Lipoprotein metabolism mediates hematopoietic stem cell responses under acute anemic conditions.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
16 Sep 2024
16 Sep 2024
Historique:
received:
05
12
2022
accepted:
06
09
2024
medline:
17
9
2024
pubmed:
17
9
2024
entrez:
16
9
2024
Statut:
epublish
Résumé
Hematopoietic stem cells (HSCs) react to various stress conditions. However, it is unclear whether and how HSCs respond to severe anemia. Here, we demonstrate that upon induction of acute anemia, HSCs rapidly proliferate and enhance their erythroid differentiation potential. In severe anemia, lipoprotein profiles largely change and the concentration of ApoE increases. In HSCs, transcription levels of lipid metabolism-related genes, such as very low-density lipoprotein receptor (Vldlr), are upregulated. Stimulation of HSCs with ApoE enhances their erythroid potential, whereas HSCs in Apoe knockout mice do not respond to anemia induction. Vldlr
Identifiants
pubmed: 39284836
doi: 10.1038/s41467-024-52509-w
pii: 10.1038/s41467-024-52509-w
doi:
Substances chimiques
Apolipoproteins E
0
Lipoproteins
0
Receptors, LDL
0
Chromatin
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
8131Informations de copyright
© 2024. The Author(s).
Références
Orkin, S. H. & Zon, L. I. Hematopoiesis: an evolving paradigm for stem cell biology. Cell 132, 631–644 (2008).
pubmed: 18295580
pmcid: 2628169
doi: 10.1016/j.cell.2008.01.025
Takizawa, H. et al. Pathogen-induced TLR4-TRIF innate immune signaling in hematopoietic stem cells promotes proliferation but reduces competitive fitness. Cell Stem Cell 21, 225–240 (2017).
pubmed: 28736216
doi: 10.1016/j.stem.2017.06.013
Umemoto, T., Hashimoto, M., Matsumura, T., Nakamura-Ishizu, A. & Suda, T. Ca
pubmed: 29946000
pmcid: 6080917
doi: 10.1084/jem.20180421
Sigurdsson, V. et al. Induction of blood-circulating bile acids supports recovery from myelosuppressive chemotherapy. Blood Adv. 4, 1833–1843 (2020).
pubmed: 32365188
pmcid: 7218440
doi: 10.1182/bloodadvances.2019000133
Umemoto, T. et al. ATP citrate lyase controls hematopoietic stem cell fate and supports bone marrow regeneration. EMBO J. 41, e109463 (2022).
pubmed: 35229328
pmcid: 9016348
doi: 10.15252/embj.2021109463
Baldridge, M. T., King, K. Y., Boles, N. C., Weksberg, D. C. & Goodell, M. A. Quiescent haematopoietic stem cells are activated by IFN-gamma in response to chronic infection. Nature 465, 793–797 (2010).
pubmed: 20535209
pmcid: 2935898
doi: 10.1038/nature09135
Mossadegh-Keller, N. et al. M-CSF instructs myeloid lineage fate in single haematopoietic stem cells. Nature 497, 239–243 (2013).
pubmed: 23575636
pmcid: 3679883
doi: 10.1038/nature12026
Pietras, E. M. et al. Chronic interleukin-1 exposure drives haematopoietic stem cells towards precocious myeloid differentiation at the expense of self-renewal. Nat. Cell Biol. 18, 607–618 (2016).
pubmed: 27111842
pmcid: 4884136
doi: 10.1038/ncb3346
Yamashita, M. & Passegué, E. TNF-α coordinates hematopoietic stem cell survival and myeloid regeneration. Cell Stem Cell 25, 357–372 (2019).
pubmed: 31230859
pmcid: 6733032
doi: 10.1016/j.stem.2019.05.019
Sender, R., Fuchs, S. & Milo, R. Revised estimates for the number of human and bacteria cells in the body. PLoS Biol. 14, e1002533 (2016).
pubmed: 27541692
pmcid: 4991899
doi: 10.1371/journal.pbio.1002533
Lee, H. Y. et al. PPAR-α and glucocorticoid receptor synergize to promote erythroid progenitor self-renewal. Nature 522, 474–477 (2015).
pubmed: 25970251
pmcid: 4498266
doi: 10.1038/nature14326
Singbrant, S., Mattebo, A., Sigvardsson, M., Strid, T. & Flygare, J. Prospective isolation of radiation induced erythroid stress progenitors reveals unique transcriptomic and epigenetic signatures enabling increased erythroid output. Haematologica 105, 2561–2571 (2020).
