Detection of intracellular iron by its regulatory effect

American Journal of Physiology - Cell Physiology

Volumn 287, Issue 6 56-6, 2004, Pages

  Li, Jau Yi ^a   Ram, Gita ^a   Gast, Katherine ^a   Chen, Xia ^a   Barasch, Kimberly ^a   Mori, Kiyoshi ^a   Schmidt Ott, Kai ^a   Wang, Jianjun ^b   Kuo, Hung Chieh ^c   Savage Dunn, Cathy ^b   Garrick, Michael D ^c   Barasch, Jonathan ^a  

^a Columbia University ^*  (United States)

^b CITY UNIVERSITY OF NEW YORK   (United States)

^c UNIVERSITY AT BUFFALO   (United States)

Author keywords

HFE; Iron regulatory proteins; Iron responsive element; Labile iron pool; Neutrophil gelatinase associated lipocalin; Siderophore; Transferrin

Indexed keywords

APOTRANSFERRIN; FLUORESCENT DYE; IRON REGULATORY FACTOR; LIPOCALIN; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; SIDEROPHORE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; FLUORESCENCE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; IRON CHELATION; IRON RESPONSIVE ELEMENT; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; TRANSLATION REGULATION;

ACUTE-PHASE PROTEINS; BACTERIAL PROTEINS; CELL LINE, TRANSFORMED; CYTOPLASM; FLOW CYTOMETRY; FLUORESCENT DYES; GENE EXPRESSION; GENES, REPORTER; HUMANS; IRON; IRON REGULATORY PROTEIN 1; IRON REGULATORY PROTEIN 2; LUMINESCENT PROTEINS; ONCOGENE PROTEINS; PROTEIN BIOSYNTHESIS; PROTO-ONCOGENE PROTEINS; RECEPTORS, TRANSFERRIN; SIGNAL TRANSDUCTION;

EID: 8644290972     PISSN: 03636143     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpcell.00260.2004     Document Type: Article

References (90)

