Experimental Hematology
Volume 37, Issue 8 , Pages 924-936.e4 , August 2009

Enhanced generation of hematopoietic cells from human hepatocarcinoma cell−stimulated human embryonic and induced pluripotent stem cells

  • Min Lu

      Affiliations

    • Terry Fox Laboratory, British Columbia Cancer Agency, Vancouver, BC, Canada
  • ,
  • Melanie D. Kardel

      Affiliations

    • Terry Fox Laboratory, British Columbia Cancer Agency, Vancouver, BC, Canada
    • University of British Columbia, Vancouver, BC, Canada
  • ,
  • Michael D. O'Connor

      Affiliations

    • Terry Fox Laboratory, British Columbia Cancer Agency, Vancouver, BC, Canada
  • ,
  • Connie J. Eaves

      Affiliations

    • Terry Fox Laboratory, British Columbia Cancer Agency, Vancouver, BC, Canada
    • University of British Columbia, Vancouver, BC, Canada
    • Corresponding Author InformationOffprint requests to: Connie Eaves, Ph.D., Terry Fox Laboratory, British Columbia Cancer Agency, 675 West 10th Avenue, Vancouver, BC V5Z 1L3, Canada

Received 27 March 2009 ,Revised 18 May 2009 ,Accepted 19 May 2009.

