{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,6]],"date-time":"2026-06-06T04:01:19Z","timestamp":1780718479051,"version":"3.54.1"},"reference-count":42,"publisher":"Japanese Society of Veterinary Science","issue":"6","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["J. Vet. Med. Sci.","The Journal of Veterinary Medical Science"],"published-print":{"date-parts":[[2026]]},"DOI":"10.1292\/jvms.26-0085","type":"journal-article","created":{"date-parts":[[2026,4,15]],"date-time":"2026-04-15T22:14:29Z","timestamp":1776291269000},"page":"813-820","source":"Crossref","is-referenced-by-count":0,"title":["Immunohistochemical characterization of neural stem cells in brains of adult brachycephalic dogs in comparison with canine oligodendroglioma cells"],"prefix":"10.1292","volume":"88","author":[{"given":"Hisaki","family":"TOKUNO","sequence":"first","affiliation":[{"name":"Laboratory of Veterinary Pathology, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kio","family":"YOSHIDA","sequence":"additional","affiliation":[{"name":"Laboratory of Veterinary Pathology, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"James K","family":"CHAMBERS","sequence":"additional","affiliation":[{"name":"Laboratory of Veterinary Pathology, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kazuyuki","family":"UCHIDA","sequence":"additional","affiliation":[{"name":"Laboratory of Veterinary Pathology, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"122","reference":[{"key":"1","doi-asserted-by":"crossref","unstructured":"1. Aldaz P, Mart\u00edn-Mart\u00edn N, Saenz-Anto\u00f1anzas A, Carrasco-Garcia E, \u00c1lvarez-Satta M, El\u00faa-Pinin A, Pollard SM, Lawrie CH, Moreno-Valladares M, Sampr\u00f3n N, Hench J, Lovell-Badge R, Carracedo A, Matheu A.  2022. High SOX9 maintains glioma stem cell activity through a regulatory loop involving STAT3 and PML. <i>Int J Mol Sci<\/i> 23: 15418.","DOI":"10.3390\/ijms23094511"},{"key":"2","doi-asserted-by":"crossref","unstructured":"2. Amin SB, Anderson KJ, Boudreau CE, Martinez-Ledesma E, Kocakavuk E, Johnson KC, Barthel FP, Varn FS, Kassab C, Ling X, Kim H, Barter M, Lau CC, Ngan CY, Chapman M, Koehler JW, Long JP, Miller AD, Miller CR, Porter BF, Rissi DR, Mazcko C, LeBlanc AK, Dickinson PJ, Packer RA, Taylor AR, Rossmeisl JH Jr, Woolard KD, Heimberger AB, Levine JM, Verhaak RGW.  2020. Comparative molecular life history of spontaneous canine and human gliomas. <i>Cancer Cell<\/i> 37: 243\u2013257.e7.","DOI":"10.1016\/j.ccell.2020.01.004"},{"key":"3","unstructured":"3. Annovazzi L, Mellai M, Caldera V, Valente G, Schiffer D.  2011. <i>SOX2<\/i> expression and amplification in gliomas and glioma cell lines. <i>Cancer Genomics Proteomics<\/i> 8: 139\u2013147."},{"key":"4","doi-asserted-by":"crossref","unstructured":"4. Barton SA, Kent M, Hecht EE.  2024. Covariation of skull and brain morphology in domestic dogs. <i>J Comp Neurol<\/i> 532: e25668.","DOI":"10.1002\/cne.25668"},{"key":"5","doi-asserted-by":"crossref","unstructured":"5. Berezovsky AD, Poisson LM, Cherba D, Webb CP, Transou AD, Lemke NW, Hong X, Hasselbach LA, Irtenkauf SM, Mikkelsen T, deCarvalho AC.  2014. <i>Sox2<\/i> promotes malignancy in glioblastoma by regulating plasticity and astrocytic differentiation. <i>Neoplasia<\/i> 