NF-κB family of transcription factors: Biochemical players of CD28 co-stimulation

Immunology Letters

Volumn 135, Issue 1-2, 2011, Pages 1-9

  Tuosto, Loretta ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

CD28 signalling; NF B; T cell survival

Indexed keywords

CD28 ANTIGEN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; T LYMPHOCYTE RECEPTOR;

CELL SURVIVAL; CYTOKINE PRODUCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; REVIEW; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

ANIMALS; ANTIGENS, CD28; CELL CYCLE; CELL SURVIVAL; CYTOKINES; HUMANS; LYMPHOCYTE ACTIVATION; NF-KAPPA B; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 78751701753     PISSN: 01652478     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.imlet.2010.09.005     Document Type: Review

References (119)

1. Hayden M.S., West A.P., Ghosh S. NF-kappaB and the immune response. Oncogene 2006, 25:6758-6780.
2. Karin M., Greten F.R. NF-kappaB: linking inflammation and immunity to cancer development and progression. Nat Rev Immunol 2005, 5:749-759.
3. Sen R., Baltimore D. Inducibility of kappa immunoglobulin enhancer-binding protein NF-kappa B by a posttranslational mechanism. Cell 1986, 47:921-928.
4. Hayden M.S., Ghosh S. Shared principles in NF-kappaB signaling. Cell 2008, 132:344-362.
5. Vallabhapurapu S., Karin M. Regulation and function of NF-kappaB transcription factors in the immune system. Annu Rev Immunol 2009, 27:693-733.
6. Karin M., Ben-Neriah Y. Phosphorylation meets ubiquitination: the control of NF-[kappa]B activity. Ann Rev Immunol 2000, 18:621-663.
7. DiDonato J.A., Rothwarf D.M., Zandi E., Karin M. A cytokine-responsive IkB kinase that activates the transcription factor NF-κB. Nature 1997, 388:548-554.
8. Reigner C.H., Song H.Y., Gao X., Goedell D.V., Cao Z., Rothe M. Identification and characterization of an IkB kinase. Cell 1997, 90:373-383.
9. Rothwarf D.M., Zandi E., Natoli G., Karin M. IKK-γ is essential regulatory subunit of the IκB kinase complex. Nature 1998, 395:297-300.
10. Woronicz J.D., Gao X., Cao Z., Rothe M., Goeddel D.V. IκB kinase β: NF-κB activation and complex formation with IκB kinase-α and NIK. Science 1997, 278:866-869.
11. Yamaoka S., Courtois G., Bessia C., Whiteside S.T., Weil R., Agou F., et al. Complementation cloning of NEMO, a component of the IkappaB kinase complex essential for NF-kappaB activation. Cell 1998, 93:1231-1240.
12. Zandi E., Rothwarf D.M., Delhase M., Hyakawa M., Karin M. The IκB kinase complex(IKK) contains two kinase subunits. IKKα and IKKβ, necessary for IκB phosphorylation and NF-κB activation. Cell 1997, 91:243-252.
13. Senftleben U., Cao Y., Xiao G., Greten F.R., Krahn G., Bonizzi G., et al. Activation by IKKα of a second evolutionary conserved, NF-κB signaling pathway. Science 2001, 293:1495-1499.
14. Coope H.J., Atkinson P.G.P., Huhse B., Belich M., Janzen J., Holman M.J., et al. CD40 regulates the processing of NF-κB2 p100 to p52. EMBO J 2002, 21:5375-5385.
15. Matsushima A., Kaisho T., Rennert P.D., Nakano H., Kurosawa K., Uchida D., et al. Essential role of nuclear factor (NF)-kappaB-inducing kinase and inhibitor of kappaB (IkappaB) kinase alpha in NF-kappaB activation through lymphotoxin beta receptor, but not through tumor necrosis factor receptor I. J Exp Med 2001, 193:631-636.
16. Yin L., Wu L., Wesche H., Arthur C.D., White J.M., Goeddel D.V., et al. Defective lymphotoxin-beta receptor-induced NF-kappaB transcriptional activity in NIK-deficient mice. Science 2001, 291:2162-2165.
