Advertisement

Age-Dependence of Neuronal Apoptosis and of Caspase Activation

  • Denson G. Fujikawa
Chapter

Abstract

A widely accepted morphological classification of cell death divides it into three types: apoptosis, autophagy and necrosis. Research into the biochemical basis of cell death began with apoptosis, and in recent years the programmed mechanisms contributing to cell death and apoptosis became synonymous. This has created confusion, because “apoptosis” refers to a particular morphology and not to a biochemical pathway. Within the central nervous system, both naturally occurring and pathologically induced neuronal apoptosis occurs during the neonatal period in rodents, and becomes virtually undetectable in adult rodents. In the same way, the caspase-dependent programmed cell death pathways are also most prominent in neonatal rodents, and also disappear in adult rodents, although there are earlier studies to the contrary. In adult rodents, acute neuronal injury induces neuronal necrosis, which involves caspase-independent programmed cell death mechanisms.

Keywords

Cerebral Ischemia Status Epilepticus Adult Rodent Lysosomal Cathepsin Flocculent Density 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Andrabi SA, Kim S-W, Wang H, Koh DW, Sasaki M, Klaus JA, Otsuka T, Zhang Z, Koehler RC, Hurn PD, Poirier GG, Dawson VL, Dawson TM (2006) Poly(ADP-ribose) (PAR) polymer is a death signal. Proc Natl Acad Sci USA 103:18308–18313PubMedCrossRefGoogle Scholar
  2. Auer RN, Kalimo H, Olsson Y, Siesjo BK (1985a) The temporal evolution of hypoglycemic brain damage. I. Light- and electron-microscopic findings in the rat cerebral cortex. Acta Neuropathol (Berl) 67:13–24Google Scholar
  3. Auer RN, Kalimo H, Olsson Y, Siesjo BK (1985b) The temporal evolution of hypoglycemic brain damage. II. Light- and electron-microscopic findings in the hippocampal gyrus and subiculum of the rat. Acta Neuropathol (Berl) 67:25–36Google Scholar
  4. Boehning D, Patterson RL, Sedaghat L, Glebova NO, Kurosaki T, Snyder SH (2003) Cytochrome c binds to inositol (1, 4, 5) trisphosphate receptors, amplifying calcium-dependent apoptosis. Nat Cell Biol 5:1051–1061PubMedCrossRefGoogle Scholar
  5. Brown AW, Brierley JB (1972) Anoxic-ischaemic cell change in rat brain light microscopic and fine-structural observations. J Neurol Sci 16:59–84PubMedCrossRefGoogle Scholar
  6. Brown AW, Brierley JB (1973) The earliest alterations in rat neurones and astrocytes after anoxia-ischaemia. Acta Neuropathol 23:9–22PubMedCrossRefGoogle Scholar
  7. Cao G, Xing J, Xiao X, Liou AK, Gao Y, Yin XM, Clark RS, Graham SH, Chen J (2007) Critical role of calpain I in mitochondrial release of apoptosis-inducing factor in ischemic neuronal injury. J Neurosci 27:9278–9293PubMedCrossRefGoogle Scholar
  8. Chen J, Nagayama T, Jin K, Stetler RA, Zhu RL, Graham SH, Simon RP (1998) Induction of caspase-3-like protease may mediate delayed neuronal death in the hippocampus after transient cerebral ischemia. J Neurosci 18:4914–4928PubMedGoogle Scholar
  9. Clarke PGH (1990) Developmental cell death: morphological diversity and multiple mechanisms. Anat Embryol 181:195–213PubMedCrossRefGoogle Scholar
  10. Cohen GM (1997) Caspases: the executioners of apoptosis. Biochem J 326:1–16PubMedGoogle Scholar
  11. Colbourne F, Sutherland GR, Auer RN (1999) Electron microscopic evidence against apoptosis as the mechanism of neuronal death in global ischemia. J Neurosci 19:4200–4210PubMedGoogle Scholar
