Patterned collagen fibers orient branching mammary epithelium through distinct signaling modules

Current Biology

Volumn 23, Issue 8, 2013, Pages 703-709

  Brownfield, Douglas G ^a,c   Venugopalan, Gautham ^a   Lo, Alvin ^b   Mori, Hidetoshi ^b   Tanner, Kandice ^b,d   Fletcher, Daniel A ^a,b   Bissell, Mina J ^a,b  

^a University of California at Berkeley   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 1; NEUROPEPTIDE; RAC1 PROTEIN; RAC1 PROTEIN, MOUSE; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHO KINASE; RHOA PROTEIN, MOUSE;

ANIMAL; ARTICLE; BAGG ALBINO MOUSE; CONFOCAL MICROSCOPY; EPITHELIUM; EXTRACELLULAR MATRIX; FEMALE; MESODERM; METABOLISM; MOUSE; SEXUAL MATURATION; SIGNAL TRANSDUCTION; UDDER;

ANIMALS; COLLAGEN TYPE I; EPITHELIUM; EXTRACELLULAR MATRIX; FEMALE; MAMMARY GLANDS, ANIMAL; MESODERM; MICE; MICE, INBRED BALB C; MICROSCOPY, CONFOCAL; NEUROPEPTIDES; RAC1 GTP-BINDING PROTEIN; RHO GTP-BINDING PROTEINS; RHO-ASSOCIATED KINASES; SEXUAL MATURATION; SIGNAL TRANSDUCTION;

EID: 84876774048     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2013.03.032     Document Type: Article

References (39)

