Vitamin A-Retinoic Acid Signaling Regulates Hematopoietic Stem Cell Dormancy
Open accessAbstract
Dormant hematopoietic stem cells (dHSCs) are atop the hematopoietic hierarchy. The molecular identity of dHSCs and the mechanisms regulating their maintenance or exit from dormancy remain uncertain. Here, we use single-cell RNA sequencing (RNA-seq) analysis to show that the transition from dormancy toward cell-cycle entry is a continuous developmental path associated with upregulation of biosynthetic processes rather than a stepwise progression. In addition, low Myc levels and high expression of a retinoic acid program are characteristic for dHSCs. To follow the behavior of dHSCs in situ, a Gprc5c-controlled reporter mouse was established. Treatment with all-trans retinoic acid antagonizes stress-induced activation of dHSCs by restricting protein translation and levels of reactive oxygen species (ROS) and Myc. Mice maintained on a vitamin A-free diet lose HSCs and show a disrupted re-entry into dormancy after exposure to inflammatory stress stimuli. Our results highlight the impact of dietary vitamin A on the regulation of cell-cycle-mediated stem cell plasticity. VIDEO ABSTRACT.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
ATRA antagonizes stress-induced activation of dormant hematopoietic stem cells by restricting protein translation and oxidative stress.
“ATRA antagonizes stress-induced activation of dormant hematopoietic stem cells by restricting protein translation and oxidative stress8.”
From Advances and challenges in retinoid delivery systems in regenerative and therapeutic medicine (2020) · cites this paper as [8]
When mice were fed a vitamin A-free diet to deplete the RA reservoir, animals suffered functional impairment of hematopoietic stem cells and their numbers were unable to recover even after injection with an immunostimulant.
“When mice were fed a vitamin A-free diet to deplete the RA reservoir, animals suffered, among other effects, functional impairment of hematopoietic stem cells and their numbers were unable to recover even after injection with an immunostimulant8.”
From Advances and challenges in retinoid delivery systems in regenerative and therapeutic medicine (2020) · cites this paper as [8]
Cites
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
Love, M. I., Huber, W., & Anders, S. (2014) · Genome Biology · doi:10.1186/s13059-014-0550-8 · Cited by 95,106 · see citing works
STAR: ultrafast universal RNA-seq aligner
Dobin, A., Davis, C. A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M., & Gingeras, T. R. (2013) · Bioinformatics · doi:10.1093/bioinformatics/bts635 · Cited by 51,709 · see citing works
Gene Ontology: tool for the unification of biology
Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T., et al. (2000) · Nature Genetics · doi:10.1038/75556 · Cited by 43,206 · see citing works
(2008) · Journal of Machine Learning Research · Cited by 33,051 · see citing works
HTSeq—a Python framework to work with high-throughput sequencing data
Anders, S., Pyl, P. T., & Huber, W. (2015) · Bioinformatics · doi:10.1093/bioinformatics/btu638 · Cited by 21,464 · see citing works
Trapnell, C., Cacchiarelli, D., Grimsby, J., Pokharel, P., Li, S., Morse, M., Lennon, N. J., Livak, K. J., Mikkelsen, T. S., & Rinn, J. L. (2014) · Nature Biotechnology · doi:10.1038/nbt.2859 · Cited by 7,314 · see citing works
