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Apoptosis in the Nervous System

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Abstract

Apoptosis (from the Greek apoptosis, i.e., falling of leaves) is the phenomenon of programmed cell death, which plays an important role in the normal embryonic development and maintenance of the homeostasis of the differentiated tissues of adult organisms. Completion of the apoptosis process is accompanied by specific morphological and biochemical changes in the involved cells. Various disturbances in the control of apoptosis underlie various neurodegenerative diseases, the formation of malignant tumors, autoimmune disturbances, and developmental abnormalities. A deficit of neurotrophic factors leads to apoptosis of neurons. The survival of specific cell populations of neurons is controlled by neurotrophic factors and their combinations. Oncogene bcl-2, a repressor of cell death, belongs to the better-studied factors controlling apoptosis. The terminal stages of cell death, including the death of neurons, depend on the activation of caspases, specifically caspase-1 (interleukin-1β-converting enzyme). Ca2+and reactive forms of oxygen play an important role in the initiation of apoptosis by changing the mitochondrial permeability. Neuregulin, a factor of neuronal origin, is the main controlling factor in apoptosis of Schwann cells, and this process determines the size of their definitive population. Fibroblast growth factor b diminishes the apoptosis of Schwann cells in regenerating nerve fibers.

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REFERENCES

  • Aubert, I., Ridet, J.-L., and Gage, F., Regeneration in the Adult Mammalian CNS: Guided by Development, Curr. Opin. Neurobiol., 1995, vol. 5, pp. 625–635.

    Google Scholar 

  • Bancher, C., Lassmann, H., Breitschopf, H., and Jellinger, K.A., Mechanisms of Cell Death in Alzheimer's Disease, J. Neurol. Transm., Suppl., 1997, vol. 50, pp. 141–152.

    Google Scholar 

  • Barrett, G.L. and Bartlett, P.F., The P75 Nerve Growth Factor Receptor Mediates Survival or Death Depending on the Stage of Sensory Neuron Development, Proc. Nat. Acad. Sci. USA, 1994, vol. 91, pp. 6501–6505.

    Google Scholar 

  • Bauerle, P.A. and Baltimore, D., NF-ϰB: Ten Years After, Cell, 1996, vol. 87, pp. 13–20.

    Google Scholar 

  • Beg, A.A. and Baltimore, D., An Essential Role for NF-ϰB in Preventing TNF-α-Induced Cell Death, Science, 1996, vol. 274, pp. 782–784.

    Google Scholar 

  • Bredesen, D.E., Genetic Control of Neural Cell Apoptosis, Perspect. Dev. Neurobiol., 1996, vol. 3, no. 2, pp. 101–109.

    Google Scholar 

  • Carayon, P., Portier, M., Dussossoy, D., et al., Involvement of Peripheral Benzodiazepine Receptors in the Protection of Hematopoietic Cells against Oxygen Radical Species, Blood, 1996, vol. 87, pp. 3170–3178.

    Google Scholar 

  • Chalmers-Redman, P.M., Fraser, A.D., Ju, W.Y., et al., Mechanisms of Nerve Cell Death: Apoptosis or Necrosis after Cerebral Ischaemia, Int. Rev. Neurobiol., 1997, vol. 40, pp. 1–25.

    Google Scholar 

  • Cheema, S.S., Barrett, G.L., and Bartlett, P.F., Reducing P75 Nerve Growth Factor Receptor Levels Using Antisense Oligonucleotides Prevents the Loss of Axotomized Sensory Neurons in the Dorsal Root Ganglia of Newborn Rats, J. Neurosci. Res., 1996, vol. 46, no. 2, pp. 239–245.

    Google Scholar 

  • Chen, D.F., Jhaveri, S., and Schneider, G.E., Intrinsic Changes in Developing Retinal Neurons Result in Regenerative Failure of Their Axons, Proc. Natl. Acad. Sci. USA, 1995, vol. 92, pp.7287–7291.

