Resistance to immune checkpoint inhibitors in the treatment of metastatic renal cancer
https://doi.org/10.21294/1814-4861-2023-22-4-109-117
Abstract
Over the past 5 years, checkpoint inhibitors including anti-CTLA-4 and anti-PD-1/PD-L1 blockers have changed approaches to therapy of metastatic renal cell cancer. However, more than 55 % of patients with advanced kidney cancer remain resistant to immunotherapy. This paper refects the causes that lead to primary and acquired resistance to immune checkpoint inhibitors during the treatment of metastatic renal cell cancer.
The purpose of the study was to elucidate the mechanisms underlying resistance to checkpoint inhibitors during the treatment of metastatic kidney cancer.
Material and Methods. A literature search was conducted using Pubmed database in the time interval between 2010 and 2023. We identifed 286 publications of which 59 were relevant for our review.
Results. There are many factors that contribute to primary or acquired resistance to immunotherapy, including factors associated with the tumor cell as well as tumor microenvironment factors.
Conclusion. Many innovative approaches to overcoming resistance to monoclonal antibodies are being investigated in clinical trials. In connection with the advent of new methods, the cellular composition of the tumor microenvironment and its role in the emergence of tumor resistance to immunotherapy are becoming increasingly clear. New biomarkers are emerging to help identify the best candidates for immunotherapy in metastatic kidney cancer. However, they require further study.
About the Authors
A. A. IzmailovRussian Federation
Adel A. Izmailov, MD, DSc, Chief Physician,
73/1, Oktyabrya Ave., 450054, Ufa
R. R. Rakhimov
Russian Federation
Radmir R. Rakhimov, MD, PhD, Oncologist of the Department of Antitumor Drug Therapy,
73/1, Oktyabrya Ave., 450054, Ufa
A. V. Sultanbayev
Russian Federation
Alexander V. Sultanbaev, MD, PhD, Head of the Department of Antitumor Drug Therapy,
73/1, Oktyabrya Ave., 450054, Ufa
K. V. Menshikov
Russian Federation
Konstantin V. Menshikov, MD, PhD, Oncologist of the Department of Antitumor Drug Therapy; Associate Professor of the Department of Oncology with courses in Oncology and Pathological Anatomy,
73/1, Oktyabrya Ave., 450054, Ufa;
47, Zaki Validi St., 450077, Ufa
I. R. Gilyazova
Russian Federation
Irina R. Gilyazova, PhD, Associate Professor of the Department of Medical Genetics and Fundamental Medicine; Senior Researcher of the Laboratory of Human Molecular Genetics
47, Zaki Validi St., 450077, Ufa;
71, Octobrya Ave., 450054, Ufa
V. M. Zabelin
Russian Federation
Vadim M. Zabelin, student,
1, Ostrovityanova St., 117997, Moscow
A. A. Izmailov
Russian Federation
Albert A. Izmailov, MD, Postgraduate,
3, 2nd Botkinsky proezd, 125284, Moscow
References
1. Malignant tumors in Russia in 2021 (morbidity and mortality). Ed. by A.D. Kaprin, V.V. Starinsky, A.O. Shakhzadova. Moscow, 2022. 252 p. (in Russian).
2. Timofeev I.V. Nivolumab: 5 years from the day of international registration of immunotherapy of metastatic kidney cancer. Malignant Tumours. 2020; 10(4): 21–9. (in Russian). doi: 10.18027/2224-5057-2020-10-4-21-29.
3. Kushlinskii N.E., Fridman M.V., Morozov A.A., Gershtein E.S., Kadagidze Z.G., Matveev V.B. Modern approaches to kidney cancer immunotherapy. Cancer Urology. 2018; 14(2): 54–67. (in Russian). doi: 10.17650/1726-9776-2018-14-2-54-67.
4. Matveev V.B., Volkova M.I., Olshanskaya A.S. Changing paradigm of immunooncology in advanced kidney cancer: nivolumab and ipilimumab combination in the frst line therapy. Cancer Urology. 2019; 15(1): 125–30. (in Russian). doi: 10.17650/1726-9776-2019-15-1-125-130.
5. Sayapina M.S., Savyolov N.A., Lyubimova N.V., Timofeev Yu.S., Nosov D.A. Potential biomarkers for nivolumab therapy of metastatic renal cell carcinoma. Cancer Urology. 2018; 14(1): 16–27. (in Russian). https://doi.org/10.17650/1726-9776-2018-14-1-16-27.