A Direct Measurement of the Radiation Sensitivity of Normal Mouse Bone Marrow Cells1
Till, J. E., & McCulloch, E. A. (2010) · Radiation Research · doi:10.1667/rrxx28.1 · Cited by 4,036 · see citing works
A Direct Measurement of the Radiation Sensitivity of Normal Mouse Bone Marrow Cells
Till, J. E., & McCulloch, E. A. (1961) · Radiation Research · doi:10.2307/3570892 · Cited by 3,770 · see citing works
Pierce, K. L., Premont, R. T., & Lefkowitz, R. J. (2002) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm908 · Cited by 2,712 · see citing works
A gene expression atlas of the central nervous system based on bacterial artificial chromosomes
Gong, S., Zheng, C., Doughty, M. L., Losos, K., Didkovsky, N., Schambra, U. B., Nowak, N. J., Joyner, A., Leblanc, G., Hatten, M. E., et al. (2003) · Nature · doi:10.1038/nature02033 · Cited by 2,108 · see citing works
Wilson, A., Laurenti, E., Oser, G., van der Wath, R. C., Blanco-Bose, W., Jaworski, M., Offner, S., Dunant, C. F., Eshkind, L., Bockamp, E., et al. (2008) · Cell · doi:10.1016/j.cell.2008.10.048 · Cited by 1,908 · see citing works
Self-citationVitamin effects on the immune system: Vitamins A and D take centre stage
Mora, J. R., Iwata, M., & von Andrian, U. H. (2008) · Nature Reviews Immunology · doi:10.1038/nri2378 · Cited by 1,559 · see citing works
Diffusion pseudotime robustly reconstructs lineage branching
Haghverdi, L., Büttner, M., Wolf, F. A., Buettner, F., & Theis, F. J. (2016) · Nature Methods · doi:10.1038/nmeth.3971 · Cited by 1,385 · see citing works
Self-citationStine, Z. E., Walton, Z. E., Altman, B. J., Hsieh, A. L., & Dang, C. V. (2015) · Cancer Discovery · doi:10.1158/2159-8290.cd-15-0507 · Cited by 1,375 · see citing works
IFNα activates dormant haematopoietic stem cells in vivo
Essers, M. A. G., Offner, S., Blanco-Bose, W. E., Waibler, Z., Kalinke, U., Duchosal, M. A., & Trumpp, A. (2009) · Nature · doi:10.1038/nature07815 · Cited by 1,368 · see citing works
Self-citationBuettner, F., Natarajan, K. N., Casale, F. P., Proserpio, V., Scialdone, A., Theis, F. J., Teichmann, S. A., Marioni, J. C., & Stegle, O. (2015) · Nature Biotechnology · doi:10.1038/nbt.3102 · Cited by 1,136 · see citing works
Self-citationProstaglandin E2 regulates vertebrate haematopoietic stem cell homeostasis
North, T. E., Goessling, W., Walkley, C. R., Lengerke, C., Kopani, K. R., Lord, A. M., Weber, G. J., Bowman, T. V., Jang, I. H., Großer, T., et al. (2007) · Nature · doi:10.1038/nature05883 · Cited by 1,095 · see citing works
Gene expression regulation by retinoic acid
Balmer, J. E., & Blomhoff, R. (2002) · Journal of Lipid Research · doi:10.1194/jlr.r100015-jlr200 · Cited by 1,039 · see citing works
Accounting for technical noise in single-cell RNA-seq experiments
Brennecke, P., Anders, S., Kim, J. K., Kołodziejczyk, A. A., Zhang, X., Proserpio, V., Baying, B., Benes, V., Teichmann, S. A., Marioni, J. C., et al. (2013) · Nature Methods · doi:10.1038/nmeth.2645 · Cited by 979 · see citing works
Self-citationHematopoietic stem cell: self‐renewal versus differentiation
Seita, J., & Weissman, I. L. (2010) · WIREs Systems Biology and Medicine · doi:10.1002/wsbm.86 · Cited by 925 · see citing works
