Camphene, a plant-derived monoterpene, reduces plasma cholesterol and triglycerides in hyperlipidemic rats independently of HMG-CoA reductase activity

PLoS ONE

Volumn 6, Issue 11, 2011, Pages

  Vallianou, Ioanna ^a   Peroulis, Nikolaos ^a   Pantazis, Panayotis ^b   Hadzopoulou Cladaras, Margarita ^a  

^a ARISTOTLE UNIVERSITY OF THESSALONIKI   (Greece)

^b ADNA Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA PINENE; CAMPHENE; CARYOPHYLLENE; CHOLESTEROL; CHOLESTEROL ESTER; DETERGENT; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; LINALOOL; LOW DENSITY LIPOPROTEIN CHOLESTEROL; MEVINOLIN; MYRCENE; PINENE; PLACEBO; TERPENE; TRIACYLGLYCEROL; TYLOXAPOL; 3 HYDROXY 3 METHYLGLUTARYL COENZYME A; 3-HYDROXY-3-METHYLGLUTARYL-COENZYME A; ACYL COENZYME A; ANTILIPEMIC AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL STRAIN HEPG2; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL SYNTHESIS; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG ACTIVITY; DRUG DOSE COMPARISON; ENZYME ACTIVITY; FEMALE; GAS CHROMATOGRAPHY; HUMAN; HUMAN CELL; HYPERLIPIDEMIA; HYPOCHOLESTEROLEMIC ACTIVITY; HYPOTRIGLYCERIDEMIC ACTIVITY; NONHUMAN; PISTACIA LENTISCUS; RAT; TREATMENT OUTCOME; TRIACYLGLYCEROL BLOOD LEVEL; ANIMAL; BLOOD; CELL LINE; DOSE RESPONSE; FISCHER 344 RAT; METABOLISM;

RATTUS;

ACYL COENZYME A; ANIMALS; CELL LINE; CHOLESTEROL; CHROMATOGRAPHY, GAS; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; HUMANS; HYPOLIPIDEMIC AGENTS; RATS; RATS, INBRED F344; TERPENES; TRIGLYCERIDES;

EID: 80455125864     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0020516     Document Type: Article

References (83)

