A nitric oxide storage and transport system that protects activated macrophages from endogenous nitric oxide cytotoxicity

Journal of Biological Chemistry

Volumn 291, Issue 53, 2016, Pages 27042-27061

  Lok, Hiu Chuen ^a   Sahni, Sumit ^a   Jansson, Patric J ^a   Kovacevic, Zaklina ^a   Hawkins, Clare L ^b   Richardson, Des R ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b HEART RESEARCH INSTITUTE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; CHEMICAL ACTIVATION; CYTOLOGY; DISEASES; IRON; IRON COMPOUNDS; MACROPHAGES; NITRIC OXIDE; TUMORS;

ACTIVATED MACROPHAGES; CYTOTOXIC DRUGS; GLUTATHIONE S-TRANSFERASE P1; MACROPHAGE ACTIVATION; MACROPHAGE CELLS; MULTIDRUG RESISTANCE; NUCLEAR FACTOR ERYTHROID 2-RELATED FACTOR 2; TRANSPORT SYSTEMS;

CYTOTOXICITY;

DINITROSYL DITHIOL IRON COMPLEX; FERROPORTIN 1; GAMMA INTERFERON; GLUTATHIONE TRANSFERASE P1; INDUCIBLE NITRIC OXIDE SYNTHASE; IRON 59; IRON COMPLEX; LIPOPOLYSACCHARIDE; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 1; NITRIC OXIDE; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; VERLUKAST; BRONCHODILATING AGENT; GLUTATHIONE; GSTP1 PROTEIN, MOUSE; GSTP2 PROTEIN, MOUSE; IRON; MULTIDRUG RESISTANCE PROTEIN; MULTIDRUG RESISTANCE-ASSOCIATED PROTEIN 1; PROPIONIC ACID DERIVATIVE; PROTECTIVE AGENT; QUINOLINE DERIVATIVE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CANCER CELL; CANCER CELL LINE; CANCER INHIBITION; CELL PROTECTION; CELL SURVIVAL; CELLS BY BODY ANATOMY; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOTOXICITY; DRUG PROTEIN BINDING; EMBRYO; GENE SILENCING; GSTP1 GENE; IRON TRANSPORT; J774 CELL LINE; MACROPHAGE ACTIVATION; MOUSE; MRP1 GENE; NONHUMAN; NRF2 GENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAW 264.7 CELL LINE; TUMOR CELL; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CULTURE; DRUG EFFECTS; GENETICS; KNOCKOUT MOUSE; MACROPHAGE; METABOLISM; PATHOLOGY; PHYSIOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; BRONCHODILATOR AGENTS; CELLS, CULTURED; GLUTATHIONE; GLUTATHIONE S-TRANSFERASE PI; IRON ISOTOPES; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; MICE, KNOCKOUT; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; NITRIC OXIDE; PROPIONATES; PROTECTIVE AGENTS; QUINOLINES; RNA, SMALL INTERFERING;

EID: 85007610433     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.763714     Document Type: Article

References (86)

1. Wink, D. A., and Mitchell, J. B. (1998) Chemical biology of nitric oxide: Insights into regulatory, cytotoxic, and cytoprotective mechanisms of nitric oxide. Free Radic. Biol. Med. 25, 434-456
2. Lancaster, J. R., Jr. (1997) A tutorial on the diffusibility and reactivity of free nitric oxide. Nitric Oxide 1, 18-30
3. Hibbs, J. B., Jr., Taintor, R. R., Vavrin, Z., and Rachlin, E. M. (1988) Nitric oxide: a cytotoxic activated macrophage effector molecule. Biochem. Biophys. Res. Commun. 157, 87-94
4. Lancaster, J. R., Jr., and Hibbs, J. B., Jr. (1990) EPR demonstration of iron-nitrosyl complex formation by cytotoxic activated macrophages. Proc. Natl. Acad. Sci. U.S.A. 87, 1223-1227
5. de Oliveira, G. A., Cheng, R., Ridnour, L. A., Basudhar, D., Somasundaram, V., McVicar, D. W., Monteiro, H. P., and Wink, D. A. (2016) Inducible nitric oxide synthase (NOS2) in the carcinogenesis of gastrointestinal cancers. Antioxid. Redox Signal. 10.1089/ars.2016.6850
6. Ignarro, L. J., Buga, G. M., Wood, K. S., Byrns, R. E., and Chaudhuri, G. (1987) Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc. Natl. Acad. Sci. U.S.A. 84, 9265-9269
7. Bult, H., Boeckxstaens, G. E., Pelckmans, P. A., Jordaens, F. H., Van Maercke, Y. M., and Herman, A. G. (1990) Nitric oxide as an inhibitory nonadrenergic non-cholinergic neurotransmitter. Nature 345, 346-347