Forcing cells to change lineages
Graf, T., & Enver, T. (2009) · Nature · doi:10.1038/nature08533 · Cited by 899 · see citing works
Camera: a competitive gene set test accounting for inter-gene correlation
Wu, D., & Smyth, G. K. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks461 · Cited by 880 · see citing works
Quiescent haematopoietic stem cells are activated by IFN-γ in response to chronic infection
Baldridge, M. T., King, K. Y., Boles, N. C., Weksberg, D. C., & Goodell, M. A. (2010) · Nature · doi:10.1038/nature09135 · Cited by 877 · see citing works
Metabolic Regulation of Hematopoietic Stem Cells in the Hypoxic Niche
Suda, T., Takubo, K., & Semenza, G. L. (2011) · Cell Stem Cell · doi:10.1016/j.stem.2011.09.010 · Cited by 844 · see citing works
mTORC1 controls the adaptive transition of quiescent stem cells from G0 to GAlert
Rodgers, J. T., King, K. Y., Brett, J. O., Cromie, M. J., Charville, G. W., Maguire, K. K., Brunson, C., Mastey, N., Liu, L., Tsai, C.-R., et al. (2014) · Nature · doi:10.1038/nature13255 · Cited by 776 · see citing works
Beerman, I., Bhattacharya, D., Zandi, S., Sigvardsson, M., Weissman, I. L., Bryder, D., & Rossi, D. J. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1000834107 · Cited by 711 · see citing works
Deep imaging of bone marrow shows non-dividing stem cells are mainly perisinusoidal
Acar, M., Kocherlakota, K. S., Murphy, M. M., Peyer, J. G., Oguro, H., Inra, C. N., Jaiyeola, C., Zhao, Z., Luby‐Phelps, K., & Morrison, S. J. (2015) · Nature · doi:10.1038/nature15250 · Cited by 702 · see citing works
Haematopoietic stem cells require a highly regulated protein synthesis rate
Signer, R. A. J., Magee, J. A., Salic, A., & Morrison, S. J. (2014) · Nature · doi:10.1038/nature13035 · Cited by 674 · see citing works
Diffusion maps for high-dimensional single-cell analysis of differentiation data
Haghverdi, L., Buettner, F., & Theis, F. J. (2015) · Bioinformatics · doi:10.1093/bioinformatics/btv325 · Cited by 649 · see citing works
Self-citation<i>destiny</i> : diffusion maps for large-scale single-cell data in R
Angerer, P., Haghverdi, L., Büttner, M., Theis, F. J., Marr, C., & Buettner, F. (2016) · Bioinformatics · doi:10.1093/bioinformatics/btv715 · Cited by 640 · see citing works
Self-citationExit from dormancy provokes DNA-damage-induced attrition in haematopoietic stem cells
Walter, D., Lier, A., Geiselhart, A., Thalheimer, F. B., Huntscha, S., Sobotta, M. C., Moehrle, B., Brocks, D., Bayindir, I., Kaschutnig, P., et al. (2015) · Nature · doi:10.1038/nature14131 · Cited by 619 · see citing works
Self-citationRetinoids, Retinoic Acid Receptors, and Cancer
Tang, X.-H., & Gudas, L. J. (2011) · Annual Review of Pathology: Mechanisms of Disease · doi:10.1146/annurev-pathol-011110-130303 · Cited by 596 · see citing works
Analysis of histone 2B-GFP retention reveals slowly cycling hematopoietic stem cells
Foudi, A., Hochedlinger, K., Van Buren, D., Schindler, J. W., Jaenisch, R., Carey, V., & Hock, H. (2009) · Nature Biotechnology · doi:10.1038/nbt.1517 · Cited by 586 · see citing works
Fluorescent Protein-Based Redox Probes
Meyer, A. J., & Dick, T. P. (2010) · Antioxidants and Redox Signaling · doi:10.1089/ars.2009.2948 · Cited by 528 · see citing works
