• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of transbhomepageaboutsubmitalertseditorial board
Philos Trans R Soc Lond B Biol Sci. Jun 29, 1998; 353(1370): 857–870.
PMCID: PMC1692274

Tissue architecture: the ultimate regulator of epithelial function?


The architecture of a tissue is defined by the nature and the integrity of its cellular and extracellular compartments, and is based on proper adhesive cell-cell and cell-extracellular matrix interactions. Cadherins and integrins are major adhesion-mediators that assemble epithelial cells together laterally and attach them basally to a subepithelial basement membrane, respectively. Because cell adhesion complexes are linked to the cytoskeleton and to the cellular signalling pathways, they represent checkpoints for regulation of cell shape and gene expression and thus are instructive for cell behaviour and function. This organization allows a reciprocal flow of mechanical and biochemical information between the cell and its microenvironment, and necessitates that cells actively maintain a state of homeostasis within a given tissue context. The loss of the ability of tumour cells to establish correct adhesive interactions with their microenvironment results in disruption of tissue architecture with often fatal consequences for the host organism. This review discusses the role of cell adhesion in the maintenance of tissue structure and analyses how tissue structure regulates epithelial function.

Full Text

The Full Text of this article is available as a PDF (382K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Adams JC, Watt FM. Regulation of development and differentiation by the extracellular matrix. Development. 1993 Apr;117(4):1183–1198. [PubMed]
  • Alexander CM, Howard EW, Bissell MJ, Werb Z. Rescue of mammary epithelial cell apoptosis and entactin degradation by a tissue inhibitor of metalloproteinases-1 transgene. J Cell Biol. 1996 Dec;135(6 Pt 1):1669–1677. [PMC free article] [PubMed]
  • Alford D, Taylor-Papadimitriou J. Cell adhesion molecules in the normal and cancerous mammary gland. J Mammary Gland Biol Neoplasia. 1996 Apr;1(2):207–218. [PubMed]
  • Alman BA, Li C, Pajerski ME, Diaz-Cano S, Wolfe HJ. Increased beta-catenin protein and somatic APC mutations in sporadic aggressive fibromatoses (desmoid tumors). Am J Pathol. 1997 Aug;151(2):329–334. [PMC free article] [PubMed]
  • Ballard ST, Hunter JH, Taylor AE. Regulation of tight-junction permeability during nutrient absorption across the intestinal epithelium. Annu Rev Nutr. 1995;15:35–55. [PubMed]
  • Barcellos-Hoff MH, Aggeler J, Ram TG, Bissell MJ. Functional differentiation and alveolar morphogenesis of primary mammary cultures on reconstituted basement membrane. Development. 1989 Feb;105(2):223–235. [PMC free article] [PubMed]
  • Barth AI, Pollack AL, Altschuler Y, Mostov KE, Nelson WJ. NH2-terminal deletion of beta-catenin results in stable colocalization of mutant beta-catenin with adenomatous polyposis coli protein and altered MDCK cell adhesion. J Cell Biol. 1997 Feb 10;136(3):693–706. [PMC free article] [PubMed]
  • Beaulieu JF, Vachon PH. Reciprocal expression of laminin A-chain isoforms along the crypt-villus axis in the human small intestine. Gastroenterology. 1994 Apr;106(4):829–839. [PubMed]
  • Behrens J, Mareel MM, Van Roy FM, Birchmeier W. Dissecting tumor cell invasion: epithelial cells acquire invasive properties after the loss of uvomorulin-mediated cell-cell adhesion. J Cell Biol. 1989 Jun;108(6):2435–2447. [PMC free article] [PubMed]
  • Behrens J, Vakaet L, Friis R, Winterhager E, Van Roy F, Mareel MM, Birchmeier W. Loss of epithelial differentiation and gain of invasiveness correlates with tyrosine phosphorylation of the E-cadherin/beta-catenin complex in cells transformed with a temperature-sensitive v-SRC gene. J Cell Biol. 1993 Feb;120(3):757–766. [PMC free article] [PubMed]
  • Behrens J, von Kries JP, Kühl M, Bruhn L, Wedlich D, Grosschedl R, Birchmeier W. Functional interaction of beta-catenin with the transcription factor LEF-1. Nature. 1996 Aug 15;382(6592):638–642. [PubMed]
  • Bissell MJ, Barcellos-Hoff MH. The influence of extracellular matrix on gene expression: is structure the message? J Cell Sci Suppl. 1987;8:327–343. [PubMed]
