Zika Virus Infection in Dexamethasone-immunosuppressed Mice Demonstrating Disseminated Infection with Multi-organ Involvement Including Orchitis Effectively Treated by Recombinant Type I Interferons

EBioMedicine

Volumn 14, Issue , 2016, Pages 112-122

  Chan, Jasper Fuk Woo ^a,b   Zhang, Anna Jinxia ^b   Chan, Chris Chung Sing ^b   Yip, Cyril Chik Yan ^b   Mak, Winger Wing Nga ^b   Zhu, Houshun ^b   Poon, Vincent Kwok Man ^b   Tee, Kah Meng ^b   Zhu, Zheng ^b   Cai, Jian Piao ^b   Tsang, Jessica Oi Ling ^b   Chik, Kenn Ka Heng ^b   Yin, Feifei ^c   Chan, Kwok Hung ^b   Kok, Kin Hang ^b   Jin, Dong Yan ^b   Au Yeung, Rex Kwok Him ^b   Yuen, Kwok Yung ^a,b  

^a THE UNIVERSITY OF HONG KONG   (Hong Kong)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

^c HAINAN MEDICAL UNIVERSITY   (China)

Author keywords

Animal; Flavivirus; Interferon; Model; Mouse; Orchitis; Steroid; Testis; Treatment; Zika

Indexed keywords

CD45 ANTIGEN; CD8 ANTIGEN; INTERFERON BETA SERINE; NONSTRUCTURAL PROTEIN 1; PEGINTERFERON ALPHA2B; ANTIVIRUS AGENT; DEXAMETHASONE; INTERFERON;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE TRANSMISSION; FEMALE; HISTOPATHOLOGY; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; INFLAMMATORY INFILTRATE; MALE; MALE FERTILITY; MOUSE; NONHUMAN; ORCHITIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIRAL CLEARANCE; VIRUS LOAD; WEIGHT REDUCTION; ZIKA FEVER; ANIMAL; BRAIN; DISEASE MODEL; DRUG EFFECTS; IMMUNOCOMPROMISED PATIENT; IMMUNOLOGY; KIDNEY; METABOLISM; PATHOLOGY; VIROLOGY; ZIKA VIRUS; ZIKA VIRUS INFECTION;

ANIMALS; ANTIVIRAL AGENTS; BRAIN; DEXAMETHASONE; DISEASE MODELS, ANIMAL; FEMALE; IMMUNOCOMPROMISED HOST; INTERFERON TYPE I; KIDNEY; MALE; MICE; ORCHITIS; VIRAL LOAD; ZIKA VIRUS; ZIKA VIRUS INFECTION;

EID: 85004000295     PISSN: None     EISSN: 23523964     Source Type: Journal    
DOI: 10.1016/j.ebiom.2016.11.017     Document Type: Article

References (58)

