Analytical and Bioanalytical Chemistry

, Volume 378, Issue 4, pp 898–909 | Cite as

The impact of chromatography and mass spectrometry on the analysis of protein phosphorylation sites

Review

Abstract

Protein phosphorylation analysis is an enormous challenge. This review summarises the currently used techniques, which are based on radiolabelling and mass spectrometry as well as electrophoretic and chromatographic separation. Many methods exist, but there is still no single procedure applicable to all phosphoproteins. MS is able to deliver information about the location of phosphorylation sites, but phosphospecific properties with respect to ionisation present obstacles. Therefore, multidimensional approaches involving several analytical methods are often necessary to conquer phosphorylation site identification.

Keywords

Protein phosphorylation Mass spectrometry HPLC IMAC Radiolabelling 

Abbreviations

2D

Two-dimensional

CE

Capillary electrophoresis

CID

Collision-induced dissociation

ECD

Electron capture dissociation

ESI

Electrospray ionisation

FT-ICR

Fourier transform ion cyclotron resonance

HPLC

High performance liquid chromatography

ICAT

Isotope coded affinity tags

ICP

Inductively-coupled plasma

IDA

Immino-diacetic acid

IMAC

Immobilised metal affinity chromatography

IRMPD

Infrared multiphoton dissociation

IT

Ion trap

MALDI

Matrix-assisted laser desorption/ionisation

MRP14

Myeloid-related protein 14

MS

Mass spectrometry

NTA

Nitrilo-triacetic acid

PAGE

Polyacrylamide gel electrophoresis

PDI

Protein disulfide isomerase

pS

Phosphoserine residue

PSD

Post-source decay

pT

Phosphothreonine residue

PVDF

Polyvinylidene fluoride

pY

Phosphotyrosine residue

Q-TOF

Quadrupole-time-of-flight

RP

Reversed phase

SIM

Single-ion monitoring

SDS

Sodium dodecyl sulfate

SORI

Sustained off-resonance irradiation

TLC

Thin-layer chromatography

TOF

Time-of-flight

References

  1. 1.
    Fenn JB, Mann M, Meng CK, Wong SF, Whitehouse CM (1989) Science 246:64–71PubMedGoogle Scholar
  2. 2.
    Karas M, Hillenkamp F (1988) Anal Chem 60:2299–2301PubMedGoogle Scholar
  3. 3.
    Krebs EG (1983) Philos Tr R Soc B 302:3–11Google Scholar
  4. 4.
    Hunter T (1995) Cell 80:225–236PubMedGoogle Scholar
  5. 5.
    Blume-Jensen P, Hunter T (2001) Nature 411:355–365PubMedGoogle Scholar
  6. 6.
    Yaffe MB, Elia AEH (2001) Curr Opin Cell Biol 13:131–138CrossRefPubMedGoogle Scholar
  7. 7.
    Hunter T (1998) Philos Tr R Soc B 353:583–605CrossRefGoogle Scholar
  8. 8.
    Matthews HR (1995) Pharmacol Therapeut 67:323–350CrossRefGoogle Scholar
  9. 9.
    Besant PG, Tan E, Attwood PV (2003) Int J Biochem Cell Biol 35:297–309CrossRefPubMedGoogle Scholar
  10. 10.
    Cho H, Wang W, Kim R, Yokota H, Damo S, Kim S-H, Wemmer D, Kustu S, Yan D (2001) P Natl Acad Sci USA 98:8525–8530CrossRefGoogle Scholar
  11. 11.
    Lewis RJ, Brannigan JA, Muchova K, Barak I, Wilkinson AJ (1999) J Biol Chem 294:9–15CrossRefGoogle Scholar
  12. 12.
    Iuchi S (1993) J Biol Chem 268:23972–23980PubMedGoogle Scholar
  13. 13.
    Bourret R, Hess J, Simon M (1990) P Natl Acad Sci USA 87:41–45Google Scholar
  14. 14.
    Jacobs MA, Connell L, Cattolico RA (1999) Plant Mol Biol 41:645–655CrossRefPubMedGoogle Scholar
  15. 15.
    Wagner PD, Vu N-D (2000) Biochem J 346:623–630CrossRefPubMedGoogle Scholar
  16. 16.
    Collet J-F, Stroobant V, Pirard M, Delpierre G, Van Schaftingen E (1998) J Biol Chem 273:14107–14112CrossRefPubMedGoogle Scholar
