Development of the corneal stroma, and the collagen-proteoglycan associations that help define its structure and function

Developmental Dynamics

Volumn 237, Issue 10, 2008, Pages 2607-2621

  Quantock, Andrew J ^a   Young, Robert D ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

Collagen; Cornea; Corneal development; Glycosaminoglycans; Proteoglycans

Indexed keywords

COLLAGEN; COLLAGEN FIBRIL; GLYCOSAMINOGLYCAN; KERATOCAN; PROTEOGLYCAN;

BIOCHEMISTRY; CELL GROWTH; CELL INVASION; CELL MATURATION; CELL MIGRATION; CHICK; CONNECTIVE TISSUE; CORNEA; CORNEA CELL; CORNEA OPACITY; CORNEA STROMA; EMBRYO DEVELOPMENT; GENE EXPRESSION; HUMAN; MAMMAL; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; STRUCTURE ANALYSIS; TECHNOLOGY; TISSUE STRUCTURE;

ANIMALS; COLLAGEN; CORNEAL STROMA; EXTRACELLULAR MATRIX; HUMANS; PROTEOGLYCANS;

EID: 54549084469     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.21579     Document Type: Review

References (130)

1. 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.
2. 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.
3. Anseth A. 1961. Glycosaminoglycans in the developing corneal stroma. Exp Eye Res 1:116-121.
4. Bard JB, Hay ED. 1975. The behavior of fibroblasts from the developing avian cornea. Morphology and movement in situ and in vitro. J Cell Biol 67:400-418.
5. Bard JB, Higginson K. 1977. Fibroblast-collagen interactions in the formation of the secondary stroma of the chick cornea. J Cell Biol 74:816-827.
6. Bard JB, Kratochwil K. 1987. Corneal morphogenesis in the Mov13 mutant mouse is characterized by normal cellular organization but disordered and thin collagen. Development 101:547-555.
7. Bard JB, Bansal MK, Ross AS. 1988. The extracellular matrix of the developing cornea: deposition and function. Development 103:195-205.
8. Beecher N, Chakravarti S, Joyce S, Meek KM, Quantock AJ. 2006. Neonatal development of the corneal stroma in wild-type and lumican-null mice. Invest Ophthalmol Vis Sci 47:146-150.
9. Benedek GB. 1971. Theory of transparency of the eye. Appl Opt 10:459-473.
10. Bettelheim FA, Plessy B. 1975. The hydration of proteoglycans of bovine cornea. Biochim Biophys Acta 381:203-214.
11. Birk DE, Trelstad RL. 1984. Extracellular compartments in matrix morphogenesis: collagen fibril, bundle, and lamellar formation by corneal fibroblasts. J Cell Biol 99:2024-2033.
12. Birk DE, Fitch JM, Linsenmayer TF. 1986. Organisation of collagen types I and V in the embryonic chicken cornea. Invest Ophthalmol Vis Sci 27:1470-1477.
13. 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.
14. Birk DE, Fitch JF, Babiarz JP, Doane KJ, Linsenmayer TF. 1990. Collagen fibrillogenesis in vitro: interaction of types I and V collagen regulates fibril diameter. J Cell Sci 95:649-657.
15. Blochberger TC, Vergnes JP, Hempel J, Hassell JR. 1992a. 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.
16. Blochberger TC, Cornuet PK, Hassell JR. 1992b. Isolation and partial characterization of lumican and decorin from adult chicken corneas. A keratan sulfate-containing isoform of decorin is developmentally regulated. J Biol Chem 267:20613-20619.
17. Borcherding MS, Blacik LJ, Sittig RA, Bizzell JW, Breen M, Weinstein HG. 1975. Proteoglycans and collagen fibre organization in human corneoscleral tissue. Exp Eye Res 21:59-70.
18. Cai CX, Fitch JM, Svoboda KK, Birk DE, Linsenmayer TF. 1994. Cellular invasion and collagen type IX in the primary corneal stroma in vitro. Dev Dyn 201:206-215.
19. Cai CX, Gibney E, Gordon MK, Marchant JK, Birk DE, Linsenmayer TF. 1996. Characterization and developmental regulation of avian corneal β-1,4-galactosyltransferase mRNA. Exp Eye Res 63:193-200.
20. Canty EG, Kadler KE. 2005. Procollagen trafficking, processing and fibrillogenesis. J Cell Sci 118:1341-1353.
