7,909
Views
91
CrossRef citations to date
0
Altmetric
Original Research

PD-L1 blockade enhances anti-tumor efficacy of NK cells

ORCID Icon, , & ORCID Icon
Article: e1509819 | Received 22 Mar 2018, Accepted 04 Aug 2018, Published online: 27 Aug 2018

References

  • Jiang T, Zhou C. The past, present and future of immunotherapy against tumor. Transl Lung Cancer Res. 2015;4(3):253–264. doi:10.3978/j.issn.2218-6751.2015.01.06.
  • Herbst RS, Soria JC, Kowanetz M, Fine GD, Hamid O, Gordon MS, Sosman JA, McDermott DF, Powderly JD, Gettinger SN, et al. Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients. Nature. 2014;515(7528):563–567. doi:10.1038/nature14011.
  • Tumeh PC, Harview CL, Yearley JH, Shintaku IP, Taylor EJ, Robert L, Chmielowski B, Spasic M, Henry G, Ciobanu V, et al. PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature. 2014;515(7528):568–571. doi:10.1038/nature13954.
  • Guirgis HM. The impact of PD-L1 on survival and value of the immune check point inhibitors in non-small-cell lung cancer; proposal, policies and perspective. J Immunother Cancer. 2018;6(1):15. doi:10.1186/s40425-018-0320-3.
  • Garcia-Diaz A, Shin DS, Moreno BH, Saco J, Escuin-Ordinas H, Rodriguez GA, Zaretsky JM, Sun L, Hugo W, Wang X, et al. Interferon receptor signaling pathways regulating PD-L1 and PD-L2 expression. Cell Rep. 2017;19(6):1189–1201. doi:10.1016/j.celrep.2017.04.031.
  • Abiko K, Matsumura N, Hamanishi J, Horikawa N, Murakami R, Yamaguchi K, Yoshioka Y, Baba T, Konishi I, Mandai M. IFN-gamma from lymphocytes induces PD-L1 expression and promotes progression of ovarian cancer. Br J Cancer. 2015;112(9):1501–1509. doi:10.1038/bjc.2015.101.
  • Allen F, Bobanga ID, Rauhe P, Barkauskas D, Teich N, Tong C, Myers J, Huang AY. CCL3 augments tumor rejection and enhances CD8(+) T cell infiltration through NK and CD103(+) dendritic cell recruitment via IFNgamma. Oncoimmunology. 2018;7(3):e1393598. doi:10.1080/2162402X.2017.1393598.
  • Pandey V, Oyer JL, Igarashi RY, Gitto SB, Copik AJ, Altomare DA. Anti-ovarian tumor response of donor peripheral blood mononuclear cells is due to infiltrating cytotoxic NK cells. Oncotarget. 2016. doi:10.18632/oncotarget.6939.
  • Morvan MG, Lanier LL. NK cells and cancer: you can teach innate cells new tricks. Nat Rev Cancer. 2016;16(1):7–19. doi:10.1038/nrc.2015.5.
  • Van Elssen CH, Oth T, Germeraad WT, Bos GM, Vanderlocht J. Natural killer cells: the secret weapon in dendritic cell vaccination strategies. Clin Cancer Res. 2014;20(5):1095–1103. doi:10.1158/1078-0432.CCR-13-2302.
  • Deauvieau F, Ollion V, Doffin AC, Achard C, Fonteneau JF, Verronese E, Durand I, Ghittoni R, Marvel J, Dezutter-Dambuyant C, et al. Human natural killer cells promote cross-presentation of tumor cell-derived antigens by dendritic cells. Int J Cancer. 2015;136(5):1085–1094. doi:10.1002/ijc.29087.
  • Nouri-Shirazi M, Banchereau J, Bell D, Burkeholder S, Kraus ET, Davoust J, Palucka KA. Dendritic cells capture killed tumor cells and present their antigens to elicit tumor-specific immune responses. J Immunol. 2000;165(7):3797–3803. doi:10.4049/jimmunol.165.7.3797.
  • Parkhurst MR, Riley JP, Dudley ME, Rosenberg SA. Adoptive transfer of autologous natural killer cells leads to high levels of circulating natural killer cells but does not mediate tumor regression. Clin Cancer Res. 2011;17(19):6287–6297. doi:10.1158/1078-0432.CCR-11-1347.
  • Miller JS, Soignier Y, Panoskaltsis-Mortari A, McNearney SA, Yun GH, Fautsch SK, McKenna D, Le C, Defor TE, Burns LJ, et al. Successful adoptive transfer and in vivo expansion of human haploidentical NK cells in patients with cancer. Blood. 2005;105(8):3051–3057. doi:10.1182/blood-2004-07-2974.
