Skip to main content

Advertisement

SpringerLink
Log in

Basement membranes in the cornea and other organs that commonly develop fibrosis

  • Review
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

Basement membranes are thin connective tissue structures composed of organ-specific assemblages of collagens, laminins, proteoglycan-like perlecan, nidogens, and other components. Traditionally, basement membranes are thought of as structures which primarily function to anchor epithelial, endothelial, or parenchymal cells to underlying connective tissues. While this role is important, other functions such as the modulation of growth factors and cytokines that regulate cell proliferation, migration, differentiation, and fibrosis are equally important. An example of this is the critical role of both the epithelial basement membrane and Descemet’s basement membrane in the cornea in modulating myofibroblast development and fibrosis, as well as myofibroblast apoptosis and the resolution of fibrosis. This article compares the ultrastructure and functions of key basement membranes in several organs to illustrate the variability and importance of these structures in organs that commonly develop fibrosis.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Abrahamson DR (2009) Development of kidney glomerular endothelial cells and their role in basement membrane assembly. Organogenesis 5:275–287

    PubMed  PubMed Central  Google Scholar 

  • Arikawa-Hirasawa E, Watanabe H, Takami H, Hassell JR, Yamada Y (1999) Perlecan is essential for cartilage and cephalic development. Nat Genet 23:354–358

    CAS  PubMed  Google Scholar 

  • 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 43:7–12

    CAS  PubMed  Google Scholar 

  • Aumailley M, Bruckner-Tuderman L, Carter WG, Deutzmann R, Edgar D, Ekblom P, Engel J, Engvall E, Hohenester E, Jones JC, Kleinman HK, Marinkovich MP, Martin GR, Mayer U, Meneguzzi G, Miner JH, Miyazaki K, Patarroyo M, Paulsson M, Quaranta V, Sanes JR, Sasaki T, Sekiguchi K, Sorokin LM, Talts JF, Tryggvason K, Uitto J, Virtanen I, von der Mark K, Wewer UM, Yamada Y, Yurchenco PD (2005) A simplified laminin nomenclature. Matrix Biol 24:326–332

    CAS  PubMed  Google Scholar 

  • Bader BL, Smyth N, Nedbal S, Miosge N, Baranowsky A, Mokkapati S, Murshed M, Nischt R (2005) Compound genetic ablation of nidogen 1 and 2 causes basement membrane defects and perinatal lethality in mice. Mol Cell Biol 25:6846–6856

    CAS  PubMed  PubMed Central  Google Scholar 

  • Barbosa FL, Chaurasia SS, Cutler A, Asosingh K, Kaur H, de Medeiros FW, Agrawal V, Wilson SE (2010) Corneal myofibroblast generation from bone marrow-derived cells. Exp Eye Res 91:92–96

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bechtel M, Keller MV, Bloch W, Sasaki T, Boukamp P, Zaucke F, Paulsson M, Nischt R (2012) Different domains in nidogen-1 and nidogen-2 drive basement membrane formation in skin organotypic cocultures. FASEB J 26:3637–3648

    CAS  PubMed  Google Scholar 

  • Behrens DT, Villone D, Koch M, Brunner G, Sorokin L, Robenek H, Bruckner-Tuderman L, Bruckner P, Hansen U (2012) The epidermal basement membrane is a composite of separate laminin- or collagen IV-containing networks connected by aggregated perlecan, but not by nidogens. J Biol Chem 287:18700–18,709

    CAS  PubMed  PubMed Central  Google Scholar 

  • Benya PD, Padilla SR (1986) Isolation and characterization of type VIII collagen synthesized by cultured rabbit corneal endothelial cells. A conventional structure replaces the interrupted-helix model. J Biol Chem 261:4160–4169

    CAS  PubMed  Google Scholar 

  • Ben-Zvi A, Rodrigues MM, Krachmer JH, Fujikawa LS (1986) Immunohistochemical characterization of extracellular matrix in the developing human cornea. Curr Eye Res 5:105–117

    CAS  PubMed  Google Scholar 

  • Bonod-Bidaud C, Roulet M, Hansen U, Elsheikh A, Malbouyres M, Ricard-Blum S, Faye C, Vaganay E, Rousselle P, Ruggiero F (2012) In vivo evidence for a bridging role of a collagen V subtype at the epidermis-dermis interface. J Invest Dermatol 132:1841–1849

    CAS  PubMed  Google Scholar 

  • Boudreau NJ, Jones PL (1999) Extracellular matrix and integrin signaling: the shape of things to come. Biochem J 339(Pt 3):481–488

    CAS  PubMed  PubMed Central  Google Scholar 

  • Breitkreutz D, Bohnert A, Herzmann E, Bowden PE, Boukamp P, Fusenig NE (1984) Differentiation specific functions in cultured and transplanted mouse keratinocytes: environmental influences on ultrastructure and keratin expression. Differentiation 26:154–169

    CAS  PubMed  Google Scholar 

  • Breitkreutz D, Stark HJ, Mirancea N, Tomakidi P, Steinbauer H, Fusenig NE (1997) Integrin and basement membrane normalization in mouse grafts of human keratinocytes—implications for epidermal homeostasis. Differentiation 61:195–209

    CAS  PubMed  Google Scholar 

  • Breitkreutz D, Schoop VM, Mirancea N, Baur M, Stark HJ, Fusenig NE (1998) Epidermal differentiation and basement membrane formation by HaCaT cells in surface transplants. Eur J Cell Biol 75:273–286

    CAS  PubMed  Google Scholar 

  • Breitkreutz D, Koxholt I, Thiemann K, Nischt R (2013) Skin basement membrane: the foundation of epidermal integrity-BM functions and diverse roles of bridging molecules nidogen and perlecan. Biomed Res Int 2013:179784

