Acrolein induces heme oxygenase-1 through PKC-δ and PI3K in human bronchial epithelial cells

American Journal of Respiratory Cell and Molecular Biology

Volumn 38, Issue 4, 2008, Pages 483-490

  Zhang, Hongqiao ^a   Forman, Henry Jay ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Acrolein; Akt; Heme oxygenase 1; PKC

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 [1 (3 AMIDINOTHIOPROPYL) 1H INDOL 3 YL] 3 (1 METHYL 1H INDOL 3 YL)MALEIMIDE; 2 MORPHOLINO 8 PHENYLCHROMONE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ACROLEIN; HEME OXYGENASE 1; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE C; ROTTLERIN; STAUROSPORINE; TRANSCRIPTION FACTOR NRF2; TRANSFER RNA; WORTMANNIN; ENZYME INHIBITOR; PROTEIN KINASE C DELTA; SMALL INTERFERING RNA;

ARTICLE; BRONCHUS MUCOSA; CELL NUCLEUS; CONTROLLED STUDY; ENZYME INDUCTION; EPITHELIUM CELL; GENE SILENCING; HUMAN; HUMAN CELL; BIOSYNTHESIS; BRONCHUS; CELL CULTURE; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; SIGNAL TRANSDUCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ACROLEIN; BRONCHI; CELLS, CULTURED; ENZYME INDUCTION; ENZYME INHIBITORS; EPITHELIAL CELLS; HEME OXYGENASE-1; HUMANS; MAP KINASE SIGNALING SYSTEM; NF-E2-RELATED FACTOR 2; PROTEIN KINASE C-DELTA; RNA, SMALL INTERFERING; TRANSCRIPTION, GENETIC;

EID: 41449112375     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2007-0260OC     Document Type: Article

References (62)

