Pub Date : 2024-12-16DOI: 10.1016/j.devcel.2024.11.013
Brent K. Young, Jeffrey L. Goldberg
Critical molecular pathways promote central nervous system (CNS) axon regeneration, but can axons be guided to their correct targets in adulthood? In this issue of Developmental Cell, Delpech et al. show that axonal guidance cues in the CNS can be manipulated to enhance anatomic and functional recovery.
{"title":"Axon guidance in central nervous system regeneration","authors":"Brent K. Young, Jeffrey L. Goldberg","doi":"10.1016/j.devcel.2024.11.013","DOIUrl":"https://doi.org/10.1016/j.devcel.2024.11.013","url":null,"abstract":"Critical molecular pathways promote central nervous system (CNS) axon regeneration, but can axons be guided to their correct targets in adulthood? In this issue of <em>Developmental Cell</em>, Delpech et al. show that axonal guidance cues in the CNS can be manipulated to enhance anatomic and functional recovery.","PeriodicalId":11157,"journal":{"name":"Developmental cell","volume":"51 1","pages":""},"PeriodicalIF":11.8,"publicationDate":"2024-12-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142825704","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}
Pub Date : 2024-12-16DOI: 10.1016/j.devcel.2024.11.018
Andrew C. Willoughby, Lucia C. Strader
Apical hook opening is crucial for seedling establishment and is regulated by unequal distribution of the hormone auxin through unknown mechanisms. In this issue of Developmental Cell, Walia et al.4 demonstrate that apical hook opening is an output of tissue-wide forces; auxin and cell wall integrity (CWI) signaling interact to restrict elongation to the concave side of the apical hook.
{"title":"Apical hook opening of plant seedlings: Unfolding the role of auxin and the cell wall","authors":"Andrew C. Willoughby, Lucia C. Strader","doi":"10.1016/j.devcel.2024.11.018","DOIUrl":"https://doi.org/10.1016/j.devcel.2024.11.018","url":null,"abstract":"Apical hook opening is crucial for seedling establishment and is regulated by unequal distribution of the hormone auxin through unknown mechanisms. In this issue of <em>Developmental Cell</em>, Walia et al.<span><span><sup>4</sup></span></span> demonstrate that apical hook opening is an output of tissue-wide forces; auxin and cell wall integrity (CWI) signaling interact to restrict elongation to the concave side of the apical hook.","PeriodicalId":11157,"journal":{"name":"Developmental cell","volume":"50 1","pages":""},"PeriodicalIF":11.8,"publicationDate":"2024-12-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142825705","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}
Pub Date : 2024-12-13DOI: 10.1016/j.devcel.2024.11.019
Caitlyn L. McCafferty, Ophelia Papoulas, Chanjae Lee, Khanh Huy Bui, David W. Taylor, Edward M. Marcotte, John B. Wallingford
Motile cilia are ancient, evolutionarily conserved organelles whose dysfunction underlies motile ciliopathies, a broad class of human diseases. Motile cilia contain a myriad of different proteins that assemble into an array of distinct machines, and understanding the interactions and functional hierarchies among them presents an important challenge. Here, we defined the protein interactome of motile axonemes using cross-linking mass spectrometry in Tetrahymena thermophila. From over 19,000 cross-links, we identified over 4,700 unique amino acid interactions among over 1,100 distinct proteins, providing both macromolecular and atomic-scale insights into diverse ciliary machines, including the intraflagellar transport system, axonemal dynein arms, radial spokes, the 96-nm ruler, and microtubule inner proteins. Guided by this dataset, we used vertebrate multiciliated cells to reveal functional interactions among several poorly defined human ciliopathy proteins. This dataset provides a resource for studying the biology of an ancient organelle and the molecular etiology of human genetic disease.
