Conservation of protein abundance patterns reveals the regulatory architecture of the EGFR-MAPK pathway

Science Signaling

Volumn 9, Issue 436, 2016, Pages

  Shi, Tujin ^a   Niepel, Mario ^b   McDermott, Jason E ^a   Gao, Yuqian ^a   Nicora, Carrie D ^a   Chrisler, William B ^a   Markillie, Lye M ^c   Petyuk, Vladislav A ^a   Smith, Richard D ^a,c   Rodland, Karin D ^a   Sorger, Peter K ^b   Qian, Wei Jun ^a   Wiley, H Steven ^c  

^a PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; CORE PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; GAB1 PROTEIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; SOS PROTEIN; SOS2 PROTEIN; UNCLASSIFIED DRUG; EGFR PROTEIN, HUMAN; MITOGEN ACTIVATED PROTEIN KINASE KINASE; TUMOR PROTEIN;

ARTICLE; BREAST CANCER CELL LINE; BREAST EPITHELIUM CELL; CELL SPECIFICITY; CELL SURFACE; CONTROLLED STUDY; ENDOCYTOSIS; FEEDBACK SYSTEM; FIBROBLAST; HUMAN; HUMAN CELL; MITOGENICITY; OBSERVATIONAL STUDY; PRIORITY JOURNAL; PROTEOMICS; RNA SEQUENCE; SIGNAL TRANSDUCTION; STOICHIOMETRY; BREAST TUMOR; FEMALE; GENETICS; MAPK SIGNALING; METABOLISM; TUMOR CELL LINE;

BREAST NEOPLASMS; CELL LINE, TUMOR; FEMALE; HUMANS; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; NEOPLASM PROTEINS; RECEPTOR, EPIDERMAL GROWTH FACTOR;

EID: 84978818649     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.aaf0891     Document Type: Article

References (84)

1. D. Hanahan, R. A. Weinberg, Hallmarks of cancer: The next generation. Cell 144, 646-674 (2011).
2. L. Zhao, T. Sun, J. Pei, Q. Ouyang, Mutation-induced protein interaction kinetics changes affect apoptotic network dynamic properties and facilitate oncogenesis. Proc. Natl. Acad. Sci. U.S.A. 112, E4046-E4054 (2015).
3. F. B. L. Hogervorst, P. M. Nederlof, J. J. P. Gille, C. J. McElgunn, M. Grippeling, R. Pruntel, R. Regnerus, T. van Welsem, R. van Spaendonk, F. H. Menko, I. Kluijt, C. Dommering, S. Verhoef, J. P. Schouten, L. J. van't Veer, G. Pals, Large genomic deletions and duplications in the BRCA1 gene identified by a novel quantitative method. Cancer Res. 63, 1449-1453 (2003).
4. I. Nobeli, A. D. Favia, J. M. Thornton, Protein promiscuity and its implications for biotechnology. Nat. Biotechnol. 27, 157-167 (2009).
5. R. Worthylake, L. K. Opresko, H. S. Wiley, ErbB-2 amplification inhibits down-regulation and induces constitutive activation of both ErbB-2 and epidermal growth factor receptors. J. Biol. Chem. 274, 8865-8874 (1999).
6. D. J. Klinke II, Signal transduction networks in cancer: Quantitative parameters influence network topology. Cancer Res. 70, 1773-1782 (2010).
7. R. Meyer, L A. D'Alessandro, S. Kar, B. Kramer, B. She, D. Kaschek, B. Hahn, D. Wrangborg, J. Karlsson, M. Kvarnström, M. Jirstrand, W.-D. Lehmann, J. Timmer, T. Höfer, U. Klingmüller, Heterogeneous kinetics of AKT signaling in individual cells are accounted for by variable protein concentration. Front Physiol. 3, 451 (2012).
8. E. C. Stites, M. Aziz, M. S. Creamer, D. D. Von Hoff, R. G. Posner, W. S. Hlavacek, Use of mechanistic models to integrate and analyze multiple proteomic datasets. Biophys. J. 108, 1819-1829 (2015).
9. E. H. Wilkes, C. Terfve, J. G. Gribben, J. Saez-Rodriguez, P. R. Cutillas, Empirical inference of circuitry and plasticity in a kinase signaling network. Proc. Natl. Acad. Sci. U.S.A. 112, 7719-7724 (2015).
