Mice lacking mitochondrial ferritin are more sensitive to doxorubicin-mediated cardiotoxicity

Journal of Molecular Medicine

Volumn 92, Issue 8, 2014, Pages 859-869

  Maccarinelli, Federica ^a   Gammella, Elena ^b   Asperti, Michela ^a   Regoni, Maria ^a   Biasiotto, Giorgio ^a   Turco, Emilia ^c   Altruda, Fiorella ^c   Lonardi, Silvia ^a   Cornaghi, Laura ^b   Donetti, Elena ^b   Recalcati, Stefania ^b   Poli, Maura ^a   Finazzi, Dario ^a   Arosio, Paolo ^a   Cairo, Gaetano ^b  

^a UNIVERSITY OF BRESCIA   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITY OF TURIN   (Italy)

Author keywords

Doxorubicin; Ferritin; Mitochondria; Oxidative damage

Indexed keywords

ADENOSINE TRIPHOSPHATE; BRAIN NATRIURETIC PEPTIDE; CASPASE 3; DOXORUBICIN; FERRIC FERROCYANIDE; FERRITIN; HEART MUSCLE EXTRACT; HEME OXYGENASE 1; LC3 PROTEIN; MITOCHONDRIAL FERRITIN; PROTEIN; SODIUM CHLORIDE; TOLONIUM CHLORIDE; UNCLASSIFIED DRUG; ANTINEOPLASTIC ANTIBIOTIC; MITOCHONDRIAL PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGY; CARDIOTOXICITY; CELL DAMAGE; CHROMATIN CONDENSATION; CONTROLLED STUDY; DISEASE SEVERITY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ELECTRON MICROSCOPY; ENZYME ACTIVITY; FEMALE; GENE TARGETING; GENOTYPE; HEART MITOCHONDRION; HEART MUSCLE; HEART PROTECTION; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; LIPID PEROXIDATION; MALE; MORTALITY; MOUSE; MUSCLE FIBRIL; NATIVE POLYACRYLAMIDE GEL ELECTROPHORESIS; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPERMATOCYTE; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING; ANIMAL; DEFICIENCY; DISEASE PREDISPOSITION; DRUG EFFECTS; GENE VECTOR; GENETICS; HEART; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; ULTRASTRUCTURE;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; CARDIOTOXICITY; DISEASE SUSCEPTIBILITY; DOXORUBICIN; FEMALE; FERRITINS; GENE TARGETING; GENETIC VECTORS; HEART; MICE; MICE, KNOCKOUT; MITOCHONDRIAL PROTEINS; MYOCARDIUM; OXIDATIVE STRESS; PHENOTYPE;

EID: 84906791754     PISSN: 09462716     EISSN: 14321440     Source Type: Journal    
DOI: 10.1007/s00109-014-1147-0     Document Type: Article

References (53)

