DOI QR코드

DOI QR Code

High Food Efficiency Ratio of Prepubertal Growth Period Leads to a Long-Term Susceptibility for Obesity and Insulin Resistance in Obesity-Prone and Obesity-Resistant Sprague Dawley Rats

  • Choi, Joo Sun (Dept. of Home Economics, College of Education, Kyungnam University)
  • Received : 2017.06.29
  • Accepted : 2017.08.24
  • Published : 2017.08.31

Abstract

Excessive body weight gain during the growth period of early life may predispose individuals towards obesity and metabolic disorder in later life. We investigated the possibility of using the food efficiency ratio as an early indicator for predicting susceptibility to diet-induced obesity and insulin resistance. Four-week-old, prepubertal, male Sprague Dawley rats were divided into obesity-prone and obesity-resistant groups based on food efficiency ratio values after five days on a high-fat diet. Metabolic parameters measured after 2, 6, and 10 weeks, and specific phenotypes were compared with each group. Obesity-prone rats had higher increases in body weight and fat mass compared to obesity-resistant rats over the study period. Obesity-prone rats became glucose intolerant early in this study and remained so throughout the experimental period, with increases in fat weight and leptin levels occurring first, followed by increases in insulin level. Gluconeogenesis and insulin resistance significantly increased in obesity-prone groups in which activities of glucose-6-phosphatase and phosphoenolpyruvate carboxykinase were increased and glucokinase activity decreased. Higher food efficiency ratio at an early age was closely correlated with body fat accumulation, hyperleptinemia, and hyperinsulinemia of middle and elderly age. We suggest a high food efficiency ratio in prepubertal subjects may be a useful predictor of future obesity and insulin resistance.

