{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,12]],"date-time":"2025-10-12T01:59:08Z","timestamp":1760234348188,"version":"build-2065373602"},"reference-count":51,"publisher":"MDPI AG","issue":"10","license":[{"start":{"date-parts":[[2021,5,12]],"date-time":"2021-05-12T00:00:00Z","timestamp":1620777600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>The multiple functions of the wild type Huntington\u2019s disease protein of the sea urchin Hemicentrotus pulcherrimus (Hp-Htt) have been examined using the anti-Hp-Htt antibody (Ab) raised against synthetic oligopeptides. According to immunoblotting, Hp-Htt was detected as a single band at around the 350 kDa region at the swimming blastula stage to the prism larva stage. From the 2-arm pluteus stage (2aPL), however, an additional smaller band at the 165 kDa region appeared. Immunohistochemically, Hp-Htt was detected in the nuclei and the nearby cytoplasm of the ectodermal cells from the swimming blastula stage, and the blastocoelar cells from the mid-gastrula stage. The Ab-positive signal was converged to the ciliary band-associated strand (CBAS). There, it was accompanied by several CBAS-marker proteins in the cytoplasm, such as glutamate decarboxylase. Application of Hp-Htt morpholino (Hp-Htt-MO) has resulted in shortened larval arms, accompanied by decreased 5-bromo-2-deoxyuridin (BrdU) incorporation by the ectodermal cells of the larval arms. Hp-Htt-MO also resulted in lowered ciliary beating activity, accompanied by a disordered swirling pattern formation around the body. These Hp-Htt-MO-induced deficiencies took place after the onset of CBAS system formation at the larval arms. Thus, Hp-Htt is involved in cell proliferation and the ciliary beating pattern regulation signaling system in pluteus larvae.<\/jats:p>","DOI":"10.3390\/ijms22105116","type":"journal-article","created":{"date-parts":[[2021,5,12]],"date-time":"2021-05-12T10:59:12Z","timestamp":1620817152000},"page":"5116","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["Involvement of Huntingtin in Development and Ciliary Beating Regulation of Larvae of the Sea Urchin, Hemicentrotus pulcherrimus"],"prefix":"10.3390","volume":"22","author":[{"given":"Hideki","family":"Katow","sequence":"first","affiliation":[{"name":"Institute of Development, Aging and Cancer, Tohoku University, Sendai 980-8575, Japan"},{"name":"Research Center for Marine Biology, Tohoku University, Aomori 039-3501, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Tomoko","family":"Katow","sequence":"additional","affiliation":[{"name":"Research Center for Marine Biology, Tohoku University, Aomori 039-3501, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hiromi","family":"Yoshida","sequence":"additional","affiliation":[{"name":"Institute of Development, Aging and Cancer, Tohoku University, Sendai 980-8575, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Masato","family":"Kiyomoto","sequence":"additional","affiliation":[{"name":"Institute of Development, Aging and Cancer, Tohoku University, Sendai 980-8575, Japan"},{"name":"Marine and Coastal Research Center, Ochanomizu University, Chiba 294-0301, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2021,5,12]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"The Huntington\u2019s Disease Collaborative Research Group (1993). A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington\u2019s disease chromosomes. Cell, 72, 971\u2013983.","DOI":"10.1016\/0092-8674(93)90585-E"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1242\/dmm.000653","article-title":"Inactivation of Drosophila Huntingtin affects long-term adult functioning and the pathogenesis of a Huntington\u2019s disease model","volume":"2","author":"Zhang","year":"2009","journal-title":"Dis. Model. Mech."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"305","DOI":"10.1016\/j.ydbio.2015.07.013","article-title":"Huntingtin is required for ciliogenesis and neurogenesis during early Xenopus development","volume":"408","author":"Haremaki","year":"2015","journal-title":"Dev. Biol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1093\/hmg\/ddl467","article-title":"Wild-type huntingtin participates in protein trafficking between the Golgi and the extracellular space","volume":"16","author":"Strehlow","year":"2006","journal-title":"Hum. Mol. Genet."},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Choi, Y.-B., Kadakkuzha, B.M., Liu, X.-A., Akhmedov, K., Kandel, E.R., and Puthanveettil, S.V. (2014). Huntingtin Is Critical Both Pre- and Postsynaptically for Long-Term Learning-Related Synaptic Plasticity in Aplysia. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0103004"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"4372","DOI":"10.1172\/JCI57552","article-title":"Ciliogenesis is regulated by a huntingtin-HAP1-PCM1 pathway and is altered in Huntington disease","volume":"121","author":"Keryer","year":"2011","journal-title":"J. Clin. Investig."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1186\/2046-2530-2-12","article-title":"Ciliogenesis and cerebrospinal fluid flow in the developing Xenopus brain are regulated by foxj1","volume":"2","author":"Hagenlocher","year":"2013","journal-title":"Cilia"},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Thouvenin, O.L., Keiser, L., CantautBelarif, Y., Carbo-Tano, M., Verweij, F., JurischYaksi, N., Bardet, P.-L., Van Niel, G., Gallaire, F., and Wyart, C. (2019). Origin of the bidirectionality of cerebrospinal fluid flow and impact on long-range transport between brain and spinal cord. BioRxiv Prepr.","DOI":"10.1101\/627166"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"20190154","DOI":"10.1098\/rstb.2019.0154","article-title":"Cilia-driven flows in the brain third ventricle","volume":"375","author":"Eichele","year":"2020","journal-title":"Philos. Trans. R. Soc. B Biol. Sci."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Liu, G., Zhou, Y., Liu, D., Wang, Q., Ruan, Z., He, Q., and Zhang, L. (2015). Global Transcriptome Analysis of the Tentacle of the Jellyfish Cyanea capillata Using Deep Sequencing and Expressed Sequence Tags: Insight into the Toxin- and Degenerative Disease-Related Transcripts. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0142680"},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Candiani, S., Pestarino, M., Cattaneo, E., and Tartari, M. (2007). Characterization, developmental expression and evolutionary features of the huntingtin gene in the amphioxus Branchiostoma floridae. BMC Dev. Biol., 7.","DOI":"10.1186\/1471-213X-7-127"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Gissi, C., Pesole, G., Cattaneo, E., and Tartari, M. (2006). Huntingtin gene evolution in Chordata and its peculiar features in the ascidian Ciona genus. BMC Genom., 7.","DOI":"10.1186\/1471-2164-7-288"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1002\/jez.b.20","article-title":"Neural expression of the Huntington\u2019s disease gene as a chordate evolutionary novelty","volume":"297","author":"Kauffman","year":"2003","journal-title":"J. Exp. Zool. Part B Mol. Dev. Evol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"330","DOI":"10.1093\/molbev\/msm258","article-title":"Phylogenetic Comparison of Huntingtin Homologues Reveals the Appearance of a Primitive polyQ in Sea Urchin","volume":"25","author":"Tartari","year":"2008","journal-title":"Mol. Biol. Evol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"905","DOI":"10.1152\/physrev.00041.2009","article-title":"Molecular Mechanisms and Potential Therapeutical Targets in Huntington\u2019s Disease","volume":"90","author":"Zuccato","year":"2010","journal-title":"Physiol. Rev."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"792","DOI":"10.1016\/j.devcel.2020.07.022","article-title":"A Weak Link with Actin Organizes Tight Junctions to Control Epithelial Permeability","volume":"54","author":"Belardi","year":"2020","journal-title":"Dev. Cell"},{"key":"ref_17","unstructured":"Katow, H., Uemura, I., Yoshida, H., and Katow, T. (2017, January 29). Tjp1 expression at the ciliary band-associated strand (CBAS) of sea urchin larva. Proceedings of the Annual Meeting of Zoological Society of Japan, Tohoku Branch Conference (Aomori), Yamagata, Japan."},{"key":"ref_18","first-page":"1704","article-title":"Development of the GABA-ergic signaling system and its role in larval swimming in sea urchin","volume":"216","author":"Katow","year":"2013","journal-title":"J. Exp. Biol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1002\/cne.10865","article-title":"Expression of Tryptophan 5-Hydroxylase Gene during Sea Urchin Neurogenesis and Role of Serotonergic Nervous System in Larval Behavior","volume":"466","author":"Yaguchi","year":"2003","journal-title":"J. Comp. Neurol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1351","DOI":"10.1016\/j.mod.2003.06.005","article-title":"Mechanisms, mechanics and function of epithelial\u2013mesenchymal transitions in early development","volume":"120","author":"Shook","year":"2003","journal-title":"Mech. Dev."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"39594","DOI":"10.1074\/jbc.C200353200","article-title":"Calcium-dependent cleavage of endogenous wild-type Huntingtin in primary cortical neurons","volume":"277","author":"Goffredo","year":"2002","journal-title":"J. Biol. Chem."