Extracellular matrix signaling: Integration of form and function in normal and malignant cells

Current Opinion in Cell Biology

Volumn 10, Issue 5, 1998, Pages 640-646

  Boudreau, Nancy ^a   Bissell, Mina J ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION MOLECULE; CELL RECEPTOR; GROWTH FACTOR; GROWTH FACTOR RECEPTOR; INTEGRIN; SCLEROPROTEIN;

CANCER CELL; CARCINOGENESIS; CELL ADHESION; CELL DIFFERENTIATION; CELL STRUCTURE; CHROMATIN; EXTRACELLULAR MATRIX; GENE EXPRESSION; GENE FUNCTION; GENE MUTATION; HOMEOBOX; HUMAN; HUMAN CELL; MALIGNANT TRANSFORMATION; MORPHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; REGULATOR GENE; REVIEW; SIGNAL TRANSDUCTION; TISSUE DIFFERENTIATION; TISSUE SPECIFICITY;

EID: 0031713433     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0955-0674(98)80040-9     Document Type: Article

References (55)

1. Weaver VM, Petersen OW, Wang F, Larabell CA, Briand P, Damsky C, Bissell MJ. Reversion of the malignant phenotype of human breast cells in 3-dimensional culture and in vivo using integrin blocking antibodies. of outstanding interest J Cell Biol. 137:1997;231-245 This paper elegantly demonstrates that, by restoring normal cell - ECM interactions, by blocking signaling from inappropriately expressed integrins, it is possible to restore growth arrest and a differentiated phenotype in otherwise malignant breast epithelial cells. Furthermore, growth arrest could be achieved despite the fact that these cells had already acquired a significant number of genotypic abnormalities, including amplification of growth promoting genes such as c-myc.
2. Spinardi L, Einheber S, Cullen T, Milner TA, Giancotti FG. A recombinant tall-less integrin beta 4 subunit disrupts hemidesmosomes, but does not suppress alpha 6 beta 4-mediated cell adhesion to laminins. J Cell Biol. 129:1995;473-487.
3. Clarke AS, Lotz MM, Chao C, Mercurio AM. Activation of the p21 pathway of growth arrest and apoptosis by the beta 4 integrin cytoplasmic domain. J Biol Chem. 270:1995;22673-22676.
4. 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. 108:1995;1945-1957.
5. Shaw LM, Rabinovitz I, Wang HH-F, Toker A, Mercurio AM. Activation of phosphoinositide 3-OH kinase by the α6β4 integrin promotes carcinoma invasion. of special interest Cell. 91:1997;949-960 This is the first demonstration that the laminin receptor, α6β4 could contribute to the invasive behavior of tumor cells. Furthermore, it demonstrates that ligation of α6β4 could selectively activate the phosphatidylinositol 3-kinase signaling cascade. Also, although α6β4 had been linked to proliferation of keratinocytes, it has also been linked to growth arrest in mammary and intestinal epithelial cells.
6. Hall A. Rho GTPases and the actin cytoskeleton. Science. 279:1998;509-514.
7. Keeley PJ, Westwick JK, Whitehead IP, Der CJ, Parise LV. Cdc42 and Rac1 induce integrin-mediated cell motility and invasiveness through PI(3)K. of special interest Nature. 390:1977;632-636 This paper documents the role of the actin-cytoskeleton-modulating proteins, Rac and Cdc42, in extracellular-matrix - integrin mediated metastasis of breast epithelial cells.
8. Barrett K, Leptin M, Settleman J. The Rho GTPase and a putative RhoGEF mediate a signaling pathway for the cell shape changes in Drosophila gastrulation. Cell. 91:1997;905-915.
9. Rezniczek GA, dePereda JM, Reipert S, Wiche G. Linking integrin alpha 6 beta 4-based cell adhesion to the intermediate filament cytoskeleton: direct interaction between the beta 4 subunit and plectin at multiple molecular sites. J Cell Biol. 141:1998;209-225.
10. Biffo S, Sanvito F, Costa S, Preve L, Pignatelli R, Spinardi L, Marchisio PC. Isolation of a novel beta4 integrin-binding protein (p27(BBP)) highly expressed in epithelial cells. J Biol Chem. 272:1997;30314-30321.
11. Hannigan GE, Lueng-Hagesteijn C, Fitz-Gibbon L, Coppolino MG, Radeva G, Filmus J, Bell JC, Dedhar S. Regulation of cell adhesion and anchorage-dependent growth by a new β1-integrin linked protein kinase. Nature. 379:1996;91-96.
