Laminin and β1 integrins are crucial for normal mammary gland development in the mouse

Developmental Biology

Volumn 215, Issue 1, 1999, Pages 13-32

  Klinowska, Teresa C M ^a   Soriano, Jesus V ^b   Edwards, Gwynneth M ^a   Oliver, Janine M ^a   Valentijn, Anthony J ^a   Montesano, Roberto ^b   Streuli, Charles H ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

Author keywords

Extracellular matrix; Hepatocyte growth factor; Integrin; Laminin; Morphogenesis; Mouse mammary gland

Indexed keywords

INTEGRIN; LAMININ; BETA1 INTEGRIN; COLLAGEN; MONOCLONAL ANTIBODY;

ANIMAL TISSUE; ARTICLE; BREAST DEVELOPMENT; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EXTRACELLULAR MATRIX; IMMUNOCYTOCHEMISTRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ANIMAL; APOPTOSIS; CELL ADHESION; CYTOLOGY; DRUG ANTAGONISM; FEMALE; GROWTH, DEVELOPMENT AND AGING; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; INSTITUTE FOR CANCER RESEARCH MOUSE; KINETICS; MITOSIS; MORPHOGENESIS; MOUSE STRAIN; PHYSIOLOGY; SEXUAL MATURATION; UDDER;

ANIMALIA;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD29; APOPTOSIS; CELL ADHESION; COLLAGEN; EXTRACELLULAR MATRIX; FEMALE; IMMUNOHISTOCHEMISTRY; KINETICS; LAMININ; MAMMARY GLANDS, ANIMAL; MICE; MICE, INBRED ICR; MICE, INBRED STRAINS; MITOSIS; MORPHOGENESIS; SEXUAL MATURATION;

EID: 0033216536     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.1999.9435     Document Type: Article

References (64)

