In CD28-costimulated human naïve CD4+ T cells, I-κB kinase controls the expression of cell cycle regulatory proteins via interleukin-2-independent mechanisms

Immunology

Volumn 131, Issue 2, 2010, Pages 231-241

  Lupino, Elisa ^a   Buccinnà, Barbara ^a   Ramondetti, Cristina ^a   Lomartire, Annarosa ^a   De Marco, Giovanni ^a   Ricotti, Emanuela ^a   Tovo, Pier Angelo ^a   Rinaudo, Maria T ^a   Piccinini, Marco ^a  

^a UNIVERSITY OF TURIN   (Italy)

Author keywords

CD28; CD4+ T cells; cell cycle; I B kinase; I B kinase inhibitors; interleukin 2

Indexed keywords

4 (2 AMINOETHYLAMINO) 1,8 DIMETHYLIMIDAZO[1,2 A]QUINOXALINE; 6 CHLORO 8 NICOTINAMIDO BETA CARBOLINE; CD28 ANTIGEN; CYCLIN D3; CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE INHIBITOR 1B; CYCLIN E; F BOX PROTEIN; I KAPPA B KINASE; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR; S PHASE KINASE ASSOCIATED PROTEIN 2;

ARTICLE; AUTOCRINE EFFECT; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL CYCLE REGULATION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE RELEASE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEGRADATION; REAL TIME POLYMERASE CHAIN REACTION; T LYMPHOCYTE ACTIVATION;

ACTIVE TRANSPORT, CELL NUCLEUS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD28; ANTIGENS, CD3; CARRIER PROTEINS; CD4-POSITIVE T-LYMPHOCYTES; CELL CYCLE; CELL CYCLE PROTEINS; CELL PROLIFERATION; CYCLIN D3; CYCLIN E; CYCLIN-DEPENDENT KINASE 2; CYCLIN-DEPENDENT KINASES; GENE EXPRESSION; GENE EXPRESSION REGULATION; HETEROCYCLIC COMPOUNDS, 3-RING; HUMANS; I-KAPPA B KINASE; I-KAPPA B PROTEINS; IMIDAZOLES; INTERLEUKIN-2; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LYMPHOCYTE ACTIVATION; NF-KAPPA B; ONCOGENE PROTEINS; PROTEIN KINASE INHIBITORS; PYRIDINES; QUINOXALINES; S-PHASE KINASE-ASSOCIATED PROTEINS; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 77956318018     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/j.1365-2567.2010.03297.x     Document Type: Article

References (50)

