Effects of lysosomal instability on the non-apoptotic Purkinje cell death

• Project/Area Number: 17K08522
• Research Category: Grant-in-Aid for Scientific Research (C)
• Allocation Type: Multi-year Fund
• Section: 一般
• Research Field: General anatomy (including histology/embryology)
• Research Institution: Juntendo University
• Principal Investigator: Koike Masato 順天堂大学, 医学(系)研究科(研究院), 教授 (80347210)
• Project Period (FY): 2017-04-01 – 2020-03-31
• Project Status: Completed (Fiscal Year 2019)
• Budget Amount: ¥4,810,000 (Direct Cost: ¥3,700,000、Indirect Cost: ¥1,110,000); Fiscal Year 2019: ¥1,820,000 (Direct Cost: ¥1,400,000、Indirect Cost: ¥420,000); Fiscal Year 2018: ¥1,560,000 (Direct Cost: ¥1,200,000、Indirect Cost: ¥360,000); Fiscal Year 2017: ¥1,430,000 (Direct Cost: ¥1,100,000、Indirect Cost: ¥330,000)
• Keywords: オートファジー / リソソーム / カテプシン / ゴルジ体 / 小脳 / プルキンエ細胞 / 細胞死 / 軸索変性 / LC3 / 免疫電子顕微鏡 / 凍結超薄切片法 / カテプシンD

Outline of Final Research Achievements

We generated mice with a cathepsin D (CTSD) deficiency specifically in the Purkinje (PCs) and basket cells (BCs) and compared their phenotypes with those of PC and BC-selective Atg7-deficient mice. In both strains of mice, PCs underwent degeneration, but the CTSD-deficient PCs disappeared more rapidly than their Atg7-deficient counterparts. The neuronal cell death of CTSD- and Atg7-deficient PCs was distinct from apoptosis. Axonal spheroids and the swelling of presynaptic terminals of PCs were more pronounced in Atg7-deficient PCs than in CTSD-deficient PCs.These results suggested that PCs were more vulnerable to CTSD deficiency in lysosomes than to autophagy impairment, and this vulnerability does not depend on the severity of axonal swelling.
We also generated mice with a Golgi pH regulator (GPHR) deficiency specifically in the PCs and BCs and found that PCs from the mutant mice exhibited axonal degeneration and progressive cell loss.

Academic Significance and Societal Importance of the Research Achievements

ヒトではカテプシンDの遺伝子変異は最も重篤なタイプの神経性セロイドリポフスチン蓄積症発症に関与する。同患者では、カテプシンDの活性が低いほど症状が重篤であるが、全ての症例において小脳失調が認められる。本研究成果は、神経性セロイドリポフスチン蓄積症における神経変性のメカニズムの一端を明らかにするもので、同疾患の理解につながる社会的意義を有する。
ゴルジ体の機能不全については、これまでゴルジ体を特異的に制御する薬剤が存在せず、神経変性疾患におけるゴルジ体の構造異常がその原因なのかを知る術がなかった。今回のGPHR欠損マウスの解析で、ゴルジ体の異常と神経変性との直接的な因果関係を明らかにした。

Research Products

• [Int'l Joint Research] Utrecht University(オランダ)
• [Int'l Joint Research] ユトレヒト大学(オランダ)
• [Int'l Joint Research] ユトレヒト大学(オランダ)
• [Journal Article] a-Synuclein BAC transgenic mice exhibit RBD-like behaviour and hyposmia:a prodromal Parkinson’s disease model (2020)
  • Author(s): Taguchi T, Ikuno M, Hondo M, Parajuli LK, Taguchi K, Ueda J, Sawamura M, Okuda S, Nakanishi E, Hara J, Uemura N, Hatanaka Y, Ayaki T, Matsuzawa S, Tanaka M, El-Agnaf OMA, Koike M, Yanagisawa M, Uemura MT, Yamakado H, Takahashi R
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  • DOI: 10.1093/brain/awz380
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• [Journal Article] 三次元電子顕微鏡法 (2020)
  • Author(s): 9. 小池正人
  • Journal Title: 医学のあゆみ Volume: 272 Pages: 934-939
• [Journal Article] Peroxisomes control mitochondrial dynamics and the mitochondrion-dependent pathway of apoptosis. (2019)
  • Author(s): Tanaka, H., *Okazaki, T., Aoyama, S., Yokota, M., Koike, M., Okada, Y., Fujiki, Y., and Gotoh, Y.