6. Motzer R.J., Escudier B., McDermott D.F., George S., Hammers H.J., Srinivas S., Tykodi S.S., Sosman J.A., Procopio G., Plimack E.R., Castellano D., Choueiri T.K., Gurney H., Donskov F., Bono P., Wagstaff J., Gauler T.C., Ueda T., Tomita Y., Schutz F.A., Kollmannsberger C., Larkin J., Ravaud A., Simon J.S., Xu L.A., Waxman I.M., Sharma P.; CheckMate 025 Investigators. Nivolumab versus Everolimus in Advanced RenalCell Carcinoma. N Engl J Med. 2015; 373(19): 1803–13. doi: 10.1056/NEJMoa1510665.
7. Motzer R.J., Rini B.I., McDermott D.F., Arén Frontera O., Hammers H.J., Carducci M.A., Salman P., Escudier B., Beuselinck B., Amin A., Porta C., George S., Neiman V., Bracarda S., Tykodi S.S., Barthélémy P., Leibowitz-Amit R., Plimack E.R., Oosting S.F., Redman B., Melichar B., Powles T., Nathan P., Oudard S., Pook D., Choueiri T.K., Donskov F., Grimm M.O., Gurney H., Heng D.Y.C., Kollmannsberger C.K., Harrison M.R., Tomita Y., Duran I., Grünwald V., McHenry M.B., Mekan S., Tannir N.M.; CheckMate 214 investigators. Nivolumab plus ipilimumab versus sunitinib in frst-line treatment for advanced renal cell carcinoma: extended follow-up of efcacy and safety results from a randomised, controlled, phase 3 trial. Lancet Oncol. 2019; 20(10): 1370–85. doi: 10.1016/S1470-2045(19)30413-9. Erratum in: Lancet Oncol. 2019; Erratum in: Lancet Oncol. 2020; 21(6). Erratum in: Lancet Oncol. 2020; 21(11).
8. Rini B.I., Plimack E.R., Stus V., Gafanov R., Hawkins R., Nosov D., Pouliot F., Alekseev B., Soulières D., Melichar B., Vynnychenko I., Kryzhanivska A., Bondarenko I., Azevedo S.J., Borchiellini D., Szczylik C., Markus M., McDermott R.S., Bedke J., Tartas S., Chang Y.H., Tamada S., Shou Q., Perini R.F., Chen M., Atkins M.B., Powles T.; KEYNOTE-426 Investigators. Pembrolizumab plus Axitinib versus Sunitinib for Advanced Renal-Cell Carcinoma. N Engl J Med. 2019; 380(12): 1116–27. doi: 10.1056/NEJMoa1816714.
9. Motzer R.J., Penkov K., Haanen J., Rini B., Albiges L., Campbell M.T., Venugopal B., Kollmannsberger C., Negrier S., Uemura M., Lee J.L., Vasiliev A., Miller W.H., Gurney H., Schmidinger M., Larkin J., Atkins M.B., Bedke J., Alekseev B., Wang J., Mariani M., Robbins P.B., Chudnovsky A., Fowst C., Hariharan S., Huang B., di Pietro A., Choueiri T.K. Avelumab plus Axitinib versus Sunitinib for Advanced Renal-Cell Carcinoma. N Engl J Med. 2019; 380(12): 1103–15. doi: 10.1056/NEJMoa1816047.
10. Khan K.A., Kerbel R.S. Improving immunotherapy outcomes with anti-angiogenic treatments and vice versa. Nat Rev Clin Oncol. 2018; 15(5): 310–24. doi: 10.1038/nrclinonc.2018.9.
11. Conforti F., Pala L., Bagnardi V., De Pas T., Martinetti M., Viale G., Gelber R.D., Goldhirsch A. Cancer immunotherapy efcacy and patients’ sex: a systematic review and meta-analysis. Lancet Oncol. 2018; 19(6): 737–46. doi: 10.1016/S1470-2045(18)30261-4.
12. Polanczyk M.J., Hopke C., Vandenbark A.A., Offner H. Estrogenmediated immunomodulation involves reduced activation of efector T cells, potentiation of Treg cells, and enhanced expression of the PD-1 costimulatory pathway. J Neurosci Res. 2006; 84(2): 370–8. doi: 10.1002/jnr.20881.
