Discovery of colorectal cancer biomarker candidates by membrane proteomic analysis and subsequent verification using Selected Reaction Monitoring (SRM) and Tissue Microarray (TMA) Analysis

Molecular and Cellular Proteomics

Volumn 13, Issue 6, 2014, Pages 1471-1484

  Kume, Hideaki ^a   Muraoka, Satoshi ^a   Kuga, Takahisa ^a   Adachi, Jun ^a   Narumi, Ryohei ^a   Watanabe, Shio ^a   Kuwano, Masayoshi ^a   Kodera, Yoshio ^b   Matsushita, Kazuyuki ^c,d   Fukuoka, Junya ^e   Masuda, Takeshi ^f   Ishihama, Yasushi ^g   Matsubara, Hisahiro ^c   Nomura, Fumio ^c,d   Tomonaga, Takeshi ^a  

^a NATIONAL INSTITUTE OF BIOMEDICAL INNOVATION   (Japan)

^b KITASATO UNIVERSITY   (Japan)

^c CHIBA UNIVERSITY   (Japan)

^d CHIBA UNIVERSITY HOSPITAL   (Japan)

^e NAGASAKI UNIVERSITY GRADUATE SCHOOL OF BIOMEDICAL SCIENCES   (Japan)

^f KEIO UNIVERSITY   (Japan)

^g KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYL CYCLASE 2; ALPHA5 INTEGRIN; ANTHRAX TOXIN RECEPTOR 1; BIOLOGICAL MARKER; CARCINOEMBRYONIC ANTIGEN RELATED CELL ADHESION MOLECULE 5; CARCINOEMBRYONIC ANTIGEN RELATED CELL ADHESION MOLECULE 6; CD177 ANTIGEN; CELL PROTEIN; CLAUDIN 1; COLLAGENASE 4; DESMOGLEIN 3; DIPEPTIDASE 1; EGF CONTAINING FIBULIN LIKE EXTRACELLULAR MATRIX PROTEIN 1; GUANINE NUCLEOTIDE BINDING PROTEIN SUBUNIT GAMMA 4; INTEGRIN ALPHA 11; LATENT TRANSFORMING GROWTH FACTOR BETA BINDING PROTEIN 2; LEUCINE RICH REPEAT CONTAINING PROTEIN 15; MATRIX REMODELING ASSOCIATED PROTEIN 7; MEMBRANE PROTEIN; MICROFIBRILLAR ASSOCIATED PROTEIN 2; MYELOBLASTIN; PEROXISOMAL MEMBRANE PROTEIN 4; PROTEIN C8ORF55; PROTEIN PDGFRB; PROTEIN S100 A12; PROTEIN TFRC; RETINOIC ACID INDUCED PROTEIN 3; SEPRASE; UNCLASSIFIED DRUG; VANG LIKE PROTEIN 2; ZINC TRANSPORTER; TUMOR MARKER; TUMOR PROTEIN;

ARTICLE; CANCER TISSUE; COLORECTAL CANCER; COLORECTAL POLYP; CONTROLLED STUDY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; ISOTOPE LABELING; METASTASIS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEOMICS; SELECTED REACTION MONITORING; TISSUE MICROARRAY; UNINDEXED SEQUENCE; WESTERN BLOTTING; BIOSYNTHESIS; COLORECTAL TUMOR; GENE EXPRESSION REGULATION; GENETICS; ISOLATION AND PURIFICATION; PATHOLOGY;

COLORECTAL NEOPLASMS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MEMBRANE PROTEINS; NEOPLASM PROTEINS; PROTEOMICS; TISSUE ARRAY ANALYSIS; TUMOR MARKERS, BIOLOGICAL;

EID: 84901914359     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M113.037093     Document Type: Article

References (43)

