Анализ возможных маркеров эффективного противоопухолевого клеточного иммунного ответа при назначении ингибиторов контрольных точек

Автор: Малкова А.М., Орлова Р.В., Жукова Н.В., Губаль А.Р., Шаройко В.В.

Журнал: Сибирский онкологический журнал @siboncoj

Рубрика: Обзоры

Статья в выпуске: 2 т.21, 2022 года.

Бесплатный доступ

Цель исследования - анализ возможных маркеров эффективного противоопухолевого клеточного иммунного ответа. Материал и методы. С помощью ключевых слов: ингибиторы контрольных точек, иммунотерапия, Т-лимфоциты, истощенные Т-лимфоциты, противоопухолевый иммунный ответ - были отобраны обзорные и оригинальные статьи (n=34), опубликованные с 2005 по 2020 г. в международных базах данных PubMed, Web of Science, Elsevier. Результаты. Исследование выявило потенциальные маркеры, отражающие высокую активность адаптивного иммунного ответа, основанного на эффективном распознавании антигенов опухоли через молекулы главного комплекса гистосовместимости (MHC), достаточном количестве Т-лимфоцитов и преобладании Т-цитотоксических клеток, а также на низком уровне экспрессии ингибиторных рецепторов и малых молекул. Свою предиктивную значимость показали наличие полиморфизмов единичных нуклеотидов в генах HLA-I и HLA-II, кодирующих белки MHC-I и MHC-II соответственно, высокий уровень лимфоцитов, среди которых наиболее важно преобладание CD8+ Т-клеток и низкий уровень Т-регуляторных клеток (Т-рег), а также наличие полиморфизмов единичных нуклеотидов в генах, кодирующих FcγR рецепторы Т-лимфоцитов. Также была выявлена диагностическая значимость определения экспрессии ингибиторных рецепторов Т-лимфоцитов - TIM3, LAG3, TIGIT, особенно в комплексе с определением уровня экспрессии PD1. Заключение. Полученные результаты могут быть актуальны для внедрения новых методов оценки функциональной активности Т-клеточного иммунного ответа перед назначением ИКТ, а также для разработки новых диагностических панелей, что может представлять интерес для сотрудников клинико-диагностических лабораторий и исследовательских центров.

Еще

Опухоль, адаптивный иммунный ответ, маркеры, эффективность, противоопухолевая терапия

Короткий адрес: https://sciup.org/140293891

IDR: 140293891

Список литературы Анализ возможных маркеров эффективного противоопухолевого клеточного иммунного ответа при назначении ингибиторов контрольных точек

  • DarvinP., Toor S.M., SasidharanNair V., ElkordE. Immune checkpoint inhibitors: recent progress and potential biomarkers. Exp Mol Med. 2018; 50(12): 1-11. doi: 10.1038/s12276-018-0191-1.
  • Longo V., Brunetti O., AzzaritiA., GalettaD., NardulliP., LeonettiF., Silvestris N. Strategies to Improve Cancer Immune Checkpoint Inhibitors Efficacy, Other Than Abscopal Effect: A Systematic Review. Cancers (Basel). 2019; 11(4): 539. doi: 10.3390/cancers11040539.
  • Kambayashi Y., Fujimura T., Hidaka T., Aiba S. Biomarkers for Predicting Efficacies of Anti-PD1 Antibodies. Front Med. 2019; 6: 174. doi: 10.3389/fmed.2019.00174.
  • Davis A.A., Patel V.G. The role of PD-L1 expression as a predictive biomarker: an analysis of all US Food and Drug Administration (FDA) approvals of immune checkpoint inhibitors. J Immunother Cancer. 2019; 7(1): 278. doi: 10.1186/s40425-019-0768-9.
  • Aguiar P.N. Jr., Santoro I.L., Tadokoro H., de Lima Lopes G., Filardi B.A., Oliveira P., Mountzios G., de Mello R.A. The role of PD-L1 expression as a predictive biomarker in advanced non-small-cell lung cancer: a network meta-analysis. Immunotherapy. 2016; 8(4): 479-88. doi: 10.2217/imt-2015-0002.
  • Munhoz R.R., Postow M.A. Recent advances in understanding antitumor immunity. F1000Res. 2016; 5: 2545. doi: 10.12688/f1000re-search.9356.1.