    PubMed  PubMed Central  Google Scholar 

  • Bucher NL (1963) Regeneration of mammalian liver. Int Rev Cytol 15:245–300

    CAS  PubMed  Google Scholar 

  • Cabrera S, Selman M, Lonzano-Bolanos A, Konishi K, Richards TJ, Kaminski N, Pardo A (2013) Gene expression profiles reveal molecular mechanisms involved in the progression and resolution of bleomycin-induced lung fibrosis. Am J Physiol Lung Cell Mol Physiol 304:L593–L601

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cameron JD, Skubitz AP, Furcht LT (1991) Type IV collagen and corneal epithelial adhesion and migration. Effects of type IV collagen fragments and synthetic peptides on rabbit corneal epithelial cell adhesion and migration in vitro. Invest Ophthalmol Vis Sci 32:2766–2773

    CAS  PubMed  Google Scholar 

  • Carlin B, Jaffe R, Bender B, Chung AE (1981) Entactin, a novel basal lamina-associated sulfated glycoprotein. J Biol Chem 256:5209–5214

    CAS  PubMed  Google Scholar 

  • Carlson EC, Meezan E, Brendel K, Kenney MC (1981) Ultrastructural analyses of control and enzyme-treated isolated renal basement membranes. Anat Rec 200:421–436

    CAS  PubMed  Google Scholar 

  • Chaurasia SS, Kaur H, de Medeiros FW, Smith SD, Wilson SE (2009) Dynamics of the expression of intermediate filaments vimentin and desmin during myofibroblast differentiation after corneal injury. Exp Eye Res 89:133–139

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen L, Hazlett LD (2001) Human corneal epithelial extracellular matrix perlecan serves as a site for Pseudomonas aeruginosa binding. Curr Eye Res 22:19–27

    PubMed  Google Scholar 

  • Chen H, Qu J, Huang X, Kurundkar A, Zhu L, Yang N, Venado A, Ding Q, Liu G, Antony VB, Thannickal VJ, Zhou Y (2016) Mechanosensing by the alpha6-integrin confers an invasive fibroblast phenotype and mediates lung fibrosis. Nat Commun 7:12564

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chi HH, Teng CC, Katzin HM (1958) Histopathology of primary endothelial-epithelial dystrophy of the cornea. Am J Ophthalmol 45:518–535

    CAS  PubMed  Google Scholar 

  • Chung AE, Freeman IL, Braginski JE (1977) A novel extracellular membrane elaborated by a mouse embryonal carcinoma-derived cell line. Biochem Biophys Res Commun 79:859–868

    CAS  PubMed  Google Scholar 

  • Chung AE, Jaffe R, Freeman IL, Vergnes JP, Braginski JE, Carlin B (1979) Properties of a basement membrane-related glycoprotein synthesized in culture by a mouse embryonal carcinoma-derived cell line. Cell 16:277–287

    CAS  PubMed  Google Scholar 

  • Costell M, Gustafsson E, Aszodi A, Morgelin M, Bloch W, Hunziker E, Addicks K, Timpl R, Fassler R (1999) Perlecan maintains the integrity of cartilage and some basement membranes. J Cell Biol 147:1109–1122

    CAS  PubMed  PubMed Central  Google Scholar 

  • Denzer AJ, Gesemann M, Schumacher B, Ruegg MA (1995) An amino-terminal extension is required for the secretion of chick agrin and its binding to extracellular matrix. J Cell Biol 131:1547–1560

    CAS  PubMed  Google Scholar 

  • Derry CJ, Pusey CD (1994) Tissue-specific distribution of the Goodpasture antigen demonstrated by 2-D electrophoresis and western blotting. Nephrol Dial Transplant 9:355–361

    CAS  PubMed  Google Scholar 

  • Di Nunzio F, Maruggi G, Ferrari S, Di Iorio E, Poletti V, Garcia M, Del Rio M, De Luca M, Larcher F, Pellegrini G, Mavilio F (2008) Correction of laminin-5 deficiency in human epidermal stem cells by transcriptionally targeted lentiviral vectors. Mol Ther 16:1977–1985

    PubMed  Google Scholar 

  • Dong S, Cole GJ, Halfter W (2003) Expression of collagen XVIII and localization of its glycosaminoglycan attachment sites. J Biol Chem 278:1700–1707

    CAS  PubMed  Google Scholar 

  • El Ghalbzouri A, Ponec M (2004) Diffusible factors released by fibroblasts support epidermal morphogenesis and deposition of basement membrane components. Wound Repair Regen 12:359–367

    PubMed  Google Scholar 

  • El Ghalbzouri A, Jonkman MF, Dijkman R, Ponec M (2005) Basement membrane reconstruction in human skin equivalents is regulated by fibroblasts and/or exogenously activated keratinocytes. J Invest Dermatol 124:79–86

    PubMed  Google Scholar 

  • Ettner N, Gohring W, Sasaki T, Mann K, Timpl R (1998) The N-terminal globular domain of the laminin alpha1 chain binds to alpha1beta1 and alpha2beta1 integrins and to the heparan sulfate-containing domains of perlecan. FEBS Lett 430:217–221

    CAS  PubMed  Google Scholar 

  • Filenius S, Hormia M, Rissanen J, Burgeson RE, Yamada Y, Araki-Sasaki K, Nakamura M, Virtanen I, Tervo T (2001) Laminin synthesis and the adhesion characteristics of immortalized human corneal epithelial cells to laminin isoforms. Exp Eye Res 72:93–103

    CAS  PubMed  Google Scholar 

  • Fini ME (1999) Keratocyte and fibroblast phenotypes in the repairing cornea. Prog Retin Eye Res 18:529–551

    CAS  PubMed  Google Scholar 

  • Fleischmajer R, Schechter A, Bruns M, Perlish JS, Macdonald ED, Pan TC, Timpl R, Chu ML (1995) Skin fibroblasts are the only source of nidogen during early basal lamina formation in vitro. J Invest Dermatol 105:597–601

