Preventive and ameliorating effects of citrus D-limonene on dyslipidemia and hyperglycemia in mice with high-fat diet-induced obesity

European Journal of Pharmacology

Volumn 715, Issue 1-3, 2013, Pages 46-55

  Jing, Li ^a,b   Zhang, Yu ^c   Fan, Shengjie ^c   Gu, Ming ^c   Guan, Yu ^c   Lu, Xiong ^c   Huang, Cheng ^c   Zhou, Zhiqin ^a,b  

^a SOUTHWEST UNIVERSITY   (China)

^b BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

^c SHANGHAI UNIVERSITY OF TRADITIONAL CHINESE MEDICINE   (China)

Author keywords

D limonene; Dyslipidemia; Hyperglycemia; Metabolic disorder

Indexed keywords

5,7 DIMETHOXYCOUMARIN; AURANTIIN; AURAPTENE; DIOSMIN; GERANIOL; GLUCOSE; HESPERETIN; HESPERIDIN; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; ISOBERGAPTEN; LIMONENE; LIVER X RECEPTOR BETA; LOW DENSITY LIPOPROTEIN CHOLESTEROL; NARINGENIN; NARIRUTIN; NEOERIOCITRIN; NEOHESPERIDIN; NEOSPERIDINDIHYDROCHALCONE; NEROL; NOBILETIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PONCIRIN; QUERCETIN; RUTOSIDE; SANGUINARINE CITRATE; TANGERITIN; TRIACYLGLYCEROL; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; BROWN ADIPOSE TISSUE; CHOLESTEROL BLOOD LEVEL; CITRUS; CONTROLLED STUDY; DYSLIPIDEMIA; FEMALE; FOOD INTAKE; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE; HYPERGLYCEMIA; LIPID DIET; LIPID LIVER LEVEL; METABOLIC DISORDER; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; SERIAL ANALYSIS OF GENE EXPRESSION; THERAPY EFFECT; TRIACYLGLYCEROL BLOOD LEVEL; WHITE ADIPOSE TISSUE;

D-LIMONENE; DYSLIPIDEMIA; HYPERGLYCEMIA; METABOLIC DISORDER;

3T3-L1 CELLS; ADIPOCYTES; ANIMALS; BODY WEIGHT; CELL DIFFERENTIATION; CELL SIZE; CITRUS; CYCLOHEXENES; DIET, HIGH-FAT; DIETARY SUPPLEMENTS; DYSLIPIDEMIAS; FEMALE; GENE EXPRESSION REGULATION; GLUCOSE; HYPERGLYCEMIA; LIPIDS; LIVER; MICE; MICE, INBRED C57BL; OBESITY; ORPHAN NUCLEAR RECEPTORS; PPAR ALPHA; SIGNAL TRANSDUCTION; TERPENES;

EID: 84885479203     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2013.06.022     Document Type: Article

References (42)