  12. Ding WX, Shen HM, Ong CN (2002) Calpain activation after mitochondrial permeability transition in microcystin-induced cell death in rat hepatocytes. Biochem Biophys Res Commun 291:321–331PubMedCrossRefGoogle Scholar
  13. Earnshaw WC, Martins LC, Kaufmann SH (1999) Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Annu Rev Biochem 68:383–424PubMedCrossRefGoogle Scholar
  14. Eliasson MJL, Sampei K, Mandir AS, Hurn PD, Traystman RJ, Bao J, Pieper A, Wang Z-Q, Dawson TM, Snyder SH, Dawson VL (1997) Poly (ADP-ribose) polymerase gene disruption renders mice resistant to cerebral ischemia. Nature Med 3:1089–1095PubMedCrossRefGoogle Scholar
  15. Enari M, Sakahira H, Yokoyama H, Okawa K, Iwamatsu A, Nagata S (1998) A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD. Nature 391:43–50PubMedCrossRefGoogle Scholar
  16. Fujikawa DG (2000) Confusion between neuronal apoptosis and activation of programmed cell death mechanisms in acute necrotic insults. Trends Neurosci 23:410–411PubMedCrossRefGoogle Scholar
  17. Fujikawa DG (2002) Apoptosis: ignoring morphology and focusing on biochemical mechanisms will not eliminate confusion. Trends Pharmacol Sci 23:309–310PubMedCrossRefGoogle Scholar
  18. Fujikawa DG, Shinmei SS, Cai B (1999) Lithium-pilocarpine-induced status epilepticus produces necrotic neurons with internucleosomal DNA fragmentation in adult rats. Eur J Neurosci 11:1605–1614PubMedCrossRefGoogle Scholar
  19. Fujikawa DG, Shinmei SS, Cai B (2000) Kainic acid-induced seizures produce necrotic, not apoptotic, neurons with internucleosomal DNA cleavage: implications for programmed cell death mechanisms. Neuroscience 98:41–53PubMedCrossRefGoogle Scholar
  20. Fujikawa DG, Ke X, Trinidad RB, Shinmei SS, Wu A (2002) Caspase-3 is not activated in seizure-induced neuronal necrosis with internucleosomal DNA cleavage. J Neurochem 83:229–240PubMedCrossRefGoogle Scholar
  21. Fujikawa DG, Shinmei SS, Zhao S, Aviles ER Jr (2007) Caspase-dependent programmed cell death pathways are not activated in generalized seizure-induced neuronal death. Brain Res 1135:206–218PubMedCrossRefGoogle Scholar
  22. Gao G, Dou QP (2000) N-terminal cleavage of bax by calpain generates a potent proapoptotic 18-kDa fragment that promotes bcl-2-independent cytochrome C release and apoptotic cell death. J Cell Biochem 80:53–72PubMedCrossRefGoogle Scholar
  23. Griffiths T, Evans MC, Meldrum BS (1984) Status epilepticus: the reversibility of calcium loading and acute neuronal pathological changes in the rat hippocampus. Neuroscience 12:557–567PubMedCrossRefGoogle Scholar
  24. Hara H, Friedlander RM, Gagliardini V, Ayata C, Fink K, Huang Z, Shimizu-Sasamata M, Yuan J, Moskowitz MA (1997) Inhibition of interleukin-1-beta converting enzyme family proteases reduces ischemic and excitotoxic neuronal damage. Proc Natl Acad Sci USA 94:2007–2012PubMedCrossRefGoogle Scholar
  25. Henshall DC, Chen J, Simon RP (2000) Involvement of caspase-3-like protease in the mechanism of cell death following focally evoked limbic seizures. J Neurochem 74:1215–1223PubMedCrossRefGoogle Scholar
  26. Henshall DC, Bonislawski DP, Skradski SL, Araki T, Lan J-Q, Schindler CK, Meller R, Simon RP (2001a) Formation of the Apaf-1/cytochrome c complex precedes activation of caspase-9 during seizure-induced neuronal death. Cell Death Diff 8:1169–1181CrossRefGoogle Scholar