    CAS  PubMed  Google Scholar 

  • Fox JW, Mayer U, Nischt R, Aumailley M, Reinhardt D, Wiedemann H, Mann K, Timpl R, Krieg T, Engel J et al (1991) Recombinant nidogen consists of three globular domains and mediates binding of laminin to collagen type IV. EMBO J 10:3137–3146

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fritsch A, Spassov S, Elfert S, Schlosser A, Gache Y, Meneguzzi G, Bruckner-Tuderman L (2009) Dominant-negative effects of COL7A1 mutations can be rescued by controlled overexpression of normal collagen VII. J Biol Chem 284:30248–30256

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fukai N, Eklund L, Marneros AG, Oh SP, Keene DR, Tamarkin L, Niemela M, Ilves M, Li E, Pihlajaniemi T, Olsen BR (2002) Lack of collagen XVIII/endostatin results in eye abnormalities. EMBO J 21:1535–1544

    CAS  PubMed  PubMed Central  Google Scholar 

  • Furuyama A, Kimata K, Mochitate K (1997) Assembly of basement membrane in vitro by cooperation between alveolar epithelial cells and pulmonary fibroblasts. Cell Struct Funct 22:603–614

    CAS  PubMed  Google Scholar 

  • Gersdorff N, Kohfeldt E, Sasaki T, Timpl R, Miosge N (2005) Laminin gamma3 chain binds to nidogen and is located in murine basement membranes. J Biol Chem 280:22146–22153

    CAS  PubMed  Google Scholar 

  • Gersdorff N, Otto S, Roediger M, Kruegel J, Miosge N (2007) The absence of one or both nidogens does not alter basement membrane composition in adult murine kidney. Histol Histopathol 22:1077–1084

    CAS  PubMed  Google Scholar 

  • Gipson IK, Spurr-Michaud SJ, Tisdale AS (1988) Hemidesmosomes and anchoring fibril collagen appear synchronously during development and wound healing. Dev Biol 126:253–262

    CAS  PubMed  Google Scholar 

  • Groffen AJ, Ruegg MA, Dijkman H, van de Velden TJ, Buskens CA, van den Born J, Assmann KJ, Monnens LA, Veerkamp JH, van den Heuvel LP (1998) Agrin is a major heparan sulfate proteoglycan in the human glomerular basement membrane. J Histochem Cytochem 46:19–27

    CAS  PubMed  Google Scholar 

  • Gubler MC (2008) Inherited diseases of the glomerular basement membrane. Nat Clin Pract Nephrol 4:24–37

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Halfter W, Dong S, Schurer B, Cole GJ (1998) Collagen XVIII is a basement membrane heparan sulfate proteoglycan. J Biol Chem 273:25404–25,412

    CAS  PubMed  Google Scholar 

  • Halfter W, Oertle P, Monnier CA, Camenzind L, Reyes-Lua M, Hu H, Candiello J, Labilloy A, Balasubramani M, Henrich PB, Plodinec M (2015) New concepts in basement membrane biology. FEBS J 282:4466–4479

    CAS  PubMed  Google Scholar 

  • Hammers CM, Stanley JR (2016) Mechanisms of disease: pemphigus and bullous pemphigoid. Annu Rev Pathol 11:175–197

    CAS  PubMed  PubMed Central  Google Scholar 

  • Harvey SJ, Jarad G, Cunningham J, Rops AL, van der Vlag J, Berden JH, Moeller MJ, Holzman LB, Burgess RW, Miner JH (2007) Disruption of glomerular basement membrane charge through podocyte-specific mutation of agrin does not alter glomerular permselectivity. Am J Pathol 171:139–152

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hassell JR, Birk DE (2010) The molecular basis of corneal transparency. Exp Eye Res 91:326–335

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hassell JR, Robey PG, Barrach HJ, Wilczek J, Rennard SI, Martin GR (1980) Isolation of a heparan sulfate-containing proteoglycan from basement membrane. Proc Natl Acad Sci U S A 77:4494–4498

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hassell JR, Schrecengost PK, Rada JA, SundarRaj N, Sossi G, Thoft RA (1992) Biosynthesis of stromal matrix proteoglycans and basement membrane components by human corneal fibroblasts. Invest Ophthalmol Vis Sci 33:547–557

    CAS  PubMed  Google Scholar 

  • Heidet L, Cai Y, Guicharnaud L, Antignac C, Gubler MC (2000) Glomerular expression of type IV collagen chains in normal and X-linked Alport syndrome kidneys. Am J Pathol 156:1901–1910

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ho MS, Bose K, Mokkapati S, Nischt R, Smyth N (2008) Nidogens-extracellular matrix linker molecules. Microsc Res Tech 71:387–395

    CAS  PubMed  Google Scholar 

  • Inomata T, Ebihara N, Funaki T, Matsuda A, Watanabe Y, Ning L, Xu Z, Murakami A, Arikawa-Hirasawa E (2012) Perlecan-deficient mutation impairs corneal epithelial structure. Invest Ophthalmol Vis Sci 53:1277–1284

    CAS  PubMed  Google Scholar 

  • Ishizaki M, Zhu G, Haseba T, Shafer SS, Kao WW (1993) Expression of collagen I, smooth muscle alpha-actin, and vimentin during the healing of alkali-burned and lacerated corneas. Invest Ophthalmol Vis Sci 34:3320–3328

    CAS  PubMed  Google Scholar 

  • Jester JV, Rodrigues MM, Herman IM (1987) Characterization of avascular corneal wound healing fibroblasts. New insights into the myofibroblast. Am J Pathol 127:140–148

