5-Aminolevulinic acid combined with ferrous iron enhances the expression of heme oxygenase-1

International Immunopharmacology

Volumn 19, Issue 2, 2014, Pages 300-307

  Nishio, Yoshiaki ^a,b   Fujino, Masayuki ^a,c   Zhao, Mingyi ^a   Ishii, Takuya ^d   Ishizuka, Masahiro ^d   Ito, Hidenori ^d   Takahashi, Kiwamu ^d   Abe, Fuminori ^d   Nakajima, Motowo ^d   Tanaka, Tohru ^d   Taketani, Shigeru ^e   Nagahara, Yukitoshi ^b   Li, Xiao Kang ^a  

^a NATIONAL RESEARCH INSTITUTE FOR CHILD HEALTH AND DEVELOPMENT   (Japan)

^b TOKYO DENKI UNIVERSITY   (Japan)

^c NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^d SBI Pharmaceuticals Co   (Japan)

^e KYOTO INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

5 Aminolevulinic acid (ALA); Bach1; Heme; Heme oxygenase 1 (HO 1); Mitogen activated protein kinases (MAPKs); Nrf2

Indexed keywords

AMINOLEVULINIC ACID; BACH1 PROTEIN; FERROUS ION; HEME; HEME OXYGENASE 1; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; MITOGEN ACTIVATED PROTEIN KINASE P38 INHIBITOR; SMALL INTERFERING RNA; SODIUM FERROUS CITRATE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; CYTOSOL; DRUG MECHANISM; DRUG METABOLISM; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; IMMUNOPRECIPITATION; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; UPREGULATION;

5-AMINOLEVULINIC ACID (ALA); BACH1; HEME; HEME OXYGENASE-1 (HO-1); MITOGEN-ACTIVATED PROTEIN KINASES (MAPKS); NRF2;

AMINOLEVULINIC ACID; ANIMALS; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CELL LINE; ENZYME INDUCTION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FERROUS COMPOUNDS; HEME OXYGENASE-1; MEMBRANE PROTEINS; MICE; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RNA, MESSENGER; RNA, SMALL INTERFERING;

EID: 84896823326     PISSN: 15675769     EISSN: 18781705     Source Type: Journal    
DOI: 10.1016/j.intimp.2014.02.003     Document Type: Article

References (51)

