Hostname: page-component-8448b6f56d-dnltx Total loading time: 0 Render date: 2024-04-24T06:12:27.629Z Has data issue: false hasContentIssue false

Cochlin and glaucoma: A mini-review

Published online by Cambridge University Press:  06 December 2005

SANJOY K. BHATTACHARYA
Affiliation:
Cole Eye Institute, Cleveland Clinic Foundation, Cleveland
NEAL S. PEACHEY
Affiliation:
Cole Eye Institute, Cleveland Clinic Foundation, Cleveland Louis Stokes VA Medical Center, Cleveland
JOHN W. CRABB
Affiliation:
Cole Eye Institute, Cleveland Clinic Foundation, Cleveland Lerner Research Institute, Cleveland Clinic Foundation, Cleveland

Abstract

Primary open angle glaucoma (POAG) is a leading cause of late onset, progressive, irreversible blindness and, although its etiology is poorly understood, elevated intraocular pressure (IOP) often appears to be a contributory factor. Proteomic and Western analyses of trabecular meshwork (TM) from patients with POAG and age-matched controls originally implicated cochlin as possibly contributing to glaucoma pathogenesis. Cochlin deposits were subsequently detected in glaucomatous but not in control TM and older glaucomatous TM was found to contain higher levels of cochlin and significantly lower amounts of collagen type II. More recently, similar results were reported in DBA/2J mice, which at older ages develop elevated IOP, retinal ganglion cell degeneration, and optic nerve damage. Notably, cochlin was absent in TM from C57BL/6J, CD1, and BALBc/ByJ mice, which do not exhibit elevated IOP or glaucoma. Cochlin was found in the TM of very young DBA/2J mice, prior to elevated IOP, suggesting that over time the protein may contribute to the events leading to increased IOP and optic nerve damage. Here we review these findings and describe how future studies in DBA/2J mice can help resolve whether cochlin plays a causal role in mechanisms of POAG and elevated IOP.

Type
Research Article
Copyright
© 2005 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Ahsan, M., Ohta, K., Kuriyama, S., & Tanaka, H. (2005). Novel soluble molecule, Akhirin, is expressed in the embryonic chick eyes and exhibits heterophilic cell-adhesion activity. Developmental Dynamics 233, 95104.CrossRefGoogle Scholar
Anderson, M.G., Smith, R.S., Hawes, N.L., Zabaleta, A., Chang, B., Wiggs, J.L., & John, S.W. (2002). Mutations in genes encoding melanosomal proteins cause pigmentary glaucoma in DBA/2J mice. Nature Genetics 30, 8185.CrossRefGoogle Scholar
Anderson, M.G., Smith, R.S., Savinova, O.V., Hawes, N.L., Chang, B., Zabaleta, A., Wilpan, R., Heckenlively, J.R., Davisson, M., & John, S.W. (2001). Genetic modification of glaucoma associated phenotypes between AKXD-28/Ty and DBA/2J mice. BMC Genetics 2, 1.CrossRefGoogle Scholar
Annangudi, S.P., Rockwood, E.J., Smith, S.D., Salomon, R.G., Bhattacharya, S.K. and Crabb, J.W. (2005). Oxidative protein modifications in glaucomatous trabecular meshwork. Investigative Ophthalmology and Visual Science 46, ARVO E-abstract 3694.Google Scholar
Bayer, A.U., Neuhardt, T., May, A.C., Martus, P., Maag, K.P., Brodie, S., Lutjen-Drecoll, E., Podos, S.M., & Mittag, T. (2001). Retinal morphology and ERG response in the DBA/2NNia mouse model of angle-closure glaucoma. Investigative Ophthalmology and Visual Science 42, 12581265.Google Scholar
Bhattacharya, S.K., Rockwood, E.J., Smith, S.D., Bonilha, V.L., Crabb, J.S., Kuchtey, R.W., Robertson, N.G., Peachey, N.S., Morton, C.C., & Crabb, J.W. (2005a). Proteomics reveals cochlin deposits associated with glaucomatous trabecular meshwork. Journal of Biological Chemistry 280, 60806084.Google Scholar
