Bcl-xL protein protects from C/EBP homologous protein (CHOP)-dependent apoptosis during plasma cell differentiation

Journal of Biological Chemistry

Volumn 289, Issue 34, 2014, Pages 23629-23640

  Gaudette, Brian T ^a   Iwakoshi, Neal N ^b   Boise, Lawrence H ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; CELL DEATH; CHEMICAL ACTIVATION;

APOPTOTIC; CELL LINES; HOMOLOGOUS PROTEINS; INDUCED APOPTOSIS; PLASMA CELL DIFFERENTIATION; STRESS-INDUCED; TUNICAMYCIN; UNFOLDED PROTEIN RESPONSE;

PROTEINS;

4 [4 (4' CHLORO 2 BIPHENYLYLMETHYL) 1 PIPERAZINYL] N [4 [3 DIMETHYLAMINO 1 (PHENYLTHIOMETHYL)PROPYLAMINO] 3 NITROBENZENESULFONYL]BENZAMIDE; BIM PROTEIN; CCAAT ENHANCER BINDING PROTEIN; INTERLEUKIN 5; LIPOPOLYSACCHARIDE; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN MCL 1; TUNICAMYCIN; ABT-737; BCL2L1 PROTEIN, MOUSE; BIPHENYL DERIVATIVE; DDIT3 PROTEIN, MOUSE; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; NITROPHENOL; PIPERAZINE DERIVATIVE; PRIMER DNA; PROTEIN BCL X; SULFONAMIDE;

ANIMAL CELL; APOPTOSIS; ARTICLE; B LYMPHOCYTE; CELL DEATH; CELL DIFFERENTIATION; CELL SURVIVAL; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; IN VITRO STUDY; INTRACELLULAR SIGNALING; LYMPHOCYTE ACTIVATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE; ANIMAL; C57BL MOUSE; CELL LINE; CYTOLOGY; DRUG EFFECTS; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE SILENCING; GENETICS; PHYSIOLOGY;

ANIMALS; APOPTOSIS; BASE SEQUENCE; BCL-X PROTEIN; BIPHENYL COMPOUNDS; CELL DIFFERENTIATION; CELL LINE; DNA PRIMERS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE SILENCING; INTERLEUKIN-5; LIPOPOLYSACCHARIDES; MICE; MICE, INBRED C57BL; NITROPHENOLS; PIPERAZINES; PLASMA CELLS; SULFONAMIDES; TRANSCRIPTION FACTOR CHOP; UNFOLDED PROTEIN RESPONSE;

EID: 84906569010     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.569376     Document Type: Article

References (41)

