A strategy for large-scale phosphoproteomics and SRM-based validation of human breast cancer tissue samples

Journal of Proteome Research

Volumn 11, Issue 11, 2012, Pages 5311-5322

  Narumi, Ryohei ^a   Murakami, Tatsuo ^a   Kuga, Takahisa ^a   Adachi, Jun ^a   Shiromizu, Takashi ^a   Muraoka, Satoshi ^a   Kume, Hideaki ^a   Kodera, Yoshio ^b,c   Matsumoto, Masaki ^d   Nakayama, Keiichi ^d   Miyamoto, Yasuhide ^e   Ishitobi, Makoto ^e   Inaji, Hideo ^e   Kato, Kikuya ^e   Tomonaga, Takeshi ^a,c  

^a NATIONAL INSTITUTE OF BIOMEDICAL INNOVATION   (Japan)

^b KITASATO UNIVERSITY   (Japan)

^c CHIBA UNIVERSITY HOSPITAL   (Japan)

^d KYUSHU UNIVERSITY   (Japan)

^e OSAKA MEDICAL CENTER FOR CANCER AND CARDIOVASCULAR DISEASES   (Japan)

Author keywords

breast cancer tissue; iTRAQ; mammaprint; phosphoproteome; SRM

Indexed keywords

PHOSPHOPEPTIDE; PHOSPHOPROTEIN; PROTEOME;

ARTICLE; BREAST CANCER; CANCER RECURRENCE; DISEASE MARKER; HUMAN; HUMAN TISSUE; INTRACELLULAR SIGNALING; ISOTOPE LABELING; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEOMICS;

BIOLOGICAL MARKERS; BLOTTING, WESTERN; BREAST NEOPLASMS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CHROMATOGRAPHY, ION EXCHANGE; FEMALE; HUMANS; PHOSPHOPROTEINS; PROTEOMICS; TANDEM MASS SPECTROMETRY;

EID: 84868312185     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr3005474     Document Type: Article

References (63)

