Carnosic Acid Induces Anti-Inflammatory Effects in Paraquat-Treated SH-SY5Y Cells Through a Mechanism Involving a Crosstalk Between the Nrf2/HO-1 Axis and NF-κB

Molecular Neurobiology

Volumn 55, Issue 1, 2018, Pages 890-897

  de Oliveira, Marcos Roberto ^a   de Souza, Izabel Cristina Custódio ^b   Fürstenau, Cristina Ribas ^c  

^a FEDERAL UNIVERSITY OF MATO GROSSO   (Brazil)

^b FEDERAL UNIVERSITY OF PELOTAS   (Brazil)

^c FEDERAL UNIVERSITY OF UBERLÂNDIA   (Brazil)

Author keywords

Anti inflammatory; Antioxidant; Carnosic acid; Heme oxygenase 1; Nrf2; Nuclear factor B

Indexed keywords

ABIETANE DERIVATIVE; ANTIINFLAMMATORY AGENT; CARNOSIC ACID; CYTOKINE; HEME OXYGENASE 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NITRIC OXIDE; PARAQUAT; TRANSCRIPTION FACTOR NRF2;

CELL SURVIVAL; DOWN REGULATION; DRUG EFFECT; GENE KNOCKDOWN; HUMAN; METABOLISM; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANTI-INFLAMMATORY AGENTS; CELL LINE, TUMOR; CELL SURVIVAL; CYTOKINES; DITERPENES, ABIETANE; DOWN-REGULATION; GENE KNOCKDOWN TECHNIQUES; HEME OXYGENASE-1; HUMANS; NF-E2-RELATED FACTOR 2; NF-KAPPA B; NITRIC OXIDE; PARAQUAT; SIGNAL TRANSDUCTION;

EID: 85009274738     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-017-0389-6     Document Type: Article

References (79)