  • Bissell MJ, Hall HG, Parry G. How does the extracellular matrix direct gene expression? J Theor Biol. 1982 Nov 7;99(1):31–68. [PubMed]
  • Borradori L, Sonnenberg A. Hemidesmosomes: roles in adhesion, signaling and human diseases. Curr Opin Cell Biol. 1996 Oct;8(5):647–656. [PubMed]
  • Boudreau N, Sympson CJ, Werb Z, Bissell MJ. Suppression of ICE and apoptosis in mammary epithelial cells by extracellular matrix. Science. 1995 Feb 10;267(5199):891–893. [PMC free article] [PubMed]
  • Boudreau N, Werb Z, Bissell MJ. Suppression of apoptosis by basement membrane requires three-dimensional tissue organization and withdrawal from the cell cycle. Proc Natl Acad Sci U S A. 1996 Apr 16;93(8):3509–3513. [PMC free article] [PubMed]
  • Boyer B, Vallés AM, Tucker GC, Delouvée A, Thiery JP. Involvement of cell motility in tumor progression. Symp Soc Exp Biol. 1993;47:183–195. [PubMed]
  • Briand P, Petersen OW, Van Deurs B. A new diploid nontumorigenic human breast epithelial cell line isolated and propagated in chemically defined medium. In Vitro Cell Dev Biol. 1987 Mar;23(3):181–188. [PubMed]
  • Briand P, Nielsen KV, Madsen MW, Petersen OW. Trisomy 7p and malignant transformation of human breast epithelial cells following epidermal growth factor withdrawal. Cancer Res. 1996 May 1;56(9):2039–2044. [PubMed]
  • Bruckner-Tuderman L. Collagen VII and bullous disorders of the skin. Dermatology. 1994;189 (Suppl 2):16–20. [PubMed]
  • Bruckner-Tuderman L. Blistering skin diseases: models for studies on epidermal-dermal adhesion. Biochem Cell Biol. 1996;74(6):729–736. [PubMed]
  • Burgeson RE, Chiquet M, Deutzmann R, Ekblom P, Engel J, Kleinman H, Martin GR, Meneguzzi G, Paulsson M, Sanes J, et al. A new nomenclature for the laminins. Matrix Biol. 1994 Apr;14(3):209–211. [PubMed]
  • Campbell KP. Three muscular dystrophies: loss of cytoskeleton-extracellular matrix linkage. Cell. 1995 Mar 10;80(5):675–679. [PubMed]
  • Chen LH, Bissell MJ. A novel regulatory mechanism for whey acidic protein gene expression. Cell Regul. 1989 Nov;1(1):45–54. [PMC free article] [PubMed]
  • Chiquet M, Matthisson M, Koch M, Tannheimer M, Chiquet-Ehrismann R. Regulation of extracellular matrix synthesis by mechanical stress. Biochem Cell Biol. 1996;74(6):737–744. [PubMed]
  • Chiquet-Ehrismann R, Tannheimer M, Koch M, Brunner A, Spring J, Martin D, Baumgartner S, Chiquet M. Tenascin-C expression by fibroblasts is elevated in stressed collagen gels. J Cell Biol. 1994 Dec;127(6 Pt 2):2093–2101. [PMC free article] [PubMed]
  • Cress AE, Rabinovitz I, Zhu W, Nagle RB. The alpha 6 beta 1 and alpha 6 beta 4 integrins in human prostate cancer progression. Cancer Metastasis Rev. 1995 Sep;14(3):219–228. [PubMed]
  • Damsky CH, Richa J, Solter D, Knudsen K, Buck CA. Identification and purification of a cell surface glycoprotein mediating intercellular adhesion in embryonic and adult tissue. Cell. 1983 Sep;34(2):455–466. [PubMed]
  • Daniel CW, Strickland P, Friedmann Y. Expression and functional role of E- and P-cadherins in mouse mammary ductal morphogenesis and growth. Dev Biol. 1995 Jun;169(2):511–519. [PubMed]
  • Dauça M, Bouziges F, Colin S, Kedinger M, Keller MK, Schilt J, Simon-Assmann P, Haffen K. Development of the vertebrate small intestine and mechanisms of cell differentiation. Int J Dev Biol. 1990 Mar;34(1):205–218. [PubMed]
  • Deng G, Lu Y, Zlotnikov G, Thor AD, Smith HS. Loss of heterozygosity in normal tissue adjacent to breast carcinomas. Science. 1996 Dec 20;274(5295):2057–2059. [PubMed]
  • Dimitratos SD, Woods DF, Bryant PJ. Camguk, Lin-2, and CASK: novel membrane-associated guanylate kinase homologs that also contain CaM kinase domains. Mech Dev. 1997 Apr;63(1):127–130. [PubMed]
  • Doyle JP, Stempak JG, Cowin P, Colman DR, D'Urso D. Protein zero, a nervous system adhesion molecule, triggers epithelial reversion in host carcinoma cells. J Cell Biol. 1995 Oct;131(2):465–482. [PMC free article] [PubMed]
  • Dufour S, Saint-Jeannet JP, Broders F, Wedlich D, Thiery JP. Differential perturbations in the morphogenesis of anterior structures induced by overexpression of truncated XB- and N-cadherins in Xenopus embryos. J Cell Biol. 1994 Oct;127(2):521–535. [PMC free article] [PubMed]