pubmed: 33131245
pmcid: 7604643
doi: 10.3324/haematol.2019.234542
Kirby, S., Walton, W. & Smithies, O. Hematopoietic stem cells with controllable tEpoR transgenes have a competitive advantage in bone marrow transplantation. Blood 95, 3710–3175 (2000).
pubmed: 10845901
doi: 10.1182/blood.V95.12.3710
Koury, M. L. & Haase, V. H. Anaemia in kidney disease: harnessing hypoxia responses for therapy. Nat. Rev. Nephrol. 11, 394–410 (2015).
pubmed: 26055355
pmcid: 4497972
doi: 10.1038/nrneph.2015.82
Zhang, H. et al. EpoR-tdTomato-Cre mice enable identification of EpoR expression in subsets of tissue macrophages and hematopoietic cells. Blood 138, 1986–1997 (2021).
pubmed: 34098576
pmcid: 8767788
doi: 10.1182/blood.2021011410
Shiozawa, Y. et al. Erythropoietin couples hematopoiesis with bone formation. PLoS One 5, e10853 (2010).
pubmed: 20523730
pmcid: 2877712
doi: 10.1371/journal.pone.0010853
Grover, A. et al. Erythropoietin guides multipotent hematopoietic progenitor cells toward an erythroid fate. J. Exp. Med. 211, 181–188 (2014).
pubmed: 24493804
pmcid: 3920567
doi: 10.1084/jem.20131189
Zhang, D. et al. The microbiota regulates hematopoietic stem cell fate decisions by controlling iron availability in bone marrow. Cell Stem Cell 29, 232–247 (2022).
pubmed: 35065706
pmcid: 8818037
doi: 10.1016/j.stem.2021.12.009
Singh, R. P. et al. Hematopoietic stem cells but not multipotent progenitors drive erythropoiesis during chronic erythroid stress in EPO transgenic mice. Stem Cell Rep. 10, 1908–1919 (2018).
doi: 10.1016/j.stemcr.2018.04.012
Miyagawa, S., Kobayashi, M., Konishi, N., Sato, T. & Ueda, K. Insulin and insulin-like growth factor I support the proliferation of erythroid progenitor cells in bone marrow through the sharing of receptors. Br. J. Haematol. 109, 555–562 (2000).
pubmed: 10886204
doi: 10.1046/j.1365-2141.2000.02047.x
Lenox, L. E., Perry, J. M. & Paulson, R. F. BMP4 and Madh5 regulate the erythroid response to acute anemia. Blood 105, 2741–2748 (2005).
pubmed: 15591122
doi: 10.1182/blood-2004-02-0703
Kadri, Z. et al. Erythropoietin and IGF-1 signaling synchronize cell proliferation and maturation during erythropoiesis. Genes Dev. 29, 2603–2616 (2015).
pubmed: 26680303
pmcid: 4699388
doi: 10.1101/gad.267633.115
Mahley, R. W., Innerarity, T. L., Rall, S. C. Jr. & Weisgraber, K. H. Plasma lipoproteins: apolipoprotein structure and function. J. Lipid Res. 25, 1277–1294 (1984).
pubmed: 6099394
doi: 10.1016/S0022-2275(20)34443-6
Marais, A. D. Apolipoprotein E in lipoprotein metabolism, health and cardiovascular disease. Pathology 51, 165–176 (2019).
pubmed: 30598326
doi: 10.1016/j.pathol.2018.11.002
Gordon, D. J. et al. High-density lipoprotein cholesterol and cardiovascular disease. Four prospective American studies. Circulation 79, 8–15 (1989).
pubmed: 2642759
doi: 10.1161/01.CIR.79.1.8
Hansson, G. K. & Hermansson, A. The immune system in atherosclerosis. Nat. Immunol. 12, 204–212 (2011).
pubmed: 21321594
doi: 10.1038/ni.2001
Schnitzler, J. G. et al. Atherogenic Lipoprotein(a) increases vascular glycolysis, thereby facilitating inflammation and leukocyte extravasation. Circ. Res. 126, 1346–1359 (2020).
pubmed: 32160811
pmcid: 7208285
doi: 10.1161/CIRCRESAHA.119.316206
Heyde, A. et al. Increased stem cell proliferation in atherosclerosis accelerates clonal hematopoiesis. Cell 184, 1348–1361 (2021).
pubmed: 33636128
pmcid: 8109274
doi: 10.1016/j.cell.2021.01.049
Yvan-Charvet, L. et al. ATP-binding cassette transporters and HDL suppress hematopoietic stem cell proliferation. Science 328, 1689–1693 (2010).
