Starvation-induced changes in somatic insulin/IGF-1R signaling drive metabolic programming across generations

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Abstract

Exposure to adverse nutritional and metabolic environments during critical periods of development can exert long-lasting effects on health outcomes of an individual and its descendants. Although such metabolic programming has been observed in multiple species and in response to distinct nutritional stressors, conclusive insights into signaling pathways and mechanisms responsible for initiating, mediating, and manifesting changes to metabolism and behavior across generations remain scarce. By using a starvation paradigm in Caenorhabditis elegans, we show that starvation-induced changes in dauer formation-16/forkhead box transcription factor class O (DAF-16/FoxO) activity, the main downstream target of insulin/insulin-like growth factor 1 (IGF-1) receptor signaling, are responsible for metabolic programming phenotypes. Tissue-specific depletion of DAF-16/FoxO during distinct developmental time points demonstrates that DAF-16/FoxO acts in somatic tissues, but not directly in the germline, to both initiate and manifest metabolic programming. In conclusion, our study deciphers multifaceted and critical roles of highly conserved insulin/IGF-1 receptor signaling in determining health outcomes and behavior across generations.

Abstract

Diet-induced changes in somatic insulin signaling mediate adverse physiological and behavioral outcomes in subsequent generations.

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Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2

Michael Love, Wolfgang Huber, Simon Anders (2014)

In comparative high-throughput sequencing assays, a fundamental task is the analysis of count data, such as read counts per gene in RNA-seq, for evidence of systematic changes across experimental conditions. Small replicate numbers, discreteness, large dynamic range and the presence of outliers require a suitable statistical approach. We present DESeq2, a method for differential analysis of count data, using shrinkage estimation for dispersions and fold changes to improve stability and interpretability of estimates. This enables a more quantitative analysis focused on the strength rather than the mere presence of differential expression. The DESeq2 package is available at http://www.bioconductor.org/packages/release/bioc/html/DESeq2.html. Electronic supplementary material The online version of this article (doi:10.1186/s13059-014-0550-8) contains supplementary material, which is available to authorized users.

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featureCounts: an efficient general purpose program for assigning sequence reads to genomic features.

Y. Liao, G K Smyth, W Shi (2014)

Next-generation sequencing technologies generate millions of short sequence reads, which are usually aligned to a reference genome. In many applications, the key information required for downstream analysis is the number of reads mapping to each genomic feature, for example to each exon or each gene. The process of counting reads is called read summarization. Read summarization is required for a great variety of genomic analyses but has so far received relatively little attention in the literature. We present featureCounts, a read summarization program suitable for counting reads generated from either RNA or genomic DNA sequencing experiments. featureCounts implements highly efficient chromosome hashing and feature blocking techniques. It is considerably faster than existing methods (by an order of magnitude for gene-level summarization) and requires far less computer memory. It works with either single or paired-end reads and provides a wide range of options appropriate for different sequencing applications. featureCounts is available under GNU General Public License as part of the Subread (http://subread.sourceforge.net) or Rsubread (http://www.bioconductor.org) software packages.

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Health Effects of Overweight and Obesity in 195 Countries over 25 Years.

Ashkan Afshin, Mohammad Forouzanfar, Marissa Reitsma … (2018)

Background While the rising pandemic of obesity has received significant attention in many countries, the effect of this attention on trends and the disease burden of obesity remains uncertain. Methods We analyzed data from 67.8 million individuals to assess the trends in obesity and overweight prevalence among children and adults between 1980 and 2015. Using the Global Burden of Disease study data and methods, we also quantified the burden of disease related to high body mass index (BMI), by age, sex, cause, and BMI level in 195 countries between 1990 and 2015. Results In 2015, obesity affected 107.7 million (98.7-118.4) children and 603.7 million (588.2- 619.8) adults worldwide. Obesity prevalence has doubled since 1980 in more than 70 countries and continuously increased in most other countries. Although the prevalence of obesity among children has been lower than adults, the rate of increase in childhood obesity in many countries was greater than the rate of increase in adult obesity. High BMI accounted for 4.0 million (2.7- 5.3) deaths globally, nearly 40% of which occurred among non-obese. More than two-thirds of deaths related to high BMI were due to cardiovascular disease. The disease burden of high BMI has increased since 1990; however, the rate of this increase has been attenuated due to decreases in underlying cardiovascular disease death rates. Conclusions The rapid increase in prevalence and disease burden of elevated BMI highlights the need for continued focus on surveillance of BMI and identification, implementation, and evaluation of evidence-based interventions to address this problem.

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Contributors

Merly C. Vogt:

ORCID: https://orcid.org/0000-0002-1738-7155

Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

Oliver Hobert:

ORCID: https://orcid.org/0000-0002-7634-2854

Role: ConceptualizationRole: Funding acquisitionRole: Project administrationRole: SupervisionRole: Writing - review & editing

Journal

Journal ID (nlm-ta): Sci Adv

Journal ID (iso-abbrev): Sci Adv

Journal ID (publisher-id): sciadv

Journal ID (hwp): advances

Title: Science Advances

Publisher: American Association for the Advancement of Science

ISSN (Electronic): 2375-2548

Publication date Collection: April 2023

Publication date (Electronic, pub): 07 April 2023

Volume: 9

Issue: 14

Electronic Location Identifier: eade1817

Affiliations

[1]Department of Biological Sciences, Howard Hughes Medical Institute, Columbia University, New York, NY 10027, USA.

Author notes

[* ]Corresponding author. Email: merly.vogt@ 123456helmholtz-munich.de

[†]

Present address: Helmholtz Diabetes Center, Institute for Diabetes and Cancer, Neuherberg 85764, Germany.

Author information

Merly C. Vogt https://orcid.org/0000-0002-1738-7155

Oliver Hobert https://orcid.org/0000-0002-7634-2854

Article

Publisher ID: ade1817

DOI: 10.1126/sciadv.ade1817

PMC ID: 10081852

PubMed ID: 37027477

SO-VID: 10656798-5602-440c-8b5a-17c34f4a4f00

Copyright © Copyright © 2023 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution License 4.0 (CC BY).

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution license, which permits which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

History

Date received : 30 July 2022

Date accepted : 08 March 2023

Funding

Funded by: FundRef http://dx.doi.org/10.13039/100000011, Howard Hughes Medical Institute;

Award ID: N/A

Funded by: FundRef http://dx.doi.org/10.13039/501100000854, Human Frontier Science Program;

Award ID: LT000175/2016-L

Funded by: FundRef http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;

Award ID: VO 2159/1-1

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Starvation-induced changes in somatic insulin/IGF-1R signaling drive metabolic programming across generations

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Most cited references 104

Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2

featureCounts: an efficient general purpose program for assigning sequence reads to genomic features.

Health Effects of Overweight and Obesity in 195 Countries over 25 Years.

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