ABCG5 gene responses to treadmill running with or without administration of Pistachio atlantica in female rats

Document Type : Original Article

Authors

1 Exercise Biochemistry Division, Faculty of Physical Education and Sport Science, University of Mazandaran, Baboulsar, Mazandaran, Iran

2 Tehran Heart Center, Tehran University of Medical Sciences, Tehran, Iran

Abstract

 
Objective(s): ABC transporters comprise a large family of transmembrane proteins that use the energy provided by ATP hydrolysis to translocate a variety of substrates across biological membranes. All members of the human ABCG subfamily, except for ABCG2, are cholesterol-transporter. The aim of this study was to determine the liver, the small intestine and kidney ABCG5 relative gene expression in response to treadmill-running training in female rats.
Materials and Methods: Twenty Wistar rats (6-8 weeks old and 125-135 g weight) were used. Animals were randomly assigned to saline-control (SC), saline-training (ST), and Baneh-control (BC), and Baneh-training (BT) groups. Training groups did the exercise on a motor-driven treadmill at 25 m/min (0% grade) for 60 min/day for eight weeks (5 days/week). Rats were fed orally, with Baneh extraction and saline for six weeks. The two-way ANOVA was employed for statistical analysis.  ABCG5 relative gene expression was detected by Real-time PCR method.
Results:The current findings indicate that the Baneh-treated tissues had significantly lower levels of ABCG5 gene expression in the liver, small intestine, and kidneys (P< 0.001, P< 0.003, P< 0.001, respectively), when compared with saline-treated tissues. However, a higher level of gene expression was observed in exercise groups. A lower level of HDL-c but not triglyceride (TG) and total cholesterol (TC) levels were found in Baneh-treated animals at rest.
Conclusion: Exercise training increases ABCG5 relative gene expression in the liver, small intestine and kidney tissues; therefore exercise training may adjust the reduction of ABCG5 relative gene expression in Baneh-training group.

