Skip to main content

Advertisement

Log in

Collagens and proteoglycans of the cornea: importance in transparency and visual disorders

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

Abstract

The cornea represents the external part of the eye and consists of an epithelium, a stroma and an endothelium. Due to its curvature and transparency this structure makes up approximately 70 % of the total refractive power of the eye. This function is partly made possible by the particular organization of the collagen extracellular matrix contained in the corneal stroma that allows a constant refractive power. The maintenance of such an organization involves other molecules such as type V collagen, FACITs (fibril-associated collagens with interrupted triple helices) and SLRPs (small leucine-rich proteoglycans). These components play crucial roles in the preservation of the correct organization and function of the cornea since their absence or modification leads to abnormalities such as corneal opacities. Thus, the aim of this review is to describe the different corneal collagens and proteoglycans by highlighting their importance in corneal transparency as well as their implication in corneal visual disorders.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Adachi E, Hayashi T (1986) In vitro formation of hybrid fibrils of type V collagen and type I collagen. Limited growth of type I collagen into thick fibrils by type V collagen. Connect Tissue Res 14:257–266

    Article  CAS  PubMed  Google Scholar 

  • Akhtar S, Kerr BC, Hayes AJ, Hughes CE, Meek KM, Caterson B (2008) Immunochemical localization of keratan sulfate proteoglycans in cornea, sclera, and limbus using a keratanase-generated neoepitope monoclonal antibody. Invest Ophthalmol Vis Sci 49:2424–2431

    Article  PubMed  Google Scholar 

  • Akimoto Y, Yamakawa N, Furukawa K, Kimata K, Kawakami H, Hirano H (2002) Changes in distribution of the long form of type XII collagen during chicken corneal development. J Histochem Cytochem 50:851–862

    Article  CAS  PubMed  Google Scholar 

  • Alberto D, Garello R (2013) Corneal sublayers thickness estimation obtained by high-resolution FD-OCT. Int J Biomed Imaging 2013:989624

    Article  PubMed Central  PubMed  Google Scholar 

  • Anderson S, SundarRaj S, Fite D, Wessel H, SundarRaj N (2000) Developmentally regulated appearance of spliced variants of type XII collagen in the cornea. Invest Ophthalmol Vis Sci 41:55–63

    CAS  PubMed  Google Scholar 

  • Axelsson I, Heinegard D (1978) Characterization of the keratan sulphate proteoglycans from bovine corneal stroma. Biochem J 169:517–530

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bateman JF, Chan D, Mascara T, Rogers JG, Cole WG (1986) Collagen defects in lethal perinatal osteogenesis imperfecta. Biochem J 240:699–708

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bettelheim FA, Plessy B (1975) The hydration of proteoglycans of bovine cornea. Biochim Biophys Acta 381:203–214

    Article  CAS  PubMed  Google Scholar 

  • Birk DE (2001) Type V collagen: heterotypic type I/V collagen interactions in the regulation of fibril assembly. Micron 32:223–237

    Article  CAS  PubMed  Google Scholar 

  • Birk DE, Fitch JM, Babiarz JP, Linsenmayer TF (1988) Collagen type I and type V are present in the same fibril in the avian corneal stroma. J Cell Biol 106:999–1008

    Article  CAS  PubMed  Google Scholar 

  • Birk DE, Fitch JM, Babiarz JP, Doane KJ, Linsenmayer TF (1990) Collagen fibrillogenesis in vitro: interaction of types I and V collagen regulates fibril diameter. J Cell Sci 95(Pt 4):649–657

    CAS  PubMed  Google Scholar 

  • Blochberger TC, Vergnes JP, Hempel J, Hassell JR (1992) cDNA to chick lumican (corneal keratan sulfate proteoglycan) reveals homology to the small interstitial proteoglycan gene family and expression in muscle and intestine. J Biol Chem 267:347–352

    CAS  PubMed  Google Scholar 

  • Bohme K, Li Y, Oh PS, Olsen BR (1995) Primary structure of the long and short splice variants of mouse collagen XII and their tissue-specific expression during embryonic development. Dev Dyn 204:432–445

    Article  CAS  PubMed  Google Scholar 

  • Bonanno JA (2003) Identity and regulation of ion transport mechanisms in the corneal endothelium. Prog Retin Eye Res 22:69–94

    Article  CAS  PubMed  Google Scholar 

  • Borel JP, Bellon G (1985) Vascular collagens. General review. Pathol Biol (Paris) 33:254–260

