Lumican regulates collagen fibril assembly: Skin fragility and corneal opacity in the absence of lumican

Journal of Cell Biology

Volumn 141, Issue 5, 1998, Pages 1277-1286

  Chakravarti, Shukti ^a,c   Magnuson, Terry ^b   Lass, Jonathan H ^b   Jepsen, Karl J ^b   LaMantia, Christian ^b   Carroll, Heidi ^a  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

^b UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN FIBRIL; KERATAN SULFATE; LEUCINE; LUMICAN; PROTEOGLYCAN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONNECTIVE TISSUE DISEASE; CONTROLLED STUDY; CORNEA OPACITY; EHLERS DANLOS SYNDROME; MALE; MOUSE; MOUSE MUTANT; NONHUMAN; PRIORITY JOURNAL; SKIN DEFECT;

ANIMALS; COLLAGEN; CORNEAL OPACITY; GENE EXPRESSION; GENE TARGETING; IN SITU HYBRIDIZATION; KERATAN SULFATE; MICE; PROTEOCHONDROITIN SULFATES; SKIN DISEASES, METABOLIC; TENSILE STRENGTH;

ANIMALIA;

EID: 0032101311     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.141.5.1277     Document Type: Article

References (47)

1. Birk, D.E., J.M. Fitch, J.P. Babiarz, K.J. Doane, and T.E. Linsenmayer. 1990. Collagen fibrillogenesis in vitro: interactions of types I and V collagen regulates fibril diameter. J. Cell Sci. 95:649-657.
2. Blochberger, T.C., J.-P. Vergnes, J. Hempel, and J.R. Hassell. 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.
3. Burch, G.H., Y. Gong, W. Liu, R.W. Dettman, C.J. Curry, L. Smith, W.L. Miller, and J. Bristow. 1997. Tenascin-X deficiency is associated with Ehlers-Danlos syndrome. Nat. Genet. 17:104-108.
4. Byers, P.H., K.A. Holbrook, J.G. Hall, P. Bornstein, and J.W. Chandler. 1978. A new variety of spondyoepiphyseal dysplasia characterized by punctate corneal dystrophy and abnormal collagen fibrils. Hum. Genet. 40:157-169.
5. Casey, T.A., and K.W. Sharif. 1991. A Color Atlas of Corneal Dystrophies and Degenerations. Wolfe Publishing Limited, London. 21-51.
6. Chakravarti, S., and T. Magnuson. 1995. Localization of mouse lumican (keratan sulfate proteoglycan) to distal chromosome 10. Mamm. Genome. 6:367-368.
7. Chakravarti, S., R. Stalling, D. Fite, N. SundarRaj, and J.R. Hassell. 1995. Primary structure of human lumican (keratan sulfate proteoglycan) and localization of the gene (LUM) to chromosome 12q21.3-q22. Genomics. 27:481-488.
8. Cintron, C., J.D. Gregory, S.P. Damle, and C.L. Kublin. 1990. Biochemical analyses of proteoglycans in rabbit corneal scars. Investig. Ophthalmol. Vis. Sci. 31:1975-1981.
9. Cornuet, P.K., T.C. Blochberger, and J.R. Hassell. 1994. Molecular polymorphisms of lumican during corneal development. Investig. Ophthalmol. Vis. Sci. 35:870-876.
10. Corpuz, L.M., J.L. Funderburgh, M.L. Funderburgh, G.S. Bottomley, S. Prakash, and G.W. Conrad. 1996. Molecular cloning and tissue distribution of keratocan. J. Biol. Chem. 271:9759-9763.
11. Daly, C.H. 1982. Biomechanical properties of dermis. J. Invest. Dermatol. 79:17S-20S.
12. Danielson, K.G., H. Baribault, D.F. Holmes, H. Graham, K.E. Kadler, and R.V. Iozzo. 1997. Targeted disruption of decorin leads to abnormal collagen fibril morphology and skin fragility. J. Cell Biol. 136:729-743.
13. Dunlevy, J.R., S. Chakravarti, P. Gyalzen, J.-P. Vergnes, and J.R. Hassell, 1998. Cloning and chromosomal localization of mouse keratocan, a corneal keratan sulfate proteoglycan. Mamm. Genome. 9:316-319.
