Progranulin regulates zebrafish muscle growth and regeneration through maintaining the pool of myogenic progenitor cells

Li, Yen-Hsing; Chen, Hsu-Yu; Li, Ya-Wen; Wu, Sung–Yu; Wangta-Liu,; Lin, Gen; Hu, Shao‐Yang; Chang, Zen-Kuei; Gong, Hong‐Yi; Liao, Chia-Hsuan; Chiang, Keng-Yu; Huang, Chang-Wen; Wu, Jen‐Leih

doi:10.1038/srep01176

Cited by 29 publications

(38 citation statements)

References 29 publications

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“…Due to a teleost-specific genome duplication event, the zebrafish has two pax7 genes: pax7a and pax7b . Because pax7a and pax7b are both expressed in larval and/or adult zebrafish satellite-like cells and are implicated in repair and/or regeneration (Devoto et al, 2006, Feng et al, 2006, Gurevich et al, 2016; Hollway et al, 2007, Knappe et al, 2015; Li et al, 2013; Nord et al, 2013; Otten et al, 2012; Pipalia et al, 2016; Seger et al, 2011; Siegel et al, 2013; Stellabotte et al, 2007; Windner et al, 2015; this study), we made loss-of-function mutations in both genes (Fig. 9A, B).…”

Section: Resultsmentioning

confidence: 99%

“…It is well established that larval zebrafish muscle contains satellite-like cells (Devoto et al, 2006; Feng et al, 2006; Gurevich et al, 2016; Knappe et al, 2015; Li et al, 2013; Nord et al, 2013; Otten et al, 2012; Seger et al, 2011; Siegel et al, 2013; Stellabotte et al, 2007; Windner et al, 2015), suggesting that they may also be present in adult muscle. Separate studies have noted the presence of Pax7-positive cells in adult zebrafish skeletal muscle and on isolated myofibers from adult zebrafish (Hollway et al, 2007; Tee et al, 2012; Zhang and Anderson, 2014); however, it is still unclear how similar zebrafish satellite-like cells are to mammalian satellite cells.…”

Section: Introductionmentioning

confidence: 99%

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Satellite-like cells contribute to pax7-dependent skeletal muscle repair in adult zebrafish

Berberoglu

Gallagher

Morrow

et al. 2017

Developmental Biology

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Satellite cells, also known as muscle stem cells, are responsible for skeletal muscle growth and repair in mammals. Pax7 and Pax3 transcription factors are established satellite cell markers required for muscle development and regeneration, and there is great interest in identifying additional factors that regulate satellite cell proliferation, differentiation, and/or skeletal muscle regeneration. Due to the powerful regenerative capacity of many zebrafish tissues, even in adults, we are exploring the regenerative potential of adult zebrafish skeletal muscle. Here, we show that adult zebrafish skeletal muscle contains cells similar to mammalian satellite cells. Adult zebrafish satellite-like cells have dense heterochromatin, express Pax7 and Pax3, proliferate in response to injury, and show peak myogenic responses 4–5 days post-injury (dpi). Furthermore, using a pax7a-driven GFP reporter, we present evidence implicating satellite-like cells as a possible source of new muscle. In lieu of central nucleation, which distinguishes regenerating myofibers in mammals, we describe several characteristics that robustly identify newly-forming myofibers from surrounding fibers in injured adult zebrafish muscle. These characteristics include partially overlapping expression in satellite cells and regenerating myofibers of two RNA-binding proteins Rbfox2 and Rbfoxl1, known to regulate embryonic muscle development and function. Finally, by analyzing pax7a; pax7b double mutant zebrafish, we show that Pax7 is required for adult skeletal muscle repair, as it is in the mouse.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Satellite-like cells contribute to pax7-dependent skeletal muscle repair in adult zebrafish

Berberoglu

Gallagher

Morrow

et al. 2017

Developmental Biology

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“…Measured gli1 and ptch1 mRNA levels, we found a reduction in expression levels of these genes in the 2DG treated as compared with the non-treatment group (Figure S2E). Injection of ampk morpholino (MO) into zebrafish embryos led to a reduction of ampk mRNA level in comparison with the control MO (Five base pair mismatches of the ampk MO)(Li et al, 2013) and two-fold elevation of gli1 and ptch1 mRNA levels as compared to the control group (Figure S2F). …”

Section: Resultsmentioning

confidence: 99%

AMP-Activated Protein Kinase Directly Phosphorylates and Destabilizes Hedgehog Pathway Transcription Factor GLI1 in Medulloblastoma

