Proteomics reveals dynamic metabolic changes in human hematopoietic stem progenitor cells from fetal to adulthood.

Humans Hematopoietic Stem Cells / metabolism Proteomics / methods Reactive Oxygen Species / metabolism Fetus / metabolism Adult Fetal Blood / cytology Buthionine Sulfoximine / pharmacology Glutathione / metabolism
Adult bone marrow (aBM) Fetal liver (FL) Glutathione (GSH) Hematopoietic stem progenitor cells (HSPCs) Metabolic remodelling Proteomics Umbilical cord blood (UCB)

Journal

Stem cell research & therapy
ISSN: 1757-6512
Titre abrégé: Stem Cell Res Ther
Pays: England
ID NLM: 101527581

Informations de publication

Date de publication:
15 Sep 2024
Historique:
received: 23 07 2024
accepted: 06 09 2024
medline: 16 9 2024
pubmed: 16 9 2024
entrez: 15 9 2024
Statut: epublish

Résumé

Hematopoietic stem progenitor cells (HSPCs) undergo phenotypical and functional changes during their emergence and development. Although the molecular programs governing the development of human hematopoietic stem cells (HSCs) have been investigated broadly, the relationships between dynamic metabolic alterations and their functions remain poorly characterized. In this study, we comprehensively described the proteomics of HSPCs in the human fetal liver (FL), umbilical cord blood (UCB), and adult bone marrow (aBM). The metabolic state of human HSPCs was assessed via a Seahorse assay, RT‒PCR, and flow cytometry-based metabolic-related analysis. To investigate whether perturbing glutathione metabolism affects reactive oxygen species (ROS) production, the metabolic state, and the expansion of human HSPCs, HSPCs were treated with buthionine sulfoximine (BSO), an inhibitor of glutathione synthetase, and N-acetyl-L-cysteine (NAC). We investigated the metabolomic landscape of human HSPCs from the fetal, perinatal, and adult developmental stages by in-depth quantitative proteomics and predicted a metabolic switch from the oxidative state to the glycolytic state during human HSPC development. Seahorse assays, mitochondrial activity, ROS level, glucose uptake, and protein synthesis rate analysis supported our findings. In addition, immune-related pathways and antigen presentation were upregulated in UCB or aBM HSPCs, indicating their functional maturation upon development. Glutathione-related metabolic perturbations resulted in distinct responses in human HSPCs and progenitors. Furthermore, the molecular and immunophenotypic differences between human HSPCs at different developmental stages were revealed at the protein level for the first time. The metabolic landscape of human HSPCs at three developmental stages (FL, UCB, and aBM), combined with proteomics and functional validations, substantially extends our understanding of HSC metabolic regulation. These findings provide valuable resources for understanding human HSC function and development during fetal and adult life.

Sections du résumé

BACKGROUND BACKGROUND
Hematopoietic stem progenitor cells (HSPCs) undergo phenotypical and functional changes during their emergence and development. Although the molecular programs governing the development of human hematopoietic stem cells (HSCs) have been investigated broadly, the relationships between dynamic metabolic alterations and their functions remain poorly characterized.
METHODS METHODS
In this study, we comprehensively described the proteomics of HSPCs in the human fetal liver (FL), umbilical cord blood (UCB), and adult bone marrow (aBM). The metabolic state of human HSPCs was assessed via a Seahorse assay, RT‒PCR, and flow cytometry-based metabolic-related analysis. To investigate whether perturbing glutathione metabolism affects reactive oxygen species (ROS) production, the metabolic state, and the expansion of human HSPCs, HSPCs were treated with buthionine sulfoximine (BSO), an inhibitor of glutathione synthetase, and N-acetyl-L-cysteine (NAC).
RESULTS RESULTS
We investigated the metabolomic landscape of human HSPCs from the fetal, perinatal, and adult developmental stages by in-depth quantitative proteomics and predicted a metabolic switch from the oxidative state to the glycolytic state during human HSPC development. Seahorse assays, mitochondrial activity, ROS level, glucose uptake, and protein synthesis rate analysis supported our findings. In addition, immune-related pathways and antigen presentation were upregulated in UCB or aBM HSPCs, indicating their functional maturation upon development. Glutathione-related metabolic perturbations resulted in distinct responses in human HSPCs and progenitors. Furthermore, the molecular and immunophenotypic differences between human HSPCs at different developmental stages were revealed at the protein level for the first time.
CONCLUSION CONCLUSIONS
The metabolic landscape of human HSPCs at three developmental stages (FL, UCB, and aBM), combined with proteomics and functional validations, substantially extends our understanding of HSC metabolic regulation. These findings provide valuable resources for understanding human HSC function and development during fetal and adult life.

