Targeted disruption of Col8a1 and Col8a2 genes in mice leads to anterior segment abnormalities in the eye

FASEB Journal

Volumn 19, Issue 10, 2005, Pages 1232-1244

  Hopfer, Ulrike ^a,b   Fukai, Naomi ^a   Hopfer, Helmut ^b   Wolf, Gunter ^b   Joyce, Nancy ^c   Li, En ^d,e   Olsen, Björn R ^a  

^a HARVARD SCHOOL OF DENTAL MEDICINE   (United States)

^b UNIVERSITY OF HAMBURG   (Germany)

^c SCHEPENS EYE RESEARCH INSTITUTE   (United States)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

^e NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

Corneal endothelial cells; Proliferation; Type VIII collagen

Indexed keywords

COLLAGEN TYPE 8; COLLAGEN TYPE 8A1; COLLAGEN TYPE 8A2; POLYPEPTIDE; PROTEIN SUBUNIT; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ANTERIOR EYE CHAMBER DISEASE; ARTICLE; BASEMENT MEMBRANE; CELL PROLIFERATION; CELL SIZE; CELL STRUCTURE; COL8A1 GENE; COL8A2 GENE; CONTROLLED STUDY; CORNEA ENDOTHELIUM; CORNEA STROMA; DESCEMET MEMBRANE; EXTRACELLULAR MATRIX; EYE DEVELOPMENT; EYE MALFORMATION; GENE DISRUPTION; GENE FUNCTION; GENE INACTIVATION; GENE TARGETING; HISTOPATHOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION;

ANIMALS; ANTERIOR EYE SEGMENT; AORTA; CELL PROLIFERATION; COLLAGEN TYPE VIII; CORNEA; ENDOTHELIUM, CORNEAL; EYE ABNORMALITIES; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; MICE; MICE, INBRED C57BL;

EID: 23444448102     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.04-3019com     Document Type: Article

References (63)