  17. 17.
    Klumpp S, Krieglstein J (2002) Eur J Biochem 269:1067–1071CrossRefPubMedGoogle Scholar
  18. 18.
    Yeargin J, Haas M (1995) Curr Biol 5:423–431PubMedGoogle Scholar
  19. 19.
    Hu VW, Heikka DS, Dieffenbach PB, Ha L (2001) FASEB J 15:1562–1568CrossRefPubMedGoogle Scholar
  20. 20.
    Ruotolo BT, Verbeck GF, Thomson LM, Woods AS, Gillig KJ, Russell DH (2002) J Proteome Res 1:303–306CrossRefPubMedGoogle Scholar
  21. 21.
    Gibb GM, Pearce J, Betts JC, Lovestone S, Hoffmann MM, Maerz W, Blackstock WP, Anderton BH (2000) FEBS Lett 485:99–103CrossRefPubMedGoogle Scholar
  22. 22.
    Ogueta S, Rogado R, Marina A, Moreno F, Redondo JM, Vazquez J (2000) J Mass Spectrom 35:556–565Google Scholar
  23. 23.
    Boyle WJ, van der Geer P, Hunter T (1991) Method Enzymol 201:110–149Google Scholar
  24. 24.
    Winz R, Hess D, Aebersold R, Brownsey R (1994) J Biol Chem 269:14438–14445PubMedGoogle Scholar
  25. 25.
    De Corte V, Demol H, Goethals M, Van Damme J, Gettemans J, Vandekerckhove J (1999) Protein Sci 8:234–241PubMedGoogle Scholar
  26. 26.
    Wettenhall RE, Aebersold RH, Hood LE (1991) Methods Enzymol 201:186–199PubMedGoogle Scholar
  27. 27.
    Goodlett DR, Aebersold R, Watts JD (2000) Rapid Commun Mass Sp 14:344–348CrossRefGoogle Scholar
  28. 28.
    Liao PC, Leykam J, Andrews PC, Gage DA, Allison J (1994) Anal Biochem 219:9–20CrossRefPubMedGoogle Scholar
  29. 29.
    Yamagata A, Kristensen DB, Takeda Y, Miyamoto Y, Okada K, Inamatsu M, Yoshizato K (2002) Proteomics 2:1267–1276CrossRefPubMedGoogle Scholar
  30. 30.
    König S, Grote J, Zeller M (2002) In: Cullen P (eds) Analyzing gene expression, 1st edn. Wiley-VCH, Weinheim, Germany, p 638–668Google Scholar
  31. 31.
    Shevchenko A, Wilm M, Vorm O, Mann M (1996) Anal Chem 68:850–858CrossRefPubMedGoogle Scholar
  32. 32.
    Gronborg M, Kristiansen TZ, Stensballe A, Andersen JS, Ohara O, Mann M, Jensen ON, Pandey A (2002) Mol Cell Proteomics 1:517–527CrossRefPubMedGoogle Scholar
  33. 33.
    Soskic V, Gorlach M, Poznanovic S, Boehmer FD, Godovac-Zimmermann J (1999) Biochemistry-US 38:1757–1764Google Scholar
  34. 34.
    Godovac-Zimmermann J, Soskic V, Poznanovic S, Brianza F (1999) Electrophoresis 20:952–961CrossRefPubMedGoogle Scholar
  35. 35.
    Spengler B, Kirsch D, Kaufmann R, Jaeger E (1992) Rapid Commun Mass Sp 6:105–108Google Scholar
  36. 36.
    Marcus K, Immler D, Sternberger J, Meyer HE (2000) Electrophoresis 21:2622–2636CrossRefPubMedGoogle Scholar
  37. 37.
    Talbo GH, Suckau D, Malkoski M, Reynolds EC (2001) Peptides 22:1093–1098CrossRefPubMedGoogle Scholar
  38. 38.
    Metzger S, Hoffmann R (2000) J Mass Spectrom 35:1165–1177CrossRefPubMedGoogle Scholar
  39. 39.
    Hoffmann R, Metzger S, Spengler B, Otvos L (1999) J Mass Spectrom 34:1195–1204CrossRefPubMedGoogle Scholar
  40. 40.
    Medzihradszky KF, Campbell JM, Baldwin MA, Falick AM, Juhasz P, Vestal ML, Burlingame AL (2000) Anal Chem 72:552–558CrossRefPubMedGoogle Scholar
  41. 41.
    Thompson AJ, Hart SR, Franz C, Barnouin K, Ridley A, Cramer R (2003) Anal Chem 75:3232–3243CrossRefPubMedGoogle Scholar
  42. 42.
    Covey T, Shushan B, Bonner R, Schröder W, Hucho F (1991) In: Jörnvall H, Höög JO, Gustavsson AM (eds) Methods in protein sequence analysis. Birkhauser, Basel, p 249–256Google Scholar
  43. 43.
    Hunter AP, Games DE (1994) Rapid Commun Mass Sp 8:559–570PubMedGoogle Scholar
  44. 44.
    Bateman RH, Carruthers R, Hoyes JB, Jones C, Langridge JI, Millar A, Vissers JP (2002) J Am Soc Mass Spectr 13:792–803CrossRefGoogle Scholar
