Роль ABC-транспортеров в поддержании гомеостаза, патогенезе и терапии онкологических заболеваний
https://doi.org/10.17650/2313-805X-2024-11-1-8-21
Аннотация
ABC-транспортеры (ATP binding cassette (ABC) transporters), АТФ-зависимые транспортеры – белки, играющие двоякую роль в переносе веществ через мембрану. С одной стороны, они транспортируют питательные вещества и другие молекулы внутрь клетки, поставляя необходимые нутриенты, с другой, экскретируют некоторые эндогенные и экзогенные субстраты из клетки, поддерживая их гомеостаз в организме и предотвращая агрессивные воздействия внешней среды. ABC-транспортеры, исходя из своих функций, играют большую роль в патогенезе различных метаболических нарушений. Кроме того, накоплено много данных об участии этих белков в онкогенезе за счет их вклада в инициацию, прогрессию, инвазию и метастазирование опухолей, а также в развитие фенотипа множественной лекарственной устойчивости. В настоящее время данные белки являются привлекательными терапевтическими мишенями, воздействие на которые способно существенным образом повысить эффективность противоопухолевой терапии и улучшить прогноз пациентов с онкологическими заболеваниями, в том числе рецидивирующих, метастатических и неоперабельных форм. В обзоре представлена информация о лекарственных препаратах как являющихся субстратами для ABC-транспортеров, так и оказывающих влияние на их функциональную активность, а также результаты клинических испытаний по изучению эффективности использования этих ингибиторов в практической онкологии.
Ключевые слова
Об авторах
С. В. БойчукРоссия
Сергей Васильевич Бойчук
420012 Казань, ул. Бутлерова, 49; 420008 Казань, ул. Кремлевская, 18; 125993 Москва, ул. Баррикадная, 2/1, стр. 1
Т. В. Ивойлова
Россия
420012 Казань, ул. Бутлерова, 49
Список литературы
1. Housman G., Byler S., Heerboth S. et al. Drug resistance in cancer: an overview. Cancers (Basel) 2014;6(3):1769–92. DOI: 10.3390/cancers6031769
2. Rueff J., Rodrigues A.S. Cancer drug resistance: a brief overview from a genetic viewpoint. Methods Mol Biol 2016;1395:1–18. DOI: 10.1007/978-1-4939-3347-1_1
3. Ставровская А.А., Генс Г.П. Новое в изучении множественной лекарственной устойчивости клеток рака молочной железы. Успехи молекулярной онкологии 2015;2(1):39–51. DOI: 10.17650/2313-805X.2015.2.1.039–051
4. Deng J., Bai X., Feng X. et al. Inhibition of PI3K/Akt/mTOR signaling pathway alleviates ovarian cancer chemoresistance through reversing epithelial-mesenchymal transition and decreasing cancer stem cell marker expression. BMC Cancer 2019;19(1):618. DOI: 10.1186/s12885-019-5824-9
5. Stefan S.M. Multi-target ABC transporter modulators: what next and where to go? Future Med Chem 2019;11(18):2353–8. DOI: 10.4155/fmc-2019-0185
6. Juan-Carlos P.M., Perla-Lidia P.P., Stephanie-Talia M.M. et al. ABC transporter superfamily. An updated overview, relevance in cancer multidrug resistance and perspectives with personalized medicine. Mol Biol Rep 2021;48(2):1883–901. DOI: 10.1007/s11033-021-06155-w
7. Robey R.W., Pluchino K.M., Hall M.D. et al. Revisiting the role of ABC transporters in multidrug-resistant cancer. Nat Rev Cancer 2018;18(7):452–64. DOI: 10.1038/s41568-018-0005-8