    Google Scholar 

  • Chen, D.F., Schneider, G.E., Martinou, J.C., and Tonegawa, S., Bcl-2 Promotes Regeneration of Severed Axons in Mammalian CNS, Nature, 1997, vol. 385, pp.434–439.

    Google Scholar 

  • Chinnaiyan, A.M., O'Rourke, K., Lane, B.R., and Dixit V.M., Interaction of CED-4 with CED-3 and CED-9: A Molecular Frame for Cell Death, Science, 1997, vol. 275, pp. 1122–1126.

    Google Scholar 

  • Choi, S.S., Park, I.-C., Yun, J.W., et al., A Novel Bcl-2 Related Gene, Bfl-1, Is Overexpressed in Stomach Cancer and Preferentially Expressed in Bone Marrow, Oncogene, 1995, vol. 11, pp. 1693–1698.

    Google Scholar 

  • Ciutat, D., Caldero, J., Oppenheim, R.W., and Esquerda, J.E., Schwann Cell Apoptosis during Normal Development and after Axonal Degeneration Induced by Neurotoxins in the Chick Embryo, J. Neurosci., 1996, vol. 16, no. 12, pp. 3979–3990.

    Google Scholar 

  • Cortazzo, M.H., Kassis, E.S., Sproul, K.A., and Schor, N.F., Nerve Growth Factor (NGF)-Mediated Protection of Neural Crest Cells from Antimitotic Agent-Induced Apoptosis: The Role of the Low-Affinity NGF Receptor, J. Neurosci., 1996, vol. 16, no. 12, pp. 3895–3899.

    Google Scholar 

  • Cotman, C.W. and Su, J.H., Mechanisms of Neuronal Death in Alzheimer's Disease, Brain Pathol., 1996, vol. 6, no. 4, pp. 493–506.

    Google Scholar 

  • Crowley, C., Spencer, S.D., Nishimura, M.C., et al., Mice Lacking Nerve Growth Factor Display Perinatal Loss of Sensory and Sympathetic Neurons Yet Develop Basal Forebrain Cholinergic Neurons, Cell, 1994, vol. 76, pp.10 001–10 011.

    Google Scholar 

  • Das, R., Reddy, E.P., Chatterjee, D., and Andrews, D.W., Identification of a Novel Bcl-2 Related Gene, BRAG-1, in Human Glioma, Oncogene, 1996, vol. 12, pp. 947–951.

    Google Scholar 

  • Davies, A.M., Neurotrophins: The Yin and Yang of Nerve Growth Factor, Curr. Biol., 1997, vol. 7, no. 1, pp. R38-R40.

    Google Scholar 

  • Debilbao, F. and Duboisdauphin, M., Acute Application of an Interleukin-1 Beta-Converting Enzyme-Specific Inhibitor Delays Axotomy-Induced Motoneuron Death, Neuroreport., 1996, vol. 7, no. 18, pp. 3051–3054.

    Google Scholar 

  • Deckwerth, T.L. and Johnson, E.M., Jr., Temporal Analysis of Events Associated with Programmed Cell Death (Apoptosis) of Sympathetic Neurons Deprived of Nerve Growth Factor, J. Cell Biol., 1993, vol. 123, no. 5, pp. 1207–1222.

    Google Scholar 

  • Dong, Z., Brennan, A., Liu, N., et al., Neu Differentiation Factor Is a Neuron-Glial Signal and Regulates Survival, Proliferation, and Maturation of Rat Schwann Cell Precursors, Neuron., 1995, vol. 15, pp. 585–596.

    Google Scholar 

  • Doyle, C.A. and Hunt, S.P., Reduced Nuclear Factor Kappa B (P65) Expression in Rat Primary Sensory Neurons after Peripheral Nerve Injury, Neuroreport., 1997, vol. 8, no. 13, pp. 2937–2942.

