Login Register Cart 0
Generic placeholder image

Current Chemical Biology

Editor-in-Chief

ISSN (Print): 2212-7968
ISSN (Online): 1872-3136

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Review Article

Natural Compounds as Heme Oxygenase-1 Inducers to Reduce the Deleterious Consequences Following SARS-CoV-2 Infection

Author(s): Valeria Sorrenti*, Valeria Consoli , Salvo Grosso S. and Luca Vanella

Volume 15, Issue 3, 2021

Published on: 11 October, 2021

Page: [205 - 214] Pages: 10

DOI: 10.2174/2212796815666211011142101

Price: $65

Open Access Journals Promotions 2
conference banner
Abstract

The virus SARS-CoV-2 (Severe acute respiratory syndrome coronavirus 2) causes COVID 19 (CoronaVIrus Disease 19), a global pandemic with multi-organ failure, resulting in high morbidity and mortality. Some individuals are more vulnerable than others and have deleterious consequences following covid- 19. It has been postulated that Heme oxygenase-1 (HO-1) reduction and free heme may contribute to many of the inflammatory phenomena observed in COVID-19 patients. Therefore, HO-1 inducers could prove to be potential therapeutic or preventive agents for COVID 19. Many of the natural compounds present in fruits and vegetables, such as polyphenols, were able to induce HO-1. The aim of this review is to focus on the main foods containing bioactive compounds able to induce HO-1 for an informed choice of foods to use to counteract damage from SARS-CoV-2 infection.

Keywords: SARS-CoV-2, heme oxygenase-1, heme oxygenase-1 inducers, oxidative stress, natural compounds, food.

