Biomarker discovery and verification of esophageal squamous cell carcinoma using integration of SWATH/MRM

Journal of Proteome Research

Volumn 14, Issue 9, 2015, Pages 3793-3803

  Hou, Guixue ^a,b,c   Lou, Xiaomin ^a   Sun, Yulin ^d   Xu, Shaohang ^c   Zi, Jin ^c   Wang, Quanhui ^a,c   Zhou, Baojin ^c   Han, Bo ^d   Wu, Lin ^a   Zhao, Xiaohang ^d   Lin, Liang ^c   Liu, Siqi ^a,c  

^a Chinese Academy of Sciences   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c BGI SHENZHEN   (China)

^d CANCER HOSPITAL   (China)

Author keywords

biomarker; ESCC; MRM; SWATH

Indexed keywords

PROTEIN; TUMOR MARKER; TUMOR PROTEIN;

ARTICLE; CHEMICAL PROCEDURES; CONTROLLED STUDY; ESOPHAGEAL SQUAMOUS CELL CARCINOMA; ESOPHAGEAL TISSUE; HUMAN; HUMAN TISSUE; INFORMATION PROCESSING; MASS SPECTROMETRY; MULTIPLE REACTION MONITORING; PRIORITY JOURNAL; PROTEIN ANALYSIS; SEQUENTIAL WINDOW ACQUISITION OF ALL THEORETICAL SPECTRA; UPREGULATION; ESOPHAGUS TUMOR; METABOLISM; PROTEOMICS; SQUAMOUS CELL CARCINOMA;

BIOMARKERS, TUMOR; CARCINOMA, SQUAMOUS CELL; ESOPHAGEAL NEOPLASMS; HUMANS; NEOPLASM PROTEINS; PROTEOMICS;

EID: 84941061556     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/acs.jproteome.5b00438     Document Type: Article

References (44)

