Chikungunya disease in nonhuman primates involves long-term viral persistence in macrophages

Journal of Clinical Investigation

Volumn 120, Issue 3, 2010, Pages 894-906

  Labadie, Karine ^a,b   Larcher, Thibaut ^c   Joubert, Christophe ^a,b   Mannioui, Abdelkrim ^a,b   Delache, Benoit ^a,b   Brochard, Patricia ^a,b   Guigand, Lydie ^c   Dubreil, Laurence ^c   Lebon, Pierre ^d   Verrier, Bernard ^e   De Lamballerie, Xavier ^f,g   Suhrbier, Andreas ^h   Cherel, Yan ^c   Grand, Roger Le ^a,b   Roques, Pierre ^a,b  

^a CEA   (France)

^b UMR E1   (France)

^c INRA UMR 703   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

^e University Lyon i   (France)

^f AIX MARSEILLE UNIVERSITY   (France)

^g INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

^h QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE AMINOTRANSFERASE; ALPHA INTERFERON; ASPARTATE AMINOTRANSFERASE; BETA INTERFERON; CARBON TETRACHLORIDE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12P40; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 6; INTERLEUKIN 8; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; TUMOR NECROSIS FACTOR ALPHA; VIRUS RNA;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTHRALGIA; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; BIOASSAY; BLOOD LEVEL; CELL INFILTRATION; CHIKUNGUNYA ALPHAVIRUS; CLINICAL ASSESSMENT; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DEATH; DENDRITIC CELL; DISEASE MODEL; EDEMA; ENDOTHELIUM CELL; FEVER; GINGIVA BLEEDING; GRANULOCYTOSIS; HEADACHE; INOCULATION; JOINT; JOINT EFFUSION; LIVER; LYMPHOCYTOPENIA; LYMPHOID ORGAN; MACACA; MACROPHAGE; MENINGOENCEPHALITIS; MONOCYTOPENIA; MONONUCLEAR CELL; MUSCLE; MUSCLE NECROSIS; MYALGIA; NONHUMAN; PATHOGENESIS; PERSISTENT VIRUS INFECTION; PRIMATE; PRIORITY JOURNAL; RASH; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; THROMBOCYTOPENIA; VIREMIA; VIROGENESIS; VIRUS DETECTION; VIRUS LOAD; VIRUS STRAIN;

ALPHAVIRUS INFECTIONS; ANIMALS; CHIKUNGUNYA VIRUS; DISEASE MODELS, ANIMAL; HUMANS; JOINTS; LIVER; LYMPHOID TISSUE; MACACA FASCICULARIS; MACROPHAGES; MICE; MUSCLES;

EID: 77949752839     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI40104     Document Type: Article

References (73)

