Hematopoietic Stem Cells and Their Bone Marrow Niches.

Aging Hematopoietic stem cells Leukemia Niche

Journal

Advances in experimental medicine and biology
ISSN: 0065-2598
Titre abrégé: Adv Exp Med Biol
Pays: United States
ID NLM: 0121103

Informations de publication

Date de publication:
2023
Historique:
medline: 17 1 2024
pubmed: 17 1 2024
entrez: 16 1 2024
Statut: ppublish

Résumé

Hematopoietic stem cells (HSCs) are maintained in the bone marrow microenvironment, also known as the niche, that regulates their proliferation, self-renewal, and differentiation. In this chapter, we will introduce the history of HSC niche research and review the interdependencies between HSCs and their niches. We will further highlight recent advances in our understanding of HSC heterogeneity with regard to HSC subpopulations and their interacting cellular and molecular bone marrow niche constituents.

Identifiants

DOI: 10.1007/978-981-99-7471-9_2 PMID: 38228956
pubmed: 38228956
doi: 10.1007/978-981-99-7471-9_2
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

17-28

Informations de copyright

© 2023. The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd.

Références

Agathocleous M, Meacham CE, Burgess RJ, Piskounova E, Zhao Z, Crane GM et al (2017) Ascorbate regulates haematopoietic stem cell function and leukaemogenesis. Nature 549(7673):476–481. https://doi.org/10.1038/nature23876
doi: 10.1038/nature23876 pubmed: 28825709 pmcid: 5910063
Aguayo A, Kantarjian H, Manshouri T, Gidel C, Estey E, Thomas D et al (2000) Angiogenesis in acute and chronic leukemias and myelodysplastic syndromes. Blood 96(6):2240–2245
doi: 10.1182/blood.V96.6.2240 pubmed: 10979972
Ambrosi TH, Scialdone A, Graja A, Gohlke S, Jank AM, Bocian C et al (2017) Adipocyte accumulation in the bone marrow during obesity and aging impairs stem cell-based hematopoietic and bone regeneration. Cell Stem Cell 20(6):771–784.e776. https://doi.org/10.1016/j.stem.2017.02.009
doi: 10.1016/j.stem.2017.02.009 pubmed: 28330582 pmcid: 5459794
Arranz L, Sanchez-Aguilera A, Martin-Perez D, Isern J, Langa X, Tzankov A et al (2014) Neuropathy of haematopoietic stem cell niche is essential for myeloproliferative neoplasms. Nature 512(7512):78–81. https://doi.org/10.1038/nature13383
doi: 10.1038/nature13383 pubmed: 25043017
Asada N, Kunisaki Y, Pierce H, Wang Z, Fernandez NF, Birbrair A et al (2017) Differential cytokine contributions of perivascular haematopoietic stem cell niches. Nat Cell Biol 19(3):214–223. https://doi.org/10.1038/ncb3475
doi: 10.1038/ncb3475 pubmed: 28218906 pmcid: 5467892
Baccin C, Al-Sabah J, Velten L, Helbling PM, Grünschläger F, Hernández-Malmierca P et al (2020) Combined single-cell and spatial transcriptomics reveal the molecular, cellular and spatial bone marrow niche organization. Nat Cell Biol 22(1):38–48. https://doi.org/10.1038/s41556-019-0439-6
doi: 10.1038/s41556-019-0439-6 pubmed: 31871321
Baldridge MT, King KY, Boles NC, Weksberg DC, Goodell MA (2010) Quiescent haematopoietic stem cells are activated by IFN-gamma in response to chronic infection. Nature 465(7299):793–797. https://doi.org/10.1038/nature09135
doi: 10.1038/nature09135 pubmed: 20535209 pmcid: 2935898
Baryawno N, Przybylski D, Kowalczyk MS, Kfoury Y, Severe N, Gustafsson K et al (2019) A cellular taxonomy of the bone marrow stroma in homeostasis and leukemia. Cell 177(7):1915–1932.e1916. https://doi.org/10.1016/j.cell.2019.04.040
doi: 10.1016/j.cell.2019.04.040 pubmed: 31130381 pmcid: 6570562
Benveniste P, Frelin C, Janmohamed S, Barbara M, Herrington R, Hyam D, Iscove NN (2010) Intermediate-term hematopoietic stem cells with extended but time-limited reconstitution potential. Cell Stem Cell 6(1):48–58. https://doi.org/10.1016/j.stem.2009.11.014
doi: 10.1016/j.stem.2009.11.014 pubmed: 20074534
Bianco P, Robey PG, Simmons PJ (2008) Mesenchymal stem cells: revisiting history, concepts, and assays. Cell Stem Cell 2(4):313–319. https://doi.org/10.1016/j.stem.2008.03.002
doi: 10.1016/j.stem.2008.03.002 pubmed: 18397751 pmcid: 2613570
Bogeska R, Mikecin AM, Kaschutnig P, Fawaz M, Buchler-Schaff M, Le D et al (2022) Inflammatory exposure drives long-lived impairment of hematopoietic stem cell self-renewal activity and accelerated aging. Cell Stem Cell 29(8):1273–1284.e1278. https://doi.org/10.1016/j.stem.2022.06.012
doi: 10.1016/j.stem.2022.06.012 pubmed: 35858618 pmcid: 9357150
Bowers M, Zhang B, Ho Y, Agarwal P, Chen CC, Bhatia R (2015) Osteoblast ablation reduces normal long-term hematopoietic stem cell self-renewal but accelerates leukemia development. Blood 125(17):2678–2688. https://doi.org/10.1182/blood-2014-06-582924
doi: 10.1182/blood-2014-06-582924 pubmed: 25742698 pmcid: 4408292
Boyd AL, Reid JC, Salci KR, Aslostovar L, Benoit YD, Shapovalova Z et al (2017) Acute myeloid leukaemia disrupts endogenous myelo-erythropoiesis by compromising the adipocyte bone marrow niche. Nat Cell Biol 19(11):1336–1347. https://doi.org/10.1038/ncb3625
