Regulation of PI-3-kinase and Akt signaling in T lymphocytes and other cells by TNFR family molecules

Frontiers in Immunology

Volumn 4, Issue JUN, 2013, Pages

  So, Takanori ^a   Croft, Michael ^b  

^a TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

Author keywords

Akt; PI3K; Signalosome; Tnfrsf; Tnfsf; Traf

Indexed keywords

B CELL ACTIVATING FACTOR RECEPTOR; CD134 ANTIGEN; CD137 LIGAND; CD28 ANTIGEN; CD40 ANTIGEN; HERPESVIRUS ENTRY MEDIATOR LIGAND; HLA DR3 ANTIGEN; INTERLEUKIN 1; MEMBRANE LIPID; NERVE GROWTH FACTOR RECEPTOR; OSTEOCLAST DIFFERENTIATION FACTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOINOSITIDE DEPENDENT PROTEIN KINASE 1; PROTEIN KINASE B; T LYMPHOCYTE RECEPTOR; TRANSMEMBRANE ACTIVATOR AND CAML INTERACTOR; TUMOR NECROSIS FACTOR RECEPTOR; TUMOR NECROSIS FACTOR RECEPTOR 2; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR;

ARTICLE; CELL DIFFERENTIATION; CELL EXPANSION; CELL FUNCTION; CELL SURVIVAL; CELLULAR IMMUNITY; CYTOLOGY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INTRACELLULAR SIGNALING; OLIGOMERIZATION; REGULATORY MECHANISM; T LYMPHOCYTE ACTIVATION;

EID: 84883768106     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2013.00139     Document Type: Article

References (133)

1. Aiba, Y., Yamazaki, T., Okada, T., Gotoh, K., Sanjo, H., Ogata, M., et al. (2006). BANK negatively regulates Akt activation and subsequent B cell responses. Immunity 24, 259-268. doi:10.1016/j.immuni.2006.01.002
2. Andjelic, S., Hsia, C., Suzuki, H., Kadowaki, T., Koyasu, S., and Liou, H. C. (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.
3. Ando, T., Ichikawa, J., Wako, M., Hatsushika, K., Watanabe, Y., Sakuma, M., et al. (2006). TWEAK/Fn14 interaction regulates RANTES production, BMP-2-induced differentiation, and RANKL expression in mouse osteoblastic MC3T3-E1 cells. Arthritis Res. Ther. 8, R146. doi:10.1186/ar2038
4. Arron, J. R., Pewzner-Jung, Y., Walsh, M. C., Kobayashi, T., and Choi, Y. (2002). Regulation of the subcellular localization of tumor necrosis factor receptor-associated factor (TRAF)2 by TRAF1 reveals mechanisms of TRAF2 signaling. J. Exp. Med. 196, 923-934. doi:10.1084/jem.20020774
5. Arron, J. R., Vologodskaia, M., Wong, B. R., Naramura, M., Kim, N., Gu, H., et al. (2001). A positive regulatory role for Cbl family proteins in tumor necrosis factor-related activation-induced cytokine (trance) and CD40L-mediated Akt activation. J. Biol. Chem. 276, 30011-30017. doi:10.1074/jbc. M100414200
6. Aspalter, R. M., Eibl, M. M., and Wolf, H. M. (2003). Regulation of TCR-mediated T cell activation by TNF-RII. J. Leukoc. Biol. 74, 572-582. doi:10.1189/jlb.0303112
7. Benson, R. J., Hostager, B. S., and Bishop, G. A. (2006). Rapid CD40-mediated rescue from CD95-induced apoptosis requires TNFR-associated factor-6 and PI3K. Eur. J. Immunol. 36, 2535-2543. doi:10.1002/eji.200535483
8. Bilderback, T. R., Gazula, V. R., Lisanti, M. P., and Dobrowsky, R. T. (1999). Caveolin interacts with Trk A and p75(NTR) and regulates neurotrophin signaling pathways. J. Biol. Chem. 274, 257-263. doi:10.1074/jbc.274.1.257
9. Bossen, C., Cachero, T. G., Tardivel, A., Ingold, K., Willen, L., Dobles, M., et al. (2008). TACI, unlike BAFF-R, is solely activated by oligomeric BAFF and APRIL to support survival of activated B cells and plasmablasts. Blood 111, 1004-1012. doi:10.1182/blood-2007-09-110874
10. Brown, S. A., Richards, C. M., Hanscom, H. N., Feng, S. L., and Winkles, J. A. (2003). The Fn14 cytoplasmic tail binds tumour-necrosis-factor-receptor-associated factors 1, 2, 3 and 5 and mediates nuclear factor-kappaB activation. Biochem. J. 371, 395-403. doi:10.1042/BJ20021730
11. Chan, F. K. (2007). Three is better than one: pre-ligand receptor assembly in the regulation of TNF receptor signaling. Cytokine 37, 101-107. doi:10.1016/j.cyto.2007.03.005
12. Chinnaiyan, A. M., O'Rourke, K., Yu, G. L., Lyons, R. H., Garg, M., Duan, D. R., et al. (1996). Signal transduction by DR3, a death domain-containing receptor related to TNFR-1 and CD95. Science 274, 990-992. doi:10.1126/science.274.5289.990
13. Croft, M. (2003). Co-stimulatory members of the TNFR family: keys to effective T-cell immunity? Nat. Rev. Immunol. 3, 609-620. doi:10.1038/nri1148
14. Croft, M. (2009). The role of TNF superfamily members in T-cell function and diseases. Nat. Rev. Immunol. 9, 271-285. doi:10.1038/nri2526
15. Croft, M. (2010). Control of immunity by the TNFR-related molecule OX40 (CD134). Annu. Rev. Immunol. 28, 57-78. doi:10.1146/annurev-immunol-030409-101243
