Epidermal growth factor/heat shock protein 27 pathway regulates vasculogenic mimicry activity of breast cancer stem/progenitor cells

Biochimie

Volumn 104, Issue 1, 2014, Pages 117-126

  Lee, Che Hsin ^a   Wu, Yu Ting ^b   Hsieh, Hung Chun ^b   Yu, Yun ^b   Yu, Alice L ^c,d   Chang, Wen Wei ^b,e  

^a CHINA MEDICAL UNIVERSITY   (Taiwan)

^b CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

^c CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e CHUNG SHAN MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

Breast cancer; Cancer stem progenitor cells; Epidermal growth factor; Heat shock protein 27; Vasculogenic mimicry

Indexed keywords

EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; GEFITINIB; HEAT SHOCK PROTEIN 27; QUERCETIN; SHORT HAIRPIN RNA; SMALL INTERFERING RNA;

ARTICLE; BREAST CANCER; CANCER STEM CELL; CELL STRUCTURE; CONTROLLED STUDY; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; MICROVASCULAR ENDOTHELIAL CELL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TUMOR VASCULARIZATION; ANIMAL; BREAST TUMOR; CELL TRANSFORMATION; CHEMICALLY INDUCED; DRUG EFFECTS; FEMALE; METABOLISM; MOUSE; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; PHOSPHORYLATION; TUMOR CELL LINE;

ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; EPIDERMAL GROWTH FACTOR; FEMALE; HSP27 HEAT-SHOCK PROTEINS; HUMANS; MICE; NEOPLASTIC STEM CELLS; NEOVASCULARIZATION, PATHOLOGIC; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

EID: 84905445848     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2014.06.011     Document Type: Article

References (46)

