Abstract
Basement membranes are layered structures of the extracellular matrix which separate cells of various kinds from the surrounding stroma. One of the frequently recurring questions about basement membranes is how these structures are formed in vivo. Up to a few years ago, it was thought that basement membranes were formed spontaneously by a process of self-assembly of their components. However, it has now become clear that cell membrane receptors for basement membrane components are essential factors for the formation and stability of basement membranes in vivo. The present review highlights the modern concepts of basement membrane formation.
Similar content being viewed by others
References
Airenne T, Lin Y, Olsson M, Ekblom P, Vainio S, Tryggvason K (2000) Differential expression of mouse laminin γ 2 and γ 2* chain transcripts. Cell Tissue Res 300: 129–137
Amano S, Akutsu N, Matsunaga Y, Kadoya K, Nishiyama T, Champliaud MF, Burgeson RE, Adachi A (2001) Importance of balance between extracellular matrix synthesis and degradation in basement membrane formation. Exp Cell Res 271: 249–262.
Aumailley M, Smyth N (1998) The role of laminins in basement membrane function. J Anat 193: 1–21.
Aumailley M, Battaglia C, Mayer U, Reinhardt D, Nischt R, Timpl R, Fox JW (1993) Nidogen mediates the formation of ternary complexes of basement membrane components. Kidney Int 42, 7–12.
Aumailley M, Pesch M, Tungaal L, Gaill F, Fässler R (2000) Altered synthesis of laminin-1 and absence of basement membrane component deposition in β1-integrin deficient embryoid bodies. J Cell Sci 113: 259–268.
Baloch Z, Klapper J, Buchanan L, Schwartz M, Amenta PS (1992) Ontogenesis of the murine hepatic extracellular matrix: an immunohistochemical study. Differentiation 51: 209–218.
Banerjee SD, Cohn RH, Bernfield MR (1977) Basal lamina of embryonic salivary epithelia. Production by the epithelium and role in maintaining the lobular morphology. J Cell Biol 73: 445–463.
Battaglia C, Mayer U, Aumailley M, Timpl R (1992) Basement-membrane heparan sulfate proteoglycan binds to laminin. Eur J Biochem 208: 359–366
Bernfield MR, Banerjee SB, Cohn RH (1972) Dependence of salivary epithelial morphology and branching morphogenesis upon acid mucopolysaccharide-protein (proteoglycan) at the epithelial surface. J Cell Biol 52: 674–689.
Bernfield M, Banerjee SD, Koda JK, Rapraeger AC (1984) Remodelling of basement membrane: morphogenesis and maturation. In: Bernfield M, ed. Basement Membrane and Cell Movement. Ciba Foundation Symposium 108. London: Pitman, pp. 179–192.
Bhowmick NA, Zent R, Ghiassi M, Mcdonnel M, Moses HL (2001) Integrin β1 signaling is necessary for transforming growth factor β activation of p38MAPK and epithelial plasticity. J Biol Chem 276: 46707–46713.
Borges E, Jan Y, Ruoslahti E (2000) Platelet derived growth factor receptor β and vascular endothelial factor receptor 2 bind to the β3 integrin through its extracellular domain. J Biol Chem 275: 39867–39873.
Bouvard D, Brakebusch C, Gustafsson E, Aszodi A, Bengtsson T, Berna A, Fässler R (2001) Functional consequences of integrin gene mutations in mice. Circulation Res 89: 211–213.
Brakebusch C, Grose R, Quondamatteo F, Ramirez A, Pirro A, Svensson M, Herken R, Sasaki T, Timpl R, Werner S, Fässler R (2000) Skin and hair follicle integrity is crucially dependent on β1integrin expression on keratinocytes. EMBO J 19: 3990–4003.
Bruckner-Tudermann L, Bruckner P (1998) Genetic diseases of the extracellular matrix: more than just connective tissue disorders. J Mol Med 76: 226–237.
Burgeson RE, Chiquet M, Deutzmann R, Ekblom P, Engel J, Kleinman HK, Martin GR, Meneguzzi G, Paulsson M, Sanes J, Timpl R, Trygvasson K, Yamada Y, Yurchenco PD (1994) A new nomenclature for the laminins. Matrix Biol 14: 209–211.
