. 2023 Apr 11;56(4):783-796.e7.

doi: 10.1016/j.immuni.2023.01.024. Epub 2023 Feb 23.

Monocytes re-enter the bone marrow during fasting and alter the host response to infection

Henrike Janssen¹, Florian Kahles², Dan Liu², Jeffrey Downey¹, Laura L Koekkoek³, Vladimir Roudko⁴, Darwin D'Souza⁴, Cameron S McAlpine¹, Lennard Halle², Wolfram C Poller¹, Christopher T Chan¹, Shun He², John E Mindur², Máté G Kiss¹, Sumnima Singh¹, Atsushi Anzai², Yoshiko Iwamoto², Rainer H Kohler², Kashish Chetal⁵, Ruslan I Sadreyev⁵, Ralph Weissleder⁶, Seunghee Kim-Schulze⁷, Miriam Merad⁸, Matthias Nahrendorf⁹, Filip K Swirski¹⁰

Affiliations

¹ Cardiovascular Research Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA; Center for Systems Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA.
² Center for Systems Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA.
³ Cardiovascular Research Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
⁴ Human Immune Monitoring Center, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
⁵ Department of Molecular Biology and Department of Pathology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA.
⁶ Center for Systems Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA; Department of Radiology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA; Department of Systems Biology, Harvard Medical School, Boston, MA, USA.
⁷ Human Immune Monitoring Center, Icahn School of Medicine at Mount Sinai, New York, NY, USA; Marc and Jennifer Lipschultz Precision Immunology Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
⁸ Cardiovascular Research Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA; Human Immune Monitoring Center, Icahn School of Medicine at Mount Sinai, New York, NY, USA; Marc and Jennifer Lipschultz Precision Immunology Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
⁹ Center for Systems Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA; Department of Radiology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA.
¹⁰ Cardiovascular Research Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA; Center for Systems Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA; Marc and Jennifer Lipschultz Precision Immunology Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA. Electronic address: filip.swirski@mssm.edu.

PMID: 36827982
PMCID: PMC10101885
DOI: 10.1016/j.immuni.2023.01.024

Monocytes re-enter the bone marrow during fasting and alter the host response to infection

Henrike Janssen et al. Immunity. 2023.

. 2023 Apr 11;56(4):783-796.e7.

doi: 10.1016/j.immuni.2023.01.024. Epub 2023 Feb 23.

Authors

Affiliations

¹ Cardiovascular Research Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA; Center for Systems Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA.
² Center for Systems Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA.
³ Cardiovascular Research Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
⁴ Human Immune Monitoring Center, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
⁵ Department of Molecular Biology and Department of Pathology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA.
⁶ Center for Systems Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA; Department of Radiology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA; Department of Systems Biology, Harvard Medical School, Boston, MA, USA.
⁷ Human Immune Monitoring Center, Icahn School of Medicine at Mount Sinai, New York, NY, USA; Marc and Jennifer Lipschultz Precision Immunology Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
⁸ Cardiovascular Research Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA; Human Immune Monitoring Center, Icahn School of Medicine at Mount Sinai, New York, NY, USA; Marc and Jennifer Lipschultz Precision Immunology Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
⁹ Center for Systems Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA; Department of Radiology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA.
¹⁰ Cardiovascular Research Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA; Center for Systems Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA; Marc and Jennifer Lipschultz Precision Immunology Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA. Electronic address: filip.swirski@mssm.edu.

PMID: 36827982
PMCID: PMC10101885
DOI: 10.1016/j.immuni.2023.01.024

Abstract

Diet profoundly influences physiology. Whereas over-nutrition elevates risk for disease via its influence on immunity and metabolism, caloric restriction and fasting appear to be salutogenic. Despite multiple correlations observed between diet and health, the underlying biology remains unclear. Here, we identified a fasting-induced switch in leukocyte migration that prolongs monocyte lifespan and alters susceptibility to disease in mice. We show that fasting during the active phase induced the rapid return of monocytes from the blood to the bone marrow. Monocyte re-entry was orchestrated by hypothalamic-pituitary-adrenal (HPA) axis-dependent release of corticosterone, which augmented the CXCR4 chemokine receptor. Although the marrow is a safe haven for monocytes during nutrient scarcity, re-feeding prompted mobilization culminating in monocytosis of chronologically older and transcriptionally distinct monocytes. These shifts altered response to infection. Our study shows that diet-in particular, a diet's temporal dynamic balance-modulates monocyte lifespan with consequences for adaptation to external stressors.