1. Benya, P. D. (1980) EC collagen: biosynthesis by corneal endothelial cells and separation from type IV without pepsin treatment or denaturation. Ren. Physiol. 3, 30-35
2. Muragaki, Y., Shiota, C., Inoue, M., Ooshima, A., Olsen, B. R., and Ninomiya, Y. (1992) alpha 1 (VIII)-collagen gene transcripts encode a short-chain collagen polypeptide and are expressed by various epithelial, endothelial and mesenchymal cells in newborn mouse tissues. Eur. J. Biochem. 207, 895-902
3. Kittelberger, R., Davis, P. F., Flynn, D. W., and Greenhill, N. S. (1990) Distribution of type VIII collagen in tissues: an immunohistochemical study. Connect. Tissue Res. 24, 303-318
4. Sage, H., Pritzl, P., and Bornstein, P. (1982) Endothelial cells secrete a novel collagen type in vitro independently of prolyl hydroxylation. Coll. Relat. Res. 2, 465-479
5. Liu, C. Y., Birk, D. E., Hassell, J. R., Kane, B., and Kao, W. W. (2003) Keratocan-deficient mice display alterations in corneal structure. J. Biol. Chem. 28, 28
6. Yamaguchi, N., Benya, P. D., van der Rest, M., and Ninomiya, Y. (1989) The cloning and sequencing of alpha 1 (VIII) collagen cDNAs demonstrate that type VIII collagen is a short chain collagen and contains triple-helical and carboxyl-terminal non-triple-helical domains similar to those of type X collagen. J. Biol. Chem. 264, 16022-16029
7. Muragaki, Y., Jacenko, O., Apte, S., Mattei, M. G., Ninomiya, Y., and Olsen, B. R. (1991) The alpha 2(VIII) collagen gene. A novel member of the short chain collagen family located on the human chromosome 1. J. Biol. Chem. 266, 7721-7727
8. Muragaki, Y., Mattei, M. G., Yamaguchi, N., Olsen, B. R., and Ninomiya, Y. (1991) The complete primary structure of the human alpha 1 (VIII) chain and assignment of its gene (COL8A1) to chromosome 3. Eur. J. Biochem. 197, 615-622
9. Yamaguchi, N., Mayne, R., and Ninomiya, Y. (1991) The alpha 1 (VIII) collagen gene is homologous to the alpha 1 (X) collagen gene and contains a large exon encoding the entire triple helical and carboxyl-terminal non-triple helical domains of the alpha 1 (VIII) polypeptide. J. Biol. Chem. 266, 4508-4513
10. Illidge, C., Kielty, C., and Shuttleworth, A. (1998) The alpha1(VIII) and alpha2(VIII) chains of type VIII collagen can form stable homotrimeric molecules. J. Biol. Chem. 273, 22091-22095
11. Greenhill, N. S., Ruger, B. M., Hasan, Q., and Davis, P. F. (2000) The alphal (VIII) and alpha2(VIII) collagen chains form two distinct homotrimeric proteins in vivo. Matrix Biol. 19, 19-28
12. Sawada, H., Konomi, H., and 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
13. Jakus, M. A. (1956) Studies on the cornea. II. The fine structure of Descemet's membrane. J. Biophys. Biochem. Cytol. 2, Suppl., 243-252
14. Levy, S. G., McCartney, A. C., Sawada, H., Dopping-Hepenstal, P. J., Alexander, R. A., and Moss, J. (1995) Descemet's membrane in the iridocorneal-endothelial syndrome: morphology and composition. Exp. Eye Res. 61, 323-333
15. Murphy, C., Alvarado, J., and Juster, R. (1984) Prenatal and postnatal growth of the human Descemet's membrane. Invest. Ophthalmol. Vis. Sci. 25, 1402-1415
16. Biswas, S., Munier, F. L., Yardley, J., Hart-Holden, N., Perveen, R., Cousin, P., Sutphin, J. E., Noble, B., Batterbury, M., Kielty, C., et al. (2001) Missense mutations in COL8A2, the gene encoding the alpha2 chain of type VIII collagen, cause two forms of corneal endothelial dystrophy. Hum. Mol. Genet. 10, 2415-2423
17. Grupcheva, C. N., Chew, G. S., Edwards, M., Craig, J. P., and McGhee, C. N. (2001 ) Imaging posterior polymorphous corneal dystrophy by in vivo confocal microscopy. Clin. Exp. Ophthalmol. 29, 256-259
18. Li, E., Bestor, T. H., and Jaenisch, R. (1992) Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69, 915-926
19. Laird, P. W., Zijderveld, A., Linders, K., Rudnicki, M. A., Jaenisch, R., and Berns, A. (1991) Simplified mammalian DNA isolation procedure. Nucleic Acids Res. 19, 4293
20. Chen, K. H., Harris, D. L., and Joyce, N. C. (1999) TGF-beta2 in aqueous humor suppresses S-phase entry in cultured corneal endothelial cells. Invest. Ophthalmol. Vis. Sci. 40, 2513-2519
21. Gospodarowicz, D., Mescher, A. L., and Birdwell, C. R. (1977) Stimulation of corneal endothelial cell proliferations in vitro by fibroblast and epidermal growth factors. Exp. Eye Res. 25, 75-89
