Paxillin binding to the cytoplasmic domain of CD103 promotes cell adhesion and effector functions for CD8+ resident memory T cells in tumors

Cancer Research

Volumn 77, Issue 24, 2017, Pages 7072-7082

  Gauthier, Ludiane ^a   Corgnac, Stéphanie ^a   Boutet, Marie ^a,d   Gros, Gwendoline ^a   Validire, Pierre ^b   Bismuth, Georges ^c   Mami Chouaib, Fathia ^a  

^a Faculty of Medicine University of Paris Sud   (France)

^b INSTITUT MUTUALISTE MONTSOURIS   (France)

^c INSTITUT COCHIN   (France)

^d ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHAEBETA7 INTEGRIN; CD103 ANTIGEN; FOCAL ADHESION KINASE 2; PAXILLIN; SARACATINIB; SERINE; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; UVOMORULIN; ALPHA E INTEGRINS; ALPHA INTEGRIN; LEUKOCYTE ANTIGEN; PROTEIN BINDING;

ARTICLE; CD8+ T LYMPHOCYTE; CELL ADHESION; CELL MIGRATION; CONTROLLED STUDY; CYTOPLASM; HUMAN; HUMAN CELL; HUMAN TISSUE; LUNG TUMOR; LYSOSOME; MEMORY T LYMPHOCYTE; NON SMALL CELL LUNG CANCER; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TISSUE RESIDENT MEMORY T CELL; TUMOR ASSOCIATED LEUKOCYTE; CHEMISTRY; CYTOTOXICITY; HEK293 CELL LINE; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; JURKAT CELL LINE; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE; TUMOR MICROENVIRONMENT;

ANTIGENS, CD; CD8-POSITIVE T-LYMPHOCYTES; CELL ADHESION; CELL LINE, TUMOR; CYTOPLASM; CYTOTOXICITY, IMMUNOLOGIC; HEK293 CELLS; HUMANS; IMMUNOLOGIC MEMORY; INTEGRIN ALPHA CHAINS; JURKAT CELLS; LYMPHOCYTES, TUMOR-INFILTRATING; PAXILLIN; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; TUMOR MICROENVIRONMENT;

EID: 85038410856     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-17-1487     Document Type: Article

References (48)