1. Abbink, P., Larocca, R.A., De La Barrera, R.A., et al. Protective efficacy of multiple vaccine platforms against Zika virus challenge in rhesus monkeys. Science, 2016 (pii: aah6157. Epub ahead of print).
2. Aliota, M.T., Caine, E.A., Walker, E.C., Larkin, K.E., Camacho, E., Osorio, J.E., Characterization of lethal Zika virus infection in AG129 mice. PLoS Negl. Trop. Dis., 10, 2016, e0004682.
3. Arzuza-Ortega, L., Polo, A., Perez-Tatis, G., et al. Fatal sickle cell disease and Zika virus infection in girl from Colombia. Emerg. Infect. Dis. 22 (2016), 925–927.
4. Bell, T.M., Field, E.J., Narang, H.K., Zika virus infection of the central nervous system of mice. Arch. Gesamte. Virusforsch. 35 (1971), 183–193.
5. Bhagat, M., Zaki, S.A., Sharma, S., Manglani, M.V., Acute glomerulonephritis in dengue haemorrhagic fever in the absence of shock, sepsis, haemolysis or rhabdomyolysis. Paediatr. Int. Child Health 32 (2012), 161–163.
6. Bonaldo, M.C., Ribeiro, I.P., Lima, N.S., et al. Isolation of infective Zika virus from urine and saliva of patients in Brazil. PLoS Negl. Trop. Dis., 10, 2016, e0004816.
7. Brault, J.B., Khou, C., Basset, J., et al. Comparative analysis between Flaviviruses reveals specific neural stem cell tropism for Zika virus in the mouse developing Neocortex. EBioMedicine 10 (2016), 71–76.
8. Calvet, G., Aguiar, R.S., Melo, A.S., et al. Detection and sequencing of Zika virus from amniotic fluid of fetuses with microcephaly in Brazil: a case study. Lancet Infect. Dis. 16 (2016), 653–660.
9. Cao-Lormeau, V.M., Blake, A., Mons, S., et al. Guillain-Barre syndrome outbreak associated with Zika virus infection in French Polynesia: a case-control study. Lancet 387 (2016), 1531–1539.
10. Carteaux, G., Maquart, M., Bedet, A., et al. Zika virus associated with Meningoencephalitis. N. Engl. J. Med. 374 (2016), 1595–1596.
11. Chan, J.F., Chan, K.H., Kao, R.Y., et al. Broad-spectrum antivirals for the emerging Middle East respiratory syndrome coronavirus. J. Infect. 67 (2013), 606–616.
12. Chan, J.F., Choi, G.K., Tsang, A.K., et al. Development and evaluation of novel real-time reverse transcription-PCR assays with locked nucleic acid probes targeting leader sequences of human-pathogenic coronaviruses. J. Clin. Microbiol. 53 (2015), 2722–2726.
13. Chan, J.F., Yao, Y., Yeung, M.L., et al. Treatment with Lopinavir/ritonavir or interferon-beta1b improves outcome of MERS-CoV infection in a nonhuman primate model of common marmoset. J. Infect. Dis. 212 (2015), 1904–1913.
14. Chan, J.F., Choi, G.K., Yip, C.C., Cheng, V.C., Yuen, K.Y., Zika fever and congenital Zika syndrome: an unexpected emerging arboviral disease. J. Infect. 72 (2016), 507–524.
15. Chan, J.F., Yip, C.C., Tsang, J.O., 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., 5, 2016, e93.
16. Chatterjee, N., Mukhopadhyay, M., Ghosh, S., Mondol, M., Das, C., Patar, K., An observational study of dengue fever in a tertiary care hospital of eastern India. J. Assoc. Physicians India 62 (2014), 224–227.
17. Cugola, F.R., Fernandes, I.R., Russo, F.B., et al. The Brazilian Zika virus strain causes birth defects in experimental models. Nature 534 (2016), 267–271.
18. de Paula, F.B., de Oliveira Dias, J.R., Prazeres, J., et al. Ocular findings in infants with microcephaly associated with presumed Zika virus congenital infection in Salvador, Brazil. JAMA Ophthalmol., 2016, 10.1001/jamaophthalmol.2016.0267 (Epub ahead of print).
19. Dick, G.W., Zika virus. II. Pathogenicity and physical properties. Trans. R. Soc. Trop. Med. Hyg. 46 (1952), 521–534.