1. Ahima, R.S., 2011. Digging deeper into obesity. J. Clin. Invest. 121, 2076-2079.
2. Bakkali, F., Averbeck, S., Averbeck, D., Idaomar, M., 2008. Biological effects of essential oils - a review. Food Chem. Toxicol. 46, 446-475. (Pubitemid 350297552)
3. Barter, P.J., Rye, K.-A., 2008. Is there a role for fibrates in the management of dyslipidemia in the metabolic syndrome? Arteriosclerosis, Thrombosis, Vascular Biol. 28, 39-46.
4. Berger, J.P., Akiyama, T.E., Meinke, P.T., 2005. PPARs: therapeutic targets for metabolic disease. Trends Pharmacol. Sci. 26, 244-251. (Pubitemid 40603072)
5. Canbakan, B., Tahan, V., Balci, H., Hatemi, I., Erer, B., Ozbay, G., Sut, N., Hacibekiroglu, M., Imeryuz, N., Senturk, H., 2008. Leptin in nonalcoholic fatty liver disease. Ann. Hepatol. 7, 249-254.
6. Chun, T.-H., Inoue, M., Morisaki, H., Yamanaka, I., Miyamoto, Y., Okamura, T., Sato-Kusubata, K., Weiss, S.J., 2010. Genetic link between obesity and MMP14-dependent adipogenic collagen turnover. Diabetes 59, 2484-2494.
7. Chung, M.J., Cho, S.-Y, Bhuiyan, M.J.H., Kim, K.H., Lee, S.-J., 2010. Anti-diabetic effects of lemon balm (Melissa officinalis) essential oil on glucose- and lipid-regulating enzymes in type 2 diabetic mice. Br. J. Nutr. 104, 180-188.
8. Clegg, R.J., Middleton, B., Bell, G.D., White, D.A., 1980. Inhibition of hepatic cholesterol synthesis and S-3-hydroxy-3-methylglutaryl-CoA reductase by mono and bicyclic monoterpenes administered in vivo. Biochem. Pharmacol. 29, 2125-2127. (Pubitemid 10086433)
9. Clegg, R.J., Middleton, B., Bell, G.D., White, DA, 1982. The mechanism of cyclic monoterpene inhibition of hepatic 3-hydroxy-3-methylglutaryl coenzyme A reductase in vivo in the rat. J. Biol. Chem. 257, 2294-2299. (Pubitemid 12069783)
10. Eberlé, D., Clément, K., Meyre, D., Sahbatou, M., Vaxillaire, M., Le Gall, A., Ferré, P., Basdevant, A., Froguel, P., Foufelle, F., 2004. SREBF-1 gene polymorphisms are associated with obesity and type 2 diabetes in French obese and diabetic cohorts. Diabetes 53, 2153-2157. (Pubitemid 38970769)
11. Fukumoto, S., Morishita, A., Furutachi, K., Terashima, T., Nakayama, T, Yokogoshi, H., 2008. Effect of flavour components in lemon essential oil on physical or psychological stress. Stress Health 24, 3-12. (Pubitemid 351314260)
12. Gabbi, C, Warner, M., Gustafsson, J.-Å., 2009. Minireview: Liver X Receptor β: emerging roles in physiology and diseases. Mol. Endocrinol. 23, 129-136.
13. Genest, J., Frohlich, J., Fodor, G., McPherson, R., 2003. Recommendations for the management of dyslipidemia and the prevention of cardiovascular disease: summary of the 2003 update. Can. Med. Assoc. J. 169, 921-924. (Pubitemid 37372465)
14. Goldberg, R.B., Kendall, D.M., Deeg, M.A., Buse, J.B., Zagar, A.J., Pinaire, JA, and Tan., M. H., Khan, M.A., Perez, A.T., Jacober, S.J., 2005. A comparison of lipid and glycemic effects of pioglitazone and rosiglitazone in patients with type 2 diabetes and dyslipidemia. Diabetes Care 28, 1547-1554. (Pubitemid 40923063)
15. Goldwasser, J., Cohen, P.Y, Yang, E., Balaguer, P., Yarmush, M.L, Nahmias, Y, 2010. Transcriptional regulation of human and rat hepatic lipid metabolism by the grapefruit flavonoid naringenin: role of PPARα, PPARγ and LXRα. PLoS ONE 5, e12399.
16. Gong, Z., Huang, C, Sheng, X., Zhang, Y, Li, Q., Wang, M.-W, Peng, L., Zang, Y.Q., 2009. The Role of Tanshinone IIA in the treatment of obesity through peroxisome proliferator-activated receptor y antagonism. Endocrinology 150, 104-113.
17. Jay, M.A., Ren, J., 2007. Peroxisome proliferator-activated receptor (PPAR) in metabolic syndrome and type 2 diabetes mellitus. Curr. Diabetes Rev. 3, 33-39. (Pubitemid 46592792)
18. Kawakami, K., Kawamoto, M., Nomura, M., Otani, H., Nabika, T., Gonda, T., 2004. Effects of phytoncides on blood pressure under restraint stress in SHRSP. Clin. Exp. Pharmacol. Physiol. 31, S27-S28.
19. Keen, H.L., Ryan, M.J., Beyer, A., Mathur, S., Scheetz, T.E., Gackle, B.D., Faraci, F.M., Casavant, T.L, Sigmund, C.D., 2004. Gene expression profiling of potential PPARγ target genes in mouse aorta. Physiol. Genomics 18, 33-42. (Pubitemid 39319484)
20. Kim, G.-S., Park, H.J., Woo, J.-H., Kim, M.-K., Koh, P.-O., Min, W, Ko, Y.-G., Kim, C.-H., Won, C.-K., Cho, J.-H., 2012a. Citrus aurantium flavonoids inhibit adipogenesis through the Akt signaling pathway in 3T3-L1 cells. BMC Complementary Alternative Med. 12, 31.