1. Mason PJ, Haddow AJ. An epidemic of virus disease in Southern Province, Tanganyika Territory, in 1952-53; an additional note on Chikungunya virus isolations and serum antibodies. Trans R Soc Trop Med Hyg. 1957;51(3):238-240.
2. Brighton SW, Prozesky OW, de la Harpe AL. Chikungunya virus infection. A retrospective study of 107 cases. S Afr Med J. 1983;63(9):313-315.
3. McGill PE. Viral infections: alpha-viral arthropathy. Baillieres Clin Rheumatol. 1995;9(1):145-150.
4. Powers AM, Logue CH. Changing patterns of chikungunya virus: re-emergence of a zoonotic arbovirus. J Gen Virol. 2007;88(Pt 9):2363-2377.
5. Mavalankar D, Shastri P, Raman P. Chikungunya epidemic in India: a major public-health disaster. Lancet Infect Dis. 2007;7(5):306-307.
6. Pastorino B, et al. Epidemic resurgence of Chikungunya virus in democratic Republic of the Congo: identification of a new central African strain. J Med Virol. 2004;74(2):277-282.
7. Peyrefitte CN, et al. Chikungunya virus, Cameroon, 2006. Emerg Infect Dis. 2007;13(5):768-771.
8. Saxena SK, Singh M, Mishra N, Lakshmi V. Resurgence of chikungunya virus in India: an emerging threat. Euro Surveill. 2006;11(8):E060810.2.
9. Yergolkar PN, et al. Chikungunya outbreaks caused by African genotype, India. Emerg Infect Dis. 2006; 12(10):1580-1583.
10. Gerardin P, et al. Estimating Chikungunya prevalence in La Reunion Island outbreak by serosurveys: two methods for two critical times of the epidemic. BMC Infect Dis. 2008;8:99.
11. Sissoko D, et al. Seroprevalence and risk factors of chikungunya virus infection in Mayotte, Indian Ocean, 2005-2006: a population-based survey. PLoS ONE. 2008;3(8):e3066.
12. Renault P, et al. A major epidemic of chikungunya virus infection on Reunion Island, France, 2005-2006. Am J Trop Med Hyg. 2007;77(4):727-731.
13. Economopoulou A, et al. Atypical Chikungunya virus infections: clinical manifestations, mortality and risk factors for severe disease during the 2005-2006 outbreak on Reunion. Epidemiol Infect. 2009;137(4):534-541.
14. Dominguez M, and Economopoulou A. Active surveillance system for hospitalized atypical forms of chikungunya fever, Reunion Island, March 2005-April 2006. Saint-Maurice: Institut de Veille Sanitaire. http://www.invs.sante.fr/publications/2007/ chik-surveillance-2007/. Published online August 2, 2007. Accessed January 8, 2010.
15. Borgherini G, et al. Persistent arthralgia associated with chikungunya virus: a study of 88 adult patients on Reunion Island. Clin Infect Dis. 2008; 47(4):469-475.
16. Queyriaux B, Simon F, Grandadam M, Michel R, Tolou H, Boutin JP. Clinical burden of Chikungunya virus infection. Lancet Infect Dis. 2008;8(1):2-3.
17. Simon F, et al. Chikungunya infection: an emerging rheumatism among travelers returned from Indian Ocean islands. Report of 47 cases. Medicine (Baltimore). 2007;86(1):123-137.
18. Couderc T, et al. A mouse model for Chikungunya: young age and inefficient type-I interferon signaling are risk factors for severe disease. PLoS Pathog. 2008; 4(2):e29.
19. Ziegler SA, Lu L, da Rosa AP, Xiao SY, Tesh RB. An animal model for studying the pathogenesis of Chikungunya virus infection. Am J Trop Med Hyg. 2008;79(1):133-139.
20. Reed DS, Lind CM, Lackemeyer MG, Sullivan LJ, Pratt WD, Parker MD. Genetically engineered, live, attenuated vaccines protect nonhuman primates against aerosol challenge with a virulent IE strain of Venezuelan equine encephalitis virus. Vaccine. 2005; 23(24):3139-3147.
21. Verrier B, et al. Evaluation in rhesus macaques of Tat and rev-targeted immunization as a preventive vaccine against mucosal challenge with SHIV-BX08. DNA Cell Biol. 2002;21(9):653-658.
22. Vierboom MP, Jonker M, Tak PP, Hart BA. Preclinical models of arthritic disease in non-human primates. Drug Discov Today. 2007;12(7-8):327-335.
23. Walsh GP, et al. The Philippine cynomolgus monkey (Macaca fasicularis) provides a new nonhuman primate model of tuberculosis that resembles human disease. Nat Med. 1996;2(4):430-436.
24. Binn LN, Harrison VR, Randall R. Patterns of viremia and antibody observed in rhesus monkeys inoculated with chikungunya and other serologically related group A arboviruses. Am J Trop Med Hyg. 1967;16(6):782-785.
