Mass spectrometry mapping of epidermal growth factor receptor phosphorylation related to oncogenic mutations and tyrosine kinase inhibitor sensitivity

Journal of Proteome Research

Volumn 10, Issue 1, 2011, Pages 305-319

  Zhang, Guolin ^a   Fang, Bin ^a   Liu, Richard Z ^a   Lin, Huiyi ^a   Kinose, Fumi ^a   Bai, Yun ^a   Oguz, Umut ^a   Remily Wood, Elizabeth R ^a   Li, Jiannong ^a   Altiok, Soner ^a   Eschrich, Steven ^a   Koomen, John ^a   Haura, Eric B ^a  

^a H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

Author keywords

Epidermal growth factor receptor; Erlotinib; Lung cancer; Mass spectrometry; Proteomics; Tyrosine kinase inhibitor; Tyrosine phosphorylation

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; ERLOTINIB; PROTEIN TYROSINE KINASE INHIBITOR; RECOMBINANT PROTEIN;

CANCER CELL; CANCER CHEMOTHERAPY; CHEMOSENSITIVITY; CONFERENCE PAPER; CONTROLLED STUDY; ENZYME INHIBITION; HUMAN; HUMAN CELL; LIQUID CHROMATOGRAPHY; LUNG CANCER; LUNG NON SMALL CELL CANCER; MASS SPECTROMETRY; PEPTIDE SYNTHESIS; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEOMICS; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; SOMATIC MUTATION; TANDEM MASS SPECTROMETRY; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ANIMALS; BLOTTING, WESTERN; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; CHROMATOGRAPHY, LIQUID; DRUG RESISTANCE, NEOPLASM; IMMUNOPRECIPITATION; LUNG NEOPLASMS; MICE; MICE, NUDE; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PEPTIDE MAPPING; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTEIN-TYROSINE KINASES; QUINAZOLINES; RECEPTOR, EPIDERMAL GROWTH FACTOR; REPRODUCIBILITY OF RESULTS; TANDEM MASS SPECTROMETRY; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 79951521007     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr1006203     Document Type: Conference Paper

References (76)

1. Blume-Jensen, P.; Hunter, T. Oncogenic kinase signalling. Nature 2001, 411 (6835), 355-65. (Pubitemid 32467045)
2. Pawson, T. Specificity in signal transduction: from phosphotyrosine- SH2 domain interactions to complex cellular systems. Cell 2004, 116 (2), 191-203. (Pubitemid 38167312)
3. Hackel, P. O.; Zwick, E.; Prenzel, N.; Ullrich, A. Epidermal growth factor receptors: critical mediators of multiple receptor pathways. Curr. Opin. Cell Biol. 1999, 11 (2), 184-9. (Pubitemid 29164032)
4. Zwick, E.; Hackel, P. O.; Prenzel, N.; Ullrich, A. The EGF receptor as central transducer of heterologous signalling systems. Trends Pharmacol. Sci. 1999, 20 (10), 408-12. (Pubitemid 29450362)
5. Schulze, W. X.; Deng, L.; Mann, M. Phosphotyrosine interactome of the ErbB-receptor kinase family. Mol. Syst. Biol. 2005, 1, 2005-0008.
6. Dowell, J.; Minna, J. D.; Kirkpatrick, P. Erlotinib hydrochloride. Nat. Rev. Drug Discovery 2005, 4 (1), 13-4. (Pubitemid 40109581)
7. Melnikova, I.; Golden, J. Targeting protein kinases. Nat. Rev. Drug Discovery 2004, 3 (12), 993-4. (Pubitemid 39642356)
8. Copeman, M. Prolonged response to first-line erlotinib for advanced lung adenocarcinoma. J. Exp. Clin. Cancer Res. 2008, 27, 59.
9. Sharma, S. P. New predictors of survival for early-stage NSCLC. Lancet Oncol. 2007, 8 (4), 288.
10. Sharma, S. P. Gene signature for predicting NSCLC outcome. Lancet Oncol. 2007, 8 (2), 105.
11. Sharma, S. V.; Bell, D. W.; Settleman, J.; Haber, D. A. Epidermal growth factor receptor mutations in lung cancer. Nat. Rev. Cancer 2007, 7 (3), 169-81.
