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High leptin in pregnant mink (Mustela vison) may exert anorexigenic effects: a permissive factor for rapid increase in food intake during lactation

Published online by Cambridge University Press:  09 March 2007

Anne-Helene Tauson ,
Mats Forsberg  and
André Chwalibog
Anne-Helene Tauson*
Affiliation:
Department of Animal Science and Animal Health, The Royal Veterinary and Agricultural University, Bülowsvej 13, DK-1870, Frederiksberg C, Denmark
Mats Forsberg
Affiliation:
Centre for Reproductive Biology in Uppsala, Department of Clinical Chemistry, Swedish University of Agricultural Sciences, Box 7038, S-750 07, Uppsala, Sweden
André Chwalibog
Affiliation:
Department of Animal Science and Animal Health, The Royal Veterinary and Agricultural University, Bülowsvej 13, DK-1870, Frederiksberg C, Denmark
*
*Corresponding author: Dr Anne-Helene Tauson, fax +45 35 28 30 20, email [email protected]
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Abstract

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The role for leptin in food intake regulation in the mink, a polytocous seasonal breeder with altricial young, was investigated in pregnant and lactating dams and data were related to quantitative energy metabolism measurements and plasma concentrations of other important metabolic hormones. A total of nine mink dams were measured in consecutive 1-week balance periods, each including a 22h measurement of heat production by means of indirect calorimetry, and blood was sampled at weekly intervals throughout gestation and during lactation weeks 1–4. Intake of metabolisable energy (ME) was high and energy balance was positive until the first third of true gestation. During mid- and late gestation ME intake decreased (P<0·001) while heat production remained almost constant, resulting in negative energy balance and the loss of body weight. From late gestation until lactation week 4, ME intake increased by 3·5 times, but weight loss continued. Plasma concentrations of leptin were approximately doubled during the last two-thirds of true gestation (P<0·01), demonstrating a clear gestational hyperleptinaemia. Concentrations declined rapidly after parturition and then remained stable. Insulin was independent of leptin, with low concentrations coincident with hyperleptinaemia. Also, concentrations of thyroid hormones declined during gestation, probably reflecting the low food intake. Hyperleptinaemia concomitant with low ME intake, negative energy balance and mobilisation of body reserves suggested an anorexigenic effect of leptin in pregnant mink. This suppression of food intake in late gestation might be permissive for the rapid increase in food intake occurring after parturition.

Keywords

Energy metabolismSubstrate oxidationThyroid hormonesInsulinInsulin-like growth factor-1
Type
Research Article
Information
British Journal of Nutrition , Volume 91 , Issue 3 , March 2004 , pp. 411 - 421
Copyright
Copyright © The Nutrition Society 2004

