Mapping the differential distribution of glycosaminoglycans in the adult human retina, choroid, and sclera

Investigative Ophthalmology and Visual Science

Volumn 52, Issue 9, 2011, Pages 6511-6521

  Clark, Simon J ^a   Keenan, Tiarnan D L ^b,c   Fielder, Helen L ^a,d   Collinson, Lisa J ^a   Holley, Rebecca J ^b   Merry, Catherine L R ^b   van Kuppevelt, Toin H ^e   Day, Anthony J ^a   Bishop, Paul N ^b,c  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CHONDROITIN SULFATE; DERMATAN SULFATE; GLYCOSAMINOGLYCAN; HEPARAN SULFATE; HYALURONIC ACID; KERATAN SULFATE; FLUORESCENT DYE;

ADULT; AGED; ARTICLE; BASEMENT MEMBRANE; CHOROID; CONTROLLED STUDY; FEMALE; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN TISSUE; MALE; NERVE FIBER; PHOTORECEPTOR; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RETINA; RETINA GANGLION CELL; SCLERA; SULFATION; DONOR; METABOLISM; MIDDLE AGED;

AGED, 80 AND OVER; CHONDROITIN SULFATES; CHOROID; DERMATAN SULFATE; FEMALE; FLUORESCENT DYES; GLYCOSAMINOGLYCANS; HEPARITIN SULFATE; HUMANS; KERATAN SULFATE; MALE; MICROSCOPY, FLUORESCENCE; MIDDLE AGED; RETINA; SCLERA; TISSUE DONORS;

EID: 80054693561     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.11-7909     Document Type: Article

References (46)

