Epelboin Y et al. (2016), The Kinome of Pacific Oyster Crassostrea gigas,...

ECB-ART-44718

PLoS One 2016 May 04;115:e0155435. doi: 10.1371/journal.pone.0155435.

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The Kinome of Pacific Oyster Crassostrea gigas, Its Expression during Development and in Response to Environmental Factors.

Epelboin Y , Quintric L , Guévélou E , Boudry P , Pichereau V , Corporeau C .

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Oysters play an important role in estuarine and coastal marine habitats, where the majority of humans live. In these ecosystems, environmental degradation is substantial, and oysters must cope with highly dynamic and stressful environmental constraints during their lives in the intertidal zone. The availability of the genome sequence of the Pacific oyster Crassostrea gigas represents a unique opportunity for a comprehensive assessment of the signal transduction pathways that the species has developed to deal with this unique habitat. We performed an in silico analysis to identify, annotate and classify protein kinases in C. gigas, according to their kinase domain taxonomy classification, and compared with kinome already described in other animal species. The C. gigas kinome consists of 371 protein kinases, making it closely related to the sea urchin kinome, which has 353 protein kinases. The absence of gene redundancy in some groups of the C. gigas kinome may simplify functional studies of protein kinases. Through data mining of transcriptomes in C. gigas, we identified part of the kinome which may be central during development and may play a role in response to various environmental factors. Overall, this work contributes to a better understanding of key sensing pathways that may be central for adaptation to a highly dynamic marine environment.

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Genes referenced: cope gsk3a LOC100887844 LOC105440140 LOC115919910 LOC576733 LOC586799 LOC589947 LOC590870

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References [+] :

