Молекулярная биология, 2022, T. 56, № 5, стр. 710-731

Мышиные модели хронических вирусных инфекций и ассоциированных с ними опухолей

Д. В. Авдошина a, А. С. Кондрашова a, М. Г. Беликова abc, Е. О. Баюрова ab*

a Федеральный научный центр исследований и разработки иммунобиологических препаратов им. М.П. Чумакова Российской академии наук (Институт полиомиелита)
108819 Москва, Россия

b Национальный исследовательский центр эпидемиологии и микробиологии им. почетного академика Н.Ф. Гамалеи Минздрава России
123098 Москва, Россия

c Российский университет дружбы народов
117198 Москва, Россия

* E-mail: bayurova_eo@chumakovs.su

Поступила в редакцию 18.03.2022
После доработки 12.04.2022
Принята к публикации 13.04.2022

Аннотация

В настоящее время вирусы признаны одними из этиологических факторов развития опухолей человека. К онкогенным вирусам относятся вирус Эпштейна–Барр, папилломавирусы человека высокого канцерогенного риска, вирусы гепатита В и С, вирус Т-клеточного лейкоза человека типа I, вирус иммунодефицита человека типа 1 (опосредованно) и еще несколько предположительно онкогенных вирусов. Показано, что в патогенезе примерно 15% диагностируемых во всем мире опухолей человека участвуют вирусы. Онкогенные вирусы вызывают длительные персистирующие инфекции, при этом опухоль является случайным побочным продуктом стратегии вирусной репликации. Вирусы, как правило, не способны к индукции быстрого канцерогенеза, что подтверждает концепцию о развитии опухолей в результате совокупности множества накладывающихся друг на друга событий, в которых онкогенные вирусы человека играют разные, часто противоположные, роли. Одной из лучших экспериментальных in vivo систем для моделирования патологии человека, включая вирусные инфекции и образование опухолей, считается мышь. Однако мыши невосприимчивы к инфицированию известными онкогенными вирусами. Для преодоления этого ограничения и изучения различных аспектов вирус-ассоциированного канцерогенеза разработано множество мышиных моделей, начиная с ксенотрансплантатов тканей и клеток человека, включая вирус-инфицированные и опухолевые, и заканчивая генетически модифицированными мышами, восприимчивыми к вирусным инфекциям и вирус-ассоциированному канцерогенезу. В представленном обзоре рассмотрены основные известные на данные момент модели, проанализированы их преимущества и недостатки, описаны области их применения и намечены перспективы дальнейшего развития таких моделей.

Ключевые слова: мышиные модели, хроническая вирусная инфекция, вирусный онкогенез, вирусные онкогены, ксенотрансплантат, вирус гепатита В, вирус гепатита С, вирус иммунодефицита человека типа 1 (ВИЧ-1), вирус Эпштейна–Барр, вирус Т-клеточного лейкоза человека типа 1

Список литературы

  1. Frese K.K., Tuveson D.A. (2007) Maximizing mouse cancer models. Nat. Rev. Cancer. 7, 645–658.

  2. Morton C.L., Houghton P.J. (2007) Establishment of human tumor xenografts in immunodeficient mice. Nat. Protocols. 2, 247–250.

  3. Rubio-Viqueira B., Jimeno A., Cusatis G., Zhang X., Iacobuzio-Donahue C., Karikari C., Shi C., Danenberg K., Danenberg P.V., Kuramochi H., Tanaka K., Singh S., Salimi-Moosavi H., Bouraoud N., Amador M.L., Altiok S., Kulesza P., Yeo C., Messersmith W., Eshleman J., Hruban R.H., Maitra A., Hidalgo M. (2006) An in vivo platform for translational drug development in pancreatic cancer. Clin. Cancer Res.: An Official J. Am. Ass. Cancer Res. 12, 4652–4661.

  4. Szadvari I., Krizanova O., Babula P. (2016) Athymic nude mice as an experimental model for cancer treatment. Physiol. Res. 65, S441–S453.

  5. Bosma M.J., Carroll A.M. (1991) The SCID mouse mutant: definition, characterization, and potential uses. Annu. Rev. Immunol. 9, 323–350.

  6. Shultz L.D., Schweitzer P.A., Christianson S.W., Gott B., Schweitzer I.B., Tennent B., McKenna S., Mobraaten L., Rajan T.V., Greiner D.L. (1995) Multiple defects in innate and adaptive immunologic function in NOD/LtSz-SCID mice. J. Immunol. 154, 180–191.

  7. Ito M., Hiramatsu H., Kobayashi K., Suzue K., Kawahata M., Hioki K., Ueyama Y., Koyanagi Y., Sugamura K., Tsuji K., Heike T., Nakahata T. (2002) NOD/SCID/gamma(c)(null) mouse: an excellent recipient mouse model for engraftment of human cells. Blood. 100, 3175–3182.

