Survey of Ophthalmology
Volume 45 , Pages S277-S283 , May 2001

Maintaining Mitochondrial Membrane Impermeability: An Opportunity for New Therapy in Glaucoma?

  • William G Tatton, MD, PhD

      Affiliations

    • Departments of Ophthalmology, Mount Sinai School of Medicine, New York, NY, USA
    • Departments of Neurology, Mount Sinai School of Medicine, New York, NY, USA
    • Corresponding Author InformationReprint address: Dr. William G. Tatton, Department of Neurology, Annenberg 14-70, Mount Sinai Medical Center, One Gustave L. Levy Place, New York, New York 10029.
    • ,
  • Ruth M.E Chalmers-Redman, PhD

      Affiliations

    • Departments of Neurology, Mount Sinai School of Medicine, New York, NY, USA
    • ,
  • Ajay Sud

      Affiliations

    • The School of Pharmacy, University of London, London, England, UK
    • ,
  • Steven M Podos, MD

      Affiliations

    • Departments of Ophthalmology, Mount Sinai School of Medicine, New York, NY, USA
    • ,
  • Thomas W Mittag, PhD

      Affiliations

    • Departments of Ophthalmology, Mount Sinai School of Medicine, New York, NY, USA

References 

  1. Ankarcrona M, Dypbukt JM, Bonfoco E, et al.  Glutamate-induced neuronal death (a succession of necrosis or apoptosis depending on mitochondrial function). Neuron. 1995;15:961–973
  2. Antonawich FJ. Translocation of cytochrome C following transient global ischemia in the gerbil. Neurosci Lett. 1999;274:123–126
  3. Bernardi P, Colonna R, Costantini P, et al.  The mitochondrial permeability transition. Biofactors. 1998;8:273–281
  4. Bernardi P, Scorrano L, Colonna R, et al.  Mitochondria and cell death. Mechanistic aspects and methodological issues. Eur J Biochem. 1999;264:687–701
  5. Bratton SB, MacFarlane M, Cain K, Cohen GM. Protein complexes activate distinct caspase cascades in death receptor and stress-induced apoptosis. Exp Cell Res. 2000;256:27–33
  6. Brenner C, Cadiou H, Vieira HL, et al.  Bcl-2 and Bax regulate the channel activity of the mitochondrial adenine nucleotide translocator. Oncogene. 2000;19:329–336
  7. Brenner C, Kroemer G. Apoptosis. Mitochondria—the death signal integrators. Science. 2000;289:1150–1151
  8. Bruce AJ, Boling W, Kindy MS, et al.  Altered neuronal and microglial responses to excitotoxic and ischemic brain injury in mice lacking TNF receptors. Nat Med. 1996;2:788–794
  9. Budd SL. Mechanisms of neuronal damage in brain hypoxia/ischemia (focus on the role of mitochondrial calcium accumulation). Pharmacol Ther. 1998;80:203–229
  10. Burren CP, Berka JL, Edmondson SR, et al.  Localization of mRNAs for insulin-like growth factor-I (IGF-I), IGF-I receptor, and IGF binding proteins in rat eye. Invest Ophthalmol Vis Sci. 1996;37:1459–1468
  11. Buys YM, Trope GE, Tatton WG. Deprenyl increases the survival of rat retinal ganglion cells after optic nerve crush. Curr Eye Res. 1995;14:119–126
  12. Casaccia-Bonnefil P, Gu C, Chao MV. Neurotrophins in cell survival/death decisions. Adv Exp Med Biol. 1999;468:275–282
  13. Chalmers-Redman RM, Fraser AD, Carlile GW, et al.  Glucose protection from MPP+-induced apoptosis depends on mitochondrial membrane potential and ATP synthase. Biochem Biophys Res Commun. 1999;257:440–447
  14. Cioffi GA, Wang L. Optic nerve blood flow in glaucoma. Semin Ophthalmol. 1999;14:164–170
  15. Crompton M. The mitochondrial permeability transition pore and its role in cell death. Biochemical Journal. 1999;341:233–249
  16. Crompton M. Mitochondrial intermembrane junctional complexes and their role in cell death. J Physiol. 2000;529(Pt 1):11–21
  17. Cui Q, Lu Q, So KF, Yip HK. CNTF, not other trophic factors, promotes axonal regeneration of axotomized retinal ganglion cells in adult hamsters. Invest Ophthalmol Vis Sci. 1999;40:760–766
