Cellular and subcellular localization of the Nramp2 iron transporter in the intestinal brush border and regulation by dietary iron

Blood

Volumn 93, Issue 12, 1999, Pages 4406-4417

  Canonne Hergaux, F ^b   Gruenheid, S ^b   Ponka, P ^b   Gros, P ^a  

^a MCGILL UNIVERSITY   (Canada)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

HYBRID PROTEIN; IRON; TRANSFERRIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; APICAL MEMBRANE; ARTICLE; CHINESE HAMSTER; CONTROLLED STUDY; DUODENUM; GENE CONTROL; GENE LOCATION; INTESTINE BRUSH BORDER; INTESTINE CELL; IRON INTAKE; IRON RESPONSIVE ELEMENT; IRON TRANSPORT; MOUSE; NONHUMAN; PRIORITY JOURNAL; RNA SPLICING;

EID: 0033564656     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood.v93.12.4406     Document Type: Article

References (81)

1. De Silva DM, Askwith CC, Kaplan J: Molecular mechanisms of iron uptake in eukaryotes. Physiol Rev 76:31, 1996
2. Richardson DR, Ponka P: The molecular mechanisms of the metabolism and transport of iron in normal and neoplastic cells. Biochim Biophys Acta 1331:1, 1997
3. McCord JM: Effects of positive iron status at a cellular level. Nutr Rev 54:85, 1996
4. Bothwell TH: The control of iron absorption. Br J Haematol 14:453, 1968
5. Bothwell TH, Charlton RW: Absorption of iron. Annu Rev Med 21:145, 1970
6. Forth W, Rummel W: Iron absorption. Physiol Rev 53:724, 1973
7. Manis JG, Schachter D: Active transport of iron by intestine: Features of a two-step mechanism. Am J Physiol 203:73, 1962
8. Conrad ME, Parmley RT, Osterloh K: Small intestinal regulation of iron absorption in the rat. J Lab Clin Med 110:418, 1987
9. Bezkorovainy A: Biochemistry of nonheme iron in man. II. Absorption of iron. Clin Physiol Biochem 7:53, 1989
10. Raja KB, Simpson RJ, Peters TJ: Investigation of a role for reduction in ferric iron uptake by mouse duodenum. Biochem Biophys Acta 1135:141, 1992
11. Han O, Failla ML, Hill AD, Morris ER, Smith JC Jr: Reduction of Fe(III) is required for uptake of nonheme iron by Caco-2 cells. J Nutr 125:1291, 1995
12. Nathanson MH, McLaren GD, Saidel GM: A model of intestinal iron absorption and plasma iron kinetics: Optimal parameter estimates for normal dogs. Comput Biomed Res 17:55, 1984
13. Muir A, Hopfer U: Regional specificity of iron uptake by small intestinal brush-border membranes from normal and iron-deficient mice. Am J Physiol 248:G376, 1985
14. Simpson RJ, Raja KB, Peters TJ: Fe2+ uptake by mouse intestinal mucosa in vivo and by isolated intestinal brush-border membrane vesicles. Biochim Biophys Acta 860:229, 1986
15. Ikeda-Moore Y, Orimo H, Hisayasu S, Yoshino Y: Characteristics of iron binding to solubilized brush border membrane of the rat intestine. J Nutr Sci Vitaminol (Tokyo) 41:419, 1995
16. Russell ES, Nash DJ, Bernstein SE, Kent EL, McFarland EC, Matthews SM, Norwood MS: Characterization and genetic studies of microcytic anemia in house mouse. Blood 35:838, 1970
17. Edwards JA, Hoke JE: Defect of intestinal mucosal iron uptake in mice with hereditary microcytic anemia. Proc Soc Exp Biol Med 141:81, 1972
18. Farcich EA, Morgan EH: Diminished iron acquisition by cells and tissues of Belgrade laboratory rats. Am J Physiol 262:R220, 1992
19. Garrick M, Scott D, Walpole S, Finkelstein E, Whitbred J, Chopra S, Trivikram L, Mayes D, Rhodes D, Cabbagestalk K, Oklu R, Sadiq A, Mascia B, Hoke J, Garrick L: Iron supplementation moderates but does not cure the Belgrade anemia. Biometals 10:65, 1997
20. Oates PS, Morgan EH: Defective iron uptake by the duodenum of Belgrade rats fed diets of different iron contents. Am J Physiol 270:G826, 1996
21. Bannerman RM: Genetic defects of iron transport. Fed Proc 35:2281, 1976
22. Fleming MD, Trenor CC 3rd, Su MA, Foernzler D, Beier DR, Dietrich WF, Andrews NC: Microcytic anaemia mice have a mutation in Nramp2, a candidate iron transporter gene. Nat Genet 16:383, 1997
23. 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 USA 95:1148, 1998
24. Su MA, Trenor CC, Fleming JC, Fleming MD, Andrews NC: The G185R mutation disrupts function of the iron transporter Nramp2. Blood 92:2157, 1998
25. 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 388:482, 1997
26. Vidal S, Belouchi AM, Cellier M, Beatty B, Gros P: Cloning and characterization of a second human NRAMP gene on chromosome 12q13. Mamm Genome 6:224, 1995
27. Gruenheid S, Cellier M, Vidal S, Gros P: Identification and characterization of a second mouse Nramp gene. Genomics 25:514, 1995
