Dietary Intake Regulates the Circulating Inflammatory Monocyte Pool

Stefan Jordan; Navpreet Tung; M. Casanova-Acebes; Christie Chang; Claudia Cantoni; Dachuan Zhang; Theresa H. Wirtz; Shruti Naik; Samuel A. Rose; Chad N. Brocker; Anastasiia Gainullina; Daniel Hornburg; Sam Horng; Barbara B. Maier; P. Cravedi; D. LeRoith; Frank J. Gonzalez; F. Meissner; J. Ochando; A. Rahman; Jerry E. Chipuk; Maxim N. Artyomov; Paul S. Frenette; L. Piccio; Marie Luise Berres; Emily J. Gallagher; Miriam Merad

doi:10.1016/j.cell.2019.07.050

Dietary Intake Regulates the Circulating Inflammatory Monocyte Pool

Stefan Jordan, Navpreet Tung, M. Casanova-Acebes, Christie Chang, Claudia Cantoni, Dachuan Zhang, Theresa H. Wirtz, Shruti Naik, Samuel A. Rose, Chad N. Brocker, Anastasiia Gainullina, Daniel Hornburg, Sam Horng, Barbara B. Maier, P. Cravedi, D. LeRoith, Frank J. Gonzalez, F. Meissner, J. Ochando, A. RahmanJerry E. Chipuk, Maxim N. Artyomov, Paul S. Frenette, L. Piccio, Marie Luise Berres, Emily J. Gallagher, Miriam Merad

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

237 Scopus citations

Abstract

Caloric restriction is known to improve inflammatory and autoimmune diseases. However, the mechanisms by which reduced caloric intake modulates inflammation are poorly understood. Here we show that short-term fasting reduced monocyte metabolic and inflammatory activity and drastically reduced the number of circulating monocytes. Regulation of peripheral monocyte numbers was dependent on dietary glucose and protein levels. Specifically, we found that activation of the low-energy sensor 5′-AMP-activated protein kinase (AMPK) in hepatocytes and suppression of systemic CCL2 production by peroxisome proliferator-activator receptor alpha (PPARα) reduced monocyte mobilization from the bone marrow. Importantly, we show that fasting improves chronic inflammatory diseases without compromising monocyte emergency mobilization during acute infectious inflammation and tissue repair. These results reveal that caloric intake and liver energy sensors dictate the blood and tissue immune tone and link dietary habits to inflammatory disease outcome.

Original language	English (US)
Pages (from-to)	1102-1114.e17
Journal	Cell
Volume	178
Issue number	5
DOIs	https://doi.org/10.1016/j.cell.2019.07.050
State	Published - Aug 22 2019

Keywords

AMPK
CCL2
Caloric restriction
PPARα
fasting
inflammation
inflammatory disease
liver
metabolism
monocyte

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology

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Jordan, S., Tung, N., Casanova-Acebes, M., Chang, C., Cantoni, C., Zhang, D., Wirtz, T. H., Naik, S., Rose, S. A., Brocker, C. N., Gainullina, A., Hornburg, D., Horng, S., Maier, B. B., Cravedi, P., LeRoith, D., Gonzalez, F. J., Meissner, F., Ochando, J., ... Merad, M. (2019). Dietary Intake Regulates the Circulating Inflammatory Monocyte Pool. Cell, 178(5), 1102-1114.e17. https://doi.org/10.1016/j.cell.2019.07.050

Jordan, S, Tung, N, Casanova-Acebes, M, Chang, C, Cantoni, C, Zhang, D, Wirtz, TH, Naik, S, Rose, SA, Brocker, CN, Gainullina, A, Hornburg, D, Horng, S, Maier, BB, Cravedi, P, LeRoith, D, Gonzalez, FJ, Meissner, F, Ochando, J, Rahman, A, Chipuk, JE, Artyomov, MN, Frenette, PS, Piccio, L, Berres, ML, Gallagher, EJ & Merad, M 2019, 'Dietary Intake Regulates the Circulating Inflammatory Monocyte Pool', Cell, vol. 178, no. 5, pp. 1102-1114.e17. https://doi.org/10.1016/j.cell.2019.07.050

