Peptidomics: The integrated approach of MS, hyphenated techniques and bioinformatics for neuropeptide analysis
Bart Landuyt
Laboratory for Functional Genomics and Proteomics, Leuven, Belgium. Fax: +32-16-323902
Search for more papers by this authorGeert Baggerman
Laboratory for Functional Genomics and Proteomics, Leuven, Belgium. Fax: +32-16-323902
Search for more papers by this authorSteven J. Husson
Laboratory for Functional Genomics and Proteomics, Leuven, Belgium. Fax: +32-16-323902
Search for more papers by this authorJurgen Huybrechts
Laboratory for Functional Genomics and Proteomics, Leuven, Belgium. Fax: +32-16-323902
Search for more papers by this authorLiliane Schoofs
Laboratory for Functional Genomics and Proteomics, Leuven, Belgium. Fax: +32-16-323902
Search for more papers by this authorBart Landuyt
Laboratory for Functional Genomics and Proteomics, Leuven, Belgium. Fax: +32-16-323902
Search for more papers by this authorGeert Baggerman
Laboratory for Functional Genomics and Proteomics, Leuven, Belgium. Fax: +32-16-323902
Search for more papers by this authorSteven J. Husson
Laboratory for Functional Genomics and Proteomics, Leuven, Belgium. Fax: +32-16-323902
Search for more papers by this authorJurgen Huybrechts
Laboratory for Functional Genomics and Proteomics, Leuven, Belgium. Fax: +32-16-323902
Search for more papers by this authorLiliane Schoofs
Laboratory for Functional Genomics and Proteomics, Leuven, Belgium. Fax: +32-16-323902
Search for more papers by this authorAbstract
MS is currently one of the most important analytical techniques in biological and medical research. ESI and MALDI launched the field of MS into biology. The performance of mass spectrometers increased tremendously over the past decades. Other technological advances increased the analytical power of biological MS even more. First, the advent of the genome projects allowed an automated analysis of mass spectrometric data. Second, improved separation techniques, like nanoscale HPLC, are essential for MS analysis of biomolecules. The recent progress in bioinformatics is the third factor that accelerated the biochemical analysis of macromolecules. The first part of this review will introduce the basics of these techniques. The field that integrates all these techniques to identify endogenous peptides is called peptidomics and will be discussed in the last section. This integrated approach aims at identifying all the present peptides in a cell, organ or organism (the peptidome). Today, peptidomics is used by several fields of research. Special emphasis will be given to the identification of neuropeptides, a class of short proteins that fulfil several important intercellular signalling functions in every animal. MS imaging techniques and biomarker discovery will also be discussed briefly.
References
- [1]
Thomson, J. J.,
Rays of Positive Electricity and Their Applications to Chemical Analysis, Longmans Green, London 1913.
- [2]
Aston, F. W.,
Philos. Mag.
1919,
38,
707–714.
- [3]
Dempster, A. J.,
Phys. Rev.
1918,
11,
316–324.
- [4]
Mattauch, J.,
Herzog, R.,
Z. Phys.
1934,
89,
786–795.
- [5]
Tanaka, K.,
Waki, H.,
Ido, Y.,
Yoshida, Y.,
Yoshida, T.,
Rapid Commun. Mass Spectrom.
1988,
2,
151.
- [6]
Karas, M.,
Bachmann, D.,
Bahr, U.,
Hillenkamp, F.,
Int. J. Mass Spectrom. Ion Process.
1987,
78,
53–68.
- [7]
Fenn, J. B.,
Mann, M.,
Meng, C. K.,
Wong, S. F.,
Whitehouse, C. M.,
Science
1989,
246,
64–71.
- [8]
Murray, K. K.,
J. Mass Spectrom.
1996,
31,
1203–1215.
- [9]
Kriwacki, R. W.,
Wu, J.,
Siuzdak, G.,
Wright, P. E.,
J. Am. Chem. Soc.
1996,
118,
5320.
- [10]
Fuerstenau, S. D.,
Benner, W. H.,
Thomas, J. J.,
Brugidou, C.,
Bothner, B.,
Siuzdak, G.,
Angew. Chem. Int. Ed. Engl.
2001,
40,
542–544.
- [11]
Andren, P. E.,
Emmett, M. R.,
Caprioli, R.,
J. Am. Soc. Mass Spectrom.
1994,
5,
867–869.
- [12]
Clynen, E.,
Baggerman, G.,
Veelaert, D.,
Cerstiaens, A.,
Van der Horst, D.,
Harthoorn, L.,
Derua, R.,
Waelkens, E.,
De Loof, A.,
Schoofs, L.,
Eur. J. Biochem.
2001,
268,
1929–1939.
- [13]
Schulz-Knappe, P.,
Zucht, H. D.,
Heine, G.,
Jurgens, M.,
Hess, R.,
Schrader, M.,
Comb. Chem. High Throughput Screen.
2001,
4,
207–217.
- [14]
Verhaert, P.,
Uttenweiler-Joseph, S.,
de Vries, M.,
Loboda, A.,
Ens, W.,
Standing, K. G.,
Proteomics
2001,
1,
118–131.
- [15]
Klavdieva, M. M.,
Front. Neuroendocrinol.
1995,
16,
293–321.
- [16]
Wei, S.,
Feng, Y.,
Kalinina, E.,
Fricker, L. D.,
Life Sci.
2003,
73,
655–662.
- [17]
Johnson, G. D.,
Stevenson, T.,
Ahn, K.,
J. Biol. Chem.
1999,
274,
4053–4058.