Bhattacharya, S.K., Annangudi, S.P., Salomon, R.G., Kuchtey, R.W., Peachey, N.S., & Crabb, J.W. (2005b). Cochlin deposits in the trabecular meshwork of the glaucomatous DBA/2J mouse. Experimental Eye Research 80, 741744.Google Scholar
Bishop, P.N., Takanosu, M., Le Goff, M., & Mayne, R. (2002). The role of the posterior ciliary body in the biosynthesis of vitreous humour. Eye 16, 454460.Google Scholar
Camarini, R. & Hodge, C.W. (2004). Ethanol preexposure increases ethanol self-administration in C57BL/6J and DBA/2J mice. Pharmacology, Biochemistry and Behavior 79, 623632.CrossRefGoogle Scholar
Chang, B., Smith, R.S., Hawes, N.L., Anderson, M.G., Zabaleta, A., Savinova, O., Roderick, T.H., Heckenlively, J.R., Davisson, M.T., & John, S.W. (1999). Interacting loci cause severe iris atrophy and glaucoma in DBA/2J mice. Nature Genetics 21, 405409.Google Scholar
Clark, H.F., Gurney, A.L., Abaya, E., Baker, K., Baldwin, D., Brush, J., Chen, J., Chow, B., Chui, C., Crowley, C., Currell, B., Deuel, B., Dowd, P., Eaton, D., Foster, J., Grimaldi, C., Gu, Q., Hass, P.E., Heldens, S., Huang, A., Kim, H.S., Klimowski, L., Jin, Y., Johnson, S., Lee, J., Lewis, L., Liao, D., Mark, M., Robbie, E., Sanchez, C., Schoenfield, J., Seshagiri, S., Simmons, L., Singh, J., Smith, V., Stinson, J., Vagts, A., Vandlen, R., Watanbe, C., Wieand, D., Woods, K., Xie, M.H., Yansura, D., Yi, S., Yu, G., Yuan, J., Zhang, M., Zhang, Z., Goddard, A., Wood, W.I., Godowski, I.P., & Gray, A. (2003). The secreted protein discovery initiative (SPDI), a large-scale effort to identify novel human secreted and transmembrane proteins: A bioinformatics assessment. Genome Research 13, 22652270.CrossRefGoogle Scholar
Colombatti, A., Bonaldo, P., & Doliana, R. (1993). Type A modules: interacting domains found in several non-fibrillar collagens and in other extracellular matrix proteins. Matrix 13, 297306.CrossRefGoogle Scholar
Crawley, J.N., Belknap, J.K., Collins, A., Crabbe, J.C., Frankel, W., Henderson, N., Hitzemann, R.J., Maxson, S.C., Miner, L.L., Silva, A.J., Wehner, J.M., Wynshaw-Boris, A., & Paylor, R. (1997). Behavioral phenotypes of inbred mouse strains: Implications and recommendations for molecular studies. Psychopharmacology (Berlin) 132, 107124.CrossRefGoogle Scholar
Danias, J., Lee, K.C., Zamora, M.F., Chen, B., Shen, F., Filippopoulos, T., Su, Y., Goldblum, D., Podos, S.M., & Mittag, T. (2003). Quantitative analysis of retinal ganglion cell (RGC) loss in aging DBA/2NNia glaucomatous mice: Comparison with RGC loss in aging C57/BL6 mice. Investigative Ophthalmology and Visual Science 44, 51515162.CrossRefGoogle Scholar
Dong, J.F., Moake, J.L., Bernardo, A., Fujikawa, K., Ball, C., Nolasco, L., Lopez, J.A., & Cruz, M.A. (2003). ADAMTS-13 metalloprotease interacts with the endothelial cell-derived ultra-large von Willebrand factor. Journal of Biological Chemistry 278, 2963329639.CrossRefGoogle Scholar
Eble, J.A. & Tuckwell, D.S. (2003). The alpha2beta1 integrin inhibitor rhodocetin binds to the A-domain of the integrin alpha2 subunit proximal to the collagen-binding site. Biochemical Journal 376, 7785.CrossRefGoogle Scholar
Festing, M.F.W. (1979). Inbred Strains in Biomedical Research. New York: Oxford University Press.CrossRef
Friedman, D.S., Wilson, M.R., Liebmann, J.M., Fechtner, R.D., & Weinreb, R.N. (2004). An evidence-based assessment of risk factors for the progression of ocular hypertension and glaucoma. American Journal of Ophthalmology 138, S19S31.CrossRefGoogle Scholar
