Intercellular Mitochondria Transfer to Macrophages Regulates White Adipose Tissue Homeostasis and Is Impaired in Obesity

Jonathan R. Brestoff; Craig B. Wilen; John R. Moley; Yongjia Li; Wei Zou; Nicole P. Malvin; Marina N. Rowen; Brian T. Saunders; Hongming Ma; Madison R. Mack; Barry L. Hykes; Dale R. Balce; Anthony Orvedahl; Jesse W. Williams; Nidhi Rohatgi; Xiaoyan Wang; Michael R. McAllaster; Scott A. Handley; Brian S. Kim; John G. Doench; Bernd H. Zinselmeyer; Michael S. Diamond; Herbert W. Virgin; Andrew E. Gelman; Steven L. Teitelbaum

doi:10.1016/j.cmet.2020.11.008

Intercellular Mitochondria Transfer to Macrophages Regulates White Adipose Tissue Homeostasis and Is Impaired in Obesity

Jonathan R. Brestoff, Craig B. Wilen, John R. Moley, Yongjia Li, Wei Zou, Nicole P. Malvin, Marina N. Rowen, Brian T. Saunders, Hongming Ma, Madison R. Mack, Barry L. Hykes, Dale R. Balce, Anthony Orvedahl, Jesse W. Williams, Nidhi Rohatgi, Xiaoyan Wang, Michael R. McAllaster, Scott A. Handley, Brian S. Kim, John G. DoenchBernd H. Zinselmeyer, Michael S. Diamond, Herbert W. Virgin, Andrew E. Gelman, Steven L. Teitelbaum

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232 Scopus citations

Abstract

Brestoff et al. show that adipose-tissue-resident macrophages acquire mitochondria from neighboring adipocytes in a heparan-sulfate-dependent process that is impaired in obesity. Genetic disruption of mitochondria uptake by macrophages reduces energy expenditure and exacerbates diet-induced obesity in mice, indicating that intercellular mitochondria transfer to macrophages mediates systemic metabolic homeostasis.

Original language	English
Pages (from-to)	270-282.e8
Journal	Cell metabolism
Volume	33
Issue number	2
DOIs	https://doi.org/10.1016/j.cmet.2020.11.008
State	Published - Feb 2 2021

Keywords

beige adipose tissue
brown adipose tissue
horizontal mitochondria transfer
immunometabolism
intercellular mitochondria transfer
macrophage
metabolism
mitochondria
obesity
white adipose tissue

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10.1016/j.cmet.2020.11.008

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Brestoff, J. R., Wilen, C. B., Moley, J. R., Li, Y., Zou, W., Malvin, N. P., Rowen, M. N., Saunders, B. T., Ma, H., Mack, M. R., Hykes, B. L., Balce, D. R., Orvedahl, A., Williams, J. W., Rohatgi, N., Wang, X., McAllaster, M. R., Handley, S. A., Kim, B. S., ... Teitelbaum, S. L. (2021). Intercellular Mitochondria Transfer to Macrophages Regulates White Adipose Tissue Homeostasis and Is Impaired in Obesity. Cell metabolism, 33(2), 270-282.e8. https://doi.org/10.1016/j.cmet.2020.11.008

@article{180a116402f146458fde0eb0bd71b403,

title = "Intercellular Mitochondria Transfer to Macrophages Regulates White Adipose Tissue Homeostasis and Is Impaired in Obesity",

abstract = "Brestoff et al. show that adipose-tissue-resident macrophages acquire mitochondria from neighboring adipocytes in a heparan-sulfate-dependent process that is impaired in obesity. Genetic disruption of mitochondria uptake by macrophages reduces energy expenditure and exacerbates diet-induced obesity in mice, indicating that intercellular mitochondria transfer to macrophages mediates systemic metabolic homeostasis.",

keywords = "beige adipose tissue, brown adipose tissue, horizontal mitochondria transfer, immunometabolism, intercellular mitochondria transfer, macrophage, metabolism, mitochondria, obesity, white adipose tissue",