12. Novak A, Hsu SC, Leung-Hagesteijn C, Radeva G, Papkoff J, Montesano R, Roskelley CD, Grosschedl R, Dedhar S. Cell adhesion and the integrin-linked kinase regulate the LEF-1 and beta-catenin signaling pathways. Proc Natl Acad Sci USA. 95:1998;4374-4379.
13. Hodivala KJ, Watt FM. Evidence that cadherins play a role in the downregulation of integrin expression that occurs during keratinocyte terminal differentiation. J Cell Biol. 124:1994;589-600.
14. Huttenlocher A, Lakonishok M, Kinder M, Wu S, Truong T, Knudsen KA, Horwitz AF. Integrin and cadherin synergy regulates contact inhibition of migration and motile activity. of special interest J Cell Biol. 141:1998;515-526 Although individual α5 integrin-expressing myoblasts readily migrate, contact between these cells results in an inhibition of migration and motile activity. Furthermore, although these cells express increased levels of N-cadherin which enhances cell - cell contact, additional input from the α5 integrin was necessary to stop all motile activity. Together this demonstrates how the coordinated activities of integrins and cadherins contribute to a particular phenotype.
15. Monier-Gavelle F, Duband JL. Cross talk between adhesion molecules: control of N-cadherin activity by intracellular signals elicited by beta1 and beta3 integrins in migrating neural crest cells. J Cell Biol. 137:1997;1663-1681.
16. Miyamoto S, Teramoto H, Gutkind JS, Yamada KM. Integrins can collaborate with growth factors for phosphorylation of receptor tyrosine kinases and MAP kinase activation: roles of integrin aggregation and occupancy of receptors. J Cell Biol. 135:1996;1633-1642.
17. Elicieri BP, Klemke R, Stromblad S, Cheresh DA. Integrin αvβ3 requirement for sustained mitogen-activated protein kinase activity during angiogenesis. J Cell Biol. 140:1998;1255-1263.
18. Schneller M, Vuori K, Ruoslahti E. Alpha v beta 3 integrin associates with activated insulin and PDGF beta receptors and potentiates the biological activity of PDGF. EMBO J. 16:1997;5600-5607.
19. Jones PL, Crack J, Rabinovitch M. Regulation of tenascin-C, a vascular smooth muscle cell survival factor that interacts with the alpha v beta 3 integrin to promote epidermal growth factor receptor phosphorylation and growth. J Cell Biol. 139:1997;279-293.
20. Grabham PW, Goldberg DJ. Nerve growth factor stimulates the accumulation of beta1-integrin at the tips of filopodia in the growth cones of sympathetic neurons. J Neurosci. 17:1997;5455-5465.
21. Condic ML, LeToumeau PC. Ligand-induced changes in integrin expression regulate neuronal adhesion and neurite outgrowth. Nature. 389:1997;852-856.
22. Chen CS, Mrksich M, Huang S, Whitesides GM, Ingber DE. Geometric control of cell life and death. of special interest Science. 276:1997;1425-1428 Using patterned grids coated with predetermined concentrations of extracellular matrix molecules or immobilized antibodies against integrin receptors, the authors showed that the cellular response could be modulated by changing only the area which the cell occupied. When cells were allowed to spread they could proliferate, while cells forced to become round usually underwent apoptosis, despite maintaining a similar degree of ECM - integrin contact.
23. Kheradmand F, Werner E, Tremble P, Symons M, Werb Z. Role of Rac1 and oxygen radicals in collagenase-1 expression induced by cell shape change. of outstanding interest Science. 280:1998;898-901 Although collagenase expression in synovial fibroblasts requires ligation of the α5β1 integrin receptor, the authors show that the downstream pathway activated by this receptor is dependent upon cell shape. Whereas round cells require subsequent activation of Rac1, flattened cells could activate collagenase expression via α5β1 in the presence of a dominant-negative mutant of Rac 1.
24. Boudreau N, Sympson CJ, Werb Z, Bissell MJ. Suppression of ICE and apoptosis in mammary epithelial cells by extracellular matrix. Science. 267:1995;891-893.
25. Chen Z-L, Strickland S. Neuronal death in the hippocampus is promoted by plasmin-catalyzed degradation of laminin. Cell. 91:1997;917-925.