1. P. Auguste, S. Lemiere, F. Larrieu-Lahargue, and A. Bikfalvi Molecular mechanisms of tumor vascularization Crit Rev. Oncol. Hematol. 54 2005 53 61
2. P. Carmeliet, and R.K. Jain Molecular mechanisms and clinical applications of angiogenesis Nature 473 2011 298 307
3. R.E. Seftor, A.R. Hess, E.A. Seftor, D.A. Kirschmann, K.M. Hardy, N.V. Margaryan, and M.J. Hendrix Tumor cell vasculogenic mimicry: from controversy to therapeutic promise Am. J. Pathol. 181 2012 1115 1125
4. A.J. Maniotis, R. Folberg, A. Hess, E.A. Seftor, L.M. Gardner, J. Pe'er, J.M. Trent, P.S. Meltzer, and M.J. Hendrix Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry Am. J. Pathol. 155 1999 739 752
5. D.A. Kirschmann, E.A. Seftor, K.M. Hardy, R.E. Seftor, and M.J. Hendrix Molecular pathways: vasculogenic mimicry in tumor cells: diagnostic and therapeutic implications Clin. Cancer Res. 18 2012 2726 2732
6. G.D. Basu, W.S. Liang, D.A. Stephan, L.T. Wegener, C.R. Conley, B.A. Pockaj, and P. Mukherjee A novel role for cyclooxygenase-2 in regulating vascular channel formation by human breast cancer cells Breast Cancer Res. 8 2006 R69
7. T. Liu, B. Sun, X. Zhao, Q. Gu, X. Dong, Z. Yao, N. Zhao, J. Chi, N. Liu, R. Sun, and Y. Ma HER2/neu expression correlates with vasculogenic mimicry in invasive breast carcinoma J. Cell. Mol. Med. 17 2013 116 122
8. T.J. Liu, B.C. Sun, X.L. Zhao, X.M. Zhao, T. Sun, Q. Gu, Z. Yao, X.Y. Dong, N. Zhao, and N. Liu CD133+ cells with cancer stem cell characteristics associates with vasculogenic mimicry in triple-negative breast cancer Oncogene 32 2013 544 553
9. S. Bomken, K. Fiser, O. Heidenreich, and J. Vormoor Understanding the cancer stem cell Br. J. Cancer 103 2010 439 445
10. E. Charafe-Jauffret, F. Monville, C. Ginestier, G. Dontu, D. Birnbaum, and M.S. Wicha Cancer stem cells in breast: current opinion and future challenges Pathobiology 75 2008 75 84
11. S.Y. Yi, Y.B. Hao, K.J. Nan, and T.L. Fan Cancer stem cells niche: a target for novel cancer therapeutics Cancer Treat. Rev. 39 2013 290 296
12. C. Tang, B.T. Ang, and S. Pervaiz Cancer stem cell: target for anti-cancer therapy FASEB J. 21 2007 3777 3785
13. M. Al-Hajj, M.S. Wicha, A. Benito-Hernandez, S.J. Morrison, and M.F. Clarke Prospective identification of tumorigenic breast cancer cells Proc. Natl. Acad. Sci. U. S. A. 100 2003 3983 3988
14. C. Ginestier, M.H. Hur, E. Charafe-Jauffret, F. Monville, J. Dutcher, M. Brown, J. Jacquemier, P. Viens, C.G. Kleer, S. Liu, A. Schott, D. Hayes, D. Birnbaum, M.S. Wicha, and G. Dontu ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome Cell Stem Cell 1 2007 555 567
15. D. Ponti, A. Costa, N. Zaffaroni, G. Pratesi, G. Petrangolini, D. Coradini, S. Pilotti, M.A. Pierotti, and M.G. Daidone Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties Cancer Res. 65 2005 5506 5511
16. K. Saadin, and I.M. White Breast cancer stem cell enrichment and isolation by mammosphere culture and its potential diagnostic applications Expert Rev. Mol. Diagn. 13 2013 49 60
17. A.B. Alvero, H.H. Fu, J. Holmberg, I. Visintin, L. Mor, C.C. Marquina, J. Oidtman, D.A. Silasi, and G. Mor Stem-like ovarian cancer cells can serve as tumor vascular progenitors Stem Cells 27 2009 2405 2413
18. C. Folkins, Y. Shaked, S. Man, T. Tang, C.R. Lee, Z. Zhu, R.M. Hoffman, and R.S. Kerbel Glioma tumor stem-like cells promote tumor angiogenesis and vasculogenesis via vascular endothelial growth factor and stromal-derived factor 1 Cancer Res. 69 2009 7243 7251
19. L. Ricci-Vitiani, R. Pallini, M. Biffoni, M. Todaro, G. Invernici, T. Cenci, G. Maira, E.A. Parati, G. Stassi, L.M. Larocca, and R. De Maria Tumour vascularization via endothelial differentiation of glioblastoma stem-like cells Nature 468 2010 824 828
20. R. Wang, K. Chadalavada, J. Wilshire, U. Kowalik, K.E. Hovinga, A. Geber, B. Fligelman, M. Leversha, C. Brennan, and V. Tabar Glioblastoma stem-like cells give rise to tumour endothelium Nature 468 2010 829 833
21. M.J. Hendrix, E.A. Seftor, D.A. Kirschmann, and R.E. Seftor Molecular biology of breast cancer metastasis. Molecular expression of vascular markers by aggressive breast cancer cells Breast Cancer Res. 2 2000 417 422
22. L.A. Shevde, B.J. Metge, A. Mitra, Y. Xi, J. Ju, J.A. King, and R.S. Samant Spheroid-forming subpopulation of breast cancer cells demonstrates vasculogenic mimicry via hsa-miR-299-5p regulated de novo expression of osteopontin J. Cell. Mol. Med. 14 2010 1693 1706
23. C.M. Tate, W. Blosser, L. Wyss, G. Evans, Q. Xue, Y. Pan, and L. Stancato LY2228820 dimesylate, a selective inhibitor of p38 mitogen-activated protein kinase, reduces angiogenic endothelial cord formation in vitro and in vivo J. Biol. Chem. 288 2013 6743 6753
24. O. Straume, T. Shimamura, M.J. Lampa, J. Carretero, A.M. Oyan, D. Jia, C.L. Borgman, M. Soucheray, S.R. Downing, S.M. Short, S.Y. Kang, S. Wang, L. Chen, K. Collett, I. Bachmann, K.K. Wong, G.I. Shapiro, K.H. Kalland, J. Folkman, R.S. Watnick, L.A. Akslen, and G.N. Naumov Suppression of heat shock protein 27 induces long-term dormancy in human breast cancer Proc. Natl. Acad. Sci. U. S. A. 109 2012 8699 8704
