DOI: 10.1073/pnas.0912925107. Mitochondrial iron trafficking and the integration of iron metabolism between the mitochondrion and cytosol

Mitochondrial iron trafficking and the integration of iron metabolism between the mitochondrion and cytosol

10.1073/pnas.0912925107

Crossref journal-article

Proceedings of the National Academy of Sciences

Proceedings of the National Academy of Sciences (341)

Abstract

The mitochondrion is well known for its key role in energy transduction. However, it is less well appreciated that it is also a focal point of iron metabolism. Iron is needed not only for heme and iron sulfur cluster (ISC)-containing proteins involved in electron transport and oxidative phosphorylation, but also for a wide variety of cytoplasmic and nuclear functions, including DNA synthesis. The mitochondrial pathways involved in the generation of both heme and ISCs have been characterized to some extent. However, little is known concerning the regulation of iron uptake by the mitochondrion and how this is coordinated with iron metabolism in the cytosol and other organelles (e.g., lysosomes). In this article, we discuss the burgeoning field of mitochondrial iron metabolism and trafficking that has recently been stimulated by the discovery of proteins involved in mitochondrial iron storage (mitochondrial ferritin) and transport (mitoferrin-1 and -2). In addition, recent work examining mitochondrial diseases (e.g., Friedreich's ataxia) has established that communication exists between iron metabolism in the mitochondrion and the cytosol. This finding has revealed the ability of the mitochondrion to modulate whole-cell iron-processing to satisfy its own requirements for the crucial processes of heme and ISC synthesis. Knowledge of mitochondrial iron-processing pathways and the interaction between organelles and the cytosol could revolutionize the investigation of iron metabolism.

Bibliography

Richardson, D. R., Lane, D. J. R., Becker, E. M., Huang, M. L.-H., Whitnall, M., Rahmanto, Y. S., Sheftel, A. D., & Ponka, P. (2010). Mitochondrial iron trafficking and the integration of iron metabolism between the mitochondrion and cytosol. Proceedings of the National Academy of Sciences, 107(24), 10775â10782.

Authors 8

Des R. Richardson (first)
Darius J. R. Lane (additional)
Erika M. Becker (additional)
Michael L.-H. Huang (additional)
Megan Whitnall (additional)
Yohan Suryo Rahmanto (additional)
Alex D. Sheftel (additional)
Prem Ponka (additional)

