FoxO Function Is Essential for Maintenance of Autophagic Flux and Neuronal Morphogenesis in Adult Neurogenesis
Open accessAbstract
Autophagy is a conserved catabolic pathway with emerging functions in mammalian neurodevelopment and human neurodevelopmental diseases. The mechanisms controlling autophagy in neuronal development are not fully understood. Here, we found that conditional deletion of the Forkhead Box O transcription factors FoxO1, FoxO3, and FoxO4 strongly impaired autophagic flux in developing neurons of the adult mouse hippocampus. Moreover, FoxO deficiency led to altered dendritic morphology, increased spine density, and aberrant spine positioning in adult-generated neurons. Strikingly, pharmacological induction of autophagy was sufficient to correct abnormal dendrite and spine development of FoxO-deficient neurons. Collectively, these findings reveal a novel link between FoxO transcription factors, autophagic flux, and maturation of developing neurons.
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FOXO factors may be critical in distinguishing different states of quiescence, perhaps by connecting quiescence to clearing mechanisms, including autophagy.
“FOXO factors may be critical in distinguishing different states of quiescence, perhaps by connecting quiescence to clearing mechanisms, including autophagy91,92.”
From Ageing and rejuvenation of tissue stem cells and their niches (2023) · cites this paper as [91]
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“To this end, we retrovirally overexpressed a dominant-negative mutant of the mTOR activator Rheb GTPase, Rheb, which powerfully inhibits mTOR activity (Tabancay et al., 2003).”
A FOXO–Pak1 transcriptional pathway controls neuronal polarityPreprint
de la Torre-Ubieta, L., Gaudilliere, B. L., Yang, Y., Ikeuchi, Y., Yamada, T., DiBacco, S., Stegmüller, J., Schüller, U., Salih, D. A. M., Rowitch, D. H., et al. (2010) · Genes & Development · doi:10.1101/gad.1880510 · Cited by 97 · see citing works
In vivo imaging of dendritic pruning in dentate granule cells
Gonçalves, J. T., Bloyd, C. W., Shtrahman, M., Johnston, S. T., Schafer, S. T., Parylak, S., Tran, T., Chang, T., & Gage, F. H. (2016) · Nature Neuroscience · doi:10.1038/nn.4301 · Cited by 97 · cited 5× · see citing works
“In vivo, treatment with pharmacological inducers of autophagy may have also affected the function of neurogenic niche cells, which provide regulatory signals for the development of adultgenerated neurons (Gonçalves et al., 2016a).”
InfluentialTian, Y., Voineagu, I., Paşca, S. P., Won, H., Chandran, V., Horvath, S., Dolmetsch, R. E., & Geschwind, D. H. (2014) · Genome Medicine · doi:10.1186/s13073-014-0075-5 · Cited by 93 · see citing works
Feliciano, D. M., Lin, T. V., Hartman, N. W., Bartley, C. M., Kubera, C., Hsieh, L. S., Lafourcade, C., O’Keefe, R. A., & Bordey, A. (2013) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2013.02.008 · Cited by 93 · cited 1× · see citing works
“Overall, the mTOR inhibitor rapamycin and the mTOR-independent inducer of autophagy trehalose were equally powerful in rescuing the FoxO-phenotype, indicating that the FoxO-phenotype was caused by impaired autophagic activity and not by autophagy-independent functions of the hyperactivatedmTOR pathway (Feliciano et al…”
Neural Stem Cell of the Hippocampus
Rolando, C., & Taylor, V. (2014) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/b978-0-12-416022-4.00007-x · Cited by 90 · cited 1× · see citing works
“Moreover, there is evidence that impaired adult neurogenesis contributes to the pathogenesis of cognitive and behavioral deficits in aging and neuropsychiatric diseases (Abrous and Wojtowicz, 2015; Rolando and Taylor, 2014).”
Xi, Y., Dhaliwal, J., Ceizar, M., Vaculik, M., Kumar, K. L., & Lagace, D. C. (2016) · Cell Death and Disease · doi:10.1038/cddis.2015.406 · Cited by 87 · cited 2× · see citing works
“A previous study investigated the function of autophagy in adult-born DG neuron development through knockout of the autophagy-related gene Atg5 and observed only a transient decrease in spine numbers and no alteration of dendrite morphology (Xi et al., 2016).”
The Crucial Role of Atg5 in Cortical Neurogenesis During Early Brain Development
Lv, X., Jiang, H., Li, B., Liang, Q., Wang, S., Zhao, Q., & Jiao, J. (2014) · Scientific Reports · doi:10.1038/srep06010 · Cited by 83 · cited 1× · see citing works
“Deletion of different autophagy genes in the same cell type can produce divergent outcomes (Li et al., 2016; Lv et al., 2014; Vázquez et al., 2012; Wang et al., 2016, 2017; Wu et al., 2016; Yazdankhah et al., 2014).”
