Current Biology最新文献

{"title":"Systems mapping of bidirectional endosomal transport through the crowded cell","authors":"Marlieke L.M. Jongsma, Nina Bakker, Lenard M. Voortman, Roman I. Koning, Erik Bos, Jimmy J.L.L. Akkermans, Lennert Janssen, Jacques Neefjes","doi":"10.1016/j.cub.2024.08.026","DOIUrl":"https://doi.org/10.1016/j.cub.2024.08.026","url":null,"abstract":"<p>Kinesin and dynein-dynactin motors move endosomes and other vesicles bidirectionally along microtubules, a process mainly studied under <em>in vitro</em> conditions. Here, we provide a physiological bidirectional transport model following color-coded, endogenously tagged transport-related proteins as they move through a crowded cellular environment. Late endosomes (LEs) surf bidirectionally on Protrudin-enriched endoplasmic reticulum (ER) membrane contact sites, while hopping and gliding along microtubules and bypassing cellular obstacles, such as mitochondria. During bidirectional transport, late endosomes do not switch between opposing Rab7 GTPase effectors, RILP and FYCO1, or their associated dynein and KIF5B motor proteins, respectively. In the endogenous setting, far fewer motors associate with endosomal membranes relative to effectors, implying coordination of transport with other aspects of endosome physiology through GTPase-regulated mechanisms. We find that directionality of transport is provided in part by various microtubule-associated proteins (MAPs), including MID1, EB1, and CEP169, which recruit Lis1-activated dynein motors to microtubule plus ends for transport of early and late endosomal populations. At these microtubule plus ends, activated dynein motors encounter the dynactin subunit p150^glued and become competent for endosomal capture and minus-end movement in collaboration with membrane-associated Rab7-RILP. We show that endosomes surf over the ER through the crowded cell and move bidirectionally under the control of MAPs for motor activation and through motor replacement and capture by endosomal anchors.</p>","PeriodicalId":11359,"journal":{"name":"Current Biology","volume":null,"pages":null},"PeriodicalIF":9.2,"publicationDate":"2024-09-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142216388","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Protofilament-specific nanopatterns of tubulin post-translational modifications regulate the mechanics of ciliary beating","authors":"Gonzalo Alvarez Viar, Nikolai Klena, Fabrizio Martino, Adrian Pascal Nievergelt, Davide Bolognini, Paola Capasso, Gaia Pigino","doi":"10.1016/j.cub.2024.08.021","DOIUrl":"https://doi.org/10.1016/j.cub.2024.08.021","url":null,"abstract":"<p>Controlling ciliary beating is essential for motility and signaling in eukaryotes. This process relies on the regulation of various axonemal proteins that assemble in stereotyped patterns onto individual microtubules of the ciliary structure. Additionally, each axonemal protein interacts exclusively with determined tubulin protofilaments of the neighboring microtubule to carry out its function. While it is known that tubulin post-translational modifications (PTMs) are important for proper ciliary motility, the mode and extent to which they contribute to these interactions remain poorly understood. Currently, the prevailing understanding is that PTMs can confer functional specialization at the level of individual microtubules. However, this paradigm falls short of explaining how the tubulin code can manage the complexity of the axonemal structure where functional interactions happen in defined patterns at the sub-microtubular scale. Here, we combine immuno-cryo-electron tomography (cryo-ET), expansion microscopy, and mutant analysis to show that, in motile cilia, tubulin glycylation and polyglutamylation form mutually exclusive protofilament-specific nanopatterns at a sub-microtubular scale. These nanopatterns are consistent with the distributions of axonemal dyneins and nexin-dynein regulatory complexes, respectively, and are indispensable for their regulation during ciliary beating. Our findings offer a new paradigm for understanding how different tubulin PTMs, such as glycylation, glutamylation, acetylation, tyrosination, and detyrosination, can coexist within the ciliary structure and specialize individual protofilaments for the regulation of diverse protein complexes. The identification of a ciliary tubulin nanocode by cryo-ET suggests the need for high-resolution studies to better understand the molecular role of PTMs in other cellular compartments beyond the cilium.