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Low temperature decreases bone mass in mice: Implications for humans
dc.contributor.authorRobbins, Amy
dc.contributor.authorTom, Christina A. T. M. B.
dc.contributor.authorCosman, Miranda N.
dc.contributor.authorMoursi, Cleo
dc.contributor.authorShipp, Lillian
dc.contributor.authorSpencer, Taylor M.
dc.contributor.authorBrash, Timothy
dc.contributor.authorDevlin, Maureen J.
dc.date.accessioned2018-11-20T15:34:42Z
dc.date.available2020-01-06T16:40:59Zen
dc.date.issued2018-11
dc.identifier.citationRobbins, Amy; Tom, Christina A. T. M. B.; Cosman, Miranda N.; Moursi, Cleo; Shipp, Lillian; Spencer, Taylor M.; Brash, Timothy; Devlin, Maureen J. (2018). "Low temperature decreases bone mass in mice: Implications for humans." American Journal of Physical Anthropology 167(3): 557-568.
dc.identifier.issn0002-9483
dc.identifier.issn1096-8644
dc.identifier.urihttps://hdl.handle.net/2027.42/146428
dc.description.abstractObjectivesHumans exhibit significant ecogeographic variation in bone size and shape. However, it is unclear how significantly environmental temperature influences cortical and trabecular bone, making it difficult to recognize adaptation versus acclimatization in past populations. There is some evidence that cold‐induced bone loss results from sympathetic nervous system activation and can be reduced by nonshivering thermogenesis (NST) via uncoupling protein (UCP1) in brown adipose tissue (BAT). Here we test two hypotheses: (1) low temperature induces impaired cortical and trabecular bone acquisition and (2) UCP1, a marker of NST in BAT, increases in proportion to degree of low‐temperature exposure.MethodsWe housed wildtype C57BL/6J male mice in pairs at 26 °C (thermoneutrality), 22 °C (standard), and 20 °C (cool) from 3 weeks to 6 or 12 weeks of age with access to food and water ad libitum (N = 8/group).ResultsCool housed mice ate more but had lower body fat at 20 °C versus 26 °C. Mice at 20 °C had markedly lower distal femur trabecular bone volume fraction, thickness, and connectivity density and lower midshaft femur cortical bone area fraction versus mice at 26 °C (p < .05 for all). UCP1 expression in BAT was inversely related to temperature.DiscussionThese results support the hypothesis that low temperature was detrimental to bone mass acquisition. Nonshivering thermogenesis in brown adipose tissue increased in proportion to low‐temperature exposure but was insufficient to prevent bone loss. These data show that chronic exposure to low temperature impairs bone architecture, suggesting climate may contribute to phenotypic variation in humans and other hominins.
dc.publisherJohn Wiley & Sons, Inc.
dc.subject.othernonshivering thermogenesis
dc.subject.othertrabecular bone
dc.subject.othersympathetic tone
dc.subject.othertemperature
dc.titleLow temperature decreases bone mass in mice: Implications for humans
dc.typeArticleen_US
dc.rights.robotsIndexNoFollow
dc.subject.hlbsecondlevelAnthropology
dc.subject.hlbtoplevelSocial Sciences
dc.description.peerreviewedPeer Reviewed
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/146428/1/ajpa23684.pdf
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/146428/2/ajpa23684_am.pdf
dc.identifier.doi10.1002/ajpa.23684
dc.identifier.sourceAmerican Journal of Physical Anthropology
dc.identifier.citedreferenceRoberts, D. F. ( 1953 ). Body weight, race, and climate. American Journal of Physical Anthropology, 11, 533 – 558.
dc.identifier.citedreferenceRuff, C. B. ( 1993 ). Climatic adaptation and hominid evolution: The thermoregulatory imperative. Evolutionary Anthropology, 2, 53 – 60.
dc.identifier.citedreferenceRuff, C. B. ( 1994 ). Morphological adaptation to climate in modern and fossil hominids. American Journal of Physical Anthropology, 37 ( S19 ), 65 – 107.
dc.identifier.citedreferenceSaito, M., Okamatsu‐Ogura, Y., Matsushita, M., Watanabe, K., Yoneshiro, T., Nio‐Kobayashi, J., et al. ( 2009 ). High incidence of metabolically active brown adipose tissue in healthy adult humans: Effects of cold exposure and adiposity. Diabetes, 58 ( 7 ), 1526 – 1531.