{"title":"An amino acid-resolution interactome for motile cilia identifies the structure and function of ciliopathy protein complexes","authors":"Caitlyn L. McCafferty, Ophelia Papoulas, Chanjae Lee, Khanh Huy Bui, David W. Taylor, Edward M. Marcotte, John B. Wallingford","doi":"10.1016/j.devcel.2024.11.019","DOIUrl":"https://doi.org/10.1016/j.devcel.2024.11.019","url":null,"abstract":"Motile cilia are ancient, evolutionarily conserved organelles whose dysfunction underlies motile ciliopathies, a broad class of human diseases. Motile cilia contain a myriad of different proteins that assemble into an array of distinct machines, and understanding the interactions and functional hierarchies among them presents an important challenge. Here, we defined the protein interactome of motile axonemes using cross-linking mass spectrometry in <em>Tetrahymena thermophila</em>. From over 19,000 cross-links, we identified over 4,700 unique amino acid interactions among over 1,100 distinct proteins, providing both macromolecular and atomic-scale insights into diverse ciliary machines, including the intraflagellar transport system, axonemal dynein arms, radial spokes, the 96-nm ruler, and microtubule inner proteins. Guided by this dataset, we used vertebrate multiciliated cells to reveal functional interactions among several poorly defined human ciliopathy proteins. This dataset provides a resource for studying the biology of an ancient organelle and the molecular etiology of human genetic disease.","PeriodicalId":11157,"journal":{"name":"Developmental cell","volume":"8 1","pages":""},"PeriodicalIF":11.8,"publicationDate":"2024-12-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142816456","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}
Pub Date : 2024-12-12DOI: 10.1016/j.devcel.2024.11.016
Christopher A. Brimson, Robert Baines, Elisabeth Sams-Dodd, Ioanina Stefanescu, Bethany Evans, Satoshi Kuwana, Hidenori Hashimura, Satoshi Sawai, Christopher R.L. Thompson
Oscillatory phenomena play widespread roles in the control of biological systems. In D. discoideum, oscillatory cyclic adenosine monophosphate (cAMP) signaling drives collective behavior and induces a temporal developmental gene expression program. How collective cAMP oscillations emerge or how they encode temporal transcriptional information is still poorly understood. To address this, we identified a transcription factor required for the initiation of collective behavior. Hbx5 activity is cAMP dependent and provides a sensitive single-cell readout for cAMP signaling. Extensive stochastic pulsatile cAMP signaling is found to precede collective oscillations. Stochastic signaling induces Hbx5-dependent transcriptional feedback, which enhances signal sensitivity and cell-cell coupling. This results in the emergence of synchronized collective oscillations, which subsequently activates the GtaC transcription factor and triggers shifts in developmental gene expression. Our results suggest this temporal coordination is encoded by changes in the amplitude of cAMP oscillations and differential sensitivity of these transcription factors to the cAMP-regulated kinase ErkB.
{"title":"Collective oscillatory signaling in Dictyostelium discoideum acts as a developmental timer initiated by weak coupling of a noisy pulsatile signal","authors":"Christopher A. Brimson, Robert Baines, Elisabeth Sams-Dodd, Ioanina Stefanescu, Bethany Evans, Satoshi Kuwana, Hidenori Hashimura, Satoshi Sawai, Christopher R.L. Thompson","doi":"10.1016/j.devcel.2024.11.016","DOIUrl":"https://doi.org/10.1016/j.devcel.2024.11.016","url":null,"abstract":"Oscillatory phenomena play widespread roles in the control of biological systems. In <em>D. discoideum</em>, oscillatory cyclic adenosine monophosphate (cAMP) signaling drives collective behavior and induces a temporal developmental gene expression program. How collective cAMP oscillations emerge or how they encode temporal transcriptional information is still poorly understood. To address this, we identified a transcription factor required for the initiation of collective behavior. Hbx5 activity is cAMP dependent and provides a sensitive single-cell readout for cAMP signaling. Extensive stochastic pulsatile cAMP signaling is found to precede collective oscillations. Stochastic signaling induces Hbx5-dependent transcriptional feedback, which enhances signal sensitivity and cell-cell coupling. This results in the emergence of synchronized collective oscillations, which subsequently activates the GtaC transcription factor and triggers shifts in developmental gene expression. Our results suggest this temporal coordination is encoded by changes in the amplitude of cAMP oscillations and differential sensitivity of these transcription factors to the cAMP-regulated kinase ErkB.","PeriodicalId":11157,"journal":{"name":"Developmental cell","volume":"1 1","pages":""},"PeriodicalIF":11.8,"publicationDate":"2024-12-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142809461","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}
Pub Date : 2024-12-11DOI: 10.1016/j.devcel.2024.11.017
Xiangyi Ke, Benjamin van Soldt, Lukas Vlahos, Yizhuo Zhou, Jun Qian, Joel George, Claudia Capdevila, Ian Glass, Kelley Yan, Andrea Califano, Wellington V. Cardoso
Transitional cell states are at the crossroads of crucial developmental and regenerative events, yet little is known about how these states emerge and influence outcomes. The alveolar and airway epithelia arise from distal lung multipotent progenitors, which undergo cell fate transitions to form these distinct compartments. The identification and impact of cell states in the developing lung are poorly understood. Here, we identified a population of Icam1/Nkx2-1 epithelial progenitors harboring a transitional state program remarkably conserved in humans and mice during lung morphogenesis and regeneration. Lineage-tracing and functional analyses reveal their role as progenitors to both airways and alveolar cells and the requirement of this transitional program to make distal lung progenitors competent to undergo airway cell fate specification. The identification of a common progenitor cell state in vastly distinct processes suggests a unified program reiteratively regulating outcomes in development and regeneration.
