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Obesity induced during sexual maturation is linked to LDL-triacylglycerols in Yucatan miniature swine

Published online by Cambridge University Press:  08 March 2007

Sylvain P. Sébert ,
Gérard Lecannu ,
Sandrine Sené ,
Séverine Hucteau ,
Maud Chetiveaux ,
Khadija Ouguerram  and
Martine M.-J. Champ
Sylvain P. Sébert
Affiliation:
Human Nutrition and Gut Functions Unit, National Institute of Agronomic Research Rue de la Géraudière, BP 71627, 44316, Nantes, Cedex 3, France
Gérard Lecannu
Affiliation:
Human Nutrition and Gut Functions Unit, National Institute of Agronomic Research Rue de la Géraudière, BP 71627, 44316, Nantes, Cedex 3, France
Sandrine Sené
Affiliation:
Human Nutrition and Gut Functions Unit, National Institute of Agronomic Research Rue de la Géraudière, BP 71627, 44316, Nantes, Cedex 3, France
Séverine Hucteau
Affiliation:
Human Nutrition and Gut Functions Unit, National Institute of Agronomic Research Rue de la Géraudière, BP 71627, 44316, Nantes, Cedex 3, France
Maud Chetiveaux
Affiliation:
Human Nutrition Research Centre, CHU Hôtel Dieu Nantes, 1 place Alexis Ricordeau, 44093, Nantes, Cedex 1, France
Khadija Ouguerram
Affiliation:
Human Nutrition Research Centre, CHU Hôtel Dieu Nantes, 1 place Alexis Ricordeau, 44093, Nantes, Cedex 1, France
Martine M.-J. Champ*
Affiliation:
Human Nutrition and Gut Functions Unit, National Institute of Agronomic Research Rue de la Géraudière, BP 71627, 44316, Nantes, Cedex 3, France Human Nutrition Research Centre, CHU Hôtel Dieu Nantes, 1 place Alexis Ricordeau, 44093, Nantes, Cedex 1, France
*
*Corresponding author: Dr Martine Champ, fax +33 (0)2 40 67 51 12, email [email protected]
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Abstract

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The incidence of childhood obesity is rising dramatically throughout industrialised countries. To evaluate and study the impact of childhood obesity on lipoprotein metabolism, we developed a new animal model of premature obesity. Yucatan mini-pigs aged 4 months were studied over a 12-month period from childhood to adulthood. Animals were divided into two groups: the first group were overfed a Western misbalanced diet; the second group were normally fed a recommended human-type diet. Cholesterol and triacylglycerol concentrations in VLDL-, LDL- and HDL-lipoproteins were followed from baseline to adulthood by fast protein liquid chromatography. At 10 (the end of sexual maturation) and 16 months old (adulthood), liver, visceral and subcutaneous adipose tissues were sampled. Real-time RT-PCR was performed in order to compare apo AI, apo B, apo C-III, PPAR-α, insulin receptor and lipoprotein lipase gene expression between groups and ages. Differences between groups were observed only after sexual maturity. Adult overfed mini-pigs had a higher LDL-cholesterol:HDL-cholesterol ratio (P<0·05; 0·55 (SE 0·06) for overfed v. 0·42 (SE 0·04) for normally fed pigs at the tenth month of the study). In both groups, VLDL-triacylglycerol decreased (P<0·05). VLDL-triacylglycerol evolution in the overfed group was associated with an increase in LDL-triacylglycerol plasma concentrations (P<0·05) after sexual maturation. LDL-triacylglycerol concentration in overfed mini-pigs went from an average of 0·28 mmol/l before sexual maturation to reach an average concentration of 0·56 mmol/l afterwards. This phenomenon has never been observed in similar studies when obesity is induced in adult mini-pigs and may represent a specific hallmark of an obesity induced during sexual maturity.

Keywords

ObesityChildhoodAdulthoodLipoproteinsMini-pigs
Type
Research Article
Information
British Journal of Nutrition , Volume 94 , Issue 2 , August 2005 , pp. 282 - 289
Copyright
Copyright © The Nutrition Society 2005

