Oncostatin M regulates hematopoietic stem cell (HSC) niches in the bone marrow to restrict HSC mobilization.
Journal
Leukemia
ISSN: 1476-5551
Titre abrégé: Leukemia
Pays: England
ID NLM: 8704895
Informations de publication
Date de publication:
02 2022
02 2022
Historique:
received:
15
02
2021
accepted:
01
09
2021
revised:
23
08
2021
pubmed:
15
9
2021
medline:
16
2
2022
entrez:
14
9
2021
Statut:
ppublish
Résumé
We show that pro-inflammatory oncostatin M (OSM) is an important regulator of hematopoietic stem cell (HSC) niches in the bone marrow (BM). Treatment of healthy humans and mice with granulocyte colony-stimulating factor (G-CSF) dramatically increases OSM release in blood and BM. Using mice null for the OSM receptor (OSMR) gene, we demonstrate that OSM provides a negative feed-back acting as a brake on HSPC mobilization in response to clinically relevant mobilizing molecules G-CSF and CXCR4 antagonist. Likewise, injection of a recombinant OSM molecular trap made of OSMR complex extracellular domains enhances HSC mobilization in poor mobilizing C57BL/6 and NOD.Cg-Prkdc
Identifiants
pubmed: 34518644
doi: 10.1038/s41375-021-01413-z
pii: 10.1038/s41375-021-01413-z
doi:
Substances chimiques
Oncostatin M
106956-32-5
Granulocyte Colony-Stimulating Factor
143011-72-7
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
333-347Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Crane GM, Jeffery E, Morrison SJ. Adult haematopoietic stem cell niches. Nat Rev Immunol. 2017;17:573–90.
pubmed: 28604734
doi: 10.1038/nri.2017.53
Spencer JA, Ferraro F, Roussakis E, Klein A, Wu J, Runnels JM, et al. Direct measurement of local oxygen concentration in the bone marrow of live animals. Nature. 2014;508:269–73.
pubmed: 24590072
pmcid: 3984353
doi: 10.1038/nature13034
Forristal CE, Nowlan B, Jacobsen RN, Barbier V, Walkinshaw G, Walkley CR, et al. HIF-1α is required for hematopoietic stem cell mobilization and 4-prolyl hydroxylase inhibitors enhance mobilization by stabilizing HIF-1α. Leukemia. 2015;29:1366–78.
pubmed: 25578474
pmcid: 4498452
doi: 10.1038/leu.2015.8
Ding L, Saunders TL, Enikolopov G, Morrison SJ. Endothelial and perivascular cells maintain haematopoietic stem cells. Nature. 2012;481:457–62.
pubmed: 22281595
pmcid: 3270376
doi: 10.1038/nature10783
Ding L, Morrison SJ. Haematopoietic stem cells and early lymphoid progenitors occupy distinct bone marrow niches. Nature. 2013;495:231–5.
pubmed: 23434755
pmcid: 3600153
doi: 10.1038/nature11885
Greenbaum A, Hsu Y-MS, Day RB, Schuettpelz LG, Christopher MJ, Borgerding JN, et al. CXCL12 in early mesenchymal progenitors is required for haematopoietic stem-cell maintenance. Nature. 2013;495:227–30.
pubmed: 23434756
pmcid: 3600148
doi: 10.1038/nature11926
Hatzfeld J, Li ML, Brown EL, Sookdeo H, Levesque JP, O’Toole T, et al. Release of early human hematopoietic progenitors from quiescence by antisense transforming growth factor beta 1 or Rb oligonucleotides. J Exp Med. 1991;174:925–9.
pubmed: 1717634
doi: 10.1084/jem.174.4.925
Zhao M, Perry JM, Marshall H, Venkatraman A, Qian P, He XC, et al. Megakaryocytes maintain homeostatic quiescence and promote post-injury regeneration of hematopoietic stem cells. Nat Med. 2014;20:1321–6.
