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Journal of Nutrition and Metabolism
Volume 2015 (2015), Article ID 758080, 13 pages
http://dx.doi.org/10.1155/2015/758080
Research Article

A Comparative Study of the Metabolic and Skeletal Response of C57BL/6J and C57BL/6N Mice in a Diet-Induced Model of Type 2 Diabetes

1Department of Nutritional Sciences, Oklahoma State University, Stillwater, OK 74078, USA
2Center for Cancer Prevention and Drug Development, University of Oklahoma Health Sciences Center, Oklahoma City, OK 73104, USA

Received 4 December 2014; Revised 8 May 2015; Accepted 12 May 2015

Academic Editor: H. K. Biesalski

Copyright © 2015 Elizabeth Rendina-Ruedy et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. U. Rishaug, K. I. Birkeland, J. A. Falch, and S. Vaaler, “Bone mass in non-insulin-dependent diabetes mellitus,” Scandinavian Journal of Clinical and Laboratory Investigation, vol. 55, no. 3, pp. 257–262, 1995. View at Publisher · View at Google Scholar · View at Scopus
  2. P. L. A. van Daele, R. P. Stolk, H. Burger et al., “Bone density in non-insulin-dependent diabetes mellitus: the Rotterdam study,” Annals of Internal Medicine, vol. 122, no. 6, pp. 409–414, 1995. View at Publisher · View at Google Scholar · View at Scopus
  3. R. P. Stolk, P. L. A. van Daele, H. A. P. Pols et al., “Hyperinsulinemia and bone mineral density in an elderly population: the Rotterdam study,” Bone, vol. 18, no. 6, pp. 545–549, 1996. View at Publisher · View at Google Scholar · View at Scopus
  4. K. K. Nicodemus and A. R. Folsom, “Type 1 and type 2 diabetes and incident hip fractures in postmenopausal women,” Diabetes Care, vol. 24, no. 7, pp. 1192–1197, 2001. View at Publisher · View at Google Scholar · View at Scopus
  5. L. J. Melton III, C. L. Leibson, S. J. Achenbach, T. M. Therneau, and S. Khosla, “Fracture risk in type 2 diabetes: update of a population-based study,” Journal of Bone and Mineral Research, vol. 23, no. 8, pp. 1334–1342, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. A. V. Schwartz, D. E. Sellmeyer, K. E. Ensrud et al., “Older women with diabetes have an increased risk of fracture: a prospective study,” Journal of Clinical Endocrinology and Metabolism, vol. 86, no. 1, pp. 32–38, 2001. View at Publisher · View at Google Scholar · View at Scopus
  7. M. Janghorbani, D. Feskanich, W. C. Willett, and F. Hu, “Prospective study of diabetes and risk of hip fracture: the nurses' health study,” Diabetes Care, vol. 29, no. 7, pp. 1573–1578, 2006. View at Publisher · View at Google Scholar · View at Scopus
  8. A. V. Schwartz, E. Vittinghoff, D. C. Bauer et al., “Association of BMD and FRAX score with risk of fracture in older adults with type 2 diabetes,” Journal of the American Medical Association, vol. 305, no. 21, pp. 2184–2192, 2011. View at Publisher · View at Google Scholar · View at Scopus
  9. R. J. Fajardo, L. Karim, V. I. Calley, and M. L. Bouxsein, “A review of rodent models of type 2 diabetic skeletal fragility,” Journal of Bone and Mineral Research, vol. 29, no. 5, pp. 1025–1040, 2014. View at Publisher · View at Google Scholar · View at Scopus
  10. R. S. Surwit, C. M. Kuhn, C. Cochrane, J. A. McCubbin, and M. N. Feinglos, “Diet-induced type II diabetes in C57BL/6J mice,” Diabetes, vol. 37, no. 9, pp. 1163–1167, 1988. View at Publisher · View at Google Scholar · View at Scopus
  11. S. Collins, T. L. Martin, R. S. Surwit, and J. Robidoux, “Genetic vulnerability to diet-induced obesity in the C57BL/6J mouse: physiological and molecular characteristics,” Physiology & Behavior, vol. 81, no. 2, pp. 243–248, 2004. View at Publisher · View at Google Scholar · View at Scopus
  12. C. Gallou-Kabani, A. Vigé, M.-S. Gross et al., “C57BL/6J and A/J mice fed a high-fat diet delineate components of metabolic syndrome,” Obesity, vol. 15, no. 8, pp. 1996–2005, 2007. View at Publisher · View at Google Scholar · View at Scopus
