Structural Interactions between Collagen and Proteoglycans Are Elucidated by Three-Dimensional Electron Tomography of Bovine Cornea

Structure

Volumn 18, Issue 2, 2010, Pages 239-245

  Lewis, Philip N ^a   Pinali, Christian ^a   Young, Robert D ^a   Meek, Keith M ^a   Quantock, Andrew J ^a   Knupp, Carlo ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

CELLBIO; PROTEINS

Indexed keywords

COLLAGEN; GLYCOSAMINOGLYCAN; PROTEOGLYCAN;

ANIMAL TISSUE; ARTICLE; CHEMICAL PARAMETERS; CORNEA; COW; ELECTRON TOMOGRAPHY; IMAGE RECONSTRUCTION; NONHUMAN; OSMOTIC PRESSURE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; THERMAL MOTION; THREE DIMENSIONAL IMAGING;

ANIMALS; CATTLE; CHONDROITINASES AND CHONDROITIN LYASES; COLLAGEN; CORNEA; ELECTRON MICROSCOPE TOMOGRAPHY; GLYCOSAMINOGLYCANS; GLYCOSIDE HYDROLASES; MODELS, MOLECULAR; PROTEOGLYCANS;

BOVINAE;

EID: 75849129553     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2009.11.013     Document Type: Article

References (41)

