Register      Login
Australian Journal of Chemistry Australian Journal of Chemistry Society
An international journal for chemical science
Shopping Cart: ( empty )
You are here: Home > Journals > CH > CH13164
RESEARCH FRONT
Contents Vol 66(7)

Chemical Cross-linking and Mass Spectrometry for the Structural Analysis of Protein Assemblies

Antonio N. Calabrese A and Tara L. Pukala A B
+ Author Affiliations
- Author Affiliations

A School of Chemistry and Physics, The University of Adelaide, Adelaide, SA 5005, Australia.

B Corresponding author. Email: tara.pukala@adelaide.edu.au




Antonio Calabrese is a Ph.D. candidate at the University of Adelaide under the supervision of both Dr Tara Pukala and Professor John H. Bowie. His research interests include the development of novel chemical cross-linking mass spectrometry methodologies and the use of complementary techniques to probe the structures of protein assemblies of biological importance.


Dr Tara Pukala obtained a Ph.D. from the University of Adelaide (with J. H. Bowie), which was followed by a postdoctoral role at the University of Cambridge, UK (with C. V. Robinson). She returned to a lectureship position at the University of Adelaide in 2008, where she has established a research group focussed on the development and application of mass spectrometric and related technologies for the investigation of biomolecular systems.

Australian Journal of Chemistry 66(7) 749-759 https://doi.org/10.1071/CH13164
Submitted: 8 April 2013  Accepted: 23 May 2013   Published: 1 July 2013

Abstract

Cellular functions are performed and regulated at a molecular level by the coordinated action of intricate protein assemblies, and hence the study of protein folding, structure, and interactions is vital to the appreciation and understanding of complex biological problems. In the past decade, continued development of chemical cross-linking methodologies combined with mass spectrometry has seen this approach develop to enable detailed structural information to be elucidated for protein assemblies often intractable by traditional structural biology methods. In this review article, we describe recent advances in reagent design, cross-linking protocols, mass spectrometric analysis, and incorporation of cross-linking constraints into structural models, which are contributing to overcoming the intrinsic challenges of the cross-linking method. We also highlight pioneering applications of chemical cross-linking mass spectrometry approaches to the study of structure and function of protein assemblies.


References

[1]  C. Clegg, D. Hayes, Eur. J. Biochem. 1974, 42, 21.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2cXktFSmt74%3D&md5=4cf3c76387df0f3a2a7cb16341072b69CAS | 4598101PubMed |

[2]  T. Sun, A. Bollen, L. Kahan, R. R. Traut, Biochem. 1974, 13, 2334.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2cXksVKlsrc%3D&md5=32034ff81fcc0a4ea5b302dd2640742eCAS |

[3]  R. Aebersold, M. Mann, Nature 2003, 422, 198.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhvFKgs7s%3D&md5=5bca9334fa0a1d79721bb915fee77311CAS | 12634793PubMed |

[4]  J. Rappsilber, J. Struct. Biol. 2011, 173, 530.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhvFWntb0%3D&md5=13e2b10bc4798a374959be25068bf7e9CAS | 21029779PubMed |

[5]  A. Leitner, T. Walzthoeni, A. Kahraman, F. Herzog, O. Rinner, M. Beck, R. Aebersold, Mol. Cell. Proteomics 2010, 9, 1634.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlWgtLrN&md5=5471c74d48cae86f3211753b69c44906CAS | 20360032PubMed |

[6]  D. Paramelle, G. Miralles, G. Subra, J. Martinez, Proteomics 2013, 13, 438.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlejsL0%3D&md5=7113b581c25672f00800423f1ae85f41CAS | 23255214PubMed |

[7]  Z. Grabarek, J. Gergely, Anal. Biochem. 1990, 185, 131.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXhtlGmtr0%3D&md5=e8257201c9a42ac8107a20a37549164eCAS | 2344038PubMed |

[8]  B. L. Simons, M. C. King, T. Cyr, M. A. Hefford, H. Kaplan, Protein Sci. 2002, 11, 1558.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktFWgs7k%3D&md5=575ce34850edb0a04c9b5978262a3dc6CAS | 12021454PubMed |

