Hematopoietic stem cell subtypes expand differentially during development and display distinct lymphopoietic programs

Cell Stem Cell

Volumn 10, Issue 3, 2012, Pages 273-283

  Benz, Claudia ^a   Copley, Michael R ^a   Kent, David G ^a   Wohrer, Stefan ^a   Cortes, Adrian ^a   Aghaeepour, Nima ^a   Ma, Elaine ^a   Mader, Heidi ^a   Rowe, Keegan ^a   Day, Christopher ^a   Treloar, David ^a   Brinkman, Ryan R ^a,b   Eaves, Connie J ^a,b  

^a BRITISH COLUMBIA CANCER AGENCY   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ARTICLE; CD45+EPCR+CD48-CD150+ T LYMPHOCYTE; CELL AGING; CELL DIFFERENTIATION; CELL MATURATION; CELL REGENERATION; CELL SUBPOPULATION; FETUS DEVELOPMENT; HEMATOPOIETIC STEM CELL; LYMPHOPOIESIS; MOUSE; NONHUMAN; PERINATAL DEVELOPMENT; PHENOTYPE; PRINCIPAL COMPONENT ANALYSIS; PRIORITY JOURNAL; STEM CELL EXPANSION; T LYMPHOCYTE;

ANIMALS; CELL AGING; CELL DIFFERENTIATION; CELL LINEAGE; FEMALE; FLOW CYTOMETRY; HEMATOPOIETIC STEM CELLS; HUMANS; LYMPHOPOIESIS; MICE; MICE, INBRED C57BL; PREGNANCY;

EID: 84857873445     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2012.02.007     Document Type: Article

References (47)