Park, J. M., Tougeron, D., Huang, S., Okamoto, K., & Sinicrope, F. A. (2014) · PLoS ONE · doi:10.1371/journal.pone.0100819 · Cited by 76 · cited 1× · see citing works
“Autophagy can directly target spines and degrade organelles such as centrosomes and mitochondria, whose activity has recently been linked to neuronal morphogenesis and spine development (Beckervordersandforth et al., 2017; Li et al., 2004; Nikoletopoulou et al., 2017; Park et al., 2014; Ploumi et al., 2017; Steib et a…”
Formation and maturation of autophagosomes in higher eukaryotes: a social network
Zhao, Y. G., & Zhang, H. (2018) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2018.04.003 · Cited by 71 · see citing works
Transcription-Factor-Dependent Control of Adult Hippocampal NeurogenesisPreprint
Beckervordersandforth, R., Zhang, C., & Lie, D. C. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a018879 · Cited by 70 · see citing works
Self-citationWang, C., Chen, S., Yeo, S., Karsli-Uzunbas, G., White, E., Mizushima, N., Virgin, H. W., & Guan, J.-L. (2016) · Journal of Cell Biology · doi:10.1083/jcb.201507023 · Cited by 69 · see citing works
FOXO protects against age‐progressive axonal degeneration
Hwang, I., Oh, H., Santo, E. E., Kim, D., Chen, J. W., Bronson, R. T., Locasale, J. W., Na, Y., Lee, J., Reed, S., et al. (2017) · Aging Cell · doi:10.1111/acel.12701 · Cited by 64 · cited 5× · see citing works
“Notably, FoxO expression is not confined to NSPCs but is observed throughout the adult DG (Hwang et al., 2018; Renault et al., 2009), raising the possibility that FoxOs have a function in later steps of the adult neurogenic sequence.”
InfluentialSelf-citationThe Ever-Changing Morphology of Hippocampal Granule Neurons in Physiology and Pathology
Llorens-Martı́n, M., Rábano, A., & Ávila, J. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00526 · Cited by 61 · cited 2× · see citing works
“Absence of the apical dendrite of adult-born DG neurons was suggested as a common sign of cellular stress in the developing DG neuron (Llorens-Martı́n et al., 2016), raising the possibility that the dendritic phenotype may primarily reflect cellular stress due to loss of FoxO-dependent autophagy (Webb and Brunet, 2014…”
Rapamycin Treatment Improves Neuron Viability in an In Vitro Model of Stroke
Fletcher, L., Evans, T., Watts, L., Jimenez, D., & Digicaylioglu, M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0068281 · Cited by 54 · cited 1× · see citing works
“For activation, we used the mTOR inhibitor rapamycin and the mTOR-independent autophagy activator trehalose (DeBosch et al., 2016; Fletcher et al., 2013; Mayer et al., 2016; Sarkar et al., 2007) (for experimental scheme, see Figure S4I).”
MethodDoxycycline increases neurogenesis and reduces microglia in the adult hippocampus
Sultan, S., Gebara, E., & Toni, N. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00131 · Cited by 53 · see citing works
Bai, L., Mei, X., Shen, Z., Bi, Y., Yuan, Y., Guo, Z., Wang, H., Zhao, H., Zhou, Z., Wang, C., et al. (2017) · Scientific Reports · doi:10.1038/srep42288 · Cited by 51 · cited 1× · see citing works
“mTOR kinase activity suppresses the ALP by negatively regulating autophagosome formation and is used as an additional indirect indicator of ALP activity (Bai et al., 2017; Boland et al., 2008; Zhang et al., 2017).”
EVA1A/TMEM166 Regulates Embryonic Neurogenesis by Autophagy
Li, M., Lu, G. X., Hu, J. N., Shen, X., Ju, J., Gao, Y., Qu, L., Xia, Y., Chen, Y., & Bai, Y. (2016) · Stem Cell Reports · doi:10.1016/j.stemcr.2016.01.011 · Cited by 49 · cited 1× · see citing works
“Deletion of different autophagy genes in the same cell type can produce divergent outcomes (Li et al., 2016; Lv et al., 2014; Vázquez et al., 2012; Wang et al., 2016, 2017; Wu et al., 2016; Yazdankhah et al., 2014).”
Jungenitz, T., Radic, T., Jedlička, P., & Schwarzacher, S. W. (2013) · Cerebral Cortex · doi:10.1093/cercor/bht035 · Cited by 47 · cited 1× · see citing works
“Expression of the immediate early gene c-fos is associated with neuronal activity and is commonly used as a proxy for the functional incorporation of adult-born neurons into the hippocampal circuit (Jungenitz et al., 2014; Kee et al., 2007; McAvoy et al., 2016).”
Autophagy controls centrosome number by degrading Cep63
Watanabe, Y., Honda, S., Konishi, A., Arakawa, S., Murohashi, M., Yamaguchi, H., Torii, S., Tanabe, M., Tanaka, S., Warabi, E., et al. (2016) · Nature Communications · doi:10.1038/ncomms13508 · Cited by 38 · see citing works
Wang, C., Yeo, S. K., Haas, M. A., & Guan, J. (2017) · The Journal of Cell Biology · doi:10.1083/jcb.201609093 · Cited by 37 · cited 1× · see citing works
“Finally, impaired autophagy was described to affect interaction of the postnatal neurogenic lineage with microglia (Wang et al., 2017).”
