Значение иммунодефицитных мышей для экспериментальных и доклинических исследований в онкологии
Реферат
Важную роль в исследованиях по разработке средств противоопухолевой терапии играют модели in vivo, созданные с использованием различных линий мышей. Адекватно выбранная модель позволяет в достаточной степени оценить значимость воздействия изучаемого вещества на молекулярные мишени, ее влияние на рост и жизнеспособность опухоли, а также выявить терапевтическое окно между эффективностью лечения и токсичностью. Ксенотрансплантаты опухолей человека, пересаживаемые иммунодефицитным мышам, представляют собой одну из наиболее востребованных моделей для изучения туморогенеза и эффективности противоопухолевых воздействий. Иммунодефицитный статус животных-реципиентов является обязательным условием для предотвращения отторжения опухолевого материала другого биологического вида. В настоящее время разработано большое количество различных линий мышей, отличающихся различной степенью дефектов иммунной системы, а также имеющих различные фено- и генотипические характеристики. Выбор линии животного для создания модели зависит от задач научного исследования. Успех эксперимента непосредственно зависит от правильного выбора линии экспериментальных животных.
Тэги
1. Трещалина Е.М., Жукова О.С., Герасимова Г.К., Андронова Н.В., Гарин А.М. Методические рекомендации по доклиническому изучению противоопухолевой активности лекарственных средств. Руководство по проведению доклинических исследований лекарственных средств. Ч. 1. М.: Гриф и К, 2012. 642–657.
Treshchalina E.M. Zhukova O.S., Gerasimova G.K., Andronova N.V., Garin A.M. Guidelines for the preclinical study of the antitumor activity of drugs. Preclinical Drug Research Guide. Part 1. Moscow: Grif i K, 2012. 642–657. [In Russian].
2. Gould S.E., Junttila M.R., de Sauvage F.J. Translational value of mouse models in oncology drug development. Nat. Med. 2015; 21 (5): 431–439. doi: 10.1038/nm.3853
3. Rangarajan A., Weinberg R.A. Comparative biology of mouse versus human cells: modelling human cancer in mice. Nat. Rev. Cancer. 2003; 3 (12): 952–959. doi: 10.1038/nrc1235
4. Kelland L.R. «Of mice and men»: values and liabilities of the athymic nude mouse model in anticancer drug development. Eur. J. Cancer. 2004; 40 (6): 827–836. doi: 10.1016/j.ejca.2003.11.028
5. Giovanella B.C., Fogh J. The nude mouse in cancer research. Adv. Cancer Res. 1985; 44: 69–120. doi: 10.1016/S0065-230X(08)60026-3
6. O’Connell M.P., Marchbank K., Webster M.R., Valiga A.A., Kaur A., Vultur A., Li L., Herlyn M., Villanueva J., Liu Q., Yin X., Widura S., Nelson J., Ruiz N., Camilli T.C., Indig F.E., Flaherty K.T., Wargo J.A., Frederick D.T., Cooper Z.A., Nair S., Amaravadi R.K., Schuchter L.M., Karakousis G.C., Xu W., Xu X., Weeraratna A.T. Hypoxia induces phenotypic plasticity and therapy resistance in melanoma via the tyrosine kinase receptors ROR1 and ROR2. Cancer Discov. 2013; 3 (12): 1378–1393. doi: 10.1158/2159-8290.CD-13-0005
7. Szadvari I., Krizanova O., Babula P. Athymic nude mice as an experimental model for cancer treatment. Physiol. Res. 2016; 65 (4): 441–453. doi: 10.33549/physiolres.933526
8. Holub M. The nude mouse. ILAR J. 1992; 34 (1-2): 1–3. doi: 10.1093/ilar.34.1-2.1
9. Hong H.K., Noveroske J.K., Headon D.J., Liu T., Sy M.S., Justice M.J., Chakravarti A. The winged helix/forkhead transcription factor Foxq1 regulates differentiation of hair in satin mice. Genesis. 2001; 29 (4): 163–171. doi: 10.1002/gene.1020
10. Bankert R.B., Egilmez N.K., Hess S.D. Human–SCID mouse chimeric models for the evaluation of anti-cancer therapies. Trends Immunol. 2001; 22 (7): 386–393. doi: 10.1016/s1471-4906(01)01943-3
11. Fugmann S.D. RAG1 and RAG2 in V (D) J recombination and transposition. Immunol. Res. 2001; 23 (1): 23–39. doi: 10.1385/IR:23:1:23
