The DOI matches its Crossref record; 30 of the 30 references it cites were found in a registry or an index.
Regulation of oxidative stress by ATM is required for self-renewal of haematopoietic stem cells
Abstract
The 'ataxia telangiectasia mutated' (Atm) gene maintains genomic stability by activating a key cell-cycle checkpoint in response to DNA damage, telomeric instability or oxidative stress. Mutational inactivation of the gene causes an autosomal recessive disorder, ataxia-telangiectasia, characterized by immunodeficiency, progressive cerebellar ataxia, oculocutaneous telangiectasia, defective spermatogenesis, premature ageing and a high incidence of lymphoma. Here we show that ATM has an essential function in the reconstitutive capacity of haematopoietic stem cells (HSCs) but is not as important for the proliferation or differentiation of progenitors, in a telomere-independent manner. Atm-/- mice older than 24 weeks showed progressive bone marrow failure resulting from a defect in HSC function that was associated with elevated reactive oxygen species. Treatment with anti-oxidative agents restored the reconstitutive capacity of Atm-/- HSCs, resulting in the prevention of bone marrow failure. Activation of the p16(INK4a)-retinoblastoma (Rb) gene product pathway in response to elevated reactive oxygen species led to the failure of Atm-/- HSCs. These results show that the self-renewal capacity of HSCs depends on ATM-mediated inhibition of oxidative stress.
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In the citing paper
“other studies have shown the potential of antioxidants to improve the function of old HSCs (76,96).”
From Causes, consequences, and reversal of immune system aging (2013) · cites this paper as [96]
In the citing paper
“in HSCs and neural stem cells (NSCs) of mice, excessive cellular ROS concentrations lead to abnormal proliferation, malignancy and compromised stem cell self-renewal11–14”
From Stem cell aging: mechanisms, regulators and therapeutic opportunities (2014) · cites this paper as [11]
In the citing paper
“experimentally induced genetic disruption of DDR pathways in mice also produces cell-autonomous defects in HSC function, as assayed by in vivo hematopoietic reconstitution and in vitro colony forming assays11,36,52,53.”
From Stem cell aging: mechanisms, regulators and therapeutic opportunities (2014) · cites this paper as [11]
In the citing paper
“age-dependent alterations in regulation of SOD2 by FoxO3 and the DNA damage sensing serine/threonine protein kinase ATM (ataxia-telangiectasia mutated) have been shown to contribute to loss of HSC function with aging11,16, 24.”
From Stem cell aging: mechanisms, regulators and therapeutic opportunities (2014) · cites this paper as [11]
In the citing paper
“Another potential function for ATM in suppressing progeroid phenotypes may be related to reported ATM functions in regulating intracellular ROS levels and sensitivity to these molecules (Barzilai et al., 2002; Ito et al., 2004”
From DNA Repair, Genome Stability, and Aging (2005) · cites this paper as Ito et al., 2004
In the citing paper
“Inactivation of the p16-Rb pathway restores the reproductive function of ATM−/− HSCs, whereas inhibition of the Arf-p53 pathway has no such effect.20,21”
From Total body irradiation causes long-term mouse BM injury via induction of HSC premature senescence in an Ink4a- and Arf-independent manner (2014) · cites this paper as [20]
In the citing paper
“Furthermore, mutation of the ataxia telangiectasia mutated (ATM) gene also results in upregulation of p16 and Arf in HSCs.”
From Total body irradiation causes long-term mouse BM injury via induction of HSC premature senescence in an Ink4a- and Arf-independent manner (2014) · cites this paper as [20]
In the citing paper
“ROS plays an important role in mediating induction of HSC senescence under various pathological conditions, such as mutation of ATM and various Fanconi anemia genes; deletion of Bmi1, FoxOs, Mdm2, and Tsc1; and aging.15,19,20,35-38”
From Total body irradiation causes long-term mouse BM injury via induction of HSC premature senescence in an Ink4a- and Arf-independent manner (2014) · cites this paper as [20]
In the citing paper
“mice lacking Atm show rapid ageing and depletion of their haematopoietic stem cell compartment 34”
From The common biology of cancer and ageing (2007) · cites this paper as [34]
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“ATM is preferentially expressed in cycling stem cell fractions (Ito et al., 2004), but quiescent stem cells are not detected in ATM-deficient mouse bone marrow cells (Ito et al.”
