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. 1995 Apr;79(4):368–375. doi: 10.1136/bjo.79.4.368

Changes in the collagenous matrix of the aging human lamina cribrosa.

J Albon 1, W S Karwatowski 1, N Avery 1, D L Easty 1, V C Duance 1
PMCID: PMC505104  PMID: 7742286

Abstract

AIMS--The age-related changes in the biochemical composition of the collagenous matrix of the human lamina cribrosa were investigated. METHODS--An age range (3 weeks to 92 years old) of human laminae cribrosae, dissected free of any surrounding structures which contained collagen, were analysed for collagen solubility (n = 58) total collagen content (n = 46), proportion of collagen types (n = 38), and collagen cross linking (n = 30), using hydroxyproline analysis, scanning densitometry of peptides after cyanogen bromide digestion, and high performance liquid chromatography, respectively. RESULTS--Age-related changes included an increase in total collagen and a decrease in the proportion of type III collagen within the lamina cribrosa. The collagen cross link pyridinoline was present at low levels, but demonstrated no trend with age. An age-related increase was found in pentosidine, an advanced glycation product. CONCLUSION--These changes in collagen composition imply that the mechanical properties of the lamina cribrosa are altered, resulting in a stiffer, less resilient structure with age. Such alterations in structure may contribute to the increased susceptibility of the elderly to axonal damage in chronic open angle glaucoma.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anderson D. R. Glaucoma: the damage caused by pressure. XLVI Edward Jackson memorial lecture. Am J Ophthalmol. 1989 Nov 15;108(5):485–495. doi: 10.1016/0002-9394(89)90423-6. [DOI] [PubMed] [Google Scholar]
  2. Andreassen T. T., Seyer-Hansen K., Bailey A. J. Thermal stability, mechanical properties and reducible cross-links of rat tail tendon in experimental diabetes. Biochim Biophys Acta. 1981 Oct 12;677(2):313–317. doi: 10.1016/0304-4165(81)90101-x. [DOI] [PubMed] [Google Scholar]
  3. Bailey A. J., Kent M. J. Non-enzymatic glycosylation of fibrous and basement membrane collagens. Prog Clin Biol Res. 1989;304:109–122. [PubMed] [Google Scholar]
  4. Bannister D. W., Burns A. B. Adaptation of the Bergman and Loxley technique for hydroxyproline determination to the autoanalyzer and its use in determining plasma hydroxyproline in the domestic fowl. Analyst. 1970 Jun;95(131):596–600. doi: 10.1039/an9709500596. [DOI] [PubMed] [Google Scholar]
  5. Birk D. E., Fitch J. M., Babiarz J. P., Linsenmayer T. F. Collagen type I and type V are present in the same fibril in the avian corneal stroma. J Cell Biol. 1988 Mar;106(3):999–1008. doi: 10.1083/jcb.106.3.999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dyer D. G., Blackledge J. A., Thorpe S. R., Baynes J. W. Formation of pentosidine during nonenzymatic browning of proteins by glucose. Identification of glucose and other carbohydrates as possible precursors of pentosidine in vivo. J Biol Chem. 1991 Jun 25;266(18):11654–11660. [PubMed] [Google Scholar]
  7. Eyre D. R., Koob T. J., Van Ness K. P. Quantitation of hydroxypyridinium crosslinks in collagen by high-performance liquid chromatography. Anal Biochem. 1984 Mar;137(2):380–388. doi: 10.1016/0003-2697(84)90101-5. [DOI] [PubMed] [Google Scholar]
  8. Eyre D. R., Paz M. A., Gallop P. M. Cross-linking in collagen and elastin. Annu Rev Biochem. 1984;53:717–748. doi: 10.1146/annurev.bi.53.070184.003441. [DOI] [PubMed] [Google Scholar]