21. Canty EG, Lu Y, Meadows RS, Shaw MK, Holmes DF, Kadler KE. 2004. Coalignment of plasma membrane channels and protrusions (fibripositors) specifies the parallelism of tendon. J Cell Biol 165:553-563.
22. Carlson EC, Liu C-Y, Chikama T-I, Hayashi Y, Kao CW-C, Birk DE, Funderburgh JL, Jester JV, Kao WW. 2005. Keratocan, a cornea-specific keratan sulphate proteoglycan, is regulated by lumican. J Biol Chem 280:25541-25547.
23. 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.
24. Chakravarti S, Petroll WM, Hassell JR, Jester JV, Lass JH, Paul J, Birk DE. 2000. Corneal opacity in lumican-null mice: defects in collagen fibril structure and packing in the posterior stroma. Invest Ophthalmol Vis Sci 41:3365-3373.
25. Chakravarti S, Zhang G, Chervoneva I, Roberts L, Birk DE. 2006. Collagen fibril assembly during postnatal development and dysfunctional regulation in the lumican-deficient murine cornea. Dev Dyn 235:2493-2506.
26. Chen Q, Fitch JM, Gibney E, Linsenmayer TF. 1993. Type II collagen during cartilage and corneal development: immunohistochemical analysis with an anti-telopeptide antibody. Dev Dyn 196:47-53.
27. Cho HI, Covington HI, Cintron C. 1990. Immunolocalization of type VI collagen in developing and healing rabbit cornea. Invest Ophthalmol Vis Sci 31:1096-1102.
28. Cintron C, Covington HI. 1990. Proteoglycan distribution in developing rabbit cornea. J Histochem Cytochem 38:675-684.
29. Cintron C, Hong BS, Kublin CL. 1981. Quantitative analysis of collagen from normal developing corneas and corneal scars. Curr Eye Res 1:1-8.
30. Cintron C, Szamier RB, Hassinger LC, Kublin CL. 1982. Scanning electron microscopy of rabbit corneal scars. Invest Ophthalmol Vis Sci 23:50-63.
31. Cintron C, Covington H, Kublin CL. 1983. Morphogenesis of rabbit corneal stroma. Invest Ophthalmol Vis Sci 24:543-556.
32. Cintron C, Covington HI, Kublin CL. 1988. Morphogenesis of rabbit corneal endothelium. Curr Eye Res 7:913-929.
33. Connon CJ, Siegler V, Meek KM, Hodson SA, Caterson B, Kinoshita S, Quantock AJ. 2003. Proteoglycan alterations and collagen reorganisation in the secondary avian cornea during development. Ophthalmic Res 35:177-184.
34. Connon CJ, Meek KM, Kinoshita S, Quantock AJ. 2004. Spatial and temporal alterations in the collagen fibrillar array during the onset of transparency in the avian cornea. Exp Eye Res 78:909-915.
35. Conrad GW. 1970. Collagen and mucopolysaccharide biosynthesis in the developing chick cornea. Dev Biol 21:292-317.
36. Conrad AH, Conrad GW. 2003. The keratocan gene is expressed in both ocular and non-ocular tissues during early chick development. Matrix Biol 22:323-337.
37. Conrad AH, Zhang Y, Walker AR, Olberding LA, Hanzlick A, Zimmer AJ, Morffi R, Conrad GW. 2006. Thyroxine affects expression of KSPG-related genes, the carbonic anhydrase II gene, and KS sulphation in the embryonic chicken cornea. Invest Ophthalmol Vis Sci 47:120-132.
38. Cornuet PK, Blochberger TC, Hassell JR. 1994. Molecular polymorphism of lumican during corneal development. Invest Ophthalmol Vis Sci 35:870-877.
39. 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.
40. Coulombre AJ, Coulombre JL. 1958. Corneal development. I. Corneal transparency. J Cell Comp Physiol 51:1-11.
41. Coulombre AJ, Coulombre JL. 1961. The development of the structural and optical properties of the cornea. In: Smelser GK, editor. The structure of the eye. London and New York: Academic Press. p 405-420.
42. Cox JL, Farrell RA, Hart RW, Langham ME. 1970. The transparency of the mammalian cornea. J Physiol 210:601-616.
43. Doane KJ, Birk DE. 1991. Fibroblasts retain their tissue phenotype when grown in three-dimensional collagen gels. Exp Cell Res 195:432-442.