dc.identifier.citedreferenceSchneider, D. L., Barrett‐Connor, E. L., & Morton, D. J. ( 1994 ). Thyroid hormone use and bone mineral density in elderly women. Effects of estrogen. JAMA: the journal of the American Medical Association, 271 ( 16 ), 1245 – 1,249.
dc.identifier.citedreferenceSchneider, D. L., Barrett‐Connor, E. L., & Morton, D. J. ( 1995 ). Thyroid hormone use and bone mineral density in elderly men. Archives of Internal Medicine, 155 ( 18 ), 2005 – 2007.
dc.identifier.citedreferenceSerrat, M. A. ( 2013 ). Allen’s rule revisited: Temperature influences bone elongation during a critical period of postnatal development. The Anatomical Record, 296 ( 10 ), 1534 – 1,545.
dc.identifier.citedreferenceSerrat, M. A. ( 2014 ). Environmental temperature impact on bone and cartilage growth. Comprehensive Physiology, 4 ( 2 ), 621 – 655.
dc.identifier.citedreferenceSerrat, M. A., King, D., & Lovejoy, C. O. ( 2008 ). Temperature regulates limb length in homeotherms by directly modulating cartilage growth. Proceedings of the National Academy of Sciences of the United States of America, 105 ( 49 ), 19348 – 19353.
dc.identifier.citedreferenceSerrat, M. A., Schlierf, T. J., Efaw, M. L., Shuler, F. D., Godby, J., Stanko, L. M., & Tamski, H. L. ( 2015 ). Unilateral heat accelerates bone elongation and lengthens extremities of growing mice. Journal of Orthopaedic Research, 33 ( 5 ), 692 – 698.
dc.identifier.citedreferenceSerrat, M. A., Williams, R. M., & Farnum, C. E. ( 2009 ). Temperature alters solute transport in growth plate cartilage measured by in vivo multiphoton microscopy. Journal of Applied Physiology, 106 ( 6 ), 2016 – 2025.
dc.identifier.citedreferenceSerrat, M. A., Williams, R. M., & Farnum, C. E. ( 2010 ). Exercise mitigates the stunting effect of cold temperature on limb elongation in mice by increasing solute delivery to the growth plate. Journal of Applied Physiology, 109 ( 6 ), 1869 – 1879.
dc.identifier.citedreferenceSharp, L. Z., Shinoda, K., Ohno, H., Scheel, D. W., Tomoda, E., Ruiz, L., et al. ( 2012 ). Human BAT possesses molecular signatures that resemble beige/brite cells. PLoS One, 7 ( 11 ), e49452.
dc.identifier.citedreferenceSinder, B. P., Salemi, J. D., Ominsky, M. S., Caird, M. S., Marini, J. C., & Kozloff, K. M. ( 2015 ). Rapidly growing Brtl/+ mouse model of osteogenesis imperfecta improves bone mass and strength with sclerostin antibody treatment. Bone, 71, 115 – 123.
dc.identifier.citedreferenceSmith, L., Bigelow, E. M., & Jepsen, K. J. ( 2013 ). Systematic evaluation of skeletal mechanical function. Current Protocols in Mouse Biology, 3, 39 – 67.
dc.identifier.citedreferenceSpeakman, J. R., & Keijer, J. ( 2012 ). Not so hot: Optimal housing temperatures for mice to mimic the thermal environment of humans. Molecular Metabolism, 2 ( 1 ), 5 – 9.
dc.identifier.citedreferenceSteegmann, A. T., Jr. ( 2007 ). Human cold adaptation: An unfinished agenda. American Journal of Human Biology: The Official Journal of the Human Biology Council, 19 ( 2 ), 218 – 227.
dc.identifier.citedreferenceSumner, F. B. ( 1909 ). Some effects of external conditions upon the white mouse. Journal of Experimental Zoology, 7 ( 1 ), 97 – 155.
dc.identifier.citedreferenceThompson, D. D., & Gunness‐Hey, M. ( 1981 ). Bone mineral‐osteon analysis of Yupik‐Inupiaq skeletons. American Journal of Physical Anthropology, 55 ( 1 ), 1 – 7.
dc.identifier.citedreferenceToth, L. A., Trammell, R. A., & Ilsley‐Woods, M. ( 2015 ). Interactions between housing density and ambient temperature in the cage environment: Effects on mouse physiology and behavior. Journal of the American Association for Laboratory Animal Science, 54 ( 6 ), 708 – 717.
