Механизм работы разных поколений ингибиторов EGFR при злокачественных опухолях легких. Обзор литературы и обобщение данных

Насретдинов А.Ф., Меньшиков К.В., Султанбаев А.В., Мусин Ш.И., Султанбаева Н.И., Меньшикова И.А. Механизм работы разных поколений ингибиторов EGFR при злокачественных опухолях легких. Обзор литературы и обобщение данных. Современная Онкология. 2022;24(3):340–344.
DOI: 10.26442/18151434.2022.3.201813

© ООО «КОНСИЛИУМ МЕДИКУМ», 2022 г.

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Nasretdinov AF, Menshikov KV, Sultanbaev AV, Musin SI, Sultanbaeva NI, Men'shikova IA. The mechanism of action of different generations of EGFR-inhibitors in malignant lung tumors. Literature review and data synthesis. Journal of Modern Oncology. 2022;24(3):340–344. DOI: 10.26442/18151434.2022.3.201813

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Аннотация

Знание молекулярно-генетических особенностей прогрессии немелкоклеточной опухоли легкого в настоящее время позволяет обеспечить пациента лучшими вариантами лечения. Одним из самых известных и изученных генетических отклонений является мутация в гене EGFR, делающая опухоль чувствительной к терапии ингибиторами тирозинкиназ. В условиях существования сразу нескольких терапевтических опций требуются знания не только результатов клинических исследований, но и фундаментальных особенностей механизмов действия того или иного препарата. В статье представлен обзор литературы, анализирующий особенности функционирования EGFR (рецептор эпидермального фактора роста), механизмы действия ингибиторов EGFR различных поколений (эрлотиниб, гефитиниб, афатиниб, осимертиниб), обобщение и анализ основных различий между ними.

Ключевые слова: рак легкого, ингибиторы тирозинкиназ, EGFR, эрлотиниб, гефитиниб, афатиниб, осимертиниб

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Knowledge of the molecular characteristics of the progression of non-small cell lung tumors currently provides the patient with the best treatment options. One of the most well-known and studied genetic abnormalities is a mutation in the EGFR gene, which makes the tumor sensitive to therapy with tyrosine kinase inhibitors. In the conditions of the existence of several therapeutic options at once, it is required to know not only the results of clinical trials, but also the fundamental features of the mechanisms of action of a particular drug. The article contains a literature review, presenting the features of the functioning of EGFR (epidermal growth factor receptor), the mechanisms of action of EGFR inhibitors of different generations (erlotinib, gefitinib, afatinib, osimertinib), generalization and analysis of the main differences between them.

Keywords: lung cancer, tyrosine kinase inhibitors, EGFR, erlotinib, gefitinib, afatinib, osimertinib

