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Взаимосвязь молекул главного комплекса гистосовместимости HLA-I и II классов с клиникоморфологическими признаками рака молочной железы
Взаимосвязь молекул главного комплекса гистосовместимости HLA-I и II классов с клиникоморфологическими признаками рака молочной железы
Чулкова С.В., Шолохова Е.Н., Поддубная И.В., Стилиди И.С., Буров Д.А., Тупицын Н.Н. Взаимосвязь молекул главного комплекса гистосовместимости HLA-I и II классов с клинико-морфологическими признаками рака молочной железы. Современная Онкология. 2023;25(2):208–213.
DOI: 10.26442/18151434.2023.2.202082
© ООО «КОНСИЛИУМ МЕДИКУМ», 2023 г.
DOI: 10.26442/18151434.2023.2.202082
© ООО «КОНСИЛИУМ МЕДИКУМ», 2023 г.
________________________________________________
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Аннотация
Обоснование. Длительное время не ослабевает интерес к HLA-пептидному комплексу, клиническое значение которого при раке по сей день является предметом напряженных дискуссий. Через презентацию HLA-антигенов опухолевые клетки становятся доступными для распознавания и уничтожения эффекторными клетками иммунной системы. Детальный анализ экспрессии молекул HLA клетками рака молочной железы представляет собой и научную, и важную практическую ценность, поскольку может привнести дополнительную информацию об иммунной системе для определения дальнейшей стратегии лечения больных раком молочной железы.
Цель. Оценить экспрессию молекул HLA I и II класса клетками рака молочной железы и определить их взаимосвязи с морфологическими и клиническими характеристиками опухоли.
Материалы и методы. В данную работу включены 82 больные раком молочной железы, которые получали лечение в ФГБУ «НМИЦ онкологии им. Н.Н. Блохина». Иммунофенотипирование первичной опухоли выполнено иммуногистохимическим методом (иммунофлуоресцентного окрашивания) на криостатных срезах. Оценка реакции проводилась с помощью люминесцентного микроскопа ZEISS (AXIOSKOP, Германия). Изучена частота экспрессии молекул HLA I и II класса в зависимости от клинических и морфологических характеристик рака молочной железы.
Результаты. Частота экспрессии молекул HLA I и II класса клетками рака молочной железы различалась. Антигены HLA I класса экспрессированы почти в 1/2 случаев (54,5%), тогда как антигены HLA II класса – в 22,0%. Выявлены ассоциации молекул главного комплекса гистосовместимости с клинико-морфологическими признаками рака молочной железы. С увеличением стадии возрастает частота HLA-DR-негативных случаев (p=0,029). Частота мономорфной экспрессии HLA II класса при размерах опухоли, соответствующих Т1, составила 50% против 0% при Т4 (p=0,032). Отрицательные по рецепторам эстрогенов опухоли молочной железы в большинстве случаев не экспрессировали HLA II класса (85,2% против 64%; p=0,034). Не установлено связи с другими клинико-морфологическими признаками опухоли.
Заключение. В большинстве случаев рака молочной железы отсутствует экспрессия молекул HLA II класса при сохранной экспрессии HLA I класса в 1/2 случаев. Мономорфная экспрессия HLA II класса характерна для раннего этапа развития рака молочной железы и преимущественно для рецептор-положительных опухолей.
Ключевые слова: HLA-I, HLA-DR, рак молочной железы, иммунофенотипирование, иммунофлуоресценция, криостатные срезы
system. A detailed analysis of the expression status of HLA molecules by breast cancer cells is of both scientific and important practical value. It can provide additional information about the immune system to determine a further strategy for treating breast cancer.
Aim. To evaluate the frequency of expression of HLA-I and class II molecules by breast cancer cells and to determine its relationship with the morphological and clinical characteristics of the tumor.
Materials and methods. This study included 82 patients with breast cancer who received treatment at the Blokhin National Medical Research Center of Oncology. Immunophenotyping of the primary tumor was performed by the immunohistochemical method (immunofluorescent staining) on cryostat sections. The reaction was evaluated using a ZEISS luminescent microscope (AXIOSKOP, Germany). The frequency of expression of HLA-I and class II molecules was studied depending on the clinical and morphological characteristics of breast cancer.