1. Anderson KM, Wilson PW, Garrison RJ, Castelli WP (1987) Longitudinal and secular trends in lipoprotein cholesterol measurements in a general population sample. The Framingham Offspring Study. Atherosclerosis 68: 59-66.
2. Gordon (1972) Predisposition to atherosclerosis in the head, heart, and legs. The Framingham study.
3. Grundy SM (1977) Treatment of hypercholesterolemia. Am J Clin Nutr 30: 985-992.
4. ExpertPanel (2002) Third Report of the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III) final report. Circulation 106: 3143-3421.
5. Blankenhorn DH, Johnson RL, Nessim SA, Azen SP, Sanmarco ME, et al. (1987) The Cholesterol Lowering Atherosclerosis Study (CLAS): design, methods, and baseline results. Control Clin Trials 8: 356-387.
6. Grundy SM (1978) Cholesterol metabolism in man. West J Med 128: 13-25.
7. Endo A (1992) The discovery and development of HMG-CoA reductase inhibitors. J Lipid Res 33: 1569-1582.
8. Illingworth DR, Bacon S (1987) Hypolipidemic effects of HMG-CoA reductase inhibitors in patients with hypercholesterolemia. Am J Cardiol 60: 33G-42G.
9. Endo A, Hasumi K (1989) Biochemical aspect of HMG CoA reductase inhibitors. Adv Enzyme Regul 28: 53-64.
10. LaRosa JC, He J, Vupputuri S (1999) Effect of statins on risk of coronary disease: a meta-analysis of randomized controlled trials. Jama 282: 2340-2346.
11. Tobert JA (2003) Lovastatin and beyond: the history of the HMG-CoA reductase inhibitors. Nat Rev Drug Discov 2: 517-526.
12. Vaughan CJ, Gotto AM, Jr., Basson CT (2000) The evolving role of statins in the management of atherosclerosis. J Am Coll Cardiol 35: 1-10.
13. Al-Habbal MJ, Al-Habbal Z, Huwez FU (1984) A double-blind controlled clinical trial of mastic and placebo in the treatment of duodenal ulcer. Clin Exp Pharmacol Physiol 11: 541-544.
14. Marone P, Bono L, Leone E, Bona S, Carretto E, et al. (2001) Bactericidal activity of Pistacia lentiscus mastic gum against Helicobacter pylori. J Chemother 13: 611-614.
15. Duru ME, Cakir A, Kordali S, Zengin H, Harmandar M, et al. (2003) Chemical composition and antifungal properties of essential oils of three Pistacia species. Fitoterapia 74: 170-176.
16. Takahashi K, Fukazawa M, Motohira H, Ochiai K, Nishikawa H, et al. (2003) A pilot study on antiplaque effects of mastic chewing gum in the oral cavity. J Periodontol 74: 501-505.
17. Koutsoudaki C, Krsek M, Rodger A (2005) Chemical composition and antibacterial activity of the essential oil and the gum of Pistacia lentiscus Var. chia. J Agric Food Chem 53: 7681-7685.
18. Aksoy A, Duran N, Toroglu S, Koksal F (2007) Short-term effect of mastic gum on salivary concentrations of cariogenic bacteria in orthodontic patients. Angle Orthod 77: 124-128.
19. Sterer N, Nuas S, Mizrahi B, Goldenberg C, Weiss EI, et al. (2008) Oral malodor reduction by a palatal mucoadhesive tablet containing herbal formulation. J Dent 36: 535-539.
20. Paraschos S, Magiatis P, Mitakou S, Petraki K, Kalliaropoulos A, et al. (2007) In vitro and in vivo activities of Chios mastic gum extracts and constituents against Helicobacter pylori. Antimicrob Agents Chemother 51: 551-559.
21. Sakagami H, Kishino K, Kobayashi M, Hashimoto K, Iida S, et al. (2009) Selective antibacterial and apoptosis-modulating activities of mastic. In Vivo 23: 215-223.
22. Dabos KJ, Sfika E, Vlatta LJ, Giannikopoulos G (2010) The effect of mastic gum on Helicobacter pylori: a randomized pilot study. Phytomedicine 17: 296-299.
23. Al-Said MS, Ageel AM, Parmar NS, Tariq M (1986) Evaluation of mastic, a crude drug obtained from Pistacia lentiscus for gastric and duodenal anti-ulcer activity. J Ethnopharmacol 15: 271-278.