16: 193\u2013206, 206.e19\u2013206.e25.","DOI":"10.1016\/j.neo.2014.03.006"},{"key":"6","doi-asserted-by":"crossref","unstructured":"6. Cheung M, Briscoe J.  2003. Neural crest development is regulated by the transcription factor <i>Sox9<\/i>. <i>Development<\/i> 130: 5681\u20135693.","DOI":"10.1242\/dev.00808"},{"key":"7","doi-asserted-by":"crossref","unstructured":"7. Doetsch F.  2003. A niche for adult neural stem cells. <i>Curr Opin Genet Dev<\/i> 13: 543\u2013550.","DOI":"10.1016\/j.gde.2003.08.012"},{"key":"8","doi-asserted-by":"crossref","unstructured":"8. Doetsch F, Garc\u00eda-Verdugo JM, Alvarez-Buylla A.  1997. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. <i>J Neurosci<\/i> 17: 5046\u20135061.","DOI":"10.1523\/JNEUROSCI.17-13-05046.1997"},{"key":"9","doi-asserted-by":"crossref","unstructured":"9. Ekenstedt KJ, Crosse KR, Risselada M.  2020. Canine brachycephaly: anatomy, pathology, genetics and welfare. <i>J Comp Pathol<\/i> 176: 109\u2013115.","DOI":"10.1016\/j.jcpa.2020.02.008"},{"key":"10","doi-asserted-by":"crossref","unstructured":"10. Elsir T, Edqvist PH, Carlson J, Ribom D, Bergqvist M, Ekman S, Popova SN, Alafuzoff I, Ponten F, Nist\u00e9r M, Smits A.  2014. A study of embryonic stem cell-related proteins in human astrocytomas: identification of Nanog as a predictor of survival. <i>Int J Cancer<\/i> 134: 1123\u20131131.","DOI":"10.1002\/ijc.28441"},{"key":"11","doi-asserted-by":"crossref","unstructured":"11. Ernst A, Alkass K, Bernard S, Salehpour M, Perl S, Tisdale J, Possnert G, Druid H, Fris\u00e9n J.  2014. Neurogenesis in the striatum of the adult human brain. <i>Cell<\/i> 156: 1072\u20131083.","DOI":"10.1016\/j.cell.2014.01.044"},{"key":"12","doi-asserted-by":"crossref","unstructured":"12. Faigle R, Song H.  2013. Signaling mechanisms regulating adult neural stem cells and neurogenesis. <i>Biochim Biophys Acta<\/i> 1830: 2435\u20132448.","DOI":"10.1016\/j.bbagen.2012.09.002"},{"key":"13","doi-asserted-by":"crossref","unstructured":"13. Fern\u00e1ndez-Flores F, Garc\u00eda-Verdugo JM, Mart\u00edn-Ib\u00e1\u00f1ez R, Herranz C, Fondevila D, Canals JM, Ar\u00fas C, Pumarola M.  2018. Characterization of the canine rostral ventricular-subventricular zone: Morphological, immunohistochemical, ultrastructural, and neurosphere assay studies. <i>J Comp Neurol<\/i> 526: 721\u2013741.","DOI":"10.1002\/cne.24365"},{"key":"14","doi-asserted-by":"crossref","unstructured":"14. Furutachi S, Miya H, Watanabe T, Kawai H, Yamasaki N, Harada Y, Imayoshi I, Nelson M, Nakayama KI, Hirabayashi Y, Gotoh Y.  2015. Slowly dividing neural progenitors are an embryonic origin of adult neural stem cells. <i>Nat Neurosci<\/i> 18: 657\u2013665.","DOI":"10.1038\/nn.3989"},{"key":"15","doi-asserted-by":"crossref","unstructured":"15. Helton WS.  2009. Cephalic index and perceived dog trainability. <i>Behav Processes<\/i> 82: 355\u2013358.","DOI":"10.1016\/j.beproc.2009.08.004"},{"key":"16","doi-asserted-by":"crossref","unstructured":"16. Hirota Y, Sawada M, Kida YS, Huang SH, Yamada O, Sakaguchi M, Ogura T, Okano H, Sawamoto K.  2012. Roles of planar cell polarity signaling in maturation of neuronal precursor cells in the postnatal mouse olfactory bulb. <i>Stem Cells<\/i> 30: 