Hartigan, N., Garrigue-Antar, L., & Kadler, K.E. (2003). Bone morphogenetic protein-1 (BMP-1). Identification of the minimal domain structure for procollagen C-proteinase activity. Journal of Biological Chemistry 278, 1804518049.CrossRefGoogle Scholar
Ikeda, Y., Murata, M., & Goto, S. (1997). Von Willebrand factor-dependent shear-induced platelet aggregation: Basic mechanisms and clinical implications. Annals of New York Academy of Sciences 811, 325336.CrossRefGoogle Scholar
Ikezono, T., Shindo, S., Li, L., Omori, A., Ichinose, S., Watanabe, A., Kobayashi, T., Pawankar, R., & Yagi, T. (2004). Identification of a novel Cochlin isoform in the perilymph: Insights to Cochlin function and the pathogenesis of DFNA9. Biochemical Biophysical Research Communication 314, 440446.CrossRefGoogle Scholar
Jeskey, J.E. & Willott, J.F. (2000). Modulation of prepulse inhibition by an augmented acoustic environment in DBA/2J mice. Behavioral Neuroscience 114, 991997.CrossRefGoogle Scholar
John, S.W., Hagaman, J.R., MacTaggart, T.E., Peng, L., & Smithes, O. (1997). Intraocular pressure in inbred mouse strains. Investigative Ophthalmology and Visual Science 38, 249253.Google Scholar
John, S.W., Smith, R.S., Savinova, O.V., Hawes, N.L., Chang, B., Turnbull, D., Davisson, M., Roderick, T.H., & Heckenlively, J.R. (1998). Essential iris atrophy, pigment dispersion, and glaucoma in DBA/2J mice. Investigative Ophthalmology and Visual Science 39, 951962.Google Scholar
Kamarinos, M., McGill, J., Lynch, M., & Dahl, H. (2001). Identification of a novel COCH mutation, I109N, highlights the similar clinical features observed in DFNA9 families. Human Mutation 17, 351.Google Scholar
Kaplan, F., Ledoux, P., Kassamali, F.Q., Gagnon, S., Post, M., Koehler, D., Deimling, J., & Sweezey, N.B. (1999). A novel developmentally regulated gene in lung mesenchyme: Homology to a tumor-derived trypsin inhibitor. American Journal of Physiology 276, L1027L1036.Google Scholar
Kimura, R.S. (1986). Animal models of inner ear vascular disturbances. American Journal of Otolaryngology 7, 132139.CrossRefGoogle Scholar
Kroll, M.H., Hellums, J.D., McIntire, L.V., Schafer, A.I., & Moake, J.L. (1996). Platelets and shear stress. Blood 88, 15251541.Google Scholar
Leighton, M. & Kadler, K.E. (2003). Paired basic/Furin-like proprotein convertase cleavage of Pro-BMP-1 in the trans-Golgi network. Journal of Biological Chemistry 278, 1847818484.CrossRefGoogle Scholar
Libby, R.T., Smith, R.S., Savinova, O.V., Zabaleta, A., Martin, J.E., Gonzalez, F.J., & John, S.W. (2003). Modification of ocular defects in mouse developmental glaucoma models by tyrosinase. Science 299, 15781581.CrossRefGoogle Scholar
Liepinsh, E., Trexler, M., Kaikkonen, A., Weigelt, J., Banyai, L., Patthy, L., & Otting, G. (2001). NMR structure of the LCCL domain and implications for DFNA9 deafness disorder. EMBO Journal 20, 53475353.CrossRefGoogle Scholar
Lutjen-Drecoll, E. (1999). Functional morphology of the trabecular meshwork in primate eyes. Progress in Retina and Eye Research 18, 91119.CrossRefGoogle Scholar
Lutjen-Drecoll, E. (2000). Importance of trabecular meshwork changes in the pathogenesis of primary open-angle glaucoma. Journal of Glaucoma 9, 417418.CrossRefGoogle Scholar
Lutjen-Drecoll, E., Shimizu, T., Rohrbach, M., & Rohen, J.W. (1986). Quantitative analysis of ‘plaque material’ between ciliary muscle tips in normal- and glaucomatous eyes. Experimental Eye Research 42, 457465.CrossRefGoogle Scholar
