Fine tuning and efficient T cell activation with stimulatory aCD3 nanoarrays

Nano Letters

Volumn 13, Issue 11, 2013, Pages 5090-5097

  Matic, Jovana ^a,b   Deeg, Janosch ^a,b   Scheffold, Alexander ^c,d   Goldstein, Itamar ^e,f   Spatz, Joachim P ^a,b  

^a MAX PLANCK INSTITUTE FOR INTELLIGENT SYSTEMS   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^d POTSDAM INSTITUTE FOR CLIMATE IMPACT RESEARCH PIK   (Germany)

^e SHEBA MEDICAL CENTER   (Israel)

^f TEL AVIV UNIVERSITY   (Israel)

Author keywords

anti CD3 monoclonal antibody; Artificial antigen presenting interfaces; block copolymer micellar nanolithography (BCML); CD4+ T cells; nanopattern; T cell activation

Indexed keywords

ARTIFICIAL ANTIGEN; CELL ACTIVATION; NANO PATTERN; PROTEIN IMMOBILIZATION; SELF-ASSEMBLED; SURFACE DENSITY; T CELL ACTIVATION; T-CELL RESPONSE;

CELL IMMOBILIZATION; CELL PROLIFERATION; CELLS; CYTOLOGY; MONOCLONAL ANTIBODIES; PLASTIC COATINGS;

T-CELLS;

CD4 ANTIGEN; NANOMATERIAL;

HUMAN; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; T LYMPHOCYTE;

ANTIGENS, CD4; HUMANS; LYMPHOCYTE ACTIVATION; NANOSTRUCTURES; T-LYMPHOCYTES;

EID: 84887833736     PISSN: 15306984     EISSN: 15306992     Source Type: Journal    
DOI: 10.1021/nl4022623     Document Type: Article

References (66)