1. de Oliveira MR (2016) The dietary components carnosic acid and carnosol as neuroprotective agents: a mechanistic view. Mol Neurobiol 53:6155–6168. doi:10.1007/s12035-015-9519-1 DOI: 10.1007/s12035-015-9519-1
2. Bahri S, Jameleddine S, Shlyonsky V (2016) Relevance of carnosic acid to the treatment of several health disorders: molecular targets and mechanisms. Biomed Pharmacother 84:569–582. doi:10.1016/j.biopha.2016.09.067 DOI: 10.1016/j.biopha.2016.09.067
3. Maione F, Cantone V, Pace S, Chini MG, Bisio A, Romussi G, Pieretti S, Werz O et al (2016) Anti-inflammatory and analgesic activity of carnosol and carnosic acid in vivo and in vitro and in silico analysis of their target interactions. Br J Pharmacol. doi:10.1111/bph.13545
4. Hayes JD, Dinkova-Kostova AT (2014) The Nrf2 regulatory network provides an interface between redox and intermediary metabolism. Trends Biochem Sci 39:199–218. doi:10.1016/j.tibs.2014.02.002 DOI: 10.1016/j.tibs.2014.02.002
5. Esteras N, Dinkova-Kostova AT, Abramov AY (2016) Nrf2 activation in the treatment of neurodegenerative diseases: a focus on its role in mitochondrial bioenergetics and function. Biol Chem 397:383–400. doi:10.1515/hsz-2015-0295 DOI: 10.1515/hsz-2015-0295
6. Zhang R, Xu M, Wang Y, Xie F, Zhang G, Qin X (2016) Nrf2-a promising therapeutic target for defensing against oxidative stress in stroke. Mol Neurobiol. doi:10.1007/s12035-016-0111-0
7. Lu SC (2013) Glutathione synthesis. Biochim Biophys Acta 1830:3143–3153. doi:10.1016/j.bbagen.2012.09.008 DOI: 10.1016/j.bbagen.2012.09.008
8. Nakagami Y (2016) Nrf2 is an attractive therapeutic target for retinal diseases. Oxidative Med Cell Longev 2016:7469326. doi:10.1155/2016/7469326 DOI: 10.1155/2016/7469326
9. Brown KK, Hampton MB (2011) Biological targets of isothiocyanates. Biochim Biophys Acta 1810:888–894. doi:10.1016/j.bbagen.2011.06.004 DOI: 10.1016/j.bbagen.2011.06.004
10. Bai Y, Wang X, Zhao S, Ma C, Cui J, Zheng Y (2015) Sulforaphane protects against cardiovascular disease via Nrf2 activation. Oxidative Med Cell Longev 2015:407580. doi:10.1155/2015/407580 DOI: 10.1155/2015/407580
11. de Oliveira MR, Nabavi SF, Habtemariam S, Erdogan Orhan I, Daglia M, Nabavi SM (2015) The effects of baicalein and baicalin on mitochondrial function and dynamics: a review. Pharmacol Res 100:296–308. doi:10.1016/j.phrs.2015.08.021 DOI: 10.1016/j.phrs.2015.08.021
12. de Oliveira MR (2016) Phloretin-induced cytoprotective effects on mammalian cells: a mechanistic view and future directions. Biofactors 42:13–40. doi:10.1002/biof.1256
13. de Oliveira MR, Nabavi SF, Manayi A, Daglia M, Hajheydari Z, Nabavi SM (2016) Resveratrol and the mitochondria: from triggering the intrinsic apoptotic pathway to inducing mitochondrial biogenesis, a mechanistic view. Biochim Biophys Acta 1860:727–745. doi:10.1016/j.bbagen.2016.01.017 DOI: 10.1016/j.bbagen.2016.01.017
14. de Oliveira MR (2016) The effects of ellagic acid upon brain cells: a mechanistic view and future directions. Neurochem Res 41:1219–1228. doi:10.1007/s11064-016-1853-9 DOI: 10.1007/s11064-016-1853-9
15. Oliveira MR, Nabavi SF, Daglia M, Rastrelli L, Nabavi SM (2016) Epigallocatechin gallate and mitochondria—a story of life and death. Pharmacol Res 104:70–85. doi:10.1016/j.phrs.2015.12.027 DOI: 10.1016/j.phrs.2015.12.027
16. Gibbs PE, Maines MD (2007) Biliverdin inhibits activation of NF-kappaB: reversal of inhibition by human biliverdin reductase. Int J Cancer 121:2567–2574 DOI: 10.1002/ijc.22978
17. Paine A, Eiz-Vesper B, Blasczyk R, Immenschuh S (2010) Signaling to heme oxygenase-1 and its anti-inflammatory therapeutic potential. Biochem Pharmacol 80:1895–1903. doi:10.1016/j.bcp.2010.07.014 DOI: 10.1016/j.bcp.2010.07.014
18. Gullotta F, di Masi A, Coletta M, Ascenzi P (2012) CO metabolism, sensing, and signaling. Biofactors 38:1–13 DOI: 10.1002/biof.192
