DNICs and intracellular iron. Nitrogen monoxide (NO)-mediated iron release from cells is linked to NO-mediated glutathione efflux via MRP1

Radicals for Life: The Various Forms of Nitric Oxide

Volumn , Issue , 2007, Pages 97-118

  Richardson, Des R ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

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EID: 84857728271     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1016/B978-044452236-8/50004-6     Document Type: Chapter

References (110)

1. Marletta MA Nitric oxide synthase: aspects concerning structure and catalysis. Cell 1994, 78:927-930.
2. Moncada S, Palmer RMJ, Higgs EA Nitric oxide: physiology pathophysiology and pharmacology. Pharmacol. Rev. 1991, 43:109-142.
3. Hibbs JB, Taintor RR, Vavrin Z Iron depletion: possible cause of tumor cell cytotoxicity induced by activated macrophages. Biochem. Biophys. Res. Commun. 1984, 123:716-723.
4. Hibbs JB, Taintor RR, Vavrin Z, Rachlin EM Nitric oxide: a cytotoxic activated macrophage effector molecule. Biochem. Biophys. Res. Commun. 1988, 157:87-94.
5. Nathan CF, Hibbs JB Role of nitric oxide synthases in macrophage antimicrobial activity. Curr. Opin. Immunol. 1991, 3:65-70.
6. Stuehr DJ, Gross SS, Sakuma I, Levi R, Nathan CF Activated murine macrophages secrete a metabolite of arginine with the bioactivity of epithelium-derived relaxing factor and the chemical reactivity of nitric. J. Exp. Med. 1989, 169:1011-1020.
7. Richardson DR, Ponka P Effects of nitrogen monoxide on cellular iron metabolism. Nitric Oxide Synthase: Characterization and Functional Analysis 1996, 329-345. Academic Press, San Diego. M.D. Maines (Ed.).
8. Nathan C, Xie Q-W Nitric oxide synthases: roles, tolls, and controls. Cell 1994, 78:915-918.
9. Alderton WK, Cooper CE, Knowles RG Nitric oxide synthases: structure, function and inhibition. Biochem. J. 2001, 357:593-615.
10. Stamler JS, Singel DJ, Loscalzo J Biochemistry of nitric oxide and its redox-activated forms. Science 1992, 258:1898-1902.
11. 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.
12. Lepoivre M, Fieschi F, Coves J, Thelander L, Fontecave M Inactivation of ribonucleotide reductase by nitric oxide. Biochem. Biophys. Res. Commun. 1991, 179:442-448.
13. Lee M, Arosio P, Cozzi A, Chasteen ND Identification of the EPR-active iron-nitrosyl complexes in mammalian ferritins. Biochemistry 1994, 33:3679-3687.
14. Griscavage JM, Fukuto JM, Komori Y, Ignarro LJ Nitric oxide inhibits neuronal nitric oxide synthase by interacting with the heme prosthetic group. Role of tetrahydrobiopterin in modulating the inhibitory a nitric oxide. J. Biol. Chem. 1994, 269:21644-21649.
15. Ignarro LJ Heme-dependent activation of guanylate cyclase by nitric oxide: a novel signal transduction mechanism. Blood Vessels 1991, 28:67-73.
16. Khatsenko OG, Gross SS, Rifkind RR, Vane JR Nitric oxide is a mediator of the decrease in cytochrome P450-dependent metabolism caused by immunostimulants. Proc. Natl. Acad. Sci. USA 1993, 90:11147-11151.
17. Kim Y-M, Bergonia HA, Muller C, Pitt BR, Watkins WD, Lancaster JR Loss and degradation of enzyme-bound heme induced by cellular nitric oxide synthesis. J. Biol. Chem. 1995, 270:5710-5713.
18. Drapier J-C, Hibbs JB Murine cytotoxic activated macrophages inhibit aconitase in tumor cells. J. Clin. Invest. 1986, 78:790-797.
19. Drapier J-C, Hibbs JB Differentiation of murine macrophages to express nonspecific cytotoxicity for tumor cells results in L-arginine-dependent inhibition of mitochondrial iron-sul in the macrophage effector cells. J. Immunol. 1988, 140:2829-2838.
