PD-1/PD-L1 Blockade Therapy for Tumors with Downregulated MHC Class I Expression
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články, přehledy
PubMed
28635644
PubMed Central
PMC5486151
DOI
10.3390/ijms18061331
PII: ijms18061331
Knihovny.cz E-zdroje
- Klíčová slova
- MHC class I, PD-1, PD-L1, biomarker, cancer immunotherapy, checkpoint blockade, interferon gamma, tumor escape,
- MeSH
- antigeny CD274 antagonisté a inhibitory imunologie MeSH
- antigeny CD279 antagonisté a inhibitory imunologie MeSH
- down regulace * MeSH
- geny MHC třídy I MeSH
- histokompatibilita - antigeny třídy I genetika MeSH
- imunoterapie metody MeSH
- lidé MeSH
- monoklonální protilátky terapeutické užití MeSH
- nádory genetika imunologie terapie MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
- Názvy látek
- antigeny CD274 MeSH
- antigeny CD279 MeSH
- histokompatibilita - antigeny třídy I MeSH
- monoklonální protilátky MeSH
The therapy of different advanced-stage malignancies with monoclonal antibodies blocking programmed cell death protein 1 (PD-1)/PD-1 ligand 1 (PD-L1) signaling has had an impressive long-lasting effect in a portion of patients, but in most cases, this therapy was not successful, or a secondary resistance developed. To enhance its efficacy in treated patients, predictive biomarkers are searched for and various combination treatments are intensively investigated. As the downregulation of major histocompatibility complex (MHC) class I molecules is one of the most frequent mechanisms of tumor escape from the host's immunity, it should be considered in PD-1/PD-L1 checkpoint inhibition. The potential for the use of a PD-1/PD-L1 blockade in the treatment of tumors with aberrant MHC class I expression is discussed, and some strategies of combination therapy are suggested.
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Ishida Y., Agata Y., Shibahara K., Honjo T. Induced expression of PD-1, a novel member of the immunoglobulin gene superfamily, upon programmed cell death. EMBO J. 1992;11:3887–3895. PubMed PMC
Agata Y., Kawasaki A., Nishimura H., Ishida Y., Tsubata T., Yagita H., Honjo T. Expression of the PD-1 antigen on the surface of stimulated mouse T and B lymphocytes. Int. Immunol. 1996;8:765–772. doi: 10.1093/intimm/8.5.765. PubMed DOI
Chikuma S., Terawaki S., Hayashi T., Nabeshima R., Yoshida T., Shibayama S., Okazaki T., Honjo T. PD-1-mediated suppression of IL-2 production induces CD8+ T cell anergy in vivo. J. Immunol. 2009;182:6682–6689. doi: 10.4049/jimmunol.0900080. PubMed DOI
Ahmadzadeh M., Johnson L.A., Heemskerk B., Wunderlich J.R., Dudley M.E., White D.E., Rosenberg S.A. Tumor antigen–specific CD8 T cells infiltrating the tumor express high levels of PD-1 and are functionally impaired. Blood. 2009;114:1537–1544. doi: 10.1182/blood-2008-12-195792. PubMed DOI PMC
Chemnitz J.M., Parry R.V., Nichols K.E., June C.H., Riley J.L. SHP-1 and SHP-2 associate with immunoreceptor tyrosine-based switch motif of programmed death 1 upon primary human T cell stimulation, but only receptor ligation prevents T cell activation. J. Immunol. 2004;173:945–954. doi: 10.4049/jimmunol.173.2.945. PubMed DOI
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;5:1365–1369. doi: 10.1038/70932. PubMed DOI
