Three conserved histidine residues contribute to mitochondrial iron transport through mitoferrins

Biochemical Journal

Volumn 460, Issue 1, 2014, Pages 79-89

  Brazzolotto, Xavier ^a,b,c   Pierrel, Fabien ^b,c,d,e   Pelosi, Ludovic ^a,b,d,f  

^a DIF   (France)

^b UNIV GRENOBLE ALPES   (France)

^c INSTITUT DE RECHERCHE BIOMÉDICALE DES ARMÉES   (France)

^d CEA GRENOBLE   (France)

^e CNRS   (France)

^f INSERM   (France)

Author keywords

Iron ligand; Iron metabolism; Mitochondrial transport; Mitoferrin; Yeas

Indexed keywords

FERROUS ION; GENOMIC DNA; HISTIDINE; IMIDAZOLE;

ARTICLE; BACTERIAL STRAIN; COMPARATIVE STUDY; CONTROLLED STUDY; ESCHERICHIA COLI; FUNGAL STRAIN; IN VIVO STUDY; IRON TRANSPORT; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; RNA SPLICING; YEAST;

AMINO ACID SEQUENCE; BIOLOGICAL TRANSPORT, ACTIVE; CATION TRANSPORT PROTEINS; CONSERVED SEQUENCE; ELECTRON TRANSPORT; ESCHERICHIA COLI PROTEINS; HISTIDINE; IRON; LIPOSOMES; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, SECONDARY; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84899452926     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20140107     Document Type: Article

References (43)