Keywords: bone marrow; corticosterone; fasting; hematopoiesis; hypothalamus; infection; monocyte.

PubMed Disclaimer

Conflict of interest statement

Declaration of interests M.N. has received funding or material research support from Alnylam, Biotronik, CSL Behring, GlycoMimetics, GSK, Medtronic, Novartis, and Pfizer as well as consulting fees from Lilly, Biogen, Gimv, IFM Therapeutics, Molecular Imaging, Sigilon, and Verseau Therapeutics. F.K.S. has received funds or material research support from Novartis, Partner Therapeutics, Pfizer, and Verseau Therapeutics.

Figures

**Figure 1:. Fasting reorganizes the leukocyte distribution landscape**
A. Relative shifts of major leukocyte populations in depicted organs compared between mice fed ad libitum and after a 24h fast. Baseline cell content in each organ is defined as “5 cells”. Fasted results are calculated in relative relation to fed. Ly-6C^hi monocytes are defined as CD45⁺ CD11b⁺ LIN1(CD19, CD3, NK 1.1, CD90⁻⁾ Ly-6G⁻ CX3CR1⁺ Ly-6C^hi, neutrophils as CD45⁺ CD11b⁺ LIN1⁻ Ly-6G⁺, T cells as CD45⁺ CD11b⁻ LIN1⁺ MHCII⁻, B cells as CD45⁺ CD11b⁻ LIN1⁺ MHCII⁺. Absolute numbers for each organ are depicted in Table 1. (n=3–5 mice per group). Unpaired t test. B. Representative gating strategy of all major leukocyte populations in the blood. C. Absolute blood leukocyte count and blood glucose concentration divided by inactive (light) and active (dark) period compared between mice fed ad libitum or fasted for up to 12h. Orange zeitgeber (ZT) indicates start of the fast (n=3–10 per group). Two-way ANOVA. Data presented as mean ±SEM, *p < 0.05, **p<0.01, ***p < 0.001. Mono: Ly-6C^hi monocytes, Neutro: Neutrophils, WAT: White adipose tissue, BAT: Brown adipose tissue, LP: Lamina propria, LN: Lymph node, AT: Adipose tissue, FI: Fluorescence intensity, ZT: Zeitgeber. Please also see Table 1 and Supplement Table 1.

**Figure 2:. Fasting returns Ly-6C^hi monocytes back from circulation to the bone marrow**
A. Ly-6C^hi monocytes isolated from GFP positive mice were injected intravenously into wild type mice directly prior to initiation of a 24h fast or feeding ad libitum. B. Representative flow cytometry plots of GFP positive monocytes after feeding ad libitum and fasting in the blood. Adoptively transferred monocytes are defined as CD45⁺ GFP⁺. (n=5–6 per group, two independent experiments combined) C. Representative flow cytometry plots of GFP positive monocytes after feeding ad libitum and fasting in the bone marrow (BM). Adoptively transferred monocytes are defined as CD45⁺ GFP⁺. (n=5–6 per group, two independent experiments combined) D. Relative decrease of GFP positive monocytes in the blood and relative increase of GFP positive monocytes in the bone marrow after 24h fasting compared to fed control (n=5–6 per group, two independent experiments combined). Unpaired t test. E. Relative expression of target genes of sorted blood Ly-6C^hi monocytes after 24h fasting normalized to fed control (n=3 mice per group). Unpaired t test. F. Circulating Ly-6C^hi monocytes measured at indicated timepoints in *Cxcr4*^fl/fl *Lyz2*^Cre and *Cxcr4*^fl/fl under fed and fasted conditions (n=4–10, timepoints are independent experiments). Start of the fast is indicated by orange zeitgeber (ZT). Two-way ANOVA. G. Plasma corticosterone (CORT) in *Cxcr4*^fl/fl under fed and fasted conditions at indicated timepoints (n=4–8, timepoints are independent experiments). Start of the fast is indicated by orange zeitgeber (ZT). Two-way ANOVA. H. Relative expression of *Cxcr4* on sorted blood Ly-6C^hi monocytes after incubation with CORT (n=10 mice pooled for sort, n=3 technical replicates per group). Unpaired t test. I. Mice underwent bilateral adrenalectomy (ADX) or sham surgery and were allowed to recover for 2 weeks, prior to submission to feeding ad libitum or a 12h fast. Blood Ly-6C^hi monocytes in mice 2 weeks post ADX or sham surgery after fasting compared to fed ad libitum (n=4–6 per group). Unpaired t test. J. Blood Ly-6C^hi monocytes measured at indicated times in *Nr3c1*^fl/fl *Lyz2*^Cre and *Nr3c1*^fl/fl under fed and fasted conditions (n=4–11, timepoints areindependent experiments). Start of the fast is indicated by orange ZT. Two-way ANOVA. K. Blood Ly-6C^hi monocytes in *Crh*^fl/fl *Sim1*^Cre and *Crh*^fl/fl after 4h of fasting compared to fed ad libitum (n=3–6 per group). Unpaired t test. Data presented as mean ±SEM, *p < 0.05, **p<0.01, ***p < 0.001. FI: Fluorescence intensity, BM: Bone marrow, CORT: Corticosterone, ADX: Adrenalectomy. Please also see Figure S1.

