Document Type : Original Article
Author
Department of Biology, Payam Noor University, Tehran, Iran
Abstract
BACKGROUND: Liver X receptors (LXR) play an essential role in the regulation of cholesterol metabolism, and their activation increases ABCG5 and ABCG8 gene expression for the improvement of cholesterol excretion from the body during reverse cholesterol transport (RCT). The aim of this study was to investigate the effects of high-intensity interval (HIT) and low-intensity continuous (LIT) trainings on gene expression of these substances after a high-fat diet in Wistar rats.
METHODS: Fifteen male Wistar rats were divided into 3 groups: control group (n = 5), HIT exercise group (n = 5), and LIT exercise group (n = 5). All groups were fed a high-fat diet for 13 weeks, and the HIT and LIT groups performed the specific training program. The expression of LXRβ, ABCG5, and ABCG8 genes was measured after the training period.
RESULTS: Data analysis showed significantly higher levels of LXRβ, ABCG5, and ABCG8 gene expression in the HIT and LIT groups compared to the control group (P ≤ 0.05).
CONCLUSION: HIT and LIT trainings after a high-fat diet have beneficial effects on RCT, preventing heart attacks. Additionally, HIT training may have a greater effect on cholesterol excretion during the reverse cholesterol transport mechanism than LIT.
Keywords
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3. Schaltenberg N, John C, Heine M, Haumann F, Rinninger F, Scheja L, et al. Endothelial Lipase Is Involved in Cold-Induced High-Density Lipoprotein Turnover and Reverse Cholesterol Transport in Mice. Front Cardiovasc Med. 2021 Mar 5;8:628235. https://doi.org/10.3389/fcvm.2021.628235
4. Xie J, Peng L, Wang T, Yang C, Chen N, Feng X, et al. QiShenYiQi pill inhibits atherosclerosis by promoting reverse cholesterol transport PPARγ-LXRα/β-ABCA1 pathway. J Ethnopharmacol. 2023 Oct 28;315:116684. https://doi.org/10.1016/j.jep.2023.116684
5. Xu D, Li Y, Yang F, Sun CR, Pan J, Wang L, et al. Structure and transport mechanism of the human cholesterol transporter ABCG1. Cell Rep. 2022 Jan 25;38(4):110298. https://doi.org/10.1016/j.celrep.2022.110298
6. Kojima N, Tada H, Nomura A, Usui S, Sakata K, Hayashi K, et al. Putative Pathogenic Variants of ABCG5 and ABCG8 of Sitosterolemia in Patients With Hyper-Low-Density Lipoprotein Cholesterolemia. J Lipid Atheroscler. 2024 Jan;13(1):53-60. https://doi.org/10.12997/jla.2024.13.1.53
7. Halmos B, La Rose AM, Groenen AG, Nakladal D, Bazioti V, Koster MH, Kloosterhuis NJ, et al. Deficiency of Abca1 and Abcg1 mediated cholesterol efflux pathways in smooth muscle cells enhances vasoconstriction but does not affect atherosclerosis. Cardiovasc Res. 2024; 120(Supplement_1):cvae088-152. https://doi.org/10.1093/cvr/cvae088.152
8. Yang TM, Miao M, Yu WQ, Wang X, Xia FJ, Li YJ, et al. Targeting macrophages in atherosclerosis using nanocarriers loaded with liver X receptor agonists: A narrow review. Front Mol Biosci. 2023 Mar 2;10:1147699. https://doi.org/10.3389/fmolb.2023.1147699
9. Russo-Savage L, Schulman IG. Liver X receptors and liver physiology. Biochim Biophys Acta Mol Basis Dis. 2021 Jun 1;1867(6):166121. https://doi.org/10.1016/j.bbadis.2021.166121