14. Fisher, L.W., J.T. Stubbs, and M.F. Young. 1995. Antisera and cDNA robes to human and certain animal bone matrix noncollagenous proteins. Acta. Orthop. Scand. Suppl. 266:61-65.
15. Green, E.L. 1975. Biology of the Laboratory Mouse. E.L. Green, editor. Dover Publications, New York. 94-95.
16. Hedbom, E., and D. Heinegard. 1993. Binding of fibromodulin and decorin to separate sites on fibrillar collagens. J. Biol. Chem. 268:27307-27312.
17. Hogan, B., R. Bedington, F. Constantini, and E. Lacy. 1994. Manipulating the Mouse Embryo. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY. 219-323.
18. Iozzo, R.V., and A.D. Murdoch. 1996. Proteoglycans of the extracellular environment: clues from the gene and protein side offer novel perspectives in molecular diversity and function. FASEB (Fed. Am. Soc. Exp. Biol.) J. 10:598-614.
19. Irvine, A.D., L.D. Corden, O. Swensson, B. Swensson, J.E. Moore, D.G. Frazer, F.J.D. Smith, R.G.K. Christophers, R. Rochels, J. Uitto, and W.H.I. McLean. 1997. Mutations in cornea-specific keratin K3 or K12 genes cause Meesmann's corneal dystrophy. Nat. Genet. 16:184-187.
20. Klintworth, G.K., R. Meyer, and R. Dennis. 1986. Macular corneal dystrophy. Lack of keratan sulfate in serum and cornea. Ophthalmic. Paediatr. Genet. 7:139-143.
21. Kobe, B., and J. Deisenhofer. 1993. Crystal structure of porcine ribonuclease inhibitor, a protein with leucine-rich repeats. Nature. 366:751-756.
22. Kresse, H., C. Liszio, E. Schonherr, and L.W. Fisher. 1997. Critical role of glutamate in a central leucine-rich repeat of decorin for interaction with type I collagen. J. Biol. Chem. 272:18404-18410.
23. Kuivaniemi, H., G. Tromp, and D. Prockop. 1991. Mutations in collagen genes: causes of rare and some common diseases in humans. FASEB (Fed. Am. Soc. Exp. Biol.) J. 5:2052-2060.
24. Kyriakides, T.R., Y.-H. Zhu, L.T. Smith, S.D. Bain, Z. Yang, M.T. Lin, K.G. Danielson, R.V. Iozzo, M. LaMarca, C.F. McKinney, and E.I. Ginns. 1998. Mice that lack thrombospondin 2 display connective tissue abnormalities that are associated with disordered collagen fibrillogenesis. an increased vascular density, and a bleeding diathesis. J. Cell Biol. 140: 419-430.
25. Maurice, D.M. 1957. The structure and transparency of the cornea. J. Physiol. 136:263.
26. McKusick, V.A. 1992. Mendelian Inheritance in Man. Vol. 1 and 2. The Johns Hopkins University Press, Baltimore.
27. Midura, R.J., V. Hascall, D.K. MacCallum, R.F. Meyer, E.J. Thonar, J.R. Hassell, C.F. Smith, and G.K. Klintworth. 1990. Proteoglycan biosynthesis by human corneas from patients with types 1 and 2 macular corneal dystrophy. J. Biol. Chem. 265:15947-15955.
28. Mohanaradhakrishnan, V., P.L. Muthiah, and A. Hadhanyi. 1975. A few factors contributing to the mechanical strength of collagen fibres. Arzneimittelforschung. 25:726-735.
29. Munier, F.L., E. Korvatska, A. Djemai, D. Le Paslier, L. Zografos, G. Pescia, and D.F. Schorderet. 1997. Kerato-epithelin mutations in four 5q31-linked corneal dystrophies. Nat. Genet. 15:247-251.
30. Parkinson, J., A. Brass, G. Canova, and Y. Brechet. 1997. The mechanical properties of simulated collagen fibrils. J. Biomech. 30:549-554.
