Download PDF
Exp Clin Endocrinol Diabetes 2016; 124(10): 622-629
DOI: 10.1055/s-0042-109605
Article
© Georg Thieme Verlag KG Stuttgart · New York

Genotype-dependent Metabolic Responses to Semi-Purified High-Sucrose High-Fat Diets in the TALLYHO/Jng vs. C57BL/6 Mouse during the Development of Obesity and Type 2 Diabetes

J. K. Parkman
1   Pharmacology, Physiology and Toxicology, Marshall University, Huntington, United States
,
X. Mao
1   Pharmacology, Physiology and Toxicology, Marshall University, Huntington, United States
,
K. Dillon
1   Pharmacology, Physiology and Toxicology, Marshall University, Huntington, United States
,
A. Gudivada
1   Pharmacology, Physiology and Toxicology, Marshall University, Huntington, United States
,
N. Moustaid-Moussa
2   Department of Nutritional Sciences, Texas Tech University, Lubbock, United States
,
A. M. Saxton
3   Department of Animal Science, University of Tennessee, Knoxville, United States
,
J. H. Kim
1   Pharmacology, Physiology and Toxicology, Marshall University, Huntington, United States
› Author Affiliations
Further Information

Publication History

received 12 January 2016
first decision 16 May 2016

accepted 01 June 2016

Publication Date:
20 July 2016 (online)

Also available at
    Permissions and Reprints

Abstract

Background: The co-epidemic of obesity and type 2 diabetes is associated with increased morbidity and mortality. Genetic factors are highly involved in the development of these diseases, in the form of interactions of multiple genes within obesogenic and diabetogenic environments, such as a high fat diet. The TALLYHO/Jng (TH) mouse is an inbred polygenic model for human obesity and type 2 diabetes. In order to further develop the TH mouse as a clinically relevant model, we investigated diet dependence of obesity and type 2 diabetes in TH mice vs. C57BL/6 (B6) mice.

Results: TH and B6 mice were weaned onto a standard rodent chow, semi-purified high-sucrose low-fat (HSLF), or semi-purified high-sucrose high-fat (HSHF) diet and maintained on these diets throughout the study. Despite similar fat contents in HSLF diets and chow, both B6 and TH mice responded to HSLF diets, with increases in adiposity. TH mice, but not B6 mice, exhibited significantly higher adiposity with severely aggravated glucose intolerance and hyperglycemia on HSHF diets compared to the other diets. HSLF diets also advanced diabetes in TH mice compared to chow, but it did not surpass the effects of HSHF diets. The severe glucose intolerance and hyperglycemia in TH mice on both HSLF and HSHF diets were accompanied by significantly reduced Glut4 mRNA levels compared to B6 mice.

Conclusions: The present data demonstrate that diets are important modulators of genetic susceptibility to type 2 diabetes and obesity in TH mice. The interplay between heredity and dietary environment in TH mice appears to amplify insulin resistance, contributing to severe glucose intolerance and diabetes.

Key words

high fat diet - high sucrose diet - obesity - type 2 diabetes - genetics - TALLYHO
 

