Journal of Biological Rhythms最新文献

{"title":"Menstrual Cycle Variations in Wearable-Detected Finger Temperature and Heart Rate, But Not in Sleep Metrics, in Young and Midlife Individuals.","authors":"Elisabet Alzueta, Marie Gombert-Labedens, Harold Javitz, Dilara Yuksel, Evelyn Perez-Amparan, Leticia Camacho, Orsolya Kiss, Massimiliano de Zambotti, Negin Sattari, Andres Alejandro-Pena, Jing Zhang, Alessandra Shuster, Allison Morehouse, Katharine Simon, Sara Mednick, Fiona C Baker","doi":"10.1177/07487304241265018","DOIUrl":"10.1177/07487304241265018","url":null,"abstract":"<p><p>Most studies about the menstrual cycle are laboratory-based, in small samples, with infrequent sampling, and limited to young individuals. Here, we use wearable and diary-based data to investigate menstrual phase and age effects on finger temperature, sleep, heart rate (HR), physical activity, physical symptoms, and mood. A total of 116 healthy females, without menstrual disorders, were enrolled: 67 young (18-35 years, reproductive stage) and 53 midlife (42-55 years, late reproductive to menopause transition). Over one menstrual cycle, participants wore Oura ring Gen2 to detect finger temperature, HR, heart rate variability (root mean square of successive differences between normal heartbeats [RMSSD]), steps, and sleep. They used luteinizing hormone (LH) kits and daily rated sleep, mood, and physical symptoms. A cosinor rhythm analysis was applied to detect menstrual oscillations in temperature. The effect of menstrual cycle phase and group on all other variables was assessed using hierarchical linear models. Finger temperature followed an oscillatory trend indicative of ovulatory cycles in 96 participants. In the midlife group, the temperature rhythm's mesor was higher, but period, amplitude, and number of days between menses and acrophase were similar in both groups. In those with oscillatory temperatures, HR was lowest during menses in both groups. In the young group only, RMSSD was lower in the late-luteal phase than during menses. Overall, RMSSD was lower, and number of daily steps was higher, in the midlife group. No significant menstrual cycle changes were detected in wearable-derived or self-reported measures of sleep efficiency, duration, wake-after-sleep onset, sleep onset latency, or sleep quality. Mood positivity was higher around ovulation, and physical symptoms manifested during menses. Temperature and HR changed across the menstrual cycle; however, sleep measures remained stable in these healthy young and midlife individuals. Further work should investigate over longer periods whether individual- or cluster-specific sleep changes exist, and if a buffering mechanism protects sleep from physiological changes across the menstrual cycle.</p>","PeriodicalId":15056,"journal":{"name":"Journal of Biological Rhythms","volume":null,"pages":null},"PeriodicalIF":2.9,"publicationDate":"2024-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11416332/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141897515","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Transcriptomic Plasticity of the Circadian Clock in Response to Photoperiod: A Study in Male Melatonin-Competent Mice.","authors":"Olivia H Cox, Manuel A Gianonni-Guzmán, Jean-Philippe Cartailler, Matthew A Cottam, Douglas G McMahon","doi":"10.1177/07487304241265439","DOIUrl":"10.1177/07487304241265439","url":null,"abstract":"<p><p>Seasonal daylength, or circadian photoperiod, is a pervasive environmental signal that profoundly influences physiology and behavior. In mammals, the central circadian clock resides in the suprachiasmatic nuclei (SCN) of the hypothalamus where it receives retinal input and synchronizes, or entrains, organismal physiology and behavior to the prevailing light cycle. The process of entrainment induces sustained plasticity in the SCN, but the molecular mechanisms underlying SCN plasticity are incompletely understood. Entrainment to different photoperiods persistently alters the timing, waveform, period, and light resetting properties of the SCN clock and its driven rhythms. To elucidate novel candidate genes for molecular mechanisms of photoperiod plasticity, we performed RNA sequencing on whole SCN dissected from mice raised in long (light:dark [LD] 16:8) and short (LD 8:16) photoperiods. Fewer rhythmic genes were detected in mice subjected to long photoperiod, and in general, the timing of gene expression rhythms was advanced 4-6 h. However, a few genes showed