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PMID: 16772866 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Review

Autophagic stress in neuronal injury and disease.

Journal of neuropathology and experimental neurology ·Vol. 65 ·No. 5 ·2006-05-00 ·Pages 423-32

Chu CT

Abstract

Autophagy is the regulated process by which cytoplasmic organelles and long-lived proteins are delivered for lysosomal degradation. Increased numbers of autophagosomes and autolysosomes often represent prominent ultrastructural features of degenerating or dying neurons. This morphology is characteristic not only of neurons undergoing pathologic degeneration, but also during developmental programmed cell death of some neuronal populations. In recent years, a growing number of reports highlight potentially important roles for autophagy-related processes in relation to protein aggregation, regulated cell death pathways, and neurodegeneration. While starvation-induced autophagy involves nonselective bulk degradation of cytoplasm, mechanisms that regulate selective targeting of damaged organelles form an emerging area. As the study of autophagy evolves from physiologic homeostasis to pathologic situations, consideration of terminology and definitions becomes important. Increased autophagic vacuoles do not necessarily correlate with increased autophagic activity or flux. Instead, the striking accumulation of autophagic vacuoles in dying or degenerating neurons likely reflects an imbalance between the rates of autophagic sequestration and completion of the degradative process. In other words, these cells can be thought of as undergoing "autophagic stress." The concept of autophagic stress may reconcile apparently conflicting roles of autophagy-related processes in adaptive, homeostatic responses and in pathways of neurodegeneration and cell death.

MeSH Terms
Animals Autophagy/physiology Cell Death/physiology Humans Lysosomal Storage Diseases/physiopathology Models, Biological Neurodegenerative Diseases/physiopathology Signal Transduction/physiology Stress, Physiological
Authors & Affiliations
1 authors, click to expand affiliations / ORCID
Chu Charleen T
Department of Pathology/Division of Neuropathology, Department of Ophthalmology, Center for Neuroscience (CNUP), Pittsburgh Institute for Neurodegenerative Diseases (PIND), University of Pittsburgh School of Medicine, Pennsylvania, USA. ctc4@pitt.edu
References (114)
114 references, click to expand
  1. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy.
    Cell. 2005 Sep 23;122(6):927-39 PMID: 16179260
  2. Autophagy in cell death: an innocent convict?
    J Clin Invest. 2005 Oct;115(10):2679-88 PMID: 16200202
  3. Macroautophagy--a novel Beta-amyloid peptide-generating pathway activated in Alzheimer's disease.
    J Cell Biol. 2005 Oct 10;171(1):87-98 PMID: 16203860
  4. Autophagy and signaling: their role in cell survival and cell death.
    Cell Death Differ. 2005 Nov;12 Suppl 2:1509-18 PMID: 16247498
  5. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death.
    J Cell Biol. 2005 Nov 21;171(4):603-14 PMID: 16286508
  6. HDAC6 and microtubules are required for autophagic degradation of aggregated huntingtin.
    J Biol Chem. 2005 Dec 2;280(48):40282-92 PMID: 16192271
  7. Participation of autophagy in storage of lysosomes in neurons from mouse models of neuronal ceroid-lipofuscinoses (Batten disease).
