Department of Ophthalmology and Visual Sciences, Illinois Eye and Ear Infirmary, College of Medicine, University of Illinois at Chicago, Chicago, IL, USA.
Department of Stem Cells and Human Disease Models, Shiga University of Medical Science, Otsu, Japan.
Angiogenesis. 2018 Nov;21(4):677-698. doi: 10.1007/s10456-018-9629-2. Epub 2018 Jul 3.
The study of lymphangiogenesis is an emerging science that has revealed the lymphatic system as a central player in many pathological conditions including cancer metastasis, lymphedema, and organ graft rejection. A thorough understanding of the mechanisms of lymphatic growth will play a key role in the development of therapeutic strategies against these conditions. Despite the known potential of this field, the study of lymphatics has historically lagged behind that of hemangiogenesis. Until recently, significant strides in lymphatic studies were impeded by a lack of lymphatic-specific markers and suitable experimental models compared to those of the more immediately visible blood vasculature. Lymphangiogenesis has also been shown to be a key phenomenon in developmental biological processes, such as cell proliferation, guided migration, differentiation, and cell-to-cell communication, making lymphatic-specific visualization techniques highly desirable and desperately needed. Imaging modalities including immunohistochemistry and in situ hybridization are limited by the need to sacrifice animal models for tissue harvesting at every experimental time point. Moreover, the processes of mounting and staining harvested tissues may introduce artifacts that can confound results. These traditional methods for investigating lymphatic and blood vasculature are associated with several problems including animal variability (e.g., between mice) when replicating lymphatic growth environments and the cost concerns of prolonged, labor-intensive studies, all of which complicate the study of dynamic lymphatic processes. With the discovery of lymphatic-specific markers, researchers have been able to develop several lymphatic and blood vessel-specific, promoter-driven, fluorescent-reporter transgenic mice for visualization of lymphatics in vivo and in vitro. For instance, GFP, mOrange, tdTomato, and other fluorescent proteins can be expressed under control of a lymphatic-specific marker like Prospero-related homeobox 1 (Prox1), which is a highly conserved transcription factor for determining embryonic organogenesis in vertebrates that is implicated in lymphangiogenesis as well as several human cancers. Importantly, Prox1-null mouse embryos develop without lymphatic vessels. In human adults, Prox1 maintains lymphatic endothelial cells and upregulates proteins associated with lymphangiogenesis (e.g., VEGFR-3) and downregulates angiogenesis-associated gene expression (e.g., STAT6). To visualize lymphatic development in the context of angiogenesis, dual fluorescent-transgenic reporters, like Prox1-GFP/Flt1-DsRed mice, have been bred to characterize lymphatic and blood vessels simultaneously in vivo. In this review, we discuss the trends in lymphatic visualization and the potential usage of transgenic breeds in hemangiogenesis and lymphangiogenesis research to understand spatial and temporal correlations between vascular development and pathological progression.
淋巴管生成的研究是一门新兴科学,它揭示了淋巴管系统在许多病理状况中起着核心作用,包括癌症转移、淋巴水肿和器官移植排斥。对淋巴管生长机制的深入了解将在开发针对这些疾病的治疗策略方面发挥关键作用。尽管该领域具有已知的潜力,但与更直观的血管生成相比,淋巴管的研究历史一直滞后。直到最近,与更易于观察的血液脉管系统相比,淋巴管研究的显著进展受到缺乏淋巴管特异性标志物和合适的实验模型的阻碍。淋巴管生成也被证明是细胞增殖、导向迁移、分化和细胞间通讯等发育生物学过程中的关键现象,这使得淋巴管特异性可视化技术非常理想和急需。包括免疫组织化学和原位杂交在内的成像方式受到需要在每个实验时间点牺牲动物模型进行组织收获的限制。此外,收获组织的安装和染色过程可能会引入混淆结果的伪影。这些用于研究淋巴管和血管的传统方法存在几个问题,包括在复制淋巴管生长环境时动物的变异性(例如,小鼠之间)以及长期、劳动密集型研究的成本问题,所有这些都使动态淋巴管过程的研究变得复杂。随着淋巴管特异性标志物的发现,研究人员已经能够开发几种淋巴管和血管特异性、启动子驱动、荧光报告转基因小鼠,用于体内和体外淋巴管的可视化。例如,GFP、mOrange、tdTomato 和其他荧光蛋白可以在淋巴管特异性标志物(如 Prospero 相关同源盒 1(Prox1))的控制下表达,Prox1 是一种高度保守的转录因子,决定脊椎动物的胚胎器官发生,它与淋巴管生成以及几种人类癌症有关。重要的是,Prox1 缺失的小鼠胚胎没有淋巴管。在人类成年中,Prox1 维持淋巴管内皮细胞,并上调与淋巴管生成相关的蛋白质(例如,VEGFR-3),下调与血管生成相关的基因表达(例如,STAT6)。为了在血管生成的背景下观察淋巴管的发育,已经培育了双荧光转基因报告小鼠,例如 Prox1-GFP/Flt1-DsRed 小鼠,以在体内同时对淋巴管和血管进行特征化。在这篇综述中,我们讨论了淋巴管可视化的趋势以及在血管生成和淋巴管生成研究中使用转基因品种的潜力,以了解血管发育和病理进展之间的时空相关性。