</p>","PeriodicalId":11359,"journal":{"name":"Current Biology","volume":null,"pages":null},"PeriodicalIF":9.2,"publicationDate":"2024-09-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142216282","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Serotonergic modulation of swallowing in a complete fly vagus nerve connectome","authors":"Andreas Schoofs, Anton Miroschnikow, Philipp Schlegel, Ingo Zinke, Casey M. Schneider-Mizell, Albert Cardona, Michael J. Pankratz","doi":"10.1016/j.cub.2024.08.025","DOIUrl":"https://doi.org/10.1016/j.cub.2024.08.025","url":null,"abstract":"<p>How the body interacts with the brain to perform vital life functions, such as feeding, is a fundamental issue in physiology and neuroscience. Here, we use a whole-animal scanning transmission electron microscopy volume of <em>Drosophila</em> to map the neuronal circuits that connect the entire enteric nervous system to the brain via the insect vagus nerve at synaptic resolution. We identify a gut-brain feedback loop in which Piezo-expressing mechanosensory neurons in the esophagus convey food passage information to a cluster of six serotonergic neurons in the brain. Together with information on food value, these central serotonergic neurons enhance the activity of serotonin receptor 7-expressing motor neurons that drive swallowing. This elemental circuit architecture includes an axo-axonic synaptic connection from the glutamatergic motor neurons innervating the esophageal muscles onto the mechanosensory neurons that signal to the serotonergic neurons. Our analysis elucidates a neuromodulatory sensory-motor system in which ongoing motor activity is strengthened through serotonin upon completion of a biologically meaningful action, and it may represent an ancient form of motor learning.</p>","PeriodicalId":11359,"journal":{"name":"Current Biology","volume":null,"pages":null},"PeriodicalIF":9.2,"publicationDate":"2024-09-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142216283","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Evolutionarily diverse fungal zoospores show contrasting swimming patterns specific to ultrastructure","authors":"Luis Javier Galindo, Thomas A. Richards, Jasmine A. Nirody","doi":"10.1016/j.cub.2024.08.016","DOIUrl":"https://doi.org/10.1016/j.cub.2024.08.016","url":null,"abstract":"<p>Zoosporic fungi, also called chytrids, produce single-celled motile spores with flagellar swimming tails (zoospores).<span><span>¹</span></span>^,<span><span>²</span></span> These fungi are key components of aquatic food webs, acting as pathogens, saprotrophs, and prey.<span><span>³</span></span>^,<span><span>⁴</span></span>^,<span><span>⁵</span></span>^,<span><span>⁶</span></span>^,<span><span>⁷</span></span>^,<span><span>⁸</span></span> Little is known about the swimming behavior of fungal zoospores, a crucial factor governing dispersal, biogeographical range, ecological function, and infection dynamics.<span><span>⁶</span></span>^,<span><span>⁹</span></span> Here, we track the swimming patterns of zoospores from 12 evolutionarily divergent species of zoosporic fungi from across seven orders of the Chytridiomycota and the Blastocladiomycota. We report two major swimming patterns that correlate with the cytoskeletal ultrastructure of these zoospores. Specifically, we show that species without major cytoplasmic tubulin components swim in a circular fashion, while species with prominent cytoplasmic tubulin structures swim in a pattern akin to a random walk (move-stop-redirect-move). We confirm cytoskeletal architecture by performing fluorescence confocal microscopy across all 12 species. We then treat representative species with variant swimming behaviors and cytoplasmic-cytoskeletal arrangements with tubulin-stabilizing (Taxol) and depolymerizing (nocodazole) pharmacological compounds. We observed that when treating the “random walk” species with nocodazole, their swimming behavior changed to a circular-swimming pattern. Confocal imaging of the nocodazole-treated zoospores demonstrates that these cells maintain flagellum tubulin structures but lack their characteristic cytoplasmic tubulin structures. Our data demonstrate that the capability of zoospores to perform “complex” random-walk movement is linked to the presence of prominent cytoplasmic tubulin structures and suggest a link between cytology, sensory systems, and swimming behavior in a diversity of zoosporic fungi.</p>","PeriodicalId":11359,"journal":{"name":"Current Biology","volume":null,"pages":null},"PeriodicalIF":9.2,"publicationDate":"2024-09-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142216121","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Stretch triggers microtubule stabilization and MARCKS-dependent membrane incorporation in the shaft of embryonic axons","authors":"Sara C. Sousa, Miguel Aroso, Rita Bessa, Eduardo Veríssimo, Tiago Ferreira da Silva, Cátia D.F. Lopes, Pedro Brites, Jorge Vieira, Cristina P. Vieira, Paulo C. Aguiar, Monica M. Sousa","doi":"10.1016/j.cub.2024.08.018","DOIUrl":"https://doi.org/10.1016/j.cub.2024.08.018","url":null,"abstract":"<p>Neurons have a unique polarized nature that must adapt to environmental changes throughout their lifespan. During embryonic development, axon elongation is led by the growth cone,<span><span>¹</span></span> culminating in the formation of a presynaptic terminal. After synapses are formed, axons elongate in a growth cone-independent manner to accompany body growth while maintaining their ultrastructure and function.