Diabetes-induced morphological, biomechanical, and compositional changes in ocular basement membranes

Experimental Eye Research

Volumn 116, Issue , 2013, Pages 298-307

  To, Margaret ^a   Goz, Alexandra ^b   Camenzind, Leon ^b,c   Oertle, Philipp ^c   Candiello, Joseph ^d   Sullivan, Mara ^e   Henrich, Paul Bernhard ^b   Loparic, Marko ^c   Safi, Farhad ^a   Eller, Andrew ^a   Halfter, Willi ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF BASEL   (Switzerland)

^c UNIVERSITY OF BASEL   (Switzerland)

^d University of Pittsburgh   (United States)

^e UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Basement membrane; Collagen IV; Inner limiting membrane; Laminin; Proteoglycans

Indexed keywords

AGRIN; COLLAGEN TYPE 4; CORE PROTEIN; FIBRONECTIN; LAMININ; SCLEROPROTEIN; TENASCIN;

ADULT; AGED; ARTICLE; ATOMIC FORCE MICROSCOPY; BASEMENT MEMBRANE; BIOCHEMICAL COMPOSITION; BRAIN HEMORRHAGE; CAPILLARY TUBE; CEREBROVASCULAR ACCIDENT; CLINICAL ARTICLE; CONGESTIVE HEART FAILURE; CONTROLLED STUDY; DEGLYCOSYLATION; DIABETES MELLITUS; DIABETIC PATIENT; FEMALE; HEART INFARCTION; HUMAN; IMMUNOCYTOCHEMISTRY; INSULIN DEPENDENT DIABETES MELLITUS; MALE; MALIGNANT NEOPLASTIC DISEASE; MICROSCOPY; NON INSULIN DEPENDENT DIABETES MELLITUS; OCULAR BASEMENT MEMBRANE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; RETINAL THICKNESS; TRAFFIC ACCIDENT; TRANSMISSION ELECTRON MICROSCOPY; UPREGULATION; WESTERN BLOTTING;

BASEMENT MEMBRANE; COLLAGEN IV; INNER LIMITING MEMBRANE; LAMININ; PROTEOGLYCANS;

ADULT; AGED; AGED, 80 AND OVER; BASEMENT MEMBRANE; BLOTTING, WESTERN; DIABETIC RETINOPATHY; ELASTICITY; EXTRACELLULAR MATRIX PROTEINS; FEMALE; HUMANS; MALE; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, ELECTRON, TRANSMISSION; MIDDLE AGED; RETINA;

EID: 84886865742     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2013.09.011     Document Type: Article

References (51)

