{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,8]],"date-time":"2026-10-08T20:56:50Z","timestamp":1791493010368,"version":"4.3.4"},"reference-count":85,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2020,4,18]],"date-time":"2020-04-18T00:00:00Z","timestamp":1587168000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Ministry of Science Techmology, Taiwan","award":["107-2622-B-033-001-CC2; 108-2622-B-033-001-CC2"],"award-info":[{"award-number":["107-2622-B-033-001-CC2; 108-2622-B-033-001-CC2"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Lysophosphatidic acid (LPA) is a small lysophospholipid molecule that activates multiple cellular functions through pathways with G-protein-coupled receptors. So far, six LPA receptors (LPAR1 to LPAR6) have been discovered and each one of them can connect to the downstream cell message-transmitting network. A previous study demonstrated that LPA receptors found in blood-producing stem cells can enhance erythropoietic processes through the activation of LPAR3. In the current study, newly discovered functions of LPAR3 were identified through extensive behavioral tests in lpar3 knockout (KO) zebrafish. It was found that the adult lpar3 KO zebrafish display an abnormal movement orientation and altered exploratory behavior compared to that of the control group in the three-dimensional locomotor and novel tank tests, respectively. Furthermore, consistent with those results, in the circadian rhythm locomotor activity test, the lpar3 KO zebrafish showed a lower level of angular velocity and average speed during the light cycles, indicating an hyperactivity-like behavior. In addition, the mutant fish also exhibited considerably higher locomotor activity during the dark cycle. Supporting those findings, this phenomenon was also displayed in the lpar3 KO zebrafish larvae. Furthermore, several important behavior alterations were also observed in the adult lpar3 KO fish, including a lower degree of aggression, less interest in conspecific social interaction, and looser shoal formation. However, there was no significant difference regarding the predator avoidance behavior between the mutant and the control fish. In addition, lpar3 KO zebrafish displayed memory deficiency in the passive avoidance test. These in vivo results support for the first time that the lpar3 gene plays a novel role in modulating behaviors of anxiety, aggression, social interaction, circadian rhythm locomotor activity, and memory retention in zebrafish.<\/jats:p>","DOI":"10.3390\/ijms21082837","type":"journal-article","created":{"date-parts":[[2020,4,21]],"date-time":"2020-04-21T04:49:38Z","timestamp":1587444578000},"page":"2837","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":14,"title":["A Novel Function of the Lysophosphatidic Acid Receptor 3 (LPAR3) Gene in Zebrafish on Modulating Anxiety, Circadian Rhythm Locomotor Activity, and Short-Term Memory"],"prefix":"10.3390","volume":"21","author":[{"given":"Yu-Nung","family":"Lin","sequence":"first","affiliation":[{"name":"Department of Life Science, National Taiwan University, Taipei 11221, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gilbert","family":"Audira","sequence":"additional","affiliation":[{"name":"Department of Chemistry, Chung Yuan Christian University, Chung-Li 32023, Taiwan"},{"name":"Department of Bioscience Technology, Chung Yuan Christian University, Chung-Li 32023, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nemi","family":"Malhotra","sequence":"additional","affiliation":[{"name":"Department of Biomedical Engineering, Chung Yuan Christian University, Chung-Li 32023, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nguyen Thi","family":"Ngoc Anh","sequence":"additional","affiliation":[{"name":"Department of Bioscience Technology, Chung Yuan Christian University, Chung-Li 32023, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Petrus","family":"Siregar","sequence":"additional","affiliation":[{"name":"Department of Bioscience Technology, Chung Yuan Christian University, Chung-Li 32023, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2056-3065","authenticated-orcid":false,"given":"Jen-Her","family":"Lu","sequence":"additional","affiliation":[{"name":"Department of Pediatrics, Taipei