Experimental Hematology
Volume 35, Issue 3 , Pages 385-393 , March 2007

Bcl-2 and Bcl-XL are indispensable for the late phase of mast cell development from mouse embryonic stem cells

  • Christine Möller

      Affiliations

    • Department of Medicine, Karolinska Institutet, Stockholm, Sweden
    • Corresponding Author InformationOffprint requests to: Christine Möller, Ph.D., Karolinska Institutet, Department of Medicine, Clinical Immunology and Allergy Unit, KS L2:04, SE-171 76 Stockholm, Sweden
    • ,
  • Mats Karlberg

      Affiliations

    • Department of Medicine, Karolinska Institutet, Stockholm, Sweden
    • ,
  • Magnus Åbrink

      Affiliations

    • Department of Molecular Biosciences, Swedish University of Agricultural Sciences, Uppsala, Sweden
    • ,
  • Keiichi I. Nakayama

      Affiliations

    • Division of Cell Biology, Department of Molecular and Cellular Biology, Medical Institute of Bioregulation, Kyushu University, Fukuoka, Japan
    • ,
  • Noboru Motoyama

      Affiliations

    • Department of Geriatric Research, National Institute for Longevity Sciences, National Center for Geriatrics and Gerontology, Obu, Aichi, Japan
    • ,
  • Gunnar Nilsson

      Affiliations

    • Department of Medicine, Karolinska Institutet, Stockholm, Sweden

Received 3 May 2006 ,Revised 16 November 2006 ,Accepted 16 November 2006.

