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PMID: 10662823 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Evidence that Wallerian degeneration and localized axon degeneration induced by local neurotrophin deprivation do not involve caspases.

Finn JT, Weil M, Archer F, Siman R, Srinivasan A, Raff MC

Abstract

The selective degeneration of an axon, without the death of the parent neuron, can occur in response to injury, in a variety of metabolic, toxic, and inflammatory disorders, and during normal development. Recent evidence suggests that some forms of axon degeneration involve an active and regulated program of self-destruction rather than a passive "wasting away" and in this respect and others resemble apoptosis. Here we investigate whether selective axon degeneration depends on some of the molecular machinery that mediates apoptosis, namely, the caspase family of cysteine proteases. We focus on two models of selective axon degeneration: Wallerian degeneration of transected axons and localized axon degeneration induced by local deprivation of neurotrophin. We show that caspase-3 is not activated in the axon during either form of degeneration, although it is activated in the dying cell body of the same neurons. Moreover, caspase inhibitors do not inhibit or retard either form of axon degeneration, although they inhibit apoptosis of the same neurons. Finally, we cannot detect cleaved substrates of caspase-3 and its close relatives immunocytochemically or caspase activity biochemically in axons undergoing Wallerian degeneration. Our results suggest that a neuron contains at least two molecularly distinct self-destruction programs, one for caspase-dependent apoptosis and another for selective axon degeneration.

MeSH Terms
Animals Apoptosis Axons/drug effects,pathology,physiology Caspase 3 Caspases/metabolism Cycloheximide/pharmacology Cysteine Proteinase Inhibitors/pharmacology Enzyme Activation Ganglia, Spinal/physiology,physiopathology Mice Mice, Inbred C57BL Nerve Degeneration/physiopathology Nerve Growth Factors/pharmacology,physiology Neurons/physiology Optic Nerve/pathology,physiology,physiopathology Organ Culture Techniques Rats Rats, Sprague-Dawley Retina/drug effects,physiology Sciatic Nerve/pathology,physiology,physiopathology Wallerian Degeneration/physiopathology
Chemicals
Cysteine Proteinase Inhibitors Nerve Growth Factors Cycloheximide Casp3 protein, mouse Casp3 protein, rat Caspase 3 Caspases
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Finn J T
Medical Research Council Laboratory for Molecular Cell Biology, University College London, London WC1E 6BT, United Kingdom. [email protected]
Weil M
Archer F
Siman R
Srinivasan A
Raff M C
References (50)
50 references, click to expand
  1. Block of neuronal apoptosis by a sustained increase of steady-state free Ca2+ concentration.
    Philos Trans R Soc Lond B Biol Sci. 1994 Aug 30;345(1313):251-6 PMID: 7846122
  2. The Bcl-2 protein family: arbiters of cell survival.
    Science. 1998 Aug 28;281(5381):1322-6 PMID: 9735050
  3. A gene affecting Wallerian nerve degeneration maps distally on mouse chromosome 4.
    Proc Natl Acad Sci U S A. 1993 Oct 15;90(20):9717-20 PMID: 8415768
  4. Absence of Wallerian Degeneration does not Hinder Regeneration in Peripheral Nerve.
    Eur J Neurosci. 1989;1(1):27-33 PMID: 12106171
  5. Neonatal motoneurons overexpressing the bcl-2 protooncogene in transgenic mice are protected from axotomy-induced cell death.
    Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):3309-13 PMID: 8159744
  6. Caspases: killer proteases.
    Trends Biochem Sci. 1997 Aug;22(8):299-306 PMID: 9270303
  7. Development of projection neuron types, axon pathways, and patterned connections of the mammalian cortex.
    Neuron. 1993 Jun;10(6):991-1006 PMID: 8318235
  8. Development of sympathetic neurons in compartmentalized cultures. II. Local control of neurite survival by nerve growth factor.
