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Modulation of lipid homeostasis in response to continuous or intermittent high-fat diet in pigs

Published online by Cambridge University Press:  04 February 2015

E. Puccinelli ,
P. G. Gervasi ,
M. G. Trivella ,
A. Vornoli ,
F. Viglione ,
G. Pelosi ,
O. Parodi ,
T. Sampietro  and
M. Puntoni
E. Puccinelli
Affiliation:
CNR Institute of Clinical Physiology, Via Moruzzi 1, 56100 Pisa, Italy
P. G. Gervasi
Affiliation:
CNR Institute of Clinical Physiology, Via Moruzzi 1, 56100 Pisa, Italy
M. G. Trivella
Affiliation:
CNR Institute of Clinical Physiology, Via Moruzzi 1, 56100 Pisa, Italy
A. Vornoli
Affiliation:
CNR Institute of Clinical Physiology, Via Moruzzi 1, 56100 Pisa, Italy
F. Viglione
Affiliation:
CNR Institute of Clinical Physiology, Via Moruzzi 1, 56100 Pisa, Italy
G. Pelosi
Affiliation:
CNR Institute of Clinical Physiology, Via Moruzzi 1, 56100 Pisa, Italy
O. Parodi
Affiliation:
CNR Institute of Clinical Physiology, Via Moruzzi 1, 56100 Pisa, Italy
T. Sampietro
Affiliation:
Fondazione Gabriele Monasterio CNR-Regione Toscana, Via Moruzzi 1, 56100 Pisa, Italy
M. Puntoni*
Affiliation:
CNR Institute of Clinical Physiology, Via Moruzzi 1, 56100 Pisa, Italy
*
†E-mail: mpuntoni@ifc.cnr.it
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Abstract

A high-fat diet is known to induce atherosclerosis in animal models. Dietary factors and timing of atherogenic food delivery may affect plasma lipoprotein content composition and its potential atherogenic effect. Increasingly often, humans spend periods/days eating in a completely unregulated way, ingesting excessive amounts of food rich in oils and fats, alternating with periods/days when food intake is more or less correct. We investigate the effect on lipid homeostasis of a high-fat diet administered either continuously or intermittently. We investigated control pigs receiving standard diet (C, n=7), pigs receiving a high-fat diet every day for 10 weeks (CHF, n=5), and pigs receiving a high-fat diet every other week for 10 weeks (IHF, n=7). IHF animals were shown to have a different lipid profile compared with CHF animals, with a significant increase in high-density lipoproteins (HDL) levels with respect to C and CHF groups. CHF also showed significantly higher values of TC/HDL cholesterol compared with C and IHF. Hepatic expression analysis of genes involved in lipid homeostasis showed an increasing trend of nuclear receptor LXRα along with its target genes in the CHF group and in the IHF group, whereas SREBP2 and LDLr were significantly inhibited. A significant correlation was found between ABCA1 expression and circulating levels of HDL-C. Periodic withdrawals of a high-fat atherogenic diet compared with a regular administration results in a different adaptive response of lipoprotein metabolism, which leads to a significantly higher plasma level of HDL-C and lower TC/HDL-C.

Keywords

high-fat dietpiglipoproteinsatherosclerosis
Type
Research Article
Information
animal , Volume 9 , Supplement 6 , June 2015 , pp. 1000 - 1007
Copyright
© The Animal Consortium 2015 

