Heme oxygenase-1 and breast cancer resistance protein protect against hemeinduced toxicity

Current Pharmaceutical Design

Volumn 19, Issue 15, 2013, Pages 2698-2707

  Wagener, Frank A D T G ^a   Dankers, Anita C A ^a   van Summeren, Frank ^a   Scharstuhl, Alwin ^a   van den Heuvel, Jeroen J M W ^a   Koenderink, Jan B ^a   Pennings, Sebastiaan W C ^a   Russel, Frans G M ^a   Masereeuw, Rosalinde ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Abc transporter; Abcg2; Bcrp; Cytotoxicity; Dna damage; Heme ho system; Reactive oxygen species; Redox balance

Indexed keywords

ACETYLCYSTEINE; BILIRUBIN; BILIVERDIN; BREAST CANCER RESISTANCE PROTEIN; CARBON MONOXIDE; HEME; HEME OXYGENASE 1; IRON; MESOPORPHYRIN; REACTIVE OXYGEN METABOLITE;

ARTICLE; BACULOVIRUS EXPRESSION SYSTEM; CELL DEATH; CELL PROTECTION; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; DNA DAMAGE; EMBRYO; FLOW CYTOMETRY; HUMAN; HUMAN CELL; KIDNEY CELL CULTURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; WESTERN BLOTTING;

ATP-BINDING CASSETTE TRANSPORTERS; BENZIMIDAZOLES; BLOTTING, WESTERN; DNA DAMAGE; HEK293 CELLS; HEME; HEME OXYGENASE-1; HUMANS; NEOPLASM PROTEINS; OXIDANTS; REACTIVE OXYGEN SPECIES;

EID: 84876701346     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/1381612811319150004     Document Type: Article

References (58)