31. Pope, F.M., and N.P. Burrows. 1997. Ehlers-Danlos syndrome has varied molecular mechanisms. J. Med. Genet. 34:400-410.
32. Rada, J.A., P.K. Cornuet, and J.H. Hassell. 1993. Regulation of corneal collagen fibrillogenesis in vitro by corneal keratan sulfate proteoglycan (lumican) and decorin core proteins. Exp. Eye Res. 56:635-648.
33. Rada, J.A., M.E. Fini, and J.R. Hassell. 1996. Regionalized growth patterns of young chicken corneas. Investigative Ophthalmol. Vis. Sci. 37:2060-2067.
34. Sassoon, D., and N. Rosenthal. 1993. Detection of messenger RNA by in situ hybridization. In Guide to Techniques in Mouse Development. P.M. Wasserman, and M.L. DePamphilis, editors. Academic Press, New York. 384-404.
35. Schonherr, E., H. Hausser, L. Beavan, and H. Kresse. 1995. Decorin-type I collagen interaction. J. Biol. Chem. 270:8877-8883.
36. Schonherr, E., P. Witsch-Prehm, B. Harach, H. Robenek, J. Raurerberg, and H. Kresse. 1995. Interactions of biglycan with Type I collagen. J. Biol. Chem. 270:2776-2783.
37. Schrecengost, P.K., T.C. Blochberger, and J.R. Hassell. 1992. Identification of chick corneal keratan sulfate proteoglycan precursor protein in whole corneas and in cultured corneal fibroblasts. Arch. Biochem. Biophys. 292: 54-61.
38. Scott, J.E. 1988. Proteoglycan-fibrillar collagen interactions. Review article. Biochem. J. 252:313-323.
39. Scott, J.E. 1996. Proteodermatan and proteokeratan sulfate (decorin, lumican/fibromodulin)proteins are horseshoe shaped. Implications for their interactions with collagen. Biochemistry. 35:8795-8799.
40. Scott, J.E., and C.R. Orford. 1981. Dermatan sulfate rich proteoglycan associates with rat tail tendon collagen at the d band in the gap region. Biochem. J. 197:213-216.
41. Steinmann, B., P.M. Royce, and A. Superti-Furga. 1993. The Ehlers-Danlos Syndrome. In Connective Tissue and Its Heritable Disorders: Molecular, Genetic, and Medical Aspects. P.M. Royce, and B. Steinmann, editors. Wiley-Liss Inc., New York. 351-408.
42. Tahvanainen, E., A.S. Villnueva, H. Forsius, P. Salo, and A. de la Chapelle. 1996. Dominantly and recessively inherited Cornea Plana Congenita map to the same small region of chromosome 12. Genome Res. 6:249-253.
43. Toriello, H.V., T.W. Glover, K. Takahara, P.H. Byers, D.E. Miller, J.V. Higgins, and D.S. Greenspan. 1996. A translocation interrupts the COL5A1 gene in a patient with Ehlers-Danlos syndrome and hypomelanosis of Ito. Nat. Genet. 13:361-365.
44. Vance, J.M., F. Jonasson, F. Lennon, J. Sarrica, K.F. Damji, J. Stauffer, M.A. Pericak-Vance, and G.K. Klintworth. 1996. Linkage of a gene for macular corneal dystrophy to chromosome 16. Am. J. Hum. Genet. 58:757-762.
45. Vogel, K.G., and J.A. Trotter. 1987. The effect of proteoglycans on the morphology of collagen fibrils formed in vitro. Collagen Relat. Res. 7:105-114.
46. Vogel, K.G., M. Paulsson, and D. Heinegard. 1984. Specific inhibition of type I and type II collagen fibrillogenesis by the small proteoglycans of tendon. Biochem. J. 223:587-597.
47. Weber, I.T., R.W. Harrison, and R.V. Iozzo. 1996. Model structure of decorin and implications for collagen fibrillogenesis. J. Biol. Chem. 271: 31767-31770.