Tumor-associated myoepithelial cells promote the invasive progression of ductal carcinoma in situ through activation of TGFβ signaling

Journal of Biological Chemistry

Volumn 292, Issue 27, 2017, Pages 11466-11484

  Lo, Pang Kuo ^a   Zhang, Yongshu ^a   Yao, Yuan ^a   Wolfson, Benjamin ^a   Yu, Justine ^a   Han, Shu Yan ^a,b   Duru, Nadire ^a   Zhou, Qun ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b PEKING UNIVERSITY CANCER HOSPITAL AND INSTITUTE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; CHEMICAL ACTIVATION; CYTOLOGY; TUMORS;

CELL-CELL INTERACTION; DUCTAL CARCINOMA IN SITU; EPITHELIAL-MESENCHYMAL TRANSITION; EXPERIMENTAL EVIDENCE; INVASIVE DUCTAL CARCINOMATA; MECHANISTIC STUDIES; SIGNALING PATHWAYS; TUMOR SUPPRESSOR GENES;

CELL SIGNALING;

MICRORNA 10B; SMAD PROTEIN; TRANSFORMING GROWTH FACTOR BETA1; MICRORNA; RNA; TRANSFORMING GROWTH FACTOR BETA; TUMOR PROTEIN;

ARTICLE; BREAST CARCINOMA; CANCER GROWTH; CELL FUNCTION; CELL INTERACTION; CELL STIMULATION; COCULTURE; CONTROLLED STUDY; CYTOKINE RELEASE; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; GENE INDUCTION; HUMAN; HUMAN CELL; IN VITRO STUDY; INTRADUCTAL CARCINOMA; MYOEPITHELIUM CELL; PHENOTYPE; PRIORITY JOURNAL; RB1CC1 GENE; SIGNAL TRANSDUCTION; TUMOR ASSOCIATED MYOEPITHELIUM CELL; TUMOR INVASION; TUMOR SUPPRESSOR GENE; TUMOR XENOGRAFT; ANIMAL; BONE MARROW CELL; BREAST TUMOR; CANCER TRANSPLANTATION; EPITHELIUM CELL; FEMALE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOUSE; NUDE MOUSE; PATHOLOGY; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; BREAST NEOPLASMS; CARCINOMA, INTRADUCTAL, NONINFILTRATING; CELL LINE, TUMOR; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HETEROGRAFTS; HUMANS; MICE; MICE, NUDE; MICRORNAS; MYELOID CELLS; NEOPLASM INVASIVENESS; NEOPLASM PROTEINS; NEOPLASM TRANSPLANTATION; RNA, NEOPLASM; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 85023625821     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M117.775080     Document Type: Article

References (67)

1. Siegel, R. L., Miller, K. D., and Jemal, A. (2017) Cancer statistics, 2017. CA Cancer J. Clin. 67, 7–30
2. Kerlikowske, K., Molinaro, A., Cha, I., Ljung, B. M., Ernster, V. L., Stewart, K., Chew, K., Moore, D. H., 2nd, and Waldman, F. (2003) Characteristics associated with recurrence among women with ductal carcinoma in situ treated by lumpectomy. J. Natl. Cancer Inst. 95, 1692–1702
3. Chin, K., de Solorzano, C. O., Knowles, D., Jones, A., Chou, W., Rodriguez, E. G., Kuo, W. L., Ljung, B. M., Chew, K., Myambo, K., Miranda, M., Krig, S., Garbe, J., Stampfer, M., Yaswen, P., et al. (2004) In situ analyses of genome instability in breast cancer. Nat. Genet. 36, 984–988
4. Ma, X. J., Salunga, R., Tuggle, J. T., Gaudet, J., Enright, E., McQuary, P., Payette, T., Pistone, M., Stecker, K., Zhang, B. M., Zhou, Y. X., Varnholt, H., Smith, B., Gadd, M., Chatfield, E., et al. (2003) Gene expression profiles of human breast cancer progression. Proc. Natl. Acad. Sci. U.S.A. 100, 5974–5979