**Figure 3:. Re-feeding leads to a surge of monocytes into the bloodstream**
A. Mice were fasted for 24h and divided into further fasting or re-feeding for 4h. Control mice were fed ad libitum. B. Representative flow cytometry plots of blood Ly-6C^hi monocytes after feeding ad libitum, fasting for 28h or fasting for 24h followed by 4h of re-feeding. Ly-6C^hi monocytes are defined as CD45⁺ CD11b⁺ LIN1⁻ Ly-6G⁻ CX3CR1⁺ Ly-6C^hi (n=4–5 per group). C. Blood Ly-6C^hi monocytes after feeding ad libitum, fasting or fasting+re-feeding (n=4–5 per group). One-way ANOVA. D. Blood glucose concentration after feeding ad libitum, fasting or fasting+re-feeding (n=4–5 per group). One-way ANOVA. E. Plasma corticosterone (CORT) concentration after feeding ad libitum, fasting or fasting+re-feeding (n=4–5 per group). One-way ANOVA F. Ly-6C^hi monocytes sorted from GFP positive mice were injected intravenously into wild type mice directly prior to submission to 28h of fasting or 24h of fasting and 4h of re-feeding. G. Adoptively transferred monocytes in the blood and bone marrow (BM) of wild type recipients. Adoptively transferred monocytes are defined as CD45+ GFP+. (n=5 per group). Unpaired t test. H. Parabiosis of GFP positive and wild type mice. After two weeks, mice were separated and wild type mice were either fasted for 28h or fasted for 24h followed by 4h of re-feeding. I. GFP positive Ly-6C^hi monocytes in the blood and BM of wild type parabionts after fasting or fasting+re-feeding. (n=4 per group). Unpaired t test. J. Blood Ly-6C^hi monocytes in *Cxcr4*^fl/fl *Lyz2*^Cre and *Cxcr4*^fl/fl after feeding ad libitum or fasting+re-feeding (n=5 per group). Unpaired t test. K. Blood Ly-6C^hi monocytes in *Nr3c1*^fl/fl *Lyz2*^Cre and *Nr3c1*^fl/fl after feeding ad libitum or fasting+re-feeding (n=5–6 per group). Unpaired t test. L. Blood Ly-6C^hi monocytes in *Crh*^fl/fl *Sim1*^Cre and *Crh*^fl/fl after feeding ad libitum or fasting+re-feeding (n=4–8 per group). Unpaired t test. Data presented as mean ±SEM, *p < 0.05, **p<0.01, ***p < 0.001. FI: Fluorescence intensity CORT: Corticosterone, BM: Bone marrow. Please also see Figure S2.