1. 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., and Pappin, D. J. (2004) Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents, Mol. Cell. Proteomics 3, 1154-1169
2. Ong, S. E., Blagoev, B., Kratchmarova, I., Kristensen, D. B., Steen, H., Pandey, A., and Mann, M. (2002) Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 1, 376-386
3. Whiteaker, J. R., Zhang, H., Zhao, L., Wang, P., Kelly-Spratt, K. S., Ivey, R. G., Piening, B. D., Feng, L. C., Kasarda, E., Gurley, K. E., Eng, J. K., Chodosh, L. A., Kemp, C. J., McIntosh, M. W., and Paulovich, A. G. (2007) Integrated pipeline for mass spectrometry-based discovery and confirmation of biomarkers demonstrated in a mouse model of breast cancer. J. Proteome Res. 6, 3962-3975 (Pubitemid 350032560)
4. Keshishian, H., Addona, T., Burgess, M., Mani, D. R., Shi, X., Kuhn, E., Sabatine, M. S., Gerszten, R. E., and Carr, S. A. (2009) Quantification of cardiovascular biomarkers in patient plasma by targeted mass spectrometry and stable isotope dilution. Mol. Cell. Proteomics 8, 2339-2349
5. 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., and Paulovich, A. G. (2011) A targeted proteomics-based pipeline for verification of biomarkers in plasma. Nat. Biotechnol. 29, 625-634
6. Ahram, M., Litou, Z. I., Fang, R., and Al-Tawallbeh, G. (2006) Estimation of membrane proteins in the human proteome. In Silico Biol. 6, 379-386 (Pubitemid 44857635)
7. Hopkins, A. L., and Groom, C. R. (2002) The druggable genome. Nat. Rev. Drug Discovery 1, 727-730 (Pubitemid 37361545)
8. Chen, E. I., Cociorva, D., Norris, J. L., and Yates, J. R., 3rd. (2007) Optimization of mass spectrometry-compatible surfactants for shotgun proteomics. J. Proteome Res. 6, 2529-2538 (Pubitemid 47122350)
9. Mitra, S. K., Gantt, J. A., Ruby, J. F., Clouse, S. D., and Goshe, M. B. (2007) Membrane proteomic analysis of Arabidopsis thaliana using alternative solubilization techniques. J. Proteome Res. 6, 1933-1950 (Pubitemid 46814515)
10. Zhang, N., Chen, R., Young, N., Wishart, D., Winter, P., Weiner, J. H., and Li, L. (2007) Comparison of SDS- and methanol-assisted protein solubilization and digestion methods for Escherichia coli membrane proteome analysis by 2-D LC-MS/MS. Proteomics 7, 484-493 (Pubitemid 46362611)
11. Zhou, J., Zhou, T., Cao, R., Liu, Z., Shen, J., Chen, P., Wang, X., and Liang, S. (2006) Evaluation of the application of sodium deoxycholate to proteomic analysis of rat hippocampal plasma membrane. J. Proteome Res. 5, 2547-2553 (Pubitemid 44595157)
12. Masuda, T., Tomita, M., and Ishihama, Y. (2008) Phase transfer surfactant-aided trypsin digestion for membrane proteome analysis. J. Proteome Res. 7, 731-740 (Pubitemid 351294035)
13. Masuda, T., Saito, N., Tomita, M., and Ishihama, Y. (2009) Unbiased quantitation of Escherichia coli membrane proteome using phase transfer surfactants. Mol. Cell. Proteomics 8, 2770-2777
14. Tomonaga, T., Matsushita, K., Yamaguchi, S., Oh-Ishi, M., Kodera, Y., Maeda, T., Shimada, H., Ochiai, T., and Nomura, F. (2004) Identification of altered protein expression and post-translational modifications in primary colorectal cancer by using agarose two-dimensional gel electrophoresis. Clin. Cancer Res. 10, 2007-2014 (Pubitemid 38375560)
15. Nishimori, T., Tomonaga, T., Matsushita, K., Oh-Ishi, M., Kodera, Y., Maeda, T., Nomura, F., Matsubara, H., Shimada, H., and Ochiai, T. (2006) Proteomic analysis of primary esophageal squamous cell carcinoma reveals downregulation of a cell adhesion protein, periplakin. Proteomics 6, 1011-1018 (Pubitemid 43260225)
16. Seimiya, M., Tomonaga, T., Matsushita, K., Sunaga, M., Oh-Ishi, M., Kodera, Y., Maeda, T., Takano, S., Togawa, A., Yoshitomi, H., Otsuka, M., Yamamoto, M., Nakano, M., Miyazaki, M., and Nomura, F. (2008) Identification of novel immunohistochemical tumor markers for primary hepatocellular carcinoma; clathrin heavy chain and formiminotransferase cyclodeaminase. Hepatology 48, 519-530