Self-citationChute, J. P., Muramoto, G. G., Whitesides, J. G., Colvin, M., Safi, R., Chao, N. J. A., & McDonnell, D. P. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0603806103 · Cited by 467 · see citing works
Wilson, N. K., Kent, D. G., Buettner, F., Shehata, M., Macaulay, I. C., Calero-Nieto, F. J., Sánchez Castillo, M., Oedekoven, C. A., Diamanti, E., Schulte, R., et al. (2015) · Cell Stem Cell · doi:10.1016/j.stem.2015.04.004 · Cited by 466 · see citing works
Self-citationHeterogeneity and hierarchy within the most primitive hematopoietic stem cell compartment
Morita, Y., Ema, H., & Nakauchi, H. (2010) · The Journal of Experimental Medicine · doi:10.1084/jem.20091318 · Cited by 456 · see citing works
Imaging protein synthesis in cells and tissues with an alkyne analog of puromycin
Liu, J., Xu, Y., Stoleru, D., & Salic, A. N. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1111561108 · Cited by 429 · see citing works
WikiPathways: capturing the full diversity of pathway knowledge
Kutmon, M., Riutta, A., Nunes, N. M., Hanspers, K., Willighagen, E., Bohler, A., Mélius, J., Waagmeester, A., Sinha, S. R., Miller, R. A., et al. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv1024 · Cited by 418 · see citing works
Computational assignment of cell-cycle stage from single-cell transcriptome data
Scialdone, A., Natarajan, K. N., Saraiva, L. R., Proserpio, V., Teichmann, S. A., Stegle, O., Marioni, J. C., & Buettner, F. (2015) · Methods · doi:10.1016/j.ymeth.2015.06.021 · Cited by 410 · see citing works
Self-citationHematopoietic Cytokines Can Instruct Lineage Choice
Rieger, M. A., Hoppe, P. S., Smejkal, B. M., Eitelhuber, A. C., & Schroeder, T. (2009) · Science · doi:10.1126/science.1171461 · Cited by 404 · see citing works
Self-citationMolecular Signatures of Proliferation and Quiescence in Hematopoietic Stem Cells
Bowman, T. V., Merchant, A. A., Ramos, C. A., Whitehouse, N. L., Young, A., Shaw, C. A., & Goodell, M. A. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020301 · Cited by 363 · see citing works
Cabezas-Wallscheid, N., Klimmeck, D., Hansson, J., Lipka, D., Reyes, A., Wang, Q., Weichenhan, D., Lier, A., von Paleske, L., Renders, S., et al. (2014) · Cell Stem Cell · doi:10.1016/j.stem.2014.07.005 · Cited by 352 · see citing works
Self-citationHoxb5 marks long-term haematopoietic stem cells and reveals a homogenous perivascular niche
Chen, J. Y., Miyanishi, M., Wang, S. K., Yamazaki, S., Sinha, R., Kao, K. S., Seita, J., Sahoo, D., Nakauchi, H., & Weissman, I. L. (2016) · Nature · doi:10.1038/nature16943 · Cited by 345 · see citing works
CDK6 Levels Regulate Quiescence Exit in Human Hematopoietic Stem Cells
Laurenti, E., Frelin, C., Xie, S. Z.-J., Ferrari, R., Dunant, C. F., Zandi, S., Neumann, A. L., Plumb, I., Doulatov, S. R., Chen, J., et al. (2015) · Cell stem cell · doi:10.1016/j.stem.2015.01.017 · Cited by 340 · see citing works
Ludin, A., Gur‐Cohen, S., Golan, K., Kaufmann, K. B., Itkin, T., Medaglia, C., Lu, X., Ledergor, G., Kollet, Ó., & Lapidot, T. (2014) · Antioxidants and Redox Signaling · doi:10.1089/ars.2014.5941 · Cited by 333 · see citing works
Hematopoietic stem cell function and survival depend on c-Myc and N-Myc activity