{"title":"Morphogenesis and regeneration share a conserved core transition cell state program that controls lung epithelial cell fate","authors":"Xiangyi Ke, Benjamin van Soldt, Lukas Vlahos, Yizhuo Zhou, Jun Qian, Joel George, Claudia Capdevila, Ian Glass, Kelley Yan, Andrea Califano, Wellington V. Cardoso","doi":"10.1016/j.devcel.2024.11.017","DOIUrl":"https://doi.org/10.1016/j.devcel.2024.11.017","url":null,"abstract":"Transitional cell states are at the crossroads of crucial developmental and regenerative events, yet little is known about how these states emerge and influence outcomes. The alveolar and airway epithelia arise from distal lung multipotent progenitors, which undergo cell fate transitions to form these distinct compartments. The identification and impact of cell states in the developing lung are poorly understood. Here, we identified a population of Icam1/Nkx2-1 epithelial progenitors harboring a transitional state program remarkably conserved in humans and mice during lung morphogenesis and regeneration. Lineage-tracing and functional <strong>analyses</strong> reveal their role as progenitors to both airways and alveolar cells and the requirement of this transitional program to make distal lung progenitors competent to undergo airway cell fate specification. The identification of a common progenitor cell state in vastly distinct processes suggests a unified program reiteratively regulating outcomes in development and regeneration.","PeriodicalId":11157,"journal":{"name":"Developmental cell","volume":"9 1","pages":""},"PeriodicalIF":11.8,"publicationDate":"2024-12-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142804892","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}
Pub Date : 2024-12-10DOI: 10.1016/j.devcel.2024.11.015
Alexa C. Blanchard, Anna Maximova, Taylor Phillips-Jones, Matthew R. Bruce, Pavlos Anastasiadis, Christie V. Dionisos, Kaliroi Engel, Erin Reinl, Aidan Pham, Sonia Malaiya, Nevil Singh, Seth Ament, Margaret M. McCarthy
Brain development is a non-linear process of regionally specific epochs occurring during windows of sensitivity to endogenous and exogenous stimuli. We have identified an epoch in the neonatal rat brain defined by a transient population of peri-hippocampal mast cells (phMCs) that are abundant from birth through 2-weeks post-natal but absent thereafter. The phMCs are maintained by proliferation and harbor a unique transcriptome compared with mast cells residing in the skin, bone marrow, or other brain regions. Pharmacological activation of this population broadly increases blood-brain barrier permeability, recruits peripheral immune cells, and stunts local microglia proliferation. Examination of the post-mortem human brain demonstrated mast cells in the peri-hippocampal region of a newborn, but not an older infant, suggesting a similar developmental period exists in humans. Mast cells specifically, and early-life inflammation generally, have been linked to heightened risk for neurodevelopmental disorders, and these results demonstrate a plausible source of that risk.