8. Смирнов Л.П. АТФ-связывающие транспортные белки семейства abc (ATP-binding cassette transporters, abc). Номенклатура, структура, молекулярное разнообразие, функция, участие в функционировании системы биотрансформации ксенобиотиков. Труды Карельского научного центра РАН 2020;3:5–19. DOI: 10.17076/eb1044
9. Alam A., Locher K.P. Structure and mechanism of human ABC transporters. Annu Rev Biophys 2023;52:275–300. DOI: 10.1146/annurev-biophys-111622-091232
10. Thomas C., Tampé R. Structural and mechanistic principles of ABC transporters. Annu Rev Biochem 2020;89:605–36. DOI: 10.1146/annurev-biochem-011520-105201
11. Rees D.C., Johnson E., Lewinson O. ABC transporters: the power to change. Nat Rev Mol Cell Biol 2009;10(3):218–27. DOI: 10.1038/nrm2646
12. Wilkens S. Structure and mechanism of ABC transporters. F1000Prime Rep 2015;7:14. DOI: 10.12703/P7-14
13. Fitzgerald M.L., Mujawar Z., Tamehiro N. ABC transporters, atherosclerosis and inflammation. Atherosclerosis 2010;211(2):361–70. DOI: 10.1016/j.atherosclerosis.2010.01.011
14. Yvan-Charvet L., Wang N., Tall A.R. Role of HDL, ABCA1, and ABCG1 transporters in cholesterol efflux and immune responses. Arterioscler Thromb Vasc Biol 2010;30(2):139–43. DOI: 10.1161/ATVBAHA.108.179283
15. Davis W. Jr. The ATP-binding cassette transporter-2 (ABCA2) overexpression modulates sphingosine levels and transcription of the amyloid precursor protein (APP) Gene. Curr Alzheimer Res 2015;12(9):847–59. DOI: 10.2174/156720501209151019105834
16. Michaki V., Guix F.X., Vennekens K. et al. Down-regulation of the ATP-binding cassette transporter 2 (Abca2) reduces amyloid-β production by altering Nicastrin maturation and intracellular localization. J Biol Chem 2012;287(2):1100–11. DOI: 10.1074/jbc.M111.288258
17. Hovnanian A. Harlequin ichthyosis unmasked: a defect of lipid transport. J Clin Invest 2005;115(7):1708–10. DOI: 10.1172/JCI25736
18. Thomas A.C., Cullup T., Norgett E.E. et al. ABCA12 is the major harlequin ichthyosis gene. J Invest Dermatol 2006;126(11):2408–13. DOI: 10.1038/sj.jid.5700455
19. de Vree J.M., Jacquemin E., Sturm E. et al. Mutations in the MDR3 gene cause progressive familial intrahepatic cholestasis. Proc Natl Acad Sci USA 1998;95(1):282–7. DOI: 10.1073/pnas.95.1.282
20. Zhang Y., Li F., Patterson A.D. et al. Abcb11 deficiency induces cholestasis coupled to impaired β-fatty acid oxidation in mice. J Biol Chem 2012;287(29):24784–94. DOI: 10.1074/jbc.M111.329318
21. Zhang C., Li D., Zhang J. et al. Mutations in ABCB6 cause dyschromatosis universalis hereditaria. J Invest Dermatol 2013;133(9):2221–8. DOI: 10.1038/jid.2013.145
22. Helias V., Saison C., Ballif B.A. et al. ABCB6 is dispensable for eryth- ropoiesis and specifies the new blood group system Langereis. Nat Genet 2012;44(2):170–3. DOI: 10.1038/ng.1069
23. Bekri S., Kispal G., Lange H. et al. Human ABC7 transporter: gene structure and mutation causing X-linked sideroblastic anemia with ataxia with disruption of cytosolic iron-sulfur protein maturation. Blood 2000;96(9):3256–64.