  13. J. J. Cao, B. R. Gregoire, and H. Gao, “High-fat diet decreases cancellous bone mass but has no effect on cortical bone mass in the tibia in mice,” Bone, vol. 44, no. 6, pp. 1097–1104, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. J. M. Patsch, F. W. Kiefer, P. Varga et al., “Increased bone resorption and impaired bone microarchitecture in short-term and extended high-fat diet-induced obesity,” Metabolism: Clinical and Experimental, vol. 60, no. 2, pp. 243–249, 2011. View at Publisher · View at Google Scholar · View at Scopus
  15. S. S. Ionova-Martin, J. M. Wade, S. Tang et al., “Changes in cortical bone response to high-fat diet from adolescence to adulthood in mice,” Osteoporosis International, vol. 22, no. 8, pp. 2283–2293, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. F. Parhami, Y. Tintut, W. G. Beamer, N. Gharavi, W. Goodman, and L. L. Demer, “Atherogenic high-fat diet reduces bone mineralization in mice,” Journal of Bone and Mineral Research, vol. 16, no. 1, pp. 182–188, 2001. View at Publisher · View at Google Scholar · View at Scopus
  17. G. V. Halade, M. M. Rahman, P. J. Williams, and G. Fernandes, “High fat diet-induced animal model of age-associated obesity and osteoporosis,” The Journal of Nutritional Biochemistry, vol. 21, no. 12, pp. 1162–1169, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. C. M. Steppan, D. T. Crawford, K. L. Chidsey-Frink, H. Ke, and A. G. Swick, “Leptin is a potent stimulator of bone growth in ob/ob mice,” Regulatory Peptides, vol. 92, no. 1–3, pp. 73–78, 2000. View at Publisher · View at Google Scholar · View at Scopus
  19. P. Ducy, M. Amling, S. Takeda et al., “Leptin inhibits bone formation through a hypothalamic relay: a central control of bone mass,” Cell, vol. 100, no. 2, pp. 197–207, 2000. View at Publisher · View at Google Scholar · View at Scopus
  20. N. K. Lee, H. Sowa, E. Hinoi et al., “Endocrine regulation of energy metabolism by the skeleton,” Cell, vol. 130, no. 3, pp. 456–469, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. X. M. Lu, H. Zhao, and E. H. Wang, “A high-fat diet induces obesity and impairs bone acquisition in young male mice,” Molecular Medicine Reports, vol. 7, no. 4, pp. 1203–1208, 2013. View at Publisher · View at Google Scholar · View at Scopus
  22. K. Mekada, K. Abe, A. Murakami et al., “Genetic differences among C57BL/6 substrains,” Experimental Animals, vol. 58, no. 2, pp. 141–149, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. H. C. Freeman, A. Hugill, N. T. Dear, F. M. Ashcroft, and R. D. Cox, “Deletion of nicotinamide nucleotide transhydrogenase: a new quantitive trait locus accounting for glucose intolerance in C57BL/6J mice,” Diabetes, vol. 55, no. 7, pp. 2153–2156, 2006. View at Publisher · View at Google Scholar · View at Scopus
  24. T.-T. Huang, M. Naeemuddin, S. Elchuri et al., “Genetic modifiers of the phenotype of mice deficient in mitochondrial superoxide dismutase,” Human Molecular Genetics, vol. 15, no. 7, pp. 1187–1194, 2006. View at Publisher · View at Google Scholar · View at Scopus
  25. B. Ahrén and G. Pacini, “Insufficient islet compensation to insulin resistance vs. reduced glucose effectiveness in glucose-intolerant mice,” American Journal of Physiology: Endocrinology and Metabolism, vol. 283, no. 4, pp. E738–E744, 2002. View at Publisher · View at Google Scholar · View at Scopus
  26. M. Poggi, D. Bastelica, P. Gual et al., “C3H/HeJ mice carrying a toll-like receptor 4 mutation are protected against the development of insulin resistance in white adipose tissue in response to a high-fat diet,” Diabetologia, vol. 50, no. 6, pp. 1267–1276, 2007. View at Publisher · View at Google Scholar · View at Scopus
  27. D. M. L. Tsukumo, M. A. Carvalho-Filho, J. B. C. Carvalheira et al., “Loss-of-function mutation in toll-like receptor 4 prevents diet-induced obesity and insulin resistance,” Diabetes, vol. 56, no. 8, pp. 1986–1998, 2007. View at Publisher · View at Google Scholar · View at Scopus
  28. H. Nakamura, Y. Fukusaki, A. Yoshimura et al., “Lack of Toll-like receptor 4 decreases lipopolysaccharide-induced bone resorption in C3H/HeJ mice in vivo,” Oral Microbiology and Immunology, vol. 23, no. 3, pp. 190–195, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. M. Rauner, W. Sipos, and P. Pietschmann, “Osteoimmunology,” International Archives of Allergy and Immunology, vol. 143, no. 1, pp. 31–48, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. K. Bandow, A. Maeda, K. Kakimoto et al., “Molecular mechanisms of the inhibitory effect of lipopolysaccharide (LPS) on osteoblast differentiation,” Biochemical and Biophysical Research Communications, vol. 402, no. 4, pp. 755–761, 2010. View at Publisher · View at Google Scholar · View at Scopus
