C-Rel deficiency increases caspase-4 expression and leads to ER stress and necrosis in EBV-transformed cells

PLoS ONE

Volumn 6, Issue 10, 2011, Pages

  Valentín Acevedo, Aníbal ^a   Sinquett, Frank L ^a   Covey, Lori R ^a  

^a RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 4; CD40 LIGAND; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOCORTIN 5; MYC PROTEIN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR REL; CASP4 PROTEIN, HUMAN; CD40 ANTIGEN; EBV ASSOCIATED MEMBRANE ANTIGEN, EPSTEIN BARR VIRUS; EBV-ASSOCIATED MEMBRANE ANTIGEN, EPSTEIN-BARR VIRUS; INITIATOR CASPASE; MATRIX PROTEIN;

APOPTOSIS; ARTICLE; AUTOPHAGY; CELL DEATH; CELL PROLIFERATION; CELL STRESS; CELL SURVIVAL; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; EPSTEIN BARR VIRUS; GENE CONTROL; GENE EXPRESSION PROFILING; HEMATOPOIETIC CELL; IN VITRO STUDY; NONHUMAN; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; RABBIT; VIRUS CELL TRANSFORMATION; CELL LINE; CELL SHAPE; ENDOPLASMIC RETICULUM; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; NECROSIS; PATHOLOGY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; SIGNAL TRANSDUCTION; ULTRASTRUCTURE;

HUMAN HERPESVIRUS 4;

ANTIGENS, CD40; AUTOPHAGY; CASPASES, INITIATOR; CELL LINE, TRANSFORMED; CELL PROLIFERATION; CELL SHAPE; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HERPESVIRUS 4, HUMAN; HUMANS; NECROSIS; PROTO-ONCOGENE PROTEINS C-MYC; PROTO-ONCOGENE PROTEINS C-REL; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; VIRAL MATRIX PROTEINS;

EID: 84856262667     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0025467     Document Type: Article

References (58)

