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Inherited glaucoma in DBA/2J mice: Pertinent disease features for studying the neurodegeneration

Published online by Cambridge University Press:  06 December 2005

RICHARD T. LIBBY
Affiliation:
The Jackson Laboratory, Bar Harbor
MICHAEL G. ANDERSON
Affiliation:
The Jackson Laboratory, Bar Harbor The Howard Hughes Medical Institute, Bar Harbor Current address of Michael G. Anderson: Department of Physiology and Biophysics. The University of Iowa, Iowa City, IA, 52242, USA
IOK-HOU PANG
Affiliation:
Alcon Research, Ltd. Ft. Worth
ZACHARY H. ROBINSON
Affiliation:
The Jackson Laboratory, Bar Harbor The Howard Hughes Medical Institute, Bar Harbor
OLGA V. SAVINOVA
Affiliation:
The Jackson Laboratory, Bar Harbor The Howard Hughes Medical Institute, Bar Harbor
I. MIHAI COSMA
Affiliation:
The Jackson Laboratory, Bar Harbor
AMY SNOW
Affiliation:
The Jackson Laboratory, Bar Harbor The Howard Hughes Medical Institute, Bar Harbor
LAWRISTON A. WILSON
Affiliation:
The Jackson Laboratory, Bar Harbor The Howard Hughes Medical Institute, Bar Harbor
RICHARD S. SMITH
Affiliation:
The Jackson Laboratory, Bar Harbor The Howard Hughes Medical Institute, Bar Harbor
ABBOT F. CLARK
Affiliation:
Alcon Research, Ltd. Ft. Worth
SIMON W.M. JOHN
Affiliation:
The Jackson Laboratory, Bar Harbor The Howard Hughes Medical Institute, Bar Harbor Department of Ophthalmology, Tufts University School of Medicine, Boston

Abstract

The glaucomas are neurodegenerative diseases involving death of retinal ganglion cells and optic nerve head excavation. A major risk factor for this neurodegeneration is a harmfully elevated intraocular pressure (IOP). Human glaucomas are typically complex, progressive diseases that are prevalent in the elderly. Family history and genetic factors are clearly important in human glaucoma. Mouse studies have proven helpful for investigating the genetic and mechanistic basis of complex diseases. We previously reported inherited, age-related progressive glaucoma in DBA/2J mice. Here, we report our updated findings from studying the disease in a large number of DBA/2J mice. The period when mice have elevated IOP extends from 6 months to 16 months, with 8–9 months representing an important transition to high IOP for many mice. Optic nerve degeneration follows IOP elevation, with the majority of optic nerves being severely damaged by 12 months of age. This information should help with the design of experiments, and we present the data in a manner that will be useful for future studies of retinal ganglion cell degeneration and optic neuropathy.