    CAS  Google Scholar 

  • Bredrup C, Knappskog PM, Majewski J, Rodahl E, Boman H (2005) Congenital stromal dystrophy of the cornea caused by a mutation in the decorin gene. Invest Ophthalmol Vis Sci 46:420–426

    Article  PubMed  Google Scholar 

  • Cameron GJ, Alberts IL, Laing JH, Wess TJ (2002) Structure of type I and type III heterotypic collagen fibrils: an X-ray diffraction study. J Struct Biol 137:15–22

    Article  CAS  PubMed  Google Scholar 

  • Canty EG, Kadler KE (2005) Procollagen trafficking, processing and fibrillogenesis. J Cell Sci 118:1341–1353

    Article  CAS  PubMed  Google Scholar 

  • Chakravarti S (2006) Focus on molecules: keratocan (KERA). Exp Eye Res 82:183–184

    Article  CAS  PubMed  Google Scholar 

  • Chakravarti S, Magnuson T, Lass JH, Jepsen KJ, LaMantia C, Carroll H (1998) Lumican regulates collagen fibril assembly: skin fragility and corneal opacity in the absence of lumican. J Cell Biol 141:1277–1286

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chang JH, Gabison EE, Kato T, Azar DT (2001) Corneal neovascularization. Curr Opin Ophthalmol 12:242–249

    Article  CAS  PubMed  Google Scholar 

  • Chen S, Birk DE (2011) Focus on molecules: decorin. Exp Eye Res 92:444–445

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chen S, Birk DE (2013) The regulatory roles of small leucine-rich proteoglycans in extracellular matrix assembly. FEBS J 280:2120–2137

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chen L, Kato T, Toshida H, Nakamura S, Murakami A (2005) Immunohistochemical characterization of epithelial cells implanted in the flap-stroma interface of the cornea. Jpn J Ophthalmol 49:79–83

    Article  PubMed  Google Scholar 

  • Chen YT, Huang CW, Huang FC, Tseng SY, Tseng SH (2006) The cleavage plane of corneal epithelial adhesion complex in traumatic recurrent corneal erosion. Mol Vis 12:196–204

    CAS  PubMed  Google Scholar 

  • Chen P, Yin H, Wang Y, Mi J, He W, Xie L, Wang Y (2010) Multi-gene targeted antiangiogenic therapies for experimental corneal neovascularization. Mol Vis 16:310–319

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cintron C, Kublin CL (1977) Regeneration of corneal tissue. Dev Biol 61:346–357

    Article  CAS  PubMed  Google Scholar 

  • Cintron C, Hassinger LC, Kublin CL, Cannon DJ (1978) Biochemical and ultrastructural changes in collagen during corneal wound healing. J Ultrastruct Res 65:13–22

    Article  CAS  PubMed  Google Scholar 

  • Corpuz LM, Funderburgh JL, Funderburgh ML, Bottomley GS, Prakash S, Conrad GW (1996) Molecular cloning and tissue distribution of keratocan. Bovine corneal keratan sulfate proteoglycan 37A. J Biol Chem 271:9759–9763

    Article  CAS  PubMed  Google Scholar 

  • Dawson DG, Kramer TR, Grossniklaus HE, Waring GO 3rd, Edelhauser HF (2005) Histologic, ultrastructural, and immunofluorescent evaluation of human laser-assisted in situ keratomileusis corneal wounds. Arch Ophthalmol 123:741–756

    Article  PubMed  Google Scholar 

  • Del Pero RA, Gigstad JE, Roberts AD, Klintworth GK, Martin CA, L’Esperance FA Jr, Taylor DM (1990) A refractive and histopathologic study of excimer laser keratectomy in primates. Am J Ophthalmol 109:419–429

    Article  PubMed  Google Scholar 

  • Di Iorio E, Barbaro V, Volpi N, Bertolin M, Ferrari B, Fasolo A, Arnaldi R, Brusini P, Prosdocimo G, Ponzin D, Ferrari S (2010) Localization and expression of CHST6 and keratan sulfate proteoglycans in the human cornea. Exp Eye Res 91:293–299

    Article  CAS  PubMed  Google Scholar 

  • Dunlevy JR, Beales MP, Berryhill BL, Cornuet PK, Hassell JR (2000) Expression of the keratan sulfate proteoglycans lumican, keratocan and osteoglycin/mimecan during chick corneal development. Exp Eye Res 70:349–362

    Article  CAS  PubMed  Google Scholar 

  • Ebihara N, Mizushima H, Miyazaki K, Watanabe Y, Ikawa S, Nakayasu K, Kanai A (2000) The functions of exogenous and endogenous laminin-5 on corneal epithelial cells. Exp Eye Res 71:69–79

