Histological and morphometric evaluation of transient retinal and optic nerve ischemia in rat

Brain Research

Volumn 1096, Issue 1, 2006, Pages 20-29

  Danylkova, Nataliya O ^a   Pomeranz, Howard D ^a   Alcala, Sandra R ^a   McLoon, Linda K ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Hypoxia; Ischemia; Optic nerve injury

Indexed keywords

ARGON; HYPOXIA INDUCIBLE FACTOR 1ALPHA; ROSE BENGAL;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD CLOTTING DISORDER; CELL DEGENERATION; COMPARATIVE STUDY; CONTROLLED STUDY; HISTOLOGY; ISCHEMIC OPTIC NEUROPATHY; LOW LEVEL LASER THERAPY; MORPHOLOGY; MORPHOMETRICS; NERVE CELL; NERVE FIBER; NONHUMAN; OPTIC DISK; PHYSIOLOGY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RAT; RETINA; RETINA ISCHEMIA; STAINING; UPREGULATION;

ANIMALS; AXONS; BIOLOGICAL MARKERS; BLOOD COAGULATION DISORDERS; CELL COUNT; CELL SURVIVAL; FLUORESCENT DYES; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; ISCHEMIA; LASERS; OPTIC NEUROPATHY, ISCHEMIC; RATS; RATS, LONG-EVANS; RETINA; RETINAL GANGLION CELLS; RETINAL VESSELS; ROSE BENGAL; SURVIVAL ANALYSIS; UP-REGULATION;

EID: 33747011155     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2006.04.061     Document Type: Article

References (62)