  45. 45.
    Xiang R, Horvath C, Wilkins JA (2003) Anal Chem 75:1819–1827CrossRefPubMedGoogle Scholar
  46. 46.
    DeGnore JP, Qin J (1998) J Am Soc Mass Spectr 9:1175–1188CrossRefGoogle Scholar
  47. 47.
    Schlosser A, Pipkorn R, Bossemeyer D, Lehmann WD (2001) Anal Chem 73:170–176CrossRefPubMedGoogle Scholar
  48. 48.
    Moyer SC, VonSeggern CE, Cotter RJ (2003) J Am Soc Mass Spectr 14:581–592CrossRefGoogle Scholar
  49. 49.
    Carr SA, Huddleston MJ, Annan RS (1996) Anal Biochem 239:180–192CrossRefPubMedGoogle Scholar
  50. 50.
    Tholey A, Reed J, Lehmann WD (1999) J Mass Spectrom 34:117–123CrossRefPubMedGoogle Scholar
  51. 51.
    Annan RS, Carr SA (1996) Anal Chem 68:3413–3421CrossRefPubMedGoogle Scholar
  52. 52.
    Qin J, Chait, B T (1997) Anal Chem 69:4002–4009CrossRefPubMedGoogle Scholar
  53. 53.
    Bennett KL, Stensballe A, Podtelejnikov AV, Moniatte M, Jensen ON (2002) J Mass Spectrom 37:179–190CrossRefPubMedGoogle Scholar
  54. 54.
    Baldwin MA, Medzihradszky KF, Lock CM, Fisher B, Settineri TA, Burlingame AL (2001) Anal Chem 73:1707–1720CrossRefPubMedGoogle Scholar
  55. 55.
    Hager JW, Yves Le Blanc JC (2003) Rapid Commun Mass Sp 17:1056–1064PubMedGoogle Scholar
  56. 56.
    Hoffmann R, Wehofsky M, Metzger S (2001) Anal Chem 73:4845–4851CrossRefPubMedGoogle Scholar
  57. 57.
    Flora JW, Muddiman DC (2001) Anal Chem 73:3305–3311PubMedGoogle Scholar
  58. 58.
    Chalmers MJ, Quinn JP, Blakney GT, Emmett MR, Mischak H, Gaskell SJ, Marshall AG (2003) J Proteome Res 2:373–382CrossRefPubMedGoogle Scholar
  59. 59.
    Wilm M, Neubauer G, Mann M (1996) Anal Chem 68:527–533CrossRefPubMedGoogle Scholar
  60. 60.
    Neubauer G, Mann M (1999) Anal Chem 71:235–242CrossRefPubMedGoogle Scholar
  61. 61.
    Köcher T, Allmaier G, Wilm M (2003) J Mass Spectrom 38:131–137CrossRefPubMedGoogle Scholar
  62. 62.
    Verma R, Annan RS, Huddleston MJ, Carr SA, Reynard G, Deshaies RJ (1997) Science 278:455–460CrossRefPubMedGoogle Scholar
  63. 63.
    Annan RS, Huddleston MJ, Verma R, Deshaies RJ, Carr SA (2001) Anal Chem 73:393–404CrossRefPubMedGoogle Scholar
  64. 64.
    Lennon JJ, Walsh KA (1999) Protein Sci 8:2487–2493PubMedGoogle Scholar
  65. 65.
    Kinumi T, Niwa H, Matsumoto H (2000) Anal Biochem 277:177–186CrossRefPubMedGoogle Scholar
  66. 66.
    Steen H, Kuster B, Fernandez M, Pandey A, Mann M (2001) Anal Chem 73:1440–1448CrossRefPubMedGoogle Scholar
  67. 67.
    Steen H, Fernandez M, Ghaffari S, Pandey A, Mann M (2003) Mol Cell Proteomics 2:138–145CrossRefPubMedGoogle Scholar
  68. 68.
    Salek M, Alonso A, Pipkorn R, Lehmann WD (2003) Anal Chem 75:2724–2729CrossRefPubMedGoogle Scholar
  69. 69.
    Steen H, Pandey A, Andersen JS, Mann M (2002) Sci STKE 154:PL16Google Scholar
  70. 70.
    Steen H, Kuster B, Fernandez M, Pandey A, Mann M (2002) J Biol Chem 277:1031–1039CrossRefPubMedGoogle Scholar
  71. 71.
    Hoffmann R, Wachs WO, Berger RG, Kalbitzer HR, Waidelich D, Bayer E, Wagner-Redeker W, Zeppezauer M (1995) Int J Pept Prot Res 45:26–34Google Scholar
  72. 72.
    Steen H, Kuster B, Mann M (2001) J Mass Spectrom 36:782–790CrossRefPubMedGoogle Scholar
  73. 73.
    Rappsilber J, Steen H, Mann M (2001) J Mass Spectrom 36:832–833CrossRefPubMedGoogle Scholar
  74. 74.
    Wolfender J-L, Chu F, Ball H, Wolfender F, Fainzilber M, Baldwin MA, Burlingame AL (1999) J Mass Spectrom 34:447–454CrossRefPubMedGoogle Scholar
  75. 75.