    Google Scholar 

  • D'Sa-Eipper, C., Subramanian, T., and Chinnadurai, G., Bfl-1, a Bcl-2 Homologue, Suppresses P53-Induced Apoptosis and Exhibits Potent Cooperative Transforming Activity, Cancer Res., 1996, vol. 56, pp. 3879–3882.

    Google Scholar 

  • Edstrom, A., Ekstrom, P.A.R., and Tonge, D., Axonal Outgrowth and Neuronal Apoptosis in Cultured Adult Mouse Dorsal Root Ganglion Preparations: Effects of Neurotrophins, of Inhibition of Neurotrophin Actions and of Prior Axotomy, Neurosci., 1996, vol. 75, no. 4, pp. 1165–1174.

    Google Scholar 

  • Ekstrom, P.A.R., Neurones and Glial Cells of the Mouse Sciatic Nerve Undergo Apoptosis after Injury in vivo and in vitro, Neuroreport., 1995, vol. 9, pp. 1029–1032.

    Google Scholar 

  • Ernfors, P., Lee, K.F., and Jaenisch, R., Mice Lacking Brain-Derived Neurotrophic Factor Develop with Sensory Deficits, Nature, 1994, vol. 368, pp. 147–150.

    Google Scholar 

  • Frade, J.M., Rodriguez-Tebar, A., and Barde, Y.A., Induction of Cell Death by Endogenous Nerve Growth Factor through Its P75 Receptor, Nature, 1996, vol. 383, no. 6596, pp. 166–168.

    Google Scholar 

  • Fujimura, M., Tominaga, T., and Yoshimoto, T., Nicotinamide Inhibits Inducible Nitric Oxide Synthase mRNA in Primary Rat Glial Cells, Neurosci. Lett., 1997, vol. 228, pp. 107–110.

    Google Scholar 

  • Fulle, S., Mariggio, M.A., Belia, S., et al., Nerve Growth Factor Inhibits Apoptosis Induced by S-100 Binding in Neuronal PC 12 Cells, Neurosci., 1997, vol. 76, pp. 159–166.

    Google Scholar 

  • Gavrilovic, J., Brennan, A., Mirsky, R., and Jessen, K.R., Fibroblast Growth Factors and Insulin Growth Factors Combine to Promote Survival of Rat Schwann Cell Precursors without Induction of DNA Synthesis, Eur. J. Neurosci., 1995, vol. 7, pp. 77–85.

    Google Scholar 

  • Gerschenson, L.E. and Rotello, R.J., Apoptosis: A Different Type of Cell Death, FASEB J., 1992, vol. 6, pp. 2450–2455.

    Google Scholar 

  • Gillardon, F., Klimaschewski, L., Wickert, H., et al., Expression Pattern of Candidate Cell Death Effector Proteins Bax, Bcl-2, Bcl-X, and C-Jun in Sensory and Motor Neurons Following Sciatic Nerve Transection in the Rat, Brain Res., 1996, vol. 739, nos. 1–2, pp. 244–250.

    Google Scholar 

  • Grilli, M., Pizzi, M., Memo, M., and Spano, P., Neuroprotection by Aspirin and Sodium Salicylate through Blockade of NF-ϰB Activation, Science, 1996, vol. 274, pp. 1383–1385.

    Google Scholar 

  • Grinspan, J.B., Marchionni, M.A., Reeves, M., et al., Axonal Interactions Regulate Schwann Cell Apoptosis in Developing Peripheral Nerve: Neuregulin Receptors and the Role of Neuregulins, J. Neurosci., 1996, vol. 16, pp.6107–6118.

    Google Scholar 

  • Groves, M.J., Christopherson, T., Giometto, B., and Scaravilli, F., Axotomy-Induced Apoptosis in Adult Rat Primary Sensory Neurons, J. Neurocytol., 1997, vol. 26, no. 9, pp. 615–624.

