Experimental Hematology
Volume 37, Issue 12 , Pages 1400-1410 , December 2009

Bone marrow engraftment but limited expansion of hematopoietic cells from multipotent germline stem cells derived from neonatal mouse testis

  • Momoko Yoshimoto

      Affiliations

    • Department of Pediatrics, Kyoto University, Kyoto, Japan
    • Department of Pediatrics, Herman B Wells Center for Pediatric Research, Indiana University School of Medicine, Indianapolis, Ind., USA
    • Corresponding Author InformationOffprint requests to: Momoko Yoshimoto, M.D., Ph.D., Wells Center for Pediatric Research, Indiana University School of Medicine, Indianapolis, IN 46202, USA
  • ,
  • Toshio Heike

      Affiliations

    • Department of Pediatrics, Kyoto University, Kyoto, Japan
  • ,
  • Hsi Chang

      Affiliations

    • Department of Pediatrics, Kyoto University, Kyoto, Japan
  • ,
  • Mito Kanatsu-Shinohara

      Affiliations

    • Molecular Genetics, Graduate School of Medicine, Kyoto University, Kyoto, Japan
  • ,
  • Shiro Baba

      Affiliations

    • Department of Pediatrics, Kyoto University, Kyoto, Japan
  • ,
  • Joseph T. Varnau

      Affiliations

    • Department of Pediatrics, Herman B Wells Center for Pediatric Research, Indiana University School of Medicine, Indianapolis, Ind., USA
  • ,
  • Takashi Shinohara

      Affiliations

    • Molecular Genetics, Graduate School of Medicine, Kyoto University, Kyoto, Japan
  • ,
  • Mervin C. Yoder

      Affiliations

    • Department of Pediatrics, Herman B Wells Center for Pediatric Research, Indiana University School of Medicine, Indianapolis, Ind., USA
  • ,
  • Tatsutoshi Nakahata

      Affiliations

    • Department of Pediatrics, Kyoto University, Kyoto, Japan

Received 28 March 2009 ,Revised 1 September 2009 ,Accepted 21 September 2009.

