Syntaxin-4 is implicated in the secretion of antibodies by human plasma cells

Journal of Leukocyte Biology

Volumn 95, Issue 2, 2014, Pages 305-312

  Gómez Jaramillo, Laura ^a   Delgado Pérez, Luis ^a   Reales, Elena ^a,b   Mora López, Francisco ^a   Mateos, Rosa M ^a   García Poley, Antonio ^a   Brieva, José A ^a   Campos Caro, Antonio ^a  

^a HOSPITAL UNIVERSITARIO PUERTA DEL MAR   (Spain)

^b CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

Author keywords

Immunoglobulin exocytosis; RNAi protein knockdown; SNARE

Indexed keywords

IMMUNOGLOBULIN E; MEMBRANE PROTEIN; SHORT HAIRPIN RNA; SYNAPTOSOMAL ASSOCIATED PROTEIN 23; SYNTAXIN 3; SYNTAXIN 4; UNCLASSIFIED DRUG; ANTIBODY; DOXYCYCLINE; IMMUNOGLOBULIN A; QB SNARE PROTEIN; QC SNARE PROTEIN; SMALL INTERFERING RNA; SNAP23 PROTEIN, HUMAN; SYNTAXIN; SYNTAXIN 4, HUMAN;

ANTIBODY PRODUCTION; ARTICLE; CELL ISOLATION; CELL MEMBRANE; COLON; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMORAL IMMUNITY; IMMUNOGLOBULIN PRODUCTION; MEMBRANE FUSION; MULTIPLE MYELOMA; MULTIPLE MYELOMA CELL LINE; PLASMA CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; U266 CELL LINE; BIOSYNTHESIS; CELL FRACTIONATION; CELL LINE; CELL SEPARATION; DRUG EFFECT; IMMUNOGLOBULIN EXOCYTOSIS; METABOLISM; PATHOLOGY; PROTEIN BINDING; PROTEIN TRANSPORT; RNAI PROTEIN KNOCKDOWN; SECRETION (PROCESS); SNARE;

IMMUNOGLOBULIN EXOCYTOSIS; RNAI PROTEIN KNOCKDOWN; SNARE;

ANTIBODIES; CELL LINE; CELL MEMBRANE; CELL SEPARATION; DOXYCYCLINE; HUMANS; IMMUNOGLOBULIN A; IMMUNOGLOBULIN E; MULTIPLE MYELOMA; PLASMA CELLS; PROTEIN BINDING; PROTEIN TRANSPORT; QA-SNARE PROTEINS; QB-SNARE PROTEINS; QC-SNARE PROTEINS; RNA, SMALL INTERFERING; SUBCELLULAR FRACTIONS;

EID: 84897020335     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.0113031     Document Type: Article

References (40)

