Iron transport by Nramp2/DMT1: pH regulation of transport by 2 histidines in transmembrane domain 6

Blood

Volumn 101, Issue 9, 2003, Pages 3699-3707

  Lam Yuk Tseung, Steven ^b   Govoni, Gregory ^b   Forbes, John ^b   Gros, Philippe ^a  

^a MCGILL UNIVERSITY   (Canada)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

HISTIDINE; MEMBRANE PROTEIN; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 2; CARRIER PROTEIN; CATION TRANSPORT PROTEIN; DIVALENT CATION; HYBRID PROTEIN; IRON; IRON BINDING PROTEIN; ISOPROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; SMF1 PROTEIN, S CEREVISIAE; SMF2 PROTEIN, S CEREVISIAE; SOLUTE CARRIER FAMILY 11 (PROTON COUPLED DIVALENT METAL ION TRANSPORTERS), MEMBER 2; SOLUTE CARRIER FAMILY 11- (PROTON-COUPLED DIVALENT METAL ION TRANSPORTERS), MEMBER 2;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; CATION TRANSPORT; CELL FUNCTION; CONTROLLED STUDY; DISEASE PREDISPOSITION; DISEASE SEVERITY; FEMALE; GENETIC IDENTIFICATION; HOMEOSTASIS; ION TRANSPORT; MAMMAL CELL; MEMBRANE TRANSPORT; METAL BINDING; MICROCYTIC ANEMIA; MOUSE; MUTATION; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN DOMAIN; RAT; REGULATORY MECHANISM; YEAST; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANEMIA; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; CHO CELL; CRICETULUS; GENETIC COMPLEMENTATION; GENETICS; HAMSTER; METABOLISM; MISSENSE MUTATION; MOLECULAR GENETICS; MOUSE MUTANT; PHYSIOLOGY; POINT MUTATION; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE; RAT STRAIN; SACCHAROMYCES CEREVISIAE; SITE DIRECTED MUTAGENESIS; STRUCTURE ACTIVITY RELATION;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANEMIA; ANIMALS; CARRIER PROTEINS; CATION TRANSPORT PROTEINS; CATIONS, DIVALENT; CHO CELLS; CRICETINAE; CRICETULUS; GENETIC COMPLEMENTATION TEST; HISTIDINE; HYDROGEN-ION CONCENTRATION; ION TRANSPORT; IRON; IRON-BINDING PROTEINS; MEMBRANE PROTEINS; MICE; MICE, MUTANT STRAINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION, MISSENSE; POINT MUTATION; PROTEIN CONFORMATION; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; RATS; RATS, MUTANT STRAINS; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 0037528706     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood-2002-07-2108     Document Type: Article

References (49)

