Single and repeated low-dose UVB radiation exposures affect the visual system

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Abstract

The visual system is an important biological indicator of effects induced by ultraviolet (UV) radiation. However, research has extensively investigated the effects of high-dose UV radiation in a single exposure, thus, the differential of this work was to investigate the effects of UVB radiation in low doses in single and repeated exposure. Therefore, we investigated the effects of repeated exposure to environmental UVB doses (0.09 J/cm2) on the retina and optic lobes of the crab Neohelice granulata. We evaluated the reactive oxygen species (ROS) concentration, antioxidant capacity against peroxyl radicals (ACAP) levels, catalase (CAT) and glutathione S-transferase (GST) activities and lipoperoxidation (LPO) levels and performed histological analysis. The crabs were exposed to UVB radiation for 1 or 60 days, while the control group was exposed to visible light. In the retina region, increases in ROS concentration and CAT and GST activities after the single exposure were observed. After 60 days of exposure, we observed an increase in ACAP levels. In the optic lobes, we observed an increase in GST activity and a decrease in LPO levels after the single exposure. However, we observed an increase in ROS concentration after 60 days of exposure. Moreover, after 60 days of exposure, infiltrating hemocytes in the retina and disorganization in neuron cell bodies of the external medulla were observed. In this sense, single and repeated exposure to low doses of UVB radiation induced changes in oxidative status and inflammatory process in the visual system of the crab Neohelice granulata.

Introduction

The characteristics of any region of the electromagnetic spectrum vary according to the wavelength [1]. Therefore, considering the possible biological effects, such as the capacity to damage the varied cellular components, ultraviolet (UV) radiation is subdivided into three different bands: UVA (315–400 nm), UVB (280–315 nm) and UVC (100–280 nm). The UV radiation that reaches the Earth's surface is attenuated after interacting with the different atmospheric components. Among these, ozone (O3) is responsible for absorbing most of the incident UV radiation. Moreover, this attenuation is directly related to the kind of radiation, as it is more intense at a shorter wavelength [2]. Therefore, the range comprised of UVB and UVC radiation is heavily absorbed, whereas UVA radiation, which is virtually not absorbed, represents about 95% of the UV radiation that reaches the earth's surface [3].

Anthropogenic activity has progressively depleted the stratospheric ozone, resulting in what is known as a “hole in the ozone layer”, through the production of toxic compounds released into the environment [2]. Due to the depletion of ozone, there is a consequent marked increase in the incidence of UV radiation on the Earth's surface, especially UVB radiation [3]. Hence, this may have important influences on biological processes [4], being able to provoke serious damage to biodiversity.

Furthermore, UV radiation has mainly targeted the animal's body surface and eyes. In the eyes, ROS generation triggered by exposure to UV radiation has been implicated in the pathogenesis of various diseases [5]. In addition, exposure to UV radiation, with stronger evidence of a specific effect of UVB radiation, increases the risk of development of various ocular conditions, such as photokeratitis, pterygium, and cataracts [6]. However, this knowledge is more restricted to mammals. In this sense, studies that have approached the action of UV radiation, have observed cellular and morphological damage. Besides, to that exposure to UV radiation, can trigger an increase in the generation of reactive oxygen species (ROS), affecting several biomolecules, making them highly vulnerable to oxidative damage [5]. However, enzymatic and non-enzymatic mechanisms can act defend against the possible damage triggered by ROS [7].

Miguel and co-workers [8], verified that the retina of rats exposed to UV radiation (UVB and UVC) showed significant changes in the nucleus and cytoplasmic organelles. Also, another type of damage very characteristic of exposure of the visual system to UV radiation is cell death [9]. Although the characterization of UV damage has been investigated in vertebrates, few works have addressed this subject in invertebrates.

Miguel and co-workers [10] showed that retinal and lamina ganglionaris cells from the crab Ucides cordatus presented nuclear (karyolysis and increased chromatin condensation) and organellar (distension of the rough endoplasmic reticulum and mitochondrial rupture) damage as a function of exposure to UVB and UVC radiation. Vargas and co-workers [11], working with acute exposure to UVA and UVB radiation in the crab Neohelice granulata, observed alterations in the oxidative status in the visual system of this animal. Besides, Hollmann and co-workers [12], exposing U. cordatus to UVA, UVB and a solar simulator at 1, 3 and 5 day intervals, observed changes in antioxidant activity during the first day of exposure.