10. Bilotta MT, Petillo S, Santoni A, Cippitelli M. Liver X Receptors: Regulators of Cholesterol Metabolism, Inflammation, Autoimmunity, and Cancer. Front Immunol. 2020 Nov 3;11:584303. https://doi.org/10.3389/fimmu.2020.584303
11. Domínguez-Avila JA. Dietary Phenolic Compounds Exert Some of Their Health-Promoting Bioactivities by Targeting Liver X Receptor (LXR) and Retinoid X Receptor (RXR). Foods. 2023 Nov 22;12(23):4205. https://doi.org/10.3390/foods12234205
12. Na Y, Ke L, Jie Z, Jinping W, Tao M, Jie Z, et al. Amelioration of Cholesterol Rich diet-induced Impaired Cognition in AD Transgenic Mice by an LXR Agonist TO901317 Is Associated with the Activation of the LXR-β-RXR-α-ABCA1 Transmembrane Transport System and Improving the Composition of Lipid Raft. Exp Aging Res. 2023 May-Jun;49(3):214-25. https://doi.org/10.1080/0361073x.2022.2095605
13. Srivastava RAK, Cefalu AB, Srivastava NS, Averna M. NPC1L1 and ABCG5/8 induction explain synergistic fecal cholesterol excretion in ob/ob mice co-treated with PPAR-α and LXR agonists. Mol Cell Biochem. 2020 Oct;473(1-2):247-62. https://doi.org/10.1007/s11010-020-03826-3
14. Ramalingam PS, Elangovan S, Mekala JR, Arumugam S. Liver X Receptors (LXRs) in cancer-an Eagle’s view on molecular insights and therapeutic opportunities. Front Cell Dev Biol. 2024 Mar 14;12:1386102. https://doi.org/10.3389/fcell.2024.1386102
15. Mirghani SJ, Peeri M, Yaghoobpour Yekani O, Zamani M, Feizolahi F, Nikbin S, et al. Role or Synergistic Interaction of Adenosine and Vitamin D3 Alongside High-Intensity Interval Training and Isocaloric Moderate Intensity Training on Metabolic Parameters: Protocol for an Experimental Study. JMIR Res Protoc. 2019 Jan 30;8(1):e10753. https://doi.org/10.2196/10753
16. Baranowski M, Zabielski P, Błachnio-Zabielska AU, Harasiuk D, Górski J. LXR activation prevents exhaustive exercise-induced hypoglycaemia and spares muscle glycogen but does not enhance running endurance in untrained rats. Acta Physiol (Oxf). 2011 Mar;201(3):373-9. https://doi.org/10.1111/j.1748-1716.2010.02199.x
17. Hajighasem A, Farzanegi P, Mazaheri Z, Naghizadeh M, Salehi G. Effects of resveratrol, exercises and their combination on Farnesoid X receptor, Liver X receptor and Sirtuin 1 gene expression and apoptosis in the liver of elderly rats with nonalcoholic fatty liver. PeerJ. 2018 Sep 10;6:e5522. https://doi.org/10.7717/peerj.5522
18. Parsa H, Hasanvand BA, Mehrialvar Y, Zirrahiyan F. Evaluation of Changes in Liver X Receptor Gene Expression Following Exercise and Myocardial Ischemia: A Shourt Report. J Rafsanjan Univ Med Sci. 2021; 20(2):243-50. http://dx.doi.org/10.52547/jrums.20.2.243
19. Côté I, Ngo Sock ET, Lévy É, 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. https://doi.org/10.1007/s00394-012-0459-5
20. Ghanbari-Niaki A, Abarghooi SG, Gholizadeh M. Heart ATP-Binding Cassette Protein A1 and G1, Peroxisome Proliferator Activated Receptor-α and Liver X Receptors Genes Expression in Response to Intensive Treadmill Running and Red Crataegus pentaegyna (Sorkh valik) in Male Rats. Zahedan J Res Med Sci. 2015;17(5):964. http://dx.doi.org/10.5812/zjrms.17(5)2015.964