significant delays, including <i>Gem</i>. There were significant changes in the expression of the clock-associated gene <i>Timeless</i> and in SCN genes related to light responses, neuropeptides, gamma aminobutyric acid (GABA), ion channels, and serotonin. Particularly striking were differences in the expression of the neuropeptide signaling genes <i>Prokr2</i> and <i>Cck</i>, as well as convergent regulation of the expression of 3 SCN light response genes, <i>Dusp4</i>, <i>Rasd1</i>, and <i>Gem</i>. Transcriptional modulation of <i>Dusp4</i> and <i>Rasd1</i> and phase regulation of <i>Gem</i> are compelling candidate molecular mechanisms for plasticity in the SCN light response through their modulation of the critical NMDAR-MAPK/ERK-CREB/CRE light signaling pathway in SCN neurons. Modulation of <i>Prokr2</i> and <i>Cck</i> may critically support SCN neural network reconfiguration during photoperiodic entrainment. Our findings identify the SCN light response and neuropeptide signaling gene sets as rich substrates for elucidating novel mechanisms of photoperiod plasticity. Data are also available at http://circadianphotoperiodseq.com/, where users can view the expression and rhythmic properties of genes across these photoperiod conditions.</p>","PeriodicalId":15056,"journal":{"name":"Journal of Biological Rhythms","volume":null,"pages":null},"PeriodicalIF":2.9,"publicationDate":"2024-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11425976/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141878742","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Toward an Indoor Lighting Solution for Social Jet Lag.","authors":"Alexandra Neitz, Alicia Rice, Leandro Casiraghi, Ivana L Bussi, Ethan D Buhr, Maureen Neitz, Jay Neitz, Horacio O de la Iglesia, James A Kuchenbecker","doi":"10.1177/07487304241262918","DOIUrl":"10.1177/07487304241262918","url":null,"abstract":"<p><p>There is growing interest in developing artificial lighting that stimulates intrinsically photosensitive retinal ganglion cells (ipRGCs) to entrain circadian rhythms to improve mood, sleep, and health. Efforts have focused on stimulating the intrinsic photopigment, melanopsin; however, specialized color vision circuits have been elucidated in the primate retina that transmit blue-yellow cone-opponent signals to ipRGCs. We designed a light that stimulates color-opponent inputs to ipRGCs by temporally alternating short- and long-wavelength components that strongly modulate short-wavelength sensitive (S) cones. Two-hour exposure to this S-cone modulating light produced an average circadian phase advance of 1 h and 20 min in 6 subjects (mean age = 30 years) compared to no phase advance for the subjects after exposure to a 500 lux white light equated for melanopsin effectiveness. These results are promising for developing artificial lighting that is highly effective in controlling circadian rhythms by invisibly modulating cone-opponent circuits.</p>","PeriodicalId":15056,"journal":{"name":"Journal of Biological Rhythms","volume":null,"pages":null},"PeriodicalIF":2.9,"publicationDate":"2024-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11416324/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141855626","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Environmental Light Controls the Daily Organization of Breathing by Activating Brn3b-expressing Intrinsically Photosensitive Retinal Ganglion Cells in Mice.","authors":"Aaron A Jones,Allison R Spears,Deanna M Arble","doi":"10.1177/07487304241276888","DOIUrl":"https://doi.org/10.1177/07487304241276888","url":null,"abstract":"Rhythmic, daily fluctuations in minute ventilation are controlled by the endogenous circadian clock located in the suprachiasmatic nucleus (SCN). While light serves as a potent synchronizer for the SCN, it also influences physiology and behavior by activating Brn3b-expressing, intrinsically photosensitive retinal ganglion cells (ipRGCs). It is currently unclear the extent to which the external light environment shapes daily ventilatory patterns independent of the SCN. To determine the relative influence of environmental light versus circadian timing on the organization of daily rhythms in minute ventilation, we used whole-body plethysmography to measure the breathing of mice housed on a non-entraining T28 cycle (14 h light:14 h dark). Using this protocol, we found that minute ventilation exhibits a ~28-h rhythm with a peak at dark onset that coincides with the light:dark cycle and the