5. Yao, J., Weremowicz, S., Feng, B., Gentleman, R. C., Marks, J. R., Gelman, R., Brennan, C., and Polyak, K. (2006) Combined cDNA array comparative genomic hybridization and serial analysis of gene expression analysis of breast tumor progression. Cancer Res. 66, 4065–4078
6. Bissell, M. J., Kenny, P. A., and Radisky, D. C. (2005) Microenvironmental regulators of tissue structure and function also regulate tumor induction and progression: the role of extracellular matrix and its degrading enzymes. Cold Spring Harb. Symp. Quant. Biol. 70, 343–356
7. Weinberg, R., and Mihich, E. (2006) Eighteenth annual pezcoller symposium: tumor microenvironment and heterotypic interactions. Cancer Res. 66, 11550–11553
8. Sternlicht, M. D., Kedeshian, P., Shao, Z. M., Safarians, S., and Barsky, S. H. (1997) The human myoepithelial cell is a natural tumor suppressor. Clin. Cancer Res. 3, 1949–1958
9. Barsky, S. H., and Karlin, N. J. (2005) Myoepithelial cells: autocrine and paracrine suppressors of breast cancer progression. J. Mammary Gland Biol. Neoplasia 10, 249–260
10. Hu, M., Yao, J., Carroll, D. K., Weremowicz, S., Chen, H., Carrasco, D., Richardson, A., Violette, S., Nikolskaya, T., Nikolsky, Y., Bauerlein, E. L., Hahn, W. C., Gelman, R. S., Allred, C., Bissell, M. J., et al. (2008) Regulation of in situ to invasive breast carcinoma transition. Cancer Cell 13, 394–406
11. Cowell, C. F., Weigelt, B., Sakr, R. A., Ng, C. K. Y., Hicks, J., King, T. A., and Reis-Filho, J. S. (2013) Progression from ductal carcinoma in situ to invasive breast cancer: revisited. Mol. Oncol. 7, 859–869
12. Gudjonsson, T., Rønnov-Jessen, L., Villadsen, R., Rank, F., Bissell, M. J., and Petersen, O. W. (2002) Normal and tumor-derived myoepithelial cells differ in their ability to interact with luminal breast epithelial cells for polarity and basement membrane deposition. J. Cell Sci. 115, 39–50
13. Allinen, M., Beroukhim, R., Cai, L., Brennan, C., Lahti-Domenici, J., Huang, H., Porter, D., Hu, M., Chin, L., Richardson, A., Schnitt, S., Sellers, W. R., and Polyak, K. (2004) Molecular characterization of the tumor microenvironment in breast cancer. Cancer Cell 6, 17–32
14. Allen, M. D., Marshall, J. F., and Jones, J. L. (2014) vβ6 expression in myoepithelial cells: a novel marker for predicting DCIS progression with therapeutic potential. Cancer Res. 74, 5942–5947
15. Allen, M. D., Thomas, G. J., Clark, S., Dawoud, M. M., Vallath, S., Payne, S. J., Gomm, J. J., Dreger, S. A., Dickinson, S., Edwards, D. R., Pennington, C. J., Sestak, I., Cuzick, J., Marshall, J. F., Hart, I. R., and Jones, J. L. (2014) Altered microenvironment promotes progression of preinvasive breast cancer: myoepithelial expression of αvβ6 integrin in DCIS identifies high-risk patients and predicts recurrence. Clin. Cancer Res. 20, 344–357
16. Yang, J., and Weinberg, R. A. (2008) Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev. Cell 14, 818–829