21. Sahin K, Orhan C, Tuzcu M, Sahin N, Erten F, Juturu V. Capsaicinoids improve consequences of physical activity. Toxicol Rep. 2018 May 15;5:598-607. https://doi.org/10.1016/j.toxrep.2018.05.001
22. Desvergne B, Michalik L, Wahli W. Transcriptional regulation of metabolism. Physiol Rev. 2006 Apr;86(2):465-514. https://doi.org/10.1152/physrev.00025.2005
23. Chen G, Liang G, Ou J, Goldstein JL, Brown MS. Central role for liver X receptor in insulin-mediated activation of Srebp-1c transcription and stimulation of fatty acid synthesis in liver. Proc Natl Acad Sci U S A. 2004 Aug 3;101(31):11245-50. https://doi.org/10.1073/pnas.0404297101
24. N Nagy L, Szanto A, Szatmari I, Széles L. Nuclear hormone receptors enable macrophages and dendritic cells to sense their lipid environment and shape their immune response. Physiol Rev. 2012 Apr;92(2):739-89. https://doi.org/10.1152/physrev.00004.2011
25. Lin G, Bornfeldt KE. Cyclic AMP-specific phosphodiesterase 4 inhibitors promote ABCA1 expression and cholesterol efflux. Biochem Biophys Res Commun. 2002 Jan 18;290(2):663-9. https://doi.org/10.1006/bbrc.2001.6259
26. Khovidhunkit W, Moser AH, Shigenaga JK, Grunfeld C, Feingold KR. Endotoxin down-regulates ABCG5 and ABCG8 in mouse liver and ABCA1 and ABCG1 in J774 murine macrophages: differential role of LXR. J Lipid Res. 2003 Sep;44(9):1728-36. https://doi.org/10.1194/jlr.m300100-jlr200
27. DiBlasio-Smith EA, Arai M, Quinet EM, Evans MJ, Kornaga T, Basso MD, et al. Discovery and implementation of transcriptional biomarkers of synthetic LXR agonists in peripheral blood cells. J Transl Med. 2008 Oct 16;6:59. https://doi.org/10.1186/1479-5876-6-59
28. Khovidhunkit W, Kim MS, Memon RA, Shigenaga JK, Moser AH, Feingold KR, et al. Effects of infection and inflammation on lipid and lipoprotein metabolism: mechanisms and consequences to the host. J Lipid Res. 2004 Jul;45(7):1169-96. https://doi.org/10.1194/jlr.r300019-jlr200
29. 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 Jul;40(7):1263-70. https://doi.org/10.1249/mss.0b013e31816c091d
30. Sadeghi Fazel F, Rashid Lamir A, Khajeie R, Safipour Afshar A. The Effect of Combined Training on ABCG5 and ABCG8 in Coronary Artery Bypass Graft Patients. Intern Med Today. 2022; 28(3):398-411. http://dx.doi.org/10.32598/hms.28.3.3775.1
31. Bagheri R, Darroudi S, Hosseini SM, Nikkar H, Khodadadi F, Kasraee S, et al. Effects of High-Intensity Resistance Training and Aerobic Exercise on Expression of ABCG4, ABCG5 and ABCG8 Genes in Female Athletes. Med Lab J. 2020; 14(3):40-5. http://dx.doi.org/10.29252/mlj.14.3.40
32. Ghanbari-Niaki A, Zare-Kookandeh N, Deldar H, Zare-Kookandeh A, Baghaei-Tehrani R. Visceral fat ABCG1, ABCG5 and visfatin gene expression in response to a treadmill running program with or without a liquid Pistachio-atlantica (Bene) extraction in female rats. Iran J Card Surg. 2013;5(2&3):10-6.
33. Ghanbari-Niaki A, Zare-Kookandeh N, Zare-Kookandeh A. ABCG5 gene responses to treadmill running with or without administration of Pistachio atlantica in female rats. Iran J Basic Med Sci. 2014 Mar;17(3):162-71.
