Distinct splice variants and pathway enrichment in the cell-line models of aggressive human breast cancer subtypes

Journal of Proteome Research

Volumn 13, Issue 1, 2014, Pages 212-227

  Menon, Rajasree ^a   Im, Hogune ^d   Zhang, Emma ^e   Wu, Shiaw Lin ^e   Chen, Rui ^d   Snyder, Michael ^d   Hancock, William S ^e,f   Omenn, Gilbert S ^a,b,c  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

^d STANFORD UNIVERSITY   (United States)

^e NORTHEASTERN UNIVERSITY   (United States)

^f Yonsei University   (South Korea)

Author keywords

breast cancer subtypes; EGFR; ERBB2+ (Her2 neu); I TASSER; proteotypic peptide; splice variant protein (SpP); splice variant transcript (SpT); splice variants (SpV)

Indexed keywords

AMINOSUGAR; BRCA1 PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTROGEN RECEPTOR; HORMONE RECEPTOR; INTEGRIN; LIPID; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NUCLEOTIDE; PROGESTERONE RECEPTOR; PROTEIN P53; RNA; TUMOR SUPPRESSOR PROTEIN;

AMINO ACID METABOLISM; ARTICLE; BREAST CANCER; BREAST CELL; CANCER CELL; CANCER CELL CULTURE; CELL ADHESION; CELL AGGREGATION; CHROMOSOME 17; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME ACTIVITY; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; INFLAMMATORY BREAST CANCER; ONTOLOGY; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROTEIN PROCESSING; RNA SEQUENCE; RNA SPLICING; RNA TRANSLATION; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR GENE;

BREAST NEOPLASMS; CELL LINE, TUMOR; FEMALE; HUMANS; MASS SPECTROMETRY; RNA SPLICING;

EID: 84891762234     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr400773v     Document Type: Article

References (50)

