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      Vitreous advanced glycation endproducts and α-dicarbonyls in retinal detachment patients with type 2 diabetes mellitus and non-diabetic controls

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          Abstract

          Purpose

          Advanced glycation endproducts (AGEs) and their precursors α-dicarbonyls are implicated in the progression of diabetic retinopathy. The purpose of this study was to assess AGEs and α-dicarbonyls in the vitreous of patients with type 2 diabetes mellitus (T2DM) with early stages or absence of diabetic retinopathy.

          Methods

          We examined vitreous samples obtained during vitrectomy from 31 T2DM patients presenting themselves with rhegmatogenous retinal detachment and compared these to 62 non-diabetic rhegmatogenous retinal detachment patients, matched on age, estimated glomerular filtration rate, smoking, intra-ocular lens implantation, and proliferative vitreoretinopathy. AGEs (pentosidine, N ε-(carboxymethyl)lysine, N ε-(carboxyethyl)lysine, and 5-hydro-5-methylimidazolone) and α-dicarbonyls (3-deoxyglucosone, methylglyoxal, and glyoxal) were measured by ultra performance liquid chromatography or high performance liquid chromatography. Skin autofluorescence was measured by the AGE Reader.

          Results

          Mean age was 64 ± 7.6 years for T2DM patients and 63 ± 8.1 years for controls. For T2DM patients, median diabetes duration was 2.2 (0.3–7.4) years. Non-proliferative diabetic retinopathy was present in 1 patient and classified as absent or background retinopathy in 30 patients. Vitreous levels of pentosidine (2.20 vs. 1.59 μmol/mol lysine, p = 0.012) and 3-deoxyglucosone (809 vs. 615 nmol/L, p = 0.001) were significantly elevated in T2DM patients compared to controls. Other AGEs and α-dicarbonyls in the vitreous were not significantly different. There was a trend for increased skin autofluorescence in T2DM patients as compared to controls (p = 0.07).

          Conclusions

          Pentosidine and 3-deoxyglucosone concentrations were increased in the vitreous of rhegmatogenous retinal detachment patients with a relatively short duration of diabetes compared to non-diabetic rhegmatogenous retinal detachment patients.

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          Most cited references41

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          Report of the Expert Committee on the Diagnosis and Classification of Diabetes Mellitus

          (2002)
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            Formation of glyoxal, methylglyoxal and 3-deoxyglucosone in the glycation of proteins by glucose.

            P Thornalley, A Langborg, H S Minhas (1999)
            The glycation of proteins by glucose has been linked to the development of diabetic complications and other diseases. Early glycation is thought to involve the reaction of glucose with N-terminal and lysyl side chain amino groups to form Schiff's base and fructosamine adducts. The formation of the alpha-oxoaldehydes, glyoxal, methylglyoxal and 3-deoxyglucosone, in early glycation was investigated. Glucose (50 mM) degraded slowly at pH 7.4 and 37 degrees C to form glyoxal, methylglyoxal and 3-deoxyglucosone throughout a 3-week incubation period. Addition of t-BOC-lysine and human serum albumin increased the rate of formation of alpha-oxoaldehydes - except glyoxal and methylglyoxal concentrations were low with albumin, as expected from the high reactivity of glyoxal and methylglyoxal with arginine residues. The degradation of fructosyl-lysine also formed glyoxal, methylglyoxal and 3-deoxyglucosone. alpha-Oxoaldehyde formation was dependent on the concentration of phosphate buffer and availability of trace metal ions. This suggests that alpha-oxoaldehydes were formed in early glycation from the degradation of glucose and Schiff's base adduct. Since alpha-oxoaldehydes are important precursors of advanced glycation adducts, these adducts may be formed from early and advanced glycation processes. Short periods of hyperglycaemia, as occur in impaired glucose tolerance, may be sufficient to increase the concentrations of alpha-oxoaldehydes in vivo.
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              AGE restriction in diabetes mellitus: a paradigm shift.

              Helen Vlassara, Gary Striker (2011)
              Persistently elevated oxidative stress and inflammation precede or occur during the development of type 1 or type 2 diabetes mellitus and precipitate devastating complications. Given the rapidly increasing incidence of diabetes mellitus and obesity in the space of a few decades, new genetic mutations are unlikely to be the cause, instead pointing to environmental initiators. A hallmark of contemporary culture is a preference for thermally processed foods, replete with pro-oxidant advanced glycation endproducts (AGEs). These molecules are appetite-increasing and, thus, efficient enhancers of overnutrition (which promotes obesity) and oxidant overload (which promotes inflammation). Studies of genetic and nongenetic animal models of diabetes mellitus suggest that suppression of host defenses, under sustained pressure from food-derived AGEs, may potentially shift homeostasis towards a higher basal level of oxidative stress, inflammation and injury of both insulin-producing and insulin-responsive cells. This sequence promotes both types of diabetes mellitus. Reducing basal oxidative stress by AGE restriction in mice, without energy or nutrient change, reinstates host defenses, alleviates inflammation, prevents diabetes mellitus, vascular and renal complications and extends normal lifespan. Studies in healthy humans and in those with diabetes mellitus show that consumption of high amounts of food-related AGEs is a determinant of insulin resistance and inflammation and that AGE restriction improves both. This Review focuses on AGEs as novel initiators of oxidative stress that precedes, rather than results from, diabetes mellitus. Therapeutic gains from AGE restriction constitute a paradigm shift.
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                Author and article information

