Skip to main content

Advertisement

SpringerLink
Log in

Salivary gland morphogenesis and basement membranes

  • Review Article
  • Published:
Anatomical Science International Aims and scope Submit manuscript

Abstract

The basement membrane separates the epithelium from the surrounding mesenchyme and plays an essential role in the development of various epithelial-mesenchymal organs. Among these, the submandibular salivary gland (SMG) has been chosen to review the expression patterns and roles of the epithelial basement membrane and its components, in particular the laminins, during SMG morphogenesis. At the outset, a brief description of SMG development is provided with special reference to changes in the epithelial architecture and the epithelial basement membrane. The restricted expression patterns of various laminin isoforms in the developing SMGs are also summarized. Furthermore, an overview is given of several lines of experimental evidence that indicate significant but distinct roles for laminin-1 and laminin-10, their individual domains and their receptor-mediated signaling in SMG morphogenesis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Aberdam D, Aguzzi A, Baudoin C, Galliano MF, Ortonne JP, Meneguzzi G (1994) Developmental expression of nicein adhesion protein (laminin-5) subunits suggests multiple morphogenic roles. CellAdh Commun 2, 115–29.

    CAS  Google Scholar 

  • Adachi E, Hopkinson I, Hayashi T (1997) Basement-membrane stromal relationships: Interactions between collagen fibrils and the lamina densa. Int Rev Cytol 173, 73–156.

    Article  CAS  PubMed  Google Scholar 

  • Bernfield M, Banerjee SD (1982) The turnover of basal lamina glycosaminoglycan correlates with epithelial morphogenesis. DevBiol 90, 291–305.

    CAS  Google Scholar 

  • Borghese E (1950) The development in vitro of the submandibular and sublingual glands of Mus musculus. J Anat 84, 287–302.

    CAS  PubMed  Google Scholar 

  • Chan FL, Inoue S (1994) Lamina lucidaof basement membrane: An artefact. Microsc Res Tech 28, 48–59.

    Article  CAS  PubMed  Google Scholar 

  • Colognato H, Yurchenco PD (2000) Form and function: The laminin family of heterotrimers. Dev Dyn 218, 213–34.

    Article  CAS  PubMed  Google Scholar 

  • Comoglio PM, Boccaccio C, Trusolino L (2003) Interactions between growth factor receptors and adhesion molecules: Breaking the rules. Curr Opin Cell Biol 15, 565–71.

    Article  CAS  PubMed  Google Scholar 

  • Couchman JR (2003) Syndecans: Proteoglycan regulators of cell-surface microdomains? Nat Rev Mol Cell Biol 4, 926–37.

    Article  CAS  PubMed  Google Scholar 

  • Coughlin MD (1975) Early development of parasympathetic nerves in the mouse submandibular gland. Dev Biol 43, 123–39.

    Article  CAS  PubMed  Google Scholar 

  • Cutler LS, Chaudhry AP (1973) Intercellular contacts at the epithelial-mesenchymal interface during the prenatal development of the rat submandibular gland. Dev Biol 33, 229–40.

    Article  CAS  PubMed  Google Scholar 

  • Cutler LS, Chaudhry AP (1974) Cytodifferentiation of the acinar cells of the rat submandibular gland. Dev Biol 41, 32–41.

    Article  Google Scholar 

  • Cutler LS, Christian CP, Rozenski D (1991) Xylose-linked proteoglycan sysnthesis does not have a primary role in the control of secretory cell differentiation in salivary glands. Dev Biol 147, 14–21.

    Article  CAS  PubMed  Google Scholar 

  • De Arcangelis A, Mark M, Kreidberg J, Sorokin L, Georges-Labouesse E (1999) Synergistic activities of α3 and α6 integrins are required during apical ectodermal ridge formation and organogenesis in the mouse. Development 126, 3957–68.

    PubMed  Google Scholar 

  • Durbeej M, Talts JF, Henry MD, Yurchenco PD, Campbell KP, Ekblom P (2001) Dystroglycan binding to laminin α1LG4 module influences epithelial morphogenesis of salivary gland and lung in vitro. Differentiation 69, 121–34.

    Article  CAS  PubMed  Google Scholar 

  • Ekblom M, Klein G, Mugrauer G et al. (1990) Transient and locally restricted expression of laminin A chain mRNA by developing epithelial cells during kidney organogenesis. Cell 60, 337–46.

    Article  CAS  PubMed  Google Scholar 

  • Ekblom P, Lonai P, Talts JF (2003) Expression and biological role of laminin-1. Matrix Biol 22, 35–47.

