Breast cancer normalization induced by embryonic mesenchyme is mediated by extracellular matrix biglycan

Integrative Biology (United Kingdom)

Volumn 5, Issue 8, 2013, Pages 1045-1056

  Bischof, Ashley G ^a,b   Yüksel, Deniz ^b   Mammoto, Tadanori ^a   Mammoto, Akiko ^a   Krause, Silva ^a   Ingber, Donald E ^a,b,c  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD UNIVERSITY   (United States)

^c HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIGLYCAN; CULTURE MEDIUM; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR ALPHA, HUMAN; SMALL INTERFERING RNA; TENASCIN;

ANIMAL; BREAST TUMOR; CELL DIFFERENTIATION; CELL PROLIFERATION; CHEMISTRY; COCULTURE; CULTURE MEDIUM; CULTURE TECHNIQUE; EMBRYOLOGY; EPITHELIUM; EXPERIMENTAL MAMMARY NEOPLASM; EXTRACELLULAR MATRIX; FEMALE; FIBROBLAST; HUMAN; IMMUNOHISTOCHEMISTRY; MESODERM; METABOLISM; MOUSE; PATHOLOGY; PHYSIOLOGY; PROCEDURES; PROTEOMICS; TIME; TISSUE ENGINEERING; UDDER; ARTICLE; METHODOLOGY; PRENATAL DEVELOPMENT;

ANIMALS; BIGLYCAN; BREAST NEOPLASMS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL PROLIFERATION; COCULTURE TECHNIQUES; CULTURE MEDIA, CONDITIONED; EPITHELIUM; ESTROGEN RECEPTOR ALPHA; EXTRACELLULAR MATRIX; FEMALE; FIBROBLASTS; HUMANS; IMMUNOHISTOCHEMISTRY; MAMMARY GLANDS, ANIMAL; MAMMARY NEOPLASMS, ANIMAL; MESODERM; MICE; PROTEOMICS; RNA, SMALL INTERFERING; TENASCIN; TIME FACTORS; TISSUE ENGINEERING;

EID: 84893450991     PISSN: 17579694     EISSN: 17579708     Source Type: Journal    
DOI: 10.1039/c3ib40103k     Document Type: Article

References (67)