Laurenti, E., Varnum-Finney, B., Wilson, A., Ferrero, I., Blanco-Bose, W. E., Ehninger, A., Knoepfler, P. S., Cheng, P.-F., MacDonald, H. R., Eisenman, R. N., et al. (2008) · Cell Stem Cell · doi:10.1016/j.stem.2008.09.005 · Cited by 305 · see citing works
Self-citationZou, P., Yoshihara, H., Hosokawa, K., Tai, I., Shinmyozu, K., Tsukahara, F., Maru, Y., Nakayama, K., Nakayama, K. I., & Suda, T. (2011) · Cell stem cell · doi:10.1016/j.stem.2011.07.003 · Cited by 289 · see citing works
Hematopoietic stem cells count and remember self-renewal divisions
Bernitz, J. M., Kim, H. S., MacArthur, B., Sieburg, H., & Moore, K. (2016) · Cell · doi:10.1016/j.cell.2016.10.022 · Cited by 285 · see citing works
Dynamic variation in cycling of hematopoietic stem cells in steady state and inflammation
Takizawa, H., Regoes, R. R., Boddupalli, C. S., Bonhoeffer, S., & Manz, M. G. (2011) · The Journal of Experimental Medicine · doi:10.1084/jem.20101643 · Cited by 283 · see citing works
Myc Depletion Induces a Pluripotent Dormant State Mimicking Diapause
Scognamiglio, R., Cabezas-Wallscheid, N., Thier, M. C., Altamura, S., Reyes, A., Prendergast, Á. M., Baumgärtner, D., Carnevalli, L. S., Atzberger, A., Haas, S., et al. (2016) · Cell · doi:10.1016/j.cell.2015.12.033 · Cited by 271 · see citing works
Self-citationRegulation of Ribosome Biogenesis and Protein Synthesis Controls Germline Stem Cell Differentiation
Sanchez, C. G., Teixeira, F. K., Czech, B., Preall, J. B., Zamparini, A. L., Seifert, J. R. K., Malone, C. D., Hannon, G. J., & Lehmann, R. (2015) · Cell stem cell · doi:10.1016/j.stem.2015.11.004 · Cited by 240 · see citing works
MYC inhibition induces metabolic changes leading to accumulation of lipid droplets in tumor cells
Zirath, H., Frenzel, A., Oliynyk, G., Segerström, L., Westermark, U., Larsson, K., Persson, M. M., Hultenby, K. R., Lehtiö, J., Einvik, C., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1222404110 · Cited by 229 · see citing works
Reinisch, A., Thomas, D., Corces, M. R., Zhang, X., Gratzinger, D. A., Hong, W., Schallmoser, K., Strunk, D., & Majeti, R. (2016) · Nature Medicine · doi:10.1038/nm.4103 · Cited by 222 · see citing works
Antonchuk, J., Sauvageau, G., & Humphries, R. K. (2001) · Experimental Hematology · doi:10.1016/s0301-472x(01)00681-6 · Cited by 221 · see citing works
Retinoic Acid Signaling Is Essential for Embryonic Hematopoietic Stem Cell Development
Chanda, B., Ditadi, A., Iscove, N. N., & Keller, G. (2013) · Cell · doi:10.1016/j.cell.2013.08.055 · Cited by 201 · see citing works
Fgd5 identifies hematopoietic stem cells in the murine bone marrow
Gazit, R., Mandal, P. K., Ebina, W., Ben‐Zvi, A., Nombela‐Arrieta, C., Silberstein, L. E., & Rossi, D. J. (2014) · The Journal of Experimental Medicine · doi:10.1084/jem.20130428 · Cited by 194 · see citing works
Ghiaur, G., Yegnasubramanian, S., Perkins, B. N., Gucwa, J. L., Gerber, J. M., & Jones, R. J. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1305937110 · Cited by 136 · see citing works
Divisional History and Hematopoietic Stem Cell Function during Homeostasis
Qiu, J., Papatsenko, D., Niu, X., Schaniel, C., & Moore, K. A. (2014) · Stem Cell Reports · doi:10.1016/j.stemcr.2014.01.016 · Cited by 131 · see citing works
Purton, L. E., Bernstein, I. D., & Collins, S. J. (2000) · Blood · doi:10.1182/blood.v95.2.470 · Cited by 129 · see citing works