10. M. H. Kraus, N. C. Popescu, S. C. Amsbaugh, C. R. King, Overexpression of the EGF receptor-related proto-oncogene erbB-2 in human mammary tumor cell lines by different molecular mechanisms. EMBO J. 6, 605-610 (1987).
11. T. A. Libermann, H. R. Nusbaum, N. Razon, R. Kris, I. Lax, H. Soreq, N. Whittle, M. D. Waterfield, A Ullrich, J. Schlessinger, Amplification, enhanced expression and possible rearrangement of EGF receptor gene in primary human brain tumours of glial origin. Nature 313, 144-147 (1985).
12. T. Maier, M. Güell, L. Serrano, Correlation of mRNAand protein in complex biological samples. FEBS Lett. 583, 3966-3973 (2009).
13. N. Nagaraj, J. R. Wisniewski, T. Geiger, J. Cox, M. Kircher, J. Kelso, S. Pääbo, M. Mann, Deep proteome and transcriptome mapping of a human cancer cell line. Mol. Syst. Biol. 7, 548 (2011).
14. R. T. Lawrence, E. M. Perez, D. Hernández, C. P. Miller, K. M. Haas, H. Y. Irie, S.-I. Lee, C. A. Blau, J. Villén, The proteomic landscape of triple-negative breast cancer. Cell Rep. 11, 630-644 (2015).
15. J. Li, Y. Lu, R. Akbani, Z. Ju, P. L Roebuck, W. Liu, J.-Y Yang, B. M. Broom, R. G. W. Verhaak, D. W. Kane, C. Wakefield, J. N. Weinstein, G. B. Mills, H. Liang, TCPA: A resource for cancer functional proteomics data. Nat Methods 10, 1046-1047 (2013).
16. P. J. Roberts, C. J. Der, Targeting the Raf-MEK-ERK mitogen-activated protein kinase cascade for the treatment of cancer. Oncogene 26, 3291-3310 (2007).
17. A. Citri, Y. Yarden, EGF-ERBB signalling: Towards the systems level. Nat. Rev. Mol. Cell Biol. 7, 505-516 (2006).
18. R. I. Nicholson, J. M. W. Gee, M. E. Harper, EGFR and cancer prognosis. Eur. J. Cancer 37 (Suppl. 4), S9-S15 (2001).
19. D. J. Slamon, G. M. Clark, S. G. Wong, W. J. Levin, A. Ullrich, W. L. McGuire, Human breast cancer: Correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 235, 177-182 (1987).
20. W. Pao, J. Chmielecki, Rational, biologically based treatment of EGFR-mutant non-small cell lung cancer. Nat. Rev. Cancer 10, 760-774 (2010).
21. X. Qian, L Esteban, W. C. Vass, C. Upadhyaya, A. G. Papageorge, K. Yienger, J. M. Ward, D. R. Lowy, E. Santos, The Sos1 and Sos2 Ras-specific exchange factors: Differences in placental expression and signaling properties. EMBO J. 19, 642-654 (2000).
22. S.-s. Yang, L. Van Aelst, D. Bar-Sagi, Differential interactions of human Sos1 and Sos2 with Grb2. J. Biol. Chem. 270, 18212-18215 (1995).
23. S. Anastasi, M. F. Baietti, Y. Frosi, S. Alemà, O. Segatto, The evolutionary conserved EBR module of RALT/MIG6 mediates suppression of the EGFR catalytic activity. Oncogene 26, 7833-7846 (2007).
24. M. G. Mohi, B. G. Neel, The role of Shp2 (PTPN11) in cancer. Curr. Opin. Genet. Dev. 17, 23-30 (2007).
25. R. Aebersold, A. L. Burlingame, R. A. Bradshaw, Western blots versus selected reaction monitoring assays: Time to turn the tables? Mol. Cell. Proteomics 12, 2381-2382 (2013).
26. M. Gassmann, B. Grenacher, B. Rohde, J. Vogel, Quantifying Western blots: Pitfalls of densitometry. Electrophoresis 30, 1845-1855 (2009).
27. S. Y. Ow, M. Salim, J. Noirel, C. Evans, I. Rehman, P. C. Wright, iTRAQ underestimation in simple and complex mixtures: "The good, the bad and the ugly". J. Proteome Res. 8, 5347-5355 (2009).