1. Adamec E., Yang F., Cole G.M., and Nixon R.A. Multiple-label immunocytochemistry for the evaluation of nature of cell death in experimental models of neurodegeneration. Brain Res. Brain Res. Protoc. 7 (2001) 193-202
2. Aviles-Trigueros M., Mayor-Torroglosa S., Garcia-Aviles A., Lafuente M.P., Rodriguez M.E., Miralles de Imperial J., Villegas-Perez M.P., and Vidal-Sanz M. Transient ischemia of the retina results in massive degeneration of the retinotectal projection: long-term neuroprotection with brimonidine. Exp. Neurol. 184 (2003) 767-777
3. Berkelaar M., Clarke D.B., Wang Y.C., Bray G.M., and Aguayo A.J. Axotomy results in delayed death and apoptosis of retinal ganglion cells in adult rats. J. Neurosci. 14 (1994) 4368-4374
4. Bernstein S.L., Guo Y., Kelman S.E., Flower R.W., and Johnson M.A. Functional and cellular responses in a novel rodent model of anterior ischemic optic neuropathy. Invest. Ophthalmol. Visual Sci. 44 (2003) 4153-4162
5. Carmeliet P., Dor Y., Herbert J.M., Fukumura D., Brusselmans K., Dewerchin M., Neeman M., Bono F., Abramovitch R., Maxwell P., Koch C.J., Ratcliffe P., Moons L., Jain R.K., Collen D., and Keshert E. Role of HIF-1alpha in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. Nature 394 (1998) 485-490
6. Chavez J.C., and LaManna J.C. Activation of hypoxia-inducible factor-1 in the rat cerebral cortex after transient global ischemia: potential role of insulin-like growth factor-1. J. Neurosci. 22 (2002) 8922-8931
7. Chen T.A., Yang F., Cole G.M., and Chan S.O. Inhibition of caspase 3 like activity decreases glutamate induced cell death in adult rat retina. Brain Res. 904 (2001) 177-188
8. Chun Y.S., Kim M.S., and Park J.W. Oxygen-dependent and -independent regulation of HIF-1alpha. J. Korean Med. Sci. 17 (2002) 581-588
9. Danylkova N., Pomeranz H.D., Sadeghi Y., Alcala S., and McLoon L.K. Neuroprotection by brimonidine in a rat model of anterior ischemic optic neuropathy. Invest. Ophthalmol. Visual Sci. 46 (2005) 668
10. Evans S.M., Joiner B., Jenkins W.T., Laughlin K.M., Lord E.M., and Koch C.J. Identification of hypoxia in cells and tissues of epigastric 9(L rat glioma using EF5 2-(2-nitro-1H-imidazol-1-yl)-N-(2,2,3,3,3,-pentafluoropropyl) acetamide. Br. J. Cancer 72 (1995) 822-875
11. Feldon S.E. Anterior ischemic optic neuropathy: trouble waiting to happen. Ophthalmology 106 (1999) 651-652
12. Forsythe J.A., Jiang B.H., Iyer N.V., Agani F., Leung S.W., Koos R.D., and Semenza G.L. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol. Cell. Biol. 16 (1996) 4604-4613
13. Gardiner T.A., Gibson D.S., de Gooyer T.E., de la Cruz V.F., McDonald D.M., and Stitt A.W. Inhibition of tumor necrosis factor-a improves physiological angiogenesis and reduces pathological neovascularization in ischemic retinopathy. Am. J. Pathol. 166 (2005) 637-644
14. Glueck C.J., Wang P., Bell H., Rangaraj V., and Goldenberg N. Nonarteritic anterior ischemic optic neuropathy: associations with homozygosity for the C677T methyenetetrahydrofolate reductase mutation. J. Lab. Clin. Med. 143 (2004) 184-192
15. Goda N., Ryan H.E., Khadivi B., McNulty W., Rickert R.C., and Johnson R.S. Hypoxia-inducible factor 1alpha is essential for cell cycle arrest during hypoxia. Mol. Cell. Biol. 23 (2003) 359-369
16. Goldenberg-Cohen N., Guo Y., Margolis F., Cohen Y., Miller N.R., and Bernstein S.L. Oligodendrocyte dysfunction after induction of experimental anterior optic nerve ischemia. Invest. Ophthalmol. Visual Sci. 46 (2005) 2716-2725
17. Grimm C., Wenzel A., Groszer M., Mayser H., Seeliger M., Samardzija M., Bauer C., Gassmann M., and Reme C.E. HIF-1-induced erythropoietin in the hypoxic retina protects against light-induced retinal degeneration. Nat. Med. 8 (2002) 718-724
18. Grozdanic S.D., Sakaguchi D.S., Kwon Y.H., Kardon R.H., and Sonea I.M. Functional characterization of retina and optic nerve after acute ocular ischemia in rats. Invest. Ophthalmol. Visual Sci. 44 (2003) 2597-2605
