Mechanisms underlying the attenuation of chronic inflammatory diseases by aged garlic extract: Involvement of the activation of AMP‑activated protein kinase (Review)
- Authors:
- Satomi Miki
- Jun‑Ichiro Suzuki
- Kayo Kunimura
- Naoaki Morihara
-
Affiliations: Central Research Institute, Wakunaga Pharmaceutical Co., Ltd., Akitakata‑shi, Hiroshima 739‑1195, Japan - Published online on: December 27, 2019 https://doi.org/10.3892/etm.2019.8372
- Pages: 1462-1467
-
Copyright: © Miki et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
 |
 |
|
Hardie DG, Ross FA and Hawley SA: AMPK: A nutrient and energy sensor that maintains energy homeostasis. Nat Rev Mol Cell Biol. 13:251–262. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Mihaylova MM and Shaw RJ: The AMPK signalling pathway coordinates cell growth, autophagy and metabolism. Nat Cell Biol. 13:1016–1023. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Garcia D and Shaw RJ: AMPK: Mechanisms of Cellular Energy Sensing and Restoration of Metabolic Balance. Mol Cell. 66:789–800. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Bai A, Ma AG, Yong M, Weiss CR, Ma Y, Guan Q, Bernstein CN and Peng Z: AMPK agonist downregulates innate and adaptive immune responses in TNBS-induced murine acute and relapsing colitis. Biochem Pharmacol. 80:1708–1717. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Nath N, Giri S, Prasad R, Salem ML, Singh AK and Singh I: 5-aminoimidazole-4-carboxamide ribonucleoside: A novel immunomodulator with therapeutic efficacy in experimental autoimmune encephalomyelitis. J Immunol. 175:566–574. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Zhao X, Zmijewski JW, Lorne E, Liu G, Park YJ, Tsuruta Y and Abraham E: Activation of AMPK attenuates neutrophil proinflammatory activity and decreases the severity of acute lung injury. Am J Physiol Lung Cell Mol Physiol. 295:L497–L504. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Lorenzatti AJ and Servato ML: New evidence on the role of inflammation in CVD risk. Curr Opin Cardiol. 34:418–423. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Geovanini GR and Libby P: Atherosclerosis and inflammation: Overview and updates. Clin Sci (Lond). 132:1243–1252. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Liu CH, Abrams ND, Carrick DM, Chander P, Dwyer J, Hamlet MRJ, Macchiarini F, PrabhuDas M, Shen GL, Tandon P, et al: Biomarkers of chronic inflammation in disease development and prevention: Challenges and opportunities. Nat Immunol. 18:1175–1180. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Arulselvan P, Fard MT, Tan WS, Gothai S, Fakurazi S, Norhaizan ME and Kumar SS: Role of Antioxidants and Natural Products in Inflammation. Oxid Med Cell Longev. 2016:52761302016. View Article : Google Scholar : PubMed/NCBI | |
|
Conti P and Shaik-Dasthagirisaeb Y: Atherosclerosis: A chronic inflammatory disease mediated by mast cells. Cent Eur J Immunol. 40:380–386. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Piccinini AM and Midwood KS: DAMPening inflammation by modulating TLR signalling. Mediators Inflamm. 2010:6723952010. View Article : Google Scholar : PubMed/NCBI | |
|
Vénéreau E, Ceriotti C and Bianchi ME: DAMPs from Cell Death to New Life. Front Immunol. 6:4222015. View Article : Google Scholar : PubMed/NCBI | |
|
Patel S: Danger-Associated Molecular Patterns (DAMPs): The Derivatives and Triggers of Inflammation. Curr Allergy Asthma Rep. 18:632018. View Article : Google Scholar : PubMed/NCBI | |
|
Matsutomo T and Kodera Y: Development of an Analytic Method for Sulfur Compounds in Aged Garlic Extract with the Use of a Postcolumn High Performance Liquid Chromatography Method with Sulfur-Specific Detection. J Nutr. 146:450S–455S. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Kodera Y, Ushijima M, Amano H, Suzuki JI and Matsutomo T: Chemical and biological properties of S−1-propenyl-l-cysteine in aged garlic extract. Molecules. 22:E5702017. View Article : Google Scholar : PubMed/NCBI | |
|
Nantz MP, Rowe CA, Muller CE, Creasy RA, Stanilka JM and Percival SS: Supplementation with aged garlic extract improves both NK and γδ-T cell function and reduces the severity of cold and flu symptoms: A randomized, double-blind, placebo-controlled nutrition intervention. Clin Nutr. 31:337–344. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Xu C, Mathews AE, Rodrigues C, Eudy BJ, Rowe CA, O'Donoughue A and Percival SS: Aged garlic extract supplementation modifies inflammation and immunity of adults with obesity: A randomized, double-blind, placebo-controlled clinical trial. Clin Nutr ESPEN. 24:148–155. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Suzuki JI, Kodera Y, Miki S, Ushijima M, Takashima M, Matsutomo T and Morihara N: Anti-inflammatory action of cysteine derivative S−1-propenylcysteine by inducing MyD88 degradation. Sci Rep. 8:141482018. View Article : Google Scholar : PubMed/NCBI | |