pubmed: 20488992
pmcid: 3032591
doi: 10.1126/science.1189731
Miharada, K., Hiroyama, T., Sudo, K., Nagasawa, T. & Nakamura, Y. Lipocalin 2 functions as a negative regulator of red blood cell production in an autocrine fashion. FASEB J. 19, 1881–1883 (2005).
pubmed: 16157692
doi: 10.1096/fj.05-3809fje
Bennett, L. F., Liao, C. & Paulson, R. F. Stress erythropoiesis model systems. Methods Mol. Biol. 1698, 91–102 (2018).
pubmed: 29076085
pmcid: 6510234
doi: 10.1007/978-1-4939-7428-3_5
Nakada, D. et al. Oestrogen increases haematopoietic stem-cell self-renewal in females and during pregnancy. Nature 505, 555–558 (2014).
pubmed: 24451543
pmcid: 4015622
doi: 10.1038/nature12932
Akashi, K., Traver, D., Miyamoto, T. & Weissman, I. L. A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature 404, 193–197 (2000).
pubmed: 10724173
doi: 10.1038/35004599
Mende, N. & Laurenti, E. Hematopoietic stem and progenitor cells outside the bone marrow: where, when, and why. Exp. Hematol. 104, 9–16 (2021).
pubmed: 34687807
doi: 10.1016/j.exphem.2021.10.002
Hamanaka, S. et al. Generation of transgenic mouse line expressing Kusabira Orange throughout body, including erythrocytes, by random segregation of provirus method. Biochem. Biophys. Res. Commun. 435, 586–591 (2013).
pubmed: 23685154
doi: 10.1016/j.bbrc.2013.05.017
Yamamoto, R. et al. Clonal analysis unveils self-renewing lineage-restricted progenitors generated directly from hematopoietic stem cells. Cell 154, 1112–1126 (2013).
pubmed: 23993099
doi: 10.1016/j.cell.2013.08.007
Sugiyama, T., Kohara, H., Noda, M. & Nagasawa, T. Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity 25, 977–988 (2006).
pubmed: 17174120
doi: 10.1016/j.immuni.2006.10.016
Ding, L., Saunders, T. L., Enikolopov, G. & Morrison, S. J. Endothelial and perivascular cells maintain haematopoietic stem cells. Nature 481, 457–462 (2012).
pubmed: 22281595
pmcid: 3270376
doi: 10.1038/nature10783
Greenbaum, A. et al. CXCL12 in early mesenchymal progenitors is required for haematopoietic stem-cell maintenance. Nature 495, 227–230 (2013).
pubmed: 23434756
pmcid: 3600148
doi: 10.1038/nature11926
Comazzetto, S. et al. Restricted hematopoietic progenitors and erythropoiesis require SCF from leptin receptor+ niche cells in the bone marrow. Cell Stem Cell 24, 477–486 (2019).
pubmed: 30661958
pmcid: 6813769
doi: 10.1016/j.stem.2018.11.022
Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 102, 15545–15550 (2005).
pubmed: 16199517
pmcid: 1239896
doi: 10.1073/pnas.0506580102
Alayash, A. I. Oxygen therapeutics: can we tame haemoglobin? Nat. Rev. Drug Discov. 3, 152–159 (2004).
pubmed: 15043006
doi: 10.1038/nrd1307
Ascenzi, P. et al. Hemoglobin and heme scavenging. IUBMB Life 57, 749–759 (2005).
pubmed: 16511968
doi: 10.1080/15216540500380871
Theilgaard-Mönch, K. et al. Haptoglobin is synthesized during granulocyte differentiation, stored in specific granules, and released by neutrophils in response to activation. Blood 108, 353–361 (2006).
pubmed: 16543473
doi: 10.1182/blood-2005-09-3890
Andersen, C. B. F. et al. Haptoglobin. Antioxid. Redox Signal 26, 814–831 (2017).
pubmed: 27650279
doi: 10.1089/ars.2016.6793
Law, S. K. et al. A new macrophage differentiation antigen which is a member of the scavenger receptor superfamily. Eur. J. Immunol. 23, 2320–2325 (1993).
pubmed: 8370408
doi: 10.1002/eji.1830230940
Kristensen, M. et al. Identification of the haemoglobin scavenger receptor. Nature 409, 198–201 (2001).
doi: 10.1038/35051594
Schaer, D. J. et al. CD163 is the macrophage scavenger receptor for native and chemically modified hemoglobins in the absence of haptoglobin. Blood 107, 373–380 (2006).
pubmed: 16189277
doi: 10.1182/blood-2005-03-1014
Buehler, P. W. et al. Haptoglobin preserves the CD163 hemoglobin scavenger pathway by shielding hemoglobin from peroxidative modification. Blood 113, 2578–2586 (2009).