doi: 10.1038/ncb3625 pubmed: 29035359
Bruns I, Lucas D, Pinho S, Ahmed J, Lambert MP, Kunisaki Y et al (2014) Megakaryocytes regulate hematopoietic stem cell quiescence through CXCL4 secretion. Nat Med 20(11):1315–1320. https://doi.org/10.1038/nm.3707
doi: 10.1038/nm.3707 pubmed: 25326802 pmcid: 4258871
Burt R, Dey A, Aref S, Aguiar M, Akarca A, Bailey K et al (2019) Activated stromal cells transfer mitochondria to rescue acute lymphoblastic leukemia cells from oxidative stress. Blood 134(17):1415–1429. https://doi.org/10.1182/blood.2019001398
doi: 10.1182/blood.2019001398 pubmed: 31501154 pmcid: 6856969
Cabezas-Wallscheid N, Buettner F, Sommerkamp P, Klimmeck D, Ladel L, Thalheimer FB et al (2017) Vitamin A-retinoic acid signaling regulates hematopoietic stem cell dormancy. Cell 169(5):807–823.e819. https://doi.org/10.1016/j.cell.2017.04.018
doi: 10.1016/j.cell.2017.04.018 pubmed: 28479188
Calvi LM, Adams GB, Weibrecht KW, Weber JM, Olson DP, Knight MC et al (2003) Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 425(6960):841–846. https://doi.org/10.1038/nature02040
doi: 10.1038/nature02040 pubmed: 14574413
Chambers SM, Shaw CA, Gatza C, Fisk CJ, Donehower LA, Goodell MA (2007) Aging hematopoietic stem cells decline in function and exhibit epigenetic dysregulation. PLoS Biol 5(8):e201. https://doi.org/10.1371/journal.pbio.0050201
doi: 10.1371/journal.pbio.0050201 pubmed: 17676974 pmcid: 1925137
Chanda B, Ditadi A, Iscove NN, Keller G (2013) Retinoic acid signaling is essential for embryonic hematopoietic stem cell development. Cell 155(1):215–227. https://doi.org/10.1016/j.cell.2013.08.055
doi: 10.1016/j.cell.2013.08.055 pubmed: 24074870
Colmone A, Amorim M, Pontier AL, Wang S, Jablonski E, Sipkins DA (2008) Leukemic cells create bone marrow niches that disrupt the behavior of normal hematopoietic progenitor cells. Science 322(5909):1861–1865. https://doi.org/10.1126/science.1164390
doi: 10.1126/science.1164390 pubmed: 19095944
Decker M, Leslie J, Liu Q, Ding L (2018) Hepatic thrombopoietin is required for bone marrow hematopoietic stem cell maintenance. Science 360(6384):106–110. https://doi.org/10.1126/science.aap8861
doi: 10.1126/science.aap8861 pubmed: 29622652 pmcid: 5930357
Ding L, Morrison SJ (2013) Haematopoietic stem cells and early lymphoid progenitors occupy distinct bone marrow niches. Nature 495(7440):231–235. https://doi.org/10.1038/nature11885
doi: 10.1038/nature11885 pubmed: 23434755 pmcid: 3600153
Ding L, Saunders TL, Enikolopov G, Morrison SJ (2012) Endothelial and perivascular cells maintain haematopoietic stem cells. Nature 481(7382):457–462. https://doi.org/10.1038/nature10783
doi: 10.1038/nature10783 pubmed: 22281595 pmcid: 3270376
Dong L, Yu WM, Zheng H, Loh ML, Bunting ST, Pauly M et al (2016) Leukaemogenic effects of Ptpn11 activating mutations in the stem cell microenvironment. Nature 539(7628):304–308. https://doi.org/10.1038/nature20131
doi: 10.1038/nature20131 pubmed: 27783593 pmcid: 5317374
Duan CW, Shi J, Chen J, Wang B, Yu YH, Qin X et al (2014) Leukemia propagating cells rebuild an evolving niche in response to therapy. Cancer Cell 25(6):778–793. https://doi.org/10.1016/j.ccr.2014.04.015
doi: 10.1016/j.ccr.2014.04.015 pubmed: 24937459
Duarte D, Hawkins ED, Akinduro O, Ang H, De Filippo K, Kong IY et al (2018) Inhibition of endosteal vascular niche remodeling rescues hematopoietic stem cell loss in AML. Cell Stem Cell 22(1):64–77.e66. https://doi.org/10.1016/j.stem.2017.11.006
doi: 10.1016/j.stem.2017.11.006 pubmed: 29276143 pmcid: 5766835
Dykstra B, Kent D, Bowie M, McCaffrey L, Hamilton M, Lyons K et al (2007) Long-term propagation of distinct hematopoietic differentiation programs in vivo. Cell Stem Cell 1(2):218–229. https://doi.org/10.1016/j.stem.2007.05.015
doi: 10.1016/j.stem.2007.05.015 pubmed: 18371352
Eaves CJ (2015) Hematopoietic stem cells: concepts, definitions, and the new reality. Blood 125(17):2605–2613. https://doi.org/10.1182/blood-2014-12-570200
doi: 10.1182/blood-2014-12-570200 pubmed: 25762175 pmcid: 4440889
Ergen AV, Boles NC, Goodell MA (2012) Rantes/Ccl5 influences hematopoietic stem cell subtypes and causes myeloid skewing. Blood 119(11):2500–2509. https://doi.org/10.1182/blood-2011-11-391730
doi: 10.1182/blood-2011-11-391730 pubmed: 22289892 pmcid: 3311273
Essers MA, Offner S, Blanco-Bose WE, Waibler Z, Kalinke U, Duchosal MA, Trumpp A (2009) IFNalpha activates dormant haematopoietic stem cells in vivo. Nature 458(7240):904–908. https://doi.org/10.1038/nature07815
doi: 10.1038/nature07815 pubmed: 19212321
Fiedler W, Graeven U, Ergün S, Verago S, Kilic N, Stockschläder M, Hossfeld DK (1997) Vascular endothelial growth factor, a possible paracrine growth factor in human acute myeloid leukemia. Blood 89(6):1870–1875
doi: 10.1182/blood.V89.6.1870 pubmed: 9058706
