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Original Research

IFNα signaling through PKC-θ is essential for antitumor NK cell function

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Article: e948705 | Received 04 Sep 2014, Accepted 06 Jun 2014, Published online: 29 Oct 2014

References

  • Baier G, Telford D, Giampa KM, Coggeshall KM, Baier-Bitterlich G, Isakov N, Altman A. Molecular cloning and characterization of PKC-q, a human novel member of the protein kinase C (PKC) gene family expressed predominantly in hematopoietic cells. J Biol Chem 1993; 268:4997-5004; PMID:8444877
  • Altman A, Kaminski S, Busuttil V, Droin N, Hu J, Tadevosyan Y, Hipskind RA, Villalba M. Positive feedback regulation of PLCg1/Ca2+ signaling by PKCq in restimulated T cells via a tec kinase-dependent pathway. Eur J Immunol 2004; 34:2001-11; PMID:15214048; http://dx.doi.org/10.1002/eji.200324625
  • Baier-Bitterlich G, Uberall F, Bauer B, Fresser F, Wachter H, Grunicke H, Utermann G, Altman A, Baier G. Protein kinase C-q isoenzyme selective stimulation of the transcription factor complex AP-1 in T lymphocytes. Mol Cell Biol 1996; 16:1842-50; PMID:8657160
  • Coudronniere N, Villalba M, Englund N, Altman A. NF-kB activation induced by TCR/CD28 costimulation is mediated by PKC-q. Proc Natl Acad Sci USA 2000; 97:3394-9; PMID:10716728
  • Pfeifhofer C, Kofler K, Gruber T, Tabrizi NG, Lutz C, Maly K, Leitges M, Baier G. Protien kinase C q affects Ca2+ mobilization and NFAT cell activation in primary mouse T cells. J Exp Med 2003; 197:1525-35; PMID:12782715; http://dx.doi.org/10.1084/jem.20020234
  • Sun Z, Arendt CW, Ellmeier W, Schaeffer EM, Sunshine MJ, Gandhi L, Annes J, Petrzilka D, Kupfer A, Schwartzberg PL, et al. PKC-q is required for TCR-induced NF-kB activation in mature but not in immature T lymphocytes. Nature 2000; 404:402-7; PMID:10746729; http://dx.doi.org/10.1038/35006090
  • Isakov N, Altman A. Protein kinase C q in T cell activation. Annu Rev Immunol 2002; 20:761-94; PMID:11861617; http://dx.doi.org/10.1146/annurev.immunol.20.100301.064807
  • Dunn GP, Bruce AT, Ikeda H, Old LJ, Schreiber RD. Cancer immunoediting : from immunosurveillance to tumor escape. Nature Immunol 2002; 3:991-8; http://dx.doi.org/10.1038/ni1102-991
  • Dunn GP, Koebel CM, Schreiber RD. Interferons, immunity and cancer immunoediting. Nature Rev Immunol 2006; 6:836-48; http://dx.doi.org/10.1038/nri1961
  • Koebel CM, Vermi W, Swann JB, Zerafa N, Rodig SJ, Old LJ, Smyth MJ, Schreiber RD. Adaptive immunity maintains occult cancer in an equilibrium state. Nature 2007; 450:903-7; PMID:18026089; http://dx.doi.org/10.1038/nature06309
  • Villalba M, López-Royuela N, Krzywinska E, Rathore M, Hipskind R, Haouas H, Allende-Vega N. Chemical metabolic inhibitors for the treatment of blood-borne cancers. Anti-Cancer Ag Med Chem 2014; 14:223-32;
  • Villalba M, Rathore MG, López-Royuela N, Krzywinska E, Garaude J, Allende-Vega N. From tumor cell metabolism to tumor immune escape. Int J Biochem Cell Biol 2013; 45:106-13; PMID:22568930; http://dx.doi.org/10.1016/j.biocel.2012.04.024
  • Garaude J, Kaminski S, Charni S, Aguiló JI, Jacquet C, Plays M, Rodriguez F, Hernández J, Hipskind RA, Anel A, et al. Impaired anti-leukemic immune response in PKCq-deficient mice. Mol Immunol 2008; 45:3463-9; PMID:18462800; http://dx.doi.org/10.1016/j.molimm.2008.03.016
  • Ljunggren HG, Karre K. Host resistance directed selectively against H-2-deficient lymphoma variants. Analysis of the mechanism. J Exp Med 1985; 162:1745-95; PMID:3877776; http://dx.doi.org/10.1084/jem.162.6.1745
  • Terme M, Ullrich E, Delahaye NF, Chaput N, Zitvogel L. Natural killer cell–directed therapies: moving from unexpected results to successful strategies. Nature Immunol 2008; 9:486-94; http://dx.doi.org/10.1038/ni1580
  • Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S. Functions of natural killer cells. Nature Immunol 2008; 9:503-10; http://dx.doi.org/10.1038/ni1582
  • Pardo J, Balkow S, Anel A, Simon MM. Granzymes are critically involved in NK-mediated control of RMA-S tumor growth in vivo. Eur J Immunol 2002; 32:2881-6; PMID:12355441; http://dx.doi.org/10.1002/1521-4141(2002010)32:10<2881::AID-IMMU2881>3.0.CO;2-K
  • Van den Broek MF, Kägi D, Zinkernagel RM, Hengartner H. Perforin dependence of natural killer cell-mediated tumor control in vivo. Eur J Immunol 1995; 25:3514-6; PMID:8566046; http://dx.doi.org/10.1002/eji.1830251246
  • Screpanti V, Wallin RPA, Ljunggren HG, Grandien A. A central role for death receptor-mediated apoptosis in the rejection of tumors by NK cells. J Immunol 2001; 167:2068-73; PMID:11489989; http://dx.doi.org/10.4049/jimmunol.167.4.2068
  • Villalba M, Kasibhatla S, Genestier L, Mahboubi A, Green DR, Altman A. Protein kinase C-q cooperates with calcineurin to induce Fas ligand expression during activation-induced T cell death. J Immunol 1999; 163:5813-9; PMID:10570264
  • Pardo J, Buferne M, Martínez-Lorenzo MJ, Naval J, Schmitt-Verhulst AM, Boyer C, Anel A. Differential implication of PKC isoforms in TCR/CD3-induced Fas ligand expression and in CTL degranulation. Int Immunol 2003; 15:1441-50; PMID:14645153; http://dx.doi.org/10.1093/intimm/dxg141
  • Garrido F, Algarra I, García-Lora AM. The escape of cancer from T lymphocytes: immunoselection of MHC class I loss variants harboring structural-irreversible “hard” lesions. Cancer Immunol Immunother 2010; 59:1601-6; PMID:20625726; http://dx.doi.org/10.1007/s00262-010-0893-2
  • Aguiló JI, Garaude J, Pardo J, Villalba M, Anel A. Protein kinase C-q is required for NK cell activation and in vivo control of tumor progression. J Immunol 2009; 182:1972-81; http://dx.doi.org/10.4049/jimmunol.0801820
  • Anel A, Aguiló JI, Catalán E, Garaude J, Rathore MG, Pardo J, Villalba M. Protein kinase C-q (PKC-q) in natural killer cell function and anti-tumor immunity. Front Immunol 2012; 3:187; PMID:22783260; http://dx.doi.org/10.3389/fimmu.2012.00187
  • Akazawa T, Ebihara T, Okuno M, Okuda Y, Shingai M, Tsujimura K, Takahashi T, Ikawa M, Okabe M, Inoue N, et al. Antitumor NK activation induced by the Toll-like receptor 3-TICAM-1 (TRIF) pathway in myeloid dendritic cells. Proc Natl Acad Sci USA 2007; 104:252-7; PMID:17190817; http://dx.doi.org/10.1073/pnas.0605978104
  • Page KM, Chaudhary D, Goldman SJ, Kasaian MT. Natural killer cells from protein kinase C q–/– mice stimulated with interleukin-12 are deficient in production of interferon-g. J Leukoc Biol 2008; 83:1267-76; PMID:18263766; http://dx.doi.org/10.1189/jlb.1107745
  • Carson WE, Giri JG, Lindemann MJ, Linett ML, Ahdieh M, Paxton R, Anderson D, Eisenmann J, Grabstein K, Caligiuri MA. Interleukin (IL) 15 is a novel cytokine that activates human natural killer cells via components of the IL-2 receptor. J Exp Med 1994; 180:1395-403; PMID:7523571; http://dx.doi.org/10.1084/jem.180.4.1395
  • Cooper MA, Fehniger TA, VanDeusen JB, Waite RE, Liu Y, Aguila HL, Caligiuri MA. In vivo evidence for a dependence on interleukin 15 for survival of natural killer cells. Blood 2002; 100:3633-8; PMID:12393617; http://dx.doi.org/10.1182/blood-2001-12-0293
  • Liu RB, Engels B, Arina A, Schreiber K, Hyjek E, Schietinger A, Binder DC, Butz E, Krausz T, Rowley DA, et al. Densely granulated murine NK cells eradicate large solid tumors. Cancer Res 2012; 72:1964-74; PMID:22374983; http://dx.doi.org/10.1158/0008-5472.CAN-11-3208
  • Villalba M, Bi K, Hu J, Altman Y, Bushway P, Reits E, Neefjes J, Baier G, Abraham RT, Altman A. Translocation of PKCq in T cells is mediated by a nonconventional, PI3-K- and Vav-dependent pathway, but does not absolutely require phospholipase C. J Cell Biol 2002; 157:253-63; PMID:11956228; http://dx.doi.org/10.1083/jcb.200201097
