Arachidonic Acid Induces ARE/Nrf2-Dependent Heme Oxygenase-1 Transcription in Rat Brain Astrocytes

Chih-Chung Lin1, Chien-Chung Yang2, Yu‐Wen Chen3, Li-Der Hsiao1, Chih-Hui Yang4
1Department of Anesthetics, Chang Gung Memorial Hospital at Linkou, and College of Medicine, Chang Gung University, Tao-Yuan, Taiwan
2Department of Traditional Chinese Medicine, Chang Gung Memorial Hospital, Linkou, Kwei-San, Tao-Yuan, Taiwan
3Department of Physiology and Pharmacology and Health Aging Research Center, College of Medicine, Chang Gung University, Tao-Yuan, Taiwan
4Department of Physiology and Pharmacology and Health Aging Research Center, College of Medicine, Chang Gung University, Kwei-San, Tao-Yuan, Taiwan

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Halliwell B (2006) Oxidative stress and neurodegeneration: where are we now? J Neurochem 97(6):1634–1658. doi: 10.1111/j.1471-4159.2006.03907.x

Block K, Ricono JM, Lee DY, Bhandari B, Choudhury GG, Abboud HE, Gorin Y (2006) Arachidonic acid-dependent activation of a p22phox-based NAD(P)H oxidase mediates angiotensin II-induced mesangial cell protein synthesis and fibronectin expression via Akt/PKB. Antioxid Redox Signal 8(9–10):1497–1508. doi: 10.1089/ars.2006.8.1497

Diau GY, Hsieh AT, Sarkadi-Nagy EA, Wijendran V, Nathanielsz PW, Brenna JT (2005) The influence of long chain polyunsaturate supplementation on docosahexaenoic acid and arachidonic acid in baboon neonate central nervous system. BMC Med 3:11. doi: 10.1186/1741-7015-3-11

Uauy R, Dangour AD (2006) Nutrition in brain development and aging: role of essential fatty acids. Nutr Rev 64(5 Pt 2):S24–S33 discussion S72-91

Martin C, Martinez R, Navarro R, Ruiz-Sanz JI, Lacort M, Ruiz-Larrea MB (2001) tert-Butyl hydroperoxide-induced lipid signaling in hepatocytes: involvement of glutathione and free radicals. Biochem Pharmacol 62(6):705–712

Schnellmann RG, Yang X, Carrick JB (1994) Arachidonic acid release in renal proximal tubule cell injuries and death. J Biochem Toxicol 9(4):211–217

Tommasini I, Guidarelli A, Cerioni L, Cantoni O (2004) The arachidonate-dependent cytoprotective signaling evoked by peroxynitrite is a general response of the monocyte/macrophage lineage. Biochem Biophys Res Commun 316(4):1191–1195. doi: 10.1016/j.bbrc.2004.02.172

Palomba L, Cerioni L, Cantoni O (2009) Arachidonic acid: a key molecule for astrocyte survival to peroxynitrite. Glia 57(15):1672–1679. doi: 10.1002/ glia.20879

Ryter SW, Alam J, Choi AM (2006) Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev 86(2):583–650. doi: 10.1152/physrev.00011.2005

Jamal Uddin M, Joe Y, Kim SK, Oh Jeong S, Ryter SW, Pae HO, Chung HT (2016) IRG1 induced by heme oxygenase-1/carbon monoxide inhibits LPS-mediated sepsis and pro-inflammatory cytokine production. Cell Mol Immunol 13(2):170–179. doi: 10.1038/cmi.2015.02

Chi PL, Lin CC, Chen YW, Hsiao LD, Yang CM (2015) CO induces Nrf2-dependent heme oxygenase-1 transcription by cooperating with Sp1 and c-Jun in rat brain astrocytes. Mol Neurobiol 52(1):277–292. doi: 10.1007/s12035-014-8869-4

Itoh K, Mochizuki M, Ishii Y, Ishii T, Shibata T, Kawamoto Y, Kelly V, Sekizawa K et al (2004) Transcription factor Nrf2 regulates inflammation by mediating the effect of 15-deoxy-Δ12,14-prostaglandin J2. Mol Cell Biol 24(1):36–45