Latchman Y., Wood C.R., Chernova T., Chaudhary D., Borde M., Chernova I., Iwai Y., Long A.J., Brown J.A., Nunes R., et al. PD-L2 is a second ligand for PD-1 and inhibits T cell activation. Nat. Immunol. 2001;2:261–268. doi: 10.1038/85330. PubMed DOI
Intlekofer A.M., Thompson C.B. At the bench: Preclinical rationale for CTLA-4 and PD-1 blockade as cancer immunotherapy. J. Leukoc. Biol. 2013;94:25–39. doi: 10.1189/jlb.1212621. PubMed DOI PMC
Dong H., Strome S.E., Salomao D.R., Tamura H., Hirano F., Flies D.B., Roche P.C., Lu J., Zhu G., Tamada K., et al. Tumor-associated B7-H1 promotes T-cell apoptosis: A potential mechanism of immune evasion. Nat. Med. 2002;8:793–800. doi: 10.1038/nm0902-1039c. PubMed DOI
Wang X., Teng F., Kong L., Yu J. PD-L1 expression in human cancers and its association with clinical outcomes. OncoTargets Ther. 2016;9:5023–5039. doi: 10.2147/OTT.S105862. PubMed DOI PMC
Berry S., Taube J.M. Innate vs. adaptive: PD-L1-mediated immune resistance by melanoma. OncoImmunology. 2015;4:e1029704. doi: 10.1080/2162402X.2015.1029704. PubMed DOI PMC
Topalian S.L., Drake C.G., Pardoll D.M. Immune checkpoint blockade: A common denominator approach to cancer therapy. Cancer Cell. 2015;27:450–461. doi: 10.1016/j.ccell.2015.03.001. PubMed DOI PMC
Parsa A.T., Waldron J.S., Panner A., Crane C.A., Parney I.F., Barry J.J., Cachola K.E., Murray J.C., Tihan T., Jensen M.C., et al. Loss of tumor suppressor PTEN function increases B7-H1 expression and immunoresistance in glioma. Nat. Med. 2007;13:84–88. doi: 10.1038/nm1517. PubMed DOI
Lastwika K.J., Wilson W., Li Q.K., Norris J., Xu H., Ghazarian S.R., Kitagawa H., Kawabata S., Taube J.M., Yao S., et al. Control of PD-L1 expression by oncogenic activation of the AKT-mTOR pathway in non-small cell lung cancer. Cancer Res. 2016;76:227–238. doi: 10.1158/0008-5472.CAN-14-3362. PubMed DOI
Marzec M., Zhang Q., Goradia A., Raghunath P.N., Liu X., Paessler M., Wang H.Y., Wysocka M., Cheng M., Ruggeri B.A., et al. Oncogenic kinase NPM/ALK induces through STAT3 expression of immunosuppressive protein CD274 (PD-L1, B7-H1) Proc. Natl. Acad. Sci. USA. 2008;105:20852–20857. doi: 10.1073/pnas.0810958105. PubMed DOI PMC
Akbay E.A., Koyama S., Carretero J., Altabef A., Tchaicha J.H., Christensen C.L., Mikse O.R., Cherniack A.D., Beauchamp E.M., Pugh T.J., et al. Activation of the PD-1 pathway contributes to immune escape in EGFR-driven lung tumors. Cancer Discov. 2013;3:1355–1363. doi: 10.1158/2159-8290.CD-13-0310. PubMed DOI PMC
Dorand R.D., Nthale J., Myers J.T., Barkauskas D.S., Avril S., Chirieleison S.M., Pareek T.K., Abbott D.W., Stearns D.S., Letterio J.J., et al. Cdk5 disruption attenuates tumor PD-L1 expression and promotes antitumor immunity. Science. 2016;353:399–403. doi: 10.1126/science.aae0477. PubMed DOI PMC
Casey S.C., Tong L., Li Y., Do R., Walz S., Fitzgerald K.N., Gouw A.M., Baylot V., Gütgemann I., Eilers M., et al. MYC regulates the antitumor immune response through CD47 and PD-L1. Science. 2016;352:227–231. doi: 10.1126/science.aac9935. PubMed DOI PMC
Green M.R., Monti S., Rodig S.J., Juszczynski P., Currie T., O’Donnell E., Chapuy B., Takeyama K., Neuberg D., Golub T.R., et al. Integrative analysis reveals selective 9p24.1 amplification, increased PD-1 ligand expression, and further induction via JAK2 in nodular sclerosing Hodgkin lymphoma and primary mediastinal large B-cell lymphoma. Blood. 2010;116:3268–3277. doi: 10.1182/blood-2010-05-282780. PubMed DOI PMC