1. Ryter SW, Alam J, Choi AM. Heme oxygenase-1/carbonmonoxide: from basic science to therapeutic applications. Physiol Rev 2006;86:583-650.
2. Morse D, Choi AM. Heme oxygenase-1: the "emerging molecule" has arrived. Am J Respir Cell Mol Biol 2002;27:8-16.
3. Celec P, Prihodova M. Pathogenesis of Alzheimer's disease and the role of heme oxygenase: new perspectives and hypothesis. Folia Neuropathol 2003;41:155-160.
4. Takeda A, Itoyama Y, Kimpara T, Zhu X, Avila J, Dwyer BE, Perry G, Smith MA. Heme catabolism and heme oxygenase in neurodegenerative disease. Antioxid Redox Signal 2004;6:888-894.
5. Dulak J, Loboda A, Zagorska A, Jozkowicz A. Complex role of heme oxygenase-1 in angiogenesis. Antioxid Redox Signal 2004;6:858-866.
6. Slebos DJ, Ryter SW, Choi AM. Heme oxygenase-1 and carbon monoxide in pulmonary medicine. Respir Res 2003;4:7.
7. Fredenburgh LE, Perrella MA, Mitsialis SA. The role of heme oxygenase-1 in pulmonary disease. Am J Respir Cell Mol Biol 2007;36:158-165.
8. Kobayashi M, Yamamoto M. Molecular mechanisms activating the nrf2-keap1 pathway of antioxidant gene regulation. Antioxid Redox Signal 2005;7:385-394.
9. Katoh Y, Iida K, Kang MI, Kobayashi A, Mizukami M, Tong KI, McMahon M, Hayes JD, Itoh K, Yamamoto M. Evolutionary conserved N-terminal domain of Nrf2 is essential for the Keap1-mediated degradation of the protein by proteasome. Arch Biochem Biophys 2005;433:342-350.
10. Nguyen T, Yang CS, Pickett CB. The pathways and molecular mechanisms regulating Nrf2 activation in response to chemical stress. Free Radic Biol Med 2004;37:433-441.
11. Alam J, Wicks C, Stewart D, Gong P, Touchard C, Otterbein S, Choi AM, Burow ME, Tou J. Mechanism of heme oxygenase-1 gene activation by cadmium in MCF-7 mammary epithelial cells. Role of p38 kinase and Nrf2 transcription factor. J Biol Chem 2000;275:27694-27702.
12. Alam J, Killeen E, Gong P, Naquin R, Hu B, Stewart D, Ingelfinger JR, Nath KA. Heme activates the heme oxygenase-1 gene in renal epithelial cells by stabilizing Nrf2. Am J Physiol Renal Physiol 2003;284:F743-F752.
13. Balogun E, Hoque M, Gong P, Killeen E, Green CJ, Foresti R, Alam J, Motterlini R. Curcumin activates the haem oxygenase-1 gene via regulation of Nrf2 and the antioxidant-responsive element. Biochem J 2003;371:887-895.
14. Martin D, Rojo AI, Salinas M, Diaz R, Gallardo G, Alam J, De Galarreta CM, Cuadrado A. 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 2004;279:8919-8929.
15. Anwar AA, Li FY, Leake DS, Ishii T, Mann GE, Siow RC. Induction of heme oxygenase 1 by moderately oxidized low-density lipoproteins in human vascular smooth muscle cells: role of mitogen-activated protein kinases and Nrf2. Free Radic Biol Med 2005;39:227-236.
16. Chen CY, Jang JH, Li MH, Surh YJ. Resveratrol upregulates heme oxygenase-1 expression via activation of NF-E2-related factor 2 in PC12 cells. Biochem Biophys Res Commun 2005;331:993-1000.
17. Andreadi CK, Howells LM, Atherfold PA, Manson MM. 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 2006;69:1033-1040.
18. Shan Y, Lambrecht RW, Donohue SE, Bonkovsky HL. Role of Bach1 and Nrf2 in up-regulation of the heme oxygenase-1 gene by cobalt protoporphyrin. FASEB J 2006;20:2651-2653.
19. Liu XM, Peyton KJ, Ensenat D, Wang H, Hannink M, Alam J, Durante W. Nitric oxide stimulates heme oxygenase-1 gene transcription via the Nrf2/ARE complex to promote vascular smooth muscle cell survival. Cardiovasc Res 2007;75:381-389.
20. Keum YS, Yu S, Chang PP, Yuan X, Kim JH, Xu C, Han J, Agarwal A, Kong AN. Mechanism of Action of sulforaphane: inhibition of p38 mitogen-activated protein kinase isoforms contributing to the induction of antioxidant response element-mediated heme oxygenase-1 in human hepatoma HepG2 cells. Cancer Res 2006;66:8804-8813.
21. Kocanova S, Buytaert E, Matroule JY, Piette J, Golab J, de Witte P, Agostinis P. Induction of heme-oxygenase 1 requires the p38(MAPK) and PI3K pathways and suppresses apoptotic cell death following hypericin-mediated photodynamic therapy. Apoptosis 2007;12:731-741.
22. Huang HC, Nguyen T, Pickett CB. Regulation of the antioxidant response element by protein kinase C-mediated phosphorylation of NF-E2-related factor 2. Proc Natl Acad Sci USA 2000;97:12475-12480.