Paine A, Eiz-Vesper B, Blasczyk R, Immenschuh S (2010) Signaling to heme oxygenase-1 and its anti-inflammatory therapeutic potential. Biochem Pharmacol 80(12):1895–1903. doi: 10.1016/j.bcp.2010.07.014

Poss KD, Tonegawa S (1997) Reduced stress defense in heme oxygenase 1-deficient cells. Proc Natl Acad Sci U S A 94(20):10925–10930

Chao XD, Ma YH, Luo P, Cao L, Lau WB, Zhao BC, Han F, Liu W et al (2013) Up-regulation of heme oxygenase-1 attenuates brain damage after cerebral ischemia via simultaneous inhibition of superoxide production and preservation of NO bioavailability. Exp Neurol 239:163–169. doi: 10.1016/j.expneurol.2012.09.020

Alexander LD, Ding Y, Alagarsamy S, Cui XL, Douglas JG (2006) Arachidonic acid induces ERK activation via Src SH2 domain association with the epidermal growth factor receptor. Kidney Int 69(10):1823–1832. doi: 10.1038/sj.ki.5000363

Han Z, Varadharaj S, Giedt RJ, Zweier JL, Szeto HH, Alevriadou BR (2009) Mitochondria-derived reactive oxygen species mediate heme oxygenase-1 expression in sheared endothelial cells. J Pharmacol Exp Ther 329(1):94–101. doi: 10.1124/jpet.108.145557

Yang CM, Lin CC, Lee IT, Hsu CK, Tai YC, Hsieh HL, Chi PL, Hsiao LD (2015) c-Src-dependent transactivation of EGFR mediates CORM-2-induced HO-1 expression in human tracheal smooth muscle cells. J Cell Physiol 230(10):2351–2361. doi: 10.1002/jcp.24912

Schauwienold D, Sastre AP, Genzel N, Schaefer M, Reusch HP (2008) The transactivated epidermal growth factor receptor recruits Pyk2 to regulate Src kinase activity. J Biol Chem 283(41):27748–27756. doi: 10.1074/jbc.M801431200

Elbirt KK, Whitmarsh AJ, Davis RJ, Bonkovsky HL (1998) Mechanism of sodium arsenite-mediated induction of heme oxygenase-1 in hepatoma cells. Role of mitogen-activated protein kinases. J Biol Chem 273(15):8922–8931

Kietzmann T, Samoylenko A, Immenschuh S (2003) Transcriptional regulation of heme oxygenase-1 gene expression by MAP kinases of the JNK and p38 pathways in primary cultures of rat hepatocytes. J Biol Chem 278(20):17927–17936. doi: 10.1074/jbc.M203929200

Lee SH, Lee YJ, Han HJ (2010) Effect of arachidonic acid on hypoxia-induced IL-6 production in mouse ES cells: involvement of MAPKs, NF-κB, and HIF-1α. J Cell Physiol 222(3):574–585. doi: 10.1002/jcp.21973

Martin D, Rojo AI, Salinas M, Diaz R, Gallardo G, Alam J, De Galarreta CM, Cuadrado A (2004) 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(10):8919–8929. doi: 10.1074/jbc.M309660200

Salinas M, Diaz R, Abraham NG, Ruiz de Galarreta CM, Cuadrado A (2003) Nerve growth factor protects against 6-hydroxydopamine-induced oxidative stress by increasing expression of heme oxygenase-1 in a phosphatidylinositol 3-kinase-dependent manner. J Biol Chem 278(16):13898–13904. doi: 10.1074/jbc.M209164200

Jaiswal AK (2004) Nrf2 signaling in coordinated activation of antioxidant gene expression. Free Radic Biol Med 36(10):1199–1207. doi: 10.1016/j.freeradbiomed.2004.02.074

Bianchi A, Moulin D, Hupont S, Koufany M, Netter P, Reboul P, Jouzeau JY (2014) Oxidative stress-induced expression of HSP70 contributes to the inhibitory effect of 15d-PGJ2 on inducible prostaglandin pathway in chondrocytes. Free Radic Biol Med 76:114–126. doi: 10.1016/j.freeradbiomed.2014.07.028

Jou TC, Jou MJ, Chen JY, Lee SY (1985) Properties of rat brain astrocytes in long-term culture. Taiwan Yi Xue Hui Za Zhi 84(8):865–881