1. M. Ishizuka, F. Abe, Y. Sano, K. Takahashi, K. Inoue, and M. Nakajima et al. Novel development of 5-aminolevurinic acid (ALA) in cancer diagnoses and therapy Int Immunopharmacol 11 2011 358 365
2. S. Taketani Aquisition, mobilization and utilization of cellular iron and heme: endless findings and growing evidence of tight regulation Tohoku J Exp Med 205 2005 297 318
3. A.S. Tsiftsoglou, A.I. Tsamadou, and L.C. Papadopoulou Heme as key regulator of major mammalian cellular functions: molecular, cellular, and pharmacological aspects Pharmacol Ther 111 2006 327 345
4. Y. Hagiya, T. Adachi, S. Ogura, R. An, A. Tamura, and H. Nakagawa et al. Nrf2-dependent induction of human ABC transporter ABCG2 and heme oxygenase-1 in HepG2 cells by photoactivation of porphyrins: biochemical implications for cancer cell response to photodynamic therapy J Exp Ther Oncol 7 2008 153 167
5. J. Hou, S. Cai, Y. Kitajima, M. Fujino, H. Ito, and K. Takahashi et al. 5-Aminolevulinic acid combined with ferrous iron induces carbon monoxide generation in mouse kidneys and protects from renal ischemia-reperfusion injury Am J Physiol Ren Physiol 305 2013 F1149 F1157
6. M.D. Maines Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications FASEB J 2 1988 2557 2568
7. S.A. Rushworth, X.L. Chen, N. Mackman, R.M. Ogborne, and M.A. O'Connell Lipopolysaccharide-induced heme oxygenase-1 expression in human monocytic cells is mediated via Nrf2 and protein kinase C J Immunol 175 2005 4408 4415
8. M. Rizzardini, M. Terao, F. Falciani, and L. Cantoni Cytokine induction of haem oxygenase mRNA in mouse liver. Interleukin 1 transcriptionally activates the haem oxygenase gene Biochem J 290 Pt 2 1993 343 347
9. C.M. Terry, J.A. Clikeman, J.R. Hoidal, and K.S. Callahan TNF-alpha and IL-1alpha induce heme oxygenase-1 via protein kinase C, Ca2 +, and phospholipase A2 in endothelial cells Am J Physiol 276 1999 H1493 H1501
10. J. Alam, S. Shibahara, and A. Smith Transcriptional activation of the heme oxygenase gene by heme and cadmium in mouse hepatoma cells J Biol Chem 264 1989 6371 6375
11. V.E. Reeve, M. Allanson, J.L. Cho, S.J. Arun, and D. Domanski Interdependence between heme oxygenase-1 induction and estrogen-receptor-beta signaling mediates photoimmune protection by UVA radiation in mice J Invest Dermatol 129 2009 2702 2710
12. M.D. Maines, and J.F. Ewing Stress response of the rat testis: in situ hydridization and immunohistochemical analysis of heme oxygenase-1 (HSP32) induction by hyperthermia Biol Reprod 54 1996 1070 1079
13. T. Kitamuro, K. Takahashi, K. Ogawa, R. Udono-Fujimori, K. Takeda, and K. Furuyama et al. Bach1 functions as a hypoxia-inducible repressor for the heme oxygenase-1 gene in human cells J Biol Chem 278 2003 9125 9133
14. C.L. Hartsfield, J. Alam, J.L. Cook, and A.M. Choi Regulation of heme oxygenase-1 gene expression in vascular smooth muscle cells by nitric oxide Am J Physiol 273 1997 L980 L988
15. C. Hualin, X. Wenli, L. Dapeng, L. Xijing, P. Xiuhua, and P. Qingfeng The anti-inflammatory mechanism of heme oxygenase-1 induced by hemin in primary rat alveolar macrophages Inflammation 35 2012 1087 1093
16. C. Cai, L. Teng, D. Vu, J.Q. He, Y. Guo, and Q. Li et al. The heme oxygenase 1 inducer (CoPP) protects human cardiac stem cells against apoptosis through activation of the extracellular signal-regulated kinase (ERK)/NRF2 signaling pathway and cytokine release J Biol Chem 287 2012 33720 33732
17. Y. Shan, R.W. Lambrecht, S.E. Donohue, and H.L. Bonkovsky Role of Bach1 and Nrf2 in up-regulation of the heme oxygenase-1 gene by cobalt protoporphyrin FASEB J 20 2006 2651 2653