1. Alcantara O, Denham CA, Phillips JL, and Boldt DH. Transcriptional regulation of transferrin receptor expression by cultured lymphoblastoid T cells treated with phorbol diesters. J Immunol 142: 1719-1726, 1989.
2. Aziz N and Munro HN. Iron regulates ferritin mRNA translation through a segment of its 5′ untranslated region. Proc Natl Acad Sci USA 84: 8478-8482, 1987.
3. Barasch J. Iron, lipocalins and induction of nephrons (Abstract). Scientific Committee of the American Society of Hematology, 2003 (http://www.abstracts2view.com/hem/sessionindex.php?p = 4).
4. Barasch J and Li JY. Measurement of intracellular iron (Abstract). J Am Soc Nephrol 13: 504A, 2002.
5. Barasch J, Mori K, and Li JY. Novel reporter for the regulatory pool of iron (Abstract). J Am Soc Nephrol 14: 329A, 2003.
6. Bourdon E, Kang DK, Ghosh MC, Drake SK, Wey J, Levine RL, and Rouault TA. The role of endogenous heme synthesis and degradation domain cysteines in cellular iron-dependent degradation of IRP2. Blood Cells Mol Dis 31: 247-255, 2003.
7. Bouton C, Oliveira L, and Drapier JC. Converse modulation of IRP1 and IRP2 by immunological stimuli in murine RAW 264.7 macrophages. J Biol Chem 273: 9403-9408, 1998.
8. Brekelmans P, van Soest P, Voerman J, Platenburg PP, Leenen PJ, and van Ewijk W. Transferrin receptor expression as a marker of immature cycling thymocytes in the mouse. Cell Immunol 159: 331-339, 1994.
9. Brenner S. The genetics of Caenorhabditis elegans. Genetics 77: 71-94, 1974.
10. Busfield SJ, Tilbrook PA, Callus BA, Spadaccini A, Kuhn L, and Klinken SP. Complex regulation of transferrin receptors during erythropoietin-induced differentiation of J2E erythroid cells - elevated transcription and mRNA stabilisation produce only a modest rise in protein content. Eur J Biochem 249: 77-84, 1997.
11. Chan RY, Seiser C, Schulman HM, Kuhn LC, and Ponka P. Regulation of transferrin receptor mRNA expression. Distinct regulatory features in erythroid cells. Eur J Biochem 220: 683-692, 1994.
12. Chaudhary J, Cupp AS, and Skinner MK. Role of basic-helix-loop-helix transcription factors in Sertoli cell differentiation: identification of an Å-box response element in the transferrin promoter. Endocrinology 138: 667-675, 1997.
13. Chen X, Wang LQ, Huang Y, Qiu P, Murgolo NJ, Greene JR, Wu CH, and Jiang Y. IRE_FINDER-computational search of iron response element in human and mouse UTRs. Sheng Wu Hua Xue Yu Sheng Wu Wu Li Xue Bao (Shanghai) 34: 743-747, 2002.
14. Cherry SR, Biniszkiewicz D, van Parijs L, Baltimore D, and Jaenisch R. Retroviral expression in embryonic stem cells and hematopoietic stem cells. Mol Cell Biol 20: 7419-7426, 2002.
15. Chitambar CR and Wereley JP. Resistance to the antitumor agent gallium nitrate in human leukemic cells is associated with decreased gallium/iron uptake, increased activity of iron regulatory protein-1, and decreased ferritin production. J Biol Chem 272: 12151-12157, 1997.
16. Constable A, Quick S, Gray NK, and Hentze MW. Modulation of the RNA-binding activity of a regulatory protein by iron in vitro: switching between enzymatic and genetic function? Proc Natl Acad Sci USA 89: 4554-4558, 1992.
17. Drapier JC, Hirling H, Wietzerbin J, Kaldy P, and Kuhn LC. Biosynthesis of nitric oxide activates iron regulatory factor in macrophages. EMBO J 12: 3643-3649, 1993.
18. Eisenstein R and Blemings KP. Iron regulatory proteins, iron responsive elements and iron homeostasis. J Nutr 128: 2295-2298, 1998.
19. Ekblom P, Thesleff I, Saxen L, Miettinen A, and Timpl R. Transferrin as a fetal growth factor: acquisition of responsiveness related to embryonic induction. Proc Natl Acad Sci USA 80: 2651-2655, 1983.
20. Epsztejn S, Kakhlon O, Glickstein H, Breuer W, and Cabantchik ZI. Fluorescence analysis of the labile iron pool of mammalian cells. Anal Biochem 248: 31-40, 1997.
21. Esposito BP, Epsztejn S, Breuer W, and Cabantchik ZI. A review of fluorescence methods for assessing labile iron in cells and biological fluids. Anal Biochem 304: 1-18, 2002.
22. Feder JN, Penny DM, Irrinki A, Lee VK, Lebron JA, Watson N, Tsuchihashi Z, Sigal E, Bjorkman PJ, and Schatzman RC. The hemochromatosis gene product complexes with the transferrin receptor and lowers its affinity for ligand binding. Proc Natl Acad Sci USA 95: 1472-1477, 1998.