**Figure 4:. The monocyte surge is dominated by aged Ly-6C^hi monocytes**
A. EdU and BrdU were sequentially injected for labelling of Ly-6C^hi monocytes under feeding ad libitum, fasting and fasting+re-feeding conditions. EdU was injected 24h prior to fasting. BrdU was injected half-way through the fast. After a 24h fast, fasted mice were divided into groups submitted to a further 4h fast or 4h of re-feeding. B. Representative flow cytometry plots for Ly-6C^hi monocytes in the bone marrow under conditions of feeding ad libitum, fasting and fasting+re-feeding. Ly-6C^hi monocytes are defined as CD45⁺ CD11b⁺ LIN1⁻ Ly-6G⁻ CX3CR1⁺ Ly-6C^hi. “EdU monocytes” are Ly-6C^hi monocytes with EdU-only label (labelled prior to fasting). “BrdU monocytes” are Ly-6C^hi monocytes with BrdU-only label (labelled under fasting). (n=4–5 per group) C. Relative EdU positivity of Ly-6C^hi monocytes and absolute EdU Ly-6C^hi monocyte count under feeding ad libitum, fasting and fasting+re-feeding conditions in the bone marrow. Relative BrdU positivity of Ly-6C^hi monocytes and absolute BrdU Ly-6C^hi monocyte count under feeding ad libitum, fasting and fasting+re-feeding conditions in the bone marrow (n=4–5 per group). One-way ANOVA. D. Representative flow cytometry plots for Ly-6C^hi monocytes in the blood under conditions of feeding ad libitum, fasting and fasting+re-feeding. Ly-6C^hi monocytes are defined as CD45⁺ CD11b⁺ LIN1⁻ Ly-6G⁻ CX3CR1⁺ Ly-6C^hi. “EdU monocytes” are Ly-6C^hi monocytes with EdU-only label (labelled prior to fasting). “BrdU monocytes” are Ly-6C^hi monocytes with BrdU-only label (labelled under fasting). (n=4–5 per group) E. Absolute count of EdU monocytes and BrdU monocytes in the blood under feeding, fasting or fasting+re-feeding conditions (n=4–5 per group). One-way ANOVA. F. Relative quantification of Ly-6C^hi monocyte subpopulations, based on EdU and BrdU label in the blood after feeding or fasting+re-feeding conditions (n=4–5 per group). The surface of the rectangle resembles the size of the whole pool of Ly-6C^hi monocytes in the blood. EdU monocytes can be considered chronologically older (“old”) than BrdU monocytes (“young”) (n=4–5 per group). Chi-square test. Data presented as mean ±SEM, *p < 0.05, **p<0.01, ***p < 0.001. Please also see Figure S3.

**Figure 5:. Fasting and re-feeding generates a chronologically older and transcriptionally distinct monocyte population**
A. Volcano plot indicating differentially regulated genes (FC>1.0, FDR<0.05, p<0.05) of sorted blood Ly-6C^hi monocytes after feeding ad libitum or fasting for 24h followed by 4h re-feeding. (n=3 samples per group, 4 mice pooled per sample). B. Heatmap of differentially expressed genes after conservative hierarchical clustering of sorted blood Ly-6C^hi monocytes after feeding ad libitum or fasting+re-feeding. (n=3 samples per group, 4 mice pooled per sample) C. UMAP representations, colored by clusters computed by FindClusters function of Seurat and relative representation of the clusters of sorted blood Ly-6C^hi monocytes under fed and fasting+re-fed conditions. (n=1 sample per group, 5 mice pooled per sample) D. Expression of Top 3 defining marker genes of cluster 0 visualized by feature plots. E. Plasma Chi3l3 in *Nr3c1*^fl/fl and *Nr3c1*^fl/fl *Lyz2*^Cre under feeding ad libitum or fasting conditions. Orange zeitgeber (ZT) indicates start of the fast (n=4–12, timepoints are independent experiments). Two-way ANOVA. F. Pseudotime computed with Monocle 3. The white circled 1 indicates the root cell from where pseudotime analaysis begins. Gray circles correspond to the different outcomes in the trajectory. UMAP representation overlaying conditions of feeding ad libitum and fasting+re-feeding. G. Pseudotime of trajectories 5, 6 and 7 projecting into cluster 0 in mice under feeding ad libitum and fasting+re-feeding. Kolmogorov-Smirnov test. Data presented as mean ±SEM, *p < 0.05, **p<0.01, ***p < 0.001. ZT: zeitgeber. Please also see Figure S4.