19. O’Brien L, Hosick PA, John K, Stec DE, Hinds TD Jr (2015) Biliverdin reductase isozymes in metabolism. Trends Endocrinol Metab 26:212–220. doi:10.1016/j.tem.2015.02.001 DOI: 10.1016/j.tem.2015.02.001
20. Kim HP, Ryter SW, Choi AM (2006) CO as a cellular signaling molecule. Annu Rev Pharmacol Toxicol 46:411–449 DOI: 10.1146/annurev.pharmtox.46.120604.141053
21. Desmard M, Boczkowski J, Poderoso J, Motterlini R (2007) Mitochondrial and cellular heme-dependent proteins as targets for the bioactive function of the heme oxygenase/carbon monoxide system. Antioxid Redox Signal 9:2139–2155 DOI: 10.1089/ars.2007.1803
22. Lukiw WJ, Bazan NG (2000) Neuroinflammatory signaling upregulation in Alzheimer’s disease. Neurochem Res 25:1173–1184 DOI: 10.1023/A:1007627725251
23. Mattson MP (2005) NF-kappaB in the survival and plasticity of neurons. Neurochem Res 30:883–893 DOI: 10.1007/s11064-005-6961-x
24. Lee CH, Jeon YT, Kim SH, Song YS (2007) NF-kappaB as a potential molecular target for cancer therapy. Biofactors 29:19–35 DOI: 10.1002/biof.5520290103
25. Shih RH, Wang CY, Yang CM (2015) NF-kappaB signaling pathways in neurological inflammation: a mini review. Front Mol Neurosci 8:77. doi:10.3389/fnmol.2015.00077 DOI: 10.3389/fnmol.2015.00077
26. Li W, Khor TO, Xu C, Shen G, Jeong WS, Yu S, Kong AN (2008) Activation of Nrf2-antioxidant signaling attenuates NFkappaB-inflammatory response and elicits apoptosis. Biochem Pharmacol 76:1485–1489. doi:10.1016/j.bcp.2008.07.017 DOI: 10.1016/j.bcp.2008.07.017
27. Pan H, Wang H, Wang X, Zhu L, Mao L (2012) The absence of Nrf2 enhances NF-κB-dependent inflammation following scratch injury in mouse primary cultured astrocytes. Mediat Inflamm 2012:217580. doi:10.1155/2012/217580 DOI: 10.1155/2012/217580
28. Cuadrado A, Martín-Moldes Z, Ye J, Lastres-Becker I (2014) Transcription factors NRF2 and NF-κB are coordinated effectors of the Rho family, GTP-binding protein RAC1 during inflammation. J Biol Chem 289:15244–15258. doi:10.1074/jbc.M113.540633 DOI: 10.1074/jbc.M113.540633
29. Ramyaa P, Krishnaswamy R, Padma VV (2014) Quercetin modulates OTA-induced oxidative stress and redox signalling in HepG2 cells—up regulation of Nrf2 expression and down regulation of NF-κB and COX-2. Biochim Biophys Acta 1840:681–692. doi:10.1016/j.bbagen.2013.10.024 DOI: 10.1016/j.bbagen.2013.10.024
30. Li W, Suwanwela NC, Patumraj S (2016) Curcumin by down-regulating NF-kB and elevating Nrf2, reduces brain edema and neurological dysfunction after cerebral I/R. Microvasc Res 106:117–127. doi:10.1016/j.mvr.2015.12.008 DOI: 10.1016/j.mvr.2015.12.008
31. Tak PP, Firestein GS (2001) NF-kappaB: a key role in inflammatory diseases. J Clin Invest 107:7–11 DOI: 10.1172/JCI11830
32. Hoesel B, Schmid JA (2013) The complexity of NF-κB signaling in inflammation and cancer. Mol Cancer 12:86. doi:10.1186/1476-4598-12-86 DOI: 10.1186/1476-4598-12-86
33. Kay E, Scotland RS, Whiteford JR (2014) Toll-like receptors: role in inflammation and therapeutic potential. Biofactors 40:284–294 DOI: 10.1002/biof.1156
34. Aktan F (2004) iNOS-mediated nitric oxide production and its regulation. Life Sci 75:639–653 DOI: 10.1016/j.lfs.2003.10.042
35. Arias-Salvatierra D, Silbergeld EK, Acosta-Saavedra LC, Calderon-Aranda ES (2011) Role of nitric oxide produced by iNOS through NF-κB pathway in migration of cerebellar granule neurons induced by lipopolysaccharide. Cell Signal 23:425–435. doi:10.1016/j.cellsig.2010.10.017 DOI: 10.1016/j.cellsig.2010.10.017
36. Dai Z, Wu Z, Yang Y, Wang J, Satterfield MC, Meininger CJ, Bazer FW, Wu G (2013) Nitric oxide and energy metabolism in mammals. Biofactors 39:383–391 DOI: 10.1002/biof.1099