1. Abraham W. M., Sielczak M. W., Ahmed A., Cortes A., Lauredo I. T., Kim J., Pepinsky B., Benjamin C. D., Leone D. R., Lobb R. R. Alpha 4-integrins mediate antigen-induced late bronchial responses and prolonged airway hyperresponsiveness in sheep. J. Clin. Invest. 93:1994;776-787.
2. Adler S., Chen X. Anti-Fx1A antibody recognizes a beta 1-integrin on glomerular epithelial cells and inhibits adhesion and growth. Am. J. Physiol. 262:1992;F770-776.
3. Agbas A., Sarras M. P. Jr. Evidence for cell surface extracellular matrix binding proteins in Hydra vulgaris. Cell Adhes. Commun. 2:1994;59-73.
4. Alford D., Baeckstrom D., Geyp M., Pitha P., Taylor Papadimitriou J. 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.
5. Ashkenas J., Muschler J., Bissell M. J. The extracellular matrix in epithelial biology: Shared molecules and common themes in distant phyla. Dev. Biol. 180:1996;433-444.
6. Berdichevsky F., Gilbert C., Shearer M., Taylor Papadimitriou J. Collagen-induced rapid morphogenesis of human mammary epithelial cells: The role of the alpha 2 beta 1 integrin. J. Cell Sci. 102:1992;437-446.
7. Boucaut J. C., Darribere T., Boulekbache H., Thiery J. P. Prevention of gastrulation but not neurulation by antibodies to fibronectin in amphibian embryos. Nature. 307:1984;364-367.
8. Boudreau N., Sympson C. J., Werb Z., Bissell M. J. Suppression of ice and apoptosis in mammary epithelial cells by extracellular matrix. Science. 267:1995;891-893.
9. Bronner Fraser M. Alterations in neural crest migration by a monoclonal antibody that affects cell adhesion. J. Cell Biol. 101:1985;610-617.
10. Coleman S., Silberstein G. B., Daniel C. W. Ductal morphogenesis in the mouse mammary gland: Evidence supporting a role for epidermal growth factor. Dev. Biol. 127:1988;304-315.
11. Coucouvanis E., Martin G. R. Signals for death and survival - A 2-step mechanism for cavitation in the vertebrate embryo. Cell. 83:1995;279-287.
12. Daniel C. W., Berger J. J., Strickland P., Garcia R. Similar growth pattern of mouse mammary epithelium cultivated in collagen matrix in vivo and in vitro. Dev. Biol. 104:1984;57-64.
13. Daniel C. W., Strickland P., Friedmann Y. Expression and functional role of E-cadherin and P-cadherin in mouse mammary ductal morphogenesis and growth. Dev. Biol. 169:1995;511-519.
14. D'Ardenne A. J., Richman P. I., Horton M. A., McAulay A. E., Jordan S. Co-ordinate expression of the alpha-6 integrin laminin receptor sub-unit and laminin in breast cancer. J. Pathol. 165:1991;213-220.
15. Delcommenne M., Streuli C. H. Control of integrin expression by extracellular matrix. J. Biol. Chem. 270:1995;26794-26801.
16. Edwards G. M., Streuli C. H. Preparing a polyclonal antibody to mouse β1 integrin with function-blocking activity. Howlett A. Integrin Protocols. 1999;135-152 Humana Press, Clifton.
17. Edwards G. M., Wilford F. H., Liu X. W., Hennighausen L., Djiane J., Streuli C. H. Regulation of mammary differentiation by extracellular matrix involves protein-tyrosine phosphatases. J. Biol. Chem. 273:1998;9495-9500.
18. Elliott B. E., Ekblom P., Pross H., Niemann A., Rubin K. Anti-beta(1)-integrin IgG inhibits pulmonary macrometastasis and the size of micrometastases from a murine mammary-carcinoma. Cell Adhes. Commun. 1:1994;319-332.
19. Faraldo M. M., Deugnier M. A., Lukashev M., Thiery J. P., Glukhova M. A. Perturbation of beta 1-integrin function alters the development of murine mammary gland. EMBO J. 17:1998;2139-2147.
20. Farrelly N., Lee Y-J., Oliver J., Dive C., Streuli C. H. Extracellular matrix regulates apoptosis in mammary epithelium through a control on insulin signaling. J. Cell Biol. 144:1999;1337-1348.
21. Fassler R., Georges Labouesse E., Hirsch E. Genetic analyses of integrin function in mice. Curr. Opin. Cell Biol. 8:1996;641-646.
22. Fassler R., Meyer M. Consequences of lack of beta 1 integrin gene expression in mice. Genes Dev. 9:1995;1896-1908.
23. Fialka I., Schwarz H., Reichmann E., Oft M., Busslinger M., Beug H. The estrogen-dependent C-Jun ER protein causes a reversible loss of mammary epithelial cell polarity involving a destabilization of adherens junctions. J. Cell Biol. 132:1996;1115-1132.