Flach J, Bakker ST, Mohrin M, Conroy PC, Pietras EM, Reynaud D et al (2014) Replication stress is a potent driver of functional decline in ageing haematopoietic stem cells. Nature 512(7513):198–202. https://doi.org/10.1038/nature13619
doi: 10.1038/nature13619 pubmed: 25079315 pmcid: 4456040
Florian MC, Nattamai KJ, Dorr K, Marka G, Uberle B, Vas V et al (2013) A canonical to non-canonical Wnt signalling switch in haematopoietic stem-cell ageing. Nature 503(7476):392–396. https://doi.org/10.1038/nature12631
doi: 10.1038/nature12631 pubmed: 24141946 pmcid: 4078992
Forte D, García-Fernández M, Sánchez-Aguilera A, Stavropoulou V, Fielding C, Martín-Pérez D et al (2020) Bone marrow mesenchymal stem cells support acute myeloid leukemia bioenergetics and enhance antioxidant defense and escape from chemotherapy. Cell Metab 32(5):829–843.e829. https://doi.org/10.1016/j.cmet.2020.09.001
doi: 10.1016/j.cmet.2020.09.001 pubmed: 32966766 pmcid: 7658808
Frenette PS, Pinho S, Lucas D, Scheiermann C (2013) Mesenchymal stem cell: keystone of the hematopoietic stem cell niche and a stepping-stone for regenerative medicine. Annu Rev Immunol 31:285–316. https://doi.org/10.1146/annurev-immunol-032712-095919
doi: 10.1146/annurev-immunol-032712-095919 pubmed: 23298209
Gao X, Zhang D, Xu C, Li H, Caron KM, Frenette PS (2021) Nociceptive nerves regulate haematopoietic stem cell mobilization. Nature 589(7843):591–596. https://doi.org/10.1038/s41586-020-03057-y
doi: 10.1038/s41586-020-03057-y pubmed: 33361809
Gekas C, Graf T (2013) CD41 expression marks myeloid-biased adult hematopoietic stem cells and increases with age. Blood 121(22):4463–4472. https://doi.org/10.1182/blood-2012-09-457929
doi: 10.1182/blood-2012-09-457929 pubmed: 23564910
Goncalves KA, Silberstein L, Li S, Severe N, Hu MG, Yang H et al (2016) Angiogenin promotes hematopoietic regeneration by dichotomously regulating quiescence of stem and progenitor cells. Cell 166(4):894–906. https://doi.org/10.1016/j.cell.2016.06.042
doi: 10.1016/j.cell.2016.06.042 pubmed: 27518564 pmcid: 4988404
Greenbaum A, Hsu YM, Day RB, Schuettpelz LG, Christopher MJ, Borgerding JN et al (2013) CXCL12 in early mesenchymal progenitors is required for haematopoietic stem-cell maintenance. Nature 495(7440):227–230. https://doi.org/10.1038/nature11926
doi: 10.1038/nature11926 pubmed: 23434756 pmcid: 3600148
Gu H, Chen C, Hao X, Wang C, Zhang X, Li Z et al (2016) Sorting protein VPS33B regulates exosomal autocrine signaling to mediate hematopoiesis and leukemogenesis. J Clin Invest 126(12):4537–4553. https://doi.org/10.1172/jci87105
doi: 10.1172/jci87105 pubmed: 27797340 pmcid: 5127665
Hanoun M, Zhang D, Mizoguchi T, Pinho S, Pierce H, Kunisaki Y et al (2014) Acute myelogenous leukemia-induced sympathetic neuropathy promotes malignancy in an altered hematopoietic stem cell niche. Cell Stem Cell 15(3):365–375. https://doi.org/10.1016/j.stem.2014.06.020
doi: 10.1016/j.stem.2014.06.020 pubmed: 25017722 pmcid: 4156919
Hao X, Gu H, Chen C, Huang D, Zhao Y, Xie L et al (2019) Metabolic imaging reveals a unique preference of symmetric cell division and homing of leukemia-initiating cells in an endosteal niche. Cell Metab 29(4):950–965.e956. https://doi.org/10.1016/j.cmet.2018.11.013
doi: 10.1016/j.cmet.2018.11.013 pubmed: 30581117
Hawkins ED, Duarte D, Akinduro O, Khorshed RA, Passaro D, Nowicka M et al (2016) T-cell acute leukaemia exhibits dynamic interactions with bone marrow microenvironments. Nature 538(7626):518–522. https://doi.org/10.1038/nature19801
doi: 10.1038/nature19801 pubmed: 27750279 pmcid: 5164929
He X, Wan J, Yang X, Zhang X, Huang D, Li X et al (2021) Bone marrow niche ATP levels determine leukemia-initiating cell activity via P2X7 in leukemic models. J Clin Invest 131(4):e140242. https://doi.org/10.1172/jci140242
doi: 10.1172/jci140242 pubmed: 33301426 pmcid: 7880412
Himburg HA, Termini CM, Schlussel L, Kan J, Li M, Zhao L et al (2018) Distinct bone marrow sources of pleiotrophin control hematopoietic stem cell maintenance and regeneration. Cell Stem Cell 23(3):370–381.e375. https://doi.org/10.1016/j.stem.2018.07.003
doi: 10.1016/j.stem.2018.07.003 pubmed: 30100167 pmcid: 6482945
Ho TT, Warr MR, Adelman ER, Lansinger OM, Flach J, Verovskaya EV et al (2017) Autophagy maintains the metabolism and function of young and old stem cells. Nature 543(7644):205–210. https://doi.org/10.1038/nature21388
doi: 10.1038/nature21388 pubmed: 28241143 pmcid: 5344718
Ho YH, Del Toro R, Rivera-Torres J, Rak J, Korn C, García-García A et al (2019) Remodeling of bone marrow hematopoietic stem cell niches promotes myeloid cell expansion during premature or physiological aging. Cell Stem Cell 25(3):407–418.e406. https://doi.org/10.1016/j.stem.2019.06.007
doi: 10.1016/j.stem.2019.06.007 pubmed: 31303548 pmcid: 6739444
Hoggatt J, Mohammad KS, Singh P, Hoggatt AF, Chitteti BR, Speth JM et al (2013) Differential stem- and progenitor-cell trafficking by prostaglandin E2. Nature 495(7441):365–369. https://doi.org/10.1038/nature11929
doi: 10.1038/nature11929 pubmed: 23485965 pmcid: 3606692
