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Журнал микробиологии, эпидемиологии и иммунобиологии. 2020; 97: 159-164

Модели in vitro для изучения вируса Зика

Пименова Екатерина Владимировна, Храпова Наталья Петровна, Замарина Татьяна Валерьевна

https://doi.org/10.36233/0372-9311-2020-97-2-159-164

Аннотация

В связи с глобализацией, увеличением торговых и миграционных потоков вероятность возникновения вспышек лихорадки Зика существенно возрастает во всем мире, включая Черноморское побережье Кавказа в России. Лихорадка Зика имеет тенденцию к быстрому распространению и расширению географических границ, поэтому изучение данного вируса остается актуальной задачей. Накопленные за последнее время знания способствовали всестороннему изучению вируса Зика, однако до сих пор многие вопросы этиологии, эпидемиологии, клиники, специфической диагностики и профилактики остаются нерешенными. Настоящий обзор основан главным образом на публикациях зарубежных авторов и ведущих международных организаций по изучению вируса Зика в культуре клеточных линий. В обзоре обобщены экспериментальные данные последних лет по применению клеточных линий, используемых в качестве клеток-мишеней для изучения вируса Зика, отмечены их преимущества и недостатки, приведено сравнение чувствительности клеточных линий разного происхождения.
Список литературы

1. Fagbami A.H. Zika virus infections in Nigeria: virological and seroepidemiological investigations in Oyo State. J. Hyg. (Lond). 1979; 83(2): 213-9. DOI: http://doi.org/10.1017/s0022172400025997

2. Filipe A.R., Martins C.M.V., Rocha H. Laboratory infection with Zika virus after vaccination against yellow fever. Arch. Gesamte Virusforsch. 1973; 43(4): 315-9. DOI: http://doi.org/10.1007/bf01556147

3. Moore D.L., Causey O.R., Carey D.E., Reddy S., Cooke A.R., Akinkugbe F.M., et al. Arthropod-borne viral infections of man in Nigeria, 1964–1970. Ann. Trop. Med. Parasitol. 1975; 69(1): 49-64. DOI: http://doi.org/10.1080/00034983.1975.11686983

4. Olson J.G., Ksiazek T.G., Suhandiman, Triwibowo. Zika virus, a cause of fever in central Java, Indonesia. Trans. R. Soc. Trop. Med. Hyg. 1981; 75(3): 389-93. DOI: http://doi.org/10.1016/0035-9203(81)90100-0

5. Simpson D.I. Zika virus infection in man. Trans. R. Soc. Trop. Med. Hyg. 1964; 58: 335-8.

6. Duffy M.R., Chen T.H., Hancock W.T., Powers A.M., Kool J.L., Lanciotti R.S., et al. Zika virus outbreak on Yap Island, Federated States of Micronesia. N. Engl. J. Med. 2009; 360(24): 2536-43. DOI: http://doi.org/10.1056/NEJMoa0805715

7. Faye O., Freire C.C., Iamarino A., Faye O., de Oliveira J.V., Diallo M., et al. Molecular evolution of Zika virus during its emergence in the 20th century. PLoS. Negl. Trop. Dis. 2014; 8(1): e2636. DOI: http://doi.org/10.1371/journal.pntd.0002636

8. Carteaux G., Maquart M., Bedet A., Contou D., Brugières P., Fourati S., et al. Zika virus associated with meningoencephalitis. N. Engl. J. Med. 2016; 374(16): 1595-6. DOI: http://doi.org/10.1056/NEJMc1602964

9. Craig A.T., Butler M.T., Pastore R., Paterson B.J., Durrheim D.N. Acute flaccid paralysis incidence and Zika virus surveillance, Pacific Islands. Bull. World Health Organ. 2017; 95(1): 69-75. DOI: http://doi.org/10.2471/BLT.16.171892

10. Parra B., Lizarazo J., Jiménez-Arango J.A., Zea-Vera A.F., González-Manrique G., Vargas J., et al. Guillain-Barré syndrome associated with Zika virus infection in Colombia. N. Engl. J. Med. 2016; 375(16): 1513-23. DOI: http://doi.org/10.1056/NEJMoa1605564