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jester JV, Petroll WM, Barry PA, Cavanagh HD (1995) Temporal, 3-dimensional, cellular anatomy of corneal wound tissue. J Anat 186(Pt 2):301–311

    PubMed  PubMed Central  Google Scholar 

  • Jester JV, Huang J, Barry-Lane PA, Kao WW, Petroll WM, Cavanagh HD (1999) Transforming growth factor(beta)-mediated corneal myofibroblast differentiation requires actin and fibronectin assembly. Invest Ophthalmol Vis Sci 40:1959–1967

    CAS  PubMed  Google Scholar 

  • Jester JV, Huang J, Petroll WM, Cavanagh HD (2002) TGFbeta induced myofibroblast differentiation of rabbit keratocytes requires synergistic TGFbeta, PDGF and integrin signaling. Exp Eye Res 75:645–657

    CAS  PubMed  Google Scholar 

  • Johnson DH, Bourne WM, Campbell RJ (1982) The ultrastructure of Descemet’s membrane. II Aphakic bullous keratopathy. Arch Ophthalmol 100:1948–1951

    CAS  PubMed  Google Scholar 

  • Kabosova A, Azar DT, Bannikov GA, Campbell KP, Durbeej M, Ghohestani RF, Jones JC, Kenney MC, Koch M, Ninomiya Y, Patton BL, Paulsson M, Sado Y, Sage EH, Sasaki T, Sorokin LM, Steiner-Champliaud MF, Sun TT, Sundarraj N, Timpl R, Virtanen I, Ljubimov AV (2007) Compositional differences between infant and adult human corneal basement membranes. Invest Ophthalmol Vis Sci 48:4989–4999

    PubMed  PubMed Central  Google Scholar 

  • Kanwar YS, Danesh FR, Chugh SS (2007) Contribution of proteoglycans towards the integrated functions of renal glomerular capillaries: a historical perspective. Am J Pathol 171:9–13

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kapoor R, Bornstein P, Sage EH (1986) Type VIII collagen from bovine Descemet’s membrane: structural characterization of a triple-helical domain. Biochemistry 25:3930–3937

    CAS  PubMed  Google Scholar 

  • Kaur H, Chaurasia SS, Agrawal V, Suto C, Wilson SE (2009) Corneal myofibroblast viability: opposing effects of IL-1 and TGF beta1. Exp Eye Res 89:152–158

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kefalides NA, Denduchis B (1969) Structural components of epithelial and endothelial basement membranes. Biochemistry 8:4613–4621

    CAS  PubMed  Google Scholar 

  • Kefalides NA, Cameron JD, Tomichek EA, Yanoff M (1976) Biosynthesis of basement membrane collagen by rabbit corneal endothelium in vitro. J Biol Chem 251:730–733

    CAS  PubMed  Google Scholar 

  • Khoshnoodi J, Pedchenko V, Hudson BG (2008) Mammalian collagen IV. Microsc Res Tech 71:357–370

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Kleinman HK, Martin GR (2005) Matrigel: basement membrane matrix with biological activity. Semin Cancer Biol 15:378–386

    CAS  PubMed  Google Scholar 

  • Kleinman HK, McGarvey ML, Liotta LA, Robey PG, Tryggvason K, Martin GR (1982) Isolation and characterization of type IV procollagen, laminin, and heparan sulfate proteoglycan from the EHS sarcoma. Biochemistry 21:6188–6193

    CAS  PubMed  Google Scholar 

  • Kruegel J, Miosge N (2012) Basement membrane components are key players in specialized extracellular matrices. Cell Mol Life Sci 67:2879–2895

    Google Scholar 

  • Labermeier U, Kenney MC (1983) The presence of EC collagen and type IV collagen in bovine Descemet’s membranes. Biochem Biophys Res Commun 116:619–625

    CAS  PubMed  Google Scholar 

  • Lawson WE, Polosukhin VV, Stathopoulos GT, Zoia O, Han W, Lane KB, Li B, Donnelly EF, Holburn GE, Lewis KG, Collins RD, Hull WM, Glasser SW, Whitsett JA, Blackwell TS (2005) Increased and prolonged pulmonary fibrosis in surfactant protein C-deficient mice following intratracheal bleomycin. Am J Pathol 167:1267–1277

    CAS  PubMed  PubMed Central  Google Scholar 

  • LeBleu VS, Macdonald B, Kalluri R (2007) Structure and function of basement membranes. Exp Biol Med 232:1121–1129

    CAS  Google Scholar 

  • Lemaire R, Burwell T, Sun H, Delaney T, Bakken J, Cheng L, Rebelatto MC, Czapiga M, de-Mendez I, Coyle AJ, Herbst R, Lafyatis R, Connor J (2016) Resolution of skin fibrosis by neutralization of the antifibrinolytic function of plasminogen activator inhibitor 1. Arthritis Rheumatol 68:473–483

    CAS  PubMed  Google Scholar 

  • Li M, Krishnaveni MS, Li C, Zhou B, Xing Y, Banfalvi A, Li A, Lombardi V, Akbari O, Borok Z, Minoo P (2011) Epithelium-specific deletion of TGF-beta receptor type II protects mice from bleomycin-induced pulmonary fibrosis. J Clin Invest 121:277–287

    CAS  PubMed  Google Scholar 

  • Limat A, Stockhammer E, Breitkreutz D, Schaffner T, Egelrud T, Salomon D, Fusenig NE, Braathen LR, Hunziker T (1996) Endogeneously regulated site-specific differentiation of human palmar skin keratinocytes in organotypic cocultures and in nude mouse transplants. Eur J Cell Biol 69:245–258

    CAS  PubMed  Google Scholar 

  • Lin HC, Chang JH, Jain S, Gabison EE, Kure T, Kato T, Fukai N, Azar DT (2001) Matrilysin cleavage of corneal collagen type XVIII NC1 domain and generation of a 28-kDa fragment. Invest Ophthalmol Vis Sci 42:2517–2524

