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PMID: 16163384 Published · ppublish English Comparative Study Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Novel role of p53 in maintaining mitochondrial genetic stability through interaction with DNA Pol gamma.

The EMBO journal ·Vol. 24 ·No. 19 ·2005-10-05 ·Pages 3482-92

Achanta G, Sasaki R, Feng L, Carew JS, Lu W, Pelicano H, Keating MJ, Huang P

Abstract

Mitochondrial DNA (mtDNA) mutations and deletions are frequently observed in cancer, and contribute to altered energy metabolism, increased reactive oxygen species (ROS), and attenuated apoptotic response to anticancer agents. The mechanisms by which cells maintain mitochondrial genomic integrity and the reason why cancer cells exhibit more frequent mtDNA mutations remain unclear. Here, we report that the tumor suppressor molecule p53 has a novel role in maintaining mitochondrial genetic stability through its ability to translocate to mitochondria and interact with mtDNA polymerase gamma (pol gamma) in response to mtDNA damage induced by exogenous and endogenous insults including ROS. The p53 protein physically interacts with mtDNA and pol gamma, and enhances the DNA replication function of pol gamma. Loss of p53 results in a significant increase in mtDNA vulnerability to damage, leading to increased frequency of in vivo mtDNA mutations, which are reversed by stable transfection of wild-type p53. This study provides a mechanistic explanation for the accelerating genetic instability and increased ROS stress in cancer cells associated with loss of p53.