1. Ashton N. Vascular basement membrane changes in diabetic retinopathy. Br. J. Ophthalmol. 1974, 58:344-366.
2. Balasubramani M., Schreiber E.M., Candiello J., Balasubramani G.K., Kurtz J., Halfter W. Molecular interactions in the retinal basement membrane system: a proteomics approach. Matrix Biol. 2010, 29:471-483.
3. Bishop P.N., Holmes D.F., Kadler K.E., McLeod D., Bos K.J. Age-related changes on the surface of vitreous collagen fibrils. Investig. Ophthalmol. Vis. Sci. 2003, 45:1041-1046.
4. Caligliero E., Maiello M., Boeri D., et al. Increased expression of of basement membrane components in human endothelial cells cultured in high glucose. J.Clin. Investig. 1988, 82:735-738.
5. Candiello J., Balasubramani M., Schreiber E.M., Cole G.J., Mayer U., Halfter W., Lin H. Biomechanical properties of native basement membranes. FEBS J. 2007, 274:2897-2908.
6. Candiello J., Cole G.J., Halfter W. Age-dependent changes in the structure, composition and biophysical properties of a human basement membrane. Matrix Biol. 2010, 29:402-410.
7. Cheung N., Mitchell P., Wong T.Y. Diabetic retinopathy. Lancet 2010, 376:124-136.
8. Chiquet-Ehrismann R., Tucker R.P. Connective tissues: signaling by tenascins. Int. J. Biochem. Cell Biol. 2004, 36L:1085-1089.
9. Coorey N.J., Shen W., Chung S.H., Gilles M.C. The role of glia in retinal vascular disease. Clin. Exp. Optom. 2012, 35:266-281.
10. Cotman S., Halfter W., Cole G.J. Agrin binds to amyloid (Aβ), accelerates Aβ fibril formation, and is localized to Aβ deposits in Alzheimer's disease brain. Mol. Cell Neurosci. 2000, 15:183-198.
11. Curtis T.M., Gardiner T.A., Stitt A.W. Microvascular lesions of diabetic retinopathy: clues towards understanding pathogenesis?. Eye 2009, 23:1496-1508.
12. Danysh B.P., Czymmek K.J., Olurin P.T., Sivak J.G., Duncan M.K. Contributions of mouse genetic background and age on anterior lens capsule thickness. Anat. Rec. 2008, 291:1619-1627.
13. Danysh B.P., Duncan M.K. The lens capsule. Exp. Eye Res. 2008, 88:151-164.
14. Degenhardt T.P., Thorpe S.R., Baynes J.W. Chemical modification of proteins by methylglyoxal. Cell Mol. Biol. 1998, 44:1139-1145.
15. Duhamel R.C., Meezan E., Brendel K. Selective solubilization of two populations of polypeptides from bovine retinal basement membranes. Exp. Eye Res. 1983, 36:257-267.
16. Durham J.T., Herman I.M. Microvascular modifications in diabetic retinopathy. Curr. Diabetes Rep. 2011, 11:253-264.
17. Erickson A.C., Couchman J.R. Still more complexity in mammalian basement membranes. J.Histochem. Cytochem. 2000, 48:1291-1306.
18. Fong D.S., Aiello L.P., Ferris F.L., Klein R. Diabetic retinopathy. Diabetes Care 2004, 27:2540-2553.
19. Frank R.N. Diabetic retinopathy. N.Engl. J. Med. 2004, 350:48-58.
20. Gardiner T.A., Anderson H.R., Degenhardt T., et al. Prevention of retinal capillary basement membrane thickening in diabetic dogs by a non-steroidal anti-inflammatory drug. Diabetologia 2003, 46:1269-1275.
21. Halfter W., Candiello J., Hu H., Zhang P., Schreiber E., Balasubramani M. Protein composition and biochemical properties of invivo-derived basement membranes. Cell Adhes. Migration 2013, 7:1-8.
22. Halfter W., Monnier C., Müller D., Oertle P., Uechi G., Balasubramani M., Safi F., Lim R., Loparic M., Henrich P.B. The bi-functional organization of human basement membranes. PLoS One 2013, 8:e67660.
23. Halfter W., Dong S., Dong A., Eller A.W., Nischt R. Origin and turnover of ECM proteins from the inner limiting membrane and vitreous body. Eye 2008, 22:1207-1213.
24. Halfter W., Dong S., Schurer B., Ring C., Cole G.J., Eller A.W. Embryonic synthesis of the inner limiting membrane and vitreous body. Investig. Ophtalmol. Vis. Sci. 2005, 46:2202-2220.
25. Henrich P.B., Monnier C.A., Halfter W., Haritoglou C., Strauss R.W., Lim R.Y., Loparic M. Nanoscale topographic and biomechanical studies of the human internal limiting membrane. Investig. Ophthalmol. Vis. Sci. 2012, 53:2561-2570.
26. Hutter J.L., Bechhoefer J. Calibration of atomic-force microscope tips. J.Rev. Sci. Instrum. 1993, 64:1868-1873.
