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Collective Locomotion of Human Cells, Wound Healing and Their Control by Extracts and Isolated Compounds from Marine Invertebrates

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Collective Locomotion of Human Cells, Wound Healing and Their Control by Extracts and Isolated Compounds from Marine Invertebrates molecules Review Collective Locomotion of Human Cells, Wound Healing and Their Control by Extracts and Isolated Compounds from Marine Invertebrates Claudio Luparello * , Manuela Mauro , Valentina Lazzara and Mirella Vazzana Department of Biological, Chemical and Pharmaceutical Sciences and Technologies (STEBICEF), University of Palermo, 90128 Palermo, Italy; [email protected] (M.M.); [email protected] (V.L.); [email protected] (M.V.) * Correspondence: [email protected]; Tel.: +39-91-238-97405 Received: 10 May 2020; Accepted: 25 May 2020; Published: 26 May 2020 Abstract: The collective migration of cells is a complex integrated process that represents a common theme joining morphogenesis, tissue regeneration, and tumor biology. It is known that a remarkable amount of secondary metabolites produced by aquatic invertebrates displays active pharmacological properties against a variety of diseases. The aim of this review is to pick up selected studies that report the extraction and identification of crude extracts or isolated compounds that exert a modulatory effect on collective cell locomotion and/or skin tissue reconstitution and recapitulate the molecular, biochemical, and/or physiological aspects, where available, which are associated to the substances under examination, grouping the producing species according to their taxonomic hierarchy. Taken all of the collected data into account, marine invertebrates emerge as a still poorly-exploited valuable resource of natural products that may significantly improve the process of skin regeneration and restrain tumor cell migration, as documented by in vitro and in vivo studies. Therefore, the identification of the most promising invertebrate-derived extracts/molecules for the utilization as new targets for biomedical translation merits further and more detailed investigations. Keywords: marine invertebrates; cell migration; wound healing 1. Introduction The collective migration of cells is a complex integrated process at the basis of several different physiological events, such as embryo development, tissue shaping, and wound healing, whereas, in the course of diseases, like carcinogenesis, it is strongly implied in the step of tumor cell metastatization. In the recent years, a great deal of literature papers has focused on the molecular, biophysical and cytological aspects of cell locomotory patterns in the awareness of the clinical relevance shown by the advancement of knowledge on the mechanism and dynamism of collective cell migration. These studies shed light upon the mechanobiological bases of movement generation and speed/orientation setting and unveiled some of the signal transduction properties that are linked to the biochemical features of the migratory process. As a result of this research, the roles played in epithelial-mesenchymal transition (EMT) by integrin, junction protein and cytoskeletal dynamics, growth factor/cytokine and metalloprotease secretion, as well as cell interactions with components of the extracellular matrix (ECM) have been increasingly elucidated. A comprehensive overview of these topics can be found in several previously-published reviews [1–3]. Among the events of tissue repair involving collective cell motility, skin wound healing represents a multi-step coordinated process, which, following the initial inflammatory and hemostatic stages, associates re-epithelization, i.e., epidermal cell locomotion and growth on top of the granulation tissue, Molecules 2020, 25, 2471; doi:10.3390/molecules25112471 www.mdpi.com/journal/molecules Molecules 2020, 25, x FOR PEER REVIEW 2 of 42 Molecules 2020, 25, 2471 2 of 40 hemostatic stages, associates re-epithelization, i.e., epidermal cell locomotion and growth on top of the granulation tissue, with tissue recovery implying the restoration of vascularization via withangiogenesis tissue recovery and fibroplasia, implying the which restoration is the ofrecruitment vascularization of activated via angiogenesis fibroblasts and and fibroplasia, newly- whichdifferentiated is the recruitment myofibroblasts of activated for ECM fibroblasts reconsti andtution newly-di and woundfferentiated contraction myofibroblasts [4–8]. Once for ECMthe reconstitutionwound damage and is woundrepaired, contraction a final tissue [4– 8remodeling]. Once the is woundundertaken damage to restore is repaired, skin integrity a final tissueand remodelingstructure [9,10]. is undertaken During towound restore re-epithelization, skin integrity and human structure keratinocytes [9,10]. During move wound in a re-epithelization,spatially- and humandirectionally-organized