1. Fan Y, Dutta J, Gupta N, Fan G, Gelinas C, (2008) Regulation of programmed cell death by NF-kappaB and its role in tumorigenesis and therapy. Adv Exp Med Biol 615: 223-250.
2. Purchase HG, Witter RL, (1975) The reticuloendotheliosis viruses. Curr Top Microbiol Immunol 71: 103-124.
3. Gilmore TD, Cormier C, Jean-Jacques J, Gapuzan ME, (2001) Malignant transformation of primary chicken spleen cells by human transcription factor c-Rel. Oncogene 20: 7098-7103.
4. Starczynowski DT, Reynolds JG, Gilmore TD, (2003) Deletion of either C-terminal transactivation subdomain enhances the in vitro transforming activity of human transcription factor REL in chicken spleen cells. Oncogene 22: 6928-6936.
5. Rosenwald A, Wright G, Chan WC, Connors JM, Campo E, et al. (2002) The use of molecular profiling to predict survival after chemotherapy for diffuse large-B-cell lymphoma. N Engl J Med 346: 1937-1947.
6. Houldsworth J, Mathew S, Rao PH, Dyomina K, Louie DC, et al. (1996) REL proto-oncogene is frequently amplified in extranodal diffuse large cell lymphoma. Blood 87: 25-29.
7. Barth TF, Bentz M, Leithauser F, Stilgenbauer S, Siebert R, et al. (2001) Molecular-cytogenetic comparison of mucosa-associated marginal zone B-cell lymphoma and large B-cell lymphoma arising in the gastro-intestinal tract. Genes Chromosomes Cancer 31: 316-325.
8. Savage KJ, Monti S, Kutok JL, Cattoretti G, Neuberg D, et al. (2003) The molecular signature of mediastinal large B-cell lymphoma differs from that of other diffuse large B-cell lymphomas and shares features with classical Hodgkin lymphoma. Blood 102: 3871-3879.
9. Tian W, Liou HC, (2009) RNAi-mediated c-Rel silencing leads to apoptosis of B cell tumor cells and suppresses antigenic immune response in vivo. PLoS One 4: e5028.
10. Liou HC, Sha WC, Scott ML, Baltimore D, (1994) Sequential induction of NF-kappa B/Rel family proteins during B-cell terminal differentiation. Mol Cell Biol 14: 5349-5359.
11. Bottero V, Withoff S, Verma IM, (2006) NF-kappaB and the regulation of hematopoiesis. Cell Death Differ 13: 785-797.
12. Miyamoto S, Verma IM, (1995) Rel/NF-kappa B/I kappa B story. Adv Cancer Res 66: 255-292.
13. Weih F, Carrasco D, Bravo R, (1994) Constitutive and inducible Rel/NF-kappa B activities in mouse thymus and spleen. Oncogene 9: 3289-3297.
14. Kontgen F, Grumont RJ, Strasser A, Metcalf D, Li R, et al. (1995) Mice lacking the c-rel proto-oncogene exhibit defects in lymphocyte proliferation, humoral immunity, and interleukin-2 expression. Genes Dev 9: 1965-1977.
15. Tumang JR, Owyang A, Andjelic S, Jin Z, Hardy RR, et al. (1998) c-Rel is essential for B lymphocyte survival and cell cycle progression. Eur J Immunol 28: 4299-4312.
16. Hsia CY, Cheng S, Owyang AM, Dowdy SF, Liou HC, (2002) c-Rel regulation of the cell cycle in primary mouse B lymphocytes. Int Immunol 14: 905-916.
17. Cheng S, Hsia CY, Leone G, Liou HC, (2003) Cyclin E and Bcl-xL cooperatively induce cell cycle progression in c-Rel-/- B cells. Oncogene 22: 8472-8486.
18. Andjelic S, Hsia C, Suzuki H, Kadowaki T, Koyasu S, et al. (2000) Phosphatidylinositol 3-kinase and NF-kappa B/Rel are at the divergence of CD40-mediated proliferation and survival pathways. J Immunol 165: 3860-3867.
19. Lee HH, Dadgostar H, Cheng Q, Shu J, Cheng G, (1999) NF-kappa B-mediated up-regulation of Bcl-x and Bfl-1/A1 is required for CD40 survival signaling in B lymphocytes. PNAS 96: 9136-9141.
20. Owyang AM, Tumang JR, Schram BR, Hsia CY, Behrens TW, et al. (2001) c-Rel is required for the protection of B cells from antigen receptor-mediated, but not Fas-mediated, apoptosis. J Immunol 167: 4948-4956.
21. Zong WX, Edelstein LC, Chen C, Bash J, Gelinas C, (1999) The prosurvival Bcl-2 homolog Bfl-1/A1 is a direct transcriptional target of NF-kappaB that blocks TNFalpha-induced apoptosis. Genes Dev 13: 382-387.
22. Grumont RJ, Strasser A, Gerondakis S, (2002) B cell growth is controlled by phosphatidylinosotol 3-kinase-dependent induction of Rel/NF-kappaB regulated c-myc transcription. Mol Cell 10: 1283-1294.
23. Okkenhaug K, Vanhaesebroeck B, (2003) PI3K in lymphocyte development, differentiation and activation. Nat Rev Immunol 3: 317-330.
24. Suzuki H, Matsuda S, Terauchi Y, Fujiwara M, Ohteki T, et al. (2003) PI3K and Btk differentially regulate B cell antigen receptor-mediated signal transduction. Nat Immunol 4: 280-286.
25. Xue L, Morris SW, Orihuela C, Tuomanen E, Cui X, et al. (2003) Defective development and function of Bcl10-deficient follicular, marginal zone and B1 B cells. Nat Immunol 4: 857-865.
26. Jun JE, Wilson LE, Vinuesa CG, Lesage S, Blery M, et al. (2003) Identifying the MAGUK protein Carma-1 as a central regulator of humoral immune responses and atopy by genome-wide mouse mutagenesis. Immunity 18: 751-762.
27. Newton K, Dixit VM, (2003) Mice lacking the CARD of CARMA1 exhibit defective B lymphocyte development and impaired proliferation of their B and T lymphocytes. Curr Biol 13: 1247-1251.
28. Moscat J, Diaz-Meco MT, Rennert P, (2003) NF-kappaB activation by protein kinase C isoforms and B-cell function. EMBO Rep 4: 31-36.
29. Gilmore TD, Kalaitzidis D, Liang MC, Starczynowski DT, (2004) The c-Rel transcription factor and B-cell proliferation: a deal with the devil. Oncogene 23: 2275-2286.
