Differential role of reactive oxygen species in the activation of mitogen-activated protein kinases and akt by key receptors on b-lymphocytes: Cd40, the b cell antigen receptor, and cxcr4

Journal of Cell Communication and Signaling

Volumn 1, Issue 1, 2007, Pages 33-43

  Lee, Rosaline L ^a   Westendorf, Jens ^a   Gold, Michael R ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Akt; B lymphocytes; BCR; CD40; CXCR4; MAP kinases; Reactive oxygen species

Indexed keywords

EID: 60649089324     PISSN: 18739601     EISSN: 1873961X     Source Type: Journal    
DOI: 10.1007/s12079-007-0006-y     Document Type: Article

References (82)

1. Adler V, Yin Z, Tew KD, Ronai Z (1999) Role of redox potential and reactive oxygen species in stress signaling. Oncogene 18:6104–6111
2. Aiba Y, Yamazaki T, Okada T, Gotoh K, Sanjo H, Ogata M, Kurosaki T (2006) BANK negatively regulates Akt activation and subsequent B cell responses. Immunity 24:259–268
3. Andjelic S, Hsia C, Suzuki H, Kadowaki T, Koyasu S, Liou HC (2000) Phosphatidylinositol 3-kinase and NF-kappa B/Rel are at the divergence of CD40-mediated proliferation and survival pathways. J Immunol 165:3860–3867
4. Aruoma OI, Halliwell B, Hoey BM, Butler J (1989) The antioxidant action of N-acetylcysteine: its reaction with hydrogen peroxide, hydroxyl radical, superoxide, and hypochlorous acid. Free Radic Biol Med 6:593–597
5. Asehnoune K, Strassheim D, Mitra S, Kim JY, Abraham E (2004) Involvement of reactive oxygen species in Toll-like receptor 4-dependent activation of NF-kappa B. J Immunol 172:2522–2529.
6. Banerji L, Glassford J, Lea NC, Thomas NS, Klaus GG, Lam EW (2001) BCR signals target p27(Kip1) and cyclin D2 via the PI3- K signalling pathway to mediate cell cycle arrest and apoptosis of WEHI 231 B cells. Oncogene 20:7352–7367
7. Berberich I, Shu G, Siebelt F, Woodgett JR, Kyriakis JM, Clark EA (1996) Cross-linking CD40 on B cells preferentially induces stress-activated protein kinases rather than mitogen-activated protein kinases. EMBO J 15:90–92
8. Bilancio A, Okkenhaug K, Camps M, Emery JL, Ruckle T, Rommel C, Vanhaesebroeck B (2006) Key role of the p110delta isoform of PI3K in B-cell antigen and IL-4 receptor signaling: comparative analysis of genetic and pharmacologic interference with p110delta function in B cells. Blood 107:642–650
9. Bishop GA, Haxhinasto SA, Stunz LL, Hostager BS (2003) Antigen-specific B-lymphocyte activation. Crit Rev Immunol 23:149–197
10. Bishop GA, Hostager BS (2003) The CD40-CD154 interaction in B cell-T cell liaisons. Cytokine Growth Factor Rev 14:297–309
11. Clayton E, Bardi G, Bell SE, Chantry D, Downes CP, Gray A, Humphries LA, Rawlings D, Reynolds H, Vigorito E, Turner M (2002) A crucial role for the p110delta subunit of phosphatidyl- Inositol 3-kinase in B cell development and activation. J Exp Med 196:753–763
12. Craxton A, Shu G, Graves JD, Saklatvala J, Krebs EG, Clark EA (1998) p38 MAPK is required for CD40-induced gene expression and proliferation in B lymphocytes. J Immunol 161:3225–3236
13. Dadgostar H, Zarnegar B, Hoffmann A, Qin XF, Truong U, Rao G, Baltimore D, Cheng G (2002) Cooperation of multiple signaling pathways in CD40-regulated gene expression in B lymphocytes. Proc Natl Acad Sci U S A 99:1497–1502