animals' locomotor activity. To determine if this 28-h rhythm in minute ventilation was mediated by Brn3b-expressing ipRGCs, we measured the breathing of Brn3bDTA mice housed under the T28 cycle. Brn3bDTA mice lack the Brn3b-expressing ipRGCs that project to many non-SCN brain regions. We found that despite rhythmic light cues occurring on a 28-h basis, Brn3bDTA mice exhibited 24-h rhythms in minute ventilation, locomotor activity, and core body temperature consistent with organization by the SCN. The 24-h minute ventilation rhythm of Brn3bDTA mice was found to be driven predominantly by tidal volume rather than respiratory rate. These data indicate that the external light:dark cycle can directly drive daily patterns in minute ventilation by way of Brn3b-expressing ipRGCs. In addition, these data strongly suggest that the activation of Brn3b-expressing ipRGCs principally organizes daily patterns in breathing and locomotor activity when light:dark cues are presented in opposition to endogenous clock timing.","PeriodicalId":15056,"journal":{"name":"Journal of Biological Rhythms","volume":null,"pages":null},"PeriodicalIF":3.5,"publicationDate":"2024-09-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142188488","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Transient Cooling Resets Circadian Rhythms of Locomotor Activity in Lizards","authors":"Sakimi Nagashima, Sho T. Yamaguchi, Zhiwen Zhou, Hiroaki Norimoto","doi":"10.1177/07487304241273190","DOIUrl":"https://doi.org/10.1177/07487304241273190","url":null,"abstract":"Animals frequently experience temperature fluctuations in their natural life cycle, including periods of low temperatures below their activity range. For example, poikilothermic animals are known to enter a hibernation-like state called brumation during transient cooling. However, the knowledge regarding the physiological responses of brumation is limited. Specifically, the impact of exposure to low-temperature conditions outside the range of temperature compensation on the subsequent circadian behavioral rhythms remains unclear. In this study, we investigated the effects of transient cooling on the behavioral circadian rhythm in the non-avian reptile, the bearded dragon ( Pogona vitticeps). Under constant light (LL) conditions at 30 °C, the animals exhibited a free-running rhythm, and exposure to low temperatures (4 °C) caused a complete cessation of locomotion. Furthermore, we revealed that the behavioral rhythm after rewarming is determined not by the circadian phase at the onset or the duration of cooling, but by the timing of cooling cessation.","PeriodicalId":15056,"journal":{"name":"Journal of Biological Rhythms","volume":null,"pages":null},"PeriodicalIF":3.5,"publicationDate":"2024-09-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142188486","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Using Wearable Skin Temperature Data to Advance Tracking and Characterization of the Menstrual Cycle in a Real-World Setting.","authors":"Marie Gombert-Labedens, Elisabet Alzueta, Evelyn Perez-Amparan, Dilara Yuksel, Orsolya Kiss, Massimiliano de Zambotti, Katharine Simon, Jing Zhang, Alessandra Shuster, Allison Morehouse, Andres Alessandro Pena, Sara Mednick, Fiona C Baker","doi":"10.1177/07487304241247893","DOIUrl":"10.1177/07487304241247893","url":null,"abstract":"<p><p>The menstrual cycle is a loop involving the interplay of different organs and hormones, with the capacity to impact numerous physiological processes, including body temperature and heart rate, which in turn display menstrual rhythms. The advent of wearable devices that can continuously track physiological data opens the possibility of using these prolonged time series of skin temperature data to noninvasively detect the temperature variations that occur in ovulatory menstrual cycles. Here, we show that the menstrual skin temperature variation is better represented by a model of oscillation, the cosinor, than by a biphasic square wave model. We describe how applying a cosinor model to a menstrual cycle of distal skin temperature data can be used to assess whether the data oscillate or not, and in cases of oscillation, rhythm metrics for the cycle, including mesor, amplitude, and acrophase, can be obtained. We apply the method to wearable temperature data collected at a minute resolution each day from 120 female individuals over a menstrual cycle to illustrate how the method can be used to derive and present menstrual cycle characteristics, which can be used in other analyses examining indicators of female health. The cosinor method, frequently used in circadian rhythms studies, can be employed in research to facilitate the assessment of menstrual cycle effects on physiological parameters, and in clinical settings to use the characteristics of the menstrual cycles as health markers or to facilitate menstrual chronotherapy.