  • Ekblom P, Timpl R. Cell-to-cell contact and extracellular matrix. A multifaceted approach emerging. Curr Opin Cell Biol. 1996 Oct;8(5):599–601. [PubMed]
  • Fannon AM, Sherman DL, Ilyina-Gragerova G, Brophy PJ, Friedrich VL, Jr, Colman DR. Novel E-cadherin-mediated adhesion in peripheral nerve: Schwann cell architecture is stabilized by autotypic adherens junctions. J Cell Biol. 1995 Apr;129(1):189–202. [PMC free article] [PubMed]
  • Friedrichs K, Ruiz P, Franke F, Gille I, Terpe HJ, Imhof BA. High expression level of alpha 6 integrin in human breast carcinoma is correlated with reduced survival. Cancer Res. 1995 Feb 15;55(4):901–906. [PubMed]
  • Frixen UH, Behrens J, Sachs M, Eberle G, Voss B, Warda A, Löchner D, Birchmeier W. E-cadherin-mediated cell-cell adhesion prevents invasiveness of human carcinoma cells. J Cell Biol. 1991 Apr;113(1):173–185. [PMC free article] [PubMed]
  • Fujimori T, Takeichi M. Disruption of epithelial cell-cell adhesion by exogenous expression of a mutated nonfunctional N-cadherin. Mol Biol Cell. 1993 Jan;4(1):37–47. [PMC free article] [PubMed]
  • Fujita S, Suzuki H, Kinoshita M, Hirohashi S. Inhibition of cell attachment, invasion and metastasis of human carcinoma cells by anti-integrin beta 1 subunit antibody. Jpn J Cancer Res. 1992 Dec;83(12):1317–1326. [PubMed]
  • Fujita S, Watanabe M, Kubota T, Teramoto T, Kitajima M. Alteration of expression in integrin beta 1-subunit correlates with invasion and metastasis in colorectal cancer. Cancer Lett. 1995 May 4;91(1):145–149. [PubMed]
  • Gamallo C, Palacios J, Suarez A, Pizarro A, Navarro P, Quintanilla M, Cano A. Correlation of E-cadherin expression with differentiation grade and histological type in breast carcinoma. Am J Pathol. 1993 Apr;142(4):987–993. [PMC free article] [PubMed]
  • Glukhova M, Koteliansky V, Sastre X, Thiery JP. Adhesion systems in normal breast and in invasive breast carcinoma. Am J Pathol. 1995 Mar;146(3):706–716. [PMC free article] [PubMed]
  • Gould KA, Dove WF. Localized gene action controlling intestinal neoplasia in mice. Proc Natl Acad Sci U S A. 1997 May 27;94(11):5848–5853. [PMC free article] [PubMed]
  • Gumbiner BM. Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell. 1996 Feb 9;84(3):345–357. [PubMed]
  • Gumbiner BM. Carcinogenesis: a balance between beta-catenin and APC. Curr Biol. 1997 Jul 1;7(7):R443–R446. [PubMed]
  • Hahn U, Stallmach A, Hahn EG, Riecken EO. Basement membrane components are potent promoters of rat intestinal epithelial cell differentiation in vitro. Gastroenterology. 1990 Feb;98(2):322–335. [PubMed]
  • Hay ED, Zuk A. Transformations between epithelium and mesenchyme: normal, pathological, and experimentally induced. Am J Kidney Dis. 1995 Oct;26(4):678–690. [PubMed]
  • Hazan RB, Kang L, Whooley BP, Borgen PI. N-cadherin promotes adhesion between invasive breast cancer cells and the stroma. Cell Adhes Commun. 1997 Mar;4(6):399–411. [PubMed]
  • Hermiston ML, Gordon JI. In vivo analysis of cadherin function in the mouse intestinal epithelium: essential roles in adhesion, maintenance of differentiation, and regulation of programmed cell death. J Cell Biol. 1995 Apr;129(2):489–506. [PMC free article] [PubMed]
  • Hermiston ML, Gordon JI. Inflammatory bowel disease and adenomas in mice expressing a dominant negative N-cadherin. Science. 1995 Nov 17;270(5239):1203–1207. [PubMed]
  • Hermiston ML, Wong MH, Gordon JI. Forced expression of E-cadherin in the mouse intestinal epithelium slows cell migration and provides evidence for nonautonomous regulation of cell fate in a self-renewing system. Genes Dev. 1996 Apr 15;10(8):985–996. [PubMed]
  • Hilkens J, Vos HL, Wesseling J, Boer M, Storm J, van der Valk S, Calafat J, Patriarca C. Is episialin/MUC1 involved in breast cancer progression? Cancer Lett. 1995 Mar 23;90(1):27–33. [PubMed]
  • Howlett AR, Bailey N, Damsky C, Petersen OW, Bissell MJ. Cellular growth and survival are mediated by beta 1 integrins in normal human breast epithelium but not in breast carcinoma. J Cell Sci. 1995 May;108(Pt 5):1945–1957. [PubMed]
  • Huber O, Korn R, McLaughlin J, Ohsugi M, Herrmann BG, Kemler R. Nuclear localization of beta-catenin by interaction with transcription factor LEF-1. Mech Dev. 1996 Sep;59(1):3–10. [PubMed]