28. Vidal SM, Malo D, Vogan K, Skamene E, Gros P: Natural resistance to infection with intracellular parasites: Isolation of a candidate for Bcg. Cell 73:469, 1993
29. Vidal S, Gros P, Skamene E: Natural resistance to infection with intracellular parasites: Molecular genetics identifies Nramp1 as the Bcg/Ity/Lsh locus. J Leukoc Biol 58:382, 1995
30. Vidal S, Tremblay ML, Govoni G, Gauthier S, Sebastiani G, Malo D, Skamene E, Olivier M, Jothy S, Gros P: 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, 1995
31. Canonne-Hergaux F, Gruenheid S, Govoni G, Gros P: The Nramp1 protein and its role in resistance to infection and macrophage function. Proc Assoc Am Phys (in press)
32. Skamene E, Schurr E, Gros P: Infection genomics: Nramp1 as a major determinant of natural resistance to intracellular infections. Annu Rev Med 49:275, 1998
33. Bellamy R, Ruwende C, Corrah T, McAdam KP, Whittle HC, Hill AV: Variations in the NRAMP1 gene and susceptibility to tuberculosis in West Africans. N Engl J Med 338:640, 1998
34. Abel L, Sanchez FO, Oberti J, Thuc NV, Hoa LV, Lap VD, Skamene E, Lagrange PH, Schurr E: Susceptibility to leprosy is linked to the human NRAMP1 gene. J Infect Dis 177:133, 1998
35. Cellier M, Belouchi A, Gros P: Resistance to intracellular infections: Comparative genomic analysis of Nramp. Trends Genet 12:201, 1996
36. Cellier M, Prive G, Belouchi A, Kwan T, Rodrigues V, Chia W, Gros P: Nramp defines a family of membrane proteins. Proc Natl Acad Sci USA 92:10089, 1995
37. 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 62:277, 1997
38. Cellier M, Shustik C, Dalton W, Rich E, Hu J, Malo D, Schurr E, Gros P: 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, 1997
39. Moffett P, Dayo M, Recce M, McCormick MK, Pelletier J: Characterization of msim, a murine homologue of the Drosophila sim transcription factor. Genomics 35:144, 1996
40. 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 24:199, 1998
41. Theil EC: The iron responsive element (IRE) family of mRNA regulators. Regulation of iron transport and uptake compared in animals, plants, and microorganisms. Met Ions Biol Syst 35:403, 1998
42. Theil EC, McKenzie RA, Sierzputowska-Gracz H: Structure and function of IREs, the noncoding mRNA sequences regulating synthesis of ferritin, transferrin receptor and (erythroid) 5-aminolevulinate synthase. Adv Exp Med Biol 356:111, 1994
43. Rouault T, Klausner R: Regulation of iron metabolism in eukaryotes, Curr Top Cell Regul 35:1, 1997
44. Henderson BR: Iron regulatory proteins 1 and 2. Bioessays 18:739, 1996
45. 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 185:717, 1997
46. Hackam DJ, Rotstein OD, Zhang W, Gruenheid S, Gros P, Grinstein S: Host resistance to intracellular infection: Mutation of natural resistance-associated macrophage protein 1 (Nramp1) impairs phagosomal acidification. J Exp Med 188:351, 1998
47. Pollard JW, Stanners CP: Characterization of cell lines showing growth control isolated from both the wild type and a leucyl-tRNA synthetase mutant of Chinese hamster ovary cells. J Cell Physiol 98:571, 1979
48. 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 272:28933, 1997
49. 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 34:4402, 1995
50. Jorgensen PL: Purification and characterization of (Na+ plus K+)-ATPase. 3. Purification from the outer medulla of mammalian kidney after selective removal of membrane components by sodium dodecylsulphate. Biochim Biophys Acta 356:36, 1974
51. 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 157:3559, 1996
52. Ausubel F, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K: Protein expression in Janssen K (ed): Current Protocols in Molecular Biology, vol 2. New York, NY, Wiley, 1996
53. Smith DE, Fisher PA: 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, 1984
54. McCuaig K, Rosenberg M, Nedellec P, Turbide C, Beauchemin N: Expression of the Bgp gene and characterization of mouse colon biliary glycoprotein isoforms. Gene 127:173, 1993
55. Rosenberg M, Nedellec P, Jothy S, Fleiszer D, Turbide C, Beauchemin N: The expression of mouse biliary glycoprotein, a carcinoembryonic antigen-related gene, is down-regulated in malignant mouse tissues. Cancer Res 53:4938, 1993
56. Daniels E, Letourneau S, Turbide C, Kuprina N, Rudinskaya T, Yazova AC, Holmes KV, Dveksler GS, Beauchemin N: Biliary glycoprotein 1 expression during embryogenesis: Correlation with events of epithelial differentiation, mesenchymal-epithelial interactions, absorption, and myogenesis. Dev Dyn 206:272, 1996