    Am J Pathol. 2005 Dec;167(6):1713-28 PMID: 16314482
  8. Molecular mechanisms and regulation of specific and nonspecific autophagy pathways in yeast.
    J Biol Chem. 2005 Dec 23;280(51):41785-8 PMID: 16230342
  9. Bafilomycin A1 inhibits chloroquine-induced death of cerebellar granule neurons.
    Mol Pharmacol. 2006 Apr;69(4):1125-36 PMID: 16391239
  10. Functional repression of cAMP response element in 6-hydroxydopamine-treated neuronal cells.
    J Biol Chem. 2006 Jun 30;281(26):17870-81 PMID: 16621793
  11. Maturation of autophagic vacuoles in Mammalian cells.
    Autophagy. 2005 Apr;1(1):1-10 PMID: 16874026
  12. Autophagy and its possible roles in nervous system diseases, damage and repair.
    Autophagy. 2005 Apr;1(1):11-22 PMID: 16874045
  13. Does autophagy contribute to cell death?
    Autophagy. 2005 Jul;1(2):66-74 PMID: 16874022
  14. Lysosomal turnover, but not a cellular level, of endogenous LC3 is a marker for autophagy.
    Autophagy. 2005 Jul;1(2):84-91 PMID: 16874052
  15. Tracker dyes to probe mitochondrial autophagy (mitophagy) in rat hepatocytes.
    Autophagy. 2006 Jan-Mar;2(1):39-46 PMID: 16874071
  16. The role of macroautophagy in the ageing process, anti-ageing intervention and age-associated diseases.
    Int J Biochem Cell Biol. 2004 Dec;36(12):2392-404 PMID: 15325580
  17. Autophagy is activated by apoptotic signalling in sympathetic neurons: an alternative mechanism of death execution.
    Mol Cell Neurosci. 1999 Sep;14(3):180-98 PMID: 10576889
  18. Distinct classes of phosphatidylinositol 3'-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells.
    J Biol Chem. 2000 Jan 14;275(2):992-8 PMID: 10625637
  19. The lysosomotropic agent monodansylcadaverine also acts as a solvent polarity probe.
    J Histochem Cytochem. 2000 Feb;48(2):251-8 PMID: 10639491
  20. Neuromelanin biosynthesis is driven by excess cytosolic catecholamines not accumulated by synaptic vesicles.
    Proc Natl Acad Sci U S A. 2000 Oct 24;97(22):11869-74 PMID: 11050221
  21. Caspase-3 activation and caspase-like proteolytic activity in human perinatal hypoxic-ischemic brain injury.
    Acta Neuropathol. 2002 Jan;103(1):66-73 PMID: 11841033
  22. The first molecular evidence that autophagy relates rimmed vacuole formation in chloroquine myopathy.
    J Biochem. 2002 May;131(5):647-51 PMID: 11983070
  23. Mitochondrial disappearance from cells: a clue to the role of autophagy in programmed cell death and disease?
    Biochimie. 2002 Feb-Mar;84(2-3):233-40 PMID: 12022954
  24. Regulation of an ATG7-beclin 1 program of autophagic cell death by caspase-8.
    Science. 2004 Jun 4;304(5676):1500-2 PMID: 15131264
  25. Pivotal role of the cell death factor BNIP3 in ceramide-induced autophagic cell death in malignant glioma cells.
    Cancer Res. 2004 Jun 15;64(12):4286-93 PMID: 15205343
  26. Alfy, a novel FYVE-domain-containing protein associated with protein granules and autophagic membranes.
    J Cell Sci. 2004 Aug 15;117(Pt 18):4239-51 PMID: 15292400
  27. Autophagy, proteasomes, lipofuscin, and oxidative stress in the aging brain.
    Int J Biochem Cell Biol. 2004 Dec;36(12):2376-91 PMID: 15325579
  28. Apoptosis, autophagy, and more.
    Int J Biochem Cell Biol. 2004 Dec;36(12):2405-19 PMID: 15325581
  29. LC3 conjugation system in mammalian autophagy.
    Int J Biochem Cell Biol. 2004 Dec;36(12):2503-18 PMID: 15325588
  30. Microtubule disruption inhibits autophagosome-lysosome fusion: implications for studying the roles of aggresomes in polyglutamine diseases.
