High c-Kit expression identifies hematopoietic stem cells with impaired self-renewal and megakaryocytic bias

Journal of Experimental Medicine

Volumn 211, Issue 2, 2014, Pages 217-231

  Shin, Joseph Y ^a   Hu, Wenhuo ^a   Naramura, Mayumi ^b   Park, Christopher Y ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; CELL LINEAGE; CELL PROLIFERATION; COLONY-FORMING UNITS ASSAY; FLUOROURACIL; GENE EXPRESSION PROFILING; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEMATOPOIETIC STEM CELLS; MEGAKARYOCYTES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PROTO-ONCOGENE PROTEINS C-KIT; THROMBOPOIESIS;

EID: 84893803625     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20131128     Document Type: Article

References (50)

1. Agosti, V., S. Corbacioglu, I. Ehlers, C. Waskow, G. Sommer, G. Berrozpe, H. Kissel, C.M. Tucker, K. Manova, M.A. Moore, et al. 2004. Critical role for Kit-mediated Src kinase but not PI 3-kinase signaling in pro T and pro B cell development. J. Exp. Med. 199:867-878. http://dx.doi .org/10.1084/jem.20031983
2. Beerman, I., D. Bhattacharya, S. Zandi, M. Sigvardsson, I.L. Weissman, D. Bryder, and D.J. Rossi. 2010. Functionally distinct hematopoietic stem cells modulate hematopoietic lineage potential during aging by a mechanism of clonal expansion. Proc. Natl. Acad. Sci. USA. 107:5465-5470. http://dx.doi.org/10.1073/pnas.1000834107
3. Bosbach, B., S. Deshpande, F. Rossi, J.H. Shieh, G. Sommer, E. de Stanchina, D.R. Veach, J.M. Scandura, K. Manova-Todorova, M.A. Moore, et al. 2012. Imatinib resistance and microcytic erythrocytosis in a KitV558?;T669I/+ gatekeeper-mutant mouse model of gastrointestinal stromal tumor. Proc. Natl. Acad. Sci. USA. 109:E2276-E2283. http://dx.doi.org/10.1073/pnas.1115240109
4. Bryder, D., D.J. Rossi, and I.L. Weissman. 2006. Hematopoietic stem cells: the paradigmatic tissue-specific stem cell. Am. J. Pathol. 169:338-346. http://dx.doi.org/10.2353/ajpath.2006.060312
5. Caligiuri, M.A., R. Briesewitz, J. Yu, L. Wang, M. Wei, K.J. Arnoczky, T.B. Marburger, J. Wen, D. Perrotti, C.D. Bloomfield, and S.P. Whitman. 2007. Novel c-CBL and CBL-b ubiquitin ligase mutations in human acute myeloid leukemia. Blood. 110:1022-1024. http://dx.doi .org/10.1182/blood-2006-12-061176
6. Challen, G.A., N.C. Boles, S.M. Chambers, and M.A. Goodell. 2010. Distinct hematopoietic stem cell subtypes are differentially regulated by TGF-beta1. Cell Stem Cell. 6:265-278. http://dx.doi.org/10.1016/j.stem .2010.02.002
7. Christensen, J.L., and I.L. Weissman. 2001. Flk-2 is a marker in hematopoietic stem cell differentiation: a simple method to isolate long-term stem cells. Proc. Natl. Acad. Sci. USA. 98:14541-14546. http://dx.doi.org/ 10.1073/pnas.261562798
8. Czechowicz, A., D. Kraft, I.L. Weissman, and D. Bhattacharya. 2007. Efficient transplantation via antibody-based clearance of hematopoietic stem cell niches. Science. 318:1296-1299. http://dx.doi.org/10.1126/ science.1149726
9. Dykstra, B., D. Kent, M. Bowie, L. McCaffrey, M. Hamilton, K. Lyons, S.J. Lee, R. Brinkman, and C. Eaves. 2007. Long-term propagation of distinct hematopoietic differentiation programs in vivo. Cell Stem Cell. 1:218-229. http://dx.doi.org/10.1016/j.stem.2007.05.015
10. Forsberg, E.C., T. Serwold, S. Kogan, I.L. Weissman, and E. Passegué. 2006. New evidence supporting megakaryocyte-erythrocyte potential of flk2/flt3+ multipotent hematopoietic progenitors. Cell. 126:415-426. http://dx.doi.org/10.1016/j.cell.2006.06.037
11. Foudi, A., K. Hochedlinger, D. Van Buren, J.W. Schindler, R. Jaenisch, V. Carey, and H. Hock. 2009. Analysis of histone 2B-GFP retention reveals slowly cycling hematopoietic stem cells. Nat. Biotechnol. 27:84-90. http://dx.doi.org/10.1038/nbt.1517
12. Gerrits, A., B. Dykstra, O.J. Kalmykowa, K. Klauke, E. Verovskaya, M.J. Broekhuis, G. de Haan, and L.V. Bystrykh. 2010. Cellular barcoding tool for clonal analysis in the hematopoietic system. Blood. 115:2610-2618. http://dx.doi.org/10.1182/blood-2009-06-229757
13. Glimm, H., I.H. Oh, and C.J. Eaves. 2000. Human hematopoietic stem cells stimulated to proliferate in vitro lose engraftment potential during their S/G(2)/M transit and do not reenter G(0). Blood. 96:4185-4193.