  18. Datta SR, Dudek H, Tao X, et al.  Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell. 1997;91:231–241
  19. Deshmukh M, Kuida K, Johnson EM. Caspase inhibition extends the commitment to neuronal death beyond cytochrome C release to the point of mitochondrial depolarization. J Cell Biol. 2000;150:131–143
  20. Downward J. Mechanisms and consequences of activation of protein kinase B/Akt. Curr Opin Cell Biol. 1998;10:262–267
  21. Downward J. Ras signalling and apoptosis. Curr Opin Genet Dev. 1998;8:49–54
  22. Fall CP, Bennett JP. Visualization of cyclosporin A and Ca2+-sensitive cyclical mitochondrial depolarizations in cell culture. Biochim Biophys Acta. 1999;1410:77–84
  23. Fujimura M, Morita-Fujimura Y, Murakami K, et al.  Cytosolic redistribution of cytochrome C after transient focal cerebral ischemia in rats. J Cereb Blood Flow Metab. 1998;18:1239–1247
  24. Garcia-Valenzuela E, Shareef S, Walsh J, Sharma SC. Programmed cell death of retinal ganglion cells during experimental glaucoma. Exp Eye Res. 1995;61:33–44
  25. Grant SM, Shankar SL, Chalmers-Redman RM, et al.  Mitochondrial abnormalities in neuroectodermal cells stably expressing human amyloid precursor protein (hAPP751). Neuroreport. 1999;10:41–46
  26. Heiskanen KM, Bhat MB, Wang HW, et al.  Mitochondrial depolarization accompanies cytochrome C release during apoptosis in PC6 cells. J Biol Chem. 1999;274:5654–5658
  27. Jacotot E, Costantini P, Laboureau E, et al.  Mitochondrial membrane permeabilization during the apoptotic process. Ann NY Acad Sci. 1999;887:18–30
  28. Ji L, Mochon E, Arcinas M, Boxer LM. CREB proteins function as positive regulators of the translocated bcl-2 allele in t(14;18) lymphomas. J Biol Chem. 1996;271:22687–22691
  29. Jing Y, Dai J, Chalmers-Redman RM, et al.  Arsenic trioxide selectively induces acute promyelocytic leukemia cell apoptosis via a hydrogen peroxide-dependent pathway. Blood. 1999;94:2102–2111
  30. Kaim G, Dimroth P. ATP synthesis by F-type ATP synthase is obligatorily dependent on the transmembrane voltage. Embo J. 1999;18:4118–4127
  31. Kelekar A, Chang BS, Harlan JE, et al.  Bad is a BH3 domain-containing protein that forms an inactivating dimer with Bcl-XL. Mol Cell Biol. 1997;17:7040–7046
  32. Kermer P, Klocker N, Labes M, Bahr M. Insulin-like growth factor-I protects axotomized rat retinal ganglion cells from secondary death via PI3-K-dependent Akt phosphorylation and inhibition of caspase-3 In vivo. J Neurosci. 2000;20:2–8
  33. Kerrigan LA, Zack DJ, Quigley HA, et al.  TUNEL-positive ganglion cells in human primary open-angle glaucoma. Arch Ophthalmol. 1997;115:1031–1035
  34. Korsmeyer SJ. BCL-2 gene family and the regulation of programmed cell death. Cancer Res. 1999;59:1693S–1700S
  35. Krajewski S, Krajewska M, Ellerby LM, et al.  Release of caspase-9 from mitochondria during neuronal apoptosis and cerebral ischemia. Proc Natl Acad Sci USA. 1999;96:5752–5757
  36. Kroemer G, Zamzami N, Susin SA. Mitochondrial control of apoptosis. Immunol Today. 1997;18:44–51
  37. Li P, Nijhawan D, Budihardjo I, et al.  Cytochrome C and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell. 1997;91:479–489
  38. Lipton P. Ischemic cell death in brain neurons. Physiol Rev. 1999;79:1431–1568
  39. Liu T, Clark RK, McDonnell PC, et al.  Tumor necrosis factor-alpha expression in ischemic neurons. Stroke. 1994;25:1481–1488
  40. Liu XS, Zou H, Slaughter C, Wang XD. DFF, a heterodimeric protein that functions downstream of caspase-3 to trigger DNA fragmentation during apoptosis. Cell. 1997;89:175–184
  41. Loeffler M, Kroemer G. The mitochondrion in cell death control (certainties and incognita). Exp Cell Res. 2000;256:19–26
  42. Marzo I, Brenner C, Zamzami N, et al.  The permeability transition pore complex (a target for apoptosis regulation by caspases and bcl-2-related proteins). J Exp Med. 1998;187:1261–1271