Hooper AT, Butler JM, Nolan DJ, Kranz A, Iida K, Kobayashi M et al (2009) Engraftment and reconstitution of hematopoiesis is dependent on VEGFR2-mediated regeneration of sinusoidal endothelial cells. Cell Stem Cell 4(3):263–274. https://doi.org/10.1016/j.stem.2009.01.006
doi: 10.1016/j.stem.2009.01.006 pubmed: 19265665 pmcid: 3228275
Huang D, Sun G, Hao X, He X, Zheng Z, Chen C et al (2021) ANGPTL2-containing small extracellular vesicles from vascular endothelial cells accelerate leukemia progression. J Clin Invest 131(1):e138986. https://doi.org/10.1172/jci138986
doi: 10.1172/jci138986 pubmed: 33108353 pmcid: 7773400
Hussong JW, Rodgers GM, Shami PJ (2000) Evidence of increased angiogenesis in patients with acute myeloid leukemia. Blood 95(1):309–313
doi: 10.1182/blood.V95.1.309 pubmed: 10607717
Itkin T, Ludin A, Gradus B, Gur-Cohen S, Kalinkovich A, Schajnovitz A et al (2012) FGF-2 expands murine hematopoietic stem and progenitor cells via proliferation of stromal cells, c-kit activation, and CXCL12 down-regulation. Blood 120(9):1843–1855. https://doi.org/10.1182/blood-2011-11-394692
doi: 10.1182/blood-2011-11-394692 pubmed: 22645180
Itkin T, Gur-Cohen S, Spencer JA, Schajnovitz A, Ramasamy SK, Kusumbe AP et al (2016) Distinct bone marrow blood vessels differentially regulate haematopoiesis. Nature 532(7599):323–328. https://doi.org/10.1038/nature17624
doi: 10.1038/nature17624 pubmed: 27074509 pmcid: 6450701
Jones CL, Stevens BM, D’Alessandro A, Reisz JA, Culp-Hill R, Nemkov T et al (2018) Inhibition of amino acid metabolism selectively targets human leukemia stem cells. Cancer Cell 34(5):724–740.e724. https://doi.org/10.1016/j.ccell.2018.10.005
doi: 10.1016/j.ccell.2018.10.005 pubmed: 30423294 pmcid: 6280965
Jones CL, Inguva A, Jordan CT (2021) Targeting energy metabolism in cancer stem cells: progress and challenges in leukemia and solid tumors. Cell Stem Cell 28(3):378–393. https://doi.org/10.1016/j.stem.2021.02.013
doi: 10.1016/j.stem.2021.02.013 pubmed: 33667359 pmcid: 7951949
Ju Z, Jiang H, Jaworski M, Rathinam C, Gompf A, Klein C et al (2007) Telomere dysfunction induces environmental alterations limiting hematopoietic stem cell function and engraftment. Nat Med 13(6):742–747. https://doi.org/10.1038/nm1578
doi: 10.1038/nm1578 pubmed: 17486088
Katayama Y, Battista M, Kao WM, Hidalgo A, Peired AJ, Thomas SA, Frenette PS (2006) Signals from the sympathetic nervous system regulate hematopoietic stem cell egress from bone marrow. Cell 124(2):407–421. https://doi.org/10.1016/j.cell.2005.10.041
doi: 10.1016/j.cell.2005.10.041 pubmed: 16439213
Kfoury YS, Ji F, Mazzola M, Sykes DB, Scherer AK, Anselmo A et al (2021) tiRNA signaling via stress-regulated vesicle transfer in the hematopoietic niche. Cell Stem Cell 28(12):2090–2103.e2099. https://doi.org/10.1016/j.stem.2021.08.014
doi: 10.1016/j.stem.2021.08.014 pubmed: 34551362
Kiel MJ, Yilmaz OH, Iwashita T, Terhorst C, Morrison SJ (2005) SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 121(7):1109–1121. https://doi.org/10.1016/j.cell.2005.05.026
doi: 10.1016/j.cell.2005.05.026 pubmed: 15989959
Kode A, Manavalan JS, Mosialou I, Bhagat G, Rathinam CV, Luo N et al (2014) Leukaemogenesis induced by an activating β-catenin mutation in osteoblasts. Nature 506(7487):240–244. https://doi.org/10.1038/nature12883
doi: 10.1038/nature12883 pubmed: 24429522 pmcid: 4116754
Kovtonyuk LV, Caiado F, Garcia-Martin S, Manz EM, Helbling P, Takizawa H et al (2022) IL-1 mediates microbiome-induced inflammaging of hematopoietic stem cells in mice. Blood 139(1):44–58. https://doi.org/10.1182/blood.2021011570
doi: 10.1182/blood.2021011570 pubmed: 34525198
Kunisaki Y, Bruns I, Scheiermann C, Ahmed J, Pinho S, Zhang D et al (2013) Arteriolar niches maintain haematopoietic stem cell quiescence. Nature 502(7473):637–643. https://doi.org/10.1038/nature12612
doi: 10.1038/nature12612 pubmed: 24107994 pmcid: 3821873
Kusumbe AP, Ramasamy SK, Itkin T, Mäe MA, Langen UH, Betsholtz C et al (2016) Age-dependent modulation of vascular niches for haematopoietic stem cells. Nature 532(7599):380–384. https://doi.org/10.1038/nature17638
doi: 10.1038/nature17638 pubmed: 27074508 pmcid: 5035541
Kwan W, Cortes M, Frost I, Esain V, Theodore LN, Liu SY et al (2016) The central nervous system regulates embryonic HSPC production via stress-responsive glucocorticoid receptor signaling. Cell Stem Cell 19(3):370–382. https://doi.org/10.1016/j.stem.2016.06.004
doi: 10.1016/j.stem.2016.06.004 pubmed: 27424782 pmcid: 5181112
Lagadinou ED, Sach A, Callahan K, Rossi RM, Neering SJ, Minhajuddin M et al (2013) BCL-2 inhibition targets oxidative phosphorylation and selectively eradicates quiescent human leukemia stem cells. Cell Stem Cell 12(3):329–341. https://doi.org/10.1016/j.stem.2012.12.013
doi: 10.1016/j.stem.2012.12.013 pubmed: 23333149 pmcid: 3595363