1. Hanahan, D.; Weinberg, R. A. The hallmarks of cancer Cell 2000, 100 (1) 57-70
2. Kaminska, B. MAPK signalling pathways as molecular targets for anti-inflammatory therapy - from molecular mechanisms to therapeutic benefits Biochim. Biophys. Acta 2005, 1754 (1-2) 253-62
3. Peifer, C.; Wagner, G.; Laufer, S. New approaches to the treatment of inflammatory disorders small molecule inhibitors of p38 MAP kinase Curr. Top. Med. Chem. 2006, 6 (2) 113-49
4. White, M. F. Regulating insulin signaling and beta-cell function through IRS proteins Can. J. Physiol. Pharmacol. 2006, 84 (7) 725-37
5. Neville, D. C.; Rozanas, C. R.; Price, E. M.; Gruis, D. B.; Verkman, A. S.; Townsend, R. R. Evidence for phosphorylation of serine 753 in CFTR using a novel metal-ion affinity resin and matrix-assisted laser desorption mass spectrometry Protein Sci. 1997, 6 (11) 2436-45
6. Ong, S. E.; Blagoev, B.; Kratchmarova, I.; Kristensen, D. B.; Steen, H.; Pandey, A.; Mann, M. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics Mol. Cell. Proteomics 2002, 1 (5) 376-86
7. Ross, P. L.; Huang, Y. N.; Marchese, J. N.; Williamson, B.; Parker, K.; Hattan, S.; Khainovski, N.; Pillai, S.; Dey, S.; Daniels, S.; Purkayastha, S.; Juhasz, P.; Martin, S.; Bartlet-Jones, M.; He, F.; Jacobson, A.; Pappin, D. J. Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents Mol. Cell. Proteomics 2004, 3 (12) 1154-69
8. Collins, M. O.; Yu, L.; Coba, M. P.; Husi, H.; Campuzano, I.; Blackstock, W. P.; Choudhary, J. S.; Grant, S. G. Proteomic analysis of in vivo phosphorylated synaptic proteins J. Biol. Chem. 2005, 280 (7) 5972-82
9. Molina, H.; Horn, D. M.; Tang, N.; Mathivanan, S.; Pandey, A. Global proteomic profiling of phosphopeptides using electron transfer dissociation tandem mass spectrometry Proc. Natl. Acad. Sci. U. S. A. 2007, 104 (7) 2199-204
10. Wissing, J.; Jansch, L.; Nimtz, M.; Dieterich, G.; Hornberger, R.; Keri, G.; Wehland, J.; Daub, H. Proteomics analysis of protein kinases by target class-selective prefractionation and tandem mass spectrometry Mol. Cell. Proteomics 2007, 6 (3) 537-47
11. Villen, J.; Beausoleil, S. A.; Gerber, S. A.; Gygi, S. P. Large-scale phosphorylation analysis of mouse liver Proc. Natl. Acad. Sci. U. S. A. 2007, 104 (5) 1488-93
12. Ballif, B. A.; Villen, J.; Beausoleil, S. A.; Schwartz, D.; Gygi, S. P. Phosphoproteomic analysis of the developing mouse brain Mol. Cell. Proteomics 2004, 3 (11) 1093-101
13. Beausoleil, S. A.; Jedrychowski, M.; Schwartz, D.; Elias, J. E.; Villen, J.; Li, J.; Cohn, M. A.; Cantley, L. C.; Gygi, S. P. Large-scale characterization of HeLa cell nuclear phosphoproteins Proc. Natl. Acad. Sci. U. S. A. 2004, 101 (33) 12130-5
14. Ficarro, S. B.; McCleland, M. L.; Stukenberg, P. T.; Burke, D. J.; Ross, M. M.; Shabanowitz, J.; Hunt, D. F.; White, F. M. Phosphoproteome analysis by mass spectrometry and its application to Saccharomyces cerevisiae Nat. Biotechnol. 2002, 20 (3) 301-5
15. Lee, J.; Xu, Y.; Chen, Y.; Sprung, R.; Kim, S. C.; Xie, S.; Zhao, Y. Mitochondrial phosphoproteome revealed by an improved IMAC method and MS/MS/MS Mol. Cell. Proteomics 2007, 6 (4) 669-76
16. Moser, K.; White, F. M. Phosphoproteomic analysis of rat liver by high capacity IMAC and LC-MS/MS J. Proteome Res. 2006, 5 (1) 98-104
17. Trinidad, J. C.; Specht, C. G.; Thalhammer, A.; Schoepfer, R.; Burlingame, A. L. Comprehensive identification of phosphorylation sites in postsynaptic density preparations Mol. Cell. Proteomics 2006, 5 (5) 914-22
18. Li, X.; Gerber, S. A.; Rudner, A. D.; Beausoleil, S. A.; Haas, W.; Villen, J.; Elias, J. E.; Gygi, S. P. Large-scale phosphorylation analysis of alpha-factor-arrested Saccharomyces cerevisiae J. Proteome Res. 2007, 6 (3) 1190-7
