| More

Apoptotic cell death in the mammalian central nervous system during development and in pathological conditions

Views: 104 Downloads: 108
I. DORI (Ι. ΔΩΡΗ), T. ZACHARAKI (Θ. ΖΑΧΑΡΑΚΗ)
I. DORI (Ι. ΔΩΡΗ), T. ZACHARAKI (Θ. ΖΑΧΑΡΑΚΗ)

Abstract


Mammalian central nervous system (CNS) development involves genetically controlled, opposing processes, such as neuronal proliferation, migration, differentiation and death. The natural, developmental cell death is a ubiquitous phenomenon and is referred to as «programmed cell death» (PCD). Apoptosis, a type of PCD, is a central event in normal development of the CNS, playing an important role in the control of cell numbers and the establishment of neuronal circuitry. During embryogenesis, apoptosis takes place in proliferating cell populations and is involved in CNS morphogenesis. At later stages of development, apoptosis occurs in postmitotic neurons, because of the competition for limited supply of neurotrophic factors, that originally suppress the endogenous genetic death programme. Data concerning apoptotic cell death during normal CNS development of domestic mammals is lacking, therefore information about the developmental pattern of this phenomenon is restricted to rodents and rabbits. In these animals it has been suggested that apoptosis follows a mono- or biphasic time course and is completed during

an early, critical period of CNS development, that is characterized by morphological and functional neuronal maturation and synapse formation. Apart from its role in CNS development, apoptosis has also been implicated in neuronal loss accompanying neurodegenerative diseases and traumatic brain injuries in humans and animals. In the domestic canine brain, it has been shown that neurons die via apoptosis in Alzheimer's-like dementia, cerebellar abiotrophy, global and focal ischemia and virus-induced encephalopathies. In addition, cell death in ruminants with transmissible spongiform encephalopathy has been reported to be apoptotic in nature. A plethora of studies using animal models have been employed to elucidate the mechanisms than govern cell loss in neurological disorders. These studies provided strong evidence that experimental lesions of the connections between CNS areas and withdrawal of neurotrophic factors result in an increase of apoptosis, that is age-dependent. Specifically, developing neurons are more dependent on the integrity of their connections than mature ones. In addition, the response of neurons to apoptotic stimuli shows regional specificity. According to epidemiologic studies, CNS disorders are of major concern for animal and human public health, with a high socioeconomic impact. A major goal of neuroscientists is the development of therapeutic approaches for CNS repair. Contemporary strategies that are under trial include neurotrophic factor substitution and transplantation of stem cells. Investigation of the principles and mechanisms controlling cell loss in neurodegenerative diseases and traumatic brain injuries are universally considered of high priority and hopefully will lead to novel therapeutic approaches, with encouraging outcome. The present review summarises recent data on the molecular mechanisms and factors controlling neuronal apoptosis during development and in pathological conditions, describes popular animal models used in lesion studies and discusses therapeutic approaches aiming at preventing or restricting apoptotic cell death.


Keywords


Apoptosis; development; neurodegenerative diseases

Full Text:

PDF

References


Abe Κ (2000) Therapeutic potential of neurotrophic factors and neural stem cells against ischemic brain injury. J Cereb Blood Flow Metab, 20:1393-1408.

Alexi T, Borlongan CV, Faull RL, Williams CE, Clark RG, Gluckman PD, Hughes PE (2000) Neuroprotective strategies for basal ganglia degeneration: Parkinson's and Huntington's diseases. Prog Neurobiol, 60:409-470.

Anderson AJ, Ruehl WW, Fleischmann LK, Stenstrom K, Entriken TL, Cummings BJ (2000) DNA damage and apoptosis in the aged canine brain: relationship to Abeta deposition in the absence of neuritic pathology. Prog Neuropsychopharmacol Biol Psychiatry, 24:787-799.

Armstrong JS (2006) Mitochondrial membrane permeabilization: the sine qua non for cell death. Bioessays, 28:253-260.

Baldi A, Calia E, Ciampini A, Riccio M, Vetuschi A, Persico AM, Keller F (2000) Deafferentation-induced apoptosis of neurons in thalamic somatosensory nuclei of the newborn rat: critical period and rescue from cell death by peripherally applied neurotrophins. Eur JNeurosci, 12:2281-2290.

Barde YA, Edgar D, Thoenen H (1982) Purification of a new neurotrophic factor from mammalian brain. EMBO J, 1:549-553.

Behl C (2000) Apoptosis and Alzheimer's disease. J Neural Transm, 107:1325-1344.

