Mitochondria represent another locale for the divalent metal transporter 1 (DMT1)

Channels

Volumn 8, Issue 5, 2014, Pages 458-466

  Wolff, Natascha A ^a   Garrick, Laura M ^b   Zhao, Lin ^b   Garrick, Michael D ^b   Thévenod, Frank ^a  

^a UNIVERSITY OF WITTEN HERDECKE   (Germany)

^b UNIVERSITY AT BUFFALO   (United States)

Author keywords

Divalent metal transporter 1 (DMT1); Flow cytometry; Immunofluorescence microscopy; Iron transport; Mitochondrial outer membrane

Indexed keywords

MANGANESE; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 2; DMRT1 PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CHO CELL LINE; FLOW CYTOMETRY; GENE EXPRESSION SYSTEM; HEK293 CELL LINE; IMMUNOFLUORESCENCE MICROSCOPY; IRON TRANSPORT; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; MOUSE; NONHUMAN; PROTEIN EXPRESSION; RAT; ANIMAL; CRICETULUS; HUMAN; METABOLISM;

ANIMALS; CHO CELLS; CRICETULUS; HUMANS; MITOCHONDRIA; TRANSCRIPTION FACTORS;

EID: 84926644935     PISSN: 19336950     EISSN: 19336969     Source Type: Journal    
DOI: 10.4161/19336950.2014.956564     Document Type: Article

References (53)