pubmed: 25326798
doi: 10.1038/nm.3706
Winkler IG, Barbier V, Nowlan B, Jacobsen RN, Forristal CE, Patton JT, et al. Vascular niche E-selectin regulates hematopoietic stem cell dormancy, self renewal and chemoresistance. Nat Med. 2012;18:1651–7.
pubmed: 23086476
doi: 10.1038/nm.2969
Ulyanova T, Scott LM, Priestley GV, Jiang Y, Nakamoto B, Koni PA, et al. VCAM-1 expression in adult hematopoietic and nonhematopoietic cells is controlled by tissue-inductive signals and reflects their developmental origin. Blood. 2005;106:86–94.
pubmed: 15769895
pmcid: 1895134
doi: 10.1182/blood-2004-09-3417
Yao L, Setiadi H, Xia L, Laszik Z, Taylor FB, McEver RP. Divergent inducible expression of P-selectin and E-selectin in mice and primates. Blood. 1999;94:3820–8.
pubmed: 10572097
doi: 10.1182/blood.V94.11.3820
Tanaka M, Hirabayashi Y, Sekiguchi T, Inoue T, Katsuki M, Miyajima A. Targeted disruption of oncostatin M receptor results in altered hematopoiesis. Blood. 2003;102:3154–62.
pubmed: 12855584
doi: 10.1182/blood-2003-02-0367
Minehata K, Takeuchi M, Hirabayashi Y, Inoue T, Donovan PJ, Tanaka M, et al. Oncostatin M maintains the hematopoietic microenvironment and retains hematopoietic progenitors in the bone marrow. Int J Hematol. 2006;84:319–27.
pubmed: 17118758
doi: 10.1532/IJH97.06090
Walker EC, McGregor NE, Poulton IJ, Solano M, Pompolo S, Fernandes TJ, et al. Oncostatin M promotes bone formation independently of resorption when signaling through leukemia inhibitory factor receptor in mice. J Clin Invest. 2010;120:582–92.
pubmed: 20051625
pmcid: 2810087
doi: 10.1172/JCI40568
Sims NA, Quinn JM. Osteoimmunology: oncostatin M as a pleiotropic regulator of bone formation and resorption in health and disease. Bonekey Rep. 2014;3:527.
pubmed: 24876928
pmcid: 4037876
doi: 10.1038/bonekey.2014.22
Guihard P, Boutet MA, Brounais-Le Royer B, Gamblin AL, Amiaud J, Renaud A, et al. Oncostatin M, an inflammatory cytokine produced by macrophages, supports intramembranous bone healing in a mouse model of tibia injury. Am J Pathol. 2015;185:765–75.
pubmed: 25559270
doi: 10.1016/j.ajpath.2014.11.008
Torossian F, Guerton B, Anginot A, Alexander KA, Desterke C, Soave S, et al. Macrophage-derived oncostatin M contributes to human and mouse neurogenic heterotopic ossifications. JCI Insight. 2017;2:e96034.
pmcid: 5752299
doi: 10.1172/jci.insight.96034
Calvi LM, Adams GB, Weibrecht KW, Weber JM, Olson DP, Knight MC, et al. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature. 2003;425:841–6.
pubmed: 14574413
doi: 10.1038/nature02040
Kaur S, Raggatt LJ, Batoon L, Hume DA, Levesque J-P, Pettit AR. Role of bone marrow macrophages in controlling homeostasis and repair in bone and bone marrow niches. Semin Cell Dev Biol. 2017;61:12–21.
pubmed: 27521519
doi: 10.1016/j.semcdb.2016.08.009
Winkler IG, Sims NA, Pettit AR, Barbier V, Nowlan B, Helwani F, et al. Bone marrow macrophages maintain hematopoietic stem cell (HSC) niches and their depletion mobilizes HSCs. Blood. 2010;116:4815–28.