17. Claudio E., Brown K., Park S., Wang H., Siebenlist U. BAFF-induced NEMO-independent processing of NF-kappa B2 in maturing B cells. Nat Immunol 2002, 3:958-965.
18. Novack D.V., Yin L., Hagen-Stapleton A., Schreiber R.D., Goeddel D.V., Ross F.P., et al. The IkappaB function of NF-kappaB2 p100 controls stimulated osteoclastogenesis. J Exp Med 2003, 198:771-781.
19. Saitoh T., Nakayama M., Nakano H., Yagita H., Yamamoto N., Yamaoka S. TWEAK induces NF-kappaB2 p100 processing and long lasting NF-kappaB activation. J Biol Chem 2003, 278:36005-36012.
20. Schmitz M.L., Krappmann D. Controlling NF-kappaB activation in T cells by costimulatory receptors. Cell Death Differ 2006, 13:834-842.
21. Schulze-Luehrmann J., Ghosh S. Antigen-receptor signaling to nuclear factor kappa B. Immunity 2006, 25:701-715.
22. Weil R., Israel A. Deciphering the pathway from the TCR to NF-kappaB. Cell Death Differ 2006, 13:826-833.
23. Kane L.P., Lin J., Weiss A. Signal transduction by the TCR for antigen. Curr Opin Immunol 2000, 12:242-249.
24. Horejsi V., Zhang W., Schraven B. Transmembrane adaptor proteins: organizers of immunoreceptor signalling. Nat Rev Immunol 2004, 4:603-616.
25. Tybulewicz V.L.J. Vav-family proteins in T-cell signalling. Current Opinion in Immunology 2005, 17:267-274.
26. Costello P.S., Walters A.E., Mee P.J., Turner M., Reynolds L.F., Prisco A., et al. The Rho-family GTP exchange factor Vav is a critical transducer of T cell receptor signals to the calcium. ERK, and NF-kappaB pathways. Proc Natl Acad Sci USA 1999, 96:3035-3040.
27. Herndon T.M., Shan X.C., Tsokos G.C., Wange R.L., ZAP-70 SLP-76 regulate protein kinase C-theta and NF-kappa B activation in response to engagement of CD3 and CD28. J Immunol 2001, 166:5654-5664.
28. Villalba M., Bi K., Hu J., Altman Y., Bushway P., Reits E., et al. Translocation of PKC[theta] in T cells is mediated by a nonconventional. PI3-K- and Vav-dependent pathway, but does not absolutely require phospholipase C. J Cell Biol 2002, 157.
29. Villalba M., Coudronniere N., Deckert M., Teixeiro E., Mas P., Altman A. A novel functional interaction between Vav and PKCtheta is required for TCR-induced T cell activation. Immunity 2000, 12:151-160.
30. Sun Z., Arendt C.W., Ellmeier W., Schaeffer E.M., Sunshine M.J., Gandhi L., et al. PKC-theta is required for TCR-induced NF-kappaB activation in mature but not immature T lymphocytes. Nature 2000, 404:402-407.
31. Bi K., Tanaka Y., Coudronniere N., Sugie K., Hong S., van Stipdonk M.J., et al. Antigen-induced translocation of PKC-theta to membrane rafts is required for T cell activation. Nat Immunol 2001, 2:556-563.
32. Sedwick C.E., Altman A. Perspectives on PKCtheta in T cell activation. Mol Immunol 2004, 41:675-686.
33. Khoshnan A., Bae D., Tindell C.A., Nel A.E. The physical association of protein kinase C theta with a lipid raft-associated inhibitor of kappa B factor kinase (IKK) complex plays a role in the activation of the NF-kappa B cascade by TCR and CD28. J Immunol 2000, 165:6933-6940.
34. Rebeaud F., Hailfinger S., Posevitz-Fejfar A., Tapernoux M., Moser R., Rueda D., et al. The proteolytic activity of the paracaspase MALT1 is key in T cell activation. Nat Immunol 2008, 9:272-281.