23. Festa M, Ricciardelli G, Mele G, Pietropaolo C, Ruffo A, and Colonna A. Overexpression of H ferritin and up-regulation of iron regulatory protein genes during differentiation of 3T3-L1 pre-adipocytes. J Biol Chem 275: 36708-36712, 2000.
24. Fleming S and Jones DB. Immunocytochemical evidence for transferrin-dependent proliferation during renal tubulogenesis. J Anat 153: 191-201, 1987.
25. Flower DR, North AC, and Sansom CE. The lipocalin protein family: structural and sequence overview. Biochim Biophys Acta 1482: 9-24, 2000.
26. Garate MA and Nunez MT. Overexpression of the ferritin iron-responsive element decreases the labile iron pool and abolishes the regulation of iron absorption by intestinal epithelial (Caco-2) cells. J Biol Chem 275: 1651-1655, 2000.
27. Gazitt Y, Reddy SV, Alcantara O, Yang J, and Boldt DH. A new molecular role for iron in regulation of cell cycling and differentiation of HL-60 human leukemia cells: iron is required for transcription of p21(WAF1/CIP1) in cells induced by phorbol myristate acetate. J Cell Physiol 187: 124-135, 2001.
28. Goetz DH, Holmes MA, Borregaard N, Bluhm ME, Raymond KN, and Strong RK. The neutrophil lipocalin NGAL is a bacteriostatic agent that interferes with siderophore-mediated iron acquisition. Mol Cell 10: 1033-1043, 2002.
29. Goetze B, Grunewald B, Kiebler MA, and Macchi P. Coupling the iron-responsive element to GFP - an inducible system to study translation in a single living cell. Sci STKE 2003: PL12, 2003.
30. Gourley BL, Parker SB, Jones BJ, Zumbrennen KB, and Leibold EA. Cytosolic aconitase and ferritin are regulated by iron in Caenorhabditis elegans. J Biol Chem 278: 3227-3234, 2003.
31. Gross CN, Irrinki A, Feder JN, and Enns CA. Co-trafficking of HFE, a nonclassical major histocompatibility complex class I protein, with the transferrin receptor implies a role in intracellular iron regulation. J Biol Chem 273: 22068-22074, 1998.
32. Haile DJ. Regulation of genes of iron metabolism by the iron-response proteins. Am J Med Sci 318: 230-240, 1999.
33. Hanson ES and Leibold EA. Regulation of iron regulatory protein 1 during hypoxia and hypoxia/reoxygenation. J Biol Chem 273: 7588-7593, 1998.
34. Hanson ES, Rawlins ML, and Leibold EA. Oxygen and iron regulation of iron regulatory protein 2. J Biol Chem 278: 40337-40342, 2003.
35. Henderson BR and Kuhn LC. Differential modulation of the RNA-binding proteins IRP-1 and IRP-2 in response to iron. IRP-2 inactivation requires translation of another protein. J Biol Chem 270: 20509-20515, 1995.
36. Henderson RJ, Patton SM, and Connor JR. Development of a novel method for the measurement of cellular iron levels and iron-regulated protein expression. BioIron 2003. 16th International Conference of the International BioIron Society, NIH. Bethesda, MD, May 4-9, 2003 (poster abst 195).
37. Hentze MW, Caughman SW, Rouault TA, Barriocanal G, Dancis A, Harford JB, and Klausner RD. Identification of the iron-responsive element for the translational regulation of human ferritin mRNA. Science 238: 1570-1573, 1987.
38. Hirsch S and Miskimins W. Mitogen induction of nuclear factors that interact with a delayed responsive region of the transferrin receptor gene promoter. Cell Growth Differ 6: 719-726, 1995.
39. Iwai K, Klausner RD, and Rouault TA. Requirements for iron-regulated degradation of the RNA binding protein, iron regulatory protein 2. EMBO J 14: 5350-5357, 1995.
40. Kanayasu-Toyoda T, Yamaguchi T, Uchida E, and Hayakawa T. Commitment of neutrophilic differentiation and proliferation of HL-60 cells coincides with expression of transferrin receptor. Effect of granulocyte colony stimulating factor on differentiation and proliferation. J Biol Chem 274: 25471-25480, 1999.
41. Kim S and Ponka P. Control of transferrin receptor expression via nitric oxide-mediated modulation of iron-regulatory protein 2. J Biol Chem 274: 33035-33042, 1999.
42. Kim S and Ponka P. Effects of interferon-γ and lipopolysaccharide on macrophage iron metabolism are mediated by nitric oxide-induced degradation of iron regulatory protein 2. J Biol Chem 275: 6220-6226, 2000.
43. Kim S and Ponka P. Nitrogen monoxide-mediated control of ferritin synthesis: implications for macrophage iron homeostasis. Proc Natl Acad Sci USA 99: 12214-12219, 2002.
44. Kim S, Wing SS, and Ponka P. S-nitrosylation of IRP2 regulates its stability via the ubiquitin-proteasome pathway. Mol Cell Biol 24: 330-337, 2004.
