Fat-tailed and thin-tailed lambs responses to glucose and insulin challenges during different energy balances

Document Type : Original Research Article (Regular Paper)

Authors

Department of Animal Science, University of Tehran, Karaj, Iran

Abstract

The proportion of adipose depots varies considerably between fat-tailed (FT) and thin-tailed (TT) sheep breeds. FT breeds accumulate majority of body fat in fat-tail depot, whereas TT breeds deposit considerable proportion of body fat in visceral depots. These differences in proportion of adipose depots seem to affect body metabolism due to differences in metabolism of different depots. Hence, the current research aimed to evaluate the response of fat-tailed lambs (FTL) and thin-tailed lambs (TTL) to glucose and insulin challenges during negative energy balance (NEB) and positive energy balance (PEB). Glucose tolerance and insulin challenge tests were conducted on randomly selected lambs from each genotypes at the end of induced NEB and PEB. Glucose injection during NEB caused greater plasma glucose concentration in TTL, whereas in PEB, the enhancement in glucose concentration as a consequence of glucose injection was higher in FTL (P≤0.09). The area under the glucose curve was higher in FT compared to TT lambs during glucose tolerance test regardless of energy balance (EB; P≤0.03). The clearance rates of insulin (P≤0.09) and glucose (P≤0.006) in the respective insulin and glucose tolerance tests were higher during PEB compared to NEB regardless of the genotypes. These results demonstrated that induced NEB can enhance insulin resistance in both FT and TT lambs, severity of which is greater in FT than in TT lambs. 

