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PMID: 7536749 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Antibodies against domain E3 of laminin-1 and integrin alpha 6 subunit perturb branching epithelial morphogenesis of submandibular gland, but by different modes.

The Journal of cell biology ·Vol. 129 ·No. 2 ·1995-04-00 ·Pages 521-34

Kadoya Y, Kadoya K, Durbeej M, Holmvall K, Sorokin L, Ekblom P

Abstract

Branching epithelial morphogenesis requires interactions between the surrounding mesenchyme and the epithelium, as well as interactions between basement membrane components and the epithelium. Embryonic submandibular gland was used to study the roles of two mesenchymal proteins, epimorphin and tenascin-C, as well as the epithelial protein laminin-1 and one of its integrin receptors on branching morphogenesis. Laminin-1 is a heterotrimer composed of an alpha 1 chain and two smaller chains (beta 1 and gamma 1). Immunofluorescence revealed a transient expression of laminin alpha 1 chain in the epithelial basement membrane during early stages of branching morphogenesis. Other laminin-1 chains and alpha 6, beta 1, and beta 4 integrin subunits seemed to be expressed constitutively. Expression of epimorphin, but not tenascin-C, was seen in the mesenchyme during early developmental stages, but a mAb against epimorphin did not perturb branching morphogenesis of this early epithelium. In contrast, inhibition of branching morphogenesis was seen with a mAb against the carboxy terminus of laminin alpha 1 chain, the E3 domain. An inhibition of branching was also seen with a mAb against the integrin alpha 6 subunit. The antibodies against laminin alpha 1 chain and integrin alpha 6 subunit perturbed development in distinct fashions. Whereas treatment with the anti-E3 resulted in discontinuities of the basement membrane at the tips of the branching epithelium, treatment with the mAb against alpha 6 integrin subunit seemed to leave the basement membrane intact. We suggest that the laminin E3 domain is involved in basement membrane formation, whereas alpha 6 beta 1 integrin binding to laminin-1 may elicit differentiation signals to the epithelial cells.