References

Amico, JA, Thomas, A, Crowley, RS & Burmeister, LA (1998) Concentrations of leptin in serum of pregnant, lactating and cycling rats and of leptin messenger ribonucleic acid in rat placental tissue. Life Sci 63, 1387–1395.Google Scholar
Anonymous (1986) European Convention for the Protection of Vertebrate Animals Used for Experimental and Other Scientific Purposes. European Treaty Series no. 123. Strasbourg: Council of Europe.Google Scholar
Baile, CA, Della-Fera, MA & Martin, RJ (2000) Regulation of metabolism and body fat mass by leptin. Ann Rev Nutr 20, 105–127.CrossRefGoogle ScholarPubMed
Baker, JR, Metcalf, PA, Johnson, RN, Newman, D & Rietz, P (1985) Use of protein based standards in automated colorimetric determination of fructoseamine in serum. Clin Chem 31, 1550–1554.Google Scholar
Blixenkrone-Møller, M, Lund, E, Mikkelsen, G & Uttenthal, Å (1987) Blood collection in mink. Scand J Lab Anim Sci 14, 99.Google Scholar
Block, SS, Butler, WR, Erhardt, RA, Bell, AW, Van Amburgh, ME & Boisclair, YR (2001) Decreased concentration of plasma leptin in periparturient dairy cows is caused by negative energy balance. J Endocrinol 171, 339–348.CrossRefGoogle ScholarPubMed
Bondar, RJL & Mead, DC (1974) Evaluation of glucose-6-phosphate dehydrogenase from Leuconostoc mesenteroides in the hexokinase method for determining glucose in serum. Clin Chem 20, 586–590.CrossRefGoogle ScholarPubMed
Brogan, RS, Mitchell, SE, Trayhurn, P & Smith, MS (1999) Suppression of leptin during lactation: contribution of the suckling stimulus versus milk production. Endocrinology 14, 2621–2627.Google Scholar
Brouwer, E (1965) Report of sub-committee on constants and factors. In Proceedings of the 3rd Symposium on Energy Metabolism. European Association of Animal Production, vol. 11, pp. 441–443 [Blaxter, KL, editor]. London: Academic Press.Google Scholar
Butte, NF, Hopkinson, JM & Nicolson, MA (1997) Leptin in human reproduction: serum leptin levels in pregnant and lactating women. J Clin Endocrinol Metab 82, 585–589.Google Scholar
Caprio, M, Fabbrini, E, Isidori, AM, Aveersa, A & Fabbri, A (2001) Leptin in reproduction. Trends Endocrinol Metab 12, 65–72.Google Scholar
Chwalibog, A, Jakobsen, K, Henckel, S & Thorbek, G (1992) Estimation of quantitative oxidation and fat retention from carbohydrate, protein and fat in growing pigs. J Anim Physiol Anim Nutr 68, 123–135.CrossRefGoogle Scholar
Cunningham, MJ, Clifton, DK & Steiner, RA (1999) Leptin's actions on the reproductive axis: perspectives and mechanisms. Biol Reprod 60, 216–222.Google Scholar
Ehrhardt, RA, Slepetis, RM, Bell, AW & Boisclair, YR (2001) Maternal leptin is elevated during pregnancy in sheep. Dom Anim Endocrinol 21, 85–96.CrossRefGoogle ScholarPubMed
Escobar-Morreale, HF, Escobar del Rey, F & Morreale de Escobar, G (1997) Thyroid hormones influence serum leptin concentrations in the rat. Endocrinology 138, 4485–4488.Google Scholar
Fink, R & Tauson, A-H (1998) Flushing of mink ( Mustela vison ): effects on energy metabolism and some blood metabolites. Anim Sci 66, 277–284.Google Scholar
Fink, R, Tauson, A-H & Forsberg, M (1998) Influence of different planes of energy supply prior to the breeding season on blood metabolites in female mink ( Mustela vison ). Reprod Nutr Dev 38, 107–116.Google Scholar
Fink, R, Tauson, A-H, Hansen, KB, Wamberg, S & Kristensen, NB (2001) Energy intake and milk production in mink ( Mustela vison ) - effect of litter size. Arch Anim Nutr 55, 221–242.Google Scholar
Frübeck, G (2001) A heliocentric view of leptin. Proc Nutr Soc 60, 301–318.Google Scholar
García, MDC, Casanueva, FF, Diéguez, C & Señarís, RM (2000) Gestational profile of leptin messenger ribonucleic acid (mRNA) content in the placenta and adipose tissue in the rat, and regulation of the mRNA levels of the leptin receptor subtypes in the hypothalamus during pregnancy and lactation. Biol Reprod 62, 698–703.CrossRefGoogle ScholarPubMed
Gavrilova, O, Barr, V, Marcus-Samuels, B & Reitman, M (1997) Hyperleptinemia of pregnancy associated with the appearance of a circulating form of the leptin receptor. J Biol Chem 272, 30546–30551.Google Scholar
Gualillo, O, Lago, F & Garcia, M (1999) Prolactin stimulates leptin secretion by rat white adipose tissue. Endocrinology 140, 5149–5153.CrossRefGoogle ScholarPubMed