dc.identifier.citedreferencevan Marken Lichtenbelt, W. D., Vanhommerig, J. W., Smulders, N. M., Drossaerts, J. M., Kemerink, G. J., Bouvy, N. D., … Teule, G. J. ( 2009 ). Cold‐activated brown adipose tissue in healthy men. The New England Journal of Medicine, 360 ( 15 ), 1500 – 1508.
dc.identifier.citedreferenceVirtanen, K. A., Lidell, M. E., Orava, J., Heglind, M., Westergren, R., Niemi, T., et al. ( 2009 ). Functional brown adipose tissue in healthy adults. The New England Journal of Medicine, 360 ( 15 ), 1518 – 1525.
dc.identifier.citedreferenceWallace, I. J., Nesbitt, A., Mongle, C., Gould, E. S., & Grine, F. E. ( 2014 ). Age‐related variation in limb bone diaphyseal structure among Inuit foragers from point hope, northern Alaska. Archives of Osteoporosis, 9, 202.
dc.identifier.citedreferenceWeaver, M. E., & Ingram, D. L. ( 1969 ). Morphological changes in swine associated with environmental temperature. Ecology, 50 ( 4 ), 710 – 713.
dc.identifier.citedreferenceWu J, Bostrom P, Sparks LM, Ye L, Choi JH, Giang AH, Khandekar M, Virtanen KA, Nuutila P, Schaart G Spiegelman BM 2012. Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell 150 ( 2 ): 366 – 376.
dc.identifier.citedreferenceYang, S., Nguyen, N. D., Eisman, J. A., & Nguyen, T. V. ( 2012 ). Association between beta‐blockers and fracture risk: A Bayesian meta‐analysis. Bone, 51 ( 5 ), 969 – 974.
dc.identifier.citedreferenceAguirre, J. I., Leal, M. E., Rivera, M. F., Vanegas, S. M., Jorgensen, M., & Wronski, T. J. ( 2007 ). Effects of basic fibroblast growth factor and a prostaglandin E2 receptor subtype 4 agonist on osteoblastogenesis and adipogenesis in aged ovariectomized rats. Journal of Bone and Mineral Research: The Official Journal of the American Society for Bone and Mineral Research, 22 ( 6 ), 877 – 888.
dc.identifier.citedreferenceAl‐Hilli, F., & Wright, E. A. ( 1983 ). The effects of changes in the environmental temperature on the growth of bone in the mouse. Radiological and morphological study. British Journal of Experimental Pathology, 64 ( 1 ), 43 – 52.
dc.identifier.citedreferenceAldridge, G. M., Podrebarac, D. M., Greenough, W. T., & Weiler, I. J. ( 2008 ). The use of total protein stains as loading controls: An alternative to high‐abundance single‐protein controls in semi‐quantitative immunoblotting. Journal of Neuroscience Methods, 172 ( 2 ), 250 – 254.
dc.identifier.citedreferenceAllain, T. J., & McGregor, A. M. ( 1993 ). Thyroid hormones and bone. The Journal of endocrinology, 139 ( 1 ), 9 – 18.
dc.identifier.citedreferenceAllen, J. A. ( 1877 ). The influence of physical conditions in the genesis of species. Radical Review, 1, 108 – 140.
dc.identifier.citedreferenceAshoub, M. A. ( 1958 ). Effect of two extreme temperatures on growth and tail‐length of mice. Nature, 181 ( 4604 ), 284.
dc.identifier.citedreferenceAu‐Yong, I. T., Thorn, N., Ganatra, R., Perkins, A. C., & Symonds, M. E. ( 2009 ). Brown adipose tissue and seasonal variation in humans. Diabetes, 58 ( 11 ), 2583 – 2587.
dc.identifier.citedreferenceBergmann, C. ( 1847 ). Ueber die verhaltnisse der warmeokonomie der thiere zu ihrer grosse. Gottinger Studien, 3, 595 – 708.
dc.identifier.citedreferenceBilezikian, J. P., Raisz, L. G., & Rodan, G. A. ( 2002 ). Principles of bone biology. San Diego: Academic Press.