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References

Abourbih, S, Filion, KB, Joseph, L, Schiffrin, EL, Rinfret, S, Poirier, P, Pilote, L, Genest, J and Eisenberg, MJ 2009. Effect of fibrates on lipid profiles and cardiovascular outcomes: a systematic review. American Journal of Medicine 122, 962.e1–962.e8.CrossRefGoogle ScholarPubMed
Baranowski, M 2008. Biological role of liver X receptor. Journal of Physiology and Pharmacology 59, 31–55.Google Scholar
Cabrero, A, Jové, M, Planavila, A, Merlos, M, Laguna, JC and Vazquez-Carrera, M 2003. Down-regulation of acyl-coa oxidase gene expression in heart of troglitazone-treated mice through a mechanism involving chicken ovalbumin upstream promoter transcription factor II. Molecular Pharmacology 64, 764–772.CrossRefGoogle ScholarPubMed
Casani, L, Sanchez-Gomez, S, Vilahur, G and Badimon, L 2005. Pravastatin reduces thrombogenicity by mechanisms beyond plasma cholesterol lowering. Thrombosis and Haemostasis 94, 1035–1041.CrossRefGoogle ScholarPubMed
Chakravarthy, MV, Lodhi, IJ, Yin, L, Malapaka, RR, Xu, HE, Turk, J and Semenkovich, CF 2009. Identification of a physiologically relevant endogenous ligand for PPAR alpha in liver. Cell 138, 476–488.CrossRefGoogle ScholarPubMed
Chatzizisis, YS, Jonas, M, Coskun, AU, Beigel, R, Stone, BV, Maynard, C, Gerrity, RG, Daley, W, Rogers, C, Edelman, ER, Feldman, CL and Stone, PH 2008. Prediction of the localization of high-risk coronary atherosclerotic plaques on the basis of low endothelial shear stress: an intravascular ultrasound and histopathology natural history study. Circulation 117, 993–1002.CrossRefGoogle ScholarPubMed
Cheon, Y, Nara, TY, Band, MR, Beever, JE, Wallig, MA and Nakamura, MT 2005. Induction of overlapping genes by fasting and a peroxisome proliferator in pigs: evidence of functional PPAR alpha in nonproliferating species. American Journal of Physiology – Regulatory Integrative and Comparative Physiology 288, 1525–1535.CrossRefGoogle Scholar
Chiang, JYL 2004. Regulation of bile acid synthesis: pathway, nuclear receptors, and mechanisms. Journal of Hepatology 40, 539–551.CrossRefGoogle ScholarPubMed
Chiang, JYL, Kimmel, R and Stroup, D 2001. Regulation of cholesterol 7α-hydroxylase gene (CYP7A1) transcription by the liver orphan receptor (LXRα). Gene 262, 257–265.CrossRefGoogle ScholarPubMed
Dixon, JL, Stoops, JD, Parker, JL, Laughlin, MH, Weisman, GA and Sturek, M 1999. Dyslipidemia and vascular dysfunction in diabetic pigs fed an atherogenic diet. Arteriosclerosis Thrombosis and Vascular Biology 19, 2981–2992.CrossRefGoogle ScholarPubMed
Duran-Montgé, P, Theil, PK, Lauridsen, C and Esteve-Garcia, E 2009a. Dietary fat source affects metabolism of fatty acids in pigs as evaluated by altered expression of lipogenic genes in liver and adipose tissues. Animal 3, 535–542.CrossRefGoogle ScholarPubMed
Duran-Montgé, P, Theil, PK, Lauridsen, C and Esteve-Garcia, E 2009b. Fat metabolism is regulated by altered gene expression of lipogenic enzymes and regulatory factors in liver and adipose tissue but not in semimembranosus muscle of pigs during the fattening period. Animal 3, 1580–1590.CrossRefGoogle Scholar
Dussault, I, Yoo, HD, Lin, M, Wang, E, Fan, M, Batta, AK, Salen, G, Erickson, SK and Forman, BM 2003. Identification of an endogenous ligand that activates pregnane X receptor-mediated sterol clearance. Proceedings of the National Academy of Science of the USA 100, 833–838.CrossRefGoogle ScholarPubMed
Friedman, SL 2000. Molecular regulation of hepatic fibrosis, an integrated cellular response to tissue injury. Journal of Biological Chemistry 275, 2247–2250.CrossRefGoogle ScholarPubMed
Friedewald, WT, Levy, RI and Fredrickson, DS 1972. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clinical Chemistry 18, 499–502.CrossRefGoogle ScholarPubMed
Geeraert, B, De Keyzer, D, Davey, PC, Crombé, F, Benhabilès, N and Holvoet, P 2007. Oxidized low-density lipoprotein-induced expression of ABCA1 in blood monocytes precedes coronary atherosclerosis and is associated with plaque complexity in hypercholesterolemic pigs. Journal of Thrombosis and Haemostasis 5, 2529–2536.CrossRefGoogle ScholarPubMed
Gordon, T, Castelli, WP, Hjortland, MC, Kannel, WB and Dawber, TR 1977. High density lipoprotein as a protective factor against coronary heart disease. The Framingham Study. American Journal of Medicine 62, 707–714.CrossRefGoogle ScholarPubMed
