[KSCI] Korea Science Citation Index Service

http://dx.doi.org/10.4062/biomolther.2014.066

Protective Effects of Chlorogenic Acid against Experimental Reflux Esophagitis in Rats

Kang, Jung-Woo (School of Pharmacy, Sungkyunkwan University)
Lee, Sun-Mee (School of Pharmacy, Sungkyunkwan University)

Publication Information

Biomolecules & Therapeutics / v.22, no.5, 2014 , pp. 420-425 More about this Journal

Abstract

Esophageal reflux of gastric contents causes esophageal mucosal damage and inflammation. Recent studies show that oxygen-derived free radicals mediate mucosal damage in reflux esophagitis (RE). Chlorogenic acid (CGA), an ester of caffeic acid and quinic acid, is one of the most abundant polyphenols in the human diet and possesses anti-inflammatory, antibacterial and anti-oxidant activities. In this context, we investigated the effects of CGA against experimental RE in rats. RE was produced by ligating the transitional region between the forestomach and the glandular portion and covering the duodenum near the pylorus ring with a small piece of catheter. CGA (10, 30 and 100 mg/kg) and omeprazole (positive control, 10 mg/kg) were administered orally 48 h after the RE operation for 12 days. CGA reduced the severity of esophageal lesions, and this beneficial effect was confirmed by histopathological observations. CGA reduced esophageal lipid peroxidation and increased the reduced glutathione/oxidized glutathione ratio. CGA attenuated increases in the serum level of tumor necrosis factor- ${\alpha}$ , and expressions of inducible nitric oxide synthase and cyclooxygenase-2 protein. CGA alleviates RE-induced mucosal injury, and this protection is associated with reduced oxidative stress and the anti-inflammatory properties of CGA.

Keywords

Chlorogenic acid; Gastroesophageal reflux disease; Inflammation; Oxidative stress; Reflux esophagitis;

Citations & Related Records

Times Cited By KSCI : 1 (Citation Analysis)