17. Lu, J., Guo, H., Treekitkarnmongkol, W., Li, P., Zhang, J., Shi, B., Ling, C., Zhou, X., Chen, T., Chiao, P. J., Feng, X., Seewaldt, V. L., Muller, W. J., Sahin, A., Hung, M. C., and Yu, D. (2009) 14-3-3ζ cooperates with ErbB2 to promote ductal carcinoma in situ progression to invasive breast cancer by inducing epithelial-mesenchymal transition. Cancer Cell 16, 195–207
18. Mani, S. A., Guo, W., Liao, M. J., Eaton, E. N., Ayyanan, A., Zhou, A. Y., Brooks, M., Reinhard, F., Zhang, C. C., Shipitsin, M., Campbell, L. L., Polyak, K., Brisken, C., Yang, J., and Weinberg, R. A. (2008) The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133, 704–715
19. Bartel, D. P. (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281–297
20. Liz, J., and Esteller, M. (2016) lncRNAs and microRNAs with a role in cancer development. Biochim. Biophys. Acta 1859, 169–176
21. Volinia, S., Galasso, M., Sana, M. E., Wise, T. F., Palatini, J., Huebner, K., and Croce, C. M. (2012) Breast cancer signatures for invasiveness and prognosis defined by deep sequencing of microRNA. Proc. Natl. Acad. Sci. U.S.A. 109, 3024–3029
22. Mardekian, S. K., Bombonati, A., and Palazzo, J. P. (2016) Ductal carcinoma in situ of the breast: the importance of morphologic and molecular interactions. Hum. Pathol. 49, 114–123
23. Blahna, M. T., and Hata, A. (2013) Regulation of miRNA biogenesis as an integrated component of growth factor signaling. Curr. Opin. Cell Biol. 25, 233–240
24. Gregory, P. A., Bracken, C. P., Bert, A. G., and Goodall, G. J. (2008) MicroRNAs as regulators of epithelial-mesenchymal transition. Cell Cycle 7, 3112–3118
25. Sivadas, V. P., and Kannan, S. (2014) The microRNA networks of TGFβ signaling in cancer. Tumour Biol. 35, 2857–2869
26. Miller, F. R., Santner, S. J., Tait, L., and Dawson, P. J. (2000) MCF10DCIS.com xenograft model of human comedo ductal carcinoma in situ. J. Natl. Cancer Inst. 92, 1185–1186
27. Hackett, A. J., Smith, H. S., Springer, E. L., Owens, R. B., Nelson-Rees, W. A., Riggs, J. L., and Gardner, M. B. (1977) Two syngeneic cell lines from human breast tissue: the aneuploid mammary epithelial (Hs578T) and the diploid myoepithelial (Hs578Bst) cell lines. J. Natl. Cancer Inst. 58, 1795–1806
28. Thiery, J. P., Acloque, H., Huang, R. Y., and Nieto, M. A. (2009) Epithelial-mesenchymal transitions in development and disease. Cell 139, 871–890
29. Lamouille, S., Xu, J., and Derynck, R. (2014) Molecular mechanisms of epithelial-mesenchymal transition. Nat. Rev. Mol. Cell Biol. 15, 178–196
30. Inman, G. J., Nicolás, F. J., Callahan, J. F., Harling, J. D., Gaster, L. M., Reith, A. D., Laping, N. J., and Hill, C. S. (2002) SB-431542 is a potent and specific inhibitor of transforming growth factor-β superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7. Mol. Pharmacol. 62, 65–74
31. Takahashi, H., Kanno, T., Nakayamada, S., Hirahara, K., Sciumè, G., Muljo, S. A., Kuchen, S., Casellas, R., Wei, L., Kanno, Y., and O’Shea, J. J. (2012) TGF-β and retinoic acid induce the microRNA miR-10a, which targets Bcl-6 and constrains the plasticity of helper T cells. Nat. Immunol. 13, 587–595