The crab N. granulata is a semi-terrestrial species of the southern coast of Brazil, Uruguay and Argentina, which is exposed to UV radiation during its life cycle. This decapod crustacean has an important ecological role in the saltmarsh regions, influencing different physicochemical and biological aspects of these ecosystems [13]. In this sense, because of its semi-terrestrial habit, N. granulata has been used as a model for studies on the effects of UV radiation [11,[14], [15], [16], [17]].

The visual system is an important biological indicator of effects induced by UV radiation. However, research has extensively investigated the effects of high-dose UV radiation in a single exposure, thus, the differential of this work was to investigate the effects of UVB radiation in low doses in single and repeated exposures. In this sense, the aim of the present study was to evaluate the effects of low-dose in a single and repeated exposures of UVB radiation on the antioxidant defense system as well as to assess morphological changes in the visual system of the crab N. granulata.

Section snippets

Animal Collection and Laboratory Maintenance

Adult male crabs of N. granulata (10.8 ± 1.8 g) were collected in salt marshes around Rio Grande/RS, Brazil and transported to the laboratory at the Universidade Federal do Rio Grande - FURG. The animals were maintained for 10 days in tanks with a biological filter and constant water circulation, with a photoperiod of 12 L:12D, under fluorescent lamps (Philips TLT 40 W/75, São Paulo, Brazil), irradiated with 96.0 mW/cm2 of visible light, at a temperature of 20 °C and salinity of 20. The animals

Results

The results obtained are represented in the raw data in table A. The control group of the retina (Table 1A) and optic lobe (Table 1B), showed different values for ROS concentration, ACAP levels, CAT activity, GST activity and LPO levels for 1 or 60 days.

Discussion

UVB radiation is an important environmental stressor, concerning aquatic ecosystems, that might alter the growth, behavior and survival of organisms living in coastal areas [[23], [24], [25], [26], [27]]. Among the most different physiological systems, the visual system is constantly vulnerable to harmful effects caused by UV radiation, increasing the risk of ocular disorders [28]. Acting as an exogenous source of ROS generation, the UVB radiation contributes to oxidative damage in ocular

Conclusion

Based on our results, we conclude that single and repeated exposures to UVB radiation at environmental doses can affect the visual system of the crab N. granulata. Our data indicate a change in the oxidative parameters evaluated, such as the increase in reactive species, and in the total antioxidant capacity against peroxyl radicals. In addition, our results show a pronounced inflammatory process in the peduncle of the crab N. granulata, thus being able to trigger structural alterations in the

Credit Author Statement

Valmor Vinicius Araujo Vaz: Graduated in Biological Sciences and Master in Physiological Sciences at the Universidade Federal do Rio Grande. He is currently a doctoral candidate at the Graduate Program in Physiological Sciences at the Universidade Federal do Rio Grande.

Leandra da Silva Jardim: Graduated in Biological Sciences at the Universidade Federal do Rio Grande.

Márcio Alberto Geihs: Graduated in Oceanology from Universidade Federal do Rio Grande and Degree in Biological Sciences from

Author Statement

Valmor Vinicius Araujo Vaz: Contextualization, Development of methodologies and analyses made, Discussion of results, Investigation, Scientific writing. Leandra da Silva Jardim: Contextualization, Development of methodologies and analyses made. Márcio Alberto Geihs: Contextualization, Discussion of results, Investigation, Writing – Review and Editing. Fábio Everton Maciel: Contextualization, Resources, Discussion of results, Investigation, Writing – Review and Editing. Luiz Eduardo Maia Nery:

Declaration of Competing Interest

None.

Acknowledgments

This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001 and Institute of Biological Sciences of the Federal University of Rio Grande (Brazil). NERY, L.E.M is a productivity fellow from CNPq (PQ 310830/2017-6). We are grateful to Diego Matheus Reinicke, Carolina de Andrade Teixeira Leite, Ana Clara Castanheira Cataud Pereira and Mariana Quaresma Souza for assistance.

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