19. Matsuoka, S.; Ballif, B. A.; Smogorzewska, A.; McDonald, E. R., 3rd; Hurov, K. E.; Luo, J.; Bakalarski, C. E.; Zhao, Z.; Solimini, N.; Lerenthal, Y.; Shiloh, Y.; Gygi, S. P.; Elledge, S. J. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage Science 2007, 316 (5828) 1160-6
20. Olsen, J. V.; Blagoev, B.; Gnad, F.; Macek, B.; Kumar, C.; Mortensen, P.; Mann, M. Global, in vivo, and site-specific phosphorylation dynamics in signaling networks Cell 2006, 127 (3) 635-48
21. Trinidad, J. C.; Thalhammer, A.; Specht, C. G.; Lynn, A. J.; Baker, P. R.; Schoepfer, R.; Burlingame, A. L. Quantitative analysis of synaptic phosphorylation and protein expression Mol. Cell. Proteomics 2008, 7 (4) 684-96
22. Nguyen, V.; Cao, L.; Lin, J. T.; Hung, N.; Ritz, A.; Yu, K.; Jianu, R.; Ulin, S. P.; Raphael, B. J.; Laidlaw, D. H.; Brossay, L.; Salomon, A. R. A new approach for quantitative phosphoproteomic dissection of signaling pathways applied to T cell receptor activation Mol. Cell. Proteomics 2009, 8 (11) 2418-31
23. Zanivan, S.; Gnad, F.; Wickstrom, S. A.; Geiger, T.; Macek, B.; Cox, J.; Fassler, R.; Mann, M. Solid tumor proteome and phosphoproteome analysis by high resolution mass spectrometry J. Proteome Res. 2008, 7 (12) 5314-26
24. Anderson, N. L. The roles of multiple proteomic platforms in a pipeline for new diagnostics Mol. Cell. Proteomics 2005, 4 (10) 1441-4
25. Lange, V.; Malmstrom, J. A.; Didion, J.; King, N. L.; Johansson, B. P.; Schafer, J.; Rameseder, J.; Wong, C. H.; Deutsch, E. W.; Brusniak, M. Y.; Buhlmann, P.; Bjorck, L.; Domon, B.; Aebersold, R. Targeted quantitative analysis of Streptococcus pyogenes virulence factors by multiple reaction monitoring Mol. Cell. Proteomics 2008, 7 (8) 1489-500
26. Kuhn, E.; Wu, J.; Karl, J.; Liao, H.; Zolg, W.; Guild, B. Quantification of C-reactive protein in the serum of patients with rheumatoid arthritis using multiple reaction monitoring mass spectrometry and 13C-labeled peptide standards Proteomics 2004, 4 (4) 1175-86
27. Anderson, L.; Hunter, C. L. Quantitative mass spectrometric multiple reaction monitoring assays for major plasma proteins Mol. Cell. Proteomics 2006, 5 (4) 573-88
28. Keshishian, H.; Addona, T.; Burgess, M.; Kuhn, E.; Carr, S. A. Quantitative, multiplexed assays for low abundance proteins in plasma by targeted mass spectrometry and stable isotope dilution Mol. Cell. Proteomics 2007, 6 (12) 2212-29
29. Keshishian, H.; Addona, T.; Burgess, M.; Mani, D. R.; Shi, X.; Kuhn, E.; Sabatine, M. S.; Gerszten, R. E.; Carr, S. A. Quantification of cardiovascular biomarkers in patient plasma by targeted mass spectrometry and stable isotope dilution Mol. Cell. Proteomics 2009, 8 (10) 2339-49
30. van 't Veer, L. J.; Dai, H.; van de Vijver, M. J.; He, Y. D.; Hart, A. A.; Mao, M.; Peterse, H. L.; van der Kooy, K.; Marton, M. J.; Witteveen, A. T.; Schreiber, G. J.; Kerkhoven, R. M.; Roberts, C.; Linsley, P. S.; Bernards, R.; Friend, S. H. Gene expression profiling predicts clinical outcome of breast cancer Nature 2002, 415 (6871) 530-6
31. Masuda, T.; Tomita, M.; Ishihama, Y. Phase transfer surfactant-aided trypsin digestion for membrane proteome analysis J. Proteome Res. 2008, 7 (2) 731-40
32. Matsumoto, M.; Oyamada, K.; Takahashi, H.; Sato, T.; Hatakeyama, S.; Nakayama, K. I. Large-scale proteomic analysis of tyrosine-phosphorylation induced by T-cell receptor or B-cell receptor activation reveals new signaling pathways Proteomics 2009, 9 (13) 3549-63
33. Kokubu, M.; Ishihama, Y.; Sato, T.; Nagasu, T.; Oda, Y. Specificity of immobilized metal affinity-based IMAC/C18 tip enrichment of phosphopeptides for protein phosphorylation analysis Anal. Chem. 2005, 77 (16) 5144-54
34. Taus, T.; Kocher, T.; Pichler, P.; Paschke, C.; Schmidt, A.; Henrich, C.; Mechtler, K. Universal and confident phosphorylation site localization using phosphoRS J. Proteome Res. 2011, 10 (12) 5354-62