« Previous Next »
Graphical Abstract

[1]
Renu K, Prasanna PL, Valsala Gopalakrishnan A. Coronaviruses pathogenesis, comorbidities and multi-organ damage - A review. Life Sci 2020; 255: 117839.
[http://dx.doi.org/10.1016/j.lfs.2020.117839] [PMID: 32450165]
[2]
Dömling A, Gao L. Chemistry and biology of SARS-CoV-2. Chem 2020; 6(6): 1283-95.
[http://dx.doi.org/10.1016/j.chempr.2020.04.023] [PMID: 32529116]
[3]
Sungnak W, Huang N, Bécavin C, et al. SARS-CoV-2 entry factors are highly expressed in nasal epithelial cells together with innate immune genes. Nat Med 2020; 26(5): 681-7.
[http://dx.doi.org/10.1038/s41591-020-0868-6] [PMID: 32327758]
[4]
Zou X, Chen K, Zou J, Han P, Hao J, Han Z. Single-cell RNA-seq data analysis on the receptor ACE2 expression reveals the potential risk of different human organs vulnerable to 2019-nCoV infection. Front Med 2020; 14(2): 185-92.
[http://dx.doi.org/10.1007/s11684-020-0754-0] [PMID: 32170560]
[5]
Shang J, Wan Y, Luo C, et al. Cell entry mechanisms of SARS-CoV-2. Proc Natl Acad Sci USA 2020; 117(21): 11727-34.
[http://dx.doi.org/10.1073/pnas.2003138117] [PMID: 32376634]
[6]
Guan WJ, Ni ZY, Hu Y, et al. Clinical characteristics of coronavirus disease 2019 in China. N Engl J Med 2020; 382(18): 1708-20.
[http://dx.doi.org/10.1056/NEJMoa2002032] [PMID: 32109013]
[7]
Hooper PL. COVID-19 and heme oxygenase: Novel insight into the disease and potential therapies. Cell Stress Chaperones 2020; 25(5): 707-10.
[http://dx.doi.org/10.1007/s12192-020-01126-9] [PMID: 32500379]
[8]
Su WL, Lin CP, Hang HC, Wu PS, Cheng CF, Chao YC. Desaturation and heme elevation during COVID-19 infection: A potential prognostic factor of heme oxygenase-1. J Microbiol Immunol Infect 2021; 54(1): 113-6.
[http://dx.doi.org/10.1016/j.jmii.2020.10.001] [PMID: 33176981]
[9]
Arutyunov GP, Koziolova NA, Tarlovskaya EI, et al. The agreed experts’ position of the Eurasian Association of therapists on some new mechanisms of COVID-19 pathways: focus on hemostasis, hemotransfusion issues and blood gas exchange. Kardiologiia 2020; 60(5): 9-19.
[http://dx.doi.org/10.18087/cardio.2020.5.n1132] [PMID: 32515699]
[10]
Wagener FADTG, Pickkers P, Peterson SJ, Immenschuh S, Abraham NG. Targeting the heme-heme oxygenase system to prevent severe complications following COVID-19 infections. Antioxidants 2020; 9(6): E540.
[http://dx.doi.org/10.3390/antiox9060540] [PMID: 32575554]
[11]
Singh D, Wasan H, Reeta KH. Heme oxygenase-1 modulation: A potential therapeutic target for COVID-19 and associated complications. Free Radic Biol Med 2020; 161: 263-71.
[http://dx.doi.org/10.1016/j.freeradbiomed.2020.10.016] [PMID: 33091573]
[12]
Yoshida T, Migita CT. Mechanism of heme degradation by heme oxygenase. J Inorg Biochem 2000; 82(1-4): 33-41.
[http://dx.doi.org/10.1016/S0162-0134(00)00156-2] [PMID: 11132636]
[13]
Maines MD. The heme oxygenase system: past, present, and future. Antioxid Redox Signal 2004; 6(5): 797-801.
[http://dx.doi.org/10.1089/ars.2004.6.797] [PMID: 15345138]
[14]
Funes SC, Rios M, Fernández-Fierro A, et al. Naturally derived heme-oxygenase 1 inducers and their therapeutic application to immune-mediated diseases. Front Immunol 2020; 11: 1467.
[http://dx.doi.org/10.3389/fimmu.2020.01467] [PMID: 32849503]
[15]
Ayer A, Zarjou A, Agarwal A, Stocker R. Heme oxygenases in cardiovascular health and disease. Physiol Rev 2016; 96(4): 1449-508.
[http://dx.doi.org/10.1152/physrev.00003.2016] [PMID: 27604527]
[16]
Bereczki D Jr, Balla J, Bereczki D. Heme oxygenase-1: Clinical relevance in ischemic stroke. Curr Pharm Des 2018; 24(20): 2229-35.
[http://dx.doi.org/10.2174/1381612824666180717101104] [PMID: 30014798]
[17]
Haines DD, Trushin MV, Rose S, Bernard IAS, Mahmoud FF. Parkinson’s disease: Alpha synuclein, heme oxygenase and biotherapeutic countermeasures. Curr Pharm Des 2018; 24(20): 2317-21.
[http://dx.doi.org/10.2174/1381612824666180717161338] [PMID: 30019639]
[18]
Li S, Fujino M, Takahara T, Li XK. Protective role of heme oxygenase-1 in fatty liver ischemia-reperfusion injury. Med Mol Morphol 2019; 52(2): 61-72.
[http://dx.doi.org/10.1007/s00795-018-0205-z] [PMID: 30171344]
[19]
Farsalinos K, Niaura R, Le Houezec J, et al. Editorial: Nicotine and SARS-CoV-2: COVID-19 may be a disease of the nicotinic cholinergic system. Toxicol Rep 2020; 7: 658-63.
[http://dx.doi.org/10.1016/j.toxrep.2020.04.012] [PMID: 32355638]
[20]
Dolinay T, Choi AM, Ryter SW. Heme Oxygenase-1/CO as protective mediators in cigarette smoke- induced lung cell injury and chronic obstructive pulmonary disease. Curr Pharm Biotechnol 2012; 13(6): 769-76.
