The scaffolding function of the RLT PR protein explains its essential role for CD28 co-stimulation in mouse and human T cells

Journal of Experimental Medicine

Volumn 213, Issue 11, 2016, Pages 2437-2457

  Roncagalli, Romain ^a   Cucchetti, Margot ^a   Jarmuzynski, Nicolas ^a   Grégoire, Claude ^a   Bergot, Elise ^a   Audebert, Stéphane ^a   Baudelet, Emilie ^a   Menoita, Marisa Goncalves ^a   Joachim, Anais ^a   Durand, Stéphane ^a   Suchanek, Miloslav ^b   Fiore, Frédéric ^a   Zhang, Lichen ^a,c   Liang, Yinming ^a,c   Camoin, Luc ^a   Malissen, Marie ^a   Malissen, Bernard ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

^b EXBIO Praha   (Czech Republic)

^c XINXIANG MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CARMIL2 PROTEIN; CD28 ANTIGEN; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG; ACTIN BINDING PROTEIN; LRRC16A PROTEIN, HUMAN; LRRC16A PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL FATE; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; JURKAT CELL LINE; LYMPHOCYTE DIFFERENTIATION; MASS SPECTROMETRY; MOUSE; NONHUMAN; PLECKSTRIN HOMOLOGY DOMAIN; PRIORITY JOURNAL; RAJI CELL LINE; T LYMPHOCYTE; TH1 CELL; TH17 CELL; ANIMAL; BIOLOGICAL MODEL; BONE MARROW CELL; CHEMISTRY; DENDRITIC CELL; ENDOCYTOSIS; GENE TARGETING; GENETICS; HEK293 CELL LINE; LYMPHOCYTE; METABOLISM; MUTATION; NATURAL KILLER CELL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN MULTIMERIZATION; PROTEOMICS; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; THYMOCYTE;

AMINO ACID MOTIFS; ANIMALS; ANTIGENS, CD28; DENDRITIC CELLS; ENDOCYTOSIS; GENE TARGETING; HEK293 CELLS; HUMANS; JURKAT CELLS; KILLER CELLS, NATURAL; LYMPHOCYTES; MICE; MICROFILAMENT PROTEINS; MODELS, BIOLOGICAL; MUTATION; MYELOID CELLS; PROTEIN DOMAINS; PROTEIN INTERACTION MAPPING; PROTEIN MULTIMERIZATION; PROTEOMICS; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; T-LYMPHOCYTES, REGULATORY; THYMOCYTES;

EID: 85008149494     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/JEM.20160579     Document Type: Article

References (54)