28. F. Xie, T. Liu, W.-J. Qian, V. A. Petyuk, R. D. Smith, Liquid chromatography-mass spectrometry-based quantitative proteomics. J. Biol. Chem. 286, 25443-25449 (2011).
29. T. Shi, D. Su, T. Liu, K. Tang, D. G. Camp II, W.-J. Qian, R. D. Smith, Advancing the sensitivity of selected reaction monito ring-based targeted quantitative proteomics. Proteomics 12, 1074-1092 (2012).
30. J. Dong, L. K. Opresko, P. J. Dempsey, D. A. Lauffenburger, R. J. Coffey, H. S. Wiley, Metalloprotease-mediated ligand release regulates autocrine signaling through the epidermal growth factor receptor. Proc. Natl. Acad. Sci. U.S.A. 96, 6235-6240 (1999).
31. M. R. Stampfer, C. H. Pan, J. Hosoda, J. Bartholomew, J. Mendelsohn, P. Yaswen, Blockage of EGF receptor signal transduction causes reversible arrest of normal and immortal human mammary epithelial cells with synchronous reentry into the cell cycle. Exp. Cell Res. 208, 175-188 (1993).
32. D. C. Kirouac, J. Saez-Rodriguez, J. Swantek, J. M. Burke, D. A. Lauffenburger, P. K. Sorger, Creating and analyzing pathway and protein interaction compendia for modelling signal transduction networks. BMC Syst. Biol. 6, 29 (2012).
33. J. M. Jacobs, H. M. Mottaz, L R. Yu, D. J. Anderson, R. J. Moore, W. N. U. Chen, K. J. Auberry, E. F. Strittmatter, M. E. Monroe, B. D. Thrall, D. G. Camp II, R. D. Smith, Multidimensional proteome analysis of human mammary epithelial cells. J. Proteome Res. 3, 68-75 (2004).
34. K. M. Waters, T. Liu, R. D. Quesenberry, A. R. Willse, S. Bandyopadhyay, L E. Kathmann, T. J. Weber, R. D. Smith, H. S. Wiley, B. D. Thrall, Network analysis of epidermal growth factor signaling using integrated genomic, proteomic and phosphorylation data. PLOS One 7, e34515 (2012).
35. A. Wolf-Yadlin, S. Hautaniemi, D. A. Lauffenburger, F. M. White, Multiple reaction monitoring for robust quantitative proteomic analysis of cellular signaling networks. Proc. Natl. Acad. Sci. U.S.A. 104, 5860-5865 (2007).
36. Y. Zheng, C. Zhang, D. R. Croucher, M. A. Soliman, N. St-Denis, A. Pasculescu, L Taylor, S. A. Tate, W. R. Hardy, K. Colwill, A. Y. Dai, R. Bagshaw, J. W. Dennis, A.-C. Gingras, R. J. Daly, T. Pawson, Temporal regulation of EGF signalling networks by the scaffold protein Shc1. Nature 499, 166-171 (2013).
37. A. Montagner, A. Yart, M. Dance, B. Perret, J.-P. Salles, P. Raynal, A novel role for Gab1 and SHP2 in epidermal growth factor-induced Ras activation. J. Biol. Chem. 280, 5350-5360 (2005).
38. N. Borisov, E. Aksamitiene, A Kiyatkin, S. Legewie, J. Berkhout, T. Maiwald, N. P. Kaimachnikov, J. Timmer, J. B. Hoek, B. N. Kholodenko, Systems-level interactions between insulin-EGF networks amplify mitogenic signaling. Mol. Syst. Biol. 5, 256 (2009).
39. C. Kiel, H. A. Ebhardt, J. Burnier, C. Portugal, E. Sabidó, T. Zimmermann, R. Aebersold, L. Serrano, Quantification of ErbB network proteins in three cell types using complementary approaches identifies cell-general and cell-type-specific signaling proteins. J. Proteome Res. 13, 300-313 (2014).
40. C.-C. Wang, M. Cirit, J. M. Haugh, PI3K-dependent cross-talk interactions converge with Ras as quantifiable inputs integrated by Erk. Mol. Syst. Biol. 5, 246 (2009).