[http://dx.doi.org/10.2174/138920112800399338] [PMID: 22201606]
[21]
Pechlaner R, Willeit P, Summerer M, et al. Heme oxygenase-1 gene promoter microsatellite polymorphism is associated with progressive atherosclerosis and incident cardiovascular disease. Arterioscler Thromb Vasc Biol 2015; 35(1): 229-36.
[http://dx.doi.org/10.1161/ATVBAHA.114.304729] [PMID: 25359861]
[22]
Yamada N, Yamaya M, Okinaga S, et al. Microsatellite polymorphism in the heme oxygenase-1 gene promoter is associated with susceptibility to emphysema. Am J Hum Genet 2000; 66(1): 187-95.
[http://dx.doi.org/10.1086/302729] [PMID: 10631150]
[23]
Okamoto I, Krögler J, Endler G, et al. A microsatellite polymorphism in the heme oxygenase-1 gene promoter is associated with risk for melanoma. Int J Cancer 2006; 119(6): 1312-5.
[http://dx.doi.org/10.1002/ijc.21937] [PMID: 16596642]
[24]
Hirai H, Kubo H, Yamaya M, et al. Microsatellite polymorphism in heme oxygenase-1 gene promoter is associated with susceptibility to oxidant-induced apoptosis in lymphoblastoid cell lines. Blood 2003; 102(5): 1619-21.
[http://dx.doi.org/10.1182/blood-2002-12-3733] [PMID: 12730098]
[25]
Bao W, Song F, Li X, et al. Association between heme oxygenase-1 gene promoter polymorphisms and type 2 diabetes mellitus: A HuGE review and meta-analysis. Am J Epidemiol 2010; 172(6): 631-6.
[http://dx.doi.org/10.1093/aje/kwq162] [PMID: 20682519]
[26]
Guénégou A, Leynaert B, Bénessiano J, et al. Association of lung function decline with the heme oxygenase-1 gene promoter microsatellite polymorphism in a general population sample. Results from the European Community Respiratory Health Survey (ECRHS), France. J Med Genet 2006; 43(8): e43.
[http://dx.doi.org/10.1136/jmg.2005.039743] [PMID: 16882737]
[27]
Alcaraz MJ, Fernández P, Guillén MI. Anti-inflammatory actions of the heme oxygenase-1 pathway. Curr Pharm Des 2003; 9(30): 2541-51.
[http://dx.doi.org/10.2174/1381612033453749] [PMID: 14529552]
[28]
Keum YS, Choi BY. Molecular and chemical regulation of the Keap1-Nrf2 signaling pathway. Molecules 2014; 19(7): 10074-89.
[http://dx.doi.org/10.3390/molecules190710074] [PMID: 25014534]
[29]
Battino M, Giampieri F, Pistollato F, et al. Nrf2 as regulator of innate immunity: A molecular Swiss army knife! Biotechnol Adv 2018; 36(2): 358-70.
[http://dx.doi.org/10.1016/j.biotechadv.2017.12.012] [PMID: 29277308]
[30]
Davies TG, Wixted WE, Coyle JE, et al. Monoacidic inhibitors of the Kelch-like ECH-Associated Protein 1: Nuclear Factor Erythroid 2-Related Factor 2 (KEAP1:NRF2) protein-protein interaction with high cell potency identified by fragment-based discovery. J Med Chem 2016; 59(8): 3991-4006.
[http://dx.doi.org/10.1021/acs.jmedchem.6b00228] [PMID: 27031670]
[31]
Huerta C, Jiang X, Trevino I, et al. Characterization of novel small-molecule NRF2 activators: Structural and biochemical validation of stereospecific KEAP1 binding. Biochim Biophys Acta 2016; 1860(11 Pt A): 2537-52.
[http://dx.doi.org/10.1016/j.bbagen.2016.07.026] [PMID: 27474998]
[32]
Scapagnini G, Foresti R, Calabrese V, Giuffrida Stella AM, Green CJ, Motterlini R. Caffeic acid phenethyl ester and curcumin: A novel class of heme oxygenase-1 inducers. Mol Pharmacol 2002; 61(3): 554-61.
[http://dx.doi.org/10.1124/mol.61.3.554] [PMID: 11854435]
[33]
Pittala V, Vanella L, Salerno L, et al. Novel Caffeic acid phenethyl ester (Cape) analogues as inducers of heme oxygenase-1. Curr Pharm Des 2017; 23(18): 2657-64.
[http://dx.doi.org/10.2174/1381612823666170210151411] [PMID: 28190391]
[34]
Pittala V, Vanella L, Salerno L, et al. Effects of polyphenolic derivatives on heme oxygenase-system in metabolic dysfunctions. Curr Med Chem 2018; 25(13): 1577-95.
[http://dx.doi.org/10.2174/0929867324666170616110748] [PMID: 28618991]
[35]
Kim J, Oh J, Averilla JN, Kim HJ, Kim JS, Kim JS. Grape peel extract and resveratrol inhibit wrinkle formation in mice model through activation of Nrf2/HO-1 signaling pathway. J Food Sci 2019; 84(6): 1600-8.
[http://dx.doi.org/10.1111/1750-3841.14643] [PMID: 31132143]
[36]
Iddir M, Brito A, Dingeo G, et al. Strengthening the immune system and reducing inflammation and oxidative stress through diet and nutrition: Considerations during the COVID-19 crisis. Nutrients 2020; 12(6): E1562.
[http://dx.doi.org/10.3390/nu12061562] [PMID: 32471251]
[37]
Kaluza J, Harris HR, Linden A, Wolk A. Long-term consumption of fruits and vegetables and risk of chronic obstructive pulmonary disease: A prospective cohort study of women. Int J Epidemiol 2018; 47(6): 1897-909.