    CAS  PubMed  Google Scholar 

  • Ljubimov AV, Burgeson RE, Butkowski RJ, Michael AF, Sun TT, Kenney MC (1995) Human corneal basement membrane heterogeneity: topographical differences in the expression of type IV collagen and laminin isoforms. Lab Invest 72:461–473

    CAS  PubMed  Google Scholar 

  • Maatta M, Heljasvaara R, Pihlajaniemi T, Uusitalo M (2007) Collagen XVIII/endostatin shows a ubiquitous distribution in human ocular tissues and endostatin-containing fragments accumulate in ocular fluid samples. Graefe’s archive for clinical and experimental ophthalmology. Albrecht Von Graefes Arch Klin Exp Ophthalmol 245:74–81

    Google Scholar 

  • Mak KM, Mei R (2017) Basement membrane type IV collagen and laminin: an overview of their biology and value as fibrosis biomarkers of liver disease. Anat Rec (Hoboken) 300:1371–1390

    CAS  Google Scholar 

  • Mak KM, Chen LL, Lee TF (2013) Codistribution of collagen type IV and laminin in liver fibrosis of elderly cadavers: immunohistochemical marker of perisinusoidal basement membrane formation. Anat Rec (Hoboken) 296:953–964

    CAS  Google Scholar 

  • Marinkovich MP, Keene DR, Rimberg CS, Burgeson RE (1993) Cellular origin of the dermal-epidermal basement membrane. Dev Dyn 197:25,5–25,2267

    CAS  PubMed  Google Scholar 

  • Marino GK, Santhiago MR, Santhanam A, Lassance L, Thangavadivel S, Medeiros CS, Bose K, Tam KP, Wilson SE (2017a) Epithelial basement membrane injury and regeneration modulates corneal fibrosis after pseudomonas corneal ulcers in rabbits. Exp Eye Res 161:101–105

    CAS  PubMed  PubMed Central  Google Scholar 

  • Marino GK, Santhiago MR, Santhanam A, Torricelli AAM, Wilson SE (2017b) Regeneration of defective epithelial basement membrane and restoration of corneal transparency after photorefractive keratectomy. J Refract Surg 33:337–346

    PubMed  PubMed Central  Google Scholar 

  • Marneros AG, Olsen BR (2003) Age-dependent iris abnormalities in collagen XVIII/endostatin deficient mice with similarities to human pigment dispersion syndrome. Invest Ophthalmol Vis Sci 44:2367–2372

    PubMed  Google Scholar 

  • Marneros AG, Keene DR, Hansen U, Fukai N, Moulton K, Goletz PL, Moiseyev G, Pawlyk BS, Halfter W, Dong S, Shibata M, Li T, Crouch RK, Bruckner P, Olsen BR (2004) Collagen XVIII/endostatin is essential for vision and retinal pigment epithelial function. EMBO J 23:89–99

    CAS  PubMed  Google Scholar 

  • Martinez-Hernandez A, Amenta PS (1995) The extracellular matrix in hepatic regeneration. FASEB J 9:1401–1410

    CAS  PubMed  Google Scholar 

  • Matejas V, Hinkes B, Alkandari F, Al-Gazali L, Annexstad E, Aytac MB, Barrow M, Blahova K, Bockenhauer D, Cheong HI, Maruniak-Chudek I, Cochat P, Dotsch J, Gajjar P, Hennekam RC, Janssen F, Kagan M, Kariminejad A, Kemper MJ, Koenig J, Kogan J, Kroes HY, Kuwertz-Broking E, Lewanda AF, Medeira A, Muscheites J, Niaudet P, Pierson M, Saggar A, Seaver L, Suri M, Tsygin A, Wuhl E, Zurowska A, Uebe S, Hildebrandt F, Antignac C, Zenker M (2010) Mutations in the human laminin beta2 (LAMB2) gene and the associated phenotypic spectrum. Hum Mutat 31:992–1002

    CAS  PubMed  PubMed Central  Google Scholar 

  • Matsumoto S, Yamamoto K, Nagano T, Okamoto R, Ibuki N, Tagashira M, Tsuji T (1999) Immunohistochemical study on phenotypical changes of hepatocytes in liver disease with reference to extracellular matrix composition. Liver 19:32–38

    CAS  PubMed  Google Scholar 

  • May CA (2012) Distribution of nidogen in the murine eye and ocular phenotype of the nidogen-1 knockout mouse. ISRN Ophthalmol 2012:378641

    PubMed  PubMed Central  Google Scholar 

  • Medeiros CS, Lassance L, Saikia P, Wilson SE (2018) Posterior stromal keratocyte apoptosis triggered by mechanical endothelial injury and nidogen-1 production in the cornea. Exp Eye Res 172:30–35

    CAS  PubMed  Google Scholar 

  • Menzel O, Bekkeheien RC, Reymond A, Fukai N, Boye E, Kosztolanyi G, Aftimos S, Deutsch S, Scott HS, Olsen BR, Antonarakis SE, Guipponi M (2004) Knobloch syndrome: novel mutations in COL18A1, evidence for genetic heterogeneity, and a functionally impaired polymorphism in endostatin. Hum Mutat 23:77–84

    CAS  PubMed  Google Scholar 

  • Michelacci YM (2003) Collagens and proteoglycans of the corneal extracellular matrix. Braz J Med Biol Res 36:1037–1046

    CAS  PubMed  Google Scholar 

  • Miner JH (2012) The glomerular basement membrane. Exp Cell Res 318:973–978

    CAS  PubMed  PubMed Central  Google Scholar 

  • Miner JH, Li C (2000) Defective glomerulogenesis in the absence of laminin alpha5 demonstrates a developmental role for the kidney glomerular basement membrane. Dev Biol 217:278–289