References 107 Referenced 428

10.1182/blood-2004-10-3856
10.1146/annurev.biochem.76.052705.162653
10.1016/S0891-5849(02)00772-4
10.1073/pnas.80.8.2263
10.1016/S0021-9258(17)44637-0
10.1016/j.bbrc.2005.12.155
10.1016/j.bbrc.2010.02.148
10.1074/jbc.M402264200
10.1038/ng1659
10.1016/j.exphem.2006.02.004
10.1182/blood.V89.1.1
10.1016/j.tcb.2006.12.003
10.1021/bi00216a003
10.1038/ng1658
10.1073/pnas.0801318105
10.1073/pnas.95.3.1148
10.1182/blood.V50.3.433.433
10.1681/ASN.2006070802
10.1053/j.seminhematol.2009.06.001
10.1016/S0092-8674(04)00343-5
10.1073/pnas.93.16.8175
10.1017/S1462399407000531
10.1038/sj.emboj.7600041
10.1126/science.1103786
10.1016/S0021-9258(17)41250-6
JF Ross, The metabolism of inorganic and hemoglobin iron. J Clin Invest 25, 933 (1964). / J Clin Invest / The metabolism of inorganic and hemoglobin iron by Ross JF (1964)
10.1016/0014-5793(79)80111-8
10.1182/blood.V89.8.3025
10.1182/blood-2007-01-068148
10.1182/blood.V87.8.3477.bloodjournal8783477
10.1016/0167-4889(92)90196-I
10.1126/science.1157643
10.1038/nchembio.72
10.1023/A:1021202119942
10.1016/j.abb.2007.04.021
10.1042/BJ20061099
10.1159/000207141
P Ponka, J Neuwirt, J Borova, O Fuchs, Control of iron delivery to haemoglobin in erythroid cells. Ciba Foundation Symposium 51 - Iron Metabolism, eds R Porter, DW Fitzsimons (Elsevier/Excerpta Medica/North-Holland, Amsterdam), pp. 167–200 (1976). / Ciba Foundation Symposium 51 - Iron Metabolism by Ponka P (1976)
10.1182/blood-2004-06-2226
10.1073/pnas.0305895101
10.1016/0167-4889(82)90043-X
10.1016/0167-4889(89)90104-3
10.1038/84818
10.1073/pnas.0804261105
10.1073/pnas.0906784106
10.1126/science.276.5319.1709
10.1038/ng1097-215
10.1016/S0014-5793(99)00961-8
10.1093/hmg/ddn127
10.1182/blood-2004-07-2722
10.1007/s00109-009-0565-x
10.1016/j.ajhg.2007.12.012
10.1038/nature03887
10.1182/blood-2007-02-072520
10.1007/s00418-008-0394-y
10.1016/j.abb.2007.01.013
10.1074/jbc.M111789200
10.1074/jbc.M307847200
10.1016/j.bbamem.2009.03.004
10.1038/nature04512
10.1128/MCB.01685-08
10.1073/pnas.0904519106
10.1093/emboj/19.11.2492
10.1016/j.cmet.2009.06.012
10.1101/gad.873001
10.1074/jbc.C100141200
10.1369/jhc.7A7273.2007
10.1182/blood-2002-07-2006
10.1182/blood-2006-04-018341
10.1016/j.bbamcr.2006.05.011
10.1016/j.tem.2009.12.006
10.1016/j.tig.2008.05.008
10.1073/pnas.90.7.2754
10.1016/S1097-2765(00)80295-6
10.1021/bi000931n
10.1006/jmbi.1999.3294
10.1073/pnas.1732541100
10.1093/hmg/ddh324
10.1182/blood.V96.9.3256
10.1073/pnas.84.8.2256
10.1038/nature05125
10.1074/jbc.275.23.17536
10.1074/jbc.273.47.31388
10.1016/j.bbagen.2008.09.008
10.1093/hmg/6.11.1771
10.1038/ng0897-345
10.1093/hmg/9.8.1219
10.1074/jbc.M006539200
10.1038/nsmb.1579
10.1021/ja027967i
10.1074/jbc.C400107200
10.1007/s00415-009-1003-2
10.1080/10409230600846058
10.1042/BJ20091959
10.1086/303056
10.1093/hmg/11.16.1865
10.1021/bi048459j
10.1093/hmg/11.3.217
10.1182/blood.V99.10.3813
10.1016/j.bbagen.2008.09.004
10.1074/jbc.M800399200
10.1093/hmg/ddp495
10.1039/B703195E
SS Bottomley, Congenital sideroblastic anemias. Curr Hematol Rep 5, 41–49 (2006). / Curr Hematol Rep / Congenital sideroblastic anemias by Bottomley SS (2006)
10.1016/S0145-2126(99)00160-5
10.1038/ng.359
10.1086/421530

Dates

Type	When
Created	15 years, 3 months ago (May 21, 2010, 10:18 p.m.)
Deposited	3 years, 4 months ago (April 12, 2022, 6:41 p.m.)
Indexed	4 days, 5 hours ago (Sept. 3, 2025, 6:49 a.m.)
Issued	15 years, 3 months ago (May 21, 2010)
Published	15 years, 3 months ago (May 21, 2010)
Published Online	15 years, 3 months ago (May 21, 2010)
Published Print	15 years, 2 months ago (June 15, 2010)

Funders 0

None

BibTeX

@article{Richardson_2010, title={Mitochondrial iron trafficking and the integration of iron metabolism between the mitochondrion and cytosol}, volume={107}, ISSN={1091-6490}, url={http://dx.doi.org/10.1073/pnas.0912925107}, DOI={10.1073/pnas.0912925107}, number={24}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={Richardson, Des R. and Lane, Darius J. R. and Becker, Erika M. and Huang, Michael L.-H. and Whitnall, Megan and Rahmanto, Yohan Suryo and Sheftel, Alex D. and Ponka, Prem}, year={2010}, month=may, pages={10775–10782} }

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