  • Ben Ahmed M, Belhadj Hmida N, Moes N, Buyse S, Abledadhim M, Louzir H, Cerf-Bensussan N. IL-15 renders conventional lymphocytes resistant to suppressive functions of regulatory T cells through activation of the phosphatidylinositol 3-kinase pathway. J Immunol 2009; 182:6763-70; PMID:19454671; http://dx.doi.org/10.4049/jimmunol.0801792
  • Brennan P, Babage JW, Burgering BMT, Gromer B, Reif K, D.A. C. Phosphatidylinositol 3-kinase couples the interleukin-2 receptor to the cell cycle regulator E2F. Immunity 1997; 7:679-89; PMID:9390691; http://dx.doi.org/10.1016/S1074-7613(00)80388-X
  • Truitt KE, Mills GB, Turck CW, Imboden JB. SH2-dependent association of phosphatidylinositol 3'-kinase 85-kDa regulatory subunit with the interleukin-2 receptor b chain. J Biol Chem 1994; 269:5937-43; PMID:7509794
  • Uddin S, Fish E, Sher D, Gardziola C, White M, Platanias L. Activation of the phosphatidylinositol 3-kinase serine kinase by IFN-a. J Immunol 1997; 158:2390-7; PMID:9036989
  • Premecz G, Markovits A, Bagi G, Farkas T, Földes I. Phospholipase C and phospholipase A2 are involved in the antiviral activity of human interferon-a. FEBS Lett 1989; 249:257-60; PMID:2544450; http://dx.doi.org/10.1016/0014-5793(89)80635-0
  • Srivastava KK, Batra S, Sassano A, Li Y, Majchrzak B, Kiyokawa H, Altman A, Fish EN, Platanias LC. Engagement of protein kinase C-q in interferon signaling in T-cells. J Biol Chem 2004; 279:29911-20; PMID:15150272; http://dx.doi.org/10.1074/jbc.M401997200
  • Wang J, Campbell IL. Innate STAT1-dependent genomic response of neurons to the antiviral cytokine alpha interferon. J Virol 2005; 79:8295-302; PMID:15956575; http://dx.doi.org/10.1128/JVI.79.13.8295-8302.2005
  • Fu YY. A transcription factor with SH2 and SH3 domains is directly activated by an interferon alpha-induced cytoplasmic protein tyrosine kinase(s). Cell 1992; 70:323-35.
  • Hardy PO, Diallo TO, Matte C, Descoteaux A. Roles of phosphatidylinositol 3-kinase and p38 mitogen-activated protein kinase in the regulation of protein kinase C-a activation in interferon-g-stimulated macrophages. Immunology 2009; 128:e652-e60; PMID:19740326; http://dx.doi.org/10.1111/j.1365-2567.2009.03055.x
  • Deb D, Sassano A, Lekmine F, Majchrzak B, Verma A, Kambhampati S, Uddin S, Rahman A, Fish E, Platanias L. Activation of protein kinase Cd by IFN-g. J Immunol 2003; 171:267-73; PMID:12817007; http://dx.doi.org/10.4049/jimmunol.171.1.267
  • Swann JB, Hayakawa Y, Zerafa N, Sheelman KCF, Scott B, Schreiber RD, Hertzog P, Smyth MJ. Type I IFN contributes to NK cell homeostasis, activation, and antitumor function. J Immunol 2007; 178:7540-9; PMID:17548588; http://dx.doi.org/10.4049/jimmunol.178.12.7540
  • Merino E, Abeyweera TP, Firth MA, Zawislak CL, Basu R, Liu X, Sun JC, Huse M. Protein kinase C-q clustering at immunological synapses amplifies effector responses in NK cells. J Immunol 2012; 189:4859-69; PMID:23077238; http://dx.doi.org/10.4049/jimmunol.1200825
  • Tassi I, Cella M, Presti R, Colucci A, Gilfillan S, Littman DR, Colonna M. NK cell activating receptors require PKCq for sustained signaling, transcriptional activation and IFN-g secretion. Blood 2008; 112:4109-16; PMID:18784374; http://dx.doi.org/10.1182/blood-2008-02-139527
  • Grybko MJ, Pores-Fernando AT, Wurth GA, Zweifach A. Protein kinase C activity is required for cytotoxic T cell lytic granule exocytosis, but the q isoform does not play a preferential role. J Leukoc Biol 2007; 81:509-19; PMID:17077164; http://dx.doi.org/10.1189/jlb.0206109
  • Puente LG, He JS, Ostergaard HL. A novel PKC regulates ERK activation and degranulation of cytotoxic T lymphocytes: Plasticity in PKC regulation of ERK. Eur J Immunol 2006; 36:1009-18; PMID:16552708; http://dx.doi.org/10.1002/eji.200535277