    Google Scholar 

  • Gu, Z.Z., Pan, Y.C., Cui, J.K., et al., Gene Expression and Apoptosis in the Spinal Cord Neurons after Sciatic Nerve Injury, Neurochem. Int., 1997, vol. 30, nos. 4–5, pp. 417–426.

    Google Scholar 

  • Gunasekar, P.G., Kantasamy, A.G., Borowitz, J.L., and Isom, G.E., NMDA Receptor Activation Produces Concurrent Generation of Nitric Oxide and Reactive Oxygen Species: Implication for Cell Death, J. Neurochem., 1995, vol. 65, pp. 2016–2021.

    Google Scholar 

  • Gupta, S., Apoptosis/Programmed Cell Death. A Historical Perspective, Adv. Exp. Med. Biol., 1996, vol. 406, pp. 1–9.

    Google Scholar 

  • Haldar, S., Chintapalli, J., and Croce, C.M.,Taxol Induces Bcl-2 Phosphorylation and Death of Orostate Cancer Cells, Cancer Res., 1996, vol. 56, pp. 1253–1255.

    Google Scholar 

  • Hilton, M., Middleton, G., and Davies, A.M., Bcl-2 Influences Axonal Growth Rate in Embryonic Sensory Neurons, Curr. Biol., 1997, vol. 7, pp. 798–800.

    Google Scholar 

  • Hockenbery, D.M., Oltvai, Z.N., Yin, X.-M., et al., Bcl-2 Functions in an Antioxidant Pathway to Prevent Apoptosis, Cell, 1993, vol. 75, pp. 241–251.

    Google Scholar 

  • Huang, Z., Huang, P.L., Panahian, N., et al., Effects of Cerebral Ischemia in Mice Deficient in Neuronal Nitric Oxide Synthase, Science, 1994, vol. 265, pp. 1883–1885.

    Google Scholar 

  • Ichimiya, S., Davis, J.G., Orourke, D.M., et al., Murine Thioredoxin Peroxidase Delays Neuronal Apoptosis and Is Expressed in Areas of the Brain Most Susceptible to Hypoxic and Ischemic Injury, DNA and Cell Biol., 1997, vol. 16, pp. 311–321.

    Google Scholar 

  • Jessen, K.R., Brennan, A., Morgan, L., et al., The Schwann Cell Precursor and Its Fate: A Study of Cell Death and Differentiation During Gliogenesis in Rat Embryonic Nerves, Neuron., 1994, vol. 12, pp. 509–527.

    Google Scholar 

  • Jordan, J.G., Hadge, G.D., Prehn, J.H.M., et al., Expression of Human Copper/ Zinc Superoxide Dismutase Inhibits the Death of Rat Sympathetic Neurons Caused by Withdrawal of Nerve Growth Factor, Mol. Pharmacol., 1995, vol. 47, no. 6, pp. 1095–1100.

    Google Scholar 

  • Juurlink, B.H.J. and Sweeney, M.I., Mechanisms That Result in Damage during and Following Cerebral Ischemia, Neurosci. and Biobehav. Rev., 1997, vol. 21, pp. 121–128.

    Google Scholar 

  • Katoh, S., Mitsui, Y., Kitani, K., and Suzuki, T., The Rescuing Effect of Nerve Growth Factor Is the Result of Up-Regulation of Bcl-2 in Hyperoxia-Induced Apoptosis of a Subclone of Pheochromocytoma Cells, PC12h, Neurosci. Lett., 1997, vol. 232, pp. 71–74.

    Google Scholar 

  • Kiatipattanasakul, W., Nakamura, S., Hossain, M.M., et al., Apoptosis in the Aged Dog Brain, Acta Neuropathol. Berl., 1996, vol. 92, no. 3, pp. 242–249.

    Google Scholar 

  • Klein, R., Silos-Santiago, I., Smeyne, R.J., et al., Distribution of the Neurotrophin-3 Receptor Gene trkC Eliminates La Muscle Afferents and Results in Abnormal Movement, Nature, 1994, vol. 368, pp. 249–251.