44. Doane KJ, Birk DE. 1994. Differences in integrin expression during avian corneal stromal development. Invest Ophthalmol Vis Sci 35:2834-2842.
45. Doane KJ, Ting WH, McLaughlin JS, Birk DE. 1996. Spatial and temporal variations in extracellular matrix of periocular and corneal regions during corneal stromal development. Exp Eye Res 62:271-283.
46. Doutch J, Tucker C, Quantock AJ, Ade PAR, Meek KM. 2007. Propagation of infrared wavelengths through the corneal stroma, with reference to hydration changes. Proc SPIE 6535:65350V1-8.
47. Dunlevy JR, Neame PJ, Vergnes J-P, Hassell JR. 1998. Identification on the N-linked oligosaccharide sites in chick corneal lumican and keratocan that receive keratan sulfate. J Biol Chem 273:9615-9621.
48. 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.
49. Farrell RA. 1994. Corneal transparency. In: Albert DM, Jacobiec SA, editors. Principles and practice of ophthalmology. Philadelphia: WB Saunders.
50. Fitch JM, Mentzer A, Mayne R, Linsenmayer TF. 1988. Acquisition of type IX collagen by the developing avian primary corneal stroma and vitreous. Dev Biol 128:396-405.
51. Fitch JM, Birk DE, Linsenmayer CA, Linsenmayer TF. 1990. The spatial organisation of Descemet's membrane-associated type IV collagen in the avian cornea. J Cell Biol 110:1457-1468.
52. Fitch JM, Birk DE, Linsenmayer C, Linsenmayer TF. 1991. Stromal assemblies containing collagen types IV and VI and fibronectin in the developing embryonic avian cornea. Dev Biol 144:379-391.
53. Fitch JM, Linsenmayer CM, Linsenmayer TF. 1994. Collagen fibril assembly in the developing avian primary corneal stroma. Invest Ophthalmol Vis Sci 35:862-869.
54. Fitch J, Fini ME, Beebe DC, Linsenmayer TF. 1998. Collagen type IX and developmentally regulated swelling of the avian primary corneal stroma. Dev Dyn 212:27-37.
55. Fitch JM, Kidder JM, Linsenmayer TF. 2005. Cellular invasion of the chicken corneal stroma during development: regulation by multiple matrix metalloproteases and the lens. Dev Dyn 232:106-118.
56. Freund DE, McCally RL, Farrell RA. 1986. Direct summation of fields for light scattering by fibrils with applications to normal corneas. Appl Opt 25:2739-2746.
57. Funderburgh JL, Caterson B, Conrad GW. 1986. Keratan sulfate proteoglycan during embryonic development of the chicken cornea. Dev Biol 116:267-277.
58. 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.
59. Gealy C, Kerr B, Young RD, Tudor D, Hayes A, Hughes C, Caterson B, Quantock AJ, Ralphs J. 2007. Differential expression of the keratan sulphate proteoglycan, keratocan, during chick corneal embryogenesis. Histochem Cell Biol 128:551-555.
60. Giraud-Guille MM. 1996. Twisted liquid crystalline supramolecular arrangements in morphogenesis. Int Rev Cytol 166:59-101.
61. Giraud-Guille MM, Besseau L, Martin R. 2003. Liquid crystalline assemblies of collagen in bone and in vitro systems. J Biomech 36:1571-1579.
62. Gordon MK, Gerecke DR, Olsen BR. 1987. Type XII collagen: distinct extracellular matrix component discovered by cDNA cloning. Proc Natl Acad Sci U S A 84:6040-6044.
63. Gordon MK, Foley JW, Linsenmayer TF, Fitch JM. 1996. Temporal expression of types XII and XIV collagen mRNA and protein during avian corneal development. Dev Dyn 206:49-58.
64. Grant DS, Leblond CP. 1988. Immunogold quantitation of laminin, type IV collagen and heparan sulphate proteoglycan in a variety of basement membranes. J Histochem Cytochem 36:271-283.
65. Gregory JD, Damle SP, Covington HI, Cintron C. 1988. Developmental changes in proteoglycans of rabbit corneal stroma. Invest Ophthalmol Vis Sci 29:1413-1417.
66. Guo X, Hutcheon AEK, Suzanna A. Melotti SA, James D. Zieske JD, Trinkaus-Randall V, Ruberti JW. 2007. Morphologic characterization of organized extracellular matrix deposition by ascorbic acid-stimulated human corneal fibroblasts. Invest Ophthalmol Vis Sci 48:4050-4060.