  • Ames E, Canter RJ, Grossenbacher SK, Mac S, Chen M, Smith RC, Hagino T, Perez-Cunningham J, Sckisel GD, Urayama S, et al. NK cells preferentially target tumor cells with a cancer stem cell phenotype. J Immunol. 2015;195(8):4010–4019. doi:10.4049/jimmunol.1500447.
  • Veluchamy JP, Lopez-Lastra S, Spanholtz J, Bohme F, Kok N, Heideman DA, Verheul HM, Di Santo JP, De Gruijl TD, van der Vliet HJ. In Vivo efficacy of umbilical cord blood stem cell-derived NK cells in the treatment of metastatic colorectal cancer. Front Immunol. 2017;8:87. doi:10.3389/fimmu.2017.00087.
  • Romee R, Rosario M, Berrien-Elliott MM, Wagner JA, Jewell BA, Schappe T, Leong JW, Abdel-Latif S, Schneider SE, Willey S, et al. Cytokine-induced memory-like natural killer cells exhibit enhanced responses against myeloid leukemia. Sci Transl Med. 2016;8(357):357ra123. doi:10.1126/scitranslmed.aaf0746.
  • Ciurea SO, Schafer JR, Bassett R, Denman CJ, Cao K, Willis D, Rondon G, Chen J, Soebbing D, Kaur I, et al. Phase 1 clinical trial using mbIL21 ex vivo-expanded donor-derived NK cells after haploidentical transplantation. Blood. 2017;130(16):1857–1868. doi:10.1182/blood-2017-05-785659.
  • Lee DA, Denman CJ, Rondon G, Woodworth G, Chen J, Fisher T, Kaur I, Fernandez-Vina M, Cao K, Ciurea S, et al. Haploidentical natural killer cells infused before allogeneic stem cell transplantation for myeloid malignancies: A phase i trial. Biol Blood Marrow Transplantation. 2016;22(7):1290–1298. doi:10.1016/j.bbmt.2016.04.009.
  • Parisi S, Lecciso M, Ocadlikova D, Salvestrini V, Ciciarello M, Forte D, Corradi G, Cavo M, Curti A, More T. The better: “Do the Right Thing” for natural killer immunotherapy in acute myeloid leukemia. Front Immunol. 2017;8:1330. doi:10.3389/fimmu.2017.01330.
  • Fujisaki H, Kakuda H, Shimasaki N, Imai C, Ma J, Lockey T, Eldridge P, Leung WH, Campana D. Expansion of highly cytotoxic human natural killer cells for cancer cell therapy. Cancer Res. 2009;69(9):4010–4017. doi:10.1158/0008-5472.CAN-08-3712.
  • Denman CJ, Senyukov VV, Somanchi SS, Phatarpekar PV, Kopp LM, Johnson JL, Singh H, Hurton L, Maiti SN, Huls MH, et al. Membrane-bound IL-21 promotes sustained ex vivo proliferation of human natural killer cells. PLoS One. 2012;7(1):e30264. doi:10.1371/journal.pone.0030264.
  • Berg M, Lundqvist A, McCoy P Jr., Samsel L, Fan Y, Tawab A, Childs R. Clinical-grade ex vivo-expanded human natural killer cells up-regulate activating receptors and death receptor ligands and have enhanced cytolytic activity against tumor cells. Cytotherapy. 2009;11(3):341–355. doi:10.1080/14653240902807034.
  • Oyer JL, Igarashi RY, Kulikowski AR, Colosimo DA, Solh MM, Zakari A, Khaled YA, Altomare DA, Copik AJ. Generation of highly cytotoxic natural killer cells for treatment of acute myelogenous leukemia using a feeder-free, particle-based approach. Biol Blood Marrow Transplant. 2015;21(4):632–639. doi:10.1016/j.bbmt.2014.12.037.
  • Oyer JL, Pandey V, Igarashi RY, Somanchi SS, Zakari A, Solh M, Lee DA, Altomare DA, Copik AJ. NK cells stimulated with PM21 particles expand and biodistribute in vivo: clinical implications for cancer treatment. Cytotherapy. 2016;18(5):653–663. doi:10.1016/j.jcyt.2016.02.006.
