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}
Pub Date : 2024-12-06DOI: 10.1016/j.devcel.2024.11.009
Hanyang Cai, Kaichuang Liu, Suzhuo Ma, Han Su, Jiahong Yang, Ling Sun, Ziqi Liu, Yuan Qin
How do growth hormones interact to specify female-germline cell types in flowering plants and control production of the first female-germline cell? Here, we find that gibberellin (GA) biosynthesis and signaling are restricted in ovule primordia, with overexpression of receptors and biosynthetic enzymes resulting in multiple and enlarged megaspore mother cells (MMCs) in Arabidopsis. GA signaling machinery interacts with and promotes the degradation of cytokinin (CK) type-B Arabidopsis response regulators (ARR1/10/12), which also directly interact with DELLA proteins. CK biosynthesis and signaling components are expressed in both MMCs and sporophytic cells, with signaling negatively controlled by GA in ovule primordia, and perturbations leading to the induction of multiple, enlarged MMC-like cells. The vacuolar sorting protein SHRUBBY (SHBY) interacts with GA and CK signaling components to block GA-induced degradation. CK signaling restricts multiple sub-epidermal cells in distal ovule primordia from acquiring MMC identity. By balancing degradation activity, GA and CK signaling antagonistically control female-germline cell specification.
{"title":"Gibberellin and cytokinin signaling antagonistically control female-germline cell specification in Arabidopsis","authors":"Hanyang Cai, Kaichuang Liu, Suzhuo Ma, Han Su, Jiahong Yang, Ling Sun, Ziqi Liu, Yuan Qin","doi":"10.1016/j.devcel.2024.11.009","DOIUrl":"https://doi.org/10.1016/j.devcel.2024.11.009","url":null,"abstract":"How do growth hormones interact to specify female-germline cell types in flowering plants and control production of the first female-germline cell? Here, we find that gibberellin (GA) biosynthesis and signaling are restricted in ovule primordia, with overexpression of receptors and biosynthetic enzymes resulting in multiple and enlarged megaspore mother cells (MMCs) in <em>Arabidopsis</em>. GA signaling machinery interacts with and promotes the degradation of cytokinin (CK) type-B <em>Arabidopsis</em> response regulators (ARR1/10/12), which also directly interact with DELLA proteins. CK biosynthesis and signaling components are expressed in both MMCs and sporophytic cells, with signaling negatively controlled by GA in ovule primordia, and perturbations leading to the induction of multiple, enlarged MMC-like cells. The vacuolar sorting protein SHRUBBY (SHBY) interacts with GA and CK signaling components to block GA-induced degradation. CK signaling restricts multiple sub-epidermal cells in distal ovule primordia from acquiring MMC identity. By balancing degradation activity, GA and CK signaling antagonistically control female-germline cell specification.","PeriodicalId":11157,"journal":{"name":"Developmental cell","volume":"243 1","pages":""},"PeriodicalIF":11.8,"publicationDate":"2024-12-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142782650","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 : 2024-12-05DOI: 10.1016/j.devcel.2024.11.007
Haengdueng Jeong, Buhyun Lee, Soo Young Cho, Yura Lee, Jiseon Kim, Sumin Hur, Kyungrae Cho, Kwang H. Kim, Sung-Hee Kim, Ki Taek Nam
The gastric mucosa is a highly dynamic tissue that undergoes constant self-renewal through stem cell differentiation. Chief cells maintain a quiescent state in homeostasis but are responsible for regeneration after injury. Although the role of microbiome-host interactions in the intestine is well studied, less is known about these interactions in the stomach. Using the mouse organoid and germ-free mouse models, we show that microbiota-derived short-chain fatty acids (SCFAs) suppress the proliferation of chief cells in mice. This effect is mediated by activation of G-protein-coupled receptor 43. Most importantly, through metabolomics and transplantation studies, we show butyrate-producing Lactobacillus intestinalis modulates the proliferation of chief cells in mice. Our findings identify a mechanism by which the microbiota regulates the cell characteristics of chief cells, providing insight into the complex interplay between the host and its microbial environment and the mechanisms underlying gastric homeostasis, with potential therapeutic implications for gastric diseases.
