Proteomic analysis of the crustacean molting gland (Y-organ) over the course of the molt cycle

Talia B. Head1, Donald L. Mykles2, Lars Tomanek1
1Department of Biological Sciences, Environmental Proteomics Laboratory, California Polytechnic State University, San Luis Obispo, CA 93407, USA
2Department of Biology, Colorado State University, Fort Collins, CO 80523, USA

Tài liệu tham khảo

Abuhagr, 2014, Molt regulation in green and red color morphs of the crab Carcinus maenas: gene expression of molt-inhibiting hormone signaling components, J. Exp. Biol., 217, 796, 10.1242/jeb.093385 Abuhagr, 2014, Mechanistic target of rapamycin (mTOR) signaling genes in decapod crustaceans: cloning and tissue expression of mTOR, Akt, Rheb, and p70 S6 kinase in the green crab, Carcinus maenas, and blackback land crab, Gecarcinus lateralis, Comp. Biochem. Physiol., 168A, 25, 10.1016/j.cbpa.2013.11.008 Abuhagr, 2016, Roles of mechanistic target of rapamycin and transforming growth factor-β signaling in the molting gland (Y-organ) of the blackback lan crab, Gecarcinus lateralis, Comp. Biochem. Physiol., 198A, 15, 10.1016/j.cbpa.2016.03.018 Babu, 1989, Cytoarchitecture of ecdysal gland/Y-organ of Charybdis annulata (Fabricius) (Crustacea: Decapoda: Brachyura), Raffles Bull. Zool., 16, 309 Berth, 2007, The state of the art in the analysis of two-dimensional gel electrophoresis images, Appl. Microbiol. Biotechnol., 76, 1223, 10.1007/s00253-007-1128-0 Birkenbiel, 1983, Ultrastructural and immunocytochemical investigation of ecdysteroid secretion by the prothoracic gland of the warmth Galleria mellonella, Cell Tissue Res., 299, 433 Brouwer, 2003, Replacement of a cytosolic cooper/zinc superoxide dismutase by a novel cytosolic manganese superoxide dismutase in crustaceans that use copper (haemocyanin) for oxygen transport, J. Biochem., 374, 219, 10.1042/bj20030272 Brown, 1986, A receptor-mediated pathway for cholesterol homeostasis, Science, 232, 34, 10.1126/science.3513311 Buchholz, 1980, The ultrastructural basis of steroid production in the Y-organ and the mandibular organ of the crabs Hemigrapsus nudus (Dana) and Carcninus maenas L, Cell Tissue Res., 206, 83, 10.1007/BF00233610 Burmester, 2002, Origin and evolution of arthropod hemocyanins and related proteins, J. Comp. Physiol. B., 172, 95, 10.1007/s00360-001-0247-7 Cerenius, 2010 Chandel, 2015 Chang, 2011, Regulation of crustacean molting: a review and our perspectives, Gen. Comp. Endocrinol., 172, 323, 10.1016/j.ygcen.2011.04.003 Chassard-Bouchaud, 1975, Sur l'existence de vesicules de reticulum endoplasmique lisse dans l'organe Y de Carcinus maenas, C. R. Acad. Sci., 281, 707 Chelikani, 2004, Diversity of structures and properties among catalases, Cell. Mol. Life Sci., 61, 192, 10.1007/s00018-003-3206-5 Cheng, 2002, Effects of environmental factors on the immune responses of freshwater prawn Macrobrachium rosenbergii and other decapod crustaceans, J. Taiwan Fisheries Res., 29, 1 Chung, 2008, A trehalose 6-phosphate synthase gene of the hemocytes of the blue crab, Callinectes sapidus: cloning, the expression, its enzyme activity and relationship to hemolymph trehalose levels, Saline Syst., 4, 18, 10.1186/1746-1448-4-18 Conus, 2010, Cathepsins: key modulators of cell death and inflammatory responses, Biochem. Pharmacol., 76, 1374, 10.1016/j.bcp.2008.07.041 Cooper, 1997, Transglutaminase-catalyzed inactivation of glyceraldehyde 