References 

  1. Thomson JA, Itskovitz-Eldor J, Shapiro SS, et al. Embryonic stem cell lines derived from human blastocysts. Science. 1998;282:1145–1147
  2. Durand C, Dzierzak E. Embryonic beginnings of adult hematopoietic stem cells. Haematologica. 2005;90:100–108
  3. Park IH, Zhao R, West JA, et al. Reprogramming of human somatic cells to pluripotency with defined factors. Nature. 2008;451:141–146
  4. Schenke-Layland K, Rhodes KE, Angelis E, et al. Reprogrammed mouse fibroblasts differentiate into cells of the cardiovascular and hematopoietic lineages. Stem Cells. 2008;26:1537–1546
  5. Anderson JS, Bandi S, Kaufman DS, Akkina R. Derivation of normal macrophages from human embryonic stem (hES) cells for applications in HIV gene therapy. Retrovirology. 2006;3:24
  6. Chadwick K, Wang L, Li L, et al. Cytokines and BMP-4 promote hematopoietic differentiation of human embryonic stem cells. Blood. 2003;102:906–915
  7. Galic Z, Kitchen SG, Kacena A, et al. T lineage differentiation from human embryonic stem cells. Proc Natl Acad Sci U S A. 2006;103:11742–11747
  8. Kennedy M, D'Souza SL, Lynch-Kattman M, Schwantz S, Keller G. Development of the hemangioblast defines the onset of hematopoiesis in human ES cell differentiation cultures. Blood. 2007;109:2679–2687
  9. Slukvin , Vodyanik MA, Thomson JA, Gumenyuk ME, Choi KD. Directed differentiation of human embryonic stem cells into functional dendritic cells through the myeloid pathway. J Immunol. 2006;176:2924–2932
  10. Vodyanik MA, Bork JA, Thomson JA, Slukvin . Human embryonic stem cell-derived CD34+ cells: efficient production in the coculture with OP9 stromal cells and analysis of lymphohematopoietic potential. Blood. 2005;105:617–626
  11. Wang L, Li L, Shojaei F, et al. Endothelial and hematopoietic cell fate of human embryonic stem cells originates from primitive endothelium with hemangioblastic properties. Immunity. 2004;21:31–41
  12. Woll PS, Martin CH, Miller JS, Kaufman DS. Human embryonic stem cell-derived NK cells acquire functional receptors and cytolytic activity. J Immunol. 2005;175:5095–5103
  13. Ledran MH, Krassowska A, Armstrong L, et al. Efficient hematopoietic differentiation of human embryonic stem cells on stromal cells derived from hematopoietic niches. Cell Stem Cell. 2008;3:85–98
  14. Tian X, Woll PS, Morris JK, Linehan JL, Kaufman DS. Hematopoietic engraftment of human embryonic stem cell-derived cells is regulated by recipient innate immunity. Stem Cells. 2006;24:1370–1380
  15. Wang L, Menendez P, Shojaei F, et al. Generation of hematopoietic repopulating cells from human embryonic stem cells independent of ectopic HOXB4 expression. J Exp Med. 2005;201:1603–1614
  16. Narayan AD, Chase JL, Lewis RL, et al. Human embryonic stem cell-derived hematopoietic cells are capable of engrafting primary as well as secondary fetal sheep recipients. Blood. 2006;107:2180–2183
  17. Chang KH, Nelson AM, Cao H, et al. Definitive-like erythroid cells derived from human embryonic stem cells coexpress high levels of embryonic and fetal globins with little or no adult globin. Blood. 2006;108:1515–1523
  18. Pick M, Azzola L, Mossman A, Stanley EG, Elefanty AG. Differentiation of human embryonic stem cells in serum-free medium reveals distinct roles for bone morphogenetic protein 4, vascular endothelial growth factor, stem cell factor, and fibroblast growth factor 2 in hematopoiesis. Stem Cells. 2007;25:2206–2214
  19. Srivastava AS, Nedelcu E, Esmaeli-Azad B, Mishra R, Carrier E. Thrombopoietin enhances generation of CD34+ cells from human embryonic stem cells. Stem Cells. 2007;25:1456–1461
  20. Bowles KM, Vallier L, Smith JR, Alexander MR, Pedersen RA. HOXB4 overexpression promotes hematopoietic development by human embryonic stem cells. Stem Cells. 2006;24:1359–1369
  21. Lu SJ, Feng Q, Ivanova Y, et al. Recombinant HoxB4 fusion proteins enhance hematopoietic differentiation of human embryonic stem cells. Stem Cells Dev. 2007;16:547–559
  22. Unger C, Karner E, Treschow A, et al. Lentiviral-mediated HoxB4 expression in human embryonic stem cells initiates early hematopoiesis in a dose-dependent manner but does not promote myeloid differentiation. Stem Cells. 2008;26:2455–2466
  23. Woll PS, Morris JK, Painschab MS, et al. Wnt signaling promotes hematoendothelial cell development from human embryonic stem cells. Blood. 2008;111:122–131