Veterans General Hospital, Taipei 11221, Taiwan"},{"name":"School of Medicine, National Yang-Ming University, Taipei 11221, Taiwan"},{"name":"School of Medicine, National Defense Medical Center, Taipei 11490, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1477-0183","authenticated-orcid":false,"given":"Hsinyu","family":"Lee","sequence":"additional","affiliation":[{"name":"Department of Life Science, National Taiwan University, Taipei 11221, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6398-8672","authenticated-orcid":false,"given":"Chung-Der","family":"Hsiao","sequence":"additional","affiliation":[{"name":"Department of Chemistry, Chung Yuan Christian University, Chung-Li 32023, Taiwan"},{"name":"Department of Bioscience Technology, Chung Yuan Christian University, Chung-Li 32023, Taiwan"},{"name":"Center for nanotechnology, Chung Yuan Christian University, Chung-Li 32023, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2020,4,18]]},"reference":[{"key":"ref_1","first-page":"3704","article-title":"Lysophosphatidic acid induces urokinase secretion by ovarian cancer cells","volume":"5","author":"Pustilnik","year":"1999","journal-title":"Clin. Cancer Res."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1006\/mcne.2002.1123","article-title":"Lysophosphatidic acid influences the morphology and motility of young, postmitotic cortical neurons","volume":"20","author":"Fukushima","year":"2002","journal-title":"Mol. Cell. Neurosci."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"12949","DOI":"10.1074\/jbc.270.22.12949","article-title":"Lysophosphatidic acid, a multifunctional phospholipid messenger","volume":"270","author":"Moolenaar","year":"1995","journal-title":"J. Biol. Chem."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"7983","DOI":"10.1158\/0008-5472.CAN-05-4381","article-title":"Hypoxia enhances lysophosphatidic acid responsiveness in ovarian cancer cells and lysophosphatidic acid induces ovarian tumor metastasis in vivo","volume":"66","author":"Kim","year":"2006","journal-title":"Cancer Res."},{"key":"ref_5","first-page":"649702","article-title":"Lysophosphatidic acid (LPA) signaling in human and ruminant reproductive tract","volume":"2014","author":"Boruszewska","year":"2014","journal-title":"Mediat. Inflamm."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"48737","DOI":"10.1074\/jbc.M206812200","article-title":"Serum lysophosphatidic acid is produced through diverse phospholipase pathways","volume":"277","author":"Aoki","year":"2002","journal-title":"J. Biol. Chem."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1095\/biolreprod61.1.195","article-title":"Production of lysophosphatidic acids by lysophospholipase D in human follicular fluids of in vitro fertilization patients","volume":"61","author":"Tokumura","year":"1999","journal-title":"Biol. Reprod."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1530\/REP-08-0209","article-title":"Lysophosphatic acid modulates prostaglandin secretion in the bovine uterus","volume":"137","author":"Komiyama","year":"2009","journal-title":"Reproduction"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"364","DOI":"10.1006\/gyno.1998.5193","article-title":"Phorbol 12-myristate 13-acetate stimulates lysophosphatidic acid secretion from ovarian and cervical cancer cells but not from breast or leukemia cells","volume":"71","author":"Shen","year":"1998","journal-title":"Gynecol. Oncol."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Woclawek-Potocka, I., Brzezicka, E., and Skarzynski, D.J. (2009). Lysophosphatic acid modulates prostaglandin secretion in the bovine endometrial cells differently on days 8-10 of the estrous cycle and early pregnancy. J. Reprod. Dev.","DOI":"10.1262\/jrd.20206"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1963","DOI":"10.1194\/jlr.M300188-JLR200","article-title":"Role of phospholipase D in agonist-stimulated lysophosphatidic acid synthesis by ovarian cancer cells","volume":"44","author":"Luquain","year":"2003","journal-title":"J. Lipid Res."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"661","DOI":"10.1262\/jrd.2012-060","article-title":"Lysophosphatidic acid action in the bovine corpus luteum\u2014An in vitro study","volume":"58","author":"Boruszewska","year":"2012","journal-title":"J. Reprod. Dev."