    Google Scholar 

  • Klimiuk, P.A., Bernacka, K., and Kuryliszyn-Moskal, A., Apoptosis in Autoimmune Diseases, Rocz. Akad, Med. im. Juliana Marchlewskiego Bialymstoku, 1995, vol. 40, no. 2, pp. 227–232.

    Google Scholar 

  • Kopp, D.M., Trachtenberg, J.T., and Thompson, W.J., Title Dial Growth Factor Rescues Schwann Cells of Mechanoreceptors from Denervation-Induced Apoptosis, J. Neurosci., 1997, vol. 17, pp. 6697–6706.

    Google Scholar 

  • Kristian, T. and Siesjo, B.K., Calcium-Related Damage in Ischemia, Life Sci., 1996, vol. 59, pp. 357–367.

    Google Scholar 

  • Kroemer, G., The Proto-Oncogene Bcl-2 and Its Role in Regulating Apoptosis, Nat. Med., 1997, vol. 3, pp. 614–620.

    Google Scholar 

  • Kroemer, G., Zamzami, N., and Susin, S.A., Mitochondrial Control of Apoptosis, Immunol. Today, 1997, vol. 18, pp. 44–51.

    Google Scholar 

  • Kubo, T., Nonomura, T., Enokido, Y., and Hatanaka, H., Brain-Derived Neurotrophic Factor (BDNF) Can Prevent Apoptosis of Rat Cerebellar Granule Neurons in Culture, Dev. Brain Res., 1995, vol. 85, no. 2, pp. 249–258.

    Google Scholar 

  • Lin, E.Y., Orlofsky, A., Berger, M.S., and Prystowsky, M.B., Characterization of Al, a Novel Hemopoietic-Specific Early-Response Gene with Sequence Similarity to Bcl-2, J. Immun., 1993, vol. 151, pp. 1979–1988.

    Google Scholar 

  • Lin, K.I., Lee, S.H., Narayanan, R., et al., Thiol Agents and Bcl-2 Identify an Alphavirus-Induced Apoptotic Pathway That Requires Activation of the Transcription Factor NF-Kappa B, J. Cell Biol., 1995, vol. 131, pp. 1149–1161.

    Google Scholar 

  • Lin, E.Y., Orlofsky, A., Wang, H.-G., et al., A Bcl-2 Family Member Prolongs Cell Survival and Permits Myeloid Differentiation, Blood, 1996, vol. 87, pp. 983–992.

    Google Scholar 

  • Lin, E.Y., Kozak, C.A., Orlofsky, A., and Prystowsky, M.B., The Bcl-2 Family Member, Bcl2al Maps to Mouse Chromosome 9 and Human Chromosome 15, Mamm. Genome, 1997, vol. 8, pp. 293–294.

    Google Scholar 

  • Macaya, A., Apoptosis en el Sistema Nervioso, Rev. Neurol., 1996, vol. 24, no. 135, pp. 1356–1360.

    Google Scholar 

  • Macewan, D.J., Elevated cPLA(2) Levels as a Mechanism by Which the P70 TNF and P75 NGF Receptors Enhance Apoptosis, FEBS Lett., 1996, vol. 379, no. 1, pp. 77–81.

    Google Scholar 

  • Marchetti, P., Decaudin, D., Macho, A., et al., Redox Regulation of Apoptosis: Impact of Thiol Oxidation Status on Mitochondrial Function, Europ. J. Immunol., 1997, vol. 27, pp. 289–296.

    Google Scholar 

  • Masliah, E., Ge, N., and Mucke, L., Pathogenesis of HIV-1 Associated Neurodegeneration, Crit. Rev. Neurobiol., 1996, vol. 10, no. 1, pp. 57–67.