37. Ridnour LA, Thomas DD, Mancardi D, Espey MG, Miranda KM, Paolocci N, Feelisch M, Fukuto J et al (2004) The chemistry of nitrosative stress induced by nitric oxide and reactive nitrogen oxide species. Putting perspective on stressful biological situations. Biol Chem 385:1–10 DOI: 10.1515/BC.2004.001
38. de Oliveira MR, Peres A, Ferreira GC, Schuck PF, Gama CS, Bosco SM (2016) Carnosic acid protects mitochondria of human neuroblastoma SH-SY5Y cells exposed to paraquat through activation of the Nrf2/HO-1Axis. Mol Neurobiol. doi:10.1007/s12035-016-0100-3
39. Yang W, Tiffany-Castiglioni E, Lee MY, Son IH (2010) Paraquat induces cyclooxygenase-2 (COX-2) implicated toxicity in human neuroblastoma SH-SY5Y cells. Toxicol Lett 199:239–246. doi:10.1016/j.toxlet.2010.09.005 DOI: 10.1016/j.toxlet.2010.09.005
40. Liu MW, Su MX, Zhang W, Wang YQ, Chen M, Wang L, Qian CY (2014) Protective effect of Xuebijing injection on paraquat-induced pulmonary injury via down-regulating the expression of p38 MAPK in rats. BMC Complement Altern Med 14:498. doi:10.1186/1472-6882-14-498 DOI: 10.1186/1472-6882-14-498
41. Han J, Ma D, Zhang M, Yang X, Tan D (2015) Natural antioxidant betanin protects rats from paraquat-induced acute lung injury interstitial pneumonia. Biomed Res Int 2015:608174. doi:10.1155/2015/608174
42. Amirshahrokhi K, Khalili AR (2016) Carvedilol attenuates paraquat-induced lung injury by inhibition of proinflammatory cytokines, chemokine MCP-1, NF-κB activation and oxidative stress mediators. Cytokine 88:144–153. doi:10.1016/j.cyto.2016.09.004 DOI: 10.1016/j.cyto.2016.09.004
43. Miller RL, James-Kracke M, Sun GY, Sun AY (2009) Oxidative and inflammatory pathways in Parkinson’s disease. Neurochem Res 34:55–65. doi:10.1007/s11064-008-9656-2 DOI: 10.1007/s11064-008-9656-2
44. Taylor JM, Main BS, Crack PJ (2013) Neuroinflammation and oxidative stress: co-conspirators in the pathology of Parkinson’s disease. Neurochem Int 62:803–819. doi:10.1016/j.neuint.2012.12.016 DOI: 10.1016/j.neuint.2012.12.016
45. Anderson G, Maes M (2014) Neurodegeneration in Parkinson’s disease: interactions of oxidative stress, tryptophan catabolites and depression with mitochondria and sirtuins. Mol Neurobiol 49:771–783. doi:10.1007/s12035-013-8554-z DOI: 10.1007/s12035-013-8554-z
46. Kumar A, Leinisch F, Kadiiska MB, Corbett J, Mason RP (2016) Formation and implications of alpha-synuclein radical in Maneb- and paraquat-induced models of Parkinson’s disease. Mol Neurobiol 53:2983–2994. doi:10.1007/s12035-015-9179-1 DOI: 10.1007/s12035-015-9179-1
47. Baltazar MT, Dinis-Oliveira RJ, de Lourdes BM, Tsatsakis AM, Duarte JA, Carvalho F (2014) Pesticides exposure as etiological factors of Parkinson’s disease and other neurodegenerative diseases—a mechanistic approach. Toxicol Lett 230:85–103. doi:10.1016/j.toxlet.2014.01.039 DOI: 10.1016/j.toxlet.2014.01.039
48. Khalighi Z, Rahmani A, Cheraghi J, Ahmadi MR, Soleimannejad K, Asadollahi R, Asadollahi K (2016) Perfluorocarbon attenuates inflammatory cytokines, oxidative stress and histopathologic changes in paraquat-induced acute lung injury in rats. Environ Toxicol Pharmacol 42:9–15. doi:10.1016/j.etap.2015.12.002 DOI: 10.1016/j.etap.2015.12.002
49. de Oliveira MR, Ferreira GC, Schuck PF (2016) Protective effect of carnosic acid against paraquat-induced redox impairment and mitochondrial dysfunction in SH-SY5Y cells: role for PI3K/Akt/Nrf2 pathway. Toxicol in Vitro 32:41–54. doi:10.1016/j.tiv.2015.12.005 DOI: 10.1016/j.tiv.2015.12.005
50. Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55–63 DOI: 10.1016/0022-1759(83)90303-4
51. de Oliveira MR, Ferreira GC, Schuck PF, Dal Bosco SM (2015) Role for the PI3K/Akt/Nrf2 signaling pathway in the protective effects of carnosic acid against methylglyoxal-induced neurotoxicity in SH-SY5Y neuroblastoma cells. Chem Biol Interact 242:396–406. doi:10.1016/j.cbi.2015.11.003 DOI: 10.1016/j.cbi.2015.11.003
