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 journalArticle

8 Citations (Scopus)

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 languageEnglish (US)
Pages (from-to)1102-1114.e17
JournalCell
Volume178
Issue number5
DOIs
StatePublished - Aug 22 2019

Fingerprint

Monocytes
Tissue
Peroxisome Proliferators
Energy Intake
AMP-Activated Protein Kinases
Sensors
Fasting
Liver
Bone
Inflammation
Repair
Blood
Caloric Restriction
Chemical activation
Dietary Proteins
Glucose
Feeding Behavior
Autoimmune Diseases
Hepatocytes
Emergencies

Keywords

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

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)

Cite this

Jordan, S., Tung, N., Casanova-Acebes, M., Chang, C., Cantoni, C., Zhang, D., ... 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

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

In: Cell, Vol. 178, No. 5, 22.08.2019, p. 1102-1114.e17.

Research output: Contribution to journalArticle

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
Jordan S, Tung N, Casanova-Acebes M, Chang C, Cantoni C, Zhang D et al. Dietary Intake Regulates the Circulating Inflammatory Monocyte Pool. Cell. 2019 Aug 22;178(5):1102-1114.e17. https://doi.org/10.1016/j.cell.2019.07.050
Jordan, Stefan ; Tung, Navpreet ; Casanova-Acebes, M. ; Chang, Christie ; Cantoni, Claudia ; Zhang, Dachuan ; Wirtz, Theresa H. ; Naik, Shruti ; Rose, Samuel A. ; Brocker, Chad N. ; Gainullina, Anastasiia ; Hornburg, Daniel ; Horng, Sam ; Maier, Barbara B. ; Cravedi, P. ; LeRoith, D. ; Gonzalez, Frank J. ; Meissner, F. ; Ochando, J. ; Rahman, A. ; Chipuk, Jerry E. ; Artyomov, Maxim N. ; Frenette, Paul S. ; Piccio, L. ; Berres, Marie Luise ; Gallagher, Emily J. ; Merad, Miriam. / Dietary Intake Regulates the Circulating Inflammatory Monocyte Pool. In: Cell. 2019 ; Vol. 178, No. 5. pp. 1102-1114.e17.
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