dc.identifier.citedreferenceBonnet, N., Gadois, C., McCloskey, E., Lemineur, G., Lespessailles, E., Courteix, D., & Benhamou, C. L. ( 2007 ). Protective effect of beta blockers in postmenopausal women: Influence on fractures, bone density, micro and macroarchitecture. Bone, 40 ( 5 ), 1209 – 1216.
dc.identifier.citedreferenceBonnet, N., Pierroz, D. D., & Ferrari, S. L. ( 2008 ). Adrenergic control of bone remodeling and its implications for the treatment of osteoporosis. Journal of Musculoskeletal & Neuronal Interactions, 8 ( 2 ), 94 – 104.
dc.identifier.citedreferenceBouxsein, M. L., Boyd, S. K., Christiansen, B. A., Guldberg, R. E., Jepsen, K. J., & Müller, R. ( 2010 ). Guidelines for assessment of bone microstructure in rodents using micro–computed tomography. Journal of Bone and Mineral Research, 25 ( 7 ), 1468 – 1486.
dc.identifier.citedreferenceBouxsein, M. L., Devlin, M. J., Glatt, V., Dhillon, H., Pierroz, D. D., & Ferrari, S. L. ( 2009 ). Mice lacking Beta‐adrenergic receptors have increased bone mass, but are not protected from deleterious skeletal effects of ovariectomy. Endocrinology, 150 ( 1 ), 144 – 52.
dc.identifier.citedreferenceBouxsein, M. L., Pierroz, D. D., Glatt, V., Goddard, D. S., Cavat, F., Rizzoli, R., & Ferrari, S. L. ( 2005 ). Beta‐Arrestin2 regulates the differential response of cortical and trabecular bone to intermittent PTH in female mice. Journal of Bone and Mineral Research: The Official Journal of the American Society for Bone and Mineral Research, 20 ( 4 ), 635 – 643.
dc.identifier.citedreferenceBredella, M. A., Fazeli, P. K., Freedman, L. M., Calder, G., Lee, H., Rosen, C. J., & Klibanski, A. ( 2012 ). Young women with cold‐activated brown adipose tissue have higher bone mineral density and lower Pref‐1 than women without brown adipose tissue: A study in women with anorexia nervosa, women recovered from anorexia nervosa, and normal‐weight women. The Journal of Clinical Endocrinology and Metabolism, 97 ( 4 ), E584 – E590.
dc.identifier.citedreferenceBredella, M. A., Gill, C. M., Rosen, C. J., Klibanski, A., & Torriani, M. ( 2014 ). Positive effects of brown adipose tissue on femoral bone structure. Bone, 58, 55 – 58.
dc.identifier.citedreferenceCannon, B., & Nedergaard, J. ( 2011 ). Nonshivering thermogenesis and its adequate measurement in metabolic studies. The Journal of Experimental Biology, 214 ( Pt 2 ), 242 – 253.
dc.identifier.citedreferenceChurchill, S. E. ( 1998 ). Cold adaptation, heterochrony, and Neandertals. Evolutionary Anthropology, 7 ( 2 ), 46 – 61.
dc.identifier.citedreferenceCypess, A. M., Lehman, S., Williams, G., Tal, I., Rodman, D., Goldfine, A. B., et al. ( 2009 ). Identification and importance of brown adipose tissue in adult humans. The New England Journal of Medicine, 360 ( 15 ), 1509 – 1517.
dc.identifier.citedreferenceDavid, J. M., Chatziioannou, A. F., Taschereau, R., Wang, H., & Stout, D. B. ( 2013 ). The hidden cost of housing practices: Using noninvasive imaging to quantify the metabolic demands of chronic cold stress of laboratory mice. Comparative Medicine, 63 ( 5 ), 386 – 391.
dc.identifier.citedreferenceDempster, D. W., Compston, J. E., Drezner, M. K., Glorieux, F. H., Kanis, J. A., Malluche, H., … Parfitt, A. M. ( 2013 ). Standardized nomenclature, symbols, and units for bone histomorphometry: A 2012 update of the report of the ASBMR Histomorphometry Nomenclature Committee. Journal of Bone and Mineral Research: The Official Journal of the American Society for Bone and Mineral Research, 28 ( 1 ), 2 – 17.
dc.identifier.citedreferenceDevlin, M. J. ( 2015 ). The “skinny” on brown fat, obesity, and bone. American Journal of Physical Anthropology, 156 ( Suppl 59 ), 98 – 115.