1. Germann, S.; Gratadou, L.; Dutertre, M.; Auboeuf, D. Splicing Programs and Cancer J. Nucleic Acids 2012, 2012, 1-9
2. Revil, T.; Toutant, J.; Shkreta, L.; Garneau, D.; Cloutier, P.; Chabot, B. Protein kinase C-dependent control of bcl-x alternative splicing Mol. Cell. Biol. 2007, 27 (24) 8431-8441
3. Végran, F.; Boidot, R.; Oudin, C.; Riedinger, J.-M.; Bonnetain, F.; Lizard-Nacol, S. Overexpression of caspase-3s splice variant in locally advanced breast carcinoma is associated with poor response to neoadjuvant chemotherapy Clin. Cancer Res. 2006, 12 (19) 5794-5800
4. Kawai, S.; Kato, T.; Inaba, H.; Okahashi, N.; Amano, A. Odd-skipped related 2 splicing variants show opposite transcriptional activity Biochem. Biophys. Res. Commun. 2005, 328 (1) 306-311
5. Menon, R.; Roy, A.; Mukherjee, S.; Belkin, S.; Zhang, Y.; Omenn, G. S. Functional implications of structural predictions for alternative splice proteins expressed in Her2/neu-induced breast cancers J. Proteome Res 2011, 10 (12) 5503-11
6. Liu, Z.; Wang, Y.; Wang, S.; Zhang, J.; Zhang, F.; Niu, Y. Nek2C functions as a tumor promoter in human breast tumorigenesis Int. J. Mol. Med. 2012, 775-82
7. Choi, J. W.; Kim, D. G.; Lee, A. E.; Kim, H. R.; Lee, J. Y.; Kwon, N. H.; Shin, Y. K.; Hwang, S. K.; Chang, S. H.; Cho, M. H.; Choi, Y. L.; Kim, J.; Oh, S. H.; Kim, B.; Kim, S. Y.; Jeon, H. S.; Park, J. Y.; Kang, H. P.; Park, B. J.; Han, J. M.; Kim, S. Cancer-associated splicing variant of tumor suppressor AIMP2/p38: pathological implication in tumorigenesis PLoS Genet 2011, 7 (3) 1-13
8. Marko-Varga, G.; Omenn, G. S.; Paik, Y.-K.; Hancock, W. S. A First Step Toward Completion of a Genome-Wide Characterization of the Human Proteome J. Proteome Res. 2013, 12 (1) 1-5
9. Liu, S.; Im, H.; Bairoch, A.; Cristofanilli, M.; Chen, R.; Deutsch, E. W.; Dalton, S.; Fenyo, D.; Fanayan, S.; Gates, C.; Gaudet, P.; Hincapie, M.; Hanash, S.; Kim, H.; Jeong, S.-K.; Lundberg, E.; Mias, G.; Menon, R.; Mu, Z.; Nice, E.; Paik, Y.-K.; Uhlen, M.; Wells, L.; Wu, S.-L.; Yan, F.; Zhang, F.; Zhang, Y.; Snyder, M.; Omenn, G. S.; Beavis, R. C.; Hancock, W. S. A Chromosome-centric Human Proteome Project (C-HPP) to Characterize the Sets of Proteins Encoded in Chromosome 17 J. Proteome Res. 2013, 12 (1) 45-57
10. Zhang, E. Y.; Cristofanilli, M.; Robertson, F.; Reuben, J. M.; Mu, Z.; Beavis, R. C.; Im, H.; Snyder, M.; Hofree, M.; Ideker, T.; Omenn, G. S.; Fanayan, S.; Jeong, S.-K.; Paik, Y.-k.; Zhang, A. F.; Wu, S.-L.; Hancock, W. S. Genome Wide Proteomics of ERBB2 and EGFR and Other Oncogenic Pathways in Inflammatory Breast Cancer J. Proteome Res. 2013, 12 (6) 2805-17
11. Aebersold, R.; Bader, G. D.; Edwards, A. M.; van Eyk, J. E.; Kussmann, M.; Qin, J.; Omenn, G. S. The Biology/Disease-driven Human Proteome Project (B/D-HPP): Enabling Protein Research for the Life Sciences Community J. Proteome Res. 2013, 12 (1) 23-27
12. Yu, D.; Hung, M. C. Overexpression of ErbB2 in cancer and ErbB2-targeting strategies Oncogene 2000, 19 (53) 6115-21
13. Berchuck, A.; Kamel, A.; Whitaker, R.; Kerns, B.; Olt, G.; Kinney, R.; Soper, J. T.; Dodge, R.; Clarke-Pearson, D. L.; Marks, P. Overexpression of HER-2/neu is associated with poor survival in advanced epithelial ovarian cancer Cancer Res. 1990, 50 (13) 4087-91