BackgroundInfluentialAntiaging Mechanism of Natural Compounds: Effects on Autophagy and Oxidative Stress
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ResultInfluentialRNAi screen identifies MAPK14 as a druggable suppressor of human hematopoietic stem cell expansion
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“How TRC8 induces ATM phosphorylation is unknown, but ATM inactivation leads to increased reactive oxygen species (Ito et al., 2004), suggesting a connection to the VHL/HIF system (Kaelin, 2005) and/or to the hypoxic activation of SREBPs (Hughes et al., 2005).”
BackgroundFoxo3a is essential for maintenance of the hematopoietic stem cell pool.
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“It has been shown that neural and hematopoietic stem cells (HSC) contain lower levels of ROS than their more mature progeny and that these differences are essential for maintaining stem cell function [36–42].”
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ResultMa, X., Han, Y., Song, X., Do, T., Yang, Z., Ni, J., & Xie, T. (2016) · Development · doi:10.1242/dev.141069 · Cited by 39
“Interestingly, ATM has been shown to be required for maintaining self-renewal of adult hematopoietic stem cells and germline stem cells in mice in the absence of DNA damage (Ito et al., 2004; Takubo et al., 2008), and ATR has also been shown to be required in multiple tissue stem cells in mice (Ruzankina et al.”
InfluentialImmunometabolic control of hematopoiesis
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“ROS than their mature progeny, and that ROS accumulation triggers intracellular signaling required for differentiation (Ito et al., 2004; Smith et al., 2000; Tsatmali et al., 2005; Yanes et al., 2010).”
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“ATM is especially important for controlling ROS-related DNA damage in HSCs [78], an activity mediated through phosphorylation of the pro-apoptotic protein BID [81].”
BackgroundTo breathe or not to breathe: Understanding how oxygen sensing contributes to age-related phenotypes
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“by oxidative stress and can be prevented by antioxidant treatment (Ito et al., 2004).”
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ATM Regulates Adipocyte Differentiation and Contributes to Glucose Homeostasis
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“ATM-deficient cells accumulate reactive oxygen species (ROS) (Ito et al., 2004), which may interfere with differentiation in vitro.”
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“, 2008b), ATM-CDK-inhibitors p16 and p19 (Ito et al., 2004; 2006), ATM-BID (Maryanovich et al.”
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“…of free oxygen radicals were observed in ATM null haematopoietic stem cell leading to the upregulation of the cyclin-dependent kinase inhibitor (CDKi) p16INK4a and the hypo-phosphorylation of Rb, which limits haematopoietic stem cell proliferation and self renewal capacity (Ito et al., 2004).”
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“ROS associated defects in FoxO and Atm deficient mice (models with increased ROS level in HSC) (Ito et al., 2004; Tothova et al., 2007) can also be rescued by NAC.”
InfluentialChen, F., Su, R., Ni, S., Liu, Y., Huang, J., Li, G., Wang, Q., Zhang, X., & Yang, Y. (2020) · Redox Biology · doi:10.1016/j.redox.2020.101835 · Cited by 38
“As a low intracellular concentration of ROS has been proposed critical for stemness and pluripotency of stem cells [1], we tested whether changes of ROS affected the ISCs homeostasis.”
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Iron Toxicity and Chelation Therapy in Hematopoietic Stem Cell Transplant
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Term vs. preterm cord blood cells for the prevention of preterm brain injury
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“In vitro evidence has shown that stem cells possess antioxidant capacity (23,24), with more immature and younger cells demonstrating a stronger antioxidant ability (25).”
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“Production of ROS is capable to cause oxidative damage to HSPCs (Shao et al., 2013; Wang et al., 2010; Ito et al., 2006; Ito et al., 2004).”
BackgroundAdult Cardiac Stem Cell Aging: A Reversible Stochastic Phenomenon?