  • Journal Title: J. Cell Sci. Volume: － Issue: 11
  • DOI: 10.1242/jcs.224766
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  • Author(s): Shindo R, Ohmuraya M, Komazawa-Sakon S, Miyake S, Deguchi Y, Yamazaki S, Nishina T, Yoshimoto T, Kakuta S, Koike M, Uchiyama Y, Konishi H, Kiyama H, Mikami T, Moriwaki K, Araki K, Nakano H.
  • Journal Title: iScience Volume: 15 Pages: 536-551
  • DOI: 10.1016/j.isci.2019.05.011
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• [Journal Article] Cerebellar Neurodegeneration and Neuronal Circuit Remodeling in Golgi pH Regulator-Deficient Mice (2019)
  • Author(s): Sou Yu-shin、Kakuta Soichiro、Kamikubo Yuji、Niisato Kazue、Sakurai Takashi、Parajuli Laxmi Kumar、Tanida Isei、Saito Hiromitsu、Suzuki Noboru、Sakimura Kenji、Maeda Yusuke、Kinoshita Taroh、Uchiyama Yasuo、Koike Masato
  • Journal Title: eNeuro Volume: 6 Issue: 3 Pages: 0427-18
  • DOI: 10.1523/eneuro.0427-18.2019
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• [Journal Article] Bone Mineral Density Is Increased in the Cadmium-Induced Omphalocele Chick Model by Using Three-Dimensional Micro-Computed Tomography (2019)
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  • Journal Title: Journal of the Endocrine Society Volume: 3 Pages: 1979-92
  • DOI: 10.1210/js.2019-00075
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• [Journal Article] Reduction of Freezing Behavior by Acupuncture Stimulation at HT7 in Contextual Fear-Conditioned Mice (2019)
  • Author(s): HWANG JUNGWON、KOIKE MASATO、HIOKI HIROYUKI
  • Journal Title: Juntendo Medical Journal Volume: 65 Issue: 6 Pages: 554-560
  • DOI: 10.14789/jmj.2019.65.JMJ19-OA17
  • NAID: 130007784488
  • ISSN: 2187-9737, 2188-2126
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• [Journal Article] Loss of autophagy impairs physiological steatosis by accumulation of NCoR1. (2019)
  • Author(s): Takahashi SS, Sou YS, Saito T, Kuma A, Yabe T, Sugiura Y, Lee HC, Suematsu M, Yokomizo T, Koike M, Terai S, Mizushima N, Waguri S, Komatsu M.
  • Journal Title: Life Sci Alliance. Volume: 3 Issue: 1 Pages: 201900513-201900513
  • DOI: 10.26508/lsa.201900513
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• [Journal Article] Oxytocin induced labor causes region and sex‐specific transient oligodendrocyte cell death in neonatal mouse brain (2019)
  • Author(s): Hirayama Takashi、Hiraoka Yuichi、Kitamura Eri、Miyazaki Shinji、Horie Kengo、Fukuda Tomokazu、Hidema Shizu、Koike Masato、Itakura Atsuo、Takeda Satoru、Nishimori Katsuhiko
  • Journal Title: Journal of Obstetrics and Gynaecology Research Volume: 46 Issue: 1 Pages: 66-78
  • DOI: 10.1111/jog.14149
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  • Journal Title: Leukemia Volume: 34 Issue: 2 Pages: 499-509
  • DOI: 10.1038/s41375-019-0564-z
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  • Author(s): Hayakawa Hideki、Nakatani Rie、Ikenaka Kensuke、Aguirre Cesar、Choong Chi‐Jing、Tsuda Hiroshi、Nagano Seiichi、Koike Masato、Ikeuchi Takeshi、Hasegawa Masato、Papa Stella M.、Nagai Yoshitaka、Mochizuki Hideki、Baba Kousuke