Keywords

References

 1. Davidson Davidson AL, Chen J. ATP-binding cassette transporters in bacteria. Annu Rev Biochem 2004; 73:241–268.
2. Choi H, Jin J Y, Choi S, Hwang JU, Kim YY, Suh MC,et al. An ABCG/WBC-type ABC transporter is essential for transport of sporopollenin precursors for exine formation in developing pollen. Plant J 2011; 65:181-193.
3. Mcfarlane HE, Shin JJ, Birdb DA, Samuelsa AL. Arabidopsis ABCG transporters, which are required for Ghanbari-Niaki et al Endurance exercise running and tissues ABCG5 gene expression export of diverse cuticular lipids, dimerize in different combinations. Plant Cell 2010; 22:3066-3075.
4. Ozvegy C, Litman T, Szakلcsc G, Nagyd Z, Batese S, Sarkadi B,et al. Functional characterization of the human multidrug transporter, ABCG2, expressed in insect cells. Biochem Biophys Res Commun 2001; 285:111-117.
5. Xu J, Liu Y, Yang Y, Bates S, Ting Zhang J. Characterization of oligomeric human half-ABC transporter ATP-binding cassette G2. J Biol Chem 2004; 279:19781-19789.
6. Kusuhara H, Sugiyama Y. ATP-binding cassette, subfamily G (ABCG family). Pflügers Arch 2007; 453:735–744.
7. Dikkers A, Tietge UJ. Biliary cholesterol secretion: More than a simple ABC. World J Gastroenterol 2010; 16:5936-5945.
8. Graf GA, Li WP, Gerard RD, Gelissen I, White A, Cohen JC,et al. Coexpression of ATP-binding cassette proteins ABCG5 and ABCG8 permits their transport to the apical surface . J Clin Invest 2002; 110:659–669.
9. Graf GA, Yu L, Li WP, Gerard R, Tuma PL, Cohen JC,et al. ABCG5 and ABCG8 are obligate heterodimers for protein trafficking and biliary cholesterol excretion. J Biol Chem 2003; 278:48275- 48282.
10. Graf GA, Cohen JC, Hobbs HH. Missense mutations in ABCG5 and ABCG8 disrupt heterodimerization and trafficking. J Biol Chem 2004; 279:24881–24888.
11. Berge KE, Tian H, Graf GA, Yu L, Grishin NV, Schultz J,et al. Accumulation of dietary cholesterol in sitosterolemia caused by mutations in adjacent ABC transporters. Science 2000; 5497:1771–1775.
12. Hubacek JA, Berge KE, Cohen JC, Hobbs HH. Mutations in ATP-cassette binding proteins G5 (ABCG5) and G8 (ABCG8) causing sitosterolemia. Hum Mutat 2001; 4:359–360.
13. Lee MH, Lu K, Hazard S, Yu H, Shulenin S, Hidaka H,et al. Identification of a gene, ABCG5, important in the regulation of dietary cholesterol absorption. Nat Genet 2001; 1:79–83
14. Lu K, Lee MH, Hazard S, Brooks-Wilson A, Hidaka H, Kojima H,et al. Two genes that map to the STSL locus cause sitosterolemia: Genomic structure and spectrum of mutations involving sterolin-1 and sterolin-2,Encoded by ABCG5 and ABCG8, respectively. Am J Hum Genet 2001; 2:278–290.
15. Shulenin S, Schriml LM, Remaley AT, Fojo S, Brewer B, Allikmets R, Dean M. An ATP-binding cassette gene (ABCG5) from the ABCG (White) gene subfamily maps to human chromosome 2p21 in the region of the Sitosterolemia locus. Cytogenet Cell Genet 2001; 92:204–208.
16. Yu L, Hammer Re, Li-Hawkins J, Von Bergmann K, Lutjohann D, Cohen JC, et al. Disruption of Abcg5 and Abcg8 in mice reveals their crucial role in biliary cholesterol secretion. Proc Natl Acad Sci U S A 2002a; 99:16237-16242.
17. Yu L, Li-Hawkins J, Hamme RE, Berge KE, Horton JD, Cohen JC,et al. Overexpression of ABCG5 and ABCG8 promotes biliary cholesterol secretion and reduces fractional absorption of dietary cholesterol. J Clin Invest 2002b; 110:671-680.
18. Belamarich PF, Deckelbaum RJ, Starc TJ, Dobrin BE, Tint GS, Salen G. Response to diet and cholestyraminein a patient with sitosterolemia. Pediatrics 1990; 6:977–981.
19. Bhattacharyya AK, Connor WE. Beta-sitosterolemia and xanthomatosis, A newly described lipid storage disease in two sisters. J Clin Invest 1974; 53:1033–1043.
20. Morganroth J, Levy RI, Mcmahon AE, Gotto AM. Pseudohomozygous type II hyperlipoproteinemia. J Pediatr 1974; 85: 639–643.
21. Salen G, Shefer S, Nguyen L Ness GC, Tint G. S, Shore V. Sitosterolemia. J Lipid Res 1992;7:945–955.
22. Beaty TH, Kwiterovich POJr, Khoury MJ, White S, Bachorik PS, Smith HH,et al. Genetic analysis of plasma sitosterol, apoprotein B, and lipoproteins in a large Amish pedigree with sitosterolemia. Am J Hum Genet 1986; 4:492–504.
23. Gregg Re, Connor WE, Lin DS, Brewer, HB. Abnormal metabolism of shellfish sterols in a patient with sitosterolemia and xanthomatosis. J Clin Invest 1986; 6:1864–1872.