[9]  S. Mädler, C. Bich, D. Touboul, R. Zenobi, J. Mass Spectrom. 2009, 44, 694.
         | Crossref | GoogleScholarGoogle Scholar | 19132714PubMed |

[10]  S. Kalkhof, A. Sinz, Anal. Bioanal. Chem. 2008, 392, 305.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFeiurrO&md5=e47e9d5c6be8b769cad5e9926a2634f0CAS | 18724398PubMed |

[11]  C. L. Swain, J. B. Smith, D. L. Smith, J. Am. Soc. Mass Spectrom. 2004, 15, 736.
         | Crossref | GoogleScholarGoogle Scholar |

[12]  O. V. Kovalenko, X. H. Yang, M. E. Hemler, Mol. Cell. Proteomics 2007, 6, 1855.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVeisbrK&md5=0150ede27c1b7c0914200b36a70e0962CAS | 17644758PubMed |

[13]  Y. Kim, S. O. Ho, N. R. Gassman, Y. Korlann, E. V. Landorf, F. R. Collart, S. Weiss, Bioconjug. Chem. 2008, 19, 786.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXitVamsL0%3D&md5=5a9d61126e6ca9525117924e72d21d12CAS | 18275130PubMed |

[14]  A. F. Gomes, F. C. Gozzo, J. Mass Spectrom. 2010, 45, 892.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtV2rsL3M&md5=60d0610c50d6bf936c9cf191eecf7085CAS | 20635431PubMed |

[15]  G. A. Korshunova, N. V. Sumbatyan, A. N. Topin, M. T. Mtchedlidze, Mol. Biol. 2000, 34, 823.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhsF2gtg%3D%3D&md5=8671a1685569da4bd8dbcd0c64e1f39eCAS |

[16]  P. Novak, G. H. Kruppa, Eur. J. Mass Spectrom. 2008, 14, 355.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1KltLo%3D&md5=52a7fe863ea00e9b09109bfbcb666927CAS |

[17]  G. Bitan, D. B. Teplow, Acc. Chem. Res. 2004, 37, 357.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXitFSjsrw%3D&md5=8c9b9f4c4c777ea39c7451a32e4abed3CAS | 15196045PubMed |

[18]  G. Bitan, A. Lomakin, D. B. Teplow, J. Biol. Chem. 2001, 276, 35176.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmvFCksLs%3D&md5=769a37fa1e29fd7e5dfb2543f816d37eCAS | 11441003PubMed |

[19]  G. Bitan, M. D. Kirkitadze, A. Lomakin, S. S. Vollers, G. B. Benedek, D. B. Teplow, Proc. Natl. Acad. Sci. USA 2003, 100, 330.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXktlOlsg%3D%3D&md5=14d77973393305ec2e73d30b96aef70aCAS | 12506200PubMed |

[20]  B. Schilling, R. H. Row, B. W. Gibson, X. Guo, M. M. Young, J. Am. Soc. Mass Spectrom. 2003, 14, 834.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlvVCqtbo%3D&md5=dc53d489e2f9c100d015276613f25153CAS | 12892908PubMed |

[21]  D. R. Müller, P. Schindler, H. Towbin, U. Wirth, H. Voshol, S. Hoving, M. O. Steinmetz, Anal. Chem. 2001, 73, 1927.
         | Crossref | GoogleScholarGoogle Scholar | 11354472PubMed |

[22]  E. V. Petrotchenko, J. J. Serpa, C. H. Borchers, Anal. Chem. 2010, 82, 817.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFKlsg%3D%3D&md5=4cac654e243b7accf9c8d799bacb1ab9CAS | 20050626PubMed |

[23]  F. Chu, S. Mahrus, C. S. Craik, A. L. Burlingame, J. Am. Chem. Soc. 2006, 128, 10362.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xnt12ntrs%3D&md5=ca25fe3ee97c314291144692fbaf43f7CAS | 16895390PubMed |

[24]  T. Taverner, N. E. Hall, R. A. O’Hair, R. J. Simpson, J. Biol. Chem. 2002, 277, 46487.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovFKhuro%3D&md5=6482b770c5ed166c039ae8cd31c2e058CAS | 12235153PubMed |