  8. Christianson S.W., Greiner D.L., Hesselton R.A., Leif J.H., Wagar E.J., Schweitzer I.B., Rajan T.V., Gott B., Roopenian D.C., Shultz L.D. (1997) Enhanced human CD4+ T cell engraftment in beta2-microglobulin-deficient NOD-scid mice. J. Immunol. 158, 3578–3586.

  9. Audige A., Rochat M.A., Li D., Ivic S., Fahrny A., Muller C.K.S., Gers-Huber G., Myburgh R., Bredl S., Schlaepfer E., Scherrer A.U., Kuster S.P., Speck R.F. (2017) Long-term leukocyte reconstitution in NSG mice transplanted with human cord blood hematopoietic stem and progenitor cells. BMC Immunol. 18, 28.

  10. Ishikawa F. (2013) Modeling normal and malignant human hematopoiesis in vivo through newborn NSG xenotransplantation. Internat. I. Hematol. 98, 634–640.

  11. Murakami M., Hoshikawa Y., Satoh Y., Ito H., Tajima M., Okinaga K., Miyazawa Y., Kurata T., Sairenji T. (2000) Tumorigenesis of Epstein–Barr virus-positive epithelial cell lines derived from gastric tissues in the SCID mouse. Virology. 277, 20–26.

  12. Dubich T., Lieske A., Santag S., Beauclair G., Ruckert J., Herrmann J., Gorges J., Busche G., Kazmaier U., Hauser H., Stadler M., Schulz T.F., Wirth D. (2019) An endothelial cell line infected by Kaposi’s sarcoma-associated herpes virus (KSHV) allows the investigation of Kaposi’s sarcoma and the validation of novel viral inhibitors in vitro and in vivo. J. Mol. Med. 97, 311–324.

  13. Fujii E., Kato A., Chen Y.J., Matsubara K., Ohnishi Y., Suzuki M. (2014) Characterization of EBV-related lymphoproliferative lesions arising in donor lymphocytes of transplanted human tumor tissues in the NOG mouse. Exp. Animals. 63, 289–296.

  14. Bondarenko G., Ugolkov A., Rohan S., Kulesza P., Dubrovskyi O., Gursel D., Mathews J., O’Halloran T.V., Wei J.J., Mazar A.P. (2015) Patient-derived tumor xenografts are susceptible to formation of human lymphocytic tumors. Neoplasia. 17, 735–741.

  15. Tanaka T., Nishie R., Ueda S., Miyamoto S., Hashida S., Konishi H., Terada S., Kogata Y., Sasaki H., Tsunetoh S., Taniguchi K., Komura K., Ohmichi M. (2021) Patient-derived xenograft models in cervical cancer: a systematic review. Internat. J. Mol. Sci. 22(17), 9369.

  16. Larmour L.I., Cousins F.L., Teague J.A., Deane J.A., Jobling T.W., Gargett C.E. (2018) A patient derived xenograft model of cervical cancer and cervical dysplasia. PLoS One. 13, e0206539.

  17. Ilan E., Burakova T., Dagan S., Nussbaum O., Lubin I., Eren R., Ben-Moshe O., Arazi J., Berr S., Neville L., Yuen L., Mansour T.S., Gillard J., Eid A., Jurim O., Shouval D., Reisner Y., Galun E. (1999) The hepatitis B virus-trimera mouse: a model for human HBV infection and evaluation of anti-HBV therapeutic agents. Hepatology. 29, 553–562.

  18. Liu J., Chen S., Zou Z., Tan D., Liu X., Wang X. (2019) Pathological pattern of intrahepatic HBV in HCC is phenocopied by PDX-derived mice: a novel model for antiviral treatment. Translat. Oncol. 12, 1138–1146.

  19. Nazzal M., Sur S., Steele R., Khatun M., Patra T., Phillips N., Long J., Ray R., Ray R.B. (2020) Establishment of a patient-derived xenograft tumor from hepatitis C-associated liver cancer and evaluation of imatinib treatment efficacy. Hepatology. 72, 379–388.

  20. Cho S.Y. (2020) Patient-derived xenografts as compatible models for precision oncology. Lab. Animal Res. 36, 14.

  21. Malaney P., Nicosia S.V., Dave V. (2014) One mouse, one patient paradigm: new avatars of personalized cancer therapy. Cancer Lett. 344, 1–12.

  22. De Both N.J., Vermey M., Groen N., Dinjens W.N., Bosman F.T. (1997) Clonal growth of colorectal-carcinoma cell lines transplanted to nude mice. Internat. J. Cancer. 72, 1137–1141.

  23. Becher O.J., Holland E.C. (2006) Genetically engineered models have advantages over xenografts for preclinical studies. Cancer Res. 66, 3355–3358, discussion 3358–3359.

  24. Fiebig H.H., Berger D.P., Winterhalter B.R., Plowman J. (1990) In vitro and in vivo evaluation of US-NCI compounds in human tumor xenografts. Cancer Treat. Rev. 17, 109–117.

