Viremia and antibody response in green monkeys (Chlorocebus aethiops sabaeus) infected with dengue virus type 2: A potential model for vaccine testing

Microbiology and Immunology

Volumn 53, Issue 4, 2009, Pages 216-223

  Martín, Jorge ^a   Hermida, Lisset ^a   Castro, Jorge ^a   Lazo, Laura ^a   Martínez, Rafael ^a   Gil, Lázaro ^a   Romero, Yaremis ^a   Puente, Pedro ^a   Zaragoza, Santiago ^a   Cosme, Karelia ^a   Guzmán, María G ^b   Cardosa, Jane ^c   Guillén, Gerardo ^a  

^a CENTER FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Cuba)

^b INSTITUTO DE MEDICINA TROPICAL PEDRO KOURÍ   (Cuba)

^c Faculty of Engineering   (Malaysia)

Author keywords

Dengue; Monkeys; Viremia

Indexed keywords

IMMUNOGLOBULIN G; VACCINE; VIRUS ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TESTING ALTERNATIVE; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; BEHAVIOR; BLOOD SAMPLING; CERCOPITHECUS; CHLOROCEBUS AETHIOPS SABAEUS; CLINICAL ASSESSMENT; CONTROLLED STUDY; DENGUE VIRUS; DENGUE VIRUS 2; DRUG BLOOD LEVEL; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMORAL IMMUNITY; IMMUNE RESPONSE; INOCULATION; MACACA; NONHUMAN; RHESUS MONKEY; VIREMIA; ANIMAL; BLOOD; DENGUE; DISEASE MODEL; IMMUNOLOGY; PATHOGENICITY; VIROLOGY;

ANIMALIA; CERCOPITHECUS AETHIOPS; CERCOPITHECUS SABAEUS; DENGUE VIRUS TYPE 2; MACACA;

ANIMALS; ANTIBODIES, VIRAL; CERCOPITHECUS AETHIOPS; DENGUE; DENGUE VIRUS; DISEASE MODELS, ANIMAL; VACCINES; VIREMIA;

EID: 70249150038     PISSN: 03855600     EISSN: 13480421     Source Type: Journal    
DOI: 10.1111/j.1348-0421.2009.00112.x     Document Type: Article

References (55)