Results. It was found that the frequency of expression of HLA I and II class molecules by breast cancer cells differed. HLA class I antigens are preserved in almost half of the cases 54.5%, while HLA class II antigens are preserved in 22.0%. Associations of molecules of the major histocompatibility
complex with clinical and morphological signs of breast cancer were revealed. The frequency of HLA-DR negative cases increases in the stage advanсed (p=0.029). The frequency of monomorphic expression of HLA class II with T1 tumor was 50% versus 0% at T4 tumor (p=0.032). Estrogen
receptor-negative tumors in most cases did not express HLA-II class (85.2% vs 64%; p=0.034). No connection with other clinical and morphological features of the tumor has been established.
Conclusion. In most cases of breast cancer, the expression of HLA class II molecules is lost, while the expression of HLA class I is preserved in half of the cases. Monomorphic expression of HLA class II is characteristic of the early stage of breast cancer development and predominantly of receptor-positive tumors.
Keywords: HLA-I, HLA-DR, breast cancer, immunophenotyping, immunofluorescence, cryostat sections
Цель. Оценить экспрессию молекул HLA I и II класса клетками рака молочной железы и определить их взаимосвязи с морфологическими и клиническими характеристиками опухоли.
Материалы и методы. В данную работу включены 82 больные раком молочной железы, которые получали лечение в ФГБУ «НМИЦ онкологии им. Н.Н. Блохина». Иммунофенотипирование первичной опухоли выполнено иммуногистохимическим методом (иммунофлуоресцентного окрашивания) на криостатных срезах. Оценка реакции проводилась с помощью люминесцентного микроскопа ZEISS (AXIOSKOP, Германия). Изучена частота экспрессии молекул HLA I и II класса в зависимости от клинических и морфологических характеристик рака молочной железы.
Результаты. Частота экспрессии молекул HLA I и II класса клетками рака молочной железы различалась. Антигены HLA I класса экспрессированы почти в 1/2 случаев (54,5%), тогда как антигены HLA II класса – в 22,0%. Выявлены ассоциации молекул главного комплекса гистосовместимости с клинико-морфологическими признаками рака молочной железы. С увеличением стадии возрастает частота HLA-DR-негативных случаев (p=0,029). Частота мономорфной экспрессии HLA II класса при размерах опухоли, соответствующих Т1, составила 50% против 0% при Т4 (p=0,032). Отрицательные по рецепторам эстрогенов опухоли молочной железы в большинстве случаев не экспрессировали HLA II класса (85,2% против 64%; p=0,034). Не установлено связи с другими клинико-морфологическими признаками опухоли.
Заключение. В большинстве случаев рака молочной железы отсутствует экспрессия молекул HLA II класса при сохранной экспрессии HLA I класса в 1/2 случаев. Мономорфная экспрессия HLA II класса характерна для раннего этапа развития рака молочной железы и преимущественно для рецептор-положительных опухолей.
Ключевые слова: HLA-I, HLA-DR, рак молочной железы, иммунофенотипирование, иммунофлуоресценция, криостатные срезы
________________________________________________
system. A detailed analysis of the expression status of HLA molecules by breast cancer cells is of both scientific and important practical value. It can provide additional information about the immune system to determine a further strategy for treating breast cancer.
Aim. To evaluate the frequency of expression of HLA-I and class II molecules by breast cancer cells and to determine its relationship with the morphological and clinical characteristics of the tumor.
Materials and methods. This study included 82 patients with breast cancer who received treatment at the Blokhin National Medical Research Center of Oncology. Immunophenotyping of the primary tumor was performed by the immunohistochemical method (immunofluorescent staining) on cryostat sections. The reaction was evaluated using a ZEISS luminescent microscope (AXIOSKOP, Germany). The frequency of expression of HLA-I and class II molecules was studied depending on the clinical and morphological characteristics of breast cancer.
Results. It was found that the frequency of expression of HLA I and II class molecules by breast cancer cells differed. HLA class I antigens are preserved in almost half of the cases 54.5%, while HLA class II antigens are preserved in 22.0%. Associations of molecules of the major histocompatibility
complex with clinical and morphological signs of breast cancer were revealed. The frequency of HLA-DR negative cases increases in the stage advanсed (p=0.029). The frequency of monomorphic expression of HLA class II with T1 tumor was 50% versus 0% at T4 tumor (p=0.032). Estrogen
receptor-negative tumors in most cases did not express HLA-II class (85.2% vs 64%; p=0.034). No connection with other clinical and morphological features of the tumor has been established.