  43. Mittag T, Danias J, Pohorenec G, et al.  Retinal damage after 3 to 4 months of elevated intraocular pressure in a rat glaucoma model. Invest Ophthalmol Vis Sci. 2000;41:3451–3459
  44. Montal M. Mitochondria, glutamate neurotoxicity and the death cascade. Biochim Biophys Acta. 1998;1366:113–126
  45. Nicholls DG, Budd SL. Mitochondria and neuronal survival. Physiol Rev. 2000;80:315–360
  46. Nicholls DG, Ferguson SJ. Bioenergetics 2. London: Academic Press; 1992;
  47. Nobes CD, Reppas JB, Markus A, Tolkovsky AM. Active p21Ras is sufficient for rescue of NGF-dependent rat sympathetic neurons. Neuroscience. 1996;70:1067–1079
  48. Nobes CD, Tolkovsky AM. Neutralizing anti-p21ras Fabs suppress rat sympathetic neuron survival induced by NGF, LIF, CNTF and cAMP. Eur J Neurosci. 1995;7:344–350
  49. Ohsato M, Hayashi H, Oshima K, et al.  In situ localization of basic fibroblast growth factor protein and mRNA in the retina. Ophthalmic Res. 1997;29:24–30
  50. Okisaka S, Murakami A, Mizukawa A, Ito J. Apoptosis in retinal ganglion cell decrease in human glaucomatous eyes. Jpn J Ophthalmol. 1997;41:84–88
  51. Osborne NN, Ugarte M, Chao M, et al.  Neuroprotection in relation to retinal ischemia and relevance to glaucoma. Surv Ophthalmol. 1999;43(Suppl 1):S102–S128
  52. Pease ME, McKinnon SJ, Quigley HA, et al.  Obstructed axonal transport of BDNF and its receptor TrkB in experimental glaucoma. Invest Ophthalmol Vis Sci. 2000;41:764–774
  53. Petronilli V, Penzo D, Scorrano L, et al.  The mitochondrial permeability transition, release of cytochrome C and cell death. Correlation wit the duration of pore openings in situ. J Biol Chem. 2001;276:12030–12034
  54. Pugazhenthi S, Nesterova A, Sable C, et al.  Akt/protein kinase B up-regulates Bcl-2 expression through cAMP-response element-binding protein. J Biol Chem. 2000;275:10761–10766
  55. Quan MZ, Kosaka M, Watanabe M, Fukuda Y. Localization of FGFR-1 in axotomized and peripheral nerve transplanted ferret retina. Neuroreport. 1999;10:3903–3907
  56. Quigley HA, Nickells RW, Kerrigan LA, et al.  Retinal ganglion cell death in experimental glaucoma and after axotomy occurs by apoptosis. Invest Ophthalmol Vis Sci. 1995;36:774–786
  57. Ragaiey T, Ma JX, Jiang WJ, et al.  L-deprenyl protects injured retinal precursor cells in vitro. J Ocul Pharmacol Ther. 1997;13:479–488
  58. Reddy SA, Huang JH, Liao WS. Phosphatidylinositol 3-kinase as a mediator of TNF-induced NF-kappa B activation. J Immunol. 2000;164:1355–1363
  59. Romashkova JA, Makarov SS. NF-kappaB is a target of AKT in anti-apoptotic PDGF signalling. Nature. 1999;401:86–90
  60. Rottenberg H, Wu S. Quantitative assay by flow cytometry of the mitochondrial membrane potential in intact cells. Biochim Biophys Acta. 1998;1404:393–404
  61. Scorrano L, Petronilli V, Bernardi P. On the voltage dependence of the mitochondrial permeability transition pore—A critical appraisal. J Biol Chem. 1997;272:12295–12299
  62. Scorrano L, Petronilli V, Colonna R, et al.  Interactions of chloromethyltetramethylrosamine (Mitotracker Orange) with isolated mitochondria and intact cells. Ann NY Acad Sci. 1999;893:391–395
  63. Shareef SR, Garcia-Valenzuela E, Salierno A, et al.  Chronic ocular hypertension following episcleral venous occlusion in rats. Exp Eye Res. 1995;61:379–382[letter]
  64. Sugrue MM, Wang Y, Rideout HJ, et al.  Reduced mitochondrial membrane potential and altered responsiveness of a mitochondrial membrane megachannel in p53-induced senescence. Biochem Biophys Res Commun. 1999;261:123–130
  65. Susin SA, Lorenzo HK, Zamzami N, et al.  Molecular characterization of mitochondrial apoptosis-inducing factor. Nature. 1999;397:441–446