Luo

Mosley

et al. 2015

Cell Reports

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Summary The Hedgehog (Hh) pathway regulates cell differentiation and proliferation during development by controlling the Gli transcription factors. Cell fate decisions and progression toward organ and tissue maturity must be coordinated and how energy sensor regulates Hh pathway is not clear. AMP-activated Protein Kinase (AMPK) is an important sensor of energy stores that controls protein synthesis and other energy-intensive processes. AMPK is directly responsive to intracellular AMP levels, inhibiting a wide range of cell activities if ATP is low and AMP is high. Thus, AMPK can affect development by influencing protein synthesis and other processes needed for growth and differentiation. Activation of AMPK reduces GLI1 protein levels and stability, thus blocking Sonic hedgehog-induced transcriptional activity. AMPK phosphorylates GLI1 at serines 102 and 408 and threonine 1074. Mutation of these three sites into alanine prevents phosphorylation by AMPK. This in turn leads to increased GLI1 protein stability, transcriptional activity, and oncogenic potency.

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“…In addition, several chemicals identified in drug screens performed on zebrafish embryos stimulated either hair cell regeneration Larvae CuSO 4 mantle cells skin prep for FACS skins of 50 larvae microarray 8,569 [69] or supernumerary hair cell development in the absence of injury, suggesting the same developmental pathways are being triggered in both cases [71] . This reactivation of developmental pathways was also observed during regeneration of other tissues in zebrafish [92] , as well as in other model systems [90,93] . These findings suggest that under certain conditions triggering specific differentiation pathways can result in some restoration of hair cell numbers.…”

Section: Shared Mechanisms Between Regeneration and Developmentmentioning

confidence: 65%

Using Zebrafish to Study Human Deafness and Hearing Regeneration

Varshney¹,

Pei²,

Burgess³

2016

Monographs in Human Genetics

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Since the publication of the first draft of the human genome sequence in 2001, there has been an explosion in the number of genes associated with human genetic diseases, including those involved in human deafness. Clinical studies, genome-wide association studies, and exome resequencing have all added to the ever-expanding candidate list of genes with a role in hearing. Because human genetic data is primarily correlative, this explosion of data has increased the need for more efficient approaches to confirm these candidate genes in a model system. In addition, as our understanding of stem cells and genome editing advances, the potential for restoring hearing through regenerative medicine increases. This review highlights the role zebrafish can play as a model for human deafness, and also its potential role in discovering regenerative medicine therapies to restore lost hearing. © 2016 S. Karger AG, BaselHearing loss is one of the most common quality-oflife pathologies affecting the human population. Approximately 2-3 of every 1,000 newborns have a detectable level of hearing loss in one or both ears, and more than 10% of the American population over 18 years of age are suffering with some level of hearing loss, with a clear progression in hearing loss as the person ages (National Institute on Deafness and Other Communication Disorders, http:// www.nidcd.nih.gov/health/ statistics/Pages/quick. aspx). At age 70 and above, over 50% of the population has measurable hearing loss.Hearing is mediated by a sensory epithelium containing acoustic mechanosensory receptors called hair cells and a second cell type known as supporting cells located in the cochlea of the inner ear [1] . This epithelium converts sound waves into electrical impulses ultimately interpreted as hearing in the brain. Hearing loss can be caused by many factors such as exposure to loud noise (https://www.nidcd.nih.gov/staticresources/ health/hearing/NIDCD-Noise-Induced-HearingLoss.pdf), ototoxic chemicals (aminoglycoside antibiotics, cisplatin) [2] , infection [3] , or head injury [4,5] . Genetic factors are likely to play an important role in disease pathogenesis, and recent work has attempted to identify genes that make individuals more susceptible to progressive hearing loss [6] .Like most fish, zebrafish have two related sensory organs that utilize the mechanosensory hair cell receptors: (1) the inner ear similar to mammalian ears used to detect sound, gravity, and motion, and (2) the lateral line [7] , a fish-and am-

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Progranulin regulates zebrafish muscle growth and regeneration through maintaining the pool of myogenic progenitor cells

Cited by 29 publications

References 29 publications

Satellite-like cells contribute to pax7-dependent skeletal muscle repair in adult zebrafish

Satellite-like cells contribute to pax7-dependent skeletal muscle repair in adult zebrafish

AMP-Activated Protein Kinase Directly Phosphorylates and Destabilizes Hedgehog Pathway Transcription Factor GLI1 in Medulloblastoma

Using Zebrafish to Study Human Deafness and Hearing Regeneration

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