8. Marletta, M. A. (1994) Nitric oxide synthase: aspects concerning structure and catalysis. Cell 78, 927-930
9. Förstermann, U., and Sessa, W. C. (2012) Nitric oxide synthases: regulation and function. Eur. Heart J. 33, 829-837
10. Marletta, M. A. (1993) Nitric oxide synthase structure and mechanism. J. Biol. Chem. 268, 12231-12234
11. McLeod, R., and Remington, J. S. (1977) Studies on the specificity of killing of intracellular pathogens by macrophages. Cell. Immunol. 34, 156-174
12. Murray, H. W. (1981) Interaction of Leishmania with a macrophage cell line. Correlation between intracellular killing and the generation of oxygen intermediates. J. Exp. Med. 153, 1690-1695
13. Murray, H. W. (1981) Susceptibility of Leishmania to oxygen intermediates and killing by normal macrophages. J. Exp. Med. 153, 1302-1315
14. Drapier, J. C., and Hibbs, J. B., Jr. (1986) Murine cytotoxic activated macrophages inhibit aconitase in tumor cells. Inhibition involves the iron-sulfur prosthetic group and is reversible. J. Clin. Invest. 78, 790-797
15. Hibbs, J. B., Jr., Taintor, R. R., and Vavrin, Z. (1984) Iron depletion: possible cause of tumor cell cytotoxicity induced by activated macrophages. Biochem. Biophys. Res. Commun. 123, 716-723
16. Nathan, C. F., Arrick, B. A., Murray, H. W., DeSantis, N. M., and Cohn, Z. A. (1981) Tumor cell anti-oxidant defenses. Inhibition of the glutathione redox cycle enhances macrophage-mediated cytolysis. J. Exp. Med. 153, 766-782
17. Drapier, J. C., Pellat, C., and Henry, Y. (1991) Generation of EPR-detectable nitrosyl-iron complexes in tumor target cells cocultured with activated macrophages. J. Biol. Chem. 266, 10162-10167
18. Bastian, N. R., Yim, C. Y., Hibbs, J. B., Jr., and Samlowski, W. E. (1994) Induction of iron-derived EPR signals in murine cancers by nitric oxide. Evidence for multiple intracellular targets. J. Biol. Chem. 269, 5127-5131
19. Vanin, A. F., Serezhenkov, V. A., Mikoyan, V. D., and Genkin, M. V. (1998) The 2.03 signal as an indicator of dinitrosyl-iron complexes with thiol-containing ligands. Nitric Oxide 2, 224-234
20. Hickok, J. R., Sahni, S., Shen, H., Arvind, A., Antoniou, C., Fung, L. W., and Thomas, D. D. (2011) Dinitrosyliron complexes are the most abundant nitric oxide-derived cellular adduct: biological parameters of assembly and disappearance. Free Radic. Biol. Med. 51, 1558-1566
21. Li, Q., Li, C., Mahtani, H. K., Du, J., Patel, A. R., and Lancaster, J. R., Jr. (2014) Nitrosothiol formation and protection against Fenton chemistry by nitric oxide-induced dinitrosyliron complex formation from anoxia-initiated cellular chelatable iron increase. J. Biol. Chem. 289, 19917-19927
22. Watts, R. N., Hawkins, C., Ponka, P., and Richardson, D. R. (2006) 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. U.S.A. 103, 7670-7675
23. Lok, H. C., Suryo Rahmanto, Y., Hawkins, C. L., Kalinowski, D. S., Morrow, C. S., Townsend, A. J., Ponka, P., and Richardson, D. R. (2012) Nitric oxide storage and transport in cells are mediated by glutathione S-transferase P1-1 and multidrug resistance protein 1 via dinitrosyl iron complexes. J. Biol. Chem. 287, 607-618
24. Cole, S. P., Sparks, K. E., Fraser, K., Loe, D. W., Grant, C. E., Wilson, G. M., and Deeley, R. G. (1994) Pharmacological characterization of multidrug resistant MRP-transfected human tumor cells. Cancer Res. 54, 5902-5910
25. Grant, C. E., Valdimarsson, G., Hipfner, D. R., Almquist, K. C., Cole, S. P., and Deeley, R. G. (1994) Overexpression of multidrug resistance-associated protein (MRP) increases resistance to natural product drugs. Cancer Res. 54, 357-361