  • References

  • 1 Kelly T, Yang W, Chen CS et al. Global burden of obesity in 2005 and projections to 2030. Int J Obes (Lond) 2008; 32: 1431-1437
    CrossrefPubMedSearch in Google Scholar
  • 2 Guariguata L, Whiting DR, Hambleton I et al. Global estimates of diabetes prevalence for 2013 and projections for 2035. Diabetes Res Clin Pract 2014; 103: 137-149
    Search in Google Scholar
  • 3 Gavin 3rd JR, Freeman JS, Shubrook Jr JH et al. Type 2 diabetes mellitus: practical approaches for primary care physicians. J Am Osteopath Assoc 2011; 111 (Suppl. 04) S3-S12
    PubMedSearch in Google Scholar
  • 4 Bouret S, Levin BE, Ozanne SE. Gene-environment interactions controlling energy and glucose homeostasis and the developmental origins of obesity. Physiol Rev 2015; 95: 47-82
    CrossrefPubMedSearch in Google Scholar
  • 5 Walker CG, Solis-Trapala I, Holzapfel C et al. Modelling the Interplay between Lifestyle Factors and Genetic Predisposition on Markers of Type 2 Diabetes Mellitus Risk. PLoS One 2015; 10: e0131681
    CrossrefPubMedSearch in Google Scholar
  • 6 Hariri N, Thibault L. High-fat diet-induced obesity in animal models. Nutr Res Rev 2010; 23: 270-299
    CrossrefPubMedSearch in Google Scholar
  • 7 Kim JH, Saxton AM. The TALLYHO mouse as a model of human type 2 diabetes. Methods Mol Biol 2012; 933: 75-87
    PubMedSearch in Google Scholar
  • 8 Grarup N, Sandholt CH, Hansen T et al. Genetic susceptibility to type 2 diabetes and obesity: from genome-wide association studies to rare variants and beyond. Diabetologia 2014; 57: 1528-1541
    CrossrefPubMedSearch in Google Scholar
  • 9 Kim JH, Sen S, Avery CS et al. Genetic analysis of a new mouse model for non-insulin dependent diabetes. Genomics 2001; 74: 273-286
    CrossrefPubMedSearch in Google Scholar
  • 10 Kim JH, Stewart TP, Soltani-Bejnood M et al. Phenotypic characterization of polygenic type 2 diabetes in TALLYHO/JngJ mice. J Endocrinol 2006; 191: 437-446
    CrossrefPubMedSearch in Google Scholar
  • 11 Mao X, Dillon KD, McEntee MF et al. Islet insulin secretion, β-cell mass, and energy balance in a polygenic mouse model of Type 2 diabetes with obesity. JIEMS 2014; 1-6
    PubMedSearch in Google Scholar
  • 12 Arai C, Miyake M, Matsumoto Y et al. Trehalose prevents adipocyte hypertrophy and mitigates insulin resistance in mice with established obesity. J Nutr Sci Vitaminol (Tokyo) 2013; 59: 393-401
    CrossrefPubMedSearch in Google Scholar
  • 13 Dalen KT, Ulven SM, Bamberg K et al. Expression of the insulin-responsive glucose transporter GLUT4 in adipocytes is dependent on liver X receptor alpha. J Biol Chem 2003; 278: 48283-48291
    CrossrefPubMedSearch in Google Scholar
  • 14 Stewart TP, Kim HY, Saxton AM et al. Genetic and genomic analysis of hyperlipidemia, obesity and diabetes using (C57BL/6J×TALLYHO/JngJ) F2 mice. BMC Genomics 2010; 11: 713
    CrossrefPubMedSearch in Google Scholar
  • 15 Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25: 402-408
    CrossrefPubMedSearch in Google Scholar
  • 16 Tschöp MH, Speakman JR, Arch JR et al. A guide to analysis of mouse energy metabolism. Nat Methods 2011; 9: 57-63
    CrossrefPubMedSearch in Google Scholar
  • 17 Vaitheesvaran B, LeRoith D, Kurland IJ. MKR mice have increased dynamic glucose disposal despite metabolic inflexibility, and hepatic and peripheral insulin insensitivity. Diabetologia 2010; 53: 2224-2232
    CrossrefPubMedSearch in Google Scholar
  • 18 Lauterio TJ, Bond JP, Ulman EA. Development and characterization of a purified diet to identify obesity-susceptible and resistant rat populations. J Nutr 1994; 124: 2172-2178
    PubMedSearch in Google Scholar
  • 19 Levin BE, Triscari J, Sullivan AC. Altered sympathetic activity during development of diet-induced obesity in rat. Am J Physiol 1983; 244: R347-R355
    PubMedSearch in Google Scholar
  • 20 Levin BE, Triscari J, Sullivan AC. Relationship between sympathetic activity and diet-induced obesity in two rat strains. Am J Physiol 1983; 245: R364-R371
    PubMedSearch in Google Scholar
  • 21 Last AR, Wilson SA. Low-carbohydrate diets. Am Fam Physician 2006; 73: 1942-1948
    PubMedSearch in Google Scholar
  • 22 Mirhashemi F, Scherneck S, Kluth O et al. Diet dependence of diabetes in the New Zealand Obese (NZO) mouse: total fat, but not fat quality or sucrose accelerates and aggravates diabetes. Exp Clin Endocrinol Diabetes 2011; 119: 167-171
    Thieme ConnectPubMedSearch in Google Scholar
  • 23 Opara EC, Petro A, Tevrizian A et al. L-glutamine supplementation of a high fat diet reduces body weight and attenuates hyperglycemia and hyperinsulinemia in C57BL/6J mice. J Nutr 1996; 126: 273-279
    PubMedSearch in Google Scholar
  • 24 Black BL, Croom J, Eisen EJ et al. Differential effects of fat and sucrose on body composition in A/J and C57BL/6 mice. Metabolism 1998; 47: 1354-1359
    CrossrefPubMedSearch in Google Scholar
  • 25 Hill CM, Arum O, Boparai RK et al. Female PAPP-A knockout mice are resistant to metabolic dysfunction induced by high-fat/high-sucrose feeding at middle age. Age (Dordr) 2015; 37: 9765
    PubMedSearch in Google Scholar
  • 26 Heber D, Zhang Y, Yang J et al. Green tea, black tea, and oolong tea polyphenols reduce visceral fat and inflammation in mice fed high-fat, high-sucrose obesogenic diets. J Nutr 2014; 144: 1385-1393
    CrossrefPubMedSearch in Google Scholar
  • 27 Cope MB, Jumbo-Lucioni P, Walton RG et al. No effect of dietary fat on short-term weight gain in mice treated with atypical antipsychotic drugs. Int J Obes (Lond) 2007; 31: 1014-1022
    CrossrefPubMedSearch in Google Scholar
  • 28 Chassaing B, Miles-Brown J, Pellizzon M et al. Lack of soluble fiber drives diet-induced adiposity in mice. Am J Physiol Gastrointest Liver Physiol 2015; 309: G528-G541
    CrossrefPubMedSearch in Google Scholar
  • 29 Mhyre TR, Chesler EJ, Thiruchelvam M et al. Heritability, correlations and in silico mapping of locomotor behavior and neurochemistry in inbred strains of mice. Genes Brain Behav 2005; 4: 209-228
    PubMedSearch in Google Scholar
  • 30 Leibel RL, Rosenbaum M, Hirsch J. Changes in energy expenditure resulting from altered body weight. N Engl J Med 1995; 332: 621-628
    CrossrefPubMedSearch in Google Scholar
  • 31 Scheepers A, Joost HG, Schürmann A. The glucose transporter families SGLT and GLUT: molecular basis of normal and aberrant function. JPEN J Parenter Enteral Nutr 2004; 28: 364-371
    CrossrefPubMedSearch in Google Scholar
  • 32 Leiter EH. The NOD mouse: a model for analyzing the interplay between heredity and environment in development of autoimmune disease. ILAR News 1993; 35: 4-14
    CrossrefPubMedSearch in Google Scholar
  • 33 Cheng ZJ, Jiang YF, Ding H et al. Vascular dysfunction in type 2 diabetic TallyHo mice: role for an increase in the contribution of PGH2/TxA2 receptor activation and cytochrome p450 products. Can J Physiol Pharmacol 2007; 85: 404-412
    CrossrefPubMedSearch in Google Scholar