtine. 2002. PCR-based engineering of yeast genome. Methods Enzymol. 350: 445-469.
53. Ho, Y., A. Gruhler, A. Heilbut, G.D. Bader, L. Moore, S.-L. Adams, A. Millar, P. Taylor, et al. 2002. Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 415:180-183.
54. Gavin, A.-C., P. Aloy, P. Grandi, R. Krause, M. Boesche, M. Marzioch, C. Rau, L.J. Jensen, et al. 2006. Proteome survey reveals modularity of the yeast cell machinery. Nature 440:631-636.
55. Krogan, N.J., G. Cagney, H. Yu, G. Zhong, X. Guo, A. Ignatchenko, J. Li, S. Pu, et al. 2006. Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature. 440:637-643.
56. Huh, W.-K., J.V. Falvo, L.C. Gerke, A.S. Carroll, R.W. Howson, J.S. Weissman, and E.K. O’Shea. 2003. Global analysis of protein localization in budding yeast. Nature 425:686-691.
57. Ghaemmaghami, S., W.-K. Huh, K. Bower, R.W. Howson, A. Belle, N. Dephoure, E.K. O’Shea, and J.S. Weissman. 2003. Global analysis of protein expression in yeast. Nature 425:737-741.
58. Gavin, A.-C., M. Bösche, R. Krause, P. Grandi, M. Marzioch, A. Bauer, J. Schultz, J.M. Rick, et al. 2002. Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415:141-147.
59. Mering von, C., R. Krause, B. Snel, M. Cornell, S.G. Oliver, S. Fields, and P. Bork. 2002. Comparative assessment of large-scale data sets of protein-protein interactions. Nature 417:399–403.
60. Royer, L., M. Reimann, A.F. Stewart, and M. Schroeder. 2012. Network compression as a quality measure for protein interaction networks. PLoS ONE 7:e35729.
61. Gerhard, D.S., L. Wagner, E.A. Feingold, C.M. Shenmen, L.H. Grouse, G. Schuler, S.L. Klein, S. Old, et al. 2004. The status, quality, and expansion of the NIH full-length cDNA project: the Mammalian Gene Collection (MGC). Genome Res. 14:2121-2127.
62. Hartley, J.L., G.F. Temple, and M.A. Brasch. 2000. DNA cloning using in vitro site-specific recombination. Genome Res. 10:1788-1795.
63. Katzen, F. 2007. Gateway® recombinational cloning: a biological operating system. Expert Opin Drug Discov. 2:571-589.
64. Lamesch, P., N. Li, S. Milstein, C. Fan, T. Hao, G. Szabo, Z. Hu, K. Venkatesan, et al. 2007. hORFeome v3.1: a resource of human open reading frames representing over 10,000 human genes. Genomics 89:307-315.
65. Recillas-Targa, F. 2006. Multiple strategies for gene transfer, expression, knockdown, and chromatin influence in mammalian cell lines and transgenic animals. Mol. Biotechnol. 34:337-354.
66. Poser, I., M. Sarov, J.R.A. Hutchins, J.-K. Hériché, Y. Toyoda, A. Pozniakovsky, D. Weigl, A. Nitzsche, et al. 2008. BAC TransgeneOmics: a high-throughput method for exploration of protein function in mammals. Nat. Methods 5:409-415.
67. Ciotta, G., H. Hofemeister, M. Maresca, J. Fu, M. Sarov, K. Anastassiadis, and A.F. Stewart. 2011. Recombineering BAC transgenes for protein tagging. Methods 53:113-119.
68. Torres, J.Z., J.J. Miller, and P.K. Jackson. 2009. High-throughput generation of tagged stable cell lines for proteomic analysis. Proteomics 9:2888-2891.
69. Cong, L., F.A. Ran, D. Cox, S. Lin, R. Barretto, N. Habib, P.D. Hsu, X. Wu, et al. 2013. Multiplex genome engineering using CRISPR/Cas systems. Science 339:819-823.
70. Mali, P., L. Yang, K.M. Esvelt, J. Aach, M. Guell, J.E. DiCarlo, J.E. Norville, and G.M. Church. 2013. RNA-guided human genome engineering via Cas9. Science 339:823-826.
71. Böttcher, R., M. Hollmann, K. Merk, V. Nitschko, C. Obermaier, J. Philippou-Massier, I. Wieland, U. Gaul, and K. Förstemann. 2014. Efficient chromosomal gene modification with CRISPR/cas9 and PCR-based homologous recombination donors in cultured Drosophila cells. Nucleic Acids Res. 42:e89.
