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      Gene Expression Dynamics Accompanying the Sponge Thermal Stress Response

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      PLoS ONE
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          Abstract

          Marine sponges are important members of coral reef ecosystems. Thus, their responses to changes in ocean chemistry and environmental conditions, particularly to higher seawater temperatures, will have potential impacts on the future of these reefs. To better understand the sponge thermal stress response, we investigated gene expression dynamics in the shallow water sponge, Haliclona tubifera (order Haplosclerida, class Demospongiae), subjected to elevated temperature. Using high-throughput transcriptome sequencing, we show that these conditions result in the activation of various processes that interact to maintain cellular homeostasis. Short-term thermal stress resulted in the induction of heat shock proteins, antioxidants, and genes involved in signal transduction and innate immunity pathways. Prolonged exposure to thermal stress affected the expression of genes involved in cellular damage repair, apoptosis, signaling and transcription. Interestingly, exposure to sublethal temperatures may improve the ability of the sponge to mitigate cellular damage under more extreme stress conditions. These insights into the potential mechanisms of adaptation and resilience of sponges contribute to a better understanding of sponge conservation status and the prediction of ecosystem trajectories under future climate conditions.

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          Most cited references36

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          The Amphimedon queenslandica genome and the evolution of animal complexity.

          Sponges are an ancient group of animals that diverged from other metazoans over 600 million years ago. Here we present the draft genome sequence of Amphimedon queenslandica, a demosponge from the Great Barrier Reef, and show that it is remarkably similar to other animal genomes in content, structure and organization. Comparative analysis enabled by the sequencing of the sponge genome reveals genomic events linked to the origin and early evolution of animals, including the appearance, expansion and diversification of pan-metazoan transcription factor, signalling pathway and structural genes. This diverse 'toolkit' of genes correlates with critical aspects of all metazoan body plans, and comprises cell cycle control and growth, development, somatic- and germ-cell specification, cell adhesion, innate immunity and allorecognition. Notably, many of the genes associated with the emergence of animals are also implicated in cancer, which arises from defects in basic processes associated with metazoan multicellularity.
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            Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants.

            The potential of oxygen free radicals and other reactive oxygen species (ROS) to damage tissues and cellular components, called oxidative stress, in biological systems has become a topic of significant interest for environmental toxicology studies. The balance between prooxidant endogenous and exogenous factors (i.e., environmental pollutants) and antioxidant defenses (enzymatic and nonenzymatic) in biological systems can be used to assess toxic effects under stressful environmental conditions, especially oxidative damage induced by different classes of chemical pollutants. The role of these antioxidant systems and their sensitivity can be of great importance in environmental toxicology studies. In the past decade, numerous studies on the effects of oxidative stress caused by some environmental pollutants in terrestrial and aquatic species were published. Increased numbers of agricultural and industrial chemicals are entering the aquatic environment and being taken up into tissues of aquatic organisms. Transition metals, polycyclic aromatic hydrocarbons, organochlorine and organophosphate pesticides, polychlorinated biphenyls, dioxins, and other xenobiotics play important roles in the mechanistic aspects of oxidative damage. Such a diverse array of pollutants stimulate a variety of toxicity mechanisms, such as oxidative damage to membrane lipids, DNA, and proteins and changes to antioxidant enzymes. Although there are considerable gaps in our knowledge of cellular damage, response mechanisms, repair processes, and disease etiology in biological systems, free radical reactions and the production of toxic ROS are known to be responsible for a variety of oxidative damages leading to adverse health effects and diseases. In the past decade, mammalian species were used as models for the study of molecular biomarkers of oxidative stress caused by environmental pollutants to elucidate the mechanisms underlying cellular oxidative damage and to study the adverse effects of some environmental pollutants with oxidative potential in chronic exposure and/or sublethal concentrations. This review summarizes current knowledge and advances in the understanding of such oxidative processes in biological systems. This knowledge is extended to specific applications in aquatic organisms because of their sensitivity to oxidative pollutants, their filtration capacity, and their potential for environmental toxicology studies.
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              The MAP kinase signaling cascades: a system of hundreds of components regulates a diverse array of physiological functions.