  • McGranahanN., FurnessA.J., RosenthalR., RamskovS., LyngaaR., Saini S.K., Jamal-Hanjani M., Wilson G.A., Birkbak N.J., Hiley C.T., Watkins T.B., Shafi S., Murugaesu N., Mitter R., Akarca A.U., Linares J., Marafioti T., Henry J.Y., Van Allen E.M., Miao D., Schilling B., Schadendorf D., Garraway L.A., Makarov V., Rizvi N.A., Snyder A., Hell-mannM.D., Merghoub T., WolchokJ.D., Shukla S.A., Wu C.J., PeggsK.S., Chan T.A., Hadrup S.R., Quezada S.A., Swanton C. Clonal neoantigens elicit T cell immunoreactivity and sensitivity to immune checkpoint blockade. Science. 2016; 351(6280): 1463-9. doi: 10.1126/science.aaf1490.
  • Rizvi N.A., Hellmann M.D., Snyder A., Kvistborg P., Makarov V., Havel J.J., Lee W., Yuan J., Wong P., Ho T.S., Miller M.L., Rekhtman N., Moreira A.L., Ibrahim F., Bruggeman C., Gasmi B., Zappasodi R., Ma-eda Y, Sander C., GaronE.B., Merghoub T., WolchokJ.D., Schumacher T.N., Chan T.A. Cancer immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science. 2015; 348(6230): 124-8. doi: 10.1126/science.aaa1348.
  • Snyder A., Makarov V., Merghoub T., Yuan J., Zaretsky J.M., Desrichard A., Walsh L.A., Postow M.A., Wong P., Ho T.S., Hollmann T.J., Bruggeman C., Kannan K., Li Y., Elipenahli C., Liu C., Harbison C.T., Wang L., Ribas A., Wolchok J.D., Chan T.A. Genetic basis for clinical response to CTLA-4 blockade in melanoma. N Engl J Med. 2014; 371(23): 2189-99. doi: 10.1056/NEJMoa1406498.
  • Le D.T., Durham J.N., Smith K.N., Wang H., Bartlett B.R., Aulakh L.K., Lu S., Kemberling H., Wilt C., Luber B.S., Wong F., Azad N.S., Rucki A.A., Laheru D., Donehower R., Zaheer A., Fisher G.A., Crocenzi T.S., Lee J.J., Greten T.F., Duffy A.G., Ciombor K.K., Eyring A.D., Lam B.H., Joe A., Kang S.P., Holdhoff M., Danilova L., Cope L., Meyer C., Zhou S., Goldberg R.M., Armstrong D.K., Bever K.M., Fader A.N., Taube J., Housseau F., Spetzler D., Xiao N., Pardoll D.M., Papadopoulos N., Kinzler K.W., Eshleman J.R., Vogelstein B., Anders R.A., Diaz L.A. Jr. Mismatch repair deficiency predicts response of solid tumors to PD-1 blockade. Science. 2017; 357(6349): 409-13. doi: 10.1126/science.aan6733.
  • Ascierto M.L., Kmieciak M., Idowu M.O., Manjili R., Zhao Y., GrimesM., Dumur C., WangE., Ramakrishnan V., WangX.Y., BearH.D., Marincola F.M., Manjili M.H. A signature of immune function genes associated with recurrence-free survival in breast cancer patients. Breast Cancer Res Treat. 2012; 131(3): 871-80. doi: 10.1007/s10549-011-1470-x.
  • Simeone E., Gentilcore G., Giannarelli D., Grimaldi A.M., Caracd C., CurviettoM., Esposito A., PaoneM., PallaM., Cavalcanti E., Sandomenico F., Petrillo A., Botti G., Fulciniti F., Palmieri G., Queirolo P., Marchetti P., Ferraresi V., Rinaldi G., PistilloM.P., Ciliberto G., Mozzillo N., Ascierto P.A. Immunological and biological changes during ipilimumab treatment and their potential correlation with clinical response and survival in patients with advanced melanoma. Cancer Immunol Im-munother. 2014; 63(7): 675-83. doi: 10.1007/s00262-014-1545-8.