Hansen, NE, Finne, L, Skrede, A & Tauson, A-H (1991) Energiforsyningen hos Mink og Rev (Energy Supply of Mink and Foxes). NJF Utredning/Rapport no. 63. Copenhagen: DSR Forlag, Landbohøjskolen.Google Scholar
Hardie, L, Trayhurn, P, Abramovich, D & Fowler, P (1997) Circulating leptin in women: a longitudinal study in the menstrual cycle and during pregnancy. Clin Endocrinol 47, 101–106.CrossRefGoogle ScholarPubMed
Harigaya, A, Nagashima, K, Nako, Y & Morikawa, A (1997) Relationship between concentration of serum leptin and fetal growth. J Clin Endocrinol Met 82, 3281–3284.Google Scholar
Havel, PJ (2000) Role of adipose tissue in body-weight regulation: mechanisms regulating leptin production and energy balance. Proc Nutr Soc 59, 359–371.CrossRefGoogle ScholarPubMed
Henson, MC & Castracane, VD (2000) Leptin in pregnancy. Biol Reprod 63, 1219–1228.CrossRefGoogle ScholarPubMed
Henson, MC, Castracane, VD & O'Neil, JS (1999) Serum leptin concentrations and expression of leptin transcripts in placental trophoblast with advancing baboon pregnancy. J Clin Endocrinol Metab 84, 2543–2549.Google Scholar
Highman, TJ, Friedman, JE, Huston, LP, Wong, WW & Catalano, PM (1998) Longitudinal changes in maternal serum leptin concentrations, body composition, and resting metabolic rate in pregnancy. Am J Obstet Gynecol 178, 1010–1015.CrossRefGoogle ScholarPubMed
Jørgensen, G, Glem-Hansen, N (1973) A cage designed for metabolism and nitrogen balance trials with mink. Acta Agric Scand 23, 3–5.CrossRefGoogle Scholar
Kawai, M, Yamaguchi, M, Murakami, T, Shima, K, Murata, Y & Kishi, K (1997) The placenta is not the main source of leptin production in pregnant rat: gestational profile of leptin in plasma and adipose tissue. Biochem Biophys Res Commun 240, 798–802.CrossRefGoogle ScholarPubMed
Koistinen, HA, Koivisto, VA, Andersson, S, et al. (1997) Leptin concentration in cord blood correlates with intrauterine growth. J Clin Endocrinol Metab 82, 3328–3330.Google ScholarPubMed
Korhonen, H & Niemälä, P (1998) Effect of ad libitum and restrictive feeding on seasonal weight changes in captive minks (Mustela vison). J Anim Physiol Anim Nutr 79, 269–280.Google Scholar
Leonhardt, U, Gerdes, E, Ritzel, U, Schäfer, G, Becker, W & Ramadori, G (1999) Immunoreactive leptin and leptin mRNA expression are increased in rat hypo- but not hyperthyroidism. J Endocrinol 163, 115–121.Google Scholar
Littell, RC, Milliken, GA, Stroup, WW & Wolfinger, RD (1996) SAS ® System for Mixed Models. Cary, NC: SAS Institute, Inc.Google Scholar
McNeill, DM, Slepetis, R, Erhardt, RA, Smith, DM & Bell, AW (1997) Protein requirement of sheep in late pregnancy: partitioning of nitrogen between gravid uterus and maternal tissues. J Anim Sci 75, 809–816.CrossRefGoogle ScholarPubMed
Masuzaki, H, Ogawa, Y, Sagawa, N et al. (1997) Non-adipose tissue production of leptin: leptin as a novel placenta-derived hormone in humans. Nature Med 3, 1029–1033.CrossRefGoogle Scholar
Morrison, CD, Wood, R, McFadin, EL, Whitley, NC & Keisler, DH (2002) Effect of intravenous infusion of recombinant ovine leptin on feed intake and serum concentrations of GH, LH, insulin, IGF-1, cortisol and thyroxine in growing prepubertal ewe lambs. Dom Anim Endocrinol 22, 103–122.Google Scholar
Mostyn, A, Keisler, DH, Webb, R, Stephenson, T & Symonds, ME (2001) The role of leptin in the transition from fetus to neonate. Proc Nutr Soc 60, 187–194.Google Scholar
Murphy, B & Douglas, D (1992) Reproduction in female mink. In Reproduction in Carnivorous Fur Bearing Animals. NJF-Utredning/Rapport no. 75, pp. 39–49 [Tauson, A-H, Valtonen, M, editors]. Copenhagen: Jordbrugsforlaget.Google Scholar
Nagatani, S, Zeng, Y, Keisler, DH, Foster, DL & Jaffe, CA (2000) Leptin regulates pulsatile luteinizing hormone and growth hormone secretion in the sheep. Endocrinology 141, 3965–3975.Google Scholar
Naismith, DJ & Morgan, BLG (1976) The biphasic nature of protein metabolism during pregnancy in the rat. Br J Nutr 36, 563–566.Google Scholar
Nes, N, Einarsson, EJ & Lohi, O (1987) Beautiful Fur Animals - and their Colour Genetics. Hillerød, Denmark: Scientifur.Google Scholar
Papke, RL, Concannon, PW, Travis, HF & Hansel, W (1980) Control of luteal function and implantation in the mink by prolactin. J Anim Sci 50, 1102–1107.Google Scholar