Conclusion. In most cases of breast cancer, the expression of HLA class II molecules is lost, while the expression of HLA class I is preserved in half of the cases. Monomorphic expression of HLA class II is characteristic of the early stage of breast cancer development and predominantly of receptor-positive tumors.
Keywords: HLA-I, HLA-DR, breast cancer, immunophenotyping, immunofluorescence, cryostat sections
Полный текст
Список литературы
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31. Yan M, Jene N, Byrne D, et al. Recruitment of regulatory T cells is correlated with hypoxia-induced CXCR4 expression, and is associated with poor prognosis in basal-like breast cancers. Breast Cancer Res. 2011;13:R47.
32. Olkhanud PB, Damdinsuren B, Bodogai M, et al. Tumor-evoked regulatory B cells promote breast cancer metastasis by converting resting CD4(+) T cells to T-regulatory cells. Cancer Res. 2011;71:3505-15.
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2. McCormack V, McKenzie F, Foerster M, et al. Breast cancer survival and survival gap apportionment in sub-Saharan Africa (ABC-DO): a prospective cohort study. The Lancet Global Health. 2020;8(9):e1203-12. Available at: http://www.ncbi.nlm.nih.gov/pubmed/32827482. Accessed: 01.12.2021.
3. Titov KS, Kazakov AM, Baryshnikova MA, et al. Nekotorye molekulyarnye i immunologicheskie faktory prognoza trizhdy negativnogo raka molochnoi zhelezy. Onkoginekologiya. 2019;4(32):26-34 (in Russian)].
4. Mutebi M, Anderson BO, Duggan C, et al. Breast cancer treatment: A phased approach to implementation. Cancer. 2020;126(Suppl.10):236578. Available at: http://www.ncbi.nlm.nih.gov/pubmed/32348571. Accessed: 01.12.2021.
5. Ryabchikov DA, Abdullaeva EI, Dudina IA, et al. Rol' mikro-RNK v kantserogeneze i prognoze zlokachestvennykh novoobrazovanii molochnoi zhelezy. Vestnik Rossiiskogo nauchnogo tsentra rentgenoradiologii. 2018;18(2):5 (in Russian).
6. Sabbatino F, Liguori L, Polcaro G, et al. Role of Human Leukocyte Antigen System as A Predictive Biomarker for Checkpoint-Based Immunotherapy in Cancer Patients. Int J Mol Sci. 2020;21:7295. DOI:10.3390/ijms21197295
7. Shukla A, Cloutier M, Santharam AM, et al. The MHC Class-I Transactivator NLRC5: Implications to Cancer Immunology and Potential Applications to Cancer Immunotherapy. Int J Mol Sci. 2021;22(4):1964. DOI:10.3390/ijms22041964
8. Trowsdale J, Knight JC. Major histocompatibility complex genomics and human disease. Annu Rev Genom Hum Genet. 2013;14:301-23.
9. Trowsdale J. Genomic structure and function in the MHC. Trends Genet. 1993;9:117-22.
10. Norman PJ, Norberg SJ, Guethlein LA, et al. Sequences of 95 human MHC haplotypes reveal extreme coding variation in genes other than highly polymorphic HLA class I and II. Genome Res. 2017;27:813-23.
11. Horton R, Wilming L, Rand V, et al. Gene map of the extended human MHC. Nat Rev Genet. 2004;5:889-99.
12. Neefjes J, Jongsma MLM, Paul P, Bakke O. Towards a systems understanding of MHC class I and MHC class II antigen presentation. Nat Rev Immunol. 2011;11:823-36.
13. Rock KL, Reits E, Neefjes J. Present Yourself! By MHCClass I and MHCClass II Molecules. Trends Immunol. 2016;37:724-37.
14. Holling TM, Schooten E, Van Den Elsen PJ. Function and regulation of MHC class II molecules in T-lymphocytes: Of mice and men. Hum Immunol. 2004;65:282-90.
15. Blum JS, Wearsch PA, Cresswell P. Pathways of antigen processing. Annu Rev Immunol. 2013;31:443-73.
16. Farhood B, Najafi M, Mortezaee K. CD8+ cytotoxic T lymphocytes in cancer immunotherapy: A review. J Cell Physiol. 2019;234:8509-21.
17. Cruz FM, Colbert JD, Merino E, et al. The Biology and Underlying Mechanisms of Cross-Presentation of Exogenous Antigens on MHC-I Molecules. Annu Rev Immunol.
2017;35:149-76.
