J. E. Smith-garvin, G. A. Koretzky, and M. S. Jordan, T cell activation, Annu Rev Immunol, vol.27, pp.591-619, 2009.

O. Acuto and F. Michel, CD28-mediated co-stimulation: a quantitative support for TCR signalling, Nat Rev Immunol, vol.3, pp.939-51, 2003.

J. S. Boomer and J. M. Green, An enigmatic tail of CD28 signaling, Cold Spring Harb Perspect Biol, vol.2, p.2436, 2010.

F. Michel, G. Bonnefoy, G. Mangino, S. Mise-omata, and O. Acuto, CD28 as a molecular amplifier extending TCR ligation and signaling capabilities, Immunity, vol.15, pp.935-980, 2001.

Z. Cai, H. Kishimoto, A. Brunmark, M. R. Jackson, P. A. Peterson et al., Requirements for peptide-induced T cell receptor downregulation on naive CD8+ T cells, J Exp Med, vol.185, pp.641-51, 1997.

S. Valitutti, S. Muller, M. Cella, E. Padovan, and A. Lanzavecchia, Serial triggering of many T-cell receptors by a few peptide-MHC complexes, Nature, vol.375, pp.148-51, 1995.

S. K. Bromley, A. Iaboni, S. J. Davis, A. Whitty, J. M. Green et al., The immunological synapse and CD28-CD80 interactions, Nat Immunol, vol.2, pp.1159-66, 2001.

S. A. Wetzel, T. W. Mckeithan, and D. C. Parker, Live-cell dynamics and the role of costimulation in immunological synapse formation, J Immunol, vol.169, pp.6092-101, 2002.

C. Wulfing, C. Sumen, M. D. Sjaastad, L. C. Wu, M. L. Dustin et al., Costimulation and endogenous MHC ligands contribute to T cell recognition, Nat Immunol, vol.3, pp.42-49, 2002.

P. G. Andres, K. C. Howland, D. Dresnek, S. Edmondson, A. K. Abbas et al., CD28 signals in the immature immunological synapse, J Immunol, vol.172, pp.5880-5886, 2004.

S. Y. Tseng, M. Liu, and M. L. Dustin, CD80 cytoplasmic domain controls localization of CD28, CTLA-4, and protein kinase Ctheta in the immunological synapse, J Immunol, vol.175, pp.7829-7865, 2005.

M. Sanchez-lockhart, M. Kim, and J. Miller, Cutting edge: A role for inside-out signaling in TCR regulation of CD28 ligand binding, J Immunol, vol.187, pp.5515-5524, 2011.

M. Sanchez-lockhart, A. V. Rojas, M. M. Fettis, R. Bauserman, T. R. Higa et al., T cell receptor signaling can directly enhance the avidity of CD28 ligand binding, PLoS ONE, vol.9, p.89263, 2014.

W. Y. Ho, M. P. Cooke, C. C. Goodnow, and M. M. Davis, Resting and anergic B cells are defective in CD28-dependent costimulation of naive CD4+ T cells, J Exp Med, vol.179, pp.1539-1588, 1994.

A. Salles, C. Billaudeau, A. Serge, A. M. Bernard, M. C. Phelipot et al., Barcoding T cell calcium response diversity with methods for automated and accurate analysis of cell signals (MAAACS), PLoS Comput Biol, vol.9, p.1003245, 2013.
URL : https://hal.archives-ouvertes.fr/hal-00870686

N. Chouaki-benmansour, K. Ruminski, A. M. Sartre, M. C. Phelipot, A. Salles et al., Phosphoinositides regulate the TCR/CD3 complex membrane dynamics and activation, Sci Rep, vol.8, p.4966, 2018.
URL : https://hal.archives-ouvertes.fr/hal-01920092

B. M. Carreno and M. Collins, The B7 family of ligands and its receptors: new pathways for costimulation and inhibition of immune responses, Annu Rev Immunol, vol.20, pp.29-53, 2002.

