Iron Regulatory Protein 1 Sustains Mitochondrial Iron Loading and Function in Frataxin Deficiency

Cell Metabolism

Volumn 21, Issue 2, 2015, Pages 311-323

  Martelli, Alain ^a,b,c,d,e   Schmucker, Stéphane ^a,b,c,d,e   Reutenauer, Laurence ^a,b,c,d,e   Mathieu, Jacques R R ^f   Peyssonnaux, Carole ^f   Karim, Zoubida ^g   Puy, Hervé ^g,h   Galy, Bruno ⁱ   Hentze, Matthias W ⁱ   Puccio, Hélène ^a,b,c,d,e  

^a INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^b INSERM   (France)

^c CNRS   (France)

^d UNIVERSITÉ DE STRASBOURG   (France)

^e Centre de Recherche Interdisciplinaire en Biologie   (France)

^f INSTITUT COCHIN   (France)

^g CENTRE DE RECHERCHE SUR L INFLAMMATION   (France)

^h HÔPITAL LOUIS MOURIER   (France)

ⁱ EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FRATAXIN; HEME; IRON; IRON REGULATORY PROTEIN 1; IRON SULFUR CLUSTER; MITOFERRIN 2; PROTEIN; SULFUR; UNCLASSIFIED DRUG; IRON BINDING PROTEIN; IRON SULFUR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FRIEDREICH ATAXIA; IRON METABOLISM; IRON STORAGE; METABOLISM; MITOCHONDRION; MOLECULAR BIOLOGY; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN FUNCTION; ANIMAL; C57BL MOUSE; DEFICIENCY; GENETICS; KNOCKOUT MOUSE; LIVER; PATHOLOGY;

MUS;

ANIMALS; FRIEDREICH ATAXIA; IRON; IRON REGULATORY PROTEIN 1; IRON-BINDING PROTEINS; IRON-SULFUR PROTEINS; LIVER; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA;

EID: 84922861201     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2015.01.010     Document Type: Article

References (52)