1. June, C. H. Adoptive T cell therapy for cancer in the clinic J. Clin. Invest. 2007, 117 (6) 1466-1476
2. June, C. H. Principles of adoptive T cell cancer therapy J. Clin. Invest. 2007, 117 (5) 1204-12
3. Germain, R. N. MHC-dependent antigen processing and peptide presentation: Providing ligands for T lymphocyte activation Cell 1994, 76 (2) 287-299
4. Altman, A.; Mark Coggeshall, K.; Mustelin, T. Molecular events mediating T cell activation Adv. Immunol. 1990, 48, 227-360
5. Kim, J. V.; Latouche, J.-B.; Riviere, I.; Sadelain, M. The ABCs of artificial antigen presentation Nat. Biotechnol. 2004, 22 (4) 403-410
6. Platzman, I.; Janiesch, J.-W.; Matić, J.; Spatz, J. P. Artificial Antigen-Presenting Interfaces in the Service of Immunology Isr. J. Chem. 2013, 10.1002/ijch.201300060
7. Steenblock, E. R.; Wrzesinski, S. H.; Flavell, R. A.; Fahmy, T. M. Antigen presentation on artificial acellular substrates: modular systems for flexible, adaptable immunotherapy Exp. Opin. Biol. Ther. 2009, 9 (4) 451-464
8. Steenblock, E. R.; Fahmy, T. M. A Comprehensive Platform for Ex Vivo T-cell Expansion Based on Biodegradable Polymeric Artificial Antigen-presenting Cells Mol.Ther. 2008, 16 (4) 765-772
9. Platzman, I.; Janiesch, J. W.; Spatz, J. P. Synthesis of nanostructured and biofunctionalized water-in-oil droplets as tools for homing T cells J. Am. Chem. Soc. 2013, 135 (9) 3339-42
10. Irvine, D. J.; Doh, J. Synthetic surfaces as artificial antigen presenting cells in the study of T cell receptor triggering and immunological synapse formation Semin. Immunol. 2007, 19 (4) 245-254
11. Acuto, O.; Michel, F. CD28-mediated co-stimulation: a quantitative support for TCR signalling Nat. Rev. Immunol. 2003, 3 (12) 939-951
12. Frauwirth, K. A.; Thompson, C. B. Activation and inhibition of lymphocytes by costimulation J. Clin. Invest. 2002, 109 (3) 295-299
13. Sharpe, A. H.; Freeman, G. J. The B7-CD28 superfamily Nat. Rev. Immunol. 2002, 2 (2) 116-26
14. Hosseini, B. H.; Louban, I.; Djandji, D.; Wabnitz, G. H.; Deeg, J.; Bulbuc, N.; Samstag, Y.; Gunzer, M.; Spatz, J. P.; Hammerling, G. J. Immune synapse formation determines interaction forces between T cells and antigen-presenting cells measured by atomic force microscopy Proc Natl Acad Sci U S A 2009, 106 (42) 17852-7
15. Lanzavecchia, A.; Sallusto, F. Progressive differentiation and selection of the fittest in the immune response Nat. Rev. Immunol. 2002, 2 (12) 982-987
16. Andersen, P. S.; Menné, C.; Mariuzza, R. A.; Geisler, C.; Karjalainen, K. A Response Calculus for Immobilized T Cell Receptor Ligands J. Biol. Chem. 2001, 276 (52) 49125-49132
17. Iezzi, G.; Karjalainen, K.; Lanzavecchia, A. The Duration of Antigenic Stimulation Determines the Fate of Naive and Effector T Cells Immunity 1998, 8 (1) 89-95
18. Gett, A. V.; Sallusto, F.; Lanzavecchia, A.; Geginat, J. T cell fitness determined by signal strength Nat. Immunol. 2003, 4 (4) 355-360
19. Lanzavecchia, A.; Sallusto, F. Understanding the generation and function of memory T cell subsets Curr. Opin. Immunol. 2005, 17 (3) 326-332
20. Paul, W. E. What determines Th2 differentiation, in vitro and in vivo? Immunol. Cell Biol. 2010, 88 (3) 236-9
21. Paul, W. E.; Zhu, J. How are TH2-type immune responses initiated and amplified? Nat. Rev. Immunol. 2010, 10 (4) 225-235
22. Purvis, H. A.; Stoop, J. N.; Mann, J.; Woods, S.; Kozijn, A. E.; Hambleton, S.; Robinson, J. H.; Isaacs, J. D.; Anderson, A. E.; Hilkens, C. M. Low-strength T-cell activation promotes Th17 responses Blood 2010, 116 (23) 4829-37
23. Turner, M. S.; Kane, L. P.; Morel, P. A. Dominant role of antigen dose in CD4+Foxp3+ regulatory T cell induction and expansion J. Immunol. 2009, 183 (8) 4895-903
24. Long, S. A.; Rieck, M.; Tatum, M.; Bollyky, P. L.; Wu, R. P.; Muller, I.; Ho, J. C.; Shilling, H. G.; Buckner, J. H. Low-dose antigen promotes induction of FOXP3 in human CD4+ T cells J. Immunol. 2011, 187 (7) 3511-20
25. Badou, A.; Savignac, M.; Moreau, M.; Leclerc, C.; Foucras, G.; Cassar, G.; Paulet, P.; Lagrange, D.; Druet, P.; Guéry, J.-C.; Pelletier, L. Weak TCR stimulation induces a calcium signal that triggers IL-4 synthesis, stronger TCR stimulation induces MAP kinases that control IFN-γ production Eur. J. Immunol. 2001, 31 (8) 2487-2496