N. Tarantino, J. Y. Tinevez, E. F. Crowell, B. Boisson, R. Henriques et al., TNF and IL-1 exhibit distinct ubiquitin requirements for inducing NEMO-IKK supramolecular structures, J Cell Biol, vol.204, pp.231-276, 2014.
URL : https://hal.archives-ouvertes.fr/pasteur-01539965

A. Serge, N. Bertaux, H. Rigneault, and D. Marguet, Dynamic multiple-target tracing to probe spatiotemporal cartography of cell membranes, Nat Methods, vol.5, pp.687-94, 2008.
URL : https://hal.archives-ouvertes.fr/hal-00295014

J. Honerkamp, Stochastic Dynamical Systems: Concepts, Numerical Methods, Data Analysis, 1994.

G. J. Freeman, J. G. Gribben, V. A. Boussiotis, J. W. Ng, R. Vajr et al., Cloning of B7-2: a CTLA-4 counter-receptor that costimulates human T cell proliferation, Science, vol.262, pp.909-920, 1993.

R. A. Seder, R. N. Germain, P. S. Linsley, and W. E. Paul, CD28-mediated costimulation of interleukin 2 (IL-2) production plays a critical role in T cell priming for IL-4 and interferon gamma production, J Exp Med, vol.179, pp.299-304, 1994.

L. B. Klickstein, M. R. York, A. R. Fougerolles, and T. A. Springer, Localization of the binding site on intercellular adhesion molecule-3 (ICAM-3) for lymphocyte function-associated antigen 1 (LFA-1), J Biol Chem, vol.271, pp.23920-23927, 1996.

J. L. Gaglia, A. Mattoo, E. A. Greenfield, G. J. Freeman, and V. K. Kuchroo, Characterization of endogenous Chinese hamster ovary cell surface molecules that mediate T cell costimulation, Cell Immunol, vol.213, pp.83-93, 2001.

M. L. Dustin, T-cell activation through immunological synapses and kinapses, Immunol Rev, vol.221, pp.77-89, 2008.

H. D. Moreau, F. Lemaitre, E. Terriac, G. Azar, M. Piel et al., Dynamic in situ cytometry uncovers T cell receptor signaling during immunological synapses and kinapses in vivo, Immunity, vol.37, pp.351-63, 2012.

T. R. Mempel, S. E. Henrickson, V. Andrian, and U. H. , T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases, Nature, vol.427, pp.154-163, 2004.

M. J. Miller, O. Safrina, I. Parker, and M. D. Cahalan, Imaging the single cell dynamics of CD4+ T cell activation by dendritic cells in lymph nodes, J Exp Med, vol.200, pp.847-56, 2004.

A. Scholer, S. Hugues, A. Boissonnas, L. Fetler, and S. Amigorena, Intercellular adhesion molecule-1-dependent stable interactions between T cells and dendritic cells determine CD8+ T cell memory, Immunity, vol.28, pp.258-70, 2008.

R. S. Friedman, P. Beemiller, C. M. Sorensen, J. Jacobelli, and M. F. Krummel, Realtime analysis of T cell receptors in naive cells in vitro and in vivo reveals flexibility in synapse and signaling dynamics, J Exp Med, vol.207, pp.2733-2782, 2010.

J. Jacobelli, R. S. Friedman, M. A. Conti, A. M. Lennon-dumenil, M. Piel et al., Confinement-optimized three-dimensional T cell amoeboid motility is modulated via myosin IIA-regulated adhesions, Nat Immunol, vol.11, pp.953-61, 2010.

R. S. Lewis and M. D. Cahalan, Potassium and calcium channels in lymphocytes, Annu Rev Immunol, vol.13, pp.623-53, 1995.

S. Feske, J. Giltnane, R. Dolmetsch, L. M. Staudt, and A. Rao, Gene regulation mediated by calcium signals in T lymphocytes, Nat Immunol, vol.2, pp.316-340, 2001.

S. S. Skanland, K. Moltu, T. Berge, E. M. Aandahl, and K. Tasken, T-cell co-stimulation through the CD2 and CD28 co-receptors induces distinct signalling responses, Biochem J, vol.460, pp.399-410, 2014.