1. M. Abitbol, F. Bernex, H. Puy, H. Jouault, J.C. Deybach, J.L. Guénet, and X. Montagutelli A mouse model provides evidence that genetic background modulates anemia and liver injury in erythropoietic protoporphyria Am. J. Physiol. Gastrointest. Liver Physiol. 288 2005 G1208 G1216
2. R. Allikmets, W.H. Raskind, A. Hutchinson, N.D. Schueck, M. Dean, and D.M. Koeller Mutation of a putative mitochondrial iron transporter gene (ABC7) in X-linked sideroblastic anemia and ataxia (XLSA/A) Hum. Mol. Genet. 8 1999 743 749
3. S.A. Anderson, C.P. Nizzi, Y.I. Chang, K.M. Deck, P.J. Schmidt, B. Galy, A. Damnernsawad, A.T. Broman, C. Kendziorski, and M.W. Hentze The IRP1-HIF-2α axis coordinates iron and oxygen sensing with erythropoiesis and iron absorption Cell Metab. 17 2013 282 290
4. L.K. Beilschmidt, and H.M. Puccio Mammalian Fe-S cluster biogenesis and its implication in disease Biochimie 100 2014 48 60
5. G. Bozzini, P. Colin, N. Betrouni, C.A. Maurage, X. Leroy, S. Simonin, C. Martin-Schmitt, A. Villers, and S. Mordon Efficiency of 5-ALA mediated photodynamic therapy on hypoxic prostate cancer: a preclinical study on the Dunning R3327-AT2 rat tumor model Photodiagn. Photodyn. Ther. 10 2013 296 303
6. N. Calmels, S. Schmucker, M. Wattenhofer-Donzé, A. Martelli, N. Vaucamps, L. Reutenauer, N. Messaddeq, C. Bouton, M. Koenig, and H. Puccio The first cellular models based on frataxin missense mutations that reproduce spontaneously the defects associated with Friedreich ataxia PLoS ONE 4 2009 e6379
7. D. Casarrubea, L. Viatte, T. Hallas, A. Vasanthakumar, R.S. Eisenstein, K. Schümann, M.W. Hentze, and B. Galy Abnormal body iron distribution and erythropoiesis in a novel mouse model with inducible gain of iron regulatory protein (IRP)-1 function J. Mol. Med. 91 2013 871 881
8. S. Cipolat, O. Martins de Brito, B. Dal Zilio, and L. Scorrano OPA1 requires mitofusin 1 to promote mitochondrial fusion Proc. Natl. Acad. Sci. USA 101 2004 15927 15932
9. S.L. Clarke, A. Vasanthakumar, S.A. Anderson, C. Pondarré, C.M. Koh, K.M. Deck, J.S. Pitula, C.J. Epstein, M.D. Fleming, and R.S. Eisenstein Iron-responsive degradation of iron-regulatory protein 1 does not require the Fe-S cluster EMBO J. 25 2006 544 553
10. S. Cogliati, C. Frezza, M.E. Soriano, T. Varanita, R. Quintana-Cabrera, M. Corrado, S. Cipolat, V. Costa, A. Casarin, and L.C. Gomes Mitochondrial cristae shape determines respiratory chain supercomplexes assembly and respiratory efficiency Cell 155 2013 160 171
11. F. Colin, A. Martelli, M. Clémancey, J.M. Latour, S. Gambarelli, L. Zeppieri, C. Birck, A. Page, H. Puccio, and S. Ollagnier de Choudens Mammalian frataxin controls sulfur production and iron entry during de novo Fe4S4 cluster assembly J. Am. Chem. Soc. 135 2013 733 740
12. D.R. Crooks, T.G. Natarajan, S.Y. Jeong, C. Chen, S.Y. Park, H. Huang, M.C. Ghosh, W.H. Tong, R.G. Haller, C. Wu, and T.A. Rouault Elevated FGF21 secretion, PGC-1α and ketogenic enzyme expression are hallmarks of iron-sulfur cluster depletion in human skeletal muscle Hum. Mol. Genet. 23 2014 24 39
13. C. Delaby, N. Pilard, H. Puy, and F. Canonne-Hergaux Sequential regulation of ferroportin expression after erythrophagocytosis in murine macrophages: early mRNA induction by haem, followed by iron-dependent protein expression Biochem. J. 411 2008 123 131
14. F. Diaz, S. Garcia, D. Hernandez, A. Regev, A. Rebelo, J. Oca-Cossio, and C.T. Moraes Pathophysiology and fate of hepatocytes in a mouse model of mitochondrial hepatopathies Gut 57 2008 232 242
15. B. Galy, D. Ferring, B. Minana, O. Bell, H.G. Janser, M. Muckenthaler, K. Schümann, and M.W. Hentze Altered body iron distribution and microcytosis in mice deficient in iron regulatory protein 2 (IRP2) Blood 106 2005 2580 2589
16. B. Galy, D. Ferring-Appel, S.W. Sauer, S. Kaden, S. Lyoumi, H. Puy, S. Kölker, H.J. Gröne, and M.W. Hentze Iron regulatory proteins secure mitochondrial iron sufficiency and function Cell Metab. 12 2010 194 201