  9. Fechtner R. D., Weinreb R. N. Mechanisms of optic nerve damage in primary open angle glaucoma. Surv Ophthalmol. 1994 Jul-Aug;39(1):23–42. doi: 10.1016/s0039-6257(05)80042-6. [DOI] [PubMed] [Google Scholar]
  10. Goldbaum M. H., Jeng S. Y., Logemann R., Weinreb R. N. The extracellular matrix of the human optic nerve. Arch Ophthalmol. 1989 Aug;107(8):1225–1231. doi: 10.1001/archopht.1989.01070020291041. [DOI] [PubMed] [Google Scholar]
  11. Hernandez M. R., Andrzejewska W. M., Neufeld A. H. Changes in the extracellular matrix of the human optic nerve head in primary open-angle glaucoma. Am J Ophthalmol. 1990 Feb 15;109(2):180–188. doi: 10.1016/s0002-9394(14)75984-7. [DOI] [PubMed] [Google Scholar]
  12. Hernandez M. R., Luo X. X., Andrzejewska W., Neufeld A. H. Age-related changes in the extracellular matrix of the human optic nerve head. Am J Ophthalmol. 1989 May 15;107(5):476–484. doi: 10.1016/0002-9394(89)90491-1. [DOI] [PubMed] [Google Scholar]
  13. Hernandez M. R., Luo X. X., Igoe F., Neufeld A. H. Extracellular matrix of the human lamina cribrosa. Am J Ophthalmol. 1987 Dec 15;104(6):567–576. doi: 10.1016/0002-9394(87)90165-6. [DOI] [PubMed] [Google Scholar]
  14. Hernandez M. R. Ultrastructural immunocytochemical analysis of elastin in the human lamina cribrosa. Changes in elastic fibers in primary open-angle glaucoma. Invest Ophthalmol Vis Sci. 1992 Sep;33(10):2891–2903. [PubMed] [Google Scholar]
  15. Hernandez M. R., Wang N., Hanley N. M., Neufeld A. H. Localization of collagen types I and IV mRNAs in human optic nerve head by in situ hybridization. Invest Ophthalmol Vis Sci. 1991 Jul;32(8):2169–2177. [PubMed] [Google Scholar]
  16. Hernandez M. R., Ye H. Glaucoma: changes in extracellular matrix in the optic nerve head. Ann Med. 1993 Aug;25(4):309–315. doi: 10.3109/07853899309147290. [DOI] [PubMed] [Google Scholar]
  17. Keene D. R., Engvall E., Glanville R. W. Ultrastructure of type VI collagen in human skin and cartilage suggests an anchoring function for this filamentous network. J Cell Biol. 1988 Nov;107(5):1995–2006. doi: 10.1083/jcb.107.5.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Keene D. R., Sakai L. Y., Bächinger H. P., Burgeson R. E. Type III collagen can be present on banded collagen fibrils regardless of fibril diameter. J Cell Biol. 1987 Nov;105(5):2393–2402. doi: 10.1083/jcb.105.5.2393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  20. Levene R. Z. Low tension glaucoma: a critical review and new material. Surv Ophthalmol. 1980 May-Jun;24(6):621–664. doi: 10.1016/0039-6257(80)90123-x. [DOI] [PubMed] [Google Scholar]
  21. Light N. D. Estimation of types I and III collagens in whole tissue by quantitation of CNBr peptides on SDS-polyacrylamide gels. Biochim Biophys Acta. 1982 Mar 18;702(1):30–36. doi: 10.1016/0167-4838(82)90024-3. [DOI] [PubMed] [Google Scholar]
  22. Lovell C. R., Smolenski K. A., Duance V. C., Light N. D., Young S., Dyson M. Type I and III collagen content and fibre distribution in normal human skin during ageing. Br J Dermatol. 1987 Oct;117(4):419–428. doi: 10.1111/j.1365-2133.1987.tb04921.x. [DOI] [PubMed] [Google Scholar]
  23. Malak T. M., Ockleford C. D., Bell S. C., Dalgleish R., Bright N., Macvicar J. Confocal immunofluorescence localization of collagen types I, III, IV, V and VI and their ultrastructural organization in term human fetal membranes. Placenta. 1993 Jul-Aug;14(4):385–406. doi: 10.1016/s0143-4004(05)80460-6. [DOI] [PubMed] [Google Scholar]