41. K. D. Rodland, N. Bollinger, D. Ippolito, L K. Opresko, R. J. Coffey, R. Zangar, H. S. Wiley, Multiple mechanisms are responsible for transactivation of the epidermal growth factor receptor in mammary epithelial cells. J. Biol. Chem. 283, 31477-31487 (2008).
42. E. J. Joslin, H. Shankaran, L K. Opresko, N. Bollinger, D. A. Lauffenburger, H. S. Wiley, Structure of the EGF receptor transactivation circuit integrates multiple signals with cell context. Mol. Biosyst. 6, 1293-1306 (2010).
43. M. Gensler, M. Buschbeck, A. Ullrich, Negative regulation of HER2 signaling by the PEST type protein-tyrosine phosphatase BDP1. J. Biol. Chem. 279, 12110-12116 (2004).
44. S. Legewie, H. Herzel, H. V. Westerhoff, N. Blüthgen, Recurrent design patterns in the feedback regulation of the mammalian signalling network. Mol. Syst. Biol. 4, 190 (2008).
45. H. Liu, R. G. Sadygov, J. R. Yates III, A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal. Chem. 76, 4193-4201 (2004).
46. C. Vogel, E. M. Marcotte, Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nat. Rev. Genet. 13, 227-232 (2012).
47. T. Geiger, A. Wehner, C. Schaab, J. Cox, M. Mann, Comparative proteomic analysis of eleven common cell lines reveals ubiquitous but varying expression of most proteins. Mol. Cell. Proteomics 11, M111 014050 (2012).
48. Z. Khan, M. J. Ford, D. A. Cusanovich, A. Mitrano, J. K. Pritchard, Y. Gilad, Primate transcript and protein expression levels evolve under compensatory selection pressures. Science 342, 1100-1104 (2013).
49. P. L Ross, Y. N. Huang, J. N. Marchese, B. Williamson, K. Parker, S. Hattan, N. Khainovski, S. Pillai, S. Dey, S. Daniels, S. Purkayastha, P. Juhasz, S. Martin, M. Bartlet-Jones, F. He, A. Jacobson, D. J. Pappin, Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol. Cell. Proteomics 3, 1154-1169 (2004).
50. P. P. Łabaj, G. G. Leparc, B. E. Linggi, L. M. Markillie, H. S. Wiley, D. P. Kreil, Characterization and improvement of RNA-Seq precision in quantitative transcript expression profiling. Bioinformatics 27, i383-i391 (2011).
51. R. C. Taylor, B.-J. Webb Robertson, L M. Markillie, M. H. Serres, B. E. Linggi, J. T. Aldrich, E. A. Hill, M. F. Romine, M. S. Lipton, H. S. Wiley, Changes in translational efficiency is a dominant regulatory mechanism in the environmental response of bacteria. Integr. Biol. 5, 1393-1406 (2013).
52. T. Shi, T. L. Fillmore, X. Sun, R. Zhao, A. A. Schepmoes, M. Hossain, F. Xie, S. Wu, J.-S. Kim, N. Jones, R. J. Moore, L Paša-Tolić, J. Kagan, K. D. Rodland, T. Liu, K. Tang, D. G. Camp II, R. D. Smith, W.-J. Qian, Antibody-free, targeted mass-spectrometric approach for quantification of proteins at low picogram per milliliter levels in human plasma/serum. Proc. Natl. Acad. Sci. U.S.A. 109, 15395-15400 (2012).
53. C.-Y. Huang, T.-H. Tan, DUSPs, to MAP kinases and beyond. Cell Biosci. 2, 24 (2012).
54. D. J. Knauer, H. S. Wiley, D. D. Cunningham, Relationship between epidermal growth factor receptor occupancy and mitogenic response. J. Biol. Chem. 259, 5623-5631 (1984).
55. T. Shi, Y. Gao, M. J. Gaffrey, C. D. Nicora, T. L. Fillmore, W. B. Chrisler, M. A. Gritsenko, C. Wu, J. He, K. J. Bloodsworth, R. Zhao, D. G. Camp II, T. Liu, K. D. Rodland, R. D. Smith, H. S. Wiley, W.-J. Qian, Sensitive targeted quantification of ERK phosphorylation dynamics and stoichiometry in human cells without affinity enrichment. Anal. Chem. 87, 1103-1110 (2015).
