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Oxidative Medicine and Cellular Longevity
Volume 2013, Article ID 639541, 12 pages
http://dx.doi.org/10.1155/2013/639541
Review Article

Therapeutic Roles of Heme Oxygenase-1 in Metabolic Diseases: Curcumin and Resveratrol Analogues as Possible Inducers of Heme Oxygenase-1

1Department of Anesthesiology and Pain Medicine, Wonkwang University School of Medicine, 460 Iksandae-ro, Iksan 570-749, Republic of Korea
2Department of Biological Science, University of Ulsan, 30 Daehack-ro, Ulsan 680-749, Republic of Korea
3Department of Microbiology and Immunology, Wonkwang University School of Medicine, 460 Iksandae-ro, Iksan 570-749, Republic of Korea

Received 5 June 2013; Revised 4 August 2013; Accepted 12 August 2013

Academic Editor: Joseph Fomusi Ndisang

Copyright © 2013 Yong Son et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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  • Bin Li, Hee-Jin Choi, Dong-Sung Lee, Hyuncheol Oh, Youn-Chul Kim, Jin-Young Moon, Won-Hwan Park, Sun-Dong Park, and Jai-Eun Kim, “ Amomum tsao-ko Suppresses Lipopolysaccharide-Induced Inflammatory Responses in RAW264.7 Macrophages via Nrf2-Dependent Heme Oxygenase-1 Expression ,” The American Journal of Chinese Medicine, pp. 1–16, 2014. View at Publisher · View at Google Scholar
  • Yanmin Song, Lili Long, Ning Zhang, and Yunhai Liu, “Inhibitory effects of hydroxysafflor yellow A on PDGF-BB-induced proliferation and migration of vascular smooth muscle cells via mediating Akt signaling,” Molecular Medicine Reports, vol. 10, no. 3, pp. 1555–1560, 2014. View at Publisher · View at Google Scholar
  • Shereen M. Hamza, and Jason R. B. Dyck, “Systemic and renal oxidative stress in the pathogenesis of hypertension: modulation of long-term control of arterial blood pressure by resveratrol,” Frontiers in Physiology, vol. 5, 2014. View at Publisher · View at Google Scholar
  • R. Domínguez, and J. M. Lorenzo, “Effect of genotype on fatty acid composition of intramuscular and subcutaneous fat of Celta pig breed,” Grasas y Aceites, vol. 65, no. 3, pp. e037, 2014. View at Publisher · View at Google Scholar
  • Jarmila Vojtkova, Peter Durdik, Zuzana Michnova, Tomas Turcan, and Miriam Ciljakova, “Exhaled carbon monoxide in adolescents with diabetic cardiovascular autonomic neuropathy,” Journal of Pediatric Endocrinology & Metabolism, vol. 27, no. 7-8, pp. 709–715, 2014. View at Publisher · View at Google Scholar
  • Joanna Gerszon, Aleksandra Rodacka, and Mieczysław Puchała, “Antioxidant properties of resveratrol and its protective effects in neurodegenerative diseases,” Advances in Cell Biology, vol. 2014, pp. 97–117, 2014. View at Publisher · View at Google Scholar
  • Aamir Khan, Sumit Jamwal, Krishna Reddy V. Bijjem, Atish Prakash, and Puneet Kumar, “Neuroprotective effect of Hemeoxygenase-1/Glycogen Synthase Kinase-3β modulators in 3-Nitropropionic Acid Induced Neurotoxicity in Rats,” Neuroscience, 2014. View at Publisher · View at Google Scholar