1. I. Beerman, D. Bhattacharya, S. Zandi, M. Sigvardsson, I.L. Weissman, D. Bryder, and D.J. Rossi Functionally distinct hematopoietic stem cells modulate hematopoietic lineage potential during aging by a mechanism of clonal expansion Proc. Natl. Acad. Sci. USA 107 2010 5465 5470
2. D.R. Boggs The total marrow mass of the mouse: a simplified method of measurement Am. J. Hematol. 16 1984 277 286 (Pubitemid 14127685)
3. M.B. Bowie, K.D. McKnight, D.G. Kent, L. McCaffrey, P.A. Hoodless, and C.J. Eaves Hematopoietic stem cells proliferate until after birth and show a reversible phase-specific engraftment defect J. Clin. Invest. 116 2006 2808 2816 (Pubitemid 44511644)
4. M.B. Bowie, D.G. Kent, B. Dykstra, K.D. McKnight, L. McCaffrey, P.A. Hoodless, and C.J. Eaves Identification of a new intrinsically timed developmental checkpoint that reprograms key hematopoietic stem cell properties Proc. Natl. Acad. Sci. USA 104 2007 5878 5882 (Pubitemid 47175627)
5. G.A. Challen, N.C. Boles, S.M. Chambers, and M.A. Goodell Distinct hematopoietic stem cell subtypes are differentially regulated by TGF-beta1 Cell Stem Cell 6 2010 265 278
6. R.H. Cho, H.B. Sieburg, and C.E. Muller-Sieburg A new mechanism for the aging of hematopoietic stem cells: aging changes the clonal composition of the stem cell compartment but not individual stem cells Blood 111 2008 5553 5561
7. G.A. Colvin, J.F. Lambert, M. Abedi, C.C. Hsieh, J.E. Carlson, F.M. Stewart, and P.J. Quesenberry Murine marrow cellularity and the concept of stem cell competition: geographic and quantitative determinants in stem cell biology Leukemia 18 2004 575 583 (Pubitemid 38425873)
8. J.E. Dick, M.C. Magli, D. Huszar, R.A. Phillips, and A. Bernstein Introduction of a selectable gene into primitive stem cells capable of long-term reconstitution of the hemopoietic system of W/Wv mice Cell 42 1985 71 79 (Pubitemid 16237557)
9. B. Dykstra, D. Kent, M. Bowie, L. McCaffrey, M. Hamilton, K. Lyons, S.J. Lee, R. Brinkman, and C. Eaves Long-term propagation of distinct hematopoietic differentiation programs in vivo Cell Stem Cell 1 2007 218 229 (Pubitemid 47215588)
10. B. Dykstra, S. Olthof, J. Schreuder, M. Ritsema, and G. de Haan Clonal analysis reveals multiple functional defects of aged murine hematopoietic stem cells J. Exp. Med. 208 2011 2691 2703
11. E. Dzierzak The emergence of definitive hematopoietic stem cells in the mammal Curr. Opin. Hematol. 12 2005 197 202 (Pubitemid 40676826)
12. W.H. Fleming, E.J. Alpern, N. Uchida, K. Ikuta, G.J. Spangrude, and I.L. Weissman Functional heterogeneity is associated with the cell cycle status of murine hematopoietic stem cells J. Cell Biol. 122 1993 897 902 (Pubitemid 23241098)
13. A. Foudi, K. Hochedlinger, D. Van Buren, J.W. Schindler, R. Jaenisch, V. Carey, and H. Hock Analysis of histone 2B-GFP retention reveals slowly cycling hematopoietic stem cells Nat. Biotechnol. 27 2009 84 90
14. M.A. Goodell, K. Brose, G. Paradis, A.S. Conner, and R.C. Mulligan Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo J. Exp. Med. 183 1996 1797 1806 (Pubitemid 26134320)
15. Y. Hu, and G.K. Smyth ELDA: extreme limiting dilution analysis for comparing depleted and enriched populations in stem cell and other assays J. Immunol. Methods 347 2009 70 78
16. C.T. Jordan, and I.R. Lemischka Clonal and systemic analysis of long-term hematopoiesis in the mouse Genes Dev. 4 1990 220 232
17. G. Keller, and R. Snodgrass Life span of multipotential hematopoietic stem cells in vivo J. Exp. Med. 171 1990 1407 1418 (Pubitemid 20167539)
18. D. Kent, B. Dykstra, and C. Eaves Isolation and assessment of long-term reconstituting hematopoietic stem cells from adult mouse bone marrow Curr. Protoc. Stem Cell Biol. 2007 Chapter 2, Unit 2A 4
19. D.G. Kent, M.R. Copley, C. Benz, S. Wöhrer, B.J. Dykstra, E. Ma, J. Cheyne, Y. Zhao, M.B. Bowie, and Y. Zhao Prospective isolation and molecular characterization of hematopoietic stem cells with durable self-renewal potential Blood 113 2009 6342 6350
20. M.J. Kiel, T. Iwashita, O.H. Yilmaz, and S.J. Morrison Spatial differences in hematopoiesis but not in stem cells indicate a lack of regional patterning in definitive hematopoietic stem cells Dev. Biol. 283 2005 29 39 (Pubitemid 40828840)
21. J.E. Labrie 3rd, A.P. Sah, D.M. Allman, M.P. Cancro, and R.M. Gerstein Bone marrow microenvironmental changes underlie reduced RAG-mediated recombination and B cell generation in aged mice J. Exp. Med. 200 2004 411 423 (Pubitemid 39121899)
22. I.R. Lemischka, D.H. Raulet, and R.C. Mulligan Developmental potential and dynamic behavior of hematopoietic stem cells Cell 45 1986 917 927 (Pubitemid 16083695)
23. C. Lescale, S. Dias, J. Maës, A. Cumano, P. Szabo, D. Charron, M.E. Weksler, C. Dosquet, P. Vieira, and M. Goodhardt Reduced EBF expression underlies loss of B-cell potential of hematopoietic progenitors with age Aging Cell 9 2010 410 419