- [18]
Mouse Genome Sequencing Consortium, Waterston, R. H.,
Lindblad-Toh, K.,
Birney, E.,
Rogers, J.,
Abril, J. F.,
Agarwal, P.,
Agarwala, R.,
Ainscough, R.,
Alexandersson, M.,
An, P.,
Antonarakis, S. E.,
Attwood, J.,
Baertsch, R.,
Bailey, J.,
Barlow, K.,
Beck, S.,
Berry, E, Birren, B.,
Bloom, T.,
Bork, P.,
Botcherby, M.,
Bray, N.,
Brent, M. R.,
Brown, D. G.,
Brown, S. D.,
Bult, C.,
Burton, J.,
Butler, J.,
Campbell, R. D.,
Carninci, P.,
Cawley, S.,
Chiaromonte, F.,
Chinwalla, A. T.,
Church, D. M.,
Clamp, M.,
Clee, C.,
Collins, F. S.,
Cook, L. L.,
Copley, R. R.,
Coulson, A.,
Couronne, O.,
Cuff, J.,
Curwen, V.,
Cutts, T.,
Daly, M.,
David, R.,
Davies, J.,
Delehaunty, K. D.,
Deri, J.,
Dermitzakis, E. T.,
Dewey, C.,
Dickens, N. J.,
Diekhans, M.,
Dodge, S.,
Dubchak, I.,
Dunn, D. M.,
Eddy, S. R.,
Elnitski, L.,
Emes, R. D.,
Eswara, P.,
Eyras, E.,
Felsenfeld, A.,
Fewell, G. A.,
Flicek, P.,
Foley, K.,
Frankel, W. N.,
Fulton, L. A.,
Fulton, R. S.,
Furey, T. S.,
Gage, D.,
Gibbs, R. A.,
Glusman, G.,
Gnerre, S.,
Goldman, N.,
Goodstadt, L.,
Grafham, D.,
Graves, T. A.,
Green, E. D.,
Gregory, S.,
Guigo, R.,
Guyer, M.,
Hardison, R. C.,
Haussler, D.,
Hayashizaki, Y.,
Hillier, L. W.,
Hinrichs, A.,
Hlavina, W.,
Holzer, T.,
Hsu, F.,
Hua, A.,
Hubbard, T.,
Hunt, A.,
Jackson, I.,
Jaffe, D. B.,
Johnson, L. S.,
Jones, M.,
Jones, T. A.,
Joy, A.,
Kamal, M.,
Karlsson, E. K.,
Karolchik, D.,
Kasprzyk, A.,
Kawai, J.,
Keibler, E.,
Kells, C.,
Kent, W. J.,
Kirby, A.,
Kolbe, D. L.,
Korf, I.,
Kucherlapati, R. S.,
Kulbokas, E. J.,
Kulp, D.,
Landers, T.,
Leger, J. P.,
Leonard, S.,
Letunic, I.,
Levine, R.,
Li, J.,
Li, M.,
Lloyd, C.,
Lucas, S.,
Ma, B.,
Maglott, D. R.,
Mardis, E. R.,
Matthews, L.,
Mauceli, E.,
Mayer, J. H.,
McCarthy, M.,
McCombie, W. R.,
McLaren, S.,
McLay, K.,
McPherson, J. D.,
Meldrim, J.,
Meredith, B.,
Mesirov, J. P.,
Miller, W.,
Miner, T. L.,
Mongin, E.,
Montgomery, K. T.,
Morgan, M.,
Mott, R.,
Mullikin, J. C.,
Muzny, D. M.,
Nash, W. E.,
Nelson, J. O.,
Nhan, M. N.,
Nicol, R.,
Ning, Z.,
Nusbaum, C.,
O'Connor, M. J.,
Okazaki, Y.,
Oliver, K.,
Overton-Larty, E.,
Pachter, L.,
Parra, G.,
Pepin, K. H.,
Peterson, J.,
Pevzner, P.,
Plumb, R.,
Pohl, C. S.,
Poliakov, A.,
Ponce, T. C.,
Ponting, C. P.,
Potter, S.,
Quail, M.,
Reymond, A.,
Roe, B. A.,
Roskin, K. M.,
Rubin, E. M.,
Rust, A. G.,
Santos, R.,
Sapojnikov, V.,
Schultz, B.,
Schultz, J.,
Schwartz, M. S.,
Schwartz, S.,
Scott, C.,
Seaman, S.,
Searle, S.,
Sharpe, T.,
Sheridan, A.,
Shownkeen, R.,
Sims, S.,
Singer, J. B.,
Slater, G.,
Smit, A.,
Smith, D. R.,
Spencer, B.,
Stabenau, A.,
Stange-Thomann, N.,
Sugnet, C.,
Suyama, M.,
Tesler, G.,
Thompson, J.,
Torrents, D.,
Trevaskis, E.,
Tromp, J.,
Ucla, C.,
Ureta-Vidal, A.,
Vinson, J. P.,
Von Niederhausern, A. C.,
Wade, C. M.,
Wall, M.,
Weber, R. J.,
Weiss, R. B.,
Wendl, M. C.,
West, A. P.,
Wetterstrand, K.,
Wheeler, R.,
Whelan, S.,
Wierzbowski, J.,
Willey, D.,
Williams, S.,
Wilson, R. K.,
Winter, E.,
Worley, K. C.,
Wyman, D.,
Yang, S.,
Yang, S. P.,
Zdobnov, E. M.,
Zody, M. C.,
Lander, E. S.,
Nature
2002,
420,
520–562.