72. Park, A., S.T. Won, M. Pentecost, W. Bartkowski, and B. Lee. 2014. CRISPR/Cas9 allows efficient and complete knock-in of a destabilization domain-tagged essential protein in a human cell line, allowing rapid knockdown of protein function. PLoS ONE 9: e95101.
73. Yates, J.L., N. Warren, and B. Sugden. 1985. Stable replication of plasmids derived from Epstein-Barr virus in various mammalian cells. Nature 313:812-815.
74. Yu, J. 2012. Episomal Vectors. P. 51–83. In Primary and Stem Cells: Gene Transfer Technologies and Applications, U. Lakshmipathy, and B. Thyagarajan (Eds.), John Wiley & Sons, Inc., Hoboken, NJ.
75. O’Gorman, S., D.T. Fox, and G.M. Wahl. 1991. Recombinase-mediated gene activation and site-specific integration in mammalian cells. Science 251:1351-1355.
76. Turan, S., M. Galla, E. Ernst, J. Qiao, C. Voelkel, B. Schiedlmeier, C. Zehe, and J. Bode. 2011. Recombinase-Mediated Cassette Exchange (RMCE): Traditional Concepts and Current Challenges. J. Mol. Biol. 407:193-221.
77. Yao, F., T. Svensjö, T. Winkler, M. Lu, C. Eriksson, and E. Eriksson. 1998. Tetracycline repressor, tetR, rather than the tetR-mammalian cell transcription factor fusion derivatives, regulates inducible gene expression in mammalian cells. Hum. Gene Ther. 9:1939-1950.
78. Berens, C. and W. Hillen. 2004. Gene regulation by tetracyclines. p. 255–277. In J.K. Setlow (Ed.), Genetic Engineering: Principles and Methods. Springer US, New York, NY.
79. Andersen, P.R., M. Domanski, M.S. Kristiansen, H. Storvall, E. Ntini, C. Verheggen, A. Schein, J. Bunkenborg, et al. 2013. The human cap-binding complex is functionally connected to the nuclear RNA exosome. Nat. Struct. Mol. Biol. 20:1367-1376.
80. Gossen, M., S. Freundlieb, G. Bender, G. Müller, W. Hillen, and H. Bujard. 1995. Transcriptional Activation by Tetracyclines in Mammalian Cells. Science. 268: 1766-1769.
81. Kramer, B.P., W. Weber, and M. Fussenegger. 2003. Artificial regulatory networks and cascades for discrete multilevel transgene control in mammalian cells. Biotechnol. Bioeng. 83:810-820.
82. Nevozhay, D., T. Zal, and G. Balázsi. 2013. Transferring a synthetic gene circuit from yeast to mammalian cells. Nat Commun. 4:1451.
83. Forler, D., T. Köcher, M. Rode, M. Gentzel, E. Izaurralde, and M. Wilm. 2003. An efficient protein complex purification method for functional proteomics in higher eukaryotes. Nat. Biotechnol. 21:89-92.
84. Kittler, R., L. Pelletier, C. Ma, I. Poser, S. Fischer, A.A. Hyman, and F. Buchholz. 2005. RNA interference rescue by bacterial artificial chromosome transgenesis in mammalian tissue culture cells. Proc. Natl. Acad. Sci. USA 102:2396-2401.
85. Sarov, M., S. Schneider, A. Pozniakovski, A. Roguev, S. Ernst, Y. Zhang, A.A. Hyman, and A.F. Stewart. 2006. A recombineering pipeline for functional genomics applied to Caenorhabditis elegans. Nat. Methods 3:839-844.
86. Cheeseman, I.M. and A. Desai. 2005. A combined approach for the localization and tandem affinity purification of protein complexes from metazoans. Sci. STKE 2005:pl1.
87. Hubner, N.C., A.W. Bird, J. Cox, B. Splettstoesser, P. Bandilla, I. Poser, A. Hyman, and M. Mann. 2010. Quantitative proteomics combined with BAC TransgeneOmics reveals in vivo protein interactions. J. Cell Biol. 189:739-754.
88. Leary, J.F. 2001. High-speed cell sorting. Curr Protoc Cytom. Chapter 1:Unit 1.7.
89. Herzenberg, L.A., D. Parks, B. Sahaf, O. Perez, and M. Roederer. 2002. The history and future of the Fluorescence Activated Cell Sorter and flow cytometry: A view from Stanford. Clin. Chem. 48:1819-1827.
