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Tissue architecture and function: dynamic reciprocity via extra- and intra-cellular matrices

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Abstract

Mammary gland development, functional differentiation, and homeostasis are orchestrated and sustained by a balance of biochemical and biophysical cues from the organ’s microenvironment. The three-dimensional microenvironment of the mammary gland, predominantly ‘encoded’ by a collaboration between the extracellular matrix (ECM), hormones, and growth factors, sends signals from ECM receptors through the cytoskeletal intracellular matrix to nuclear and chromatin structures resulting in gene expression; the ECM in turn is regulated and remodeled by signals from the nucleus. In this chapter, we discuss how coordinated ECM deposition and remodeling is necessary for mammary gland development, how the ECM provides structural and biochemical cues necessary for tissue-specific function, and the role of the cytoskeleton in mediating the extra—to intracellular dialogue occurring between the nucleus and the microenvironment. When operating normally, the cytoskeletal-mediated dynamic and reciprocal integration of tissue architecture and function directs mammary gland development, tissue polarity, and ultimately, tissue-specific gene expression. Cancer occurs when these dynamic interactions go awry for an extended time.

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Abbreviations

2D:

two-dimensional

3D:

three-dimensional

BM:

basement membrane

C/EBP,CAAT/:

enhancer-binding protein

DG:

dystroglycan

ECM:

extracellular matrix

EGFR:

epidermal growth factor receptor

FN:

fibronectin

JAK:

Janus kinase

lrECM:

laminin-rich ECM

MMP:

matrix metalloproteinases

PI3K:

Phosphoinositide-3 kinase

polyHEMA:

poly(2-hydroxyethyl methacrylate)

STAT5:

signal transducers and activators of transcription protein 5

TGF-α:

transforming growth factor-α

WAP:

whey acidic protein

References

  1. Nelson, C. M., & Bissell, M. J. (2006). Of extracellular matrix, scaffolds, and signaling: tissue architecture regulates development, homeostasis, and cancer. Annual review of cell and developmental biology, 22, 287–309.

    Article  PubMed  CAS  Google Scholar 

  2. Bissell, M. J., Hall, H. G., & Parry, G. (1982). How does the extracellular matrix direct gene expression? Journal of theoretical biology, 99, 31–68.

    Article  PubMed  CAS  Google Scholar 

  3. Hynes, R. O. (2002). Integrins: bidirectional, allosteric signaling machines. Cell, 110, 673–687.

    Article  PubMed  CAS  Google Scholar 

  4. Maxwell, C. A., McCarthy, J., & Turley, E. (2008). Cell-surface and mitotic-spindle RHAMM: moonlighting or dual oncogenic functions? Journal of Cell Science, 121, 925–932.

    Article  PubMed  CAS  Google Scholar 

  5. Sanderson, R. D., Yang, Y., Suva, L. J., & Kelly, T. (2004). Heparan sulfate proteoglycans and heparanase–partners in osteolytic tumor growth and metastasis. Matrix biol, 23, 341–352.

    Article  PubMed  CAS  Google Scholar 

  6. Yurchenco, P. D., & Wadsworth, W. G. (2004). Assembly and tissue functions of early embryonic laminins and netrins. Current opinion in cell biology, 16, 572–579.

    Article  PubMed  CAS  Google Scholar 

  7. Fata, J. E., Werb, Z., & Bissell, M. J. (2004). Regulation of mammary gland branching morphogenesis by the extracellular matrix and its remodeling enzymes. Breast cancer research, 6, 1–11.

    PubMed  CAS  Google Scholar 

  8. Keely, P. J., Wu, J. E., & Santoro, S. A. (1995). The spatial and temporal expression of the alpha 2 beta 1 integrin and its ligands, collagen I, collagen IV, and laminin, suggest important roles in mouse mammary morphogenesis. Differentiation, 59, 1–13.

    Article  PubMed  CAS  Google Scholar 

  9. Talhouk, R. S., Chin, J. R., Unemori, E. N., Werb, Z., & Bissell, M. J. (1991). Proteinases of the mammary gland: developmental regulation in vivo and vectorial secretion in culture. Development, 112, 439–449.