1. Gubler D.J. (2002) Epidemic dengue/dengue hemorrhagic fever as a public health, social and economic problem in the 21st century. Trends Microbiol 10: 100-03.
2. Halstead S.B. (1982) Immune enhancement of viral infection. Prog Allergy 31: 301-64.
3. Vaughn D.W. (2000) Invited commentary: Dengue lessons from Cuba. Am J Epidemiol 152: 800-03.
4. Gubler D.J. (2004) The changing epidemiology of yellow fever and dengue, 1900 to 2003: full circle? Comp Immunol Microbiol Infect Dis 27: 319-30.
5. Bente D.A., Rico-Hesse R. (2006) Models of dengue virus infection. Drug Discov Today Dis Models 3: 97-103.
6. Charlier N., De Clercq E., Neyts J. (2006) Mouse and hamster models for flavivirus infections. Novartis Foundation Symposium 277: 217-31.
7. Yauch L.E., Shresta S. (2008) Mouse models of dengue virus infection and disease. Antiviral Res 80: 87-93.
8. Halstead S.B., Shotwell H., Casals S. (1973) Studies on the pathogenesis of dengue infection in monkeys. I. Clinical laboratory responses to primary infection. J Infect Dis 128: 7-14.
9. Scott R.M., Nisalak A., Eckels K.H., Tingpalapong M., Harrison V.R., Gould D.J., Chapple F.E., Russell P.K. (1980) Dengue-2 vaccine: viremia and immune responses in rhesus monkeys. Infect Immun 27: 181-86.
10. Capitanio J.P., Kyes R.C., Fairbanks L.A. (2006) Considerations in the Selection and Conditioning of Old World Monkeys for Laboratory Research: Animals from Domestic Sources. ILAR J 47: 294-306.
11. Research Resources Information Center (2003) Demands for rhesus monkeys in biomedical research: a workshop report. ILAR J 44: 222-35.
12. Alvarez-Lajonchere L., Amador-Cañizares Y., Frías R., Milian Y., Musacchio A., Guerra I., Acosta-Rivero N., Martínez G., Castro J., Puentes P., Cosme K., Dueñas-Carrera S. (2008) Immunization with a recombinant fowlpox virus expressing a hepatitis C virus core-E1 polyprotein variant, protects mice and African green monkeys (Chlorocebus aethiops sabaeus) against challenge with a surrogate vaccinia virus. Biotechnol Appl Biochem 51: 97-105.
13. Pandrea I., Apetrei C., Dufour J., Dillon N., Barbercheck J., Metzger M., Jacquelin B., Bohm R., Marx P.A., Barre-Sinoussi F., Hirsch V.M., Müller-Trutwin M.C., Lackner A.A., Veazey R.S. (2006) Simian immunodeficiency virus SIVagm.sab infection of Caribbean African green monkeys: a new model for the study of SIV pathogenesis in natural hosts. J Virol 80: 4858-67.
14. WeissW.J., Murphy T., Lynch M.E., Frye J., Buklan A., Gray B., Lenoy E., Mitelman S., O'Connell J., Quartuccio S., Huntley C. (2003) Inhalation efficacy of RFI-641 in an African green monkey model of RSV infection. J Med Primatol 32: 82-88.
15. Yalcin S., Mukai T., Kondo K., Ami Y., Okawa T., Kojima A., Kurata T., Yamanishi K. (1992) Experimental infection of cynomolgus and African green monkeys with human herpesvirus 6. J Gen Virol 73: 1673-77.
16. Churdboonchart V., Bhamarapravati N., Peampramprecha S. (1991) Antibodies against dengue viral proteins in primary and secondary dengue hemorrhagic fever. Am J Trop Med Hyg 44: 481-93.
17. Alison J.J., Martin D.A., Karabatsos N., Roehrig J.T. (2000) Detection of anti-arboviral immunoglobulin G by using a monoclonal antibody based capture enzyme-linked immunosorbent assay. J Clin Microbiol 38: 1827-31.
18. Roehrig J.T. (1997) Immunochemistry of dengue virus. In: Gubler D.J., Kuno G., eds. Dengue and dengue hemorrhagic fever, 1st edn. New York: CAB International, pp. 199-219.
19. Morens D.M., Halstead S.B., Repik P.M. (1985) Simplified plaque reduction assay for dengue viruses by semimicro methods in BHK 21 cells: comparison of the BHK suspension test with standard plaque reduction neutralization. J Clin Microbiol 22: 250-54.
20. Blair P.J., Kochel T.J., Raviprakash K., Guevara C., Salazar M.,Wu S.J., Olson J.G., Porter K.R. (2006) Evaluation of immunity and protective efficacy of a dengue-3 pre-membrane and envelope DNA vaccine in Aotus nancymae monkeys. Vaccine 24: 1427-32.
21. Koraka P., Benton S., van Amerongen G., Stittelaar K.J., Osterhaus A.D. (2007) Efficacy of a live attenuated tetravalent candidate dengue vaccine in naïve and previously infected cynomolgus macaques. Vaccine 25: 5409-16.
22. McGee C.E., Lewis M.G., Claire M.S.,Wagner W., Lang J., Guy B., Tsetsarkin K., Higgs S., Decelle T. (2008) Recombinant chimeric virus with wild-type dengue 4 virus premembrane and envelope and virulent yellow fever virus Asibi backbone sequences is dramatically attenuated in nonhuman primates. J Infect Dis 197: 693-97.