- [19]
Adams, M. D.,
Celniker, S. E.,
Holt, R. A.,
Evans, C. A.,
Gocayne, J. D.,
Amanatides, P. G.,
Scherer, S. E.,
Li, P. W.,
Hoskins, R. A.,
Galle, R. F.,
George, R. A.,
Lewis, S. E.,
Richards, S.,
Ashburner, M.,
Henderson, S. N.,
Sutton, G. G.,
Wortman, J. R.,
Yandell, M. D.,
Zhang, Q.,
Chen, L. X.,
Brandon, R. C.,
Rogers, Y. H.,
Blazej, R. G.,
Champe, M.,
Pfeiffer, B. D.,
Wan, K. H.,
Doyle, C.,
Baxter, E. G.,
Helt, G.,
Nelson, C. R.,
Gabor, G. L.,
Abril, J. F.,
Agbayani, A.,
An, H. J.,
Andrews-Pfannkoch, C.,
Baldwin, D.,
Ballew, R. M.,
Basu, A.,
Baxendale, J.,
Bayraktaroglu, L.,
Beasley, E. M.,
Beeson, K. Y.,
Benos, P. V.,
Berman, B. P.,
Bhandari, D.,
Bolshakov, S.,
Borkova, D.,
Botchan, M. R.,
Bouck, J.,
Brokstein, P.,
Brottier, P.,
Burtis, K. C.,
Busam, D. A.,
Butler, H.,
Cadieu, E.,
Center, A.,
Chandra, I.,
Cherry, J. M.,
Cawley, S.,
Dahlke, C.,
Davenport, L. B.,
Davies, P.,
de Pablos, B.,
Delcher, A.,
Deng, Z.,
Mays, A. D.,
Dew, I.,
Dietz, S. M.,
Dodson, K.,
Doup, L. E.,
Downes, M.,
Dugan-Rocha, S.,
Dunkov, B. C.,
Dunn, P.,
Durbin, K. J.,
Evangelista, C. C.,
Ferraz, C.,
Ferriera, S.,
Fleischmann, W.,
Fosler, C.,
Gabrielian, A. E.,
Garg, N. S.,
Gelbart, W. M.,
Glasser, K.,
Glodek, A.,
Gong, F.,
Gorrell, J. H.,
Gu, Z.,
Guan, P.,
Harris, M.,
Harris, N. L.,
Harvey, D.,
Heiman, T. J.,
Hernandez, J. R.,
Houck, J.,
Hostin, D.,
Houston, K. A.,
Howland, T. J.,
Wei, M. H.,
Ibegwam, C.,
Jalali, M.,
Kalush, F.,
Karpen, G. H.,
Ke, Z.,
Kennison, J. A.,
Ketchum, K. A.,
Kimmel, B. E.,
Kodira, C. D.,
Kraft, C.,
Kravitz, S.,
Kulp, D.,
Lai, Z.,
Lasko, P.,
Lei, Y.,
Levitsky, A. A.,
Li, J.,
Li, Z.,
Liang, Y.,
Lin, X.,
Liu, X.,
Mattei, B.,
McIntosh, T. C.,
McLeod, M. P.,
McPherson, D.,
Merkulov, G.,
Milshina, N. V.,
Mobarry, C.,
Morris, J.,
Moshrefi, A.,
Mount, S. M.,
Moy, M.,
Murphy, B.,
Murphy, L.,
Muzny, D. M.,
Nelson, D. L.,
Nelson, D. R.,
Nelson, K. A.,
Nixon, K.,
Nusskern, D. R.,
Pacleb, J. M.,
Palazzolo, M.,
Pittman, G. S.,
Pan, S.,
Pollard, J.,
Puri, V.,
Reese, M. G.,
Reinert, K.,
Remington, K.,
Saunders, R. D.,
Scheeler, F.,
Shen, H.,
Shue, B. C.,
Siden-Kiamos, I.,
Simpson, M.,
Skupski, M. P.,
Smith, T.,
Spier, E.,
Spradling, A. C.,
Stapleton, M.,
Strong, R.,
Sun, E.,
Svirskas, R.,
Tector, C.,
Turner, R.,
Venter, E.,
Wang, A. H.,
Wang, X.,
Wang, Z. Y.,
Wassarman, D. A.,
Weinstock, G. M.,
Weissenbach, J.,
Williams, S. M.,
Woodage, T.,
Worley, K. C.,
Wu, D.,
Yang, S.,
Yao, Q. A.,
Ye, J.,
Yeh, R. F.,
Zaveri, J. S.,
Zhan, M.,
Zhang, G.,
Zhao, Q.,
Zheng, L.,
Zheng, X. H.,
Zhong, F. N.,
Zhong, W.,
Zhou, X.,
Zhu, S.,
Zhu, X.,
Smith, H. O.,
Gibbs, R. A.,
Myers, E. W.,
Rubin, G. M.,
Venter, J. C.,
Science
2000,
287,
2185–2195.
- [20]
The C. elegans Sequencing Consortium, Science 1998, 285, 1493.
- [21]
Tatemoto, K.,
Mutt, V.,
Nature
1980,
285,
417–418.
- [22]
Siuzdak, G.,
The Expanding Role of Mass Spectrometry in Biotechnology, 2nd Edn., MCC press, San Diego 2006.
- [23]
De Hoffmann, E.,
Stroobant, V.,
Mass Spectrometry Principles and Applications, 2nd Edn., Wiley, Chichester 2002.
- [24]
Gross, J. H.,
Mass Spectrometry: A Textbook, Springer, Heidelberg 2004.
- [25]
Jonsson, A. P.,
Cell. Mol. Life Sci.
2001,
58,
868–884.
- [26]
Nier, A. O.,
Rev. Sci. Instrum.
1947,
18,
415.
- [27]
Harrison, A. G.,
Chemical Ionization Mass Spectrometry, CRC Press, Boca Raton 1983.
- [28]
Mcfarlane, R. D.,
Torgesson, T. F.,
Science
1976,
191,
970.
- [29]
Barber, M.,
Bardoli, R. S.,
Sedgwick, R. D.,
Tyler, A. N.,
Nature
1981,
293,
270–275.
- [30]
Barber, M.,
Vickerman, J. C.,
Wolstenholme, J.,
J. Chem. Soc., Faraday Trans.
1980,
76,
549–559.
- [31]
Zenobi, R.,
Knochenmuss, R.,
Mass Spectrom. Rev.
1998,
17,
337–366.
- [32]
Börnsen, K. O.,
in: Chapman, J. R. (Ed.), Mass Spectrometry of Proteins and Peptides, Humana Press, NJ 2000, pp. 287–404.
- [33]
Kussman, M.,
Roepstorff, P.,
in: Chapman, J. R. (Ed.), Mass Spectrometry of Proteins and Peptides, Humana Press, NJ 2000, pp. 405–424.
- [34]
Pan, C.,
Xu, S.,
Zhou, H.,
Fu, Y.,
Ye, M.,
Zou, H.,
Anal. Bioanal. Chem.
2007,
387,
193–204.
- [35]
Wei, J.,
Buriak, J. M.,
Siuzdak, G.,
Nature
1999,
399,
243–246.
- [36]
Gobom, J.,
Nordhoff, E.,
Mirgorodskaya, E.,
Ekman, R.,
Roepstorff, P.,
Spectroscopy
1999,
24,
105–116.