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References

Almeida, A.M., Palhinhas, R.G., Kilminster, T., Scanlon, T., van Harten, S., Milton, J., Blache, D., Greeff, J., Oldham, C, Coelho, A.V., 2016. The effect of weight loss on the muscle proteome in the damara, dorper and australian merino ovine breeds. PloS One 11, e0146367.
Bossaert, P., Leroy, J., De Vliegher, S., Opsomer, G., 2008. Interrelations between glucose-induced insulin response, metabolic indicators, and time of first ovulation in high-yielding dairy cows. Journal of Dairy Science 91, 3363-3371.
Bradford, B.J., Mamedova, L.K., Minton, J.E., Drouillard, J.S., Johnson, B.J., 2009. Daily injection of tumor necrosis factor-α increases hepatic triglycerides and alters transcript abundance of metabolic genes in lactating dairy cattle. The Journal of Nutrition 139, 1451-1456.
Cincović, M., Hristovska, T., Belić, B., 2018. Niacin, Metabolic Stress and Insulin Resistance in Dairy Cows. In: B Group Vitamins-Current Uses and Perspectives, IntechOpen. 107-124.
De Koster, J.D., Opsomer, G., 2013. Insulin resistance in dairy cows. Veterinary Clinics of North America: Food Animal Practice 29, 299-322.
De Koster, J.D., Hostens, M., Van Eetvelde, M., Hermans, K., Moerman, S., Bogaert, H., Depreester, E., Van Den Broeck, W, Opsomer, G., 2015. Insulin response of the glucose and fatty acid metabolism in dry dairy cows across a range of body condition scores. Journal of Dairy Science 98, 4580-4592.
De Fronzo, R.A., 2004. Pathogenesis of type 2 diabetes mellitus. Medical Clinics of North America 88, 787-835.
Drackley, J., Wallace, R., Graugnard, D., Vasquez, J., Richards, B., Loor, J., 2014. Visceral adipose tissue mass in nonlactating dairy cows fed diets differing in energy density 1. Journal of Dairy Science 97, 3420-3430.
Duehlmeier, R., Fluegge, I., Schwert, B., Ganter, M., 2013. Insulin sensitivity during late gestation in ewes affected by pregnancy toxemia and in ewes with high and low susceptibility to this disorder. Journal of Veterinary Internal Medicine 27, 359-366.
Duhlmeier, R., Hacker, A., Widdel, A., Von Engelhardt, W., Sallmann, H.-P., 2005. Mechanisms of insulin-dependent glucose transport into porcine and bovine skeletal muscle. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology 289, R187-R197.
Duwaerts, C.C., Maher, J.J., 2019. Macronutrients and the adipose-liver axis in obesity and fatty liver. Cellular and Molecular Gastroenterology and Hepatology 7, 749-761.
Eryavuz, A., Avci, G., Kuculkkurt, I., Fidan, A., 2007. Comparison of plasma leptin, insulin and thyroid hormone concentrations and some biochemical parameters between fat-tailed and thin-tailed sheep breeds. Revue de Médecine Vétérinaire 158, 244-249.
Fontana, L., Eagon, J.C., Trujillo, M.E., Scherer, P.E., Klein, S., 2007. Visceral fat adipokine secretion is associated with systemic inflammation in obese humans. Diabetes 56, 1010-1013.
Guilherme, A., Henriques, F., Bedard, A.H., Czech, M.P., 2019. Molecular pathways linking adipose innervation to insulin action in obesity and diabetes mellitus. Nature Reviews Endocrinology 15, 207-225.
Herdt, T.H., 2013. Metabolic diseases of dairy cattle. The Veterinary Clinics of North America. Food animal practice V29, N2.
Ibrahim, M.M., 2010. Subcutaneous and visceral adipose tissue: structural and functional differences. Obesity Reviews 11, 11-18.
Ji, P., Drackley, J., Khan, M., Loor, J., 2014. Inflammation-and lipid metabolism-related gene network expression in visceral and subcutaneous adipose depots of Holstein cows. Journal of Dairy Science 97, 3441-3448.
Johnston, L.W., Harris, S.B., Retnakaran, R., Giacca, A., Liu, Z., Bazinet, R.P., Hanley, A.J., 2018. Association of NEFA composition with insulin sensitivity and beta cell function in the Prospective Metabolism and Islet Cell Evaluation (Promise) cohort. Diabetologia 61, 821-830.
Kaneko, J.J., 1989. Carbohydrate metabolism and its diseases. Clinical Biochemistry of Domestic Animals 4, 44-81.
Kerestes, M., Faigl, V., Kulcsár, M., Balogh, O., Földi, J., Fébel, H., Chilliard, Y., Huszenicza, G., 2009. Periparturient insulin secretion and whole-body insulin responsiveness in dairy cows showing various forms of ketone pattern with or without puerperal metritis. Domestic Animal Endocrinology 37, 250-261.
Kerouz, N.J., Hörsch, D., Pons, S., Kahn, C.R., 1997. Differential regulation of insulin receptor substrates-1 and-2 (IRS-1 and IRS-2) and phosphatidylinositol 3-kinase isoforms in liver and muscle of the obese diabetic (ob/ob) mouse. Journal of Clinical Investigation 100, 3164.
Khachadurian, A., Adrouni, B., Yacoubian, H., 1966. Metabolism of adipose tissue in the fat tail of the sheep in vivo. Journal of Lipid Research 7, 427-436.
Kushibiki, S., Hodate, K., Shingu, H., Ueda, Y., Mori, Y., Itoh, T., Yokomizo, Y., 2001. Effects of long-term administration of recombinant bovine tumor necrosis factor-α on glucose metabolism and growth hormone secretion in steers. American Journal of Veterinary Research 62, 794-798.
Lee, M.-W., Lee, M., Oh, K.-J., 2019. Adipose tissue-derived signatures for obesity and type 2 diabetes: adipokines, batokines and microRNAs. Journal of Clinical Medicine 8, 854.
Lewis, G.F., Zinman, B., Groenewoud, Y., Vranic, M., Giacca, A., 1996. Hepatic glucose production is regulated both by direct hepatic and extrahepatic effects of insulin in humans. Diabetes 45, 454-462.
Marcadenti, A., de Abreu-Silva, E.O., 2015. Different adipose tissue depots: Metabolic implications and effects of surgical removal. Endocrinologia y Nutrición 62, 458-464.
Newsholme, P., Cruzat, V., Arfuso, F., Keane, K., 2014. Nutrient regulation of insulin secretion and action. Journal of Endocrinology 221, R105-R120.
Ohtsuka, H., Koiwa, M., Hatsugaya, A., Kudo, K., Hoshi, F., Itoh, N., Yokota, H., Okada, H., Kawamura, S.-i., 2001. Relationship between serum TNF activity and insulin resistance in dairy cows affected with naturally occurring fatty liver. Journal of Veterinary Medical Science 63, 1021-1025.
Saremi, B., Winand, S., Friedrichs, P., Kinoshita, A., Rehage, J., Dänicke, S., Häussler, S., Breves, G., Mielenz, M., Sauerwein, H., 2014. Longitudinal profiling of the tissue-specific expression of genes related with insulin sensitivity in dairy cows during lactation focusing on different fat depots. PloS One 9, e86211.
SAS, 2008. SAS User’s Guide: Statistics. Version 9.2. SAS Institute Inc., Cary, North Carolina. USA.
Sears, B., Perry, M., 2015. The role of fatty acids in insulin resistance. Lipids in Health and Disease 14, 1-9.
Shiang, K., 2004. The SAS calculations of areas under the curve (AUC) for multiple metabolic readings. In: SAS Conference Proceedings Western Users of SAS (WUSS), pp. 13-15.
Spalding, K.L., Bernard, S., Näslund, E., Salehpour, M., Possnert, G., Appelsved, L., Fu, K.-Y., Alkass, K., Druid, H., Thorell, A., 2017. Impact of fat mass and distribution on lipid turnover in human adipose tissue. Nature Communications 8, 1-9.
Xu, C., Shu, S., Xia, C., Wang, B., Zhang, H., Jun, B., 2014. Investigation on the relationship of insulin resistance and ketosis in dairy cows. Journal of Veterinary Science and Technology 5. 162.
Zachut, M., Honig, H., Striem, S., Zick, Y., Boura-Halfon, S., Moallem, U., 2013. Periparturient dairy cows do not exhibit hepatic insulin resistance, yet adipose-specific insulin resistance occurs in cows prone to high weight loss. Journal of Dairy Science 96, 5656-5669.

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