[25]  J. W. Back, V. Notenboom, L. J. de Koning, A. O. Muijsers, T. K. Sixma, C. G. de Koster, L. de Jong, Anal. Chem. 2002, 74, 4417.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xls1ajtbs%3D&md5=95fa137ea8ba61a60dc27264a7522d02CAS | 12236350PubMed |

[26]  B. X. Huang, H.-Y. Kim, C. Dass, J. Am. Soc. Mass Spectrom. 2004, 15, 1237.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtVSqtrs%3D&md5=8643fc7aa3a33df4865b32c9dc8505deCAS | 15276171PubMed |

[27]  X. Chen, Y. H. Chen, V. E. Anderson, Anal. Biochem. 1999, 273, 192.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlsFyitLs%3D&md5=0f564b454faa27250e426033ee09cfe8CAS | 10469490PubMed |

[28]  A. Zelter, M. R. Hoopmann, R. Vernon, D. Baker, M. J. MacCoss, T. N. Davis, J. Proteome Res. 2010, 9, 3583.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmsFOktr0%3D&md5=893efb01155afbf5bf1a538213ddf4d8CAS | 20476776PubMed |

[29]  L. Fischer, Z. A. Chen, J. Rappsilber, J. Proteomics 2013,
         | Crossref | GoogleScholarGoogle Scholar | 23541715PubMed |

[30]  D. Ilver, A. Arnqvist, J. Ögren, I.-M. Frick, D. Kersulyte, E. T. Incecik, D. E. Berg, A. Covacci, L. Engstrand, T. Borén, Science 1998, 279, 373.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmtlyqtQ%3D%3D&md5=d5de1eb9146d5391e641d37637521e7bCAS | 9430586PubMed |

[31]  K. M. Bobofchak, E. Tarasov, K. W. Olsen, Biochim Biophys Acta 2008, 1784, 1410.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFCkurfL&md5=f7d758f49fd476b3abe4159d736dc07cCAS | 18298961PubMed |

[32]  B. Paoli, R. Pellarin, A. Caflisch, J. Phys. Chem. B 2010, 114, 2023.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXot1Kntw%3D%3D&md5=2d2834e7072b0d89032f04ac253f36a6CAS | 20088553PubMed |

[33]  M. Trester-Zedlitz, K. Kamada, S. K. Burley, D. Fenyö, B. T. Chait, T. W. Muir, J. Am. Chem. Soc. 2003, 125, 2416.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXptV2lug%3D%3D&md5=8ec0c9ae4b8c4ebad962839f852d6726CAS | 12603129PubMed |

[34]  S. Kang, L. Mou, J. Lanman, S. Velu, W. J. Brouillette, P. E. Prevelige, Rapid Commun. Mass Spectrom. 2009, 23, 1719.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtVKmtLk%3D&md5=2862eb151f06643f88e5981c7e9f611bCAS | 19412923PubMed |

[35]  D. Vellucci, A. Kao, R. Kaake, S. Rychnovsky, L. Huang, J. Am. Soc. Mass Spectrom. 2010, 21, 1432.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXps1eitr4%3D&md5=6b9484de2b9fb77a424d2801b0eb0b79CAS | 20472459PubMed |

[36]  S. M. Chowdhury, X. Du, N. Tolić, S. Wu, R. J. Moore, M. U. Mayer, R. D. Smith, J. N. Adkins, Anal. Chem. 2009, 81, 5524.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmvVemtLg%3D&md5=d9c8ae3f0a539bae08a640c9241f0b17CAS | 19496583PubMed |

[37]  M. A. Nessen, G. Kramer, J. Back, J. M. Baskin, L. E. J. Smeenk, L. J. de Koning, J. H. van Maarseveen, L. de Jong, C. R. Bertozzi, H. Hiemstra, C. G. de Koster, J. Proteome Res. 2009, 8, 3702.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtlKitbg%3D&md5=32e25e947a53ec0a893be9056274887aCAS | 19402736PubMed |

[38]  C. H. Sohn, H. D. Agnew, J. E. Lee, M. J. Sweredoski, R. L. J. Graham, G. T. Smith, S. Hess, G. Czerwieniec, J. A. Loo, J. R. Heath, R. J. Deshaies, J. L. Beauchamp, Anal. Chem. 2012, 84, 2662.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XisFSiurc%3D&md5=d0a504da46f52def93ba942adcaf5ff5CAS | 22339618PubMed |