Cheng YS, Champliaud MF, Burgeson RE, Marinkovich MP, Yurchenco PD (1997) Self-assembly of laminin isoforms. J Biol Chem 272: 31525–31532.
Cohn RD, Henry MD, Michele DE, Barresi R, Saito F, Moore SA, Flanagan JD, Skwarchuk MW, Robbins ME, Mendell JR, Williamson RA, Campbell KP (2002) Disruption of Dag1 in differentiated skeletal muscle reveals a role for dystroglycan in muscle regeneration. Cell 110: 639–648.
Colognato H, Yurchenco PD (1999) The laminin α2 expressed by dystrophic dy 2j mice is defective in its ability to form polymers. Current Biol 9: 1327–1330.
Colognato H, Yurchenco PD (2000) Form and function: the laminin family of heterotrimers. Dev Dyn 218: 213–234.
Colognato H, Winkelmann DA, Yurchenco PD (1999) Laminin polymerization induces a receptor-cytoskeleton network. J Cell Biol 145: 619–631.
Costell M, Gustafsson E, Aszodi A, Mörgelin M, Bloch W, Hunziker E, Addicks K, Timpl R, Fässler R (1999) Perlecan maintains the integrity of cartilage and some basement membranes. J Cell Biol 147: 1109–1122.
Cote PD, Moukhles H, Lindenbaum M, Carbonetto S (1999) Chimaeric mice deficient in dystroglycan develop muscular dystrophy and have disrupted myoneural synapses. Nat Genet 23: 338–342.
Cote PD, Moukhles H, Carbonetto S (2002) Dystroglycan is not required for localization of dystrophin, syntrophin and neuronal nitric-oxide synthase at the sarcolemma but regulates integrin α7B expression and caveolin-3 distribution. J Biol Chem 227: 4672–4679.
Couvelard A, Bringuer AF, Dauge MC, Nejjari M, Darai E, Benfila JL, Feldmann G, Henin D, Scoazec JY (1998) Expression of integrins during liver organogenesis in humans. Hepatology 26: 839–847.
Couvelard A, Scoazec JY, Dauge MC, Bringuer AF, Potet F, Feldmann G (1996) Structural and functional differentiation of sinusoidal endothelial cells during liver organogenesis in humans. Blood 87: 4568–4580.
Defilippi P, Olivo C, Venturino M, Dolce L, Silengo L, Tarone G (1999) Actin cytoskeleton organization in response to integrin-mediated adhesion. Microsc Res Techn 47: 67–78.
DiPersio CM, Hodivala-Dilke K, Jaenisch R, Kreidberg JA, Hynes RO (1997) α3β1 integrin is required for normal development of the epidermal basement membrane. J Cell Biol 137: 729–742.
Dong L, Chen Y, Lewis M, Hsieh J-C, Reing J, Chaillet JR, Howell CY, Mehlem M, Inoue S, Kuszak JR, DeGeest K, Chung AE (2002) Neurologic defects and selective disruption of basement membranes in mice lacking entactin-1/nidogen-1. Lab Invest 82: 1617–1630
Dowling J, Yu QC, Fuchs E (1996) β4 integrin is required for hemidesmosome formation, cell adhesion and cell survival. J Cell Biol 134: 559–572.
Durbeej M, Campbell KP (1999) Biochemical characterization of the epithelial dystroglycan complex. J Biol Chem 274: 26609–26616.
Durbeej M, Larsson E, Ibraghimov-Beskrovnaya O, Roberds SL, Campbell KP, Ekblom P (1995) Non-muscle α-dystroglycan is involved in epithelial development. J Cell Biol 130: 79–91.
Durbeej M, Henry MD, Ferletta M, Campbell KP, Ekblom P (1998) Distribution of dystroglycan in normal adult mouse tissues. J Histochem Cytochem 46: 449–457.
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: 121–134.
Ekblom P (1989) Developmentally regulated conversion of mesenchyme to epithelium. FASEB J 3: 2141–2150.
Ekblom P (1993). Basement membranes in development. In: Rohrbach DH, Timpl R eds. Molecular and Cellular Aspects of Basement Membranes. San Diego: Academic Press, pp. 359–383.