  • ChowellD., MorrisL.G.T., GriggC.M., Weber J.K., SamsteinR.M., Makarov V., Kuo F., Kendall S.M., Requena D., Riaz N., Greenbaum B., Carroll J., Garon E., Hyman D.M., Zehir A., Solit D., Berger M., Zhou R., Rizvi N.A., Chan T.A. Patient HLA class I genotype influences cancer response to checkpoint blockade immunotherapy. Science. 2018; 359(6375): 582-7. doi: 10.1126/science.aao4572.
  • Van Allen E.M., Miao D., Schilling B., Shukla S.A., Blank C., Zimmer L., Sucker A., Hillen U., Foppen M.H.G., Goldinger S.M., Utikal J., Hassel J.C., Weide B., Kaehler K.C., Loquai C., Mohr P., Gutzmer R., DummerR., GabrielS., Wu C.J., Schadendorf D., GarrawayL.A. Genomic correlates of response to CTLA-4 blockade in metastatic melanoma. Science. 2015; 350(6257): 207-11. doi: 10.1126/science.aad0095.
  • Bradburn M.J., Clark T.G., Love S.B., Altman D.G. Survival analysis part II: multivariate data analysis--an introduction to concepts and methods. Br J Cancer. 2003; 89(3): 431-6. doi: 10.1038/sj.bjc.6601119.
  • JohnsonD.B., EstradaM.V., SalgadoR., Sanchez V., DoxieD.B., OpalenikS.R., VilgelmA.E., Feld E., JohnsonA.S., GreenplateA.R., Sanders M.E., Lovly C.M., Frederick D.T., Kelley M.C., RichmondA., Irish J.M., Shyr Y., Sullivan R.J., Puzanov I., Sosman J.A., Balko J.M. 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.
  • RoemerM.G.M., Redd RA., CaderF.Z., PakC.J., AbdelrahmanS., Ouyang J., Sasse S., Younes A., Fanale M., Santoro A., Zinzani P.L., Timmerman J., Collins G.P., Ramchandren R., Cohen J.B., De Boer J.P., Kuruvilla J., Savage K.J., Trneny M., Ansell S., Kato K., Farsaci B., Sumbul A., Armand P., Neuberg D.S., Pinkus G.S., Ligon A.H., Rodig S.J., Shipp M.A. Major Histocompatibility Complex Class II and Programmed Death Ligand 1 Expression Predict Outcome After Programmed Death 1 Blockade in Classic Hodgkin Lymphoma. J Clin Oncol. 2018; 36(10): 942-50. doi: 10.1200/JC0.2017.77.3994.
  • Wulfkuhle J.D., Yau C., Wolf D.M., Gallagher R.I., SwigartL.B., Hirst G.L., Campbell M., Nanda R., Liu M.C., Pusztai L., Esserman L., Berry D.A., VeerL., Petricoin E. Quantitative MHC II protein expression levels in tumor epithelium to predict response to the PD1 inhibitor pem-brolizumab in the I-SPY 2 Trial. J Clin Oncol. 2019; 37(15).
  • Rodig S.J., GusenleitnerD., JacksonD.G., GjiniE., Giobbie-Hur-der A., Jin C., ChangH., Lovitch S.B., HorakC., Weber J.S., Weirather J.L., Wolchok J.D., Postow M.A., Pavlick A.C., Chesney J., Hodi F.S. MHC proteins confer differential sensitivity to CTLA-4 and PD-1 blockade in untreated metastatic melanoma. Sci Transl Med. 2018; 10(450). doi: 10.1126/scitranslmed.aar3342.
  • Johnson D.B., Nixon M.J., Wang Y., Wang D.Y., Castellanos E., EstradaM.V., Ericsson-GonzalezP.I., Cote C.H., SalgadoR., Sanchez V., Dean P.T., Opalenik S.R., Schreeder D.M., Rimm D.L., Kim J.Y., Bordeaux J., Loi S., HornL., SandersM.E., FerrellP.B. Jr., Xu Y., Sosman J.A., Davis R.S., Balko J.M. Tumor-specific MHC-II expression drives a unique pattern of resistance to immunotherapy via LAG-3/FCRL6 engagement. JCI Insight. 2018; 3(24). doi: 10.1172/jci.insight.120360.
  • De Angulo G., Yuen C., Palla S.L., Anderson P.M., Zweidler-McKay P.A. Absolute lymphocyte count is a novel prognostic indicator in ALL and AML: implications for risk stratification and future studies. Cancer. 2008; 112(2): 407-15. doi: 10.1002/cncr.23168.