GSK3β Controls mTOR and Prosurvival Signaling in Neurons
Urbańska, M., Góźdź, A., Macias, M., Cymerman, I. A., Liszewska, E., Kondratiuk, I., Devijver, H., Lechat, B., LEUVEN, F. V., & Jaworski, J. (2017) · Molecular Neurobiology · doi:10.1007/s12035-017-0823-9 · Cited by 25 · cited 2× · see citing works
“In vivo, however, Rheb caused death of adult-generated neurons prior to the time points for analysis of the dendrite and spine compartment—potentially because of the prolonged massive inhibition of the mTOR pathway (Urbanska et al., 2018), which precluded further analysis of the impact of cell-autonomous induction of…”
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RNA m6A methylation regulates sorafenib resistance in liver cancer through FOXO3‐mediated autophagy
Lin, Z., Niu, Y., Wan, A. H., Chen, D., Liang, H., Chen, X., Sun, L., Zhan, S., Chen, L., Cheng, C., et al. (2020) · The EMBO Journal · doi:10.15252/embj.2019103181 · Cited by 442 · see citing works
“…that FOXO3 controls autophagy in neuronal development, and FOXO3 deficiency induced autophagy to correct abnormal dendrite and spine development (Schaffner et al , 2018), which is consistent with our results that down-regulation of FOXO3 triggers autophagy signaling pathway in liver tumor…”
Ageing and rejuvenation of tissue stem cells and their niches
Brunet, A., Goodell, M. A., & Rando, T. A. (2023) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-022-00510-w · Cited by 407 · see citing works
Quiescence of Adult Mammalian Neural Stem Cells: A Highly Regulated Rest
Urbán, N., Blomfield, I. M., & Guillemot, F. (2019) · Neuron · doi:10.1016/j.neuron.2019.09.026 · Cited by 370 · see citing works
Formation and integration of new neurons in the adult hippocampus
Denoth‐Lippuner, A., & Jessberger, S. (2021) · Nature reviews. Neuroscience · doi:10.1038/s41583-021-00433-z · Cited by 274 · see citing works
The FoxO–Autophagy Axis in Health and Disease
Cheng, Z. (2019) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2019.07.009 · Cited by 257 · see citing works
Aging and Rejuvenation of Neural Stem Cells and Their Niches
Navarro Negredo, P., Yeo, R. W., & Brunet, A. (2020) · Cell Stem Cell · doi:10.1016/j.stem.2020.07.002 · Cited by 246 · see citing works
FOXO transcription factors as mediators of stress adaptation
Colman, M. J. R., Dansen, T. B., & Burgering, B. M. T. (2023) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-023-00649-0 · Cited by 225 · see citing works
“Foxo3 deletion drives premature neural stem cell differentiation, resulting in the depletion of the neural stem cell pool and brain development defects 142,143,152,153 .”
Li, K., Deng, Y., Deng, G., Chen, P., Wang, Y., Wu, H., Ji, Z., Yao, Z., Zhang, X., Yu, B., et al. (2020) · Stem Cell Research & Therapy · doi:10.1186/s13287-020-01643-5 · Cited by 168 · see citing works
Pan, H., Wang, Y., Na, K., Wang, Y., Wang, L., Li, Z., Guo, C., Guo, D., & Wang, X. (2019) · Cell Death and Disease · doi:10.1038/s41419-019-1653-7 · Cited by 161 · see citing works
Audesse, A. J., Dhakal, S., Hassell, L.-A., Gardell, Z., Nemtsova, Y., & Webb, A. E. (2019) · PLOS Genetics · doi:10.1371/journal.pgen.1008097 · Cited by 155 · see citing works
Self-citationRole of FoxO transcription factors in aging and age-related metabolic and neurodegenerative diseases
Du, S., & Zheng, H. (2021) · Cell & Bioscience · doi:10.1186/s13578-021-00700-7 · Cited by 140 · see citing works
Sirtuins and FoxOs in osteoporosis and osteoarthritis
Almeida, M., & Porter, R. M. (2019) · Bone · doi:10.1016/j.bone.2019.01.018 · Cited by 129 · see citing works
SUMMERS, K. M., Bush, S. J., & Hume, D. A. (2020) · PLoS Biology · doi:10.1371/journal.pbio.3000859 · Cited by 111 · see citing works
Mei, Z., Huang, Y.-G., Feng, Z., Luo, Y.-N., Yang, S., Du, L., Jiang, K., Liu, X., Fu, X., Deng, Y., et al. (2020) · Aging · doi:10.18632/aging.103420 · Cited by 113 · see citing works
The Endolysosomal System and Proteostasis: From Development to Degeneration
Winckler, B., Faúndez, V., Maday, S., Cai, Q., Almeida, C. G., & Zhang, H. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.1665-18.2018 · Cited by 105 · see citing works
Autophagy in Neuronal Development and Plasticity
Fleming, A., & Rubinsztein, D. C. (2020) · Trends in Neurosciences · doi:10.1016/j.tins.2020.07.003 · Cited by 93 · see citing works
S100A11 Promotes Liver Steatosis via FOXO1-Mediated Autophagy and Lipogenesis
Zhang, L., Zhang, Z., Li, C., Zhu, T., Gao, J. X., Zhou, H., Zheng, Y., Chang, Q., Wang, M., Wu, J., et al. (2020) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2020.10.006 · Cited by 91 · see citing works
Karmon, G., Sragovich, S., Hacohen-Kleiman, G., Ben-Horin-Hazak, I., Kašpárek, P., Schuster, B., Sedláček, R., Pasmanik‐Chor, M., Theotokis, P., Touloumi, O., et al. (2021) · Biological Psychiatry · doi:10.1016/j.biopsych.2021.09.018 · Cited by 75 · see citing works
The Multifaceted Functions of Autophagy in Breast Cancer Development and Treatment
Niklaus, N. J., Tokarchuk, I., Zbinden, M., Schläfli, A. M., Maycotte, P., & Tschan, M. P. (2021) · Cells · doi:10.3390/cells10061447 · Cited by 75 · see citing works
Matsubara, S., Matsuda, T., & Nakashima, K. (2021) · Cells · doi:10.3390/cells10051145 · Cited by 70 · see citing works
Leschik, J., Lutz, B., & Gentile, A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22147339 · Cited by 70 · see citing works
Autophagy and Breast Cancer: Connected in Growth, Progression, and Therapy
Wu, Q., & Sharma, D. (2023) · Cells · doi:10.3390/cells12081156 · Cited by 69 · see citing works
Autophagy deficiency in neurodevelopmental disorders
Deng, Z., Zhou, X., Lu, J., & Yue, Z. (2021) · Cell & Bioscience · doi:10.1186/s13578-021-00726-x · Cited by 64 · see citing works
“FOXO1/3/4 deficiency leads to altered dendrite and spine development of adult-generated neurons and impaired long-term survival eventually [70].”