25. R.W. Storms, A.P. Trujillo, J.B. Springer, L. Shah, O.M. Colvin, S.M. Ludeman, and C. Smith Isolation of primitive human hematopoietic progenitors on the basis of aldehyde dehydrogenase activity Proc. Natl. Acad. Sci. U. S. A. 96 1999 9118 9123
26. W.W. Chang, R.J. Lin, J. Yu, W.Y. Chang, C.H. Fu, A.C. Lai, J.C. Yu, and A.L. Yu The expression and significance of insulin-like growth factor-1 receptor and its pathway on breast cancer stem/progenitors Breast Cancer Res. 15 2013 R39
27. L. Wei, T.T. Liu, H.H. Wang, H.M. Hong, A.L. Yu, H.P. Feng, and W.W. Chang Hsp27 participates in the maintenance of breast cancer stem cells through regulation of epithelial-mesenchymal transition and nuclear factor-kappaB Breast Cancer Res. 13 2011 R101
28. C.H. Lee, H.M. Hong, Y.Y. Chang, and W.W. Chang Inhibition of heat shock protein (Hsp) 27 potentiates the suppressive effect of Hsp90 inhibitors in targeting breast cancer stem-like cells Biochimie 94 2012 1382 1389
29. W.W. Chang, Y.D. Kuan, M.C. Chen, S.T. Lin, and C.H. Lee Tracking of mouse breast cancer stem-like cells with Salmonella Exp. Biol. Med. (Maywood) 237 2012 1189 1196
30. E. Aranda, and G.I. Owen A semi-quantitative assay to screen for angiogenic compounds and compounds with angiogenic potential using the EA.hy926 endothelial cell line Biol. Res. 42 2009 377 389
31. J.T. Zhang, W. Sun, W.Z. Zhang, C.Y. Ge, Z.Y. Liu, Z.M. Zhao, X.S. Lu, and Y.Z. Fan Norcantharidin inhibits tumor growth and vasculogenic mimicry of human gallbladder carcinomas by suppression of the PI3-K/MMPs/Ln-5gamma2 signaling pathway BMC Cancer 14 2014 193
32. H. Wang, W. Sun, W.Z. Zhang, C.Y. Ge, J.T. Zhang, Z.Y. Liu, and Y.Z. Fan Inhibition of tumor vasculogenic mimicry and prolongation of host survival in highly aggressive gallbladder cancers by norcantharidin via blocking the ephrin type a receptor 2/focal adhesion kinase/paxillin signaling pathway PLoS One 9 2014 e96982
33. Y. Qu, L. Zhang, Z. Rong, T. He, and S. Zhang Number of glioma polyploid giant cancer cells (PGCCs) associated with vasculogenic mimicry formation and tumor grade in human glioma J. Exp. Clin. Cancer Res. 32 2013 75
34. M.J. Hendrix, E.A. Seftor, P.S. Meltzer, L.M. Gardner, A.R. Hess, D.A. Kirschmann, G.C. Schatteman, and R.E. Seftor Expression and functional significance of VE-cadherin in aggressive human melanoma cells: role in vasculogenic mimicry Proc. Natl. Acad. Sci. U. S. A. 98 2001 8018 8023
35. A.R. Hess, E.A. Seftor, L.M. Gardner, K. Carles-Kinch, G.B. Schneider, R.E. Seftor, M.S. Kinch, and M.J. Hendrix Molecular regulation of tumor cell vasculogenic mimicry by tyrosine phosphorylation: role of epithelial cell kinase (Eck/EphA2) Cancer Res. 61 2001 3250 3255
36. M.P. Wymann, and C. Schultz The chemical biology of phosphoinositide 3-kinases Chembiochem 13 2012 2022 2035
37. H. Masuda, D. Zhang, C. Bartholomeusz, H. Doihara, G.N. Hortobagyi, and N.T. Ueno Role of epidermal growth factor receptor in breast cancer Breast Cancer Res. Treat. 136 2012 331 345
38. H.W. Lo, S.C. Hsu, and M.C. Hung EGFR signaling pathway in breast cancers: from traditional signal transduction to direct nuclear translocalization Breast Cancer Res. Treat. 95 2006 211 218
39. S. Rousseau, F. Houle, and J. Huot Integrating the VEGF signals leading to actin-based motility in vascular endothelial cells Trends Cardiovasc. Med. 10 2000 321 327
40. S. Rousseau, F. Houle, J. Landry, and J. Huot p38 MAP kinase activation by vascular endothelial growth factor mediates actin reorganization and cell migration in human endothelial cells Oncogene 15 1997 2169 2177
41. S.M. Keezer, S.E. Ivie, H.C. Krutzsch, A. Tandle, S.K. Libutti, and D.D. Roberts Angiogenesis inhibitors target the endothelial cell cytoskeleton through altered regulation of heat shock protein 27 and cofilin Cancer Res. 63 2003 6405 6412
42. T. Sun, N. Zhao, X.L. Zhao, Q. Gu, S.W. Zhang, N. Che, X.H. Wang, J. Du, Y.X. Liu, and B.C. Sun Expression and functional significance of Twist1 in hepatocellular carcinoma: its role in vasculogenic mimicry Hepatology 51 2010 545 556
43. Q. Qin, Y. Xu, T. He, C. Qin, and J. Xu Normal and disease-related biological functions of Twist1 and underlying molecular mechanisms Cell Res. 22 2012 90 106
44. M. Shiota, J.L. Bishop, K.M. Nip, A. Zardan, A. Takeuchi, T. Cordonnier, E. Beraldi, J. Bazov, L. Fazli, K. Chi, M. Gleave, and A. Zoubeidi Hsp27 regulates epithelial mesenchymal transition, metastasis, and circulating tumor cells in prostate cancer Cancer Res. 73 2013 3109 3119
45. D.W. Miles Bevacizumab in breast cancer: fundamental questions remain Lancet Oncol. 14 2013 99 101
46. I. Lang, T. Brodowicz, L. Ryvo, Z. Kahan, R. Greil, S. Beslija, S.M. Stemmer, B. Kaufman, Z. Zvirbule, G.G. Steger, B. Melichar, T. Pienkowski, D. Sirbu, D. Messinger, and C. Zielinski Bevacizumab plus paclitaxel versus bevacizumab plus capecitabine as first-line treatment for HER2-negative metastatic breast cancer: interim efficacy results of the randomised, open-label, non-inferiority, phase 3 TURANDOT trial Lancet Oncol. 14 2013 125 133