宿主 GTPase Dynamin 2 可调节顶端连接结构,从而控制李斯特菌在细胞间的传播。

IF 2.9 3区 医学 Q3 IMMUNOLOGY
Infection and Immunity Pub Date : 2024-10-15 Epub Date: 2024-08-12 DOI:10.1128/iai.00136-24
Serena Tijoriwalla, Thiloma Liyanage, Thilina U B Herath, Nicole Lee, Attika Rehman, Antonella Gianfelice, Keith Ireton
{"title":"宿主 GTPase Dynamin 2 可调节顶端连接结构,从而控制李斯特菌在细胞间的传播。","authors":"Serena Tijoriwalla, Thiloma Liyanage, Thilina U B Herath, Nicole Lee, Attika Rehman, Antonella Gianfelice, Keith Ireton","doi":"10.1128/iai.00136-24","DOIUrl":null,"url":null,"abstract":"<p><p>The food-borne pathogen <i>Listeria monocytogenes</i> uses actin-based motility to generate plasma membrane protrusions that mediate the spread of bacteria between host cells. In polarized epithelial cells, efficient protrusion formation by <i>L. monocytogenes</i> requires the secreted bacterial protein InlC, which binds to a carboxyl-terminal Src homology 3 (SH3) domain in the human scaffolding protein Tuba. This interaction antagonizes Tuba, thereby diminishing cortical tension at the apical junctional complex and enhancing <i>L. monocytogenes</i> protrusion formation and spread. Tuba contains five SH3 domains apart from the domain that interacts with InlC. Here, we show that human GTPase Dynamin 2 associates with two SH3 domains in the amino-terminus of Tuba and acts together with this scaffolding protein to control the spread of <i>L. monocytogenes</i>. Genetic or pharmacological inhibition of Dynamin 2 or knockdown of Tuba each restored normal protrusion formation and spread to a bacterial strain deleted for the <i>inlC</i> gene (∆<i>inlC</i>). Dynamin 2 localized to apical junctions in uninfected human cells and protrusions in cells infected with <i>L. monocytogenes</i>. Localization of Dynamin 2 to junctions and protrusions depended on Tuba. Knockdown of Dynamin 2 or Tuba diminished junctional linearity, indicating a role for these proteins in controlling cortical tension. Infection with <i>L. monocytogenes</i> induced InlC-dependent displacement of Dynamin 2 from junctions, suggesting a possible mechanism of antagonism of this GTPase. Collectively, our results show that Dynamin 2 cooperates with Tuba to promote intercellular tension that restricts the spread of ∆<i>inlC Listeria</i>. By expressing InlC, wild-type <i>L. monocytogenes</i> overcomes this restriction.</p>","PeriodicalId":13541,"journal":{"name":"Infection and Immunity","volume":null,"pages":null},"PeriodicalIF":2.9000,"publicationDate":"2024-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11475654/pdf/","citationCount":"0","resultStr":"{\"title\":\"The host GTPase Dynamin 2 modulates apical junction structure to control cell-to-cell spread of <i>Listeria monocytogenes</i>.\",\"authors\":\"Serena Tijoriwalla, Thiloma Liyanage, Thilina U B Herath, Nicole Lee, Attika Rehman, Antonella Gianfelice, Keith Ireton\",\"doi\":\"10.1128/iai.00136-24\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>The food-borne pathogen <i>Listeria monocytogenes</i> uses actin-based motility to generate plasma membrane protrusions that mediate the spread of bacteria between host cells. In polarized epithelial cells, efficient protrusion formation by <i>L. monocytogenes</i> requires the secreted bacterial protein InlC, which binds to a carboxyl-terminal Src homology 3 (SH3) domain in the human scaffolding protein Tuba. This interaction antagonizes Tuba, thereby diminishing cortical tension at the apical junctional complex and enhancing <i>L. monocytogenes</i> protrusion formation and spread. Tuba contains five SH3 domains apart from the domain that interacts with InlC. Here, we show that human GTPase Dynamin 2 associates with two SH3 domains in the amino-terminus of Tuba and acts together with this scaffolding protein to control the spread of <i>L. monocytogenes</i>. Genetic or pharmacological inhibition of Dynamin 2 or knockdown of Tuba each restored normal protrusion formation and spread to a bacterial strain deleted for the <i>inlC</i> gene (∆<i>inlC</i>). Dynamin 2 localized to apical junctions in uninfected human cells and protrusions in cells infected with <i>L. monocytogenes</i>. Localization of Dynamin 2 to junctions and protrusions depended on Tuba. Knockdown of Dynamin 2 or Tuba diminished junctional linearity, indicating a role for these proteins in controlling cortical tension. Infection with <i>L. monocytogenes</i> induced InlC-dependent displacement of Dynamin 2 from junctions, suggesting a possible mechanism of antagonism of this GTPase. Collectively, our results show that Dynamin 2 cooperates with Tuba to promote intercellular tension that restricts the spread of ∆<i>inlC Listeria</i>. By expressing InlC, wild-type <i>L. monocytogenes</i> overcomes this restriction.</p>\",\"PeriodicalId\":13541,\"journal\":{\"name\":\"Infection and Immunity\",\"volume\":null,\"pages\":null},\"PeriodicalIF\":2.9000,\"publicationDate\":\"2024-10-15\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11475654/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Infection and Immunity\",\"FirstCategoryId\":\"3\",\"ListUrlMain\":\"https://doi.org/10.1128/iai.00136-24\",\"RegionNum\":3,\"RegionCategory\":\"医学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"2024/8/12 0:00:00\",\"PubModel\":\"Epub\",\"JCR\":\"Q3\",\"JCRName\":\"IMMUNOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Infection and Immunity","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1128/iai.00136-24","RegionNum":3,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/8/12 0:00:00","PubModel":"Epub","JCR":"Q3","JCRName":"IMMUNOLOGY","Score":null,"Total":0}
引用次数: 0

