Mouse models for dengue vaccines and antivirals

Journal of Immunological Methods

Volumn 410, Issue , 2014, Pages 34-38

  Plummer, Emily M ^a   Shresta, Sujan ^a  

^a LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

Author keywords

Dengue virus; Mouse model; Non human primate

Indexed keywords

ANTIVIRUS AGENT; DENGUE VACCINE; INTERFERON RECEPTOR; LIVE VACCINE; GAMMA INTERFERON;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN INFECTION; DENGUE; DENGUE VIRUS; DISEASE SEVERITY; MOUSE; MOUSE MODEL; NONHUMAN; PRIMATE MODEL; REINFECTION; VIRUS REPLICATION; WILD TYPE; ANIMAL; DISEASE MODEL; GENETICS; HUMAN; IMMUNOLOGY; MUTANT MOUSE STRAIN; NON-HUMAN PRIMATE; PHYSIOLOGY;

DENGUE VIRUS; MOUSE MODEL; NON-HUMAN PRIMATE;

ANIMALS; DENGUE; DENGUE VACCINES; DENGUE VIRUS; DISEASE MODELS, ANIMAL; HUMANS; INTERFERON-GAMMA; MICE; MICE, MUTANT STRAINS; VIRUS REPLICATION;

EID: 84908553668     PISSN: 00221759     EISSN: 18727905     Source Type: Journal    
DOI: 10.1016/j.jim.2014.01.001     Document Type: Article

References (52)

