An Slfn2 mutation causes lymphoid and myeloid immunodeficiency due to loss of immune cell quiescence

Nature Immunology

Volumn 11, Issue 4, 2010, Pages 335-343

  Berger, Michael ^a   Krebs, Philippe ^a   Crozat, Karine ^a,c   Li, Xiaohong ^a   Croker, Ben A ^a,c,d   Siggs, Owen M ^a   Popkin, Daniel ^a   Du, Xin ^a   Lawson, Brian R ^a   Theofilopoulos, Argyrios N ^a   Xia, Yu ^a   Khovananth, Kevin ^a   Moresco, Eva Marie Y ^a   Satoh, Takashi ^b   Takeuchi, Osamu ^b   Akira, Shizuo ^b   Beutler, Bruce ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b OSAKA UNIVERSITY   (Japan)

^c CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^d WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ETHYLNITROSOUREA; FAS LIGAND; GAMMA INTERFERON; HERMES ANTIGEN; INTERLEUKIN 2 RECEPTOR BETA; INTERLEUKIN 7 RECEPTOR ALPHA; PROTEIN BCL 2; REGULATOR PROTEIN; SCHLAFEN 2; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOMEGALOVIRUS; DNA REPLICATION; HOMOZYGOSITY; HOST RESISTANCE; IMMUNE DEFICIENCY; INFECTION SENSITIVITY; LISTERIA MONOCYTOGENES; LYMPHOCYTE PROLIFERATION; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MONOCYTE; MOUSE; NATURAL KILLER CELL MEDIATED CYTOTOXICITY; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION;

ANIMALS; APOPTOSIS; BASE SEQUENCE; CELL CYCLE PROTEINS; CELL SEPARATION; FLOW CYTOMETRY; IMMUNOLOGIC DEFICIENCY SYNDROMES; LEUKOCYTES, MONONUCLEAR; LYMPHOCYTE ACTIVATION; MICE; MICE, TRANSGENIC; MUTATION; PHENOTYPE; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 77949837209     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.1847     Document Type: Article

References (46)