</p>","PeriodicalId":15056,"journal":{"name":"Journal of Biological Rhythms","volume":null,"pages":null},"PeriodicalIF":2.9,"publicationDate":"2024-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11294004/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141071010","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Practical Advice on Measuring and Applying Light for Laboratory Mammals.","authors":"Robert J Lucas, Stuart N Peirson","doi":"10.1177/07487304241259514","DOIUrl":"https://doi.org/10.1177/07487304241259514","url":null,"abstract":"<p><p>Light is recognized as an important component of the environment for laboratory animals. It supports vision, sets the phase of circadian clocks, and drives wide-ranging adjustments in physiological and behavioral state. Manipulating light is meanwhile a key experimental approach in the fields of vision science and chronobiology. Nevertheless, until recently, there has been no consensus on methods for quantifying light as experienced by laboratory animals. Widely adopted practices employ metrics such as illuminance (units = lux) that are designed to quantify light as experienced by human observers. These weight energy across the spectrum according to a spectral sensitivity profile for human vision that is not widely replicated for non-human species. Recently, a Consensus View was published that proposes methods of light measurement and standardization that take account of these species-specific differences in wavelength sensitivity. Here, we draw upon the contents of that consensus to provide simplified advice on light measurement in laboratory mammal experimentation and husbandry and quantitative guidance on what constitutes appropriate lighting for both visual and circadian function.</p>","PeriodicalId":15056,"journal":{"name":"Journal of Biological Rhythms","volume":null,"pages":null},"PeriodicalIF":2.9,"publicationDate":"2024-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141859798","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Biological Sex Influences Daily Locomotor Rhythms in Mice Held Under Different Housing Conditions.","authors":"Amanda Pastrick, Matthew Diaz, Griffin Adaya, Victoria Montinola, Madeline Arzbecker, Deborah A M Joye, Jennifer A Evans","doi":"10.1177/07487304241256004","DOIUrl":"10.1177/07487304241256004","url":null,"abstract":"<p><p>Daily rhythms are programmed by a central circadian clock that is modulated by photoperiod. Here, we recorded locomotor activity rhythms in C57Bl/6 or mPer2^Luc mice of both sexes held under different housing conditions. First, we confirm that the structure of locomotor activity rhythms differs between male and female mice in both genetic backgrounds. Male mice exhibit a nightly \"siesta,\" whereas female mice fluctuate between nights with and without a nightly siesta, which corresponds with changes in locomotor activity levels, circadian period, and vaginal cytology. The nightly siesta is modulated by the presence of a running wheel in both sexes but is not required for the infradian patterning of locomotor rhythms in females. Finally, photoperiodic changes in locomotor rhythms differed by sex, and females displayed phase-jumping responses earlier than males under a parametric photoentrainment assay simulating increasing day length. Collectively, these results highlight that sex and sex hormones influence daily locomotor rhythms under a variety of different environmental conditions.