32. Han, X., Yan, S., Weijie, Z., Feng, W., Liuxing, W., Mengquan, L., and Qingxia, F. (2014) Critical role of miR-10b in transforming growth factor-β1-induced epithelial-mesenchymal transition in breast cancer. Cancer Gene Ther. 21, 60–67
33. Mayorga, M. E., and Penn, M. S. (2012) miR-145 is differentially regulated by TGF-β1 and ischaemia and targets Disabled-2 expression and wnt/β-catenin activity. J. Cell Mol. Med. 16, 1106–1113
34. Lino Cardenas, C. L., Henaoui, I. S., Courcot, E., Roderburg, C., Cauffiez, C., Aubert, S., Copin, M. C., Wallaert, B., Glowacki, F., Dewaeles, E., Milosevic, J., Maurizio, J., Tedrow, J., Marcet, B., Lo-Guidice, J. M., et al. (2013) miR-199a-5p Is upregulated during fibrogenic response to tissue injury and mediates TGFβ-induced lung fibroblast activation by targeting caveolin-1. PLoS Genet. 9, e1003291
35. Gregory, P. A., Bert, A. G., Paterson, E. L., Barry, S. C., Tsykin, A., Farshid, G., Vadas, M. A., Khew-Goodall, Y., and Goodall, G. J. (2008) The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat. Cell Biol. 10, 593–601
36. - single-cell derived stem cell population in basal-like DCIS cells. Oncotarget 7, 47511–47525
37. John, B., Enright, A. J., Aravin, A., Tuschl, T., Sander, C., and Marks, D. S. (2004) Human microRNA targets. PLoS Biol. 2, e363
38. Krek, A., Grün, D., Poy, M. N., Wolf, R., Rosenberg, L., Epstein, E. J., MacMenamin, P., da Piedade, I., Gunsalus, K. C., Stoffel, M., and Rajewsky, N. (2005) Combinatorial microRNA target predictions. Nat. Genet. 37, 495–500
39. Agarwal, V., Bell, G. W., Nam, J. W., and Bartel, D. P. (2015) Predicting effective microRNA target sites in mammalian mRNAs. Elife 4, 10.7554/eLife.05005
40. Lal, A., Thomas, M. P., Altschuler, G., Navarro, F., O’Day, E., Li, X. L., Concepcion, C., Han, Y. C., Thiery, J., Rajani, D. K., Deutsch, A., Hofmann, O., Ventura, A., Hide, W., and Lieberman, J. (2011) Capture of microRNA-bound mRNAs identifies the tumor suppressor miR-34a as a regulator of growth factor signaling. PLoS Genet. 7, e1002363
41. Chano, T., Kontani, K., Teramoto, K., Okabe, H., and Ikegawa, S. (2002) Truncating mutations of RB1CC1 in human breast cancer. Nat. Genet. 31, 285–288
42. Rhodes, D. R., Yu, J., Shanker, K., Deshpande, N., Varambally, R., Ghosh, D., Barrette, T., Pandey, A., and Chinnaiyan, A. M. (2004) ONCOMINE: a cancer microarray database and integrated data-mining platform. Neoplasia 6, 1–6
43. Esserman, L. J., Berry, D. A., Cheang, M. C., Yau, C., Perou, C. M., Carey, L., DeMichele, A., Gray, J. W., Conway-Dorsey, K., Lenburg, M. E., Buxton, M. B., Davis, S. E., van’t Veer, L. J., Hudis, C., Chin, K., et al. (2012) Chemotherapy response and recurrence-free survival in neoadjuvant breast cancer depends on biomarker profiles: results from the I-SPY 1 TRIAL (CALGB 150007/150012; ACRIN 6657). Breast Cancer Res. Treat. 132, 1049–1062
