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      Expression of Inducible Heat Shock Proteins Hsp27 and Hsp70 in the Visual Pathway of Rats Subjected to Various Models of Retinal Ganglion Cell Injury

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      Author(s): 1 , 2 , * , 1 , 2 , 1 , 2
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      Journal: PLoS ONE
      Publisher: Public Library of Science

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          Abstract

          Inducible heat shock proteins (Hsps) are upregulated in the central nervous system in response to a wide variety of injuries. Surprisingly, however, no coherent picture has emerged regarding the magnitude, duration and cellular distribution of inducible Hsps in the visual system following injury to retinal ganglion cells (RGCs). The current study sought, therefore, to achieve the following two objectives. The first aim of this study was to systematically characterise the patterns of Hsp27 and −70 expression in the retina and optic nerve in four discrete models of retinal ganglion cell (RGC) degeneration: axonal injury (ON crush), somato-dendritic injury (NMDA-induced excitotoxicity), chronic hypoperfusion (bilateral occlusion of the carotid arteris) and experimental glaucoma. The second aim was to document Hsp27 and −70 expression in the optic tract, the subcortical retinorecipient areas of the brain, and the visual cortex during Wallerian degeneration of RGC axons. Hsp27 was robustly upregulated in the retina in each injury paradigm, with the chronic models, 2VO and experimental glaucoma, displaying a more persistent Hsp27 transcriptional response than the acute models. Hsp27 expression was always associated with astrocytes and with a subset of RGCs in each of the models excluding NMDA. Hsp27 was present within astrocytes of the optic nerve/optic tract in control rats. During Wallerian degeneration, Hsp27 was upregulated in the optic nerve/optic tract and expressed de novo by astrocytes in the lateral geniculate nucleus and the stratum opticum of the superior colliculus. Conversely, the results of our study indicate Hsp70 was minimally induced in any of the models of injury, either in the retina, or in the optic nerve/optic tract, or in the subcortical, retinorecipient areas of the brain. The findings of the present study augment our understanding of the involvement of Hsp27 and Hsp70 in the response of the visual system to RGC degeneration.

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          Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology.

          M. FEDER, G. E. Hofmann (1999)
          Molecular chaperones, including the heat-shock proteins (Hsps), are a ubiquitous feature of cells in which these proteins cope with stress-induced denaturation of other proteins. Hsps have received the most attention in model organisms undergoing experimental stress in the laboratory, and the function of Hsps at the molecular and cellular level is becoming well understood in this context. A complementary focus is now emerging on the Hsps of both model and nonmodel organisms undergoing stress in nature, on the roles of Hsps in the stress physiology of whole multicellular eukaryotes and the tissues and organs they comprise, and on the ecological and evolutionary correlates of variation in Hsps and the genes that encode them. This focus discloses that (a) expression of Hsps can occur in nature, (b) all species have hsp genes but they vary in the patterns of their expression, (c) Hsp expression can be correlated with resistance to stress, and (d) species' thresholds for Hsp expression are correlated with levels of stress that they naturally undergo. These conclusions are now well established and may require little additional confirmation; many significant questions remain unanswered concerning both the mechanisms of Hsp-mediated stress tolerance at the organismal level and the evolutionary mechanisms that have diversified the hsp genes.
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            Distal axonopathy with structural persistence in glaucomatous neurodegeneration.

            Denise M. Inman, P Horner, Rebecca Sappington … (2010)
            An early hallmark of neuronal degeneration is distal transport loss and axon pathology. Glaucoma involves the degeneration of retinal ganglion cell (RGC) neurons and their axons in the optic nerve. Here we show that, like other neurodegenerations, distal axon injury appears early in mouse glaucoma. Where RGC axons terminate in the superior colliculus, reduction of active transport follows a retinotopic pattern resembling glaucomatous vision loss. Like glaucoma, susceptibility to transport deficits increases with age and is not necessarily associated with elevated ocular pressure. Transport deficits progress distal-to-proximal, appearing in the colliculus first followed by more proximal secondary targets and then the optic tract. Transport persists through the optic nerve head before finally failing in the retina. Although axon degeneration also progresses distal-to-proximal, myelinated RGC axons and their presynaptic terminals persist in the colliculus well after transport fails. Thus, distal transport loss is predegenerative and may represent a therapeutic target.
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              Microglial activation in the visual pathway in experimental glaucoma: spatiotemporal characterization and correlation with axonal injury.