**Figure 6. Fasting and re-feeding alters host response to infection**
A. EdU and BrdU were sequentially injected for labelling of Ly-6C^hi monocytes in mice under feeding ad libitum and fasting+re-feeding conditions. EdU was injected 24h prior to fasting. BrdU was injected half-way through the fast. After a 24h fast, fasted mice were refed for 4h. LPS (20μg/mouse) was administered intranasally at the timepoint of re-feeding and mice sacrificed 4h later. B. Representative flow cytometry plots for double labelling of Ly-6C^hi monocytes in the lung parenchyma. Intravascular Ly-6C^hi monocytes were excluded by intravenous CD45 staining prior to sacrifice. Ly-6C^hi monocytes are defined as CD45⁺ CD11b⁺ LIN1⁻ Ly-6G⁻ CX3CR1⁺ MHCII⁻ Ly-6C^hi. EdU monocytes are Ly-6C^hi monocytes with EdU-only label (labelled prior to fasting, old). BrdU monocytes are Ly-6C^hi monocytes with BrdU-only label (labelled under fasting, young). (n=3 per group) C. Absolute count of Ly-6C^hi monocytes and TNFα-positive Ly-6C^hi monocytes in the parenchyma after intranasal LPS challenge in mice undergoing feeding ad libitum or fasting+re-feeding. Absolute counts of “old” and “young” Ly-6C^hi monocytes in the parenychma. “Old” are Ly-6C^hi monocytes with EdU-only label. “Young” are Ly-6C^hi monocytes with BrdU-only label (n=3 per group). Unpaired t test. D. Blood Ly-6C^hi monocytes under feeding or fasting+re-feeding conditions followed for 24h after re-feeding normalized to group’s baseline before fasting. Orange −24h indicates baseline before start of a 24h fast. Blue 0 indicates start of re-feeding. Bar graphs represent absolute Ly-6C^hi monocytes counts of indicated timepoints (n=4–5 per group, timepoints are independent experiments). Two-way ANOVA. E. Blood glucose under feeding or fasting+re-feeding conditions followed for 24h after re-feeding. Orange −24h indicates baseline before start of a 24h fast. Blue 0 indicates start of re-feeding (n=4–5 per group, timepoints are independent experiments). Two-way ANOVA. F. Plasma corticosterone (CORT) under under feeding or fasting+re-feeding conditions followed for 24h after re-feeding. Orange −24h indicates baseline before start of a 24h fast. Blue 0 indicates start of re-feeding (n=4–5 per group, timepoints are independent experiments). Two-way ANOVA. G. Plasma Chi3l3 concentration under feeding or fasting+re-feeding conditions followed for 24h after re-feeding. Orange −24h indicates baseline before start of a 24h fast. Blue 0 indicates start of re-feeding (n=4–5 per group, timepoints are independent experiments). Two-way ANOVA. H. Mice were infected intranasally with Pseudomonas aeruginosa (PAE) at a dose of 5×10⁷/mouse. Refed mice were infected after a 24h fast, followed by a 4h re-feeding period. Control mice were fed ad libitum and both groups followed for survival (n= 22–23 per group, two independent experiments combined). Log-rank (Mantel-Cox) test. I. Fed ad libitum mice and mice after 24h fast followed by 4h of re-feeding were intranasally infected with PAE at a dose of 5×10⁷/mouse and sacrificed 12h after. J. To distinguish between circulating and parenchymal leukocytes, CD45 was injected i.v. before sacrifice. Representative gating strategy for flow cytometery on parenchymal Ly-6C^hi monocytes defined as CD45⁺CD11c⁻CD11b⁺Ly6G⁻Ly-6C^hi MHCII⁻ and macrophages (Mφ) defined as CD45⁺CD11c⁻CD11b⁺Ly6G⁻MHCII⁺CD64⁺ in the lung. (n=7 per group) K. Parenchymal myeloid cell content in the lung after infection with PAE as described in panel I (n=7 per group). Unpaired t test. L. Bacterial load after infection as described in panel I from homogenized lungs comparing fed and fasted+re-fed mice (n=6–8 per group). Unpaired t test. M. Plasma concentration of cytokines after infection as described in panel I (n=13–15 per group, two experiments combined). Unpaired t test. Data presented as mean ±SEM, *p < 0.05, **p<0.01, ***p < 0.001. FI: Fluorescence intensity, RF: Re-feeding, PAE: Pseudomonas aeruginosa, Mφ: Macrophages. Please also see Figure S5 and S6.