- [37]
Holmes, L. D.,
Schiller, M. R.,
J. Liq. Chromatogr. Relat. Technol.
1997,
20,
123.
- [38]
Raska, C. S.,
Parker, C. E.,
Sunnarborg, S. W.,
Pope, R. M.,
Lee, D. C.,
Glish, G. L.,
Borchers, C. H.,
J. Am. Soc. Mass Spectrom.
2003,
14,
1076.
- [39]
Stoeckli, M.,
Chaurand, P.,
Hallahan, D. E.,
Caprioli, R. M.,
Nat. Med.
2001,
7,
493–496.
- [40]
Dole, M.,
Mack, L. L.,
Hines, R. L.,
Mobley, R. C.,
Ferguson, L.,
Alice, M. B.,
J. Chem. Phys.
1968,
49,
2240–2247.
- [41]
Alexandrov, M. L.,
Gall, L. N.,
Krasnov, N. V.,
Nikolaev, V. I.,
Pavlenko, V. A.,
Skhuzov, V. A.,
Bioorg. Khim.
1984,
10,
710–712.
- [42]
Taylor, G.,
Proc. R. Soc.
1964,
A280,
383–397.
- [43]
Kebarle, P.,
Ho, Y.,
in: Cole, R. B. (Ed.), Electrospray Ionization Mass Spectrometry: Fundamentals, Instrumentation and Applications, Wiley, New York 1997, pp. 3–63.
- [44]
Iribarne, J. V.,
Thomson, B. A.,
J. Chem. Phys.
1976,
64,
2287–2294.
- [45]
Bruins, A. P.,
J. Chromatogr.
1991,
554,
39–46.
- [46]
Richards, D.,
Verrier, H.,
Major, H.,
Rontree, J.,
Proc. 16th IMMS 1998, pp. 75.
- [47]
Emmett, M. R.,
Caprioli, R. M.,
J. Am. Soc. Mass Spectrom.
1994,
5,
605–613.
- [48]
Wilm, M.,
Mann, M.,
Anal. Chem.
1996,
68,
1–8.
- [49]
Stephens, W. E.,
Phys. Rev.
1946,
69,
691.
- [50]
Wiley, W. C.,
McLaren, I. H.,
Rev. Sci. Instrum.
1955,
26,
1150–1157.
- [51]
Mamyrin, B. A.,
Int. J. Mass Spectrom. Ion Proc.
1994,
131,
1–19.
- [52]
Cotter, R. J.,
Anal. Chem.
1992,
64,
1027A–1039A.
- [53]
Kaufmann, R.,
Kirsch, D.,
Spengler, B.,
Int. J. Mass Spectrom. Ion Proc.
1994,
131,
355–385.
- [54]
Cordero, M. M.,
Cornish, T. J.,
Cotter, R. J.,
Rapid Commun. Mass Spectrom.
1995,
91,
1356–1361.
- [55]
Dawson, J. H. J.,
Guilhaus, M.,
Rapid Commun. Mass Spectrom.
1989,
3,
155–159.
- [56]
Paul, W.,
Steinwedel, H.,
Naturforschung
1953,
8A,
448–450.
- [57]
Dawson, P. H.,
Mass Spectrom. Rev.
1986,
5,
1–37.
- [58]
Huang, Y.,
Guan, S.,
Kim, H. S.,
Marschall, A. G.,
Int. J. Mass Spectrom. Ion Proc.
1996,
152,
121–133.
- [59]
Lock, C. M.,
Dyer, E.,
Rapid Commun. Mass Spectrom.
1999,
13,
432–448.
- [60]
Yost, R. A.,
Enke, C. G.,
Anal. Chem.
1979,
51,
1251A–1262A.
- [61]
March, R. E.,
Rapid Commun. Mass Spectrom.
1998,
12,
1543–1554.
- [62]
Tolmachev, A. V.,
Udseth, H. R.,
Smith, R. D.,
Rapid Commun. Mass Spectrom.
2000,
14,
1907–1913.
- [63]
Comisarow, M. B.,
Marshall, A. G.,
J. Mass Spectrom.
1996,
31,
581–585.
- [64]
Comisarow, M. B.,
Marshall, A. G.,
Chem. Phys. Lett.
1974,
25,
282–283.
- [65]
Gauthier, J. W.,
Trautman, T. R.,
Jacobson, D. B.,
Anal. Chim. Acta
1991,
246,
211–225.
- [66]
Hu, Q.,
Noll, R. J.,
Li, H.,
Makarov, A.,
Hardman, M.,
Graham Cooks, R.,
J. Mass Spectrom.
2005,
40,
430–443.
- [67]
Shevchenko, A.,
Chernushevich, I. V.,
Ens, W.,
Standing, K. G.,
Thompson, B.,
Wilm, M.,
Mann, M.,
Rapid Commun. Mass Spectrom.
1997,
11,
1015–1024.
- [68]
Yergey, A. L.,
Coorssen, J. R.,
Backlund, P. S.,
Blank, P. S.,
Humphrey, G. A.,
Zimmerberg, J.,
Campbell, J. M.,
Vestal, M. L.,
J. Am. Soc. Mass Spectrom.
2002,
13,
784–791.
- [69]
Ehlers, M.,
Schmidt, S.,
Lee, B. J.,
Grotemeyer, J.,
Eur. J. Mass Spectrom.
2000,
6,
377–385.
- [70]
Edman, P.,
Begg, G.,
Eur. J. Biochem.
1967,
1,
80–91.
- [71]
Hunt, D. F.,
Buko, A. M.,
Ballard, J. M.,
Shabanowitz, J.,
Giordani, A. B.,
Biomed. Mass Spectrom.
1981,
8,
397–408.
- [72]
Papayannopoulos, I. A.,
Mass Spectrom. Rev.
1995,
14,
49–73.
- [73]
Johnson, R. S.,
Martin, S. A.,
Biemann, K.,
Stultz, J. T.,
Watson, J. T.,
Anal. Chem.
1987,
59,
2621–2625.
- [74]
Roepstorff, P.,
Fohlman, J.,
Biomed. Mass Spectrom.
