High bone mass in adult mice with diet-induced obesity results from a combination of initial increase in bone mass followed by attenuation in bone formation; implications for high bone mass and decreased bone quality in obesity

Molecular and Cellular Endocrinology

Volumn 410, Issue , 2015, Pages 35-41

  Lecka Czernik, B ^a,b   Stechschulte, L A ^a,b   Czernik, P J ^a   Dowling, A R ^a  

^a MEDICAL COLLEGE OF OHIO   (United States)

^b UNIVERSITY OF TOLEDO   (United States)

Author keywords

Bone formation; Bone mass; Diet induced obesity; Energy metabolism; High fat diet; Obesity

Indexed keywords

ADIPONECTIN; DIO2 PROTEIN; FATTY ACID BINDING PROTEIN 4; MARKER; SOMATOMEDIN BINDING PROTEIN 2; TRANSCRIPTION FACTOR AP 2; TRANSCRIPTION FACTOR FOXC2; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; CYTOKINE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE DENSITY; BONE MASS; BONE STRENGTH; BONE TURNOVER; CONTROLLED STUDY; CORTICAL THICKNESS (BONE); CYTOKINE PRODUCTION; DIET INDUCED OBESITY; ENERGY METABOLISM; GLUCOSE INTOLERANCE; LIPID DIET; MALE; MECHANICAL STRESS; MOUSE; NONHUMAN; OSSIFICATION; PRIORITY JOURNAL; WHITE ADIPOSE TISSUE; ADVERSE EFFECTS; ANIMAL; BLOOD; BODY WEIGHT; BONE DEVELOPMENT; CHEMICALLY INDUCED; COMPLICATION; DISEASE MODEL; METABOLISM; OBESITY; PATHOPHYSIOLOGY;

ADIPOSE TISSUE, WHITE; ANIMALS; BIOMARKERS; BODY WEIGHT; BONE DENSITY; CYTOKINES; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; GLUCOSE INTOLERANCE; MALE; MICE; OBESITY; OSTEOGENESIS;

EID: 84930090500     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2015.01.001     Document Type: Article

References (37)