67. Hahn RA, Birk DE. 1992. β-D xyloside alters dermatan sulfate proteoglycan synthesis and the organization of the developing avian corneal stroma. Development 115:383-393.
68. Hart GW. 1976. Biosynthesis of glycosaminoglycans during corneal development. J Biol Chem 251:6513-6521.
69. Hart RW, Farrell RA. 1969. Light scattering in the cornea. J Opt Soc Am 59:766-774.
70. Hassell JR, Cintron C, Kublin C, Newsome DA. 1983. Proteoglycan changes during restoration of transparency in corneal scars. Arch Biochem Biophys 222:362-369.
71. Haustein J. 1983. On the ultrastructure of the developing and adult mouse corneal stroma. Anat Embryol (Berl) 168:291-305.
72. Hay ED, Revel J-P. 1969. Fine structure of the developing avian cornea. In: Wolsky A, Chen PS, editors. Monographs in developmental biology. Vol. 1. Basel: S. Karger. p 1-144.
73. Hayashi M, Ninomiya Y, Hayashi K, Linsenmayer TF, Olsen BR, Trelstad RL. 1988. Secretion of collagen types I and II by epithelial and endothelial cells in the developing chick cornea demonstrated by in situ hybridization and immunohistochemistry. Development 103:27-36.
74. Hendrix MJ, Hay ED, von der Mark K, Linsenmayer TF. 1982. Immunohistochemical localization of collagen types I and II in the developing chick cornea and tibia by electron microscopy. Invest Ophthalmol Vis Sci 22:359-375.
75. Hirsch M, Noske W, Prenant G, Renard G. 1999. Fine structure of the developing avian corneal stroma as revealed by quick-freeze, deep-etch electron microscopy. Exp Eye Res 69:267-277.
76. Hopfer U, Fukai N, Hopfer H, Wolf G, Joyce N, Li E, Olsen BR. 2005. Targeted disruption of Col8a1 and Col8a2 genes in mice leads to anterior segment abnormalities in the eye. FASEB J 19:1232-1244.
77. Huh MI, Lee YM, Seo SK, Kang BS, Chang Y, Lee YS, Fini ME, Kang SS, Jung JC. 2007. Roles of MMP/TIMP in regulating matrix swelling and cell migration during chick corneal development. J Cell Biochem 101:1222-1237.
78. Kessler L. 1877. Zur Entwicklung des Auges der Wirbeltiere (Vogel, Leipzig, 1877)
79. Kielty CM, Grant ME. 2002. The collagen family: structure, assembly and organization in the extracellular matrix. In: Royce PM, Steinman B, editors. Connective tissue and its heritable disorders. Part 1. New York: Wiley-Liss. p 159-221.
80. Koch M, Laub F, Zhou P, Hahn RA, Tanaka S, Burgeson RE, Gerecke DR, Ramirez F, Gordon MK. 2003. Collagen XXIV, a vertebrate fibrillar collagen with structural features of invertebrate collagens: selective expression in developing cornea and bone. J Biol Chem 278:43236-43244.
81. Koch M, Veit G, Stricker S, Bhatt P, Kutsch S, Zhou P, Reinders E, Hahn RA, Song R, Burgeson RE, Gerecke DR, Mundlos S, Gordon MK. 2006. Expression of type XXIII collagen mRNA and protein. J Biol Chem 281:21546-21557.
82. 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.
83. Laguesse E. 1926. Development de la cornee chez le poulet: role du mesostroma son impenance generale les membranes busales. Arch d'Anat Microsc 22:216-265.
84. Lewis PN, Quantock A, Meek K, Knupp C. 2008. Three dimensional structural organisation of collagen proteoglycan interactions in the cornea. ARVO abstract.
85. Li W, Vergnes J-P, Cornuet PK, Hassell JR. 1992. cDNA clone to chick corneal chondroitin dermatan sulfate proteoglycan reveals identity to decorin. Arch Biochem Biophys 296:190-197.
86. 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.
87. Linsenmayer TF, Smith GN, Hay ED. 1977. Synthesis of 2 collagen types by embryonic chick corneal epithelium in vitro. Proc Natl Acad Sci U S A 74:39-43.
88. Linsenmayer TF, Fitch JM, Mayne R. 1984. Extracellular matrices in the developing avian eye: type V collagen in corneal and noncorneal tissues. Invest Ophthalmol Vis Sci 25:41-47.