Robbins, M. J., Michalovich, D., Hill, J., Calver, A. R., Medhurst, A. D., Gloger, I., Sims, M., Middlemiss, D. N., & Pangalos, M. N. (2000) · Genomics · doi:10.1006/geno.2000.6226 · Cited by 128 · see citing works
Huang, C., Bredemeyer, A. L., Walker, L. M., et al. (2008) · European Journal of Immunology · doi:10.1002/eji.200737972 · Cited by 125 · see citing works
Seeing through the dark: New insights into the immune regulatory functions of vitamin A
Brown, C. C., & Noelle, R. J. (2015) · European Journal of Immunology · doi:10.1002/eji.201344398 · Cited by 116 · see citing works
Purton, L. E., Bernstein, I. D., & Collins, S. J. (1999) · Blood · doi:10.1182/blood.v94.2.483 · Cited by 113 · see citing works
van der Wath, R. C., Wilson, A., Laurenti, E., Trumpp, A., & Lió, P. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006972 · Cited by 82 · see citing works
Self-citationMouse redox histology using genetically encoded probes
Fujikawa, Y., Roma, L., Sobotta, M. C., Rose, A., Diaz, M. B., Locatelli, G., Breckwoldt, M., Misgeld, T., Kerschensteiner, M., Herzig, S., et al. (2016) · Science Signaling · doi:10.1126/scisignal.aad3895 · Cited by 77 · see citing works
Self-citationRetinoic acid receptors, hematopoiesis and leukemogenesis
Collins, S. J. (2008) · Current Opinion in Hematology · doi:10.1097/moh.0b013e3283007edf · Cited by 71 · see citing works
Haetscher, N., Feuermann, Y., Wingert, S., Rehage, M., Thalheimer, F. B., Weiser, C., Bohnenberger, H., Jung, K., Schroeder, T., Serve, H. L., et al. (2015) · Nature Communications · doi:10.1038/ncomms9928 · Cited by 59 · see citing works
Self-citationHematopoietic stem cell quiescence and function are controlled by the CYLD–TRAF2–p38MAPK pathway
Tesio, M., Tang, Y., Müdder, K., Saini, M., von Paleske, L., Macintyre, E. A., Pasparakis, M., Waisman, A., & Trumpp, A. (2015) · The Journal of Experimental Medicine · doi:10.1084/jem.20141438 · Cited by 55 · see citing works
Self-citationAll-transretinoic acid in the treatment of pediatric acute promyelocytic leukemia
Masetti, R., Vendemini, F., Zama, D., Biagi, C., Gasperini, P., & Pession, A. (2012) · Expert Review of Anticancer Therapy · doi:10.1586/era.12.101 · Cited by 51 · see citing works
Die experimentelle Avitaminose A beim Menschen. Mit 9 Figure im Text und auf Tafel III.
Wagner, K. (1940) · Hoppe-Seyler´s Zeitschrift für physiologische Chemie · doi:10.1515/bchm2.1940.264.3-4.153 · Cited by 48 · see citing works
Lipka, D. B., Wang, Q., Cabezas‐Wallscheid, N., Klimmeck, D., Weichenhan, D., Herrmann, C., Lier, A., Brocks, D., von Paleske, L., Renders, S., et al. (2014) · Cell Cycle · doi:10.4161/15384101.2014.973334 · Cited by 46 · see citing works
Self-citationCytokine-Regulated GADD45G Induces Differentiation and Lineage Selection in Hematopoietic Stem Cells
Thalheimer, F. B., Wingert, S., Giacomo, P. D., Haetscher, N., Rehage, M., Brill, B., Theis, F. J., Hennighausen, L. G., Schroeder, T., & Rieger, M. A. (2014) · Stem Cell Reports · doi:10.1016/j.stemcr.2014.05.010 · Cited by 44 · see citing works
Self-citationRole of key regulators of the cell cycle in maintenance of hematopoietic stem cells
Matsumoto, A., & Nakayama, K. I. (2012) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2012.07.004 · Cited by 43 · see citing works
