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Repair of Damaged Articular Cartilage: Current Approaches and Future Directions

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Repair of Damaged Articular Cartilage: Current Approaches and Future Directions International Journal of Molecular Sciences Review Repair of Damaged Articular Cartilage: Current Approaches and Future Directions Ekaterina V. Medvedeva 1,*, Ekaterina A. Grebenik 1, Svetlana N. Gornostaeva 1, Vladimir I. Telpuhov 1, Aleksey V. Lychagin 2, Peter S. Timashev 1,3,4 and Andrei S. Chagin 1,5,* 1 Institute for Regenerative Medicine, Sechenov University, 8-2 Trubetskaya St., Moscow 119991, Russia; [email protected] (E.A.G.); [email protected] (S.N.G.); [email protected] (V.I.T.); [email protected] (P.S.T.) 2 Department of Trauma, Orthopedics and Disaster Surgery, Sechenov University, 8-2 Trubetskaya St., Moscow 119991, Russia; [email protected] 3 Department of Polymers and Composites, N. N. Semenov Institute of Chemical Physics, 4 Kosygin St., Moscow 119991, Russia 4 Institute of Photonic Technologies, Research Center “Crystallography and Photonics”, RAS, 2 Pionerskaya St., Troitsk, Moscow 142190, Russia 5 Department of Physiology and Pharmacology, Karolinska Institutet, Biomedicum 6D, Stockholm 17177, Sweden * Correspondence: [email protected] (E.V.M.); [email protected] (A.S.C.) Received: 29 June 2018; Accepted: 7 August 2018; Published: 11 August 2018 Abstract: Articular hyaline cartilage is extensively hydrated, but it is neither innervated nor vascularized, and its low cell density allows only extremely limited self-renewal. Most clinical and research efforts currently focus on the restoration of cartilage damaged in connection with osteoarthritis or trauma. Here, we discuss current clinical approaches for repairing cartilage, as well as research approaches which are currently developing, and those under translation into clinical practice. We also describe potential future directions in this area, including tissue engineering based on scaffolding and/or stem cells as well as a combination of gene and cell therapy. Particular focus is placed on cell-based approaches and the potential of recently characterized chondro-progenitors; progress with induced pluripotent stem cells is also discussed. In this context, we also consider the ability of different types of stem cell to restore hyaline cartilage and the importance of mimicking the environment in vivo during cell expansion and differentiation into mature chondrocytes. Keywords: articular hyaline cartilage; regenerative medicine approaches; stem cells; tissue-engineered constructs; cell-based therapy; micro-fracture; mosaicplasty; autologous chondrocyte implantation (ACI); matrix-induced autologous chondrocyte implantation (MACI) 1. Introduction Hyaline articular cartilage tissue is extensively hydrated, but it is neither innervated nor vascularized, and its very low cell density allows, unlike bone, only extremely limited self-renewal. Thus, in vivo restoration and/or in vitro reconstruction of hyaline cartilage is the goal of numerous tissue-engineering approaches; however, success remains limited to date. The apparent structural simplicity of hyaline cartilage is deceptive. Despite lacking innervation and blood vessels, this tissue consists of several layers, differing slightly in organization (e.g., cell density, composition of the extracellular matrix (ECM), and orientation of collagen fibers [1]), and thereby, in local elastic modulus [2]. Moreover, although the cartilage contains only a single type of cell referred to as chondrocytes, the cells in different layers have distinct morphologies and functionalities [3]. This tissue is usually divided into four zones: (i) the superficial zone in contact with Int. J. Mol. Sci. 2018, 19, 2366; doi:10.3390/ijms19082366 www.mdpi.com/journal/ijms Int.Int. J. Mol. Sci. 2018, 19, 2366x 22 of 2322 functionalities [3]. This tissue is usually divided into four zones: (i) the superficial zone in contact thewith synovial the synovial fluid, containingfluid, containing chondro-progenitors chondro‑progenitors [4,5]; (ii) [4,5]; the middle(ii) the ormiddle transitional or transitional zone beneath zone thebeneath superficial the superficial zone, containing zone, containing round chondrocytes; round chondrocytes; (iii) the deep (iii) or the radial deep zone; or radial and (iv) zone; the calcifiedand (iv) layerthe calcified in direct layer contact in direct with thecontact underlying with the subchondral underlying subchondral bone (Figure 1bone). (Figure 1). Figure 1. Structure of human articular cartilage. Articular cartilage from a 57‑year‑old man is stained Figure 1. Structure of human articular cartilage. Articular cartilage from a 57-year-old man is stained with Safranin O/Fast Green (images were made by E. V. Medvedeva). with Safranin O/Fast Green (images were made by E. V. Medvedeva). Degenerative