Cianflone, E., Torella, M., Chimenti, C., Angelis, A. D., Beltrami, A. P., Urbanek, K., Rota, M., & Torella, D. (2019) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2019/5813147 · Cited by 40
ATM blocks tunicamycin‐induced endoplasmic reticulum stress
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“Although Atm deficiency has been reported to induce ER stress through oxidative stress [18,19], there has been no conclusive evidence that ATM prevents the ER stress.”
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Histone H2AX deficiency causes neurobehavioral deficits and impaired redox homeostasis
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“HIF-1a Important role in proliferation, differentiation, and growth of stem cells (62, 63) Regulation of the genes controlling quiescence of HSCs Maintaining the ability of HSCs to regulate ROS, keep quiescence state, and long-term repopulation potential ATM Reduced level of ROS by up-regulation of G6PD and stimulatio…”
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Rad18 is required for long-term maintenance of spermatogenesis in mouse testes
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Good cells gone bad: the cellular origins of cancer
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Acquisition of G0 state by CD34-positive cord blood cells after bone marrow transplantation
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BackgroundSelf-citationRosu‐Myles, M., Taylor, B. J., & Wolff, L. (2007) · Experimental Hematology · doi:10.1016/j.exphem.2006.11.005 · Cited by 35
The NFKB Inducing Kinase Modulates Hematopoiesis During Stress
González‐Murillo, Á., Fernández, L., Baena, S., Melen, G. J., Sánchez‐Domínguez, R., Sánchez-Valdepeñas, C., Segovia, J. C., Liou, H., Schmid, R. M., Madero, L., et al. (2015) · Stem Cells · doi:10.1002/stem.2066 · Cited by 35
Heritability of resistance to oxidative stress in early life
Kim, S. ‐., Noguera, J. C., Morales, J., & Velando, A. (2010) · Journal of Evolutionary Biology · doi:10.1111/j.1420-9101.2010.01942.x · Cited by 35
Selective Autophagy in Normal and Malignant Hematopoiesis
Koschade, S. E., & Brandts, C. (2019) · Journal of Molecular Biology · doi:10.1016/j.jmb.2019.06.025 · Cited by 37
Germline CHEK2 and ATM Variants in Myeloid and Other Hematopoietic Malignancies
Stubbins, R. J., Korotev, S. C., & Godley, L. A. (2022) · Current Hematologic Malignancy Reports · doi:10.1007/s11899-022-00663-7 · Cited by 40
“However, intact ATM function has been well established as being critical for hematopoietic stem cell function [71], and ATM function and the associated signaling axis have been shown to have shown in vitro to modulate pathogenesis in AML [72–75].”
BackgroundB Cells: From Early Development to Regulating Allergic Diseases
Samitas, K., Lötvall, J., & Bossios, A. (2010) · Archivum Immunologiae et Therapiae Experimentalis · doi:10.1007/s00005-010-0073-2 · Cited by 39
Kim, S., Velando, A., Sorci, G., & Alonso‐Álvarez, C. (2009) · Evolution · doi:10.1111/j.1558-5646.2009.00862.x · Cited by 35
“Similarly, HSC from mice lacking FoxO transcription factors showed high ROS levels (Tothova et al. 2007; see also Warren and Rossi 2009).”
BackgroundAlves, H., Mentink, A., Le, B. Q., van Blitterswijk, C., & de Boer, J. (2012) · Tissue Engineering Part A · doi:10.1089/ten.tea.2011.0700 · Cited by 35
“For instance, in hematopoietic stem cells defective in the cell cycle checkpoint activator ataxia telangiectasia mutated, the selfrenewal capacity can be enhanced through the supplementation of antioxidative substances such as N-acetyl-L-cysteine (NAC) to the culture medium.(26) Recently, it was demonstrated that duri…”
BackgroundAging, metabolism and stem cells: Spotlight on muscle stem cells
García-Prat, L., & Muñoz-Cánoves, P. (2017) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2016.08.021 · Cited by 34
Bae, S., Cho, C., Kim, H., Kim, Y., Kim, H., Hwang, Y., Yoon, J., Kang, J. S., & Lee, W. J. (2013) · Antioxidants and Redox Signaling · doi:10.1089/ars.2012.4756 · Cited by 34
Hematopoietic Stem Cell Function in a Murine Model of Sickle Cell Disease
Javazon, E. H., Radhi, M. A., Gangadharan, B., Perry, J., & Archer, D. R. (2012) · Anemia · doi:10.1155/2012/387385 · Cited by 34
“We found a significant increase in both lipid peroxidation and ROS in sickle-derived KSL cells.”