  25. Johnson J.I., Decker S., Zaharevitz D., Rubinstein L.V., Venditti J.M., Schepartz S., Kalyandrug S., Christian M., Arbuck S., Hollingshead M., Sausville E.A. (2001) Relationships between drug activity in NCI preclinical in vitro and in vivo models and early clinical trials. Br. J. Cancer. 84, 1424–1431.

  26. Byrne A.T., Alferez D.G., Amant F., Annibali D., Arribas J., Biankin A.V., Bruna A., Budinska E., Caldas C., Chang D.K., Clarke R.B., Clevers H., Coukos G., Dangles-Marie V., Eckhardt S.G., Gonzalez-Suarez E., Hermans E., Hidalgo M., Jarzabek M.A., de Jong S., Jonkers J., Kemper K., Lanfrancone L., Maelandsmo G.M., Marangoni E., Marine J.C., Medico E., Norum J.H., Palmer H.G., Peeper D.S., Pelicci P.G., Piris-Gimenez A., Roman-Roman S., Rueda O.M., Seoane J., Serra V., Soucek L., Vanhecke D., Villanueva A., Vinolo E., Bertotti A., Trusolino L. (2017) Interrogating open issues in cancer precision medicine with patient-derived xenografts. Nat. Rev. Cancer. 17, 254–268.

  27. Buitrago-Perez A., Hachimi M., Duenas M., Lloveras B., Santos A., Holguin A., Duarte B., Santiago J.L., Akgul B., Rodriguez-Peralto J.L., Storey A., Ribas C., Larcher F., del Rio M., Paramio J.M., Garcia-Escudero R. (2012) A humanized mouse model of HPV-associated pathology driven by E7 expression. PLoS One. 7, e41743.

  28. Hazari S., Hefler H.J., Chandra P.K., Poat B., Gunduz F., Ooms T., Wu T., Balart L.A., Dash S. (2011) Hepatocellular carcinoma xenograft supports HCV replication: a mouse model for evaluating antivirals. World J. Gastroenterol. 17, 300–312.

  29. Meuleman P., Leroux-Roels G. (2008) The human liver-uPA-SCID mouse: a model for the evaluation of antiviral compounds against HBV and HCV. Antiviral Res. 80, 231–238.

  30. Guevin C., Lamarre A., Labonte P. (2009) Novel HCV replication mouse model using human hepatocellular carcinoma xenografts. Antiviral Res. 84, 14–22.

  31. Akkina R. (2013) New generation humanized mice for virus research: comparative aspects and future prospects. Virology. 435, 14–28.

  32. Richmond A., Su Y. (2008) Mouse xenograft models vs GEM models for human cancer therapeutics. Disease Models Mech. 1, 78–82.

  33. Jin K., Teng L., Shen Y., He K., Xu Z., Li G. (2010) Patient-derived human tumour tissue xenografts in immunodeficient mice: a systematic review. Clin. Translat. Oncol.: Official Publ. Fed. Spanish Oncol. Soc. Nat. Canc. Inst. Mexico. 12, 473–480.

  34. Walsh N.C., Kenney L.L., Jangalwe S., Aryee K.E., Greiner D.L., Brehm M.A., Shultz L.D. (2017) Humanized mouse models of clinical disease. Annu. Rev. Pathol. 12, 187–215.

  35. Hatziioannou T., Evans D.T. (2012) Animal models for HIV/AIDS research. Nat. Rev. Microbiol. 10, 852–867.

  36. Brehm M.A., Shultz L.D., Greiner D.L. (2010) Humanized mouse models to study human diseases. Curr. Opin. Endocrinol. Diabetes Obesity. 17, 120–125.

  37. Wang L.X., Kang G., Kumar P., Lu W., Li Y., Zhou Y., Li Q., Wood C. (2014) Humanized-BLT mouse model of Kaposi’s sarcoma-associated herpesvirus infection. Proc. Natl. Acad. Sci. USA. 111, 3146–3151.

  38. Ma S.D., Xu X., Plowshay J., Ranheim E.A., Burlingham W.J., Jensen J.L., Asimakopoulos F., Tang W., Gulley M.L., Cesarman E., Gumperz J.E., Kenney S.C. (2015) LMP1-deficient Epstein–Barr virus mutant requires T cells for lymphomagenesis. J. Clin. Invest. 125, 304–315.

  39. Ahmed E.H., Baiocchi R.A. (2016) Murine models of Epstein–Barr virus-associated lymphomagenesis. ILAR Jl. 57, 55–62.

  40. Gauduin M.C., Parren P.W., Weir R., Barbas C.F., Burton D.R., Koup R.A. (1997) Passive immunization with a human monoclonal antibody protects hu-PBL-SCID mice against challenge by primary isolates of HIV-1. Nat. Med. 3, 1389–1393.

  41. Parren P.W., Ditzel H.J., Gulizia R.J., Binley J.M., Barbas C.F., 3rd, Burton D.R., Mosier D.E. (1995) Protection against HIV-1 infection in hu-PBL-SCID mice by passive immunization with a neutralizing human monoclonal antibody against the gp120 CD4-binding site. AIDS. 9, F1–F6.