  • Journal Title: Movement Disorders Volume: 35 Issue: 2 Pages: 256-267
  • DOI: 10.1002/mds.27887
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• [Journal Article] GBA haploinsufficiency accelerates alpha-synuclein pathology with altered lipid metabolism in a prodromal model of Parkinson’s disease (2019)
  • Author(s): Ikuno Masashi、Yamakado Hodaka、Akiyama Hisako、Parajuli Laxmi Kumar、Taguchi Katsutoshi、Hara Junko、Uemura Norihito、Hatanaka Yusuke、Higaki Katsumi、Ohno Kousaku、Tanaka Masaki、Koike Masato、Hirabayashi Yoshio、Takahashi Ryosuke
  • Journal Title: Human Molecular Genetics Volume: 印刷中 Issue: 11 Pages: 1894-1904
  • DOI: 10.1093/hmg/ddz030
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• [Journal Article] Cathepsin L-deficiency enhances liver regeneration after partial hepatectomy (2019)
  • Author(s): Sato Toshifumi、Yamashina Shunhei、Izumi Kosuke、Ueno Takashi、Koike Masato、Ikejima Kenichi、Peters Christoph、Watanabe Sumio
  • Journal Title: Life Sciences Volume: 221 Pages: 293-300
  • DOI: 10.1016/j.lfs.2019.02.040
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• [Journal Article] 快人快説 最先端の研究テクノロジー紹介⑤-電子顕微鏡三次元立体再構築による組織細胞の観察の有用性と今後の課題 (2018)
  • Author(s): 小池 正人
  • Journal Title: LiSA Volume: 25 Issue: 1 Pages: 79-89
  • DOI: 10.11477/mf.3101201038
  • ISSN: 1340-8836, 1883-5511
  • Year and Date: 2018-01-01
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  • DOI: 10.1371/journal.pone.0198039
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• [Journal Article] Defective autophagy in vascular smooth muscle cells enhances cell death and atherosclerosis. (2018)
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  • Journal Title: Autophagy Volume: 14 Issue: 11 Pages: 1991-2006
  • DOI: 10.1080/15548627.2018.1501132
  • Peer Reviewed / Open Access
• [Journal Article] LRRK2 and its substrate Rab GTPases are sequentially targeted onto stressed lysosomes and maintain their homeostasis (2018)
  • Author(s): Eguchi Tomoya、Kuwahara Tomoki、Sakurai Maria、Komori Tadayuki、Fujimoto Tetta、Ito Genta、Yoshimura Shin-ichiro、Harada Akihiro、Fukuda Mitsunori、Koike Masato、Iwatsubo Takeshi
  • Journal Title: Proceedings of the National Academy of Sciences Volume: 115 Issue: 39
  • DOI: 10.1073/pnas.1812196115
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• [Journal Article] Optimization of mNeonGreen for Homo sapiens increases its fluorescent intensity in mammalian cells (2018)
  • Author(s): Tanida-Miyake Emiko、Koike Masato、Uchiyama Yasuo、Tanida Isei
  • Journal Title: PLOS ONE Volume: 13 Issue: 1 Pages: e0191108-e0191108
  • DOI: 10.1371/journal.pone.0191108
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• [Journal Article] Innate immune adaptor TRIF deficiency accelerates disease progression of ALS mice with accumulation of aberrantly activated astrocytes (2018)