12. Mekada K., Abe K., Murakami A., Nakamura S., Nakata H., Moriwaki K., Obata Y., Yoshiki A. Genetic differences among C57BL/6 substrains. Exp. Anim. 2009; 58 (2): 141–149. doi: 10.1538/expanim.58.141
13. Vladutiu A.O. The severe combined immunodeficient (SCID) mouse as a model for the study of autoimmune diseases. Clin. Exp. Immunol. 1993; 93 (1): 1–8. doi: 10.1111/j.1365-2249.1993.tb06488.x
14. Lee J.H., Park J.H., Nam T.W., Seo S.M., Kim J.Y., Lee H.K., Han J.H., Park S.Y., Choi Y.K., Lee H.W. Differences between immunodeficient mice generated by classical gene targeting and CRISPR/Cas9-mediated gene knockout. Transgenic Res. 2018; 27 (3): 1–11. doi: 10.1007/s11248-018-0069-y
15. Fischer A. Severe combined immunodeficiencies (SCID). Clin. Exp. Immunol. 2000; 122 (2): 143–149. doi: 10.1046/j.1365-2249.2000.01359.x
16. Jung J., Seol H.S., Chang S. The generation and application of patient-derived xenograft model for cancer research. Cancer Res. Treat. 2018; 50 (1): 1. doi: 10.4143/crt.2017.307
17. De Camargo M.M., Nahum L.A. Adapting to a changing world: RAG genomics and evolution. Hum. Genomics. 2005; 2 (2): 132–137. doi: 10.1186/1479-7364-2-2-132
18. Mehalow A.K., Kameya S., Smith R.S., Hawes N.L., Denegre J.M., Young J.A., Bechtold L., Haider N.B., Tepass U., Heckenlively J.R., Chang B., Naggert J.K., Nishina P.M. CRB1 is essential for external limiting membrane integrity and photoreceptor morphogenesis in the mammalian retina. Hum. Mol. Genet. 2003; 12 (17): 2179–2189. doi: 10.1093/hmg/ddg232
19. Huang T.T., Naeemuddin M., Elchuri S., Yamaguchi M., Kozy H.M., Carlson E.J., Epstein C.J. Genetic modifiers of the phenotype of mice deficient in mitochondrial superoxide dismutase. Hum. Mol. Genet. 2006; 15 (7): 1187–1194. doi: 10.1093/hmg/ddl034
20. Leiter E.H. The NOD mouse: a model for analyzing the interplay between heredity and environment in development of autoimmune disease. ILAR J. 1993; 35 (1): 4–14. doi: 10.1093/ilar.35.1.4
21. Watanabe Y., Takahashi T., Okajima A., Shiokawa M., Ishii N., Katano I., Ito R, Ito M., Minegishi M., Minegishi N., Tsuchiya S., Sugamura K. The analysis of the functions of human B and T cells in humanized NOD/shi-scid/γcnull (NOG) mice (hu-HSC NOG mice). Int. Immunol. 2009; 21 (7): 843–858. doi: 10.1093/intimm/dxp050
22. Bente D.A., Melkus M.W., Garcia J.V., Rico-Hesse R. Dengue fever in humanized NOD/SCID mice. J. Virol. 2005; 79 (21): 13797–13799. doi: 10.1128/JVI.79.21.13797-13799.2005
23. Anderson M.S., Bluestone J.A. The NOD mouse: a model of immune dysregulation. Annu. Rev. Immunol. 2005; 23: 447–485. doi: 10.1146/annurev.immunol.23.021704.115643
24. Shultz L.D., Goodwin N., Ishikawa F., Hosur V., Lyons B.L., Greiner D.L. Human cancer growth and therapy in NOD/SCID/IL2Rγnull (NSG) mice. Cold Spring Harb. Protoc. 2014; 2014 (7): 694–708. doi: 10.1101/pdb.top073585
25. Puchalapalli M., Zeng X., Mu L., Anderson A., Glickman L.H., Zhang M., Sayyad M.R., Mosticone Wangensteen S., Clevenger C.V., Koblinski J.E. NSG mice provide a better spontaneous model of breast cancer metastasis than athymic (nude) mice. PLoS One. 2016; 11 (9): e0163521. doi: 10.1371/journal.pone.0163521
26. Sweeney C.L., Choi U., Liu C., Koontz S., Ha S.K., Malech H.L. CRISPR-mediated knockout of Cybb in NSG mice establishes a model of chronic granulomatous disease for human stem-cell gene therapy transplants. Hum. Gene Ther. 2017; 28 (7): 565–575. doi: 10.1089/hum.2017.005
27. Ohbo K., Suda T., Hashiyama M., Mantani A., Ikebe M., Miyakawa K., Moriyama M., Nakamura M., Katsuki M., Takahashi K., Yamamura K., Sugamura K. Modulation of hematopoiesis in mice with a truncated mutant of the interleukin-2 receptor gamma chain. Blood. 1996; 87 (3): 956–967.