Lin CC, Lee IT, Chi PL, Hsieh HL, Cheng SE, Hsiao LD, Liu CJ, Yang CM (2014) c-Src/Jak2/PDGFR/PKCδ-dependent MMP-9 induction is required for thrombin-stimulated rat brain astrocytes migration. Mol Neurobiol 49(2):658–672. doi: 10.1007/s12035-013-8547-y

Yang CM, Lin CC, Lee IT, Lin YH, Yang CM, Chen WJ, Jou MJ, Hsiao LD (2012) Japanese encephalitis virus induces matrix metalloproteinase-9 expression via a ROS/c-Src/PDGFR/PI3K/Akt/MAPKs-dependent AP-1 pathway in rat brain astrocytes. J Neuroinflammation 9:12. doi: 10.1186/1742-2094-9-12

Kitamura Y, Kakimura J, Matsuoka Y, Nomura Y, Gebicke-Haerter PJ, Taniguchi T (1999) Activators of peroxisome proliferator-activated receptor-γ (PPARγ) inhibit inducible nitric oxide synthase expression but increase heme oxygenase-1 expression in rat glial cells. Neurosci Lett 262(2):129–132

Matono R, Miyano K, Kiyohara T, Sumimoto H (2014) Arachidonic acid induces direct interaction of the p67phox-Rac complex with the phagocyte oxidase Nox2, leading to superoxide production. J Biol Chem 289(36):24874–24884. doi: 10.1074/jbc.M114.581785

Choi AM, Alam J (1996) Heme oxygenase-1: function, regulation, and implication of a novel stress-inducible protein in oxidant-induced lung injury. Am J Respir Cell Mol Biol 15(1):9–19. doi: 10.1165/ajrcmb.15.1.8679227

Chrissobolis S, Faraci FM (2008) The role of oxidative stress and NADPH oxidase in cerebrovascular disease. Trends Mol Med 14(11):495–502. doi: 10.1016/j.molmed.2008.09.003

Lee IT, Yang CM (2012) Role of NADPH oxidase/ROS in pro-inflammatory mediators-induced airway and pulmonary diseases. Biochem Pharmacol 84(5):581–590. doi: 10.1016/j.bcp.2012.05.005

Lipinski CA, Loftus JC (2010) Targeting Pyk2 for therapeutic intervention. Expert Opin Ther Targets 14(1):95–108. doi: 10.1517/14728220903473194

Yeh PY, Li CY, Hsieh CW, Yang YC, Yang PM, Wung BS (2014) CO-releasing molecules and increased heme oxygenase-1 induce protein S-glutathionylation to modulate NF-κB activity in endothelial cells. Free Radic Biol Med 70:1–13. doi: 10.1016/j.freeradbiomed.2014.01.042

Shih RH, Lee IT, Hsieh HL, Kou YR, Yang CM (2010) Cigarette smoke extract induces HO-1 expression in mouse cerebral vascular endothelial cells: involvement of c-Src/NADPH oxidase/PDGFR/JAK2/STAT3 pathway. J Cell Physiol 225(3):741–750. doi: 10.1002/jcp.22270

McCubrey JA, Lahair MM, Franklin RA (2006) Reactive oxygen species-induced activation of the MAP kinase signaling pathways. Antioxid Redox Signal 8(9–10):1775–1789. doi: 10.1089/ars.2006.8.1775

Wagener FA, Volk HD, Willis D, Abraham NG, Soares MP, Adema GJ, Figdor CG (2003) Different faces of the heme-heme oxygenase system in inflammation. Pharmacol Rev 55(3):551–571. doi: 10.1124/pr.55.3.5

Magierowska K, Magierowski M, Hubalewska-Mazgaj M, Adamski J, Surmiak M, Sliwowski Z, Kwiecien S, Brzozowski T (2015) Carbon monoxide (CO) released from tricarbonyldichlororuthenium (II) dimer (CORM-2) in gastroprotection against experimental ethanol-induced gastric damage. PLoS One 10(10):e0140493. doi: 10.1371/journal.pone.0140493

Wegiel B, Hanto DW, Otterbein LE (2013) The social network of carbon monoxide in medicine. Trends Mol Med 19(1):3–11. doi: 10.1016/j.molmed.2012.10.001