3-phosphate dehydrogenase and α-ketoglutarate dehydrogenase complex by polyglutamine domains of pathological length, Proc. Natl. Acad. Sci. U. S. A., 94, 12604, 10.1073/pnas.94.23.12604 Covi, 2009, Conserved role of cyclic nucleotides in the regulation of ecdysteroidogenesis by the crustacean molting gland, Comp. Biochem. Physiol., 152A, 470, 10.1016/j.cbpa.2008.12.005 Covi, 2010, Molt cycle regulation of protein synthesis in skeletal muscle of the blackback land crab, Gecarcinus lateralis, and the differential expression of a myostatin-like factor during atrophy induced by molting or unweighting, J. Exp. Biol., 213, 172, 10.1242/jeb.034389 Covi, 2012, Neuropeptide signaling mechanisms in crustacean and insect molting glands, Invertebr. Reprod. Dev., 56, 33, 10.1080/07924259.2011.588009 Cox, 2010, Mitochondrial peroxiredoxin involvement in antioxidant defence and redox signalling, Biochem. J., 425, 313, 10.1042/BJ20091541 Das, 2016, Transcriptome analysis of the molting gland (Y-organ) from the blackback land crab, Gecarcinus lateralis, Comp. Biochem. Physiol., 17D, 26 Das, 2018, Transcriptomic analysis of differentially expressed genes in the molting gland (Y-organ) of the blackback land crab, Gecarcinus lateralis, during molt-cycle stage transitions, Comp. Biochem. Physiol., 28D, 37 Decker, 2004, Recent findings on phenoloxidase activity and antimicrobial activity of hemocyanins, Dev. Comp. Immunol., 28, 673, 10.1016/j.dci.2003.11.007 Destoumieux-Garzón, 2001, Antifungal peptides are generated from the c terminus of shrimp hemocyanin in response to microbial challenge, J. Biol. Chem., 276, 47070, 10.1074/jbc.M103817200 Durán, 2012, Glutaminolysis feeds mTORC1, Cell Cycle, 11, 4107, 10.4161/cc.22632 Durstewitz, 1997, cDNA cloning of a developmentally regulated hemocyanin subunit in the crustacean Cancer magister and phylogenetic analysis of the hemocyanin gene family, Mol. Biol. Evol., 14, 266, 10.1093/oxfordjournals.molbev.a025762 Durstewitz, 1997, Developmental changes in hemocyanin expression in the Dungeness crab, Cancer magister, J. Biol. Chem., 272, 4347, 10.1074/jbc.272.7.4347 Foyer, 2005, Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses, Plant Cell, 17, 1866, 10.1105/tpc.105.033589 Garnham, 2012, The chemical complexity of cellular microtubules: tubulin post-translational modification enzymes and their roles in tuning microtubule functions, Cytoskeleton, 69, 442, 10.1002/cm.21027 Giogio, 2007, Hydrogen peroxide: a metabolic by-product or a common mediator of ageing signals?, Nat. Rev. Mol. Cell Biol., 8, 722, 10.1038/nrm2240 Gottfredsen, 2012, The C-terminal proteolytic processing of extracellular superoxide dismutase is redox regulated, Free Radic. Biol. Med., 52, 191, 10.1016/j.freeradbiomed.2011.10.443 Hall, 1979, The role of microfilaments in the response of adrenal tumor cells to adrenocorticotropic hormone, J. Biol. Chem., 254, 9080, 10.1016/S0021-9258(19)86812-6 Halliwell, 2015 Hegedus, 2009, New insights into peritrophic matrix synthesis, architecture, and function, Annu. Rev. Entomol., 54, 285, 10.1146/annurev.ento.54.110807.090559 Hopkins, 2012, The eyes have it: a brief history of crustacean neuroendocrinology, Gen. Comp. Endocrinol., 175, 357, 10.1016/j.ygcen.2011.12.002 Intra, 2008, Phylogenetic analyses suggest multiple changes of substrate specificity within the glycosyl hydrolase 20 family, BMC Evol. Biol., 8, 214, 