Beneficial effects of kimchi, a Korean fermented vegetable food, on pathophysiological factors related to atherosclerosis

Journal of Medicinal Food

Volumn 21, Issue 2, 2018, Pages 127-135

  Kim, Hyun Ju ^a   Noh, Jeong Sook ^b   Song, Yeong Ok ^c  

^a World Institute of Kimchi an Annex of Korea Food Research Institute   (South Korea)

^b Tongmyong University   (South Korea)

^c Pusan National University   (South Korea)

Author keywords

3 (40 Hydroxyl 30,50 dimethoxyphenyl)propionic acid; atherosclerosis; hypercholesterolemia; kimchi; LDL oxidation

Indexed keywords

3 (4' HYDROXYL 3',5' DIMETHOXYPHENYL)PROPIONIC ACID; ANTIINFLAMMATORY AGENT; ANTILIPEMIC AGENT; ANTIOXIDANT; UNCLASSIFIED DRUG;

ANTI ATHEROSCLEROSCLEROTIC EFFECT; ANTI ENDOPLASMIC RETICULUM STRESS EFFECT; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; ATHEROSCLEROSIS; DRUG ACTIVITY; ENDOPLASMIC RETICULUM STRESS; HUMAN; KIMCHI; LIPID LOWERING EFFECT; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; ANALYSIS; ANIMAL; BRASSICA; CHEMISTRY; DIET THERAPY; FERMENTED PRODUCT; METABOLISM;

ANIMALS; ANTIOXIDANTS; ATHEROSCLEROSIS; BRASSICA; FERMENTED FOODS; HUMANS;

EID: 85042232247     PISSN: 1096620X     EISSN: 15577600     Source Type: Journal    
DOI: 10.1089/jmf.2017.3946     Document Type: Article

References (88)

