Resistance of corneal RFUVA-cross-linked collagens and small leucine-rich proteoglycans to degradation by matrix metalloproteinases

Investigative Ophthalmology and Visual Science

Volumn 54, Issue 2, 2013, Pages 1014-1025

  Zhang, Yuntao ^a   Mao, Xiuli ^a   Schwend, Tyler ^a   Littlechild, Stacy ^a   Conrad, Gary W ^a  

^a KANSAS STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIGLYCAN; COLLAGEN; COLLAGEN TYPE 1; COLLAGEN TYPE 4; COLLAGENASE 3; DECORIN; GELATINASE A; GELATINASE B; HISTIDINE; HYDROXYLYSINE; INTERSTITIAL COLLAGENASE; KERATOCAN; LYSINE; MATRIX METALLOPROTEINASE; METHIONINE; MIMECAN; PROTEOGLYCAN; RIBOFLAVIN; TYROSINE;

AMINO ACID ANALYSIS; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORNEA SURGERY; CORNEAL CROSS LINKING; COW; KERATOCONUS; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN CROSS LINKING; PROTEIN DEGRADATION; ULTRAVIOLET A RADIATION; WESTERN BLOTTING;

ANIMALS; CATTLE; COLLAGEN TYPE I; CORNEA; DISEASE MODELS, ANIMAL; EXTRACELLULAR MATRIX; EXTRACELLULAR MATRIX PROTEINS; KERATOCONUS; MATRIX METALLOPROTEINASES; PROTEOGLYCANS;

EID: 84874965736     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.12-11277     Document Type: Article

References (68)