    Int J Biochem Cell Biol. 2004 Dec;36(12):2541-50 PMID: 15325591
  31. Involvement of macroautophagy in the dissolution of neuronal inclusions.
    Int J Biochem Cell Biol. 2004 Dec;36(12):2551-62 PMID: 15325592
  32. Autophagy is a part of ultrastructural synaptic pathology in Creutzfeldt-Jakob disease: a brain biopsy study.
    Int J Biochem Cell Biol. 2004 Dec;36(12):2563-73 PMID: 15325593
  33. Impaired degradation of mutant alpha-synuclein by chaperone-mediated autophagy.
    Science. 2004 Aug 27;305(5688):1292-5 PMID: 15333840
  34. Uth1p is involved in the autophagic degradation of mitochondria.
    J Biol Chem. 2004 Sep 10;279(37):39068-74 PMID: 15247238
  35. Peroxisome turnover by micropexophagy: an autophagy-related process.
    Trends Cell Biol. 2004 Sep;14(9):515-23 PMID: 15350980
  36. Studies on cellular autophagocytosis. Cyclic AMP- and dibutyryl cyclic AMP-stimulated autophagy in rat liver.
    Am J Pathol. 1973 Sep;72(3):521-40 PMID: 4125701
  37. Studies on cellular autophagocytosis. The relationship of autophagocytosis to protein synthesis and to energy metabolism in rat liver and flounder kidney tubules in vitro.
    Am J Pathol. 1973 Dec;73(3):641-70 PMID: 4767257
  38. Ultrastructural differences during embryonic cell death in normal and peripherally deprived ciliary ganglia.
    J Cell Biol. 1976 Feb;68(2):339-56 PMID: 942724
  39. Developmental cell death: morphological diversity and multiple mechanisms.
    Anat Embryol (Berl). 1990;181(3):195-213 PMID: 2186664
  40. Studies on the mechanisms of autophagy: maturation of the autophagic vacuole.
    J Cell Biol. 1990 Jun;110(6):1935-45 PMID: 2161853
  41. Inhibition of protein synthesis separates autophagic sequestration from the delivery of lysosomal enzymes.
    J Cell Sci. 1993 Jun;105 ( Pt 2):473-80 PMID: 8408278
  42. Gene expression and cellular content of cathepsin D in Alzheimer's disease brain: evidence for early up-regulation of the endosomal-lysosomal system.
    Neuron. 1995 Mar;14(3):671-80 PMID: 7695914
  43. Monodansylcadaverine (MDC) is a specific in vivo marker for autophagic vacuoles.
    Eur J Cell Biol. 1995 Jan;66(1):3-14 PMID: 7750517
  44. Apoptosis and autophagy in nigral neurons of patients with Parkinson's disease.
    Histol Histopathol. 1997 Jan;12(1):25-31 PMID: 9046040
  45. Phosphoinositide 3-kinases: a conserved family of signal transducers.
    Trends Biochem Sci. 1997 Jul;22(7):267-72 PMID: 9255069
  46. Huntingtin localization in brains of normal and Huntington's disease patients.
    Ann Neurol. 1997 Oct;42(4):604-12 PMID: 9382472
  47. Tor, a phosphatidylinositol kinase homologue, controls autophagy in yeast.
    J Biol Chem. 1998 Feb 13;273(7):3963-6 PMID: 9461583
  48. Mechanisms of MPTP toxicity.
    Mov Disord. 1998;13 Suppl 1:35-8 PMID: 9613716
  49. Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells.
    Cell Struct Funct. 1998 Feb;23(1):33-42 PMID: 9639028
  50. Purification and characterization of autophagosomes from rat hepatocytes.
    Biochem J. 1998 Oct 15;335 ( Pt 2):217-24 PMID: 9761717
  51. Striatal 6-hydroxydopamine induces apoptosis of nigral neurons in the adult rat.
    Brain Res. 2002 Dec 20;958(1):185-91 PMID: 12468044
  52. Role of mitochondrial inner membrane permeabilization in necrotic cell death, apoptosis, and autophagy.
    Antioxid Redox Signal. 2002 Oct;4(5):769-81 PMID: 12470504
  53. Autophagic vacuolar myopathies.
    Curr Neurol Neurosci Rep. 2003 Jan;3(1):64-9 PMID: 12507414
  54. Steroid-triggered programmed cell death of a motoneuron is autophagic and involves structural changes in mitochondria.