26. Morrow, C. S., Diah, S., Smitherman, P. K., Schneider, E., and Townsend, A. J. (1998) Multidrug resistance protein and glutathione S-transferase P1-1 act in synergy to confer protection from 4-nitroquinoline 1-oxide toxicity. Carcinogenesis 19, 109-115
27. Morrow, C. S., Smitherman, P. K., Diah, S. K., Schneider, E., and Townsend, A. J. (1998) Coordinated action of glutathione S-transferases (GSTs) and multidrug resistance protein 1 (MRP1) in antineoplastic drug detoxification. Mechanism of GST A1-1- and MRP1-associated resistance to chlorambucil in MCF7 breast carcinoma cells. J. Biol. Chem. 273, 20114-20120
28. Morrow, C. S., Smitherman, P. K., and Townsend, A. J. (1998) Combined expression of multidrug resistance protein (MRP) and glutathione S-transferase P1-1 (GSTP1-1) in MCF7 cells and high level resistance to the cytotoxicities of ethacrynic acid but not oxazaphosphorines or cisplatin. Biochem. Pharmacol. 56, 1013-1021
29. Depeille, P., Cuq, P., Mary, S., Passagne, I., Evrard, A., Cupissol, D., and Vian, L. (2004) Glutathione S-transferase M1 and multidrug resistance protein 1 act in synergy to protect melanoma cells from vincristine effects. Mol. Pharmacol. 65, 897-905
30. Depeille, P., Cuq, P., Passagne, I., Evrard, A., and Vian, L. (2005) Combined effects of GSTP1 and MRP1 in melanoma drug resistance. Br. J. Cancer 93, 216-223
31. Peklak-Scott, C., Smitherman, P. K., Townsend, A. J., and Morrow, C. S. (2008) Role of glutathione S-transferase P1-1 in the cellular detoxification of cisplatin. Mol. Cancer Ther. 7, 3247-3255
32. Sibhatu, M. B., Smitherman, P. K., Townsend, A. J., and Morrow, C. S. (2008) Expression of MRP1 and GSTP1-1 modulate the acute cellular response to treatment with the chemopreventive isothiocyanate, sulforaphane. Carcinogenesis 29, 807-815
33. Paumi, C. M., Ledford, B. G., Smitherman, P. K., Townsend, A. J., and Morrow, C. S. (2001) Role of multidrug resistance protein 1 (MRP1) and glutathione S-transferase A1-1 in alkylating agent resistance. Kinetics of glutathione conjugate formation and efflux govern differential cellular sensitivity to chlorambucil versus melphalan toxicity. J. Biol. Chem. 276, 7952-7956
34. Hayes, J. D., Flanagan, J. U., and Jowsey, I. R. (2005) Glutathione transferases. Annu. Rev. Pharmacol. Toxicol. 45, 51-88
35. Sheehan, D., Meade, G., Foley, V. M., and Dowd, C. A. (2001) Structure, function and evolution of glutathione transferases: implications for classification of non-mammalian members of an ancient enzyme superfamily. Biochem. J. 360, 1-16
36. De Maria, F., Pedersen, J. Z., Caccuri, A. M., Antonini, G., Turella, P., Stella, L., Lo Bello, M., Federici, G., and Ricci, G. (2003) The specific interaction of dinitrosyl-diglutathionyl-iron complex, a natural NO carrier, with the glutathione transferase superfamily: suggestion for an evolutionary pressure in the direction of the storage of nitric oxide. J. Biol. Chem. 278, 42283-42293
37. Cesareo, E., Parker, L. J., Pedersen, J. Z., Nuccetelli, M., Mazzetti, A. P., Pastore, A., Federici, G., Caccuri, A. M., Ricci, G., Adams, J. J., Parker, M. W., and Lo Bello, M. (2005) Nitrosylation of human glutathione transferase P1-1 with dinitrosyl diglutathionyl iron complex in vitro and in vivo. J. Biol. Chem. 280, 42172-42180
38. Lo Bello, M., Nuccetelli, M., Caccuri, A. M., Stella, L., Parker, M. W., Rossjohn, J., McKinstry, W. J., Mozzi, A. F., Federici, G., Polizio, F., Pedersen, J. Z., and Ricci, G. (2001) Human glutathione transferase P1-1 and nitric oxide carriers; a new role for an old enzyme. J. Biol. Chem. 276, 42138-42145