Becker EB, Bonni A (2004) Cell cycle regulation of neuronal apoptosis in development and disease. Prog Neurobiol, 72:1-25.

Bittigau P, Sifringer M, Pohl D, Stadthaus D, Ishimaru M, Shimizu H, Ikeda M, Lang D, Speer A, Olney JW, Ikonomidou C (1999) Apoptotic neurodegeneration following trauma is markedly enhanced in the immature brain. Ann Neurol, 45:724-735.

Bredesen DE (2000) Apoptosis: overview and signal transduction pathways. J Neurotrauma, 17:801-810.

Burek M J, Oppenheim RW (1996) Programmed cell death in the developing nervous system. Brain Pathol, 6:427-446.

Burke RE, Franklin SO, Inturrisi CE (1994) Acute and persistent suppression of preproenkephalin mRNA expression in the striatum following developmental hypoxic-ischemic injury. J Neurochem, 62:1878-1886.

Burke RE (2004) Ontogenic cell death in the nigrostriatal system. Cell Tissue Res, 318:63-72.

Buss RR, Sun W, Oppenheim RW (2006) Adaptive roles of programmed cell death during nervous system development. Annu Rev Neurosci, 29:1-35.

Chao MV, Rajagopal R, Lee FS (2006) Neurotrophin signalling in health and disease. Clin Sci (Lond), 110:167-173.

Chipuk JE, Bouchier-Hayes L, Green DR (2006) Mitochondrial outer membrane permeabilization during apoptosis: the innocent bystander scenario. Cell Death Differ, 13:1396-1402.

Clarke PG (1985) Neuronal death in the development of the vertebrate nervous system. Trends Neurosci, 8:345-349.

Cui Q (2006) Actions of neurotrophic factors and their signaling pathways in neuronal survival and axonal regeneration. Mol Neurobiol, 33:155-179.

Danial NN, Korsmeyer SJ (2004) Cell death: critical control points. Cell, 116:205-219.

Davies AM (2003) Regulation of neuronal survival and death by extracellular signals during development. EMBO J, 22:2537-2545.

de la Rosa EJ, de Pablo F (2000) Cell death in early neural development: Beyond the neurotrophic theory. Trends Neurosci, 23:454-458.

Denault JB, Salvesen GS (2002) Caspases: keys in the ignition of cell death. Chem Rev, 102:4489-4500.

Ernfors P, Ibanez CF, Ebendal T, Olson L, Persson H (1990) Molecular cloning and neurotrophic activities of a protein with structural similarities to nerve growth factor: developmental and topographical expression in the brain. Proc Natl Acad Sci, 14:5454-5458.

Fan TJ, Han LH, Cong RS, Liang J (2005) Caspase family proteases and apoptosis. Acta Biochim Biophys Sin (Shanghai), 37:719-727.

Ferrer I, Serrano T, Soriano E (1990) Naturally occurring cell death in the subicular complex and hippocampus in the rat during development. Neurosci Res, 8:60-66.

Ferrer I, Tortosa A, Blanco R, Martin F, Serrano T, Planas A, Macaya A (1994) Naturally occurring cell death in the developing cerebralcortex of the rat. Evidence of apoptosis-associated internucleosomal DNA fragmentation. Neurosci Lett, 182:77-79.

Ferrer I, Blanco R, Cutillas B, Ambrosio S (2000) Fas and Fas-L expression in Huntington's disease and Parkinson's disease. Neuropathol Appi Neurobiol, 26:424-433

Ferrer I (2002) Synaptic pathology and cell death in the cerebellum in Creutzfeldt-Jakob disease. Cerebellum, 3:213-222.

Fischer U, Janicke RU, Schulze-Osthoff Κ (2003) Many cuts to ruin: a comprehensive update of caspase substrates. Cell Death Differ, 10:76-100.

Fiske and Brunjes (2001) Cell death in the developing and sensory deprived rat olfactory bulb. J Comp Neurol, 431:311-319.

Gavrieli Y, Sherman Y, Ben-Sasson SA (1992) Identification of programmed cell death in situ via specific labelling of nuclear DNA fragmentation. J Cell Biol, 119:493-501.

Hacker G (2000) The morphology of apoptosis. Cell Tissue Res, 301:5-17.

Hallbook F, Ibanez CF, Persson H (1991) Evolutionary studies of the nerve growth factor family reveal a novel member abundantly expressed in Xenopus ovary. Neuron, 5:845-858.

Hengartner MO (2000) The biochemistry of apoptosis. Nature, 407:770-776.