    J Comp Neurol. 2003 Mar 17;457(4):384-403 PMID: 12561078
  55. Autophagosome formation in mammalian cells.
    Cell Struct Funct. 2002 Dec;27(6):421-9 PMID: 12576635
  56. Lurcher GRID2-induced death and depolarization can be dissociated in cerebellar Purkinje cells.
    Neuron. 2003 Mar 6;37(5):813-9 PMID: 12628171
  57. At the acidic edge: emerging functions for lysosomal membrane proteins.
    Trends Cell Biol. 2003 Mar;13(3):137-45 PMID: 12628346
  58. Degradation of normal and proliferated peroxisomes in rat hepatocytes: regulation of peroxisomes quantity in cells.
    Microsc Res Tech. 2003 Jun 1;61(2):151-60 PMID: 12740821
  59. A developmentally regulated, neuron-specific splice variant of the variable subunit Bbeta targets protein phosphatase 2A to mitochondria and modulates apoptosis.
    J Biol Chem. 2003 Jul 4;278(27):24976-85 PMID: 12716901
  60. Alpha-Synuclein is degraded by both autophagy and the proteasome.
    J Biol Chem. 2003 Jul 4;278(27):25009-13 PMID: 12719433
  61. Dopamine induces autophagic cell death and alpha-synuclein increase in human neuroblastoma SH-SY5Y cells.
    J Neurosci Res. 2003 Aug 1;73(3):341-50 PMID: 12868068
  62. N-methyl-d-aspartate-triggered neuronal death in organotypic hippocampal cultures is endocytic, autophagic and mediated by the c-Jun N-terminal kinase pathway.
    Eur J Neurosci. 2003 Aug;18(3):473-85 PMID: 12911744
  63. A unified nomenclature for yeast autophagy-related genes.
    Dev Cell. 2003 Oct;5(4):539-45 PMID: 14536056
  64. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing.
    EMBO J. 2000 Nov 1;19(21):5720-8 PMID: 11060023
  65. Erk1/2-dependent phosphorylation of Galpha-interacting protein stimulates its GTPase accelerating activity and autophagy in human colon cancer cells.
    J Biol Chem. 2000 Dec 15;275(50):39090-5 PMID: 10993892
  66. Molecular dissection of autophagy: two ubiquitin-like systems.
    Nat Rev Mol Cell Biol. 2001 Mar;2(3):211-6 PMID: 11265251
  67. Mitochondria are selectively eliminated from eukaryotic cells after blockade of caspases during apoptosis.
    Curr Biol. 2001 Mar 6;11(5):361-5 PMID: 11267874
  68. Direct binding and functional coupling of alpha-synuclein to the dopamine transporters accelerate dopamine-induced apoptosis.
    FASEB J. 2001 Apr;15(6):916-26 PMID: 11292651
  69. Beclin-phosphatidylinositol 3-kinase complex functions at the trans-Golgi network.
    EMBO Rep. 2001 Apr;2(4):330-5 PMID: 11306555
  70. Experimental models of Parkinson's disease.
    Nat Rev Neurosci. 2001 May;2(5):325-34 PMID: 11331916
  71. Accumulation of mutant huntingtin fragments in aggresome-like inclusion bodies as a result of insufficient protein degradation.
    Mol Biol Cell. 2001 May;12(5):1393-407 PMID: 11359930
  72. Autophagy delays sulindac sulfide-induced apoptosis in the human intestinal colon cancer cell line HT-29.
    Exp Cell Res. 2001 Aug 15;268(2):139-49 PMID: 11478840
  73. The autophagosomal-lysosomal compartment in programmed cell death.
    Cell Death Differ. 2001 Jun;8(6):569-81 PMID: 11536007
  74. Caspases, apoptosis, and Alzheimer disease: causation, correlation, and confusion.
    J Neuropathol Exp Neurol. 2001 Sep;60(9):829-38 PMID: 11556539
  75. Autophagic cell death and its execution by lysosomal cathepsins.
    Arch Histol Cytol. 2001 Aug;64(3):233-46 PMID: 11575420
  76. Expression of A53T mutant but not wild-type alpha-synuclein in PC12 cells induces alterations of the ubiquitin-dependent degradation system, loss of dopamine release, and autophagic cell death.