21. Kim, Y.-i., Hirai, S., Goto, T, Ohyane, C, Takahashi, H., Tsugane, T., Konishi, C, Fujii, T, Inai, S., Iijima, Y, Aoki, K., Shibata, D., Takahashi, N., Kawada, T., 2012b. Potent PPARα activator derived from tomato juice, 13-oxo-9,11-octadecadienoic acid, decreases plasma and hepatic triglyceride in obese diabetic mice. PLoS ONE 7, e31317.
22. Kumar Sharma, A., Bharti, S., Ojha, S., Bhatia, J., Kumar, N., Ray, R., Kumari, S., Singh Arya, D., 2011. Up-regulation of PPARγ, heat shock protein-27 and -72 by naringin attenuates insulin resistance, β-cell dysfunction, hepatic steatosis and kidney damage in a rat model of type 2 diabetes. Br. J. Nutr. 106, 1713-1723.
23. Miller, J., Thompson, P., Hakim, I., Chow, H.H.S., Thomson, C, 2011. D-Limonene: a bioactive food component from citrus and evidence for a potential role in breast cancer prevention and treatment. Oncol. Rev. 5, 31-42.
24. Mulvihill, E.E., Allister, E.M., Sutherland, B.G., Telford, D.E., Sawyez, CG., Edwards, J.Y, Markle, J.M., Hegele, RA, Huff, M.W, 2009. Naringenin prevents dyslipidemia, apolipoprotein B overproduction, and hyperinsulinemia in LDL receptor-null mice with diet-induced insulin resistance. Diabetes 58, 2198-2210.
25. Pandima Devi, K., Sreepriya, M., Balakrishna, K., Devaki, T., 2004. Protective effect of Premna tomentosa (L Verbenaceae) extract on membrane-bound phosphatases and inorganic cations transport in acetaminophen-induced hepatotoxicity rats. J. Ethnopharmacol. 93, 371-375. (Pubitemid 38962431)
26. Pruessner, J.C., Kirschbaum, C, Meinlschmid, G., Hellhammer, D.H., 2003. Two formulas for computation of the area under the curve represent measures of total hormone concentration versus time-dependent change. Psychoneuroen- docrinology 28, 916-931. (Pubitemid 36936799)
27. Rakhshandehroo, M., Knoch, B., Müller, M., Kersten, S., 2010. Peroxisome proliferator-activated receptor alpha target genes. PPAR Research 2010, 1-20, http://dx.doi.org/10.1155/2010/612089.
28. Repa, J.J., Mangelsdorf, D.J., 2000. The role of orphan nuclear receptors in the regulation of cholesterol homeostasis. Annu. Rev. Cell Dev. Biol. 16, 459-481. (Pubitemid 32037514)
29. Seidell, J.C., 1995. The impact of obesity on health status: some implications for health care costs. Int. J. Obesity Relat. Metab. Disord.: J. Int. Assoc. Study Obesity 19 (6), S13-S16.
30. Shibata, H., Fujiwara, R., Iwamoto, M., Matsuoka, H., Yokoyama, M.M., 1991. Immunological and behavioral effects of fragrance in mice. Int. J. Neurosci. 57, 151-159.
31. Shu, G., 2010. Use of volatile oil from plants in preparing medicaments for preventing and treating diabetes. Google Patents.
32. Staels, B., 2007. PPAR agonists and the metabolic syndrome. Therapie 62, 319-326. (Pubitemid 351211747)
33. Sun, J., 2007. D-Limonene: safety and clinical applications. Alternative Med. Rev. 12, 259.
34. Tiraby, C, Langin, D., 2003. Conversion from white to brown adipocytes: a strategy for the control of fat mass? Trends Endocrinol. Metab. 14, 439-441. (Pubitemid 37517342)
35. Tontonoz, P., Mangelsdorf, D.J., 2003. Liver X Receptor signaling pathways in cardiovascular disease. Mol. Endocrinol. 17, 985-993. (Pubitemid 36683707)
36. Ulven, S.M., Dalen, K.T., Gustafsson, J.-Å., Nebb, H.I., 2004. Tissue-specific autoregulation of the LXRα gene facilitates induction of apoE in mouse adipose tissue. J. Lipid Res. 45, 2052-2062. (Pubitemid 41001296)
37. Santiago, Victor Antony, Jayachitra, J., Shenbagam, J., Nalini, N. M., 2012. Dietary D-limonene alleviates insulin resistance and oxidative stress-induced liver injury in high-fat diet and L-NAME-treated rats. Eur. J. Nutr. 51, 57-68.
38. Vigushin, D.M., Poon, G.K., Boddy, A., English, J., Halbert, G.W., Pagonis, C., Jarman, M., Coombes, R.C., 1998. Phase I and pharmacokinetic study of D-limonene in patients with advanced cancer. Cancer Chemother. Pharmacol. 42, 111-117. (Pubitemid 28267291)
39. Wang, Y.C., McPherson, K., Marsh, T., Gortmaker, S.L., Brown, M., 2011. Health and economic burden of the projected obesity trends in the USA and the UK. The Lancet 378, 815-825.
40. Yang, X., Zhao, H., Wang, J., Meng, Q., Zhang, H., Yao, L., Zhang, Y., Dong, A., Ma, Y., Wang, Z., 2010. Chemical composition and antioxidant activity of essential oil of pine cones of Pinus armandii from the southwest region of China. J. Med. Plants Res. 4, 1668-1672.
41. Yoon, M., 2009. The role of PPARα in lipid metabolism and obesity: focusing on the effects of estrogen on PPARα actions. Pharmacol. Res. 60, 151-159.
42. Yun, J.W., 2010. Possible anti-obesity therapeutics from nature - a review. Phytochemistry 71, 1625-1641.