Alterations of ATG4A and LC3B in neurons derived from Alzheimer's disease patients.


Journal

Genes to cells : devoted to molecular & cellular mechanisms
ISSN: 1365-2443
Titre abrégé: Genes Cells
Pays: England
ID NLM: 9607379

Informations de publication

Date de publication:
Apr 2023
Historique:
revised: 24 01 2023
received: 22 12 2022
accepted: 27 01 2023
medline: 5 4 2023
pubmed: 1 2 2023
entrez: 31 1 2023
Statut: ppublish

Résumé

We investigated the alterations in autophagy-related molecules in neurons differentiated from induced pluripotent stem cells obtained from patients with Alzheimer's disease (AD). Consistent with our previous microarray data, ATG4A protein was upregulated in the neurons derived from a familial AD patient with an APP-E693Δ mutation who showed accumulation of intracellular amyloid β peptide (Aβ). This upregulation was reversed by inhibiting Aβ production, suggesting that the intracellular Aβ may be responsible for the upregulation of ATG4A. The LC3B-II/LC3B-I ratio, an index of autophagosome formation, was lower in the neurons derived from the AD patient with APP-E693Δ as well as the neurons derived from other familial and sporadic AD patients. These findings indicate that dysregulation of autophagy-related molecules may accelerate the pathogenesis of AD.

Identifiants

pubmed: 36719634
doi: 10.1111/gtc.13010
doi:

Substances chimiques

Amyloid beta-Peptides 0
ATG4A protein, human EC 3.4.22.-
Autophagy-Related Proteins 0
Cysteine Endopeptidases EC 3.4.22.-
MAP1LC3B protein, human 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

319-325

Subventions

Organisme : Core Research for Evolutional Science and Technology

Informations de copyright

© 2023 Molecular Biology Society of Japan and John Wiley & Sons Australia, Ltd.