    Dev Biol. 1982 Sep;93(1):13-21 PMID: 7128928
  9. Beta-amyloid induces local neurite degeneration in cultured hippocampal neurons: evidence for neuritic apoptosis.
    Neurobiol Dis. 1998 Nov;5(5):365-78 PMID: 10069579
  10. Calcium-mediated degeneration of the axonal cytoskeleton in the Ola mouse.
    J Neurochem. 1994 Jun;62(6):2472-5 PMID: 8189250
  11. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c.
    Cell. 1996 Jul 12;86(1):147-57 PMID: 8689682
  12. Role of Ced-3/ICE-family proteases in staurosporine-induced programmed cell death.
    J Cell Biol. 1996 Jun;133(5):1041-51 PMID: 8655577
  13. Axon loss in multiple sclerosis.
    Lancet. 1998 Aug 1;352(9125):340-1 PMID: 9717917
  14. Very Slow Retrograde and Wallerian Degeneration in the CNS of C57BL/Ola Mice.
    Eur J Neurosci. 1991;3(1):102-5 PMID: 12106273
  15. Protein or RNA synthesis inhibition induces apoptosis of mature human CD4+ T cell blasts.
    Immunol Lett. 1993 Feb;35(2):125-34 PMID: 7685316
  16. Morphometric analysis of the peripheral neuropathy of AIDS.
    Muscle Nerve. 1998 Sep;21(9):1188-95 PMID: 9703445
  17. Caspase inhibitors block the retinal ganglion cell death following optic nerve transection.
    Brain Res Mol Brain Res. 1999 Apr 6;67(1):36-45 PMID: 10101230
  18. Inhibition of CPP32-like proteases rescues axotomized retinal ganglion cells from secondary cell death in vivo.
    J Neurosci. 1998 Jun 15;18(12):4656-62 PMID: 9614240
  19. Wallerian degeneration in peripheral nerve disease.
    Baillieres Clin Neurol. 1996 Mar;5(1):65-75 PMID: 8732200
  20. Neurites can remain viable after destruction of the neuronal soma by programmed cell death (apoptosis).
    Dev Biol. 1994 Sep;165(1):63-72 PMID: 8088451
  21. An 85-kb tandem triplication in the slow Wallerian degeneration (Wlds) mouse.
    Proc Natl Acad Sci U S A. 1998 Aug 18;95(17):9985-90 PMID: 9707587
  22. Prolonged survival of transected nerve fibres in C57BL/Ola mice is an intrinsic characteristic of the axon.
    J Neurocytol. 1993 May;22(5):311-21 PMID: 8315413
  23. A combinatorial approach defines specificities of members of the caspase family and granzyme B. Functional relationships established for key mediators of apoptosis.
    J Biol Chem. 1997 Jul 18;272(29):17907-11 PMID: 9218414
  24. Activation and cleavage of caspase-3 in apoptosis induced by experimental cerebral ischemia.
    J Neurosci. 1998 May 15;18(10):3659-68 PMID: 9570797
  25. Emerging roles of caspase-3 in apoptosis.
    Cell Death Differ. 1999 Feb;6(2):99-104 PMID: 10200555
  26. Evidence that the Rate of Wallerian Degeneration is Controlled by a Single Autosomal Dominant Gene.
    Eur J Neurosci. 1990;2(5):408-13 PMID: 12106028
  27. Programmed cell death and Bcl-2 protection in the absence of a nucleus.
    EMBO J. 1994 Apr 15;13(8):1899-910 PMID: 8168488
  28. Proteases to die for.
    Genes Dev. 1998 Jun 1;12(11):1551-70 PMID: 9620844
  29. Axotomy-induced axonal degeneration is mediated by calcium influx through ion-specific channels.
    J Neurosci. 1995 Oct;15(10):6445-52 PMID: 7472407
  30. Growth of a rat neuroblastoma cell line in serum-free supplemented medium.
    Proc Natl Acad Sci U S A. 1979 Jan;76(1):514-7 PMID: 284369
  31. Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice.