12. Morandell, S.; Stasyk, T.; Skvortsov, S.; Ascher, S.; Huber, L. A. Quantitative proteomics and phosphoproteomics reveal novel insights into complexity and dynamics of the EGFR signaling network. Proteomics 2008, 8 (21), 4383-401.
13. Rikova, K.; Guo, A.; Zeng, Q.; Possemato, A.; Yu, J.; Haack, H.; Nardone, J.; Lee, K.; Reeves, C.; Li, Y.; Hu, Y.; Tan, Z.; Stokes, M.; Sullivan, L.; Mitchell, J.; Wetzel, R.; Macneill, J.; Ren, J. M.; Yuan, J.; Bakalarski, C. E.; Villen, J.; Kornhauser, J. M.; Smith, B.; Li, D.; Zhou, X.; Gygi, S. P.; Gu, T. L.; Polakiewicz, R. D.; Rush, J.; Comb, M. J. Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer. Cell 2007, 131 (6), 1190-203. (Pubitemid 350235027)
14. Blagoev, B.; Kratchmarova, I.; Ong, S. E.; Nielsen, M.; Foster, L. J.; Mann, M. A proteomics strategy to elucidate functional proteinprotein interactions applied to EGF signaling. Nat. Biotechnol. 2003, 21 (3), 315-8. (Pubitemid 36314817)
15. Boeri Erba, E.; Bergatto, E.; Cabodi, S.; Silengo, L.; Tarone, G.; Defilippi, P.; Jensen, O. N. Systematic analysis of the epidermal growth factor receptor by mass spectrometry reveals stimulationdependent multisite phosphorylation. Mol. Cell. Proteomics 2005, 4 (8), 1107-21. (Pubitemid 41223370)
16. Huang, P. H.; White, F. M. Phosphoproteomics: unraveling the signaling web. Mol. Cell 2008, 31 (6), 777-81.
17. 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. (Pubitemid 44647421)
18. Oppermann, F. S.; Gnad, F.; Olsen, J. V.; Hornberger, R.; Greff, Z.; Keri, G.; Mann, M.; Daub, H. Large-scale proteomics analysis of the human kinome. Mol. Cell. Proteomics 2009, 8 (7), 1751-64.
19. Oyama, M.; Kozuka-Hata, H.; Tasaki, S.; Semba, K.; Hattori, S.; Sugano, S.; Inoue, J.; Yamamoto, T. Temporal perturbation of tyrosine phosphoproteome dynamics reveals the system-wide regulatory networks. Mol. Cell. Proteomics 2009, 8 (2), 226-31.
20. Pan, C.; Olsen, J. V.; Daub, H.; Mann, M. Global effects of kinase inhibitors on signaling networks revealed by quantitative phosphoproteomics. Mol. Cell. Proteomics 2009.
21. Zhang, Y.; Wolf-Yadlin, A.; Ross, P. L.; Pappin, D. J.; Rush, J.; Lauffenburger, D. A.; White, F. M. Time-resolved mass spectrometry of tyrosine phosphorylation sites in the epidermal growth factor receptor signaling network reveals dynamic modules. Mol. Cell. Proteomics 2005, 4 (9), 1240-50. (Pubitemid 41448712)
22. VanMeter, A. J.; Rodriguez, A. S.; Bowman, E. D.; Jen, J.; Harris, C. C.; Deng, J.; Calvert, V. S.; Silvestri, A.; Fredolini, C.; Chandhoke, V.; Petricoin, E. F., 3rd; Liotta, L. A.; Espina, V. Laser capture microdissection and protein microarray analysis of human nonsmall cell lung cancer: differential epidermal growth factor receptor (EGPR) phosphorylation events associated with mutated EGFR compared with wild type. Mol. Cell. Proteomics 2008, 7 (10), 1902-24.