14. Gotoh, A., H. Takahira, C. Mantel, S. Litz-Jackson, H.S. Boswell, and H.E. Broxmeyer. 1996. Steel factor induces serine phosphorylation of Stat3 in human growth factor-dependent myeloid cell lines. Blood. 88:138-145.
15. Iwasaki, H., S. Mizuno, Y. Arinobu, H. Ozawa, Y. Mori, H. Shigematsu, K. Takatsu, D.G. Tenen, and K. Akashi. 2006. The order of expression of transcription factors directs hierarchical specification of hematopoietic lineages. Genes Dev. 20:3010-3021. http://dx.doi.org/10.1101/gad.1493506
16. Katayama, N., J.P. Shih, S. Nishikawa, T. Kina, S.C. Clark, and M. Ogawa. 1993. Stage-specific expression of c-kit protein by murine hematopoietic progenitors. Blood. 82:2353-2360.
17. Kiel, M.J., O.H. Yilmaz, T. Iwashita, O.H. Yilmaz, C. Terhorst, and S.J. Morrison. 2005. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell. 121:1109-1121. http://dx.doi.org/10.1016/j.cell.2005.05.026
18. Laurenti, E., and J.E. Dick. 2012. Molecular and functional characterization of early human hematopoiesis. Ann. N. Y. Acad. Sci. 1266:68-71. http://dx.doi.org/10.1111/j.1749-6632.2012.06577.x
19. Maloney, M.A., M.J. Dorie, R.A. Lamela, Z.R. Rogers, and H.M. Patt. 1978. Hematopoietic stem cell regulatory volumes as revealed in studies of the bgj/bgj:W/WV chimera. J. Exp. Med. 147:1189-1197. http:// dx.doi.org/10.1084/jem.147.4.1189
20. Masson, K., E. Heiss, H. Band, and L. Rönnstrand. 2006. Direct binding of Cbl to Tyr568 and Tyr936 of the stem cell factor receptor/c-Kit is required for ligand-induced ubiquitination, internalization and degradation. Biochem. J. 399:59-67. http://dx.doi.org/10.1042/BJ20060464
21. Matsuoka, Y., Y. Sasaki, R. Nakatsuka, M. Takahashi, R. Iwaki, Y. Uemura, and Y. Sonoda. 2011. Low level of c-kit expression marks deeply quiescent murine hematopoietic stem cells. Stem Cells. 29:1783-1791. http:// dx.doi.org/10.1002/stem.721
22. McCulloch, E.A., L. Siminovitch, and J.E. Till. 1964. Spleen-Colony Formation in Anemic Mice of Genotype Ww. Science. 144:844-846. http://dx.doi.org/10.1126/science.144.3620.844
23. McGowan, K.A., W.W. Pang, R. Bhardwaj, M.G. Perez, J.V. Pluvinage, B.E. Glader, R. Malek, S.M. Mendrysa, I.L. Weissman, C.Y. Park, and G.S. Barsh. 2011. Reduced ribosomal protein gene dosage and p53 activation in low-risk myelodysplastic syndrome. Blood. 118:3622-3633. http://dx.doi.org/10.1182/blood-2010-11-318584
24. Miller, C.L., V.I. Rebel, M.E. Lemieux, C.D. Helgason, P.M. Lansdorp, and C.J. Eaves. 1996. Studies of W mutant mice provide evidence for alternate mechanisms capable of activating hematopoietic stem cells. Exp. Hematol. 24:185-194.