16. Croft, M., So, T., Duan, W., and Soroosh, P. (2009). The significance of OX40 and OX40L to T-cell biology and immune disease. Immunol. Rev. 229, 173-191. doi:10.1111/j.1600-065X.2009.00766.x
17. Darnay, B. G., Ni, J., Moore, P. A., and Aggarwal, B. B. (1999). Activation of NF-kappaB by RANK requires tumor necrosis factor receptor-associated factor (TRAF) 6 and NF-kappaB-inducing kinase. Identification of a novel TRAF6 interaction motif. J. Biol. Chem. 274, 7724-7731. doi:10.1074/jbc.274.12.7724
18. Davies, C. C., Mak, T. W., Young, L. S., and Eliopoulos, A. G. (2005). TRAF6 is required for TRAF2-dependent CD40 signal transduction in nonhemopoietic cells. Mol. Cell. Biol. 25, 9806-9819. doi:10.1128/MCB.25.22.9806-9819.2005
19. Deregibus, M. C., Buttiglieri, S., Russo, S., Bussolati, B., and Camussi, G. (2003). CD40-dependent activation of phosphatidylinositol 3-kinase/Akt pathway mediates endothelial cell survival and in vitro angiogenesis. J. Biol. Chem. 278, 18008-18014. doi:10.1074/jbc. M300711200
20. Dykstra, M., Cherukuri, A., Sohn, H. W., Tzeng, S. J., and Pierce, S. K. (2003). Location is everything: lipid rafts and immune cell signaling. Annu. Rev. Immunol. 21, 457-481. doi:10.1146/annurev.immunol.21.120601.141021
21. Eggeling, C., Ringemann, C., Medda, R., Schwarzmann, G., Sandhoff, K., Polyakova, S., et al. (2009). Direct observation of the nanoscale dynamics of membrane lipids in a living cell. Nature 457, 1159-1162. doi:10.1038/nature07596
22. Faustman, D., and Davis, M. (2010). TNF receptor 2 pathway: drug target for autoimmune diseases. Nat. Rev. Drug Discov. 9, 482-493. doi:10.1038/nrd3030
23. Feng, X., Gaeta, M. L., Madge, L. A., Yang, J. H., Bradley, J. R., and Pober, J. S. (2001). Caveolin-1 associates with TRAF2 to form a complex that is recruited to tumor necrosis factor receptors. J. Biol. Chem. 276, 8341-8349. doi:10.1074/jbc. M007116200
24. Finlay, D., and Cantrell, D. (2011). The coordination of T-cell function by serine/threonine kinases. Cold Spring Harb. Perspect. Biol. 3, a002261. doi:10.1101/cshperspect.a002261
25. Fruman, D. A., and Bismuth, G. (2009). Fine tuning the immune response with PI3K. Immunol. Rev. 228, 253-272. doi:10.1111/j.1600-065X.2008.00750.x
26. Gommerman, J. L., and Summers deLuca, L. (2011). LTbetaR and CD40: working together in dendritic cells to optimize immune responses. Immunol. Rev. 244, 85-98. doi:10.1111/j.1600-065X.2011.01056.x
27. 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. doi:10.1111/j.1600-065X.2010.00932.x
28. Gramaglia, I., Jember, A., Pippig, S. D., Weinberg, A. D., Killeen, N., and Croft, M. (2000). The OX40 costimulatory receptor determines the development of CD4 memory by regulating primary clonal expansion. J. Immunol. 165, 3043-3050.
29. Grell, M., Douni, E., Wajant, H., Lohden, M., Clauss, M., Maxeiner, B., et al. (1995). The transmembrane form of tumor necrosis factor is the prime activating ligand of the 80 kDa tumor necrosis factor receptor. Cell 83, 793-802. doi:10.1016/0092-8674(95)90192-2
30. Gupta, M., Dillon, S. R., Ziesmer, S. C., Feldman, A. L., Witzig, T. E., Ansell, S. M., et al. (2009). A proliferation-inducing ligand mediates follicular lymphoma B-cell proliferation and cyclin D1 expression through phosphatidylinositol 3-kinase-regulated mammalian target of rapamycin activation. Blood 113, 5206-5216. doi:10.1182/blood-2008-09-179762
31. Ha, H., Kwak, H. B., Lee, S. K., Na, D. S., Rudd, C. E., Lee, Z. H., et al. (2003). Membrane rafts play a crucial role in receptor activator of nuclear factor kappaB signaling and osteoclast function. J. Biol. Chem. 278, 18573-18580. doi:10.1074/jbc. M212626200
32. Hanna, A. N., Chan, E. Y., Xu, J., Stone, J. C., and Brindley, D. N. (1999). A novel pathway for tumor necrosis factor-alpha and ceramide signaling involving sequential activation of tyrosine kinase, p21(ras), and phosphatidylinositol 3-kinase. J. Biol. Chem. 274, 12722-12729. doi:10.1074/jbc.274.18.12722
33. Haswell, L. E., Glennie, M. J., and Al-Shamkhani, A. (2001). Analysis of the oligomeric requirement for signaling by CD40 using soluble multimeric forms of its ligand, CD154. Eur. J. Immunol. 31, 3094-3100. doi:10.1002/1521-4141(2001010)31:10<3094::AIDIMMU3094>3.0.CO;2-F
34. Hatzoglou, A., Roussel, J., Bourgeade, M. F., Rogier, E., Madry, C., Inoue, J., et al. (2000). TNF receptor family member BCMA (B cell maturation) associates with TNF receptor-associated factor (TRAF) 1, TRAF2, and TRAF3 and activates NF-kappa B, elk-1, c-Jun N-terminal kinase, and p38 mitogen-activated protein kinase. J. Immunol. 165, 1322-1330.