1. J. J. DeCosse, C. L. Gossens, J. F. Kuzma, B. R. Unsworth, Breast cancer: induction of differentiation by embryonic tissue, Science, 1973, 181, 1057-1058
2. G. R. Cunha, H. Fujii, B. L. Neubauer, J. M. Shannon, L. Sawyer, B. A. Reese, Epithelial-mesenchymal interactions in prostatic development. I. morphological observations of prostatic induction by urogenital sinus mesenchyme in epithelium of the adult rodent urinary bladder, J. Cell Biol. 1983, 96, 1662-1670
3. Y. C. Wong, G. R. Cunha, N. Hayashi, Effects of mesenchyme of the embryonic urogenital sinus and neonatal seminal vesicle on the cytodifferentiation of the Dunning tumor: ultrastructural study, Acta Anat. 1992, 143, 139-150
4. G. R. Cunha, N. Hayashi, Y. C. Wong, Regulation of differentiation and growth of normal adult and neoplastic epithelia by inductive mesenchyme, Cancer Surv. 1991, 11, 73-90
5. M. L. Ellison, E. J. Ambrose, G. C. Easty, Differentiation in a transplantable rat tumour maintained in organ culture, Exp. Cell Res. 1969, 55, 198-204
6. C. J. Dawe, W. D. Morgan, M. S. Slatick, Influence of epithelio-mesenchymal interactions on tumor induction by polyoma virus, Int. J. Cancer, 1966, 1, 419-450
7. C. J. Dawe, J. Whang-Peng, W. D. Morgan, E. C. Hearon, T. Knutsen, Epithelial origin of polyoma salivary tumors in mice: evidence based on chromosome-marked cells, Science, 1971, 171, 394-397
8. M. V. Maffini, A. M. Soto, J. M. Calabro, A. A. Ucci, C. Sonnenschein, The stroma as a crucial target in rat mammary gland carcinogenesis, J. Cell Sci. 2004, 117, 1495-1502
9. M. H. Barcellos-Hoff, S. A. Ravani, Irradiated mammary gland stroma promotes the expression of tumorigenic potential by unirradiated epithelial cells, Cancer Res. 2000, 60, 1254-1260
10. D. E. Ingber, J. A. Madri, J. D. Jamieson, Neoplastic disorganization of pancreatic epithelial cell-cell relations. Role of basement membrane, Am. J. Pathol. 1985, 121, 248-260
11. D. E. Ingber, Cancer as a disease of epithelial-mesenchymal interactions and extracellular matrix regulation, Differentiation, 2002, 70, 547-560
12. D. E. Ingber, J. A. Madri, J. D. Jamieson, Role of basal lamina in neoplastic disorganization of tissue architecture, Proc. Natl. Acad. Sci. U. S. A. 1981, 78, 3901-3905
13. D. E. Ingber, J. A. Madri, J. D. Jamieson, Basement membrane as a spatial organizer of polarized epithelia. Exogenous basement membrane reorients pancreatic epithelial tumor cells in vitro, Am. J. Pathol. 1986, 122, 129-139
14. T. K. Watanabe, L. J. Hansen, N. K. Reddy, Y. S. Kanwar, J. K. Reddy, Differentiation of pancreatic acinar carcinoma cells cultured on rat testicular seminiferous tubular basement membranes, Cancer Res. 1984, 44, 5361-5368
15. B. Y. Karlan, R. L. Baldwin, F. D. Cirisano, P. W. Mamula, J. Jones, L. D. Lagasse, Secreted ovarian stromal substance inhibits ovarian epithelial cell proliferation, Gynecol. Oncol. 1995, 59, 67-74
16. X. Dong-Le Bourhis, Y. Berthois, G. Millot, A. Degeorges, M. Sylvi, P. M. Martin, F. Calvo, Effect of stromal and epithelial cells derived from normal and tumorous breast tissue on the proliferation of human breast cancer cell lines in co-culture, Int. J. Cancer, 1997, 71, 42-48
17. C. M. Verfaillie, P. Catanzaro, Direct contact with stroma inhibits proliferation of human long-term culture initiating cells, Leukemia, 1996, 10, 498-504
18. F. H. Paraguassu-Braga, R. Borojevic, L. F. Bouzas, M. A. Barcinski, A. Bonomo, Bone marrow stroma inhibits proliferation and apoptosis in leukemic cells through gap junction-mediated cell communication, Cell Death Differ. 2003, 10, 1101-1108