Identifiants

DOI: 10.1186/s13287-024-03930-x PMID: 39278906
pubmed: 39278906
doi: 10.1186/s13287-024-03930-x
pii: 10.1186/s13287-024-03930-x
doi:

Substances chimiques

Reactive Oxygen Species 0
Buthionine Sulfoximine 5072-26-4
Glutathione GAN16C9B8O

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

303

Subventions

Organisme : the National Key R&D Program of China
ID : 2022YFA1106300
Organisme : the National Key R&D Program of China
ID : 2021YFA1102400
Organisme : the National Natural Science Foundation of China
ID : 82370108
Organisme : the National Natural Science Foundation of China
ID : 81800102
Organisme : Beijing Nova Program
ID : Z201100006820057
Organisme : Beijing Nova Program
ID : 20230484404
Organisme : Young Elite Scientists Sponsorship Program by CAST
ID : 2022QNRC001
Organisme : the Young Talent Foundation of PLA General Hospital
ID : 2019-YQPY-002

Informations de copyright

© 2024. The Author(s).

Références

Ivanovs A, Rybtsov S, Ng ES, Stanley EG, Elefanty AG, Medvinsky A. Human haematopoietic stem cell development: from the embryo to the dish. Development (Cambridge, England). 2017;144(13):2323–37.
pubmed: 28676567 doi: 10.1242/dev.134866
Zheng Z, He H, Tang XT, Zhang H, Gou F, Yang H, et al. Uncovering the emergence of HSCs in the human fetal bone marrow by single-cell RNA-seq analysis. Cell Stem Cell. 2022;29(11):1562-79.e7.
pubmed: 36332570 doi: 10.1016/j.stem.2022.10.005
Zhou F, Li X, Wang W, Zhu P, Zhou J, He W, et al. Tracing haematopoietic stem cell formation at single-cell resolution. Nature. 2016;533(7604):487–92.
pubmed: 27225119 doi: 10.1038/nature17997
Ranzoni AM, Tangherloni A, Berest I, Riva SG, Myers B, Strzelecka PM, et al. Integrative single-cell RNA-Seq and ATAC-Seq analysis of human developmental hematopoiesis. Cell Stem Cell. 2021;28(3):472-87.e7.
pubmed: 33352111 pmcid: 7939551 doi: 10.1016/j.stem.2020.11.015
Suda T, Takubo K, Semenza GL. Metabolic regulation of hematopoietic stem cells in the hypoxic niche. Cell Stem Cell. 2011;9(4):298–310.
pubmed: 21982230 doi: 10.1016/j.stem.2011.09.010
Wahlster L, Daley GQ. Progress towards generation of human haematopoietic stem cells. Nat Cell Biol. 2016;18(11):1111–7.
pubmed: 27723718 doi: 10.1038/ncb3419
Qiu J, Gjini J, Arif T, Moore K, Lin M, Ghaffari S. Using mitochondrial activity to select for potent human hematopoietic stem cells. Blood Adv. 2021;5(6):1605–16.
pubmed: 33710339 pmcid: 7993096 doi: 10.1182/bloodadvances.2020003658
Chandel NS, Jasper H, Ho TT, Passegué E. Metabolic regulation of stem cell function in tissue homeostasis and organismal ageing. Nat Cell Biol. 2016;18(8):823–32.
pubmed: 27428307 doi: 10.1038/ncb3385
Bowie MB, Kent DG, Dykstra B, McKnight KD, McCaffrey L, Hoodless PA, et al. Identification of a new intrinsically timed developmental checkpoint that reprograms key hematopoietic stem cell properties. Proc Natl Acad Sci USA. 2007;104(14):5878–82.