30. Bhushan A, Barnhart B, Shone S, Song C, Covey LR, (2000) A transcriptional defect underlies B lymphocyte dysfunction in a patient diagnosed with non-X-linked hyper-IgM syndrome. J Immunol 164: 2871-2880.
31. Kilger E, Kieser A, Baumann M, Hammerschmidt W, (1998) Epstein-Barr virus-mediated B-cell proliferation is dependent upon latent membrane protein 1, which simulates an activated CD40 receptor. Embo J 17: 1700-1709.
32. Lu KT, Sinquett FL, Dryer RL, Song C, Covey LR, (2006) c-Rel plays a key role in deficient activation of B cells from a non-X-linked hyper-IgM patient. Blood 108: 3769-3776.
33. Grumont R, Lock P, Mollinari M, Shannon FM, Moore A, et al. (2004) The mitogen-induced increase in T cell size involves PKC and NFAT activation of Rel/NF-kappaB-dependent c-myc expression. Immunity 21: 19-30.
34. de Alboran IM, O'Hagan RC, Gartner F, Malynn B, Davidson L, et al. (2001) Analysis of C-MYC function in normal cells via conditional gene-targeted mutation. Immunity 14: 45-55.
35. Bhatia S, Kaul D, Varma N, (2010) Potential tumor suppressive function of miR-196b in B-cell lineage acute lymphoblastic leukemia. Mol Cell Biochem 340: 97-106.
36. Luoto KR, Meng AX, Wasylishen AR, Zhao H, Coackley CL, et al. (2010) Tumor cell kill by c-MYC depletion: role of MYC-regulated genes that control DNA double-strand break repair. Cancer Res 70: 8748-8759.
37. Soucek L, Whitfield J, Martins CP, Finch AJ, Murphy DJ, et al. (2008) Modelling Myc inhibition as a cancer therapy. Nature 455: 679-683.
38. Wang H, Mannava S, Grachtchouk V, Zhuang D, Soengas MS, et al. (2008) c-Myc depletion inhibits proliferation of human tumor cells at various stages of the cell cycle. Oncogene 27: 1905-1915.
39. Darzynkiewicz Z, Pozarowski P, Lee BW, Johnson GL, (2011) Fluorochrome-labeled inhibitors of caspases: convenient in vitro and in vivo markers of apoptotic cells for cytometric analysis. Methods Mol Biol 682: 103-114.
40. Rabinowitz JD, White E, (2010) Autophagy and metabolism. Science 330: 1344-1348.
41. White E, (2008) Autophagic cell death unraveled: Pharmacological inhibition of apoptosis and autophagy enables necrosis. Autophagy 4: 399-401.
42. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, et al. (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 19: 5720-5728.
43. Tanida I, Ueno T, Kominami E, (2004) Human light chain 3/MAP1LC3B is cleaved at its carboxyl-terminal Met121 to expose Gly120 for lipidation and targeting to autophagosomal membranes. J Biol Chem 279: 47704-47710.
44. Chan MA, Stein LD, Dosch HM, Sigal NH, (1986) Heterogeneity of EBV-transformable human B lymphocyte populations. J Immunol 136: 106-112.
45. Hibi T, Chan MA, Petsche D, Dosch HM, (1986) Phenotype, frequency, and EBV responsiveness of human marrow B and pre-B cells. J Immunol 136: 3211-3218.
46. Martinon F, Tschopp J, (2007) Inflammatory caspases and inflammasomes: master switches of inflammation. Cell Death Differ 14: 10-22.
47. Hitomi J, Katayama T, Eguchi Y, Kudo T, Taniguchi M, et al. (2004) Involvement of caspase-4 in endoplasmic reticulum stress-induced apoptosis and Abeta-induced cell death. J Cell Biol 165: 347-356.
48. Pelletier N, Casamayor-Palleja M, De Luca K, Mondiere P, Saltel F, et al. (2006) The endoplasmic reticulum is a key component of the plasma cell death pathway. J Immunol 176: 1340-1347.
49. Oh SH, Lim SC, (2009) Endoplasmic reticulum stress-mediated autophagy/apoptosis induced by capsaicin (8-methyl-N-vanillyl-6-nonenamide) and dihydrocapsaicin is regulated by the extent of c-Jun NH2-terminal kinase/extracellular signal-regulated kinase activation in WI38 lung epithelial fibroblast cells. J Pharmacol Exp Ther 329: 112-122.
50. Feuillard J, Schuhmacher M, Kohanna S, Asso-Bonnet M, Ledeur F, et al. (2000) Inducible loss of NF-kappaB activity is associated with apoptosis and Bcl-2 down-regulation in Epstein-Barr virus-transformed B lymphocytes. Blood 95: 2068-2075.
51. Cahir-McFarland ED, Davidson DM, Schauer SL, Duong J, Kieff E, (2000) NF-kappa B inhibition causes spontaneous apoptosis in Epstein-Barr virus-transformed lymphoblastoid cells. Proc Natl Acad Sci U S A 97: 6055-6060.
52. Paoluzzi L, O'Connor OA, (2010) Targeting survival pathways in lymphoma. Adv Exp Med Biol 687: 79-96.
53. Dirmeier U, Hoffmann R, Kilger E, Schultheiss U, Briseno C, et al. (2005) Latent membrane protein 1 of Epstein-Barr virus coordinately regulates proliferation with control of apoptosis. Oncogene 24: 1711-1717.
54. Cahir-McFarland ED, Carter K, Rosenwald A, Giltnane JM, Henrickson SE, et al. (2004) Role of NF-kappa B in cell survival and transcription of latent membrane protein 1-expressing or Epstein-Barr virus latency III-infected cells. J Virol 78: 4108-4119.
55. Nakagawa T, Zhu H, Morishima N, Li E, Xu J, et al. (2000) Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 403: 98-103.
56. Walsh CM, Edinger AL, (2010) The complex interplay between autophagy, apoptosis, and necrotic signals promotes T-cell homeostasis. Immunol Rev 236: 95-109.
57. Mathew R, Karp CM, Beaudoin B, Vuong N, Chen G, et al. (2009) Autophagy suppresses tumorigenesis through elimination of p62. Cell 137: 1062-1075.
58. Lu KT, Dryer RL, Song C, Covey LR, (2005) Maintenance of the CD40-related immunodeficient response in hyper-IgM B cells immortalized with a LMP1-regulated mini-EBV. J Leukoc Biol 78: 620-629.