[http://dx.doi.org/10.1093/ije/dyy178] [PMID: 30239739]
[38]
Holt EM, Steffen LM, Moran A, et al. Fruit and vegetable consumption and its relation to markers of inflammation and oxidative stress in adolescents. J Am Diet Assoc 2009; 109(3): 414-21.
[http://dx.doi.org/10.1016/j.jada.2008.11.036] [PMID: 19248856]
[39]
Serino A, Salazar G. Protective role of polyphenols against vascular inflammation, aging and cardiovascular disease. Nutrients 2018; 11(1): E53.
[http://dx.doi.org/10.3390/nu11010053] [PMID: 30597847]
[40]
Lichota A, Gwozdzinski L, Gwozdzinski K. Therapeutic potential of natural compounds in inflammation and chronic venous insufficiency. Eur J Med Chem 2019; 176: 68-91.
[http://dx.doi.org/10.1016/j.ejmech.2019.04.075] [PMID: 31096120]
[41]
Kang NJ, Shin SH, Lee HJ, Lee KW. Polyphenols as small molecular inhibitors of signaling cascades in carcinogenesis. Pharmacol Ther 2011; 130(3): 310-24.
[http://dx.doi.org/10.1016/j.pharmthera.2011.02.004] [PMID: 21356239]
[42]
Ferrándiz ML, Devesa I. Inducers of heme oxygenase-1. Curr Pharm Des 2008; 14(5): 473-86.
[http://dx.doi.org/10.2174/138161208783597399] [PMID: 18289074]
[43]
Hahn D, Shin SH, Bae JS. Natural antioxidant and anti-inflammatory compounds in foodstuff or medicinal herbs inducing heme oxygenase-1 expression. Antioxidants 2020; 9(12): E1191.
[http://dx.doi.org/10.3390/antiox9121191] [PMID: 33260980]
[44]
Amorini AM, Fazzina G, Lazzarino G, et al. Activity and mechanism of the antioxidant properties of cyanidin-3-O-beta-glucopyranoside. Free Radic Res 2001; 35(6): 953-66.
[http://dx.doi.org/10.1080/10715760100301451] [PMID: 11811546]
[45]
Lee HS. Characterization of major anthocyanins and the color of red-fleshed Budd Blood orange (Citrus sinensis). J Agric Food Chem 2002; 50(5): 1243-6.
[http://dx.doi.org/10.1021/jf011205+] [PMID: 11853511]
[46]
Tsuda T, Horio F, Uchida K, Aoki H, Osawa T. Dietary cyanidin 3-O-beta-D-glucoside-rich purple corn color prevents obesity and ameliorates hyperglycemia in mice. J Nutr 2003; 133(7): 2125-30.
[http://dx.doi.org/10.1093/jn/133.7.2125] [PMID: 12840166]
[47]
Serraino I, Dugo L, Dugo P, et al. Protective effects of cyanidin-3-O-glucoside from blackberry extract against peroxynitrite-induced endothelial dysfunction and vascular failure. Life Sci 2003; 73(9): 1097-114.
[http://dx.doi.org/10.1016/S0024-3205(03)00356-4] [PMID: 12818719]
[48]
Tsuda T, Horio F, Osawa T. Cyanidin 3-O-beta-D-glucoside suppresses nitric oxide production during a zymosan treatment in rats. J Nutr Sci Vitaminol (Tokyo) 2002; 48(4): 305-10.
[http://dx.doi.org/10.3177/jnsv.48.305] [PMID: 12489822]
[49]
Cao G, Muccitelli HU, Sánchez-Moreno C, Prior RL. Anthocyanins are absorbed in glycated forms in elderly women: A pharmacokinetic study. Am J Clin Nutr 2001; 73(5): 920-6.
[http://dx.doi.org/10.1093/ajcn/73.5.920] [PMID: 11333846]
[50]
Matsumoto H, Inaba H, Kishi M, Tominaga S, Hirayama M, Tsuda T. Orally administered delphinidin 3-rutinoside and cyanidin 3-rutinoside are directly absorbed in rats and humans and appear in the blood as the intact forms. J Agric Food Chem 2001; 49(3): 1546-51.
[http://dx.doi.org/10.1021/jf001246q] [PMID: 11312894]
[51]
Sorrenti V, Mazza F, Campisi A, et al. Heme oxygenase induction by cyanidin-3-O-beta-glucoside in cultured human endothelial cells. Mol Nutr Food Res 2007; 51(5): 580-6.
[http://dx.doi.org/10.1002/mnfr.200600204] [PMID: 17440991]
[52]
Sivasinprasasn S, Pantan R, Thummayot S, Tocharus J, Suksamrarn A, Tocharus C. Cyanidin-3-glucoside attenuates angiotensin II-induced oxidative stress and inflammation in vascular endothelial cells. Chem Biol Interact 2016; S0009-2797(16)30510-5.
[http://dx.doi.org/10.1016/j.cbi.2016.10.022] [PMID: 27983965]
[53]
Xu W, Zhang N, Zhang Z, Jing P. Effects of dietary cyanidin-3-diglucoside-5-glucoside complexes with rutin/Mg(II) against H2O2-induced cellular oxidative stress. Food Res Int 2019; 126: 108591.
[http://dx.doi.org/10.1016/j.foodres.2019.108591] [PMID: 31732077]
[54]
Serra D, Almeida LM, Dinis TC. Anti-inflammatory protection afforded by cyanidin-3-glucoside and resveratrol in human intestinal cells via Nrf2 and PPAR-γ: Comparison with 5-aminosalicylic acid. Chem Biol Interact 2016; 260: 102-9.
[http://dx.doi.org/10.1016/j.cbi.2016.11.003] [PMID: 27818126]
[55]
Basu A, Penugonda K. Pomegranate juice: A heart-healthy fruit juice. Nutr Rev 2009; 67(1): 49-56.
[http://dx.doi.org/10.1111/j.1753-4887.2008.00133.x] [PMID: 19146506]
[56]
