Differential proteome analysis identifies TGF-β-related pro-metastatic proteins in a 4T1 murine breast cancer model

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Sato, Misako ^a,b   Matsubara, Tsutomu ^b   Adachi, Jun ^a   Hashimoto, Yuuki ^a   Fukamizu, Kazuna ^a   Kishida, Marina ^a   Yang, Yu An ^c   Wakefield, Lalage M ^c   Tomonaga, Takeshi ^a  

^a National Institute of Biomedical Innovation   (Japan)

^b OSAKA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 [4 (1,3 BENZODIOXOL 5 YL) 5 (2 PYRIDINYL) 1H IMIDAZOL 2 YL]BENZAMIDE; INITIATION FACTOR; INITIATION FACTOR 2; INITIATION FACTOR 4A1; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; 1,3 DIOXOLANE DERIVATIVE; 4-(5-BENZO(1,3)DIOXOL-5-YL-4-PYRIDIN-2-YL-1H-IMIDAZOL-2-YL)BENZAMIDE; BENZAMIDE DERIVATIVE; PROTEOME; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; TUMOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ARTICLE; BREAST CANCER; CONTROLLED STUDY; DOWN REGULATION; DRUG TARGETING; FEMALE; IMMUNOHISTOCHEMISTRY; LUNG METASTASIS; METASTASIS INHIBITION; METASTASIS POTENTIAL; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEOMICS; QUANTITATIVE ANALYSIS; TANDEM MASS SPECTROMETRY; UPREGULATION; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; HUMAN; LUNG NEOPLASMS; MAMMARY NEOPLASMS, EXPERIMENTAL; METABOLISM; SECONDARY; TUMOR CELL LINE;

EUKARYOTA; MURINAE; MUS;

ANIMALS; BENZAMIDES; CELL LINE, TUMOR; DIOXOLES; EUKARYOTIC INITIATION FACTORS; FEMALE; HUMANS; LUNG NEOPLASMS; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, INBRED BALB C; NEOPLASM PROTEINS; PROTEOME; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA;

EID: 84930626851     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0126483     Document Type: Article

References (48)