    Article  CAS  PubMed  Google Scholar 

  • Erickson AC, Couchman JR (2000) Still more complexity in mammalian basement membranes. J Histochem Cytochem 48, 1291–306.

    CAS  PubMed  Google Scholar 

  • Ervasti JM, Campbell KP (1993) A role for the dystrophinglycoprotein complex as a transmembrane linker between laminin and actin. J Cell Biol 122, 809–23.

    Article  CAS  PubMed  Google Scholar 

  • Fässler R, Meyer M (1995) Consequences of lack of beta 1 integrin gene expression in mice. Genes Dev 9, 1896–908.

    Article  PubMed  Google Scholar 

  • Galliano MF, Aberdam D, Aguzzi A, Ortonne JP, Meneguzzi G (1995) Cloning and complete primary structure of the mouse laminin α3 chain. Distinct expression pattern of the laminin α3A and α3B chain isoforms. J Biol Chem 270, 21820–6.

    Article  CAS  PubMed  Google Scholar 

  • Garbe JHO, Gohring W, Mann K, Timpl R, Sasaki T (2002) Complete sequence, recombinant analysis and binding to laminins and sulphated ligands of the N-terminal domains of laminin α3B and α5 chains. Biochem J 362, 213–21.

    Article  CAS  PubMed  Google Scholar 

  • Goldberg M, Escaig-Haye F (1986) Is the lamina lucida of the basement membrane a fixation artifact? Eur J Cell Biol 42, 365–8.

    CAS  PubMed  Google Scholar 

  • Grobstein C (1953) Epithelio-mesenchymal specificity in the morphogenesis of mouse sub-mandibular rudiments in vitro. J Exp Zool 124, 383–413.

    Article  Google Scholar 

  • Handler M, Yurchenco PD, Iozzo RV (1997) Developmental expression of perlecan during murine embryogenesis. Dev Dyn 210, 130–45.

    Article  CAS  PubMed  Google Scholar 

  • Hardman P, Spooner BS (1992) Localization of extracellular matrix components in developing mouse salivary glands by confocal microscopy. Anat Rec 234, 452–9.

    Article  CAS  PubMed  Google Scholar 

  • Hieda Y, Nakanishi Y (1997) Epithelial morphogenesis in mopuse embryonic submandibular gland: Its relationships to the tissue organization of epithelium and mesenchyme. Dev Growth Differ 39, 1–8.

    Article  CAS  PubMed  Google Scholar 

  • Hoffman MP, Kidder BL, Steinberg ZL et al. (2002) Gene expression profiles of mouse submandibular gland development: FGFR1 regulates branching morphogenesis in vitro through BMP- and FGF-dependent mechanisms. Development 129, 5767–78.

    Article  CAS  PubMed  Google Scholar 

  • Hosokawa Y, Takahashi Y, Kadoya Y et al. (1999) Significant role of laminin-1 in branching morphogenesis of mouse salivary epithelium cultured in basement membrane matrix. Dev Growth Differ 41, 207–16.

    Article  CAS  PubMed  Google Scholar 

  • Hynes RO (2002) Integrins: Bidirectional, allosteric signaling machines. Cell 110, 673–87.

    Article  CAS  PubMed  Google Scholar 

  • Ikari T, Hiraki A, Seki K, Sugiura T, Matsumoto K, Shirasuna K (2003) Involvement of hepatocyte growth factor in branching morphogenesis of murine salivary gland. Dev Dyn 228, 173–84.

    Article  CAS  PubMed  Google Scholar 

  • Jacoby F, Leeson CR (1959) The postnatal development of the rat submaxillary gland. J Anat 93, 201–16.

    CAS  PubMed  Google Scholar 

  • Jaskoll T, Melnick M (1999) Submandibular gland morphogenesis: Stage-specific expression of TGF-α/EGF, IGF, TGF-β, and IL-6 signal transduction in normal embryonic mice and the phenotypic effects of TGF-β2, TGF-β3, and EGF-R null mutations. Anat Rec 256, 252–68.

    Article  CAS  PubMed  Google Scholar 

  • Jaskoll T, Zhou YM, Chai Y et al. (2001) Embryonic submandibular gland morphogenesis: Stage-specific protein localization of FGFs, BMPs, Pax6 and Pax9 in normal mice and abnormal SMG phenotypes in FgfR2-iiic+/Δ, BMP7-/- and Pax6-/- mice. Cell Tissue Organs 170, 83–98.

    Article  Google Scholar 

  • Kadoya Y, Yamashina S (1989) Intracellular accumulation of basement membrane components during morphogenesis of rat submandibular gland. J Histochem Cytochem 37, 1387–92.

