Bone marrow adipose tissue is an endocrine organ that contributes to increased circulating adiponectin during caloric restriction

William P. Cawthorn; Erica L. Scheller; Brian S. Learman; Sebastian D. Parlee; Becky R. Simon; Hiroyuki Mori; Xiaomin Ning; Adam J. Bree; Benjamin Schell; David T. Broome; Sandra S. Soliman; Jenifer L. Delproposto; Carey N. Lumeng; Aditi Mitra; Sandeep V. Pandit; Katherine A. Gallagher; Joshua D. Miller; Venkatesh Krishnan; Susanta K. Hui; Miriam A. Bredella; Pouneh K. Fazeli; Anne Klibanski; Mark C. Horowitz; Clifford J. Rosen; Ormond A. Macdougald

doi:10.1016/j.cmet.2014.06.003

Bone marrow adipose tissue is an endocrine organ that contributes to increased circulating adiponectin during caloric restriction

William P. Cawthorn, Erica L. Scheller, Brian S. Learman, Sebastian D. Parlee, Becky R. Simon, Hiroyuki Mori, Xiaomin Ning, Adam J. Bree, Benjamin Schell, David T. Broome, Sandra S. Soliman, Jenifer L. Delproposto, Carey N. Lumeng, Aditi Mitra, Sandeep V. Pandit, Katherine A. Gallagher, Joshua D. Miller, Venkatesh Krishnan, Susanta K. Hui, Miriam A. BredellaPouneh K. Fazeli, Anne Klibanski, Mark C. Horowitz, Clifford J. Rosen, Ormond A. Macdougald

Radiation Oncology

Research output: Contribution to journal › Article › peer-review

328 Scopus citations

Abstract

Summary The adipocyte-derived hormone adiponectin promotes metabolic and cardiovascular health. Circulating adiponectin increases in lean states such as caloric restriction (CR), but the reasons for this paradox remain unclear. Unlike white adipose tissue (WAT), bone marrow adipose tissue (MAT) increases during CR, and both MAT and serum adiponectin increase in many other clinical conditions. Thus, we investigated whether MAT contributes to circulating adiponectin. We find that adiponectin secretion is greater from MAT than WAT. Notably, specific inhibition of MAT formation in mice results in decreased circulating adiponectin during CR despite unaltered adiponectin expression in WAT. Inhibiting MAT formation also alters skeletal muscle adaptation to CR, suggesting that MAT exerts systemic effects. Finally, we reveal that both MAT and serum adiponectin increase during cancer therapy in humans. These observations identify MAT as an endocrine organ that contributes significantly to increased serum adiponectin during CR and perhaps in other adverse states.

Original language	English (US)
Pages (from-to)	368-375
Number of pages	8
Journal	Cell Metabolism
Volume	20
Issue number	2
DOIs	https://doi.org/10.1016/j.cmet.2014.06.003
State	Published - Aug 5 2014

Bibliographical note

Funding Information:
This work was supported by the National Institutes of Health (R24 DK092759 to O.A.M., A.K., M.C.H., and C.J.R.; R01 DK62876 to O.A.M.; K99-DE-024178 to E.L.S.; R01 DK090262 to C.N.L.; 1R03AR055333 and 1K12-HD055887 to S.K.H.; P30 DK089503 to the Michigan Nutrition Obesity Research Center). S.K.H. is also supported by the Translational Science Institute of University of Minnesota (8UL1TR0001114). O.A.M. holds a Fulbright Scholar Award. W.P.C. holds a Lilly Innovation Fellowship Award and previously a Postdoctoral Research Fellowship from the Royal Commission for the Exhibition of 1851. H.M. was supported by a mentor-based postdoctoral fellowship from the American Diabetes Association. D.T.B. and S.S.S. were supported by the University of Michigan Molecular & Integrative Physiology Department SURF program. W.P.C. holds a postdoctoral fellowship funded by Eli Lilly and Company; V.K. is employed by Eli Lilly and Company; O.A.M. holds stock in MRK and ESRX and has received research funding from Eli Lilly and Company. E.L.S. and O.A.M. have received research funding from Biomet Biologics. A.K. has received research funding from Rhythm Pharmaceuticals.