35. Tanner M.J., Hanel W., Gaffen S.L., Lin X. CARMA1 coiled-coil domain is involved in the oligomerization and subcellular localization of CARMA1 and is required for T cell receptor-induced NF-kappaB activation. J Biol Chem 2007, 282:17141-17147.
36. Wang D., Matsumoto R., You Y., Che T., Lin X.Y., Gaffen S.L., et al. CD3/CD28 costimulation-induced NF-kappaB activation is mediated by recruitment of protein kinase C-theta. Bcl10, and IkappaB kinase beta to the immunological synapse through CARMA1. Mol Cell Biol 2004, 24:164-171.
37. Thome M., Tschopp J., TCR-induced NF-kappaB activation: a crucial role for Carma1. Bcl10 and MALT1. Trends Immunol 2003, 24:419-424.
38. Li Y., Sedwick C.E., Hu J., Altman A. Role for protein kinase Ctheta (PKCtheta) in TCR/CD28-mediated signaling through the canonical but not the non-canonical pathway for NF-kappaB activation. J Biol Chem 2005, 280:1217-1223.
39. Lin X., O'Mahony A., Mu Y., Geleziunas R., Greene W.C. Protein kinase C-theta participates in NF-kappaB activation induced by CD3-CD28 costimulation through selective activation of IkappaB kinase beta. Mol Cell Biol 2000, 20:2933-2940.
40. 2+ mobilization and NFAT cell activation in primary mouse T cells. J Exp Med 2003, 197:1525-1535.
41. Lin X., Cunningham E.T., Mu Y., Geleziunas R., Greene W.C. The proto-oncogene Cot kinase participates in CD3/CD28 induction of NF-kappaB acting through the NF-kappaB-inducing kinase and IkappaB kinases. Immunity 1999, 10:271-280.
42. Matsumoto M., Yamada T., Yoshinaga S.K., Boone T., Horan T., Fujita S., et al. Essential role of NF-kappa B-inducing kinase in T cell activation through the TCR/CD3 pathway. J Immunol 2002, 169:1151-1158.
43. Tao L., Wadsworth S., Mercer J., Mueller C., Lynn K., Siekierka J., et al. Opposing roles of serine/threonine kinases MEKK1 and LOK in regulating the CD28 responsive element in T-cells. Biochem J 2002, 363:175-182.
44. Tuosto L., Costanzo A., Guido F., Marinari B., Vossio S., Moretti F., et al. Mitogen-activated kinase kinase kinase 1 regulates T cell receptor- and CD28-mediated signaling events which lead to NF-kappaB activation. Eur J Immunol 2000, 30:2445-2454.
45. Acuto O., Mise-Omata S., Mangino G., Michel F. Molecular modifiers of T cell antigen receptor triggering threshold: the mechanism of CD28 costimulatory receptor. Immunol Rev 2003, 192:21-31.
46. Rudd C.E., Taylor A., Schneider H. CD28 and CTLA-4 coreceptor expression and signal transduction. Immunol Rev 2009, 229:12-26.
47. Tuosto L., Acuto O. CD28 affects the earliest signaling events generated by TCR engagement. Eur J Immunol 1998, 28:2132-2142.
48. Viola A., Schroeder S., Sakakibara Y., Lanzavecchia A. T lymphocyte costimulation mediated by reorganization of membrane microdomains. Science 1999, 283:680-682.
49. Kundig T.M., Shahinian A., Kawai K., Mittrucker H.W., Sebzda E., Bachmann M.F., et al. Duration of TCR stimulation determines costimulatory requirement of T cells. Immunity 1996, 5:41-52.
50. Kane L.P., Lin Y., Weiss A. It's all Rel-ative: NF-kappaB and CD28 costimulation of T-cell activation. Trends Immunol 2002, 23:413-420.
51. Takeda K., Harada Y., Watanabe R., Inutake Y., Ogawa S., Onuki K., et al. CD28 stimulation triggers NF-kappaB activation through the CARMA1-PKCtheta-Grb2/Gads axis. Int Immunol 2008, 20:1507-1515.