1. Murray AW. Recycling the cell cycle: cyclins revisited. Cell 2004 116 : 221 234.
2. Mohapatra S, Agrawal D, Pledger WJ. p27Kip1 regulates T cell proliferation. J Biol Chem 2001 276 : 21976 21983.
3. Appleman LJ, Berezovskaya A, Grass I, Boussiotis VA. CD28 costimulation mediates T cell expansion via IL-2-independent and IL-2-dependent regulation of cell cycle progression. J Immunol 2000 164 : 144 151.
4. Sherr CJ, Roberts JM. CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev 1999 13 : 1501 1512.
5. Malumbres M, Barbacid M. Mammalian cyclin-dependent kinases. Trends Biochem Sci 2005 30 : 630 641.
6. Carrano AC, Eytan E, Hershko A, Pagano M. SKP2 is required for ubiquitin-mediated degradation of the CDK inhibitor p27. Nat Cell Biol 1999 1 : 193 199.
7. Sutterluty H, Chatelain E, Marti A, Wirbelauer C, Senften M, Muller U, Krek W. p45SKP2 promotes p27Kip1 degradation and induces S phase in quiescent cells. Nat Cell Biol 1999 1 : 207 214.
8. Ganoth D, Bornstein G, Ko TK, Larsen B, Tyers M, Pagano M, Hershko A. The cell-cycle regulatory protein Cks1 is required for SCF(Skp2)-mediated ubiquitinylation of p27. Nat Cell Biol 2001 3 : 321 324.
9. Spruck C, Strohmaier H, Watson M, Smith AP, Ryan A, Krek TW, Reed SI. A CDK-independent function of mammalian Cks1: targeting of SCF(Skp2) to the CDK inhibitor p27Kip1. Mol Cell 2001 7 : 639 650.
10. Pagano M, Tam SW, Theodoras AM et al. Role of the ubiquitin-proteasome pathway in regulating abundance of the cyclin-dependent kinase inhibitor p27. Science 1995 269 : 682 685.
11. Schmitz ML, Krappmann D. Controlling NF-kappaB activation in T cells by costimulatory receptors. Cell Death Differ 2006 13 : 834 842.
12. Huang Y, Wange RL. T cell receptor signaling: beyond complex complexes. J Biol Chem 2004 279 : 28827 28830.
13. Weil R, Israel A. Deciphering the pathway from the TCR to NF-kappaB. Cell Death Differ 2006 13 : 826 833.
14. Schulze-Luehrmann J, Ghosh S. Antigen-receptor signaling to nuclear factor kappa B. Immunity 2006 25 : 701 715.
15. Vallabhapurapu S, Karin M. Regulation and function of NF-kappaB transcription factors in the immune system. Annu Rev Immunol 2009 27 : 693 733.
16. Perkins ND. Integrating cell-signalling pathways with NF-kappaB and IKK function. Nat Rev Mol Cell Biol 2007 8 : 49 62.
17. Kim HP, Imbert J, Leonard WJ. Both integrated and differential regulation of components of the IL-2/IL-2 receptor system. Cytokine Growth Factor Rev 2006 17 : 349 366.
18. Shapiro VS, Truitt KE, Imboden JB, Weiss A. CD28 mediates transcriptional upregulation of the interleukin-2 (IL-2) promoter through a composite element containing the CD28RE and NF-IL-2B AP-1 sites. Mol Cell Biol 1997 17 : 4051 4058.
19. Thompson CB, Lindsten T, Ledbetter JA, Kunkel SL, Young HA, Emerson SG, Leiden JM, June CH. CD28 activation pathway regulates the production of multiple T-cell-derived lymphokines/cytokines. Proc Natl Acad Sci U S A 1989 86 : 1333 1337.
20. Shahinian A, Pfeffer K, Lee KP et al. Differential T cell costimulatory requirements in CD28-deficient mice. Science 1993 261 : 609 612.
21. Schorle H, Holtschke T, Hunig T, Schimpl A, Horak I. Development and function of T cells in mice rendered interleukin-2 deficient by gene targeting. Nature 1991 352 : 621 624.
22. Tivol EA, Borriello F, Schweitzer AN, Lynch WP, Bluestone JA, Sharpe AH. Loss of CTLA-4 leads to massive lymphoproliferation and fatal multiorgan tissue destruction, revealing a critical negative regulatory role of CTLA-4. Immunity 1995 3 : 541 547.
23. Iezzi G, Karjalainen K, Lanzavecchia A. The duration of antigenic stimulation determines the fate of naive and effector T cells. Immunity 1998 8 : 89 95.
24. Colombetti S, Basso V, Mueller DL, Mondino A. Prolonged TCR/CD28 engagement drives IL-2-independent T cell clonal expansion through signaling mediated by the mammalian target of rapamycin. J Immunol 2006 176 : 2730 2738.
25. Burke JR, Pattoli MA, Gregor KR et al. BMS-345541 is a highly selective inhibitor of I kappa B kinase that binds at an allosteric site of the enzyme and blocks NF-kappa B-dependent transcription in mice. J Biol Chem 2003 278 : 1450 1456.