18. M.H. Kapturczak, C. Wasserfall, T. Brusko, M. Campbell-Thompson, T.M. Ellis, and M.A. Atkinson et al. Heme oxygenase-1 modulates early inflammatory responses: evidence from the heme oxygenase-1-deficient mouse Am J Pathol 165 2004 1045 1053
19. A. Yachie, Y. Niida, T. Wada, N. Igarashi, H. Kaneda, and T. Toma et al. Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency J Clin Invest 103 1999 129 135
20. K.D. Poss, and S. Tonegawa Reduced stress defense in heme oxygenase 1-deficient cells Proc Natl Acad Sci U S A 94 1997 10925 10930
21. Y. Masuya, K. Hioki, R. Tokunaga, and S. Taketani Involvement of the tyrosine phosphorylation pathway in induction of human heme oxygenase-1 by hemin, sodium arsenite, and cadmium chloride J Biochem 124 1998 628 633
22. X. Zhang, E.L. Bedard, R. Potter, R. Zhong, J. Alam, and A.M. Choi et al. Mitogen-activated protein kinases regulate HO-1 gene transcription after ischemia-reperfusion lung injury Am J Physiol Lung Cell Mol Physiol 283 2002 L815 L829
23. C.K. Andreadi, L.M. Howells, P.A. Atherfold, and M.M. Manson Involvement of Nrf2, p38, B-Raf, and nuclear factor-kappaB, but not phosphatidylinositol 3-kinase, in induction of hemeoxygenase-1 by dietary polyphenols Mol Pharmacol 69 2006 1033 1040
24. P. Moi, K. Chan, I. Asunis, A. Cao, and Y.W. Kan Isolation of NF-E2-related factor 2 (Nrf2), a NF-E2-like basic leucine zipper transcriptional activator that binds to the tandem NF-E2/AP1 repeat of the beta-globin locus control region Proc Natl Acad Sci U S A 91 1994 9926 9930
25. T. Oyake, K. Itoh, H. Motohashi, N. Hayashi, H. Hoshino, and M. Nishizawa et al. Bach proteins belong to a novel family of BTB-basic leucine zipper transcription factors that interact with MafK and regulate transcription through the NF-E2 site Mol Cell Biol 16 1996 6083 6095
26. K. Igarashi, H. Hoshino, A. Muto, N. Suwabe, S. Nishikawa, and H. Nakauchi et al. Multivalent DNA binding complex generated by small Maf and Bach1 as a possible biochemical basis for beta-globin locus control region complex J Biol Chem 273 1998 11783 11790
27. M. Fujino, X.K. Li, Y. Kitazawa, L. Guo, M. Kawasaki, and N. Funeshima et al. Distinct pathways of apoptosis triggered by FTY720, etoposide, and anti-Fas antibody in human T-lymphoma cell line (Jurkat cells) J Pharmacol Exp Ther 300 2002 939 945
28. R. Mashima, L. Tilley, M.A. Siomos, V. Papalexis, M.J. Raftery, and R. Stocker Plasmodium falciparum histidine-rich protein-2 (PfHRP2) modulates the redox activity of ferri-protoporphyrin IX (FePPIX): peroxidase-like activity of the PfHRP2-FePPIX complex J Biol Chem 277 2002 14514 14520
29. P. Vanachayangkul, and W.H. Tolleson Inhibition of heme peroxidases by melamine Enzyme Res 2012 2012 416062
30. K. Ogawa, J. Sun, S. Taketani, O. Nakajima, C. Nishitani, and S. Sassa et al. Heme mediates derepression of Maf recognition element through direct binding to transcription repressor Bach1 EMBO J 20 2001 2835 2843
31. Y. Shan, R.W. Lambrecht, T. Ghaziani, S.E. Donohue, and H.L. Bonkovsky Role of Bach-1 in regulation of heme oxygenase-1 in human liver cells: insights from studies with small interfering RNAS J Biol Chem 279 2004 51769 51774
32. S. Okada, A. Muto, E. Ogawa, A. Nakanome, Y. Katoh, and S. Ikawa et al. Bach1-dependent and -independent regulation of heme oxygenase-1 in keratinocytes J Biol Chem 285 2010 23581 23589
33. N.G. Abraham, Y. Lavrovsky, M.L. Schwartzman, R.A. Stoltz, R.D. Levere, and M.E. Gerritsen et al. Transfection of the human heme oxygenase gene into rabbit coronary microvessel endothelial cells: protective effect against heme and hemoglobin toxicity Proc Natl Acad Sci U S A 92 1995 6798 6802
34. P.J. Lee, J. Alam, G.W. Wiegand, and A.M. Choi Overexpression of heme oxygenase-1 in human pulmonary epithelial cells results in cell growth arrest and increased resistance to hyperoxia Proc Natl Acad Sci U S A 93 1996 10393 10398