MeSH Terms
Animals Animals, Newborn Antibodies, Monoclonal Base Sequence Basement Membrane/chemistry,ultrastructure Cadherins/analysis Cell Adhesion Molecules, Neuronal/analysis,physiology Epithelium/physiology Extracellular Matrix Proteins/analysis,physiology Gene Expression Regulation, Developmental Integrin alpha6 Integrin alpha6beta1 Integrins/analysis,immunology,physiology Laminin/analysis,immunology,physiology Membrane Glycoproteins/analysis,immunology,physiology Mesoderm/chemistry Mice Molecular Sequence Data Morphogenesis Organ Culture Techniques RNA, Messenger/analysis Submandibular Gland/embryology,physiology Tenascin
Chemicals
Antibodies, Monoclonal Cadherins Cell Adhesion Molecules, Neuronal Epim protein, mouse Extracellular Matrix Proteins Integrin alpha6 Integrin alpha6beta1 Integrins Laminin Membrane Glycoproteins RNA, Messenger Tenascin nidogen
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Kadoya Y
Department of Animal Physiology, Uppsala University, Sweden.
Kadoya K
Durbeej M
Holmvall K
Sorokin L
Ekblom P
References (59)
59 references, click to expand
  1. Purification and structural characterization of intact and fragmented nidogen obtained from a tumor basement membrane.
    Eur J Biochem. 1986 May 2;156(3):467-78 PMID: 3084254
  2. Identification of a putative cell adhesion domain of uvomorulin.
    EMBO J. 1985 Dec 16;4(13A):3393-8 PMID: 2419126
  3. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction.
    Anal Biochem. 1987 Apr;162(1):156-9 PMID: 2440339
  4. Role of laminin A chain in the development of epithelial cell polarity.
    Cell. 1988 Oct 21;55(2):331-41 PMID: 3048705
  5. Laminin, a multidomain protein. The A chain has a unique globular domain and homology with the basement membrane proteoglycan and the laminin B chains.
    J Biol Chem. 1988 Nov 15;263(32):16536-44 PMID: 3182802
  6. The high-affinity binding of laminin to cells. Assignation of a major cell-binding site to the long arm of laminin and of a latent cell-binding site to its short arms.
    Eur J Biochem. 1989 Mar 1;180(1):9-14 PMID: 2651126
  7. Structure and biological activity of basement membrane proteins.
    Eur J Biochem. 1989 Apr 1;180(3):487-502 PMID: 2653817
  8. Identification of integrin-like matrix receptors with affinity for interstitial collagens.
    J Biol Chem. 1989 Jul 25;264(21):12686-94 PMID: 2545715
  9. Intracellular accumulation of basement membrane components during morphogenesis of rat submandibular gland.
    J Histochem Cytochem. 1989 Sep;37(9):1387-92 PMID: 2768808
  10. Tenascin-C, tenascin-R and tenascin-X: a family of talented proteins in search of functions.
    Curr Opin Cell Biol. 1993 Oct;5(5):869-76 PMID: 7694605
  11. The laminin family.
    Curr Opin Cell Biol. 1993 Oct;5(5):877-82 PMID: 8240830
  12. Cell and heparin binding in the distal long arm of laminin: identification of active and cryptic sites with recombinant and hybrid glycoprotein.
    J Cell Biol. 1993 Dec;123(5):1255-68 PMID: 8267779
  13. Alternative extracellular and cytoplasmic domains of the integrin alpha 7 subunit are differentially expressed during development.
    J Biol Chem. 1993 Dec 15;268(35):26773-83 PMID: 8253814
  14. Differential expression of neurotrophin receptors during renal development.
    Development. 1993 Dec;119(4):977-89 PMID: 8306895
  15. A novel laminin E8 cell adhesion site required for lung alveolar formation in vitro.
    J Cell Biol. 1994 Mar;124(6):1083-90 PMID: 8132708
  16. Expression of collagen alpha 1(IV), laminin and nidogen genes in the embryonic mouse lung: implications for branching morphogenesis.
    Mech Dev. 1994 Mar;45(3):193-201 PMID: 7516699
  17. Variants of the alpha 6 beta 1 laminin receptor in early murine development: distribution, molecular cloning and chromosomal localization of the mouse integrin alpha 6 subunit.
    Cell Adhes Commun. 1993 May;1(1):33-53 PMID: 8081870
  18. A new nomenclature for the laminins.
    Matrix Biol. 1994 Apr;14(3):209-11 PMID: 7921537
  19. Role of mesenchymal nidogen for epithelial morphogenesis in vitro.
    Development. 1994 Jul;120(7):2003-14 PMID: 7925005
  20. Regulation of cellular interactions with laminin by integrin cytoplasmic domains: the A and B structural variants of the alpha 6 beta 1 integrin differentially modulate the adhesive strength, morphology, and migration of macrophages.
    Mol Biol Cell. 1994 Jun;5(6):679-90 PMID: 7949424
  21. Sodium-dodecyl-sulfate-resistant complex formation of epimorphin monomers and interaction of the 150-kDa complex with the cell surface.
    Eur J Biochem. 1994 Nov 1;225(3):1133-9 PMID: 7957204
  22. The laminins.
    Matrix Biol. 1994 Aug;14(4):275-81 PMID: 7827749
  23. Transient and locally restricted expression of laminin A chain mRNA by developing epithelial cells during kidney organogenesis.
    Cell. 1990 Jan 26;60(2):337-46 PMID: 2404613
  24. Structure and function of laminin: anatomy of a multidomain glycoprotein.
    FASEB J. 1990 Feb 1;4(2):148-60 PMID: 2404817
  25. Heparin modulation of laminin polymerization.
    J Biol Chem. 1990 Mar 5;265(7):3981-91 PMID: 2303489
  26. Integrin recognition of different cell-binding fragments of laminin (P1, E3, E8) and evidence that alpha 6 beta 1 but not alpha 6 beta 4 functions as a major receptor for fragment E8.
    J Cell Biol. 1990 Jun;110(6):2145-55 PMID: 1693624
  27. The alpha 1/beta 1 and alpha 6/beta 1 integrin heterodimers mediate cell attachment to distinct sites on laminin.