14. Daou GB, Srivastava AK (2004) Reactive oxygen species mediate Endothelin-1-induced activation of ERK1/2, PKB, and Pyk2 signaling, as well as protein synthesis, in vascular smooth muscle cells. Free Radic Biol Med 37:208–215
15. Devadas S, Zaritskaya L, Rhee SG, Oberley L, Williams MS (2002) Discrete generation of superoxide and hydrogen peroxide by T cell receptor stimulation: selective regulation of mitogen-activat-ed protein kinase activation and fas ligand expression. J Exp Med 195:59–70
16. Enomoto A, Murakami H, Asai N, Morone N, Watanabe T, Kawai K, Murakumo Y, Usukura J, Kaibuchi K, Takahashi M (2005) Akt/ PKB regulates actin organization and cell motility via Girdin/ APE. Dev Cell 9:389–402
17. Fang W, Rivard JJ, Ganser JA, LeBien TW, Nath KA, Mueller DL, Behrens TW (1995) Bcl-xL rescues WEHI 231 B lymphocytes from oxidant-mediated death following diverse apoptotic stimuli. J Immunol 155:66–75
18. Faruqi RM, Poptic EJ, Faruqi TR, De La Motte C, DiCorleto PE (1997) Distinct mechanisms for N-acetylcysteine inhibition of cytokine-induced E-selectin and VCAM-1 expression. Am J Physiol 273:H817–H826
19. Fedyk ER, Phipps RP (1994) Reactive oxygen species and not lipoxygenase products are required for mouse B-lymphocyte activation and differentiation. Int J Immunopharmacol 16: 533–546
20. Ganju RK, Brubaker SA, Meyer J, Dutt P, Yang Y, Qin S, Newman W, Groopman JE (1998) The alpha-chemokine, stromal cell-derived factor-1alpha, binds to the transmembrane G-protein-coupled CXCR-4 receptor and activates multiple signal transduction pathways. J Biol Chem 273:23169–23175
21. Gold MR (2002) To make antibodies or not: signaling by the B-cell antigen receptor. Trends Pharmacol Sci 23:316–324
22. Gold MR, Scheid MP, Santos L, Dang-Lawson M, Roth RA, Matsuuchi L, Duronio V, Krebs DL (1999) The B cell antigen receptor activates the Akt (protein kinase B)/glycogen synthase kinase-3 signaling pathway via phosphatidylinositol 3-kinase. J Immunol 163:1894–1905
23. Gorin Y, Kim NH, Feliers D, Bhandari B, Choudhury GG, Abboud HE (2001) Angiotensin II activates Akt/protein kinase B by an arachidonic acid/redox-dependent pathway and independent of phosphoinositide 3-kinase. FASEB J 15:1909–1920
24. Graves JD, Draves KE, Craxton A, Krebs EG, Clark EA (1998) A comparison of signaling requirements for apoptosis of human B lymphocytes induced by the B cell receptor and CD95/Fas. J Immunol 161:168–174
25. Griendling KK, Ushio-Fukai M (2000) Reactive oxygen species as mediators of angiotensin II signaling. Regulatory Pept 91:21–27
26. Grill B, Schrader JW (2002) Activation of Rac-1, Rac-2, and Cdc42 by hemopoietic growth factors or cross-linking of the B-lymphocyte receptor for antigen. Blood 100:3183–3192
27. Ha YJ, Lee JR (2004a) Role of TNF receptor-associated factor 3 in the CD40 signaling by production of reactive oxygen species through association with p40phox, a cytosolic subunit of nicotinamide adenine dinucleotide phosphate oxidase. J Immunol 172:231–239
28. Ha H, Kwak HB, Lee SW, Jin HM, Kim HM, Kim HH, Lee ZH (2004b) Reactive oxygen species mediate RANK signaling in osteoclasts. Exp Cell Res 301:119–127
29. Hamano T, Iwasaki T, Ogata A, Hashimoto N, Kakishita E (2002) The molecular mechanism in activation-induced cell death of an Ag-reactive B cell clone. Clin Exp Immunol 128:436–443