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1007\/s00428-007-0425-4","article-title":"Submucosal connective tissue-type mast cells contribute to the production of lysophosphatidic acid (LPA) in the gastrointestinal tract through the secretion of autotaxin (ATX)\/lysophospholipase D (lysoPLD)","volume":"451","author":"Mori","year":"2007","journal-title":"Virchows Arch."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"919","DOI":"10.1016\/0092-8674(95)90295-3","article-title":"Secretory phospholipase A2 generates the novel lipid mediator lysophosphatidic acid in membrane microvesicles shed from activated cells","volume":"80","author":"Fourcade","year":"1995","journal-title":"Cell"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1006\/dbio.2000.9930","article-title":"Lysophosphatidic acid (LPA) is a novel extracellular regulator of cortical neuroblast morphology","volume":"228","author":"Fukushima","year":"2000","journal-title":"Dev. Biol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"104","DOI":"10.1095\/biolreprod.115.137174","article-title":"Lysophosphatidic acid (LPA) receptor 3-mediated LPA signal transduction pathways: A possible relationship with early development of peri-implantation porcine conceptus","volume":"94","author":"Jeong","year":"2016","journal-title":"Biol. Reprod."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1095\/biolreprod.112.099564","article-title":"Analysis of the lysophosphatidic acid-generating enzyme ENPP2 in the uterus during pregnancy in pigs","volume":"87","author":"Seo","year":"2012","journal-title":"Biol. Reprod."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Aoki, J., and Yukiura, H. (2015). Zebrafish as a Model. Animal for Studying Lysophosphatidic Acid Signaling. Bioactive Lipid Mediators, Springer.","DOI":"10.1007\/978-4-431-55669-5_14"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"953","DOI":"10.1016\/j.tips.2018.08.006","article-title":"\u2019Crystal\u2019 Clear? Lysohphospholipid Receptor Structure Insights and Controversies","volume":"39","author":"Blaho","year":"2018","journal-title":"Trends Pharmacol. Sci."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1192","DOI":"10.1194\/jlr.R046458","article-title":"LPA receptor signaling: Pharmacology, physiology, and pathophysiology","volume":"55","author":"Yung","year":"2014","journal-title":"J. Lipid Res."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"27776","DOI":"10.1074\/jbc.274.39.27776","article-title":"Molecular cloning and characterization of a novel human G-protein-coupled receptor, EDG7, for lysophosphatidic acid","volume":"274","author":"Bandoh","year":"1999","journal-title":"J. Biol. Chem."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"4439","DOI":"10.1242\/dev.081745","article-title":"Autotaxin\/Lpar3 signaling regulates Kupffer\u2019s vesicle formation and left-right asymmetry in zebrafish","volume":"139","author":"Lai","year":"2012","journal-title":"Development"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"216","DOI":"10.1089\/scd.2017.0190","article-title":"Activation of Lysophosphatidic Acid Receptor 3 Inhibits Megakaryopoiesis in Human Hematopoietic Stem Cells and Zebrafish","volume":"27","author":"Lin","year":"2018","journal-title":"Stem Cells Dev."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"705.5","DOI":"10.1096\/fasebj.2019.33.1_supplement.705.5","article-title":"Histological Analysis of Lysophosphatidic Acid Receptor 3 Deficient Zebrafish","volume":"33","author":"Chen","year":"2019","journal-title":"FASEB J."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1016\/j.mcn.2012.03.006","article-title":"Lysophosphatidic acid induces neurite branch formation through LPA3","volume":"50","author":"Furuta","year":"2012","journal-title":"Mol. Cell. Neurosci."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Ramesh, S., Govindarajulu, M., Suppiramaniam, V., Moore, T., and Dhanasekaran, M. (2018). Autotaxin\u2013Lysophosphatidic Acid Signaling in Alzheimer\u2019s Disease. Int. J. Mol. Sci., 19.","DOI":"10.3390\/ijms19071827"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"182","DOI":"10.1016\/S0006-8993(03)03527-3","article-title":"Pharmacological characterization of lysophospholipid receptor signal transduction pathways in rat cerebrocortical astrocytes","volume":"990","author":"Rao","year":"2003","journal-title":"Brain Res."