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The Effects of High Fat, Low Carbohydrate and Low Fat, High Carbohydrate Diets on Tumor Necrosis Factor Superfamily Proteins and Proinflammatory Cytokines in C57Bl/6 Mice

Abstract

There has been considerable inconsistency regarding the potential relationship between dyslipidemia and bone metabolism. The inflammatory stimulation through the receptor activator of the nuclear factor kappa-B ligand (RANKL)/ receptor activator of the nuclear factor kappa-B (RANK)/ osteoprotegerin (OPG) pathway could be the infrastructural mechanism for hypercholesterolemia-induced bone loss.
In this study, we investigated the effect of dyslipidemia on RANKL and OPG  alongside with pro-inflammatory cytokines. Thirty male C57Bl/6 mice (4 weeks old) were randomized to two purified diet groups (15 animals in each group), high fat, low carbohydrate diet (HFLCD) and its matched low fat, high carbohydrate diet (LFHCD). After 12 weeks of feeding in standard situations, the plasma concentration of lipid profile, interleukin (IL)1Beta, IL-6, tumor  necrosis factor-alpha (TNF-α) and RANKL, OPG,  and RANKL: OPG ratio were measured.
In the present study, although the body weight significantly increased during 12 weeks in HFLCD and LFHCD groups, there were no significant differences in food intake, food efficiency ratio and weight gain between the two groups. The LFHCD group had significantly higher median RANKL and RANKL/OPG ratio. There was no significant difference in plasma IL-1β, IL-6 and TNF-α concentration between LFHCD and HFLCD groups.
These unexpected findings from  LFHCD,  that  seem to  be as a result of its higher carbohydrate proportion  in comparison to HFLCD,  implicate dietary carbohydrate rather than dietary fat as a more significant nutritional factor contributing to change in RANKL level and RANKL: OPG ratio.

1. Arnold M, Stas P, Kummermehr J, Schultz-Hector S, Trott KR. Radiation-induced impairment of bone healing in the rat femur: effects of radiation dose, sequence and interval between surgery and irradiation. Radiother Oncol 1998; 48(3):259-65.

2. Kwan Tat S, Padrines M, Theoleyre S, Heymann D, Fortun Y. IL-6, RANKL, TNF-alpha/IL-1: interrelations in bone resorption pathophysiology. Cytokine Growth Factor Rev 2004; 15(1):49-60.

3. Walsh MC, Kim N, Kadono Y, Rho J, Lee SY, Lorenzo J, et al. Osteoimmunology: interplay between the immune system and bone metabolism. Annu Rev Immunol 2006;24:33-6.

4. Jones DH, Glimcher LH, Aliprantis AO.Osteoimmunology at the nexus of arthritis, osteoporosis, cancer and infection. J Clin Invest 2011; 121(7):2534-42.

5. Sirjani M, Pourpak Z. Osteoimmunology and Nutritional Science. Iran J Allergy Asthma Immunol 2013;12(3):290-1.

6. Takayanagi H. Osteoimmunology: shared mechanisms and crosstalk between the immune and bone systems. Nat Rev Immunol 2007; 7(4):292-304.

7. Graham LS, Parhami F, Tintut Y, Kitchen CM, Demer LL, Effros RB. Oxidized lipids enhance RANKL production by T lymphocytes: implications for lipid- induced bone loss. Clin Immunol 2009; 133(2):265-75.

8. Wong BR, Rho J, Arron JR, Robinson E, Orlinick J, Chao M, et al. TRANCE is a novel ligand of the tumor necrosis factor receptor family that activates c-Jun N- terminal kinase in T cells. J Biol Chem 1997;272(40):25190-4.

9. Yasuda H, Sima N, Nakagawa N, Yamaguchi K, Kinosaki M, Mochizuki S, et al. Osteoclast differntiation factor is a ligand for osteoprotegerin/osteoclastogenesis- inhibitory factor and is identical to TRANCE/RANKL. Proc Natl Acad Sci 1998; 95(7):3597-602.

10. Lacey DL, Timms E, Tan HL, Kelley MJ, Dunstan CR, Burgess T, et al. Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell 1998; 93(2):165-76.

11. Wong BR, Josien R, Choi Y. TRANCE is a TNF family member that regulates dendritic cell and osteoclast function. J Leukoc Biol 1999; 65(6):715-24.

12. Theoleyre S, Wittrant Y, Tat SK, Fortun Y, Redini F, Heymann D. The molecular triad OPG/RANK/RANKL: involvement in the orchestration of pathophysiological bone remodeling. Cytokine Growth Factor Rev 2004;15(6):457-75.

13. Boyle WJ, Simonet WS, Lacey DL. Osteoclast differentiation and activation. Nature 2003;423(6937):337-42.

14. Suda T, Takahashi N, Udagawa N, Jimi E, Gillespie MT, Martin TJ. Modulation of osteoclast differentiation and function by the new members of the tumor necrosis factor receptor and ligand families. Endocr Rev 1999; 20(3):345-57.

15. Shils ME, Shike M, Ross AC, Caballero B, Cousins RJ.MODERN NUTRITION IN HEALTH AND DISEASE. 2006.

16. Cui LH, Shin MH, Chung EK, Lee YH, Kweon SS, Park KS, et al. Association between bone mineral densities and serum lipid profiles of pre- and post-menopausal rural women in South Korea. Osteoporosis international : a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA. 2005;16(12):1975-81.