dc.identifier.citedreferenceDevlin, M. J., Brooks, D. J., Conlon, C., Vliet, M., Louis, L., Rosen, C. J., & Bouxsein, M. L. ( 2016 ). Daily leptin blunts marrow fat but does not impact bone mass in calorie‐restricted mice. The Journal of Endocrinology, 229 ( 3 ), 295 – 306.
dc.identifier.citedreferenceDevlin, M. J., Van Vliet, M., Motyl, K., Karim, L., Brooks, D. J., Louis, L., … Bouxsein, M. L. ( 2014 ). Early‐onset type 2 diabetes impairs skeletal acquisition in the Male TALLYHO/JngJ mouse. Endocrinology, 155 ( 10 ), 3806 – 3,816.
dc.identifier.citedreferenceErikson, H., Krog, J., Andersen, K. L., & Scholander, P. F. ( 1956 ). The critical temperature in naked man. Acta Physiologica Scandinavica, 37 ( 1 ), 35 – 39.
dc.identifier.citedreferenceFischer, A. W., Cannon, B., & Nedergaard, J. ( 2018 ). Optimal housing temperatures for mice to mimic the thermal environment of humans: An experimental study. Molecular Metabolism, 7, 161 – 170.
dc.identifier.citedreferenceFoster, F., & Collard, M. ( 2013 ). A reassessment of Bergmann’s rule in modern humans. PLoS One, 8 ( 8 ), e72269.
dc.identifier.citedreferenceGaskill, B. N., Gordon, C. J., Pajor, E. A., Lucas, J. R., Davis, J. K., & Garner, J. P. ( 2012 ). Heat or insulation: Behavioral titration of mouse preference for warmth or access to a nest. PLoS One, 7 ( 3 ), e32799.
dc.identifier.citedreferenceGilda, J. E., & Gomes, A. V. ( 2013 ). Stain‐free total protein staining is a superior loading control to beta‐actin for western blots. Analytical Biochemistry, 440 ( 2 ), 186 – 188.
dc.identifier.citedreferenceGilsanz, V., Smith, M. L., Goodarzian, F., Kim, M., Wren, T. A., & Hu, H. H. ( 2012 ). Changes in brown adipose tissue in boys and girls during childhood and puberty. The Journal of Pediatrics, 160 ( 4 ), 604 – 609 e601.
dc.identifier.citedreferenceGordon, C. J. ( 2012 ). Thermal physiology of laboratory mice: Defining thermoneutrality. Journal of Thermal Biology, 37 ( 8 ), 654 – 685.
dc.identifier.citedreferenceHardy, J. D., & Dubois, E. F. ( 1937 ). Regulation of heat loss from the human body. Proceedings of the National Academy of Sciences of the United States of America, 23 ( 12 ), 624 – 631.
dc.identifier.citedreferenceHarper, A. B., Laughlin, W. S., & Mazess, R. B. ( 1984 ). Bone mineral content in St. Lawrence Island Eskimos. Human Biology, 56 ( 1 ), 63 – 78.
dc.identifier.citedreferenceHeaton, J. M. ( 1972 ). The distribution of brown adipose tissue in the human. Journal of Anatomy, 112 ( Pt 1 ), 35 – 39.
dc.identifier.citedreferenceHildebrand, T., Laib, A., Muller, R., Dequeker, J., & Ruegsegger, P. ( 1999 ). Direct three‐dimensional morphometric analysis of human cancellous bone: Microstructural data from spine, femur, iliac crest, and calcaneus. Journal of Bone and Mineral Research: The Official Journal of the American Society for Bone and Mineral Research, 14 ( 7 ), 1167 – 1174.
dc.identifier.citedreferenceHildebrand, T., & Rüegsegger, P. ( 1997 ). A new method for the model independent assessment of thickness in three‐dimensional images. Journal of Microscopy, 185, 67 – 75.
dc.identifier.citedreferenceHolliday, T. W. ( 1997 ). Body proportions in late Pleistocene Europe and modern human origins. Journal of Human Evolution, 32 ( 5 ), 423 – 448.
dc.identifier.citedreferenceHolliday, T. W., & Hilton, C. E. ( 2010 ). Body proportions of circumpolar peoples as evidenced from skeletal data: Ipiutak and Tigara (point hope) versus Kodiak Island Inuit. American Journal of Physical Anthropology., 142 ( 2 ), 287 – 302.