    Google Scholar 

  • Meisinger, C. and Grothe, C., Differential Regulation of Fibroblast Growth Factor (FGF)-2 and FGF Receptor 1 mRNAs and FGF-2 Isoforms in Spinal Ganglia and Sciatic Nerve after Peripheral Nerve Lesion, J. Neurochem., 1997, vol. 68, no. 3, pp. 1150–1158.

    Google Scholar 

  • Mills, J.C., Kim, L.H., and Pittman, R.N., Differentiation to an NGF-Dependent State and Apoptosis Following NGF Removal Both Occur Asynchronously in Cultures of PC 12 Cells, Exp. Cell. Res., 1997, vol. 231, pp. 337–345.

    Google Scholar 

  • Miura, M., Zhu, H., Rotello, R., et al., Induction of Apoptosis in Fibroblasts by IL-1-Beta-Converting Enzyme, a Mammalian Homolog of the C. elegans Cell Death Gene Ced-3, Cell, 1993, vol. 75, pp. 653–660.

    Google Scholar 

  • Muragaki, Y., Chou, T.T., Kaplan, D.R., et al., Nerve Growth Factor Induces Apoptosis in Human Medulloblastoma Cell Lines That Express TrkA Receptors, J. Neurosci., 1997, vol. 17, pp. 530–542.

    Google Scholar 

  • Murphy, A.N., Bredesen, D.E., Cortopassi, G., et al., Bcl-2 Potentiates the Maximal Calcium Uptake Capacity of Neural Cell Mitochondria, Proc. Natl. Acad. Sci. USA, 1996, vol. 93, pp. 9893–9898.

    Google Scholar 

  • Nakao, J., Shinoda, J., Nakai, Y., et al., Apoptosis Regulates the Number of Schwann Cells at the Premyelinating Stage, J. Neurochem., 1997, vol. 68, no. 5, pp. 1853–1862.

    Google Scholar 

  • Olasode, B.J., Dying by Default, the Biology of Apoptosis: A Review [See Comments], East Afr. Med. J., 1997, vol. 74, no. 2, pp. 108–111.

    Google Scholar 

  • Oliveira, A.L.R., Risling, M., Deckner, M., et al., Neonatal Sciatic Nerve Transection Induces TUNEL Labeling of Neurons in the Rat Spinal Cord and DRG, Neuroreport., 1997, vol. 8, no. 13, pp. 2837–2840.

    Google Scholar 

  • Oppenheim, R.W., Cell Death during Development of the Nervous System, Ann. Rev. Neurosci., 1991, vol. 14, pp. 453–501.

    Google Scholar 

  • Pan, H., Yin, C., and Van-Dyke, T., Apoptosis and Cancer Mechanisms, Cancer Surv., 1997, vol. 29, pp. 305–327.

    Google Scholar 

  • Ratan, R.R., Murphy, T.H., and Baraban, J.M., Oxidative Stress Induces Apoptosis in Embryonic Cortical Neurons, J. Neurochem., 1994, vol. 62, pp. 376–379.

    Google Scholar 

  • Reed, J.C., Double Identity for Proteins of the Bcl-2 Family, Nature, 1997, vol. 387, pp. 773–776.

    Google Scholar 

  • Rosenblum, W.I., Histopathologic Clues to the Pathways of Neuronal Death Following Ischemia/Hypoxia, J. Neurotrauma., 1997, vol. 14, pp. 313–326.

    Google Scholar 

  • Roytta, M. and Salonen, V., Long-Term Endoneuronal Changes after Nerve Transection, Acta Neuropathol., 1988, vol. 76, no. 1, pp. 35–45.

    Google Scholar 

  • Schulz, J.B., Matthews, R.T., Muqit, M.M., et al., Inhibition of Neuronal Nitric Oxide Synthase by 7-Nitroindazole Protects against MPTP-Induced Neurotoxicity in Mice, J. Neurochem., 1995, vol. 64, pp. 936–939.

