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Photobiomodulation Mediates Neuroprotection against Retinal

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International Journal of Molecular Sciences Article Photobiomodulation Mediates Neuroprotection against Blue Light Induced Retinal Photoreceptor Degeneration Nora Heinig 1,*, Ulrike Schumann 1, Daniela Calzia 2, Isabella Panfoli 2 , Marius Ader 3, Mirko H. H. Schmidt 1,4,5 , Richard H. W. Funk 1 and Cora Roehlecke 1 1 2 3 4 5 Received: 21 February 2020; Accepted: 27 March 2020; Published: 30 March 2020 Institute of Anatomy, Medical Faculty Carl Gustav Carus, Technische Universität (TU) Dresden, School of Medicine, Dresden 01307, Germany; ulrike.schumann@tu-dresden.de (U.S.); mhhs@mailbox.tu-dresden.de (M.H.H.S.); richard.funk@tu-dresden.de (R.H.W.F.); cora.roehlecke@tu-dresden.de (C.R.) Department of Pharmacy-DIFAR, Biochemistry and Physiology Lab., University of Genoa, Genova 16132, Italy; dcalzia@gmail.com (D.C.); panfoli@difar.unige.it (I.P.) Center for Regenerative Therapies Dresden (CRTD), TU Dresden, Dresden 01307, Germany; marius.ader@tu-dresden.de German Cancer Consortium (DKTK), Partner Site Dresden 01309, Germany German Cancer Research center (DKFZ), Heidelberg 69120, Germany * Correspondence: nora.heinig@tu-dresden.de Abstract: Potent neuroprotective effects of photobiomodulation with 670 nm red light (RL) have been demonstrated in several models of retinal disease. RL improves mitochondrial metabolism, reduces retinal inflammation and oxidative cell stress, showing its ability to enhance visual function. However, the current knowledge is limited to the main hypothesis that the respiratory chain complex IV, cytochrome c oxidase, serves as the primary target of RL. Here, we demonstrate a comprehensive cellular, molecular, and functional characterization of neuroprotective effects of 670 nm RL and 810 nm near-infrared light (NIRL) on blue light damaged murine primary photoreceptors. We show that respiratory chain complexes I and II are additional PBM targets, besides complex IV, leading to enhanced mitochondrial energy metabolism. Accordingly, our study identified mitochondria related RL- and NIRL-triggered defense mechanisms promoting photoreceptor neuroprotection. The observed improvement of mitochondrial and extramitochondrial respiration in both inner and outer segments is linked with reduced oxidative stress including its cellular consequences and reduced mitochondria-induced apoptosis. Analysis of regulatory mechanisms using gene expression analysis identified upregulation α-crystallins that indicate enhanced production of proteins with protective functions that point to the rescued mitochondrial function. The results support the hypothesis that energy metabolism is a major target for retinal light therapy. Keywords: low-level laser therapy; red light; near-infrared light; photoreceptor survival; respiratory chain complexes; oxidative stress; α-Crystallins; neuroprotection 1. Introduction Stimulation with far red light (RL) to near-infrared light (NIRL) in a range of 600–1000 nm with low intensities, called photobiomodulation (PBM), is described as a possible non-invasive strategy for additive therapy in retinal disorders. It has been used over many years for a range of clinical applications, including chiropractic, dental and dermatologic disorders and central nervous system injury [1]. A range of applications have shown beneficial effects in tissue injury, for example wound healing [2,3] improved 􏰁􏰂􏰃 􏰅􏰆􏰇 􏰈􏰉􏰊􏰋􏰌􏰂􏰍 Int. J. Mol. Sci. 2020, 21, 2370; doi:10.3390/ijms21072370 www.mdpi.com/journal/ijms

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