Ivanović, Z., Duchez, P., Dazey, B., Hermitte, F., Lamrissi‐Garcia, I., Mazurier, F., Praloran, V., Reiffers, J. J., Vezon, G., & Boiron, J.-M. (2005) · Transfusion · doi:10.1111/j.1537-2995.2005.00675.x · Cited by 34
“Indeed, the “management” of oxidative stress within stem cells allows them to maintain their self-renewal capacity.(13) The addition of antioxidants could help the maintenance Fig.”
BackgroundCarroll, D. W., Howard, D., Zhu, H., Paumi, C. M., Vore, M. E., Bondada, S., Liang, Y., Wang, C., & Clair, D. K. S. (2016) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2016.05.005 · Cited by 34
Gene therapy and gene editing strategies for hemoglobinopathies
Lidonnici, M. R., & Ferrari, G. (2018) · Blood Cells Molecules and Diseases · doi:10.1016/j.bcmd.2017.12.001 · Cited by 34
Li, X., Gao, J., Yu, Z., Jiang, W., Sun, W., Yu, C., Sun, J., Wang, C., Chen, J., Jing, S., et al. (2020) · Clinical Interventions in Aging · doi:10.2147/cia.s237601 · Cited by 36
Immuno-Modulation of Hematopoietic Stem and Progenitor Cells in Inflammation
Sezaki, M., Hayashi, Y., Wang, Y., Johansson, A., Umemoto, T., & Takizawa, H. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.585367 · Cited by 38
“This is essential for initiating HSC cellular division and hematopoietic repopulation (95), but contradicts with a previous study claiming the negative regulation of ROS on HSC maintenance (96), and high mitochondrial membrane potential with reduced hematopoietic repopulating ability in steady-state and IFN-a-stimulat…”
BackgroundHow does suppression of IGF-1 signaling by DNA damage affect aging and longevity?
Hinkal, G. W., & Donehower, L. A. (2008) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2008.02.005 · Cited by 33
“It has been demonstrated that in Atm-deficient mouse HSCs, increased reactive oxygen species (ROS) levels compromise HSC function, in part through activation of p16 INK4a and ARF, tumor suppressors implicated in induction of senescence (Ito et al., 2004).”
Zhu, H., Kwak, H. J., Liu, P., Bajrami, B., Xu, Y., Park, S., Nombela‐Arrieta, C., Mondal, S., Kambara, H., Yu, H., et al. (2017) · The Journal of Immunology · doi:10.4049/jimmunol.1602006 · Cited by 34
Susceptibility of acute myeloid leukemia cells to ferroptosis and evasion strategies
Zhang, H., Sun, C., Sun, Q., Ye, L., Zhou, C., & Sun, C. (2023) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2023.1275774 · Cited by 35
Yamaguchi, M., & Kashiwakura, I. (2013) · PLoS ONE · doi:10.1371/journal.pone.0070503 · Cited by 38
Distinct Brca1 Mutations Differentially Reduce Hematopoietic Stem Cell Function
Mgbemena, V. E., Signer, R. A. J., Wijayatunge, R., Laxson, T., Morrison, S. J., & Ross, T. S. (2017) · Cell Reports · doi:10.1016/j.celrep.2016.12.075 · Cited by 36
“Deficiency for homologous recombination-mediated double-strand-break repair proteins, however, can lead to hematopoietic failure in patients (Kottemann and Smogorzewska, 2013), and it can impair hematopoiesis in mice as well as HSC function upon transplantation into irradiated mice (Bender et al., 2002; Carreau et al.…”
BackgroundMitochondrial ROS direct the differentiation of murine pluripotent P19 cells
Pashkovskaia, N., Gey, U., & Rödel, G. (2018) · Stem Cell Research · doi:10.1016/j.scr.2018.06.007 · Cited by 33
Kaneko, Y., Tanigawa, N., Sato, Y., Kobayashi, T., Nakamura, S., Ito, E., Soma, T., Miyamoto, K., Kobayashi, S., Harato, K., et al. (2019) · Scientific Reports · doi:10.1038/s41598-019-55297-2 · Cited by 33
Stem cell fate determination through protein O-GlcNAcylation
Sheikh, M. A., Emerald, B. S., & Ansari, S. A. (2020) · Journal of Biological Chemistry · doi:10.1074/jbc.rev120.014915 · Cited by 34
“FOXOs help in the maintenance of genomic and protein integrity by preventing accumulation of ROS in stem cells by inducing the transcription of ROS scavenger genes, superoxide dismutase (SOD), catalase, and others (156).”