24. Maguire A., Hellier K., Hammans S. et al. X-linked cerebellar ataxia and sideroblastic anaemia associated with a missense mutation in the ABC7 gene predicting V411L. Br J Haematol 2001;115(4):910–7. DOI: 10.1046/j.1365-2141.2001.03015.x
25. Leslie E.M., Deeley R.G., Cole S.P. Multidrug resistance proteins: role of P-glycoprotein, MRP1, MRP2, and BCRP (ABCG2) in tissue defense. Toxicol Appl Pharmacol 2005;204(3):216–37. DOI: 10.1016/j.taap.2004.10.012
26. Bienengraeber M., Olson T.M., Selivanov V.A. et al. ABCC9 mutations identified in human dilated cardiomyopathy disrupt catalytic KATP channel gating. Nat Genet 2004;36(4):382–7. DOI: 10.1038/ng1329
27. Singareddy S.S., Roessler H.I., McClenaghan C. et al. ATP-sensitive potassium channels in zebrafish cardiac and vascular smooth muscle. J Physiol 2022;600(2):299–312. DOI: 10.1113/JP282157.
28. van Bon B.W., Gilissen C., Grange D.K. et al. Cantú syndrome is caused by mutations in ABCC9. Am J Hum Genet 2012;90(6):1094–101. DOI: 10.1016/j.ajhg.2012.04.014
29. Engelen M., Kemp S., de Visser M. et al. X-linked adrenoleukodystrophy (X-ALD): clinical presentation and guidelines for diagnosis, follow-up and management. Orphanet J Rare Dis 2012;7:51. DOI: 10.1186/1750-1172-7-51
30. Kemp S., Wanders R.J. X-linked adrenoleukodystrophy: very longchain fatty acid metabolism, ABC half-transporters and the complicated route to treatment. Mol Genet Metab 2007;90(3):268–76. DOI: 10.1016/j.ymgme.2006.10.001
31. Ferdinandusse S., Jimenez-Sanchez G., Koster J. et al. A novel bile acid biosynthesis defect due to a deficiency of peroxisomal ABCD3. Hum Mol Genet 2015;24(2):361–70. DOI: 10.1093/hmg/ddu448
32. Coelho D., Kim J.C., Miousse I.R. et al. Mutations in ABCD4 cause a new inborn error of vitamin B12 metabolism. Nat Genet 2012;44(10):1152–5. DOI: 10.1038/ng.2386
33. Deme J.C., Hancock M.A., Xia X. et al. Purification and interaction analyses of two human lysosomal vitamin B12 transporters: LMBD1 and ABCD4. Mol Membr Biol 2014;31(7–8):250–61. DOI: 10.3109/09687688.2014.990998
34. Lu K., Lee M.H., Hazard S. et al. Two genes that map to the STSL locus cause sitosterolemia: genomic structure and spectrum of mutations involving sterolin-1 and sterolin-2, encoded by ABCG5 and ABCG8, respectively. Am J Hum Genet 2001;69(2):278–90. DOI: 10.1086/321294
35. Hlavata I., Mohelnikova-Duchonova B., Vaclavikova R. et al. The role of ABC transporters in progression and clinical outcome of colorectal cancer. Mutagenesis 2012;27(2):187–96. DOI: 10.1093/mutage/ger075
36. Mohelnikova-Duchonova B., Brynychova V., Oliverius M. et al. Differences in transcript levels of ABC transporters between pancreatic adenocarcinoma and nonneoplastic tissues. Pancreas 2013;42(4):707–16. DOI: 10.1097/MPA.0b013e318279b861
37. Moore J.M., Bell E.L., Hughes R.O. et al. ABC transporters: human disease and pharmacotherapeutic potential. Trends Mol Med 2023;29(2):152–72. DOI: 10.1016/j.molmed.2022.11.001
38. Zhao X., Guo Y., Yue W. et al. ABCC4 is required for cell proliferation and tumorigenesis in non-small cell lung cancer. Onco Targets Ther 2014;7:343–51. DOI: 10.2147/OTT.S56029
39. Zheng S., Liu D., Wang F. et al. ABCA12 promotes proliferation and migration and inhibits apoptosis of pancreatic cancer cells through the AKT signaling pathway. Front Genet 2022;13:906326. DOI: 10.3389/fgene.2022.906326
40. Demidenko R., Razanauskas D., Daniunaite K. et al. Frequent down-regulation of ABC transporter genes in prostate cancer. BMC Cancer. 2015;15:683. DOI: 10.1186/s12885-015-1689-8
41. Andersen V., Svenningsen K., Knudsen L.A. et al. Novel understanding of ABC transporters ABCB1/ MDR/P-glycoprotein, ABCC2/MRP2, and ABCG2/BCRP in colorectal pathophysiology. World J Gastroenterol 2015;21(41):11862–76. DOI: 10.3748/wjg.v21.i41.11862
42. Begicevic R.R., Falasca M. ABC transporters in cancer stem cells: beyond chemoresistance. Int J Mol Sci 2017;18(11):2362. DOI: 10.3390/ijms18112362
43. Bradley G., Sharma R., Rajalakshmi S. et al. P-glycoprotein expression during tumor progression in the rat liver. Cancer Res 1992;52(19):5154–61.