[39]  H. Buncherd, M. A. Nessen, N. Nouse, S. K. Stelder, W. Roseboom, H. L. Dekker, J. C. Arents, L. E. Smeenk, M. J. Wanner, J. H. van Maarseveen, X. Yang, P. J. Lewis, L. J. de Koning, C. G. de Koster, L. de Jong, J. Proteomics 2012, 75, 2205.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xis1Ortbo%3D&md5=1ccda6d3626638463b04638f167472a9CAS | 22326961PubMed |

[40]  F. Yan, F.-Y. Che, D. Rykunov, E. Nieves, A. Fiser, L. M. Weiss, R. Hogue Angeletti, Anal. Chem. 2009, 81, 7149.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXptF2ltLg%3D&md5=d57adc68f70715e40e531b7d821912eeCAS | 19642656PubMed |

[41]  R. N. Wine, J. M. Dial, K. B. Tomer, C. H. Borchers, Anal. Chem. 2002, 74, 1939.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xit12msLs%3D&md5=803cf8a458959351e2d410cc12c78beaCAS | 12033289PubMed |

[42]  A. Sinz, K. Wang, Anal. Biochem. 2004, 331, 27.
         | 1:CAS:528:DC%2BD2cXls1Wlur4%3D&md5=ffbe498a6e4f4a3315f1f116255af2c8CAS | 15245993PubMed |

[43]  M. A. Lauber, J. P. Reilly, Anal. Chem. 2010, 82, 7736.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVKrsLzP&md5=1592548925185a868d9bf601d2afb42dCAS | 20795639PubMed |

[44]  E. V. Petrotchenko, V. K. Olkhovik, C. H. Borchers, Mol. Cell. Proteomics 2005, 4, 1167.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpsFalsL0%3D&md5=160888d5edfa4e3cc02ad56e25b48607CAS | 15901824PubMed |

[45]  L. Yang, X. Tang, C. R. Weisbrod, G. R. Munske, J. K. Eng, P. D. von Haller, N. K. Kaiser, J. E. Bruce, Anal. Chem. 2010, 82, 3556.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXksVagurg%3D&md5=07b9025bd832a5cc9c0d4a4bfe3f4e52CAS | 20373789PubMed |

[46]  E. J. Soderblom, M. B. Goshe, Anal. Chem. 2006, 78, 8059.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFChu7rI&md5=cd4db43ba03e9e2337cda9e3a0153731CAS | 17134140PubMed |

[47]  A. Kao, C.-l. Chiu, D. Vellucci, Y. Yang, V. R. Patel, S. Guan, A. Randall, P. Baldi, S. D. Rychnovsky, L. Huang, Mol. Cell. Proteomics 2011, 10, M110.002212.
         | Crossref | GoogleScholarGoogle Scholar | 20736410PubMed |

[48]  Y. Lu, M. Tanasova, B. Borhan, G. E. Reid, Anal. Chem. 2008, 80, 9279.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlWqtLjP&md5=cb86bca9e80554b7a267063db0364d74CAS | 19551991PubMed |

[49]  A. N. Calabrese, N. J. Good, T. Wang, J. He, J. H. Bowie, T. L. Pukala, J. Am. Soc. Mass Spectrom. 2012, 23, 1364.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVGhsLvF&md5=c6247dbb32d748b05a325bb7fd649aa6CAS | 22644737PubMed |

[50]  A. N. Calabrese, T. Wang, J. H. Bowie, T. L. Pukala, Rapid Commun. Mass Spectrom. 2013, 27, 238.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVCktr3I&md5=a2cea68af0dac5e76f1c89a3c46e24efCAS | 23239338PubMed |

[51]  M. W. Gardner, L. A. Vasicek, S. Shabbir, E. V. Anslyn, J. S. Brodbelt, Anal. Chem. 2008, 80, 4807.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmsF2gsbk%3D&md5=c1a05324b75096e03609ecf1a351c8ecCAS | 18517224PubMed |

