Cited by 625Autophagy in Disease and TherapyHematopoietic Stem Cell TransplantationFOXO transcription factor regulation

The DOI matches its Crossref record; 40 of the 40 references it cites were found in a registry or an index.

FOXO3A directs a protective autophagy program in haematopoietic stem cells

Open access

Warr, Matthew R., Binnewies, Mikhail, Flach, Johanna, Reynaud, Damien, Garg, Trit, Malhotra, Ritu, Debnath, Jayanta, Passegué, Emmanuelle·2013·Nature

DOI 10.1038/nature11895PMC PMC3579002

Open this paper in CoChat — free account

Abstract

Blood production is ensured by rare, self-renewing haematopoietic stem cells (HSCs). How HSCs accommodate the diverse cellular stresses associated with their life-long activity remains elusive. Here we identify autophagy as an essential mechanism protecting HSCs from metabolic stress. We show that mouse HSCs, in contrast to their short-lived myeloid progeny, robustly induce autophagy after ex vivo cytokine withdrawal and in vivo calorie restriction. We demonstrate that FOXO3A is critical to maintain a gene expression program that poises HSCs for rapid induction of autophagy upon starvation. Notably, we find that old HSCs retain an intact FOXO3A-driven pro-autophagy gene program, and that ongoing autophagy is needed to mitigate an energy crisis and allow their survival. Our results demonstrate that autophagy is essential for the life-long maintenance of the HSC compartment and for supporting an old, failing blood system.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1038/nature11895

Cites

40 of 40 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cell Death
Danial, N. N., & Korsmeyer, S. J. (2004) · Cell · doi:10.1016/s0092-8674(04)00046-7 · Cited by 4,651
Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours
Donehower, L. A., Harvey, M., Slagle, B. L., McArthur, M. J., Montgomery, C. A., Butel, J. S., & Bradley, A. (1992) · Nature · doi:10.1038/356215a0 · Cited by 4,649
Methods in Mammalian Autophagy Research
Mizushima, N., Yoshimori, T., & Levine, B. (2010) · Cell · doi:10.1016/j.cell.2010.01.028 · Cited by 4,497
Self-eating and self-killing: crosstalk between autophagy and apoptosis
Maiuri, M. C., Zalckvar, E., Kimchi, A., & Kroemer, G. (2007) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2239 · Cited by 3,638
Regulation mechanisms and signaling pathways of autophagy
He, C., & Klionsky, D. J. (2009) · Annual Review of Genetics · doi:10.1146/annurev-genet-102808-114910 · Cited by 3,609
Autophagy in immunity and inflammation
Levine, B., Mizushima, N., & Virgin, H. W. (2011) · Nature · doi:10.1038/nature09782 · Cited by 3,289
Hematopoiesis: An Evolving Paradigm for Stem Cell Biology
Orkin, S. H., & Zon, L. I. (2008) · Cell · doi:10.1016/j.cell.2008.01.025 · Cited by 2,570
Autophagy and Aging
Rubinsztein, D. C., Mariño, G., & Kroemer, G. (2011) · Cell · doi:10.1016/j.cell.2011.07.030 · Cited by 2,107
In Vivo Analysis of Autophagy in Response to Nutrient Starvation Using Transgenic Mice Expressing a Fluorescent Autophagosome Marker
Mizushima, N., Yamamoto, A., Matsui, M., Yoshimori, T., & Ohsumi, Y. (2004) · Molecular Biology of the Cell · doi:10.1091/mbc.e03-09-0704 · Cited by 2,105
FoxO3 Controls Autophagy in Skeletal Muscle In Vivo
Mammucari, C., Milan, G., Romanello, V., Masiero, E., Rudolf, R., Del Piccolo, P., Burden, S. J., Di Lisi, R., Sandri, C., Zhao, J., et al. (2007) · Cell Metabolism · doi:10.1016/j.cmet.2007.11.001 · Cited by 1,953