1726\u20131733.","DOI":"10.1002\/stem.1137"},{"key":"17","doi-asserted-by":"crossref","unstructured":"17. Jos\u00e9-L\u00f3pez R, Gutierrez-Quintana R, de la Fuente C, Manzanilla EG, Su\u00f1ol A, Pi Castro D, A\u00f1or S, S\u00e1nchez-Masian D, Fern\u00e1ndez-Flores F, Ricci E, Marioni-Henry K, Mascort J, Matiasek LA, Matiasek K, Brennan PM, Pumarola M.  2021. Clinical features, diagnosis, and survival analysis of dogs with glioma. <i>J Vet Intern Med<\/i> 35: 1902\u20131917.","DOI":"10.1111\/jvim.16199"},{"key":"18","doi-asserted-by":"crossref","unstructured":"18. Jovanovic VM, Salti A, Tilleman H, Zega K, Jukic MM, Zou H, Friedel RH, Prakash N, Blaess S, Edenhofer F, Brodski C.  2018. BMP\/SMAD pathway promotes neurogenesis of midbrain dopaminergic neurons <i>in vivo<\/i> and in human induced pluripotent and neural stem cells. <i>J Neurosci<\/i> 38: 1662\u20131676.","DOI":"10.1523\/JNEUROSCI.1540-17.2018"},{"key":"19","doi-asserted-by":"crossref","unstructured":"19. Kajdic N, Spazzapan P, Velnar T.  2018. Craniosynostosis - recognition, clinical characteristics, and treatment. <i>Bosn J Basic Med Sci<\/i> 18: 110\u2013116.","DOI":"10.17305\/bjbms.2017.2083"},{"key":"20","doi-asserted-by":"crossref","unstructured":"20. Kishimoto TE, Uchida K, Chambers JK, Kok MK, Son NV, Shiga T, Hirabayashi M, Ushio N, Nakayama H.  2020. A retrospective survey on canine intracranial tumors between 2007 and 2017. <i>J Vet Med Sci<\/i> 82: 77\u201383.","DOI":"10.1292\/jvms.19-0486"},{"key":"21","doi-asserted-by":"crossref","unstructured":"21. Kishimoto TE, Uchida K, Thongtharb A, Shibato T, Chambers JK, Nibe K, Kagawa Y, Nakayama H.  2018. Expression of oligodendrocyte precursor cell markers in canine oligodendrogliomas. <i>Vet Pathol<\/i> 55: 634\u2013644.","DOI":"10.1177\/0300985818777794"},{"key":"22","doi-asserted-by":"crossref","unstructured":"22. Koehler JW, Miller AD, Miller CR, Porter B, Aldape K, Beck J, Brat D, Cornax I, Corps K, Frank C, Giannini C, Horbinski C, Huse JT, O\u2019Sullivan MG, Rissi DR, Mark Simpson R, Woolard K, Shih JH, Mazcko C, Gilbert MR, LeBlanc AK.  2018. A revised diagnostic classification of canine glioma: towards validation of the canine glioma patient as a naturally occurring preclinical model for human glioma. <i>J Neuropathol Exp Neurol<\/i> 77: 1039\u20131054.","DOI":"10.1093\/jnen\/nly085"},{"key":"23","doi-asserted-by":"crossref","unstructured":"23. Kurki P, Vanderlaan M, Dolbeare F, Gray J, Tan EM.  1986. Expression of proliferating cell nuclear antigen (PCNA)\/cyclin during the cell cycle. <i>Exp Cell Res<\/i> 166: 209\u2013219.","DOI":"10.1016\/0014-4827(86)90520-3"},{"key":"24","doi-asserted-by":"crossref","unstructured":"24. Le Douarin NM, Brito JM, Creuzet S.  2007. Role of the neural crest in face and brain development. <i>Brain Res Brain Res Rev<\/i> 55: 237\u2013247.","DOI":"10.1016\/j.brainresrev.2007.06.023"},{"key":"25","doi-asserted-by":"crossref","unstructured":"25. Lee JH, Lee JE, Kahng JY, Kim SH, Park JS, Yoon SJ, Um JY, Kim WK, Lee JK, Park J, Kim EH, Lee JH, Lee JH, Chung WS, Ju YS, Park SH, Chang JH, Kang SG, Lee JH.  2018. Human glioblastoma arises from subventricular zone cells with low-level driver mutations. <i>Nature<\/i> 560: 243\u2013247.","DOI":"10.1038\/s41586-018-0389-3"},{"key":"26","doi-asserted-by":"crossref","unstructured":"26. Mansour