    Nature. 1996 Nov 28;384(6607):368-72 PMID: 8934524
  32. Motor neuron death induced by axotomy in neonatal mice occurs more slowly in a mutant strain in which Wallerian degeneration is very slow.
    Eur J Neurosci. 1994 Mar 1;6(3):473-7 PMID: 8019683
  33. Constitutive expression of the machinery for programmed cell death.
    J Cell Biol. 1996 Jun;133(5):1053-9 PMID: 8655578
  34. Activation of the CED3/ICE-related protease CPP32 in cerebellar granule neurons undergoing apoptosis but not necrosis.
    J Neurosci. 1997 Jan 15;17(2):553-62 PMID: 8987778
  35. Immunolocalization of caspase proteolysis in situ: evidence for widespread caspase-mediated apoptosis of neurons and glia in the postnatal rat brain.
    Neuroscience. 1999;92(4):1425-42 PMID: 10426497
  36. Essential contribution of caspase 3/CPP32 to apoptosis and its associated nuclear changes.
    Genes Dev. 1998 Mar 15;12(6):806-19 PMID: 9512515
  37. Apoptotic cell death induced by optic nerve lesion in the neonatal rat.
    J Neurosci. 1994 Sep;14(9):5292-301 PMID: 8083737
  38. Glial cells are increased proportionally in transgenic optic nerves with increased numbers of axons.
    J Neurosci. 1996 Mar 15;16(6):2064-73 PMID: 8604051
  39. Regressive events in neurogenesis.
    Science. 1984 Sep 21;225(4668):1258-65 PMID: 6474175
  40. Evidence for synaptic apoptosis.
    Exp Neurol. 1998 Sep;153(1):35-48 PMID: 9743565
  41. ICE, neuronal apoptosis and neurodegeneration.
    Cell Death Differ. 1998 Oct;5(10):823-31 PMID: 10203693
  42. Reactivity of a panel of neurofilament antibodies on phosphorylated and dephosphorylated neurofilaments.
    Eur J Cell Biol. 1986 Oct;42(1):1-9 PMID: 3539605
  43. The rate of Wallerian degeneration in cultured neurons from wild type and C57BL/WldS mice depends on time in culture and may be extended in the presence of elevated K+ levels.
    Eur J Neurosci. 1995 Jul 1;7(7):1596-602 PMID: 7551186
  44. Are caspases involved in the death of cells with a transcriptionally inactive nucleus? Sperm and chicken erythrocytes.
    J Cell Sci. 1998 Sep;111 ( Pt 18):2707-15 PMID: 9718364
  45. In situ immunodetection of activated caspase-3 in apoptotic neurons in the developing nervous system.
    Cell Death Differ. 1998 Dec;5(12):1004-16 PMID: 9894607
  46. Oligodendrocyte apoptosis mediated by caspase activation.
    J Neurosci. 1999 Apr 15;19(8):3043-9 PMID: 10191321
  47. Evidence that Very Slow Wallerian Degeneration in C57BL/Ola Mice is an Intrinsic Property of the Peripheral Nerve.
    Eur J Neurosci. 1990;2(9):802-8 PMID: 12106282
  48. Effects of sphingosine, staurosporine, and phorbol ester on neurites of rat sympathetic neurons growing in compartmented cultures.
    J Neurosci. 1991 Apr;11(4):1126-39 PMID: 2010808
  49. Bcl-2 overexpression prevents motoneuron cell body loss but not axonal degeneration in a mouse model of a neurodegenerative disease.
    J Neurosci. 1995 Nov;15(11):7727-33 PMID: 7472523
  50. Amyloid beta-peptide induces apoptosis-related events in synapses and dendrites.
    Brain Res. 1998 Oct 5;807(1-2):167-76 PMID: 9757026
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
0270-6474
Published
2000-02-15
Pages
1333-41
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6772375
Subset
IM
Grants
Wellcome Trust · United Kingdom
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