1. McGill HC, Henry C, Strong JP: The geographic pathology of atherosclerosis. Ann N Y Acad Sci 1968;149:923-927.
2. Lawler PR, Akinkuolie AO, Chu AY, Shah SH, Kraus WE, Craig D, Padmanabhan L, Glynn RJ, Ridker PM, Chasman DI, Mora S: Atherogenic lipoprotein determinants of cardiovascular disease and residual risk among individuals with low-density lipoprotein cholesterol. J Am Heart Assoc 2017;6. pii: e005549.
3. Konukoglu D, Uzun H: Endothelial dysfunction and hypertension. Adv Exp Med Biol 2017;956:511-540.
4. Barua RS, Sharma M, Dileepan KN: Cigarette smoke amplifies inflammatory response and atherosclerosis progression through activation of theH1R-TLR2/4-COX2axis. Front Immunol 2015;6:572-579.
5. Prasad K, Dhar I, Caspar-Bell G: Role of advanced glycation end products and its receptors in the pathogenesis of cigarette smokeinduced cardiovascular disease. Int J Angiol 2015;24:75-80.
6. Siasos G, Tsiqkou V, Kokkou E, Oikonomou E, Vavuranakis M, Vlachopoulos C, Verveniotis A, Limperi M, Genimata V, Papavassiliou AG, Stefanadis C, Tousoulis D: Smoking and ath-erosclerosis: Mechanisms of disease and new therapeutic approaches. Curr Med Chem 2014;21:3936-3948.
7. Fadini GP, Ciciliot S: Vascular smooth muscle cells and monocyte-macrophages accomplice in the accelerated atherosclerosis of insulin resistance states. Cardiovasc Res 2014;103: 194-195.
8. Yahagi K, Kolodgie FD, Lutter C, Mori H, Romero ME, Finn AV, Virmani R: Pathology of human coronary and carotid artery atherosclerosis and vascular calcification in diabetes mellitus. Arterioscler Thromb Vasc Biol 2017;37:191-204.
9. Lovren F, Teoh H, Verma S: Obesity and atherosclerosis: Mechanistic insights. Can J Cardiol 2015;31:177-183.
10. Wu W, Wang H, Jiao G, Yue J, Wang G: Aerobic exercise suppresses atherosclerosis through adiponectin-nuclear transcription factor kB pathway in apolipoprotein E-deficient mice. Am J Med Sci 2017;353:275-281.
11. Nettleton JA, Polak JF, Tracy R, Burke GL, Jacobs DR Jr.: Dietary patterns and incident cardiovascular disease in the multiethnic study of atherosclerosis. Am J Clin Nutr 2009;90:647-654.
12. Shah AM, Claggett B, Kitzman D, Biering-Sørensen T, Jensen JS, Cheng S, Matsushita K, Konety S, Folsom AR, Mosley TH, Wright JD, Heiss G, Solomon SD: Contemporary assessment of left ventricular diastolic function in older adults: The atherosclerosis risk in communities study. Circulation 2017;135:426-439.
13. Hindieh W, Pilote L, Cheema A, Al-Lawati H, Labos C, Dufresne L, Engert JC, Thanassoulis G: Association between family history, a genetic risk score, and severity of coronary artery disease in patients with premature acute coronary syndromes. Arterioscler Thromb Vasc Biol 2016;36:1286-1292.
14. Fredman G, Tabas I: Boosting inflammation resolution in atherosclerosis: The next frontier for therapy. Am J Pathol 2017; 187:1211-1221.
15. Eltoft A, Arntzen KA, Hansen JB, Wilsqaard T, Mathiesen EB, Johnsen SH: C-reactive protein in atherosclerosis-A risk marker but not a causal factor? A 13-year population-based longitudinal study: The Tromsø study. Atherosclerosis 2017; 263:293-300.
16. Dron JS, Hegele RA: Genetics of triglycerides and the risk of atherosclerosis. Curr Atheroscler Rep 2017;19:31-40.
17. Zychowski KE, Sanchez B, Pedrosa RP, Lorenzi-Filho G, Drager LF, Polotsky VY, Campen MJ: Serum from obstructive sleep apnea patients induces inflammatory responses in coronary artery endothelial cells. Atherosclerosis 2016;254:59-66.
18. Bailey KA, Haj FG, Simon SI, Passerini AG: Atherosusceptible shear stress activates endoplasmic reticulum stress to promote endothelial inflammation. Sci Rep 2017;7:8196-8212.
19. Tanaka A, Cui R, Kitamura A, Liu K, Imano H, Yamagishi K, Kiyama M, Okada T, Iso H: Heavy alcohol consumption is associated with impaired endothelial function. J Atheroscler Thromb 2016;23:1047-1054.
20. Ross R: The pathogenesis of atherosclerosis: A perspective for the 1990s. Nature 1993;362:801-809.
21. Cheigh HS, Park KY, Lee CY: Biochemical, microbiological, and nutritional aspects of kimchi (Korean fermented vegetable products). Crit Rev Food Sci Nutr 1994;34:175-203.