1. Theocharis AD, Skandalis SS, Tzanakakis GN, Karamanos NK. Proteoglycans in health and disease: novel roles for proteoglycans in malignancy and their pharmacological targeting. FEBS Lett J. 2010; 277:3904-3923.
2. Lindahl U, Li JP. Interactions between heparan sulfate and proteins-design and functional implications. Int Rev Cell Mol Biol. 2009;276:105-159.
3. Kresse H, Schonherr E. Proteoglycans of the extracellular matrix and growth control. J Cell Physiol. 2001;189:266-274.
4. Taylor KR, Gallo RL. Glycosaminoglycans and their proteoglycans: host-associated molecular patterns for initiation and modulation of inflammation. FASEB J. 2006;20:9-22.
5. Mulloy B, Forster MJ. Conformation and dynamics of heparin and heparan sulfate. Glycobiology. 2000;10:1147-1156.
6. Tammi MI, Day AJ, Turley EA. Hyaluronan and homeostasis: a balancing act. J Biol Chem. 2002;277:4581-4584.
7. Toole BP. Hyaluronan: from extracellular glue to pericellular cue. Nat Rev Cancer. 2004;4:528-539.
8. Inatani M, Tanihara H. Proteoglycans in retina. Prog Retin Eye Res. 2002;21:429-447.
9. Clark SJ, Bishop PN, Day AJ. Complement factor H and age-related macular degeneration: the role of glycosaminoglycan recognition in disease pathology. Biochem Soc Trans. 2010;38:1342-1348.
10. Clark SJ, Perveen R, Hakobyan S, et al. Impaired binding of the age-related macular degeneration-associated complement factor H 402H allotype to Bruch's membrane in human retina. J Biol Chem. 2010;285:30192-30202.
11. David G, Bai XM, van der Schueren B, Cassiman JJ, van den Berghe H. Developmental changes in heparan sulfate expression: In situ detection with mAbs. J Cell Biol. 1992;119:961-975.
12. Wijnhoven TJ, de Westerlo EM, Smits NC et al. Characterization of anticoagulant heparinoids by immunoprofiling. Glycoconj J. 2008; 25:177-185.
13. Dennissen MABA, Jenniskens GJ, Pieffers M, et al. Large, tissueregulated domain diversity of heparan sulfates demonstrated by phage display antibodies. J Biol Chem. 2002;277:10982-10986.
14. Kurup S, Wijnhoven TJM, Jenniskens GJ et al. Characterization of anti-heparan sulfate phage display antibodies AO4B08 and HS4E4. J Biol Chem. 2007;282:21032-21042.
15. ten Dam GB, Kurup S, van de Westerlo EMA, et al. 3-O-sulfated oligosaccharide structures are recognized by anti-heparan sulfate antibody HS4C3. J Biol Chem. 2006;281:4654-4662.
16. Caterson B, Christner JE, Couchman JR. Production and characterization of monoclonal antibodies directed against connective tissue proteoglycans. Fed Proc. 1985;44:386-393.
17. Yada T, Arai M, Suzuki S, Kimata K. Occurrence of collagen and proteoglycan forms of type IX collagen in chick embryo cartilage. J Biol Chem. 1992;267:9391-9397.
18. Jandik KA, Gu K, Linhardt JL. Action pattern of polysaccharide lyases on glycosaminoglycans. Glycobiology. 1994;4:289-296.
19. Caterson B, Christner JE, Barker JR. Identification of a monoclonal antibody that specifically recognizes corneal and skeletal keratan sulfate: monoclonal antibodies to cartilage proteoglycans. J Biol Chem. 1983;258:8848-8854.
20. Lamanna WC, Baldwin RJ, Padva M, et al. Heparan sulphate 6-Oendosulphatases-discrete in vivo activities and functional cooperativity. Biochem J. 2006;400:63-73.
21. Johnson CE, Crawford BE, Stavridis M, et al. Essential alterations of heparan sulfate during the differentiation of embryonic stem cells to Sox1-enhanced green fluorescent protein-expressing neural progenitor cells. Stem Cells. 2007;25:1913-1923.
22. Baldwin RB, ten Dam GB, van Kuppevelt TH, et al. A developmentally-regulated heparan sulfate epitope defines a sub-population with increased blood potential during mesodermal differentiation. Stem Cells. 2008;26:3108-3118.
23. Van Kuppevelt TH, Dennissen MABA, van Venrooij WJ, Hoet RMA, Veerkamp JH. Generation and application of type-specific antiheparan sulfate antibodies using phage display technology. J Biol Chem. 1998;273:12960-12966.
24. Jenniskens GJ, Oosterhof A, Brandwijk R, Veerkamp JH, van Kuppevelt TH. Heparan sulfate heterogeneity in skeletal muscle basal lamina: demonstration by phage display-derived antibodies. J Neurosci. 2000;20:4099-4111.
25. Zimmermann DR, Ruoslahti E. Multiple domains of the large fibroblast proteoglycan, versican. EMBO J. 1989;8:2975-2981.
26. Seyfried NT, McVey GF, Almond A, et al. Expression and purification of functionally active hyaluronan-binding domains from human cartilage link protein, aggrecan and versican: formation of ternary complexes with defined hyaluronan oligosaccharides. J Biol Chem. 2005;280:5435-5448.
27. Day AJ, Aplin RT, Willis AC. Overexpression, purification, and refolding of link module from human TSG-6 in Escherichia coli: effect of temperature, media, and mutagenesis on lysine misincorporation at arginine AGA codons. Protein Expr Purif. 1996;8:1-16.
28. Clark SJ, Higman VA, Mulloy B, et al. His-384 allotypic variant of factor H associated with age-related macular degeneration has different heparin binding properties from the non-disease-associated form. J Biol Chem. 2006;281:24713-24720.
29. White J, Lukacik P, Esser D, et al. Biological activity, membrane-targeting modification, and crystallization of soluble human decay accelerating factor expressed in E. coli. Protein Sci. 2004;13:2406-2415.
30. Kuznetsova SA, Issa P, Perruccio EM, et al. Versican-thrombospondin-1 binding in vitro and colocalization in microfibrils by inflammation on vascular smooth muscle cells. J Cell Sci. 2006;119:4499-4509.
31. Call TW, Hollyfield JG. Sulfated proteoglycans in Bruch's membrane of the human eye: localization and characterization using cupromeronic blue. Exp. Eye Res. 1990;51:451-462.
32. Witmer AN, van den Born J, Vrensen GFJM and Schlingemann RO. Vascular localization of heparan sulfate proteoglycans in retinas of patients with diabetes mellitus and in VEGF-induced retinopathy using domain-specific antibodies. Curr Eye Res. 2001;3:190-197.
33. Esko JD, Selleck SB. Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu Rev Biochem. 2002;71:435-471.
34. Couchman JR, Caterson B, Christner JE, Baker JR. Mapping by monoclonal antibody detection of glycosaminoglycans in connective tissues. Nature. 1984;307:650-652.
35. Day AJ, Clark SJ, Bishop PN. Understanding the molecular basis of age-related macular degeneration and how the identification of new mechanisms may aid the development of novel therapies. Expert Rev Ophthalmol. 2011;6:123-128.
36. Ashikari-Hada S, Habuchi H, Kariya Y, Kimata K. Heparin regulates vascular endothelial growth factor165-dependent mitotic activity, tube formation, and its receptor phosphorylation of human endothelial cells. J Biol Chem. 2005;280:31508-31515.
37. Fuster MM, Wang L. Endothelial heparan sulfate in angiogenesis. Prog Mol Biol Transl Sci. 2010;93:179-212.
38. Hollyfield JG, Rayborn ME, Midura RJ, Shadreach KG, Acharya S. Chondroitin sulfate proteoglycan core proteins in the interphotoreceptor matrix: a comparative study using biochemical and immunohistochemical analysis. Exp Eye Res. 1999;69:311-322.
39. Acharya S, Foletta VC, Lee JW et al. SPACRCAN, a novel human interphotoreceptor matrix hyaluronan-binding proteoglycan synthesized by photoreceptors and pinealocytes. J Biol Chem. 2000; 275:6945-6955.
40. Young RD. The ultrastructural organization of proteoglycans and collagen in human and rabbit scleral matrix. J Cell Sci. 1985;74: 95-104.
41. Quantock AJ, Mek KM. Axial electron density of human scleral collagen: Location of proteoglycans by X-ray diffraction. J Biophys. 1988;54:159-164.
42. Day AJ, Prestwich GD. Hyaluronan-binding proteins: tying up the giant. J Biol Chem. 2002;277:4585-4588.
43. Hollyfield JG, Rayborn ME, Tammi M, Tammi R. Hyaluronan in the interphotoreceptor matrix of the eye: species differences in content, distribution, ligand binding and degradation. Exp Eye Res. 1998;66:241-248.
44. Geisert EE, Williams RC, Bidanset DJ. A CNS specific proteoglycan associated with astrocytes in rat optic nerve. Brain Res. 1992;571: 165-168.
45. McAdams BD, McLoon SC. Expression of chondroitin sulfate and keratan sulfate proteoglycans in the path of growing retinal axons in the developing chick. J Comp Neurol. 1995;352:594-606.
46. McCabe CF, Cole GJ. Expression of the barrier-associated proteins EAP-300 and claustrin in the developing central nervous system. Brain Res Dev Brain Res. 1992;70:9-24.