1. Beri R, Chandra R. Chemistry and biology of heme. Effect of metal salts, organometals, and metalloporphyrins on heme synthesis and catabolism, with special reference to clinical implications and interactions with cytochrome P-450. Drug Metab Rev 1993; 25(1- 2): 49-152.
2. Wagener FA, Volk HD, Willis D, et al. Different faces of the heme-heme oxygenase system in inflammation. Pharmacol Rev 2003; 55(3): 551-71.
3. Fortes GB, Alves LS, de Oliveira R, et al. Heme induces programmed necrosis on macrophages through autocrine TNF and ROS production. Blood 2012; 119(10): 2368-75.
4. Vinchi F, Gastaldi S, Silengo L, Altruda F, Tolosano E. Hemopexin prevents endothelial damage and liver congestion in a mouse model of heme overload. Am J Pathol 2008; 173(1): 289-99.
5. Wagener FA, Eggert A, Boerman OC, et al. Heme is a potent inducer of inflammation in mice and is counteracted by heme oxygenase. Blood 2001; 98(6): 1802-11.
6. Wagener FA, Scharstuhl A, Tyrrell RM, et al. The heme-heme oxygenase system in wound healing; implications for scar formation. Curr Drug Targets 2010; 11(12): 1571-85.
7. Belcher JD, Beckman JD, Balla G, Balla J, Vercellotti G. Heme degradation and vascular injury. Antioxid Redox Signal 2010; 12(2): 233-48.
8. Belcher JD, Vineyard JV, Bruzzone CM, et al. Heme oxygenase-1 gene delivery by Sleeping Beauty inhibits vascular stasis in a murine model of sickle cell disease. Journal of molecular medicine 2010; 88(7): 665-75.
9. Tracz MJ, Alam J, Nath KA. Physiology and pathophysiology of heme: implications for kidney disease. J Am Soc Nephrol 2007; 18(2): 414-20.
10. Lundvig DM, Immenschuh S, Wagener FA. Heme oxygenase, inflammation, and fibrosis: the good, the bad, and the ugly? Frontiers in Pharmacology 2012; 3(81): 1-14.
11. Fernandez PL, Dutra FF, Alves L, et al. Heme amplifies the innate immune response to microbial molecules through spleen tyrosine kinase (Syk)-dependent reactive oxygen species generation. J Biol Chem 2010; 285(43): 32844-51.
12. Pamplona A, Hanscheid T, Epiphanio S, Mota MM, Vigario AM. Cerebral malaria and the hemolysis/methemoglobin/heme hypothesis: shedding new light on an old disease. Int J Biochem Cell Biol 2009; 41(4): 711-6.
13. Pamplona A, Ferreira A, Balla J, et al. Heme oxygenase-1 and carbon monoxide suppress the pathogenesis of experimental cerebral malaria. Nat Med 2007; 13(6): 703-10.
14. Larsen R, Gozzelino R, Jeney V, et al. A central role for free heme in the pathogenesis of severe sepsis. Science translational medicine 2010; 2(51): 51ra71.
15. Zager RA. Mitochondrial free radical production induces lipid peroxidation during myohemoglobinuria. Kidney Int 1996; 49(3): 741-51.
16. Schaer DJ, Alayash AI. Clearance and control mechanisms of hemoglobin from cradle to grave. Antioxid Redox Signal 2010; 12(2): 181-4.
17. Nath KA, Haggard JJ, Croatt AJ, Grande JP, Poss KD, Alam J. The indispensability of heme oxygenase-1 in protecting against acute heme protein-induced toxicity in vivo. Am J Pathol 2000; 156(5): 1527-35.
18. Nath KA, Croatt AJ, Haggard JJ, Grande JP. Renal response to repetitive exposure to heme proteins: chronic injury induced by an acute insult. Kidney Int 2000; 57(6): 2423-33.
19. Nath KA, Balla G, Vercellotti GM, et al. Induction of heme oxygenase is a rapid, protective response in rhabdomyolysis in the rat. J Clin Invest 1992; 90(1): 267-70.
20. Li Volti G, Sorrenti V, Murabito P, et al. Pharmacological induction of heme oxygenase-1 inhibits iNOS and oxidative stress in renal ischemia-reperfusion injury. Transplant Proc 2007; 39(10): 2986-91.
21. Wagener FA, da Silva JL, Farley T, de Witte T, Kappas A, Abraham NG. Differential effects of heme oxygenase isoforms on heme mediation of endothelial intracellular adhesion molecule 1 expression. J Pharmacol Exp Ther 1999; 291(1): 416-23.
22. Sacerdoti D, Escalante B, Abraham NG, McGiff JC, Levere RD, Schwartzman ML. Treatment with tin prevents the development of hypertension in spontaneously hypertensive rats. Science 1989; 243(4889): 388-90.
23. Krishnamurthy P, Schuetz JD. The role of ABCG2 and ABCB6 in porphyrin metabolism and cell survival. Curr Pharm Biotechnol 2011; 12(4): 647-55.
24. Staud F, Pavek P. Breast cancer resistance protein (BCRP/ ABCG2). Int J Biochem Cell Biol 2005; 37(4): 720-5.
25. Zhou S, Zong Y, Ney PA, Nair G, Stewart CF, Sorrentino BP. Increased expression of the Abcg2 transporter during erythroid maturation plays a role in decreasing cellular protoporphyrin IX levels. Blood 2005; 105(6): 2571-6.
26. Krishnamurthy P, Schuetz JD. The ABC transporter Abcg2/Bcrp: role in hypoxia mediated survival. Biometals 2005; 18(4): 349-58.
27. Krishnamurthy P, Ross DD, Nakanishi T, et al. The stem cell marker Bcrp/ABCG2 enhances hypoxic cell survival through interactions with heme. J Biol Chem 2004; 279(23): 24218-25.
28. Krishnamurthy P, Schuetz JD. Role of ABCG2/BCRP in biology and medicine. Annu Rev Pharmacol Toxicol 2006; 46: 381-410.
29. Scharstuhl A, Mutsaers HA, Pennings SW, Szarek WA, Russel FG, Wagener FA. Curcumin-induced fibroblast apoptosis and in vitro wound contraction are regulated by antioxidants and heme oxygenase: implications for scar formation. J Cell Mol Med 2009; 13(4): 712-25.