[52]  S. M. Chowdhury, G. R. Munske, X. Tang, J. E. Bruce, Anal. Chem. 2006, 78, 8183.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1Sjtb7O&md5=99c7d36a1b6f46557a38518fa928025eCAS | 17165806PubMed |

[53]  M. J. Trnka, A. L. Burlingame, Mol. Cell. Proteomics 2010, 9, 2306.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlegt7jF&md5=954389457a2ace19e10c36bad97037efCAS | 20813910PubMed |

[54]  E. V. Petrotchenko, K. Xiao, J. Cable, Y. Chen, N. V. Dokholyan, C. H. Borchers, Mol. Cell. Proteomics 2009, 8, 273.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXitV2lu7c%3D&md5=f408cb693107279baf0aa04d4f7b5a9fCAS | 18838738PubMed |

[55]  J. W. Back, A. F. Hartog, H. L. Dekker, A. Muijsers, L. J. Koning, L. Jong, J. Am. Soc. Mass Spectrom. 2001, 12, 222.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXpsVyqsQ%3D%3D&md5=d40ee97829bf45979997cea2bbfa8858CAS | 11212007PubMed |

[56]  X. Tang, G. R. Munske, W. F. Siems, J. E. Bruce, Anal. Chem. 2005, 77, 311.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVSqsLfM&md5=dc3c1e191f947b79928d30b59dd53accCAS | 15623310PubMed |

[57]  A. Iglesias, L. A. Santos, F. Gozzo, J. Am. Soc. Mass Spectrom. 2009, 20, 557.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjs1ansLg%3D&md5=145fe7fc5614d30023bb6c08e792c007CAS | 19138533PubMed |

[58]  H. Zhang, X. Tang, G. R. Munske, N. Tolic, G. A. Anderson, J. E. Bruce, Mol. Cell. Proteomics 2009, 8, 409.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjt12jt7s%3D&md5=3ae1e9e3d04d4fbcd5e1fadbf084ac51CAS | 18936057PubMed |

[59]  M. Q. Müller, F. Dreiocker, C. H. Ihling, M. Schafer, A. Sinz, Anal. Chem. 2010, 82, 6958.
         | Crossref | GoogleScholarGoogle Scholar | 20704385PubMed |

[60]  F. Dreiocker, M. Q. Müller, A. Sinz, M. Schäfer, J. Mass Spectrom. 2010, 45, 178.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitVSmt78%3D&md5=6aede0b3d01e7514991abd3fd5481318CAS | 19950134PubMed |

[61]  B. Clifford-Nunn, H. D. H. Showalter, P. Andrews, J. Am. Soc. Mass Spectrom. 2012, 23, 201.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XltVaitbY%3D&md5=5e93edcfe360e86206e74666d1220bc3CAS | 22131227PubMed |

[62]  D. C. Perdian, Y. J. Lee, Anal. Chem. 2010, 82, 9393.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtleitbzK&md5=93b2b945830f1c9f45b2db5bd240d486CAS | 20977220PubMed |

[63]  O. Rinner, J. Seebacher, T. Walzthoeni, L. Mueller, M. Beck, A. Schmidt, M. Mueller, R. Aebersold, Nat. Methods 2008, 5, 315.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjvFOgu7w%3D&md5=f32d04bb49dadace1a01cec0cacebfceCAS | 18327264PubMed |

[64]  Z. A. Chen, A. Jawhari, L. Fischer, C. Buchen, S. Tahir, T. Kamenski, M. Rasmussen, L. Lariviere, J. Bukowski-Wills, M. Nilges, P. Cramer, J. Rappsilber, EMBO J. 2010, 29, 717.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlvFGkug%3D%3D&md5=04d5d94effb04a0bc52b32ee869a32b3CAS | 20094031PubMed |

[65]  B. Paizs, S. Suhai, Mass Spectrom. Rev. 2005, 24, 508.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlvFShsLg%3D&md5=003d08c4015603be216a39db5669419cCAS | 15389847PubMed |

[66]  L. M. Mikesh, B. Ueberheide, A. Chi, J. J. Coon, J. E. P. Syka, J. Shabanowitz, D. F. Hunt, Biochim. Biophys. Acta 2006, 1764, 1811.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlaltLzN&md5=18c0da4a3f92b3e21b6b5494a50a171eCAS | 17118725PubMed |