    Article  CAS  PubMed  Google Scholar 

  • Esipov R, Beyrakhova K, Likhvantseva V, Stepanova E, Stepanenko V, Kostromina M, Abramchik Y, Miroshnikov A (2012) Antiangiogenic and antivascular effects of a recombinant tumstatin-derived peptide in a corneal neovascularization model. Biochimie 94:1368–1375

    Article  CAS  PubMed  Google Scholar 

  • Fichard A, Kleman JP, Ruggiero F (1995) Another look at collagen V and XI molecules. Matrix Biol 14:515–531

    Article  CAS  PubMed  Google Scholar 

  • Font B, Eichenberger D, Goldschmidt D, Boutillon MM, Hulmes DJ (1998) Structural requirements for fibromodulin binding to collagen and the control of type I collagen fibrillogenesis–critical roles for disulphide bonding and the C-terminal region. Eur J Biochem 254:580–587

    Article  CAS  PubMed  Google Scholar 

  • Fournié P, Gordon GM, Ledee DR, Roberts CJ, Fini ME (2008) Corneal stroma: shape, structure and biomechanical properties. In: Brightbill FS, McDonnell PJ, McGhee CNJ, Farjo AA, Serdarevic O (eds) Corneal surgery: theory, technique and tissue (4th edn). Elsevier, New York, pp 33–44

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Funderburgh JL (2000) Keratan sulfate: structure, biosynthesis, and function. Glycobiology 10:951–958

    Article  CAS  PubMed  Google Scholar 

  • Funderburgh JL, Caterson B, Conrad GW (1986) Keratan sulfate proteoglycan during embryonic development of the chicken cornea. Dev Biol 116:267–277

    Article  CAS  PubMed  Google Scholar 

  • Funderburgh JL, Corpuz LM, Roth MR, Funderburgh ML, Tasheva ES, Conrad GW (1997) Mimecan, the 25-kDa corneal keratan sulfate proteoglycan, is a product of the gene producing osteoglycin. J Biol Chem 272:28089–28095

    Article  CAS  PubMed  Google Scholar 

  • Funderburgh JL, Hevelone ND, Roth MR, Funderburgh ML, Rodrigues MR, Nirankari VS, Conrad GW (1998) Decorin and biglycan of normal and pathologic human corneas. Invest Ophthalmol Vis Sci 39:1957–1964

    CAS  PubMed  Google Scholar 

  • Galiacy SD, Fournie P, Massoudi D, Ancele E, Quintyn JC, Erraud A, Raymond-Letron I, Rolling F, Malecaze F (2011) Matrix metalloproteinase 14 overexpression reduces corneal scarring. Gene Ther 18:462–468

    Article  CAS  PubMed  Google Scholar 

  • Ge H, Tian P, Guan L, Yin X, Liu H, Xiao N, Xiong Y, Luo X, Sun Y, Qi D, Ni S, Liu P (2013) A C-terminal fragment BIGH3 protein with an RGDRGD motif inhibits corneal neovascularization in vitro and in vivo. Exp Eye Res 112:10–20

    Article  CAS  PubMed  Google Scholar 

  • Gelse K, Poschl E, Aigner T (2003) Collagens–structure, function, and biosynthesis. Adv Drug Deliv Rev 55:1531–1546

    Article  CAS  PubMed  Google Scholar 

  • Gerecke DR, Meng X, Liu B, Birk DE (2003) Complete primary structure and genomic organization of the mouse Col14a1 gene. Matrix Biol 22:209–216

    Article  CAS  PubMed  Google Scholar 

  • Gipson IK, Spurr-Michaud SJ, Tisdale AS (1987) Anchoring fibrils form a complex network in human and rabbit cornea. Invest Ophthalmol Vis Sci 28:212–220

    CAS  PubMed  Google Scholar 

  • Gipson IK, Spurr-Michaud S, Tisdale A, Keough M (1989) Reassembly of the anchoring structures of the corneal epithelium during wound repair in the rabbit. Invest Ophthalmol Vis Sci 30:425–434

    CAS  PubMed  Google Scholar 

  • Gordon MK, Hahn RA (2010) Collagens. Cell Tissue Res 339:247–257

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gordon MK, Foley JW, Birk DE, Fitch JM, Linsenmayer TF (1994) Type V collagen and Bowman’s membrane quantitation of mRNA in corneal epithelium and stroma. J Biol Chem 269:24959–24966