34. 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 Fall;10(4):604-10. https://doi.org/10.5812/ijem.5305
35. Meissner M, Nijstad N, Kuipers F, Tietge UJ. Voluntary exercise increases cholesterol efflux but not macrophage reverse cholesterol transport in vivo in mice. Nutr Metab (Lond). 2010 Jul 1;7:54-59. https://doi.org/10.1186/1743-7075-7-54
36. Ngo Sock ET, Farahnak Z, Lavoie JM. Exercise training decreases gene expression of endo- and xeno-sensors in rat small intestine. Appl Physiol Nutr Metab. 2014 Oct;39(10):1098-103. https://doi.org/10.1139/apnm-2013-0573
37. Mohammadi A, Mirzaei F, Moradi MN, Jamshidi M, Ghiasvand T, Yari R, et al. Effect of flaxseed on Serum Lipid Profile and expression of NPC1L1, ABCG5 and ABCG8 genes in the intestine of diabetic rat. Avicenna J Med Biochem. 2013;1(1):1-6.
38. Back SS, Kim J, Choi D, Lee ES, Choi SY, Han K. Cooperative transcriptional activation of ATP-binding cassette sterol transporters ABCG5 and ABCG8 genes by nuclear receptors including Liver-X-Receptor. BMB Rep. 2013 Jun;46(6):322-7. https://doi.org/10.5483/bmbrep.2013.46.6.246
39. Malik P, Berisha SZ, Santore J, Agatisa-Boyle C, Brubaker G, Smith JD. Zymosan-mediated inflammation impairs in vivo reverse cholesterol transport. J Lipid Res. 2011 May;52(5):951-7. https://doi.org/10.1194/jlr.M011122
40. Freeman LA, Kennedy A, Wu J, Bark S, Remaley AT, Santamarina-Fojo S, et al. The orphan nuclear receptor LRH-1 activates the ABCG5/ABCG8 intergenic promoter. J Lipid Res. 2004 Jul;45(7):1197-206. https://doi.org/10.1194/jlr.c400002-jlr200
41. Fitzgerald ML, Mujawar Z, Tamehiro N. ABC transporters, atherosclerosis and inflammation. Atherosclerosis. 2010 Aug;211(2):361-70. https://doi.org/10.1016/j.atherosclerosis.2010.01.011
42. Panousis CG, Zuckerman SH. Interferon-gamma induces downregulation of Tangier disease gene (ATP-binding-cassette transporter 1) in macrophage-derived foam cells. Arterioscler Thromb Vasc Biol. 2000 Jun;20(6):1565-71. https://doi.org/10.1161/01.atv.20.6.1565
2. Kumarapperuma H, Chia ZJ, Malapitan SM, Wight TN, Little PJ, Kamato D. Response to retention hypothesis as a source of targets for arterial wall-directed therapies to prevent atherosclerosis: A critical review. Atherosclerosis. 2024 Oct;397:118552. https://doi.org/10.1016/j.atherosclerosis.2024.118552
3. Schaltenberg N, John C, Heine M, Haumann F, Rinninger F, Scheja L, et al. Endothelial Lipase Is Involved in Cold-Induced High-Density Lipoprotein Turnover and Reverse Cholesterol Transport in Mice. Front Cardiovasc Med. 2021 Mar 5;8:628235. https://doi.org/10.3389/fcvm.2021.628235
4. Xie J, Peng L, Wang T, Yang C, Chen N, Feng X, et al. QiShenYiQi pill inhibits atherosclerosis by promoting reverse cholesterol transport PPARγ-LXRα/β-ABCA1 pathway. J Ethnopharmacol. 2023 Oct 28;315:116684. https://doi.org/10.1016/j.jep.2023.116684
5. Xu D, Li Y, Yang F, Sun CR, Pan J, Wang L, et al. Structure and transport mechanism of the human cholesterol transporter ABCG1. Cell Rep. 2022 Jan 25;38(4):110298. https://doi.org/10.1016/j.celrep.2022.110298
6. Kojima N, Tada H, Nomura A, Usui S, Sakata K, Hayashi K, et al. Putative Pathogenic Variants of ABCG5 and ABCG8 of Sitosterolemia in Patients With Hyper-Low-Density Lipoprotein Cholesterolemia. J Lipid Atheroscler. 2024 Jan;13(1):53-60. https://doi.org/10.12997/jla.2024.13.1.53
