Differential Activation of the ERK, JNK, and p38 Mitogen-Activated Protein Kinases by CD40 and the B Cell Antigen Receptor

Journal of Immunology

Volumn 157, Issue 8, 1996, Pages 3381-3390

  Sutherland, Claire L ^a   Heath, Andrew W ^b,e   Pelech, Steven L ^a,c   Young, Peter R ^d   Gold, Michael R ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b MERCK RESEARCH LABORATORIES   (United States)

^c Kinetek Biotechnology Corporation   (Canada)

^d GLAXOSMITHKLINE   (United Kingdom)

^e UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIIDIOTYPIC ANTIBODY; CD40 ANTIGEN; IMMUNOGLOBULIN M; LYMPHOCYTE ANTIGEN RECEPTOR; MAP KINASE ACTIVATED KINASE 2; MAP-KINASE-ACTIVATED KINASE 2; MAP2K1 PROTEIN, MOUSE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN KINASE; PROTEIN KINASE (CALCIUM,CALMODULIN); PROTEIN SERINE THREONINE KINASE; PROTEIN TYROSINE KINASE; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL; APOPTOSIS; ARTICLE; B LYMPHOCYTE; CELL LINE; CYTOLOGY; ENZYME ACTIVATION; ENZYMOLOGY; IMMUNOLOGY; METABOLISM; MOUSE; SIGNAL TRANSDUCTION;

ANIMALS; ANTIBODIES, ANTI-IDIOTYPIC; ANTIGENS, CD40; APOPTOSIS; B-LYMPHOCYTES; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CELL LINE; ENZYME ACTIVATION; IMMUNOGLOBULIN M; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE KINASE 1; MAP KINASE KINASE 4; MICE; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MITOGEN-ACTIVATED PROTEIN KINASES; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; RECEPTORS, ANTIGEN, B-CELL; SIGNAL TRANSDUCTION;

EID: 0030587829     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (77)