  24. Miller K. M., Quigley H. A. The clinical appearance of the lamina cribrosa as a function of the extent of glaucomatous optic nerve damage. Ophthalmology. 1988 Jan;95(1):135–138. doi: 10.1016/s0161-6420(88)33219-7. [DOI] [PubMed] [Google Scholar]
  25. Modesti A., Kalebic T., Scarpa S., Togo S., Grotendorst G., Liotta L. A., Triche T. J. Type V collagen in human amnion is a 12 nm fibrillar component of the pericellular interstitium. Eur J Cell Biol. 1984 Nov;35(2):246–255. [PubMed] [Google Scholar]
  26. Morrison J. C., Jerdan J. A., Dorman M. E., Quigley H. A. Structural proteins of the neonatal and adult lamina cribrosa. Arch Ophthalmol. 1989 Aug;107(8):1220–1224. doi: 10.1001/archopht.1989.01070020286040. [DOI] [PubMed] [Google Scholar]
  27. Quigley H. A., Addicks E. M., Green W. R., Maumenee A. E. Optic nerve damage in human glaucoma. II. The site of injury and susceptibility to damage. Arch Ophthalmol. 1981 Apr;99(4):635–649. doi: 10.1001/archopht.1981.03930010635009. [DOI] [PubMed] [Google Scholar]
  28. Quigley H. A., Addicks E. M. Regional differences in the structure of the lamina cribrosa and their relation to glaucomatous optic nerve damage. Arch Ophthalmol. 1981 Jan;99(1):137–143. doi: 10.1001/archopht.1981.03930010139020. [DOI] [PubMed] [Google Scholar]
  29. Quigley H. A. Childhood glaucoma: results with trabeculotomy and study of reversible cupping. Ophthalmology. 1982 Mar;89(3):219–226. doi: 10.1016/s0161-6420(82)34803-4. [DOI] [PubMed] [Google Scholar]
  30. Quigley H. A., Dorman-Pease M. E., Brown A. E. Quantitative study of collagen and elastin of the optic nerve head and sclera in human and experimental monkey glaucoma. Curr Eye Res. 1991 Sep;10(9):877–888. doi: 10.3109/02713689109013884. [DOI] [PubMed] [Google Scholar]
  31. Quigley H. A., Hohman R. M., Addicks E. M., Massof R. W., Green W. R. Morphologic changes in the lamina cribrosa correlated with neural loss in open-angle glaucoma. Am J Ophthalmol. 1983 May;95(5):673–691. doi: 10.1016/0002-9394(83)90389-6. [DOI] [PubMed] [Google Scholar]
  32. Quigley H. A. The pathogenesis of reversible cupping in congenital glaucoma. Am J Ophthalmol. 1977 Sep;84(3):358–370. doi: 10.1016/0002-9394(77)90680-8. [DOI] [PubMed] [Google Scholar]
  33. Radius R. L., Gonzales M. Anatomy of the lamina cribrosa in human eyes. Arch Ophthalmol. 1981 Dec;99(12):2159–2162. doi: 10.1001/archopht.1981.03930021035010. [DOI] [PubMed] [Google Scholar]
  34. Sawaguchi S., Yue B. Y., Fukuchi T., Iwata K., Kaiya T. Age-related changes of sulfated proteoglycans in the human lamina cribrosa. Curr Eye Res. 1993 Aug;12(8):685–692. doi: 10.3109/02713689308995763. [DOI] [PubMed] [Google Scholar]
  35. Sell D. R., Monnier V. M. End-stage renal disease and diabetes catalyze the formation of a pentose-derived crosslink from aging human collagen. J Clin Invest. 1990 Feb;85(2):380–384. doi: 10.1172/JCI114449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Sell D. R., Monnier V. M. Structure elucidation of a senescence cross-link from human extracellular matrix. Implication of pentoses in the aging process. J Biol Chem. 1989 Dec 25;264(36):21597–21602. [PubMed] [Google Scholar]
  37. Sommer A. Intraocular pressure and glaucoma. Am J Ophthalmol. 1989 Feb 15;107(2):186–188. doi: 10.1016/0002-9394(89)90221-3. [DOI] [PubMed] [Google Scholar]
  38. Ye H., Yang J., Hernandez M. R. Localization of collagen type III mRNA in normal human optic nerve heads. Exp Eye Res. 1994 Jan;58(1):53–63. doi: 10.1006/exer.1994.1194. [DOI] [PubMed] [Google Scholar]

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