1. Lill, R. (2009) Function and biogenesis of iron-sulphur proteins. Nature 460, 831-838 CrossRef PubMed
2. Ajioka, R. S., Phillips, J. D. and Kushner, J. P. (2006) Biosynthesis of heme in mammals. Biochim. Biophys. Acta 1763, 723-736 CrossRef PubMed
3. Lill, R., Hoffmann, B., Molik, S., Pierik, A. J., Rietzschel, N., Stehling, O., Uzarska, M. A., Webert, H., Wilbrecht, C. and Muhlenhoff, U. (2012) The role of mitochondria in cellular iron-sulfur protein biogenesis and iron metabolism. Biochim. Biophys. Acta 1823, 1491-1508 CrossRef PubMed
4. Hamza, I. and Dailey, H. A. (2012) One ring to rule them all: trafficking of heme and heme synthesis intermediates in the metazoans. Biochim. Biophys. Acta 1823, 1617-1632 CrossRef PubMed
5. Richardson, D. R., Lane, D. J., Becker, E. M., Huang, M. L., Whitnall, M., Suryo Rahmanto, Y., Sheftel, A. D. and Ponka, P. (2010) Mitochondrial iron trafficking and the integration of iron metabolism between the mitochondrion and cytosol. Proc. Natl. Acad. Sci. U.S.A. 107, 10775-10782 CrossRef PubMed
6. Palmieri, F., Pierri, C. L., De Grassi, A., Nunes-Nesi, A. and Fernie, A. R. (2013) Evolution, structure and function of mitochondrial carriers: a review with new insights. Plant J. 66, 161-181 CrossRef
7. Walker, J. E. and Runswick, M. J. (1993) The mitochondrial transport protein superfamily. J. Bioenerg. Biomembr. 25, 435-446 CrossRef PubMed
8. Pebay-Peyroula, E., Dahout-Gonzalez, C., Kahn, R., Trézé guet, V., Lauquin, G. J. and Brandolin, G. (2003) Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside. Nature 426, 39-44 CrossRef PubMed
9. Palmieri, F., Agrimi, G., Blanco, E., Castegna, A., Di Noia, M. A., Iacobazzi, V., Lasorsa, F. M., Marobbio, C. M., Palmieri, L., Scarcia, P. et al. (2006) Identification of mitochondrial carriers in Saccharomyces cerevisiae by transport assay of reconstituted recombinant proteins. Biochim. Biophys. Acta 1757, 1249-1262 CrossRef PubMed
10. Foury, F. and Cazzalini, O. (1997) Deletion of the yeast homologue of the human gene associated with Friedreich's ataxia elicits iron accumulation in mitochondria. FEBS Lett. 411, 373-377 CrossRef PubMed
11. Foury, F. and Roganti, T. (2002) Deletion of the mitochondrial carrier genes MRS3 and MRS4 suppresses mitochondrial iron accumulation in a yeast frataxin-deficient strain. J. Biol. Chem. 277, 24475-24483CrossRef PubMed
12. Muhlenhoff, U., Stadler, J. A., Richhardt, N., Seubert, A., Eickhorst, T., Schweyen, R. J., Lill, R. and Wiesenberger, G. (2003) A specific role of the yeast mitochondrial carriers MRS3/4p in mitochondrial iron acquisition under iron-limiting conditions. J. Biol. Chem. 278, 40612-40620 CrossRef PubMed.
13. Zhang, Y., Lyver, E. R., Knight, S. A., Lesuisse, E. and Dancis, A. (2005) Frataxin and mitochondrial carrier proteins, Mrs3p and Mrs4p, cooperate in providing iron for heme synthesis. J. Biol. Chem. 280, 19794-19807 CrossRef PubMed
14. Zhang, Y., Lyver, E. R., Knight, S. A., Pain, D., Lesuisse, E. and Dancis, A. (2006) Mrs3p, Mrs4p, and frataxin provide iron for Fe-S cluster synthesis in mitochondria. J. Biol. Chem. 281, 22493-22502 CrossRef PubMed
15. Froschauer, E. M., Schweyen, R. J. and Wiesenberger, G. (2009) The yeast mitochondrial carrier proteins Mrs3p/Mrs4p mediate iron transport across the inner mitochondrial membrane. Biochim. Biophys. Acta 1788, 1044-1050 CrossRef PubMed
16. Shaw, G. C., Cope, J. J., Li, L., Corson, K., Hersey, C., Ackermann, G. E., Gwynn, B., Lambert, A. J., Wingert, R. A., Traver, D. et al. (2006) Mitoferrin is essential for erythroid iron assimilation. Nature 440, 96-100 CrossRef PubMed
17. Metzendorf, C., Wu, W. and Lind, M. I. (2009) Overexpression of Drosophila mitoferrin in l(2)mbn cells results in dysregulation of Fer1HCH expression. Biochem. J. 421, 463-471 CrossRef PubMed
18. Metzendorf, C. and Lind, M. I. (2010) Drosophila mitoferrin is essential for male fertility: evidence for a role of mitochondrial iron metabolism during spermatogenesis. BMC Dev. Biol. 10, 68 CrossRef PubMed
19. Ren, Y., Yang, S., Tan, G., Ye, W., Liu, D., Qian, X., Ding, Z., Zhong, Y., Zhang, J., Jiang, D. et al. (2012) Reduction of mitoferrin results in abnormal development and extended lifespan in Caenorhabditis elegans. PLoS ONE 7, e29666 CrossRef PubMed
20. Paradkar, P. N., Zumbrennen, K. B., Paw, B. H., Ward, D. M. and Kaplan, J. (2009) Regulation of mitochondrial iron import through differential turnover of mitoferrin 1 and mitoferrin 2. Mol. Cell. Biol. 29, 1007-1016 CrossRef PubMed
21. Huang, M. L., Becker, E. M., Whitnall, M., Suryo Rahmanto, Y., Ponka, P. and Richardson, D. R. (2009) Elucidation of the mechanism of mitochondrial iron loading in Friedreich's ataxia by analysis of a mouse mutant. Proc. Natl. Acad. Sci. U.S.A. 106, 16381-16386 CrossRef PubMed
22. Richardson, D. R., Huang, M. L., Whitnall, M., Becker, E. M., Ponka, P. and Suryo Rahmanto, Y. (2010) The ins and outs of mitochondrial iron-loading: the metabolic defect in Friedreich's ataxia. J. Mol. Med. 88, 323-329 CrossRef PubMed
