Claudio Costantini, Stefano Brancorsini, Francesco Grignani, Luigina Romani, Marina Maria Bellet
{"title":"Circadian metabolic adaptations to infections.","authors":"Claudio Costantini, Stefano Brancorsini, Francesco Grignani, Luigina Romani, Marina Maria Bellet","doi":"10.1098/rstb.2023.0473","DOIUrl":"10.1098/rstb.2023.0473","url":null,"abstract":"<p><p>Circadian clocks are biological oscillators that evolved to coordinate rhythms in behaviour and physiology around the 24-hour day. In mammalian tissues, circadian rhythms and metabolism are highly intertwined. The clock machinery controls rhythmic levels of circulating hormones and metabolites, as well as rate-limiting enzymes catalysing biosynthesis or degradation of macromolecules in metabolic tissues, such control being exerted both at the transcriptional and post-transcriptional level. During infections, major metabolic adaptation occurs in mammalian hosts, at the level of both the single immune cell and the whole organism. Under these circumstances, the rhythmic metabolic needs of the host intersect with those of two other players: the pathogen and the microbiota. These three components cooperate or compete to meet their own metabolic demands across the 24 hours. Here, we review findings describing the circadian regulation of the host response to infection, the circadian metabolic adaptations occurring during host-microbiota-pathogen interactions and how such regulation can influence the immune response of the host and, ultimately, its own survival.This article is part of the Theo Murphy meeting issue 'Circadian rhythms in infection and immunity'.</p>","PeriodicalId":19872,"journal":{"name":"Philosophical Transactions of the Royal Society B: Biological Sciences","volume":"380 1918","pages":"20230473"},"PeriodicalIF":5.4,"publicationDate":"2025-01-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11753887/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143024259","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Christine T Major-Styles, Jack Munns, Aiwei Zeng, Michael Vanden Oever, John S O'Neill, Rachel S Edgar
{"title":"Chronic CRYPTOCHROME deficiency enhances cell-intrinsic antiviral defences.","authors":"Christine T Major-Styles, Jack Munns, Aiwei Zeng, Michael Vanden Oever, John S O'Neill, Rachel S Edgar","doi":"10.1098/rstb.2023.0344","DOIUrl":"10.1098/rstb.2023.0344","url":null,"abstract":"<p><p>The within-host environment changes over circadian time and influences the replication and severity of viruses. Genetic knockout of the circadian transcription factors CRYPTOCHROME 1 and CRYPTOCHROME 2 (<i>CRY1</i><sup>-/-</sup>/<i>CRY2</i><sup>-/-</sup>; CKO) leads to altered protein homeostasis and chronic activation of the integrated stress response (ISR). The adaptive ISR signalling pathways help restore cellular homeostasis by downregulating protein synthesis in response to endoplasmic reticulum overloading or viral infections. By quantitative mass spectrometry analysis, we reveal that many viral recognition proteins and type I interferon (IFN) effectors are significantly upregulated in lung fibroblast cells from CKO mice compared with wild-type (WT) mice. This basal 'antiviral state' restricts the growth of influenza A virus and is governed by the interaction between proteotoxic stress response pathways and constitutive type I IFN signalling. CKO proteome composition and type I IFN signature were partially phenocopied upon sustained depletion of CRYPTOCHROME (CRY) proteins using a small-molecule CRY degrader, with modest differential gene expression consistent with differences seen between CKO and WT cells. Our results highlight the crosstalk between circadian rhythms, cell-intrinsic antiviral defences and protein homeostasis, providing a tractable molecular model to investigate the interface of these key contributors to human health and disease.This article is part of the Theo Murphy meeting issue 'Circadian rhythms in infection and immunity'.</p>","PeriodicalId":19872,"journal":{"name":"Philosophical Transactions of the Royal Society B: Biological Sciences","volume":"380 1918","pages":"20230344"},"PeriodicalIF":5.4,"publicationDate":"2025-01-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11753882/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143024254","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Samuel S C Rund, Aidan J O'Donnell, Kimberley F Prior, Daan R van der Veen