22. Woo M, Kim M, Noh JS, Song YO: Kimchi methanol extracts attenuate hepatic steatosis induced by high cholesterol diet in low-density lipoprotein receptor knockout mice through inhibition of endoplasmic reticulum stress. J Funct Food 2017;32:218-225.
23. Kwon MJ, Chun JH, Song YS, Song YO: Daily kimchi consumption and its hypolipidemic effect in middle-aged men. J Korean Soc Food Sci Nutr 2005;2:1144-1150.
24. Baek YH, Kwak JR, Kim SJ, Han SS, Song YO: Effects of kimchi supplementation and/or exercise training on body composition and plasma lipids in obese middle school girls. J Korean Soc Food Sci Nutr 2001;30:906-912.
25. Choi SH, Kim HJ, Kwon MJ, Baek YH, Song YO: The effects of kimchi pill supplementation on plasma lipid concentration in healthy people. J Korean Soc Food Sci Nutr 2001;30:913-920.
26. Kim EK, An SY, Lee MS, et al.: Fermented kimchi reduces body weight and improves metabolic parameters in overweight and obese patients. Nutr Res 2011;31:436-443.
27. Oh IM, Joung HJ, Oh SW, et al.: Relationship of combined consumption of rice and kimchi, Korean traditional diet and the risk of metabolic syndrome in healthy Korean volunteers. J Korean Soc Parenter Enter Nutr 2013;5:100-116.
28. Choi IH, Noh JS, Han JS, Kim HJ, Han ES, Song YO: Kimchi, a fermented vegetable, improves serum lipid profiles in healthy young adults: Randomized clinical trial. J Med Food 2013;16: 223-229.
29. Kim HJ, Lee JS, Chung HY, et al.: 3-(40-Hydroxyl-30, 50-dimethoxyphenyl) propionic acid, an active principle of kimchi, inhibits development of atherosclerosis in rabbits. J Agric Food Chem 2007;55:10486-10492.
30. Noh JS, Kim HJ, Kwon MJ, Song YO: Active principle of kimchi, 3-(40-hydroxyl-30, 50-dimethoxyphenyl) propionic acid, retards fatty streak formation at aortic sinus of apolipoprotein E knockout mice. J Med Food 2009;12:1206-1212.
31. Noh JS, Choi YH, Song YO: Beneficial effects of the active principle component of Korean cabbage kimchi via increasing nitric oxide production and suppressing inflammation in the aorta of aopE knockout mice. Br J Nutr 2013;109:17-24.
32. Lee YM, Kwon MJ, Kim JK, Suh HS, Chio JS, Song YO: Isolation and identification of active principle in Chinese cabbage kimchi responsible for antioxidant activity. Korean J Food Sci Technol 2004;36:129-133.
33. Park KY, Jeong JK, Lee YE, Daily III JW: Health benefits of kimchi (Korean fermented vegetables) as a probiotic food. J Med Food 2014;17:6-20.
34. McGill HC, McMahan CA, Herderick EE, Malcom GT, Tracy RE, Strong JP: Origin of atherosclerosis in childhood and adolescence. Am J Clin Nutr 2000;72:1307S-13015S.
35. Fuster V: Lewis A: Mechanism leading to myocardial infarction: Insights from studies of vascular biology. Circulation 1994;90: 2126-2146.
36. Napoli C, D'Armiento FP, Mancini FP, et al.: Fatty streak formation occurs in human fetal aortas and is greatly enhanced by maternal hypercholesterolemia. Intimal accumulation of LDL and its oxidation precede monocyte recruitment into early atherosclerotic lesions. J Clin Invest 1997;100:2680-2690.
37. Lusis AJ: Atherosclerosis. Nature 2000;407:233-241.
38. Libby P, Theroux P: Pathophysiology of coronary artery disease. Circulation 2005;111:3481-3488.
39. Glass CK, Witztum JL: Atherosclerosis: The road ahead. Cell 2001;104:503-516.
40. Kwon MJ, Song YO, Song YS: Effects of kimchi on tissue and fecal lipid composition and apolipoprotein and thyroxine levels in rats. J Korean Soc Food Sci Nutr 1997;26:507-513.
41. Kim JY, Lee YS: The effects of kimchi intake on lipid contents of body and mitogen response of spleen lymphocytes in rats. J Korean Soc Food Sci Nutr 1997;26:1200-1207.
42. Sheo HJ, Seo YS: The effects of dietary Chinese cabbage kimchi juice on the lipid metabolism and body weight gain in rats fed high-calories-diet. J Korean Soc Food Sci Nutr 2004;33:91-100.
43. Hwang JW, Song YO: The effects of solvent fractions of kimchi on plasma lipid concentration of rabbit fed high cholesterol diet. J Korean Soc Food Sci Nutr 2000;29:204-210.
