CD40 ligand protects from TRAIL-induced apoptosis in follicular lymphomas through NF-κB activation and up-regulation of c-FLIP and Bcl-xL

Journal of Immunology

Volumn 181, Issue 2, 2008, Pages 1001-1011

  Travert, Marion ^a   Ame Thomas, Patricia ^a,b   Pangault, Céline ^a,b   Morizot, Alexandre ^c   Micheau, Olivier ^c   Semana, Gilbert ^a,d   Lamy, Thierry ^a,b   Fest, Thierry ^a,b   Tarte, Karin ^a,b   Guillaudeux, Thierry ^a  

^a UNIVERSITÉ DE RENNES 1   (France)

^b PONTCHAILLOU UNIVERSITY HOSPITAL   (France)

^c UNIVERSITÉ DE BOURGOGNE   (France)

^d ETABLISSEMENT FRANÇAIS DU SANG   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BAY 117085; CASPASE 8; CD40 LIGAND; DEATH RECEPTOR 4; FLICE INHIBITORY PROTEIN; I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN BCL XL; RNA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG; 3 (4 TERT BUTYLPHENYLSULFONYL) 2 PROPENENITRILE; CD40 ANTIGEN; NITRILE; PROTEIN BCL X; RECOMBINANT PROTEIN; SULFONE; TNFRSF10A PROTEIN, HUMAN; TNFSF10 PROTEIN, HUMAN; TUMOR NECROSIS FACTOR RECEPTOR;

ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; B CELL LYMPHOMA; B LYMPHOCYTE; BURKITT LYMPHOMA; CANCER THERAPY; CD4+ T LYMPHOCYTE; CELL PROTECTION; CHILD; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG INHIBITION; ENZYME ACTIVATION; FOLLICULAR LYMPHOMA; GERMINAL CENTER; HUMAN; HUMAN CELL; MITOCHONDRION; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; T LYMPHOCYTE SUBPOPULATION; UPREGULATION; CELL CULTURE; DRUG EFFECT; IMMUNOLOGY; METABOLISM; PATHOLOGY; TONSIL; TUMOR CELL LINE;

ANTIGENS, CD40; APOPTOSIS; B-LYMPHOCYTES; BCL-X PROTEIN; CASP8 AND FADD-LIKE APOPTOSIS REGULATING PROTEIN; CASPASE 8; CD4-POSITIVE T-LYMPHOCYTES; CD40 LIGAND; CELL LINE, TUMOR; CELLS, CULTURED; HUMANS; LYMPHOMA, FOLLICULAR; NF-KAPPA B; NITRILES; RECEPTORS, TUMOR NECROSIS FACTOR; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; SULFONES; TNF-RELATED APOPTOSIS-INDUCING LIGAND; TONSIL; UP-REGULATION;

EID: 49049086995     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.2.1001     Document Type: Article

References (69)