1. Le Floc's A, Jalil A, Vergnon I, Le Maux Chansac B, Lazar V, Bismuth G, et al. Alpha E beta 7 integrin interaction with E-cadherin promotes antitumor CTL activity by triggering lytic granule polarization and exocytosis. J Exp Med 2007;204: 559-70.
2. Franciszkiewicz K, Le Floc'h A, Boutet M, Vergnon I, Schmitt A, Mami-Chouaib F. 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 2013;73: 617-28.
3. Piet B, de Bree GJ, Smids-Dierdorp BS, van der Loos CM, Remmerswaal EB, von der Thusen JH, et al. CD8(+) T cells with an intraepithelial phenotype upregulate cytotoxic function upon influenza infection in human lung. J Clin Inves 2011;121: 2254-63.
4. Jiang X, Clark RA, Liu L, Wagers AJ, Fuhlbrigge RC, Kupper TS. Skin infection generates non-migratory memory CD8+ T(RM) cells providing global skin immunity. Nature 2012;483: 227-31.
5. Mackay LK, Stock AT, MaJZ, Jones CM, Kent SJ, Mueller SN, et al. Long-lived epithelial immunity by tissue-resident memory T (TRM) cells in the absence of persisting local antigen presentation. Proc Natl Acad Sci U S A 2012;109: 7037-42.
6. Mueller SN, Mackay LK. Tissue-residentmemory T cells: local specialists in immune defence. Nat Rev Immunol 2016;16: 79-89.
7. Turner DL, Farber DL. Mucosal resident memory CD4 T cells in protection and immunopathology. Front Immunol 2014;5: 331.
8. Mackay LK, Minnich M, Kragten NA, Liao Y, Nota B, Seillet C, et al. Hobit and Blimp1 instruct a universal transcriptional program of tissue residency in lymphocytes. Science 2016;352: 459-63.
9. Webb JR, Milne K, Watson P, Deleeuw RJ, Nelson BH. Tumor-infiltrating lymphocytes expressing the tissue resident memory marker CD103 are associated with increased survival in high-grade serous ovarian cancer. Clin Cancer Res 2014;20: 434-44.
10. Djenidi F, Adam J, Goubar A, Durgeau A, Meurice G, de Montpreville V, et al. CD8+CD103+ tumor-infiltrating lymphocytes are tumor-specific tissue-resident memory T cells and a prognostic factor for survival in lung cancer patients. J Immunol 2015;194: 3475-86.
11. Workel HH, Komdeur FL, Wouters MC, Plat A, Klip HG, Eggink FA, et al. CD103 defines intraepithelial CD8+ PD1+ tumour-infiltrating lymphocytes of prognostic significance in endometrial adenocarcinoma. Eur J Cancer 2016;60: 1-11.
12. Wang ZQ, Milne K, Derocher H, Webb JR, Nelson BH, Watson PH. CD103 and intratumoral immune response in breast cancer. Clin Cancer Res 201622: 6290-7.
13. Boutet M, Gauthier L, Leclerc M, Gros G, de Montpreville V, Theret N, et al. TGFbeta signaling intersects with CD103 integrin signaling to promote Tlymphocyte accumulation and antitumor activity in the lung tumor microenvironment. Cancer Res 2016;76: 1757-69.
14. Le Floc'h A, Jalil A, Franciszkiewicz K, Validire P, Vergnon I, Mami- Chouaib F. Minimal engagement of CD103 on cytotoxic T lymphocytes with an E-cadherin-Fc molecule triggers lytic granule polarization via a phospholipase Cgamma-dependent pathway. Cancer Res 2011;71: 328-38.
15. Hashimoto-Tane A, Saito T. Dynamic Regulation of TCR-Microclusters and the Microsynapse for T Cell Activation. Front Immunol 2016;7: 255.
16. Hashimoto-Tane A, Sakuma M, Ike H, Yokosuka T, Kimura Y, Ohara O, et al. Micro-adhesion rings surrounding TCR microclusters are essential for T cell activation. J Exp Med 2016;213: 1609-25.
17. Petit V, Boyer B, Lentz D, Turner CE, Thiery JP, Valles AM. Phosphorylation of tyrosine residues 31 and 118 on paxillin regulates cell migration through an association with CRK in NBT-II cells. J Cell Biol 2000;148: 957-70.
18. Tsubouchi A, Sakakura J, Yagi R, Mazaki Y, Schaefer E, Yano H, et al. Localized suppression of RhoA activity by Tyr31/118-phosphorylated paxillin in cell adhesion and migration. J Cell Biol 2002;159: 673-83.
19. Lee YC, Chang AY, Lin-Feng MH, Tsou WI, Chiang IH, Lai MZ. Paxillin phosphorylation by JNK and p38 is required for NFAT activation. Eur J Immunol 2012;42: 2165-75.
20. Doucey MA, Legler DF, Faroudi M, Boucheron N, Baumgaertner P, Naeher D, et al. The beta1 and beta3 integrins promote T cell receptor-mediated cytotoxic T lymphocyte activation. J Biol Chem 2003;278: 26983-91.
21. Robertson LK, Ostergaard HL. Paxillin associates with the microtubule cytoskeleton and the immunological synapse of CTL through its leucineaspartic acid domains and contributes to microtubule organizing center reorientation. J Immunol 2011;187: 5824-33.
22. Romanova LY, Mushinski JF. Central role of paxillin phosphorylation in regulation of LFA-1 integrins activity and lymphocyte migration. Cell Adh Migr 2011;5: 457-62.
23. Liu S, Thomas SM, Woodside DG, Rose DM, Kiosses WB, Pfaff M, et al. Binding of paxillin to alpha4 integrins modifies integrin-dependent biological responses. Nature 1999;402: 676-81.
24. Liu S, Ginsberg MH. Paxillin binding to a conserved sequence motif in the alpha 4 integrin cytoplasmic domain. J Biol Chem 2000;275: 22736-42.
