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PMID: 10632588 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Proteasome involvement and accumulation of ubiquitinated proteins in cerebellar granule neurons undergoing apoptosis.

Canu N, Barbato C, Ciotti MT, Serafino A, Dus L, Calissano P

Abstract

We investigated the potential role of the ubiquitin proteolytic system in the death of cerebellar granule neurons induced by reduction of extracellular potassium. Inhibitors of proteasomal function block apoptosis if administered at onset of this process, but they do not exert such effect when added 2-3 hr later. The same inhibitors also prevent caspase-3 activity and calpain-caspase-3-mediated processing of tau protein, suggesting that proteasomes are involved upstream of the caspase activation. Although the proteasomes seem to play an early primary role in programmed cell death, we found that with progression of apoptosis, during the execution phase, a perturbation in normal ubiquitin-proteasome function occurs, and high levels of ubiquitinated proteins accumulate in the cytoplasm of dying cells. Such accumulation correlates with a progressive decline of proteasome chymotrypsin and trypsin-like activities and, to a lower extent, of postacidic-like activity. Both intracytoplasmic accumulation of ubiquitinated proteins and decline of proteasome function are reversed by the pan-caspase inhibitor Z-VAD-fmk. The decline in proteasome function is accompanied by, and likely attributable to, a marked and progressive decline of deubiquitinating activities. The finding that the proteasomes are early involved in apoptosis and that ubiquitinated proteins accumulate during this process prospect granule neurons as a model system aimed at correlating these events with neurodegenerative diseases.

MeSH Terms
Acetylcysteine/analogs & derivatives,pharmacology Animals Apoptosis/drug effects,physiology Cell Division Cell Survival/drug effects Cells, Cultured Cerebellum/cytology,physiology Culture Media, Serum-Free Cysteine Endopeptidases/metabolism Cysteine Proteinase Inhibitors/pharmacology Leucine/analogs & derivatives,pharmacology Leupeptins/pharmacology Multienzyme Complexes/metabolism Neurons/cytology,drug effects,physiology Oligopeptides/pharmacology Proteasome Endopeptidase Complex Protein Processing, Post-Translational Rats Rats, Wistar Ubiquitins/metabolism
Chemicals
Culture Media, Serum-Free Cysteine Proteinase Inhibitors Leupeptins Multienzyme Complexes Oligopeptides Ubiquitins lactacystin Cysteine Endopeptidases Proteasome Endopeptidase Complex Leucine leupeptin aloxistatin Acetylcysteine
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Canu N
Dipartimento di Neuroscienze, Facoltà di Medicina e Chirurgia, Università di Tor Vergata, 00133 Roma, Italia. nadia@biocell.irmkant.rm.cnr.it
Barbato C
Ciotti M T
Serafino A
Dus L
Calissano P
References (64)
64 references, click to expand
  1. MHC-linked LMP gene products specifically alter peptidase activities of the proteasome.
    Nature. 1993 Sep 16;365(6443):262-4 PMID: 8371781
  2. The ubiquitin pathway in Parkinson's disease.
    Nature. 1998 Oct 1;395(6701):451-2 PMID: 9774100
  3. The sizes of peptides generated from protein by mammalian 26 and 20 S proteasomes. Implications for understanding the degradative mechanism and antigen presentation.
    J Biol Chem. 1999 Feb 5;274(6):3363-71 PMID: 9920878
  4. Tau cleavage and dephosphorylation in cerebellar granule neurons undergoing apoptosis.
    J Neurosci. 1998 Sep 15;18(18):7061-74 PMID: 9736630
  5. Potassium deprivation-induced apoptosis of cerebellar granule neurons: a sequential requirement for new mRNA and protein synthesis, ICE-like protease activity, and reactive oxygen species.
    J Neurosci. 1996 Aug 1;16(15):4696-706 PMID: 8764657
  6. Proteinase yscE, the yeast proteasome/multicatalytic-multifunctional proteinase: mutants unravel its function in stress induced proteolysis and uncover its necessity for cell survival.
    EMBO J. 1991 Mar;10(3):555-62 PMID: 2001673
  7. The ubiquitin-proteasome proteolytic pathway.
    Cell. 1994 Oct 7;79(1):13-21 PMID: 7923371
  8. Non-erythroid alpha-spectrin breakdown by calpain and interleukin 1 beta-converting-enzyme-like protease(s) in apoptotic cells: contributory roles of both protease families in neuronal apoptosis.