20. Drapier J-C, Hirling H, Weitzerbin J, Kaldy P, Kuhn LC Biosynthesis of nitric oxide activates iron regulatory factor in macrophages. EMBO J. 1993, 12:3643-3649.
21. Weiss G, Goossen B, Doppler W, Fuchs D, Pantopoulos K, Werner-Felmayer G, Wachter H, Hentze MW Translational regulation via iron-responsive elements by the nitric oxide/NO-synthase pathway. EMBO J. 1993, 12:3651-3657.
22. Richardson DR, Neumannova V, Nagy E, Ponka P The effect of redox-related species of nitrogen monoxide on transferrin and iron uptake and cellular proliferation of erythroleukemia (K562) cells. Blood 1995, 86:3211-3219.
23. Cairo G, Ronchi R, Recalcati S, Campanella A, Minotti G Nitric oxide and peroxynitrite activate the iron regulatory protein-1 of J774A.1 macrophages by direct dissembly of the Fe-S cluster of cytoplasmic aconitase. Biochemistry 2002, 41:7435-7442.
24. Soum E, Brazzolotto X, Goussias C, Bouton C, Moulis J-M, Mattioli TA, Drapier J-C Peroxynitrite and nitric oxide differently target the iron-sulfur cluster and amino acid residues of human iron regulatory protein 1. Biochemistry 2003, 42:7648-7654.
25. Wardrop SL, Watts RN, Richardson DR Nitrogen monoxide (NO) activates iron regulatory protein 1-RNA-binding activity by two possible mechanisms: Effect on the [4Fe-4S] cluster and iron mobilizati. Biochemistry 2000, 39:2748-2758.
26. Lancaster JR, Hibbs JB EPR demonstration of iron-nitrosyl complex formation by cytotoxic activated macrophages. Proc. Natl. Acad. Sci. USA 1990, 87:1223-1227.
27. Pellat C, Henry Y, Drapier J-C IFN-gamma-activated macrophages: Detection by electron paramagnetic resonance of complexes between L-arginine-derived nitric oxide and non-heme iron proteins. Biochem. Biophys. Res. Commun. 1990, 166:119-125.
28. Vanin AF, Bliumenfeld LA, Chetverikov AG EPR study of non-heme iron complexes in cells and tissues. Biofizika (Rus.) 1967, 12:829-841.
29. Vanin AF Endothelium-derived relaxing factor is a nitrosyl iron complex with thiol ligands. FEBS Lett. 1991, 289:1-3.
30. Woolum JC, Tiezzi E, Commoner B Electron spin resonance of iron-nitric oxide complexes with amino acids, peptides and proteins. Biochim. Biophys. Acta 1968, 160:311-320.
31. Bastian NR, Yim C-Y, Hibbs JB Samlovski WE. Induction of iron-derived EPR signals in murine cancers by nitric oxide. J. Biol. Chem. 1994, 269:5127-5131.
32. Commoner B, Woolum JC, Senturia BH, Ternberg JL The effects of 2-acetylaminofluorene and nitrite on free radicals and carcinogenesis in rat liver. Cancer Res. 1970, 30:2091-2097.
33. Drapier J-C, Pellat C, Henry Y Generation of EPR-detectable nitrosyl-iron complexes in tumor target cells cocultured with activated macrophages. J. Biol. Chem. 1991, 266:10162-10167.
34. Vanin AF, Men'shikov GB, Moroz IA, Mordvintcev PI, Serezhenkov VA, Burbaev DS The source of non-heme iron that binds nitric oxide in cultivated macrophages. Biochim. Biophys. Acta 1992, 1135:275-279.
35. Andrews NC Disorders of iron metabolism. New Engl. J. Med. 1999, 341:1986-1995.
36. Richardson DR Molecular mechanisms of iron uptake by cells and the use of iron chelators for the treatment of cancer. Curr. Med. Chem. 2005, 12:2711-2729.
37. McKie AT, Barrow D, Latunde-Dada GO, Rolfs A, Sager G, Mudaly E, Mudaly M, Richardson C, Barlow D, Bomford A, Peters TJ, Raja KB, Shirali S, Hediger MA, Farzaneh F, Simpson RJ An iron-regulated ferric reductase associated with the absorption of dietary iron. Science 2001, 291:1755-1759.
