用综合生物学方法理解生物玻璃刺激的角质细胞集体迁移。

IF 1.5 4区 生物学 Q4 CELL BIOLOGY
Joseph Siegfreid, Ali Crampton, Saghi Saghazadeh, Randilynn Christensen, Jacob Notbohm, Jason Bjork, Bryan Baker
{"title":"用综合生物学方法理解生物玻璃刺激的角质细胞集体迁移。","authors":"Joseph Siegfreid, Ali Crampton, Saghi Saghazadeh, Randilynn Christensen, Jacob Notbohm, Jason Bjork, Bryan Baker","doi":"10.1093/intbio/zyae008","DOIUrl":null,"url":null,"abstract":"<p><p>A critical phase of wound healing is the coordinated movement of keratinocytes. To this end, bioglasses show promise in speeding healing in hard tissues and skin wounds. Studies suggest that bioglass materials may promote wound healing by inducing positive cell responses in proliferation, growth factor production, expression of angiogenic factors, and migration. Precise details of how bioglass may stimulate migration are unclear, however, because the common assays for studying migration in wound healing focus on simplified outputs like rate of migration or total change in wound area. These outputs are limited in that they represent the average behavior of the collective, with no connection between the motion of the individual cells and the collective wound healing response. There is a need to apply more refined tools that identify how the motion of the individual cells changes in response to perturbations, such as by bioglass, and in turn affects motion of the cell collective. Here, we apply an integrative biology strategy that combines an in vitro wound healing assay using primary neonatal human keratinocytes with time lapse microscopy and quantitative image analysis. The resulting data set provides the cell velocity field, from which we define key metrics that describe cooperative migration phenotypes. Treatment with growth factors led to faster single-cell speeds compared to control, but the migration was not cooperative, with cells breaking away from their neighbors and migrating as individuals. Treatment with calcium or bioglass led to migration phenotypes that were highly collective, with greater coordination in space compared to control. We discuss the link between bioglass treatment and observed increases in free calcium ions that are hypothesized to promote these distinct coordinated behaviors in primary keratinocytes. These findings have been enabled by the unique descriptors developed through applying image analysis to interpret biological response in migration models. Insight Box/Paragraph Statement: Bioglasses are important materials for tissue engineering and have more recently shown promise in skin and wound healing by mechanisms tied to their unique ionic properties. The precise details, however, of how cell migration may be affected by bioglass are left unclear by traditional cell assay methods. The following describes the integration of migration assays of keratinocytes, cells critical for skin and wound healing, with the tools of time lapse microscopy and image analysis to generate a quantitative description of coordinated, tissue-like migration behavior, stimulated by bioglass, that would not have been accessible without the combination of these analytical tools.</p>","PeriodicalId":80,"journal":{"name":"Integrative Biology","volume":"16 ","pages":""},"PeriodicalIF":1.5000,"publicationDate":"2024-01-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"An integrative biology approach to understanding keratinocyte collective migration as stimulated by bioglass.\",\"authors\":\"Joseph Siegfreid, Ali Crampton, Saghi Saghazadeh, Randilynn Christensen, Jacob Notbohm, Jason Bjork, Bryan Baker\",\"doi\":\"10.1093/intbio/zyae008\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>A critical phase of wound healing is the coordinated movement of keratinocytes. To this end, bioglasses show promise in speeding healing in hard tissues and skin wounds. Studies suggest that bioglass materials may promote wound healing by inducing positive cell responses in proliferation, growth factor production, expression of angiogenic factors, and migration. Precise details of how bioglass may stimulate migration are unclear, however, because the common assays for studying migration in wound healing focus on simplified outputs like rate of migration or total change in wound area. These outputs are limited in that they represent the average behavior of the collective, with no connection between the motion of the individual cells and the collective wound healing response. There is a need to apply more refined tools that identify how the motion of the individual cells changes in response to perturbations, such as by bioglass, and in turn affects motion of the cell collective. Here, we apply an integrative biology strategy that combines an in vitro wound healing assay using primary neonatal human keratinocytes with time lapse microscopy and quantitative image analysis. The resulting data set provides the cell velocity field, from which we define key metrics that describe cooperative migration phenotypes. Treatment with growth factors led to faster single-cell speeds compared to control, but the migration was not cooperative, with cells breaking away from their neighbors and migrating as individuals. Treatment with calcium or bioglass led to migration phenotypes that were highly collective, with greater coordination in space compared to control. We discuss the link between bioglass treatment and observed increases in free calcium ions that are hypothesized to promote these distinct coordinated behaviors in primary keratinocytes. These findings have been enabled by the unique descriptors developed through applying image analysis to interpret biological response in migration models. Insight Box/Paragraph Statement: Bioglasses are important materials for tissue engineering and have more recently shown promise in skin and wound healing by mechanisms tied to their unique ionic properties. The precise details, however, of how cell migration may be affected by bioglass are left unclear by traditional cell assay methods. The following describes the integration of migration assays of keratinocytes, cells critical for skin and wound healing, with the tools of time lapse microscopy and image analysis to generate a quantitative description of coordinated, tissue-like migration behavior, stimulated by bioglass, that would not have been accessible without the combination of these analytical tools.</p>\",\"PeriodicalId\":80,\"journal\":{\"name\":\"Integrative Biology\",\"volume\":\"16 \",\"pages\":\"\"},\"PeriodicalIF\":1.5000,\"publicationDate\":\"2024-01-23\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Integrative Biology\",\"FirstCategoryId\":\"99\",\"ListUrlMain\":\"https://doi.org/10.1093/intbio/zyae008\",\"RegionNum\":4,\"RegionCategory\":\"生物学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q4\",\"JCRName\":\"CELL BIOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Integrative Biology","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1093/intbio/zyae008","RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q4","JCRName":"CELL BIOLOGY","Score":null,"Total":0}
引用次数: 0