35. Haxhinasto, S., Mathis, D., and Benoist, C. (2008). The AKT-mTOR axis regulates de novo differentiation of CD4+Foxp3+ cells. J. Exp. Med. 205, 565-574. doi:10.1084/jem.20071477
36. Hemingway, F., Kashima, T. G., Knowles, H. J., and Athanasou, N. A. (2013). Investigation of osteoclastogenic signalling of the RANKL substitute LIGHT. Exp. Mol. Pathol. 94, 380-385. doi:10.1016/j.yexmp.2013.01.003
37. Henley, T., Kovesdi, D., and Turner, M. (2008). B-cell responses to B-cell activation factor of the TNF family (BAFF) are impaired in the absence of PI3K delta. Eur. J. Immunol. 38, 3543-3548. doi:10.1002/eji.200838618
38. Hiraoka, E., Kawashima, S., Takahashi, T., Rikitake, Y., Kitamura, T., Ogawa, W., et al. (2001). TNF-alpha induces protein synthesis through PI3-kinase-Akt/PKB pathway in cardiac myocytes. Am. J. Physiol. Heart Circ. Physiol. 280, H1861-H1868.
39. Hosokawa, Y., Hosokawa, I., Ozaki, K., Nakae, H., and Matsuo, T. (2006). Proinflammatory effects of tumour necrosis factor-like weak inducer of apoptosis (TWEAK) on human gingival fibroblasts. Clin. Exp. Immunol. 146, 540-549. doi:10.1111/j.1365-2249.2006.03233.x
40. Hosokawa, Y., Hosokawa, I., Shindo, S., Ozaki, K., Nakae, H., and Matsuo, T. (2012). Tumor necrosis factor-like weak inducer of apoptosis increases CC chemokine ligand 20 production in interleukin 1beta-stimulated human gingival fibroblasts. Hum. Immunol. 73, 470-473. doi:10.1016/j.humimm.2012.02.021
41. 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. doi:10.1074/jbc. M909520199
42. Huang, C. S., Zhou, J., Feng, A. K., Lynch, C. C., Klumperman, J., Dearmond, S. J., et al. (1999). Nerve growth factor signaling in caveolae-like domains at the plasma membrane. J. Biol. Chem. 274, 36707-36714. doi:10.1074/jbc.274.51.36707
43. Huang, Y. H., and Sauer, K. (2010). Lipid signaling in T-cell development and function. Cold Spring Harb. Perspect. Biol. 2, a002428. doi:10.1101/cshperspect.a002428
44. Ibanez, C. F., and Simi, A. (2012). p75 Neurotrophin receptor signaling in nervous system injury and degeneration: paradox and opportunity. Trends Neurosci. 35, 431-440. doi:10.1016/j.tins.2012.03.007
45. Ingold, K., Zumsteg, A., Tardivel, A., Huard, B., Steiner, Q. G., Cachero, T. G., et al. (2005). Identification of proteoglycans as the APRIL-specific binding partners. J. Exp. Med. 201, 1375-1383. doi:10.1084/jem.20042309
46. Ishii, N., Takahashi, T., Soroosh, P., and Sugamura, K. (2010). OX40-OX40 ligand interaction in T-cell-mediated immunity and immunopathology. Adv. Immunol. 105, 63-98. doi:10.1016/S0065-2776(10)05003-0
47. Ito, T., Wang, Y. H., Duramad, O., Hanabuchi, S., Perng, O. A., Gilliet, M., et al. (2006). OX40 ligand shuts down IL-10-producing regulatory T cells. Proc. Natl. Acad. Sci. U.S.A. 103, 13138-13143. doi:10.1073/pnas.0603107103
48. Jackson, T. R., Blader, I. J., Hammonds-Odie, L. P., Burga, C. R., Cooke, F., Hawkins, P. T., et al. (1996). Initiation and maintenance of NGF-stimulated neurite outgrowth requires activation of a phosphoinositide 3-kinase. J. Cell Sci. 109(Pt 2), 289-300.