  • Spranger S, Spaapen RM, Zha Y, Williams J, Meng Y, Ha TT, Gajewski TF. Up-regulation of PD-L1, IDO, and T(regs) in the melanoma tumor microenvironment is driven by CD8(+) T cells. Sci Transl Med. 2013;5(200):200ra116. doi:10.1126/scitranslmed.3006504.
  • Chen L, Han X. Anti-PD-1/PD-L1 therapy of human cancer: past, present, and future. J Clin Invest. 2015;125(9):3384–3391. doi:10.1172/JCI80011.
  • 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(13):2286–2294. doi:10.1182/blood-2010-02-271874.
  • Francisco LM, Salinas VH, Brown KE, Vanguri VK, Freeman GJ, Kuchroo VK, Sharpe AH. PD-L1 regulates the development, maintenance, and function of induced regulatory T cells. J Exp Med. 2009;206(13):3015–3029. doi:10.1084/jem.20090847.
  • Keskin DB, Allan DS, Rybalov B, Andzelm MM, Stern JN, Kopcow HD, Koopman LA, Strominger JL. TGFbeta promotes conversion of CD16+ peripheral blood NK cells into CD16- NK cells with similarities to decidual NK cells. Proc Natl Acad Sci U S A. 2007;104(9):3378–3383. doi:10.1073/pnas.0611098104.
  • Ghiringhelli F, Menard C, Terme M, Flament C, Taieb J, Chaput N, Puig PE, Novault S, Escudier B, Vivier E, et al. CD4+CD25+ regulatory T cells inhibit natural killer cell functions in a transforming growth factor-beta-dependent manner. J Exp Med. 2005;202(8):1075–1085. doi:10.1084/jem.20051511.
  • Sitrin J, Ring A, Garcia KC, Benoist C, Mathis D. Regulatory T cells control NK cells in an insulitic lesion by depriving them of IL-2. J Exp Med. 2013;210(6):1153–1165. doi:10.1084/jem.20122248.
  • Pesce S, Tabellini G, Cantoni C, Patrizi O, Coltrini D, Rampinelli F, Matta J, Vivier E, Moretta A, Parolini S, et al. B7-H6-mediated downregulation of NKp30 in NK cells contributes to ovarian carcinoma immune escape. Oncoimmunology. 2015;4(4):e1001224. doi:10.1080/2162402X.2015.1008371.
  • Nham T, Poznanski SM, Fan IY, Shenouda MM, Chew MV, Lee AJ, Vahedi F, Karimi Y, Butcher M, Lee DA, et al. Ex vivo-expanded NK cells from blood and ascites of ovarian cancer patients are cytotoxic against autologous primary ovarian cancer cells. Cancer Immunol Immunother. 2018;67:575–587. doi:10.1007/s00262-017-2112-x.
  • Nielsen CM, White MJ, Goodier MR, Riley EM. Functional significance of CD57 expression on human NK cells and relevance to disease. Front Immunol. 2013;4:422. doi:10.3389/fimmu.2013.00422.
  • Geller MA, Knorr DA, Hermanson DA, Pribyl L, Bendzick L, McCullar V, Miller JS, Kaufman DS. Intraperitoneal delivery of human natural killer cells for treatment of ovarian cancer in a mouse xenograft model. Cytotherapy. 2013;15(10):1297–1306. doi:10.1016/j.jcyt.2013.05.022.
  • Gasteiger G, Hemmers S, Bos PD, Sun JC, Rudensky AY. IL-2-dependent adaptive control of NK cell homeostasis. J Exp Med. 2013;210(6):1179–1187. doi:10.1084/jem.20122571.
  • Watanabe M, Kono K, Kawaguchi Y, Mizukami Y, Mimura K, Maruyama T, Izawa S, Fujii H. NK cell dysfunction with down-regulated CD16 and up-regulated CD56 molecules in patients with esophageal squamous cell carcinoma. Dis Esophagus. 2010;23(8):675–681. doi:10.1111/j.1442-2050.2010.01073.x.
  • Carrega P, Morandi B, Costa R, Frumento G, Forte G, Altavilla G, Ratto GB, Mingari MC, Moretta L, Ferlazzo G. Natural killer cells infiltrating human nonsmall-cell lung cancer are enriched in CD56 bright CD16(-) cells and display an impaired capability to kill tumor cells. Cancer. 2008;112(4):863–875. doi:10.1002/cncr.23239.
  • Villegas FR, Coca S, Villarrubia VG, Jimenez R, Chillon MJ, Jareno J, Zuil M, Callol L. Prognostic significance of tumor infiltrating natural killer cells subset CD57 in patients with squamous cell lung cancer. Lung Cancer. 2002;35(1):23–28.