13. Polanczyk M.J., Hopke C., Vandenbark A.A., Offner H. Treg suppressive activity involves estrogen-dependent expression of programmed death-1 (PD-1). Int Immunol. 2007; 19(3): 337–43. doi: 10.1093/intimm/dxl151.
14. Chowell D., Krishna C., Pierini F., Makarov V., Rizvi N.A., Kuo F., Morris L.G.T., Riaz N., Lenz T.L., Chan T.A. Evolutionary divergence of HLA class I genotype impacts efcacy of cancer immunotherapy. Nat Med. 2019; 25(11): 1715–20. doi: 10.1038/s41591-019-0639-4.
15. Chowell D., Morris L.G.T., Grigg C.M., Weber J.K., Samstein R.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 infuences cancer response to checkpoint blockade immunotherapy. Science. 2018; 359(6375): 582–7. doi: 10.1126/science.aao4572.
16. Jouinot A., Vazeille C., Goldwasser F. Resting energy metabolism and anticancer treatments. Curr Opin Clin Nutr Metab Care. 2018; 21(3): 145–51. doi: 10.1097/MCO.0000000000000457.
17. Soldati L., Di Renzo L., Jirillo E., Ascierto P.A., Marincola F.M., De Lorenzo A. The infuence of diet on anti-cancer immune responsiveness. J Transl Med. 2018; 16(1): 75. doi: 10.1186/s12967-018-1448-0.
18. Schmid D., Leitzmann M.F. Association between physical activity and mortality among breast cancer and colorectal cancer survivors: a systematic review and meta-analysis. Ann Oncol. 2014; 25(7): 1293–311. doi: 10.1093/annonc/mdu012.
19. Cortellini A., Bozzetti F., Palumbo P., Brocco D., Di Marino P., Tinari N., De Tursi M., Agostinelli V., Patruno L., Valdesi C., Mereu M., Verna L., Lanfuti Baldi P., Venditti O., Cannita K., Masciocchi C., Barile A., McQuade J.L., Ficorella C., Porzio G. Weighing the role of skeletal muscle mass and muscle density in cancer patients receiving PD-1/PD-L1 checkpoint inhibitors: a multicenter real-life study. Sci Rep. 2020; 10: 1456. doi: 10.1038/s41598-020-58498-2.
20. Routy B., Le Chatelier E., Derosa L., Duong C.P.M., Alou M.T., Daillère R., Fluckiger A., Messaoudene M., Rauber C., Roberti M.P., Fidelle M., Flament C., Poirier-Colame V., Opolon P., Klein C., Iribarren K., Mondragón L., Jacquelot N., Qu B., Ferrere G., Clémenson C., Mezquita L., Masip J.R., Naltet C., Brosseau S., Kaderbhai C., Richard C., Rizvi H., Levenez F., Galleron N., Quinquis B., Pons N., Ryffel B., Minard-Colin V., Gonin P., Soria J.C., Deutsch E., Loriot Y., Ghiringhelli F., Zalcman G., Goldwasser F., Escudier B., Hellmann M.D., Eggermont A., Raoult D., Albiges L., Kroemer G., Zitvogel L. Gut microbiome infuences efcacy of PD-1-based immunotherapy against epithelial tumors. Science. 2018; 359(6371): 91–7. doi: 10.1126/science.aan3706.
21. Elkrief A., Derosa L., Kroemer G., Zitvogel L., Routy B. The negative impact of antibiotics on outcomes in cancer patients treated with immunotherapy: a new independent prognostic factor? Ann Oncol. 2019; 30(10): 1572–9. doi: 10.1093/annonc/mdz206.
22. Routy B., Gopalakrishnan V., Daillère R., Zitvogel L., Wargo J.A., Kroemer G. The gut microbiota infuences anticancer immunosurveillance and general health. Nat Rev Clin Oncol. 2018; 15(6): 382–96. doi: 10.1038/s41571-018-0006-2.
23. Derosa L., Hellmann M.D., Spaziano M., Halpenny D., Fidelle M., Rizvi H., Long N., Plodkowski A.J., Arbour K.C., Chaft J.E., Rouche J.A., Zitvogel L., Zalcman G., Albiges L., Escudier B., Routy B. Negative association of antibiotics on clinical activity of immune checkpoint inhibitors in patients with advanced renal cell and non-small-cell lung cancer. Ann Oncol. 2018; 29(6): 1437–44. doi: 10.1093/annonc/mdy103.