49. Jang, I. K., Lee, Z. H., Kim, Y. J., Kim, S. H., and Kwon, B. S. (1998). Human 4-1BB (CD137) signals are mediated by TRAF2 and activate nuclear factor-kappa B. Biochem. Biophys. Res. Commun. 242, 613-620. doi:10.1006/bbrc.1997.8016
50. Josefowicz, S. Z., Lu, L. F., and Rudensky, A. Y. (2012). Regulatory T cells: mechanisms of differentiation and function. Annu. Rev. Immunol. 30, 531-564. doi:10.1146/annurev.immunol.25.022106.141623
51. Kawamata, S., Hori, T., Imura, A., Takaori-Kondo, A., and Uchiyama, T. (1998). Activation of OX40 signal transduction pathways leads to tumor necrosis factor receptor-associated factor (TRAF) 2-and TRAF5-mediated NF-kappaB activation. J. Biol. Chem. 273, 5808-5814. doi:10.1074/jbc.273.10.5808
52. Khursigara, G., Orlinick, J. R., and Chao, M. V. (1999). Association of the p75 neurotrophin receptor with TRAF6. J. Biol. Chem. 274, 2597-2600. doi:10.1074/jbc.274.5.2597
53. Kim, E. Y., Priatel, J. J., Teh, S. J., and Teh, H. S. (2006). TNF receptor type 2 (p75) functions as a costimulator for antigen-driven T cell responses in vivo. J. Immunol. 176, 1026-1035.
54. Kim, E. Y., and Teh, H. S. (2001). TNF type 2 receptor (p75) lowers the threshold of T cell activation. J. Immunol. 167, 6812-6820.
55. Kim, E. Y., and Teh, H. S. (2004). Critical role of TNF receptor type-2 (p75) as a costimulator for IL-2 induction and T cell survival: a functional link to CD28. J. Immunol. 173, 4500-4509.
56. Kimberley, F. C., Van Bostelen, L., Cameron, K., Hardenberg, G., Marquart, J. A., Hahne, M., et al. (2009). The proteoglycan (heparan sulfate proteoglycan) binding domain of APRIL serves as a platform for ligand multimerization and cross-linking. FASEB J. 23, 1584-1595. doi:10.1096/fj.08-124669
57. Kumar, M., Makonchuk, D. Y., Li, H., Mittal, A., and Kumar, A. (2009). TNF-like weak inducer of apoptosis (TWEAK) activates proinflammatory signaling pathways and gene expression through the activation of TGF-beta-activated kinase 1. J. Immunol. 182, 2439-2448. doi:10.4049/jimmunol.0803357
58. Lasserre, R., Guo, X. J., Conchonaud, F., Hamon, Y., Hawchar, O., Bernard, A. M., et al. (2008). Raft nanodomains contribute to Akt/PKB plasma membrane recruitment and activation. Nat. Chem. Biol. 4, 538-547. doi:10.1038/nchembio.103
59. Lee, H. W., Nam, K. O., Park, S. J., and Kwon, B. S. (2003). 4-1BB enhances CD8+ T cell expansion by regulating cell cycle progression through changes in expression of cyclins D and E and cyclin-dependent kinase inhibitor p27kip1. Eur. J. Immunol. 33, 2133-2141. doi:10.1002/eji.200323996
60. Lee, H. W., Park, S. J., Choi, B. K., Kim, H. H., Nam, K. O., and Kwon, B. S. (2002). 4-1BB promotes the survival of CD8+ T lymphocytes by increasing expression of Bcl-xL and Bfl-1. J. Immunol. 169, 4882-4888.
61. Lee, S. H., Kim, E. J., Suk, K., Kim, I. S., and Lee, W. H. (2010). TL1A induces the expression of TGF-beta-inducible gene h3 (betaig-h3) through PKC, PI3K, and ERK in THP-1 cells. Cell. Immunol. 266, 61-66. doi:10.1016/j.cellimm.2010.08.013
62. Leibbrandt, A., and Penninger, J. M. (2008). RANK/RANKL: regulators of immune responses and bone physiology. Ann. N. Y. Acad. Sci. 1143, 123-150. doi:10.1196/annals.1443.016
63. Leonardi, A., Ellinger-Ziegelbauer, H., Franzoso, G., Brown, K., and Siebenlist, U. (2000). Physical and functional interaction of filamin (actin-binding protein-280) and tumor necrosis factor receptor-associated factor 2. J. Biol. Chem. 275, 271-278. doi:10.1074/jbc.275.1.271
64. Liu, Y., Xu, L., Opalka, N., Kappler, J., Shu, H. B., and Zhang, G. (2002). Crystal structure of sTALL-1 reveals a virus-like assembly of TNF family ligands. Cell 108, 383-394. doi:10.1016/S0092-8674(02)00631-1
65. Madireddi, S., Schabowsky, R. H., Srivastava, A. K., Sharma, R. K., Yolcu, E. S., and Shirwan, H. (2012). SA-4-1BBL costimulation inhibits conversion of conventional CD4+ T cells into CD4+ FoxP3+ T regulatory cells by production of IFN-gamma. PLoS ONE 7:e42459. doi:10.1371/journal.pone.0042459
66. Marchetti, L., Klein, M., Schlett, K., Pfizenmaier, K., and Eisel, U. L. (2004). Tumor necrosis factor (TNF)-mediated neuroprotection against glutamate-induced excitotoxicity is enhanced by N-methyl-D-aspartate receptor activation. Essential role of a TNF receptor 2-mediated phosphatidylinositol 3-kinase-dependent NF-kappa B pathway. J. Biol. Chem. 279, 32869-32881. doi:10.1074/jbc. M311766200