1. Yusuf, I. & Fruman, D.A. Regulation of quiescence in lymphocytes. Trends Immunol. 24, 380-386 (2003).
2. Chechlinska, M. et al. Molecular signature of cell cycle exit induced in human T lymphoblasts by IL-2 withdrawal. BMC Genomics 10, 261 (2009).
3. Coller, H.A., Sang, L. & Roberts, J.M. A new description of cellular quiescence. PLoS Biol. 4, e83 (2006).
4. Glynne, R., Ghandour, G., Rayner, J., Mack, D.H. & Goodnow, C.C. B-lymphocyte quiescence, tolerance and activation as viewed by global gene expression profling on microarrays. Immunol. Rev. 176, 216-246 (2000).
5. Teague, T.K. et al. Activation changes the spectrum but not the diversity of genes expressed by T cells. Proc. Natl. Acad. Sci. USA 96, 12691-12696 (1999).
6. Tothova, Z. et al. FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell 128, 325-339 (2007).
7. Kuo, C.T., Veselits, M.L. & Leiden, J.M. LKLF: A transcriptional regulator of single-positive T cell quiescence and survival. Science 277, 1986-1990 (1997).
8. Tzachanis, D. et al. Tob is a negative regulator of activation that is expressed in anergic and quiescent T cells. Nat. Immunol. 2, 1174-1182 (2001).
9. Crozat, K. et al. Analysis of the MCMV resistome by ENU mutagenesis. Mamm. Genome 17, 398-406 (2006).
10. Webb, J.R., Lee, S.H. & Vidal, S.M. Genetic control of innate immune responses against cytomegalovirus: MCMV meets its match 3. Genes Immun. 3, 250-262 (2002).
11. Jiang, Z. et al. Details of Toll-like receptor:adapter interaction revealed by germ-line mutagenesis. Proc. Natl. Acad. Sci. USA 103, 10961-10966 (2006).
12. Macian, F. NFAT proteins: key regulators of T-cell development and function. Nat. Rev. Immunol. 5, 472-484 (2005).
13. Li, Q. & Verma, I.M. NF-κB regulation in the immune system. Nat. Rev. Immunol. 2, 725-734 (2002).
14. Juntilla, M.M. & Koretzky, G.A. Critical roles of the PI3K/Akt signaling pathway in T cell development. Immunol. Lett. 116, 104-110 (2008).
15. Wada, T. & Penninger, J.M. Mitogen-activated protein kinases in apoptosis regulation. Oncogene 23, 2838-2849 (2004).
16. + T cells. Immunol. Rev. 192, 131-142 (2003).
17. Boyman, O., Ramsey, C., Kim, D.M., Sprent, J. & Surh, C.D. IL-7/anti-IL-7 mAb complexes restore T cell development and induce homeostatic T cell expansion without lymphopenia. J. Immunol. 180, 7265-7275 (2008).
18. Kieper, W.C. & Jameson, S.C. Homeostatic expansion and phenotypic conversion of naive T cells in response to self peptide/MHC ligands. Proc. Natl. Acad. Sci. USA 96, 13306-13311 (1999).
19. Goldrath, A.W., Bogatzki, L.Y. & Bevan, M.J. Naive T cells transiently acquire a memory-like phenotype during homeostasis-driven proliferation. J. Exp. Med. 192, 557-564 (2000).
20. Cho, B.K., Rao, V.P., Ge, Q., Eisen, H.N. & Chen, J. Homeostasis-stimulated proliferation drives naive T cells to differentiate directly into memory T cells. J. Exp. Med. 192, 549-556 (2000).
21. Khaled, A.R. & Durum, S.K. Lymphocide: cytokines and the control of lymphoid homeostasis. Nat. Rev. Immunol. 2, 817-830 (2002).
22. Hildeman, D.A. et al. Activated T cell death in vivo mediated by proapoptotic bcl-2 family member bim. Immunity 16, 759-767 (2002).
23. Pellegrini, M., Belz, G., Bouillet, P. & Strasser, A. Shutdown of an acute T cell immune response to viral infection is mediated by the proapoptotic Bcl-2 homology 3-only protein Bim. Proc. Natl. Acad. Sci. USA 100, 14175-14180 (2003).
24. Krammer, P.H., Arnold, R. & Lavrik, I.N. Life and death in peripheral T cells. Nat. Rev. Immunol. 7, 532-542 (2007).
25. Boyman, O., Cho, J.H., Tan, J.T., Surh, C.D. & Sprent, J. A major histocompatibility complex class I-dependent subset of memory phenotype CD8+ cells. J. Exp. Med. 203, 1817-1825 (2006).
26. Oehen, S. & Brduscha-Riem, K. Differentiation of naive CTL to effector and memory CTL: correlation of effector function with phenotype and cell division. J. Immunol. 161, 5338-5346 (1998).
27. Chao, C.C., Jensen, R. & Dailey, M.O. Mechanisms of L-selectin regulation by activated T cells. J. Immunol. 159, 1686-1694 (1997).
28. Serbina, N.V. et al. Sequential MyD88-independent and-dependent activation of innate immune responses to intracellular bacterial infection. Immunity 19, 891-901 (2003).
29. Schwarz, D.A., Katayama, C.D. & Hedrick, S.M. Schlafen, a new family of growth regulatory genes that affect thymocyte development. Immunity 9, 657-668 (1998).
30. + T cell responsiveness to antigen. J. Immunol. 161, 2141-2150 (1998).
31. Buckley, A.F., Kuo, C.T. & Leiden, J.M. Transcription factor LKLF is suffcient to program T cell quiescence via a c-Myc-dependent pathway. Nat. Immunol. 2, 698-704 (2001).
32. Bai, A., Hu, H., Yeung, M. & Chen, J. Kruppel-like factor 2 controls T cell traffcking by activating L-selectin (CD62L) and sphingosine-1-phosphate receptor 1 transcription. J. Immunol. 178, 7632-7639 (2007).
33. Carlson, C.M. et al. Kruppel-like factor 2 regulates thymocyte and T-cell migration. Nature 442, 299-302 (2006).
34. Kerdiles, Y.M. et al. Foxo1 links homing and survival of naive T cells by regulating L-selectin, CCR7 and interleukin 7 receptor. Nat. Immunol. 10, 176-184 (2009).
35. Geserick, P., Kaiser, F., Klemm, U., Kaufmann, S.H. & Zerrahn, J. Modulation of T cell development and activation by novel members of the Schlafen (slfn) gene family harbouring an RNA helicase-like motif. Int. Immunol. 16, 1535-1548 (2004).
36. Ferguson, D.A., Chiang, J.T., Richardson, J.A. & Graff, J. eXPRESSION: an in silico tool to predict patterns of gene expression. Gene Expr. Patterns 5, 619-628 (2005).
37. Hanson, P.I. & Whiteheart, S.W. AAA+ proteins: have engine, will work. Nat. Rev. Mol. Cell Biol. 6, 519-529 (2005).
38. White, S.R. & Lauring, B. AAA+ ATPases: achieving diversity of function with conserved machinery. Traffc 8, 1657-1667 (2007).
39. Brady, G., Boggan, L., Bowie, A. & O'Neill, L.A. Schlafen-1 causes a cell cycle arrest by inhibiting induction of cyclin D1. J. Biol. Chem. 280, 30723-30734 (2005).
40. Kaufmann, A. et al. Defense against infuenza A virus infection: essential role of the chemokine system. Immunobiology 204, 603-613 (2001).
41. Barbalat, R., Lau, L., Locksley, R.M. & Barton, G.M. Toll-like receptor 2 on infammatory monocytes induces type I interferon in response to viral but not bacterial ligands. Nat. Immunol. 10, 1200-1207 (2009).
42. Gubser, C. et al. Camelpox virus encodes a schlafen-like protein that affects orthopoxvirus virulence. J. Gen. Virol. 88, 1667-1676 (2007).
43. Hoebe, K., Du, X., Goode, J., Mann, N. & Beutler, B. Lps2: a new locus required for responses to lipopolysaccharide, revealed by germline mutagenesis and phenotypic screening. J. Endotoxin Res. 9, 250-255 (2003).
44. Rutschmann, S. et al. PanR1, a dominant negative missense allele of the gene encoding TNF-α (Tnf), does not impair lymphoid development. J. Immunol. 176, 7525-7532 (2006).
45. Krebs, P. et al. NK-cell-mediated killing of target cells triggers robust antigen-specifc T-cell-mediated and humoral responses. Blood 113, 6593-6602 (2009).
46. Reeves, J.P., Reeves, P.A. and Chin, L.T. in Current Protocols in Immunol.ogy (eds. Coligan, J.E. et al.) 1.10.5-1.10.6 (John Wiley & Sons, Hoboken, New Jersey, 2009).