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Список литературы

1. Imyanitov EN, Demidova IA, Gordiev MG, et al. Distribution of EGFR Mutations in 10,607 Russian Patients with Lung Cancer. Mol Diagn Ther. 2016;20(4):401-6.
DOI:10.1007/s40291-016-0213-4
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5. Wang Z. ErbB Receptors and Cancer. Methods Mol Biol. 2017;1652:3-35. DOI:10.1007/978-1-4939-7219-7_1
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15. O'Kane GM, Bradbury PA, Feld R, et al. Uncommon EGFR mutations in advanced non-small cell lung cancer. Lung Cancer. 2017;109:137-44. DOI:10.1016/j.lungcan.2017.04.016
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17. Landi L, Cappuzzo F. Experience with erlotinib in the treatment of non-small cell lung cancer. Ther Adv Respir Dis. 2015;9(4):146-63. DOI:10.1177/1753465815588053
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20. Yuan Y, Li X, Chen J, et al. Critical appraisal of the role of gefitinib in the management of locally advanced or metastatic non-small cell lung cancer. Onco Targets Ther. 2014;7:841-52 DOI:10.2147/OTT.S34124
21. Mok TS, Wu YL, Thongprasert S, et al. Gefitinib or carboplatin-paclitaxel in pulmonary adenocarcinoma. N Engl J Med. 2009;361(10):947-57. DOI:10.1056/NEJMoa0810699
22. Mitsudomi T, Morita S, Yatabe Y, et al. Gefitinib versus cisplatin plus docetaxel in patients with non-small-cell lung cancer harbouring mutations of the epidermal growth factor receptor (WJTOG3405): an open label, randomised phase 3 trial. Lancet Oncol. 2010;11(2):121-8. DOI:10.1016/S1470-2045(09)70364-X
23. Maemondo M, Inoue A, Kobayashi K, et al. Gefitinib or chemotherapy for non-small-cell lung cancer with mutated EGFR. N Engl J Med. 2010;362(25):2380-8. DOI:10.1056/NEJMoa0909530
24. Zhou C, Wu YL, Chen G, et al. Final overall survival results from a randomised, phase III study of erlotinib versus chemotherapy as first-line treatment of EGFR mutation-positive advanced non-small-cell lung cancer (OPTIMAL, CTONG-0802). Ann Oncol. 2015;26(9):1877-83. DOI:10.1093/annonc/mdv276
25. Han JY, Park K, Kim SW, et al. First-SIGNAL: first-line single-agent iressa versus gemcitabine and cisplatin trial in never-smokers with adenocarcinoma of the lung. J Clin Oncol. 2012;30(10):1122-8. DOI:10.1200/JCO.2011.36.8456
26. Rosell R, Carcereny E, Gervais R, et al. Erlotinib versus standard chemotherapy as first-line treatment for European patients with advanced EGFR mutation-positive non-small-cell lung cancer (EURTAC): a multicentre, open-label, randomised phase 3 trial. Lancet Oncol. 2012;13(3):239-46. DOI:10.1016/S1470-2045(11)70393-X
27. Wind S, Schnell D, Ebner T, et al. Clinical Pharmacokinetics and Pharmacodynamics of Afatinib. Clin Pharmacokinet. 2017;56(3):235-50. DOI:10.1007/s40262-016-0440-1
28. Hirsh V. New developments in the treatment of advanced squamous cell lung cancer: focus on afatinib. Onco Targets Ther. 2017;10:2513-26. DOI:10.2147/OTT.S104177
29. Sequist LV, Yang JC, Yamamoto N, et al. Phase III study of afatinib or cisplatin plus pemetrexed in patients with metastatic lung adenocarcinoma with EGFR mutations. J Clin Oncol. 2013;31(27):3327-34. DOI:10.1200/JCO.2012.44.2806
30. Wu YL, Zhou C, Hu CP, et al. Afatinib versus cisplatin plus gemcitabine for first-line treatment of Asian patients with advanced non-small-cell lung cancer harbouring EGFR mutations (LUX-Lung 6): an open-label, randomised phase 3 trial. Lancet Oncol. 2014;15(2):213-22. doi:10.1016/S1470-2045(13)70604-1