  • Author(s): Komine Okiru、Yamashita Hirofumi、Fujimori-Tonou Noriko、Koike Masato、Jin Shijie、Moriwaki Yasuhiro、Endo Fumito、Watanabe Seiji、Uematsu Satoshi、Akira Shizuo、Uchiyama Yasuo、Takahashi Ryosuke、Misawa Hidemi、Yamanaka Koji
  • Journal Title: Cell Death & Differentiation Volume: 印刷中 Issue: 12 Pages: 2130-2146
  • DOI: 10.1038/s41418-018-0098-3
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• [Journal Article] Molecular mechanisms of Streptococcus pneumoniae-targeted autophagy via pneumolysin, Golgi-resident Rab41, and Nedd4-1-mediated K63-linked ubiquitination (2018)
  • Author(s): Ogawa M, Matsuda R, Takada N, Tomokiyo M, Yamamoto S, Shizukusihi S, Yamaji T, Yoshikawa Y, Yoshida M, Tanida I, Koike M, Murai M, Morita H, Takeyama H, Ryo A, Guan JL, Yamamoto M, Inoue JI, Yanagawa T, Fukuda M, Kawabe H, Ohnishi M
  • Journal Title: Cellular Microbiology Volume: e12846 Issue: 8
  • DOI: 10.1111/cmi.12846
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• [Journal Article] Blockade of TNF receptor superfamily 1 (TNFR1)-dependent and TNFR1-independent cell death is crucial for normal epidermal differentiation (2018)
  • Author(s): Piao Xuehua、Miura Ryosuke、Miyake Sanae、Komazawa-Sakon Sachiko、Koike Masato、Shindo Ryodai、Takeda Junji、Hasegawa Akito、Abe Riichiro、Nishiyama Chiharu、Mikami Tetsuo、Yagita Hideo、Uchiyama Yasuo、Nakano Hiroyasu
  • Journal Title: Journal of Allergy and Clinical Immunology Volume: - Issue: 1 Pages: 213-228.e10
  • DOI: 10.1016/j.jaci.2018.02.043
  • Peer Reviewed / Open Access
• [Journal Article] Purkinje Cells Are More Vulnerable to the Specific Depletion of Cathepsin D Than to That of Atg7 (2017)
  • Author(s): Koike Masato、Shibata Masahiro、Sunabori Takehiko、Yamaguchi Junji、Sakimura Kenji、Komatsu Masaaki、Tanaka Keiji、Uchiyama Yasuo
  • Journal Title: The American Journal of Pathology Volume: 187 Issue: 7 Pages: 1586-1600
  • DOI: 10.1016/j.ajpath.2017.02.020
  • Peer Reviewed
• [Journal Article] Vps35 in cooperation with LRRK2 regulates synaptic vesicle endocytosis through the endosomal pathway in Drosophila (2017)
  • Author(s): Inoshita Tsuyoshi、Arano Taku、Hosaka Yuka、Meng Hongrui、Umezaki Yujiro、Kosugi Sakiko、Morimoto Takako、Koike Masato、Chang Hui-Yun、Imai Yuzuru、Hattori Nobutaka
  • Journal Title: Human Molecular Genetics Volume: 26 Issue: 15 Pages: 2933-2948
  • DOI: 10.1093/hmg/ddx179
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• [Journal Article] Non-steroidal anti-inflammatory drug delays corneal wound healing by reducing production of 12-hydroxyheptadecatrienoic acid, a ligand for leukotriene B4 receptor 2 (2017)
  • Author(s): Iwamoto Satoshi、Koga Tomoaki、Ohba Mai、Okuno Toshiaki、Koike Masato、Murakami Akira、Matsuda Akira、Yokomizo Takehiko
  • Journal Title: Scientific Reports Volume: 7 Issue: 1 Pages: 13267-13267
  • DOI: 10.1038/s41598-017-13122-8
  • Peer Reviewed / Open Access
• [Journal Article] TDP-43 accelerates age-dependent degeneration of interneurons (2017)
  • Author(s): Tsuiji Hitomi、Inoue Ikuyo、Takeuchi Mari、Furuya Asako、Yamakage Yuko、Watanabe Seiji、Koike Masato、Hattori Mitsuharu、Yamanaka Koji
