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Cilia, Centrosomes and Skeletal Muscle

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Cilia, Centrosomes and Skeletal Muscle International Journal of Molecular Sciences Review Cilia, Centrosomes and Skeletal Muscle Dominic C. H. Ng 1,*, Uda Y. Ho 1 and Miranda D. Grounds 2,* 1 School of Biomedical Science, Faculty of Medicine, University of Queensland, St Lucia, Brisbane, QLD 4072, Australia; [email protected] 2 School of Human Sciences, Faculty of Medicine, University of Western Australia, Perth, WA 6009, Australia * Correspondence: [email protected] (D.C.H.N.); [email protected] (M.D.G.) Abstract: Primary cilia are non-motile, cell cycle-associated organelles that can be found on most vertebrate cell types. Comprised of microtubule bundles organised into an axoneme and anchored by a mature centriole or basal body, primary cilia are dynamic signalling platforms that are intimately involved in cellular responses to their extracellular milieu. Defects in ciliogenesis or dysfunction in cilia signalling underlie a host of developmental disorders collectively referred to as ciliopathies, reinforcing important roles for cilia in human health. Whilst primary cilia have long been recognised to be present in striated muscle, their role in muscle is not well understood. However, recent studies indicate important contributions, particularly in skeletal muscle, that have to date remained underappreciated. Here, we explore recent revelations that the sensory and signalling functions of cilia on muscle progenitors regulate cell cycle progression, trigger differentiation and maintain a commitment to myogenesis. Cilia disassembly is initiated during myoblast fusion. However, the remnants of primary cilia persist in multi-nucleated myotubes, and we discuss their potential role in late-stage differentiation and myofiber formation. Reciprocal interactions between cilia and the extracellular matrix (ECM) microenvironment described for other tissues may also inform on parallel interactions in skeletal muscle. We also discuss emerging evidence that cilia on fibroblasts/fibro– adipogenic progenitors and myofibroblasts may influence cell fate in both a cell autonomous and non- Citation: Ng, D.C.H.; Ho, U.Y.; autonomous manner with critical consequences for skeletal muscle ageing and repair in response to Grounds, M.D. Cilia, Centrosomes injury and disease. This review addresses the enigmatic but emerging role of primary cilia in satellite and Skeletal Muscle. Int. J. Mol. Sci. cells in myoblasts and myofibers during myogenesis, as well as the wider tissue microenvironment 2021, 22, 9605. https://doi.org/ required for skeletal muscle formation and homeostasis. 10.3390/ijms22179605 Keywords: myogenesis; primary cilia; proliferation; differentiation; satellite cells; cytoskeleton; Academic Editor: Daniel Taillandier extracellular matrix Received: 5 August 2021 Accepted: 1 September 2021 Published: 4 September 2021 1. Introduction Cilia are evolutionarily conserved, microtubule-based cellular appendages that per- Publisher’s Note: MDPI stays neutral form numerous functions required for normal development. Ciliary dysfunction underlies with regard to jurisdictional claims in a broad spectrum of clinical conditions collectively known as ciliopathies. Cilia are com- published maps and institutional affil- posed of a core of microtubule bundles, termed axonemes, that are ensheathed in a ciliary iations. membrane compartment and anchored at the base by the matured mother centriole or basal body (Figure1A). In some specialised cells, such as spermatozoa and respiratory epithelia, the microtubule motor-driven biomechanical motion of cilia is required for fertility and to prevent chronic airway infections. Canonical axonomes in motile cilia are comprised Copyright: © 2021 by the authors. of nine doublet microtubules arranged in a radial configuration surrounding two cen- Licensee MDPI, Basel, Switzerland. tral microtubules in a 9 + 2 arrangement, whereas, in contrast, non-motile or primary This article is an open access article cilia axonemes are typically 9 + 0 in structure and lack central singlet microtubules [1] distributed under the terms and (Figure1B). These non-motile primary cilia are found in almost all other cell types, includ- conditions of the Creative Commons ing muscle myoblasts and myofibroblasts, where their full spectrum of functions remains Attribution (CC BY) license (https:// incompletely defined [2]. Originally believed to be vestigial organelles, it is now evident creativecommons.org/licenses/by/ that primary cilia function as sensory appendages that co-ordinate cell signalling pathways 4.0/). Int. J. Mol. Sci. 2021, 22, 9605. https://doi.org/10.3390/ijms22179605 https://www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2021, 22, x FOR PEER REVIEW 2 of 16 Int. J. Mol. Sci. 2021, 22, 9605 2 