Иммунологическая толерантность при раке молочной железы: некоторые причины развития
https://doi.org/10.17650/2313-805X-2024-11-3-24-31
Аннотация
Иммунологическая толерантность является одной из причин возникновения и прогрессирования злокачественных опухолей. Противоопухолевый иммунный цикл регулирует нормальный противоопухолевый иммунный ответ, а его нарушение вызывает развитие иммунологической толерантности. В статье представлен обзор отечественной и зарубежной литературы, опубликованной за последние 5 лет в базах PubMed, Medline, Cochrane, eLibrary и посвященой вопросам возникновения иммунологической толерантности при раке молочной железы с позиции нарушения регуляции фаз противоопухолевого иммунного цикла. В настоящее время выделяют следующие этапы противоопухолевого иммунного цикла: экспрессия антигенов на поверхности опухолевых клеток, созревание антигенпрезентирующих клеток и распознавание опухолевых антигенов, праймирование и активация Т-клеток, иммунная инфильтрация опухолевого очага, распознавание и уничтожение опухолевых клеток. Понимание механизмов, лежащих в основе противоопухолевого иммунного цикла, важно для выявления новых иммунопатогенетических звеньев развития рака молочной железы и таргетируемых мишеней с целью улучшения эффективности терапии распространенного рака молочной железы.
Об авторах
Е. В. КаюковаРоссия
672000 Чита, ул. Горького, 39А
Э. С. Болотов
Россия
Элбэк Саянович Болотов
672000 Чита, ул. Горького, 39А
Список литературы
1. Ghorani E., Swanton C., Quezada S.A. Cancer cell-intrinsic mechanisms driving acquired immune tolerance. Immunity 2023;56(10):2270–95. DOI: 10.1016/j.immuni.2023.09.004
2. Schreiber R.D., Old L.J., Smyth M.J. Cancer immunoediting: integrating immunity’s roles in cancer suppression and promotion. Science 2011;331(6024):1565–70. DOI: 10.1126/science.1203486
3. Chen D.S., Mellman I. Oncology meets immunology: the cancerimmunity cycle. Immunity 2013;39(1):1–10. DOI: 10.1016/j.immuni.2013.07.012
4. Li M., Gao X., Wang X. Identification of tumor mutation burdenassociated molecular and clinical features in cancer by analyzing multi-omics data. Front Immunol 2023;14:1090838. DOI: 10.3389/fimmu.2023.1090838
5. Kikuchi T., Mimura K., Okayama H. et al. A subset of patients with MSS/MSI-low-colorectal cancer showed increased CD8(+) TILs together with up-regulated IFN-γ. Oncol Lett 2019;18(6):5977–85. DOI: 10.3892/ol.2019.10953
6. Liu K., Mao X., Li T. et al. Immunotherapy and immunobiomarker in breast cancer: current practice and future perspectives. Am J Cancer Res 2022;12(8):3532–47.
7. Barroso-Sousa R., Pacífico J.P., Sammons S., Tolaney S.M. Tumor mutational burden in breast cancer: current evidence, challenges, and opportunities. Cancers (Basel) 2023;15(15):3997. DOI: 10.3390/cancers15153997
8. Schmid P., Rugo H.S., Adams S. et al. Atezolizumab plus nabpaclitaxel as first-line treatment for unresectable, locally advanced or metastatic triple-negative breast cancer (IMpassion130): updated efficacy results from a randomised, double-blind, placebocontrolled, phase 3 trial. Lancet Oncol 2020;21(1):44–59. DOI: 10.1016/S1470-2045(19)30689-8
9. Emens L.A., Molinero L., Adams S. et al. Tumour mutational burden and clinical outcomes with first-line atezolizumab and nab-paclitaxel in triple negative breast cancer: exploratory analysis of the phase III Impassion130 trial. Ann Oncol 2020;31:360–1. DOI: 10.1016/j.annonc.2020.08.398
