Single-cell transcriptome analysis reveals three sequential phases of gene expression during zebrafish sensory hair cell regeneration

Baek, Sungmin; Tran, Nhung T. T.; Diaz, Daniel C; Tsai, Ya-Yin; Acedo, Joaquín Navajas; Lush, Mark E.; Piotrowski, Tatjana

doi:10.1016/j.devcel.2022.03.001

Cited by 57 publications

(59 citation statements)

References 128 publications

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“…While inner ear and lateral line hair cells share many structural and functional features, we sought to determine if these cells also have distinct molecular signatures. We compared published datasets of lateral line hair cells (Baek et al, 2022; Kozak et al, 2020; Ohta et al, 2020) to our data, restricting analysis to datasets generated by 10x Chromium preparation to avoid technical batch effects across studies. Using Scanorama for alignments (Hie et al, 2019), hair cells from the inner ear and lateral line form distinct clusters, with a number of differentially expressed genes (Supplemental Figure 5), including the known markers for lateral line ( s100t ) and inner ear ( strc ) (Figure 3).…”

Section: Resultsmentioning

confidence: 99%

Single-Cell Transcriptomic Profiling of the Zebrafish Inner Ear Reveals Molecularly Distinct Hair Cell and Supporting Cell Subtypes

Shi

Beaulieu

Saunders

et al. 2022

Preprint

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A major cause of human deafness and vestibular dysfunction is permanent loss of the mechanosensory hair cells of the inner ear. In non-mammalian vertebrates such as zebrafish, regeneration of missing hair cells can occur throughout life. While a comparative approach has the potential to reveal the basis of such differential regenerative ability, the degree to which the inner ears of fish and mammals share common hair cells and supporting cell types remains unresolved. Here we perform single-cell RNA sequencing of the zebrafish inner ear at embryonic through adult stages to catalog the diversity of hair cell and non-sensory supporting cells. We identify a putative progenitor population for hair cells and supporting cells, as well as distinct hair cells and supporting cell types in the maculae versus cristae. The hair cell and supporting cell types differ from those described for the lateral line system, a distributed mechanosensory organ in zebrafish in which most studies of hair cell regeneration have been conducted. In the maculae, we identify two subtypes of hair cells that share gene expression with mammalian striolar or extrastriolar hair cells. In situ hybridization reveals that these hair cell subtypes occupy distinct spatial domains within the two major macular organs, the utricle and saccule, consistent with the reported distinct electrophysiological properties of hair cells within these domains. These findings suggest that primitive specialization of spatially distinct striolar and extrastriolar hair cells likely arose in the last common ancestor of fish and mammals. The similarities of inner ear cell type composition between fish and mammals also support using zebrafish as a relevant model for understanding inner ear-specific hair cell function and regeneration.

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Section: Resultsmentioning

confidence: 99%

Single-Cell Transcriptomic Profiling of the Zebrafish Inner Ear Reveals Molecularly Distinct Hair Cell and Supporting Cell Subtypes

Shi

Beaulieu

Saunders

et al. 2022

Preprint

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“…From an evolutionary perspective, compared to other regeneration model species, such as planarians, zebrafish, and amphibians, echinoderms are still left behind. Single-cell transcriptomes have been applied to the regeneration of hydra [ 104 ], planaria [ 105 ], amphibian [ 106 ], and zebrafish [ 107 ], and cell types important for regeneration have been discovered. In the future, single-cell transcriptome and spatial transcriptome will help reveal typical cell type and spatial orientation.…”

Section: Discussionmentioning

confidence: 99%

A Review of Histocytological Events and Molecular Mechanisms Involved in Intestine Regeneration in Holothurians

Yang

Sun

2022

Biology

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Most species of the class Holothuroidea are able to regenerate most of their internal organs following a typical evisceration process, which is a unique mechanism that allows sea cucumbers to survive in adverse environments. In this review, we compare autotomy among different type of sea cucumber and summarize the histocytological events that occur during the five stages of intestinal regeneration. Multiple cytological activities, such as apoptosis and dedifferentiation, take place during wound healing and anlage formation. Many studies have focused on the molecular regulation mechanisms that underlie regeneration, and herein we describe the techniques that have been used as well as the development-related signaling pathways and key genes that are significantly expressed during intestinal regeneration. Future analyses of the underlying mechanisms responsible for intestinal regeneration should include mapping at the single-cell level. Studies of visceral regeneration in echinoderms provide a unique perspective for understanding whole-body regeneration or appendage regeneration.