References

Arai, T, Yamashita, S, Hirano, K, et al. (1994) Increased plasma cholesteryl ester transfer protein in obese subjects. A possible mechanism for the reduction of serum HDL cholesterol levels in obesity. Arterioscler Thromb 14, 1129–1136.CrossRefGoogle ScholarPubMed
Asayama, K, Hayashibe, H, Dobashi, K, Uchida, N, Nakane, T, Kodera, K & Shirahata, A (2002) Increased serum cholesteryl ester transfer protein in obese children. Obes Res 10, 439–446.CrossRefGoogle ScholarPubMed
Bollen, JA, Hansen, AK & Rasmussen, HJ (2000) The laboratory swine. Boca Raton, FL: CRC Press.Google Scholar
Carrilho, AJ, Cunha-Neto, MB, Nunes, VS, Lottenberg, AM, Medina, WL, Nakandakare, ER, Musolino, NR, Bronstein, MD & Quintao, EC (2001) Plasma cholesteryl ester transfer protein and lipoprotein levels during treatment of growth hormone-deficient adult humans. Lipids 36, 549–554.CrossRefGoogle ScholarPubMed
Chomczynski, P & Sacchi, N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162, 156–159.CrossRefGoogle ScholarPubMed
De Benedetti, F, Meazza, C & Martini, A (2002) Role of interleukin-6 in growth failure: an animal model. Horm Res 58 Suppl 1, 24–27.Google ScholarPubMed
Desvergne, B, IJPenberg, A, Devchand, PR & Wahli, W (1998) The peroxisome proliferator-activated receptors at the cross-road of diet and hormonal signalling. J Steroid Biochem Mol Biol 65, 65–74.CrossRefGoogle ScholarPubMed
Dietz, WH (1998) Childhood weight affects adult morbidity and mortality. J Nutr 128, 411S–414S.CrossRefGoogle ScholarPubMed
Dixon, JL, Shen, S, Vuchetich, JP, Wysocka, E, Sun, GY & Sturek, M (2002) Increased atherosclerosis in diabetic dyslipidemic swine: protection by atorvastatin involves decreased VLDL triglycerides but minimal effects on the lipoprotein profile. J Lipid Res 43, 1618–1629.CrossRefGoogle ScholarPubMed
Dixon, JL, Stoops, JD, Parker, JL, Laughlin, MH, Weisman, GA & Sturek, M (1999) Dyslipidemia and vascular dysfunction in diabetic pigs fed an atherogenic diet. Arterioscler Thromb Vasc Biol 19, 2981–2992.Google ScholarPubMed
Franklin, FA Jr, Dashti, N & Franklin, CC (1998) Evaluation and management of dyslipoproteinemia in children. Endocrinol Metab Clin North Am 27, 641–654.CrossRefGoogle ScholarPubMed
Freedman, DS, Dietz, WH, Srinivasan, SR & Berenson, GS (1999) The relation of overweight to cardiovascular risk factors among children and adolescents: the Bogalusa Heart Study. Pediatrics 103, 1175–1182.CrossRefGoogle ScholarPubMed
Freedman, DS, Khan, LK, Serdula, MK, Dietz, WH, Srinivasan, SR & Berenson, GS (2004) Inter-relationships among childhood BMI, childhood height, and adult obesity: the Bogalusa Heart Study. Int J Obes Relat Metab Disord 28, 10–16.CrossRefGoogle ScholarPubMed
Fruchart, JC (2001) Peroxysome proliferator-activated receptor-alpha activation and high-density lipoprotein metabolism. Am J Cardiol 88, 24–29.CrossRefGoogle Scholar
Galeano, NF, Al-Haideri, M, Keyserman, F, Rumsey, SC & Deckelbaum, RJ (1998) Small dense low density lipoprotein has increased affinity for LDL receptor-independent cell surface binding sites: a potential mechanism for increased atherogenicity. J Lipid Res 39, 1263–1273.CrossRefGoogle ScholarPubMed
Gerrity, RG, Natarajan, R, Nadler, JL & Kimsey, T (2001) Diabetes-induced accelerated atherosclerosis in swine. Diabetes 50, 1654–1665.CrossRefGoogle ScholarPubMed
Gill, JM, Brown, JC, Caslake, MJ, Wright, DM, Cooney, J, Bedford, D, Hughes, DA, Stanley, JC & Packard, CJ (2003) Effects of dietary monounsaturated fatty acids on lipoprotein concentrations, compositions, and subfraction distributions and on VLDL apolipoprotein B kinetics: dose-dependent effects on LDL. Am J Clin Nutr 78, 47–56.CrossRefGoogle ScholarPubMed
Ginsberg, HN (2000) Insulin resistance and cardiovascular disease. J Clin Invest 106, 453–458.CrossRefGoogle ScholarPubMed
