Experimental Hematology
Volume 36, Issue 5 , Pages 587-597 , May 2008

Regulation of human B lymphopoiesis by the transforming growth factor-β superfamily in a newly established coculture system using human mesenchymal stem cells as a supportive microenvironment

  • Michiko Ichii

      Affiliations

    • Department of Hematology and Oncology, Osaka University Graduate School of Medicine, Osaka, Japan
  • ,
  • Kenji Oritani

      Affiliations

    • Department of Hematology and Oncology, Osaka University Graduate School of Medicine, Osaka, Japan
    • Corresponding Author InformationOffprint requests to: Kenji Oritani, M.D., Department of Hematology and Oncology, Osaka University Graduate School of Medicine, 2-2 Yamadaoka, Suita City, Osaka 565-0871 Japan
  • ,
  • Takafumi Yokota

      Affiliations

    • Department of Hematology and Oncology, Osaka University Graduate School of Medicine, Osaka, Japan
  • ,
  • Makoto Nishida

      Affiliations

    • Health Care Center, Osaka University, Graduate School of Medicine, Osaka, Japan
  • ,
  • Isao Takahashi

      Affiliations

    • Department of Hematology and Oncology, Osaka University Graduate School of Medicine, Osaka, Japan
  • ,
  • Takahiro Shirogane

      Affiliations

    • Department of Hematology and Oncology, Osaka University Graduate School of Medicine, Osaka, Japan
  • ,
  • Sachiko Ezoe

      Affiliations

    • Department of Hematology and Oncology, Osaka University Graduate School of Medicine, Osaka, Japan
  • ,
  • Norimitsu Saitoh

      Affiliations

    • Department of Hematology and Oncology, Osaka University Graduate School of Medicine, Osaka, Japan
  • ,
  • Rie Tanigawa

      Affiliations

    • Department of Hematology and Oncology, Osaka University Graduate School of Medicine, Osaka, Japan
  • ,
  • Paul W. Kincade

      Affiliations

    • Oklahoma Medical Research Foundation, Oklahoma City, Okla., USA
  • ,
  • Yuzuru Kanakura

      Affiliations

    • Department of Hematology and Oncology, Osaka University Graduate School of Medicine, Osaka, Japan

Received 7 August 2007 ,Revised 27 December 2007 ,Accepted 31 December 2007.

