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      Cytokine profiles in the aqueous humor and serum of patients with dry and treated wet age-related macular degeneration

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          Abstract

          Purpose

          To identify disease-specific cytokine profile differences in the aqueous humor (AH) (other than the vascular endothelial growth factor) between patients with dry and treated wet age-related macular degeneration (AMD) and healthy controls.

          Methods

          This retrospective study drew on a case-series of patients diagnosed with dry AMD ( n = 25) and treated wet AMD ( n = 19), as well as on healthy controls (no systemic therapy; n = 20) undergoing phacoemulsification or vitrectomy. Samples of AH and serum were collected in parallel at the beginning of surgery. The levels of 43 cytokines were simultaneously determined using the Bio-Plex® multiplex beads system. Differences between the three groups were statistically compared using the Kruskal-Wallis H-Test after applying the Bonferroni correction for multiple comparisons ( p<0.0012).

          Results

          The concentrations of three cytokines were elevated in the AH of patients with dry AMD (CXCL6; p = 0.00067) and treated wet AMD (CXCL5, CXCL6, MIG/XCXL; all p<0.001) relative to those in the healthy controls. No other differences between the three groups were identified. The AH levels of seven cytokines (16%), including CXCL6, ranged below the lower limit of quantitation of the assay. Without the correction for multiple comparisons ( p<0.05), the levels of 31 of the 43 cytokines in the AH of patients with AMD would have differed significantly from those in the control. The systemic cytokine profiles (serum) were similar in all three groups.

          Conclusions

          No systematic differences in the AH cytokine environment were identified between patients with dry AMD and those with treated wet AMD. This finding might indicate that AMD is either the result of a persistent imbalance in the physiological tissue milieu, or that the localized process induces no significant change in the cytokine environment of the anterior ocular segment.

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          Most cited references51

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          Inflammaging and Anti-Inflammaging: The Role of Cytokines in Extreme Longevity.

          Longevity and aging are two sides of the same coin, as they both derive from the interaction between genetic and environmental factors. Aging is a complex, dynamic biological process characterized by continuous remodeling. One of the most recent theories on aging focuses on immune response, and takes into consideration the activation of subclinical, chronic low-grade inflammation which occurs with aging, named "inflammaging". Long-lived people, especially centenarians, seem to cope with chronic subclinical inflammation through an anti-inflammatory response, called therefore "anti-inflammaging". In the present review, we have focused our attention on the contrast between inflammaging and anti-inflammaging systems, by evaluating the role of cytokines and their impact on extreme longevity. Cytokines are the expression of a network involving genes, polymorphisms and environment, and are involved both in inflammation and anti-inflammation. We have described the role of IL-1, IL-2, IL-6, IL-12, IL-15, IL-18, IL-22, IL-23, TNF-α, IFN-γ as pro-inflammatory cytokines, of IL-1Ra, IL-4, IL-10, TGF-β1 as anti-inflammatory cytokines, and of lipoxin A4 and heat shock proteins as mediators of cytokines. We believe that if inflammaging is a key to understand aging, anti-inflammaging may be one of the secrets of longevity.
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            Inflammaging decreases adaptive and innate immune responses in mice and humans.

            Both the innate and adaptive immune systems decline with age, causing greater susceptibility to infectious diseases and reduced responses to vaccination. Diseases are more severe in elderly than in young individuals and have a greater impact on health outcomes such as morbidity, disability and mortality. Aging is characterized by increased low-grade chronic inflammation, called "inflammaging", measured by circulating levels of TNF-α, IL-6 and CRP, as well as by latent infections with viruses such as cytomegalovirus. Inflammaging has received considerable attention because it proposes a link between changes in immune cells and a number of diseases and syndromes typical of old age. In this review we aim at summarizing the current knowledge on pathways contributing to inflammaging, on immune responses down-regulated by inflammation and mechanisms proposed. The defects in the immune response of elderly individuals presented in this review should help to discover avenues for effective intervention to promote healthy aging.
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              Anti-inflammatory cytokines.