10.1186/1471-2148-8-214 Johnson, 2016, Uncovering hemocyanin subunit heterogeneity in penaeid shrimp using RNA-Seq, Integr. Comp. Biol., 56, 1080, 10.1093/icb/icw088 Kuballa, 2008, Differential expression profiling of components associated with exoskeletal hardening in crustaceans, BMC Genomics, 9, 575, 10.1186/1471-2164-9-575 Lachaise, 1993, The molting gland of crustaceans: localization, activity, and endocrine control (a review), J. Crustac. Biol., 13, 198, 10.2307/1548970 Lai, 2017, Role of tissue transglutaminase-2 (TG2)-mediated aminylation in biological processes, Amino Acids, 49, 501, 10.1007/s00726-016-2270-8 Lee, 2006, Proteomics and signal transduction in the crustacean molting gland, Integr. Comp. Biol., 46, 965, 10.1093/icb/icl047 Lee, 2003, Processing of an antibacterial peptide from hemocyanin of the freshwater crayfish Pacifatacus leniusculus, J. Biol. Chem., 278, 7927, 10.1074/jbc.M209239200 Liang, 1997, Pacifastin, a novel 155-kDa heterodimeric proteinase inhibitor containing a unique transferrin chain, Proc. Natl. Acad. Sci. U. S. A., 94, 6682, 10.1073/pnas.94.13.6682 Lin, 2008, Transglutaminase activity in the hematopoietic tissue of a crustacean, Pacifasticus leniusculus, importance in hemocyte homeostasis, BMC Immunol., 9, 58, 10.1186/1471-2172-9-58 Lu, 2006, Lysosomal metabolism of lipid-modified proteins, J. Lipid Res., 47, 1352, 10.1194/jlr.R600010-JLR200 Magdeldin, 2014, Basics and recent advances of two-dimensional polyacrylamide gel electrophoresis, Clin. Proteomics, 11, 16, 10.1186/1559-0275-11-16 Matsuda, 2007, An arthropod cuticular chitin-binding protein endows injured sites with transglutaminase-dependent mesh, J. Biol. Chem., 282, 10.1074/jbc.M705731200 Mentch, 2016, One-carbon metabolism and epigenetics: understanding the specificity, Ann. N. Y. Acad. Sci., 1363, 91, 10.1111/nyas.12956 Morris, 2002, Regulation of enzymes of the urea cycle and arginine metabolism, Annu. Rev. Nutr., 22, 87, 10.1146/annurev.nutr.22.110801.140547 Muller, 2012, Specific functions of lysosomal proteases in endocytic and autophagic pathways, Biochim. Biophys. Acta, 1824, 34, 10.1016/j.bbapap.2011.07.003 Mykles, 1980, The mechanism of fluid absorption at ecdysis in the American lobster, Homarus americanus, J. Exp. Biol., 84, 89, 10.1242/jeb.84.1.89 Mykles, 2001, Interactions between limb regeneration and molting in decapod crustaceans, Am. Zool., 41, 399 Mykles, 2011, Ecdysteroid metabolism in crustaceans, J. Steroid Biochem. Mol. Biol., 127, 196, 10.1016/j.jsbmb.2010.09.001 Mykles, 2015, Skeletal muscle differentiation, growth, and plasticity, 134 Mykles, 2010, Neuropeptide action in insects and crustaceans, Physiol. Biochem. Zool., 83, 836, 10.1086/648470 Petit, 2016, A hemocyanin-derived antimicrobial peptide from the penaeid shrimp adopts an alpha-helical structure that specifically permeabilizes fungal membranes, Biochim. Biophys. Acta, 1860, 557, 10.1016/j.bbagen.2015.12.010 Prasterlux, 2011, Molecular characterization and expression of the prostaglandin reductase 1 gene and protein during ovarian development of the giant tiger shrimp, Penaeus monodon, Aquaculture, 322, 134, 10.1016/j.aquaculture.2011.09.037 Qiu, 2008, Molecular cloning and mRNA expression of cathepsin C gene in black tiger shrimp (Penaeus monodon), Comp. Biochem. Physiol., 150A, 320 Rbycznski, 1995, Prothoracicotropic hormone elicits a rapid, developmentally specific synthesis of β