    PubMed  CAS  Google Scholar 

  10. Schedin, P., Mitrenga, T., McDaniel, S., & Kaeck, M. (2004). Mammary ECM composition and function are altered by reproductive state. Molecular carcinogenesis, 41, 207–220.

    Article  PubMed  CAS  Google Scholar 

  11. Wicha, M. S., Liotta, L. A., Vonderhaar, B. K., & Kidwell, W. R. (1980). Effects of inhibition of basement membrane collagen deposition on rat mammary gland development. Developments in biologicals, 80, 253–256.

    Article  CAS  Google Scholar 

  12. Silberstein, G. B., & Daniel, C. W. (1982). Glycosaminoglycans in the basal lamina and extracellular matrix of the developing mouse mammary duct. Developmental biology, 90, 215–222.

    Article  PubMed  CAS  Google Scholar 

  13. Turley, E. A., Veiseh, M., Radisky, D. C., & Bissell, M. J. (2008). Mechanisms of disease: epithelial-mesenchymal transition–does cellular plasticity fuel neoplastic progression? Nat Clin Pract Oncol, 5, 280–290.

    Article  PubMed  CAS  Google Scholar 

  14. Taddei, I., Deugnier, M. A., Faraldo, M. M., Petit, V., Bouvard, D., Medina, D., et al. (2008). Beta1 integrin deletion from the basal compartment of the mammary epithelium affects stem cells. Nature cell biology, 10, 716–722.

    Article  PubMed  CAS  Google Scholar 

  15. Woodward, T. L., Mienaltowski, A. S., Modi, R. R., Bennett, J. M., & Haslam, S. Z. (2001). Fibronectin and the alpha(5)beta(1) integrin are under developmental and ovarian steroid regulation in the normal mouse mammary gland. Endocrinology, 142, 3214–3222.

    Article  PubMed  CAS  Google Scholar 

  16. Williams, C. M., Engler, A. J., Slone, R. D., Galante, L. L., & Schwarzbauer, J. E. (2008). Fibronectin expression modulates mammary epithelial cell proliferation during acinar differentiation. Cancer research, 68, 3185–3192.

    Article  PubMed  CAS  Google Scholar 

  17. Sandal, T., Valyi-Nagy, K., Spencer, V. A., Folberg, R., Bissell, M. J., & Maniotis, A. J. (2007). Epigenetic reversion of breast carcinoma phenotype is accompanied by changes in DNA sequestration as measured by AluI restriction enzyme. American journal of pathology, 170, 1739–1749.

    Article  PubMed  CAS  Google Scholar 

  18. Werb, Z., & Chin, J. R. (1998). Extracellular matrix remodeling during morphogenesis. Ann N Y Acad Sci, 857, 110–118.

    Article  PubMed  CAS  Google Scholar 

  19. Lochter, A., Sternlicht, M. D., Werb, Z., & Bissell, M. J. (1998). The significance of matrix metalloproteinases during early stages of tumor progression. Ann N Y Acad Sci, 857, 180–193.

    Article  PubMed  CAS  Google Scholar 

  20. Talhouk, R. S., Bissell, M. J., & Werb, Z. (1992). Coordinated expression of extracellular matrix-degrading proteinases and their inhibitors regulates mammary epithelial function during involution. Journal of cell biology, 118, 1271–1282.

    Article  PubMed  CAS  Google Scholar 

  21. Witty, J. P., Wright, J. H., & Matrisian, L. M. (1995). Matrix metalloproteinases are expressed during ductal and alveolar mammary morphogenesis, and misregulation of stromelysin-1 in transgenic mice induces unscheduled alveolar development. Molecular biology of the cell, 6, 1287–1303.

    PubMed  CAS  Google Scholar 

  22. Thomasset, N., Lochter, A., Sympson, C. J., Lund, L. R., Williams, D. R., Behrendtsen, O., et al. (1998). Expression of autoactivated stromelysin-1 in mammary glands of transgenic mice leads to a reactive stroma during early development. American journal of pathology, 153, 457–467.

