ADAP and SKAP55 deficiency suppresses PD-1 expression in CD8+ cytotoxic T lymphocytes for enhanced anti-tumor immunotherapy

EMBO Molecular Medicine

Volumn 7, Issue 6, 2015, Pages 754-769

  Li, Chunyang ^a   Li, Weiyun ^a   Xiao, Jun ^a,b   Jiao, Shaozhuo ^a   Teng, Fei ^a   Xue, Shengjie ^a   Zhang, Chi ^a   Sheng, Chun ^b   Leng, Qibin ^c   Rudd, Christopher E ^d   Wei, Bin ^e   Wang, Hongyan ^a  

^a INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^b SHANGHAI NORMAL UNIVERSITY   (China)

^c INSTITUTE PASTEUR OF SHANGHAI   (China)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e WUHAN INSTITUTE OF VIROLOGY   (China)

Author keywords

ADAP SKAP55; Anti tumor immunotherapy; CsA; CTL cytotoxicity; PD 1

Indexed keywords

ADAPTOR PROTEIN; ADHESION AND DEGRANULATION PROMOTING ADAPTOR PROTEIN; CALCIUM ION; CD4 ANTIGEN; CYCLOSPORIN A; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; PROGRAMMED DEATH 1 RECEPTOR; PROTEIN SKAP55; PROTEIN TYROSINE KINASE; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG; FYB PROTEIN, MOUSE; MEMBRANE PROTEIN; PDCD1 PROTEIN, MOUSE; PHOSPHOPROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SKAP55 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER IMMUNOTHERAPY; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; DOWN REGULATION; LYMPHOCYTE COUNT; LYMPHOCYTIC INFILTRATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; TUMOR GROWTH; WILD TYPE; ANIMAL; CYTOTOXIC T LYMPHOCYTE; DEFICIENCY; IMMUNOLOGY; IMMUNOTHERAPY; KNOCKOUT MOUSE; METABOLISM; NEOPLASMS; PROCEDURES;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; IMMUNOTHERAPY; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; NEOPLASMS; PHOSPHOPROTEINS; PROGRAMMED CELL DEATH 1 RECEPTOR; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84930177783     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.15252/emmm.201404578     Document Type: Article

References (59)