pubmed: 19131549
doi: 10.1182/blood-2008-08-174466
Martin, E. W. et al. Chromatin accessibility maps provide evidence of multilineage gene priming in hematopoietic stem cells. Epigenetics Chromatin 14, 2 (2021).
pubmed: 33407811
pmcid: 7789351
doi: 10.1186/s13072-020-00377-1
Buenrostro, J. D., Giresi, P. G., Zaba, L. C., Chang, H. Y. & Greenleaf, W. J. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat. Methods 10, 1213–1218 (2013).
pubmed: 24097267
pmcid: 3959825
doi: 10.1038/nmeth.2688
Reddy, E. S., Rao, V. N. & Papas, T. S. The erg gene: a human gene related to the ets oncogene. Proc. Natl. Acad. Sci. USA 84, 6131–6135 (1987).
pubmed: 3476934
pmcid: 299022
doi: 10.1073/pnas.84.17.6131
Loughran, S. J. et al. The transcription factor Erg is essential for definitive hematopoiesis and the function of adult hematopoietic stem cells. Nat. Immunol. 9, 810–819 (2008).
pubmed: 18500345
doi: 10.1038/ni.1617
Stankiewicz, M. J. & Crispino, J. D. ETS2 and ERG promote megakaryopoiesis and synergize with alterations in GATA-1 to immortalize hematopoietic progenitor cells. Blood 113, 3337–3347 (2009).
pubmed: 19168790
pmcid: 2665899
doi: 10.1182/blood-2008-08-174813
Kruse, E. A. et al. Dual requirement for the ETS transcription factors Fli-1 and Erg in hematopoietic stem cells and the megakaryocyte lineage. Proc. Natl. Acad. Sci. USA 106, 13814–13819 (2009).
pubmed: 19666492
pmcid: 2728977
doi: 10.1073/pnas.0906556106
Ng, A. P. et al. Erg is required for self-renewal of hematopoietic stem cells during stress hematopoiesis in mice. Blood 118, 2454–2461 (2011).
pubmed: 21673349
doi: 10.1182/blood-2011-03-344739
Knudsen, K. J. et al. ERG promotes the maintenance of hematopoietic stem cells by restricting their differentiation. Genes Dev. 29, 1915–1929 (2015).
pubmed: 26385962
pmcid: 4579349
doi: 10.1101/gad.268409.115
Pimkin, M. et al. Divergent functions of hematopoietic transcription factors in lineage priming and differentiation during erythro-megakaryopoiesis. Genome Res. 24, 1932–1944 (2014).
pubmed: 25319996
pmcid: 4248311
doi: 10.1101/gr.164178.113
Holtzman, D. M., Herz, J. & Bu, G. Apolipoprotein E and apolipoprotein E receptors: normal biology and roles in Alzheimer disease. Cold Spring Harb. Perspect. Med. 2, a006312 (2012).
pubmed: 22393530
pmcid: 3282491
doi: 10.1101/cshperspect.a006312
Getz, G. S., Reardon, C. A. & Apoprotein, E. Reverse cholesterol transport. Int. J. Mol. Sci. 19, 3479 (2018).
pubmed: 30404132
pmcid: 6275009
doi: 10.3390/ijms19113479
Piedrahita, J. A., Zhang, S. H., Hagaman, J. R., Oliver, P. M. & Maeda, N. Generation of mice carrying a mutant apolipoprotein E gene inactivated by gene targeting in embryonic stem cells. Proc. Natl. Acad. Sci. USA 89, 4471–4475 (1992).
pubmed: 1584779
pmcid: 49104
doi: 10.1073/pnas.89.10.4471
Seita, J. et al. Gene Expression Commons: an open platform for absolute gene expression profiling. PLoS One 7, e40321 (2012).
pubmed: 22815738
pmcid: 3399844
doi: 10.1371/journal.pone.0040321
Pradeep, S. et al. Erythropoietin stimulates tumor growth via EphB4. Cancer Cell 28, 610–622 (2015).
pubmed: 26481148
pmcid: 4643364
doi: 10.1016/j.ccell.2015.09.008
Fagundes, R. R. et al. HIF1alpha-dependent induction of Tfrc by a combination of intestinal inflammation and systemic iron deficiency in inflammatory bowel disease. Front Physiol. 13, 889091 (2022).
pubmed: 35755436
pmcid: 9214203
doi: 10.3389/fphys.2022.889091
Ozgür, B. et al. Hypoxia increases expression of selected blood-brain barrier transporters GLUT-1, P-gp, SLC7A5 and TFRC, while maintaining barrier integrity, in brain capillary endothelial monolayers. Fluids Barriers CNS 19, 1 (2022).