BackgroundPeeling Back the Layers of Lymph Gland Structure and Regulation
Kharrat, B., Csordás, G., & Honti, V. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23147767 · Cited by 35
ATM and KAT5 safeguard replicating chromatin against formaldehyde damage
Ortega-Atienza, S., Wong, V. C., DeLoughery, Z. J., Łuczak, M. W., & Zhitkovich, A. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv957 · Cited by 33
“Administration of a commonly used antioxidant N-acetylcysteine to Atm-/mice inhibited bone marrow degeneration and the development of leukemia (54,55), which is viewed as evidence for the importance of ATM in protection of bone marrow stem cells against oxidative stress.”
BackgroundApoptosis-Inducing Factor Regulates Skeletal Muscle Progenitor Cell Number and Muscle Phenotype
Armand, A., Laziz, I., Djeghloul, D., Lécolle, S., Bertrand, A., Biondi, O., Windt, L. J. D., & Chanoine, C. (2011) · PLoS ONE · doi:10.1371/journal.pone.0027283 · Cited by 35
“Several syndromes like Ataxia telangiectasia mutated (ATM) are characterized by increased oxidative stress [14], and interestingly, the self-renewal of haematopoietic stem cells derived from ATM-deficient mice was impaired, ROS levels were increased in ATM-deficient haematopoietic cells, and bone-marrow failure was re…”
BackgroundAyrault, O., Godeny, M. D., Dillon, C. P., Zindy, F., Fitzgerald, P., Roussel, M. F., & Beere, H. M. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0902880106 · Cited by 32
“In addition, Atm deficiency is associated with elevated levels of ROS (31) that may render cells more sensitive to any added imposed stress including (but not necessarily restricted to) 17-DMAG treatment.”
BackgroundDuong, H., Hong, Y. B., Kim, J. S., Lee, H., Yi, Y. W., Kim, Y. J., Wang, A., Zhao, W., Cho, C., Seong, Y., et al. (2013) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.12101 · Cited by 35
“ATM knockout mice study suggests that checkpoint components can have some function to detoxify ROS induced by DNA damage [44].”
BackgroundMorita, A., Tanimoto, K., Murakami, T., Morinaga, T., & Hosoi, Y. (2014) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2013.12.139 · Cited by 32
Cell intrinsic and extrinsic mechanisms of stem cell aging depend on telomere status
Song, Z., Ju, Z., & Rudolph, K. L. (2008) · Experimental Gerontology · doi:10.1016/j.exger.2008.06.009 · Cited by 34
“Indeed, ATM deficiency affected the function of HSCs in wild type mice with long telomeres (Ito et al., 2004).”
BackgroundRole of reactive oxygen species in myelodysplastic syndromes
Jing, Q., Zhou, C., Zhang, J., Zhang, P., Wu, Y., Zhou, J., Tong, X., Li, Y., Du, J., & Wang, Y. (2024) · Cellular & Molecular Biology Letters · doi:10.1186/s11658-024-00570-0 · Cited by 33
“Previous studies have reported the critical role of mitochondria and ROS in self-renewal [70, 71], differentiation [72], fate [73], and function [74].”
