Diet and gene interactions influence the skeletal response to polyunsaturated fatty acids

Bone

Volumn 68, Issue , 2014, Pages 100-107

  Bonnet, Nicolas ^a   Somm, Emmanuel ^b,c   Rosen, Clifford J ^d  

^a GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^b LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^c UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^d Maine Medical Center Research Institute   (United States)

Author keywords

Aging; Bone microCT; Bone fat interactions; Genetic animal models; Omega 3s

Indexed keywords

FISH OIL; LEPTIN; OMEGA 3 FATTY ACID; OMEGA 6 FATTY ACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; POLYUNSATURATED FATTY ACID; SAFFLOWER OIL; BIOLOGICAL MARKER; ADIPONECTIN; FAS ANTIGEN; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 10; INTERLEUKIN 6; OSTEOCALCIN; SOMATOMEDIN B; TUMOR NECROSIS FACTOR ALPHA;

ADIPOGENESIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACKCROSSING; BODY COMPOSITION; BODY FAT; BODY WEIGHT; BONE DENSITY; BONE MARROW; BONE METABOLISM; BONE STRUCTURE; C57BL 6 MOUSE; CHROMOSOME 6; CONGENIC STRAIN; CONTROLLED STUDY; CORTICAL THICKNESS (BONE); DIET; DNA POLYMORPHISM; ENERGY; FEMALE; FEMUR; FORCE; GAIN OF FUNCTION MUTATION; GENE INTERACTION; GENOTYPE; INFLAMMATION; MOUSE; NONHUMAN; OBESITY; OSTEOLYSIS; TRABECULAR BONE; VERTEBRA; WEIGHT GAIN; ANATOMY AND HISTOLOGY; ANIMAL; BIOMECHANICS; BONE; BROWN ADIPOSE TISSUE; C3H MOUSE; C57BL MOUSE; CELL COUNT; CYTOLOGY; DIET SUPPLEMENTATION; DRUG EFFECTS; GENE EXPRESSION REGULATION; METABOLISM; ORGAN SIZE; OSTEOCLAST; PHYSIOLOGY; SPINE; TIBIA; WHITE ADIPOSE TISSUE; AGING; BLOOD SAMPLING; BONE DEVELOPMENT; BONE MASS; FAT MASS; FISH; GENE EXPRESSION; INSULIN SENSITIVITY; LEAN BODY WEIGHT; MICRO-COMPUTED TOMOGRAPHY; MORPHOMETRICS; OSTEOPOROSIS; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RNA EXTRACTION; SAFFLOWER;

ADIPOSE TISSUE, BROWN; ADIPOSE TISSUE, WHITE; ADIPOSITY; ANIMALS; BIOMARKERS; BIOMECHANICAL PHENOMENA; BODY COMPOSITION; BONE AND BONES; BONE DENSITY; BONE MARROW; CELL COUNT; DIET; DIETARY SUPPLEMENTS; FATTY ACIDS, OMEGA-3; FATTY ACIDS, OMEGA-6; FEMALE; FEMUR; FISH OILS; GENE EXPRESSION REGULATION; MICE, INBRED C3H; MICE, INBRED C57BL; ORGAN SIZE; OSTEOCLASTS; SPINE; TIBIA;

EID: 84906732178     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2014.07.024     Document Type: Article

References (52)