22. Savion, N., Vlodavsky, I., and Gospodarowicz, D. (1981) Nuclear accumulation of epidermal growth factor in cultured bovine corneal endothelial and granulosa cells. J. Biol. Chem. 256, 1149-1154
23. Fabricant, R. N., Alpar, A. J., Centifanto, Y. M., and Kaufman, H. E. (1981) Epidermal growth factor receptors on corneal endothelium. Arch. Ophthalmol. 99, 305-308
24. Waring, G. O., III, Bourne, W. M., Edelhauser, H. F., and Kenyon, K. R. (1982) The corneal endothelium. Normal and pathologic structure and function. Ophthalmology 89, 531-590
25. Johnson, D. H., Bourne, W. M., and Campbell, R. J. (1982) The ultrastructure of Descemet's membrane. I. Changes with age in normal corneas. Arch. Ophthalmol. 100, 1942-1947
26. Rao, G. N., Lohman, L. E., and Aquavella, J. V. (1982) Cell size-shape relationships in corneal endothelium. Invest. Ophthalmol. Vis. Sci. 22, 271-274
27. Weitkamp, B., Cullen, P., Plenz, G., Robenek, H., and Rauterberg, J. (1999) Human macrophages synthesize type VIII collagen in vitro and in the atherosclerotic plaque. FASEB J. 13, 1445-1457
28. Henriquez, A. S., Kenyon, K. R., Dohlman, C. H., Boruchoff, S. A., Forstot, S. L., Meyer, R. F., and Hanninen, L. A. (1984) Morphologic characteristics of posterior polymorphous dystrophy. A study of nine corneas and review of the literature. Surv. Ophthalmol. 29, 139-147
29. Chen, K. H., Azar, D., and Joyce, N. C. (2001) Transplantation of adult human corneal endothelium ex vivo: a morphologic study. Cornea 20, 731-737
30. Pearce, W. G., Tripathi, R. C., and Morgan, G. (1969) Congenital endothelial corneal dystrophy. Clinical, pathological, and genetic study. Br. J. Ophthalmol. 53, 577-591
31. Forsberg, E., Hirsch, E., Frohlich, L., Meyer, M., Ekblom, P., Aszodi, A., Werner, S., and Fassler, R. (1996) Skin wounds and severed nerves heal normally in mice lacking tenascin-C. Proc. Natl. Acad. Sci. USA 93, 6594-6599
32. Aszodi, A., Pfeifer, A., Wendel, M., Hiripi, L., and Fassler, R. (1998) Mouse models for extracellular matrix diseases. J. Mol. Med. 76, 238-252
33. Jones, P. L., and Jones, F. S. (2000) Tenascin-C in development and disease: gene regulation and cell function. Matrix Biol. 19, 581-596
34. Paulus, W., Sage, E. H., Liszka, U., Iruela-Arispe, M. L., and Jellinger, K. (1991) Increased levels of type VIII collagen in human brain tumours compared to normal brain tissue and non-neoplastic cerebral disorders. Br. J. Cancer 63, 367-371
35. Paulus, W., Sage, E. H., Jellinger, K., and Roggendorf, W. (1992) Type VIII collagen in the normal and diseased human brain. Acta Histochem. Suppl. 42, 195-199
36. Iruela-Arispe, M. L., and Sage, E. H. (1991) Expression of type VIII collagen during morphogenesis of the chicken and mouse heart. Dev. Biol. 144, 107-118
37. Flugel-Koch, C., Ohlmann, A., Piatigorsky, J., and Tamm, E. R. (2002) Disruption of anterior segment development by TGF-betaI overexpression in the eyes of transgenic mice. Dev. Dyn. 225, 111-125
38. Hay, E. D. (1979) Development of the vertebrate cornea. Int. Rev. Cytol. 63, 263-322
39. Reneker, L. W., Silversides, D. W., Xu, L., and Overbeek, P. A. (2000) Formation of corneal endothelium is essential for anterior segment development - a transgenic mouse model of anterior segment dysgenesis. Development 127, 533-542
40. Saika, S., Liu, C. Y., Azhar, M., Sanford, L. P., Doetschman, T., Gendron, R. L., Kao, C. W., and Kao, W. W. (2001) TGFbeta2 in corneal morphogenesis during mouse embryonic development. Dev. Biol 240, 419-432.
41. Bard, J. B., Bansal, M. K., and Ross, A. S. (1988) The extracellular matrix of the developing cornea: diversity, deposition and function. Development 103, 195-205 (Suppl.)
42. Chakravarti, S., Magnuson, T., Lass, J. H., Jepsen, K. J., LaMantia, C., and Carroll, H. (1998) Lumican regulates collagen fibril assembly: skin fragility and corneal opacity in the absence of lumican. J. Cell Biol. 141, 1277-1286
43. Alitalo, K., Bornstein, P., Vaheri, A., and Sage, H. (1983) Biosynthesis of an unusual collagen type by human astrocytoma cells in vitro. J. Biol. Chem. 258, 2653-2661
44. Tan, S. T., Velickovic, M., Ruger, B. M., and Davis, P. F. (2000) Cellular and extracellular markers of hemangioma. Plast. Reconstr. Surg. 106, 529-538