    J Cell Biol. 1990 Jun;110(6):2175-84 PMID: 2351695
  28. 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. 1990 Sep;111(3):1265-73 PMID: 2144001
  29. Receptor functions for the integrin VLA-3: fibronectin, collagen, and laminin binding are differentially influenced by Arg-Gly-Asp peptide and by divalent cations.
    J Cell Biol. 1991 Jan;112(1):169-81 PMID: 1986004
  30. Differential expression of laminin A and B chains during development of embryonic mouse organs.
    Development. 1990 Nov;110(3):823-37 PMID: 2088723
  31. Developmental loss of laminin from the interstitial extracellular matrix correlates with decreased laminin gene expression.
    Development. 1990 Dec;110(4):1285-93 PMID: 2100263
  32. Molecular cloning of the human alpha 6 integrin subunit. Alternative splicing of alpha 6 mRNA and chromosomal localization of the alpha 6 and beta 4 genes.
    Eur J Biochem. 1991 Jul 15;199(2):425-33 PMID: 2070796
  33. Reconstruction of the basement membrane in a cultured submandibular gland.
    Anat Embryol (Berl). 1991;183(5):491-9 PMID: 1713752
  34. Identification of laminin domains involved in branching morphogenesis: effects of anti-laminin monoclonal antibodies on mouse embryonic lung development.
    Dev Biol. 1991 Aug;146(2):531-41 PMID: 1907584
  35. Branching morphogenesis of mouse salivary epithelium in basement membrane-like substratum separated from mesenchyme by the membrane filter.
    Development. 1991 Feb;111(2):327-35 PMID: 1893867
  36. The major laminin receptor of mouse embryonic stem cells is a novel isoform of the alpha 6 beta 1 integrin.
    J Cell Biol. 1991 Nov;115(3):843-50 PMID: 1833411
  37. Substitution for mesenchyme by basement-membrane-like substratum and epidermal growth factor in inducing branching morphogenesis of mouse salivary epithelium.
    Development. 1991 Jul;112(3):855-61 PMID: 1935691
  38. Cell type-specific integrin variants with alternative alpha chain cytoplasmic domains.
    Proc Natl Acad Sci U S A. 1991 Nov 15;88(22):10183-7 PMID: 1946438
  39. Skeletal myoblasts utilize a novel beta 1-series integrin and not alpha 6 beta 1 for binding to the E8 and T8 fragments of laminin.
    J Biol Chem. 1991 Dec 15;266(35):23593-601 PMID: 1748636
  40. Laminin-binding integrin alpha 7 beta 1: functional characterization and expression in normal and malignant melanocytes.
    Cell Regul. 1991 Oct;2(10):805-17 PMID: 1839357
  41. Epithelial morphogenesis.
    Cell. 1992 May 1;69(3):385-7 PMID: 1581959
  42. Epimorphin: a mesenchymal protein essential for epithelial morphogenesis.
    Cell. 1992 May 1;69(3):471-81 PMID: 1581962
  43. Monoclonal antibodies against laminin A chain fragment E3 and their effects on binding to cells and proteoglycan and on kidney development.
    Exp Cell Res. 1992 Jul;201(1):137-44 PMID: 1612119
  44. Biochemical characterization and tissue distribution of the A and B variants of the integrin alpha 6 subunit.
    J Cell Biol. 1993 Apr;121(1):179-91 PMID: 7681434
  45. Recombinant laminin G domain mediates myoblast adhesion and heparin binding.
    J Biol Chem. 1993 Apr 15;268(11):8356-65 PMID: 8463343
  46. Is epimorphin involved in vesicular transport?
    Cell. 1993 May 7;73(3):425-6 PMID: 8490959
  47. Reexamination of the properties of epimorphin and its possible roles.
    Cell. 1993 May 7;73(3):426-7 PMID: 8490960
  48. A single EGF-like motif of laminin is responsible for high affinity nidogen binding.
    EMBO J. 1993 May;12(5):1879-85 PMID: 8491180
  49. A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin.
    J Cell Biol. 1993 Aug;122(4):809-23 PMID: 8349731
  50. Distribution of alpha 6 integrin subunit in developing mouse submandibular gland.
    J Histochem Cytochem. 1993 Nov;41(11):1707-14 PMID: 8409377
  51. A monoclonal antibody against an activation epitope on mouse integrin chain beta 1 blocks adhesion of lymphocytes to the endothelial integrin alpha 6 beta 1.
    Proc Natl Acad Sci U S A. 1993 Oct 1;90(19):9051-5 PMID: 7692444
  52. An analysis of salivary gland morphogenesis: role of cytoplasmic microfilaments and microtubules.
    Dev Biol. 1972 Jan;27(1):38-54 PMID: 5009494
  53. Influence of oxygen and culture media on plating efficiency of some mammalian tissue cells.
    J Natl Cancer Inst. 1972 Dec;49(6):1705-12 PMID: 4675109
  54. Collagen involvement in branching morphogenesis of embryonic lung and salivary gland.
    Dev Biol. 1980 Jun 1;77(1):84-102 PMID: 7190523
  55. Organogenesis in a defined medium supplemented with transferrin.
    Cell Differ. 1981 Nov;10(5):281-8 PMID: 7307079
  56. Protease resistance and conformation of laminin.
    Eur J Biochem. 1982 Mar;123(1):63-72 PMID: 7040076
  57. Subunits of laminin are differentially synthesized in mouse eggs and early embryos.
    Dev Biol. 1983 Apr;96(2):467-71 PMID: 6403399
  58. The heparin-binding domain of laminin is responsible for its effects on neurite outgrowth and neuronal survival.
    EMBO J. 1984 Jul;3(7):1463-8 PMID: 6745238
  59. Tenascin: an extracellular matrix protein involved in tissue interactions during fetal development and oncogenesis.
    Cell. 1986 Oct 10;47(1):131-9 PMID: 2428505
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
DOI
10.1083/jcb.129.2.521
Published
1995-04-00
Pages
521-34
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2199919
Subset
IM
External Links
PubMed source DOI: 10.1083/jcb.129.2.521 PMC Full Text View journal details
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