Type
Research Article
Copyright
© 2005 Cambridge University Press

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References

REFERENCES

AGIS Investigators. (2000). 7. The relationship between control of intraocular pressure and visual field deterioration. American Journal of Ophthalmology 130, 429440.Google Scholar
AGIS Investigators. (2002). 11. Risk factors for failure of trabeculectomy and argon laser trabeculoplasty. American Journal of Ophthalmology 134, 481498.Google Scholar
Aihara, M., Lindsey, J.D., & Weinreb, R.N. (2003). Experimental mouse ocular hypertension: establishment of the model. Investigative Ophthalmology and Visual Science 44, 43144320.CrossRefGoogle Scholar
Anderson, D.R. (1977). Is Ischemia the villain in glaucomatous cupping and atrophy? In Controversy in Ophthalmology, eds. Brockhurst, R.J., Boruchoff, S.A., Hutchinson, B.T. & Lessell, S., pp. 312319. Philadelphia: Saunders.
Anderson, D.R. (1999). Introductory comments on blood flow autoregulation in the optic nerve head and vascular risk factors in glaucoma. Survey of Ophthalmology 43 Suppl 1, S59.CrossRefGoogle Scholar
Anderson, D.R. & Hendrickson, A. (1974). Effect of intraocular pressure on rapid axoplasmic transport in monkey optic nerve. Investigative Ophthalmology 13, 771783.Google Scholar
Anderson, M.G., Libby, R.T., Gould, D.B., Smith, R.S., & John, S.W.M. (2005). High-dose Radiation with bone marrow transfer prevents neurodegeneration in an inherited glaucoma. Proceedings of the National Academy of Sciences of the U.S.A. 102, 45664571.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.M. (2001). Genetic modification of glaucoma associated phenotypes between AKXD-28/Ty and DBA/2J mice. BMC Genetics 2, 1. http://www.biomedcentral.com/1471-2156/1472/1471.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
Bonfoco, E., Krainc, D., Ankarcrona, M., Nicotera, P., & Lipton, S.A. (1995). Apoptosis and necrosis: Two distinct events induced, respectively, by mild and intense insults with N-methyl-D-aspartate or nitric oxide/superoxide in cortical cell cultures. Proceedings of the National Academy of Sciences of the U.S.A. 92, 71627166.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
Chew, S.J. (1996). Animal models of glaucoma. In The Glaucomas, vol. 1, ed. Ritch, R., Shields, M.B. & Krupin, T., pp. 5569. Boston: Massachusetts: Mosby-Year Book, Inc.
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
Garcia-Valenzuela, E., Shareef, S., Walsh, J., & Sharma, S.C. (1995). Programmed cell death of retinal ganglion cells during experimental glaucoma. Experimental Eye Research 61, 3344.CrossRefGoogle Scholar
Goldblum, D. & Mittag, T. (2002). Prospects for relevant glaucoma models with retinal ganglion cell damage in the rodent eye. Vision Research 42, 471478.CrossRefGoogle Scholar
Gross, R.L., Ji, J., Chang, P., Pennesi, M.E., Yang, Z., Zhang, J., & Wu, S.M. (2003). A mouse model of elevated intraocular pressure: retina and optic nerve findings. Transactions of the American Ophthalmological Society 101, 163169; discussion 169–171.Google Scholar
Heijl, A., Leske, M.C., Bengtsson, B., Hyman, L., & Hussein, M. (2002). Reduction of intraocular pressure and glaucoma progression: Results from the Early Manifest Glaucoma Trial. Archives of Ophthalmology 120, 12681279.CrossRefGoogle Scholar
Jampel, H.D., Nickells, R., & Zack, D.J. (1996). Glaucoma. In Principles and Practice of Medical Genetics, Vol. 2, ed. Rimoin, D.L., Connor, J.M. & Pyeritz, R.E., pp. 25052521. New York: Churchill Livingstone.
Jeon, C.J., Strettoi, E., & Masland, R.H. (1998). The major cell populations of the mouse retina. Journal of Neuroscience 18, 89368946.Google Scholar
John, S.W., Anderson, M.G., & Smith, R.S. (1999). Mouse genetics: a tool to help unlock the mechanisms of glaucoma. Journal of Glaucoma 8, 400412.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
John, S.W.M. (2005). Mechanistic insights to glaucoma provided by experimental genetics: The Cogan lecture. Investigative Ophthalmology and Visual Science 46, 26492661.Google Scholar
John, S.W.M. & Savinova, O.V. (2002). Intraocular pressure measurement in mice:technical aspects. In Systematic Evaluation of the Mouse Eye: Anatomy, Pathology and Biomethods, ed. Smith, R.S., John, S.W.M., Nishina, P.M. & Sundberg, J.P., pp. 313320. Boca Raton, Florida: CRC Press.
Johnson, E.C., Morrison, J.C., Farrell, S., Deppmeier, L., Moore, C.G., & McGinty, M.R. (1996). The effect of chronically elevated intraocular pressure on the rat optic nerve head extracellular matrix. Experimental Eye Research 62, 663674.Google Scholar
Kass, M.A., Heuer, D.K., Higginbotham, E.J., Johnson, C.A., Keltner, J.L., Miller, J.P., Parrish, R.K., II, Wilson, M.R., & Gordon, M.O. (2002). The ocular hypertension treatment study: A randomized trial determines that topical ocular hypotensive medication delays or prevents the onset of primary open-angle glaucoma. Archives of Ophthalmology 120, 701713; discussion 829–730.Google Scholar