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1199","DOI":"10.1124\/mol.64.5.1199","article-title":"Common signaling pathways link activation of murine PAR-1, LPA, and S1P receptors to proliferation of astrocytes","volume":"64","author":"Sorensen","year":"2003","journal-title":"Mol. Pharmacol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1073","DOI":"10.1046\/j.1471-4159.1997.69031073.x","article-title":"Lysophosphatidic acid-induced proliferation-related signals in astrocytes","volume":"69","author":"Keller","year":"1997","journal-title":"J. Neurochem."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"2300","DOI":"10.1046\/j.1471-4159.1996.67062300.x","article-title":"Lysophosphatidic acid decreases glutamate and glucose uptake by astrocytes","volume":"67","author":"Keller","year":"1996","journal-title":"J. Neurochem."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"573","DOI":"10.1023\/A:1007542532395","article-title":"Expression of lysophosphatidic acid receptor in rat astrocytes: Mitogenic effect and expression of neurotrophic genes","volume":"25","author":"Tabuchi","year":"2000","journal-title":"Neurochem. Res."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1009","DOI":"10.1111\/j.1601-183X.2012.00840.x","article-title":"LPA5 receptor plays a role in pain sensitivity, emotional exploration and reversal learning","volume":"11","author":"Leo","year":"2012","journal-title":"Genes Brain Behav."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"772","DOI":"10.1111\/j.1601-183X.2009.00524.x","article-title":"Behavioral phenotype of maLPA1-null mice: Increased anxiety-like behavior and spatial memory deficits","volume":"8","author":"Santin","year":"2009","journal-title":"Genes Brain Behav."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1007\/s00213-011-2446-6","article-title":"Attenuation of cocaine-induced conditioned locomotion is associated with altered expression of hippocampal glutamate receptors in mice lacking LPA1 receptors","volume":"220","author":"Blanco","year":"2012","journal-title":"Psychopharmacology"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/j.nlm.2010.04.003","article-title":"Exploratory, anxiety and spatial memory impairments are dissociated in mice lacking the LPA1 receptor","volume":"94","author":"Chun","year":"2010","journal-title":"Neurobiol. Learn. Mem."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"13384","DOI":"10.1073\/pnas.97.24.13384","article-title":"Requirement for the lpA1 lysophosphatidic acid receptor gene in normal suckling behavior","volume":"97","author":"Contos","year":"2000","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Chen, W.M., Chiang, J.C., Lin, Y.C., Lin, Y.N., Chuang, P.Y., Chang, Y.C., Chen, C.C., Wu, K.Y., Hsieh, J.C., and Chen, S.K. (2019). Lysophosphatidic acid receptor LPA3 prevents oxidative stress and cellular senescence in Hutchinson\u2013Gilford progeria syndrome. Aging Cell, e13064.","DOI":"10.1111\/acel.13064"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1016\/j.jneumeth.2015.07.023","article-title":"A novel 3D method of locomotor analysis in adult zebrafish: Implications for automated detection of CNS drug-evoked phenotypes","volume":"255","author":"Stewart","year":"2015","journal-title":"J. Neurosci. Methods"},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Audira, G., Sampurna, B.P., Juniardi, S., Liang, S.T., Lai, Y.H., and Hsiao, C.D. (2018). A simple setup to perform 3D locomotion tracking in zebrafish by using a single camera. Inventions, 3.","DOI":"10.3390\/inventions3010011"},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Audira, G., Sampurna, B.P., Juniardi, S., Liang, S.T., Lai, Y.H., and Hsiao, C.D. (2018). A versatile setup for measuring multiple behavior endpoints in zebrafish. Inventions, 3.","DOI":"10.3390\/inventions3040075"},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Pham, M., Raymond, J., Hester, J., Kyzar, E., Gaikwad, S., Bruce, I., Fryar, C., Chanin, S., Enriquez, J., and Bagawandoss, S. (2012). Assessing social behavior phenotypes in adult zebrafish: Shoaling, social