1. Drysdale J, Arosio P, Invernizzi R, Cazzola M, Volz A, Corsi B, Biasiotto G, Levi S (2002) Mitochondrial ferritin: a new player in iron metabolism. Blood Cells Mol Dis 29:376-383
2. Levi S, Corsi B, Bosisio M, Invernizzi R, Volz A, Sanford D, Arosio P, Drysdale J (2001) A human mitochondrial ferritin encoded by an intronless gene. J Biol Chem 276:24437-24440
3. D'estaintot B, Paolo S, Granier T, Gallois B, Chevalier J, PRECIGOUX G, Levi S, Arosio P (2004) Crystal structure and biochemical properties of the human mitochondrial ferritin and its mutant Ser144Ala. J Mol Biol 340:277-293
4. Levi S, Arosio P (2004) Mitochondrial ferritin. Int J Biochem Cell Biol 36:1887-1889 (Pubitemid 38760019)
5. Snyder AM, Wang X, Patton SM, Arosio P, Levi S, Earley CJ, Allen RP, Connor JR (2009) Mitochondrial ferritin in the substantia nigra in restless legs syndrome. J Neuropathol Exp Neurol 68:1193-1199
6. Cazzola M, Invernizzi R, Bergamaschi G, Levi S, Corsi B, Travaglino E, Rolandi V, Biasiotto G, Drysdale J, Arosio P (2003) Mitochondrial ferritin expression in erythroid cells frompatients with sideroblastic anemia. Blood 101:1996-2000 (Pubitemid 36237606)
7. Corsi B, Cozzi A, Arosio P, Drysdale J, Santambrogio P, Campanella A, Biasiotto G, Albertini A, Levi S (2002) Human mitochondrial ferritin expressed in HeLa cells incorporates iron and affects cellular iron metabolism. J Biol Chem 277:22430-22437 (Pubitemid 34967214)
8. Campanella A, Rovelli E, Santambrogio P, Cozzi A, Taroni F, Levi S (2009) Mitochondrial ferritin limits oxidative damage regulating mitochondrial iron availability: hypothesis for a protective role in Friedreich ataxia. Hum Mol Genet 18:1-11
9. Campanella A, Isaya G, O'Neill HA, Santambrogio P, Cozzi A, Arosio P, Levi S (2004) The expression of human mitochondrial ferritin rescues respiratory function in frataxin-deficient yeast. Hum Mol Genet 13:2279-2288 (Pubitemid 39359926)
10. Zanella I, Derosas M, Corrado M, Cocco E, Cavadini P, Biasiotto G, Poli M, Verardi R, Arosio P (2008) The effects of frataxin silencing in HeLa cells are rescued by the expression of human mitochondrial ferritin. Biochim Biophys Acta Mol Basis Dis 1782:90-98
11. Santambrogio P, Erba BG, Campanella A, Cozzi A, Causarano V, Cremonesi L, Gallì A, Della Porta MG, Invernizzi R, Levi S (2011) Over-expression of mitochondrial ferritin affects the JAK2/STAT5 pathway in K562 cells and causes mitochondrial iron accumulation. Haematologica 96:1424-1432
12. Invernizzi R, Travaglino E, Della Porta MG, Gallì A, Malcovati L, Rosti V, Bergamaschi G, Erba BG, Bellistri F, Bastia R et al (2013) Effects of mitochondrial ferritin overexpression in normal and sideroblastic erythroid progenitors. Br J Haematol 161:726-737
13. Tehranchi R, Invernizzi R, Grandien A, Zhivotovsky B, Fadeel B, Forsblom AM, Travaglino E, Samuelsson J, Hast R, Nilsson L et al (2005) Aberrant mitochondrial iron distribution and maturation arrest characterize early erythroid precursors in low-risk myelodysplastic syndromes. Blood 106:247-253 (Pubitemid 40967200)
14. Nie G, Chen G, Sheftel AD, Pantopoulos K, Ponka P (2006) In vivo tumor growth is inhibited by cytosolic iron deprivation caused by the expression of mitochondrial ferritin. Blood 108:2428-2434 (Pubitemid 44497529)
15. Nie G, Sheftel AD, Kim SF, Ponka P (2005) Overexpression of mitochondrial ferritin causes cytosolic iron depletion and changes cellular iron homeostasis. Blood 105:2161-2167 (Pubitemid 40731808)
16. Santambrogio P, Biasiotto G, Sanvito F, Olivieri S, Arosio P, Levi S (2007) Mitochondrial ferritin expression in adult mouse tissues. J Histochem Cytochem 55:1129-1137 (Pubitemid 350006295)
17. Jeong S, Rathore K, Schulz K, Ponka P, Arosio P, David S (2009) Dysregulation of iron homeostasis in the CNS contributes to disease progression in a mouse model of amyotrophic lateral sclerosis. J Neurosci 29:570-579