J. Delon, N. Bercovici, G. Raposo, R. Liblau, and A. Trautmann, Antigen-dependent and-independent Ca 2+ responses triggered in T cells by dendritic cells compared with B cells, J Exp Med, vol.188, pp.1473-84, 1998.

L. Borgne, M. Raju, S. Zinselmeyer, B. H. Le, V. T. Li et al., Real-Time analysis of calcium signals during the early phase of T cell activation using a genetically encoded calcium biosensor, J Immunol, vol.196, pp.1471-1480, 2016.

T. X. Dong, S. Othy, M. L. Greenberg, A. Jairaman, C. Akunwafo et al., Intermittent Ca2+ signals mediated by Orai1 regulate basal T cell motility, vol.6, p.27827, 2017.

Y. Boutin, D. Leitenberg, X. Tao, and K. Bottomly, Distinct biochemical signals characterize agonist-and altered peptide ligand-induced differentiation of naive CD4+ T cells into Th1 and Th2 subsets, J Immunol, vol.159, pp.5802-5811, 1997.

R. Zaru, C. P. Berrie, C. Iurisci, D. Corda, and S. Valitutti, CD28 co-stimulates TCR/CD3-induced phosphoinositide turnover in human T lymphocytes

, Eur J Immunol, vol.31, p.8, 2001.

C. Utzny, M. Faroudi, and S. Valitutti, Frequency encoding of T-cell receptor engagement dynamics in calcium time series, Biophys J, vol.88, pp.1-14, 2005.

B. Liu, W. Chen, B. D. Evavold, and C. Zhu, Accumulation of dynamic catch bonds between TCR and agonist peptide-MHC triggers T cell signaling, Cell, vol.157, pp.357-68, 2014.

R. M. Pielak, G. P. O'donoghue, J. J. Lin, K. N. Alfieri, N. C. Fay et al., Early T cell receptor signals globally modulate ligand:receptor affinities during antigen discrimination, Proc Natl Acad Sci, vol.114, pp.12190-12195, 2017.

F. Marangoni, T. T. Murooka, T. Manzo, E. Y. Kim, E. Carrizosa et al., The transcription factor NFAT exhibits signal memory during serial T cell interactions with antigen-presenting cells, Immunity, vol.38, pp.237-286, 2013.

R. Courjaret, M. Dib, and K. Machaca, Spatially restricted subcellular Ca(2+) signaling downstream of store-operated calcium entry encoded by a cortical tunneling mechanism, Sci Rep, vol.8, p.11214, 2018.

R. Rizzuto and T. Pozzan, Microdomains of intracellular Ca2+: molecular determinants and functional consequences, Physiol Rev, vol.86, pp.369-408, 2006.

A. Quintana, M. Pasche, C. Junker, D. Al-ansary, H. Rieger et al., Calcium microdomains at the immunological synapse: how ORAI channels, mitochondria and calcium pumps generate local calcium signals for efficient T-cell activation, Guse AH. Ca(2+) Microdomains in T-Lymphocytes. Front Oncol, vol.30, p.73, 2011.

S. Monaco, B. Jahraus, Y. Samstag, and H. Bading, Nuclear calcium is required for human T cell activation, J Cell Biol, vol.215, pp.231-274, 2016.

K. M. Fracchia, C. Y. Pai, and C. M. Walsh, Modulation of T Cell metabolism and function through calcium signaling, Front Immunol, vol.4, p.324, 2013.

M. F. Bachmann, K. Mckall-faienza, R. Schmits, D. Bouchard, J. Beach et al., Distinct roles for LFA-1 and CD28 during activation of naive T cells: adhesion versus costimulation, Immunity, vol.7, pp.549-57, 1997.

, Conflict of Interest Statement: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest

F. Xia, C. Qian, Z. Xun, Y. Hamon, A. Sartre et al., TCR and CD28 Concomitant Stimulation Elicits a Distinctive Calcium, Naive T Cells. Front. Immunol, vol.9, p.2864, 2018.
URL : https://hal.archives-ouvertes.fr/hal-02084941

Q. Xia, . Xun, . Hamon, . Sartre, . Formisano et al., This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, Copyright, 2018.