  • Jiang T., Qiao M., Zhao C., Li X., Gao G., Su C., Ren S., Zhou C. Pretreatment neutrophil-to-lymphocyte ratio is associated with outcome of advanced-stage cancer patients treated with immunotherapy: a meta-analysis. Cancer Immunol Immunother. 2018; 67(5): 713-27. doi: 10.1007/ s00262-018-2126-z.
  • Martens A., Wistuba-Hamprecht K., Yuan J., Postow MA., Wong P., Capone M., Madonna G., Khammari A., Schilling B., Sucker A., Schadendorf D., Martus P., Dreno B., Ascierto P.A., Wolchok J.D., Pawelec G., Garbe C., Weide B. Increases in Absolute Lymphocytes and Circulating CD4+ and CD8+ T Cells Are Associated with Positive Clinical Outcome of Melanoma Patients Treated with Ipilimumab. Clin Cancer Res. 2016; 22(19): 4848-58. doi: 10.1158/1078-0432.CCR-16-0249.
  • Subrahmanyam P.B., Dong Z., GusenleitnerD., Giobbie-Hurder A., Severgnini M., Zhou J., Manos M., Eastman L.M., Maecker H.T., Hodi F.S. Distinct predictive biomarker candidates for response to anti-CTLA-4 and anti-PD-1 immunotherapy in melanoma patients. J Immunother Cancer. 2018; 6(1): 18. doi: 10.1186/s40425-018-0328-8.
  • Reuben J.M., LeeB.N., Li C., Gomez-Navarro J., Bozon V.A., Parker C.A., HernandezI.M., Gutierrez C., Lopez-Berestein G., CamachoL.H. Biologic and immunomodulatory events after CTLA-4 blockade with ticilimumab in patients with advanced malignant melanoma. Cancer. 2006; 106(11): 2437-44. doi: 10.1002/cncr.21854.
  • Kelderman S., HeemskerkB., van Tinteren H., van den Brom R.R., Hospers G.A., van den Eertwegh A.J., Kapiteijn E.W., de Groot J.W., Soetekouw P., Jansen R.L., Fiets E., Furness A.J., Renn A., KrzystanekM., Szallasi Z., Lorigan P., Gore M.E., Schumacher T.N., Haanen J.B., Larkin J.M., Blank C.U. Lactate dehydrogenase as a selection criterion for ipilimumab treatment in metastatic melanoma. Cancer Immunol Im-munother. 2014; 63(5): 449-58. doi: 10.1007/s00262-014-1528-9.
  • Xia A., Zhang Y., Xu J., Yin T., Lu X.J. T Cell Dysfunction in Cancer Immunity and Immunotherapy. Front Immunol. 2019; 10: 1719. doi: 10.3389/fimmu.2019.01719.
  • Arce VargasF, FurnessA.J.S., LitchfieldK., JoshiK., RosenthalR., Ghorani E., Solomon I., Lesko M.H., Ruef N., Roddie C., Henry J.Y., Spain L., Ben Aissa A., Georgiou A., Wong Y.N.S., Smith M., Strauss D., Hayes A., Nicol D., O 'Brien T., Martensson L., Ljungars A., Teige I., Frendeus B.; TRACERx Melanoma; TRACERx Renal; TRACERx Lung consortia, Pule M., Marafioti T., Gore M., Larkin J., Turajlic S., Swanton C., Peggs K.S., Quezada S.A. Fc Effector Function Contributes to the Activity of Human Anti-CTLA-4 Antibodies. Cancer Cell. 2018; 33(4): 649-63. doi: 10.1016/j.ccell.2018.02.010.
  • Fujii S., ShimizuK., Shimizu T., LotzeM.T. Interleukin-10 promotes the maintenance of antitumor CD8(+) T-cell effector function in situ. Blood. 2001; 98(7): 2143-51. doi: 10.1182/blood.v98.7.2143.
  • Wherry E.J., Blattman J.N., Murali-Krishna K., van der Most R., AhmedR. Viral persistence alters CD8 T-cell immunodominance and tissue distribution and results in distinct stages of functional impairment. J Virol. 2003; 77(8): 4911-27. doi: 10.1128/jvi.77.8.4911-4927.2003.