24. Huwez FU, Thirlwell D, Cockayne A, Ala'Aldeen DA (1998) Mastic gum kills Helicobacter pylori. N Engl J Med 339: 1946.
25. Kaliora AC, Stathopoulou MG, Triantafillidis JK, Dedoussis GV, Andrikopoulos NK (2007) Alterations in the function of circulating mononuclear cells derived from patients with Crohn's disease treated with mastic. World J Gastroenterol 13: 6031-6036.
26. Mahmoudi M, Ebrahimzadeh MA, Nabavi SF, Hafezi S, Nabavi SM, et al. (2010) Antiinflammatory and antioxidant activities of gum mastic. Eur Rev Med Pharmacol Sci 14: 765-769.
27. Qiao J, Li A, Jin X, Wang J (2010) Mastic Alleviates Allergic Inflammation in Asthmatic Model Mice by Inhibiting Recruitment of Eosinophils. Am J Respir Cell Mol Biol.
28. Braca A, Dal Piaz F, Marzocco S, Autore G, Vassallo A, et al. (2011) Triterpene derivatives as inhibitors of protein involved in the inflammatory process: molecules interfering with phospholipase a(2), cycloxygenase, and lipoxygenase. Curr Drug Targets 12: 302-321.
29. Zhou L, Satoh K, Takahashi K, Watanabe S, Nakamura W, et al. (2009) Reevaluation of anti-inflammatory activity of mastic using activated macrophages. In Vivo 23: 583-589.
30. Andrikopoulos NK, Kaliora AC, Assimopoulou AN, Papapeorgiou VP (2003) Biological activity of some naturally occurring resins, gums and pigments against in vitro LDL oxidation. Phytother Res 17: 501-507.
31. Loizou S, Paraschos S, Mitakou S, Chrousos GP, Lekakis I, et al. (2009) Chios mastic gum extract and isolated phytosterol tirucallol exhibit anti-inflammatory activity in human aortic endothelial cells. Exp Biol Med (Maywood) 234: 553-561.
32. He ML, Li A, Xu CS, Wang SL, Zhang MJ, et al. (2007) Mechanisms of antiprostate cancer by gum mastic: NF-kappaB signal as target. Acta Pharmacol Sin 28: 446-452.
33. Balan KV, Demetzos C, Prince J, Dimas K, Cladaras M, et al. (2005) Induction of apoptosis in human colon cancer HCT116 cells treated with an extract of the plant product, Chios mastic gum. In Vivo 19: 93-102.
34. He ML, Yuan HQ, Jiang AL, Gong AY, Chen WW, et al. (2006) Gum mastic inhibits the expression and function of the androgen receptor in prostate cancer cells. Cancer 106: 2547-2555.
35. He ML, Chen WW, Zhang PJ, Jiang AL, Fan W, et al. (2007) Gum mastic increases maspin expression in prostate cancer cells. Acta Pharmacol Sin 28: 567-572.
36. Balan KV, Prince J, Han Z, Dimas K, Cladaras M, et al. (2007) Antiproliferative activity and induction of apoptosis in human colon cancer cells treated in vitro with constituents of a product derived from Pistacia lentiscus L. var. chia. Phytomedicine 14: 263-272.
37. Dimas K, Hatziantoniou S, Wyche JH, Pantazis P (2009) A mastic gum extract induces suppression of growth of human colorectal tumor xenografts in immunodeficient mice. In Vivo 23: 63-68.
38. Loutrari H, Magkouta S, Pyriochou A, Koika V, Kolisis FN, et al. (2006) Mastic oil from Pistacia lentiscus var. chia inhibits growth and survival of human K562 leukemia cells and attenuates angiogenesis. Nutr Cancer 55: 86-93.
39. Magkouta S, Stathopoulos GT, Psallidas I, Papapetropoulos A, Kolisis FN, et al. (2009) Protective effects of mastic oil from Pistacia lentiscus variation chia against experimental growth of lewis lung carcinoma. Nutr Cancer 61: 640-648.
40. Moulos P, Papadodima O, Chatziioannou A, Loutrari H, Roussos C, et al. (2009) A transcriptomic computational analysis of mastic oil-treated Lewis lung carcinomas reveals molecular mechanisms targeting tumor cell growth and survival. BMC Med Genomics 2: 68.
41. Dabos KJ, Sfika E, Vlatta LJ, Frantzi D, Amygdalos GI, et al. (2010) Is Chios mastic gum effective in the treatment of functional dyspepsia? A prospective randomised double-blind placebo controlled trial. J Ethnopharmacol 127: 205-209.