|
Kyo E, Uda N, Kasuga S and Itakura Y: Immunomodulatory effects of aged garlic extract. J Nutr. 131((3s)): 1075S–1079S. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Morihara N, Ide N and Weiss N: Aged garlic extract inhibits CD36 expression in human macrophages via modulation of the PPARgamma pathway. Phytother Res. 24:602–608. 2010.PubMed/NCBI | |
|
Morihara N, Hino A, Yamaguchi T and Suzuki J: Aged garlic extract suppresses the development of atherosclerosis apolipoprotein E-knockout mice. J Nutr. 146:460S–463S. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Morihara N, Hino A, Miki S, Takashima M and Suzuki JI: Aged garlic extract suppresses inflammation in apolipoprotein E-knockout mice. Mol Nutr Food Res. 61:17003082017. View Article : Google Scholar | |
|
Matsumoto S, Nakanishi R, Li D, Alani A, Rezaeian P, Prabhu S, Abraham J, Fahmy MA, Dailing C, Flores F, et al: Aged Garlic Extract Reduces Low Attenuation Plaque in Coronary Arteries of Patients with Metabolic Syndrome in a Prospective Randomized Double-Blind Study. J Nutr. 146:427S–432S. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Budoff M: Aged garlic extract retards progression of coronary artery calcification. J Nutr. 136 (Suppl):741S–744S. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Ried K, Frank OR and Stocks NP: Aged garlic extract reduces blood pressure in hypertensives: A dose-response trial. Eur J Clin Nutr. 67:64–70. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Matsutomo T, Ushijima M, Kodera Y, Nakamoto M, Takashima M, Morihara N and Tamura K: Metabolomic study on the antihypertensive effect of S−1-propenylcysteine in spontaneously hypertensive rats using liquid chromatography coupled with quadrupole-Orbitrap mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci. 1046:147–155. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Ried K, Travica N and Sali A: The effect of aged garlic extract on blood pressure and other cardiovascular risk factors in uncontrolled hypertensives: The AGE at Heart trial. Integr Blood Press Control. 9:9–21. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Ried K, Travica N and Sali A: The Effect of Kyolic Aged Garlic Extract on Gut Microbiota, Inflammation, and Cardiovascular Markers in Hypertensives: The GarGIC Trial. Front Nutr. 5:1222018. View Article : Google Scholar : PubMed/NCBI | |
|
Hiramatsu K, Tsuneyoshi T, Ogawa T and Morihara N: Aged garlic extract enhances heme oxygenase-1 and glutamate-cysteine ligase modifier subunit expression via the nuclear factor erythroid 2-related factor 2-antioxidant response element signaling pathway in human endothelial cells. Nutr Res. 36:143–149. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Tsuneyoshi T, Kunimura K and Morihara N: S−1-Propenylcysteine augments BACH1 degradation and heme oxygenase 1 expression in a nitric oxide-dependent manner in endothelial cells. Nitric Oxide. 84:22–29. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Thomson M, Al-Qattan KK, Js D and Ali M: Anti-diabetic and anti-oxidant potential of aged garlic extract (AGE) in streptozotocin-induced diabetic rats. BMC Complement Altern Med. 16:172016. View Article : Google Scholar : PubMed/NCBI | |
|
Ushijima M, Takashima M, Kunimura K, Kodera Y, Morihara N and Tamura K: Effects of S−1-propenylcysteine, a sulfur compound in aged garlic extract, on blood pressure and peripheral circulation in spontaneously hypertensive rats. J Pharm Pharmacol. 70:559–565. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Miki S, Inokuma KI, Takashima M, Nishida M, Sasaki Y, Ushijima M, Suzuki JI and Morihara N: Aged garlic extract suppresses the increase of plasma glycated albumin level and enhances the AMP-activated protein kinase in adipose tissue in TSOD mice. Mol Nutr Food Res. 61:16007972017. View Article : Google Scholar | |
|
Hwang YP, Kim HG, Choi JH, Do MT, Chung YC, Jeong TC and Jeong HG: S-allylcysteine attenuates free fatty acid-induced lipogenesis in human HepG2 cells through activation of the AMP-activated protein kinase-dependent pathway. J Nutr Biochem. 24:1469–1478. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Yu L, Di W, Dong X, Li Z, Xue X, Zhang J, Wang Q, Xiao X, Han J, Yang Y, et al: Diallyl trisulfide exerts cardioprotection against myocardial ischemia-reperfusion injury in diabetic state, role of AMPK-mediated AKT/GSK-3β/HIF-1α activation. Oncotarget. 8:74791–74805. 2017.PubMed/NCBI | |