  • Gros A., Robbins P.F., Yao X., Li Y.F., Turcotte S., Tran E., Wunderlich J.R., Mixon A., Farid S., Dudley M.E., Hanada K., Almeida J.R., Darko S., Douek D.C., Yang J.C., Rosenberg S.A. PD-1 identifies the patient-specific CD8+ tumor-reactive repertoire infiltrating human tumors. J Clin Invest. 2014; 124(5): 2246-59. doi: 10.1172/JCI73639.
  • Katsurada M., Nagano T., Tachihara M., Kiriu T., Furukawa K., Koyama K., Otoshi T., Sekiya R., Hazama D., Tamura D., Nakata K., Katsurada N., Yamamoto M., Kobayashi K., Nishimura Y. Baseline Tumor Size as a Predictive and Prognostic Factor of Immune Checkpoint Inhibitor Therapy for Non-small Cell Lung Cancer. Anticancer Res. 2019; 39(2): 815-25. doi: 10.21873/anticanres.13180.
  • Qu J., Wang L., Jiang M., Zhao D., Wang Y., Zhang F., Li J., Zhang X. A Review About Pembrolizumab in First-Line Treatment of Advanced NSCLC: Focus on KEYNOTE Studies. Cancer Manag Res. 2020; 12: 6493-6509. doi: 10.2147/CMAR.S257188.
  • Wherry E.J., Kurachi M. Molecular and cellular insights into T cell exhaustion. Nat Rev Immunol. 2015; 15(8): 486-99. doi: 10.1038/ nri3862.
  • Francisco L.M., Sage P.T., Sharpe A.H. The PD-1 pathway in tolerance and autoimmunity. Immunol Rev. 2010; 236: 219-42. doi: 10.1111/j.1600-065X.2010.00923.x.
  • Joller N., Lozano E., Burkett P.R., Patel B., Xiao S., Zhu C., Xia J., Tan T.G., Sefik E., Yajnik V., Sharpe A.H., Quintana F.J., Mathis D., Benoist C., Hafler D.A., Kuchroo V.K. Treg cells expressing the coin-hibitory molecule TIGIT selectively inhibit proinflammatory Th1 and Th17 cell responses. Immunity. 2014; 40(4): 569-81. doi: 10.1016/j. immuni.2014.02.012.
  • Kurtulus S., Sakuishi K., Ngiow S.F., JollerN., Tan D.J., TengM.W., Smyth M.J., Kuchroo V.K., Anderson A.C. TIGIT predominantly regulates the immune response via regulatory T cells. J Clin Invest. 2015; 125(11): 4053-62. doi: 10.1172/JCI81187.
  • SugiyamaD., NishikawaH., Maeda Y., NishiokaM., TanemuraA., Katayama I., Ezoe S., Kanakura Y., Sato E., Fukumori Y., Karbach J., Jäger E., Sakaguchi S. Anti-CCR4 mAb selectively depletes effector-type FoxP3+CD4+ regulatory T cells, evoking antitumor immune responses in humans. Proc Natl Acad Sci U S A. 2013; 110(44): 17945-50. doi: 10.1073/pnas.1316796110.
  • Egen J.G., Allison J.P. Cytotoxic T lymphocyte antigen-4 accumulation in the immunological synapse is regulated by TCR signal strength. Immunity. 2002; 16(1): 23-35. doi: 10.1016/s1074-7613(01)00259-x.
  • Quigley M., Pereyra F., Nilsson B., Porichis F., Fonseca C., Eichbaum Q., JulgB., Jesneck J.L., BrosnahanK., Imam S., RussellK., Toth I., Piechocka-Trocha A., Dolfi D., Angelosanto J., Crawford A., Shin H., KwonD.S., Zupkosky J., FranciscoL., Freeman G.J., WherryE.J., Kaufmann D.E., WalkerB.D., EbertB., Haining W.N. Transcriptional analysis of HIV-specific CD8+ T cells shows that PD-1 inhibits T cell function by upregulating BATF. Nat Med. 2010; 16(10): 1147-51. doi: 10.1038/ nm.2232.
  • Chauvin JM., Pagliano O., Fourcade J., Sun Z., WangH., Sander C., Kirkwood J.M., Chen T.H., MaurerM., KormanA.J., ZarourH.M. TIGIT and PD-1 impair tumor antigen-specific CD8+ T cells in melanoma patients. J Clin Invest. 2015; 125(5): 2046-58. doi: 10.1172/JCI80445.
  • He Q.F., Xu Y., Li J., Huang Z.M., Li X.H., WangX. CD8+ T-cell exhaustion in cancer: mechanisms and new area for cancer immunotherapy. Brief Funct Genomics. 2019; 18(2): 99-106. doi: 10.1093/bfgp/ely006.
  • Fourcade J., Sun Z., Benallaoua M., Guillaume P., Luescher I.F., Sander C., Kirkwood J.M., Kuchroo V., Zarour H.M. Upregulation of Tim-3 and PD-1 expression is associated with tumor antigen-specific CD8+ T cell dysfunction in melanoma patients. J Exp Med. 2010; 207(10): 2175-86. doi: 10.1084/jem.20100637.
  • Piao Y.R., Piao L.Z., Zhu LH, Jin Z.H., DongX.Z. Prognostic value of T cell immunoglobulin mucin-3 in prostate cancer. Asian Pac J Cancer Prev. 2013; 14(6): 3897-901. doi: 10.7314/apjcp.2013.14.6.3897.
  • Yuan J., Jiang B., Zhao H., Huang Q. Prognostic implication of TIM-3 in clear cell renal cell carcinoma. Neoplasma. 2014; 61(1): 35-40.
  • Jiang J., Jin M.S., Kong^ F., Cao D., Ma H.X., Jia Z., Wang Y.P., Suo J., Cao X. Decreased galectin-9 and increased Tim-3 expression are related to poor prognosis in gastric cancer. PLoS One. 2013; 8(12). doi: 10.1371/journal.pone.0081799.
  • Cao Y., Zhou X., Huang X., Li Q., Gao L., Jiang L., Huang M., Zhou J. Tim-3 expression in cervical cancer promotes tumor metastasis. PLoS One. 2013; 8(1). doi: 10.1371/journal.pone.0053834.
  • Chen J., Chen Z. The effect of immune microenvironment on the progression and prognosis of colorectal cancer. Med Oncol. 2014; 31(8): 82. doi: 10.1007/s12032-014-0082-9.
  • Kotaskova J., Tichy B., TrbusekM., FrancovaH.S., Kabathova J., Malcikova J., Doubek M., Brychtova Y., Mayer J., Pospisilova S. High expression of lymphocyte-activation gene 3 (LAG3) in chronic lympho-cytic leukemia cells is associated with unmutated immunoglobulin variable heavy chain region (IGHV) gene and reduced treatment-free survival. J Mol Diagn. 2010; 12(3): 328-34. doi: 10.2353/jmoldx.2010.090100.
  • Chen Q., Daniel V., Maher D.W., Hersey P. Production of IL-10 by melanoma cells: examination of its role in immunosuppression mediated by melanoma. Int J Cancer. 1994; 56(5): 755-60. doi: 10.1002/ ijc.2910560524.
  • Koustas E., Sarantis P., Papavassiliou A.G., Karamouzis M.V. The Resistance Mechanisms of Checkpoint Inhibitors in Solid Tumors. Biomolecules. 2020; 10(5): 666. doi: 10.3390/biom10050666.
  • Raskovalova T., Lokshin A., Huang X., Su Y., Mandic M., Zarour H.M., Jackson E.K., Gorelik E. Inhibition of cytokine production and cytotoxic activity of human antimelanoma specific CD8+ and CD4+ T lymphocytes by adenosine-protein kinase A type I signaling. Cancer Res. 2007; 67(12): 5949-56. doi: 10.1158/0008-5472.CAN-06-4249.
  • Ohta A., Sitkovsky M. Extracellular adenosine-mediated modulation of regulatory T cells. Front Immunol. 2014; 5: 304. doi: 10.3389/ fimmu.2014.00304.
  • MunnD.H., Mellor A.L. Indoleamine 2,3-dioxygenase and tumor-induced tolerance. J Clin Invest. 2007; 117(5): 1147-54. doi: 10.1172/ JCI31178.
  • Holmgaard R.B., ZamarinD., Munn D.H., Wolchok J.D., Allison J.P. Indoleamine 2,3-dioxygenase is a critical resistance mechanism in antitumor T cell immunotherapy targeting CTLA-4. J Exp Med. 2013; 210(7): 1389-402. doi: 10.1084/jem.20130066.