{"title":"Microbiota-derived short-chain fatty acids determine stem cell characteristics of gastric chief cells","authors":"Haengdueng Jeong, Buhyun Lee, Soo Young Cho, Yura Lee, Jiseon Kim, Sumin Hur, Kyungrae Cho, Kwang H. Kim, Sung-Hee Kim, Ki Taek Nam","doi":"10.1016/j.devcel.2024.11.007","DOIUrl":"https://doi.org/10.1016/j.devcel.2024.11.007","url":null,"abstract":"The gastric mucosa is a highly dynamic tissue that undergoes constant self-renewal through stem cell differentiation. Chief cells maintain a quiescent state in homeostasis but are responsible for regeneration after injury. Although the role of microbiome-host interactions in the intestine is well studied, less is known about these interactions in the stomach. Using the mouse organoid and germ-free mouse models, we show that microbiota-derived short-chain fatty acids (SCFAs) suppress the proliferation of chief cells in mice. This effect is mediated by activation of G-protein-coupled receptor 43. Most importantly, through metabolomics and transplantation studies, we show butyrate-producing <em>Lactobacillus intestinalis</em> modulates the proliferation of chief cells in mice. Our findings identify a mechanism by which the microbiota regulates the cell characteristics of chief cells, providing insight into the complex interplay between the host and its microbial environment and the mechanisms underlying gastric homeostasis, with potential therapeutic implications for gastric diseases.","PeriodicalId":11157,"journal":{"name":"Developmental cell","volume":"16 1","pages":""},"PeriodicalIF":11.8,"publicationDate":"2024-12-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142776811","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 : 2024-12-05DOI: 10.1016/j.devcel.2024.11.006
Can Li, Jase Gehring, Marianne E. Bronner
Neural crest cells give rise to the neurons of the enteric nervous system (ENS) that innervate the gastrointestinal (GI) tract to regulate gut motility. The immense size and distinct subregions of the gut present a challenge to understanding the spatial organization and sequential differentiation of different neuronal subtypes. Here, we profile enteric neurons (ENs) and progenitors at single-cell resolution during zebrafish embryonic and larval development to provide a near-complete picture of transcriptional changes that accompany the emergence of ENS neurons throughout the GI tract. Multiplex spatial RNA transcript analysis identifies the temporal order and distinct localization patterns of neuronal subtypes along the length of the gut. Finally, we show that functional perturbation of select transcription factors Ebf1a, Gata3, and Satb2 alters the cell fate choice, respectively, of inhibitory, excitatory, and serotonergic neuronal subtypes in the developing ENS.
{"title":"Spatiotemporal dynamics of the developing zebrafish enteric nervous system at the whole-organ level","authors":"Can Li, Jase Gehring, Marianne E. Bronner","doi":"10.1016/j.devcel.2024.11.006","DOIUrl":"https://doi.org/10.1016/j.devcel.2024.11.006","url":null,"abstract":"Neural crest cells give rise to the neurons of the enteric nervous system (ENS) that innervate the gastrointestinal (GI) tract to regulate gut motility. The immense size and distinct subregions of the gut present a challenge to understanding the spatial organization and sequential differentiation of different neuronal subtypes. Here, we profile enteric neurons (ENs) and progenitors at single-cell resolution during zebrafish embryonic and larval development to provide a near-complete picture of transcriptional changes that accompany the emergence of ENS neurons throughout the GI tract. Multiplex spatial RNA transcript analysis identifies the temporal order and distinct localization patterns of neuronal subtypes along the length of the gut. Finally, we show that functional perturbation of select transcription factors <em>Ebf1a</em>, <em>Gata3</em>, and <em>Satb2</em> alters the cell fate choice, respectively, of inhibitory, excitatory, and serotonergic neuronal subtypes in the developing ENS.","PeriodicalId":11157,"journal":{"name":"Developmental cell","volume":"27 1","pages":""},"PeriodicalIF":11.8,"publicationDate":"2024-12-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142776466","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 : 2024-12-03DOI: 10.1016/j.devcel.2024.11.005
Ke Zhou, Fangming Wu, Lei Deng, Yu Xiao, Wentao Yang, Jiuhai Zhao, Qinyang Wang, Zeqian Chang, Huawei Zhai, Chuanlong Sun, Hongyu Han, Minmin Du, Qian Chen, Jijun Yan, Peiyong Xin, Jinfang Chu, Zhifu Han, Jijie Chai, Gregg A. Howe, Chang-Bao Li, Chuanyou Li
Pattern recognition receptor (PRR)-mediated perception of damage-associated molecular patterns (DAMPs) triggers the first line of inducible defenses in both plants and animals. Compared with animals, plants are sessile and regularly encounter physical damage by biotic and abiotic factors. A longstanding problem concerns how plants achieve a balance between wound defense response and normal growth, avoiding overcommitment to catastrophic defense. Here, we report that two antagonistic systemin receptors, SYR1 and SYR2, of the wound peptide hormone systemin in tomato act in a ligand-concentration-dependent manner to regulate immune homeostasis. Whereas SYR1 acts as a high-affinity receptor to initiate systemin signaling, SYR2 functions as a low-affinity receptor to attenuate systemin signaling. The expression of systemin and SYR2, but not SYR1, is upregulated upon SYR1 activation. Our findings provide a mechanistic explanation for how plants appropriately respond to tissue damage based on PRR-mediated perception of DAMP concentrations and have implications for uncoupling defense-growth trade-offs.