38. Gunshin H, Starr CN, Direnzo C, Fleming MD, Jin J, Greer EL, Sellers VM, Galica SM, Andrews NC Cybrd1 (duodenal cytochrome b) is not necessary for dietary iron absorption in mice. Blood 2005, 106:2879-2883.
39. 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 1997, 388:482-488.
40. Fleming MD, Trenor CC, Su MA, Foernzler D, Beier DH, Dietrich WF, Andrews NC Micro- cytic anaemia mice have a mutation in Nramp2, a candidate iron transporter gene. Nat. Genet. 1997, 16:383-386.
41. 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 1998, 95:1148-1153.
42. Shayeghi M, Latunde-Dada GO, Oakhill JS, Laftah AH, Takeuchi K, Halliday N, Khan Y, Warley A, McCann FE, Hider RC, Frazer DM, Anderson GJ, Vulpe CD, Simpson RJ, McKie AT Identification of an intestinal heme transporter. Cell 2005, 122:789-801.
43. Quigley JG, Yang Z, Worthington MT, Phillips JD, Sabo KM, Sabath DE, Berg CL, Sassa S, Wood BL, Abkowitz JL Identification of a human heme exporter that is essential for erythropoiesis. Cell 2004, 118:757-766.
44. Donovan A, Alison AYZ, Shepard J, Pratt S, Moynihan J, Paw BH, Drejer A, Barut B, Zapata A, Law TC, Brugnara C, Lux SE, Pinkus GS, Pinkus JL, Kingsley PD, Palis J, Fleming MD, Andrews NC, Zon LI Positional cloning of zebrafish ferroportin 1 identifies a conserved vertebrate iron transporter. Nature 2000, 403:776-781.
45. Abboud S, Haile DJ A novel mammalian iron-regulated protein involved in intracellular iron metabolism. J. Biol. Chem. 2000, 275:19906-19912.
46. McKie AT, Marciani P, Rolfs A, Brennan K, Wehr K, Barrow D, Miret S, Bomford A, Peters TJ, Farzaneh F Hediger MA, Hentze MW, Simpson RJ A novel duodenal iron-regulated transporter, IREG1, implicated in the basolateral transfer of iron to the circulation. Mol. Cell 2000, 5:299-309.
47. Petrak J, Vyoral D Hephaestin-a ferroxidase of cellular iron export. Int. J. Biochem. Cell Biol. 2005, 37:1173-1178.
48. Nemeth E, Tuttle MS, Powelson J, Vaughn MB, Donovan A, Ward DM, Ganz T, Kaplan J Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization. Science 2004, 306:2090-2093.
49. Richardson DR The role of ceruloplasmin and ascorbate in cellular iron release. J. Lab. Clin. Med. 1999, 134:454-465.
50. Vyoral D, Petrak J Hepcidin: a direct link between iron metabolism and immunity. Int. J. Biochem. Cell Biol. 2005, 37:1768-1773.
51. Celec P Hemojuvelin: a supposed role in iron metabolism one year after its discovery. J. Mol. Med. 2005, 83:521-525.
52. Feder JN, Gnirke A, Thomas W, Tsuchihashi Z, Ruddy DA, Basava A, Dormishian F, Domingo R, Ellis MC, Fullan A, Hinton LM, Jones NL, Kimmel BE, Kronmal GS, Lauer P, Lee VK, Loeb DB, Mapa FA, McClelland E, Meyer NC, Mintier GA, Moeller N, Moore T, Morikang E, Prass CE, Quintana L, Starnes SM, Schatzman RC, Brunke KJ, Drayna DT, Risch NJ, Bacon BR, Wolff RK A novel MHC class I-like gene is mutated in patients with hereditary haemochromatosis. Nat. Genet. 1996, 13:399-408.
53. Hentze MW, Kuhn LC Molecular control of vertebrate iron metabolism: mRNA-based regulatory circuits operated by iron, nitric oxide, and oxidative stress. Proc. Natl. Acad. Sci. USA 1996, 93:8175-8182.
54. 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 1997, 388:482-488.
55. Ponka P, Beaumont C, Richardson DR Function and regulation of transferrin and ferritin. Semin. Haematol. 1998, 35:35-54.