25. Morita, Y., H. Ema, and H. Nakauchi. 2010. Heterogeneity and hierarchy within the most primitive hematopoietic stem cell compartment. J. Exp. Med. 207:1173-1182. http://dx.doi.org/10.1084/jem.20091318
26. Müller-Sieburg, C.E., R.H. Cho, M. Thoman, B. Adkins, and H.B. Sieburg. 2002. Deterministic regulation of hematopoietic stem cell self-renewal and differentiation. Blood. 100:1302-1309.
27. Nakano, T., N. Waki, H. Asai, and Y. Kitamura. 1989. Lymphoid differentiation of the hematopoietic stem cell that reconstitutes total erythropoiesis of a genetically anemic W/Wv mouse. Blood. 73:1175-1179.
28. Naramura, M., N. Nandwani, H. Gu, V. Band, and H. Band. 2010. Rapidly fatal myeloproliferative disorders in mice with deletion of Casitas B-cell lymphoma (Cbl) and Cbl-b in hematopoietic stem cells. Proc. Natl. Acad. Sci. USA. 107:16274-16279. http://dx.doi.org/10.1073/ pnas.1007575107
29. Pang, W.W., E.A. Price, D. Sahoo, I. Beerman, W.J. Maloney, D.J. Rossi, S.L. Schrier, and I.L. Weissman. 2011. Human bone marrow hematopoietic stem cells are increased in frequency and myeloid-biased with age. Proc. Natl. Acad. Sci. USA. 108:20012-20017. http://dx.doi.org/10 .1073/pnas.1116110108
30. Passegué, E., A.J. Wagers, S. Giuriato, W.C. Anderson, and I.L. Weissman. 2005. Global analysis of proliferation and cell cycle gene expression in the regulation of hematopoietic stem and progenitor cell fates. J. Exp. Med. 202:1599-1611. http://dx.doi.org/10.1084/jem.20050967
31. Pietras, E.M., M.R. Warr, and E. Passegué. 2011. Cell cycle regulation in hematopoietic stem cells. J. Cell Biol. 195:709-720. http://dx.doi.org/10 .1083/jcb.201102131
32. Pronk, C.J., D.J. Rossi, R. Månsson, J.L. Attema, G.L. Norddahl, C.K. Chan, M. Sigvardsson, I.L. Weissman, and D. Bryder. 2007. Elucidation of the phenotypic, functional, and molecular topography of a myeloerythroid progenitor cell hierarchy. Cell Stem Cell. 1:428-442. http:// dx.doi.org/10.1016/j.stem.2007.07.005
33. Randall, T.D., and I.L. Weissman. 1997. Phenotypic and functional changes induced at the clonal level in hematopoietic stem cells after 5-fluorouracil treatment. Blood. 89:3596-3606.
34. Rathinam, C., C.B. Thien, W.Y. Langdon, H. Gu, and R.A. Flavell. 2008. The E3 ubiquitin ligase c-Cbl restricts development and functions of hematopoietic stem cells. Genes Dev. 22:992-997. http://dx.doi .org/10.1101/gad.1651408
35. Rathinam, C., C.B. Thien, R.A. Flavell, and W.Y. Langdon. 2010. Myeloid leukemia development in c-Cbl RING finger mutant mice is dependent on FLT3 signaling. Cancer Cell. 18:341-352. http://dx.doi .org/10.1016/j.ccr.2010.09.008
36. Rizo, A., E. Vellenga, G. de Haan, and J.J. Schuringa. 2006. Signaling pathways in self-renewing hematopoietic and leukemic stem cells: do all stem cells need a niche? Hum. Mol. Genet. 15(Spec No 2, Spec No 2):R210-R219. http://dx.doi.org/10.1093/hmg/ddl175
37. Ryan, J.J., H. Huang, L.J. McReynolds, C. Shelburne, J. Hu-Li, T.F. Huff, and W.E. Paul. 1997. Stem cell factor activates STAT-5 DNA binding in IL-3-derived bone marrow mast cells. Exp. Hematol. 25:357-362.