7. Halmos B, La Rose AM, Groenen AG, Nakladal D, Bazioti V, Koster MH, Kloosterhuis NJ, et al. Deficiency of Abca1 and Abcg1 mediated cholesterol efflux pathways in smooth muscle cells enhances vasoconstriction but does not affect atherosclerosis. Cardiovasc Res. 2024; 120(Supplement_1):cvae088-152. https://doi.org/10.1093/cvr/cvae088.152
8. Yang TM, Miao M, Yu WQ, Wang X, Xia FJ, Li YJ, et al. Targeting macrophages in atherosclerosis using nanocarriers loaded with liver X receptor agonists: A narrow review. Front Mol Biosci. 2023 Mar 2;10:1147699. https://doi.org/10.3389/fmolb.2023.1147699
9. Russo-Savage L, Schulman IG. Liver X receptors and liver physiology. Biochim Biophys Acta Mol Basis Dis. 2021 Jun 1;1867(6):166121. https://doi.org/10.1016/j.bbadis.2021.166121
10. Bilotta MT, Petillo S, Santoni A, Cippitelli M. Liver X Receptors: Regulators of Cholesterol Metabolism, Inflammation, Autoimmunity, and Cancer. Front Immunol. 2020 Nov 3;11:584303. https://doi.org/10.3389/fimmu.2020.584303
11. Domínguez-Avila JA. Dietary Phenolic Compounds Exert Some of Their Health-Promoting Bioactivities by Targeting Liver X Receptor (LXR) and Retinoid X Receptor (RXR). Foods. 2023 Nov 22;12(23):4205. https://doi.org/10.3390/foods12234205
12. Na Y, Ke L, Jie Z, Jinping W, Tao M, Jie Z, et al. Amelioration of Cholesterol Rich diet-induced Impaired Cognition in AD Transgenic Mice by an LXR Agonist TO901317 Is Associated with the Activation of the LXR-β-RXR-α-ABCA1 Transmembrane Transport System and Improving the Composition of Lipid Raft. Exp Aging Res. 2023 May-Jun;49(3):214-25. https://doi.org/10.1080/0361073x.2022.2095605
13. Srivastava RAK, Cefalu AB, Srivastava NS, Averna M. NPC1L1 and ABCG5/8 induction explain synergistic fecal cholesterol excretion in ob/ob mice co-treated with PPAR-α and LXR agonists. Mol Cell Biochem. 2020 Oct;473(1-2):247-62. https://doi.org/10.1007/s11010-020-03826-3
14. Ramalingam PS, Elangovan S, Mekala JR, Arumugam S. Liver X Receptors (LXRs) in cancer-an Eagle’s view on molecular insights and therapeutic opportunities. Front Cell Dev Biol. 2024 Mar 14;12:1386102. https://doi.org/10.3389/fcell.2024.1386102
15. Mirghani SJ, Peeri M, Yaghoobpour Yekani O, Zamani M, Feizolahi F, Nikbin S, et al. Role or Synergistic Interaction of Adenosine and Vitamin D3 Alongside High-Intensity Interval Training and Isocaloric Moderate Intensity Training on Metabolic Parameters: Protocol for an Experimental Study. JMIR Res Protoc. 2019 Jan 30;8(1):e10753. https://doi.org/10.2196/10753
16. Baranowski M, Zabielski P, Błachnio-Zabielska AU, Harasiuk D, Górski J. LXR activation prevents exhaustive exercise-induced hypoglycaemia and spares muscle glycogen but does not enhance running endurance in untrained rats. Acta Physiol (Oxf). 2011 Mar;201(3):373-9. https://doi.org/10.1111/j.1748-1716.2010.02199.x
17. Hajighasem A, Farzanegi P, Mazaheri Z, Naghizadeh M, Salehi G. Effects of resveratrol, exercises and their combination on Farnesoid X receptor, Liver X receptor and Sirtuin 1 gene expression and apoptosis in the liver of elderly rats with nonalcoholic fatty liver. PeerJ. 2018 Sep 10;6:e5522. https://doi.org/10.7717/peerj.5522
18. Parsa H, Hasanvand BA, Mehrialvar Y, Zirrahiyan F. Evaluation of Changes in Liver X Receptor Gene Expression Following Exercise and Myocardial Ischemia: A Shourt Report. J Rafsanjan Univ Med Sci. 2021; 20(2):243-50. http://dx.doi.org/10.52547/jrums.20.2.243