26. Goldfinger LE, Stack SM, Jones JCR. Processing of laminin-5 and its functional consequences: role of plasmin and tissue-type plasminogen activator. of special interest J Cell Biol. 141:1998;255-265 Laminin was found to either promote or impair epithelial cell motility. Consequently, it was noted that the capacity of the epithelial cell to enzymatically process laminin was responsible for these divergent responses. In this case, proteolytically cleaved laminin contributed to impaired motility.
27. Gianelli G, Falk-Marziller J, Schiraldi O, Stetler-Stevenson WG, Quaranta V. Induction of cell migration by matrix metalloprotease-2 cleavage of laminin-5. of special interest Science. 277:1997;225-228 Matrix-metalloproteinase-processed laminin-5, but not intact laminin-5, resulted in enhanced keratinocyte motility. Since both native laminin-5 and matrix-metalloproteinase-cleaved laminin-5 require interaction with the α3β1 integrin receptor, the implication was that different signals might be activated by intact versus proteolyzed fragments of the same molecule.
28. Montgomery AM, Reisfeld RA, Cheresh DA. Integrin alpha v beta 3 rescues melanoma cells from apoptosis in three-dimensional dermal collagen. Proc Natl Acad Sci USA. 91:1994;8856-8860.
29. Zhong C, Chrzanowska-Wodnicka M, Brown J, Shaub A, Belkin AM, Burridge K. Rho-mediated contractility exposes a cryptic site in fibronectin and induces fibronectin matrix assembly. J Cell Biol. 141:1998;539-551.
30. Fischer D, Brown-Ludi M, Schulthess T, Chiquet-Erismann R. Concerted action of tenascin-C domains in cell adhesion, anti-adhesion and promotion of neurite outgrowth. J Cell Sci. 110:1997;1513-1522.
31. Care A, Silvani A, Meccia E, Mattia G, Stoppacciaro A, Parmiani G, Peschle C, Colombo MP. Hox B7 constitutively activates basic FGF in melanomas. Mol Cell Biol. 16:1996;4842-4851.
32. Boylan JF, Lohnes D, Teneja R, Chambon P, Gudas LJ. Loss of retinoic acid receptor gamma function in F9 cell by gene disruption results in aberrant Hoxa-1 expression and differentiation upon retinoic acid treatment. Proc Natl Acad Sci USA. 90:1993;9601-9605.
33. Streuli CH, Bissell MJ. Expression of extracellular matrix components is regulated by substratum. J Cell Biol. 110:1990;1405-1415.
34. Edelman GM, Jones FS. Outside and downstream of the homeobox. J Biol Chem. 268:1993;20683-20686.
35. Li C, Gudas LJ. Murine laminin B1 gene regulation during the retinoic acid and dibutyrl cAMP induced differentiation of embryonic F9 teratocarcinoma stem cells. J Biol Chem. 271:1996;6810-6818.
36. Wang W, Wei W, Desai T, Ward DC, Kaufmann SJ. Localization of the α7-integrin gene on human chromosome 12q13: clustering of integrin and Hox genes implies parallel evolution of these gene families. Genomics. 26:1995;563-570.
37. Boudreau N, Andrews C, Srebrow A, Ravanpay A, Cheresh DA. Hox D3 induces an angiogenic phenotype. of special interest J Cell Biol. 139:1997;257-264 The authors show that during angiogenesis expression of HOXD3 allows endothelial cells to upregulate αvβ3 integrin and the urokinase plasminogen activator (u-PA). In the presence of basement membrane, however, Hoxd3 expression is suppressed in these cells, and αvβ3 and u-PA expression are also downregulated, thereby allowing endothelial cells to resume a quiescent differentiated state.
38. Safeei R. A target of the Hox B5 gene from mouse nervous system. Dev Brain Res. 100:1997;5-12.
39. Volpe MV, Martin A, Vosatka RJ, Mazzoni CL, Neilson HC. HOX B5 expression in the developing mouse lung suggests a role in branching morphogenesis and epithelial fate. Histochem Cell Biol. 108:1997;495-504.
40. Sympson CJ, Talhouk RS, Alexander CM, Chin SK, 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. 125:1994;681-693.
41. Bissell MJ, Hall HG, Parry G. How does the extracellular matrix direct gene expression? J Theor Biol. 99:1982;31-68.
42. Chariot A, Moreau L, Senterre G, Sobel ME, Castronovo V. Retinoic acid induces three newly cloned hox A1 transcripts in MCF7 breast cancer cells. Biochem Biophys Res Commun. 215:1995;713-720.