[67]  R. Bakhtiar, Z. Guan, Biotechnol. Lett. 2006, 28, 1047.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmsFCis7g%3D&md5=0334e5954b9059575928405b5726473dCAS | 16794768PubMed |

[68]  Y. J. Lee, L. L. Lackner, J. M. Nunnari, B. S. Phinney, J. Proteome Res. 2007, 6, 3908.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVegsrrP&md5=c917369d06da72a6d5646bbfd9d0f852CAS | 17854217PubMed |

[69]  A. Maiolica, D. Cittaro, D. Borsotti, L. Sennels, C. Ciferri, C. Tarricone, A. Musacchio, J. Rappsilber, Mol. Cell. Proteomics 2007, 6, 2200.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXksF2hsg%3D%3D&md5=6a8697a99c6b602f21a607da5a026a3eCAS | 17921176PubMed |

[70]  P. Singh, S. A. Shaffer, A. Scherl, C. Holman, R. A. Pfuetzner, T. J. Larson Freeman, S. I. Miller, P. Hernandez, R. D. Appel, D. R. Goodlett, Anal. Chem. 2008, 80, 8799.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1yitbnI&md5=38f6666d5af6bf595a790e536826f290CAS | 18947195PubMed |

[71]  B. Yang, Y.-J. Wu, M. Zhu, S.-B. Fan, J. Lin, K. Zhang, S. Li, H. Chi, Y.-X. Li, H.-F. Chen, S.-K. Luo, Y.-H. Ding, L.-H. Wang, Z. Hao, L.-Y. Xiu, S. Chen, K. Ye, S.-M. He, M.-Q. Dong, Nat. Methods 2012, 9, 904.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XpvFClu74%3D&md5=a63776ec837a940c53b49ccb972f75b4CAS | 22772728PubMed |

[72]  T. Walzthoeni, M. Claassen, A. Leitner, F. Herzog, S. Bohn, F. Forster, M. Beck, R. Aebersold, Nat. Methods 2012, 9, 901.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XpvFGit7w%3D&md5=eb59553518bcc6f01caac5c9983931ccCAS | 22772729PubMed |

[73]  T. F. Havel, G. M. Crippen, I. D. Kuntz, Biopolymers 1979, 18, 73.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXhtlCitLo%3D&md5=eb3857f60ecb04e89a7b0a24960dd1e5CAS |

[74]  A. Sinz, Mass Spectrom. Rev. 2006, 25, 663.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmslOqurs%3D&md5=ce5fe3de79af5e65384f8ae8114e1c0bCAS | 16477643PubMed |

[75]  Y. Jin Lee, Mol. Biosyst. 2008, 4, 816.
         | Crossref | GoogleScholarGoogle Scholar | 18633483PubMed |

[76]  C. Tang, G. M. Clore, J. Biomol. NMR 2006, 36, 37.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVSitb%2FO&md5=0e8be7c5857a6d14887c0de163864344CAS | 16967193PubMed |

[77]  D. M. Schulz, S. Kalkhof, A. Schmidt, C. Ihling, C. Stingl, K. Mechtler, O. Zschörnig, A. Sinz, Proteins 2007, 69, 254.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVykt7rK&md5=6da1edcf62327dadd5908fdfc03b04d3CAS | 17607745PubMed |

[78]  M. Heymann, D. Paramelle, G. Subra, E. Forest, J. Martinez, C. Geourjon, G. Deléage, Bioinformatics 2008, 24, 2782.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVWmsrbJ&md5=64cd8f1d03e5e7954dc7fa3af8af187aCAS | 18826958PubMed |

[79]  Y. S. Choi, J.-S. Yang, Y. Choi, S. H. Ryu, S. Kim, Proteins 2009, 77, 14.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVChtLnJ&md5=c04c06ef742d220ada12edc30d10a996CAS | 19350617PubMed |

[80]  F. Chu, J. C. Maynard, G. Chiosis, C. V. Nicchitta, A. L. Burlingame, Protein Sci. 2006, 15, 1260.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XlsVKqtb8%3D&md5=d878b95f5af8216badbf05f31c10ebd9CAS | 16731965PubMed |