{"title":"Seasonal plasticity in daily timing of flight activity in <i>Anopheles stephensi</i> is driven by temperature modulation of dawn entrainment.","authors":"Samuel S C Rund, Aidan J O'Donnell, Kimberley F Prior, Daan R van der Veen","doi":"10.1098/rstb.2023.0343","DOIUrl":"10.1098/rstb.2023.0343","url":null,"abstract":"<p><p>The Asian malaria vector <i>Anopheles stephensi</i> is invading Africa, requiring it to adapt to novel climates and ecosystems. In part, this may be facilitated by <i>An. stephensi</i>'s poorly understood seasonal behavioural plasticity in flight timing, leading to earlier biting activity in cold Asian winters and later biting times in the warm summer. Changes in behavioural timing could be directly imposed by seasonal variation in ambient light and temperature levels or result from altered entrainment of intrinsically expressed circadian rhythms by these factors. We demonstrate that <i>An. stephensi</i> entrained flight activity timing is phase-locked to dawn and is not affected by constant ambient temperature, which cannot explain earlier biting activity in colder winters with later dawn. Instead, we show that where night temperatures are the colder part of daily temperature cycle; the entrained phase-angle between dawn and flight activity is altered, hereby increasingly colder, winter-like nights progressively advance flight activity onset. We propose that seasonal timing plasticity optimizes behaviour to warmer daytime in winter, and colder nights in summer, providing protection against both heat-desiccation and cold immobility. The adaptive advantage of this plasticity could be relevant to the successful invasion and survival of <i>An. stephensi</i> in African climates, and changing climate worldwide.This article is part of the Theo Murphy meeting issue, 'Circadian rhythms in infection and immunity'.</p>","PeriodicalId":19872,"journal":{"name":"Philosophical Transactions of the Royal Society B: Biological Sciences","volume":"380 1918","pages":"20230343"},"PeriodicalIF":5.4,"publicationDate":"2025-01-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11753879/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143024296","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Developmental synchrony and extraordinary multiplication rates in pathogenic organisms.","authors":"Megan A Greischar, Lauren M Childs","doi":"10.1098/rstb.2023.0337","DOIUrl":"10.1098/rstb.2023.0337","url":null,"abstract":"<p><p>The multiplication rates of pathogenic organisms influence disease progression, efficacy of immunity and therapeutics, and potential for within-host evolution. Thus, accurate estimates of multiplication rates are essential for biological understanding. We recently showed that common methods for inferring multiplication rates from malaria infection data substantially overestimate true values (i.e. under simulated scenarios), providing context for extraordinarily large estimates in human malaria parasites. A key unknown is whether this bias arises specifically from malaria parasite biology or represents a broader concern. Here, we identify the potential for biased multiplication rate estimates across pathogenic organisms with different developmental biology by generalizing a within-host malaria model. We find that diverse patterns of developmental sampling bias-the change in detectability over developmental age-reliably generate overestimates of the fold change in abundance, obscuring not just true growth rates but potentially even whether populations are expanding or declining. This pattern emerges whenever synchrony-the degree to which development is synchronized across the population of pathogenic organisms comprising an infection-decays with time. Only with simulated increases in synchrony do we find noticeable underestimates of multiplication rates. Obtaining robust estimates of multiplication rates may require accounting for diverse patterns of synchrony in pathogenic organisms.This article is part of the Theo Murphy meeting issue 'Circadian rhythms in infection and immunity'.</p>","PeriodicalId":19872,"journal":{"name":"Philosophical Transactions of the Royal Society B: Biological Sciences","volume":"380 1918","pages":"20230337"},"PeriodicalIF":5.4,"publicationDate":"2025-01-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11753877/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143024270","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Andrei Mihut, John S O'Neill, Carrie L Partch, Priya Crosby
{"title":"PERspectives on circadian cell biology.","authors":"Andrei Mihut, John S O'Neill, Carrie L Partch, Priya Crosby","doi":"10.1098/rstb.2023.0483","DOIUrl":"10.1098/rstb.2023.0483","url":null,"abstract":"<p><p>Daily rhythms in the activities of PERIOD proteins are critical to the temporal regulation of mammalian physiology. While the molecular partners and genetic circuits that allow PERIOD to effect auto-repression and regulate transcriptional programmes are increasingly well understood, comprehension of the time-resolved mechanisms that allow PERIOD to conduct this daily dance is incomplete. Here, we consider the character and controversies of this central mammalian clock protein with a focus on its intrinsically disordered nature.This article is part of the Theo Murphy meeting issue 'Circadian rhythms in infection and immunity'.</p>","PeriodicalId":19872,"journal":{"name":"Philosophical Transactions of the Royal Society B: Biological Sciences","volume":"380 1918","pages":"20230483"},"PeriodicalIF":5.4,"publicationDate":"2025-01-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11753889/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143024287","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Estefanía Martínez-Albert, Josef J Bless, Luciana Besedovsky