44. Skinner K.T., Palkar A.M., Hong A.L. Genetics of ABCB1 in Cancer. Cancers (Basel). 2023;15(17):4236. DOI: 10.3390/cancers15174236.
45. Abe T., Mori T., Wakabayashi Y. et al. Expression of multidrug resistance protein gene in patients with glioma after chemotherapy. J Neurooncol 1998;40(1):11–8. DOI: 10.1023/a:1005954406809
46. Kunická T., Souček P. Importance of ABCC1 for cancer therapy and prognosis. Drug Metab Rev 2014;46(3):325–42. DOI: 10.3109/03602532.2014.901348
47. Andersen V., Vogel L.K., Kopp T.I. et al. High ABCC2 and low ABCG2 gene expression are early events in the colorectal adenomacarcinoma sequence. PLoS One 2015;10(3):e0119255. DOI: 10.1371/journal.pone.0119255
48. Cervenkova L., Vycital O., Bruha J. et al. Protein expression of ABCC2 and SLC22A3 associates with prognosis of pancreatic adenocarcinoma. Sci Rep 2019;9(1):19782. DOI: 10.1038/s41598-019-56059-w
49. Chen Y., Zhou H., Yang S. et al. Increased ABCC2 expression predicts cisplatin resistance in non-small cell lung cancer. Cell Biochem Funct 2021;39(2):277–86. DOI: 10.1002/cbf.3577
50. Li J., Zhang J.T., Jiang X. et al. The cystic fibrosis transmembrane conductance regulator as a biomarker in non-small cell lung cancer. Int J Oncol 2015;46(5):2107–15. DOI: 10.3892/ijo.2015.2921
51. Wu Z., Peng X., Li J. et al. Constitutive activation of nuclear factor κB contributes to cystic fibrosis transmembrane conductance regulator expression and promotes human cervical cancer progression and poor prognosis. Int J Gynecol Cancer 2013;23(5):906–15. DOI: 10.1097/IGC.0b013e318292da82
52. Xu J., Yong M., Li J. et al. High level of CFTR expression is associated with tumor aggression and knockdown of CFTR suppresses proliferation of ovarian cancer in vitro and in vivo. Oncol Rep 2015;33(5):2227–34. DOI: 10.3892/or.2015.3829
53. Zhang J.T., Jiang X.H., Xie C. et al. Downregulation of CFTR promotes epithelial-to-mesenchymal transition and is associated with poor prognosis of breast cancer. Biochim Biophys Acta 2013;1833(12):2961–9. DOI: 10.1016/j.bbamcr.2013.07.021
54. Theodoulou F.L., Kerr I.D. ABC transporter research: going strong 40 years on. Biochem Soc Trans 2015;43(5):1033–40. DOI: 10.1042/BST20150139
55. Linton K.J. Structure and function of ABC transporters. Physiology (Bethesda) 2007;22:122–30. DOI: 10.1152/physiol.00046.2006
56. Литвяков Н.В., Цыганов М.М. Клинические исследования вклада ABC-транспортеров в реализацию фенотипа множественной лекарственной устойчивости рака молочной железы. Вопросы онкологии 2016;62(1):45–52.