52. de Oliveira MR, Peres A, Gama CS, Bosco SM (2016) Pinocembrin provides mitochondrial protection by the activation of the Erk1/2-Nrf2 signaling pathway in SH-SY5Y neuroblastoma cells exposed to paraquat. Mol Neurobiol. doi:10.1007/s12035-016-0135-5
53. de Oliveira MR, da Rocha RF, Stertz L, Fries GR, de Oliveira DL, Kapczinski F, Moreira JC (2011) Total and mitochondrial nitrosative stress, decreased brain-derived neurotrophic factor (BDNF) levels and glutamate uptake, and evidence of endoplasmic reticulum stress in the hippocampus of vitamin A-treated rats. Neurochem Res 36:506–517. doi:10.1007/s11064-010-0372-3 DOI: 10.1007/s11064-010-0372-3
54. de Oliveira MR, Lorenzi R, Schnorr CE, Morrone M, Moreira JC (2011) Increased 3-nitrotyrosine levels in mitochondrial membranes and impaired respiratory chain activity in brain regions of adult female rats submitted to daily vitamin a supplementation for 2 months. Brain Res Bull 86:246–253. doi:10.1016/j.brainresbull.2011.08.006 DOI: 10.1016/j.brainresbull.2011.08.006
55. de Oliveira MR, da Rocha RF, Pasquali MA, Moreira JC (2012) The effects of vitamin a supplementation for 3 months on adult rat nigrostriatal axis: increased monoamine oxidase enzyme activity, mitochondrial redox dysfunction, increased β-amyloid(1-40) peptide and TNF-α contents, and susceptibility of mitochondria to an in vitro H2O2 challenge. Brain Res Bull 87:432–444. doi:10.1016/j.brainresbull.2012.01.005 DOI: 10.1016/j.brainresbull.2012.01.005
56. de Oliveira MR, Schuck PF, Bosco SM (2016) Tanshinone I induces mitochondrial protection through an Nrf2-dependent mechanism in paraquat-treated human neuroblastoma SH-SY5Y cells. Mol Neurobiol. doi:10.1007/s12035-016-0009-x
57. Satoh T, Kosaka K, Itoh K, Kobayashi A, Yamamoto M, Shimojo Y, Kitajima C, Cui J et al (2008) Carnosic acid, a catechol-type electrophilic compound, protects neurons both in vitro and in vivo through activation of the Keap1/Nrf2 pathway via S-alkylation of targeted cysteines on Keap1. J Neurochem 104:1116–1131 DOI: 10.1111/j.1471-4159.2007.05039.x
58. Morris G, Anderson G, Dean O, Berk M, Galecki P, Martin-Subero M, Maes M (2014) The glutathione system: a new drug target in neuroimmune disorders. Mol Neurobiol 50:1059–1084. doi:10.1007/s12035-014-8705-x DOI: 10.1007/s12035-014-8705-x
59. Denzer I, Münch G, Friedland K (2016) Modulation of mitochondrial dysfunction in neurodegenerative diseases via activation of nuclear factor erythroid-2-related factor 2 by food-derived compounds. Pharmacol Res 103:80–94. doi:10.1016/j.phrs.2015.11.019 DOI: 10.1016/j.phrs.2015.11.019
60. de Oliveira MR, Nabavi SM, Braidy N, Setzer WN, Ahmed T, Nabavi SF (2016) Quercetin and the mitochondria: a mechanistic view. Biotechnol Adv 34:532–549. doi:10.1016/j.biotechadv.2015.12.014 DOI: 10.1016/j.biotechadv.2015.12.014
61. Oh J, Yu T, Choi SJ, Yang Y, Baek HS, An SA, Kwon LK et al (2012) Syk/Src pathway-targeted inhibition of skin inflammatory responses by carnosic acid. Mediat Inflamm 2012:781375. doi:10.1155/2012/781375 DOI: 10.1155/2012/781375
62. Schwager J, Richard N, Fowler A, Seifert N, Raederstorff D (2016) Carnosol and related substances modulate chemokine and cytokine production in macrophages and chondrocytes. Molecules 21:465. doi:10.3390/molecules21040465 DOI: 10.3390/molecules21040465
63. Heinecke LF, Grzanna MW, Au AY, Mochal CA, Rashmir-Raven A, Frondoza CG (2010) Inhibition of cyclooxygenase-2 expression and prostaglandin E2 production in chondrocytes by avocado soybean unsaponifiables and epigallocatechin gallate. Osteoarthr Cartil 18:220–227. doi:10.1016/j.joca.2009.08.015 DOI: 10.1016/j.joca.2009.08.015
64. Luo C, Urgard E, Vooder T, Metspalu A (2011) The role of COX-2 and Nrf2/ARE in anti-inflammation and antioxidative stress: aging and anti-aging. Med Hypotheses 77:174–178. doi:10.1016/j.mehy.2011.04.002 DOI: 10.1016/j.mehy.2011.04.002
