Partial Sleep Restriction Activates Immune Response-Related Gene Expression Pathways: Experimental and Epidemiological Studies in Humans
Open accessAbstract
Epidemiological studies have shown that short or insufficient sleep is associated with increased risk for metabolic diseases and mortality. To elucidate mechanisms behind this connection, we aimed to identify genes and pathways affected by experimentally induced, partial sleep restriction and to verify their connection to insufficient sleep at population level. The experimental design simulated sleep restriction during a working week: sleep of healthy men (N = 9) was restricted to 4 h/night for five nights. The control subjects (N = 4) spent 8 h/night in bed. Leukocyte RNA expression was analyzed at baseline, after sleep restriction, and after recovery using whole genome microarrays complemented with pathway and transcription factor analysis. Expression levels of the ten most up-regulated and ten most down-regulated transcripts were correlated with subjective assessment of insufficient sleep in a population cohort (N = 472). Experimental sleep restriction altered the expression of 117 genes. Eight of the 25 most up-regulated transcripts were related to immune function. Accordingly, fifteen of the 25 most up-regulated Gene Ontology pathways were also related to immune function, including those for B cell activation, interleukin 8 production, and NF-κB signaling (P<0.005). Of the ten most up-regulated genes, expression of STX16 correlated negatively with self-reported insufficient sleep in a population sample, while three other genes showed tendency for positive correlation. Of the ten most down-regulated genes, TBX21 and LGR6 correlated negatively and TGFBR3 positively with insufficient sleep. Partial sleep restriction affects the regulation of signaling pathways related to the immune system. Some of these changes appear to be long-lasting and may at least partly explain how prolonged sleep restriction can contribute to inflammation-associated pathological states, such as cardiometabolic diseases.
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The low LDL concentration in the SR may have been induced by the inflammation, particularly by the activation of the acute phase response, induced by the sleep restriction.
“The low LDL concentration in the SR may have been induced by the inflammation, particularly by the activation of the acute phase response, induced by the sleep restriction5.”
From Prolonged sleep restriction induces changes in pathways involved in cholesterol metabolism and inflammatory responses (2016) · cites this paper as [5]
The GO cluster 5 ('Lipid cluster', P = 0.045) included 4/5 of the top pathways that were enriched among down-regulated genes in the SR study (permuted P < 0.001).
“The GO cluster 5 (“Lipid cluster”, P = 0.045, Supplementary Table S2 and Supplementary Fig. S2) included 4/5 of the top pathways that were enriched among down-regulated genes in the SR study (permuted P < 0.001) reported previously (Table 1)5.”
From Prolonged sleep restriction induces changes in pathways involved in cholesterol metabolism and inflammatory responses (2016) · cites this paper as [5]
Lipid-related pathways were enriched among transcripts down-regulated after 5 nights of experimental SR.
“Lipid-related pathways were enriched among transcripts down-regulated after 5 nights of experimental SR5.”
From Prolonged sleep restriction induces changes in pathways involved in cholesterol metabolism and inflammatory responses (2016) · cites this paper as [5]
The gene coding for TLR4 was up-regulated in our 5 nights' SR protocol.
“We have earlier shown that the gene coding for TLR4 was up-regulated in our 5 nights’ SR protocol5.”
From Prolonged sleep restriction induces changes in pathways involved in cholesterol metabolism and inflammatory responses (2016) · cites this paper as [5]
At gene expression level, the activation included increases in expression of toll-like receptors, NF-kB signalling pathway and interleukin-8 production pathways.
“At gene expression level, the activation included increases in expression of toll-like receptors, NF-kB signalling pathway and interleukin-8 production pathways5.”
From Prolonged sleep restriction induces changes in pathways involved in cholesterol metabolism and inflammatory responses (2016) · cites this paper as [5]
Partial sleep restriction for 4 hours in bed per night for 5-7 days activated several gene pathways, notably those involved in the stress response and apoptosis, as measured by gene microarray.
“Partial sleep restriction for 4 hours in bed per night for 5–7 days activated several gene pathways, notably those that were involved in the stress response and apoptosis, as measured by gene microarray [94, 95].”
From Association between sleep deficiency and cardiometabolic disease: implications for health disparities (2016) · cites this paper as [94]
Partial sleep restriction to 4 h for 5 nights leads to changes in leukocyte RNA expression.
“Moreover, partial sleep restriction to 4 h for 5 nights compared to a control group who slept 8 h/night led to changes in leukocyte RNA expression assessed by whole genome microarrays complemented with pathways and transcription factors analysis [44].”
From Metabolic effects of sleep disruption, links to obesity and diabetes (2014) · cites this paper as [44]
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Working hours and health - 2014
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- Authors
- Aho, V., Ollila, H. M., Rantanen, V., Kronholm, E., Surakka, I., van Leeuwen, W. M. A., Lehto, M., Matikainen, S., Ripatti, S., Härmä, M., Sallinen, M., Salomaa, V., Jauhiainen, M., Alenius, H., Paunio, T., & Porkka-Heiskanen, T.
- Affiliations
- University of Helsinki (FI)
- Finnish Institute for Health and Welfare (FI)
- Finnish Institute of Occupational Health (FI)
- Wellcome Sanger Institute (GB)
- Helsinki University Hospital (FI)
- ORCID
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2013-10-23
- Volume
- 8
- Issue
- 10
- Pages
- e77184
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3806729
- OpenAlex
- W2013913648
- Cited by
- 93
- References
- 73
- Citations by year
- 2026: 3 · 2025: 6 · 2024: 5 · 2023: 9 · 2022: 10 · 2021: 7 · 2020: 13 · 2019: 6 · 2018: 1 · 2017: 8 · 2016: 10 · 2015: 8 · 2014: 6 · 2013: 1
- FWCI
- 4.55
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, other-oa)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Jyväskylä University Digital Archive (University of Jyväskylä) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Työväentutkimus Vuosikirja (submittedVersion)
- STM:n Hallinnonalan avoin julkaisuarkisto (Julkari) (submittedVersion)
- Funders
- Foundation for Cardiovascular Research
- Jalmari ja Rauha Ahokkaan Säätiö
- Academy of Finland (129680, 137575, 129494, 213506 and 129680, #213506, 139635, 251217)
- Työsuojelurahasto
- Biomedicum Helsinki-säätiö
- Emil Aaltosen Säätiö
- Sydäntutkimussäätiö
- Paavo Nurmen Säätiö
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and Work-Related Fatigue
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Keywords
- sleep restriction, insufficient sleep, immune response, gene expression, leukocyte transcriptome, NF-κB signaling, interleukin-8, B cell activation, TBX21, LGR6, TGFBR3, inflammation, cardiometabolic disease, sleep duration
- MeSH terms
- T-bet Transcription Factor, Adult, Gene Expression Regulation, Humans, Leukocytes, Male, Proteoglycans, RNA, Sleep Deprivation, NF-kappa B, Receptors, Transforming Growth Factor beta, T-Box Domain Proteins, Gene Expression Profiling, Receptors, G-Protein-Coupled, Microarray Analysis, STAT1 Transcription Factor, Syntaxin 16
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