Megakaryocytes maintain homeostatic quiescence and promote post-injury regeneration of hematopoietic stem cells

Nature Medicine

Volumn 20, Issue 11, 2014, Pages 1321-1326

  Zhao, Meng ^a   Perry, John M ^a   Marshall, Heather ^a   Venkatraman, Aparna ^a,b   Qian, Pengxu ^a   He, Xi C ^a   Ahamed, Jasimuddin ^c   Li, Linheng ^a,d  

^a STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b CHRISTIAN MEDICAL COLLEGE   (India)

^c ROCKEFELLER UNIVERSITY   (United States)

^d UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR 1; FLUOROURACIL; RECOMBINANT PROTEIN; RECOMBINANT TRANSFORMING GROWTH FACTOR BETA1; SMAD2 PROTEIN; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE MARROW; CELL ACTIVATION; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL EXPANSION; CELL NUCLEUS; CELL PROLIFERATION; CELL REGENERATION; CONTROLLED STUDY; FEMALE; GENE DELETION; HEMATOPOIETIC STEM CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MEGAKARYOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RNA SEQUENCE; SIGNAL TRANSDUCTION; STEM CELL NICHE; STROMA CELL; ANIMAL; C57BL MOUSE; CELL CYCLE; CYTOLOGY; DRUG EFFECTS; HOMEOSTASIS; METABOLISM; PATHOLOGY; PHYSIOLOGICAL STRESS; REGENERATION; SEQUENCE ANALYSIS;

ANIMALS; CELL CYCLE; CELL PROLIFERATION; FIBROBLAST GROWTH FACTOR 1; FLUOROURACIL; HEMATOPOIETIC STEM CELLS; HOMEOSTASIS; MEGAKARYOCYTES; MICE, INBRED C57BL; REGENERATION; SEQUENCE ANALYSIS, RNA; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TRANSFORMING GROWTH FACTOR BETA;

EID: 84920448202     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.3706     Document Type: Article

References (40)

