Multipotent hematopoietic progenitors divide asymmetrically to create progenitors of the lymphomyeloid and erythromyeloid lineages

Stem Cell Reports

Volumn 3, Issue 6, 2014, Pages 1058-1072

  Görgens, André ^a,b   Ludwig, Anna Kristin ^a   Möllmann, Michael ^a   Krawczyk, Adalbert ^a   Dürig, Jan ^a   Hanenberg, Helmut ^c   Horn, Peter A ^a,b   Giebel, Bernd ^a,b  

^a UNIVERSITY HOSPITAL ESSEN   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD133 ANTIGEN; EPITOPE; PARAFORMALDEHYDE; MEMBRANE ANTIGEN;

ANTIGEN EXPRESSION; ARTICLE; CELL FUNCTION; CELL LEVEL; CELL LINEAGE; CONTROLLED STUDY; DAUGHTER CELL; ERYTHROMYELOID LINEAGE; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; KINETICS; LYMPHOMYELOID LINEAGE; MOUSE; MULTIPOTENT STEM CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; ANIMAL; ASYMMETRIC CELL DIVISION; CELL ADHESION; CELL CULTURE; CELL DIFFERENTIATION; CELL MOTION; CFU COUNTING; CYTOLOGY; ERYTHROID PRECURSOR CELL; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; IMMUNOPHENOTYPING; LYMPHOID PROGENITOR CELL; METABOLISM; MYELOID PROGENITOR CELL; XENOGRAFT;

ANIMALS; ANTIGENS, SURFACE; ASYMMETRIC CELL DIVISION; CELL ADHESION; CELL DIFFERENTIATION; CELL LINEAGE; CELL MOVEMENT; CELLS, CULTURED; COLONY-FORMING UNITS ASSAY; ERYTHROID PRECURSOR CELLS; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEMATOPOIETIC STEM CELLS; HETEROGRAFTS; HUMANS; IMMUNOPHENOTYPING; LYMPHOID PROGENITOR CELLS; MICE; MYELOID PROGENITOR CELLS; PHENOTYPE;

EID: 84923802795     PISSN: 22136711     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stemcr.2014.09.016     Document Type: Article

References (37)