Mousa HA. Prevention and treatment of influenza, influenza-like illness, and common cold by herbal, complementary, and natural therapies. J Evid Based Complementary Altern Med 2017; 22(1): 166-74.
[http://dx.doi.org/10.1177/2156587216641831] [PMID: 27055821]
[57]
Xu L, He S, Yin P, et al. Punicalagin induces Nrf2 translocation and HO-1 expression via PI3K/Akt, protecting rat intestinal epithelial cells from oxidative stress. Int J Hyperthermia 2016; 32(5): 465-73.
[http://dx.doi.org/10.3109/02656736.2016.1155762] [PMID: 27055862]
[58]
Hseu YC, Chou CW, Senthil Kumar KJ, et al. Ellagic acid protects human keratinocyte (HaCaT) cells against UVA-induced oxidative stress and apoptosis through the upregulation of the HO-1 and Nrf-2 antioxidant genes. Food Chem Toxicol 2012; 50(5): 1245-55.
[http://dx.doi.org/10.1016/j.fct.2012.02.020] [PMID: 22386815]
[59]
Raffaele M, Greish K, Vanella L, Carota G, Bahman F, Bindayna KM, et al. Potential health benefits of a pomegranate extract, rich in phenolic compounds, in Intestinal Inflammation. accepted- in press. Curr Nutr Food Sci 2021.
[http://dx.doi.org/10.2174/1573401317666210222103032]
[60]
Stec DE, Hinds TD Jr. Natural product heme oxygenase inducers as treatment for nonalcoholic fatty liver disease. Int J Mol Sci 2020; 21(24): E9493.
[http://dx.doi.org/10.3390/ijms21249493] [PMID: 33327438]
[61]
Higdon JV, Frei B. Tea catechins and polyphenols: Health effects, metabolism, and antioxidant functions. Crit Rev Food Sci Nutr 2003; 43(1): 89-143.
[http://dx.doi.org/10.1080/10408690390826464] [PMID: 12587987]
[62]
Gao Z, Han Y, Hu Y, et al. Targeting HO-1 by epigallocatechin-3-gallate reduces contrast-induced renal injury via anti-oxidative stress and anti-inflammation pathways. PLoS One 2016; 11(2): e0149032.
[http://dx.doi.org/10.1371/journal.pone.0149032] [PMID: 26866373]
[63]
Pullikotil P, Chen H, Muniyappa R, et al. Epigallocatechin gallate induces expression of heme oxygenase-1 in endothelial cells via p38 MAPK and Nrf-2 that suppresses proinflammatory actions of TNF-α. J Nutr Biochem 2012; 23(9): 1134-45.
[http://dx.doi.org/10.1016/j.jnutbio.2011.06.007] [PMID: 22137262]
[64]
Kakuta Y, Okumi M, Isaka Y, et al. Epigallocatechin-3-gallate protects kidneys from ischemia reperfusion injury by HO-1 upregulation and inhibition of macrophage infiltration. Transpl Int 2011; 24(5): 514-22.
[http://dx.doi.org/10.1111/j.1432-2277.2011.01224.x] [PMID: 21291499]
[65]
Kim Y, Lee J. Effect of (-)-epigallocatechin-3-gallate on anti-inflammatory response via heme oxygenase-1 induction during adipocyte-macrophage interactions. Food Sci Biotechnol 2016; 25(6): 1767-73.
[http://dx.doi.org/10.1007/s10068-016-0269-2] [PMID: 30263473]
[66]
Lestari ML, Indrayanto G. Curcumin. Profiles Drug Subst Excip Relat Methodol 2014; 39: 113-204.
[http://dx.doi.org/10.1016/B978-0-12-800173-8.00003-9] [PMID: 24794906]
[67]
Reddy RC, Vatsala PG, Keshamouni VG, Padmanaban G, Rangarajan PN. Curcumin for malaria therapy. Biochem Biophys Res Commun 2005; 326(2): 472-4.
[http://dx.doi.org/10.1016/j.bbrc.2004.11.051] [PMID: 15582601]
[68]
Mahady GB, Pendland SL, Yun G, Lu ZZ. Turmeric (Curcuma longa) and curcumin inhibit the growth of Helicobacter pylori, a group 1 carcinogen. Anticancer Res 2002; 22(6C): 4179-81.
[PMID: 12553052]
[69]
Xie Z, Wu B, Shen G, Li X, Wu Q. Curcumin alleviates liver oxidative stress in type 1 diabetic rats. Mol Med Rep 2018; 17(1): 103-8.
[http://dx.doi.org/10.3892/mmr.2017.7911] [PMID: 29115468]
[70]
Peng X, Dai C, Liu Q, Li J, Qiu J. Curcumin attenuates on carbon tetrachloride-induced acute liver injury in mice via modulation of the Nrf2/HO-1 and TGF-β1/Smad3 pathway. Molecules 2018; 23(1): E215.
[http://dx.doi.org/10.3390/molecules23010215] [PMID: 29351226]
[71]
Yu Y, Shen Q, Lai Y, et al. Anti-inflammatory effects of curcumin in microglial cells. Front Pharmacol 2018; 9: 386.
[http://dx.doi.org/10.3389/fphar.2018.00386] [PMID: 29731715]
[72]
Chen MH, Lee MY, Chuang JJ, et al. Curcumin inhibits HCV replication by induction of heme oxygenase-1 and suppression of AKT. Int J Mol Med 2012; 30(5): 1021-8.
[http://dx.doi.org/10.3892/ijmm.2012.1096] [PMID: 22922731]
[73]
Fetoni AR, Eramo SL, Paciello F, et al. Curcuma longa (curcumin) decreases in vivo cisplatin-induced ototoxicity through heme oxygenase-1 induction. Otol Neurotol 2014; 35(5): e169-77.
[http://dx.doi.org/10.1097/MAO.0000000000000302] [PMID: 24608370]
[74]
Zheng KM, Zhang J, Zhang CL, Zhang YW, Chen XC. Curcumin inhibits appoptosin-induced apoptosis via upregulating heme oxygenase-1 expression in SH-SY5Y cells. Acta Pharmacol Sin 2015; 36(5): 544-52.