1. Sherr, C. J., Uhr, J. W. (1971) Immunoglobulin synthesis and secretion. VI. Synthesis and intracellular transport of immunoglobulin in nonsecretory lymphoma cells. J. Exp. Med. 133, 901-920.
2. Uhr, J. W. (1970) Intracellular events underlying synthesis and secretion of immunoglobulin. Cell. Immunol. 1, 228-244.
3. Gonzalez-Garcia, I., Rodriguez-Bayona, B., Mora-Lopez, F., Campos-Caro, A., Brieva, J. A. (2008) Increased survival is a selective feature of human circulating antigen-induced plasma cells synthesizing high-affinity antibodies. Blood 111, 741-749.
4. Medina, F., Segundo, C., Campos-Caro, A., Salcedo, I., Garcia-Poley, A., Brieva, J. A. (2003) Isolation, maturational level, and functional capacity of human colon lamina propria plasma cells. Gut 52, 383-389.
5. Medina, F., Segundo, C., Campos-Caro, A., Gonzalez-Garcia, I., Brieva, J. A. (2002) The heterogeneity shown by human plasma cells from tonsil, blood, and bone marrow reveals graded stages of increasing maturity, but local profiles of adhesion molecule expression. Blood 99, 2154-2161.
6. Jimenez-Gomez, G., Gomez-Perales, J. L., Ramos-Amaya, A., Gonzalez-Garcia, I., Campos-Caro, A., Brieva, J. A. (2010) Modulated selection of IGHV gene somatic hypermutation during systemic maturation of human plasma cells. J. Leukoc. Biol. 87, 523-530.
7. Reales, E., Mora-Lopez, F., Rivas, V., Garcia-Poley, A., Brieva, J. A., Campos-Caro, A. (2005) Identification of soluble N-ethylmaleimide-sensitive factor attachment protein receptor exocytotic machinery in human plasma cells: SNAP-23 is essential for antibody secretion. J. Immunol. 175, 6686-6693.
8. Hong, W. (2005) SNAREs and traffic. Biochim. Biophys. Acta 1744, 493-517.
9. Südhof, T. C., Rizo, J. (2011) Synaptic vesicle exocytosis. Cold Spring Harb. Perspect. Biol 3, pii: a005637.
10. Jahn, R., Scheller, R. H. (2006) SNAREs-engines for membrane fusion. Nat. Rev. Mol. Cell. Biol. 7, 631-643.
11. Sutton, R. B., Fasshauer, D., Jahn, R., Brunger, A. T. (1998) Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution. Nature 395, 347-353.
12. Fasshauer, D., Sutton, R. B., Brunger, A. T., Jahn, R. (1998) Conserved structural features of the synaptic fusion complex: SNARE proteins reclassified as Q-and R-SNAREs. Proc. Natl. Acad. Sci. USA 95, 15781-15786.
13. Sollner, T., Whiteheart, S. W., Brunner, M., Erdjument-Bromage, H., Geromanos, S., Tempst, P., Rothman, J. E. (1993) SNAP receptors implicated in vesicle targeting and fusion. Nature 362, 318-324.
14. Stow, J. L., Manderson, A. P., Murray, R. Z. (2006) SNAREing immunity: the role of SNAREs in the immune system. Nat. Rev. Immunol. 6, 919-929.
15. Martin-Martin, B., Nabokina, S. M., Lazo, P. A., Mollinedo, F. (1999) Co-expression of several human syntaxin genes in neutrophils and differentiating HL-60 cells: variant isoforms and detection of syntaxin 1. J. Leukoc. Biol. 65, 397-406.
16. Sander, L. E., Frank, S. P., Bolat, S., Blank, U., Galli, T., Bigalke, H., Bischoff, S. C., Lorentz, A. (2008) Vesicle associated membrane protein (VAMP)-7 and VAMP-8, but not VAMP-2 or VAMP-3, are required for activation-induced degranulation of mature human mast cells. Eur. J. Immunol. 38, 855-863.
17. Murray, R. Z., Kay, J. G., Sangermani, D. G., Stow, J. L. (2005) A role for the phagosome in cytokine secretion. Science 310, 1492-1495.
18. Bryceson, Y. T., Rudd, E., Zheng, C., Edner, J., Ma, D., Wood, S. M., Bechensteen, A. G., Boelens, J. J., Celkan, T., Farah, R. A., Hultenby, K., Winiarski, J., Roche, P. A., Nordenskjold, M., Henter, J. I., Long, E. O., Ljunggren, H. G. (2007) Defective cytotoxic lymphocyte degranulation in syntaxin-11 deficient familial hemophagocytic lymphohistiocytosis 4 (FHL4) patients. Blood 110, 1906-1915.
19. Pattu, V., Qu, B., Schwarz, E. C., Strauss, B., Weins, L., Bhat, S. S., Halimani, M., Marshall, M., Rettig, J., Hoth, M. (2012) SNARE protein expression and localization in human cytotoxic T lymphocytes. Eur. J. Immunol. 42, 470-475.
20. Ye, S., Karim, Z. A., Al Hawas, R., Pessin, J. E., Filipovich, A. H., Whiteheart, S. W. (2012) Syntaxin-11, but not syntaxin-2 or syntaxin-4, is required for platelet secretion. Blood 120, 2484-2492.
21. Krzewski, K., Gil-Krzewska, A., Watts, J., Stern, J. N., Strominger, J. L. (2011) VAMP4-and VAMP7-expressing vesicles are both required for cytotoxic granule exocytosis in NK cells. Eur. J. Immunol. 41, 3323-3329.