pubmed: 17379664 pmcid: 1829493 doi: 10.1073/pnas.0700460104
Manesia JK, Franch M, Tabas-Madrid D, Nogales-Cadenas R, Vanwelden T, Van Den Bosch E, et al. Distinct molecular signature of murine fetal liver and adult hematopoietic stem cells identify novel regulators of hematopoietic stem cell function. Stem Cells Dev. 2017;26(8):573–84.
pubmed: 27958775 doi: 10.1089/scd.2016.0294
Manesia JK, Xu Z, Broekaert D, Boon R, van Vliet A, Eelen G, et al. Highly proliferative primitive fetal liver hematopoietic stem cells are fueled by oxidative metabolic pathways. Stem Cell Res. 2015;15(3):715–21.
pubmed: 26599326 doi: 10.1016/j.scr.2015.11.001
Jang YY, Sharkis SJ. A low level of reactive oxygen species selects for primitive hematopoietic stem cells that may reside in the low-oxygenic niche. Blood. 2007;110(8):3056–63.
pubmed: 17595331 pmcid: 2018677 doi: 10.1182/blood-2007-05-087759
Kocabas F, Zheng J, Thet S, Copeland NG, Jenkins NA, DeBerardinis RJ, et al. Meis1 regulates the metabolic phenotype and oxidant defense of hematopoietic stem cells. Blood. 2012;120(25):4963–72.
pubmed: 22995899 pmcid: 3525021 doi: 10.1182/blood-2012-05-432260
Zhou C, Kuang M, Tao Y, Wang J, Luo Y, Fu Y, et al. Nynrin preserves hematopoietic stem cell function by inhibiting the mitochondrial permeability transition pore opening. Cell Stem Cell. 2024;31(9):1359–1375.e8.
Zhang Y, Xie X, Huang Y, Liu M, Li Q, Luo J, et al. Temporal molecular program of human hematopoietic stem and progenitor cells after birth. Dev Cell. 2022;57(24):2745-60.e6.
pubmed: 36493772 doi: 10.1016/j.devcel.2022.11.013
Yokomizo T, Ideue T, Morino-Koga S, Tham CY, Sato T, Takeda N, et al. Independent origins of fetal liver haematopoietic stem and progenitor cells. Nature. 2022;609(7928):779–84.
pubmed: 36104564 doi: 10.1038/s41586-022-05203-0
Ganuza M, Hall T, Myers J, Nevitt C, Sánchez-Lanzas R, Chabot A, et al. Murine foetal liver supports limited detectable expansion of life-long haematopoietic progenitors. Nat Cell Biol. 2022;24(10):1475–86.
pubmed: 36202972 pmcid: 10026622 doi: 10.1038/s41556-022-00999-5
Amon S, Meier-Abt F, Gillet LC, Dimitrieva S, Theocharides APA, Manz MG, et al. Sensitive quantitative proteomics of human hematopoietic stem and progenitor cells by data-independent acquisition mass spectrometry. Molecul cell Proteomics MCP. 2019;18(7):1454–67.
doi: 10.1074/mcp.TIR119.001431
Kocabas F, Xie L, Xie J, Yu Z, DeBerardinis RJ, Kimura W, et al. Hypoxic metabolism in human hematopoietic stem cells. Cell Biosci. 2015;5:39.
pubmed: 26221532 pmcid: 4517642 doi: 10.1186/s13578-015-0020-3
Hennrich ML, Romanov N, Horn P, Jaeger S, Eckstein V, Steeples V, et al. Cell-specific proteome analyses of human bone marrow reveal molecular features of age-dependent functional decline. Nat Commun. 2018;9(1):4004.