45. Xu, R., Yao, Z. Y., Xin, L., Zhang, Q., Li, T. P., and Can, R. B. (2001) NC1 domain of human type VIII collagen (alpha 1) inhibits bovine aortic endothelial cell proliferation and causes cell apoptosis. Biochem. Biophys. Res. Commun. 289, 264-268
46. Iruela-Arispe, M. L., Hasselaar, P., and Sage, H. (1991) Differential expression of extracellular proteins is correlated with angiogenesis in vitro. Lab. Invest. 64, 174-186
47. MacBeath, J. R., Kielty, C. M., and Shuttleworth, C. A. (1996) Type VIII collagen is a product of vascular smooth-muscle cells in development and disease. Biochem. J. 319, 993-998
48. Bendeck, M. P., Regenass, S., Tom, W. D., Giachelli, C. M., Schwartz, S. M., Hart, C., and Reidy, M. A. (1996) Differential expression of alpha 1 type VIII collagen in injured platelet-derived growth factor-BB-stimulated rat carotid arteries. Cric. Res. 79, 524-531
49. Chakravarti, S. (2001) The cornea through the eyes of knockout mice. Exp. Eye Res. 73, 411-419
50. Hou, G., Mulholland, D., Gronska, M. A., and Bendeck, M. P. (2000) Type VIII collagen stimulates smooth muscle cell migration and matrix metalloproteinase synthesis after arterial injury. Am. J. Pathol. 156, 467-476
51. Tan, S. T., Wallis, R. A., He, Y., and Davis, P. F. (2004) Mast cells and hemangioma. Plast. Reconstr. Surg. 113, 999-1011
52. Hirano, S., Yonezawa, T., Hasegawa, H., Hattori, S., Greenhill, N. S., Davis, P. F., Sage, E. H., and Ninomiya, Y. (2004) Astrocytes express type VIII collagen during the repair process of brain cold injury. Biochem. Biophys. Res. Commun. 317, 437-443
53. Sibinga, N. E., Foster, L. C., Hsieh, C. M., Perrella, M. A., Lee, W. S., Endege, W. O., Sage, E. H., Lee, M. E., and Haber, E. (1997) Collagen VIII is expressed by vascular smooth muscle cells in response to vascular injury. Circ. Res. 80, 532-541
54. Semina, E. V., Mintz-Hittner, H. A., and Murray, J. C. (2000) Isolation and characterization of a novel human paired-like homeodomain-containing transcription factor gene, VSX1, expressed in ocular tissues. Genomics 63, 289-293
55. Heon, E., Greenberg, A., Kopp, K. K., Rootman, D., Vincent, A. L., Billingsley, G., Priston, M., Dorval, K. M., Chow, R. L., McInnes, R. R., et al. (2002) VSX1: a gene for posterior polymorphous dystrophy and keratoconus. Hum. Mol. Genet. 11, 1029-1036
56. Pellegata, N. S., Dieguez-Lucena, J. L., Joensuu, T., Lau, S., Montgomery, K. T., Krahe, R., Kivela, T., Kucherlapati, R., Forsius, H., and de la Chapelle, A. (2000) Mutations in KERA, encoding keratocan, cause cornea plana. Nat. Genet. 25, 91-95
57. Kenney, M. C., Labermeier, U., Hinds, D., and Waring, G. O., III (1984) Characterization of the Descemet's membrane/posterior collagenous layer isolated from Fuchs' endothelial dystrophy corneas. Exp. Eye Res. 39, 267-277
58. Levy, S. G., Moss, J., Noble, B. A., and McCartney, A. C. (1996) Early-onset posterior polymorphous dystrophy. Arch. Ophthalmol. 114, 1265-1268
59. Heon, E., Mathers, W. D., Alward, W. L., Weisenthal, R. W., Sunden, S. L., Fishbaugh, J. A., Taylor, C. M., Krachmer, J. H., Sheffield, V. C., and Stone, E. M. (1995) Linkage of posterior polymorphous corneal dystrophy to 20q11. Hum. Mol. Genet. 4, 485-488
60. Gottsch, J. D., Bowers, A. L., Margulies, E. H., Seitzman, G. D., Kim, S. W., Saha, S., Jun, A. S., Stark, W. J., and Liu, S. H. (2003) Serial analysis of gene expression in the corneal endothelium of Fuchs' dystrophy. Invest. Ophthalmol. Vis. Sci. 44, 594-599
61. Li, Q. J., Ashraf, M. F., Shen, D. F., Green, W. R., Stark, W. J., Chan, C. C., and O'Brien, T. P. (2001) The role of apoptosis in the pathogenesis of Fuchs endothelial dystrophy of the cornea. Arch. Ophthalmol. 119, 1597-1604
62. Bendeck, M. P., Regenass, S., Tom, W. D., Giachelli, C. M., Schwartz, S. M., Hart, C., and Reidy, M. A. (1996) Differential expression of alpha 1 type VIII collagen in injured platelet-derived growth factor-BB-stimulated rat carotid arteries. Circ. Res. 79, 524-531
63. Sinha, S., Kielty, C. M., Heagerty, A. M., Canfield, A. E., and Shuttleworth, C. A. (2001) Up-regulation of collagen VIII following porcine coronary artery angioplasty is related to smooth muscle cell migration not angiogenesis. Int. J. Exp. Pathol. 82, 295-302