MeSH Terms
Cell Line, Tumor DNA Damage/genetics,physiology DNA Polymerase gamma DNA Primers DNA, Mitochondrial/genetics,metabolism,physiology DNA-Directed DNA Polymerase/metabolism Genomic Instability/physiology Humans Immunoblotting Immunohistochemistry Immunoprecipitation Mutation/genetics Polymerase Chain Reaction Reactive Oxygen Species/metabolism Transfection Tumor Suppressor Protein p53/metabolism
Chemicals
DNA Primers DNA, Mitochondrial Reactive Oxygen Species Tumor Suppressor Protein p53 DNA Polymerase gamma DNA-Directed DNA Polymerase
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Achanta Geetha
Department of Molecular Pathology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA.
Sasaki Ryohei
Feng Li
Carew Jennifer S
Lu Weiqin
Pelicano Helene
Keating Michael J
Huang Peng
References (40)
40 references, click to expand
  1. Role of p53 in sensing oxidative DNA damage in response to reactive oxygen species-generating agents.
    Cancer Res. 2004 Sep 1;64(17):6233-9 PMID: 15342409
  2. Mitochondrial diseases in man and mouse.
    Science. 1999 Mar 5;283(5407):1482-8 PMID: 10066162
  3. Altered ribosomal RNA genes in mitochondria from mammalian cells with chloramphenicol resistance.
    Nature. 1981 Apr 16;290(5807):607-8 PMID: 7219548
  4. Mitochondrial DNA of chloramphenicol-resistant mouse cells contains a single nucleotide change in the region encoding the 3' end of the large ribosomal RNA.
    Proc Natl Acad Sci U S A. 1981 Jun;78(6):3789-93 PMID: 6943583
  5. Death signal-induced localization of p53 protein to mitochondria. A potential role in apoptotic signaling.
    J Biol Chem. 2000 May 26;275(21):16202-12 PMID: 10821866
  6. Superoxide dismutase as a target for the selective killing of cancer cells.
    Nature. 2000 Sep 21;407(6802):390-5 PMID: 11014196
  7. Strategies for manipulating the p53 pathway in the treatment of human cancer.
    Biochem J. 2000 Nov 15;352 Pt 1:1-17 PMID: 11062053
  8. Surfing the p53 network.
    Nature. 2000 Nov 16;408(6810):307-10 PMID: 11099028
  9. Mitochondrial D-loop mutations as clonal markers in multicentric hepatocellular carcinoma and plasma.
    Clin Cancer Res. 2002 Feb;8(2):481-7 PMID: 11839667
  10. Mitochondrial superoxide radical formation is controlled by electron bifurcation to the high and low potential pathways.
    Free Radic Res. 2002 Apr;36(4):381-7 PMID: 12069101
  11. Mitochondrial DNA alterations in cancer.
    Cancer Invest. 2002;20(4):557-69 PMID: 12094550
  12. Progressive external ophthalmoplegia and multiple mitochondrial DNA deletions.
    Acta Neurol Belg. 2002 Mar;102(1):39-42 PMID: 12094562
  13. Maintenance of mitochondrial DNA integrity: repair and degradation.
    Curr Genet. 2002 Aug;41(5):311-22 PMID: 12185497
  14. Cell sorting experiments link persistent mitochondrial DNA damage with loss of mitochondrial membrane potential and apoptotic cell death.
    J Biol Chem. 2003 Jan 17;278(3):1728-34 PMID: 12424245
  15. Electrophile and oxidant damage of mitochondrial DNA leading to rapid evolution of homoplasmic mutations.
    Proc Natl Acad Sci U S A. 2003 Feb 18;100(4):1838-43 PMID: 12578990
  16. p53 has a direct apoptogenic role at the mitochondria.
    Mol Cell. 2003 Mar;11(3):577-90 PMID: 12667443
  17. Mutations in DNA polymerase gamma cause error prone DNA synthesis in human mitochondrial disorders.
    Acta Biochim Pol. 2003;50(1):155-67 PMID: 12673356
  18. Drug discovery and p53.
    Drug Discov Today. 2003 Apr 15;8(8):347-55 PMID: 12681938
  19. Mitochondrial impairment in p53-deficient human cancer cells.
    Mutagenesis. 2003 May;18(3):287-92 PMID: 12714696
  20. Mitochondrial DNA mutations in primary leukemia cells after chemotherapy: clinical significance and therapeutic implications.
    Leukemia. 2003 Aug;17(8):1437-47 PMID: 12886229
  21. Inhibition of mitochondrial respiration: a novel strategy to enhance drug-induced apoptosis in human leukemia cells by a reactive oxygen species-mediated mechanism.
    J Biol Chem. 2003 Sep 26;278(39):37832-9 PMID: 12853461
  22. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis.
    Science. 2004 Feb 13;303(5660):1010-4 PMID: 14963330
  23. Mitochondrial disease: mutations and mechanisms.
    Neurochem Res. 2004 Mar;29(3):589-600 PMID: 15038606
  24. ROS stress in cancer cells and therapeutic implications.
    Drug Resist Updat. 2004 Apr;7(2):97-110 PMID: 15158766
  25. Premature ageing in mice expressing defective mitochondrial DNA polymerase.
    Nature. 2004 May 27;429(6990):417-23 PMID: 15164064
  26. DNA polymerase gamma, the mitochondrial replicase.
    Annu Rev Biochem. 2004;73:293-320 PMID: 15189144
  27. Reconstitution of a minimal mtDNA replisome in vitro.
    EMBO J. 2004 Jun 16;23(12):2423-9 PMID: 15167897
  28. Mitochondrial dysfunction is a common phenotype in aging and cancer.
    Ann N Y Acad Sci. 2004 Jun;1019:260-4 PMID: 15247025
  29. In vivo mitochondrial p53 translocation triggers a rapid first wave of cell death in response to DNA damage that can precede p53 target gene activation.
    Mol Cell Biol. 2004 Aug;24(15):6728-41 PMID: 15254240
  30. Mitochondrial defects in cancer.
    Mol Cancer. 2002 Dec 9;1:9 PMID: 12513701
  31. Mitochondrial p53 levels parallel total p53 levels independent of stress response in human colorectal carcinoma and glioblastoma cells.
    Oncogene. 2004 Aug 19;23(37):6226-36 PMID: 15247902
  32. p53 functions in the incorporation step in DNA base excision repair in mouse liver mitochondria.
    Oncogene. 2004 Aug 26;23(39):6559-68 PMID: 15208669
  33. Isolation of human cell lines lacking mitochondrial DNA.
    Methods Enzymol. 1996;264:304-13 PMID: 8965704
  34. Inhibitors of NADH-ubiquinone reductase: an overview.
    Biochim Biophys Acta. 1998 May 6;1364(2):222-35 PMID: 9593904
  35. Mitochondrial mutagenesis in human cells and tissues.
    Mutat Res. 1999 Jul 30;434(3):177-203 PMID: 10486591
  36. Identification of a putative p53 binding sequence within the human mitochondrial genome.
    FEBS Lett. 2004 Dec 3;578(1-2):198-202 PMID: 15581641
  37. Inhibition of glycolysis in cancer cells: a novel strategy to overcome drug resistance associated with mitochondrial respiratory defect and hypoxia.
    Cancer Res. 2005 Jan 15;65(2):613-21 PMID: 15695406
  38. Mitochondrial reactive oxygen species trigger hypoxia-induced transcription.
    Proc Natl Acad Sci U S A. 1998 Sep 29;95(20):11715-20 PMID: 9751731
  39. Requirement for p53 and p21 to sustain G2 arrest after DNA damage.
    Science. 1998 Nov 20;282(5393):1497-501 PMID: 9822382
  40. Sequence and organization of the human mitochondrial genome.
    Nature. 1981 Apr 9;290(5806):457-65 PMID: 7219534
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
2005-10-05
Epub
2005-00-15
Pages
3482-92
Language
English
Region
England
NLM ID
8208664
PMCID
PMC1276176
Subset
IM
Grants
NCI NIH HHS · R01 CA100428 · United States
NCI NIH HHS · P30 CA016672 · United States
NCI NIH HHS · R01 CA085563 · United States
NCI NIH HHS · CA16672 · United States
NCI NIH HHS · CA109041 · United States
NCI NIH HHS · CA85563 · United States
NCI NIH HHS · R01 CA109041 · United States
NCI NIH HHS · CA100428 · United States
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