Intracellular kinetics of iron in reticulocytes: Evidence for endosome involvement in iron targeting to mitochondria

Blood

Volumn 105, Issue 1, 2005, Pages 368-375

  Zhang, An Sheng ^b   Sheftel, Alex D ^b   Ponka, Prem ^a  

^a MCGILL UNIVERSITY   (Canada)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

BAFILOMYCIN A1; BIPYRIDINE; CALMODULIN INHIBITOR; FERROCHELATASE; HEME; IRON; IRON 59; MYOSIN LIGHT CHAIN KINASE INHIBITOR; N (6 AMINOHEXYL) 5 CHLORO 1 NAPHTHALENESULFONAMIDE; PORPHOBILINOGEN SYNTHASE; PROTOPORPHYRIN; SALICYLALDEHYDE ISONICOTINOYLHYDRAZONE; SUCCINYLACETONE; UNCLASSIFIED DRUG; WORTMANNIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENDOSOME; HEME SYNTHESIS; HEMOGLOBIN SYNTHESIS; IRON KINETICS; IRON TRANSPORT; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; RETICULOCYTE;

EID: 11144226961     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood-2004-06-2226     Document Type: Article

References (73)

1. Ponka P. Tissue-specific regulation of iron metabolism and heme synthesis: distinct control mechanisms in erythroid cells. Blood. 1997;89:1-25.
2. Richardson DR, Ponka P. The molecular mechanisms of the metabolism and transport of iron in normal and neoplastic cells. Biochim Biophys Acta. 1997;1331:1-40.
3. Hentze MW, Muckenthaler MU, Andrews NC. Balancing acts: molecular control of mammalian iron metabolism. Cell. 2004;117:285-297.
4. Andrews NC. Disorders of iron metabolism. N Engl J Med. 1999;341:1986-1995.
5. Gunshin H, Mackenzie B, Berger UV, et al. Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature. 1997;388:482-488.
6. 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.
7. Fleming MD, Romano MA, Su MA, et al. 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.
8. Gruenheid S, Canonne-Hergaux F, Gauthier S, et al. The iron transport protein NRAMP2 is an integral membrane glycoprotein that colocalizes with transferrin in recycling endosomes. J Exp Med. 1999;189:831-841.
9. Cellier M, Prive G, Belouchi A, et al. Nramp defines a family of membrane proteins. Proc Natl Acad Sci USA. 1995;92:10089-10093.
10. Jacobs A. Low molecular weight intracellular iron transport compounds. Blood. 1977;50:433-439.
11. Epsztejn S, Kakhlon O, Glickstein H, Breuer W, Cabantchik I. Fluorescence analysis of the labile iron pool of mammalian cells. Anal Biochem. 1997;248:31-40.
12. Borova J, Ponka P, Neuwirt J. Study of intracellular iron distribution in rabbit reticulocytes with normal and inhibited heme synthesis. Biochim Biophys Acta. 1973;320:143-156.
13. Ponka P, Wilczynska A, Schulman HM. Iron utilization in rabbit reticulocytes: a study using succinylacetone as an inhibitor or heme synthesis. Biochim Biophys Acta. 1982;720:96-105.
14. Morgan EH. Chelator-mediated iron efflux from reticulocytes. Biochim Biophys Acta. 1983;733:39-50.
15. Garrick LM, Gniecko K, Liu Y, et al. Iron distribution in Belgrade rat reticulocytes after inhibition of heme synthesis with succinylacetone. Blood. 1993;81:3414-3421.
16. Richardson DR, Ponka P, Vyoral D. Distribution of iron in reticulocytes after inhibition of heme synthesis with succinylacetone: examination of the intermediates involved in iron metabolism. Blood. 1996;87:3477-3488.
17. May A, Fitzsimons E. Sideroblastic anaemia. Baillieres Clin Haematol. 1994;7:851-879.
18. Adams ML, Ostapiuk I, Grasso JA. The effects of inhibition of heme synthesis on the intracellular localization of iron in rat reticulocytes. Biochim Biophys Acta. 1989;1012:243-253.
19. Ponka P, Borova J, Neuwirt J, Fuchs O, Necas E. A study of intracellular iron metabolism using pyridoxal isonicotinoyl hydrazone and other synthetic chelating agents. Biochim Biophys Acta. 1979;586:278-297.
20. Martinez-Medellin J, Schulman HM. The kinetics of iron and transferrin incorporation into rabbit erythroid cells and the nature of stromal-bound iron. Biochim Biophys Acta. 1972;264:272-274.
21. Teale FW. Cleavage of the haem-protein link by acid methylethylketone. Biochim Biophys Acta. 1959;35:543.
22. Huang AR, Ponka P. A study of the mechanism of action of pyridoxal isonicotinoyl hydrazone at the cellular level using reticulocytes loaded with non-heme 59Fe. Biochim Biophys Acta. 1983;757:306-315.