19. Halterman M.W., and Federoff H.J. HIF-1alpha and p53 promote hypoxia-induced delayed neuronal death in models of CNS ischemia. Exp. Neurol. 159 (1999) 65-72
20. Halterman M.W., Miller C.C., and Federoff H.J. Hypoxia-inducible factor-1alpha mediates hypoxia-induced delayed neuronal death that involves p53. J. Neurosci. 19 (1999) 6818-6824
21. Hattenhauer M.G., Leavitt J.A., Hodge D.O., Grill R., and Gray D.T. Incidence of nonarteritic anterior ischemic optic neuropathy. Am. J. Ophthalmol. 123 (1997) 103-107
22. Hayreh S.S. Inter-individual variation in blood supply of the optic nerve head. Its importance in various ischemic disorders of the optic nerve head, and glaucoma, low-tension glaucoma and allied disorders. Doc. Ophthalmol. 59 (1985) 217-246
23. Hayreh S.S. Acute ischemic disorders of the optic nerve: pathogenesis, clinical manifestations and management. Ophthalmol. Clin. North Am. 9 (1996) 407-442
24. Hayreh S.S. Posterior ciliary artery circulation in health and disease. Invest. Ophthalmol. Visual Sci. 45 (2004) 749-751
25. Hayreh S.S., Zimmerman M.B., Podhajski P., and Alward W.M. Nocturnal arterial hypotension and its role in optic nerve head and ocular ischemic disorders. Am. J. Ophthalmol. 117 (1994) 603-624
26. Hickman S.J., Miszkiel K.A., Plant G.T., and Miller D.H. The optic nerve sheath on MRI in acute optic neuritis. Neuroradiology 47 (2005) 51-55
27. Hirose F., Kiryu J., Miyamoto K., Nishijima K., Miyahara S., Katsuta H., Tamura H., and Honda Y. In vivo evaluation of retinal injury after transient ischemia in hypertensive rats. Hypertension 43 (2004) 1098-1102
28. Hofer S.O.P., Mitchell G.M., Penington A.J., Morrison W.A., RomeoMeeuw R., Keramidaris E., Palmer J., and Knight K.R. The use of pimonidazole to characterize hypoxia in the internal environment of an in vivo tissue engineering chamber. Br. J. Plast. Surg. 58 (2005) 1104-1114
29. 2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 7987-7992
30. Jacobson D.M., Vierkant R.A., and Belongia E.A. Nonarteritic anterior ischemic optic neuropathy. A case-control study of potential risk factors. Arch. Ophthalmol. 15 (1997) 1403-1407
31. Jewell U., Kvietikova I., Scheid A., Bauer C., Wenger R.H., and Gassmann M. Induction of HIF-1α in response to hypoxia is instantaneous. FASEB J. 15 (2001) 1312-1314
32. 2 tension. Am. J. Physiol. 271 (1996) C1172-C1180
33. Johnson L.N., and Arnold A.C. Incidence of nonarteritic and arteritic anterior ischemic optic neuropathy. Population-based study in the state of Missouri and Los Angeles County, California. J. Neuroophthalmol. 14 (1994) 38-44
34. Kusama Y., Bernier M., and Hearse D.J. Singlet oxygen-induced arrhythmias. Dose- and light-response studies for photoactivation of Rose Bengal in the rat heart. Circulation. 80 (1989) 1432-1448
35. Li B., Pang I.H., Barnes G., McLaughlin M., and Holt W. A new method and device to induce transient retinal ischemia in the rat. Curr. Eye Res. 24 (2002) 458-464
36. Loddick S.A., MacKenzie A., and Rothwell N.J. An ICE inhibitor, z-VAD-DCB attenuates ischemic brain damage in the rat. NeuroReport 7 (1996) 1465-1468
37. McCulley T.J., Lam B.L., and Feuer W.J. Nonarteritic anterior ischemic optic neuropathy and surgery of the anterior segment: temporal relationship analysis. Am. J. Ophthalmol. 136 (2003) 1171-1172
38. Miller G.R., and Smith J.L. Ischemic optic neuropathy. Am. J. Ophthalmol. 62 (1966) 103-115
39. Mosinger J.L., and Olney J.W. Photothrombosis-induced ischemic neuronal degeneration in the rat retina. Exp. Neurol. 105 (1989) 110-113
40. Newman N.J., Scherer R., Langenberg P., Kelman S., Feldon S., Kaufman D., and Dickersin K. Ischemic optic neuropathy decompression trial research group. The fellow eye in NAION: report from the ischemic optic neuropathy decompression trial follow-up study. Am. J. Ophthalmol. 134 (2002) 317-328
41. Nicholson D.W. Caspase structure, proteolytic substrates, and function during apoptotic cell death. Cell Death Differ. 6 (1999) 1028-1042
42. Olive P.L., Durand R.E., Raleigh J.A., Luo C., and Aquino-Parsons C. Comparison between the comet assay and pimonidazole binding for measuring tumour hypoxia. Br. J. Cancer 83 (2000) 1525-1531