    CAS  PubMed  Google Scholar 

  • Gordon MK, Foley JW, Lisenmayer TF, Fitch JM (1996) Temporal expression of types XII and XIV collagen mRNA and protein during avian corneal development. Dev Dyn 206:49–58

    Article  CAS  PubMed  Google Scholar 

  • Gould DB, Marchant JK, Savinova OV, Smith RS, John SW (2007) Col4a1 mutation causes endoplasmic reticulum stress and genetically modifiable ocular dysgenesis. Hum Mol Genet 16:798–807

    Article  CAS  PubMed  Google Scholar 

  • Greenhill NS, Ruger BM, Hasan Q, Davis PF (2000) The alpha1(VIII) and alpha2(VIII) collagen chains form two distinct homotrimeric proteins in vivo. Matrix Biol 19:19–28

    Article  CAS  PubMed  Google Scholar 

  • Gregory JD, Coster L, Damle SP (1982) Proteoglycans of rabbit corneal stroma Isolation and partial characterization. J Biol Chem 257:6965–6970

    CAS  PubMed  Google Scholar 

  • Han S, Makareeva E, Kuznetsova NV, DeRidder AM, Sutter MB, Losert W, Phillips CL, Visse R, Nagase H, Leikin S (2010) Molecular mechanism of type I collagen homotrimer resistance to mammalian collagenases. J Biol Chem 285:22276–22281

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hanna KD, Pouliquen Y, Waring GO 3rd, Savoldelli M, Cotter J, Morton K, Menasche M (1989) Corneal stromal wound healing in rabbits after 193-nm excimer laser surface ablation. Arch Ophthalmol 107:895–901

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hassell JR, Newsome DA, Hascall VC (1979) Characterization and biosynthesis of proteoglycans of corneal stroma from rhesus monkey. J Biol Chem 254:12346–12354

    CAS  PubMed  Google Scholar 

  • Hassell JR, Newsome DA, Krachmer JH, Rodrigues MM (1980) Macular corneal dystrophy: failure to synthesize a mature keratan sulfate proteoglycan. Proc Natl Acad Sci U S A 77:3705–3709

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hassell JR, Cintron C, Kublin C, Newsome DA (1983) Proteoglycan changes during restoration of transparency in corneal scars. Arch Biochem Biophys 222:362–369

    Article  CAS  PubMed  Google Scholar 

  • Hatami-Marbini H, Etebu E (2013) Hydration dependent biomechanical properties of the corneal stroma. Exp Eye Res 116:47–54

  • Hayashida Y, Akama TO, Beecher N, Lewis P, Young RD, Meek KM, Kerr B, Hughes CE, Caterson B, Tanigami A, Nakayama J, Fukada MN, Tano Y, Nishida K, Quantock AJ (2006) Matrix morphogenesis in cornea is mediated by the modification of keratan sulfate by GlcNAc 6-O-sulfotransferase. Proc Natl Acad Sci U S A 103:13333–13338

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Helena MC, Baerveldt F, Kim WJ, Wilson SE (1998) Keratocyte apoptosis after corneal surgery. Invest Ophthalmol Vis Sci 39:276–283

    CAS  PubMed  Google Scholar 

  • Igo RP Jr, Kopplin LJ, Joseph P, Truitt B, Fondran J, Bardenstein D, Aldave AJ, Croasdale CR, Price MO, Rosenwasser M, Lass JH, Iyengar SK (2012) Differing roles for TCF4 and COL8A2 in central corneal thickness and fuchs endothelial corneal dystrophy. PLoS ONE 7, e46742

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Illidge C, Kielty C, Shuttleworth A (2001) Type VIII collagen: heterotrimeric chain association. Int J Biochem Cell Biol 33:521–529

    Article  CAS  PubMed  Google Scholar 

  • Iozzo RV (1998) Matrix proteoglycans: from molecular design to cellular function. Annu Rev Biochem 67:609–652

    Article  CAS  PubMed  Google Scholar 

  • Iozzo RV, Moscatello DK, McQuillan DJ, Eichstetter I (1999) Decorin is a biological ligand for the epidermal growth factor receptor. J Biol Chem 274:4489–4492

    Article  CAS  PubMed  Google Scholar 

  • Izu Y, Sun M, Zwolanek D, Veit G, Williams V, Cha B, Jepsen KJ, Koch M, Birk DE (2011) Type XII collagen regulates osteoblast polarity and communication during bone formation. J Cell Biol 193:1115–1130