10. Karn T., Denkert C., Weber K.E. et al. Tumor mutational burden and immune infiltration as independent predictors of response to neoadjuvant immune checkpoint inhibition in early TNBC in GeparNuevo. Ann Oncol 2020;31(9):1216–22. DOI: 10.1016/j.annonc.2020.05.015
11. Park S.E., Park K., Lee E. et al. Clinical implication of tumor mutational burden in patients with HER2-positive refractory metastatic breast cancer. Oncoimmunology 2018;7(8):e1466768. DOI: 10.1080/2162402X.2018.1466768
12. Narang P., Chen M., Sharma A.A. et al. The neoepitope landscape of breast cancer: implications for immunotherapy. BMC Cancer 2019;19(1):200. DOI: 10.1186/s12885-019-5402-1
13. Schaafsma E., Fugle C.M., Wang X., Cheng C. Pan-cancer association of HLA gene expression with cancer prognosis and immunotherapy efficacy. Br J Cancer 2021;125(3):422–32. DOI: 10.1038/s41416-021-01400-2
14. Degenhardt F., Wendorff M., Wittig M. et al. Construction and benchmarking of a multi-ethnic reference panel for the imputation of HLA class I and II alleles. Hum Mol Genet 2019;28(12):2078–92. DOI: 10.1093/hmg/ddy443
15. da Silva G.B., Silva T.G., Duarte R.A. et al. Expression of the classical and nonclassical HLA molecules in breast cancer. Int J Breast Cancer 2013;2013:250435. DOI: 10.1155/2013/250435
16. Чулкова С.В., Шолохова Е.Н., Поддубная И.В. и др. HLA-мономорфные детерминанты первичной опухоли у больных ра- ком молочной железы. Российский биотерапевтический журнал 2022;21(2):56–66. DOI: 10.17650/1726-9784-2022-21-2-56-66
17. Li K., Du H., Lian X. et al. Characterization of β2-microglobulin expression in different types of breast cancer. BMC Cancer 2014;14:750. DOI: 10.1186/1471-2407-14-750
18. Zheng G., Jia L., Yang A.G. Roles of HLA-G/KIR2DL4 in breast cancer immune microenvironment. Front Immunol 2022;13:791975. DOI: 10.3389/fimmu.2022.791975
19. Mohanty R., Chowdhury C.R., Arega S. et al. CAR T cell therapy: a new era for cancer treatment (Review). Oncol Rep 2019;42(6):2183–95. DOI: 10.3892/or.2019.7335
20. Zagorulya M., Yim L., Morgan D.M. et al. Tissue-specific abundance of interferon-gamma drives regulatory T cells to restrain DC1-mediated priming of cytotoxic T cells against lung cancer. Immunity 2023;56(2):386–405.e10. DOI: 10.1016/j.immuni.2023.01.010
21. Manuel M., Tredan O., Bachelot T. et al. Lymphopenia combined with low TCR diversity (divpenia) predicts poor overall survival in metastatic breast cancer patients. Oncoimmunology 2012;1(4):432–40. DOI: 10.4161/onci.19545
22. Chandran S.S., Klebanoff C.A. T cell receptor-based cancer immunotherapy: Emerging efficacy and pathways of resistance. Immunol Rev 2019;290(1):127–47. DOI: 10.1111/imr.12772
23. Azizi D., Carr A.J., Plitas G. et al. Single-cell map of diverse immune phenotypes in the breast tumor microenvironment. Cell 2018;174(5):1293–1308.e36. DOI: 10.1016/j.cell.2018.05.060.
24. Liu X., Si F., Bagley D. et al. Blockades of effector T cell senescence and exhaustion synergistically enhance antitumor immunity and immunotherapy. J Immunother Cancer 2022;10(10):e005020. DOI: 10.1136/jitc-2022-005020
25. Каюкова Е.В., Белокриницкая Т.Е., Мудров В.А. Молекулярные показатели клеток шейки матки в качестве диагностических маркеров цервикальной интраэпителиальной неоплазии третьей степени. Эффективная фармакотерапия 2022;18 (21): 14–9.