  42. Dexter D.L., Diamond M., Creveling J., Chen S.F. (1993) Chemotherapy of mammary carcinomas arising in ras transgenic mice. Invest. New Drugs. 11, 161–168.

  43. Haddad A.F., Young J.S., Amara D., Berger M.S., Raleigh D.R., Aghi M.K., Butowski N.A. (2021) Mouse models of glioblastoma for the evaluation of novel therapeutic strategies. Neuro-Oncol. Adv. 3, vdab100.

  44. Nomura T., Tamaoki N., Takakura A., Suemizu H. (2008) Basic concept of development and practical application of animal models for human diseases. Curr. Topics Microbiol. Immunol. 324, 1–24.

  45. Coussens L.M., Hanahan D., Arbeit J.M. (1996) Genetic predisposition and parameters of malignant progression in K14-HPV16 transgenic mice. Am. J. Pathol. 149, 1899–1917.

  46. Winkler E.S., Bailey A.L., Kafai N.M., Nair S., McCune B.T., Yu J., Fox J.M., Chen R.E., Earnest J.T., Keeler S.P., Ritter J.H., Kang L.I., Dort S., Robichaud A., Head R., Holtzman M.J., Diamond M.S. (2020) SARS-CoV-2 infection of human ACE2-transgenic mice causes severe lung inflammation and impaired function. Nat. Immunol. 21, 1327–1335.

  47. Ren R.B., Costantini F., Gorgacz E.J., Lee J.J., Racaniello V.R. (1990) Transgenic mice expressing a human poliovirus receptor: a new model for poliomyelitis. Cell. 63, 353–362.

  48. Mouse Genome Sequencing C., Waterston R.H., Lindblad-Toh K., Birney E., Rogers J., Abril J.F., Agarwal P., Agarwala R., Ainscough R., Alexandersson M., An P., Antonarakis S.E., Attwood J., Baertsch R., Bailey J., Barlow K., Beck S., Berry E., Birren B., Bloom T., Bork P., Botcherby M., Bray N., Brent M.R., Brown D.G., Brown S.D., Bult C., Burton J., Butler J., Campbell R.D., Carninci P., Cawley S., Chiaromonte F., Chinwalla A.T., Church D.M., Clamp M., Clee C., Collins F.S., Cook L.L., Copley R.R., Coulson A., Couronne O., Cuff J., Curwen V., Cutts T., Daly M., David R., Davies J., Delehaunty K.D., Deri J., Dermitzakis E.T., Dewey C., Dickens N.J., Diekhans M., Dodge S., Dubchak I., Dunn D.M., Eddy S.R., Elnitski L., Emes R.D., Eswara P., Eyras E., Felsenfeld A., Fewell G.A., Flicek P., Foley K., Frankel W.N., Fulton L.A., Fulton R.S., Furey T.S., Gage D., Gibbs R.A., Glusman G., Gnerre S., Goldman N., Goodstadt L., Grafham D., Graves T.A., Green E.D., Gregory S., Guigo R., Guyer M., Hardison R.C., Haussler D., Hayashizaki Y., Hillier L.W., Hinrichs A., Hlavina W., Holzer T., Hsu F., Hua A., Hubbard T., Hunt A., Jackson I., Jaffe D.B., Johnson L.S., Jones M., Jones T.A., Joy A., Kamal M., Karlsson E.K., Karolchik D., Kasprzyk A., Kawai J., Keibler E., Kells C., Kent W.J., Kirby A., Kolbe D.L., Korf I., Kucherlapati R.S., Kulbokas E.J., Kulp D., Landers T., Leger J.P., Leonard S., Letunic I., Levine R., Li J., Li M., Lloyd C., Lucas S., Ma B., Maglott D.R., Mardis E.R., Matthews L., Mauceli E., Mayer J.H., McCarthy M., McCombie W.R., McLaren S., McLay K., McPherson J.D., Meldrim J., Meredith B., Mesirov J.P., Miller W., Miner T.L., Mongin E., Montgomery K.T., Morgan M., Mott R., Mullikin J.C., Muzny D.M., Nash W.E., Nelson J.O., Nhan M.N., Nicol R., Ning Z., Nusbaum C., O’Connor M.J., Okazaki Y., Oliver K., Overton-Larty E., Pachter L., Parra G., Pepin K.H., Peterson J., Pevzner P., Plumb R., Pohl C.S., Poliakov A., Ponce T.C., Ponting C.P., Potter S., Quail M., Reymond A., Roe B.A., Roskin K.M., Rubin E.M., Rust A.G., Santos R., Sapojnikov V., Schultz B., Schultz J., Schwartz M.S., Schwartz S., Scott C., Seaman S., Searle S., Sharpe T., Sheridan A., Shownkeen R., Sims S., Singer J.B., Slater G., Smit A., Smith D.R., Spencer B., Stabenau A., Stange-Thomann N., Sugnet C., Suyama M., Tesler G., Thompson J., Torrents D., Trevaskis E., Tromp J., Ucla C., Ureta-Vidal A., Vinson J.P., Von Niederhausern A.C., Wade C.M., Wall M., Weber R.J., Weiss R.B., Wendl M.C., West A.P., Wetterstrand K., Wheeler R., Whelan S., Wierzbowski J., Willey D., Williams S., Wilson R.K., Winter E., Worley K.C., Wyman D., Yang S., Yang S.P., Zdobnov E.M., Zody M.C., Lander E.S. (2002) Initial sequencing and comparative analysis of the mouse genome. Nature. 420, 520–562.

