Glial coverage in the optic nerve expands in proportion to optic axon loss in chronic mouse glaucoma

Experimental Eye Research

Volumn 150, Issue , 2016, Pages 34-43

  Bosco, Alejandra ^a   Breen, Kevin T ^a   Anderson, Sarah R ^a   Steele, Michael R ^a   Calkins, David J ^b   Vetter, Monica L ^a  

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

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Axon loss; Glaucoma; Gliosis; Microglia; Neurodegeneration; Optic nerve; Remodeling; Segmentation

Indexed keywords

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; CELL AGGREGATION; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE COURSE; FEMALE; GLAUCOMA; GLIA CELL; HYPERTROPHY; MALE; MICROGLIA; MOUSE; NERVE FIBER DEGENERATION; NONHUMAN; OLIGODENDROGLIA; OPTIC NERVE DISEASE; PRIORITY JOURNAL; SCAR; TISSUE STRUCTURE; ANIMAL; AXON; CHRONIC DISEASE; COMPLICATION; CONFOCAL MICROSCOPY; DBA MOUSE; DISEASE MODEL; GLIA; GLIOSIS; MICROPHOTOGRAPHY; OPTIC NERVE; OPTIC NERVE DISEASES; PATHOLOGY; RETINA GANGLION CELL;

ANIMALS; ASTROCYTES; AXONS; CHRONIC DISEASE; DISEASE MODELS, ANIMAL; FEMALE; GLAUCOMA; GLIOSIS; MALE; MICE; MICE, INBRED DBA; MICROSCOPY, CONFOCAL; NEUROGLIA; OPTIC NERVE; OPTIC NERVE DISEASES; PHOTOMICROGRAPHY; RETINAL GANGLION CELLS;

EID: 84957664105     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2016.01.014     Document Type: Article

References (72)