  66. Susin SA, Zamzami N, Kroemer G. Mitochondria as regulators of apoptosis (doubt no more). Biochim Biophys Acta. 1998;1366:151–165
  67. Tatton NA, Tezel G, Insolia S, et al.  In situ detection of apoptosis in normal pressure glaucoma. Surv Ophthalmol. 2001;45:S268–S272
  68. Tatton NA. Increased caspase 3 and bax immunoreactivity accompany nuclear GAPDH translocation and neuronal apoptosis in Parkinson's disease. Exp Neurol. 2000;166:29–43[In Process Citation]
  69. Tatton NA, Maclean-Fraser A, Tatton WG, et al.  A fluorescent double-labeling method to detect and confirm apoptotic nuclei in Parkinson's disease. Ann Neurol. 1998;44:S142–S148
  70. Tatton WG, Chalmers-Redman RME. Modulation of gene expression rather than monoamine oxidase inhibition ((-)-deprenyl-related compounds in controlling neurodegeneration). Neurol. 1996;47:S171–S183
  71. Tatton WG, Olanow CW. Apoptosis in neurodegenerative diseases (the role of mitochondria). Biochim Biophys Acta. 1999;1410:195–213
  72. Tenneti L, D'Emilia DM, Troy CM, Lipton SA. Role of caspases in N-methyl-D-aspartate-induced apoptosis in cerebrocortical neurons. J Neurochem. 1998;71:946–959
  73. Vorwerk CK, Gorla MS, Dreyer EB. An experimental basis for implicating excitotoxicity in glaucomatous optic neuropathy. Surv Ophthalmol. 1999;43(Suppl 1):S142–S150
  74. Wadia JS, Chalmers-Redman RME, Ju WJH, et al.  Mitochondrial membrane potential and nuclear changes in apoptosis caused by serum and nerve growth factor withdrawal (time course and modification by (-)-deprenyl). J Neurosci. 1998;18:932–947
  75. Wahlin KJ, Campochiaro PA, Zack DJ, Adler R. Neurotrophic factors cause activation of intracellular signaling pathways in Muller cells and other cells of the inner retina, but not photoreceptors. Invest Ophthalmol Vis Sci. 2000;41:927–936
  76. Weibel D, Kreutzberg GW, Schwab ME. Brain-derived neurotrophic factor (BDNF) prevents lesion-induced axonal die-back iNYoung rat optic nerve. Brain Res. 1995;679:249–254
  77. Wilson BE, Mochon E, Boxer LM. Induction of bcl-2 expression by phosphorylated CREB proteins during B-cell activation and rescue from apoptosis. Mol Cell Biol. 1996;16:5546–5556
  78. Xu L, Ma J, Seigel GM, Ma JX. l-Deprenyl, blocking apoptosis and regulating gene expression in cultured retinal neurons. Biochem Pharmacol. 1999;58:1183–1190
  79. Xue L, Murray JH, Tolkovsky AM. The Ras/phosphatidylinositol 3-kinase and Ras/ERK pathways function as independent survival modules each of which inhibits a distinct apoptotic signaling pathway in sympathetic neurons. J Biol Chem. 2000;275:8817–8824
  80. Yang E, Zha J, Jockel J, et al.  Bad, a heterodimeric partner for Bcl-XL and Bcl-2, displaces Bax and promotes cell death. Cell. 1995;80:285–291
  81. Yoles E, Wheeler LA, Schwartz M. Alpha2-adrenoreceptor agonists are neuroprotective in a rat model of optic nerve degeneration. Invest Ophthalmol Vis Sci. 1999;40:65–73[published erratum appears in Invest Ophthalmol Vis Sci 199 Oct;40(11):2470]
  82. Zamzami N, Brenner C, Marzo I, et al.  Subcellular and submitochondrial mode of action of Bcl-2-like oncoproteins. Oncogene. 1998;16:2265–2282
  83. Zha J, Harada H, Osipov K, et al.  BH3 domain of BAD is required for heterodimerization with BCL-XL and pro-apoptotic activity. J Biol Chem. 1997;272:24101–24104
  84. Zhang C, Takahashi K, Lam TT, Tso MO. Effects of basic fibroblast growth factor in retinal ischemia. Invest Ophthalmol Vis Sci. 1994;35:3163–3168
  85. Zou H, Henzel WJ, Liu XS, et al.  Apaf-1, a human protein homologous to C elegans CED-4, participates in cytochrome C-dependent activation of caspase-3. Cell. 1997;90:405–413

PII: S0039-6257(01)00207-7

Survey of Ophthalmology
Volume 45 , Pages S277-S283 , May 2001

Article Tools

* Image Usage & Resolution