    CAS  PubMed  Google Scholar 

  • Kadoya Y, Yamashina S (1991) Reconstruction of the basement membrane in a cultured submandibular gland. Anat Embryol 183, 491–9.

    Article  CAS  PubMed  Google Scholar 

  • Kadoya Y, Yamashina S (1993) Distribution of α6 integrin subunit in developing mouse submandibular gland. J Histochem Cytochem 41, 1704–14.

    Google Scholar 

  • Kadoya Y, Yamashina S (1999) Localization of laminin-5, HD1/ plectin, and BP230 in the submandibular glands of developing and adult mice. Histochem Cell Biol 112, 417–25.

    Article  CAS  PubMed  Google Scholar 

  • Kadoya Y, Kadoya K, Durbeej M, Holmvall K, Sorokin L, Ekblom P (1995) Antibodies against domain E3 of laminin-1 and integrin α6 subunit perturb branching epithelial morphogenesis of submandibular gland, but by different modes. J Cell Biol 129, 521–34.

    Article  CAS  PubMed  Google Scholar 

  • Kadoya Y, Katsumata O, Yamashina S (1997) Substructures of the acinar basement membrane of rat submandibular gland as shown by alcian blue staining and cryo-fixation followed by freeze-substitution. J Electon Microsc 46, 405–12.

    CAS  Google Scholar 

  • Kadoya Y, Nomizu M, Sorokin LM, Yamashina S, Yamada Y (1998) Laminin α1 chain G domain peptide, RKRLQVQLSIRT, inhibits epithelial branching morphogenesis of cultured embryonic mouse submandibular gland. Dev Dyn 212, 394–402.

    Article  CAS  PubMed  Google Scholar 

  • Kadoya Y, Mochizuki M, Nomizu M, Sorokin L, Yamashina S (2003) Role for laminin-α5 chain LG4 module in epithelial branching morphogenesis. Dev Biol 263, 153–64.

    Article  CAS  PubMed  Google Scholar 

  • Kashimata M, Gresik EW (1997) Epidermal growth factor system is a physiological regulator of development of the mouse fetal submandibular gland and regulates expression of the alpha6-integrin subunit. Dev Dyn 208, 149–61.

    Article  CAS  PubMed  Google Scholar 

  • Kashimata M, Sakagami H, Gresik EW (2000a) Intracellular signaling cascades activated by the EGF receptor and/or integrins, with potential relevance for branching morphogenesis of the fetal mouse submandibular gland. Eur J Morphol 38, 269–75.

    Article  CAS  PubMed  Google Scholar 

  • Kashimata M, Sayeed S, Ka A et al. (2000b) The ERK-1/2 signaling pathway involved in the stimulation of branching morphogenesis of fetal mouse submandiublar glands by EGF. Dev Biol 220, 183–96.

    Article  CAS  PubMed  Google Scholar 

  • Kikkawa Y, Moulson CL, Virtanen I, Miner JH (2002) Identification of the binding site for the Lutheran blood group glycoprotein on laminin α5 through expression of chimeric laminin chains in vivo. J Biol Chem 277, 44864–9.

    Article  CAS  PubMed  Google Scholar 

  • Koyama Y, Kashimata M, Sakashita H, Sakagami H, Gresik EG (2003) EGF-stimulated signaling by means of PI3K, PLCg1, and PKC isozymes regulates branching morphogenesis of the fetal mouse submandibularr gland. Dev Dyn 227, 216–26.

    Article  CAS  PubMed  Google Scholar 

  • Kratochwil K (1969) Organ specificity in mesenchymal induction demonstrated in the embryonic development of the mammary gland of the mouse. Dev Biol 20, 46–71.

    Article  CAS  PubMed  Google Scholar 

  • Kreidberg JA, Donovan MJ, Goldstein SL et al. (1996) Alpha 3 beta 1 integrin has a crucial role in kidney and lung organogenesis. Development 122, 3537–47.

    CAS  PubMed  Google Scholar 

  • Larsen M, Hoffman MP, Sakai T, Neibaur JC, Mitchell JM, Yamada KM (2003) Role of PI 3-kinase and PIP3 in submandibular gland branching morphogenesis. Dev Biol 255, 178–91.

    Article  CAS  PubMed  Google Scholar 

  • Laurie GW, Leblond CP (1985) Basement membrane nomenclature. Nature 313, 272.