1984,
11,
601.
- [75]
Biemann, K.,
Methods Enzymol.
1990,
193,
886–887.
- [76]
Polce, M. J.,
Ren, D.,
Wesdemiotis, C.,
J. Mass Spectrom.
2000,
35,
1391–1398.
- [77]
Wysocki, V. H.,
Tsaprailis, G.,
Smith, L. L.,
Breci, L. A.,
J. Mass Spectrom.
2000,
35,
1399–1406.
- [78]
Mabud, M. A.,
Dekrey, M. J.,
Cooks, R. G.,
Int. J. Mass Spectrom. Ion Proc.
1985,
67,
285–294.
- [79]
Patterson, D. H.,
Tarr, G. E.,
Regnier, F. E.,
Martin, S. A.,
Anal. Chem.
1995,
67,
3971–3978.
- [80]
Chait, B. T.,
Wang, R.,
Beavis, R. C.,
Kent, S. B. H.,
Science
1993,
262,
89–92.
- [81]
Hakansson, K.,
Cooper, H. J.,
Emmet, M. R.,
Costello, C. E.,
Marshall, A. G.,
Anal. Chem.
2001,
73,
4530–4536.
- [82]
Axelson, J.,
Palmblad, M.,
Hakansson, K.,
Hakansson, P.,
Rapid Commun. Mass Spectrom.
1999,
13,
474–477.
- [83]
Rissler, K.,
Katlein, R.,
Cramer, H.,
J. Chromatogr.
1993,
612,
150–155.
- [84]
Cohen, S. L.,
Chait, B. T.,
Anal. Chem.
1996,
68,
31.
- [85]
Beavis, R. C.,
Chait, B. T.,
Anal. Chem.
1990,
62,
1836.
- [86]
Baggerman, G.,
Vierstraete, E.,
De Loof, A.,
Schoofs, L.,
Comb. Chem. High Throughput Screen.
2005,
8,
669–677.
- [87]
Bogdanov, B.,
Smith, R. D.,
Mass Spectrom. Rev.
2005,
24,
168–200.
- [88]
Gevaert, K.,
Goethals, M.,
Martens, L.,
Van Damme, J.,
Staes, A.,
Thomas, G. R.,
Vandekerckhove, J.,
Nat. Biotechnol.
2003,
21,
566–569.
- [89]
McFadden, W. H.,
Schwartz, H. L.,
Evans, S.,
J. Chromatogr.
1976,
122,
389–396.
- [90]
Wilougby, R. C.,
Browner, R. F.,
Anal. Chem.
1984,
56,
2626.
- [91]
Caprioli, R. M.,
Fan, T.,
Cotrell, J. S.,
Anal. Chem.
1986,
58,
2949–2954.
- [92]
Chesnov, S.,
Bigler, L.,
Hesse, M.,
Eur. Mass Spectrom.
2002,
8,
1–16.
- [93]
Robb, D. B.,
Covey, T. R.,
Bruins, A. P.,
Anal. Chem.
2000,
72,
3653–3659.
- [94]
Williams, J. D.,
Burinsky, D. J.,
Int. J. Mass Spectrom.
2001,
212,
111–133.
- [95]
Shen, Y.,
Zhao, R.,
Berger, S. J.,
Anderson, G. A.,
Rodriguez, N.,
Anal. Chem.
2002,
74,
4235–4239.
- [96]
Thomas, R.,
Spectroscopy
2001,
16,
28–37.
- [97]
Shen, Y.,
Smith, R. D.,
Electrophoresis
2002,
23,
3106–3124.
- [98]
Ericson, C.,
Phung, Q. T.,
Horn, D. M.,
Peters, E. C.,
Fitchett, J. R.,
Ficarro, S. B.,
Salomon, A. R.,
Brill, L. M.,
Brock, A.,
Anal. Chem.
2003,
75,
2309–2315.
- [99]
Issaq, H. J.,
Chan, K. C.,
Janini, G. M.,
Conrads, T. P.,
Veenstra, T. D.,
J. Chromatogr. B
2005,
817,
38–47.
- [100]
Baggerman, G.,
Boonen, K.,
Verleyen, P.,
De Loof, A.,
Schoofs, L.,
J. Mass Spectrom.
2006,
40,
250–260.
- [101]
Canas, B.,
Pineiro, C.,
Calvo, E.,
Lopez-Ferrer, D.,
Gallardo, J. M.,
J. Chromatogr. A
2007,
1153,
235–258.
- [102]
Washburn, M. P.,
Wolters, D.,
Yates, J. R.,
Nat. Biotechnol.
2001,
19,
242–247.
- [103]
Amini, A.,
Chakraborty, F. E.,
Regnier, J.,
J. Chromatogr. B.
2002,
772,
35.
- [104]
Che, F. Y.,
Yan, L.,
Li, H.,
Mzhavia, N.,
Devi, L. A.,
Fricker, L. D.,
Proc. Natl. Acad. Sci. USA
2001,
98,
9971–9976.
- [105]
Smith, R. D.,
Baringa, C. J.,
Udseth, H. R.,
Anal. Chem.
1988,
60,
1948–1952.
- [106]
Olivares, J. A.,
Nguyen, N. T.,
Yonker, C. R.,
Smith, R. D.,
Anal. Chem.
1987,
59,
1230–1232.
- [107]
Barnidge, D. R.,
Nilsson, S.,
Markides, K. E.,
Rapp, H.,
Hjort, K.,
Rapid Commun. Mass Spectrom.
1999,
13,
994–1002.
- [108]
Chang, Y.,
Her, G. R.,
Anal. Chem.
2000,
72,
626–630.
- [109]
Jäverfalk-Hoyes, E. M.,
Bondesson, U.,
Westerlund, D.,
Andren, P. E.,
Electrophoresis
1999,
20,
1527–1532.
- [110]
Stutz, H.,
Electrophoresis
2005,
26,
1254–1290.
- [111]
Monton, M. R.,
Terabe, S.,
Anal. Sci.
2005,
21,
5–13.
- [112]
Simpson, D. C.,
Smith, R. D.,
Electrophoresis
2005,
26,
1291–1305.