keratinocytes move way, in a spatially- whose andmolecular directionally-organized basis can be found way, whose in specific molecular cell-ECM basis can beinteractions, found in specific like the cell-ECM binding interactions, of type XVII like thecolla bindinggen by of both type intermediate XVII collagen filament by both intermediateand actin filamentcytoskeleton and actinvia hemidesmosomal cytoskeleton via actinin hemidesmosomal 4, and the creation actinin 4,of andgradients the creation of epidermal of gradients growthof epidermalfactor (EGF) growth immobilized factor (EGF) within immobilized the ECM and within presen theted ECM to andcell receptors presented [11,12]. to cell receptorsIndeed, EGF [11 ,is12 ]. Indeed,one of EGFthe most is one potent of the regulators most potent of keratinocy regulatorste of locomotory keratinocyte behavior locomotory along behaviorwith transforming along with transforminggrowth factor growth (TGF)- factorβ, whose (TGF)- prominentβ, whose prominentregulatory regulatoryeffect on epidermal effect on epidermalcell motility cell during motility duringwound wound repair repairvia ERK via signaling ERK signaling pathways pathways is widely is widely acknowledged acknowledged [13]. Scientific [13]. Scientific interest interest has hasalso also focused focused upon upon the the transcriptional transcriptional factors factors that that are are up-regulated up-regulated and and activated activated in inmigrating migrating keratinocyteskeratinocytes during during the the repair repair process, process, leading leading to theto the identification, identification, among among others, others, of Smad7, of Smad7, Stat3, andStat3, c-Jun, and which c-Jun, are which functionally are functionally involved ininvolved the promotion in the promotion of cutaneous of woundcutaneous healing, wound as extensively healing, reviewedas extensively by Boudra reviewed and Ramsey by Boudra [14 ].and Ramsey [14]. CollectiveCollective cell cell motility motility can can be studiedbe studied both both in culture in culture and in and vivo in. Invivo. the firstIn the case, first the case, migratory the behaviourmigratory of behaviour cell monolayers of cell canmonolayers be evaluated can be via evaluated the “in vitro via woundthe “in healing”vitro wound or “scratch” healing” assay, or in“scratch” which a assay, gap is in created which bya gap scratching is created a pipetteby scratching tip through a pipette a confluent tip through sheet a confluent of cells insheet culture of (Figurecells in1A), culture and the(Figure eventually-occurring 1A), and the eventually-occurring bidimensional cell bidimensional migration leading cell migration to the closure leading of to the scratchthe closure being of recorded the scratch by eitherbeing recorded phase-contrast by either microscopic phase-contrast images microscopic captured at images regular captured intervals at or time-lapseregular intervals videomicroscopy or time-lapse [15]. videomicroscopy [15]. FigureFigure 1. 1.(A A)) Phase-contrastPhase-contrast microscopic image of of a a scratch scratch created created in in a amonolayer monolayer of of HEPG2 HEPG2 liver liver carcinomacarcinoma cells. cells. (B )B Light) Light microscopic microscopic image image of MDA-MB231 of MDA-MB breast231 breast carcinoma carcinoma cells migratedcells migrated through thethrough pores of the a polycarbonate pores of a polycarbonate filter in a Boyden filter chamberin a Boyden assay, cham fixedber with assay, 95% fixed ethanol, with and 95% stained ethanol, with 0.02and g stained toluidine with blue 0.02/mL. g Bartoluidine= 10 µ blue/mL.m. Bar = 10 μm. WhenWhen the the model model system system studied studied is a tumor is a celltumor line, cell the scratchline, the assay scratch is commonly assay is complemented commonly bycomplemented either the “Boyden by either chamber” the “Boyden or the “transwell chamber” migration or the “transwell/invasion” migration/invasion” assays, as originally assays, developed as byoriginally Albini and developed coworkers by [ 16Albini], which and measure coworkers the [16], ability which of a populationmeasure the of ability neoplastic of a population cells to migrate of individuallyneoplastic cells through to migrate a physical individually barrier, i.e.,through an untreated a physical or barrier, basement i.e., membrane an untreated (Matrigel)-coated or basement porousmembrane polyester (Matrigel)-coated membrane, in porous response polyester to a chemoattractant membrane, in response or a motility-promoting to a chemoattractant compound or a (Figuremotility-promoting1B) [17,18]. compound (Figure 1B) [17,18]. DealingDealing with within vivoin vivoexperimental experimental systems, systems, the group the group locomotion locomotion of tumor of cellstumor might cells be might examined be throughexamined the through chick embryo the chick chorioallantoic embryo chorioallantoic membrane
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