TA, Lucot K, Konopelski SE, Dickinson PJ, Sturges BK, Vernau KL, Choi S, Stern JA, Thomasy SM, D\u00f6ring S, Verstraete FJM, Johnson EG, York D, Rebhun RB, Ho HH, Brown CT, Bannasch DL.  2018. Whole genome variant association across 100 dogs identifies a frame shift mutation in <i>DISHEVELLED 2<\/i> which contributes to Robinow-like syndrome in Bulldogs and related screw tail dog breeds. <i>PLoS Genet<\/i> 14: e1007850.","DOI":"10.1371\/journal.pgen.1007850"},{"key":"27","doi-asserted-by":"crossref","unstructured":"27. Mayousse V, Desquilbet L, Jeandel A, Blot S.  2017. Prevalence of neurological disorders in French bulldog: a retrospective study of 343 cases (2002\u20132016). <i>BMC Vet Res<\/i> 13: 212.","DOI":"10.1186\/s12917-017-1132-2"},{"key":"28","doi-asserted-by":"crossref","unstructured":"28. McGreevy PD, Georgevsky D, Carrasco J, Valenzuela M, Duffy DL, Serpell JA.  2013. Dog behavior co-varies with height, bodyweight and skull shape. <i>PLoS One<\/i> 8: e80529.","DOI":"10.1371\/journal.pone.0080529"},{"key":"29","doi-asserted-by":"crossref","unstructured":"29. Miller AD, Miller CR, Rossmeisl JH.  2019. Canine primary intracranial cancer: a clinicopathologic and comparative review of glioma, meningioma, and choroid plexus tumors. <i>Front Oncol<\/i> 9: 1151.","DOI":"10.3389\/fonc.2019.01151"},{"key":"30","doi-asserted-by":"crossref","unstructured":"30. Pulvirenti T, Van Der Heijden M, Droms LA, Huse JT, Tabar V, Hall A.  2011. Dishevelled 2 signaling promotes self-renewal and tumorigenicity in human gliomas. <i>Cancer Res<\/i> 71: 7280\u20137290.","DOI":"10.1158\/0008-5472.CAN-11-1531"},{"key":"31","doi-asserted-by":"crossref","unstructured":"31. Roberts T, McGreevy P, Valenzuela M.  2010. Human induced rotation and reorganization of the brain of domestic dogs. <i>PLoS One<\/i> 5: e11946.","DOI":"10.1371\/journal.pone.0011946"},{"key":"32","doi-asserted-by":"crossref","unstructured":"32. Schoenebeck JJ, Hutchinson SA, Byers A, Beale HC, Carrington B, Faden DL, Rimbault M, Decker B, Kidd JM, Sood R, Boyko AR, Fondon JW 3rd, Wayne RK, Bustamante CD, Ciruna B, Ostrander EA.  2012. Variation of <i>BMP3<\/i> contributes to dog breed skull diversity. <i>PLoS Genet<\/i> 8: e1002849.","DOI":"10.1371\/journal.pgen.1002849"},{"key":"33","doi-asserted-by":"crossref","unstructured":"33. Scott CE, Wynn SL, Sesay A, Cruz C, Cheung M, Gomez Gaviro MV, Booth S, Gao B, Cheah KS, Lovell-Badge R, Briscoe J.  2010. SOX9 induces and maintains neural stem cells. <i>Nat Neurosci<\/i> 13: 1181\u20131189.","DOI":"10.1038\/nn.2646"},{"key":"34","doi-asserted-by":"crossref","unstructured":"34. Song RB, Vite CH, Bradley CW, Cross JR.  2013. Postmortem evaluation of 435 cases of intracranial neoplasia in dogs and relationship of neoplasm with breed, age, and body weight. <i>J Vet Intern Med<\/i> 27: 1143\u20131152.","DOI":"10.1111\/jvim.12136"},{"key":"35","doi-asserted-by":"crossref","unstructured":"35. Truv\u00e9 K, Dickinson P, Xiong A, York D, Jayashankar K, Pielberg G, Koltookian M, Mur\u00e9n E, Fuxelius HH, Weishaupt H, Swartling FJ, Andersson G, Hedhammar \u00c5, Bongcam-Rudloff E, Forsberg-Nilsson K, Bannasch D, Lindblad-Toh K.  2016. Utilizing the dog genome in the search for