  31. K. Gunaratnam, C. Vidal, R. Boadle, C. Thekkedam, and G. Duque, “Mechanisms of palmitate-induced cell death in human osteoblasts,” Biology Open, vol. 2, no. 12, pp. 1382–1389, 2013. View at Publisher · View at Google Scholar
  32. E. A. Droke, K. A. Hager, M. R. Lerner et al., “Soy isoflavones avert chronic inflammation-induced bone loss and vascular disease,” Journal of Inflammation, vol. 4, article 17, 2007. View at Publisher · View at Google Scholar · View at Scopus
  33. M. R. Hill, K. D. Denson, S. Y. Bu et al., “LPS-mediated chronic inflammation increases circulating RANKL coincident with bone loss in C57BL/6 mice,” Journal of Bone and Mineral Research, abstract S410, 2006. View at Google Scholar
  34. S.-R. Oh, O.-J. Sul, Y.-Y. Kim et al., “Saturated fatty acids enhance osteoclast survival,” Journal of Lipid Research, vol. 51, no. 5, pp. 892–899, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. R. S. Surwit, M. N. Feinglos, J. Rodin et al., “Differential effects of fat and sucrose on the development of obesity and diabetes in C57BL/6J and A/J mice,” Metabolism, vol. 44, no. 5, pp. 645–651, 1995. View at Publisher · View at Google Scholar · View at Scopus
  36. E. Rendina, Y. F. Lim, D. Marlow et al., “Dietary supplementation with dried plum prevents ovariectomy-induced bone loss while modulating the immune response in C57BL/6J mice,” Journal of Nutritional Biochemistry, vol. 23, no. 1, pp. 60–68, 2012. View at Publisher · View at Google Scholar · View at Scopus
  37. E. Rendina, K. D. Hembree, M. R. Davis et al., “Dried plum's unique capacity to reverse bone loss and alter bone metabolism in postmenopausal osteoporosis model,” PLoS ONE, vol. 8, no. 3, Article ID e60569, 2013. View at Publisher · View at Google Scholar · View at Scopus
  38. K. L. Svenson, R. von Smith, P. A. Magnani et al., “Multiple trait measurements in 43 inbred mouse strains capture the phenotypic diversity characteristic of human populations,” Journal of Applied Physiology, vol. 102, no. 6, pp. 2369–2378, 2007. View at Publisher · View at Google Scholar · View at Scopus
  39. A. A. Toye, J. D. Lippiat, P. Proks et al., “A genetic and physiological study of impaired glucose homeostasis control in C57BL/6J mice,” Diabetologia, vol. 48, no. 4, pp. 675–686, 2005. View at Publisher · View at Google Scholar · View at Scopus
  40. A. Nicholson, P. C. Reifsnyder, R. D. Malcolm et al., “Diet-induced obesity in two C57BL/6 substrains with intact or mutant nicotinamide nucleotide transhydrogenase (Nnt) gene,” Obesity, vol. 18, no. 10, pp. 1902–1905, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. H. Freeman, K. Shimomura, E. Horner, R. D. Cox, and F. M. Ashcroft, “Nicotinamide nucleotide transhydrogenase: a key role in insulin secretion,” Cell Metabolism, vol. 3, no. 1, pp. 35–45, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. E. Riu, T. Ferre, A. Hidalgo et al., “Overexpression of c-myc in the liver prevents obesity and insulin resistance,” The FASEB Journal, vol. 17, no. 12, pp. 1715–1717, 2003. View at Google Scholar · View at Scopus
  43. Q. M. Anstee and R. D. Goldin, “Mouse models in non-alcoholic fatty liver disease and steatohepatitis research,” International Journal of Experimental Pathology, vol. 87, no. 1, pp. 1–16, 2006. View at Publisher · View at Google Scholar · View at Scopus
  44. G. R. Hajer, T. W. van Haeften, and F. L. J. Visseren, “Adipose tissue dysfunction in obesity, diabetes, and vascular diseases,” European Heart Journal, vol. 29, no. 24, pp. 2959–2971, 2008. View at Publisher · View at Google Scholar · View at Scopus
  45. M. Haluzik, C. Colombo, O. Gavrilova et al., “Genetic background (C57BL/6J Versus FVB/N) strongly influences the severity of diabetes and insulin resistance in ob/ob mice,” Endocrinology, vol. 145, no. 7, pp. 3258–3264, 2004. View at Publisher · View at Google Scholar · View at Scopus