52. August A., Dupont B. CD28 of T lymphocytes associates with phosphatidylinositol 3-kinase. Int Immunol 1994, 6:769-774.
53. Harada Y., Ohgai D., Watanabe R., Okano K., Koiwai O., Tanabe K., et al. A single amino acid alteration in cytoplasmic domain determines IL-2 promoter activation by ligation of CD28 but not inducible costimulator (ICOS). J Exp Med 2003, 197:257-262.
54. Pages F., Ragueneau M., Rottapel R., Truneh A., Nunes J., Imbert J., et al. Binding of phosphatidylinositol-3-OH kinase to CD28 is required for T-cell signalling. Nature 1994, 369:327-329.
55. Prasad K.V., Cai Y.C., Raab M., Duckworth B., Cantley L., Shoelson S.E., et al. T-cell antigen CD28 interacts with the lipid kinase phosphatidylinositol 3-kinase by a cytoplasmic Tyr(P)-Met-Xaa-Met motif. Proc Natl Acad Sci USA 1994, 91:2834-2838.
56. Truitt K.E., Hicks C.M., Imboden J.B. Stimulation of CD28 triggers an association between CD28 and phosphatidylinositol 3-kinase in Jurkat T cells. J Exp Med 1994, 179:1071-1076.
57. Holdford A.D., Green J.M., Levin S.D., Denny M.F., Straus D.B., Link P.S., et al. Proline residues in CD28 and the Src homology (SH)3 domain of Lck are required for T cell costimulation. J Exp Med 1999, 190:375-384.
58. Tavano R., Gri G., Molon B., Marinari B., Rudd C.E., Tuosto L., et al. CD28 and lipid rafts coordinate recruitment of Lck to the immunological synapse of human T lymphocytes. J Immunol 2004, 173:5392-5397.
59. Kim H.H., Tharayil M., Rudd C.E. Growth factor receptor-bound protein 2 SH2/SH3 domain binding to CD28 and its role in co-signaling. J Biol Chem 1998, 273:296-301.
60. Tavano R., Contento R.L., Baranda S.J., Soligo M., Tuosto L., Manes S., et al. CD28 interaction with filamin-A controls lipid raft accumulation at the T-cell immunological synapse. Nat Cell Biol 2006, 8:1270-1276.
61. Verweij C.L., Geerts M., Aarden L.A. Activation of interleukin-2 gene transcription via the T-cell surface molecule CD28 is mediated through an NF-κB-like response element. J Biol Chem 1991, 266:14179-14182.
62. Sanchez-Lockhart M., Marin E., Graf B., Abe R., Harada Y., Sedwick C.E., et al. Cutting edge: CD28-mediated transcriptional and posttranscriptional regulation of IL-2 expression are controlled through different signaling pathways. J Immunol 2004, 173:7120-7124.
63. Lemmon M.A. Pleckstrin homology domains: two halves make a hole?. Cell 2005, 120:574-576.
64. Lee K.Y., D'Acquisto F., Hayden M.S., Shim J.H., Ghosh S. PDK1 nucleates T cell receptor-induced signaling complex for NF-kappaB activation. Science 2005, 308:114-118.
65. Yokosuka T., Kobayashi W., Sakata-Sogawa K., Takamatsu M., Hashimoto-Tane A., Dustin M.L., et al. Spatiotemporal regulation of T cell costimulation by TCR-CD28 microclusters and protein kinase C theta translocation. Immunity 2008, 29:589-601.
66. Jones R.G., Parsons M., Bonnard M., Chan V.S., Yeh W.C., Woodgett J.R., et al. Protein kinase B regulates T lymphocyte survival, nuclear factor kappaB activation, and Bcl-X(L) levels in vivo. J Exp Med 2000, 191:1721-1734.
67. Kane L.P., Shapiro V.S., Stokoe D., Weiss A. Induction of NF-kappaB by the Akt/PKB kinase. Curr Biol 1999, 9:601-604.
68. Kane L.P., Abdres P.G., Howland K.C., Abbas A.K., Weiss A. Akt provides the CD28 costimulatory signal for up-regulation of IL-2 and IFN-gamma but not TH2 cytokines. Nat Immunol 2001, 2:37-44.