BackgroundInfluentialConserved and Divergent Features of Adult Neurogenesis in Zebrafish
Labusch, M., Mancini, L., Morizet, D., & Bally‐Cuif, L. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00525 · Cited by 60 · see citing works
Yan, D., Yang, Y., Lang, J., Wang, X., Huang, Y., Meng, J., Wu, J., Zeng, X., Li, H., Ma, H., et al. (2023) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2023.114872 · Cited by 56 · see citing works
Mechanisms of enhanced quiescence in neural stem cell aging
Audesse, A. J., & Webb, A. E. (2020) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2020.111323 · Cited by 53 · see citing works
Self-citationMetabolic control of adult neural stem cell self-renewal by the mitochondrial protease YME1L
Wani, G. A., Sprenger, H., Ndoci, K., Chandragiri, S., Acton, R., Schatton, D., Kochan, S. M. V., Sakthivelu, V., Jevtic, M., Seeger, J. M., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110370 · Cited by 53 · see citing works
De novo DNA methylation controls neuronal maturation during adult hippocampal neurogenesis
Zocher, S., Overall, R. W., Berdugo‐Vega, G., Rund, N., Karasinsky, A., Adusumilli, V. S., Steinhauer, C., Scheibenstock, S., Händler, K., Schultze, J. L., et al. (2021) · The EMBO Journal · doi:10.15252/embj.2020107100 · Cited by 51 · see citing works
“Although a number of transcription factors controlling this process have been identified (Beckervordersandforth et al , 2015; Mukherjee et al , 2016; Sch € affner et al , 2018), the epigenetic machinery which enables the molecular changes required for the generation of functional neurons from NSPCs…”
Elucidating the Possible Role of FoxO in Depression
Rana, T., Behl, T., Sehgal, A., Mehta, V., Singh, S., Sharma, N., & BUNGAU, S. G. (2021) · Neurochemical Research · doi:10.1007/s11064-021-03364-4 · Cited by 51 · see citing works
The Role of Autophagy in Osteoarthritic Cartilage
Kao, W.-C., Chen, J., Liu, P., Lu, C., Lin, S., Chuang, S., Wu, S., Chang, L.-H., Lee, M., Yang, C., et al. (2022) · Biomolecules · doi:10.3390/biom12101357 · Cited by 46 · see citing works
“Promotion of autophagic gene expression by FOXOs has occurred in neurons, muscle and even hematopoietic stem cells [67,68], and there is FOXO3 which elicit autophagy in chondrocytes of mouse and human [69].”
BackgroundHuang, Z., Chen, Y., Guo, H., & Chen, G. (2021) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2021.630876 · Cited by 47 · see citing works
Roles of forkhead box O (FoxO) transcription factors in neurodegenerative diseases: A panoramic view
Hu, W., Yang, Z. P., Yang, W., Han, M., Xu, B., Yu, Z., Shen, M., & Yang, Y. (2019) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2019.101645 · Cited by 43 · see citing works
Zhu, J.-W., Zou, M.-M., Li, Y.-F., Chen, W.-J., Liu, J.-C., Chen, H., Fang, L., Zhang, Y., Wang, Z.-T., Chen, J.-B., et al. (2019) · Cerebral Cortex · doi:10.1093/cercor/bhz306 · Cited by 41 · see citing works
“Mice lacking mTOR show smaller brain, which is contributed by both the reduced numbers of neural progenitor cells (NPCs) and the smaller size of neurons (Cloetta et al. 2013; Ka et al. 2014; Ka et al. 2017).”
BackgroundInfluentialDu, S., Jin, F., Maneix, L., Gedam, M., Xu, Y., Catic, A., Wang, M. C., & Zheng, H. (2021) · Aging Cell · doi:10.1111/acel.13432 · Cited by 42 · see citing works
“FoxO3 deletion drives NSC differentiation, resulting in the depletion of the NSC pool (Paik et al., 2009; Renault et al., 2009; Schäffner et al., 2018; Yeo et al., 2013).”
BackgroundNazio, F., Pò, A., Abballe, L., Ballabio, C., Diomedi‐Camassei, F., Bordi, M., Camera, A., Caruso, S., Caruana, I., Pezzullo, M., et al. (2021) · Acta Neuropathologica · doi:10.1007/s00401-021-02347-7 · Cited by 40 · see citing works
“Interestingly, FOXOs have been reported to regulate gene expression of a large number of genes encoding proteins involved in autophagy [81, 96].”
BackgroundWang, C., Haas, M., Yeo, S. K., Sebti, S., Fernández, Á. F., Zou, Z., Levine, B., & Guan, J. (2021) · Autophagy · doi:10.1080/15548627.2021.1936358 · Cited by 37 · see citing works
“In this study, we found that higher autophagy could eliminate dysfunctional mitochondria (mitophagy) [47] to reduce aberrant ROS accumulation in old NSCs (Figure 5), which might be associated with increased maintenance and functions of aged NSCs in KI mice.”