1. Espandar L, Meyer J. Keratoconus: overview and update on treatment. Middle East Afr J Ophthalmol. 2010;17:15-20.
2. Romero-Jiménez M, Santodomingo-Rubido J, Wolffsohn JS. Keratoconus: a review. Cont Lens Anterior Eye. 2010;33:157-166.
3. Edrington TB, Zadnik K, Barr JT. Keratoconus. Optom Clin. 1995;4:65-73.
4. 2011 eye banking statistical report. Eye Bank Association of America Web site. http://www.restoresight.org/about-us/ ebaa-materials-publications. Accessed January 2013.
5. Beuerman RW, Pedroza L. Ultrastructure of the human cornea. Microsc Res Tech. 1996;33:320-335.
6. Worthington CR. The structure of cornea. Q Rev Biophys. 1984;17:423-451.
7. Robert L, Legeais JM, Robert AM, Renard G. Corneal collagens. Pathol Biol. 2001;49:353-363.
8. Hay ED. Matrix-cytoskeletal interactions in the developing eye. J Cell Biochem. 1985;27:143-156.
9. Hassell JR, Birk DE. The molecular basis of corneal transparency. Exp Eye Res. 2010;91:326-335.
10. Newsome DA, Gross J, Hassell JR. Human corneal stroma contains three distinct collagens. Invest Ophthalmol Vis Sci. 1982;22:376-381.
11. Scott JE. Proteoglycan: collagen interactions and corneal ultrastructure. Biochem Soc Trans. 1991;19:877-881.
12. Funderburgh JL, Funderburgh ML, Brown SJ, et al. Sequence and structural implications of a bovine corneal keratan sulfate proteoglycan core protein. Protein 37B represents bovine lumican and proteins 37A and 25 are unique. J Biol Chem. 1993;268:11874-11880.
13. Funderburgh JL, Corpuz LM, Roth MR, Funderburgh ML, Tasheva ES, Conrad GW. Mimecan, the 25-kDa corneal keratan sulfate proteoglycan, is a product of the gene producing osteoglycin. J Biol Chem. 1997;272:28089-28095.
14. Corpuz LM, Funderburgh JL, Funderburgh ML, et al. Molecular cloning and tissue distribution of keratocan. Bovine corneal keratan sulfate proteoglycan 37A. J Biol Chem. 1996;271: 9759-9763.
15. Funderburgh JL, Funderburgh ML, Mann MM, Conrad GW. Physical and biological properties of keratan sulphate proteoglycan. Biochem Soc Trans. 1991;19:871-876.
16. Kao WW, Liu CY. Roles of lumican and keratocan on corneal transparency. Glycoconj J. 2002;19:275-285.
17. Carlson EC, Liu CY, Chikama T, et al. Keratocan, a corneaspecific keratan sulfate proteoglycan, is regulated by lumican. J Biol Chem. 2005;280:25541-25547.
18. Li W, Vergnes JP, Cornuet PK, Hassell JR. cDNA clone to chick corneal chondroitin/dermatan sulfate proteoglycan reveals identity to decorin. Arch Biochem Biophys. 1992;296:190-197.
19. Bianco P, Fisher LW, Young MF, Termine JD, Robey PG. Expression and localization of the two small proteoglycans biglycan and decorin in developing human skeletal and nonskeletal tissues. J Histochem Cytochem. 1990;38:1549-1563.
20. Fisher LW, Termine JD, Young MF. Deduced protein sequence of bone small proteoglycan I (biglycan) shows homology with proteoglycan II (decorin) and several nonconnective tissue proteins in a variety of species. J Biol Chem. 1989;264:4571-4576.
21. Blaschke UK, Hedbom E, Bruckner P. Distinct isoforms of chicken decorin contain either one or two dermatan sulfate chains. J Biol Chem. 1996;271:30347-30353.
22. Corpuz LM, Dunlevy JR, Hassell JR, Conrad AH, Conrad GW. Molecular cloning and relative tissue expression of decorin and lumican in embryonic quail cornea. Matrix Biol. 2000;19: 699-704.
23. Dunlevy JR, Neame PJ, Vergnes JP, Hassell JR. Identification of the N-linked oligosaccharide sites in chick corneal lumican and keratocan that receive keratan sulfate. J Biol Chem. 1998; 273:9615-9621.
24. Corpuz LM, Dunlevy JR, Hassell JR, Conrad AH, Conrad GW. Molecular cloning and relative tissue expression of keratocan and mimecan in embryonic quail cornea. Matrix Biol. 2000; 273:693-698.
25. Chen R, Jiang X, Sun D, et al. Glycoproteomics analysis of human liver tissue by combination of multiple enzyme digestion and hydrazide chemistry. J Proteome Res. 2009;8: 651-661.
26. Edrington TB, Zadnik K, Barr JT. Keratoconus. Optom Clin. 1995;4:65-73.
27. Meek KM, Tuft SJ, Huang Y, et al. Changes in collagen orientation and distribution in keratoconus corneas. Invest Ophthalmol Vis Sci. 2005;46:1948-1956.
28. Collier SA. Is the corneal degradation in keratoconus caused by matrix-metalloproteinases? Clin Experiment Ophthalmol. 2001;29:340-344.
29. Balasubramanian SA, Pye DC, Willcox MD. Are proteinases the reason for keratoconus? Curr Eye Res. 2010;35:185-191.
30. Mackiewicz Z, M̈äatẗa M, Stenman M, Konttinen L, Tervo T, Konttinen YT. Collagenolytic proteinases in keratoconus. Cornea. 2006;25:603-610.
31. Sepp̈al̈a HP, M̈äatẗa M, Rautia M, et al. EMMPRIN and MMP-1 in keratoconus. Cornea. 2006;25:325-330.
32. Birkedal-Hansen H, Moore WG, Bodden MK, et al. Matrix metalloproteinases: a review. Crit Rev Oral Biol Med. 1993;4: 197-250.
33. Verma RP, Hansch C. Matrix metalloproteinases (MMPs): chemical-biological functions and (Q)SARs. Bioorg Med Chem. 2007;15:2223-2268.
34. Leonard A, Brun P, Abatangelo G, Plebani M, Secchi AG. Tear levels and activity of matrix metalloproteinase (MMP)-1 and MMP-9 in vernal keratoconjunctivitis. Invest Ophthalmol Vis Sci. 2003;44:3052-3058.
35. Kenney MC, Chwa M, Alba A, Saghizadeh M, Huang ZS, Brown DJ. Localization of TIMP-1, TIMP-2, TIMP-3, gelatinase A and gelatinase B in pathological human corneas. Curr Eye Res. 1998;17:238-246.