Herrup K, Shojaeian-Zanjani H, Panzini L, Sunter K, Mariani J (1996) The numerical matching of source and target populations in the CNS: the inferior olive to Purkinje cell projection. Brain Res Dev Brain Res, 96:28-35.

Honig LS, Rosenberg RN (2000) Apoptosis and neurologic disease. Am J Med, 108:317-330.

Horvitz HR (2003) Nobel lecture. Worms, life and death. Biosci Rep, 23:239-303.

Jäättelä M (2002) Programmed cell death: many ways for cells to die decently. Ann Med, 34:480-488.

Jackson-Lewis V, Vila M, Djaldetti R, Guegan C, Liberatore G, Liu J, O'Malley KL, Burke RE, Przedborski S (2000) Developmental cell death in dopaminergic neurons of the substantia nigra of mice. J Comp Neurol, 424:476-488.

Jeon BS, Kholodilov NG, Oo TF, Kim SY, Tomaselli KJ, Srinivasan A, Stefanis L, Burke RE (1999) Activation of caspase-3 in developmental models of programmed cell death in neurons of the substantia nigra. J Neurochem, 73:322-333.

Kerr JF, Wyllie AH, Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer, 26:239-257.

Kiatipattanasakul W, Nakamura S, Hossain MM, Nakayama H, Uchino T, Shumiya S, Goto N, Doi Κ (1996) Apoptosis in the aged dog brain. Acta Neuropathol, 92:242-248.

Kiechle T, Dedeoglu A, Kubilus J, Kowall NW, Beai MF, Friedlander RM, Hersch SM, Ferrante RJ (2002) Cytochrome C and caspase-9 expression in Huntington's disease. Neuromolecular Med, 1:183-195.

Krajewska M, Rosenthal RE, Mikolajczyk J, Stennicke HR, Wiesenthal Τ, Mai J, Naito M, Salvesen GS, Reed JC, Fiskum G, Krajewski S (2004) Early processing of Bid and caspase-6, -8, -10, -14 in the canine brain during cardiac arrest and resuscitation. Exp Neurol, 189:261-279.

Krantic S, Mechawar N, Reix S, Quirion R (2005) Molecular basis of programmed cell death involved in neurodegeneration. Trends Neurosci, 28:670-676.

Kuida K, Zheng TS, Na S, Kuan C, Yang D, Karasuyama H, Rakic P, Flavell RA (1996) Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature, 384:368-372.

Leist M, Jäättelä M (2001) Four deaths and a funeral: from caspases to alternative mechanisms. Nat Rev Mol Cell Biol, 2:589-598.

Levi-Montalcini R (1987) The nerve growth factor: thirty-five years later. EMBO J, 6:1145-1154.

Linden R (1994) The survival of developing neurons: a review of afferent control. Neuroscience, 58:671-682.

Lindsten Τ, Zong WX, Thompson CB (2005) Defining the role of the Bcl-2 family of proteins in the nervous system. Neuroscientist, 11:10-15.

Loopuijt LD, Villablanca JR, Hovda DA, Huang E, Mancuso S (1997) The effect of neocortical lesions on the number of cells in neonatal or adult feline caudate nucleus: comparison to fetal lesions. Neuroscience, 77:403-418.

Los M, Wesselborg S, Schulze-Osthoff Κ (1999) The role of caspases in development, immunity and apoptotic signal transduction: lessons from knockout mice. Immunity, 10:629-639.

Lossi L, Gambino G (2008) Apoptosis of the cerebellar neurons. Histol Histopathol, 23:367-380.

Marti MJ, James CJ, Oo TF, Kelly WJ, Burke RE (1997) Early developmental destruction of terminals in the striatal targetinduces apoptosis in dopamine neurons of the substantia nigra. J Neurosci, 17:2030-2039.

Marti MJ, Saura J, Burke RE, Jackson-Lewis V, Jimenez A, Bonastre M, Tolosa E (2002) Striatal 6-hydroxydopamine induces apoptosis of nigral neurons in the adult rat. Brain Res, 958:185-191.

Mattson MP (2000) Apoptosis in neurodegenerative disorders. Nat Rev Mol Cell Biol, 1:120-129.

Mellios Κ, Sophou S, Latsari M, Dinopoulos A, Antonopoulos J, Parnavelas JG, Dori I (2005) Apoptosis in the rat striatum during development and following lesions of afferent and efferent connections. In: Abstract Viewer/Itinerary Planner Society for Neuroscience, 35th Annual Meeting, (Washington DC) U.S.A., Program No. 250.11. 2005.