31. Yang JC, Wu YL, Schuler M, et al. Afatinib versus cisplatin-based chemotherapy for EGFR mutation-positive lung adenocarcinoma (LUX-Lung 3 and LUX‑Lung 6): analysis of overall survival data from two randomised, phase 3 trials. Lancet Oncol. 2015;16(2):141-51. doi:10.1016/S1470-2045(14)71173-8
32. Paz-Ares L, Tan EH, O'Byrne K, et al. Afatinib versus gefitinib in patients with EGFR mutation-positive advanced non-small-cell lung cancer: overall survival data from the phase IIb LUX-Lung 7 trial. Ann Oncol. 2017;28(2):270-7. DOI:10.1093/annonc/mdw611
33. Russo A, Franchina T, Ricciardi G, et al. Heterogeneous Responses to Epidermal Growth Factor Receptor (EGFR) Tyrosine Kinase Inhibitors (TKIs) in Patients with Uncommon EGFR Mutations: New Insights and Future Perspectives in this Complex Clinical Scenario. Int J Mol Sci. 2019;20(6):1431. DOI:10.3390/ijms20061431
34. Kobayashi Y, Togashi Y, Yatabe Y, et al. EGFR Exon 18 Mutations in Lung Cancer: Molecular Predictors of Augmented Sensitivity to Afatinib or Neratinib as Compared with First- or Third-Generation TKIs. Clin Cancer Res. 2015;21(23):5305-13. DOI:10.1158/1078-0432.CCR-15-1046
35. Davis MI, Hunt JP, Herrgard S, et al. Comprehensive analysis of kinase inhibitor selectivity. Nat Biotechnol. 2011;29(11):1046-51. DOI:10.1038/nbt.1990
36. Насретдинов А.Ф., Султанбаев А.В., Меньшиков К.В., и др. Ландшафт мутаций генов эпидермального фактора роста у больных раком легкого в Республике Башкортостан. Эффективная фармакотерапия. 2020;16(33):18-23 [Nasretdinov AF, Sultanbayev AV, Menshikov KV, et al. Landscape of Epidermal Growth Factor Gene Mutations in Patients with Lung Cancer in the Republic of Bashkortostan. Effektivnaia farmakoterapiia. 2020;16(33):18-23 (in Russian)]. DOI:10.33978/2307-3586-2020-16-33-18-23
37. Kobayashi S, Boggon TJ, Dayaram T, et al. EGFR mutation and resistance of non-small-cell lung cancer to gefitinib. N Engl J Med. 2005;352(8):786-92. DOI:10.1056/NEJMoa044238
38. Hochmair MJ, Buder A, Schwab S, et al. Liquid-Biopsy-Based Identification of EGFR T790M Mutation-Mediated Resistance to Afatinib Treatment in Patients with Advanced EGFR Mutation-Positive NSCLC, and Subsequent Response to Osimertinib. Target Oncol. 2019;14(1):75-83. DOI:10.1007/s11523-018-0612-z
39. Cross DA, Ashton SE, Ghiorghiu S, et al. AZD9291, an irreversible EGFR TKI, overcomes T790M-mediated resistance to EGFR inhibitors in lung cancer. Cancer Discov. 2014;4(9):1046-61. DOI:10.1158/2159-8290.CD-14-0337
40. Ramalingam SS, Vansteenkiste J, Planchard D, et al. Overall Survival with Osimertinib in Untreated, EGFR-Mutated Advanced NSCLC. N Engl J Med. 2020;382(1):41-50. DOI:10.1056/NEJMoa1913662
41. Soria JC, Ohe Y, Vansteenkiste J, et al. Osimertinib in Untreated EGFR-Mutated Advanced Non-Small-Cell Lung Cancer. N Engl J Med. 2018;378(2):113-25. DOI:10.1056/NEJMoa1713137
42. Reungwetwattana T, Nakagawa K, Cho BC, et al. CNS Response to Osimertinib Versus Standard Epidermal Growth Factor Receptor Tyrosine Kinase Inhibitors in Patients With Untreated EGFR-Mutated Advanced Non-Small-Cell Lung Cancer. J Clin Oncol. 2018:JCO2018783118. DOI:10.1200/JCO.2018.78.3118
43. Реутова Е.В., Лактионов К.К., Ардзинба М.С., и др. Приобретенная резистентность к ингибиторам тирозинкиназы EGFR: пути преодоления. Медицинский Совет. 2017;(14):24-8 [Reutova EV, Laktionov KK, Ardzinba MS, et al. Priobretennaia rezistentnost' k ingibitoram tirozinkinazy EGFR: puti preodoleniia. Meditsinskiy Sovet. 2017;(14):24-8 (in Russian)].