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jester JV, Petroll WM, Barry PA, Cavanagh HD (1995) Expression of alpha-smooth muscle (alpha-SM) actin during corneal stromal wound healing. Invest Ophthalmol Vis Sci 36:809–819

    CAS  PubMed  Google Scholar 

  • Jun AS, Meng H, Ramanan N, Matthaei M, Chakravarti S, Bonshek R, Black GC, Grebe R, Kimos M (2012) An alpha 2 collagen VIII transgenic knock-in mouse model of Fuchs endothelial corneal dystrophy shows early endothelial cell unfolded protein response and apoptosis. Hum Mol Genet 21:384–393

    Article  CAS  PubMed Central  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

    Article  PubMed Central  PubMed  Google Scholar 

  • Kania AM, Reichenberger E, Baur ST, Karimbux NY, Taylor RW, Olsen BR, Nishimura I (1999) Structural variation of type XII collagen at its carboxyl-terminal NC1 domain generated by tissue-specific alternative splicing. J Biol Chem 274:22053–22059

    Article  CAS  PubMed  Google Scholar 

  • Kao WW, Funderburgh JL, Xia Y, Liu CY, Conrad GW (2006) Focus on molecules: lumican. Exp Eye Res 82:3–4

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Keene DR, Lunstrum GP, Morris NP, Stoddard DW, Burgeson RE (1991) Two type XII-like collagens localize to the surface of banded collagen fibrils. J Cell Biol 113:971–978

    Article  CAS  PubMed  Google Scholar 

  • Kietly CM, Grant ME (2002) The collagen family: structure, assembly, and organization of the extracellular matrix. In: Royce PM, Steinmann B (eds) Connective tissue and its heritable disorders. Wiley, New York, pp 159–221

    Google Scholar 

  • Knupp C, Pinali C, Lewis PN, Parfitt GJ, Young RD, Meek KM, Quantock AJ (2009) The architecture of the cornea and structural basis of its transparency. Adv Protein Chem Struct Biol 78:25–49

    Article  CAS  PubMed  Google Scholar 

  • Koch M, Bernasconi C, Chiquet M (1992) A major oligomeric fibroblast proteoglycan identified as a novel large form of type-XII collagen. Eur J Biochem 207:847–856

    Article  CAS  PubMed  Google Scholar 

  • Koch M, Bohrmann B, Matthison M, Hagios C, Trueb B, Chiquet M (1995) Large and small splice variants of collagen XII: differential expression and ligand binding. J Cell Biol 130:1005–1014

    Article  CAS  PubMed  Google Scholar 

  • Lai LJ, Xiao X, Wu JH (2007) Inhibition of corneal neovascularization with endostatin delivered by adeno-associated viral (AAV) vector in a mouse corneal injury model. J Biomed Sci 14:313–322

    Article  CAS  PubMed  Google Scholar 

  • Li W, Vergnes JP, Cornuet PK, Hassell JR (1992) cDNA clone to chick corneal chondroitin/dermatan sulfate proteoglycan reveals identity to decorin. Arch Biochem Biophys 296:190–197

    Article  CAS  PubMed  Google Scholar 

  • Linsenmayer TF, Fitch JM, Schmid TM, Zak NB, Gibney E, Sanderson RD, Mayne R (1983) Monoclonal antibodies against chicken type V collagen: production, specificity, and use for immunocytochemical localization in embryonic cornea and other organs. J Cell Biol 96:124–132

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Linsenmayer TF, Gibney E, Igoe F, Gordon MK, Fitch JM, Fessler LI, Birk DE (1993) Type V collagen: molecular structure and fibrillar organization of the chicken alpha 1(V) NH2-terminal domain, a putative regulator of corneal fibrillogenesis. J Cell Biol 121:1181–1189

    Article  CAS  PubMed  Google Scholar 

  • Liu CY, Birk DE, Hassell JR, Kane B, Kao WW (2003) Keratocan-deficient mice display alterations in corneal structure. J Biol Chem 278:21672–21677

    Article  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 

  • Ljubimov AV, Alba SA, Burgeson RE, Ninomiya Y, Sado Y, Sun TT, Nesburn AB, Kenney MC, Maguen E (1998) Extracellular matrix changes in human corneas after radial keratotomy. Exp Eye Res 67:265–272

    Article  CAS  PubMed  Google Scholar 

  • Maatta M, Heljasvaara R, Sormunen R, Pihlajaniemi T, Autio-Harmainen H, Tervo T (2006) Differential expression of collagen types XVIII/endostatin and XV in normal, keratoconus, and scarred human corneas. Cornea 25:341–349