1. Aguirre S., Maestre A.M., Pagni S., Patel J.R., Savage T., Gutman D., Maringer K., Bernal-Rubio D., Shabman R.S., Simon V., Rodriguez-Madoz J.R., Mulder L.C., Barber G.N., Fernandez-Sesma A. DENV inhibits type I IFN production in infected cells by cleaving human STING. PLoS Pathog. 2012, 8(10):e1002934. 10.1371/journal.ppat.1002934.
2. Akkina R. New generation humanized mice for virus research: comparative aspects and future prospects. Virology 2013, 435(1):14. 10.1016/j.virol.2012.10.007.
3. Akkina R., Berges B.K., Palmer B.E., Remling L., Neff C.P., Kuruvilla J., Connick E., Folkvord J., Gagliardi K., Kassu A., Akkina S.R. Humanized Rag1-/- gammac-/- mice support multilineage hematopoiesis and are susceptible to HIV-1 infection via systemic and vaginal routes. PLoS One 2011, 6(6):e20169. 10.1371/journal.pone.0020169.
4. Ashour J., Morrison J., Laurent-Rolle M., Belicha-Villanueva A., Plumlee C.R., Bernal-Rubio D., Williams K.L., Harris E., Fernandez-Sesma A., Schindler C., Garcia-Sastre A. Mouse STAT2 restricts early dengue virus replication. Cell Host Microbe 2010, 8(5):410. 10.1016/j.chom.2010.10.007.
5. Baker M.A., Cronin M.J., Mountjoy D.G. Variability of skin temperature in the waking monkey. Am. J. Physiol. 1976, 230(2):449.
6. Balmaseda A., Hammond S.N., Perez L., Tellez Y., Saborio S.I., Mercado J.C., Cuadra R., Rocha J., Perez M.A., Silva S., Rocha C., Harris E. Serotype-specific differences in clinical manifestations of dengue. Am. J. Trop. Med. Hyg. 2006, 74(3):449.
7. Balsitis S.J., Williams K.L., Lachica R., Flores D., Kyle J.L., Mehlhop E., Johnson S., Diamond M.S., Beatty P.R., Harris E. Lethal antibody enhancement of dengue disease in mice is prevented by Fc modification. PLoS Pathog. 2010, 6(2):e1000790. 10.1371/journal.ppat.1000790.
8. Bhatt S., Gething P.W., Brady O.J., Messina J.P., Farlow A.W., Moyes C.L., Drake J.M., Brownstein J.S., Hoen A.G., Sankoh O., Myers M.F., George D.B., Jaenisch T., Wint G.R., Simmons C.P., Scott T.W., Farrar J.J., Hay S.I. The global distribution and burden of dengue. Nature 2013, 496(7446):504. 10.1038/nature12060.
9. Blaney J.E., Matro J.M., Murphy B.R., Whitehead S.S. Recombinant, live-attenuated tetravalent dengue virus vaccine formulations induce a balanced, broad, and protective neutralizing antibody response against each of the four serotypes in rhesus monkeys. J. Virol. 2005, 79(9):5516. 10.1128/JVI.79.9.5516-5528.2005.
10. Cole G.A., Wisseman C.L. Pathogenesis of type 1 dengue virus infection in suckling, weanling and adult mice. 1. The relation of virus replication to interferon and antibody formation. Am. J. Epidemiol. 1969, 89(6):669.
11. Diallo M., Ba Y., Sall A.A., Diop O.M., Ndione J.A., Mondo M., Girault L., Mathiot C. Amplification of the sylvatic cycle of dengue virus type 2, Senegal, 1999-2000: entomologic findings and epidemiologic considerations. Emerg. Infect. Dis. 2003, 9(3):362. 10.3201/eid0903.020219.
12. Gibbons R.V., Vaughn D.W. Dengue: an escalating problem. Bmj 2002, 324(7353):1563.
13. Grant D., Tan G.K., Qing M., Ng J.K., Yip A., Zou G., Xie X., Yuan Z., Schreiber M.J., Schul W., Shi P.Y., Alonso S. A single amino acid in nonstructural protein NS4B confers virulence to dengue virus in AG129 mice through enhancement of viral RNA synthesis. J. Virol. 2011, 85(15):7775. 10.1128/JVI.00665-11.
14. Gubler D.J. The economic burden of dengue. Am. J. Trop. Med. Hyg. 2012, 86(5):743. 10.4269/ajtmh.2012.12-0157.
15. Guirakhoo F., Pugachev K., Zhang Z., Myers G., Levenbook I., Draper K., Lang J., Ocran S., Mitchell F., Parsons M., Brown N., Brandler S., Fournier C., Barrere B., Rizvi F., Travassos A., Nichols R., Trent D., Monath T. Safety and efficacy of chimeric yellow Fever-dengue virus tetravalent vaccine formulations in nonhuman primates. J. Virol. 2004, 78(9):4761.
16. Halstead S.B. Dengue. Lancet 2007, 370(9599):1644. 10.1016/S0140-6736(07)61687-0.
17. Halstead S.B. Identifying protective dengue vaccines: guide to mastering an empirical process. Vaccine 2013, 31(41):4501. 10.1016/j.vaccine.2013.06.079.
