Metabolite profiling of the post-ovulatory oocytes of the common carp, Cyprinus carpio: A 1H NMR-based metabolomics approach

Abbaszadeh, 2021, An application of histological technique for monitoring health status of fish species, Leuciscus aspius (Linnaeus, 1758) inhabiting Aras River, Iran, Caspian J. Environ. Sci., 19, 187 Aegerter, 2004, Effects of post-ovulatory oocyte ageing and temperature on egg quality and on the occurrence of triploid fry in rainbow trout, Oncorhynchus mykiss, Aquaculture, 231, 59, 10.1016/j.aquaculture.2003.08.019 Aliferis, 2011, Metabolomics–a robust bioanalytical approach for the discovery of the modes-of-action of pesticides: a review, Pestic. Biochem. Physiol., 100, 105, 10.1016/j.pestbp.2011.03.004 Asgharzadeh, 2021, Antibacterial activity of metabolites isolated from Streptomyces ssp. on soil sample of West Azerbaijan, Iran, Int. J. Adv. Biol. Biomed. Res., 9, 147 Baldissera, 2018, Gill bioenergetics dysfunction and oxidative damage induced by thiamethoxam exposure as relevant toxicological mechanisms in freshwater silver catfish Rhamdia quelen, Sci. Total Environ., 636, 420, 10.1016/j.scitotenv.2018.04.292 Banaee, 2014, Alterations in biochemical parameters of the freshwater fish, Alburnus mossulensis, exposed to sub-lethal concentrations of fenpropathrin, Int. J. Aquat. Biol., 2, 58 Beckonert, 2007, Metabolic profiling, metabolomic and metabonomic procedures for NMR spectroscopy of urine, plasma, serum and tissue extracts, Nat. Protoc., 2, 2692, 10.1038/nprot.2007.376 Bessman, 1985, The creatine-creatine phosphate energy shuttle, Annu. Rev. Biochem., 54, 831, 10.1146/annurev.bi.54.070185.004151 Bobe, 2010, Egg and sperm quality in fish, Gen. Comp. Endocrinol., 165, 535, 10.1016/j.ygcen.2009.02.011 Bonnet, 2007, Effect of photoperiod manipulation on rainbow trout (Oncorhynchus mykiss) egg quality: a genomic study, Aquaculture, 268, 13, 10.1016/j.aquaculture.2007.04.027 Boulekbache, 1989, Ageing of fish oocytes: effects on adenylic nucleotides content, energy charge and viability of carp embryo, Comp. Biochem. Physiol. Part B Comp. Biochem., 93, 471, 10.1016/0305-0491(89)90109-0 Boussouar, 2004, Lactate and energy metabolism in male germ cells, Trends Endocrinol. Metab., 15, 345, 10.1016/j.tem.2004.07.003 Bozkurt, 2014, Effect of different avian egg yolk types on fertilization ability of cryopreserved common carp (Cyprinus carpio) spermatozoa, Aquac. Int., 22, 131, 10.1007/s10499-013-9728-4 Brooks, 2002, Lactate shuttles in nature, Biochem. Soc. Trans., 30, 258, 10.1042/bst0300258 Buckley, 2005, In vivo inosine protects alveolar epithelial type 2 cells against hyperoxia-induced DNA damage through MAP kinase signaling, Am. J. Phys. Lung Cell. Mol. Phys., 288, L569 Bundy, 2009, Environmental metabolomics: a critical review and future perspectives, Metabolomics, 5, 3, 10.1007/s11306-008-0152-0 Cappello, 2021, Time-dependent metabolic disorders induced by short-term exposure to polystyrene microplastics in the Mediterranean mussel Mytilus galloprovincialis, Ecotoxicol. Environ. Saf., 209, 10.1016/j.ecoenv.2020.111780 Carnevali, 1999, Molecular cloning and expression of ovarian cathepsin D in seabream,Sparus aurata, Biol. Reprod., 61, 785, 10.1095/biolreprod61.3.785 Carnevali, 2001, Molecular components related to egg viability in the gilthead sea bream, Sparus aurata, Mol. Reprod. Dev., 58, 330, 10.1002/1098-2795(200103)58:3<330::AID-MRD11>3.0.CO;2-7 Cevallos-Cevallos, 2009, Metabolomic analysis in food science: a review, Trends Food Sci. Technol., 20, 557, 10.1016/j.tifs.2009.07.002 Chari, 2008, Activation of central lactate metabolism lowers glucose production in uncontrolled diabetes and diet-induced insulin resistance, Diabetes, 57, 836, 10.2337/db07-1464 Deng, 2006, Effects of inosine on neuronal apoptosis and the expression of cytochrome C mRNA following hypoxic-ischemic brain damage in neonatal rats, Zhongguo Dang dai er ke za zhi= Chin. J. Contemp. Pediatr., 8, 266 Dorafshan, 