36. Kenney MC, Chwa M, Opbroek AJ, Brown DJ. Increased gelatinolytic activity in keratoconus keratocyte cultures. A correlation to an altered matrix metalloproteinase-2/tissue inhibitor of metalloproteinase ratio. Cornea. 1994;13:114-124.
37. Brown D, Chwa MM, Opbroek A, Kenney MC. Keratoconus corneas: increased gelatinolytic activity appears after modification of inhibitors. Curr Eye Res. 1993;12:571-581.
38. Kao WW, Vergnes JP, Ebert J, Sundar-Raj CV, Brown SI. Increased gelatinase and collagenase activities in keratoconus. Biochem Biophys Res Commun. 1982;107:929-936.
39. Critchfield JW, Calandra AJ, Nesburn AB, Kenny MC. Keratoconus. I. Biochemical Studies. Exp Eye Res. 1988;46:953-963.
40. Wollensak G, Sporl E, Seiler T. Treatment of keratoconus by collagen cross linking. Ophthalmologe. 2003;100:44-49.
41. McCall AS, Kraft S, Edelhauser HF, et al. Mechanisms of corneal tissue cross-linking in response to treatment with topical riboflavin and long-wavelength ultraviolet radiation (UVA). Invest Ophthalmol Vis Sci. 2010;51:129-138.
42. Zhang Y, Conrad AH, Conrad GW. Effects of ultraviolet-A and riboflavin on the interaction of collagen and proteoglycans during corneal cross-linking. J Biol Chem. 2011;286:13011-13022.
43. Conrad GW, Ager-Johnson P, Woo ML. Antibodies against the predominant glycosaminoglycan of the mammalian cornea, keratan sulfate-I. J Biol Chem. 1982;257:464-471.
44. Wollensak G, Redl B. Gel electrophoretic analysis of corneal collagen after Photodynamic cross-linking treatment. Cornea. 2008;27:353-356.
45. Geng Y, McQuillan D, Roughley PJ. SLRP interaction can protect collagen fibrils from cleavage by collagenases. Matrix Biol. 2006;25:484-491.
46. Daxer A, Misof K, Grabner B, Ettl A, Fratzl P. Collagen fibrils in the human corneal stroma: structure and aging. Invest Ophthalmol Vis Sci. 1998;39:644-648.
47. Reiser KM, Amigable MA, Last JA. Nonenzymatic glycation of type I collagen. The effects of aging on preferential glycation sites. J Biol Chem. 1992;267:24207-24216.
48. Snibson GR. Collagen cross-linking: a new treatment paradigm in corneal disease-a review. Clin Experiment Ophthalmol. 2010;38:141-153.
49. Remucal CK, McNeill K. Photosensitized amino acid degradation in the presence of riboflavin and its derivatives. Environ Sci Technol. 2011;45:5230-5237.
50. Brummer G, Littlechild S, McCall S, Zhang Y, Conrad GW. The role of nonenzymatic glycation and carbonyls in collagen cross-linking for the treatment of keratoconus. Invest Ophthalmol Vis Sci. 2011;52:6363-6369.
51. Spikes JD, Shen HR, Kopeckova P, Kopecek J. Photodynamic crosslinking of proteins, III: kinetics of the FMN-and rose Bengal-sensitized photooxidation and intermolecular crosslinking of model tyrosine-containing N-(2 hydroxypropyl)methacrylamide copolymers. Photochem Photobiol. 1999;70: 130-137.
52. de La Rochette A, Birlouez-Aragon I, Silva E, Morliére P. Advanced glycation end products as UVA photosensitizers of tryptophan and ascorbic acid: consequences for the lens. Biochim Biophys Acta. 2003;1621:235-241.
53. Dalsgaard TK, Otzen D, Nielsen JH, Larsen LB. Changes in structures of milk proteins upon photo-oxidation. J Agric Food Chem. 2007;55:10968-10976.
54. Slifkin MA. Interaction of amino-acids with riboflavin. Nature. 1963;197:275-276.
55. Huang R, Choe E, Min DB. Kinetics for singlet oxygen formation by riboflavin photosensitization and the reaction between riboflavin and singlet oxygen. J Food Sci. 2004;69: C726-C732.
56. LaBella F, Waykole P, Queen G. Formation of insoluble gels and dityrosine by the action of peroxidase on soluble collagens. Biochem Biophys Res Commun. 1968;30:333-338.
57. Waykole P, Heidemann E. Dityrosine in collagen. Connect Tissue Res. 1976;4:219-222.
58. Kato Y, Uchida K, Kawakishi S. Aggregation of collagen exposed to UVA in the presence of riboflavin: a plausible role of tyrosine modification. Photochem Photobiol. 1994;59:343-349.
59. Ishitsuka Y, Maniwa F, Koide C, et al. Detection of modified tyrosines as an inflammation marker in a photo-aged skin model. Photochem Photobiol. 2007;83:698-705.
60. Au V, Madison A. Effects of singlet oxygen on the extracellular matrix protein collagen: oxidation of the collagen crosslink histidinohydroxylysinonorleucine and histidine. Arch Biochem Biophys. 2000;384:133-142.
61. Deyl Z, Miǩs i'ik I. Separation of collagen type I chain polymers by electrophoresis in non-cross-linked polyacrylamide-filled capillaries. Journal of Chromatography A. 1995; 698:369-373.
62. Sung HW, Chang WH, Ma CY, Lee MH. Crosslinking of biological tissues using genipin and/or carbodiimide. J Biomed Mater Res A. 2003;64:427-438.
63. Parry DAD. The molecular fibrillar structure of collagen and its relationship to the mechanical properties of connective tissue. Biophys Chem.1988;29:195-209.
64. Spoerl E, Wollensak G, Seiler T. Increased resistance of crosslinked cornea against enzymatic digestion. Curr Eye Res. 2004;29:35-40.
65. Schilde T, Kohlhaas M, Spoerl E, Pillunat LE. Enzymatic evidence of the depth dependence of stiffening on riboflavin/ UVA treated corneas. Ophthalmologe. 2008;105:165-169.
66. Berman. Collagenase inhibitors: rationale for their use in treating corneal ulceration. Int Ophthalmol Clin. 1975;15:49-66.
67. Brooks DE, Ollivier FJ. Matrix metalloproteinase inhibition in corneal ulceration. Vet Clin North Am Small Anim Pract. 2004;34:611-622.
68. Funderburgh JL. Keratan sulfate: structure, biosynthesis, and function. Glycobiology. 2000;10:951-958.