Scaffold protein JLP is critical for CD40 signaling in B lymphocytes

Journal of Biological Chemistry

Volumn 290, Issue 9, 2015, Pages 5256-5266

  Wang, Hui Ming ^a   Yan, Qi ^a   Yang, Tao ^a   Cheng, Hui ^a   Du, Juan ^a   Yoshioka, Katsuji ^c   Kung, Sam K P ^b   Ding, Guo Hua ^a  

^a WUHAN UNIVERSITY   (China)

^b UNIVERSITY OF MANITOBA   (Canada)

^c KANAZAWA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROLIFERATION; LYMPHOCYTES; MAMMALS; PROTEINS; SIGNAL TRANSDUCTION;

B LYMPHOCYTES; BIOLOGICAL FUNCTIONS; CELL PERIPHERY; CELLULAR EVENTS; CO-LOCALIZATIONS; COGNATE LIGANDS; SCAFFOLD PROTEIN; TEMPORAL AND SPATIAL;

SCAFFOLDS (BIOLOGY);

CD40 ANTIGEN; CD40 LIGAND; CILIOBREVIN D; DYNEIN ADENOSINE TRIPHOSPHATASE; ENZYME INHIBITOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; JNK ASSOCIATED LEUCINE ZIPPER PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; RAB PROTEIN; SCAFFOLD PROTEIN; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; PROTEIN BINDING; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SPAG9 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; FLOW CYTOMETRY; IMMUNOPRECIPITATION; INTERNALIZATION; LYMPHOCYTE CULTURE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; SPLEEN CELL; WESTERN BLOTTING; ANIMAL; CELL CULTURE; CYTOLOGY; DEFICIENCY; ENDOCYTOSIS; GENETICS; HEK293 CELL LINE; HUMAN; KNOCKOUT MOUSE; METABOLISM; RNA INTERFERENCE; SPLEEN;

MURINAE; MUS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANTIGENS, CD40; B-LYMPHOCYTES; BLOTTING, WESTERN; CD40 LIGAND; CELLS, CULTURED; DYNEINS; ENDOCYTOSIS; FEMALE; FLOW CYTOMETRY; HEK293 CELLS; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MALE; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; MITOGEN-ACTIVATED PROTEIN KINASES; PROTEIN BINDING; RAB5 GTP-BINDING PROTEINS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SPLEEN;

EID: 84923914152     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.618496     Document Type: Article

References (44)