1. Anderson, M.G., Libby, R.T., Gould, D.B., Smith, R.S., John, S.W., High-dose radiation with bone marrow transfer prevents neurodegeneration in an inherited glaucoma. Proc. Natl. Acad. Sci. U. S. A. 102 (2005), 4566–4571.
2. Bosco, A., Romero, C.O., Breen, K.T., Chagovetz, A.A., Steele, M.R., Ambati, B.K., Vetter, M.L., Neurodegeneration severity can be predicted from early microglia alterations monitored in vivo in a mouse model of chronic glaucoma. Dis. Model Mech. 8 (2015), 443–455.
3. Bosco, A., Steele, M.R., Vetter, M.L., Early microglia activation in a mouse model of chronic glaucoma. J. Comp. Neurol. 519 (2011), 599–620.
4. Buckingham, B.P., Inman, D.M., Lambert, W., Oglesby, E., Calkins, D.J., Steele, M.R., Vetter, M.L., Marsh-Armstrong, N., Horner, P.J., Progressive ganglion cell degeneration precedes neuronal loss in a mouse model of glaucoma. J. Neurosci. Off. J. Soc. Neurosci. 28 (2008), 2735–2744.
5. Buffo, A., Vosko, M.R., Erturk, D., Hamann, G.F., Jucker, M., Rowitch, D., Gotz, M., Expression pattern of the transcription factor Olig2 in response to brain injuries: implications for neuronal repair. Proc. Natl. Acad. Sci. U. S. A. 102 (2005), 18183–18188.
6. Burda, J.E., Sofroniew, M.V., Reactive gliosis and the multicellular response to CNS damage and disease. Neuron 81 (2014), 229–248.
7. Calkins, D.J., Critical pathogenic events underlying progression of neurodegeneration in glaucoma. Prog. Retin. Eye Res. 31 (2012), 702–719.
8. Calkins, D.J., Sappington, R.M., Hendry, S.H., Morphological identification of ganglion cells expressing the alpha subunit of type II calmodulin-dependent protein kinase in the macaque retina. J. Comp. Neurol. 481 (2005), 194–209.
9. Cassiani-Ingoni, R., Coksaygan, T., Xue, H., Reichert-Scrivner, S.A., Wiendl, H., Rao, M.S., Magnus, T., Cytoplasmic translocation of Olig2 in adult glial progenitors marks the generation of reactive astrocytes following autoimmune inflammation. Exp. Neurol. 201 (2006), 349–358.
10. Casson, R.J., Chidlow, G., Wood, J.P., Crowston, J.G., Goldberg, I., Definition of glaucoma: clinical and experimental concepts. Clin. Exp. Ophthalmol. 40 (2012), 341–349.
11. Chauhan, B.C., Levatte, T.L., Garnier, K.L., Tremblay, F., Pang, I.H., Clark, A.F., Archibald, M.L., Semiquantitative optic nerve grading scheme for determining axonal loss in experimental optic neuropathy. Investig. Ophthalmol. Vis. Sci. 47 (2006), 634–640.
12. Chen, H., Wei, X., Cho, K.S., Chen, G., Sappington, R., Calkins, D.J., Chen, D.F., Optic neuropathy due to microbead-induced elevated intraocular pressure in the mouse. Investig. Ophthalmol. Vis. Sci. 52 (2011), 36–44.
13. Chen, Y., Miles, D.K., Hoang, T., Shi, J., Hurlock, E., Kernie, S.G., Lu, Q.R., The basic helix-loop-helix transcription factor olig2 is critical for reactive astrocyte proliferation after cortical injury. J. Neurosci. Off. J. Soc. Neurosci. 28 (2008), 10983–10989.
14. Chidlow, G., Ebneter, A., Wood, J.P., Casson, R.J., The optic nerve head is the site of axonal transport disruption, axonal cytoskeleton damage and putative axonal regeneration failure in a rat model of glaucoma. Acta neuropathol. 121 (2011), 737–751.
15. Cooper, M.L., Crish, S.D., Inman, D.M., Horner, P.J., Calkins, D.J., Early astrocyte redistribution in the optic nerve precedes axonopathy in the DBA/2J mouse model of glaucoma. Exp Eye Res. 150 (2016 Dec 2), 22–33.
16. Crish, S.D., Sappington, R.M., Inman, D.M., Horner, P.J., Calkins, D.J., Distal axonopathy with structural persistence in glaucomatous neurodegeneration. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 5196–5201.
17. Dai, C., Khaw, P.T., Yin, Z.Q., Li, D., Raisman, G., Li, Y., Structural basis of glaucoma: the fortified astrocytes of the optic nerve head are the target of raised intraocular pressure. Glia 60 (2012), 13–28.
18. Ebneter, A., Casson, R.J., Wood, J.P., Chidlow, G., Microglial activation in the visual pathway in experimental glaucoma: spatiotemporal characterization and correlation with axonal injury. Investig. Ophthalmol. Vis. Sci. 51 (2010), 6448–6460.