<span><span>²</span></span>^,<span><span>³</span></span>^,<span><span>⁴</span></span>^,<span><span>⁵</span></span>^,<span><span>⁶</span></span> To further understand mechanical strains on the axon shaft, we developed a computer-controlled stretchable microfluidic platform compatible with multi-omics and live imaging. Our data show that sensory embryonic dorsal root ganglia (DRGs) neurons have high plasticity, with axon shaft microtubules decreasing polymerization rates, aligning with the direction of tension, and undergoing stabilization. Moreover, in embryonic DRGs, stretch triggers yes-associated protein (YAP) nuclear translocation, supporting its participation in the regulatory network that enables tension-driven axon growth. Other than cytoskeleton remodeling, stretch prompted MARCKS-dependent formation of plasmalemmal precursor vesicles (PPVs), resulting in new membrane incorporation throughout the axon shaft. In contrast, adolescent DRGs showed a less robust adaptation, with axonal microtubules being less responsive to stretch. Also, while adolescent DRGs were still amenable to strain-induced PPV formation at higher stretch rates, new membrane incorporation in the axon shaft failed to occur. In summary, we developed a new resource to study the biology of axon stretch growth. By unraveling cytoskeleton adaptation and membrane remodeling in the axon shaft of stretched neurons, we are moving forward in understanding axon growth.</p>","PeriodicalId":11359,"journal":{"name":"Current Biology","volume":null,"pages":null},"PeriodicalIF":9.2,"publicationDate":"2024-09-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142216120","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Cingulate to septal circuitry facilitates the preference to affiliate with large peer groups","authors":"","doi":"10.1016/j.cub.2024.08.019","DOIUrl":"https://doi.org/10.1016/j.cub.2024.08.019","url":null,"abstract":"Despite the prevalence of large-group living across the animal kingdom, no studies have examined the neural mechanisms that make group living possible…","PeriodicalId":11359,"journal":{"name":"Current Biology","volume":null,"pages":null},"PeriodicalIF":9.2,"publicationDate":"2024-09-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142216119","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"A distributed auditory network mediated by pontine central gray underlies ultra-fast awakening in response to alerting sounds","authors":"Jinxing Wei, Cuiyu Xiao, Guang-Wei Zhang, Li Shen, Huizhong W. Tao, Li I. Zhang","doi":"10.1016/j.cub.2024.08.020","DOIUrl":"https://doi.org/10.1016/j.cub.2024.08.020","url":null,"abstract":"<p>Sleeping animals can be woken up rapidly by external threat signals, which is an essential defense mechanism for survival. However, neuronal circuits underlying the fast transmission of sensory signals for this process remain unclear. Here, we report in mice that alerting sound can induce rapid awakening within hundreds of milliseconds and that glutamatergic neurons in the pontine central gray (PCG) play an important role in this process. These neurons exhibit higher sensitivity to auditory stimuli in sleep than wakefulness. Suppressing these neurons results in reduced sound-induced awakening and increased sleep in intrinsic sleep/wake cycles, whereas their activation induces ultra-fast awakening from sleep and accelerates awakening from anesthesia. Additionally, the sound-induced awakening can be attributed to the propagation of auditory signals from the PCG to multiple arousal-related regions, including the mediodorsal thalamus, lateral hypothalamus, and ventral tegmental area. Thus, the PCG serves as an essential distribution center to orchestrate a global auditory network to promote rapid awakening.</p>","PeriodicalId":11359,"journal":{"name":"Current Biology","volume":null,"pages":null},"PeriodicalIF":9.2,"publicationDate":"2024-09-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142216123","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Direct evidence of frugivory in the Mesozoic bird Longipteryx contradicts morphological proxies for diet","authors":"Jingmai O’Connor, Alexander Clark, Fabiany Herrera, Xin Yang, Xiaoli Wang, Xiaoting Zheng, Han Hu, Zhonghe Zhou","doi":"10.1016/j.cub.2024.08.012","DOIUrl":"https://doi.org/10.1016/j.cub.2024.08.012","url":null,"abstract":"<p>Diet is one of the most important aspects of an animal’s ecology, as it reflects direct interactions with other organisms and shapes morphology, behavior, and other life history traits. Modern birds (Neornithes) have a highly efficient and phenotypically plastic digestive system, allowing them to utilize diverse trophic resources, and digestive function has been put forth as a factor in the selectivity of the end-Cretaceous mass extinction, in which only neornithine dinosaurs survived.<span><span>¹</span></span> Although diet is directly documented in several early-diverging avian lineages,<span><span>²</span></span> only a single specimen preserves evidence of diet in Enantiornithes, the dominant group of terrestrial Cretaceous birds.