XBP-1 specifically promotes IgM synthesis and secretion, but is dispensable for degradation of glycoproteins in primary B cells

Journal of Experimental Medicine

Volumn 202, Issue 4, 2005, Pages 505-516

  Tirosh, Boaz ^a   Iwakoshi, Neal N ^b   Glimcher, Laurie H ^b   Ploegh, Hidde L ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; GLYCOPROTEIN; IMMUNOGLOBULIN LIGHT CHAIN; IMMUNOGLOBULIN M; LIPOPOLYSACCHARIDE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MESSENGER RNA; PROTEIN US11; T LYMPHOCYTE RECEPTOR ALPHA CHAIN; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; CPG ISLAND; ENDOPLASMIC RETICULUM; IMMUNOGLOBULIN PRODUCTION; MAJOR HISTOCOMPATIBILITY COMPLEX; MEMBRANE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; STIMULATION; TRANSGENIC MOUSE;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; CPG ISLANDS; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION; GLYCOPROTEINS; HISTOCOMPATIBILITY ANTIGENS CLASS I; IMMUNOGLOBULIN LIGHT CHAINS; IMMUNOGLOBULIN MU-CHAINS; LIPOPOLYSACCHARIDES; MICE; MICE, KNOCKOUT; NUCLEAR PROTEINS; PLASMA CELLS; PROTEIN BIOSYNTHESIS; PROTEIN TRANSPORT; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RNA, MESSENGER;

EID: 23944434028     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20050575     Document Type: Article

References (38)