56. Hentze MW, Kuhn LC Molecular control of vertebrate iron metabolism: mRNA-based regulatory circuits operated by iron, nitric oxide, and oxidative stress. Proc. Natl. Acad. Sci. USA 1996, 93:8175-8182.
57. Giannetti AM, Bjorkman PJ HFE and transferrin directly compete for transferrin receptor in solution and at the cell surface. J. Biol. Chem. 2004, 279:25866-25875.
58. Ohgami RS, Campagna DR, Greer EL, Antiochos B, McDonald A, Chen J, Sharp JJ, Fujiwara Y, Barker JE, Fleming MD Identification of a ferrireductase required for efficient transferrin-dependent iron uptake in erythroid cells. Nat. Genet. 2005, 37:1264-1269.
59. 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 1998, 95:1148-1153.
60. Jacobs A Low molecular weight intracellular Fe transport compounds. Blood 1977, 50:433-439.
61. Richardson DR, Ponka P, Vyoral D Distribution of iron in reticulocytes after inhibition of heme synthesis with succinylacetate: examination of the intermediates involved in iron metabolism. Blood 1996, 87:3477-3488.
62. 59Fe autoradiography. Biochim. Biophys. Acta 1998, 1403:179-188.
63. Ponka P Tissue-specific regulation of iron metabolism and heme synthesis: Distinct control mechanisms in erythroid cells. Blood 1997, 89:1-25.
64. 2) control mammalian iron metabolism by different pathways. Mol. Cell. Biol. 1996, 16:3781-3788.
65. Watts RN, Richardson DR Nitrogen monoxide and glucose: unexpected links between energy metabolism and NO-mediated iron mobilisation from cells. J. Biol. Chem. 2001, 276:4724-4732.
66. Watts RN, Richardson DR Differential effects on cellular iron metabolism of the physiologically relevant diatomic effector molecules, NO and CO, that bind iron. Biochim. Biophys. Acta 2004, 1692:1-15.
67. Nestel FP, Greene RN, Kichian K, Ponka P, Lapp WS Activation of macrophage cytostatic effector mechanisms during acute graft-versus-host disease: release of intracellular iron and nitric oxide-mediated cytost. Blood 2000, 50:433-439.
68. Kim S, Ponka P Control of transferrin receptor expression via nitric oxide-mediated modulation of iron-regulatory protein 2. J. Biol. Chem. 1999, 274:33035-33042.
69. Kim S, Ponka P Effects of interferonγ and lipopolysaccharide on macrophage iron metabolism are mediated by nitric oxide-induced degradation of iron regulatory protein 2. J. Biol. Chem. 2000, 275:6220-6226.
70. Kim S, Wing SS, Ponka P S-nitrosylation of IRP2 regulates its stability via the ubiquitin-proteasome pathway. Mol. Cell Biol. 2004, 24:330-337.
71. Weiss G, Werner-Felmayer G, Werner ER, Gunewald K, Wachter H, Hentze MW Iron regulates nitric oxide synthase activity by controlling nuclear transcription. J. Exp. Med. 1994, 180:969-976.
72. Oliveira L, Drapier J-C Down-regulation of iron regulatory protein 1 gene expression by nitric oxide. Proc. Natl. Acad. Sci. USA 2000, 97:6550-6555.
73. Richardson DR, Neumannova V, Ponka P Nitrogen monoxide decreases iron uptake from transferrin but does not mobilize iron from prelabelled neoplastic cells. Biochim. Biophys. Acta 1995, 1266:250-260.
74. Carmichael AJ, Steel-Goodwin L, Gray B, Arroyo CM Nitric oxide interaction with lactoferrin and its production by macrophage cells studied by EPR and spin trapping. Free Radic. Res. Comm. 1993, 19:S201-S209.
75. Watts RN, Richardson DR Examination of the mechanism of action of nitrogen monoxide on iron uptake from transferrin. J. Lab. Clin. Med. 2000, 136:149-156.
76. Morgan EH, Baker E The effect of metabolic inhibitors on transferrin and iron uptake and transferrin release from reticulocytes. Biochim. Biophys. Acta 1969, 184:442-454.