45. Klausner RD and Rouault TA. The molecular basis of iron metabolism. In: The Harvey Lectures. New York: Wiley-Liss, 1998, vol. 92, p. 99-112.
46. LaVaute T, Smith S, Cooperman S, Iwai K, Land W, Meyron-Holtz E, Drake SK, Miller G, Abu-Asab M, Tsokos M, Switzer R, Grinberg A, Love P, Tresser N, and Rouault TA. Targeted deletion of the gene encoding iron regulatory protein-2 causes misregulation of iron metabolism and neurodegenerative disease in mice. Nat Genet 27: 209-214, 2001.
47. Leibold EA, Gahring LC, and Rogers SW. Immunolocalization of iron regulatory protein expression in the murine central nervous system. Histochem Cell Biol 115: 195-203, 2001.
48. Leibold EA and Munro HN. Cytoplasmic protein binds in vitro to a highly conserved sequence in the 5′ untranslated region of ferritin heavy-and light-subunit mRNAs. Proc Natl Acad Sci USA 85: 2171-2175, 1988.
49. Levy JE, Jin O, Fujiwara Y, Kuo F, and Andrews NC. Transferrin receptor is necessary for development of erythrocytes and the nervous system. Nat Genet 21: 396-399, 1999.
50. Lok CN and Ponka P. Identification of a hypoxia response element in the transferrin receptor gene. J Biol Chem 274: 24147-25152, 1999.
51. Lok CN, Chan KF, and Loh TT. Transcriptional regulation of transferrin receptor expression during phorbol-ester-induced HL-60 cell differentiation. Evidence for a negative regulatory role of the phorbol-ester-responsive element-like sequence. Eur J Biochem 236: 614-619, 1996.
52. Macchi P, Hemraj I, Goetze B, Grunewald B, Mallardo M, and Kiebler MA. A GFP-based system to uncouple mRNA transport from translation in a single living neuron. Mol Biol Cell 14: 1570-1582, 2003.
53. Marziali G, Perrotti E, Ilari R, Lulli V, Coccia EM, Moret R, Kuhn LC, Testa U, and Battistini A. Role of Ets-1 in transcriptional regulation of transferrin receptor and erythroid differentiation. Oncogene 21: 7933-7944, 2002.
54. McGraw TE, Greenfield L, and Maxfield FR. Functional expression of the human transferrin receptor cDNA in Chinese hamster ovary cells deficient in endogenous transferrin receptor. J Cell Biol 105: 207-214, 1987.
55. Mello CC, Kramer JM, Stinchcomb DT, and Ambros V. Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J 10: 3959-3970, 1991.
56. Meyron-Holtz EG, Ghosh MC, Iwai K, LaVaute T, Brazzolotto X, Berger UV, Land W, Ollivierre-Wilson H, Grinberg A, Love P, and Rouault TA. Genetic ablations of iron regulatory proteins 1 and 2 reveal why iron regulatory protein 2 dominates iron homeostasis. EMBO J 23: 386-395, 2004.
57. Miller JC and Miller JN. Statistics for Analytical Chemistry. New York: Wiley, 1984, chapts. 2 and 3, p. 46-48.
58. Naviaux RK, Costanzi E, Haas M, and Verma IM. The pCL vector system: rapid production of helper-free, high-titer, recombinant retroviruses. J Virol 70: 5701-5705, 1996.
59. Ned RM, Swat W, and Andrews NC. Transferrin receptor 1 is differentially required in lymphocyte development. Blood 102: 3711-3718, 2003.
60. Oshiro S, Nozawa K, Hori M, Zhang C, Hashimoto Y, Kitajima S, and Kawamura K. Modulation of iron regulatory protein-1 by various metals. Biochem Biophys Res Commun 290: 213-218, 2002.
61. 2) control mammalian iron metabolism by different pathways. Mol Cell Biol 16: 3781-3788, 1996.
62. Ponka P. Tissue-specific regulation of iron metabolism and heme synthesis: distinct control mechanisms in erythroid cells. Blood 89: 1-25, 1997.
63. Ponka P and Lok C. The transferrin receptor: role in health and disease. Int J Biochem Cell Biol 31: 1111-1137, 1999.
64. Ponka P, Schulman HM, and Woodworth RC. Iron Transport and Storage. Boston, MA: CRC, 1990, chapt. 10.
65. Richardson DR, Neumannova V, Nagy E, and Ponka P. The effect of redox-related species of nitrogen monoxide on transferrin and iron uptake and cellular proliferation of erythroleukemia (K562) cells. Blood 86: 3211-3219, 1995.
66. Riedel HD, Muckenthaler MU, Gehrke SG, Mohr I, Brennan K, Hermann T, Fitscher BA, Hentze MW, and Stremmel W. HFE downregulates iron uptake from transferrin and induces iron-regulatory protein activity in stably transfected cells. Blood 94: 3915-3921, 1999.
67. Rogers JT. Ferritin translation by interleukin-1 and interleukin-6: the role of sequences upstream of the start codons of the heavy and light subunit genes. Blood 87: 2525-2537, 1996.
