Neural Crest Origin of Retinal and Choroidal Pericytes

Trost, Andrea; Schroedl, Falk; Lange, Simona; Rivera, Francisco J.; Tempfer, Herbert; Korntner, Stefanie; Stolt, C. Claus; Wegner, Michael; Bogner, Barbara; Kaser-Eichberger, Alexandra; Krefft, Karolina; Runge, Christian; Aigner, Ludwig; Reitsamer, Herbert A.

doi:10.1167/iovs.13-12946

Cited by 74 publications

(79 citation statements)

References 59 publications

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“…To date, contribution of neural crest cells to brain MCs has been demonstrated in vertebrates including mice, bird and zebrafish (Etchevers et al, 2001;Heglind et al, 2005;Korn et al, 2002;Trost et al, 2013;Wang et al, 2014;Yamanishi et al, 2012). In agreement with this, our analyses indicated a neural crest origin of MCs in the anterior part of the brain and in the hyaloid vessels.…”

Section: Discussionsupporting

confidence: 89%

Clarification of mural cell coverage of vascular endothelial cells by live imaging of zebrafish

et al. 2016

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Mural cells (MCs) consisting of vascular smooth muscle cells and pericytes cover the endothelial cells (ECs) to regulate vascular stability and homeostasis. Here, we clarified the mechanism by which MCs develop and cover ECs by generating transgenic zebrafish lines that allow live imaging of MCs and by lineage tracing in vivo. To cover cranial vessels, MCs derived from either neural crest cells or mesoderm emerged around the preformed EC tubes, proliferated and migrated along EC tubes. During their migration, the MCs moved forward by extending their processes along the inter-EC junctions, suggesting a role for inter-EC junctions as a scaffold for MC migration. In the trunk vasculature, MCs derived from mesoderm covered the ventral side of the dorsal aorta (DA), but not the posterior cardinal vein. Furthermore, the MCs migrating from the DA or emerging around intersegmental vessels (ISVs) preferentially covered arterial ISVs rather than venous ISVs, indicating that MCs mostly cover arteries during vascular development. Thus, live imaging and lineage tracing enabled us to clarify precisely how MCs cover the EC tubes and to identify the origins of MCs.

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Section: Discussionsupporting

confidence: 89%

Clarification of mural cell coverage of vascular endothelial cells by live imaging of zebrafish

et al. 2016

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“…It is possible that these cells are glia that are not in immediate contact with neural processes, given prior reports of heterogeneous glial cells in the enteric nervous system that varied in expression of traditional glial markers, morphology and location in the intestinal wall (Boesmans et al, 2015). However, others have reported that vascular pericytes in the thymus, retina, and choroid derive from neural crest based on studies using Cre lineage tracing (Trost et al, 2013; Zachariah and Cyster, 2010). The nature and function of the rare Sox10+ vascular-associated cells we observe in the bladder wall remain to be investigated.…”

Section: Discussionmentioning

confidence: 99%

Migration pathways of sacral neural crest during development of lower urogenital tract innervation

Wiese

Deal

Ireland

et al. 2017

Developmental Biology

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The migration and fate of cranial and vagal neural crest-derived progenitor cells (NCPCs) have been extensively studied; however, much less is known about sacral NCPCs particularly in regard to their distribution in the urogenital system. To construct a spatiotemporal map of NCPC migration pathways into the developing lower urinary tract, we utilized the Sox10-H2BVenus transgene to visualize NCPCs expressing Sox10. Our aim was to define the relationship of Sox10-expressing NCPCs relative to bladder innervation, smooth muscle differentiation, and vascularization through fetal development into adulthood. Sacral NCPC migration is a highly regimented, specifically timed process, with several potential regulatory mileposts. Neuronal differentiation occurs concomitantly with sacral NCPC migration, and neuronal cell bodies are present even before the pelvic ganglia coalesce. Sacral NCPCs reside within the pelvic ganglia anlagen through 13.5 days post coitum (dpc), after which they begin streaming into the bladder body in progressive waves. Smooth muscle differentiation and vascularization of the bladder initiate prior to innervation and appear to be independent processes. In adult bladder, the majority of Sox10+ cells express the glial marker S100β, consistent with Sox10 being a glial marker in other tissues. However, rare Sox10+ NCPCs are seen in close proximity to blood vessels and not all are S100β+, suggesting either glial heterogeneity or a potential nonglial role for Sox10+ cells along vasculature. Taken together, the developmental atlas of Sox10+ NCPC migration and distribution profile of these cells in adult bladder provided here will serve as a roadmap for future investigation in mouse models of lower urinary tract dysfunction.