30. Hannken T, Schroeder R, Zahner G, Stahl RA, Wolf G (2000) Reactive oxygen species stimulate p44/42 mitogen-activated protein kinase and induce p27(Kip1): role in angiotensin II-mediated hypertrophy of proximal tubular cells. J Am Soc Nephrol 11:1387–1397
31. Harfouche R, Malak NA, Brandes RP, Karsan A, Irani K, Hussain SN (2005) Roles of reactive oxygen species in angiopoietin-1/tie-2 receptor signaling. FASEB J 19:1728–1730
32. Hargreaves DC, Hyman PL, Lu TT, Ngo VN, Bidgol A, Suzuki G, Zou YR, Littman DR, Cyster JG (2001) A coordinated change in chemokine responsiveness guides plasma cell movements. J Exp Med 194:45–56
33. Hashimoto A, Okada H, Jiang A, Kurosaki M, Greenberg S, Clark EA, Kurosaki T (1998) Involvement of guanosine triphosphatases and phospholipase C-gamma2 in extracellular signal-regulated kinase, c-Jun NH2-terminal kinase, and p38 mitogen-activated protein kinase activation by the B cell antigen receptor. J Exp Med 188:1287–1295
34. Hsu JH, Shi Y, Hu L, Fisher M, Franke TF, Lichtenstein A (2002) Role of the AKT kinase in expansion of multiple myeloma clones: effects on cytokine-dependent proliferative and survival responses. Oncogene 21:1391–1400
35. Ichijo H (1999) From receptors to stress-activated MAP kinases. Oncogene 18:6087–6093
36. Jabara HH, Geha RS (2005) Jun N-terminal kinase is essential for CD40-mediated IgE class switching in B cells. J Allergy Clin Immunol 115:856–863
37. Kane LP, Shapiro VS, Stokoe D, Weiss A (1999) Induction of NF-kappaB by the Akt/PKB kinase. Curr Biol 9:601–604
38. Karin M, Gallagher E (2005) From JNK to pay dirt: jun kinases, their biochemistry, physiology and clinical importance. IUBMB Life 57:283–295
39. Laxmanan S, Datta D, Geehan C, Briscoe DM, Pal S (2005) CD40: a mediator of pro- and anti-inflammatory signals in renal tubular epithelial cells. J Am Soc Nephrol 16:2714–2723
40. Lee JR, Koretzky GA (1998) Production of reactive oxygen intermediates following CD40 ligation correlates with c-Jun N-terminal kinase activation and IL-6 secretion in murine B lymphocytes. Eur J Immunol 28:4188–4197
41. Li F, Malik KU (2005) Angiotensin II-induced Akt activation is mediated by metabolites of arachidonic acid generated by CaMKII-stimulated Ca2(+)-dependent phospholipase A2. Am J Physiol Heart Circ Physiol 288:H2306–H2316
42. Liu H, Nishitoh H, Ichijo H, Kyriakis JM (2000) Activation of apoptosis signal-regulating kinase 1 (ASK1) by tumor necrosis factor receptor-associated factor 2 requires prior dissociation of the ASK1 inhibitor thioredoxin. Mol Cell Biol 20:2198–2208
43. Lo YY, Cruz TF (1995) Involvement of reactive oxygen species in cytokine and growth factor induction of c-fos expression in chondrocytes. J Biol Chem 270:11727–11730
44. Lo YY, Wong JM, Cruz TF (1996) Reactive oxygen species mediate cytokine activation of c-Jun NH2-terminal kinases. J Biol Chem 271:15703–15707
45. Lo IC, Shih JM, Jiang MJ (2005) Reactive oxygen species and ERK 1/2 mediate monocyte chemotactic protein-1-stimulated smooth muscle cell migration. J Biomed Sci 12:377–388