68. Roskams AJ and Connor JR. Iron, transferrin, and ferritin in the rat brain during development and aging. J Neurochem 63: 709-716, 1994.
69. Rouault TA, Hentze MW, Caughman SW, Harford JB, and Klausner RD. Binding of a cytosolic protein to the iron-responsive element of human ferritin messenger RNA. Science 241: 1207-1210, 1988.
70. Rouault TA and Klausner R. Regulation of iron metabolism in eukaryotes. Curr Top Cell Regul 35: 1-19, 1997.
71. Roy CN, Blemings KP, Deck KM, Davies PS, Anderson EL, Eisenstein RS, and Enns CA. Increased IRP-1 and IRP-2 RNA binding activity accompanies a reduction of the labile iron pool in HFE-expressing cells. J Cell Physiol. 190: 218-226, 2002.
72. Roy CN, Penny DM, Feder JN, and Enns CA. The hereditary hemochromatosis protein, HFE, specifically regulates transferrin-mediated iron uptake in HeLa cells. J Biol Chem 274: 9022-9028, 1999.
73. Seiser C, Teixeira S, and Kuhn LC. Interleukin-2-dependent transcriptional and post-transcriptional regulation of transferrin receptor mRNA. J Biol Chem 268: 13074-13080, 1993.
74. Siddappa AJ, Rao RB, Wobken JD, Leibold EA, Connor JR, and Georgieff MK. Developmental changes in the expression of iron regulatory proteins and iron transport proteins in the perinatal rat brain. J Neurosci Res 68: 761-775, 2002.
75. Soum E and Drapier JC. Nitric oxide and peroxynitrite promote complete disruption of the [4Fe-4S] cluster of recombinant human iron regulatory protein 1. J Biol Inorg Chem 8: 226-232, 2003.
76. Sposi N, Cianetti L, Tritarelli E, Pelosi E, Militi S, Barberi T, Gabbianelli M, Saulle E, Kuhn L, Peschle C, and Testa U. Mechanisms of differential transferrin receptor expression in normal hematopoiesis. Eur J Biochem 267: 6762-6774, 2000.
77. Srinivas S, Watanabe T, Lin CS, William CM, Tanabe Y, Jessell TM, and Costantini F. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol 1: 4, 2001.
78. Sturrock A, Alexander J, Lamb J, Craven C, and Kaplan J. Characterization of a transferrin-independent uptake system for iron in HeLa cells. J Biol Chem 265: 3139-3145, 1990.
79. Tacchini L, Bianchi L, Bernelli ZA, and Cairo G. Transferrin receptor induction by hypoxia. HIF-1-mediated transcriptional activation and cell-specific post-transcriptionai regulation. J Biol Chem 274: 24142-24146, 1999.
80. Testa U, Kuhn L, Petrini M, Quaranta MT, Pelosi E, and Peschle C. Differential regulation of iron regulatory element-binding protein(s) in cell extracts of activated lymphocytes versus monocytes-macrophages. J Biol Chem 266: 13925-13930, 1991.
81. Waheed A, Grubb JH, Zhou XY, Tomatsu S, Fleming R, Costaldi M, Britton RS, Bacon BS, and Sly WS. Regulation of transferrin-mediated iron uptake by HFE, the protein defective in hereditary hemochromatosis. Proc Natl Acad Sci USA 99: 3117-3122, 2002.
82. Wang J, Chen GH, Muckenthaler M, Galy B, Hentze MW, and Pantopoulos K. Iron-mediated degradation of IRP2, an unexpected pathway involving a 2-oxoglutarate-dependent oxygenase activity. Mol Cell Biol 24: 954-965, 2004.
83. Wang J, Tokarz R, and Savage-Dunn C. The expression of TGFβ signal transducers in the hypodermis regulates body size in C. elegans. Development 129: 4989-4998, 2002.
84. Weiss G, Bogdan G, and Hentze MW. Pathways for the regulation of macrophage iron metabolism by the anti-inflammatory cytokines IL-4 and IL-13. J Immunol 158: 420-425, 1997.
85. Weiss G, Goossen B, Doppler W, Fuchs D, Pantopoulos K, Werner-Felmayer G, Wachter H, and Hentze MW. Translational regulation via iron-responsive elements by the nitric oxide/NO-synthase pathway. EMBO J 12: 3651-3657, 1993.
86. Yamaguchi-Iwai Y, Ueta R, Fukunaka A, and Sasaki R. Subcellular localization of Aftl transcription factor responds to iron status in Saccharomyces cerevisiae. J Biol Chem 277: 18914-18918, 2002.
87. Yang J, Goetz D, Li JY, Wang W, Mori K, Setlik D, Du T, Erdjument-Bromage H, Tempst P, Strong R, and Barasch J. An iron delivery pathway mediated by a lipocalin. Mol Cell 10: 1045-1056, 2002.
88. Yang J, Mori K, Li JY, and Barasch J. Iron, lipocalin, and kidney epithelia. Am J Physiol Renal Physiol 285: F9-F18, 2003.
89. Ye Z and Connor J. Screening of transcriptionally regulated genes following iron chelation in human astrocytoma cells. Biochem Biophys Res Commun 264: 709-713, 1999.
90. Zakin MM, Baron B, and Guillou F. Regulation of the tissue-specific expression of transferrin gene. Dev Neurosci 24: 222-226, 2002.