Show all 40 references

Sorted by citations

Items 101–200 of 620

Losing Sense of Self and Surroundings: Hematopoietic Stem Cell Aging and Leukemic Transformation
Verovskaya, E. V., Dellorusso, P. V., & Passegue, E. A. (2019) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2019.04.006 · Cited by 130
Hematopoietic stem cells through the ages: A lifetime of adaptation to organismal demands
Kasbekar, M., Mitchell, C. A., Proven, M. A., & Passegue, E. A. (2023) · Cell stem cell · doi:10.1016/j.stem.2023.09.013 · Cited by 130
Metabolic regulation of the hallmarks of stem cell biology
Jackson, B. T., & Finley, L. W. S. (2024) · Cell stem cell · doi:10.1016/j.stem.2024.01.003 · Cited by 132
SGK1 inhibition induces autophagy-dependent apoptosis via the mTOR-Foxo3a pathway
Liu, W., Wang, X., Liu, Z., Wang, Y., Yin, B., Pan, Y., Duan, X., Liao, Z., Chen, Y., Liu, C., et al. (2017) · British Journal of Cancer · doi:10.1038/bjc.2017.293 · Cited by 121
Loss of the selective autophagy receptor p62 impairs murine myeloid leukemia progression and mitophagy
Nguyen, T. D., Shaid, S., Vakhrusheva, O., Koschade, S. E., Klann, K., Thölken, M., Baker, F., Zhang, J., Oellerich, T., Sürün, D., et al. (2018) · Blood · doi:10.1182/blood-2018-02-833475 · Cited by 122
Sphingolipid Modulation Activates Proteostasis Programs to Govern Human Hematopoietic Stem Cell Self-Renewal
Xie, S. Z.-J., García‐Prat, L., Voisin, V., Ferrari, R., Gan, O. I., Wagenblast, E., Kaufmann, K. B., Zeng, A. G. X., Takayanagi, S., Patel, I., et al. (2019) · Cell stem cell · doi:10.1016/j.stem.2019.09.008 · Cited by 120
Autophagy induction promoted by m6A reader YTHDF3 through translation upregulation of FOXO3 mRNA
Hao, W.-C., Dian, M., Zhou, Y., Zhong, Q., Pang, W., Li, Z., Zhao, Y., Ma, J., Lin, X., Luo, R., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-32963-0 · Cited by 115
Replication stress caused by low MCM expression limits fetal erythropoiesis and hematopoietic stem cell functionality
Álvarez, S., Díaz, M., Flach, J., Rodríguez‐Acebes, S., Lopez-Contreras, A. J., Martínez, D., Cañamero, M., Fernández-Capetillo, Ó., Isern, J., Passegue, E. A., et al. (2015) · Nature Communications · doi:10.1038/ncomms9548 · Cited by 115
Self-citation
Intercellular Transfer of Microvesicles from Young Mesenchymal Stromal Cells Rejuvenates Aged Murine Hematopoietic Stem Cells
Kulkarni, R. S., Bajaj, M. S., Ghode, S. S., Jalnapurkar, S. S., Limaye, L. S., & Kale, V. P. (2017) · Stem Cells · doi:10.1002/stem.2756 · Cited by 111
Drug discovery for Diamond-Blackfan anemia using reprogrammed hematopoietic progenitors
Doulatov, S. R., Vo, L. T., Macari, E. R., Wahlster, L., Kinney, M. A., Taylor, A. M., Barragan, J., Gupta, M., McGrath, K. E., Lee, H., et al. (2017) · Science Translational Medicine · doi:10.1126/scitranslmed.aah5645 · Cited by 105
C10ORF10/DEPP-mediated ROS accumulation is a critical modulator of FOXO3-induced autophagy
Salcher, S., Hermann, M., Kiechl‐Kohlendorfer, U., Ausserlechner, M. J., & Obexer, P. (2017) · Molecular Cancer · doi:10.1186/s12943-017-0661-4 · Cited by 107
The Role of Autophagy in the Maintenance of Stemness and Differentiation of Mesenchymal Stem Cells
Sbrana, F. V., Cortini, M., Avnet, S., Perut, F., Columbaro, M., Milito, A. D., & Baldini, N. (2016) · Stem Cell Reviews and Reports · doi:10.1007/s12015-016-9690-4 · Cited by 108
The physiological roles of autophagy in the mammalian life cycle
Wang, L., Ye, X., & Zhao, T. (2018) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12464 · Cited by 105
Modest Declines in Proteome Quality Impair Hematopoietic Stem Cell Self-Renewal
Jose, L. H. S., Sunshine, M. J., Dillingham, C. H., Chua, B. A., Krutá, M., Hong, Y., Hatters, D. M., & Signer, R. A. J. (2020) · Cell Reports · doi:10.1016/j.celrep.2019.12.003 · Cited by 106
FOXO3 determines the accumulation of α-synuclein and controls the fate of dopaminergic neurons in the substantia nigra