{"title":"Antagonistic systemin receptors integrate the activation and attenuation of systemic wound signaling in tomato","authors":"Ke Zhou, Fangming Wu, Lei Deng, Yu Xiao, Wentao Yang, Jiuhai Zhao, Qinyang Wang, Zeqian Chang, Huawei Zhai, Chuanlong Sun, Hongyu Han, Minmin Du, Qian Chen, Jijun Yan, Peiyong Xin, Jinfang Chu, Zhifu Han, Jijie Chai, Gregg A. Howe, Chang-Bao Li, Chuanyou Li","doi":"10.1016/j.devcel.2024.11.005","DOIUrl":"https://doi.org/10.1016/j.devcel.2024.11.005","url":null,"abstract":"Pattern recognition receptor (PRR)-mediated perception of damage-associated molecular patterns (DAMPs) triggers the first line of inducible defenses in both plants and animals. Compared with animals, plants are sessile and regularly encounter physical damage by biotic and abiotic factors. A longstanding problem concerns how plants achieve a balance between wound defense response and normal growth, avoiding overcommitment to catastrophic defense. Here, we report that two antagonistic systemin receptors, SYR1 and SYR2, of the wound peptide hormone systemin in tomato act in a ligand-concentration-dependent manner to regulate immune homeostasis. Whereas SYR1 acts as a high-affinity receptor to initiate systemin signaling, SYR2 functions as a low-affinity receptor to attenuate systemin signaling. The expression of systemin and SYR2, but not SYR1, is upregulated upon SYR1 activation. Our findings provide a mechanistic explanation for how plants appropriately respond to tissue damage based on PRR-mediated perception of DAMP concentrations and have implications for uncoupling defense-growth trade-offs.","PeriodicalId":11157,"journal":{"name":"Developmental cell","volume":"82 1","pages":""},"PeriodicalIF":11.8,"publicationDate":"2024-12-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142760669","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 : 2024-12-03DOI: 10.1016/j.devcel.2024.11.002
Biruk A. Feyissa, Elsa M. de Becker, Coralie E. Salesse-Smith, Jin Zhang, Timothy B. Yates, Meng Xie, Kuntal De, Dhananjay Gotarkar, Margot S.S. Chen, Sara S. Jawdy, Dana L. Carper, Kerrie Barry, Jeremy Schmutz, David J. Weston, Paul E. Abraham, Chung-Jui Tsai, Jennifer L. Morrell-Falvey, Gail Taylor, Jin-Gui Chen, Gerald A. Tuskan, Wellington Muchero
Organelle-to-nucleus DNA transfer is an ongoing process playing an important role in the evolution of eukaryotic life. Here, genome-wide association studies (GWAS) of non-photochemical quenching parameters in 743 Populus trichocarpa accessions identified a nuclear-encoded genomic region associated with variation in photosynthesis under fluctuating light. The identified gene, BOOSTER (BSTR), comprises three exons, two with apparent endophytic origin and the third containing a large fragment of plastid-encoded Rubisco large subunit. Higher expression of BSTR facilitated anterograde signaling between nucleus and plastid, which corresponded to enhanced expression of Rubisco, increased photosynthesis, and up to 35% greater plant height and 88% biomass in poplar accessions under field conditions. Overexpression of BSTR in Populus tremula × P. alba achieved up to a 200% in plant height. Similarly, Arabidopsis plants heterologously expressing BSTR gained up to 200% in biomass and up to 50% increase in seed.
