{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,7]],"date-time":"2026-10-07T22:48:52Z","timestamp":1791413332875,"version":"4.3.3"},"reference-count":95,"publisher":"Wiley","issue":"4","license":[{"start":{"date-parts":[[2014,8,1]],"date-time":"2014-08-01T00:00:00Z","timestamp":1406851200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Developmental Neurobiology"],"published-print":{"date-parts":[[2015,4]]},"abstract":"<jats:title>ABSTRACT<\/jats:title><jats:p>In the developing brain, immature neurons migrate from their sites of origin to their final destination, where they reside for the rest of their lives. This active movement of immature neurons is essential for the formation of normal neuronal cytoarchitecture and proper differentiation. Deficits in migration result in the abnormal development of the brain, leading to a variety of neurological disorders. A myriad of extracellular guidance molecules and intracellular effector molecules is involved in controlling the migration of immature neurons in a cell type, cortical layer and birth\u2010date\u2010specific manner. To date, little is known about how extracellular guidance molecules transfer their information to the intracellular effector molecules, which regulate the migration of immature neurons. In this article, to fill the gap between extracellular guidance molecules and intracellular effector molecules, using the migration of cerebellar granule cells as a model system of neuronal cell migration, we explore the role of second messenger signaling (specifically Ca<jats:sup>2+<\/jats:sup> and cyclic nucleotide signaling) in the regulation of neuronal cell migration. We will, first, describe the cortical layer\u2010specific changes in granule cell migration. Second, we will discuss the roles of Ca<jats:sup>2+<\/jats:sup> and cyclic nucleotide signaling in controlling granule cell migration. Third, we will present recent studies showing the roles of Ca<jats:sup>2+<\/jats:sup> and cyclic nucleotide signaling in the deficits in granule cell migration in mouse models of fetal alcohol spectrum disorders and fetal Minamata disease. \u00a9 2014 Wiley Periodicals, Inc. Develop Neurobiol 75: 369\u2013387, 2015<\/jats:p>","DOI":"10.1002\/dneu.22219","type":"journal-article","created":{"date-parts":[[2014,7,28]],"date-time":"2014-07-28T09:10:09Z","timestamp":1406538609000},"page":"369-387","source":"Crossref","is-referenced-by-count":23,"title":["The role of calcium and cyclic nucleotide signaling in cerebellar granule cell migration under normal and pathological conditions"],"prefix":"10.1002","volume":"75","author":[{"given":"Yutaro","family":"Komuro","sequence":"first","affiliation":[{"name":"Department of Neurosciences Lerner Research Institute, Cleveland Clinic Foundation  Cleveland Ohio 44195"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ludovic","family":"Galas","sequence":"additional","affiliation":[{"name":"INSERM, PRIMACEN, Cell Imaging Platform of Normandy 76821 Mont\u2010Saint\u2010Aignan France"},{"name":"University of Rouen Institute for Research and Innovation in Biomedicine (IRIB)  Rouen France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alexis","family":"Lebon","sequence":"additional","affiliation":[{"name":"INSERM, PRIMACEN, Cell Imaging Platform of Normandy 76821 Mont\u2010Saint\u2010Aignan France"},{"name":"University of Rouen Institute for Research and Innovation in Biomedicine (IRIB)  Rouen France"},{"name":"INSERM, U982, DC2N 76821 Mont\u2010Saint\u2010Aignan France"},{"name":"International Associated laboratory Samuel de Champlain, INSERM\u2010INRS  France Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Emilie","family":"Raoult","sequence":"additional","affiliation":[{"name":"INSERM, PRIMACEN, Cell Imaging Platform of Normandy 76821 Mont\u2010Saint\u2010Aignan France"},{"name":"University of Rouen Institute for Research and Innovation in Biomedicine (IRIB)  Rouen France"},{"name":"INSERM, U982, DC2N 76821 Mont\u2010Saint\u2010Aignan France"},{"name":"International Associated laboratory Samuel de Champlain, INSERM\u2010INRS  France Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jennifer K.","family":"Fahrion","sequence":"additional","affiliation":[{"name":"Department of Neurosciences Lerner Research