Pino, E., Amamoto, R., Zheng, L., Cacquevel, M., Sarria, J. ‐. F., Knott, G. W., & Schneider, B. L. (2013) · Human Molecular Genetics · doi:10.1093/hmg/ddt530 · Cited by 105
Transcriptomic profile of leg muscle during early growth in chicken
Xue, Q., Zhang, G., Li, T., Ling, J., Zhang, X., & Wang, J. (2017) · PLoS ONE · doi:10.1371/journal.pone.0173824 · Cited by 101
Mitochondrial Role in Stemness and Differentiation of Hematopoietic Stem Cells
Papa, L., Djedaini, M., & Hoffman, R. (2019) · Stem Cells International · doi:10.1155/2019/4067162 · Cited by 108
The Role of MicroRNAs in Chemoresistance
Bahreini, F., & Rezaei, N. (2023) · Springer eBooks · doi:10.1007/978-3-030-80962-1_336-1 · Cited by 100
The role of interferon-gamma in hematopoietic stem cell development, homeostasis, and disease
Morales-Mantilla, D. E., & King, K. Y. (2018) · Current Stem Cell Reports · doi:10.1007/s40778-018-0139-3 · Cited by 99
Autophagy maintains the stemness of ovarian cancer stem cells by FOXA2.
Peng, Q., Qin, J., Zhang, Y., Cheng, X., Wang, X., Lü, W., Xie, X., & Zhang, S. (2017) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-017-0644-8 · Cited by 101
The MicroRNA-132 and MicroRNA-212 Cluster Regulates Hematopoietic Stem Cell Maintenance and Survival with Age by Buffering FOXO3 Expression
Mehta, A., Zhao, J. L., Sinha, N., Marinov, G. K., Mann, M., Kowalczyk, M. S., Galimidi, R. P., Du, X., Erikci, E., Regev, A., et al. (2015) · Immunity · doi:10.1016/j.immuni.2015.05.017 · Cited by 95
Roles of microRNA-34a targeting SIRT1 in mesenchymal stem cells
Zhang, F., Cui, J., Liu, X., Lv, B., Liu, X., Xie, Z., & Yu, B. (2015) · Stem Cell Research & Therapy · doi:10.1186/s13287-015-0187-x · Cited by 99
The Impact of Chemotherapy on the Ovaries: Molecular Aspects and the Prevention of Ovarian Damage
Sonigo, C., Beau, I., Binart, N., & Grynberg, M. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20215342 · Cited by 101
Decline in biological resilience as key manifestation of aging: Potential mechanisms and role in health and longevity
Ukraintseva, S. V., Arbeev, K. G., Duan, M., Akushevich, I. V., Kulminski, A. M., Stallard, E., & Yashin, A. I. (2020) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2020.111418 · Cited by 100
Bone Marrow Niches of Hematopoietic Stem and Progenitor Cells
Kandarakov, O. F., Belyavsky, A. V., & Semenova, E. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23084462 · Cited by 107
Control of Inflammation by Calorie Restriction Mimetics: On the Crossroad of Autophagy and Mitochondria
Gabandé‐Rodríguez, E., Heras, M. M. G. D. L., & Mittelbrunn, M. (2019) · Cells · doi:10.3390/cells9010082 · Cited by 101
The links between AKT and two intracellular proteolytic cascades: Ubiquitination and autophagy
Noguchi, M., Hirata, N., & Suizu, F. (2014) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2014.07.013 · Cited by 99
Aging and Regeneration in Vertebrates
Sousounis, K., Baddour, J., & Tsonis, P. A. (2014) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/b978-0-12-391498-9.00008-5 · Cited by 96
Autophagy in acute leukemias: A double-edged sword with important therapeutic implications
Evangelisti, C., Evangelisti, C., Chiarini, F., Lonetti, A., Buontempo, F., Neri, L. M., McCubrey, J. A., & Martelli, A. M. (2014) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2014.09.023 · Cited by 96
Low-Dose Irradiation Promotes Persistent Oxidative Stress and Decreases Self-Renewal in Hematopoietic Stem Cells
Rodrigues-Moreira, S., Moreno, S. G., Ghinatti, G., Lewandowski, D., Hoffschir, F., Ferri, F., Gallouët, A.-S., Gay, D. L., Motohashi, H., Yamamoto, M. P., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.09.013 · Cited by 99
An ERK-Dependent Feedback Mechanism Prevents Hematopoietic Stem Cell Exhaustion
Baumgärtner, C., Toifl, S., Farlik, M., Halbritter, F., Scheicher, R., Fischer, I., Sexl, V., Bock, C., & Baccarini, M. (2018) · Cell stem cell · doi:10.1016/j.stem.2018.05.003 · Cited by 99
Hematopoietic stem cell fate through metabolic control