17. M.C. Ghosh, D.L. Zhang, S.Y. Jeong, G. Kovtunovych, H. Ollivierre-Wilson, A. Noguchi, T. Tu, T. Senecal, G. Robinson, and D.R. Crooks Deletion of iron regulatory protein 1 causes polycythemia and pulmonary hypertension in mice through translational derepression of HIF2α Cell Metab. 17 2013 271 281
18. B. Guillon, A.L. Bulteau, M. Wattenhofer-Donzé, S. Schmucker, B. Friguet, H. Puccio, J.C. Drapier, and C. Bouton Frataxin deficiency causes upregulation of mitochondrial Lon and ClpP proteases and severe loss of mitochondrial Fe-S proteins FEBS J. 276 2009 1036 1047
19. H. Gunshin, C.R. Allerson, M. Polycarpou-Schwarz, A. Rofts, J.T. Rogers, F. Kishi, M.W. Hentze, T.A. Rouault, N.C. Andrews, and M.A. Hediger Iron-dependent regulation of the divalent metal ion transporter FEBS Lett. 509 2001 309 316
20. M.W. Hentze, M.U. Muckenthaler, B. Galy, and C. Camaschella Two to tango: regulation of Mammalian iron metabolism Cell 142 2010 24 38
21. C. Homedan, J. Laafi, C. Schmitt, N. Gueguen, T. Lefebvre, Z. Karim, V. Desquiret-Dumas, C. Wetterwald, J.C. Deybach, and L. Gouya Acute intermittent porphyria causes hepatic mitochondrial energetic failure in a mouse model Int. J. Biochem. Cell Biol. 51 2014 93 101
22. M.L. Huang, E.M. Becker, M. Whitnall, Y. Suryo Rahmanto, P. Ponka, and D.R. Richardson Elucidation of the mechanism of mitochondrial iron loading in Friedreich's ataxia by analysis of a mouse mutant Proc. Natl. Acad. Sci. USA 106 2009 16381 16386
23. M.L. Huang, S. Sivagurunathan, S. Ting, P.J. Jansson, C.J. Austin, M. Kelly, C. Semsarian, D. Zhang, and D.R. Richardson Molecular and functional alterations in a mouse cardiac model of Friedreich ataxia: activation of the integrated stress response, eIF2α phosphorylation, and the induction of downstream targets Am. J. Pathol. 183 2013 745 757
24. E. Lesuisse, R. Santos, B.F. Matzanke, S.A. Knight, J.M. Camadro, and A. Dancis Iron use for haeme synthesis is under control of the yeast frataxin homologue (Yfh1) Hum. Mol. Genet. 12 2003 879 889
25. K. Li, E.K. Besse, D. Ha, G. Kovtunovych, and T.A. Rouault Iron-dependent regulation of frataxin expression: implications for treatment of Friedreich ataxia Hum. Mol. Genet. 17 2008 2265 2273
26. R. Lill Function and biogenesis of iron-sulphur proteins Nature 460 2009 831 838
27. R.L. Lindberg, C. Porcher, B. Grandchamp, B. Ledermann, K. Bürki, S. Brandner, A. Aguzzi, and U.A. Meyer Porphobilinogen deaminase deficiency in mice causes a neuropathy resembling that of human hepatic porphyria Nat. Genet. 12 1996 195 199
28. R.L. Lindberg, R. Martini, M. Baumgartner, B. Erne, J. Borg, J. Zielasek, K. Ricker, A. Steck, K.V. Toyka, and U.A. Meyer Motor neuropathy in porphobilinogen deaminase-deficient mice imitates the peripheral neuropathy of human acute porphyria J. Clin. Invest. 103 1999 1127 1134
29. A. Martelli, and H. Puccio Dysregulation of cellular iron metabolism in Friedreich ataxia: from primary iron-sulfur cluster deficit to mitochondrial iron accumulation Front Pharmacol 5 2014 130
30. A. Martelli, M. Wattenhofer-Donzé, S. Schmucker, S. Bouvet, L. Reutenauer, and H. Puccio Frataxin is essential for extramitochondrial Fe-S cluster proteins in mammalian tissues Hum. Mol. Genet. 16 2007 2651 2658
31. A. Martelli, L.S. Friedman, L. Reutenauer, N. Messaddeq, S.L. Perlman, D.R. Lynch, K. Fedosov, J.B. Schulz, M. Pandolfo, and H. Puccio Clinical data and characterization of the liver conditional mouse model exclude neoplasia as a non-neurological manifestation associated with Friedreich's ataxia Dis. Model. Mech. 5 2012 860 869
32. A. Martelli, M. Napierala, and H. Puccio Understanding the genetic and molecular pathogenesis of Friedreich's ataxia through animal and cellular models Dis. Model. Mech. 5 2012 165 176
33. M. Mastrogiannaki, P. Matak, J.R. Mathieu, S. Delga, P. Mayeux, S. Vaulont, and C. Peyssonnaux Hepatic hypoxia-inducible factor-2 down-regulates hepcidin expression in mice through an erythropoietin-mediated increase in erythropoiesis Haematologica 97 2012 827 834
34. E.G. Meyron-Holtz, M.C. Ghosh, K. Iwai, T. LaVaute, X. Brazzolotto, U.V. Berger, W. Land, H. Ollivierre-Wilson, A. Grinberg, P. Love, and T.A. Rouault Genetic ablations of iron regulatory proteins 1 and 2 reveal why iron regulatory protein 2 dominates iron homeostasis EMBO J. 23 2004 386 395
