The iron transport protein NRAMP2 is an integral membrane glycoprotein that colocalizes with transferrin in recycling endosomes

Journal of Experimental Medicine

Volumn 189, Issue 5, 1999, Pages 831-841

  Gruenheid, Samantha ^a   Canonne Hergaux, François ^a   Gauthier, Susan ^a   Hackam, David J ^b   Grinstein, Sergio ^b   Gros, Philippe ^a  

^a MCGILL UNIVERSITY   (Canada)

^b HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

Anemia; Infection; Iron; Macrophage; Transport

Indexed keywords

CARRIER PROTEIN; MEMBRANE PROTEIN; TRANSFERRIN;

ANIMAL CELL; ANTIGENICITY; ARTICLE; CELL COMPARTMENTALIZATION; ENDOSOME; GENE LOCUS; GLYCOSYLATION; IRON DEFICIENCY ANEMIA; IRON METABOLISM; IRON TRANSPORT; MEMBRANE BINDING; MEMBRANE TRANSPORT; MOUSE; MULTIGENE FAMILY; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; RECYCLING;

ANIMALS; ANTIBODY SPECIFICITY; BIOLOGICAL TRANSPORT; CARRIER PROTEINS; CATION TRANSPORT PROTEINS; CELL COMPARTMENTATION; CELL LINE; ENDOCYTOSIS; ENDOSOMES; FLUORESCENT ANTIBODY TECHNIQUE; IRON; IRON-BINDING PROTEINS; MACROPHAGES; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MICE; MODELS, BIOLOGICAL; MONOCYTES; TRANSFERRIN;

EID: 0033103978     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.189.5.831     Document Type: Article

References (43)