Ekblom P, Ekblom M, Fecker L, Klein K, Zhang HY, Kadoya Y, Chu ML, Mayer U, Timpl R (1994) Role of mesenchymal nidogen for epithelial morphogenesis in vitro. Development 120: 2003–2014.
Engel J (1993) Structure and function of laminin. In: Rohrbach DH, Timpl R eds. Molecular and Cellular Aspects of Basement Membranes. San Diego: Academic Press, pp. 147–176.
Engel J (1994) Concepts of self-assembly in biological systems. In: Yurchenco PD, Birk DE, Mecham RP eds. Extracellular Matrix Assembly and Structure. San Diego: Academic Press, pp. 1–14.
Engvall E, Wewer UM (1996) Domains of laminin. J Cell Biochem 61: 493–501.
Enzan H, Himeno H, Hiroi M, Saibara T, Onishi S (1997) Development of hepatic sinusoidal structure with special reference to the Ito cells. Microsc Res Tech 39: 336–349.
Erickson AC, Couchman JR (2000) Still more complexity in mammalian basement membranes. J Histochem Cytochem 48: 1291–1306.
Ervasti JM, Ohlendieck K, Kahl SD, Gaver MG, Campbell KP (1990) Deficiency of a glycoprotein component of the dystrophin complex in dystrophic muscle. Nature 345: 315–319.
Feltri ML, Graus-Porta D, Previtali S, Nodari A, Migliavacca B, Cassetti A, Littlewood-Evans A, Reichardt LF, Messing A, Quattrini A, Mueller U, Wrabetz L (2002) Conditional disruption of β1 integrin in Schwann cells impedes interactions with axons. J Cell Biol 156: 199–209.
Fleischmajer R, Perlish JS, Macdonald II ED, Schechter A, Murdoch AD, Iozzo RV, Yamada Y (1998a) There is binding of collagen IV to β1 integrin during early skin basement membrane assembly. Ann NY Acad Sci 857: 212–227.
Fleischmajer R, Utani A, Macdonald II ED, Perlish JS, Pan TC, Chu ML, Nomizu M, Ninomiya Y, Yamada Y (1998b) Initiation of basement membrane formation at the epidemo-dermal interface involves assembly of laminins through binding to cell membrane receptors. J Cell Sci 111: 1929–1940.
Fox JW, Mayer U, Nischt R, Aumailley M, Reinhardt D, Weidemann H, Mann K, Timpl R, Kreig T, Engel J, Chu ML (1991) Recombinant nidogen consists of three globular domains and mediates binding of laminin to collagen type IV. EMBO J 10: 3137–3146.
Freire E, Coelho-Sampaio T (2000) Self-assembly of laminin induced by acidic pH. J Biol Chem 275: 817–822.
Georges-Labouesse E, Messadeq N, Yehia G, Cadalbert L, Dierich A, Le Meur M (1996) Absence of integrin α6 leads to epidermolysis bullosa and neonatal death in mice. Nat Genet 13: 370–373.
Gesemann M, Brancaccio A, Schumacher B, Rüegg MA (1998) Agrin is a high affinity binding protein of dystroglycan in non-muscle tissue. J Biol Chem 273: 600–605.
Giancotti F, Ruoslahti E (1999) Integrin signaling. Science 285: 1028–1032.
Grant DS, Leblond CP, Kleinmann HK, Inoue S, Hassel J (1989) The incubation of laminin, collagen IV and heparan sulfate proteoglycan at 35°C yields basement membrane-like structures. J Cell Biol 108: 1567–1574.
Hahn E, Wick G, Pencev D, Timpl R (1980) Distribution of basement membrane proteins in normal and fibrotic human liver: collagen type IV, laminin and fibronectin. Gut 21: 63–71.
Halfter W, Dong S, Schurer B, Cole GJ (1998) Collagen XVIII is a basement membrane heparan sulfate proteoglycan. J Biol Chem 273: 25404–25412.
Halfter W, Dong S, Balasubramani M, Bier ME (2001) Temporary disruption of the retinal basal lamina and its effect on retinal histogenesis. Dev Biol 238: 79–96.
Hassel JR, Gehron Robey P, Barrach HJ, Wilczeck J, Rennard SI, Martin GR (1980) Isolation of heparan sulfate-containing proteoglycan from basement membrane. Proc Natl Acad Sci USA 77: 4494–4498.
