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The Vitreous Ecosystem in Diabetic Retinopathy: Insight Into the Patho-Mechanisms of Disease

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The Vitreous Ecosystem in Diabetic Retinopathy: Insight Into the Patho-Mechanisms of Disease International Journal of Molecular Sciences Review The Vitreous Ecosystem in Diabetic Retinopathy: Insight into the Patho-Mechanisms of Disease Siva S.R. Iyer * , Mollie K. Lagrew, Stephanie M. Tillit , Ramak Roohipourmoallai and Samuel Korntner Department of Ophthalmology, University of Florida College of Medicine, 1600 SW Archer Road, Gainesville, FL 32610, USA; mollie.mansfield@ufl.edu (M.K.L.); [email protected] (S.M.T.); [email protected] (R.R.); korntner@ufl.edu (S.K.) * Correspondence: ssr@ufl.edu Abstract: Diabetic retinopathy is one of the leading causes of blindness in the world with the incidence of disease ever-increasing worldwide. The vitreous humor represents an extensive and complex interactive arena for cytokines in the diabetic eye. In recent decades, there has been significant progress in understanding this environment and its implications in disease pathophysiology. In this review, we investigate the vitreous ecosystem in diabetic retinopathy at the molecular level. Areas of concentration include: the current level of knowledge of growth factors, cytokine and chemokine mediators, and lipid-derived metabolites in the vitreous. We discuss the molecular patho-mechanisms of diabetic retinopathy based upon current vitreous research. Keywords: vitreous; diabetes; retinopathy; cytokine; interleukin; eicosanoid Citation: Iyer, S.S.R.; Lagrew, M.K.; Tillit, S.M.; Roohipourmoallai, R.; 1. Introduction Korntner, S. The Vitreous Ecosystem Diabetic retinopathy (DR) is a leading cause of blindness in the developed world [1]. in Diabetic Retinopathy: Insight into The worldwide DR prevalence among individuals with diabetes is as high as 34.6%. It the Patho-Mechanisms of Disease. Int. is estimated that DR affected approximately 93 million individuals globally in 2010. Fur- J. Mol. Sci. 2021, 22, 7142. https:// thermore, because the prevalence of diabetes mellitus is growing, particularly in low- doi.org/10.3390/ijms22137142 and middle-income countries, it is expected that the incidence of DR will increase in the future [1]. Among individuals with diabetes, the annual incidence of DR ranges from Academic Editor: Stephanie about 2.2% to 12.7% depending on geographic region [2]. The prevalence of DR and its C. Joachim subsequent sequela is substantially higher in individuals with type 1 diabetes, increased diabetes duration, poor glucose control, and other comorbidities such as high blood pres- Received: 12 May 2021 sure or high cholesterol [1]. Proliferative diabetic retinopathy (PDR) with complications Accepted: 14 June 2021 such as vitreous hemorrhage and tractional retinal detachment (TRD) represents the most Published: 1 July 2021 advanced stage of DR [3]. The vitreous is a near acellular and avascular body composed of 97–99% water [4,5]. Publisher’s Note: MDPI stays neutral Over 70% of the collagen in the vitreous is type II [5]. Hyaluronan (HA) is the major with regard to jurisdictional claims in published maps and institutional affil- glycosaminoglycan (GAG) in the human vitreous [5]. As one might expect, the molecular iations. make-up of the animal vitreous is not equivalent to the human vitreous. The components of the vitreous humor are not uniform or pattern-driven, even among animal species, and there are differences in concentrations of electrolytes, and GAGs [6]. For example, chondroitin sulfate is the predominant GAG in chicks rather than hyalauronin [7]. The vitreous cortex is identifiable in youthful vitreous gel, and with age, liquefaction of the Copyright: © 2021 by the authors. vitreous body occurs [8,9]. Liquefaction occurs earlier in the diabetic eye [8]. However, the Licensee MDPI, Basel, Switzerland. delay of complete posterior vitreous detachment sets the stage for structural damage to the This article is an open access article distributed under the terms and retina as proliferative retinal disease progresses. conditions of the Creative Commons The vitreous molecular ecosystem in the diabetic eye is generally reflective of retinal Attribution (CC BY) license (https:// disease and is an emerging science. Most of the literature currently available on molecular creativecommons.org/licenses/by/ vitreous mediators in the human vitreous has been from the study of eyes with PDR. This 4.0/). is understandable as non-proliferative diabetic eyes undergo surgical intervention less Int. J. Mol. Sci. 2021, 22, 7142. https://doi.org/10.3390/ijms22137142 https://www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2021, 22, 7142 2 of 29 often. Molecular study of the vitreous may seem a recondite science, but the importance of vitreous molecular constituents cannot be overstated because it helps us understand disease pathogenesis and processes. The vitreoretinal interface and micro-environment represent an intimate and complex relationship. In this review, we explore the current knowledge on vitreous mediators in DR and discuss their characteristics and known dynamics. 