1. Malo, D., K. Vogan, S. Vidal, J. Hu, M. Cellier, E. Schurr, A. Fuks, N. Bumstead, K. Morgan, and P. Gros. 1994. Haplotype mapping and sequence analysis of the mouse Nramp gene predict susceptibility to infection with intracellular parasites. Genomics. 23:51-61.
2. Vidal, S., M.L. Tremblay, G. Govoni, S. Gauthier, G. Sebastiani, D. Malo, E. Skamene, M. Olivier, S. Jothy, and P. Gros. 1995. The Ity/Lsh/Bcg locus: natural resistance to infection with intracellular parasites is abrogated by disruption of the Nramp1 gene J. Exp. Med. 182:655-666.
3. Abel, L., F.O. Sanchez, J. Oberti, N.V. Thuc, L.V. Hoa, V.D. Lap, E. Skamene, P.H. Lagrange, and E. Schurr. 1998. Susceptibility to leprosy is linked to the human NRAMP1 gene. J. Infect. Dis. 177:133-145.
4. Bellamy, R., C. Ruwende, T. Corrah, K.P. McAdam, H.C. Whittle, and A.V. Hill. 1998. Variations in the NRAMP1 gene and susceptibility to tuberculosis in West Africans. N. Engl. J. Med. 338:640-644.
5. Vidal, S.M., D. Malo, K. Vogan, E. Skamene, and P. Gros. 1993. Natural resistance to infection with intracellular parasites: isolation of a candidate for Bcg. Cell. 73:469-485.
6. Govoni, G., S. Gauthier, F. Billia, N.N. Iscove, and P. Gros. 1997. Cell-specific and inducible Nramp1 gene expression in mouse macrophages in vitro and in vivo. J. Leukoc. Biol. 62: 277-286.
7. Cellier, M., C. Shustik, W. Dalton, E. Rich, J. Hu, D. Malo, E. Schurr, and P. Gros. 1997. Expression of the human NRAMP1 gene in professional primary phagocytes: studies in blood cells and in HL-60 promyelocytic leukemia. J. Leukoc. Biol. 61:96-105.
8. Vidal, S.M., E. Pinner, P. Lepage, S. Gauthier, and P. Gros. 1996. Natural resistance to intracellular infections: Nramp1 encodes a membrane phosphoglycoprotein absent in macrophages from susceptible (Nramp1 D169) mouse strains. J. Immunol. 157:3559-3568.
9. Gruenheid, S., E. Pinner, M. Desjardins, and P. Gros. 1997. Natural resistance to infection with intracellular pathogens: the Nramp1 protein is recruited to the membrane of the phagosome. J. Exp. Med. 185:717-730.
10. Gruenheid, S., M. Cellier, S. Vidal, and P. Gros. 1995. Identification and characterization of a second mouse Nramp gene. Genomics. 25:514-525.
11. Moffett, P., M. Dayo, M. Reece, M.K. McCormick, and J. Pelletier. 1996. Characterization of msim, a murine homologue of the Drosophila sim transcription factor. Genomics. 35:144-155.
12. Gunshin, H., B. Mackenzie, U.V. Berger, Y. Gunshin, M.F. Romero, W.F. Boron, S. Nussberger, J.L. Gollan, and M.A. Hediger. 1997. Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature. 388:482-488.
13. Fleming, M.D., C.C. Trenor, III, M.A. Su, D. Foernzler, D.R. Beier, W.F. Dietrich, and N.C. Andrews. 1997. Microcytic anaemia mice have a mutation in Nramp2, a candidate iron transporter gene. Nat. Genet. 16:383-386.
14. Fleming, M.D., M.A. Romano, M.A. Su, L.M. Garrick, M.D. Garrick, and N.C. Andrews. 1998. Nramp2 is mutated in the anemic Belgrade (b) rat: evidence of a role for Nramp2 in endosomal iron transport. Proc. Natl. Acad. Sci. USA. 95: 1148-1153.
15. Russell, E.S., D.J. Nash, S.E. Bernstein, E.L. Kent, E.C. McFarland, S.M. Matthews, and M.S. Norwood. 1970. Characterization and genetic studies of microcytic anemia in house mouse. Blood. 35:838-850.
16. Edwards, J.A., and J.E. Hoke. 1972. Defect of intestinal mucosal iron uptake in mice with hereditary microcytic anemia. Proc. Soc. Exp. Biol. Med. 141:81-84.
17. Farcich, E.A., and E.H. Morgan. 1992. Diminished iron acquisition by cells and tissues of Belgrade laboratory rats. Am. J. Physiol. 262:R220-224.
18. Cellier, M., G. Prive, A. Belouchi, T. Kwan, V. Rodrigues, W. Chia, and P. Gros. 1995. Nramp defines a family of membrane proteins. Proc. Natl. Acad. Sci. USA. 92:10089-10093.
19. Ausubel, F., R. Brent, R.E. Kingston, D.D. Moore, J.G. Seidman, J.A. Smith, and K. Struhl. 1996. Current Protocols in Molecular Biology. Vol. 2. K. Janssen, editor. John Wiley and Sons Inc., New York. 16.7.1-16.7.5.
20. Smith, D.E., and P.A. Fisher. 1984. Identification, developmental regulation, and response to heat shock of two antigenically related forms of a major nuclear envelope protein in Drosophila embryos: application of an improved method for affinity purification of antibodies using polypeptides immobilized on nitrocellulose blots. J. Cell. Biol. 99:20-28.