18. Leone P, Shin EC, Perosa F, et al. MHC class I antigen processing and presenting machinery: Organization, function, and defects in tumor cells. J Natl Cancer Inst. 2013;105:1172-87.
19. Thielens A, Vivier E, Romagné F. NK cell MHC class I specific receptors (KIR): From biology to clinical intervention. Curr Opin Immunol. 2012;24:239-45.
20. Cabrera T, Maleno I, Collado A, et al. Analysis of HLA class I alterations in tumors: Choosing a strategy based on known patterns of underlying molecular mechanisms. Tissue Antigens. 2007;69 (Suppl. S1):264-8.
21. Cai L, Michelakos T, Yamada T, et al. Defective HLAclass I antigen processing machinery in cancer. Cancer Immunol Immunother. 2018;67:999-1009.
22. Garrido F, Algarra I. MHC antigens and tumor escape from immune surveillance. Adv Cancer Res. 2001;83:117-58.
23. Martin HP, Brian LH, Hans ChB, et al. Downregulation of antigen presentation-associated pathway proteins is linked to poor outcome in triple-negative breast cancer patient tumors. OncoImmunology. 2017;6(5):e1305531. DOI:10.1080/2162402X.2017.1305531
24. Sinn BV, Weber KE, Schmitt WD, et al. Human leucocyte antigen class I in hormone receptor-positive, HER2-negative breast cancer: association with response and survival after neoadjuvant chemotherapy. Breast Cancer Res. 2019;21:142. DOI:10.1186/s13058-019-1231-z
25. Artamonova EV. Rol' immunofenotipirovaniia v diagnostike i prognoze raka molochnoi zhelezy. Immunologiia gemopoeza. 2009;1(9):8-52 (in Russian).
26. Burov DA, Beznos OA, Vorotnikov IK, et al. Klinicheskoie znacheniie ekspressii molekul gistosovmestimosti na kletkakh raka molochnoi zhelezy. Immunologiia gemopoeza. 2016;2(14):33-53 (in Russian).
27. Berishvili AI, Tupitsyn NN, Laktionov KP. Immunophenotypic characteristics of inflammatory breast cancer. Tumors of Female Reproductive System. 2009;3-4:15-9 (in Russian).
28. Engay DA. Immunologicheskaia kharakteristika Pgp170 pozitivnogo raka molochnoi zhelezy: dis. … kand. med. nauk. Moscow, 2008 (in Russian).
29. Rodriguez JA. HLA-mediated tumor escape mechanisms that may impair immunotherapy clinical outcomes via T-cell activation. Oncol Lett. 2017;14:4415-27.
30. Haen SP, Loffler MW, Rammensee HG, Brossart P. Towards new horizons: Characterization, classification and implications of the tumour antigenic repertoire. Nat Rev Clin Oncol. 2020;17:595-610.
31. Yan M, Jene N, Byrne D, et al. Recruitment of regulatory T cells is correlated with hypoxia-induced CXCR4 expression, and is associated with poor prognosis in basal-like breast cancers. Breast Cancer Res. 2011;13:R47.
32. Olkhanud PB, Damdinsuren B, Bodogai M, et al. Tumor-evoked regulatory B cells promote breast cancer metastasis by converting resting CD4(+) T cells to T-regulatory cells. Cancer Res. 2011;71:3505-15.
33. Munir MT, Kay MK, Kang MH, et al. Tumor-Associated Macrophages asMultifaceted Regulators of Breast Tumor Growth. Int J Mol Sci. 2021;22:6526.
34. Lim B, Woodward WA, Wang X, et al. Inflammatory breast cancer biology: The tumour microenvironment is key. Nat Rev Cancer. 2018;18:485-99.
35. Burugu S, Asleh-Aburaya K, Nielsen TO. Immune infiltrates in the breast cancer microenvironment: Detection, characterization and clinical implication. Breast Cancer. 2017;24:3-15.
2. McCormack V, McKenzie F, Foerster M, et al. Breast cancer survival and survival gap apportionment in sub-Saharan Africa (ABC-DO): a prospective cohort study. The Lancet Global Health. 2020;8(9):e1203-12. Available at: http://www.ncbi.nlm.nih.gov/pubmed/32827482. Accessed: 01.12.2021.