BackgroundLiu, S., Hu, Y., Xu, W., Liu, W., Wang, B., Zeng, X., Shao, Z., Cao, Y., Xiong, L., & Cai, X. (2024) · Autophagy · doi:10.1080/15548627.2024.2440844 · Cited by 39 · see citing works
“Autophagic flux was analyzed by tandem mRFP-GFP-LC3 adenoviral vectors (HanBio, HB-AP210 000) as previously described [44].”
Ma, R., Zhou, G., Qu, M., Yi, J., Tang, Y., Yang, X., Nie, Y., & Gu, H. (2019) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.13212 · Cited by 38 · see citing works
Akt Regulates Sox10 Expression to Control Oligodendrocyte Differentiation via Phosphorylating FoxO1
Wang, H., Liu, M., Ye, Z., Zhou, C., Bi, H., Wang, L., Zhang, C., Fu, H. Q., Shen, Y., Yang, J., et al. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.2432-20.2021 · Cited by 38 · see citing works
Guo, Y., Shen, M., Dong, Q., Méndez-Albelo, N. M., Huang, S. X., Sirois, C. L., Le, J., Li, M., Jarzembowski, E. D., Schoeller, K. A., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-39337-0 · Cited by 39 · see citing works
Oli, V., Gupta, R. V., & Kumar, P. (2021) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2021.102012 · Cited by 36 · see citing works
Tang, F., Wang, J., Itokazu, Y., & Yu, R. K. (2020) · Journal of Neurochemistry · doi:10.1111/jnc.15137 · Cited by 35 · see citing works
Gillotin, S., Sahni, V., Lepko, T., Hanspal, M. A., Swartz, J., Alexopoulou, Z., & Marshall, F. H. (2021) · Ageing Research Reviews · doi:10.1016/j.arr.2021.101447 · Cited by 32 · see citing works
Zhang, R., Ma, Z., Liu, K., Li, Y., Liu, D., Xu, L., Deng, X., Qu, R., Ma, Z., & Ma, S. (2019) · Life Sciences · doi:10.1016/j.lfs.2019.02.033 · Cited by 34 · see citing works
Autophagy Deficiency Leads to Impaired Antioxidant Defense via p62-FOXO1/3 Axis
Zhao, L., Li, H., Wang, Y., Zheng, A., Cao, L., & Liu, J. (2019) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2019/2526314 · Cited by 34 · see citing works
“FOXOs are also considered as an upstream modulator of autophagy; for instance, conditional deletion of FOXOs strongly impairs autophagic flux in adult neurogenesis [51].”
BackgroundOxidative stress sensing and response in neural stem cell fate
Hwang, I., Tang, D., & Paik, J. (2021) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2021.03.043 · Cited by 32 · see citing works
Self-citationSefiani, A., & Geoffroy, C. G. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.682259 · Cited by 31 · see citing works
Zhang, S.-Q., Deng, Q., Zhu, Q., Hu, Z., Long, L., Wu, P., He, J., Chen, H.-S., Yue, Z., Lu, J., et al. (2023) · Cell Discovery · doi:10.1038/s41421-023-00583-7 · Cited by 32 · see citing works
“Schaffner et al. have found that conditional knockout of FOXOs in aNSCs impair autophagic fl ux and results in altered dendritic morphology and increased spine density in newborn neurons 37 .”
BackgroundMethodDas, S., Murumulla, L., Ghosh, P., & Challa, S. (2025) · BioMetals · doi:10.1007/s10534-025-00665-x · Cited by 31 · see citing works
“This disruption leads to altered dendritic morphology, increased spine density, and abnormal spine positioning in adult-born neurons, underscoring the critical role of FoxOs in brain development through the regulation of autophagy in neural stem cells (Schäffner et al. 2018; Vilchez et al. 2013).”
The endocrine role of bone: Novel functions of bone-derived cytokines
Wang, H., Zheng, X.-Q., Zhang, Y., Huang, J., Zhou, W., Li, X., Tian, H., Wang, B., Xing, D., Fu, W., et al. (2020) · Biochemical Pharmacology · doi:10.1016/j.bcp.2020.114308 · Cited by 29 · see citing works
Lysosomes and signaling pathways for maintenance of quiescence in adult neural stem cells
Kobayashi, T., & Kageyama, R. (2021) · The FEBS Journal · doi:10.1111/febs.15555 · Cited by 28 · see citing works
Homeostatic Roles of the Proteostasis Network in Dendrites
Lottes, E. N., & Cox, D. N. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.00264 · Cited by 26 · see citing works
“In mammals, decreased autophagy can lead to increased spine density but a decrease in total dendritic length via shortening of the apical dendrite in mouse dentate gyrus neurons (Schäffner et al., 2018) – whether that is an overall increase or decrease in arbor complexity is unclear.”
BackgroundBoecker, C. A., & Holzbaur, E. L. F. (2019) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2019.01.005 · Cited by 28 · see citing works
Maybury‐Lewis, S. Y., Brown, A. K., Yeary, M., Sloutskin, A., Dhakal, S., Juven‐Gershon, T., & Webb, A. E. (2021) · Aging Cell · doi:10.1111/acel.13499 · Cited by 27 · see citing works
Self-citationA Single-Cell Transcriptomic Analysis of the Mouse Hippocampus After Voluntary Exercise
Methi, A., Islam, R., Kaurani, L., Sakib, M. S., Krüger, D. M., Peña, T., Burkhardt, S., Liebetanz, D., & Fischer, A. (2024) · Molecular Neurobiology · doi:10.1007/s12035-023-03869-9 · Cited by 30 · see citing works
“…Zfhx2 which is involved in neuronal differentiation [105], and Foxo1 which regulates the long-term maintenance of adult neural stem cells and belongs to the FoxO family that plays an important role in the maintenance of autophagic flux and neuronal morphogenesis in adult neurogenesis [106, 107].”