References 

  1. Adams JM. Ways of dying: multiple pathways to apoptosis. Genes Dev. 2003;17:2481–2495
  2. Adams JM, Cory S. Life-or-death decisions by the Bcl-2 protein family. Trends Biochem Sci. 2001;26:61–66
  3. Strasser A, O'Connor L, Dixit VM. Apoptosis signaling. Annu Rev Biochem. 2000;69:217–245
  4. Kawakami T, Galli SJ. Regulation of mast-cell and basophil function and survival by IgE. Nat Rev Immunol. 2002;2:773–786
  5. Mekori YA, Oh CK, Metcalfe DD. IL-3-dependent murine mast cells undergo apoptosis on removal of IL-3. Prevention of apoptosis by c-kit ligand. J Immunol. 1993;151:3775–3784
  6. Iemura A, Tsai M, Ando A, Wershil BK, Galli SJ. The c-kit ligand, stem cell factor, promotes mast cell survival by suppressing apoptosis. Am J Pathol. 1994;144:321–328
  7. Moller C, Alfredsson J, Engstrom M, et al. Stem cell factor promotes mast cell survival via inactivation of FOXO3a-mediated transcriptional induction and MEK-regulated phosphorylation of the proapoptotic protein Bim. Blood. 2005;106:1330–1336
  8. Xiang Z, Ahmed AA, Moller C, Nakayama K, Hatakeyama S, Nilsson G. Essential role of the prosurvival bcl-2 homologue A1 in mast cell survival after allergic activation. J Exp Med. 2001;194:1561–1569
  9. Boise LH, Gonzalez-Garcia M, Postema CE, et al. bcl-x, a bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell. 1993;74:597–608
  10. Yang E, Korsmeyer SJ. Molecular thanatopsis: a discourse on the BCL2 family and cell death. Blood. 1996;88:386–401
  11. Baghestanian M, Jordan JH, Kiener HP, et al. Activation of human mast cells through stem cell factor receptor (KIT) is associated with expression of bcl-2. Int Arch Allergy Immunol. 2002;129:228–236
  12. Mekori YA, Gilfillan AM, Akin C, Hartmann K, Metcalfe DD. Human mast cell apoptosis is regulated through Bcl-2 and Bcl-XL. J Clin Immunol. 2001;21:171–174
  13. Hartmann K, Artuc M, Baldus SE, et al. Expression of Bcl-2 and Bcl-xL in cutaneous and bone marrow lesions of mastocytosis. Am J Pathol. 2003;163:819–826
  14. Maurer M, Tsai M, Metz M, Fish S, Korsmeyer SJ, Galli SJ. A role for Bax in the regulation of apoptosis in mouse mast cells. J Invest Dermatol. 2000;114:1205–1206
  15. Cohen-Saidon C, Nechushtan H, Kahlon S, Livni N, Nissim A, Razin E. A novel strategy using single-chain antibody to show the importance of Bcl-2 in mast cell survival. Blood. 2003;102:2506–2512
  16. Alfredsson J, Puthalakath H, Martin H, Strasser A, Nilsson G. Proapoptotic Bcl-2 family member Bim is involved in the control of mast cell survival and is induced together with Bcl-XL upon IgE-receptor activation. Cell Death Differ. 2005;12:136–144
  17. Motoyama N, Wang F, Roth KA, et al. Massive cell death of immature hematopoietic cells and neurons in Bcl-x-deficient mice. Science. 1995;267:1506–1510
  18. Nakayama K, Negishi I, Kuida K, et al. Disappearance of the lymphoid system in Bcl-2 homozygous mutant chimeric mice. Science. 1993;261:1584–1588
  19. Wiles MV, Keller G. Multiple hematopoietic lineages develop from embryonic stem (ES) cells in culture. Development. 1991;111:259–267
  20. Tsai M, Wedemeyer J, Ganiatsas S, Tam SY, Zon LI, Galli SJ. In vivo immunological function of mast cells derived from embryonic stem cells: an approach for the rapid analysis of even embryonic lethal mutations in adult mice in vivo. Proc Natl Acad Sci U S A. 2000;97:9186–9190
  21. Nakayama K, Negishi I, Kuida K, Sawa H, Loh DY. Targeted disruption of Bcl-2 alpha beta in mice: occurrence of gray hair, polycystic kidney disease, and lymphocytopenia. Proc Natl Acad Sci U S A. 1994;91:3700–3704
  22. Tsai M, Tam SY, Wedemeyer J, Galli SJ. Mast cells derived from embryonic stem cells: a model system for studying the effects of genetic manipulations on mast cell development, phenotype, and function in vitro and in vivo. Int J Hematol. 2002;75:345–349
  23. Miller HR, Wright SH, Knight PA, Thornton EM. A novel function for transforming growth factor-beta1: upregulation of the expression and the IgE-independent extracellular release of a mucosal mast cell granule-specific beta-chymase, mouse mast cell protease-1. Blood. 1999;93:3473–3486
  24. Hatakeyama S, Hamasaki A, Negishi I, Loh DY, Sendo F, Nakayama K. Multiple gene duplication and expression of mouse bcl-2-related genes, A1. Int Immunol. 1998;10:631–637
  25. Verschelde C, Michonneau D, Trescol-Biemont MC, Berberich I, Schimpl A, Bonnefoy-Berard N. Overexpression of the antiapoptotic protein A1 promotes the survival of double positive thymocytes awaiting positive selection. Cell Death Differ. 2005;13:1213–1217
  26. Moller C, Xiang Z, Nilsson G. Activation of mast cells by immunoglobulin E-receptor cross-linkage, but not through adenosine receptors, induces A1 expression and promotes survival. Clin Exp Allergy. 2003;33:1135–1140
  27. Bullock ED, Johnson EM. Nerve growth factor induces the expression of certain cytokine genes and bcl-2 in mast cells. Potential role in survival promotion. J Biol Chem. 1996;271:27500–27508
  28. Yeatman CF, Jacobs-Helber SM, Mirmonsef P, et al. Combined stimulation with the T helper cell type 2 cytokines interleukin (IL)-4 and IL-10 induces mouse mast cell apoptosis. J Exp Med. 2000;192:1093–1103
  29. Gurish MF, Boyce JA. Mast cell growth, differentiation, and death. Clin Rev Allergy Immunol. 2002;22:107–118
  30. Kitamura Y, Go S. Decreased production of mast cells in S1/S1d anemic mice. Blood. 1979;53:492–497
  31. Kitamura Y, Go S, Hatanaka K. Decrease of mast cells in W/Wv mice and their increase by bone marrow transplantation. Blood. 1978;52:447–452
  32. Lantz CS, Boesiger J, Song CH, et al. Role for interleukin-3 in mast-cell and basophil development and in immunity to parasites. Nature. 1998;392:90–93
  33. Ody C, Kindler V, Vassalli P. Interleukin 3 perfusion in W/Wv mice allows the development of macroscopic hematopoietic spleen colonies and restores cutaneous mast cell number. J Exp Med. 1990;172:403–406
  34. Kohno M, Yamasaki S, Tybulewicz VL, Saito T. Rapid and large amount of autocrine IL-3 production is responsible for mast cell survival by IgE in the absence of antigen. Blood. 2005;105:2059–2065
  35. Karlsson R, Engstrom M, Jonsson M, et al. Phosphatidylinositol 3-kinase is essential for kit ligand-mediated survival, whereas interleukin-3 and flt3 ligand induce expression of antiapoptotic Bcl-2 family genes. J Leukoc Biol. 2003;74:923–931
  36. Domen J, Weissman IL. Hematopoietic stem cells need two signals to prevent apoptosis; BCL-2 can provide one of these, Kitl/c-Kit signaling the other. J Exp Med. 2000;192:1707–1718
  37. Shelburne CP, McCoy ME, Piekorz R, et al. Stat5 expression is critical for mast cell development and survival. Blood. 2003;102:1290–1297
  38. Xiang Z, Moller C, Nilsson G. IgE-receptor activation induces survival and Bfl-1 expression in human mast cells but not basophils. Allergy. 2006;61:1040–1046
  39. Yan W, Suominen J, Samson M, Jegou B, Toppari J. Involvement of Bcl-2 family proteins in germ cell apoptosis during testicular development in the rat and pro-survival effect of stem cell factor on germ cells in vitro. Mol Cell Endocrinol. 2000;165:115–129
  40. Alfredsson J, Moller C, Nilsson G. IgE-receptor activation of mast cells regulates phosphorylation and expression of forkhead and Bcl-2 family members. Scand J Immunol. 2006;63:1–6
  41. Blume-Jensen P, Janknecht R, Hunter T. The kit receptor promotes cell survival via activation of PI 3-kinase and subsequent Akt-mediated phosphorylation of Bad on Ser136. Curr Biol. 1998;8:779–782

PII: S0301-472X(06)00704-1

doi: 10.1016/j.exphem.2006.11.008

Experimental Hematology
Volume 35, Issue 3 , Pages 385-393 , March 2007

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