42. Magiatis P, Melliou E, Skaltsounis AL, Chinou IB, Mitaku S (1999) Chemical composition and antimicrobial activity of the essential oils of Pistacia lentiscus var. chia. Planta Med 65: 749-752.
43. Papageorgiou VPB-CMN, Apazidou KK, Psarros EE (1997) Gas chromatographic-mass spectroscopic analysis of the acidic triterpenic fraction of mastic gum. Journal of Chromatography A 769: 263-273.
44. Marner F-J, Freyer A, Lex J (1991) Triterpenoids from mastic gum, the resin of Pistacia lentiscus. Phytochemistry 30: 3709-3712.
45. Papageorgiou VP, Mellidis AS, Argyriadou N (1991) The chemical composition of the essential oil of mastic gum. J Essent Oil Res 3: 107-110.
46. Garća-Pelayo MC, Garcća-Peregŕn E, M-C M (2000) An improved assay of 3- hydroxy-3-methylglutaryl-CoA reductase activity in Reuber H35 hepatoma cells without microsomes isolation. Analyst 125: 1583-1585.
47. Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65: 55-63.
48. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37: 911-917.
49. Fiser RH, Jr., Denniston JC, Rindsig RB, Beisel WR (1974) Triglyceride secretion rates: use of Triton WR 1339 in the rhesus monkey. J Nutr 104: 223-226.
50. Kalopissis AD, Griglio S, Malewiak MI, Rozen R (1980) Effect of a high-fat diet on rat very low density lipoprotein secretion. Biochim Biophys Acta 620: 111-119.
51. Kellner A, Correll JW, Ladd AT (1951) Sustained hyperlipemia induced in rabbits by means of intravenously injected surface-active agents. J Exp Med 93: 373-384.
52. Schurr PE, Schultz JR, Parkinson TM (1972) Triton-induced hyperlipidemia in rats as an animal model for screening hypolipidemic drugs. Lipids 7: 68-74.
53. Seok SH, Park JH, Cho SA, Choi SA, Park JH (2004) Cholesterol lowering effect of SG-GN3, the extract of salted and fermented small shrimps, Acetes japonicus, in Triton WR-1339 or high cholesterol-diet induced hypercholesterolemic rats. J Ethnopharmacol 91: 231-235.
54. Busch SJ, Barnhart RL, Martin GA, Flanagan MA, Jackson RL (1990) Differential regulation of hepatic triglyceride lipase and 3-hydroxy-3-methylglutaryl- CoA reductase gene expression in a human hepatoma cell line, HepG2. J Biol Chem 265: 22474-22479.
55. Harper CR, Jacobson TA (2007) The broad spectrum of statin myopathy: from myalgia to rhabdomyolysis. Curr Opin Lipidol 18: 401-408.
56. Kornbrust DJ, MacDonald JS, Peter CP, Duchai DM, Stubbs RJ, et al. (1989) Toxicity of the HMG-coenzyme A reductase inhibitor, lovastatin, to rabbits. J Pharmacol Exp Ther 248: 498-505.
57. Masters BA, Palmoski MJ, Flint OP, Gregg RE, Wang-Iverson D, et al. (1995) In vitro myotoxicity of the 3-hydroxy-3-methylglutaryl coenzyme A reductase inhibitors, pravastatin, lovastatin, and simvastatin, using neonatal rat skeletal myocytes. Toxicol Appl Pharmacol 131: 163-174.
58. Bays H, Stein EA (2003) Pharmacotherapy for dyslipidaemia-current therapies and future agents. Expert Opin Pharmacother 4: 1901-1938.
59. Costet P (2010) Molecular pathways and agents for lowering LDL-cholesterol in addition to statins. Pharmacol Ther 126: 263-278.
60. Dedoussis GV, Kaliora AC, Psarras S, Chiou A, Mylona A, et al. (2004) Antiatherogenic effect of Pistacia lentiscus via GSH restoration and downregulation of CD36 mRNA expression. Atherosclerosis 174: 293-303.
61. Janakat S, Al-Merie H (2002) Evaluation of hepatoprotective effect of Pistacia lentiscus, Phillyrea latifolia and Nicotiana glauca. J Ethnopharmacol 83: 135-138.
62. Triantafyllou A, Chaviaras N, Sergentanis TN, Protopapa E, Tsaknis J (2007) Chios mastic gum modulates serum biochemical parameters in a human population. J Ethnopharmacol 111: 43-49.