1. A. Propper, and L. Gomot Control of chick epidermis differentiation by rabbit mammary mesenchyme Experientia 29 1973 1543 1544
2. T. Sakakura, Y. Nishizuka, and C.J. Dawe Mesenchyme-dependent morphogenesis and epithelium-specific cytodifferentiation in mouse mammary gland Science 194 1976 1439 1441
3. G.R. Cunha, P. Young, K. Christov, R. Guzman, S. Nandi, F. Talamantes, and G. Thordarson Mammary phenotypic expression induced in epidermal cells by embryonic mammary mesenchyme Acta Anat. (Basel) 152 1995 195 204
4. W.V. Ingman, J. Wyckoff, V. Gouon-Evans, J. Condeelis, and J.W. Pollard Macrophages promote collagen fibrillogenesis around terminal end buds of the developing mammary gland Dev. Dyn. 235 2006 3222 3229
5. M.W. Conklin, J.C. Eickhoff, K.M. Riching, C.A. Pehlke, K.W. Eliceiri, P.P. Provenzano, A. Friedl, and P.J. Keely Aligned collagen is a prognostic signature for survival in human breast carcinoma Am. J. Pathol. 178 2011 1221 1232
6. P.P. Provenzano, K.W. Eliceiri, J.M. Campbell, D.R. Inman, J.G. White, and P.J. Keely Collagen reorganization at the tumor-stromal interface facilitates local invasion BMC Med. 4 2006 38
7. R.A. Boerboom, K.N. Krahn, R.T. Megens, M.A. van Zandvoort, M. Merkx, and C.V. Bouten High resolution imaging of collagen organisation and synthesis using a versatile collagen specific probe J. Struct. Biol. 159 2007 392 399
8. R. Rezakhaniha, A. Agianniotis, J.T. Schrauwen, A. Griffa, D. Sage, C.V. Bouten, F.N. van de Vosse, M. Unser, and N. Stergiopulos Experimental investigation of collagen waviness and orientation in the arterial adventitia using confocal laser scanning microscopy Biomech. Model. Mechanobiol. 11 2012 461 473
9. M. Simian, Y. Hirai, M. Navre, Z. Werb, A. Lochter, and M.J. Bissell The interplay of matrix metalloproteinases, morphogens and growth factors is necessary for branching of mammary epithelial cells Development 128 2001 3117 3131
10. L.M. Machesky, and A. Hall Role of actin polymerization and adhesion to extracellular matrix in Rac- and Rho-induced cytoskeletal reorganization J. Cell Biol. 138 1997 913 926
11. N. Kureishy, V. Sapountzi, S. Prag, N. Anilkumar, and J.C. Adams Fascins, and their roles in cell structure and function Bioessays 24 2002 350 361
12. M.A. Wozniak, R. Desai, P.A. Solski, C.J. Der, and P.J. Keely ROCK-generated contractility regulates breast epithelial cell differentiation in response to the physical properties of a three-dimensional collagen matrix J. Cell Biol. 163 2003 583 595
13. J.E. Fata, Z. Werb, and M.J. Bissell Regulation of mammary gland branching morphogenesis by the extracellular matrix and its remodeling enzymes Breast Cancer Res. 6 2004 1 11
14. P.J. Keely, J.E. Wu, and S.A. Santoro 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 1995 1 13
15. M.S. Wicha, L.A. Liotta, B.K. Vonderhaar, and W.R. Kidwell Effects of inhibition of basement membrane collagen deposition on rat mammary gland development Dev. Biol. 80 1980 253 256
16. D. Stopak, N.K. Wessells, and A.K. Harris Morphogenetic rearrangement of injected collagen in developing chicken limb buds Proc. Natl. Acad. Sci. USA 82 1985 2804 2808
17. D. Alford, D. Baeckström, M. Geyp, P. Pitha, and J. Taylor-Papadimitriou Integrin-matrix interactions affect the form of the structures developing from human mammary epithelial cells in collagen or fibrin gels J. Cell Sci. 111 1998 521 532
18. C.M. Nelson, M.M. Vanduijn, J.L. Inman, D.A. Fletcher, and M.J. Bissell Tissue geometry determines sites of mammary branching morphogenesis in organotypic cultures Science 314 2006 298 300
19. H.G. Hall, D.A. Farson, and M.J. Bissell Lumen formation by epithelial cell lines in response to collagen overlay: a morphogenetic model in culture Proc. Natl. Acad. Sci. USA 79 1982 4672 4676
20. P. Monaghan, M.J. Warburton, N. Perusinghe, and P.S. Rudland Topographical arrangement of basement membrane proteins in lactating rat mammary gland: comparison of the distribution of type IV collagen, laminin, fibronectin, and Thy-1 at the ultrastructural level Proc. Natl. Acad. Sci. USA 80 1983 3344 3348
21. P.P. Provenzano, D.R. Inman, K.W. Eliceiri, and P.J. Keely Matrix density-induced mechanoregulation of breast cell phenotype, signaling and gene expression through a FAK-ERK linkage Oncogene 28 2009 4326 4343
22. N. Gjorevski, and C.M. Nelson Endogenous patterns of mechanical stress are required for branching morphogenesis Integr Biol (Camb) 2 2010 424 434
23. G.B. Silberstein, P. Strickland, S. Coleman, and C.W. Daniel Epithelium-dependent extracellular matrix synthesis in transforming growth factor-beta 1-growth-inhibited mouse mammary gland J. Cell Biol. 110 1990 2209 2219
24. B.E. Hall, C. Zheng, W.D. Swaim, A. Cho, C.N. Nagineni, M.A. Eckhaus, K.C. Flanders, I.S. Ambudkar, B.J. Baum, and A.B. Kulkarni Conditional overexpression of TGF-β1 disrupts mouse salivary gland development and function Lab. Invest. 90 2010 543 555
25. D. Vader, A. Kabla, D. Weitz, and L. Mahadevan Strain-induced alignment in collagen gels PLoS ONE 4 2009 e5902
26. T.S. Girton, V.H. Barocas, and R.T. Tranquillo Confined compression of a tissue-equivalent: collagen fibril and cell alignment in response to anisotropic strain J. Biomech. Eng. 124 2002 568 575
27. T.T. Tower, M.R. Neidert, and R.T. Tranquillo Fiber alignment imaging during mechanical testing of soft tissues Ann. Biomed. Eng. 30 2002 1221 1233
28. M.J. Naylor, N. Li, J. Cheung, E.T. Lowe, E. Lambert, R. Marlow, P. Wang, F. Schatzmann, T. Wintermantel, and G. Schüetz Ablation of β1 integrin in mammary epithelium reveals a key role for integrin in glandular morphogenesis and differentiation J. Cell Biol. 171 2005 717 728
29. F. Berdichevsky, D. Alford, B. D'Souza, and J. Taylor-Papadimitriou Branching morphogenesis of human mammary epithelial cells in collagen gels J. Cell Sci. 107 1994 3557 3568
30. R. Pankov, Y. Endo, S. Even-Ram, M. Araki, K. Clark, E. Cukierman, K. Matsumoto, and K.M. Yamada A Rac switch regulates random versus directionally persistent cell migration J. Cell Biol. 170 2005 793 802
31. N. Xia, C.K. Thodeti, T.P. Hunt, Q. Xu, M. Ho, G.M. Whitesides, R. Westervelt, and D.E. Ingber Directional control of cell motility through focal adhesion positioning and spatial control of Rac activation FASEB J. 22 2008 1649 1659
32. I. Migeotte, T. Omelchenko, A. Hall, and K.V. Anderson Rac1-dependent collective cell migration is required for specification of the anterior-posterior body axis of the mouse PLoS Biol. 8 2010 e1000442
33. Y. Hashimoto, M. Parsons, and J.C. Adams Dual actin-bundling and protein kinase C-binding activities of fascin regulate carcinoma cell migration downstream of Rac and contribute to metastasis Mol. Biol. Cell 18 2007 4591 4602
34. T. Watanabe, S. Wang, J. Noritake, K. Sato, M. Fukata, M. Takefuji, M. Nakagawa, N. Izumi, T. Akiyama, and K. Kaibuchi Interaction with IQGAP1 links APC to Rac1, Cdc42, and actin filaments during cell polarization and migration Dev. Cell 7 2004 871 883
35. Y. Nishimura, K. Applegate, M.W. Davidson, G. Danuser, and C.M. Waterman Automated screening of microtubule growth dynamics identifies MARK2 as a regulator of leading edge microtubules downstream of Rac1 in migrating cells PLoS ONE 7 2012 e41413
36. H. Kouros-Mehr, and Z. Werb Candidate regulators of mammary branching morphogenesis identified by genome-wide transcript analysis Dev. Dyn. 235 2006 3404 3412
37. C.L. Guo, M. Ouyang, J.Y. Yu, J. Maslov, A. Price, and C.Y. Shen Long-range mechanical force enables self-assembly of epithelial tubular patterns Proc. Natl. Acad. Sci. USA 109 2012 5576 5582
38. T. Vargo-Gogola, B.M. Heckman, E.J. Gunther, L.A. Chodosh, and J.M. Rosen P190-B Rho GTPase-activating protein overexpression disrupts ductal morphogenesis and induces hyperplastic lesions in the developing mammary gland Mol. Endocrinol. 20 2006 1391 1405
39. A.J. Ewald, A. Brenot, M. Duong, B.S. Chan, and Z. Werb Collective epithelial migration and cell rearrangements drive mammary branching morphogenesis Dev. Cell 14 2008 570 581