Poe, A. R., Xu, Y., Zhang, C., Lei, J., Li, K., Labib, D., & Han, C. (2020) · eLife · doi:10.7554/elife.53351 · Cited by 26 · see citing works
Compressive force‐induced LincRNA‐p21 inhibits mineralization of cementoblasts by impeding autophagy
Liu, H., Huang, Y., Yang, Y., Han, Y., Jia, L., & Li, W. (2021) · The FASEB Journal · doi:10.1096/fj.202101589r · Cited by 26 · see citing works
Regulation of autophagy gene expression and its implications in cancer
Metur, S. P., Lei, Y., Zhang, Z., & Klionsky, D. J. (2023) · Journal of Cell Science · doi:10.1242/jcs.260631 · Cited by 26 · see citing works
Autophagy in neural stem cells and glia for brain health and diseases
Nagayach, A., & Wang, C. (2023) · Neural Regeneration Research · doi:10.4103/1673-5374.382227 · Cited by 25 · see citing works
“Recent evidence also confirms a critical role of FoxOs in brain development via the regulation of autophagy in NSCs (Schäffner et al., 2018).”
Rasetto, N. B., Giacomini, D., Berardino, A. A., Waichman, T. V., Beckel, M. S., Bella, D. J. D., Brown, J. R., Davies-Sala, M. G., Gerhardinger, C., Lie, D. C., et al. (2024) · Science Advances · doi:10.1126/sciadv.adp6039 · Cited by 24 · see citing works
Self-citationMitochondrial and Autophagic Regulation of Adult Neurogenesis in the Healthy and Diseased Brain
Büeler, H. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22073342 · Cited by 24 · see citing works
“Although autophagy is necessary for adult neurogenesis under physiological conditions [98,99,101,103], pathologically increased autophagy can be detrimental to AHN and may be involved in development of stress-induced cognitive and affective dysfunction.”
BackgroundMolecular modulation of autophagy: New venture to target resistant cancer stem cells
Mandhair, H. K., Arambasic, M., Novak, U., & Radpour, R. (2020) · World Journal of Stem Cells · doi:10.4252/wjsc.v12.i5.303 · Cited by 23 · see citing works
Nutrients and neurogenesis: the emerging role of autophagy and gut microbiota
Cavallucci, V., Fidaleo, M., & Pani, G. (2019) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2019.11.004 · Cited by 23 · see citing works
Jing, D., Wu, W., Deng, X., Peng, Y., Yang, W., Huang, D., Shao, Z., & Zheng, D. (2020) · Journal of Cellular Physiology · doi:10.1002/jcp.29895 · Cited by 23 · see citing works
“Abnormal FoxOs functions are related to several diseases, such as osteoarthritis and osteoporosis (Matsuzaki et al., 2018; Schaffner et al., 2018).”
BackgroundPARP1 inhibition protects mice against Japanese encephalitis virus infection
Desingu, P. A., Mishra, S., Dindi, L., Srinivasan, S., Rajmani, R. S., Ravi, V., Tamta, A. K., Raghu, S., Murugasamy, K., Pandit, A. S., et al. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.113103 · Cited by 23 · see citing works
Ghrelin mediated hippocampal neurogenesis.
Davies, J. (2022) · Vitamins and hormones · doi:10.1016/bs.vh.2021.12.003 · Cited by 12 · see citing works
Ansari, M. S., Chauhan, V., Singh, A. R. A. S. K., Akhtar, A., Chaudhary, N., Tyagi, R., Divya, Husain, K., Sheetal, S. S., Alam, R., et al. (2026) · Nature Communications · doi:10.1038/s41467-025-68272-5 · Cited by 19 · see citing works
Pandaram, A., Paul, J., Wankhar, W., Thakur, A., Verma, S., Vasudevan, K., Wankhar, D., Kammala, A. K., Sharma, P., Jaganathan, R., et al. (2024) · Biomedicines · doi:10.3390/biomedicines12040855 · Cited by 19 · see citing works
“They ensure the necessary proteins and signals are available while also preventing the accumulation of potentially toxic substances [60].”
BackgroundJiang, M. H., Vanan, S., Tu, H., Zhang, W., Zhang, Z.-W., Chia, S., Jang, S. E., Zeng, X., Yu, W., Xu, J., et al. (2020) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2020.07.031 · Cited by 19 · see citing works
Molecular Basis of Neuronal Autophagy in Ageing: Insights from Caenorhabditis elegans
Konstantinidis, G., & Tavernarakis, N. (2021) · Cells · doi:10.3390/cells10030694 · Cited by 18 · see citing works
FOXO Regulates Neuromuscular Junction Homeostasis During Drosophila Aging
Birnbaum, A., Sodders, M., Bouska, M. J., Chang, K., Kang, P., McNeill, E. M., & Bai, H. (2021) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2020.567861 · Cited by 18 · see citing works
“FOXOs can also function as regulators of neuronal homeostasis (Paik et al 2009; Kim and Webb 2017; Schaffner et al 2018).”