Steidl C., Shah S.P., Woolcock B.W., Rui L., Kawahara M., Farinha P., Johnson N.A., Zhao Y., Telenius A., Neriah S.B., et al. MHC class II transactivator CIITA is a recurrent gene fusion partner in lymphoid cancers. Nature. 2011;471:377–381. doi: 10.1038/nature09754. PubMed DOI PMC
The Cancer Genome Atlas Research Network Comprehensive molecular characterization of gastric adenocarcinoma. Nature. 2014;513:202–209. doi: 10.1038/nature13480. PubMed DOI PMC
The Cancer Genome Atlas Research Network Integrated genomic and molecular characterization of cervical cancer. Nature. 2017;543:378–384. doi: 10.1038/nature21386. PubMed DOI PMC
Bi X., Wang H., Zhang W., Wang J., Liu W., Xia Z., Huang H., Jiang W., Zhang Y., Wang L. PD-L1 is upregulated by EBV-driven LMP1 through NF-κB pathway and correlates with poor prognosis in natural killer/T-cell lymphoma. J. Hematol. Oncol. 2016;9:109. doi: 10.1186/s13045-016-0341-7. PubMed DOI PMC
Kataoka K., Shiraishi Y., Takeda Y., Sakata S., Matsumoto M., Nagano S., Maeda T., Nagata Y., Kitanaka A., Mizuno S., et al. Aberrant PD-L1 expression through 3′-UTR disruption in multiple cancers. Nature. 2016;534:402–406. doi: 10.1038/nature18294. PubMed DOI
Yamazaki T., Akiba H., Iwai H., Matsuda H., Aoki M., Tanno Y., Shin T., Tsuchiya H., Pardoll D.M., Okumura K., et al. Expression of programmed death 1 ligands by murine T cells and APC. J. Immunol. 2002;169:5538–5545. doi: 10.4049/jimmunol.169.10.5538. PubMed DOI
Chikuma S. Basics of PD-1 in self-tolerance, infection, and cancer immunity. Int. J. Clin. Oncol. 2016;21:448–455. doi: 10.1007/s10147-016-0958-0. PubMed DOI
Teng M.W.L., Galon J., Fridman W.-H., Smyth M.J. From mice to humans: Developments in cancer immunoediting. J. Clin. Investig. 2015;125:3338–3346. doi: 10.1172/JCI80004. PubMed DOI PMC
Garrido F., Ruiz-Cabello F., Aptsiauri N. Rejection versus escape: The tumor MHC dilemma. Cancer Immunol. Immunother. 2017;66:259–271. doi: 10.1007/s00262-016-1947-x. PubMed DOI PMC
Leone P., Shin E.-C., Perosa F., Vacca A., Dammacco F., Racanelli V. MHC class I antigen processing and presenting machinery: Organization, function, and defects in tumor cells. J. Natl. Cancer Inst. 2013;105:1172–1187. doi: 10.1093/jnci/djt184. PubMed DOI
Garrido F., Aptsiauri N., Doorduijn E.M., Garcia Lora A.M., van Hall T. The urgent need to recover MHC class I in cancers for effective immunotherapy. Curr. Opin. Immunol. 2016;39:44–51. doi: 10.1016/j.coi.2015.12.007. PubMed DOI PMC
Aust S., Felix S., Auer K., Bachmayr-Heyda A., Kenner L., Dekan S., Meier S.M., Gerner C., Grimm C., Pils D. Absence of PD-L1 on tumor cells is associated with reduced MHC I expression and PD-L1 expression increases in recurrent serous ovarian cancer. Sci. Rep. 2017;7:42929. doi: 10.1038/srep42929. PubMed DOI PMC
Lopez-Nevot M.A., Esteban F., Ferron A., Gutierrez J., Oliva M.R., Romero C., Huelin C., Ruiz-Cabello F., Garrido F. HLA class I gene expression on human primary tumours and autologous metastases: Demonstration of selective losses of HLA antigens on colorectal, gastric and laryngeal carcinomas. Br. J. Cancer. 1989;59:221–226. doi: 10.1038/bjc.1989.45. PubMed DOI PMC
Méndez R., Ruiz-Cabello F., Rodríguez T., Del Campo A., Paschen A., Schadendorf D., Garrido F. Identification of different tumor escape mechanisms in several metastases from a melanoma patient undergoing immunotherapy. Cancer Immunol. Immunother. 2007;56:88–94. doi: 10.1007/s00262-006-0166-2. PubMed DOI PMC