pubmed: 20713966
doi: 10.1182/blood-2009-11-253534
Levesque JP, Summers KM, Millard SM, Bisht K, Winkler IG, Pettit AR. Role of macrophages and phagocytes in orchestrating normal and pathological haematopoietic niches. Exp Hematol. 2021;100:12–31.
pubmed: 34298116
doi: 10.1016/j.exphem.2021.07.001
Modur V, Feldhaus MJ, Weyrich AS, Jicha DL, Prescott SM, Zimmerman GA, et al. Oncostatin M is a proinflammatory mediator. In vivo effects correlate with endothelial cell expression of inflammatory cytokines and adhesion molecules. J Clin Invest. 1997;100:158–68.
pubmed: 9202068
pmcid: 508176
doi: 10.1172/JCI119508
Levesque JP, Helwani FM, Winkler IG. The endosteal ‘osteoblastic’ niche and its role in hematopoietic stem cell homing and mobilization. Leukemia. 2010;24:1979–92.
pubmed: 20861913
doi: 10.1038/leu.2010.214
Tay J, Levesque J-P, Winkler IG. Cellular players of hematopoietic stem cell mobilization in the bone marrow niche. Int J Hematol. 2017;105:129–40.
pubmed: 27943116
doi: 10.1007/s12185-016-2162-4
Bendall L. Extracellular molecules in hematopoietic stem cell mobilisation. Int J Hematol. 2017;105:118–28.
pubmed: 27826715
doi: 10.1007/s12185-016-2123-y
Pelus LM, Broxmeyer HE. Peripheral blood stem cell mobilization: a look ahead. Curr Stem Cell Rep. 2018;4:273–81.
pubmed: 31131207
pmcid: 6532982
doi: 10.1007/s40778-018-0141-9
Levesque JP, Winkler IG. Mobilization of hematopoietic stem cells: state of the art. Curr Opin Organ Transpl. 2008;13:53–8.
doi: 10.1097/MOT.0b013e3282f42473
To LB, Levesque J-P, Herbert KE. How I treat patients who mobilize hematopoietic stem cells poorly. Blood. 2011;118:4530–40.
pubmed: 21832280
doi: 10.1182/blood-2011-06-318220
Seita J, Sahoo D, Rossi DJ, Bhattacharya D, Serwold T, Inlay MA, et al. Gene expression commons: An open platform for absolute gene expression profiling. PLoS ONE. 2012;7:e40321.
pubmed: 22815738
pmcid: 3399844
doi: 10.1371/journal.pone.0040321
Choi J, Baldwin TM, Wong M, Bolden JE, Fairfax KA, Lucas EC, et al. Haemopedia RNA-seq: a database of gene expression during haematopoiesis in mice and humans. Nucleic Acids Res. 2018;47:D780–D5.
pmcid: 6324085
doi: 10.1093/nar/gky1020
Levesque JP, Hendy J, Takamatsu Y, Williams B, Winkler IG, Simmons PJ. Mobilization by either cyclophosphamide or granulocyte colony-stimulating factor transforms the bone marrow into a highly proteolytic environment. Exp Hematol. 2002;30:440–9.
pubmed: 12031650
doi: 10.1016/S0301-472X(02)00788-9
Pelus LM, Bian H, King AG, Fukuda S. Neutrophil-derived MMP-9 mediates synergistic mobilization of hematopoietic stem and progenitor cells by the combination of G-CSF and the chemokines GROβ/CXCL2 and GROβT /CXCL2Δ4. Blood. 2004;103:110–9.
pubmed: 12958067
doi: 10.1182/blood-2003-04-1115
Brolund L, Küster A, Korr S, Vogt M, Müller-Newen G. A receptor fusion protein for the inhibition of murine oncostatin M. BMC Biotechnol. 2011;11:3.