26. Castro AC, Dang LC, Soucy F et al. Novel IKK inhibitors: beta-carbolines. Bioorg Med Chem Lett 2003 13 : 2419 2422.
27. + regulatory T cells and their therapeutic potential. Annu Rev Med 2006 57 : 381 402.
28. Riccardi C, Nicoletti I. Analysis of apoptosis by propidium iodide staining and flow cytometry. Nat Protoc 2006 1 : 1458 1461.
29. Garfin DE. One-dimensional gel electrophoresis. In : Deutscher MP, ed. Methods in Enzymology. Guide to Protein Purification. San Diego : Academic Press 1990 182 : 425 441.
30. Schagger H, von Jagow G. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 1987 166 : 368 379.
31. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002 3 : RESEARCH0034.
32. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001 25 : 402 408.
33. Appleman LJ, Chernova I, Li L, Boussiotis VA. CD28 costimulation mediates transcription of SKP2 and CKS1, the substrate recognition components of SCFSkp2 ubiquitin ligase that leads p27kip1 to degradation. Cell Cycle 2006 5 : 2123 2129.
34. Bashir T, Pagano M. Don't skip the G1 phase: how APC/CCdh1 keeps SCFSKP2 in check. Cell Cycle 2004 3 : 850 852.
35. Diehn M, Alizadeh AA, Rando OJ, Liu CL, Stankunas K, Botstein D, Crabtree GR, Brown PO. Genomic expression programs and the integration of the CD28 costimulatory signal in T cell activation. Proc Natl Acad Sci U S A 2002 99 : 11796 11801.
36. Hess K, Yang Y, Golech S, Sharov A, Becker KG, Weng NP. Kinetic assessment of general gene expression changes during human naive CD4+ T cell activation. Int Immunol 2004 16 : 1711 1721.
37. Safford M, Collins S, Lutz MA et al. Egr-2 and Egr-3 are negative regulators of T cell activation. Nat Immunol 2005 6 : 472 480.
38. Ajchenbaum F, Ando K, DeCaprio JA, Griffin JD. Independent regulation of human D-type cyclin gene expression during G1 phase in primary human T lymphocytes. J Biol Chem 1993 268 : 4113 4119.
39. Martino A, Holmes JHt, Lord JD, Moon JJ, Nelson BH. Stat5 and Sp1 regulate transcription of the cyclin D2 gene in response to IL-2. J Immunol 2001 166 : 1723 1729.
40. Joshi I, Minter LM, Telfer J et al. Notch signaling mediates G1/S cell-cycle progression in T cells via cyclin D3 and its dependent kinases. Blood 2009 113 : 1689 1698.
41. Harper JW. Protein destruction: adapting roles for Cks proteins. Curr Biol 2001 11 : R431 5.
42. Skp2/Cks1 ubiquitin-protein isopeptide ligase. J Biol Chem 2007 282 : 15462 15470.
43. Lin HK, Wang G, Chen Z et al. Phosphorylation-dependent regulation of cytosolic localization and oncogenic function of Skp2 by Akt/PKB. Nat Cell Biol 2009 11 : 420 432.
44. Gao D, Inuzuka H, Tseng A, Chin RY, Toker A, Wei W. Phosphorylation by Akt1 promotes cytoplasmic localization of Skp2 and impairs APCCdh1-mediated Skp2 destruction. Nat Cell Biol 2009 11 : 397 408.
45. Karin M, Yamamoto Y, Wang QM. The IKK NF-kappa B system: a treasure trove for drug development. Nat Rev Drug Discov 2004 3 : 17 26.
46. Bain J, Plater L, Elliott M et al. The selectivity of protein kinase inhibitors: a further update. Biochem J 2007 408 : 297 315.
47. Abe MK, Saelzler MP, Espinosa R III., Kahle KT, Hershenson MB, Le Beau MM, Rosner MR. ERK8, a new member of the mitogen-activated protein kinase family. J Biol Chem 2002 277 (19 16733 16743.
48. Schmidt-Supprian M, Tian J, Grant EP et al. Differential dependence of CD4+CD25+ regulatory and natural killer-like T cells on signals leading to NF-kappaB activation. Proc Natl Acad Sci U S A 2004 101 : 4566 4571.
49. Boothby MR, Mora AL, Scherer DC, Brockman JA, Ballard DW. Perturbation of the T lymphocyte lineage in transgenic mice expressing a constitutive repressor of nuclear factor (NF)-kappaB. J Exp Med 1997 185 : 1897 1907.
50. Ferreira V, Sidenius N, Tarantino N, Hubert P, Chatenoud L, Blasi F, Korner M. In vivo inhibition of NF-kappa B in T-lineage cells leads to a dramatic decrease in cell proliferation and cytokine production and to increased cell apoptosis in response to mitogenic stimuli, but not to abnormal thymopoiesis. J Immunol 1999 162 : 6442 50.