1. Chen C, Paw BH. Cellular and mitochondrial iron homeostasis in vertebrates. Biochim Biophys Acta 2012; 1823:1459-67; PMID:22285816; http://dx.doi.org/10.1016/j.bbamcr.2012.01.003
2. Sheftel AD, Mason AB, Ponka P. The long history of iron in the Universe and in health and disease. Biochim Biophys Acta 2012; 1820:161-87; PMID:21856378; http://dx.doi.org/10.1016/j.bbagen.2011.08.002
3. Lill R, Hoffmann B, Molik S, Pierik AJ, Rietzschel N, Stehling O, Uzarska MA, Webert H, Wilbrecht C, Mühlenhoff U. The role of mitochondria in cellular iron-sulfur protein biogenesis and iron metabolism. Biochim Biophys Acta 2012; 1823:1491-508; PMID:22609301; http://dx.doi.org/10.1016/j.bbamcr.2012.05.009
4. Paradkar PN, Zumbrennen KB, Paw BH, Ward DM, Kaplan J. Regulation of mitochondrial iron import through differential turnover of mitoferrin 1 and mitoferrin 2. Mol Cell Biol 2009; 29:1007-16; PMID:19075006; http://dx.doi.org/10.1128/MCB.01685-08
5. Xu W, Barrientos T, Andrews NC. Iron and copper in mitochondrial diseases. Cell Metab 2013; 17:319-28; PMID:23473029; http://dx.doi.org/10.1016/j.cmet.2013.02.004
6. Colombini M. VDAC structure, selectivity, and dynamics. Biochim Biophys Acta 2012; 1818:1457-65; PMID:22240010; http://dx.doi.org/10.1016/j.bbamem.2011.12.026
7. Fleming MD, Romano MA, Su MA, Garrick LM, Garrick MD, Andrews NC. Nramp2 is mutated in the anemic Belgrade (b) rat: evidence of a role for Nramp2 in endosomal iron transport. Proc Natl Acad Sci U S A 1998; 95:1148-53; PMID:9448300; http://dx.doi.org/10.1073/pnas.95.3.1148
8. Zhang AS, Enns CA. Molecular mechanisms of normal iron homeostasis. Hematology Am Soc Hematol Educ Program 2009: 207-14; PMID:20008200; http://dx.doi.org/10.1182/asheducation-2009.1.207
9. Wolff NA, Ghio AJ, Garrick LM, Garrick MD, Zhao L, Fenton RA, Thévenod F. Evidence for mitochondrial localization of divalent metal transporter 1 (DMT1). FASEB J 2014; 28:2134-45; PMID:24448823; http://dx.doi.org/10.1096/fj.13-240564
10. Bolte S, Cordelieres FP. A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 2006; 224:213-32; PMID:17210054; http://dx.doi.org/10.1111/j.1365-2818.2006.01706.x
11. Woost PG, Orosz DE, Jin W, Frisa PS, Jacobberger JW, Douglas JG, Hopfer U. Immortalization and characterization of proximal tubule cells derived from kidneys of spontaneously hypertensive and normotensive rats. Kidney Int 1996; 50:125-34; PMID:8807581; http://dx.doi.org/10.1038/ki.1996.295
12. Abouhamed M, Gburek J, Liu W, Torchalski B, Wilhelm A, Wolff NA, Christensen EI, Thévenod F, Smith CP. Divalent metal transporter 1 in the kidney proximal tubule is expressed in late endosomeslysosomal membranes: implications for renal handling of proteinmetal complexes. Am J Physiol Renal Physiol 2006; 290:F1525-F1533; PMID:16449358; http://dx.doi.org/10.1152/ajprenal.00359.2005
13. Porcelli AM, Ghelli A, Zanna C, Pinton P, Rizzuto R, Rugolo M. pH difference across the outer mitochondrial membrane measured with a green fluorescent protein mutant. Biochem Biophys Res Commun 2005; 326:799-804; PMID:15607740; http://dx.doi.org/10.1016/j.bbrc.2004.11.105
14. Richardson DR, Lane DJ, Becker EM, Huang ML, Whitnall M, Suryo RY, Sheftel AD, Ponka P. Mitochondrial iron trafficking and the integration of iron metabolism between the mitochondrion and cytosol. Proc Natl Acad Sci U S A 2010; 107:10775-82; PMID:20495089; http://dx.doi.org/10.1073/pnas.0912925107
15. Sheftel AD, Richardson DR, Prchal J, Ponka P. Mitochondrial iron metabolism and sideroblastic anemia. Acta Haematol 2009; 122:120-33; PMID:19907149; http://dx.doi.org/10.1159/000243796
16. Pantopoulos K, Porwal SK, Tartakoff A, Devireddy L. Mechanisms of mammalian iron homeostasis. Biochemistry 2012; 51:5705-24; PMID:22703180; http://dx.doi.org/10.1021/bi300752r
17. Pagliarini DJ, Calvo SE, Chang B, Sheth SA, Vafai SB, Ong SE, Walford GA, Sugiana C, Boneh A, Chen WK, et al. A mitochondrial protein compendium elucidates complex I disease biology. Cell 2008; 134:112-23; PMID:18614015; http://dx.doi.org/10.1016/j.cell.2008.06.016
18. Nilsson R, Schultz IJ, Pierce EL, Soltis KA, Naranuntarat A, Ward DM, Baughman JM, Paradkar PN, Kingsley PD, Culotta VC, et al. Discovery of genes essential for heme biosynthesis through large-scale gene expression analysis. Cell Metab 2009; 10:119-30; PMID:19656490; http://dx.doi.org/10.1016/j.cmet.2009.06.012