    Steen H, Mann M (2002) J Am Soc Mass Spectr 13:996–1003CrossRefGoogle Scholar
  76. 76.
    Carr SA, Huddleston MJ, Bean MF (1993) Protein Sci 2:183–196PubMedGoogle Scholar
  77. 77.
    Huddleston MJ, Annan RS, Bean MF, Carr SA (1993) J Am Soc Mass Spectr 4:710–717CrossRefGoogle Scholar
  78. 78.
    Till J, Annan R, Carr S, Miller W (1994) J Biol Chem 269:7423–7428PubMedGoogle Scholar
  79. 79.
    Jedrzejewski PT, Lehmann WD (1997) Anal Chem 69:294–301CrossRefPubMedGoogle Scholar
  80. 80.
    Ding J, Burkhart W, Kassel DB (1994) Rapid Commun Mass Sp 8:94–98Google Scholar
  81. 81.
    Zolodz MD, Wood KV (2003) J Mass Spectrom 38:257–264CrossRefPubMedGoogle Scholar
  82. 82.
    Zhang X, Herring CJ, Romano PR, Szczepanowska J, Brzeska H, Hinnebusch AG, Qin J (1998) Anal Chem 70:2050–2059CrossRefPubMedGoogle Scholar
  83. 83.
    Wind M, Edler M, Jakubowski N, Linscheid M, Wesch H, Lehmann WD (2001) Anal Chem 73:29–35Google Scholar
  84. 84.
    Busman M, Schey KL, Oatis JEJ, Knapp DR (1996) J Am Soc Mass Spectr 7:243–249CrossRefGoogle Scholar
  85. 85.
    Janek K, Wenschuh H, Bienert M, Krause E (2001) Rapid Commun Mass Sp 15:1593–1599CrossRefGoogle Scholar
  86. 86.
    Ma Y, Lu Y, Zeng H, Ron D, Mo W, Neubert TA (2001) Rapid Commun Mass Sp 15:1693–1700CrossRefGoogle Scholar
  87. 87.
    Chalmers MJ, Quinn JP, Blakney GT, Emmett MR, Mischak H, Gaskell SJ, Marshall AG (2003) J Proteome Res (in press)Google Scholar
  88. 88.
    Zubarev RA (2003) Mass Spectrom Rev 22:57–77CrossRefPubMedGoogle Scholar
  89. 89.
    Budnik BA, Haselmann KF, Zubarev RA (2001) Chem Phys Lett 342:299–302CrossRefGoogle Scholar
  90. 90.
    Haselmann KF, Budnik BA, Kjeldsen F, Nielsen ML, Olsen JV, Zubarev RA (2002) Eur J Mass Spectrom 8:117–121CrossRefGoogle Scholar
  91. 91.
    Asara JM, Allison J (1999) J Am Soc Mass Spectr 10:35–44CrossRefGoogle Scholar
  92. 92.
    Lee CH, McComb ME, Bromirski M, Jilkine A, Ens W, Standing KG, Perreault H (2001) Rapid Commun Mass Sp 15:181–202Google Scholar
  93. 93.
    Wilm M, Mann M (1996) Anal Chem 68:1–8PubMedGoogle Scholar
  94. 94.
    Wilm MS, Mann M (1994) Int J Mass Spectrom 136:167–180Google Scholar
  95. 95.
    Juraschek R, Dulcks T, Karas M (1999) J Am Soc Mass Spectr 10:300–308CrossRefGoogle Scholar
  96. 96.
    Amster IJ (1996) J Mass Spectrom 31:1325–1337CrossRefGoogle Scholar
  97. 97.
    Marshall AG, Hendrickson CL, Jackson GS (1998) Mass Spectrom Rev 17:1–35CrossRefPubMedGoogle Scholar
  98. 98.
    Marshall AG (2000) Int J Mass Spectrom 200:331–356CrossRefGoogle Scholar
  99. 99.
    Witt M, Fuchser J, Baykut G (2003) J Am Soc Mass Spectr 14:553–561CrossRefGoogle Scholar
  100. 100.
    Martin SE, Shabanowitz J, Hunt DF, Marto JA (2000) Anal Chem 72:4266–4274CrossRefPubMedGoogle Scholar
  101. 101.
    Zubarev RA, Kelleher NL, McLafferty FW (1998) J Am Chem Soc 120:3265–3266Google Scholar
  102. 102.
    Turecek F (2003) J Am Chem Soc 125:5954–5963CrossRefPubMedGoogle Scholar
  103. 103.
    Zubarev RA, Haselmann KF, Budnik BA, Kjeldsen F, Jensen F (2002) Eur J Mass Spectrom 8:337–349CrossRefGoogle Scholar
  104. 104.
    Haselmann KF, Budnik BA, Olsen JV, Nielsen ML, Reis CA, Clausen H, Johnsen AH, Zubarev RA (2001) Anal Chem 73:2998–3005CrossRefPubMedGoogle Scholar
  105. 105.
    Tsybin YO, Hakansson P, Budnik BA, Haselmann KF, Kjeldsen F, Gorshkov M, Zubarev RA (2001) Rapid Commun Mass Sp 15:1849–1854CrossRefGoogle Scholar
  106. 106.
    Palmblad M, Tsybin YO, Ramstrom M, Bergquist J, Hakansson P (2002) Rapid Commun Mass Sp 16:988–992CrossRefGoogle Scholar