23. Bloom DA, Jaiswal AK. Phosphorylation of Nrf2 at Ser40 by protein kinase C in response to antioxidants leads to the release of Nrf2 from INrf2, but is not required for Nrf2 stabilization/accumulation in the nucleus and transcriptional activation of antioxidant response element-mediated NAD(P)H:quinone oxidoreductase-1 gene expression. J Biol Chem 2003;278:44675-44682.
24. Jain AK, Jaiswal AK. GSK-3beta Acts Upstream of Fyn Kinase in Regulation of Nuclear Export and Degradation of NF-E2 Related Factor 2. J Biol Chem 2007;282:16502-16510.
25. Zhang H, Liu H, Iles KE, Liu RM, Postlethwait EM, Laperche Y, Forman HJ. 4-hydroxynonenal induces rat gamma-glutamyl transpeptidase through mitogen-activated protein kinase-mediated electrophile response element/nuclear factor erythroid 2-related factor 2 signaling. Am J Respir Cell Mol Biol 2006;34:174-181.
26. Ghilarducci DP, Tjeerdema RS. Fate and effects of acrolein. Rev Environ Contam Toxicol 1995;144:95-146.
27. Uchida K, Kanematsu M, Morimitsu Y, Osawa T, Noguchi N, Niki E. Acrolein is a product of lipid peroxidation reaction: formation of free acrolein and its conjugate with lysine residues in oxidized low density lipoproteins. J Biol Chem 1998;273:16058-16066.
28. Uchida K, Kanematsu M, Sakai K, Matsuda T, Hattori N, Mizuno Y, Suzuki D, Miyata T, Noguchi N, Niki E, et al. Protein-bound acrolein: potential markers for oxidative stress. Proc Natl Acad Sci USA 1998;95:4882-4887.
29. Calingasan NY, Uchida K, Gibson GE. Protein-bound acrolein: a novel marker of oxidative stress in Alzheimer's disease. J Neurochem 1999;72:751-756.
30. Kehrer JP, Biswal SS. The molecular effects of acrolein. Toxicol Sci 2000;57:6-15.
31. Harper R, Wu K, Chang MM, Yoneda K, Pan R, Reddy SP, Wu R. Activation of nuclear factor-kappa b transcriptional activity in airway epithelial cells by thioredoxin but not by N-acetyl-cysteine and glutathione. Am J Respir Cell Mol Biol 2001;25:178-185.
32. Zhang H, Dickinson DA, Liu RM, Forman HJ. 4-Hydroxynonenal increases gamma-glutamyl transpeptidase gene expression through mitogen-activated protein kinase pathways. Free Radic Biol Med 2005;38:463-471.
33. Dickinson DA, Iles KE, Watanabe N, Iwamoto T, Zhang H, Krzywanski DM, Forman HJ. 4-hydroxynonenal induces glutamate cysteine ligase through JNK in HBE1 cells. Free Radic Biol Med 2002;33:974.
34. Kronke G, Bochkov VN, Huber J, Gruber F, Bluml S, Furnkranz A, Kadl A, Binder BR, Leitinger N. Oxidized phospholipids induce expression of human heme oxygenase-1 involving activation of cAMP-responsive element-binding protein. J Biol Chem 2003;278:51006-51014.
35. Zhang H, Court N, Forman HJ. Submicromolar concentrations of 4-hydroxynonenal induce glutamate cysteine ligase expression in HBE1 cells. Redox Rep 2007;12:101-106.
36. Wu CC, Hsieh CW, Lai PH, Lin JB, Liu YC, Wung BS. Upregulation of endothelial heme oxygenase-1 expression through the activation of the JNK pathway by sublethal concentrations of acrolein. Toxicol Appl Pharmacol 2006;214:244-252.
37. Li L, Hamilton RF Jr, Taylor DE, Holian A. Acrolein-induced cell death in human alveolar macrophages. Toxicol Appl Pharmacol 1997;145:331-339.
38. Aggeli IK, Gaitanaki C, Beis I. Involvement of JNKs and p38-MAPK/MSK1 pathways in H2O2-induced upregulation of heme oxygenase-1 mRNA in H9c2 cells. Cell Signal 2006;18:1801-1812.
39. Iles KE, Dickinson DA, Wigley AF, Welty NE, Blank V, Forman HJ. HNE increases HO-1 through activation of the ERK pathway in pulmonary epithelial cells. Free Radic Biol Med 2005;39:355-364.
40. McNally SJ, Harrison EM, Ross JA, Garden OJ, Wigmore SJ. Curcumin induces heme oxygenase 1 through generation of reactive oxygen species, p38 activation and phosphatase inhibition. Int J Mol Med 2007;19:165-172.
41. Rushworth SA, Ogborne RM, Charalambos CA, O'Connell MA. Role of protein kinase C delta in curcumin-induced antioxidant response element-mediated gene expression in human monocytes. Biochem Biophys Res Commun 2006;341:1007-1016.
42. Wung BS, Hsu MC, Wu CC, Hsieh CW. Piceatannol upregulates endothelial heme oxygenase-1 expression via novel protein kinase C and tyrosine kinase pathways. Pharmacol Res 2006;53:113-122.
