International Journal of Hematology

, Volume 91, Issue 5, pp 808–819 | Cite as

Differential effects of BAFF on B cell precursor acute lymphoblastic leukemia and Burkitt lymphoma

  • Keiko Onda
  • Kazutoshi Iijima
  • Yohko U. Katagiri
  • Hajime Okita
  • Masahiro Saito
  • Toshiaki Shimizu
  • Nobutaka Kiyokawa
Original Article

Abstract

B cell-activating factor belonging to the tumor necrosis factor superfamily (BAFF) is a crucial factor for B cell development and is involved in the survival of malignant B cells, but its effect on B cell precursors (BCPs) remains unclear. We investigated BCP acute lymphoblastic leukemia (-ALL) cells for BAFF receptor (-R) expression and compared the effect of BAFF on BCP-ALL cells and Burkitt lymphoma (BL) cells. Expression of BAFF-R was detected in some cell lines and some clinical specimens of both BL and BCP-ALL. BAFF acted on both BL and BCP-ALL cells and promoted proliferation by both. BAFF also inhibited apoptosis by BL cells induced by cross-linking of cell surface molecules and anticancer drugs, but failed to inhibit apoptosis by BCP-ALL cells. BAFF induced prompt and obvious activation of the NF-κB signaling pathway in BL cells, but only weak and delayed activation of the pathway in BCP-ALL cells. The results of this study indicate that some BCP-ALL cells and some BL cells express BAFF-R, but that the effects of BAFF on BCP-ALL cells are different from its effects on mature B cell malignancies.

Keywords

BAFF B cell precursor ALL Burkitt lymphoma Apoptosis 

Notes

Acknowledgments

We thank Dr. K. J. Mori and Dr. Y. Matsuo for the gift of murine BM stromal cell line MS-5 and BL/BCP-ALL cell lines, respectively. We also thank Ms. H. Kiyokawa for her assistance in preparing the manuscript. This work was supported by a grant from the Japan Health Sciences Foundation for Research on Publicly Essential Drugs and Medical Devices (KHA1004), Health and Labour Sciences Research Grants (the 3rd-term comprehensive 10-year-strategy for cancer control H19-010), and a Grant for Child Health and Development from the Ministry of Health, Labour and Welfare of Japan.

Conflict of interest statement

We have no financial relationships or conflicts of interest related to this manuscript.