Al Quobaili, CK2 and the regulation of the carbohydrate metabolism. 2012, Pubmed

Al Quobaili, CK2 and the regulation of the carbohydrate metabolism. 2012, Pubmed
Bateman, The Pfam protein families database. 2004, Pubmed
Berthelin, Storage metabolism in the Pacific oyster (Crassostrea gigas) in relation to summer mortalities and reproductive cycle (west coast of France). 2000, Pubmed
Berwick, LRRK2 functions as a Wnt signaling scaffold, bridging cytosolic proteins and membrane-localized LRP6. 2012, Pubmed
Bettinger, The MEK kinases MEKK4/Ssk2p facilitate complexity in the stress signaling responses of diverse systems. 2007, Pubmed
Boutet, Characterization of reproduction-specific genes in a marine bivalve mollusc: influence of maturation stage and sex on mRNA expression. 2008, Pubmed
Bradham, The sea urchin kinome: a first look. 2006, Pubmed , Echinobase
C. elegans Sequencing Consortium, Genome sequence of the nematode C. elegans: a platform for investigating biology. 1998, Pubmed
Caenepeel, The mouse kinome: discovery and comparative genomics of all mouse protein kinases. 2004, Pubmed
Cambray, Protein kinase KIS localizes to RNA granules and enhances local translation. 2009, Pubmed
Cao, Oxidative stress activates both Src-kinases and their negative regulator Csk and induces phosphorylation of two targeting proteins for Csk: caveolin-1 and paxillin. 2004, Pubmed
Carling, The AMP-activated protein kinase cascade--a unifying system for energy control. 2004, Pubmed
Chen, De novo analysis of transcriptome dynamics in the migratory locust during the development of phase traits. 2010, Pubmed
Chen, Expression of calmodulin and myosin light chain kinase during larval settlement of the Barnacle Balanus amphitrite. 2012, Pubmed
Choi, The regulation of AMP-activated protein kinase by H(2)O(2). 2001, Pubmed
Choudhary, Lysine acetylation targets protein complexes and co-regulates major cellular functions. 2009, Pubmed
Clark, Identification of molecular and physiological responses to chronic environmental challenge in an invasive species: the Pacific oyster, Crassostrea gigas. 2013, Pubmed
Coburn, A putative cyclic nucleotide-gated channel is required for sensory development and function in C. elegans. 1996, Pubmed
Cohen, The regulation of protein function by multisite phosphorylation--a 25 year update. 2000, Pubmed
Cohen, Evolutionary and functional perspectives on signaling from neuronal surface to nucleus. 2015, Pubmed
Corporeau, A functional study of transforming growth factor-beta from the gonad of Pacific oyster Crassostrea gigas. 2011, Pubmed
Deretic, Autophagy, immunity, and microbial adaptations. 2009, Pubmed
Deshmukh, Evolution of domain combinations in protein kinases and its implications for functional diversity. 2010, Pubmed
Doroquez, Signal integration during development: mechanisms of EGFR and Notch pathway function and cross-talk. 2006, Pubmed
Duda, Allosteric modification, the primary ATP activation mechanism of atrial natriuretic factor receptor guanylate cyclase. 2011, Pubmed
Epelboin, Energy and antioxidant responses of pacific oyster exposed to trace levels of pesticides. 2015, Pubmed
Erce, The methylproteome and the intracellular methylation network. 2012, Pubmed
Escoubas, Oyster IKK-like protein shares structural and functional properties with its mammalian homologues. 1999, Pubmed
Fleury, Characterization of a gonad-specific transforming growth factor-beta superfamily member differentially expressed during the reproductive cycle of the oyster Crassostrea gigas. 2008, Pubmed
Fry, Cell cycle regulation by the NEK family of protein kinases. 2012, Pubmed
Gale, Molecular mechanisms of interferon resistance mediated by viral-directed inhibition of PKR, the interferon-induced protein kinase. 1998, Pubmed
Glatz, Structural mechanism for the specific assembly and activation of the extracellular signal regulated kinase 5 (ERK5) module. 2013, Pubmed
Goldberg, The dictyostelium kinome--analysis of the protein kinases from a simple model organism. 2006, Pubmed
Goodchild, AMP-activated protein kinase is a biomarker of energetic status in freshwater mussels exposed to municipal effluents. 2015, Pubmed
Gotoh, Identification and characterization of a novel MAP kinase kinase kinase, MLTK. 2001, Pubmed
Gourgou, Hyperthermia-induced Hsp70 and MT20 transcriptional upregulation are mediated by p38-MAPK and JNKs in Mytilus galloprovincialis (Lamarck); a pro-survival response. 2010, Pubmed
Green, Poly I:C induces a protective antiviral immune response in the Pacific oyster (Crassostrea gigas) against subsequent challenge with Ostreid herpesvirus (OsHV-1 μvar). 2013, Pubmed
Green, Ontogeny and water temperature influences the antiviral response of the Pacific oyster, Crassostrea gigas. 2014, Pubmed
Gricourt, Insulin-like system and growth regulation in the Pacific oyster Crassostrea gigas: hrIGF-1 effect on protein synthesis of mantle edge cells and expression of an homologous insulin receptor-related receptor. 2003, Pubmed
Guindon, New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. 2010, Pubmed
Guo, Immune and stress responses in oysters with insights on adaptation. 2015, Pubmed
Guévélou, Regulation of a truncated isoform of AMP-activated protein kinase α (AMPKα) in response to hypoxia in the muscle of Pacific oyster Crassostrea gigas. 2013, Pubmed
Guévélou, Sex-specific regulation of AMP-activated protein kinase (AMPK) in the Pacific oyster Crassostrea gigas. 2013, Pubmed
Hanks, Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. 1995, Pubmed
Hardie, The AMP-activated/SNF1 protein kinase subfamily: metabolic sensors of the eukaryotic cell? 1998, Pubmed
Hawley, Characterization of the AMP-activated protein kinase kinase from rat liver and identification of threonine 172 as the major site at which it phosphorylates AMP-activated protein kinase. 1996, Pubmed
Hayashi, PAR-1/MARK: a kinase essential for maintaining the dynamic state of microtubules. 2012, Pubmed
Heide, Regulation and possible function of axl expression in immature human mast cells. 1998, Pubmed
Herpin, Gene structure and expression of cg-ALR1, a type I activin-like receptor from the bivalve mollusc Crassostrea gigas. 2002, Pubmed
Herpin, Structural and functional evidences for a type 1 TGF-beta sensu stricto receptor in the lophotrochozoan Crassostrea gigas suggest conserved molecular mechanisms controlling mesodermal patterning across bilateria. 2005, Pubmed
Herpin, Structural and functional evidence for a singular repertoire of BMP receptor signal transducing proteins in the lophotrochozoan Crassostrea gigas suggests a shared ancestral BMP/activin pathway. 2005, Pubmed
Imai, Phosphorylation of 4E-BP by LRRK2 affects the maintenance of dopaminergic neurons in Drosophila. 2008, Pubmed
Jouaux, Identification of Ras, Pten and p70S6K homologs in the Pacific oyster Crassostrea gigas and diet control of insulin pathway. 2012, Pubmed
Kefaloyianni, Acute thermal stress and various heavy metals induce tissue-specific pro- or anti-apoptotic events via the p38-MAPK signal transduction pathway in Mytilus galloprovincialis (Lam.). 2005, Pubmed
Kim, The cytoplasmic tyrosine kinase FER is associated with the catenin-like substrate pp120 and is activated by growth factors. 1995, Pubmed