pubmed: 30275468 pmcid: 6167374 doi: 10.1038/s41467-018-06353-4
Raffel S, Klimmeck D, Falcone M, Demir A, Pouya A, Zeisberger P, et al. Quantitative proteomics reveals specific metabolic features of acute myeloid leukemia stem cells. Blood. 2020;136(13):1507–19.
pubmed: 32556243 doi: 10.1182/blood.2019003654
Yan JS, Yang MY, Zhang XH, Luo CH, Du CK, Jiang Y, et al. Mitochondrial oxidative phosphorylation is dispensable for survival of CD34(+) chronic myeloid leukemia stem and progenitor cells. Cell Death Dis. 2022;13(4):384.
pubmed: 35444236 pmcid: 9021200 doi: 10.1038/s41419-022-04842-5
Zeng Y, He J, Bai Z, Li Z, Gong Y, Liu C, et al. Tracing the first hematopoietic stem cell generation in human embryo by single-cell RNA sequencing. Cell Res. 2019;29(11):881–94.
pubmed: 31501518 pmcid: 6888893 doi: 10.1038/s41422-019-0228-6
Calvanese V, Capellera-Garcia S, Ma F, Fares I, Liebscher S, Ng ES, et al. Mapping human haematopoietic stem cells from haemogenic endothelium to birth. Nature. 2022;604(7906):534–40.
pubmed: 35418685 pmcid: 9645817 doi: 10.1038/s41586-022-04571-x
Qian P, De Kumar B, He XC, Nolte C, Gogol M, Ahn Y, et al. Retinoid-sensitive epigenetic regulation of the hoxb cluster maintains normal hematopoiesis and inhibits leukemogenesis. Cell Stem Cell. 2018;22(5):740-54.e7.
pubmed: 29727682 doi: 10.1016/j.stem.2018.04.012
Signer RA, Magee JA, Salic A, Morrison SJ. Haematopoietic stem cells require a highly regulated protein synthesis rate. Nature. 2014;509(7498):49–54.
pubmed: 24670665 pmcid: 4015626 doi: 10.1038/nature13035
Notta F, Doulatov S, Laurenti E, Poeppl A, Jurisica I, Dick JE. Isolation of single human hematopoietic stem cells capable of long-term multilineage engraftment. Science (New York, NY). 2011;333(6039):218–21.
doi: 10.1126/science.1201219
Doulatov S, Notta F, Laurenti E, Dick JE. Hematopoiesis: a human perspective. Cell Stem Cell. 2012;10(2):120–36.
pubmed: 22305562 doi: 10.1016/j.stem.2012.01.006
Calvanese V, Nguyen AT, Bolan TJ, Vavilina A, Su T, Lee LK, et al. MLLT3 governs human haematopoietic stem-cell self-renewal and engraftment. Nature. 2019;576(7786):281–6.
pubmed: 31776511 pmcid: 7278275 doi: 10.1038/s41586-019-1790-2
Hammond CA, Wu SW, Wang F, MacAldaz ME, Eaves CJ. Aging alters the cell cycle control and mitogenic signaling responses of human hematopoietic stem cells. Blood. 2023;141(16):1990–2002.
pubmed: 36652668 doi: 10.1182/blood.2022017174
Celhar T, Li X, Zhao Y, Tay HC, Lee A, Liew HH, et al. Fetal liver CD34(+) contain human immune and endothelial progenitors and mediate solid tumor rejection in NOG mice. Stem Cell Res Ther. 2024;15(1):164.
pubmed: 38853275 pmcid: 11163708 doi: 10.1186/s13287-024-03756-7
Popescu DM, Botting RA, Stephenson E, Green K, Webb S, Jardine L, et al. Decoding human fetal liver haematopoiesis. Nature. 2019;574(7778):365–71.