43. Rushworth SA, Chen XL, Mackman N, Ogborne RM, O'Connell MA. Lipopolysaccharide-induced heme oxygenase-1 expression in human monocytic cells is mediated via Nrf2 and protein kinase C. J Immunol 2005;175:4408-4415.
44. Numazawa S, Ishikawa M, Yoshida A, Tanaka S, Yoshida T. A typical protein kinase C mediates activation of NF-E2-related factor 2 in response to oxidative stress. Am J Physiol Cell Physiol 2003;285:C334-C342.
45. Rojo AI, Salina M, Salazar M, Takahashi S, Suske G, Calvo V, de Sagarra MR, Cuadrado A. Regulation of heme oxygenase-1 gene expression through the phosphatidylinositol 3-kinase/PKC-zeta pathway and Sp1. Free Radic Biol Med 2006;41:247-261.
46. Kanashiro CA, Khalil RA. Signal transduction by protein kinase C in mammalian cells. Clin Exp Pharmacol Physiol 1998;25:974-985.
47. Casabona G. Intracellular signal modulation: a pivotal role for protein kinase C. Prog Neuropsychopharmacol Biol Psychiatry 1997;21:407-425.
48. Bain J, McLauchlan H, Elliott M, Cohen P. The specificities of protein kinase inhibitors: an update. Biochem J 2003;371:199-204.
49. Dinkova-Kostova AT, Holtzclaw WD, Cole RN, Itoh K, Wakabayashi N, Katoh Y, Yamamoto M, Talalay P. Direct evidence that sulfhydryl groups of Keap1 are the sensors regulating induction of phase 2 enzymes that protect against carcinogens and oxidants. Proc Natl Acad Sci USA 2002;99:11908-11913.
50. Kang MI, Kobayashi A, Wakabayashi N, Kim SG, Yamamoto M. Scaffolding of Keap1 to the actin cytoskeleton controls the function of Nrf2 as key regulator of cytoprotective phase 2 genes. Proc Natl Acad Sci USA 2004;101:2046-2051.
51. Wakabayashi N, Dinkova-Kostova AT, Holtzclaw WD, Kang MI, Kobayashi A, Yamamoto M, Kensler TW, Talalay P. Protection against electrophile and oxidant stress by induction of the phase 2 response: fate of cysteines of the Keap1 sensor modified by inducers. Proc Natl Acad Sci USA 2004;101:2040-2045.
52. Levonen AL, Landar A, Ramachandran A, Ceaser EK, Dickinson DA, Zanoni G, Morrow JD, Darley-Usmar VM. Cellular mechanisms of redox cell signalling: role of cysteine modification in controlling antioxidant defences in response to electrophilic lipid oxidation products. Biochem J 2004;378:373-382.
53. Katoh Y, Itoh K, Yoshida E, Miyagishi M, Fukamizu A, Yamamoto M. Two domains of Nrf2 cooperatively bind CBP, a CREB binding protein, and synergistically activate transcription. Genes Cells 2001;6:857-868.
54. Shen G, Hebbar V, Nair S, Xu C, Li W, Lin W, Keum YS, Han J, Gallo MA, Kong AN. Regulation of Nrf2 transactivation domain activity: the differential effects of mitogen-activated protein kinase cascades and synergistic stimulatory effect of Raf and CREB-binding protein. J Biol Chem 2004;279:23052- 23060.
55. Xing J, Kornhauser JM, Xia Z, Thiele EA, Greenberg ME. Nerve growth factor activates extracellular signal-regulated kinase and p38 mitogen-activated protein kinase pathways to stimulate CREB serine 133 phosphorylation. Mol Cell Biol 1998;18:1946-1955.
56. Liu YZ, Chrivia JC, Latchman DS. Nerve growth factor up-regulates the transcriptional activity of CBP through activation of the p42/p44(MAPK) cascade. J Biol Chem 1998;273:32400-32407.
57. Ait-Si-Ali S, Carlisi D, Ramirez S, Upegui-Gonzalez LC, Duquet A, Robin P, Rudkin B, Harel-Bellan A, Trouche D. Phosphorylation by p44 MAP Kinase/ERK1 stimulates CBP histone acetyl transferase activity in vitro. Biochem Biophys Res Commun 1999;262:157-162.
58. Liu YZ, Thomas NS, Latchman DS. CBP associates with the p42/p44 MAPK enzymes and is phosphorylated following NGF treatment. Neuroreport 1999;10:1239-1243.
59. See RH, Calvo D, Shi Y, Kawa H, Luke MP, Yuan Z. Stimulation of p300-mediated transcription by the kinase MEKK1. J Biol Chem 2001;276:16310-16317.
60. Gusterson R, Brar B, Faulkes D, Giordano A, Chrivia J, Latchman D. The transcriptional co-activators CBP and p300 are activated via phenylephrine through the p42/p44 MAPK cascade. J Biol Chem 2002;277:2517-2524.
61. Sang N, Stiehl DP, Bohensky J, Leshchinsky I, Srinivas V, Caro J. MAPK signaling up-regulates the activity of hypoxia-inducible factors by its effects on p300. J Biol Chem 2003;278:14013-14019.
62. Chung SW, Chen YH, Perrella MA. Role of Ets-2 in the regulation of heme oxygenase-1 by endotoxin. J Biol Chem 2005;280:4578-4584.