[http://dx.doi.org/10.1038/aps.2014.166] [PMID: 25891083]
[75]
Chen D, Wu C, Qiu YB, et al. Curcumin ameliorates hepatic chronic inflammation induced by bile duct obstruction in mice through the activation of heme oxygenase-1. Int Immunopharmacol 2020; 78: 106054.
[http://dx.doi.org/10.1016/j.intimp.2019.106054] [PMID: 31812069]
[76]
Visioli F, Poli A, Gall C. Antioxidant and other biological activities of phenols from olives and olive oil. Med Res Rev 2002; 22(1): 65-75.
[http://dx.doi.org/10.1002/med.1028] [PMID: 11746176]
[77]
Al-Azzawie HF, Alhamdani MS. Hypoglycemic and antioxidant effect of oleuropein in alloxan-diabetic rabbits. Life Sci 2006; 78(12): 1371-7.
[http://dx.doi.org/10.1016/j.lfs.2005.07.029] [PMID: 16236331]
[78]
Somova LI, Shode FO, Ramnanan P, Nadar A. Antihypertensive, antiatherosclerotic and antioxidant activity of triterpenoids isolated from Olea europaea, subspecies Africana leaves. J Ethnopharmacol 2003; 84(2-3): 299-305.
[http://dx.doi.org/10.1016/S0378-8741(02)00332-X] [PMID: 12648829]
[79]
Omar SH. Oleuropein in olive and its pharmacological effects. Sci Pharm 2010; 78(2): 133-54.
[http://dx.doi.org/10.3797/scipharm.0912-18] [PMID: 21179340]
[80]
Acquaviva R, Di Giacomo C, Sorrenti V, et al. Antiproliferative effect of oleuropein in prostate cell lines. Int J Oncol 2012; 41(1): 31-8.
[http://dx.doi.org/10.3892/ijo.2012.1428] [PMID: 22484302]
[81]
Castejon ML, Sánchez-Hidalgo M, Aparicio-Soto M, et al. Dietary oleuropein and its new acyl-derivate attenuate murine lupus nephritis through HO-1/Nrf2 activation and suppressing JAK/STAT, NF-κB, MAPK and NLRP3 inflammasome signaling pathways. J Nutr Biochem 2019; 74: 108229.
[http://dx.doi.org/10.1016/j.jnutbio.2019.108229] [PMID: 31698204]
[82]
Savouret JF, Quesne M. Resveratrol and cancer: a review. Biomed Pharmacother 2002; 56(2): 84-7.
[http://dx.doi.org/10.1016/S0753-3322(01)00158-5] [PMID: 12000139]
[83]
Orallo F. Comparative studies of the antioxidant effects of cis- and trans-resveratrol. Curr Med Chem 2006; 13(1): 87-98.
[http://dx.doi.org/10.2174/092986706775197962] [PMID: 16457641]
[84]
Berman AY, Motechin RA, Wiesenfeld MY, Holz MK. The therapeutic potential of resveratrol: A review of clinical trials. NPJ Precis Oncol 2017; 1: 35.
[http://dx.doi.org/10.1038/s41698-017-0038-6] [PMID: 28989978]
[85]
Hui Y, Chengyong T, Cheng L, Haixia H, Yuanda Z, Weihua Y. Resveratrol attenuates the cytotoxicity induced by amyloid-β1-42 in PC12 cells by upregulating heme oxygenase-1 via the PI3K/Akt/Nrf2 pathway. Neurochem Res 2018; 43(2): 297-305.
[http://dx.doi.org/10.1007/s11064-017-2421-7] [PMID: 29090409]
[86]
Gu J, Song ZP, Gui DM, Hu W, Chen YG, Zhang DD. Resveratrol attenuates doxorubicin-induced cardiomyocyte apoptosis in lymphoma nude mice by heme oxygenase-1 induction. Cardiovasc Toxicol 2012; 12(4): 341-9.
[http://dx.doi.org/10.1007/s12012-012-9178-7] [PMID: 22763982]
[87]
Juan SH, Cheng TH, Lin HC, Chu YL, Lee WS. Mechanism of concentration-dependent induction of heme oxygenase-1 by resveratrol in human aortic smooth muscle cells. Biochem Pharmacol 2005; 69(1): 41-8.
[http://dx.doi.org/10.1016/j.bcp.2004.09.015] [PMID: 15588712]
[88]
Kim JW, Lim SC, Lee MY, et al. Inhibition of neointimal formation by trans-resveratrol: Role of phosphatidyl inositol 3-kinase-dependent Nrf2 activation in heme oxygenase-1 induction. Mol Nutr Food Res 2010; 54(10): 1497-505.
[http://dx.doi.org/10.1002/mnfr.201000016] [PMID: 20486211]
[89]
Zhuang H, Kim YS, Koehler RC, Doré S. Potential mechanism by which resveratrol, a red wine constituent, protects neurons. Ann N Y Acad Sci 2003; 993: 276-86.
[http://dx.doi.org/10.1111/j.1749-6632.2003.tb07534.x] [PMID: 12853318]
[90]
Lin TK, Chen SD, Chuang YC, et al. Resveratrol partially prevents rotenone-induced neurotoxicity in dopaminergic SH-SY5Y cells through induction of heme oxygenase-1 dependent autophagy. Int J Mol Sci 2014; 15(1): 1625-46.
[http://dx.doi.org/10.3390/ijms15011625] [PMID: 24451142]
[91]
Walle T. Bioavailability of resveratrol. Ann N Y Acad Sci 2011; 1215: 9-15.
[http://dx.doi.org/10.1111/j.1749-6632.2010.05842.x] [PMID: 21261636]
[92]
Santos AC, Pereira I, Pereira-Silva M, et al. Nanotechnology-based formulations for resveratrol delivery: Effects on resveratrol in vivo bioavailability and bioactivity. Colloids Surf B Biointerfaces 2019; 180: 127-40.
[http://dx.doi.org/10.1016/j.colsurfb.2019.04.030] [PMID: 31035056]
[93]
Renaud S, de Lorgeril M. Wine, alcohol, platelets, and the French paradox for coronary heart disease. Lancet 1992; 339(8808): 1523-6.