89. Linsenmayer TF, Bruns RR, Mentzer A, Mayne R. 1986a. Type VI collagen immunohistochemical identification as a filamentous component of the extracellular matrix of the developing avian corneal stroma. Dev Biol 118:425-431.
90. Linsenmayer TF, Gibney E, Fitch JM. 1986b. Embryonic avian cornea contains layers of collagen with greater than average stability. J Cell Biol 103:1587-1593.
91. Linsenmayer TF, Gibney E, Gordon MK, Marchant JK, Hayashi M, Fitch JM. 1990. Extracellular matrices of the developing chick retina and cornea. Localization of mRNAs for collagen types II and IX by in situ hybridization. Invest Ophthalmol Vis Sci 31:1271-1276.
92. Linsenmayer TF, Fitch JM, Gordon MK, Cai CX, Igoe F, Marchant JK, Birk DE. 1998. Development and roles of collagenous matrices in the embryonic avian cornea. Prog Retin Eye Res 17:231-265.
93. Liu C-Y, Shiraishi A, Kao CW, Converse RL, Funderburgh JL, Corpus LM, Conrad GW, Kao WW. 1998. The cloning of mouse keratocan cDNA and genomic DNA and the characterization of its expression during eye development. J Biol Chem 273:22584-22588.
94. Marchant JK, Zhang G, Birk DE. 2002. Association of type XII collagen with regions of increased stability and keratocyte debsity in the cornea. Exp Eye Res 75:683-694.
95. Marneros AG, Olsen BR. 2005. Physiological role of collagen XVIII and endostatin. FASEB J 19:716-728.
96. Maurice DM. 1957. The structure and transparency of the cornea. J Physiol (Lond) 186:263-286.
97. Meek KM, Quantock AJ. 2001. The use of x-ray scattering techniques to determine corneal ultrastructure. Prog Retin Eye Res 20:95-137.
98. Midura RJ, Hascall VC. 1989. Analysis of the proteoglycans synthesized by corneal explants from embryonic chicken. II. Structural characterization of the keratan sulfate and dermatan sulfate proteoglycans from corneal stroma. J Biol Chem 264:1423-1430.
99. Musselmann K, Kane B, Alexandrou B, Hassell JR. 2006. Stimulation of collagen synthesis by insulin and proteoglycan accumulation by ascorbate in bovine keratocytes in vitro. Invest Ophthalmol Vis Sci 47:5260-5266.
100. Norman B, Davis J, Piatigorsky J. 2004. Postnatal gene expression in the normal mouse cornea by SAGE. Invest Ophthalmol Vis Sci 45:429-440.
101. 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.
102. Ozanics V, Rayborn M, Sagun D. 1977. Observations on the morphology of the developing primate corneal epithelium, its innervation and anterior stroma. J Morphol 153:263-297.
103. Pins GD, Christiansen DL, Patel R, Silver FH. 1997. Self-assembly of collagen fibres. Influence of fibrillar alignment and decorin on mechanical properties. Biophys J 73:2164-2172.
104. Plumb DA, Dhir V, Mironov A, Ferrara L, Poulsom R, Kadler KE, Thornton DJ, Briggs MD, Boot-Handford RP. 2007. Collagen XXVII is developmentally regulated and forms thin fibrillar structures distinct from those of classical vertebrate fibrillar collagens. J Biol Chem 282:12791-12795.
105. Quantock AJ, Kinoshita S, Capel MC, Schanzlin DJ. 1998. A synchrotron x-ray diffraction study of developing chick corneas. Biophys J 74:995-998.
106. Quantock AJ, Meek KM, Chakravarti S. 2001. An x-ray diffraction investigation of corneal structure in lumican-deficient mice. Invest Ophthalmol Vis Sci 42:1750-1756.
107. Quantock AJ, Boote C, Siegler V, Meek KM. 2003. Collagen organization in the secondary chick cornea during development. Invest Ophthalmol Vis Sci 44:130-136.
108. Quantock AJ, Boote C, Young RD, Hayes S, Tanioka H, Kawasaki S, Ohta N, Iida T, Yagi N, Kinoshita S, Meek KM. 2007. Small-angle fibre diffraction studies of corneal matrix structure: a depth-profiled investigation of the human eyebank cornea. J Appl Crystal 40:335-340.
109. Rada J, 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.