    J Neurosci. 2001 Dec 15;21(24):9549-60 PMID: 11739566
  77. Molecular crosstalk between p70S6k and MAPK cell signaling pathways.
    Biochem Biophys Res Commun. 2002 Apr 26;293(1):463-9 PMID: 12054624
  78. Autophagy in neurons: a review.
    Histol Histopathol. 2002;17(3):897-908 PMID: 12168801
  79. Lipofuscin: mechanisms of age-related accumulation and influence on cell function.
    Free Radic Biol Med. 2002 Sep 1;33(5):611-9 PMID: 12208347
  80. A novel protein complex linking the delta 2 glutamate receptor and autophagy: implications for neurodegeneration in lurcher mice.
    Neuron. 2002 Aug 29;35(5):921-33 PMID: 12372286
  81. Methamphetamine-induced degeneration of dopaminergic neurons involves autophagy and upregulation of dopamine synthesis.
    J Neurosci. 2002 Oct 15;22(20):8951-60 PMID: 12388602
  82. Loss of cardiolipin and mitochondria during programmed neuronal death: evidence of a role for lipid peroxidation and autophagy.
    Neuroscience. 2002;115(2):587-602 PMID: 12421624
  83. Cytoplasmic aggregates of phosphorylated extracellular signal-regulated protein kinases in Lewy body diseases.
    Am J Pathol. 2002 Dec;161(6):2087-98 PMID: 12466125
  84. Diversity in the mechanisms of neuronal cell death.
    Neuron. 2003 Oct 9;40(2):401-13 PMID: 14556717
  85. Alternative programs of cell death in developing retinal tissue.
    J Biol Chem. 2003 Oct 24;278(43):41938-46 PMID: 12917395
  86. Emerging role for autophagy in the removal of aggresomes in Schwann cells.
    J Neurosci. 2003 Nov 19;23(33):10672-80 PMID: 14627652
  87. Critical function of endogenous XIAP in regulating caspase activation during sympathetic neuronal apoptosis.
    J Cell Biol. 2003 Nov 24;163(4):789-99 PMID: 14623868
  88. Autophagy regulates the processing of amino terminal huntingtin fragments.
    Hum Mol Genet. 2003 Dec 15;12(24):3231-44 PMID: 14570716
  89. Localization of phosphorylated ERK/MAP kinases to mitochondria and autophagosomes in Lewy body diseases.
    Brain Pathol. 2003 Oct;13(4):473-81 PMID: 14655753
  90. Class III phosphoinositide 3-kinase--Beclin1 complex mediates the amino acid-dependent regulation of autophagy in C2C12 myotubes.
    Biochem J. 2003 Dec 15;376(Pt 3):577-86 PMID: 12967324
  91. GDNF-deprived sympathetic neurons die via a novel nonmitochondrial pathway.
    J Cell Biol. 2003 Dec 8;163(5):987-97 PMID: 14657232
  92. Methamphetamine produces neuronal inclusions in the nigrostriatal system and in PC12 cells.
    J Neurochem. 2004 Jan;88(1):114-23 PMID: 14675155
  93. Amino acids and insulin control autophagic proteolysis through different signaling pathways in relation to mTOR in isolated rat hepatocytes.
    J Biol Chem. 2004 Feb 27;279(9):8452-9 PMID: 14610086
  94. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker.