57. Badiee S.A., Isu U.H., Khodadadi E. et al. The alternating access mechanism in mammalian multidrug resistance transporters and their bacterial homologs. Membranes 2023;13(6):568. DOI: 10.3390/membranes13060568
58. Shaikh S., Wen P.C., Enkavi G. et al. Capturing functional motions of membrane channels and transporters with molecular dynamics simulation. J Comput Theor Nanosci 2010;7(12):2481–500. DOI: 10.1166/jctn.2010.1636
59. George A.M., Jones P.M. Perspectives on the structure-function of ABC transporters: the Switch and Constant Contact models. Prog Biophys Mol Biol 2012;109(3):95–107. DOI: 10.1016/j.pbiomolbio.2012.06.003
60. Higgins C.F., Linton K.J. The ATP switch model for ABC transporters. Nat Struct Mol Biol 2004;11(10):918–26. DOI: 10.1038/nsmb836
61. Jones P.M., George A.M. Mechanism of the ABC transporter ATPase domains: catalytic models and the biochemical and biophysical record. Crit Rev Biochem Mol Biol 2013;48(1):39–50. DOI: 10.3109/10409238.2012.735644
62. Mochida Y., Taguchi K., Taniguchi S. et al. The role of P-glycoprotein in intestinal tumorigenesis: disruption of mdr1a suppresses polyp formation in Apc(Min/+) mice. Carcinogenesis 2003;24(7):1219–24. DOI: 10.1093/carcin/bgg073
63. Henderson M.J., Haber M., Porro A. et al. ABCC multidrug transporters in childhood neuroblastoma: clinical and biological effects independent of cytotoxic drug efflux. J Natl Cancer Inst 2011;103(16):1236–51. DOI: 10.1093/jnci/djr256
64. Yamada A., Ishikawa T., Ota I. et al. High expression of ATP-binding cassette transporter ABCC11 in breast tumors is associated with aggressive subtypes and low disease-free survival. Breast Cancer Res Treat 2013;137(3):773–82. DOI: 10.1007/s10549-012-2398-5
65. Omran O.M. The prognostic value of breast cancer resistance protein (BCRB/ABCG2) expression in breast carcinomas. J Environ Pathol Toxicol Oncol 2012;31(4):367–76. DOI: 10.1615/jenvironpatholtoxicoloncol.2013006767
66. Xiang L., Su P., Xia S. et al. ABCG2 is associated with HER-2 expression, lymph node metastasis and clinical stage in breast invasive ductal carcinoma. Diagn Pathol 2011;6:90. DOI: 10.1186/1746-1596-6-90
67. Liu T., Li Z., Zhang Q. et al. Targeting ABCB1 (MDR1) in multidrug resistant osteosarcoma cells using the CRISPR-Cas9 system to reverse drug resistance. Oncotarget 2016;7(50):83502–13. DOI: 10.18632/oncotarget.13148
68. Serra M., Pasello M., Manara M.C. et al. May P-glycoprotein status be used to stratify high-grade osteosarcoma patients? Results from the Italian/Scandinavian Sarcoma Group 1 treatment protocol. Int J Oncol 2006;29(6):1459–68.