摘要

食源性病原体单核细胞增生李斯特菌利用肌动蛋白运动产生质膜突起,从而介导细菌在宿主细胞间传播。在极化上皮细胞中,单核细胞增多性李斯特氏菌有效的突起形成需要分泌的细菌蛋白 InlC,它与人类支架蛋白 Tuba 中的羧基末端 Src 同源 3(SH3)结构域结合。这种相互作用可拮抗 Tuba,从而降低顶端连接复合体的皮层张力,促进单核细胞增多性乳酸杆菌突起的形成和扩散。除了与 InlC 相互作用的结构域外,Tuba 还含有五个 SH3 结构域。在这里,我们发现人类 GTPase Dynamin 2 与 Tuba 氨基末端的两个 SH3 结构域结合,并与这一支架蛋白一起控制单核细胞增多性乳酸杆菌的扩散。通过基因或药物抑制 Dynamin 2 或敲除 Tuba,可使缺失 inlC 基因的细菌菌株(ΔinlC)恢复正常的突起形成和扩散。在未感染的人体细胞中,Dynamin 2定位于顶端连接处,而在感染了单核细胞增多症的细胞中,Dynamin 2定位于突起处。Dynamin 2在连接处和突起处的定位取决于Tuba。敲除Dynamin 2或Tuba会降低连接的线性度,这表明这些蛋白在控制皮层张力方面发挥作用。感染单核细胞增生性酵母菌会诱导依赖 InlC 的 Dynamin 2 从连接处移位,这表明这种 GTP 酶可能存在拮抗作用。总之,我们的研究结果表明,Dynamin 2 与 Tuba 合作促进细胞间张力,从而限制了 ∆inlC 李斯特菌的扩散。通过表达 InlC,野生型李斯特菌克服了这种限制。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
The host GTPase Dynamin 2 modulates apical junction structure to control cell-to-cell spread of Listeria monocytogenes.

The food-borne pathogen Listeria monocytogenes uses actin-based motility to generate plasma membrane protrusions that mediate the spread of bacteria between host cells. In polarized epithelial cells, efficient protrusion formation by L. monocytogenes requires the secreted bacterial protein InlC, which binds to a carboxyl-terminal Src homology 3 (SH3) domain in the human scaffolding protein Tuba. This interaction antagonizes Tuba, thereby diminishing cortical tension at the apical junctional complex and enhancing L. monocytogenes protrusion formation and spread. Tuba contains five SH3 domains apart from the domain that interacts with InlC. Here, we show that human GTPase Dynamin 2 associates with two SH3 domains in the amino-terminus of Tuba and acts together with this scaffolding protein to control the spread of L. monocytogenes. Genetic or pharmacological inhibition of Dynamin 2 or knockdown of Tuba each restored normal protrusion formation and spread to a bacterial strain deleted for the inlC gene (∆inlC). Dynamin 2 localized to apical junctions in uninfected human cells and protrusions in cells infected with L. monocytogenes. Localization of Dynamin 2 to junctions and protrusions depended on Tuba. Knockdown of Dynamin 2 or Tuba diminished junctional linearity, indicating a role for these proteins in controlling cortical tension. Infection with L. monocytogenes induced InlC-dependent displacement of Dynamin 2 from junctions, suggesting a possible mechanism of antagonism of this GTPase. Collectively, our results show that Dynamin 2 cooperates with Tuba to promote intercellular tension that restricts the spread of ∆inlC Listeria. By expressing InlC, wild-type L. monocytogenes overcomes this restriction.

求助全文
通过发布文献求助,成功后即可免费获取论文全文。 去求助
来源期刊
Infection and Immunity
Infection and Immunity 医学-传染病学
CiteScore
6.00
自引率
6.50%
发文量
268
审稿时长
3 months
期刊介绍: Infection and Immunity (IAI) provides new insights into the interactions between bacterial, fungal and parasitic pathogens and their hosts. Specific areas of interest include mechanisms of molecular pathogenesis, virulence factors, cellular microbiology, experimental models of infection, host resistance or susceptibility, and the generation of innate and adaptive immune responses. IAI also welcomes studies of the microbiome relating to host-pathogen interactions.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信