Label-free quantitative proteomics and N-glycoproteomics analysis of KRAS-activated human bronchial epithelial cells

Molecular and Cellular Proteomics

Volumn 11, Issue 10, 2012, Pages 901-915

  Sudhir, Putty Reddy ^a   Chen, Chein Hung ^a   Kumari, Madireddy Pavana ^a   Wang, Mei Jung ^b   Tsou, Chih Chiang ^c   Sung, Ting Yi ^c   Chen, Jeou Yuan ^b   Chen, Chung Hsuan ^a  

^a GENOMICS RESEARCH CENTER   (Taiwan)

^b INSTITUTE OF BIOMEDICAL SCIENCES   (Taiwan)

^c INSTITUTE OF INFORMATION SCIENCE   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

5' NUCLEOTIDASE; ACTIVATED LEUKOCYTE CELL ADHESION MOLECULE; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ALDEHYDE DEHYDROGENASE; ALDEHYDE DEHYDROGENASE 3A1; ALPHA3 INTEGRIN; BASAL CELL ADHESION MOLECULE; BULLOUS PEMPHIGOID ANTIGEN 1; CARBONATE DEHYDRATASE II; CATHEPSIN D; CELL ADHESION MOLECULE; EPHRIN RECEPTOR A2; FATTY ACID BINDING PROTEIN; FATTY ACID BINDING PROTEIN 5; GLUTAMATE AMMONIA LIGASE; GLYCOPROTEIN; HISTONE H4; K RAS PROTEIN; MESSENGER RNA; MICROTUBULE ASSOCIATED PROTEIN 5; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 2; PROTEOME; SEMAPHORIN; SEMAPHORIN 4B; SODIUM POTASSIUM TRANSPORTING ATPASE SUBUNIT BETA 1; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TUMOR MARKER; TUMOR PROTEIN; UNCLASSIFIED DRUG; VIMENTIN;

ARTICLE; BRONCHUS EPITHELIUM CELL; BRONCHUS MUCOSA; CANCER CELL CULTURE; CANCER INVASION; CANCER TISSUE; CELL ACTIVATION; COMPUTER MODEL; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EPITHELIUM CELL; GENE MUTATION; HUMAN; HUMAN CELL; LIVER CARCINOGENESIS; MICROARRAY ANALYSIS; ONCOGENE K RAS; PEPTIDE ANALYSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN GLYCOSYLATION; PROTEIN SYNTHESIS REGULATION; PROTEOMICS; QUANTITATIVE ANALYSIS;

ADENOCARCINOMA; APOPTOSIS REGULATORY PROTEINS; BRONCHI; CELL LINE, TUMOR; EPITHELIAL CELLS; FATTY ACID-BINDING PROTEINS; GENE EXPRESSION REGULATION, NEOPLASTIC; GLYCOPROTEINS; GLYCOSYLATION; HUMANS; LUNG NEOPLASMS; PROTEOME; PROTEOMICS; PROTO-ONCOGENE PROTEINS; RAS PROTEINS; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS; SEMAPHORINS; TISSUE INHIBITOR OF METALLOPROTEINASE-1; TUMOR MARKERS, BIOLOGICAL;

EID: 84867166590     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M112.020875     Document Type: Article

References (48)