pubmed: 21223559
pmcid: 3040522
doi: 10.1186/1472-6750-11-3
West NR, Hegazy AN, Owens BMJ, Bullers SJ, Linggi B, Buonocore S, et al. Oncostatin M drives intestinal inflammation and predicts response to tumor necrosis factor-neutralizing therapy in patients with inflammatory bowel disease. Nat Med. 2017;23:579–89.
pubmed: 28368383
pmcid: 5420447
doi: 10.1038/nm.4307
Reca R, Cramer D, Yan J, Laughlin MJ, Janowska-Wieczorek A, Ratajczak J, et al. A novel role of complement in mobilization: immunodeficient mice are poor granulocyte-colony stimulating factor mobilizers because they lack complement-activating immunoglobulins. Stem Cells. 2007;25:3093–100.
pubmed: 17717064
doi: 10.1634/stemcells.2007-0525
Nowlan B, Futrega K, Brunck ME, Walkinshaw G, Flippin LE, Doran MR, et al. HIF-1α-stabilizing agent FG-4497 rescues human CD34
pubmed: 28527810
doi: 10.1016/j.exphem.2017.05.004
Nowlan B, Williams ED, Doran MR, Levesque J-P. CD27, CD201, FLT3, CD48, and CD150 cell surface staining identifies long-term mouse hematopoietic stem cells in immunodeficient non-obese diabetic severe combined immune deficient-derived strains. Haematologica. 2020;105:71–82.
pubmed: 31073070
pmcid: 6939540
doi: 10.3324/haematol.2018.212910
Tikhonova AN, Dolgalev I, Hu H, Sivaraj KK, Hoxha E, Cuesta-Domínguez Á, et al. The bone marrow microenvironment at single-cell resolution. Nature. 2019;569:222–8.
pubmed: 30971824
pmcid: 6607432
doi: 10.1038/s41586-019-1104-8
Broxmeyer HE, Orschell CM, Clapp DW, Hangoc G, Cooper S, Plett PA, et al. Rapid mobilization of murine and human hematopoietic stem and progenitor cells with AMD3100, a CXCR4 antagonist. J Exp Med. 2005;201:1307–18.
pubmed: 15837815
pmcid: 2213145
doi: 10.1084/jem.20041385
Foudi A, Jarrier P, Zhang Y, Wittner M, Geay JF, Lecluse Y, et al. Reduced retention of radioprotective hematopoietic cells within the bone marrow microenvironment in CXCR4−/− chimeric mice. Blood. 2006;107:2243–51.
pubmed: 16291599
doi: 10.1182/blood-2005-02-0581
Levesque JP, Hendy J, Takamatsu Y, Simmons PJ, Bendall LJ. Disruption of the CXCR4/CXCL12 chemotactic interaction during hematopoietic stem cell mobilization induced by GCSF or cyclophosphamide. J Clin Invest. 2003;111:187–96.
pubmed: 12531874
pmcid: 151860
doi: 10.1172/JCI15994
Petit I, Szyper-Kravitz M, Nagler A, Lahav M, Peled A, Habler L, et al. G-CSF induces stem cell mobilization by decreasing bone marrow SDF-1 and up-regulating CXCR4. Nat Immunol. 2002;3:687–94.
pubmed: 12068293
doi: 10.1038/ni813
Winkler IG, Barbier V, Wadley R, Zannettino ACW, Williams S, Levesque J-P. Positioning of bone marrow hematopoietic and stromal cells relative to blood flow in vivo: serially reconstituting hematopoietic stem cells reside in distinct nonperfused niches. Blood. 2010;116:375–85.
pubmed: 20393133
doi: 10.1182/blood-2009-07-233437
Pietras EM, Reynaud D, Kang Y-A, Carlin D, Calero-Nieto Fernando J, Leavitt, et al. Functionally distinct subsets of lineage-biased multipotent progenitors control blood production in normal and regenerative conditions. Cell Stem Cell. 2015;17:35–46.