Moro L, Martins AS, Alves CM, Santos FG, Del Puerto HL,Vasconcelos AC (2003) Apoptosis in the cerebellum of dogs with distemper. J Vet Med Β Infect Dis Vet Public Health, 50:221-225.

Nieto-Sampedro M, Manthrope M, Barbin G, Varon S, Cotman CW(1983) Injury-induced neuronotrophic activity in adult rat brain: correlation with survival of delayed implants in the wound cavity. J Neurosci, 3:2219-2229.

Northington FJ, Ferriero DM, Flock DL, Martin LJ (2001) Delayed neuro degeneration in neonatal rat thalamus after hypoxiaischemia is apoptosis. J Neurosci, 21:1931-1938.

Nunez JL, Lauschke DM, Juraska JM (2001) Cell death in the development of the posterior cortex in male and female rats. J Comp Neurol, 436:32-41.

Oo TF, Burke RE (1997) The time course of developmental cell deathin phenotypically defined dopaminergic neurons of the substantia nigra. Brain Res Dev Brain Res, 98:191-196.

Oppenheim RW (1991) Cell death during development of the nervoussystem. Annu Rev Neurosci, 14:453-501.

Plaschke M, Kasper EM, Naumann Τ, Frotscher M (1994) Survival and transmitter expression of rat cholinergic medial septal neurons despite removal of hippocampus in the early postnatal period. Neurosci Lett, 176:243-246.

Porter AG, Jänicke RU (1999) Emerging roles of caspase-3 in apoptosis. Cell Death Differ, 6:99-104.

Repici M, Atzori C, Migheli A, Vercelli A (2003) Molecular mechanisms of neuronal death in the dorsal lateral geniculate nucleus following visual cortical lesions. Neuroscience, 117:859-867.

Sandy JR, Slocombe RE, Mitten RW, Jedwab D (2002) Cerebellar abiotrophy in a family of Border Collie dogs.Vet Pathol, 39:736-738.

Shiozaki EN, Shi Y (2004) Caspases, IAPs and Smac/DIABLO: mechanisms from structural biology. Trends Biochem Sci, 29:486-494.

Sophou S, Dori I, Antonopoulos J, Parnavelas JG, Dinopoulos A (2006) Apoptosis in the rat basal forebrain during development and following lesions of connections. Eur J Neurosci, 24:573-585.

Spreafico R, Frassoni C, Arcelli P, Selvaggio M, DeBaisi S (1995) In situ labelling of apoptotic cell death in the cerebral cortex and thalamus of rats during development. J Comp Neurol, 363:281-295.

Stefanis L (2005) Caspase-dependent and -independent neuronal death: two distinct pathways to neuronal injury. Neuroscientist, 11:50-62.

Tanaka M, Momoi T, Marunouchi Τ (2000) In situ detection of activated caspase-3 in apoptotic granule neurons in the developing cerebellum in slice cultures and in vivo. Brain Res Dev Brain Res, 121:223-228.

Theerasurakarn S, Ubol S (1998) Apoptosis induction in brain during the fixed strain of rabies infection correlates with onset and severity of illness. J Neurovirol, 4:407-414.

Thoenen H, Sendtner M (2002) Neurotrophins: from enthusiastic expectations through sobering experiences to rational therapeutic approaches. Nat Neurosci, 5 (Suppl): 1046-1050.

Yakovlev AG, Faden AI (2004) Mechanisms of neural cell death: implications for development of neuroprotective treatment strategies. NeuroRx, 1:5-16.

Yeo W, Gautier J (2004) Early neural cell death: dying to become neurons. Dev Biol, 274:233-244.

Yuan J, Yankner BA (2000) Apoptosis in the nervous system. Nature, 407:802-809.

Zacharaki T, Sophou S, Dinopoulos A, Antonopoulos J, Parnavelas JG, and Dori I, (2005). Apoptosis following deafferentation and target deprivation in the immature rat dorsal lateral geniculate nucleus. In: Abstracts of the 19th Meeting of the Hellenic Society

for Neuroscience, (Patra) Greece, pp.93-95.

Zietlow R, Lane EL, Dunnett SB, Rosser AE (2008) Human stem cells for CNS repair. Cell Tissue Res, 331:301-322.


Refbacks

  • There are currently no refbacks.


Copyright (c) 2018 I. DORI (Ι. ΔΩΡΗ), T. ZACHARAKI (Θ. ΖΑΧΑΡΑΚΗ)

Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.