3. Титов К.С., Казаков А.М., Барышникова М.А., и др. Некоторые молекулярные и иммунологические факторы прогноза трижды негативного рака молочной железы. Онкогинекология. 2019;4(32):26-34 [Titov KS, Kazakov AM, Baryshnikova MA, et al. Nekotorye molekulyarnye i immunologicheskie faktory prognoza trizhdy negativnogo raka molochnoi zhelezy. Onkoginekologiya. 2019;4(32):26-34 (in Russian)].
4. Mutebi M, Anderson BO, Duggan C, et al. Breast cancer treatment: A phased approach to implementation. Cancer. 2020;126(Suppl.10):236578. Available at: http://www.ncbi.nlm.nih.gov/pubmed/32348571. Accessed: 01.12.2021.
5. Рябчиков Д.А., Абдуллаева Э.И., Дудина И.А., и др. Роль микро-РНК в канцерогенезе и прогнозе злокачественных новообразований молочной железы. Вестник Российского научного центра рентгенорадиологии. 2018;18(2):5 [Ryabchikov DA, Abdullaeva EI, Dudina IA, et al. Rol' mikro-RNK v kantserogeneze i prognoze zlokachestvennykh novoobrazovanii molochnoi zhelezy. Vestnik Rossiiskogo nauchnogo tsentra rentgenoradiologii. 2018;18(2):5 (in Russian)].
6. Sabbatino F, Liguori L, Polcaro G, et al. Role of Human Leukocyte Antigen System as A Predictive Biomarker for Checkpoint-Based Immunotherapy in Cancer Patients. Int J Mol Sci. 2020;21:7295. DOI:10.3390/ijms21197295
7. Shukla A, Cloutier M, Santharam AM, et al. The MHC Class-I Transactivator NLRC5: Implications to Cancer Immunology and Potential Applications to Cancer Immunotherapy. Int J Mol Sci. 2021;22(4):1964. DOI:10.3390/ijms22041964
8. Trowsdale J, Knight JC. Major histocompatibility complex genomics and human disease. Annu Rev Genom Hum Genet. 2013;14:301-23.
9. Trowsdale J. Genomic structure and function in the MHC. Trends Genet. 1993;9:117-22.
10. Norman PJ, Norberg SJ, Guethlein LA, et al. Sequences of 95 human MHC haplotypes reveal extreme coding variation in genes other than highly polymorphic HLA class I and II. Genome Res. 2017;27:813-23.
11. Horton R, Wilming L, Rand V, et al. Gene map of the extended human MHC. Nat Rev Genet. 2004;5:889-99.
12. Neefjes J, Jongsma MLM, Paul P, Bakke O. Towards a systems understanding of MHC class I and MHC class II antigen presentation. Nat Rev Immunol. 2011;11:823-36.
13. Rock KL, Reits E, Neefjes J. Present Yourself! By MHCClass I and MHCClass II Molecules. Trends Immunol. 2016;37:724-37.
14. Holling TM, Schooten E, Van Den Elsen PJ. Function and regulation of MHC class II molecules in T-lymphocytes: Of mice and men. Hum Immunol. 2004;65:282-90.
15. Blum JS, Wearsch PA, Cresswell P. Pathways of antigen processing. Annu Rev Immunol. 2013;31:443-73.
16. Farhood B, Najafi M, Mortezaee K. CD8+ cytotoxic T lymphocytes in cancer immunotherapy: A review. J Cell Physiol. 2019;234:8509-21.
17. Cruz FM, Colbert JD, Merino E, et al. The Biology and Underlying Mechanisms of Cross-Presentation of Exogenous Antigens on MHC-I Molecules. Annu Rev Immunol.
2017;35:149-76.
18. Leone P, Shin EC, Perosa F, et al. MHC class I antigen processing and presenting machinery: Organization, function, and defects in tumor cells. J Natl Cancer Inst. 2013;105:1172-87.
19. Thielens A, Vivier E, Romagné F. NK cell MHC class I specific receptors (KIR): From biology to clinical intervention. Curr Opin Immunol. 2012;24:239-45.
20. Cabrera T, Maleno I, Collado A, et al. Analysis of HLA class I alterations in tumors: Choosing a strategy based on known patterns of underlying molecular mechanisms. Tissue Antigens. 2007;69 (Suppl. S1):264-8.
21. Cai L, Michelakos T, Yamada T, et al. Defective HLAclass I antigen processing machinery in cancer. Cancer Immunol Immunother. 2018;67:999-1009.