摘要

伤口愈合的一个关键阶段是角质细胞的协调运动。为此,生物玻璃有望加速硬组织和皮肤伤口的愈合。研究表明,生物玻璃材料可通过诱导细胞在增殖、产生生长因子、表达血管生成因子和迁移方面的积极反应来促进伤口愈合。然而,生物玻璃如何刺激迁移的具体细节尚不清楚,因为研究伤口愈合中迁移的常用方法侧重于简化的输出,如迁移率或伤口面积的总变化。这些结果是有限的,因为它们代表的是集体的平均行为,单个细胞的运动与集体的伤口愈合反应之间没有联系。我们需要应用更精细的工具,以确定单个细胞的运动如何对生物玻璃等扰动做出反应,进而影响细胞集体的运动。在这里,我们采用了一种综合生物学策略,将使用原代新生人类角质细胞进行的体外伤口愈合试验与延时显微镜和定量图像分析相结合。由此产生的数据集提供了细胞速度场,我们据此定义了描述合作迁移表型的关键指标。与对照组相比,使用生长因子处理可使单细胞速度加快,但迁移并不合作,细胞会脱离邻近细胞,作为个体迁移。与对照组相比,用钙或生物玻璃处理会导致高度集体的迁移表型,在空间上有更大的协调性。我们讨论了生物玻璃处理与观察到的游离钙离子增加之间的联系,假设游离钙离子的增加促进了原代角质形成细胞中这些不同的协调行为。这些发现得益于通过应用图像分析来解释迁移模型中的生物反应而开发的独特描述符。洞察框/段落陈述:生物玻璃是组织工程学的重要材料,最近在皮肤和伤口愈合方面显示出与其独特离子特性相关的机制。然而,传统的细胞检测方法并不清楚生物玻璃如何影响细胞迁移的具体细节。下文介绍了如何将角质形成细胞(对皮肤和伤口愈合至关重要的细胞)的迁移测定与延时显微镜和图像分析工具相结合,从而对生物玻璃刺激下的协调组织样迁移行为进行定量描述。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
An integrative biology approach to understanding keratinocyte collective migration as stimulated by bioglass.

A critical phase of wound healing is the coordinated movement of keratinocytes. To this end, bioglasses show promise in speeding healing in hard tissues and skin wounds. Studies suggest that bioglass materials may promote wound healing by inducing positive cell responses in proliferation, growth factor production, expression of angiogenic factors, and migration. Precise details of how bioglass may stimulate migration are unclear, however, because the common assays for studying migration in wound healing focus on simplified outputs like rate of migration or total change in wound area. These outputs are limited in that they represent the average behavior of the collective, with no connection between the motion of the individual cells and the collective wound healing response. There is a need to apply more refined tools that identify how the motion of the individual cells changes in response to perturbations, such as by bioglass, and in turn affects motion of the cell collective. Here, we apply an integrative biology strategy that combines an in vitro wound healing assay using primary neonatal human keratinocytes with time lapse microscopy and quantitative image analysis. The resulting data set provides the cell velocity field, from which we define key metrics that describe cooperative migration phenotypes. Treatment with growth factors led to faster single-cell speeds compared to control, but the migration was not cooperative, with cells breaking away from their neighbors and migrating as individuals. Treatment with calcium or bioglass led to migration phenotypes that were highly collective, with greater coordination in space compared to control. We discuss the link between bioglass treatment and observed increases in free calcium ions that are hypothesized to promote these distinct coordinated behaviors in primary keratinocytes. These findings have been enabled by the unique descriptors developed through applying image analysis to interpret biological response in migration models. Insight Box/Paragraph Statement: Bioglasses are important materials for tissue engineering and have more recently shown promise in skin and wound healing by mechanisms tied to their unique ionic properties. The precise details, however, of how cell migration may be affected by bioglass are left unclear by traditional cell assay methods. The following describes the integration of migration assays of keratinocytes, cells critical for skin and wound healing, with the tools of time lapse microscopy and image analysis to generate a quantitative description of coordinated, tissue-like migration behavior, stimulated by bioglass, that would not have been accessible without the combination of these analytical tools.

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
Integrative Biology
Integrative Biology 生物-细胞生物学
CiteScore
4.90
自引率
0.00%
发文量
15
审稿时长
1 months
期刊介绍: Integrative Biology publishes original biological research based on innovative experimental and theoretical methodologies that answer biological questions. The journal is multi- and inter-disciplinary, calling upon expertise and technologies from the physical sciences, engineering, computation, imaging, and mathematics to address critical questions in biological systems. Research using experimental or computational quantitative technologies to characterise biological systems at the molecular, cellular, tissue and population levels is welcomed. Of particular interest are submissions contributing to quantitative understanding of how component properties at one level in the dimensional scale (nano to micro) determine system behaviour at a higher level of complexity. Studies of synthetic systems, whether used to elucidate fundamental principles of biological function or as the basis for novel applications are also of interest.
×
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