________________________________________________

1. Imyanitov EN, Demidova IA, Gordiev MG, et al. Distribution of EGFR Mutations in 10,607 Russian Patients with Lung Cancer. Mol Diagn Ther. 2016;20(4):401-6.
DOI:10.1007/s40291-016-0213-4
2. Kobayashi Y, Mitsudomi T. Not all epidermal growth factor receptor mutations in lung cancer are created equal: Perspectives for individualized treatment strategy. Cancer Sci. 2016;107(9):1179-86. DOI:10.1111/cas.12996
3. Soria JC, Ohe Y, Vansteenkiste J, et al. Osimertinib in Untreated EGFR-Mutated Advanced Non-Small-Cell Lung Cancer. N Engl J Med. 2018;378(2):113-25. DOI:10.1056/NEJMoa1713137
4. Yang JC, Ahn MJ, Kim DW, et al. Osimertinib in Pretreated T790M-Positive Advanced Non-Small-Cell Lung Cancer: AURA Study Phase II Extension Component. J Clin Oncol. 2017;35(12):1288-96. DOI:10.1200/JCO.2016.70.3223
5. Wang Z. ErbB Receptors and Cancer. Methods Mol Biol. 2017;1652:3-35. DOI:10.1007/978-1-4939-7219-7_1
6. Voldborg BR, Damstrup L, Spang-Thomsen M, Poulsen HS. Epidermal growth factor receptor (EGFR) and EGFR mutations, function and possible role in clinical trials. Ann Oncol. 1997;8(12):1197-206. DOI:10.1023/a:1008209720526
7. Zhang H, Berezov A, Wang Q, et al. ErbB receptors: from oncogenes to targeted cancer therapies. J Clin Invest. 2007;117(8):2051-8. DOI:10.1172/JCI32278
8. Bromberg J. Stat proteins and oncogenesis. J Clin Invest. 2002;109(9):1139-42. DOI:10.1172/JCI15617
9. Scaltriti M, Baselga J. The epidermal growth factor receptor pathway: a model for targeted therapy. Clin Cancer Res. 2006;12(18):5268-72. DOI:10.1158/1078-0432.CCR-05-1554
10. Roepstorff K, Grandal MV, Henriksen L, et al. Differential effects of EGFR ligands on endocytic sorting of the receptor. Traffic. 2009;10(8):1115-27.
DOI:10.1111/j.1600-0854.2009.00943.x
11. Chan BA, Hughes BG. Targeted therapy for non-small cell lung cancer: current standards and the promise of the future. Transl Lung Cancer Res. 2015;4(1):36‑54. DOI:10.3978/j.issn.2218-6751.2014.05.01
12. Harrison PT, Vyse S, Huang PH. Rare epidermal growth factor receptor (EGFR) mutations in non-small cell lung cancer. Semin Cancer Biol. 2020;61:167-79. DOI:10.1016/j.semcancer.2019.09.015
13. Byeon S, Kim Y, Lim SW, et al. Clinical Outcomes of EGFR Exon 20 Insertion Mutations in Advanced Non-small Cell Lung Cancer in Korea. Cancer Res Treat. 2019;51(2):623-31. DOI:10.4143/crt.2018.151
14. Li K, Yang M, Liang N, et al. Determining EGFR-TKI sensitivity of G719X and other uncommon EGFR mutations in non-small cell lung cancer: Perplexity and solution (Review). Oncol Rep. 2017;37(3):1347-58. DOI:10.3892/or.2017.5409
15. O'Kane GM, Bradbury PA, Feld R, et al. Uncommon EGFR mutations in advanced non-small cell lung cancer. Lung Cancer. 2017;109:137-44. DOI:10.1016/j.lungcan.2017.04.016
16. Sultanbaev A, Nasretdinov A, Sultanbaeva N, et al. 12P EGFR gene mutations landscape at lung cancer in a multinational region located in the southeast of the European part of Russia. Ann Oncol. 2020;31:S1220-1. DOI:10.1016/j.annonc.2020.08.2171
17. Landi L, Cappuzzo F. Experience with erlotinib in the treatment of non-small cell lung cancer. Ther Adv Respir Dis. 2015;9(4):146-63. DOI:10.1177/1753465815588053
18. Hu J, Li Y, Zhang Y, Yu DJ. ATPbind: Accurate Protein-ATP Binding Site Prediction by Combining Sequence-Profiling and Structure-Based Comparisons. J Chem Inf Model. 2018;58(2):501-10. DOI:10.1021/acs.jcim.7b00397