1. Rosen C.J., Bouxsein M.L. Mechanisms of disease: is osteoporosis the obesity of bone?. Nat Clin Pract Rheumatol 2006, 2(1):35-43.
2. Abellan van Kan G., Gambassi G., de Groot L.C., Andrieu S., Cederholm T., André E., et al. Nutrition and aging, the Carla Workshop. J Nutr Health Aging 2008, 12(6):355-364.
3. Ohnell O., Gullberg B., Allander E., Kanis J.A., MEDOS Study Group The apparent incidence of hip fracture in Europe: a study of national register sources. Osteoporos Int 1992, 2(6):298-302.
4. Kannus P., Parkkari J., Sievänen H., Heinonen A., Vuori I., Järvinen M. Epidemiology of hip fractures. Bone 1996, 18(1 Suppl):57S-63S.
5. Willett W.C., Sacks F., Trichopoulou A., Drescher G., Ferro-Luzzi A., Helsing E., et al. Mediterranean diet pyramid: a cultural model for healthy eating. Am J Clin Nutr 1995, 61(6 Suppl):1402S-1406S.
6. Kontogianni M.D., Melistas L., Yannakoulia M., Malagaris I., Panagiotakos D.B., Yiannakouris N. Association between dietary patterns and indices of bone mass in a sample of Mediterranean women. Nutrition 2009, 25(2):165-171.
7. Puel C., Coxam V., Davicco M.J. Mediterranean diet and osteoporosis prevention. Med Sci 2007, 23(8-9):756-760.
8. Farina E.K., Kiel D.P., Roubenoff R., Schaefer E.J., Cupples L.A., Tucker K.L. Protective effects of fish intake and interactive effects of long-chain polyunsaturated fatty acid intakes on hip bone mineral density in older adults: the Framingham Osteoporosis Study. Am J Clin Nutr 2011, 93(5):1142-1151.
9. 2 Study. Am J Clin Nutr 2007, 85(3):803-807.
10. Nawata K., Yamauchi M., Takaoka S., Yamaguchi T., Sugimoto T. Association of n-3 polyunsaturated fatty acid intake with bone mineral density in postmenopausal women. Calcif Tissue Int 2013, 93(2):147-154.
11. Farina E.K., Kiel D.P., Roubenoff R., Schaefer E.J., Cupples L.A., Tucker K.L. Dietary intakes of arachidonic acid and alpha-linolenic acid are associated with reduced risk of hip fracture in older adults. J Nutr 2011, 141(6):1146-1153.
12. Salari Sharif P., Asalforoush M., Ameri F., Larijani B., Abdollahi M. The effect of n-3 fatty acids on bone biomarkers in Iranian postmenopausal osteoporotic women: a randomized clinical trial. Age 2010, 32(2):179-186.
13. Brownbill R.A., Ilich J.Z. Lipid profile and bone paradox: higher serum lipids are associated with higher bone mineral density in postmenopausal women. J Womens Health 2006, 15(3):261-270.
14. Virtanen J.K., Mozaffarian D., Cauley J.A., Mukamal K.J., Robbins J., Siscovick D.S. Fish consumption, bone mineral density, and risk of hip fracture among older adults: the cardiovascular health study. J Bone Miner Res 2010, 25(9):1972-1979.
15. Orchard T.S., Cauley J.A., Frank G.C., Neuhouser M.L., Robinson J.G., Snetselaar L., et al. Fatty acid consumption and risk of fracture in the Women's Health Initiative. Am J Clin Nutr 2010, 92(6):1452-1460.
16. Ralston S.H. Genetics of osteoporosis. Proc Nutr Soc 2007, 66(2):158-165.
17. Ackert-Bicknell C.L., Salisbury J.L., Horowitz M., DeMambro V.E., Horton L.G., Shultz K.L., et al. A chromosomal inversion within a quantitative trait locus has a major effect on adipogenesis and osteoblastogenesis. Ann N Y Acad Sci 2007, 1116:291-305.
18. Ackert-Bicknell C.L., Demissie S., Marín de Evsikova C., Hsu Y.H., DeMambro V.E., Karasik D., et al. PPARG by dietary fat interaction influences bone mass in mice and humans. J Bone Miner Res 2008, 23(9):1398-1408.