22. Garrido F, Algarra I. MHC antigens and tumor escape from immune surveillance. Adv Cancer Res. 2001;83:117-58.
23. Martin HP, Brian LH, Hans ChB, et al. Downregulation of antigen presentation-associated pathway proteins is linked to poor outcome in triple-negative breast cancer patient tumors. OncoImmunology. 2017;6(5):e1305531. DOI:10.1080/2162402X.2017.1305531
24. Sinn BV, Weber KE, Schmitt WD, et al. Human leucocyte antigen class I in hormone receptor-positive, HER2-negative breast cancer: association with response and survival after neoadjuvant chemotherapy. Breast Cancer Res. 2019;21:142. DOI:10.1186/s13058-019-1231-z
25. Артамонова Е.В. Роль иммунофенотипирования в диагностике и прогнозе рака молочной железы. Иммунология гемопоэза. 2009;1(9):8-52 [Artamonova EV. Rol' immunofenotipirovaniia v diagnostike i prognoze raka molochnoi zhelezy. Immunologiia gemopoeza. 2009;1(9):8-52 (in Russian)].
26. Буров Д.А., Безнос О.А., Воротников И.К., и др. Клиническое значение экспрессии молекул гистосовместимости на клетках рака молочной железы. Иммунология гемопоэза. 2016;2(14):33-53 [Burov DA, Beznos OA, Vorotnikov IK, et al. Klinicheskoie znacheniie ekspressii molekul gistosovmestimosti na kletkakh raka molochnoi zhelezy. Immunologiia gemopoeza. 2016;2(14):33-53 (in Russian)].
27. Беришвили А.И., Тупицын Н.Н., Лактионов К.П. Иммунофенотипическая характеристика отечно-инфильтративной формы рака молочной железы. Опухоли женской репродуктивной системы. 2009;3-4:15-9 [Berishvili AI, Tupitsyn NN, Laktionov KP. Immunophenotypic characteristics of inflammatory breast cancer. Tumors of Female Reproductive System. 2009;3-4:15-9 (in Russian)].
28. Енгай Д.А. Иммунологическая характеристика Pgp170 позитивного рака молочной железы: дис. … канд. мед. наук. М., 2008 [Engay DA. Immunologicheskaia kharakteristika Pgp170 pozitivnogo raka molochnoi zhelezy: dis. … kand. med. nauk. Moscow, 2008 (in Russian)].
29. Rodriguez JA. HLA-mediated tumor escape mechanisms that may impair immunotherapy clinical outcomes via T-cell activation. Oncol Lett. 2017;14:4415-27.
30. Haen SP, Loffler MW, Rammensee HG, Brossart P. Towards new horizons: Characterization, classification and implications of the tumour antigenic repertoire. Nat Rev Clin Oncol. 2020;17:595-610.
31. Yan M, Jene N, Byrne D, et al. Recruitment of regulatory T cells is correlated with hypoxia-induced CXCR4 expression, and is associated with poor prognosis in basal-like breast cancers. Breast Cancer Res. 2011;13:R47.
32. Olkhanud PB, Damdinsuren B, Bodogai M, et al. Tumor-evoked regulatory B cells promote breast cancer metastasis by converting resting CD4(+) T cells to T-regulatory cells. Cancer Res. 2011;71:3505-15.
33. Munir MT, Kay MK, Kang MH, et al. Tumor-Associated Macrophages asMultifaceted Regulators of Breast Tumor Growth. Int J Mol Sci. 2021;22:6526.
34. Lim B, Woodward WA, Wang X, et al. Inflammatory breast cancer biology: The tumour microenvironment is key. Nat Rev Cancer. 2018;18:485-99.
35. Burugu S, Asleh-Aburaya K, Nielsen TO. Immune infiltrates in the breast cancer microenvironment: Detection, characterization and clinical implication. Breast Cancer. 2017;24:3-15.
________________________________________________
2. McCormack V, McKenzie F, Foerster M, et al. Breast cancer survival and survival gap apportionment in sub-Saharan Africa (ABC-DO): a prospective cohort study. The Lancet Global Health. 2020;8(9):e1203-12. Available at: http://www.ncbi.nlm.nih.gov/pubmed/32827482. Accessed: 01.12.2021.
3. Titov KS, Kazakov AM, Baryshnikova MA, et al. Nekotorye molekulyarnye i immunologicheskie faktory prognoza trizhdy negativnogo raka molochnoi zhelezy. Onkoginekologiya. 2019;4(32):26-34 (in Russian)].
