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Original Research

Interferon-γ-induced activation of JAK1 and JAK2 suppresses tumor cell susceptibility to NK cells through upregulation of PD-L1 expression

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Article: e1008824 | Received 10 Nov 2014, Accepted 14 Jan 2015, Published online: 22 May 2015

References

  • Caligiuri MA. Human natural killer cells. Blood 2008; 112:461-9; PMID:18650461; http://dx.doi.org/10.1182/blood-2007-09-077438
  • Orr MT, Lanier LL. Natural killer cell education and tolerance. Cell 2010; 142:847-56; PMID:20850008; http://dx.doi.org/10.1016/j.cell.2010.08.031
  • Vivier E, Raulet DH, Moretta A, Caligiuri MA, Zitvogel L, Lanier LL, Yokoyama WM, Ugolini S. Innate or adaptive immunity? The example of natural killer cells. Science 2011; 331:44-9; PMID:21212348; http://dx.doi.org/10.1126/science.1198687
  • Lanier LL. Up on the tightrope: natural killer cell activation and inhibition. Nat Immunol 2008; 9:495-502; PMID:18425106; http://dx.doi.org/10.1038/ni1581
  • Robertson MJ, Ritz J. Biology and clinical relevance of human natural killer cells. Blood 1990; 76:2421-38; PMID:2265240
  • Smyth MJ, Dunn GP, Schreiber RD. Cancer immunosurveillance and immunoediting: the roles of immunity in suppressing tumor development and shaping tumor immunogenicity. AdvImmunol 2006; 90:1-50; PMID:16730260; http://dx.doi.org/10.1016/S0065-2776(06)90001-7
  • Bellucci R, Nguyen HN, Martin A, Heinrichs S, Schinzel AC, Hahn WC, Ritz J. Tyrosine kinase pathways modulate tumor susceptibility to natural killer cells. J Clin Invest 2012; 122:2369-83; PMID:22684105; http://dx.doi.org/10.1172/JCI58457
  • Chen E, Staudt LM, Green AR. Janus kinase deregulation in leukemia and lymphoma. Immunity 2012; 36:529-41; PMID:22520846; http://dx.doi.org/10.1016/j.immuni.2012.03.017
  • Jelinek J, Oki Y, Gharibyan V, Bueso-Ramos C, Prchal JT, Verstovsek S, Beran M, Estey E, Kantarjian HM, Issa JP. JAK2 mutation 1849G>T is rare in acute leukemias but can be found in CMML, Philadelphia chromosome-negative CML, and megakaryocytic leukemia. Blood 2005; 106:3370-3; PMID:16037387; http://dx.doi.org/10.1182/blood-2005-05-1800
  • Lacronique V, Boureux A, Valle VD, Poirel H, Quang CT, Mauchauffe M, Berthou C, Lessard M, Berger R, Ghysdael J et al. A TEL-JAK2 fusion protein with constitutive kinase activity in human leukemia. Science 1997; 278:1309-12; PMID:9360930; http://dx.doi.org/10.1126/science.278.5341.1309
  • Darnell JE, Jr, Kerr IM, Stark GR. Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 1994; 264:1415-21; PMID:8197455; http://dx.doi.org/10.1126/science.8197455
  • Matsuzawa T, Kim BH, Shenoy AR, Kamitani S, Miyake M, Macmicking JD. IFN-gamma Elicits Macrophage Autophagy via the p38 MAPK Signaling Pathway. J Immunol 2012; 189:813-8; PMID:22675202; http://dx.doi.org/10.4049/jimmunol.1102041
  • Navarro A, Anand-Apte B, Tanabe Y, Feldman G, Larner AC. A PI-3 kinase-dependent, Stat1-independent signaling pathway regulates interferon-stimulated monocyte adhesion. J LeukocBiol 2003; 73:540-5; PMID:12660229; http://dx.doi.org/10.1189/jlb.1002508