Ito, K., & Ito, K. (2018) · Experimental Hematology · doi:10.1016/j.exphem.2018.05.005 · Cited by 98
FOXO3‐mTOR metabolic cooperation in the regulation of erythroid cell maturation and homeostasis
Zhang, X., Campreciós, G., Rimmelé, P., Liang, R. H.-S., Yalcin, S., Mungamuri, S. K., Barminko, J., d’Escamard, V., Baron, M. H., Brugnara, C., et al. (2014) · American Journal of Hematology · doi:10.1002/ajh.23786 · Cited by 100
Molecular Mechanisms Underlying Autophagy-Mediated Treatment Resistance in Cancer
Ho, C. J., & Gorski, S. M. (2019) · Cancers · doi:10.3390/cancers11111775 · Cited by 93
Inhibition of autophagy as a treatment strategy for p53 wild-type acute myeloid leukemia
Folkerts, H., Hilgendorf, S., Wierenga, A. T. J., Jaques, J., Mulder, A. B., Coffer, P. J., Schuringa, J. J., & Vellenga, E. (2017) · Cell Death and Disease · doi:10.1038/cddis.2017.317 · Cited by 91
Oxidative Stress and ROS-Mediated Signaling in Leukemia: Novel Promising Perspectives to Eradicate Chemoresistant Cells in Myeloid Leukemia
Trombetti, S., Cesaro, E., Catapano, R., Sessa, R., Bianco, A. L., Izzo, P., & Grosso, M. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22052470 · Cited by 91
Autophagy and the kidney: health and disease
Takabatake, Y., Kimura, T., Takahashi, A., & Isaka, Y. (2014) · Nephrology Dialysis Transplantation · doi:10.1093/ndt/gft535 · Cited by 92
Quiescence Entry, Maintenance, and Exit in Adult Stem Cells
Mohammad, K., Dakik, P., Medkour, Y., Mitrofanova, D., & Titorenko, V. I. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20092158 · Cited by 94
Overexpression of FoxO3a is associated with glioblastoma progression and predicts poor patient prognosis
Qian, Z., Ren, L., Wu, D., Yang, X., Zhou, Z., Nie, Q., Jiang, G., Xue, S., Weng, W., Qiu, Y., et al. (2017) · International Journal of Cancer · doi:10.1002/ijc.30690 · Cited by 88
Aging and brain rejuvenation as systemic events
Bouchard, J. J., & Villeda, S. (2014) · Journal of Neurochemistry · doi:10.1111/jnc.12969 · Cited by 90
Autophagy Proteins ATG5 and ATG7 Are Essential for the Maintenance of Human CD34+ Hematopoietic Stem-Progenitor Cells
Gomez‐Puerto, M. C., Folkerts, H., Wierenga, A. T. J., Schepers, K., Schuringa, J. J., Coffer, P. J., & Vellenga, E. (2016) · Stem Cells · doi:10.1002/stem.2347 · Cited by 90
IGF2 Preserves Osteosarcoma Cell Survival by Creating an Autophagic State of Dormancy That Protects Cells against Chemotherapeutic Stress
Shimizu, T., Sugihara, E., Yamaguchi‐Iwai, S., Tamaki, S., Koyama, Y., Kamel, W., Ueki, A., Ishikawa, T., Chiyoda, T., Osuka, S., et al. (2014) · Cancer Research · doi:10.1158/0008-5472.can-14-0914 · Cited by 87
Cytoprotective autophagy maintains leukemia-initiating cells in murine myeloid leukemia
Sumitomo, Y., Koya, J., Nakazaki, K., Kataoka, K., Tsuruta-Kishino, T., Morita, K., Sato, T., & Kurokawa, M. (2016) · Blood · doi:10.1182/blood-2015-12-684696 · Cited by 89
p73 regulates autophagy and hepatocellular lipid metabolism through a transcriptional activation of the ATG5 gene
He, Z., Liu, H., Agostini, M., Yousefi, S., Perren, A. A., Tschan, M. P., Mak, T. W., Melino, G., & Simon, H. (2013) · Cell Death and Differentiation · doi:10.1038/cdd.2013.104 · Cited by 87
Efficient Promotion of Autophagy and Angiogenesis Using Mesenchymal Stem Cell Therapy Enhanced by the Low-Energy Shock Waves in the Treatment of Erectile Dysfunction
Zhu, G., Jeon, S. H., Bae, W. J., Choi, S. W., Jeong, H. C., Kim, K. S., Kim, S. J., Cho, H. J., Ha, U., Hong, S., et al. (2018) · Stem Cells International · doi:10.1155/2018/1302672 · Cited by 83
Enhanced viability and function of mesenchymal stromal cell spheroids is mediated via autophagy induction
Regmi, S., Raut, P. K., Pathak, S., Shrestha, P. S., Park, P., & Jeong, J. (2020) · Autophagy · doi:10.1080/15548627.2020.1850608 · Cited by 84
Autophagy of cancer stem cells is involved with chemoresistance of colon cancer cells
Wu, S., Wang, X., Chen, J.-X., & Chen, Y. (2013) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2013.04.053 · Cited by 80