{"title":"Individual associations of self-reported sleep duration, sleep quality, chronotype and social jet lag with infectious disease risk.","authors":"Estefanía Martínez-Albert, Josef J Bless, Luciana Besedovsky","doi":"10.1098/rstb.2023.0472","DOIUrl":"10.1098/rstb.2023.0472","url":null,"abstract":"<p><p>Sleep deficiency is associated with infectious disease risk. However, little is known about the individual roles of different aspects of sleep, including sleep duration, sleep quality, sleep timing (assessed by chronotype) and sleep regularity (in the form of social jet lag) in this context. Here, we examined associations of the probability of reporting a cold or other infections with self-reported sleep duration, sleep quality and chronotype in a sample of 642 adults, and with social jet lag in a subsample of 274 adults. We found that short (≤ 6 h) and long sleepers (≥ 9 h) were more likely to report a cold in the past 30 days than average sleepers (7-8 h). Also, individuals with a definite evening chronotype were more likely to report a cold in the past 30 days than those with an intermediate chronotype, even when controlling for sleep duration. Finally, social jet lag was dose-dependently associated with the risk of reporting a cold in the past 12 months, independently of sleep duration, sleep quality and chronotype. No associations were found with sleep quality or with infections other than colds. The findings show that different aspects of sleep are independently associated with incidence of reported colds.This article is part of the Theo Murphy meeting issue 'Circadian rhythms in infection and immunity'.</p>","PeriodicalId":19872,"journal":{"name":"Philosophical Transactions of the Royal Society B: Biological Sciences","volume":"380 1918","pages":"20230472"},"PeriodicalIF":5.4,"publicationDate":"2025-01-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11753884/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143024282","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pirita Paajanen, Jacqueline M Kimmey, Antony N Dodd
{"title":"Circadian gating: concepts, processes, and opportunities.","authors":"Pirita Paajanen, Jacqueline M Kimmey, Antony N Dodd","doi":"10.1098/rstb.2023.0346","DOIUrl":"10.1098/rstb.2023.0346","url":null,"abstract":"<p><p>Circadian clocks provide a biological measure of time that coordinates metabolism, physiology and behaviour with 24 h cycles in the environment. Circadian systems have a variety of characteristic properties, such as entrainment to environmental cues, a self-sustaining rhythm of about 24 h and temperature compensation of the circadian rhythm. In this perspective, we discuss the process of circadian gating, which refers to the restriction of a biological event to particular times of day by the circadian clock. We introduce principles and processes associated with circadian gating in a variety of organisms, including some associated mechanisms. We highlight socioeconomic opportunities presented by the investigation of circadian gating, using selected examples from circadian medicine and agricultural crop production to illustrate its importance.This article is part of the Theo Murphy meeting issue 'Circadian rhythms in infection and immunity'.</p>","PeriodicalId":19872,"journal":{"name":"Philosophical Transactions of the Royal Society B: Biological Sciences","volume":"380 1918","pages":"20230346"},"PeriodicalIF":5.4,"publicationDate":"2025-01-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11753883/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143024257","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Characterization of extracellular vesicles released from <i>Prochlorococcus</i> MED4 at the steady state and under a light-dark cycle.","authors":"Ziqing Peng, Yaxin Liu, Haiying Ma, Shiwei Xiao, Allan Au-Yeung, Liang Zhang, Qinglu Zeng, Yusong Guo","doi":"10.1098/rstb.2023.0339","DOIUrl":"10.1098/rstb.2023.0339","url":null,"abstract":"<p><p>Bacterial extracellular vesicles (EVs) are vesicles secreted by bacteria into the extracellular environment. Containing DNA, RNA and proteins, EVs are implicated to mediate intercellular communications. The marine cyanobacterium <i>Prochlorococcus</i>, the most abundant photosynthetic organism in marine ecosystems, has been shown to generate EVs continuously during cell growth. However, biogenesis and functions of EVs released by <i>Prochlorococcus</i> remain largely unclear. Here, we isolated and characterized EVs released by <i>Prochlorococcus</i> MED4 culture. We found that the majority of MED4 EVs are elliptical and enriched with specific proteins performing particular cellular functions. The light-dark cycle has been demonstrated to affect the cell cycle of <i>Prochlorococcus</i>, with cell division occurring at night time. Interestingly, we found that the net production of MED4 EVs was faster during the night time. Moreover, we revealed that MED4 EVs that are released or absorbed in the night time are enriched with distinct proteins, suggesting the release and absorbance of EVs are influenced by the diel cycle. We found that inhibiting cell division decreased the net production of MED4 EVs during the night time, suggesting that cell division is important for the biogenesis of MED4 EVs. These analyses provide novel insights into biogenesis and functions of EVs released from bacteria.This article is part of the Theo Murphy meeting issue 'Circadian rhythms in infection and immunity'.