  49. Dorner M., Horwitz J.A., Robbins J.B., Barry W.T., Feng Q., Mu K., Jones C.T., Schoggins J.W., Catanese M.T., Burton D.R., Law M., Rice C.M., Ploss A. (2011) A genetically humanized mouse model for hepatitis C virus infection. Nature. 474, 208–211.

  50. Burm R., Collignon L., Mesalam A.A., Meuleman P. (2018) Animal models to study hepatitis C virus infection. Front. Immunol. 9, 1032.

  51. Li H., Zhuang Q., Wang Y., Zhang T., Zhao J., Zhang Y., Zhang J., Lin Y., Yuan Q., Xia N., Han J. (2014) HBV life cycle is restricted in mouse hepatocytes expressing human NTCP. Cell Mol. Immunol. 11, 175–183.

  52. Boberg A., Brave A., Johansson S., Wahren B., Hin-kula J., Rollman E. (2008) Murine models for HIV vaccination and challenge. Expert Rev. Vaccines. 7, 117–130.

  53. Mestas J., Hughes C.C. (2004) Of mice and not men: differences between mouse and human immunology. J. Immunol. 172, 2731–2738.

  54. Masemann D., Ludwig S., Boergeling Y. (2020) Advances in transgenic mouse models to study infections by human pathogenic viruses. Internat. J. Mol. Sci. 21(23), 9289.

  55. Inuzuka T., Takahashi K., Chiba T., Marusawa H. (2014) Mouse models of hepatitis B virus infection comprising host–virus immunologic interactions. Pathogens. 3, 377–389.

  56. Li Y.T., Wu H.L., Liu C.J. (2021) Molecular mechanisms and animal models of HBV-related hepatocellular carcinoma: with emphasis on metastatic tumor antigen 1. Internat. J. Mol. Sci. 22(17), 9380.

  57. Moriya K., Nakagawa K., Santa T., Shintani Y., Fujie H., Miyoshi H., Tsutsumi T., Miyazawa T., Ishibashi K., Horie T., Imai K., Todoroki T., Kimura S., Koike K. (2001) Oxidative stress in the absence of inflammation in a mouse model for hepatitis C virus-associated hepatocarcinogenesis. Cancer Res. 61, 4365–4370.

  58. Liu Y., Maya S., Ploss A. (2021) Animal models of hepatitis B virus infection-success, challenges, and future directions. Viruses. 13(5), 777

  59. Leonard J.M., Abramczuk J.W., Pezen D.S., Rutledge R., Belcher J.H., Hakim F., Shearer G., Lamperth L., Travis W., Fredrickson T., Notkinsand A.L., Martin M.A. (1988) Development of disease and virus recovery in transgenic mice containing HIV proviral DNA. Science. 242, 1665–1670.

  60. Goudreau G., Carpenter S., Beaulieu N., Jolicoeur P. (1996) Vacuolar myelopathy in transgenic mice expressing human immunodeficiency virus type 1 proteins under the regulation of the myelin basic protein gene promoter. Nat. Med. 2, 655–661.

  61. Vogel J., Hinrichs S.H., Reynolds R.K., Luciw P.A., Jay G. (1988) The HIV tat gene induces dermal lesions resembling Kaposi’s sarcoma in transgenic mice. Nature. 335, 606–611.

  62. Brady H.J., Abraham D.J., Pennington D.J., Miles C.G., Jenkins S., Dzierzak E.A. (1995) Altered cytokine expression in T lymphocytes from human immunodeficiency virus Tat transgenic mice. J. Virol. 69, 7622–7629.

  63. Bravo Cruz A.G., Damania B. (2019) In vivo models of oncoproteins encoded by Kaposi’s sarcoma-associated herpesvirus. J. Virol. 93(11), e01053-18.

  64. Yu M., Chandra J. (2021) Therapeutic DNA vaccine against HPV16-associated cancer. Meth. Mol. Biol. 2197, 241–252.

  65. Pascolo S. (2005) HLA class I transgenic mice: development, utilisation and improvement. Expert Opin. Biol. Therapy. 5, 919–938.

  66. Pascolo S., Bervas N., Ure J.M., Smith A.G., Lemonnier F.A., Perarnau B. (1997) HLA-A2.1-restricted education and cytolytic activity of CD8(+) T lymphocytes from beta2 microglobulin (beta2m) HLA-A2.1 monochain transgenic H-2Db beta2m double knockout mice. J. Exp. Med. 185, 2043–2051.