Pine, AP, Jessop, NS & Oldham, JD (1994) Maternal protein reserves and their influence on lactational performance in rats. Br J Nutr 71, 13–27.CrossRefGoogle ScholarPubMed
SAS Institute, Inc. (1990) SAS Procedures Guide, version 6 third ed., Cary, NC: SAS Institute, Inc.Google Scholar
Schubring, C, Englaro, P & Siebler, T (1998) Longitudinal analysis of maternal serum leptin levels during pregnancy, at birth and up to six weeks after birth: relation to body mass index, skinfolds, sex steroids and umbilical cord blood leptin levels. Horm Res 50, 276–283.Google ScholarPubMed
Schwartz, MW, Woods, SC, Porte, D, Seeley, RJ & Baskin, DG (2000) Central nervous system control of food intake. Nature 404, 661–671.CrossRefGoogle ScholarPubMed
Señarís, R, Garcia-Caballero, T & Casabiell, X (1997) Synthesis of leptin in human placenta. Endocrinology 138, 4501–4504.Google Scholar
Sivan, E, Whittaker, PG, Sinha, D et al. (1998) Leptin in human pregnancy: the relationship with gestational hormones. Am J Obst Gynecol 179, 1128–1132.CrossRefGoogle ScholarPubMed
Tauson, A-H (1991) Effect of flushing on plasma progesterone and plasma estradiol throughout gestation in mink. J Anim Physiol Anim Nutr 66, 100–110.Google Scholar
Tauson, A-H (1993) Effect of body condition and dietary energy supply on reproductive processes in the female mink ( Mustela vison ). J Reprod Fert 47, Suppl., 37–45.Google Scholar
Tauson, A-H (1994) Postnatal development in mink kits. Acta Agric Scand 44A, 177–184.Google Scholar
Tauson, A-H (1997) Prolactin profiles of pregnant, lactating and non-mated female mink ( Mustela vison ). J Reprod Fert 51, Suppl.195–201.Google Scholar
Tauson, A-H, Chwalibog, A, Fink, R, Valtonen, M & Wamberg, S (1999) A proposed model for studies on regulation of food intake in a seasonal breeder, the mink (Mustela vison). In Regulation of Feed Intake, pp. 109–113 [Van der Heide, D, Huisman, EA, Kanis, E, Osse, JWM, Verstegen, MWA, editors]. Wallingford, Oxon: CABI Publishing.Google Scholar
Tauson, A-H, Elnif, J & Hansen, NE (1991) Energy metabolism and foetal growth in the pregnant mink ( Mustela vison ). Norw J Agric Sci 9, Suppl.261–267.Google Scholar
Tauson, A-H, Elnif, J & Hansen, NE (1994) Energy metabolism and nutrient oxidation in the pregnant mink ( Mustela vison ) as a model for other carnivores. J Nutr 124, 2609S–2613S.Google Scholar
Tauson, A-H, Fink, R, Forsberg, M, Lagerkvist, G & Wamberg, S (2000) LH release in mink ( Mustela vison ). Pattern of the LH surge and effect of metabolic status. Reprod Nutr Dev 40, 229–247.Google Scholar
Tauson, A-H & Forsberg, M (2002) Body-weight changes are clearly reflected in plasma concentrations of leptin in female mink ( Mustela vison ). Br J Nutr 87, 101–105.Google Scholar
Theil, PK, Jørgensen, H & Jakobsen, K (2002) Energy and protein metabolism in pregnant sows fed two levels of dietary protein. J Anim Physiol Anim Nutr 86, 399–413.Google Scholar
Thomas, L, Wallace, JM, Aitken, RP, Mercer, JG, Trayhurn, P & Haggard, N (2001) Circulating leptin during ovine pregnancy in relation to maternal nutrition, body composition and pregnancy outcome. J Endocrinol 169, 465–476.CrossRefGoogle ScholarPubMed
Tomimatsu, T, Yamaguchi, M, Murakami, T et al. (1997) Increase of mouse leptin production by adipose tissue after midpregnancy: gestational profile of serum leptin concentration. Biochem Biophys Res Commun 240, 213–215.Google Scholar
Wang, J-LChinookoswong, N, Yin, S & Shi, Z-Q (2000) Calorigenic actions of leptin are additive to, but not dependent on, those of thyroid hormones. Am J Physiol 279, E1278–E1285.Google Scholar
Woodside, B, Abizaid, A, Walker, C-D (2000) Changes in leptin levels during lactation: implications for lactational hyperphagia and anovulation. Horm Behav 37, 353–365.CrossRefGoogle ScholarPubMed
Xiao, Y, Forsberg, M, Laitinen, JT & Valtonen, M (1995) Effects of melatonin implants in spring on testicular regression and moulting in adult male raccoon dogs ( Nyctereutes procynoides ). J Reprod Fert 105, 9–15.CrossRefGoogle ScholarPubMed
Zhang, Y, Proenca, R, Maffei, M, Barone, M, Leopold, L & Friedman, JM (1994) Positional cloning of the mouse obese gene and its human homologue. Nature 372, 425–432.CrossRefGoogle ScholarPubMed