Metabolism as master of hematopoietic stem cell fate
Ito, K., Bonora, M., & Ito, K. (2018) · International Journal of Hematology · doi:10.1007/s12185-018-2534-z · Cited by 85
Distinct role of autophagy on angiogenesis: highlights on the effect of autophagy in endothelial lineage and progenitor cells
Hassanpour, M., Rezabakhsh, A., Pezeshkian, M., Rahbarghazi‬, R., & Nouri, M. (2018) · Stem Cell Research & Therapy · doi:10.1186/s13287-018-1060-5 · Cited by 80
Phosphoinositide 3-kinases as accelerators and brakes of autophagy
O’Farrell, F., Rusten, T. E., & Stenmark, H. (2013) · FEBS Journal · doi:10.1111/febs.12486 · Cited by 81
ROS-Induced CXCR4 Signaling Regulates Mantle Cell Lymphoma (MCL) Cell Survival and Drug Resistance in the Bone Marrow Microenvironment via Autophagy
Chen, Z., Teo, A. E., & McCarty, N. (2015) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-15-0987 · Cited by 81
Autophagy induction is a survival response against oxidative stress in bone marrow–derived mesenchymal stromal cells
Song, C., Song, C., & Tong, F. (2014) · Cytotherapy · doi:10.1016/j.jcyt.2014.04.006 · Cited by 79
Reduced FoxO3a expression causes low autophagy in idiopathic pulmonary fibrosis fibroblasts on collagen matrices
Im, J., Hergert, P. J., & Nho, R. S. (2015) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00079.2015 · Cited by 79
Normal Hematopoiesis Is a Balancing Act of Self-Renewal and RegenerationPreprint
Olson, O. C., Kang, Y.-A., & Passegue, E. A. (2020) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a035519 · Cited by 89
Biology of Tendon Stem Cells and Tendon in Aging
Lui, P. P. Y., & Wong, C. M. (2020) · Frontiers in Genetics · doi:10.3389/fgene.2019.01338 · Cited by 77
Interaction between epigenetic and metabolism in aging stem cells
Brunet, A., & Rando, T. A. (2017) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2016.12.009 · Cited by 79
Developing therapeutic approaches for metachromatic leukodystrophy
Maegawa, G. H. B., & Patil, P. (2013) · Drug Design Development and Therapy · doi:10.2147/dddt.s15467 · Cited by 75
FoxO Transcription Factors: Applicability as a Novel Immune Cell Regulators and Therapeutic Targets in Oxidative Stress-Related Diseases
Kim, M. E., Kim, D. H., & Lee, J. S. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms231911877 · Cited by 77
Hematopoietic stem cells preferentially traffic misfolded proteins to aggresomes and depend on aggrephagy to maintain protein homeostasis
Chua, B. A., Lennan, C., Sunshine, M. J., Dreifke, D., Chawla, A., Bennett, E. J., & Signer, R. A. J. (2023) · Cell stem cell · doi:10.1016/j.stem.2023.02.010 · Cited by 74
Autophagy induction by leptin contributes to suppression of apoptosis in cancer cells and xenograft model: Involvement of p53/FoxO3A axis
Nepal, S., Kim, M. J., Hong, J. T., Kim, S. H., Sohn, D., Lee, S. H., Song, K., Choi, D. Y., Lee, E. S., & Park, P. (2015) · Oncotarget · doi:10.18632/oncotarget.3347 · Cited by 74
Autophagy in Stem Cell Biology: A Perspective on Stem Cell Self-Renewal and Differentiation
Chen, X., He, Y., & Lu, F. (2018) · Stem Cells International · doi:10.1155/2018/9131397 · Cited by 73
Autophagy in stem and progenitor cells
Rodolfo, C., Bartolomeo, S. D., & Cecconi, F. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-015-2071-3 · Cited by 72
A Systems Approach Identifies Essential FOXO3 Functions at Key Steps of Terminal Erythropoiesis
Liang, R. H.-S., Campreciós, G., Kou, Y., McGrath, K. E., Nowak, R. B., Catherman, S. C., Bigarella, C. L., Rimmelé, P., Zhang, X., Gnanapragasam, M. N., et al. (2015) · PLoS Genetics · doi:10.1371/journal.pgen.1005526 · Cited by 75
Mechanistic roles of autophagy in hematopoietic differentiation
Riffelmacher, T., & Simon, A. K. (2016) · FEBS Journal · doi:10.1111/febs.13962 · Cited by 75
Atg5 Is Essential for the Development and Survival of Innate Lymphocytes
O’Sullivan, T. E., Geary, C. D., Weizman, O.-E., Geiger, T. L., Rapp, M., Dorn, G. W., Overholtzer, M., & Sun, J. C.-Y. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.04.082 · Cited by 76