63. Kaliora AC, Stathopoulou MG, Triantafillidis JK, Dedoussis GV, Andrikopoulos NK (2007) Chios mastic treatment of patients with active Crohn's disease. World J Gastroenterol 13: 748-753.
64. Kang JS, Wanibuchi H, Salim EI, Kinoshita A, Fukushima S (2007) Evaluation of the toxicity of mastic gum with 13 weeks dietary administration to F344 rats. Food Chem Toxicol 45: 494-501.
65. Sheorain VS, Nageswara Rao T, Subrahmanyam D (1980) On the inhibition of lipoprotein lipase by Triton WR 1339. Enzyme 25: 81-86.
66. Kourounakis AP, Victoratos P, Peroulis N, Stefanou N, Yiangou M, et al. (2002) Experimental hyperlipidemia and the effect of NSAIDs. Exp Mol Pathol 73: 135-138.
67. Lomnicky Y, Friedman M, Luria MH, Raz I, Hoffman A (1998) The effect of the mode of administration on the hypolipidaemic activity of niacin: continuous gastrointestinal administration of low-dose niacin improves lipid-lowering efficacy in experimentally-induced hyperlipidaemic rats. J Pharm Pharmacol 50: 1233-1239.
68. Sirtori CR, Gomarasca P, D'Atri G, Cerutti S, Tronconi G, et al. (1978) Pharmacological profile of BR-931, a new hypolipidemic agent that increases high-density lipoproteins. Atherosclerosis 30: 45-56.
69. Padalia RC, Chanotiya CS, Sundaresan V (2010) Compositional variability in essential oil from different parts of Alpinia speciosa from India. Nat Prod Commun 5: 279-282.
70. Pintore G, Marchetti M, Chessa M, Sechi B, Scanu N, et al. (2009) Rosmarinus officinalis L.: chemical modifications of the essential oil and evaluation of antioxidant and antimicrobial activity. Nat Prod Commun 4: 1685-1690.
71. Satou T, Matsuura M, Murakami S, Hayashi S, Koike K (2009) Composition and seasonal variation of the essential oil from Abies sachalinensis from Hokkaido, Japan. Nat Prod Commun 4: 845-848.
72. Tabanca N, Demirci B, Turner JL, Pounders C, Demirci F, et al. (2010) Microdistillation and analysis of volatiles from eight ornamental Salvia taxa. Nat Prod Commun 5: 1421-1426.
73. Tschiggerl C, Bucar F (2010) Investigation of the Volatile Fraction of Rosemary Infusion Extracts. Sci Pharm 78: 483-492.
74. Verschueren K (2001) fourth ed. Handbook of Environmental Data on Organic Chemicals. John Wiley and Sons, New York 1-2: 419.
75. Tiwari M, Kakkar P (2009) Plant derived antioxidants - Geraniol and camphene protect rat alveolar macrophages against t-BHP induced oxidative stress. Toxicol In Vitro 23: 295-301.
76. Ho SS, Pal S (2005) Margarine phytosterols decrease the secretion of atherogenic lipoproteins from HepG2 liver and Caco2 intestinal cells. Atherosclerosis 182: 29-36.
77. Pal S, Thomson AM, Bottema CD, Roach PD (2002) Polyunsaturated fatty acids downregulate the low density lipoprotein receptor of human HepG2 cells. J Nutr Biochem 13: 55-63.
78. Clegg RJ, Middleton B, Bell GD, White DA (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.
79. Brown MS, Goldstein JL (1974) Suppression of 3-hydroxy-3-methylglutaryl coenzyme A reductase activity and inhibition of growth of human fibroblasts by 7-ketocholesterol. J Biol Chem 249: 7306-7314.
80. Tsutsumi K (2003) Lipoprotein lipase and atherosclerosis. Curr Vasc Pharmacol 1: 11-17.
81. Grundy SM (2005) Stanol esters as a component of maximal dietary therapy in the National Cholesterol Education Program Adult Treatment Panel III report. Am J Cardiol 96: 47D-50D.
82. Plat J, Mensink RP (2005) Plant stanol and sterol esters in the control of blood cholesterol levels: mechanism and safety aspects. Am J Cardiol 96: 15D-22D.
83. Thompson GR, Grundy SM (2005) History and development of plant sterol and stanol esters for cholesterol-lowering purposes. Am J Cardiol 96: 3D-9D.