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

Publisher link

10.1016/j.cmet.2014.06.003

Find It

Find It at U of M Libraries

Cite this

Cawthorn, W. P., Scheller, E. L., Learman, B. S., Parlee, S. D., Simon, B. R., Mori, H., Ning, X., Bree, A. J., Schell, B., Broome, D. T., Soliman, S. S., Delproposto, J. L., Lumeng, C. N., Mitra, A., Pandit, S. V., Gallagher, K. A., Miller, J. D., Krishnan, V., Hui, S. K., ... Macdougald, O. A. (2014). Bone marrow adipose tissue is an endocrine organ that contributes to increased circulating adiponectin during caloric restriction. Cell Metabolism, 20(2), 368-375. https://doi.org/10.1016/j.cmet.2014.06.003

Cawthorn, WP, Scheller, EL, Learman, BS, Parlee, SD, Simon, BR, Mori, H, Ning, X, Bree, AJ, Schell, B, Broome, DT, Soliman, SS, Delproposto, JL, Lumeng, CN, Mitra, A, Pandit, SV, Gallagher, KA, Miller, JD, Krishnan, V, Hui, SK, Bredella, MA, Fazeli, PK, Klibanski, A, Horowitz, MC, Rosen, CJ & Macdougald, OA 2014, 'Bone marrow adipose tissue is an endocrine organ that contributes to increased circulating adiponectin during caloric restriction', Cell Metabolism, vol. 20, no. 2, pp. 368-375. https://doi.org/10.1016/j.cmet.2014.06.003

@article{1cdb0c3655a24956ad8e549837a65592,

title = "Bone marrow adipose tissue is an endocrine organ that contributes to increased circulating adiponectin during caloric restriction",

abstract = "Summary The adipocyte-derived hormone adiponectin promotes metabolic and cardiovascular health. Circulating adiponectin increases in lean states such as caloric restriction (CR), but the reasons for this paradox remain unclear. Unlike white adipose tissue (WAT), bone marrow adipose tissue (MAT) increases during CR, and both MAT and serum adiponectin increase in many other clinical conditions. Thus, we investigated whether MAT contributes to circulating adiponectin. We find that adiponectin secretion is greater from MAT than WAT. Notably, specific inhibition of MAT formation in mice results in decreased circulating adiponectin during CR despite unaltered adiponectin expression in WAT. Inhibiting MAT formation also alters skeletal muscle adaptation to CR, suggesting that MAT exerts systemic effects. Finally, we reveal that both MAT and serum adiponectin increase during cancer therapy in humans. These observations identify MAT as an endocrine organ that contributes significantly to increased serum adiponectin during CR and perhaps in other adverse states.",

author = "Cawthorn, {William P.} and Scheller, {Erica L.} and Learman, {Brian S.} and Parlee, {Sebastian D.} and Simon, {Becky R.} and Hiroyuki Mori and Xiaomin Ning and Bree, {Adam J.} and Benjamin Schell and Broome, {David T.} and Soliman, {Sandra S.} and Delproposto, {Jenifer L.} and Lumeng, {Carey N.} and Aditi Mitra and Pandit, {Sandeep V.} and Gallagher, {Katherine A.} and Miller, {Joshua D.} and Venkatesh Krishnan and Hui, {Susanta K.} and Bredella, {Miriam A.} and Fazeli, {Pouneh K.} and Anne Klibanski and Horowitz, {Mark C.} and Rosen, {Clifford J.} and Macdougald, {Ormond A.}",

note = "Funding Information: This work was supported by the National Institutes of Health (R24 DK092759 to O.A.M., A.K., M.C.H., and C.J.R.; R01 DK62876 to O.A.M.; K99-DE-024178 to E.L.S.; R01 DK090262 to C.N.L.; 1R03AR055333 and 1K12-HD055887 to S.K.H.; P30 DK089503 to the Michigan Nutrition Obesity Research Center). S.K.H. is also supported by the Translational Science Institute of University of Minnesota (8UL1TR0001114). O.A.M. holds a Fulbright Scholar Award. W.P.C. holds a Lilly Innovation Fellowship Award and previously a Postdoctoral Research Fellowship from the Royal Commission for the Exhibition of 1851. H.M. was supported by a mentor-based postdoctoral fellowship from the American Diabetes Association. D.T.B. and S.S.S. were supported by the University of Michigan Molecular & Integrative Physiology Department SURF program. W.P.C. holds a postdoctoral fellowship funded by Eli Lilly and Company; V.K. is employed by Eli Lilly and Company; O.A.M. holds stock in MRK and ESRX and has received research funding from Eli Lilly and Company. E.L.S. and O.A.M. have received research funding from Biomet Biologics. A.K. has received research funding from Rhythm Pharmaceuticals. ",

year = "2014",

month = aug,

day = "5",

doi = "10.1016/j.cmet.2014.06.003",

language = "English (US)",

volume = "20",

pages = "368--375",

journal = "Cell Metabolism",

issn = "1550-4131",

publisher = "Cell Press",

number = "2",

}

TY - JOUR

T1 - Bone marrow adipose tissue is an endocrine organ that contributes to increased circulating adiponectin during caloric restriction

AU - Cawthorn, William P.

AU - Scheller, Erica L.

AU - Learman, Brian S.