57. Turbide C, Kunath T, Daniels E, Beauchemin N: Optimal ratios of biliary glycoprotein isoforms required for inhibition of colonic tumor cell growth. Cancer Res 57:2781, 1997
58. 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 USA 93:5105, 1996
59. Gruenheid S, Canonne-Hergaux F, Gauthier S, Hackam D, Grinstein S, Gros P: The iron transport protein Nramp2 is an integral membrane glycoprotein that co-localyzes with transferrin in recycling endosomes. J Exp Med 189:831, 1999
60. McEwan GTA, Daniel H, Fett H, Burgess MN, Lucas ML: The effect of Escherichia coli STa enterotoxin and other secretagogues on mucosal surface pH of rat small intestine in vivo. Proc R Soc Lond 234:219, 1988
61. Stremmel W, Lotz G, Niederau C, Teschke R, Strohmeyer G: Iron uptake by rat duodenal microvillous membrane vesicles: Evidence for a carrier mediated transport system. Eur J Clin Invest 17:136, 1987
62. O'Riordan DK, Debnam ES, Sharp PA, Simpson RJ, Taylor EM, Srai SK: Mechanisms involved in increased iron uptake across rat duodenal brush-border membrane during hypoxia. J Physiol (Lond) 500:379, 1997
63. Pietrangelo A, Camaschella C: Molecular genetics and control of iron metabolism in hemochromatosis. Haematologica 83:456, 1998
64. Wood RJ, Han O: Recently identified molecular aspects of intestinal iron absorption. J Nutr 128:1841, 1998
65. Nunez MT, Alvarez X, Smith M, Tapia V, Glass J: Role of redox systems on Fe3+ uptake by transformed human intestinal epithelial (Caco-2) cells. Am J Physiol 267:C1582, 1994
66. Muir WA, Hopfer U, King M: Iron transport across brush-border membranes from normal and iron-deficient mouse upper small intestine. J Biol Chem 259:4896, 1984
67. Teichmann R, Stremmel W: Iron uptake by human upper small intestine microvillous membrane vesicles. Indication for a facilitated transport mechanism mediated by a membrane iron-binding protein. J Clin Invest 86:2145, 1990
68. Conrad ME, Umbreit JN, Peterson RD, Moore EG, Harper KP: Function of integrin in duodenal mucosal uptake of iron. Blood 81:517, 1993
69. Bedard YC, Pinkerton PH, Simon GT: Uptake of circulating iron by the duodenum of normal mice and mice with altered iron stores, including sex-linked anemia: High resolution radioautographic study. Lab Invest 34:611, 1976
70. Peppriell JE, Edwards JA, Bannerman RM: The kinetics of iron uptake by isolated intestinal cells from normal mice and mice with sex-linked anemia. Blood 60:635, 1982
71. Anderson GJ, Murphy TL, Cowley L, Evans BA, Halliday JW, McLaren GD: Mapping the gene for sex-linked anemia: An inherited defect of intestinal iron absorption in the mouse. Genomics 48:34, 1998
72. Owen CA Jr. Metabolism of copper 67 by the copper-deficient rat. Am J Physiol 221:1722, 1971
73. Prohaska JR: Changes in Cu,Zn-superoxide dismutase, cytochrome c oxidase, glutathione peroxidase and glutathione transferase activities in copper-deficient mice and rats. J Nutr 121:355, 1991
74. Wollenberg P, Mahlberg R, Rummel W: The valency state of absorbed iron appearing in the portal blood and ceruloplasmin substitution. Biol Met 3:1, 1990
75. Vulpe C, Askwith C, Kuo Y, Libina N, Murphy T, Anderson G, Jytschier J: Defect in a novel ceruloplasmin homologue involved in iron transport in the sla mouse. Am J Hum Genet 63:A-35, 1998 (abstr)
76. Merryweather-Clarke AT, Shearman JD, Robson KJ, Pointon JJ, Liu YT, Bomford A, Dooley J, Walker AP, Worwood M: Hemochromatosis-related mutation detection. Blood 91:2620, 1998 (letter)
77. Bomford AB, Dymock IW, Hamilton EB : Genetic haemochromatosis. Gut S111, 1991 (suppl)
78. Santos M, Clevers H, de Sousa M, Marx JJ: Adaptive response of iron absorption to anemia, increased erythropoiesis, iron deficiency, and iron loading in beta2-microglobulin knockout mice. Blood 91:3059, 1998
79. Oates PS, Morgan EH: Effects of dietary iron loading with carbonyl iron and of iron depletion on intestinal growth, morphology, and expression of transferrin receptor in the rat. Anat Rec 246:364, 1996
80. Gunshin H, Rouault T, Rogers J, Allerson C, Gollan JL, Hediger MA: Regulation of the divalent cation transporter DCT1 at the mRNA level. FASEB J 12:A820, 1998 (abstr)
81. Oates PS, Thomas C, Morgan EH: Characterization of isolated duodenal epithelial cells along a crypt-villus axis in rats fed diets with different iron content. J Gastroenterol Hepatol 12:829, 1997