21. Chow, L.M., D. Davidson, M. Fournel, P. Gosselin, S. Lemieux, M.S. Lyu, C.A. Kozak, L.A. Matis, and A. Veillette. 1994. Two distinct protein isoforms are encoded by ntk, a csk-related tyrosine protein kinase gene. Oncogene. 9:3437-3448.
22. Pollard, J.W., and C.P. Stanners. 1979. Characterization of cell lines showing growth control isolated from both the wild type and a leucyl-tRNA synthetase mutant of Chinese ham-ster ovary cells. J. Cell. Physiol. 98:571-585.
23. Pinner, E., S. Gruenheid, M. Raymond, and P. Gros. 1997. 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. 272:28933-28938.
24. Canfield, V.A., and R. Levenson. 1993. Transmembrane organization of the Na,K-ATPase determined by epitope addition. Biochemistry. 32:13782-13786 (erratum published 33: 3142).
25. Kaufman, R.J., M.V. Davies, V.K. Pathak, and J.W.B. Hershey. 1989. The phosphorylation site of eucaryotic initiation factor 2 alters translational efficiency of specific mRNAs. Mol. Cell. Biol. 9:946-958.
26. Kast, C., V. Canfield, R. Levenson, and P. Gros. 1995. Membrane topology of P-Glycoprotein as determined by epitope insertion: transmembrane organization of the N-terminal domain of mdr3. Biochemistry. 34:4402-4411.
27. Devault, A., and P. Gros. 1990. Two members of the mouse mdr gene family confer multidrug resistance with overlap-ping but distinct drug specificities. Mol. Cell. Biol. 10:1652-1663.
28. Chirgwin, J.M., A.E. Przybyla, R.J. MacDonald, and W.J. Rutter. 1979. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 18:5294-5299.
29. Desjardins, M., L.A. Huber, R.G. Parton and G. Griffiths. 1994. Biogenesis of phagolysosomes proceeds through a sequential series of interactions with the endocytic apparatus. J. Cell. Biol. 124:677-688.
30. Evan, G.I., G.K. Lewis, G. Ramsay, and J.M. Bishop. 1985. Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol. Cell. Biol. 5:3610-3616.
31. Supek, F., L. Supekova, H. Nelson, and N. Nelson. 1996. A yeast manganese transporter related to the macrophage protein involved in conferring resistance to mycobacteria. Proc. Natl. Acad. Sci. USA. 93:5105-5110.
32. Edwards, J.A., and J.E. Hoke. 1975. Red cell iron uptake in hereditary microcytic anemia. Blood. 46:381-388.
33. Edwards, J.A., L.M. Garrick, and J.E. Hoke. 1978. Defective iron uptake and globin synthesis by erythroid cells in the anemia of the Belgrade laboratory rat. Blood. 51:347-357.
34. Edwards, J.A., A.L. Sullivan, and J.E. Hoke. 1980. Defective delivery of iron to the developing red cell of the Belgrade laboratory rat. Blood. 55:645-648.
35. Farcich, E.A., and E.H. Morgan. 1992. Uptake of transferrin-bound and nontransferrin-bound iron by reticulocytes from the Belgrade laboratory rat: comparison with Wistar rat transferrin and reticulocytes. Am. J. Hematol. 39:9-14.
36. Garrick, M.D., K. Gniecko, Y. Liu, D.S. Cohan, and L.M. Garrick. 1993. Transferrin and the transferrin cycle in Belgrade rat reticulocytes. J. Biol. Chem. 268:14867-14874.
37. Bannerman, R.M. 1976. Genetic defects of iron transport. Fed. Proc. 35, 11:2281-2285.
38. Ponka, P., C. Beaumont, and D.R. Richardson. 1998. Function and regulation of transferrin and ferritin. Semin. Hematol. 35:35-54.
39. Dautry-Varsat, A., A. Ciechanover, and H.F. Lodish. 1983. pH and the recycling of transferrin during receptor-mediated endocytosis. Proc. Natl. Acad. Sci. USA. 80:2258-2262.
40. Teter, K., G. Chandy, B. Quinones, K. Pereyra, T. Machen, and H.P.H. Moore. 1998. Cellubrevin-targeted fluorescence uncovers heterogeneity in the recycling endosomes. J. Biol. Chem. 273:19625-19633.
41. Hackam, D.J., O.D. Rotstein, W. Zhang, S. Gruenheid, P. Gros, and S. Grinstein. 1998. Host resistance to intracellular infection: mutation of natural resistance-associated macrophage protein 1 (Nramp1) impairs phagosomal acidification. J. Exp. Med. 188:351-364.
42. Sipe, D.M., A. Jesurum, and R.F. Murphy. 1991. Absence of Na+,K(+)-ATPase regulation of endosomal acidification in K562 erythroleukemia cells. Analysis via inhibition of transferrin recycling by low temperatures. J. Biol. Chem. 266: 3469-3474.
43. Yurko, M.A., and S. Gluck. 1987. Production and characterization of a monoclonal antibody to vacuolar H+ATPase of renal epithelia. J. Biol. Chem. 262:15770-15779.