Références

Agrotis, A., Pengo, N., Burden, J. J., & Ketteler, R. (2019). Redundancy of human ATG4 protease isoforms in autophagy and LC3/GABARAP processing revealed in cells. Autophagy, 15, 976-997.
Boland, B., Kumar, A., Lee, S., Platt, F. M., Wegiel, J., Yu, W. H., & Nixon, R. A. (2008). Autophagy induction and autophagosome clearance in neurons: Relationship to autophagic pathology in Alzheimer's disease. Journal of Neuroscience, 28, 6926-6937.
Carvalho, C., Santos, M. S., Oliveira, C. R., & Moreira, P. I. (2015). Alzheimer's disease and type 2 diabetes-related alterations in brain mitochondria, autophagy and synaptic markers. Biochimica et Biophysica Acta - Molecular Basis of Disease, 1852, 1665-1675.
Deng, Z., Sun, R., Han, X., Zhang, Y., Zhou, Y., Shan, Y., Xu, J., Li, X., He, F., & Fang, W. (2022). Porcine circovirus 2 activates the PERK-reactive oxygen species axis to induce p53 phosphorylation with subsequent cell cycle arrest at S phase in favor of its replication. Journal of Virology, 96, e0127422. https://doi.org/10.1128/jvi.01274-22
Emmanouilidou, E., Melachroinou, K., Roumeliotis, T., Garbis, S. D., Ntzouni, M., Margaritis, L. H., Stefanis, L., & Vekrellis, K. (2010). Cell-produced α-synuclein is secreted in a calcium-dependent manner by exosomes and impacts neuronal survival. Journal of Neuroscience, 30, 6838-6851.
Haass, C., & Selkoe, D. (2022). If amyloid drives Alzheimer disease, why have anti-amyloid therapies not yet slowed cognitive decline? PLoS Biology, 20, 1-15.
Hernandez, D., Torres, C. A., Setlik, W., Cebrián, C., Mosharov, E. V., Tang, G., Cheng, H. C., Kholodilov, N., Yarygina, O., Burke, R. E., Gershon, M., & Sulzer, D. (2012). Regulation of presynaptic neurotransmission by macroautophagy. Neuron, 74, 277-284.
Huang, Y., Chuang, A. Y., Romano, R. A., Liégeois, N. J., Sinha, S., Trink, B., Ratovitski, E., & Sidransky, D. (2010). Phospho-ΔNp63α/NF-Y protein complex transcriptionally regulates DDIT3 expression in squamous cell carcinoma cells upon cisplatin exposure. Cell Cycle, 9, 328-338.
Kim, S., Lee, D., Song, J. C., Cho, S. J., Yun, S. M., Koh, Y. H., Song, J., Johnson, G. V. W., & Jo, C. (2014). NDP52 associates with phosphorylated tau in brains of an Alzheimer disease mouse model. Biochemical and Biophysical Research Communications, 454, 196-201.
Kondo, T., Asai, M., Tsukita, K., Kutoku, Y., Ohsawa, Y., Sunada, Y., Imamura, K., Egawa, N., Yahata, N., Okita, K., Takahashi, K., Asaka, I., Aoi, T., Watanabe, A., Watanabe, K., Kadoya, C., Nakano, R., Watanabe, D., Maruyama, K., … Inoue, H. (2013). Modeling Alzheimer's disease with iPSCs reveals stress phenotypes associated with intracellular Aβ and differential drug responsiveness. Cell Stem Cell, 12, 487-496.
Lachance, V., Wang, Q., Sweet, E., Choi, I., Cai, C. Z., Zhuang, X. X., Zhang, Y., Jiang, J. L., Blitzer, R. D., Bozdagi-Gunal, O., Zhang, B., Lu, J. H., & Yue, Z. (2019). Autophagy protein NRBF2 has reduced expression in Alzheimer's brains and modulates memory and amyloid-beta homeostasis in mice. Molecular Neurodegeneration, 14, 1-13.
Long, J. M., & Holtzman, D. M. (2019). Alzheimer disease: An update on pathobiology and treatment strategies. Cell, 179, 312-339.
Minakaki, G., Menges, S., Kittel, A., et al. (2018). Autophagy inhibition promotes SNCA/alpha-synuclein release and transfer via extracellular vesicles with a hybrid autophagosome-exosome-like phenotype. Autophagy, 14, 98-119.
Mizushima, N. (2004). Methods for monitoring autophagy. International Journal of Biochemistry and Cell Biology, 36, 2491-2502.
Nilsson, P., Loganathan, K., Sekiguchi, M., Matsuba, Y., Hui, K., Tsubuki, S., Tanaka, M., Iwata, N., Saito, T., & Saido, T. C. (2013). Aβ secretion and plaque formation depend on autophagy. Cell Reports, 5, 61-69.
Nixon, R. A. (2007). Autophagy, amyloidogenesis and Alzheimer disease. Journal of Cell Science, 120, 4081-4091.
Nixon, R. A., Wegiel, J., Kumar, A., Yu, W. H., Peterhoff, C., Cataldo, A., & Cuervo, A. M. (2005). Extensive involvement of autophagy in Alzheimer disease: An immuno-electron microscopy study. Journal of Neuropathology and Experimental Neurology, 64, 113-122.
Pickford, F., Masliah, E., Britschgi, M., Lucin, K., Narasimhan, R., Jaeger, P. A., Small, S., Spencer, B., Rockenstein, E., Levine, B., & Wyss-Coray, T. (2008). The autophagy-related protein beclin 1 shows reduced expression in early Alzheimer disease and regulates amyloid β accumulation in mice. Journal of Clinical Investigation, 118, 2190-2199.
Reggiori, F., & Ungermann, C. (2017). Autophagosome maturation and fusion. Journal of Molecular Biology, 429, 486-496.
Saman, S., Kim, W. H., Raya, M., Visnick, Y., Miro, S., Saman, S., Jackson, B., McKee, A. C., Alvarez, V. E., Lee, N. C. Y., & Hall, G. F. (2012). Exosome-associated tau is secreted in tauopathy models and is selectively phosphorylated in cerebrospinal fluid in early Alzheimer disease. Journal of Biological Chemistry, 287, 3842-3849.
Selkoe, D. J., & Hardy, J. (2016). The amyloid hypothesis of Alzheimer's disease at 25 years. EMBO Molecular Medicine, 8, 595-608.
Shehata, M., Matsumura, H., Okubo-Suzuki, R., Ohkawa, N., & Inokuchi, K. (2012). Neuronal stimulation induces autophagy in hippocampal neurons that is involved in AMPA receptor degradation after chemical long-term depression. Journal of Neuroscience, 32, 10413-10422.
Shen, H., Zhu, H., Panja, D., Gu, Q., & Li, Z. (2020). Autophagy controls the induction and developmental decline of NMDAR-LTD through endocytic recycling. Nature Communications, 11, 2979.
Uddin, M. S., Al Mamun, A., Labu, Z. K., Hidalgo-Lanussa, O., Barreto, G. E., & Ashraf, G. M. (2019). Autophagic dysfunction in Alzheimer's disease: Cellular and molecular mechanistic approaches to halt Alzheimer's pathogenesis. Journal of Cellular Physiology, 234, 8094-8112.
Whyte, L. S., Hassiotis, S., Hattersley, K. J., Hemsley, K. M., Hopwood, J. J., Lau, A. A., & Sargeant, T. J. (2020). Lysosomal dysregulation in the murine AppNL-G-F/NL-G-F model of Alzheimer's disease. Neuroscience, 429, 143-155.
Yang, D. S., Stavrides, P., Mohan, P. S., Kaushik, S., Kumar, A., Ohno, M., Schmidt, S. D., Wesson, D., Bandyopadhyay, U., Jiang, Y., Pawlik, M., Peterhoff, C. M., Yang, A. J., Wilson, D. A., St George-Hyslop, P., Westaway, D., Mathews, P. M., Levy, E., Cuervo, A. M., & Nixon, R. A. (2011). Reversal of autophagy dysfunction in the TgCRND8 mouse model of Alzheimer's disease ameliorates amyloid pathologies and memory deficits. Brain, 134, 258-277.
Yoshida, H., Okada, T., Haze, K., Yanagi, H., Yura, T., Negishi, M., & Mori, K. (2001). Endoplasmic reticulum stress-induced formation of transcription factor complex ERSF including NF-Y (CBF) and activating transcription factors 6α and 6β that activates the mammalian unfolded protein response. Molecular and Cellular Biology, 21, 1239-1248.