20. Dowall, S.D., Graham, V.A., Rayner, E., et al. A susceptible mouse model for Zika virus infection. PLoS Negl. Trop. Dis., 10, 2016, e0004658.
21. Dudley, D.M., Aliota, M.T., Mohr, E.L., et al. A rhesus macaque model of Asian-lineage Zika virus infection. Nat. Commun., 7, 2016, 12204.
22. Duffy, M.R., Chen, T.H., Hancock, W.T., et al. Zika virus outbreak on Yap Island, Federated States of Micronesia. N. Engl. J. Med. 360 (2009), 2536–2543.
23. Duijster, J.W., Goorhuis, A., van Genderen, P.J., et al. Zika virus infection in 18 travellers returning from Surinam and the Dominican Republic, The Netherlands, November 2015–March 2016. Infection, 2016 (Epub ahead of print).
24. Foy, B.D., Kobylinski, K.C., Chilson Foy, J.L., et al. Probable non-vector-borne transmission of Zika virus, Colorado, USA. Emerg. Infect. Dis. 17 (2011), 880–882.
25. Gourinat, A.C., O'Connor, O., Calvez, E., Goarant, C., Dupont-Rouzeyrol, M., Detection of Zika virus in urine. Emerg. Infect. Dis. 21 (2015), 84–86.
26. Govero, J., Esakky, P., Scheaffer, S.M., et al. Zika virus infection damages the testes in mice. Nature, 2016, 10.1038/nature20556 (Epub ahead of print).
27. Graham, J.B., Thomas, S., Swarts, J., et al. Genetic diversity in the collaborative cross model recapitulates human West Nile virus disease outcomes. MBio, 6, 2015 (e00493-15).
28. Grant, A., Ponia, S.S., Tripathi, S., et al. Zika virus targets human STAT2 to inhibit type I interferon signaling. Cell Host Microbe 19 (2016), 882–890.
29. Hamel, R., Dejarnac, O., Wichit, S., et al. Biology of Zika virus infection in human skin cells. J. Virol. 89 (2015), 8880–8896.
30. Hughes, B.W., Addanki, K.C., Sriskanda, A.N., McLean, E., Bagasra, O., Infectivity of immature neurons to Zika virus: a link to congenital Zika syndrome. EBioMedicine 10 (2016), 65–70.
31. Khorsandi, L., Mirhoseini, M., Mohamadpour, M., Orazizadeh, M., Khaghani, S., Effect of curcumin on dexamethasone-induced testicular toxicity in mice. Pharm. Biol. 51 (2013), 206–212.
32. Lazear, H.M., Govero, J., Smith, A.M., et al. A mouse model of Zika virus pathogenesis. Cell Host Microbe 19 (2016), 720–730.
33. Leal, M.C., Muniz, L.F., Ferreira, T.S., et al. Hearing loss in infants with microcephaly and evidence of congenital Zika virus infection - Brazil, November 2015–May 2016. MMWR Morb. Mortal. Wkly Rep. 65 (2016), 917–919.
34. Macnamara, F.N., Zika virus: a report on three cases of human infection during an epidemic of jaundice in Nigeria. Trans. R. Soc. Trop. Med. Hyg. 48 (1954), 139–145.
35. Mecharles, S., Herrmann, C., Poullain, P., et al. Acute myelitis due to Zika virus infection. Lancet, 387, 2016, 1481.
36. Mercado, M., Acosta-Reyes, J., Parra, E., et al. Clinical and histopathological features of fatal cases with dengue and chikungunya virus co-infection in Colombia, 2014 to 2015. Eur. Surg., 21, 2016.
37. Miner, J.J., Cao, B., Govero, J., et al. Zika virus infection during pregnancy in mice causes placental damage and fetal demise. Cell 165 (2016), 1081–1091.
38. Mlakar, J., Korva, M., Tul, N., et al. Zika virus associated with microcephaly. N. Engl. J. Med. 374 (2016), 951–958.
39. Musso, D., Gubler, D.J., Zika Virus. Clin. Microbiol. Rev. 29 (2016), 487–524.
40. Musso, D., Roche, C., Robin, E., Nhan, T., Teissier, A., Cao-Lormeau, V.M., Potential sexual transmission of Zika virus. Emerg. Infect. Dis. 21 (2015), 359–361.
41. Musso, D., Roche, C., Nhan, T.X., Robin, E., Teissier, A., Cao-Lormeau, V.M., Detection of Zika virus in saliva. J. Clin. Virol. 68 (2015), 53–55.