1. Reimold, A.M., N.N. Iwakoshi, J. Manis, P. Vallabhajosyula, E. Szomolanyi-Tsuda, E.M. Gravallese, D. Friend, M.J. Grusby, F. Alt, and L.H. Glimcher. 2001. Plasma cell differentiation requires the transcription factor XBP-1. Nature. 412:300-307.
2. Harding, H.P., M. Calfon, F. Urano, I. Novoa, and D. Ron. 2002. Transcriptional and translational control in the mammalian unfolded protein response. Annu. Rev. Cell Dev. Biol. 18:575-599.
3. Kaufman, R.J. 1999. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev. 13:1211-1233.
4. Lee, A.H., N.N. Iwakoshi, and L.H. Glimcher. 2003. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol. Cell. Biol. 23:7448-7459.
5. Sidrauski, C., and P. Walter. 1997. The transmembrane kinase Ire1p is a site-specific endonuclease that initiates mRNA splicing in the unfolded protein response. Cell. 90:1031-1039.
6. Calfon, M., H. Zeng, F. Urano, J.H. Till, S.R. Hubbard, H.P. Harding, S.G. Clark, and D. Ron. 2002. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature. 415:92-96.
7. Lee, K., W. Tirasophon, X. Shen, M. Michalak, R. Prywes, T. Okada, H. Yoshida, K. Mori, and R.J. Kaufman. 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.
8. Sriburi, R., S. Jackowski, K. Mori, and J.W. Brewer. 2004. XBP1: a link between the unfolded protein response, lipid biosynthesis, and biogenesis of the endoplasmic reticulum. J. Cell Biol. 167:35-41.
9. van Anken, E., E.P. Romijn, C. Maggioni, A. Mezghrani, R. Sitia, I. Braakman, and A.J. Heck. 2003. Sequential waves of functionally related proteins are expressed when B cells prepare for antibody secretion. Immunity. 18:243-253.
10. Iwakoshi, N.N., A.H. Lee, P. Vallabhajosyula, K.L. Otipoby, K. Rajewsky, and L.H. Glimcher. 2003. Plasma cell differentiation and the unfolded protein response intersect at the transcription factor XBP-1. Nat. Immunol. 4:321-329.
11. Shaffer, A.L., M. Shapiro-Shelef, N.N. Iwakoshi, A.H. Lee, S.B. Qian, H. Zhao, X. Yu, L. Yang, B.K. Tan, A. Rosenwald, et al. 2004. XBP1, downstream of Blimp-1, expands the secretory apparatus and other organelles, and increases protein synthesis in plasma cell differentiation. Immunity. 21:81-93.
12. Casagrande, R., P. Stern, M. Diehn, C. Shamu, M. Osario, M. Zuniga, P.O. Brown, and H. Ploegh. 2000. Degradation of proteins from the ER of S. cerevisiae requires an intact unfolded protein response pathway. Mol. Cell. 5:729-735.
13. Travers, K.J., C.K. Patil, L. Wodicka, D.J. Lockhart, J.S. Weissman, and P. Walter. 2000. Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell. 101:249-258.
14. Yoshida, H., T. Matsui, N. Hosokawa, R.J. Kaufman, K. Nagata, and K. Mori. 2003. A time-dependent phase shift in the mammalian unfolded protein response. Dev. Cell. 4:265-271.
15. Krieg, A.M., A.K. Yi, S. Matson, T.J. Waldschmidt, G.A. Bishop, R. Teasdale, G.A. Koretzky, and D.M. Klinman. 1995. CpG motifs in bacterial DNA trigger direct B-cell activation. Nature. 374:546-549.
16. Stevens, R.H., B.A. Askonas, and J.L. Welstead. 1975. Immunoglobulin heavy chain mRNA in mitogen-stimulated B cells. Eur. J. Immunol. 5:47-53.
17. Levine, C.G., D. Mitra, A. Sharma, C.L. Smith, and R.S. Hegde. 2005. The efficiency of protein compartmentalization into the secretory pathway. Mol. Biol. Cell. 16:279-291.
18. Tirosh, B., N.N. Iwakoshi, B.N. Lilley, A.H. Lee, L.H. Glimcher, and H.L. Ploegh. 2005. Human cytomegalovirus protein US11 provokes an unfolded protein response that may facilitate the degradation of class I major histocompatibility complex products. J. Virol. 79:2768-2779.
19. Huppa, J.B., and H.L. Ploegh. 1997. The alpha chain of the T cell antigen receptor is degraded in the cytosol. Immunity. 7:113-122.
20. Yu, H., G. Kaung, S. Kobayashi, and R.R. Kopito. 1997. Cytosolic degradation of T-cell receptor alpha chains by the proteasome. J. Biol. Chem. 272:20800-20804.
21. Hombach, J., T. Tsubata, L. Leclercq, H. Stappert, and M. Reth. 1990. Molecular components of the B-cell antigen receptor complex of the IgM class. Nature. 343:760-762.
22. Fagioli, C., A. Mezghrani, and R. Sitia. 2001. Reduction of interchain disulfide bonds precedes the dislocation of Ig-mu chains from the endoplasmic reticulum to the cytosol for proteasomal degradation. J. Biol. Chem. 276:40962-40967.
23. Calame, K.L., K.I. Lin, and C. Tunyaplin. 2003. Regulatory mechanisms that determine the development and function of plasma cells. Annu. Rev. Immunol. 21:205-230.
24. Sakaguchi, N., S. Kashiwamura, M. Kimoto, P. Thalmann, and F. Melchers. 1988. B lymphocyte lineage-restricted expression of mb-1, a gene with CD3-like structural properties. EMBO J. 7:3457-3464.
25. Boes, M., C. Esau, M.B. Fischer, T. Schmidt, M. Carroll, and J. Chen. 1998. Enhanced B-1 cell development, but impaired IgG antibody responses in mice deficient in secreted IgM. J. Immunol. 160:4776-4787.
26. Tsai, B., Y. Ye, and T.A. Rapoport. 2002. Retro-translocation of proteins from the endoplasmic reticulum into the cytosol. Nat. Rev. Mol. Cell Biol. 3:246-255.
27. Qiu, W., R. Kohen-Avramoglu, S. Mhapsekar, J. Tsai, R.C. Austin, and K. Adeli. 2005. Glucosamine-induced endoplasmic reticulum stress promotes ApoB100 degradation: evidence for Grp78-mediated targeting to proteasomal degradation. Arterioscler Thromb Vasc Biol. 25:571-577.
28. Iwakoshi, N.N., A.H. Lee, and L.H. Glimcher. 2003. The X-box binding protein-1 transcription factor is required for plasma cell differentiation and the unfolded protein response. Immunol. Rev. 194:29-38.
29. Gass, J.N., N.M. Gifford, and J.W. Brewer. 2002. Activation of an unfolded protein response during differentiation of antibody-secreting B cells. J. Biol. Chem. 277:49047-49054.
30. Gunn, K.E., N.M. Gifford, K. Mori, and J.W. Brewer. 2004. A role for the unfolded protein response in optimizing antibody secretion. Mol. Immunol. 41:919-927.
31. Walter, P., and A.E. Johnson. 1994. Signal sequence recognition and protein targeting to the endoplasmic reticulum membrane. Annu. Rev. Cell Biol. 10:87-119.
32. Song, W., D. Raden, E.C. Mandon, and R. Gilmore. 2000. Role of Sec61alpha in the regulated transfer of the ribosome-nascent chain complex from the signal recognition particle to the translocation channel. Cell. 100:333-343.
33. Voigt, S., B. Jungnickel, E. Hartmann, and T.A. Rapoport. 1996. Signal sequence-dependent function of the TRAM protein during early phases of protein transport across the endoplasmic reticulum membrane. J. Cell Biol. 134:25-35.
34. Misaghi, S., M.E. Pacold, D. Blom, H.L. Ploegh, and G.A. Korbel. 2004. Using a small molecule inhibitor of peptide: N-glycanase to probe its role in glycoprotein turnover. Chem. Biol. 11:1677-1687.
35. Rehm, A., P. Stern, H.L. Ploegh, and D. Tortorella. 2001. Signal peptide cleavage of a type I membrane protein, HCMV US11, is dependent on its membrane anchor. EMBO J. 20:1573-1582.
36. Tortorella, D., C.M. Story, J.B. Huppa, E.J. Wiertz, T.R. Jones, I. Bacik, J.R. Bennink, J.W. Yewdell, and H.L. Ploegh. 1998. Dislocation of type I membrane proteins from the ER to the cytosol is sensitive to changes in redox potential. J. Cell Biol. 142:365-376.
37. Villadangos, J.A., R.A. Bryant, J. Deussing, C. Driessen, A.M. Lennon-Dumenil, R.J. Riese, W. Roth, P. Saftig, G.P. Shi, H.A. Chapman, et al. 1999. Proteases involved in MHC class II antigen presentation. Immunol. Rev. 172:109-120.
38. Kuzin, I.I., G.D. Ugine, D. Wu, F. Young, J. Chen, and A. Bottaro. 2000. Normal isotype switching in B cells lacking the I mu exon splice donor site: evidence for multiple I mu-like germline transcripts. J. Immunol. 164:1451-1457.