Henry MD, Campbell KP (1998) A role of dystroglycan in basement membrane assembly. Cell 95: 859–870.
Henry MD, Campbell KP (1999) Dystroglycan inside and out. Curr Opin Cell Biol 11: 602–607.
Henry MD, Satz J, Brakebusch C, Costell M, Gustafsson E, Fässler R, Campbell KP (2001) Distinct roles for dystroglycan, β1-integrin and perlecan in cell surface laminin organization. J Cell Sci 114: 1137–1144.
Herken R, Barrach HJ (1985) Ultrastructural localization of type IV collagen and laminin in the seven-day-old mouse embryo. Anat Embryol 171: 365–371.
Herken R, Götz W, Wattjes KH (1989) Initial development of capillaries in the neuroepithelium of the mouse. J Anat 164: 85–92.
Herken R, Götz W, Thies M (1990) Appearance of laminin, heparan sulfate proteoglycan and collagen type IV during initial stages of vascularisation of the neuroepithelium of the mouse embryo. J Anat 169: 189–195.
Hudson BG, Reeders ST, Tryggvason K (1993) Type IV collagen: structure, gene organization and role in human diseases. J Biol Chem 268: 26033–26036.
Hynes RO (1992) Integrins: versatility, modulation and signaling in cell adhesion. Cell 69: 11–25.
Iivanaien A, Morita T, Tryggvason K (1999) Molecular cloning and tissues-specific expression of a novel murine laminin γ 3 chain. J Biol Chem 274: 14107–14111.
Inoue S (1989) Ultrastructure of basement membranes. Int Rev Cytol 117: 57–98.
Inoue S, Leblond CP, Laurie GW (1983). Ultrastructure of Reichert's membrane, a multilayered basement membrane in the parietal wall of the rat yolk sac. J Cell Biol 97: 1524–1537.
Iozzo RV (2001) Series introduction: heparan sulfate proteoglycans: intricate molecules with intriguing functions. J Clin Invest 108: 165–167.
Jacobson C, Cote P, Rossi S, Rotundo R, Carbonetto S (2001) The dystroglycan complex is necessary for stabilization of acetylcholine receptor clusters at neuromuscular junctions and formation of the synaptic basement membrane. J Cell Biol 152: 435–450.
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: 521–534.
Kadoya Y, Salmivirta K, Talts JF, Kadoya K, Mayer U, Timpl R, Ekblom P (1997) Importance of nidogen binding to laminin γ 1 for branching epithelial morphogenesis of the submandibular gland. Development 124: 683–691.
Kalb E, Engel J (1991) Binding and calcium-induced aggregation of laminin onto lipid bilayers. J Biol Chem 266: 19047–19052.
Kimura N, Toyoshima T, Kojima T, Shimane M (1998) Entactin-2: a new member of basement membrane protein with high homology to entactin/nidogen. Exp Cell Res 241: 36–45.
Klass CM, Couchmann J, Woods A (2000) Control of extracellular matrix assembly by syndecan-2 proteoglycan. J Cell Sci 113: 493–506.
Koch M, Olson PF, Albus A, Jin W, Hunter DD, Brunken WJ, Burgeson RE, Champliaud MF (1999) Characterization and expression of the laminin γ 3 chain: a novel, non-basement membrane-associated laminin chain. J Cell Biol 145: 605–617.
Kohfeld E, Sasaki T, Göhring W, Timpl R (1998) Nidogen-2: a new basement membrane protein with diverse binding properties. J Mol Biol 282: 99–109.
Kreidberg JA, Donovan MJ, Goldstein SL, Rennke H, Shepherd K, Jones RC, Jaenisch R (1996) Alpha 3 beta 1 integrin has a crucial role in kidney and lung organogenesis. Development 122: 3537–3547.
Kühn K, Glanville RW, Babel W, Qian RQ, Dieringer H, Voss T, Siebold B, Oberbäumer I, Schwarz U, Yamada Y (1985) The structure of type IV collagen. Ann NY Acad Sci 460: 14–24.
Li S, Harrison D, Carbonetto S, Fässler R, Smyth N, Edgar D, Yurchenco PD (2002) Matrix assembly, regulation and survival functions of laminin and its receptors in embryonic stem cell differentiation. J Cell Biol 157: 1279–1290.