26. Restifo, N. P.; Dudley, M. E.; Rosenberg, S. A. Adoptive immunotherapy for cancer: harnessing the T cell response Nat. Rev. Immunol. 2012, 12 (4) 269-281
27. Gattinoni, L.; Klebanoff, C. A.; Restifo, N. P. Paths to stemness: building the ultimate antitumour T cell Nat. Rev. Cancer 2012, 12 (10) 671-84
28. Gattinoni, L.; Powell, D. J., Jr.; Rosenberg, S. A.; Restifo, N. P. Adoptive immunotherapy for cancer: building on success Nat. Rev. Immunol. 2006, 6 (5) 383-93
29. Hinrichs, C. S.; Gattinoni, L.; Restifo, N. P. Programming CD8+ T cells for effective immunotherapy Curr. Opin. Immunol. 2006, 18 (3) 363-70
30. Mossman, K. D.; Campi, G.; Groves, J. T.; Dustin, M. L. Altered TCR Signaling from Geometrically Repatterned Immunological Synapses Science 2005, 310 (5751) 1191-1193
31. Giannoni, F.; Barnett, J.; Bi, K.; Samodal, R.; Lanza, P.; Marchese, P.; Billetta, R.; Vita, R.; Klein, M. R.; Prakken, B.; Kwok, W. W.; Sercarz, E.; Altman, A.; Albani, S. Clustering of T Cell Ligands on Artificial APC Membranes Influences T Cell Activation and Protein Kinase C θ Translocation to the T Cell Plasma Membrane J. Immunol. 2005, 174 (6) 3204-3211
32. Fadel, T. R.; Look, M.; Staffier, P. A.; Haller, G. L.; Pfefferle, L. D.; Fahmy, T. M. Clustering of Stimuli on Single-Walled Carbon Nanotube Bundles Enhances Cellular Activation Langmuir 2009, 26 (8) 5645-5654
33. Doh, J.; Irvine, D. J. Immunological synapse arrays: patterned protein surfaces that modulate immunological synapse structure formation in T cells Proc. Natl. Acad. Sci. U.S.A. 2006, 103 (15) 5700-5
34. Shen, K.; Thomas, V. K.; Dustin, M. L.; Kam, L. C. Micropatterning of costimulatory ligands enhances CD4+ T cell function Proc. Natl. Acad. Sci. U.S.A. 2008, 105 (22) 7791-6
35. Schamel, W. W.; Arechaga, I.; Risueno, R. M.; van Santen, H. M.; Cabezas, P.; Risco, C.; Valpuesta, J. M.; Alarcon, B. Coexistence of multivalent and monovalent TCRs explains high sensitivity and wide range of response J. Exp. Med. 2005, 202 (4) 493-503
36. Molnar, E.; Swamy, M.; Holzer, M.; Beck-Garcia, K.; Worch, R.; Thiele, C.; Guigas, G.; Boye, K.; Luescher, I. F.; Schwille, P.; Schubert, R.; Schamel, W. W. A. Cholesterol and Sphingomyelin Drive Ligand-independent T-cell Antigen Receptor Nanoclustering J. Biol. Chem. 2012, 287 (51) 42664-42674
37. Lillemeier, B. F.; Mortelmaier, M. A.; Forstner, M. B.; Huppa, J. B.; Groves, J. T.; Davis, M. M. TCR and Lat are expressed on separate protein islands on T cell membranes and concatenate during activation Nat. Immunol. 2010, 11 (1) 90-96
38. Cavalcanti-Adam, E. A.; Volberg, T.; Micoulet, A.; Kessler, H.; Geiger, B.; Spatz, J. P. Cell Spreading and Focal Adhesion Dynamics Are Regulated by Spacing of Integrin Ligands Biophys. J. 2007, 92 (8) 2964-2974
39. Thelen, K.; Wolfram, T.; Maier, B.; Jährling, S.; Tinazli, A.; Piehler, J.; Spatz, J. P.; Pollerberg, G. E. Cell adhesion molecule DM-GRASP presented as nanopatterns to neurons regulates attachment and neurite growth Soft Matter 2007, 3 (12) 1486-1491
40. Ranzinger, J.; Krippner-Heidenreich, A.; Haraszti, T.; Bock, E.; Tepperink, J.; Spatz, J. P.; Scheurich, P. Nanoscale Arrangement of Apoptotic Ligands Reveals a Demand for a Minimal Lateral Distance for Efficient Death Receptor Activation Nano Lett. 2009, 9 (12) 4240-4245
41. Heller, K. N.; Gurer, C.; Münz, C. Virus-specific CD4+ T cells: ready for direct attack J. Exp. Med. 2006, 203 (4) 805-808
42. Muranski, P.; Restifo, N. P. Adoptive immunotherapy of cancer using CD4(+) T cells Curr. Opin. Immunol. 2009, 21 (2) 200-8
43. Spatz, J. P.; Mössmer, S.; Hartmann, C.; Möller, M.; Herzog, T.; Krieger, M.; Boyen, H.-G.; Ziemann, P.; Kabius, B. Ordered Deposition of Inorganic Clusters from Micellar Block Copolymer Films Langmuir 1999, 16 (2) 407-415
44. 2-based interfaces Biomaterials 2007, 28 (32) 4739-4747
45. Aydin, D.; Schwieder, M.; Louban, I.; Knoppe, S.; Ulmer, J.; Haas, T. L.; Walczak, H.; Spatz, J. P. Micro-nanostructured protein arrays: a tool for geometrically controlled ligand presentation Small 2009, 5 (9) 1014-8