24. Sanmamed M.F., Chen L. A Paradigm Shift in Cancer Immunotherapy: From Enhancement to Normalization. Cell. 2018; 175(2): 313–26. doi: 10.1016/j.cell.2018.09.035. Erratum in: Cell. 2019; 176(3): 677.
25. Tinsley N., Zhou C., Tan G., Rack S., Lorigan P., Blackhall F., Krebs M., Carter L., Thistlethwaite F., Graham D., Cook N. Cumulative Antibiotic Use Signifcantly Decreases Efcacy of Checkpoint Inhibitors in Patients with Advanced Cancer. Oncologist. 2020; 25(1): 55–63. doi: 10.1634/theoncologist.2019-0160.
26. Mahata B., Zhang X., Kolodziejczyk A.A., Proserpio V., HaimVilmovsky L., Taylor A.E., Hebenstreit D., Dingler F.A., Moignard V., Göttgens B., Arlt W., McKenzie A.N., Teichmann S.A. Single-cell RNA sequencing reveals T helper cells synthesizing steroids de novo to contribute to immune homeostasis. Cell Rep. 2014; 7(4): 1130–42. doi: 10.1016/j.celrep.2014.04.011.
27. Arbour K.C., Mezquita L., Long N., Rizvi H., Auclin E., Ni A., Martínez-Bernal G., Ferrara R., Lai W.V., Hendriks L.E.L., Sabari J.K., Caramella C., Plodkowski A.J., Halpenny D., Chaft J.E., Planchard D., Riely G.J., Besse B., Hellmann M.D. Impact of Baseline Steroids on Effcacy of Programmed Cell Death-1 and Programmed Death-Ligand 1 Blockade in Patients With Non-Small-Cell Lung Cancer. J Clin Oncol. 2018; 36(28): 2872–8. doi: 10.1200/JCO.2018.79.0006.
28. Fucà G., Galli G., Poggi M., Lo Russo G., Proto C., Imbimbo M., Ferrara R., Zilembo N., Ganzinelli M., Sica A., Torri V., Colombo M.P., Vernieri C., Balsari A., de Braud F., Garassino M.C., Signorelli D. Modulation of peripheral blood immune cells by early use of steroids and its association with clinical outcomes in patients with metastatic non-small cell lung cancer treated with immune checkpoint inhibitors. ESMO Open. 2019; 4(1). doi: 10.1136/esmoopen-2018-000457.
29. Gubin M.M., Zhang X., Schuster H., Caron E., Ward J.P., Noguchi T., Ivanova Y., Hundal J., Arthur C.D., Krebber W.J., Mulder G.E., Toebes M., Vesely M.D., Lam S.S., Korman A.J., Allison J.P., Freeman G.J., Sharpe A.H., Pearce E.L., Schumacher T.N., Aebersold R., Rammensee H.G., Melief C.J., Mardis E.R., Gillanders W.E., Artyomov M.N., Schreiber R.D. Checkpoint blockade cancer immunotherapy targets tumour-specifc mutant antigens. Nature. 2014; 515(7528): 577–81. doi: 10.1038/nature13988.
30. Yarchoan M., Hopkins A., Jaffee E.M. Tumor Mutational Burden and Response Rate to PD-1 Inhibition. N Engl J Med. 2017; 377(25): 2500–1. doi: 10.1056/NEJMc1713444.
31. Labriola M.K., Zhu J., Gupta R.T., McCall S., Jackson J., Kong E.F., White J.R., Cerqueira G., Gerding K., Simmons J.K., George D., Zhang T. Characterization of tumor mutation burden, PD-L1 and DNA repair genes to assess relationship to immune checkpoint inhibitors response in metastatic renal cell carcinoma. J Immunother Cancer. 2020; 8(1). doi: 10.1136/jitc2019-000319. Erratum in: J Immunother Cancer. 2020; 8(1).
32. Turajlic S., Litchfeld K., Xu H., Rosenthal R., McGranahan N., Reading J.L., Wong Y.N.S., Rowan A., Kanu N., Al Bakir M., Chambers T., Salgado R., Savas P., Loi S., Birkbak N.J., Sansregret L., Gore M., Larkin J., Quezada S.A., Swanton C. Insertion-and-deletion-derived tumour-specifc neoantigens and the immunogenic phenotype: a pan-cancer analysis. Lancet Oncol. 2017; 18(8): 1009–21. doi: 10.1016/S1470-2045(17)30516-8.
