Home LiteratureArticle Details
PMID: 18815198 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Mitochondrial ferritin limits oxidative damage regulating mitochondrial iron availability: hypothesis for a protective role in Friedreich ataxia.

Human molecular genetics ·Vol. 18 ·No. 1 ·2009-01-01 ·Pages 1-11

Campanella A, Rovelli E, Santambrogio P, Cozzi A, Taroni F, Levi S

Abstract

Mitochondrial ferritin (FtMt) is a nuclear-encoded iron-sequestering protein that specifically localizes in mitochondria. In mice it is highly expressed in cells characterized by high-energy consumption, while is undetectable in iron storage tissues like liver and spleen. FtMt expression in mammalian cells was shown to cause a shift of iron from cytosol to mitochondria, and in yeast it rescued the defects associated with frataxin deficiency. To study the role of FtMt in oxidative damage, we analyzed the effect of its expression in HeLa cells after incubation with H(2)O(2) and Antimycin A, and after a long-term growth in glucose-free media that enhances mitochondrial respiratory activity. FtMt reduced the level of reactive oxygen species (ROS), increased the level of adenosine 5'triphosphate and the activity of mitochondrial Fe-S enzymes, and had a positive effect on cell viability. Furthermore, FtMt expression reduces the size of cytosolic and mitochondrial labile iron pools. In cells grown in glucose-free media, FtMt level was reduced owing to faster degradation rate, however it still protected the activity of mitochondrial Fe-S enzymes without affecting the cytosolic iron status. In addition, FtMt expression in fibroblasts from Friedreich ataxia (FRDA) patients prevented the formation of ROS and partially rescued the impaired activity of mitochondrial Fe-S enzymes, caused by frataxin deficiency. These results indicate that the primary function of FtMt involves the control of ROS formation through the regulation of mitochondrial iron availability. They are consistent with the expression pattern of FtMt observed in mouse tissues, suggesting a FtMt protective role in cells characterized by defective iron homeostasis and respiration, such as in FRDA.