19. J. J. DeCosse, C. Gossens, J. F. Kuzma, B. R. Unsworth, Embryonic inductive tissues that cause histologic differentiation of murine mammary carcinoma in vitro, J. Natl. Cancer Inst. 1975, 54, 913-922
20. M. F. Rousseau-Merck, M. N. Lombard, C. Nezelof, H. Mouly, Limitation of the potentialities of nephroblastoma differentiation in vitro, Eur. J. Cancer, 1977, 13, 163-170
21. M. Gleave, J. T. Hsieh, C. A. Gao, A. C. von Eschenbach, L. W. Chung, Acceleration of human prostate cancer growth in vivo by factors produced by prostate and bone fibroblasts, Cancer Res. 1991, 51, 3753-3761
22. K. R. Baumann, H. L. Hosick, Replication of mouse mammary tumor cells in monolayer cultures stimulated with embryo extract, Exp. Cell Biol. 1978, 46, 325-337
23. T. Mammoto, A. Mammoto, Y. S. Torisawa, T. Tat, A. Gibbs, R. Derda, R. Mannix, M. de Bruijn, C. W. Yung, D. Huh, D. E. Ingber, Mechanochemical control of mesenchymal condensation and embryonic tooth organ formation, Dev. Cell, 2011, 21, 758-769
24. A. W. James, A. A. Theologis, S. A. Brugmann, Y. Xu, A. L. Carre, P. Leucht, K. Hamilton, K. S. Korach, M. T. Longaker, Estrogen/estrogen receptor alpha signaling in mouse posterofrontal cranial suture fusion, PLoS One, 2009, 4, e7120
25. K. Yamamoto, N. Ohga, Y. Hida, N. Maishi, T. Kawamoto, K. Kitayama, K. Akiyama, T. Osawa, M. Kondoh, K. Matsuda, Y. Onodera, M. Fujie, K. Kaga, S. Hirano, N. Shinohara, M. Shindoh, K. Hida, Biglycan is a specific marker and an autocrine angiogenic factor of tumour endothelial cells, Br. J. Cancer, 2012, 106, 1214-1223
26. E. Cukierman, Cell migration analyses within fibroblast-derived 3-D matrices, Methods Mol. Biol. 2005, 294, 79-93
27. C. L. Chu, J. A. Buczek-Thomas, M. A. Nugent, Heparan sulphate proteoglycans modulate fibroblast growth factor-2 binding through a lipid raft-mediated mechanism, Biochem. J. 2004, 379, 331-341
28. M. Vigny, M. P. Ollier-Hartmann, M. Lavigne, N. Fayein, J. C. Jeanny, M. Laurent, Y. Courtois, Specific binding of basic fibroblast growth factor to basement membrane-like structures and to purified heparan sulfate proteoglycan of the EHS tumor, J. Cell. Physiol. 1988, 137, 321-328
29. M. A. Carvalho, K. Arcanjo, L. C. Silva, R. Borojevic, The capacity of connective tissue stromas to sustain myelopoiesis depends both upon the growth factors and the local intercellular environment, Biol. Cell, 2000, 92, 605-614
30. R. G. Holzer, C. MacDougall, G. Cortright, K. Atwood, J. E. Green, C. L. Jorcyk, Development and characterization of a progressive series of mammary adenocarcinoma cell lines derived from the C3(1)/SV40 Large T-antigen transgenic mouse model, Breast Cancer Res. Treat. 2003, 77, 65-76
31. J. E. Green, M. A. Shibata, K. Yoshidome, M. L. Liu, C. Jorcyk, M. R. Anver, J. Wigginton, R. Wiltrout, E. Shibata, S. Kaczmarczyk, W. Wang, Z. Y. Liu, A. Calvo, C. Couldrey, The C3(1)/SV40 T-antigen transgenic mouse model of mammary cancer: ductal epithelial cell targeting with multistage progression to carcinoma, Oncogene, 2000, 19, 1020-1027
32. I. G. Maroulakou, M. Anver, L. Garrett, J. E. Green, Prostate and mammary adenocarcinoma in transgenic mice carrying a rat C3(1) simian virus 40 large tumor antigen fusion gene, Proc. Natl. Acad. Sci. U. S. A. 1994, 91, 11236-11240
33. S. Krause, M. V. Maffini, A. M. Soto, C. Sonnenschein, A novel 3D in vitro culture model to study stromal-epithelial interactions in the mammary gland, Tissue Eng. Part C, 2008, 14, 261-271
34. S. Ali, R. C. Coombes, Estrogen receptor alpha in human breast cancer: occurrence and significance, J. Mammary Gland Biol. Neoplasia, 2000, 5, 271-281