23. Ponka P, Neuwirt J. The use of reticulocytes with high non-haem iron pool for studies of regulation of haem synthesis. Br J Haematol. 1970;19:593-604.
24. Finbow ME, Harrison MA. The vacuolar H +-ATPase: a universal proton pump of eukaryotes. Biochem J. 1997;324(Pt 3):697-712.
25. Nunez MT, Gaete V, Watkins JA, Glass J. Mobilization of iron from endocytic vesicles. The effects of acidification and reduction. J Biol Chem. 1990;265:6688-6692.
26. Hermes-Lima M, Santos NC, Van J, et al. EPR spin trapping and 2-deoxyribose degradation studies of the effect of pyridoxal isonicotinoyl hydrazone (PIH) on *OH formation by the Fenton reaction. Biochim Biophys Acta. 1999;1426:475-482.
27. Mukherjee S, Ghosh RN, Maxfield FR. Endocytosis. Physiol Rev. 1997;77:759-803.
28. Durrbach A, Louvard D, Coudrier E. Actin filaments facilitate two steps of endocytosis. J Cell Sci. 1996;109(Pt 2):457-465.
29. Subtil A, Dautry-Varsat A. Microtubule depolymerization inhibits clathrin coated-pit internalization ir non-adherent cell lines while interleukin 2 endocytosis is not affected. J Cell Sci. 1997;110(Pt 19):2441-2447.
30. Thatte HS, Bridges KR, Golan DE. Microtubule inhibitors differentially affect transitional movement, cell surface expression, and endocytosis of transferrin receptors in K562 cells. J Cell Physiol. 1994;160:345-357.
31. Goodson HV, Valetti C, Kreis TE. Motors and membrane traffic. Curr Opin Cell Biol. 1997;9:18-28.
32. Riezman H, Woodman PG, van Meer G, Marsh M. Molecular mechanisms of endocytosis. Cell. 1997;91:731-738.
33. Maxfield FR, McGraw TE. Endocytic recycling. Nat Rev Mol Cell Biol. 2004;5:121-132.
34. Jin M, Snider MD. Role of microtubules in transferrin receptor transport from the cell surface to endosomes and the Golgi complex. J Biol Chem. 1993;268:18390-18397.
35. Hamm-Alvarez SF, Sonee M, Loran-Goss K, Shen WC. Paclitaxel and nocodazole differentially alter endocytosis in cultured cells. Pharm Res. 1996;13:1647-1656.
36. Drmota T, Gould GW, Milligan G. Real time visualization of agonist-mediated redistribution and internalization of a green fluorescent protein-tagged form of the thyrotropin-releasing hormone receptor. J Biol Chem. 1998;273:24000-24008.
37. Novikoff PM, Cammer M, Tao L, et al. Three-dimensional organization of rat hepatocyte cytoskeleton: relation to the asialoglycoprotein endocytosis pathway. J Cell Sci. 1996;109(Pt 1):21-32.
38. Li R, Riordan JF, Hu G. Nuclear translocation of human angiogenin in cultured human umbilical artery endothelial cells is microtubule and lysosome independent. Biochem Biophys Res Commun. 1997;238:305-312.
39. Rapp S, Saffrich R, Anton M, et al. Microtubule-based peroxisome movement. J Cell Sci. 1996;109(Pt 4):837-849.
40. Welch MD, Mallavarapu A, Rosenblatt J, Mitchison TJ. Actin dynamics in vivo. Curr Opin Cell Biol. 1997;9:54-61.
41. Cooper JA. Effects of cytochalasin and phalloidin on actin. J Cell Biol. 1987;105:1473-1478.
42. Fowler VM. Regulation of actin filament length in erythrocytes and striated muscle. Curr Opin Cell Biol. 1996;8:86-96.
43. Nakanishi S, Kakita S, Takahashi I, et al. Wortmannin, a microbial product inhibitor of myosin light chain kinase. J Biol Chem. 1992;267:2157-2163.
44. Mochida S, Kobayashi H, Matsuda Y, et al. Myosin II is involved in transmitter release at synapses formed between rat sympathetic neurons in culture. Neuron. 1994;13:1131-1142.
45. Samizo K, Okagaki T, Kohama K. Inhibitory effect of phosphorylated myosin light chain kinase on the ATP-dependent actin-myosin interaction. Biochem Biophys Res Commun. 1999;261:95-99.
46. Ryan TA. Inhibitors of myosin light chain kinase block synaptic vesicle pool mobilization during action potential firing. J Neurosci. 1999;19:1317-1323.
47. Poulsen NC, Spector I, Spurck TP, Schultz TF, Wetherbee R. Diatom gliding is the result of an actin-myosin motility system. Cell Motil Cytoskeleton. 1999;44:23-33.
48. Soeno Y, Shimada Y, Obinata T. BDM (2,3-butanedione monoxime), an inhibitor of myosin-actin interaction, suppresses myofibrillogenesis in skeletal muscle cells in culture. Cell Tissue Res. 1999;295:307-316.