24. R. Lu, N.F. Neff, S.R. Quake, and I.L. Weissman Tracking single hematopoietic stem cells in vivo using high-throughput sequencing in conjunction with viral genetic barcoding Nat. Biotechnol. 29 2011 928 933
25. J.P. Miller, and D. Allman The decline in B lymphopoiesis in aged mice reflects loss of very early B-lineage precursors J. Immunol. 171 2003 2326 2330 (Pubitemid 37025538)
26. J.P. Miller, and D. Allman Linking age-related defects in B lymphopoiesis to the aging of hematopoietic stem cells Semin. Immunol. 17 2005 321 329 (Pubitemid 41058762)
27. Y. Morita, H. Ema, and H. Nakauchi Heterogeneity and hierarchy within the most primitive hematopoietic stem cell compartment J. Exp. Med. 207 2010 1173 1182
28. S.J. Morrison, and I.L. Weissman The long-term repopulating subset of hematopoietic stem cells is deterministic and isolatable by phenotype Immunity 1 1994 661 673 (Pubitemid 124000730)
29. S.J. Morrison, H.D. Hemmati, A.M. Wandycz, and I.L. Weissman The purification and characterization of fetal liver hematopoietic stem cells Proc. Natl. Acad. Sci. USA 92 1995 10302 10306
30. C.E. Muller-Sieburg, and H.B. Sieburg Clonal diversity of the stem cell compartment Curr. Opin. Hematol. 13 2006 243 248 (Pubitemid 44288900)
31. C.E. Muller-Sieburg, R.H. Cho, L. Karlsson, J.F. Huang, and H.B. Sieburg Myeloid-biased hematopoietic stem cells have extensive self-renewal capacity but generate diminished lymphoid progeny with impaired IL-7 responsiveness Blood 103 2004 4111 4118 (Pubitemid 38685351)
32. T. Nakano, H. Kodama, and T. Honjo Generation of lymphohematopoietic cells from embryonic stem cells in culture Science 265 1994 1098 1101 (Pubitemid 24293078)
33. D.L. Northrup, and D. Allman Transcriptional regulation of early B cell development Immunol. Res. 42 2008 106 117
34. P. Papathanasiou, J.L. Attema, H. Karsunky, J. Xu, S.T. Smale, and I.L. Weissman Evaluation of the long-term reconstituting subset of hematopoietic stem cells with CD150 Stem Cells 27 2009 2498 2508
35. R. Pawliuk, C. Eaves, and R.K. Humphries Evidence of both ontogeny and transplant dose-regulated expansion of hematopoietic stem cells in vivo Blood 88 1996 2852 2858 (Pubitemid 26357365)
36. T.D. Randall, and I.L. Weissman Phenotypic and functional changes induced at the clonal level in hematopoietic stem cells after 5-fluorouracil treatment Blood 89 1997 3596 3606 (Pubitemid 27227082)
37. V.I. Rebel, C.L. Miller, C.J. Eaves, and P.M. Lansdorp The repopulation potential of fetal liver hematopoietic stem cells in mice exceeds that of their liver adult bone marrow counterparts Blood 87 1996 3500 3507 (Pubitemid 26115384)
38. D.J. Rossi, D. Bryder, J.M. Zahn, H. Ahlenius, R. Sonu, A.J. Wagers, and I.L. Weissman Cell intrinsic alterations underlie hematopoietic stem cell aging Proc. Natl. Acad. Sci. USA 102 2005 9194 9199 (Pubitemid 40923540)
39. L.G. Smith, I.L. Weissman, and S. Heimfeld Clonal analysis of hematopoietic stem-cell differentiation in vivo Proc. Natl. Acad. Sci. USA 88 1991 2788 2792 (Pubitemid 21916504)
40. G.J. Spangrude, D.M. Brooks, and D.B. Tumas Long-term repopulation of irradiated mice with limiting numbers of purified hematopoietic stem cells: in vivo expansion of stem cell phenotype but not function Blood 85 1995 1006 1016
41. S.J. Szilvassy, P.L. Ragland, C.L. Miller, and C.J. Eaves The marrow homing efficiency of murine hematopoietic stem cells remains constant during ontogeny Exp. Hematol. 31 2003 331 338 (Pubitemid 36407610)
42. N. Takeda, R. Jain, M.R. LeBoeuf, Q. Wang, M.M. Lu, and J.A. Epstein Interconversion between intestinal stem cell populations in distinct niches Science 334 2011 1420 1424
43. H. Tian, B. Biehs, S. Warming, K.G. Leong, L. Rangell, O.D. Klein, and F.J. de Sauvage A reserve stem cell population in small intestine renders Lgr5-positive cells dispensable Nature 478 2011 255 259
44. A. Van Keymeulen, A.S. Rocha, M. Ousset, B. Beck, G. Bouvencourt, J. Rock, N. Sharma, S. Dekoninck, and C. Blanpain Distinct stem cells contribute to mammary gland development and maintenance Nature 479 2011 189 193
45. A.M. Wu, J.E. Till, L. Siminovitch, and E.A. McCulloch Cytological evidence for a relationship between normal hemotopoietic colony-forming cells and cells of the lymphoid system J. Exp. Med. 127 1968 455 464
46. K.S. Yan, L.A. Chia, X. Li, A. Ootani, J. Su, J.Y. Lee, N. Su, Y. Luo, S.C. Heilshorn, and M.R. Amieva The intestinal stem cell markers Bmi1 and Lgr5 identify two functionally distinct populations Proc. Natl. Acad. Sci. USA 109 2012 466 471
47. R.K. Zhong, C.M. Astle, and D.E. Harrison Distinct developmental patterns of short-term and long-term functioning lymphoid and myeloid precursors defined by competitive limiting dilution analysis in vivo J. Immunol. 157 1996 138 145 (Pubitemid 26190540)