    Article  PubMed  Google Scholar 

  • Madisen L, Neubauer M, Plowman G, Rosen D, Segarini P, Dasch J, Thompson A, Ziman J, Bentz H, Purchio AF (1990) Molecular cloning of a novel bone-forming compound: osteoinductive factor. DNA Cell Biol 9:303–309

    Article  CAS  PubMed  Google Scholar 

  • Maguen E, Alba SA, Burgeson RE, Butkowski RJ, Michael AF, Kenney MC, Nesburn AB, Ljubimov AV (1997) Alterations of corneal extracellular matrix after multiple refractive procedures: a clinical and immunohistochemical study. Cornea 16:675–682

    Article  CAS  PubMed  Google Scholar 

  • Marchant JK, Hahn RA, Linsenmayer TF, Birk DE (1996) Reduction of type V collagen using a dominant-negative strategy alters the regulation of fibrillogenesis and results in the loss of corneal-specific fibril morphology. J Cell Biol 135:1415–1426

    Article  CAS  PubMed  Google Scholar 

  • Massoudi D, Malecaze F, Soler V, Butterworth J, Erraud A, Fournie P, Koch M, Galiacy SD (2012) NC1 long and NC3 short splice variants of type XII collagen are overexpressed during corneal scarring. Invest Ophthalmol Vis Sci 53:7246–7256

    Article  CAS  PubMed  Google Scholar 

  • Meek KM, Quantock AJ, Boote C, Liu CY, Kao WW (2003) An X-ray scattering investigation of corneal structure in keratocan-deficient mice. Matrix Biol 22:467–475

    Article  CAS  PubMed  Google Scholar 

  • Merjava S, Liskova P, Sado Y, Davis PF, Greenhill NS, Jirsova K (2009) Changes in the localization of collagens IV and VIII in corneas obtained from patients with posterior polymorphous corneal dystrophy. Exp Eye Res 88:945–952

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Midura RJ, Hascall VC, MacCallum DK, Meyer RF, Thonar EJ, Hassell JR, Smith CF, Klintworth GK (1990) Proteoglycan biosynthesis by human corneas from patients with types 1 and 2 macular corneal dystrophy. J Biol Chem 265:15947–15955

    CAS  PubMed  Google Scholar 

  • Mohan RR, Tovey JC, Gupta R, Sharma A, Tandon A (2011) Decorin biology, expression, function and therapy in the cornea. Curr Mol Med 11:110–128

    Article  CAS  PubMed  Google Scholar 

  • Murthy RC, McFarland TJ, Yoken J, Chen S, Barone C, Burke D, Zhang Y, Appukuttan B, Stout JT (2003) Corneal transduction to inhibit angiogenesis and graft failure. Invest Ophthalmol Vis Sci 44:1837–1842

    Article  PubMed  Google Scholar 

  • Musselmann K, Hassell JR (2006) Focus on molecules: CHST6 (carbohydrate sulfotransferase 6; corneal N-acetylglucosamine-6-sulfotransferase). Exp Eye Res 83:707–708

    Article  CAS  PubMed  Google Scholar 

  • Neame PJ, Kay CJ, McQuillan DJ, Beales MP, Hassell JR (2000) Independent modulation of collagen fibrillogenesis by decorin and lumican. Cell Mol Life Sci 57:859–863

    Article  CAS  PubMed  Google Scholar 

  • Nishiyama T, McDonough AM, Bruns RR, Burgeson RE (1994) Type XII and XIV collagens mediate interactions between banded collagen fibers in vitro and may modulate extracellular matrix deformability. J Biol Chem 269:28193–28199

    CAS  PubMed  Google Scholar 

  • Noske W, Fromm M, Levarlet B, Kreusel KM, Hirsch M (1994) Tight junctions of the human corneal endothelium: morphological and electrophysiological features. Ger J Ophthalmol 3:253–257

    CAS  PubMed  Google Scholar 

  • Oh SP, Griffith CM, Hay ED, Olsen BR (1993) Tissue-specific expression of type XII collagen during mouse embryonic development. Dev Dyn 196:37–46

    Article  CAS  PubMed  Google Scholar 

  • Pellegata NS, Dieguez-Lucena JL, Joensuu T, Lau S, Montgomery KT, Krahe R, Kivela T, Kucherlapati R, Forsius H, de la Chapelle A (2000) Mutations in KERA, encoding keratocan, cause cornea plana. Nat Genet 25:91–95