69. Parry R.V., Reif G., Smith D.M., Sanson B.A., Hemmings B.A., Ward S.G. Ligation of the T cell co-stimulatory receptor CD28 activates the serin-threonin protein kinase B. Eur J Immunol 1997, 27:2495-2501.
70. Kane L.P., Mollenauer M.N., Xu Z., Turck C.W., Weiss A. Akt-dependent phosphorylation specifically regulates Cot induction of NF-kappa B-dependent transcription. Mol Cell Biol 2002, 22:5962-5974.
71. Sanchez-Valdepenas C., Martin A.G., Ramakrishnan P., Wallach D., Fresno M. NF-kappaB-inducing kinase is involved in the activation of the CD28 responsive element through phosphorylation of c-Rel and regulation of its transactivating activity. J Immunol 2006, 176:4666-4674.
72. Sanchez-Valdepenas C., Punzon C., San-Antonio B., Martin A.G., Fresno M. Differential regulation of p65 and c-Rel NF-kappaB transactivating activity by Cot, protein kinase C zeta and NIK protein kinases in CD3/CD28 activated T cells. Cell Signal 2007, 19:528-537.
73. Bauer B., Krumbock N., Fresser F., Hochholdinger F., Spitaler M., Simm A., et al. Complex formation and cooperation of protein kinase C theta and Akt1/protein kinase B alpha in the NF-kappa B transactivation cascade in Jurkat T cells. J Biol Chem 2001, 276:31627-31634.
74. Narayan P., Holt B., Tosti R., Kane L.P. CARMA1 is required for Akt-mediated NF-kappaB activation in T cells. Mol Cell Biol 2006, 26:2327-2336.
75. Okkenhaug K., Rottapel R. Grb2 forms an inducible protein complex with CD28 through a Src homology 3 domain-proline interaction. J Biol Chem 1998, 273:21194-21202.
76. Schneider H., Cai Y.C., Prasad K.V., Shoelson S.E., Rudd C.E. T cell antigen CD28 binds to the GRB-2/SOS complex, regulators of p21ras. Eur J Immunol 1995, 25:1044-1050.
77. Sanchez-Lockhart M., Graf B., Miller J. Signals and sequences that control CD28 localization to the central region of the immunological synapse. J Immunol 2008, 181:7639-7648.
78. Michel F., Acuto O. CD28 costimulation: a source of Vav-1 for TCR signaling with the help of SLP-76?. Sci STKE 2002, 144:PE35.
79. Tuosto L., Michel F. Acuto O. p95vav associates with tyrosine-phosphorylated SLP-76 in antigen-stimulated T cells. J Exp Med 1996, 184:1161-1166.
80. Wu J., Motto D.G., Koretzky G.A., Weiss A., Vav SLP-76 interact and functionally cooperate in IL-2 gene activation. Immunity 1996, 4:593-602.
81. Dienz O., Hehner S.P., Droge W., Schmitz M.L. Synergistic activation of NF-kappa B by functional cooperation between vav and PKCtheta in T lymphocytes. J Biol Chem 2000, 275:24547-24551.
82. Marinari B., Costanzo A., Viola A., Michel F., Mangino G., Acuto O., et al. Vav cooperates with CD28 to induce NF-kappaB activation via a pathway involving Rac-1 and mitogen-activated kinase kinase 1. Eur J Immunol 2002, 32:447-456.
83. Hehner S.P., Hofmann T.G., Dienz O., Droge W., Schmitz M.L. Tyrosine-phosphorylated Vav1 as a point of integration for T-cell receptor- and CD28-mediated activation of JNK, p38, and interleukin-2 transcription. J Biol Chem 2000, 275:18160-18171.
84. Kaga S., Ragg S., Rogers K.A., Ochi A. Activation of p21-CDC42/Rac-activated kinases by CD28 signaling: p21-activated kinase (PAK) and MEK kinase 1 (MEKK1) may mediate the interplay between CD3 and CD28 signals. J Immunol 1998, 160:4182-4189.