Auteurs

Keiro Shirotani (K)

Department of Genome-Based Drug Discovery, Graduate School of Biomedical Sciences, Nagasaki University, Nagasaki, Japan.
Leading Medical Research Core Unit, Graduate School of Biomedical Sciences, Nagasaki University, Nagasaki, Japan.
Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Agency (JST), Saitama, Japan.

Kaori Watanabe (K)

Department of Genome-Based Drug Discovery, Graduate School of Biomedical Sciences, Nagasaki University, Nagasaki, Japan.

Daisuke Hatta (D)

Department of Genome-Based Drug Discovery, Graduate School of Biomedical Sciences, Nagasaki University, Nagasaki, Japan.

Yumiko Kutoku (Y)

Department of Neurology, Kawasaki Medical School, Okayama, Japan.

Yutaka Ohsawa (Y)

Department of Neurology, Kawasaki Medical School, Okayama, Japan.

Yoshihide Sunada (Y)

Department of Neurology, Kawasaki Medical School, Okayama, Japan.

Takayuki Kondo (T)

Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Agency (JST), Saitama, Japan.
Center for iPS Cell Research and Application (CiRA), Kyoto University, Kyoto, Japan.

Haruhisa Inoue (H)

Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Agency (JST), Saitama, Japan.
Center for iPS Cell Research and Application (CiRA), Kyoto University, Kyoto, Japan.

Nobuhisa Iwata (N)

Department of Genome-Based Drug Discovery, Graduate School of Biomedical Sciences, Nagasaki University, Nagasaki, Japan.
Leading Medical Research Core Unit, Graduate School of Biomedical Sciences, Nagasaki University, Nagasaki, Japan.
Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Agency (JST), Saitama, Japan.

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