{"title":"Mast cells proliferate in the peri-hippocampal space during early development and modulate local and peripheral immune cells","authors":"Alexa C. Blanchard, Anna Maximova, Taylor Phillips-Jones, Matthew R. Bruce, Pavlos Anastasiadis, Christie V. Dionisos, Kaliroi Engel, Erin Reinl, Aidan Pham, Sonia Malaiya, Nevil Singh, Seth Ament, Margaret M. McCarthy","doi":"10.1016/j.devcel.2024.11.015","DOIUrl":"https://doi.org/10.1016/j.devcel.2024.11.015","url":null,"abstract":"Brain development is a non-linear process of regionally specific epochs occurring during windows of sensitivity to endogenous and exogenous stimuli. We have identified an epoch in the neonatal rat brain defined by a transient population of peri-hippocampal mast cells (phMCs) that are abundant from birth through 2-weeks post-natal but absent thereafter. The phMCs are maintained by proliferation and harbor a unique transcriptome compared with mast cells residing in the skin, bone marrow, or other brain regions. Pharmacological activation of this population broadly increases blood-brain barrier permeability, recruits peripheral immune cells, and stunts local microglia proliferation. Examination of the post-mortem human brain demonstrated mast cells in the peri-hippocampal region of a newborn, but not an older infant, suggesting a similar developmental period exists in humans. Mast cells specifically, and early-life inflammation generally, have been linked to heightened risk for neurodevelopmental disorders, and these results demonstrate a plausible source of that risk.","PeriodicalId":11157,"journal":{"name":"Developmental cell","volume":"22 1","pages":""},"PeriodicalIF":11.8,"publicationDate":"2024-12-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142797528","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}
Pub Date : 2024-12-10DOI: 10.1016/j.devcel.2024.11.014
Chiara M. Schröder, Lea Zissel, Sophie-Luise Mersiowsky, Mehmet Tekman, Simone Probst, Katrin M. Schüle, Sebastian Preissl, Oliver Schilling, H. Th. Marc Timmers, Sebastian J. Arnold
Mammalian pluripotent cells first segregate into neuroectoderm (NE), or mesoderm and endoderm (ME), characterized by lineage-specific transcriptional programs and chromatin states. To date, the relationship between transcription factor activities and dynamic chromatin changes that guide cell specification remains ill-defined. In this study, we employ mouse embryonic stem cell differentiation toward ME lineages to reveal crucial roles of the Tbx factor Eomes to globally establish ME enhancer accessibility as the prerequisite for ME lineage competence and ME-specific gene expression. EOMES cooperates with the SWItch/sucrose non-fermentable (SWI/SNF) complex to drive chromatin rewiring that is essential to overcome default NE differentiation, which is favored by asymmetries in chromatin accessibility at pluripotent state. Following global ME enhancer remodeling, ME-specific gene transcription is controlled by additional signals such as Wnt and transforming growth factor β (TGF-β)/NODAL, as a second layer of gene expression regulation, which can be mechanistically separated from initial chromatin remodeling activities.
{"title":"EOMES establishes mesoderm and endoderm differentiation potential through SWI/SNF-mediated global enhancer remodeling","authors":"Chiara M. Schröder, Lea Zissel, Sophie-Luise Mersiowsky, Mehmet Tekman, Simone Probst, Katrin M. Schüle, Sebastian Preissl, Oliver Schilling, H. Th. Marc Timmers, Sebastian J. Arnold","doi":"10.1016/j.devcel.2024.11.014","DOIUrl":"https://doi.org/10.1016/j.devcel.2024.11.014","url":null,"abstract":"Mammalian pluripotent cells first segregate into neuroectoderm (NE), or mesoderm and endoderm (ME), characterized by lineage-specific transcriptional programs and chromatin states. To date, the relationship between transcription factor activities and dynamic chromatin changes that guide cell specification remains ill-defined. In this study, we employ mouse embryonic stem cell differentiation toward ME lineages to reveal crucial roles of the Tbx factor <em>Eomes</em> to globally establish ME enhancer accessibility as the prerequisite for ME lineage competence and ME-specific gene expression. EOMES cooperates with the SWItch/sucrose non-fermentable (SWI/SNF) complex to drive chromatin rewiring that is essential to overcome default NE differentiation, which is favored by asymmetries in chromatin accessibility at pluripotent state. Following global ME enhancer remodeling, ME-specific gene transcription is controlled by additional signals such as Wnt and transforming growth factor β (TGF-β)/NODAL, as a second layer of gene expression regulation, which can be mechanistically separated from initial chromatin remodeling activities.","PeriodicalId":11157,"journal":{"name":"Developmental cell","volume":"10 1","pages":""},"PeriodicalIF":11.8,"publicationDate":"2024-12-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142797524","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}
Ependymal cells (ECs) are multiciliated cells in the brain that contribute to cerebrospinal fluid flow. ECs are specified during embryonic stages but differentiate later in development. Their differentiation depends on genes such as GEMC1 and MCIDAS in conjunction with E2F4/5 as well as on cell-cycle-related factors. In the mouse brain, we observe that nuclear deformation accompanies EC differentiation. Tampering with these deformations either by decreasing F-actin levels or by severing the link between the nucleus and the actin cytoskeleton blocks differentiation. Conversely, increasing F-actin by knocking out the Arp2/3 complex inhibitor Arpin or artificially deforming the nucleus activates differentiation. These data are consistent with actin polymerization triggering nuclear deformation and jump starting the signaling that produces ECs. A player in this process is the retinoblastoma 1 (RB1) protein, whose phosphorylation prompts MCIDAS activation. Overall, this study identifies a role for actin-based mechanical inputs to the nucleus as controlling factors in cell differentiation.