  107. 107.
    Stensballe A, Jensen ON, Olsen JV, Haselmann KF, Zubarev RA (2000) Rapid Commun Mass Sp 14:1793–1800CrossRefPubMedGoogle Scholar
  108. 108.
    Horn DM, Ge Y, McLafferty FW (2000) Anal Chem 72:4778–4784CrossRefPubMedGoogle Scholar
  109. 109.
    Zubarev RA, Horn DM, Fridriksson EK, Kelleher NL, Kruger NA, Lewis MA, Carpenter BK, McLafferty FW (2000) Anal Chem 72:563–573CrossRefPubMedGoogle Scholar
  110. 110.
    Shi SD, Hemling ME, Carr SA, Horn DM, Lindh I, McLafferty FW (2001) Anal Chem 73:19–22CrossRefPubMedGoogle Scholar
  111. 111.
    Hakansson K, Chalmers MJ, Quinn JP, McFarland MA, Hendrickson CL, Marshall AG (2003) Anal Chem 75:3256–3262CrossRefPubMedGoogle Scholar
  112. 112.
    Taylor GK, Kim Y-B, Forbes AJ, Meng F, McCarthy R, Kelleher NL (2003) Anal Chem 75:4081–4086CrossRefGoogle Scholar
  113. 113.
    Wind M, Kelm O, Nigg EA, Lehmann WD (2002) Proteomics 2:1516–1523CrossRefPubMedGoogle Scholar
  114. 114.
    Wind M, Gosenca D, Kubler D, Lehmann WD (2003) Anal Biochem 317:26–33CrossRefPubMedGoogle Scholar
  115. 115.
    Tsugita A, Miyazaki K, Nabetani T, Nozawa T, Kamo M, Kawakami T (2001) Proteomics 1:1082–1091CrossRefPubMedGoogle Scholar
  116. 116.
    Ekstrom S, Nilsson J, Helldin G, Laurell T, Marko-Varga G (2001) Electrophoresis 22:3984–3392CrossRefPubMedGoogle Scholar
  117. 117.
    Liu Q, Hintz M, Li J, Linder M, Geyer R, Hobom G (2000) Arch Virol 145:1211–1223CrossRefPubMedGoogle Scholar
  118. 118.
    Claverol S, Burlet-Schiltz O, Gairin JE, Monsarrat B (2003) Mol Cell Proteomics 2:483–493PubMedGoogle Scholar
  119. 119.
    Edgeworth J, Freemont P, Hogg N (1989) Nature 342:189–192CrossRefPubMedGoogle Scholar
  120. 120.
    Jensen ON, Larsen MR, Roepstorff P (1998) Proteins Suppl 2:74–89Google Scholar
  121. 121.
    Stensballe A, Andersen S, Jensen ON (2001) Proteomics 1:207–222CrossRefPubMedGoogle Scholar
  122. 122.
    Larsen MR, Sorensen GL, Fey SJ, Larsen PM, Roepstorff P (2001) Proteomics 1:223–2238CrossRefPubMedGoogle Scholar
  123. 123.
    Dahma H, Gourlet P, Vandermeers A, Vandermeers-Piret M-C, Robberecht P (2001) Peptides 22:1491–1499CrossRefPubMedGoogle Scholar
  124. 124.
    Bauer SHJ, Zhang XY, Van Dongen W, Claeys M, Przybylski M (1999) Anal Biochem 274:69–80CrossRefPubMedGoogle Scholar
  125. 125.
    Kussmann M, Hauser K, Kissmehl R, Breed J, Plattner H, Roepstorff P (1999) Biochemistry-US 38:7780–7790Google Scholar
  126. 126.
    Kuyama H, Toda C, Watanabe M, Tanaka K, Nishimura O (2003) Rapid Commun Mass Sp 17:1493–1496CrossRefGoogle Scholar
  127. 127.
    Amankwa LN, Harder K, Jirik F, Aebersold R (1995) Protein Sci 4:113–125PubMedGoogle Scholar
  128. 128.
    Ladner RD, Carr SA, Huddleston MJ, McNulty DE, Caradonna SJ (1996) J Biol Chem 271:7752–7757CrossRefPubMedGoogle Scholar
  129. 129.
    Michel HP, Bennett J (1987) FEBS Lett 212:103–108CrossRefGoogle Scholar
  130. 130.
    Anguenot R, Yelle S, Nguyen-Quoc B (1999) Arch Biochem Biophys 365:163–169CrossRefPubMedGoogle Scholar
  131. 131.
    Andersson L, Porath J (1986) Anal Biochem 154:250–254PubMedGoogle Scholar
  132. 132.
    Ueda EK, Gout PW, Morganti L (2003) J Chromatogr A 988:1–23CrossRefPubMedGoogle Scholar
  133. 133.
    Posewitz MC, P T (1999) Anal Chem 71:2883–2892CrossRefPubMedGoogle Scholar
  134. 134.
    Neville DC, Rozanas CR, Price EM, Gruis DB, Verkman AS, Townsend RR (1997) Protein Sci 6:2436–2445PubMedGoogle Scholar
  135. 135.