  • O'Shea JJ, Holland SM, Staudt LM. JAKs and STATs in immunity, immunodeficiency, and cancer. N Engl J Med 2013; 368:161-70; PMID:23301733; http://dx.doi.org/10.1056/NEJMra1202117
  • Farag SS, Caligiuri MA. Human natural killer cell development and biology. Blood Rev 2006; 20:123-37; PMID:16364519; http://dx.doi.org/10.1016/j.blre.2005.10.001
  • Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S. Functions of natural killer cells. Nat Immunol 2008; 9:503-10; PMID:18425107; http://dx.doi.org/10.1038/ni1582
  • Alter G, Malenfant JM, Altfeld M. CD107a as a functional marker for the identification of natural killer cell activity. JImmunolMethods 2004; 294:15-22; PMID:15604012; http://dx.doi.org/10.1016/j.jim.2004.08.008
  • Depraetere H, Depla E, Haelewyn J, De Ley M. An anti-idiotypic antibody with an internal image of human interferon-gamma and human interferon-gamma-like antiviral activity. EurJBiochem 2000; 267:2260-7; PMID:10759849; http://dx.doi.org/10.1046/j.1432-1327.2000.01231.x
  • Lanier LL. NK cell recognition. Annu Rev Immunol 2005; 23:225-74; PMID:15771571; http://dx.doi.org/10.1146/annurev.immunol.23.021704.115526
  • Maio M, Altomonte M, Tatake R, Zeff RA, Ferrone S. Reduction in susceptibility to natural killer cell-mediated lysis of human FO-1 melanoma cells after induction of HLA class I antigen expression by transfection with B2m gene. J Clin Invest 1991; 88:282-9; PMID:1905328; http://dx.doi.org/10.1172/JCI115289
  • Beatty GL, Paterson Y. IFN-gamma can promote tumor evasion of the immune system in vivo by down-regulating cellular levels of an endogenous tumor antigen. J Immunol 2000; 165:5502-8; PMID:11067903; http://dx.doi.org/10.4049/jimmunol.165.10.5502
  • Boraschi D, Censini S, Tagliabue A. Interferon-gamma reduces macrophage-suppressive activity by inhibiting prostaglandin E2 release and inducing interleukin 1 production. J Immunol 1984; 133:764-8; PMID:6330202
  • Naganuma H, Sasaki A, Satoh E, Nagasaka M, Nakano S, Isoe S, Nukui H. Down-regulation of transforming growth factor-beta and interleukin-10 secretion from malignant glioma cells by cytokines and anticancer drugs. JNeurooncol 1998; 39:227-36; PMID:9821108; http://dx.doi.org/10.1023/A:1005902120612
  • Dolen Y, Esendagli G. Myeloid leukemia cells with a B7-2(+) subpopulation provoke Th-cell responses and become immuno-suppressive through the modulation of B7 ligands. Eur J Immunol 2013; 43:747-57; PMID:23175469; http://dx.doi.org/10.1002/eji.201242814
  • Velu V, Titanji K, Zhu B, Husain S, Pladevega A, Lai L, Vanderford TH, Chennareddi L, Silvestri G, Freeman GJ et al. Enhancing SIV-specific immunity in vivo by PD-1 blockade. Nature 2009; 458:206-10; PMID:19078956; http://dx.doi.org/10.1038/nature07662
  • Yao S, Zhu Y, Chen L. Advances in targeting cell surface signalling molecules for immune modulation. NatRev Drug Discov 2013; 12:130-46; PMID:23370250; http://dx.doi.org/10.1038/nrd3877
  • Zitvogel L, Kroemer G. Targeting PD-1/PD-L1 interactions for cancer immunotherapy. Oncoimmunology 2012; 1:1223-5; PMID:23243584; http://dx.doi.org/10.4161/onci.21335