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title = "Dietary Intake Regulates the Circulating Inflammatory Monocyte Pool",

abstract = "Caloric restriction is known to improve inflammatory and autoimmune diseases. However, the mechanisms by which reduced caloric intake modulates inflammation are poorly understood. Here we show that short-term fasting reduced monocyte metabolic and inflammatory activity and drastically reduced the number of circulating monocytes. Regulation of peripheral monocyte numbers was dependent on dietary glucose and protein levels. Specifically, we found that activation of the low-energy sensor 5′-AMP-activated protein kinase (AMPK) in hepatocytes and suppression of systemic CCL2 production by peroxisome proliferator-activator receptor alpha (PPARα) reduced monocyte mobilization from the bone marrow. Importantly, we show that fasting improves chronic inflammatory diseases without compromising monocyte emergency mobilization during acute infectious inflammation and tissue repair. These results reveal that caloric intake and liver energy sensors dictate the blood and tissue immune tone and link dietary habits to inflammatory disease outcome.",

keywords = "AMPK, CCL2, Caloric restriction, PPARα, fasting, inflammation, inflammatory disease, liver, metabolism, monocyte",

author = "Stefan Jordan and Navpreet Tung and M. Casanova-Acebes and Christie Chang and Claudia Cantoni and Dachuan Zhang and Wirtz, {Theresa H.} and Shruti Naik and Rose, {Samuel A.} and Brocker, {Chad N.} and Anastasiia Gainullina and Daniel Hornburg and Sam Horng and Maier, {Barbara B.} and P. Cravedi and D. LeRoith and Gonzalez, {Frank J.} and F. Meissner and J. Ochando and A. Rahman and Chipuk, {Jerry E.} and Artyomov, {Maxim N.} and Frenette, {Paul S.} and L. Piccio and Berres, {Marie Luise} and Gallagher, {Emily J.} and Miriam Merad",

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doi = "10.1016/j.cell.2019.07.050",

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AU - Jordan, Stefan

AU - Tung, Navpreet

AU - Casanova-Acebes, M.

AU - Chang, Christie

AU - Cantoni, Claudia

AU - Zhang, Dachuan

AU - Wirtz, Theresa H.

AU - Naik, Shruti

AU - Rose, Samuel A.

AU - Brocker, Chad N.

AU - Gainullina, Anastasiia

AU - Hornburg, Daniel

AU - Horng, Sam

AU - Maier, Barbara B.

AU - Cravedi, P.

AU - LeRoith, D.

AU - Gonzalez, Frank J.

AU - Meissner, F.

AU - Ochando, J.

AU - Rahman, A.

AU - Chipuk, Jerry E.

AU - Artyomov, Maxim N.

AU - Frenette, Paul S.

AU - Piccio, L.

AU - Berres, Marie Luise

AU - Gallagher, Emily J.

AU - Merad, Miriam

PY - 2019/8/22

Y1 - 2019/8/22

N2 - Caloric restriction is known to improve inflammatory and autoimmune diseases. However, the mechanisms by which reduced caloric intake modulates inflammation are poorly understood. Here we show that short-term fasting reduced monocyte metabolic and inflammatory activity and drastically reduced the number of circulating monocytes. Regulation of peripheral monocyte numbers was dependent on dietary glucose and protein levels. Specifically, we found that activation of the low-energy sensor 5′-AMP-activated protein kinase (AMPK) in hepatocytes and suppression of systemic CCL2 production by peroxisome proliferator-activator receptor alpha (PPARα) reduced monocyte mobilization from the bone marrow. Importantly, we show that fasting improves chronic inflammatory diseases without compromising monocyte emergency mobilization during acute infectious inflammation and tissue repair. These results reveal that caloric intake and liver energy sensors dictate the blood and tissue immune tone and link dietary habits to inflammatory disease outcome.

AB - Caloric restriction is known to improve inflammatory and autoimmune diseases. However, the mechanisms by which reduced caloric intake modulates inflammation are poorly understood. Here we show that short-term fasting reduced monocyte metabolic and inflammatory activity and drastically reduced the number of circulating monocytes. Regulation of peripheral monocyte numbers was dependent on dietary glucose and protein levels. Specifically, we found that activation of the low-energy sensor 5′-AMP-activated protein kinase (AMPK) in hepatocytes and suppression of systemic CCL2 production by peroxisome proliferator-activator receptor alpha (PPARα) reduced monocyte mobilization from the bone marrow. Importantly, we show that fasting improves chronic inflammatory diseases without compromising monocyte emergency mobilization during acute infectious inflammation and tissue repair. These results reveal that caloric intake and liver energy sensors dictate the blood and tissue immune tone and link dietary habits to inflammatory disease outcome.

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KW - Caloric restriction

KW - PPARα

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KW - inflammation

KW - inflammatory disease

KW - liver

KW - metabolism

KW - monocyte

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Dietary Intake Regulates the Circulating Inflammatory Monocyte Pool

Abstract

Keywords

ASJC Scopus subject areas

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