1. Graham, J. P., Arcipowski, K. M., and Bishop, G. A. (2010) Differential B-lymphocyte regulation by CD40 and its viral mimic, latent membrane protein 1. Immunol. Rev. 237, 226-248
2. Lee, C. M., Onésime, D., Reddy, C. D., Dhanasekaran, N., and Reddy, E. P. (2002) JLP: a scaffolding protein that tethers JNK/p38MAPK signaling modules and transcription factors. Proc. Natl. Acad. Sci. U.S.A. 99, 14189-14194
3. Ikonomov, O. C., Fligger, J., Sbrissa, D., Dondapati, R., Mlak, K., Deeb, R., and Shisheva, A. (2009) Kinesin adapter JLP links PIKfyve to microtubulebased endosome-to-trans-Golgi network traffic of furin. J. Biol. Chem. 284, 3750-3761
4. Verhey, K. J., and Hammond, J. W. (2009) Traffic control: regulation of kinesin motors. Nat. Rev. Mol. Cell Biol. 10, 765-777
5. Roberts, A. J., Kon, T., Knight, P. J., Sutoh, K., and Burgess, S. A. (2013) Functions and mechanics of dynein motor proteins. Nat. Rev. Mol. Cell Biol. 14, 713-726
6. Pham, L. V., Tamayo, A. T., Yoshimura, L. C., Lo, P., Terry, N., Reid, P. S., and Ford, R. J. (2002) A CD40 signalosome anchored in lipid rafts leads to constitutive activation of NF-κB and autonomous cell growth in B cell lymphomas. Immunity 16, 37-50
7. Grassmé, H., Jendrossek, V., Bock, J., Riehle, A., and Gulbins, E. (2002) Ceramide-rich membrane rafts mediate CD40 clustering. J. Immunol. 168, 298-307
8. Grassmé, H., Bock, J., Kun, J., and Gulbins, E. (2002) Clustering of CD40 ligand is required to form a functional contact with CD40. J. Biol. Chem. 277, 30289-30299
9. Reyes-Moreno, C., Sharif-Askari, E., Girouard, J., Léveillé, C., Jundi, M., Akoum, A., Lapointe, R., Darveau, A., and Mourad, W. (2007) Requirement of oxidation-dependent CD40 homodimers for CD154/CD40 bidirectional signaling. J. Biol. Chem. 282, 19473-19480
10. Chen, Y., Chen, J., Xiong, Y., Da, Q., Xu, Y., Jiang, X., and Tang, H. (2006) Internalization of CD40 regulates its signal transduction in vascular endothelial cells. Biochem. Biophys. Res. Commun. 345, 106-117
11. Wang, H., Zhao, C., Zhang, M., Lee, C. M., Reddy, E. P., and Kung, S. K. (2013) A novel role of the scaffolding protein JLP in tuning CD40-induced activation of dendritic cells. Immunobiology 218, 835-843
12. Iwanaga, A., Wang, G., Gantulga, D., Sato, T., Baljinnyam, T., Shimizu, K., Takumi, K., Hayashi, M., Akashi, T., Fuse, H., Sugihara, K., Asano, M., and Yoshioka, K. (2008) Ablation of the scaffold protein JLP causes reduced fertility in male mice. Transgenic Res. 17, 1045-1058
13. Kashef, K., Lee, C. M., Ha, J. H., Reddy, E. P., and Dhanasekaran, D. N. (2005) JNK-interacting leucine zipper protein is a novel scaffolding protein in the Gα13 signaling pathway. Biochemistry 44, 14090-14096
14. Kashef, K., Xu, H., Reddy, E. P., and Dhanasekaran, D. N. (2006) Endodermal differentiation of murine embryonic carcinoma cells by retinoic acid requires JLP, a JNK-scaffolding protein. J. Cell. Biochem. 98, 715-722
15. Takaesu, G., Kang, J. S., Bae, G. U., Yi, M. J., Lee, C. M., Reddy, E. P., and Krauss, R. S. (2006) Activation of p38α/β MAPK in myogenesis via binding of the scaffold protein JLP to the cell surface protein Cdo. J. Cell Biol. 175, 383-388
16. Hostager, B. S., Catlett, I. M., and Bishop, G. A. (2000) Recruitment of CD40 and tumor necrosis factor receptor-associated factors 2 and 3 to membrane microdomains during CD40 signaling. J. Biol. Chem. 275, 15392-15398
17. Manning, E., Pullen, S. S., Souza, D. J., Kehry, M., and Noelle, R. J. (2002) Cellular responses to murine CD40 in a mouse B cell line may be TRAF dependent or independent. Eur. J. Immunol. 32, 39-49
18. Chen, J., Chen, L., Wang, G., and Tang, H. (2007) Cholesterol-dependent and -independent CD40 internalization and signaling activation in cardiovascular endothelial cells. Arterioscler. Thromb. Vasc. Biol. 27, 2005-2013
19. Anolik, J., Looney, R. J., Bottaro, A., Sanz, I., and Young, F. (2003) Downregulation of CD20 on B cells upon CD40 activation. Eur. J. Immunol. 33, 2398-2409
20. Gennerich, A., and Vale, R. D. (2009) Walking the walk: how kinesin and dynein coordinate their steps. Curr. Opin. Cell Biol. 21, 59-67
21. Caviston, J. P., and Holzbaur, E. L. (2006) Microtubule motors at the intersection of trafficking and transport. Trends Cell Biol. 16, 530-537