30. Avishai N, Rabinowitz C, Moiseeva E, Rinkevich B. Genotoxicity of the Kishon River, Israel: the application of an in vitro cellular assay. Mutat Res 2002; 518(1): 21-37.
31. El-Sheikh AA, van den Heuvel JJ, Koenderink JB, Russel FG. Interaction of nonsteroidal anti-inflammatory drugs with multidrug resistance protein (MRP) 2/ABCC2- and MRP4/ABCC4-mediated methotrexate transport. J Pharmacol Exp Ther 2007; 320(1): 229-35.
32. El-Sheikh AA, van den Heuvel JJ, Krieger E, Russel FG, Koenderink JB. Functional role of arginine 375 in transmembrane helix 6 of multidrug resistance protein 4 (MRP4/ABCC4). Mol Pharmacol 2008; 74(4): 964-71.
33. El-Sheikh AA, Masereeuw R, Russel FG. Mechanisms of renal anionic drug transport. Eur J Pharmacol 2008; 585(2-3): 245-55.
34. El-Sheikh AA, van den Heuvel JJ, Koenderink JB, Russel FG. Effect of hypouricaemic and hyperuricaemic drugs on the renal urate efflux transporter, multidrug resistance protein 4. Br J Pharmacol 2008; 155(7): 1066-75.
35. Balla J, Vercellotti GM, Nath K, et al. Haem, haem oxygenase and ferritin in vascular endothelial cell injury. Nephrol Dial Transplant 2003; 18 Suppl 5: v8-12.
36. Platt JL, Nath KA. Heme oxygenase: protective gene or Trojan horse. Nat Med 1998; 4(12): 1364-5.
37. Takahashi T, Shimizu H, Morimatsu H, et al. Heme oxygenase-1: a fundamental guardian against oxidative tissue injuries in acute inflammation. Mini Rev Med Chem 2007; 7(7): 745-53.
38. Belcher JD, Mahaseth H, Welch TE, Otterbein LE, Hebbel RP, Vercellotti GM. Heme oxygenase-1 is a modulator of inflammation and vaso-occlusion in transgenic sickle mice. J Clin Invest 2006; 116(3): 808-16.
39. Wagener FA, Abraham NG, van Kooyk Y, de Witte T, Figdor CG. Heme-induced cell adhesion in the pathogenesis of sickle-cell disease and inflammation. Trends Pharmacol Sci 2001; 22(2): 52-4.
40. Allhorn M, Lundqvist K, Schmidtchen A, Akerstrom B. Hemescavenging role of alpha1-microglobulin in chronic ulcers. J Invest Dermatol 2003; 121(3): 640-6.
41. Wagener FA, van Beurden HE, von den Hoff JW, Adema GJ, Figdor CG. The heme-heme oxygenase system: a molecular switch in wound healing. Blood 2003; 102(2): 521-8. Epub 2003/03/22.
42. Ferreira A, Balla J, Jeney V, Balla G, Soares MP. A central role for free heme in the pathogenesis of severe malaria: the missing link? Journal of molecular medicine 2008; 86(10): 1097-111.
43. Zenclussen ML, Casalis PA, El-Mousleh T, et al. Haem oxygenase- 1 dictates intrauterine fetal survival in mice via carbon monoxide. J Pathol 2011; 225(2): 293-304.
44. Yachie A, Niida Y, Wada T, Igarashi N, Kaneda H, Toma T, et al. Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency. J Clin Invest 1999; 103(1): 129-35.
45. Letarte PB, Lieberman K, Nagatani K, Haworth RA, Odell GB, Duff TA. Hemin: levels in experimental subarachnoid hematoma and effects on dissociated vascular smooth-muscle cells. J Neurosurg 1993; 79(2): 252-5.
46. Visch HJ, Rutter GA, Koopman WJ, et al. Inhibition of mitochondrial Na+-Ca2+ exchange restores agonist-induced ATP production and Ca2+ handling in human complex I deficiency. J Biol Chem 2004; 279(39): 40328-36.
47. Abraham NG, Cao J, Sacerdoti D, Li X, Drummond GS. Heme Oxygenase: The Key to Renal Function Regulation. Am J Physiol Renal Physiol 2009.
48. Ascenzi P, Bocedi A, Visca P, et al. Hemoglobin and heme scavenging. IUBMB Life 2005; 57(11): 749-59. Epub 2006/03/04.
49. Belcher JD, Vineyard JV, Bruzzone CM, et al. Heme oxygenase-1 gene delivery by Sleeping Beauty inhibits vascular stasis in a murine model of sickle cell disease. J Mol Med 2010; 88: 665-75.
50. Uc A, Stokes JB, Britigan BE. Heme transport exhibits polarity in Caco-2 cells: evidence for an active and membrane proteinmediated process. Am J Physiol-Gastr L 2004; 287(6): G1150-G7.
51. Immenschuh S, Nell C, Iwahara S, Katz N, Muller-Eberhard U. Gene regulation of HBP 23 by metalloporphyrins and protoporphyrin IX in liver and hepatocyte cultures. Biochem Biophys Res Commun 1997; 231(3): 667-70.
52. Akagi R, Takahashi T, Sassa S. Cytoprotective effects of heme oxygenase in acute renal failure. Contributions to nephrology 2005; 148: 70-85.
53. Shimizu H, Takahashi T, Suzuki T, et al. Protective effect of heme oxygenase induction in ischemic acute renal failure. Crit Care Med 2000; 28(3): 809-17.
54. Dankers ACA, Sweep FCGJ, Pertijs JCLM, Verweij V, et al. Localization of breast cancer resistance protein (BCRP) in endocrine organs and inhibition of its transport activity by steroid hormones. Cell Tissue Res 2012; 349(2): 551-63.
55. Huls M, Russel FG, Masereeuw R. The role of ATP binding cassette transporters in tissue defense and organ regeneration. J Pharmacol Exp Ther 2009; 328(1): 3-9.
56. Huls M, Brown CD, Windass AS, et al. The breast cancer resistance protein transporter ABCG2 is expressed in the human kidney proximal tubule apical membrane. Kidney Int 2008; 73(2): 220-5.
57. Fernandez-Funez A, Polo FJ, Broseta L, Valer J, Zafrilla L. Effects of N-acetylcysteine on myoglobinuric-acute renal failure in rats. Ren Fail 2002; 24(6): 725-33.
58. Dekker D, Dorresteijn MJ, Pijnenburg M, et al. The bilirubinincreasing drug atazanavir improves endothelial function in patients with type 2 diabetes mellitus. Arterioscler Thromb Vasc Biol 2011; 31(2): 458-63.