Keywords

References

  1. Aas AM, Hanssen KF, Berg JP, Thorsby PM, Birkeland KI. 2009. Insulin-stimulated increase in serum leptin levels precedes and correlates with weight gain during insulin therapy in type 2 diabetes. J Clin Endocrinol Metab 94:2900-2906 https://doi.org/10.1210/jc.2008-1005
  2. Alexander J, Chang GQ, Dourmashkin JT, Leibowitz SF. 2006. Distinct phenotypes of obesity-prone AKR/J, DBA2J and C57BL/6J mice compared to control strains. Int J Obes 30:50-59 https://doi.org/10.1038/sj.ijo.0803110
  3. Baginski ES, Foa PP, Zak B. 1974. Glucose-6-phosphatase. In: Methods of Enzymatic Analysis. p. 876. Academic Press
  4. Bentla LA, Lardy HA. 1976. Interaction of anions and divalent metal ions with phosphoenolpyruvate carboxykinase. J Biol Chem 251:2916-2921
  5. Bjornholm M, Munzberg H, Leshan RL, Villanueva EC, Bates SH, Louis GW, Jones JC, Ishida-Takahashi R, Bjorbaek C, Myers MG, Jr. 2007. Mice lacking inhibitory leptin receptor signals are lean with normal endocrine function. J Clinical Invest 117:1354-1360 https://doi.org/10.1172/JCI30688
  6. Bligh EG, Dyer WJ. 1959. A rapid method of total lipid extraction and purification. Can J Med Sci 37:911-917
  7. Cerf ME, Williams K, Nkomo XI, Muller J, Du Toit DF, Louw J, Wolfe-Coote SA. 2005. Islet cell response in the neonatal rat after exposure to a high-fat diet during pregnancy. Am J Physiol Regul Integr Comp Physiol 288:R1122-R1128 https://doi.org/10.1152/ajpregu.00335.2004
  8. Dourmashkin JT, Chang GQ, Hill JO, Gayles EC, Fried SK, Leibowitz SF. 2006. Model for predicting and phenotyping at normal weight the long-term propensity for obesity in Sprague-Dawley rats. Physiol Behavior 87:666-678 https://doi.org/10.1016/j.physbeh.2006.01.008
  9. Ehrenberg HM, Huston-Presley L, Catalano PM. 2003. The influence of obesity and gestational diabetes mellitus on accretion and the distribution of adipose tissue in pregnancy. Am J Obstet Gynecol 189:944-948 https://doi.org/10.1067/S0002-9378(03)00761-0
  10. Friedewald WT, Levy RI, Fredrickson DS. 1972. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 18:499-502
  11. Frihauf JB, Fekete EM, Nagy TR, Levin BE, Zorrilla EP. 2016. Maternal western diet increases adiposity even in male offspring of obesity-resistant rat dams: early endocrine risk markers. Am J Physiol Regul Integr Comp Physiol 311:R1045-R1059 https://doi.org/10.1152/ajpregu.00023.2016
  12. Fujimoto S, Ishida H, Kato S, Okamoto Y, Tsuji K, Mizuno N, Ueda S, Mukai E, Seino Y. 1998. The novel insulinotropic mechanism of pimobendan: direct enhancement of the exocytotic process of insulin secretory granules by increased $Ca^{2+}$ sensitivity in ${\beta}$-cells. Endocrinol 139:1133-1140 https://doi.org/10.1210/endo.139.3.5771
  13. Giles ED, Jackman MR, MacLean PS. 2016. Modeling diet-induced obesity with obesity-prone rats: implications for studies in females. Front Nutr 3:50
  14. Gorski JN, Dunn-Meynell AA, Hartman TG, Levin BE. 2006. Postnatal environment overrides genetic and prenatal factors influencing offspring obesity and insulin resistance. Am J Physiol Regulatory Integrative Comp Physiol 291:768-778 https://doi.org/10.1152/ajpregu.00138.2006
  15. Ikenasio-Thorpe BA, Breier BH, Vickers MH, Fraser M. 2007. Prenatal influences on susceptibility to diet-induced obesity are mediated by altered neuroendocrine gene expression. J Endocrinol 193:31-37 https://doi.org/10.1677/joe.1.07017
  16. Ji H, Friedman MI. 2008. Reduced hepatocyte fatty acid oxidation in outbred rats prescreened for susceptibility to diet-induced obesity. Int J Obes 32:1331-1334 https://doi.org/10.1038/ijo.2008.71
  17. Kang MJ, Park JY, Kim JY, Lee YJ, Do MH, Lee SS. 2014. The prevalence of obesity by percentage of body fat, waist circumference, and body mass index and their association with prevalence of chronic diseases of elderly in Seoul area. Korean J Food Nutr 27:358-368 https://doi.org/10.9799/ksfan.2014.27.3.358
  18. Kotronen A, Juurinen L, Tiikkainen M, Vehkavaara S, Yki-Jarvinen H. 2008. Increased liver fat, impaired insulin clearance, and hepatic and adipose tissue insulin resistance in type 2 diabetes. Gastroenterol 135:122-130 https://doi.org/10.1053/j.gastro.2008.03.021
  19. Leibowitz SF, Chang GQ, Dourmashkin JT, Yun R, Julien C, Pamy PP. 2006. Leptin secretion after a high-fat meal in normal-weight rats: strong predictor of long-term body fat accrual on a high-fat diet. Am J Physiol Endocrinol Metab 290:E258-E267 https://doi.org/10.1152/ajpendo.00609.2004