67. Marsters, S. A., Ayres, T. M., Skubatch, M., Gray, C. L., Rothe, M., and Ashkenazi, A. (1997). Herpesvirus entry mediator, a member of the tumor necrosis factor receptor (TNFR) family, interacts with members of the TNFR-associated factor family and activates the transcription factors NF-kappaB and AP-1. J. Biol. Chem. 272, 14029-14032. doi:10.1074/jbc.272.22.14029
68. Meylan, F., Richard, A. C., and Siegel, R. M. (2011). TL1A and DR3, a TNF family ligand-receptor pair that promotes lymphocyte costimulation, mucosal hyperplasia, and autoimmune inflammation. Immunol. Rev. 244, 188-196. doi:10.1111/j.1600-065X.2011.01068.x
69. Moreaux, J., Legouffe, E., Jourdan, E., Quittet, P., Reme, T., Lugagne, C., et al. (2004). BAFF and APRIL protect myeloma cells from apoptosis induced by interleukin 6 deprivation and dexamethasone. Blood 103, 3148-3157. doi:10.1182/blood-2003-06-1984
70. Muller, N., Wyzgol, A., Munkel, S., Pfizenmaier, K., and Wajant, H. (2008). Activity of soluble OX40 ligand is enhanced by oligomerization and cell surface immobilization. FEBS J. 275, 2296-2304. doi:10.1111/j.1742-4658.2008.06382.x
71. Nam, K. O., Kang, H., Shin, S. M., Cho, K. H., Kwon, B., Kwon, B. S., et al. (2005). Cross-linking of 4-1BB activates TCR-signaling pathways in CD8+ T lymphocytes. J. Immunol. 174, 1898-1905.
72. Novoyatleva, T., Diehl, F., Van Amerongen, M. J., Patra, C., Ferrazzi, F., Bellazzi, R., et al. (2010). TWEAK is a positive regulator of cardiomyocyte proliferation. Cardiovasc. Res. 85, 681-690. doi:10.1093/cvr/cvp360
73. Okkenhaug, K. (2013). Signaling by the phosphoinositide 3-kinase family in immune cells. Annu. Rev. Immunol. 31, 675-704. doi:10.1146/annurev-immunol-032712-095946
74. Osawa, Y., Banno, Y., Nagaki, M., Brenner, D. A., Naiki, T., Nozawa, Y., et al. (2001). TNF-alpha-induced sphingosine 1-phosphate inhibits apoptosis through a phosphatidylinositol 3-kinase/Akt pathway in human hepatocytes. J. Immunol. 167, 173-180.
75. Otipoby, K. L., Sasaki, Y., Schmidt-Supprian, M., Patke, A., Gareus, R., Pasparakis, M., et al. (2008). BAFF activates Akt and Erk through BAFF-R in an IKK1-dependent manner in primary mouse B cells. Proc. Natl. Acad. Sci. U.S.A. 105, 12435-12438. doi:10.1073/pnas.0805460105
76. Ozes, O. N., Mayo, L. D., Gustin, J. A., Pfeffer, S. R., Pfeffer, L. M., and Donner, D. B. (1999). NF-kappaB activation by tumour necrosis factor requires the Akt serine-threonine kinase. Nature 401, 82-85. doi:10.1038/43466
77. Pages, F., Ragueneau, M., Rottapel, R., Truneh, A., Nunes, J., Imbert, J., et al. (1994). Binding of phosphatidylinositol-3-OH kinase to CD28 is required for T-cell signalling. Nature 369, 327-329. doi:10.1038/369327a0
78. Park, Y. C., Burkitt, V., Villa, A. R., Tong, L., and Wu, H. (1999). Structural basis for self-association and receptor recognition of human TRAF2. Nature 398, 533-538. doi:10.1038/19110
79. Pastorino, J. G., Tafani, M., and Farber, J. L. (1999). Tumor necrosis factor induces phosphorylation and translocation of BAD through a phosphatidylinositide-3-OH kinase-dependent pathway. J. Biol. Chem. 274, 19411-19416. doi:10.1074/jbc.274.27.19411
80. Patke, A., Mecklenbrauker, I., Erdjument-Bromage, H., Tempst, P., and Tarakhovsky, A. (2006). BAFF controls B cell metabolic fitness through a PKC beta- and Akt-dependent mechanism. J. Exp. Med. 203, 2551-2562. doi:10.1084/jem.20060990
81. Pike, L. J., and Casey, L. (1996). Localization and turnover of phosphatidylinositol 4,5-bisphosphate in caveolin-enriched membrane domains. J. Biol. Chem. 271, 26453-26456. doi:10.1074/jbc.271.43.26453
82. Porquet, N., Poirier, A., Houle, F., Pin, A. L., Gout, S., Tremblay, P. L., et al. (2011). Survival advantages conferred to colon cancer cells by E-selectin-induced activation of the PI3K-NFkappaB survival axis downstream of Death receptor-3. BMC Cancer 11:285. doi:10.1186/1471-2407-11-285
83. Pullen, S. S., Miller, H. G., Everdeen, D. S., Dang, T. T., Crute, J. J., and Kehry, M. R. (1998). CD40-tumor necrosis factor receptor-associated factor (TRAF) interactions: regulation of CD40 signaling through multiple TRAF binding sites and TRAF hetero-oligomerization. Biochemistry 37, 11836-11845. doi:10.1021/bi981067q
84. Reddy, S. A., Huang, J. H., and Liao, W. S. (2000). Phosphatidylinositol 3-kinase as a mediator of TNF-induced NF-kappa B activation. J. Immunol. 164, 1355-1363.