  67. Boucherma R., Kridane-Miledi H., Bouziat R., Rasmussen M., Gatard T., Langa-Vives F., Lemercier B., Lim A., Berard M., Benmohamed L., Buus S., Rooke R., Lemonnier F.A. (2013) HLA-A*01:03, HLA-A*24:02, HLA-B*08:01, HLA-B*27:05, HLA-B*35:01, HLA-B*44:02, and HLA-C*07:01 monochain transgenic/H-2 class I null mice: novel versatile preclinical models of human T cell responses. J. Iimmunol. 191, 583–593.

  68. Zottnick S., Voss A.L., Riemer A.B. (2020) Inducing immunity where it matters: orthotopic HPV tumor models and therapeutic vaccinations. Front. Immunol. 11, 1750.

  69. Eiben G.L., Velders M.P., Schreiber H., Cassetti M.C., Pullen J.K., Smith L.R., Kast W.M. (2002) Establishment of an HLA-A*0201 human papillomavirus type 16 tumor model to determine the efficacy of vaccination strategies in HLA-A*0201 transgenic mice. Cancer Res. 62, 5792–5799.

  70. Sun S., Li J. (2017) Humanized chimeric mouse models of hepatitis B virus infection. Internat. J. Infect. Dis.: IJID: Official Publ. Internat. Soc. Infect. Dis. 59, 131–136.

  71. Tateno C., Yoshizane Y., Saito N., Kataoka M., Utoh R., Yamasaki C., Tachibana A., Soeno Y., Asahina K., Hino H., Asahara T., Yokoi T., Furukawa T., Yoshizato K. (2004) Near completely humanized liver in mice shows human-type metabolic responses to drugs. Am. J. Pathol. 165, 901–912.

  72. Dandri M., Burda M.R., Torok E., Pollok J.M., Iwanska A., Sommer G., Rogiers X., Rogler C.E., Gupta S., Will H., Greten H., Petersen J. (2001) Repopulation of mouse liver with human hepatocytes and in vivo infection with hepatitis B virus. Hepatology. 33, 981–988.

  73. Tsuge M., Hiraga N., Takaishi H., Noguchi C., Oga H., Imamura M., Takahashi S., Iwao E., Fujimoto Y., Ochi H., Chayama K., Tateno C., Yoshizato K. (2005) Infection of human hepatocyte chimeric mouse with genetically engineered hepatitis B virus. Hepatology. 42, 1046–1054.

  74. Yuan L., Jiang J., Liu X., Zhang Y., Zhang L., Xin J., Wu K., Li X., Cao J., Guo X., Shi D., Li J., Jiang L., Sun S., Wang T., Hou W., Zhang T., Zhu H., Zhang J., Yuan Q., Cheng T., Li J., Xia N. (2019) HBV infection-induced liver cirrhosis development in dual-humanised mice with human bone mesenchymal stem cell transplantation. Gut. 68, 2044–2056.

  75. Hu J., Lin Y.Y., Chen P.J., Watashi K., Wakita T. (2019) Cell and animal models for studying hepatitis B virus infection and drug development. Gastroenterology. 156, 338–354.

  76. Ilan E., Arazi J., Nussbaum O., Zauberman A., Eren R., Lubin I., Neville L., Ben-Moshe O., Kischitzky A., Litchi A., Margalit I., Gopher J., Mounir S., Cai W., Daudi N., Eid A., Jurim O., Czerniak A., Galun E., Dagan S. (2002) The hepatitis C virus (HCV)-Trimera mouse: a model for evaluation of agents against HCV. J. Infect. Dis. 185, 153–161.

  77. Mercer D.F., Schiller D.E., Elliott J.F., Douglas D.N., Hao C., Rinfret A., Addison W.R., Fischer K.P., Churchill T.A., Lakey J.R., Tyrrell D.L., Kneteman N.M. (2001) Hepatitis C virus replication in mice with chimeric human livers. Nat. Medicine. 7, 927–933.

  78. Kneteman N.M., Weiner A.J., O’Connell J., Collett M., Gao T., Aukerman L., Kovelsky R., Ni Z.J., Zhu Q., Hashash A., Kline J., Hsi B., Schiller D., Douglas D., Tyrrell D.L., Mercer D.F. (2006) Anti-HCV therapies in chimeric scid-Alb/uPA mice parallel outcomes in human clinical application. Hepatology. 43, 1346–1353.

  79. Turrini P., Sasso R., Germoni S., Marcucci I., Celluci A., Di Marco A., Marra E., Paonessa G., Eutropi A., Laufer R., Migliaccio G., Padron J. (2006) Development of humanized mice for the study of hepatitis C virus infection. Transplant. Proc. 38, 1181–1184.