  • Benson DM, Jr, Bakan CE, Mishra A, Hofmeister CC, Efebera Y, Becknell B, Baiocchi RA, Zhang J, Yu J, Smith MK et al. The PD-1/PD-L1 axis modulates the natural killer cell versus multiple myeloma effect: a therapeutic target for CT-011, a novel monoclonal anti-PD-1 antibody. Blood 2010; 116:2286-94; PMID:20460501; http://dx.doi.org/10.1182/blood-2010-02-271874
  • Wiesmayr S, Webber SA, Macedo C, Popescu I, Smith L, Luce J, Metes D. Decreased NKp46 and NKG2D and elevated PD-1 are associated with altered NK-cell function in pediatric transplant patients with PTLD. Eur J Immunol 2012; 42:541-50; PMID:22105417; http://dx.doi.org/10.1002/eji.201141832
  • Coughlin CM, Salhany KE, Gee MS, LaTemple DC, Kotenko S, Ma X, Gri G, Wysocka M, Kim JE, Liu L et al. Tumor cell responses to IFNgamma affect tumorigenicity and response to IL-12 therapy and antiangiogenesis. Immunity 1998; 9:25-34; PMID:9697833; http://dx.doi.org/10.1016/S1074-7613(00)80585-3
  • Dighe AS, Richards E, Old LJ, Schreiber RD. Enhanced in vivo growth and resistance to rejection of tumor cells expressing dominant negative IFN gamma receptors. Immunity 1994; 1:447-56; PMID:7895156; http://dx.doi.org/10.1016/1074-7613(94)90087-6
  • Dunn GP, Sheehan KC, Old LJ, Schreiber RD. IFN unresponsiveness in LNCaP cells due to the lack of JAK1 gene expression. Cancer Res 2005; 65:3447-53; PMID:15833880
  • Fisher PB, Miranda AF, Babiss LE. Measurement of the effect of interferons on cellular differentiation in murine and human melanoma cells. Methods Enzymol 1986; 119:611-8; PMID:3762411; http://dx.doi.org/10.1016/0076-6879(86)19082-3
  • Kortylewski M, Komyod W, Kauffmann ME, Bosserhoff A, Heinrich PC, Behrmann I. Interferon-gamma-mediated growth regulation of melanoma cells: involvement of STAT1-dependent and STAT1-independent signals. JInvestDermatol 2004; 122:414-22; PMID:15009724; http://dx.doi.org/10.1046/j.0022-202X.2004.22237.x
  • Creagan ET, Ahmann DL, Long HJ, Frytak S, Sherwin SA, Chang MN. Phase II study of recombinant interferon-gamma in patients with disseminated malignant melanoma. Cancer TreatReports 1987; 71:843-4; PMID:3113730
  • Meyskens FL, Jr, Kopecky K, Samson M, Hersh E, Macdonald J, Jaffe H, Crowley J, Coltman C. Recombinant human interferon gamma: adverse effects in high-risk stage I and II cutaneous malignant melanoma. J Natl Cancer Inst 1990; 82:1071; PMID:2112201; http://dx.doi.org/10.1093/jnci/82.12.1071-a
  • Lollini PL, Bosco MC, Cavallo F, De Giovanni C, Giovarelli M, Landuzzi L, Musiani P, Modesti A, Nicoletti G, Palmieri G et al. Inhibition of tumor growth and enhancement of metastasis after transfection of the gamma-interferon gene. Int J Cancer 1993; 55:320-9; PMID:8370628; http://dx.doi.org/10.1002/ijc.2910550224
  • Taniguchi K, Petersson M, Hoglund P, Kiessling R, Klein G, Karre K. Interferon gamma induces lung colonization by intravenously inoculated B16 melanoma cells in parallel with enhanced expression of class I major histocompatibility complex antigens. ProcNatlAcadSci US A 1987; 84:3405-9; PMID:3106968; http://dx.doi.org/10.1073/pnas.84.10.3405