    Article  CAS  PubMed  Google Scholar 

  • Li S, Edgar D, Fässler R, Wadsworth W, Yurchenco PD (2003) The role of laminin in embryonic cell polarization and tissue organization. Dev Cell 4, 613–24.

    Article  CAS  PubMed  Google Scholar 

  • Makino M, Okazaki I, Nishi N, Nomizu M (1999) Biologically active sequences in laminin, a multifunctional extracellular matrix protein. Connect Tissue Res 31, 227–34.

    CAS  Google Scholar 

  • Menko AS, Kreidberg JA, Ryan TT, Van Bockstaele E, Kukuruzinska MA (2001) Loss of α3β1 integrin function results in an altered differentiation program in the mouse submandibular gland. Dev Dyn 220, 337–49.

    Article  CAS  PubMed  Google Scholar 

  • Miner JH, Patton BL, Lentz SI et al. (1997) The laminin alpha chains: Expression, developmental transitions, and chromosomal locations of α1-5, identification of heterotrimeric laminins 8-11, and cloning of a novel α3 isoform. J Cell Biol 137, 685–701.

    Article  CAS  PubMed  Google Scholar 

  • Miner JH, Li C, Mudd JL, Go G, Sutherland AE (2004a) Compositional and structural requirements for laminin and basement membranes during mouse embryo implantation and gastrulation. Development 131, 2247–56.

    Article  CAS  PubMed  Google Scholar 

  • Miner JH, Li C, Patton BL (2004b) Laminins α2 and α4 in pancreatic acinar basement membranes are required for basal receptor localization. J Histochem Cytochem 52, 153–6.

    CAS  PubMed  Google Scholar 

  • Miyazaki Y, Nakanishi Y, Hieda Y (2004) Tissue interaction mediated by neuregulin-1 and ErbB receptors regulates epithelial morphogenesis of mouse embryonic submandibular gland. Dev Dyn 230, 591–6.

    Article  CAS  PubMed  Google Scholar 

  • Morita K, Nogawa H (1999) EGF-dependent lobule formation and FGF-7-dependent stalk elomgation in branching morphogenesis of mouse salivary epithelium in vitro. Dev Dyn 215, 148–54.

    Article  CAS  PubMed  Google Scholar 

  • Moulson CL, Li C, Miner JH (2001) Localization of Lutheran, a novel laminin receptor, in normal, knockout, and transgenic mice suggests an interaction with laminin α5 in vivo. Dev Dyn 222, 101–14.

    Article  CAS  PubMed  Google Scholar 

  • Nakanishi Y, Morita T, Nogawa H (1987) Cell proliferation is not required for the initiation of early cleft formation in mouse embryonic submandibular epithelium in vitro. Development 99, 429–37.

    CAS  PubMed  Google Scholar 

  • Nakanishi Y, Uematsu J, Takamatsu H, Fukuda Y, Yoshida K (1993) Removal of heparan sulfate chains halted epithelial branching morphogenesis of the developing mouse submandibular gland in vitro. Dev Growth Differ 35, 371–84.

    Article  CAS  Google Scholar 

  • Nogawa H (1983) Determination of the curvature of epithelial cell mass by mesenchyme in branching morphogenesis of mouse salivary gland. J Embryol Exp Morphol 73, 221–32.

    CAS  PubMed  Google Scholar 

  • Nogawa H, Takahashi Y (1991) Substitution for mesenchyme by basement-membrane-like substratum and epidermal growth factor in inducing branching morphogenesis of mouse salivary epithelium. Development 112, 855–61.

    CAS  PubMed  Google Scholar 

  • Orian-Rousseau V, Aberdam D, Fontao L et al. (1996) Developmental expression of laminin-5 and HD1 in the intestine: Epithelial to mesenchymal shift for the laminin gamma-2 chain subunit deposition. Dev Dyn 206, 12–23.

    Article  CAS  PubMed  Google Scholar 

  • Petajaniemi N, Korhonen M, Kortesmaa J et al. (2002) Localization of laminin α4-chain in developing and adult human tissues. J Histochem Cytochem 50, 1113–30.

    CAS  PubMed  Google Scholar 

  • Ritvos O, Tuuri T, Erämaa M et al. (1995) Activin disrupts epithelial branching morphogenesis in developing glandular organs of the mouse. Mech Dev 50, 229–45.

    Article  CAS  PubMed  Google Scholar 

  • Sakai T, Larsen M, Yamada KM (2003) Fibronectin requirement in branching morphogenesis. Nature 423, 876–61.