17. Katada, K., Tomonaga, T., Satoh, M., Matsushita, K., Tonoike, Y., Kodera, Y., Hanazawa, T., Nomura, F., and Okamoto, Y. (2012) Plectin promotes migration and invasion of cancer cells and is a novel prognostic marker for head and neck squamous cell carcinoma. J. Proteomics 75, 1803-1815
18. Lazebnik, Y. (2010) What are the hallmarks of cancer? Nat. Rev. Cancer 10, 232-233
19. Muraoka, S., Kume, H., Watanabe, S., Adachi, J., Kuwano, M., Sato, M., Kawasaki, N., Kodera, Y., Ishitobi, M., Inaji, H., Miyamoto, Y., Kato, K., and Tomonaga, T. (2012) Strategy for SRM-based verification of biomarker candidates discovered by iTRAQ method in limited breast cancer tissue samples. J. Proteome Res. 11, 4201-4210
20. Muraoka, S., Kume, H., Adachi, J., Shiromizu, T., Watanabe, S., Masuda, T., Ishihama, Y., and Tomonaga, T. (2013) In-depth membrane proteomic study of breast cancer tissues for the generation of a chromosome-based protein list. J. Proteome Res. 12, 208-213
21. Narumi, R., Murakami, T., Kuga, T., Adachi, J., Shiromizu, T., Muraoka, S., Kume, H., Kodera, Y., Matsumoto, M., Nakayama, K., Miyamoto, Y., Ishitobi, M., Inaji, H., Kato, K., and Tomonaga, T. (2012) A strategy for large-scale phosphoproteomics and SRM-based validation of human breast cancer tissue samples. J. Proteome Res. 11, 5311-5322
22. Shiromizu, T., Adachi, J., Watanabe, S., Murakami, T., Kuga, T., Muraoka, S., and Tomonaga, T. (2013) Identification of missing proteins in the nextprot database and unregistered phosphopeptides in the phosphositeplus database as part of the chromosome-centric human proteome project. J. Proteome Res. DOI 10.1021/pr300825v
23. Rappsilber, J., Ishihama, Y., and Mann, M. (2003) Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal. Chem. 75, 663-670 (Pubitemid 36176744)
24. Selevsek, N., Matondo, M., Sanchez Carbayo, M., Aebersold, R., and Domon, B. Systematic quantification of peptides/proteins in urine using selected reaction monitoring. Proteomics 11, 1135-1147
25. Kitano, H., Kageyama, S., Hewitt, S. M., Hayashi, R., Doki, Y., Ozaki, Y., Fujino, S., Takikita, M., Kubo, H., and Fukuoka, J. (2010) Podoplanin expression in cancerous stroma induces lymphangiogenesis and predicts lymphatic spread and patient survival. Arch. Pathol. Lab Med. 134, 1520-1527
26. Yang, B., Gao, J., Rao, Z., and Shen, Q. (2013) Clinicopathological and Prognostic Significance of alpha5beta1-integrin and MMP-14 Expressions in Colorectal Cancer. Neoplasma DOI 10.4149/neo-2013-034
27. Zougman, A., Hutchins, G. G., Cairns, D. A., Verghese, E., Perry, S. L., Jayne, D. G., Selby, P. J., and Banks, R. E. (2013) Retinoic acid-induced protein 3: identification and characterisation of a novel prognostic colon cancer biomarker. Eur. J. Cancer 49, 531-539
28. Sillars-Hardebol, A. H., Carvalho, B., de Wit, M., Postma, C., Delis-van Diemen, P. M., Mongera, S., Ylstra, B., van de Wiel, M. A., Meijer, G. A., and Fijneman, R. J. (2010) Identification of key genes for carcinogenic pathways associated with colorectal adenoma-to-carcinoma progression. Tumour Biol. 31, 89-96
29. Prutki, M., Poljak-Blazi, M., Jakopovic, M., Tomas, D., Stipancic, I., and Zarkovic, N. (2006) Altered iron metabolism, transferrin receptor 1 and ferritin in patients with colon cancer. Cancer Lett. 238, 188-196 (Pubitemid 43867908)
30. Luo, Y., Wang, L., and Wang, J. (2013) Developing proteomics-based biomarkers for colorectal neoplasms for clinical practice: Opportunities and challenges. Proteomics Clin. Appl. 7, 30-41
31. Lehtio, J., and De Petris, L. (2010) Lung cancer proteomics, clinical and technological considerations. J. Proteomics 73, 1851-1863
