DNA-PKcs controls an endosomal signaling pathway for a proinflammatory response by natural killer cells

Science Signaling

Volumn 3, Issue 110, 2010, Pages

  Rajagopalan, Sumati ^a   Moyle, Mark W ^a   Joosten, Irma ^b   Long, Eric O ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DEPENDENT PROTEIN KINASE; HLA G ANTIGEN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOGLOBULIN RECEPTOR; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL4; PROTEIN KINASE B; HLA ANTIGEN; HLA ANTIGEN CLASS 1; HLA-G ANTIGEN; KIR2DL4 PROTEIN, HUMAN;

ARTICLE; CONTROLLED STUDY; ENDOSOME; ENZYME ACTIVE SITE; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; INFLAMMATION; NATURAL KILLER CELL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; CELL LINE; CONFOCAL MICROSCOPY; IMMUNOPRECIPITATION; MASS SPECTROMETRY; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; POLYACRYLAMIDE GEL ELECTROPHORESIS;

CELL LINE; DNA-ACTIVATED PROTEIN KINASE; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENDOSOMES; HISTOCOMPATIBILITY ANTIGENS CLASS I; HLA ANTIGENS; HUMANS; IMMUNOPRECIPITATION; INFLAMMATION; KILLER CELLS, NATURAL; MASS SPECTROMETRY; MICROSCOPY, CONFOCAL; NF-KAPPA B; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, KIR2DL4; SIGNAL TRANSDUCTION;

EID: 77952572147     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2000467     Document Type: Article

References (52)