39. Pedersen, J. Z., De Maria, F., Turella, P., Federici, G., Mattei, M., Fabrini, R., Dawood, K. F., Massimi, M., Caccuri, A. M., and Ricci, G. (2007) Glutathione transferases sequester toxic dinitrosyl-iron complexes in cells. A protection mechanism against excess nitric oxide. J. Biol. Chem. 282, 6364-6371
40. Cole, S. P., and Deeley, R. G. (2006) Transport of glutathione and glutathione conjugates by MRP1. Trends Pharmacol. Sci. 27, 438-446
41. Ji, L., Li, H., Gao, P., Shang, G., Zhang, D. D., Zhang, N., and Jiang, T. (2013) Nrf2 pathway regulates multidrug-resistance-associated protein 1 in small cell lung cancer. PLoS ONE 8, e63404
42. Itoh, K., Chiba, T., Takahashi, S., Ishii, T., Igarashi, K., Katoh, Y., Oyake, T., Hayashi, N., Satoh, K., Hatayama, I., Yamamoto, M., and Nabeshima, Y. (1997) An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem. Biophys. Res. Commun. 236, 313-322
43. Dhakshinamoorthy, S., and Porter, A. G. (2004) Nitric oxide-induced transcriptional up-regulation of protective genes by Nrf2 via the antioxidant response element counteracts apoptosis of neuroblastoma cells. J. Biol. Chem. 279, 20096-20107
44. Ishii, T., Itoh, K., Takahashi, S., Sato, H., Yanagawa, T., Katoh, Y., Bannai, S., and Yamamoto, M. (2000) Transcription factor Nrf2 coordinately regulates a group of oxidative stress-inducible genes in macrophages. J. Biol. Chem. 275, 16023-16029
45. Ishii, Y., Itoh, K., Morishima, Y., Kimura, T., Kiwamoto, T., Iizuka, T., Hegab, A. E., Hosoya, T., Nomura, A., Sakamoto, T., Yamamoto, M., and Sekizawa, K. (2005) Transcription factor Nrf2 plays a pivotal role in protection against elastase-induced pulmonary inflammation and emphysema. J. Immunol. 175, 6968-6975
46. Innamorato, N. G., Rojo, A. I., García-Yagüe, A. J., Yamamoto, M., de Ceballos, M. L., and Cuadrado, A. (2008) The transcription factor Nrf2 is a therapeutic target against brain inflammation. J. Immunol. 181, 680-689
47. Jain, A., Lamark, T., Sjøttem, E., Larsen, K. B., Awuh, J. A., Øvervatn, A., McMahon, M., Hayes, J. D., and Johansen, T. (2010) p62/SQSTM1 is a target gene for transcription factor NRF2 and creates a positive feedback loop by inducing antioxidant response element-driven gene transcription. J. Biol. Chem. 285, 22576-22591
48. Wardrop, S. L., Watts, R. N., and Richardson, D. R. (2000) Nitrogen monoxide activates iron regulatory protein 1 RNA-binding activity by two possible mechanisms: effect on the [4Fe-4S] cluster and iron mobilization from cells. Biochemistry 39, 2748-2758
49. Wardrop, S. L., and Richardson, D. R. (2000) Interferon-γ and lipopolysaccharide regulate the expression of Nramp2 and increase the uptake of iron from low relative molecular mass complexes by macrophages. Eur. J. Biochem. 267, 6586-6593
50. LaMarre, J., Wolf, B. B., Kittler, E. L., Quesenberry, P. J., and Gonias, S. L. (1993) Regulation of macrophage α2-macroglobulin receptor/low density lipoprotein receptor-related protein by lipopolysaccharide and interferon-γ. J. Clin. Invest. 91, 1219-1224
51. Held, T. K., Weihua, X., Yuan, L., Kalvakolanu, D. V., and Cross, A. S. (1999) γ Interferon augments macrophage activation by lipopolysaccharide by two distinct mechanisms, at the signal transduction level and via an autocrine mechanism involving tumor necrosis factor alpha and interleukin-1. Infect. Immun. 67, 206-212
52. Gomez-Flores, R., Rodriguez-Padilla, C., Mehta, R. T., Galan-Wong, L., Mendoza-Gamboa, E., and Tamez-Guerra, R. (1997) Nitric oxide and TNF-α production by murine peritoneal macrophages activated with a novel 20-kDa protein isolated from Bacillus thuringiensis var. thuringiensis parasporal bodies. J. Immunol. 158, 3796-3799