  • Bukowski JF, Welsh RM. Inability of interferon to protect virus-infected cells against lysis by natural killer (NK) cells correlates with NK cell-mediated antiviral effects in vivo. J Immunol 1985; 135:3537-41; PMID:2413125
  • Zaidi MR, Merlino G. The two faces of interferon-gamma in cancer. Clin Cancer Res 2011; 17:6118-24; PMID:21705455; http://dx.doi.org/10.1158/1078-0432.CCR-11-0482
  • Dong H, Zhu G, Tamada K, Chen L. B7-H1, a third member of the B7 family, co-stimulates T-cell proliferation and interleukin-10 secretion. Nat Med 1999; 5:1365-9; PMID:10581077; http://dx.doi.org/10.1038/70932
  • Freeman GJ, Long AJ, Iwai Y, Bourque K, Chernova T, Nishimura H, Fitz LJ, Malenkovich N, Okazaki T, Byrne MC et al. Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. J Exp Med 2000; 192:1027-34; PMID:11015443; http://dx.doi.org/10.1084/jem.192.7.1027
  • Kaplan DH, Shankaran V, Dighe AS, Stockert E, Aguet M, Old LJ, Schreiber RD. Demonstration of an interferon gamma-dependent tumor surveillance system in immunocompetent mice. ProcNatlAcadSci U S A 1998; 95:7556-61; PMID:9636188; http://dx.doi.org/10.1073/pnas.95.13.7556
  • Pena J, Alonso C, Solana R, Serrano R, Carracedo J, Ramirez R. Natural killer susceptibility is independent of HLA class I antigen expression on cell lines obtained from human solid tumors. Eur J Immunol 1990; 20:2445-8; PMID:1701392; http://dx.doi.org/10.1002/eji.1830201113
  • Brown JA, Dorfman DM, Ma FR, Sullivan EL, Munoz O, Wood CR, Greenfield EA, Freeman GJ. Blockade of programmed death-1 ligands on dendritic cells enhances T cell activation and cytokine production. J Immunol 2003; 170:1257-66; PMID:12538684; http://dx.doi.org/10.4049/jimmunol.170.3.1257
  • Chen J, Feng Y, Lu L, Wang H, Dai L, Li Y, Zhang P. Interferon-gamma-induced PD-L1 surface expression on human oral squamous carcinoma via PKD2 signal pathway. Immunobiology 2012; 217:385-93; PMID:22204817; http://dx.doi.org/10.1016/j.imbio.2011.10.016
  • Brahmer JR, Tykodi SS, Chow LQ, Hwu WJ, Topalian SL, Hwu P, Drake CG, Camacho LH, Kauh J, Odunsi K et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 2012; 366:2455-65; PMID:22658128; http://dx.doi.org/10.1056/NEJMoa1200694
  • Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, Powderly JD, Carvajal RD, Sosman JA, Atkins MB et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012; 366:2443-54; PMID:22658127; http://dx.doi.org/10.1056/NEJMoa1200690
  • Gong JH, Maki G, Klingemann HG. Characterization of a human cell line (NK-92) with phenotypical and functional characteristics of activated natural killer cells. Leukemia 1994; 8:652-8; PMID:8152260
  • Robertson MJ, Cochran KJ, Cameron C, Le JM, Tantravahi R, Ritz J. Characterization of a cell line, NKL, derived from an aggressive human natural killer cell leukemia. ExpHematol 1996; 24:406-15; PMID:8599969
  • Fuller MJ, Callendret B, Zhu B, Freeman GJ, Hasselschwert DL, Satterfield W, Sharpe AH, Dustin LB, Rice CM, Grakoui A et al. Immunotherapy of chronic hepatitis C virus infection with antibodies against programmed cell death-1 (PD-1). ProcNatlAcadSci U S A 2013; 110:15001-6; PMID:23980172; http://dx.doi.org/10.1073/pnas.1312772110