23. Blaney J.E. Jr., Sathe N.S., Goddard L., Hanson C.T., Romero T.A., Hanley K.A., Murphy B.R.,Whitehead S.S. (2008) Dengue virus type 3 vaccine candidates generated by introduction of deletions in the 3′ untranslated region (3′-UTR) or by exchange of the DENV-3 3′-UTR with that of DENV-4. Vaccine 26: 817-28.
24. Pletnev A.G., Bray M., Hanley K.A., Speicher J., Elkins R. (2001) Tick-borne Langat/mosquito-borne dengue flavivirus chimera, a candidate live attenuated vaccine for protection against disease caused by members of the tick-borne encephalitis virus complex: evaluation in rhesus monkeys and in mosquitoes. J Virol 75: 8259-67.
25. Raviprakash K.,Wang D., Ewing D., Holman D.H., Block K., Woraratanadharm J., Chen L., Hayes C., Dong J.Y., Porter K. (2008) A tetravalent dengue vaccine based on a complex adenovirus vector provides significant protection in rhesus monkeys against all four serotypes of dengue virus. J Virol 82: 6927-34.
26. Schiavetta A.M., Harre J.G.,Wagner E., Simmons M., Raviprakash K. (2003) Variable susceptibility of the Owl monkey (Aotus nacymae) to four serotypes of dengue virus. Contemp Top Lab Anim Sci 42: 12-20.
27. Simmons M., Porter K.R., Hayes C.G., Vaughn D.W., Putnak R. (2006) Characterization of antibody responses to combinations of a dengue virus type 2 DNA vaccine and two dengue virus type 2 protein vaccines in rhesus macaques. J Virol 80: 9577-85.
28. Putnak J.R., Coller B.A., Voss G., Vaughn D.W., Clements D., Peters I., Bignami G., Houng H.S., Chen R.C., Barvir D.A., Seriwatana J., Cayphas S., Garçon N., Gheysen D., Kanesa-Thasan N., McDonell M., Humphreys T., Eckels K.H., Prieels J.P., Innis B.L. (2005) An evaluation of dengue type-2 inactivated, recombinant subunit, and live-attenuated vaccine candidates in the rhesus macaque model. Vaccine 23: 4442-52.
29. SunW., Nisalak A., Gettayacamin M., Eckels K.H., Putnak J.R., Vaughn D.W., Innis B.L., Thomas S.J., Endy T.P. (2006) Protection of rhesus monkeys against dengue virus challenge after tetravalent live attenuated dengue virus vaccination. J Infect Dis 193: 1658-65.
30. Velzing J., Groen J., Drouet M.T., van Amerongen G., Copra C., Osterhaus A.D., Deubel V. (1999) Induction of protective immunity against Dengue virus type 2: comparison of candidate live attenuated and recombinant vaccines. Vaccine 17: 1312-20.
31. Hermida L., Bernardo L., Martín J., Alvarez M., Prado I., López C., de la C Sierra B., Martínez R., Rodríguez R., Zulueta A., Pérez A.B., Lazo L., Rosario D., Guillén G., Guzmán M.G. (2006) A recombinant fusion protein containing the domain III of the dengue-2 envelope protein is immunogenic and protective in nonhuman primates. Vaccine 24: 3165-71.
32. Lanciotti R.S., Calisher C.H., Gubler D.J., Chang G.J., Vorndam A.V. (1992) Rapid detection and typing of dengue viruses from clinical samples using reverse transcriptase-polymerase chain reaction. J Clin Microbiol 30: 545-51.
33. Rosario D., Alvarez M., Díaz J., Contreras R., Rodríguez R., Vázquez S., Guzmán M.G. (1998) Polymerase chain reaction for rapid detection and serotyping of dengue virus in clinical samples. Rev Panam Salud Publica 4: 1-5.
34. Sa-ngasang A.,Wibulwattanakij S., Chanama S., O-rapinpatipat A., A-nuegoonpipat A., Anantapreecha S., Sawanpanyalert P., Kurane I. (2003) Evaluation of RT-PCR as a tool for diagnosis of secondary dengue virus infection. Jpn J Infect Dis 56: 205-09.
35. Saxena P., Dash P.K., Santhosh S.R., Shrivastava A., Parida M., Rao P.L. (2008) Development and evaluation of one step single tube multiplex RT-PCR for rapid detection and typing of dengue viruses. Virol J 30: 5-20.
36. Freire M.S., Marchevsky R.S., Almeida L.F.C., Yamamura A.M.Y., Caride E.C., Brindeiro P.A., Motta M.C.A., Nogueira R.M.R., Kubelka C.F., Bonaldo M.C., Galler R. (2007)Wild dengue virus types 1, 2 and 3 viremia in rhesus monkeys. Mem Inst Oswaldo Cruz 102: 203-08.
37. Guirakhoo F., Zhang Z., Myers G., Johnson B.W., Pugachev K., Nichols R., Brown N., Levenbook I., Draper K., Cyrek S., Lang J., Fournier C., Barrere B., Delagrave S., Monath T.P. (2004) A single amino acid substitution in the envelope protein of chimeric yellow fever-dengue 1 vaccine virus reduces neurovirulence for suckling mice and viremia/viscerotropism for monkeys. J Virol 78: 9998-10008.