35. A. E. Karnoub, A. B. Dash, A. P. Vo, A. Sullivan, M. W. Brooks, G. W. Bell, A. L. Richardson, K. Polyak, R. Tubo, R. A. Weinberg, Mesenchymal stem cells within tumour stroma promote breast cancer metastasis, Nature, 2007, 449, 557-563
36. T. Sakakura, Y. Nishizuka, C. J. Dawe, Mesenchyme-dependent morphogenesis and epithelium-specific cytodifferentiation in mouse mammary gland, Science, 1976, 194, 1439-1441
37. C. J. Watson, W. T. Khaled, Mammary development in the embryo and adult: a journey of morphogenesis and commitment, Development, 2008, 135, 995-1003
38. J. M. Veltmaat, A. A. Mailleux, J. P. Thiery, S. Bellusci, Mouse embryonic mammogenesis as a model for the molecular regulation of pattern formation, Differentiation, 2003, 71, 1-17
39. A. Naba, K. R. Clauser, S. Hoersch, H. Liu, S. A. Carr, R. O. Hynes, The matrisome: in silico definition and in vivo characterization by proteomics of normal and tumor extracellular matrices, Mol. Cell. Proteomics, 2012, 11, M111.014647. doi: 10.1074/mcp.M111.014647
40. B. Wang, G. X. Li, S. G. Zhang, Q. Wang, Y. G. Wen, H. M. Tang, C. Z. Zhou, A. Y. Xing, J. W. Fan, D. W. Yan, G. Q. Qiu, Z. H. Yu, Z. H. Peng, Biglycan expression correlates with aggressiveness and poor prognosis of gastric cancer, Exp. Biol. Med. 2011, 236, 1247-1253
41. X. Gu, Y. Ma, J. Xiao, H. Zheng, C. Song, Y. Gong, X. Xing, Up-regulated biglycan expression correlates with the malignancy in human colorectal cancers, Clin. Exp. Med. 2012, 12, 195-199
42. C. K. Weber, G. Sommer, P. Michl, H. Fensterer, M. Weimer, F. Gansauge, G. Leder, G. Adler, T. M. Gress, Biglycan is overexpressed in pancreatic cancer and induces G1-arrest in pancreatic cancer cell lines, Gastroenterology, 2001, 121, 657-667
43. G. Orend, R. Chiquet-Ehrismann, Tenascin-C induced signaling in cancer, Cancer Lett. 2006, 244, 143-163
44. T. Oskarsson, S. Acharyya, X. H. Zhang, S. Vanharanta, S. F. Tavazoie, P. G. Morris, R. J. Downey, K. Manova-Todorova, E. Brogi, J. Massague, Breast cancer cells produce tenascin C as a metastatic niche component to colonize the lungs, Nat. Med. 2011, 17, 867-874
45. I. Paron, S. Berchtold, J. Voros, M. Shamarla, M. Erkan, H. Hofler, I. Esposito, Tenascin-C enhances pancreatic cancer cell growth and motility and affects cell adhesion through activation of the integrin pathway, PLoS One, 2011, 6, e21684
46. R. A. Hancox, M. D. Allen, D. L. Holliday, D. R. Edwards, C. J. Pennington, D. S. Guttery, J. A. Shaw, R. A. Walker, J. H. Pringle, J. L. Jones, Tumour-associated tenascin-C isoforms promote breast cancer cell invasion and growth by matrix metalloproteinase-dependent and independent mechanisms, Breast Cancer Res. 2009, 11, R24
47. R. L. Brinster, The effect of cells transferred into the mouse blastocyst on subsequent development, J. Exp. Med. 1974, 140, 1049-1056
48. P. Rous, A Sarcoma of the Fowl Transmissible by an Agent Separable from the Tumor Cells, J. Exp. Med. 1911, 13, 397-411
49. D. S. Dolberg, M. J. Bissell, Inability of Rous sarcoma virus to cause sarcomas in the avian embryo, Nature, 1984, 309, 552-556
50. S. Huang, D. E. Ingber, The structural and mechanical complexity of cell-growth control, Nat. Cell Biol. 1999, 1, E131-E138
51. S. D. Banerjee, R. H. Cohn, M. R. Bernfield, Basal lamina of embryonic salivary epithelia. Production by the epithelium and role in maintaining lobular morphology, J. Cell Biol. 1977, 73, 445-463
52. C. J. Sympson, R. S. Talhouk, C. M. Alexander, J. R. Chin, S. M. Clift, M. J. Bissell, Z. Werb, Targeted expression of stromelysin-1 in mammary gland provides evidence for a role of proteinases in branching morphogenesis and the requirement for an intact basement membrane for tissue-specific gene expression, J. Cell Biol. 1994, 125, 681-693
