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Is the Conjunctiva a Potential Target for Advanced Therapy Medicinal Products?

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Is the Conjunctiva a Potential Target for Advanced Therapy Medicinal Products? pharmaceutics Review Is the Conjunctiva a Potential Target for Advanced Therapy Medicinal Products? Yolanda Diebold 1,2,* and Laura García-Posadas 1 1 Ocular Surface Group, Instituto de Oftalmobiología Aplicada (IOBA), Universidad de Valladolid, 47011 Valladolid, Spain; [email protected] 2 Centro de Investigación Biomédica en Red de Bioingeniería, Biomateriales y Nanomedicina (CIBER-BBN), Instituto de Salud Carlos III, 28029 Madrid, Spain * Correspondence: [email protected] Abstract: The conjunctiva is a complex ocular tissue that provides mechanical, sensory, and immune protection for the ocular surface. It is affected by many diseases through different pathological mechanisms. If a disease is not treated and conjunctival function is not fully restored, the whole ocular surface and, therefore, sight is at risk. Different therapeutic approaches have been proposed, but there are still unsolved conjunctival alterations that require more sophisticated therapeutic options. Advanced therapy medicinal products (ATMPs) comprise a wide range of products that includes cell therapy, tissue engineering, and gene therapy. To the best of our knowledge, there is no commercialized ATMP specifically for conjunctival treatment yet. However, the conjunctiva can be a potential target for ATMPs for different reasons. In this review, we provide an overview of the advances in experimental phases of potential ATMPs that primarily target the conjunctiva. Important advances have been achieved through the techniques of cell therapy and tissue engineering, whereas Citation: Diebold, Y.; García- the use of gene therapy in the conjunctiva is still marginal. Undoubtedly, future research in this field Posadas, L. Is the Conjunctiva a will lead to achieving commercially available ATMPs for the conjunctiva, which may provide better Potential Target for Advanced treatments for patients. Therapy Medicinal Products? Pharmaceutics 2021, 13, 1140. Keywords: advanced therapies; cell therapy; conjunctiva; ocular mucosa; gene therapy; tissue engi- https://doi.org/10.3390/ neering pharmaceutics13081140 Academic Editor: Monica M. Jablonski 1. Introduction The human conjunctiva is a complex and fascinating ocular tissue. Traditionally Received: 28 June 2021 neglected in favor of the cornea, its functions are essential in maintaining ocular surface Accepted: 23 July 2021 Published: 26 July 2021 homeostasis. Over the years, as our knowledge of tear film complexity and the patho- physiology of the ocular surface has increased, the conjunctiva has slowly come to be Publisher’s Note: MDPI stays neutral acknowledged as an essential protective element for ocular surface structures. MUC5AC, a with regard to jurisdictional claims in well-known mucin specifically secreted by the conjunctival goblet cells, as well as many published maps and institutional affil- other different secretory products, participates in the maintenance of the tear film [1,2]. iations. The conjunctiva is a mucosal tissue that extends from the mucocutaneous junction at the lid margin to the limbal region next to the peripheral cornea and rests on the sclera. In essence, the role of the conjunctiva is to protect the transparency of the cornea, a much more vulnerable tissue that lacks blood and lymphatic vessels, as well as a sufficiently strong in situ immune response for full protection from foreign invaders. Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. Due to its anatomical features and many roles, the conjunctiva is difficult to study This article is an open access article and model in the laboratory. We now know that conjunctival pathophysiology is complex distributed under the terms and and affects the homeostasis of the so-called lacrimal functional unit [3,4]. Conventional conditions of the Creative Commons pharmacological treatments are not sufficient or curative in many instances for recovering Attribution (CC BY) license (https:// a functional conjunctiva and/or maintaining healthy ocular surface tissues. creativecommons.org/licenses/by/ 4.0/). Pharmaceutics 2021, 13, 1140. https://doi.org/10.3390/pharmaceutics13081140 https://www.mdpi.com/journal/pharmaceutics Pharmaceutics 2021, 13, x 2 of 14 Pharmaceutics 2021, 13, 1140 2 of 13 The aim of this review is to present the challenges that the conjunctiva poses from The aim of this review is to present the challenges that the conjunctiva poses from clinical and therapeutic points of view and analyze the reported developments that may clinical and therapeutic points of view and analyze the reported developments that may become advanced therapies for conjunctival diseases in the future. become advanced therapies for conjunctival diseases in the future. 