author = "Brestoff, \{Jonathan R.\} and Wilen, \{Craig B.\} and Moley, \{John R.\} and Yongjia Li and Wei Zou and Malvin, \{Nicole P.\} and Rowen, \{Marina N.\} and Saunders, \{Brian T.\} and Hongming Ma and Mack, \{Madison R.\} and Hykes, \{Barry L.\} and Balce, \{Dale R.\} and Anthony Orvedahl and Williams, \{Jesse W.\} and Nidhi Rohatgi and Xiaoyan Wang and McAllaster, \{Michael R.\} and Handley, \{Scott A.\} and Kim, \{Brian S.\} and Doench, \{John G.\} and Zinselmeyer, \{Bernd H.\} and Diamond, \{Michael S.\} and Virgin, \{Herbert W.\} and Gelman, \{Andrew E.\} and Teitelbaum, \{Steven L.\}",

note = "Publisher Copyright: {\textcopyright} 2020 Elsevier Inc.",

year = "2021",

month = feb,

day = "2",

doi = "10.1016/j.cmet.2020.11.008",

language = "English",

volume = "33",

pages = "270--282.e8",

journal = "Cell metabolism",

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Brestoff, JR, Wilen, CB, Moley, JR, Li, Y, Zou, W, Malvin, NP, Rowen, MN, Saunders, BT, Ma, H, Mack, MR, Hykes, BL, Balce, DR, Orvedahl, A, Williams, JW, Rohatgi, N, Wang, X, McAllaster, MR, Handley, SA, Kim, BS, Doench, JG, Zinselmeyer, BH , Diamond, MS, Virgin, HW, Gelman, AE & Teitelbaum, SL 2021, 'Intercellular Mitochondria Transfer to Macrophages Regulates White Adipose Tissue Homeostasis and Is Impaired in Obesity', Cell metabolism, vol. 33, no. 2, pp. 270-282.e8. https://doi.org/10.1016/j.cmet.2020.11.008

TY - JOUR

T1 - Intercellular Mitochondria Transfer to Macrophages Regulates White Adipose Tissue Homeostasis and Is Impaired in Obesity

AU - Brestoff, Jonathan R.

AU - Wilen, Craig B.

AU - Moley, John R.

AU - Li, Yongjia

AU - Zou, Wei

AU - Malvin, Nicole P.

AU - Rowen, Marina N.

AU - Saunders, Brian T.

AU - Ma, Hongming

AU - Mack, Madison R.

AU - Hykes, Barry L.

AU - Balce, Dale R.

AU - Orvedahl, Anthony

AU - Williams, Jesse W.

AU - Rohatgi, Nidhi

AU - Wang, Xiaoyan

AU - McAllaster, Michael R.

AU - Handley, Scott A.

AU - Kim, Brian S.

AU - Doench, John G.

AU - Zinselmeyer, Bernd H.

AU - Diamond, Michael S.

AU - Virgin, Herbert W.

AU - Gelman, Andrew E.

AU - Teitelbaum, Steven L.

PY - 2021/2/2

Y1 - 2021/2/2

N2 - Brestoff et al. show that adipose-tissue-resident macrophages acquire mitochondria from neighboring adipocytes in a heparan-sulfate-dependent process that is impaired in obesity. Genetic disruption of mitochondria uptake by macrophages reduces energy expenditure and exacerbates diet-induced obesity in mice, indicating that intercellular mitochondria transfer to macrophages mediates systemic metabolic homeostasis.

AB - Brestoff et al. show that adipose-tissue-resident macrophages acquire mitochondria from neighboring adipocytes in a heparan-sulfate-dependent process that is impaired in obesity. Genetic disruption of mitochondria uptake by macrophages reduces energy expenditure and exacerbates diet-induced obesity in mice, indicating that intercellular mitochondria transfer to macrophages mediates systemic metabolic homeostasis.

KW - beige adipose tissue

KW - brown adipose tissue

KW - horizontal mitochondria transfer

KW - immunometabolism

KW - intercellular mitochondria transfer

KW - macrophage

KW - metabolism

KW - mitochondria

KW - obesity

KW - white adipose tissue

UR - http://www.scopus.com/inward/record.url?scp=85097880087&partnerID=8YFLogxK

U2 - 10.1016/j.cmet.2020.11.008

DO - 10.1016/j.cmet.2020.11.008

M3 - Article

C2 - 33278339

AN - SCOPUS:85097880087

SN - 1550-4131

VL - 33

SP - 270-282.e8

JO - Cell metabolism

JF - Cell metabolism

IS - 2

ER -

Intercellular Mitochondria Transfer to Macrophages Regulates White Adipose Tissue Homeostasis and Is Impaired in Obesity

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Keywords

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