44. Tabchy, A., Valero, V., Vidaurre, T., Lluch, A., Gomez, H., Martin, M., Qi, Y., Barajas-Figueroa, L. J., Souchon, E., Coutant, C., Doimi, F. D., Ibrahim, N. K., Gong, Y., Hortobagyi, G. N., Hess, K. R., et al. (2010) Evaluation of a 30-gene paclitaxel, fluorouracil, doxorubicin, and cyclophosphamide chemotherapy response predictor in a multicenter randomized trial in breast cancer. Clin. Cancer Res. 16, 5351–5361
45. Shipitsin, M., Campbell, L. L., Argani, P., Weremowicz, S., Bloushtain-Qimron, N., Yao, J., Nikolskaya, T., Serebryiskaya, T., Beroukhim, R., Hu, M., Halushka, M. K., Sukumar, S., Parker, L. M., Anderson, K. S., Harris, L. N., et al. (2007) Molecular definition of breast tumor heterogeneity. Cancer Cell 11, 259–273
46. Choi, Y., Lee, H. J., Jang, M. H., Gwak, J. M., Lee, K. S., Kim, E. J., Kim, H. J., Lee, H. E., and Park, S. Y. (2013) Epithelial-mesenchymal transition increases during the progression of in situ to invasive basal-like breast cancer. Hum. Pathol. 44, 2581–2589
47. Zheng, X., Carstens, J. L., Kim, J., Scheible, M., Kaye, J., Sugimoto, H., Wu, C. C., LeBleu, V. S., and Kalluri, R. (2015) Epithelial-to-mesenchymal transition is dispensable for metastasis but induces chemoresistance in pancreatic cancer. Nature 527, 525–530
48. Fischer, K. R., Durrans, A., Lee, S., Sheng, J., Li, F., Wong, S. T., Choi, H., El Rayes, T., Ryu, S., Troeger, J., Schwabe, R. F., Vahdat, L. T., Altorki, N. K., Mittal, V., and Gao, D. (2015) Epithelial-to-mesenchymal transition is not required for lung metastasis but contributes to chemoresistance. Nature 527, 472–476
49. Ma, L., Teruya-Feldstein, J., and Weinberg, R. A. (2007) Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 449, 682–688
50. Ma, L., Reinhardt, F., Pan, E., Soutschek, J., Bhat, B., Marcusson, E. G., Teruya-Feldstein, J., Bell, G. W., and Weinberg, R. A. (2010) Therapeutic silencing of miR-10b inhibits metastasis in a mouse mammary tumor model. Nat. Biotechnol. 28, 341–347
51. Yigit, M. V., Ghosh, S. K., Kumar, M., Petkova, V., Kavishwar, A., Moore, A., and Medarova, Z. (2013) Context-dependent differences in miR-10b breast oncogenesis can be targeted for the prevention and arrest of lymph node metastasis. Oncogene 32, 1530–1538
52. Baffa, R., Fassan, M., Volinia, S., O’Hara, B., Liu, C. G., Palazzo, J. P., Gardiman, M., Rugge, M., Gomella, L. G., Croce, C. M., and Rosenberg, A. (2009) MicroRNA expression profiling of human metastatic cancers identifies cancer gene targets. J. Pathol. 219, 214–221
53. Fkih M’hamed, I., Privat, M., Ponelle, F., Penault-Llorca, F., Kenani, A., and Bignon, Y. J. (2015) Identification of miR-10b, miR-26a, miR-146a and miR-153 as potential triple-negative breast cancer biomarkers. Cell Oncol. 38, 433–442
54. Bahena-Ocampo, I., Espinosa, M., Ceballos-Cancino, G., Lizarraga, F., Campos-Arroyo, D., Schwarz, A., Garcia-Lopez, P., Maldonado, V., and Melendez-Zajgla, J. (2016) miR-10b expression in breast cancer stem cells supports self-renewal through negative PTEN regulation and sustained AKT activation. EMBO Rep. 17, 1081