19. Ebneter, A., Casson, R.J., Wood, J.P., Chidlow, G., Estimation of axon counts in a rat model of glaucoma: comparison of fixed-pattern sampling with targeted sampling. Clin. Exp. Ophthalmol. 40 (2012), 626–633.
20. Gottanka, J., Kuhlmann, A., Scholz, M., Johnson, D.H., Lutjen-Drecoll, E., Pathophysiologic changes in the optic nerves of eyes with primary open angle and pseudoexfoliation glaucoma. Investig. Ophthalmol. Vis. Sci. 46 (2005), 4170–4181.
21. Harder, J.M., Fernandes, K.A., Libby, R.T., The Bcl-2 family member BIM has multiple glaucoma-relevant functions in DBA/2J mice. Sci. Rep., 2, 2012, 530.
22. Hernandez, M.R., The optic nerve head in glaucoma: role of astrocytes in tissue remodeling. Prog. Retin. Eye Res. 19 (2000), 297–321.
23. Howell, G.R., Libby, R.T., Jakobs, T.C., Smith, R.S., Phalan, F.C., Barter, J.W., Barbay, J.M., Marchant, J.K., Mahesh, N., Porciatti, V., Whitmore, A.V., Masland, R.H., John, S.W., Axons of retinal ganglion cells are insulted in the optic nerve early in DBA/2J glaucoma. J. Cell Biol. 179 (2007), 1523–1537.
24. Howell, G.R., Libby, R.T., Marchant, J.K., Wilson, L.A., Cosma, I.M., Smith, R.S., Anderson, M.G., John, S.W., Absence of glaucoma in DBA/2J mice homozygous for wild-type versions of Gpnmb and Tyrp1. BMC Genet., 8, 2007, 45.
25. Howell, G.R., Macalinao, D.G., Sousa, G.L., Walden, M., Soto, I., Kneeland, S.C., Barbay, J.M., King, B.L., Marchant, J.K., Hibbs, M., Stevens, B., Barres, B.A., Clark, A.F., Libby, R.T., John, S.W., Molecular clustering identifies complement and endothelin induction as early events in a mouse model of glaucoma. J. Clin. Investig. 121 (2011), 1429–1444.
26. Howell, G.R., Soto, I., Zhu, X., Ryan, M., Macalinao, D.G., Sousa, G.L., Caddle, L.B., MacNicoll, K.H., Barbay, J.M., Porciatti, V., Anderson, M.G., Smith, R.S., Clark, A.F., Libby, R.T., John, S.W., Radiation treatment inhibits monocyte entry into the optic nerve head and prevents neuronal damage in a mouse model of glaucoma. J. Clin. Investig. 122 (2012), 1246–1261.
27. Inman, D.M., Horner, P.J., Reactive nonproliferative gliosis predominates in a chronic mouse model of glaucoma. Glia 55 (2007), 942–953.
28. Inman, D.M., Lupien, C.B., Horner, P.J., Manipulating glia to protect retinal ganglion cells in glaucoma. Gunvant, P., (eds.) Glaucoma – Current Clinical Research Aspects, 2011, InTech, Rijeka, Croatia 978-953-307-263-0.
29. Inman, D.M., Sappington, R.M., Horner, P.J., Calkins, D.J., Quantitative correlation of optic nerve pathology with ocular pressure and corneal thickness in the DBA/2 mouse model of glaucoma. Investig. Ophthalmol. Vis. Sci. 47 (2006), 986–996.
30. Isaacs, J., Mallu, S., Batchelor, M., Modification of commercially available image analysis software for semi-automated qualitative analysis of axon regeneration and myelination in the rat sciatic nerve. J. Neurosci. Methods 233 (2014), 45–49.
31. Jia, L., Cepurna, W.O., Johnson, E.C., Morrison, J.C., Patterns of intraocular pressure elevation after aqueous humor outflow obstruction in rats. Investig. Ophthalmol. Vis. Sci. 41 (2000), 1380–1385.
32. John, S.W., Smith, R.S., Savinova, O.V., Hawes, N.L., Chang, B., Turnbull, D., Davisson, M., Roderick, T.H., Heckenlively, J.R., Essential iris atrophy, pigment dispersion, and glaucoma in DBA/2J mice. Investig. Ophthalmol. Vis. Sci. 39 (1998), 951–962.
33. Johnson, E.C., Jia, L., Cepurna, W.O., Doser, T.A., Morrison, J.C., Global changes in optic nerve head gene expression after exposure to elevated intraocular pressure in a rat glaucoma model. Investig. Ophthalmol. Vis. Sci. 48 (2007), 3161–3177.
34. Jonas, J.B., Schmidt, A.M., Muller-Bergh, J.A., Naumann, G.O., Optic nerve fiber count and diameter of the retrobulbar optic nerve in normal and glaucomatous eyes. Graefes Arch. Clin. Exp. Ophthalmol. 233 (1995), 421–424.
35. Joos, K.M., Li, C., Sappington, R.M., Morphometric changes in the rat optic nerve following short-term intermittent elevations in intraocular pressure. Investig. Ophthalmol. Vis. Sci. 51 (2010), 6431–6440.