{"title":"An orphan gene BOOSTER enhances photosynthetic efficiency and plant productivity","authors":"Biruk A. Feyissa, Elsa M. de Becker, Coralie E. Salesse-Smith, Jin Zhang, Timothy B. Yates, Meng Xie, Kuntal De, Dhananjay Gotarkar, Margot S.S. Chen, Sara S. Jawdy, Dana L. Carper, Kerrie Barry, Jeremy Schmutz, David J. Weston, Paul E. Abraham, Chung-Jui Tsai, Jennifer L. Morrell-Falvey, Gail Taylor, Jin-Gui Chen, Gerald A. Tuskan, Wellington Muchero","doi":"10.1016/j.devcel.2024.11.002","DOIUrl":"https://doi.org/10.1016/j.devcel.2024.11.002","url":null,"abstract":"Organelle-to-nucleus DNA transfer is an ongoing process playing an important role in the evolution of eukaryotic life. Here, genome-wide association studies (GWAS) of non-photochemical quenching parameters in 743 <em>Populus trichocarpa</em> accessions identified a nuclear-encoded genomic region associated with variation in photosynthesis under fluctuating light. The identified gene, <em>BOOSTER</em> (<em>BSTR</em>), comprises three exons, two with apparent endophytic origin and the third containing a large fragment of plastid-encoded Rubisco large subunit. Higher expression of <em>BSTR</em> facilitated anterograde signaling between nucleus and plastid, which corresponded to enhanced expression of Rubisco, increased photosynthesis, and up to 35% greater plant height and 88% biomass in poplar accessions under field conditions. Overexpression of <em>BSTR</em> in <em>Populus tremula</em> × <em>P. alba</em> achieved up to a 200% in plant height. Similarly, <em>Arabidopsis</em> plants heterologously expressing <em>BSTR</em> gained up to 200% in biomass and up to 50% increase in seed.","PeriodicalId":11157,"journal":{"name":"Developmental cell","volume":"261 1","pages":""},"PeriodicalIF":11.8,"publicationDate":"2024-12-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142760182","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 : 2024-12-02DOI: 10.1016/j.devcel.2024.09.019
Dan Lu, Yuxin Yin
In this issue of Developmental Cell, Zhang et al. report that secreted PTEN reprograms immunosuppressive tumor-associated macrophages into an inflammatory phenotype by binding to PLXDC2, which enhances antitumor immunity. This Preview discusses diverse functions of PTEN in the nucleus, cytoplasm, and extracellular matrix, highlighting its multifaceted roles in cancer.
{"title":"From nuclear to extracellular PTEN: Multiple roles in tumor suppression and immune modulation","authors":"Dan Lu, Yuxin Yin","doi":"10.1016/j.devcel.2024.09.019","DOIUrl":"https://doi.org/10.1016/j.devcel.2024.09.019","url":null,"abstract":"In this issue of <em>Developmental Cell</em>, Zhang et al. report that secreted PTEN reprograms immunosuppressive tumor-associated macrophages into an inflammatory phenotype by binding to PLXDC2, which enhances antitumor immunity. This Preview discusses diverse functions of PTEN in the nucleus, cytoplasm, and extracellular matrix, highlighting its multifaceted roles in cancer.","PeriodicalId":11157,"journal":{"name":"Developmental cell","volume":"174 1","pages":""},"PeriodicalIF":11.8,"publicationDate":"2024-12-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142760424","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 : 2024-11-29DOI: 10.1016/j.devcel.2024.11.001
Stephanie Cheung, Danila Bredikhin, Tobias Gerber, Petrus J. Steenbergen, Soham Basu, Richard Bailleul, Pauline Hansen, Alexandre Paix, Matthew A. Benton, Hendrik C. Korswagen, Detlev Arendt, Oliver Stegle, Aissam Ikmi
The complexity of regeneration extends beyond local wound responses, eliciting systemic processes across the entire organism. However, the functional relevance and coordination of distant molecular processes remain unclear. In the cnidarian Nematostella vectensis, we show that local regeneration triggers a systemic homeostatic response, leading to coordinated whole-body remodeling. Leveraging spatial transcriptomics, endogenous protein tagging, and live imaging, we comprehensively dissect this systemic response at the organismal scale. We identify proteolysis as a critical process driven by both local and systemic upregulation of metalloproteases. We show that metalloproteinase expression levels and activity scale with the extent of tissue loss. This proportional response drives long-range tissue and extracellular matrix movement. Our findings demonstrate the adaptive nature of the systematic response in regeneration, enabling the organism to maintain shape homeostasis while coping with a wide range of injuries.