- [113]
Kasicka, V.,
Electrophoresis
2006,
27,
142–175.
- [114]
Miksik, I.,
Sedlakova, P.,
J. Sep. Sci.
2007,
30,
1686–1703.
- [115]
Woods, A. S.,
Ugarov, M.,
Egan, T.,
Koomen, J.,
Gillig, K. J.,
Fuhrer, K.,
Gonin, M.,
Schultz, J. A.,
Anal. Chem.
2004,
76,
2187–2195.
- [116]
Liu, X.,
Valentine, S. J.,
Plasencia, M. D.,
Trimpin, S.,
Naylor, S.,
Clemmer, D. E.,
J. Am. Soc. Mass Spectrom.
2007,
18,
1249–1264.
- [117]
Merenbloom, S. I.,
Koeniger, S. L.,
Valentine, S. J.,
Plasencia, M. D.,
Clemmer, D. E.,
Anal. Chem.
2006,
78,
2802–2809.
- [118]
Merenbloom, S. I.,
Bohrer, B. C.,
Koeniger, C. L.,
Clemmer, D. E.,
Anal. Chem.
2007,
79,
515–522.
- [119]
Shadforth, I.,
Crowther, D.,
Bessant, C.,
Proteomics
2005,
5,
4082–4095.
- [120]
Xu, C.,
Ma, B.,
Drug Discov. Today
2006,
1,
595–600.
- [121]
Perkins, D. N.,
Pappin, D. J.,
Creasy, D. M.,
Cottrell, J. S.,
Electrophoresis
1999,
20,
3551–3567.
- [122]
Eng, J. K.,
McCormack, A. L.,
Yates, I. I. I.,
J. Am. Soc. Mass Spectrom.
1994,
5,
976–989.
- [123]
Ma, B.,
Zhang, K. Z.,
Hendrie, C.,
Liang, C. Z.,
Ming, L.,
Doherty-Kirby, A.,
Lajoie, G.,
Rapid Commun. Mass Spectrom.
2003,
17,
2337–2342.
- [124]
Frank, A.,
Pevzner, P.,
Anal. Chem.
2005,
77,
964–973.
- [125]
Taylor, J. A.,
Johnson, R. S.,
Rapid Commun. Mass Spectrom.
1997,
11,
1067–1075.
- [126]
Vanden Broeck, J.,
Peptides
2001,
22,
241–254.
- [127]
Hewes, R. S.,
Taghert, P. H.,
Genome Res.
2001,
11,
1126–1142.
- [128]
Liu, F.,
Baggerman, G.,
Schoofs, L.,
Wets, G.,
Peptides
2006,
27,
3137–3153.
- [129]
Mirabeau, O.,
Perlas, E.,
Severini, C.,
Audero, E.,
Gascuel, O.,
Rossenti, R.,
Birney, E.,
Rosenthal, N.,
Gross, C.,
Genome Res.
2007,
17,
320–327.
- [130]
Liu, F.,
Baggerman, G.,
D'Hertog, W.,
Verleyen, P.,
Schoofs, L.,
Wets, G.,
Mol. Cell. Proteomics
2006,
5,
510–522.
- [131]
Zamyatin, A. A.,
Borchikov, A. S.,
Vladimirov, M. G.,
Voronina, O. L.,
Nucleic Acids Res.
2006,
34,
D261–D266.
- [132]
Falth, M.,
Skold, K.,
Norrman, M.,
Svensson, M.,
Andren, P. E.,
Mol. Cell. Proteomics
2006,
5,
998–1005.
- [133]
Emanuelsson, O.,
Nielsen, H.,
Brunak, S.,
Von Heijne, G.,
J. Mol. Biol.
2000,
300,
1005–1016.
- [134]
Nielsen, H.,
Brunak, S.,
Von Heijne, G.,
Protein Eng.
1999,
12,
3–9.
- [135]
Southey, B. R.,
Amare, A.,
Zimmerman, T. A.,
Rodriguez-Zas, S. L.,
Sweedler, J. V.,
Nucleic Acids Res.
2006,
34,
W267–W272.
- [136]
Veenstra, J. A.,
Arch. Insect Biochem. Physiol.
2000,
43,
49–63.
- [137]
Hummon, A. B.,
Kelley, W. P.,
Sweedler, J. V.,
J. Neurochem.
2002,
82,
1398–1405.
- [138]
Konkoy, C. S.,
Davis, T. P.,
Trends Pharmacol. Sci.
1996,
17,
288–294.
- [139]
Baggerman, G.,
Verleyen, P.,
Clynen, E.,
Huybrechts, J.,
De Loof, A.,
Schoofs, L.,
J. Chromatogr. B Analyt. Technol. Biomed. Life Sci.
2004,
803,
3–16.
- [140]
Svensson, M.,
Sköld, K.,
Nilsson, A.,
Fälth, M.,
Svenningsson, P.,
Andren, P. E.,
Biochem. Soc. Trans.
2007,
35,
588–593.
- [141]
Soloviev, M.,
Finch, P.,
J. Chromatogr. B Analyt. Technol. Biomed. Life Sci.
2005,
815,
11–24.
- [142]
Ivanov, V. T.,
Yatskin, O. N.,
Expert Rev. Proteomics
2005,
2,
463–473.
- [143]
Caldwell, R. L.,
Caprioli, R. M.,
Mol. Cell. Proteomics
2005,
4,
394–401.
- [144]
Diamandis, E. P.,
J. Proteome Res.
2006,
5,
2079–2082.
- [145]
Schulte, I.,
Tammen, H.,
Selle, H.,
Schulz-Knappe, P.,
Expert. Rev. Mol. Diagn.
2005,
5,
145–157.
- [146]
Tammen, H.,
Hess, R.,
Schulte, I.,
Kellman, M.,
Appel, A.,
Budde, P.,
Zucht, H. D.,
Schulz-Knappe, P.,
Comb. Chem. High Throughput Screen.
2005,
8,
734–741.
- [147]
Brantl, V.,
Gramsch, C.,
Lottspeich, F.,
Mertz, R.,
Jaeger, K. H.,
Eur. J. Pharmacol.