19. Yun CH, Mengwasser KE, Toms A, et al. The T790M mutation in EGFR kinase causes drug resistance by increasing the affinity for ATP. Proc Natl Acad Sci USA. 2008;105(6):2070-5. DOI:10.1073/pnas.0709662105
20. Yuan Y, Li X, Chen J, et al. Critical appraisal of the role of gefitinib in the management of locally advanced or metastatic non-small cell lung cancer. Onco Targets Ther. 2014;7:841-52 DOI:10.2147/OTT.S34124
21. Mok TS, Wu YL, Thongprasert S, et al. Gefitinib or carboplatin-paclitaxel in pulmonary adenocarcinoma. N Engl J Med. 2009;361(10):947-57. DOI:10.1056/NEJMoa0810699
22. Mitsudomi T, Morita S, Yatabe Y, et al. Gefitinib versus cisplatin plus docetaxel in patients with non-small-cell lung cancer harbouring mutations of the epidermal growth factor receptor (WJTOG3405): an open label, randomised phase 3 trial. Lancet Oncol. 2010;11(2):121-8. DOI:10.1016/S1470-2045(09)70364-X
23. Maemondo M, Inoue A, Kobayashi K, et al. Gefitinib or chemotherapy for non-small-cell lung cancer with mutated EGFR. N Engl J Med. 2010;362(25):2380-8. DOI:10.1056/NEJMoa0909530
24. Zhou C, Wu YL, Chen G, et al. Final overall survival results from a randomised, phase III study of erlotinib versus chemotherapy as first-line treatment of EGFR mutation-positive advanced non-small-cell lung cancer (OPTIMAL, CTONG-0802). Ann Oncol. 2015;26(9):1877-83. DOI:10.1093/annonc/mdv276
25. Han JY, Park K, Kim SW, et al. First-SIGNAL: first-line single-agent iressa versus gemcitabine and cisplatin trial in never-smokers with adenocarcinoma of the lung. J Clin Oncol. 2012;30(10):1122-8. DOI:10.1200/JCO.2011.36.8456
26. Rosell R, Carcereny E, Gervais R, et al. Erlotinib versus standard chemotherapy as first-line treatment for European patients with advanced EGFR mutation-positive non-small-cell lung cancer (EURTAC): a multicentre, open-label, randomised phase 3 trial. Lancet Oncol. 2012;13(3):239-46. DOI:10.1016/S1470-2045(11)70393-X
27. Wind S, Schnell D, Ebner T, et al. Clinical Pharmacokinetics and Pharmacodynamics of Afatinib. Clin Pharmacokinet. 2017;56(3):235-50. DOI:10.1007/s40262-016-0440-1
28. Hirsh V. New developments in the treatment of advanced squamous cell lung cancer: focus on afatinib. Onco Targets Ther. 2017;10:2513-26. DOI:10.2147/OTT.S104177
29. Sequist LV, Yang JC, Yamamoto N, et al. Phase III study of afatinib or cisplatin plus pemetrexed in patients with metastatic lung adenocarcinoma with EGFR mutations. J Clin Oncol. 2013;31(27):3327-34. DOI:10.1200/JCO.2012.44.2806
30. Wu YL, Zhou C, Hu CP, et al. Afatinib versus cisplatin plus gemcitabine for first-line treatment of Asian patients with advanced non-small-cell lung cancer harbouring EGFR mutations (LUX-Lung 6): an open-label, randomised phase 3 trial. Lancet Oncol. 2014;15(2):213-22. doi:10.1016/S1470-2045(13)70604-1
31. Yang JC, Wu YL, Schuler M, et al. Afatinib versus cisplatin-based chemotherapy for EGFR mutation-positive lung adenocarcinoma (LUX-Lung 3 and LUX‑Lung 6): analysis of overall survival data from two randomised, phase 3 trials. Lancet Oncol. 2015;16(2):141-51. doi:10.1016/S1470-2045(14)71173-8
32. Paz-Ares L, Tan EH, O'Byrne K, et al. Afatinib versus gefitinib in patients with EGFR mutation-positive advanced non-small-cell lung cancer: overall survival data from the phase IIb LUX-Lung 7 trial. Ann Oncol. 2017;28(2):270-7. DOI:10.1093/annonc/mdw611