Institute, Cleveland Clinic Foundation  Cleveland Ohio 44195"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Amanda","family":"Tilot","sequence":"additional","affiliation":[{"name":"Department of Neurosciences Lerner Research Institute, Cleveland Clinic Foundation  Cleveland Ohio 44195"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tasturo","family":"Kumada","sequence":"additional","affiliation":[{"name":"Department of Occupational Therapy Tokoha University  Hamamatsu 431\u20102102 Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nobuhiko","family":"Ohno","sequence":"additional","affiliation":[{"name":"Department of Anatomy and Molecular Histology Interdisciplinary Graduate school of Medicine and Engineering University of Yamanashi  Yamanashi 409\u20103898 Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David","family":"Vaudry","sequence":"additional","affiliation":[{"name":"INSERM, PRIMACEN, Cell Imaging Platform of Normandy 76821 Mont\u2010Saint\u2010Aignan France"},{"name":"University of Rouen Institute for Research and Innovation in Biomedicine (IRIB)  Rouen France"},{"name":"INSERM, U982, DC2N 76821 Mont\u2010Saint\u2010Aignan France"},{"name":"International Associated laboratory Samuel de Champlain, INSERM\u2010INRS  France Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hitoshi","family":"Komuro","sequence":"additional","affiliation":[{"name":"Department of Neurosciences Lerner Research Institute, Cleveland Clinic Foundation  Cleveland Ohio 44195"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2014,8]]},"reference":[{"key":"e_1_2_6_2_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0022-3476(74)80291-X"},{"key":"e_1_2_6_3_1","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.1999-04.2004"},{"key":"e_1_2_6_4_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuron.2009.01.034"},{"key":"e_1_2_6_5_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.peptides.2007.04.013"},{"key":"e_1_2_6_6_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuroscience.2007.02.025"},{"key":"e_1_2_6_7_1","doi-asserted-by":"publisher","DOI":"10.1007\/s12311-009-0121-9"},{"key":"e_1_2_6_8_1","doi-asserted-by":"publisher","DOI":"10.1016\/S1054-3589(08)60011-3"},{"key":"e_1_2_6_9_1","first-page":"591","article-title":"Methylmercury poisoning of the developing nervous system: I. Pattern of neuronal migration in the cerebral cortex","volume":"7","author":"Choi BH","year":"1986","journal-title":"Neurotoxicol"},{"key":"e_1_2_6_10_1","doi-asserted-by":"publisher","DOI":"10.1097\/00005072-197811000-00001"},{"key":"e_1_2_6_11_1","doi-asserted-by":"publisher","DOI":"10.3109\/10408369708998098"},{"key":"e_1_2_6_12_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0022-3476(78)80072-9"},{"key":"e_1_2_6_13_1","first-page":"359","article-title":"Fetal Alcohol Spectrum Disorder (FASD): Neurobehavioral profile, indications for diagnosis and treatment","volume":"48","author":"Coriale G","year":"2013","journal-title":"Riv Psichiatr"},{"key":"e_1_2_6_14_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.taap.2003.11.032"},{"key":"e_1_2_6_15_1","first-page":"209","article-title":"Environmental medicine. Part 3. Long\u2010term effects of chronic low\u2010dose mercury exposure","volume":"5","author":"Crinnion WJ","year":"2000","journal-title":"Altern Med Rev"},{"key":"e_1_2_6_16_1","doi-asserted-by":"publisher","DOI":"10.1177\/15353702-0323006-06"},{"key":"e_1_2_6_17_1","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.5333-08.2009"},{"key":"e_1_2_6_18_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.devbrainres.2004.11.005"},{"key":"e_1_2_6_19_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.jns.2007.06.036"},{"key":"e_1_2_6_20_1","doi-asserted-by":"publisher","DOI":"10.1177\/019262339702500612"},{"key":"e_1_2_6_21_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF03159968"},{"key":"e_1_2_6_22_1","doi-asserted-by":"publisher","DOI":"10.1146\/annurev-cellbio-101512-122400"},{"key":"e_1_2_6_23_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1120747109"},{"key":"e_1_2_6_24_1","doi-asserted-by":"publisher","DOI":"10.1016\/B978-0-12-397265-1.00042-3"},{"key":"e_1_2_6_25_1","doi-asserted-by":"publisher","DOI":"10.1002\/9783527633968.ch13"},{"key":"e_1_2_6_26_1","doi-asserted-by":"publisher","DOI":"10.1038\/368335a0"},{"key":"e_1_2_6_27_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuron.2012.02.035"},{"key":"e_1_2_6_28_1","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.140.1.131"},{"key":"e_1_2_6_29_1","doi-asserted-by":"publisher","DOI":"10.1242\/dev.00612"},{"key":"e_1_2_6_30_1","first-page":"426","article-title":"Neuropsychiatric