MeSH Terms
Animals Cells, Cultured Ferritins/genetics,metabolism Fibroblasts/metabolism Friedreich Ataxia/genetics,metabolism Gene Expression Gene Expression Regulation HeLa Cells Humans Iron/metabolism Mice Mitochondria/genetics,metabolism Mitochondrial Proteins/genetics,metabolism Oxidation-Reduction Oxidative Stress Reactive Oxygen Species/metabolism
Chemicals
Mitochondrial Proteins Reactive Oxygen Species Ferritins Iron
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Campanella Alessandro
1IIT Network, Research Unit of Molecular Neuroscience, Vita-Salute San Raffaele University, Milano 20132, Italy.
Rovelli Elisabetta
Santambrogio Paolo
Cozzi Anna
Taroni Franco
Levi Sonia
References (53)
53 references, click to expand
  1. Antioxidant defence mechanisms: from the beginning to the end (of the beginning).
    Free Radic Res. 1999 Oct;31(4):261-72 PMID: 10517532
  2. Overexpression of mitochondrial ferritin causes cytosolic iron depletion and changes cellular iron homeostasis.
    Blood. 2005 Mar 1;105(5):2161-7 PMID: 15522954
  3. Iron trafficking in the mitochondrion: novel pathways revealed by disease.
    Blood. 2005 Mar 1;105(5):1867-74 PMID: 15528311
  4. Unique iron binding and oxidation properties of human mitochondrial ferritin: a comparative analysis with Human H-chain ferritin.
    J Mol Biol. 2005 Apr 1;347(3):543-54 PMID: 15755449
  5. Intracellular labile iron pools as direct targets of iron chelators: a fluorescence study of chelator action in living cells.
    Blood. 2005 Nov 1;106(9):3242-50 PMID: 16020512
  6. Frataxin deficiency alters heme pathway transcripts and decreases mitochondrial heme metabolites in mammalian cells.
    Hum Mol Genet. 2005 Dec 15;14(24):3787-99 PMID: 16239244
  7. Targeted disruption of hepatic frataxin expression causes impaired mitochondrial function, decreased life span and tumor growth in mice.
    Hum Mol Genet. 2005 Dec 15;14(24):3857-64 PMID: 16278235
  8. Iron(II) and hydrogen peroxide detoxification by human H-chain ferritin. An EPR spin-trapping study.
    Biochemistry. 2006 Mar 14;45(10):3429-36 PMID: 16519538
  9. Flow cytometry evaluation of erythroid dysplasia in patients with myelodysplastic syndrome.
    Leukemia. 2006 Apr;20(4):549-55 PMID: 16498394
  10. Characterization of mitochondrial ferritin in Drosophila.
    Proc Natl Acad Sci U S A. 2006 Apr 11;103(15):5893-8 PMID: 16571656
  11. The effects of mitochondrial iron homeostasis on cofactor specificity of superoxide dismutase 2.
    EMBO J. 2006 Apr 19;25(8):1775-83 PMID: 16601688
  12. Frataxin, iron-sulfur clusters, heme, ROS, and aging.
    Antioxid Redox Signal. 2006 Mar-Apr;8(3-4):506-16 PMID: 16677095
  13. Activation of superoxide dismutases: putting the metal to the pedal.
    Biochim Biophys Acta. 2006 Jul;1763(7):747-58 PMID: 16828895
  14. In vivo tumor growth is inhibited by cytosolic iron deprivation caused by the expression of mitochondrial ferritin.
    Blood. 2006 Oct 1;108(7):2428-34 PMID: 16757684
  15. Iron and Friedreich ataxia.
    J Neural Transm Suppl. 2006;(70):143-6 PMID: 17017521
  16. GAA repeat expansion mutation mouse models of Friedreich ataxia exhibit oxidative stress leading to progressive neuronal and cardiac pathology.
    Genomics. 2006 Nov;88(5):580-90 PMID: 16919418
  17. Iron and iron-responsive proteins in the cardiomyopathy of Friedreich's ataxia.
    Cerebellum. 2006;5(4):257-67 PMID: 17134988
  18. Conditional mouse models for Friedreich ataxia, a neurodegenerative disorder associating cardiomyopathy.
    Handb Exp Pharmacol. 2007;(178):365-75 PMID: 17203663
  19. Oxidative stress and protease dysfunction in the yeast model of Friedreich ataxia.
    Free Radic Biol Med. 2007 May 15;42(10):1561-70 PMID: 17448903
  20. The chemical form of mitochondrial iron in Friedreich's ataxia.
    J Inorg Biochem. 2007 Jun;101(6):957-66 PMID: 17475338
  21. The dentate nucleus in Friedreich's ataxia: the role of iron-responsive proteins.
    Acta Neuropathol. 2007 Aug;114(2):163-73 PMID: 17443334
  22. Mitochondrial ferritin expression in adult mouse tissues.
    J Histochem Cytochem. 2007 Nov;55(11):1129-37 PMID: 17625226
  23. Assessment of chelatable mitochondrial iron by using mitochondrion-selective fluorescent iron indicators with different iron-binding affinities.
    Chembiochem. 2007 Feb 12;8(3):341-52 PMID: 17219451
  24. The effects of frataxin silencing in HeLa cells are rescued by the expression of human mitochondrial ferritin.
    Biochim Biophys Acta. 2008 Feb;1782(2):90-8 PMID: 18160053
  25. Escherichia coli FtnA acts as an iron buffer for re-assembly of iron-sulfur clusters in response to hydrogen peroxide stress.
    Biometals. 2008 Dec;21(6):693-703 PMID: 18618270