1. Kitamura, D., A. Kudo, S. Schall, W. Muller, F. Melchers, and K. Rajewsky. 1992. A critical role of λ5 protein in B cell development. Cell 69:823.
2. Reth, M., E. Petrac, P. Wiese, L. Lobel, and F. W. Alt. 1987. Activation of Vκ gene rearrangement in pre-B cells follows the expression of membrane-bound immunoglobulin heavy chains. EMBO J. 6:3299.
3. Gold, M. R., and L. Matsuuchi. 1995. Signal transduction by the antigen receptors of B and T lymphocytes. Int. Rev. Cytol. 157:182.
4. Liu, Y.-J., D. Joshua, G. Williams, C. Smith, J. Gordon, and I. MacLennan. 1989. Mechanism of antigen-driven selection in germinal centres. Nature 342:929.
5. Noelle, R. J., M. Roy, D. M. Shepherd, I. Stamenkovic, J. A. Ledbetter, and A. Aruffo. 1992. A 39-kDa protein on activated helper T cells binds CD40 and transduces the signal for cognate activation of B cells. Proc. Natl. Acad. Sci. USA 89:6550.
6. Parry, S. L., J. Hasbold, M. Holman, and G. G. B. Klaus. 1994. Hypercrosslinking surface IgM or IgD receptors on mature B cells induces apoptosis that is reversed by costimulation with IL-4 and anti-CD40. J. Immunol. 152:2821.
7. Banchereau, I., F. Bazan, D. Blanchard, F. Briere, J. P. Galizzi, C. van Kooten, Y. J. Liu, F. Rousset, and S. Saeland. 1994. The CD40 antigen and its ligand. Annu. Rev. Immunol. 12:881.
8. Lane, P., T. Brocker, S. Hubele, E. Padovan, A. Lanzavecchia, and F. McConnell. 1993. Soluble CD40 ligand can replace the normal T cell-derived CD40 ligand signal to B cells in T cell-dependent activation. J. Exp. Med. 177:1209.
9. Snapper, C. M., M. R. Kehry, B. E. Castle, and J. J. Mond. 1995. Multivalent, but not divalent, antigen receptor cross-linkers synergize with CD40 ligand for induction of Ig synthesis and class switching in normal murine B cells. J. Immunol. 154:1177.
10. Lederman, S., M. J. Yellin, A. M. Cleary, A. Pernis, G. Inghirami, L. E. Cohn, L. R. Covey, J. J. Lee, P. Rothman, and L. Chess. 1994. T-BAM/CD40-L on helper T lymphocytes augments lymphokine-induced B cell Ig isotype switch recombination and rescues B cells from programmed cell death. J. Immunol. 152:2163.
11. Hasbold, J., C. Johnson-Leger, C. J. Atkins, E. A. Clark, and G. G. B. Klaus. 1994. Properties of mouse CD40: cellular distribution of CD40 and B cell activation by monoclonal anti-mouse CD40 antibodies. Eur. J. Immunol. 24:1835.
12. Galibert, L., N. Burdin, B. de Saint-Vis, P. Gamme, C. V. Kooten, J. Banchereau, and F. Rousset. 1996. CD40 and B cell antigen receptor dual triggering of resting B lymphocytes turns on a partial germinal center phenotype. J. Exp. Med. 183:77.
13. Fanslow, W. C., D. M. Anderson, K. H. Grabstein, E. A. Clark, D. Cosman, and R. J. Armitage. 1992. Soluble forms of CD40 inhibit biologic responses of human B cells. J. Immunol. 149:655.
14. 1 phase restriction point. Mol. Cell. Biol. 10:3003.
15. Benhamou, L. E., P.-A. Cazenave, and P. Sarthou. 1990. Anti-immunoglobulins induce death by apoptosis in WEHI-231 B lymphoma cells. Eur. J. Immunol. 20:1405.
16. Hasbold, J., and G. B. Klaus. 1990. Anti-immunoglobulin antibodies induce apoptosis in immature B cell lymphomas. Eur. J. Immunol. 20:1685.
17. Tsubata, T., J. Wu, and T. Honjo. 1993. B-cell apoptosis induced by antigen receptor crosslinking is blocked by a T-cell signal through CD40. Nature 364: 645.
18. Heath, A. W., W. W. Wu, and M. C. Howard. 1994. Monoclonal antibodies to murine CD40 define two distinct functional epitopes. Eur. J. Immunol. 24:1828.
19. Santos-Argumedo, L., J. Gordon, A. W. Heath, and M. Howard. 1994. Antibodies to murine CD40 protect normal and malignant B cells from induced growth arrest. Cell. Immunol. 156:272.