33. Voss M.H., Novik J.B., Hellmann M.D., Ball M., Hakimi A.A., Miao D., Margolis C., Horak C., Wind-Rotolo M., De Velasco G., Tannir N.M., Tamboli P., Appleman L.J., Rathmell K., Hsieh J.J., Allaf M., Choueiri T.K., VanAllen E., Snyder A., Motzer R.J. Correlation of degree of tumor immune infltration and insertion-and-deletion (indel) burden with outcome on programmed death 1 (PD1) therapy in advanced renal cell cancer (RCC). J Clin Oncol 2018; 36(15s): 4518. doi: 10.1200/JCO.2018.36.15_suppl.4518.
34. Kalbasi A., Ribas A. Tumour-intrinsic resistance to immune checkpoint blockade. Nat Rev Immunol. 2020; 20(1): 25–39. doi: 10.1038/s41577-019-0218-4.
35. Platanias L.C. Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat Rev Immunol. 2005; 5(5): 375–86. doi: 10.1038/nri1604.
36. 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., Saco J., Homet Moreno B., Mezzadra R., Chmielowski B., Ruchalski K., Shintaku I.P., Sanchez P.J., Puig-Saus C., Cherry G., Seja E., Kong X., Pang J., Berent-Maoz B., Comin-Anduix B., Graeber T.G., Tumeh P.C., Schumacher T.N., Lo R.S., Ribas A. Mutations associated with acquired resistance to PD-1 blockade in melanoma. N Engl J Med 2016; 375: 819–29. doi: 10.1056/NEJMoa1604958.
37. Spranger S., Bao R., Gajewski T.F. Melanoma-intrinsic β-catenin signalling prevents anti-tumour immunity. Nature. 2015; 523(7559): 231–5. doi: 10.1038/nature14404.
38. Sweis R.F., Spranger S., Bao R., Paner G.P., Stadler W.M., Steinberg G., Gajewski T.F. Molecular Drivers of the Non-T-cell-Infamed Tumor Microenvironment in Urothelial Bladder Cancer. Cancer Immunol Res. 2016; 4(7): 563–8. doi: 10.1158/2326-6066.CIR-15-0274.
39. Seiwert T.Y., Zuo Z., Keck M.K., Khattri A., Pedamallu C.S., Stricker T., Brown C., Pugh T.J., Stojanov P., Cho J., Lawrence M.S., Getz G., Brägelmann J., DeBoer R., Weichselbaum R.R., Langerman A., Portugal L., Blair E., Stenson K., Lingen M.W., Cohen E.E., Vokes E.E., White K.P., Hammerman P.S. Integrative and comparative genomic analysis of HPV-positive and HPV-negative head and neck squamous cell carcinomas. Clin Cancer Res. 2015; 21(3): 632–41. doi: 10.1158/1078-0432.CCR-13-3310.
40. Jiménez-Sánchez A., Memon D., Pourpe S., Veeraraghavan H., Li Y., Vargas H.A., Gill M.B., Park K.J., Zivanovic O., Konner J., Ricca J., Zamarin D., Walther T., Aghajanian C., Wolchok J.D., Sala E., Merghoub T., Snyder A., Miller M.L. Heterogeneous Tumor-Immune Microenvironments among Diferentially Growing Metastases in an Ovarian Cancer Patient. Cell. 2017; 170(5): 927–38. doi: 10.1016/j.cell.2017.07.025.
41. Boni A., Cogdill A.P., Dang P., Udayakumar D., Njauw C.N., Sloss C.M., Ferrone C.R., Flaherty K.T., Lawrence D.P., Fisher D.E., Tsao H., Wargo J.A. Selective BRAFV600E inhibition enhances T-cell recognition of melanoma without afecting lymphocyte function. Cancer Res. 2010; 70(13): 5213–9. doi: 10.1158/0008-5472.CAN-10-0118.
42. Goel S., DeCristo M.J., Watt A.C., BrinJones H., Sceneay J., Li B.B., Khan N., Ubellacker J.M., Xie S., Metzger-Filho O., Hoog J., Ellis M.J., Ma C.X., Ramm S., Krop I.E., Winer E.P., Roberts T.M., Kim H.J., McAllister S.S., Zhao J.J. CDK4/6 inhibition triggers anti-tumour immunity. Nature. 2017; 548(7668): 471–5. doi: 10.1038/nature23465.