1. Agnellini P, Wolint P, Rehr M, Cahenzli J, Karrer U, Oxenius A (2007) Impaired NFAT nuclear translocation results in split exhaustion of virus-specific CD8(+) T cell functions during chronic viral infection. Proc Natl Acad Sci USA 104: 4565-4570
2. Barber DL, Wherry EJ, Masopust D, Zhu B, Allison JP, Sharpe AH, Freeman GJ, Ahmed R (2006) Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439: 682-687
3. Bhardwaj N (2007) Harnessing the immune system to treat cancer. J Clin Invest 117: 1130-1136
4. Blank C, Brown I, Peterson AC, Spiotto M, Iwai Y, Honjo T, Gajewski TF (2004) PD-L1/B7H-1 inhibits the effector phase of tumor rejection by T Cell Receptor (TCR) transgenic CD8+ T Cells. Cancer Res 64: 1140-1145
5. Brahmer JR, Tykodi SS, Chow LQM, Hwu W-J, Topalian SL, Hwu P, Drake CG, Camacho LH, Kauh J, Odunsi K et al (2012) Safety and activity of Anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 366: 2455-2465
6. Chemnitz JM, Parry RV, Nichols KE, June CH, Riley JL (2004) SHP-1 and SHP-2 associate with immunoreceptor tyrosine-based switch motif of programmed death 1 upon primary human T cell stimulation, but only receptor ligation prevents T cell activation. J Immunol 173: 945-954
7. Curiel TJ, Wei S, Dong H, Alvarez X, Cheng P, Mottram P, Krzysiek R, Knutson KL, Daniel B, Zimmermann MC et al (2003) Blockade of B7-H1 improves myeloid dendritic cell-mediated antitumor immunity. Nat Med 9: 562-567
8. Ding Z-C, Huang L, Blazar BR, Yagita H, Mellor AL, Munn DH, Zhou G (2012) Polyfunctional CD4(+) T cells are essential for eradicating advanced B-cell lymphoma after chemotherapy. Blood 120: 2229-2239
9. Dotti G (2009) Blocking PD-1 in cancer immunotherapy. Blood 114: 1457-1458
10. Duke-Cohan JS, Kang H, Liu H, Rudd CE (2006) Regulation and function of SKAP-55 non-canonical motif binding to the SH3c domain of adhesion and degranulation-promoting adaptor protein. J Biol Chem 281: 13743-13750
11. Duraiswamy J, Kaluza KM, Freeman GJ, Coukos G (2013) Dual blockade of PD-1 and CTLA-4 combined with tumor vaccine effectively restores T Cell rejection function in tumors. Cancer Res 73: 3591-3603
12. Filby A, Seddon B, Kleczkowska J, Salmond R, Tomlinson P, Smida M, Lindquist JA, Schraven B, Zamoyska R (2007) Fyn regulates the duration of TCR engagement needed for commitment to effector function. J Immunol 179: 4635-4644
13. Flanagan WM, Corthesy B, Bram RJ, Crabtree GR (1991) Nuclear association of a T-cell transcription factor blocked by FK-506 and cyclosporin A. Nature 352: 803-807
14. Franciszkiewicz K, Le Floc'h A, Boutet M, Vergnon I, Schmitt A, Mami-Chouaib F (2013) CD103 or LFA-1 engagement at the immune synapse between cytotoxic T cells and tumor cells promotes maturation and regulates T-cell effector functions. Cancer Res 73: 617-628
15. de Goër de Herve MG, Jaafoura S, Vallée M, Taoufik Y (2012) FoxP3+ regulatory CD4 T cells control the generation of functional CD8 memory. Nat Commun 3: 986
16. Gravitz L (2013) Cancer immunotherapy. Nature 504: S1-S1
17. Griffiths EK, Krawczyk C, Kong YY, Raab M, Hyduk SJ, Bouchard D, Chan VS, Kozieradzki I, Oliveira-Dos-Santos AJ, Wakeham A et al (2001) Positive regulation of T cell activation and integrin adhesion by the adapter Fyb/Slap. Science 293: 2260-2263
18. Gubin MM, Zhang X, Schuster H, Caron E, Ward JP, Noguchi T, Ivanova Y, Hundal J, Arthur CD, Krebber W-J et al (2014) Checkpoint blockade cancer immunotherapy targets tumour-specific mutant antigens. Nature 515: 577-581
19. Ha SJ, Mueller SN, Wherry EJ, Barber DL, Aubert RD, Sharpe AH, Freeman GJ, Ahmed R (2008) Enhancing therapeutic vaccination by blocking PD-1-mediated inhibitory signals during chronic infection. J Exp Med 205: 543-555
20. Hamanishi J, Mandai M, Iwasaki M, Okazaki T, Tanaka Y, Yamaguchi K, Higuchi T, Yagi H, Takakura K, Minato N et al (2007) Programmed cell death 1 ligand 1 and tumor-infiltrating CD8+ T lymphocytes are prognostic factors of human ovarian cancer. Proc Natl Acad Sci USA 104: 3360-3365
21. Hansel TT, Kropshofer H, Singer T, Mitchell JA, George AJT (2010) The safety and side effects of monoclonal antibodies. Nat Rev Drug Discov 9: 325-338