24. Nguyen LB, Shefer S, Salen G, Ness GC, Tint G, Zaki FG, et al. A molecular defect in hepatic cholesterol biosynthesis in sitosterolemia with xanthomatosis. J Clin Invest 1990; 3:923–931.
25. Miettinen TA. Phytosterolaemia, xanthomatosis and premature atherosclerotic arterial disease: a case with high plant sterol absorption, impaired sterol elimination and low cholesterol synthesis. Eur J Clin Invest 1980; 10:27–35.
26. Mymin D, Wang J, Frohlich J, Hegele RA. Image in cardiovascular medicine. Aortic xanthomatosis with coronary ostial occlusion in a child homozygous for a nonsense mutation in ABCG8. Circulation 2003; 5;791.
27. Glueck CJ, Speirs J, Tracy T, Streicher P, Illig E, Vandegrift J. Relationships of serum plant sterols (phytosterols) and cholesterol in 595 hypercholesterole-mic subjects, and familial aggregation of phytosterols, cholesterol, and premature coronary heart disease in hyperphytosterolemic probands and their first-degree relatives. Metabolism 1991; 8:842–848.
28. Sudhop T, Gottwald BM, Von Bergmann K. Serum plant sterols as a potential risk factor for coronary heart disease. Metabolism 2002; 12:1519–1521.
29. Wang H, Wu G, Park HJ, Jiang PP, Sit WH, van Griensven LJ,et al. Protective effect of Phellinus linteus polysaccharide extracts against thioacetamide-induced liver fibrosis in rats: a proteomics analysis. Chin Med 2012; 7:23.
30. Shi J, Tian J, Zhang X, Wei M, Yin L, Wang P,et al. A combination extract of ginseng, epimedium, polygala, and tuber curcumae increases synaptophysin expression in APPV717I transgenic mice. Chin Med 2012; 7:13.
31. Rajasekaran A, Periyasamy M. Hepatoprotective effect of ethanolic extract of Trichosanthes lobata on paracetamol-induced liver toxicity in rats. Chin Med 2012; 7:12.
32. Cheung F, Feng Y, Wang N, Yuen M F, Tong Y, Wong VT. Effectiveness of Chinese herbal medicine in treating liver fibrosis: a systematic review and meta-analysis of randomized controlled trials. Chin Med 2012; 7:5.
33. Su SY, Hsieh CL. Anti-inflammatory effects of Chinese medicinal herbs on cerebral ischemia. Chin Med 2011; 6:26.Endurance exercise running and tissues ABCG5 gene expression Ghanbari-Niaki et al
34. Yeo J, Kang YM, Cho SI, Jung MH. Effects of a multi-herbal extract on type 2 diabetes. Chin Med 2011; 6:10.
35. Liao JF, Chiou WF, Shen YC, Wang GJ, Chen CF. Anti-inflammatory and antiinfectious effects of Evodia rutaecarpa (Wuzhuyu) and its major bioactive components. Chin Med 2011; 6:6.
36. Chacko SM, Thambi PT, Kuttan R, Nishigaki I. Beneficial effects of green tea: a literature review. Chin Med 2010; 5:13.
37. Kurian GA, Suryanarayanan S, Raman A, Padikkala J. Antioxidant effects of ethyl acetate extract of Desmodium gangeticum root on myocardial ischemia reperfusion injury in rat hearts. Chin Med 2010; 5:3.
38. Liu J, Xing J, Fei Y. Green tea (Camellia sinensis) and cancer prevention: a systematic review of randomized trials and epidemiological studies. Chin Med 2008; 3:12.
39. Sabate J, Fraser GE, Burke K, Knutsen SF, Bennett H, Lindsted KD. Effects of walnuts on serum lipid levels and blood pressure in normal men. N Engl J Med 1993; 328:603-607.
40. Vecera R, Zacharova A, Orolin J, Skottova N, Anzenbacher P. The effect of silymarin on expression of selected ABC transporters in the rat. Vet Med 2011; 56:59–62.
41. Sobolova L, Skottova N, Vecera R, Urbanek K. Effect of silymarin and its polyphenolic fraction on cholesterol absorption in rats. Pharmacol Res 2006; 53:104-112.
42. Ghanbari-Niaki A, Khabazian BM, Hossaini-Kakhak SA, Rahbarizadeh F, Hedayati M. Treadmill exercise enhances ABCA1 expression in rat liver. Biochem Biophys Res Commun 2007; 361:841-846.
43. Khabazian BM, Ghanbari-Niaki A, Safarzadeh-Golpordesari AR, Ebrahimi M, Rahbarizadeh F, Abednazari H. Endurance training enhances ABCA1 expression in rat small intestine. Eur J Appl Physiol 2009; 107:351-358.
44. Delazar A, Reid RG, Sarker SD. GC-MS Analysis of the Essential Oil from the oleoresin of Pistacia atlantica var. mutica. Chemistry Natural Compounds 2004; 40:24-27.
45. Hamdan II, Afifi FU. Studies on the in vitro and in vivo hypoglycemic activities of some medicinal plants used in treatment of diabetes in Jordanian traditional medicine. J Ethnopharmacol 2004; 93:117-121.