11. Chibueze E.C., Tirado V., Lopes K.D., Balogun O.O., Takemoto Y., Swa T., et al. Zika virus infection in pregnancy: a systematic review of disease course and complications. Reprod. Health. 2017; 14(1): 28. DOI: http://doi.org/10.1186/s12978-017-0285-6

12. Mlakar J., Korva M., Tul N., Popović M., Poljšak-Prijatelj M., Mraz J., et al. Zika virus associated with microcephaly. N. Engl. J. Med. 2016; 374(10): 951-8. DOI: http://doi.org/10.1056/NEJMoa1600651

13. Rasmussen S.A., Jamieson D.J., Honein M.A., Petersen L.R. Zika virus and birth defects — reviewing the evidence for causality. N. Engl. J. Med. 2016; 374(20): 1981-7. DOI: http://doi.org/10.1056/NEJMsr1604338

14. Brasil P., Pereira J.P., Moreira M.E., Ribeiro Nogueira R.M., Damasceno L., Wakimoto M., et al. Zika virus infection in pregnant women in Rio de Janeiro. N. Engl. J. Med. 2016; 375(24): 2321-34. DOI: http://doi.org/10.1056/NEJMoa1602412

15. Himmelsbach K., Hildt E. Identification of various cell culture models for the study of Zika virus. World J. Virol. 2018; 7(1): 10-20. DOI: http://doi.org/10.5501/wjv.v7.i1.10

16. Chan J.F., Yip C.C., Tsang J.O., Tee K.M., Cai J.P., Chik K.K., et al. Differential cell line susceptibility to the emerging Zika virus: implications for disease pathogenesis, non‐vector‐borne human transmission and animal reservoirs. Emerg. Microbes Infect. 2016; 5: e93. DOI: http://doi.org/10.1038/emi.2016.99

17. Ramos da Silva S., Cheng F., Huang I.C., Jung J.U., Gao S.J. Efficiencies and kinetics of infection in different cell types/lines by African and Asian strains of Zika virus. J. Med. Virol. 2019; 91(2): 179-89. DOI: http://doi.org/10.1002/jmv.25306

18. Barr K.L., Anderson B.D., Prakoso D., Long M.T. Working with Zika and Usutu viruses in vitro. PLoS neglected tropical diseases. PLoS. Negl. Trop. Dis. 2016; 10(8): e0004931. DOI: http://doi.org/10.1371/journal.pntd.0004931

19. Vicenti I., Boccuto A., Giannini A., Dragoni F., Saladini F., Zazzi M. Comparative analysis of different cell systems for Zika virus (ZIKV) propagation and evaluation of anti-ZIKV compounds in vitro. Virus Res. 2018; 244: 64-70. DOI: http://doi.org/0.1016/j.virusres.2017.11.003

20. Willard K.A., Demakovsky L., Tesla B., Goodfellow F.T., Stice S.L., Murdock C.C., et al. Zika virus exhibits lineage-specific phenotypes in cell culture, in aedes aegypti mosquitoes, and in an embryo model. Viruses. 2017; 9(12): 383. DOI: http://doi.org/10.3390/v9120383

21. Kumar A., Jovel J., Lopez-Orozco J., Limonta D., Airo A.M., Hou S., et al. Human Sertoli cells support high levels of Zika virus replication and persistence. Sci. Rep. 2018; 8(1): 5477. DOI: http://doi.org/10.1038/s41598-018-23899-x

22. Kumar A., Hou S., Airo A.M., Limonta D., Mancinelli V., Branton W., et al. Zika virus inhibits type-I interferon production and downstream signaling. EMBO Rep. 2016; 17(12): 1766-75. DOI: http://doi.org/10.15252/embr.201642627

23. Ma W., Li S., Ma S., Jia L., Zhang F., Zhang Y., et al. Zika virus causes testis damage and leads to male infertility in mice. Cell. 2017; 168(3): 542. DOI: http://doi.org/10.1016/j.cell.2017.01.009