Carretero R., Romero J.M., Ruiz-Cabello F., Maleno I., Rodriguez F., Camacho F.M., Real L.M., Garrido F., Cabrera T. Analysis of HLA class I expression in progressing and regressing metastatic melanoma lesions after immunotherapy. Immunogenetics. 2008;60:439–447. doi: 10.1007/s00251-008-0303-5. PubMed DOI
Hicklin D.J., Marincola F.M., Ferrone S. HLA class I antigen downregulation in human cancers: T-cell immunotherapy revives an old story. Mol. Med. Today. 1999;5:178–186. doi: 10.1016/S1357-4310(99)01451-3. PubMed DOI
Iwai Y., Ishida M., Tanaka Y., Okazaki T., Honjo T., Minato N. Involvement of PD-L1 on tumor cells in the escape from host immune system and tumor immunotherapy by PD-L1 blockade. Proc. Natl. Acad. Sci. USA. 2002;99:12293–12297. doi: 10.1073/pnas.192461099. PubMed DOI PMC
Brahmer J.R., Drake C.G., Wollner I., Powderly J.D., Picus J., Sharfman W.H., Stankevich E., Pons A., Salay T.M., McMiller T.L., et al. Phase I study of single-agent anti-programmed death-1 (MDX-1106) in refractory solid tumors: Safety, clinical activity, pharmacodynamics, and immunologic correlates. J. Clin. Oncol. 2010;28:3167–3175. doi: 10.1200/JCO.2009.26.7609. PubMed DOI PMC
Jiang T., Zhou C. The past, present and future of immunotherapy against tumor. Transl. Lung Cancer Res. 2015;4:253–264. doi: 10.3978/j.issn.2218-6751.2015.01.06. PubMed DOI PMC
Ma W., Gilligan B.M., Yuan J., Li T. Current status and perspectives in translational biomarker research for PD-1/PD-L1 immune checkpoint blockade therapy. J. Hematol. Oncol. 2016;9:47. doi: 10.1186/s13045-016-0277-y. PubMed DOI PMC
Ribas A., Hamid O., Daud A., Hodi F.S., Wolchok J.D., Kefford R., Joshua A.M., Patnaik A., Hwu W.-J., et al. Association of pembrolizumab with tumor response and survival among patients with advanced melanoma. JAMA. 2016;315:1600–1609. doi: 10.1001/jama.2016.4059. PubMed DOI
Larkin J., Chiarion-Sileni V., Gonzalez R., Grob J.J., Cowey C.L., Lao C.D., Schadendorf D., Dummer R., Smylie M., Rutkowski P., et al. Combined nivolumab and ipilimumab or monotherapy in untreated melanoma. N. Engl. J. Med. 2015;373:23–34. doi: 10.1056/NEJMoa1504030. PubMed DOI PMC
Gibney G.T., Weiner L.M., Atkins M.B. Predictive biomarkers for checkpoint inhibitor-based immunotherapy. Lancet Oncol. 2016;17:e542–e551. doi: 10.1016/S1470-2045(16)30406-5. PubMed DOI PMC
Ascierto P.A., Capone M., Urba W.J., Bifulco C.B., Botti G., Lugli A., Marincola F.M., Ciliberto G., Galon J., Fox B.A. The additional facet of immunoscore: Immunoprofiling as a possible predictive tool for cancer treatment. J. Transl. Med. 2013;11:54. doi: 10.1186/1479-5876-11-54. PubMed DOI PMC
Pagès F., Kirilovsky A., Mlecnik B., Asslaber M., Tosolini M., Bindea G., Lagorce C., Wind P., Marliot F., Bruneval P., et al. In situ cytotoxic and memory T cells predict outcome in patients with early-stage colorectal cancer. J. Clin. Oncol. 2009;27:5944–5951. doi: 10.1200/JCO.2008.19.6147. PubMed DOI
Tumeh P.C., Harview C.L., Yearley J.H., Shintaku I.P., Taylor E.J.M., Robert L., Chmielowski B., Spasic M., Henry G., Ciobanu V., et al. PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature. 2014;515:568–571. doi: 10.1038/nature13954. PubMed DOI PMC