See this image and copyright information in PMC

Comment in

Fasting affects monocyte lifespan and migration.
Flemming A. Flemming A. Nat Rev Immunol. 2023 Apr;23(4):203. doi: 10.1038/s41577-023-00863-z. Nat Rev Immunol. 2023. PMID: 36918664 No abstract available.
Old and "hangry" monocytes turn from friend to foe under assault.
O'Brien CJO, Domingos AI. O'Brien CJO, et al. Immunity. 2023 Apr 11;56(4):747-749. doi: 10.1016/j.immuni.2023.03.013. Immunity. 2023. PMID: 37044065
Energy saver: Monocytes hibernate in bone marrow upon fasting.
Tuckermann J, Fischer-Posovszky P. Tuckermann J, et al. Cell Metab. 2023 May 2;35(5):734-736. doi: 10.1016/j.cmet.2023.04.008. Cell Metab. 2023. PMID: 37137288
The immune hunger games: the effects of fasting on monocytes.
Domínguez-Andrés J, Reinecke H, Sohrabi Y. Domínguez-Andrés J, et al. Cell Mol Immunol. 2023 Oct;20(10):1098-1100. doi: 10.1038/s41423-023-01033-w. Epub 2023 May 10. Cell Mol Immunol. 2023. PMID: 37165013 Free PMC article. No abstract available.

References

1. Dehghan M et al. (2017). Associations of fats and carbohydrate intake with cardiovascular disease and mortality in 18 countries from five continents (PURE): a prospective cohort study. Lancet 390, 2050–2062. - PubMed
1. Flegal KM, Kit BK, Orpana H, and Graubard BI (2013). Association of all-cause mortality with overweight and obesity using standard body mass index categories: a systematic review and meta-analysis. JAMA 309, 71–82. - PMC - PubMed
1. Yang Q, Zhang Z, Gregg EW, Flanders WD, Merritt R, and Hu FB (2014). Added sugar intake and cardiovascular diseases mortality among US adults. JAMA Intern Med 174, 516–524. - PMC - PubMed
1. Lumeng CN, and Saltiel AR (2011). Inflammatory links between obesity and metabolic disease. J Clin Invest 121, 2111–2117. - PMC - PubMed
1. Ma T et al. (2011). Sucrose counteracts the anti-inflammatory effect of fish oil in adipose tissue and increases obesity development in mice. PLoS One 6, e21647. - PMC - PubMed

Publication types

Actions
Actions

MeSH terms

Actions
Actions
Actions
Actions
Actions
Actions
Actions

Substances

Actions

Grants and funding

LinkOut - more resources

Full Text Sources
Other Literature Sources
- The Lens - Patent Citations Database
Molecular Biology Databases
- Mouse Genome Informatics (MGI)
- NIAID Data Ecosystem - Find datasets on Infectious and Immune-mediated Diseases

Save citation to file

Email citation

Add to Collections

Add to My Bibliography

Your saved search

Create a file for external citation management software

Your RSS Feed

Monocytes re-enter the bone marrow during fasting and alter the host response to infection

Affiliations

Monocytes re-enter the bone marrow during fasting and alter the host response to infection

Authors

Affiliations

Abstract

Conflict of interest statement

Figures

Comment in

References

Publication types

MeSH terms

Substances

Grants and funding

LinkOut - more resources

Full Text Sources

Other Literature Sources

Molecular Biology Databases