1. Zhang, J. et al. Identification of the haematopoietic stem cell niche and control of the niche size. Nature 425, 836–841 (2003).
2. Calvi, L.M. et al. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 425, 841–846 (2003).
3. Kiel, M.J., Yilmaz, O.H., Iwashita, T., Terhorst, C. & Morrison, S.J. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 121, 1109–1121 (2005).
4. 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).
5. Méndez-Ferrer, S. et al. Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 466, 829–834 (2010).
6. Ding, L., Saunders, T.L., Enikolopov, G. & Morrison, S.J. Endothelial and perivascular cells maintain haematopoietic stem cells. Nature 481, 457–462 (2012).
7. Kunisaki, Y. et al. Arteriolar niches maintain haematopoietic stem cell quiescence. Nature 23, 3865–3873 (2013).
8. Yamazaki, S. et al. TGF-β as a candidate bone marrow niche signal to induce hematopoietic stem cell hibernation. Blood 113, 1250–1256 (2009).
9. Yamazaki, S. et al. Nonmyelinating Schwann cells maintain hematopoietic stem cell hibernation in the bone marrow niche. Cell 147, 1146–1158 (2011).
10. Zhao, M. et al. FGF signaling facilitates postinjury recovery of mouse hematopoietic system. Blood 120, 1831–1842 (2012).
11. Itkin, T. et al. FGF-2 expands murine hematopoietic stem and progenitor cells via proliferation of stromal cells, c-Kit activation, and CXCL12 down-regulation. Blood 120, 1843–1855 (2012).
12. Li, L. & Clevers, H. Coexistence of quiescent and active adult stem cells in mammals. Science 327, 542–545 (2010).
13. Winkler, I.G. et al. Bone marrow macrophages maintain hematopoietic stem cell (HSC) niches and their depletion mobilizes HSCs. Blood 116, 4815–4828 (2010).
14. + macrophages promote the retention of hematopoietic stem and progenitor cells in the mesenchymal stem cell niche. J. Exp. Med. 208, 261–271 (2011).
15. + macrophages provide a niche promoting erythropoiesis under homeostasis and stress. Nat. Med. 19, 429–436 (2013).
16. Dominici, M. et al. Restoration and reversible expansion of the osteoblastic hematopoietic stem cell niche after marrow radioablation. Blood 114, 2333–2343 (2009).
17. Olson, T.S. et al. Megakaryocytes promote murine osteoblastic HSC niche expansion and stem cell engraftment after radioablative conditioning. Blood 121, 5238–5249 (2013).
18. Heazlewood, S.Y. et al. Megakaryocytes co-localise with hemopoietic stem cells and release cytokines that up-regulate stem cell proliferation. Stem Cell Res. 11, 782–792 (2013).
19. Deutsch, V.R. & Tomer, A. Megakaryocyte development and platelet production. Br. J. Haematol. 134, 453–466 (2006).
20. Xie, Y. et al. Detection of functional haematopoietic stem cell niche using real-time imaging. Nature 457, 97–101 (2009).
21. Tiedt, R., Schomber, T., Hao-Shen, H. & Skoda, R.C. Pf4-Cre transgenic mice allow the generation of lineage-restricted gene knockouts for studying megakaryocyte and platelet function in vivo. Blood 109, 1503–1506 (2007).
22. Madisen, L. et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 13, 133–140 (2010).
23. Buch, T. et al. A Cre-inducible diphtheria toxin receptor mediates cell lineage ablation after toxin administration. Nat. Methods 2, 419–426 (2005).
24. − short-term hematopoietic stem cells capable of rapidly reconstituting and rescuing myeloablated transplant recipients. Blood 105, 2717–2723 (2005).
25. Chen, C.Z. et al. Identification of endoglin as a functional marker that defines long-term repopulating hematopoietic stem cells. Proc. Natl. Acad. Sci. USA 99, 15468–15473 (2002).
26. Bruns, I. et al. Megakaryocytes regulate hematopoietic stem cell quiescence through Cxcl4 secretion. Nat. Med. 10.1038/nm.3707 (19 October 2014).
27. Longley, D.B., Harkin, D.P. & Johnston, P.G. 5-fluorouracil: mechanisms of action and clinical strategies. Nat. Rev. Cancer 3, 330–338 (2003).
28. Essers, M.A. et al. IFNα activates dormant haematopoietic stem cells in vivo. Nature 458, 904–908 (2009).
29. Elmasri, H. et al. Fatty acid binding protein 4 is a target of VEGF and a regulator of cell proliferation in endothelial cells. FASEB J. 23, 3865–3873 (2009).
30. Avecilla, S.T. et al. Chemokine-mediated interaction of hematopoietic progenitors with the bone marrow vascular niche is required for thrombopoiesis. Nat. Med. 10, 64–71 (2004).
31. Brenet, F., Kermani, P., Spektor, R., Rafii, S. & Scandura, J.M. TGFβ restores hematopoietic homeostasis after myelosuppressive chemotherapy. J. Exp. Med. 210, 623–639 (2013).
32. de Haan, G. et al. In vitro generation of long-term repopulating hematopoietic stem cells by fibroblast growth factor-1. Dev. Cell 4, 241–251 (2003).
33. Zhang, C.C. et al. Angiopoietin-like proteins stimulate ex vivo expansion of hematopoietic stem cells. Nat. Med. 12, 240–245 (2006).
34. Perry, J.M. et al. Cooperation between both Wnt/β-catenin and PTEN/PI3K/Akt signaling promotes primitive hematopoietic stem cell self-renewal and expansion. Genes Dev. 25, 1928–1942 (2011).
35. Calaminus, S.D. et al. Lineage tracing of Pf4-Cre marks hematopoietic stem cells and their progeny. PLoS ONE 7, e51361 (2012).
36. Xu, X., Qiao, W., Li, C. & Deng, C.X. Generation of Fgfr1 conditional knockout mice. Genesis 32, 85–86 (2002).
37. Azhar, M. et al. Generation of mice with a conditional allele for transforming growth factor β1 gene. Genesis 47, 423–431 (2009).
38. Meyer, A. et al. Platelet TGF-β1 contributions to plasma TGF-β1, cardiac fibrosis, and systolic dysfunction in a mouse model of pressure overload. Blood 119, 1064–1074 (2012).
39. Sugimura, R. et al. Noncanonical Wnt signaling maintains hematopoietic stem cells in the niche. Cell 150, 351–365 (2012).
40. Krause, D.S. et al. Differential regulation of myeloid leukemias by the bone marrow microenvironment. Nat. Med. 19, 1513–1517 (2013).