69. Nobili S., Lapucci A., Landini I. et al. Role of ATP-binding cassette transporters in cancer initiation and progression. Semin Cancer Biol 2020;60:72–95. DOI: 10.1016/j.semcancer.2019.08.006
70. Jiang Z.S., Sun Y.Z., Wang S.M. et al. Epithelial-mesenchymal transition: potential regulator of ABC transporters in tumor progression. J Cancer 2017;8(12):2319–27. DOI: 10.7150/jca.19079
71. Stewart T.A., Azimi I., Thompson E.W. et al. A role for calcium in the regulation of ATP-binding cassette, sub-family C, member 3 (ABCC3) gene expression in a model of epidermal growth factor-mediated breast cancer epithelial-mesenchymal transition. Biochem Biophys Res Commun 2015;458(3):509–14. DOI: 10.1016/j.bbrc.2015.01.141
72. Tian Y., Tian X., Han X. et al. Expression of ATP binding cassette E1 enhances viability and invasiveness of lung adenocarcinoma cells in vitro. Mol Med Rep 2016;14(2):1345–50. DOI: 10.3892/mmr.2016.5388
73. Цыганов М.М., Цыденова И.А., Маркович В.А. и др. Экспрессионная гетерогенность генов семейства ABC-транспортеров и генов химиочувствительности в опухоли желудка, канцероматозе и метастазах в лимфатические узлы. Успехи молекулярной онкологии 2022;9(4):78–88. DOI: 10.17650/2313-805X-2022-9-4-78-88
74. Цыганов М.М., Ибрагимова М.К., Певзнер А.М. и др. Анализ экспрессии генов семейства ABC-транспортеров в опухоли молочной железы: связь с эффективностью химиотерапии и прогнозом заболевания. Успехи молекулярной онкологии 2020;7(2):29–38. DOI: 10.17650/2313-805X-2020-7-2-29-38
75. Durmus S., Hendrikx J.J., Schinkel A.H. Apical ABC transporters and cancer chemotherapeutic drug disposition. Adv Cancer Res 2015;125:1–41. DOI: 10.1016/bs.acr.2014.10.001
76. Leonard G.D., Fojo T., Bates S.E. The role of ABC transporters in clinical practice. Oncologist 2003;8(5):411–24. DOI: 10.1634/theoncologist.8-5-411
77. Mo W., Zhang J.T. Human ABCG2: structure, function, and its role in multidrug resistance. Int J Biochem Mol Biol 2012;3(1):1–27.
78. Xiao H., Zheng Y., Ma L. et al. Clinically-relevant ABC transporter for anti-cancer drug resistance. Front Pharmacol 2021;12:648407. DOI: 10.3389/fphar.2021.648407
79. Lhommé C., Joly F., Walker J.L. et al. Phase III study of valspodar (PSC 833) combined with paclitaxel and carboplatin compared with paclitaxel and carboplatin alone in patients with stage IV or suboptimally debulked stage III epithelial ovarian cancer or primary peritoneal cancer. J Clin Oncol 2008;26(16):2674–82. DOI: 10.1200/JCO.2007.14.9807
80. Adamska A., Falasca M. ATP-binding cassette transporters in progression and clinical outcome of pancreatic cancer: What is the way forward? World J Gastroenterol 2018;24(29):3222–38. DOI: 10.3748/wjg.v24.i29.3222
81. Boichuk S., Dunaev P., Mustafin I. et al. Infigratinib (BGJ 398), a Pan-FGFR inhibitor, targets P-glycoprotein and increases chemotherapeutic-induced mortality of multidrug-resistant tumor cells. Biomedicines 2022;10(3):601. DOI: 10.3390/biomedicines10030601