1. Sotiriou C, Piccart MJ (2007) Taking gene-expression profiling to the clinic: when will molecular signatures become relevant to patient care? Nat Rev Cancer 7: 545-553. PMID: 17585334
2. Weigelt B, Peterse JL, van 't Veer LJ (2005) Breast cancer metastasis: markers and models. Nat Rev Cancer 5: 591-602. PMID: 16056258
3. O'Shaughnessy J (2005) Extending survival with chemotherapy in metastatic breast cancer. Oncologist 10 Suppl 3: 20-29. PMID: 16368868
4. Massague J (2008) TGFbeta in Cancer. Cell 134: 215-230. doi: 10.1016/j.cell.2008.07.001 PMID: 18662538
5. Roberts AB, Wakefield LM (2003) The two faces of transforming growth factor beta in carcinogenesis. Proc Natl Acad Sci U S A 100: 8621-8623. PMID: 12861075
6. Wakefield LM, Hill CS (2013) Beyond TGFbeta: roles of other TGFbeta superfamily members in cancer. Nat Rev Cancer 13: 328-341. doi: 10.1038/nrc3500 PMID: 23612460
7. Akhurst RJ, Hata A (2012) Targeting the TGFbeta signalling pathway in disease. Nat Rev Drug Discov 11: 790-811. doi: 10.1038/nrd3810 PMID: 23000686
8. Bonafoux D, Lee WC (2009) Strategies for TGF-beta modulation: a review of recent patents. Expert Opin Ther Pat 19: 1759-1769. doi: 10.1517/13543770903397400 PMID: 19939191
9. Yingling JM, Blanchard KL, Sawyer JS (2004) Development of TGF-beta signalling inhibitors for cancer therapy. Nat Rev Drug Discov 3: 1011-1022. PMID: 15573100
10. Bao L, Haque A, Jackson K, Hazari S, Moroz K, Jetly R, et al. (2011) Increased expression of P-glycoprotein is associated with doxorubicin chemoresistance in the metastatic 4T1 breast cancer model. Am J Pathol 178: 838-852. doi: 10.1016/j.ajpath.2010.10.029 PMID: 21281816
11. Tao K, Fang M, Alroy J, Sahagian GG (2008) Imagable 4T1 model for the study of late stage breast cancer. BMC Cancer 8: 228. doi: 10.1186/1471-2407-8-228 PMID: 18691423
12. Issa A, Gill JW, Heideman MR, Sahin O, Wiemann S, Dey JH, et al. (2013) Combinatorial targeting of FGF and ErbB receptors blocks growth and metastatic spread of breast cancer models. Breast Cancer Res 15: R8. doi: 10.1186/bcr3379 PMID: 23343422
13. Nam JS, Suchar AM, Kang MJ, Stuelten CH, Tang B, Michalowska AM, et al. (2006) Bone sialoprotein mediates the tumor cell-targeted prometastatic activity of transforming growth factor beta in a mouse model of breast cancer. Cancer Res 66: 6327-6335. PMID: 16778210
14. Nam JS, Terabe M, Mamura M, Kang MJ, Chae H, Stuelten C, et al. (2008) An anti-transforming growth factor beta antibody suppresses metastasis via cooperative effects on multiple cell compartments. Cancer Res 68: 3835-3843. doi: 10.1158/0008-5472.CAN-08-0215 PMID: 18483268
15. Ho J, Kong JW, Choong LY, Loh MC, Toy W, Chong PK, et al. (2009) Novel breast cancer metastasis-associated proteins. J Proteome Res 8: 583-594. doi: 10.1021/pr8007368 PMID: 19086899
16. Xue T, Zhang Y, Zhang L, Yao L, Hu X, Xu LX (2013) Proteomic Analysis of Two Metabolic Proteins with Potential to Translocate to Plasma Membrane Associated with Tumor Metastasis Development and Drug Targets. J Proteome Res.
17. Ali NA, Molloy MP (2011) Quantitative phosphoproteomics of transforming growth factor-beta signaling in colon cancer cells. Proteomics 11: 3390-3401. doi: 10.1002/pmic.201100036 PMID: 21751366
18. Souchelnytskyi S (2005) Proteomics of TGF-beta signaling and its impact on breast cancer. Expert Rev Proteomics 2: 925-935. PMID: 16307521
19. Aslakson CJ, Miller FR (1992) Selective events in the metastatic process defined by analysis of the sequential dissemination of subpopulations of a mouse mammary tumor. Cancer Res 52: 1399-1405. PMID: 1540948
20. Halder SK, Beauchamp RD, Datta PK (2005) A specific inhibitor of TGF-beta receptor kinase, SB-431542, as a potent antitumor agent for human cancers. Neoplasia 7: 509-521. PMID: 15967103
21. Laping NJ, Grygielko E, Mathur A, Butter S, Bomberger J, Tweed C, et al. (2002) Inhibition of transforming growth factor (TGF)-beta1-induced extracellular matrix with a novel inhibitor of the TGF-beta type I receptor kinase activity: SB-431542. Mol Pharmacol 62: 58-64. PMID: 12065755
22. Tanaka H, Shinto O, Yashiro M, Yamazoe S, Iwauchi T, Muguruma K, et al. (2010) Transforming growth factor beta signaling inhibitor, SB-431542, induces maturation of dendritic cells and enhances anti-tumor activity. Oncol Rep 24: 1637-1643. PMID: 21042762
23. Masuda T, Tomita M, Ishihama Y (2008) Phase transfer surfactant-aided trypsin digestion for membrane proteome analysis. J Proteome Res 7: 731-740. doi: 10.1021/pr700658q PMID: 18183947
24. Rappsilber J, Mann M, Ishihama Y (2007) Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat Protoc 2: 1896-1906. PMID: 17703201
25. Boersema PJ, Raijmakers R, Lemeer S, Mohammed S, Heck AJ (2009) Multiplex peptide stable isotope dimethyl labeling for quantitative proteomics. Nat Protoc 4: 484-494. doi: 10.1038/nprot.2009.21 PMID: 19300442
26. Muraoka S, Kume H, Watanabe S, Adachi J, Kuwano M, Sato M, et al. (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. doi: 10.1021/pr300322q PMID: 22716024