pubmed: 26095048
pmcid: 4542150
doi: 10.1016/j.stem.2015.05.003
Barbier V, Nowlan B, Levesque JP, Winkler IG. Flow cytometry analysis of cell cycling and proliferation in mouse hematopoietic stem and progenitor cells. Methods Mol Biol. 2012;844:31–43.
pubmed: 22262433
doi: 10.1007/978-1-61779-527-5_3
Sato F, Miyaoka Y, Miyajima A, Tanaka M. Oncostatin M maintains the hematopoietic microenvironment in the bone marrow by modulating adipogenesis and osteogenesis. PLoS ONE. 2014;9:e116209.
pubmed: 25551451
pmcid: 4281151
doi: 10.1371/journal.pone.0116209
Elbjeirami WM, Donnachie EM, Burns AR, Smith CW. Endothelium-derived GM-CSF influences expression of oncostatin M. Am J Physiol Cell Physiol. 2011;301:C947–C53.
pubmed: 21775705
pmcid: 3191567
doi: 10.1152/ajpcell.00205.2011
Wang J, Zheng Z, Huang B, Wu H, Zhang X, Chen Y, et al. Osteal tissue macrophages are involved in endplate osteosclerosis through the OSM-STAT3/YAP1 signaling axis in modic changes. J Immunol. 2020;205:968–80.
pubmed: 32690652
doi: 10.4049/jimmunol.1901001
Broxmeyer HE, Bruns HA, Zhang S, Cooper S, Hangoc G, McKenzie ANJ, et al. Th1 cells regulate hematopoietic progenitor cell homeostasis by production of oncostatin M. Immunity. 2002;16:815–25.
pubmed: 12121663
doi: 10.1016/S1074-7613(02)00319-9
Levesque JP, Takamatsu Y, Nilsson SK, Haylock DN, Simmons PJ. Vascular cell adhesion molecule-1 (CD106) is cleaved by neutrophil proteases in the bone marrow following hematopoietic progenitor cell mobilization by granulocyte colony-stimulating factor. Blood. 2001;98:1289–97.
pubmed: 11520773
doi: 10.1182/blood.V98.5.1289
Albiero M, Poncina N, Ciciliot S, Cappellari R, Menegazzo L, Ferraro F, et al. Bone marrow macrophages contribute to diabetic stem cell mobilopathy by producing oncostatin M. Diabetes. 2015;64:2957–68.
pubmed: 25804939
doi: 10.2337/db14-1473
Albiero M, Ciciliot S, Tedesco S, Menegazzo L, D’Anna M, Scattolini V, et al. Diabetes-associated myelopoiesis drives stem cell mobilopathy through an OSM-p66Shc signaling pathway. Diabetes. 2019;68:1303–14.
pubmed: 30936144
doi: 10.2337/db19-0080
Tanaka M, Hara T, Copeland NG, Gilbert DJ, Jenkins NA, Miyajima A. Reconstitution of the functional mouse oncostatin M (OSM) receptor: molecular cloning of the mouse OSM receptor β subunit. Blood. 1999;93:804–15.
pubmed: 9920829
doi: 10.1182/blood.V93.3.804
Winkler IG, Barbier V, Perkins AC, Magnani JL, Levesque J-P. Mobilisation of reconstituting HSC is boosted by synergy between G-CSF and E-selectin antagonist GMI-1271. Blood. 2014;124:317. (abstract)
doi: 10.1182/blood.V124.21.317.317
Zheng J, Lu Z, Kocabas F, Böttcher RT, Costell M, Kang X, et al. Profilin 1 is essential for retention and metabolism of mouse hematopoietic stem cells in bone marrow. Blood. 2014;123:992–1001.
pubmed: 24385538
pmcid: 3924932
doi: 10.1182/blood-2013-04-498469
Sugimoto M, Nakamura T, Ohtani N, Hampson L, Hampson IN, Shimamoto A, et al. Regulation of CDK4 activity by a novel CDK4-binding protein, p34SEI-1. Genes Dev. 1999;13:3027–33.