1. Aguirre L., Napoli N., Waters D., Qualls C., Villareal D.T., Armamento-Villareal R. Increasing adiposity is associated with higher adipokine levels and lower bone mineral density in obese older adults. J. Clin. Endocrinol. Metab 2014, 99:3290-3297.
2. Bonnet N., Somm E., Rosen C.J. Diet and gene interactions influence the skeletal response to polyunsaturated fatty acids. Bone 2014, 68:100-107.
3. Bouxsein M.L., Boyd S.K., Christiansen B.A., Guldberg R.E., Jepsen K.J., Muller R. Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J. Bone Miner. Res 2010, 25:1468-1486.
4. Brown M.L., Yukata K., Farnsworth C.W., Chen D.G., Awad H., Hilton M.J., et al. Delayed fracture healing and increased callus adiposity in a C57BL/6J murine model of obesity-associated type 2 diabetes mellitus. PLoS ONE 2014, 9. e99656.
5. Cao J.J., Gregoire B.R., Gao H. High-fat diet decreases cancellous bone mass but has no effect on cortical bone mass in the tibia in mice. Bone 2009, 44:1097-1104.
6. Cartwright M.J., Tchkonia T., Kirkland J.L. Aging in adipocytes: potential impact of inherent, depot-specific mechanisms. Exp. Gerontol 2007, 42:463-471.
7. Cawsey S., Padwal R., Sharma A.M., Wang X., Li S., Siminoski K. Women with severe obesity and relatively low bone mineral density have increased fracture risk. Osteoporos. Int 2014, Epub ahead of print. 10.1007/s00198-014-2833-z.
8. Compston J.E., Watts N.B., Chapurlat R., Cooper C., Boonen S., Greenspan S., et al. Obesity is not protective against fracture in postmenopausal women: GLOW. Am. J. Med 2011, 124:1043-1050.
9. Garcia-Martin A., Rozas-Moreno P., Reyes-Garcia R., Morales-Santana S., Garcia-Fontana B., Garcia-Salcedo J.A., et al. Circulating levels of sclerostin are increased in patients with type 2 diabetes mellitus. J. Clin. Endocrinol. Metab 2012, 97:234-241.
10. Gennari L., Merlotti D., Valenti R., Ceccarelli E., Ruvio M., Pietrini M.G., et al. Circulating sclerostin levels and bone turnover in type 1 and type 2 diabetes. J. Clin. Endocrinol. Metab 2012, 97:1737-1744.
11. Glatt V., Canalis E., Stadmeyer L., Bouxsein M.L. Age-related changes in trabecular architecture differ in female and male C57BL/6J mice. J. Bone Miner. Res 2007, 22:1197-1207.
12. Gunaratnam K., Vidal C., Gimble J.M., Duque G. Mechanisms of palmitate-induced lipotoxicity in human osteoblasts. Endocrinology 2014, 155:108-116.
13. Kajimura D., Lee H.W., Riley K.J., Arteaga-Solis E., Ferron M., Zhou B., et al. Adiponectin regulates bone mass via opposite central and peripheral mechanisms through FoxO1. Cell Metab 2013, 17:901-915.
14. Krakauer J.C., McKenna M.J., Buderer N.F., Rao D.S., Whitehouse F.W., Parfitt A.M. Bone loss and bone turnover in diabetes. Diabetes 1995, 44:775-782.
15. Krings A., Rahman S., Huang S., Lu Y., Czernik P.J., Lecka-Czernik B. Bone marrow fat has brown adipose tissue characteristics, which are attenuated with aging and diabetes. Bone 2012, 50:546-552.
16. Lecka-Czernik B., Stechschulte L.A. Bone and fat: a relationship of different shades. Arch. Biochem. Biophys 2014, 561:124-129.
17. Lee P., Brychta R.J., Collins M.T., Linderman J., Smith S., Herscovitch P., et al. Cold-activated brown adipose tissue is an independent predictor of higher bone mineral density in women. Osteoporos. Int 2013, 24:1513-1518.
18. Lee P., Linderman J., Smith S., Brychta R.J., Perron R., Idelson C., et al. Fibroblast growth factor 21 (FGF21) and bone: is there a relationship in humans?. Osteoporos. Int 2013, 24:3053-3057.
19. Li Z., Picard F. Modulation of IGFBP2 mRNA expression in white adipose tissue upon aging and obesity. Horm. Metab. Res 2010, 42:787-791.
20. Liu L., Aronson J., Huang S., Lu Y., Czernik P., Rahman S., et al. Rosiglitazone inhibits bone regeneration and causes significant accumulation of fat at sites of new bone formation. Calcif. Tissue Int 2012, 91:139-148.
21. Manavalan J.S., Cremers S., Dempster D.W., Zhou H., Dworakowski E., Kode A., et al. Circulating osteogenic precursor cells in type 2 diabetes mellitus. J. Clin. Endocrinol. Metab 2012, 97:3240-3250.
22. Melton L.J., Leibson C.L., Achenbach S.J., Therneau T.M., Khosla S. Fracture risk in type 2 diabetes: update of a population-based study. J. Bone Miner. Res 2008, 23:1334-1342.
23. Misra M., Klibanski A. Endocrine consequences of anorexia nervosa. Lancet Diabetes Endocrinol 2014, 2:581-592.
24. Naot D., Cornish J. Cytokines and hormones that contribute to the positive association between fat and bone. Front. Endocrinol. (Lausanne) 2014, 5:70.
25. Parfitt A.M., Drezner M.K., Glorieux F.H., Kanis J.A., Malluche H., Meunier P.J., et al. Bone histomorphometry: standardization of nomenclature, symbols, and units. Report of the ASBMR Histomorphometry Nomenclature Committee. J. Bone Miner. Res 1987, 2:595-610.
26. Petit M.A., Paudel M.L., Taylor B.C., Hughes J.M., Strotmeyer E.S., Schwartz A.V., et al. Bone mass and strength in older men with type 2 diabetes: the Osteoporotic Fractures in Men Study. J. Bone Miner. Res 2010, 25:285-291.
27. Premaor M.O., Ensrud K., Lui L., Parker R.A., Cauley J., Hillier T.A., et al. Risk factors for nonvertebral fracture in obese older women. J. Clin. Endocrinol. Metab 2011, 96:2414-2421.
28. Rahman S., Lu Y., Czernik P.J., Rosen C.J., Enerback S., Lecka-Czernik B. Inducible brown adipose tissue, or beige fat, is anabolic for the skeleton. Endocrinology 2013, 154:2687-2701.
29. Reid I.R. Fat and bone. Arch. Biochem. Biophys 2010, 503:20-27.
30. Shen X., Xi G., Maile L.A., Wai C., Rosen C.J., Clemmons D.R. Insulin-like growth factor (IGF) binding protein 2 functions coordinately with receptor protein tyrosine phosphatase beta and the IGF-I receptor to regulate IGF-I-stimulated signaling. Mol. Cell. Biol 2012, 32:4116-4130.
31. Srikanthan P., Crandall C.J., Miller-Martinez D., Seeman T.E., Greendale G.A., Binkley N., et al. Insulin resistance and bone strength: findings from the study of midlife in the United States. J. Bone Miner. Res 2014, 29:796-803.
32. Styner M., Thompson W.R., Galior K., Uzer G., Wu X., Kadari S., et al. Bone marrow fat accumulation accelerated by high fat diet is suppressed by exercise. Bone 2014, 64:39-46.
33. Wei J., Ferron M., Clarke C.J., Hannun Y.A., Jiang H., Blaner W.S., et al. Bone-specific insulin resistance disrupts whole-body glucose homeostasis via decreased osteocalcin activation. J. Clin. Invest 2014, 124:1-13.
34. Wei W., Dutchak P.A., Wang X., Ding X., Wang X., Bookout A.L., et al. Fibroblast growth factor 21 promotes bone loss by potentiating the effects of peroxisome proliferator-activated receptor gamma. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:3143-3148.
35. Wheatcroft S.B., Kearney M.T., Shah A.M., Ezzat V.A., Miell J.R., Modo M., et al. IGF-binding protein-2 protects against the development of obesity and insulin resistance. Diabetes 2007, 56:285-294.
36. Woo D.G., Lee B.Y., Lim D., Kim H.S. Relationship between nutrition factors and osteopenia: effects of experimental diets on immature bone quality. J. Biomech 2009, 42:1102-1107.
37. Yeh L.C., Ford J.J., Lee J.C., Adamo M.L. Palmitate attenuates osteoblast differentiation of fetal rat calvarial cells. Biochem. Biophys. Res. Commun 2014, 450:777-781.