85. Ren, C. L., Morio, T., Fu, S. M., and Geha, R. S. (1994). Signal transduction via CD40 involves activation of lyn kinase and phosphatidylinositol-3-kinase, and phosphorylation of phospholipase C gamma 2. J. Exp. Med. 179, 673-680. doi:10.1084/jem.179.2.673
86. 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. doi:10.1111/j.1600-065X.2011.01067.x
87. Rogers, P. R., Song, J., Gramaglia, I., Killeen, N., and Croft, M. (2001). OX40 promotes Bcl-xL and Bcl-2 expression and is essential for long-term survival of CD4 T cells. Immunity 15, 445-455. doi:10.1016/S1074-7613(01)00191-1
88. Rothe, M., Wong, S. C., Henzel, W. J., and Goeddel, D. V. (1994). A novel family of putative signal transducers associated with the cytoplasmic domain of the 75 kDa tumor necrosis factor receptor. Cell 78, 681-692. doi:10.1016/0092-8674(94)90532-0
89. Sanz, A. B., Sanchez-Nino, M. D., Izquierdo, M. C., Jakubowski, A., Justo, P., Blanco-Colio, L. M., et al. (2009). Tweak induces proliferation in renal tubular epithelium: a role in uninephrectomy induced renal hyperplasia. J. Cell. Mol. Med. 13, 3329-3342. doi:10.1111/j.1582-4934.2009.00766.x
90. Sauer, S., Bruno, L., Hertweck, A., Finlay, D., Leleu, M., Spivakov, M., et al. (2008). T cell receptor signaling controls Foxp3 expression via PI3K, Akt, and mTOR. Proc. Natl. Acad. Sci. U.S.A. 105, 7797-7802. doi:10.1073/pnas.0800928105
91. Schreiber, T. H., Wolf, D., Tsai, M. S., Chirinos, J., Deyev, V. V., Gonzalez, L., et al. (2010). Therapeutic Treg expansion in mice by TNFRSF25 prevents allergic lung inflammation. J. Clin. Invest. 120, 3629-3640. doi:10.1172/JCI42933
92. Shu, H. B., and Johnson, H. (2000). B cell maturation protein is a receptor for the tumor necrosis factor family member TALL-1. Proc. Natl. Acad. Sci. U.S.A. 97, 9156-9161. doi:10.1073/pnas.160213497
93. Snell, L. M., Lin, G. H., McPherson, A. J., Moraes, T. J., and Watts, T. H. (2011). T-cell intrinsic effects of GITR and 4-1BB during viral infection and cancer immunotherapy. Immunol. Rev. 244, 197-217. doi:10.1111/j.1600-065X.2011.01063.x
94. So, T., Choi, H., and Croft, M. (2011a). OX40 complexes with phosphoinositide 3-kinase and protein kinase B (PKB) to augment TCR-dependent PKB signaling. J. Immunol. 186, 3547-3555. doi:10.4049/jimmunol.1003156
95. So, T., Soroosh, P., Eun, S. Y., Altman, A., and Croft, M. (2011b). Antigen-independent signalosome of CARMA1, PKCtheta, and TNF receptor-associated factor 2 (TRAF2) determines NF-kappaB signaling in T cells. Proc. Natl. Acad. Sci. U.S.A. 108, 2903-2908. doi:10.1073/pnas.1008765108
96. So, T., and Croft, M. (2007). Cutting edge: OX40 inhibits TGF-beta- and antigen-driven conversion of naive CD4 T cells into CD25+Foxp3+ T cells. J. Immunol. 179, 1427-1430.
97. So, T., Lee, S. W., and Croft, M. (2006). Tumor necrosis factor/tumor necrosis factor receptor family members that positively regulate immunity. Int. J. Hematol. 83, 1-11. doi:10.1532/IJH97.05120
98. So, T., Lee, S. W., and Croft, M. (2008). Immune regulation and control of regulatory T cells by OX40 and 4-1BB. Cytokine Growth Factor Rev. 19, 253-262. doi:10.1016/j.cytogfr.2008.04.003
99. Soltoff, S. P., Rabin, S. L., Cantley, L. C., and Kaplan, D. R. (1992). Nerve growth factor promotes the activation of phosphatidylinositol 3-kinase and its association with the trk tyrosine kinase. J. Biol. Chem. 267, 17472-17477.