  80. Nolan K., Verzosa G., Cleaver T., Tippimanchai D., DePledge L.N., Wang X.J., Young C., Le A., Doebele R., Li H., Malkoski S.P. (2020) Development of syngeneic murine cell lines for use in immunocompetent orthotopic lung cancer models. Cancer Cell Internat. 20, 417.

  81. Talmadge J.E., Singh R.K., Fidler I.J., Raz A. (2007) Murine models to evaluate novel and conventional therapeutic strategies for cancer. Am. J. Pathol. 170, 793–804.

  82. Takaki H., Oshiumi H., Shingai M., Matsumoto M., Seya T. (2017) Development of mouse models for analysis of human virus infections. Microbiol. Immunol. 61, 107–113.

  83. Zitvogel L., Pitt J.M., Daillere R., Smyth M.J., Kroemer G. (2016) Mouse models in oncoimmunology. Nat. Rev. Cancer. 16, 759–773.

  84. Gunther J.H., Jurczok A., Wulf T., Brandau S., Deinert I., Jocham D., Bohle A. (1999) Optimizing syngeneic orthotopic murine bladder cancer (MB49). Cancer Res. 59, 2834–2837.

  85. Mittal V.K., Bhullar J.S., Jayant K. (2015) Animal models of human colorectal cancer: current status, uses and limitations. W. J. Gastroenterol. 21, 11854–11861.

  86. Tsukiyama-Kohara K. (2012) Role of oxidative stress in hepatocarcinogenesis induced by hepatitis C virus. Internat. J. Mol. Sci. 13, 15271–15278.

  87. Bayurova E., Jansons J., Skrastina D., Smirnova O., Mezale D., Kostyusheva A., Kostyushev D., Petkov S., Podschwadt P., Valuev-Elliston V. (2019) HIV-1 reverse transcriptase promotes tumor growth and metastasis formation via ROS-dependent upregulation of twist. Oxidative Med. Cell. Longevity. 2019, 6016278. https://doi.org/10.1155/2019/601627

  88. Lawson J.S., Salmons B., Glenn W.K. (2018) Oncogenic viruses and breast cancer: mouse mammary tumor virus (MMTV), bovine leukemia virus (BLV), human papilloma virus (HPV), and Epstein–Barr virus (EBV). Fron. Oncol. 8, 1.

  89. Wei T., Buehler D., Ward-Shaw E., Lambert P.F. (2020) An infection-based murine model for papillomavirus-associated head and neck cancer. mBio. 11(3), e00908-20.

  90. Spurgeon M.E., Lambert P.F. (2019) Sexual transmission of murine papillomavirus (MmuPV1) in Mus musculus. eLife. 8, e50056.

  91. Yu L., Majerciak V., Xue X.Y., Uberoi A., Lobanov A., Chen X., Cam M., Hughes S.H., Lambert P.F., Zheng Z.M. (2021) Mouse papillomavirus type 1 (MmuPV1) DNA is frequently integrated in benign tumors by microhomology-mediated end-joining. PLoS Pathog. 17, e1009812.

  92. Liang X., Paden C.R., Morales F.M., Powers R.P., Jacob J., Speck S.H. (2011) Murine gamma-herpesvirus immortalization of fetal liver-derived B cells requires both the viral cyclin D homolog and latency-associated nuclear antigen. PLoS Pathog. 7, e1002220.

  93. Butel J.S. (2000) Viral carcinogenesis: revelation of molecular mechanisms and etiology of human disease. Carcinogenesis. 21, 405–426.

  94. Замараев А.В., Животовский Б., Копеина Г.С. (2020) Вирусные инфекции: негативный регулятор апоптоза и фактор онкогенности. Биохимия. 85(10), 1398–1410.

  95. Sun W., Yang J. (2010) Functional mechanisms for human tumor suppressors. J. Cancer. 1, 136–140.

  96. Attardi L.D., Jacks T. (1999) The role of p53 in tumour suppression: lessons from mouse models. Cell. Mol. Life Sci: CMLS. 55, 48–63.

  97. Clarke A.R., Hollstein M. (2003) Mouse models with modified p53 sequences to study cancer and ageing. Cell Death Differ. 10, 443–450.

  98. Levine A.J., Oren M. (2009) The first 30 years of p53: growing ever more complex. Nat. Rev. Cancer. 9, 749–758.

  99. Ahuja D., Saenz-Robles M.T., Pipas J.M. (2005) SV40 large T antigen targets multiple cellular pathways to elicit cellular transformation. Oncogene. 24, 7729–7745.

  100. Hudson A.L., Colvin E.K. (2016) Transgenic mouse models of SV40-induced cancer. ILAR J. 57, 44–54.

  101. Engeland K. (2018) Cell cycle arrest through indirect transcriptional repression by p53: I have a DREAM. Cell Death Differ. 25, 114–132.

  102. Lipinski M.M., Jacks T. (1999) The retinoblastoma gene family in differentiation and development. Oncogene. 18, 7873–7882.