1. Gillet, L. C.; Navarro, P.; Tate, S.; Rost, H.; Selevsek, N.; Reiter, L.; Bonner, R.; Aebersold, R. Targeted data extraction of the MS/MS spectra generated by data-independent acquisition: a new concept for consistent and accurate proteome analysis Mol. Cell. Proteomics 2012, 11, O111 016717 10.1074/mcp.O111.016717
2. Liu, Y.; Huttenhain, R.; Surinova, S.; Gillet, L. C.; Mouritsen, J.; Brunner, R.; Navarro, P.; Aebersold, R. Quantitative measurements of N-linked glycoproteins in human plasma by SWATH-MS Proteomics 2013, 13, 1247-56 10.1002/pmic.201200417
3. Collins, B. C.; Gillet, L. C.; Rosenberger, G.; Rost, H. L.; Vichalkovski, A.; Gstaiger, M.; Aebersold, R. Quantifying protein interaction dynamics by SWATH mass spectrometry: application to the 14-3-3 system Nat. Methods 2013, 10, 1246-53 10.1038/nmeth.2703
4. Haverland, N. A.; Fox, H. S.; Ciborowski, P. Quantitative proteomics by SWATH-MS reveals altered expression of nucleic acid binding and regulatory proteins in HIV-1-infected macrophages J. Proteome Res. 2014, 13, 2109-19 10.1021/pr4012602
5. George, R.; Ching, C. K.; Guo, T.; Hannes, L. R.; Petri, K.; Collins, B. C.; Moritz, H.; Liu, Y.; Etienne, C.; Anton, V.; Marco, F.; Olga, T. S.; Pouya, F.; H, A. E.; Mariette, M.; Henry, L.; Samuel, L. B.; David, S. C.; Eric, W. D.; Robert, L. M.; Tate, Stephen; Aebersold, R. A repository of assays to quantify 10,000 human proteins by SWATH-MS Sci. Data 2014, 1, 140031 10.1038/sdata.2014.31
6. Pawar, H.; Kashyap, M. K.; Sahasrabuddhe, N. A.; Renuse, S.; Harsha, H. C.; Kumar, P.; Sharma, J.; Kandasamy, K.; Marimuthu, A.; Nair, B.; Rajagopalan, S.; Maharudraiah, J.; Premalatha, C. S.; Kumar, K. V.; Vijayakumar, M.; Chaerkady, R.; Prasad, T. S.; Kumar, R. V.; Kumar, R. V.; Pandey, A. Quantitative tissue proteomics of esophageal squamous cell carcinoma for novel biomarker discovery Cancer Biol. Ther. 2011, 12, 510-22 10.4161/cbt.12.6.16833
7. Zhang, J.; Wang, K.; Zhang, J.; Liu, S. S.; Dai, L.; Zhang, J. Y. Using proteomic approach to identify tumor-associated proteins as biomarkers in human esophageal squamous cell carcinoma J. Proteome Res. 2011, 10, 2863-72 10.1021/pr200141c
8. Abbatiello, S. E.; Mani, D. R.; Schilling, B.; Maclean, B.; Zimmerman, L. J.; Feng, X.; Cusack, M. P.; Sedransk, N.; Hall, S. C.; Addona, T.; Allen, S.; Dodder, N. G.; Ghosh, M.; Held, J. M.; Hedrick, V.; Inerowicz, H. D.; Jackson, A.; Keshishian, H.; Kim, J. W.; Lyssand, J. S.; Riley, C. P.; Rudnick, P.; Sadowski, P.; Shaddox, K.; Smith, D.; Tomazela, D.; Wahlander, A.; Waldemarson, S.; Whitwell, C. A.; You, J.; Zhang, S.; Kinsinger, C. R.; Mesri, M.; Rodriguez, H.; Borchers, C. H.; Buck, C.; Fisher, S. J.; Gibson, B. W.; Liebler, D.; Maccoss, M.; Neubert, T. A.; Paulovich, A.; Regnier, F.; Skates, S. J.; Tempst, P.; Wang, M.; Carr, S. A. Design, implementation and multisite evaluation of a system suitability protocol for the quantitative assessment of instrument performance in liquid chromatography-multiple reaction monitoring-MS (LC-MRM-MS) Mol. Cell. Proteomics 2013, 12, 2623-39 10.1074/mcp.M112.027078
9. Addona, T. A.; Abbatiello, S. E.; Schilling, B.; Skates, S. J.; Mani, D. R.; Bunk, D. M.; Spiegelman, C. H.; Zimmerman, L. J.; Ham, A. J.; Keshishian, H.; Hall, S. C.; Allen, S.; Blackman, R. K.; Borchers, C. H.; Buck, C.; Cardasis, H. L.; Cusack, M. P.; Dodder, N. G.; Gibson, B. W.; Held, J. M.; Hiltke, T.; Jackson, A.; Johansen, E. B.; Kinsinger, C. R.; Li, J.; Mesri, M.; Neubert, T. A.; Niles, R. K.; Pulsipher, T. C.; Ransohoff, D.; Rodriguez, H.; Rudnick, P. A.; Smith, D.; Tabb, D. L.; Tegeler, T. J.; Variyath, A. M.; Vega-Montoto, L. J.; Wahlander, A.; Waldemarson, S.; Wang, M.; Whiteaker, J. R.; Zhao, L.; Anderson, N. L.; Fisher, S. J.; Liebler, D. C.; Paulovich, A. G.; Regnier, F. E.; Tempst, P.; Carr, S. A. Multi-site assessment of the precision and reproducibility of multiple reaction monitoring-based measurements of proteins in plasma Nat. Biotechnol. 2009, 27, 633-41 10.1038/nbt.1546