disturbances due to organic mercury poisoning during the prenatal period","volume":"66","author":"Harada M","year":"1964","journal-title":"Psychiatr Neurol Jpn"},{"key":"e_1_2_6_31_1","doi-asserted-by":"publisher","DOI":"10.1002\/tera.1420180216"},{"key":"e_1_2_6_32_1","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.0240-10.2010"},{"key":"e_1_2_6_33_1","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.3758-12.2013"},{"key":"e_1_2_6_34_1","doi-asserted-by":"publisher","DOI":"10.1159\/000109847"},{"key":"e_1_2_6_35_1","doi-asserted-by":"crossref","first-page":"409","DOI":"10.1007\/s00401-002-0571-3","article-title":"Neuronal migration disturbance and consequent cytoarchitecture in the cerebral cortex following transplacental administration of methylmercury","volume":"104","author":"Kakita A","year":"2002","journal-title":"Acta Neuropathol"},{"key":"e_1_2_6_36_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.ceca.2005.01.006"},{"key":"e_1_2_6_37_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.1323145"},{"key":"e_1_2_6_38_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.8096653"},{"key":"e_1_2_6_39_1","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.15-02-01110.1995"},{"key":"e_1_2_6_40_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0896-6273(00)80159-2"},{"key":"e_1_2_6_41_1","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.18-04-01478.1998"},{"key":"e_1_2_6_42_1","doi-asserted-by":"publisher","DOI":"10.1002\/(SICI)1097-4695(199810)37:1<110::AID-NEU9>3.0.CO;2-C"},{"key":"e_1_2_6_43_1","first-page":"57","volume-title":"The Neuron in Tissue Culture","author":"Komuro H","year":"1999"},{"key":"e_1_2_6_44_1","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1523\/JNEUROSCI.21-02-00527.2001","article-title":"Mode and tempo of tangential cell migration in the cerebellar external granular layer","volume":"21","author":"Komuro H","year":"2001","journal-title":"J Neurosci"},{"key":"e_1_2_6_45_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00018-003-2248-z"},{"key":"e_1_2_6_46_1","first-page":"107","volume-title":"Handbook of the Cerebellum and Cerebellar Disorders","author":"Komuro Y","year":"2012"},{"key":"e_1_2_6_47_1","doi-asserted-by":"publisher","DOI":"10.1016\/B978-0-12-397266-8.00030-2"},{"key":"e_1_2_6_48_1","doi-asserted-by":"publisher","DOI":"10.1016\/0006-8993(79)90785-6"},{"key":"e_1_2_6_49_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0401000101"},{"key":"e_1_2_6_50_1","doi-asserted-by":"publisher","DOI":"10.1002\/jnr.21149"},{"key":"e_1_2_6_51_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.ydbio.2008.11.012"},{"key":"e_1_2_6_52_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuroscience.2010.07.059"},{"key":"e_1_2_6_53_1","doi-asserted-by":"publisher","DOI":"10.1007\/978-0-387-92271-3_182"},{"key":"e_1_2_6_54_1","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.4478-05.2006"},{"key":"e_1_2_6_55_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0304-3940(97)00273-5"},{"key":"e_1_2_6_56_1","first-page":"689","article-title":"An analysis of autopy brain tissue from infants prenatally exposed to methylmercury","volume":"16","author":"Lapham LW","year":"1995","journal-title":"Neurotoxicology"},{"key":"e_1_2_6_57_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1111326109"},{"key":"e_1_2_6_58_1","doi-asserted-by":"publisher","DOI":"10.1055\/s-2008-1052471"},{"key":"e_1_2_6_59_1","doi-asserted-by":"publisher","DOI":"10.1006\/taap.1997.8262"},{"key":"e_1_2_6_60_1","doi-asserted-by":"publisher","DOI":"10.1016\/0014-4886(61)90055-3"},{"key":"e_1_2_6_61_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.3749878"},{"key":"e_1_2_6_62_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1530-0277.1993.tb00768.x"},{"key":"e_1_2_6_63_1","doi-asserted-by":"publisher","DOI":"10.1097\/00005072-196510000-00002"},{"key":"e_1_2_6_64_1","doi-asserted-by":"publisher","DOI":"10.1016