56. S. C. Kozma, M. E. Bogaard, K. Buser, S. M. Saurer, J. L. Bos, B. Groner, N. E. Hynes, The human c-Kirsten ras gene is activated by a novel mutation in codon 13 in the breast carcinoma cell line MDA-MB231. Nucleic Acids Res. 15, 5963-5971 (1987).
57. Y. J. Kim, P. Zhan, B. Feild, S. M. Ruben, T. He, Reproducibility assessment of relative quantitation strategies for LC-MS based proteomics. Anal. Chem. 79, 5651-5658 (2007).
58. B. Schwänhausser, D. Busse, N. Li, G. Dittmar, J. Schuchhardt, J. Wolf, W. Chen, M. Selbach, Global quantification of mammalian gene expression control. Nature 473, 337-342 (2011).
59. ras through the formation of a complex of receptor, Grb2 adapter protein, and Sos nucleotide exchange factor. Cell 73, 611-620 (1993).
60. W. W. Lockwood, R. Chari, B. P. Coe, L. Girard, C. MacAulay, S. Lam, A. F. Gazdar, J. D. Minna, W. L. Lam, DNA amplification is a ubiquitous mechanism of oncogene activation in lung and other cancers. Oncogene 27, 4615-4624 (2008).
61. R. J. Daly, M. D. Binder, R. L. Sutherland, Overexpression of the Grb2 gene in human breast cancer cell lines. Oncogene 9, 2723-2727 (1994).
62. T. Kobayashi, Y. Aoki, T. Niihori, H. Cavé, A. Verloes, N. Okamoto, H. Kawame, I. Fujiwara, F. Takada, T. Ohata, S. Sakazume, T. Ando, N. Nakagawa, P. Lapunzina, A. G. Meneses, G. Gillessen-Kaesbach, D. Wieczorek, K. Kurosawa, S. Mizuno, H. Ohashi, A. David, N. Philip, A. Guliyeva, Y. Narumi, S. Kure, S. Tsuchiya, Y. Matsubara, Molecular and clinical analysis of RAF1 in Noonan syndrome and related disorders: Dephosphorylation of serine 259 as the essential mechanism for mutant activation. Hum. Mutat. 31, 284-294 (2010).
63. A. E. Roberts, T. Araki, K. D. Swanson, K. T. Montgomery, T. A. Schiripo, V. A. Joshi, L. Li, Y. Yassin, A. M. Tamburino, B. G. Neel, R. S. Kucherlapati, Germline gain-of function mutations in SOS1 cause Noonan syndrome. Nat. Genet. 39, 70-74 (2007).
64. M. K. Gilson, J. A. Given, B. L. Bush, J. A. McCammon, The statistical-thermodynamic basis for computation of binding affinities: A critical review. Biophys. J. 72, 1047-1069 (1997).
65. P. M. Burke, H. S. Wiley, Human mammary epithelial cells rapidly exchange empty EGFR between surface and intracellular pools. J. Cell. Physiol. 180, 448-460 (1999).
66. L. K. Goh, F. Huang, W. Kim, S. Gygi, A. Sorkin, Multiple mechanisms collectively regulate clathrin-mediated endocytosis of the epidermal growth factor receptor. J. Cell Biol. 189, 871-883 (2010).
67. K. A. Lund, L. K. Opresko, C. Starbuck, B. J. Walsh, H. S. Wiley, Quantitative analysis of the endocytic system involved in hormone-induced receptor internalization. J. Biol. Chem. 265, 15713-15723 (1990).
68. J. A. Krall, E. M. Beyer, G. MacBeath, High-and low-affinity epidermal growth factor receptor-ligand interactions activate distinct signaling pathways. PLOS One 6, e15945 (2011).
69. B. Schoeberl, C. Eichler-Jonsson, E. D. Gilles, G. Müller, Computational modeling of the dynamics of the MAP kinase cascade activated by surface and internalized EGF receptors. Nat. Biotechnol. 20, 370-375 (2002).
70. A. Gordus, J. A. Krall, E. M. Beyer, A. Kaushansky, A. Wolf-Yadlin, M. Sevecka, B. H. Chang, J. Rush, G. MacBeath, Linear combinations of docking affinities explain quantitative differences in RTK signaling. Mol. Syst. Biol. 5, 235 (2009).