                Contributors
                Andreas Wedrich: Role: Editor
                Journal
                Journal ID (nlm-ta): PLoS One
                Journal ID (iso-abbrev): PLoS ONE
                Journal ID (publisher-id): plos
                Journal ID (pmc): plosone
                Title: PLoS ONE
                Publisher: Public Library of Science (San Francisco, CA USA )
                ISSN (Electronic): 1932-6203
                Publication date (Electronic): 6 March 2017
                Publication date Collection: 2017
                Volume: 12
                Issue: 3
                Electronic Location Identifier: e0173379
                Affiliations
                [1 ]Department of Internal Medicine, University of Groningen, University Medical Center Groningen (UMCG), Groningen, the Netherlands
                [2 ]Research Institute GUIDE, Graduate School of Medical Sciences, University of Groningen, University Medical Center Groningen (UMCG), Groningen, the Netherlands
                [3 ]Department of Ophthalmology, University of Groningen, University Medical Center Groningen (UMCG), the Netherlands
                [4 ]Laboratory for Metabolism and Vascular Medicine, Maastricht University, Department of Experimental Internal Medicine, Maastricht, the Netherlands
                [5 ]W.J. Kolff Institute, Graduate School of Medical Sciences, University of Groningen, University Medical Center Groningen (UMCG), Groningen, the Netherlands
                Medizinische Universitat Graz, AUSTRIA
                Author notes

                Competing Interests: Prof. Dr. A.J. Smit is founder and shareholder of Diagnoptics Technologies BV (the Netherlands) which is the company that has developed the autofluorescence reader that was used in this study to assess skin accumulation of AGEs. This does not alter our adherence to PLOS ONE policies on sharing data and materials.

                • Conceptualization: BTF DJM CGS AJS LIL.

                • Data curation: BTF.

                • Formal analysis: BTF.

                • Funding acquisition: BTF LIL.

                • Investigation: BTF JLS.

                • Methodology: BTF DJM CGS JLS AJS LIL.

                • Project administration: BTF LIL.

                • Resources: CGS AJS LIL.

                • Supervision: AJS LIL.

                • Validation: BTF JLS.

                • Visualization: BTF.

                • Writing – original draft: BTF.

                • Writing – review & editing: DJM CGS JLS AJS LIL.

                Author information
                http://orcid.org/0000-0002-9275-7865
                Article
                Publisher ID: PONE-D-16-45919
                DOI: 10.1371/journal.pone.0173379
                PMC ID: 5338797
                PubMed ID: 28264049
                SO-VID: d6176828-d0a4-4c2e-bb00-5f68e682ecf9
                Copyright © © 2017 Fokkens et al
                License:

                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
                Date received : 18 November 2016
                Date accepted : 20 February 2017
                Page count
                Figures: 0, Tables: 2, Pages: 11
                Funding
                Funded by: Stichting Blindenhulp
                Award Recipient : Bernardina Teunisje Fokkens
                BTF was supported financially by Stichting Blindenhulp, The Netherlands ( http://www.blindenhulp.nl/). This organization had no role in the design or conduct of this research.
                Categories
                Subject: Research Article
                Subject: Medicine and Health Sciences
                Subject: Endocrinology
                Subject: Endocrine Disorders
                Subject: Diabetes Mellitus
                Subject: Medicine and Health Sciences
                Subject: Metabolic Disorders
                Subject: Diabetes Mellitus
                Subject: Medicine and Health Sciences
                Subject: Endocrinology
                Subject: Endocrine Disorders
                Subject: Diabetes Mellitus
                Subject: Type 2 Diabetes
                Subject: Medicine and Health Sciences
                Subject: Metabolic Disorders
                Subject: Diabetes Mellitus
                Subject: Type 2 Diabetes
                Subject: Physical Sciences
                Subject: Chemistry
                Subject: Chemical Compounds
                Subject: Organic Compounds
                Subject: Amino Acids
                Subject: Basic Amino Acids
                Subject: Lysine
                Subject: Physical Sciences
                Subject: Chemistry
                Subject: Organic Chemistry
                Subject: Organic Compounds
                Subject: Amino Acids
                Subject: Basic Amino Acids
                Subject: Lysine
                Subject: Biology and Life Sciences
                Subject: Biochemistry
                Subject: Proteins
                Subject: Amino Acids
                Subject: Basic Amino Acids
                Subject: Lysine
                Subject: Medicine and Health Sciences
                Subject: Ophthalmology
                Subject: Retinal Disorders
                Subject: Retinal Detachment
                Subject: Medicine and Health Sciences
                Subject: Ophthalmology
                Subject: Retinal Disorders
                Subject: Retinopathy
                Subject: Diabetic Retinopathy
                Subject: Medicine and health sciences
                Subject: Diagnostic medicine
                Subject: Diabetes diagnosis and management
                Subject: HbA1c
                Subject: Biology and life sciences
                Subject: Biochemistry
                Subject: Proteins
                Subject: Hemoglobin
                Subject: HbA1c
                Subject: Medicine and Health Sciences
                Subject: Surgical and Invasive Medical Procedures
                Subject: Ophthalmic Procedures
                Subject: Vitrectomy
                Subject: Biology and Life Sciences
                Subject: Biochemistry
                Subject: Proteins
                Subject: Post-Translational Modification
                Subject: Glycation
                Custom metadata
                Data Availability Data are available on the website of DataverseNL ( http://hdl.handle.net/10411/20841).

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                ScienceOpen disciplines: Uncategorized

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