[http://dx.doi.org/10.1016/0140-6736(92)91277-F] [PMID: 1351198]
[94]
Castaldo S, Capasso F. Propolis, an old remedy used in modern medicine. Fitoterapia 2002; 73(Suppl. 1): S1-6.
[http://dx.doi.org/10.1016/S0367-326X(02)00185-5] [PMID: 12495704]
[95]
Armutcu F, Akyol S, Ustunsoy S, Turan FF. Therapeutic potential of caffeic acid phenethyl ester and its anti-inflammatory and immunomodulatory effects. Exp Ther Med 2015; 9(5): 1582-8.
[http://dx.doi.org/10.3892/etm.2015.2346] [PMID: 26136862]
[96]
Kim H, Kim W, Yum S, et al. Caffeic acid phenethyl ester activation of Nrf2 pathway is enhanced under oxidative state: Structural analysis and potential as a pathologically targeted therapeutic agent in treatment of colonic inflammation. Free Radic Biol Med 2013; 65: 552-62.
[http://dx.doi.org/10.1016/j.freeradbiomed.2013.07.015] [PMID: 23892357]
[97]
Lee Y, Shin DH, Kim JH, et al. Caffeic acid phenethyl ester-mediated Nrf2 activation and IkappaB kinase inhibition are involved in NFkappaB inhibitory effect: Structural analysis for NFkappaB inhibition. Eur J Pharmacol 2010; 643(1): 21-8.
[http://dx.doi.org/10.1016/j.ejphar.2010.06.016] [PMID: 20599928]
[98]
Morroni F, Sita G, Graziosi A, et al. Neuroprotective effect of caffeic acid phenethyl ester in a mouse model of Alzheimer’s disease involves Nrf2/HO-1 pathway. Aging Dis 2018; 9(4): 605-22.
[http://dx.doi.org/10.14336/AD.2017.0903] [PMID: 30090650]
[99]
Sorrenti V, Raffaele M, Vanella L, et al. Protective effects of caffeic acid phenethyl ester (CAPE) and novel cape analogue as inducers of heme oxygenase-1 in streptozotocin-induced type 1 diabetic rats. Int J Mol Sci 2019; 20(10): E2441.
[http://dx.doi.org/10.3390/ijms20102441] [PMID: 31108850]
[100]
Cheng Y, Yang C, Luo D, Li X, Le XC, Rong J. N-propargyl caffeamide skews macrophages towards a resolving M2-like phenotype against myocardial ischemic injury via activating Nrf2/HO-1 pathway and inhibiting NF-κB pathway. Cell Physiol Biochem 2018; 47(6): 2544-57.
[http://dx.doi.org/10.1159/000491651] [PMID: 29996121]
[101]
Kim YM, Kim HJ, Chang KC. Glycyrrhizin reduces HMGB1 secretion in lipopolysaccharide-activated RAW 264.7 cells and endotoxemic mice by p38/Nrf2-dependent induction of HO-1. Int Immunopharmacol 2015; 26(1): 112-8.
[http://dx.doi.org/10.1016/j.intimp.2015.03.014] [PMID: 25812767]
[102]
Mou K, Pan W, Han D, et al. Glycyrrhizin protects human melanocytes from H2O2-induced oxidative damage via the Nrf2-dependent induction of HO-1. Int J Mol Med 2019; 44(1): 253-61.
[http://dx.doi.org/10.3892/ijmm.2019.4200] [PMID: 31115551]
[103]
Sakai-Sugino K, Uematsu J, Kamada M, et al. Glycyrrhizin inhibits human parainfluenza virus type 2 replication by the inhibition of genome RNA, mRNA and protein syntheses. Drug Discov Ther 2017; 11(5): 246-52.
[http://dx.doi.org/10.5582/ddt.2017.01048] [PMID: 29070744]
[104]
Sun ZG, Zhao TT, Lu N, Yang YA, Zhu HL. Research progress of glycyrrhizic acid on antiviral activity. Mini Rev Med Chem 2019; 19(10): 826-32.
[http://dx.doi.org/10.2174/1389557519666190119111125] [PMID: 30659537]
[105]
Michaelis M, Geiler J, Naczk P, et al. Glycyrrhizin exerts antioxidative effects in H5N1 influenza A virus-infected cells and inhibits virus replication and pro-inflammatory gene expression. PLoS One 2011; 6(5): e19705.
[http://dx.doi.org/10.1371/journal.pone.0019705] [PMID: 21611183]
[106]
Bailly C, Vergoten G. Glycyrrhizin: An alternative drug for the treatment of COVID-19 infection and the associated respiratory syndrome? Pharmacol Ther 2020; 214: 107618.
[http://dx.doi.org/10.1016/j.pharmthera.2020.107618] [PMID: 32592716]
[107]
Anand David AV, Arulmoli R, Parasuraman S. Overviews of biological importance of quercetin: A bioactive flavonoid. Pharmacogn Rev 2016; 10(20): 84-9.
[http://dx.doi.org/10.4103/0973-7847.194044] [PMID: 28082789]
[108]
Legault J, Perron T, Mshvildadze V, et al. Antioxidant and anti-inflammatory activities of quercetin 7-O-β-D-glucopyranoside from the leaves of Brasenia schreberi. J Med Food 2011; 14(10): 1127-34.
[http://dx.doi.org/10.1089/jmf.2010.0198] [PMID: 21859349]
[109]
Lin HC, Cheng TH, Chen YC, Juan SH. Mechanism of heme oxygenase-1 gene induction by quercetin in rat aortic smooth muscle cells. Pharmacology 2004; 71(2): 107-12.
[http://dx.doi.org/10.1159/000076947] [PMID: 15118350]
[110]
Chow JM, Shen SC, Huan SK, Lin HY, Chen YC. Quercetin, but not rutin and quercitrin, prevention of H2O2-induced apoptosis via anti-oxidant activity and heme oxygenase 1 gene expression in macrophages. Biochem Pharmacol 2005; 69(12): 1839-51.