46. Sigal, G. B.; Bamdad, C.; Barberis, A.; Strominger, J.; Whitesides, G. M. A self-assembled monolayer for the binding and study of histidine-tagged proteins by surface plasmon resonance Anal. Chem. 1996, 68 (3) 490-7
47. Wolfram, T.; Belz, F.; Schoen, T.; Spatz, J. P. Site-specific presentation of single recombinant proteins in defined nanoarrays Biointerphases 2007, 2 (1) 44-48
48. Aydin, D.; Louban, I.; Perschmann, N.; Blümmel, J.; Lohmüller, T.; Cavalcanti-Adam, E. A.; Haas, T. L.; Walczak, H.; Kessler, H.; Fiammengo, R.; Spatz, J. P. Polymeric Substrates with Tunable Elasticity and Nanoscopically Controlled Biomolecule Presentation Langmuir 2010, 26 (19) 15472-15480
49. Groll, J.; Albrecht, K.; Gasteier, P.; Riethmueller, S.; Ziener, U.; Moeller, M. Nanostructured Ordering of Fluorescent Markers and Single Proteins on Substrates ChemBioChem 2005, 6 (10) 1782-1787
50. Caruso, A.; Licenziati, S.; Corulli, M.; Canaris, A. D.; De Francesco, M. A.; Fiorentini, S.; Peroni, L.; Fallacara, F.; Dima, F.; Balsari, A.; Turano, A. Flow cytometric analysis of activation markers on stimulated T cells and their correlation with cell proliferation Cytometry 1997, 27 (1) 71-76
51. Reddy, M.; Eirikis, E.; Davis, C.; Davis, H. M.; Prabhakar, U. Comparative analysis of lymphocyte activation marker expression and cytokine secretion profile in stimulated human peripheral blood mononuclear cell cultures: an in vitro model to monitor cellular immune function J. Immunol. Methods 2004, 293 (1,AI2) 127-142
52. Muul, L. M.; Silvin, C.; James, S. P.; Candotti, F. Measurement of proliferative responses of cultured lymphocytes. Curr. Protoc. Immunol. 2008, Chapter 7, Unit 7 10 1-7 10 24.
53. Nielsen; Afzelius; ErsbØll; Hansen Expression of the activation antigen CD69 predicts functionality of in vitro expanded peripheral blood mononuclear cells (PBMC) from healthy donors and HIV-infected patients Clin. Exp. Immunol. 1998, 114 (1) 66-72
54. Lindsey, W.; Lowdell, M.; Marti, G.; Abbasi, F.; Zenger, V.; King, K.; Lamb, L. CD69 expression as an index of T-cell function: assay standardization, validation and use in monitoring immune recovery Cytotherapy 2007, 9 (2) 123-132
55. Bretscher, P. The two-signal model of lymphocyte activation twenty-one years later Immunol. Today 1992, 13 (2) 74-76
56. June, C. H.; Bluestone, J. A.; Nadler, L. M.; Thompson, C. B. The B7 and CD28 receptor families Immunol. Today 1994, 15 (7) 321-331
57. Viola, A.; Lanzavecchia, A.; Cell, T. Activation Determined by T Cell Receptor Number and Tunable Thresholds Science 1996, 273 (5271) 104-106
58. Levine, B. L.; Bernstein, W. B.; Connors, M.; Craighead, N.; Lindsten, T.; Thompson, C. B.; June, C. H. Effects of CD28 costimulation on long-term proliferation of CD4+ T cells in the absence of exogenous feeder cells J. Immunol. 1997, 159 (12) 5921-30
59. - Regulatory T Cells that Modulates Their Suppressive Function J. Immunol. 2010, 184 (7) 3570-3581
60. Lyons, A. B.; Parish, C. R. Determination of lymphocyte division by flow cytometry J. Immunol. Methods 1994, 171 (1) 131-137
61. Dustin, M. L. A dynamic view of the immunological synapse Semin. Immunol. 2005, 17 (6) 400-10
62. Wegner, S. V.; Spatz, J. P. Cobalt(III) as a Stable and Inert Mediator Ion between NTA and His6-Tagged Proteins Angew. Chem., Int. Ed. 2013, 10.1002/anie.201210317
63. Graeter, S. V.; Huang, J.; Perschmann, N.; López-García, M.; Kessler, H.; Ding, J.; Spatz, J. P. Mimicking Cellular Environments by Nanostructured Soft Interfaces Nano Lett. 2007, 7 (5) 1413-1418
64. O'Garra, A.; Gabrysova, L.; Spits, H. Quantitative events determine the differentiation and function of helper T cells Nat. Immunol. 2011, 12 (4) 288-294
65. Kalamasz, D.; Long, S. A.; Taniguchi, R.; Buckner, J. H.; Berenson, R. J.; Bonyhadi, M. Optimization of Human T-Cell Expansion Ex Vivo Using Magnetic Beads Conjugated with Anti-CD3 and Anti-CD28 Antibodies J. Immunother. 2004, 27 (5) 405-418
66. Mescher, M. Surface contact requirements for activation of cytotoxic T lymphocytes J. Immunol. 1992, 149 (7) 2402-2405