Teng M.W., Ngiow S.F., Ribas A., Smyth M.J. Classifying cancers based on T-cell infiltration and PD-L1. Cancer Res. 2015;75:2139–2145. doi: 10.1158/0008-5472.CAN-15-0255. PubMed DOI PMC
Champiat S., Ferté C., Lebel-Binay S., Eggermont A., Soria J.C. Exomics and immunogenics: Bridging mutational load and immune checkpoints efficacy. OncoImmunology. 2014;3:e27817. doi: 10.4161/onci.27817. PubMed DOI PMC
Rizvi N.A., Hellmann M.D., Snyder A., Kvistborg P., Makarov V., Havel J.J., Lee W., Yuan J., Wong P., Ho T.S., et al. Mutational landscape determines sensitivity to PD-1 blockade in non–small cell lung cancer. Science. 2015;348:124–128. doi: 10.1126/science.aaa1348. PubMed DOI PMC
McGranahan N., Furness A.J.S., Rosenthal R., Ramskov S., Lyngaa R., Saini S.K., Jamal-Hanjani M., Wilson G.A., Birkbak N.J., Hiley C.T., et al. Clonal neoantigens elicit T cell immunoreactivity and sensitivity to immune checkpoint blockade. Science. 2016;351:1463–1469. doi: 10.1126/science.aaf1490. PubMed DOI PMC
Le D.T., Uram J.N., Wang H., Bartlett B.R., Kemberling H., Eyring A.D., Skora A.D., Luber B.S., Azad N.S., Laheru D., et al. PD-1 blockade in tumors with mismatch-repair deficiency. N. Engl. J. Med. 2015;372:2509–2520. doi: 10.1056/NEJMoa1500596. PubMed DOI PMC
Hugo W., Zaretsky J.M., Sun L., Song C., Moreno B.H., Hu-Lieskovan S., Berent-Maoz B., Pang J., Chmielowski B., Cherry G., et al. Genomic and transcriptomic features of response to anti-PD-1 therapy in metastatic melanoma. Cell. 2016;165:35–44. doi: 10.1016/j.cell.2016.02.065. PubMed DOI PMC
Chen P.-L., Roh W., Reuben A., Cooper Z.A., Spencer C.N., Prieto P.A., Miller J.P., Bassett R.L., Gopalakrishnan V., Wani K., et al. Analysis of immune signatures in longitudinal tumor samples yields insight into biomarkers of response and mechanisms of resistance to immune checkpoint blockade. Cancer Discov. 2016;6:827–837. doi: 10.1158/2159-8290.CD-15-1545. PubMed DOI PMC
Inoue H., Park J.-H., Kiyotani K., Zewde M., Miyashita A., Jinnin M., Kiniwa Y., Okuyama R., Tanaka R., Fujisawa Y., et al. Intratumoral expression levels of PD-L1, GZMA, and HLA-A along with oligoclonal T cell expansion associate with response to nivolumab in metastatic melanoma. OncoImmunology. 2016;5:e1204507. doi: 10.1080/2162402X.2016.1204507. PubMed DOI PMC
Johnson D.B., Estrada M.V., Salgado R., Sanchez V., Doxie D.B., Opalenik S.R., Vilgelm A.E., Feld E., Johnson A.S., Greenplate A.R., et al. Melanoma-specific MHC-II expression represents a tumour-autonomous phenotype and predicts response to anti-PD-1/PD-L1 therapy. Nat. Commun. 2016;7:10582. doi: 10.1038/ncomms10582. PubMed DOI PMC
Zaretsky J.M., Garcia-Diaz A., Shin D.S., Escuin-Ordinas H., Hugo W., Hu-Lieskovan S., Torrejon D.Y., Abril-Rodriguez G., Sandoval S., Barthly L., et al. Mutations associated with acquired resistance to PD-1 blockade in melanoma. N. Engl. J. Med. 2016;375:819–829. doi: 10.1056/NEJMoa1604958. PubMed DOI PMC
Shin D.S., Zaretsky J.M., Escuin-Ordinas H., Garcia-Diaz A., Hu-Lieskovan S., Kalbasi A., Grasso C.S., Hugo W., Sandoval S., Torrejon D.Y., et al. Primary resistance to PD-1 blockade mediated by JAK1/2 mutations. Cancer Discov. 2017;7:188–201. doi: 10.1158/2159-8290.CD-16-1223. PubMed DOI PMC
Gao J., Shi L.Z., Zhao H., Chen J., Xiong L., He Q., Chen T., Roszik J., Bernatchez C., Woodman S.E., et al. Loss of IFN-γ pathway genes in tumor cells as a mechanism of resistance to anti-CTLA-4 therapy. Cell. 2016;167:397–404. doi: 10.1016/j.cell.2016.08.069. PubMed DOI PMC