2. Challenges to the Study of the Vitreous 2.1. Approaches The study of the vitreous structure is difficult because its ultrastructure can be altered with processing, leading to the introduction of artifacts. For example, the early assertion of chondroitin sulfate’s role in glycosaminoglycan (GAG)–GAG interactions with collagen crosslinking may have been due, in part, to artifactual findings [4,10]. Many types of techniques have been used to study the vitreous including whole dissections [9,11], electron microscopy with rotary shadowing [7], dark-field illumination [9,12], spectroscopy [13], and digestion by proteinases, to name a few [4,6,7,9,10,14]. Early gross human anatomical studies were that of cadaveric eyes [9], but the study of the molecular science of the vitreous cannot be conducted in this manner if the study is to reflect active and ongoing disease. Most molecular studies are conducted after a vitreous sample is obtained [13]. Un- targeted, proteomic-based approaches such as liquid chromatography tandem mass spec- troscopy (LC-MS/MS) can provide the sensitivity and specificity needed to objectively analyze the vitreous [15]. For targeted analysis, enzyme-linked immunosorbent assay (ELISA) by far has been the most common way to detect and analyze vitreous cytokines, having replaced radioimmunoassay [16], but in the early 2000s, multiplex methods arrived which were more cost-effective as well as efficient in measuring multiple mediators simul- taneously [17–19]. Methods using multiplex technology that enhance reproducibility and detect proteins in lower concentrations such as electrochemiluminescent (ECL) sandwich immunoassay and proximity extension assay (PEA) are now widely available [20]. These techniques allow many proteins to be analyzed simultaneously with as small as 1 µL of volume [20]. As human samples are taken from a small volume and generally require aseptic ocular surface conditions, they are most safely obtained in controlled clinical and surgical settings. Non-invasive techniques to study the vitreous from patients such as from vitreous reflux after intravitreal treatment have been recently described [17]. The majority of all vitreous samplings for molecular studies, however, are conducted in the surgical suite. The vitreous has to be removed without damage to the retina or other eye structures [21] and has to be cooled and stored immediately (usually on dry ice), transported appropriately, and then stored again (usually in the −30 to −80 C range) until analysis can be conducted [22]. Many vitreoretinal operations at academic centers are performed after hours and are often unscheduled. Therefore, it follows that from a technical and logistical standpoint, vitreous sampling has to be planned and performed meticulously. Infusion fluid dynamics prior to sampling and pre-treatment with a variety of intravitreal therapies can alter the natural state of the vitreous [3]. In addition, the sample obtained from one area in the vitreous may not represent the molecular environment in another area [23]. Herein, we describe our sampling technique for pure undiluted human vitreous in the surgical suite. 2.2. Human Vitreous Sampling Technique Pure vitreous removal for the purposes of study should be conducted after institu- tional review board approval has been established and informed consent has been obtained. The vitreous can safely be removed under direct visibility with immediate access to in- traocular pressure adjustment to avoid lens damage (posterior collapse), hemorrhage, and suprachoroidal fluid accumulation as the eye is decompressed. The vitreous cutter (27 gauge, 25 gauge, or 23 gauge) after priming (to remove fluid from the tubing) is a functional tool using aspiration and, in some instances, high cut rates (≥7500 cuts per minute) to obtain the sample with connection to a 1 mL tuberculin syringe handled by Int. J. Mol. Sci. 2021, 22, 7142 3 of 29 an assistant. The cutter can be maneuvered (with a careful cutter aperture orientation) to obtain a mid-vitreous sample or moved to different areas with care. In the case of a TRD, awareness of the location of the posterior cortex (sometimes very anterior in the mid-periphery) is important as cortical incision may result in unintended retro-cortical sampling. Using the technique above, approximately 1 mL of sample in most cases can be obtained from the human eye safely prior to significant decompression. Simultaneous air exchange to maintain eye volume while the sample is being removed may be more favorable in high-risk cases and in cases of pre-incisional hypotony. 2.3. Interpretation
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