44. Jeon HN, Kwon MJ, Song YO: Effects of kimchi solvent fractions on accumulation of lipids in heart, kidney, and lung of rabbit fed high cholesterol diet. J Korean Soc Food Sci Nutr 2002;31:814-818.
45. Kwon MJ, Song YS, Choi MS, Song YO: Red pepper attenuates cholesteryl ester transfer protein activity and atherosclerosis in cholesterol-fed rabbits. Clin Chim Acta 2003;332:37-44.
46. Kim HJ, Kwon MJ, Seo JM, et al.: The effects of 3-(40-hydroxyl-3050-dimethoxyphenyl) propionic acid in Chinese cabbage kimchi on lowering hypercholesterolemia. J Korean Soc Food Sci Nutr 2004;33:52-58.
47. Kong YH, Cheigh HS, Song YO, Jo YO, Choi SY: Anti-obesity effects of kimchi tablet composition in rats fed high-fat diet. J Korean Soc Food Sci Nutr 2007;36:1529-1536.
48. Park KY, Ha JO, Rhee SH: A study on the contents dietary fibers and crude fiber in kimchi ingredients and kimchi. J Korean Soc Food Sci Nutr 1996;25:69-75.
49. Smet ED, Mensink RP, Plat J: Effects of plant sterols and stanols on intestinal cholesterol metabolism: Suggested mechanisms from past to present. Mol Nutr Food Res 2012;56: 1058-1072.
50. Sheela CG, Augusti KT: Effects of S-allyl cysteine sulfoxide isolated from Allium sativum Linn and gugulipid on some enzymes and fecal excretions of bile acids and sterols in cholesterol fed rats. Indian J Exp Biol 1995;33:749-751.
51. Focke M, Feld A, Lichtenthaler HK: Allicin, a naturally occurring antibiotic from garlic, specifically inhibits acetyl-CoA synthetase. FEBS Lett 1990;261:106-108.
52. Kumari K, Mathew BC, Augusti KT: Antidiabetic and hypolipidaemic effects of S-methyl cysteine sulfoxide, isolated from Allium cepa Linn. Indian J Biochem Biophys 1995;32:49-54.
53. Srinivasan K: Biological activities of red pepper (Capsicum annuum) and its pungent principle capsaicin: A review. Crit Rev Food Sci Nutr 2016;56:1488-1500.
54. Yoshioka M, St-Pierre S, Suzuki M, Tremblay A: Effects of red pepper added to high-fat and high-carbohydrate meals on energy metabolism and substrate utilization in Japanese women. Br J Nutr 1998;80:503-510.
55. Kumar M, Nagpal R, Kumar R, Hemalatha R, Verma V, Kumar A, Chakraborty C, Singh B, Marotta F, Jain S, Yadav H: Cholesterol-lowering probiotics as potential biotherapeutics for metabolic diseases. Exp Diabetes Res 2012;2012:902917.
56. Gilliland SE, Speck ML: Deconjugation of bile acids by intestinal lactobacilli. Appl Environ Microbiol 1977;33:15-18.
57. Gilliland SE, Nelson CR, Maxwell C: Assimilation of cholesterol by Lactobacillus acidophilus. Appl Environ Microbiol 1985;49: 377-381.
58. Jo SY, Choi EA, Lee JJ, Chang HC: Characterization of starter kimchi fermented with Leuconostoc kimchi GJ2 and its cholesterol-lowering effects in rats fed a high-fat and highcholesterol diet. J Sci Food Agric 2015;95:2750-2756.
59. Huang Y, Wang J, Quan G, Wang X, Yang L, Zhong L: Lactobacillus acidophilus ATCC 4356 prevents atherosclerosis via inhibition of intestinal cholesterol absorption in apolipoprotein E-knockout mice. Appl Environ Microbiol 2014;80:7496-7504.
60. Ryu BM, Ryu SH, Jeon YS, Lee YS, Moon GS: Inhibitory effect of solvent fraction of various kinds of kimchi on ultraviolet B induced oxidation and erythema formation of hairless mice skin. J Korean Soc Food Sci Nutr 2004;33:785-790.
61. Ryu SH, Jeon YS, Kwon MJ, Lee YS, Moon GS: Effect of kimchi extracts to reactive oxygen species in skin cell cytotoxicity. J Korean Soc Food Sci Nutr 1997;26:814-821.
62. Ryu BM, Ryu SH, Lee YS, Jeon YS, Moon GS: Effect of different kimchi diets on oxidation and photooxidation in liver and skin of hairless mice. J Korean Soc Food Sci Nutr 2004;33:291-298.
63. Park JM, Shin JH, Gu JG, et al.: Effect of antioxidant activity in kimchi during a short-term and over-ripening fermentation period. J Biosci Bioeng 2011;112:356-359.
64. Kim BK, Choi JM, Kang SA, Park KY, Cho EJ: Antioxidant effects of kimchi under different fermentation stage on radicalinduced oxidative stress. Nutr Res Pract 2014;8:638-643.
65. Collins T, Cybulsky MI: NF-jB: Pivotal mediator or innocent bystander in atherogenesis? J Clin Invest 2001;107:255-264.