35. Martins-de-Souza, D.; Guest, P. C.; Vanattou-Saifoudine, N.; Rahmoune, H.; Bahn, S. Phosphoproteomic differences in major depressive disorder postmortem brains indicate effects on synaptic function. Eur. Arch. Psychiatry Clin. Neurosci. 2012, not supplied.
36. Jarvinen, T. A.; Tanner, M.; Barlund, M.; Borg, A.; Isola, J. Characterization of topoisomerase II alpha gene amplification and deletion in breast cancer Genes, Chromosomes Cancer 1999, 26 (2) 142-50
37. Nielsen, K. V.; Muller, S.; Moller, S.; Schonau, A.; Balslev, E.; Knoop, A. S.; Ejlertsen, B. Aberrations of ERBB2 and TOP2A genes in breast cancer Mol. Oncol. 2010, 4 (2) 161-8
38. Futreal, P. A.; Liu, Q.; Shattuck-Eidens, D.; Cochran, C.; Harshman, K.; Tavtigian, S.; Bennett, L. M.; Haugen-Strano, A.; Swensen, J.; Miki, Y. BRCA1 mutations in primary breast and ovarian carcinomas Science 1994, 266 (5182) 120-2
39. O'Donovan, P. J.; Livingston, D. M. BRCA1 and BRCA2: breast/ovarian cancer susceptibility gene products and participants in DNA double-strand break repair Carcinogenesis 2010, 31 (6) 961-7
40. Castilla, L. H.; Couch, F. J.; Erdos, M. R.; Hoskins, K. F.; Calzone, K.; Garber, J. E.; Boyd, J.; Lubin, M. B.; Deshano, M. L.; Brody, L. C. Mutations in the BRCA1 gene in families with early-onset breast and ovarian cancer Nat. Genet. 1994, 8 (4) 387-91
41. Kim, S. J.; Nakayama, S.; Miyoshi, Y.; Taguchi, T.; Tamaki, Y.; Matsushima, T.; Torikoshi, Y.; Tanaka, S.; Yoshida, T.; Ishihara, H.; Noguchi, S. Determination of the specific activity of CDK1 and CDK2 as a novel prognostic indicator for early breast cancer Ann. Oncol. 2008, 19 (1) 68-72
42. Nasir, A.; Chen, D. T.; Gruidl, M.; Henderson-Jackson, E. B.; Venkataramu, C.; McCarthy, S. M.; McBride, H. L.; Harris, E.; Khakpour, N.; Yeatman, T. J. Novel molecular markers of malignancy in histologically normal and benign breast Pathol. Res. Int. 2011, 2011, 489064
43. Zheng, M. Z.; Zheng, L. M.; Zeng, Y. X. SCC-112 gene is involved in tumor progression and promotes the cell proliferation in G2/M phase J. Cancer Res. Clin. Oncol. 2008, 134 (4) 453-62
44. Rakha, E. A.; Boyce, R. W.; Abd El-Rehim, D.; Kurien, T.; Green, A. R.; Paish, E. C.; Robertson, J. F.; Ellis, I. O. Expression of mucins (MUC1, MUC2, MUC3, MUC4, MUC5AC and MUC6) and their prognostic significance in human breast cancer Mod. Pathol. 2005, 18 (10) 1295-304
45. Wei, X.; Xu, H.; Kufe, D. MUC1 oncoprotein stabilizes and activates estrogen receptor alpha Mol. Cell 2006, 21 (2) 295-305
46. Mulligan, A. M.; Pinnaduwage, D.; Bane, A. L.; Bull, S. B.; O'Malley, F. P.; Andrulis, I. L. CK8/18 expression, the basal phenotype, and family history in identifying BRCA1-associated breast cancer in the Ontario site of the breast cancer family registry Cancer 2011, 117 (7) 1350-9
47. Busch, T.; Milena; Eiseler, T.; Joodi, G.; Temme, C.; Jansen, J.; Wichert, G. V.; Omary, M. B.; Spatz, J.; Seufferlein, T. Keratin 8 phosphorylation regulates keratin reorganization and migration of epithelial tumor cells J. Cell Sci. 2012, 2148-59
48. Hu, Q.; Guo, C.; Li, Y.; Aronow, B. J.; Zhang, J. LMO7 mediates cell-specific activation of the Rho-myocardin-related transcription factor-serum response factor pathway and plays an important role in breast cancer cell migration Mol. Cell. Biol. 2011, 31 (16) 3223-40
49. Merrell, K. W.; Crofts, J. D.; Smith, R. L.; Sin, J. H.; Kmetzsch, K. E.; Merrell, A.; Miguel, R. O.; Candelaria, N. R.; Lin, C. Y. Differential recruitment of nuclear receptor coregulators in ligand-dependent transcriptional repression by estrogen receptor-alpha Oncogene 2011, 30 (13) 1608-14