4. Mutebi M, Anderson BO, Duggan C, et al. Breast cancer treatment: A phased approach to implementation. Cancer. 2020;126(Suppl.10):236578. Available at: http://www.ncbi.nlm.nih.gov/pubmed/32348571. Accessed: 01.12.2021.
5. Ryabchikov DA, Abdullaeva EI, Dudina IA, et al. Rol' mikro-RNK v kantserogeneze i prognoze zlokachestvennykh novoobrazovanii molochnoi zhelezy. Vestnik Rossiiskogo nauchnogo tsentra rentgenoradiologii. 2018;18(2):5 (in Russian).
6. Sabbatino F, Liguori L, Polcaro G, et al. Role of Human Leukocyte Antigen System as A Predictive Biomarker for Checkpoint-Based Immunotherapy in Cancer Patients. Int J Mol Sci. 2020;21:7295. DOI:10.3390/ijms21197295
7. Shukla A, Cloutier M, Santharam AM, et al. The MHC Class-I Transactivator NLRC5: Implications to Cancer Immunology and Potential Applications to Cancer Immunotherapy. Int J Mol Sci. 2021;22(4):1964. DOI:10.3390/ijms22041964
8. Trowsdale J, Knight JC. Major histocompatibility complex genomics and human disease. Annu Rev Genom Hum Genet. 2013;14:301-23.
9. Trowsdale J. Genomic structure and function in the MHC. Trends Genet. 1993;9:117-22.
10. Norman PJ, Norberg SJ, Guethlein LA, et al. Sequences of 95 human MHC haplotypes reveal extreme coding variation in genes other than highly polymorphic HLA class I and II. Genome Res. 2017;27:813-23.
11. Horton R, Wilming L, Rand V, et al. Gene map of the extended human MHC. Nat Rev Genet. 2004;5:889-99.
12. Neefjes J, Jongsma MLM, Paul P, Bakke O. Towards a systems understanding of MHC class I and MHC class II antigen presentation. Nat Rev Immunol. 2011;11:823-36.
13. Rock KL, Reits E, Neefjes J. Present Yourself! By MHCClass I and MHCClass II Molecules. Trends Immunol. 2016;37:724-37.
14. Holling TM, Schooten E, Van Den Elsen PJ. Function and regulation of MHC class II molecules in T-lymphocytes: Of mice and men. Hum Immunol. 2004;65:282-90.
15. Blum JS, Wearsch PA, Cresswell P. Pathways of antigen processing. Annu Rev Immunol. 2013;31:443-73.
16. Farhood B, Najafi M, Mortezaee K. CD8+ cytotoxic T lymphocytes in cancer immunotherapy: A review. J Cell Physiol. 2019;234:8509-21.
17. Cruz FM, Colbert JD, Merino E, et al. The Biology and Underlying Mechanisms of Cross-Presentation of Exogenous Antigens on MHC-I Molecules. Annu Rev Immunol.
2017;35:149-76.
18. Leone P, Shin EC, Perosa F, et al. MHC class I antigen processing and presenting machinery: Organization, function, and defects in tumor cells. J Natl Cancer Inst. 2013;105:1172-87.
19. Thielens A, Vivier E, Romagné F. NK cell MHC class I specific receptors (KIR): From biology to clinical intervention. Curr Opin Immunol. 2012;24:239-45.
20. Cabrera T, Maleno I, Collado A, et al. Analysis of HLA class I alterations in tumors: Choosing a strategy based on known patterns of underlying molecular mechanisms. Tissue Antigens. 2007;69 (Suppl. S1):264-8.
21. Cai L, Michelakos T, Yamada T, et al. Defective HLAclass I antigen processing machinery in cancer. Cancer Immunol Immunother. 2018;67:999-1009.
22. Garrido F, Algarra I. MHC antigens and tumor escape from immune surveillance. Adv Cancer Res. 2001;83:117-58.
23. Martin HP, Brian LH, Hans ChB, et al. Downregulation of antigen presentation-associated pathway proteins is linked to poor outcome in triple-negative breast cancer patient tumors. OncoImmunology. 2017;6(5):e1305531. DOI:10.1080/2162402X.2017.1305531
24. Sinn BV, Weber KE, Schmitt WD, et al. Human leucocyte antigen class I in hormone receptor-positive, HER2-negative breast cancer: association with response and survival after neoadjuvant chemotherapy. Breast Cancer Res. 2019;21:142. DOI:10.1186/s13058-019-1231-z
25. Artamonova EV. Rol' immunofenotipirovaniia v diagnostike i prognoze raka molochnoi zhelezy. Immunologiia gemopoeza. 2009;1(9):8-52 (in Russian).