26. Li J., Wu J., Han J. et al. Analysis of tumor microenvironment heterogeneity among breast cancer subtypes to identify subtypespecific signatures. Genes (Basel) 2022;14(1):44. DOI: 10.3390/genes14010044
27. Onkar S., Cui J., Zou J. et al. Immune landscape in invasive ductal and lobular breast cancer reveals a divergent macrophage-driven microenvironment. Nat Cancer 2023;4(4):516–34. DOI: 10.1038/s43018-023-00527-w
28. Mittal S., Brown N.J., Holen I. et al. The breast tumor microenvironment: role in cancer development, progression and response to therapy. Expert Rev Mol Diagn 2018;18(3):227–43. DOI: 10.1080/14737159.2018.1439382
29. Yuan X., Wang J., Huang Y. et al. Single-cell profiling to explore immunological heterogeneity of tumor microenvironment in breast cancer. Front Immunol 2021;12:643692. DOI: 10.3389/fimmu.2021.643692
30. So J.Y., Ohm J., Lipkowitz S., Yang L. Triple negative breast cancer (TNBC): non-genetic tumor heterogeneity and immune microenvironment: emerging treatment options. Pharmacol Ther 2022;237:108253. DOI: 10.1016/j.pharmthera.2022.108253
31. Loi S., Michiels S., Adams S. et al. The journey of tumor-infiltrating lymphocytes as a biomarker in breast cancer: clinical utility in an era of checkpoint inhibition. Ann Oncol 2021;32(10):1236–44. DOI: 10.1016/j.annonc.2021.07.007
32. Jiang P., Gao W., Ma T. et al. CD137 promotes bone metastasis of breast cancer by enhancing the migration and osteoclast differentiation of monocytes/macrophages. Theranostics 2019;9(10):2950–66. DOI: 10.7150/thno.29617
33. Chester C., Sanmamed M.F., Wang J., Melero I. Immunotherapy targeting 4-1BB: mechanistic rationale, clinical results, and future strategies. Blood 2018;131(1):49–57. DOI: 10.1182/blood-2017-06-741041
34. Kohrt H.E., Houot R., Weiskopf K. et al. Stimulation of natural killer cells with a CD137-specific antibody enhances trastuzumab efficacy in xenotransplant models of breast cancer. J Clin Invest 2019;129(6):2595. DOI: 10.1172/JCI129688
35. Fang J., Chen F., Liu D. et al. Prognostic value of immune checkpoint molecules in breast cancer. Biosci Rep 2020;40(7):BSR20201054. DOI: 10.1042/BSR20201054
36. Yan C., Richmond A. Hiding in the dark: pan-cancer characterization of expression and clinical relevance of CD40 to immune checkpoint blockade therapy. Mol Cancer 2021;20(1):146. DOI: 10.1186/s12943-021-01442-3
37. Petrau C., Cornic M., Bertrand P. et al. CD70: a potential target in breast cancer? J Cancer 2014;5(9):761–4. DOI: 10.7150/jca.10360
38. Rhee D.K., Park S.H., Jang Y.K. Molecular signatures associated with transformation and progression to breast cancer in the isogenic MCF10 model. Genomics 2008;92(6):419–28. DOI: 10.1016/j.ygeno.2008.08.005
39. Teillaud J.L. L’immunothérapie des cancers couronnée avec l’attribution du prix Nobel de Physiologie ou Médecine à James Allison et Tasuku Honjo [Cancer immunotherapy crowned with Nobel Prize in Physiology or Medicine awarded to James Allison and Tasuku Honjo]. Med Sci (Paris) 2019;35(4):365–6. DOI: 10.1051/medsci/2019073
40. Ai L., Xu A., Xu J. Roles of PD-1/PD-L1 Pathway: Signaling, Cancer, and Beyond. Adv Exp Med Biol 2020;1248:33–59. PMID: 32185706. DOI: 10.1007/978-981-15-3266-5_3
41. Schütz F., Stefanovic S., Mayer L. et al. PD-1/PD-L1 pathway in breast cancer. Oncol Res Treat 2017;40(5):294–7. DOI: 10.1159/000464353
42. Sun W.Y., Lee Y.K., Koo J.S. Expression of PD-L1 in triple-negative breast cancer based on different immunohistochemical antibodies. J Transl Med 2016;14(1):173. DOI: 10.1186/s12967-016-0925-6
43. Vranic S., Cyprian F.S., Gatalica Z., Palazzo J. PD-L1 status in breast cancer: Current view and perspectives. Semin Cancer Biol 2021;72:146–54. PMID: 31883913. DOI: 10.1016/j.semcancer.2019.12.003
44. Zhang H., Mi J., Xin Q. et al. Recent research and clinical progress of CTLA-4-based immunotherapy for breast cancer. Front Oncol 2023;4;13:1256360. PMID: 37860188. DOI: 10.3389/fonc.2023.1256360.