23. Wu, S. L.; Kim, J.; Bandle, R. W.; Liotta, L.; Petricoin, E.; Karger, B. L. Dynamic profiling of the post-translational modifications and interaction partners of epidermal growth factor receptor signaling after stimulation by epidermal growth factor using Extended Range Proteomic Analysis (ERPA). Mol. Cell. Proteomics 2006, 5 (9), 1610-27. (Pubitemid 44480389)
24. 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. (Pubitemid 46554547)
25. Wu, S. L.; Kim, J.; Hancock, W. S.; Karger, B. Extended Range Proteomic Analysis (ERPA): a new and sensitive LC-MS platform for high sequence coverage of complex proteins with extensive post-translational modifications- comprehensive analysis of betacasein and epidermal growth factor receptor (EGFR). J. Proteome Res. 2005, 4 (4), 1155-70. (Pubitemid 41208674)
26. Tong, J.; Taylor, P.; Jovceva, E.; St-Germain, J. R.; Jin, L. L.; Nikolic, A.; Gu, X.; Li, Z. H.; Trudel, S.; Moran, M. F. Tandem immunoprecipitation of phosphotyrosine-mass spectrometry (TIPY-MS) indicates C19ORF19 becomes tyrosine-phosphorylated and associated with activated epidermal growth factor receptor. J. Proteome Res. 2008, 7 (3), 1067-77.
27. 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.
28. Guha, U.; Chaerkady, R.; Marimuthu, A.; Patterson, A. S.; Kashyap, M. K.; Harsha, H. C.; Sato, M.; Bader, J. S.; Lash, A. E.; Minna, J. D.; Pandey, A.; Varmus, H. E. Comparisons of tyrosine phosphorylated proteins in cells expressing lung cancer-specific alleles of EGFR and KRAS. Proc. Natl. Acad. Sci. U.S.A. 2008, 105 (37), 14112M-7.
29. Guo, A.; Villen, J.; Kornhauser, J.; Lee, K. A.; Stokes, M. P.; Rikova, K.; Possemato, A.; Nardone, J.; Innocenti, G.; Wetzel, R.; Wang, Y.; MacNeill, J.; Mitchell, J.; Gygi, S. P.; Rush, J.; Polakiewicz, R. D.; Comb, M. J. Signaling networks assembled by oncogenic EGFR and c-Met. Proc. Natl. Acad. Sci. U.S.A. 2008, 105 (2), 692-7. (Pubitemid 351171770)
30. Macek, B.; Mann, M.; Olsen, J. V. Global and site-specific uantitative phosphoproteomics: principles and applications. Annu. Rev. Pharmacol. Toxicol. 2009, 49, 199-221.
31. Heisermann, G. J.; Gill, G. N. Epidermal growth factor receptor threonine and serine residues phosphorylated in vivo. J. Biol. Chem. 1988, 263 (26), 13152-8.
32. Heisermann, G. J.; Wiley, H. S.; Walsh, B. J.; Ingraham, H. A.; Fiol, C. J.; Gill, G. N. Mutational removal of the Thr669 and Ser671 phosphorylation sites alters substrate specificity and ligandinduced internalization of the epidermal growth factor receptor. J. Biol. Chem. 1990, 265 (22), 12820-7.
33. Bishayee, A.; Beguinot, L.; Bishayee, S. Phosphorylation of tyrosine 992, 1068, and 1086 is required for conformational change of the human epidermal growth factor receptor c-terminal tail. Mol. Biol. Cell 1999, 10 (3), 525-36. (Pubitemid 29144621)
34. Kuppuswamy, D.; Dalton, M.; Pike, L. J. Serine 1002 is a site of in vivo and in vitro phosphorylation of the epidermal growth factor receptor. J. Biol. Chem. 1993, 268 (25), 19134-42. (Pubitemid 23273870)
35. Pao, W.; Miller, V.; Zakowski, M.; Doherty, J.; Politi, K.; Sarkaria, I.; Singh, B.; Heelan, R.; Rusch, V.; Fulton, L.; Mardis, E.; Kupfer, D.; Wilson, R.; Kris, M.; Varmus, H. EGF receptor gene mutations are common in lung cancers from "never smokers" and are associated with sensitivity of tumors to gefitinib and erlotinib. Proc. Natl. Acad. Sci. U.S.A. 2004, 101 (36), 13306-11. (Pubitemid 39209661)
36. Morgan, M. A.; Parsels, L. A.; Kollar, L. E.; Normolle, D. P.; Maybaum, J.; Lawrence, T. S. The combination of epidermal growth factor receptor inhibitors with gemcitabine and radiation in pancreatic cancer. Clin. Cancer Res. 2008, 14 (16), 5142-9.