[http://dx.doi.org/10.1016/j.bcp.2005.03.017] [PMID: 15876423]
[111]
Yang Y, Zhang X, Xu M, Wu X, Zhao F, Zhao C. Quercetin attenuates collagen-induced arthritis by restoration of Th17/Treg balance and activation of heme oxygenase 1-mediated anti-inflammatory effect. Int Immunopharmacol 2018; 54: 153-62.
[http://dx.doi.org/10.1016/j.intimp.2017.11.013] [PMID: 29149703]
[112]
Guazelli CFS, Staurengo-Ferrari L, Zarpelon AC, et al. Quercetin attenuates zymosan-induced arthritis in mice. Biomed Pharmacother 2018; 102: 175-84.
[http://dx.doi.org/10.1016/j.biopha.2018.03.057] [PMID: 29554596]
[113]
Kim CS, Choi HS, Joe Y, Chung HT, Yu R. Induction of heme oxygenase-1 with dietary quercetin reduces obesity-induced hepatic inflammation through macrophage phenotype switching. Nutr Res Pract 2016; 10(6): 623-8.
[http://dx.doi.org/10.4162/nrp.2016.10.6.623] [PMID: 27909560]
[114]
Kim Y, Kim CS, Joe Y, Chung HT, Ha TY, Yu R. Quercetin reduces tumor necrosis factor alpha-induced muscle atrophy by upregulation of heme oxygenase-1. J Med Food 2018; 21(6): 551-9.
[http://dx.doi.org/10.1089/jmf.2017.4108] [PMID: 29569982]
[115]
Derosa G, Maffioli P, D’Angelo A, Di Pierro F. A role for quercetin in coronavirus disease 2019 (COVID-19). Phytother Res 2021; 35(3): 1230-6.
[http://dx.doi.org/10.1002/ptr.6887] [PMID: 33034398]
[116]
Choi J, Kim TH, Choi TY, Lee MS. Ginseng for health care: A systematic review of randomized controlled trials in Korean literature. PLoS One 2013; 8(4): e59978.
[http://dx.doi.org/10.1371/journal.pone.0059978] [PMID: 23560064]
[117]
Ellis JM, Reddy P. Effects of Panax ginseng on quality of life. Ann Pharmacother 2002; 36(3): 375-9.
[http://dx.doi.org/10.1345/aph.1A245] [PMID: 11895046]
[118]
Lee DH, Cho HJ, Kang HY, Rhee MH, Park HJ. Total saponin from Korean red ginseng inhibits thromboxane A2 production associated microsomal enzyme activity in platelets. J Ginseng Res 2012; 36(1): 40-6.
[http://dx.doi.org/10.5142/jgr.2012.36.1.40] [PMID: 23717102]
[119]
Seo EY, Kim WK. Red ginseng extract reduced metastasis of colon cancer cells in vitro and in vivo. J Ginseng Res 2011; 35(3): 315-24.
[http://dx.doi.org/10.5142/jgr.2011.35.3.315] [PMID: 23717075]
[120]
Liu CX, Xiao PG. Recent advances on ginseng research in China. J Ethnopharmacol 1992; 36(1): 27-38.
[http://dx.doi.org/10.1016/0378-8741(92)90057-X] [PMID: 1501490]
[121]
Chen RJ, Chung TY, Li FY, Lin NH, Tzen JT. Effect of sugar positions in ginsenosides and their inhibitory potency on Na+/K+-ATPase activity. Acta Pharmacol Sin 2009; 30(1): 61-9.
[http://dx.doi.org/10.1038/aps.2008.6] [PMID: 19060914]
[122]
Hwang YP, Jeong HG. Ginsenoside Rb1 protects against 6-hydroxydopamine-induced oxidative stress by increasing heme oxygenase-1 expression through an estrogen receptor-related PI3K/Akt/Nrf2-dependent pathway in human dopaminergic cells. Toxicol Appl Pharmacol 2010; 242(1): 18-28.
[http://dx.doi.org/10.1016/j.taap.2009.09.009] [PMID: 19781563]
[123]
Kim M, Yoon Choi S, Kim K-T, Rhee YK, Hur J. Ginsenoside Rg18 suppresses lipopolysaccharide-induced neuroinflammation in BV2 microglia and amyloid-β-induced oxidative stress in SH-SY5Y neurons via nuclear factor erythroid 2-related factor 2/heme oxygenase-1 induction. J Funct Foods 2017; 31: 71-8.
[124]
Li Q, Xiang Y, Chen Y, Tang Y, Zhang Y. Ginsenoside Rg1 protects cardiomyocytes against hypoxia/reoxygenation injury via activation of Nrf2/HO-1 signaling and inhibition of JNK. Cell Physiol Biochem 2017; 44(1): 21-37.
[http://dx.doi.org/10.1159/000484578] [PMID: 29130959]
[125]
Ning C, Gao X, Wang C, et al. Protective effects of ginsenoside Rg1 against lipopolysaccharide/d-galactosamine-induced acute liver injury in mice through inhibiting toll-like receptor 4 signaling pathway. Int Immunopharmacol 2018; 61: 266-76.
[http://dx.doi.org/10.1016/j.intimp.2018.06.008] [PMID: 29902710]
[126]
Kim SJ, Choi HS, Cho HI, et al. Protective effect of wild ginseng cambial meristematic cells on d-galactosamine-induced hepatotoxicity in rats. J Ginseng Res 2015; 39(4): 376-83.
[http://dx.doi.org/10.1016/j.jgr.2015.04.002] [PMID: 26869831]
[127]
Wang W, Zhang Y, Li H, et al. Protective effects of sesquiterpenoids from the root of Panax ginseng on fulminant liver injury induced by lipopolysaccharide/d-galactosamine. J Agric Food Chem 2018; 66(29): 7758-63.
[http://dx.doi.org/10.1021/acs.jafc.8b02627] [PMID: 29974747]

Rights & Permissions Print Cite
Article Metrics
23
2
1
Wayfinder Image
Open Access Journals Promotions
© 2024 Bentham Science Publishers | Privacy Policy