36. Libby, R.T., Anderson, M.G., Pang, I.H., Robinson, Z.H., Savinova, O.V., Cosma, I.M., Snow, A., Wilson, L.A., Smith, R.S., Clark, A.F., John, S.W., Inherited glaucoma in DBA/2J mice: pertinent disease features for studying the neurodegeneration. Vis. Neurosci. 22 (2005), 637–648.
37. Libby, R.T., Li, Y., Savinova, O.V., Barter, J., Smith, R.S., Nickells, R.W., John, S.W., Susceptibility to neurodegeneration in a glaucoma is modified by Bax gene dosage. PLoS Genet. 1 (2005), 17–26.
38. Lye-Barthel, M., Sun, D., Jakobs, T.C., Morphology of astrocytes in a glaucomatous optic nerve. Investig. Ophthalmol. Vis. Sci. 54 (2013), 909–917.
39. Mabuchi, F., Aihara, M., Mackey, M.R., Lindsey, J.D., Weinreb, R.N., Optic nerve damage in experimental mouse ocular hypertension. Investig. Ophthalmol. Vis. Sci. 44 (2003), 4321–4330.
40. Magnus, T., Coksaygan, T., Korn, T., Xue, H., Arumugam, T.V., Mughal, M.R., Eckley, D.M., Tang, S.C., Detolla, L., Rao, M.S., Cassiani-Ingoni, R., Mattson, M.P., Evidence that nucleocytoplasmic Olig2 translocation mediates brain-injury-induced differentiation of glial precursors to astrocytes. J. Neurosci. Res. 85 (2007), 2126–2137.
41. Marina, N., Bull, N.D., Martin, K.R., A semiautomated targeted sampling method to assess optic nerve axonal loss in a rat model of glaucoma. Nat. Protoc. 5 (2010), 1642–1651.
42. May, C.A., Mittag, T., Optic nerve degeneration in the DBA/2NNia mouse: is the lamina cribrosa important in the development of glaucomatous optic neuropathy?. Acta Neuropathol. 111 (2006), 158–167.
43. Morrison, J.C., Moore, C.G., Deppmeier, L.M., Gold, B.G., Meshul, C.K., Johnson, E.C., A rat model of chronic pressure-induced optic nerve damage. Exp. Eye Res. 64 (1997), 85–96.
44. Nakazawa, T., Nakazawa, C., Matsubara, A., Noda, K., Hisatomi, T., She, H., Michaud, N., Hafezi-Moghadam, A., Miller, J.W., Benowitz, L.I., Tumor necrosis factor-alpha mediates oligodendrocyte death and delayed retinal ganglion cell loss in a mouse model of glaucoma. J. Neurosci. Off. J. Soc. Neurosci. 26 (2006), 12633–12641.
45. Naskar, R., Wissing, M., Thanos, S., Detection of early neuron degeneration and accompanying microglial responses in the retina of a rat model of glaucoma. Investig. Ophthalmol. Vis. Sci. 43 (2002), 2962–2968.
46. Nickells, R.W., Howell, G.R., Soto, I., John, S.W., Under pressure: cellular and molecular responses during glaucoma, a common neurodegeneration with axonopathy. Annu. Rev. Neurosci. 35 (2012), 153–179.
47. Nuschke, A.C., Farrell, S.R., Levesque, J.M., Chauhan, B.C., Assessment of retinal ganglion cell damage in glaucomatous optic neuropathy: axon transport, injury and soma loss. Exp. Eye Res. 141 (2015), 111–124.
48. Pelzel, H.R., Schlamp, C.L., Waclawski, M., Shaw, M.K., Nickells, R.W., Silencing of Fem1cR3 gene expression in the DBA/2J mouse precedes retinal ganglion cell death and is associated with histone deacetylase activity. Investig. Ophthalmol. Vis. Sci. 53 (2012), 1428–1435.
49. Qu, J., Jakobs, T.C., The time course of gene expression during reactive gliosis in the optic nerve. PloS One, 8, 2013, e67094.
50. Quigley, H.A., Glaucoma. Lancet 377 (2011), 1367–1377.
51. Quigley, H.A., Addicks, E.M., Green, W.R., Optic nerve damage in human glaucoma. III. Quantitative correlation of nerve fiber loss and visual field defect in glaucoma, ischemic neuropathy, papilledema, and toxic neuropathy. Arch. Ophthalmol. 100 (1982), 135–146.
52. Radius, R.L., Pederson, J.E., Laser-induced primate glaucoma. II. Histopathology. Arch. Ophthalmol. 102 (1984), 1693–1698.
53. Reynaud, J., Cull, G., Wang, L., Fortune, B., Gardiner, S., Burgoyne, C.F., Cioffi, G.A., Automated Quantification of Optic Nerve Axons in Primate Glaucomatous and Normal Eyes–method and Comparison to Semi-Automated Manual Quantification. 2012.
54. Salinas-Navarro, M., Alarcon-Martinez, L., Valiente-Soriano, F.J., Jimenez-Lopez, M., Mayor-Torroglosa, S., Aviles-Trigueros, M., Villegas-Perez, M.P., Vidal-Sanz, M., Ocular hypertension impairs optic nerve axonal transport leading to progressive retinal ganglion cell degeneration. Exp. Eye Res. 90 (2010), 168–183.