    PubMed  CAS  Google Scholar 

  23. Wiseman, B. S., Sternlicht, M. D., Lund, L. R., Alexander, C. M., Mott, J., Bissell, M. J., et al. (2003). Site-specific inductive and inhibitory activities of MMP-2 and MMP-3 orchestrate mammary gland branching morphogenesis. Journal of cell biology, 162, 1123–1133.

    Article  PubMed  CAS  Google Scholar 

  24. Mori, H., Nelson, C. M., Alcaraz, J., Chen, C. S., Lo, A. T., Fata, J. E., et al. (Submitted). The catalytic and non-catalytic domains of MMP14 and stromal collagen density regulate signaling loops that direct invasion and branching of mammary epithelial cells.

  25. Sympson, C. J., Talhouk, R. S., Alexander, C. M., Chin, J. R., Clift, S. M., Bissell, M. J., et al. (1994). 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. Journal of cell biology, 125, 681–693.

    Article  PubMed  CAS  Google Scholar 

  26. Koshikawa, N., Minegishi, T., Sharabi, A., Quaranta, V., & Seiki, M. (2005). Membrane-type matrix metalloproteinase-1 (MT1-MMP) is a processing enzyme for human laminin gamma 2 chain. Journal of biological chemistry, 280, 88–93.

    PubMed  CAS  Google Scholar 

  27. Koshikawa, N., Schenk, S., Moeckel, G., Sharabi, A., Miyazaki, K., Gardner, H., et al. (2004). Proteolytic processing of laminin-5 by MT1-MMP in tissues and its effects on epithelial cell morphology. FASEB journal, 18, 364–366.

    PubMed  CAS  Google Scholar 

  28. Bissell, M. J., Rizki, A., & Mian, I. S. (2003). Tissue architecture: the ultimate regulator of breast epithelial function. Current opinion in cell biology, 15, 753–762.

    Article  PubMed  CAS  Google Scholar 

  29. Hagios, C., Lochter, A., & Bissell, M. J. (1998). Tissue architecture: the ultimate regulator of epithelial function? Philosophical transactions of the Royal Society of London. Series B, Biological sciences, 353, 857–870.

    Article  PubMed  CAS  Google Scholar 

  30. Emerman, J. T., & Pitelka, D. R. (1977). Maintenance and induction of morphological differentiation in dissociated mammary epithelium on floating collagen membranes. In Vitro, 13, 316–328.

    Article  PubMed  CAS  Google Scholar 

  31. Kleinman, H. K., McGarvey, M. L., Liotta, L. A., Robey, P. G., Tryggvason, K., & Martin, G. R. (1982). Isolation and characterization of type IV procollagen, laminin, and heparan sulfate proteoglycan from the EHS sarcoma. Biochemistry, 21, 6188–6193.

    Article  PubMed  CAS  Google Scholar 

  32. Li, M. L., Aggeler, J., Farson, D. A., Hatier, C., Hassell, J., & Bissell, M. J. (1987). Influence of a reconstituted basement membrane and its components on casein gene expression and secretion in mouse mammary epithelial cells. Proceedings of the National Academy of Sciences of the United States of America, 84, 136–140.

    Article  PubMed  CAS  Google Scholar 

  33. Barcellos-Hoff, M. H., Aggeler, J., Ram, T. G., & Bissell, M. J. (1989). Functional differentiation and alveolar morphogenesis of primary mammary cultures on reconstituted basement membrane. Development, 105, 223–235.

    PubMed  CAS  Google Scholar 

  34. Bissell, M. J., Kenny, P. A., & 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 Harbor Symposia on Quantitative Biology, 70, 343–356.

    Article  PubMed  CAS  Google Scholar 

  35. Bissell, M. J., & Bilder, D. (2003). Polarity determination in breast tissue: desmosomal adhesion, myoepithelial cells, and laminin 1. Breast cancer research, 5, 117–119.

    Article  PubMed  CAS  Google Scholar 

  36. Gudjonsson, T., Ronnov-Jessen, L., Villadsen, R., Rank, F., Bissell, M. J., & 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. Journal of Cell Science, 115, 39–50.