1. Ai, H.W., J.N. Henderson, S.J. Remington, and R.E. Campbell. 2006. Directed evolution of a monomeric, bright and photostable version of Clavularia cyan fluorescent protein: structural characterization and applications in fluorescence imaging. Biochem. J. 400:531-540. http://dx.doi.org/10.1042/BJ20060874
2. Bunting, M., K.E. Bernstein, J.M. Greer, M.R. Capecchi, and K.R. Thomas. 1999. Targeting genes for self-excision in the germ line. Genes Dev. 13:1524-1528. http://dx.doi.org/10.1101/gad.13.12.1524
3. Chiossone, L., J. Chaix, N. Fuseri, C. Roth, E. Vivier, and T. Walzer. 2009. Maturation of mouse NK cells is a 4-stage developmental program. Blood. 113:5488-5496. http://dx.doi.org/10.1182/blood-2008-10.-187179
4. Cox, J., and M. Mann. 2008. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26:1367-1372. http://dx.doi.org/10.1038/nbt.1511
5. Cox, J., N. Neuhauser, A. Michalski, R.A. Scheltema, J.V. Olsen, and M. Mann. 2011. Andromeda: a peptide search engine integrated into the MaxQuant environment. J. Proteome Res. 10:1794-1805. http://dx.doi.org/10.1021/pr101065j
6. Cox, J., M.Y. Hein, C.A. Luber, I. Paron, N. Nagaraj, and M. Mann. 2014. Accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction, termed MaxLFQ. Mol. Cell. Proteomics. 13:2513-2526. http://dx.doi.org/10.1074/mcp.M113.031591
7. Delogu, A., A. Schebesta, Q. Sun, K. Aschenbrenner, T. Perlot, and M. Busslinger. 2006. Gene repression by Pax5 in B cells is essential for blood cell homeostasis and is reversed in plasma cells. Immunity. 24:269-281. http://dx.doi.org/10.1016/j.immuni.2006.01.012
8. Dodson, L.F., J.S. Boomer, C.M. Deppong, D.D. Shah, J. Sim, T.L. Bricker, J.H. Russell, and J.M. Green. 2009. Targeted knock-in mice expressing mutations of CD28 reveal an essential pathway for costimulation. Mol. Cell. Biol. 29:3710-3721. http://dx.doi.org/10.1128/MCB.01869-08
9. Eastburn, D.J., M.M. Zegers, and K.E. Mostov. 2012. Scrib regulates HGFmediated epithelial morphogenesis and is stabilized by Sgt1-HSP90. J. Cell Sci. 125:4147-4157. http://dx.doi.org/10.1242/jcs.108670
10. Edwards, M., A. Zwolak, D.A. Schafer, D. Sept, R. Dominguez, and J.A. Cooper. 2014. Capping protein regulators fine-tune actin assembly dynamics. Nat. Rev. Mol. Cell Biol. 15:677-689. http://dx.doi.org/10.1038/nrm3869
11. Fan, Q.R., and W.A. Hendrickson. 2005. Structure of human folliclestimulating hormone in complex with its receptor. Nature. 433:269-277. http://dx.doi.org/10.1038/nature03206
12. Fujiwara, I., K. Remmert, and J.A. Hammer III. 2010. Direct observation of the uncapping of capping protein-capped actin filaments by CAR MIL homology domain 3. J. Biol. Chem. 285:2707-2720. http://dx.doi.org/10.1074/jbc.M109.031203
13. Galea-Lauri, J., D. Darling, S.U. Gan, L. Krivochtchapov, M. Kuiper, J. Gäken, B. Souberbielle, and F. Farzaneh. 1999. Expression of a variant of CD28 on a subpopulation of human NK cells: implications for B7-mediated stimulation of NK cells. J. Immunol. 163:62-70
14. Hernandez-Valladares, M., T. Kim, B. Kannan, A. Tung, A.H. Aguda, M. Larsson, J.A. Cooper, and R.C. Robinson. 2010. Structural characterization of a capping protein interaction motif defines a family of actin filament regulators. Nat. Struct. Mol. Biol. 17:497-503. http://dx.doi.org/10.1038./nsmb.1792
15. Higo, K., M. Oda, H. Morii, J. Takahashi, Y. Harada, S. Ogawa, and R. Abe. 2014. Quantitative analysis by surface plasmon resonance of CD28 interaction with cytoplasmic adaptor molecules Grb2, Gads and p85 PI3K. Immunol. Invest. 43:278-291. http://dx.doi.org/10.3109/08820139.2013.875039
16. Horejsí, V., W. Zhang, and B. Schraven. 2004. Transmembrane adaptor proteins: organizers of immunoreceptor signalling. Nat. Rev. Immunol. 4:603-616. http://dx.doi.org/10.1038/nri1414
17. Hukelmann, J.L., K.E. Anderson, L.V. Sinclair, K.M. Grzes, A.B. Murillo, P.T. Hawkins, L.R. Stephens, A.I. Lamond, and D.A. Cantrell. 2016. The cytotoxic T cell proteome and its shaping by the kinase mTOR. Nat. Immunol. 17:104-112. http://dx.doi.org/10.1038/ni.3314
18. Jiang, C., and X. Lin. 2012. Regulation of NF-?B by the CARD proteins. Immunol. Rev. 246:141-153. http://dx.doi.org/10.1111/j.1600-065X.2012.01110.x
19. Junttila, M.R., S. Saarinen, T. Schmidt, J. Kast, and J. Westermarck. 2005. Single-step Strep-tag purification for the isolation and identification of protein complexes from mammalian cells. Proteomics. 5:1199-1203. http://dx.doi.org/10.1002/pmic.200400991
20. Kibe, T., G.A. Osawa, C.E. Keegan, and T. de Lange. 2010. Telomere protection by TPP1 is mediated by POT1a and POT1b. Mol. Cell. Biol. 30:1059-1066. http://dx.doi.org/10.1128/MCB.01498-09
21. Kim, T., G.E. Ravilious, D. Sept, and J.A. Cooper. 2012. Mechanism for CAR MIL protein inhibition of heterodimeric actin-capping protein. J. Biol. Chem. 287:15251-15262. http://dx.doi.org/10.1074/jbc.M112.345447
22. Kong, K.F., T. Yokosuka, A.J. Canonigo-Balancio, N. Isakov, T. Saito, and A. Altman. 2011. A motif in the V3 domain of the kinase PKC-? determines its localization in the immunological synapse and functions in T cells via association with CD28. Nat. Immunol. 12:1105-1112. http://dx.doi.org/10.1038/ni.2120
23. Lanier, M.H., T. Kim, J.A. Cooper, E. Judokusumo, G. Carmona, F.B. Gertler, L.C. Kam, C.V. Carman, J.K. Burkhardt, D.J. Irvine, and M.L. Dustin. 2015. CAR MIL2 is a novel molecular connection between vimentin and actin essential for cell migration and invadopodia formation. Mol. Biol. Cell. 26:4577-4588. http://dx.doi.org/10.1091/mbc.E15-08-0552
24. Lanier, M.H., P. McConnell, and J.A. Cooper. 2016. Cell migration and invadopodia formation require a membrane-binding domain of CAR MIL2. J. Biol. Chem. 291:1076-1091. http://dx.doi.org/10.1074/jbc.M115.676882
25. Liang, Y., H. Niederstrasser, M. Edwards, C.E. Jackson, and J.A. Cooper. 2009. Distinct roles for CAR MIL isoforms in cell migration. Mol. Biol. Cell. 20:5290-5305. http://dx.doi.org/10.1091/mbc.E08-10-1071
26. Liang, Y., M. Cucchetti, R. Roncagalli, T. Yokosuka, A. Malzac, E. Bertosio, J. Imbert, I.J. Nijman, M. Suchanek, T. Saito, et al. 2013. The lymphoid lineage-specific actin-uncapping protein Rltpr is essential for costimulation via CD28 and the development of regulatory T cells. Nat. Immunol. 14:858-866. http://dx.doi.org/10.1038/ni.2634
27. Macal, M., M.A. Tam, C. Hesser, J. Di Domizio, P. Leger, M. Gilliet, and E.I. Zuniga. 2016. CD28 Deficiency Enhances Type I IFN production by murine plasmacytoid dendritic cells. J. Immunol. 196:1900-1909. http://dx.doi.org/10.4049/jimmunol.1501658
28. Malissen, B., C. Grégoire, M. Malissen, and R. Roncagalli. 2014. Integrative biology of T cell activation. Nat. Immunol. 15:790-797. http://dx.doi.org/10.1038/ni.2959
29. Marinari, B., A. Costanzo, A. Viola, F. Michel, G. Mangino, O. Acuto, M. Levrero, E. Piccolella, and L. Tuosto. 2002. Vav cooperates with CD28 to induce NF-kappaB activation via a pathway involving Rac-1 and mitogenactivated kinase kinase 1. Eur. J. Immunol. 32:447-456. http://dx.doi.org/10.1002/1521-4141(200202)32 :2<447::AID-IMMU447>3.0.CO;2-5
30. Mingueneau, M., R. Roncagalli, C. Grégoire, A. Kissenpfennig, A. Miazek, C. Archambaud, Y. Wang, P. Perrin, E. Bertosio, A. Sansoni, et al. 2009. Loss of the LAT adaptor converts antigen-responsive T cells into pathogenic effectors that function independently of the T cell receptor. Immunity. 31:197-208. http://dx.doi.org/10.1016/j.immuni.2009.05.013
31. Okkenhaug, K., L. Wu, K.M. Garza, J. La Rose, W. Khoo, B. Odermatt, T.W. Mak, P.S. Ohashi, and R. Rottapel. 2001. A point mutation in CD28. distinguishes proliferative signals from survival signals. Nat. Immunol. 2:325-332. http://dx.doi.org/10.1038/86327
32. Pagán, A.J., M. Pepper, H.H. Chu, J.M. Green, and M.K. Jenkins. 2012. CD28. promotes CD4+ T cell clonal expansion during infection independently of its YMNM and PYAP motifs. J. Immunol. 189:2909-2917. http://dx.doi.org/10.4049/jimmunol.1103231
33. Pettitt, S.J., Q. Liang, X.Y. Rairdan, J.L. Moran, H.M. Prosser, D.R. Beier, K.C. Lloyd, A. Bradley, and W.C. Skarnes. 2009. Agouti C57BL/6N embryonic stem cells for mouse genetic resources. Nat. Methods. 6:493-495. http://dx.doi.org/10.1038/nmeth.1342
34. Raab, M., S. Pfister, and C.E. Rudd. 2001. CD28 signaling via VAV/SLP-76 adaptors: regulation of cytokine transcription independent of TCR ligation. Immunity. 15:921-933. http://dx.doi.org/10.1016/S1074.-7613(01)00248-5
35. Rodríguez, C.I., F. Buchholz, J. Galloway, R. Sequerra, J. Kasper, R. Ayala, A.F. Stewart, and S.M. Dymecki. 2000. High-efficiency deleter mice show that FLPe is an alternative to Cre-loxP. Nat. Genet. 25:139-140. http://dx.doi.org/10.1038/75973
36. Roncagalli, R., S. Hauri, F. Fiore, Y. Liang, Z. Chen, A. Sansoni, K. Kanduri, R. Joly, A. Malzac, H. Lähdesmäki, et al. 2014. Quantitative proteomics analysis of signalosome dynamics in primary T cells identifies the surface receptor CD6 as a Lat adaptor-independent TCR signaling hub. Nat. Immunol. 15:384-392. http://dx.doi.org/10.1038/ni.2843
37. Rozanski, C.H., A. Utley, L.M. Carlson, M.R. Farren, M. Murray, L.M. Russell, J.R. Nair, Z. Yang, W. Brady, L.A. Garrett-Sinha, et al. 2015. CD28 promotes plasma cell survival, sustained antibody responses, and BLI MP-1 upregulation through its distal PYAP proline motif. J. Immunol. 194:4717-4728. http://dx.doi.org/10.4049/jimmunol.1402260
38. Shahinian, A., K. Pfeffer, K.P. Lee, T.M. Kündig, K. Kishihara, A. Wakeham, K. Kawai, P.S. Ohashi, C.B. Thompson, and T.W. Mak. 1993. Differential T cell costimulatory requirements in CD28-deficient mice. Science. 261:609-612. http://dx.doi.org/10.1126/science.7688139
39. Shevchenko, A., M. Wilm, O. Vorm, and M. Mann. 1996. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68:850-858. http://dx.doi.org/10.1021/ac950914h
40. Shirasu, K. 2009. The HSP90-SGT1 chaperone complex for NLR immune sensors. Annu. Rev. Plant Biol. 60:139-164. http://dx.doi.org/10.1146/annurev.arplant.59.032607.092906
41. Soriano, P. 1997. The PDGF alpha receptor is required for neural crest cell development and for normal patterning of the somites. Development. 124:2691-2700
42. Soskic, B., O.S. Qureshi, T. Hou, and D.M. Sansom. 2014. A transendocytosis perspective on the CD28/CTLA-4 pathway. Adv. Immunol. 124:95-136. http://dx.doi.org/10.1016/B978-0-12-800147-9.00004-2
43. Srivastava, R., B.J. Burbach, and Y. Shimizu. 2010. NF-kappaB activation in T cells requires discrete control of IkappaB kinase alpha/beta (IKKalpha/beta) phosphorylation and IKKgamma ubiquitination by the ADAP adapter protein. J. Biol. Chem. 285:11100-11105. http://dx.doi.org/10.1074/jbc.M109.068999
44. Tan, Y.X., B.N. Manz, T.S. Freedman, C. Zhang, K.M. Shokat, and A. Weiss. 2014. Inhibition of the kinase Csk in thymocytes reveals a requirement for actin remodeling in the initiation of full TCR signaling. Nat. Immunol. 15:186-194. http://dx.doi.org/10.1038/ni.2772
45. Thome, M., J.E. Charton, C. Pelzer, and S. Hailfinger. 2010. Antigen receptor signaling to NF-kappaB via CAR MA1, BCL10, and MALT1. Cold Spring Harb. Perspect. Biol. 2:a003004. http://dx.doi.org/10.1101/cshperspect.a003004
46. Tian, R., H. Wang, G.D. Gish, E. Petsalaki, A. Pasculescu, Y. Shi, M. Mollenauer, R.D. Bagshaw, N. Yosef, T. Hunter, et al. 2015. Combinatorial proteomic analysis of intercellular signaling applied to the CD28 T-cell costimulatory receptor. Proc. Natl. Acad. Sci. USA. 112:E1594-E1603. http://dx.doi.org/10.1073/pnas.1503286112
47. Vang, K.B., J. Yang, A.J. Pagán, L.X. Li, J. Wang, J.M. Green, A.A. Beg, and M.A. Farrar. 2010. Cutting edge: CD28 and c-Rel-dependent pathways initiate regulatory T cell development. J. Immunol. 184:4074-4077. http://dx.doi.org/10.4049/jimmunol.0903933
48. Wang, X., H.C. Chuang, J.P. Li, and T.H. Tan. 2012. Regulation of PKC-? function by phosphorylation in T cell receptor signaling. Front. Immunol. 3:197. http://dx.doi.org/10.3389/fimmu.2012.00197
49. Wang, Y., C.S. Ma, Y. Ling, A. Bousfiha, Y. Camcioglu, S. Jacquot, K. Payne, E. Crestani, R. Roncagalli, A. Belkadi, et al. 2016. Dual T cell-and B cell-intrinsic deficiency in humans with biallelic RLT PR mutations. J. Exp. Med. This issue. http://dx.doi.org/10.1084/jem.20160576
50. Yang, C., M. Pring, M.A. Wear, M. Huang, J.A. Cooper, T.M. Svitkina, and S.H. Zigmond. 2005. Mammalian CAR MIL inhibits actin filament capping by capping protein. Dev. Cell. 9:209-221. http://dx.doi.org/10.1016/j.devcel.2005.06.008
51. Yokosuka, T., and T. Saito. 2010. The immunological synapse, TCR microclusters, and T cell activation. Curr. Top. Microbiol. Immunol. 340:81-107. http://dx.doi.org/10.1007/978-3-642-03858-7 5
52. Zhang, Q., C.G. Dove, J.L. Hor, H.M. Murdock, D.M. Strauss-Albee, J.A. Garcia, J.N. Mandl, R.A. Grodick, H. Jing, D.B. Chandler-Brown, et al. 2014. DOCK8 regulates lymphocyte shape integrity for skin antiviral immunity. J. Exp. Med. 211:2549-2566. http://dx.doi.org/10.1084/jem.20141307
53. Zhang, Y., J.P. Muyrers, G. Testa, and A.F. Stewart. 2000. DNA cloning by homologous recombination in Escherichia coli. Nat. Biotechnol. 18:1314-1317. http://dx.doi.org/10.1038/82449
54. Zwolak, A., C. Yang, E.A. Feeser, E.M. Ostap, T. Svitkina, and R. Dominguez. 2013. CAR MIL leading edge localization depends on a non-canonical PH domain and dimerization. Nat. Commun. 4:2523. http://dx.doi.org/10.1038/ncomms3523