1. M. Miaczynska, L. Pelkmans, M. Zerial, Not just a sink: Endosomes in control of signal transduction. Curr. Opin. Cell Biol. 16, 400-406 (2004).
2. S. Polo, P. P. Di Fiore, Endocytosis conducts the cell signaling orchestra. Cell 124, 897-900 (2006).
3. M. von Zastrow, A. Sorkin, Signaling on the endocytic pathway. Curr. Opin. Cell Biol. 19, 436-445 (2007).
4. D. Hoeller, S. Volarevic, I. Dikic, Compartmentalization of growth factor receptor signalling. Curr. Opin. Cell Biol. 17, 107-111 (2005).
5. A. Sorkin, M. Von Zastrow, Signal transduction and endocytosis: Close encounters of many kinds. Nat. Rev. Mol. Cell Biol. 3, 600-614 (2002).
6. S. Akira, S. Uematsu, O. Takeuchi, Pathogen recognition and innate immunity. Cell 124, 783-801 (2006).
7. S. Rajagopalan, Y. T. Bryceson, S. P. Kuppusamy, D. E. Geraghty, A. van der Meer, I. Joosten, E. O. Long, Activation of NK cells by an endocytosed receptor for soluble HLA-G. PLoS Biol. 4, e9 (2006).
8. A. Kikuchi-Maki, T. L. Catina, K. S. Campbell, Cutting edge: KIR2DL4 transduces signals into human NK cells through association with the Fc receptor g protein. J. Immunol. 174, 3859-3863 (2005).
9. E. O. Long, Negative signaling by inhibitory receptors: The NK cell paradigm. Immunol. Rev. 224, 70-84 (2008).
10. S. Rajagopalan, E. O. Long, A human histocompatibility leukocyte antigen (HLA)-Gspecific receptor expressed on all natural killer cells. J. Exp. Med. 189, 1093-1100 (1999).
11. S. Rajagopalan, J. Fu, E. O. Long, Cutting edge: Induction of IFN-g production but not cytotoxicity by the killer cell Ig-like receptor KIR2DL4 (CD158d) in resting NK cells. J. Immunol. 167, 1877-1881 (2001).
12. A. Moffett-King, Natural killer cells and pregnancy. Nat. Rev. Immunol. 2, 656-663 (2002).
13. A. Moffett, C. Loke, Immunology of placentation in eutherian mammals. Nat. Rev. Immunol. 6, 584-594 (2006).
14. S. Vallabhapurapu, M. Karin, Regulation and function of NF-kB transcription factors in the immune system. Annu. Rev. Immunol. 27, 693-733 (2009).
15. K. Brown, S. Gerstberger, L. Carlson, G. Franzoso, U. Siebenlist, Control of IkB-a proteolysis by site-specific, signal-induced phosphorylation. Science 267, 1485-1488 (1995).
16. R. J. Salmond, A. Filby, I. Qureshi, S. Caserta, R. Zamoyska, T-cell receptor proximal signaling via the Src-family kinases, Lck and Fyn, influences T-cell activation, differentiation, and tolerance. Immunol. Rev. 228, 9-22 (2009).
17. D. A. Fruman, G. Bismuth, Fine tuning the immune response with PI3K. Immunol. Rev. 228, 253-272 (2009).
18. J. R. Ortaldo, H. A. Young, IL-18 as critical co-stimulatory molecules in modulating the immune response of ITAM bearing lymphocytes. Semin. Immunol. 18, 193-196 (2006).
19. B. D. Manning, L. C. Cantley, AKT/PKB signaling: Navigating downstream. Cell 129, 1261-1274 (2007).
20. L. Bozulic, B. A. Hemmings, PIKKing on PKB: Regulation of PKB activity by phosphorylation. Curr. Opin. Cell Biol. 21, 256-261 (2009).
21. V. Calleja, M. Laguerre, P. J. Parker, B. Larijani, Role of a novel PH-kinase domain interface in PKB/Akt regulation: Structural mechanism for allosteric inhibition. PLoS Biol. 7, e17 (2009).
22. E. Macia, M. Ehrlich, R. Massol, E. Boucrot, C. Brunner, T. Kirchhausen, Dynasore, a cell-permeable inhibitor of dynamin. Dev. Cell 10, 839-850 (2006).
23. S. Duclos, R. Corsini, M. Desjardins, Remodeling of endosomes during lysosome biogenesis involves 'kiss and run' fusion events regulated by rab5. J. Cell Sci. 116, 907-918 (2003).
24. H. Stenmark, R. G. Parton, O. Steele-Mortimer, A. Lutcke, J. Gruenberg, M. Zerial, Inhibition of rab5 GTPase activity stimulates membrane fusion in endocytosis. EMBO J. 13, 1287-1296 (1994).
25. O. N. Ozes, L. D. Mayo, J. A. Gustin, S. R. Pfeffer, L. M. Pfeffer, D. B. Donner, NF-kB activation by tumour necrosis factor requires the Akt serine-threonine kinase. Nature 401, 82-85 (1999).
26. J. A. Romashkova, S. S. Makarov, NF-kB is a target of AKT in anti-apoptotic PDGF signalling. Nature 401, 86-90 (1999).
27. R. T. Abraham, PI 3-kinase related kinases: 'Big' players in stress-induced signaling pathways. DNA Repair (Amst.) 3, 883-887 (2004).
28. L. Bozulic, B. Surucu, D. Hynx, B. A. Hemmings, PKBa/Akt1 acts downstream of DNA-PK in the DNA double-strand break response and promotes survival. Mol. Cell 30, 203-213 (2008).
29. S. J. Collis, T. L. DeWeese, P. A. Jeggo, A. R. Parker, The life and death of DNA-PK. Oncogene 24, 949-961 (2005).
30. A. Kurimasa, S. Kumano, N. V. Boubnov, M. D. Story, C. S. Tung, S. R. Peterson, D. J. Chen, Requirement for the kinase activity of human DNA-dependent protein kinase catalytic subunit in DNA strand break rejoining. Mol. Cell. Biol. 19, 3877-3884 (1999).
31. L. S. Zweifel, R. Kuruvilla, D. D. Ginty, Functions and mechanisms of retrograde neurotrophin signalling. Nat. Rev. Neurosci. 6, 615-625 (2005).