              J. Wood, Andreas Ebneter, Robert J. Casson … (2010)
              Glia are the main cellular CNS elements initiating defense mechanisms against destructive influences and promoting regenerative processes. The aim of the current work was to characterize the microglial response within the visual pathway in a rat model of experimental glaucoma and to correlate the microglial response with the severity of axonal degeneration. Experimental glaucoma was induced in each right eye of adult Sprague-Dawley rats by translimbal laser photocoagulation of the trabecular meshwork. Rats were subsequently killed at various times from 3 days to 6 weeks. Tissue sections were obtained from globes, optic nerves, chiasmata, and optic tracts for immunohistochemistry and toluidine blue staining. This model of experimental glaucoma led to a marked activation of microglia in the retina, optic nerve, and tract. Indeed, microglial activity remained elevated, even after intraocular pressure returned to basal levels. It is postulated that this process accompanies ongoing axonal degeneration. The degree of activation in the optic nerve correlated with axonal damage. Activation was characterized by increased density and morphologic changes. Both major histocompatibility complex (MHC) class I and MHC class II surface proteins were persistently upregulated in optic nerves and localized to microglial cells; however, this did not correlate with any significant T-cell infiltration. Interestingly, MHC class II expression was not detected in the retina. The present data may have implications for the study of the pathology associated with the visual pathway in diseases such as glaucoma.
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                Author and article information

                Contributors
                Marta Agudo-Barriuso: 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, USA )
                ISSN (Electronic): 1932-6203
                Publication date Collection: 2014
                Publication date (Electronic): 23 December 2014
                Volume: 9
                Issue: 12
                Electronic Location Identifier: e114838
                Affiliations
                [1 ]Ophthalmic Research Laboratories, South Australian Institute of Ophthalmology, Hanson Institute Centre for Neurological Diseases, Frome Road, Adelaide SA-5000, Australia
                [2 ]Department of Ophthalmology and Visual Sciences, University of Adelaide, Frome Road, Adelaide SA-5000, Australia
                Instituto Murciano de Investigación Biosanitaria-Virgen de la Arrixaca, Spain
                Author notes

                Competing Interests: The authors confirm that co-author Glyn Chidlow is a PLOS ONE Editorial Board member. This confirmation does not alter the authors' adherence to PLOS ONE Editorial policies and criteria.

                Conceived and designed the experiments: GC. Performed the experiments: GC JW. Analyzed the data: GC JW RC. Contributed reagents/materials/analysis tools: RC. Wrote the paper: GC JW RC.

                Article
                Publisher ID: PONE-D-14-41049
                DOI: 10.1371/journal.pone.0114838
                PMC ID: 4275305
                PubMed ID: 25535743
                SO-VID: ace8e849-728e-4e84-ab81-0123b8fb7e02
                Copyright statement: Copyright @ 2014
                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 : 14 September 2014
                Date accepted : 14 November 2014
                Page count
                Pages: 26
                Funding
                Support from the National Health and Medical Research Council (project grant: APP1050982) and the Ophthalmic Research Institute of Ophthalmology is gratefully acknowledged. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Subject: Research Article
                Subject: Biology and Life Sciences
                Subject: Anatomy
                Subject: Brain
                Subject: Superior Colliculus
                Subject: Ocular System
                Subject: Optic Nerve
                Subject: Cell Biology
                Subject: Cellular Types
                Subject: Animal Cells
                Subject: Neurons
                Subject: Afferent Neurons
                Subject: Retinal Ganglion Cells
                Subject: Ganglion Cells
                Subject: Neuroscience
                Subject: Sensory Systems
                Subject: Visual System
                Subject: Medicine and Health Sciences
                Subject: Ophthalmology
                Subject: Eye Diseases
                Subject: Glaucoma
                Subject: Research and analysis methods
                Subject: Histochemistry and cytochemistry techniques
                Subject: Immunohistochemistry techniques
                Subject: Streptavidin-Biotin immunohistochemistry
                Custom metadata
                Data Availability The authors confirm that all data underlying the findings are fully available without restriction. All relevant data are within the paper and its Supporting Information files.

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                ScienceOpen disciplines: Uncategorized

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