AMP-activated protein kinase α1 promotes atherogenesis by increasing monocyte-to-macrophage differentiation
Zhang, M., Zhu, H., Ding, Y., Liu, Z., Cai, Z., & Zou, M. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.m117.779447 · Cited by 70
Hematopoietic Stem Cell Factors: Their Functional Role in Self-Renewal and Clinical Aspects
Mann, Z., Sengar, M., Verma, Y. K., Rajalingam, R., & Raghav, P. K. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.664261 · Cited by 69
Aging of the hematopoietic system
Snoeck, H. (2013) · Current Opinion in Hematology · doi:10.1097/moh.0b013e3283623c77 · Cited by 73
A Genome-Wide mRNA Screen and Functional Analysis Reveal FOXO3 as a Candidate Gene for Chicken Growth
Chen, B., Xu, J., He, X., Xu, H., Li, G., Du, H., Nie, Q., & Zhang, X. (2015) · PLoS ONE · doi:10.1371/journal.pone.0137087 · Cited by 71
Targeting mTOR signaling by polyphenols: A new therapeutic target for ageing
Pazoki–Toroudi, H., Amani, H., Ajami, M., Nabavi, S. F., Braidy, N., Kasi, P. D., & Nabavi, S. M. (2016) · Ageing Research Reviews · doi:10.1016/j.arr.2016.07.004 · Cited by 70
Uromodulin p.Cys147Trp mutation drives kidney disease by activating ER stress and apoptosis
Johnson, B. G., Dang, L. T. H., Marsh, G. A., Roach, A. M., Levine, Z. G., Monti, A., Reyon, D., Feigenbaum, L., & Duffield, J. S. (2017) · Journal of Clinical Investigation · doi:10.1172/jci93817 · Cited by 68
Mitophagy in hematopoietic stem cells
Joshi, A., & Kundu, M. (2013) · Autophagy · doi:10.4161/auto.26681 · Cited by 72
microRNA-143 is associated with the survival of ALDH1 + CD133 + osteosarcoma cells and the chemoresistance of osteosarcoma
Zhou, J., Wu, S., Chen, Y., Zhao, J., Zhang, K., Wang, J., & Chen, S. (2015) · Experimental Biology and Medicine · doi:10.1177/1535370214563893 · Cited by 66
Autophagy and cell reprogramming
Wang, S., Xia, P., Rehm, M., & Fan, Z. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-014-1829-3 · Cited by 66
Low Autophagy (ATG) Gene Expression Is Associated with an Immature AML Blast Cell Phenotype and Can Be Restored during AML Differentiation Therapy
Jin, J., Britschgi, A., Schläfli, A. M., Humbert, M., Shan-Krauer, D., Batliner, J., Federzoni, E. A., Ernst, M., Torbett, B. E., Yousefi, S., et al. (2018) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2018/1482795 · Cited by 50
Autophagy contributes to the enrichment and survival of colorectal cancer stem cells under oxaliplatin treatment
Yang, H., Ma, Y., Zhou, Y., Xu, L., Chen, X., Ding, W., & Zou, H. (2015) · Cancer Letters · doi:10.1016/j.canlet.2015.02.045 · Cited by 69
Emerging roles of autophagy in metabolism and metabolic disorders
Rocchi, A., & He, C. (2015) · Frontiers in Biology · doi:10.1007/s11515-015-1354-2 · Cited by 66
Autophagy maintains stem cells and intestinal homeostasis in Drosophila
Nagy, P., Sándor, G. O., & Juhász, G. (2018) · Scientific Reports · doi:10.1038/s41598-018-23065-3 · Cited by 65
Current Outlook on Autophagy in Human Leukemia: Foe in Cancer Stem Cells and Drug Resistance, Friend in New Therapeutic Interventions
Rothe, K., Porter, V., & Jiang, X. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20030461 · Cited by 67
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 66
Autophagy as a Therapeutic Target to Enhance Aged Muscle Regeneration
Lee, D. E., Bareja, A., Bartlett, D. B., & White, J. P. (2019) · Cells · doi:10.3390/cells8020183 · Cited by 65
Physiological Systems in Promoting Frailty
Perazza, L. R., Brown‐Borg, H. M., & Thompson, L. V. (2022) · Comprehensive physiology · doi:10.1002/cphy.c210034 · Cited by 69
NPM1 Mutant Mediated PML Delocalization and Stabilization Enhances Autophagy and Cell Survival in Leukemic Cells
Zou, Q., Tan, S., Yang, Z., Zhan, Q., Jin, H., Xian, J., Zhang, S., Yang, L., Wang, L., & Zhang, L. (2017) · Theranostics · doi:10.7150/thno.19439 · Cited by 66
Autophagy counters inflammation-driven glycolytic impairment in aging hematopoietic stem cells