1986,
125,
309–310.
- [148]
Boonen, K.,
Husson, S. J.,
Baggerman, G.,
Cerstiaens, A.,
Luyten, W.,
Schoofs, L.,
in: Soloviev, M., Shaw, C., Andren, P. E. (Eds.), Peptidomics: Methods and Applications, Wiley, Hoboken 2007, pp. 355–386.
- [149]
Boonen, K.,
Baggerman, G.,
D'Hertog, W.,
Husson, S. J.,
Overbergh, L.,
Mathieu, C.,
Schoofs, L.,
Gen. Comp. Endocrinol.
2007,
152,
231–241.
- [150]
Dowell, J. A.,
Vander Heyden, W.,
Lingjun, Li,
J. Proteome. Res.
2006,
5,
3368–3375.
- [151]
Che, F. Y.,
Lim, J.,
Pan, H.,
Biswas, R.,
Fricker, L. D.,
Mol. Cell. Proteomics
2005,
4,
1391–1405.
- [152]
Hummon, A. B.,
Amare, A.,
Sweedler, J. V.,
Mass Spectrom. Rev.
2006,
25,
77–98.
- [153]
Predel, R.,
J. Comp. Neurol.
2001,
436,
363–375.
- [154]
Huybrechts, J.,
Nusbaum, M. P.,
Vanden Bosch, L.,
Baggerman, G.,
De Loof, A.,
Schoofs, L.,
Biochem. Biophys. Res. Commun.
2003,
308,
535–544.
- [155]
Verleyen, P.,
Huybrechts, J.,
Sas, F.,
Clynen, E.,
Baggerman, G.,
De Loof, A.,
Schoofs, L.,
Biochem. Biophys. Res. Commun.
2004,
316,
763–770.
- [156]
Honey Bee Genome Sequencing Consortium, Nature 2006, 443, 931.
- [157]
Baggerman, G.,
Cerstiaens, A.,
De Loof, A.,
Schoofs, L.,
J. Biol. Chem.
2002,
277,
40368–40374.
- [158]
Husson, S. J.,
Clynen, E.,
Baggerman, G.,
De Loof, A.,
Schoofs, L.,
Biochem. Biophys. Res. Commun.
2005,
355,
76–86.
- [159]
Hummon, A. B.,
Richmond, T. A.,
Verleyen, P.,
Baggerman, G.,
Huybrechts, J.,
Ewing, M. A.,
Vierstraete, E.,
Rodriguez-Zas, S. L.,
Schoofs, L.,
Robinson, G. E.,
Sweedler, J. V.,
Science
2006,
314,
578–579.
- [160]
Uttenweiler-Joseph, S.,
Moniatte, M.,
Lagueux, M.,
Van Dorsselaer, A.,
Hoffmann, J. A.,
Bulet, P.,
Proc. Natl. Acad. Sci. USA
1998,
95,
11342–11347.
- [161]
Clynen, E.,
Stubbe, D.,
De Loof, A.,
Schoofs, L.,
Comp. Biochem. Physiol. B Biochem. Mol. Biol.
2002,
132,
107–115.
- [162]
Huybrechts, J.,
De Loof, A.,
Schoofs, L.,
Biochem. Biophys. Res. Commun.
2004,
317,
909–916.
- [163]
Predel, R.,
Gäde, G.,
Peptides
2005,
26,
3–9.
- [164]
Husson, S. J.,
Clynen, E.,
Baggerman, G.,
Janssen, T.,
Schoofs, L.,
J. Neurochem.
2006,
98,
1999–2012.
- [165]
Husson, S. J.,
Janssen, T.,
Baggerman, G.,
Bogert, B.,
Kahn-Kirby, A. H.,
Ashrafi, K.,
Schoofs, L.,
J. Neurochem.
2007,
102,
246–260.
- [166]
Husson, S. J.,
Schoofs, L.,
FEBS Lett.
2007,
581,
4288–4292.
- [167]
Basir, Y. J.,
Conlon, J. M.,
Peptides
2003,
24,
379–383.
- [168]
McCrudden, C. M.,
Zhou, M.,
Chen, T.,
O'Rourke, M.,
Walker, B.,
Hirst, D.,
Shaw, C.,
Peptides
2007,
28,
1275–1281.
- [169]
Li, J.,
Xu, X.,
Xu, C.,
Zhou, W.,
Zhang, K.,
Yu, H.,
Zhang, Y.,
Zheng, Y.,
Rees, H. H.,
Lai, R.,
Yang, D.,
Wu, J.,
Mol. Cell. Proteomics
2007,
6,
882–894.
- [170]
Skold, K.,
Svensson, M.,
Kaplan, A.,
Bjorkesten, L.,
Astrom, J.,
Andren, P. E.,
Proteomics
2002,
2,
447–454.
- [171]
Minamino, N.,
Tanaka, J.,
Kuwahara, H.,
Kihara, T.,
Satomi, Y.,
Matsubae, M.,
Takao, T.,
J. Chromatogr. B. Analyt. Technol. Biomed. Life Sci.
2003,
792,
33–48.
- [172]
Svensson, M.,
Skold, K.,
Svenningsson, P.,
Andren, P. E.,
J. Proteome Res.
2003,
2,
213–219.
- [173]
Conlon, J. M.,
Kim, J. B.,
Johansson, A.,
Kikuyama, S.,
J. Endocrinol.
2002,
175,
769–777.
- [174]
Ramström, M.,
Hagman, C.,
Tsybin, Y. O.,
Markides, K. E.,
Hakansson, P.,
Salehi, A.,
Lundquist, I.,
Hakanson, R.,
Bergquist, J.,
Eur. J. Biochem.
2003,
270,
3146–3152.
- [175]
Yuan, X.,
Desiderio, D. M.,
J. Mass Spectrom.
2005,
40,
186–181.
- [176]
Norden, A. G.,
Rodriguez-Cutillas, P.,
Unwin, R. J.,
Clin. Chem.
2007,
53,
375–376.
- [177]
Tian, R.,
Ye, M.,
Hu, L.,
Li, X.,
Zou, H.,
J. Sep. Sci.
2007,
30,
2204–2209.