17. Orozco P. Atherogenic lipid profile and elevated lipoprotein (a) are associated with lower bone mineral density in early postmenopausal overweight women. Eur J Epidemiol 2004; 19(12):1105-12.

18. Tanko LB, Bagger YZ, Nielsen SB, Christiansen C. Does serum cholesterol contribute to vertebral bone loss in postmenopausal women? Bone 2003; 32(1):8-14.

19. Wu LY, Yang TC, Kuo SW, Hsiao CF, Hung YJ, Hsieh CH, et al. Correlation between bone mineral density and plasma lipids in Taiwan. Endocr Res 2003; 29(3):317-25.

20. Yang RL, Li W, Shi YH, Le GW. Lipoic acid prevents high-fat diet-induced dyslipidemia and oxidative stress: a microarray analysis. Nutrition 2008; 24(6):582-8.

21. Solomon DH, Avorn J, Canning CF, Wang PS. Lipid levels and bone mineral density. Am J Med 2005;118(12):1414.

22. Warden CH, Fisler JS. Comparisons of diets used in animal models of high-fat feeding. Cell Metab 2008;7(4):277.

23. Ricci MR. Laboratory Animal Diets: A Critical Part of Your In Vivo Research 2008. Available from: http://www.alnmag.com/articles?pid=120.

24. Halloran BP, Ferguson VL, Simske SJ, Burghardt A, Venton LL, Majumdar S. Changes in bone structure and mass with advancing age in the male C57BL/6J mouse. J Bone Miner Res 2002; 17(6):1044-50.

25. Graham LS, Tintut Y, Parhami F, Kitchen CM, Ivanov Y, Tetradis S, et al. Bone density and hyperlipidemia: the T- lymphocyte connection. J Bone Miner Res 2010;25(11):2460-9.

26. Cao JJ, Gregoire BR, Gao H. High-fat diet decreases cancellous bone mass but has no effect on cortical bone mass in the tibia in mice. Bone 2009; 44(6):1097-104.

27. Xiao Y, Cui J, Li YX, Shi YH, Wang B, Le GW, et al.Dyslipidemic high-fat diet affects adversely bone metabolism in mice associated with impaired antioxidant capacity. Nutrition 2011; 27(2):214-20.

28. Ishida H, Uesugi T, Hirai K, Toda T, Nukaya H, Yokotsuka K, et al. Preventive effects of the plant isoflavones, daidzin and genistin, on bone loss in ovariectomized rats fed a calcium-deficient diet. Biol Pharm Bull 1998; 21(1):62-6.

29. Forsythe CE, Phinney SD, Fernandez ML, Quann EE, Wood RJ, Bibus DM, et al. Comparison of low fat and low carbohydrate diets on circulating fatty acid composition and markers of inflammation. Lipids 2008;43(1):65-77.

30. Volek JS, Phinney SD, Forsythe CE, Quann EE, Wood RJ, Puglisi MJ, et al. Carbohydrate restriction has a more favorable impact on the metabolic syndrome than a low fat diet. Lipids 2009; 44(4):297-309.

31. Lee JY, Hwang DH. The modulation of inflammatory gene expression by lipids: mediation through Toll-like receptors. Mol Cells 2006; 21(2):174-85.

32. Ikemoto S, Takahashi M, Tsunoda N, Maruyama K, Itakura H, Kawanaka K, et al. Cholate inhibits high-fat diet-induced hyperglycemia and obesity with acyl-CoA synthetase mRNA decrease. Am J Physiol 1997; 273(1 Pt1):E37-45.

33. Watanabe M, Houten SM, Mataki C, Christoffolete MA, Kim BW, Sato H, et al. Bile acids induce energy expenditure by promoting intracellular thyroid hormone activation. Nature 2006; 439(7075):484-9.

34. Xiao Y, Cui J, Li Y-X, Shi Y-H, Le G-W. Expression of Genes Associated with Bone Resorption is Increased and Bone Formation is Decreased in Mice Fed a High-Fat Diet. Lipids 2010; 45(4):345-55.

35. Ding T, Yao Y, Pratico D. Increase in peripheral oxidative stress during hypercholesterolemia is not reflected in the central nervous system: evidence from two mouse models. Neurochem Int 2005; 46(6):435-9.

36. Oh SR, Sul OJ, Kim YY, Kim HJ, Yu R, Suh JH, et al.Saturated fatty acids enhance osteoclast survival. J Lipid Res 2010; 51(5):892-9.

37. Cao JJ. Effects of obesity on bone metabolism. J Orthop Surg Res 2011; 6:30.

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IssueVol 13, No 4 (2014) QRcode
SectionArticles
Keywords
Bone Cytokines Diet Dyslipidemia Fat RANKL

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How to Cite
1.
Sirjani M, Taleban FA, Hekmatdoost A, Amiri Z, Pellizzon M, Hedayati M, Bidad K, Shokouhi Shoormasti R, Pourpak Z. The Effects of High Fat, Low Carbohydrate and Low Fat, High Carbohydrate Diets on Tumor Necrosis Factor Superfamily Proteins and Proinflammatory Cytokines in C57Bl/6 Mice. Iran J Allergy Asthma Immunol. 1;13(4):247-255.