1. Gass, J. N., Gunn, K. E., Sriburi, R., and Brewer, J. W. (2004) Stressed-out B cells? Plasma-cell differentiation and the unfolded protein response. Trends Immunol. 25, 17-24
2. Gass, J. N., Gifford, N. M., and Brewer, J. W. (2002) Activation of an unfolded protein response during differentiation of antibody-secreting B cells. J. Biol. Chem. 277, 49047-49054
3. Schröder, M., and Kaufman, R. J. (2005) ER stress and the unfolded protein response. Mutat. Res. 569, 29-63
4. Yoshida, H., Haze, K., Yanagi, H., Yura, T., and Mori, K. (1998) Identification of the cis-Acting endoplasmic reticulum stress response element responsible for transcriptional induction of mammalian glucose-regulated proteins: involvement of basic leucine zipper transcription factors. J. Biol. Chem. 273, 33741-33749
5. Haze, K., Yoshida, H., Yanagi, H., Yura, T., and Mori, K. (1999) Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol. Biol. Cell 10, 3787-3799
6. Shen, J., Chen, X., Hendershot, L., and Prywes, R. (2002) ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev Cell 3, 99-111
7. Kokame, K., Kato, H., and Miyata, T. (2001) Identification of ERSE-II, a new cis-Acting element responsible for the ATF6-dependent mammalian unfolded protein response. J. Biol. Chem. 276, 9199-9205
8. Yoshida, H., Okada, T., Haze, K., Yanagi, H., Yura, T., Negishi, M., and Mori, K. (2001) Endoplasmic reticulum stress-induced formation of transcription factor complex ERSF including NF-Y (CBF) and activating transcription factors 6α and 6β that activates the mammalian unfolded protein response. Mol. Cell. Biol. 21, 1239-1248
9. Shamu, C. E., and Walter, P. (1996) Oligomerization and phosphorylation of the Ire1p kinase during intracellular signaling from the endoplasmic reticulum to the nucleus. EMBO J. 15, 3028-3039
10. Bertolotti, A., Zhang, Y., Hendershot, L. M., Harding, H. P., and Ron, D. (2000) Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat. Cell Biol. 2, 326-332
11. Liu, C. Y., Xu, Z., and Kaufman, R. J. (2003) Structure and intermolecular interactions of the luminal dimerization domain of human IRE1α. J. Biol. Chem. 278, 17680-17687
12. Sidrauski, C., and Walter, P. (1997) The transmembrane kinase Ire1p is a site-specific endonuclease that initiates mRNA splicing in the unfolded protein response. Cell 90, 1031-1039
13. Calfon, M., Zeng, H., Urano, F., Till, J. H., Hubbard, S. R., Harding, H. P., Clark, S. G., and Ron, D. (2002) IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415, 92-96
14. Clauss, I. M., Chu, M., Zhao, J. L., and Glimcher, L. H. (1996) The basic domain/leucine zipper protein hXBP-1 preferentially binds to and transactivates CRE-like sequences containing an ACGT core. Nucleic Acids Res. 24, 1855-1864
15. Lee, A. H., Iwakoshi, N. N., and Glimcher, L. H. (2003) XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol. Cell. Biol. 23, 7448-7459
16. Harding, H. P., Zhang, Y., and Ron, D. (1999) Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397, 271-274
17. Harding, H. P., Novoa, I., Zhang, Y., Zeng, H., Wek, R., Schapira, M., and Ron, D. (2000) Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell 6, 1099-1108
18. Ma, Y., Brewer, J. W., Diehl, J. A., and Hendershot, L. M. (2002) Two distinct stress signaling pathways converge upon the CHOP promoter during the mammalian unfolded protein response. J. Mol. Biol. 318, 1351-1365
19. Jiang, H. Y., Wek, S. A., McGrath, B. C., Lu, D., Hai, T., Harding, H. P., Wang, X., Ron, D., Cavener, D. R., and Wek, R. C. (2004) Activating transcription factor 3 is integral to the eukaryotic initiation factor 2 kinase stress response. Mol. Cell. Biol. 24, 1365-1377
20. McCullough, K. D., Martindale, J. L., Klotz, L. O., Aw, T. Y., and Holbrook, N. J. (2001) Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol. Cell. Biol. 21, 1249-1259
21. Puthalakath, H., O'Reilly, L. A., Gunn, P., Lee, L., Kelly, P. N., Huntington, N. D., Hughes, P. D., Michalak, E. M., McKimm-Breschkin, J., Motoyama, N., Gotoh, T., Akira, S., Bouillet, P., and Strasser, A. (2007) ER stress triggers apoptosis by activating BH3-only protein Bim. Cell 129, 1337-1349
22. Reimold, A. M., Iwakoshi, N. N., Manis, J., Vallabhajosyula, P., Szomolanyi- Tsuda, E., Gravallese, E. M., Friend, D., Grusby, M. J., Alt, F., and Glimcher, L. H. (2001) Plasma cell differentiation requires the transcription factor XBP-1. Nature 412, 300-307
23. Gunn, K. E., Gifford, N. M., Mori, K., and Brewer, J. W. (2004) A role for the unfolded protein response in optimizing antibody secretion. Mol. Immunol. 41, 919-927