90. Yates, J.L. and N. Guan. 1991. Epstein-Barr virus-derived plasmids replicate only once per cell cycle and are not amplified after entry into cells. J. Virol. 65:483-488.
91. Bornkamm, G.W., C. Berens, C. Kuklik-Roos, J.-M. Bechet, G. Laux, J. Bachl, M. Korndoerfer, M. Schlee, et al. 2005. Stringent doxycycline-dependent control of gene activities using an episomal one-vector system. Nucleic Acids Res. 33:e137.
92. O’Donnell, K.A., W. An, C.T. Schrum, S.J. Wheelan, and J.D. Boeke. 2013. Controlled inser tional mutagenesis using a LINE-1 (ORFeus) gene-trap mouse model. Proc Natl Acad Sci U S A. 110:E2706–E2713.
93. Matentzoglu, K. and M. Scheffner. 2009. Ubiquitin-fusion protein system: A powerful tool for ectopic protein expression in mammalian cells. BioTechniques 46:21-22.
94. Novick, A. and M. Weiner. 1957. ENZYME INDUCTION AS AN ALL-OR-NONE PHENOMENON. Proc. Natl. Acad. Sci. USA 43:553-566.
95. Ko, M.S.H., H. Nakauchi, and N. Takahashi. 1990. The dose dependence of glucocorticoid-inducible gene expression results from changes in the number of transcriptionally active templates. EMBO J. 9:2835-2842.
96. Raj, A. and A. van Oudenaarden. 2008. Nature, Nurture, or Chance: Stochastic Gene Expression and Its Consequences. Cell 135:216-226.
97. Goldberg, S. 2008. Mechanical/physical methods of cell disruption and tissue homogenization. Methods Mol Biol. 424:3-22.
98. Salazar, O. 2008. Bacteria and yeast cell disruption using lytic enzymes. Methods Mol Biol. 424:23-34.
99. Ji, H. 2010. Lysis of cultured cells for immunoprecipitation. Cold Spring Harb Protoc.2010:pdb.prot5466.
100. Saleem, R.A., R.S. Rogers, A.V. Ratushny, D.J. Dilworth, P.T. Shannon, D. Shteynberg, Y. Wan, R.L. Moritz, et al. 2010. Integrated phosphoproteomics analysis of a signaling network governing nutrient response and peroxisome induction. Mol. Cell. Proteomics 9:2076-2088.
101. Schultz, M.C. 1999. Chromatin assembly in yeast cell-free extracts. Methods 17:161-172.
102. Fernandez-Martinez, J., J. Phillips, M.D. Sekedat, R. Diaz-Avalos, J. Velazquez-Muriel, J.D. Franke, R. Williams, D.L. Stokes, et al. 2012. Structure-function mapping of a heptameric module in the nuclear pore complex. J. Cell Biol. 196:419-434.
103. Grabski, A.C. 2009. Advances in preparation of biological extracts for protein purification. Methods Enzymol. 463:285-303.
104. Keck, J.M., M.H. Jones, C.C.L. Wong, J. Binkley, D. Chen, S.L. Jaspersen, E.P. Holinger, T. Xu, et al. 2011. A cell cycle phosphoproteome of the yeast centrosome. Science 332:1557-1561.
105. Bloom, J., I.M. Cristea, A.L. Procko, V. Lubkov, B.T. Chait, M. Snyder, and F.R. Cross. 2011. Global analysis of Cdc14 phosphatase reveals diverse roles in mitotic processes. J. Biol. Chem. 286:5434-5445.
106. Oeffinger, M., K.E. Wei, R. Rogers, J.A. DeGrasse, B.T. Chait, J.D. Aitchison, and M.P. Rout. 2007. Comprehensive analysis of diverse ribonucleoprotein complexes. Nat. Methods 4:951-956.
107. Zhang, J., P. Harnpicharnchai, J. Jakovljevic, L. Tang, Y. Guo, M. Oeffinger, M.P. Rout, S.L. Hiley, et al. 2007. Assembly factors Rpf2 and Rrs1 recruit 5S rRNA and ribosomal proteins rpL5 and rpL11 into nascent ribosomes. Genes Dev. 21:2580-2592.