25. Inoue S, et al. Distribution of three arbovirus antibodies among monkeys (Macaca fascicularis) in the Philippines. J Med Primatol. 2003;32(2):89-94.
26. Kaschula VR, Van Dellen AF, de Vos V. Some infectious diseases of wild vervet monkeys (Cercopithecus aethiops pygerythrus) in South Africa. J S Afr Vet Assoc. 1978;49(3):223-227.
27. Kirya BG, Okia NO. A yellow fever epizootic in Zika Forest, Uganda, during 1972: Part 2: Monkey serology. Trans R Soc Trop Med Hyg. 1977;71(4):300-303.
28. Marchette NJ, Rudnick A, Garcia R, MacVean DW. Alphaviruses in Peninusular Malaysia: I. Virus isolations and animal serology. Southeast Asian J Trop Med Public Health. 1978;9(3):317-329.
29. McCrae AW, Henderson BE, Kirya BG, Sempala SD. Chikungunya virus in the Entebbe area of Uganda: isolations and epidemiology. Trans R Soc Trop Med Hyg. 1971;65(2):152-168.
30. Peiris JS, Dittus WP, Ratnayake CB. Seroepidemiology of dengue and other arboviruses in a natural population of toque macaques (Macaca sinica) at Polonnaruwa, Sri Lanka. J Med Primatol. 1993; 22(4):240-245.
31. Levitt NH, Ramsburg HH, Hasty SE, Repik PM, Cole FE Jr, Lupton HW. Development of an attenuated strain of chikungunya virus for use in vaccine production. Vaccine. 1986;4(3):157-162.
32. Paul SD, Singh KR. Experimental infection of Macaca radiata with Chikungunya virus and transmission of virus by mosquitoes. Indian J Med Res. 1968;56(6):802-811.
33. Ozden S, et al. Human muscle satellite cells as targets of chikungunya virus infection. PLoS ONE. 2007; 2(6):e527.
34. Sourisseau M, et al. Characterization of reemerging chikungunya virus. PLoS Pathog. 2007;3(6):e89.
35. Parola P, et al. Novel chikungunya virus variant in travelers returning from Indian Ocean islands. Emerg Infect Dis. 2006;12(10):1493-1499.
36. Vazeille M, et al. Two chikungunya isolates from the outbreak of La Reunion (Indian Ocean) exhibit different patterns of infection in the mosquito, Aedes albopictus. PLoS ONE. 2007;2(11):e1168.
37. Gerardin P, et al. Multidisciplinary prospective study of mother-to-child chikungunya virus infections on the island of La Reunion. PLoS Med. 2008; 5(3):e60.
38. Laurent P, et al. Development of a sensitive realtime reverse transcriptase PCR assay with an internal control to detect and quantify chikungunya virus. Clin Chem. 2007;53(8):1408-1414.
39. Panning M, Grywna K, van Esbroeck M, Emmerich P, Drosten C. Chikungunya Fever in travelers returning to europe from the Indian ocean region, 2006. Emerg Infect Dis. 2008;14(3):416-422.
40. Borgherini G, et al. Outbreak of chikungunya on Reunion Island: early clinical and laboratory features in 157 adult patients. Clin Infect Dis. 2007; 44(11):1401-1407.
41. Pialoux G, Gauzere BA, Jaureguiberry S, Strobel M. Chikungunya, an epidemic arbovirosis. Lancet Infect Dis. 2007;7(5):319-327.
42. Ng LF, et al. IL-1beta, IL-6, and RANTES as biomarkers of Chikungunya severity. PLoS ONE. 2009; 4(1):e4261.
43. Tournebize P, Charlin C, Lagrange M. Neurological manifestations in Chikungunya: about 23 cases collected in Reunion Island [In French]. Rev Neurol (Paris). 2009;165(1):48-51.
44. Krakowka S, et al. Features of cell degeneration and death in hepatic failure and systemic lymphoid depletion characteristic of porcine circovirus-2-associated postweaning multisystemic wasting disease. Vet Pathol. 2004;41(5):471-481.
45. Ellis AE, et al. Pathology and epidemiology of natural West Nile viral infection of raptors in Georgia. J Wildl Dis. 2007;43(2):214-223.
46. Kage M, et al. Pathology of chronic hepatitis C in children. Child Liver Study Group of Japan. Hepatology. 1997;26(3):771-775.
47. Kobune M, Kohgo Y, Kato J, Miyazaki E, Niitsu Y. Interleukin-6 enhances hepatic transferrin uptake and ferritin expression in rats. Hepatology. 1994; 19(6):1468-1475.
48. Lidbury BA, Simeonovic C, Maxwell GE, Marshall ID, Hapel AJ. Macrophage-induced muscle pathology results in morbidity and mortality for Ross River virus-infected mice. J Infect Dis. 2000;181(1):27-34.
49. Soden M, et al. Detection of viral ribonucleic acid and histologic analysis of inflamed synovium in Ross River virus infection. Arthritis Rheum. 2000; 43(2):365-369.
50. Mogal A, Abdulkadir SA. Effects of histone deacetylase inhibitor (HDACi); trichostatin-A (TSA) on the expression of housekeeping genes. Mol Cell Probes. 2006;20(2):81-86.