55. Sandell, J.H., Peters, A., Effects of age on the glial cells in the rhesus monkey optic nerve. J. Comp. Neurol. 445 (2002), 13–28.
56. Sappington, R.M., Carlson, B.J., Crish, S.D., Calkins, D.J., The microbead occlusion model: a paradigm for induced ocular hypertension in rats and mice. Investig. Ophthalmol. Vis. Sci. 51 (2010), 207–216.
57. Sappington, R.M., Pearce, D.A., Calkins, D.J., Optic nerve degeneration in a murine model of juvenile ceroid lipofuscinosis. Investig. Ophthalmol. Vis. Sci. 44 (2003), 3725–3731.
58. Schlamp, C.L., Li, Y., Dietz, J.A., Janssen, K.T., Nickells, R.W., Progressive ganglion cell loss and optic nerve degeneration in DBA/2J mice is variable and asymmetric. BMC Neurosci., 7, 2006, 66.
59. Scholz, M., Buder, T., Seeber, S., Adamek, E., Becker, C.M., Lutjen-Drecoll, E., Dependency of intraocular pressure elevation and glaucomatous changes in DBA/2J and DBA/2J-Rj mice. Investig. Ophthalmol. Vis. Sci. 49 (2008), 613–621.
60. Schuettauf, F., Rejdak, R., Walski, M., Frontczak-Baniewicz, M., Voelker, M., Blatsios, G., Shinoda, K., Zagorski, Z., Zrenner, E., Grieb, P., Retinal neurodegeneration in the DBA/2J mouse-a model for ocular hypertension. Acta neuropathol. 107 (2004), 352–358.
61. Smith, R.S., Zabaleta, A., John, S.W., Bechtold, L.S., Ikeda, S., Relyea, M., Sundberg, J., Liu, C.-Y., Kao, W., General and specific histopathology. Smith, R.S., (eds.) Systemic Evaluation of the Mouse Eye, 2002, CRC Press, New York, 265–297.
62. Sofroniew, M.V., Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci. 32 (2009), 638–647.
63. Son, J.L., Soto, I., Oglesby, E., Lopez-Roca, T., Pease, M.E., Quigley, H.A., Marsh-Armstrong, N., Glaucomatous optic nerve injury involves early astrocyte reactivity and late oligodendrocyte loss. Glia 58 (2010), 780–789.
64. Soto, I., Oglesby, E., Buckingham, B.P., Son, J.L., Roberson, E.D., Steele, M.R., Inman, D.M., Vetter, M.L., Horner, P.J., Marsh-Armstrong, N., Retinal ganglion cells downregulate gene expression and lose their axons within the optic nerve head in a mouse glaucoma model. J. Neurosci. Off. J. Soc. Neurosci. 28 (2008), 548–561.
65. Soto, I., Pease, M.E., Son, J.L., Shi, X., Quigley, H.A., Marsh-Armstrong, N., Retinal ganglion cell loss in a rat ocular hypertension model is sectorial and involves early optic nerve axon loss. Investig. Ophthalmol. Vis. Sci. 52 (2011), 434–441.
66. Sun, D., Jakobs, T.C., Structural remodeling of astrocytes in the injured CNS. Neurosci. Rev. J. Bring. Neurobiol. Neurol. Psychiatr. 18 (2012), 567–588.
67. Sun, D., Lye-Barthel, M., Masland, R.H., Jakobs, T.C., The morphology and spatial arrangement of astrocytes in the optic nerve head of the mouse. J. Comp. Neurol. 516 (2009), 1–19.
68. Teixeira, L.B., Buhr, K.A., Bowie, O., Duke, F.D., Nork, T.M., Dubielzig, R.R., McLellan, G.J., Quantifying optic nerve axons in a cat glaucoma model by a semi-automated targeted counting method. Mol. Vis. 20 (2014), 376–385.
69. Templeton, J.P., Struebing, F.L., Lemmon, A., Geisert, E.E., ImagePAD, a novel counting application for the Apple iPad, used to quantify axons in the mouse optic nerve. Exp. Eye Res. 128 (2014), 102–108.
70. Verkhratsky, A., Parpura, V., Pekna, M., Pekny, M., Sofroniew, M., Glia in the pathogenesis of neurodegenerative diseases. Biochem. Soc. Trans. 42 (2014), 1291–1301.
71. Vidal-Sanz, M., Salinas-Navarro, M., Nadal-Nicolas, F.M., Alarcon-Martinez, L., Valiente-Soriano, F.J., de Imperial, J.M., Aviles-Trigueros, M., Agudo-Barriuso, M., Villegas-Perez, M.P., Understanding glaucomatous damage: anatomical and functional data from ocular hypertensive rodent retinas. Prog. Retin. Eye Res. 31 (2012), 1–27.
72. Yang, Q., Cho, K.S., Chen, H., Yu, D., Wang, W.H., Luo, G., Pang, I.H., Guo, W., Chen, D.F., Microbead-induced ocular hypertensive mouse model for screening and testing of aqueous production suppressants for glaucoma. Investig. Ophthalmol. Vis. Sci. 53 (2012), 3733–3741.