20. Wang, Z., J. G. Karras, R. G. Howard, and T. L. Rothstein. 1995. Induction of bcl-x by CD40 engagement rescues sIg-induced apoptosis in murine B cells J. Immunol. 155:3722.
21. L, cdk4, and cdk6. J. Immunol. 155: 5527.
22. L in CD40-mediated rescue from anti-μ-induced apoptosis in WEHI-231 B lymphoma cells. Eur. J. Immunol. 25:1352.
23. L rescues WEHI-231 B lymphocytes from oxidant-mediated death following diverse apoptotic stimuli. J. Immunol. 155:66.
24. Cobb, M. H., T. G. Boulton, and D. J. Robbins. 1991. Extracellular signal-regulated kinases: ERKs in progress. Cell Regul. 2:965.
25. Welham, M. J., V. Duronio, J. S. Sanghera, S. L. Pelech, and J. W. Schrader. 1992. Multiple hemopoietic growth factors stimulate activation of mitogen-activated protein kinase family members. J. Biol. Chem. 267:1683.
26. Raingeaud, J., S. Gupta, J. S. Rogers, M. Dickens, J. Han, R. J. Ulevitch, and R. J. Davis. 1995. Pro-inflammatory cytokines and environmental stress cause p38 mitogen-activated protein kinase activation by dual phosphorylation on tyrosine and threonine. J. Biol. Chem. 270:7420.
27. Xia, Z., M. Dickens, J. Raingeaud, R. J. Davis, and M. E. Greenberg. 1995. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270: 1326.
28. Cano, E., and L. C. Mahadevan. 1995. Parallel signal processing among mammalian MAPKs. Trends Biochem. Sci. 20:117.
29. Cobb, M. H., and E. J. Goldsmith. 1995. How MAP kinases are regulated. J. Biol. Chem. 270:14843.
30. Karin, M. 1995. The regulation of AP-1 activity by mitogen-activated protein kinases. J. Biol. Chem. 270:16483.
31. ras oncoprotein. EMBO J. 11:569.
32. Koide, H., T. Satoh, M. Nakafuku, and Y. Kaziro. 1993. GTP-dependent association of Raf-1 with Ha-Ras: identification of Raf as a target downstream of Ras in mammalian cells. Proc. Natl. Acad Sci. USA 90:8683.
33. Cook, S. J., and F.. McCormick. 1993. Inhibition by cAMP of Ras-dependent activation of Raf. Science 262:1069.
34. Kryiakis, J. M., H. App, X.-F. Zhang, P. Banerjee, D. L. Brautigan, U. R. Rapp. and J. Avruch. 1992. Raf-1 activates MAP kinase-kinase. Nature 358:417.
35. Davis, R. J. 1993. The mitogen-activated protein kinase signal transduction pathway. J. Biol. Chem. 268:14553.
36. Hibi, M., A. Lin, T. Smeal, A. Minden, and M. Karin. 1993. Identification of an oncoprotein-and UV-responsive protein kinase that binds and potentiates the c-Jun activation domain. Genes Dev. 7:2135.
37. Kyriakis, J. M., P. Banerjee, E. Nikolakaki, T. Dai, E. A. Rubie, M. F. Ahmad, J. Avruch, and J. R. Woodgett. 1994. The stress-activated protein kinase sub-family of c-Jun kinases. Nature 369:156.
38. Galcheva-Gargova, Z., B. Derijard, I. H. Wu, and R. J. Davis. 1994. An osmosensing signal transduction pathway in mammalian cells. Science 265:806.
39. Sluss, H. K., T. Barrett, B. Derijard, and R. J. Davis. 1994. Signal transduction by tumor necrosis factor mediated by JNK protein kinases. Mol. Cell. Biol. 14: 8376.
40. Bird, T. A., J. M. Kryiakis, L. Tyshler, M. Gayle, A. Milne, and G. D. Virca. 1994. Interleukin-1 activates p54 mitogen-activated protein (MAP) kinase/stress-activated protein kinase by a pathway that is independent of p21ras, Raf-1, and MAP kinase kinase. J. Biol. Chem. 269:31836.
41. Cuenda, A., J. Rouse, Y. N. Doza, R. Meier, P. Cohen, T. F. Gallagher, P. R. Young, and J. C. Lee. 1995. SB203580 is a specific inhibitor of a MAP kinase homologue which is stimulated by cellular stresses and interleukin-1. FEBS Lett. 364:229.
42. Han, J., J. D. Lee, L. Bibbs, and R. J. Ulevitch. 1994. A MAP kinase targeted by endotoxin and hyperosmolarity in mammalian cells. Science 265:808.