    PubMed  CAS  Google Scholar 

  37. Streuli, C. H., Bailey, N., & Bissell, M. J. (1991). Control of mammary epithelial differentiation: basement membrane induces tissue-specific gene expression in the absence of cell-cell interaction and morphological polarity. Journal of cell biology, 115, 1383–1395.

    Article  PubMed  CAS  Google Scholar 

  38. Weir, M. L., Oppizzi, M. L., Henry, M. D., Onishi, A., Campbell, K. P., Bissell, M. J., et al. (2006). Dystroglycan loss disrupts polarity and beta-casein induction in mammary epithelial cells by perturbing laminin anchoring. Journal of Cell Science, 119, 4047–4058.

    Article  PubMed  CAS  Google Scholar 

  39. Naylor, M. J., Li, N., Cheung, J., Lowe, E. T., Lambert, E., Marlow, R., et al. (2005). Ablation of beta1 integrin in mammary epithelium reveals a key role for integrin in glandular morphogenesis and differentiation. Journal of cell biology, 171, 717–728.

    Article  PubMed  CAS  Google Scholar 

  40. Xu, R., Nelson, C. M., Muschler, J., Veiseh, M., Vonderhaar, B. K., Bissell, M. J. (2008). Sustained activation of STAT5 is essential for chromatin remodeling and maintenance of mammary-specific function. Journal of cell biology, In press.

  41. Ben-Jonathan, N., Mershon, J. L., Allen, D. L., & Steinmetz, R. W. (1996). Extrapituitary prolactin: distribution, regulation, functions, and clinical aspects. Endocrine reviews, 17, 639–669.

    PubMed  CAS  Google Scholar 

  42. Lin, C. Q., Dempsey, P. J., Coffey, R. J., & Bissell, M. J. (1995). Extracellular matrix regulates whey acidic protein gene expression by suppression of TGF-alpha in mouse mammary epithelial cells: studies in culture and in transgenic mice. Journal of cell biology, 129, 1115–1126.

    Article  PubMed  CAS  Google Scholar 

  43. Chen, L. H., & Bissell, M. J. (1989). A novel regulatory mechanism for whey acidic protein gene expression. Cell regulation, 1, 45–54.

    PubMed  CAS  Google Scholar 

  44. Vermeer, P. D., Einwalter, L. A., Moninger, T. O., Rokhlina, T., Kern, J. A., Zabner, J., et al. (2003). Segregation of receptor and ligand regulates activation of epithelial growth factor receptor. Nature, 422, 322–326.

    Article  PubMed  CAS  Google Scholar 

  45. Liu, H., Radisky, D. C., Wang, F., & Bissell, M. J. (2004). Polarity and proliferation are controlled by distinct signaling pathways downstream of PI3-kinase in breast epithelial tumor cells. Journal of cell biology, 164, 603–612.

    Article  PubMed  CAS  Google Scholar 

  46. Xu, R., Spencer, V. A., & Bissell, M. J. (2007). Extracellular matrix-regulated gene expression requires cooperation of SWI/SNF and transcription factors. Journal of biological chemistry, 282, 14992–14999.

    Article  PubMed  CAS  Google Scholar 

  47. Streuli, C. H., Schmidhauser, C., Bailey, N., Yurchenco, P., Skubitz, A. P., Roskelley, C., et al. (1995). Laminin mediates tissue-specific gene expression in mammary epithelia. Journal of cell biology, 129, 591–603.

    Article  PubMed  CAS  Google Scholar 

  48. Schmidhauser, C., Casperson, G. F., Myers, C. A., Sanzo, K. T., Bolten, S., & Bissell, M. J. (1992). A novel transcriptional enhancer is involved in the prolactin—and extracellular matrix-dependent regulation of beta-casein gene expression. Molecular biology of the cell, 3, 699–709.

    PubMed  CAS  Google Scholar 

  49. Myers, C. A., Schmidhauser, C., Mellentin-Michelotti, J., Fragoso, G., Roskelley, C. D., Casperson, G., et al. (1998). Characterization of BCE-1, a transcriptional enhancer regulated by prolactin and extracellular matrix and modulated by the state of histone acetylation. Molecular and cellular biology, 18, 2184–2195.