|
Xiao J, Guo R, Fung ML, Liong EC, Chang RC, Ching YP and Tipoe GL: Garlic-Derived S-Allylmercaptocysteine Ameliorates Nonalcoholic Fatty Liver Disease in a Rat Model through Inhibition of Apoptosis and Enhancing Autophagy. Evid Based Complement Alternat Med. 2013:6429202013. View Article : Google Scholar : PubMed/NCBI | |
|
Kim J, Yang G, Kim Y, Kim J and Ha J: AMPK activators: Mechanisms of action and physiological activities. Exp Mol Med. 48:e2242016. View Article : Google Scholar : PubMed/NCBI | |
|
Coughlan KA, Valentine RJ, Ruderman NB and Saha AK: AMPK activation: A therapeutic target for type 2 diabetes? Diabetes Metab Syndr Obes. 7:241–253. 2014.PubMed/NCBI | |
|
Bäck M, Yurdagul A Jr, Tabas I, Öörni K and Kovanen PT: Inflammation and its resolution in atherosclerosis: Mediators and therapeutic opportunities. Nat Rev Cardiol. 16:389–406. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Salminen A, Hyttinen JM and Kaarniranta K: AMP-activated protein kinase inhibits NF-κB signaling and inflammation: Impact on healthspan and lifespan. J Mol Med (Berl). 89:667–676. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Salminen A and Kaarniranta K: AMP-activated protein kinase (AMPK) controls the aging process via an integrated signaling network. Ageing Res Rev. 11:230–241. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Ou H, Liu C, Feng W, Xiao X, Tang S and Mo Z: Role of AMPK in atherosclerosis via autophagy regulation. Sci China Life Sci. 61:1212–1221. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Liu-Bryan R: Inflammation and intracellular metabolism: New targets in OA. Osteoarthritis Cartilage. 23:1835–1842. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Li Y, Xu S, Mihaylova MM, Zheng B, Hou X, Jiang B, Park O, Luo Z, Lefai E, Shyy JY, et al: AMPK phosphorylates and inhibits SREBP activity to attenuate hepatic steatosis and atherosclerosis in diet-induced insulin-resistant mice. Cell Metab. 13:376–388. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Doddapattar P, Radović B, Patankar JV, Obrowsky S, Jandl K, Nusshold C, Kolb D, Vujić N, Doshi L, Chandak PG, et al: Xanthohumol ameliorates atherosclerotic plaque formation, hypercholesterolemia, and hepatic steatosis in ApoE-deficient mice. Mol Nutr Food Res. 57:1718–1728. 2013.PubMed/NCBI | |
|
Wang Q, Zhang M, Liang B, Shirwany N, Zhu Y and Zou MH: Activation of AMP-activated protein kinase is required for berberine-induced reduction of atherosclerosis in mice: The role of uncoupling protein 2. PLoS One. 6:e254362011. View Article : Google Scholar : PubMed/NCBI | |
|
Van Gaal LF, Mertens IL and De Block CE: Mechanisms linking obesity with cardiovascular disease. Nature. 444:875–880. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Shoelson SE, Lee J and Goldfine AB: Inflammation and insulin resistance. J Clin Invest. 116:1793–1801. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Rameshrad M, Maleki-Dizaji N, Soraya H, Toutounchi NS, Barzegari A and Garjani A: Effect of A-769662, a direct AMPK activator, on Tlr-4 expression and activity in mice heart tissue. Iran J Basic Med Sci. 19:1308–1317. 2016.PubMed/NCBI | |
|
Mancini SJ, White AD, Bijland S, Rutherford C, Graham D, Richter EA, Viollet B, Touyz RM, Palmer TM and Salt IP: Activation of AMP-activated protein kinase rapidly suppresses multiple pro-inflammatory pathways in adipocytes including IL-1 receptor-associated kinase-4 phosphorylation. Mol Cell Endocrinol. 440:44–56. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Malekpour-Dehkordi Z, Javadi E, Doosti M, Paknejad M, Nourbakhsh M, Yassa N, Gerayesh-Nejad S and Heshmat R: S-Allylcysteine, a garlic compound, increases ABCA1 expression in human THP-1 macrophages. Phytother Res. 27:357–361. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Kemmerer M, Wittig I, Richter F, Brüne B and Namgaladze D: AMPK activates LXRα and ABCA1 expression in human macrophages. Int J Biochem Cell Biol. 78:1–9. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Olokoba AB, Obateru OA and Olokoba LB: Type 2 diabetes mellitus: A review of current trends. Oman Med J. 27:269–273. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Kahn SE, Cooper ME and Del Prato S: Pathophysiology and treatment of type 2 diabetes: Perspectives on the past, present, and future. Lancet. 383:1068–1083. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