- [178]
Ivanov, V. T.,
Karelin, A. A.,
Yatskin, O. N.,
Biopolymers
2005,
80,
332–346.
- [179]
Hickman, H. D.,
Luis, A. D.,
Buchli, R.,
Few, S. R.,
Sathiamurthy, M.,
Vangundy, R. S.,
Giberson, C. F.,
Hildebrand, W. A.,
J. Immunol.
2004,
172,
2944–2952.
- [180]
Jiménez, C. R.,
Li, K. W.,
Dreisewerd, K.,
Mansvelder, H. D.,
Brussaard, A. B.,
Reinhold, B. B.,
Van der Schors, R. E.,
Karas, M.,
Hillenkamp, F.,
Burbach, J. P.,
Costello, C. E.,
Geraerts, W. P.,
Proc. Natl. Acad. Sci. USA
1994,
94,
9481–9486.
- [181]
Che, F. Y.,
Fricker, L. D.,
J. Mass Spectrom.
2005,
40,
238–249.
- [182]
Che, F. Y.,
Yuan, Q.,
Kalinina, E.,
Fricker, L. D.,
J. Biol. Chem.
2005,
280,
4451–4461.
- [183]
Che, F. Y.,
Biswas, R.,
Fricker, L. D.,
J. Mass Spectrom.
2005,
40,
227–237.
- [184]
Decaillot, F. M.,
Che, F. Y.,
Fricker, L. D.,
Devi, L. A.,
J. Mol. Neurosci.
2006,
28,
277–284.
- [185]
Che, F. Y.,
Vathy, I.,
Fricker, L. D.,
J. Mol. Neurosci.
2006,
28,
265–275.
- [186]
Pan, H.,
Nanno, D.,
Che, F. Y.,
Zhu, X.,
Salton, S. R.,
Steiner, D. F.,
Fricker, L. D.,
Devi, L. A.,
Biochemistry
2005,
44,
4939–4948.
- [187]
Pan, H.,
Che, F. Y.,
Peng, B.,
Steiner, D. F.,
Pintar, J. E.,
Fricker, L. D.,
J. Neurochem.
2006,
98,
1763–1777.
- [188]
Li, L.,
Romanov, E. V.,
Rubakhin, S. S.,
Alexeeva, V.,
Weis, K. R.,
Vilim, F. S.,
Sweedler, J. V.,
Anal. Chem.
2000,
72,
3867–3874.
- [189]
Jurchen, J. C.,
Rubakhin, S. S.,
Sweedler, J. V.,
J. Am. Soc. Mass Spectrom.
2005,
16,
1654–1659.
- [190]
Chaurand, P.,
Caprioli, R. M.,
Electrophoresis
2002,
23,
3125–3135.
- [191]
Altelaar, A. F.,
Klinkert, I.,
Jalink, K.,
de Lange, R. P.,
Adan, R. A.,
Heeren, R. M.,
Piersma, S. R.,
Anal. Chem.
2006,
78,
734–742.
- [192]
DeKeyser, S. S.,
Kutz-Naber, K. K.,
Schimdt, J. J.,
Barrett-Wilt, G. A.,
Li, L.,
J. Proteome Res.
2007,
6,
1782–1791.
- [193]
Taban, I. M.,
Altelaar, A. F.,
van der Burgt, Y. E.,
McDonnell, L. A.,
Heeren, R. M.,
Fuchser, J.,
Baykut, G.,
J. Am. Soc. Mass Spectrom.
2007,
18,
145–151.
- [194]
Rubakhin, S. S.,
Garden, R. W.,
Fuller, R. R.,
Sweedler, J. V.,
Nat. Biotechnol.
2000,
18,
172–175.
- [195]
van Veelen, P. A.,
Jiménez, C. R.,
Li, K. W.,
Wildering, W. C.,
Geraerts, W. P.,
Tjaden, U. R.,
Van der Greef, J.,
Org. Mass Spectrom.
1993,
28,
1542–1546.
- [196]
Jiménez, C. R.,
Spijker, S.,
de Schipper, S.,
Lodder, J. C.,
Janse, C. K.,
Geraerts, W. P.,
van Minnen, J.,
Burlingame, A. L.,
Smit, A. B.,
Li, K.,
J. Neurosci.
2006,
26,
518–529.
- [197]
Sweedler, J. V.,
J. Exp. Biol.
2000,
203,
3565–3573.
- [198]
Predel, R.,
Eckert, M.,
J. Comp. Neurol.
2000,
419,
352–363.
- [199]
Predel, R.,
Wegener, C.,
Russell, W. K.,
Tichy, S. E.,
Russel, D. H.,
Nachman, R. J.,
J. Comp. Neurol.
2004,
474,
379–392.
- [200]
Stoeckli, M.,
Staab, D.,
Staufenbiel, M.,
Wiederhold, K. H.,
Signor, L.,
Anal. Biochem.
2002,
311,
33–39.
- [201]
Levin, Y.,
Schwarz, E.,
Wang, L.,
Leweke, F. M.,
Bahn, S.,
J. Sep. Sci.
2007,
30,
2198–2203.
- [202]
Tammen, H.,
Schorn, K.,
Selle, H.,
Hess, R.,
Neitz, S.,
Comb. Chem. High Throughput Screen.
2005,
8,
783–788.
- [203]
Traub, F.,
Jost, M.,
Hess, R.,
Schom, K.,
Menzel, C.,
Lab. Invest.
2006,
86,
103–114.
- [204]
Budde, P.,
Schulte, I.,
Appel, A.,
Neitz, S.,
Kellman, M.,
Comb. Chem. High Throughput Screen.
2005,
8,
775–781.
- [205]
Villanueva, J.,
Martorella, A. J.,
Lawlor, K.,
Philip, J.,
Fleisher, M.,
Robbins, R. J.,
Tempst, P.,
Mol. Cell. Proteomics
2006,
5,
1840–1852.
- [206]
Petricoin, E. F.,
Belluco, C.,
Araujo, R. P.,
Liotta, L. A.,
Nat. Rev.
2006,
6,
961–967.