24. Lee, K., Tirasophon, W., Shen, X., Michalak, M., Prywes, R., Okada, T., Yoshida, H., Mori, K., and Kaufman, R. J. (2002) IRE1-mediated unconventional mRNA splicing and S2P-mediated ATF6 cleavage merge to regulate XBP1 in signaling the unfolded protein response. Genes Dev. 16, 452-466
25. Gass, J. N., Jiang, H. Y., Wek, R. C., and Brewer, J. W. (2008) The unfolded protein response of B-lymphocytes: PERK-independent development of antibody-secreting cells. Mol. Immunol. 45, 1035-1043
26. Ma, Y., Shimizu, Y., Mann, M. J., Jin, Y., and Hendershot, L. M. (2010) Plasma cell differentiation initiates a limited ER stress response by specifically suppressing the PERK-dependent branch of the unfolded protein response. Cell Stress Chaperones 15, 281-293
27. Masciarelli, S., Fra, A. M., Pengo, N., Bertolotti, M., Cenci, S., Fagioli, C., Ron, D., Hendershot, L. M., and Sitia, R. (2010) CHOP-independent apoptosis and pathway-selective induction of the UPR in developing plasma cells. Mol. Immunol. 47, 1356-1365
28. Strasser, A., and Bouillet, P. (2003) The control of apoptosis in lymphocyte selection. Immunol. Rev. 193, 82-92
29. Veis, D. J., Sorenson, C. M., Shutter, J. R., and Korsmeyer, S. J. (1993) Bcl-2-deficient mice demonstrate fulminant lymphoid apoptosis, polycystic kidneys, and hypopigmented hair. Cell 75, 229-240
30. Vikstrom, I., Carotta, S., Lüthje, K., Peperzak, V., Jost, P. J., Glaser, S., Busslinger, M., Bouillet, P., Strasser, A., Nutt, S. L., and Tarlinton, D. M. (2010) Mcl-1 is essential for germinal center formation and B cell memory. Science 330, 1095-1099
31. Danial, N. N., and Korsmeyer, S. J. (2004) Cell death: critical control points. Cell 116, 205-219
32. Cory, S., and Adams, J. M. (2002) The Bcl2 family: regulators of the cellular life-or-death switch. Nat. Rev. Cancer 2, 647-656
33. Oltersdorf, T., Elmore, S. W., Shoemaker, A. R., Armstrong, R. C., Augeri, D. J., Belli, B. A., Bruncko, M., Deckwerth, T. L., Dinges, J., Hajduk, P. J., Joseph, M. K., Kitada, S., Korsmeyer, S. J., Kunzer, A. R., Letai, A., Li, C., Mitten, M. J., Nettesheim, D. G., Ng, S., Nimmer, P. M., O'Connor, J. M., Oleksijew, A., Petros, A. M., Reed, J. C., Shen, W., Tahir, S. K., Thompson, C. B., Tomaselli, K. J., Wang, B., Wendt, M. D., Zhang, H., Fesik, S. W., and Rosenberg, S. H. (2005) An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 435, 677-681
34. Carrington, E. M., Vikstrom, I. B., Light, A., Sutherland, R. M., Londrigan, S. L., Mason, K. D., Huang, D. C., Lew, A. M., and Tarlinton, D. M. (2010) BH3 mimetics antagonizing restricted prosurvival Bcl-2 proteins represent another class of selective immune modulatory drugs. Proc. Natl. Acad. Sci. U.S.A. 107, 10967-10971
35. Peperzak, V., Vikström, I., Walker, J., Glaser, S. P., LePage, M., Coquery, C. M., Erickson, L. D., Fairfax, K., Mackay, F., Strasser, A., Nutt, S. L., and Tarlinton, D. M. (2013) Mcl-1 is essential for the survival of plasma cells. Nat. Immunol. 14, 290-297
36. Morales, A. A., Gutman, D., Lee, K. P., and Boise, L. H. (2008) BH3-only proteins Noxa, Bmf, and Bim are necessary for arsenic trioxide-induced cell death in myeloma. Blood 111, 5152-5162
37. Boise, L. H., Minn, A. J., Noel, P. J., June, C. H., Accavitti, M. A., Lindsten, T., and Thompson, C. B. (1995) CD28 costimulation can promote T cell survival by enhancing the expression of Bcl-xL. Immunity 3, 87-98
38. Morales, A. A., Kurtoglu, M., Matulis, S. M., Liu, J., Siefker, D., Gutman, D. M., Kaufman, J. L., Lee, K. P., Lonial, S., and Boise, L. H. (2011) Distribution of Bim determines Mcl-1 dependence or codependence with BclxL/Bcl-2 in Mcl-1-expressing myeloma cells. Blood 118, 1329-1339
39. Blackman, M. A., Tigges, M. A., Minie, M. E., and Koshland, M. E. (1986) A model system for peptide hormone action in differentiation: interleukin 2 induces a B lymphoma to transcribe the J chain gene. Cell 47, 609-617
40. Mita, S., Harada, N., Naomi, S., Hitoshi, Y., Sakamoto, K., Akagi, M., Tominaga, A., and Takatsu, K. (1988) Receptors for T cell-replacing factor/ interleukin 5: specificity, quantitation, and its implication. J. Exp. Med. 168, 863-878
41. Souers, A. J., Leverson, J. D., Boghaert, E. R., Ackler, S. L., Catron, N. D., Chen, J., Dayton, B. D., Ding, H., Enschede, S. H., Fairbrother, W. J., Huang, D. C., Hymowitz, S. G., Jin, S., Khaw, S. L., Kovar, P. J., Lam, L. T., Lee, J., Maecker, H. L., Marsh, K. C., Mason, K. D., Mitten, M. J., Nimmer, P. M., Oleksijew, A., Park, C. H., Park, C. M., Phillips, D. C., Roberts, A. W., Sampath, D., Seymour, J. F., Smith, M. L., Sullivan, G. M., Tahir, S. K., Tse, C., Wendt, M. D., Xiao, Y., Xue, J. C., Zhang, H., Humerickhouse, R. A., Rosenberg, S. H., and Elmore, S. W. (2013) ABT-199, a potent and selective BCL-2 inhibitor, achieves antitumor activity while sparing platelets. Nat. Med. 19, 202-208