Guerin, M, Le Goff, W, Lassel, TS, Van Tol, A, Steiner, G & Chapman, MJ (2001) Atherogenic role of elevated CE transfer from HDL to VLDL(1) and dense LDL in type 2 diabetes: impact of the degree of triglyceridemia. Arterioscler Thromb Vasc Biol 21, 282–288.CrossRefGoogle ScholarPubMed
Ha, YC & Barter, PJ (1982) Differences in plasma cholesteryl ester transfer activity in sixteen vertebrate species. Comp Biochem Physiol B 71, 265–269.CrossRefGoogle ScholarPubMed
Han, TS, Richmond, P, Avenell, A & Lean, ME (1997) Waist circumference reduction and cardiovascular benefits during weight loss in women. Int J Obes Relat Metab Disord 21, 127–134.CrossRefGoogle ScholarPubMed
Hayashibe, H, Asayama, K, Nakane, T, Uchida, N, Kawada, Y & Nakazawa, S (1997) Increased plasma cholesteryl ester transfer activity in obese children. Atherosclerosis 129, 53–58.CrossRefGoogle ScholarPubMed
Heude, B, Lafay, L, Borys, JM, Thibult, N, Lommez, A, Romon, M, Ducimetiere, P & Charles, MA (2003) Time trend in height, weight, and obesity prevalence in school children from Northern France. Diabetes Metab 29, 235–240.CrossRefGoogle ScholarPubMed
Johansen, T, Hansen, HS, Richelsen, B & Malmlof, R (2001) The obese Gottingen minipig as a model of the metabolic syndrome: dietary effects on obesity, insulin sensitivity, and growth hormone profile. Comp Med 51, 150–155.Google Scholar
Jolliffe, D (2004) Extent of overweight among US children and adolescents from 1971 to 2000. Int J Obes Relat Metab Disord 28, 4–9.CrossRefGoogle ScholarPubMed
Klesges, RC, Klesges, LM, Haddock, CK & Eck, LH (1992) A longitudinal analysis of the impact of dietary intake and physical activity on weight change in adults. Am J Clin Nutr 55, 818–822.CrossRefGoogle ScholarPubMed
Kouda, K, Nakamura, H, Fan, W & Takeuchi, H (2003) Negative relationships between growth in height and levels of cholesterol in puberty: a 3-year follow-up study. Int J Epidemiol 32, 1105–1110.CrossRefGoogle ScholarPubMed
Lahdenpera, S, Syvanne, M, Kahri, J & Taskinen, MR (1996) Regulation of low-density lipoprotein particle size distribution in NIDDM and coronary disease: importance of serum triglycerides. Diabetologia 39, 453–461.CrossRefGoogle ScholarPubMed
Larsen, MO, Rolin, B, Wilken, M, Carr, RD & Svendsen, O (2002) High-fat high-energy feeding impairs fasting glucose and increases fasting insulin levels in the Gottingen minipig: results from a pilot study. Ann N Y Acad Sci 967, 414–423.CrossRefGoogle ScholarPubMed
Luscombe, ND, Noakes, M & Clifton, PM (1999) Diets high and low in glycemic index versus high monounsaturated fat diets: effects on glucose and lipid metabolism in NIDDM. Eur J Clin Nutr 53, 473–478.CrossRefGoogle ScholarPubMed
Machado, MO, Hirata, RD, Hirata, MH, Hirszel, P, Sellitti, DF & Doi, SQ, (2003) Growth hormone increases low-density lipoprotein receptor and HMG-CoA reductase mRNA expression in mesangial cells. Nephron Exp Nephrol 93, e134–e140.CrossRefGoogle ScholarPubMed
Maffeis, C, Moghetti, P, Grezzani, A, Clementi, M, Gaudino, R & Tato, L (2002) Insulin resistance and the persistence of obesity from childhood into adulthood. J Clin Endocrinol Metab 87, 71–76.CrossRefGoogle ScholarPubMed
Mahley, RW, Weisgraber, KH, Innerarity, T, Brewer, HB Jr & Assmann, G (1975) Swine lipoproteins and atherosclerosis. Changes in the plasma lipoproteins and apoproteins induced by cholesterol feeding. Biochemistry 14, 2817–2823.CrossRefGoogle ScholarPubMed
Moran, A, Jacobs, DR Jr, Steinberger, J, Hong, CP, Prineas, R, Luepker, R & Sinaiko, AR (1999) Insulin resistance during puberty: results from clamp studies in 357 children. Diabetes 48, 2039–2044.CrossRefGoogle ScholarPubMed
Moughan, PJ, Birtles, MJ, Cranwell, PD, Smith, WC & Pedraza, M (1992) The piglet as a model animal for studying aspects of digestion and absorption in milk-fed human infants. World Rev Nutr Diet 67, 40–113.CrossRefGoogle Scholar