  • Hynes RO. Integrins: versatility, modulation, and signaling in cell adhesion. Cell. 1992 Apr 3;69(1):11–25. [PubMed]
  • Hynes RO. Targeted mutations in cell adhesion genes: what have we learned from them? Dev Biol. 1996 Dec 15;180(2):402–412. [PubMed]
  • Ingber DE. Cellular tensegrity: defining new rules of biological design that govern the cytoskeleton. J Cell Sci. 1993 Mar;104(Pt 3):613–627. [PubMed]
  • Ingber DE. Tensegrity: the architectural basis of cellular mechanotransduction. Annu Rev Physiol. 1997;59:575–599. [PubMed]
  • Inomata M, Ochiai A, Akimoto S, Kitano S, Hirohashi S. Alteration of beta-catenin expression in colonic epithelial cells of familial adenomatous polyposis patients. Cancer Res. 1996 May 1;56(9):2213–2217. [PubMed]
  • Jesaitis LA, Goodenough DA. Molecular characterization and tissue distribution of ZO-2, a tight junction protein homologous to ZO-1 and the Drosophila discs-large tumor suppressor protein. J Cell Biol. 1994 Mar;124(6):949–961. [PMC free article] [PubMed]
  • Jones PH, Watt FM. Separation of human epidermal stem cells from transit amplifying cells on the basis of differences in integrin function and expression. Cell. 1993 May 21;73(4):713–724. [PubMed]
  • Jones PL, Schmidhauser C, Bissell MJ. Regulation of gene expression and cell function by extracellular matrix. Crit Rev Eukaryot Gene Expr. 1993;3(2):137–154. [PubMed]
  • Kato M, Saunders S, Nguyen H, Bernfield M. Loss of cell surface syndecan-1 causes epithelia to transform into anchorage-independent mesenchyme-like cells. Mol Biol Cell. 1995 May;6(5):559–576. [PMC free article] [PubMed]
  • Kedinger M, Simon-Assmann PM, Lacroix B, Haffen K. Role of glucocorticoids on the maturation of brush border enzymes in fetal rat gut endoderm. Experientia. 1983 Oct 15;39(10):1150–1152. [PubMed]
  • Kedinger M, Simon-Assmann P, Bouziges F, Haffen K. Epithelial-mesenchymal interactions in intestinal epithelial differentiation. Scand J Gastroenterol Suppl. 1988;151:62–69. [PubMed]
  • Keely PJ, Wu JE, Santoro SA. 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. 1995 Jul;59(1):1–13. [PubMed]
  • Kemler R. From cadherins to catenins: cytoplasmic protein interactions and regulation of cell adhesion. Trends Genet. 1993 Sep;9(9):317–321. [PubMed]
  • Kemperman H, Wijnands Y, Wesseling J, Niessen CM, Sonnenberg A, Roos E. The mucin epiglycanin on TA3/Ha carcinoma cells prevents alpha 6 beta 4-mediated adhesion to laminin and kalinin and E-cadherin-mediated cell-cell interaction. J Cell Biol. 1994 Dec;127(6 Pt 2):2071–2080. [PMC free article] [PubMed]
  • Kim SK. Tight junctions, membrane-associated guanylate kinases and cell signaling. Curr Opin Cell Biol. 1995 Oct;7(5):641–649. [PubMed]
  • Kintner C. Regulation of embryonic cell adhesion by the cadherin cytoplasmic domain. Cell. 1992 Apr 17;69(2):225–236. [PubMed]
  • Kinzler KW, Vogelstein B. Lessons from hereditary colorectal cancer. Cell. 1996 Oct 18;87(2):159–170. [PubMed]
  • Koretz K, Schlag P, Boumsell L, Möller P. Expression of VLA-alpha 2, VLA-alpha 6, and VLA-beta 1 chains in normal mucosa and adenomas of the colon, and in colon carcinomas and their liver metastases. Am J Pathol. 1991 Mar;138(3):741–750. [PMC free article] [PubMed]
  • Korinek V, Barker N, Morin PJ, van Wichen D, de Weger R, Kinzler KW, Vogelstein B, Clevers H. Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC-/- colon carcinoma. Science. 1997 Mar 21;275(5307):1784–1787. [PubMed]
  • Koukoulis GK, Virtanen I, Korhonen M, Laitinen L, Quaranta V, Gould VE. Immunohistochemical localization of integrins in the normal, hyperplastic, and neoplastic breast. Correlations with their functions as receptors and cell adhesion molecules. Am J Pathol. 1991 Oct;139(4):787–799. [PMC free article] [PubMed]
  • Kühl M, Wedlich D. Wnt signalling goes nuclear. Bioessays. 1997 Feb;19(2):101–104. [PubMed]
  • Leivo I, Tani T, Laitinen L, Bruns R, Kivilaakso E, Lehto VP, Burgeson RE, Virtanen I. Anchoring complex components laminin-5 and type VII collagen in intestine: association with migrating and differentiating enterocytes. J Histochem Cytochem. 1996 Nov;44(11):1267–1277. [PubMed]