    Article  CAS  PubMed  Google Scholar 

  • Salmivirta M, Mali M, Heino J, Hermonen J, Jalkanen M (1994) A novel laminin-binding form of syndecan-1 (cell surface proteoglycan) producing by syndecan-1 cDNA-treated NIH- 3T3 cells. Exp Cell Res 215, 180–18.

    Article  CAS  PubMed  Google Scholar 

  • Salmivirta K, Sorokin LM, Ekblom P (1997) Differential expression of laminin alpha chains during murine tooth development. Dev Dyn 210, 206–15.

    Article  CAS  PubMed  Google Scholar 

  • Simon-Assmann P, Duclos B, Orian-Rousseau V et al. (1994) Differential expression of laminin isoforms and alpha 6-beta 4 integrin subunits in the developing human and mouse intestine. Dev Dyn 201, 71–85.

    CAS  PubMed  Google Scholar 

  • Smyth N, Vatansever HS, Murray P et al. (1999) Absence of basement membranes after targeting the LAMC1 gene results in embryonic lethality due to failure of endoderm differentiation. J Cell Biol 144, 151–60.

    Article  CAS  PubMed  Google Scholar 

  • Sorokin LM, Pausch F, Durbeej M, Ekblom P (1997) Differential expression of five laminin (1-5) chains in developing and adult mouse kidney. Dev Dyn 210, 446–62.

    Article  CAS  PubMed  Google Scholar 

  • Spooner BS, Thompson-Pletscher HA, Stokes B, Bassett KE (1986) Extracellular matrix involvement in epithelial branching morphogenesis. In: Developmental Biology: A Comprehensive Synthesis, Vol. 3, The Cell Surface in Development and Cancer (Steinberg MS, ed.). Plenum, New York, 225–60.

    Google Scholar 

  • Stephens LE, Sutherland AE, Klimanskaya IV et al. (1995) Deletion of beta 1 integrins in mice results in inner cell mass failure and periimplantation lethality. Genes Dev 9, 1883–95.

    Article  CAS  PubMed  Google Scholar 

  • Suzuki N, Nakatsuka H, Mochizuki M et al. (2003) Biological activities of homologous loop regions in the laminin α chain G domains. J Biol Chem 278, 45697–705.

    Article  CAS  PubMed  Google Scholar 

  • Thomas T, Dziadek M (1993) Genes coding for basement membrane glycoproteins laminin, nidogen, and collagen IV are differentially expressed in the nervous system and by epithelial, endothelial, and mesenchymal cells of the mouse embryo. Exp Cell Res 208, 54–67.

    Article  CAS  PubMed  Google Scholar 

  • Umeda Y, Miyazaki Y, Shiinoki H, Higashiyama S, Nakanishi Y, Hieda Y (2001) Involvement of heparin-binding EGF-like growth factor and its processing by metalloproteinases in early epithelial morphogenesis of the submandibular gland. Dev Biol 237, 202–11.

    Article  CAS  PubMed  Google Scholar 

  • Utani A, Nomizu M, Matsuura H et al. (2001) A unique sequence of the laminin α3 G domain binds to heparin and promotes cell adhesion through syndecan-2 and -4. J Biol Chem 276, 28779–88.

    Article  CAS  PubMed  Google Scholar 

  • Virtanen I, Gullberg D, Rissanen J et al. (2000) Laminin alpha1chain shows a restricted distribution in epithelial basement membranes of fetal and adult human tissues. Exp Cell Res 257, 298–309.

    Article  CAS  PubMed  Google Scholar 

  • Wessells NK, Spooner BS, Ash JF et al. (1971) Microfilaments in cellular and developmental processes. Science 171, 135–43.

    Article  CAS  PubMed  Google Scholar 

  • Williamson RA, Henry MD, Daniels KJ et al. (1997) Dystroglycan is essential for early embryonic development: Disruption of Reichert’s membrane in Dag1-null mice. Hum Mol Genet 6, 831–41.

    Article  CAS  PubMed  Google Scholar 

  • Yamada KM, Even-Ram S (2002) Integrin regulation of growth factor receptors. Nat Cell Biol 4, E75–6.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy, Kitasato University School of Medicine, 1-15-1 Kitasato, 228-8555, Sagamihara, Japan

    Yuichi Kadoya & Shohei Yamashina

Authors
  1. Yuichi Kadoya
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shohei Yamashina
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yuichi Kadoya.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kadoya, Y., Yamashina, S. Salivary gland morphogenesis and basement membranes. Anato Sci Int 80, 71–79 (2005). https://doi.org/10.1111/j.1447-073x.2005.00102.x

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1111/j.1447-073x.2005.00102.x

Key words

Search

Navigation