19. Côté I, Ngo Sock ET, Lévy É, 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. https://doi.org/10.1007/s00394-012-0459-5
20. Ghanbari-Niaki A, Abarghooi SG, Gholizadeh M. Heart ATP-Binding Cassette Protein A1 and G1, Peroxisome Proliferator Activated Receptor-α and Liver X Receptors Genes Expression in Response to Intensive Treadmill Running and Red Crataegus pentaegyna (Sorkh valik) in Male Rats. Zahedan J Res Med Sci. 2015;17(5):964. http://dx.doi.org/10.5812/zjrms.17(5)2015.964
21. Sahin K, Orhan C, Tuzcu M, Sahin N, Erten F, Juturu V. Capsaicinoids improve consequences of physical activity. Toxicol Rep. 2018 May 15;5:598-607. https://doi.org/10.1016/j.toxrep.2018.05.001
22. Desvergne B, Michalik L, Wahli W. Transcriptional regulation of metabolism. Physiol Rev. 2006 Apr;86(2):465-514. https://doi.org/10.1152/physrev.00025.2005
23. Chen G, Liang G, Ou J, Goldstein JL, Brown MS. Central role for liver X receptor in insulin-mediated activation of Srebp-1c transcription and stimulation of fatty acid synthesis in liver. Proc Natl Acad Sci U S A. 2004 Aug 3;101(31):11245-50. https://doi.org/10.1073/pnas.0404297101
24. N Nagy L, Szanto A, Szatmari I, Széles L. Nuclear hormone receptors enable macrophages and dendritic cells to sense their lipid environment and shape their immune response. Physiol Rev. 2012 Apr;92(2):739-89. https://doi.org/10.1152/physrev.00004.2011
25. Lin G, Bornfeldt KE. Cyclic AMP-specific phosphodiesterase 4 inhibitors promote ABCA1 expression and cholesterol efflux. Biochem Biophys Res Commun. 2002 Jan 18;290(2):663-9. https://doi.org/10.1006/bbrc.2001.6259
26. Khovidhunkit W, Moser AH, Shigenaga JK, Grunfeld C, Feingold KR. Endotoxin down-regulates ABCG5 and ABCG8 in mouse liver and ABCA1 and ABCG1 in J774 murine macrophages: differential role of LXR. J Lipid Res. 2003 Sep;44(9):1728-36. https://doi.org/10.1194/jlr.m300100-jlr200
27. DiBlasio-Smith EA, Arai M, Quinet EM, Evans MJ, Kornaga T, Basso MD, et al. Discovery and implementation of transcriptional biomarkers of synthetic LXR agonists in peripheral blood cells. J Transl Med. 2008 Oct 16;6:59. https://doi.org/10.1186/1479-5876-6-59
28. Khovidhunkit W, Kim MS, Memon RA, Shigenaga JK, Moser AH, Feingold KR, et al. Effects of infection and inflammation on lipid and lipoprotein metabolism: mechanisms and consequences to the host. J Lipid Res. 2004 Jul;45(7):1169-96. https://doi.org/10.1194/jlr.r300019-jlr200
29. 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 Jul;40(7):1263-70. https://doi.org/10.1249/mss.0b013e31816c091d
30. Sadeghi Fazel F, Rashid Lamir A, Khajeie R, Safipour Afshar A. The Effect of Combined Training on ABCG5 and ABCG8 in Coronary Artery Bypass Graft Patients. Intern Med Today. 2022; 28(3):398-411. http://dx.doi.org/10.32598/hms.28.3.3775.1
31. Bagheri R, Darroudi S, Hosseini SM, Nikkar H, Khodadadi F, Kasraee S, et al. Effects of High-Intensity Resistance Training and Aerobic Exercise on Expression of ABCG4, ABCG5 and ABCG8 Genes in Female Athletes. Med Lab J. 2020; 14(3):40-5. http://dx.doi.org/10.29252/mlj.14.3.40
32. Ghanbari-Niaki A, Zare-Kookandeh N, Deldar H, Zare-Kookandeh A, Baghaei-Tehrani R. Visceral fat ABCG1, ABCG5 and visfatin gene expression in response to a treadmill running program with or without a liquid Pistachio-atlantica (Bene) extraction in female rats. Iran J Card Surg. 2013;5(2&3):10-6.