Li C, Wu B, Li Y, Chen J, Ye Z, Tian X et al (2022) Amino acid catabolism regulates hematopoietic stem cell proteostasis via a GCN2-eIF2α axis. Cell Stem Cell 29(7):1119–1134.e1117. https://doi.org/10.1016/j.stem.2022.06.004
doi: 10.1016/j.stem.2022.06.004 pubmed: 35803229
Liang Y, Van Zant G, Szilvassy SJ (2005) Effects of aging on the homing and engraftment of murine hematopoietic stem and progenitor cells. Blood 106(4):1479–1487. https://doi.org/10.1182/blood-2004-11-4282
doi: 10.1182/blood-2004-11-4282 pubmed: 15827136 pmcid: 1895199
Lou Q, Jiang K, Xu Q, Yuan L, Xie S, Pan Y et al (2022) The RIG-I-NRF2 axis regulates the mesenchymal stromal niche for bone marrow transplantation. Blood 139(21):3204–3221. https://doi.org/10.1182/blood.2021013048
doi: 10.1182/blood.2021013048 pubmed: 35259210
Lucas D, Scheiermann C, Chow A, Kunisaki Y, Bruns I, Barrick C et al (2013) Chemotherapy-induced bone marrow nerve injury impairs hematopoietic regeneration. Nat Med 19(6):695–703. https://doi.org/10.1038/nm.3155
doi: 10.1038/nm.3155 pubmed: 23644514 pmcid: 3964478
Marchand T, Pinho S (2021) Leukemic stem cells: from leukemic niche biology to treatment opportunities. Front Immunol 12:775128. https://doi.org/10.3389/fimmu.2021.775128
doi: 10.3389/fimmu.2021.775128 pubmed: 34721441 pmcid: 8554324
Maryanovich M, Zahalka AH, Pierce H, Pinho S, Nakahara F, Asada N et al (2018) Adrenergic nerve degeneration in bone marrow drives aging of the hematopoietic stem cell niche. Nat Med 24(6):782–791. https://doi.org/10.1038/s41591-018-0030-x
doi: 10.1038/s41591-018-0030-x pubmed: 29736022 pmcid: 6095812
Meacham CE, Jeffery EC, Burgess RJ, Sivakumar CD, Arora MA, Stanley AM et al (2022) Adiponectin receptors sustain haematopoietic stem cells throughout adulthood by protecting them from inflammation. Nat Cell Biol 24(5):697–707. https://doi.org/10.1038/s41556-022-00909-9
doi: 10.1038/s41556-022-00909-9 pubmed: 35513711 pmcid: 9107511
Mendez-Ferrer S, Michurina TV, Ferraro F, Mazloom AR, Macarthur BD, Lira SA et al (2010) Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 466(7308):829–834. https://doi.org/10.1038/nature09262
doi: 10.1038/nature09262 pubmed: 20703299 pmcid: 3146551
Mohrin M, Shin J, Liu Y, Brown K, Luo H, Xi Y et al (2015) Stem cell aging. A mitochondrial UPR-mediated metabolic checkpoint regulates hematopoietic stem cell aging. Science 347(6228):1374–1377. https://doi.org/10.1126/science.aaa2361
doi: 10.1126/science.aaa2361 pubmed: 25792330 pmcid: 4447312
Muller-Sieburg CE, Cho RH, Karlsson L, Huang JF, Sieburg HB (2004) Myeloid-biased hematopoietic stem cells have extensive self-renewal capacity but generate diminished lymphoid progeny with impaired IL-7 responsiveness. Blood 103(11):4111–4118. https://doi.org/10.1182/blood-2003-10-3448
doi: 10.1182/blood-2003-10-3448 pubmed: 14976059
Nakada D, Oguro H, Levi BP, Ryan N, Kitano A, Saitoh Y et al (2014) Oestrogen increases haematopoietic stem-cell self-renewal in females and during pregnancy. Nature 505(7484):555–558. https://doi.org/10.1038/nature12932
doi: 10.1038/nature12932 pubmed: 24451543 pmcid: 4015622
Nakahara F, Borger DK, Wei Q, Pinho S, Maryanovich M, Zahalka AH et al (2019) Engineering a haematopoietic stem cell niche by revitalizing mesenchymal stromal cells. Nat Cell Biol 21(5):560–567. https://doi.org/10.1038/s41556-019-0308-3
doi: 10.1038/s41556-019-0308-3 pubmed: 30988422 pmcid: 6499646
Nakamura-Ishizu A, Takubo K, Fujioka M, Suda T (2014) Megakaryocytes are essential for HSC quiescence through the production of thrombopoietin. Biochem Biophys Res Commun 454(2):353–357. https://doi.org/10.1016/j.bbrc.2014.10.095
doi: 10.1016/j.bbrc.2014.10.095 pubmed: 25451253
Nishikawa K, Nakashima T, Takeda S, Isogai M, Hamada M, Kimura A et al (2010) Maf promotes osteoblast differentiation in mice by mediating the age-related switch in mesenchymal cell differentiation. J Clin Invest 120(10):3455–3465. https://doi.org/10.1172/JCI42528
doi: 10.1172/JCI42528 pubmed: 20877012 pmcid: 2947225
Nombela-Arrieta C, Pivarnik G, Winkel B, Canty KJ, Harley B, Mahoney JE et al (2013) Quantitative imaging of haematopoietic stem and progenitor cell localization and hypoxic status in the bone marrow microenvironment. Nat Cell Biol 15(5):533–543. https://doi.org/10.1038/ncb2730
doi: 10.1038/ncb2730 pubmed: 23624405 pmcid: 4156024
Oburoglu L, Tardito S, Fritz V, de Barros SC, Merida P, Craveiro M et al (2014) Glucose and glutamine metabolism regulate human hematopoietic stem cell lineage specification. Cell Stem Cell 15(2):169–184. https://doi.org/10.1016/j.stem.2014.06.002
doi: 10.1016/j.stem.2014.06.002 pubmed: 24953180
Ossenkoppele GJ, Stussi G, Maertens J, van Montfort K, Biemond BJ, Breems D et al (2012) Addition of bevacizumab to chemotherapy in acute myeloid leukemia at older age: a randomized phase 2 trial of the Dutch-Belgian Cooperative Trial Group for Hemato-Oncology (HOVON) and the Swiss Group for Clinical Cancer Research (SAKK). Blood 120(24):4706–4711. https://doi.org/10.1182/blood-2012-04-420596
