Single cell dynamics of embryonic muscle progenitor cells in zebrafish

Sharma, Priyanka; Ruel, Tyler D.; Kocha, Katrinka M.; Liao, Shan; Huang, Peng

doi:10.1242/dev.178400

Cited by 20 publications

(29 citation statements)

References 68 publications

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“…3C). Since perivascular fibroblasts are more abundant along ISVs compared to pericytes, we took advantage of a mosaic col1a2:Gal4; UAS:Kaede line (referred to as col1a2 Kaede ) (49) to sparsely label single perivascular fibroblasts for easier visualization. In contrast to pericytes, perivascular fibroblasts were more loosely associated with ISVs and had a globular morphology with shorter and finer processes that wrapped diametrically around the associated ISV in an ‘awkward hug’ (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Since col1a2 transgenic lines such as col1a2:GFP are mosaic (Fig. S3A) (49), the number above likely under-estimates the proportion of pericytes derived from perivascular fibroblasts. To further test our model, we performed time-lapse experiments in nkx3.1 NTR-mCherry ; pdgfrb:GFP embryos.…”

Section: Resultsmentioning

confidence: 99%

“…Together, these results indicate that some perivascular fibroblasts serve as pericyte precursors, contributing to most, if not all, pericytes associated with ISVs in the trunk. Incomplete labeling or ablation likely reflects the mosaic nature of the col1a2 transgenic lines (49).…”

Section: Discussionmentioning

confidence: 99%

“…All protocols were approved by the Animal Care Committee at the University of Calgary (#AC17-0128). The following transgenic strains were utilized in this study: TgBAC(col1a2:Gal4)ca102 (46, 49), TgBAC(col1a2:GFP)ca103 (46), Tg(kdrl:EGFP)la116 (72), Tg(kdrl:mCherry)ci5 (73), TgBAC(nkx3.1:Gal4)ca101 (46), TgBAC(pdgfrb:Gal4FF)ca42 (45,74), TgBAC(pdgfrb:GFP)ca41 (45), Tg(UAS:Kaede)s1999t (75), Tg(UAS:NTR-mCherry)c264 (75). The mosaic col1a2:Gal4; UAS:Kaede line was maintained by growing embryos with more mosaic Kaede expression.…”

Section: Methodsmentioning

confidence: 99%

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Dual function of perivascular fibroblasts in vascular stabilization in zebrafish

Rajan

Roger

Kocha

et al. 2020

Preprint

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24Blood vessels are vital to sustain life in all vertebrates. While it is known that mural cells (pericytes 25 and smooth muscle cells) regulate vascular integrity, the contribution of other cell types to vascular 26 stabilization has been largely unexplored. Using zebrafish, we identified sclerotome-derived 27 perivascular fibroblasts as a novel population of blood vessel associated cells. In contrast to pericytes, 28 perivascular fibroblasts emerge early during development, express the extracellular matrix (ECM) 29 genes col1a2 and col5a1, and display distinct morphology and distribution. Time-lapse imaging 30 reveals that perivascular fibroblasts serve as pericyte precursors. Genetic ablation of perivascular 31 fibroblasts results in dysmorphic blood vessels with variable diameters. Strikingly, col5a1 mutants 32show spontaneous hemorrhage, and the penetrance of the phenotype is strongly enhanced by the 33 additional loss of col1a2. Together, our work reveals dual roles of perivascular fibroblasts in vascular 34 stabilization where they establish the ECM around nascent vessels and function as pericyte 35 progenitors. 36 3 AUTHOR SUMMARY 37 38 Blood vessels are essential to sustain life in humans. Defects in blood vessels can lead to serious 39 diseases, such as hemorrhage, tissue ischemia, and stroke. However, how blood vessel stability is 40 maintained by surrounding support cells is still poorly understood. Using the zebrafish model, we 41 identify a new population of blood vessel associated cells termed perivascular fibroblasts, which 42 originate from the sclerotome, an embryonic structure that is previously known to generate the 43 skeleton of the animal. Perivascular fibroblasts are distinct from pericytes, a known population of 44 blood vessel support cells. They become associated with blood vessels much earlier than pericytes 45 and express several collagen genes, encoding main components of the extracellular matrix. Loss of 46 perivascular fibroblasts or mutations in collagen genes result in fragile blood vessels prone to 47 53 54The vascular system is crucial to the survival of vertebrates. Blood vessels must rapidly expand 55 and contract in response to systemic cues, but also maintain the stability to withstand the stress of 56 blood flow. To maintain their integrity, blood vessels are supported by a highly specialized 57 perivascular architecture comprised of blood vessel associated cells and the surrounding extracellular 58 matrix (ECM) (1,2). Compromised vascular integrity can result in devastating human diseases, such 59 as aneurysms, vascular malformations, and hemorrhagic strokes (3-6). However, how blood vessels 60 are stabilized by different perivascular components is still poorly understood. 61The prevailing model is that vascular stability is maintained at three different levels: endothelial 62 cells, mural cells and the surrounding ECM (2). First, blood vessels are lined by endothelial cells. 63Adherens and tight junctions between endothelial cells provide the primary barrier to passage o...

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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Dual function of perivascular fibroblasts in vascular stabilization in zebrafish

Rajan

Roger

Kocha

et al. 2020

Preprint

Self Cite

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“…The second population of muscle stem cells resides in a teleost specific structure known as the external cell layer (ECL), which is formed during myogenesis from the anterior compartment of the somite, and subsequently sits on the lateral surface of the animal (Hollway et al, ; Stellabotte, Dobbs‐McAuliffe, Fernández, Feng, & Devoto, ). This structure serves a similar role to the amniote dermomyotome but unlike the latter it exists throughout the life of the animal and is critical for secondary myogenesis and growth of the teleost myotome (discussed below) (Marschallinger, Obermayer, Sänger, Stoiber, & Steinbacher, ; Nguyen et al, ; Sharma, Ruel, Kocha, Liao, & Huang, ). These stem cells are from here on referred to as growth‐specific stem cells.…”

Section: Defining Muscle Stem Cells In Amniotes and Teleostsmentioning

confidence: 99%

Stem cells in skeletal muscle growth and regeneration in amniotes and teleosts: Emerging themes

Ruparelia

Ratnayake

Currie

2019

WIREs Developmental Biology

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Skeletal muscle is a contractile, postmitotic tissue that retains the capacity to grow and regenerate throughout life in amniotes and teleost. Both muscle growth and regeneration are regulated by obligate tissue resident muscle stem cells. Given that considerable knowledge exists on the myogenic process, recent studies have focused on examining the molecular markers of muscle stem cells, and on the intrinsic and extrinsic signals regulating their function. From this, two themes emerge: firstly, muscle stem cells display remarkable heterogeneity not only with regards to their gene expression profile, but also with respect to their behavior and function; and secondly, the stem cell niche is a critical regulator of muscle stem cell function during growth and regeneration. Here, we will address the current understanding of these emerging themes with emphasis on the distinct processes used by amniotes and teleost, and discuss the challenges and opportunities in the muscle growth and regeneration fields.

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