    Ficarro S, Chertihin O, Westbrook VA, White F, Jayes F, Kalab P, Marto JA, Shabanowitz J, Herr JC, Hunt DF, Visconti PE (2003) J Biol Chem 278:11579–11589CrossRefPubMedGoogle Scholar
  136. 136.
    Porath J (1992) Protein Expres Purif 3:263–281Google Scholar
  137. 137.
    Yip TT, Hutchens TW (1994) Mol Biotechnol 1:151–164PubMedGoogle Scholar
  138. 138.
    Gaberc-Porekar V, Menart V (2001) J Biochem Bioph Meth 49:335–360CrossRefGoogle Scholar
  139. 139.
    Muszynska G, Andersson L, Porath J (1986) Biochemistry 25:6850–6853PubMedGoogle Scholar
  140. 140.
    Kucerova Z, Majercakova P (2001) J Biochem Biophys Methods 49:523–531CrossRefPubMedGoogle Scholar
  141. 141.
    Belew M, Yip TT, Andersson L, Ehrnstrom R (1987) Anal Biochem 164:457–465PubMedGoogle Scholar
  142. 142.
    Belew M, Yip TT, Andersson L, Porath J (1987) J Chromatogr 403:197–206CrossRefPubMedGoogle Scholar
  143. 143.
    Cleverley KE, Betts JC, Blackstock WP, Gallo J-M, Anderton BH (1998) Biochemistry-US 37:3917–3930Google Scholar
  144. 144.
    Li S, Dass C (1999) Anal Biochem 270:9–14CrossRefPubMedGoogle Scholar
  145. 145.
    Schneider U, Mini T, Jenoe P, Fisher PA, Stuurman N (1999) Biochemistry-US 38:4620–4632Google Scholar
  146. 146.
    Merrick BA, Zhou W, Martin KJ, Jeyarajah S, Parker CE, Selkirk JK, Tomer KB, Borchers CH (2001) Biochemistry-US 40:4053–4066Google Scholar
  147. 147.
    Li S, Dass C (1999) Eur J Mass Spectrom 5:279–284Google Scholar
  148. 148.
    Betts JC, Blackstock WP, Ward MA, Anderton BH (1997) J Biol Chem 272:12922–12927CrossRefPubMedGoogle Scholar
  149. 149.
    Zhou W, Merrick BA, Khaledi MG, Tomer KB (2000) J Am Soc Mass Spectr 11:273–282CrossRefPubMedGoogle Scholar
  150. 150.
    Hart SR, Waterfield MD, Burlingame AL, Cramer R (2002) J Am Soc Mass Spectr 13:1042–1051CrossRefGoogle Scholar
  151. 151.
    Raska CS, Parker CE, Dominski Z, Marzluff WF, Glish GL, Pope RM, Borchers CH (2002) Anal Chem 74:3429–3422CrossRefPubMedGoogle Scholar
  152. 152.
    Scanff P, Yvon M, Pelissier JP (1991) J Chromatogr A 539:425–432CrossRefGoogle Scholar
  153. 153.
    Michel H, Hunt D, Shabanowitz J, Bennett J (1988) J Biol Chem 263:1123–1130PubMedGoogle Scholar
  154. 154.
    Ficarro SB, McCleland ML, Stukenberg PT, Burke DJ, Ross MM, Shabanowitz J, Hunt DF, White FM (2002) Nat Biotechnol 20:301–305CrossRefPubMedGoogle Scholar
  155. 155.
    Salomon AR, Ficarro SB, Brill LM, Brinker A, Phung QT, Ericson C, Sauer K, Brock A, Horn DM, Schultz PG, Peters EC (2003) P Natl Acad Sci USA 100:443–448CrossRefGoogle Scholar
  156. 156.
    Nuwaysir LM, Stults JT (1993) J Am Soc Mass Spectr 4:662–669CrossRefGoogle Scholar
  157. 157.
    Watts J, Affolter M, Krebs D, Wange R, Samelson L, Aebersold R (1994) J Biol Chem 269:29520–29529PubMedGoogle Scholar
  158. 158.
    Figeys D, Gygi SP, Zhang Y, Watts J, Gu M, Aebersold R (1998) Electrophoresis 19:1811–1818PubMedGoogle Scholar
  159. 159.
    Cao P, Stults JT (1999) J Chromatogr A 853:225–235PubMedGoogle Scholar
  160. 160.
    Nuhse TS, Stensballe A, Jensen, Ole N, Peck SC (2003) Mol Cell Proteomics (in press)Google Scholar
  161. 161.
    Patterson SD, Aebersold R, Goodlett DR (2001) In: Pennington SR, Dunn MJ (eds), Proteomics – from protein sequence to function. Bios Scientific, Oxford, p 87–130Google Scholar
  162. 162.
    Davis MT, Stahl DC, Hefta SA, Lee TD (1995) Anal Chem 67:4549–4556PubMedGoogle Scholar
  163. 163.
    Davis MT, Stahl DC, Lee TD (1995) J Am Soc Mass Spectr 6:571–577CrossRefGoogle Scholar