Libby R, Champliaud MF, Claudepierre T, Xu Y, Gibbons EP, Koch M, Burgeson RE, Hunter DD, Brunken W (2000) Laminin expression in adult and developing retiane: evidence of two novel CNS laminins. J Neurosci 20: 6517–6528.
Liesi P, Kauppila T (2002) Induction of type IV collagen and other basement membrane associated proteins after spinal cord injury of the adult rat may participate in formation of the glial scar. Exp Neurol 173: 31–45.
Lohikangas L, Gullberg D, Johansson S (2001) Assembly of laminin polymers is dependent on β1-integrins. Exp Cell Res 265: 135–144.
Martinez-Hernandez A (1984) The hepatic extracellular matrix. I. Electron immunohistochemical studies in normal rat liver. Lab Invest 51: 57–74.
Martinez-Hernandez A, Amenta PS (1983) The basement membrane in pathology. Lab Invest 48: 656–677.
Martinez-Hernandez A, Martinez J (1991) The role of capillarization in hepatic failure: studies in carbon tetrachloride induced cirrhosis. Hepatology 14: 864–874.
Mayer U, Timpl R (1994) Nidogen, a versatile binding protein of basement membranes. In: Yurchenco PD, Birk DE, Mecham RP, eds. Extracellular Matrix Assembly and Structure. San Diego: Academic Press, pp. 389–416.
Miao H, Hu YL, Yuan S, Zhao Y, Chen BPC, Puzon-Mclaughin W, Tarui T, Shyy JYJ, Takada Y, Usami S, Chien S (2002) Differential regulation of Rho GTPases by β1 and β3 integrins: the role of an extracellular domain of integrin in intracellular signaling. J Cell Sci 115: 2199–2206.
Michele DE, Barresi R, Kanagawa M, Saito F, Cohn RD, Satz JS, Dollar J, Nishino I, Kelley RI, Somer H, Straub V, Mathews KD, Moore SA, Campbell KP (2002) Post-translational disruption of dystroglycan— ligand interactions in congenital muscular dystrophies. Nature 418: 417–422.
Miner JH, Patton BL, Lentz SL, GIlbert DJ, Snider WD, Jenkins NA, Copeland NG, Sanes JR (1997) The laminin α chains: expression, develpomental 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.
Miosge N (2001) The ultrastructural composition of basement membranes in vivo. Histol Histopathol 16: 1239–1248.
Miosge N, Klenczar C, Herken R, Willem M, Mayer U (1999) Organization of the myotendinous junction is dependent on the presence of α7β1 integrin. Lab Invest 79: 1591–1599.
Miosge N, Quondamatteo F, Klenczar C, Herken R (2000) Nidogen-1: expression and ultrastructural localization during the onset of mesoderm formation in the early mouse embryo. J Histochem Cytochem 48: 229–237.
Montanaro F, Lindenbaum M, Carbonetto S (1999) α-dystroglycan is a laminin receptor involved in extracellular matrix assembly on myotubes and muscle cell viability. J Cell Biol 145: 1325–1340.
Moore SA, Saito F, Chen J, Michele DE, Henry MD, Messing A, Cohn RD, Ross-Barta SE, Westra S, Williamson RA, Hoshi T, Campbell KP (2002) Deletion of brain dystroglycan recapitulates aspects of congenital muscular dystrophy. Nature 418: 422–425.
Moro L, Venturino M, Bozzo C, Silengo L, Altruda F, Beguinot L, Tarone G, Defilippi P (1998) Integrins induce activation of EGF receptor: role in MAP kinase induction and adhesion-dependent cell survival. EMBO J 17: 6622–6632.
Murdoch AD, Liu B, Schwarting R, Tuan RS, Iozzo RV (1993) Widespread expression of perlecan proteoglycan in basement membrane and extracellular matrices of human tissues as detected by a novel monoclonal antibody against domain III and by in situ hybridization. J Histochem Cytochem 42: 239–249.
Murgia C, Blaike P, Kim N, Dans M, Petrie HT, Giancotti FG (1998) Cell cycle and adhesion defects in mice carrying a targeted deletion of the integrin β4 cytoplasmic domain. EMBO J 17: 3940–3951.