pubmed: 31597962 pmcid: 6861135 doi: 10.1038/s41586-019-1652-y
Futschik ME, Carlisle B. Noise-robust soft clustering of gene expression time-course data. J Bioinform Comput Biol. 2005;3(4):965–88.
pubmed: 16078370 doi: 10.1142/S0219720005001375
Tothova Z, Kollipara R, Huntly BJ, Lee BH, Castrillon DH, Cullen DE, et al. FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell. 2007;128(2):325–39.
pubmed: 17254970 doi: 10.1016/j.cell.2007.01.003
Lv K, Gong C, Antony C, Han X, Ren JG, Donaghy R, et al. HectD1 controls hematopoietic stem cell regeneration by coordinating ribosome assembly and protein synthesis. Cell Stem Cell. 2021;28(7):1275-90.e9.
pubmed: 33711283 pmcid: 8254759 doi: 10.1016/j.stem.2021.02.008
Signer RA, Qi L, Zhao Z, Thompson D, Sigova AA, Fan ZP, et al. The rate of protein synthesis in hematopoietic stem cells is limited partly by 4E-BPs. Genes Dev. 2016;30(15):1698–703.
pubmed: 27492367 pmcid: 5002975 doi: 10.1101/gad.282756.116
Unwin RD, Smith DL, Blinco D, Wilson CL, Miller CJ, Evans CA, et al. Quantitative proteomics reveals posttranslational control as a regulatory factor in primary hematopoietic stem cells. Blood. 2006;107(12):4687–94.
pubmed: 16507774 doi: 10.1182/blood-2005-12-4995
Eliasson P, Jönsson JI. The hematopoietic stem cell niche: low in oxygen but a nice place to be. J Cell Physiol. 2010;222(1):17–22.
pubmed: 19725055 doi: 10.1002/jcp.21908
Simsek T, Kocabas F, Zheng J, Deberardinis RJ, Mahmoud AI, Olson EN, et al. The distinct metabolic profile of hematopoietic stem cells reflects their location in a hypoxic niche. Cell Stem Cell. 2010;7(3):380–90.
pubmed: 20804973 pmcid: 4159713 doi: 10.1016/j.stem.2010.07.011
Takubo K, Nagamatsu G, Kobayashi CI, Nakamura-Ishizu A, Kobayashi H, Ikeda E, et al. Regulation of glycolysis by Pdk functions as a metabolic checkpoint for cell cycle quiescence in hematopoietic stem cells. Cell Stem Cell. 2013;12(1):49–61.
pubmed: 23290136 pmcid: 6592822 doi: 10.1016/j.stem.2012.10.011
Guitart AV, Panagopoulou TI, Villacreces A, Vukovic M, Sepulveda C, Allen L, et al. Fumarate hydratase is a critical metabolic regulator of hematopoietic stem cell functions. J Exp Med. 2017;214(3):719–35.
pubmed: 28202494 pmcid: 5339674 doi: 10.1084/jem.20161087
Griffith OW. Mechanism of action, metabolism, and toxicity of buthionine sulfoximine and its higher homologs, potent inhibitors of glutathione synthesis. J Biol Chem. 1982;257(22):13704–12.
pubmed: 6128339 doi: 10.1016/S0021-9258(18)33504-X
Oberlin E, Fleury M, Clay D, Petit-Cocault L, Candelier JJ, Mennesson B, et al. VE-cadherin expression allows identification of a new class of hematopoietic stem cells within human embryonic liver. Blood. 2010;116(22):4444–55.
pubmed: 20693433 doi: 10.1182/blood-2010-03-272625