doi: 10.1182/blood-2012-04-420596 pubmed: 23047822
Padró T, Ruiz S, Bieker R, Bürger H, Steins M, Kienast J et al (2000) Increased angiogenesis in the bone marrow of patients with acute myeloid leukemia. Blood 95(8):2637–2644
doi: 10.1182/blood.V95.8.2637 pubmed: 10753845
Pang WW, Price EA, Sahoo D, Beerman I, Maloney WJ, Rossi DJ et al (2011) Human bone marrow hematopoietic stem cells are increased in frequency and myeloid-biased with age. Proc Natl Acad Sci U S A 108(50):20012–20017. https://doi.org/10.1073/pnas.1116110108
doi: 10.1073/pnas.1116110108 pubmed: 22123971 pmcid: 3250139
Passaro D, Di Tullio A, Abarrategi A, Rouault-Pierre K, Foster K, Ariza-McNaughton L et al (2017) Increased vascular permeability in the bone marrow microenvironment contributes to disease progression and drug response in acute myeloid leukemia. Cancer Cell 32(3):324–341.e326. https://doi.org/10.1016/j.ccell.2017.08.001
doi: 10.1016/j.ccell.2017.08.001 pubmed: 28870739 pmcid: 5598545
Pierce H, Zhang D, Magnon C, Lucas D, Christin JR, Huggins M et al (2017) Cholinergic signals from the CNS regulate G-CSF-mediated HSC mobilization from bone marrow via a glucocorticoid signaling relay. Cell Stem Cell 20(5):648–658.e644. https://doi.org/10.1016/j.stem.2017.01.002
doi: 10.1016/j.stem.2017.01.002 pubmed: 28196601 pmcid: 5467872
Pinho S, Frenette PS (2019) Haematopoietic stem cell activity and interactions with the niche. Nat Rev Mol Cell Biol 20(5):303–320. https://doi.org/10.1038/s41580-019-0103-9
doi: 10.1038/s41580-019-0103-9 pubmed: 30745579 pmcid: 6483843
Pinho S, Lacombe J, Hanoun M, Mizoguchi T, Bruns I, Kunisaki Y, Frenette PS (2013) PDGFRalpha and CD51 mark human nestin+ sphere-forming mesenchymal stem cells capable of hematopoietic progenitor cell expansion. J Exp Med 210(7):1351–1367. https://doi.org/10.1084/jem.20122252
doi: 10.1084/jem.20122252 pubmed: 23776077 pmcid: 3698522
Pinho S, Marchand T, Yang E, Wei Q, Nerlov C, Frenette PS (2018) Lineage-biased hematopoietic stem cells are regulated by distinct niches. Dev Cell 44(5):634–641.e634. https://doi.org/10.1016/j.devcel.2018.01.016
doi: 10.1016/j.devcel.2018.01.016 pubmed: 29456137 pmcid: 5886750
Pioli PD, Casero D, Montecino-Rodriguez E, Morrison SL, Dorshkind K (2019) Plasma cells are obligate effectors of enhanced myelopoiesis in aging bone marrow. Immunity 51(2):351–366.e356. https://doi.org/10.1016/j.immuni.2019.06.006
doi: 10.1016/j.immuni.2019.06.006 pubmed: 31303400 pmcid: 6703913
Poulos MG, Ramalingam P, Gutkin MC, Llanos P, Gilleran K, Rabbany SY, Butler JM (2017) Endothelial transplantation rejuvenates aged hematopoietic stem cell function. J Clin Invest 127(11):4163–4178. https://doi.org/10.1172/jci93940
doi: 10.1172/jci93940 pubmed: 29035282 pmcid: 5663355
Qi L, Martin-Sandoval MS, Merchant S, Gu W, Eckhardt M, Mathews TP et al (2021) Aspartate availability limits hematopoietic stem cell function during hematopoietic regeneration. Cell Stem Cell 28(11):1982–1999.e1988. https://doi.org/10.1016/j.stem.2021.07.011
doi: 10.1016/j.stem.2021.07.011 pubmed: 34450065 pmcid: 8571029
Raaijmakers MH, Mukherjee S, Guo S, Zhang S, Kobayashi T, Schoonmaker JA et al (2010) Bone progenitor dysfunction induces myelodysplasia and secondary leukaemia. Nature 464(7290):852–857. https://doi.org/10.1038/nature08851
doi: 10.1038/nature08851 pubmed: 20305640 pmcid: 3422863
Ranganath SH, Levy O, Inamdar MS, Karp JM (2012) Harnessing the mesenchymal stem cell secretome for the treatment of cardiovascular disease. Cell Stem Cell 10(3):244–258. https://doi.org/10.1016/j.stem.2012.02.005
doi: 10.1016/j.stem.2012.02.005 pubmed: 22385653 pmcid: 3294273
Rossi DJ, Bryder D, Zahn JM, Ahlenius H, Sonu R, Wagers AJ, Weissman IL (2005) Cell intrinsic alterations underlie hematopoietic stem cell aging. Proc Natl Acad Sci U S A 102(26):9194–9199. https://doi.org/10.1073/pnas.0503280102
doi: 10.1073/pnas.0503280102 pubmed: 15967997 pmcid: 1153718
Rossi DJ, Bryder D, Seita J, Nussenzweig A, Hoeijmakers J, Weissman IL (2007) Deficiencies in DNA damage repair limit the function of haematopoietic stem cells with age. Nature 447(7145):725–729. https://doi.org/10.1038/nature05862
doi: 10.1038/nature05862 pubmed: 17554309
Sacma M, Pospiech J, Bogeska R, de Back W, Mallm JP, Sakk V et al (2019) Haematopoietic stem cells in perisinusoidal niches are protected from ageing. Nat Cell Biol 21(11):1309–1320. https://doi.org/10.1038/s41556-019-0418-y
doi: 10.1038/s41556-019-0418-y pubmed: 31685996
Saito Y, Chapple RH, Lin A, Kitano A, Nakada D (2015) AMPK protects leukemia-initiating cells in myeloid leukemias from metabolic stress in the bone marrow. Cell Stem Cell 17(5):585–596. https://doi.org/10.1016/j.stem.2015.08.019
doi: 10.1016/j.stem.2015.08.019 pubmed: 26440282 pmcid: 4597792