14. Vogel, C.; Chan, A.; Gril, B.; Kim, S. B.; Kurebayashi, J.; Liu, L.; Lu, Y. S.; Moon, H. Management of ErbB2-positive breast cancer: insights from preclinical and clinical studies with lapatinib Jpn. J. Clin. Oncol. 2010, 40 (11) 999-1013
15. Jelovac, D.; Wolff, A. C. The adjuvant treatment of HER2-positive breast cancer Curr. Treat. Options Oncol. 2012, 13 (2) 230-9
16. Pohlmann, P. R.; Mayer, I. A.; Mernaugh, R. Resistance to Trastuzumab in Breast Cancer Clin. Cancer Res. 2009, 15 (24) 7479-7491
17. Nokes, B. T.; Cunliffe, H. E.; Lafleur, B.; Mount, D. W.; Livingston, R. B.; Futscher, B. W.; Lang, J. E. In Vitro Assessment of the Inflammatory Breast Cancer Cell Line SUM 149: Discovery of 2 Single Nucleotide Polymorphisms in the RNase L Gene J. Cancer 2013, 4 (2) 104-16
18. Olayioye, M. A. Update on HER-2 as a target for cancer therapy: intracellular signaling pathways of ErbB2/HER-2 and family members Breast Cancer Res. 2001, 3 (6) 385-9
19. Chen, R.; Mias, G. I.; Li-Pook-Than, J.; Jiang, L.; Lam, H. Y.; Miriami, E.; Karczewski, K. J.; Hariharan, M.; Dewey, F. E.; Cheng, Y.; Clark, M. J.; Im, H.; Habegger, L.; Balasubramanian, S.; O'Huallachain, M.; Dudley, J. T.; Hillenmeyer, S.; Haraksingh, R.; Sharon, D.; Euskirchen, G.; Lacroute, P.; Bettinger, K.; Boyle, A. P.; Kasowski, M.; Grubert, F.; Seki, S.; Garcia, M.; Whirl-Carrillo, M.; Gallardo, M.; Blasco, M. A.; Greenberg, P. L.; Snyder, P.; Klein, T. E.; Altman, R. B.; Butte, A. J.; Ashley, E. A.; Gerstein, M.; Nadeau, K. C.; Tang, H.; Snyder, M. Personal omics profiling reveals dynamic molecular and medical phenotypes Cell 2012, 148 (6) 1293-307
20. Altschul, S. F.; Gish, W.; Miller, W.; Myers, E. W.; Lipman, D. J. Basic local alignment search tool J. Mol. Biol. 1990, 215 (3) 403-10
21. Geiger, T.; Cox, J.; Mann, M. Proteomic changes resulting from gene copy number variations in cancer cells PLoS Genet. 2010, 6 (9) 1-15
22. Menon, R.; Zhang, Q.; Zhang, Y.; Fermin, D.; Bardeesy, N.; DePinho, R. A.; Lu, C.; Hanash, S. M.; Omenn, G. S.; States, D. J. Identification of novel alternative splice isoforms of circulating proteins in a mouse model of human pancreatic cancer Cancer Res. 2009, 69 (1) 300-9
23. Menon, R.; Omenn, G. S. Proteomic characterization of novel aternative splice variant proteins in Human epidermal growth factor receptor 2/neu induced breast cancers Cancer Res. 2010, 70 (9) 3440-3449
24. Jeong, K.; Kim, S.; Bandeira, N. False discovery rates in spectral identification BMC Bioinf. 2012, 13 (Suppl 16) 1-15
25. Subramanian, A.; Tamayo, P.; Mootha, V. K.; Mukherjee, S.; Ebert, B. L.; Gillette, M. A.; Paulovich, A.; Pomeroy, S. L.; Golub, T. R.; Lander, E. S.; Mesirov, J. P. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles Proc. Natl. Acad. Sci. U. S. A. 2005, 102 (43) 15545-50
26. Henjes, F.; Bender, C.; von der Heyde, S.; Braun, L.; Mannsperger, H. A.; Schmidt, C.; Wiemann, S.; Hasmann, M.; Aulmann, S.; Beissbarth, T.; Korf, U., Strong EGFR signaling in cell line models of ERBB2-amplified breast cancer attenuates response towards ERBB2-targeting drugs. Oncogenesis 1, (7), 1-14.