BackgroundGadd45a regulates hematopoietic stem cell stress responses in mice
Chen, Y., Ma, X., Zhang, M., Wang, X., Wang, C.-X., Wang, H., Guo, P., Yuan, W., Rudolph, K. L., Zhan, Q., et al. (2013) · Blood · doi:10.1182/blood-2013-05-504084 · Cited by 34
FANCL ubiquitinates β-catenin and enhances its nuclear function
Dao, K.-H. T., Rotelli, M. D., Petersen, C. L., Kaech, S., Nelson, W. D., Yates, J. E., Newell, A. E. H., Olson, S. B., Druker, B. J., & Bagby, G. C. (2012) · Blood · doi:10.1182/blood-2011-11-388355 · Cited by 32
ATM protects against oxidative stress induced by oxidized low-density lipoprotein
Semlitsch, M., Shackelford, R. E., Zirkl, S., Sattler, W., & Malle, E. (2011) · DNA repair · doi:10.1016/j.dnarep.2011.05.004 · Cited by 33
The Emerging Role of Estrogens in Thyroid Redox Homeostasis and Carcinogenesis
de Faria, C. C., Peixoto, M. S., de Carvalho, D. P., & Fortunato, R. S. (2019) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2019/2514312 · Cited by 36
“In fact, the antioxidant N-acetylcysteine (NAC) rescues some of the defects that result from the loss of ATM, suggesting that the normal function of ATM might be to control ROS levels [44, 45].”
BackgroundMaciejczyk, M., Heropolitańska–Pliszka, E., Pietrucha, B. M., Sawicka-Powierza, J., Bernatowska, E. A., Wolska‐Kuśnierz, B., Pac, M., Car, H., Zalewska, A., & Mikołuć, B. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.02322 · Cited by 32
“The central function in the pathway is played by ATM and ATR (Ataxia telangiectasia Rad 3-related) kinases belonging to the PIKK (phosphatidylinositol 3-kinase-related kinase) family (42, 46).”
Background
Metadata
- Authors
- Ito, K., Hirao, A., Arai, F., Matsuoka, S., Takubo, K., Hamaguchi, I., Nomiyama, K., Hosokawa, K., Sakurada, K., Nakagata, N., Ikeda, Y., Mak, T. W., & Suda, T.
- Affiliations
- Keio University (JP)
- Kumamoto University (JP)
- University of Toronto (CA)
- Corresponding author
- Hirao, Atsushi
- Suda, Toshio
- ORCID
- Venue
- Nature
- Published
- 2004-10
- Volume
- 431
- Issue
- 7011
- Pages
- 997-1002
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2041897873
- Cited by
- 1,175
- References
- 30
- Citations by year
- 2026: 15 · 2025: 29 · 2024: 38 · 2023: 31 · 2022: 37 · 2021: 51 · 2020: 44 · 2019: 58 · 2018: 47 · 2017: 59 · 2016: 73 · 2015: 71 · 2014: 75 · 2013: 88 · 2012: 77
- FWCI
- 25.91
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Topics
- Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
- Keywords
- ATM, oxidative stress, hematopoietic stem cells, self-renewal, reactive oxygen species, ataxia telangiectasia, bone marrow failure, p16INK4a, retinoblastoma protein, DNA damage response, antioxidant therapy
- MeSH terms
- Acetylcysteine, Animals, Antioxidants, Cell Division, DNA-Binding Proteins, Hematopoiesis, Hematopoietic Stem Cells, Mice, Inbred C57BL, RNA, Messenger, Signal Transduction, Retinoblastoma Protein, Protein Serine-Threonine Kinases, Gene Deletion, Reactive Oxygen Species, Mice, Knockout, Oxidative Stress, Cell Cycle Proteins, Cell Lineage, Cyclin-Dependent Kinase Inhibitor p16, Tumor Suppressor Proteins, Mice, Ataxia Telangiectasia Mutated Proteins
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