Hirano F., Kaneko K., Tamura H., Dong H., Wang S., Ichikawa M., Rietz C., Flies D.B., Lau J.S., Zhu G., et al. Blockade of B7-H1 and PD-1 by monoclonal antibodies potentiates cancer therapeutic immunity. Cancer Res. 2005;65:1089–1096. PubMed
Moreno B.H., Zaretsky J.M., Garcia-Diaz A., Tsoi J., Parisi G., Robert L., Meeth K., Ndoye A., Bosenberg M., Weeraratna A.T., et al. Response to programmed cell death-1 blockade in a murine melanoma syngeneic model requires costimulation, CD4, and CD8 T cells. Cancer Immunol. Res. 2016;4:845–857. doi: 10.1158/2326-6066.CIR-16-0060. PubMed DOI PMC
Roemer M.G.M., Advani R.H., Redd R.A., Pinkus G.S., Natkunam Y., Ligon A.H., Connelly C.F., Pak C.J., Carey C.D., Daadi S.E., et al. Classical Hodgkin lymphoma with reduced B2M/MHC class I expression is associated with Inferior outcome independent of 9p24.1 status. Cancer Immunol. Res. 2016;4:910–916. doi: 10.1158/2326-6066.CIR-16-0201. PubMed DOI PMC
Bercovici N., Trautmann A. Revisiting the role of T cells in tumor regression. OncoImmunology. 2012;1:346–350. doi: 10.4161/onci.18800. PubMed DOI PMC
Thoreau M., Penny H.L., Tan K., Regnier F., Weiss J.M., Lee B., Johannes L., Dransart E., Bon A.L., Abastado J.-P., et al. Vaccine-induced tumor regression requires a dynamic cooperation between T cells and myeloid cells at the tumor site. Oncotarget. 2015;6:27832–27846. doi: 10.18632/oncotarget.4940. PubMed DOI PMC
Lin K.-Y., Guarnieri F.G., Staveley-O’Carroll K.F., Levitsky H.I., August J.T., Pardoll D.M., Wu T.-C. Treatment of established tumors with a novel vaccine that enhances major histocompatibility class II presentation of tumor antigen. Cancer Res. 1996;56:21–26. PubMed
Moynihan K.D., Opel C.F., Szeto G.L., Tzeng A., Zhu E.F., Engreitz J.M., Williams R.T., Rakhra K., Zhang M.H., Rothschilds A.M., et al. Eradication of large established tumors in mice by combination immunotherapy that engages innate and adaptive immune responses. Nat. Med. 2016;22:1402–1410. doi: 10.1038/nm.4200. PubMed DOI PMC
Beldi-Ferchiou A., Lambert M., Dogniaux S., Vely F., Vivier E., Olive D., Dupuy S., Levasseur F., Zucman D., Lebbe C., et al. PD-1 mediates functional exhaustion of activated NK cells in patients with Kaposi sarcoma. Oncotarget. 2016;7:72961–72977. doi: 10.18632/oncotarget.12150. PubMed DOI PMC
Pesce S., Greppi M., Tabellini G., Rampinelli F., Parolini S., Olive D., Moretta L., Moretta A., Marcenaro E. Identification of a subset of human natural killer cells expressing high levels of programmed death 1: A phenotypic and functional characterization. J. Allergy Clin. Immunol. 2017;139:335–346. doi: 10.1016/j.jaci.2016.04.025. PubMed DOI
Kamata T., Suzuki A., Mise N., Ihara F., Takami M., Makita Y., Horinaka A., Harada K., Kunii N., Yoshida S., et al. Blockade of programmed death-1/programmed death ligand pathway enhances the antitumor immunity of human invariant natural killer T cells. Cancer Immunol. Immunother. 2016;65:1477–1489. doi: 10.1007/s00262-016-1901-y. PubMed DOI PMC
Chang W.-S., Kim J.-Y., Kim Y.-J., Kim Y.-S., Lee J.-M., Azuma M., Yagita H., Kang C.-Y. Cutting edge: Programmed death-1/programmed death ligand 1 interaction regulates the induction and maintenance of invariant NKT cell anergy. J. Immunol. 2008;181:6707–6710. doi: 10.4049/jimmunol.181.10.6707. PubMed DOI