Mabuchi, F., Lindsey, J.D., Aihara, M., Mackey, M.R., & Weinreb, R.N. (2004). Optic nerve damage in mice with a targeted type I collagen mutation. Investigative Ophthalmology and Visual Science 45, 18411845.CrossRefGoogle Scholar
Marchant, J.K., Hahn, R.A., Linsenmayer, T.F., & Birk, D.E. (1996). Reduction of type V collagen using a dominant-negative strategy alters the regulation of fibrillogenesis and results in the loss of corneal-specific fibril morphology. Journal of Cell Biology 135, 14151426.CrossRefGoogle Scholar
Masliah, E. & Hashimoto, M. (2002). Development of new treatments for Parkinson's disease in transgenic animal models: A role for beta-synuclein. Neurotoxicology 23, 461468.CrossRefGoogle Scholar
McKinnon, S.J. (2003). Glaucoma: Ocular Alzheimer's disease? Frontiers in Biosciences 8, s1140s1156.Google Scholar
Mayne, R., Ren, Z.X., Liu, J., Cook, T., Carson, M., & Narayana, S. (1999). VIT-1: The second member of a new branch of the von Willebrand factor A domain superfamily. Biochemical Society Transactions 27, 832835.CrossRefGoogle Scholar
Morrison, J.C. & Acott, T.S. (2003). Anatomy and physiology of aqueous humor outflow. In Glaucoma—Science and Practice, ed. Morrison, J.C. & Pollack, I.P., pp. 3441. New York: Thieme Medical Publishers Inc.
Nakamura, T., Furunaka, H., Miyata, T., Tokunaga, F., Muta, T., Iwanaga, S., Niwa, M., Takao, T., & Shimonishi, Y. (1988a). Tachyplesin, a class of antimicrobial peptide from the hemocytes of the horseshoe crab (Tachypleus tridentatus). Isolation and chemical structure. Journal of Biological Chemistry 263, 1670916713.Google Scholar
Nakamura, T., Tokunaga, F., Morita, T., Iwanaga, S., Kusumoto, S., Shiba, T., Kobayashi, T., & Inoue, K. (1988b). Intracellular serine-protease zymogen, factor C, from horseshoe crab hemocytes. Its activation by synthetic lipid A analogues and acidic phospholipids. European Journal of Biochemistry 176, 8994.Google Scholar
O'Brien, J.R. & Salmon, G.P. (1987). Shear stress activation of platelet glycoprotein IIb/IIIa plus von Willebrand factor causes aggregation: Filter blockage and the long bleeding time in von Willebrand's disease. Blood 70, 13541361.Google Scholar
Pareti, F.I., Niiya, K., McPherson, J.M., & Ruggeri, Z.M. (1987). Isolation and characterization of two domains of human von Willebrand factor that interact with fibrillar collagen types I and III. Journal of Biological Chemistry 262, 1383513841.Google Scholar
Parisi, V. (2003). Correlation between morphological and functional retinal impairment in patients affected by ocular hypertension, glaucoma, demyelinating optic neuritis and Alzheimer's disease. Seminars in Ophthalmology 18, 5057.Google Scholar
Quigley, H.A. (1996). Number of people with glaucoma worldwide. British Journal of Ophthalmology 80, 389393.CrossRefGoogle Scholar
Robertson, N.G., Hamaker, S.A., Patriub, V., Aster, J.C., & Morton, C.C. (2003). Subcellular localisation, secretion, and post-translational processing of normal cochlin, and of mutants causing the sensorineural deafness and vestibular disorder, DFNA9. Journal of Medical Genetics 40, 479486.CrossRefGoogle Scholar
Robertson, N.G., Khetarpal, U., Gutierrez-Espeleta, G.A., Bieber, F.R., & Morton, C.C. (1994). Isolation of novel and known genes from a human fetal cochlear cDNA library using subtractive hybridization and differential screening. Genomics 23, 4250.CrossRefGoogle Scholar