  26. Overexpression of wild type and mutated human ferritin H-chain in HeLa cells: in vivo role of ferritin ferroxidase activity.
    J Biol Chem. 2000 Aug 18;275(33):25122-9 PMID: 10833524
  27. A human mitochondrial ferritin encoded by an intronless gene.
    J Biol Chem. 2001 Jul 6;276(27):24437-40 PMID: 11323407
  28. Assembly and iron-binding properties of human frataxin, the protein deficient in Friedreich ataxia.
    Hum Mol Genet. 2002 Feb 1;11(3):217-27 PMID: 11823441
  29. Sideroblastic anaemias.
    Br J Haematol. 2002 Mar;116(4):733-43 PMID: 11886376
  30. The chelatable iron pool in living cells: a methodically defined quantity.
    Biol Chem. 2002 Mar-Apr;383(3-4):489-502 PMID: 12033438
  31. Human mitochondrial ferritin expressed in HeLa cells incorporates iron and affects cellular iron metabolism.
    J Biol Chem. 2002 Jun 21;277(25):22430-7 PMID: 11953424
  32. Ferritin, iron homeostasis, and oxidative damage.
    Free Radic Biol Med. 2002 Aug 15;33(4):457-63 PMID: 12160928
  33. The yeast frataxin homolog Yfh1p plays a specific role in the maturation of cellular Fe/S proteins.
    Hum Mol Genet. 2002 Aug 15;11(17):2025-36 PMID: 12165564
  34. Mitochondrial ferritin: a new player in iron metabolism.
    Blood Cells Mol Dis. 2002 Nov-Dec;29(3):376-83 PMID: 12547228
  35. Mitochondrial ferritin expression in erythroid cells from patients with sideroblastic anemia.
    Blood. 2003 Mar 1;101(5):1996-2000 PMID: 12406866
  36. Multiple pathways for mineral core formation in mammalian apoferritin. The role of hydrogen peroxide.
    Biochemistry. 2003 Mar 18;42(10):3142-50 PMID: 12627982
  37. Frataxin deficiency in pancreatic islets causes diabetes due to loss of beta cell mass.
    J Clin Invest. 2003 Aug;112(4):527-34 PMID: 12925693
  38. Energy substrate modulates mitochondrial structure and oxidative capacity in cancer cells.
    Cancer Res. 2004 Feb 1;64(3):985-93 PMID: 14871829
  39. Analysis of the biologic functions of H- and L-ferritins in HeLa cells by transfection with siRNAs and cDNAs: evidence for a proliferative role of L-ferritin.
    Blood. 2004 Mar 15;103(6):2377-83 PMID: 14615379
  40. Crystal structure and biochemical properties of the human mitochondrial ferritin and its mutant Ser144Ala.
    J Mol Biol. 2004 Jul 2;340(2):277-93 PMID: 15201052
  41. Mitochondrial ferritin.
    Int J Biochem Cell Biol. 2004 Oct;36(10):1887-9 PMID: 15203103
  42. Frataxin acts as an iron chaperone protein to modulate mitochondrial aconitase activity.
    Science. 2004 Jul 9;305(5681):242-5 PMID: 15247478
  43. Evidence for the presence of ferritin in plant mitochondria.
    Eur J Biochem. 2004 Sep;271(18):3657-64 PMID: 15355342
  44. The expression of human mitochondrial ferritin rescues respiratory function in frataxin-deficient yeast.
    Hum Mol Genet. 2004 Oct 1;13(19):2279-88 PMID: 15282205
  45. Oxidoreductases involved in cell carbon synthesis of Methanobacterium thermoautotrophicum.
    J Bacteriol. 1977 Nov;132(2):604-13 PMID: 914779
  46. Evaluation of 2',7'-dichlorofluorescin and dihydrorhodamine 123 as fluorescent probes for intracellular H2O2 in cultured endothelial cells.
    Arch Biochem Biophys. 1993 May;302(2):348-55 PMID: 8387741
  47. Assay of succinate dehydrogenase activity by a colorimetric-continuous method using iodonitrotetrazolium chloride as electron acceptor.
    Anal Biochem. 1993 Aug 1;212(2):506-9 PMID: 8214593
  48. Respiration and growth defects in transmitochondrial cell lines carrying the 11778 mutation associated with Leber's hereditary optic neuropathy.
    J Biol Chem. 1996 May 31;271(22):13155-61 PMID: 8662757
  49. The ferritins: molecular properties, iron storage function and cellular regulation.
    Biochim Biophys Acta. 1996 Jul 31;1275(3):161-203 PMID: 8695634
  50. Aconitases: a class of metalloproteins highly sensitive to nitric oxide synthesis.
    Methods Enzymol. 1996;269:26-36 PMID: 8791634
  51. Regulation of mitochondrial iron accumulation by Yfh1p, a putative homolog of frataxin.
    Science. 1997 Jun 13;276(5319):1709-12 PMID: 9180083
  52. Aconitase and mitochondrial iron-sulphur protein deficiency in Friedreich ataxia.
    Nat Genet. 1997 Oct;17(2):215-7 PMID: 9326946
  53. The Friedreich's ataxia mutation confers cellular sensitivity to oxidant stress which is rescued by chelators of iron and calcium and inhibitors of apoptosis.
    Hum Mol Genet. 1999 Mar;8(3):425-30 PMID: 9949201
Article Info
Journal
Human molecular genetics
Abbr.
Hum Mol Genet
ISSN
1460-2083
Published
2009-01-01
Epub
2008-00-24
Pages
1-11
Language
English
Region
England
NLM ID
9208958
PMCID
PMC3298861
Subset
IM
Grants
Telethon · GGP05141 · Italy
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com