1. Jemal, A., Bray, F., Center, M. M., Ferlay, J., Ward, E., and Forman, D. (2011) Global cancer statistics. Cancer J. Clin. 61, 69-90
2. Rodenhuis, S., Slebos, R. J., Boot, A. J., Evers, S. G., Mooi, W. J., Wagenaar, S. S., van Bodegom, P. C., and Bos, J. L. (1988) Incidence and possible clinical significance of K-ras oncogene activation in adenocarcinoma of the human lung. Cancer Res. 48, 5738-5741
3. Ding, L., Getz, G., Wheeler, D. A., Mardis, E. R., McLellan, M. D., Cibulskis, K., Sougnez, C., Greulich, H., Muzny, D. M., Morgan, M. B., Fulton, L., Fulton, R. S., Zhang, Q., Wendl, M. C., Lawrence, M. S., Larson, D. E., Chen, K., Dooling, D. J., Sabo, A., Hawes, A. C., Shen, H., Jhangiani, S. N., Lewis, L. R., Hall, O., Zhu, Y., Mathew, T., Ren, Y., Yao, J., Scherer, S. E., Clerc, K., Metcalf, G. A., Ng, B., Milosavljevic, A., Gonzalez-Garay, M. L., Osborne, J. R., Meyer, R., Shi, X., Tang, Y., Koboldt, D. C., Lin, L., Abbott, R., Miner, T. L., Pohl, C., Fewell, G., Haipek, C., Schmidt, H., Dunford-Shore, B. H., Kraja, A., Crosby, S. D., Sawyer, C. S., Vickery, T., Sander, S., Robinson, J., Winckler, W., Baldwin, J., Chirieac, L. R., Dutt, A., Fennell, T., Hanna, M., Johnson, B. E., Onofrio, R. C., Thomas, R. K., Tonon, G., Weir, B. A., Zhao, X., Ziaugra, L., Zody, M. C., Giordano, T., Orringer, M. B., Roth, J. A., Spitz, M. R., Wistuba, II, Ozenberger, B., Good, P. J., Chang, A. C., Beer, D. G., Watson, M. A., Ladanyi, M., Broderick, S., Yoshizawa, A., Travis, W. D., Pao, W., Province, M. A., Weinstock, G. M., Varmus, H. E., Gabriel, S. B., Lander, E. S., Gibbs, R. A., Meyerson, M., and Wilson, R. K. (2008) Somatic mutations affect key pathways in lung adenocarcinoma. Nature 455, 1069-1075
4. Malumbres, M., and Barbacid, M. (2003) RAS oncogenes: the first 30 years. Nat. Rev. Cancer 3, 459-465 (Pubitemid 37328850)
5. Riely, G. J., Marks, J., and Pao, W. (2009) KRAS mutations in non-small cell lung cancer. Proc. Am. Thorac. Soc. 6, 201-205
6. Forbes, S., Clements, J., Dawson, E., Bamford, S., Webb, T., Dogan, A., Flanagan, A., Teague, J., Wooster, R., Futreal, P. A., and Stratton, M. R. (2006) COSMIC 2005. Br. J. Cancer 94, 318-322 (Pubitemid 43151554)
7. Perona, R., and Sánchez-Pérez, I. (2004) Control of oncogenesis and cancer therapy resistance. Br. J. Cancer 90, 573-577 (Pubitemid 38297192)
8. Bernhard, E. J., Stanbridge, E. J., Gupta, S., Gupta, A. K., Soto, D., Bakanauskas, V. J., Cerniglia, G. J., Muschel, R. J., and McKenna, W. G. (2000) Direct evidence for the contribution of activated N-ras and K-ras oncogenes to increased intrinsic radiation resistance in human tumor cell lines. Cancer Res. 60, 6597-6600
9. Rachagani, S., Senapati, S., Chakraborty, S., Ponnusamy, M. P., Kumar, S., Smith, L. M., Jain, M., and Batra, S. K. (2011) Activated KrasG(1)(2)D is associated with invasion and metastasis of pancreatic cancer cells through inhibition of E-cadherin. Br. J. Cancer 104, 1038-1048
10. Tchernitsa, O. I., Sers, C., Zuber, J., Hinzmann, B., Grips, M., Schramme, A., Lund, P., Schwendel, A., Rosenthal, A., and Schäfer, R. (2004) Transcriptional basis of KRAS oncogene-mediated cellular transformation in ovarian epithelial cells. Oncogene 23, 4536-4555 (Pubitemid 38850403)
11. Qian, J., Niu, J., Li, M., Chiao, P. J., and Tsao, M. S. (2005) In vitro modeling of human pancreatic duct epithelial cell transformation defines gene expression changes induced by K-ras oncogenic activation in pancreatic carcinogenesis. Cancer Res. 65, 5045-5053 (Pubitemid 40827312)
12. 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., and Varmus, H. E. (2008) Comparisons of tyrosine phosphorylated proteins in cells expressing lung cancer-specific alleles of EGFR and KRAS. Proc. Natl. Acad. Sci. U.S.A. 105, 14112-14117
13. Sudhir, P. R., Hsu, C. L., Wang, M. J., Wang, Y. T., Chen, Y. J., Sung, T. Y., Hsu, W. L., Yang, U. C., and Chen, J. Y. (2011) Phosphoproteomics Identifies Oncogenic Ras Signaling Targets and Their Involvement in Lung Adenocarcinomas. PLoS ONE 6, e20199