Ehninger, A., Boch, T., Uckelmann, H. J., et al. (2014) · Blood · doi:10.1182/blood-2013-10-531038 · Cited by 36 · see citing works
Klimmeck, D., Cabezas‐Wallscheid, N., Reyes, A., von Paleske, L., Renders, S., Hansson, J., Krijgsveld, J., Huber, W. K., & Trumpp, A. (2014) · Stem Cell Reports · doi:10.1016/j.stemcr.2014.08.012 · Cited by 36 · see citing works
Self-citationJacobsen, S. E. W., Fahlman, C., Blomhoff, H. K., et al. (1994) · The Journal of Experimental Medicine · doi:10.1084/jem.179.5.1665 · Cited by 34 · see citing works
Sano, T., Kim, Y., Oshima, E., Shimizu, C., Kiyonari, H., Abe, T., Higashi, H., Yamada, K., & Hirabayashi, Y. (2011) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2011.07.118 · Cited by 34 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Giladi, A., Paul, F., Herzog, Y., Lubling, Y., Weiner, A., Yofe, I., Jaitin, D., Cabezas-Wallscheid, N., Dress, R., Ginhoux, F., et al. (2018) · Nature Cell Biology · doi:10.1038/s41556-018-0121-4 · Cited by 366 · see citing works
Self-citationHepatic stellate cells suppress NK cell-sustained breast cancer dormancy
Correia, A. L., Guimaraes, J. C., Auf der Maur, P., De Silva, D., Trefny, M. P., Okamoto, R., Bruno, S., Schmidt, A., Mertz, K., Volkmann, K., et al. (2021) · Nature · doi:10.1038/s41586-021-03614-z · Cited by 339 · see citing works
Bogeska, R., Mikecin, A.-M., Kaschutnig, P., Fawaz, M., Büchler-Schäff, M., Le, D., Ganuza, M., Vollmer, A., Paffenholz, S. V., Asada, N., et al. (2022) · Cell Stem Cell · doi:10.1016/j.stem.2022.06.012 · Cited by 299 · see citing works
Self-citationCellular and epigenetic drivers of stem cell ageing
Ermolaeva, M., Neri, F., Ori, A., & Rudolph, K. L. (2018) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-018-0020-3 · Cited by 272 · see citing works
Harris, L., Rigo, P., Stiehl, T., Gaber, Z. B., Austin, S. H. L., Masdeu, M. D. M., Edwards, A., Urbán, N., Marciniak-Czochra, A., & Guillemot, F. (2021) · Cell Stem Cell · doi:10.1016/j.stem.2021.01.003 · Cited by 173 · see citing works
Advances and challenges in retinoid delivery systems in regenerative and therapeutic medicine
Ferreira, R., Napoli, J., Enver, T., Bernardino, L., & Ferreira, L. (2020) · Nature Communications · doi:10.1038/s41467-020-18042-2 · Cited by 138 · see citing works
Haematopoietic stem cells in perisinusoidal niches are protected from ageing
Saçma, M., Pospiech, J., Bogeska, R., de Back, W., Mallm, J.-P., Sakk, V., Soller, K., Marka, G., Vollmer, A., Karns, R., et al. (2019) · Nature Cell Biology · doi:10.1038/s41556-019-0418-y · Cited by 133 · see citing works
Self-citationMetabolic regulation of somatic stem cells in vivo
Meacham, C. E., DeVilbiss, A. W., & Morrison, S. J. (2022) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-022-00462-1 · Cited by 85 · see citing works
Metabolic regulation of tissue stem cells
Shapira, S. N., & Christofk, H. R. (2020) · Trends in Cell Biology · doi:10.1016/j.tcb.2020.04.004 · Cited by 82 · see citing works
Dissecting Murine Muscle Stem Cell Aging through Regeneration Using Integrative Genomic Analysis
Shcherbina, A., Larouche, J., Fraczek, P., Yang, B. A., Brown, L. A., Markworth, J. F., Chung, C. H., Khaliq, M., de Silva, K., Choi, J. J., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107964 · Cited by 76 · see citing works
