TGFβ signaling intersects with CD103 integrin signaling to promote T-Lymphocyte accumulation and antitumor activity in the lung tumor microenvironment

Cancer Research

Volumn 76, Issue 7, 2016, Pages 1757-1769

  Boutet, Marie ^a   Gauthier, Ludiane ^a   Leclerc, Marine ^a   Gros, Gwendoline ^a   De Montpreville, Vincent ^a,b   Theret, Nathalie ^c   Donnadieu, Emmanuel ^d,e,f   Mami Chouaib, Fathia ^a  

^a INSERM   (France)

^b CENTRE CHIRURGICAL MARIE LANNELONGUE   (France)

^c UNIVERSITÉ DE RENNES 1   (France)

^d INSTITUT COCHIN   (France)

^e CNRS   (France)

^f UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD103 ANTIGEN; INTEGRIN; INTEGRIN LINKED KINASE; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; PROTEIN KINASE B; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; ALPHA E INTEGRINS; ALPHA INTEGRIN; CD3 ANTIGEN; LEUKOCYTE ANTIGEN;

ARTICLE; CELL ADHESION; CELL MOTILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN TISSUE; LUNG TUMOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TUMOR MICROENVIRONMENT; CONFOCAL MICROSCOPY; GENETICS; METABOLISM; PATHOLOGY;

ANTIGENS, CD; ANTIGENS, CD3; HUMANS; INTEGRIN ALPHA CHAINS; LUNG NEOPLASMS; MICROSCOPY, CONFOCAL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TRANSFORMING GROWTH FACTOR BETA; TUMOR MICROENVIRONMENT;

EID: 84963738682     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-15-1545     Document Type: Article

References (46)

1. Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pages C, et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 2006;313:1960-4.
2. Pribila JT, Quale AC, Mueller KL, Shimizu Y. Integrins and T cell-mediated immunity. Annu Rev Immunol 2004;22:157-80.
3. Epler JA, Liu R, Shimizu Y. From the ECM to the cytoskeleton and back: how integrins orchestrate T cell action. Dev Immunol 2000; 7:155-70.
4. van Kooyk Y, Figdor CG. Avidity regulation of integrins: The driving force in leukocyte adhesion. Curr Opin Cell Biol 2000;12:542-7.
5. Constantin G, Majeed M, Giagulli C, Piccio L, Kim JY, Butcher EC, et al. Chemokines trigger immediate beta2 integrin affinity and mobility changes: differential regulation and roles in lymphocyte arrest under flow. Immunity 2000;13:759-69.
6. Dustin ML, Springer TA. T-cell receptor cross-linking transiently stimulates adhesiveness through LFA-1. Nature 1989;341:619-24.
7. Lek HS, Morrison VL, Conneely M, Campbell PA, McGloin D, Kliche S, et al. The spontaneously adhesive leukocyte function-associated antigen-1 (LFA-1) integrin in effector T cells mediates rapid actin- And calmodulin- dependent adhesion strengthening to ligand under shear flow. J Biol Chem 2013;288:14698-708.
8. Le Floc'h 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.
9. 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.
10. 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 viaa phospholipase Cgamma-dependent pathway. Cancer Res 2011;71: 328-38.
11. Wagner N, Lohler J, Kunkel EJ, Ley K, Leung E, Krissansen G, et al. Critical role for beta7 integrins in formation of the gut-associated lymphoid tissue. Nature 1996;382:366-70.
12. Lefrancois L, Parker CM, Olson S, Muller W, Wagner N, Schon MP, et al. The role of beta7 integrins in CD8 T cell trafficking during an antiviral immune response. J Exp Med 1999;189:1631-8.
13. Schon MP, Arya A, Murphy EA, Adams CM, Strauch UG, Agace WW, et al. Mucosal T lymphocyte numbers are selectively reduced in integrin alpha E (CD103)-deficient mice. J Immunol 1999;162:6641-9.
14. Franciszkiewicz K, Le Floc'h A, Jalil A, Vigant F, Robert T, Vergnon I, et al. Intratumoral induction of CD103 triggers tumor-specific CTL function and CCR5-dependent T-cell retention. Cancer Res 2009;69: 6249-55.
15. Webb JR, Milne K, Watson P, Deleeuw RJ, Nelson BH. Tumor-infiltrating lymphocytes expressing the tissue resident memory marker CD103 are associatedwith increased survival in high-grade serous ovarian cancer. Clin Cancer Res 2014;20:434-44.
16. Djenidi F, Adam J, Goubar A, Durgeau A, Meurice G, de Montpreville V, et al. CD8CD103 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.
17. Parker CM, Cepek KL, Russell GJ, Shaw SK, Posnett DN, Schwarting R, et al. A family of beta 7 integrins on human mucosal lymphocytes. Proc Natl Acad Sci U S A 1992;89:1924-8.
18. 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.
19. Salmon H, Franciszkiewicz K, Damotte D, Dieu-Nosjean MC, Validire P, Trautmann A, et al. Matrix architecture defines the preferential localization andmigration of T cells into the stroma ofhuman lung tumors. JClin Invest 2012;122:899-910.
20. Kinashi T. Intracellular signalling controlling integrin activation in lymphocytes. Nat Rev Immunol 2005;5:546-59.
21. Laudanna C, Kim JY, Constantin G, Butcher E. Rapid leukocyte integrin activation by chemokines. Immunol Rev 2002;186:37-46.
22. Friedrich EB, Sinha S, Li L, Dedhar S, Force T, Rosenzweig A, et al. Role of integrin-linked kinase in leukocyte recruitment. J Biol Chem 2002;277: 16371-5.
23. Liu E, Sinha S, Williams C, Cyrille M, Heller E, Snapper SB, et al. Targeted deletion of integrin-linked kinase reveals a role in T-cell chemotaxis and survival. Mol Cell Biol 2005;25:11145-55.
24. Janji B, Melchior C, Gouon V, Vallar L, Kieffer N. Autocrine TGF-betaregulated expression of adhesion receptors and integrin-linked kinase in HT-144 melanoma cells correlates with their metastatic phenotype. Int J Cancer 1999;83:255-62.
25. Feng Y, Wang D, Yuan R, Parker CM, Farber DL, Hadley GA. CD103 expression is required for destruction of pancreatic islet allografts by CD8 () T cells. J Exp Med 2002;196:877-86.
26. Passlick B, Pantel K, Kubuschok B, Angstwurm M, Neher A, Thetter O, et al. Expression of MHC molecules and ICAM-1 on non-small cell lung carcinomas: Association with early lymphatic spread of tumour cells. Eur J Cancer 1996;32A:141-5.
27. Asselin-Paturel C, Echchakir H, Carayol G, Gay F, Opolon P, Grunenwald D, et al. Quantitative analysis of Th1, Th2 and TGF-beta1 cytokine expression in tumor, TIL and PBL of non-small cell lung cancer patients. Int J Cancer 1998;77:7-12.
28. Sela U, Mauermann N, Hershkoviz R, Zinger H, Dayan M, Cahalon L, et al. The inhibition of autoreactive T cell functions by a peptide based on the CDR1 of an anti-DNA autoantibody is via TGF-beta-mediated suppression of LFA-1 and CD44 expression and function. J Immunol 2005;175:7255-63.
29. Schlickum S, Sennefelder H, Friedrich M, Harms G, Lohse MJ, Kilshaw P, et al. Integrin alpha E(CD103)beta 7 influences cellular shape and motility in a ligand-dependent fashion. Blood 2008;112:619-25.
30. Zhang Q, Yu N, Lee C. Mysteries of TGF-beta Paradox in Benign and Malignant Cells. Front Oncol 2014;4:94.
31. Li MO, Sanjabi S, Flavell RA. Transforming growth factor-beta controls development, homeostasis, and tolerance of T cells by regulatory T celldependent and -independent mechanisms. Immunity 2006;25:455-71.
32. Marie JC, Liggitt D, Rudensky AY. Cellularmechanisms of fatal early-onset autoimmunity in mice with the T cell-specific targeting of transforming growth factor-beta receptor. Immunity 2006;25:441-54.
33. Thomas DA, Massague J. TGF-beta directly targets cytotoxic T cell functions during tumor evasion of immune surveillance. Cancer Cell 2005;8:369-80.
34. Gebhardt T, Mackay LK. Local immunity by tissue-resident CD8() memory T cells. Front Immunol 2012;3:340.
35. Sela U, Hershkoviz R, Cahalon L, Lider O, Mozes E. Down-regulation of stromal cell-derived factor-1alpha-induced T cell chemotaxis by a peptide based on the complementarity-determining region 1 of an anti-DNA autoantibody via up-regulation of TGF-beta secretion. J Immunol 2005; 174:302-9.
36. Shi Y, Massague J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 2003;113:685-700.
37. Zhang YE. Non-Smad pathways in TGF-beta signaling. Cell Res 2009; 19:128-39.
38. Vi L, Boo S, Sayedyahossein S, Singh RK, McLean S, DiGuglielmo GM, et al. Modulation of type II TGF-beta receptor degradation by integrin-linked kinase. J Invest Dermatol 2015;135:885-94.
39. Hannigan GE, Leung-Hagesteijn C, Fitz-Gibbon L, Coppolino MG, Radeva G, Filmus J, et al. Regulation of cell adhesion and anchorage-dependent growth by a new beta 1-integrin-linked protein kinase. Nature 1996; 379:91-6.
40. Honda S, Shirotani-Ikejima H, Tadokoro S, Maeda Y, Kinoshita T, Tomiyama Y, et al. Integrin-linked kinase associated with integrin activation. Blood 2009;113:5304-13.
41. Qian Y, Zhong X, Flynn DC, Zheng JZ, Qiao M, Wu C, et al. ILK mediates actin filament rearrangements and cell migration and invasion through PI3K/Akt/Rac1 signaling. Oncogene 2005;24:3154-65.
42. Legate KR, Montanez E, Kudlacek O, Fassler R. ILK, PINCH and parvin: The tIPP of integrin signalling. Nat Rev Mol Cell Biol 2006;7:20-31.
43. Grashoff C, Aszodi A, Sakai T, Hunziker EB, Fassler R. Integrin-linked kinase regulates chondrocyte shape and proliferation. EMBO Rep 2003; 4:432-8.
44. 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.
45. Zhang M, March ME, Lane WS, Long EO. Asignaling network stimulated by beta2 integrin promotes the polarization of lytic granules in cytotoxic cells. Sci Signal 2014;7:ra96.
46. Kutlesa S, Wessels JT, Speiser A, Steiert I, Muller CA, Klein G. E-cadherinmediated interactions of thymic epithelial cells with CD103 thymocytes lead to enhanced thymocyte cell proliferation. J Cell Sci 2002;115(Pt 23):4505-15.