27. Pagni, M.; Ioannidis, V.; Cerutti, L.; Zahn-Zabal, M.; Jongeneel, C. V.; Hau, J.; Martin, O.; Kuznetsov, D.; Falquet, L. MyHits: improvements to an interactive resource for analyzing protein sequences Nucleic Acids Res. 2007, 35 (suppl-2) W433-437
28. Fanayan, S.; Smith, J. T.; Lee, L. Y.; Yan, F.; Snyder, M.; Hancock, W. S.; Nice, E. Proteogenomic Analysis of Human Colon Carcinoma Cell Lines LIM1215, LIM1899, and LIM2405 J. Proteome Res. 2013, 12 (4) 1732-1742
29. Ning, K.; Nesvizhskii, A. I. The utility of mass spectrometry-based proteomic data for validation of novel alternative splice forms reconstructed from RNA-Seq data: a preliminary assessment BMC Bioinf. 2010, 11 (Suppl 11) S14
30. Goedert, M.; Jakes, R. Expression of separate isoforms of human tau protein: correlation with the tau pattern in brain and effects on tubulin polymerization EMBO J. 1990, 9 (13) 4225-30
31. Hutton, M.; Lendon, C. L.; Rizzu, P.; Baker, M.; Froelich, S.; Houlden, H.; Pickering-Brown, S.; Chakraverty, S.; Isaacs, A.; Grover, A.; Hackett, J.; Adamson, J.; Lincoln, S.; Dickson, D.; Davies, P.; Petersen, R. C.; Stevens, M.; de Graaff, E.; Wauters, E.; van Baren, J.; Hillebrand, M.; Joosse, M.; Kwon, J. M.; Nowotny, P.; Che, L. K.; Norton, J.; Morris, J. C.; Reed, L. A.; Trojanowski, J.; Basun, H.; Lannfelt, L.; Neystat, M.; Fahn, S.; Dark, F.; Tannenberg, T.; Dodd, P. R.; Hayward, N.; Kwok, J. B.; Schofield, P. R.; Andreadis, A.; Snowden, J.; Craufurd, D.; Neary, D.; Owen, F.; Oostra, B. A.; Hardy, J.; Goate, A.; van Swieten, J.; Mann, D.; Lynch, T.; Heutink, P. Association of missense and 5′-splice-site mutations in tau with the inherited dementia FTDP-17 Nature 1998, 393 (6686) 702-5
32. Gupta, P.; Srivastava, S. K. Antitumor activity of phenethyl isothiocyanate in HER2-positive breast cancer models BMC Med. 2012, 10 (80) 1-18
33. Henjes, F.; Bender, C.; von der Heyde, S.; Braun, L.; Mannsperger, H. A.; Schmidt, C.; Wiemann, S.; Hasmann, M.; Aulmann, S.; Beissbarth, T.; Korf, U. Strong EGFR signaling in cell line models of ERBB2-amplified breast cancer attenuates response towards ERBB2-targeting drugs Oncogenesis 2012, 1, 1-9
34. Marcotte, R.; Zhou, L.; Kim, H.; Roskelly, C. D.; Muller, W. J. c-Src associates with ErbB2 through an interaction between catalytic domains and confers enhanced transforming potential Mol. Cell. Biol. 2009, 29 (21) 5858-71
35. Nagy, P.; Vereb, G.; Sebestyen, Z.; Horvath, G.; Lockett, S. J.; Damjanovich, S.; Park, J. W.; Jovin, T. M.; Szollosi, J. Lipid rafts and the local density of ErbB proteins influence the biological role of homo- and heteroassociations of ErbB2 J. Cell Sci. 2002, 115 (22) 4251-4262
36. Adesso, L.; Calabretta, S.; Barbagallo, F.; Capurso, G.; Pilozzi, E.; Geremia, R.; Delle Fave, G.; Sette, C. Gemcitabine triggers a pro-survival response in pancreatic cancer cells through activation of the MNK2/eIF4E pathway Oncogene 2013, 32 (23) 2848-57
37. Unruh, D.; Turner, K.; Srinivasan, R.; Kocaturk, B.; Qi, X.; Chu, Z.; Aronow, B. J.; Plas, D. R.; Gallo, C. A.; Kalthoff, H.; Kirchhofer, D.; Ruf, W.; Ahmad, S. A.; Lucas, F. V.; Versteeg, H. H.; Bogdanov, V. Y. Alternatively spliced tissue factor contributes to tumor spread and activation of coagulation in pancreatic ductal adenocarcinoma Int. J. Cancer 2013, 134, 9-20