  • Pardo J, Aguiló J, Anel A, Martin P, Joeckel L, Borner C, Wallich R, Müllbacher A, Froelich C, Simon M. The biology of cytotoxic cell granule exocytosis pathway: granzymes have evolved to induce cell death and inflammation. Microbes & Infection 2009; 11:452-9; PMID:19249384; http://dx.doi.org/10.1016/j.micinf.2009.02.004
  • Fehniger TA, Cai SF, Cao X, Bredemeyer AJ, Presti RM, French AR, Ley TJ. Acquisition of murine NK cell cytotoxicity requires the translation of a pre-existing pool of granzyme B and perforin mRNAs. Immunity 2007; 26:798-811; PMID:17540585; http://dx.doi.org/10.1016/j.immuni.2007.04.010
  • Lucas M, Schachterle W, Oberle K, Aichele P, Diefenbach A. Dendritic cells prime natural killer cells by trans-presenting interleukin 15. Immunity 2007; 26:503-17; PMID:17398124; http://dx.doi.org/10.1016/j.immuni.2007.03.006
  • Gustafsson K, Ingelsten M, Berggvist L, Nyström J, Andersson B, Karlsson-Parra A. Recruitment and activation of natural killer cells in vitro by a human dendritic cell vaccine. Cancer Res 2008; 68:5965-71; PMID:18632652; http://dx.doi.org/10.1158/0008-5472.CAN-07-6494
  • Robertson M. Role of chemokines in the biology of natural killer cells. J Leukoc Biol 2002; 71:173-83; PMID:11818437
  • Vujanovic L, Ballard W, Thorne SH, Vujanovic NL, Butterfield LH. Adenovirus-engineered human dendritic cells induce natural killer cell chemotaxis via CXCL8/IL-8 and CXCL10/IP-10. OncoImmunol 2012; 1:448-57; http://dx.doi.org/10.4161/onci.19788
  • Sánchez-Martínez D, Krzywinska E, Rathore MG, Saument A, Cornilon A, López-Royuela N, Martínez-Lostao L, Ramírez-Labrada A, Lu Z, Rossi J, et al. All-trans retinoic acid (ATRA) induces miR-23a expression, decreases CTSC expression and granzyme B activity leading to impaired NK cell cytotoxicity. Int J Biochem Cell Biol 2014; 49:42-52; http://dx.doi.org/10.1016/j.biocel.2014.01.003
  • Bancerek J, Poss Z, Steinparzer I, Sedlyarov V, Pfanffenwimmer T, Mikulic I, Dölken L, Strobl B, Müller M, Taatjes D, et al. CDK8 kinase phosphorylates transcription factor STAT1 to selectively regulate the interferon response. Immunity 2013; 38:250-62; PMID:23352233; http://dx.doi.org/10.1016/j.immuni.2012.10.017
  • Putz E, Gotthardt D, Hoemann G, Csiszar A, Wirth S, Berger A, Straka E, Rigler D, Wallner B, Jamieson A, et al. CDK8-mediated STAT1-S727 phosphorylation restrains NK cell cytotoxicity and tumor surveillance. Cell Rep 2013; 4:437-44; PMID:23933255; http://dx.doi.org/10.1016/j.celrep.2013.07.012
  • Kiessling R, Klein E, Wigzell H. ``Natural" killer cells in the mouse. I. Cytotoxic cells with specificity for Moloney leukemia cells. Specificity and distribution according to genotype. Eur J Immunol 1975; 5:112-7; PMID:1234049; http://dx.doi.org/10.1002/eji.1830050208
  • Murali-Krishna K, Altman J, Suresh M, Sourdive D, Zajac A, Miller J, Slansky J, Ahmed R. Counting antigen-specific CD8 T cells: a re-evaluation of bystander activation during viral infection. Immunity 1998; 8:177-87; PMID:9491999; http://dx.doi.org/10.1016/S1074-7613(00)80470-7
  • Pardo J, Wallich R, Ebnet K, Iden S, Zentgraf H, Martin P, Ekiciler A, Prins A, Müllbacher A, Huber M, et al. Granzyme B is expressed in mouse mast cells in vivo and in vitro and causes delayed cell death independent of perforin. Cell Death Differ 2007; 14:1768-79; PMID:17599099; http://dx.doi.org/10.1038/sj.cdd.4402183
  • Charni S, de Bettignies G, Rathore MG, Aguiló JI, van den Elsen PJ, Haouzi D, Hipskind RA, Enriquez JA, Sanchez-Beato M, Pardo J, et al. Oxidative phosphorylation induces de novo expression of the MHC class I in tumor cells through the ERK5 pathway. J Immunol 2010; 185:3498-503; PMID:20729331; http://dx.doi.org/10.4049/jimmunol.1001250

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