preference, and mirror biting tests. Zebrafish Protocols for Neurobehavioral Research, Springer.","DOI":"10.1007\/978-1-61779-597-8_17"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"bio041871","DOI":"10.1242\/bio.041871","article-title":"Establishing simple image-based methods and cost-effective instrument for toxicity assessment on circadian rhythm dysregulation in fish","volume":"8","author":"Audira","year":"2019","journal-title":"Biol. Open"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1159\/000364858","article-title":"Universal GFP Reporter for the Study of Vascular Development","volume":"36","author":"Fincher","year":"2014","journal-title":"Dev. Neurosci."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"459","DOI":"10.3233\/JAD-2011-110704","article-title":"Evaluation of color preference in zebrafish for learning and memory","volume":"28","author":"Avdesh","year":"2012","journal-title":"J. Alzheimer\u2019s Dis."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1016\/j.cbpc.2017.01.004","article-title":"A colour preference technique to evaluate acrylamide-induced toxicity in zebrafish","volume":"199","author":"Jia","year":"2017","journal-title":"Comp. Biochem. Physiol. Part C Toxicol. Pharmacol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1502","DOI":"10.1002\/jat.3169","article-title":"Directional and color preference in adult zebrafish: Implications in behavioral and learning assays in neurotoxicology studies","volume":"35","author":"Bault","year":"2015","journal-title":"J. Appl. Toxicol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"330","DOI":"10.1089\/zeb.2015.1150","article-title":"Color. preference in Danio rerio: Effects of age and anxiolytic treatments","volume":"13","author":"Peeters","year":"2016","journal-title":"Zebrafish"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"750","DOI":"10.14348\/molcells.2016.0173","article-title":"Innate color preference of zebrafish and its use in behavioral analyses","volume":"39","author":"Park","year":"2016","journal-title":"Mol. Cells"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"582","DOI":"10.1111\/j.1439-0310.2008.01515.x","article-title":"Innate and learned colour preference in the zebrafish, Danio rerio","volume":"114","author":"Spence","year":"2008","journal-title":"Ethology"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"166","DOI":"10.1089\/zeb.2014.1019","article-title":"The zebrafish world of colors and shapes: Preference and discrimination","volume":"12","author":"Oliveira","year":"2015","journal-title":"Zebrafish"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1186\/s12993-018-0145-8","article-title":"Reversal of reserpine-induced depression and cognitive disorder in zebrafish by sertraline and Traditional Chinese Medicine (TCM)","volume":"14","author":"Zhang","year":"2018","journal-title":"Behav. Brain Funct."},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Liang, S.T., Audira, G., Juniardi, S., Chen, J.R., Lai, Y.H., Du, Z.C., Lin, D.S., and Hsiao, C.D. (2019). Zebrafish Carrying pycr1 Gene Deficiency Display Aging and Multiple Behavioral Abnormalities. Cells, 8.","DOI":"10.3390\/cells8050453"},{"key":"ref_53","doi-asserted-by":"crossref","unstructured":"Audira, G., Sarasamma, S., Chen, J.R., Juniardi, S., Sampurna, B.P., Liang, S.T., Lai, Y.H., Lin, G.M., Hsieh, M.C., and Hsiao, C.D. (2018). Zebrafish Mutants Carrying Leptin a (lepa) Gene Deficiency Display Obesity, Anxiety, Less Aggression and Fear, and Circadian Rhythm and Color. Preference Dysregulation. Int. J. Mol. Sci., 19.","DOI":"10.3390\/ijms19124038"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1016\/j.prostaglandins.2009.02.002","article-title":"Lysophosphatidic acid (LPA) receptors: Signaling properties and disease relevance","volume":"91","author":"Lin","year":"2010","journal-title":"Prostaglandins Other Lipid Mediat."