Restructuring of the male mice peripheral circadian network after bariatric surgery

in Journal of Endocrinology
Authors:
Anne-Marie Neumann Institute of Neurobiology, University of Lübeck, Lübeck, Germany
Center of Brain, Behavior and Metabolism, University of Lübeck, Lübeck, Germany

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https://orcid.org/0000-0001-5831-0608
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Cathleen Geißler Center of Brain, Behavior and Metabolism, University of Lübeck, Lübeck, Germany
Institute for Human Genetics, Epigenetics and Metabolism Lab, University of Lübeck, Lübeck, Germany

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Violetta Pilorz Institute of Neurobiology, University of Lübeck, Lübeck, Germany
Center of Brain, Behavior and Metabolism, University of Lübeck, Lübeck, Germany

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Iwona Olejniczak Institute of Neurobiology, University of Lübeck, Lübeck, Germany
Center of Brain, Behavior and Metabolism, University of Lübeck, Lübeck, Germany

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Alfor G Lewis Department of Surgery, University of Michigan, Ann Arbor, Michigan, USA

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Randy J Seeley Department of Surgery, University of Michigan, Ann Arbor, Michigan, USA

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Orr Shomroni Transcriptome and Genome Analysis Core Unit, University Medical Center Göttingen, Göttingen, Germany

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Gabriela Salinas-Riester Transcriptome and Genome Analysis Core Unit, University Medical Center Göttingen, Göttingen, Germany

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Henriette Kirchner Center of Brain, Behavior and Metabolism, University of Lübeck, Lübeck, Germany
Institute for Human Genetics, Epigenetics and Metabolism Lab, University of Lübeck, Lübeck, Germany
German Center for Diabetes Research (DZD), Helmholtz Zentrum München, Bayern, Germany

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Henrik Oster Institute of Neurobiology, University of Lübeck, Lübeck, Germany
Center of Brain, Behavior and Metabolism, University of Lübeck, Lübeck, Germany

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Correspondence should be addressed to H Oster: henrik.oster@uni-luebeck.de
DOI:
https://doi.org/10.1530/JOE-20-0611
Volume/Issue:
Volume 250: Issue 2
Article Type:
Research Article
Page Range:
67–79
Online Publication Date:
28 Jun 2021
Copyright:
© Society for Endocrinology 2021
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Bariatric surgery is still the most effective long-term weight-loss therapy. Recent data indicate that surgical outcomes may be affected by diurnal food intake patterns. In this study, we aimed to investigate how surgery-induced metabolic adaptations (i.e. weight loss) interact with circadian clock function. For that reason, vertical sleeve gastrectomy (VSG) was performed in obese mice and rhythms in behavior, tissue rhythmicity, and white adipose tissue transcriptome were evaluated. VSG under constant darkness conditions led to a maximum weight loss of 18% compared to a loss of 3% after sham surgery. Post-surgical weight development was characterized by two distinct intervals of catabolic and subsequent anabolic metabolic state. Locomotor activity was not affected. However, VSG significantly increased active phase meal frequency in the anabolic state. No significant effects on clock gene rhythmicity were detected in adrenal and white adipose tissue (WAT) explant cultures. Transcriptome rhythm analyses of subcutaneous WAT revealed a reduction of cycling genes after VSG (sham: 2493 vs VSG: 1013) independent of sustained rhythms in core clock gene expression. This may be a consequence of weight loss-induced morphological reconstruction of WAT that overwrites the direct influence of the local clock machinery on the transcriptome. However, VSG altered rhythmic transcriptional regulation of WAT lipid metabolism pathways. Thus, our data suggest a reorganization of diurnal metabolic rhythms after VSG downstream of the molecular clock machinery.

Supplementary Materials

    • Suppl. Methods
    • Supplemental Table: Alphabetically ordered list of genes that were detected as rhythmic in VSG or sham animals (JTK_CYCLE p < 0.05) and genes that were detected as significantly up- or downregulated by VSG (p < 0.05).
    • Supplemental Figure 1: (A) Change to minimum weight post-surgery (n = 8/13); unpaired t¬-test: **** p < 0.0001. (B) Weight change under LD; 2-way RM-ANOVA. (C) Meal intake and (D) meal frequency after sham and VSG during CP and AP (n = 5/8); 2-way RM-ANOVA on post-surgical conditions: interaction §§§§ p < 0.0001, § p < 0.05, group effect #### p < 0.0001, # p < 0.05, and Sidak’s post-hoc comparison: **** p < 0.0001.
    • Supplemental Figure 2: Mean daily activity counts in constant darkness normalized by mean daily activity counts in LD12:12 (n = 7/9); 2-way RM-ANOVA on post-surgical conditions, group effect p-value stated.
    • Supplemental Figure 3: (A) Mean meal activity per hour pre-surgery and during (B) CP and (C) AP after sham or VSG surgery; 2-way RM-ANOVA: group effect ## p < 0.01. (D) Meal size in the active and resting phase before surgery (n=13) and during CP and AP after sham or VSG surgery (n = 5/8); mixed effects model on active phases, and Sidak’s post-hoc comparison: *p < 0.05.
    • Supplemental Figure 4: WAT bioluminescence (A) period, (B) phase, and (C) amplitude plotted against the corresponding body weight (BW) change, and (D) mean fold change (FC) of grouped sham-normalized lipogenesis genes (n=36) plotted against corresponding BW change; linear regression with 95 % confidence bands (dotted lines), p-values and squared coefficient of correlation stated.

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Print ISSN:
0022-0795
Online ISSN:
1479-6805
Copyright:
© Society for Endocrinology 2021
Page(s):
13
Article Type:
Research Article
Received Date:
16 May 2021
Accepted Date:
20 May 2021
Print Publication Date:
01 Aug 2021
Online Publication Date:
28 Jun 2021
Keywords:
bariatric surgery; vertical sleeve gastrectomy; circadian clocks; adipose tissue; mouse model

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