108. Oeffinger, M., D. Zenklusen, A. Ferguson, K.E. Wei, A. El Hage, D. Tollervey, B.T. Chait, R.H. Singer, and M.P. Rout. 2009. Rrp17p Is a Eukaryotic Exonuclease Required for 5 ‘End Processing of Pre-60S Ribosomal RNA. Mol. Cell 36:768-781.
109. Schultz, M.C., D. Hockman, T. Harkness, W. Garinther, and B. Altheim. 1997. Chromatin assembly in a yeast whole-cell extract. Proc. Natl. Acad. Sci. USA 94:9034-9039.
110. Krogan, N.J., M. Kim, S.H. Ahn, G. Zhong, M.S. Kobor, G. Cagney, A. Emili, A. Shilatifard, et al. 2002. RNA polymerase II elongation factors of Saccharomyces cerevisiae: a targeted proteomics approach. Mol. Cell. Biol. 22:6979-6992.
111. Cristea, I.M. and B.T. Chait. 2011. Affinity purification of protein complexes. Cold Spring Harb Protoc. 2011:pdb. prot5611.
112. Staley, J. 2005. Making whole cell extract of Saccharomyces cerevisiae cells using the Retsch MM301 Ball Mill. Retsch GmbH, Haan, Germany.
113. Varshavsky, A. and Y. Ilyin. 1974. Salt treatment of chromatin induces redistribution of histones. Biochim Biophys Acta. 340:207-217.
114. Li, H.J., A.W. Hu, R.A. Maciewicz, P. Cohen, R.M. Santella, and C. Chang. 1977. Structural transition in chromatin induced by ions in solution. Nucleic Acids Res. 4:3839-3854.
115. Brust, R. 1986. Viscosity of chromatin solutions increases with increasing ionic strength. Mol. Biol. Rep. 11:213-217.
116. Moore, S. 1981. Pancreatic DNase. p. 281-296. In P. Boyer (Ed.), The Enzymes. Elsevier, New York, NY.
117. Pan, C.Q. and R.A. Lazarus. 1999. Ca2+-dependent activity of human DNase I and its hyperactive variants. Protein Sci. 8:1780-1788.
118. Ellis, R.J. 2001. Macromolecular crowding: obvious but underappreciated. Trends Biochem. Sci. 26:597-604.
119. Zhou, H.-X., G. Rivas, and A.P. Minton. 2008. Macromolecular crowding and confinement: Biochemical, biophysical, and potential physiological consequences. Annu Rev Biophys. 37:375-397.
120. O Nostro, Lo, P., and B.W. Ninham. 2012. Hofmeister phenomena: an update on ion specificity in biology. Chem. Rev. 112:2286–2322.
121. Hyman, A.A., C.A. Weber, and F. Jülicher. 2014. Liquid-liquid phase separation in biology. Annu. Rev. Cell Dev. Biol. 30:39-58.
122. Kastritis, P.L. and A.M.J.J. Bonvin. 2013. On the binding affinity of macromolecular interactions: daring to ask why proteins interact. J. R. Soc. Interface 10:20120835.
123. Ugwu, S.O. and S.P. Apte. 2004. The Effect of Buffers on Protein Conformational Stability. Pharmaceutical Technology 28:86-113.
124. Mellacheruvu, D., Z. Wright, A.L. Couzens, J.P. Lambert, N.A. St-Denis, T. Li, Y.V. Miteva, S. Hauri, et al. 2013. The CRAPome: a contaminant repository for affinity purification-mass spectrometry data. Nat Methods. 10:730-736.
125. Aebersold, R. and M. Mann. 2003. Mass spectrometry-based proteomics. Nature 422:198-207.
126. Deppert, W.R. and R. Lukaĉin. 1999. Buffers and Additives. Journal of Chromatography Library 61:839-862.
127. Linke, D. 2009. Detergents: an overview. Methods Enzymol. 463:603-617.
128. Simpson, R.J. 2010. Stabilization of proteins for storage. Cold Spring Harb Protoc. 2010:pdb.top79.
129. Kunz, W., P. Lo Nostro, and B. Ninham. 2004. The present state of affairs with Hofmieister effects. Curr Opin Colloid Interface Sci. 9:1-18.
130. Bostrom, M., F. Tavares, S. Finet, F. Skouri-Panet, A. Tardieu, and B. Ninham. 2005. Why forces between proteins follow different Hofmeister series for pH above and below pI. Biophys. Chem. 117:217-224.