Kim, Constitutively active myosin light chain kinase alters axon guidance decisions in Drosophila embryos. 2002, Pubmed
Knighton, Crystal structure of the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase. 1991, Pubmed
Knippschild, The role of the casein kinase 1 (CK1) family in different signaling pathways linked to cancer development. 2005, Pubmed
Kolaiti, Isolation of a CK2α subunit and the holoenzyme from the mussel Mytilus galloprovincialis and construction of the CK2α and CK2β cDNAs. 2011, Pubmed
Kühl, Antagonistic regulation of convergent extension movements in Xenopus by Wnt/beta-catenin and Wnt/Ca2+ signaling. 2001, Pubmed
L'Etoile, Olfaction and odor discrimination are mediated by the C. elegans guanylyl cyclase ODR-1. 2000, Pubmed
LaRonde-LeBlanc, The RIO kinases: an atypical protein kinase family required for ribosome biogenesis and cell cycle progression. 2005, Pubmed
Lahiry, Kinase mutations in human disease: interpreting genotype-phenotype relationships. 2010, Pubmed
Lang, Transcriptome profiling of selectively bred Pacific oyster Crassostrea gigas families that differ in tolerance of heat shock. 2009, Pubmed
Lapraz, RTK and TGF-beta signaling pathways genes in the sea urchin genome. 2006, Pubmed , Echinobase
Le Quéré, Structural and functional characterizations of an Activin type II receptor orthologue from the pacific oyster Crassostrea gigas. 2009, Pubmed
Lelong, Structure and expression of mGDF, a new member of the transforming growth factor-beta superfamily in the bivalve mollusc Crassostrea gigas. 2000, Pubmed
Li, Genome-wide identification and comprehensive analyses of the kinomes in four pathogenic microsporidia species. 2014, Pubmed
Maier, Role of Ca2+/calmodulin-dependent protein kinase (CaMK) in excitation-contraction coupling in the heart. 2007, Pubmed
Malumbres, Physiological relevance of cell cycle kinases. 2011, Pubmed
Mann, Proteomic analysis of post-translational modifications. 2003, Pubmed
Manning, Evolution of protein kinase signaling from yeast to man. 2002, Pubmed
Manning, The protein kinase complement of the human genome. 2002, Pubmed
Manning, The minimal kinome of Giardia lamblia illuminates early kinase evolution and unique parasite biology. 2011, Pubmed
Manning, Genomic overview of protein kinases. 2005, Pubmed
Mantovani, Re-evaluating the general(ized) roles of AMPK in cellular metabolism. 2011, Pubmed
Marchi, Heavy metal interference with growth hormone signalling in trout hepatoma cells RTH-149. 2005, Pubmed
Miranda-Saavedra, Classification and functional annotation of eukaryotic protein kinases. 2007, Pubmed
Morrison, Protein kinases and phosphatases in the Drosophila genome. 2000, Pubmed
Murayama, Environmental alkalinity sensing mediated by the transmembrane guanylyl cyclase GCY-14 in C. elegans. 2013, Pubmed
Nguyen, Nek4 regulates entry into replicative senescence and the response to DNA damage in human fibroblasts. 2012, Pubmed
Pearce, The nuts and bolts of AGC protein kinases. 2010, Pubmed
Plotnikov, The MAPK cascades: signaling components, nuclear roles and mechanisms of nuclear translocation. 2011, Pubmed
Plowman, The protein kinases of Caenorhabditis elegans: a model for signal transduction in multicellular organisms. 1999, Pubmed
Portillo-López, MAPK is involved in metaphase I arrest in oyster and mussel oocytes. 2003, Pubmed
Poulos, Atrial natriuretic peptide gene expression within invertebrate hearts. 1995, Pubmed
Putzke, Essential kinase-independent role of a Fer-like non-receptor tyrosine kinase in Caenorhabditis elegans morphogenesis. 2005, Pubmed
Qi, MAP kinase pathways. 2005, Pubmed
Robinson, A scaling normalization method for differential expression analysis of RNA-seq data. 2010, Pubmed
Robinson, The protein tyrosine kinase family of the human genome. 2000, Pubmed
Roux, A functional genomic and proteomic perspective of sea urchin calcium signaling and egg activation. 2006, Pubmed , Echinobase
Saha, LRRK2 modulates vulnerability to mitochondrial dysfunction in Caenorhabditis elegans. 2009, Pubmed
Satoh, Tyrosine phosphorylation of ACK in response to temperature shift-down, hyperosmotic shock, and epidermal growth factor stimulation. 1996, Pubmed
Schenk, Signal perception and transduction: the role of protein kinases. 1999, Pubmed
Shilo, Signaling by the Drosophila epidermal growth factor receptor pathway during development. 2003, Pubmed
Silberbach, Natriuretic peptide signalling: molecular and cellular pathways to growth regulation. 2001, Pubmed
Smith, Defining specificity determinants of cGMP mediated gustatory sensory transduction in Caenorhabditis elegans. 2013, Pubmed
Sodergren, The genome of the sea urchin Strongylocentrotus purpuratus. 2006, Pubmed , Echinobase
Stull, Myosin light chain kinase and the role of myosin light chain phosphorylation in skeletal muscle. 2011, Pubmed
Sun, Interaction between protein kinase C delta and the c-Abl tyrosine kinase in the cellular response to oxidative stress. 2000, Pubmed
Sun, An EGFR gene of the Pacific oyster Crassostrea gigas functions in wound healing and promotes cell proliferation. 2014, Pubmed
Sundaram, RTK/Ras/MAPK signaling. 2006, Pubmed
Sussarellu, Transcriptomic response of the Pacific oyster Crassostrea gigas to hypoxia. 2010, Pubmed
Takei, Does the natriuretic peptide system exist throughout the animal and plant kingdom? 2001, Pubmed
Theillet, Cell signaling, post-translational protein modifications and NMR spectroscopy. 2012, Pubmed
Thiyagarajan, 2D gel-based proteome and phosphoproteome analysis during larval metamorphosis in two major marine biofouling invertebrates. 2009, Pubmed
Timmins-Schiffman, Shotgun proteomics as a viable approach for biological discovery in the Pacific oyster. 2013, Pubmed
Vesely, Atrial natriuretic peptides in the heart and hemolymph of the oyster, Crassostrea virginica: a comparison with vertebrates. 1993, Pubmed
Walsh, Protein posttranslational modifications: the chemistry of proteome diversifications. 2005, Pubmed
Wang, Tssk4 is essential for maintaining the structural integrity of sperm flagellum. 2015, Pubmed
Waskiewicz, Mitogen and stress response pathways: MAP kinase cascades and phosphatase regulation in mammals and yeast. 1995, Pubmed
Waterhouse, Jalview Version 2--a multiple sequence alignment editor and analysis workbench. 2009, Pubmed
Wong, Receptor guanylyl cyclases. 1992, Pubmed
Yamamoto, Expression and function of cGMP-dependent protein kinase type I during medaka fish embryogenesis. 2005, Pubmed
Yao, LRRK2-mediated neurodegeneration and dysfunction of dopaminergic neurons in a Caenorhabditis elegans model of Parkinson's disease. 2010, Pubmed
Yarden, The EGFR family and its ligands in human cancer. signalling mechanisms and therapeutic opportunities. 2001, Pubmed
Yoshida, Role for DYRK family kinases on regulation of apoptosis. 2008, Pubmed
Zeng, Expression of glycogen synthase (GYS) and glycogen synthase kinase 3β (GSK3β) of the Fujian oyster, Crassostrea angulata, in relation to glycogen content in gonad development. 2013, Pubmed
Zhang, The oyster genome reveals stress adaptation and complexity of shell formation. 2012, Pubmed
Zhao, Transcriptomic responses to salinity stress in the Pacific oyster Crassostrea gigas. 2012, Pubmed