26. Burov DA, Beznos OA, Vorotnikov IK, et al. Klinicheskoie znacheniie ekspressii molekul gistosovmestimosti na kletkakh raka molochnoi zhelezy. Immunologiia gemopoeza. 2016;2(14):33-53 (in Russian).
27. Berishvili AI, Tupitsyn NN, Laktionov KP. Immunophenotypic characteristics of inflammatory breast cancer. Tumors of Female Reproductive System. 2009;3-4:15-9 (in Russian).
28. Engay DA. Immunologicheskaia kharakteristika Pgp170 pozitivnogo raka molochnoi zhelezy: dis. … kand. med. nauk. Moscow, 2008 (in Russian).
29. Rodriguez JA. HLA-mediated tumor escape mechanisms that may impair immunotherapy clinical outcomes via T-cell activation. Oncol Lett. 2017;14:4415-27.
30. Haen SP, Loffler MW, Rammensee HG, Brossart P. Towards new horizons: Characterization, classification and implications of the tumour antigenic repertoire. Nat Rev Clin Oncol. 2020;17:595-610.
31. Yan M, Jene N, Byrne D, et al. Recruitment of regulatory T cells is correlated with hypoxia-induced CXCR4 expression, and is associated with poor prognosis in basal-like breast cancers. Breast Cancer Res. 2011;13:R47.
32. Olkhanud PB, Damdinsuren B, Bodogai M, et al. Tumor-evoked regulatory B cells promote breast cancer metastasis by converting resting CD4(+) T cells to T-regulatory cells. Cancer Res. 2011;71:3505-15.
33. Munir MT, Kay MK, Kang MH, et al. Tumor-Associated Macrophages asMultifaceted Regulators of Breast Tumor Growth. Int J Mol Sci. 2021;22:6526.
34. Lim B, Woodward WA, Wang X, et al. Inflammatory breast cancer biology: The tumour microenvironment is key. Nat Rev Cancer. 2018;18:485-99.
35. Burugu S, Asleh-Aburaya K, Nielsen TO. Immune infiltrates in the breast cancer microenvironment: Detection, characterization and clinical implication. Breast Cancer. 2017;24:3-15.
Авторы
С.В. Чулкова*1,2, Е.Н. Шолохова1, И.В. Поддубная3, И.С. Стилиди1,2, Д.А. Буров4, Н.Н. Тупицын1
1 ФГБУ «Национальный медицинский исследовательский центр онкологии им. Н.Н. Блохина» Минздрава России, Москва, Россия;
2 ФГАОУ ВО «Российский национальный исследовательский медицинский университет им. Н.И. Пирогова» Минздрава России, Москва, Россия;
3 ФГБОУ ДПО «Российская медицинская академия непрерывного профессионального образования» Минздрава России, Москва, Россия;
4 ФГБОУ ВО «Московский государственный медико-стоматологический университет им. А.И. Евдокимова» Минздрава России, Москва, Россия
*chulkova@mail.ru
1 Blokhin National Medical Research Center of Oncology, Moscow, Russia;
2 Pirogov Russian National Research Medical University, Moscow, Russia;
3 Russian Medical Academy of Continuous Professional Education, Moscow, Russia;
4 Yevdokimov Moscow State University of Medicine and Dentistry, Moscow, Russia
*chulkova@mail.ru
1 ФГБУ «Национальный медицинский исследовательский центр онкологии им. Н.Н. Блохина» Минздрава России, Москва, Россия;
2 ФГАОУ ВО «Российский национальный исследовательский медицинский университет им. Н.И. Пирогова» Минздрава России, Москва, Россия;
3 ФГБОУ ДПО «Российская медицинская академия непрерывного профессионального образования» Минздрава России, Москва, Россия;
4 ФГБОУ ВО «Московский государственный медико-стоматологический университет им. А.И. Евдокимова» Минздрава России, Москва, Россия
*chulkova@mail.ru
________________________________________________
1 Blokhin National Medical Research Center of Oncology, Moscow, Russia;
2 Pirogov Russian National Research Medical University, Moscow, Russia;
3 Russian Medical Academy of Continuous Professional Education, Moscow, Russia;
4 Yevdokimov Moscow State University of Medicine and Dentistry, Moscow, Russia
*chulkova@mail.ru
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