24. Friedrichs K., Ruiz P., Franke F., Gille I., Terpe H. J., Imhof B. A. High expression level of alpha 6 integrin in human breast carcinoma is correlated with reduced survival. Cancer Res. 55:1995;901-906.
25. Globus R. K., Doty S. B., Lull J. C., Holmuhamedov E., Humphries M. J., Damsky C. H. Fibronectin is a survival factor for differentiated osteoblasts. J. Cell Sci. 111:1998;1385-1393.
26. Gorcyznski R. M., Chung S., Fu X. M., Levy G., Sullivan B., Chen Z. Manipulation of skin graft rejection in alloimmune mice by anti-VCAM-1:VLA-4 but not anti-ICAM-1:LFA-1 monoclonal antibodies. Transpl. Immunol. 3:1995;55-61.
27. Hemler M. E., Huang C., Takada Y., Schwarz L., Strominger J. L., Clabby M. L. Characterization of the cell surface heterodimer VLA-4 and related peptides. J. Biol. Chem. 262:1987;11478-11485.
28. Howard J. E., Hirst E. M., Smith J. C. Are beta 1 integrins involved in Xenopus gastrulation. Mech. Dev. 38:1992;109-119.
29. Humphreys R. C., Krajewska M., Krnacik S., Jaeger R., Weiher H., Krajewski S., Reed J. C., Rosen J. M. Apoptosis in the terminal endbud of the murine mammary gland: A mechanism of ductal morphogenesis. Development. 122:1996;4013-4022.
30. Hynes R. O. Targeted mutations in cell adhesion genes: What have we learned from them. Dev. Biol. 180:1996;402-412.
31. Johnson K. E., Darribere T., Boucaut J. C. Mesodermal cell-adhesion to fibronectin-rich fibrillar extracellular-matrix is required for normal Rana pipiens gastrulation. J. Exp. Zool. 265:1993;40-53.
32. Kadoya Y., Kadoya K., Durbeej M., Holmvall K., Sorokin L., Ekblom P. Antibodies against domain E3 of laminin-1 and integrin alpha 6 subunit perturb branching epithelial morphogenesis of submandibular gland, but by different modes. J. Cell Biol. 129:1995;521-534.
33. Keely P. J., Fong A. M., Zutter M. M., Santoro S. A. Alteration of collagen-dependent adhesion, motility, and morphogenesis by the expression of antisense alpha(2) integrin messenger-RNA in mammary cells. J. Cell Sci. 108:1995;595-607.
34. Kleinberg D. L. Early mammary development: Growth hormone and IGF-1. J. Mam. Gland Biol. Neoplasia. 2:1997;49-57.
35. Koukoulis G. K., Virtanen I., Korhonen M., Laitinen L., Quaranta V., Gould V. E. Immunohistochemical localization of integrins in the normal, hyperplastic, and neoplastic breast. Correlations with their functions as receptors and cell adhesion molecules. Am. J. Pathol. 139:1991;787-799.
36. Lallier T., Leblanc G., Artinger K. B., Bronner Fraser M. Cranial and trunk neural crest cells use different mechanisms for attachment to extracellular matrices. Development. 116:1992;531-541.
37. Montesano R., Soriano J. V., Fialka I., Orci L. Isolation of EpH4 mammary epithelial cell subpopulations which differ in their morphogenetic properties. In Vitro Cell Dev. Biol. Anim. 34:1998;468-477.
38. Pullan S., Streuli C. H. The mammary gland epithelial cell. Harris A. Epithelial Cell Culture. 1996;97-121 Cambridge Univ. Press, Cambridge.
39. Pullan S., Wilson J., Metcalfe A., Edwards G. M., Goberdhan N., Tilly J., Hickman J. A., Dive C., Streuli C. H. Requirement of basement membrane for the suppression of programmed cell death in mammary epithelium. J. Cell Sci. 109:1996;631-642.
40. Richards J., Guzman R., Konrad M., Yang J., Nandi S. Growth of mouse mammary gland end buds cultured in a collagen gel matrix. Exp. Cell Res. 141:1982;433-443.
41. Robinson S. D., Silberstein G. B., Roberts A. B., Flanders K. C., Daniel C. W. Regulated expression and growth inhibitory effects of transforming growth factor-beta isoforms in mouse mammary gland development. Development. 113:1991;867-878.
42. Saelman E. U. M., Keely P. J., Santoro S. A. Loss of MDCK cell alpha-2-beta-1 integrin expression results in reduced cyst formation, failure of hepatocyte growth-factor scatter factor-induced branching morphogenesis, and increased apoptosis. J. Cell Sci. 108:1995;3531-3540.
43. Silberstein G. B., Daniel C. W. Elvax 40P implants: Sustained, local release of bioactive molecules influencing mammary ductal development. Dev. Biol. 93:1982;272-278.
44. Silberstein G. B., Daniel C. W. Reversible inhibition of mammary gland growth by transforming growth factor-beta. Science. 237:1987;291-293.