22. Herbst RS, Soria J-C, Kowanetz M, Fine GD, Hamid O, Gordon MS, Sosman JA, McDermott DF, Powderly JD, Gettinger SN et al (2014) Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients. Nature 515: 563-567
23. Huang Y, Norton DD, Precht P, Martindale JL, Burkhardt JK, Wange RL (2005) Deficiency of ADAP/Fyb/SLAP-130 destabilizes SKAP55 in Jurkat T cells. J Biol Chem 280: 23576-23583
24. Jo EK, Wang H, Rudd CE (2005) An essential role for SKAP-55 in LFA-1 clustering on T cells that cannot be substituted by SKAP-55R. J Exp Med 201: 1733-1739
25. Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG (2010) Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol 8: e1000412
26. Kliche S, Breitling D, Togni M, Pusch R, Heuer K, Wang X, Freund C, Kasirer-Friede A, Menasche G, Koretzky GA et al (2006) The ADAP/SKAP55 signaling module regulates T-cell receptor-mediated integrin activation through plasma membrane targeting of Rap1. Mol Cell Biol 26: 7130-7144
27. Kwon J, Qu CK, Maeng JS, Falahati R, Lee C, Williams MS (2005) Receptor-stimulated oxidation of SHP-2 promotes T-cell adhesion through SLP-76-ADAP. EMBO J 24: 2331-2341
28. Liu J, Kang H, Raab M, da Silva AJ, Kraeft SK, Rudd CE (1998) FYB (FYN binding protein) serves as a binding partner for lymphoid protein and FYN kinase substrate SKAP55 and a SKAP55-related protein in T cells. Proc Natl Acad Sci USA 95: 8779-8784
29. Macian F (2005) NFAT proteins: key regulators of T-cell development and function. Nat Rev Immunol 5: 472-484
30. Marie-Cardine A, Bruyns E, Eckerskorn C, Kirchgessner H, Meuer SC, Schraven B (1997) Molecular cloning of SKAP55, a novel protein that associates with the protein tyrosine kinase p59fyn in human T-lymphocytes. J Biol Chem 272: 16077-16080
31. Marie-Cardine A, Hendricks-Taylor LR, Boerth NJ, Zhao H, Schraven B, Koretzky GA (1998) Molecular interaction between the Fyn-associated protein SKAP55 and the SLP-76-associated phosphoprotein SLAP-130. J Biol Chem 273: 25789-25795
32. Menasche G, Kliche S, Chen EJ, Stradal TE, Schraven B, Koretzky G (2007) RIAM links the ADAP/SKAP-55 signaling module to Rap1, facilitating T-cell-receptor-mediated integrin activation. Mol Cell Biol 27: 4070-4081
33. Mkrtichyan M, Najjar YG, Raulfs EC, Liu L, Langerman S, Guittard G, Ozbun L, Khleif SN (2012) B7-DC-Ig enhances vaccine effect by a novel mechanism dependent on PD-1 expression level on T cell subsets. J Immunol 189: 2338-2347
34. Mueller KL, Thomas MS, Burbach BJ, Peterson EJ, Shimizu Y (2007) Adhesion and degranulation-promoting adapter protein (ADAP) positively regulates T cell sensitivity to antigen and T cell survival. J Immunol 179: 3559-3569
35. Navarro-Antolin J, Rey-Campos J, Lamas S (2000) Transcriptional induction of endothelial nitric oxide gene by cyclosporine A. A role for activator protein-1. J Biol Chem 275: 3075-3080
36. Nomi T, Sho M, Akahori T, Hamada K, Kubo A, Kanehiro H, Nakamura S, Enomoto K, Yagita H, Azuma M et al (2007) Clinical significance and therapeutic potential of the programmed death-1 ligand/programmed death-1 pathway in human pancreatic cancer. Clin Cancer Res 13: 2151-2157
37. Oestreich KJ, Yoon H, Ahmed R, Boss JM (2008) NFATc1 regulates PD-1 expression upon T cell activation. J Immunol 181: 4832-4839
38. Pazdrak K, Young TW, Stafford S, Olszewska-Pazdrak B, Straub C, Starosta V, Brasier A, Kurosky A (2008) Cross-talk between ICAM-1 and granulocyte-macrophage colony-stimulating factor receptor signaling modulates eosinophil survival and activation. J Immunol 180: 4182-4190
39. Peterson EJ, Woods ML, Dmowski SA, Derimanov G, Jordan MS, Wu JN, Myung PS, Liu QH, Pribila JT, Freedman BD et al (2001) Coupling of the TCR to integrin activation by Slap-130/Fyb. Science 293: 2263-2265
40. Powles T, Eder JP, Fine GD, Braiteh FS, Loriot Y, Cruz C, Bellmunt J, Burris HA, Petrylak DP, S-l Teng et al (2014) MPDL3280A (anti-PD-L1) treatment leads to clinical activity in metastatic bladder cancer. Nature 515: 558-562