{"title":"Systemic coordination of whole-body tissue remodeling during local regeneration in sea anemones","authors":"Stephanie Cheung, Danila Bredikhin, Tobias Gerber, Petrus J. Steenbergen, Soham Basu, Richard Bailleul, Pauline Hansen, Alexandre Paix, Matthew A. Benton, Hendrik C. Korswagen, Detlev Arendt, Oliver Stegle, Aissam Ikmi","doi":"10.1016/j.devcel.2024.11.001","DOIUrl":"https://doi.org/10.1016/j.devcel.2024.11.001","url":null,"abstract":"The complexity of regeneration extends beyond local wound responses, eliciting systemic processes across the entire organism. However, the functional relevance and coordination of distant molecular processes remain unclear. In the cnidarian <em>Nematostella vectensis</em>, we show that local regeneration triggers a systemic homeostatic response, leading to coordinated whole-body remodeling. Leveraging spatial transcriptomics, endogenous protein tagging, and live imaging, we comprehensively dissect this systemic response at the organismal scale. We identify proteolysis as a critical process driven by both local and systemic upregulation of metalloproteases. We show that metalloproteinase expression levels and activity scale with the extent of tissue loss. This proportional response drives long-range tissue and extracellular matrix movement. Our findings demonstrate the adaptive nature of the systematic response in regeneration, enabling the organism to maintain shape homeostasis while coping with a wide range of injuries.","PeriodicalId":11157,"journal":{"name":"Developmental cell","volume":"195 1","pages":""},"PeriodicalIF":11.8,"publicationDate":"2024-11-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142742610","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 : 2024-11-27DOI: 10.1016/j.devcel.2024.11.003
M. Fethullah Simsek, Didar Saparov, Kemal Keseroglu, Oriana Zinani, Angad Singh Chandel, Bibek Dulal, Bal Krishan Sharma, Soling Zimik, Ertuğrul M. Özbudak
Pulsatile activity of the extracellular signal-regulated kinase (ERK) controls several cellular, developmental, and regenerative programs. Sequential segmentation of somites along the vertebrate body axis, a key developmental program, is also controlled by ERK activity oscillation. The oscillatory expression of Her/Hes family transcription factors constitutes the segmentation clock, setting the period of segmentation. Although oscillation of ERK activity depends on Her/Hes proteins, the underlying molecular mechanism remained mysterious. Here, we show that Her/Hes proteins physically interact with and stabilize dual-specificity phosphatases (Dusp) of ERK, resulting in oscillations of Dusp4 and Dusp6 proteins. Pharmaceutical and genetic inhibition of Dusp activity disrupt ERK activity oscillation and somite segmentation in zebrafish. Our results demonstrate that post-translational interactions of Her/Hes transcription factors with Dusp phosphatases establish the fundamental vertebrate body plan. We anticipate that future studies will identify currently unnoticed post-translational control of ERK pulses in other systems.