  27. Henshall DC, Bonislawski DP, Skradski SL, Lan J-Q, Meller R, Simon RP (2001b) Cleavage of Bid may amplify caspase-8-induced neuronal death following focally evoked limbic seizures. Neurobiol Dis 8:568–580PubMedCrossRefGoogle Scholar
  28. Hu BR, Liu CL, Ouyang Y, Blomgren K, Siejö BK (2000) Involvement of caspase-3 in cell death after hypoxia-ischemia declines during brain maturation. J Cereb Blood Flow Metab 20:1294–1300PubMedCrossRefGoogle Scholar
  29. Ikonomidou C, Bosch F, Miksa M, Bittigau P, Vockler V, Dikranian K, Tenkova TI, Stefovska V, Turksi L, Olney JW (1999) Blockade of NMDA receptors and apoptotic neurodegeneration in the developing brain. Science 283:70–74PubMedCrossRefGoogle Scholar
  30. Ingvar M, Morgan PF, Auer RN (1988) The nature and timing of excitotoxic neuronal necrosis in the cerebral cortex, hippocampus and thalamus due to flurothyl-induced status epilepticus. Acta Neuropathol 75:362–369PubMedCrossRefGoogle Scholar
  31. Kerr JFR, Wyllie AH, Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26:239–257PubMedCrossRefGoogle Scholar
  32. Kitanaka C, Kuchino Y (1999) Caspase-independent programmed cell death with necrotic morphology. Cell Death Diff 6:508–515CrossRefGoogle Scholar
  33. Lankiewicz S, Luetjens CM, Bui NT, Krohn AJ, Poppe M, Cole GM, Saido TC, Prehn JHM (2000) Activation of calpain I converts excitotoxic neuron death into a caspase-independent cell death. J Biol Chem 275:17064–17071PubMedCrossRefGoogle Scholar
  34. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES, Wang X (1997) Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91:479–489PubMedCrossRefGoogle Scholar
  35. Liu X, Kim CN, Yang J, Jemmerson R, Wang X (1996) Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86:147–157PubMedCrossRefGoogle Scholar
  36. Liu X, Zou H, Slaughter C, Wang X (1997) DFF, a heterodimeric protein that functions downstream of caspase-3 to trigger DNA fragmentation during apoptosis. Cell 89:175–184PubMedCrossRefGoogle Scholar
  37. Liu X, Peng L, Widlak P, Zou H, Luo X, Garrard WT, Wang X (1998) The 40-kDa subunit of DNA fragmentation factor induces DNA fragmentation and chromatin condensation during apoptosis. Proc Natl Acad Sci USA 95:8461–8466PubMedCrossRefGoogle Scholar
  38. Liu CL, Siesjö BK, Hu BR (2004) Pathogenesis of hippocampal neuronal death after hypoxia-ischemia changes during brain development. Neuroscience 127:113–123PubMedCrossRefGoogle Scholar
  39. Nur-E-Kamal A, Gross SR, Pan Z, Balklava Z, Ma J, Liu LF (2004) Nuclear translocation of cytochrome c during apoptosis. J Biol Chem 279:24911–24914PubMedCrossRefGoogle Scholar
  40. Proskuryakov SY, Knoplyannikov AG, Gabai VL (2003) Necrosis: a specific form of programmed cell death? Exp Cell Res 283:1–16PubMedCrossRefGoogle Scholar
  41. Rubinsztein DC, DiFiglia M, Heintz N, Nixon RA, Qin ZH, Ravikumar B, Stefanis L, Tolkovsky A (2005) Autophagy and its possible roles in nervous system diseases, damage and repair. Autophagy 1:11–22PubMedCrossRefGoogle Scholar
  42. Sakahira H, Enari M, Nagata S (1998) Cleavage of CAD inhibitor in CAD activation and DNA degradation during apoptosis. Nature 391:96–99PubMedCrossRefGoogle Scholar
  43. Sloviter RS, Dean E, Neubort S (1993) Electron microscopic analysis of adrenalectomy-induced hippocampal granule cell degeneration in the rat: apoptosis in the adult central nervous system. J Comp Neurol 330:337–351PubMedCrossRefGoogle Scholar