    PubMed  CAS  Google Scholar 

  50. Clayton, D. F., Harrelson, A. L., & Darnell Jr., J. E. (1985). Dependence of liver-specific transcription on tissue organization. Molecular and cellular biology, 5, 2623–2632.

    PubMed  CAS  Google Scholar 

  51. Streuli, C. H., Edwards, G. M., Delcommenne, M., Whitelaw, C. B., Burdon, T. G., Schindler, C., et al. (1995). Stat5 as a target for regulation by extracellular matrix. Journal of biological chemistry, 270, 21639–21644.

    Article  PubMed  CAS  Google Scholar 

  52. Lelievre, S. A., Weaver, V. M., Nickerson, J. A., Larabell, C. A., Bhaumik, A., Petersen, O. W., et al. (1998). Tissue phenotype depends on reciprocal interactions between the extracellular matrix and the structural organization of the nucleus. Proceedings of the National Academy of Sciences of the United States of America, 95, 14711–14716.

    Article  PubMed  CAS  Google Scholar 

  53. Weaver, V. M., Lelievre, S., Lakins, J. N., Chrenek, M. A., Jones, J. C., Giancotti, F., et al. (2002). beta4 integrin-dependent formation of polarized three-dimensional architecture confers resistance to apoptosis in normal and malignant mammary epithelium. Cancer Cell, 2, 205–216.

    Article  PubMed  CAS  Google Scholar 

  54. Kaminker, P., Plachot, C., Kim, S. H., Chung, P., Crippen, D., Petersen, O. W., et al. (2005). Higher-order nuclear organization in growth arrest of human mammary epithelial cells: a novel role for telomere-associated protein TIN2. Journal of Cell Science, 118, 1321–1330.

    Article  PubMed  CAS  Google Scholar 

  55. Berrier, A. L., & Yamada, K. M. (2007). Cell-matrix adhesion. Journal of cellular physiology, 213, 565–573.

    Article  PubMed  CAS  Google Scholar 

  56. Zhang, Q., Skepper, J. N., Yang, F., Davies, J. D., Hegyi, L., Roberts, R. G., et al. (2001). Nesprins: a novel family of spectrin-repeat-containing proteins that localize to the nuclear membrane in multiple tissues. Journal of Cell Science, 114, 4485–4498.

    PubMed  CAS  Google Scholar 

  57. Hetzer, M. W., Walther, T. C., & Mattaj, I. W. (2005). Pushing the envelope: structure, function, and dynamics of the nuclear periphery. Annual review of cell and developmental biology, 21, 347–380.

    Article  PubMed  CAS  Google Scholar 

  58. Maniotis, A. J., Chen, C. S., & Ingber, D. E. (1997). Demonstration of mechanical connections between integrins, cytoskeletal filaments, and nucleoplasm that stabilize nuclear structure. Proceedings of the National Academy of Sciences of the United States of America, 94, 849–854.

    Article  PubMed  CAS  Google Scholar 

  59. Le Beyec, J., Xu, R., Lee, S. Y., Nelson, C. M., Rizki, A., Alcaraz, J., et al. (2007). Cell shape regulates global histone acetylation in human mammary epithelial cells. Experimental cell research, 313, 3066–3075.

    Article  PubMed  Google Scholar 

  60. Muschler, J., Lochter, A., Roskelley, C. D., Yurchenco, P., & Bissell, M. J. (1999). Division of labor among the alpha6beta4 integrin, beta1 integrins, and an E3 laminin receptor to signal morphogenesis and beta-casein expression in mammary epithelial cells. Molecular biology of the cell, 10, 2817–2828.

    PubMed  CAS  Google Scholar 

  61. Roskelley, C. D., Desprez, P. Y., & Bissell, M. J. (1994). Extracellular matrix-dependent tissue-specific gene expression in mammary epithelial cells requires both physical and biochemical signal transduction. Proceedings of the National Academy of Sciences of the United States of America, 91, 12378–12382.

    Article  PubMed  CAS  Google Scholar 

  62. McNally, J. G., Muller, W. G., Walker, D., Wolford, R., & Hager, G. L. (2000). The glucocorticoid receptor: rapid exchange with regulatory sites in living cells. Science, 287, 1262–1265.