77. Lipton SA, Choi YB, Pan SH, Lei SZ, Chen HSV, Sucer NJ, Loscalzo J, Singel DJ, Stamler JS A redox- based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso- compounds. Nature 1993, 364:626-631.
78. Watts RN, Richardson DR The mechanism of nitrogen monoxide (NO)-mediated iron mobilization from cells. Eur. J. Biochem. 2002, 269:3383-3392.
79. Watts RN, Ponka P, Richardson DR Effects of nitrogen monoxide and carbon monoxide on molecular and cellular iron metabolism: mirror-image effector molecules that target iron. Biochem. J. 2003, 369:429-440.
80. Richardson DR, Milnes K The potential of iron chelators of the pyridoxal isonicotinoyl hydrazone class as effective antiproliferative agents II: the mechanism of action of ligands de salicylaldehyde benzoyl hydrazone and 2-hydroxy-1-naphthaldehyde benzoyl hydrazide. Blood 1997, 89:3025-3038.
81. Joost HG, Thorens B The extended GLUT-family of sugar/polyol transport facilitators: nomenclature, sequence characteristics, and potential function of its novel members (review). Mol. Membr. Biol. 2001, 18:247-256.
82. Griffith OW, Meister A Potent and specific inhibition of glutathione synthesis by buthionine sulfoximine (S-n-butyl homocysteine sulfoximine). J. Biol. Chem. 1979, 254:7558-7560.
83. Zai A, Rudd MA, Scribner AW, Loscalzo J Cell-surface protein disulfide isomerase catalyzes transnitrosation and regulates intracellular transfer of nitric oxide. J. Clin. Invest. 1999, 103:393-399.
84. Ballatori N, Hammond CL, Cunningham JB, Krance SM, Marchan R Molecular mechanisms of reduced glutathione transport: role of the MRP/CFTR/ABCC and OATP/SLC21A families of membrane proteins. Toxicol. Appl. Pharmacol. 2005, 204:238-255.
85. Liu J, Chen H, Miller DS, Saavedra JE, Keefer LK, Johnson DR, Klaassen CD, Waalkes MP Over- expression of glutathione S-transferase II and multidrug resistance transport proteins is associated with acquired tolerance to inorganic arsenic. Mol. Pharmacol. 2001, 60:302-309.
86. Liu J, Liu Y, Powell DA, Waalkes MP, Klaassen CD Multidrug-resistance mdr1a/1b double knockout mice are more sensitive than wild type mice to acute arsenic toxicity, with higher arsenic accumulation in tissu. Toxicology 2002, 170:55-62.
87. Salerno M, Petroutsa M, Garnier-Suillerot A The MRP1-mediated effluxes of arsenic and antimony do not require arsenic-glutathione and antimony-glutathione complex formation. J. Bioenerg. Biomembr. 2002, 34:135-145.
88. Vernhet L, Allain N, Payen L, Anger J-P, Guillouzo A, Fardel O Resistance of human multidrug resistance-associated protein 1-overexpressing lung tumor cells to the anticancer drug arsenic trioxide. Biochem. Pharmacol. 2001, 61:1387-1391.
89. Watts RN, Hawkins C, Ponka P, Richardson DR Nitrogen monoxide (NO)-mediated iron release from cells is linked to NO-induced glutathione efflux via multidrug resistance-associated protein 1. Proc. Natl. Acad. Sci. USA 2006, 103:7670-7675.
90. Dallas S, Zhu X, Baruchel S, Schlichter L, Bendayan R Functional expression of the multidrug resistance protein 1 in microglia. J. Pharmacol. Exp. Therapeut. 2003, 307:282-290.
91. Schneider E, Horton JK, Yang CH, Nakagawa M, Cowan KH Multidrug resistance-associated protein gene overexpression and reduced drug sensitivity of topoisomerase II in a human breast carcinoma MCF7 cell line select etoposide resistance. Cancer Res. 1994, 54:152-158.
92. Benderra Z, Trussardi A, Morjani H, Villa AM, Doglia SM, Manfait M Regulation of cellular glutathione modulates nuclear accumulation of daunorubicin in human MCF7 cells overexpressing multidrug resistance associated protein. Eur. J. Cancer 2000, 36:428-434.