46. Ma Q, Jones D, Borghesani PR, Segal RA, Nagasawa T, Kishimoto T, Bronson RT, Springer TA (1998) Impaired B-lymphopoiesis, myelopoiesis, and derailed cerebellar neuron migration in CXCR4- and SDF-1-deficient mice. Proc Natl Acad Sci U S A 95:9448–9453
47. Manning BD, Cantley LC (2003) Rheb fills a GAP between TSC and TOR. Trends Biochem Sci 28:573–576
48. Matsuzawa A, Saegusa K, Noguchi T, Sadamitsu C, Nishitoh H, Nagai S, Koyasu S, Matsumoto K, Takeda K, Ichijo H (2005) ROS-dependent activation of the TRAF6-ASK1-p38 pathway is selectively required for TLR4-mediated innate immunity. Nat Immunol 6:587–592
49. McLeod SJ, Li AH, Lee RL, Burgess AE, Gold MR (2002) The Rap GTPases regulate B cell migration toward the chemokine stromal cell-derived factor-1 (CXCL12): potential role for Rap2 in promoting B cell migration. J Immunol 169:1365–1371
50. Miyasaka M, Tanaka T (2004) Lymphocyte trafficking across high endothelial venules: dogmas and enigmas. Nat Rev Immunol 4:360–370
51. Morrison DK, Davis RJ (2003) Regulation of MAP kinase signaling modules by scaffold proteins in mammals. Annu Rev Cell Dev Biol 19:91–118
52. Nagasawa T, Hirota S, Tachibana K, Takakura N, Nishikawa S, Kitamura Y, Yoshida N, Kikutani H, Kishimoto T (1996) Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature 382:635–638
53. Niiro H, Clark EA (2002) Regulation of B-cell fate by antigen-receptor signals. Nat Rev Immunol 2:945–956
54. Niu H, Ye BH, Della-Favera R (1998) Antigen receptor signaling induces MAP kinase-mediated phosphorylation and degradation of the BCL-6 transcription factor. Genes Dev 12:1953–1961
55. Ortolano S, Hwang IY, Han SB, Kehrl JH (2006) Roles for phosphoinositide 3-kinases, Bruton’s tyrosine kinase, and Jun kinases in B lymphocyte chemotaxis and homing. Eur J Immunol 36:1285–1295
56. Purkerson JM, Parker DC (1998) Differential coupling of membrane Ig and CD40 to the extracellularly regulated kinase signaling pathway. J Immunol 160:2121–2129
57. Qin S, Chock PB (2003) Implication of phosphatidylinositol 3-kinase membrane recruitment in hydrogen peroxide-induced activation of PI3K and Akt. Biochemistry 42:2995–3003
58. Reth M (2002) Hydrogen peroxide as second messenger in lymphocyte activation. Nat Immunol 3:1129–1134
59. Richards JD, Dave SH, Chou CH, Mamchak AA, DeFranco AL (2001) Inhibition of the MEK/ERK signaling pathway blocks a subset of B cell responses to antigen. J Immunol 166:3855–3864
60. Rolli V, Gallwitz M, Wossning T, Flemming A, Schamel WW, Zurn C, Reth M (2002) Amplification of B cell antigen receptor signaling by a Syk/ITAM positive feedback loop. Mol Cell 10:1057–1069
61. Rudelius M, Pittaluga S, Nishizuka S, Pham TH, Fend F, Jaffe ES, Quintanilla-Martinez L, Raffeld M (2006) Constitutive activation of Akt contributes to the pathogenesis and survival of mantle cell lymphoma. Blood 108:1668–1676
62. Saitoh M, Nishitoh H, Fujii M, Takeda K, Tobiume K, Sawada Y, Kawabata M, Miyazono K, Ichijo H (1998) Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J 17:2596–2606
63. Sakata N, Patel HR, Terada N, Aruffo A, Johnson GL, Gelfand EW (1995) Selective activation of c-Jun kinase mitogen-activated protein kinase by CD40 on human B cells. J Biol Chem 270:30823–30828
64. Santos-Argumedo L, Gordon J, Heath AW, Howard M (1994) Antibodies to murine CD40 protect normal and malignant B cells from induced growth arrest. Cell Immunol 156:272–285