    Article  PubMed  CAS  Google Scholar 

  63. Metivier, R., Penot, G., Hubner, M. R., Reid, G., Brand, H., Kos, M., et al. (2003). Estrogen receptor-alpha directs ordered, cyclical, and combinatorial recruitment of cofactors on a natural target promoter. Cell, 115, 751–763.

    Article  PubMed  CAS  Google Scholar 

  64. Zoubiane, G. S., Valentijn, A., Lowe, E. T., Akhtar, N., Bagley, S., Gilmore, A. P., et al. (2004). A role for the cytoskeleton in prolactin-dependent mammary epithelial cell differentiation. Journal of Cell Science, 117, 271–280.

    Article  PubMed  CAS  Google Scholar 

  65. Akhtar, N., & Streuli, C. H. (2006). Rac1 links integrin-mediated adhesion to the control of lactational differentiation in mammary epithelia. Journal of Cell Biology, 173, 781–793.

    Article  PubMed  CAS  Google Scholar 

  66. Jou, T. S., & Nelson, W. J. (1998). Effects of regulated expression of mutant RhoA and Rac1 small GTPases on the development of epithelial (MDCK) cell polarity. Journal of Cell Biology, 142, 85–100.

    Article  PubMed  CAS  Google Scholar 

  67. Jaffe, A. B., & Hall, A. (2005). Rho GTPases: biochemistry and biology. Annual review of cell and developmental biology, 21, 247–269.

    Article  PubMed  CAS  Google Scholar 

  68. Kheradmand, F., Werner, E., Tremble, P., Symons, M., & Werb, Z. (1998). Role of Rac1 and oxygen radicals in collagenase-1 expression induced by cell shape change. Science, 280, 898–902.

    Article  PubMed  CAS  Google Scholar 

  69. Engler, A. J., Sen, S., Sweeney, H. L., & Discher, D. E. (2006). Matrix elasticity directs stem cell lineage specification. Cell, 126, 677–689.

    Article  PubMed  CAS  Google Scholar 

  70. Paszek, M. J., Zahir, N., Johnson, K. R., Lakins, J. N., Rozenberg, G. I., Gefen, A., et al. (2005). Tensional homeostasis and the malignant phenotype. Cancer Cell, 8, 241–254.

    Article  PubMed  CAS  Google Scholar 

  71. Lee, E. Y., Parry, G., & Bissell, M. J. (1984). Modulation of secreted proteins of mouse mammary epithelial cells by the collagenous substrata. Journal of Cell Biology, 98, 146–155.

    Article  PubMed  CAS  Google Scholar 

  72. Alcaraz, J., Xu, R., Mori, H., Nelson, C. M., Mroue, R., Spencer, V. A., et al. (2008). Laminin and biomimetic extracellular elasticity enhance functional differentiation in mammary epithelia. EMBO journal, 27, 2829–2838.

    Article  PubMed  CAS  Google Scholar 

  73. Wozniak, M. A., Desai, R., Solski, P. A., Der, C. J., & Keely, P. J. (2003). ROCK-generated contractility regulates breast epithelial cell differentiation in response to the physical properties of a three-dimensional collagen matrix. Journal of Cell Biology, 163, 583–595.

    Article  PubMed  CAS  Google Scholar 

  74. Alcaraz, J., Nelson, C. M., & Bissell, M. J. (2004). Biomechanical approaches for studying integration of tissue structure and function in mammary epithelia. Journal of mammary gland biology and neoplasia, 9, 361–374.

    Article  PubMed  Google Scholar 

  75. Baneyx, G., Baugh, L., & Vogel, V. (2002). Fibronectin extension and unfolding within cell matrix fibrils controlled by cytoskeletal tension. Proceedings of the National Academy of Sciences of the United States of America, 99, 5139–5143.

    Article  PubMed  CAS  Google Scholar 

  76. Feral, C. C., Zijlstra, A., Tkachenko, E., Prager, G., Gardel, M. L., Slepak, M., et al. (2007). CD98hc (SLC3A2) participates in fibronectin matrix assembly by mediating integrin signaling. Journal of Cell Biology, 178, 701–711.