37. Tan, A. R.; Yang, X.; Hewitt, S. M.; Berman, A.; Lepper, E. R.; Sparreboom, A.; Parr, A. L.; Figg, W. D.; Chow, C.; Steinberg, S. M.; Bacharach, S. L.; Whatley, M.; Carrasquillo, J. A.; Brahim, J. S.; Ettenberg, S. A.; Lipkowitz, S.; Swain, S. M. Evaluation of biologic end points and pharmacokinetics in patients with metastatic breast cancer after treatment with erlotinib, an epidermal growth factor receptor tyrosine kinase inhibitor. J. Clin. Oncol. 2004, 22 (15), 3080-90. (Pubitemid 41103720)
38. Zhang, X.; Zhang, H.; Tighiouart, M.; Lee, J. E.; Shin, H. J.; Khuri, F. R.; Yang, C. S.; Chen, Z. G.; Shin, D. M. Synergistic inhibition of head and neck tumor growth by green tea (-)-epigallocatechin- 3-gallate and EGFR tyrosine kinase inhibitor. Int. J. Cancer 2008, 123 (5), 1005-14.
39. Li, T.; Ling, Y. H.; Perez-Soler, R. Tumor dependence on the EGFR signaling pathway expressed by the p-EGFR:p-AKT ratio predicts erlotinib sensitivity in human non-small cell lung cancer (NSCLC) cells expressing wild-type EGFR gene. J. Thorac. Oncol. 2008, 3 (6), 643-7. (Pubitemid 351787310)
40. Makarov, A.; Denisov, E.; Lange, O.; Horning, S. Dynamic range of mass accuracy in LTQ Orbitrap hybrid mass spectrometer. J. Am. Soc. Mass Spectrom. 2006, 17 (7), 977-82. (Pubitemid 43928612)
41. Yates, J. R.; Ruse, C. I.; Nakorchevsky, A. Proteomics by mass spectrometry: approaches, advances, and applications. Annu. Rev. Biomed. Eng. 2009, 11, 49-79.
42. Witze, E. S.; Old, W. M.; Resing, K. A.; Ahn, N. G. Mapping protein post-translational modifications with mass spectrometry. Nat. Methods 2007, 4 (10), 798-806. (Pubitemid 350055576)
43. Gnad, F.; Ren, S.; Cox, J.; Olsen, J. V.; Macek, B.; Oroshi, M.; Mann, M. PHOSIDA (phosphorylation site database): management, structural and evolutionary investigation, and prediction of phosphosites. Genome Biol. 2007, 8 (11), R250.
44. Diella, F.; Gould, C. M.; Chica, C.; Via, A.; Gibson, T. J. Phospho- .ELM: a database of phosphorylation sites-update 2008. Nucleic Acids Res. 2008, 36 (Database Issue), D240-4.
45. Linding, R.; Jensen, L. J.; Pasculescu, A.; Olhovsky, M.; Colwill, K.; Bork, P.; Yaffe, M. B.; Pawson, T. NetworKIN: a resource for exploring cellular phosphorylation networks. Nucleic Acids Res. 2008, 36 (Database Issue), D695-9.
46. Hornbeck, P. V.; Chabra, I.; Kornhauser, J. M.; Skrzypek, E.; Zhang, B. PhosphoSite: A bioinformatics resource dedicated to physiological protein phosphorylation. Proteomics 2004, 4 (6), 1551-61. (Pubitemid 38738314)
47. Li, H.; Xing, X.; Ding, G.; Li, Q.; Wang, C.; Xie, L.; Zeng, R.; Li, Y. SysPTM: a systematic resource for proteomic research on posttranslational modifications. Mol. Cell. Proteomics 2009, 8 (8), 1839-49.
48. Obenauer, J. C.; Cantley, L. C.; Yaffe, M. B. Scansite 2.0: Proteomewide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res. 2003, 31 (13), 3635-41. (Pubitemid 37442212)
49. Li, J.; Rix, U.; Fang, B.; Bai, Y.; Edwards, A.; Colinge, J.; Bennett, K. L.; Gao, J.; Song, L.; Eschrich, S.; Superti-Furga, G.; Koomen, J.; Haura, E. B. A chemical and phosphoproteomic characterization of dasatinib action in lung cancer. Nat. Chem. Biol. , 6 (4), 291-9.