65. Schauer SL, Wang Z, Sonenshein GE, Rothstein TL (1996) Maintenance of nuclear factor-kB/Rel and c-myc expression during CD40 ligand rescue of WEHI-231 early B cells from receptor-mediated apoptosis through modulation of IkB proteins. J Immunol 157:81–86
66. Schecter AD, Berman AB, Yi L, Mosoian A, McManus CM, Berman JW, Klotman ME, Taubman MB (2001) HIV envelope gp120 activates human arterial smooth muscle cells. Proc Natl Acad Sci U S A 98:10142–10147
67. Scheid MP, Woodgett JR (2001) PKB/AKT: functional insights from genetic models. Nat Rev Mol Cell Biol 2:760–768
68. Sies H (1993) Ebselen, a selenoorganic compound as glutathione peroxidase mimic. Free Radic Biol Med 14:313–323
69. Singh DK, Kumar D, Siddiqui Z, Basu SK, Kumar V, Rao KV (2005) The strength of receptor signaling is centrally controlled through a cooperative loop between Ca2+ and an oxidant signal. Cell 121:281–293
70. Song G, Ouyang G, Bao S (2005) The activation of Akt/PKB signaling pathway and cell survival. J Cell Mol Med 9:59–71
71. Sundaresan M, Yu ZX, Ferrans VJ, Irani K, Finkel T (1995) Requirement for generation of H2O2 for platelet-derived growth factor signal transduction. Science 270:296–299
72. Sutherland CL, Heath AW, Pelech SL, Young PR, Gold MR (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
73. Swart JM, Chiles TC (2000) Rescue of CH31 B cells from antigen receptor-induced apoptosis by inhibition of p38 MAPK. Biochem Biophys Res Commun 276:417–421
74. Takada E, Toyota H, Suzuki J, Mizuguchi J (2001) Prevention of anti-IgM-induced apoptosis accompanying G1 arrest in B lymphoma cells overexpressing dominant-negative mutant form of c-Jun N-terminal kinase 1. J Immunol 166:1641–1649
75. Tanaka K, Honda M, Takabatake T (2001) Redox regulation of MAPK pathways and cardiac hypertrophy in adult rat cardiac myocyte. J Am Coll Cardiol 37:676–685
76. Tome ME, Johnson DB, Rimsza LM, Roberts RA, Grogan TM, Miller TP, Oberley LW, Briehl MM (2005) A redox signature score identifies diffuse large B-cell lymphoma patients with a poor prognosis. Blood 106:3594–3601
77. Tonks NK (2005) Redox redux: revisiting PTPs and the control of cell signaling. Cell 121:667–670
78. Ushio-Fukai M, Alexander RW, Akers M, Griendling KK (1998) p38 Mitogen-activated protein kinase is a critical component of the redox-sensitive signaling pathways activated by angiotensin II. Role in vascular smooth muscle cell hypertrophy. J Biol Chem 273:15022–15029
79. Ushio-Fukai M, Alexander RW, Akers M, Yin Q, Fujio Y, Walsh K, Griendling KK (1999) Reactive oxygen species mediate the activation of Akt/protein kinase B by angiotensin II in vascular smooth muscle cells. J Biol Chem 274:22699–22704
80. Viedt C, Soto U, Krieger-Brauer HI, Fei J, Elsing C, Kubler W, Kreuzer J (2000) Differential activation of mitogen-activated protein kinases in smooth muscle cells by angiotensin II: involvement of p22phox and reactive oxygen species. Arterios-cler Thromb Vasc Biol 20:940–948
81. Yoon S, Seger R (2006) The extracellular signal-regulated kinase: multiple substrates regulate diverse cellular functions. Growth Factors 24:21–44
82. Zarubin T, Han J (2005) Activation and signaling of the p38 MAP kinase pathway. Cell Res 15:11–18