19. Lecka-Czernik B., Ackert-Bicknell C., Adamo M.L., Marmolejos V., Churchill G.A., Shockley K.R., et al. Activation of peroxisome proliferator-activated receptor gamma (PPARgamma) by rosiglitazone suppresses components of the insulin-like growth factor regulatory system in vitro and in vivo. Endocrinology 2007, 148(2):903-911.
20. Lecka-Czernik B., Rosen C.J., Kawai M. Skeletal aging and the adipocyte program: new insights from an "old" molecule. Cell Cycle 2010, 9(18):3648-3654.
21. Harsløf T., Tofteng C.L., Husted L.B., Nyegaard M., Børglum A., Carstens M., et al. Polymorphisms of the peroxisome proliferator-activated receptor γ (PPARγ) gene are associated with osteoporosis. Osteoporos Int Oct. 2011, 22(10):2655-2666.
22. Wan Y., Chong L.W., Evans R.M. PPAR-gamma regulates osteoclastogenesis in mice. Nat Med 2007, 13:1496-1503.
23. Cho S.W., Yang J.Y., Her S.J., Choi H.J., Jung J.Y., Sun H.J., et al. Osteoblast-targeted overexpression of PPARγ inhibited bone mass gain in male mice and accelerated ovariectomy-induced bone loss in female mice. J Bone Miner Res 2011, 26(8):1939-1952.
24. Mieczkowska A., Baslé M.F., Chappard D., Mabilleau G. Thiazolidinediones induce osteocyte apoptosis by a g protein-coupled receptor 40-dependent mechanism. J Biol Chem 2012, 287(28):23517-23526.
25. Magee P., Pearson S., Whittingham-Dowd J., Allen J. PPARγ as a molecular target of EPA anti-inflammatory activity during TNF-α-impaired skeletal muscle cell differentiation. J Nutr Biochem 2012, 23(11):1440-1448.
26. Flachs P., Rossmeisl M., Bryhn M., Kopecky J. Cellular and molecular effects of n-3 polyunsaturated fatty acids on adipose tissue biology and metabolism. Clin Sci (Lond) 2009, 116(1):1-16.
27. Lengqvist J., Mata De Urquiza A., Bergman A.C., Willson T.M., Sjövall J., Perlmann T., et al. Polyunsaturated fatty acids including docosahexaenoic and arachidonic acid bind to the retinoid×receptor alpha ligand-binding domain. Mol Cell Proteomics 2004, 3(7):692-703.
28. Sun D., Krishnan A., Zaman K., Lawrence R., Bhattacharya A., Fernandes G. Dietary n-3 fatty acids decrease osteoclastogenesis and loss of bone mass in ovariectomized mice. J Bone Miner Res 2003, 18(7):1206-1216.
29. Halade G.V., Rahman M.M., Williams P.J., Fernandes G. Combination of conjugated linoleic acid with fish oil prevents age-associated bone marrow adiposity in C57Bl/6J mice. J Nutr Biochem 2011, 22(5):459-469.
30. Bonnet N., Ferrari S.L. Effects of long-term supplementation with omega-3 fatty acids on longitudinal changes in bone mass and microstructure in mice. J Nutr Biochem 2011, 22(7):665-672.
31. Iida-Klein A., Lu S.S., Yokoyama K., Dempster D.W., Nieves J.W., Lindsay R. Precision, accuracy, and reproducibility of dual X-ray absorptiometry measurements in mice in vivo. J Clin Densitom 2003, 6(1):25-33.
32. Waarsing J.H., Day J.S., van der Linden J.C., Ederveen A.G., Spanjers C., De Clerck N., et al. Detecting and tracking local changes in the tibiae of individual rats: a novel method to analyse longitudinal in vivo micro-CT data. Bone 2004, 34:163-169.
33. Waarsing J.H., Day J.S., Weinans H. An automatic algorithm to segment 3D microCT scans of bone. The IXth Congress of the International Society of Bone Morphometry 2002, Edinburgh, UK.
34. Bouxsein M.L., Boyd S.K., Christiansen B.A., Guldberg R.E., Jepsen K.J., Müller R. Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J Bone Miner Res 2010, 25(7):1468-1486.
