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The Diversity of Muscles and Their Regenerative Potential Across Animals

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The Diversity of Muscles and Their Regenerative Potential Across Animals cells Review The Diversity of Muscles and Their Regenerative Potential across Animals Letizia Zullo 1,2,*, Matteo Bozzo 3 , Alon Daya 4 , Alessio Di Clemente 1,5, Francesco Paolo Mancini 6 , Aram Megighian 7,8 , Nir Nesher 4, Eric Röttinger 9, Tal Shomrat 4, Stefano Tiozzo 10 , Alberto Zullo 6,* and Simona Candiani 3 1 Istituto Italiano di Tecnologia, Center for Micro-BioRobotics & Center for Synaptic Neuroscience and Technology (NSYN), 16132 Genova, Italy; [email protected] 2 IRCCS Ospedale Policlinico San Martino, 16132 Genova, Italy 3 Laboratory of Developmental Neurobiology, Department of Earth, Environment and Life Sciences, University of Genova, Viale Benedetto XV 5, 16132 Genova, Italy; [email protected] (M.B.); [email protected] (S.C.) 4 Faculty of Marine Sciences, Ruppin Academic Center, Michmoret 40297, Israel; [email protected] (A.D.); [email protected] (N.N.); [email protected] (T.S.) 5 Department of Experimental Medicine, University of Genova, Viale Benedetto XV, 3, 16132 Genova, Italy 6 Department of Science and Technology, University of Sannio, 82100 Benevento, Italy; [email protected] 7 Department of Biomedical Sciences, University of Padova, 35131 Padova, Italy; [email protected] 8 Padova Neuroscience Center, University of Padova, 35131 Padova, Italy 9 Institute for Research on Cancer and Aging (IRCAN), Université Côte d’Azur, CNRS, INSERM, 06107 Nice, France; [email protected] 10 Laboratoire de Biologie du Développement de Villefranche-sur-Mer (LBDV), Sorbonne Université, CNRS, 06230 Paris, France; [email protected] * Correspondence: [email protected] (L.Z.); [email protected] (A.Z.) Received: 23 July 2020; Accepted: 17 August 2020; Published: 19 August 2020 Abstract: Cells with contractile functions are present in almost all metazoans, and so are the related processes of muscle homeostasis and regeneration. Regeneration itself is a complex process unevenly spread across metazoans that ranges from full-body regeneration to partial reconstruction of damaged organs or body tissues, including muscles. The cellular and molecular mechanisms involved in regenerative processes can be homologous, co-opted, and/or evolved independently. By comparing the mechanisms of muscle homeostasis and regeneration throughout the diversity of animal body-plans and life cycles, it is possible to identify conserved and divergent cellular and molecular mechanisms underlying muscle plasticity. In this review we aim at providing an overview of muscle regeneration studies in metazoans, highlighting the major regenerative strategies and molecular pathways involved. By gathering these findings, we wish to advocate a comparative and evolutionary approach to prompt a wider use of “non-canonical” animal models for molecular and even pharmacological studies in the field of muscle regeneration. Keywords: myogenesis; evolution; metazoans; differentiation; transdifferentiation; muscle precursors; regenerative medicine 1. Introduction One particular challenge in regenerative biology concerns the development of reconstructive strategies after muscle-related injuries, but also the treatments of degenerative myopathies for which no reliable clinical strategy exists such as muscle dystrophy, sarcopenia, cachexia, to mention just a few [1,2]. In mammals regenerative capacities are restricted to only a small number of organs [3], yet, Cells 2020, 9, 1925; doi:10.3390/cells9091925 www.mdpi.com/journal/cells Cells 2020, 9, 1925 2 of 35 Cells 2020, 9, x 2 of 35 inin otherother metazoans,metazoans, thethe abilityability toto respondrespond toto environmentalenvironmental injuriesinjuries rangesranges fromfrom “simple”“simple” woundwound healinghealing toto completecomplete anatomicalanatomical andand functionalfunctional restorationrestoration of thethe lostlost oror damageddamaged part of the body, includingincluding muscles muscles [ [4].4]. TheThe musculaturemusculature isis aa tissuetissue specializedspecialized inin contractioncontraction andand cellscells withwith contractilecontractile functionsfunctions areare presentpresent inin almostalmost allall metazoansmetazoans but,but, despitedespite theirtheir structuralstructural similarity,similarity, thethe originorigin ofof musclesmuscles isis consideredconsidered toto bebe thethe outcomeoutcome ofof aa process process of of convergent convergent evolution evolution [ 5[5].]