  164. 164.
    Vissers JPC, Blackburn RK, Moseley MA (2002) J Am Soc Mass Sp 13:760–771CrossRefPubMedGoogle Scholar
  165. 165.
    Keil O, LeRiche T, Deppe H, Volmer DA (2002) Rapid Commun Mass Sp 16:814–820CrossRefPubMedGoogle Scholar
  166. 166.
    Erdjument-Bromage H, Lui M, Lacomis L, Grewal A, Annan RS, McNulty DE, Carr SA, Tempst P (1998) J Chromatogr A 826:167–181CrossRefPubMedGoogle Scholar
  167. 167.
    Matsumoto H, Kahn ES, Komori N (1998) Anal Biochem 251:116–119CrossRefGoogle Scholar
  168. 168.
    Chin ET, Papac DI (1999) Anal Biochem 273:179–185CrossRefPubMedGoogle Scholar
  169. 169.
    Vacratsis PO, Phinney BS, Gage DA, Gallo KA (2002) Biochemistry-US 41:5613–5624Google Scholar
  170. 170.
    Larsen MR, Cordwell SJ, Roepstorff P (2002) Proteomics 2:1277–1287CrossRefPubMedGoogle Scholar
  171. 171.
    Resing KA, Johnson RS, Walsh KA (1995) Biochemistry-US 34:9477–9487Google Scholar
  172. 172.
    Bonenfant D, Mini T, Jenoe P (2002) In: Walker JM (ed) The protein protocols handbook, 2nd Edn. Humana, Totowa NJ, p 609–622Google Scholar
  173. 173.
    Weckwerth W, Willmitzer L, Fiehn O (2000) Rapid Commun Mass Sp 14:1677–1681PubMedGoogle Scholar
  174. 174.
    Sadagopan N, Malone M, Watson JT (1999) J Mass Spectrom 34:1279–1282CrossRefPubMedGoogle Scholar
  175. 175.
    Meyer HE, Hoffmann-Posorske E, Korte H, Heilmeyer J, Ludwig MG (1986) FEBS Lett 204:61–66CrossRefPubMedGoogle Scholar
  176. 176.
    Meyer HE, Hoffmann-Posorske E, Heilmeyer J, Ludwig MG (1991) In: Hunter T, Sefton BM (eds) Methods in enzymology, protein phosphorylation, Volume 201. Elsevier, Amsterdam, p 169–185Google Scholar
  177. 177.
    Li W, Boykins RA, Backlund PS, Wang G, Chen H-C (2002) Anal Chem 74:5701–5710CrossRefPubMedGoogle Scholar
  178. 178.
    Adamczyk M, Gebler JC, Wu J (2001) Rapid Commun Mass Sp 15:1481–1148CrossRefPubMedGoogle Scholar
  179. 179.
    Adamczyk M, Gebler JC, Wu J (2002) Rapid Commun Mass Sp 16:999–1001CrossRefGoogle Scholar
  180. 180.
    Molloy MP, Andrews PC (2001) Anal Chem 73:5387–5394CrossRefPubMedGoogle Scholar
  181. 181.
    Zhu H, Hunter TC, Pan S, Yau PM, Bradbury EM, Chen X (2002) Anal Chem 74:1687-1694CrossRefPubMedGoogle Scholar
  182. 182.
    Conrads TP, Issaq HJ, Veenstra TD (2002) Biochem Bioph Res Co 290:885–890CrossRefGoogle Scholar
  183. 183.
    Lill J (2003) Mass Spectrom Rev 22:182–194CrossRefPubMedGoogle Scholar
  184. 184.
    Gygi SP, Rist B, Gerber SA, Turecek F, Gelb MH, Aebersold R (1999) Nat Biotechnol 17:994–999Google Scholar
  185. 185.
    Oda Y, Huang K, Cross FR, Cowburn D, Chait BT (1999) P Natl Acad Sci USA 96:6591–6596CrossRefGoogle Scholar
  186. 186.
    Bonenfant D, Schmelzle T, Jacinto E, Crespo JL, Mini T, Hall MN, Jenoe P (2003) P Natl Acad Sci USA 100:880–885CrossRefGoogle Scholar
  187. 187.
    Yao X, Freas A, Ramirez J, Demirev PA, Fenselau C (2001) Anal Chem 73:2836–2842PubMedGoogle Scholar
  188. 188.
    Zeller M, Essmann F, Janicke RU, Schulze-Osthoff K, König S (2003) J Exp Ther Oncol 3:59–61CrossRefPubMedGoogle Scholar
  189. 189.
    Matsumoto H, Kahn ES, Komori N (1998) Anal Biochem 260:188–194CrossRefPubMedGoogle Scholar
  190. 190.
    Ruse CI, Willard B, Jin JP, Haas T, Kinter M, Bond M (2002) Anal Chem 74:1658–1664CrossRefPubMedGoogle Scholar
  191. 191.
    Glinski M, Romeis T, Witte C-P, Wienkoop S, Weckwerth W (2003) Rapid Commun Mass Sp 17:1579–1584CrossRefGoogle Scholar
  192. 192.