35. Clinthorne J.F., Adams D.J., Fenton J.I., Ritz B.W., Gardner E.M. Short-term re-feeding of previously energy-restricted C57BL/6 male mice restores body weight and body fat and attenuates the decline in natural killer cell function after primary influenza infection. J Nutr 2010, 140:1495-1501.
36. Bonnet N., Standley K.N., Bianchi E.N., Stadelmann V., Foti M., Conway S.J., et al. The matricellular protein periostin is required for sclerostin inhibition and the anabolic response to mechanical loading and physical activity. J Biol Chem 2009, 284(51):35939-35950.
37. Turner C.H., Burr D.B. Basic biomechanical measurements of bone: a tutorial. Bone 1993, 14(4):595-608.
38. Edwards I.J., O'Flaherty J.T. Omega-3 fatty acids and PPARgamma in cancer. PPAR Res 2008, 358052.
39. Deckelbaum R.J., Worgall T.S., Seo T. n-3 fatty acids and gene expression. Am J Clin Nutr 2006, 83(6 Suppl):1520S-1525S.
40. Rosen C.J., Ackert-Bicknell C.L., Adamo M.L., Shultz K.L., Rubin J., Donahue L.R., et al. Congenic mice with low serum IGF-I have increased body fat, reduced bone mineral density, and an altered osteoblast differentiation program. Bone 2004, 35(5):1046-1058.
41. Bouxsein M.L., Rosen C.J., Turner C.H., Ackert C.L., Shultz K.L., Donahue L.R., et al. Generation of a new congenic mouse strain to test the relationships among serum insulin-like growth factor I, bone mineral density, and skeletal morphology in vivo. J Bone Miner Res 2002, 17(4):570-579.
42. Hamrick M.W., Pennington C., Newton D., Xie D., Isales C. Leptin deficiency produces contrasting phenotypes in bones of the limb and spine. Bone 2004, 34(3):376-383.
43. Motyl K.J., Bishop K.A., DeMambro V.E., Bornstein S.A., Le P., Kawai M., et al. Altered thermogenesis and impaired bone remodeling in Misty mice. J Bone Miner Res 2013, 28(9):1885-1897.
44. Flachs P., Rossmeisl M., Bryhn M., Kopecky J. Cellular and molecular effects of n-3 polyunsaturated fatty acids on adipose tissue biology and metabolism. Clin Sci 2009, 116(1):1-16.
45. Bonnet N., Rizzoli R., Ferarri S.L. Effects of a diet enriched in omega-3 on bone remodeling and bone structure. J Nutrigenet Nutrigenomics 2008, 1(FP35):299.
46. Ducy P., Amling M., Takeda S., Priemel M., Schilling A.F., Beil F.T., et al. Leptin inhibits bone formation through a hypothalamic relay: a central control of bone mass. Cell 2000, 100(2):197-207.
47. Elefteriou F., Ahn J.D., Takeda S., Starbuck M., Yang X., Liu X., et al. Leptin regulation of bone resorption by the sympathetic nervous system and CART. Nature 2005, 434(7032):514-520.
48. Kopecky J., Rossmeisl M., Flachs P., Kuda O., Brauner P., Jilkova Z., et al. n-3 PUFA: bioavailability and modulation of adipose tissue function. Proc Nutr Soc 2009, 68(4):361-369.
49. Golub N., Geba D., Mousa S.A., Williams G., Block R.C. Greasing the wheels of managing overweight and obesity with omega-3 fatty acids. Med Hypotheses 2011, 77(6):1114-1120.
50. Magee P., Pearson S., Whittingham-Dowd J., Allen J. PPARγ as a molecular target of EPA anti-inflammatory activity during TNF-α-impaired skeletal muscle cell differentiation. J Nutr Biochem 2012, 23(11):1440-1448.
51. Le P., Kawai M., Bornstein S., DeMambro V.E., Horowitz M.C., Rosen C.J. A high-fat diet induces bone loss in mice lacking the Alox5 gene. Endocrinology 2012, 153(1):6-16.
52. Kelly O.J., Gilman J.C., Kim Y., Ilich J.Z. Long-chain polyunsaturated fatty acids may mutually benefit both obesity and osteoporosis. Nutr Res 2013, 33(7):521-533.