49. Bourguignon LY, Gunja-Smith Z, Iida N, et al. CD44v(3,8-10) is involved in cytoskeleton-mediated tumor cell migration and matrix metalloproteinase (MMP-9) association in metastatic breast cancer cells. J Cell Physiol. 1998;176:206-215.
50. Ito M, Tanabe F, Sato A, et al. Possible involvement of microfilaments in protein kinase C translocation. Biochem Biophys Res Commun. 1989;160:1344-1349.
51. Ponka P, Richardson DR. Can ferritin provide iron for hemoglobin synthesis? Blood. 1997;89:2611-2613.
52. Picard V, Renaudie F, Porcher C, et al. Overexpression of the ferritin H subunit in cultured erythroid cells changes the intracellular iron distribution. Blood. 1996;87:2057-2064.
53. Martinez-Medellin J. Studies on Transferrin and Intracellular Metabolism of Iron in Rabbit Erythroid Cells [dissertation]. University of California, San Diego; 1972.
54. Ponka P, Neuwirt J, Borova J, Fuchs O. Control of iron delivery to haemoglobin in erythroid cells. Ciba Found Symp. 1976;167-200.
55. Isobe K, Isobe Y, Sakurami T. Cytochemical demonstration of transferrin in the mitochondria of immature human erythroid cells. Acta Haematol. 1981;65:2-9.
56. Morgan EH, Iacopetta BJ. Vinblastine but not other microtubule inhibitors block transferrin endocytosis and iron uptake by reticulocytes. Clin Exp Pharmacol Physiol. 1987;14:119-126.
57. Fowler VM, Davis JQ, Bennett V. Human erythrocyte myosin: identification and purification. J Cell Biol. 1985;100:47-55.
58. Wong AJ, Kiehart DP, Pollard TD. Myosin from human erythrocytes. J Biol Chem. 1985;260:46-49.
59. Colin FC, Schrier SL. Myosin content and distribution in human neonatal erythrocytes are different from adult erythrocytes. Blood. 1991;78:3052-3055.
60. DePina AS, Langford GM. Vesicle transport: the role of actin filaments and myosin motors. Microsc Res Tech. 1999;47:93-106.
61. Ui M, Okada T, Hazeki K, Hazeki O. Wortmannin as a unique probe for an intracellular signalling protein, phosphoinositide 3-kinase. Trends Biochem Sci. 1995;20:303-307.
62. Spiro DJ, Boll W, Kirchhausen T, Wessling-Resnick M. Wortmannin alters the transferrin receptor endocytic pathway in vivo and in vitro. Mol Biol Cell. 1996;7:355-367.
63. Grasso JA, Bruno M, Yates AA, Wei LT, Epstein PM. Calmodulin dependence of transferrin receptor recycling in rat reticulocytes. Biochem J. 1990;266:261-272.
64. Konijn AM, Glickstein H, Vaisman B, et al. The cellular labile iron pool and intracellular ferritin in K562 cells. Blood. 1999;94:2128-2134.
65. Kakhlon O, Cabantchik ZI. The labile iron pool: characterization, measurement, and participation in cellular processes(1). Free Radic Biol Med. 2002;33:1037-1046.
66. Lange H, Kispal G, Lill R. Mechanism of iron transport to the site of heme synthesis inside yeast mitochondria. J Biol Chem. 1999;274:18989-18996.
67. Desjardins M, Huber LA, Parton RG, Griffiths G. Biogenesis of phagolysosomes proceeds through a sequential series of interactions with the endocytic apparatus. J Cell Biol. 1994;124:677-688.
68. Mannella CA, Buttle K, Rath BK, Marko M. Electron microscopic tomography of rat-liver mitochondria and their interaction with the endoplasmic reticulum. Biofactors. 1998;8:225-228.
69. Ma Y, Specian RD, Yeh KY, et al. The transcytosis of divalent metal transporter 1 and apo-transferrin during iron uptake in intestinal epithelium. Am J Physiol Gastrointest Liver Physiol. 2002;283: G965-G974.
70. Scott MD, Eaton JW. Thalassaemic erythrocytes: cellular suicide arising from iron and glutathione-dependent oxidation reactions? Br J Haematol. 1995;91:811-819.
71. Vyoral D, Petrak J. Iron transport in K562 cells: a kinetic study using native gel electrophoresis and 59Fe autoradiography. Biochim Biophys Acta. 1998;1403:179-188.
72. Penman S. Rethinking cell structure. Proc Natl Acad Sci U S A. 1995;92:5251-5257.
73. Rae TD, Schmidt PJ, Pufahl RA, Culotta VC, O'Halloran TV. Undetectable intracellular free copper: the requirement of a copper chaperone for superoxide dismutase. Science. 1999;284:805-808.