              The anti-inflammatory cytokines are a series of immunoregulatory molecules that control the proinflammatory cytokine response. Cytokines act in concert with specific cytokine inhibitors and soluble cytokine receptors to regulate the human immune response. Their physiologic role in inflammation and pathologic role in systemic inflammatory states are increasingly recognized. Major anti-inflammatory cytokines include interleukin (IL)-1 receptor antagonist, IL-4, IL-6, IL-10, IL-11, and IL-13. Specific cytokine receptors for IL-1, tumor necrosis factor-alpha, and IL-18 also function as proinflammatory cytokine inhibitors. The nature of anti-inflammatory cytokines and soluble cytokine receptors is the focus of this review. The current and future therapeutic uses of these anti-inflammatory cytokines are also reviewed.
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                Author and article information

                Contributors
                Role: Data curationRole: Formal analysisRole: VisualizationRole: Writing – original draft
                Role: Data curationRole: Formal analysisRole: MethodologyRole: SupervisionRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: SoftwareRole: Visualization
                Role: Data curationRole: Formal analysisRole: Visualization
                Role: ConceptualizationRole: Data curationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                29 August 2018
                2018
                : 13
                : 8
                : e0203337
                Affiliations
                [1 ] Swiss Eye Institute and Berner Augenklinik am Lindenhofspital, Bern, Switzerland
                [2 ] University of Bern, Bern, Switzerland
                University of Tennessee Health Science Center, UNITED STATES
                Author notes

                Competing Interests: The authors have the following interests: JGG acts as an advisor for several pharmaceutical companies (Novartis, Bayer, Allergan, Alcon, AbbVie) and contributes to a number of industry-sponsored international multicenter studies. There are no patents, products in development or marketed products to declare. This does not alter our adherence to all the PLOS ONE policies on sharing data and materials.

                Author information
                http://orcid.org/0000-0001-8752-8390
                Article
                PONE-D-18-16178
                10.1371/journal.pone.0203337
                6114931
                30157273
                3aa5378d-8425-4c84-bed4-bbc093a4b25b
                © 2018 Spindler et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 4 June 2018
                : 17 August 2018
                Page count
                Figures: 2, Tables: 5, Pages: 17
                Funding
                The manuscript was partially funded by a grant from the Scientific Funds of the Lindenhof Foundation without commercial interests. There was no additional external funding received for this study. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Physiology
                Immune Physiology
                Cytokines
                Medicine and Health Sciences
                Physiology
                Immune Physiology
                Cytokines
                Biology and Life Sciences
                Immunology
                Immune System
                Innate Immune System
                Cytokines
                Medicine and Health Sciences
                Immunology
                Immune System
                Innate Immune System
                Cytokines
                Biology and Life Sciences
                Developmental Biology
                Molecular Development
                Cytokines
                Medicine and Health Sciences
                Geriatrics
                Geriatric Ophthalmology
                Macular Degeneration
                Medicine and Health Sciences
                Ophthalmology
                Geriatric Ophthalmology
                Macular Degeneration
                Medicine and Health Sciences
                Ophthalmology
                Retinal Disorders
                Macular Disorders
                Macular Degeneration
                Medicine and Health Sciences
                Ophthalmology
                Retinal Disorders
                Retinal Degeneration
                Macular Degeneration
                Biology and Life Sciences
                Anatomy
                Head
                Eyes
                Medicine and Health Sciences
                Anatomy
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                Biology and Life Sciences
                Anatomy
                Ocular System
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                Medicine and Health Sciences
                Anatomy
                Ocular System
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                Medicine and Health Sciences
                Inflammatory Diseases
                Biology and Life Sciences
                Immunology
                Immune Response
                Inflammation
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                Immune Response
                Inflammation
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                Diagnostic Medicine
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                Pathology and Laboratory Medicine
                Signs and Symptoms
                Inflammation
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogenesis
                Biology and Life Sciences
                Cell Biology
                Cell Motility
                Chemotaxis
                Chemokines
                Medicine and Health Sciences
                Ophthalmology
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