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ARTICLE |

Ultrastructural Location of Extracellular Matrix Components in the Optic Nerve Head FREE

Harry A. Quigley, MD; Janice A. Jerdan, PhD; Nancy L. L'Hernault, MA; John C. Morrison, MD
[+] Author Affiliations

Accepted for publication April 14, 1988.

Presented in part at the Annual Meeting of the Association for Research in Vision and Ophthalmology, Sarasota, Fla, May 5, 1988.

Reprint requests to Maumenee B-110, The Wilmer Institute, The Johns Hopkins Hospital, Baltimore, MD 21205 (Dr Quigley).


Arch Ophthalmol. 1989;107(1):123-129. doi:10.1001/archopht.1989.01070010125040
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• The distributions of laminin and collagen types I through V were determined in optic nerve heads of cynomolgus monkeys using colloidal gold immunoelectron microscopy. Collagen types I and III localized to striated collagen fibrils in arterial walls throughout the optic nerve head and to fibrils comprising the core of the lamina cribrosa beams and optic nerve septa. Collagen type IV and laminin localized to basement membranes of all blood vessels and to basement membranes of astrocytes that lie between the laminar beams and line the optic nerve septa and pia mater. Collagen type V was detected both in striated collagen fibrils and in vascular and astrocyte basement membranes. These results provide a detailed understanding of the optic nerve head extracellular matrix distribution and illustrate a sensitive method for future study of its role in glaucomatous optic nerve damage.

REFERENCES

Quigley HA, Green WR:  The histology of human glaucoma cupping and optic nerve damage: Clinicopathologic correlation in 21 eyes . Ophthalmology 1979;;86:1803-1827.
Quigley HA, Addicks EM:  Chronic experimental glaucoma in primates: II. Effect of extended intraocular pressure elevation on optic nerve head and axonal transport . Invest Ophthalmol Vis Sci 1980;;19:137-152.
Minckler DS, Bunt AH, Klock IB:  Radioautographic and cytochemical ultrastructural studies of axoplasmic transport in the monkey optic nerve head . Invest Ophthalmol Vis Sci 1978;;17:33-50.
Quigley HA, Addicks EM, Green WR, et al:  Optic nerve damage in human glaucoma: II. The site of injury and susceptibility to damage . Arch Ophthalmol 1981;;99:635-649.
Anderson DR, Hendrickson A:  Effect of intraocular pressure on rapid axoplasmic transport in monkey optic nerve . Invest Ophthalmol Vis Sci 1974;;13:771-783.
Anderson DR:  Ultrastructure of human and monkey lamina cribrosa and optic nerve head . Arch Ophthalmol 1969;;82:800-814.
Hogan MJ, Alvarado JA, Weddell JE:  The optic nerve , in Histology of the Human Eye . Philadelphia, WB Saunders Co, 1971;, pp 561-571.
Timpl R, Dziadek M:  Structure, development, and molecular pathology of basement membranes . Int Rev Exp Pathol 1986;;29:1-112.
Farquhar MG:  The glomerular basement membrane: A selective macromolecular filter , in Hay ED (ed): Cell Biology of Extracellular Matrix . New York, Plenum Press, 1981;, pp 335-378.
Martinez-Hernandez A, Amenta PS:  The basement membrane in pathology . Lab Invest 1983;;48:656-677.
Drance SA:  Low-tension glaucoma: Enigma and opportunity . Arch Ophthalmol 1985;;103:1131-1133.
Levine RZ:  Low tension glaucoma: A critical review and new material . Surv Ophthalmol 1980;;24:621-663.
Tengroth B, Rehnberg M, Amitzboll:  A comparative analysis of the collagen type and distribution in the trabecular meshwork, sclera, lamina cribrosa and the optic nerve in the human eye . Acta Ophthalmol 1985;;63( (suppl) ):91-93.