18. Halstead S.B., Palumbo N.E. Studies on the immunization of monkeys against dengue. II. Protection following inoculation of combinations of viruses. Am. J. Trop. Med. Hyg. 1973, 22(3):375.
19. Halstead S.B., Casals J., Shotwell H., Palumbo N. Studies on the immunization of monkeys against dengue. I. Protection derived from single and sequential virus infections. Am. J. Trop. Med. Hyg. 1973, 22(3):365.
20. Halstead S.B., Shotwell H., Casals J. Studies on the pathogenesis of dengue infection in monkeys. I. Clinical laboratory responses to primary infection. J. Infect. Dis. 1973, 128(1):7.
21. Halstead S.B., Shotwell H., Casals J. Studies on the pathogenesis of dengue infection in monkeys. II. Clinical laboratory responses to heterologous infection. J. Infect. Dis. 1973, 128(1):15.
22. Li X.F., Deng Y.Q., Yang H.Q., Zhao H., Jiang T., Yu X.D., Li S.H., Ye Q., Zhu S.Y., Wang H.J., Zhang Y., Ma J., Yu Y.X., Liu Z.Y., Li Y.H., Qin E.D., Shi P.Y., Qin C.F. A chimeric dengue virus vaccine using Japanese encephalitis virus vaccine strain SA14-14-2 as backbone is immunogenic and protective against either parental virus in mice and nonhuman primates. J. Virol. 2013, 87(24):13694. 10.1128/JVI.00931-13.
23. Lum L.C., Lam S.K., Choy Y.S., George R., Harun F. Dengue encephalitis: a true entity?. Am. J. Trop. Med. Hyg. 1996, 54(3):256.
24. Lynch S.F., Ludlam C.A. Plasma microparticles and vascular disorders. Br. J. Haematol. 2007, 137(1):36. 10.1111/j.1365-2141.2007.06514.x.
25. Mairuhu A.T., Mac Gillavry M.R., Setiati T.E., Soemantri A., ten Cate H., Brandjes D.P., van Gorp E.C. Is clinical outcome of dengue-virus infections influenced by coagulation and fibrinolysis? A critical review of the evidence. Lancet Infect. Dis. 2003, 3(1):33.
26. Marchette N.J., Halstead S.B., Falkler W.A., Stenhouse A., Nash D. Studies on the pathogenesis of dengue infection in monkeys. 3. Sequential distribution of virus in primary and heterologous infections. J. Infect. Dis. 1973, 128(1):23.
27. Mota J., Rico-Hesse R. Dengue virus tropism in humanized mice recapitulates human dengue fever. PLoS One 2011, 6(6):e20762. 10.1371/journal.pone.0020762.
28. Nimmannitya S. Dengue hemorrhagic fever: diagnosis and management. Dengue and dengue hemorrhagic fever 1997, CAB International, New York.
29. Onlamoon N., Noisakran S., Hsiao H.M., Duncan A., Villinger F., Ansari A.A., Perng G.C. Dengue virus-induced hemorrhage in a nonhuman primate model. Blood 2010, 115(9):1823. 10.1182/blood-2009-09-242990.
30. Osorio J.E., Brewoo J.N., Silengo S.J., Arguello J., Moldovan I.R., Tary-Lehmann M., Powell T.D., Livengood J.A., Kinney R.M., Huang C.Y., Stinchcomb D.T. Efficacy of a tetravalent chimeric dengue vaccine (DENVax) in cynomolgus macaques. Am. J. Trop. Med. Hyg. 2011, 84(6):978. 10.4269/ajtmh.2011.10-0592.
31. Patey O., Ollivaud L., Breuil J., Lafaix C. Unusual neurologic manifestations occurring during dengue fever infection. Am. J. Trop. Med. Hyg. 1993, 48(6):793.
32. Perry S.T., Buck M.D., Plummer E.M., Penmasta R.A., Batra H., Stavale E.J., Warfield K.L., Dwek R.A., Butters T.D., Alonzi D.S., Lada S.M., King K., Klose B., Ramstedt U., Shresta S. An iminosugar with potent inhibition of dengue virus infection in vivo. Antivir. Res. 2013, 98(1):35. 10.1016/j.antiviral.2013.01.004.
33. Prestwood T.R., Prigozhin D.M., Sharar K.L., Zellweger R.M., Shresta S. A mouse-passaged dengue virus strain with reduced affinity for heparan sulfate causes severe disease in mice by establishing increased systemic viral loads. J. Virol. 2008, 82(17):8411. 10.1128/JVI.00611-08.
34. Rathakrishnan A., Wang S.M., Hu Y., Khan A.M., Ponnampalavanar S., Lum L.C., Manikam R., Sekaran S.D. Cytokine expression profile of dengue patients at different phases of illness. PLoS One 2012, 7(12):e52215. 10.1371/journal.pone.0052215.
35. Rico-Hesse R. Dengue virus evolution and virulence models. Clin. Infect. Dis. 2007, 44(11):1462. 10.1086/517587.