</p>","PeriodicalId":15056,"journal":{"name":"Journal of Biological Rhythms","volume":null,"pages":null},"PeriodicalIF":2.9,"publicationDate":"2024-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11322640/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141283811","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Functional Analyses of Four Cryptochromes From Aquatic Organisms After Heterologous Expression in <i>Drosophila melanogaster</i> Circadian Clock Cells.","authors":"Chenghao Chen, T Katherine Tamai, Min Xu, Libero Petrone, Paola Oliveri, David Whitmore, Ralf Stanewsky","doi":"10.1177/07487304241228617","DOIUrl":"10.1177/07487304241228617","url":null,"abstract":"<p><p>Cryptochromes (Crys) represent a multi-facetted class of proteins closely associated with circadian clocks. They have been shown to function as photoreceptors but also to fulfill light-independent roles as transcriptional repressors within the negative feedback loop of the circadian clock. In addition, there is evidence for Crys being involved in light-dependent magneto-sensing, and regulation of neuronal activity in insects, adding to the functional diversity of this cryptic protein class. In mammals, Crys are essential components of the circadian clock, but their role in other vertebrates is less clear. In invertebrates, Crys can function as circadian photoreceptors, or as components of the circadian clock, while in some species, both light-receptive and clock factor roles coexist. In the current study, we investigate the function of Cry proteins in zebrafish (<i>Danio rerio</i>), a freshwater teleost expressing 6 <i>cry</i> genes. Zebrafish peripheral circadian clocks are intrinsically light-sensitive, suggesting the involvement of Cry in light-resetting. Echinoderms (<i>Strongylocentrotus purpuratus</i>) represent the only class of deuterostomes that possess an orthologue (<i>SpuCry</i>) of the light-sensitive <i>Drosophila melanogaster</i> Cry, which is an important component of the light-resetting pathway, but also works as transcriptional repressor in peripheral clocks of fruit flies. We therefore investigated the potential of different zebrafish <i>cry</i> genes and <i>SpuCry</i> to replace the light-resetting and repressor functions of <i>Drosophila</i> Cry by expressing them in fruit flies lacking endogenous <i>cry</i> function. Using various behavioral and molecular approaches, we show that most Cry proteins analyzed are able to fulfill circadian repressor functions in flies, except for one of the zebrafish Crys, encoded by <i>cry4a</i>. Cry4a also shows a tendency to support light-dependent Cry functions, indicating that it might act in the light-input pathway of zebrafish.</p>","PeriodicalId":15056,"journal":{"name":"Journal of Biological Rhythms","volume":null,"pages":null},"PeriodicalIF":2.9,"publicationDate":"2024-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11292970/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140305734","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"The Free-Running Circasemilunar Period Is Determined by Counting Circadian Clock Cycles in the Marine Midge <i>Clunio Marinus</i>.","authors":"Jule Neumann, Dharanish Rajendra, Tobias S Kaiser","doi":"10.1177/07487304241249516","DOIUrl":"10.1177/07487304241249516","url":null,"abstract":"<p><p>Semilunar rhythms are found in numerous marine organisms, but the molecular mechanism and functional principles of endogenous circasemilunar clocks remain elusive. Here, we explore the connection between the free-running circasemilunar clock and the circadian clock in the marine midge <i>Clunio marinus</i> with three different chronobiological assays. First, we found that the free-running circasemilunar period of the adult emergence rhythm in <i>C. marinus</i> changes linearly with diel T-cycle length, supporting a day-counting mechanism. Second, under LD 6:6, periods of circasemilunar and circadian emergence were comparable to those under LD 12:12, indicating that the circasemilunar counter in <i>C. marinus</i> relies on endogenous circadian oscillations rather than external T-cycles. Finally, when desynchronizing the circadian clock with constant light, the free-running circasemilunar emergence rhythm disappeared as well, suggesting that it requires a synchronized circadian clock. These results oppose the long-held view that <i>C. marinus'</i> free-running circasemilunar clock operates independently of the circadian clock. In a broader evolutionary context, our results strengthen the idea that the circasemilunar clocks of dipterous insects are based on different functional principles compared to the circasemilunar or circalunar clocks of marine annelids and algae. These divergent clock principles may indicate multiple evolutionary origins of circasemilunar and circalunar clocks.</p>","PeriodicalId":15056,"journal":{"name":"Journal of Biological Rhythms","volume":null,"pages":null},"PeriodicalIF":2.9,"publicationDate":"2024-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11292968/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141064321","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}