1. Armitage, J. O., and D. D. Weisenburger. 1998. New approach to classifying non-Hodgkin's lymphomas: clinical features of the major histologic subtypes: Non-Hodgkin's Lymphoma Classification Project. J. Clin. Oncol. 16: 2780-2795.
2. The Non-Hodgkin's Lymphoma Classification Project. 1997. A clinical evaluation of the international lymphoma study group classification of non-Hodgkin's lymphoma. Blood 89: 3909-3918.
3. Society for Hematopathology Program. 1997. Society for hematopathology program. Am. J. Surg. Pathol. 21: 114-121.
4. Lopez-Guillermo, A., F. Cabanillas, T. I. McDonnell, P. McLaughlin, T. Smith, W. Pugh, F. Hagemeister, M. A. Rodriguez, J. E. Romaguera, A. Younes, et al. 1999. Correlation of Bcl-2 rearrangement with clinical characteristics and outcome in indolent follicular lymphoma. Blood 93: 3081-3087. (Pubitemid 29200801)
5. Dave, S. S., G. Wright, B. Tan, A. Rosenwald, R. D. Gascoyne, W. C. Chan, R. I. Fisher, R. M. Braziel, L. M. Rimsza, T. M. Grogan, et al. 2004. Prediction of survival in follicular lymphoma based on molecular features of tumor-infiltrating immune cells. N. Engl. J. Med. 351: 2159-2169.
6. Alvaro, T., M. Lejeune, M. T. Salvado, C. Lopez, J. Jaen, R. Bosch, and L. E. Pons. 2006. Immunohistochemical patterns of reactive microenvironment are associated with clinicobiologic behavior in follicular lymphoma patients. J. Clin. Oncol. 24: 5350-5357.
7. Vega, F., L. J. Medeiros, W.-H. Lang, A. Mansoor, C. Bueso-Ramos, and D. Jones. 2002. The stromal composition of malignant lymphoid aggregates in bone marrow: variations in architecture and phenotype in different B-cell tumours. Br. J. Haematol. 117: 569-576. (Pubitemid 34539230)
8. Johnson, P. W., S. M. Watt, D. R. Betts, D. Davies, S. Jordan, A. J. Norton, and T. A. Lister. 1993. Isolated follicular lymphoma cells are resistant to apoptosis and can be grown in vitro in the CD40/stromal cell system. Blood 82: 1848-1857.
9. Buske, C., A. Twinling, G. Gogowski, K. Schreiber, M. Feuring-Buske, G. Wulf, W. Hiddeman, and B. Wormann. 1997. In vitro activation of low-grade non- Hodgkin's lymphoma by murine fibroblasts, IL-4, anti-CD40 antibodies and the soluble CD40L. Leukemia 11: 1862-1867. (Pubitemid 27485131)
10. Ghia, P., V. A. Boussiotis, J. L. Schultze, A. A. Cardoso, D. M. Dorfman, J. G. Gribben, A. S. Freedman, and L. M. Nadler. 1998. Unbalanced expression of Bcl-2 family proteins in follicular lymphoma: contribution of CD40 signaling in promoting survival. Blood 91: 244-251. (Pubitemid 28018751)
11. Kehry, M. R. 1996. Commentary: CD40-mediated signaling in B cells: balancing cell survival, growth, and death. J. Immunol. 156: 2345-2348.
12. Gruss, H., F. Herrmann, V. Gattei, A. Gloghini, A. Pinto, and A. Carbone. 1997. CD40/CD40 ligand interactions in normal, reactive and malignant lympho-hematopoietic tissues. Leuk. Lymphoma 24: 393-422. (Pubitemid 27182198)
13. Choe, J., H. S. Kim, X. Zhang, R. J. Armitage, and Y. S. Choi. 1996. Cellular and molecular factors that regulate the differentiation and apoptosis of germinal center B cells: anti-Ig down-regulates Fas expression of CD40 ligand-stimulated germinal center B cells and inhibits Fas-mediated apoptosis. J. Immunol. 157: 1006-1016. (Pubitemid 126449613)
14. Choi, Y. S. 1997. Differentiation and apoptosis of human germinal center Blymphocytes. Immunol. Res. 16: 161-174. (Pubitemid 27294587)
15. Takahashi, Y., H. Ohta, and T. Takemori. 2001. Fas is required for clonal selection in germinal centers and the subsequent establishment of the memory B cell repertoire. Immunity 14: 181-192. (Pubitemid 32206520)
16. van Eijk, M., T. Defrance, A. Hennino, and C. de Groot. 2001. Death-receptor contribution to the germinal-center reaction. Trends Immunol. 22: 677-682.