Rochette L, Cottin Y, Zeller M, Vergely C (2013) Carbon monoxide: mechanisms of action and potential clinical implications. Pharmacol Ther 137(2):133–152. doi: 10.1016/j.pharmthera.2012.09.007

Kamata H, Hirata H (1999) Redox regulation of cellular signalling. Cell Signal 11(1):1–14

Rahman I, Biswas SK, Kode A (2006) Oxidant and antioxidant balance in the airways and airway diseases. Eur J Pharmacol 533(1–3):222–239. doi: 10.1016/j.ejphar.2005.12.087

Mulier B, Rahman I, Watchorn T, Donaldson K, MacNee W, Jeffery PK (1998) Hydrogen peroxide-induced epithelial injury: the protective role of intracellular nonprotein thiols (NPSH). Eur Respir J 11(2):384–391

Barbieri SS, Cavalca V, Eligini S, Brambilla M, Caiani A, Tremoli E, Colli S (2004) Apocynin prevents cyclooxygenase 2 expression in human monocytes through NADPH oxidase and glutathione redox-dependent mechanisms. Free Radic Biol Med 37(2):156–165. doi: 10.1016/j.freeradbiomed.2004.04.020

Yang CM, Lin CC, Hsieh HL (2017) High-glucose-derived oxidative stress-dependent heme oxygenase-1 expression from astrocytes contributes to the neuronal apoptosis. Mol Neurobiol 54(1):470–483. doi: 10.1007/ s12035-015-9666-4

Cheng SE, Lee IT, Lin CC, Kou YR, Yang CM (2010) Cigarette smoke particle-phase extract induces HO-1 expression in human tracheal smooth muscle cells: role of the c-Src/NADPH oxidase/MAPK/Nrf2 signaling pathway. Free Radic Biol Med 48(10):1410–1422. doi: 10.1016/j.freeradbiomed.2010.02.026

Lee IT, Wang SW, Lee CW, Chang CC, Lin CC, Luo SF, Yang CM (2008) Lipoteichoic acid induces HO-1 expression via the TLR2/MyD88/c-Src/NADPH oxidase pathway and Nrf2 in human tracheal smooth muscle cells. J Immunol 181(7):5098–5110

Benvenisti-Zarom L, Chen-Roetling J, Regan RF (2006) Inhibition of the ERK/MAP kinase pathway attenuates heme oxygenase-1 expression and heme-mediated neuronal injury. Neurosci Lett 398(3):230–234. doi: 10.1016/j.neulet.2006.01.003

Lee IT, Yang CM (2013) Inflammatory signalings involved in airway and pulmonary diseases. Mediat Inflamm 2013:791231. doi: 10.1155/2013/791231

Yuan X, Xu C, Pan Z, Keum YS, Kim JH, Shen G, Yu S, Oo KT et al (2006) Butylated hydroxyanisole regulates ARE-mediated gene expression via Nrf2 coupled with ERK and JNK signaling pathway in HepG2 cells. Mol Carcinog 45(11):841–850. doi: 10.1002/mc.20234

Foresti R, Bani-Hani MG, Motterlini R (2008) Use of carbon monoxide as a therapeutic agent: promises and challenges. Intensive Care Med 34(4):649–658. doi: 10.1007/s00134-008-1011-1

Pawate S, Shen Q, Fan F, Bhat NR (2004) Redox regulation of glial inflammatory response to lipopolysaccharide and interferongamma. Journal Neurosci Res 77(4):540–551. doi: 10.1002/jnr.20180

Reuter S, Gupta SC, Chaturvedi MM, Aggarwal BB (2010) Oxidative stress, inflammation, and cancer: how are they linked? Free Radic Biol Med 49(11):1603–1616. doi: 10.1016/j.freeradbiomed.2010.09.006

Anwar AA, Li FY, Leake DS, Ishii T, Mann GE, Siow RC (2005) 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 39(2):227–236. doi: 10.1016/j.freeradbiomed.2005.03.012

Li MH, Cha YN, Surh YJ (2006) Peroxynitrite induces HO-1 expression via PI3K/Akt-dependent activation of NF-E2-related factor 2 in PC12 cells. Free Radic Biol Med 41(7):1079–1091. doi: 10.1016/j.freeradbiomed.2006.06.010