43. Derijard, B., J. Raingeaud, T. Barrett, I.-H. Wu, J. Han, R. J. Ulevitch, and R. J. Davis. 1995. Independent human MAP kinase signal transduction pathways defined by MEK and MKK isoforms. Science 267:682.
44. Raingeaud. J., A. J. Whitmarsh, T. Barrett, B. Derijard, and R. J. Davis. 1996. MKK3- and MKK6-regulated gene expression is mediated by the p38 mitogen-activated protein kinase signal transduction pathway. Mol. Cell. Biol. 16:1247.
45. Derijard, B., M. Hibi, I. H. Wu, T. Barrett, B. Su, T. Deng, M. Karin, and R. J. Davis. 1994. JNK1: a protein kinase stimulated by UV light and Ha-ras that binds and phosphorylates the c-Jun activation domain. Cell 76:1025.
46. Kallunki, T., B. Su, I. Tsigelny, H. K. Sluss, B. Derijard, G. Moore, R. Davis, and M. Karin. 1994. JNK2 contains a specificity-determining region responsible for efficient c-Jun binding and phosphorylation. Genes Dev. 8:2996.
47. Smeal, T., M. Hibi, and M. Karin. 1994. Altering the specificity of signal transduction cascades: positive regulation of c-Jun transcriptional activity by protein kinase A. EMBO J. 13:6006.
48. Gupta, S., D. Campbell, B. Derijard, and R. J. Davis. 1995. Transcription factor ATF2 regulation by the JNK signal transduction pathway. Science 267:389.
49. Lee, J. C., J. T. Laydon, P. C. McDonnell, T. F. Gallagher, S. Kumar, D. Green, D. McNulty, M. J. Blumenthal, J. R. Heys, S. W. Landvatter, J. E. Strickler, M. M. McLaughlin, I. R. Siemens, S. M. Fisher, G. P. Livi, J. R. White, J. L. Adams, and P. R. Young. 1994. A protein kinase involved in the regulation of inflammatory cytokine biosynthesis. Nature 372:739.
50. Zervos, A. S., L. Faccio, J. P. Gatto, J. M, Kyriakis, and R. Brent. 1995. Mxi2, a mitogen-activated protein kinase that recognizes and phosphorylates Max protein. Proc. Natl. Acad. Sci. USA 92:10531.
51. Rouse, J., P. Cohen, S. Trigon, M. Morange, A. Alonso-Llamazares, D. Zamanillo, T. Hunt, and A. R. Nebreda. 1994. A novel kinase cascade triggered by stress and heat shock that stimulates MAPKAP kinase-2 and phosphorylation of the small heat shock proteins. Cell 78:1027.
52. Kumar, S., M. M. McLaughlin, P. C. McDonnell, J. C. Lee, G. P. Livi, and P. R. Young. 1995. Human mitogen-activated protein kinase CSBP1, but not CSBP2, complements a hog1 deletion in yeast. J. Biol. Chem. 270:29043.
53. Coso, O. A., M. Chiariello, G. Kalinec, J, M. Kyriakis, J. Woodgett, and J. S. Gutkind. 1995. Transforming G protein-coupled receptors potently activate JNK (SAPK). J. Biol. Chem. 270:5620.
54. Samuels, M. L., M. J. Weber, J. M. Bishop, and M. McMahon. 1993. Conditional transformation of cells and rapid activation of the mitogen-activated protein kinase cascade by an estradiol-dependent human Raf-1 protein kinase. Mol. Cell. Biol. 13:6241.
55. Gold, M. R., J. S. Sanghera, J. Stewart, and S. L. Pelech. 1992. Selective activation of p42 MAP kinase in murine B lymphoma cell lines by membrane immunoglobulin crosslinking: evidence for protein kinase C-independent and -dependent mechanisms of activation. Biochem. J. 287:269.
56. Minden, A., A. Lin, T. Smeal, B. Derijard, M. Cobb, R. Davis, and M. Karin. 1994. c-Jun-N-terminal phosphorylation correlates with activation of the JNK subgroup but not the ERK subgroup of mitogen-activated protein kinases. Mol. Cell. Biol. 14:6683.
57. Chou, S. Y., V. Baichwal, and J. E. Ferrell, Jr. 1992. Inhibition of c-Jun DNA binding by mitogen-activated protein kinase. Mol. Cell. Biol. 3:1117.
58. Su, B., E. Jacinto, M. Hibi, T. Kallunki, M. Karin, and Y. Ben-Neriah. 1994. JNK is involved in signal integration during costimulation of T lymphocytes. Cell 77:727.