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Katow, H., Yoshida, H., Katow, T., and Kiyomoto, M. (2018). Ontogeny of a synaptophysin-mediated GABA transmission mechanism from the ciliary band-associated strand to the ciliary band during the development of the sea urchin Hemicentrotus pulcher-rimus. PeerJ Prepr.","DOI":"10.7287\/peerj.preprints.26625"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41598-020-57567-w","article-title":"Initial report of \u03b3-aminobutyric acidergic locomotion regulatory system and its 3-mercaptopropionic acid-sensitivity in metamorphic juvenile of sea urchin, Hemicentrotus pulcherrimus","volume":"10","author":"Katow","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Katow, H., Abe, K., Katow, T., Yoshida, H., and Kiyomoto, M. (2020). Involvement of Netrin\/Unc-5 Interaction in Ciliary Beating and in Pattern Formation of the Ciliary Band-Associated Strand (CBAS) in the Sea Urchin, Hemicentrotus pulcherrimus. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21186587"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1393","DOI":"10.1093\/hmg\/ddg156","article-title":"Huntingtin contains a highly conserved nuclear export signal","volume":"12","author":"Xia","year":"2003","journal-title":"Hum. Mol. Genet."},{"key":"ref_26","first-page":"65","article-title":"The biological function of the Huntingtin protein and its relevance to Huntington\u2019s Disease pathology","volume":"5","author":"Schulte","year":"2011","journal-title":"Curr. Trends Neurol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"9455","DOI":"10.1523\/JNEUROSCI.4699-13.2014","article-title":"Huntingtin Is Required for Normal Excitatory Synapse Development in Cortical and Striatal Circuits","volume":"34","author":"McKinstry","year":"2014","journal-title":"J. Neurosci."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"491","DOI":"10.1016\/j.stemcr.2014.02.011","article-title":"Huntingtin Regulates Mammary Stem Cell Division and Differentiation","volume":"2","author":"Elias","year":"2014","journal-title":"Stem Cell Rep."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"3190","DOI":"10.1096\/fj.201701510RRR","article-title":"Identification of a novel caspase cleavage site in huntingtin that regulates mutant huntingtin clearance","volume":"33","author":"Martin","year":"2018","journal-title":"FASEB J."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"3705","DOI":"10.1523\/JNEUROSCI.20-10-03705.2000","article-title":"Wild-Type Huntingtin Protects from Apoptosis Upstream of Caspase-3","volume":"20","author":"Rigamonti","year":"2000","journal-title":"J. Neurosci."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1179","DOI":"10.1016\/j.cell.2006.04.026","article-title":"Cleavage at the Caspase-6 Site Is Required for Neuronal Dysfunction and Degeneration Due to Mutant Huntingtin","volume":"125","author":"Graham","year":"2006","journal-title":"Cell"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"7862","DOI":"10.1523\/JNEUROSCI.22-18-07862.2002","article-title":"Caspase Cleavage of Mutant Huntingtin Precedes Neurodegeneration in Huntington\u2019s Disease","volume":"22","author":"Wellington","year":"2002","journal-title":"J. Neurosci."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1016\/j.mod.2004.03.005","article-title":"The 5-HT receptor cell is a new member of secondary mesenchyme cell descendants and forms a major blastocoelar network in sea urchin larvae","volume":"121","author":"Katow","year":"2004","journal-title":"Mech. Dev."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"2808","DOI":"10.1242\/jeb.042150","article-title":"Development of a dopaminergic system in sea urchin embryos and larvae","volume":"213","author":"Katow","year":"2010","journal-title":"J. Exp. Biol."},{"key":"ref_35","first-page":"157","article-title":"In-ternational Union of Pharmacology classification of receptors for 5-hydroxytryptamine (Serotonin)","volume":"46","author":"Hoyer","year":"1994","journal-title":"Pharmacol. Rev."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1016\/j.cub.2018.11.059","article-title":"Ciliary Beating Compartmentalizes Cerebrospinal Fluid Flow in the Brain and Regulates Ventricular Development","volume":"29","author":"Olstad","year":"2019","journal-title":"Curr. Biol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1383","DOI":"10.1093\/hmg\/dds554","article-title":"The huntingtin N17 domain is a multifunctional CRM1 and Ran-dependent nuclear and cilial export signal","volume":"22","author":"Maiuri","year":"2013","journal-title":"Hum. Mol. Genet."