  • Yıldız Öner-İyidoğan, Sevda Tanrıkulu-Küçük, Muhammed Seyithanoğlu, Hikmet Koçak, Semra Doğru-Abbasoğlu, A. Fatih Aydın, Şule Beyhan-Özdaş, Hande Yapışlar, and Necla Koçak-Toker, “Effect of curcumin on hepatic heme oxygenase 1 expression in high fat diet fed rats: is there a triangular relationship?,” Canadian Journal of Physiology and Pharmacology, vol. 92, no. 10, pp. 805–812, 2014. View at Publisher · View at Google Scholar
  • Zheng Li, Ya-Na Geng, Jian-Dong Jiang, and Wei-Jia Kong, “Antioxidant and Anti-Inflammatory Activities of Berberine in the Treatment of Diabetes Mellitus,” Evidence-Based Complementary and Alternative Medicine, vol. 2014, pp. 1–12, 2014. View at Publisher · View at Google Scholar
  • Ying-Na Li, Yu Guo, Miao-Miao Xi, Pei Yang, Xue-Ying Zhou, Shuang Yin, Chun-Xu Hai, Jin-Gang Li, and Xu-Jun Qin, “Saponins from Aralia taibaiensis Attenuate D-Galactose-Induced Aging in Rats by Activating FOXO3a and Nrf2 Pathways,” Oxidative Medicine and Cellular Longevity, vol. 2014, pp. 1–13, 2014. View at Publisher · View at Google Scholar
  • Hsin-Ling Yang, Mallikarjuna Korivi, Ming-Wei Lin, Ssu-Ching Chen, Chih-Wei Chou, and You-Cheng Hseu, “Anti-angiogenic Properties of Coenzyme Q0 through Downregulation of MMP-9/NF-κB and Upregulation of HO-1 Signaling in TNF-α-activated Human Endothelial Cells,” Biochemical Pharmacology, 2015. View at Publisher · View at Google Scholar
  • Larissa Daniele Bobermin, Gisele Hansel, Emilene Barros da Silva Scherer, Angela T.S. Wyse, Diogo Onofre Souza, André Quincozes-Santos, and Carlos-Alberto Gonçalves, “Ammonia impairs glutamatergic communication in astroglial cells: Protective role of resveratrol,” Toxicology in Vitro, 2015. View at Publisher · View at Google Scholar
  • Nikolaos Goutzourelas, Demetrios Kouretas, Dimitrios Stagos, Anastasia Housmekeridou, Christina Karapouliou, Efthalia Kerasioti, Nektarios Aligiannis, Alexios L. Skaltsounis, Demetrios A. Spandidos, and Aristidis M. Tsatsakis, “Grape pomace extract exerts antioxidant effects through an increase in GCS levels and GST activity in muscle and endothelial cells,” International Journal of Molecular Medicine, vol. 36, no. 2, pp. 433–441, 2015. View at Publisher · View at Google Scholar
  • Yeonsoo Joe, Min Zheng, Hyo Jeong Kim, Md. Jamal Uddin, Seul-Ki Kim, Yingqing Chen, Jeongmin Park, Gyeong Jae Cho, Stefan W. Ryter, and Hun Taeg Chung, “Cilostazol attenuates murine hepatic ischemia and reperfusion injury via heme oxygenase-dependent activation of mitochondrial biogenesis,” American Journal Of Physiology-Gastrointestinal And Liver Physiology, vol. 309, no. 1, pp. G21–G29, 2015. View at Publisher · View at Google Scholar
  • Mengliu Yang, Masaki Kimura, Choaping Ng, Jingjing He, Sahar Keshvari, Felicity J. Rose, Johanna L. Barclay, and Jonathan P. Whitehead, “Induction of Heme-oxygenase-1 (HO-1) does not enhance adiponectin production in human adipocytes: Evidence against a direct HO-1 – adiponectin axis,” Molecular and Cellular Endocrinology, 2015. View at Publisher · View at Google Scholar