14. Pan, S., Chen, R., Aebersold, R., and Brentnall, T. A. (2011) Mass spectrometry based glycoproteomics-from a proteomics perspective. Mol. Cell. Proteomics 10, R110.003251
15. Reis, C. A., Osorio, H., Silva, L., Gomes, C., and David, L. (2010) Alterations in glycosylation as biomarkers for cancer detection. J. Clin. Pathol. 63, 322-329
16. Kobata, A. (1989) Altered glycosylation of surface glycoproteins in tumor cells and its clinical application. Pigment Cell Res. 2, 304-308
17. Hakomori, S. (2002) Glycosylation defining cancer malignancy: new wine in an old bottle. Proc. Natl. Acad. Sci. U.S.A. 99, 10231-10233
18. Dennis, J. W., Granovsky, M., and Warren, C. E. (1999) Glycoprotein glycosylation and cancer progression. Biochim. Biophys. Acta. 1473, 21-34
19. Wojciechowicz, D. C., Park, P. Y., and Paty, P. B. (1995) Beta 1-6 branching of N-linked carbohydrate is associated with K-ras mutation in human colon carcinoma cell lines. Biochem. Biophys. Res. Commun. 212, 758-766
20. Schwarz, R. E., Wojciechowicz, D. C., Park, P. Y., and Paty, P. B. (1996) Phytohemagglutinin-L (PHA-L) lectin surface binding of N-linked beta 1-6 carbohydrate and its relationship to activated mutant ras in human pancreatic cancer cell lines. Cancer Lett. 107, 285-291 (Pubitemid 26382002)
21. Lau, K. S., and Dennis, J. W. (2008) N-Glycans in cancer progression. Glycobiology 18, 750-760
22. Contessa, J. N., Bhojani, M. S., Freeze, H. H., Rehemtulla, A., and Lawrence, T. S. (2008) Inhibition of N-linked glycosylation disrupts receptor tyrosine kinase signaling in tumor cells. Cancer Res. 68, 3803-3809
23. Gu, J., Sato, Y., Kariya, Y., Isaji, T., Taniguchi, N., and Fukuda, T. (2009) A mutual regulation between cell-cell adhesion and N-glycosylation: implication of the bisecting GlcNAc for biological functions. J. Proteome Res. 8, 431-435
24. Yan, Z., Deng, X., Chen, M., Xu, Y., Ahram, M., Sloane, B. F., and Friedman, E. (1997) Oncogenic c-Ki-ras but not oncogenic c-Ha-ras up-regulates CEA expression and disrupts basolateral polarity in colon epithelial cells. J. Biol. Chem. 272, 27902-27907 (Pubitemid 27473593)
25. Seales, E. C., Jurado, G. A., Singhal, A., and Bellis, S. L. (2003) Ras oncogene directs expression of a differentially sialylated, functionally altered beta1 integrin. Oncogene 22, 7137-7145 (Pubitemid 37378546)
26. Mann, M. (2006) Functional and quantitative proteomics using SILAC. Nat. Rev. Mol. Cell Biol. 7, 952-958
27. Burande, C. F., Heuzé, M. L., Lamsoul, I., Monsarrat, B., Uttenweiler-Joseph, S., and Lutz, P. G. (2009) A label-free quantitative proteomics strategy to identify E3 ubiquitin ligase substrates targeted to proteasome degradation. Mol. Cell. Proteomics 8, 1719-1727
28. Ramirez, R. D., Sheridan, S., Girard, L., Sato, M., Kim, Y., Pollack, J., Peyton, M., Zou, Y., Kurie, J. M., Dimaio, J. M., Milchgrub, S., Smith, A. L., Souza, R. F., Gilbey, L., Zhang, X., Gandia, K., Vaughan, M. B., Wright, W. E., Gazdar, A. F., Shay, J. W., and Minna, J. D. (2004) Immortalization of human bronchial epithelial cells in the absence of viral oncoproteins. Cancer Res. 64, 9027-9034 (Pubitemid 39665513)
29. Sato, M., Vaughan, M. B., Girard, L., Peyton, M., Lee, W., Shames, D. S., Ramirez, R. D., Sunaga, N., Gazdar, A. F., Shay, J. W., and Minna, J. D. (2006) Multiple oncogenic changes (K-RAS(V12), p53 knockdown, mutant EGFRs, p16 bypass, telomerase) are not sufficient to confer a full malignant phenotype on human bronchial epithelial cells. Cancer Res. 66, 2116-2128
30. Hubner, N. C., Ren, S., and Mann, M. (2008) Peptide separation with immobilized pI strips is an attractive alternative to in-gel protein digestion for proteome analysis. Proteomics 8, 4862-4872
31. Zhang, H., Li, X. J., Martin, D. B., and Aebersold, R. (2003) Identification and quantification of N-linked glycoproteins using hydrazide chemistry, stable isotope labeling and mass spectrometry. Nat. Biotechnol. 21, 660-666 (Pubitemid 36638093)