[81]  F. Chu, S.-o. Shan, D. T. Moustakas, F. Alber, P. F. Egea, R. M. Stroud, P. Walter, A. L. Burlingame, Proc. Natl. Acad. Sci. USA 2004, 101, 16454.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVOisbrL&md5=fd2f4ae5e576cc0235b88314802899faCAS | 15546976PubMed |

[82]  T. Pimenova, A. Nazabal, B. Roschitzki, J. Seebacher, O. Rinner, R. Zenobi, J. Mass Spectrom. 2008, 43, 185.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXivFeitr4%3D&md5=96f90fd18c6da45fe7e336272fe2b51eCAS | 17924399PubMed |

[83]  K. Dimova, S. Kalkhof, I. Pottratz, C. Ihling, F. Rodriguez-Castaneda, T. Liepold, C. Griesinger, N. Brose, A. Sinz, O. Jahn, Biochemistry 2009, 48, 5908.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmsleis7Y%3D&md5=6b5e83be24a4b2ddc10ad8c2cf362378CAS | 19492809PubMed |

[84]  C. Ciferri, S. Pasqualato, E. Screpanti, G. Varetti, S. Santaguida, G. Dos Reis, A. Maiolica, J. Polka, J. G. De Luca, P. De Wulf, M. Salek, J. Rappsilber, C. A. Moores, E. D. Salmon, A. Musacchio, Cell 2008, 133, 427.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmt1Smtb0%3D&md5=90a68fdaa36c48acaded7a8f9baedd4dCAS | 18455984PubMed |

[85]  F. Stengel, R. Aebersold, C. V. Robinson, Mol. Cell. Proteomics 2012, 11, R111.013027.
         | Crossref | GoogleScholarGoogle Scholar |

[86]  I. G. Muñoz, H. Yébenes, M. Zhou, P. Mesa, M. Serna, A. Y. Park, E. Bragado-Nilsson, A. Beloso, G. de Cárcer, M. Malumbres, C. V. Robinson, J. M. Valpuesta, G. Montoya, Nat. Struct. Mol. Biol. 2011, 18, 14.
         | Crossref | GoogleScholarGoogle Scholar | 21151115PubMed |

[87]  S. Bohn, F. Beck, E. Sakata, T. Walzthoeni, M. Beck, R. Aebersold, F. Förster, W. Baumeister, S. Nickell, Proc. Natl. Acad. Sci. USA 2010, 107, 20992.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFyrsbbN&md5=7eab15c50a644cf53106be34bec6ac54CAS | 21098295PubMed |

[88]  F. Herzog, A. Kahraman, D. Boehringer, R. Mak, A. Bracher, T. Walzthoeni, A. Leitner, M. Beck, F. U. Hartl, N. Ban, L. Malmstrom, R. Aebersold, Science 2012, 337, 1348.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtlaitL%2FL&md5=b789ffe9f43fa01c26431fd29034056aCAS | 22984071PubMed |

[89]  G. Schmitt-Ulms, K. Hansen, J. Liu, C. Cowdrey, J. Yang, S. J. DeArmond, F. E. Cohen, S. B. Prusiner, M. A. Baldwin, Nat. Biotechnol. 2004, 22, 724.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXksV2gtrg%3D&md5=bf84ec5901d3a4fd06e603bf45c52c6fCAS | 15146195PubMed |

[90]  M. Suchanek, A. Radzikowska, C. Thiele, Nat. Methods 2005, 2, 261.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXisFejtbc%3D&md5=8aa193829534b3d4a47e72df1155bad8CAS | 15782218PubMed |

[91]  L. Yang, C. Zheng, C. R. Weisbrod, X. Tang, G. R. Munske, M. R. Hoopmann, J. K. Eng, J. E. Bruce, J. Proteome Res. 2012, 11, 1027.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1ajtr7K&md5=920d0698642fa0c7c73785ae5dc94681CAS | 22168182PubMed |

[92]  C. R. Weisbrod, J. D. Chavez, J. K. Eng, L. Yang, C. Zheng, J. E. Bruce, J. Proteome Res. 2013, 12, 1569.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXltV2mtr8%3D&md5=5edb6648f9e8f4b0d48582fe826db098CAS |