References

  1. 1.
    Mackay F, Silveira PA, Brink R. B cells and the BAFF/APRIL axis: fast-forward on autoimmunity and signaling. Curr Opin Immunol. 2007;19:327–36.CrossRefPubMedGoogle Scholar
  2. 2.
    Schneider P, MacKay F, Steiner V, et al. BAFF, a novel ligand of the tumor necrosis factor family, stimulates B cell growth. J Exp Med. 1999;189:1747–56.CrossRefPubMedGoogle Scholar
  3. 3.
    Shu HB, Hu WH, Johnson H. TALL-1 is a novel member of the TNF family that is down-regulated by mitogens. J Leukoc Biol. 1999;65:680–3.PubMedGoogle Scholar
  4. 4.
    Mukhopadhyay A, Ni J, Zhai Y, Yu GL, Aggarwal BB. Identification and characterization of a novel cytokine, THANK, a TNF homologue that activates apoptosis, nuclear factor-κB, and c-Jun NH2-terminal kinase. J Biol Chem. 1999;274:15978–81.CrossRefPubMedGoogle Scholar
  5. 5.
    Moore PA, Belvedere O, Orr A, et al. BLyS: member of the tumor necrosis factor family and B lymphocyte stimulator. Science. 1999;285:260–3.CrossRefPubMedGoogle Scholar
  6. 6.
    Gross JA, Johnston J, Mudri S, et al. TACI and BCMA are receptors for a TNF homologue implicated in B-cell autoimmune disease. Nature. 2000;404:995–9.CrossRefPubMedGoogle Scholar
  7. 7.
    Mackay F, Woodcock SA, Lawton P, et al. Mice transgenic for BAFF develop lymphocytic disorders along with autoimmune manifestations. J Exp Med. 1999;190:1697–710.CrossRefPubMedGoogle Scholar
  8. 8.
    Khare SD, Sarosi I, Xia XZ, et al. Severe B cell hyperplasia and autoimmune disease in TALL-1 transgenic mice. Proc Natl Acad Sci USA. 2000;97:3370–5.CrossRefPubMedGoogle Scholar
  9. 9.
    Schiemann B, Gommerman JL, Vora K, et al. An essential role for BAFF in the normal development of B cells through a BCMA-independent pathway. Science. 2001;293:2111–4.CrossRefPubMedGoogle Scholar
  10. 10.
    Gross JA, Dillon SR, Mudri S, et al. TACI-Ig neutralizes molecules critical for B cell development and autoimmune disease. Impaired B cell maturation in mice lacking BLyS. Immunity. 2001;15:289–302.CrossRefPubMedGoogle Scholar
  11. 11.
    Vora KA, Wang LC, Rao SP, et al. Cutting edge: germinal centers formed in the absence of B cell-activating factor belonging to the TNF family exhibit impaired maturation and function. J Immunol. 2003;171:547–51.PubMedGoogle Scholar
  12. 12.
    Schneider P. The role of APRIL and BAFF in lymphocyte activation. Curr Opin Immunol. 2005;17:282–9.CrossRefPubMedGoogle Scholar
  13. 13.
    Thompson JS, Schneider P, Kalled SL, et al. BAFF binds to the tumor necrosis factor receptor-like molecule B cell maturation antigen and is important for maintaining the peripheral B cell population. J Exp Med. 2000;192:129–35.CrossRefPubMedGoogle Scholar
  14. 14.
    Xia XZ, Treanor J, Senaldi G, et al. TACI is a TRAF-interacting receptor for TALL-1, a tumor necrosis factor family member involved in B cell regulation. J Exp Med. 2000;192:137–43.CrossRefPubMedGoogle Scholar
  15. 15.
    Marsters SA, Yan M, Pitti RM, Haas PE, Dixit VM, Ashkenazi A. Interaction of the TNF homologues BLyS and APRIL with the TNFreceptor homologues BCMA and TACI. Curr Biol. 2000;10:785–8.CrossRefPubMedGoogle Scholar
  16. 16.
    Shu HB, Johnson H. B cell maturation protein is a receptor for the tumor necrosis factor family member TALL-1. Proc Natl Acad Sci USA. 2000;97:9156–61.CrossRefPubMedGoogle Scholar
  17. 17.
    Wu Y, Bressette D, Carrell JA, et al. Tumor necrosis factor (TNF) receptor superfamily member TACI is a high affinity receptor for TNF family members APRIL and BLyS. J Biol Chem. 2000;275:35478–85.CrossRefPubMedGoogle Scholar
  18. 18.
    Thompson JS, Bixler SA, Qian F, et al. BAFF-R, a newly identified TNF receptor that specifically interacts with BAFF. Science. 2001;293:2108–11.CrossRefPubMedGoogle Scholar
  19. 19.
    Gras MP, Laabi Y, Linares-Cruz G, et al. BCMAp: an integral membrane protein in the Golgi apparatus of human mature B lymphocytes. Int Immunol. 1995;7:1093–106.CrossRefPubMedGoogle Scholar
  20. 20.
    Kayagaki N, Yan M, Seshasayee D, et al. BAFF/BLyS receptor 3 binds the B cell survival factor BAFF ligand through a discrete surface loop and promotes processing of NF-kB2. Immunity. 2002;10:515–24.CrossRefGoogle Scholar
  21. 21.
    Haiat S, Billard C, Quiney C, Ajchenbaum-Cymbalista F, Kolb JP. Role of BAFF and APRIL in human B-cell chronic lymphocytic leukaemia. Immunology. 2006;118:281–92.CrossRefPubMedGoogle Scholar
  22. 22.
    Novak AJ, Darce JR, Arendt BK, et al. Expression of BCMA, TACI, and BAFF-R in multiple myeloma: a mechanism for growth and survival. Blood. 2004;103:689–94.CrossRefPubMedGoogle Scholar
  23. 23.
    Moreaux J, Legouffe E, Jourdan E, et al. BAFF and APRIL protect myeloma cells from apoptosis induced by interleukin 6 deprivation and dexamethasone. Blood. 2004;103:3148–57.CrossRefPubMedGoogle Scholar