131. Wilson, E.K. 2012. Theoretical framework to explain effects of aqueous ions on proteins remains elusive. Chem. Eng. News 90:42-43.
132. Seddon, A.M., P. Curnow, and P.J. Booth. 2004. Membrane proteins, lipids and detergents: Not just a soap opera. Biochim Biophys Acta. 1666:105–117.
133. Niepel, M., C. Strambio-de-Castillia, J. Fasolo, B. Chait, and M. Rout. 2005. The nuclear pore complex-associated protein, Mlp2p, binds to the yeast spindle pole body and promotes its efficient assembly. J. Cell Biol. 170:225-235.
134. Magdeldin, S. and A. Moser. 2012. Affinity chromatography: Principles and applications. p. 3–28. In S. Magdeldin (Ed.), Affinity Chromatography. InTech, Rijeka, Croatia.
135. Sawin, K.E., C.C. Bicho, and H.A. Snaith. 2010. Inexpensive synthetic-based matrix for both conventional and rapid purification of protein A-and tandem affinity purification-tagged proteins. Anal. Biochem. 397:241-243.
136. Alber, F., S. Dokudovskaya, L.M. Veenhoff, W. Zhang, J. Kipper, D. Devos, A. Suprapto, O. Karni-Schmidt, et al. 2007. The molecular architecture of the nuclear pore complex. Nature 450:695-701.
137. Cristea, I.M. and B.T. Chait. 2011. Conjugation of magnetic beads for immunopurification of protein complexes. Cold Spring Harb Protoc. 2011:pdb.prot5610.
138. Williams, R.J. and C.M. Lyman. 1932. A neutral buffered standard for hydrogen ion work and accurate titrations which can be prepared in one minute. J. Am. Chem. Soc. 54:1911-1912.
139. Johnson, M. 2013. Detergents: Triton X-100, Tween-20, and More. Mater Methods 3:163.
140. Bhairi, S.M., and C. Mohan. 2007. Detergents. EMD Biosciences, La Jolla, CA.
141. LaCava, J., J. Fernandez-Martinez, Z. Hakhverdyan, and M.P. Rout. 2015. Protein Complex Purification by Affinity Capture. In C. Boone (Ed.), Budding yeast: A laboratory manual. Cold Spring Harbor Press, Woodbury NY.
142. Makarov, A., E. Denisov, O. Lange, and S. Horning. 2006. Dynamic range of mass accuracy in LTQ Orbitrap hybrid mass spectrometer. J. Am. Soc. Mass Spectrom. 17:977-982.
143. Gauci, V.J., E.P. Wright, and J.R. Coorssen. 2011. Quantitative proteomics: assessing the spectrum of in-gel protein detection methods. J Chem Biol. 4:3-29.
144. Nguyen, V.Q., A. Ranjan, F. Stengel, D. Wei, R. Aebersold, C. Wu, and A.E. Leschziner. 2013. Molecular Architecture of the ATP-Dependent Chromatin-Remodeling Complex SWR1. Cell 154:1220-1231.
145. Gevaert, K. and J. Vandekerckhove. 2000. Protein identification methods in proteomics. Electrophoresis 21:1145-1154.
146. Shevchenko, A., H. Tomas, J. Havlis, J.V. Olsen, and M. Mann. 2006. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat. Protoc. 1:2856-2860.
147. Candiano, G., M. Bruschi, L. Musante, L. Santucci, G.M. Ghiggeri, B. Carnemolla, P. Orecchia, L. Zardi, and P.G. Righetti. 2004. Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis 25:1327-1333.
148. Berggren, K.N., B. Schulenberg, M.F. Lopez, T.H. Steinberg, A. Bogdanova, G. Smejkal, A. Wang, and W.F. Patton. 2002. An improved formulation of SYPRO Ruby protein gel stain: comparison with the original formulation and with a ruthenium II tris (bathophenanthroline disulfonate) formulation. Proteomics 2:486-498.
149. Chevallet, M., S. Luche, and T. Rabilloud. 2006. Silver staining of proteins in polyacrylamide gels. Nat. Protoc. 1:1852-1858.
150. Mackintosh, J.A., H.-Y. Choi, S.-H. Bae, D.A. Veal, P.J. Bell, B.C. Ferrari, D.D. Van Dyk, N.M. Verrills, et al. 2003. A fluorescent natural product for ultra sensitive detection of proteins in one-dimensional and two-dimensional gel electrophoresis. Proteomics 3:2273-2288.