  • Ammad Ahmad Farooqi, Kun-Tzu Li, Sundas Fayyaz, Yung-Ting Chang, Muhammad Ismail, Chih-Chuang Liaw, Shyng-Shiou F. Yuan, Jen-Yang Tang, and Hsueh-Wei Chang, “Anticancer drugs for the modulation of endoplasmic reticulum stress and oxidative stress,” Tumor Biology, 2015. View at Publisher · View at Google Scholar
  • Colin J. Henderson, Amy R. Cameron, Lynsey Chatham, Lesley A. Stanley, and Charles Roland Wolf, “Evidence That the Capacity of Nongenotoxic Carcinogens to Induce Oxidative Stress Is Subject to Marked Variability,” Toxicological Sciences, vol. 145, no. 1, pp. 138–148, 2015. View at Publisher · View at Google Scholar
  • Chia-Chao Wu, Yen-Sung Huang, Jin-Shuen Chen, Ching-Feng Huang, Sui-Lung Su, Kuo-Cheng Lu, Yuh-Feng Lin, Pauling Chu, Shih-Hua Lin, and Huey-Kang Sytwu, “Resveratrol Ameliorates Renal Damage, Increases Expression of Heme Oxygenase-1, and Has Anti-Complement, Anti-Oxidative, and Anti-Apoptotic Effects in,” Plos One, vol. 10, no. 5, 2015. View at Publisher · View at Google Scholar
  • Liu Gang, Song Dongmei, Jiang Yu, Zhu Liqing, and Ge Yun, “Expression of heme oxygenase-1 in lung tissue of paraquat poisoned mice and its significance,” Chinese Critical Care Medicine, vol. 27, no. 4, pp. 280–284, 2015. View at Publisher · View at Google Scholar
  • Liyun Liu, Yunxiao Shang, Miao Li, Xiaohua Han, Jia Wang, and Juan Wang, “Curcumin ameliorates asthmatic airway inflammation by activating nuclear factor-E2-related factor 2/haem oxygenase (HO)-1 signalling pathway,” Clinical and Experimental Pharmacology and Physiology, vol. 42, no. 5, pp. 520–529, 2015. View at Publisher · View at Google Scholar
  • Li-Li Qu, Bin Yu, Zheng Li, Wen-Xiao Jiang, Jian-Dong Jiang, and Wei-Jia Kong, “Gastrodin Ameliorates Oxidative Stress and Proinflammatory Response in Nonalcoholic Fatty Liver Disease through the AMPK/Nrf2 Pathway,” Phytotherapy Research, 2015. View at Publisher · View at Google Scholar
  • Tsuyoshi Takada, Shigeru Miyaki, Hiroyuki Ishitobi, Yuya Hirai, Tomoyuki Nakasa, Kazuhiko Igarashi, Martin K. Lotz, and Mitsuo Ochi, “Bach1 deficiency reduces severity of osteoarthritis through upregulation of heme oxygenase-1,” Arthritis Research & Therapy, vol. 17, 2015. View at Publisher · View at Google Scholar
  • Wei-Wei Ma, Chao-Qun Li, Huan-Ling Yu, Dan-Di Zhang, Yuan-Di Xi, Jing Han, Quan-Ri Liu, and Rong Xiao, “The Oxysterol 27-Hydroxycholesterol Increases Oxidative Stress and Regulate Nrf2 Signaling Pathway in Astrocyte Cells,” Neurochemical Research, 2015. View at Publisher · View at Google Scholar
  • Joseph Fomusi Ndisang, “Role of the Heme Oxygenase-Adiponectin-Atrial Natriuretic Peptide Axis in Renal Function,” Current Pharmaceutical Design, vol. 21, no. 30, pp. 4380–4391, 2015. View at Publisher · View at Google Scholar
  • Souvik Sarkar, Somnath Mazumder, Shubhra J. Saha, and Uday Bandyopadhyay, “Management of inflammation by natural polyphenols: A comprehensive mechanistic update,” Current Medicinal Chemistry, vol. 23, no. 16, pp. 1657–1695, 2016. View at Publisher · View at Google Scholar