Sudo T, Yokota T, Oritani K, Satoh Y, Sugiyama T, Ishida T, et al. The endothelial antigen ESAM monitors hematopoietic stem cell status between quiescence and self-renewal. J immunol. 2012;189(1):200–10.
pubmed: 22649198 doi: 10.4049/jimmunol.1200056
Yokota T, Oritani K, Butz S, Kokame K, Kincade PW, Miyata T, et al. The endothelial antigen ESAM marks primitive hematopoietic progenitors throughout life in mice. Blood. 2009;113(13):2914–23.
pubmed: 19096010 pmcid: 2974489 doi: 10.1182/blood-2008-07-167106
Ishibashi T, Yokota T, Tanaka H, Ichii M, Sudo T, Satoh Y, et al. ESAM is a novel human hematopoietic stem cell marker associated with a subset of human leukemias. Exp Hematol. 2016;44(4):269-81.e1.
pubmed: 26774386 doi: 10.1016/j.exphem.2015.12.010
Chen CZ, Li M, de Graaf D, Monti S, Göttgens B, Sanchez MJ, et al. Identification of endoglin as a functional marker that defines long-term repopulating hematopoietic stem cells. Proc Natl Acad Sci USA. 2002;99(24):15468–73.
pubmed: 12438646 pmcid: 137740 doi: 10.1073/pnas.202614899
Ivanovs A, Rybtsov S, Anderson RA, Turner ML, Medvinsky A. Identification of the niche and phenotype of the first human hematopoietic stem cells. Stem Cell Rep. 2014;2(4):449–56.
doi: 10.1016/j.stemcr.2014.02.004
Vanuytsel K, Villacorta-Martin C, Lindstrom-Vautrin J, Wang Z, Garcia-Beltran WF, Vrbanac V, et al. Multi-modal profiling of human fetal liver hematopoietic stem cells reveals the molecular signature of engraftment. Nat Commun. 2022;13(1):1103.
pubmed: 35232959 pmcid: 8888592 doi: 10.1038/s41467-022-28616-x
Zhao K, Zheng WW, Dong XM, Yin RH, Gao R, Li X, et al. EDAG promotes the expansion and survival of human CD34+ cells. PLoS ONE. 2018;13(1): e0190794.
pubmed: 29324880 pmcid: 5764277 doi: 10.1371/journal.pone.0190794
Machherndl-Spandl S, Suessner S, Danzer M, Proell J, Gabriel C, Lauf J, et al. Molecular pathways of early CD105-positive erythroid cells as compared with CD34-positive common precursor cells by flow cytometric cell-sorting and gene expression profiling. Blood Cancer J. 2013;3(1): e100.
pubmed: 23310930 pmcid: 3556575 doi: 10.1038/bcj.2012.45
Mori Y, Chen JY, Pluvinage JV, Seita J, Weissman IL. Prospective isolation of human erythroid lineage-committed progenitors. Proc Natl Acad Sci USA. 2015;112(31):9638–43.
pubmed: 26195758 pmcid: 4534255 doi: 10.1073/pnas.1512076112
Bowie MB, Kent DG, Copley MR, Eaves CJ. Steel factor responsiveness regulates the high self-renewal phenotype of fetal hematopoietic stem cells. Blood. 2007;109(11):5043–8.
pubmed: 17327414 doi: 10.1182/blood-2006-08-037770
Holyoake TL, Nicolini FE, Eaves CJ. Functional differences between transplantable human hematopoietic stem cells from fetal liver, cord blood, and adult marrow. Exp Hematol. 1999;27(9):1418–27.
pubmed: 10480433 doi: 10.1016/S0301-472X(99)00078-8
Hernández-Malmierca P, Vonficht D, Schnell A, Uckelmann HJ, Bollhagen A, Mahmoud MAA, et al. Antigen presentation safeguards the integrity of the hematopoietic stem cell pool. Cell Stem Cell. 2022;29(5):760-75.e10.