BackgroundFoxo1 selectively regulates static mechanical pain by interacting with Nav1.7
Zhang, X., Lai, R.-C., Chen, Z., Zhong, X., Cao, X., Zhang, X., Xiao, Y.-B., Wang, J., Liu, X., & Xie, M.-X. (2020) · Pain · doi:10.1097/j.pain.0000000000002055 · Cited by 15 · see citing works
“Among them, Foxo1 plays a pivotal role in the development, autophagy, morphogenesis, and stress responses of the nervous system.(24,40,45,55,58) In hippocampal neurons, Foxo1 is necessary for the maturation of excitatory synapses,(45) which is the structural basis for the generation of action potentials and neuronal e…”
BackgroundSánchez-Ramírez, E., Ung, T. P. L., Stringari, C., & Aguilar‐Arnal, L. (2024) · Molecular Neurobiology · doi:10.1007/s12035-024-04006-w · Cited by 15 · see citing works
“Along these lines, maintaining low ROS levels in NPC is also influenced by the fork-head box O (FoxO) family of transcription factors, which tightly control metabolic fluxes and sustain redox balance in these cells [76, 77], and autophagy rates in developing and adult neurons [78].”
BackgroundSun, F., Wang, J., Meng, L., Zhou, Z., Xu, Y., Yang, M., Li, Y., Jiang, T., Liu, B., & Yan, H. (2024) · British Journal of Pharmacology · doi:10.1111/bph.16400 · Cited by 15 · see citing works
“…findings are consistent with previous reports that autophagy deficiency leads to A β deposition, impaired neurogenesis, and neuronal development (Hara et al., 2006; Komatsu et al., 2006), while activated autophagy is beneficial (Kannangara & Lagace, 2018; Schaffner et al., 2018; Wani et al., 2019).”
Schäffner, I., Wittmann, M., Vogel, T., & Lie, D. C. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01497-8 · Cited by 14 · see citing works
“and isolated the aNSPCs according to published protocols [32, 45, 46], which were modified by the use of the MACS neural tissue dissociation kit.”
MethodInfluentialSelf-citationSemkova, V., Haupt, S., Segschneider, M., Bell, C., Ingelman‐Sundberg, M., Hajo, M., Weykopf, B., Muthukottiappan, P., Till, A., & Brüstle, O. (2022) · Cells · doi:10.3390/cells11091388 · Cited by 15 · see citing works
Serum-Derived Neuronal Exosomal miRNAs as Biomarkers of Acute Severe Stress
Sung, M. K., Sung, S., Kang, K., Choi, J.-H., Lee, S., Kim, K., Lim, J., Lee, G. W., Rim, H.-D., Kim, B., et al. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22189960 · Cited by 13 · see citing works
“For example, Forkhead Box O (FoxO) deficiency is known to affect the development of neurons [64].”
BackgroundWang, B., Li, Y., Wang, H., Zhao, J., Zhao, Y., Liu, Z., & Ma, H. (2019) · Journal of Investigative Medicine · doi:10.1136/jim-2019-001145 · Cited by 13 · see citing works
Peinado, P. J., & Urbach, A. (2023) · Cells · doi:10.3390/cells12162086 · Cited by 12 · see citing works
Perez, Y., Velmeshev, D., Wang, L., White, M. L., Siebert, C., Baltazar, J., Zuo, G., Moriano, J., Chen, S., Steffen, D. M., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-61184-4 · Cited by 12 · see citing works
“We also found that FOXO3 , an essential determinant of neuronal morphogenesis and neuronal survival 42,43 , was enriched in dup15q L2_3 projection neurons of the ACC.”
Niego, A., & Benítez‐Burraco, A. (2020) · Autism · doi:10.1177/1362361320965074 · Cited by 12 · see citing works
Regulatory mechanisms of stem cell differentiation: Biotechnological applications for neurogenesis
Marques, B. L., Maciel, G. F., Júnior, M. R. D. B., Dias, L. D., Scalzo, S., Santos, A. K., Kihara, A. H., Santiago, H. C., Parreira, R. C., Birbrair, A., et al. (2022) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2022.09.014 · Cited by 12 · see citing works
Prosaposin maintains adult neural stem cells in a state associated with deep quiescence
Labusch, M., Thétiot, M., Than‐Trong, E., Morizet, D., Coolen, M., Varet, H., Legendre, R., Ortica, S., Mancini, L., & Bally‐Cuif, L. (2024) · Stem Cell Reports · doi:10.1016/j.stemcr.2024.02.007 · Cited by 10 · see citing works
FoxO3 Regulates the Progress and Development of Aging and Aging-Related Diseases
Chang, Z., He, Z., & Xia, J. (2022) · Current Molecular Medicine · doi:10.2174/1566524023666221014140817 · Cited by 9 · see citing works
Bonavita, R., Vitale, F., Verdicchio, L. V., Williams, S. V., Caporaso, M. G., Fleming, A., & Renna, M. (2025) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2025.1538377 · Cited by 8 · see citing works
FoxO3 Modulates Circadian Rhythms in Neural Stem Cells
Draijer, S., Timmerman, R., Pannekeet, J., van Harten, A., Farshadi, E. A., Kemmer, J., van Gilst, D., Chaves, I., & Hoekman, M. F. M. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241713662 · Cited by 7 · see citing works
Zhang, X., Gao, R., Yang, L., Zhu, Y., Zhang, T., Shen, X., Gu, W., Yang, L., & Peng, S. (2024) · Clinical and Translational Discovery · doi:10.1002/ctd2.287 · Cited by 7 · see citing works
Sun, T., Liu, J., Ding, J., Zhang, C., Zhang, Y.-W., Ma, Q., & Liu, Y. (2019) · Neural Regeneration Research · doi:10.4103/1673-5374.262597 · Cited by 7 · see citing works
“Other research and our previous data have indicated that adult neurogenesis occurs in the hippocampus (França, 2018; Schaffner et al., 2018).”