    Google Scholar 

  • Sendtner, M., Gotz, R., Holtmann, B., and Thoenen, H., Endogenous Ciliary Neurotrophic Factor Is a Lesion Factor for Axotomized Motoneurons in Adult Mice, J. Neurosci., 1997, vol. 17, no. 18, pp. 6999–7006.

    Google Scholar 

  • Shaw, R., Cianchetti, R., Pleasure, D., and Kreider, B., Basic Fibroblast Growth Factor Prevents cAMP-Induced Apoptosis in Cultured Schwann Cells, J. Neurosci. Res., 1997, vol. 47, no. 4, pp. 400–404.

    Google Scholar 

  • Shi, B., De-Girolami, U., He, J., et al., Apoptosis Induced by HIV-1 Infection of the Central Nervous System, J. Clin. Invest., 1996, vol. 98, no. 9, pp. 1979–1990.

    Google Scholar 

  • Siironen, J., Vuorinen, V., Taskinen, H.S., and Roytta, M., Axonal Regeneration into Chronically Denervated Distal Stump. 2. Active Expression of Type I Collagen mRNA in Epineurium, Acta Neuropathol., 1995, vol. 89, pp. 219–226.

    Google Scholar 

  • Smeyne, R.J., Klein, R., Schnapp, A., et al., Severe Sensory and Sympathetic Neuropathies in Mice Carrying Trk/NGF Receptor Gene, Nature, 1994, vol. 368, pp.–246–249.

    Google Scholar 

  • Spear, T., Estevez, A.G., Barbeito, L., et al., Nerve Growth Factor Protects PC 12 Cells against Peroxynitrite-Induced Apoptosis via a Mechanism Dependent on Phosphatidylinositol 3-Kinase, J. Neurochem., 1997, vol. 69, pp. 53–59.

    Google Scholar 

  • Strack, P.P., Frey, M.W., Rizzo, C.J., et al., Apoptosis Mediated by HIV Protease Is Preceded by Cleavage of Bcl-2, Proc. Natl. Acad. Sci. USA, 1996, vol. 93, pp. 9571–9576.

    Google Scholar 

  • Sugaya, K., Chouinard, M., and McKinney, M., Immunostimulation Protects Microglial Cells from Nitric Oxide-Mediated Apoptosis, Neuro Report., 1997, vol. 8, pp. 2241–2245.

    Google Scholar 

  • Swett, J.E., Hong, C.Z., and Miller, P.O., Most Dorsal Root Ganglion Neurons of the Adult Rat Survive Nerve Crush Injury, Somatosens. Motor Res., 1995, vol. 12, nos. 3–4, pp. 177–189.

    Google Scholar 

  • Syroid, D.E., Maycox, P.P., Burrola, P.G., et al., Cell Death in the Schwann Cell Lineage and Its Regulation by Neuragulin, Proc. Natl. Acad. Sci. USA, 1996, vol. 93, pp. 9229–9234.

    Google Scholar 

  • Taglialatela, G., Robinson, R., and Perezpolo, J.R., Inhibition of Nuclear Factor Kappa B (NF Kappa B) Activity Induces Nerve Growth Factor-Resistant Apoptosis in PC12 Cells, J. Neurosci. Res., 1997, vol. 47, no. 2, pp. 155–162.

    Google Scholar 

  • Takadera, T. and Ohyashiki, T., Apoptotic Cell Death and Caspase 3 (CPP32) Activation Induced by Calcium Ionophore at Low Concentrations and Their Prevention by Nerve Growth Factor in PC12 Cells, Eur. J. Biochem., 1997, vol. 249, no. 1, pp. 8–12.

    Google Scholar 

  • Tanaka, S., Saito, K., and Reed, J.C., Structure-Function Analysis of the Bcl-2 Oncoprotein: Addition of a Heterologous Transmembrane Domain to Portions of the Bcl-2b Protein Restores Function as a Regulator of Cell Survival, J. Biol. Chem., 1993, vol. 268, pp. 10 920–10 926.