53. Richardson, D. R., and Ponka, P. (1997) The molecular mechanisms of the metabolism and transport of iron in normal and neoplastic cells. Biochim. Biophys. Acta 1331, 1-40
54. Dunn, L. L., Suryo Rahmanto, Y., and Richardson, D. R. (2007) Iron uptake and metabolism in the new millennium. Trends Cell Biol. 17, 93-100
55. Silverstein, P. S., Audus, K. L., Qureshi, N., and Kumar, A. (2010) Lipopolysaccharide increases the expression of multidrug resistance-associated protein 1 (MRP1) in RAW 264.7 macrophages. J. Neuroimmune Pharmacol. 5, 516-520
56. Andrade, S. P., Hart, I. R., and Piper, P. J. (1992) Inhibitors of nitric oxide synthase selectively reduce flow in tumor-associated neovasculature. Br. J. Pharmacol. 107, 1092-1095
57. Tozer, G. M., Prise, V. E., and Chaplin, D. J. (1997) Inhibition of nitric oxide synthase induces a selective reduction in tumor blood flow that is reversible with L-arginine. Cancer Res. 57, 948-955
58. Richardson, D. R., and Baker, E. (1991) The release of iron and transferrin from the human melanoma cell. Biochim. Biophys. Acta 1091, 294-302
59. Baker, E., Page, M., and Morgan, E. H. (1985) Transferrin and iron release from rat hepatocytes in culture. Am. J. Physiol. 248, G93-G97
60. Baker, E., Vicary, F. R., and Huehns, E. R. (1981) Iron release from isolated hepatocytes. Br. J. Haematol. 47, 493-504
61. Gekeler, V., Ise, W., Sanders, K. H., Ulrich, W. R., and Beck, J. (1995) The leukotriene LTD4 receptor antagonist MK571 specifically modulates MRP associated multidrug resistance. Biochem. Biophys. Res. Commun. 208, 345-352
62. Lok, H. C., Sahni, S., Richardson, V., Kalinowski, D. S., Kovacevic, Z., Lane, D. J., and Richardson, D. R. (2014) Glutathione S-transferase and MRP1 form an integrated system involved in the storage and transport of dinitrosyl-dithiolato iron complexes in cells. Free Radic. Biol. Med. 75, 14-29
63. Suryo Rahmanto, Y., Kalinowski, D. S., Lane, D. J., Lok, H. C., Richardson, V., and Richardson, D. R. (2012) Nitrogen monoxide (NO) storage and transport by dinitrosyl-dithiol-iron complexes: long-lived NO that is trafficked by interacting proteins. J. Biol. Chem. 287, 6960-6968
64. Hayashi, A., Suzuki, H., Itoh, K., Yamamoto, M., and Sugiyama, Y. (2003) Transcription factor Nrf2 is required for the constitutive and inducible expression of multidrug resistance-associated protein 1 in mouse embryo fibroblasts. Biochem. Biophys. Res. Commun. 310, 824-829
65. Li, C. Q., Kim, M. Y., Godoy, L. C., Thiantanawat, A., Trudel, L. J., and Wogan, G. N. (2009) Nitric oxide activation of Keap1/Nrf2 signaling in human colon carcinoma cells. Proc. Natl. Acad. Sci. U.S.A. 106, 14547-14551
66. Itoh, K., Mochizuki, M., Ishii, Y., Ishii, T., Shibata, T., Kawamoto, Y., Kelly, V., Sekizawa, K., Uchida, K., and Yamamoto, M. (2004) Transcription factor Nrf2 regulates inflammation by mediating the effect of 15-deoxy-Δ(12,14)-prostaglandin J(2). Mol. Cell. Biol. 24, 36-45
67. Marro, S., Chiabrando, D., Messana, E., Stolte, J., Turco, E., Tolosano, E., and Muckenthaler, M. U. (2010) Heme controls ferroportin1 (FPN1) transcription involving Bach1, Nrf2 and a MARE/ARE sequence motif at position -7007 of the FPN1 promoter. Haematologica 95, 1261-1268
68. Ward, D. M., and Kaplan, J. (2012) Ferroportin-mediated iron transport: expression and regulation. Biochim. Biophys. Acta 1823, 1426-1433
69. Nairz, M., Schleicher, U., Schroll, A., Sonnweber, T., Theurl, I., Ludwiczek, S., Talasz, H., Brandacher, G., Moser, P. L., Muckenthaler, M. U., Fang, F. C., Bogdan, C., and Weiss, G. (2013) Nitric oxide-mediated regulation of ferroportin-1 controls macrophage iron homeostasis and immune function in Salmonella infection. J. Exp. Med. 210, 855-873