35. X.H. Li, X. Gong, L. Zhang, R. Jiang, H.Z. Li, and M.J. Wu et al. Protective effects of polydatin on septic lung injury in mice via upregulation of HO-1 Mediators Inflamm 2013 2013 354087
36. L.E. Otterbein, F.H. Bach, J. Alam, M. Soares, H. Tao Lu, and M. Wysk et al. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway Nat Med 6 2000 422 428
37. D.E. Baranano, M. Rao, C.D. Ferris, and S.H. Snyder Biliverdin reductase: a major physiologic cytoprotectant Proc Natl Acad Sci U S A 99 2002 16093 16098
38. J.K. Sarady-Andrews, F. Liu, D. Gallo, A. Nakao, M. Overhaus, and R. Ollinger et al. Biliverdin administration protects against endotoxin-induced acute lung injury in rats Am J Physiol Lung Cell Mol Physiol 289 2005 L1131 L1137
39. D. Martin, A.I. Rojo, M. Salinas, R. Diaz, G. Gallardo, and J. Alam et al. Regulation of heme oxygenase-1 expression through the phosphatidylinositol 3-kinase/Akt pathway and the Nrf2 transcription factor in response to the antioxidant phytochemical carnosol J Biol Chem 279 2004 8919 8929
40. K. Itoh, N. Wakabayashi, Y. Katoh, T. Ishii, K. Igarashi, and J.D. Engel et al. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain Genes Dev 13 1999 76 86
41. J. Alam, D. Stewart, C. Touchard, S. Boinapally, A.M. Choi, and J.L. Cook Nrf2, a Cap'n'Collar transcription factor, regulates induction of the heme oxygenase-1 gene J Biol Chem 274 1999 26071 26078
42. T. Ishii, K. Itoh, S. Takahashi, H. Sato, T. Yanagawa, and Y. Katoh et al. Transcription factor Nrf2 coordinately regulates a group of oxidative stress-inducible genes in macrophages J Biol Chem 275 2000 16023 16029
43. D. Talbot, and F. Grosveld The 5′HS2 of the globin locus control region enhances transcription through the interaction of a multimeric complex binding at two functionally distinct NF-E2 binding sites EMBO J 10 1991 1391 1398
44. H. Motohashi, J.A. Shavit, K. Igarashi, M. Yamamoto, and J.D. Engel The world according to Maf Nucleic Acids Res 25 1997 2953 2959
45. N.S. Rajasekaran, S. Varadharaj, G.D. Khanderao, C.J. Davidson, S. Kannan, and M.A. Firpo et al. Sustained activation of nuclear erythroid 2-related factor 2/antioxidant response element signaling promotes reductive stress in the human mutant protein aggregation cardiomyopathy in mice Antioxid Redox Signal 14 2011 957 971
46. M. Furukawa, and Y. Xiong BTB protein Keap1 targets antioxidant transcription factor Nrf2 for ubiquitination by the Cullin 3-Roc1 ligase Mol Cell Biol 25 2005 162 171
47. J.J. Boyle, M. Johns, J. Lo, A. Chiodini, N. Ambrose, and P.C. Evans et al. Heme induces heme oxygenase 1 via Nrf2: role in the homeostatic macrophage response to intraplaque hemorrhage Arterioscler Thromb Vasc Biol 31 2011 2685 2691
48. J.W. Lee, Y.J. Choi, J.H. Park, J.Y. Sim, Y.S. Kwon, and H.J. Lee et al. 3,4,5-Trihydroxycinnamic acid inhibits lipopolysaccharide-induced inflammatory response through the activation of Nrf2 pathway in BV2 microglial cells Biomol Ther 21 2013 60 65
49. E. Balogun, M. Hoque, P. Gong, E. Killeen, C.J. Green, and R. Foresti et al. Curcumin activates the haem oxygenase-1 gene via regulation of Nrf2 and the antioxidant-responsive element Biochem J 371 2003 887 895
50. N.H. Kim, M.K. Oh, H.J. Park, and I.S. Kim Auranofin, a gold(I)-containing antirheumatic compound, activates Keap1/Nrf2 signaling via Rac1/iNOS signal and mitogen-activated protein kinase activation J Pharmacol Sci 113 2010 246 254
51. J. Sun, H. Hoshino, K. Takaku, O. Nakajima, A. Muto, and H. Suzuki et al. Hemoprotein Bach1 regulates enhancer availability of heme oxygenase-1 gene EMBO J 21 2002 5216 5224