23. Carroll, C. B., Zeissler, M. L., Chadborn, N., Gibson, K., Williams, G., Zajicek, J. P., Morrison, K. E. and Hanemann, C. O. (2011) Changes in iron-regulatory gene expression occur in human cell culture models of Parkinson's disease. Neurochem. Int. 59, 73-80 CrossRef PubMed
24. Miroux, B. and Walker, J. E. (1996) Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. J. Mol. Biol. 260, 289-298 CrossRef PubMed
25. Clemencon, B., Rey, M., Dianoux, A. C., Trezeguet, V., Lauquin, G. J., Brandolin, G. and Pelosi, L. (2008) Structure-function relationships of the C-terminal end of the Saccharomyces cerevisiae ADP/ATP carrier isoform 2. J. Biol. Chem. 283, 11218-11225 CrossRef PubMed
26. Palmieri, F., Indiveri, C., Bisaccia, F. and Iacobazzi, V. (1995) Mitochondrial metabolite carrier proteins: purification, reconstitution, and transport studies. Methods Enzymol. 260, 349-369 CrossRef PubMed
27. Dahout-Gonzalez, C., Ramus, C., Dassa, E. P., Dianoux, A. C. and Brandolin, G. (2005) Conformation-dependent swinging of the matrix loop m2 of the mitochondrial Saccharomyces cerevisiae ADP/ATP carrier. Biochemistry 44, 16310-16320 CrossRef PubMed
28. Riemer, J., Hoepken, H. H., Czerwinska, H., Robinson, S. R. and Dringen, R. (2004) Colorimetric ferrozine-based assay for the quantitation of iron in cultured cells. Anal. Biochem. 331, 370-375 CrossRef PubMed
29. Pena-Diaz, P., Pelosi, L., Ebikeme, C., Colasante, C., Gao, F., Bringaud, F. and Voncken, F. (2012) Functional characterization of TbMCP5, a conserved and essential ADP/ATP carrier present in the mitochondrion of the human pathogen Trypanosoma brucei. J. Biol. Chem. 287, 41861-41874 CrossRef PubMed
30. Connor, J., Yatvin, M. B. and Huang, L. (1984) pH-sensitive liposomes: acid-induced liposome fusion. Proc. Natl. Acad. Sci. U.S.A. 81, 1715-1718 CrossRef PubMed
31. Majima, E., Koike, H., Hong, Y. M., Shinohara, Y. and Terada, H. (1993) Characterization of cysteine residues of mitochondrial ADP/ATP carrier with the SH-reagents eosin 5-maleimide and N-ethylmaleimide. J. Biol. Chem. 268, 22181-22187 PubMed
32. Schroers, A., Kramer, R. and Wohlrab, H. (1997) The reversible antiport-uniport conversion of the phosphate carrier from yeast mitochondria depends on the presence of a single cysteine. J. Biol. Chem. 272, 10558-10564 CrossRef PubMed
33. Tonazzi, A., Giangregorio, N., Palmieri, F. and Indiveri, C. (2005) Relationships of cysteine and lysine residues with the substrate binding site of the mitochondrial ornithine/citrulline carrier: an inhibition kinetic approach combined with the analysis of the homology structural model. Biochim. Biophys. Acta 1718, 53-60 CrossRef PubMed
34. Vest, K. E., Leary, S. C., Winge, D. R. and Cobine, P. A. (2013) Copper import into the mitochondrial matrix in Saccharomyces cerevisiae is mediated by Pic2, a mitochondrial carrier family protein. J. Biol. Chem. 288, 23884-23892 CrossRef PubMed
35. Niviere, V. and Fontecave, M. (2004) Discovery of superoxide reductase: an historical perspective. J. Biol. Inorg. Chem. 9, 119-123 CrossRef PubMed
36. Hakemian, A. S. and Rosenzweig, A. C. (2007) The biochemistry of methane oxidation. Annu. Rev. Biochem. 76, 223-241 CrossRef PubMed
37. Zuris, J. A., Harir, Y., Conlan, A. R., Shvartsman, M., Michaeli, D., Tamir, S., Paddock, M. L., Onuchic, J. N., Mittler, R., Cabantchik, Z. I. et al. (2011) Facile transfer of [2Fe-2S] clusters from the diabetes drug target mitoNEET to an apo-acceptor protein. Proc. Natl. Acad. Sci. U.S.A. 108, 13047-13052 CrossRef PubMed
38. Rey,M., Man, P., Clémencon, B., Trézéguet, V., Brandolin, G., Forest, E. and Pelosi, L. (2010) Conformational dynamics of the bovine mitochondrial ADP/ATP carrier isoform 1 revealed by hydrogen/deuterium exchange coupled to mass spectrometry. J. Biol. Chem. 285, 34981-34990 CrossRef PubMed
39. David, C., Arnou, B., Sanchez, J. F., Pelosi, L., Brandolin, G., Lauquin, G. J. and Trézéguet, V. (2008) Two residues of a conserved aromatic ladder of the mitochondrial ADP/ATP carrier are crucial to nucleotide transport. Biochemistry 47, 13223-13231 CrossRef PubMed
40. Shawki, A., Knight, P. B., Maliken, B. D., Niespodzany, E. J. and Mackenzie, B. (2012) H+ -coupled divalent metal-ion transporter-1: functional properties, physiological roles nd therapeutics. Curr. Top. Membr. 70, 169-214 CrossRef PubMed
41. Yoon, H., Zhang, Y., Pain, J., Lyver, E. R., Lesuisse, E., Pain, D. and Dancis, A. (2011) Rim2, a pyrimidine nucleotide exchanger, is needed for iron utilization in mitochondria. Biochem. J. 440, 137-146 CrossRef PubMed
42. Froschauer, E. M., Rietzschel, N., Hassler, M. R., Binder, M., Schweyen, R. J., Lill, R., Muhlenhoff, U. and Wiesenberger, G. (2013) The mitochondrial carrier Rim2 co-imports pyrimidine nucleotides and iron. Biochem. J. 455, 57-65 CrossRef PubMed
43. Waterhouse, A. M., Procter, J. B., Martin, D. M., Clamp, M. and Barton, G. J. (2009) Jalview Version 2: a multiple sequence alignment editor and analysis workbench. Bioinformatics 25, 1189-1191 CrossRef PubMed