{"title":"Actin-based deformations of the nucleus control mouse multiciliated ependymal cell differentiation","authors":"Marianne Basso, Alexia Mahuzier, Syed Kaabir Ali, Anaïs Marty, Marion Faucourt, Ana-Maria Lennon-Duménil, Ayush Srivastava, Michella Khoury Damaa, Alexia Bankolé, Alice Meunier, Ayako Yamada, Julie Plastino, Nathalie Spassky, Nathalie Delgehyr","doi":"10.1016/j.devcel.2024.11.008","DOIUrl":"https://doi.org/10.1016/j.devcel.2024.11.008","url":null,"abstract":"Ependymal cells (ECs) are multiciliated cells in the brain that contribute to cerebrospinal fluid flow. ECs are specified during embryonic stages but differentiate later in development. Their differentiation depends on genes such as GEMC1 and MCIDAS in conjunction with E2F4/5 as well as on cell-cycle-related factors. In the mouse brain, we observe that nuclear deformation accompanies EC differentiation. Tampering with these deformations either by decreasing F-actin levels or by severing the link between the nucleus and the actin cytoskeleton blocks differentiation. Conversely, increasing F-actin by knocking out the Arp2/3 complex inhibitor Arpin or artificially deforming the nucleus activates differentiation. These data are consistent with actin polymerization triggering nuclear deformation and jump starting the signaling that produces ECs. A player in this process is the retinoblastoma 1 (RB1) protein, whose phosphorylation prompts MCIDAS activation. Overall, this study identifies a role for actin-based mechanical inputs to the nucleus as controlling factors in cell differentiation.","PeriodicalId":11157,"journal":{"name":"Developmental cell","volume":"20 1","pages":""},"PeriodicalIF":11.8,"publicationDate":"2024-12-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142797526","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}
Upon injury, both mammalian and plant cells activate a survival mechanism by sensing endogenous damage-associated molecular patterns (DAMPs). Plant elicitor peptides (Peps), a representative DAMP, are released from their precursors (PROPEPs; Precursors of Peps) through cleavage by metacaspases (MCs), but the control of Pep generation remains unclear. Here, we discovered that several PROPEPs in Arabidopsis thaliana are substrates for SUMOylation and that Ca2+ upregulates PROPEP1 SUMOylation, facilitated by the SUMO E3 ligase SAP and MIZ1 domain-containing ligase1 (SIZ1). Mutations at the SUMOylation site on PROPEP1, or at the SUMO-interacting motifs (SIMs) on its protease MC4, reduced the PROPEP1-MC4 association and PROPEP1 cleavage. Overexpression of the wild-type form, but not the SUMOylation-defective variant of PROPEP1, enhanced plant tolerance to cell wall damage. Consistently, SIZ1 contributes to PROPEP1 processing and cell wall damage responses. These findings support the idea that SUMOylation promotes PROPEP1 cleavage via MC4 and provide insights into how DAMP generation is controlled in eukaryotic cells.