70. Donovan, A., Brownlie, A., Zhou, Y., Shepard, J., Pratt, S. J., Moynihan, J., Paw, B. H., Drejer, A., Barut, B., Zapata, A., Law, T. C., Brugnara, C., Lux, S. E., Pinkus, G. S., Pinkus, J. L., et al. (2000) Positional cloning of zebrafish ferroportin1 identifies a conserved vertebrate iron exporter. Nature 403, 776-781
71. Thimmulappa, R. K., Lee, H., Rangasamy, T., Reddy, S. P., Yamamoto, M., Kensler, T. W., and Biswal, S. (2006) Nrf2 is a critical regulator of the innate immune response and survival during experimental sepsis. J. Clin. Invest. 116, 984-995
72. Abboud, S., and Haile, D. J. (2000) A novel mammalian iron-regulated protein involved in intracellular iron metabolism. J. Biol. Chem. 275, 19906-19912
73. Hibbs, J. B., Jr, Taintor, R. R., and Vavrin, Z. (1987) Macrophage cytotoxicity: role for L-arginine deiminase and imino nitrogen oxidation to nitrite. Science 235, 473-476
74. Ruetten, H., and Thiemermann, C. (1996) Prevention of the expression of inducible nitric oxide synthase by aminoguanidine or aminoethyl-isothiourea in macrophages and in the rat. Biochem. Biophys. Res. Commun. 225, 525-530
75. Yanatori, I., Richardson, D. R., Imada, K., and Kishi, F. (2016) Iron export through the transporter ferroportin 1 is modulated by the iron chaperone PCBP2. J. Biol. Chem. 291, 17303-17318
76. Ballatori, N., Hammond, C. L., Cunningham, J. B., Krance, S. M., and Marchan, R. (2005) Molecular mechanisms of reduced glutathione transport: role of the MRP/CFTR/ABCC and OATP/SLC21A families of membrane proteins. Toxicol. Appl. Pharmacol. 204, 238-255
77. MacLeod, A. K., McMahon, M., Plummer, S. M., Higgins, L. G., Penning, T. M., Igarashi, K., and Hayes, J. D. (2009) Characterization of the cancer chemopreventive NRF2-dependent gene battery in human keratinocytes: demonstration that the KEAP1-NRF2 pathway, and not the BACH1-NRF2 pathway, controls cytoprotection against electrophiles as well as redox-cycling compounds. Carcinogenesis 30, 1571-1580
78. Buckley, B. J., Marshall, Z. M., and Whorton, A. R. (2003) Nitric oxide stimulates Nrf2 nuclear translocation in vascular endothelium. Biochem. Biophys. Res. Commun. 307, 973-979
79. Xu, X., Sutak, R., and Richardson, D. R. (2008) Iron chelation by clinically relevant anthracyclines: alteration in expression of iron-regulated genes and atypical changes in intracellular iron distribution and trafficking. Mol. Pharmacol. 73, 833-844
80. Richardson, D. R., and Baker, E. (1990) The uptake of iron and transferrin by the human malignant melanoma cell. Biochim. Biophys. Acta 1053, 1-12
81. Richardson, D., and Baker, E. (1992) Two mechanisms of iron uptake from transferrin by melanoma cells. The effect of desferrioxamine and ferric ammonium citrate. J. Biol. Chem. 267, 13972-13979
82. Watts, R. N., and Richardson, D. R. (2001) Nitrogen monoxide (NO) and glucose: unexpected links between energy metabolism and no-mediated iron mobilization from cells. J. Biol. Chem. 276, 4724-4732
83. Miranda, K. M., Espey, M. G., and Wink, D. A. (2001) A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide 5, 62-71
84. MacArthur, P. H., Shiva, S., and Gladwin, M. T. (2007) Measurement of circulating nitrite and S-nitrosothiols by reductive chemiluminescence. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 851, 93-105
85. Koley, D., and Bard, A. J. (2012) Inhibition of the MRP1-mediated transport of the menadione-glutathione conjugate (thiodione) in HeLa cells as studied by SECM. Proc. Natl. Acad. Sci. U.S.A. 109, 11522-11527
86. Richardson, D. R., Tran, E. H., and Ponka, P. (1995) The potential of iron chelators of the pyridoxal isonicotinoyl hydrazone class as effective antiproliferative agents. Blood 86, 4295-4306