pubmed: 34983574
pmcid: 8725498
doi: 10.1186/s12987-021-00297-6
Perry, J. M. et al. Maintenance of the BMP4-dependent stress erythropoiesis pathway in the murine spleen requires hedgehog signaling. Blood 113, 911–918 (2009).
pubmed: 18927434
pmcid: 2630276
doi: 10.1182/blood-2008-03-147892
Mair, K. M. et al. Sex affects bone morphogenetic protein type II receptor signaling in pulmonary artery smooth muscle cells. Am. J. Respir. Crit. Care Med. 191, 693–703 (2015).
pubmed: 25608111
pmcid: 4384779
doi: 10.1164/rccm.201410-1802OC
Qian, S. et al. BMP4 cross-talks with estrogen/ERα signaling to regulate adiposity and glucose metabolism in females. EBioMedicine 11, 91–100 (2016).
pubmed: 27522322
pmcid: 5049932
doi: 10.1016/j.ebiom.2016.07.034
Gomes, A. L., Carvalho, T., Serpa, J., Torre, C. & Dias, S. Hypercholesterolemia promotes bone marrow cell mobilization by perturbing the SDF-1:CXCR4 axis. Blood 115, 3886–3894 (2010).
pubmed: 20009035
doi: 10.1182/blood-2009-08-240580
Crysandt, M. et al. Hypercholesterolemia and its association with enhanced stem cell mobilization and harvest after high-dose cyclophosphamide+G-CSF. Bone Marrow Transpl. 46, 1426–1429 (2011).
doi: 10.1038/bmt.2010.327
Westerterp, M. et al. Regulation of hematopoietic stem and progenitor cell mobilization by cholesterol efflux pathways. Cell Stem Cell 11, 195–206 (2012).
pubmed: 22862945
pmcid: 3413200
doi: 10.1016/j.stem.2012.04.024
Murphy, A. J. et al. ApoE regulates hematopoietic stem cell proliferation, monocytosis, and monocyte accumulation in atherosclerotic lesions in mice. J. Clin. Invest. 121, 4138–4149 (2011).
pubmed: 21968112
pmcid: 3195472
doi: 10.1172/JCI57559
Sánchez, Á. et al. Stress erythropoiesis in atherogenic mice. Sci. Rep. 10, 18469 (2020).
pubmed: 33116141
pmcid: 7595174
doi: 10.1038/s41598-020-74665-x
Sanjuan-Pla, A. et al. Platelet-biased stem cells reside at the apex of the haematopoietic stem-cell hierarchy. Nature 502, 232–236 (2013).
pubmed: 23934107
doi: 10.1038/nature12495
Fernandes, V., Teles, K., Ribeiro, C., Treptow, W. & Santos, G. Fat nucleosome: role of lipids on chromatin. Prog. Lipid Res. 70, 29–34 (2018).
pubmed: 29678609
doi: 10.1016/j.plipres.2018.04.003
Radulovic, V. et al. Junctional adhesion molecule 2 represents a subset of hematopoietic stem cells with enhanced potential for T lymphopoiesis. Cell Rep. 27, 2826–2836 (2019).
pubmed: 31167130
doi: 10.1016/j.celrep.2019.05.028
Basak, O. et al. Mapping early fate determination in Lgr5+ crypt stem cells using a novel Ki67-RFP allele. EMBO J. 33, 2057–2068 (2014).
pubmed: 25092767
pmcid: 4195772
doi: 10.15252/embj.201488017
Usui, S., Hara, Y., Hosaki, S. & Okazaki, M. A new on-line dual enzymatic method for simultaneous quantification of cholesterol and triglycerides in lipoproteins by HPLC. J. Lipid Res. 43, 805–814 (2002).
pubmed: 11971952
doi: 10.1016/S0022-2275(20)30123-1
Toshima, G. et al. LipoSEARCH®; Analytical GP-HPLC method for lipoprotein profiling and its applications. J. Biol. Macromol. 13, 21–32 (2013).
Usui, S. et al. Assessment of between-instrument variations in a HPLC method for serum lipoproteins and its traceability to reference methods for total cholesterol and HDL-cholesterol. Clin. Chem. 46, 63–72 (2000).
pubmed: 10620573
doi: 10.1093/clinchem/46.1.63
Pronk, C. J. H. et al. Elucidation of the phenotypic, functional, and molecular topography of a myeloerythroid progenitor cell hierarchy. Cell Stem Cell 1, 428–442 (2007).
pubmed: 18371379
doi: 10.1016/j.stem.2007.07.005