Dellorusso, P. V., Proven, M. A., Calero‐Nieto, F. J., Wang, X., Mitchell, C. A., Hartmann, F. J., Amouzgar, M., Favaro, P. M. B., DeVilbiss, A., Swann, J. W., et al. (2024) · Cell stem cell · doi:10.1016/j.stem.2024.04.020 · Cited by 66
Resilient and resourceful: Genome maintenance strategies in hematopoietic stem cells
Bakker, S. T., & Passegue, E. A. (2013) · Experimental Hematology · doi:10.1016/j.exphem.2013.09.007 · Cited by 67
Role of OSGIN1 in mediating smoking-induced autophagy in the human airway epithelium
Wang, G., Zhou, H., Strulovici‐Barel, Y., Al-Hijji, M. A., Ou, X., Salit, J., Walters, M. S., Staudt, M. R., Kaner, R. J., & Crystal, R. G. (2017) · Autophagy · doi:10.1080/15548627.2017.1301327 · Cited by 63
Autophagy and cancer cell metabolism
Anderson, C. M., & Macleod, K. F. (2019) · International review of cytology · doi:10.1016/bs.ircmb.2019.06.002 · Cited by 63
Deficient autophagy in epithelial stem cells drives aging in the freshwater cnidarian Hydra
Tomczyk, S., Schenkelaars, Q., Suknovic, N., Wenger, Y., Ekundayo, K., Buzgariu, W., Bauer, C. R., Fischer, K. E., Austad, S. N., & Galliot, B. (2019) · Development · doi:10.1242/dev.177840 · Cited by 61
SIRT3 Activation a Promise in Drug Development? New Insights into SIRT3 Biology and Its Implications on the Drug Discovery Process
Lambona, C., Zwergel, C., Valente, S., & Mai, A. (2024) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.3c01979 · Cited by 66
The exosome complex establishes a barricade to erythroid maturation
McIver, S. C., Kang, Y.-A., DeVilbiss, A., O’Driscoll, C. A., Ouellette, J. N., Pope, N. J., Campreciós, G., Chang, C.-J., Yang, D. T., Bouhassira, E. E., et al. (2014) · Blood · doi:10.1182/blood-2014-04-571083 · Cited by 62
Hematopoietic Stem Cell Regulation by Type I and II Interferons in the Pathogenesis of Acquired Aplastic Anemia
Smith, J. N. P., Kanwar, V. S., & MacNamara, K. C. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00330 · Cited by 62
Nutritional Regulation of Intestinal Stem Cells
Alonso, S., & Yilmaz, Ö. H. (2018) · Annual Review of Nutrition · doi:10.1146/annurev-nutr-082117-051644 · Cited by 66
OGT Regulates Hematopoietic Stem Cell Maintenance via PINK1-Dependent Mitophagy
Murakami, K., Kurotaki, D., Kawase, W., Soma, S., Fukuchi, Y., Kunimoto, H., Yoshimi, R., Koide, S., Oshima, M., Hishiki, T., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2020.108579 · Cited by 62
Cellular Mechanisms of Somatic Stem Cell Aging
Jung, Y., & Brack, A. S. (2014) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/b978-0-12-416022-4.00014-7 · Cited by 63
Extinguishing the Embers: Targeting AML Metabolism
Culp‐Hill, R., D’Alessandro, A., & Pietras, E. M. (2020) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2020.10.001 · Cited by 66
High autophagic flux guards ESC identity through coordinating autophagy machinery gene program by FOXO1
Liu, P., Liu, K., Gu, H., Wang, W., Gong, J., Zhu, Y., Zhao, Q., Cao, J., Han, C., Gao, F., et al. (2017) · Cell Death & Differentiation · doi:10.1038/cdd.2017.90 · Cited by 58
Regulation of Apoptosis by Autophagy to Enhance Cancer Therapy.
Tompkins, K. D., & Thorburn, A. M. (2019) · Europe PMC (PubMed Central) · Cited by 59
Selective insulin resistance in hepatocyte senescence
Aravinthan, A. D., Challis, B., Shannon, N. B., Hoare, M., Heaney, J., & Alexander, G. (2014) · Experimental Cell Research · doi:10.1016/j.yexcr.2014.09.025 · Cited by 58
Autophagy-dependent regulatory T cells are critical for the control of graft-versus-host disease
Texier, L. L., Lineburg, K. E., Cao, B., McDonald-Hyman, C. S., Leveque, L., Nicholls, J., Melino, M., Nalkurthi, B. C., Alexander, K. A., Teal, B. E., et al. (2016) · JCI Insight · doi:10.1172/jci.insight.86850 · Cited by 58
Targeting reactive oxygen species in stem cells for bone therapy
Li, X., Li, B., Shi, Y., Wang, C., & Ye, L. (2021) · Drug Discovery Today · doi:10.1016/j.drudis.2021.03.002 · Cited by 57