38. Sharma, Y., C.M. Astle, and D.E. Harrison. 2007. Heterozygous kit mutants with little or no apparent anemia exhibit large defects in overall hematopoietic stem cell function. Exp. Hematol. 35:214-220. http:// dx.doi.org/10.1016/j.exphem.2006.10.001
39. Shiohara, M., K. Koike, T. Kubo, Y. Amano, M. Takagi, K. Muraoka, J. Nakao, T. Nakahata, and A. Komiyama. 1993. Possible role of stem cell factor as a serum factor: monoclonal anti-c-kit antibody abrogates interleukin-6-dependent colony growth in serum-containing culture. Exp. Hematol. 21:907-912.
40. Thorén, L.A., K. Liuba, D. Bryder, J.M. Nygren, C.T. Jensen, H. Qian, J. Antonchuk, and S.E. Jacobsen. 2008. Kit regulates maintenance of quiescent hematopoietic stem cells. J. Immunol. 180:2045-2053.
41. Uchida, N., B. Dykstra, K.J. Lyons, F.Y. Leung, and C.J. Eaves. 2003. Different in vivo repopulating activities of purified hematopoietic stem cells before and after being stimulated to divide in vitro with the same kinetics. Exp. Hematol. 31:1338-1347.
42. van der Wath, R.C., A. Wilson, E. Laurenti, A. Trumpp, and P. Liò. 2009. Estimating dormant and active hematopoietic stem cell kinetics through extensive modeling of bromodeoxyuridine label-retaining cell dynamics. PLoS ONE. 4:e6972. http://dx.doi.org/10.1371/journal.pone.0006972
43. Wang, Z., and K.D. Bunting. 2008. Hematopoietic stem cell transplant into non-myeloablated W/Wv mice to detect steady-state engraftment defects. Methods Mol. Biol. 430:171-181. http://dx.doi.org/10.1007/978-1-59745-182-6_12
44. Waskow, C., V. Madan, S. Bartels, C. Costa, R. Blasig, and H.R. Rodewald. 2009. Hematopoietic stem cell transplantation without irradiation. Nat. Methods. 6:267-269. http://dx.doi.org/10.1038/nmeth.1309
45. Weksberg, D.C., S.M. Chambers, N.C. Boles, and M.A. Goodell. 2008. CD150-side population cells represent a functionally distinct population of long-term hematopoietic stem cells. Blood. 111:2444-2451. http://dx.doi.org/10.1182/blood-2007-09-115006
46. Wilson, A., E. Laurenti, G. Oser, R.C. van der Wath, W. Blanco-Bose, M. Jaworski, S. Offner, C.F. Dunant, L. Eshkind, E. Bockamp, et al. 2008. Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell. 135:1118-1129. http://dx.doi.org/ 10.1016/j.cell.2008.10.048
47. Wilson, A., E. Laurenti, and A. Trumpp. 2009. Balancing dormant and selfrenewing hematopoietic stem cells. Curr. Opin. Genet. Dev. 19:461-468. http://dx.doi.org/10.1016/j.gde.2009.08.005
48. Wright, D.E., S.H. Cheshier, A.J. Wagers, T.D. Randall, J.L. Christensen, and I.L. Weissman. 2001. Cyclophosphamide/granulocyte colonystimulating factor causes selective mobilization of bone marrow hematopoietic stem cells into the blood after M phase of the cell cycle. Blood. 97:2278-2285. http://dx.doi.org/10.1182/blood.V97 .8.2278
49. Yee, N.S., I. Paek, and P. Besmer. 1994. Role of kit-ligand in proliferation and suppression of apoptosis in mast cells: basis for radiosensitivity of white spotting and steel mutant mice. J. Exp. Med. 179:1777-1787. http://dx.doi.org/10.1084/jem.179.6.1777
50. Zeng, S., Z. Xu, S. Lipkowitz, and J.B. Longley. 2005. Regulation of stem cell factor receptor signaling by Cbl family proteins (Cbl-b/c-Cbl). Blood. 105:226-232. http://dx.doi.org/10.1182/blood-2004-05-1768