41. Pyrzynska B, Serrano M, Marti'nez-A C, Kaminska B (2002) Tumor suppressor p53 mediates apoptotic cell death triggered by cyclosporin A. J Biol Chem 277: 14102-14108
42. Raab M, Wang H, Lu Y, Smith X, Wu Z, Strebhardt K, Ladbury JE, Rudd CE (2010) T cell receptor "inside-out" pathway via signaling module SKAP1-RapL regulates T cell motility and interactions in lymph nodes. Immunity 32: 541-556
43. Saunders PA, Hendrycks VR, Lidinsky WA, Woods ML (2005) PD-L2:PD-1 involvement in T cell proliferation, cytokine production, and integrin-mediated adhesion. Eur J Immunol 35: 3561-3569
44. Schmits R, Kündig TM, Baker DM, Shumaker G, Simard JJ, Duncan G, Wakeham A, Shahinian A, van der Heiden A, Bachmann MF et al (1996) LFA-1-deficient mice show normal CTL responses to virus but fail to reject immunogenic tumor. J Exp Med 183: 1415-1426
45. Shin H, Blackburn SD, Intlekofer AM, Kao C, Angelosanto JM, Reiner SL, Wherry EJ (2009) A role for the transcriptional repressor blimp-1 in CD8+ T cell exhaustion during chronic viral infection. Immunity 31: 309-320
46. Su Q, Eugster HP, Ryffel B, Dumont FJ (1996) Cyclosporin A enhances the calcium-dependent induction of AP-1 complex and c-fos mRNA in a T cell lymphoma. Biochem Biophys Res Commun 229: 249-256
47. Sugie K, Jeon MS, Grey HM (2004) Activation of naive CD4 T cells by anti-CD3 reveals an important role for Fyn in Lck-mediated signaling. Proc Natl Acad Sci USA 101: 14859-14864
48. Tang H, Zhao ZJ, Huang XY, Landon EJ, Inagami T (1999) Fyn kinase-directed activation of SH2 domain-containing protein-tyrosine phosphatase SHP-2 by Gi protein-coupled receptors in Madin-Darby canine kidney cells. J Biol Chem 274: 12401-12407
49. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, Powderly JD, Carvajal RD, Sosman JA, Atkins MB et al (2012) Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. New Engl J Med 366: 2443-2454
50. Tumeh PC, Harview CL, Yearley JH, Shintaku IP, Taylor EJM, Robert L, Chmielowski B, Spasic M, Henry G, Ciobanu V et al (2014) PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature 515: 568-571
51. Viguier M, Lemaitre F, Verola O, Cho MS, Gorochov G, Dubertret L, Bachelez H, Kourilsky P, Ferradini L (2004) Foxp3 expressing CD4+CD25(high) regulatory T cells are overrepresented in human metastatic melanoma lymph nodes and inhibit the function of infiltrating T cells. J Immunol 173: 1444-1453
52. Wang H, Liu H, Lu Y, Lovatt M, Wei B, Rudd CE (2007) Functional defects of SKAP-55-deficient T cells identify a regulatory role for the adaptor in LFA-1 adhesion. Mol Cell Biol 27: 6863-6875
53. Wang H, McCann FE, Gordan JD, Wu X, Raab M, Malik TH, Davis DM, Rudd CE (2004) ADAP-SLP-76 binding differentially regulates supramolecular activation cluster (SMAC) formation relative to T cell-APC conjugation. J Exp Med 200: 1063-1074
54. Wang H, Moon EY, Azouz A, Wu X, Smith A, Schneider H, Hogg N, Rudd CE (2003) SKAP-55 regulates integrin adhesion and formation of T cell-APC conjugates. Nat Immunol 4: 366-374
55. Werneck MB, Hottz E, Bozza PT, Viola JP (2012) Cyclosporin A inhibits colon cancer cell growth independently of the calcineurin pathway. Cell Cycle 11: 3997-4008
56. Wherry EJ, Ha SJ, Kaech SM, Haining WN, Sarkar S, Kalia V, Subramaniam S, Blattman JN, Barber DL, Ahmed R (2007) Molecular signature of CD8+ T cell exhaustion during chronic viral infection. Immunity 27: 670-684
57. Xiao G, Deng A, Liu H, Ge G, Liu X (2012) Activator protein 1 suppresses antitumor T-cell function via the induction of programmed death 1. Proc Natl Acad Sci USA 109: 15419-15424
58. Yokosuka T, Takamatsu M, Kobayashi-Imanishi W, Hashimoto-Tane A, Azuma M, Saito T (2012) Programmed cell death 1 forms negative costimulatory microclusters that directly inhibit T cell receptor signaling by recruiting phosphatase SHP2. J Exp Med 209: 1201-1217
59. Zhang Y, Joe G, Zhu J, Carroll R, Levine B, Hexner E, June C, Emerson SG (2004) Dendritic cell-activated CD44hiCD8+ T cells are defective in mediating acute graft-versus-host disease but retain graft-versus-leukemia activity. Blood 103: 3970-3978