  46. S. Kapur, M. Amoui, C. Kesavan et al., “Leptin receptor (Lepr) is a negative modulator of bone mechanosensitivity and genetic variations in Lepr may contribute to the differential osteogenic response to mechanical stimulation in the C57BL/6J and C3H/HeJ pair of mouse strains,” The Journal of Biological Chemistry, vol. 285, no. 48, pp. 37607–37618, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. A. Hamann and S. Matthaei, “Regulation of energy balance by leptin,” Experimental and Clinical Endocrinology & Diabetes, vol. 104, no. 4, pp. 293–300, 1996. View at Publisher · View at Google Scholar · View at Scopus
  48. A. C. Looker, K. M. Flegal, and L. J. Melton III, “Impact of increased overweight on the projected prevalence of osteoporosis in older women,” Osteoporosis International, vol. 18, no. 3, pp. 307–313, 2007. View at Publisher · View at Google Scholar · View at Scopus
  49. S. J. Kuruvilla, S. D. Fox, D. M. Cullen, and M. P. Akhter, “Site specific bone adaptation response to mechanical loading,” Journal of Musculoskeletal Neuronal Interactions, vol. 8, no. 1, pp. 71–78, 2008. View at Google Scholar · View at Scopus
  50. T. Yamaguchi, I. Kanazawa, M. Yamamoto et al., “Associations between components of the metabolic syndrome versus bone mineral density and vertebral fractures in patients with type 2 diabetes,” Bone, vol. 45, no. 2, pp. 174–179, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. J. N. Farr, M. T. Drake, S. Amin, L. J. Melton III, L. K. McCready, and S. Khosla, “In vivo assessment of bone quality in postmenopausal women with type 2 diabetes,” Journal of Bone and Mineral Research, vol. 29, no. 4, pp. 787–795, 2014. View at Publisher · View at Google Scholar · View at Scopus
  52. T. L. Clemens and G. Karsenty, “The osteoblast: an insulin target cell controlling glucose homeostasis,” Journal of Bone and Mineral Research, vol. 26, no. 4, pp. 677–680, 2011. View at Publisher · View at Google Scholar · View at Scopus
  53. M. Ferron, E. Hinoi, G. Karsenty, and P. Ducy, “Osteocalcin differentially regulates β cell and adipocyte gene expression and affects the development of metabolic diseases in wild-type mice,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 13, pp. 5266–5270, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. E. Hinoi, N. Gao, D. Y. Jung et al., “An osteoblast-dependent mechanism contributes to the leptin regulation of insulin secretion,” Annals of the New York Academy of Sciences, vol. 1173, supplement 1, pp. E20–E30, 2009. View at Publisher · View at Google Scholar · View at Scopus
  55. M. Ferron, J. Wei, T. Yoshizawa et al., “Insulin signaling in osteoblasts integrates bone remodeling and energy metabolism,” Cell, vol. 142, no. 2, pp. 296–308, 2010. View at Publisher · View at Google Scholar · View at Scopus
  56. M. Ferron, M. D. McKee, R. L. Levine, P. Ducy, and G. Karsenty, “Intermittent injections of osteocalcin improve glucose metabolism and prevent type 2 diabetes in mice,” Bone, vol. 50, no. 2, pp. 568–575, 2012. View at Publisher · View at Google Scholar · View at Scopus
  57. M.-T. Rached, A. Kode, B. C. Silva et al., “FoxO1 expression in osteoblasts regulates glucose homeostasis through regulation of osteocalcin in mice,” Journal of Clinical Investigation, vol. 120, no. 1, pp. 357–368, 2010. View at Publisher · View at Google Scholar · View at Scopus
  58. K. I. Larsen, M. Falany, W. Wang, and J. P. Williams, “Glucose is a key metabolic regulator of osteoclasts; glucose stimulated increases in ATP/ADP ratio and calmodulin kinase II activity,” Biochemistry and Cell Biology, vol. 83, no. 5, pp. 667–673, 2005. View at Publisher · View at Google Scholar · View at Scopus
  59. M. Haraikawa, N. Tsugawa, N. Sogabe et al., “Effects of gamma-glutamyl carboxylase gene polymorphism (R325Q) on the association between dietary vitamin K intake and gamma-carboxylation of osteocalcin in young adults,” Asia Pacific Journal of Clinical Nutrition, vol. 22, no. 4, pp. 646–654, 2013. View at Publisher · View at Google Scholar · View at Scopus