27. Narumi R, Murakami T, Kuga T, Adachi J, Shiromizu T, Muraoka S, et al. (2012) A strategy for largescale phosphoproteomics and SRM-based validation of human breast cancer tissue samples. J Proteome Res 11: 5311-5322. doi: 10.1021/pr3005474 PMID: 22985185
28. Shiromizu T, Adachi J, Watanabe S, Murakami T, Kuga T, Muraoka S, et al. (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 12: 2414-2421. doi: 10.1021/pr300825v PMID: 23312004
29. Matsubara T, Tanaka N, Krausz KW, Manna SK, Kang DW, Anderson ER, et al. (2012) Metabolomics identifies an inflammatory cascade involved in dioxin- and diet-induced steatohepatitis. Cell Metab 16: 634-644. doi: 10.1016/j.cmet.2012.10.006 PMID: 23140643
30. Muraoka RS, Dumont N, Ritter CA, Dugger TC, Brantley DM, Chen J, et al. (2002) Blockade of TGF-beta inhibits mammary tumor cell viability, migration, and metastases. J Clin Invest 109: 1551-1559. PMID: 12070302
31. Konicek BW, Dumstorf CA, Graff JR (2008) Targeting the eIF4F translation initiation complex for cancer therapy. Cell Cycle 7: 2466-2471. PMID: 18719377
32. Ramirez-Valle F, Braunstein S, Zavadil J, Formenti SC, Schneider RJ (2008) eIF4GI links nutrient sensing by mTOR to cell proliferation and inhibition of autophagy. J Cell Biol 181: 293-307. doi: 10.1083/jcb.200710215 PMID: 18426977
33. Yellen P, Chatterjee A, Preda A, Foster DA (2013) Inhibition of S6 kinase suppresses the apoptotic effect of eIF4E ablation by inducing TGF-beta-dependent G1 cell cycle arrest. Cancer Lett 333: 239-243. doi: 10.1016/j.canlet.2013.01.041 PMID: 23376634
34. Silvera D, Formenti SC, Schneider RJ (2010) Translational control in cancer. Nat Rev Cancer 10: 254-266. doi: 10.1038/nrc2824 PMID: 20332778
35. Gilles C, Polette M, Zahm JM, Tournier JM, Volders L, Foidart JM, et al. (1999) Vimentin contributes to human mammary epithelial cell migration. J Cell Sci 112 (Pt 24): 4615-4625. PMID: 10574710
36. Nagaraja GM, Kaur P, Neumann W, Asea EE, Bausero MA, Multhoff G, et al. (2012) Silencing Hsp25/Hsp27 gene expression augments proteasome activity and increases CD8+ T-cell-mediated tumor killing and memory responses. Cancer Prev Res (Phila) 5: 122-137. doi: 10.1158/1940-6207.CAPR-11-0121 PMID: 22185976
37. Jackson RJ, Hellen CU, Pestova TV (2010) The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol 11: 113-127. doi: 10.1038/nrm2838 PMID: 20094052
38. Nasr Z, Robert F, Porco JA Jr., Muller WJ, Pelletier J (2013) eIF4F suppression in breast cancer affects maintenance and progression. Oncogene 32: 861-871. doi: 10.1038/onc.2012.105 PMID: 22484424
39. De Benedetti A, Graff JR (2004) eIF-4E expression and its role in malignancies and metastases. Oncogene 23: 3189-3199. PMID: 15094768
40. de la Parra C, Otero-Franqui E, Martinez-Montemayor M, Dharmawardhane S (2012) The soy isoflavone equol may increase cancer malignancy via up-regulation of eukaryotic protein synthesis initiation factor eIF4G. J Biol Chem 287: 41640-41650. doi: 10.1074/jbc.M112.393470 PMID: 23095751
41. Silvera D, Arju R, Darvishian F, Levine PH, Zolfaghari L, Goldberg J, et al. (2009) Essential role for eIF4GI overexpression in the pathogenesis of inflammatory breast cancer. Nat Cell Biol 11: 903-908. doi: 10.1038/ncb1900 PMID: 19525934
42. Badura M, Braunstein S, Zavadil J, Schneider RJ (2012) DNA damage and eIF4G1 in breast cancer cells reprogram translation for survival and DNA repair mRNAs. Proc Natl Acad Sci U S A 109: 18767-18772. doi: 10.1073/pnas.1203853109 PMID: 23112151
43. Lou Y, Preobrazhenska O, auf dem Keller U, Sutcliffe M, Barclay L, McDonald PC, et al. (2008) Epithelial-mesenchymal transition (EMT) is not sufficient for spontaneous murine breast cancer metastasis. Dev Dyn 237: 2755-2768. doi: 10.1002/dvdy.21658 PMID: 18773493
44. Lamouille S, Derynck R (2007) Cell size and invasion in TGF-beta-induced epithelial to mesenchymal transition is regulated by activation of the mTOR pathway. J Cell Biol 178: 437-451. PMID: 17646396
45. Das F, Ghosh-Choudhury N, Bera A, Kasinath BS, Choudhury GG (2013) TGFbeta-induced PI 3 kinase-dependent Mnk-1 activation is necessary for Ser-209 phosphorylation of eIF4E and mesangial cell hypertrophy. J Cell Physiol 228: 1617-1626. doi: 10.1002/jcp.24327 PMID: 23359369
46. Inman GJ, Nicolas FJ, Callahan JF, Harling JD, Gaster LM, Reith AD, et al. (2002) SB-431542 is a potent and specific inhibitor of transforming growth factor-beta superfamily type I activin receptor-like kinase (ALK) recepotrs ALK4, ALK5, and ALK7. Mol Parmacol 62: 65-74.
47. Hjelmeland MD, Hjelmeland AB, Sathornsumetee S, Reese ED, Herbstreith MH, Laping NJ, et al. (2004) SB-431542, a small molecule transforming growth factor-beta-receptor antagonist, inhibits human glioma cell line proliferation and motility. Mol Cancer Ther 3: 737-745. PMID: 15210860
48. Matsuyama S, Iwadate M, Kondo M, Saitoh M, Hanyu A, Shimizu K, et al. (2003) SB-431542 and Gleevec inhibit transforming growth factor-beta-induced proliferation of human osteosarcoma cells. Cancer Res 63: 7791-7798. PMID: 14633705