10. Mead, J. A.; Bianco, L.; Ottone, V.; Barton, C.; Kay, R. G.; Lilley, K. S.; Bond, N. J.; Bessant, C. MRMaid, the web-based tool for designing multiple reaction monitoring (MRM) transitions Mol. Cell. Proteomics 2009, 8, 696-705 10.1074/mcp.M800192-MCP200
11. Desiere, F.; Deutsch, E. W.; King, N. L.; Nesvizhskii, A. I.; Mallick, P.; Eng, J.; Chen, S.; Eddes, J.; Loevenich, S. N.; Aebersold, R. The PeptideAtlas project Nucleic Acids Res. 2006, 34, D655-8 10.1093/nar/gkj040
12. Anderson, L.; Hunter, C. L. Quantitative mass spectrometric multiple reaction monitoring assays for major plasma proteins Mol. Cell. Proteomics 2005, 5, 573-88 10.1074/mcp.M500331-MCP200
13. Huttenhain, R.; Soste, M.; Selevsek, N.; Rost, H.; Sethi, A.; Carapito, C.; Farrah, T.; Deutsch, E. W.; Kusebauch, U.; Moritz, R. L.; Nimeus-Malmstrom, E.; Rinner, O.; Aebersold, R. Reproducible quantification of cancer-associated proteins in body fluids using targeted proteomics Sci. Transl. Med. 2012, 4, 142ra94 10.1126/scitranslmed.3003989
14. Wisniewski, J. R.; Zougman, A.; Nagaraj, N.; Mann, M. Universal sample preparation method for proteome analysis Nat. Methods 2009, 6, 359-62 10.1038/nmeth.1322
15. Guerrier, L.; Righetti, P. G.; Boschetti, E. Reduction of dynamic protein concentration range of biological extracts for the discovery of low-abundance proteins by means of hexapeptide ligand library Nat. Protoc. 2008, 3, 883-90 10.1038/nprot.2008.59
16. 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 2010, 26, 966-8 10.1093/bioinformatics/btq054
17. Reiter, L.; Rinner, O.; Picotti, P.; Huttenhain, R.; Beck, M.; Brusniak, M. Y.; Hengartner, M. O.; Aebersold, R. mProphet: automated data processing and statistical validation for large-scale SRM experiments Nat. Methods 2011, 8, 430-5 10.1038/nmeth.1584
18. Rost, H. L.; Rosenberger, G.; Navarro, P.; Gillet, L.; Miladinovic, S. M.; Schubert, O. T.; Wolski, W.; Collins, B. C.; Malmstrom, J.; Malmstrom, L.; Aebersold, R. OpenSWATH enables automated, targeted analysis of data-independent acquisition MS data Nat. Biotechnol. 2014, 32, 219-23 10.1038/nbt.2841
19. Choi, M.; Chang, C. Y.; Clough, T.; Broudy, D.; Killeen, T.; MacLean, B.; Vitek, O. MSstats: an R package for statistical analysis of quantitative mass spectrometry-based proteomic experiments Bioinformatics 2014, 30, 2524-6 10.1093/bioinformatics/btu305
20. Fan, N. J.; Gao, C. F.; Wang, C. S.; Zhao, G.; Lv, J. J.; Wang, X. L.; Chu, G. H.; Yin, J.; Li, D. H.; Chen, X.; Yuan, X. T.; Meng, N. L. Identification of the up-regulation of TP-alpha, collagen alpha-1(VI) chain, and S100A9 in esophageal squamous cell carcinoma by a proteomic method J. Proteomics 2012, 75, 3977-86 10.1016/j.jprot.2012.05.008
21. Su, H.; Hu, N.; Yang, H. H.; Wang, C.; Takikita, M.; Wang, Q. H.; Giffen, C.; Clifford, R.; Hewitt, S. M.; Shou, J. Z.; Goldstein, A. M.; Lee, M. P.; Taylor, P. R. Global gene expression profiling and validation in esophageal squamous cell carcinoma and its association with clinical phenotypes Clin. Cancer Res. 2011, 17, 2955-66 10.1158/1078-0432.CCR-10-2724
22. Muthusamy, B.; Hanumanthu, G.; Suresh, S.; Rekha, B.; Srinivas, D.; Karthick, L.; Vrushabendra, B. M.; Sharma, S.; Mishra, G.; Chatterjee, P.; Mangala, K. S.; Shivashankar, H. N.; Chandrika, K. N.; Deshpande, N.; Suresh, M.; Kannabiran, N.; Niranjan, V.; Nalli, A.; Prasad, T. S.; Arun, K. S.; Reddy, R.; Chandran, S.; Jadhav, T.; Julie, D.; Mahesh, M.; John, S. L.; Palvankar, K.; Sudhir, D.; Bala, P.; Rashmi, N. S.; Vishnupriya, G.; Dhar, K.; Reshma, S.; Chaerkady, R.; Gandhi, T. K.; Harsha, H. C.; Mohan, S. S.; Deshpande, K. S.; Sarker, M.; Pandey, A. Plasma Proteome Database as a resource for proteomics research Proteomics 2005, 5, 3531-6 10.1002/pmic.200401335