\/0896-6273(94)90210-0"},{"key":"e_1_2_6_65_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.0953-816X.2004.03118.x"},{"key":"e_1_2_6_66_1","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.3071-09.2009"},{"key":"e_1_2_6_67_1","doi-asserted-by":"publisher","DOI":"10.1620\/tjem.196.89"},{"key":"e_1_2_6_68_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1100247108"},{"key":"e_1_2_6_69_1","doi-asserted-by":"publisher","DOI":"10.1038\/nature01751"},{"key":"e_1_2_6_70_1","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.200503157"},{"key":"e_1_2_6_71_1","doi-asserted-by":"publisher","DOI":"10.1177\/0883073811428376"},{"key":"e_1_2_6_72_1","first-page":"125","article-title":"Alcohol embryo\u2010 and fetopathy. Neuropathology of 3 children and 3 fetuses","volume":"41","author":"Peiffer J","year":"1979","journal-title":"J Neurosci Sci"},{"key":"e_1_2_6_73_1","doi-asserted-by":"publisher","DOI":"10.1016\/S1352-2310(01)00101-7"},{"key":"e_1_2_6_74_1","doi-asserted-by":"publisher","DOI":"10.1002\/cne.901410303"},{"key":"e_1_2_6_75_1","doi-asserted-by":"publisher","DOI":"10.1016\/0959-4388(94)90033-7"},{"key":"e_1_2_6_76_1","doi-asserted-by":"publisher","DOI":"10.1002\/neu.480260303"},{"key":"e_1_2_6_77_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1471-4159.2011.07486.x"},{"key":"e_1_2_6_78_1","doi-asserted-by":"publisher","DOI":"10.1111\/jnc.12714"},{"key":"e_1_2_6_79_1","doi-asserted-by":"publisher","DOI":"10.1177\/15353702-0323006-03"},{"key":"e_1_2_6_80_1","doi-asserted-by":"publisher","DOI":"10.1007\/s11065-011-9166-x"},{"key":"e_1_2_6_81_1","doi-asserted-by":"publisher","DOI":"10.1016\/0028-3908(93)90018-X"},{"key":"e_1_2_6_82_1","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1007\/s004010000345","article-title":"Abnormalities of cerebellar foliation in rats prenatally exposed to ethanol","volume":"102","author":"Sakata\u2010Haga H","year":"2001","journal-title":"Acta Neuropathol"},{"key":"e_1_2_6_83_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.tins.2007.11.009"},{"key":"e_1_2_6_84_1","doi-asserted-by":"publisher","DOI":"10.1186\/1478-811X-11-94"},{"key":"e_1_2_6_85_1","doi-asserted-by":"publisher","DOI":"10.1006\/taap.2000.8967"},{"key":"e_1_2_6_86_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.281.5382.1515"},{"key":"e_1_2_6_87_1","doi-asserted-by":"publisher","DOI":"10.1056\/NEJM197105062841806"},{"key":"e_1_2_6_88_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF00685743"},{"key":"e_1_2_6_89_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0197-0186(99)00050-9"},{"key":"e_1_2_6_90_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.adnc.2005.04.007"},{"key":"e_1_2_6_91_1","doi-asserted-by":"publisher","DOI":"10.1038\/415077a"},{"key":"e_1_2_6_92_1","doi-asserted-by":"crossref","first-page":"5966","DOI":"10.1523\/JNEUROSCI.22-14-05966.2002","article-title":"Intrinsic program for migration of cerebellar granule cells in vitro","volume":"22","author":"Yacubova E","year":"2002","journal-title":"J Neurosci"},{"key":"e_1_2_6_93_1","doi-asserted-by":"publisher","DOI":"10.1385\/CBB:37:3:213"},{"key":"e_1_2_6_94_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.conb.2009.12.003"},{"key":"e_1_2_6_95_1","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.cellbio.23.090506.123221"},{"key":"e_1_2_6_96_1","doi-asserted-by":"publisher","DOI":"10.1002\/dneu.22041"}],"container-title":["Developmental Neurobiology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.wiley.com\/onlinelibrary\/tdm\/v1\/articles\/10.1002%2Fdneu.22219","content-type":"unspecified","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/dneu.22219","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,9,11]],"date-time":"2023-09-11T03:39:30Z","timestamp":1694403570000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1002\/dneu.22219"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2014,8]]},"references-count":95,"journal-issue":{"issue":"4","published-print":{"date-parts":[[2015,4]]}},"alternative-id":["10.1002\/dneu.22219"],"URL":"https:\/\/doi.org\/10.1002\/dneu.22219","archive":["Portico"],"relation":{},"ISSN":["1932-8451","1932-846X"],"issn-type":[{"value":"1932-8451","type":"print"},{"value":"1932-846X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2014,8]]}}}