93. de Maria F, Pedersen JZ, Caccuri AM, Antonini G, Turella P, Stella L, lo Bello M, Federici G, Ricci G The specific interaction of dinitrosyl-diglutathionyl-iron complex, a natural NO-carrier, with the glutathione transferase superfamily. J. Biol. Chem. 2003, 278:42283-42293.
94. Mulsch A, Mordvintcev P, Vanin AF, Busse R The potent vasodilating and guanylyl cyclase activating dinitrosyl-iron(II) complex is stored in a protein-bound form in vascular tissue and is released by th. FEBS Lett. 1991, 294:252-256.
95. Turella P, Pedersen JZ, Caccuri AM, de Maria F, Mastroberardino P, lo Bello M, Federici G, Ricci G Glutathione transferase superfamily behaves like storage proteins for dinitrosyl-diglutathionyl-iron complex in heterogeneous systems. J. Biol. Chem. 2003, 278:42294-42299.
96. Ueno T, Suzuki Y, Fujii S, Vanin AF, Yoshimaru T In vivo nitric oxide transfer of a physiological NO carrier, dinitrosyl dithiolato iron complex, to target complex. Biochem. Pharmacol. 2002, 63:485-493.
97. Ueno T, Suzuki Y, Fujii S, Vanin AF, Yoshimura T In vivo distribution and behaviour of paramagnetic dinitrosyl dithiolato iron complex in the abdomen of mouse. Free Radic. Res. 1999, 31:525-534.
98. 2. Proc. Natl. Acad. Sci. USA 2001, 98:355-360.
99. Boese M, Mordvintcev PI, Vanin AF, Busse R, Mulsch A S-nitrosation of serum albumin by dinitrosyl- iron complex. J. Biol. Chem. 1995, 270:29244-29249.
100. Vanin AF, Malenkova IV, Serenzhenkov VA Iron catalyses both decomposition and synthesis of S-nitrosothiols: optical and electron paramagnetic resonance studies. Nitric Oxide 1997, 1:191-203.
101. He Y-Y, Huang JL, Ramirez DC, Chignell CF Role of reduced glutathione efflux in apoptosis of immortalised human keratinocytes induced by UVA. J. Biol. Chem. 2003, 278:8058-8064.
102. Richardson DR, Tran EH, Ponka P The potential of iron chelators of the pyridoxal isonicotinoyl hydrazone class as effective antiproliferative agents. Blood 1995, 86:4295-4306.
103. Drapier J-C, Hibbs JB Aconitases: a class of metalloproteins highly sensitive to nitric oxide synthesis. Methods 1996, 269:26-36.
104. Ding H, Demple B Glutathione-mediated destabilization in vitro of [2Fe-2S] centers in the SoxR regulatory protein. Proc. Natl. Acad. Sci. USA 1996, 93:9449-9453.
105. Rogers PA, Ding H.L Cysteine-mediated destabilization of dinitrosyl iron complexes in proteins. J. Biol. Chem. 2001, 276:30980-30986.
106. Leier I, Jedlitschky G, Buchholz U, Cole SPC, Deeley RG, Keppler D The MRP gene encodes an ATP- dependent export pump for leukotriene C4 and structurally related conjugates. J. Biol. Chem. 1994, 269:27807-27810.
107. Leslie EM, Haimeur A, Waalkes MP Arsenic transport by the human multidrug resistance protein 1 (MRP1/ABCC1). Evidence that tri-glutathione conjugate is required. J. Biol. Chem. 2004, 279:32700-32708.
108. Cullen KV, Davey RA, Davey MW Verapamil-stimulated glutathione transport by the multidrug resistance-associated protein (MRP1) in leukaemia cells. Biochem. Pharmacol. 2001, 62:417-424.
109. Trompier D, Chang XB, Barattin R, du Moulinet D'Hardemare A, Di Pietro A, Baubichon-Cortay H Verapamil and its derivative trigger apoptosis through glutathione extrusion by multidrug resistance protein MRP1. Cancer Res. 2004, 64:4950-4956.
110. Flens MJ, Zaman GJ, van der Valk P, Izquierdo MA, Schroeijers AB, Scheffer GL, van der Groep P, de Haas M, Meijer CJ, Scheper RJ Tissue distribution of the multidrug resistance protein. Am. J. Pathol. 1996, 148:1237-1247.