tubulin in an insect endocrine gland, Dev. Biol., 169, 15, 10.1006/dbio.1995.1122 Rbycznski, 1995, Prothoracicotropic hormone-regulated expression of a hsp 70 cognate protein in the insect prothoracic gland, Mol. Cell. Endocrinol., 115, 73, 10.1016/0303-7207(95)03672-T Reglero, 1976, Glycosidases of mollusks: purification and properties of α-l-fucosidase from Chamelea gallina L, Eur. J. Biochem., 66, 379, 10.1111/j.1432-1033.1976.tb10527.x Rhee, 2005, Controlled elimination of intracellular H2O2: regulation of peroxiredoxin, catalase, and glutathione peroxidase via post-translational modification, Antioxid. Redox Signal., 7, 619, 10.1089/ars.2005.7.619 Rowley, 2005, Prostaglandins in non-insectan invertebrates: recent insights and unsolved problems, J. Exp. Biol., 208, 3, 10.1242/jeb.01275 Salaenoi, 2014, Variations of catalase and glutathione activities in molting cycle of mud crab, Scylla serrata, Kasetsart J. (Nat. Sci.), 48, 64 Shin, 2008, TGFβ mediates activation of transglutaminase 2 in response to oxidative stress that leads to protein aggregation, FASEB J., 22, 2498, 10.1096/fj.07-095455 Shyamal, 2018, Transcriptomic analysis of crustacean molting gland (Y-organ) regulation via the mTOR signaling pathway, Sci. Rep., 8, 7307, 10.1038/s41598-018-25368-x Singer, 1998, Thermotolerance in Saccharomyces cerevisiae: the yin and yang of trehalose, Trends Biotechnol., 16, 460, 10.1016/S0167-7799(98)01251-7 Skinner, 1962, Structure and metabolism of a crustacean integumentary tissue during a molt cycle, Biol. Bull., 123, 635, 10.2307/1539584 Skinner, 1985, Interacting factors in the control of the crustacean molt cycle, Am. Zool., 25, 275, 10.1093/icb/25.1.275 Skinner, 1985, Molting and regeneration, vol. 9 Smethurst, 1996, Measurement of tissue transglutaminase activity in a permeabilized cell system: its regulation by Ca2+ and nucleotides, J. Biochem., 313, 803, 10.1042/bj3130803 Smija, 2016, Histological changes of Y-organ in Travancoriana schirnerae during molt cycle and in de-eyestalked crabs, Turk. J. Fish. Aquat. Sci., 16, 533 Smith, 2001, Antimicrobial proteins in crustaceans, Phylogenet. Perspect. Vertebr. Immune Syst., 484, 95, 10.1007/978-1-4615-1291-2_10 Soldati, 1993, Rab GDI: A solubilizing and recycling factor for rab9 protein, Mol. Bio. Cell, 4, 425, 10.1091/mbc.4.4.425 Song, 1995, Multiple phosphorylation of ribosomal-protein S6 and specific protein-synthesis are required for prothoracicotropic hormone-stimulates ecdysteroid biosynthesis in the prothoracic glands of Manduca sexta, Insect Biochem. Mol. Biol., 25, 591, 10.1016/0965-1748(94)00100-V Sritunyalucksana, 2000, The proPO and clotting system in crustaceans, Aquaculture, 191, 53, 10.1016/S0044-8486(00)00411-7 Strickler, 1980, Estradiol 17-β dehydrogenase and 20α-hydroxysteroid dehydrogenase from human placental cytosol: one enzyme with two activities?, Steroids, 36, 243, 10.1016/0039-128X(80)90022-7 Stuart, 1994, HSP70 in mitochondrial biogenesis-from chaperoning nascent polypeptide-chains to facilitation of protein-degradation, Experientia, 50, 1002, 10.1007/BF01923454 Sugumaran, 2016, Critical analysis of the melanogenic pathway in insects and higher animals, Int. J. Mol. Sci., 17, 1753, 10.3390/ijms17101753 Terman, 2013, Post-translational modification and regulation of actin, Curr. Opin. Cell Biol., 25, 30, 10.1016/j.ceb.2012.10.009 Terwilliger, 2012, Gene expression profile, protein