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“…In the late stage, HC differentiation progressed in parallel with the downregulation of precursor genes. Similar to HC regeneration in gene-manipulated neonatal mouse cochleae (Li et al, 2022) and zebrafish (Baek et al, 2022), HC regeneration in chick BPs occurs in a stepwise fashion, and reversal to a precursor cell state may be a crucial process.…”

Section: Single-cell Rna Sequencing Reveals Stepwise Fate Conversion ...mentioning

confidence: 99%

“…Molecular analyses of BP development have focused on major signaling pathways, including Notch (Daudet et al, 2005; 2009; Petrovic et al, 2014), fibroblast growth factor (Bermingham-McDonogh et al, 2001; Jacques et al, 2012), and Wnt signaling (Sienknecht and Fekete, 2008; Munnamalai et al, 2017). However, information on the gene expression patterns in developing or regenerating chick BPs in comparison to those in the zebrafish lateral line was limited (Lush et al, 2019; Baek et al, 2022). The baseline data of homeostatic BPs have been recently reported (Janesick et al, 2021) using single-cell RNA-seq, which provides fundamental information to analyze the changes in gene expression in SCs toward HC regeneration, similar to the findings in zebrafish (Lush et al, 2019; Baek et al, 2022) and mice (Kolla et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

“…However, information on the gene expression patterns in developing or regenerating chick BPs in comparison to those in the zebrafish lateral line was limited (Lush et al, 2019; Baek et al, 2022). The baseline data of homeostatic BPs have been recently reported (Janesick et al, 2021) using single-cell RNA-seq, which provides fundamental information to analyze the changes in gene expression in SCs toward HC regeneration, similar to the findings in zebrafish (Lush et al, 2019; Baek et al, 2022) and mice (Kolla et al, 2020). To gain insights into the processes underlying SC-to-HC conversion in chick BPs, we conducted a high-resolution transcriptional analysis of SCs during SC-to-HC conversion in our explant culture model using single-cell RNA-seq.…”

Section: Introductionmentioning

confidence: 99%

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Single-cell RNA-seq reveals stepwise fate conversion of supporting cells to hair cells in the chick auditory epithelium

Matsunaga

Yamamoto

Kita

et al. 2022

Preprint

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In contrast to mammals, the avian cochlea, specifically the basilar papilla, can regenerate sensory hair cells, which involves fate conversion of supporting cells to hair cells. To determine the mechanisms for converting supporting cells to hair cells, we used single-cell RNA sequencing during hair cell regeneration in explant cultures of chick basilar papillae. We identified dynamic changes in the gene expression of supporting cells, and the pseudotime trajectory analysis demonstrated the stepwise fate conversion from supporting cells to hair cells. Initially, supporting cell identity was erased and transition to the precursor state occurred. A subsequent gain in hair cell identity progressed together with downregulation of precursor-state genes. Transforming growth factor beta receptor 1-mediated signaling was involved in induction of the initial step, and its inhibition resulted in suppression of hair cell regeneration. Our data provide new insights for understanding fate conversion from supporting cells to hair cells in avian basilar papillae.

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Single-cell transcriptome analysis reveals three sequential phases of gene expression during zebrafish sensory hair cell regeneration

Cited by 57 publications

References 128 publications

Single-Cell Transcriptomic Profiling of the Zebrafish Inner Ear Reveals Molecularly Distinct Hair Cell and Supporting Cell Subtypes

Single-Cell Transcriptomic Profiling of the Zebrafish Inner Ear Reveals Molecularly Distinct Hair Cell and Supporting Cell Subtypes

A Review of Histocytological Events and Molecular Mechanisms Involved in Intestine Regeneration in Holothurians

Single-cell RNA-seq reveals stepwise fate conversion of supporting cells to hair cells in the chick auditory epithelium

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