Authors: Warr, M. R., Binnewies, M., Flach, J., Reynaud, D., Garg, T., Malhotra, R., Debnath, J., & Passegué, E.
Affiliations: University of California, San Francisco (US)
ORCID: Warr, Matthew R.
Binnewies, Mikhail
Flach, Johanna
Reynaud, Damien
Debnath, Jayanta
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2013-02
Volume: 494
Issue: 7437
Pages: 323-327
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature11895
PMC: PMC3579002
OpenAlex: W2055807959
Cited by: 625
References: 40
Citations by year: 2026: 28 · 2025: 28 · 2024: 36 · 2023: 39 · 2022: 42 · 2021: 48 · 2020: 46 · 2019: 54 · 2018: 57 · 2017: 60 · 2016: 55 · 2015: 54 · 2014: 47 · 2013: 31
FWCI: 44.99
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
eScholarship (California Digital Library) (submittedVersion, cc-by-nc-nd)
RePEc: Research Papers in Economics (submittedVersion)
eScholarship (California Digital Library) (submittedVersion)
Funders: Tokyo Medical and Dental University
National Institutes of Health
University of California, San Francisco
National Heart, Lung, and Blood Institute (HL092471, R01HL111266, R01HL092471)
National Cancer Institute (R01CA184014, CA126792, R01CA126792)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › FOXO transcription factor regulation
Keywords: FOXO3, autophagy, hematopoietic stem cells, metabolic stress, caloric restriction, cytokine withdrawal, aging, energy crisis, HSC self-renewal
MeSH terms: Forkhead Box Protein O3, Aging, Animals, Autophagy, Cell Survival, Energy Metabolism, Food Deprivation, Gene Expression Regulation, Hematopoietic Stem Cells, Homeostasis, Mice, Inbred C57BL, Stress, Physiological, Cytokines, Cellular Senescence, Apoptosis, Caloric Restriction, Mice, Forkhead Transcription Factors

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

FOXO3A directs a protective autophagy program in haematopoietic stem cells

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks