Intrinsic antiproliferative activity of the innate sensor STI NG in T lymphocytes

Journal of Experimental Medicine

Volumn 214, Issue 6, 2017, Pages 1769-1785

  Cerboni, Silvia ^a   Jeremiah, Nadia ^a   Gentili, Matteo ^a   Gehrmann, Ulf ^a,e   Conrad, Cécile ^a   Stolzenberg, Marie Claude ^b   Picard, Capucine ^c   Neven, Bénédicte ^b,c   Fischer, Alain ^b,c,d   Amigorena, Sébastian ^a   Rieux Laucat, Frédéric ^b   Manel, Nicolas ^a  

^a INSTITUT CURIE   (France)

^b INSERM   (France)

^c HÔPITAL NECKER ENFANTS MALADES   (France)

^d Centre de Recherche Interdisciplinaire en Biologie   (France)

^e ASTRAZENECA R AND D   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CD3 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; RECEPTOR PROTEIN; STING PROTEIN; UNCLASSIFIED DRUG; INTERFERON REGULATORY FACTOR 3; IRF3 PROTEIN, HUMAN; MEMBRANE PROTEIN; MPYS PROTEIN, HUMAN; MUTANT PROTEIN; PROTEIN SERINE THREONINE KINASE; TBK1 PROTEIN, HUMAN;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL TISSUE; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CARBOXY TERMINAL SEQUENCE; CD3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; GENE; GENE MUTATION; GOLGI COMPLEX; HUMAN; HUMAN CELL; INNATE IMMUNITY; LYMPHOCYTE PROLIFERATION; MEMORY CELL; MITOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; T LYMPHOCYTE; TMEM173 GENE; BINDING SITE; CELL PROLIFERATION; CHEMISTRY; CYTOLOGY; DENDRITIC CELL; METABOLISM; SIGNAL TRANSDUCTION;

BINDING SITES; CELL PROLIFERATION; DENDRITIC CELLS; HUMANS; IMMUNITY, INNATE; INTERFERON REGULATORY FACTOR-3; MEMBRANE PROTEINS; MITOSIS; MUTANT PROTEINS; PROTEIN DOMAINS; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 85021856488     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20161674     Document Type: Article

References (42)

1. Abe, T., and G.N. Barber. 2014. Cytosolic-DNA-mediated, STI NGdependent proinflammatory gene induction necessitates canonical NF-κB activation through TBK1. J. Virol. 88:5328-5341. http ://dx .doi .org/10 .1128/JVI .00037-14
2. Bruchard, M., C. Rebé, V. Derangère, D. Togbé, B. Ryffel, R. Boidot, E. Humblin, A. Hamman, F. Chalmin, H. Berger, et al. 2015. The receptor NLRP3 is a transcriptional regulator of TH2 differentiation. Nat. Immunol. 16:859-870. http ://dx .doi .org/10 .1038/ni .3202
3. Burdette, D.L., K.M. Monroe, K. Sotelo-Troha, J.S. Iwig, B. Eckert, M. Hyodo, Y. Hayakawa, and R.E. Vance. 2011. STI NG is a direct innate immune sensor of cyclic di-GMP. Nature. 478:515-518. http ://dx .doi .org/10 .1038/nature10429
4. Chien, Y., C. Scuoppo, X. Wang, X. Fang, B. Balgley, J.E. Bolden, P. Premsrirut, W. Luo, A. Chicas, C.S. Lee, et al. 2011. Control of the senescenceassociated secretory phenotype by NF-κB promotes senescence and enhances chemosensitivity. Genes Dev. 25:2125-2136. http ://dx .doi .org/10 .1101/gad .17276711
5. Ching, L.M., Z. Cao, C. Kieda, S. Zwain, M.B. Jameson, and B.C. Baguley. 2002. Induction of endothelial cell apoptosis by the antivascular agent 5,6-dimethylxanthenone-4-acetic acid. Br. J. Cancer. 86:1937-1942. http ://dx .doi .org/10 .1038/sj .bjc .6600368
6. Colanzi, A., and C. Sütterlin. 2013. Signaling at the Golgi during mitosis. Methods Cell Biol. 118:383-400. http ://dx .doi .org/10 .1016/B978-0-12-417164-0 .00023-9
7. Courtois, G., A. Smahi, J. Reichenbach, R. Döffinger, C. Cancrini, M. Bonnet, A. Puel, C. Chable-Bessia, S. Yamaoka, J. Feinberg, et al. 2003. A hypermorphic IκBα mutation is associated with autosomal dominant anhidrotic ectodermal dysplasia and T cell immunodeficiency. J. Clin. Invest. 112:1108-1115. http ://dx .doi .org/10 .1172/JCI18714
8. Crow, Y.J., and N. Manel. 2015. Aicardi-Goutières syndrome and the type I interferonopathies. Nat. Rev. Immunol. 15:429-440. http ://dx .doi .org/10 .1038/nri3850
9. Gao, D., J. Wu, Y.T. Wu, F. Du, C. Aroh, N. Yan, L. Sun, and Z.J. Chen. 2013. Cyclic GMP-AMP synthase is an innate immune sensor of HIV and other retroviruses. Science. 341:903-906. http ://dx .doi .org/10 .1126/science .1240933
10. Gentili, M., J. Kowal, M. Tkach, T. Satoh, X. Lahaye, C. Conrad, M. Boyron, B. Lombard, S. Durand, G. Kroemer, et al. 2015. Transmission of innate immune signaling by packaging of cGAMP in viral particles. Science. 349:1232-1236. http ://dx .doi .org/10 .1126/science .aab3628
11. Greil, J., T. Rausch, T. Giese, O.R. Bandapalli, V. Daniel, I. Bekeredjian-Ding, A.M. Stütz, C. Drees, S. Roth, J. Ruland, et al. 2013. Whole-exome sequencing links caspase recruitment domain 11 (CARD11) inactivation to severe combined immunodeficiency. J. Allergy Clin. Immunol. 131:1376-83.e3. http ://dx .doi .org/10 .1016/j .jaci .2013 .02 .012
12. Ishikawa, H., and G.N. Barber. 2008. STI NG is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature. 455:674-678. http ://dx .doi .org/10 .1038/nature07317
13. Ishikawa, H., Z. Ma, and G.N. Barber. 2009. STI NG regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature. 461:788-792. http ://dx .doi .org/10 .1038/nature08476
14. Iwasaki, A., and R. Medzhitov. 2010. Regulation of adaptive immunity by the innate immune system. Science. 327:291-295. http ://dx .doi .org/10 .1126/science .1183021
15. Iwasaki, A., and R. Medzhitov. 2015. Control of adaptive immunity by the innate immune system. Nat. Immunol. 16:343-353. http ://dx .doi .org/10 .1038/ni .3123
16. Janeway, C.A. Jr., and R. Medzhitov. 2002. Innate immune recognition. Annu. Rev. Immunol. 20:197-216. http ://dx .doi .org/10 .1146/annurev .immunol .20 .083001 .084359
17. Jeremiah, N., B. Neven, M. Gentili, I. Callebaut, S. Maschalidi, M.C. Stolzenberg, N. Goudin, M.L. Frémond, P. Nitschke, T.J. Molina, et al. 2014. Inherited STI NG-activating mutation underlies a familial inflammatory syndrome with lupus-like manifestations. J. Clin. Invest. 124:5516-5520. http ://dx .doi .org/10 .1172/JCI79100
18. Jin, L., L.G. Xu, I.V. Yang, E.J. Davidson, D.A. Schwartz, M.M. Wurfel, and J.C. Cambier. 2011. Identification and characterization of a loss-of-function human MPYS variant. Genes Immun. 12:263-269. http ://dx .doi .org/10 .1038/gene .2010 .75
19. Kim, J.H., S.R. Lee, L.H. Li, H.J. Park, J.H. Park, K.Y. Lee, M.K. Kim, B.A. Shin, and S.Y. Choi. 2011. High cleavage efficiency of a 2A peptide derived from porcine teschovirus-1 in human cell lines, zebrafish and mice. PLoS One. 6:e18556. http ://dx .doi .org/10 .1371/journal .pone .0018556
20. Kranzusch, P.J., S.C. Wilson, A.S. Lee, J.M. Berger, J.A. Doudna, and R.E. Vance. 2015. Ancient origin of cGAS-STI NG reveals mechanism of universal 2',3' cGAMP signaling. Mol. Cell. 59:891-903. http ://dx .doi .org/10 .1016/j .molcel .2015 .07 .022
21. Lahaye, X., T. Satoh, M. Gentili, S. Cerboni, C. Conrad, I. Hurbain, A. El Marjou, C. Lacabaratz, J.D. Lelièvre, and N. Manel. 2013. The capsids of HIV-1 and HIV-2 determine immune detection of the viral cDNA by the innate sensor cGAS in dendritic cells. Immunity. 39:1132-1142. http ://dx .doi .org/10 .1016/j .immuni .2013 .11 .002
22. Lahaye, X., T. Satoh, M. Gentili, S. Cerboni, A. Silvin, C. Conrad, A. Ahmed-Belkacem, E.C. Rodriguez, J.F. Guichou, N. Bosquet, et al. 2016. Nuclear envelope protein SUN2 promotes cyclophilin-A-dependent steps of HIV replication. Cell Reports. 15:879-892. http ://dx .doi .org/10 .1016/j .celrep .2016 .03 .074
23. Li, X.D., J. Wu, D. Gao, H. Wang, L. Sun, and Z.J. Chen. 2013. Pivotal roles of cGAS-cGAMP signaling in antiviral defense and immune adjuvant effects. Science. 341:1390-1394. http ://dx .doi .org/10 .1126/science .1244040
24. Liu, S., X. Cai, J. Wu, Q. Cong, X. Chen, T. Li, F. Du, J. Ren, Y.T. Wu, N.V. Grishin, and Z.J. Chen. 2015. Phosphorylation of innate immune adaptor proteins MAVS, STI NG, and TRIF induces IRF3 activation. Science. 347:aaa2630. http ://dx .doi .org/10 .1126/science .aaa2630
25. Liu, Y., A.A. Jesus, B. Marrero, D. Yang, S.E. Ramsey, G.A. Montealegre Sanchez, K. Tenbrock, H. Wittkowski, O.Y. Jones, H.S. Kuehn, et al. 2014. Activated STI NG in a vascular and pulmonary syndrome. N. Engl. J. Med. 371:507-518. http ://dx .doi .org/10 .1056/NEJMoa1312625
26. Malik, P., N. Zuleger, J.I. de las Heras, N. Saiz-Ros, A.A. Makarov, V. Lazou, P. Meinke, M. Waterfall, D.A. Kelly, and E.C. Schirmer. 2014. NET23/STI NG promotes chromatin compaction from the nuclear envelope. PLoS One. 9:e111851. http ://dx .doi .org/10 .1371/journal .pone .0111851
27. Malissen, M., A. Gillet, L. Ardouin, G. Bouvier, J. Trucy, P. Ferrier, E. Vivier, and B. Malissen. 1995. Altered T cell development in mice with a targeted mutation of the CD3-epsilon gene. EMBO J. 14:4641-4653
28. Meyts, I., and J.L. Casanova. 2016. A human inborn error connects the a's. Nat. Immunol. 17:472-474. http ://dx .doi .org/10 .1038/ni .3420
29. Onorati, M., Z. Li, F. Liu, A.M. Sousa, N. Nakagawa, M. Li, M.T. Dell'Anno, F.O. Gulden, S. Pochareddy, A.T. Tebbenkamp, et al. 2016. Zika virus disrupts phospho-TBK1 localization and mitosis in human neuroepithelial stem cells and radial glia. Cell Reports. 16:2576-2592. http ://dx .doi .org/10 .1016/j .celrep .2016 .08 .038