  • Ming Cai, Hong Wang, Jing-jing Li, Yun-Li Zhang, Lei Xin, Feng Li, and Shu-jie Lou, “The signaling mechanisms of hippocampal endoplasmic reticulum stress affecting neuronal plasticity-related protein levels in high fat diet-induced obese rats and the regulation of aerobic exercise,” Brain, Behavior, and Immunity, 2016. View at Publisher · View at Google Scholar
  • Vikram Joshi, M. Umashankara, Chandrasekaran Ramakrishnan, Ankanahalli N. Nanjaraj Urs, Suvilesh Kanve Nagaraj, Devadasan Velmurugan, Kanchugarakoppal S. Rangappa, and Bannikuppe Sannanaik Vishwanath, “Dimethyl ester of bilirubin exhibits anti-inflammatory activity through inhibition of secretory phospholipase A2, lipoxygenase and cyclooxygenase,” Archives of Biochemistry and Biophysics, 2016. View at Publisher · View at Google Scholar
  • Ying Chen, Yi Zhang, Huifan Ji, Yuan Ji, Jigao Yang, Jing Huang, and Daguang Sun, “Involvement of hypoxia-inducible factor-1α in the oxidative stress induced by advanced glycation end products in murine Leydig cells,” Toxicology in Vitro, vol. 32, pp. 146–153, 2016. View at Publisher · View at Google Scholar
  • Ying Chen, Yi Zhang, Huifan Ji, Yuan Ji, Jigao Yang, Jing Huang, and Daguang Sun, “Involvement of hypoxia-inducible factor-1 alpha in the oxidative stress induced by advanced glycation end products in murine Leydig cells,” Toxicology In Vitro, vol. 32, pp. 146–153, 2016. View at Publisher · View at Google Scholar
  • Hui-Chun Ku, Shih-Yi Lee, Kai-Chien Yang, Yueh-Hsiung Kuo, and Ming-Jai Su, “Modification of Caffeic Acid with Pyrrolidine Enhances Antioxidant Ability by Activating AKT/HO-1 Pathway in Heart,” Plos One, vol. 11, no. 2, 2016. View at Publisher · View at Google Scholar
  • W Liu, Z Xu, H Li, M Guo, T Yang, S Feng, B Xu, and Yu Deng, “Protective effects of curcumin against mercury-induced hepatic injuries in rats, involvement of oxidative stress antagonism, and Nrf2-ARE pathway activation,” Human & Experimental Toxicology, vol. 36, no. 9, pp. 949–966, 2016. View at Publisher · View at Google Scholar
  • Christoph Steiger, Cornelius Hermann, and Lorenz Meinel, “Localized delivery of carbon monoxide,” European Journal of Pharmaceutics and Biopharmaceutics, 2016. View at Publisher · View at Google Scholar
  • Zhilong Jiang, and Lei Zhu, “Update on Molecular Mechanisms of Corticosteroid Resistance in Chronic Obstructive Pulmonary Disease,” Pulmonary Pharmacology & Therapeutics, 2016. View at Publisher · View at Google Scholar
  • Joseph Fomusi Ndisang, “Heme oxygenase in cardiac repair and regeneration,” Frontiers In Bioscience-Landmark, vol. 21, pp. 251–277, 2016. View at Publisher · View at Google Scholar
  • Stefania Sut, Valeria Baldan, Marta Faggian, Stefano Dall'Acqua, and Gregorio Peron, “Nutraceuticals, A new challenge for medicinal chemistry,” Current Medicinal Chemistry, vol. 23, no. 28, pp. 3198–3223, 2016. View at Publisher · View at Google Scholar
  • Chu-Sook Kim, Hye-Seon Choi, Yeonsoo Joe, Hun Taeg Chung, and Rina Yu, “Induction of heme oxygenase-1 with dietary quercetin reduces obesity-induced hepatic inflammation through macrophage phenotype switching,” Nutrition Research and Practice, vol. 10, no. 6, pp. 623, 2016. View at Publisher · View at Google Scholar