pubmed: 35523139 pmcid: 9202612 doi: 10.1016/j.stem.2022.04.007
Hasty P, Vijg J. Accelerating aging by mouse reverse genetics: a rational approach to understanding longevity. Aging Cell. 2004;3(2):55–65.
pubmed: 15038819 doi: 10.1111/j.1474-9728.2004.00082.x
Mohrin M, Bourke E, Alexander D, Warr MR, Barry-Holson K, Le Beau MM, et al. Hematopoietic stem cell quiescence promotes error-prone DNA repair and mutagenesis. Cell Stem Cell. 2010;7(2):174–85.
pubmed: 20619762 pmcid: 2924905 doi: 10.1016/j.stem.2010.06.014
Chua BA, Lennan CJ, Sunshine MJ, Dreifke D, Chawla A, Bennett EJ, et al. Hematopoietic stem cells preferentially traffic misfolded proteins to aggresomes and depend on aggrephagy to maintain protein homeostasis. Cell Stem Cell. 2023;30(4):460-72.e6.
pubmed: 36948186 pmcid: 10164413 doi: 10.1016/j.stem.2023.02.010
Chua BA, Van Der Werf I, Jamieson C, Signer RAJ. Post-transcriptional regulation of homeostatic, stressed, and malignant stem cells. Cell Stem Cell. 2020;26(2):138–59.
pubmed: 32032524 pmcid: 7158223 doi: 10.1016/j.stem.2020.01.005
da Silva CL, Gonçalves R, Porada CD, Ascensão JL, Zanjani ED, Cabral JM, et al. Differences amid bone marrow and cord blood hematopoietic stem/progenitor cell division kinetics. J Cell Physiol. 2009;220(1):102–11.
pubmed: 19277981 doi: 10.1002/jcp.21736
Traycoff CM, Abboud MR, Laver J, Clapp DW, Srour EF. Rapid exit from G0/G1 phases of cell cycle in response to stem cell factor confers on umbilical cord blood CD34+ cells an enhanced ex vivo expansion potential. Exp Hematol. 1994;22(13):1264–72.
pubmed: 7525328
Lansdorp PM. Telomere length and proliferation potential of hematopoietic stem cells. J Cell Sci. 1995;108(Pt 1):1–6.
pubmed: 7738087 doi: 10.1242/jcs.108.1.1
Yahata T, Muguruma Y, Yumino S, Sheng Y, Uno T, Matsuzawa H, et al. Quiescent human hematopoietic stem cells in the bone marrow niches organize the hierarchical structure of hematopoiesis. Stem Cells. 2008;26(12):3228–36.
pubmed: 18787204 doi: 10.1634/stemcells.2008-0552
Jassinskaja M, Johansson E, Kristiansen TA, Åkerstrand H, Sjöholm K, Hauri S, et al. Comprehensive proteomic characterization of ontogenic changes in hematopoietic stem and progenitor cells. Cell Rep. 2017;21(11):3285–97.
pubmed: 29241553 doi: 10.1016/j.celrep.2017.11.070
Hu L, Cheng H, Gao Y, Shi M, Liu Y, Hu Z, et al. Antioxidant N-acetyl-L-cysteine increases engraftment of human hematopoietic stem cells in immune-deficient mice. Blood. 2014;124(20):e45–8.
pubmed: 25287706 pmcid: 4231425 doi: 10.1182/blood-2014-03-559369
Cao J, Yao QJ, Wu J, Chen X, Huang L, Liu W, et al. Deciphering the metabolic heterogeneity of hematopoietic stem cells with single-cell resolution. Cell Metab. 2024;36(1):209-21.e6.
pubmed: 38171334 doi: 10.1016/j.cmet.2023.12.005