33. Ghanbari-Niaki A, Zare-Kookandeh N, Zare-Kookandeh A. ABCG5 gene responses to treadmill running with or without administration of Pistachio atlantica in female rats. Iran J Basic Med Sci. 2014 Mar;17(3):162-71.
34. 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 Fall;10(4):604-10. https://doi.org/10.5812/ijem.5305
35. Meissner M, Nijstad N, Kuipers F, Tietge UJ. Voluntary exercise increases cholesterol efflux but not macrophage reverse cholesterol transport in vivo in mice. Nutr Metab (Lond). 2010 Jul 1;7:54-59. https://doi.org/10.1186/1743-7075-7-54
36. Ngo Sock ET, Farahnak Z, Lavoie JM. Exercise training decreases gene expression of endo- and xeno-sensors in rat small intestine. Appl Physiol Nutr Metab. 2014 Oct;39(10):1098-103. https://doi.org/10.1139/apnm-2013-0573
37. Mohammadi A, Mirzaei F, Moradi MN, Jamshidi M, Ghiasvand T, Yari R, et al. Effect of flaxseed on Serum Lipid Profile and expression of NPC1L1, ABCG5 and ABCG8 genes in the intestine of diabetic rat. Avicenna J Med Biochem. 2013;1(1):1-6.
38. Back SS, Kim J, Choi D, Lee ES, Choi SY, Han K. Cooperative transcriptional activation of ATP-binding cassette sterol transporters ABCG5 and ABCG8 genes by nuclear receptors including Liver-X-Receptor. BMB Rep. 2013 Jun;46(6):322-7. https://doi.org/10.5483/bmbrep.2013.46.6.246
39. Malik P, Berisha SZ, Santore J, Agatisa-Boyle C, Brubaker G, Smith JD. Zymosan-mediated inflammation impairs in vivo reverse cholesterol transport. J Lipid Res. 2011 May;52(5):951-7. https://doi.org/10.1194/jlr.M011122
40. Freeman LA, Kennedy A, Wu J, Bark S, Remaley AT, Santamarina-Fojo S, et al. The orphan nuclear receptor LRH-1 activates the ABCG5/ABCG8 intergenic promoter. J Lipid Res. 2004 Jul;45(7):1197-206. https://doi.org/10.1194/jlr.c400002-jlr200
41. Fitzgerald ML, Mujawar Z, Tamehiro N. ABC transporters, atherosclerosis and inflammation. Atherosclerosis. 2010 Aug;211(2):361-70. https://doi.org/10.1016/j.atherosclerosis.2010.01.011
42. Panousis CG, Zuckerman SH. Interferon-gamma induces downregulation of Tangier disease gene (ATP-binding-cassette transporter 1) in macrophage-derived foam cells. Arterioscler Thromb Vasc Biol. 2000 Jun;20(6):1565-71. https://doi.org/10.1161/01.atv.20.6.1565
)