  103. Gupta S., Kumar P., Das B.C. (2018) HPV: molecular pathways and targets. Curr. Problems Cancer. 42, 161–174.

  104. Matlashewski G., Schneider J., Banks L., Jones N., Murray A., Crawford L. (1987) Human papillomavirus type 16 DNA cooperates with activated ras in transforming primary cells. EMBO J. 6, 1741–1746.

  105. Pylayeva-Gupta Y., Grabocka E., Bar-Sagi D. (2011) RAS oncogenes: weaving a tumorigenic web. Nat. Rev. Cancer. 11, 761–774.

  106. Kivinen L., Tsubari M., Haapajarvi T., Datto M.B., Wang X.F., Laiho M. (1999) Ras induces p21Cip1/Waf1 cyclin kinase inhibitor transcriptionally through Sp1-binding sites. Oncogene. 18, 6252–6261.

  107. Feltkamp M.C., Smits H.L., Vierboom M.P., Minnaar R.P., de Jongh B.M., Drijfhout J.W., ter Schegget J., Melief C.J., Kast W.M. (1993) Vaccination with cytotoxic T lymphocyte epitope-containing peptide protects against a tumor induced by human papillomavirus type 16-transformed cells. Eur. J. Immunol. 23, 2242–2249.

  108. Mermod M., Hiou-Feige A., Bovay E., Roh V., Sponarova J., Bongiovanni M., Vermeer D.W., Lee J.H., Petrova T.V., Rivals J.P., Monnier Y., Tolstonog G.V., Simon C. (2018) Mouse model of postsurgical primary tumor recurrence and regional lymph node metastasis progression in HPV-related head and neck cancer. Intern. J. Cancer. 142, 2518–2528.

  109. Paolini F., Massa S., Manni I., Franconi R., Venuti A. (2013) Immunotherapy in new pre-clinical models of HPV-associated oral cancers. Hum. Vaccin. Immunother. 9, 534–543.

  110. Henkle T.R., Lam B., Kung Y.J., Lin J., Tseng S.H., Ferrall L., Xing D., Hung C.F., Wu T.C. (2021) Development of a novel mouse model of spontaneous high-risk HPVE6/E7-expressing carcinoma in the cervicovaginal tract. Cancer Res. 81, 4560–4569.

  111. Haverkos H.W. (2004) Viruses, chemicals and co-carcinogenesis. Oncogene. 23, 6492–6499.

  112. Isaguliants M., Bayurova E., Avdoshina D., Kondrashova A., Chiodi F., Palefsky J.M. (2021) Oncogenic effects of HIV-1 proteins, mechanisms behind. Cancers. 13(2), 305.

  113. Kornek M., Raskopf E., Guetgemann I., Ocker M., Gerceker S., Gonzalez-Carmona M.A., Rabe C., Sauerbruch T., Schmitz V. (2006) Combination of systemic thioacetamide (TAA) injections and ethanol feeding accelerates hepatic fibrosis in C3H/He mice and is associated with intrahepatic up regulation of MMP-2, VEGF and ICAM-1. J. Hepatol. 45, 370–376.

  114. Longnecker D.S., Kuhlmann E.T., Freeman D.H., Jr. (1990) Characterization of the elastase 1-simian virus 40 T-antigen mouse model of pancreatic carcinoma: effects of sex and diet. Cancer Res. 50, 7552–7554.

  115. Lau T.C., Fiebig-Comyn A.A., Shaler C.R., McPhee J.B., Coombes B.K., Schertzer J.D. (2021) Low dietary fiber promotes enteric expansion of a Crohn’s disease-associated pathobiont independent of obesity. Am. J. Physiol. Endocrinol. Metabolism. 321, E338–E350.

  116. Morrison K.E., Jasarevic E., Howard C.D., Bale T.L. (2020) It’s the fiber, not the fat: significant effects of dietary challenge on the gut microbiome. Microbiome. 8, 15.

  117. Wang L., Yi T., Zhang W., Pardoll D.M., Yu H. (2010) IL-17 enhances tumor development in carcinogen-induced skin cancer. Cancer Res. 70, 10112–10120.

  118. He D., Li H., Yusuf N., Elmets C.A., Athar M., Katiyar S.K., Xu H. (2012) IL-17 mediated inflammation promotes tumor growth and progression in the skin. PLoS One. 7, e32126.

  119. Isaguliants M., Krotova O., Petkov S., Jansons J., Bayurova E., Mezale D., Fridrihsone I., Kilpelainen A., Podschwadt P., Agapkina Y., Smirnova O., Kostic L., Saleem M., Latyshev O., Eliseeva O., Malkova A., Gorodnicheva T., Wahren B., Gordeychuk I., Starodubova E., Latanova A. (2021) Cellular immune response induced by DNA immunization of mice with drug resistant integrases of HIV-1 clade A offers partial protection against growth and metastatic activity of integrase-expressing adenocarcinoma cells. Microorganisms. 9(6), 1219. https://doi.org/10.3390/microorganisms9061219

Дополнительные материалы отсутствуют.