XBP-1-deficient plasmablasts show normal protein folding but altered glycosylation and lipid synthesis

Journal of Immunology

Volumn 183, Issue 6, 2009, Pages 3690-3699

  McGehee, Annette M ^a   Dougan, Stephanie K ^a   Klemm, Elizabeth J ^a   Shui, Guanghou ^b   Park, Boyoun ^a   Kim, You Me ^a   Watson, Nicki ^a   Wenk, Markus R ^b,c   Ploegh, Hidde L ^a   Hu, Chih Chi Andrew ^a  

^a WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN KAPPA CHAIN; IMMUNOGLOBULIN M; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLINOSITOL; SPHINGOMYELIN; X BOX BINDING PROTEIN 1; DNA BINDING PROTEIN; HLA ANTIGEN CLASS 1; LIPID; MEMBRANE LIPID; REGULATORY FACTOR X TRANSCRIPTION FACTORS; TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL MATURATION; CELL MEMBRANE; ELECTRON MICROSCOPY; ENDOPLASMIC RETICULUM; IMMUNOBLOTTING; LIPID ANALYSIS; LIPOGENESIS; LIQUID CHROMATOGRAPHY; LYSOSOME; MASS SPECTROMETRY; MOUSE; NONHUMAN; PLASMA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN GLYCOSYLATION; PROTEIN ISOLATION; ANIMAL; B LYMPHOCYTE; BIOSYNTHESIS; CHEMISTRY; CYTOLOGY; GLYCOSYLATION; METABOLISM; MOUSE MUTANT; PHYSIOLOGY;

ANIMALS; B-LYMPHOCYTES; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM; GLYCOSYLATION; HISTOCOMPATIBILITY ANTIGENS CLASS I; IMMUNOGLOBULIN M; LIPIDS; MEMBRANE LIPIDS; MICE; MICE, MUTANT STRAINS; PLASMA CELLS; PROTEIN FOLDING; TRANSCRIPTION FACTORS;

EID: 70349323169     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0900953     Document Type: Article

References (39)