27. Kempen J.H., Colman B.J., Leske M.G., et al. For the Eye Disease Prevalence Research Group. The prevalence of diabetic retinopathy among adults in the United States. Arch. Ophthalmol. 2004, 122:552-563.
28. King R.H. The role of glycation in the pathology of diabetic polyneuropathy. J.Clin. Pathol. Mol. Pathol. 2001, 54:400-408.
29. Kuiper E., van Zijderveld R., Rosenberg P., Lyons K.M., et al. Connective tissue growth factor is necessary for retinal capillary basal thickening in diabetic mice. J.Histochem. 2008, 56:785-792.
30. Ljubimov A.V., Burgeson R.E., Butkowski R.J., Couchman J.R., Zardi L., Ninomiya Y., Sado Y., Huang Z.S., Nesburn A.B., Kenney M.C. Basement membrane abnormalities in human eyes with diabetic retinopathy. J.Histochem. Cytochem. 1996, 44:1469-1479.
31. Mackie E., Halfter W., Liveranio D. Induction of tenascin in healing wounds. J.Cell Biol. 1988, 107:2157-2167.
32. Maroudas A., Palla G., Gilav E. Racemization of aspartic acid in human articular cartilage. Conn. Tissue Res. 1992, 28:161-169.
33. Murphy C., Alvarado J., Juster R. Prenatal and postnatal growth of the human Descemet's membrane. Investig. Ophthal Vis. Sci. 1984, 25:1402-1415.
34. Neuman K.H., Keller C., Kuhn K.W., Stolte H., Schurek H.-J. Age-dependent thickening of glomerular basement membrane has no major effect on glomerular hydraulic conductivity. Nephrol. Dial. Transpl. 2004, 19:805-811.
35. Osterby R. Basement membrane morphology in diabetes mellitus. Diabetes Mellitus. Theory and Practice 1990, 220-233. Elsevier Science Publishing Co. Inc, New York. H. Rifkin, D. Porte (Eds.).
36. Pankov R., Yamada K.M. Fibronectin, at a glance. J.Cell Sci. 2002, 115:3861-3873.
37. Roy S., Lorenzi M. Early biosynthetic changes in the diabetic-like retinopathy of galactose-fed rats. Diabetologia 1996, 39:735-738.
38. Roy S., Cagliero E., Lorenzi M. Fibronectin overexpression in retinal microvessels of patients with diabetes. Investig. Ophthalmol. Vis. Sci. 1996, 37:258-266.
39. Roy S., Ha J., Trudeau K., Beglova E. Vascular basement membrane thickening in diabetic retinopathy. Curr. Eye Res. 2010, 35:1045-1056.
40. Sherwin R., Jastreboff A.M. Year in diabetes 2012: the diabetes Tsunami. J.Clin. Endocrinol. Metab. 2012, 97:4293-4301.
41. Stitt A.W., Li Y.M., Gardiner T.A., et al. Advanced glycation products (AGEs) co-localize with AGE receptors in the retinal vasculature of diabetic and AGE-infused rats. Am. J. Pathol. 1997, 50:523-531.
42. SundarRaj N., Wilson J. Monoclonal antibody to human basement membrane collagen IV. Immunology 1982, 47:133-140.
43. Timpl R., Brown J.C. Supramolecular assembly of basement membranes. Bioassays 1996, 18:123-132.
44. Tsilibary E.C. Microvascular basement membranes in diabetes mellitus. J.Pathol. 2003, 200:537-546.
45. Vazquez F., Palacios S., Aleman N., Guerrero F. Changes in the basement membranes and type IV collagen in human skin during aging. Maturitas 1996, 25:209-215.
46. Verzijl N., DeGroot J., Bank R.A., Shaw J.N., Lyons T.J., Bijlsma J.W.J., Lafeber F.J.G., Baynes J.W., TeKoepele J.M. Age-related accumulation of the advanced glycation endproduct of pentosie in human articular cartilage aggrecan: the use of pentosine levels as a quantitative measure of protein turnover. Matrix Biol. 2001, 20:409-417.
47. Verzijl N., DeGroot J., Thorpe S.R., Bank R.A., Shaw J.N., Lyons T.J., Bijlsma J.W., Bijlsma J.W.J., Lafeber F.J.G., Bayne J.W., TeKoepele J.M. Effect of collagen turnover on the accumulation of advanced glycation end products. J.Biol. Chem. 2000, 275:39027-39031.
48. Xi Y., Nette E.G., King D.W., Rosen M. Age-related changes in normal basement membranes. Mech. Aging Dev. 1982, 19:315-334.
49. Yurchenco P.D., Patton B.L. Developmental and pathogenic mechanisms of basement membrane assembly. Curr. Pharm. Des. 2009, 15:1277-1294.
50. Zhang Q., Ames J.M., Smith R.D., Baynes J.W., Metz T.O. Aperspective on the Maillard reaction and the analysis of protein glycation by mass spectrometry: probing the pathogenesis of chronic disease. J.Proteome Res. 2009, 8:754-769.
51. Zatz R., Brenner B.M. Pathogenesis of diabetic microangiopathy. The hemodynamic view. Am. J. Med. 1986, 80:443-453.