dc.identifier.citedreferenceHuggins, C., & Blocksom, B. H. ( 1936 ). Changes in outlying bone marrow accompanying a local increase of temperature within physiological limits. Journal of Experimental Medicine, 64 ( 2 ), 253 – 274.
dc.identifier.citedreferenceHuttunen, P., Hirvonen, J., & Kinnula, V. ( 1981 ). The occurrence of brown adipose tissue in outdoor workers. European Journal of Applied Physiology and Occupational Physiology, 46 ( 4 ), 339 – 345.
dc.identifier.citedreferenceIwaniec, U. T., Philbrick, K. A., Wong, C. P., Gordon, J. L., Kahler‐Quesada, A. M., Olson, D. A., et al. ( 2016 ). Room temperature housing results in premature cancellous bone loss in growing female mice: Implications for the mouse as a preclinical model for age‐related bone loss. Osteoporosis International, 27 ( 10 ), 3091 – 3,101.
dc.identifier.citedreferenceJepsen, K. J., Silva, M. J., Vashishth, D., Guo, X. E., & van der Meulen, M. C. ( 2015 ). Establishing biomechanical mechanisms in mouse models: Practical guidelines for systematically evaluating phenotypic changes in the diaphyses of long bones. Journal of Bone and Mineral Research: The Official Journal of the American Society for Bone and Mineral Research, 30 ( 6 ), 951 – 966.
dc.identifier.citedreferenceKajimura, D., Hinoi, E., Ferron, M., Kode, A., Riley, K. J., Zhou, B., … Karsenty, G. ( 2011 ). Genetic determination of the cellular basis of the sympathetic regulation of bone mass accrual. Journal of Experimental Medicine, 208 ( 4 ), 841 – 851.
dc.identifier.citedreferenceKarp, C. L. ( 2012 ). Unstressing intemperate models: How cold stress undermines mouse modeling. Journal of Experimental Medicine, 209 ( 6 ), 1069 – 1,074.
dc.identifier.citedreferenceKatzmarzyk, P. T., & Leonard, W. R. ( 1998 ). Climatic influences on human body size and proportions: Ecological adaptations and secular trends. American Journal of Physical Anthropology, 106 ( 4 ), 483 – 503.
dc.identifier.citedreferenceKingma, B., Frijns, A., & van Marken Lichtenbelt, W. ( 2012 ). The thermoneutral zone: Implications for metabolic studies. Frontiers in Bioscience, 4, 1975 – 1985.
dc.identifier.citedreferenceKingma, B. R., Frijns, A. J., Schellen, L., & van Marken Lichtenbelt, W. D. ( 2014 ). Beyond the classic thermoneutral zone: Including thermal comfort. Temperature (Austin), 1 ( 2 ), 142 – 149.
dc.identifier.citedreferenceLang, D. H., Sharkey, N. A., Lionikas, A., Mack, H. A., Larsson, L., Vogler, G. P., et al. ( 2005 ). Adjusting data to body size: A comparison of methods as applied to quantitative trait loci analysis of musculoskeletal phenotypes. Journal of Bone and Mineral Research: The Official Journal of the American Society for Bone and Mineral Research, 20 ( 5 ), 748 – 757.
dc.identifier.citedreferenceLazenby, R. A. ( 1997 ). Bone loss, traditional diet, and cold adaptation in Arctic populations. American Journal of Human Biology, 9 ( 3 ), 329 – 341.
dc.identifier.citedreferenceLee, P., Brychta, R. J., Collins, M. T., Linderman, J., Smith, S., Herscovitch, P., … Celi, F. S. ( 2013 ). Cold‐activated brown adipose tissue is an independent predictor of higher bone mineral density in women. Osteoporosis International, 24 ( 4 ), 1513 – 1518.
dc.identifier.citedreferenceLeonard, W. R., & Levy, S. B. ( 2015 ). Contributions of brown adipose tissue to human metabolic adaptation: Comparative and evolutionary perspectives. American Journal of Physical Anthropology, 156 ( S60 ): 202.
dc.identifier.citedreferenceLeslie, W. D., Metge, C. J., Weiler, H. A., Doupe, M., Wood Steiman, P., & O’Neil, J. D. ( 2006 ). Bone density and bone area in Canadian aboriginal women: The first nations bone health study. Osteoporosis International, 17 ( 12 ), 1755 – 1762.