22. Dabrazhynetskaya, A., Ma, J., Guerreiro-Cacais, A. O., Arany, Z., Rudd, E., Henter, J. I., Karre, K., Levitskaya, J., Levitsky, V. (2012) Syntaxin 11 marks a distinct intracellular compartment recruited to the immunological synapse of NK cells to colocalize with cytotoxic granules. J. Cell. Mol. Med. 16, 129-141.
23. Ravichandran, V., Chawla, A., Roche, P. A. (1996) Identification of a novel syntaxin-and synaptobrevin/VAMP-binding protein, SNAP-23, expressed in non-neuronal tissues. J. Biol. Chem. 271, 13300-13303.
24. Riento, K., Galli, T., Jansson, S., Ehnholm, C., Lehtonen, E., Olkkonen, V. M. (1998) Interaction of Munc-18-2 with syntaxin 3 controls the association of apical SNAREs in epithelial cells. J. Cell Sci. 111, 2681-2688.
25. Frank, S. P., Thon, K. P., Bischoff, S. C., Lorentz, A. (2011) SNAP-23 and syntaxin-3 are required for chemokine release by mature human mast cells. Mol. Immunol. 49, 353-358.
26. Lemons, P. P., Chen, D., Bernstein, A. M., Bennett, M. K., Whiteheart, S. W. (1997) Regulated secretion in platelets: identification of elements of the platelet exocytosis machinery. Blood 90, 1490-1500.
27. Brieva, J. A., Roldan, E., Rodriguez, C., Navas, G. (1994) Human tonsil, blood and bone marrow in vivo-induced B cells capable of spontaneous and high-rate immunoglobulin secretion in vitro: differences in the requirements for factors and for adherent and bone marrow stromal cells, as well as distinctive adhesion molecule expression. Eur. J. Immunol. 24, 362-366.
28. Oyler, G. A., Higgins, G. A., Hart, R. A., Battenberg, E., Billingsley, M., Bloom, F. E., Wilson, M. C. (1989) The identification of a novel synaptosomal-associated protein, SNAP-25, differentially expressed by neuronal subpopulations. J. Cell Biol. 109, 3039-3052.
29. Sudhof, T. C., Rothman, J. E. (2009) Membrane fusion: grappling with SNARE and SM proteins. Science 323, 474-477.
30. Kawanishi, M., Tamori, Y., Okazawa, H., Araki, S., Shinoda, H., Kasuga, M. (2000) Role of SNAP23 in insulin-induced translocation of GLUT4 in 3T3-L1 adipocytes. Mediation of complex formation between syntaxin4 and VAMP2. J. Biol. Chem. 275, 8240-8247.
31. Puri, N., Roche, P. A. (2006) Ternary SNARE complexes are enriched in lipid rafts during mast cell exocytosis. Traffic 7, 1482-1494.
32. Fasshauer, D., Antonin, W., Margittai, M., Pabst, S., Jahn, R. (1999) Mixed and non-cognate SNARE complexes. Characterization of assembly and biophysical properties. J. Biol. Chem. 274, 15440-15446.
33. Gresch, O., Engel, F. B., Nesic, D., Tran, T. T., England, H. M., Hickman, E. S., Korner, I., Gan, L., Chen, S., Castro-Obregon, S., Hammermann, R., Wolf, J., Muller-Hartmann, H., Nix, M., Siebenkotten, G., Kraus, G., Lun, K. (2004) New non-viral method for gene transfer into primary cells. Methods 33, 151-163.
34. Prince, H. M., Dessureault, S., Gallinger, S., Krajden, M., Sutherland, D. R., Addison, C., Zhang, Y., Graham, F. L., Stewart, A. K. (1998) Efficient adenovirus-mediated gene expression in malignant human plasma cells: relative lymphoid cell resistance. Exp. Hematol. 26, 27-36.
35. Bethani, I., Werner, A., Kadian, C., Geumann, U., Jahn, R., Rizzoli, S. O. (2009) Endosomal fusion upon SNARE knockdown is maintained by residual SNARE activity and enhanced docking. Traffic 10, 1543-1559.
36. Fu, J., Naren, A. P., Gao, X., Ahmmed, G. U., Malik, A. B. (2005) Protease-activated receptor-1 activation of endothelial cells induces protein kinase Cα-dependent phosphorylation of syntaxin 4 and Munc18c: role in signaling P-selectin expression. J. Biol. Chem. 280, 3178-3184.
37. Lafont, F., Verkade, P., Galli, T., Wimmer, C., Louvard, D., Simons, K. (1999) Raft association of SNAP receptors acting in apical trafficking in Madin-Darby canine kidney cells. Proc. Natl. Acad. Sci. USA 96, 3734-3738.
38. Low, S. H., Chapin, S. J., Wimmer, C., Whiteheart, S. W., Komuves, L. G., Mostov, K. E., Weimbs, T. (1998) The SNARE machinery is involved in apical plasma membrane trafficking in MDCK cells. J. Cell Biol. 141, 1503-1513.
39. Sadoul, K., Berger, A., Niemann, H., Weller, U., Roche, P. A., Klip, A., Trimble, W. S., Regazzi, R., Catsicas, S., Halban, P. A. (1997) SNAP-23 is not cleaved by botulinum neurotoxin E and can replace SNAP-25 in the process of insulin secretion. J. Biol. Chem. 272, 33023-33027.
40. Mestecky, J., Russell, M. W., Jackson, S., Brown, T. A. (1986) The human IgA system: a reassessment. Clin. Immunol. Immunopathol. 40, 105-114.