  20. Leibowitz KL, Chang GQ, Pamy PS, Hill JO, Gayles EC, Leibowitz SF. 2007. Weight gain model in prepubertal rats: prediction and phenotyping of obesity-prone animals at normal body weight. Int J Obes 31:1210-1221 https://doi.org/10.1038/sj.ijo.0803634
  21. Levin BE, Dunn-Meynell AA, Balkan B, Keesey RE. 1997. Selective breeding for diet-induced obesity and resistance in Sprague-Dawley rats. Am J Physiol 273:R725-R730
  22. Levin BE, Dunn-Meynell AA, Banks WA. 2004. Obesity-prone rats have normal blood brain barrier transport but defective central leptin signaling before obesity onset. Am J Physiol Regul Integr Comp Physiol 286:R143-R450 https://doi.org/10.1152/ajpregu.00393.2003
  23. Levine JA, Lanningham-Foster LM, McCrady SK, Krizan AC, Olson LR, Kane PH, Jensen MD, Clark MM. 2005. Interindividual variation in posture allocation: possible role in human obesity. Science 307:584-586 https://doi.org/10.1126/science.1106561
  24. Retnakaran R, Shen S, Hanley AJ, Vuksan V, Hamilton JK, Zinman B. 2008. Hyperbolic relationship between insulin secretion and sensitivity on oral glucose tolerance test. Obesity 16:1901-1907 https://doi.org/10.1038/oby.2008.307
  25. Li H, Xie Z, Lin J, Song H, Wang Q, Wang K, Su M, Qiu Y, Zhao T, Song K, Wang X, Zhou M, Liu P, Zhao G, Zhang Q, Jia W. 2008. Transcriptomic and metabonomic profiling of obesity-prone and obesity-resistant rats under high fat diet. J Proteome Res 7:4775-4783 https://doi.org/10.1021/pr800352k
  26. Lin S, Thomas TC, Storlien LH, Huang XF. 2000. Development of high fat diet-induced obesity and leptin resistance in C57Bl/6J mice. Int J Obes Relat Metab Disord 24:639-646 https://doi.org/10.1038/sj.ijo.0801209
  27. Matthews DR, Hosker JP, Rudenski AS. 1985. Homeostasis model assessment: insulin resistance and ${\beta}$-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28:412-419 https://doi.org/10.1007/BF00280883
  28. Maximova K, McGrath JJ, Barnett T, O'Loughlin J, Paradis G, Lambert M. 2008. Do you see what I see? Weight status misperception and exposure to obesity among children and adolescents. Int J Obes 32:1008-1015 https://doi.org/10.1038/ijo.2008.15
  29. Nam M, Choi MS, Jung S, Jung Y, Choi JY, Ryu DH, Hwang GS. 2015. Lipidomic profiling of liver tissue from obesity-prone and obesity-resistant mice fed a high fat diet. Sci Rep 5:16984 https://doi.org/10.1038/srep16984
  30. Olefsky J, Farquhar JW, Reaven G. 1973. Relationship between fasting plasma insulin level and resistance to insulin-mediated glucose uptake in normal and diabetic subjects. Diabetes 22:507-513 https://doi.org/10.2337/diab.22.7.507
  31. Pilkis SJ. 1975. Glucokinase of rat liver. In: Methods of Enzymatic Analysis. pp. 31-39. Academic Press
  32. Scarpace PJ, Zhang Y. 2009. Leptin resistance: a predisposing factor for diet-induced obesity. Am J Physiol Regul Integr Comp Physiol 296:R493-R500 https://doi.org/10.1152/ajpregu.90669.2008
  33. Shao S, Fang Z, Yu X, Zhang M. 2009. Transcription factors involved in glucose-stimulated insulin secretion of pancreatic beta cells. Biochem Biophys Res Commun 384:401-414 https://doi.org/10.1016/j.bbrc.2009.04.135
  34. Sun H, Yan J, Sun B, Song L, Yan J. 2017. Taste sensitivity to sucrose is lower in outbred Sprague-Dawley phenotypic obesity-prone rats than obesity-resistant rats. Biochem Biophys Res Commun 489:155-163 https://doi.org/10.1016/j.bbrc.2017.05.117
  35. Tulipano G, Vergoni AV, Soldi D, Muller EE, Cocchi D. 2004. Characterization of the resistance to the anorectic and endocrine effects of leptin in obesity-prone and obesity-resistant rats fed a high-fat diet. J Endocrinol 183:289-298 https://doi.org/10.1677/joe.1.05819
  36. Winzell MS, Ahren B. 2004. The high-fat diet-fed mouse: a model for studying mechanisms and treatment of impaired glucose tolerance and type 2 diabetes. Diabetes 53: S215-S219 https://doi.org/10.2337/diabetes.53.suppl_3.S215
  37. Winzell MS, Ahren B. 2008. Durable islet effects on insulin secretion and protein kinase a expression following exendin-4 treatment of high-fat diet-fed mice. J Mol Endocrinol 40:93-100 https://doi.org/10.1677/JME-07-0121
  38. Wortham M, Sander M. 2016. Mechanisms of ${\beta}$-cell functional adaptation to changes in workload. Diabetes Obes Metab 18:S78-S86 https://doi.org/10.1111/dom.12729
  39. Yura S, Itoh H, Sagawa N, Yamamoto H, Masuzaki H, Nakao K, Kawamura M, Takemura M, Kakui K, Ogawa Y, Fujii S. 2005. Role of premature leptin surge in obesity resulting from intrauterine undernutrition. Cell Metabol 1:371-378 https://doi.org/10.1016/j.cmet.2005.05.005