38. Monath T.P., Guirakhoo F., Nichols R., Yoksan S., Schrader R., Murphy C., Blum P.,Woodward S., McCarthy K., Mathis D., Johnson C., Bedford P. (2003) Chimeric live, attenuated vaccine against Japanese encephalitis (ChimeriVax-JE): phase 2 clinical trials for safety and immunogenicity, effect of vaccine dose and schedule, and memory response to challenge with inactivated Japanese encephalitis antigen. J Infect Dis 188: 1213-30.
39. Angsubhakorn S., Yoksan S., Bhamarapravati N., Moe J.B., Marchette N.J., Pradermwong A., Sahaphong S. (1988) Dengue-4 vaccine: neurovirulence, viraemia and immune responses in rhesus and cynomolgus monkeys. Trans R Soc Trop Med Hyg 82: 746-49.
40. Butrapet S., Rabablert J., Angsubhakorn S.,WirayaratW., Huang C., Kinney R., Punyim S., Bhamarapravati N. (2002) Chimeric dengue type 2/ type 1 viruses induce immune responses in cynomolgus monkeys. Southeast Asian J Trop Med Public Health 33: 589-99.
41. Guzmán M.G., Rodríguez R., Rodríguez R., Hermida L., Alvarez M., Lazo L., Muné M., Rosario D., Valdés K., Váazquez S., Martínez R., Serrano T., Páez J., Espinosa R., Pumariega T., Guillén G. (2003) Induction of neutralizing antibodies and partial protection from viral challenge in Macaca fascicularis immunized with recombinant Dengue 4 virus envelope glycoprotein expressed in Pichia pastoris. Am J Trop Med Hyg 69: 129-34.
42. Halstead S.B. (2003) Neutralization and antibody-dependent enhancement of dengue viruses. Adv Virus Res 60: 421-67.
43. Vaughn D.W., Green S., Kalayanarooj S., Innis B.L., Nimmannitya S., Suntayakorn S., Endy T.P., Raengsakulrach B., Rothman A.L., Ennis F.A., Nisalak A. (2000) Dengue viremia titer, antibody response pattern, and virus serotype correlate with disease severity. J Infect Dis 181: 2-9.
44. Fox J.P., Penna H.A. (1943) Behavior of 17D yellow fever virus in rhesus monkeys. Relation to substrain, dose and neural or extraneural inoculation. Am J Hyg 38: 152-72.
45. Guirakhoo F., Pugachev K., Zhang Z., Myers G., Levenbook I., Draper K., Lang J., Ocran F., Mitchell S., Parsons M., Brown N., Brandler S., Fournier C., Barrere B., Rizvi F., Travassos A., Nichols R., Trent D., Monath T. (2004) Safety and efficacy of chimeric yellow fever-dengue virus tetravalent vaccine formulations in nonhuman primates. J Virol 78: 4761-75.
46. Monath T.P., McCarthy K., Bedford P., Johnson C.T., Nichols R., Yoksan S., Marchesani R., Knauber M.,Wells K.H., Arroyo J., Guirakhoo F. (2002) Clinical proof of principle for ChimeriVaxTM: recombinant live, attenuated vaccines against flavivirus infections. Vaccine 20: 1004-18.
47. Blaney J.E. Jr., Matro J.M., Murphy B.R.,Whitehead S.S. (2005) 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 79: 5516-28.
48. Markoff L., Pang X., HoungH., Falgout B., Olsen R., Jones E., Polo S. (2002) Derivation and characterization of a dengue type 1 host range-restricted mutant virus that is attenuated and highly immunogenic in monkeys. J Virol 76: 3318-28.
49. Coe C.L., Savage A., Bromley L.J. (1992) Phylogenetic influences on hormone levels across the primate order. Am J Primatol 28: 81-100.
50. Higley J.D., King S.T. Jr., Hasert M.F., Champoux M., Suomi S.J., Linnoila M. (1996) Stability of interindividual differences in serotonin function and its relationship to severe aggression and competent social behavior in rhesus macaque females. Neuropsychopharmacology 14: 67-76.
51. Page S.L., Goodman M. (2001) Catarrhine phylogeny: noncoding DNA evidence for a diphyletic origin of the mangabeys and for a human-chimpanzee clade. Mol Phylogenet Evol 18: 14-25.
52. Raaum R.L., Sterner K.N., Noviello C.M., Stewart C.B., Disotell T.R. (2005) Catarrhine primate divergence dates estimated from complete mitochondrial genomes: concordance with fossil and nuclear DNA evidence. J Hum Evol 48: 237-57.
53. Baulu J., Evans G., Sutton C. (2002) Pathogenic agents found in Barbados Chlorocebus aethiops sabaeus and in Old WorldMonkeys commonly used in biomedical research. Lab Primate News 41: 4-6.
54. McGuire M.T. (1974) The St. Kitts vervet (Cercopithecus aethiops). J Med Primatol 3: 285-97.
55. Mutani A., Rhynd K., Brown G. (2003) A preliminary investigation on the gastrointestinal helminths of the Barbados green monkey, Cercopithecus aethiops sabaeus. Rev Inst Med Trop Sao Paulo 45: 193-95.