Parekh V.V., Lalani S., Kim S., Halder R., Azuma M., Yagita H., Kumar V., Wu L., Kaer L.V. PD-1/PD-L blockade prevents anergy induction and enhances the anti-tumor activities of glycolipid-activated invariant NKT cells. J. Immunol. 2009;182:2816–2826. doi: 10.4049/jimmunol.0803648. PubMed DOI PMC
Durgan K., Ali M., Warner P., Latchman Y.E. Targeting NKT cells and PD-L1 pathway results in augmented anti-tumor responses in a melanoma model. Cancer Immunol. Immunother. 2011;60:547–558. doi: 10.1007/s00262-010-0963-5. PubMed DOI PMC
Van de Berg P.J., van Leeuwen E.M., ten Berge I.J., van Lier R. Cytotoxic human CD4+ T cells. Curr. Opin. Immunol. 2008;20:339–343. doi: 10.1016/j.coi.2008.03.007. PubMed DOI
Quezada S.A., Peggs K.S. Tumor-reactive CD4+ cells: Plasticity beyond helper and regulatory activities. Immunotherapy. 2011;3:915–917. doi: 10.2217/imt.11.83. PubMed DOI
Perez-Diez A., Joncker N.T., Choi K., Chan W.F.N., Anderson C.C., Lantz O., Matzinger P. CD4 cells can be more efficient at tumor rejection than CD8 cells. Blood. 2007;109:5346–5354. doi: 10.1182/blood-2006-10-051318. PubMed DOI PMC
Yan H., Hou X., Li T., Zhao L., Yuan X., Fu H., Zhu R. CD4+ T cell-mediated cytotoxicity eliminates primary tumor cells in metastatic melanoma through high MHC class II expression and can be enhanced by inhibitory receptor blockade. Tumor Biol. 2016:15949–15958. doi: 10.1007/s13277-016-5456-5. PubMed DOI
Taube J.M., Anders R.A., Young G.D., Xu H., Sharma R., McMiller T.L., Chen S., Klein A.P., Pardoll D.M., Topalian S.L., et al. Colocalization of inflammatory response with B7-H1 expression in human melanocytic lesions supports an adaptive resistance mechanism of immune escape. Sci. Transl. Med. 2012;4:127ra37. doi: 10.1126/scitranslmed.3003689. PubMed DOI PMC
Herbst R.S., Soria J.-C., Kowanetz M., Fine G.D., Hamid O., Gordon M.S., Sosman J.A., McDermott D.F., Powderly J.D., Gettinger S.N., et al. Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients. Nature. 2014;515:563–567. doi: 10.1038/nature14011. PubMed DOI PMC
Llosa N.J., Cruise M., Tam A., Wicks E.C., Hechenbleikner E.M., Taube J.M., Blosser R.L., Fan H., Wang H., Luber B.S., et al. The vigorous immune microenvironment of microsatellite instable colon cancer is balanced by multiple counter-inhibitory checkpoints. Cancer Discov. 2015;5:43–51. doi: 10.1158/2159-8290.CD-14-0863. PubMed DOI PMC
Kleinovink J.W., Marijt K.A., Schoonderwoerd M.J.A., van Hall T., Ossendorp F., Fransen M.F. PD-L1 expression on malignant cells is no prerequisite for checkpoint therapy. OncoImmunology. 2017;6:e1294299. doi: 10.1080/2162402X.2017.1294299. PubMed DOI PMC
Ma C.J., Ni L., Zhang Y., Zhang C.L., Wu X.Y., Atia A.N., Thayer P., Moorman J.P., Yao Z.Q. PD-1 negatively regulates interleukin-12 expression by limiting STAT-1 phosphorylation in monocytes/macrophages during chronic hepatitis C virus infection. Immunology. 2011;132:421–431. doi: 10.1111/j.1365-2567.2010.03382.x. PubMed DOI PMC
Yao A., Liu F., Chen K., Tang L., Liu L., Zhang K., Yu C., Bian G., Guo H., Zheng J., et al. Programmed death 1 deficiency induces the polarization of macrophages/microglia to the M1 phenotype after spinal cord injury in mice. Neurotherapeutics. 2014;11:636–650. doi: 10.1007/s13311-013-0254-x. PubMed DOI PMC