    CAS  PubMed  Google Scholar 

  • Miner JH, Sanes JR (1994) Collagen IV alpha 3, alpha 4, and alpha 5 chains in rodent basal laminae: sequence, distribution, association with laminins, and developmental switches. J Cell Biol 127:879–891

    CAS  PubMed  Google Scholar 

  • Miner JH, Yurchenco PD (2004) Laminin functions in tissue morphogenesis. Annu Rev. Cell Dev Biol 20:255–284

    CAS  Google Scholar 

  • Miner JH, Patton BL, Lentz SI, Gilbert DJ, Snider WD, Jenkins NA, Copeland NG, Sanes JR (1997) The laminin alpha chains: expression, developmental transitions, and chromosomal locations of alpha1–5, identification of heterotrimeric laminins 8–11, and cloning of a novel alpha3 isoform. J Cell Biol 137:685–701

    CAS  PubMed  PubMed Central  Google Scholar 

  • Miosge N, Sasaki T, Timpl R (2002) Evidence of nidogen-2 compensation for nidogen-1 deficiency in transgenic mice. Matrix Biol 21:611–621

    CAS  PubMed  Google Scholar 

  • Miosge N, Simniok T, Sprysch P, Herken R (2003) The collagen type XVIII endostatin domain is co-localized with perlecan in basement membranes in vivo. J Histochem Cytochem 51:285–296

    CAS  PubMed  Google Scholar 

  • Mirancea N, Hausser I, Metze D, Stark HJ, Boukamp P, Breitkreutz D (2007) Junctional basement membrane anomalies of skin and mucosa in lipoid proteinosis (hyalinosis cutis et mucosae). J Dermatol Sci 45:175–185

    CAS  PubMed  Google Scholar 

  • Mohan RR, Hutcheon AE, Choi R, Hong J, Lee J, Mohan RR, Ambrosio R Jr, Zieske JD, Wilson SE (2003) Apoptosis, necrosis, proliferation, and myofibroblast generation in the stroma following LASIK and PRK. Exp Eye Res 76:71–87

    CAS  PubMed  Google Scholar 

  • Mokkapati S, Bechtel M, Reibetanz M, Miosge N, Nischt R (2012) Absence of the basement membrane component nidogen 2, but not of nidogen 1, results in increased lung metastasis in mice. J Histochem Cytochem 60:280–289

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mueller MM, Fusenig NE (2004) Friends or foes—bipolar effects of the tumor stroma in cancer. Nat Rev Cancer 4:839–849

    CAS  PubMed  Google Scholar 

  • Murauer EM, Gache Y, Gratz IK, Klausegger A, Muss W, Gruber C, Meneguzzi G, Hintner H, Bauer JW (2011) Functional correction of type VII collagen expression in dystrophic epidermolysis bullosa. J Invest Dermatol 131:74–83

    CAS  PubMed  Google Scholar 

  • Murphy C, Alvarado J, Juster R (1984) Prenatal and postnatal growth of the human Descemet’s membrane. Invest Ophthalmol Vis Sci 25:1402–1415

    CAS  PubMed  Google Scholar 

  • Netto MV, Mohan RR, Sinha S, Sharma A, Dupps W, Wilson SE (2006) Stromal haze, myofibroblasts, and surface irregularity after PRK. Exp Eye Res 82:788–797

    CAS  PubMed  Google Scholar 

  • Nystrom A, Bornert O, Kuhl T (2017) Cell therapy for basement membrane-linked diseases. Matrix Biol 57–58:124–139

    PubMed  Google Scholar 

  • Orkin RW, Gehron P, McGoodwin EB, Martin GR, Valentine T, Swarm R (1977) A murine tumor producing a matrix of basement membrane. J Exp Med 145:204–220

    CAS  PubMed  Google Scholar 

  • Paulsson M (1988) The role of Ca2+ binding in the self-aggregation of laminin-nidogen complexes. J Biol Chem 263:5425–5430

    CAS  PubMed  Google Scholar 

  • Poschl E, Schlotzer-Schrehardt U, Brachvogel B, Saito K, Ninomiya Y, Mayer U (2004) Collagen IV is essential for basement membrane stability but dispensable for initiation of its assembly during early development. Development 131:1619–1628

    PubMed  Google Scholar 

  • Qiao H, Shibaki A, Long HA, Wang G, Li Q, Nishie W, Abe R, Akiyama M, Shimizu H, McMillan JR (2009) Collagen XVII participates in keratinocyte adhesion to collagen IV, and in p38MAPK-dependent migration and cell signaling. J Invest Dermatol 129:2288–2295

    CAS  PubMed  Google Scholar 

  • Reiser J, Altintas MM (2016) Podocytes. F1000Res :5. https://doi.org/10.12688/f1000research.7255.1

  • Ryu M, Mulay SR, Miosge N, Gross O, Anders HJ (2012) Tumor necrosis factor-α drives Alport glomerulosclerosis in mice by promoting podocyte apoptosis. J Pathol 226:120–131

    CAS  PubMed  Google Scholar 

  • Saarela J, Ylikarppa R, Rehn M, Purmonen S, Pihlajaniemi T (1998) Complete primary structure of two variant forms of human type XVIII collagen and tissue-specific differences in the expression of the corresponding transcripts. Matrix Biol 16:319–328

    CAS  PubMed  Google Scholar 

  • Sage H, Pritzl P, Bornstein P (1981) Secretory phenotypes of endothelial cells in culture: comparison of aortic, venous, capillary, and corneal endothelium. Arteriosclerosis 1:427–442

    CAS  PubMed  Google Scholar 

  • Salmivirta K, Talts JF, Olsson M, Sasaki T, Timpl R, Ekblom P (2002) Binding of mouse nidogen-2 to basement membrane components and cells and its expression in embryonic and adult tissues suggest complementary functions of the two nidogens. Exp Cell Res 279:188–201