{"title":"SUMOylation controls peptide processing to generate damage-associated molecular patterns in Arabidopsis","authors":"Cheng Zhang, Yuanyuan Wu, Jiuer Liu, Bing Song, Zhibo Yu, Jian-Feng Li, Chengwei Yang, Jianbin Lai","doi":"10.1016/j.devcel.2024.11.010","DOIUrl":"https://doi.org/10.1016/j.devcel.2024.11.010","url":null,"abstract":"Upon injury, both mammalian and plant cells activate a survival mechanism by sensing endogenous damage-associated molecular patterns (DAMPs). Plant elicitor peptides (Peps), a representative DAMP, are released from their precursors (PROPEPs; Precursors of Peps) through cleavage by metacaspases (MCs), but the control of Pep generation remains unclear. Here, we discovered that several PROPEPs in <em>Arabidopsis thaliana</em> are substrates for SUMOylation and that Ca<sup>2+</sup> upregulates PROPEP1 SUMOylation, facilitated by the SUMO E3 ligase SAP and MIZ1 domain-containing ligase1 (SIZ1). Mutations at the SUMOylation site on PROPEP1, or at the SUMO-interacting motifs (SIMs) on its protease MC4, reduced the PROPEP1-MC4 association and PROPEP1 cleavage. Overexpression of the wild-type form, but not the SUMOylation-defective variant of PROPEP1, enhanced plant tolerance to cell wall damage. Consistently, SIZ1 contributes to PROPEP1 processing and cell wall damage responses. These findings support the idea that SUMOylation promotes PROPEP1 cleavage via MC4 and provide insights into how DAMP generation is controlled in eukaryotic cells.","PeriodicalId":11157,"journal":{"name":"Developmental cell","volume":"55 1","pages":""},"PeriodicalIF":11.8,"publicationDate":"2024-12-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142793548","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}
Pub Date : 2024-12-09DOI: 10.1016/j.devcel.2024.11.011
Ava Niazi, Ju Ang Kim, Dong-Kyu Kim, Di Lu, Igal Sterin, Joosang Park, Sungjin Park
The apical extracellular matrix (aECM), organized by polarized epithelial cells, exhibits complex structures. The tectorial membrane (TM), an aECM in the cochlea mediating auditory transduction, exhibits highly ordered domain-specific architecture. α-Tectorin (TECTA), a glycosylphosphatidylinositol (GPI)-anchored ECM protein, is essential for TM organization. Here, we identified that α-tectorin is released by distinct modes: proteolytic shedding by TMPRSS2 and GPI-anchor-dependent release from the microvillus tip in mice. In the medial/limbal domain, proteolytically shed α-tectorin forms dense fibers. In contrast, in the lateral/body domain, where supporting cells exhibit dense microvilli, shedding restricts α-tectorin to the microvillus tip, compartmentalizing collagen-binding sites. Tip-localized α-tectorin is released in a GPI-anchor-dependent manner to form collagen-crosslinking fibers, maintaining the spacing and parallel organization of collagen fibrils. Overall, these distinct release modes of α-tectorin determine domain-specific organization, with the microvillus coordinating release modes along its membrane to assemble the higher-order ECM architecture.
{"title":"Microvilli control the morphogenesis of the tectorial membrane extracellular matrix","authors":"Ava Niazi, Ju Ang Kim, Dong-Kyu Kim, Di Lu, Igal Sterin, Joosang Park, Sungjin Park","doi":"10.1016/j.devcel.2024.11.011","DOIUrl":"https://doi.org/10.1016/j.devcel.2024.11.011","url":null,"abstract":"The apical extracellular matrix (aECM), organized by polarized epithelial cells, exhibits complex structures. The tectorial membrane (TM), an aECM in the cochlea mediating auditory transduction, exhibits highly ordered domain-specific architecture. α-Tectorin (TECTA), a glycosylphosphatidylinositol (GPI)-anchored ECM protein, is essential for TM organization. Here, we identified that α-tectorin is released by distinct modes: proteolytic shedding by TMPRSS2 and GPI-anchor-dependent release from the microvillus tip in mice. In the medial/limbal domain, proteolytically shed α-tectorin forms dense fibers. In contrast, in the lateral/body domain, where supporting cells exhibit dense microvilli, shedding restricts α-tectorin to the microvillus tip, compartmentalizing collagen-binding sites. Tip-localized α-tectorin is released in a GPI-anchor-dependent manner to form collagen-crosslinking fibers, maintaining the spacing and parallel organization of collagen fibrils. Overall, these distinct release modes of α-tectorin determine domain-specific organization, with the microvillus coordinating release modes along its membrane to assemble the higher-order ECM architecture.","PeriodicalId":11157,"journal":{"name":"Developmental cell","volume":"83 1","pages":""},"PeriodicalIF":11.8,"publicationDate":"2024-12-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142793545","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}
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