novel candidate genes involved in glioma development-genome wide association mapping followed by targeted massive parallel sequencing identifies a strongly associated locus. <i>PLoS Genet<\/i> 12: e1006000.","DOI":"10.1371\/journal.pgen.1006000"},{"key":"36","doi-asserted-by":"crossref","unstructured":"36. Walton RM, Parmentier T, Wolfe JH.  2013. Postnatal neural precursor cell regions in the rostral subventricular zone, hippocampal subgranular zone and cerebellum of the dog (<i>Canis lupus familiaris<\/i>). <i>Histochem Cell Biol<\/i> 139: 415\u2013429.","DOI":"10.1007\/s00418-012-1053-x"},{"key":"37","doi-asserted-by":"crossref","unstructured":"37. Wang L, He S, Yuan J, Mao X, Cao Y, Zong J, Tu Y, Zhang Y.  2012. Oncogenic role of SOX9 expression in human malignant glioma. <i>Med Oncol<\/i> 29: 3484\u20133490.","DOI":"10.1007\/s12032-012-0267-z"},{"key":"38","doi-asserted-by":"crossref","unstructured":"38. Yoshida K, Chambers JK, Uchida K.  2024. The relationships of platelet-derived growth factor, microvascular proliferation, and tumor cell proliferation in canine high-grade oligodendrogliomas: Immunohistochemistry of 45 tumors and an AFOB-01 xenograft mouse model. <i>Vet Pathol<\/i> 61: 732\u2013742.","DOI":"10.1177\/03009858241241793"},{"key":"39","doi-asserted-by":"crossref","unstructured":"39. Yoshida K, Chambers JK, Uchida K.  2025. Chromosomal gain and mutations of <i>platelet-derived growth factor receptor-\u03b1<\/i> gene in canine high-grade oligodendroglioma. <i>Vet Pathol<\/i> 62: 478\u2013489.","DOI":"10.1177\/03009858241309396"},{"key":"40","doi-asserted-by":"crossref","unstructured":"40. Yoshida K, Chambers JK, Uchida K.  2023. Immunohistochemical study of neural stem cell lineage markers in canine brains, gliomas, and a glioma cell line. <i>Vet Pathol<\/i> 60: 35\u201346.","DOI":"10.1177\/03009858221136297"},{"key":"41","doi-asserted-by":"crossref","unstructured":"41. Zhao J, Zhang L, Dong X, Liu L, Huo L, Chen H.  2018. High expression of vimentin is associated with progression and a poor outcome in glioblastoma. <i>Appl Immunohistochem Mol Morphol<\/i> 26: 337\u2013344.","DOI":"10.1097\/PAI.0000000000000420"},{"key":"42","doi-asserted-by":"crossref","unstructured":"42. Zhong N, Gersch RP, Hadjiargyrou M.  2006. Wnt signaling activation during bone regeneration and the role of Dishevelled in chondrocyte proliferation and differentiation. <i>Bone<\/i> 39: 5\u201316.","DOI":"10.1016\/j.bone.2005.12.008"}],"container-title":["Journal of Veterinary Medical Science"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.jstage.jst.go.jp\/article\/jvms\/88\/6\/88_26-0085\/_pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,6,6]],"date-time":"2026-06-06T03:21:46Z","timestamp":1780716106000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.jstage.jst.go.jp\/article\/jvms\/88\/6\/88_26-0085\/_article"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026]]},"references-count":42,"journal-issue":{"issue":"6","published-print":{"date-parts":[[2026]]}},"URL":"https:\/\/doi.org\/10.1292\/jvms.26-0085","relation":{},"ISSN":["0916-7250","1347-7439"],"issn-type":[{"value":"0916-7250","type":"print"},{"value":"1347-7439","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026]]},"article-number":"26-0085"}}