2003, Induction of spawning in common carp Cyprinus carpio, using pituitary extract and GnRH analogue in combination with Domperidone, Iran. J. Biotechnol., 213 Fallahpour, 2014, Effects of dietary marshmallow (Althaea officinalis L.) extract on growth performance and body composition of common carp (Cyprinus carpio), Int. J. Adv. Biol. Biomed. Res., 2, 2453 Fedotova, 2017, Hydration structure of osmolyte TMAO: concentration/pressure-induced response, New J. Chem., 41, 1219, 10.1039/C6NJ03296F Formacion, 1995, Overripening of ovulated eggs in goldfish, Carassius auratus: II. Possible involvement of postovulatory follicles and steroids, Fish Physiol. Biochem., 14, 237, 10.1007/BF00004314 Gladden, 2004, Lactate metabolism: a new paradigm for the third millennium, J. Physiol., 558, 5, 10.1113/jphysiol.2003.058701 Glaser, 2010, Oxidative stress-mediated inhibition of brain creatine kinase activity by methylmercury, Neurotoxicology, 31, 454, 10.1016/j.neuro.2010.05.012 Greeley, 1986, Changes in teleost yolk proteins during oocyte maturation: correlation of yolk proteolysis with oocyte hydration, Comp. Biochem. Physiol. B Comp. Biochem., 84, 1, 10.1016/0305-0491(86)90262-2 Guo, 2013, Oxidative stress, mitochondrial damage and neurodegenerative diseases, Neural Regen. Res., 8, 2003 Hajiradkouchak, 2019, Age determination, growth indices and reproduction biology of Prussian carp, Carassius gibelio (Bloch, 1782) from four reservoirs in Golestan Province, Southeast Caspian Sea, Caspian J. Environ. Sci., 17, 337 Hajirezaee, 2010, Fish milt quality and major factors influencing the milt quality parameters: a review, Afr. J. Biotechnol., 9, 9148 Hajirezaee, 2017, NMR-based metabolomic study on the toxicological effects of pesticide, diazinon on adaptation to sea water by endangered persian sturgeon, Acipenser persicus fingerlings, Chemosphere, 185, 213, 10.1016/j.chemosphere.2017.07.016 Hajirezaee, 2018, Effects of egg aging on the metabolites of ovarian fluid in rainbow trout, Oncorhynchus mykiss, Aquacult. Res., 49, 104, 10.1111/are.13438 Hardie, 2003, Management of cellular energy by the AMP-activated protein kinase system, FEBS Lett., 546, 113, 10.1016/S0014-5793(03)00560-X Harris, 2013 Hatef, 2009, Composition of ovarian fluid in endangered Caspian brown trout, Salmo trutta caspius, and its effects on spermatozoa motility and fertilizing ability compared to freshwater and a saline medium, Fish Physiol. Biochem., 35, 695, 10.1007/s10695-008-9302-6 Heidary, 2016, Changes in biochemical and physiological responses of common carp, Cyprinus Carpio L. after long-term exposure to Pb (II), Caspian J. Environ. Sci., 14, 311 Horváth, 1985 Jeney, 2009, Use and exchange of aquatic resources relevant for food and aquaculture: common carp (Cyprinus carpio L.), Rev. Aquac., 1, 163, 10.1111/j.1753-5131.2009.01012.x Khaledi, 2019, Molecular docking and druggability studies of terpenoid-derived metabolites from marine sponges as IL-17A inhibitors, Eurasian Chem. Commun., 1, 419, 10.33945/SAMI/ECC.2019.5.2 Krastanov, 2010, Metabolomics—the state of art, Biotechnol. Biotechnol. Equip., 24, 1537, 10.2478/V10133-010-0001-Y Kumar, 2019, Utilization of a by-product from the Jatropha biodiesel industry as a fish meal replacer in common carp Cyprinus carpio L. diets, J. Appl. Aquac., 31, 48, 10.1080/10454438.2018.1545720 Lahnsteiner, 2000, Morphological, physiological and biochemical parameters characterizing the over-ripening of rainbow trout eggs, Fish Physiol. Biochem., 23, 107, 10.1023/A:1007839023540 Lenz, 2005, The creatine kinase system in human skin: protective effects of creatine against oxidative and UV damage in vitro and in vivo, J. Investig. Dermatol., 124, 443, 10.1111/j.0022-202X.2004.23522.x Maiti, 2021, Effect of TMAO on the structure and phase transition of lipid membranes: potential role of TMAO in stabilizing cell membranes under osmotic stress, J. Phys. Chem. B, 125, 1167, 10.1021/acs.jpcb.0c08335 Mansour, 2008, Morphological characterization