References 

  1. Kyba M, Perlingeiro RC, Daley GQ. HoxB4 confers definitive lymphoid-myeloid engraftment potential on embryonic stem cell and yolk sac hematopoietic progenitors. Cell. 2002;109:29–37
  2. Wang Y, Yates F, Naveiras O, Ernst P, Daley GQ. Embryonic stem cell-derived hematopoietic stem cells. Proc Natl Acad Sci U S A. 2005;102:19081–19086
  3. Kanatsu-Shinohara M, Inoue K, Lee J, et al. Generation of pluripotent stem cells from neonatal mouse testis. Cell. 2004;119:1001–1012
  4. Kennedy M, Firpo M, Choi K, et al. A common precursor for primitive erythropoiesis and definitive haematopoiesis. Nature. 1997;386:488–493
  5. Kataoka H, Takakura N, Nishikawa S, et al. Expressions of PDGF receptor alpha, c-Kit and Flk1 genes clustering in mouse chromosome 5 define distinct subsets of nascent mesodermal cells. Dev Growth Differ. 1997;39:729–740
  6. Shalaby F, Rossant J, Yamaguchi TP, et al. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature. 1995;376:62–66
  7. Shalaby F, Ho J, Stanford WL, et al. A requirement for Flk1 in primitive and definitive hematopoiesis and vasculogenesis. Cell. 1997;89:981–990
  8. Nishikawa SI, Nishikawa S, Hirashima M, Matsuyoshi N, Kodama H. Progressive lineage analysis by cell sorting and culture identifies FLK1+VE-cadherin+ cells at a diverging point of endothelial and hemopoietic lineages. Development. 1998;125:1747–1757
  9. Nakano T, Kodama H, Honjo T. Generation of lymphohematopoietic cells from embryonic stem cells in culture. Science. 1994;265:1098–1101
  10. Nishikawa SI, Nishikawa S, Kawamoto H, et al. In vitro generation of lymphohematopoietic cells from endothelial cells purified from murine embryos. Immunity. 1998;8:761–769
  11. Iida M, Heike T, Yoshimoto M, Baba S, Doi H, Nakahata T. Identification of cardiac stem cells with FLK1, CD31, and VE-cadherin expression during embryonic stem cell differentiation. FASEB J. 2005;19:371–378
  12. Schmitt TM, de Pooter RF, Gronski MA, Cho SK, Ohashi PS, Zuniga-Pflucker JC. Induction of T cell development and establishment of T cell competence from embryonic stem cells differentiated in vitro. Nat Immunol. 2004;5:410–417
  13. Nakahata T, Ogawa M. Identification in culture of a class of hemopoietic colony-forming units with extensive capability to self-renew and generate multipotential hemopoietic colonies. Proc Natl Acad Sci U S A. 1982;79:3843–3847
  14. Nakahata T, Ogawa M. Hemopoietic colony-forming cells in umbilical cord blood with extensive capability to generate mono- and multipotential hemopoietic progenitors. J Clin Invest. 1982;70:1324–1328
  15. Miwa Y, Atsumi T, Imai N, Ikawa Y. Primitive erythropoiesis of mouse teratocarcinoma stem cells PCC3/A/1 in serum-free medium. Development. 1991;111:543–549
  16. Goodell MA, Brose K, Paradis G, Conner AS, Mulligan RC. Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med. 1996;183:1797–1806
  17. Tsuchiya A, Heike T, Fujino H, et al. Long-term extensive expansion of mouse hepatic stem/progenitor cells in a novel serum-free culture system. Gastroenterology. 2005;128:2089–2104
  18. Nagato M, Heike T, Kato T, et al. Prospective characterization of neural stem cells by flow cytometry analysis using a combination of surface markers. J Neurosci Res. 2005;80:456–466
  19. Yoshimoto M, Chang H, Shiota M, et al. Two different roles of purified CD45+c-Kit+Sca-1+Lin- cells after transplantation in muscles. Stem Cells. 2005;23:610–618
  20. Umeda K, Heike T, Yoshimoto M, et al. Development of primitive and definitive hematopoiesis from nonhuman primate embryonic stem cells in vitro. Development. 2004;131:1869–1879
  21. Umeda K, Heike T, Yoshimoto M, et al. Identification and characterization of hemoangiogenic progenitors during cynomolgus monkey embryonic stem cell differentiation. Stem Cells. 2006;24:1348–1358
  22. Fujimoto T, Ogawa M, Minegishi N, et al. Step-wise divergence of primitive and definitive haematopoietic and endothelial cell lineages during embryonic stem cell differentiation. Genes Cells. 2001;6:1113–1127
  23. Yoshimoto M, Shinohara T, Heike T, Shiota M, Kanatsu-Shinohara M, Nakahata T. Direct visualization of transplanted hematopoietic cell reconstitution in intact mouse organs indicates the presence of a niche. Exp Hematol. 2003;31:733–740
  24. Arai F, Hirao A, Ohmura M, et al. Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell. 2004;118:149–161
  25. Nilsson SK, Johnston HM, Coverdale JA. Spatial localization of transplanted hemopoietic stem cells: inferences for the localization of stem cell niches. Blood. 2001;97:2293–2299
  26. Choi K. The hemangioblast: a common progenitor of hematopoietic and endothelial cells. J Hematother Stem Cell Res. 2002;11:91–101
  27. Yoder MC, Hiatt K, Dutt P, Mukherjee P, Bodine DM, Orlic D. Characterization of definitive lymphohematopoietic stem cells in the day 9 murine yolk sac. Immunity. 1997;7:335–344
  28. Yoder MC, Hiatt K, Mukherjee P. In vivo repopulating hematopoietic stem cells are present in the murine yolk sac at day 9.0 postcoitus. Proc Natl Acad Sci U S A. 1997;94:6776–6780
  29. Ito M, Hiramatsu H, Kobayashi K, et al. NOD/SCID/gamma(c)(null) mouse: an excellent recipient mouse model for engraftment of human cells. Blood. 2002;100:3175–3182
  30. Hiramatsu H, Nishikomori R, Heike T, et al. Complete reconstitution of human lymphocytes from cord blood CD34+ cells using the NOD/SCID/gammacnull mice model. Blood. 2003;102:873–880
  31. Cumano A, Ferraz JC, Klaine M, Di Santo JP, Godin I. Intraembryonic, but not yolk sac hematopoietic precursors, isolated before circulation, provide long-term multilineage reconstitution. Immunity. 2001;15:477–485
  32. 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
  33. Wilson A, Laurenti E, Oser G, et al. Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell. 2008;135:1118–1129
  34. Guan K, Nayernia K, Maier LS, et al. Pluripotency of spermatogonial stem cells from adult mouse testis. Nature. 2006;440:1199–1203
  35. Conrad S, Renninger M, Hennenlotter J, et al. Generation of pluripotent stem cells from adult human testis. Nature. 2008;456:344–349
  36. Kossack N, Meneses J, Shefi S, et al. Isolation and characterization of pluripotent human spermatogonial stem cell-derived cells. Stem Cells. 2009;27:138–149
  37. Takahashi K, Tanabe K, Ohnuki M, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell. 2007;131:861–872
  38. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006;126:663–676
  39. Wernig M, Meissner A, Foreman R, et al. In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature. 2007;448:318–324

PII: S0301-472X(09)00368-3

doi: 10.1016/j.exphem.2009.09.006

Experimental Hematology
Volume 37, Issue 12 , Pages 1400-1410 , December 2009