43. Jerby-Arnon L., Shah P., Cuoco M.S., Rodman C., Su M.J., Melms J.C., Leeson R., Kanodia A., Mei S., Lin J.R., Wang S., Rabasha B., Liu D., Zhang G., Margolais C., Ashenberg O., Ott P.A., Buchbinder E.I., Haq R., Hodi F.S., Boland G.M., Sullivan R.J., Frederick D.T., Miao B., Moll T., Flaherty K.T., Herlyn M., Jenkins R.W., Thummalapalli R., Kowalczyk M.S., Cañadas I., Schilling B., Cartwright A.N.R., Luoma A.M., Malu S., Hwu P., Bernatchez C., Forget M.A., Barbie D.A., Shalek A.K., Tirosh I., Sorger P.K., Wucherpfennig K., Van Allen E.M., Schadendorf D., Johnson B.E., Rotem A., Rozenblatt-Rosen O., Garraway L.A., Yoon C.H., Izar B., Regev A. A Cancer Cell Program Promotes T Cell Exclusion and Resistance to Checkpoint Blockade. Cell. 2018; 175(4): 984–97. doi: 10.1016/j.cell.2018.09.006.
44. Wang X., Zhang H., Chen X. Drug resistance and combating drug resistance in cancer. Cancer Drug Resist. 2019; 2(2): 141–60. doi: 10.20517/cdr.2019.10.
45. Sade-Feldman M., Jiao Y.J., Chen J.H., Rooney M.S., BarzilyRokni M., Eliane J.P., Bjorgaard S.L., Hammond M.R., Vitzthum H., Blackmon S.M., Frederick D.T., Hazar-Rethinam M., Nadres B.A., Van Seventer E.E., Shukla S.A., Yizhak K., Ray J.P., Rosebrock D., Livitz D., Adalsteinsson V., Getz G., Duncan L.M., Li B., Corcoran R.B., Lawrence D.P., Stemmer-Rachamimov A., Boland G.M., Landau D.A., Flaherty K.T., Sullivan R.J., Hacohen N. Resistance to checkpoint blockade therapy through inactivation of antigen presentation. Nat Commun. 2017; 8(1): 1136. doi: 10.1038/s41467-017-01062-w.
46. Fridman W.H., Pagès F., Sautès-Fridman C., Galon J. The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer. 2012; 12(4): 298–306. doi: 10.1038/nrc3245.
47. Becht E., Giraldo N.A., Lacroix L., Buttard B., Elarouci N., Petitprez F., Selves J., Laurent-Puig P., Sautès-Fridman C., Fridman W.H., de Reyniès A. Estimating the population abundance of tissue-infltrating immune and stromal cell populations using gene expression. Genome Biol. 2016; 17(1): 218. doi: 10.1186/s13059-016-1070-5. Erratum in: Genome Biol. 2016; 17(1): 249.
48. Giraldo N.A., Becht E., Pagès F., Skliris G., Verkarre V., Vano Y., Mejean A., Saint-Aubert N., Lacroix L., Natario I., Lupo A., Alifano M., Damotte D., Cazes A., Triebel F., Freeman G.J., Dieu-Nosjean M.C., Oudard S., Fridman W.H., Sautès-Fridman C. Orchestration and Prognostic Signifcance of Immune Checkpoints in the Microenvironment of Primary and Metastatic Renal Cell Cancer. Clin Cancer Res. 2015; 21(13): 3031–40. doi: 10.1158/1078-0432.CCR-14-2926.
49. Helmink B.A., Reddy S.M., Gao J., et al. B cells and tertiary lymphoid structures promote immunotherapy response. Nature. 2020; 577(7791): 549–55. doi: 10.1038/s41586-019-1922-8.
50. Petitprez F., de Reyniès A., Keung E.Z., Chen T.W., Sun C.M., Calderaro J., Jeng Y.M., Hsiao L.P., Lacroix L., Bougoüin A., Moreira M., Lacroix G., Natario I., Adam J., Lucchesi C., Laizet Y.H., Toulmonde M., Burgess M.A., Bolejack V., Reinke D., Wani K.M., Wang W.L., Lazar A.J., Roland C.L., Wargo J.A., Italiano A., Sautès-Fridman C., Tawbi H.A., Fridman W.H. B cells are associated with survival and immunotherapy response in sarcoma. Nature. 2020; 577(7791): 556–60. doi: 10.1038/s41586-019-1906-8.
