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PMID: 20940149 Published · ppublish English Journal Article Research Support, N.I.H., Intramural Research Support, Non-U.S. Gov't

DJ-1 acts in parallel to the PINK1/parkin pathway to control mitochondrial function and autophagy.

Human molecular genetics ·Vol. 20 ·No. 1 ·2011-01-01 ·Pages 40-50

Thomas KJ, McCoy MK, Blackinton J, Beilina A, van der Brug M, Sandebring A, Miller D, Maric D, Cedazo-Minguez A, Cookson MR

Abstract

Mutations in DJ-1, PINK1 (PTEN-induced putative kinase 1) and parkin all cause recessive parkinsonism in humans, but the relationships between these genes are not clearly defined. One event associated with loss of any of these genes is altered mitochondrial function. Recent evidence suggests that turnover of damaged mitochondria by autophagy might be central to the process of recessive parkinsonism. Here, we show that loss of DJ-1 leads to loss of mitochondrial polarization, fragmentation of mitochondria and accumulation of markers of autophagy (LC3 punctae and lipidation) around mitochondria in human dopaminergic cells. These effects are due to endogenous oxidative stress, as antioxidants will reverse all of them. Similar to PINK1 and parkin, DJ-1 also limits mitochondrial fragmentation in response to the mitochondrial toxin rotenone. Furthermore, overexpressed parkin will protect against loss of DJ-1 and, although DJ-1 does not alter PINK1 mitochondrial phenotypes, DJ-1 is still active against rotenone-induced damage in the absence of PINK1. None of the three proteins complex together using size exclusion chromatography. These data suggest that DJ-1 works in parallel to the PINK1/parkin pathway to maintain mitochondrial function in the presence of an oxidative environment.