Jeng S, Goldbaum M, Logemann RB, et al:  Extracellular matrix of the optic nerve . Invest Ophthalmol Vis Sci 1987;;28( (suppl) ):61.
Hernandez MR, Igoe F, Neufeld AH:  Extracellular matrix of the human optic nerve head . Am J Ophthalmol 1986;;102:139-148.
Hernandez MR, Luo XX, Igoe F, et al:  Extracellular matrix of the human lamina cribrosa . Am J Ophthalmol 1987;;104:567-576.
Morrison J, L'Hernault N, Jerdan J, et al: Extracellular matrix composition of the monkey optic nerve head. Invest Ophthalmol Vis Sci, in press.
Konomi H, Hayashi T, Sano J, et al:  Immunohistochemical localization of type I, III, and IV collagens in the sclera and choroid of bovine, rat, and normal and pathological human eyes . Biomed Res 1983;;4:451-458.
Quigley HA, Hohman RM:  Laser energy levels for trabecular meshwork damage in the primate eye . Invest Ophthalmol Vis Sci 1983;;24:1305-1307.
Quigley HA, Sanchez RM, Dunkelberger GR:  Chronic glaucoma selectively damages large optic nerve fibers . Invest Ophthalmol Vis Sci 1987;;28:913-920.
Altman LG, Schneider BG, Papermaster DS:  Rapid embedding of tissues in lowicryl K4M for immunoelectron microscopy . J Histochem Cytochem 1984;;32:1217-1223.
Erickson PA, Anderson DH, Fisher SK:  Use of uranyl acetate en bloc to improve tissue preservation and labeling for post-embedding immunoelectron microscopy . J Electron Microsc Tech 1987;;15:303-314.
McGarvey ML, Baron-Van Evercooren A, Kleinman HK, et al:  Synthesis and effects of basement membrane components in cultured rat Schwann cells . Dev Biol 1984;;105:18-28.
Quigley HA:  The pathogenesis of reversible cupping in congenital glaucoma . Am J Ophthalmol 1977;;84:358-370.
Birk DE, Fitch JM, Linsenmayer TF:  Organization of collagen types I and V in the embryonic chicken cornea . Invest Ophthalmol Vis Sci 1986;;27:1470-1477.
Konomi F, Hayashi T, Nakayasu K, et al:  Localization of type V collagen and type IV collagen in human cornea, lung, and skin . Am J Pathol 1984;;116:417-426.
Modesti A, Kalebic T, Scarpa S, et al:  Type V collagen in human amnion is a 12 nm fibrillar component of the pericellular interstitium . Eur J Cell Biol 1984;;35:246-255.
Smith LT, Holbrook KA, Madri JA:  Collagen types I, III, and V in human embryonic and fetal skin . Am J Anat 1986;;175:507-521.
Roll FJ, Madri JA, Albert J, et al:  Codistribution of collagen types IV and AB2 in basement membranes and mesangium of the kidney: An immunoferritin study of ultrathin frozen sections . J Cell Biol 1980;;85:597-616.
Murphy CG, Yun AJ, Newsome DA:  Localization of extracellular proteins of the human trabecular meshwork by indirect immunofluorescence . Am J Ophthalmol 1987;;104:33-43.
Konomi H, Hayashi T, Sano J, et al:  Immunohistochemical localization of type I, III, and IV collagens in the sclera and choroid of bovine, rat, and normal and pathological human eyes . Biomed Res 1983;;4:451-458.
Bailey AJ:  Structure, function and ageing of the collagens of the eye . Eye 1987;;1:175-183.
Schmut O:  The identification of type III collagen in calf and bovine cornea and sclera . Exp Eye Res 1977;;25:505-509.
Kelley FW, Morin JD, Vesely S:  Characterization of collagen from normal human sclera . Exp Eye Res 1984;;39:533-542.
Laurie GW, LeBlond CP, Martin GR:  Localization of type IV collagen, laminin, heparan sulfate proteoglycan, and fibronectin to the basal lamina of basement membranes . J Cell Biol 1982;;95:340-344.