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"1763","DOI":"10.1002\/stem.733","article-title":"Lysophosphatidic acid induces erythropoiesis through activating lysophosphatidic acid receptor 3","volume":"29","author":"Chiang","year":"2011","journal-title":"Stem Cells"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"104","DOI":"10.1038\/nature03505","article-title":"LPA3-mediated lysophosphatidic acid signalling in embryo implantation and spacing","volume":"435","author":"Ye","year":"2005","journal-title":"Nature"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"1193","DOI":"10.1189\/jlb.0407221","article-title":"LPA3 receptor mediates chemotaxis of immature murine dendritic cells to unsaturated lysophosphatidic acid (LPA)","volume":"82","author":"Chan","year":"2007","journal-title":"J. Leukoc. Biol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1016\/j.yexcr.2017.02.007","article-title":"Lysophosphatidic acid signaling via LPA1 and LPA3 regulates cellular functions during tumor progression in pancreatic cancer cells","volume":"352","author":"Fukushima","year":"2017","journal-title":"Exp. Cell Res."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"487","DOI":"10.1007\/s00702-014-1289-9","article-title":"Lysophosphatidic acid induces anxiety-like behavior via its receptors in mice","volume":"122","author":"Yamada","year":"2015","journal-title":"J. Neural Transm."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1016\/j.neuint.2016.10.006","article-title":"Effects of gintonin-enriched fraction on hippocampal cell proliferation in wild-type mice and an APPswe\/PSEN-1 double Tg mouse model of Alzheimer\u2019s disease","volume":"101","author":"Kim","year":"2016","journal-title":"Neurochem. Int."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"669","DOI":"10.1016\/j.neuron.2015.01.009","article-title":"Lysophosphatidic acid signaling in the nervous system","volume":"85","author":"Yung","year":"2015","journal-title":"Neuron"},{"key":"ref_62","first-page":"20","article-title":"Lysophospholipids and their receptors in the central nervous system","volume":"1831","author":"Choi","year":"2013","journal-title":"Biochim. Biophys. Acta (BBA)-Mol. Cell Biol. Lipids"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1038\/mp.2014.128","article-title":"Molecular psychiatry of zebrafish","volume":"20","author":"Stewart","year":"2015","journal-title":"Mol. Psychiatry"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"342","DOI":"10.1002\/cne.1390","article-title":"Comparative anatomy of the histaminergic and other aminergic systems in zebrafish (Danio rerio)","volume":"440","author":"Kaslin","year":"2001","journal-title":"J. Comp. Neurol."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"3827","DOI":"10.1002\/cne.23126","article-title":"Organization of the histaminergic system in adult zebrafish (Danio rerio) brain: Neuron number, location, and cotransmitters","volume":"520","author":"Sundvik","year":"2012","journal-title":"J. Comp. Neurol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"359","DOI":"10.1089\/zeb.2010.0669","article-title":"A review of monoaminergic neuropsychopharmacology in zebrafish","volume":"7","author":"Maximino","year":"2010","journal-title":"Zebrafish"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"692","DOI":"10.1097\/00005053-199412000-00003","article-title":"Molecular psychiatry. Adaptations of receptor-coupled signal transduction pathways underlying stress-and drug-induced neural plasticity","volume":"182","author":"Duman","year":"1994","journal-title":"J. Nerv. Ment. Dis."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1186\/2049-9256-1-3","article-title":"The origins of molecular psychiatry","volume":"1","author":"Nestler","year":"2013","journal-title":"J. Mol. Psychiatry"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1016\/j.tips.2013.12.002","article-title":"Zebrafish as an emerging model for studying complex brain disorders","volume":"35","author":"Kalueff","year":"2014","journal-title":"Trends Pharmacol. Sci."},{"key":"ref_70","first-page":"19","article-title":"Gender Differences in Cerebellar Metabolism Test.-Retest Reproducibility","volume":"154","author":"Volkow","year":"1997","journal-title":"Am. J. Psychiatry"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1016\/j.bbr.2016.06.047","article-title":"Sexual dimorphisms in swimming behavior, cerebral metabolic activity and adrenoceptors in adult zebrafish (Danio rerio)","volume":"312","author":"Ampatzis","year":"2016","journal-title":"Behav. Brain Res."