{"title":"The vertebrate segmentation clock drives segmentation by stabilizing Dusp phosphatases in zebrafish","authors":"M. Fethullah Simsek, Didar Saparov, Kemal Keseroglu, Oriana Zinani, Angad Singh Chandel, Bibek Dulal, Bal Krishan Sharma, Soling Zimik, Ertuğrul M. Özbudak","doi":"10.1016/j.devcel.2024.11.003","DOIUrl":"https://doi.org/10.1016/j.devcel.2024.11.003","url":null,"abstract":"Pulsatile activity of the extracellular signal-regulated kinase (ERK) controls several cellular, developmental, and regenerative programs. Sequential segmentation of somites along the vertebrate body axis, a key developmental program, is also controlled by ERK activity oscillation. The oscillatory expression of Her/Hes family transcription factors constitutes the segmentation clock, setting the period of segmentation. Although oscillation of ERK activity depends on Her/Hes proteins, the underlying molecular mechanism remained mysterious. Here, we show that Her/Hes proteins physically interact with and stabilize dual-specificity phosphatases (Dusp) of ERK, resulting in oscillations of Dusp4 and Dusp6 proteins. Pharmaceutical and genetic inhibition of Dusp activity disrupt ERK activity oscillation and somite segmentation in zebrafish. Our results demonstrate that post-translational interactions of Her/Hes transcription factors with Dusp phosphatases establish the fundamental vertebrate body plan. We anticipate that future studies will identify currently unnoticed post-translational control of ERK pulses in other systems.","PeriodicalId":11157,"journal":{"name":"Developmental cell","volume":"8 1","pages":""},"PeriodicalIF":11.8,"publicationDate":"2024-11-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142718619","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 : 2024-11-26DOI: 10.1016/j.devcel.2024.10.025
Eliza C.B. Jaeger, David Vijatovic, Astrid Deryckere, Nikol Zorin, Akemi L. Nguyen, Georgiy Ivanian, Jamie Woych, Rebecca C. Arnold, Alonso Ortega Gurrola, Arik Shvartsman, Francesca Barbieri, Florina A. Toma, Hollis T. Cline, Timothy F. Shay, Darcy B. Kelley, Ayako Yamaguchi, Mark Shein-Idelson, Maria Antonietta Tosches, Lora B. Sweeney
Amphibians, by virtue of their phylogenetic position, provide invaluable insights on nervous system evolution, development, and remodeling. The genetic toolkit for amphibians, however, remains limited. Recombinant adeno-associated viral vectors (AAVs) are a powerful alternative to transgenesis for labeling and manipulating neurons. Although successful in mammals, AAVs have never been shown to transduce amphibian cells efficiently. We screened AAVs in three amphibian species—the frogs Xenopus laevis and Pelophylax bedriagae and the salamander Pleurodeles waltl—and identified at least two AAV serotypes per species that transduce neurons. In developing amphibians, AAVs labeled groups of neurons generated at the same time during development. In the mature brain, AAVrg retrogradely traced long-range projections. Our study introduces AAVs as a tool for amphibian research, establishes a generalizable workflow for AAV screening in new species, and expands opportunities for cross-species comparisons of nervous system development, function, and evolution.
{"title":"Adeno-associated viral tools to trace neural development and connectivity across amphibians","authors":"Eliza C.B. Jaeger, David Vijatovic, Astrid Deryckere, Nikol Zorin, Akemi L. Nguyen, Georgiy Ivanian, Jamie Woych, Rebecca C. Arnold, Alonso Ortega Gurrola, Arik Shvartsman, Francesca Barbieri, Florina A. Toma, Hollis T. Cline, Timothy F. Shay, Darcy B. Kelley, Ayako Yamaguchi, Mark Shein-Idelson, Maria Antonietta Tosches, Lora B. Sweeney","doi":"10.1016/j.devcel.2024.10.025","DOIUrl":"https://doi.org/10.1016/j.devcel.2024.10.025","url":null,"abstract":"Amphibians, by virtue of their phylogenetic position, provide invaluable insights on nervous system evolution, development, and remodeling. The genetic toolkit for amphibians, however, remains limited. Recombinant adeno-associated viral vectors (AAVs) are a powerful alternative to transgenesis for labeling and manipulating neurons. Although successful in mammals, AAVs have never been shown to transduce amphibian cells efficiently. We screened AAVs in three amphibian species—the frogs <em>Xenopus laevis</em> and <em>Pelophylax bedriagae</em> and the salamander <em>Pleurodeles waltl</em>—and identified at least two AAV serotypes per species that transduce neurons. In developing amphibians, AAVs labeled groups of neurons generated at the same time during development. In the mature brain, AAVrg retrogradely traced long-range projections. Our study introduces AAVs as a tool for amphibian research, establishes a generalizable workflow for AAV screening in new species, and expands opportunities for cross-species comparisons of nervous system development, function, and evolution.","PeriodicalId":11157,"journal":{"name":"Developmental cell","volume":"7 1","pages":""},"PeriodicalIF":11.8,"publicationDate":"2024-11-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142713094","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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