    CAS  PubMed  Google Scholar 

  • Sannes PL, Wang J (1997) Basement membranes and pulmonary development. Exp Lung Res 23:101–108

    CAS  PubMed  Google Scholar 

  • Santhanam A, Torricelli AA, Wu J, Marino GK, Wilson SE (2015) Differential expression of epithelial basement membrane components nidogens and perlecan in corneal stromal cells in vitro. Mol Vis 21:1318–1327

    CAS  PubMed  PubMed Central  Google Scholar 

  • Santhanam A, Marino GK, Torricelli AA, Wilson SE (2017) EBM regeneration and changes in EBM component mRNA expression in stromal cells after corneal injury. Mol Vis 23:39–51

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sawada H (1982) The fine structure of the bovine Descemet’s membrane with special reference to biochemical nature. Cell Tissue Res 226:241–255

    CAS  PubMed  Google Scholar 

  • Schaffner F, Poper H (1963) Capillarization of hepatic sinusoids in man. Gastroenterology 44:239–242

    CAS  PubMed  Google Scholar 

  • Schubert D, Kimura H (1991) Substratum-growth factor collaborations are required for the mitogenic activities of activin and FGF on embryonal carcinoma cells. J Cell Biol 114:841–846

    CAS  PubMed  Google Scholar 

  • Shuttleworth CA (1997) Type VIII collagen. Int J Biochem Cell Biol 29:1145–1148

    CAS  PubMed  Google Scholar 

  • Simon-Assmann P, Lefebvre O, Bellissent-Waydelich A, Olsen J, Orian-Rousseau V, De Arcangelis A (1998) The laminins: role in intestinal morphogenesis and differentiation. Ann N Y Acad Sci 859:46–64

    CAS  PubMed  Google Scholar 

  • Smola H, Stark HJ, Thiekotter G, Mirancea N, Krieg T, Fusenig NE (1998) Dynamics of basement membrane formation by keratinocyte-fibroblast interactions in organotypic skin culture. Exp Cell Res 239:399–410

    CAS  PubMed  Google Scholar 

  • 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 embryonic lethality due to failure of endoderm differentiation. J Cell Biol 144:151–160

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sonnenberg A, Calafat J, Janssen H, Daams H, van der Raaij-Helmer LM, Falcioni R, Kennel SJ, Aplin JD, Baker J, Loizidou M et al (1991) Integrin alpha 6/beta 4 complex is located in hemidesmosomes, suggesting a major role in epidermal cell-basement membrane adhesion. J Cell Biol 113:907–917

    CAS  PubMed  Google Scholar 

  • Stark HJ, Baur M, Breitkreutz D, Mirancea N, Fusenig NE (1999) Organotypic keratinocyte cocultures in defined medium with regular epidermal morphogenesis and differentiation. J Invest Dermatol 112:681–691

    CAS  PubMed  Google Scholar 

  • Sterk LM, Geuijen CA, Oomen LC, Calafat J, Janssen H, Sonnenberg A (2000) The tetraspan molecule CD151, a novel constituent of hemidesmosomes, associates with the integrin alpha6beta4 and may regulate the spatial organization of hemidesmosomes. J Cell Biol 149:969–982

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sterk LM, Geuijen CA, van den Berg JG, Claessen N, Weening JJ, Sonnenberg A (2002) Association of the tetraspanin CD151 with the laminin-binding integrins alpha3beta1, alpha6beta1, alpha6beta4 and alpha7beta1 in cells in culture and in vivo. J Cell Sci 115:1161–1173

    CAS  PubMed  Google Scholar 

  • Strieter RM, Mehrad B (2009) New mechanisms of pulmonary fibrosis. Chest 136:1364–1370

    PubMed  PubMed Central  Google Scholar 

  • Sugawara K, Tsuruta D, Ishii M, Jones JC, Kobayashi H (2008) Laminin-332 and -511 in skin. Exp Dermatol 17:473–480

    CAS  PubMed  Google Scholar 

  • Suzuki OT, Sertie AL, Der Kaloustian VM, Kok F, Carpenter M, Murray J, Czeizel AE, Kliemann SE, Rosemberg S, Monteiro M, Olsen BR, Passos-Bueno MR (2002) Molecular analysis of collagen XVIII reveals novel mutations, presence of a third isoform, and possible genetic heterogeneity in Knobloch syndrome. Am J Hum Genet 71:1320–1329

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tervo K, Tervo T, van Setten GB, Virtanen I (1991) Integrins in human corneal epithelium. Cornea 10:461–465

    CAS  PubMed  Google Scholar 

  • Tiedemann K, Sasaki T, Gustafsson E, Gohring W, Batge B, Notbohm H, Timpl R, Wedel T, Schlotzer-Schrehardt U, Reinhardt DP (2005) Microfibrils at basement membrane zones interact with perlecan via fibrillin-1. J Biol Chem 280:11404–11,412

    CAS  PubMed  Google Scholar 

  • Timpl R (1989) Structure and biological activity of basement membrane proteins. Eur J Biochem 180:487–502

    CAS  PubMed  Google Scholar 

  • Timpl R, Brown JC (1996) Supramolecular assembly of basement membranes. Bioessays 18:123–132

    CAS  PubMed  Google Scholar 

  • Timpl R, Rohde H, Robey PG, Rennard SI, Foidart JM, Martin GR (1979) Laminin—a glycoprotein from basement membranes. J Biol Chem 254:9933–9937

    CAS  PubMed  Google Scholar 

  • Torricelli AA, Singh V, Agrawal V, Santhiago MR, Wilson SE (2013a) Transmission electron microscopy analysis of epithelial basement membrane repair in rabbit corneas with haze. Invest Ophthalmol Vis Sci 54:4026–4033