18. Shi Z, Nie G, Duan X, Rouault T, Wu W, Ning B, Zhang N, Chang Y, Zhao B (2010) Neuroprotective mechanism of mitochondrial ferritin on 6-hydroxydopamine-induced dopaminergic cell damage: implication for neuroprotection in Parkinson's disease. Antioxid Redox Signal 13:783-796
19. Lu Z, Nie G, Li Y, Soe-Lin S, Tao Y, Cao Y, Zhang Z, Liu N, Ponka P, Zhao B (2009) Overexpression of mitochondrial ferritin sensitizes cells to oxidative stress via an iron-mediated mechanism. Antioxid Redox Signal. doi:10.1089/ars.2008.2306
20. Wu WS, Zhao YS, Shi ZH, Chang SY, Nie GJ, Duan XL, Zhao SM, Wu Q, Yang ZL, Zhao BL et al (2013) Mitochondrial ferritin attenuates β-amyloid- induced neurotoxicity: reduction in oxidative damage through the Erk/P38 mitogen-activated protein kinase pathways. Antioxid Redox Signal 18:158-169
21. Yang H, Yang M, Guan H, Liu Z, Zhao S, Takeuchi S, Yanagisawa D, Tooyama I (2013) Mitochondrial ferritin in neurodegenerative diseases. Neurosci Res. doi:10.1016/j.neures.2013.07.005
22. Bartnikas TB, Campagna DR, Antiochos B, Mulhern H, Pondarré C, Fleming MD (2010) Characterization of mitochondrial ferritin-deficient mice. Am J Hematol 85:958-960
23. Minotti G, Licata S, Saponiero A, Menna P, Calafiore AM, Di Giammarco G, Liberi G, Animati F, Cipollone A, Manzini S et al (2000) Anthracycline metabolism and toxicity in human myocardium: comparisons between doxorubicin, epirubicin, and a novel disaccharide analogue with a reduced level of formation and [4Fe-4S] reactivity of its secondary alcohol metabolite. Chem Res Toxicol 13:1336-1341 (Pubitemid 32104013)
24. Minotti G, Menna P, Salvatorelli E, Cairo G, Gianni L (2004) Anthracyclines: molecular advances and pharmacologic developments in antitumor activity and cardiotoxicity. Pharmacol Rev 56:185-229 (Pubitemid 38720829)
25. Chen B, Peng X, Pentassuglia L, Lim CC, Sawyer DB (2007) Molecular and cellular mechanisms of anthracycline cardiotoxicity. Cardiovasc Toxicol 7:114-121 (Pubitemid 47339857)
26. Goormaghtigh E, Huart P, Praet M, Brasseur R, Ruysschaert JM (1990) Structure of the adriamycin-cardiolipin complex. Role in mitochondrial toxicity. Biophys Chem 35:247-257 (Pubitemid 20185442)
27. Salvatorelli E, Guarnieri S, Menna P, Liberi G, Calafiore AM, Mariggiò MA, Mordente A, Gianni L, Minotti G (2006) Defective one- or two-electron reduction of the anticancer anthracycline epirubicin in human heart. Relative importance of vesicular sequestration and impaired efficiency of electron addition. J Biol Chem281:10990-11001 (Pubitemid 43855522)
28. Octavia Y, Tocchetti CG, Gabrielson KL, Janssens S, Crijns HJ, Moens AL (2012) Doxorubicin-induced cardiomyopathy: from molecular mechanisms to therapeutic strategies. J Mol Cell Cardiol 52:1213-1225
29. Link G, Tirosh R, Pinson A, Hershko C (1996) Role of iron in the potentiation of anthracycline cardiotoxicity: identification of heart cell mitochondria as a major site of iron-anthracycline interaction. J Lab Clin Med 127:272-278 (Pubitemid 126657307)
30. Hershko C, Link G, Tzahor M, Kaltwasser JP, Athias P, Grynberg A, Pinson A (1993) Anthracycline toxicity is potentiated by iron and inhibited by deferoxamine: studies in rat heart cells in culture. J Lab Clin Med 122:245-251
31. Miranda CJ, Makui H, Soares RJ, Bilodeau M, Mui J, Vali H, Bertrand R, Andrews NC, Santos MM (2003) Hfe deficiency increases susceptibility to cardiotoxicity and exacerbates changes in iron metabolism induced by doxorubicin. Blood 102:2574-2580 (Pubitemid 37193598)
32. Panjrath GS, Patel V, Valdiviezo CI, Narula N, Narula J, Jain D (2007) Potentiation of Doxorubicin cardiotoxicity by iron loading in a rodent model. J Am Coll Cardiol 49:2457-2464 (Pubitemid 46962267)
33. Cocco E, Porrini V, Derosas M, Nardi V, Biasiotto G, Maccarinelli F, Zanella I (2013) Protective effect of mitochondrial ferritin on cytosolic iron dysregulation induced by doxorubicin in HeLa cells. Mol Biol Rep 40:6757-6764
34. Ichikawa Y, Ghanefar M, Bayeva M, Wu R, Khechaduri A, Naga Prasad SV, Mutharasan RK, Naik TJ, Ardehali H (2014) Cardiotoxicity of doxorubicin ismediated through mitochondrial iron accumulation. J Clin Invest 124:617-630