43. Srebrow A, Friedmann Y, Daniel CW, Bissell MJ. Expression of hoxa 1 and hox b-7 is regulated by ECM dependent signals in mammary epithelial cells. of special interest J Cell Biochem. 69:1998;377-391 This paper demonstrates how basement membrane is required to decrease expression of two homeobox genes in cultured mammary epithelial cells and in vivo. Furthermore, the basement membrane-induced morphological changes but not the associated growth arrest are necessary for this suppression of Hoxa1 and Hoxb7 expression.
44. Cillo C, Cantile M, Mortarini R, Barba P, Parmiani G, Anichini A. Differential patterns of HOX gene expression are associated with specific integrin and ICAM profiles in clonal populations isolated from a single human melanoma metastasis. Int J Cancer. 66:1996;692-697.
45. Rots NY, Liu M, Anderson EC, Freedman LP. A differential screen for ligand-regulated genes: Identification of Hox A10 as a target of vitamin D3 induction in myeloid cells. Mol Cell Biol. 18:1998;1911-1918.
46. + mRNA and ribosomal RNA are recruited to focal adhesion complexes initiated by endothelial cell binding to microbeads coated with fibronectin or β1 integrin antibodies but not other cell surface molecules. Furthermore, this recruitment was dependent upon an intact functional cytoskeleton.
47. Kadonaga JT. Eukaryotic transcription; an interlaced network of transcription factors and chromatin modifying machines. Cell. 92:1998;307-313.
48. Myers CA, Schmidhauser C, Mellentin-Michelotti J, Fragoso G, Roskelley CD, Casperson G, Mossi R, Pujuguet P, Hager G, Bissell MJ. Characterization of BCE-1, a transcriptional enhancer regulated by prolactin and extracellular matrix and modulated by the state of histone acetylation. of outstanding interest Mol Cell Biol. 18:1998;2184-2195 Although cells cultured in the presence or absence of basement membrane each express similar profiles of essential transcription factors, only those cultured on basement membrane are capable of transcriptionally activating the β-casein enhancer. In the absence of basement membrane, transcriptional activity could be induced by modulating the acetylation state of histones, suggesting that the basement membrane may evoke tissue-specific gene expression through such a mechanism.
49. Ogryzko VV, Schiltz RL, Russanova V, Howeard BH, Nakatani Y. The transcriptional coactivators p300 and CBP are histone acetyltransferases. Cell. 87:1996;953-959.
50. Mink S, Haenig B, Klempnauer KH, Spemann H. Interaction and functional collaboration of p300 and C/EBPβ Mol Cell Biol. 11:1997;6609-6617.
51. Missero C, Calautti E, Eckner R, Chin J, Tsai LH, Livingston DM, Dotto GP. Involvement of the cell-cycle inhibitor Clp1/waf1 and the E1A-associated p300 protein in terminal differentiation. Proc Natl Acad Sci USA. 92:1995;5451-5455.
52. Goh KL, Yang JT, Hynes RO. Mesodermal defects and cranial neural crest apoptosis in alpha 5 integrin-null embryos. Development. 124:1997;4309-4319.
53. Lorentz O, Duluc I, De Arcangelis A, Simon-Assmann P, Kedinger M, Freund J-N. Key role of the Cdx2 homeobox gene in extracellular matrix-mediated intestinal cell differentiation. of special interest J Cell Biol. 139:1997;1553-1565 This paper shows that when intestinal epithelial cells are cultured on basement membrane, expression of Cdx2 homeobox gene is induced. The Cdx2 gene in turn upregulates expression of laminin and integrin β4, which are required for the tissue-specific gene expression and differentiation of these cells.
54. Ryoo HM, Hoffmann HM, Beumer T, Frenkel B, Towler DA, Stein GS, Stein JL, van Wijnen AJ, Lian JB. Stage-specific expression of Dix-5 during osteoblast differentiation; involvement in regulation of osteocalcin gene expression. Mol Endocrinol. 11:1997;1681-1694.
55. Taniguchi Y, Komatsu N, Moriuchi T. Overexpression of the HOX4A (HOXD3) homeobox gene in human erythroleukemia HEL cells results in altered adhesive properties. Blood. 85:1995;2786-2794.