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Rada JA, Cornuet PK, Hassell JR (1993) Regulation of corneal collagen fibrillogenesis in vitro by corneal proteoglycan (lumican and decorin) core proteins. Exp Eye Res 56:635–648

    Article  CAS  PubMed  Google Scholar 

  • Rodahl E, Van Ginderdeuren R, Knappskog PM, Bredrup C, Boman H (2006) A second decorin frame shift mutation in a family with congenital stromal corneal dystrophy. Am J Ophthalmol 142:520–521

    Article  CAS  PubMed  Google Scholar 

  • Rodahl E, Knappskog PM, Majewski J, Johansson S, Telstad W, Krakenes J, Boman H (2013) Variants of anterior segment dysgenesis and cerebral involvement in a large family with a novel COL4A1 mutation. Am J Ophthalmol 155:946–953

    Article  CAS  PubMed  Google Scholar 

  • Saika S, Ooshima A, Shima K, Tanaka S, Ohnishi Y (1996) Collagen types in healing alkali-burned corneal stroma in rabbits. Jpn J Ophthalmol 40:303–309

    CAS  PubMed  Google Scholar 

  • Scott JE, Haigh M (1985) ‘Small’-proteoglycan:collagen interactions: keratan sulphate proteoglycan associates with rabbit corneal collagen fibrils at the ‘a’ and ‘c’ bands. Biosci Rep 5:765–774

    Article  CAS  PubMed  Google Scholar 

  • Scott JE, Haigh M (1988) Identification of specific binding sites for keratan sulphate proteoglycans and chondroitin-dermatan sulphate proteoglycans on collagen fibrils in cornea by the use of cupromeronic blue in ‘critical-electrolyte-concentration’ techniques. Biochem J 253:607–610

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Seppinen L, Pihlajaniemi T (2011) The multiple functions of collagen XVIII in development and disease. Matrix Biol 30:83–92

    Article  CAS  PubMed  Google Scholar 

  • Shaw LM, Olsen BR (1991) FACIT collagens: diverse molecular bridges in extracellular matrices. Trends Biochem Sci 16:191–194

    Article  CAS  PubMed  Google Scholar 

  • Shinomura T, Kimata K (1992) Proteoglycan-Lb, a small dermatan sulfate proteoglycan expressed in embryonic chick epiphyseal cartilage, is structurally related to osteoinductive factor. J Biol Chem 267:1265–1270

    CAS  PubMed  Google Scholar 

  • Smith LT, Holbrook KA, Madri JA (1986) Collagen types I, III, and V in human embryonic and fetal skin. Am J Anat 175:507–521

    Article  CAS  PubMed  Google Scholar 

  • Soriano ES, Campos MS, Michelacci YM (2000) Effect of epithelial debridement on glycosaminoglycan synthesis by human corneal explants. Clin Chim Acta 295:41–62

    Article  CAS  PubMed  Google Scholar 

  • Sun M, Chen S, Adams SM, Florer JB, Liu H, Kao WW, Wenstrup RJ, Birk DE (2011) Collagen V is a dominant regulator of collagen fibrillogenesis: dysfunctional regulation of structure and function in a corneal-stroma-specific Col5a1-null mouse model. J Cell Sci 124:4096–4105

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sundarraj N, Fite D, Belak R, Sundarraj S, Rada J, Okamoto S, Hassell J (1998) Proteoglycan distribution during healing of corneal stromal wounds in chick. Exp Eye Res 67:433–442

    Article  CAS  PubMed  Google Scholar 

  • Tanihara H, Inatani M, Koga T, Yano T, Kimura A (2002) Proteoglycans in the eye. Cornea 21:S62–S69

    Article  PubMed  Google Scholar 

  • Tasheva ES, Koester A, Paulsen AQ, Garrett AS, Boyle DL, Davidson HJ, Song M, Fox N, Conrad GW (2002) Mimecan/osteoglycin-deficient mice have collagen fibril abnormalities. Mol Vis 8:407–415

    CAS  PubMed  Google Scholar 

  • Tuori AJ, Virtanen I, Aine E, Kalluri R, Miner JH, Uusitalo HM (1997) The immunohistochemical composition of corneal basement membrane in keratoconus. Curr Eye Res 16:792–801

    Article  CAS  PubMed  Google Scholar 

  • Tzortzaki EG, Tischfield JA, Sahota A, Siafakas NM, Gordon MK, Gerecke DR (2003) Expression of FACIT collagens XII and XIV during bleomycin-induced pulmonary fibrosis in mice. Anat Rec A 275:1073–1080