71. S. O. Meakin, J. I. S. MacDonald, E. A. Gryz, C. J. Kubu, J. M. Verdi, The signaling adapter FRS-2 competes with Shc for binding to the nerve growth factor receptor TrkA. A model for discriminating proliferation and differentiation. J. Biol. Chem. 274, 9861-9870 (1999).
72. T. J. Wilson, L. I. Garner, C. Metcalfe, E. King, S. Margraf, M. H. Brown, Fine specificity and molecular competition in SLAM family receptor signalling. PLOS One 9, e92184 (2014).
73. M. Niepel, M. Hafner, E. A. Pace, M. Chung, D. H. Chai, L. Zhou, B. Schoeberl, P. K. Sorger, Profiles of basal and stimulated receptor signaling networks predict drug response in breast cancer lines. Sci. Signal. 6, ra84 (2013).
74. V. Band, R. Sager, Distinctive traits of normal and tumor-derived human mammary epithelial cells expressed in a medium that supports long-term growth of both cell types. Proc. Natl. Acad. Sci. U.S.A. 86, 1249-1253 (1989).
75. R. D. Smith, G. A. Anderson, M. S. Lipton, L. Pasa-Tolic, Y. Shen, T. P. Conrads, T. D. Veenstra, H. R. Udseth, An accurate mass tag strategy for quantitative and high throughput proteome measurements. Proteomics 2, 513-523 (2002).
76. W.-N. U. Chen, L.-R. Yu, E. F. Strittmater, B. D. Thrall, D. G. Camp II, R. D. Smith, Detection of in situ labeled cell surface proteins by mass spectrometry: Application to the membrane subproteome of human mammary epithelial cells. Proteomics 3, 1647-1651 (2003).
77. T. Liu, W.-J. Qian, E. F. Strittmater, D. G. Camp II, G. A. Anderson, B. D. Thrall, R. D. Smith, High-throughput comparative proteome analysis using a quantitative cysteinyl-peptide enrichment technology. Anal. Chem. 76, 5345-5353 (2004).
78. T. Liu, W.-J. Qian, W.-N. U. Chen, J. M. Jacobs, R. J. Moore, D. J. Anderson, M. A. Gritsenko, M. E. Monroe, B. D. Thrall, D. G. I. Camp, R. D. Smith, Improved proteome coverage by using high efficiency cysteinyl peptide enrichment: The human mammary epithelial cell proteome. Proteomics 5, 1263-1273 (2005).
79. A. D. Polpitiya, W.-J. Qian, N. Jaitly, V. A. Petyuk, J. N. Adkins, D. G. Camp II, G. A. Anderson, R. D. Smith, DAnTE: A statistical tool for quantitative analysis of-omics data. Bioinformatics 24, 1556-1558 (2008).
80. T. Shi, T. L. Fillmore, Y. Gao, R. Zhao, J. He, A. A. Schepmoes, C. D. Nicora, C. Wu, J. L. Chambers, R. J. Moore, J. Kagan, S. Srivastava, A. Y. Liu, K. D. Rodland, T. Liu, D. G. Camp II, R. D. Smith, W.-J. Qian, Long-gradient separations coupled with selected reaction monitoring for highly sensitive, large scale targeted protein quantification in a single analysis. Anal. Chem. 85, 9196-9203 (2013).
81. B. MacLean, D. M. Tomazela, N. Shulman, M. Chambers, G. L. Finney, B. Frewen, R. Kern, D. L. Tabb, D. C. Liebler, M. J. MacCoss, Skyline: An open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics 26, 966-968 (2010).
82. A. E. DeWitt, J. Y. Dong, H. S. Wiley, D. A. Lauffenburger, Quantitative analysis of the EGF receptor autocrine system reveals cryptic regulation of cell response by ligand capture. J. Cell Sci. 114, 2301-2313 (2001).
83. P. Shannon, A. Markiel, O. Ozier, N. S. Baliga, J. T. Wang, D. Ramage, N. Amin, B. Schwikowski, T. Ideker, Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498-2504 (2003).
84. N. Rauniyar, J. R. Yates III, Isobaric labeling-based relative quantification in shotgun proteomics. J. Proteome Res. 13, 5293-5309 (2014).