. Indeed,Indeed, typicaltypical musclemuscle proteinprotein corecore setssets areare presentpresent eveneven inin unicellularunicellular organismsorganisms andand inin earlyearly divergeddiverged organismsorganisms likelike sponges, sponges, which which lacks lacks a proper a proper tissue tissue organization organization and therefore and therefore “true” muscles, “true” andmuscles, in cnidarians, and in wherecnidarians, muscle-like where muscle-like cells are present cells are but present lack almost but lack all almost molecular all molecular hallmarks hallmarks of bilaterian of bilaterian striated musclesstriated thusmuscles suggesting thus suggesting evolution fromevolution cells withfromancient cells with contractile ancient machinery contractile [ 5machinery]. The processes [5]. The of myogenesisprocesses of and myogenesis muscle homeostasis and muscle have homeostasis also various have degrees also various of conservation degrees amongof conservation different clades,among anddifferent so is theclades, extent and of so muscle is the regenerativeextent of muscle capabilities regenerative [5–10 ].capabilities [5–10]. AnimalsAnimals adopt different different basi basicc strategies strategies of of regeneration regeneration that that include include the theactivation activation of adult of adult stem stemcells, cells,the dedifferentiation the dedifferentiation of preexisting of preexisting cells, and/or cells, the and proliferation/or the proliferation of differentiated of diff erentiatedcells. This cells.diversity This of mechanisms diversity of is mechanismsstill widely understudied is still widely and underexploited understudied for and biomedical underexploited applications. for biomedicalIn thisapplications. review, we provide an outline of main animals’ clades (see Figure 1), muscle types, their development,In this review, homeostasis, we provide and regeneration an outline of abilities main animals’highlighting clades what (see is known Figure1 of), muscletheir molecular types, theirmechanisms. development, We emphasize homeostasis, some andpotential regeneration contributi abilitiesons of comparative highlighting studies what into is known the biomedical of their molecularfields, therefore mechanisms. advocating We emphasize deeper employment some potential of ‘non-canonical’ contributionsof animals comparative as models studies for into muscle the biomedicalregeneration fields, studies. therefore advocating deeper employment of ‘non-canonical’ animals as models for muscle regeneration studies. Figure 1. Tree of the animals’ clades treated in this review (in brackets the corresponding sectionFigure numbers).1. Tree of the animals’ clades treated in this review (in brackets the corresponding section numbers). Understanding the molecular pathways and mechanistic underlying regenerative events may offer insightsUnderstanding into potential the methods molecular to unlock pathways regeneration and mech inanistic animals underlying where the regeneratingregenerative capabilitiesevents may areoffer more insights restricted, into e.g.,potential mammals. methods Indeed, to unlock regeneration regeneration is greatly in attenuatedanimals where in mammals the regenerating although portionscapabilities of major are organs,more restricted, such as the e.g., liver, mammals. retain event-triggered Indeed, regeneration regenerative is potentialsgreatly attenuated for the entire in animal’smammals life although [2]. Interestingly, portions recentof major pieces organs, of evidence such as suggest the liver, that retain regeneration event-triggered can be induced regenerative even inpotentials non-regenerating for the speciesentire animal’s by altering life specific [2]. Intere signalingstingly, pathways recent [ 11pieces–13]. Thisof evidence might be suggest also the casethat regeneration can be induced even in non-regenerating species by altering specific signaling pathways Cells 2020, 9, 1925 3 of 35 for mammals and thus the principles underlying the induction of regeneration in non-regenerating species may be transferred to humans to trigger regeneration [3,14]. Elucidating muscle regeneration in metazoans also provides opportunities to ‘model’ a complex biological process relevant to human health and offers a window into fundamental principles underpinning this important response. 2. Porifera: Low Body Complexity with High Regenerative Capabilities The phylum Porifera includes mainly sponges, aquatic multicellular organisms with relatively simple anatomy, lacking an organization of tissues and organs. They have a very simple functioning relying on water circulating throughout a system of canals and chambers, called a water-current system. Circulatory, digestive, nervous, and muscular systems are completely absent. Their body is composed of a few types of cells [15,16]. For instance, in demosponges we found pinacocytes (the skin cells), mesenchymal cells, choanocytes (lining in the interior body walls), archaeocytes (totipotent cells), sclerocytes, myocytes, and porocytes (surrounding canal openings). Two types of contractile cells can be identified: the pinacocytes, and the myocytes.
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