24. Duggal N.K., Ritter J.M., Pestorius S.E., Zaki S.R., Davis B.S., Chang G.J., et al. Frequent Zika virus sexual transmission and prolonged viral RNA shedding in an immunodeficient mouse model. Cell Rep. 2017; 18(7): 1751-60. DOI: http://doi.org/10.1016/j.celrep.2017.01.056

25. Hirsch A.J., Smith J.L., Haese N.N., Broeckel R.M., Parkins C.J., Kreklywich C., et al. Zika Virus infection of rhesus macaques leads to viral persistence in multiple tissues. PLoS Pathog. 2017; 13(4): e1006317. DOI: http://doi.org/10.1371/journal.ppat.1006317

26. Siemann D.N., Strange D.P., Maharaj P.N., Shi P.Y., Verma S. Zika virus infects human Sertoli cells and modulates the integrity of the in vitro blood-testis barrier model. J. Virol. 2017;91(22). pii: e00623-17. DOI: http://doi.org/10.1128/JVI.00623-17

27. Uraki R., Hwang J., Jurado K.A., Householder S., Yockey L.J., Hastings A.K., et al. Zika virus causes testicular atrophy. Sci. Adv. 2017; 3(2): e1602899. DOI: http://doi.org/10.1126/sciadv.1602899

28. Spencer J.L., Lahon A., Tran L.L., Arya R.P., Kneubehl A.R., Vogt M.B., et al. Replication of Zika virus in human prostate cells: a potential source of sexually transmitted virus. J. Infect. Dis. 2018; 217(4): 538-47. DOI: http://doi.org/10.1093/infdis/jix436

29. Kim W., Barron D.A., San Martin R., Chan K.S., Tran L.L., Yang F., et al. RUNX1 is essential for mesenchymal stem cell proliferation and myofibroblast differentiation. Proc. Natl. Acad. Sci. U.S.A. 2014; 111(46): 16389-94. DOI: http://doi.org/10.1073/pnas.1407097111

30. Lahon A., Arya R.P., Kneubehl A.R., Vogt M.B., Dailey Garnes N.J., Rico-Hesse R., et al. Characterization of a Zika virus isolate from Colombia. PLoS Negl. Trop. Dis. 2016; 10(9): e0005019. DOI: http://doi.org/10.1371/journal.pntd.0005019

31. Murray K.O., Gorchakov R., Carlson A.R., Berry R., Lai L., Natrajan M., et al. Prolonged detection of Zika virus in vaginal secretions and whole blood. Emerg. Infect. Dis. 2017; 23(1): 99-101. DOI: http://doi.org/10.3201/eid2301.161394

32. Arsuaga M., Bujalance S.G., Díaz-Menéndez M., Vázquez A., Arribas J.R. Probable sexual transmission of Zika virus from a vasectomised man. Lancet Infect. Dis. 2016; 16(10): 1107. DOI: http://doi.org/10.1016/S1473-3099(16)30320-6

33. Froeschl G., Huber K., von Sonnenburg F., Nothdurft H.D., Bretzel G., Hoelscher M., et al. Long-term kinetics of Zika virus RNA and antibodies in body fluids of a vasectomized traveller returning from Martinique: a case report. BMC Infect Dis. 2017; 17(1): 55. DOI: http://doi.org/10.1186/s12879-016-2123-9

34. Atkinson B., Thorburn F., Petridou C., Bailey D., Hewson R., Simpson A.J., et al. Presence and persistence of Zika virus RNA in semen, United Kingdom, 2016. Emerg. Infect. Dis. 2017; 23(4): 611-5. DOI: http://doi.org/10.3201/eid2304.161692

35. Kaid C., Goulart E., Caires-Júnior L.C., Araujo B.H.S., SoaresSchanoski A., Bueno H.M.S., et al. zika virus selectively kills aggressive human embryonal CNS tumor cells in vitro and in vivo. Cancer Res. 2018; 78(12): 3363-74. DOI: http://doi.org/10.1158/0008-5472.CAN-17-3201

36. El Costa H., Gouilly J., Mansuy J.M., Chen Q., Levy C., Cartron G., et al. ZIKA virus reveals broad tissue and cell tropism during the first trimester of pregnancy. Sci. Rep. 2016; 6: 35296. DOI: http://doi.org/10.1038/srep35296