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Quigley HA, Green WR:  The histology of human glaucoma cupping and optic nerve damage: Clinicopathologic correlation in 21 eyes . Ophthalmology 1979;;86:1803-1827.
Quigley HA, Addicks EM:  Chronic experimental glaucoma in primates: II. Effect of extended intraocular pressure elevation on optic nerve head and axonal transport . Invest Ophthalmol Vis Sci 1980;;19:137-152.
Minckler DS, Bunt AH, Klock IB:  Radioautographic and cytochemical ultrastructural studies of axoplasmic transport in the monkey optic nerve head . Invest Ophthalmol Vis Sci 1978;;17:33-50.
Quigley HA, Addicks EM, Green WR, et al:  Optic nerve damage in human glaucoma: II. The site of injury and susceptibility to damage . Arch Ophthalmol 1981;;99:635-649.
Anderson DR, Hendrickson A:  Effect of intraocular pressure on rapid axoplasmic transport in monkey optic nerve . Invest Ophthalmol Vis Sci 1974;;13:771-783.
Anderson DR:  Ultrastructure of human and monkey lamina cribrosa and optic nerve head . Arch Ophthalmol 1969;;82:800-814.
Hogan MJ, Alvarado JA, Weddell JE:  The optic nerve , in Histology of the Human Eye . Philadelphia, WB Saunders Co, 1971;, pp 561-571.
Timpl R, Dziadek M:  Structure, development, and molecular pathology of basement membranes . Int Rev Exp Pathol 1986;;29:1-112.
Farquhar MG:  The glomerular basement membrane: A selective macromolecular filter , in Hay ED (ed): Cell Biology of Extracellular Matrix . New York, Plenum Press, 1981;, pp 335-378.
Martinez-Hernandez A, Amenta PS:  The basement membrane in pathology . Lab Invest 1983;;48:656-677.
Drance SA:  Low-tension glaucoma: Enigma and opportunity . Arch Ophthalmol 1985;;103:1131-1133.
Levine RZ:  Low tension glaucoma: A critical review and new material . Surv Ophthalmol 1980;;24:621-663.
Tengroth B, Rehnberg M, Amitzboll:  A comparative analysis of the collagen type and distribution in the trabecular meshwork, sclera, lamina cribrosa and the optic nerve in the human eye . Acta Ophthalmol 1985;;63( (suppl) ):91-93.
Jeng S, Goldbaum M, Logemann RB, et al:  Extracellular matrix of the optic nerve . Invest Ophthalmol Vis Sci 1987;;28( (suppl) ):61.
Hernandez MR, Igoe F, Neufeld AH:  Extracellular matrix of the human optic nerve head . Am J Ophthalmol 1986;;102:139-148.
Hernandez MR, Luo XX, Igoe F, et al:  Extracellular matrix of the human lamina cribrosa . Am J Ophthalmol 1987;;104:567-576.
Morrison J, L'Hernault N, Jerdan J, et al: Extracellular matrix composition of the monkey optic nerve head. Invest Ophthalmol Vis Sci, in press.
Konomi H, Hayashi T, Sano J, et al:  Immunohistochemical localization of type I, III, and IV collagens in the sclera and choroid of bovine, rat, and normal and pathological human eyes . Biomed Res 1983;;4:451-458.
Quigley HA, Hohman RM:  Laser energy levels for trabecular meshwork damage in the primate eye . Invest Ophthalmol Vis Sci 1983;;24:1305-1307.
Quigley HA, Sanchez RM, Dunkelberger GR:  Chronic glaucoma selectively damages large optic nerve fibers . Invest Ophthalmol Vis Sci 1987;;28:913-920.
Altman LG, Schneider BG, Papermaster DS:  Rapid embedding of tissues in lowicryl K4M for immunoelectron microscopy . J Histochem Cytochem 1984;;32:1217-1223.
Erickson PA, Anderson DH, Fisher SK:  Use of uranyl acetate en bloc to improve tissue preservation and labeling for post-embedding immunoelectron microscopy . J Electron Microsc Tech 1987;;15:303-314.
McGarvey ML, Baron-Van Evercooren A, Kleinman HK, et al:  Synthesis and effects of basement membrane components in cultured rat Schwann cells . Dev Biol 1984;;105:18-28.
Quigley HA:  The pathogenesis of reversible cupping in congenital glaucoma . Am J Ophthalmol 1977;;84:358-370.
Birk DE, Fitch JM, Linsenmayer TF:  Organization of collagen types I and V in the embryonic chicken cornea . Invest Ophthalmol Vis Sci 1986;;27:1470-1477.
Konomi F, Hayashi T, Nakayasu K, et al:  Localization of type V collagen and type IV collagen in human cornea, lung, and skin . Am J Pathol 1984;;116:417-426.
Modesti A, Kalebic T, Scarpa S, et al:  Type V collagen in human amnion is a 12 nm fibrillar component of the pericellular interstitium . Eur J Cell Biol 1984;;35:246-255.
Smith LT, Holbrook KA, Madri JA:  Collagen types I, III, and V in human embryonic and fetal skin . Am J Anat 1986;;175:507-521.
Roll FJ, Madri JA, Albert J, et al:  Codistribution of collagen types IV and AB2 in basement membranes and mesangium of the kidney: An immunoferritin study of ultrathin frozen sections . J Cell Biol 1980;;85:597-616.
Murphy CG, Yun AJ, Newsome DA:  Localization of extracellular proteins of the human trabecular meshwork by indirect immunofluorescence . Am J Ophthalmol 1987;;104:33-43.
Konomi H, Hayashi T, Sano J, et al:  Immunohistochemical localization of type I, III, and IV collagens in the sclera and choroid of bovine, rat, and normal and pathological human eyes . Biomed Res 1983;;4:451-458.
Bailey AJ:  Structure, function and ageing of the collagens of the eye . Eye 1987;;1:175-183.
Schmut O:  The identification of type III collagen in calf and bovine cornea and sclera . Exp Eye Res 1977;;25:505-509.
Kelley FW, Morin JD, Vesely S:  Characterization of collagen from normal human sclera . Exp Eye Res 1984;;39:533-542.
Laurie GW, LeBlond CP, Martin GR:  Localization of type IV collagen, laminin, heparan sulfate proteoglycan, and fibronectin to the basal lamina of basement membranes . J Cell Biol 1982;;95:340-344.

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