82. Tamaki A., Ierano C., Szakacs G. et al. The controversial role of ABC transporters in clinical oncology. Essays Biochem 2011;50(1):209–32. DOI: 10.1042/bse0500209
83. Cripe L.D., Uno H., Paietta E.M. et al. Zosuquidar, a novel modulator of P-glycoprotein, does not improve the outcome of older patients with newly diagnosed acute myeloid leukemia: a randomized, placebo-controlled trial of the Eastern Cooperative Oncology Group 3999. Blood 2010;116(20):4077–85. DOI: 10.1182/blood-2010-04-277269
84. Xu T., Guo P., He Y. et al. Application of curcumin and its derivatives in tumor multidrug resistance. Phytother Res 2020;34(10): 2438–58. DOI: 10.1002/ptr.6694
85. Gonçalves B.M.F., Cardoso D.S.P., Ferreira U.M.J. Overcoming multidrug resistance: flavonoid and terpenoid nitrogen-containing derivatives as ABC transporter modulators. Molecules 2020;25(15):3364. DOI: 10.3390/molecules25153364
86. Kelly R.J., Draper D., Chen C.C. et al. A pharmacodynamic study of docetaxel in combination with the P-glycoprotein antagonist tariquidar (XR9576) in patients with lung, ovarian, and cervical cancer. Clin Cancer Res 2011;17(3):569–80. DOI: 10.1158/1078-0432.CCR-10-1725
87. Palmeira A., Sousa E., Vasconcelos M.H. et al. Three decades of P-gp inhibitors: skimming through several generations and scaffolds. Curr Med Chem 2012;19(13):1946–2025. DOI: 10.2174/092986712800167392
88. Dury L., Nasr R., Lorendeau D. et al. Flavonoid dimers are highly potent killers of multidrug resistant cancer cells overexpressing MRP1. Biochem Pharmacol 2017;124:10–8. DOI: 10.1016/j.bcp.2016.10.013
89. Ni K., Yang L., Wan C. et al. Flavonostilbenes from Sophora alopecuroides L. as multidrug resistance associated protein 1 (MRP1) inhibitors. Nat Prod Res 2014;28(23):2195–8. DOI: 10.1080/14786419.2014.930856
90. Chen J.R., Jia X.H., Wang H. et al. Timosaponin A-III reverses multi-drug resistance in human chronic myelogenous leukemia K562/ADM cells via downregulation of MDR1 and MRP1 expression by inhibiting PI3K/Akt signaling pathway. Int J Oncol 2016;48(5):2063–70. DOI: 10.3892/ijo.2016.3423
91. Ji L., Liu X., Zhang S. et al. The Novel triazolonaphthalimide derivative LSS-11 synergizes the anti-proliferative effect of paclitaxel via STAT3-dependent MDR1 and MRP1 downregulation in chemo- resistant lung cancer cells. Molecules 2017;22(11):1822. DOI: 10.3390/molecules22111822
92. Antoni F., Bause M., Scholler M. et al. Tariquidar-related triazoles as potent, selective and stable inhibitors of ABCG2 (BCRP). Eur J Med Chem 2020;191:112133. DOI: 10.1016/j.ejmech.2020.112133
93. Weidner L.D., Zoghbi S.S., Lu S. et al. The inhibitor Ko143 is not specific for ABCG2. J Pharmacol Exp Ther 2015;354(3):384–93. DOI: 10.1124/jpet.115.225482
94. Tsuruo T., Iida H., Tsukagoshi S. et al. Overcoming of vincristine resistance in P388 leukemia in vivo and in vitro through enhanced cytotoxicity of vincristine and vinblastine by verapamil. Cancer Res 1981;41(5):1967–72.