35. Liu P, Jenkins NA, Copeland NG (2003) A highly efficient recombineering-based method for generating conditional knockout mutations. Genome Res 13:476-484 (Pubitemid 36395405)
36. Corna G, Galy B, Hentze MW, Cairo G (2006) IRP1-independent alterations of cardiac iron metabolism in doxorubicin-treated mice. J Mol Med 84:551-560 (Pubitemid 43992847)
37. Stěrba M, Popelová O, Vávrová A, Jirkovský E, Kovaříková P, Geršl V, Simůnek T (2013) Oxidative stress, redox signaling, and metal chelation in anthracycline cardiotoxicity and pharmacological cardioprotection. Antioxid Redox Signal 18:899-929
38. Applegate LA, Luscher P, Tyrrell RM (1991) Induction of heme oxygenase: a general response to oxidant stress in cultured mammalian cells. Cancer Res 51:974-978
39. Corna G, Santambrogio P, Minotti G, Cairo G (2004) Doxorubicin paradoxically protects cardiomyocytes against iron-mediated toxicity: role of reactive oxygen species and ferritin. J Biol Chem 279:13738-13745 (Pubitemid 38468903)
40. Kuhn M, Voss M, Mitko D, Stypmann J, Schmid C, Kawaguchi N, Grabellus F, Baba HA (2004) Left ventricular assist device support reverses altered cardiac expression and function of natriuretic peptides and receptors in end-stage heart failure. Cardiovasc Res 64:308-314 (Pubitemid 39361692)
41. Smuder AJ, Kavazis AN, Min K (1985) Powers SK (2011) Exercise protects against doxorubicin-induced markers of autophagy signaling in skeletal muscle. J Appl Physiol 111:1190-1198
42. Takahashi H, Tainaka H, Umezawa M, Takeda K, Tanaka H, Nishimune Y, Oshio S (2011) Evaluation of testicular toxicology of doxorubicin based on microarray analysis of testicular specific gene expression. J Toxicol Sci 36:559-567
43. Figueira TR, Barros MH, Camargo AA, Castilho RF, Ferreira JC, Kowaltowski AJ, Sluse FE, Souza-Pinto NC, Vercesi AE (2013) Mitochondria as a source of reactive oxygen and nitrogen species: from molecularmechanisms to human health. Antioxid Redox Signal 18:2029-2074
44. Missirlis F, Holmberg S, Georgieva T, Dunkov BC, Rouault TA, Law JH (2006) Characterization of mitochondrial ferritin in Drosophila. Proc Natl Acad Sci U S A 103:5893-5898
45. Zancani M, Peresson C, Biroccio A, Federici G, Urbani A, Murgia I, Soave C, Micali F, Vianello A, Macri F (2004) Evidence for the presence of ferritin in plant mitochondria. Eur J Biochem 271:3657-3664 (Pubitemid 39233607)
46. Castiglioni E, Finazzi D, Goldwurm S, Levi S, Pezzoli G, Garavaglia B, Nardocci N, Malcovati L, Porta M, Gallì A et al (2010) Sequence variations in mitochondrial ferritin: distribution in healthy controls and different types of patients. Genet Test Mol Biomarkers, Ferritin. doi:10.1089/gtmb.2010.0076
47. Kang YJ, Chen Y, Yu A, Voss-McCowan M, Epstein PN (1997) Overexpression of metallothionein in the heart of transgenic mice suppresses doxorubicin cardiotoxicity. J Clin Invest 100:1501-1506 (Pubitemid 27425776)
48. Li K, Sung RY, Huang WZ, Yang M, Pong NH, Lee SM, Chan WY, Zhao H, To MY, Fok TF et al (2006) Thrombopoietin protects against in vitro and in vivo cardiotoxicity induced by doxorubicin. Circulation 113:2211-2220
49. Suliman HB, Carraway MS, Ali AS, Reynolds CM, Welty-Wolf KE, Piantadosi CA (2007) The CO/HO system reverses inhibition of mitochondrial biogenesis and prevents murine doxorubicin cardiomyopathy. J Clin Invest 117:3730-3741 (Pubitemid 350224084)
50. Sun X, Zhou Z, Kang YJ (2001) Attenuation of doxorubicin chronic toxicity in metallothionein-overexpressing transgenic mouse heart. Cancer Res 61:3382-3387 (Pubitemid 32695029)
51. Romao S, Münz C (2014) LC3-associated phagocytosis. Autophagy 10
52. Spagnuolo RD, Recalcati S, Tacchini L, Cairo G (2011) Role of hypoxia-inducible factors in the dexrazoxane-mediated protection of cardiomyocytes from doxorubicin-induced toxicity. Br J Pharmacol 163:299-312
53. Allen GF, Toth R, James J, Ganley IG (2013) Loss of iron triggers PINK1/Parkin-independent mitophagy. EMBO Rep 14:1127-1135