50. Hartmaier, R. J.; Tchatchou, S.; Richter, A. S.; Wang, J.; McGuire, S. E.; Skaar, T. C.; Rae, J. M.; Hemminki, K.; Sutter, C.; Ditsch, N.; Bugert, P.; Weber, B. H.; Niederacher, D.; Arnold, N.; Varon-Mateeva, R.; Wappenschmidt, B.; Schmutzler, R. K.; Meindl, A.; Bartram, C. R.; Burwinkel, B.; Oesterreich, S. Nuclear receptor coregulator SNP discovery and impact on breast cancer risk BMC Cancer 2009, 9, 438
51. Lemeer, S.; Heck, A. J. The phosphoproteomics data explosion Curr. Opin. Chem. Biol. 2009, 13 (4) 414-20
52. Larsen, M. R.; Thingholm, T. E.; Jensen, O. N.; Roepstorff, P.; Jorgensen, T. J. Highly selective enrichment of phosphorylated peptides from peptide mixtures using titanium dioxide microcolumns Mol. Cell. Proteomics 2005, 4 (7) 873-86
53. Rush, J.; Moritz, A.; Lee, K. A.; Guo, A.; Goss, V. L.; Spek, E. J.; Zhang, H.; Zha, X. M.; Polakiewicz, R. D.; Comb, M. J. Immunoaffinity profiling of tyrosine phosphorylation in cancer cells Nat. Biotechnol. 2005, 23 (1) 94-101
54. Dephoure, N.; Zhou, C.; Villen, J.; Beausoleil, S. A.; Bakalarski, C. E.; Elledge, S. J.; Gygi, S. P. A quantitative atlas of mitotic phosphorylation Proc. Natl. Acad. Sci. U. S. A. 2008, 105 (31) 10762-7
55. Ostasiewicz, P.; Zielinska, D. F.; Mann, M.; Wisniewski, J. R. Proteome, phosphoproteome, and N-glycoproteome are quantitatively preserved in formalin-fixed paraffin-embedded tissue and analyzable by high-resolution mass spectrometry J. Proteome Res. 2010, 9 (7) 3688-700
56. Whiteaker, J. R.; Lin, C.; Kennedy, J.; Hou, L.; Trute, M.; Sokal, I.; Yan, P.; Schoenherr, R. M.; Zhao, L.; Voytovich, U. J.; Kelly-Spratt, K. S.; Krasnoselsky, A.; Gafken, P. R.; Hogan, J. M.; Jones, L. A.; Wang, P.; Amon, L.; Chodosh, L. A.; Nelson, P. S.; McIntosh, M. W.; Kemp, C. J.; Paulovich, A. G. A targeted proteomics-based pipeline for verification of biomarkers in plasma Nat. Biotechnol. 2011, 29 (7) 625-34
57. Addona, T. A.; Shi, X.; Keshishian, H.; Mani, D. R.; Burgess, M.; Gillette, M. A.; Clauser, K. R.; Shen, D.; Lewis, G. D.; Farrell, L. A.; Fifer, M. A.; Sabatine, M. S.; Gerszten, R. E.; Carr, S. A. A pipeline that integrates the discovery and verification of plasma protein biomarkers reveals candidate markers for cardiovascular disease Nat. Biotechnol. 2011, 29 (7) 635-43
58. Atrih, A.; Turnock, D.; Sellar, G.; Thompson, A.; Feuerstein, G.; Ferguson, M. A.; Huang, J. T. Stoichiometric quantification of Akt phosphorylation using LC-MS/MS J. Proteome Res. 2010, 9 (2) 743-51
59. Jin, L. L.; Tong, J.; Prakash, A.; Peterman, S. M.; St-Germain, J. R.; Taylor, P.; Trudel, S.; Moran, M. F. Measurement of protein phosphorylation stoichiometry by selected reaction monitoring mass spectrometry J. Proteome Res. 2010, 9 (5) 2752-61
60. Tong, J.; Taylor, P.; Peterman, S. M.; Prakash, A.; Moran, M. F. Epidermal growth factor receptor phosphorylation sites Ser991 and Tyr998 are implicated in the regulation of receptor endocytosis and phosphorylations at Ser1039 and Thr1041 Mol. Cell. Proteomics 2009, 8 (9) 2131-44
61. Wolf-Yadlin, A.; Hautaniemi, S.; Lauffenburger, D. A.; White, F. M. Multiple reaction monitoring for robust quantitative proteomic analysis of cellular signaling networks Proc. Natl. Acad. Sci. U. S. A. 2007, 104 (14) 5860-5
62. Thingholm, T. E.; Bak, S.; Beck-Nielsen, H.; Jensen, O. N.; Gaster, M. Characterization of human myotubes from type 2 diabetic and nondiabetic subjects using complementary quantitative mass spectrometric methods Mol. Cell. Proteomics 2011, 10 (9) M110 006650
63. Muraoka, S.; Kume, H.; Watanabe, S.; Adachi, J.; Kuwano, M.; Sato, M.; Kawasaki, N.; Kodera, Y.; Ishitobi, M.; Inaji, H.; Miyamoto, Y.; Kato, K.; Tomonaga, T. Strategy for SRM-based verification of biomarker candidates discovered by iTRAQ method in limited breast cancer tissue samples J. Proteome Res. 2012, 11 (8) 4201-10