  • Lelièvre S, Weaver VM, Bissell MJ. Extracellular matrix signaling from the cellular membrane skeleton to the nuclear skeleton: a model of gene regulation. Recent Prog Horm Res. 1996;51:417–432. [PMC free article] [PubMed]
  • Li ML, Aggeler J, Farson DA, Hatier C, Hassell J, Bissell MJ. 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 Jan;84(1):136–140. [PMC free article] [PubMed]
  • Ligtenberg MJ, Buijs F, Vos HL, Hilkens J. Suppression of cellular aggregation by high levels of episialin. Cancer Res. 1992 Apr 15;52(8):2318–2324. [PubMed]
  • Lin CQ, Dempsey PJ, Coffey RJ, Bissell MJ. 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. J Cell Biol. 1995 May;129(4):1115–1126. [PMC free article] [PubMed]
  • Lochter A, Bissell MJ. Involvement of extracellular matrix constituents in breast cancer. Semin Cancer Biol. 1995 Jun;6(3):165–173. [PubMed]
  • Lochter A, Srebrow A, Sympson CJ, Terracio N, Werb Z, Bissell MJ. Misregulation of stromelysin-1 expression in mouse mammary tumor cells accompanies acquisition of stromelysin-1-dependent invasive properties. J Biol Chem. 1997 Feb 21;272(8):5007–5015. [PubMed]
  • Lochter A, Galosy S, Muschler J, Freedman N, Werb Z, Bissell MJ. Matrix metalloproteinase stromelysin-1 triggers a cascade of molecular alterations that leads to stable epithelial-to-mesenchymal conversion and a premalignant phenotype in mammary epithelial cells. J Cell Biol. 1997 Dec 29;139(7):1861–1872. [PMC free article] [PubMed]
  • Lund LR, Rømer J, Thomasset N, Solberg H, Pyke C, Bissell MJ, Danø K, Werb Z. Two distinct phases of apoptosis in mammary gland involution: proteinase-independent and -dependent pathways. Development. 1996 Jan;122(1):181–193. [PMC free article] [PubMed]
  • Madara JL. Maintenance of the macromolecular barrier at cell extrusion sites in intestinal epithelium: physiological rearrangement of tight junctions. J Membr Biol. 1990 Jun;116(2):177–184. [PubMed]
  • Madsen MW, Lykkesfeldt AE, Laursen I, Nielsen KV, Briand P. Altered gene expression of c-myc, epidermal growth factor receptor, transforming growth factor-alpha, and c-erb-B2 in an immortalized human breast epithelial cell line, HMT-3522, is associated with decreased growth factor requirements. Cancer Res. 1992 Mar 1;52(5):1210–1217. [PubMed]
  • Mareel MM, Van Roy FM, De Baetselier P. The invasive phenotypes. Cancer Metastasis Rev. 1990 Jul;9(1):45–62. [PubMed]
  • Mareel MM, Van Roy FM, Bracke ME. How and when do tumor cells metastasize? Crit Rev Oncog. 1993;4(5):559–594. [PubMed]
  • Marti A, Feng Z, Altermatt HJ, Jaggi R. Milk accumulation triggers apoptosis of mammary epithelial cells. Eur J Cell Biol. 1997 Jun;73(2):158–165. [PubMed]
  • Matsuyoshi N, Hamaguchi M, Taniguchi S, Nagafuchi A, Tsukita S, Takeichi M. Cadherin-mediated cell-cell adhesion is perturbed by v-src tyrosine phosphorylation in metastatic fibroblasts. J Cell Biol. 1992 Aug;118(3):703–714. [PMC free article] [PubMed]
  • Mercurio AM. Laminin receptors: achieving specificity through cooperation. Trends Cell Biol. 1995 Nov;5(11):419–423. [PubMed]
  • Moyret C, Madsen MW, Cooke J, Briand P, Theillet C. Gradual selection of a cellular clone presenting a mutation at codon 179 of the p53 gene during establishment of the immortalized human breast epithelial cell line HMT-3522. Exp Cell Res. 1994 Dec;215(2):380–385. [PubMed]
  • Natali PG, Nicotra MR, Botti C, Mottolese M, Bigotti A, Segatto O. Changes in expression of alpha 6/beta 4 integrin heterodimer in primary and metastatic breast cancer. Br J Cancer. 1992 Aug;66(2):318–322. [PMC free article] [PubMed]
  • Nielsen KV, Briand P. Cytogenetic analysis of in vitro karyotype evolution in a cell line established from nonmalignant human mammary epithelium. Cancer Genet Cytogenet. 1989 May;39(1):103–118. [PubMed]
  • Nielsen KV, Madsen MW, Briand P. In vitro karyotype evolution and cytogenetic instability in the non-tumorigenic human breast epithelial cell line HMT-3522. Cancer Genet Cytogenet. 1994 Dec;78(2):189–199. [PubMed]
  • Orian-Rousseau V, Aberdam D, Fontao L, Chevalier L, Meneguzzi G, Kedinger M, Simon-Assmann P. Developmental expression of laminin-5 and HD1 in the intestine: epithelial to mesenchymal shift for the laminin gamma-2 chain subunit deposition. Dev Dyn. 1996 May;206(1):12–23. [PubMed]