38. Cataldo, F.; Peche, L. Y.; Klaric, E.; Brancolini, C.; Myers, M. P.; Demarchi, F.; Schneider, C. CAPNS1 Regulates USP1 Stability and Maintenance of Genome Integrity Mol. Cell. Biol. 2013, 33 (12) 2485-96
39. Stewart, M. P.; McDowall, A.; Hogg, N. LFA-1-mediated adhesion is regulated by cytoskeletal restraint and by a Ca2+-dependent protease, calpain J. Cell Biol. 1998, 140 (3) 699-707
40. Shao, H.; Chou, J.; Baty, C. J.; Burke, N. A.; Watkins, S. C.; Stolz, D. B.; Wells, A. Spatial localization of m-calpain to the plasma membrane by phosphoinositide biphosphate binding during epidermal growth factor receptor-mediated activation Mol. Cell. Biol. 2006, 26 (14) 5481-96
41. Ngan, E.; Northey, J. J.; Brown, C. M.; Ursini-Siegel, J.; Siegel, P. M. A complex containing LPP and alpha-actinin mediates TGFbeta-induced migration and invasion of ErbB2-expressing breast cancer cells J. Cell Sci. 2013, 126 (Pt 9) 1981-91
42. Lahlou, H.; Muller, W. J. beta1-integrins signaling and mammary tumor progression in transgenic mouse models: implications for human breast cancer Breast Cancer Res. 2011, 13 (6) 229
43. Huck, L.; Pontier, S. M.; Zuo, D. M.; Muller, W. J. beta1-integrin is dispensable for the induction of ErbB2 mammary tumors but plays a critical role in the metastatic phase of tumor progression Proc. Natl. Acad. Sci. U. S. A. 2010, 107 (35) 15559-64
44. O'Keefe, R. T. Mutations in U5 snRNA loop 1 influence the splicing of different genes in vivo Nucleic Acids Res. 2002, 30 (24) 5476-84
45. Jin, Q.; Yuan, L. X.; Boulbes, D.; Baek, J. M.; Wang, Y. N.; Gomez-Cabello, D.; Hawke, D. H.; Yeung, S. C.; Lee, M. H.; Hortobagyi, G. N.; Hung, M. C.; Esteva, F. J. Fatty acid synthase phosphorylation: a novel therapeutic target in HER2-overexpressing breast cancer cells Breast Cancer Res. 2010, 12 (6) 1-18
46. Mani, A.; Gelmann, E. P. The ubiquitin-proteasome pathway and its role in cancer J. Clin. Oncol. 2005, 23 (21) 4776-89
47. Serce, N. B.; Boesl, A.; Klaman, I.; von Serenyi, S.; Noetzel, E.; Press, M. F.; Dimmler, A.; Hartmann, A.; Sehouli, J.; Knuechel, R.; Beckmann, M. W.; Fasching, P. A.; Dahl, E. Overexpression of SERBP1 (Plasminogen activator inhibitor 1 RNA binding protein) in human breast cancer is correlated with favourable prognosis BMC Cancer 2012, 12, 597
48. Deng, S. S.; Xing, T. Y.; Zhou, H. Y.; Xiong, R. H.; Lu, Y. G.; Wen, B.; Liu, S. Q.; Yang, H. J. Comparative proteome analysis of breast cancer and adjacent normal breast tissues in human Genomics, Proteomics Bioinf. 2006, 4 (3) 165-72
49. Bhavani, V.; Srinivasulu, M.; Ahuja, Y. R.; Hasan, Q. Role of BRCA1, HSD17B1 and HSD17B2 methylation in breast cancer tissue Cancer Biomarkers 2009, 5 (4) 207-13
50. Nordgard, S. H.; Johansen, F. E.; Alnaes, G. I.; Bucher, E.; Syvanen, A. C.; Naume, B.; Borresen-Dale, A. L.; Kristensen, V. N. Genome-wide analysis identifies 16q deletion associated with survival, molecular subtypes, mRNA expression, and germline haplotypes in breast cancer patients Genes, Chromosomes Cancer 2008, 47 (8) 680-96