DeFronzo RA, Ferrannini E, Groop L, Henry RR, Herman WH, Holst JJ, Hu FB, Kahn CR, Raz I, Shulman GI, et al: Type 2 diabetes mellitus. Nat Rev Dis Primers. 1:150192015. View Article : Google Scholar : PubMed/NCBI | |
|
de Luca C and Olefsky JM: Inflammation and insulin resistance. FEBS Lett. 582:97–105. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Mancuso P: The role of adipokines in chronic inflammation. ImmunoTargets Ther. 5:47–56. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
McArdle MA, Finucane OM, Connaughton RM, McMorrow AM and Roche HM: Mechanisms of obesity-induced inflammation and insulin resistance: Insights into the emerging role of nutritional strategies. Front Endocrinol (Lausanne). 4:522013. View Article : Google Scholar : PubMed/NCBI | |
|
León-Pedroza JI, González-Tapia LA, del Olmo-Gil E, Castellanos-Rodríguez D, Escobedo G and González-Chávez A: Low-grade systemic inflammation and the development of metabolic diseases: From the molecular evidence to the clinical practice. Cir Cir. 83:543–551. 2015.(In Spanish). PubMed/NCBI | |
|
Lumeng CN and Saltiel AR: Inflammatory links between obesity and metabolic disease. J Clin Invest. 121:2111–2117. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Rehman K and Akash MS: Mechanisms of inflammatory responses and development of insulin resistance: How are they interlinked? J Biomed Sci. 23:872016. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang BB, Zhou G and Li C: AMPK: An emerging drug target for diabetes and the metabolic syndrome. Cell Metab. 9:407–416. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Hardie DG: AMPK: A target for drugs and natural products with effects on both diabetes and cancer. Diabetes. 62:2164–2172. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Rena G, Hardie DG and Pearson ER: The mechanisms of action of metformin. Diabetologia. 60:1577–1585. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Rojas LB and Gomes MB: Metformin: An old but still the best treatment for type 2 diabetes. Diabetol Metab Syndr. 5:62013. View Article : Google Scholar : PubMed/NCBI | |
|
Setter SM, Iltz JL, Thams J and Campbell RK: Metformin hydrochloride in the treatment of type 2 diabetes mellitus: A clinical review with a focus on dual therapy. Clin Ther. 25:2991–3026. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Lagouge M, Argmann C, Gerhart-Hines Z, Meziane H, Lerin C, Daussin F, Messadeq N, Milne J, Lambert P, Elliott P, et al: Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell. 127:1109–1122. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Price NL, Gomes AP, Ling AJ, Duarte FV, Martin-Montalvo A, North BJ, Agarwal B, Ye L, Ramadori G, Teodoro JS, et al: SIRT1 is required for AMPK activation and the beneficial effects of resveratrol on mitochondrial function. Cell Metab. 15:675–690. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Zhu X, Wu C, Qiu S, Yuan X and Li L: Effects of resveratrol on glucose control and insulin sensitivity in subjects with type 2 diabetes: Systematic review and meta-analysis. Nutr Metab (Lond). 14:602017. View Article : Google Scholar : PubMed/NCBI | |
|
Liang Y, Xu X, Yin M, Zhang Y, Huang L, Chen R and Ni J: Effects of berberine on blood glucose in patients with type 2 diabetes mellitus: A systematic literature review and a meta-analysis. Endocr J. 66:51–63. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Lee YS, Kim WS, Kim KH, Yoon MJ, Cho HJ, Shen Y, Ye JM, Lee CH, Oh WK, Kim CT, et al: Berberine, a natural plant product, activates AMP-activated protein kinase with beneficial metabolic effects in diabetic and insulin-resistant states. Diabetes. 55:2256–2264. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Welsh KJ, Kirkman MS and Sacks DB: Role of Glycated Proteins in the Diagnosis and Management of Diabetes: Research Gaps and Future Directions. Diabetes Care. 39:1299–1306. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Anguizola J, Matsuda R, Barnaby OS, Hoy KS, Wa C, DeBolt E, Koke M and Hage DS: Review: Glycation of human serum albumin. Clin Chim Acta. 425:64–76. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Leto D and Saltiel AR: Regulation of glucose transport by insulin: Traffic control of GLUT4. Nat Rev Mol Cell Biol. 13:383–396. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Huang S and Czech MP: The GLUT4 glucose transporter. Cell Metab. 5:237–252. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Bijland S, Mancini SJ and Salt IP: Role of AMP-activated protein kinase in adipose tissue metabolism and inflammation. Clin Sci (Lond). 124:491–507. 2013. View Article : Google Scholar : PubMed/NCBI |