    Google Scholar 

  • Trachtenberg, J.T. and Thompson, W.J., Schwann Cell Apoptosis at Developing Neuromuscular Junctions Is Regulated by Glial Growth Factor, Nature, 1996, vol. 379, pp. 174–177.

    Google Scholar 

  • Van Antwerp, D.I., Martin, S.I., Kafri, T., et al., Suppression of TNF-α-Induced Apoptosis by NF-ϰB, Science, 1996, vol. 274, pp. 787–789.

    Google Scholar 

  • Wang, C.-Y., Mayo, M.W., and Baldwin, A.S., Jr., TNF and Cancer Therapy-Induced Apoptosis Potentiation by Inhibition of NF-ϰB, Science, 1996a, vol. 274, pp. 784–787.

    Google Scholar 

  • Wang, H.-G., Rapp, U.R., and Reed, J.C., Bcl-2 Targets the Protein Kinase Raf-1 to Mitochondria, Cell, 1996b, vol. 87, pp. 629–638.

    Google Scholar 

  • Wilcox, B.J., Applegate, M.D., Porteracailliau, C., and Koliatsos, V.E., Nerve Growth Factor Prevents Apoptotic Cell Death in Injured Central Cholinergic Neurons, J. Comp. Neurol., 1995, vol. 359, no. 4, pp. 573–585.

    Google Scholar 

  • Williams, K.A. and Coster, D.J., Rethinking Immunological Privilege: Implications for Corneal and Limbal Stem Cell Transplantation, Mol. Med. Today, 1997, vol. 3, pp. 495–501.

    Google Scholar 

  • Winter, P.M. and Tickle, C., Syndactylies and Polydactylies: Embryological Overview and Suggested Classification, Europ. J. Hum. Genet., 1993, vol. 1, pp. 96–104.

    Google Scholar 

  • Wu, D., Wallen, H.D., and Nu-Ez, G., Interaction and Regulation of Subcellular Localization of CED-4 by CED-9, Science, 1997, vol. 275, pp. 1126–1129.

    Google Scholar 

  • Yuan, J., Shaham, S., Ledoux, S., et al., The C. Elegans Cell Death Gene Ced-3 Encodes a Protein Similar to Mammalian Interleukin-1-Beta-Converting Enzyme, Cell, 1993, vol. 75, pp. 641–652.

    Google Scholar 

  • Zhang, J., Pieper, A., and Snyder, S.H., Poly(ADP-Ribose) Synthase Activation: An Early Indicator of Neurotoxic DNA Damage, J. Neurochem., 1995, vol. 65, pp. 1411–1414.

    Google Scholar 

  • Zhu, W., Cowie, A., Wasfy, G.W., et al., Bcl-2 Mutants with Restricted Subcellular Localization Reveal Spatially Distinct Pathways for Apoptosis in Different Cell Types, EMBO J., 1996, vol. 15, pp. 4130–4141.

    Google Scholar 

  • Zorattu, M. and Szabo, I., The Mitochondrial Permeability Transition, Biochim. Biophys. Acta Rev. Biomembr., 1995, vol. 1241, pp. 139–176.

    Google Scholar 

  • Zorick, T.S. and Lemke, G., Schwann Cell Differentiation, Curr. Opinion Cell Biol., 1996, vol. 8, pp. 870–876.

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  1. Kazan Medical University, Kazan, 420012, Tatarstan

    Yu. A. Chelyshev & K. I. Saitkulov

  2. Republic Medical Diagnostic Center, Kazan, 420043, Tatarstan

    G. V. Cherepnev

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  2. G. V. Cherepnev
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  3. K. I. Saitkulov
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Chelyshev, Y.A., Cherepnev, G.V. & Saitkulov, K.I. Apoptosis in the Nervous System. Russian Journal of Developmental Biology 32, 92–102 (2001). https://doi.org/10.1023/A:1012656000524

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  • DOI: https://doi.org/10.1023/A:1012656000524

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