95. Wang L., Sun Y. Efflux mechanism and pathway of verapamil pumping by human P-glycoprotein. Arch Biochem Biophys 2020;696:108675. DOI: 10.1016/j.abb.2020.108675
96. Borska S., Chmielewska M., Wysocka T. et al. In vitro effect of quercetin on human gastric carcinoma: targeting cancer cells death and MDR. Food Chem Toxicol 2012;50(9):3375–83. DOI: 10.1016/j.fct.2012.06.035
97. Chen Y.Y., Chang Y.M., Wang K.Y. et al. Naringenin inhibited migration and invasion of glioblastoma cells through multiple mechanisms. Environ Toxicol 2019;34(3):233–9. DOI: 10.1002/tox.22677
98. Eid S.Y., El-Readi M.Z., Wink M. Synergism of three-drug combinations of sanguinarine and other plant secondary metabolites with digitonin and doxorubicin in multi-drug resistant cancer cells. Phytomedicine 2012;19(14):1288–97. DOI: 10.1016/j.phymed.2012.08.010
99. Jain S., Laphookhieo S., Shi Z. et al. Reversal of P-glycoproteinmediated multidrug resistance by sipholane triterpenoids. J Nat Prod 2007;70(6):928–31. DOI: 10.1021/np0605889
100. Pires M.M., Emmert D., Hrycyna C.A. et al. Inhibition of P-glycoprotein-mediated paclitaxel resistance by reversibly linked quinine homodimers. Mol Pharmacol 2009;75(1):92–100. DOI: 10.1124/mol.108.050492
101. Zhang Y., Guo L., Huang J. et al. Inhibitory effect of berberine on broiler P-glycoprotein expression and function: in situ and in vitro studies. Int J Mol Sci 2019;20(8):1966. DOI: 10.3390/ijms20081966
102. Choi Y.H., Yu A.M. ABC transporters in multidrug resistance and pharmacokinetics, and strategies for drug development. Curr Pharm Des 2014;20(5):793–807. DOI: 10.2174/138161282005140214165212
103. Beretta G.L., Cassinelli G., Pennati M. et al. Overcoming ABC transporter-mediated multidrug resistance: the dual role of tyrosine kinase inhibitors as multitargeting agents. Eur J Med Chem 2017;142:271–89. DOI: 10.1016/j.ejmech.2017.07.062
104. Kathawala R.J., Gupta P., Ashby C.R. Jr. et al. The modulation of ABC transporter-mediated multidrug resistance in cancer: a review of the past decade. Drug Resist Updat 2015;18:1–17. DOI: 10.1016/j.drup.2014.11.002
105. Callaghan R., Higgins C.F. Interaction of tamoxifen with the multidrug resistance P-glycoprotein. Br J Cancer 1995;71(2):294–9. DOI: 10.1038/bjc.1995.59
106. Liu Z.H., Ma Y.L., He Y.P. et al. Tamoxifen reverses the multi-drugresistance of an established human cholangiocarcinoma cell line in combined chemotherapeutics. Mol Biol Rep 2011;38(3):1769–75. DOI: 10.1007/s11033-010-0291-z
107. Богуш Т.А., Дудко Е.А., Богуш Е.А. и др. Молекулярные мишени тамоксифена, отличные от эстрогеновых рецепторов. Антибиотики и химиотерапия 2012;57(1–2):50–8.
108. Bakadlag R., Limniatis G., Georges G. et al. The anti-estrogen receptor drug, tamoxifen, is selectively lethal to P-glycoprotein expressing multidrug resistant tumor cells. BMC Cancer 2023;23(1):24. DOI: 10.1186/s12885-022-10474-x
109. Shen L.Z., Hua Y.B., Yu X.M. et al. Tamoxifen can reverse multidrug resistance of colorectal carcinoma in vivo. World J Gastroenterol 2005;11(7):1060–4. DOI: 10.3748/wjg.v11.i7.1060
110. Wen S., Fu X., Li G. et al. Efficacy of tamoxifen in combination with docetaxel in patients with advanced non-small-cell lung cancer pretreated with platinum-based chemotherapy. Anticancer Drugs 2016;27(5):447–56. DOI: 10.1097/CAD.0000000000000350
Рецензия
Для цитирования:
Бойчук С.В., Ивойлова Т.В. Роль ABC-транспортеров в поддержании гомеостаза, патогенезе и терапии онкологических заболеваний. Успехи молекулярной онкологии. 2024;11(1):8-21. https://doi.org/10.17650/2313-805X-2024-11-1-8-21
For citation:
Boichuk S.V., Ivoilova T.V. The role of ABC-transporters in homeostasis, cancer pathogenesis and therapy. Advances in Molecular Oncology. 2024;11(1):8-21. (In Russ.) https://doi.org/10.17650/2313-805X-2024-11-1-8-21