1. J. Beckmann, S. Scheitza, P. Wernet, J.C. Fischer, and B. Giebel Asymmetric cell division within the human hematopoietic stem and progenitor cell compartment: identification of asymmetrically segregating proteins Blood 109 2007 5494 5501
2. S. Bidlingmaier, X. Zhu, and B. Liu The utility and limitations of glycosylated human CD133 epitopes in defining cancer stem cells J. Mol. Med. 86 2008 1025 1032
3. T.H. Brummendorf, W. Dragowska, J.M.J.M. Zijlmans, G. Thornbury, P.M. Lansdorp Zijlmans JMJM Asymmetric cell divisions sustain long-term hematopoiesis from single-sorted human fetal liver cells J. Exp. Med. 188 1998 1117 1124
4. L.M. Calvi, G.B. Adams, K.W. Weibrecht, J.M. Weber, D.P. Olson, M.C. Knight, R.P. Martin, E. Schipani, P. Divieti, and F.R. Bringhurst Osteoblastic cells regulate the haematopoietic stem cell niche Nature 425 2003 841 846
5. K.C. Chang, C. Wang, and H. Wang Balancing self-renewal and differentiation by asymmetric division: insights from brain tumor suppressors in Drosophila neural stem cells Bioessays 34 2012 301 310
6. A. Cicalese, G. Bonizzi, C.E. Pasi, M. Faretta, S. Ronzoni, B. Giulini, C. Brisken, S. Minucci, P.P. Di Fiore, and P.G. Pelicci The tumor suppressor p53 regulates polarity of self-renewing divisions in mammary stem cells Cell 138 2009 1083 1095
7. L. Ding, and S.J. Morrison Haematopoietic stem cells and early lymphoid progenitors occupy distinct bone marrow niches Nature 495 2013 231 235
8. A.V. Fonseca, N. Bauer, and D. Corbeil The stem cell marker CD133 meets the endosomal compartment - new insights into the cell division of hematopoietic stem cells Blood Cells Mol. Dis. 41 2008 194 195
9. M. Gho, Y. Bellaïche, and F. Schweisguth Revisiting the Drosophila microchaete lineage: a novel intrinsically asymmetric cell division generates a glial cell Development 126 1999 3573 3584
10. B. Giebel Cell polarity and asymmetric cell division within human hematopoietic stem and progenitor cells Cells Tissues Organs (Print) 188 2008 116 126
11. B. Giebel, and A. Wodarz Notch signaling: numb makes the difference Curr. Biol. 22 2012 R133 R135
12. B. Giebel, D. Corbeil, J. Beckmann, J. Höhn, D. Freund, K. Giesen, J. Fischer, G. Kögler, and P. Wernet Segregation of lipid raft markers including CD133 in polarized human hematopoietic stem and progenitor cells Blood 104 2004 2332 2338
13. B. Giebel, T. Zhang, J. Beckmann, J. Spanholtz, P. Wernet, A.D. Ho, and M. Punzel Primitive human hematopoietic cells give rise to differentially specified daughter cells upon their initial cell division Blood 107 2006 2146 2152
14. A. Görgens, and B. Giebel Self-renewal of primitive hematopoietic cells: a focus on asymmetric cell division S. Kadereit, G. Udolph, Umbilical Cord Blood: A Future for Regenerative Medicine 2010 World Scientific Publishing Company Singapore 51 75
15. A. Görgens, J. Beckmann, A.K. Ludwig, M. Möllmann, J. Dürig, P.A. Horn, L. Rajendran, and B. Giebel Lipid raft redistribution and morphological cell polarization are separable processes providing a basis for hematopoietic stem and progenitor cell migration Int. J. Biochem. Cell Biol. 44 2012 1121 1132
16. A. Görgens, S. Radtke, P.A. Horn, and B. Giebel New relationships of human hematopoietic lineages facilitate detection of multipotent hematopoietic stem and progenitor cells Cell Cycle 12 2013 3478 3482
17. A. Görgens, S. Radtke, M. Möllmann, M. Cross, J. Dürig, P.A. Horn, and B. Giebel Revision of the human hematopoietic tree: granulocyte subtypes derive from distinct hematopoietic lineages Cell Reports 3 2013 1539 1552
18. A. Greenbaum, Y.M. Hsu, R.B. Day, L.G. Schuettpelz, M.J. Christopher, J.N. Borgerding, T. Nagasawa, and D.C. Link CXCL12 in early mesenchymal progenitors is required for haematopoietic stem-cell maintenance Nature 495 2013 227 230