    Oda Y, Nagasu T, Chait BT (2001) Nat Biotechnol 19:379–382CrossRefPubMedGoogle Scholar
  193. 193.
    Goshe MB, Conrads TP, Panisko EA, Angell NH, Veenstra TD, Smith RD (2001) Anal Chem 73:2578–2586CrossRefPubMedGoogle Scholar
  194. 194.
    Goshe MB, Veenstra TD, Panisko EA, Conrads TP, Angell NH, Smith RD (2002) Anal Chem 74:607–616CrossRefPubMedGoogle Scholar
  195. 195.
    Fadden P, Haystead TA (1995) Anal Biochem 225:81–88CrossRefPubMedGoogle Scholar
  196. 196.
    Steinberg TH, Agnew BJ, Gee KR, Leung W-Y, Goodman T, Schulenberg B, Hendrickson J, Beechem JM, Haugland RP, Patton WF (2003) Proteomics 3:1128–1144CrossRefPubMedGoogle Scholar
  197. 197.
    Zhang X, Jin QK, Carr SA, Annan RS (2002) Rapid Commun Mass Sp 16:2325–2332CrossRefGoogle Scholar
  198. 198.
    Wind M, Feldmann I, Jakubowski N, Lehmann WD (2003) Electrophoresis 24:1276–1280CrossRefPubMedGoogle Scholar
  199. 199.
    Wind M, Wesch H, Lehmann WD (2001) Anal Chem 73:3006–3010Google Scholar
  200. 200.
    Zappacosta F, Huddleston MJ, Karcher RL, Gelfand VI, Carr SA, Annan RS (2002) Anal Chem 74:3221–3231CrossRefPubMedGoogle Scholar
  201. 201.
    Lund ET, McKenna R, Evans DB, Sharma SK, Mathews WR (2001) J Neurochem 76:1221–1232CrossRefPubMedGoogle Scholar
  202. 202.
    Loughrey Chen S, Huddleston MJ, Shou W, Deshaies RJ, Annan RS, Carr SA (2002) Mol Cell Proteomics 1:186–196CrossRefPubMedGoogle Scholar
  203. 203.
    Resing KA, Ahn NG (1997) Method Enzymol 283:29–44Google Scholar
  204. 204.
    Yan JX, Packer NH, Gooley AA, Williams KL (1998) J Chromatogr A 808:23–41CrossRefPubMedGoogle Scholar
  205. 205.
    Matsumoto H, Kahn ES, Komori N (1999) Novartis Fdn Symp 224:244–248Google Scholar
  206. 206.
    Zolnierowicz S, Bollen M (2000) EMBO J 19:483–488CrossRefPubMedGoogle Scholar
  207. 207.
    Quadroni M, James P (2000) In: Jollès P, Jörnvall H (eds) Proteomics in functional genomics, Volume 88. Birkhauser, Basel, p 199–213Google Scholar
  208. 208.
    Larsen MR, Roepstorff P (2000) Fresen J Anal Chem 366:677–690CrossRefGoogle Scholar
  209. 209.
    Pandey A, Andersen JS, Mann M (2000) Sci STKE 37:PL1Google Scholar
  210. 210.
    McLachlin DT, Chait BT (2001) Curr Opin Chem Biol 5:591–602CrossRefPubMedGoogle Scholar
  211. 211.
    Sickmann A, Meyer HE (2001) Proteomics 1:200–206CrossRefPubMedGoogle Scholar
  212. 212.
    Mann M, Ong SE, Gronborg M, Steen H, Jensen ON, Pandey A (2002) Trends Biotechnol 20:261–268CrossRefPubMedGoogle Scholar
  213. 213.
    Mann M, Jensen ON (2003) Nat Biotechnol 21:255–261CrossRefPubMedGoogle Scholar
  214. 214.
    Arnott D, Gawinowicz MA, Grant RA, Neubert TA, Packman LC, Speicher KD, Stone K, Turck CW (2003) J Biomol Tech 14:205–215PubMedGoogle Scholar
  215. 215.
    Biemann K (1990) In: McCloskey JA (ed) Methods in enzymology, Vol 193. Academic, San Diego p 886–887Google Scholar
  216. 216.
    Zeller M, König S (2003) In: Proc 51st ASMS Conf on Mass Spectrometry and Allied Topics, 8–12 June 2003, Montréal, CanadaGoogle Scholar
  217. 217.
    Zeller M, Barrow M, Kornel N, König S, Derrick PJ (2003) In: Proc 16th Int Mass Spectrometry Conf, 31 Aug–5 Sept 2003, Edinburgh, ScotlandGoogle Scholar
  218. 218.
    Zeller M, König S (2002) In: Proc 2nd NanoBioTec Congress, 30 Sept–2 Oct 2002, Münster, GermanyGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  1. 1.Integrated Functional Genomics, Interdisciplinary Center for Clinical Research Medical FacultyUniversity of MünsterMünsterGermany

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