36. Sabchareon A., Wallace D., Sirivichayakul C., Limkittikul K., Chanthavanich P., Suvannadabba S., Jiwariyavej V., Dulyachai W., Pengsaa K., Wartel T.A., Moureau A., Saville M., Bouckenooghe A., Viviani S., Tornieporth N.G., Lang J. Protective efficacy of the recombinant, live-attenuated, CYD tetravalent dengue vaccine in Thai schoolchildren: a randomised, controlled phase 2b trial. Lancet 2012, 380(9853):1559. 10.1016/S0140-6736(12)61428-7.
37. Sabin A.B., Schlesinger R.W. Production of Immunity to Dengue with Virus Modified by Propagation in Mice. Science 1945, 101(2634):640. 10.1126/science.101.2634.640.
38. Sahaphong S., Riengrojpitak S., Bhamarapravati N., Chirachariyavej T. Electron microscopic study of the vascular endothelial cell in dengue hemorrhagic fever. Southeast Asian J. Trop. Med. Public Health 1980, 11(2):194.
39. Scherer W.F., Russell P.K., Rosen L., Casals J., Dickerman R.W. Experimental infection of chimpanzees with dengue viruses. Am. J. Trop. Med. Hyg. 1978, 27(3):590.
40. Shresta S., Sharar K.L., Prigozhin D.M., Beatty P.R., Harris E. Murine model for dengue virus-induced lethal disease with increased vascular permeability. J. Virol. 2006, 80(20):10208. 10.1128/JVI.00062-06.
41. Tan G.K., Ng J.K., Trasti S.L., Schul W., Yip G., Alonso S. A non mouse-adapted dengue virus strain as a new model of severe dengue infection in AG129 mice. PLoS Negl. Trop. Dis. 2010, 4(4):e672. 10.1371/journal.pntd.0000672.
42. Tapia-Conyer R., Betancourt-Cravioto M., Mendez-Galvan J. Dengue: an escalating public health problem in Latin America. Paediatr. Int. Child Health 2012, 32(Suppl. 1):14. 10.1179/2046904712Z.00000000046.
43. Wang E., Ni H., Xu R., Barrett A.D., Watowich S.J., Gubler D.J., Weaver S.C. Evolutionary relationships of endemic/epidemic and sylvatic dengue viruses. J. Virol. 2000, 74(7):3227.
44. Watanabe S., Rathore A.P., Sung C., Lu F., Khoo Y.M., Connolly J., Low J., Ooi E.E., Lee H.S., Vasudevan S.G. Dose- and schedule-dependent protective efficacy of celgosivir in a lethal mouse model for dengue virus infection informs dosing regimen for a proof of concept clinical trial. Antivir. Res. 2012, 96(1):32. 10.1016/j.antiviral.2012.07.008.
45. Weiskopf D., Yauch L.E., Angelo M.A., John D.V., Greenbaum J.A., Sidney J., Kolla R.V., De Silva A.D., de Silva A.M., Grey H., Peters B., Shresta S., Sette A. Insights into HLA-restricted T cell responses in a novel mouse model of dengue virus infection point toward new implications for vaccine design. J. Immunol. 2011, 187(8):4268. 10.4049/jimmunol.1101970.
46. World Health Organization Dengue: Guidelines for Diagnosis, Treatment, Prevention and Control. WHO/HTM/NTD/DEN/2009.1 2009, World Health Organization.
47. World Health Organization WHO Expert Committee on Biological Standardization. World Health Organ Tech Rep Ser 2013, 979:1-366. back cover.
48. Yauch L.E., Shresta S. Mouse models of dengue virus infection and disease. Antivir. Res. 2008, 80(2):87. 10.1016/j.antiviral.2008.06.010.
49. Yauch L.E., Zellweger R.M., Kotturi M.F., Qutubuddin A., Sidney J., Peters B., Prestwood T.R., Sette A., Shresta S. A protective role for dengue virus-specific CD8+ T cells. J. Immunol. 2009, 182(8):4865. 10.4049/jimmunol.0801974.
50. Yauch L.E., Prestwood T.R., May M.M., Morar M.M., Zellweger R.M., Peters B., Sette A., Shresta S. CD4+ T cells are not required for the induction of dengue virus-specific CD8+ T cell or antibody responses but contribute to protection after vaccination. J. Immunol. 2010, 185(9):5405. 10.4049/jimmunol.1001709.
51. Yu C.Y., Chang T.H., Liang J.J., Chiang R.L., Lee Y.L., Liao C.L., Lin Y.L. Dengue virus targets the adaptor protein MITA to subvert host innate immunity. PLoS Pathog. 2012, 8(6):e1002780. 10.1371/journal.ppat.1002780.
52. Zellweger R.M., Prestwood T.R., Shresta S. Enhanced infection of liver sinusoidal endothelial cells in a mouse model of antibody-induced severe dengue disease. Cell Host Microbe 2010, 7(2):128. 10.1016/j.chom.2010.01.004.