HDAC11 deficiency disrupts oncogene-induced hematopoiesis in myeloproliferative neoplasms
Yue, L., Sharma, V., Horvat, N. P., Akuffo, A. A., Beatty, M. S., Murdun, C., Colin, C., Billington, J. M. R., Goodheart, W. E., Sahakian, E., et al. (2020) · Blood · doi:10.1182/blood.2019895326 · Cited by 67 · see citing works
The Source and Dynamics of Adult Hematopoiesis: Insights from Lineage Tracing
Pucella, J. N., Upadhaya, S., & Reizis, B. (2020) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-020520-114601 · Cited by 53 · see citing works
Rabe, J. L., Hernandez, G., Chavez, J. S., Mills, T. S., Nerlov, C., & Pietras, E. M. (2020) · Experimental Hematology · doi:10.1016/j.exphem.2019.12.003 · Cited by 49 · see citing works
PI3K alpha and delta promote hematopoietic stem cell activation
Hemmati, S., Sinclair, T., Tong, M., Bartholdy, B., Okabe, R. O., Ames, K., Ostrodka, L., Haque, T., Kaur, I., Mills, T. S., et al. (2019) · JCI Insight · doi:10.1172/jci.insight.125832 · Cited by 40 · see citing works
Advancing insights into stem cell niche complexities with next-generation technologies
Heitman, N., Saxena, N., & Rendl, M. (2018) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2018.06.012 · Cited by 31 · see citing works
- Authors
- Cabezas-Wallscheid, N., Buettner, F., Sommerkamp, P., Klimmeck, D., Ladel, L., Thalheimer, F. B., Pastor-Flores, D., Roma, L. P., Renders, S., Zeisberger, P., Przybylla, A., Schönberger, K., Scognamiglio, R., Altamura, S., Florian, C. M., Fawaz, M., Vonficht, D., Tesio, M., Collier, P., Pavlinic, D., Geiger, H., Schroeder, T., Benes, V., Dick, T. P., Rieger, M. A., Stegle, O., & Trumpp, A.
- Affiliations
- European Bioinformatics Institute (GB)
- German Cancer Research Center (DE)
- Goethe University Frankfurt (DE)
- Heidelberg University (DE)
- European Molecular Biology Laboratory (DE)
- Universität Ulm (DE)
- ETH Zurich (CH)
- Corresponding author
- Trumpp, Andreas
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2017-05
- Volume
- 169
- Issue
- 5
- Pages
- 807-823.e19
- ISSN
- 0092-8674 (ISSN-L)
- OpenAlex
- W2610808603
- Cited by
- 454
- References
- 78
- Citations by year
- 2026: 31 · 2025: 47 · 2024: 51 · 2023: 53 · 2022: 69 · 2021: 48 · 2020: 48 · 2019: 53 · 2018: 44 · 2017: 9
- FWCI
- 32.34
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
- Funders
- UK Medical Research Council (MRC (MR/M01536X/1, FOR2033, SFB873)
- Deutsche Forschungsgemeinschaft (DFG)
- Dietmar Hopp Foundation
- Topics
- Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Retinoids in leukemia and cellular processes
- Health Sciences › Medicine › Genetics › Mesenchymal stem cell research
- Keywords
- hematopoietic stem cells, stem cell quiescence, retinoic acid signaling, vitamin A, c-Myc, cell cycle entry, stem cell plasticity, reactive oxygen species, mRNA translation, inflammatory stress, single-cell RNA sequencing
- MeSH terms
- Animals, Cell Cycle, Cell Survival, Diet, Hematopoietic Stem Cells, Poly I-C, Stress, Physiological, Tretinoin, Vitamin A, Vitamins, Signal Transduction, Reactive Oxygen Species, Cell Culture Techniques, Gene Expression Profiling, Receptors, G-Protein-Coupled, Mice, Biosynthetic Pathways, Single-Cell Analysis
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