42. Pan American Health Organization/World Health Oganization (PAHO/WHO), Epidemiological alert - neurological syndrome, congenital malformations, and Zika virus infeciton. Implications for Public Health in the Americas, 1, December 2015 http://www.paho.org/hq/index.php?option=com_docman&task=doc_view&Itemid=270&gid=32405&lang=e (Accessed 1 February 2016).
43. Quaresma, J.A., Pagliari, C., Medeiros, D.B., Duarte, M.I., Vasconcelos, P.F., Immunity and immune response, pathology and pathologic changes: progress and challenges in the immunopathology of yellow fever. Rev. Med. Virol. 23 (2013), 305–318.
44. Rossi, S.L., Tesh, R.B., Azar, S.R., et al. Characterization of a novel murine model to study Zika virus. Am.J.Trop. Med. Hyg. 94 (2016), 1362–1369.
45. Sarmiento-Ospina, A., Vasquez-Serna, H., Jimenez-Canizales, C.E., Villamil-Gomez, W.E., Rodriguez-Morales, A.J., Zika virus associated deaths in Colombia. Lancet Infect. Dis., 2016, 10.1016/S1473-3099(16)30006-8 (Epub ahead of print).
46. Screaton, G., Mongkolsapaya, J., Yacoub, S., Roberts, C., New insights into the immunopathology and control of dengue virus infection. Nat. Rev. Immunol. 15 (2015), 745–759.
47. Solomon, T., Dung, N.M., Wills, B., et al. Interferon alfa-2a in Japanese encephalitis: a randomised double-blind placebo-controlled trial. Lancet 361 (2003), 821–826.
48. Tian, Y., Kuo, C.F., Cheng, W.L., Ou, J.H., Enhancement of hepatitis B virus replication by androgen and its receptor in mice. J. Virol. 86 (2012), 1904–1910.
49. Torres, J.R., Liprandi, F., Goncalvez, A.P., Acute parotitis due to dengue virus. Clin. Infect. Dis. 31 (2000), E28–E29.
50. Wang, Y., Lobigs, M., Lee, E., Mullbacher, A., CD8 + T cells mediate recovery and immunopathology in West Nile virus encephalitis. J. Virol. 77 (2003), 13323–13334.
51. Way, J.H., Bowen, E.T., Platt, G.S., Comparative studies of some African arboviruses in cell culture and in mice. J. Gen. Virol. 30 (1976), 123–130.
52. Weinbren, M.P., Williams, M.C., Zika virus: further isolations in the Zika area, and some studies on the strains isolated. Trans. R. Soc. Trop. Med. Hyg. 52 (1958), 263–268.
53. World Health Organization. Zika situation report. 27, http://who.int/emergencies/zika-virus/situation-report/27-october-2016/en/, October 2016 (Accessed 30 October 2016).
54. Zhang, A.J., Li, C., To KK, et al. Toll-like receptor 7 agonist imiquimod in combination with influenza vaccine expedites and augments humoral immune responses against influenza A(H1N1)pdm09 virus infection in BALB/c mice. Clin. Vaccine Immunol. 21 (2014), 570–579.
55. Zheng, B.J., Chan, K.W., Lin, Y.P., et al. Delayed antiviral plus immunomodulator treatment still reduces mortality in mice infected by high inoculum of influenza A/H5N1 virus. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 8091–8096.
56. Zhou, J., Chu, H., Li, C., et al. Active replication of Middle East respiratory syndrome coronavirus and aberrant induction of inflammatory cytokines and chemokines in human macrophages: implications for pathogenesis. J. Infect. Dis. 209 (2014), 1331–1342.
57. Zhu, Z., Chan, J.F., Tee, K.M., et al. Comparative genomic analysis of pre-epidemic and epidemic Zika virus strains for virological factors potentially associated with the rapidly expanding epidemic. Emerg. Microbes Infect., 5, 2016, e22.
58. Zumla, A., Chan, J.F., Azhar, E.I., Hui, D.S., Yuen, K.Y., Coronaviruses - drug discovery and therapeutic options. Nat. Rev. Drug Discov. 15 (2016), 327–347.