30. Pannicke, U., B. Baumann, S. Fuchs, P. Henneke, A. Rensing-Ehl, M. Rizzi, A. Janda, K. Hese, M. Schlesier, K. Holzmann, et al. 2013. Deficiency of innate and acquired immunity caused by an IKB KB mutation. N. Engl. J. Med. 369:2504-2514. http ://dx .doi .org/10 .1056/NEJMoa1309199
31. Pillai, S., J. Nguyen, J. Johnson, E. Haura, D. Coppola, and S. Chellappan. 2015. Tank binding kinase 1 is a centrosome-associated kinase necessary for microtubule dynamics and mitosis. Nat. Commun. 6:10072. http ://dx .doi .org/10 .1038/ncomms10072
32. Pourcelot, M., N. Zemirli, L. Silva Da Costa, R. Loyant, D. Garcin, D. Vitour, I. Munitic, A. Vazquez, and D. Arnoult. 2016. The Golgi apparatus acts as a platform for TBK1 activation after viral RNA sensing. BMC Biol. 14:69. http ://dx .doi .org/10 .1186/s12915-016-0292-z
33. Sharma, S., A.M. Campbell, J. Chan, S.A. Schattgen, G.M. Orlowski, R. Nayar, A.H. Huyler, K. Nündel, C. Mohan, L.J. Berg, et al. 2015. Suppression of systemic autoimmunity by the innate immune adaptor STI NG. Proc. Natl. Acad. Sci. USA. 112:E710-E717. http ://dx .doi .org/10 .1073/pnas .1420217112
34. Shinkai, Y., G. Rathbun, K.P. Lam, E.M. Oltz, V. Stewart, M. Mendelsohn, J. Charron, M. Datta, F. Young, A.M. Stall, and F.W. Alt. 1992. RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell. 68:855-867. http ://dx .doi .org/10 .1016/0092-8674(92)90029-C
35. Stepensky, P., B. Keller, M. Buchta, A.K. Kienzler, O. Elpeleg, R. Somech, S. Cohen, I. Shachar, L.A. Miosge, M. Schlesier, et al. 2013. Deficiency of caspase recruitment domain family, member 11 (CARD11), causes profound combined immunodeficiency in human subjects. J. Allergy Clin. Immunol. 131:477-85.e1. http ://dx .doi .org/10 .1016/j .jaci .2012 .11 .050
36. Sun, L., J. Wu, F. Du, X. Chen, and Z.J. Chen. 2013. Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science. 339:786-791. http ://dx .doi .org/10 .1126/science .1232458
37. Tanaka, Y., and Z.J. Chen. 2012. STI NG specifies IRF3 phosphorylation by TBK1 in the cytosolic DNA signaling pathway. Sci. Signal. 5:ra20. http ://dx .doi .org/10 .1126/scisignal .2002521
38. Tang, C.H., J.A. Zundell, S. Ranatunga, C. Lin, Y. Nefedova, J.R. Del Valle, and C.C. Hu. 2016. Agonist-mediated activation of STI NG induces apoptosis in malignant B cells. Cancer Res. 76:2137-2152. http ://dx .doi .org/10 .1158/0008-5472 .CAN-15-1885
39. Torres, J.M., R. Martinez-Barricarte, S. García-Gómez, M.S. Mazariegos, Y. Itan, B. Boisson, R. Rholvarez, A. Jiménez-Reinoso, L. del Pino, R. Rodríguez-Pena, et al. 2014. Inherited BCL10 deficiency impairs hematopoietic and nonhematopoietic immunity. J. Clin. Invest. 124:5239-5248. http ://dx .doi .org/10 .1172/JCI77493
40. Wu, J., L. Sun, X. Chen, F. Du, H. Shi, C. Chen, and Z.J. Chen. 2013. Cyclic GMP-AMP is an endogenous second messenger in innate immune signaling by cytosolic DNA. Science. 339:826-830. http ://dx .doi .org/10 .1126/science .1229963
41. Yan, N., A.D. Regalado-Magdos, B. Stiggelbout, M.A. Lee-Kirsch, and J. Lieberman. 2010. The cytosolic exonuclease TREX1 inhibits the innate immune response to human immunodeficiency virus type 1. Nat. Immunol. 11:1005-1013. http ://dx .doi .org/10 .1038/ni .1941
42. Yi, G., V.P. Brendel, C. Shu, P. Li, S. Palanathan, and C. Cheng Kao. 2013. Single nucleotide polymorphisms of human STI NG can affect innate immune response to cyclic dinucleotides. PLoS One. 8:e77846. http ://dx .doi .org/10 .1371/journal .pone .0077846