17. Dallman, C., P. W. Johnson, and G. Packham. 2003. Differential regulation of cell survival by CD40. Apoptosis 8: 45-53. (Pubitemid 36133137)
18. Cleary, A. M., S. M. Fortune, M. J. Yellin, L. Chess, and S. Lederman. 1995. Opposing roles of CD95 (Fas/APO-1) and CD40 in the death and rescue of human low density tonsillar B cells. J. Immunol. 155: 3329-3337.
19. Metkar, S., K. Naresh, A. Redkar, and J. Nadkarni. 1998. CD40-ligation-mediated from apoptosis of a Fas-sensitive Hodgkin's-disease- derived cell line. Cancer Immunol. Immunother. 47: 104-112. (Pubitemid 28442709)
20. Zazzeroni, F., S. Papa, A. Algeciras-Schimnich, K. Alvarez, T. Melis, C. Bubici, N. Majewski, N. Hay, E. De Smaele, M. E. Peter, and G. Franzoso. 2003. Gadd45β mediates the protective effects of CD40 costimulation against Fasinduced apoptosis. Blood 102: 3270-3279. (Pubitemid 37314766)
21. Berberich, I., G. L. Shu, and E. A. Clark. 1994. Cross-linking CD40 on B cells rapidly activates nuclear factor-κB. J. Immunol. 153: 4357-4366. (Pubitemid 24346830)
22. Rothe, M., V. Sarma, V. M. Dixit, and D. V. Goeddel. 1995. TRAF2-mediated activation of NF-κB by TNF receptor 2 and CD40. Science 269: 1424-1427.
23. Liu, Y. J., D. E. Joshua, G. T. Williams, C. A. Smith, J. Gordon, and I. C. M. MacLennan. 1989. Mechanism of antigen-driven selection in germinal centres. Nature 342: 929-931.
24. Durie, F. H., T. M. Foy, S. R. Masters, J. D. Laman, and R. J. Noelle. 1994. The role of CD40 in the regulation of humoral and cell-mediated immunity. Immunol. Today 15: 406-411. (Pubitemid 24272184)
25. Lagresle, C., C. Bella, P. T. Daniel, P. H. Krammer, and T. Defrance. 1995. Regulation of germinal center B cell differentiation: role of the human APO-1/Fas (CD95) molecule. J. Immunol. 154: 5746-5756.
26. Kreuz, S., D. Siegmund, P. Scheurich, and H. Wajant. 2001. NF-κB inducers upregulate cFLIP, a cycloheximide-sensitive inhibitor of death receptor signaling. Mol. Cell. Biol. 21: 3964-3973. (Pubitemid 32476458)
27. Lee, H. H., H. Dadgostar, Q. Cheng, J. Shu, and G. Cheng. 1999. NF-κB-mediated up-regulation of Bcl-x and Bfl-1/A1 is required for CD40 survival signaling in B lymphocytes. Proc. Natl. Acad. Sci. USA 96: 9136-9141.
28. Krueger, A., I. Schmitz, S. Baumann, P. H. Krammer, and S. Kirchhoff. 2001. Cellular FLICE-inhibitory protein splice variants inhibit different steps of caspase-8 activation at the CD95 death-inducing signaling complex. J. Biol. Chem. 276: 20633-20640. (Pubitemid 37411151)
29. Scaffidi, C., I. Schmitz, P. H. Krammer, and M. E. Peter. 1999. The role of c-FLIP in modulation of CD95-induced apoptosis. J. Biol. Chem. 274: 1541-1548. (Pubitemid 129507745)
30. Bodmer, J.-L., N. Holler, S. Reynard, P. Vinciguerra, P. Schneider, P. Juo, J. Blenis, and J. Tschopp. 2000. TRAIL receptor-2 signals apoptosis through FADD and caspase-8. Nat. Cell Biol. 2: 241-243.
31. Sprick, M. R., M. A. Weigand, E. Rieser, C. T. Rauch, P. Juo, J. Blenis, P. H. Krammer, and H. Walczak. 2000. FADD/MORT1 and caspase-8 are recruited to TRAIL receptors 1 and 2 and are essential for apoptosis mediated by TRAIL receptor 2. Immunity 12: 599-609.
32. Walczak, H., R. E. Miller, K. Ariail, B. Gliniak, T. S. Griffith, M. Kubin, W. Chin, J. Jones, A. Woodward, T. Le, et al. 1999. Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo. Nat. Med. 5: 157-163. (Pubitemid 29068521)
33. Ashkenazi, A., R. C. Pai, S. Fong, S. Leung, D. A. Lawrence, S. A. Marsters, C. Blackie, L. Chang, A. E. McMurtrey, A. Hebert, et al. 1999. Safety and antitumor activity of recombinant soluble Apo2 ligand. J. Clin. Invest. 104: 155-162.
34. Srivastava, R. K. 2000. Intracellular mechanisms of TRAIL and its role in cancer therapy. Mol. Cell Biol. Res. Commun. 4: 67-75.