Murray P, Edgar D (2000a) Regulation of programmed cell death by basement membranes in embryonic development. J Cell Biol 150: 1215–1221.
Murray P, Edgar D (2000b) Regulation of the differentiation and behaviour of extra-embryonic endodermal cells by basement membranes. J Cell Sci 114: 931–939.
Murshed M, Smyth N, Miosge N, Karolat J, Krieg T, Paulsson M, Nischt R (2000) The absence of nidogen-1 does not affect murine basement membrane formation. Mol Cell Biol 20: 7007–7012.
Noonan D, Hassel JR (1993) Proteoglycans of basement membranes. In: Rohrbach DH, Timpl R, eds. Molecular and Cellular Aspects of Basement Membranes. San Diego: Academic Press, pp. 189–210.
Parsons MJ, Campos I, Hirst EMA, Stemple D (2002) Removal of dystroglycan causes severe muscular dystrophy in zebrafish embryos. Development 129: 3505–3512.
Paulsson M (1992) Basement membrane proteins: structure, assembly and cellular interactions. Crit Rev Biochem Mol Biol 27: 93–127.
Petitclerc E, Strömblad S, von Schalscha TL, Mitjans F, Piulats J, Montgomery AMP, Cheresh DA, Brooks P (1999) Integrin αvβ3 promotes M21 melanoma growth in human skin by regulating tumor cell survival. Cancer Res 59: 2724–2730.
Quondamatteo F, Scherf C, Miosge N, Herken R (1999) Immunohistochemical localization of laminin, nidogen and type IV collagen during the early development of human liver. Histochem Cell Biol 111: 39–47.
Raghavan S, Bauer C, Mundschau G, Li Q, Fuchs E (2000) Conditional ablation of β1 integrin in skin: severe defects in epidermal proliferation, basement membrane formation and hair follicle invagination. J Cell Biol 150: 1149–1160.
Ruzzi L, Gagnoux-Palacios L, Pinola M, Belli S, Meneguzzi G, D'Alession M, Zambruno G (1997) A homozygous mutation in the integrin α6 gene in junctional epidermolysis bullosa with pyloric atresia. J Clin Invest 99: 2826–2831.
Sasaki T, Forsberg E, Bloch W, Addicks K, Fässler R, Timpl R (1998) Deficiency of β1 integrins in teratoma interferes with basement membrane assembly and laminin-1 expression. Exp Cell Res 238: 70–81.
Schaffner F, Popper H (1963) Capillarization of hepatic sinusoids in man. Gastroenterology 44: 239–242.
Schymeinsky J, Nedbal S, Miosge N, Pöschl E, Rao C, Beier DR, Skarnes WC, Timpl R, Bader BL (2002) Gene structure and functional analysis of the mouse nidogen-2 Gene: nidogen-2 is not essential for basement membrane formation in mice. Mol Cell Biol 22: 6820–6830.
Simon-Assmann P, Kedinger M, Haffen K (1986) Immunocytochemical localization of extracellular matrix proteins in relation to rat intestinal morphogenesis. Differentiation 32: 59–66.
Simon-Assmann P, Simo P, Bouziges F, Haffen K, Kedinger M (1990) Synthesis of basement membrane proteins in the small intestine. Digestion 46: 12–21.
Smyth N, Vatansever HS, Murray P, Meyer M, Frie C, Paulsson M, Edgar D (1999) Absence of basement membranes after targeting the LAMC1 gene results in early embryonic lethality due to failure of endoderm differentiation. J Cell Biol 144: 151–160.
Sorokin L, Sonnenberg A, Aumailley M, Timpl R, Ekblom P (1990) Recognition of the laminin E8 cell-binding site by an integrin possessing the α6 subunit in developing kidney tubules. J Cell Biol 111: 1265–1273.
Stichel CC, Müller HW (1998) The CNS lesion scar: new vistas on an old regeneration barrier. Cell Tissue Res 294: 1–9.
Strömblad S, Becker JC, Yebra M, Brooks PC, Cheresh DA (1996) Suppression of p53 activity and p21WAF1/CIP1 expression by vascular cell integrin avβ3 during angiogenesis. J Clin Invest 98: 426–433.
Talts JF, Andac Z, Göhring W, Brancaccio A, Timpl R (1999) Binding of the G domains of laminin α1 and α2 chains and perlecan to heparin, sulfatides, α-dystroglycan and several extracellular matrix proteins. EMBO J 18: 863–870.