  • Journal Title: Scientific Reports Volume: 7 Issue: 1 Pages: 14972-14972
  • DOI: 10.1038/s41598-017-14966-w
  • Peer Reviewed / Open Access
• [Journal Article] Cordyceps militaris improves the survival of Dahl salt-sensitive hypertensive rats possibly via influences of mitochondria and autophagy functions. (2017)
  • Author(s): Takakura K(1), Ito S(1), Sonoda J(1), Tabata K, Shiozaki M, Nagai K, Shibata M, Koike M, Uchiyama Y, Gotow T
  • Journal Title: Heliyon Volume: 3 Issue: 11 Pages: e00462-e00462
  • DOI: 10.1016/j.heliyon.2017.e00462
  • Peer Reviewed / Open Access
• [Presentation] Distinct age-dependent subcellular changes in a model mouse of Parkinson's disease as revealed by volumetric FIB/SEM imaging of striatum (2020)
  • Author(s): LK Parajuli, K Wako, S Maruo, R Takahashi, M Koike
  • Organizer: ABiS Symposium Forefront and Future of Electron Microscopic Imaging
  • Int'l Joint Research
• [Presentation] 直接路ニューロンから淡蒼球外節への投射は近接する間接路ニューロンの投射領域に包含される (2019)
  • Author(s): 岡本慎一郎、孫在隣、高橋慧、石田葉子、山内健太、小池正人、藤山文乃、日置寛之
  • Organizer: 第42回日本神経科学大会（Neuroscience2019）
• [Presentation] 神門への鍼治療は恐怖文脈条件付けしたマウスのすくみ反応を減弱させる (2019)
  • Author(s): 黄晶媛、小池正人、日置寛之
  • Organizer: 第42回日本神経科学大会（Neuroscience2019）
• [Presentation] 小脳神経系におけるゴルジ体酸性環境の重要性 (2019)
  • Author(s): 曽高友深、角田宗一郎、上窪裕二、新里和恵、櫻井隆、 崎村建司、前田祐輔、木下タロウ、内山安男、小池正人
  • Organizer: 第42回日本神経科学大会（Neuroscience2019）
• [Presentation] パーキンソン病の前駆期モデルにおいて、GBAのハプロ不全は脂質代謝変化を伴いアルファシヌクレイン病理を加速させる (2019)
  • Author(s): 生野真嗣、山門穂高、秋山央子、Parajuli Kumar Laxmi、田口勝敏、原淳子、畑中悠佑、檜垣克美、田中雅樹、小池正人、平林義雄、高橋良輔
  • Organizer: 第42回日本神経科学大会（Neuroscience2019）
• [Presentation] 変異型alpha-シヌクレインフィブリルによるマウス脳でのレビー病理の形成 (2019)
  • Author(s): 馬場孝輔、早川英規、池中建介、鐘其静、津田浩史、小池正人、長野清一、池内健、長谷川成人、永井義隆、望月秀樹
  • Organizer: 第42回日本神経科学大会（Neuroscience2019）
• [Presentation] 中枢神経系の髄鞘形成におけるLAMTOR1の役割 (2019)
  • Author(s): 砂堀毅彦、小池正人
  • Organizer: 第42回日本神経科学大会（Neuroscience2019）
• [Presentation] Distinct age-dependent subcellular changes in a model mouse of Parkinson's disease as revealed by volumetric FIB/SEM imaging of striatum (2019)
  • Author(s): LK Parajuli, K Wako, S Maruo, R Takahashi, M Koike
  • Organizer: 第42回日本神経科学大会（Neuroscience2019）
• [Presentation] Multi-scale imaging from the whole brain level to the ultrastructure level by using a modified scales method (2019)
  • Author(s): H Hioki, K Yamauchi, S Okamoto, K Isa, Y Ishida, A Takenaka, M Takahashi, J Hwang, A Yoshida, Y Uchiyama, M Koike, T Isa, T Furuta
  • Organizer: The 49th Society for Neuroscience Annual Meeting (Neuroscience 2019)
  • Int'l Joint Research
• [Presentation] Cerebellar neurodegeneration and neuronal circuit remodeling in Golgi pH regulator-deficient mice (2019)
  • Author(s): YS Sou, S Kakuta, Y Kamikubo, K Niisato, T Sakurai, LK Parajuli, I Tanida, H Saito, N Suzuki, K Sakimura, Y Maeda, T Kinoshita, Y Uchiyama, M Koike
  • Organizer: The 49th Society for Neuroscience Annual Meeting (Neuroscience 2019)
  • Int'l Joint Research
• [Presentation] Basic Sample Preparation (2019)