53. K. R. Levental, H. Yu, L. Kass, J. N. Lakins, M. Egeblad, J. T. Erler, S. F. Fong, K. Csiszar, A. Giaccia, W. Weninger, M. Yamauchi, D. L. Gasser, V. M. Weaver, Matrix crosslinking forces tumor progression by enhancing integrin signaling, Cell, 2009, 139, 891-906
54. M. L. Li, J. Aggeler, D. A. Farson, C. Hatier, J. Hassell, M. J. Bissell, Influence of a reconstituted basement membrane and its components on casein gene expression and secretion in mouse mammary epithelial cells, Proc. Natl. Acad. Sci. U. S. A. 1987, 84, 136-140
55. M. A. Nash, A. E. Loercher, R. S. Freedman, In vitro growth inhibition of ovarian cancer cells by decorin: synergism of action between decorin and carboplatin, Cancer Res. 1999, 59, 6192-6196
56. X. D. Chen, L. W. Fisher, P. G. Robey, M. F. Young, The small leucine-rich proteoglycan biglycan modulates BMP-4-induced osteoblast differentiation, FASEB J. 2004, 18, 948-958
57. K. G. Vogel, J. A. Trotter, The effect of proteoglycans on the morphology of collagen fibrils formed in vitro, Collagen Relat. Res. 1987, 7, 105-114
58. E. Schonherr, P. Witsch-Prehm, B. Harrach, H. Robenek, J. Rauterberg, H. Kresse, Interaction of biglycan with type I collagen, J. Biol. Chem. 1995, 270, 2776-2783
59. I. M. Kuc, P. G. Scott, Increased diameters of collagen fibrils precipitated in vitro in the presence of decorin from various connective tissues, Connect. Tissue Res. 1997, 36, 287-296
60. A. Corsi, T. Xu, X. D. Chen, A. Boyde, J. Liang, M. Mankani, B. Sommer, R. V. Iozzo, I. Eichstetter, P. G. Robey, P. Bianco, M. F. Young, Phenotypic effects of biglycan deficiency are linked to collagen fibril abnormalities, are synergized by decorin deficiency, and mimic Ehlers-Danlos-like changes in bone and other connective tissues, J. Bone Miner. Res. 2002, 17, 1180-1189
61. E. Pinney, M. Zimber, A. Schenone, M. Montes-Camacho, F. Ziegler, G. Naughton, Human Embryonic-like ECM (hECM) Stimulates Proliferation and Differentiation in Stem Cells While Killing Cancer Cells, Int. J. Stem Cells, 2011, 4, 70-75
62. S. Kidd, E. Spaeth, J. L. Dembinski, M. Dietrich, K. Watson, A. Klopp, V. L. Battula, M. Weil, M. Andreeff, F. C. Marini, Direct evidence of mesenchymal stem cell tropism for tumor and wounding microenvironments using in vivo bioluminescent imaging, Stem Cells, 2009, 27, 2614-2623
63. E. L. Spaeth, J. L. Dembinski, A. K. Sasser, K. Watson, A. Klopp, B. Hall, M. Andreeff, F. Marini, Mesenchymal stem cell transition to tumor-associated fibroblasts contributes to fibrovascular network expansion and tumor progression, PLoS One, 2009, 4, e4992
64. S. B. Coffelt, F. C. Marini, K. Watson, K. J. Zwezdaryk, J. L. Dembinski, H. L. LaMarca, S. L. Tomchuck, K. Honer zu Bentrup, E. S. Danka, S. L. Henkle, A. B. Scandurro, The pro-inflammatory peptide LL-37 promotes ovarian tumor progression through recruitment of multipotent mesenchymal stromal cells, Proc. Natl. Acad. Sci. U. S. A. 2009, 106, 3806-3911
65. N. C. Direkze, K. Hodivala-Dilke, R. Jeffery, T. Hunt, R. Poulsom, D. Oukrif, M. R. Alison, N. A. Wright, Bone marrow contribution to tumor-associated myofibroblasts and fibroblasts, Cancer Res. 2004, 64, 8492-8495
66. G. Ishii, T. Sangai, T. Oda, Y. Aoyagi, T. Hasebe, N. Kanomata, Y. Endoh, C. Okumura, Y. Okuhara, J. Magae, M. Emura, T. Ochiya, A. Ochiai, Bone-marrow-derived myofibroblasts contribute to the cancer-induced stromal reaction, Biochem. Biophys. Res. Commun. 2003, 309, 232-240
67. D. E. Ingber, Can cancer be reversed by engineering the tumor microenvironment, Semin. Cancer Biol. 2008, 18, 356-364