110. Saika S, Okada Y, Miyamoto T, Yamanaka O, Ohnishi Y, Yamanaka A, Ooshima A. 2004. Protein expression pattern of collagen type XV in mouse cornea. Graefes Arch Clin Exp Ophthalmol 242:432-436.
111. Sandberg-Lall M, Hägg PO, Wahlstrom I, Pihlajaniemi T. 2000. Type XIII collagen is widely expressed in the adult and developing human eye and accentuated in the ciliary muscle, the optic nerve and neural retina. Exp Eye Res 70:401-410.
112. Sawada H, Konomi H, Hirosawa K. 1990. Characterization of the collagen in the hexagonal lattice of Descemet's membrane: its relation to type VIII collagen. J Cell Biol 110:219-227.
113. 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.
114. Segev F, Heon E, Cole WG, Wenstrup RJ, Young F, Slomovic AR, Rootman DS, Whitaker-Menezes D, Chervoneva I, Birk DE. 2006. Structural abnormalities of the cornea and lid resulting from collagen V mutations. Invest Ophthalmol Vis Sci 47:565-573.
115. Sevel D, Isaacs R. 1988. A re-evaluation of corneal development. Trans Am Ophthalmol Soc 86:178-207.
116. Siegler V, Quantock AJ. 2002. Two stage compaction of the secondary avian cornea during development. Exp Eye Res 74:427-431.
117. Smelser GK, Ozanics V. 1957. Distribution of radioactive sulfate in the developing eye. Am J Ophthalmol 44:102-110.
118. Song J, Lee YG, Houston J, Petroll WM, Chakravarti S, Cavanagh HD, Jester JV. 2003. Neonatal corneal stromal development in the normal and lumican-deficient mouse. Invest Ophthalmol Vis Sci 44:548-557.
119. Sundarraj N, Chao J, Gregory JD, Damle SP. 1986. Ocular distribution of keratan sulfates during pre- and postnatal development in rabbits. J Histochem Cytochem 34:971-976.
120. Svoboda KK, Nishimura I, Sugrue SP, Ninomiya Y, Olsen BR. 1988. Embryonic chicken cornea and cartilage synthesize type IX collagen molecules with different amino-terminal domains. Proc Natl Acad Sci U S A 85:7496-7500.
121. Takahashi I, Nakamura Y, Hamada Y, Nakazawa K. 1999. Immunohistochemical analysis of proteoglycan biosynthesis during early development of the chicken cornea. J Biochem 126:804-814.
122. Toole BP, Trelstad RL. 1971. Hyaluronate production and removal during corneal development in chick. Dev Biol 26:28-35.
123. Trelstad RL, Coulombre AJ. 1971. Morphogenesis of the collagenous stroma in the chick cornea. J Cell Biol 50:840-858.
124. Wenstrup RJ, Florer JB, Davidson JM, Phillips CL, Pfeiffer BJ, Menezes DW, Chervoneva I, Birk DE. 2006. Murine model of the Ehlers-Danlos syndrome. col5a1 haploinsufficiency disrupts collagen fibril assembly at multiple stages. J Biol Chem 281:12888-12895.
125. Wu J-J, Woods PE, Eyre DR. 1992. Identification of cross-linking sites in bovine cartilage type IX collagen reveals an antiparallel type II/type IX molecular relationship and type IX-to-type IX bonding. J Biol Chem 267:23007-23014.
126. 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.
127. Young RD, Tudor D, Hayes AJ, Kerr B, Hayashida Y, Nishida K, Meek KM, Caterson B, Quantock AJ. 2005. Atypical composition and ultrastructure of proteoglycans in the mouse corneal stroma. Invest Ophthalmol Vis Sci 46:1973-1978.
128. Young RD, Gealy EC, Liles M, Caterson B, Ralphs JR, Quantock AJ. 2007. Keratan sulfate glycosaminoglycan and the association with collagen fibrils in rudimentary lamellae in the developing avian cornea. Invest Ophthalmol Vis Sci 48:3083-3088.
129. Zhang Y, Conrad AH, Tasheva ES, An K, Corpuz LM, Kariya Y, Suzuki K, Conrad GW. 2005. Detection and quantification of sulfated disaccharides from keratan sulfate and chondroitin/dermatan sulfate during chick corneal development by ESI-MS/MS. Invest Ophthalmol Vis Sci 46:1604-1614.
130. Zieske JD. 2004. Corneal development associated with eyelid opening. Int J Dev Biol 48:903-911.