55. Melkoumian, Z. K., Peng, X., Gan, B., Wu, X., and Guan, J. L. (2005) Mechanism of cell cycle regulation by FIP200 in human breast cancer cells. Cancer Res. 65, 6676–6684
56. Ikebuchi, K., Chano, T., Ochi, Y., Tameno, H., Shimada, T., Hisa, Y., and Okabe, H. (2009) RB1CC1 activates the promoter and expression of RB1 in human cancer. Int. J. Cancer 125, 861–867
57. Ochi, Y., Chano, T., Ikebuchi, K., Inoue, H., Isono, T., Arai, A., Tameno, H., Shimada, T., Hisa, Y., and Okabe, H. (2011) RB1CC1 activates the p16 promoter through the interaction with hSNF5. Oncol. Rep. 26, 805–812
58. Chano, T., Ikebuchi, K., Ochi, Y., Tameno, H., Tomita, Y., Jin, Y., Inaji, H., Ishitobi, M., Teramoto, K., Nishimura, I., Minami, K., Inoue, H., Isono, T., Saitoh, M., Shimada, T., Hisa, Y., and Okabe, H. (2010) RB1CC1 activates RB1 pathway and inhibits proliferation and cologenic survival in human cancer. PLoS One 5, e11404
59. Choi, J. D., Ryu, M., Ae Park, M., Jeong, G., and Lee, J. S. (2013) FIP200 inhibits β-catenin-mediated transcription by promoting APC-independent β-catenin ubiquitination. Oncogene 32, 2421–2432
60. Zhu, Y., Yang, R., McLenithan, J., Yu, D., Wang, H., Wang, Y., Singh, D., Olson, J., Sztalryd, C., Zhu, D., and Gong, D. W. (2015) Direct conversion of human myoblasts into brown-like adipocytes by engineered super-active PPAR. Obesity 23, 1014–1021
61. Lo, P. K., Zhang, Y., Wolfson, B., Gernapudi, R., Yao, Y., Duru, N., and Zhou, Q. (2016) Dysregulation of the BRCA1/long non-coding RNA NEAT1 signaling axis contributes to breast tumorigenesis. Oncotarget 7, 65067–65089
62. Zhu, W., Leber, B., and Andrews, D. W. (2001) Cytoplasmic O-glycosylation prevents cell surface transport of E-cadherin during apoptosis. EMBO J. 20, 5999–6007
63. Jensen, M. M., Jørgensen, J. T., Binderup, T., and Kjaer, A. (2008) Tumor volume in subcutaneous mouse xenografts measured by microCT is more accurate and reproducible than determined by 18F-FDG-microPET or external caliper. BMC Med. Imaging 8, 16
64. Eades, G., Yao, Y., Yang, M., Zhang, Y., Chumsri, S., and Zhou, Q. (2011) miR-200a regulates SIRT1 expression and epithelial to mesenchymal transition (EMT)-like transformation in mammary epithelial cells. J. Biol. Chem. 286, 25992–26002
65. Zdanov, S., Mandapathil, M., Abu Eid, R., Adamson-Fadeyi, S., Wilson, W., Qian, J., Carnie, A., Tarasova, N., Mkrtichyan, M., Berzofsky, J. A., Whiteside, T. L., and Khleif, S. N. (2016) Mutant KRAS conversion of conventional T cells into regulatory T cells. Cancer Immunol. Res. 4, 354–365
66. Wang, D., Olman, M. A., Stewart, J., Jr, Tipps, R., Huang, P., Sanders, P. W., Toline, E., Prayson, R. A., Lee, J., Weil, R. J., Palmer, C. A., Gillespie, G. Y., Liu, W. M., Pieper, R. O., Guan, J. L., and Gladson, C. L. (2011) Downregulation of FIP200 induces apoptosis of glioblastoma cells and microvascular endothelial cells by enhancing Pyk2 activity. PLoS One 6, e19629
67. Yue, P. Y., Leung, E. P., Mak, N. K., and Wong, R. N. (2010) A simplified method for quantifying cell migration/wound healing in 96-well plates. J. Biomol. Screen. 15, 427–433