    PubMed  PubMed Central  Google Scholar 

  • Torricelli AA, Singh V, Santhiago MR, Wilson SE (2013b) The corneal epithelial basement membrane: structure, function, and disease. Invest Ophthalmol Vis Sci 54:6390–6400

    CAS  PubMed  PubMed Central  Google Scholar 

  • Torricelli AA, Marino GK, Santhanam A, Wu J, Singh A, Wilson SE (2015) Epithelial basement membrane proteins perlecan and nidogen-2 are up-regulated in stromal cells after epithelial injury in human corneas. Exp Eye Res 134:33–38

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tsen G, Halfter W, Kroger S, Cole GJ (1995) Agrin is a heparan sulfate proteoglycan. J Biol Chem 270:3392–3399

    CAS  PubMed  Google Scholar 

  • Tuli SS, Liu R, Chen C, Blalock TD, Goldstein M, Schultz GS (2006) Immunohistochemical localization of EGF, TGF-alpha, TGF-beta, and their receptors in rat corneas during healing of excimer laser ablation. Curr Eye Res 31:709–719

    CAS  PubMed  Google Scholar 

  • Tuori A, Uusitalo H, Burgeson RE, Terttunen J, Virtanen I (1996) The immunohistochemical composition of the human corneal basement membrane. Cornea 15:286–294

    CAS  PubMed  Google Scholar 

  • Uitto J, Has C, Vahidnezhad H, Youssefian L, Bruckner-Tuderman L (2017) Molecular pathology of the basement membrane zone in heritable blistering diseases: the paradigm of epidermolysis bullosa. Matrix Biol 57–58:76–85

    PubMed  Google Scholar 

  • Vaccaro CA, Brody JS (1981) Structural features of alveolar wall basement membrane in the adult rat lung. J Cell Biol 91:427–437

    CAS  PubMed  Google Scholar 

  • Villone D, Fritsch A, Koch M, Bruckner-Tuderman L, Hansen U, Bruckner P (2008) Supramolecular interactions in the dermo-epidermal junction zone: anchoring fibril-collagen VII tightly binds to banded collagen fibrils. J Biol Chem 283:24506–24,513

    CAS  PubMed  PubMed Central  Google Scholar 

  • Virtanen I, Tervo K, Korhonen M, Paallysaho T, Tervo T (1992) Integrins as receptors for extracellular matrix proteins in human cornea. Acta Ophthalmol Suppl:18–21

    Google Scholar 

  • Voskarides K, Damianou L, Neocleous V, Zouvani I, Christodoulidou S, Hadjiconstantinou V, Ioannou K, Athanasiou Y, Patsias C, Alexopoulos E, Pierides A, Kyriacou K, Deltas C (2007) COL4A3/COL4A4 mutations producing focal segmental glomerulosclerosis and renal failure in thin basement membrane nephropathy. J Am Soc Nephrol: JASN 18:3004–3016

    CAS  PubMed  Google Scholar 

  • Weibel ER (1973) Morphological basis of alveolar-capillary gas exchange. Physiol Rev 53:419–495

    CAS  PubMed  Google Scholar 

  • Wells RG (2008) Cellular sources of extracellular matrix in hepatic fibrosis. Clin Liver Dis 12:759–768 viii

    PubMed  PubMed Central  Google Scholar 

  • West JB, Mathieu-Costello O (1999) Structure, strength, failure, and remodeling of the pulmonary blood-gas barrier. Annu Rev Physiol 61:543–572

    CAS  PubMed  Google Scholar 

  • Wilson SE (2012) Corneal myofibroblast biology and pathobiology: generation, persistence, and transparency. Exp Eye Res 99:78–88

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson SE, He YG, Weng J, Li Q, McDowall AW, Vital M, Chwang EL (1996) Epithelial injury induces keratocyte apoptosis: hypothesized role for the interleukin-1 system in the modulation of corneal tissue organization and wound healing. Exp Eye Res 62:325–327

    CAS  PubMed  Google Scholar 

  • Wilson SE, Chaurasia SS, Medeiros FW (2007) Apoptosis in the initiation, modulation and termination of the corneal wound healing response. Exp Eye Res 85:305–311

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson SE, Marino GK, Torricelli AAM, Medeiros CS (2017) Injury and defective regeneration of the epithelial basement membrane in corneal fibrosis: a paradigm for fibrosis in other organs? Matrix Biol 64:17–26

    CAS  PubMed  Google Scholar 

  • Yurchenco PD, Tsilibary EC, Charonis AS, Furthmayr H (1986) Models for the self-assembly of basement membrane. J Histochem Cytochem 34:93–102

    CAS  PubMed  Google Scholar 

  • Zhang J, Patel DV (2015) The pathophysiology of Fuchs’ endothelial dystrophy—a review of molecular and cellular insights. Exp Eye Res 130:97–105

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Cole Eye Institute, Cleveland Clinic, Cleveland Clinic, 9500 Euclid Ave, I-32, Cleveland, OH, USA

    Paramananda Saikia, Carla S. Medeiros, Shanmugapriya Thangavadivel & Steven E. Wilson

  2. University of São Paulo, São Paulo, Brazil

    Carla S. Medeiros

Authors
  1. Paramananda Saikia
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Carla S. Medeiros
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shanmugapriya Thangavadivel
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Steven E. Wilson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Steven E. Wilson.

Additional information

Supported in part by US Public Health Service grants RO1EY10056 (SEW) and P30-EY025585 from the National Eye Institute, National Institutes of Health, Bethesda, MD.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Saikia, P., Medeiros, C.S., Thangavadivel, S. et al. Basement membranes in the cornea and other organs that commonly develop fibrosis. Cell Tissue Res 374, 439–453 (2018). https://doi.org/10.1007/s00441-018-2934-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-018-2934-7

Keywords

Search

Navigation