  • Palacios J, Benito N, Pizarro A, Suárez A, Espada J, Cano A, Gamallo C. Anomalous expression of P-cadherin in breast carcinoma. Correlation with E-cadherin expression and pathological features. Am J Pathol. 1995 Mar;146(3):605–612. [PMC free article] [PubMed]
  • Perreault N, Vachon PH, Beaulieu JF. Appearance and distribution of laminin A chain isoforms and integrin alpha 2, alpha 3, alpha 6, beta 1, and beta 4 subunits in the developing human small intestinal mucosa. Anat Rec. 1995 Jun;242(2):242–250. [PubMed]
  • Petersen OW, Rønnov-Jessen L, Howlett AR, Bissell MJ. Interaction with basement membrane serves to rapidly distinguish growth and differentiation pattern of normal and malignant human breast epithelial cells. Proc Natl Acad Sci U S A. 1992 Oct 1;89(19):9064–9068. [PMC free article] [PubMed]
  • Pujuguet P, Hammann A, Martin F, Martin M. Abnormal basement membrane in tumors induced by rat colon cancer cells. Gastroenterology. 1994 Sep;107(3):701–711. [PubMed]
  • Ranscht B. Cadherins and catenins: interactions and functions in embryonic development. Curr Opin Cell Biol. 1994 Oct;6(5):740–746. [PubMed]
  • Rasbridge SA, Gillett CE, Sampson SA, Walsh FS, Millis RR. Epithelial (E-) and placental (P-) cadherin cell adhesion molecule expression in breast carcinoma. J Pathol. 1993 Feb;169(2):245–250. [PubMed]
  • Reichmann E, Ball R, Groner B, Friis RR. New mammary epithelial and fibroblastic cell clones in coculture form structures competent to differentiate functionally. J Cell Biol. 1989 Mar;108(3):1127–1138. [PMC free article] [PubMed]
  • Reichmann E, Schwarz H, Deiner EM, Leitner I, Eilers M, Berger J, Busslinger M, Beug H. Activation of an inducible c-FosER fusion protein causes loss of epithelial polarity and triggers epithelial-fibroblastoid cell conversion. Cell. 1992 Dec 24;71(7):1103–1116. [PubMed]
  • Resnick N, Gimbrone MA., Jr Hemodynamic forces are complex regulators of endothelial gene expression. FASEB J. 1995 Jul;9(10):874–882. [PubMed]
  • Resnick N, Collins T, Atkinson W, Bonthron DT, Dewey CF, Jr, Gimbron MA., Jr Platelet-derived growth factor B chain promoter contains a cis-acting fluid shear-stress-responsive element. Proc Natl Acad Sci U S A. 1993 Aug 15;90(16):7908–7908. [PMC free article] [PubMed]
  • Rønnov-Jessen L, Petersen OW, Bissell MJ. Cellular changes involved in conversion of normal to malignant breast: importance of the stromal reaction. Physiol Rev. 1996 Jan;76(1):69–125. [PubMed]
  • Roskelley CD, Bissell MJ. Dynamic reciprocity revisited: a continuous, bidirectional flow of information between cells and the extracellular matrix regulates mammary epithelial cell function. Biochem Cell Biol. 1995 Jul-Aug;73(7-8):391–397. [PubMed]
  • Roskelley CD, Desprez PY, Bissell MJ. Extracellular matrix-dependent tissue-specific gene expression in mammary epithelial cells requires both physical and biochemical signal transduction. Proc Natl Acad Sci U S A. 1994 Dec 20;91(26):12378–12382. [PMC free article] [PubMed]
  • Roskelley CD, Srebrow A, Bissell MJ. A hierarchy of ECM-mediated signalling regulates tissue-specific gene expression. Curr Opin Cell Biol. 1995 Oct;7(5):736–747. [PMC free article] [PubMed]
  • Rousselle P, Keene DR, Ruggiero F, Champliaud MF, Rest M, Burgeson RE. Laminin 5 binds the NC-1 domain of type VII collagen. J Cell Biol. 1997 Aug 11;138(3):719–728. [PMC free article] [PubMed]
  • Rubinfeld B, Robbins P, El-Gamil M, Albert I, Porfiri E, Polakis P. Stabilization of beta-catenin by genetic defects in melanoma cell lines. Science. 1997 Mar 21;275(5307):1790–1792. [PubMed]
  • Ryan MC, Christiano AM, Engvall E, Wewer UM, Miner JH, Sanes JR, Burgeson RE. The functions of laminins: lessons from in vivo studies. Matrix Biol. 1996 Dec;15(6):369–381. [PubMed]
  • Sakakura T. New aspects of stroma-parenchyma relations in mammary gland differentiation. Int Rev Cytol. 1991;125:165–202. [PubMed]
  • Sanderson IR, Ezzell RM, Kedinger M, Erlanger M, Xu ZX, Pringault E, Leon-Robine S, Louvard D, Walker WA. Human fetal enterocytes in vitro: modulation of the phenotype by extracellular matrix. Proc Natl Acad Sci U S A. 1996 Jul 23;93(15):7717–7722. [PMC free article] [PubMed]