35. Werner, A. B., E. de Vries, S. W. G. Tait, I. Bontjer, and J. Borst. 2002. TRAIL receptor and CD95 signal to mitochondria via FADD, caspase-8/10, Bid, and Bax but differentially regulate events downstream from truncated bid. J. Biol. Chem. 277: 40760-40767.
36. Yee, L., M. Fanale, K. Dimick, S. Calvert, C. Robins, J. Ing, J. Ling, W. Novotny, A. Ashkenazi, and H. Burris. 2007. A phase IB safety and pharmacokinetic (PK) study of recombinant human Apo2L/TRAIL in combination with rituximab in patients with low-grade non-Hodgkin lymphoma. J. Clin. Oncol. 25: 8078.
37. Zerafa, N., J. A. Westwood, E. Cretney, S. Mitchell, P. Waring, M. Iezzi, and M. J. Smyth. 2005. Cutting edge: TRAIL deficiency accelerates hematological malignancies. J. Immunol. 175: 5586-5590. (Pubitemid 41508035)
38. Beg, A. A., and D. Baltimore. 1996. An essential role for NF-κB in preventing TNF-α-induced cell death. Science 274: 782-784.
39. Wang, C.-Y., M. W. Mayo, and A. S. Baldwin, Jr. 1996. TNF- and cancer therapy- induced apoptosis: potentiation by Inhibition of NF-κB. Science 274: 784-787.
40. Van Antwerp, D. J., S. J. Martin, T. Kafri, D. R. Green, and I. M. Verma. 1996. Suppression of TNF-α-induced apoptosis by NF-κB. Science 274: 787-789.
41. Liu, Z.-g., H. Hsu, D. V. Goeddel, and M. Karin. 1996. Dissection of TNF receptor 1 effector functions: JNK activation is not linked to apoptosis while NF-κB activation prevents cell death. Cell 87: 565-576.
42. Pear, W. S., J. P. Miller, L. Xu, J. C. Pui, B. Soffer, R. C. Quackenbush, A. M. Pendergast, R. Bronson, J. C. Aster, M. L. Scott, and D. Baltimore. 1998. Efficient and rapid induction of a chronic myelogenous leukemia-like myeloproliferative disease in mice receiving P210 bcr/abl-transduced bone marrow. Blood 92: 3780-3792.
43. L sequester BH3 domain-only molecules preventing BAX- and BAK-mediated mitochondrial apoptosis. Mol. Cell 8: 705-711.
44. Ghia, P., and F. Caligaris-Cappio. 2000. The indispensable role of microenvironment in the natural history of low-grade B-cell neoplasms. Adv. Cancer Res. 79: 157-173. (Pubitemid 30228123)
45. Ame-Thomas, P., H. Maby-El Hajjami, C. Monvoisin, R. Jean, D. Monnier, S. Caulet-Maugendre, T. Guillaudeux, T. Lamy, T. Fest, and K. Tarte. 2007. Human mesenchymal stem cells isolated from bone marrow and lymphoid organs support tumor B-cell growth: role of stromal cells in follicular lymphoma pathogenesis. Blood 109: 693-702. (Pubitemid 46105971)
46. Meurette, O., A. Rebillard, L. Huc, G. Le Moigne, D. Merino, O. Micheau, D. Lagadic-Gossmann, and M. T. Dimanche-Boitrel. 2007. TRAIL induces receptor- interacting protein 1-dependent and caspase-dependent necrosis-like cell death under acidic extracellular conditions. Cancer Res. 67: 218-226. (Pubitemid 46142778)
47. Wood, D. E., and E. W. Newcomb. 2000. Cleavage of bax enhances its cell death function. Exp. Cell Res. 256: 375-382.
48. Cao, X., X. Deng, and W. S. May. 2003. Cleavage of Bax to p18 Bax accelerates stress-induced apoptosis, and a cathepsin-like protease may rapidly degrade p18 Bax. Blood 102: 2605-2614. (Pubitemid 37193602)
49. Wood, D. E., A. Thomas, L. A. Devi, Y. Berman, R. C. Beavis, J. C. Reed, and E. W. Newcomb. 1998. Bax cleavage is mediated by calpain during drug-induced apoptosis. Oncogene 17: 1069-1078. (Pubitemid 28444591)
50. Wood, D. E., and E. W. Newcomb. 1999. Caspase-dependent activation of calpain during drug-induced apoptosis. J. Biol. Chem. 274: 8309-8315. (Pubitemid 129518231)
51. Taghiyev, A. F., N. V. Guseva, H. Harada, C. M. Knudson, O. W. Rokhlin, and M. B. Cohen. 2003. Overexpression of BAD potentiates sensitivity to tumor necrosis factor-related apoptosis-inducing ligand treatment in the prostatic carcinoma cell line LNCaP. Mol. Cancer Res. 1: 500-507.