28. Pearson T., Greiner D.L., Shultz L.D. Creation of «humanized» mice to study human immunity. Curr. Protoc. Immunol. 2008; 81 (1): 15–21. doi: 10.1002/0471142735.im1521s81
29. Inoue M., Senju S., Hirata S., Irie A., Baba H., Nishimura Y. An in vivo model of priming of antigen-specific human CTL by Mo-DC in NOD/Shi-scid IL2rγnull (NOG) mice. Immunol. Lett. 2009; 126 (1-2): 67–72. doi: 10.1016/j.imlet.2009.08.001
30. Yasuda M., Ogura T., Goto T., Yagoto M., Kamai Y., Shimomura C., Hayashimoto N., Kiyokawa Y., Shinohara H., Takahashi R., Kawai K. Incidence of spontaneous lymphomas in non-experimental NOD/Shi-scid, IL-2Rγnull (NOG) mice. Exp. Anim. 2017; 66 (4): 425–435. doi: 10.1538/expanim.17-0034
31. Holen I., Speirs V., Morrissey B., Blyth K. In vivo models in breast cancer research: progress, challenges and future directions. Dis. Model Mech. 2017; 10 (4): 359–371. doi: 10.1242/dmm.028274
32. Lallo A., Frese K.K., Morrow C.J., Sloane R., Gulati S., Schenk M.W., Trapani F., Simms N., Galvin M., Brown S., Hodgkinson C.L., Priest L., Hughes A., Lai Z., Cadogan E., Khandelwal G., Simpson K.L., Miller C., Blackhall F., O’Connor M.J., Dive C. The combination of the PARP inhibitor olaparib and the Wee1 inhibitor AZD1775 as a new therapeutic option for small cell lung cancer. Clin. Cancer Res. 2018; 24 (20): 5153–5164. doi: 10.1158/1078-0432.CCR-17-2805
33. Zhang S., Zheng C., Zhu W., Xiong P., Zhou D., Huang C., Zheng D. A novel anti-DR5 antibody-drug conjugate possesses a high-potential therapeutic efficacy for leukemia and solid tumors. Theranostics. 2019; 9 (18): 5412–5423. doi: 10.7150/thno.33598
34. Lowery C.D., Dowless M., Renschler M., Blosser W., VanWye A.B., Stephens J.R., Iversen P.W., Lin A.B., Beckmann R.P., Krytska K., Cole K.A., Maris J.M., Hawkins D.S., Rubin B.P., Kurmasheva R.T., Houghton P.J., Gorlick R., Kolb E.A., Kang M.H., Reynolds C.P., Erickson S.W., Teicher B.A., Smith M.A., Stancato L.F. Broad spectrum activity of the checkpoint kinase 1 inhibitor prexasertib as a single agent or chemopotentiator across a range of preclinical pediatric tumor models. Clin. Cancer Res. 2019; 25 (7): 2278–2289. doi: 10.1158/1078-0432.CCR-18-2728
35. Dowless M., Lowery C.D., Shackleford T., Renschler M., Stephens J., Flack R., Blosser W., Gupta S., Stewart J., Webster Y., Dempsey J., VanWye A.B., Ebert P., Iversen P., Olsen J.B., Gong X., Buchanan S., Houghton P., Stancato L. Abemaciclib is active in preclinical models of ewing sarcoma via multipronged regulation of cell cycle, DNA methylation, and interferon pathway signaling. Clin. Cancer Res. 2018; 24 (23): 6028–6039. doi: 10.1158/1078-0432.CCR-18-1256
36. Xie J., Lin Y. Patient-derived xenograft models for personalized medicine in colorectal cancer. Clin. Exp. Med. 2020; 20 (4): 167–172. doi: 10.1007/s10238-020-00609-4
37. Klinghammer K., Walther W., Hoffmann J. Choosing wisely–Preclinical test models in the era of precision medicine. Cancer Treatment Rev. 2017; 55: 36–45. doi: 10.1016/j.ctrv.2017.02.009