51. Stubbs M., McSheehy P.M., Griffths J.R., Bashford C.L. Causes and consequences of tumour acidity and implications for treatment. Mol Med Today. 2000; 6(1): 15–9. doi: 10.1016/s1357-4310(99)01615-9.
52. Sormendi S., Wielockx B. Hypoxia Pathway Proteins As Central Mediators of Metabolism in the Tumor Cells and Their Microenvironment. Front Immunol. 2018; 9: 40. doi: 10.3389/fmmu.2018.00040.
53. Garcia-Lora A., Algarra I., Garrido F. MHC class I antigens, immune surveillance, and tumor immune escape. J Cell Physiol. 2003; 195(3): 346–55. doi: 10.1002/jcp.10290.
54. Tatli Dogan H., Kiran M., Bilgin B., Kiliçarslan A., Sendur M.A.N., Yalçin B., Ardiçoglu A., Atmaca A.F., Gumuskaya B. Prognostic signifcance of the programmed death ligand 1 expression in clear cell renal cell carcinoma and correlation with the tumor microenvironment and hypoxia-inducible factor expression. Diagn Pathol. 2018; 13(1): 60. doi: 10.1186/s13000-018-0742-8.
55. Zhang J., Shi Z., Xu X., Yu Z., Mi J. The infuence of microenvironment on tumor immunotherapy. FEBS J. 2019; 286(21): 4160–75. doi: 10.1111/febs.15028.
56. Pan D., Kobayashi A., Jiang P., Ferrari de Andrade L., Tay R.E., Luoma A.M., Tsoucas D., Qiu X., Lim K., Rao P., Long H.W., Yuan G.C., Doench J., Brown M., Liu X.S., Wucherpfennig K.W. A major chromatin regulator determines resistance of tumor cells to T cell-mediated killing. Science. 2018; 359(6377): 770–5. doi: 10.1126/science.aao1710.
57. Varela I., Tarpey P., Raine K., Huang D., Ong C.K., Stephens P., Davies H., Jones D., Lin M.L., Teague J., Bignell G., Butler A., Cho J., Dalgliesh G.L., Galappaththige D., Greenman C., Hardy C., Jia M., Latimer C., Lau K.W., Marshall J., McLaren S., Menzies A., Mudie L., Stebbings L., Largaespada D.A., Wessels L.F., Richard S., Kahnoski R.J., Anema J., Tuveson D.A., Perez-Mancera P.A., Mustonen V., Fischer A., Adams D.J., Rust A., Chan-on W., Subimerb C., Dykema K., Furge K., Campbell P.J., Teh B.T., Stratton M.R., Futreal P.A. Exome sequencing identifes frequent mutation of the SWI/SNF complex gene PBRM1 in renal carcinoma. Nature. 2011; 469(7331): 539–42. doi: 10.1038/nature09639. Erratum in: Nature. 2012; 484(7392): 130.
58. Miao D., Margolis C.A., Gao W., Voss M.H., Li W., Martini D.J., Norton C., Bossé D., Wankowicz S.M., Cullen D., Horak C., Wind-Rotolo M., Tracy A., Giannakis M., Hodi F.S., Drake C.G., Ball M.W., Allaf M.E., Snyder A., Hellmann M.D., Ho T., Motzer R.J., Signoretti S., Kaelin W.G., Choueiri T.K., van Allen E.M. Genomic correlates of response to immune checkpoint therapies in clear cell renal cell carcinoma. Science. 2018; 359(6377): 801–6. doi: 10.1126/science.aan5951.
59. Braun D.A., Ishii Y., Walsh A.M., Van Allen E.M., Wu C.J., Shukla S.A., Choueiri T.K. Clinical Validation of PBRM1 Alterations as a Marker of Immune Checkpoint Inhibitor Response in Renal Cell Carcinoma. JAMA Oncol. 2019; 5(11): 1631–3. doi: 10.1001/jamaoncol.2019.3158.
Review
For citations:
Izmailov A.A., Rakhimov R.R., Sultanbayev A.V., Menshikov K.V., Gilyazova I.R., Zabelin V.M., Izmailov A.A. Resistance to immune checkpoint inhibitors in the treatment of metastatic renal cancer. Siberian journal of oncology. 2023;22(4):109-117. (In Russ.) https://doi.org/10.21294/1814-4861-2023-22-4-109-117