AU - Parlee, Sebastian D.

AU - Simon, Becky R.

AU - Mori, Hiroyuki

AU - Ning, Xiaomin

AU - Bree, Adam J.

AU - Schell, Benjamin

AU - Broome, David T.

AU - Soliman, Sandra S.

AU - Delproposto, Jenifer L.

AU - Lumeng, Carey N.

AU - Mitra, Aditi

AU - Pandit, Sandeep V.

AU - Gallagher, Katherine A.

AU - Miller, Joshua D.

AU - Krishnan, Venkatesh

AU - Hui, Susanta K.

AU - Bredella, Miriam A.

AU - Fazeli, Pouneh K.

AU - Klibanski, Anne

AU - Horowitz, Mark C.

AU - Rosen, Clifford J.

AU - Macdougald, Ormond A.

N1 - Funding Information: This work was supported by the National Institutes of Health (R24 DK092759 to O.A.M., A.K., M.C.H., and C.J.R.; R01 DK62876 to O.A.M.; K99-DE-024178 to E.L.S.; R01 DK090262 to C.N.L.; 1R03AR055333 and 1K12-HD055887 to S.K.H.; P30 DK089503 to the Michigan Nutrition Obesity Research Center). S.K.H. is also supported by the Translational Science Institute of University of Minnesota (8UL1TR0001114). O.A.M. holds a Fulbright Scholar Award. W.P.C. holds a Lilly Innovation Fellowship Award and previously a Postdoctoral Research Fellowship from the Royal Commission for the Exhibition of 1851. H.M. was supported by a mentor-based postdoctoral fellowship from the American Diabetes Association. D.T.B. and S.S.S. were supported by the University of Michigan Molecular & Integrative Physiology Department SURF program. W.P.C. holds a postdoctoral fellowship funded by Eli Lilly and Company; V.K. is employed by Eli Lilly and Company; O.A.M. holds stock in MRK and ESRX and has received research funding from Eli Lilly and Company. E.L.S. and O.A.M. have received research funding from Biomet Biologics. A.K. has received research funding from Rhythm Pharmaceuticals.

PY - 2014/8/5

Y1 - 2014/8/5

N2 - Summary The adipocyte-derived hormone adiponectin promotes metabolic and cardiovascular health. Circulating adiponectin increases in lean states such as caloric restriction (CR), but the reasons for this paradox remain unclear. Unlike white adipose tissue (WAT), bone marrow adipose tissue (MAT) increases during CR, and both MAT and serum adiponectin increase in many other clinical conditions. Thus, we investigated whether MAT contributes to circulating adiponectin. We find that adiponectin secretion is greater from MAT than WAT. Notably, specific inhibition of MAT formation in mice results in decreased circulating adiponectin during CR despite unaltered adiponectin expression in WAT. Inhibiting MAT formation also alters skeletal muscle adaptation to CR, suggesting that MAT exerts systemic effects. Finally, we reveal that both MAT and serum adiponectin increase during cancer therapy in humans. These observations identify MAT as an endocrine organ that contributes significantly to increased serum adiponectin during CR and perhaps in other adverse states.

AB - Summary The adipocyte-derived hormone adiponectin promotes metabolic and cardiovascular health. Circulating adiponectin increases in lean states such as caloric restriction (CR), but the reasons for this paradox remain unclear. Unlike white adipose tissue (WAT), bone marrow adipose tissue (MAT) increases during CR, and both MAT and serum adiponectin increase in many other clinical conditions. Thus, we investigated whether MAT contributes to circulating adiponectin. We find that adiponectin secretion is greater from MAT than WAT. Notably, specific inhibition of MAT formation in mice results in decreased circulating adiponectin during CR despite unaltered adiponectin expression in WAT. Inhibiting MAT formation also alters skeletal muscle adaptation to CR, suggesting that MAT exerts systemic effects. Finally, we reveal that both MAT and serum adiponectin increase during cancer therapy in humans. These observations identify MAT as an endocrine organ that contributes significantly to increased serum adiponectin during CR and perhaps in other adverse states.

UR - http://www.scopus.com/inward/record.url?scp=84905817103&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84905817103&partnerID=8YFLogxK

U2 - 10.1016/j.cmet.2014.06.003

DO - 10.1016/j.cmet.2014.06.003

M3 - Article

C2 - 24998914

AN - SCOPUS:84905817103

SN - 1550-4131

VL - 20

SP - 368

EP - 375

JO - Cell Metabolism

JF - Cell Metabolism

IS - 2

ER -

Bone marrow adipose tissue is an endocrine organ that contributes to increased circulating adiponectin during caloric restriction

Abstract

Bibliographical note

UN SDGs

Publisher link

Find It

Other files and links

Fingerprint

Cite this