<span><span>³</span></span> Morphology-based predictions suggest enantiornithines were faunivores,<span><span>⁴</span></span>^,<span><span>⁵</span></span>^,<span><span>⁶</span></span> although the absence of evidence contrasts with the high preservation potential and relatively longer gut-retention times of these diets. <em>Longipteryx</em> is an unusual Early Cretaceous enantiornithine with an elongate rostrum; distally restricted dentition<span><span>⁷</span></span>; large, recurved, and crenulated teeth<span><span>⁸</span></span>; and tooth enamel much thicker than other paravians.<span><span>⁹</span></span> Statistical analysis of rostral length, body size, and tooth morphology predicts <em>Longipteryx</em> was primarily insectivorous.<span><span>⁴</span></span>^,<span><span>⁵</span></span> Contrasting with these results, two new specimens of <em>Longipteryx</em> preserve gymnosperm seeds within the abdominal cavity interpreted as ingesta. Like <em>Jeholornis</em>, their unmacerated preservation and the absence of gastroliths indicate frugivory.<span><span>¹⁰</span></span> As in Neornithes,<span><span>¹¹</span></span> complex diets driven by the elevated energetic demands imposed by flight, secondary rostral functions, and phylogenetic influence impede the use of morphological proxies to predict diet in early-diverging avian lineages.</p>","PeriodicalId":11359,"journal":{"name":"Current Biology","volume":null,"pages":null},"PeriodicalIF":9.2,"publicationDate":"2024-09-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142216125","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Weight-induced radial growth in plant stems depends on PIN3","authors":"Àngela Carrió-Seguí, Paula Brunot-Garau, Cristina Úrbez, Pál Miskolczi, Francisco Vera-Sirera, Hannele Tuominen, Javier Agustí","doi":"10.1016/j.cub.2024.07.065","DOIUrl":"https://doi.org/10.1016/j.cub.2024.07.065","url":null,"abstract":"<p>How multiple growth programs coordinate during development is a fundamental question in biology. During plant stem development, radial growth is continuously adjusted in response to longitudinal-growth-derived weight increase to guarantee stability.<span><span>¹</span></span>^,<span><span>²</span></span>^,<span><span>³</span></span> Here, we demonstrate that weight-stimulated stem radial growth depends on the auxin efflux carrier PIN3, which, upon weight increase, expands its cellular localization from the lower to the lateral sides of xylem parenchyma, phloem, procambium, and starch sheath cells, imposing a radial auxin flux that results in radial growth. Using the protein synthesis inhibitor cycloheximide (CHX) or the fluorescent endocytic tracer FM4-64, we reveal that this expansion of the PIN3 cellular localization domain occurs because weight increase breaks the balance between PIN3 biosynthesis and removal, favoring PIN3 biosynthesis. Experimentation using brefeldin A (BFA) treatments or <em>arg1</em> and <em>arl2</em> mutants further supports this conclusion. Analyses of CRISPR-Cas9 lines for <em>Populus PIN3</em> orthologs reveals that PIN3 dependence of weight-induced radial growth is conserved at least in these woody species. Altogether, our work sheds new light on how longitudinal and radial growth coordinate during stem development.</p>","PeriodicalId":11359,"journal":{"name":"Current Biology","volume":null,"pages":null},"PeriodicalIF":9.2,"publicationDate":"2024-09-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142216124","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Developing zebrafish utilize taste-signaling pathways for oxygen chemoreception","authors":"Yihang Kevin Pan, Steve F. Perry","doi":"10.1016/j.cub.2024.08.015","DOIUrl":"https://doi.org/10.1016/j.cub.2024.08.015","url":null,"abstract":"<p>A fundamental requirement for all animals is to sense and respond to changes in environmental O₂ availability. Low O₂ (hypoxia) typically stimulates breathing, a universal and critical response termed the hypoxic ventilatory response (HVR). In this study, we test the hypothesis that taste-signaling pathways are used for O₂ sensing and activation of the HVR. We show that Merkel-like cells (MLCs), which are part of the taste-bud complex, function as O₂ chemoreceptor cells in larval zebrafish and that transduction of the O₂ signal uses taste-signaling pathways. Specifically, MLCs responded to hypoxia <em>in vivo</em> with an increase in Ca²⁺ activity that can drive the HVR. In addition, MLCs transmit O₂ signals to afferent cranial nerves IX and X (nIX/X), which project into the area postrema within the hindbrain and synapse with interneurons that are in contact with vagal motor neurons. Hypoxia or chemo-activation of nIX/X caused Ca²⁺ activity to increase within the area postrema and elicited hyperventilation. The results provide the first demonstration of an O₂ signaling pathway that commences with the activation of taste receptors (MLCs) to yield a critical physiological reflex, the HVR.</p>","PeriodicalId":11359,"journal":{"name":"Current Biology","volume":null,"pages":null},"PeriodicalIF":9.2,"publicationDate":"2024-09-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142216127","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}