    Article  CAS  Google Scholar 

  • Van Agtmael T, Schlotzer-Schrehardt U, McKie L, Brownstein DG, Lee AW, Cross SH, Sado Y, Mullins JJ, Poschl E, Jackson IJ (2005) Dominant mutations of Col4a1 result in basement membrane defects which lead to anterior segment dysgenesis and glomerulopathy. Hum Mol Genet 14:3161–3168

    Article  PubMed  Google Scholar 

  • van der Rest M, Dublet B, Champliaud MF (1990) Fibril-associated collagens. Biomaterials 11:28–31

    PubMed  Google Scholar 

  • Veit G, Hansen U, Keene DR, Bruckner P, Chiquet-Ehrismann R, Chiquet M, Koch M (2006) Collagen XII interacts with avian tenascin-X through its NC3 domain. J Biol Chem 281:27461–27470

    Article  CAS  PubMed  Google Scholar 

  • Walchli C, Koch M, Chiquet M, Odermatt BF, Trueb B (1994) Tissue-specific expression of the fibril-associated collagens XII and XIV. J Cell Sci 107(Pt 2):669–681

    CAS  PubMed  Google Scholar 

  • Wessel H, Anderson S, Fite D, Halvas E, Hempel J, SundarRaj N (1997) Type XII collagen contributes to diversities in human corneal and limbal extracellular matrices. Invest Ophthalmol Vis Sci 38:2408–2422

    CAS  PubMed  Google Scholar 

  • Wilson SE, Kim WJ (1998) Keratocyte apoptosis: implications on corneal wound healing, tissue organization, and disease. Invest Ophthalmol Vis Sci 39:220–226

    CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Yamagata M, Yamada KM, Yamada SS, Shinomura T, Tanaka H, Nishida Y, Obara M, Kimata K (1991) The complete primary structure of type XII collagen shows a chimeric molecule with reiterated fibronectin type III motifs, von Willebrand factor A motifs, a domain homologous to a noncollagenous region of type IX collagen, and short collagenous domains with an Arg-Gly-Asp site. J Cell Biol 115:209–221

    Article  CAS  PubMed  Google Scholar 

  • Ying S, Shiraishi A, Kao CW, Converse RL, Funderburgh JL, Swiergiel J, Roth MR, Conrad GW, Kao WW (1997) Characterization and expression of the mouse lumican gene. J Biol Chem 272:30306–30313

    Article  CAS  PubMed  Google Scholar 

  • Ylikarppa R, Eklund L, Sormunen R, Kontiola AI, Utriainen A, Maatta M, Fukai N, Olsen BR, Pihlajaniemi T (2003) Lack of type XVIII collagen results in anterior ocular defects. FASEB J 17:2257–2259

    PubMed  Google Scholar 

  • Young BB, Gordon MK, Birk DE (2000) Expression of type XIV collagen in developing chicken tendons: association with assembly and growth of collagen fibrils. Dev Dyn 217:430–439

    Article  CAS  PubMed  Google Scholar 

  • Young BB, Zhang G, Koch M, Birk DE (2002) The roles of types XII and XIV collagen in fibrillogenesis and matrix assembly in the developing cornea. J Cell Biochem 87:208–220

    Article  CAS  PubMed  Google Scholar 

  • Zhang G, Ezura Y, Chervoneva I, Robinson PS, Beason DP, Carine ET, Soslowsky LJ, Iozzo RV, Birk DE (2006) Decorin regulates assembly of collagen fibrils and acquisition of biomechanical properties during tendon development. J Cell Biochem 98:1436–1449

    Article  CAS  PubMed  Google Scholar 

  • Zieske JD, Guimaraes SR, Hutcheon AE (2001) Kinetics of keratocyte proliferation in response to epithelial debridement. Exp Eye Res 72:33–39

    Article  CAS  PubMed  Google Scholar 

  • Zwolanek D, Veit G, Eble JA, Gullberg D, Ruggiero F, Heino J, et al. (2014) Collagen XXII binds to collagen binding integrins via the novel motifs GLQGER and GFKGER. Biochem J. doi:10.1042/BJ20130642

Download references

Acknowledgment

We thank Dr David Hulmes for helpful comments on the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stephane D. Galiacy.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Massoudi, D., Malecaze, F. & Galiacy, S.D. Collagens and proteoglycans of the cornea: importance in transparency and visual disorders. Cell Tissue Res 363, 337–349 (2016). https://doi.org/10.1007/s00441-015-2233-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-015-2233-5

Keywords

Navigation