1. Gunshin H, Mackenzie B, Berger UV, et al. Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature. 1997;388:482-488.
2. Fleming MD, Trenor CC III, Su MA, et al. Microcytic anaemia mice have a mutation in Nramp2, a candidate iron transporter gene. Nat Genet. 1997;16:383-386.
3. 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;95:1148-1153.
4. Gruenheid S, Canonne-Hergaux F, Gauthier S, Hackam DJ, Grinstein S, Gros P. The iron transport protein NRAMP2 is an integral membrane glycoprotein that colocalizes with transferrin in recycling endosomes. J Exp Med. 1999;189:831-841.
5. Tabuchi M, Yoshimori T, Yamaguchi K, Yoshida T, Kishi F. Human NRAMP2/DMT1, which mediates iron transport across endosomal membranes, is localized to late endosomes and lysosomes in HEp-2 cells. J Biol Chem. 2000;275:22220-22228.
6. Cellier M, Prive G, Belouchi A, et al. Nramp defines a family of membrane proteins. Proc Natl Acad Sci U S A. 1995;92:10089-10093.
7. Lee PL, Gelbart T, West C, Halloran C, Beutler E. The human Nramp2 gene: characterization of the gene structure, alternative splicing, promoter region and polymorphisms. Blood Cells Mol Dis. 1998;24:199-215.
8. Fleming MD, Andrews NC. Mammalian iron transport: an unexpected link between metal homeostasis and host defense. J Lab Clin Med. 1998;132:464-468.
9. Canonne-Hergaux F, Gruenheid S, Ponka P, Gros P. Cellular and subcellular localization of the Nramp2 iron transporter in the intestinal brush border and regulation by dietary iron. Blood. 1999;93:4406-4417.
10. Canonne-Hergaux F, Zhang AS, Ponka P, Gros P. Characterization of the iron transporter DMT1 (NRAMP2/DCT1) in red blood cells of normal and anemic mk/mk mice. Blood. 2001;98:3823-3830.
11. Tchernitchko D, Bourgeois M, Martin ME, Beaumont C. Expression of the two mRNA isoforms of the iron transporter Nrmap2/DMT1 in mice and function of the iron responsive element. Biochem J. 2002;363:449-455.
12. Canonne-Hergaux F, Gros P. Expression of the iron transporter DMT1 in kidney from normal and anemic mk mice. Kidney Int. 2002;62:147-156.
13. Picard V, Govoni G, Jabado N, Gros P. Nramp 2 (DCT1/DMT1) expressed at the plasma membrane transports iron and other divalent cations into a calcein-accessible cytoplasmic pool. J Biol Chem. 2000;275:35738-35745.
14. Tandy S, Williams M, Leggett A, et al. Nramp2 expression is associated with pH-dependent iron uptake across the apical membrane of human intestinal Caco-2 cells. J Biol Chem. 2000;275:1023-1029.
15. Edwards JA, Hoke JE. Defect of intestinal mucosal iron uptake in mice with hereditary microcytic anemia. Proc Soc Exp Biol Med. 1972;141:81-84.
16. Su MA, Trenor CC, Fleming JC, Fleming MD, Andrews NC. The G185R mutation disrupts function of the iron transporter Nramp2. Blood. 1998;92:2157-2163.
17. Canonne-Hergaux F, Fleming MD, Levy JE, et al. The Nramp2/DMT1 iron transporter is induced in the duodenum of microcytic anemia mk mice but is not properly targeted to the intestinal brush border. Blood. 2000;96:3964-3970.
18. Andrews NC. Iron metabolism: iron deficiency and iron overload. Annu Rev Genomics Hum Genet. 2000;1:75-98.
19. Wessling-Resnick M. Iron transport. Annu Rev Nutr. 2000;20:129-151.
20. Vidal SM, Malo D, Vogan K, Skamene E, Gros P. Natural resistance to infection with intracellular parasites: isolation of a candidate for Bcg. Cell. 1993;73:469-485.
21. Govoni G, Gauthier S, Billia F, Iscove NN, Gros P. Cell-specific and inducible Nramp1 gene expression in mouse macrophages in vitro and in vivo. J Leukoc Biol. 1997;62:277-286.
22. Cellier M, Shustik C, Dalton W, et al. Expression of the human NRAMP1 gene in professional primary phagocytes: studies in blood cells and in HL-60 promyelocytic leukemia. J Leukoc Biol. 1997;61:96-105.
23. Gruenheid S, Pinner E, Desjardins M, Gros P. Natural resistance to infection with intracellular pathogens: the Nramp1 protein is recruited to the membrane of the phagosome. J Exp Med. 1997;185:717-730.
24. Jabado N, Jankowski A, Dougaparsad S, Picard V, Grinstein S, Gros P. Natural resistance to intracellular infections: natural resistance-associated macrophage protein 1 (Nramp1) functions as a pH-dependent manganese transporter at the phagosomal membrane. J Exp Med. 2000;192:1237-1248.
25. Vidal S, Tremblay ML, Govoni G, et al. The Ity/Lsh/Bcg locus: natural resistance to infection with intracellular parasites is abrogated by disruption of the Nramp1 gene. J Exp Med. 1995;182:655-666.
26. Forbes JR, Gros P. Divalent-metal transport by NRAMP proteins at the interface of host-pathogen interactions. Trends Microbiol. 2001;9:397-403.