32. Tsou, C. C., Tsai, C. F., Tsui, Y. H., Sudhir, P. R., Wang, Y. T., Chen, Y. J., Chen, J. Y., Sung, T. Y., and Hsu, W. L. (2010) IDEAL-Q, an automated tool for label-free quantitation analysis using an efficient peptide alignment approach and spectral data validation. Mol. Cell. Proteomics 9, 131-144
33. Hörth, P., Miller, C. A., Preckel, T., and Wenz, C. (2006) Efficient fractionation and improved protein identification by peptide OFFGEL electrophoresis. Mol. Cell. Proteomics 5, 1968-1974 (Pubitemid 44688204)
34. Horsch, M., Recktenwald, C. V., Schädler, S., Hrabé de Angelis, M., Seliger, B., and Beckers, J. (2009) Overexpressed vs mutated Kras in murine fibroblasts: a molecular phenotyping study. Br. J. Cancer 100, 656-662
35. Hatley, M. E., Patrick, D. M., Garcia, M. R., Richardson, J. A., Bassel-Duby, R., van Rooij, E., and Olson, E. N. (2010) Modulation of K-Ras-dependent lung tumorigenesis by MicroRNA-21. Cancer Cell 18, 282-293
36. Talotta, F., Cimmino, A., Matarazzo, M. R., Casalino, L., De Vita, G., D'Esposito, M., Di Lauro, R., and Verde, P. (2009) An autoregulatory loop mediated by miR-21 and PDCD4 controls the AP-1 activity in RAS transformation. Oncogene 28, 73-84
37. Zielinska, D. F., Gnad, F., Wiśniewski, J. R., and Mann, M. (2010) Precision mapping of an in vivo N-glycoproteome reveals rigid topological and sequence constraints. Cell 141, 897-907
38. Forbes, S. A., Bhamra, G., Bamford, S., Dawson, E., Kok, C., Clements, J., Menzies, A., Teague, J. W., Futreal, P. A., and Stratton, M. R. (2008) The catalogue of somatic mutations in cancer (COSMIC). Curr. Protoc. Hum. Genet. Chapter 10, Unit 10 11
39. Coppé, J. P., Patil, C. K., Rodier, F., Sun, Y., Muñoz, D. P., Goldstein, J., Nelson, P. S., Desprez, P. Y., and Campisi, J. (2008) Senescence-associated secretory phenotypes reveal cell-nonautonomous functions of oncogenic RAS and the p53 tumor suppressor. PLoS Biol. 6, 2853-2868
40. Ramer, R., Eichele, K., and Hinz, B. (2007) Upregulation of tissue inhibitor of matrix metalloproteinases-1 confers the anti-invasive action of cisplatin on human cancer cells. Oncogene 26, 5822-5827 (Pubitemid 47312810)
41. Ramer, R., Merkord, J., Rohde, H., and Hinz, B. (2010) Cannabidiol inhibits cancer cell invasion via upregulation of tissue inhibitor of matrix metalloproteinases-1. Biochem. Pharmacol. 79, 955-966
42. Saha, D., Datta, P. K., and Beauchamp, R. D. (2001) Oncogenic ras represses transforming growth factor-beta /Smad signaling by degrading tumor suppressor Smad4. J. Biol. Chem. 276, 29531-29537
43. Wang, Q., Sun, Z., and Yang, H. S. (2008) Downregulation of tumor suppressor Pdcd4 promotes invasion and activates both beta-catenin/Tcf and AP-1-dependent transcription in colon carcinoma cells. Oncogene 27, 1527-1535 (Pubitemid 351347877)
44. Cruz-Munoz, W., and Khokha, R. (2008) The role of tissue inhibitors of metalloproteinases in tumorigenesis and metastasis. Crit. Rev. Clin. Lab. Sci. 45, 291-338 (Pubitemid 351883130)
45. Jiang, Y., Goldberg, I. D., and Shi, Y. E. (2002) Complex roles of tissue inhibitors of metalloproteinases in cancer. Oncogene 21, 2245-2252 (Pubitemid 34311378)
46. Kim, Y. S., Hwang, S. Y., Kang, H. Y., Sohn, H., Oh, S., Kim, J. Y., Yoo, J. S., Kim, Y. H., Kim, C. H., Jeon, J. H., Lee, J. M., Kang, H. A., Miyoshi, E., Taniguchi, N., Yoo, H. S., and Ko, J. H. (2008) Functional proteomics study reveals that N-Acetylglucosaminyltransferase V reinforces the invasive/ metastatic potential of colon cancer through aberrant glycosylation on tissue inhibitor of metalloproteinase-1. Mol. Cell. Proteomics 7, 1-14 (Pubitemid 351248231)
47. Haigis, K. M., Kendall, K. R., Wang, Y., Cheung, A., Haigis, M. C., Glickman, J. N., Niwa-Kawakita, M., Sweet-Cordero, A., Sebolt-Leopold, J., Shannon, K. M., Settleman, J., Giovannini, M., and Jacks, T. (2008) Differential effects of oncogenic K-Ras and N-Ras on proliferation, differentiation and tumor progression in the colon. Nat. Genet. 40, 600-608 (Pubitemid 351601205)
48. Voice, J. K., Klemke, R. L., Le, A., and Jackson, J. H. (1999) Four human ras homologs differ in their abilities to activate Raf-1, induce transformation, and stimulate cell motility. J. Biol. Chem. 274, 17164-17170