	Fig 1. A tree of the C. gigas ePKs superfamily.Phylogenic analysis of amino acid sequences of C. gigas ePKs domains by neighbor joining. The tree is visualized with Figtree. The color blocks represent the nine groups of ePKs shown in this tree: AGC (PKA, PKG, PKC containing), CAMK (Ca/Calmodulin-type), CMGC (CDK, MAPK, GSK, CDKL), CK1 (Casein kinases), RGC (receptor guanylate cyclase), TK (tyrosine kinases), TKL (tyrosine kinase-like), STE and Others. The aPK superfamily was excluded from this analysis.
	Fig 2. Phylogenetic analysis of C. gigas RGC kinases.This tree was generated from RGC domain amino acid sequences from several species (Red: C. gigas, Purple: S. Purpuratus, Green: C. elegans, Blue: H. sapiens, Black: D. melanogaster), using the PhyML maximum likehood program and visualized with Figtree. A protein kinase from the TK group was used as outgroup (Insulin-related peptide receptor [CgEKC21734.1]). Corresponding maximum parsimony (MP) bootstrap values are shown on each branch.

	Fig 4. Group-level comparison of ePK and aPK genes up and down-regulated under environmental stressors.(A) Up-regulated protein kinases. (B) Down-regulated protein kinases. Pie charts depict the proportion of the protein kinases group, and the total number of pie is presented in Table 3. The absence of a pie chart means no regulation was observed.