23. Nanjappa, V.; Thomas, J. K.; Marimuthu, A.; Muthusamy, B.; Radhakrishnan, A.; Sharma, R.; Ahmad Khan, A.; Balakrishnan, L.; Sahasrabuddhe, N. A.; Kumar, S.; Jhaveri, B. N.; Sheth, K. V.; Kumar Khatana, R.; Shaw, P. G.; Srikanth, S. M.; Mathur, P. P.; Shankar, S.; Nagaraja, D.; Christopher, R.; Mathivanan, S.; Raju, R.; Sirdeshmukh, R.; Chatterjee, A.; Simpson, R. J.; Harsha, H. C.; Pandey, A.; Prasad, T. S. Plasma Proteome Database as a resource for proteomics research: 2014 update Nucleic Acids Res. 2014, 42, D959-65 10.1093/nar/gkt1251
24. Surinova, S.; Huttenhain, R.; Chang, C. Y.; Espona, L.; Vitek, O.; Aebersold, R. Automated selected reaction monitoring data analysis workflow for large-scale targeted proteomic studies Nat. Protoc. 2013, 8, 1602-19 10.1038/nprot.2013.091
25. Lange, V.; Picotti, P.; Domon, B.; Aebersold, R. Selected reaction monitoring for quantitative proteomics: a tutorial Mol. Syst. Biol. 2008, 4, 222 10.1038/msb.2008.61
26. Zhang, H. Q.; Wang, R. B.; Yan, H. J.; Zhao, W.; Zhu, K. L.; Jiang, S. M.; Hu, X. G.; Yu, J. M. Prognostic significance of CYFRA21-1, CEA and hemoglobin in patients with esophageal squamous cancer undergoing concurrent chemoradiotherapy Asian Pacific journal of cancer prevention: APJCP 2012, 13, 199-203 10.7314/APJCP.2012.13.1.199
27. Yi, Y.; Li, B.; Wang, Z.; Sun, H.; Gong, H.; Zhang, Z. CYFRA21-1 and CEA are useful markers for predicting the sensitivity to chemoradiotherapy of esophageal squamous cell carcinoma Biomarkers 2009, 14, 480-5 10.3109/13547500903180265
28. Li, Y.; Zhang, Q.; Peng, B.; Shao, Q.; Qian, W.; Zhang, J. Y. Identification of glutathione S-transferase omega 1 (GSTO1) protein as a novel tumor-associated antigen and its autoantibody in human esophageal squamous cell carcinoma Tumor Biol. 2014, 35, 10871 10.1007/s13277-014-2394-y
29. Chen, C.; Zhao, M.; Yin, N.; He, B.; Wang, B.; Yuan, Y.; Yu, F.; Hu, J.; Yin, B.; Lu, Q. Abnormal histone acetylation and methylation levels in esophageal squamous cell carcinomas Cancer Invest. 2011, 29, 548-56 10.3109/07357907.2011.597810
30. Zhang, J.; Zhi, H.; Zhou, C.; Ding, F.; Luo, A.; Zhang, X.; Sun, Y.; Wang, X.; Wu, M.; Liu, Z. Up-regulation of fibronectin in oesophageal squamous cell carcinoma is associated with activation of the Erk pathway J. Pathol. 2005, 207, 402-9 10.1002/path.1846
31. Zhou, Z. Q.; Cao, W. H.; Xie, J. J.; Lin, J.; Shen, Z. Y.; Zhang, Q. Y.; Shen, J. H.; Xu, L. Y.; Li, E. M. Expression and prognostic significance of THBS1, Cyr61 and CTGF in esophageal squamous cell carcinoma BMC Cancer 2009, 9, 291 10.1186/1471-2407-9-291
32. Selicharova, I.; Sanda, M.; Mladkova, J.; Ohri, S. S.; Vashishta, A.; Fusek, M.; Jiracek, J.; Vetvicka, V. 2-DE analysis of breast cancer cell lines 1833 and 4175 with distinct metastatic organ-specific potentials: comparison with parental cell line MDA-MB-231 Oncol. Rep. 2008, 19, 1237-44 10.3892/or.19.5.1237
33. Shajahan, A. N.; Timblin, B. K.; Sandoval, R.; Tiruppathi, C.; Malik, A. B.; Minshall, R. D. Role of Src-induced dynamin-2 phosphorylation in caveolae-mediated endocytosis in endothelial cells J. Biol. Chem. 2004, 279, 20392-400 10.1074/jbc.M308710200
34. Kim, Y. S.; Jung, J. A.; Kim, H. J.; Ahn, Y. H.; Yoo, J. S.; Oh, S.; Cho, C.; Yoo, H. S.; Ko, J. H. Galectin-3 binding protein promotes cell motility in colon cancer by stimulating the shedding of protein tyrosine phosphatase kappa by proprotein convertase 5 Biochem. Biophys. Res. Commun. 2011, 404, 96-102 10.1016/j.bbrc.2010.11.071