43. Osborne N.N., Chidlow G., Layton C.J., Wood J.P., Casson R.J., and Melena J. Optic nerve and neuroprotection strategies. Eye 18 (2004) 1075-1084
44. Pomeranz H.D., Smith K.H., Hart W.M., and Egan R.A. Sildenafil-associated nonarteritic anterior ischemic optic neuropathy. Ophthalmology 109 (2002) 584-587
45. Raleigh J.A., Franko A.J., Koch C.J., and Born J.L. Binding of misonidazole to hypoxic cells in monolayer and spheroid culture. Br. J. Cancer 51 (1985) 229-235
46. Raleigh J.A., Chou S.C., Bono E.L., Thrall D.E., and Varia M.A. Semiquantitative immunohistochemical analysis for hypoxia in human tumors. Int. J. Radiat. Oncol. Biol. Phys. 49 (2001) 569-574
47. Rolfs A., Kvietikova I., Gassmann M., and Wenger R.H. Oxygen-regulated transferrin expression is mediated by hypoxia-inducible factor-1. J. Biol. Chem. 272 (1997) 20055-20562
48. Rossiter J.P., Anderson L.L., Yang F., and Cole G.M. Caspase-3 activation and caspase-like proteolytic activity in human perinatal hypoxic-ischemic brain injury. Acta Neuropathol. Berl. 103 (2002) 66-73
49. Ruscher K., Isaev N., Trendelenburg G., Weih M., Iurato L., Meisel A., and Dirnagl U. Induction of hypoxia inducible factor 1 by oxygen glucose deprivation is attenuated by hypoxic preconditioning in rat cultured neurons. Neurosci. Lett. 254 (1998) 117-120
50. Russelakis-Carneiro M., Silveira L.C., and Perry V.H. Factors affecting the survival of cat retinal ganglion cells after optic nerve injury. J. Neurocytol. 25 (1996) 393-402
51. Salceda S., and Caro J. Hypoxia-inducible factor 1alpha (HIF-1alpha) protein is rapidly degraded by the ubiquitin-proteasome system under normoxic conditions. Its stabilization by hypoxia depends on redox-induced changes. J. Biol. Chem. 72 (1997) 22642-22647
52. Samoszuk M.K., Walter J., and Mechetner E. Improved immunohistochemical method for detecting hypoxia gradients in mouse tissues and tumors. J. Histochem. Cytochem. 52 (2004) 837-839
53. Sievers J., Hausmann B., Unsicker K., and Berry M. Fibroblast growth factors promote the survival of adult rat retinal ganglion cells after transection of the optic nerve. Neurosci. Lett. 76 (1987) 157-162
54. Stevens W.D., Fortin T., and Pappas B.A. Retinal and optic nerve degeneration after chronic carotid ligation: time course and role of light exposure. Stroke 33 (2002) 1107-1112
55. Suurmeijer A.J., Van der Wijk J., van Veldhuisen D.J., Yang F., and Cole G.M. Fractin immunostaining for detection of apoptotic cells and apoptotic bodies in formalin-fixed and paraffin-embedded tissue. Lab. Invest. 79 (1999) 619-620
56. Tesser R.A., Niendor E.R., and Levin L.A. The morphology of an infarct in nonarteritic anterior ischemic optic neuropathy. Ophthalmology 110 (2003) 2031-2035
57. Tsujikawa A., Ogura Y., Hiroshiba N., Miyamoto K., Kiryu J., and Honda Y. In vivo evaluation of leukocyte dynamics in retinal ischemia/reperfusion injury. Invest. Ophthalmol. Visual Sci. 39 (1998) 793-800
58. Unoki K., and LaVail M.M. Protection of the rat retina from ischemic injury by brain-derived neurotrophic factor, ciliary neurotrophic factor and basic fibroblast growth factor. Invest. Ophthalmol. Visual Sci. 35 (1994) 907-915
59. Wangsa-Wirawan N.D., and Linsenmeier R.A. Retinal oxygen: fundamental and clinical aspects. Arch. Ophthalmol. 121 (2003) 547-557
60. Watson B.D., Dietrich W.D., Busto R., Wachtel M.S., and Ginsberg M.D. Induction of reproducible brain infarction by photochemically initiated thrombosis. Ann. Neurol. 7 (1985) 497-504
61. Wilson C.A., and Hatchell D.L. Photodynamic retinal vascular thrombosis. Rate and duration of vascular occlusion. Invest. Ophthalmol. Visual Sci. 32 (1991) 2357-2365
62. Yang F., Sun X., Beech W., Teter B., Wu S., Sigel J., Vinters H.V., and Frautschy S.A. Cole GM. Antibody to caspase-cleaved actin detects apoptosis in differentiated neuroblastoma and plaque-associated neurons and microglia in Alzheimer's disease. Am. J. Pathol. 152 (1998) 379-389