1. Chen-Bettecken, U., E. Wecker, and A. Schimpl. 1987. Transcriptional control of μ- and κ-gene expression in resting and bacterial lipopolysaccharide-activated normal B cells. Immunobiology 174: 162-176. (Pubitemid 17050499)
2. Shapiro-Shelef, M., and K. Calame. 2005. Regulation of plasma-cell development. Nat. Rev. Immunol. 5: 230-242.
3. 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. (Pubitemid 34062456)
4. 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.
5. Shen, X., R. E. Ellis, K. Lee, C. Y. Liu, K. Yang, A. Solomon, H. Yoshida, R. Morimoto, D. M. Kurnit, K. Mori, and R. J. Kaufman. 2001. Complementary signaling pathways regulate the unfolded protein response and are required for C. elegans development. Cell 107: 893-903.
6. 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.
7. Acosta-Alvear, D., Y. Zhou, A. Blais, M. Tsikitis, N. H. Lents, C. Arias, C. J. Lennon, Y. Kluger, and B. D. Dynlacht. 2007. XBP1 controls diverse cell type- and condition-specific transcriptional regulatory networks. Mol. Cell 27: 53-66. (Pubitemid 46991391)
8. 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.
9. Lee, A. H., G. C. Chu, N. N. Iwakoshi, and L. H. Glimcher. 2005. XBP-1 is required for biogenesis of cellular secretory machinery of exocrine glands. EMBO J. 24: 4368-4380.
10. Hu, C. C., S. K. Dougan, A. M. McGehee, J. C. Love, and H. L. Ploegh. 2009. XBP-1 regulates signal transduction, transcription factors and bone marrow colonization in B cells. EMBO J. 28: 1624-1636.
11. Hetz, C., A. H. Lee, D. Gonzalez-Romero, P. Thielen, J. Castilla, C. Soto, and L. H. Glimcher. 2008. Unfolded protein response transcription factor XBP-1 does not influence prion replication or pathogenesis. Proc. Natl. Acad. Sci. USA 105: 757-762. (Pubitemid 351171781)
12. Rickert, R. C., J. Roes, and K. Rajewsky. 1997. B lymphocyte-specific, Cremediated mutagenesis in mice. Nucleic Acids Res. 25: 1317-1318.
13. 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. (Pubitemid 28215311)
14. Goodnow, C. C., J. Crosbie, S. Adelstein, T. B. Lavoie, S. J. Smith-Gill, R. A. Brink, H. Pritchard-Briscoe, J. S. Wotherspoon, R. H. Loblay, K. Raphael, et al. 1988. Altered immunoglobulin expression and functional silencing of self-reactive B lymphocytes in transgenic mice. Nature 334: 676-682.
15. 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.
16. Sriburi, R., H. Bommiasamy, G. L. Buldak, G. R. Robbins, M. Frank, S. Jackowski, and J. W. Brewer. 2007. Coordinate regulation of phospholipid biosynthesis and secretory pathway gene expression in XBP-1(S)-induced endoplasmic reticulum biogenesis. J. Biol. Chem. 282: 7024-7034.
17. Lee, A. H., E. F. Scapa, D. E. Cohen, and L. H. Glimcher. 2008. Regulation of hepatic lipogenesis by the transcription factor XBP1. Science 320: 1492-1496.
18. Gumperz, J. E., C. Roy, A. Makowska, D. Lum, M. Sugita, T. Podrebarac, Y. Koezuka, S. A. Porcelli, S. Cardell, M. B. Brenner, and S. M. Behar. 2000. Murine CD1d-restricted T cell recognition of cellular lipids. Immunity 12: 211-221.
19. 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.
20. Bordier, C. 1981. Phase separation of integral membrane proteins in Triton X-114 solution. J. Biol. Chem. 256: 1604-1607.
21. Bligh, E. G., and W. J. Dyer. 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37: 911-917.
22. Fei, W., G. Shui, B. Gaeta, X. Du, L. Kuerschner, P. Li, A. J. Brown, M. R. Wenk, R. G. Parton, and H. Yang. 2008. Fld1p, a functional homologue of human seipin, regulates the size of lipid droplets in yeast. J. Cell Biol. 180: 473-482.
23. Chan, R., P. D. Uchil, J. Jin, G. Shui, D. E. Ott, W. Mothes, and M. R. Wenk. 2008. Retroviruses human immunodeficiency virus and murine leukemia virus are enriched in phosphoinositides. J. Virol. 82: 11228-11238.
24. 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.
25. Tirosh, B., N. N. Iwakoshi, L. H. Glimcher, and H. L. Ploegh. 2005. XBP-1 specifically promotes IgM synthesis and secretion, but is dispensable for degradation of glycoproteins in primary B cells. J. Exp. Med. 202: 505-516. (Pubitemid 41186949)
26. Genestier, L., M. Taillardet, P. Mondiere, H. Gheit, C. Bella, and T. Defrance. 2007. TLR agonists selectively promote terminal plasma cell differentiation of B cell subsets specialized in thymus-independent responses. J. Immunol. 178: 7779-7786. (Pubitemid 46898049)
27. Mulugeta, S., J. A. Maguire, J. L. Newitt, S. J. Russo, A. Kotorashvili, and M. F. Beers. 2007. Misfolded BRICHOS SP-C mutant proteins induce apoptosis via caspase-4- and cytochrome c-related mechanisms. Am. J. Physiol. 293: L720-L729.
28. Dhaunchak, A. S., and K. A. Nave. 2007. A common mechanism of PLP/DM20 misfolding causes cysteine-mediated endoplasmic reticulum retention in oligodendrocytes and Pelizaeus-Merzbacher disease. Proc. Natl. Acad. Sci. USA 104: 17813-17818.
29. 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.
30. Credle, J. J., J. S. Finer-Moore, F. R. Papa, R. M. Stroud, and P. Walter. 2005. On the mechanism of sensing unfolded protein in the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 102: 18773-18784. (Pubitemid 43049523)
31. Bertolotti, A., Y. Zhang, L. M. Hendershot, H. P. Harding, and D. Ron. 2000. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat. Cell Biol. 2: 326-332.
32. Okamura, K., Y. Kimata, H. Higashio, A. Tsuru, and K. Kohno. 2000. Dissociation of Kar2p/BiP from an ER sensory molecule, Ire1p, triggers the unfolded protein response in yeast. Biochem. Biophys. Res. Commun. 279: 445-450. (Pubitemid 32016735)
33. Gu, F., D. T. Nguyen, M. Stuible, N. Dube, M. L. Tremblay, and E. Chevet. 2004. Protein-tyrosine phosphatase 1B potentiates IRE1 signaling during endoplasmic reticulum stress. J. Biol. Chem. 279: 49689-49693. (Pubitemid 39577772)
34. 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. (Pubitemid 36262999)
35. Haze, K., H. Yoshida, H. Yanagi, T. Yura, and K. Mori. 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. (Pubitemid 29534025)
36. Yoshida, H., T. Okada, K. Haze, H. Yanagi, T. Yura, M. Negishi, and K. Mori. 2000. ATF6 activated by proteolysis binds in the presence of NF-Y (CBF) directly to the cis-acting element responsible for the mammalian unfolded protein response. Mol. Cell. Biol. 20: 6755-6767.
37. Gass, J. N., H. Y. Jiang, R. C. Wek, and J. W. Brewer. 2008. The unfolded protein response of B-lymphocytes: PERK-independent development of antibody-secreting cells. Mol. Immunol. 45: 1035-1043. (Pubitemid 350016334)
38. 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. (Pubitemid 35470877)
39. Tulp, A., M. Barnhoorn, E. Bause, and H. Ploegh. 1986. Inhibition of N-linked oligosaccharide trimming mannosidases blocks human B cell development. EMBO J. 5: 1783-1790.