</p>","PeriodicalId":19872,"journal":{"name":"Philosophical Transactions of the Royal Society B: Biological Sciences","volume":"380 1918","pages":"20230339"},"PeriodicalIF":5.4,"publicationDate":"2025-01-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11753881/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143024248","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Rageema Joseph, Jessica L Odendaal, Robert A Ingle, Laura C Roden
{"title":"The role of the jasmonate signalling transcription factors MYC2/3/4 in circadian clock-mediated regulation of immunity in Arabidopsis.","authors":"Rageema Joseph, Jessica L Odendaal, Robert A Ingle, Laura C Roden","doi":"10.1098/rstb.2023.0338","DOIUrl":"https://doi.org/10.1098/rstb.2023.0338","url":null,"abstract":"<p><p>Plants are exposed to pathogens at specific, yet predictable times of the day-night cycle. In Arabidopsis, the circadian clock influences temporal differences in susceptibility to the necrotrophic pathogen <i>Botrytis cinerea</i>. The jasmonic acid (JA) pathway regulates immune responses against <i>B. cinerea</i>. The paralogous basic helix-loop-helix transcription factors MYC2, MYC3 and MYC4 are primary regulators of the JA pathway, but their role in regulating temporal variation in immunity is untested. This study aimed to investigate the roles of the MYC transcription factors in the temporal defence response to <i>B. cinerea</i>. We inoculated leaves from wild-type, <i>myc</i> single-, double- and triple-knockout mutants, and lines overexpressing <i>MYC2</i>, <i>MYC3</i> or <i>MYC4</i>, with <i>B. cinerea</i> at two times of day in constant light, and compared lesion sizes. The presence of MYC2, MYC3 or MYC4 alone was sufficient to maintain temporal variation in susceptibility, but this was abolished in the <i>myc234</i> triple-knockout mutant. Constitutive expression of <i>MYC2</i>, <i>MYC3</i> or <i>MYC4</i> abolished time-of-day differences in susceptibility. The data suggest that MYC2, MYC3 and MYC4 function redundantly in regulating temporal defence responses against <i>B. cinerea</i> and are a point of convergence between the JA pathway and the circadian clock in Arabidopsis.This article is part of the Theo Murphy meeting issue 'Circadian rhythms in infection and immunity'.</p>","PeriodicalId":19872,"journal":{"name":"Philosophical Transactions of the Royal Society B: Biological Sciences","volume":"380 1918","pages":"20230338"},"PeriodicalIF":5.4,"publicationDate":"2025-01-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11753874/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143060346","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Circadian rhythms: pervasive, and often times evasive.","authors":"Luis F Larrondo","doi":"10.1098/rstb.2023.0477","DOIUrl":"https://doi.org/10.1098/rstb.2023.0477","url":null,"abstract":"<p><p>Most circadian texts begin by stating that clocks are pervasive throughout the tree of life. Indeed, clock mechanisms have been described from cyanobacteria to humans, representing a notable example of convergent evolution: yet, there are several phyla in animals, protists or within fungi and bacteria, in which homologs of some-or all-known clock components seem to be absent, posing inevitable questions about the evolution of circadian systems. Moreover, as we move away from model organisms, there are several taxa in which core clock elements can be identified at the genomic levels. However, the functional description of those putative clocks has been hard to achieve, as rhythmicity is not observed unless defined abiotic or nutritional cues are provided. The mechanisms 'conditioning' the functionality of clocks remain uncertain, emphasizing the need to delve further into non-model circadian systems. As the absence of evidence is not evidence of absence, the lack of known core-clock homologs or of observable rhythms in a given organism, cannot be an <i>a priori</i> criterion to discard the presence of a functional clock, as rhythmicity may be limited to yet untested experimental conditions or phenotypes. This article seeks to reflect on these topics, highlighting some of the pressing questions awaiting to be addressed.This article is part of the Theo Murphy meeting issue 'Circadian rhythms in infection and immunity'.</p>","PeriodicalId":19872,"journal":{"name":"Philosophical Transactions of the Royal Society B: Biological Sciences","volume":"380 1918","pages":"20230477"},"PeriodicalIF":5.4,"publicationDate":"2025-01-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143024261","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}