    Biochem J. 1996 Nov 1;319 ( Pt 3):683-90 PMID: 8920967
  9. Immunohistochemical evidence for apoptosis in Alzheimer's disease.
    Neuroreport. 1994 Dec 20;5(18):2529-33 PMID: 7696596
  10. Intragenic deletion in the gene encoding ubiquitin carboxy-terminal hydrolase in gad mice.
    Nat Genet. 1999 Sep;23(1):47-51 PMID: 10471497
  11. Removal of proteasomes from the nucleus and their accumulation in apoptotic blebs during programmed cell death.
    FEBS Lett. 1996 Sep 23;394(1):47-50 PMID: 8925925
  12. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  13. Biochemical and temporal analysis of events associated with apoptosis induced by lowering the extracellular potassium concentration in mouse cerebellar granule neurons.
    J Neurochem. 1997 Feb;68(2):750-9 PMID: 9003066
  14. Substrate specificity of deubiquitinating enzymes: ubiquitin C-terminal hydrolases.
    Biochemistry. 1998 Mar 10;37(10):3358-68 PMID: 9521656
  15. The multicatalytic proteinase complex, a major extralysosomal proteolytic system.
    Biochemistry. 1990 Nov 13;29(45):10289-97 PMID: 2175651
  16. Disruption of the intracellular sulfhydryl homeostasis by cadmium-induced oxidative stress leads to protein thiolation and ubiquitination in neuronal cells.
    J Biol Chem. 1998 May 22;273(21):12703-9 PMID: 9582293
  17. Involvement of the proteasome in the programmed cell death of NGF-deprived sympathetic neurons.
    EMBO J. 1996 Aug 1;15(15):3845-52 PMID: 8670889
  18. Induction of apoptosis in cerebellar granule neurons by low potassium: inhibition of death by insulin-like growth factor I and cAMP.
    Proc Natl Acad Sci U S A. 1993 Dec 1;90(23):10989-93 PMID: 8248201
  19. Caspases: the executioners of apoptosis.
    Biochem J. 1997 Aug 15;326 ( Pt 1):1-16 PMID: 9337844
  20. Activation of caspase-3 and apoptosis in cerebellar granule cells.
    J Neurosci Res. 1998 May 1;52(3):334-41 PMID: 9590441
  21. A new inhibitor of the chymotrypsin-like activity of the multicatalytic proteinase complex (20S proteasome) induces accumulation of ubiquitin-protein conjugates in a neuronal cell.
    J Neurochem. 1994 Oct;63(4):1578-81 PMID: 7931314
  22. Ubiquitin is conjugated with amino-terminally processed tau in paired helical filaments.
    Neuron. 1993 Jun;10(6):1151-60 PMID: 8391280
  23. Proteasome inhibitors: valuable new tools for cell biologists.
    Trends Cell Biol. 1998 Oct;8(10):397-403 PMID: 9789328
  24. Autoradiographic localization and depolarization-induced release of acidic amino acids in differentiating cerebellar granule cell cultures.
    Brain Res. 1984 Jan 2;290(1):77-86 PMID: 6140986
  25. Purification of two high molecular weight proteases from rabbit reticulocyte lysate.
    J Biol Chem. 1987 Jun 15;262(17):8303-13 PMID: 3298229
  26. Abnormal accumulation of NACP/alpha-synuclein in neurodegenerative disorders.
    Am J Pathol. 1998 Feb;152(2):367-72 PMID: 9466562
  27. Metabolism of the polyubiquitin degradation signal: structure, mechanism, and role of isopeptidase T.
    Biochemistry. 1995 Nov 7;34(44):14535-46 PMID: 7578059
  28. A ubiquitin C-terminal isopeptidase that acts on polyubiquitin chains. Role in protein degradation.
    J Biol Chem. 1992 Jan 15;267(2):719-27 PMID: 1309773
  29. The ubiquitin-conjugation system.
    Annu Rev Genet. 1992;26:179-207 PMID: 1336336
  30. Evidence for apoptotic cell death in Alzheimer's disease.
    Exp Neurol. 1995 Jun;133(2):225-30 PMID: 7544290
  31. Kinetic and mechanistic studies on the hydrolysis of ubiquitin C-terminal 7-amido-4-methylcoumarin by deubiquitinating enzymes.
    Biochemistry. 1998 Feb 17;37(7):1868-79 PMID: 9485312
  32. The role of CED-3-related cysteine proteases in apoptosis of cerebellar granule cells.
    J Neurosci. 1997 Aug 15;17(16):6105-13 PMID: 9236222
  33. Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules.
    Cell. 1994 Sep 9;78(5):761-71 PMID: 8087844
  34. Proteasomes: protein degradation machines of the cell.
    Trends Biochem Sci. 1994 Sep;19(9):377-82 PMID: 7985232
  35. Kinetic studies of isopeptidase T: modulation of peptidase activity by ubiquitin.
    Biochemistry. 1995 Oct 3;34(39):12616-23 PMID: 7548011
  36. Apoptosis in cerebellar granule cells is blocked by high KCl, forskolin, and IGF-1 through distinct mechanisms of action: the involvement of intracellular calcium and RNA synthesis.