  • Lopez-Verges S, Milush JM, Pandey S, York VA, Arakawa-Hoyt J, Pircher H, Norris PJ, Nixon DF, Lanier LL. CD57 defines a functionally distinct population of mature NK cells in the human CD56dimCD16+ NK-cell subset. Blood. 2010;116(19):3865–3874. doi:10.1182/blood-2010-04-282301.
  • Rubnitz JE, Inaba H, Ribeiro RC, Pounds S, Rooney B, Bell T, Pui CH, Leung W. NKAML: a pilot study to determine the safety and feasibility of haploidentical natural killer cell transplantation in childhood acute myeloid leukemia. J Clin Oncol. 2010;28(6):955–959. doi:10.1200/JCO.2009.24.4590.
  • Bachanova V, Cooley S, Defor TE, Verneris MR, Zhang B, McKenna DH, Curtsinger J, Panoskaltsis-Mortari A, Lewis D, Hippen K, et al. Clearance of acute myeloid leukemia by haploidentical natural killer cells is improved using IL-2 diphtheria toxin fusion protein. Blood. 2014;123(25):3855–3863. doi:10.1182/blood-2013-10-532531.
  • Geller MA, Cooley S, Judson PL, Ghebre R, Carson LF, Argenta PA, Jonson AL, Panoskaltsis-Mortari A, Curtsinger J, McKenna D, et al. A phase II study of allogeneic natural killer cell therapy to treat patients with recurrent ovarian and breast cancer. Cytotherapy. 2011;13(1):98–107. doi:10.3109/14653249.2010.515582.
  • Bachanova V, Burns LJ, McKenna DH, Curtsinger J, Panoskaltsis-Mortari A, Lindgren BR, Cooley S, Weisdorf D, Miller JS. Allogeneic natural killer cells for refractory lymphoma. Cancer Immunol Immunother. 2010;59(11):1739–1744. doi:10.1007/s00262-010-0896-z.
  • Bachanova V, Sarhan D, DeFor TE, Cooley S, Panoskaltsis-Mortari A, Blazar BR, Curtsinger JM, Burns L, Weisdorf DJ, Miller JS. Haploidentical natural killer cells induce remissions in non-Hodgkin lymphoma patients with low levels of immune-suppressor cells. Cancer Immunol Immunother. 2017;67(3):483–494.
  • Mandal R, Senbabaoglu Y, Desrichard A, Havel JJ, Dalin MG, Riaz N, Lee KW, Ganly I, Hakimi AA, Chan TA, et al. The head and neck cancer immune landscape and its immunotherapeutic implications. JCI Insight. 2016;1(17):e89829. doi:10.1172/jci.insight.89829.
  • Jie HB, Schuler PJ, Lee SC, Srivastava RM, Argiris A, Ferrone S, Whiteside TL, Ferris RL. CTLA-4(+) regulatory T cells increased in cetuximab-treated head and neck cancer patients suppress NK cell cytotoxicity and correlate with poor prognosis. Cancer Res. 2015;75(11):2200–2210. doi:10.1158/0008-5472.CAN-14-2788.
  • Boyerinas B, Jochems C, Fantini M, Heery CR, Gulley JL, Tsang KY, Schlom J. Antibody-dependent cellular cytotoxicity activity of a novel anti-PD-L1 antibody avelumab (MSB0010718C) on human tumor cells. Cancer Immunol Res. 2015;3(10):1148–1157. doi:10.1158/2326-6066.CIR-15-0059.
  • Aquino-Lopez A, Senyukov VV, Vlasic Z, Kleinerman ES, Lee DA. Interferon gamma induces changes in natural killer (NK) cell ligand expression and alters NK cell-mediated lysis of pediatric cancer cell lines. Front Immunol. 2017;8:391. doi:10.3389/fimmu.2017.00391.
  • Liu Z, Ravindranathan R, Kalinski P, Guo ZS, Bartlett DL. Rational combination of oncolytic vaccinia virus and PD-L1 blockade works synergistically to enhance therapeutic efficacy. Nat Commun. 2017;8:14754. doi:10.1038/ncomms14754.
  • Anderson AA, Milhem MM, Andtbacka RH, Gorski KS, Baker DM, Hamid O, Kaufman HL Pharmacodynamic gene expression changes from talimogene laherparepvec (T-VEC) plus ipilimumab in a phase Ib study for metastatic melanoma. Poster presented at: 31st SITC Annual Meeting; 2016, Nov 11; National Harbour, MD.