    Mol Biol Cell. 2004 Mar;15(3):1101-11 PMID: 14699058
  95. Development by self-digestion: molecular mechanisms and biological functions of autophagy.
    Dev Cell. 2004 Apr;6(4):463-77 PMID: 15068787
  96. Alternative, nonapoptotic programmed cell death: mediation by arrestin 2, ERK2, and Nur77.
    J Biol Chem. 2004 Apr 23;279(17):17543-53 PMID: 14769794
  97. Proteasome inhibition alters neural mitochondrial homeostasis and mitochondria turnover.
    J Biol Chem. 2004 May 14;279(20):20699-707 PMID: 14742431
  98. The p75 neurotrophin receptor can induce autophagy and death of cerebellar Purkinje neurons.
    J Neurosci. 2004 May 12;24(19):4498-509 PMID: 15140920
  99. Oxidative neuronal injury. The dark side of ERK1/2.
    Eur J Biochem. 2004 Jun;271(11):2060-6 PMID: 15153095
  100. Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease.
    Nat Genet. 2004 Jun;36(6):585-95 PMID: 15146184
  101. Neuronal death in the central nervous system during development.
    Biomed Pharmacother. 1998;52(9):356-62 PMID: 9856281
  102. Autophagy: many paths to the same end.
    Mol Cell Biochem. 2004 Aug;263(1-2):55-72 PMID: 15524167
  103. Oxidative lipidomics of apoptosis: redox catalytic interactions of cytochrome c with cardiolipin and phosphatidylserine.
    Free Radic Biol Med. 2004 Dec 15;37(12):1963-85 PMID: 15544916
  104. Effect of IGF-1 on the balance between autophagy of dysfunctional mitochondria and apoptosis.
    FEBS Lett. 2004 Nov 19;577(3):357-60 PMID: 15556609
  105. Role of Bcl-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes.
    Nat Cell Biol. 2004 Dec;6(12):1221-8 PMID: 15558033
  106. Kinase signaling cascades in the mitochondrion: a matter of life or death.
    Free Radic Biol Med. 2005 Jan 1;38(1):2-11 PMID: 15589366
  107. Inhibition of macroautophagy triggers apoptosis.
    Mol Cell Biol. 2005 Feb;25(3):1025-40 PMID: 15657430
  108. Axonopathy and transport deficits early in the pathogenesis of Alzheimer's disease.
    Science. 2005 Feb 25;307(5713):1282-8 PMID: 15731448
  109. Extensive involvement of autophagy in Alzheimer disease: an immuno-electron microscopy study.
    J Neuropathol Exp Neurol. 2005 Feb;64(2):113-22 PMID: 15751225
  110. Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice.
    J Cell Biol. 2005 May 9;169(3):425-34 PMID: 15866887
  111. Essential roles of Atg5 and FADD in autophagic cell death: dissection of autophagic cell death into vacuole formation and cell death.
    J Biol Chem. 2005 May 27;280(21):20722-9 PMID: 15778222
  112. Autophagy in metazoans: cell survival in the land of plenty.
    Nat Rev Mol Cell Biol. 2005 Jun;6(6):439-48 PMID: 15928708
  113. The co-chaperone carboxyl terminus of Hsp70-interacting protein (CHIP) mediates alpha-synuclein degradation decisions between proteasomal and lysosomal pathways.
    J Biol Chem. 2005 Jun 24;280(25):23727-34 PMID: 15845543
  114. The role of autophagy in cancer development and response to therapy.
    Nat Rev Cancer. 2005 Sep;5(9):726-34 PMID: 16148885
Article Info
Journal
Journal of neuropathology and experimental neurology
Abbr.
J Neuropathol Exp Neurol
ISSN
0022-3069
Published
2006-05-00
Pages
423-32
Language
English
Region
England
NLM ID
2985192R
PMCID
PMC1885377
Subset
IM
Grants
NINDS NIH HHS · R01 NS040817 · United States
NINDS NIH HHS · R21 NS053777 · United States
NINDS NIH HHS · NS040817 · United States
NINDS NIH HHS · NS053777 · United States
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