    J Neurosci. 1995 Feb;15(2):1172-9 PMID: 7532699
  37. Mechanisms and genes of cellular suicide.
    Science. 1995 Mar 10;267(5203):1445-9 PMID: 7878463
  38. Ubiquitin in neurodegenerative diseases.
    Brain Pathol. 1993 Jan;3(1):55-65 PMID: 8269084
  39. Ubiquitin, proteasomes, and the regulation of intracellular protein degradation.
    Curr Opin Cell Biol. 1995 Apr;7(2):215-23 PMID: 7612274
  40. Identification of an interleukin-1 beta converting enzyme-like activity that increases upon treatment of P19 cells with retinoic acid as the proteasome.
    J Biochem. 1996 Oct;120(4):699-704 PMID: 8947829
  41. Early release and subsequent caspase-mediated degradation of cytochrome c in apoptotic cerebellar granule cells.
    FEBS Lett. 1999 Aug 20;457(1):126-30 PMID: 10486578
  42. 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
  43. Inhibition of etoposide-induced apoptosis with peptide aldehyde inhibitors of proteasome.
    Biochem J. 1998 Jun 15;332 ( Pt 3):661-5 PMID: 9620867
  44. Apoptosis in the pathogenesis and treatment of disease.
    Science. 1995 Mar 10;267(5203):1456-62 PMID: 7878464
  45. In vivo disassembly of free polyubiquitin chains by yeast Ubp14 modulates rates of protein degradation by the proteasome.
    EMBO J. 1997 Aug 15;16(16):4826-38 PMID: 9305625
  46. Multicatalytic endopeptidase complex: proteasome.
    Methods Enzymol. 1994;244:331-50 PMID: 7845218
  47. Increased amyloidogenic secretion in cerebellar granule cells undergoing apoptosis.
    Proc Natl Acad Sci U S A. 1998 Feb 3;95(3):1247-52 PMID: 9448317
  48. The ubiquitin-proteasome pathway is required for processing the NF-kappa B1 precursor protein and the activation of NF-kappa B.
    Cell. 1994 Sep 9;78(5):773-85 PMID: 8087845
  49. Proteasome activation occurs at an early, premitochondrial step of thymocyte apoptosis.
    J Immunol. 1998 Jul 1;161(1):35-40 PMID: 9647204
  50. Ubiquitin is detected in neurofibrillary tangles and senile plaque neurites of Alzheimer disease brains.
    Proc Natl Acad Sci U S A. 1987 May;84(9):3033-6 PMID: 3033674
  51. An automated colorimetric microassay for neuronotrophic factors.
    Brain Res. 1986 Mar;390(2):191-8 PMID: 3955369
  52. The role of estrogens on the proliferation of human breast tumor cells (MCF-7).
    J Steroid Biochem. 1985 Jul;23(1):87-94 PMID: 4021494
  53. Inhibition of proteasome activities and subunit-specific amino-terminal threonine modification by lactacystin.
    Science. 1995 May 5;268(5211):726-31 PMID: 7732382
  54. Changes in proteasome activity following transient ischemia.
    Neurochem Int. 1996 Feb;28(2):209-12 PMID: 8719710
  55. Metabolic and genetic analyses of apoptosis in potassium/serum-deprived rat cerebellar granule cells.
    J Neurosci. 1996 Dec 1;16(23):7487-95 PMID: 8922404
  56. The yeast DOA4 gene encodes a deubiquitinating enzyme related to a product of the human tre-2 oncogene.
    Nature. 1993 Nov 25;366(6453):313-9 PMID: 8247125
  57. Proteasomes play an essential role in thymocyte apoptosis.
    EMBO J. 1996 Aug 1;15(15):3835-44 PMID: 8670888
  58. Activation of the cell death program by inhibition of proteasome function.
    Proc Natl Acad Sci U S A. 1997 Feb 4;94(3):855-60 PMID: 9023346
  59. Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain.
    Science. 1997 Sep 26;277(5334):1990-3 PMID: 9302293
  60. Development of a method for measuring cell number: application to CNS primary neuronal cultures.
    Cytometry. 1994 Nov 1;17(3):274-6 PMID: 7851163
  61. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa.
    Anal Biochem. 1987 Nov 1;166(2):368-79 PMID: 2449095
  62. Proteasome activities decrease during dexamethasone-induced apoptosis of thymocytes.
    Biochem J. 1998 Jun 1;332 ( Pt 2):315-20 PMID: 9601058
  63. Regulation of ubiquitin-dependent processes by deubiquitinating enzymes.
    FASEB J. 1997 Dec;11(14):1245-56 PMID: 9409543
  64. Sequential activation of ICE-like and CPP32-like proteases during Fas-mediated apoptosis.
    Nature. 1996 Apr 25;380(6576):723-6 PMID: 8614469
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2000-01-15
Pages
589-99
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6772397
Subset
IM
Grants
Telethon · E.0855 · Italy
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