Zaidi M.R., Merlino G. The two faces of interferon-γ in cancer. Clin. Cancer Res. 2011;17:6118–6124. doi: 10.1158/1078-0432.CCR-11-0482. PubMed DOI PMC
Mandai M., Hamanishi J., Abiko K., Matsumura N., Baba T., Konishi I. Dual faces of IFNγ in cancer progression: A role of PD-L1 induction in the determination of pro- and antitumor immunity. Clin. Cancer Res. 2016;22:2329–2334. doi: 10.1158/1078-0432.CCR-16-0224. PubMed DOI
Terawaki S., Chikuma S., Shibayama S., Hayashi T., Yoshida T., Okazaki T., Honjo T. IFN-α directly promotes programmed cell death-1 transcription and limits the duration of T cell-mediated immunity. J. Immunol. 2011;186:2772–2779. doi: 10.4049/jimmunol.1003208. PubMed DOI
Kakizaki A., Fujimura T., Furudate S., Kambayashi Y., Yamauchi T., Yagita H., Aiba S. Immunomodulatory effect of peritumorally administered interferon-beta on melanoma through tumor-associated macrophages. OncoImmunology. 2015;4:e1047584. doi: 10.1080/2162402X.2015.1047584. PubMed DOI PMC
Swart M., Verbrugge I., Beltman J.B. Combination approaches with immune-checkpoint blockade in cancer therapy. Front. Oncol. 2016;6:233. doi: 10.3389/fonc.2016.00233. PubMed DOI PMC
Smyth M.J., Ngiow S.F., Ribas A., Teng M.W.L. Combination cancer immunotherapies tailored to the tumour microenvironment. Nat. Rev. Clin. Oncol. 2015;13:143–158. doi: 10.1038/nrclinonc.2015.209. PubMed DOI
Buhtoiarov I.N., Sondel P.M., Wigginton J.M., Buhtoiarova T.N., Yanke E.M., Mahvi D.A., Rakhmilevich A.L. Anti-tumour synergy of cytotoxic chemotherapy and anti-CD40 plus CpG-ODN immunotherapy through repolarization of tumour-associated macrophages. Immunology. 2011;132:226–239. doi: 10.1111/j.1365-2567.2010.03357.x. PubMed DOI PMC
Magner W.J., Kazim A.L., Stewart C., Romano M.A., Catalano G., Grande C., Keiser N., Santaniello F., Tomasi T.B. Activation of MHC Class I, II, and CD40 gene expression by histone deacetylase inhibitors. J. Immunol. 2000;165:7017–7024. doi: 10.4049/jimmunol.165.12.7017. PubMed DOI
Licciardi P.V., Karagiannis T.C. Regulation of immune responses by histone deacetylase inhibitors. Int. Sch. Res. Not. 2012;2012:e690901. doi: 10.5402/2012/690901. PubMed DOI PMC
Kim K., Skora A.D., Li Z., Liu Q., Tam A.J., Blosser R.L., Diaz L.A., Papadopoulos N., Kinzler K.W., Vogelstein B., et al. Eradication of metastatic mouse cancers resistant to immune checkpoint blockade by suppression of myeloid-derived cells. Proc. Natl. Acad. Sci. USA. 2014;111:11774–11779. doi: 10.1073/pnas.1410626111. PubMed DOI PMC
Woods D.M., Sodré A.L., Villagra A., Sarnaik A., Sotomayor E.M., Weber J. HDAC inhibition upregulates PD-1 ligands in melanoma and augments immunotherapy with PD-1 blockade. Cancer Immunol. Res. 2015;3:1375–1385. doi: 10.1158/2326-6066.CIR-15-0077-T. PubMed DOI PMC
Zheng H., Zhao W., Yan C., Watson C.C., Massengill M., Xie M., Massengill C., Noyes D.R., Martinez G.V., Afzal R., et al. HDAC inhibitors enhance T-cell chemokine expression and augment response to PD-1 immunotherapy in lung adenocarcinoma. Clin. Cancer Res. 2016;22:4119–4132. doi: 10.1158/1078-0432.CCR-15-2584. PubMed DOI PMC
Wang X., Schoenhals J.E., Li A., Valdecanas D.R., Ye H., Zhang F., Tang C., Tang M., Liu C.-G., Liu X., et al. Suppression of type I IFN signaling in tumors mediates resistance to anti-PD-1 treatment that can be overcome by radiotherapy. Cancer Res. 2017;77:839–850. doi: 10.1158/0008-5472.CAN-15-3142. PubMed DOI PMC