  • Author(s): Koike M
  • Organizer: Tokuyasu Workshop 2019
  • Int'l Joint Research / Invited
• [Presentation] An Example of Application for Visualising Autophagy (2019)
  • Author(s): Koike M
  • Organizer: Tokuyasu Workshop 2019
  • Int'l Joint Research / Invited
• [Presentation] Distinct age-dependent subcellular changes in a model mouse of Parkinson's disease as revealed by volumetric FIB/SEM imaging of striatum (2019)
  • Author(s): Laxmi Kumal Parajuli, Ken Wako, Suiki Maruo, Ryosuke Takahashi, Masato Koike
  • Organizer: 革新脳国際シンポジウムISBM2019: From Structure to Function
  • Int'l Joint Research
• [Presentation] Distinct age-dependent subcellular changes in a model mouse of Parkinson's disease as revealed by volumetric FIB/SEM imaging of striatum (2019)
  • Author(s): Laxmi Kumal Parajuli, Ken Wako, Suiki Maruo, Ryosuke Takahashi, Masato Koike
  • Organizer: 日本顕微鏡学会関東支部第43回講演会
• [Presentation] The improvement of Tokuyasu method for the detection of autophagosomes (2018)
  • Author(s): Koike M, De Maziare A, van Dijk S, Klumperman J
  • Organizer: 第74回日本顕微鏡学会学術講演会
• [Presentation] 遺伝的リスクファクターを用いた孤発性パーキンソン病モデルマウスの作成 (2018)
  • Author(s): 生野真嗣、山門穂高、秋山央子、Laxmi Kumar Parajuli、田口勝敏、原純子、上村紀仁、畑中悠佑、檜垣克美、大野耕策、田中雅樹、小池正人、平林義雄、高橋良輔
  • Organizer: 第41回日本神経科学大会
• [Presentation] TEMを使った免疫電子顕微鏡法の実践 (2018)
  • Author(s): 小池正人
  • Organizer: 第43回組織細胞化学講習会
  • Invited
• [Presentation] The effect of impairment of autophagy versus lysosomal proteostasis on the survival of Purkinje cells (2018)
  • Author(s): Koike M
  • Organizer: 19th International Congress of Neuropathology
  • Int'l Joint Research / Invited
• [Presentation] GBA haploinsufficiency accelerated alpha synuclein pathology with altered lipid metabolism in a premotor model of Parkinson’s disease (2018)
  • Author(s): Yamakado H, Ikuno M, Akiyama K, Parajuli LK, Taguchi K, Hara J, Uemura N, Hatanaka Y, Higaki K, Tanaka M, Koike M Hirabayashi Y, Takahashi R
  • Organizer: 22nd International Congress of Parkinson's Disease and Movement Disorders
  • Int'l Joint Research
• [Presentation] オリゴデンドロサイト特異的蛋白質BCAS1のKOマウスは、ミエリンの減少、統合失調様症状、炎症関連遺伝子の上昇を示す (2017)
  • Author(s): 石本哲也、二宮賢介、井上蘭、小池正人 、内山安男、森寿
  • Organizer: 第40回日本神経科学大会
• [Presentation] 特異的カテプシンD欠損プルキンエ細胞の脆弱性 －特に、同Atg7欠損プルキンエ細胞との比較において (2017)
  • Author(s): 小池正人、柴田昌宏、砂堀毅彦、山口隼司、崎村建司、小松雅明、田中啓二、内山安男
  • Organizer: 第40回日本神経科学大会
• [Presentation] Vps35 in cooperation with LRRK2 regulates synaptic vesicle recycling through the endosomal pathway (2017)
  • Author(s): 井下強、崔長旭、荒野拓、穂坂有加、孟紅蕊、梅崎勇次郎、小杉紗紀子、森本高子、小池正人、Chang Hui-Yun、今居譲、服部信孝
  • Organizer: 第40回日本神経科学大会
• [Presentation] 徳安法の発展から見た本シンポジウムのねらいについて (2017)
  • Author(s): 小池正人
  • Organizer: 第73回日本顕微鏡学会学術講演会
• [Presentation] 凍結超薄切片法の改良による内在性LC3の検出と単層培養標本を用いた切片作成 (2017)
  • Author(s): 小池正人
  • Organizer: 第73回日本顕微鏡学会学術講演会
• [Remarks] 順天堂大学大学院医学研究科神経機能構造学講座
  • URL: https://juntendo-cellbio.jp/
• [Remarks] 神経機能構造学 教室トップページ
  • URL: https://www.juntendo.ac.jp/graduate/laboratory/labo/shinkei_kozo/