32. S. Kovats, E. K. Main, C. Librach, M. Stubblebine, S. J. Fisher, R. DeMars, A class I antigen, HLA-G, expressed in human trophoblasts. Science 248, 220-223 (1990).
33. J. Trowsdale, A. Moffett, NK receptor interactions with MHC class I molecules in pregnancy. Semin. Immunol. 20, 317-320 (2008).
34. A. van der Meer, H. G. Lukassen, B. van Cranenbroek, E. H. Weiss, D. D. Braat, M. J. van Lierop, I. Joosten, Soluble HLA-G promotes Th1-type cytokine production by cytokineactivated uterine and peripheral natural killer cells. Mol. Hum. Reprod. 13, 123-133 (2007).
35. C. Li, B. L. Houser, M. L. Nicotra, J. L. Strominger, HLA-G homodimer-induced cytokine secretion through HLA-G receptors on human decidual macrophages and natural killer cells. Proc. Natl. Acad. Sci. U. S. A. 106, 5767-5772 (2009).
36. J. Park, J. Feng, Y. Li, O. Hammarsten, D. P. Brazil, B. A. Hemmings, DNA-dependent protein kinase-mediated phosphorylation of protein kinase B requires a specific recognition sequence in the C-terminal hydrophobic motif. J. Biol. Chem. 284, 6169-6174 (2009).
37. J. Feng, J. Park, P. Cron, D. Hess, B. A. Hemmings, Identification of a PKB/Akt hydrophobic motif Ser-473 kinase as DNA-dependent protein kinase. J. Biol. Chem. 279, 41189-41196 (2004).
38. R. H. Wong, I. Chang, C. S. Hudak, S. Hyun, H. Y. Kwan, H. S. Sul, A role of DNA-PK for the metabolic gene regulation in response to insulin. Cell 136, 1056-1072 (2009).
39. E. Callén, M. Jankovic, N. Wong, S. Zha, H. T. Chen, S. Difilippantonio, M. Di Virgilio, G. Heidkamp, F. W. Alt, A. Nussenzweig, M. Nussenzweig, Essential role for DNAPKcs in DNA double-strand break repair and apoptosis in ATM-deficient lymphocytes. Mol. Cell 34, 285-297 (2009).
40. C. Allen, J. Halbrook, J. A. Nickoloff, Interactive competition between homologous recombination and non-homologous end joining. Mol. Cancer Res. 1, 913-920 (2003).
41. K. Meek, V. Dang, S. P. Lees-Miller, DNA-PK: The means to justify the ends? Adv. Immunol. 99, 33-58 (2008).
42. E. Huston, M. J. Lynch, A. Mohamed, D. M. Collins, E. V. Hill, R. MacLeod, E. Krause, G. S. Baillie, M. D. Houslay, EPAC and PKA allow cAMP dual control over DNA-PK nuclear translocation. Proc. Natl. Acad. Sci. U. S. A. 105, 12791-12796 (2008).
43. M. T. Kunkel, Q. Ni, R. Y. Tsien, J. Zhang, A. C. Newton, Spatio-temporal dynamics of protein kinase B/Akt signaling revealed by a genetically encoded fluorescent reporter. J. Biol. Chem. 280, 5581-5587 (2005).
44. K. Sasaki, M. Sato, Y. Umezawa, Fluorescent indicators for Akt/protein kinase B and dynamics of Akt activity visualized in living cells. J. Biol. Chem. 278, 30945-30951 (2003).
45. A. Schenck, L. Goto-Silva, C. Collinet, M. Rhinn, A. Giner, B. Habermann, M. Brand, M. Zerial, The endosomal protein Appl1 mediates Akt substrate specificity and cell survival in vertebrate development. Cell 133, 486-497 (2008).
46. S. M. Miah, T. L. Hughes, K. S. Campbell, KIR2DL4 differentially signals downstream functions in human NK cells through distinct structural modules. J. Immunol. 180, 2922-2932 (2008).
47. L. Sadowski, I. Pilecka, M. Miaczynska, Signaling from endosomes: Location makes a difference. Exp. Cell Res. 315, 1601-1609 (2009).
48. R. Zoncu, R. M. Perera, D. M. Balkin, M. Pirruccello, D. Toomre, P. De Camilli, A phosphoinositide switch controls the maturation and signaling properties of APPL endosomes. Cell 136, 1110-1121 (2009).
49. M. J. Van Lierop, F. Wijnands, Y. W. Loke, P. M. Emmer, H. G. Lukassen, D. D. Braat, A. van der Meer, S. Mosselman, I. Joosten, Detection of HLA-G by a specific sandwich ELISA using monoclonal antibodies G233 and 56B. Mol. Hum. Reprod. 8, 776-784 (2002).
50. S. Ramaswamy, N. Nakamura, F. Vazquez, D. B. Batt, S. Perera, T. M. Roberts, W. R. Sellers, Regulation of G1 progression by the PTEN tumor suppressor protein is linked to inhibition of the phosphatidylinositol 3-kinase/Akt pathway. Proc. Natl. Acad. Sci. U. S. A. 96, 2110-2115 (1999).
51. L. J. Kim, A. G. Seto, T. N. Nguyen, J. A. Goodrich, Human TAFII130 is a coactivator for NFATp. Mol. Cell. Biol. 21, 3503-3513 (2001).
52. Acknowledgments: We thank W. Lane (Harvard Microchemistry) for mass spectrometry analysis, and H. Young, U. Siebenlist, J. Bonifacino, Y. Bryceson, B. P. Chen, and D. J. Chen for plasmids. Funding: This work was supported by the Intramural Research Program of the NIH, National Institute of Allergy and Infectious Diseases. Author contributions: S. R. and E. O. L. designed the experiments. S. R. and M. M. performed experiments and interpreted results. I. J. prepared and characterized a recombinant protein. S. R. and E. O. L. analyzed data and wrote the paper. Competing interests: S. R. and E. O. L. have U. S. Patent 7, 435, 801: "Antibodies and other ligands directed against KIR2DL4 receptor for production of interferon gamma."