25. Echchakir H, Dorothee G, Vergnon I, Menez J, Chouaib S, Mami-Chouaib F. Cytotoxic T lymphocytes directed against a tumor-specific mutated antigen display similar HLA tetramer binding but distinct functional avidity and tissue distribution. Proc Natl Acad Sci U S A 2002;99: 9358-63.
26. Khazen R, Muller S, Gaudenzio N, Espinosa E, Puissegur MP, Valitutti S. Melanoma cell lysosome secretory burst neutralizes the CTL-mediated cytotoxicity at the lytic synapse. Nature Comm 2016;7: 10823.
27. Higgins JM, Cernadas M, Tan K, Irie A, Wang J, Takada Y, et al. The role of alpha and beta chains in ligand recognition by beta 7 integrins. J Biol Chem 2000;275: 25652-64.
28. El Hage F, Vergnon I, Grunenwald D, Soria JC, Chouaib S, Mami-Chouaib F. Generation of diverse mutated tumor antigen-specific cytotoxic T lymphocytes in a lung cancer patient with long survival. Oncol Rep 2005; 14: 763-9.
29. Mokrani M, Klibi J, Bluteau D, Bismuth G, Mami-Chouaib F. Smad and NFAT pathways cooperate to induce CD103 expression in human CD8 T lymphocytes. J Immunol 2014;192: 2471-9.
30. Adair BD, Yeager M. Three-dimensional model of the human platelet integrin alpha IIbbeta 3 based on electron cryomicroscopy and x-ray crystallography. Proc Natl Acad Sci U S A 2002;99: 14059-64.
31. Vinogradova O, Haas T, Plow EF, Qin J. A structural basis for integrin activation by the cytoplasmic tail of the alpha IIb-subunit. Proc Natl Acad Sci U S A 2000;97: 1450-5.
32. Deakin NO, Turner CE. Paxillin comes of age. J Cell Sci 2008;121: 2435-44.
33. Schaffner-Reckinger E, Gouon V, Melchior C, Plancon S, Kieffer N. Distinct involvement of beta3 integrin cytoplasmic domain tyrosine residues 747 and 759 in integrin-mediated cytoskeletal assembly and phosphotyrosine signaling. J Biol Chem 1998;273: 12623-32.
34. Lev S, MorenoH, Martinez R, Canoll P, Peles E, Musacchio JM, et al. Protein tyrosine kinase PYK2 involved in Ca(2+)-induced regulation of ion channel and MAP kinase functions. Nature 1995;376: 737-45.
35. Avraham S, Jiang S, Ota S, Fu Y, Deng B, Dowler LL, et al. Structural and functional studies of the intracellular tyrosine kinase MATK gene and its translated product. J Biol Chem 1995;270: 1833-42.
36. Salgia R, Pisick E, Sattler M, Li JL, Uemura N, Wong WK, et al. p130CAS forms a signaling complex with the adapter protein CRKL in hematopoietic cells transformed by the BCR/ABL oncogene. J Biol Chem 1996;271: 25198-203.
37. Gismondi A, Bisogno L, Mainiero F, Palmieri G, Piccoli M, Frati L, et al. Proline-rich tyrosine kinase-2 activation by beta 1 integrin fibronectin receptor cross-linking and associationwith paxillin in human natural killer cells. J Immunol 1997;159: 4729-36.
38. Rumsey LM, Teague RM, Benedict SH, Chan MA. MIP-1alpha induces activation of phosphatidylinositol-3 kinase that associates with Pyk-2 and is necessary for B-cell migration. Exp Cell Res 2001;268: 77-83.
39. Rose DM, Liu S, Woodside DG, Han J, Schlaepfer DD, Ginsberg MH. Paxillin binding to the 4 integrin subunit stimulates LFA-1 (integrin alpha L beta 2)-Dependent T cell migration by augmenting the activation of focal adhesion kinase/proline-rich tyrosine kinase-2. J Immunol 2003; 170: 5912-8.
40. Beinke S, Phee H, Clingan JM, Schlessinger J, Matloubian M, Weiss A. Proline-rich tyrosine kinase-2 is critical for CD8 T-cell short-lived effector fate. Proc Nat Acad Sci U S A 2010;107: 16234-9.
41. Cheung SM, Ostergaard HL. Pyk2 controls integrin-dependent CTL migration through regulation of de-adhesion. J Immunol 2016;197: 1945-56.
42. March ME, Long EO. beta2 integrin induces TCRzeta-Syk-phospholipase C-gamma phosphorylation and paxillin-dependent granule polarization in human NK cells. J Immunol 2011;186: 2998-3005.
43. Brown MC, Perrotta JA, Turner CE. Identification of LIM3 as the principal determinant of paxillin focal adhesion localization and characterization of a novel motif on paxillin directing vinculin and focal adhesion kinase binding. J Cell Biol 1996;135: 1109-23.
44. Nikolopoulos SN, Turner CE. Actopaxin, a new focal adhesion protein that binds paxillin LD motifs and actin and regulates cell adhesion. J Cell Biol 2000;151: 1435-48.
45. Nikolopoulos SN, Turner CE. Integrin-linked kinase (ILK) binding to paxillin LD1 motif regulates ILK localization to focal adhesions. J Biol Chem 2001;276: 23499-505.
46. Grashoff C, Aszodi A, Sakai T, Hunziker EB, Fassler R. Integrin-linked kinase regulates chondrocyte shape and proliferation. EMBO Rep 2003; 4: 432-8.
47. Stevens JM, Jordan PA, Sage T, Gibbins JM. The regulation of integrinlinked kinase in human platelets: evidence for involvement in the regulation of integrin alpha 2 beta 1. J Thromb Haemost 2004;2: 1443-52.
48. Zhang M, March ME, Lane WS, Long EO. A signaling network stimulated by beta2 integrin promotes the polarization of lytic granules in cytotoxic cells. Sci Signal 2014;7: ra96.