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41467-018-04676-w","article-title":"Ependymal cilia beating induces an actin network to protect centrioles against shear stress","volume":"9","author":"Mahuzier","year":"2018","journal-title":"Nat. Commun."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"392","DOI":"10.1016\/j.neuron.2010.06.027","article-title":"Huntingtin Is Required for Mitotic Spindle Orientation and Mammalian Neurogenesis","volume":"67","author":"Godin","year":"2010","journal-title":"Neuron"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1632","DOI":"10.1111\/ejn.14356","article-title":"Cerebrospinal fluid flow dynamics in Huntington\u2019s disease evaluated by phase contrast MRI","volume":"49","author":"Rodrigues","year":"2019","journal-title":"Eur. J. Neurosci."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"910","DOI":"10.1016\/j.neuron.2016.02.003","article-title":"The Biology of Huntingtin","volume":"89","author":"Saudou","year":"2016","journal-title":"Neuron"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"20190165","DOI":"10.1098\/rstb.2019.0165","article-title":"Neuronal coordination of motile cilia in locomotion and feeding","volume":"375","author":"Berger","year":"2020","journal-title":"Philos. Trans. R. Soc. B Biol. Sci."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1242\/jeb.200.1.9","article-title":"Modification of ciliary beating in sea urchin larvae induced by neurotransmitters: Beat-plane rotation and control of frequency fluctuation","volume":"200","author":"Wada","year":"1997","journal-title":"J. Exp. Biol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"981","DOI":"10.1098\/rstb.1999.0449","article-title":"Altered neurotransmitter receptor expression in transgenic mouse models of Huntington\u2019s disease","volume":"354","author":"Cha","year":"1999","journal-title":"Phil. Trans. R. Soc. Lond. B"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"292","DOI":"10.1111\/cns.12826","article-title":"Alteration of GABAergic neurotransmission in Huntington\u2019s dis ease","volume":"24","author":"Garret","year":"2018","journal-title":"CNS Neurosci. Ther."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"10034","DOI":"10.1523\/JNEUROSCI.0715-14.2014","article-title":"Mutant Huntingtin Affects Cortical Progenitor Cell Division and Development of the Mouse Neocortex","volume":"34","author":"Barnat","year":"2014","journal-title":"J. Neurosci."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1016\/j.ydbio.2019.10.037","article-title":"Huntingtin confers fitness but is not embryonically essential in zebrafish development","volume":"458","author":"Sidik","year":"2020","journal-title":"Dev. Biol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"174","DOI":"10.1111\/dgd.12429","article-title":"HpBase: A genome database of a sea urchin, Hemicentrotus pulcherrimus","volume":"60","author":"Kinjo","year":"2018","journal-title":"Dev. Growth Differ."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1111\/j.1440-169X.1988.00035.x","article-title":"Micromere Differentiation in the Sea Urchin Embryo: Expression of Primary Mesenchyme Cell Specific Antigen during Development. (sea urchin\/micromere\/primary mesenchyme cell\/monoclonal antibody)","volume":"30","author":"Shimizu","year":"1988","journal-title":"Dev. Growth Differ."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"112","DOI":"10.3389\/fendo.2013.00112","article-title":"Characterization and Endocytic Internalization of Epith-2 Cell Surface Glycoprotein during the Epithelial-to-Mesenchymal Transition in Sea Urchin Embryos","volume":"4","author":"Wakayama","year":"2013","journal-title":"Front. Endocrinol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1016\/0014-4827(79)90385-9","article-title":"Removal of the fertilization membrane of sea urchin embryos employing aminotriazole","volume":"120","author":"Showman","year":"1979","journal-title":"Exp. Cell Res."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/22\/10\/5116\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T05:59:44Z","timestamp":1760162384000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/22\/10\/5116"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,5,12]]},"references-count":51,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2021,5]]}},"alternative-id":["ijms22105116"],"URL":"https:\/\/doi.org\/10.3390\/ijms22105116","relation":{},"ISSN":["1422-0067"],"issn-type":[{"type":"electronic","value":"1422-0067"}],"subject":[],"published":{"date-parts":[[2021,5,12]]}}}