19. Monné M, Palmieri F. Antiporters of the mitochondrial carrier family. Curr Top Membr 2014; 73:289-20; PMID:24745987; http://dx.doi.org/10.1016/B978-0-12-800223-0.00008-6
20. Gunshin H, Mackenzie B, Berger UV, Gunshin Y, Romero MF, Boron WF, Nussberger S, Gollan JL, Hediger MA. Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature 1997; 388:482-8; PMID:9242408; http://dx.doi.org/10.1038/41343
21. Garrick MD, Kuo HC, Vargas F, Singleton S, Zhao L, Smith JJ, Paradkar P, Roth JA, Garrick LM. Comparison of mammalian cell lines expressing distinct isoforms of divalent metal transporter 1 in a tetracycline-regulated fashion. Biochem J 2006; 398:539-46; PMID:16737442; http://dx.doi.org/10.1042/BJ20051987
22. + -coupled Fe2+ transport and uncoupled fluxes. Pflugers Arch 2006; 451:544-58; PMID:16091957; http://dx.doi.org/10.1007/s00424-005-1494-3
23. Trinder D, Oates PS, Thomas C, Sadleir J, Morgan EH. Localisation of divalent metal transporter 1 (DMT1) to the microvillus membrane of rat duodenal enterocytes in iron deficiency, but to hepatocytes in iron overload. Gut 2000; 46:270-6; PMID:10644324; http://dx.doi.org/10.1136/gut.46.2.270
24. Ke Y, Chen YY, Chang YZ, Duan XL, Ho KP, Jiang DH, Wang K, Qian ZM. Post-transcriptional expression of DMT1 in the heart of rat. J Cell Physiol 2003; 196:124-30; PMID:12767048; http://dx.doi.org/10.1002/jcp.10284
25. Petrat F, Weisheit D, Lensen M, de GH, Sustmann R, Rauen U. Selective determination of mitochondrial chelatable iron in viable cells with a new fluorescent sensor. Biochem J 2002; 362:137-47; PMID:11829750; http://dx.doi.org/10.1042/0264-6021:3620137
26. Petrat F, de GH, Rauen U. Subcellular distribution of chelatable iron: a laser scanning microscopic study in isolated hepatocytes and liver endothelial cells. Biochem J 2001; 356:61-9; PMID:11336636; http://dx.doi.org/10.1042/0264-6021:3560061
27. Drysdale J, Arosio P, Invernizzi R, Cazzola M, Volz A, Corsi B, Biasiotto G, Levi S. Mitochondrial ferritin: a new player in iron metabolism. Blood Cells Mol Dis 2002; 29:376-83; PMID:12547228; http://dx.doi.org/10.1006/bcmd.2002.0577
28. Hamza I, Dailey HA. One ring to rule them all: Trafficking of heme and heme synthesis intermediates in the metazoans. Biochim Biophys Acta 2012; 1823:1617-32; PMID:22575458; http://dx.doi.org/10.1016/j.bbamcr.2012.04.009
29. Ajioka RS, Phillips JD, Kushner JP. Biosynthesis of heme in mammals. Biochim Biophys Acta 2006; 1763:723-36; PMID:16839620; http://dx.doi.org/10.1016/j.bbamcr.2006.05.005
30. Mackenzie B, Takanaga H, Hubert N, Rolfs A, Hediger MA. Functional properties of multiple isoforms of human divalent metal-ion transporter 1 (DMT1). Biochem J 2007; 403:59-69; PMID:17109629; http://dx.doi.org/10.1042/BJ20061290
31. Illing AC, Shawki A, Cunningham CL, Mackenzie B. Substrate profile and metal-ion selectivity of human divalent metal-ion transporter-1. J Biol Chem 2012; 287:30485-96; PMID:22736759; http://dx.doi.org/10.1074/jbc.M112.364208
32. Flynn JM, Melov S. SOD2 in mitochondrial dysfunction and neurodegeneration. Free Radic Biol Med 2013; 62:4-12; PMID:23727323; http://dx.doi.org/10.1016/j.freeradbiomed.2013.05.027
33. Kawaguchi T, Noji S, Uda T, Nakashiman Y, Takeyasu A, Kawai Y, Takagi H, Tohyama M, Taniguchi N. A monoclonal antibody against COOH-terminal peptide of human liver manganese superoxide dismutase. J Biol Chem 1989; 264:5762-67; PMID:2647725
34. Aguirre JD, Culotta VC. Battles with iron: manganese in oxidative stress protection. J Biol Chem 2012; 287:13541-48; PMID:22247543; http://dx.doi.org/10.1074/jbc.R111.312181
35. Roth J, Ponzoni S, Aschner M. Manganese homeostasis and transport. Met Ions Life Sci 2013; 12:169-201; PMID:23595673; http://dx.doi.org/10.1007/978-94-007-5561-1-6
36. Portnoy ME, Liu XF, Culotta VC. Saccharomyces cerevisiae expresses three functionally distinct homologues of the nramp family of metal transporters. Mol Cell Biol 2000; 20:7893-902; PMID:11027260; http://dx.doi.org/10.1128/MCB.20.21.7893-7902.2000