59. Tordia, A., R. A. Franklin, H. Patel, A. M. Gardner, G. L. Johnson, and E. W. Gelfand. 1994. Cross-linking of surface IgM stimulates the Ras/Raf-1/MEK/ MAPK cascade in human B lymphocytes. J. Biol. Chem. 269:7538.
60. Kolch, W., G. Heidecker, G. Kochs, R. Hummel, H. Vahidi, H. Mischak, G. Finkenzeller, D. Marme, and U. R. Rapp. 1993. Protein kinase C alpha activates RAF-1 by direct phosphorylation. Nature 364:249.
61. Sakata, N., H. R. Patel, N. Terada, A. Aruffo, G. L. Johnson, and E. W. Gelfand. 1995. Selective activation of c-Jun kinase mitogen-activated protein kinase by CD40 on human B cells. J. Biol. Chem. 270:30823.
62. Lavoie, J. N., E. Hickey, L. A. Weber, and J. Landry. 1993. Modulation of actin micro-filament dynamics and fluid phase pinocytosis by phosphorylation of heat shock protein 27. J. Biol. Chem. 268:24210.
63. Berberich, I., G. Shu, F. Siebelt, J. R, Woodgett, J. M. Kyriakis, and E. A. Clark. 1996. Cross-linking CD40 on B cells preferentially induces stress-activated protein kinases rather than mitogen-activated protein kinases. EMBO J. 15:92.
64. Sanchez, I., R. T. Hughes, B. J. Mayer, K. Yee, J. R. Woodgett, J. Avruch, J. M. Kyriakis, and L. I. Zon. 1994. Role of SAPK/ERK kinase-1 in the stress-activated pathway regulating transcription factor c-Jun. Nature 372:794.
65. Derijard, B., J. Raingeaud, T. Barrett, I.-H. Wu, J. Han, R. J. Ulevitch, and R. J. Davis. 1995. Independent human MAP kinase signal transduction pathways defined by MEK and MKK isoforms. Science 267:682.
66. Lin, A., A. Minden, H. Martinetto, F.-X. Claret, C. A. Lange-Carter, F. Mercurio, G. L. Johnson, and M. Karin. 1995. Identification of a dual specificity kinase that activates the Jun kinases and p38-Mpk2. Science 268:286.
67. Lange-Carter, C. A., and G. L. Johnson. 1994. Ras-dependent growth factor regulation of MEK kinase in PC12 cells. Science 265:1458.
68. Coso, O. A., M. Chiariello, J.-C. Yu, H. Teramoto, P. Crespo, N. Xu, T. Miki, and J. S. Gutkind. 1995. The small GTP-binding proteins Rac1 and Cdc42 regulate the activity of the JNK/SAPK signaling pathway. Cell 81:1137.
69. Minden, A., A. Lin, F.-X. Claret, A. Abo, and M. Karin. 1995. Selective activation of the JNK signaling cascade and c-Jun transcriptional activity by the small GTPases Rac and cdc42Hs. Cell 81:1147.
70. Bagrodia, S., B. Derijard, R. J. Davis, and R. A. Cerione. 1995. Cdc42 and PAK-mediated signaling leads to Jun kinase and p38 mitogen-activated protein kinase activation. J. Biol. Chem. 270:27995.
71. Zhang, S., J. Han, M. A. Sells, J. Chernoff, U. G. Knaus, R. J. Ulevitch, and G. M. Bokoch. 1995. Rho family GTPases regulate p38 mitogen-aclivated protein kinase through the downstream mediator Pak1. J. Biol. Chem. 270:23934.
72. Pombo, C. M., J. H. Kehrl, I. Sanchez, P. Katz, J. Avruch, L. I. Zon, J. R. Woodgett, T. Force, and J. M. Kyriakis. 1995. Activation of the SAPK pathway by the human STE20 homologue germinal centre kinase. Nature 377:750.
73. Gille, H., A. Sharrocks, and P. Shaw. 1992. Phosphorylation of p62TCF by MAP kinase stimulates ternary complex formation at c-fos promoter. Nature 358:414.
74. Marias, R., J. Wynne, and R. Treisman. 1993. The SRF accessory protein Elk-1 contains a growth factor transcriptional activation domain. Cell 73:381.
75. Monroe, J. G. 1988. Up-regulation of c-fos expression is a component of the mIg signal transduction mechanism but is not indicative of competence for proliferation. J. Immunol. 140:1454.
76. Angel, P., and M. Karin. 1991. The role of Jun, Fos, and the AP-1 complex in cell proliferation and transformation. Biochim. Biophys. Acta 1072:129.
77. Deng, T., and M. Karin. 1994. c-Fos transcriptional activity stimulated by H-Ras-activated protein kinase distinct from JNK and ERK. Nature 371:171.