References 

  1. Kincade PW, Oritani K, Zheng Z, Borghesi L, Smithson G, Yamashita Y. Cell interaction molecules utilized in bone marrow. Cell Adhes Commun. 1998;6:211–215
  2. Miyake K, Medina KL, Hayashi S, Ono S, Hamaoka T, Kincade PW. Monoclonal antibodies to Pgp-1/CD44 block lympho-hemopoiesis in long-term bone marrow cultures. J Exp Med. 1990;171:477–488
  3. Miyake K, Weissman IL, Greenberger JS, Kincade PW. Evidence for a role of the integrin VLA-4 in lympho-hemopoiesis. J Exp Med. 1991;173:599–607
  4. Oritani K, Medina KL, Tomiyama Y, et al. Limitin: an interferon-like cytokine that preferentially influences B-lymphocyte precursors. Nat Med. 2000;6:659–666
  5. Oritani K, Hirota S, Nakagawa T, et al. T lymphocytes constitutively produce an interferon like cytokine limitin characterized as a heat- and acid-stable and heparin-binding glycoprotein. Blood. 2003;101:178–185
  6. Yokota T, Meka CSR, Kouro T, et al. Adiponectin, a fat cell product, influences the earliest lymphocyte precursors in bone marrow cultures by activation of the cyclooxygenase-prostaglandin pathway in stromal cells. J Immunol. 2003;171:5091–5099
  7. Fortunel NO, Hatzfeld A, Hatzfeld JA. Transforming growth factor-β: pleiotropic role in the regulation of hematopoiesis. Blood. 2000;96:2022–2036
  8. van de Wetering M, de Lau W, Clevers H. WNT signaling and lymphocyte development. Cell. 2002;109:S13–S19
  9. Jaleco AC, Neves H, Hooijberg E, et al. Differential effects of Notch ligands Delta-1 and Jagged-1 in human lymphoid differentiation. J Exp Med. 2001;194:991–1001
  10. Kouro T, Medina KL, Oritani K, Kincade PW. Characteristics of early murine B-lymphocyte precursors and their direct sensitivity to negative regulators. Blood. 2001;97:2708–2715
  11. Borge OJ, Adolfsson J, Jacobsen AM. Lymphoid-restricted development from multipotent candidate murine stem cells: distinct and complimentary functions of the c-kit and flt3-ligands. Blood. 2000;94:3781–3790
  12. Nishihara M, Wada Y, Ogami K, et al. A combination of stem cell factor and granulocyte colony-stimulating factor enhances the growth of human progenitor B cells supported by murine stromal cell line MS-5. Eur J Immunol. 1998;28:855–864
  13. Rossi MID, Yokota T, Medina KL, et al. B lymphopoiesis is active throughout human life, but there are developmental age-related changes. Blood. 2003;101:576–584
  14. Hao QL, Zhu J, Price MA, Payne KJ, Barsky LW, Crooks GM. Identification of a novel, human multilymphoid progenitor in cord blood. Blood. 2001;97:3683–3690
  15. Miller JS, McCullar V, Punzel M, Lemischka IR, Moore KA. Single adult human CD34+/Lin-/CD38- progenitors give rise to natural killer cells, B-lineage cells, dendritic cells, and myeloid cells. Blood. 1999;93:96–106
  16. Goodwin RG, Lupton S, Schmierer A, et al. Human interleukin 7: molecular cloning and growth factor activity on human and murine B-lineage cells. Proc Natl Acad Sci U S A. 1989;86:302–306
  17. Peschon JJ, Morrissey PJ, Grabstein KH, et al. Early lymphocyte expansion is severely impaired in interleukin-7 receptor-deficient mice. J Exp Med. 1994;180:1955–1960
  18. von Freeden-Jeffrey U, Vieira P, Lucian LA, McNeil T, Burdach SE, Muray R. Lymphopenia in interlekin (IL)-7 gene-deleted mice identifies IL-7 as a nonredundant cytokine. J Exp Med. 1995;181:1519–1526
  19. Puel A, Ziegler SF, Buckley RH, Leonard WJ. Defective IL7R expression in T-B+NK+ severe combined immunodeficiency. Nat Genet. 1998;20:394–397
  20. Buckley RH. Molecular defects in human severe combined immunodeficiency and approaches to immune reconstitution. Annu Rev Immunol. 2004;22:625–655
  21. Pribyl JAR, LeBien TW. Interleukin 7 independent development of human B cells. Proc Natl Acad Sci U S A. 1996;93:10348–10353
  22. Dittel BN, LeBien TW. The growth response to IL-7 during normal human B cell ontogeny is restricted to B-lineage cells expressing CD34. J Immunol. 1995;154:58–67
  23. Miyazawa K, Shinozaki M, Hara T, Furuya T, Miyazono K. Two major Smad pathways in TGF-beta superfamily signaling. Genes Cells. 2002;7:1191–1204
  24. Shi Y, Massague J. Mechanisms of TGF-β signaling from cell membrane to the nucleus. Cell. 2003;113:685–700
  25. Blobe GC, Schiemann WP, Lodish HF. Role of transforming growth factor-β in human disease. N Engl J Med. 2000;342:1350–1358
  26. Shav-Tal Y, Zipori D. The role of Activin A in regulation of hemopoiesis. Stem Cells. 2002;20:493–500
  27. Bhatia M, Bonnet D, Wu D, et al. Bone morphogenetic proteins regulate the developmental program on human hematopoietic stem cells. J Exp Med. 1999;7:1139–1147
  28. Bertrand FE, Vogtenhuber C, Shah N, LeBien TW. Pro-B cell to pre-B cell development in B-lineage acute lymphoblastic leukemia expressing the MLL/AF4 fusion protein. Blood. 2001;98:3398–3405
  29. Masaie H, Oritani K, Yokota T, et al. Adiponectin binds to chemokines via the globular head and modulates interactions between chemokines and heparan sulfates. Exp Hematol. 2007;35:947–956
  30. Yoshida H, Tomiyama Y, Oritani K, et al. Interaction between Src homology 2 domain bearing protein tyrosine phosphatase substrate-1 and CD47 mediates the adhesion of human B lymphocytes to nonactivated endothelial cells. J Immunol. 2002;168:3213–3220
  31. Majumdar MK, Thiede MA, Mosca JD, Moorman M, Gerson SL. Phenotypic and functional comparison of cultures of marrow-derived mesenchymal stem cells (MSCs) and stromal cells. J Cell Physiol. 1998;176:57–66
  32. Kim DW, Chung YJ, Kim TG, Kim YL, Oh IH. Cotransplantation of third-party mesenchymal stromal cells can alleviate single-donor predominance and increase engraftment from double cord transplantation. Blood. 2004;103:1941–1948
  33. Nakata S, Matsumura I, Tanaka H, et al. NK-κB family proteins participate in multiple steps of hematopoesis through elimination of reactive oxygen species. J Biol Chem. 2004;279:55578–55586
  34. Sato N, Meijer L, Skaltsounis L, Greengard P, Brivanlou AH. Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nat Med. 2004;10:55–63
  35. Yaswen L, Kulkarni AB, Fredrickson T, et al. Autoimmune manifestations in the transforming growth factor-beta 1 knock-out mouse. Blood. 1996;87:1439–1445
  36. Larsson J, Blank U, Helgadottir H, et al. TGF-β signaling-deficient hematopoietic stem cells have normal self-renewal and regenerative ability in vivo despite increased proliferative capacity in vitro. Blood. 2003;102:3129–3135
  37. Cazac BB, Roes J. TGF-β receptor controls B cell responsiveness and induction of IgA in vivo. Immunity. 2000;13:443–451
  38. Kamesaki K, Nishizawa K, Michaud GY, Cossman J, Kiyono T. TGF-β1 induces the cyclin-dependent kinase inhibitor p27kip1 mRNA and protein in murine B cells. J Immunol. 1998;160:770–777
  39. Kee BL, Rivera RR, Murre C. Id3 inhibits B lymphocyte progenitor growth and survival in response to TGF-β. Nat Immunol. 2001;2:242–247
  40. Lee G, Namen AE, Gillis S, Ellingsworth LR, Kincade PW. Normal B cell precursors responsive to recombinant murine IL-7 and inhibition of IL-7 activity by transforming growth factor-β. J Immunol. 1989;142:3875–3883
  41. Zipori D, Barda-Saad M. Role of activin A in negative regulation of normal and tumor B lymphocytes. J Leukoc Biol. 2001;69:867–873

PII: S0301-472X(08)00002-7

doi: 10.1016/j.exphem.2007.12.013

Experimental Hematology
Volume 36, Issue 5 , Pages 587-597 , May 2008