Robertson, N.G., Lu, L., Heller, S., Merchant, S.N., Eavey, R.D., McKenna, M., Nadol, J.B., Jr., Miyamoto, R.T., Linthicum, F.H., Jr., Lubianca Neto, J.F., Hudspeth, A.J., Seidman, C.E., Morton, C.C., & Seidman, J.G. (1998). Mutations in a novel cochlear gene cause DFNA9, a human nonsyndromic deafness with vestibular dysfunction. Nature Genetics 20, 299303.Google Scholar
Robertson, N.G., Resendes, B.L., Lin, J.S., Lee, C., Aster, J.C., Adams, J.C., & Morton, C.C. (2001). Inner ear localization of mRNA and protein products of COCH, mutated in the sensorineural deafness and vestibular disorder, DFNA9. Human Molecular Genetics 10, 24932500.CrossRefGoogle Scholar
Rodriguez, C.I., Cheng, J.G., Liu, L., & Stewart, C.L. (2004). Cochlin, a secreted von Willebrand factor type a domain-containing factor, is regulated by leukemia inhibitory factor in the uterus at the time of embryo implantation. Endocrinology 145, 14101418.CrossRefGoogle Scholar
Ruggeri, Z.M., De Marco, L., Gatti, L., Bader, R., & Montgomery, R.R. (1983). Platelets have more than one binding site for von Willebrand factor. Journal of Clinical Investigation 72, 112.Google Scholar
Savinova, O.V., Sugiyama, F., Martin, J.E., Tomarev, S.I., Paigen, B.J., Smith, R.S., & John, S.W. (2001). Intraocular pressure in genetically distinct mice: An update and strain survey. BMC Genetics 2, 12.Google Scholar
Shankaran, H., Alexandridis, P., & Neelamegham, S. (2003). Aspects of hydrodynamic shear regulating shear-induced platelet activation and self-association of von Willebrand factor in suspension. Blood 101, 26372645.CrossRefGoogle Scholar
Tomarev, S.I. (2001). Eyeing a new route along an old pathway. Nature Medicine 7, 294295.CrossRefGoogle Scholar
Treadwell, J.A., Pagniello, K.B., & Singh, S.M. (2004). Genetic segregation of brain gene expression identifies retinaldehyde binding protein 1 and syntaxin 12 as potential contributors to ethanol preference in mice. Behavioral Genetics 34, 425439.CrossRefGoogle Scholar
Trexler, M., Banyai, L., & Patthy, L. (2000). The LCCL module. European Journal of Biochemistry 267, 57515757.CrossRefGoogle Scholar
Tuckwell, D. (1999). Evolution of von Willebrand factor A (VWA) domains. Biochemical Society Transactions 27, 835840.CrossRefGoogle Scholar
Ueda, J., Wentz-Hunter, K., & Yue, B.Y. (2002). Distribution of myocilin and extracellular matrix components in the juxtacanalicular tissue of human eyes. Investigative Ophthalmology and Visual Science 43, 10681076.Google Scholar
Vanhoorelbeke, K., Depraetere, H., Romijn, R.A., Huizinga, E.G., De Maeyer, M., & Deckmyn, H. (2003). A consensus tetrapeptide selected by phage display adopts the conformation of a dominant discontinuous epitope of a monoclonal anti-VWF antibody that inhibits the von Willebrand factor-collagen interaction. Journal of Biological Chemistry 278, 3781537821.CrossRefGoogle Scholar
Whittaker, C.A. & Hynes, R.O. (2002). Distribution and evolution of von Willebrand/integrin A domains: Widely dispersed domains with roles in cell adhesion and elsewhere. Molecular Biology of the Cell 13, 33693387.CrossRefGoogle Scholar
Willott, J.F. & Erway, L.C. (1998). Genetics of age-related hearing loss in mice. IV. Cochlear pathology and hearing loss in 25 BXD recombinant inbred mouse strains. Hearing Research 119, 2736.Google Scholar
Wilson, M.R. & Martone, J.F. (1996). Epidemiology of chronic open-angle glaucoma. In The Glaucomas, ed. Ritch, R., Shields, M.B. & Krupin, T., pp. 753768. St. Louis, Missouri: Mosby.