100. Song, J., Salek-Ardakani, S., Rogers, P. R., Cheng, M., Van Parijs, L., and Croft, M. (2004). The costimulation-regulated duration of PKB activation controls T cell longevity. Nat. Immunol. 5, 150-158. doi:10.1038/ni1030
101. Song, J., So, T., Cheng, M., Tang, X., and Croft, M. (2005). Sustained survivin expression from OX40 costimulatory signals drives T cell clonal expansion. Immunity 22, 621-631. doi:10.1016/j.immuni.2005.03.012
102. Soroosh, P., Doherty, T. A., So, T., Mehta, A. K., Khorram, N., Norris, P. S., et al. (2011). Herpesvirus entry mediator (TNFRSF14) regulates the persistence of T helper memory cell populations. J. Exp. Med. 208, 797-809. doi:10.1084/jem.20101562
103. Starck, L., Scholz, C., Dorken, B., and Daniel, P. T. (2005). Costimulation by CD137/4-1BB inhibits T cell apoptosis and induces Bcl-xL and c-FLIP(short) via phosphatidylinositol 3-kinase and AKT/protein kinase B. Eur. J. Immunol. 35, 1257-1266. doi:10.1002/eji.200425686
104. Steinberg, M. W., Cheung, T. C., and Ware, C. F. (2011). The signaling networks of the herpesvirus entry mediator (TNFRSF14) in immune regulation. Immunol. Rev. 244, 169-187. doi:10.1111/j.1600-065X.2011.01064.x
105. Stone, G. W., Barzee, S., Snarsky, V., Kee, K., Spina, C. A., Yu, X. F., et al. (2006). Multimeric soluble CD40 ligand and GITR ligand as adjuvants for human immunodeficiency virus DNA vaccines. J. Virol. 80, 1762-1772. doi:10.1128/JVI.80.4.1762-1772.2006
106. Takano, R., Hisahara, S., Namikawa, K., Kiyama, H., Okano, H., and Miura, M. (2000). Nerve growth factor protects oligodendrocytes from tumor necrosis factor-alpha-induced injury through Akt-mediated signaling mechanisms. J. Biol. Chem. 275, 16360-16365. doi:10.1074/jbc. M910419199
107. Vaillant, A. R., Mazzoni, I., Tudan, C., Boudreau, M., Kaplan, D. R., and Miller, F. D. (1999). Depolarization and neurotrophins converge on the phosphatidylinositol 3-kinase-Akt pathway to synergistically regulate neuronal survival. J. Cell Biol. 146, 955-966. doi:10.1083/jcb.146.5.955
108. Vidalain, P. O., Azocar, O., Servet-Delprat, C., Rabourdin-Combe, C., Gerlier, D., and Manie, S. (2000). CD40 signaling in human dendritic cells is initiated within membrane rafts. EMBO J. 19, 3304-3313. doi:10.1093/emboj/19.13.3304
109. Vilar, M., Charalampopoulos, I., Kenchappa, R. S., Simi, A., Karaca, E., Reversi, A., et al. (2009). Activation of the p75 neurotrophin receptor through conformational rearrangement of disulphide-linked receptor dimers. Neuron 62, 72-83. doi:10.1016/j.neuron.2009.02.020
110. Vinay, D. S., and Kwon, B. S. (2012). Immunotherapy of cancer with 4-1BB. Mol. Cancer Ther. 11, 1062-1070. doi:10.1158/1535-7163.MCT-11-0677
111. Viola, A., and Gupta, N. (2007). Tether and trap: regulation of membrane-raft dynamics by actin-binding proteins. Nat. Rev. Immunol. 7, 889-896. doi:10.1038/nri2193
112. Vu, M. D., Xiao, X., Gao, W., Degauque, N., Chen, M., Kroemer, A., et al. (2007). OX40 costimulation turns offFoxp3+ Tregs. Blood 110, 2501-2510. doi:10.1182/blood-2007-01-070748
113. Ware, C. F., and Sedy, J. R. (2011). TNF Superfamily Networks: bidirectional and interference pathways of the herpesvirus entry mediator (TNFSF14). Curr. Opin. Immunol. 23, 627-631. doi:10.1016/j.coi.2011.08.008
114. Watts, T. H. (2005). TNF/TNFR family members in costimulation of T cell responses. Annu. Rev. Immunol. 23, 23-68. doi:10.1146/annurev.immunol.23.021704.115839
115. Wei, C. Y., Chou, Y. H., Ho, F. M., Hsieh, S. L., and Lin, W. W. (2006). Signaling pathways of LIGHT induced macrophage migration and vascular smooth muscle cell proliferation. J. Cell. Physiol. 209, 735-743. doi:10.1002/jcp.20742
116. Wong, B. R., Besser, D., Kim, N., Arron, J. R., Vologodskaia, M., Hanafusa, H., et al. (1999). TRANCE, a TNF family member, activates Akt/PKB through a signaling complex involving TRAF6 and c-Src. Mol. Cell 4, 1041-1049. doi:10.1016/S1097-2765(00)80232-4
117. Wong, B. R., Josien, R., Lee, S. Y., Vologodskaia, M., Steinman, R. M., and Choi, Y. (1998). The TRAF family of signal transducers mediates NF-kappaB activation by the TRANCE receptor. J. Biol. Chem. 273, 28355-28359. doi:10.1074/jbc.273.43.28355