66. Jeong JW, Choi IW, Jo GH, et al.: Anti-inflammatory effects of 3-(40-hydroxyl-30,50-dimethoxyphenyl)propionic acid, an active component of Korean cabbage kimchi, in lipopolysaccharidestimulated BV2 microglia. J Med Food 2015;18:677-684.
67. Kim HJ, Sung YB, Song YO, et al.: Kimchi suppresses 7-ketocholesterol-induced endoplasmic reticulum stress in macrophages. Food Sci Biotechnol 2012;21:1293-1299.
68. Kwon MJ, Song YS, Song YO: Antioxidative effect of kimchi ingredients on rabbits fed cholesterol diet. J Korean Soc Food Sci Nutr 1998;27:1189-1196.
69. Kim HJ, Kwon MJ, Song YO: Effects of solvent fraction of Korean cabbage kimchi on antioxidative enzyme activities and fatty acid composition of phospholipids of rabbit fed 1% cholesterol diet. J Korean Soc Food Sci Nutr 2000;29:900-907.
70. Kim JH, Ryu JD, Lee HG, et al.: The effect of kimchi on production of free radicals and anti-oxidative enzyme activities in the brain of SAM. J Korean Soc Food Sci Nutr 2002;31: 117-123.
71. Kim JH, Ryu JD, Song YO: The effect of kimchi intake on free radical production and the inhibition of oxidation in young adults and the elderly people. Korean J Community Nutr 2002;7:257-265.
72. Kwon MJ, Song YS, Choi MS, et al.: Cholesteryl ester transfer protein activity and atherogenic parameters in rabbit supplemented with cholesterol and garlic powder. Life Sci 2003;72: 2953-2964.
73. Fu Y, Luo N, Lopes-Virella MF: Oxidized LDL induces the expression of ALBP/aP2 mRNA and protein in human THP-1 macrophages. J Lipid Res 2000;41:2017-2023.
74. Ricciarelli R, Zingg JM, Azzi A: Vitamin E reduces the uptake of oxidized LDL by inhibiting CD36 scavenger receptor expression in cultured human aortic smooth muscle cells. Circulation 2000; 102:82-87.
75. Fu Y, Luo N, Lopes-Virella MF, Garvey WT: The adipocyte lipid binding protein (ALBP/aP2) gene facilitates foam cell formation in human THP-1 macrophages. Atherosclerosis 2002;165: 259-269.
76. Fu Y, Luo L, Luo N, Garvey WT: Lipid metabolism mediated by adipocyte lipid binding protein (ALBP/aP2) gene expression in human THP-1 macrophages. Atherosclerosis 2006;188:102-111.
77. Yun YR, Kim HJ, Song YO: Kimchi methanol extract and the kimchi active compound, 30-(40-hydroxyl-30,50-dimethoxyphenyl)propionic acid, downregulate CD36 in THP-1 macrophages stimulated by oxLDL. J Med Food 2014;17:886-893.
78. Zhang K, Kaufman RJ: From endoplasmic-reticulum stress to the inflammatory response. Nature 2008;454:455-462.
79. Ron D, Walter P: Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 2007;8:519-529.
80. Schroder M, Kaufman RJ: The mammalian unfolded protein response. Annu Rev Biochem 2005;74:739-789.
81. Myoishi M, Hao H, Minamino T, et al.: Increased endoplasmic reticulum stress in atherosclerotic plaques associated with acute coronary syndrome. Circulation 2007;116:1226-1233.
82. Sanson M, Auge N, Vindis C, et al.: Oxidized low-density lipoproteins trigger endoplasmic reticulum stress in vascular cells: Prevention by oxygen-regulated protein 150 expression. Circ Res 2009;104:328-336.
83. Kim I, Xu W, Reed JC: Cell death and endoplasmic reticulum stress: Disease relevance and therapeutic opportunities. Nat Rev Drug Discov 2008;7:1013-1030.
84. Austin RC: The unfolded protein response in health and disease. Antioxid Redox Signal 2009;11:2279-2287.
85. Tabas I: The role of endoplasmic reticulum stress in the progression of atherosclerosis. Circ Res 2010;107:839-850.
86. Zhou J, Lhotak S, Hilditch BA, Austin RC: Activation of the unfolded protein response occurs at all stages of atherosclerotic lesion development in apolipoprotein E-deficient mice. Circulation 2005;111:1814-1821.
87. Oh J, Weng S, Felton SK, et al.: 1,25(OH)2 vitamin D inhibits foam cell formation and suppresses macrophage cholesterol uptake in patients with type 2 diabetes mellitus. Circulation 2009; 120:687-698.
88. Choi CH, Jung YK, Oh SH: Autophagy induction by capsaicin in malignant human breast cells is modulated by p38 and extracellular signal-regulated mitogen-activated protein kinases and retards cell death by suppressing endoplasmic reticulum stressmediated apoptosis. Mol Pharmacol 2010;78:114-125.