33. Russo A, Franchina T, Ricciardi G, et al. Heterogeneous Responses to Epidermal Growth Factor Receptor (EGFR) Tyrosine Kinase Inhibitors (TKIs) in Patients with Uncommon EGFR Mutations: New Insights and Future Perspectives in this Complex Clinical Scenario. Int J Mol Sci. 2019;20(6):1431. DOI:10.3390/ijms20061431
34. Kobayashi Y, Togashi Y, Yatabe Y, et al. EGFR Exon 18 Mutations in Lung Cancer: Molecular Predictors of Augmented Sensitivity to Afatinib or Neratinib as Compared with First- or Third-Generation TKIs. Clin Cancer Res. 2015;21(23):5305-13. DOI:10.1158/1078-0432.CCR-15-1046
35. Davis MI, Hunt JP, Herrgard S, et al. Comprehensive analysis of kinase inhibitor selectivity. Nat Biotechnol. 2011;29(11):1046-51. DOI:10.1038/nbt.1990
36. Насретдинов А.Ф., Султанбаев А.В., Меньшиков К.В., и др. Ландшафт мутаций генов эпидермального фактора роста у больных раком легкого в Республике Башкортостан. Эффективная фармакотерапия. 2020;16(33):18-23 [Nasretdinov AF, Sultanbayev AV, Menshikov KV, et al. Landscape of Epidermal Growth Factor Gene Mutations in Patients with Lung Cancer in the Republic of Bashkortostan. Effektivnaia farmakoterapiia. 2020;16(33):18-23 (in Russian)]. DOI:10.33978/2307-3586-2020-16-33-18-23
37. Kobayashi S, Boggon TJ, Dayaram T, et al. EGFR mutation and resistance of non-small-cell lung cancer to gefitinib. N Engl J Med. 2005;352(8):786-92. DOI:10.1056/NEJMoa044238
38. Hochmair MJ, Buder A, Schwab S, et al. Liquid-Biopsy-Based Identification of EGFR T790M Mutation-Mediated Resistance to Afatinib Treatment in Patients with Advanced EGFR Mutation-Positive NSCLC, and Subsequent Response to Osimertinib. Target Oncol. 2019;14(1):75-83. DOI:10.1007/s11523-018-0612-z
39. Cross DA, Ashton SE, Ghiorghiu S, et al. AZD9291, an irreversible EGFR TKI, overcomes T790M-mediated resistance to EGFR inhibitors in lung cancer. Cancer Discov. 2014;4(9):1046-61. DOI:10.1158/2159-8290.CD-14-0337
40. Ramalingam SS, Vansteenkiste J, Planchard D, et al. Overall Survival with Osimertinib in Untreated, EGFR-Mutated Advanced NSCLC. N Engl J Med. 2020;382(1):41-50. DOI:10.1056/NEJMoa1913662
41. Soria JC, Ohe Y, Vansteenkiste J, et al. Osimertinib in Untreated EGFR-Mutated Advanced Non-Small-Cell Lung Cancer. N Engl J Med. 2018;378(2):113-25. DOI:10.1056/NEJMoa1713137
42. Reungwetwattana T, Nakagawa K, Cho BC, et al. CNS Response to Osimertinib Versus Standard Epidermal Growth Factor Receptor Tyrosine Kinase Inhibitors in Patients With Untreated EGFR-Mutated Advanced Non-Small-Cell Lung Cancer. J Clin Oncol. 2018:JCO2018783118. DOI:10.1200/JCO.2018.78.3118
43. Reutova EV, Laktionov KK, Ardzinba MS, et al. Priobretennaia rezistentnost' k ingibitoram tirozinkinazy EGFR: puti preodoleniia. Meditsinskiy Sovet. 2017;(14):24-8 (in Russian).

Авторы

А.Ф. Насретдинов*1, К.В. Меньшиков1,2, А.В. Султанбаев1, Ш.И. Мусин1,2, Н.И. Султанбаева1, И.А. Меньшикова2

1 ГАУЗ «Республиканский клинический онкологический диспансер» Минздрава Республики Башкортостан, Уфа, Россия;
2 ФГБОУ ВО «Башкирский государственный медицинский университет» Минздрава России, Уфа, Россия
*rkodrb@yandex.ru

________________________________________________

Ainur F. Nasretdinov*1, Konstantin V. Menshikov1,2, Alexander V. Sultanbaev1, Shamil I. Musin1,2, Nadezda I. Sultanbaeva1, Irina A. Men'shikova2

1 Republican Clinical Oncological Dispensary, Ufa, Russia;
2 Bashkir State Medical University, Ufa, Russia
*rkodrb@yandex.ru

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Цель портала OmniDoctor – предоставление профессиональной информации врачам, провизорам и фармацевтам.