32. Kalinina, J., Peng, J., Ritchie, J. C., and Van Meir, E. G. (2011) Proteomics of gliomas: initial biomarker discovery and evolution of technology Neuro Oncol. 13, 926-942
33. Thingholm, T. E., Bak, S., Beck-Nielsen, H., Jensen, O. N., and Gaster, M. (2011) Characterization of human myotubes from type 2 diabetic and nondiabetic subjects using complementary quantitative mass spectrometric methods. Mol. Cell. Proteomics 10, DOI 10.1074/mcp.M110.006650
34. Josic, D., and Clifton, J. G. (2007) Mammalian plasma membrane proteomics. Proteomics 7, 3010-3029 (Pubitemid 47359936)
35. Chen, J. S., Chen, K. T., Fan, C. W., Han, C. L., Chen, Y. J., Yu, J. S., Chang, Y. S., Chien, C. W., Wu, C. P., Hung, R. P., and Chan, E. C. (2010) Comparison of membrane fraction proteomic profiles of normal and cancerous human colorectal tissues with gel-assisted digestion and iTRAQ labeling mass spectrometry. FEBS J. 277, 3028-3038
36. Han, C. L., Chen, J. S., Chan, E. C., Wu, C. P., Yu, K. H., Chen, K. T., Tsou, C. C., Tsai, C. F., Chien, C. W., Kuo, Y. B., Lin, P. Y., Yu, J. S., Hsueh, C., Chen, M. C., Chan, C. C., Chang, Y. S., and Chen, Y. J. (2011) An informatics-assisted label-free approach for personalized tissue membrane proteomics: case study on colorectal cancer. Mol. Cell. Proteomics 10, DOI 10.1074/mcp.M110.003087
37. Besson, D., Pavageau, A. H., Valo, I., Bourreau, A., Belanger, A., Eymerit-Morin, C., Mouliere, A., Chassevent, A., Boisdron-Celle, M., Morel, A., Solassol, J., Campone, M., Gamelin, E., Barre, B., Coqueret, O., and Guette, C. (2011) A quantitative proteomic approach of the different stages of colorectal cancer establishes OLFM4 as a new nonmetastatic tumor marker. Mol. Cell. Proteomics 10, DOI 10.1074/mcp.M111.009712
38. Polisetty, R. V., Gautam, P., Sharma, R., Harsha, H. C., Nair, S. C., Gupta, M. K., Uppin, M. S., Challa, S., Puligopu, A. K., Ankathi, P., Purohit, A. K., Chandak, G. R., Pandey, A., and Sirdeshmukh, R. (2012) LC-MS/MS analysis of differentially expressed glioblastoma membrane proteome reveals altered calcium signaling and other protein groups of regulatory functions. Mol. Cell. Proteomics 11, DOI 10.1074/mcp.M111.013565
39. Rucevic, M., Hixson, D., and Josic, D. (2011) Mammalian plasma membrane proteins as potential biomarkers and drug targets. Electrophoresis 32, 1549-1564
40. Choi, D. S., Park, J. O., Jang, S. C., Yoon, Y. J., Jung, J. W., Choi, D. Y., Kim, J. W., Kang, J. S., Park, J., Hwang, D., Lee, K. H., Park, S. H., Kim, Y. K., Desiderio, D. M., Kim, K. P., and Gho, Y. S. (2011) Proteomic analysis of microvesicles derived from human colorectal cancer ascites. Proteomics 11, 2745-2751
41. Peinado, H., Aleckovic, M., Lavotshkin, S., Matei, I., Costa-Silva, B., Moreno-Bueno, G., Hergueta-Redondo, M., Williams, C., Garcia-Santos, G., Ghajar, C., Nitadori-Hoshino, A., Hoffman, C., Badal, K., Garcia, B. A., Callahan, M. K., Yuan, J., Martins, V. R., Skog, J., Kaplan, R. N., Brady, M. S., Wolchok, J. D., Chapman, P. B., Kang, Y., Bromberg, J., and Lyden, D. (2012) Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat. Med. 18, 883-891
42. Shao, H., Chung, J., Balaj, L., Charest, A., Bigner, D. D., Carter, B. S., Hochberg, F. H., Breakefield, X. O., Weissleder, R., and Lee, H. (2012) Protein typing of circulating microvesicles allows real-time monitoring of glioblastoma therapy. Nat. Med. 18, 1835-1840
43. Vizcaino, J. A., Cote, R. G., Csordas, A., Dianes, J. A., Fabregat, A., Foster, J. M., Griss, J., Alpi, E., Birim, M., Contell, J., O'Kelly, G., Schoenegger, A., Ovelleiro, D., Perez-Riverol, Y., Reisinger, F., Rios, D., Wang, R., and Hermjakob, H. (2013) The PRoteomics IDEntifications (PRIDE) database and associated tools: status in 2013. Nucleic Acids Res. 41, D1063-1069