  • Jiajia Song, Tiange Li, Xue Cheng, Xiaomin Ji, Dongxiao Gao, Min Du, Naiyi Jiang, Xueling Liu, and Xueying Mao, “Sea cucumber peptides exert anti-inflammatory activity through suppressing NF-κB and MAPK and inducing HO-1 in RAW264.7 macrophages,” Food Funct., 2016. View at Publisher · View at Google Scholar
  • Duane T. Lowe, “Cupping therapy: An analysis of the effects of suction on skin and the possible influence on human health,” Complementary Therapies in Clinical Practice, 2017. View at Publisher · View at Google Scholar
  • Fuxing Dong, Shuang Wang, Yiwen Wang, Xiao Yang, Jiali Jiang, Dejian Wu, Xuebin Qu, Hongbin Fan, and Ruiqin Yao, “Quercetin ameliorates learning and memory via the Nrf2-ARE signaling pathway in D-galactose-induced neurotoxicity in mice,” Biochemical and Biophysical Research Communications, 2017. View at Publisher · View at Google Scholar
  • Young-Jin Seo, Kui-Jin Kim, Eun-Jeong Koh, Jia Choi, and Boo-Yong Lee, “Anti-adipogenesis mechanism of pterostilbene through the activation of heme oxygenase-1 in 3T3-L1 cells,” Phytomedicine, 2017. View at Publisher · View at Google Scholar
  • Priscila Machado Rosa, Leo Anderson Meira Martins, Diogo Onofre Souza, and André Quincozes-Santos, “Glioprotective Effect of Resveratrol: an Emerging Therapeutic Role for Oligodendroglial Cells,” Molecular Neurobiology, 2017. View at Publisher · View at Google Scholar
  • Stephan Immenschuh, Vijith Vijayan, Sabina Janciauskiene, and Faikah Gueler, “Heme as a Target for Therapeutic Interventions,” Frontiers in Pharmacology, vol. 8, 2017. View at Publisher · View at Google Scholar
  • Tae Woo Jung, Hyung-Chun Kim, and Ji Hoon Jeong, “Protectin DX suppresses hepatic gluconeogenesis through AMPK-HO-1-mediated inhibition of ER stress,” Cellular Signalling, 2017. View at Publisher · View at Google Scholar
  • Harry Robberecht, Tess De Bruyne, and Nina Hermans, “Biomarkers of the metabolic syndrome: influence of selected foodstuffs, containing bioactive components,” Phytochemistry Reviews, 2017. View at Publisher · View at Google Scholar
  • Nicole K. Campbell, Hannah K. Fitzgerald, Anna Malara, Roisin Hambly, Cheryl M. Sweeney, Brian Kirby, Jean M. Fletcher, and Aisling Dunne, “Naturally derived Heme-Oxygenase 1 inducers attenuate inflammatory responses in human dendritic cells and T cells: relevance for psoriasis treatment,” Scientific Reports, vol. 8, no. 1, 2018. View at Publisher · View at Google Scholar
  • Xueling Ma, Zhongjun Chen, Le Wang, Gesheng Wang, Zihui Wang, XiaoBo Dong, Binyu Wen, and Zhichen Zhang, “The Pathogenesis of Diabetes Mellitus by Oxidative Stress and Inflammation: Its Inhibition by Berberine,” Frontiers in Pharmacology, vol. 9, 2018. View at Publisher · View at Google Scholar
  • Ajaz Ahmad Waza, Zeenat Hamid, Sajad Ali, Shabir Ahmad Bhat, and Musadiq Ahmad Bhat, “A review on heme oxygenase-1 induction: is it a necessary evil,” Inflammation Research, 2018. View at Publisher · View at Google Scholar