ResultEpigenetic regulation of neural stem cell aging in the mouse hippocampus by Setd8 downregulation
Matsubara, S., Matsuda‐Ito, K., Sekiryu, H., Doi, H., Nakagawa, T., Murao, N., Oda, H., Nakashima, K., & Matsuda, T. (2025) · The EMBO Journal · doi:10.1038/s44318-025-00455-8 · Cited by 6 · see citing works
The interplay between autophagy and unconventional secretion in neurodegeneration
Renna, M., Bonavita, R., Dixon, G., Verdicchio, L. V., & Fleming, A. (2026) · Cell chemical biology · doi:10.1016/j.chembiol.2025.12.007 · Cited by 6 · see citing works
Transcriptional control of embryonic and adult neural progenitor activity
Singh, N., Siebzehnrübl, F. A., & Martínez‐Garay, I. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1217596 · Cited by 6 · see citing works
Dominguez‐Martín, H., Gavilán, E., Parrado, C., Burguillos, M. Á., Daza, P., & Ruano, D. (2024) · Cells · doi:10.3390/cells13242069 · Cited by 7 · see citing works
Wang, J., Wang, Z., Dai, L., Zhu, X., Guan, X., Wang, J., Li, J., Zhang, M., Bai, Y., & Guo, H. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24033035 · Cited by 6 · see citing works
Is autism a PIN1 deficiency syndrome? A proposed etiological role for glyphosate
Seneff, S., Kyriakopoulos, A. M., & Nigh, G. (2024) · Journal of Neurochemistry · doi:10.1111/jnc.16140 · Cited by 6 · see citing works
“Conditional deletion of FoxO1, FoxO3, and FoxO4 strongly impairs autophagy in developing neu - rons in the hippocampus (Schäffner et al., 2018 ).”
Murtaj, V., Butti, E., Martino, G., & Panina‐Bordignon, P. (2023) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2023.1125785 · Cited by 8 · see citing works
Zhang, H., Kang, Y., Zhao, T., Huang, D., Hu, X., Di, J., Zhang, Y., Lu, Y., Huang, M., Li, H., et al. (2026) · Autophagy · doi:10.1080/15548627.2026.2619576 · Cited by 6 · see citing works
“As described in previous literature [46], the pmCherry-EGFP-LC3B plasmid was used to analyze autophagic flux.”
FOXO family and neurodegenerative diseases: Mechanisms of action and therapeutic potential
Lv, Z., Liu, X., Zhou, Z., Huang, Q., Liu, H., Xu, Z., & Xu, P. (2026) · Redox Biology · doi:10.1016/j.redox.2026.104218 · Cited by 5 · see citing works
Seo, J., Park, S., Lee, D. C., Yoo, W., Yang, Y. R., Seo, H. W., Park, J. L., Joo, J., Park, K. C., & Byun, S. (2026) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-026-02688-3 · Cited by 5 · see citing works
FOXO3 regulates a common genomic program in aging and glioblastoma stem cells
Audesse, A. J., Karashchuk, G., Gardell, Z. A., Lakis, N. S., Maybury‐Lewis, S. Y., Brown, A. K., Leeman, D. S., Teo, Y. V., Neretti, N., Anthony, D. C., et al. (2021) · Aging and Cancer · doi:10.1002/aac2.12043 · Cited by 5 · see citing works
Self-citationLi, L., Li, X., Han, R., Wu, M., Ma, Y., Chen, Y., Zhang, H., & Li, Y. (2023) · Pharmaceuticals · doi:10.3390/ph16050706 · Cited by 5 · see citing works
- Authors
- Schäffner, I., Minakaki, G., Khan, M. A., Balta, E.-A., Schlötzer-Schrehardt, U., Schwarz, T. J., Beckervordersandforth, R., Winner, B., Webb, A. E., DePinho, R. A., Paik, J., Wurst, W., Klucken, J., & Lie, D. C.
- Affiliations
- Friedrich-Alexander-Universität Erlangen-Nürnberg (DE)
- Helmholtz Munich (DE)
- Brown University (US)
- The University of Texas MD Anderson Cancer Center (US)
- Weill Cornell Medicine (US)
- German Center for Neurodegenerative Diseases (DE)
- Corresponding author
- Lie, D. Chichung
- ORCID
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2018-09
- Volume
- 99
- Issue
- 6
- Pages
- 1188-1203.e6
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC6186958
- OpenAlex
- W2891053351
- Cited by
- 145
- References
- 77
- Citations by year
- 2026: 11 · 2025: 19 · 2024: 13 · 2023: 18 · 2022: 16 · 2021: 30 · 2020: 22 · 2019: 14 · 2018: 2
- FWCI
- 6.05
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Site cant be reached (submittedVersion, other-oa)
- DZNE Pub (submittedVersion)
- Funders
- German Research Foundation (LI 858/6-3, 9-1, INST 410/45-1 FUGG, BE 5136/1-2, 2-1, KL 1395/8-1, WU 164/5-1, CRC870)
- Bavarian Research Network
- University Hospital Erlangen (E12, E16, E21, E25)
- German Federal Ministry of Education and Research (BMBF 01GQ113, 01GM1520A, 01EK1609B, Integrament 01ZX1314H)
- NIH (AG048284, AG053268)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › FOXO transcription factor regulation
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Keywords
- FOXO transcription factors, FOXO1, FOXO3, FOXO4, autophagic flux, autophagy, adult neurogenesis, hippocampus, neuronal morphogenesis, dendritic morphology, dendritic spines, conditional gene deletion, brain development
- MeSH terms
- Animals, Autophagy, Cell Separation, Cells, Cultured, Mice, Transgenic, Morphogenesis, Neurons, Forkhead Transcription Factors, Neurogenesis
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