  24. 24.
    Chiu A, Xu W, He B, Dillon SR, et al. Hodgkin lymphoma cells express TACI and BCMA receptors and generate survival and proliferation signals in response to BAFF and APRIL. Blood. 2007;109:729–39.CrossRefPubMedGoogle Scholar
  25. 25.
    Novak AJ, Grote DM, Stenson M, et al. Expression of BLyS and its receptors in B-cell non-Hodgkin lymphoma: correlation with disease activity and patient outcome. Blood. 2004;104:2247–53.CrossRefPubMedGoogle Scholar
  26. 26.
    Rodig SJ, Shahsafaei A, Li B, Mackay CR, Dorfman DM. BAFF-R, the major B cell-activating factor receptor, is expressed on most mature B cells and B-cell lymphoproliferative disorders. Hum Pathol. 2005;36:1113–9.CrossRefPubMedGoogle Scholar
  27. 27.
    Wada K, Maeda K, Tajima K, Kato T, Kobata T, Yamakawa M. Expression of BAFF-R and TACI in reactive lymphoid tissues and B-cell lymphomas. Histopathology. 2009;54:221–32.CrossRefPubMedGoogle Scholar
  28. 28.
    Smith SH, Cancro MP. Cutting edge: B cell receptor signals regulate BLyS receptor levels in mature B cells and their immediate progenitors. J Immunol. 2003;170:5820–3.PubMedGoogle Scholar
  29. 29.
    Suzuki T, Kiyokawa N, Taguchi T, Sekino T, Katagiri YU, Fujimoto J. CD24 induces apoptosis in human B cells via the glycolipid-enriched membrane domains/rafts-mediated signaling system. J Immunol. 2001;166:5567–77.PubMedGoogle Scholar
  30. 30.
    Taguchi T, Takenouchi H, Matsui J, et al. Involvement of insulin-like growth factor-I and insulin-like growth factor binding proteins in pro-B-cell development. Exp Hematol. 2006;34:508–18.CrossRefPubMedGoogle Scholar
  31. 31.
    Kiyokawa N, Kokai Y, Ishimoto K, Fujita H, Fujimoto J, Hata JI. Characterization of the common acute lymphoblastic leukaemia antigen (CD10) as an activation molecule on mature human B cells. Clin Exp Immunol. 1990;79:322–7.PubMedCrossRefGoogle Scholar
  32. 32.
    Saito M, Kiyokawa N, Taguchi T, et al. Granulocyte colony-stimulating factor directly affects human monocytes and modulates cytokine secretion. Exp Hematol. 2002;30:1115–23.CrossRefPubMedGoogle Scholar
  33. 33.
    Kiyokawa N, Lee EK, Karunagaran D, Lin SY, Hung MC. Mitosis-specific negative regulation of epidermal growth factor receptor, triggered by a decrease in ligand binding and dimerization, can be overcome by overexpression of receptor. J Biol Chem. 1997;272:18656–65.CrossRefPubMedGoogle Scholar
  34. 34.
    Chaouchi N, Vazquez A, Galanaud P, Leprince C. B cell antigen receptor-mediated apoptosis. Importance of accessory molecules CD19 and CD22, and of surface IgM crosslinking. J Immunol. 1995;154:3096–104.PubMedGoogle Scholar
  35. 35.
    Shan D, Ledbetter JA, Press OW. Apoptosis of malignant human B cells by ligation of CD20 with monoclonal antibodies. Blood. 1998;91:1644–52.PubMedGoogle Scholar
  36. 36.
    Mimori K, Kiyokawa N, Taguchi T, et al. Costimulatory signals distinctively affect CD20- and B-cell-antigen-receptor-mediated apoptosis in Burkitt’s lymphoma/leukemia cells. Leukemia. 2003;17:1164–74.CrossRefPubMedGoogle Scholar
  37. 37.
    He B, Chadburn A, Jou E, Schattner EJ, Knowles DM, Cerutti A. Lymphoma B cells evade apoptosis through the TNF family members BAFF/BLyS and APRIL. J Immunol. 2004;172:3268–79.PubMedGoogle Scholar
  38. 38.
    Ogden CA, Pound JD, Batth BK, et al. Enhanced apoptotic cell clearance capacity and B cell survival factor production by IL-10-activated macrophages: implications for Burkitt’s lymphoma. J Immunol. 2005;174:3015–23.PubMedGoogle Scholar
  39. 39.
    Taguchi T, Kiyokawa N, Mimori K, et al. Pre-B cell antigen receptor-mediated signal inhibits CD24-induced apoptosis in human pre-B cells. J Immunol. 2003;170:252–60.PubMedGoogle Scholar
  40. 40.
    Saito Y, Miyagawa Y, Onda K, et al. B-cell-activating factor inhibits CD20-mediated and B-cell receptor-mediated apoptosis in human B cells. Immunology. 2008;125:570–90.CrossRefPubMedGoogle Scholar
  41. 41.
    Kim SJ, Lee SJ, Choi IY, et al. Serum BAFF predicts prognosis better than APRIL in diffuse large B-cell lymphoma patients treated with rituximab plus CHOP chemotherapy. Eur J Haematol. 2008;81:177–84.CrossRefPubMedGoogle Scholar

Copyright information

© The Japanese Society of Hematology 2010

Authors and Affiliations

  • Keiko Onda
    • 1
    • 2
  • Kazutoshi Iijima
    • 1
  • Yohko U. Katagiri
    • 1
  • Hajime Okita
    • 1
  • Masahiro Saito
    • 1
    • 2
  • Toshiaki Shimizu
    • 2
  • Nobutaka Kiyokawa
    • 1
  1. 1.Department of Pediatric Hematology and Oncology ResearchNational Research Institute for Child Health and DevelopmentTokyoJapan
  2. 2.Department of PediatricsJuntendo University, School of MedicineTokyoJapan

Personalised recommendations