  • Woo S.R., Turnis M.E., Goldberg M.V., Bankoti J., Selby M., Nirschl C.J., Bettini M.L., Gravano D.M., Vogel P., Liu C.L., Tangsom-batvisit S., Grosso J.F., Netto G., Smeltzer M.P., Chaux A., Utz P.J., Workman C.J., Pardoll D.M., Korman A.J., Drake C.G., Vignali D.A. Immune inhibitory molecules LAG-3 and PD-1 synergistically regulate T-cell function to promote tumoral immune escape. Cancer Res. 2012; 72(4): 917-27. doi: 10.1158/0008-5472.CAN-11-1620.
  • Fourcade J., Sun Z., Pagliano O., Guillaume P., Luescher I.F., Sander C., Kirkwood J.M., Olive D., Kuchroo V, Zarour H.M. CD8(+) T cells specific for tumor antigens can be rendered dysfunctional by the tumor microenvironment through upregulation of the inhibitory receptors BTLA and PD-1. Cancer Res. 2012; 72(4): 887-96. doi: 10.1158/0008-5472.CAN-11-2637.
  • CurranM.A., Montalvo W, YagitaH., Allison J.P. PD-1 and CTLA-4 combination blockade expands infiltrating T cells and reduces regulatory T and myeloid cells within B16 melanoma tumors. Proc Natl Acad Sci U 5 A. 2010; 107(9): 4275-80. doi: 10.1073/pnas.0915174107.
  • Shayan G., Srivastava R., Li J., Schmitt N., Kane L.P., Ferris R.L. Adaptive resistance to anti-PD 1 therapy by tim-3 upregulation is mediated by the PI3k-akt pathway in head and neck cancer. Oncoimmunology. 2017; 6(1). doi: 10.1080/2162402X.2016.1261779.
  • WeiH., ZhaoL., Li W., FanK., Qian W., Hou S., WangH., DaiM., Hellstrom I., Hellstrom K.E., Guo Y. Combinatorial PD-1 blockade and CD137 activation has therapeutic efficacy in murine cancer models and synergizes with cisplatin. PLoS One. 2013; 8(12). doi: 10.1371/journal. pone.0084927.
  • Chen S., Lee L.F., Fisher T.S., Jessen B., ElliottM., Evering W., Logronio K., Tu G.H., Tsaparikos K., Li X., Wang H., Ying C., Xiong M., VanArsdale T., Lin J.C. Combination of 4-1BB agonist and PD-1 antagonist promotes antitumor effector/memory CD8 T cells in a poorly immunogenic tumor model. Cancer Immunol Res. 2015; 3(2): 149-60. doi: 10.1158/2326-6066.CIR-14-0118.
  • Weinberg A.D., Rivera M.M., Prell R., Morris A., Ramstad T., Vetto J.T., Urba W.J., Alvord G., Bunce C., Shields J. Engagement of the OX-40 receptor in vivo enhances antitumor immunity. J Immunol. 2000; 164(4): 2160-9. doi: 10.4049/jimmunol.164.4.2160.
  • Rafei-ShamsabadiD., Lehr S., vonBubnoffD., MeissF. Successful combination therapy of systemic checkpoint inhibitors and intralesional interleukin-2 in patients with metastatic melanoma with primary therapeutic resistance to checkpoint inhibitors alone. Cancer Immunol Immunother. 2019; 68(9): 1417-28. doi: 10.1007/s00262-019-02377-x.
  • HouD.Y., Muller A.J., SharmaM.D., DuHadaway J., Banerjee T., JohnsonM., Mellor A.L., Prendergast G.C., Munn D.H. Inhibition of in-doleamine 2,3-dioxygenase in dendritic cells by stereoisomers of 1-methyl-tryptophan correlates with antitumor responses. Cancer Res. 2007; 67(2): 792-801. doi: 10.1158/0008-5472.CAN-06-2925.
  • Gangadhar T.C., Hamid O., Smith D.C., Bauer T.M., Wasser J.S., Luke J.J., Balmanoukian A.S., Kaufman D.R., Zhao Yu., Maleski J., Leopold L., Gajewski T.F. Preliminary results from a Phase I/II study of epacadostat (incb024360) in combination with pembrolizumab in patients with selected advanced cancers. J Immunother cancer. 2015; 3(2). doi: 10.1186/2051-1426-3-S2-07.
Еще
Статья научная