lesions of articular cartilage as a consequence of destructive joint disease, such as osteoarthritisDegenerative (OA) lesions, can oflead articular to disability, cartilage pain as a consequenceduring movement of destructive of the joint joint disease,, and gradual such as osteoarthritisdeformation of (OA), the canbone lead articulati to disability,on. OA pain is the during most movement common ofmusculoskeletal the joint, and gradual disorder, deformation affecting of10– the12% bone of the articulation. global population OA is the[6]. mostFor people common above musculoskeletal 65 years of age, disorder, this incidence affecting rises 10–12% to 49.7% of the(World global Health population Organization [6]. For people(WHO) abovestatistics 65 years 2010) of, age,and thisthese incidence numbers rises continue to 49.7% ris (Worlding in Healthconnection Organization with the aging (WHO) of the statistics society 2010), and an and escalating these numbers epidemic continue of obesity. rising Current in connection treatments with of theknee aging and ofhip the OA society include and cyclooxygenase an escalating epidemic 2 (COX‑ of2)‑ obesity.selective Current [7] and treatments nonselective of kneenonsteroidal and hip OAanti‑ includeinflammatory cyclooxygenase drugs (NSAIDs) 2 (COX-2)-selective, as well as [7 ]intra and‑ nonselectivearticular injections nonsteroidal of corticosteroids anti-inflammatory [8,9], drugsthereby (NSAIDs), focusing on as wellreducing as intra-articular pain and inflammation injections of without corticosteroids addressing [8,9 the], thereby underlying focusing causes, on reducingwhich eventually pain and leads inflammation to joint withoutreplacement addressing surgery. the The underlying etiology causes,of OA whichis not eventuallyyet understood leads tocompletely joint replacement; however, surgery. aging, The trauma, etiology genetic of OA ispredisposition, not yet understood obesity, completely; inflammation, however, and aging, the trauma,metabolic genetic syndrome predisposition, are known obesity, to be involved inflammation, in this anddisease the metabolic[10]. The u syndromenclear etiology are known of OA to and be involvedincreased inlevel this of disease inflammation [10]. The pose unclear additional etiology barriers of OA for and regenerative increasedlevel approaches of inflammation aiming to posecure additionalthe disease barriers, and most for clinical regenerative and research approaches effort aimings in this to area cure currently the disease, focus and on mostthe restoration clinical and of researchtraumatic efforts damage in this to cartilage, area currently which, focus if untreated, on the restoration leads ultimately of traumatic to the damage development to cartilage, of OA which, and ifthe untreated, necessity leads for joint ultimately replacement. to the developmentIn this review of, we OA summarize and the necessity and discuss for joint present replacement. approaches In this to review,cartilage we repair, summarize as well andas potential discuss new present directions approaches (Figure to cartilage2). repair, as well as potential new directionsHere,(Figure we categorized2). the therapeutic approaches for treating traumatic and degenerative pathologyHere, of we articular categorized cartilage the therapeuticinto three major approaches groups: for symptomatic treating traumatic treatment and (left degenerative‑hand side), pathologyclinically available of articular restoration cartilage intoprocedures three major (middle groups: column) symptomatic, and those treatment under (left-hand development side), clinically(right‑hand available side). restorationSymptomatic procedures procedures (middle can column),be further and sub those‑divided under developmentinto systemic (right-hand treatment side).(usually Symptomatic pain kille proceduresrs and anti can‑inflammatory be further sub-divided drugs) and into local systemic intra‑ treatmentarticular (usuallyinjections pain, such killers as andinjections anti-inflammatory of corticosteroids drugs) or and platelet local intra-articular‑rich plasma. injections,Clinically suchavailable as injections cartilage of repair corticosteroids (middle orcolumn) platelet-rich can be plasma. divided Clinically into two available sub‑categories: cartilage surgical repair (middleapproaches column) (e.g., can microfracture be divided intoand twomosaicplasty) sub-categories: and those surgical based approaches on regenerative (e.g., medicine microfracture (e.g., implantation and mosaicplasty) of expanded and those autologous based onchondrocytes). regenerative The medicine wide variety (e.g., implantationof approaches of to expandedrestoration autologous under development chondrocytes). (right‑hand The wideside) varietyinvolve ofcell approaches expansion toand restoration differentiation under in developmentto mature
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