85. Watanabe R., Harada Y., Takeda K., Takahashi J., Ohnuki K., Ogawa S., et al. Grb2 and Gads exhibit different interactions with CD28 and play distinct roles in CD28-mediated costimulation. J Immunol 2006, 177:1085-1091.
86. Annibaldi A., Sajeva A., Muscolini M., Ciccosanti F., Corazzari M., Piacentini M., et al. CD28 ligation in the absence of TCR promotes RelA/NF-kB recruitment and trans-activation of the HIV-1 LTR. Eur J Immunol 2008, 38:1446-1451.
87. Zhou A.X., Hartwig J.H., Akyurek L.M. Filamins in cell signaling, transcription and organ development. Trends Cell Biol 2010, 20:113-123.
88. Hayashi K., Altman A., Filamin A is required for T cell activation mediated by protein kinase C-theta. J Immunol 2006, 177:1721-1728.
89. Schwartz R.H. Costimulation of T lymphocytes: the role of CD28. CTLA-4, and B7/BB1 in interleukin-2 production and immunotherapy. Cell 1992, 71:1065-1068.
90. Kaga S., Ragg S., Rogers K.A., Ochi A. Stimulation of CD28 with B7-2 promotes focal adhesion-like contacts where Rho family small G proteins accumulate in T cells. J Immunol 1998, 160:24-27.
91. Michel F., Attal-Bonnefoy G., Mangino G., Mise-Omata S., Acuto O. CD28 as a molecular amplifier extending TCR ligation and signaling capabilities. Immunity 2001, 15:935-945.
92. Michel F., Mangino G., Attal-Bonnefoy G., Tuosto L., Alcover A., Roumier A., et al. CD28 utilizes Vav-1 to enhance TCR-proximal signaling and NF-AT activation. J Immunol 2000, 165:3820-3829.
93. Raab M., Pfister S., Rudd C.E. CD28 signaling via VAV/SLP-76 adaptors: regulation of cytokine transcription independent of TCR ligation. Immunity 2001, 15:921-933.
94. Nunès J., Klasen S., Ragueneau M., Pavon C., Couez D., Mawas C., et al. CD28 mAbs with distinct binding properties differ in their ability to induce T cell activation: analysis of early and late activation events. Int Immunol 1993, 5:311-315.
95. Luhder F., Huang Y., Dennehy K.M., Guntermann C., Muller I., Winkler E., et al. Topological requirements and signaling properties of T-cell activating, anti-CD28 antibody superagonists. J Exp Med 2003, 197:955-966.
96. Dennehy K.M., Elias F., Na S.-Y., Fischer K.-D., Hunig T., Luhder F. Mitogenic CD28 signals require the exchange factor vav1 to enhance TCR signaling at the SLP-76-Vav-Itk signalsome. J Immunol 2007, 178:1363-1371.
97. Waibler Z., Sender L.Y., Merten C., Hartig R., Kliche S., Gunzer M., et al. Signaling signatures and functional properties of anti-human CD28 superagonistic antibodies. PLoS One 2008, 3:e1708.
98. Beyersdorf N., Hanke T., Kerkau T., Hunig T. Superagonistic anti-CD28 antibodies: potent activators of regulatory T cells for the therapy of autoimmune diseases. Ann Rheum Dis 2005, 64(Suppl. 4):iv91-95.
99. Suntharalingam G., Perry M.R., Ward S., Brett S.J., Castello-Cortes A., Brunner M.D., et al. Cytokine storm in a phase 1 trial of the anti-CD28 monoclonal antibody TGN1412. N Engl J Med 2006, 355:1018-1028.
100. Piccolella E., Spadaro F., Ramoni C., Marinari B., Costanzo A., Levrero M., et al. Vav-1 and the IKK alpha subunit of I kappa B kinase functionally associate to induce NF-kappa B activation in response to CD28 engagement. J Immunol 2003, 170:2895-2903.