of 16 now evident that primary cilia function as sensory appendages that co-ordinate cell sig- nallingto regulate pathways proliferation, to regulate differentiation, proliferation, cell di polarityfferentiation, and cell–cell cell polarity communication and cell–cell [3 com-]. In- municationdeed, a sensory [3]. Indeed, role was a proposed sensory role for ciliawas observedproposed in for avian cilia muscle observed spindles in avian that muscle might spindlesdetect fluid that changes might indetect periaxial fluid spindle changes space in periaxial and relate spindle these changes space and to intrafusal relate these my- changesofibers [ 4to]. intrafusal In addition, myofibers primary cilia[4]. In in addition, various stem primary and progenitorcilia in various populations stem and contribute progen- itorto tissue populations morphogenesis contribute and to homeostasistissue morpho [5,genesis6]. Skeletal and musclehomeostasis constitutes [5,6]. Skeletal about 40% mus- of clean individual’sconstitutes about body 40% mass of and an individual’s is fundamental body to mass locomotion, and is fundamental temperature regulationto locomotion, and temperaturemetabolism [regulation7]. Thus, there and ismetabolism considerable [7]. interest Thus, there in the is molecular considerable and interest cellular in processes the mo- lecularinvolved and in cellular forming processes skeletal muscle involved (myogenesis) in forming during skeletal development muscle (myogenesis) and in situations during developmentof severe injury and that in situations required regenerationof severe injury and that new required muscle regeneration formation, plus andin new context muscle of formation,neuromuscular plus diseases.in context This of neuromuscular review focuses on diseases. the role This of non-motile review focuses primary on cilia the (hereinrole of non-motilereferred to simplyprimary as cilia cilia) (herein in skeletal referred myogenesis to simply and as discusses cilia) in theskeletal recent myogenesis revelations thatand discussesciliary appendages the recent revelations are intimately that involved ciliary appendages in the control are ofintimately cell fate involved decisions, in cell the cycle con- troltiming of cell and fate proliferative decisions, capacitycell cycle in ti muscle.ming and proliferative capacity in muscle. Figure 1. Primary cilia assembly and disassembly during myogenesis. ( A) The mother centriole with distal appendagesappendages forms the basal body of primary cilia. The The distal distal appendages appendages de delineatelineate a transition transition zone and and a a ciliary ciliary compartment compartment distinct from the cytoplasm. Axonemes are comprised of bundles of microtubules that extend upwards from the basal body and from the cytoplasm. Axonemes are comprised of bundles of microtubules that extend upwards from the basal body and are encased in a ciliary membrane. (B) Cross-sectional view of axoneme. Motile cilia possess a 9 + 2 radial configuration are encased in a ciliary membrane. (B) Cross-sectional view of axoneme. Motile cilia possess a 9 + 2 radial configuration of axonemal microtubules. Outer doublet microtubules are connected by nexin links and interact with central single mi- crotubulesof axonemal via microtubules. radial spoke complexes. Outer doublet Non-motile microtubules primary are cilia connected in muscle by are nexin organised links in and a 9 interact + 0 configuration. with central (C). single Cilia formationmicrotubules and via resorption radial spoke during complexes. myogenesis. Non-motile Satellite cells primary expressing cilia in PAX7 muscle (PAX7 are organised+ve) are ciliated, in a 9 and + 0 these configuration. are resorbed (C) asCilia satellite formation cells specify and resorption proliferative during myoblasts myogenesis. that express Satellite My cellsf5. Cilia expressing are briefly PAX7 reassembled (PAX7+ve )in are myoblasts ciliated, as and they these down- are regulateresorbed PAX7, as satellite upregulate cells specify MYOD proliferative (MYOD+ve) for myoblasts differentiation that express and exit Myf5. the Ciliacell cy arecle. briefly During reassembled late stage differentiation in myoblasts andas they fusion downregulate into myotubes, PAX7, cilia upregulate are disassembled, MYOD (MYOD and centroso+ve) formes differentiation undergo reduction. and exit Cilia the are cell largely cycle. Duringabsent in late mature stage myofibersdifferentiation but found and fusion on quiescent into myotubes, satellite cells cilia located are disassembled, between the and myofiber centrosomes and basal undergo lamina. reduction. Cilia are largely absent in mature myofibers but found on quiescent satellite cells located between the myofiber and basal lamina. 2. Formation and Resorption of Cilia during Skeletal Myogenesis 2. FormationSkeletal
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