22. Firestone, A. J., Weinger, J. S., Maldonado, M., Barlan, K., Langston, L. D., O'Donnell, M., Gelfand, V. I., Kapoor, T. M., and Chen, J. K. (2012) Smallmolecule inhibitors of the AAA+ ATPase motor cytoplasmic dynein. Nature 484, 125-129
23. Kikkawa, M. (2013) Big steps toward understanding dynein. J. Cell Biol. 202, 15-23
24. Clippinger, A. J., and Alwine, J. C. (2012) Dynein mediates the localization and activation of mTOR in normal and human cytomegalovirus-infected cells. Genes Dev. 26, 2015-2026
25. Schnyder, T., Castello, A., Feest, C., Harwood, N. E., Oellerich, T., Urlaub, H., Engelke, M., Wienands, J., Bruckbauer, A., and Batista, F. D. (2011) B cell receptor-mediated antigen gathering requires ubiquitin ligase Cbl and adaptors Grb2 and Dok-3 to recruit dynein to the signaling microcluster. Immunity 34, 905-918
26. Zerial, M., and McBride, H. (2001) Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2, 107-117
27. Jordens, I., Marsman, M., Kuijl, C., and Neefjes, J. (2005) Rab proteins, connecting transport and vesicle fusion. Traffic 6, 1070-1077
28. Li, Y. Y., Baccam, M., Waters, S. B., Pessin, J. E., Bishop, G. A., and Koretzky, G. A. (1996) CD40 ligation results in protein kinase C-independent activation of ERK and JNK in resting murine splenic B cells. J. Immunol. 157, 1440-1447
29. Sakata, N., Patel, H. R., Terada, N., Aruffo, A., Johnson, G. L., and Gelfand, E. W. (1995) Selective activation of c-Jun kinase mitogen-activated protein kinase by CD40 on human B cells. J. Biol. Chem. 270, 30823-30828
30. Sutherland, C. L., Heath, A. W., Pelech, S. L., Young, P. R., and Gold, M. R. (1996) Differential activation of the ERK, JNK, and p38 mitogen-activated protein kinases by CD40 and the B cell antigen receptor. J. Immunol. 157, 3381-3390
31. Blonska, M., and Lin, X. (2011) NF-B signaling pathways regulated by CARMA family of scaffold proteins. Cell Res. 21, 55-70
32. Shaw, A. S., and Filbert, E. L. (2009) Scaffold proteins and immune-cell signalling. Nat. Rev. Immunol. 9, 47-56
33. Rickert, R. C., Jellusova, J., and Miletic, A. V. (2011) Signaling by the tumor necrosis factor receptor superfamily in B-cell biology and disease. Immunol. Rev. 244, 115-133
34. Bowman, A. B., Kamal, A., Ritchings, B. W., Philp, A. V., McGrail, M., Gindhart, J. G., and Goldstein, L. S. (2000) Kinesin-dependent axonal transport is mediated by the Sunday Driver (SYD) protein. Cell 103, 583-594
35. Verhey, K. J., Meyer, D., Deehan, R., Blenis, J., Schnapp, B. J., Rapoport, T. A., and Margolis, B. (2001) Cargo of kinesin identified as JIP scaffolding proteins and associated signaling molecules. J. Cell Biol. 152, 959-970
36. Nguyen, Q., Lee, C. M., Le, A., and Reddy, E. P. (2005) JLP associates with kinesin light chain 1 through a novel leucine zipper-like domain. J. Biol. Chem. 280, 30185-30191
37. 2-terminal kinase-interacting protein-3 facilitates phosphorylation and controls localization of am-yloid-β precursor protein. J. Neurosci. 25, 3741-3751
38. Kelkar, N., Standen, C. L., and Davis, R. J. (2005) Role of the JIP4 scaffold protein in the regulation of mitogen-activated protein kinase signaling pathways. Mol. Cell. Biol. 25, 2733-2743
39. Cavalli, V., Kujala, P., Klumperman, J., and Goldstein, L. S. (2005) Sunday Driver links axonal transport to damage signaling. J. Cell Biol. 168, 775-787
40. Arimoto, M., Koushika, S. P., Choudhary, B. C., Li, C., Matsumoto, K., and Hisamoto, N. (2011) The Caenorhabditis elegans JIP3 protein UNC-16 functions as an adaptor to link kinesin-1 with cytoplasmic dynein. J. Neurosci. 31, 2216-2224
41. Fu, M. M., and Holzbaur, E. L. (2013) JIP1 regulates the directionality of APP axonal transport by coordinating kinesin and dynein motors. J. Cell Biol. 202, 495-508
42. Nadiri, A., Polyak, M. J., Jundi, M., Alturaihi, H., Reyes-Moreno, C., Hassan, G. S., and Mourad, W. (2011) CD40 translocation to lipid rafts: signaling requirements and downstream biological events. Eur. J. Immunol. 41, 2358-2367
43. Matsuzawa, A., Tseng, P. H., Vallabhapurapu, S., Luo, J. L., Zhang, W., Wang, H., Vignali, D. A., Gallagher, E., and Karin, M. (2008) Essential cytoplasmic translocation of a cytokine receptor-assembled signaling complex. Science 321, 663-668
44. Häcker, H., Tseng, P. H., and Karin, M. (2011) Expanding TRAF function: TRAF3 as a tri-faced immune regulator. Nat. Rev. Immunol. 11, 457-468