50. Patel, V. J.; Thalassinos, K.; Slade, S. E.; Connolly, J. B.; Crombie, A.; Murrell, J. C.; Scrivens, J. H. A comparison of labeling and labelfree mass spectrometry-based proteomics approaches. J. Proteome Res. 2009, 8 (7), 3752-9.
51. MacCoss, M. J.; Wu, C. C.; Yates, J. R. 3rd, Probability-based validation of protein identifications using a modified SEQUEST algorithm. Anal. Chem. 2002, 74 (21), 5593-9. (Pubitemid 35253125)
52. Perkins, D. N.; Pappin, D. J.; Creasy, D. M.; Cottrell, J. S. Probabilitybased protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 1999, 20 (18), 3551-67. (Pubitemid 30007252)
53. Hirosawa, M.; Hoshida, M.; Ishikawa, M.; Toya, T. MASCOT: multiple alignment system for protein sequences based on threeway dynamic programming. Comput. Appl. Biosci. 1993, 9 (2), 161-7. (Pubitemid 23127138)
54. Blackburn, K.; Goshe, M. B. Challenges and strategies for targeted phosphorylation site identification and quantification using mass spectrometry analysis. Brief Funct. Genomic Proteomic 2009, 8 (2), 90-103.
55. Nichols, A. M.; White, F. M. Manual validation of peptide sequence and sites of tyrosine phosphorylation from MS/MS spectra. Methods Mol. Biol. 2009, 492, 143-60.
56. Prakash, A.; Tomazela, D. M.; Frewen, B.; Maclean, B.; Merrihew, G.; Peterman, S.; Maccoss, M. J. Expediting the development of targeted SRM assays: using data from shotgun proteomics to automate method development. J. Proteome Res. 2009, 8 (6), 2733-9.
57. MacLean, B.; Tomazela, D. M.; Shulman, N.; Chambers, M.; Finney, G. L.; Frewen, B.; Kern, R.; Tabb, D. L.; Liebler, D. C.; MacCoss, M. J. Skyline: an open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics , 26 (7), 966-8.
58. Zeger, S. L.; Liang, K. Y. Longitudinal data analysis for discrete and continuous outcomes. Biometrics 1986, 42 (1), 121-30.
59. Gandhi, J.; Zhang, J.; Xie, Y.; Soh, J.; Shigematsu, H.; Zhang, W.; Yamamoto, H.; Peyton, M.; Girard, L.; Lockwood, W. W.; Lam, W. L.; Varella-Garcia, M.; Minna, J. D.; Gazdar, A. F. Alterations in genes of the EGFR signaling pathway and their relationship to EGFR tyrosine kinase inhibitor sensitivity in lung cancer cell lines. PLoS One 2009, 4 (2), e4576.
60. Gotoh, N.; Tojo, A.; Muroya, K.; Hashimoto, Y.; Hattori, S.; Nakamura, S.; Takenawa, T.; Yazaki, Y.; Shibuya, M. Epidermal growth factor-receptor mutant lacking the autophosphorylation sites induces phosphorylation of Shc protein and Shc-Grb2/ASH association and retains mitogenic activity. Proc. Natl. Acad. Sci. U.S.A. 1994, 91 (1), 167-71. (Pubitemid 24018664)
61. Sorkin, A.; Helin, K.; Waters, C. M.; Carpenter, G.; Beguinot, L. Multiple autophosphorylation sites of the epidermal growth factor receptor are essential for receptor kinase activity and internalization. Contrasting significance of tyrosine 992 in the native and truncated receptors. J. Biol. Chem. 1992, 267 (12), 8672-8.