51. Corssmit EP, et al. Effects of interferon-alpha (IFNalpha) administration on leucocytes in healthy humans. Clin Exp Immunol. 1997;107(2):359-363.
52. Tsou CL, et al. Critical roles for CCR2 and MCP-3 in monocyte mobilization from bone marrow and recruitment to inflammatory sites. J Clin Invest. 2007;117(4):902-909.
53. Jaffar-Bandjee MC, et al. Identification des cellules cibles et des mécanismes physiopathologiques du virus Chikungunya. In: Chikungunya et autres arboviroses émergentes en milieu tropical. Saint-Pierre, La Réunion; 2007. URL: http://www.invs.sante. fr/agenda/colloque- chikungunya/programme- chik-version-longue.pdf. Poster 111. Accessed 2 March 2009.
54. Jaffar-Bandjee MC, et al. Chikungunya virus takes centre stage in virally induced arthritis: possible cellular and molecular mechanisms to pathogenesis. Microbes Infect. 2009;11(14-15):1206-1208.
55. Ryman KD, Klimstra WB, Nguyen KB, Biron CA, Johnston RE. Alpha/beta interferon protects adult mice from fatal Sindbis virus infection and is an important determinant of cell and tissue tropism. J Virol. 2000;74(7):3366-3378.
56. Paessler S, et al. Inhibition of alphavirus infection in cell culture and in mice with antisense morpholino oligomers. Virology. 2008;376(2):357-370.
57. Journeaux SF, Brown WG, Aaskov JG. Prolonged infection of human synovial cells with Ross River virus. J Gen Virol. 1987;68(Pt 12):3165-3169.
58. Way SJ, Lidbury BA, Banyer JL. Persistent Ross River virus infection of murine macrophages: an in vitro model for the study of viral relapse and immune modulation during long-term infection. Virology. 2002;301(2):281-292.
59. Murphy FA, Taylor WP, Mims CA, Marshall ID. Pathogenesis of Ross River virus infection in mice. II. Muscle, heart, and brown fat lesions. J Infect Dis. 1973;127(2):129-138.
60. Suhrbier A, La Linn M. Clinical and pathologic aspects of arthritis due to Ross River virus and other alpha-viruses. Curr Opin Rheumatol. 2004;16(4):374-379.
61. Gardner JP, et al. Infection of human dendritic cells by a sindbis virus replicon vector is determined by a single amino acid substitution in the E2 glycoprotein. J Virol. 2000;74(24):11849-11857.
62. Nishimoto KP, et al. Restricted and selective tropism of a Venezuelan equine encephalitis virusderived replicon vector for human dendritic cells. Viral Immunol. 2007;20(1):88-104.
63. Shabman RS, et al. Differential induction of type I interferon responses in myeloid dendritic cells by mosquito and mammalian-cell-derived alphaviruses. J Virol. 2007;81(1):237-247.
64. Ackermann C, Kavanaugh A. Tumor necrosis factor as a therapeutic target of rheumatologic disease. Expert Opin Ther Targets. 2007;11(11):1369- 1384.
65. Suhrbier A, Mahalingam S. The immunobiology of viral arthritides. Pharmacol Ther. 2009; 124(3):301-308.
66. Hu LH, Chen FH, Li YR, Wang L. Real-time determination of human telomerase reverse transcriptase mRNA in gastric cancer. World J Gastroenterol. 2004; 10(23):3514-3517.
67. Giavedoni LD. Simultaneous detection of multiple cytokines and chemokines from nonhuman primates using luminex technology. J Immunol Methods. 2005;301(1-2):89-101.
68. Malleret B, et al. Primary infection with simian immunodeficiency virus: plasmacytoid dendritic cell homing to lymph nodes, type I interferon, and immune suppression. Blood. 2008;112(12):4598-4608.
69. Schuffenecker I, et al. Genome microevolution of chikungunya viruses causing the Indian Ocean outbreak. PLoS Med. 2006;3(7):e263.
70. Brehin AC, et al. Production and characterization of mouse monoclonal antibodies reactive to Chikungunya envelope E2 glycoprotein. Virology. 2008; 371(1):185-195.
71. Heise MT, et al. An attenuating mutation in nsP1 of the Sindbis-group virus S.A.AR86 accelerates nonstructural protein processing and up-regulates viral 26S RNA synthesis. J Virol. 2003;77(2):1149-1156.
72. Heise MT, Simpson DA, Johnston RE. Sindbisgroup alphavirus replication in periosteum and endosteum of long bones in adult mice. J Virol. 2000;74(19):9294-9299.
73. Morrison TE, et al. Characterization of Ross River virus tropism and virus-induced inflammation in a mouse model of viral arthritis and myositis. J Virol. 2006; 80(2):737-749.