Reference
Cited By KSCI

1	Abdel-Latif, M. M., Duggan, S., Reynolds, J. V. and Kelleher, D. (2009) Inflammation and esophageal carcinogenesis. Curr. Opin. Pharmacol. 9, 396-404. DOI
2	Belkaid, A., Currie, J. C., Desgagnes, J. and Annabi, B. (2006) The chemopreventive properties of chlorogenic acid reveal a potential new role for the microsomal glucose-6-phosphate translocase in brain tumor progression. Cancer Cell Int. 6, 7. DOI
3	Bredenoord, A. J., Weusten, B. L., Curvers, W. L., Timmer, R. and Smout, A. J. (2006) Determinants of perception of heartburn and regurgitation. Gut 55, 313-318. DOI ScienceOn
4	Buege, J. A. and Aust, S. D. (1978) Microsomal lipid peroxidation. Methods Enzymol. 52, 302-310. DOI
5	Cha, J. W., Piao, M. J., Kim, K. C., Yao, C. W., Zheng, J., Kim, S. M., Hyun, C. L., Ahn, Y. S. and Hyun, J. W. (2014) The polyphenol chlorogenic acid attenuates UVB-mediated oxidative stress in human HaCaT keratinocytes. Biomol. Ther. 22, 136-142. DOI ScienceOn
6	Cheng, L., Cao, W., Behar, J., Biancani, P. and Harnett, K. M. (2005a) Inflammation induced changes in arachidonic acid metabolism in cat LES circular muscle. Am. J. Physiol. Gastrointest. Liver Physiol. 288, G787-797. DOI
7	Dent, J., El-Serag, H. B., Wallander, M. A. and Johansson, S. (2005) Epidemiology of gastro-oesophageal reflux disease: a systematic review. Gut 54, 710-717. DOI ScienceOn
8	Farah, A., Monteiro, M., Donangelo, C. M. and Lafay, S. (2008) Chlorogenic acids from green coffee extract are highly bioavailable in humans. J. Nutr. 138, 2309-2315. DOI ScienceOn
9	Sato, Y., Itagaki, S., Kurokawa, T., Ogura, J., Kobayashi, M., Hirano, T., Sugawara, M. and Iseki, K. (2011) In vitro and in vivo antioxidant properties of chlorogenic acid and caffeic acid. Int. J. Pharm. 403, 136-138. DOI ScienceOn
10	Seol, S. Y., Kim, M. H., Ryu, J. S., Choi, M. G., Shin, D. W. and Ahn, B. O. (2004) DA-9601 for erosive gastritis: results of a double-blind placebo-controlled phase III clinical trial. World J. Gastroenterol. 10, 2379-2382. DOI
11	Shan, J., Fu, J., Zhao, Z., Kong, X., Huang, H., Luo, L. and Yin, Z. (2009) Chlorogenic acid inhibits lipopolysaccharide-induced cyclooxygenase-2 expression in RAW264.7 cells through suppressing NF-kappaB and JNK/AP-1 activation. Int. Immunopharmacol. 9, 1042-1048. DOI ScienceOn
12	Shimoyama, A. T., Santin, J. R., Machado, I. D., de Oliveira e Silva, A. M., de Melo, I. L., Mancini-Filho, J. and Farsky, S. H. (2013) Antiulcerogenic activity of chlorogenic acid in different models of gastric ulcer. Naunyn Schmiedebergs Arch. Pharmacol. 386, 5-14. DOI
13	Souza, R. F., Huo, X., Mittal, V., Schuler, C. M., Carmack, S. W., Zhang, H. Y., Zhang, X., Yu, C., Hormi-Carver, K., Genta, R. M. and Spechler, S. J. (2009) Gastroesophageal reflux might cause esophagitis through a cytokine-mediated mechanism rather than caustic acid injury. Gastroenterology 137, 1776-1784. DOI ScienceOn
14	Stalmach, A., Steiling, H., Williamson, G. and Crozier, A. (2010) Bioavailability of chlorogenic acids following acute ingestion of coffee by humans with an ileostomy. Arch. Biochem. Biophys. 501, 98-105. DOI
15	Tuan, P. A., Thwe, A. A., Kim, Y. B., Kim, J. K., Kim, S. J., Lee, S., Chung, S. O. and Park, S. U. (2013) Effects of white, blue, and red light-emitting diodes on carotenoid biosynthetic gene expression levels and carotenoid accumulation in sprouts of tartary buckwheat (Fagopyrum tataricum Gaertn.). J. Agric. Food Chem. 61, 12356-12361. DOI
16	Hayakawa, T., Fujiwara, Y., Hamaguchi, M., Sugawa, T., Okuyama, M., Sasaki, E., Watanabe, T., Tominaga, K., Oshitani, N., Higuchi, K. and Arakawa, T. (2006) Roles of cyclooxygenase 2 and microsomal prostaglandin E synthase 1 in rat acid reflux oesophagitis. Gut 55, 450-456. DOI
17	Farhadi, A., Fields, J., Banan, A. and Keshavarzian, A. (2002) Reactive oxygen species: are they involved in the pathogenesis of GERD, Barrett's esophagus, and the latter's progression toward esophageal cancer? Am. J. Gastroenterol. 97, 22-26. DOI ScienceOn
18	Feng, R., Lu, Y., Bowman, L. L., Qian, Y., Castranova, V. and Ding, M. (2005) Inhibition of activator protein-1, NF-kappaB, and MAPKs and induction of phase 2 detoxifying enzyme activity by chlorogenic acid. J. Biol. Chem. 280, 27888-27895. DOI ScienceOn