  • Schmidhauser C, Casperson GF, Myers CA, Sanzo KT, Bolten S, Bissell MJ. A novel transcriptional enhancer is involved in the prolactin- and extracellular matrix-dependent regulation of beta-casein gene expression. Mol Biol Cell. 1992 Jun;3(6):699–709. [PMC free article] [PubMed]
  • Schmidhauser C, Casperson GF, Bissell MJ. Transcriptional activation by viral enhancers: critical dependence on extracellular matrix-cell interactions in mammary epithelial cells. Mol Carcinog. 1994 Jun;10(2):66–71. [PubMed]
  • Shaw LM, Chao C, Wewer UM, Mercurio AM. Function of the integrin alpha 6 beta 1 in metastatic breast carcinoma cells assessed by expression of a dominant-negative receptor. Cancer Res. 1996 Mar 1;56(5):959–963. [PubMed]
  • Simon-Assmann P, Kedinger M. Heterotypic cellular cooperation in gut morphogenesis and differentiation. Semin Cell Biol. 1993 Jun;4(3):221–230. [PubMed]
  • Simon-Assmann P, Duclos B, Orian-Rousseau V, Arnold C, Mathelin C, Engvall E, Kedinger M. Differential expression of laminin isoforms and alpha 6-beta 4 integrin subunits in the developing human and mouse intestine. Dev Dyn. 1994 Sep;201(1):71–85. [PubMed]
  • Simon-Assmann P, Kedinger M, De Arcangelis A, Rousseau V, Simo P. Extracellular matrix components in intestinal development. Experientia. 1995 Sep 29;51(9-10):883–900. [PubMed]
  • Sommers CL. The role of cadherin-mediated adhesion in breast cancer. J Mammary Gland Biol Neoplasia. 1996 Apr;1(2):219–229. [PubMed]
  • Sommers CL, Gelmann EP, Kemler R, Cowin P, Byers SW. Alterations in beta-catenin phosphorylation and plakoglobin expression in human breast cancer cells. Cancer Res. 1994 Jul 1;54(13):3544–3552. [PubMed]
  • Sonnenberg A, de Melker AA, Martinez de Velasco AM, Janssen H, Calafat J, Niessen CM. Formation of hemidesmosomes in cells of a transformed murine mammary tumor cell line and mechanisms involved in adherence of these cells to laminin and kalinin. J Cell Sci. 1993 Dec;106(Pt 4):1083–1102. [PubMed]
  • Stahl S, Weitzman S, Jones JC. The role of laminin-5 and its receptors in mammary epithelial cell branching morphogenesis. J Cell Sci. 1997 Jan;110(Pt 1):55–63. [PubMed]
  • Stetler-Stevenson WG, Aznavoorian S, Liotta LA. Tumor cell interactions with the extracellular matrix during invasion and metastasis. Annu Rev Cell Biol. 1993;9:541–573. [PubMed]
  • Stoker AW, Streuli CH, Martins-Green M, Bissell MJ. Designer microenvironments for the analysis of cell and tissue function. Curr Opin Cell Biol. 1990 Oct;2(5):864–874. [PubMed]
  • Streuli CH. Extracellular matrix and gene expression in mammary epithelium. Semin Cell Biol. 1993 Jun;4(3):203–212. [PubMed]
  • Streuli CH, Bissell MJ. Expression of extracellular matrix components is regulated by substratum. J Cell Biol. 1990 Apr;110(4):1405–1415. [PMC free article] [PubMed]
  • Streuli CH, Bailey N, Bissell MJ. Control of mammary epithelial differentiation: basement membrane induces tissue-specific gene expression in the absence of cell-cell interaction and morphological polarity. J Cell Biol. 1991 Dec;115(5):1383–1395. [PMC free article] [PubMed]
  • Streuli CH, Schmidhauser C, Bailey N, Yurchenco P, Skubitz AP, Roskelley C, Bissell MJ. Laminin mediates tissue-specific gene expression in mammary epithelia. J Cell Biol. 1995 May;129(3):591–603. [PMC free article] [PubMed]
  • Sympson CJ, Talhouk RS, Alexander CM, Chin JR, Clift SM, Bissell MJ, Werb Z. 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 May;125(3):681–693. [PMC free article] [PubMed]
  • Sympson CJ, Bissell MJ, Werb Z. Mammary gland tumor formation in transgenic mice overexpressing stromelysin-1. Semin Cancer Biol. 1995 Jun;6(3):159–163. [PMC free article] [PubMed]
  • Takeichi M. Cadherins in cancer: implications for invasion and metastasis. Curr Opin Cell Biol. 1993 Oct;5(5):806–811. [PubMed]
  • Talhouk RS, Bissell MJ, Werb Z. Coordinated expression of extracellular matrix-degrading proteinases and their inhibitors regulates mammary epithelial function during involution. J Cell Biol. 1992 Sep;118(5):1271–1282. [PMC free article] [PubMed]
  • Thompson EW, Torri J, Sabol M, Sommers CL, Byers S, Valverius EM, Martin GR, Lippman ME, Stampfer MR, Dickson RB. Oncogene-induced basement membrane invasiveness in human mammary epithelial cells. Clin Exp Metastasis. 1994 May;12(3):181–194. [PubMed]