19. C.C. Homem, and J.A. Knoblich Drosophila neuroblasts: a model for stem cell biology Development 139 2012 4297 4310
20. S. Huang, P. Law, K. Francis, B.O. Palsson, and A.D. Ho Symmetry of initial cell divisions among primitive hematopoietic progenitors is independent of ontogenic age and regulatory molecules Blood 94 1999 2595 2604
21. L. Jin, K.J. Hope, Q. Zhai, F. Smadja-Joffe, and J.E. Dick Targeting of CD44 eradicates human acute myeloid leukemic stem cells Nat. Med. 12 2006 1167 1174
22. O. Kollet, A. Spiegel, A. Peled, I. Petit, T. Byk, R. Hershkoviz, E. Guetta, G. Barkai, A. Nagler, and T. Lapidot Rapid and efficient homing of human CD34(+)CD38(-/low)CXCR4(+) stem and progenitor cells to the bone marrow and spleen of NOD/SCID and NOD/SCID/B2m(null) mice Blood 97 2001 3283 3291
23. T. Lapidot, A. Dar, and O. Kollet How do stem cells find their way home? Blood 106 2005 1901 1910
24. J.P. Lévesque, F.M. Helwani, and I.G. Winkler The endosteal 'osteoblastic' niche and its role in hematopoietic stem cell homing and mobilization Leukemia 24 2010 1979 1992
25. S. Lymperi, F. Ferraro, and D.T. Scadden The HSC niche concept has turned 31. Has our knowledge matured? Ann. N Y Acad. Sci. 1192 2010 12 18
26. S. Miraglia, W. Godfrey, A.H. Yin, K. Atkins, R. Warnke, J.T. Holden, R.A. Bray, E.K. Waller, and D.W. Buck A novel five-transmembrane hematopoietic stem cell antigen: isolation, characterization, and molecular cloning Blood 90 1997 5013 5021
27. M. Punzel, T. Zhang, D. Liu, V. Eckstein, and A.D. Ho Functional analysis of initial cell divisions defines the subsequent fate of individual human CD34(+)CD38(-) cells Exp. Hematol. 30 2002 464 472
28. L. Rajendran, J. Beckmann, A. Magenau, E.M. Boneberg, K. Gaus, A. Viola, B. Giebel, and H. Illges Flotillins are involved in the polarization of primitive and mature hematopoietic cells PLoS ONE 4 2009 e8290
29. R. Schofield The relationship between the spleen colony-forming cell and the haemopoietic stem cell Blood Cells 4 1978 7 25
30. S. Shivtiel, K. Lapid, V. Kalchenko, A. Avigdor, P. Goichberg, A. Kalinkovich, A. Nagler, O. Kollet, and T. Lapidot CD45 regulates homing and engraftment of immature normal and leukemic human cells in transplanted immunodeficient mice Exp. Hematol. 39 2011 1161 1170
31. S. Sugiarto, A.I. Persson, E.G. Munoz, M. Waldhuber, C. Lamagna, N. Andor, P. Hanecker, J. Ayers-Ringler, J. Phillips, and J. Siu Asymmetry-defective oligodendrocyte progenitors are glioma precursors Cancer Cell 20 2011 328 340
32. S.K. Swaminathan, M.R. Olin, C.L. Forster, K.S. Cruz, J. Panyam, and J.R. Ohlfest Identification of a novel monoclonal antibody recognizing CD133 J. Immunol. Methods 361 2010 110 115
33. D.C. Taussig, F. Miraki-Moud, F. Anjos-Afonso, D.J. Pearce, K. Allen, C. Ridler, D. Lillington, H. Oakervee, J. Cavenagh, and S.G. Agrawal Anti-CD38 antibody-mediated clearance of human repopulating cells masks the heterogeneity of leukemia-initiating cells Blood 112 2008 568 575
34. W. Wagner, F. Wein, C. Roderburg, R. Saffrich, A. Faber, U. Krause, M. Schubert, V. Benes, V. Eckstein, H. Maul, and A.D. Ho Adhesion of hematopoietic progenitor cells to human mesenchymal stem cells as a model for cell-cell interaction Exp. Hematol. 35 2007 314 325
35. M. Wu, H.Y. Kwon, F. Rattis, J. Blum, C. Zhao, R. Ashkenazi, T.L. Jackson, N. Gaiano, T. Oliver, and T. Reya Imaging hematopoietic precursor division in real time Cell Stem Cell 1 2007 541 554
36. E.D. Zanjani, A.W. Flake, G. Almeida-Porada, N. Tran, and T. Papayannopoulou Homing of human cells in the fetal sheep model: modulation by antibodies activating or inhibiting very late activation antigen-4-dependent function Blood 94 1999 2515 2522
37. J. Zhang, C. Niu, L. Ye, H. Huang, X. He, W.G. Tong, J. Ross, J. Haug, T. Johnson, and J.Q. Feng Identification of the haematopoietic stem cell niche and control of the niche size Nature 425 2003 836 841