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"207","DOI":"10.3758\/BF03328355","article-title":"Norepinephrine elicitation of aggressive display responses in Betta splendens","volume":"5","author":"Marrone","year":"1966","journal-title":"Psychon. Sci."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1016\/0165-0173(81)90005-9","article-title":"Behavioral depression produced by an uncontrollable stressor: Relationship to norepinephrine, dopamine, and serotonin levels in various regions of rat brain","volume":"3","author":"Weiss","year":"1981","journal-title":"Brain Res. Rev."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"8451","DOI":"10.1523\/JNEUROSCI.17-21-08451.1997","article-title":"Reduced levels of norepinephrine transporters in the locus coeruleus in major depression","volume":"17","author":"Klimek","year":"1997","journal-title":"J. Neurosci."},{"key":"ref_75","unstructured":"Pasnik, D., Evans, J., and Klesius, P. (2010). Stress in fish. Fundamentals of Ornamental Fish, Wiley\u2013Blackwell Publishing. [1st ed.]."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"369","DOI":"10.1016\/j.aquatox.2004.03.016","article-title":"The effects of environmental pollutants on complex fish behaviour: Integrating behavioural and physiological indicators of toxicity","volume":"68","author":"Scott","year":"2004","journal-title":"Aquat. Toxicol."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"517","DOI":"10.1093\/icb\/42.3.517","article-title":"Stress in fishes: A diversity of responses with particular reference to changes in circulating corticosteroids","volume":"42","author":"Barton","year":"2002","journal-title":"Integr. Comp. Biol."},{"key":"ref_78","doi-asserted-by":"crossref","unstructured":"Yu, L., Tucci, V., Kishi, S., and Zhdanova, I.V. (2006). Cognitive aging in zebrafish. PLoS ONE, 1.","DOI":"10.1371\/journal.pone.0000014"},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1016\/j.bbr.2014.08.033","article-title":"Hyperglycemia induces memory impairment linked to increased acetylcholinesterase activity in zebrafish (Danio rerio)","volume":"274","author":"Capiotti","year":"2014","journal-title":"Behav. Brain Res."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1007\/s11940-003-0013-0","article-title":"Melatonin, circadian rhythms, and sleep","volume":"5","author":"Zhdanova","year":"2003","journal-title":"Curr. Treat. Options Neurol."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1016\/0006-8993(95)01365-2","article-title":"Circadian regulation of melatonin production in cultured zebrafish pineal and retina","volume":"708","author":"Cahill","year":"1996","journal-title":"Brain Res."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"469","DOI":"10.1016\/j.ygcen.2009.04.026","article-title":"Current knowledge on the melatonin system in teleost fish","volume":"165","author":"Falcon","year":"2010","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"344","DOI":"10.1016\/j.aquatox.2015.09.011","article-title":"Age matters: Developmental stage of Danio rerio larvae influences photomotor response thresholds to diazinion or diphenhydramine","volume":"170","author":"Kristofco","year":"2016","journal-title":"Aquat. Toxicol."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"743","DOI":"10.1038\/nmeth.2994","article-title":"idTracker: Tracking individuals in a group by automatic identification of unmarked animals","volume":"11","author":"Hinz","year":"2014","journal-title":"Nat. Methods"},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"W566","DOI":"10.1093\/nar\/gkv468","article-title":"ClustVis: A web tool for visualizing clustering of multivariate data using Principal Component Analysis and heatmap","volume":"43","author":"Metsalu","year":"2015","journal-title":"Nucleic Acids Res."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/21\/8\/2837\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,13]],"date-time":"2025-10-13T13:45:06Z","timestamp":1760363106000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/21\/8\/2837"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,4,18]]},"references-count":85,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2020,4]]}},"alternative-id":["ijms21082837"],"URL":"https:\/\/doi.org\/10.3390\/ijms21082837","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,4,18]]}}}