MeSH Terms
Autophagy Cell Line, Tumor Humans Intracellular Signaling Peptides and Proteins/genetics,metabolism Mitochondria/genetics,physiology Mutation Oncogene Proteins/genetics,metabolism Oxidative Stress/genetics Parkinson Disease/genetics Protein Deglycase DJ-1 Protein Kinases/genetics,metabolism Rotenone/pharmacology Ubiquitin-Protein Ligases/genetics,metabolism
Chemicals
Intracellular Signaling Peptides and Proteins Oncogene Proteins Rotenone Ubiquitin-Protein Ligases parkin protein Protein Kinases PTEN-induced putative kinase PARK7 protein, human Protein Deglycase DJ-1
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Thomas Kelly Jean
Laboratory of Neurogenetics, National Institute on Aging, Flow Cytometry Core Facility, National Institutes of Neurological Diseases and Stroke, National Institutes of Health, Bethesda, MD 20982-3707, USA.
McCoy Melissa K
Blackinton Jeff
Beilina Alexandra
van der Brug Marcel
Sandebring Anna
Miller David
Maric Dragan
Cedazo-Minguez Angel
Cookson Mark R
References (58)
58 references, click to expand
  1. Subversion of cellular autophagosomal machinery by RNA viruses.
    PLoS Biol. 2005 May;3(5):e156 PMID: 15884975
  2. Formation of a stabilized cysteine sulfinic acid is critical for the mitochondrial function of the parkinsonism protein DJ-1.
    J Biol Chem. 2009 Mar 6;284(10):6476-85 PMID: 19124468
  3. Signaling pathways in mitochondrial dysfunction and aging.
    Mech Ageing Dev. 2010 Jul-Aug;131(7-8):536-43 PMID: 20655326
  4. Similar patterns of mitochondrial vulnerability and rescue induced by genetic modification of alpha-synuclein, parkin, and DJ-1 in Caenorhabditis elegans.
    J Biol Chem. 2005 Dec 30;280(52):42655-42668 PMID: 16239214
  5. Mutations in LRRK2/dardarin associated with Parkinson disease are more toxic than equivalent mutations in the homologous kinase LRRK1.
    J Neurochem. 2007 Jul;102(1):93-102 PMID: 17394548
  6. Cytoplasmic Pink1 activity protects neurons from dopaminergic neurotoxin MPTP.
    Proc Natl Acad Sci U S A. 2008 Feb 5;105(5):1716-21 PMID: 18218782
  7. Loss of PINK1 function promotes mitophagy through effects on oxidative stress and mitochondrial fission.
    J Biol Chem. 2009 May 15;284(20):13843-13855 PMID: 19279012
  8. Regulation of autophagy by reactive oxygen species (ROS): implications for cancer progression and treatment.
    Antioxid Redox Signal. 2009 Apr;11(4):777-90 PMID: 18828708
  9. Mitochondrial pathology and muscle and dopaminergic neuron degeneration caused by inactivation of Drosophila Pink1 is rescued by Parkin.
    Proc Natl Acad Sci U S A. 2006 Jul 11;103(28):10793-8 PMID: 16818890
  10. PINK1 stabilized by mitochondrial depolarization recruits Parkin to damaged mitochondria and activates latent Parkin for mitophagy.
    J Cell Biol. 2010 Apr 19;189(2):211-21 PMID: 20404107
  11. Hypersensitivity of DJ-1-deficient mice to 1-methyl-4-phenyl-1,2,3,6-tetrahydropyrindine (MPTP) and oxidative stress.
    Proc Natl Acad Sci U S A. 2005 Apr 5;102(14):5215-20 PMID: 15784737
  12. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy.
    EMBO J. 2008 Jan 23;27(2):433-46 PMID: 18200046
  13. DJ-1 gene deletion reveals that DJ-1 is an atypical peroxiredoxin-like peroxidase.
    Proc Natl Acad Sci U S A. 2007 Sep 11;104(37):14807-12 PMID: 17766438
  14. The role of PTEN-induced kinase 1 in mitochondrial dysfunction and dynamics.
    Int J Biochem Cell Biol. 2009 Oct;41(10):2025-35 PMID: 19703660
  15. Reduced basal autophagy and impaired mitochondrial dynamics due to loss of Parkinson's disease-associated protein DJ-1.
    PLoS One. 2010 Feb 23;5(2):e9367 PMID: 20186336
  16. Mitophagy.
    Biochim Biophys Acta. 2009 Sep;1793(9):1508-15 PMID: 19289147
  17. Loss of parkin or PINK1 function increases Drp1-dependent mitochondrial fragmentation.
    J Biol Chem. 2009 Aug 21;284(34):22938-51 PMID: 19546216
  18. Pink1, Parkin, DJ-1 and mitochondrial dysfunction in Parkinson's disease.
    Curr Opin Neurobiol. 2007 Jun;17(3):331-7 PMID: 17499497
  19. The Parkinson disease-associated leucine-rich repeat kinase 2 (LRRK2) is a dimer that undergoes intramolecular autophosphorylation.
    J Biol Chem. 2008 Jun 13;283(24):16906-14 PMID: 18397888
  20. DJ-1, a cancer and Parkinson's disease associated protein, regulates autophagy through JNK pathway in cancer cells.
    Cancer Lett. 2010 Nov 1;297(1):101-8 PMID: 20510502
  21. Susceptibility to rotenone is increased in neurons from parkin null mice and is reduced by minocycline.
    J Neurochem. 2006 May;97(4):934-46 PMID: 16573651
  22. Loss of PINK1 causes mitochondrial functional defects and increased sensitivity to oxidative stress.
    Proc Natl Acad Sci U S A. 2008 Aug 12;105(32):11364-9 PMID: 18687901
  23. The Parkinson's disease protein DJ-1 is neuroprotective due to cysteine-sulfinic acid-driven mitochondrial localization.
    Proc Natl Acad Sci U S A. 2004 Jun 15;101(24):9103-8 PMID: 15181200
  24. PINK1 is recruited to mitochondria with parkin and associates with LC3 in mitophagy.
    FEBS Lett. 2010 Mar 19;584(6):1073-9 PMID: 20153330
  25. Mitochondrial dysfunction and oxidative damage in parkin-deficient mice.
    J Biol Chem. 2004 Apr 30;279(18):18614-22 PMID: 14985362
  26. Mitochondrial electron-transport-chain inhibitors of complexes I and II induce autophagic cell death mediated by reactive oxygen species.