1. Akama T.O., Nishida K., Nakayama J., Watanabe H., Ozaki K., Nakamura T., Dota A., Kawasaki S., Inoue Y., Maeda N., et al. Macular corneal dystrophy type I and type II are caused by distinct mutations in a new sulphotransferase gene. Nat. Genet. 26 (2000) 237-241
2. Akama T.O., Nakayama J., Nishida K., Hiraoka N., Suzuki M., McAuliffe J., Hindsgaul O., Fukuda M., and Fukuda M.N. Human corneal GlcNac 6-O-sulfotransferase and mouse intestinal GlcNac 6-O-sulfotransferase both produce keratan sulfate. J. Biol. Chem. 276 (2001) 16271-16278
3. Anseth A. Studies on corneal polysaccharides. III. Topographic and comparative biochemistry. Exp. Eye Res. 1 (1961) 106-115
4. Arnott S., Mitra A.K., and Raghunathan S. Hyaluronic acid double helix. J. Mol. Biol. 169 (1983) 861-872
5. Axelsson I., and Heinegard D. Characterization of the keratan sulphate proteoglycans from bovine corneal stroma. Biochem. J. 169 (1978) 517-530
6. Axelsson I., and Heinegard D. Characterization of chondroitin sulfate-rich proteoglycans from bovine corneal stroma. Exp. Eye Res. 31 (1980) 57-66
7. Benedek G. Theory of transparency of the eye. Appl. Opt. 10 (1971) 459-473
8. Bettelheim F.A., and Plessy B. The hydration of proteoglycans of bovine cornea. Biochim. Biophys. Acta 381 (1975) 203-214
9. Birk D.E., Fitch J.F., Babiarz J.P., Doane K.J., and Linsenmayer T.F. Collagen fibrillogenesis in vitro: interaction of types I and V collagen regulates fibril diameter. J. Cell Sci. 95 (1990) 649-657
10. Birk D.E., Fitch J.M., Babiarz J.P., and Linsenmayer T.F. Collagen type I and type V are present in the same fibril in the avian corneal stroma. J. Cell Biol. 106 (1988) 999-1008
11. Borcherding M.S., Blacik L.J., Sittig R.A., Bizzell J.W., Breen M., and Weinstein H.G. Proteoglycans and collagen fibre organization in human corneoscleral tissue. Exp. Eye Res. 21 (1975) 59-70
12. Carlson E.C., Liu C.-Y., Chikama T.-I., Hayashi Y., Kao C.W.-C., Birk D.E., Funderburgh J.L., Jester J.V., and Kao W.W. Keratocan, a cornea-specific keratan sulphate proteoglycan, is regulated by lumican. J. Biol. Chem. 280 (2005) 25541-25547
13. Chakravarti S., Petroll W.M., Hassell J.R., Jester J.V., Lass J.H., Paul J., and Birk D.E. Corneal opacity in lumican-null mice: Defects in collagen fibril structure and packing in the posterior stroma. Invest. Ophthalmol. Vis. Sci. 41 (2000) 3365-3373
14. Chakravarti S., Zhang G., Chervoneva I., Roberts L., and Birk D.E. Collagen fibril assembly during postnatal development and dysfunctional regulation in the lumican-deficient murine cornea. Dev. Dyn. 235 (2006) 2493-2506
15. Cooper L.J., Bentley A.J., Nieduszynski I.A., Talabani S., Thomson A., Utani A., Shinkai H., Fullwood N.J., and Brown G.M. The role of dermatopontin in the stromal organization of the cornea. Invest. Ophthalmol. Vis. Sci. 47 (2006) 3303-3310
16. Elliott G.F., and Hodson S.A. Cornea, and the swelling of polyelectrolyte gels of biological interest. Rep. Prog. Phys. 61 (1998) 1325-1365
17. Farrell R.A., and Hart R.W. On the theory of the spatial organization of macromolecules in connective tissue. Bull. Math. Biophys. 31 (1969) 727-760
18. Farrell R.A., McCally R.L., and Tatham P.E.R. Wave-length dependencies of light scattering in normal and cold swollen rabbit corneas and their structural implications. J. Physiol. 233 (1973) 589-612
19. Gregory J.D., Coster L., and Damle S.P. Proteoglycans of rabbit corneal stroma. Isolation and partial characterization. J. Biol. Chem. 257 (1982) 6965-6970
20. Hart R.W., and Farrell R.A. Light scattering in the cornea. J. Opt. Soc. Am. 59 (1969) 766-774
21. Hayashida Y., Akama T.O., Beecher N., Lewis P., Young R.D., Meek K.M., Kerr B., Hughes C.E., Caterson B., Tanigami A., et al. Matrix morphogenesis in cornea is mediated by the modification of keratan sulfate by GlcNAc 6-O-sulfotransferase. Proc. Natl. Acad. Sci. USA 103 (2006) 13333-13338
22. Holzapfel G. Collagen in arterial walls: biomechanical aspects. In: Fratzl P. (Ed). Collagen: Structure and Mechanics (2008), Springer Science and Business Media 285-324
23. Humzah M.D., and Soames R.W. Human intervertebral disc: structure and function. Anat. Rec. 220 (1998) 337-356
24. Knupp C., and Squire J. Interpretation of the X-ray patterns from the three-dimensional collagen network in the dogfish egg case wall. Proc. R. Soc. Lond. B Biol. Sci. 265 (1998) 2177-2186
25. Komai Y., and Ushiki T. The three-dimensional organization of collagen fibrils in the human cornea and sclera. Invest. Ophthalmol. Vis. Sci. 32 (1991) 2244-2258
26. Kremer J.R., Mastronarde D.N., and McIntosh J.R. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116 (1996) 71-76
27. Kühn K., and von der Mark K. The influence of proteoglycans on the macromolecular structure of collagen. Suppl. Thromb. Haemost. 63 (1978) 123-126
28. Maurice D.M. The structure and transparency of the cornea. J. Physiol. 136 (1957) 263-286
29. Maurice D.M. Clinical physiology of the cornea. Int. Ophthalmol. Clin. 2 (1962) 561-572
30. Meek K.M., and Boote C. The organization of collagen in the corneal stroma. Exp. Eye Res. 78 (2004) 503-512
31. Meek K.M., and Leonard D.W. Ultrastructure of the corneal stroma: a comparative study. Biophys. J. 64 (1993) 273-280
32. Meek K.M., Elliott G.F., and Nave C. A synchrotron X-ray diffraction study of bovine cornea stained with cupromeronic blue. Coll. Relat. Res. 6 (1986) 203-218
33. Muller L.J., Pels E., Schurmans L.R., and Vrensen G.F. A new three-dimensional model of the organization of proteoglycans and collagen fibrils in the human corneal stroma. Exp. Eye Res. 78 (2004) 493-501
34. Quantock A.J., Meek K.M., Ridgway A.E.A., Bron A.J., and Thonar E.J.-M.A. Macular corneal dystrophy: Reduction in both corneal thickness and collagen interfibrillar spacing. Curr. Eye Res. 9 (1990) 393-398
35. Ress D.B., Harlow M.L., Marshall R.M., and McMahan U.J. Methods for generating high-resolution structural models from electron microscope tomography data. Structure 12 (2004) 1763-1774
36. Scott J.E. Morphometry of cupromeronic blue-stained proteoglycan molecules in animal corneas, versus that of purified proteoglycans stained in vitro, implies that tertiary structures contribute to corneal ultrastructure. J. Anat. 180 (1992) 155-164
37. Scott J.E. Extracellular matrix, supramolecular organisation and shape. J. Anat. 187 (1995) 259-269
38. Scott J.E. Elasticity in extracellular matrix 'shape modules' of tendon, cartilage, etc. A sliding proteoglycan-filament model. J. Physiol. 553 (2003) 335-343
39. Scott J.E., and Haigh M. 'Small'-proteoglycan:collagen interactions: keratan sulphate proteoglycan associates with rabbit corneal collagen fibrils at the 'a' and 'c' bands. Biosci. Rep. 5 (1985) 765-774
40. Scott J.E., and Bosworth T.R. A comparative biochemical and ultrastructural study of proteoglycan-collagen interactions in corneal stroma. Functional and metabolic implications. Biochem. J. 270 (1990) 491-497
41. Young R.D., Tudor D., Hayes A.J., Kerr B., Hayashida Y., Nishida K., Meek K.M., Caterson B., and Quantock A.J. Atypical composition and ultrastructure of proteoglycans in the mouse corneal stroma. Invest. Ophthalmol. Vis. Sci. 46 (2005) 1973-1978