Auteurs

Mingfang Xiong (M)

Senior Department of Hematology, the Fifth Medical Center of Chinese PLA General Hospital, Beijing, 100071, China.
Medical School of the Chinese PLA General Hospital, Beijing, 100039, China.

Yanyu Xiu (Y)

Senior Department of Hematology, the Fifth Medical Center of Chinese PLA General Hospital, Beijing, 100071, China.
College of Veterinary Medicine, Shanxi Agricultural University, Taigu, 030801, Shanxi, China.

Juan Long (J)

Senior Department of Hematology, the Fifth Medical Center of Chinese PLA General Hospital, Beijing, 100071, China.

Xiao Zhao (X)

Senior Department of Hematology, the Fifth Medical Center of Chinese PLA General Hospital, Beijing, 100071, China.

Qianqian Wang (Q)

School of Basic Medical Sciences and Forensic Medicine, Hangzhou Medical College, Hangzhou, 311399, China.

Haoyu Yang (H)

College of Veterinary Medicine, Shanxi Agricultural University, Taigu, 030801, Shanxi, China.

Hang Yu (H)

Senior Department of Hematology, the Fifth Medical Center of Chinese PLA General Hospital, Beijing, 100071, China.
Medical School of the Chinese PLA General Hospital, Beijing, 100039, China.

Lihong Bian (L)

Department of Gynecology, the Fifth Medical Center of Chinese PLA General Hospital, Beijing, 100071, China.

Yan Ju (Y)

Department of Gynecology, the Fifth Medical Center of Chinese PLA General Hospital, Beijing, 100071, China.

Hongyu Yin (H)

Department of Gynecology, the Fifth Medical Center of Chinese PLA General Hospital, Beijing, 100071, China.

Qingxiang Hou (Q)

Department of Obstetrics and Gynecology, PLA Rocket Force Characteristic Medical Center, Beijing, 100088, China.

Fei Liang (F)

Senior Department of Hematology, the Fifth Medical Center of Chinese PLA General Hospital, Beijing, 100071, China.

Nan Liu (N)

Senior Department of Hematology, the Fifth Medical Center of Chinese PLA General Hospital, Beijing, 100071, China.

Fudong Chen (F)

Medical School of the Chinese PLA General Hospital, Beijing, 100039, China.

Ruiwen Fan (R)

College of Veterinary Medicine, Shanxi Agricultural University, Taigu, 030801, Shanxi, China.

Yuying Sun (Y)

Senior Department of Hematology, the Fifth Medical Center of Chinese PLA General Hospital, Beijing, 100071, China. yuyingsun001@sina.com.

Yang Zeng (Y)

Senior Department of Hematology, the Fifth Medical Center of Chinese PLA General Hospital, Beijing, 100071, China. zengzengyang89@126.com.
Medical School of the Chinese PLA General Hospital, Beijing, 100039, China. zengzengyang89@126.com.
School of Basic Medical Sciences and Forensic Medicine, Hangzhou Medical College, Hangzhou, 311399, China. zengzengyang89@126.com.
ORCID: 0000-0002-6718-9501

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Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › Proteomics reveals dynamic metabolic changes...
questionsmedicales.fr › Systèmes sanguin et immunitaire › Système hématopoïétique › Cellules de la moelle osseuse › Cellules souches hématopoïétiques › Proteomics reveals dynamic metabolic changes...
questionsmedicales.fr › Disciplines des sciences naturelles › Chimie › Biochimie › Protéomique › Proteomics reveals dynamic metabolic changes...
questionsmedicales.fr › Produits chimiques inorganiques › Composés de l'oxygène › Espèces réactives de l'oxygène › Proteomics reveals dynamic metabolic changes...
questionsmedicales.fr › Structures de l'embryon › Foetus › Proteomics reveals dynamic metabolic changes...
questionsmedicales.fr › Personnes › Tranches d'âge › Adulte › Proteomics reveals dynamic metabolic changes...
questionsmedicales.fr › Structures de l'embryon › Foetus › Sang foetal › Proteomics reveals dynamic metabolic changes...
questionsmedicales.fr › Acides aminés, peptides et protéines › Acides aminés › Acides aminés soufrés › Méthionine › Méthionine sulfoximine › Buthionine sulfoximine › Proteomics reveals dynamic metabolic changes...
questionsmedicales.fr › Acides aminés, peptides et protéines › Peptides › Oligopeptides › Glutathion › Proteomics reveals dynamic metabolic changes...