    J Cell Sci. 2007 Dec 1;120(Pt 23):4155-66 PMID: 18032788
  27. Parkin stabilizes PINK1 through direct interaction.
    Biochem Biophys Res Commun. 2009 Jun 5;383(3):331-5 PMID: 19358826
  28. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes.
    Autophagy. 2008 Feb;4(2):151-75 PMID: 18188003
  29. Reversible phosphorylation of Drp1 by cyclic AMP-dependent protein kinase and calcineurin regulates mitochondrial fission and cell death.
    EMBO Rep. 2007 Oct;8(10):939-44 PMID: 17721437
  30. Drosophila pink1 is required for mitochondrial function and interacts genetically with parkin.
    Nature. 2006 Jun 29;441(7097):1162-6 PMID: 16672981
  31. Silencing DJ-1 reveals its contribution in paraquat-induced autophagy.
    J Neurochem. 2009 May;109(3):889-98 PMID: 19425177
  32. Mitochondrial localization of the Parkinson's disease related protein DJ-1: implications for pathogenesis.
    Hum Mol Genet. 2005 Jul 15;14(14):2063-73 PMID: 15944198
  33. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy.
    J Cell Biol. 2008 Dec 1;183(5):795-803 PMID: 19029340
  34. PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1.
    Nat Cell Biol. 2010 Feb;12(2):119-31 PMID: 20098416
  35. Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by parkin.
    Nature. 2006 Jun 29;441(7097):1157-61 PMID: 16672980
  36. Parkin, PINK1, and DJ-1 form a ubiquitin E3 ligase complex promoting unfolded protein degradation.
    J Clin Invest. 2009 Mar;119(3):650-60 PMID: 19229105
  37. Loss of the Parkinson's disease-linked gene DJ-1 perturbs mitochondrial dynamics.
    Hum Mol Genet. 2010 Oct 1;19(19):3734-46 PMID: 20639397
  38. Parkin occurs in a stable, non-covalent, approximately 110-kDa complex in brain.
    Eur J Neurosci. 2008 Jan;27(2):284-93 PMID: 18190519
  39. Loss-of-function of human PINK1 results in mitochondrial pathology and can be rescued by parkin.
    J Neurosci. 2007 Nov 7;27(45):12413-8 PMID: 17989306
  40. Cyclic AMP-dependent protein kinase phosphorylation of Drp1 regulates its GTPase activity and mitochondrial morphology.
    J Biol Chem. 2007 Jul 27;282(30):21583-7 PMID: 17553808
  41. L166P mutant DJ-1, causative for recessive Parkinson's disease, is degraded through the ubiquitin-proteasome system.
    J Biol Chem. 2003 Sep 19;278(38):36588-95 PMID: 12851414
  42. DJ-1 has a role in antioxidative stress to prevent cell death.
    EMBO Rep. 2004 Feb;5(2):213-8 PMID: 14749723
  43. The kinase domain of mitochondrial PINK1 faces the cytoplasm.
    Proc Natl Acad Sci U S A. 2008 Aug 19;105(33):12022-7 PMID: 18687899
  44. DJ-1/PARK7 is an important mediator of hypoxia-induced cellular responses.
    Proc Natl Acad Sci U S A. 2009 Jan 27;106(4):1111-6 PMID: 19144925
  45. PINK1 is selectively stabilized on impaired mitochondria to activate Parkin.
    PLoS Biol. 2010 Jan 26;8(1):e1000298 PMID: 20126261
  46. Under the ROS…thiol network is the principal suspect for autophagy commitment.
    Autophagy. 2010 Oct;6(7):999-1005 PMID: 20639698
  47. Mitochondrial alterations in PINK1 deficient cells are influenced by calcineurin-dependent dephosphorylation of dynamin-related protein 1.
    PLoS One. 2009 May 27;4(5):e5701 PMID: 19492085
  48. DJ-1 up-regulates glutathione synthesis during oxidative stress and inhibits A53T alpha-synuclein toxicity.
    J Biol Chem. 2005 Dec 30;280(52):43150-8 PMID: 16227205
  49. Mutations in PTEN-induced putative kinase 1 associated with recessive parkinsonism have differential effects on protein stability.
    Proc Natl Acad Sci U S A. 2005 Apr 19;102(16):5703-8 PMID: 15824318
  50. DJ-1 and Parkin modulate dopamine-dependent behavior and inhibit MPTP-induced nigral dopamine neuron loss in mice.
    Mol Ther. 2007 Apr;15(4):698-704 PMID: 17299411
  51. RNA binding activity of the recessive parkinsonism protein DJ-1 supports involvement in multiple cellular pathways.
    Proc Natl Acad Sci U S A. 2008 Jul 22;105(29):10244-9 PMID: 18626009
  52. Mutational analysis of DJ-1 in Drosophila implicates functional inactivation by oxidative damage and aging.
    Proc Natl Acad Sci U S A. 2006 Aug 15;103(33):12517-22 PMID: 16894167
  53. PINK1-dependent recruitment of Parkin to mitochondria in mitophagy.
    Proc Natl Acad Sci U S A. 2010 Jan 5;107(1):378-83 PMID: 19966284
  54. Drosophila parkin requires PINK1 for mitochondrial translocation and ubiquitinates mitofusin.
    Proc Natl Acad Sci U S A. 2010 Mar 16;107(11):5018-23 PMID: 20194754
  55. Reduced anti-oxidative stress activities of DJ-1 mutants found in Parkinson's disease patients.
    Biochem Biophys Res Commun. 2004 Jul 23;320(2):389-97 PMID: 15219840
  56. RING finger 1 mutations in Parkin produce altered localization of the protein.
    Hum Mol Genet. 2003 Nov 15;12(22):2957-65 PMID: 14519684
  57. Biomedicine. Parkinson's--divergent causes, convergent mechanisms.
    Science. 2004 May 21;304(5674):1120-2 PMID: 15155938
  58. Molecular pathogenesis of Parkinson disease: insights from genetic studies.
    Expert Rev Mol Med. 2009 Jul 27;11:e22 PMID: 19631006
Article Info
Journal
Human molecular genetics
Abbr.
Hum Mol Genet
ISSN
1460-2083
Published
2011-01-01
Epub
2010-00-11
Pages
40-50
Language
English
Region
England
NLM ID
9208958
PMCID
PMC3000675
Subset
IM
Grants
Intramural NIH HHS · United States
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