    Article  PubMed  CAS  Google Scholar 

  77. Lambert, C. A., Colige, A. C., Munaut, C., Lapiere, C. M., & Nusgens, B. V. (2001). Distinct pathways in the over-expression of matrix metalloproteinases in human fibroblasts by relaxation of mechanical tension. Matrix Biol, 20, 397–408.

    Article  PubMed  CAS  Google Scholar 

  78. Chang, H. Y., Chi, J. T., Dudoit, S., Bondre, C., van de Rijn, M., Botstein, D., et al. (2002). Diversity, topographic differentiation, and positional memory in human fibroblasts. Proceedings of the National Academy of Sciences of the United States of America, 99, 12877–12882.

    Article  PubMed  CAS  Google Scholar 

  79. Boulanger, C. A., Mack, D. L., Booth, B. W., & Smith, G. H. (2007). Interaction with the mammary microenvironment redirects spermatogenic cell fate in vivo. Proceedings of the National Academy of Sciences of the United States of America, 104, 3871–3876.

    Article  PubMed  CAS  Google Scholar 

  80. Booth, B. W., Mack, D. L., Androutsellis-Theotokis, A., McKay, R. D., Boulanger, C. A., & Smith, G. H. (2008). The mammary microenvironment alters the differentiation repertoire of neural stem cells. Proceedings of the National Academy of Sciences of the United States of America, 105, 14891–14896.

    Article  PubMed  CAS  Google Scholar 

  81. Bissell, M. J., & Inman, J. (2008). Reprogramming stem cells is a microenvironmental task. Proceedings of the National Academy of Sciences of the United States of America, 105, 15637–15638.

    Article  PubMed  CAS  Google Scholar 

  82. Sternlicht, M. D., Lochter, A., Sympson, C. J., Huey, B., Rougier, J. P., Gray, J. W., Pinkel, D., et al. (1999). The stromal proteinase MMP3/stromelysin-1 promotes mammary carcinogenesis. Cell, 98, 137–146.

    Article  PubMed  CAS  Google Scholar 

  83. Ha, H. Y., Moon, H. B., Nam, M. S., Lee, J. W., Ryoo, Z. Y., Lee, T. H., et al. (2001). Overexpression of membrane-type matrix me0talloproteinase-1 gene induces mammary gland abnormalities and adenocarcinoma in transgenic mice. Cancer research, 61, 984–990.

    PubMed  CAS  Google Scholar 

  84. Radisky, D. C., Levy, D. D., Littlepage, L. E., Liu, H., Nelson, C. M., Fata, J. E., et al. (2005). Rac1b and reactive oxygen species mediate MMP-3-induced EMT and genomic instability. Nature, 436, 123–127.

    Article  PubMed  CAS  Google Scholar 

  85. McCawley, L. J., Wright, J., LaFleur, B. J., Crawford, H. C., & Matrisian, L. M. (2008). Keratinocyte expression of MMP3 enhances differentiation and prevents tumor establishment. American journal of pathology, 173, 1528–1539.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We apologize to those whose work could not be cited due to space limitations. This work was supported by the Office of Biological and Environmental Research of the Department of Energy (DOE-AC03-76SF00098), the National Institutes of Health (CA112970-01), (R01CA057621) to Zena Werb and M.J.B., (R01CA064786) to M.J.B. and the Breast Cancer Research Program (BCRP) of the Department of Defense (DOD) (Innovator Award) to M.J.B. M.JB. is a Distinguished Scientist of the OBER Office of the DOE. Support was also provided by a DOD BCRP postdoctoral fellowship DAMD17-02-1-0441 to R.X., a predoctoral fellowship W81XWH-05-1-0339 to A.T.B, and by a California BCRP Dissertation Award to ATB.

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Correspondence to Ren Xu or Mina J. Bissell.

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Xu, R., Boudreau, A. & Bissell, M.J. Tissue architecture and function: dynamic reciprocity via extra- and intra-cellular matrices. Cancer Metastasis Rev 28, 167–176 (2009). https://doi.org/10.1007/s10555-008-9178-z

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