of Arctic char, Salvelinus alpinus, eggs subjected to rapid post-ovulatory aging at 7 C, Aquaculture, 279, 204, 10.1016/j.aquaculture.2008.04.014 May, 2017, NMR profiling of metabolites in larval and juvenile blue mussels (Mytilus edulis) under ambient and low salinity conditions, Metabolites, 7, 33, 10.3390/metabo7030033 Migaud, 2013, Gamete quality and broodstock management in temperate fish, Rev. Aquac., 5, S194, 10.1111/raq.12025 Miller, 2007, Environmental metabolomics: a SWOT analysis (strengths, weaknesses, opportunities, and threats), J. Proteome Res., 6, 540, 10.1021/pr060623x Mohagheghi Samarin, 2010, Biochemical and histological studies of over-ripened oocyte in the Caspian brown trout (Salmo trutta caspius) to determine biomarkers for egg quality, Iran. J. Fish. Sci., 9, 33 Mohagheghi Samarin, 2015, Fish oocyte ageing and its effect on egg quality, Rev. Fish. Sci. Aquacult., 23, 302, 10.1080/23308249.2015.1053560 Nagy, 2020, Trimethylamine-N-oxide is present in human follicular fluid and is a negative predictor of embryo quality, Hum. Reprod., 35, 81, 10.1093/humrep/dez224 Niksirat, 2007, Effects of storage duration and storage media on initial and post-eyeing mortality of stored ova of rainbow trout Oncorhynchus mykiss, Aquaculture, 262, 528, 10.1016/j.aquaculture.2006.10.031 Niksirat, 2007, In vitro storage of unfertilized ova of endangered Caspian brown trout (Salmo trutta caspius) in artificial media, Anim. Reprod. Sci., 100, 356, 10.1016/j.anireprosci.2006.08.019 Niksirat, 2017, Quantification of egg proteome changes during fertilization in sterlet Acipenser ruthenus, Biochem. Biophys. Res. Commun., 490, 189, 10.1016/j.bbrc.2017.06.019 Niksirat, 2020, Proteomic changes after fertilization and before first cleavage in rainbow trout Oncorhynchus mykiss, Aquaculture, 520, 10.1016/j.aquaculture.2020.734951 Ochokwu, 2015, Effect of egg and sperm quality in successful fish breeding, IOSR J. Agric. Vet. Sci. (IOSR-JAVS), 8, 48 Pallares-Mendez, 2016, Metabolomics in diabetes, a review, Ann. Med., 48, 89, 10.3109/07853890.2015.1137630 Philp, 2005, Lactate–a signal coordinating cell and systemic function, J. Exp. Biol., 208, 4561, 10.1242/jeb.01961 Pilo, 2018, A storm in the niche: iron, oxidative stress and haemopoiesis, Blood Rev., 32, 29, 10.1016/j.blre.2017.08.005 Rabinowitz, 1974, Plasma cyclic adenosine 3′ 5′-monophosphate (AMP) levels in acute myocardial infarction, Am. J. Cardiol., 34, 7, 10.1016/0002-9149(74)90085-X Rauschert, 2014, Metabolomic biomarkers for obesity in humans: a short review, Ann. Nutr. Metab., 64, 314, 10.1159/000365040 Rime, 2004, Post-ovulatory ageing and egg quality: a proteomic analysis of rainbow trout coelomic fluid, Reprod. Biol. Endocrinol., 2, 1, 10.1186/1477-7827-2-26 Rottenberg, 2017, The path from mitochondrial ROS to aging runs through the mitochondrial permeability transition pore, Aging Cell, 16, 943, 10.1111/acel.12650 Samarin, 2018, Egg oxidation status, antioxidant enzyme activities, lipid classes, fatty acid composition profile and embryo survival rates during in vitro oocyte ageing in tench Tinca tinca (Linnaeus, 1758), Aquac. Res., 49, 2305, 10.1111/are.13693 Samarin, 2018, mRNA abundance changes during in vitro oocyte ageing in African catfish Clarias gariepinus (Burchell, 1822), Aquac. Res., 49, 1037, 10.1111/are.13552 Samarin, 2019, Cellular and molecular changes associated with fish oocyte ageing, Rev. Aquac., 11, 619, 10.1111/raq.12249 Samarin, 2019, The possible involvement of oxidative stress in the oocyte ageing process in goldfish Carassius auratus (Linnaeus, 1758), Sci. Rep., 9, 1, 10.1038/s41598-019-46895-1 Sanchís, 2018, Metabolic responses of Mytilus galloprovincialis to fullerenes in mesocosm exposure experiments, Environ. Sci. Technol., 52, 1002, 10.1021/acs.est.7b04089 Schlattner, 2006, Mitochondrial creatine kinase in human health and disease, Biochim. Biophys. Acta (BBA)-Mol. Basis Dis., 1762, 164, 10.1016/j.bbadis.2005.09.004 Sharma, 2013, Osmolyte