27. Gruenheid S, Gros P. Genetic susceptibility to intracellular infections: Nramp1, macrophage function and divalent cations transport. Curr Opin Microbiol. 2000;3:43-48.
28. Agranoff D, Monahan IM, Mangan JA, Butcher PD, Krishna S. Mycobacterium tuberculosis expresses a novel pH-dependent divalent cation transporter belonging to the Nramp family. J Exp Med. 1999;190:717-724.
29. Belouchi A, Cellier M, Kwan T, Saini HS, Leroux G, Gros P. The macrophage-specific membrane protein Nramp controlling natural resistance to infections in mice has homologues expressed in the root system of plants. Plant Mol Biol. 1995;29:1181-1196.
30. Rodrigues V, Cheah PY, Ray K, Chia W. malvolio, the Drosophila homologue of mouse NRAMP-1 (Bcg), is expressed in macrophages and in the nervous system and is required for normal taste behaviour. EMBO J. 1995;14:3007-3020.
31. Supek F, Supekova L, Nelson H, Nelson N. A yeast manganese transporter related to the macrophage protein involved in conferring resistance to mycobacteria. Proc Natl Acad Sci U S A. 1996;93:5105-5110.
32. Pinner E, Gruenheid S, Raymond M, Gros P. Functional complementation of the yeast divalent cation transporter family SMF by NRAMP2, a member of the mammalian natural resistance-associated macrophage protein family. J Biol Chem. 1997;272:28933-28938.
33. Orgad S, Nelson H, Segal D, Nelson N. Metal ions suppress the abnormal taste behavior of the Drosophila mutant malvolio. J Exp Biol. 1998;201(pt 1):115-120.
34. Urbatsch IL, Julien M, Carrier I, Rousseau ME, Cayrol R, Gros P. Mutational analysis of conserved carboxylate residues in the nucleotide binding sites of P-glycoprotein. Biochemistry. 2000;39:14138-14149.
35. Sherman F, Fink GR, Hicks JB. Methods of Yeast Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory; 1982.
36. Kwan T, Gros P. Mutational analysis of the P-glycoprotein first intracellular loop and flanking transmembrane domains. Biochemistry. 1998;37:3337-3350.
37. Kast C, Canfield V, Levenson R, Gros P. Membrane topology of P-glycoprotein as determined by epitope insertion: transmembrane organization of the N-terminal domain of mdr3. Biochemistry. 1995;34:4402-4411.
38. Nakagama H, Heinrich G, Pelletier J, Housman DE. Sequence and structural requirements for high-affinity DNA binding by the WT1 gene product. Mol Cell Biol. 1995;15:1489-1498.
39. Eng BH, Guerinot ML, Eide D, Saier MH Jr. Sequence analyses and phylogenetic characterization of the ZIP family of metal ion transport proteins. J Membr Biol. 1998;166:1-7.
40. Voss J, Hubbell WL, Kaback HR. Distance determination in proteins using designed metal ion binding sites and site-directed spin labeling: application to the lactose permease of Escherichia coli. Proc Natl Acad Sci U S A. 1995;92:12300-12303.
41. Omichinski JG, Trainor C, Evans T, Gronenborn AM, Clore GM, Felsenfeld G. A small single-"finger" peptide from the erythroid transcription factor GATA-1 binds specifically to DNA as a zinc or iron complex. Proc Natl Acad Sci U S A. 1993;90:1676-1680.
42. Ghazaleh FA, Omburo GA, Colman RW. Evidence for the presence of essential histidine and cysteine residues in platelet cGMP-inhibited phosphodiesterase. Biochem J. 1996;317(pt 2):495-501.
43. Worthington MT, Amann BT, Nathans D, Berg JM. Metal binding properties and secondary structure of the zinc-binding domain of Nup475. Proc Natl Acad Sci U S A. 1996;93:13754-13759.
44. Worthington MT, Browne L, Battle EH, Luo RQ. Functional properties of transfected human DMT1 iron transporter. Am J Physiol Gastrointest Liver Physiol. 2000;279:G1265-G1273.
45. Vidal SM, Pinner E, Lepage P, Gauthier S, Gros P. Natural resistance to intracellular infections: Nramp1 encodes a membrane phosphoglycoprotein absent in macrophages from susceptible (Nramp1 D169) mouse strains. J Immunol. 1996;157:3559-3568.
46. Voss J, Salwinski L, Kaback HR, Hubbell WL. A method for distance determination in proteins using a designed metal ion binding site and site-directed spin labeling: evaluation with T4 lysozyme. Proc Natl Acad Sci U S A. 1995;92:12295-12299.
47. Kaback HR. Lac permease of Escherichia coli: on the path of the proton. Philos Trans R Soc Lond B Biol Sci. 1990;326:425-436.
48. Muller-Berger S, Karbach D, Kang D, et al. Roles of histidine 752 and glutamate 699 in the pH dependence of mouse band 3 protein-mediated anion transport. Biochemistry. 1995;34:9325-9332.
49. Muller-Berger S, Karbach D, Konig J, et al. Inhibition of mouse erythroid band 3-mediated chloride transport by site-directed mutagenesis of histidine residues and its reversal by second site mutation of Lys 558, the locus of covalent H2DIDS binding. Biochemistry. 1995;34:9315-9324.