  • Uematsu J, Nishizawa Y, Sonnenberg A, Owaribe K. Demonstration of type II hemidesmosomes in a mammary gland epithelial cell line, BMGE-H. J Biochem. 1994 Mar;115(3):469–476. [PubMed]
  • Utani A, Kopp JB, Kozak CA, Matsuki Y, Amizuka N, Sugiyama S, Yamada Y. Mouse kalinin B1 (laminin beta 3 chain): cloning and tissue distribution. Lab Invest. 1995 Mar;72(3):300–310. [PubMed]
  • Vleminckx K, Vakaet L, Jr, Mareel M, Fiers W, van Roy F. Genetic manipulation of E-cadherin expression by epithelial tumor cells reveals an invasion suppressor role. Cell. 1991 Jul 12;66(1):107–119. [PubMed]
  • Vleminckx KL, Deman JJ, Bruyneel EA, Vandenbossche GM, Keirsebilck AA, Mareel MM, van Roy FM. Enlarged cell-associated proteoglycans abolish E-cadherin functionality in invasive tumor cells. Cancer Res. 1994 Feb 15;54(4):873–877. [PubMed]
  • Weaver VM, Howlett AR, Langton-Webster B, Petersen OW, Bissell MJ. The development of a functionally relevant cell culture model of progressive human breast cancer. Semin Cancer Biol. 1995 Jun;6(3):175–184. [PubMed]
  • Weaver VM, Fischer AH, Peterson OW, Bissell MJ. The importance of the microenvironment in breast cancer progression: recapitulation of mammary tumorigenesis using a unique human mammary epithelial cell model and a three-dimensional culture assay. Biochem Cell Biol. 1996;74(6):833–851. [PMC free article] [PubMed]
  • Weaver VM, Petersen OW, Wang F, Larabell CA, Briand P, Damsky C, Bissell MJ. Reversion of the malignant phenotype of human breast cells in three-dimensional culture and in vivo by integrin blocking antibodies. J Cell Biol. 1997 Apr 7;137(1):231–245. [PMC free article] [PubMed]
  • Werb Z, Sympson CJ, Alexander CM, Thomasset N, Lund LR, MacAuley A, Ashkenas J, Bissell MJ. Extracellular matrix remodeling and the regulation of epithelial-stromal interactions during differentiation and involution. Kidney Int Suppl. 1996 May;54:S68–S74. [PMC free article] [PubMed]
  • Wesseling J, van der Valk SW, Hilkens J. A mechanism for inhibition of E-cadherin-mediated cell-cell adhesion by the membrane-associated mucin episialin/MUC1. Mol Biol Cell. 1996 Apr;7(4):565–577. [PMC free article] [PubMed]
  • Wewer UM, Engvall E. Laminins. Methods Enzymol. 1994;245:85–104. [PubMed]
  • Wong MH, Hermiston ML, Syder AJ, Gordon JI. Forced expression of the tumor suppressor adenomatosis polyposis coli protein induces disordered cell migration in the intestinal epithelium. Proc Natl Acad Sci U S A. 1996 Sep 3;93(18):9588–9593. [PMC free article] [PubMed]
  • Woods DF, Hough C, Peel D, Callaini G, Bryant PJ. Dlg protein is required for junction structure, cell polarity, and proliferation control in Drosophila epithelia. J Cell Biol. 1996 Sep;134(6):1469–1482. [PMC free article] [PubMed]
  • Xia Y, Gil SG, Carter WG. Anchorage mediated by integrin alpha6beta4 to laminin 5 (epiligrin) regulates tyrosine phosphorylation of a membrane-associated 80-kD protein. J Cell Biol. 1996 Feb;132(4):727–740. [PMC free article] [PubMed]
  • Zettl KS, Sjaastad MD, Riskin PM, Parry G, Machen TE, Firestone GL. Glucocorticoid-induced formation of tight junctions in mouse mammary epithelial cells in vitro. Proc Natl Acad Sci U S A. 1992 Oct 1;89(19):9069–9073. [PMC free article] [PubMed]
  • Zutter MM, Mazoujian G, Santoro SA. Decreased expression of integrin adhesive protein receptors in adenocarcinoma of the breast. Am J Pathol. 1990 Oct;137(4):863–870. [PMC free article] [PubMed]
  • Zutter MM, Krigman HR, Santoro SA. Altered integrin expression in adenocarcinoma of the breast. Analysis by in situ hybridization. Am J Pathol. 1993 May;142(5):1439–1448. [PMC free article] [PubMed]
  • Zutter MM, Santoro SA, Staatz WD, Tsung YL. Re-expression of the alpha 2 beta 1 integrin abrogates the malignant phenotype of breast carcinoma cells. Proc Natl Acad Sci U S A. 1995 Aug 1;92(16):7411–7415. [PMC free article] [PubMed]

Articles from Philosophical Transactions of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society


Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...


  • PubMed
    PubMed citations for these articles

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...