38. Кит С.О., Максимов А.Ю., Гончарова А.С., Колесников Е.Н., Санамянц С.В., Кациева Т.Б., Мягков Р.Е., Лукбанова Е.А., Карнаухов Н.С., Ткачев С.Ю., Протасова Т.П., Заикина Е.В., Волкова А.В., Ходакова Д.В., Миндарь М.В. Особенности роста пациентоподобных подкожных и ортотопических ксенографтов кардиоэзофагеального рака человека на иммунодефицитных мышах. Соврем. пробл. науки и образования. 2020; (2). URL https://science-education.ru/ru/article/view?id=29573
Kit S.O., Maksimov A.Yu., Goncharova A.S., Kolesnikov E.N., Sanamyants S.V., Katsieva T.B., Myagkov R.E., Lukbanova E.A., Karnaukhov N.S., Tkachev S.Yu., Protasova T.P., Zaikina E.V., Volkova A.V., Khodakova D.V., Mindar M.V. Growth characteristics of patient-like subcutaneous and orthotopic xenografts of human cardioesophageal cancer in immunodeficient mice. Sovremennye problemy nauki i obrazovaniya = Modern Problems of Science and Education. 2020; (2). URL: https://science-education.ru/ru/article/view?id=29573 [In Russian].
39. Chen Q., Wei T., Wang J., Zhang Q., Li J., Zhang J., Ni L., Wang Y., Bai X., Liang T. Patient-derived xenograft model engraftment predicts poor prognosis after surgery in patients with pancreatic cancer. Pancreatology. 2020; 20 (3): 485–492. doi: 10.1016/j.pan.2020.02.008
40. Okano M., Oshi M., Butash A., Okano I., Saito K., Kawaguchi T., Nagahashi M., Kono K., Ohtake T., Takabe K. Orthotopic implantation achieves better engraftment and faster growth than subcutaneous implantation in breast cancer patient-derived xenografts. J. Mammary Gland Biol. Neoplasia. 2020; 25 (1): 27–36. doi: 10.1007/s10911-020-09442-7
41. Wu P., Xu R., Chen X., Zhao Y., Tan D., Zhao Y., Qin W., Zhang C., Ge X., Shi C. Establishment and characterization of patient-derived xenografts for hormone-naïve and castrate-resistant prostate cancers to improve treatment modality evaluation. Aging (Albany NY). 2020; 12 (4): 3848–3861. doi: 10.18632/aging.102854
42. Wang M., Yao L.C., Cheng M., Cai D., Martinek J., Pan C.X., Shi W., Ma A.H., de Vere White R.W., Airhart S., Liu E.T., Banchereau J., Brehm M.A., Greiner D.L., Shultz L.D., Palucka K., Keck J.G. Humanized mice in studying efficacy and mechanisms of PD-1-targeted cancer immunotherapy. FASEB J. 2018; 32 (3): 1537–1549. doi: 10.1096/fj.201700740R
43. Kuryk L., Møller A.S.W., Jaderberg M. Combination of immunogenic oncolytic adenovirus ONCOS-102 with anti-PD-1 pembrolizumab exhibits synergistic antitumor effect in humanized A2058 melanoma huNOG mouse model. Oncoimmunology. 2019; 8 (2): e1532763. doi: 10.1080/2162402X.2018.1532763
44. Zhou Z.F., Peng F., Li J.Y., Ye Y.B. Intratumoral IL-12 gene therapy inhibits tumor growth in A HCC-Hu-PBL-NOD/SCID murine model. Onco Targets Ther. 2019; 12: 7773–7784. doi: 10.2147/OTT.S222097
45. Belizário J.E. Immunodeficient mouse models: an overview. Open Immunol. J. 2009; 2 (1): 79–85. doi: 10.2174/1874226200902010079
46. Georges L.M.C., de Wever O., Galván J.A., Dawson H., Lugli A., Demetter P., Zlobec I. Cell line derived xenograft mouse models are a suitable in vivo model for studying tumor budding in colorectal cancer. Front. Med. 2019; 6: 139. doi: 10.3389/fmed.2019.00139