65. Nørregaard R, Kwon TH, Frøkiær J (2015) Physiology and pathophysiology of cyclooxygenase-2 and prostaglandin E2 in the kidney. Kidney Res Clin Pract 34:194–200. doi:10.1016/j.krcp.2015.10.004 DOI: 10.1016/j.krcp.2015.10.004
66. Qin WS, Deng YH, Cui FC (2016) Sulforaphane protects against acrolein-induced oxidative stress and inflammatory responses: modulation of Nrf-2 and COX-2 expression. Arch Med Sci 12:871–880. doi:10.5114/aoms.2016.59919 DOI: 10.5114/aoms.2016.59919
67. Davalli P, Mitic T, Caporali A, Lauriola A, D’Arca D (2016) ROS, cell senescence, and novel molecular mechanisms in aging and age-related diseases. Oxidative Med Cell Longev 2016:3565127. doi:10.1155/2016/3565127 DOI: 10.1155/2016/3565127
68. Morris G, Berk M, Klein H, Walder K, Galecki P, Maes M (2016) Nitrosative stress, hypernitrosylation, and autoimmune responses to nitrosylated proteins: new pathways in neuroprogressive disorders including depression and chronic fatigue syndrome. Mol Neurobiol. doi:10.1007/s12035-016-9975-2
69. Rehman MU, Tahir M, Khan AQ, Khan R, Lateef A, Oday-O-Hamiza QW, Ali F, Sultana S (2013) Chrysin suppresses renal carcinogenesis via amelioration of hyperproliferation, oxidative stress and inflammation: plausible role of NF-κB. Toxicol Lett 216:146–158. doi:10.1016/j.toxlet.2012.11.013 DOI: 10.1016/j.toxlet.2012.11.013
70. Sharma N, Nehru B (2015) Characterization of the lipopolysaccharide induced model of Parkinson’s disease: role of oxidative stress and neuroinflammation. Neurochem Int 87:92–105. doi:10.1016/j.neuint.2015.06.004 DOI: 10.1016/j.neuint.2015.06.004
71. Bhattacharjee N, Borah A (2016) Oxidative stress and mitochondrial dysfunction are the underlying events of dopaminergic neurodegeneration in homocysteine rat model of Parkinson’s disease. Neurochem Int 101:48–55. doi:10.1016/j.neuint.2016.10.001 DOI: 10.1016/j.neuint.2016.10.001
72. Niranjan R (2014) The role of inflammatory and oxidative stress mechanisms in the pathogenesis of Parkinson’s disease: focus on astrocytes. Mol Neurobiol 49:28–38. doi:10.1007/s12035-013-8483-x DOI: 10.1007/s12035-013-8483-x
73. Ljubisavljevic S, Stojanovic I (2015) Neuroinflammation and demyelination from the point of nitrosative stress as a new target for neuroprotection. Rev Neurosci 26:49–73. doi:10.1515/revneuro-2014-0060 DOI: 10.1515/revneuro-2014-0060
74. Ljubisavljevic S (2016) Oxidative stress and neurobiology of demyelination. Mol Neurobiol 53:744–758. doi:10.1007/s12035-014-9041-x DOI: 10.1007/s12035-014-9041-x
75. Hulsmans M, Holvoet P (2010) The vicious circle between oxidative stress and inflammation in atherosclerosis. J Cell Mol Med 14:70–78. doi:10.1111/j.1582-4934.2009.00978.x DOI: 10.1111/j.1582-4934.2009.00978.x
76. Wu JJ, Zhu YT, Hu YM (2016) Mechanism of feedback regulation of neutrophil inflammation in Henoch-Schönlein purpura. Eur Rev Med Pharmacol Sci 20:4277–4285
77. Li H, Sun JJ, Chen GY, Wang WW, Xie ZT, Tang GF, Wei SD (2016) Carnosic acid nanoparticles suppress liver ischemia/reperfusion injury by inhibition of ROS, caspases and NF-κB signaling pathway in mice. Biomed Pharmacother 82:237–246. doi:10.1016/j.biopha.2016.04.064 DOI: 10.1016/j.biopha.2016.04.064
78. Foresti R, Bains SK, Pitchumony TS, de Castro Brás LE, Drago F, Dubois-Randé JL, Bucolo C, Motterlini R (2013) Small molecule activators of the Nrf2-HO-1 antioxidant axis modulate heme metabolism and inflammation in BV2 microglia cells. Pharmacol Res 76:132–148. doi:10.1016/j.phrs.2013.07.010 DOI: 10.1016/j.phrs.2013.07.010
79. Tsai CW, Liu KL, Lin YR, Kuo WC (2014) The mechanisms of carnosic acid attenuates tumor necrosis factor-α-mediated inflammation and insulin resistance in 3 T3-L1 adipocytes. Mol Nutr Food Res 58:654–664. doi:10.1002/mnfr.201300356 DOI: 10.1002/mnfr.201300356