  • Marcos Roberto de Oliveira, Flávia Bittencourt Brasil, and Cristina Ribas Fürstenau, “Sulforaphane Attenuated the Pro-Inflammatory State Induced by Hydrogen Peroxide in SH-SY5Y Cells Through the Nrf2/HO-1 Signaling Pathway,” Neurotoxicity Research, 2018. View at Publisher · View at Google Scholar
  • Nattapon Jaisupa, Primchanien Moongkarndi, Pattamapan Lomarat, Jutima Samer, Vatchara Tunrungtavee, Weerasak Muangpaisan, and Supachoke Mangmool, “Mangosteen peel extract exhibits cellular antioxidant activity by induction of catalase and heme oxygenase-1 mRNA expression,” Journal of Food Biochemistry, pp. e12511, 2018. View at Publisher · View at Google Scholar
  • Yu-Ting Liu, Ze-Min Lin, Shi-Jun He, and Jian-Ping Zuo, “Heme oxygenase-1 as a potential therapeutic target in rheumatic diseases,” Life Sciences, 2018. View at Publisher · View at Google Scholar
  • Chaker El Kalamouni, Etienne Frumence, Sandra Bos, Jonathan Turpin, Brice Nativel, Wissal Harrabi, David Wilkinson, Olivier Meilhac, Gilles Gadea, Philippe Desprès, Pascale Krejbich-Trotot, and Wildriss Viranaïcken, “Subversion of the Heme Oxygenase-1 Antiviral Activity by Zika Virus,” Viruses, vol. 11, no. 1, pp. 2, 2018. View at Publisher · View at Google Scholar
  • Christopher P. Hopper, Lorenz Meinel, Leo E. Otterbein, and Christoph Steiger, “Where is the clinical breakthrough of heme oxygenase-1/carbon therapeutics?,” Current Pharmaceutical Design, vol. 24, no. 20, pp. 2264–2282, 2018. View at Publisher · View at Google Scholar
  • Muddasarul Hoda, Shanmugam Hemaiswarya, Mukesh Doble, Muddasarul Hoda, Shanmugam Hemaiswarya, and Mukesh Doble, “Mechanisms of Action of Phenolic Phytochemicals in Diabetes Management,” Role of Phenolic Phytochemicals in Diabetes Management, pp. 83–121, 2019. View at Publisher · View at Google Scholar
  • Eirini Chainoglou, and Dimitra Hadjipavlou-Litina, “Curcumin analogues and derivatives with anti-proliferative and anti-inflammatory activity: Structural characteristics and molecular targets,” Expert Opinion on Drug Discovery, pp. 1–22, 2019. View at Publisher · View at Google Scholar
  • Thierry Conrozier, “Prise en charge médicale de l’arthrose chez le patient obèse,” Pratiques en nutrition, vol. 15, no. 58, pp. 15–19, 2019. View at Publisher · View at Google Scholar
  • S.K. Gabr, R.O. Bakr, E.S. Mostafa, A.M. El-Fishawy, and T.S. El-Alfy, “Antioxidant activity and molecular docking study of Erythrina × neillii polyphenolics,” South African Journal of Botany, vol. 121, pp. 470–477, 2019. View at Publisher · View at Google Scholar
  • Liu Liu, Chunxiang Bian, Xiangyu Hu, Weiqi Nian, Wei Xu, Julia Li Zhong, Yan Wu, Muhammad Farrukh Nisar, Mei Wang, Qingchun Diao, and Enwen Wang, “Heme oxygenase 1 facilitates cell proliferation via the B-Raf-ERK signaling pathway in melanoma,” Cell Communication and Signaling, vol. 17, no. 1, 2019. View at Publisher · View at Google Scholar
  • Daniel Wysokiński, Patrycja Lewandowska, Daria Zątak, Michał Juszczak, Magdalena Kluska, Daria Lizińska, Bogna Rudolf, and Katarzyna Woźniak, “Photoactive CO-releasing complexes containing iron – genotoxicity and ability in HO-1 gene induction in HL-60 cells,” Toxicology Research, 2019. View at Publisher · View at Google Scholar