  24. Kouskoff V, Lacaud G, Schwantz S, Fehling HJ, Keller G. Sequential development of hematopoietic and cardiac mesoderm during embryonic stem cell differentiation. Proc Natl Acad Sci U S A. 2005;102:13170–13175
  25. Lake J, Rathjen J, Remiszewski J, Rathjen PD. Reversible programming of pluripotent cell differentiation. J Cell Sci. 2000;113(Pt 3):555–566
  26. Pelton TA, Sharma S, Schulz TC, Rathjen J, Rathjen PD. Transient pluripotent cell populations during primitive ectoderm formation: correlation of in vivo and in vitro pluripotent cell development. J Cell Sci. 2002;115:329–339
  27. Rathjen J, Haines BP, Hudson KM, Nesci A, Dunn S, Rathjen PD. Directed differentiation of pluripotent cells to neural lineages: homogeneous formation and differentiation of a neurectoderm population. Development. 2002;129:2649–2661
  28. Rathjen J, Lake JA, Bettess MD, Washington JM, Chapman G, Rathjen PD. Formation of a primitive ectoderm like cell population, EPL cells, from ES cells in response to biologically derived factors. J Cell Sci. 1999;112(Pt 5):601–612
  29. Yu J, Vodyanik MA, Smuga-Otto K, et al. Induced pluripotent stem cell lines derived from human somatic cells. Science. 2007;318:1917–1920
  30. Ludwig TE, Bergendahl V, Levenstein ME, Yu J, Probasco MD, Thomson JA. Feeder-independent culture of human embryonic stem cells. Nat Methods. 2006;3:637–646
  31. O'Connor MD, Kardel MD, Iosfina I, et al. Alkaline phosphatase-positive colony formation is a sensitive, specific, and quantitative indicator of undifferentiated human embryonic stem cells. Stem Cells. 2008;26:1109–1116
  32. Watanabe K, Ueno M, Kamiya D, et al. A ROCK inhibitor permits survival of dissociated human embryonic stem cells. Nat Biotechnol. 2007;25:681–686
  33. Ishikawa F, Yasukawa M, Lyons B, et al. Development of functional human blood and immune systems in NOD/SCID/IL2 receptor {gamma} chain(null) mice. Blood. 2005;106:1565–1573
  34. Waye JS, England SB, Willard HF. Genomic organization of alpha satellite DNA on human chromosome 7: evidence for two distinct alphoid domains on a single chromosome. Mol Cell Biol. 1987;7:349–356
  35. Bauwens C, Yin T, Dang S, Peerani R, Zandstra PW. Development of a perfusion fed bioreactor for embryonic stem cell-derived cardiomyocyte generation: oxygen-mediated enhancement of cardiomyocyte output. Biotechnol Bioeng. 2005;90:452–461
  36. Zweigerdt R, Burg M, Willbold E, Abts H, Ruediger M. Generation of confluent cardiomyocyte monolayers derived from embryonic stem cells in suspension: a cell source for new therapies and screening strategies. Cytotherapy. 2003;5:399–413
  37. Calhoun JD, Rao RR, Warrenfeltz S, et al. Transcriptional profiling of initial differentiation events in human embryonic stem cells. Biochem Biophys Res Commun. 2004;323:453–464
  38. Itskovitz-Eldor J, Schuldiner M, Karsenti D, et al. Differentiation of human embryonic stem cells into embryoid bodies compromising the three embryonic germ layers. Mol Med. 2000;6:88–95
  39. Keller GM. In vitro differentiation of embryonic stem cells. Curr Opin Cell Biol. 1995;7:862–869
  40. Smith AG. Embryo-derived stem cells: of mice and men. Annu Rev Cell Dev Biol. 2001;17:435–462
  41. Qiu CH, Olivier EN, Velho M, Bouhassira EE. Globin switches in yolk sac-like primitive and fetal-like definitive red blood cells produced from human embryonic stem cells. Blood. 2008;111:2400–2408
  42. Martin CH, Woll PS, Ni Z, Zuniga-Pflucker JC, Kaufman DS. Differences in lymphocyte developmental potential between human embryonic stem cell and umbilical cord blood-derived hematopoietic progenitor cells. Blood. 2008;112:2730–2737
  43. Meng GL, Zur Nieden NI, Liu SY, Cormier JT, Kallos MS, Rancourt DE. Properties of murine embryonic stem cells maintained on human foreskin fibroblasts without LIF. Mol Reprod Dev. 2008;75:614–622
  44. Beattie GM, Lopez AD, Bucay N, et al. Activin A maintains pluripotency of human embryonic stem cells in the absence of feeder layers. Stem Cells. 2005;23:489–495
  45. D'Amour KA, Agulnick AD, Eliazer S, Kelly OG, Kroon E, Baetge EE. Efficient differentiation of human embryonic stem cells to definitive endoderm. Nat Biotechnol. 2005;23:1534–1541
  46. Murdoch B, Chadwick K, Martin M, et al. Wnt-5A augments repopulating capacity and primitive hematopoietic development of human blood stem cells in vivo. Proc Natl Acad Sci U S A. 2003;100:3422–3427

PII: S0301-472X(09)00177-5

doi: 10.1016/j.exphem.2009.05.007

Experimental Hematology
Volume 37, Issue 8 , Pages 924-936.e4 , August 2009