45. Silberstein G. B., Strickland P., Coleman S., Daniel C. W. Epithelium-dependent extracellular matrix synthesis in transforming growth factor-beta 1-growth-inhibited mouse mammary gland. J. Cell Biol. 110:1990;2209-2219.
46. Snedeker S. M., Brown C. F., Diagustine R. P. Expression and functional properties of transforming growth factor-alpha and epidermal growth factor during mouse mammary gland ductal morphogenesis. Proc. Natl. Acad. Sci. USA. 88:1991;276-280.
47. Sonnenberg A., Daams H., Van der Valk M. A., Hilkens J., Hilgers J. Development of mouse mammary gland: Identification of stages in differentiation of luminal and myoepithelial cells using monoclonal antibodies and polyvalent antiserum against keratin. J. Histochem. Cytochem. 34:1986;1037-1046.
48. Sonnenberg A., Modderman P. W., Hogervorst F. Laminin receptor on platelets is the integrin VLA-6. Nature. 336:1988;487-489.
49. Soriano J. V., Orci L., Montesano R. TGF-β1 induces morphogenesis of branching cords by cloned mammary epithelial cells at subpicomolar concentrations. Biochem. Biophys. Res. Commun. 220:1996;879-885.
50. Soriano J. V., Pepper M. S., Nakamura T., Orci L., Montesano R. Hepatocyte growth factor stimulates extensive development of branching duct-like structures by cloned mammary gland epithelial cells. J. Cell Sci. 108:1995;413-430.
51. Sorokin L., Sonnenberg A., Aumailley M., Timpl R., Ekblom P. Recognition of the laminin E8 cell-binding site by an integrin possessing the alpha 6 subunit is essential for epithelial polarization in developing kidney tubules. J. Cell Biol. 111:1990;1265-1273.
52. Sorokin L. M., Conzelmann S., Ekblom P., Battaglia C., Aumailley M., Timpl R. Monoclonal antibodies against laminin A chain fragment E3 and their effects on binding to cells and proteoglycan and on kidney development. Exp. Cell Res. 201:1992;137-144.
53. Stephens L. E., Sutherland A. E., Klimanskaya I. V., Andrieux A., Meneses J., Pedersen R. A., Damsky C. H. Deletion of beta-1 integrins in mice results in inner cell mass failure and periimplantation lethality. Genes Dev. 9:1995;1883-1895.
54. Streuli C. H., Bailey N., Bissell M. J. 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. 115:1991;1383-1395.
55. Streuli C. H., Bissell M. J. Expression of extracellular matrix components is regulated by substratum. J. Cell Biol. 110:1990;1405-1415.
56. Streuli C. H., Edwards G. M., Delcommenne M., Whitelaw C. B. A., Burdon T. G., Schindler C., Watson C. J. Stat5 as a target for regulation by extracellular matrix. J. Biol. Chem. 270:1995;21639-21644.
57. Trikha M., De Clerck Y. A., Markland F. S. Contortrostatin, a snake venom disintegrin, inhibits beta 1 integrin-mediated human metastatic melanoma cell adhesion and blocks experimental metastasis. Cancer Res. 54:1994;4993-4998.
58. Weaver V. M., Petersen O. W., Wang F., Larabell C. A., Briand P., Damsky C., Bissell M. J. Reversion of the malignant phenotype of human breast cells in three-dimensional culture and in vivo by integrin blocking antibodies. J. Cell Biol. 137:1997;231-245.
59. Weg V. B., Williams T. J., Lobb R. R., Nourshargh S. A monoclonal antibody recognizing very late activation antigen-4 inhibits eosinophil accumulation in vivo. J. Exp. Med. 177:1993;561-566.
60. Wewer U. M., Shaw L. M., Albrechtsen R., Mercurio A. M. The integrin alpha 6 beta 1 promotes the survival of metastatic human breast carcinoma cells in mice. Am. J. Pathol. 151:1997;1191-1198.
61. Williams J. M., Daniel C. W. Mammary ductal elongation: Differentiation of myoepithelium and basal lamina during branching morphogenesis. Dev. Biol. 97:1983;274-290.
62. Yang Y., Spitzer E., Meyer D., Sachs M., Niemann C., Hartmann G., Weidner K. M., Birchmeier C., Birchmeier W. Sequential requirement of hepatocyte growth factor and neuregulin in the morphogenesis and differentiation of the mammary gland. J. Cell Biol. 131:1995;215-226.
63. Zutter M. M., Mazoujian G., Santoro S. A. Decreased expression of integrin adhesive protein receptors in adenocarcinoma of the breast. Am. J. Pathol. 137:1990;863-870.
64. Zutter M. M., Santoro S. A., Staatz W. D., Tsung Y. L. Reexpression of the alpha(2)beta(1) integrin abrogates the malignant phenotype of breast-carcinoma cells. Proc. Natl. Acad. Sci. USA. 92:1995;7411-7415.