Sánchez-Aguilera A, Arranz L, Martín-Pérez D, García-García A, Stavropoulou V, Kubovcakova L et al (2014) Estrogen signaling selectively induces apoptosis of hematopoietic progenitors and myeloid neoplasms without harming steady-state hematopoiesis. Cell Stem Cell 15(6):791–804. https://doi.org/10.1016/j.stem.2014.11.002
doi: 10.1016/j.stem.2014.11.002 pubmed: 25479752
Sanjuan-Pla A, Macaulay IC, Jensen CT, Woll PS, Luis TC, Mead A et al (2013) Platelet-biased stem cells reside at the apex of the haematopoietic stem-cell hierarchy. Nature 502(7470):232–236. https://doi.org/10.1038/nature12495
doi: 10.1038/nature12495 pubmed: 23934107
Schofield R (1978) The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells 4(1–2):7–25
pubmed: 747780
Severe N, Karabacak NM, Gustafsson K, Baryawno N, Courties G, Kfoury Y et al (2019) Stress-induced changes in bone marrow stromal cell populations revealed through single-cell protein expression mapping. Cell Stem Cell 25(4):570–583.e577. https://doi.org/10.1016/j.stem.2019.06.003
doi: 10.1016/j.stem.2019.06.003 pubmed: 31279774 pmcid: 6778015
Shen B, Tasdogan A, Ubellacker JM, Zhang J, Nosyreva ED, Du L et al (2021) A mechanosensitive peri-arteriolar niche for osteogenesis and lymphopoiesis. Nature 591(7850):438–444. https://doi.org/10.1038/s41586-021-03298-5
doi: 10.1038/s41586-021-03298-5 pubmed: 33627868 pmcid: 7979521
Shin JY, Hu W, Naramura M, Park CY (2014) High c-Kit expression identifies hematopoietic stem cells with impaired self-renewal and megakaryocytic bias. J Exp Med 211(2):217–231. https://doi.org/10.1084/jem.20131128
doi: 10.1084/jem.20131128 pubmed: 24446491 pmcid: 3920569
Sigurdsson V, Takei H, Soboleva S, Radulovic V, Galeev R, Siva K et al (2016) Bile acids protect expanding hematopoietic stem cells from unfolded protein stress in fetal liver. Cell Stem Cell 18(4):522–532. https://doi.org/10.1016/j.stem.2016.01.002
doi: 10.1016/j.stem.2016.01.002 pubmed: 26831518
Stevens BM, Jones CL, Pollyea DA, Culp-Hill R, D’Alessandro A, Winters A et al (2020) Fatty acid metabolism underlies venetoclax resistance in acute myeloid leukemia stem cells. Nat Cancer 1(12):1176–1187. https://doi.org/10.1038/s43018-020-00126-z
doi: 10.1038/s43018-020-00126-z pubmed: 33884374 pmcid: 8054994
Stier S, Ko Y, Forkert R, Lutz C, Neuhaus T, Grünewald E et al (2005) Osteopontin is a hematopoietic stem cell niche component that negatively regulates stem cell pool size. J Exp Med 201(11):1781–1791. https://doi.org/10.1084/jem.20041992
doi: 10.1084/jem.20041992 pubmed: 15928197 pmcid: 2213260
Stik G, Crequit S, Petit L, Durant J, Charbord P, Jaffredo T, Durand C (2017) Extracellular vesicles of stromal origin target and support hematopoietic stem and progenitor cells. J Cell Biol 216(7):2217–2230. https://doi.org/10.1083/jcb.201601109
doi: 10.1083/jcb.201601109 pubmed: 28630143 pmcid: 5496607
Stoddart A, Wang J, Hu C, Fernald AA, Davis EM, Cheng JX, Le Beau MM (2017) Inhibition of WNT signaling in the bone marrow niche prevents the development of MDS in the Apc(del/+) MDS mouse model. Blood 129(22):2959–2970. https://doi.org/10.1182/blood-2016-08-736454
doi: 10.1182/blood-2016-08-736454 pubmed: 28348148 pmcid: 5454335
Straussman R, Morikawa T, Shee K, Barzily-Rokni M, Qian ZR, Du J et al (2012) Tumour micro-environment elicits innate resistance to RAF inhibitors through HGF secretion. Nature 487(7408):500–504. https://doi.org/10.1038/nature11183
doi: 10.1038/nature11183 pubmed: 22763439 pmcid: 3711467
Sugimura R, He XC, Venkatraman A, Arai F, Box A, Semerad C et al (2012) Noncanonical Wnt signaling maintains hematopoietic stem cells in the niche. Cell 150(2):351–365. https://doi.org/10.1016/j.cell.2012.05.041
doi: 10.1016/j.cell.2012.05.041 pubmed: 22817897 pmcid: 4492542
Sugiyama T, Kohara H, Noda M, Nagasawa T (2006) Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity 25(6):977–988. https://doi.org/10.1016/j.immuni.2006.10.016
doi: 10.1016/j.immuni.2006.10.016 pubmed: 17174120
Taya Y, Ota Y, Wilkinson AC, Kanazawa A, Watarai H, Kasai M et al (2016) Depleting dietary valine permits nonmyeloablative mouse hematopoietic stem cell transplantation. Science 354(6316):1152–1155. https://doi.org/10.1126/science.aag3145
doi: 10.1126/science.aag3145 pubmed: 27934766
Tikhonova AN, Dolgalev I, Hu H, Sivaraj KK, Hoxha E, Cuesta-Dominguez A et al (2019) The bone marrow microenvironment at single-cell resolution. Nature 569(7755):222–228. https://doi.org/10.1038/s41586-019-1104-8
doi: 10.1038/s41586-019-1104-8 pubmed: 30971824 pmcid: 6607432
Velardi E, Tsai JJ, Radtke S, Cooper K, Argyropoulos KV, Jae-Hung S et al (2018) Suppression of luteinizing hormone enhances HSC recovery after hematopoietic injury. Nat Med 24(2):239–246. https://doi.org/10.1038/nm.4470
doi: 10.1038/nm.4470 pubmed: 29309056 pmcid: 5803436
Wilson A, Laurenti E, Oser G, van der Wath RC, Blanco-Bose W, Jaworski M et al (2008) Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell 135(6):1118–1129. https://doi.org/10.1016/j.cell.2008.10.048
doi: 10.1016/j.cell.2008.10.048 pubmed: 19062086