35. S. Michael, S.V. Petrocine, J. Qian, J.B. Lamarche, M.D. Knutson, M.D. Garrick, and A.H. Koeppen Iron and iron-responsive proteins in the cardiomyopathy of Friedreich's ataxia Cerebellum 5 2006 257 267
36. F. Mochel, M.A. Knight, W.H. Tong, D. Hernandez, K. Ayyad, T. Taivassalo, P.M. Andersen, A. Singleton, T.A. Rouault, K.H. Fischbeck, and R.G. Haller Splice mutation in the iron-sulfur cluster scaffold protein ISCU causes myopathy with exercise intolerance Am. J. Hum. Genet. 82 2008 652 660
37. F. Pallotti, and G. Lenaz Isolation and subfractionation of mitochondria from animal cells and tissue culture lines Methods Cell Biol. 80 2007 3 44
38. C. Pondarré, B.B. Antiochos, D.R. Campagna, S.L. Clarke, E.L. Greer, K.M. Deck, A. McDonald, A.P. Han, A. Medlock, and J.L. Kutok The mitochondrial ATP-binding cassette transporter Abcb7 is essential in mice and participates in cytosolic iron-sulfur cluster biogenesis Hum. Mol. Genet. 15 2006 953 964
39. H. Puccio, D. Simon, M. Cossée, P. Criqui-Filipe, F. Tiziano, J. Melki, C. Hindelang, R. Matyas, P. Rustin, and M. Koenig Mouse models for Friedreich ataxia exhibit cardiomyopathy, sensory nerve defect and Fe-S enzyme deficiency followed by intramitochondrial iron deposits Nat. Genet. 27 2001 181 186
40. A.A. Salahudeen, J.W. Thompson, J.C. Ruiz, H.W. Ma, L.N. Kinch, Q. Li, N.V. Grishin, and R.K. Bruick An E3 ligase possessing an iron-responsive hemerythrin domain is a regulator of iron homeostasis Science 326 2009 722 726
41. A. Seguin, R. Santos, D. Pain, A. Dancis, J.M. Camadro, and E. Lesuisse Co-precipitation of phosphate and iron limits mitochondrial phosphate availability in Saccharomyces cerevisiae lacking the yeast frataxin homologue (YFH1) J. Biol. Chem. 286 2011 6071 6079
42. H. Seznec, D. Simon, C. Bouton, L. Reutenauer, A. Hertzog, P. Golik, V. Procaccio, M. Patel, J.C. Drapier, M. Koenig, and H. Puccio Friedreich ataxia: the oxidative stress paradox Hum. Mol. Genet. 14 2005 463 474
43. A.D. Sheftel, C. Wilbrecht, O. Stehling, B. Niggemeyer, H.P. Elsässer, U. Mühlenhoff, and R. Lill The human mitochondrial ISCA1, ISCA2, and IBA57 proteins are required for [4Fe-4S] protein maturation Mol. Biol. Cell 23 2012 1157 1166
44. Y.S. Sohn, W. Breuer, A. Munnich, and Z.I. Cabantchik Redistribution of accumulated cell iron: a modality of chelation with therapeutic implications Blood 111 2008 1690 1699
45. O. Stehling, H.P. Elsässer, B. Brückel, U. Mühlenhoff, and R. Lill Iron-sulfur protein maturation in human cells: evidence for a function of frataxin Hum. Mol. Genet. 13 2004 3007 3015
46. W.H. Tong, and T.A. Rouault Functions of mitochondrial ISCU and cytosolic ISCU in mammalian iron-sulfur cluster biogenesis and iron homeostasis Cell Metab. 3 2006 199 210
47. C.L. Tsai, and D.P. Barondeau Human frataxin is an allosteric switch that activates the Fe-S cluster biosynthetic complex Biochemistry 49 2010 9132 9139
48. Y. Tsuji, H. Ayaki, S.P. Whitman, C.S. Morrow, S.V. Torti, and F.M. Torti Coordinate transcriptional and translational regulation of ferritin in response to oxidative stress Mol. Cell. Biol. 20 2000 5818 5827
49. A.A. Vashisht, K.B. Zumbrennen, X. Huang, D.N. Powers, A. Durazo, D. Sun, N. Bhaskaran, A. Persson, M. Uhlen, and O. Sangfelt Control of iron homeostasis by an iron-regulated ubiquitin ligase Science 326 2009 718 721
50. W.W. Wasserman, and W.E. Fahl Functional antioxidant responsive elements Proc. Natl. Acad. Sci. USA 94 1997 5361 5366
51. M. Whitnall, Y. Suryo Rahmanto, R. Sutak, X. Xu, E.M. Becker, M.R. Mikhael, P. Ponka, and D.R. Richardson The MCK mouse heart model of Friedreich's ataxia: Alterations in iron-regulated proteins and cardiac hypertrophy are limited by iron chelation Proc. Natl. Acad. Sci. USA 105 2008 9757 9762
52. M. Whitnall, Y. Suryo Rahmanto, M.L. Huang, F. Saletta, H.C. Lok, L. Gutiérrez, F.J. Lázaro, A.J. Fleming, T.G. St Pierre, and M.R. Mikhael Identification of nonferritin mitochondrial iron deposits in a mouse model of Friedreich ataxia Proc. Natl. Acad. Sci. USA 109 2012 20590 20595