Hebbachi, AM, Knight, BL, Wiggins, D, Patel, DD and Gibbons, GF 2008. Peroxisome proliferator-activated receptor α deficiency abolishes the response of lipogenic gene expression to re-feeding. Restoration of the normal response by activation of liver X receptor α. Journal of Biological Chemistry 283, 4866–4876.CrossRefGoogle ScholarPubMed
Janowschki, BA, Willy, PJ, Devi, TR, Falck, JR and Mangelsdorf, DJ 1996. An oxysterol signaling pathway mediated by the nuclear receptor LXRa. Nature 283, 728–731.CrossRefGoogle Scholar
Ji, W and Gong, BQ 2008. Hypolipidemic activity and mechanism of purified herbal extract of Salvia miltiorrhiza in hyperlipidemic rats. Journal of Ethnopharmacology 119, 291–298.CrossRefGoogle ScholarPubMed
Kmiec, Z 2001. Cooperation of liver cells in health and disease. Advances in Anatomy Embryology and Cellular Biology 161, 1–151 (review).Google ScholarPubMed
Lefebvre, P, Chinetti, G, Fruchart, J and Staels, B 2006. Sorting out the roles of PPARα in energy metabolism and vascular homeostasis. The Journal of Clinical Investigation 116, 571–580.CrossRefGoogle ScholarPubMed
Lewington, S, Whitlock, G, Clarke, R, Sherliker, F, Emberson, J, Halsey, J, Qizilbash, N, Peto, R and Collins, R 2007. Blood cholesterol and vascular mortality by age, sex, and blood pressure: a meta-analysis of individual data from 61 prospective studies with 55,000 vascular deaths. The Lancet 370, 1829–1839.Google Scholar
Lewis, GF and Rader, DJ 2005. New insights into the regulation of HDL metabolism and reverse cholesterol transport. Circulation Research 96, 1221–1232.CrossRefGoogle ScholarPubMed
Lobstein, T, Rigby, N and Leach, R 2005. EU platform on diet, physical activity and health, International Obesity Taskforce, Brussels. Retrieved March 15, 2005, from http://ec.europa.eu/health/ph_determinants/life_style/nutrition/documents/iotf_en.pdf Google Scholar
Luci, S, Giemsa, B, Kluge, H and Eder, K 2007. Clofibrate causes an upregulation of PPAR-α target genes but does not alter expression of SREBP target genes in liver and adipose tissue of pigs. American Journal of Physiology – Regulatory, Integrative and Comparative Physiology 293, R70–R77.CrossRefGoogle Scholar
Luci, S, König, B, Giemsa, B, Huber, S, Hause, G, Kluge, H, Stangl, GI and Eder, K 2007. Feeding of a deep-fried fat causes PPARα activation in the liver of pigs as a non-proliferating species. British Journal of Nutrition 97, 872–882.CrossRefGoogle ScholarPubMed
Millatt, LJ, Bocher, V, Fruchart, J and Staels, B 2003. Liver X receptors and the control of cholesterol homeostasis: potential therapeutic targets for the treatment of atherosclerosis. Biochimica et Biophysica Acta 1631, 107–118.CrossRefGoogle ScholarPubMed
Puccinelli, E, Gervasi, PG, Pelosi, G, Puntoni, M and Longo, V 2012. Modulation of cytochrome P450 enzymes in response to continuous or intermittent high-fat diet in pigs. Xenobiotica 48, 1–13.Google Scholar
Schaefer, EJ, Levy, RI, Ernst, ND, Van Sant, FD and Brewer, HB Jr. 1981. The effects of low cholesterol, high polyunsaturated fat, and low fat diets on plasma lipid and lipoprotein cholesterol levels in normal and hypercholesterolemic subjects. American Journal of Clinical Nutrition 34, 1758–1763.CrossRefGoogle ScholarPubMed
Stary, HC, Blankenhorn, DH, Chandler, AB, Glagov, S, Insull, W Jr, Richardson, M, Rosenfeld, ME, Schaffer, SA, Schwartz, CJ and Wagner, WD 1992. A definition of the intima of human arteries and of its atherosclerosis-prone regions. Arteriosclerosis Thrombosis and Vascular Biology 12, 120–134.CrossRefGoogle ScholarPubMed
Stott, WT, Yano, BL, Williams, DM, Barnard, SD, Hannah, MA, Cieszlak, FS and Herman, JR 1995. Species-dependent induction of peroxisome proliferation by haloxyfop, an aryloxyphenoxy herbicide. Fundamental and Applied Toxicology 28, 71–79.CrossRefGoogle ScholarPubMed
Tobin, KAR, Steineger, HH, Alberti, S, Spydevold, O, Auwerx, J, Gustafsson, JA and Nebb, HI 2000. Cross-talk between fatty acid and cholesterol metabolism mediated by liver X receptor-alpha. Molecular Endocrinology 14, 741–752.Google ScholarPubMed
Virmani, R, Kolodgie, FD, Burke, PA, Farb, A and Schwartz, SM 2000. Lessons from sudden coronary death: a comprehensive morphological classification scheme for atherosclerotic lesions. Arteriosclerosis Thrombosis and Vascular Biology 20, 1262–1275.CrossRefGoogle Scholar
Zhou, J, Zhai, Y, Mu, Y, Gong, H, Uppal, H, Toma, D, Ren, S, Evans, RM and Xie, W 2006. A novel pregnane X receptor-mediated and sterol regulatory element-binding protein-independent lipogenic pathway. Journal of Biological Chemistry 281, 15013–15020.CrossRefGoogle ScholarPubMed
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