46. Li Z, Duckles SP. Influence of gender on vascular reactivity in the rat. J Pharmacol Exp Ther 1994; 268:1426–1431.
47. Doolen S, Krause DN, Duckles SP. Estradiol modulates vascular response to melatonin in rat caudal artery. Am J Physiol 1999; 276:H1281–H1288.
48. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001; 4:402-408.
49. Baldan A, Tarr P, Lee R, Edwards PA. ATP-binding cassette transporter G1 and lipid homeostasis. Curr Opin Lipidol 2006; 17:227-232.
50. Out R, Hoekstra M, Hildebrand RB, Kruit JK, Meurs I, Li Z,et al. Macrophage ABCG1 deletion disrupts lipid homeostasis in alveolar macrophages and moderately influences atherosclerotic lesion development in LDL receptor-deficient mice. Arterioscler Thromb Vasc Biol 2006; 26:2295-2300.
51. Ranalletta M, Wang N, Han S, Yvan-Charvet L, Welch C, Tall AR. Decreased atherosclerosis in low-density lipoprotein receptor knockout mice transplanted with Abcg1-/- bone marrow. Arterioscler Thromb Vasc Biol 2006; 26:2308-315.
52. Cote I, Ngo Sock ET, Levy E, Lavoie JM. An atherogenic diet decreases liver FXR gene expression and causes severe hepatic steatosis and hepatic cholesterol accumulation: effect of endurance training. Eur J Nutr. 2013 Aug;52(5):1523-32
53. de Vogel-van den Bosch HM, de Wit NJ, Hooiveld GJ, Vermeulen H, Van der Veen, JN,et al. A cholesterol-free, high-fat diet suppresses gene expression of cholesteroltransporters in murine small intestine. Am J Physiol Gastrointest Liver Physiol 2008; 294:1171-1180.
54. Ghanbari-Niaki A, Rahmati- Ahmadabad S, Zare- Kookandeh N. ABCG8 gene responses to 8 weeks treadmill running with or without Pistachia atlantica (Baneh) extraction in female rats. Int J Endocrinol Metab 2012; 10:604-610.
55. Ghanbari-Niaki A, Saghebjoo M, Hedayati M. A single session of circuit-resistance exercise effects on human peripheral blood lymphocyte ABCA1 expression and plasma HDL-C level. Regul Pept 2011; 166:42-47.
56. Butcher LR,Thomas A, Backx K, Roberts A, Webb R, Morris K. Low-intensity exercise exerts beneficial effects on plasma lipids via PPARgamma. Med Sci Sports Exerc 2008; 40:1263-1270.
57. Hoang A, Tefft C, Duffy SJ, Formosa M, Henstridge DC, Kingwell BA,et al . ABCA1 expression in humans is associated with physical activity and alcohol consumption. Atherosclerosis 2008;197:203.
58. Abbey M, Nestel PJ. Plasma cholesteryl ester transfer protein activity is increased when trans-elaidic acid is substituted for cis-oleic acid in the diet. Atherosclerosis 1994; 106:99-107.
59. Lehrke M, Lebherz C, Millington SC, Guan HP, Millar J, Rader DJ,et al. Diet-dependent cardiovascular lipid metabolism controlled by hepatic LXRalpha. Cell Metab 2005; 1:297-308.
60. Zou Y, Du H, Yin M, Zhang L, Mao L, Xiao N,et al. Effects of high dietary fat and cholesterol on expression of PPAR alpha, LXR alpha, and their responsive genes in the liver of apoE and LDLR double deficient mice. Mol Cell Biochem 2009; 323:195-205.
61. Zhang S, Liu Y, Li Q, Dong X, Hu H, Hu R,et al. Exercise improved rat metabolism by raising PPAR-α. Int J Sports Med 2011; 32:568-573.
62. Horowitz JF, Leone TC, Feng W, Kelly DP, Klein S. Effect of endurance training on lipid metabolism in women: a potential role for PPARalpha in the metabolic response to training. Am J Physiol Endocrinol Metab 2000; 279:E348-355.
63. Wang N, Chen W, Linsel-Nitschke P, Martinez LO, Agerholm-Larsen B, Silver DL,et al. A PEST sequence in ABCA1 regulates degradation by calpain protease and stabilization of ABCA1 by apoA-I. J Clin Invest 2003; 111:99–107.
64. Oku H, Matsuura F, Koseki M, Sandoval JC, Yuasa-Kawase M, Tsubakio-Yamamoto K,et al. Adiponectin deficiency suppresses ABCA1 expression and ApoA-I synthesis in the liver. FEBS Lett 2007; 581:5029–5033.
65. Matsuura F, Oku H, Koseki M, Sandoval JC, Yuasa-Kawase M, Tsubakio-Yamamoto K,et al. Adiponectin accelerates reverse cholesterol transport by increasing Ghanbari-Niaki et al Endurance exercise running and tissues ABCG5 gene expression high density lipoprotein assembly in the liver. Biochem Biophys Res Commun 2007; 358:1091–1095.
66. Zeng Q, Isobe K, Fu L, Ohkoshi N, Ohmori H,Takekoshi K,et al. Effects of exercise on adiponectin and adiponectin receptor levels in rats. Life Sci 2007; 80:454–459.

Files

Share

How to cite

Statistics