Journal of microbiology, epidemiology and immunobiology. 2020; 97: 159-164

In vitro models for the study of Zika virus

Pimenova Ekaterina V., Khrapova Natalya P., Zamarina Tatyana V.

https://doi.org/10.36233/0372-9311-2020-97-2-159-164

Abstract

Due to the globalization, increased trade and migration flows the probability of outbreaks of Zika fever is significantly increasing worldwide, including Black sea coast of the Caucasus in the Russian Federation. Zika fever tends to spread rapidly and to expand its geography, so the study of this virus remains an urgent task. The accumulated knowledge recently has contributed to a comprehensive study of Zika virus, but so far many questions of etiology, epidemiology, clinic, specific diagnosis and prevention remain unresolved. This review is based mainly on publications by foreign authors and leading international organizations dedicated to the study of Zika virus in the cell lines of various sources . The review summarizes recent experimental data on the use of cell lines as target cells for the study of Zika virus, their advantages and disadvantages, and the susceptibility of different cell lines to this virus. Information from bibliographic and abstract scientific databases, search websites, and publishers: RSCI, Web of Science, Scopus, MEDLINE, Google Scholar, PubMed, Springer Nature, Elsevier, and others was used in the preparation of the review.
References

1. Fagbami A.H. Zika virus infections in Nigeria: virological and seroepidemiological investigations in Oyo State. J. Hyg. (Lond). 1979; 83(2): 213-9. DOI: http://doi.org/10.1017/s0022172400025997

2. Filipe A.R., Martins C.M.V., Rocha H. Laboratory infection with Zika virus after vaccination against yellow fever. Arch. Gesamte Virusforsch. 1973; 43(4): 315-9. DOI: http://doi.org/10.1007/bf01556147

3. Moore D.L., Causey O.R., Carey D.E., Reddy S., Cooke A.R., Akinkugbe F.M., et al. Arthropod-borne viral infections of man in Nigeria, 1964–1970. Ann. Trop. Med. Parasitol. 1975; 69(1): 49-64. DOI: http://doi.org/10.1080/00034983.1975.11686983

4. Olson J.G., Ksiazek T.G., Suhandiman, Triwibowo. Zika virus, a cause of fever in central Java, Indonesia. Trans. R. Soc. Trop. Med. Hyg. 1981; 75(3): 389-93. DOI: http://doi.org/10.1016/0035-9203(81)90100-0

5. Simpson D.I. Zika virus infection in man. Trans. R. Soc. Trop. Med. Hyg. 1964; 58: 335-8.

6. Duffy M.R., Chen T.H., Hancock W.T., Powers A.M., Kool J.L., Lanciotti R.S., et al. Zika virus outbreak on Yap Island, Federated States of Micronesia. N. Engl. J. Med. 2009; 360(24): 2536-43. DOI: http://doi.org/10.1056/NEJMoa0805715

7. Faye O., Freire C.C., Iamarino A., Faye O., de Oliveira J.V., Diallo M., et al. Molecular evolution of Zika virus during its emergence in the 20th century. PLoS. Negl. Trop. Dis. 2014; 8(1): e2636. DOI: http://doi.org/10.1371/journal.pntd.0002636

8. Carteaux G., Maquart M., Bedet A., Contou D., Brugières P., Fourati S., et al. Zika virus associated with meningoencephalitis. N. Engl. J. Med. 2016; 374(16): 1595-6. DOI: http://doi.org/10.1056/NEJMc1602964

9. Craig A.T., Butler M.T., Pastore R., Paterson B.J., Durrheim D.N. Acute flaccid paralysis incidence and Zika virus surveillance, Pacific Islands. Bull. World Health Organ. 2017; 95(1): 69-75. DOI: http://doi.org/10.2471/BLT.16.171892

10. Parra B., Lizarazo J., Jiménez-Arango J.A., Zea-Vera A.F., González-Manrique G., Vargas J., et al. Guillain-Barré syndrome associated with Zika virus infection in Colombia. N. Engl. J. Med. 2016; 375(16): 1513-23. DOI: http://doi.org/10.1056/NEJMoa1605564