Nicklas, BJ, Ferrell, RE, Rogus, EM, Berman, DM, Ryan, AS, Dennis, KE & Goldberg, AP (2000) Lipoprotein lipase gene variation is associated with adipose tissue lipoprotein lipase activity, and lipoprotein lipid and glucose concentrations in overweight postmenopausal women. Hum Genet 106, 420–424.CrossRefGoogle ScholarPubMed
Olsen, AK, Bladbjerg, EM, Marckmann, P, Larsen, LF & Hansen, AK (2002) The Gottingen minipig as a model for postprandial hyperlipidaemia in man: experimental observations. Lab Anim 36, 438–444.CrossRefGoogle Scholar
Phillips, RW, Panepinto, LM, Spangler, R & Westmoreland, N (1982) Yucatan miniature swine as a model for the study of human diabetes mellitus. Diabetes 31, 30–36.CrossRefGoogle Scholar
Plourde, G (2002) Impact of obesity on glucose and lipid profiles in adolescents at different age groups in relation to adulthood. BMC Fam Pract 3, 18.CrossRefGoogle ScholarPubMed
Pussinen, PJ, Olkkonen, VM, Jauhiainen, M & Ehnholm, C (1997) Molecular cloning and functional expression of cDNA encoding the pig plasma phospholipid transfer protein. J Lipid Res 38, 1473–1481.CrossRefGoogle ScholarPubMed
Ren, B, Thelen, A & Jump, DB (1996) Peroxisome proliferator-activated receptor alpha inhibits hepatic S14 gene transcription. Evidence against the peroxisome proliferator-activated receptor alpha as the mediator of polyunsaturated fatty acid regulation of s14 gene transcription. J Biol Chem 271, 17167–17173.CrossRefGoogle ScholarPubMed
Rolland-Cachera, MF, Castetbon, K, Arnault, N, Bellisle, F, Romano, MC, Lehingue, Y, Frelut, ML & Hercberg, S (2002) Body mass index in 7–9-y-old French children: frequency of obesity, overweight and thinness. Int J Obes Relat Metab Disord 26, 1610–1616.CrossRefGoogle ScholarPubMed
Shi, XW, Zhang, YD, Rothschild, MF & Tuggle, CK (2002) Rapid communication: genetic linkage and physical mapping of the porcine cholesteryl ester transfer protein (CETP) gene. J Anim Sci 80, 1390–1391.CrossRefGoogle ScholarPubMed
Takahashi, T, Hirano, T, Okada, K & Adachi, M (2003) Apolipoprotein CIII deficiency prevents the development of hypertriglyceridemia in streptozotocin-induced diabetic mice. Metabolism 52, 1354–1359.CrossRefGoogle ScholarPubMed
Tan, KC, Shiu, SW, Janus, ED & Lam, KS (1997) LDL subfractions in acromegaly: relation to growth hormone and insulin-like growth factor-I. Atherosclerosis 129, 59–65.CrossRefGoogle ScholarPubMed
Vanhala, M, Vanhala, P, Kumpusalo, E, Halonen, P & Takala, J (1998) Relation between obesity from childhood to adulthood and the metabolic syndrome: population based study. BMJ 317, 319.CrossRefGoogle ScholarPubMed
Vernon, RG, Barber, MC & Travers, MT (1999) Present and future studies on lipogenesis in animals and human subjects. Proc Nutr Soc 58, 541–549.CrossRefGoogle ScholarPubMed
Vu-Dac, N, Schoonjans, K, Laine, B, Fruchart, JC, Auwerx, J & Staels, B (1994) Negative regulation of the human apolipoprotein A-I promoter by fibrates can be attenuated by the interaction of the peroxisome proliferator-activated receptor with its response element. J Biol Chem 269, 31012–31018.CrossRefGoogle ScholarPubMed
Wabitsch, M, Blum, WF, Muche, R, Heinze, E, Haug, C, Mayer, H & Teller, W (1996) Insulin-like growth factors and their binding proteins before and after weight loss and their associations with hormonal and metabolic parameters in obese adolescent girls. Int J Obes Relat Metab Disord 20, 1073–1080.Google ScholarPubMed
Wright, CM, Parker, L, Lamont, D & Craft, AW (2001) Implications of childhood obesity for adult health: findings from thousand families cohort study. BMJ 323, 1280–1284.Google ScholarPubMed
Yajnik, CS (2004) Early life origins of insulin resistance and type 2 diabetes in India and other Asian countries. J Nutr 134, 205–210.CrossRefGoogle ScholarPubMed
Youssef, AA, Valdez, R, Elkasabany, A, Srinivasan, SR & Berenson, GS (2002) Time-course of adiposity and fasting insulin from childhood to young adulthood in offspring of parents with coronary artery disease: the Bogalusa Heart Study. Ann Epidemiol 12, 553–559.CrossRefGoogle ScholarPubMed