118. Woodland, R. T., Fox, C. J., Schmidt, M. R., Hammerman, P. S., Opferman, J. T., Korsmeyer, S. J., et al. (2008). Multiple signaling pathways promote B lymphocyte stimulator dependent B-cell growth and survival. Blood 111, 750-760. doi:10.1182/blood-2007-03-077222
119. Wyzgol, A., Muller, N., Fick, A., Munkel, S., Grigoleit, G. U., Pfizenmaier, K., et al. (2009). Trimer stabilization, oligomerization, and antibody-mediated cell surface immobilization improve the activity of soluble trimers of CD27L, CD40L, 41BBL, and glucocorticoid-induced TNF receptor ligand. J. Immunol. 183, 1851-1861. doi:10.4049/jimmunol.0802597
120. Xia, X. Z., Treanor, J., Senaldi, G., Khare, S. D., Boone, T., Kelley, M., et al. (2000). TACI is a TRAF-interacting receptor for TALL-1, a tumor necrosis factor family member involved in B cell regulation. J. Exp. Med. 192, 137-143. doi:10.1084/jem.192.1.137
121. Xing, L., Venegas, A. M., Chen, A., Garrett-Beal, L., Boyce, B. F., Varmus, H. E., et al. (2001). Genetic evidence for a role for Src family kinases in TNF family receptor signaling and cell survival. Genes Dev. 15, 241-253. doi:10.1101/gad.840301
122. Xu, L. G., and Shu, H. B. (2002). TNFR-associated factor-3 is associated with BAFF-R and negatively regulates BAFF-R-mediated NF-kappa B activation and IL-10 production. J. Immunol. 169, 6883-6889.
123. Yang, W. L., Wang, J., Chan, C. H., Lee, S. W., Campos, A. D., Lamothe, B., et al. (2009). The E3 ligase TRAF6 regulates Akt ubiquitination and activation. Science 325, 1134-1138. doi:10.1126/science.1175065
124. Yao, R., and Cooper, G. M. (1995). Requirement for phosphatidylinositol-3 kinase in the prevention of apoptosis by nerve growth factor. Science 267, 2003-2006. doi:10.1126/science.7701324
125. Ye, X., Mehlen, P., Rabizadeh, S., Vanarsdale, T., Zhang, H., Shin, H., et al. (1999). TRAF family proteins interact with the common neurotrophin receptor and modulate apoptosis induction. J. Biol. Chem. 274, 30202-30208. doi:10.1074/jbc.274.42.30202
126. Yu, Q., Kovacs, C., Yue, F. Y., and Ostrowski, M. A. (2004). The role of the p38 mitogen-activated protein kinase, extracellular signal-regulated kinase, and phosphoinositide-3-OH kinase signal transduction pathways in CD40 ligand-induced dendritic cell activation and expansion of virus-specific CD8+ T cell memory responses. J. Immunol. 172, 6047-6056.
127. Zhang, G. (2004). Tumor necrosis factor family ligand-receptor binding. Curr. Opin. Struct. Biol. 14, 154-160. doi:10.1016/j.sbi.2004.03.003
128. Zhang, H. G., Wang, Y., Xie, J. F., Liang, X., Liu, D., Yang, P., et al. (2001). Regulation of tumor necrosis factor alpha-mediated apoptosis of rheumatoid arthritis synovial fibroblasts by the protein kinase Akt. Arthritis Rheum. 44, 1555-1567. doi:10.1002/1529-0131(200107)44:7<1555::AIDART279>3.0.CO;2-M
129. Zhang, Q., Cui, F., Fang, L., Hong, J., Zheng, B., and Zhang, J. Z. (2013). TNF-alpha impairs differentiation and function of TGF-beta-induced Treg cells in autoimmune diseases through Akt and Smad3 signaling pathway. J. Mol. Cell Biol. 5, 85-98. doi:10.1093/jmcb/mjs063
130. Zhang, R., Xu, Y., Ekman, N., Wu, Z., Wu, J., Alitalo, K., et al. (2003a). Etk/Bmx transactivates vascular endothelial growth factor 2 and recruits phosphatidylinositol 3-kinase to mediate the tumor necrosis factor-induced angiogenic pathway. J. Biol. Chem. 278, 51267-51276. doi:10.1074/jbc. M310678200
131. Zhang, Z., Jimi, E., and Bothwell, A. L. (2003b). Receptor activator of NF-kappa B ligand stimulates recruitment of SHP-1 to the complex containing TNFR-associated factor 6 that regulates osteoclastogenesis. J. Immunol. 171, 3620-3626.
132. Zhou, Z., Song, X., Berezov, A., Zhang, G., Li, Y., Zhang, H., et al. (2008). Human glucocorticoid-induced TNF receptor ligand regulates its signaling activity through multiple oligomerization states. Proc. Natl. Acad. Sci. U.S.A. 105, 5465-5470. doi:10.1073/pnas.0711350105
133. Zonca, M., Mancheno-Corvo, P., Delarosa, O., Manes, S., Buscher, D., Lombardo, E., et al. (2012). APRIL and BAFF proteins increase proliferation of human adipose-derived stem cells through activation of Erk1/2 MAP kinase. Tissue Eng. Part A 18, 852-859. doi:10.1089/ten.tea.2011.0316