47. Marques da Costa M.E., Daudigeos-Dubus E., Gomez-Brouchet A., Bawa O., Rouffiac V., Serra M., Scotlandi K., Santos C., Geoerge B., Gaspar N. Establishment and characterization of in vivo orthotopic bioluminescent xenograft models from human osteosarcoma cell lines in Swiss nude and NSG mice. Cancer Med. 2018; 7 (3): 665–676. doi: 10.1002/cam4.1346
48. Feng B., Zhu Y., Sun C., Su Z., Tang L., Li C., Zheng G. Basil polysaccharide inhibits hypoxia-induced hepatocellular carcinoma metastasis and progression through suppression of HIF-1α-mediated epithelial-mesenchymal transition. Int. J. Biol. Macromol. 2019; 137: 32–44. doi: 10.1016/j.ijbiomac.2019.06.189
49. Vishnoi M., Liu N.H., Yin W., Boral D., Scamardo A., Hong D., Marchetti D. The identification of a TNBC liver metastasis gene signature by sequential CTC-xenograft modeling. Mol. Oncol. 2019; 13 (9): 1913–1926. doi: 10.1002/1878-0261.12533
50. Blomme A., Van Simaeys G., Doumont G., Costanza B., Bellier J., Otaka Y., Sherer F., Lovinfosse P., Boutry S., Palacios A.P., de Pauw E., Hirano T., Yokobori T., Hustinx R., Bellahcène A., Delvenne P., Detry O., Goldman S., Nishiyama M., Castronovo V., Turtoi A. Murine stroma adopts a human-like metabolic phenotype in the PDX model of colorectal cancer and liver metastases. Oncogene. 2018; 37 (9): 1237–1250. doi: 10.1038/s41388-017-0018-x
51. Bertin H., Guilho R., Brion R., Amiaud J., Battaglia S., Moreau A., Gomez A.B., Longis J., Piot B., Heymann D., Corre P., Rédini F. Jaw osteosarcoma models in mice: first description. J. Transl. Med. 2019; 17 (1): 56. doi: 10.1186/s12967-019-1807-5
52. Wang Z.M., Zhang S.L., Yang H., Zhuang R.Y., Guo X., Tong H.X., Zhang Y., Lu W.Q., Zhou Y.H. Efficacy and safety of anlotinib, a multikinase angiogenesis inhibitor, in combination with epirubicin in preclinical models of soft tissue sarcoma. Cancer Med. 2020. doi: 10.1002/cam4.2941
53. Lin S., Huang G., Cheng L., Li Z., Xiao Y., Deng Q., Jiang Y., Li B., Lin S., Wang S., Wu Q., Yao H., Cao S., Li Y., Liu P., Wei W., Pei D., Yao Y., Wen Z., Zhang X., Wu Y., Zhang Z., Cui S., Sun X., Qian X., Li P. Establishment of peripheral blood mononuclear cell-derived humanized lung cancer mouse models for studying efficacy of PD-L1/PD-1 targeted immunotherapy. MAbs. 2018; 10 (8): 1301–1311. doi: 10.1080/19420862.2018.1518948
54. Choi B., Lee J.S., Kim S.J., Hong D., Park J.B., Lee K.Y. Anti-tumor effects of anti-PD-1 antibody, pembrolizumab, in humanized NSG PDX mice xenografted with dedifferentiated liposarcoma. Cancer Lett. 2020; 478: 56–69. doi: 10.1016/j.canlet.2020.02.042
55. Landgraf M., Lahr C.A., Kaur I., Shafiee A., Sanchez-Herrero A., Janowicz P.W., Ravichandran A., Howard C.B., Cifuentes-Rius A., McGovern J.A., Voelcker N.H., Hutmacher D.W. Targeted camptothecin delivery via silicon nanoparticles reduces breast cancer metastasis. Biomaterials. 2020; 240: 119791. doi: 10.1016/j.biomaterials.2020.119791
56. Kähkönen T.E., Suominen M.I., Mäki-Jouppila J.H., Halleen J.M., Tanaka A., Seiler M., Bernoulli J. Human immune system increases breast cancer-induced osteoblastic bone growth in a humanized mouse model without affecting normal bone. J. Immunol. Res. 2019; 2019. doi: 10.1155/2019/4260987
Миндарь М.В., e-mail: m.v.mindar@gmail.com