Twist3 is required for dedifferentiation during extraocular muscle regeneration in adult zebrafish

Zhao, Yi; Louie, Ke’ale W.; Tingle, Christina F.; Sha, Cuilee; Heisel, Curtis J.; Unsworth, Shelby P.; Kish, Phillip E.; Kahana, Alon

doi:10.1371/journal.pone.0231963

Cited by 8 publications

(5 citation statements)

References 69 publications

(93 reference statements)

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“…We first assessed whether the top markers for osteoblastic cell clusters included canonical markers for MET and EMT ( Alimperti and Andreadis, 2015 ; Ansieau et al., 2008 ; Batlle et al., 2000 ; Bebee et al., 2015 ; Burguera et al., 2017 ; Cano et al., 2000 ; Comijn et al., 2001 ; Funahashi et al., 1993 ; Grooteclaes and Frisch, 2000 ; Jhingory et al., 2010 ; Kang and Massague, 2004 ; Kimura et al., 1995 ; Leptin, 1991 ; Nieto, 2002 ; Ocana et al., 2012 ; Vermeulen et al., 1999 ; Verschueren et al., 1999 ; Warzecha et al., 2009b ; Zhao et al., 2020 ). We found that the second most differentially expressed gene in cluster 1 was esrp1 .…”

Section: Resultsmentioning

confidence: 99%

Single-cell resolution of MET- and EMT-like programs in osteoblasts during zebrafish fin regeneration

et al. 2022

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Summary Zebrafish regenerate fin rays following amputation through epimorphic regeneration, a process that has been proposed to involve the epithelial-to-mesenchymal transition (EMT). We performed single-cell RNA sequencing (scRNA-seq) to elucidate osteoblastic transcriptional programs during zebrafish caudal fin regeneration. We show that osteoprogenitors are enriched with components associated with EMT and its reverse, mesenchymal-to-epithelial transition (MET), and provide evidence that the EMT markers cdh11 and twist2 are co-expressed in dedifferentiating cells at the amputation stump at 1 dpa, and in differentiating osteoblastic cells in the regenerate, the latter of which are enriched in EMT signatures. We also show that esrp1 , a regulator of alternative splicing in epithelial cells that is associated with MET, is expressed in a subset of osteoprogenitors during outgrowth. This study provides a single cell resource for the study of osteoblastic cells during zebrafish fin regeneration, and supports the contribution of MET- and EMT-associated components to this process.

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Section: Resultsmentioning

confidence: 99%

Single-cell resolution of MET- and EMT-like programs in osteoblasts during zebrafish fin regeneration

et al. 2022

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“…Twist function and cellular plasticity have been connected in the literature mainly due to its role as one of the transcriptional master regulators during the transition from epithelial to mesenchymal states (EMT), crucially required for embryonic morphogenesis and often linked to metastasis in various cancer models (Lu and Kang, 2019). In terms of myogenic cell fate plasticity it is known that prolonged Twist expression negatively regulates muscle cell differentiation during embryonic myogenesis as well as adult flight muscle development in Drosophila (Anant et al, 1998;Cripps and Olson, 1998;Domsch et al, 2020), whereas forced expression of vertebrate Twist proteins can even reverse myogenic differentiation in vitro by unwiring the myogenic regulatory network from its targets (Hjiantoniou et al, 2008;Li et al, 2019;Liu et al, 2017;Mastroyiannopoulos et al, 2013) and appear to play a role during the regeneration of craniofacial muscles (Zhao et al, 2020). Here we provide evidence that (Pan, 2010;Wang et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

Twist regulates Yorkie to guide lineage reprogramming of syncytial alary muscles

Rose

Bartle-Schultheis

Domsch

et al. 2020

Preprint

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The genesis of syncytial muscles is typically considered as a paradigm for an irreversible developmental process. Notably, transdifferentiation of syncytial muscles is naturally occurring during Drosophila development. The ventral longitudinal heart associated musculature (VLM) arises by a unique mechanism that revokes the differentiated fate from the so-called alary muscles and comprises at least two distinct steps: syncytial muscle cell fragmentation into single myoblasts and direct reprogramming into founder cells of the VLM lineage. Here we provide evidence that the mesodermal master regulator twist plays a key role during this reprogramming process. Acting downstream of Drosophila Tbx1 (Org-1) in the alary muscle lineage, Twist is crucially required for the derepression of the Hippo pathway effector Yki and thus for the initiation of syncytial muscle dedifferentiation and fragmentation. Subsequently, cell-autonomous FGFR-Ras-MAPK signaling in the resulting mononucleated myoblasts is maintaining Twist expression, thereby stabilizing nuclear Yki activity and inducing their lineage switch into the founder cells of the VLM.

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“…Tbx1 and Islet1 are required cell-autonomously for specification of ESM progenitors, Tbx1 acting genetically upstream of Islet1 ( Gopalakrishnan et al, 2015 ; Comai et al, 2019 ). More broadly, Tbx1 and Islet1 are major conserved actors in the genetic program controlling pharyngeal muscle development in chordates while Twi is involved in formation and regeneration of extraocular muscles ( Nathan et al, 2008 ; Sambasivan et al, 2011 ; Zhao et al, 2020 ; Whitman et al, 2022 ). In Drosophila, the Tbx1/Islet1 genetic hierarchy selectively controls AM/TARM development and, together with Twi, AM into VLM trans-differentiation ( Boukhatmi et al, 2014 ; Schaub et al, 2015 ; Rose et al, 2022 ).…”

Section: Ancestral Origin and Evolution Of Ams; The Tbx1-islet1 (Twi)...mentioning

confidence: 99%

Insights and perspectives on the enigmatic alary muscles of arthropods

Bataillé,

Lebreton,

Boukhatmi

et al. 2024

Front. Cell Dev. Biol.

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Three types of muscles, cardiac, smooth and skeletal muscles are classically distinguished in eubilaterian animals. The skeletal, striated muscles are innervated multinucleated syncytia, which, together with bones and tendons, carry out voluntary and reflex body movements. Alary muscles (AMs) are another type of striated syncytial muscles, which connect the exoskeleton to the heart in adult arthropods and were proposed to control hemolymph flux. Developmental studies in Drosophila showed that larval AMs are specified in embryos under control of conserved myogenic transcription factors and interact with excretory, respiratory and hematopoietic tissues in addition to the heart. They also revealed the existence of thoracic AMs (TARMs) connecting to specific gut regions. Their asymmetric attachment sites, deformation properties in crawling larvae and ablation-induced phenotypes, suggest that AMs and TARMs could play both architectural and signalling functions. During metamorphosis, and heart remodelling, some AMs trans-differentiate into another type of muscles. Remaining critical questions include the enigmatic modes and roles of AM innervation, mechanical properties of AMs and TARMS and their evolutionary origin. The purpose of this review is to consolidate facts and hypotheses surrounding AMs/TARMs and underscore the need for further detailed investigation into these atypical muscles.

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Twist3 is required for dedifferentiation during extraocular muscle regeneration in adult zebrafish

Cited by 8 publications

References 69 publications

Single-cell resolution of MET- and EMT-like programs in osteoblasts during zebrafish fin regeneration

Single-cell resolution of MET- and EMT-like programs in osteoblasts during zebrafish fin regeneration

Twist regulates Yorkie to guide lineage reprogramming of syncytial alary muscles

Insights and perspectives on the enigmatic alary muscles of arthropods

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