pubmed: 10580009
pmcid: 317153
doi: 10.1101/gad.13.22.3027
Ito K, Carracedo A, Weiss D, Arai F, Ala U, Avigan DE, et al. A PML-PPAR-δ pathway for fatty acid oxidation regulates hematopoietic stem cell maintenance. Nat Med. 2012;18:1350–8.
pubmed: 22902876
pmcid: 3566224
doi: 10.1038/nm.2882
Takihara Y, Nakamura-Ishizu A, Tan DQ, Fukuda M, Matsumura T, Endoh M, et al. High mitochondrial mass is associated with reconstitution capacity and quiescence of hematopoietic stem cells. Blood Adv. 2019;3:2323–7.
pubmed: 31387881
pmcid: 6692999
doi: 10.1182/bloodadvances.2019032169
Filippi M-D. HSC divisional memory: the journey of mitochondrial metabolism through HSC division. Exp Hematol. 2021;96:27–34.
pubmed: 33515636
doi: 10.1016/j.exphem.2021.01.006
Weiss MJ, Orkin SH. Transcription factor GATA-1 permits survival and maturation of erythroid precursors by preventing apoptosis. Proc Natl Acad Sci USA. 1995;92:9623–7.
pubmed: 7568185
pmcid: 40854
doi: 10.1073/pnas.92.21.9623
Perkins AC, Sharpe AH, Orkin SH. Lethal β-thalassaemia in mice lacking the erythroid CACCC-transcription factor EKLF. Nature. 1995;375:318–22.
pubmed: 7753195
doi: 10.1038/375318a0
Vyas P, Ault K, Jackson CW, Orkin SH, Shivdasani RA. Consequences of GATA-1 deficiency in megakaryocytes and platelets. Blood. 1999;93:2867–75.
pubmed: 10216081
doi: 10.1182/blood.V93.9.2867.409k24_2867_2875
Essers MAG, Offner S, Blanco-Bose WE, Waibler Z, Kalinke U, Duchosal MA, et al. IFNα activates dormant haematopoietic stem cells in vivo. Nature. 2009;458:904–8.
pubmed: 19212321
doi: 10.1038/nature07815
Baldridge MT, King KY, Boles NC, Weksberg DC, Goodell MA. Quiescent haematopoietic stem cells are activated by IFN-γ in response to chronic infection. Nature. 2010;465:793–7.
pubmed: 20535209
pmcid: 2935898
doi: 10.1038/nature09135
Pietras EM, Mirantes-Barbeito C, Fong S, Loeffler D, Kovtonyuk LV, Zhang S, et al. Chronic interleukin-1 exposure drives haematopoietic stem cells towards precocious myeloid differentiation at the expense of self-renewal. Nat Cell Biol. 2016;18:607–18.
pubmed: 27111842
pmcid: 4884136
doi: 10.1038/ncb3346
Schwaller J, Parganas E, Wang D, Cain D, Aster JC, Williams IR, et al. Stat5 is essential for the myelo- and lymphoproliferative disease induced by TEL/JAK2. Mol Cell. 2000;6:693–704.
pubmed: 11030348
doi: 10.1016/S1097-2765(00)00067-8
Müller TA, Grundler R, Istvanffy R, Rudelius M, Hennighausen L, Illert AL, et al. Lineage-specific STAT5 target gene activation in hematopoietic progenitor cells predicts the FLT3+-mediated leukemic phenotype. Leukemia. 2016;30:1725–33.
pubmed: 27046463
doi: 10.1038/leu.2016.72
Grundler R, Miething C, Thiede C, Peschel C, Duyster J. FLT3-ITD and tyrosine kinase domain mutants induce 2 distinct phenotypes in a murine bone marrow transplantation model. Blood. 2005;105:4792–9.
pubmed: 15718420
doi: 10.1182/blood-2004-11-4430