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“…6 In contrast, Sox10 is expressed in both neural crest and other non-neural crest lineages, such as oligodendrocytes and inner ear, during development, 7, 9 and its expression continues in later development and adult tissues, mainly in the central and peripheral nervous systems, 10 which was demonstrated by several reporter mouse lines, such as Sox10-rtTA, 11 Sox10-Venus, 12 Sox10-Cre 13 and Sox10-CreER 14 . Studies on vascular development using Sox10-Cre/CreER mice showed that Sox10+ cells differentiated into pericytes and SMCs in the brain, 14 eye, 15 thymus, 16, 17 ascending aorta, aorta arch, carotid arteries 13 , and the neural crest origin of these cells were verified by the studies on quail-chick chimera or Wnt1-Cre mice. 3–5, 16, 18 In addition, the study on Wnt1-Cre mice also showed that neural crest cells give rise to SMCs of coronary arteries in the heart, 18 although there is no such report from Sox10-Cre mice.…”

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confidence: 90%

Sox10 ⁺ Cells Contribute to Vascular Development in Multiple Organs—Brief Report

Wang

Yuan

et al. 2017

ATVB

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Objective Previous genetic lineage tracing studies showed that Sox10+ cells differentiate into vascular mural cells, limited to neural crest-derived blood vessels in craniofacial tissues, aortic arch, pulmonary arch arteries, brachiocephalic, carotid arteries and thymus. The purpose of this study was to investigate the contribution of Sox10+ cells to the vascular development in other tissues and organs and their relationship with neural crest. Approach and Results Using genetic lineage tracing technique based on Cre/LoxP system, we examined blood vessels of the adult organs of Sox10-Cre/Rosa-LoxP-RFP and Wnt1-Cre/Rosa-LoxP-RFP mice by immunohistological analysis. In addition to previously reported tissues and organs derived from neural crest, we showed that Sox10+ cells also contributed to vascular mural cells in the lung, spleen and kidney, which are derived from non-neural crest origin as evidenced by RFP- blood vessels in these three organs of Wnt1-Cre/Rosa-LoxP-RFP mice. Conclusions This study demonstrates that Sox10+ cells contribute to pericytes and smooth muscle cells in most parts of the body, including those from both neural crest and non-neural crest, which has significant implications in vascular remodeling under physiological and pathological conditions.

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Neural Crest Origin of Retinal and Choroidal Pericytes

Abstract: Since YFP-positive PCs and vSMCs are colocalized with NG2 and PDGFRβ, we propose that capillary PCs and vSMCs in the retina and the optic nerve, both parts of the central nervous system, as well as in the choroid, a tissue of mesodermal origin, derive from the neural crest.

Cited by 74 publications

References 59 publications

Clarification of mural cell coverage of vascular endothelial cells by live imaging of zebrafish

Clarification of mural cell coverage of vascular endothelial cells by live imaging of zebrafish

Migration pathways of sacral neural crest during development of lower urogenital tract innervation

Sox10 ⁺ Cells Contribute to Vascular Development in Multiple Organs—Brief Report

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Neural Crest Origin of Retinal and Choroidal Pericytes

Abstract: Since YFP-positive PCs and vSMCs are colocalized with NG2 and PDGFRβ, we propose that capillary PCs and vSMCs in the retina and the optic nerve, both parts of the central nervous system, as well as in the choroid, a tissue of mesodermal origin, derive from the neural crest.

Cited by 74 publications

References 59 publications

Clarification of mural cell coverage of vascular endothelial cells by live imaging of zebrafish

Clarification of mural cell coverage of vascular endothelial cells by live imaging of zebrafish

Migration pathways of sacral neural crest during development of lower urogenital tract innervation

Sox10 + Cells Contribute to Vascular Development in Multiple Organs—Brief Report

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Product

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Sox10 ⁺ Cells Contribute to Vascular Development in Multiple Organs—Brief Report