62. Sorkin, A.; Waters, C.; Overholser, K. A.; Carpenter, G. Multiple autophosphorylation site mutations of the epidermal growth factor receptor. Analysis of kinase activity and endocytosis. J. Biol. Chem. 1991, 266 (13), 8355-62. (Pubitemid 21906518)
63. Hsu, C. Y.; Hurwitz, D. R.; Mervic, M.; Zilberstein, A. Autophosphorylation of the intracellular domain of the epidermal growth factor receptor results in different effects on its tyrosine kinase activity with various peptide substrates. Phosphorylation of peptides representing Tyr(P) sites of phospholipase C-gamma. J. Biol. Chem. 1991, 266 (1), 603-8. (Pubitemid 21906164)
64. Margolis, B. L.; Lax, I.; Kris, R.; Dombalagian, M.; Honegger, A. M.; Howk, R.; Givol, D.; Ullrich, A.; Schlessinger, J. All autophosphorylation sites of epidermal growth factor (EGF) receptor and HER2/ neu are located in their carboxyl-terminal tails. Identification of a novel site in EGF receptor. J. Biol. Chem. 1989, 264 (18), 10667-71. (Pubitemid 19161640)
65. Gates, R. E.; King, L. E., Jr. Different forms of the epidermal growth factor receptor kinase have different autophosphorylation sites. Biochemistry 1985, 24 (19), 5209-15. (Pubitemid 15242628)
66. Downward, J.; Parker, P.; Waterfield, M. D. Autophosphorylation sites on the epidermal growth factor receptor. Nature 1984, 311 (5985), 483-5. (Pubitemid 14035459)
67. Countaway, J. L.; Northwood, I. C.; Davis, R. J. Mechanism of phosphorylation of the epidermal growth factor receptor at threonine 669. J. Biol. Chem. 1989, 264 (18), 10828-35. (Pubitemid 19161657)
68. Saito, T.; Okada, S.; Ohshima, K.; Yamada, E.; Sato, M.; Uehara, Y.; Shimizu, H.; Pessin, J. E.; Mori, M. Differential activation of epidermal growth factor (EGF) receptor downstream signaling pathways by betacellulin and EGF. Endocrinology 2004, 145 (9), 4232-43. (Pubitemid 39120572)
69. Zhang, Y.; Yan, Z.; Farooq, A.; Liu, X.; Lu, C.; Zhou, M. M.; He, C. Molecular basis of distinct interactions between Dok1 PTB domain and tyrosine-phosphorylated EGF receptor. J. Mol. Biol. 2004, 343 (4), 1147-55. (Pubitemid 39345970)
70. Jiang, X.; Huang, F.; Marusyk, A.; Sorkin, A. Grb2 regulates internalization of EGF receptors through clathrin-coated pits. Mol. Biol. Cell 2003, 14 (3), 858-70. (Pubitemid 36337438)
71. Hirsch, F. R.; Varella-Garcia, M.; Cappuzzo, F. Predictive value of EGFR and HER2 overexpression in advanced non-small-cell lung cancer. Oncogene 2009, 28 (Suppl 1), S32-7.
72. Erlotinib in Lung Cancer. N. Engl. J. Med. 2005, 353, (16), 3.
73. Tsao, M. S.; Sakurada, A.; Cutz, J. C.; Zhu, C. Q.; Kamel-Reid, S.; Squire, J.; Lorimer, I.; Zhang, T.; Liu, N.; Daneshmand, M.; Marrano, P.; da Cunha Santos, G.; Lagarde, A.; Richardson, F.; Seymour, L.; Whitehead, M.; Ding, K.; Pater, J.; Shepherd, F. A. Erlotinib in lung cancer - molecular and clinical predictors of outcome. N. Engl. J. Med. 2005, 353 (2), 133-44. (Pubitemid 41058345)
74. Wolf-Yadlin, A.; Hautaniemi, S.; Lauffenburger, D. A.; White, F. M. Multiple reaction monitoring for robust quantitative proteomicanalysis of cellular signaling networks. Proc. Natl. Acad. Sci. U.S.A. 2007, 104 (14), 5860-5. (Pubitemid 47175624)
75. Tworoger, S. S.; Spentzos, D.; Grall, F. T.; Liebermann, T. A.; Hankinson, S. E. Reproducibility of proteomic profiles over 3 years in postmenopausal women not taking postmenopausal hormones. Cancer Epidemiol. Biomarkers Prev. 2008, 17 (6), 1480-5.
76. 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. , 9 (5), 2752-61.