19	Griffith, O. W. (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal. Biochem. 106, 207-212. DOI ScienceOn
20	Ismail-Beigi, F., Horton, P. F. and Pope, C. E., 2nd (1970) Histological consequences of gastroesophageal reflux in man. Gastroenterology 58, 163-174.
21	Katz, P. O. (2003) Optimizing medical therapy for gastroesophageal reflux disease: state of the art. Rev. Gastroenterol. Disord. 3, 59-69.
22	Ku, S. K., Seo, B. I., Park, J. H., Park, G. Y., Seo, Y. B., Kim, J. S., Lee, H. S. and Roh, S. S. (2009) Effect of Lonicerae Flos extracts on reflux esophagitis with antioxidant activity. World J. Gastroenterol. 15, 4799-4805. DOI ScienceOn
23	Lee, C. H., Yoon, S. J. and Lee, S. M. (2012) Chlorogenic acid attenuates high mobility group box 1 (HMGB1) and enhances host defense mechanisms in murine sepsis. Mol. Med. 18, 1437-1448.
24	Wilson, K. T., Fu, S., Ramanujam, K. S. and Meltzer, S. J. (1998). Increased expression of inducible nitric oxide synthase and cyclooxygenase-2 in Barrett's esophagus and associated adenocarcinomas. Cancer Res. 58, 2929-2934.
25	Wetscher, G. J., Hinder, P. R., Bagchi, D., Perdikis, G., Redmond, E. J., Glaser, K., Adrian, T. E. and Hinder, R. A. (1995a) Free radical scavengers prevent reflux esophagitis in rats. Dig. Dis. Sci. 40, 1292-1296. DOI
26	Wetscher, G. J., Hinder, R. A., Bagchi, D., Hinder, P. R., Bagchi, M., Perdikis, G. and McGinn, T. (1995b) Reflux esophagitis in humans is mediated by oxygen-derived free radicals. Am. J. Surg. 170, 552-556. DOI ScienceOn
27	Wetscher, G. J., Perdikis, G., Kretchmar, D. H., Stinson, R. G., Bagchi, D., Redmond, E. J., Adrian, T. E. and Hinder, R. A. (1995c) Esophagitis in Sprague-Dawley rats is mediated by free radicals. Dig. Dis. Sci. 40, 1297-1305. DOI ScienceOn
28	Yun, N., Kang, J. W., Lee, S. M. (2012) Protective effects of chlorogenic acid against ischemia/reperfusion injury in rat liver: molecular evidence of its antioxidant and anti-inflammatory properties. J. Nutr. Biochem. 23, 1249-1255. DOI
29	Miwa, H., Oshima, T., Sakurai, J., Tomita, T., Matsumoto, T., Iizuka, S. and Koseki, J. (2009) Experimental oesophagitis in the rat is associated with decreased voluntary movement. Neurogastroenterol. Motil. 21, 296-303. DOI ScienceOn
30	Maity, S., Vedasiromoni, J. R. and Ganguly, D. K. (1998) Role of glutathione in the antiulcer effect of hot water extract of black tea (Camellia sinensis). Jpn. J. Pharmacol. 78, 285-292. DOI
31	Oh, T. Y., Lee, J. S., Ahn, B. O., Cho, H., Kim, W. B., Kim, Y. B., Surh, Y. J., Cho, S. W. and Hahm, K. B. (2001a) Oxidative damages are critical in pathogenesis of reflux esophagitis: implication of antioxidants in its treatment. Free Radic. Biol. Med. 30, 905-915. DOI ScienceOn
32	Oh, T. Y., Lee, J. S., Ahn, B. O., Cho, H., Kim, W. B., Kim, Y. B., Surh, Y. J., Cho, S. W., Lee, K. M. and Hahm, K. B. (2001b) Oxidative stress is more important than acid in the pathogenesis of reflux oesophagitis in rats. Gut 49, 364-371. DOI ScienceOn
33	Omura, N., Kashiwagi, H., Chen, G., Suzuki, Y., Yano, F. and Aoki, T. (1999) Establishment of surgically induced chronic acid reflux esophagitis in rats. Scand. J. Gastroenterol. 34, 948-953. DOI
34	Rafiee, P., Nelson, V. M., Manley, S., Wellner, M., Floer, M., Binion, D. G. and Shaker, R. (2009) Effect of curcumin on acidic pH-induced expression of IL-6 and IL-8 in human esophageal epithelial cells (HET-1A): role of PKC, MAPKs, and NF-kappaB. Am. J. Physiol. Gastrointest. Liver Physiol. 296, G388-398. DOI
35	Reimer, C., Sondergaard, B., Hilsted, L. and Bytzer, P. (2009) Protonpump inhibitor therapy induces acid-related symptoms in healthy volunteers after withdrawal of therapy. Gastroenterology 137, 80-87, 87e1. DOI
36	Robert, A., Eberle, D. and Kaplowitz, N. (1984) Role of glutathione in gastric mucosal cytoprotection. Am. J. Physiol. 247, G296-304.
37	Cheng, L., Cao, W., Fiocchi, C., Behar, J., Biancani, P. and Harnett, K. M. (2005b) Platelet-activating factor and prostaglandin E2 impair esophageal ACh release in experimental esophagitis. Am. J. Physiol. Gastrointest. Liver Physiol. 289, G418-428. DOI