11. Chibueze E.C., Tirado V., Lopes K.D., Balogun O.O., Takemoto Y., Swa T., et al. Zika virus infection in pregnancy: a systematic review of disease course and complications. Reprod. Health. 2017; 14(1): 28. DOI: http://doi.org/10.1186/s12978-017-0285-6

12. Mlakar J., Korva M., Tul N., Popović M., Poljšak-Prijatelj M., Mraz J., et al. Zika virus associated with microcephaly. N. Engl. J. Med. 2016; 374(10): 951-8. DOI: http://doi.org/10.1056/NEJMoa1600651

13. Rasmussen S.A., Jamieson D.J., Honein M.A., Petersen L.R. Zika virus and birth defects — reviewing the evidence for causality. N. Engl. J. Med. 2016; 374(20): 1981-7. DOI: http://doi.org/10.1056/NEJMsr1604338

14. Brasil P., Pereira J.P., Moreira M.E., Ribeiro Nogueira R.M., Damasceno L., Wakimoto M., et al. Zika virus infection in pregnant women in Rio de Janeiro. N. Engl. J. Med. 2016; 375(24): 2321-34. DOI: http://doi.org/10.1056/NEJMoa1602412

15. Himmelsbach K., Hildt E. Identification of various cell culture models for the study of Zika virus. World J. Virol. 2018; 7(1): 10-20. DOI: http://doi.org/10.5501/wjv.v7.i1.10

16. Chan J.F., Yip C.C., Tsang J.O., Tee K.M., Cai J.P., Chik K.K., et al. Differential cell line susceptibility to the emerging Zika virus: implications for disease pathogenesis, non‐vector‐borne human transmission and animal reservoirs. Emerg. Microbes Infect. 2016; 5: e93. DOI: http://doi.org/10.1038/emi.2016.99

17. Ramos da Silva S., Cheng F., Huang I.C., Jung J.U., Gao S.J. Efficiencies and kinetics of infection in different cell types/lines by African and Asian strains of Zika virus. J. Med. Virol. 2019; 91(2): 179-89. DOI: http://doi.org/10.1002/jmv.25306

18. Barr K.L., Anderson B.D., Prakoso D., Long M.T. Working with Zika and Usutu viruses in vitro. PLoS neglected tropical diseases. PLoS. Negl. Trop. Dis. 2016; 10(8): e0004931. DOI: http://doi.org/10.1371/journal.pntd.0004931

19. Vicenti I., Boccuto A., Giannini A., Dragoni F., Saladini F., Zazzi M. Comparative analysis of different cell systems for Zika virus (ZIKV) propagation and evaluation of anti-ZIKV compounds in vitro. Virus Res. 2018; 244: 64-70. DOI: http://doi.org/0.1016/j.virusres.2017.11.003

20. Willard K.A., Demakovsky L., Tesla B., Goodfellow F.T., Stice S.L., Murdock C.C., et al. Zika virus exhibits lineage-specific phenotypes in cell culture, in aedes aegypti mosquitoes, and in an embryo model. Viruses. 2017; 9(12): 383. DOI: http://doi.org/10.3390/v9120383

21. Kumar A., Jovel J., Lopez-Orozco J., Limonta D., Airo A.M., Hou S., et al. Human Sertoli cells support high levels of Zika virus replication and persistence. Sci. Rep. 2018; 8(1): 5477. DOI: http://doi.org/10.1038/s41598-018-23899-x

22. Kumar A., Hou S., Airo A.M., Limonta D., Mancinelli V., Branton W., et al. Zika virus inhibits type-I interferon production and downstream signaling. EMBO Rep. 2016; 17(12): 1766-75. DOI: http://doi.org/10.15252/embr.201642627

23. Ma W., Li S., Ma S., Jia L., Zhang F., Zhang Y., et al. Zika virus causes testis damage and leads to male infertility in mice. Cell. 2017; 168(3): 542. DOI: http://doi.org/10.1016/j.cell.2017.01.009