induced stabilization of protein molecules: a brief review, J. Proteins Proteomics, 3 Shaw, 2004, The tumor suppressor LKB1 kinase directly activates AMP-activated kinase and regulates apoptosis in response to energy stress, Proc. Natl. Acad. Sci., 101, 3329, 10.1073/pnas.0308061100 Souza, 2019, Oxidative stress mediated the inhibition of cerebral creatine kinase activity in silver catfish fed with aflatoxin B1-contaminated diet, Fish Physiol. Biochem., 45, 63, 10.1007/s10695-018-0534-9 Spratlin, 2009, Clinical applications of metabolomics in oncology: a review, Clin. Cancer Res., 15, 431, 10.1158/1078-0432.CCR-08-1059 Sun, 2017, Gut microbial metabolite TMAO contributes to renal dysfunction in a mouse model of diet-induced obesity, Biochem. Biophys. Res. Commun., 493, 964, 10.1016/j.bbrc.2017.09.108 Surnar, 2015, Hormone administration with induced spawning of Indian major carp, Int. J. Fish. Aquat. Stud., 3, 1 Tafani, 2016, The interplay of reactive oxygen species, hypoxia, inflammation, and sirtuins in cancer initiation and progression, Oxidative Med. Cell. Longev., 2016, 10.1155/2016/3907147 Thomas, 1994, Free radical inactivation of rabbit muscle creatine kinase: catalysis by physiological and hydrolyzed ICRF-187 (ICRF-198) iron chelates, Free Radic. Res., 21, 387, 10.3109/10715769409056591 Tokarska-Schlattner, 2012, Phosphocreatine interacts with phospholipids, affects membrane properties and exerts membrane-protective effects, PLoS One, 7, 10.1371/journal.pone.0043178 Ufnal, 2015, TMAO: a small molecule of great expectations, Nutrition, 31, 1317, 10.1016/j.nut.2015.05.006 Utley, 1967, Effect of sulfhydryl reagents on peroxidation in microsomes, Arch. Biochem. Biophys., 118, 29, 10.1016/0003-9861(67)90273-1 Váarkonyi, 1998, Chromosomal and morphological abnormalities caused by oocyte ageing in Silurus glanis, J. Fish Biol., 52, 899 Valdebenito, 2015, Gamete quality in fish: evaluation parameters and determining factors, Zygote, 23, 177, 10.1017/S0967199413000506 Van Ravenzwaay, 2007, The use of metabolomics for the discovery of new biomarkers of effect, Toxicol. Lett., 172, 21, 10.1016/j.toxlet.2007.05.021 Vercesi, 1997, The role of reactive oxygen species in mitochondrial permeability transition, Biosci. Rep., 17, 43, 10.1023/A:1027335217774 Vignet, 2019, Imidacloprid induces adverse effects on fish early life stages that are more severe in japanese medaka (Oryzias latipes) than in zebrafish (Danio rerio), Chemosphere, 225, 470, 10.1016/j.chemosphere.2019.03.002 Wang, 2001, An unusually low pK (a) for Cys282 in the active site of human muscle creatine kinase, Biochemistry, 40, 11698, 10.1021/bi011208f Weljie, 2006, Targeted profiling: quantitative analysis of 1H NMR metabolomics data, Anal. Chem., 78, 4430, 10.1021/ac060209g Wu, 2008, Reduced cell death by inosine pretreatment after photochemically induced cerebral ischemia in adult rats, Prog. Nat. Sci., 18, 1513, 10.1016/j.pnsc.2008.03.032 Xia, 2011, Metabolomic data processing, analysis, and interpretation using MetaboAnalyst, Curr. Protoc. Bioinformatics, 34, 10.1002/0471250953.bi1410s34 Yancey, 2001, Water stress, osmolytes and proteins, Am. Zool., 41, 699 Yancey, 2005, Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses, J. Exp. Biol., 208, 2819, 10.1242/jeb.01730 Zhang, 2004, EFFECTS OF INOSINE ON APOPTOSIS AND EXPRESSION OF HSP-70 mRNA IN NEURONS AFTER CEREBRAL ISCHEMIA AND REPERFUSION IN RATS [J], Acta Acad. Qingdao Umvesitatis, 4 Zhang, 2012, Serum metabolomics as a novel diagnostic approach for disease: a systematic review, Anal. Bioanal. Chem., 404, 1239, 10.1007/s00216-012-6117-1 Zhang, 2019, Chlorpyrifos induced oxidative stress to promote apoptosis and autophagy through the regulation of miR-19a-AMPK axis in common carp, Fish Shellfish Immunol., 93, 1093, 10.1016/j.fsi.2019.07.022 Zucchi, 1989, Protection of isolated rat heart from oxidative stress by exogenous creatine phosphate, J. Mol. Cell. Cardiol., 21, 67, 10.1016/0022-2828(89)91494-6