Wilson TR, Fridlyand J, Yan Y, Penuel E, Burton L, Chan E et al (2012) Widespread potential for growth-factor-driven resistance to anticancer kinase inhibitors. Nature 487(7408):505–509. https://doi.org/10.1038/nature11249
doi: 10.1038/nature11249 pubmed: 22763448 pmcid: 3724525
Xie T, Spradling AC (2000) A niche maintaining germ line stem cells in the Drosophila ovary. Science 290(5490):328–330. https://doi.org/10.1126/science.290.5490.328
doi: 10.1126/science.290.5490.328 pubmed: 11030649
Xu C, Gao X, Wei Q, Nakahara F, Zimmerman SE, Mar J, Frenette PS (2018) Stem cell factor is selectively secreted by arterial endothelial cells in bone marrow. Nat Commun 9(1):2449. https://doi.org/10.1038/s41467-018-04726-3
doi: 10.1038/s41467-018-04726-3 pubmed: 29934585 pmcid: 6015052
Yamamoto R, Morita Y, Ooehara J, Hamanaka S, Onodera M, Rudolph KL et al (2013) Clonal analysis unveils self-renewing lineage-restricted progenitors generated directly from hematopoietic stem cells. Cell 154(5):1112–1126. https://doi.org/10.1016/j.cell.2013.08.007
doi: 10.1016/j.cell.2013.08.007 pubmed: 23993099
Yamashita M, Passegué E (2019) TNF-α coordinates hematopoietic stem cell survival and myeloid regeneration. Cell Stem Cell 25(3):357–372.e357. https://doi.org/10.1016/j.stem.2019.05.019
doi: 10.1016/j.stem.2019.05.019 pubmed: 31230859 pmcid: 6733032
Yamazaki S, Ema H, Karlsson G, Yamaguchi T, Miyoshi H, Shioda S et al (2011) Nonmyelinating Schwann cells maintain hematopoietic stem cell hibernation in the bone marrow niche. Cell 147(5):1146–1158. https://doi.org/10.1016/j.cell.2011.09.053
doi: 10.1016/j.cell.2011.09.053 pubmed: 22118468
Young K, Eudy E, Bell R, Loberg MA, Stearns T, Sharma D et al (2021) Decline in IGF1 in the bone marrow microenvironment initiates hematopoietic stem cell aging. Cell Stem Cell 28(8):1473–1482.e1477. https://doi.org/10.1016/j.stem.2021.03.017
doi: 10.1016/j.stem.2021.03.017 pubmed: 33848471 pmcid: 8349778
Yu Z, Yang W, He X, Chen C, Li W, Zhao L et al (2022) Endothelial cell-derived angiopoietin-like protein 2 supports hematopoietic stem cell activities in bone marrow niches. Blood 139(10):1529–1540. https://doi.org/10.1182/blood.2021011644
doi: 10.1182/blood.2021011644 pubmed: 34929029 pmcid: 9015010
Zahiragic L, Schliemann C, Bieker R, Thoennissen NH, Burow K, Kramer C et al (2007) Bevacizumab reduces VEGF expression in patients with relapsed and refractory acute myeloid leukemia without clinical antileukemic activity. Leukemia 21(6):1310–1312. https://doi.org/10.1038/sj.leu.2404632
doi: 10.1038/sj.leu.2404632 pubmed: 17330095
Zhang J, Niu C, Ye L, Huang H, He X, Tong WG et al (2003) Identification of the haematopoietic stem cell niche and control of the niche size. Nature 425(6960):836–841. https://doi.org/10.1038/nature02041
doi: 10.1038/nature02041 pubmed: 14574412
Zhang B, Nguyen LXT, Li L, Zhao D, Kumar B, Wu H et al (2018) Bone marrow niche trafficking of miR-126 controls the self-renewal of leukemia stem cells in chronic myelogenous leukemia. Nat Med 24(4):450–462. https://doi.org/10.1038/nm.4499
doi: 10.1038/nm.4499 pubmed: 29505034 pmcid: 5965294
Zhang J, Wu Q, Johnson CB, Pham G, Kinder JM, Olsson A et al (2021) In situ mapping identifies distinct vascular niches for myelopoiesis. Nature 590(7846):457–462. https://doi.org/10.1038/s41586-021-03201-2
doi: 10.1038/s41586-021-03201-2 pubmed: 33568812 pmcid: 8020897
Zhang D, Gao X, Li H, Borger DK, Wei Q, Yang E et al (2022) The microbiota regulates hematopoietic stem cell fate decisions by controlling iron availability in bone marrow. Cell Stem Cell 29(2):232–247.e237. https://doi.org/10.1016/j.stem.2021.12.009
doi: 10.1016/j.stem.2021.12.009 pubmed: 35065706 pmcid: 8818037
Zhao M, Ross JT, Itkin T, Perry JM, Venkatraman A, Haug JS et al (2012) FGF signaling facilitates postinjury recovery of mouse hematopoietic system. Blood 120(9):1831–1842. https://doi.org/10.1182/blood-2011-11-393991
doi: 10.1182/blood-2011-11-393991 pubmed: 22802336 pmcid: 3433089
Zhao M, Perry JM, Marshall H, Venkatraman A, Qian P, He XC et al (2014) Megakaryocytes maintain homeostatic quiescence and promote post-injury regeneration of hematopoietic stem cells. Nat Med 20(11):1321–1326. https://doi.org/10.1038/nm.3706
doi: 10.1038/nm.3706 pubmed: 25326798
Zhao M, Tao F, Venkatraman A, Li Z, Smith SE, Unruh J et al (2019) N-cadherin-expressing bone and marrow stromal progenitor cells maintain reserve hematopoietic stem cells. Cell Rep 26(3):652–669.e656. https://doi.org/10.1016/j.celrep.2018.12.093
doi: 10.1016/j.celrep.2018.12.093 pubmed: 30650358 pmcid: 6890378

Auteurs

Sandra Pinho (S)

Department of Pharmacology & Regenerative Medicine, College of Medicine, University of Illinois at Chicago, Chicago, IL, USA. spinho@uic.edu.

Meng Zhao (M)

Key Laboratory of Stem Cells and Tissue Engineering (Ministry of Education), Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou, Guangdong, China. zhaom38@mail.sysu.edu.cn.

Classifications MeSH