	O Jun Kwon. (2016) Evidence-Based Complementary and Alternative Medicine Antioxidant and Anti-Inflammatory Effects of Rhei Rhizoma and Coptidis Rhizoma Mixture on Reflux Esophagitis in Rats / 2016 , 1
	Jung-Woo Kang. (2014) Evidence-Based Complementary and Alternative Medicine Protective Effect ofFlos Loniceraeagainst Experimental Gastric Ulcers in Rats: Mechanisms of Antioxidant and Anti-Inflammatory Action / 2014 , 1
	Palaniyandi Akila. (2017) Biomedicine & Pharmacotherapy Chlorogenic acid ameliorates isoproterenol-induced myocardial injury in rats by stabilizing mitochondrial and lysosomal enzymes / 85 , 582
10	Ji Hyun Song. (2016) Free Radical Research Oxidative stress from reflux esophagitis to esophageal cancer: the alleviation with antioxidants / 50 (10) , 1071
1	O Jun Kwon. (2015) BMC Complementary and Alternative Medicine Protective effect of Rhei Rhizoma on reflux esophagitis in rats via Nrf2-mediated inhibition of NF-κB signaling pathway / 16 (1)
2	(2019) Journal of Medicinal Food , Has a Gastroprotective Effect via Antioxidant and Anti-Inflammatory Activities / 22 (2) , 140
1	(2014) Applied Biological Chemistry Geraniin ameliorate experimental acute reflux esophagitis via NF-κB regulated anti-inflammatory activities in rats / 62 (1) , 13
2	Sayuko Shiraishi. (2017) CHEMICAL & PHARMACEUTICAL BULLETIN Taste-Masking Effect of Chlorogenic Acid (CGA) on Bitter Drugs Evaluated by Taste Sensor and Surface Plasmon Resonance on the Basis of CGA–Drug Interactions / 65 (2) , 127
2	(2017) Molecular Medicine Reports Chlorogenic acid prevents inflammatory responses in IL-1β-stimulated human SW-1353 chondrocytes, a model for osteoarthritis / 16 (2) , 1369
12	(2017) Journal of Medicinal Food Low-Molecular-Weight Oligonol, a Polyphenol Derived from Lychee Fruit, Attenuates Experimental Reflux Esophagitis and HCl/Ethanol-Induced Gastric Ulcer / 20 (12) , 1214
11	(2018) International Journal of Molecular Sciences Dichloromethane Extracts of Geranium Koreanum Kom. Alleviates Esophagus Damage in Acute Reflux Esophagitis-Induced Rats by Anti-Inflammatory Activities / 19 (11) , 3622
67	(2020) Pharmacognosy magazine Ethanol extract of Magnolia sieboldii buds ameliorated esophageal tissue injury induced by gastric acid reflux in rats via regulating the nuclear factor-κB signaling pathway / 16 (67) , 161
1	(2014) Gut and liver The Efficacy and Safety of GCWB104 ( <I>Flos Lonicera</I> Extract) in Functional Dyspepsia: A Single-Center, Randomized, Double-Blind, Placebo-Controlled Study / 14 (1) , 67
3	(2014) Antioxidants Inhibitory Effects of <I>Urtica thunbergiana</I> Ethanol Extract on Atopic Dermatitis-Induced NC/Nga Mice / 9 (3) , 197
9	(2020) Phytotherapy research : PTR Ameliorative effects of <I>Magnolia sieboldii</I> buds hexane extract on experimental reflux esophagitis / 34 (9) , 2385
1	(2014) Applied Biological Chemistry Costunolide inhibits inflammation in LPS-induced RAW264.7 cells and ameliorates gastric acid reflux-induced esophageal injury in rat model / 63 (1) , 33
1	(2014) Nutrients The Impact of Whole Grain Intake on Gastrointestinal Tumors: A Focus on Colorectal, Gastric, and Esophageal Cancers / 13 (1) , 81
None	(2014) BioMed research international Protective Effects of Inflammation of Curcumae Longae Rhizoma 30% EtOH Extract on Acute Reflux Esophagitis Rats / 2021 (None) , 8854945
10	(2014) Nutrients Lifestyle, WCRF/AICR Recommendations, and Esophageal Adenocarcinoma Risk: A Systematic Review of the Literature / 13 (10) , 3525