Timpl R (1993) Proteoglycans of basement membranes. Experientia 49: 417–427.
Timpl R, Dziadek M (1986) Structure, development and molecular pathology of basement membranes. Int Rev Exp Pathol 29: 1–112.
Timpl R, Rohde H, Gehron Robey P, Rennard S, Foidart JM, Martin GR (1979) Laminin a glycoprotein from basement membranes. J Biol Chem 254: 9933–9937.
Tryggvason K, Wartiovaara J (2001) Molecular basis of glomerular permselectivity. Curr Opin Nephrol Hypertens 10: 543–549.
Tsen G, Halfter W, Kröger S, Cole GJ (1995) Agrin is a heparan sulfate proteoglycan. J Biol Chem 270: 3392–3399.
Tsiper M, Yurchenco PD (2002) Laminin assembles into separate basement membrane and fibrillar matrices in Schwann cells. J Cell Sci 115: 1005–1015.
Tungaal P, Smyth N, Paulsson M, Ott MC (2000) Laminins: structure and genetic regulation. Microsc Res Techn 51: 214–227.
van der Flier A, Sonnenberg A (2001) Function and interactions of integrins. Cell Tissue Res 305: 285–298.
van der Neut R, Krimpenfort P, Calafat J, Niessen CM, Sonnenberg A (1996) Epithelial detachment due to absence of hemidesmosomes in integrin β4 null mice. Nat Genet 13: 366–369.
Vidal F, Aberdam D, Miquel C, Christiano AM, Pulkkinen L, Uitto J, Ortonne P, Meneguzzi G (1995) Integrin β4 mutations associated with junctional epidermolysis bullosa with pyloric atresia. Nat Genetics 10: 229–234.
Wang JF, Zhang XF, Groopman JE (2001) Stimulation of β1 integrin induces tyrosine phosphorilation of vascular endothelial growth factor receptor-3 and modulates cell migration. J Biol Chem 276: 41950–41957.
Watt F (2001) Stem cell fate and patterning in mammalian epidermis. Curr Opin Gen Dev 11: 410–417.
Williamson RA, Henry MD, Daniels KJ, Hrstka RF, Lee JC, Sunada Y, Ibraghimov-Beskrovnaya O, Campbell KP (1997) Dystroglycan is essential for early embryonic development: disruption of Reichert's membrane in Dag1-null mice. Hum Mol Gen 6: 831–841.
Yang Y, Palmer KC, Relan N, Diglio C, Schuger L (1998) Role of laminin polymerization at the epithelial mesenchymal interface in bronchial morphogenesis. Development 125: 2621–2629.
Yurchenco PD (1994) Assembly of laminin and type IV collagen into basement membrane networks. In: Yurchenco PD, Birk DE, Mecham RP, eds. Extracellular Matrix Assembly and Structure. San Diego: Academic Press, pp. 351–388.
Yurchenco PD, Furthmayr H (1984) Self-assembly of basement membrane collagen. Biochemistry 23: 1839–1850.
Yurchenco PD, O'Rear J (1993) Supramolecular organization of basement membranes. In: Rohrbach DH, Timpl R, eds. Molecular and Cellular Aspects of Basement Membranes. San Diego: Academic Press, pp. 20–47.
Yurchenco PD, Ruben GC (1987) Basement membrane structure in situ: evidence for lateral associations in the type IV collagen network. J Cell Biol 105: 2559–2568.
Yurchenco PD, Schittny JC (1990). Molecular architecture of basement membranes. FASEB J 4: 1577–1590.
Yurchenco PD, Tsilibary EC, Charonis AS, Furthmayr H (1985) Laminin polymerization in vitro. Evidence for a two-step assembly with domain specificity. J Biol Chem 260: 7636–7644.
Yurchenco PD, Cheng YS, Colognato H (1992) Laminin forms an independent network in basement membranes. J Cell Biol 117: 1119–1133.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Quondamatteo, F. Assembly, stability and integrity of basement membranes in vivo . Histochem J 34, 369–381 (2002). https://doi.org/10.1023/A:1023675619251
Issue Date:
DOI: https://doi.org/10.1023/A:1023675619251