35. Wang, Y.; Chen, J.; Meng, L.; Liu, J.; Du, D.; Zou, Y. A histopathologic and immunohistochemical study of prognostic factors in esophageal squamous cell carcinoma Zhonghua Binglixue Zazhi 2000, 29, 267-71
36. Uhlen, M.; Bjorling, E.; Agaton, C.; Szigyarto, C. A.; Amini, B.; Andersen, E.; Andersson, A. C.; Angelidou, P.; Asplund, A.; Asplund, C.; Berglund, L.; Bergstrom, K.; Brumer, H.; Cerjan, D.; Ekstrom, M.; Elobeid, A.; Eriksson, C.; Fagerberg, L.; Falk, R.; Fall, J.; Forsberg, M.; Bjorklund, M. G.; Gumbel, K.; Halimi, A.; Hallin, I.; Hamsten, C.; Hansson, M.; Hedhammar, M.; Hercules, G.; Kampf, C.; Larsson, K.; Lindskog, M.; Lodewyckx, W.; Lund, J.; Lundeberg, J.; Magnusson, K.; Malm, E.; Nilsson, P.; Odling, J.; Oksvold, P.; Olsson, I.; Oster, E.; Ottosson, J.; Paavilainen, L.; Persson, A.; Rimini, R.; Rockberg, J.; Runeson, M.; Sivertsson, A.; Skollermo, A.; Steen, J.; Stenvall, M.; Sterky, F.; Stromberg, S.; Sundberg, M.; Tegel, H.; Tourle, S.; Wahlund, E.; Walden, A.; Wan, J.; Wernerus, H.; Westberg, J.; Wester, K.; Wrethagen, U.; Xu, L. L.; Hober, S.; Ponten, F. A human protein atlas for normal and cancer tissues based on antibody proteomics Mol. Cell. Proteomics 2005, 4, 1920-32 10.1074/mcp.M500279-MCP200
37. Uhlen, M.; Oksvold, P.; Fagerberg, L.; Lundberg, E.; Jonasson, K.; Forsberg, M.; Zwahlen, M.; Kampf, C.; Wester, K.; Hober, S.; Wernerus, H.; Bjorling, L.; Ponten, F. Towards a knowledge-based Human Protein Atlas Nat. Biotechnol. 2010, 28, 1248-50 10.1038/nbt1210-1248
38. Bhattacharyya, S.; Bhattacharya, R.; Curley, S.; McNiven, M. A.; Mukherjee, P. Nanoconjugation modulates the trafficking and mechanism of antibody induced receptor endocytosis Proc. Natl. Acad. Sci. U. S. A. 2010, 107, 14541-6 10.1073/pnas.1006507107
39. Xu, B.; Teng, L. H.; Silva, S. D.; Bijian, K.; Al Bashir, S.; Jie, S.; Dolph, M.; Alaoui-Jamali, M. A.; Bismar, T. A. The significance of dynamin 2 expression for prostate cancer progression, prognostication, and therapeutic targeting Cancer Med. 2014, 3, 14-24 10.1002/cam4.168
40. Bhattacharya, R.; Kang-Decker, N.; Hughes, D. A.; Mukherjee, P.; Shah, V.; McNiven, M. A.; Mukhopadhyay, D. Regulatory role of dynamin-2 in VEGFR-2/KDR-mediated endothelial signaling FASEB J. 2005, 19, 1692-4 10.1096/fj.05-3889fje
41. Lee, M. Y.; Skoura, A.; Park, E. J.; Landskroner-Eiger, S.; Jozsef, L.; Luciano, A. K.; Murata, T.; Pasula, S.; Dong, Y.; Bouaouina, M.; Calderwood, D. A.; Ferguson, S. M.; De Camilli, P.; Sessa, W. C. Dynamin 2 regulation of integrin endocytosis, but not VEGF signaling, is crucial for developmental angiogenesis Development 2014, 141, 1465-72 10.1242/dev.104539
42. Praefcke, G. J.; McMahon, H. T. The dynamin superfamily: universal membrane tubulation and fission molecules Nat. Rev. Mol. Cell Biol. 2004, 5, 133-147 10.1038/nrm1313
43. Vizcaíno, J. A.; Deutsch, E. W.; Wang, R.; Csordas, A.; Reisinger, F.; Ríos, D.; Dianes, J. A.; Sun, Z.; Farrah, T.; Bandeira, N.; Binz, P. A.; Xenarios, I.; Eisenacher, M.; Mayer, G.; Gatto, L.; Campos, A.; Chalkley, R. J.; Kraus, H. J.; Albar, J. P.; Martinez-Bartolomé, S.; Apweiler, R.; Omenn, G. S.; Martens, L.; Jones, A. R.; Hermjakob, H. ProteomeXchange provides globally co-ordinated proteomics data submission and dissemination Nat. Biotechnol. 2014, 30, 223-226 10.1038/nbt.2839
44. Sharma, V.; Eckels, J.; Taylor, G. K.; Shulman, N. J.; Stergachis, A. B.; Joyner, S. A.; Yan, P.; Whiteaker, J. R.; Halusa, G. N.; Schilling, B.; Gibson, B. W.; Colangelo, C. M.; Paulovich, A. G.; Carr, S. A.; Jaffe, J. D.; MacCoss, M. J.; MacLean, B. Panorama: A Targeted Proteomics Knowledge Base J. Proteome Res. 2014, 13, 4205-4210 10.1021/pr5006636