Libby, R.T., Gould, D.B., Anderson, M.G., & John, S.W.M. (2005a). Complex genetics of glaucoma susceptibility. Annual Review of Genomics and Human Genetics 22, 1544.Google Scholar
Libby, R.T., Li, Y., Savinova, O.V., Barter, J., Smith, R.S., Nickells, R.W., & John, S.W.M. (2005b). Susceptibility to neurodegeneration in glaucoma is modified by Bax gene dosage. PLOS Genetics 1, e4.Google Scholar
Mabuchi, F., Aihara, M., Mackey, M.R., Lindsey, J.D., & Weinreb, R.N. (2003). Optic nerve damage in experimental mouse ocular hypertension. Investigative Ophthalmology and Visual Science 44, 43214330.Google Scholar
May, C.A. & Mittag, T. (2004). Neuronal nitric oxide synthase (nNOS) positive retinal amacrine cells are altered in the DBA/2NNia mouse, a murine model for angle-closure glaucoma. Journal of Glaucoma 13, 496499.Google Scholar
Mo, J.S., Anderson, M.G., Gregory, M., Smith, R.S., Savinova, O.V., Serreze, D.V., Ksander, B.R., Streilein, J.W., & John, S.W. (2003). By altering ocular immune privilege, bone marrow-derived cells pathogenically contribute to DBA/2J pigmentary glaucoma. Journal of Experimental Medicine 197, 13351344.Google Scholar
Morgan, J.E. (2000). Optic nerve head structure in glaucoma: astrocytes as mediators of axonal damage. Eye 14 (Pt. 3B), 437444.Google Scholar
Morrison, J.C., Dorman-Pease, M.E., Dunkelberger, G.R., & Quigley, H.A. (1990). Optic nerve head extracellular matrix in primary optic atrophy and experimental glaucoma. Archives of Ophthalmology 108, 10201024.Google Scholar
Osborne, N.N., Wood, J.P., Chidlow, G., Bae, J.H., Melena, J., & Nash, M.S. (1999). Ganglion cell death in glaucoma: What do we really know? British Journal of Ophthalmology 83, 980986.Google Scholar
Quigley, H.A. (1996). Number of people with glaucoma worldwide. British Journal of Ophthalmology 80, 389393.Google Scholar
Quigley, H.A. (1999). Neuronal death in glaucoma. Progress in Retinal Eye Research 18, 3957.Google Scholar
Ruberte, J., Ayuso, E., Navarro, M., Carretero, A., Nacher, V., Haurigot, V., George, M., Llombart, C., Casellas, A., Costa, C., Bosch, A., & Bosch, F. (2004). Increased ocular levels of IGF-1 in transgenic mice lead to diabetes-like eye disease. Journal of Clinical Investigation 113, 11491157.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
Schuettauf, F., Quinto, K., Naskar, R., & Zurakowski, D. (2002). Effects of anti-glaucoma medications on ganglion cell survival: The DBA/2J mouse model. Vision Research 42, 23332337.Google Scholar
Schuettauf, F., Rejdak, R., Walski, M., Frontczak-Baniewicz, M., Voelker, M., Blatsios, G., Shinoda, K., Zagorski, Z., Zrenner, E., & Grieb, P. (2004). Retinal neurodegeneration in the DBA/2J mouse-a model for ocular hypertension. Acta Neuropathology (Berlin) 107, 352358.Google Scholar
Sheffield, V.C., Alward, W.L., & Stone, E.M. (2001). The glaucomas. In The Metabolic and Molecular Bases of Inherited Disease, ed. Scriver, C.R., Beaudet, A.L., Sly, S.S. & Valle, D., pp. 60636073. New York: McGraw-Hill.
Sheldon, W.G., Warbritton, A.R., Bucci, T.J., & Turturro, A. (1995). Glaucoma in food-restricted and ad libitum-fed DBA/2NNia mice. Laboratory Animal Science 45, 508518.Google Scholar
Smith, R.S., Zabaleta, A., & John, S.W.M. (2002). Light microscopy. In Systematic Evaluation of the Mouse Eye: Anatomy, Pathology and Biomethods, ed. Smith, R.S., John, S.W.M., Nishina, P.M. & Sundberg, J.P., pp. 266271. Boca Raton, Florida: CRC Press.
Stone, J. (1981). The Wholemount Handbook. Sydney, Australia: Maitland Publishing, Ltd.
Tezel, G. & Wax, M.B. (2000). Increased production of tumor necrosis factor-alpha by glial cells exposed to simulated ischemia or elevated hydrostatic pressure induces apoptosis in cocultured retinal ganglion cells. Journal of Neuroscience 20, 86938700.Google Scholar
The Collaborative Normal-Tension Glaucoma Study Group. (1998). The effectiveness of intraocular pressure reduction in the treatment of normal-tension glaucoma. American Journal of Ophthalmology 126, 498505.Google Scholar
Thylefors, B. & Negrel, A.D. (1994). The global impact of glaucoma. Bulletin of the World Health Organization 72, 323326.Google Scholar
Ueda, J., Sawaguchi, S., Hanyu, T., Yaoeda, K., Fukuchi, T., Abe, H., & Ozawa, H. (1998). Experimental glaucoma model in the rat induced by laser trabecular photocoagulation after an intracameral injection of India ink. Japanese Journal of Ophthalmology 42, 337344.Google Scholar
van Lookeren Campagne, M., Lucassen, P.J., Vermeulen, J.P., & Balazs, R. (1995). NMDA and kainate induce internucleosomal DNA cleavage associated with both apoptotic and necrotic cell death in the neonatal rat brain. European Journal of Neuroscience 7, 16271640.Google Scholar
Vorwerk, C.K., Gorla, M.S., & Dreyer, E.B. (1999). An experimental basis for implicating excitotoxicity in glaucomatous optic neuropathy. Surv Ophthalmol 43, Suppl 1, S142150.Google Scholar
Yoles, E., Muller, S., & Schwartz, M. (1997). NMDA-receptor antagonist protects neurons from secondary degeneration after partial optic nerve crush. Journal of Neurotrauma 14, 665675.Google Scholar