52. Muhlethaler-Mottet, A., K. Balmas Bourloud, K. Auderset, J.-M. Joseph, and N. Gross. 2004. Drug-mediated sensitization to TRAIL-induced apoptosis in caspase-8-complemented neuroblastoma cells proceeds via activation of intrinsic and extrinsic pathways and caspase-dependent cleavage of XIAP, Bcl-xL and RIP. Oncogene 23: 5415-5425. (Pubitemid 39044052)
53. Mawji, I. A., C. D. Simpson, M. Gronda, M. A. Williams, R. Hurren, C. J. Henderson, A. Datti, J. L. Wrana, and A. D. Schimmer. 2007. A chemical screen identifies anisomycin as an anoikis sensitizer that functions by decreasing FLIP protein synthesis. Cancer Res. 67: 8307-8315.
54. MacFarlane, M., S. Inoue, S. L. Kohlhaas, A. Majid, N. Harper, D. B. J. Kennedy, M. J. S. Dyer, and G. M. Cohen. 2005. Chronic lymphocytic leukemic cells exhibit apoptotic signaling via TRAIL-R1. Cell. Death Differ. 12: 773-782. (Pubitemid 40945984)
55. MacFarlane, M., S. L. Kohlhaas, M. J. Sutcliffe, M. J. S. Dyer, and G. M. Cohen. 2005. TRAIL receptor-selective mutants signal to apoptosis via TRAIL-R1 in primary lymphoid malignancies. Cancer Res. 65: 11265-11270. (Pubitemid 41821680)
56. Merino, D., N. Lalaoui, A. Morizot, P. Schneider, E. Solary, and O. Micheau. 2006. Differential inhibition of TRAIL-mediated DR5-DISC formation by decoy receptors 1 and 2. Mol. Cell. Biol. 26: 7046-7055. (Pubitemid 44477684)
57. +CD4 germinal center Th cells. J. Immunol. 177: 4927-4932.
58. Bonizzi, G., and M. Karin. 2004. The two NF-κB activation pathways and their role in innate and adaptive immunity. Trends Immunol. 25: 280-288. (Pubitemid 38610351)
59. Tai, Y.-T., K. Podar, N. Mitsiades, B. Lin, C. Mitsiades, D. Gupta, M. Akiyama, L. Catley, T. Hideshima, N. C. Munshi, et al. 2003. CD40 induces human multiple myeloma cell migration via phosphatidylinositol 3-kinase/AKT/NF- κB signaling. Blood 101: 2762-2769.
60. Cuni, S., P. Perez-Aciego, G. Perez-Chacon, J. A. Vargas, A. Sanchez, F. M. Martin-Saavedra, S. Ballester, J. Garcia-Marco, J. Jorda, and A. Durantez. 2004. A sustained activation of PI3K/NF-κB pathway is critical for the survival of chronic lymphocytic leukemia B cells. Leukemia 18: 1391-1400. (Pubitemid 39136749)
61. Irmler, M., M. Thome, M. Hahne, P. Schneider, K. Hofmann, V. Steiner, J. L. Bodmer, M. Schroter, K. Burns, C. Mattmann, et al. 1997. Inhibition of death receptor signals by cellular FLIP. Nature 388: 190-195. (Pubitemid 27297457)
62. Bin, L., X. Li, L. G. Xu, and H. B. Shu. 2002. The short splice form of Casper/ c-FLIP is a major cellular inhibitor of TRAIL-induced apoptosis. FEBS Lett. 510: 37-40. (Pubitemid 34084880)
63. Eeva, J., A. Ropponen, U. Nuutinen, S. T. Eeva, M. Matto, M. Eray, and J. Pelkonen. 2007. The CD40-induced protection against CD95-mediated apoptosis is associated with a rapid upregulation of anti-apoptotic c-FLIP. Mol. Immunol. 44: 1230-1237. (Pubitemid 44415970)
64. Mathas, S., A. Lietz, I. Anagnostopoulos, F. Hummel, B. Wiesner, M. Janz, F. Jundt, B. Hirsch, K. Johrens-Leder, H. P. Vornlocher, et al. 2004. c-FLIP mediates resistance of Hodgkin/Reed-Sternberg cells to death receptor-induced apoptosis. J. Exp. Med. 199: 1041-1052. (Pubitemid 38619901)
65. +R upon CD40 stimulation is associated with inhibition of CD95-induced apoptosis in primary precursor B-ALL. Blood 110: 384-387.
66. L induction. Eur. J. Cancer 42: 3287-3293.
67. L. J. Biol. Chem. 282: 319-328.
68. Novak, A. J., D. M. Grote, M. Stenson, S. C. Ziesmer, T. E. Witzig, T. M. Habermann, B. Harder, K. M. Ristow, R. J. Bram, D. F. Jelinek, et al. 2004. Expression of BLyS and its receptors in B-cell non-Hodgkin lymphoma: correlation with disease activity and patient outcome. Blood 104: 2247-2253.
69. Tangye, S. G., V. L. Bryant, A. K. Cuss, and K. L. Good. 2006. BAFF, APRIL, and human B cell disorders. Semin. Immunol. 18: 305-317.