1.1.1.1. ConjunctivalConjunctival Structure Structure and and Functions Functions FromFrom anan anatomicalanatomical pointpoint ofof view,view, the the conjunctiva conjunctiva isis generallygenerally divisibledivisible intointo threethree mainmain regions: regions: (1) (1) the the tarsal, tarsal, or or palpebral, palpebral, which which lines lines the the inner inner surface surface of the of eyelids;the eyelids; (2) the (2) forniceal,the forniceal, which which lines lines the upper the upper and lowerand lower fornices; fornices; and (3)and the (3) bulbar,the bulbar, which which overlays overlays the sclerathe sclera on the on anterior the anterior portion portion of the globe.of the Theseglobe. three These regions three areregions specialized are specialized in different in functions,different functions, ranging from ranging trapping from trapping small foreign small foreign objects objects in a net in of a net secreted of secreted mucins mucins and facilitatingand facilitating their removaltheir removal by blinking by blinking to providing to providing immune immune protection protection to the cornea to the bycornea the localby the presence local presence of lymphoid of lymphoid tissue [5 tissue]. [5]. TheThe complexitycomplexity ofof thethe conjunctivaconjunctiva reliesrelies uponupon thethe multiplemultiple tissuestissues presentpresent inin itsits structure:structure: (1) (1) a non-keratinizeda non-keratinized stratified stratified squamous squamous epithelium epithelium that possesses that possesses five reported five epithelialreported cellepithelial subtypes, cell subtypes including, including goblet cells; goblet (2)a cells; basal (2) membrane, a basal membrane, where potential where autoantigenspotential autoantigens reside and, reside subsequently, and, subsequently, immune materialimmune becomesmaterial becomes deposited deposited in certain in autoimmunecertain autoimmune diseases diseases (e.g., mucous (e.g., mucous membrane membrane pemphigoid), pemp inhigoid), addition in addition to a loose to stroma a loose mainlystroma composed mainly composed of type IV of collagen; type IV (3)collagen; an abundant (3) an abundant vasculature; vasculature; (4) a regional (4) lymphoida regional tissue—namely,lymphoid tissue conjunctiva-associated—namely, conjunctiva lymphoid-associated tissue lymphoid (CALT) tissue and (CALT) lymphatic and vessels; lymphatic (5) avessels; melanocyte (5) a population;melanocyte and population; (6) sensory and afferent (6) sensory nerve fibersafferent derived nerve from fibers the derived ophthalmic from (inthe the ophthalmic bulbar and (in palpebral the bulbar areas) and and palpebral the maxillary areas) (in theand inferior the maxillary forniceal (in area) the branches inferior offorniceal the trigeminal area) branc nerve.hes In of addition, the trigeminal the conjunctiva nerve. In possessesaddition, thethe accessoryconjunctiva lacrimal possesses glands the ofaccessory Wolfring lacrimal and Kruse, glands which of areWolfring present and in theKruse, tarsal which conjunctiva are present and in in the the fornices, tarsal respectively,conjunctiva and in the the pseudoglands fornices, respectively, of Henle, whichand the are pseudoglands groups of abundant of Henle, goblet which cells are thatgroups also of appear abund inant the goblet tarsal cells plate. that also appear in the tarsal plate. AnAn amazingamazing varietyvariety ofof cellcell typestypes areare partpart ofof the the conjunctiva conjunctiva (Figure(Figure1 )1 and) and account account forfor itsits functionalfunctional complexity:complexity: mucin-secretingmucin-secreting epithelialepithelial cells,cells, fibroblasts,fibroblasts, melanocytes,melanocytes, dendriticdendritic cells, cells, lymphocytes, lymphocytes, eosinophils, eosinophils, neutrophils, neutrophils, and and mast mast cells, cells, not tonot mention to mention mes- enchymalmesenchymal stem cellsstem (MSCs). cells (MSCs). This illustrates This illustrates how difficult how it difficult has been it to has model been conjunctival to model tissueconjunctival in the laboratory tissue in the over laboratory the years. over the years. FigureFigure 1. 1.Tissue Tissue section section of of human human conjunctiva conjunctiva with with periodic periodicacid-Schiff acid-Schiff (PAS) (PAS) staining staining showing showing the the main cell types present in the epithelium and stroma. Magnification: 200×. main cell types present in the epithelium and stroma. Magnification: 200×. FromFrom a a functional functional point point of of view, view, the the conjunctiva conjunctiva realizes realizes the mechanical,the mechanical, sensory, sensory, and immuneand immune protection protection of the ocularof the surface; ocular thesurface; specialized the specialized secretion of secretion fluid, electrolytes, of fluid, andelectrolytes, diverse
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