production, and functions of cryptocyanin during the crustacean molt cycle, Invertebr. Reprod. Dev., 56, 229, 10.1080/07924259.2011.595972 Terwilliger, 2015, Oxygen transport proteins in crustacea: hemocyanin and hemoglobin, 359 Terwilliger, 2006, Functional and phylogenetic analysis of phenoloxidases from brachyuran (Cancer magister) and brachiopod (Artemia franciscana, Triops longicaudatus) crustaceans, Biol. Bull., 210, 38, 10.2307/4134535 Terwilliger, 1999, Cryptocyanin, a crustacean molting protein: evolutionary link with arthropod hemocyanins and insect hexamerins, Proc. Natl. Acad. Sci. U. S. A., 96, 2013, 10.1073/pnas.96.5.2013 Terwilliger, 2005, Evolution of novel functions: cryptocyanin helps build new exoskeleton in Cancer magister, J. Exp. Biol., 208, 2467, 10.1242/jeb.01667 Tharia, 2002, Complete cDNA sequence of SAP-like pentraxin from Limulus polyphemus: implication for pentraxin evolution, J. Mol. Biol., 316, 583, 10.1006/jmbi.2001.5356 Thongbuakaew, 2016, Steroid and genes related to steroid biosynthesis in the female giant freshwater prawn, Macrobrachium rosenbergii, Steroids, 107, 149, 10.1016/j.steroids.2016.01.006 Tomanek, 2011, Environmental proteomics: changes in the proteome of marine organisms in response to environmental stress, pollutants, infection, symbiosis and development, Annu. Rev. Mar. Sci., 3, 373, 10.1146/annurev-marine-120709-142729 Tomanek, 2012, Introduction to the symposium "comparative proteomics of environmental and pollution stress", Integr. Comp. Biol., 52, 622, 10.1093/icb/ics116 Tomanek, 2014, Proteomics to study adaptations in marine organisms to environmental stress, J. Proteome, 105, 92, 10.1016/j.jprot.2014.04.009 Tomanek, 2015, Proteomic responses to environmentally induced oxidative stress, J. Exp. Biol., 218, 1867, 10.1242/jeb.116475 Tomiya, 2006, Purification, characterization, cloning of a Spodoptera frugiperda Sf9 beta-N-acetylhexosaminidase that hydrolyzes terminal N-acetylglucosamine on the N-glycan core, J. Biol. Chem., 281, 19545, 10.1074/jbc.M603312200 Walsh, 2006 Wang, 2016, cDNA cloning, characterization and mRNA expression of cryptocyanin from the Chinese mitten crab, Eriocheir sinensis H. Milne Edwards, 1853, Crustaceana, 89, 273, 10.1163/15685403-00003522 Watson, 1996, Involvement of microtubules in prothorcicotropic hormone-stimulated ecdysteroidogenesis by insect (Manduca sexta) prothoracic glands, J. Exp. Zool., 276, 63, 10.1002/(SICI)1097-010X(19960901)276:1<63::AID-JEZ7>3.0.CO;2-3 Webster, 1986, Neurohormonal control of ecdysteroid biosynthesis by Carcinus maenas Y-organs in vitro and preliminary characterization of the putative molt-inhibiting hormone, Gen. Comp. Endocrinol., 61, 237, 10.1016/0016-6480(86)90201-7 Webster, 2015, Endocrinology of molting, 1 Wolcott, 1991, Nitrogen excretion is enhanced during urine recycling in two species of terrestrial crab, J. Exp. Zool., 259, 181, 10.1002/jez.1402590206 Yamanaka, 2015, Vesicle-mediated steroid hormone secretion in Drosophila melanogaster, Cell, 163, 907, 10.1016/j.cell.2015.10.022 Yokomizo, 1996, cDNA cloning, expression, and mutagenesis study of leukotriene B4 12-hydroxydehydrogenase, J. Biol. Chem., 271, 2844, 10.1074/jbc.271.5.2844 Yu, 2002, Characterization of limb autotomy factor-proecdysis (LAFpro), isolated from limb regenerates, that suspends molting in the land crab Gecarcinus lateralis, Biol. Bull., 202, 204, 10.2307/1543470