37. Sickmann A, Reinders J, Wagner Y, Joppich C, Zahedi R, Meyer HE, Schonfisch B, Perschil I, Chacinska A, Guiard B, et al. The proteome of Saccharomyces cerevisiae mitochondria. Proc Natl Acad Sci U S A 2003; 100:13207-12; PMID:14576278; http://dx.doi.org/10.1073/pnas.2135385100
38. Avila DS, Puntel RL, Aschner M. Manganese in health and disease. Met Ions Life Sci 2013; 13:199-227; PMID:24470093; http://dx.doi.org/10.1007/978-94-007-7500-8-7
39. Salazar J, Mena N, Hunot S, Prigent A, Alvarez-Fischer D, Arredondo M, Duyckaerts C, Sazdovitch V, Zhao L, Garrick LM, et al. Divalent metal transporter 1 (DMT1) contributes to neurodegeneration in animal models of Parkinson's disease. Proc Natl Acad Sci U S A 2008; 105:18578-83; PMID:19011085; http://dx.doi.org/10.1073/pnas.0804373105
40. Tennant J, Stansfield M, Yamaji S, Srai SK, Sharp P. Effects of copper on the expression of metal transporters in human intestinal Caco-2 cells. FEBS Lett 2002; 527:239-44; PMID:12220667; http://dx.doi.org/10.1016/S0014-5793(02)03253-2
41. Arredondo M, Munoz P, Mura CV, Nunez MT. DMT1, a physiologically relevant apical Cu1+ transporter of intestinal cells. Am J Physiol Cell Physiol 2003; 284:C1525-C1530; PMID:12734107; http://dx.doi.org/10.1152/ajpcell.00480.2002
42. Jiang L, Garrick MD, Garrick LM, Zhao L, Collins JF. Divalent metal transporter 1 (Dmt1) mediates copper transport in the duodenum of iron-deficient rats and when overexpressed in iron-deprived HEK-293 cells. J Nutr 2013; 143:1927-33; PMID:24089420; http://dx.doi.org/10.3945/jn.113.181867
43. Arredondo M, Mendiburo MJ, Flores S, Singleton ST, Garrick MD. Mouse divalent metal transporter 1 is a copper transporter in HEK293 cells. Biometals 2014; 27:115-23; PMID:24327293; http://dx.doi.org/10.1007/s10534-013-9691-6
44. Cobine PA, Ojeda LD, Rigby KM, Winge DR. Yeast contain a non-proteinaceous pool of copper in the mitochondrial matrix. J Biol Chem 2004; 279:14447-55; PMID:14729672; http://dx.doi.org/10.1074/jbc.M312693200
45. Cobine PA, Pierrel F, Bestwick ML, Winge DR. Mitochondrial matrix copper complex used in metallation of cytochrome oxidase and superoxide dismutase. J Biol Chem 2006; 281:36552-9; PMID:17008312; http://dx.doi.org/10.1074/jbc.M606839200
46. Cobine PA, Pierrel F, Winge DR. Copper trafficking to the mitochondrion and assembly of copper metalloenzymes. Biochim Biophys Acta 2006; 1763:759-72; PMID:16631971; http://dx.doi.org/10.1016/j.bbamcr.2006.03.002
47. Ferguson CJ, Wareing M, Ward DT, Green R, Smith CP, Riccardi D. Cellular localization of divalent metal transporter DMT-1 in rat kidney. Am J Physiol Renal Physiol 2001; 280:F803-14; PMID:11292622
48. Kuo HC, Smith JJ, Lis A, Zhao L, Gonsiorek EA, Zhou X, Higgins DM, Roth JA, Garrick MD, Garrick LM. Computer-identified nuclear localization signal in exon 1A of the transporter DMT1 is essentially ineffective in nuclear targeting. J Neurosci Res 2004; 76:497-511; PMID:15114622; http://dx.doi.org/10.1002/jnr.20112
49. Ott M, Robertson JD, Gogvadze V, Zhivotovsky B, Orrenius S. Cytochrome c release from mitochondria proceeds by a two-step process. Proc Natl Acad Sci U S A 2002; 99:1259-63; PMID:11818574; http://dx.doi.org/10.1073/pnas.241655498
50. Wieckowski MR, Giorgi C, Lebiedzinska M, Duszynski J, Pinton P. Isolation of mitochondria-associated membranes and mitochondria from animal tissues and cells. Nat Protoc 2009; 4:1582-90; PMID:19816421; http://dx.doi.org/10.1038/nprot.2009.151
51. Wolff NA, Lee WK, Abouhamed M, Thévenod F. Role of ARF6 in internalization of metal-binding proteins, metallothionein and transferrin, and cadmium-metallothionein toxicity in kidney proximal tubule cells. Toxicol Appl Pharmacol 2008; 230:78-85; PMID:18353411; http://dx.doi.org/10.1016/j.taap.2008.02.008
52. Wolff NA, Lee WK, Thévenod F. Role of Arf1 in endosomal trafficking of protein-metal complexes and cadmium-metallothionein-1 toxicity in kidney proximal tubule cells. Toxicol Lett 2011; 203:210-18; PMID:21421027; http://dx.doi.org/10.1016/j.toxlet.2011.03.014
53. Singh H, Lu R, Rodriguez PF, Wu Y, Bopassa JC, Stefani E, Toro L. Visualization and quantification of cardiac mitochondrial protein clusters with STED microscopy. Mitochondrion 2012; 12:230-6; PMID:21982778; http://dx.doi.org/10.1016/j.mito.2011.09.004