24. Duggal N.K., Ritter J.M., Pestorius S.E., Zaki S.R., Davis B.S., Chang G.J., et al. Frequent Zika virus sexual transmission and prolonged viral RNA shedding in an immunodeficient mouse model. Cell Rep. 2017; 18(7): 1751-60. DOI: http://doi.org/10.1016/j.celrep.2017.01.056

25. Hirsch A.J., Smith J.L., Haese N.N., Broeckel R.M., Parkins C.J., Kreklywich C., et al. Zika Virus infection of rhesus macaques leads to viral persistence in multiple tissues. PLoS Pathog. 2017; 13(4): e1006317. DOI: http://doi.org/10.1371/journal.ppat.1006317

26. Siemann D.N., Strange D.P., Maharaj P.N., Shi P.Y., Verma S. Zika virus infects human Sertoli cells and modulates the integrity of the in vitro blood-testis barrier model. J. Virol. 2017;91(22). pii: e00623-17. DOI: http://doi.org/10.1128/JVI.00623-17

27. Uraki R., Hwang J., Jurado K.A., Householder S., Yockey L.J., Hastings A.K., et al. Zika virus causes testicular atrophy. Sci. Adv. 2017; 3(2): e1602899. DOI: http://doi.org/10.1126/sciadv.1602899

28. Spencer J.L., Lahon A., Tran L.L., Arya R.P., Kneubehl A.R., Vogt M.B., et al. Replication of Zika virus in human prostate cells: a potential source of sexually transmitted virus. J. Infect. Dis. 2018; 217(4): 538-47. DOI: http://doi.org/10.1093/infdis/jix436

29. Kim W., Barron D.A., San Martin R., Chan K.S., Tran L.L., Yang F., et al. RUNX1 is essential for mesenchymal stem cell proliferation and myofibroblast differentiation. Proc. Natl. Acad. Sci. U.S.A. 2014; 111(46): 16389-94. DOI: http://doi.org/10.1073/pnas.1407097111

30. Lahon A., Arya R.P., Kneubehl A.R., Vogt M.B., Dailey Garnes N.J., Rico-Hesse R., et al. Characterization of a Zika virus isolate from Colombia. PLoS Negl. Trop. Dis. 2016; 10(9): e0005019. DOI: http://doi.org/10.1371/journal.pntd.0005019

31. Murray K.O., Gorchakov R., Carlson A.R., Berry R., Lai L., Natrajan M., et al. Prolonged detection of Zika virus in vaginal secretions and whole blood. Emerg. Infect. Dis. 2017; 23(1): 99-101. DOI: http://doi.org/10.3201/eid2301.161394

32. Arsuaga M., Bujalance S.G., Díaz-Menéndez M., Vázquez A., Arribas J.R. Probable sexual transmission of Zika virus from a vasectomised man. Lancet Infect. Dis. 2016; 16(10): 1107. DOI: http://doi.org/10.1016/S1473-3099(16)30320-6

33. Froeschl G., Huber K., von Sonnenburg F., Nothdurft H.D., Bretzel G., Hoelscher M., et al. Long-term kinetics of Zika virus RNA and antibodies in body fluids of a vasectomized traveller returning from Martinique: a case report. BMC Infect Dis. 2017; 17(1): 55. DOI: http://doi.org/10.1186/s12879-016-2123-9

34. Atkinson B., Thorburn F., Petridou C., Bailey D., Hewson R., Simpson A.J., et al. Presence and persistence of Zika virus RNA in semen, United Kingdom, 2016. Emerg. Infect. Dis. 2017; 23(4): 611-5. DOI: http://doi.org/10.3201/eid2304.161692

35. Kaid C., Goulart E., Caires-Júnior L.C., Araujo B.H.S., SoaresSchanoski A., Bueno H.M.S., et al. zika virus selectively kills aggressive human embryonal CNS tumor cells in vitro and in vivo. Cancer Res. 2018; 78(12): 3363-74. DOI: http://doi.org/10.1158/0008-5472.CAN-17-3201

36. El Costa H., Gouilly J., Mansuy J.M., Chen Q., Levy C., Cartron G., et al. ZIKA virus reveals broad tissue and cell tropism during the first trimester of pregnancy. Sci. Rep. 2016; 6: 35296. DOI: http://doi.org/10.1038/srep35296