              Sequential activation of kinases within the mitogen-activated protein (MAP) kinase (MAPK) cascades is a common, and evolutionary-conserved mechanism of signal transduction. Four MAPK cascades have been identified in the last 20 years and those are usually named according to the MAPK components that are the central building blocks of each of the cascades. These are the extracellular signal-regulated kinase 1/2 (ERK1/2), c-Jun N-Terminal kinase (JNK), p38, and ERK5 cascades. Each of these cascades consists of a core module of three tiers of protein kinases termed MAPK, MAPKK, and MAP3K, and often two additional tiers, the upstream MAP4K and the downstream MAPKAPK, which can complete five tiers of each cascade in certain cell lines or stimulations. The transmission of the signal via each cascade is mediated by sequential phosphorylation and activation of the components in the sequential tiers. These cascades cooperate in transmitting various extracellular signals and thus control a large number of distinct and even opposing cellular processes such as proliferation, differentiation, survival, development, stress response, and apoptosis. One way by which the specificity of each cascade is regulated is through the existence of several distinct components in each tier of the different cascades. About 70 genes, which are each translated to several alternatively spliced isoforms, encode the entire MAPK system, and allow the wide array of cascade's functions. These components, their regulation, as well as their involvement together with other mechanisms in the determination of signaling specificity by the MAPK cascade is described in this review. Mis-regulation of the MAPKs signals usually leads to diseases such as cancer and diabetes; therefore, studying the mechanisms of specificity-determination may lead to better understanding of these signaling-related diseases.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                27 October 2016
                2016
                : 11
                : 10
                : e0165368
                Affiliations
                [001]Marine Science Institute, College of Science, University of the Philippines, Diliman, Quezon City, Philippines
                University of Connecticut, UNITED STATES
                Author notes

                Competing Interests: CC was supported by a L’Oreal-UNESCO For Women in Science National Fellowship. 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, as detailed online in the guide for authors.

                • Conceptualization: CC.

                • Formal analysis: CG CC.

                • Funding acquisition: CC.

                • Investigation: CG CC.

                • Methodology: CG CC.

                • Software: CG CC.

                • Visualization: CG CC.

                • Writing – original draft: CG CC.

                • Writing – review & editing: CG CC.

                [¤]

                Current address: Okinawa Institute of Science and Technology Graduate University, 1919–1 Tancha, Onna-son, Okinawa, 904–0495, Japan

                Article
                PONE-D-16-21800
                10.1371/journal.pone.0165368
                5082814
                27788197
                082e8a67-a979-45b6-85ef-b5eb7abba7ba
                © 2016 Guzman, Conaco

                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
                : 31 May 2016
                : 11 October 2016
                Page count
                Figures: 4, Tables: 0, Pages: 15
                Funding
                Funded by: University of the Philippines System
                Award ID: OVPAA-BPhD-2012-04
                Award Recipient :
                Funded by: L’Oreal-UNESCO For Women in Science National Fellowship
                Award Recipient :
                This study was funded by the University of the Philippines System PhD Recruitment Grant (OVPAA-BPhD-2012-04) and a L’Oreal-UNESCO For Women in Science National Fellowship to CC. The funders 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
                Organisms
                Animals
                Invertebrates
                Sponges
                Physical Sciences
                Physics
                Classical Mechanics
                Mechanical Stress
                Thermal Stresses
                Biology and Life Sciences
                Genetics
                Gene Expression
                Biology and Life Sciences
                Cell Biology
                Cell Processes
                Cellular Stress Responses
                Biology and Life Sciences
                Marine Biology
                Coral Reefs
                Earth Sciences
                Marine and Aquatic Sciences
                Marine Biology
                Coral Reefs
                Earth Sciences
                Marine and Aquatic Sciences
                Reefs
                Coral Reefs
                Earth Sciences
                Marine and Aquatic Sciences
                Oceanography
                Ocean Temperature
                Biology and Life Sciences
                Computational Biology
                Genome Analysis
                Transcriptome Analysis
                Biology and Life Sciences
                Genetics
                Genomics
                Genome Analysis
                Transcriptome Analysis
                Biology and Life Sciences
                Cell Biology
                Cell Processes
                Cell Death
                Apoptosis
                Custom metadata
                Raw reads have been uploaded to the NCBI Short Read Archive database (PRJNA274004). This Transcriptome Shotgun Assembly project has been deposited at DDBJ/ENA/GenBank under the accession GFAV00000000. The version described in this paper is the first version, GFAV01000000.

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                Uncategorized

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