  44. Sloviter RS, Dean E, Sollas AL, Goodman JH (1996) Apoptosis and necrosis induced in different hippocampal neuron populations by repetitive perforant path stimulation in the rat. J Comp Neurol 366:516–533PubMedCrossRefGoogle Scholar
  45. Susin SA, Lorenzo HK, Zamzami N, Marzo I, Snow BE, Brothers GM, Mangion J, Jacotot E, Costantini P, Loeffler M, Larochette N, Goodlett DR, Aebersold R, Siderovski DP, Penninger JM, Kroemer G (1999) Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397:441–446PubMedCrossRefGoogle Scholar
  46. Syntichaki P, Tavernarakis N (2003) The biochemistry of neuronal necrosis: rogue biology? Nat Rev Neurosci 4:672–684PubMedCrossRefGoogle Scholar
  47. Tsukada T, Watanabe M, Yamashima T (2001) Implications of CAD and DNase II in ischemic neuronal necrosis specific for the primate hippocampus. J Neurochem 79:1196–1206PubMedCrossRefGoogle Scholar
  48. Uchiyama Y, Shibata M, Koike M, Yoshimura K, Sasaki M (2008) Autophagy-physiology and pathophysiology. Histochem Cell Biol 129:407–420PubMedCrossRefGoogle Scholar
  49. Vanlangenakker N, Vanden Berghe T, Krysko D, Festjens N, Vandenabeele P (2008) Molecular mechanisms and pathophysiology of necrotic cell death. Curr Mol Med 8:207–220PubMedCrossRefGoogle Scholar
  50. Volbracht C, Chua BT, Ng CP, Bahr BA, Hong W, Li P (2005) The critical role of calpain versus caspase activation in excitotoxic injury induced by nitric oxide. J Neurochem 93:1280–1292PubMedCrossRefGoogle Scholar
  51. Wyllie AH (1980) Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 284:555–556PubMedCrossRefGoogle Scholar
  52. Wyllie A (1981) Cell death: a new classification separating apoptosis from necrosis. In: Bowen I, Lockshin R (eds) Cell death in biology and pathology. Chapman and Hall, London, pp 9–34Google Scholar
  53. Yamashima T, Kohda Y, Tsuchiya K, Ueno T, Yamashita J, Yoshioka T, Kominami E (1998) Inhibition of ischaemic hippocampal neuronal death in primates with cathepsin B inhibitor CA-074: a novel strategy for neuroprotection based on ‘calpain-cathepsin hypothesis’. Eur J Neurosci 10:1723–1733PubMedCrossRefGoogle Scholar
  54. Yamashima T, Tonchev AB, Tsukada T, Saido TC, Imajoh-Ohmi S, Momoi T, Kominami E (2003) Sustained calpain activation associated with lysosomal rupture executes necrosis of the postischemic CA1 neurons in primates. Hippocampus 13:791–800PubMedCrossRefGoogle Scholar
  55. Yu S-W, Wang H, Poitras MF, Coombs C, Bowers WJ, Federoff HJ, Poirier GG, Dawson TM, Dawson VL (2002) Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science 297:259–263PubMedCrossRefGoogle Scholar
  56. Yu S-W, Andrabi SA, Wang H, Kim NS, Poirier GG, Dawson TM, Dawson VL (2006) Apoptosis-inducing factor mediates poly(ADP-ribose) (PAR) polymer-induced cell death. Proc Natl Acad Sci USA 103:18314–18319PubMedCrossRefGoogle Scholar
  57. Zhao S, Aviles ER Jr, Fujikawa DG. Nuclear translocation of mitochondrial cytochrome c and lysosomal cathepsins B and D within the first 60 minutes of generalized seizures (submitted for publication).Google Scholar
  58. Zou H, Henzel WJ, Liu X, Lutschg A, Wang X (1997) Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell 90:405–413PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  1. 1.Neurology DepartmentVA Greater Los Angeles Healthcare SystemNorth HillsUSA
  2. 2.Department of Neurology and Brain Research InstituteDavid Geffen School of Medicine, University of CaliforniaLos AngelesUSA

Personalised recommendations