151. Zhang, Y., B.R. Fonslow, B. Shan, M.C. Baek, and J.R. Yates III. 2013. Protein analysis by shotgun/bottom-up proteomics. Chem. Rev. 113:2343-2394.
152. Boulon, S., Y. Ahmad, L. Trinkle-Mulcahy, C. Verheggen, A. Cobley, P. Gregor, E. Bertrand, M. Whitehorn, and A.I. Lamond. 2010. Establishment of a protein frequency library and its application in the reliable identification of specific protein interaction partners. Mol. Cell. Proteomics 9:861-879.
153. Tackett, A.J., J.A. DeGrasse, M.D. Sekedat, M. Oeffinger, M.P. Rout, and B.T. Chait. 2005. I-DIRT, a general method for distinguishing between specific and nonspecific protein interactions. J. Proteome Res. 4:1752-1756.
154. Oda, Y., K. Huang, F.R. Cross, D. Cowburn, and B.T. Chait. 1999. Accurate quantitation of protein expression and site-specific phosphorylation. Proc. Natl. Acad. Sci. USA 96:6591-6596.
155. Ong, S.-E., B. Blagoev, I. Kratchmarova, D.B. Kristensen, H. Steen, A. Pandey, and M. Mann. 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.
156. Breitkreutz, A., H. Choi, J.R. Sharom, L. Boucher, V. Neduva, B. Larsen, Z.-Y. Lin, B.-J. Breitkreutz, et al. 2010. A global protein kinase and phosphatase interaction network in yeast. Science 328:1043-1046.
157. Wiśniewski, J.R., A. Zougman, N. Nagaraj, and M. Mann. 2009. Universal sample preparation method for proteome analysis. Nat. Methods 6:359-362.
158. Wiśniewski, J.R., P. Ostasiewicz, and M. Mann. 2011. High recovery FASP applied to the proteomic analysis of microdissected formalin fixed paraffin embedded cancer tissues retrieves known colon cancer markers. J. Proteome Res. 10:3040-3049.
159. Wiśniewski, J.R., D.F. Zielinska, and M. Mann. 2011. Comparison of ultrafiltration units for proteomic and N-glycoproteomic analysis by the filter-aided sample preparation method. Anal. Biochem. 410:307-309.
160. Fischer, R., and B.M. Kessler. Gel-aided sample preparation (GASP) -a simplified method for gel-assisted proteomic sample generation from protein extracts and intact cells. Proteomics. (In press.).
161. Speicher, K.D., O. Kolbas, S. Harper, and D. Speicher. 2000. Systematic analysis of peptide recoveries from in-gel digestions for protein identifications in proteome studies. J. Biomol. Tech. 11:74-86.
162. Bell, A.W., T. Nilsson, R.E. Kearney, and J.J.M. Bergeron. 2007. The protein microscope: Incorporating mass spectrometry into cell biology. Nat. Methods 4:783-784.
163. Uhlen, M., L. Fagerberg, B.M. Hallström, C. Lindskog, P. Oksvold, A. Mardinoglu, A. Sivertsson, C. Kampf, et al. 2015. Proteomics. Tissue-based map of the human proteome. Science. 347:1260419.
164. Goll, J. and P. Uetz. 2006. The elusive yeast interactome. Genome Biol. 7:223.
165. Devos, D. and R.B. Russell. 2007. A more complete, complexed and structured interactome. Curr. Opin. Struct. Biol. 17:370-377.
166. Breitkreutz, B.-J., C. Stark, T. Reguly, L. Boucher, A. Breitkreutz, M. Livstone, R. Oughtred, D.H. Lackner, et al. 2008. The BioGRID interaction database: 2008 update. Nucleic Acids Res. 36:D637-D640.
167. Jancarik, J. and S.-H. Kim. 1991. Sparse matrix sampling. A screening method for crystallization of proteins. J Appl Crystallogr. 24:409-411.
168. Chayen, N.E. 2009. High-throughput protein crystallization. Adv Protein Chem Struct Biol. 77:1-22.
169. Montelione, G.T. 2012. The Protein Structure Initiative: achievements and visions for the future. F1000 Biol Rep 4:7.
170. Nie, Y., C. Viola, C. Bieniossek, S. Trowitzsch, L.S. Vijay-Achandran, M. Chaillet, F. Garzoni, and I. Berger. 2009. Getting a grip on complexes. Curr. Genomics 10:558-572.