45. Triebel F., Jitsukawa S., Baixeras E. et al. LAG-3, a novel lymphocyte activation gene closely related to CD4. J Exp Med 1990;171(5):1393–405. DOI: 10.1084/jem.171.5.1393
46. Chocarro L., Blanco E., Zuazo M. et al. Understanding LAG-3 signaling. Int J Mol Sci 2021;22(10):5282. DOI: 10.3390/ijms22105282
47. Liu Q., Qi Y., Zhai J. et al. Molecular and clinical characterization of LAG3 in breast cancer through 2994 samples. Front Immunol 2021;12:599207. DOI: 10.3389/fimmu.2021.599207
48. Burugu S., Gao D., Leung S. et al. LAG-3+ tumor infiltrating lymphocytes in breast cancer: clinical correlates and association with PD-1/PD-L1+ tumors. Ann Oncol 2017;28(12):2977–84. DOI: 10.1093/annonc/mdx557
49. Zeidan A.M., Komrokji R.S., Brunner A.M. TIM-3 pathway dysregulation and targeting in cancer. Expert Rev Anticancer Ther 2021;21(5):523–34. DOI: 10.1080/14737140.2021.1865814
50. Yasinska I.M., Sakhnevych S.S., Pavlova L. et al. The Tim-3-Galectin-9 pathway and its regulatory mechanisms in human breast cancer. Front Immunol 2019;10:1594. DOI: 10.3389/fimmu.2019.01594
51. Solinas C., Garaud S., De Silva P. et al. Immune checkpoint molecules on tumor-infiltrating lymphocytes and their association with tertiary lymphoid structures in human breast cancer. Front Immunol 2017;8:1412. DOI: 10.3389/fimmu.2017.01412
52. Cong Y., Liu J., Chen G., Qiao G. The emerging role of T-CELL immunoglobulin mucin-3 in breast cancer: a promising target for immunotherapy. Front Oncol 2021;11:723238. DOI: 10.3389/fonc.2021.723238
53. Tu L., Guan R., Yang H. et al. Assessment of the expression of the immune checkpoint molecules PD-1, CTLA4, TIM-3 and LAG-3 across different cancers in relation to treatment response, tumor-infiltrating immune cells and survival. Int J Cancer 2020;147(2):423–39. DOI: 10.1002/ijc.32785
54. Burugu S., Gao D., Leung S. et al. TIM-3 expression in breast cancer. Oncoimmunology 2018;7(11):e1502128. DOI: 10.1080/2162402X.2018.1502128
55. Ашрафян Л.А., Белокриницкая Т.Е., Каюкова Е.В. и др. Локальный уровень белков контрольных точек иммунного цикла у больных раком шейки матки. Забайкальский медицинский вестник 2021;4:11–20.
56. Peyraud F., Guegan J.P., Bodet D. et al. Targeting tryptophan catabolism in the era of cancer immunotherapy: challenges and perspectives. Front Immunol 2022;13:807271. DOI: 10.3389/fimmu.2022.807271
57. León-Letelier R.A., Dou R., Vykoukal J. et al. The kynurenine pathway presents multi-faceted metabolic vulnerabilities in cancer. Front Oncol 2023;13:1256769. DOI: 10.3389/fonc.2023.1256769
58. Soliman H., Rawal B., Fulp J. et al. Analysis of indoleamine 2-3 dioxygenase (IDO1) expression in breast cancer tissue by immunohistochemistry. Cancer Immunol Immunother 2013;62(5):829–37. DOI: 10.1007/s00262-013-1393-y
59. Isla Larrain M.T., Rabassa M.E., Lacunza E. et al. IDO is highly expressed in breast cancer and breast cancer-derived circulating microvesicles and associated to aggressive types of tumors by in silico analysis. Tumour Biol 2014;35(7):6511–9. DOI: 10.1007/s13277-014-1859-3
60. Alkhayyal N., Elemam N.M., Hussein A. et al. Expression of immune checkpoints (PD-L1 and IDO) and tumour-infiltrating lymphocytes in breast cancer. Heliyon 2022;8(9):e10482. DOI: 10.1016/j.heliyon.2022.e10482
Рецензия
Для цитирования:
Каюкова Е.В., Болотов Э.С. Иммунологическая толерантность при раке молочной железы: некоторые причины развития. Успехи молекулярной онкологии. 2024;11(3):24-31. https://doi.org/10.17650/2313-805X-2024-11-3-24-31
For citation:
Kayukova E.V., Bolotov E.S. Immunological tolerance in breast cancer: some reasons for development. Advances in Molecular Oncology. 2024;11(3):24-31. (In Russ.) https://doi.org/10.17650/2313-805X-2024-11-3-24-31