dc.identifier.citedreferenceLeslie, W. D., Weiler, H. A., Lix, L. M., & Nyomba, B. L. ( 2008 ). Body composition and bone density in Canadian white and aboriginal women: The first nations bone health study. Bone, 42 ( 5 ), 990 – 995.
dc.identifier.citedreferenceLivak, K. J., & Schmittgen, T. D. ( 2001 ). Analysis of relative gene expression data using real‐time quantitative PCR and the 2(−Delta Delta C[T]) method. Methods, 25 ( 4 ), 402 – 408.
dc.identifier.citedreferenceLodhi, I. J., & Semenkovich, C. F. ( 2009 ). Why we should put clothes on mice. Cell Metabolism, 9 ( 2 ), 111 – 112.
dc.identifier.citedreferenceLowell, B. B., & Spiegelman, B. M. ( 2000 ). Towards a molecular understanding of adaptive thermogenesis. Nature, 404 ( 6778 ), 652 – 660.
dc.identifier.citedreferenceMazess, R. B., & Mather, W. ( 1974 ). Bone mineral content of north Alaskan Eskimos. The American Journal of Clinical Nutrition, 27 ( 9 ), 916 – 925.
dc.identifier.citedreferenceMazess, R. B., & Mather, W. E. ( 1975 ). Bone mineral content in Canadian Eskimos. Human Biology, 47 ( 1 ), 44 – 63.
dc.identifier.citedreferenceMeinel, L., Fajardo, R., Hofmann, S., Langer, R., Chen, J., Snyder, B., … Kaplan, D. ( 2005 ). Silk implants for the healing of critical size bone defects. Bone, 37 ( 5 ), 688 – 698.
dc.identifier.citedreferenceMotyl, K. J., Bishop, K. A., DeMambro, V. E., Bornstein, S. A., Le, P., Kawai, M., et al. ( 2013 ). Altered thermogenesis and impaired bone remodeling in misty mice. Journal of Bone and Mineral Research: The Official Journal of the American Society for Bone and Mineral Research, 28 ( 9 ), 1885 – 1897.
dc.identifier.citedreferenceMotyl, K. J., & Rosen, C. J. ( 2011 ). Temperatures rising: Brown fat and bone. Discovery Medicine, 11 ( 58 ), 179 – 185.
dc.identifier.citedreferenceMurray, I., Havel, P. J., Sniderman, A. D., & Cianflone, K. ( 2000 ). Reduced body weight, adipose tissue, and leptin levels despite increased energy intake in female mice lacking acylation‐stimulating protein. Endocrinology, 141 ( 3 ), 1041 – 1049.
dc.identifier.citedreferenceNagy, T. R., Krzywanski, D., Li, J., Meleth, S., & Desmond, R. ( 2002 ). Effect of group vs. single housing on phenotypic variance in C57BL/6J mice. Obesity Research, 10 ( 5 ), 412 – 415.
dc.identifier.citedreferenceNicholls, D. G., & Rial, E. ( 1999 ). A history of the first uncoupling protein, UCP1. Journal of Bioenergetics and Biomembranes, 31 ( 5 ), 399 – 406.
dc.identifier.citedreferenceOverton, J. M. ( 2010 ). Phenotyping small animals as models for the human metabolic syndrome: Thermoneutrality matters. International Journal of Obesity, 34 ( Suppl 2 ), S53 – S58.
dc.identifier.citedreferencePearson, O. M. ( 2000 ). Activity, climate, and postcranial robusticity: Implications for modern human origins and scenarios of adaptive change. Current Anthropologyl, 41 ( 4 ), 569 – 607.
dc.identifier.citedreferencePonrartana, S., Aggabao, P. C., Hu, H. H., Aldrovandi, G. M., Wren, T. A., & Gilsanz, V. ( 2012 ). Brown adipose tissue and its relationship to bone structure in pediatric patients. The Journal of Clinical Endocrinology and Metabolism, 97 ( 8 ), 2693 – 2,698.
dc.identifier.citedreferenceRidler, T., & Calvard, S. ( 1978 ). Picture thresholding using an iterative selection method. IEEE Transactions on Systems, Man, and Cybernetics, SMC‐8 ( 8 ), 630 – 632.
dc.identifier.citedreferenceRuff, C. ( 2002 ). Variation in human body size and shape. Annual Review of Anthropology, 31 ( 1 ), 211 – 232.
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