101. Marinari B., Costanzo A., Marzano V., Piccolella E., Tuosto L. CD28 delivers a unique signal leading to the selective recruitment of RelA and p52 NF-kappaB subunits on IL-8 and Bcl-xL gene promoters. Proc Natl Acad Sci USA 2004, 101:6098-6103.
102. Cao Y., Bonizzi G., Seagroves T.N., Greten F.R., Johnson R., Schmidt E.V., et al. IKKalpha provides an essential link between RANK signaling and cyclin D1 expression during mammary gland development. Cell 2001, 107:763-775.
103. Yamamoto Y., Verma U.N., Prajapati S., Kwak Y.T., Gaynor R.B. Histone H3 phosphorylation by IKK-alpha is critical for cytokine-induced gene expression. Nature 2003, 423:655-659.
104. Inami M., Yamashita M., Tenda Y., Hasegawa A., Kimura M., Hashimoto K., et al. CD28 costimulation controls histone hyperacetylation of the interleukin 5 gene locus in developing th2 cells. J Biol Chem 2004, 279:23123-23133.
105. Hoberg J.E., Popko A.E., Ramsey C.S., Mayo M.W. IkappaB kinase alpha-mediated derepression of SMRT potentiates acetylation of RelA/p65 by p300. Mol Cell Biol 2006, 26:457-471.
106. Boise L.H., Minn A.J., Noel P.J., June C.H., Accavitti M.A., Lindsten T., et al. CD28 costimulation can promote T cell survival by enhancing the expression of Bcl-XL. Immunity 1995, 3:87-98.
107. Kerstan A., Hunig T. Cutting edge: distinct TCR- and CD28-derived signals regulate CD95L.Bcl-xL, and the survival of primary T cells. J Immunol 2004, 172:1341-1345.
108. Khoshnan A., Tindell C., Laux I., Bae D., Bennett B., Nel A.E. The NF-kappa B cascade is important in Bcl-xL expression and for the anti-apoptotic effects of the CD28 receptor in primary human CD4+ lymphocytes. J Immunol 2000, 165:1743-1754.
109. Marsden V.S., Strasser A. Control of apoptosis in the immune system: Bcl-2, BH3-only proteins and more. Annu Rev Immunol 2003, 21:71-105.
110. Chao D.T., Korsmeyer S.J. BCL-XL-regulated apoptosis in T cell development. Int Immunol 1997, 9:1375-1384.
111. Wan Y.Y., DeGregori J. The survival of antigen-stimulated T cells requires NFkappaB-mediated inhibition of p73 expression. Immunity 2003, 18:331-342.
112. Lissy N.A., Davis P.K., Irwin M., Kaelin W.G., Dowdy S.F. A common E2F-1 and p73 pathway mediates cell death induced by TCR activation. Nature 2000, 407:642-645.
113. Melino G., De Laurenzi V., Vousden K.H. p73: friend or foe in tumorigenesis. Nat Rev Cancer 2002, 2:605-615.
114. Cosma M.P. Ordered recruitment: gene-specific mechanism of transcription activation. Mol Cell 2002, 10:227-236.
115. Cianfrocca R., Muscolini M., Marzano V., Annibaldi A., Marinari B., Levrero M., et al. RelA/NF-kappaB recruitment on the bax gene promoter antagonizes p73-dependent apoptosis in costimulated T cells. Cell Death Differ 2008, 15:354-363.
116. Burr J.S., Savage N.D., Messah G.E., Kimzey S.L., Shaw A.S., Arch R.H., et al. Cutting edge: distinct motifs within CD28 regulate T cell proliferation and induction of Bcl-XL. J Immunol 2001, 166:5331-5335.
117. Basu S. Akt inhibits DNA damage by suppressing p73, p53, Forkhead or all three?. Cell Cycle 2003, 2:69-70.
118. Tsuruta F, Masuyama N., Gotoh Y. The phosphatidylinositol 3-kinase (PI3K)-Akt pathway suppresses Bax translocation to mitochondria. J Biol Chem 2002, 277:14040-14047.
119. Taylor P.C. Antibody therapy for rheumatoid arthritis. Curr Opin Pharmacol 2003, 3:323-328.