Virologica Sinica

, Volume 32, Issue 6, pp 441–453 | Cite as

Recent progress on chikungunya virus research

  • Wenxi An
  • Ningning Ge
  • Yilin Cao
  • Jin Sun
  • Xia Jin
Open Access


Chikungunya virus (CHIKV) is an arbovirus transmitted by Aedes mosquitos in tropical and subtropical regions across the world. After decades of sporadic outbreaks, it re-emerged in Africa, Asia, India Ocean and America suddenly, causing major regional epidemics recently and becoming a notable global health problem. Infection by CHIKV results in a spectrum of clinical diseases including an acute self-limiting febrile illness in most individuals, a chronic phase of recurrent join pain in a proportion of patients, and long-term arthralgia for months to years for the unfortunate few. No specific anti-viral drugs or licensed vaccines for CHIKV are available so far. A better understanding of virus-host interactions is essential for the development of therapeutics and vaccines. To this end, we reviewed the existing knowledge on CHIKV’s epidemiology, clinical presentation, molecular virology, diagnostic approaches, host immune response, vaccine development, and available animal models. Such a comprehensive overview, we believe, will shed lights on the promises and challenges in CHIKV vaccine development.


chikungunya virus (CHIKV) epidemiology molecular virology host immune response vaccine development 



We thank Dr. Chao Zhang (Zerun Biotech Co., Ltd., China) for his help in editing the global heat map of accumulative CHIKV cases. This work is supported in part by the National Key Program Project Grant from MOST #2016YFC1201000.


  1. Aggarwal M, Sharma R, Kumar P, Parida M, Tomar S. 2015. Kinetic characterization of trans-proteolytic activity of Chikungunya virus capsid protease and development of a FRET-based HTS assay. Sci Rep, 5: 14753.CrossRefPubMedPubMedCentralGoogle Scholar
  2. Bernard E, Solignat M, Gay B, Chazal N, Higgs S, Devaux C, Briant L. 2010. Endocytosis of chikungunya virus into mammalian cells: role of clathrin and early endosomal compartments. PLoS One, 5: e11479.CrossRefPubMedPubMedCentralGoogle Scholar
  3. Borgherini G, Poubeau P, Jossaume A, Gouix A, Cotte L, Michault A, Arvin-Berod C, Paganin F. 2008. Persistent arthralgia associated with chikungunya virus: a study of 88 adult patients on reunion island. Clin Infect Dis, 47: 469–475.CrossRefPubMedGoogle Scholar
  4. Brandler S, Ruffie C, Combredet C, Brault JB, Najburg V, Prevost MC, Habel A, Tauber E, Despres P, Tangy F. 2013. A recombinant measles vaccine expressing chikungunya virus-like particles is strongly immunogenic and protects mice from lethal challenge with chikungunya virus. Vaccine, 31: 3718–3725.CrossRefPubMedGoogle Scholar
  5. Brighton SW, Simson IW. 1984. A destructive arthropathy following Chikungunya virus arthritis-a possible association. Clin Rheumatol, 3: 253–258.CrossRefPubMedGoogle Scholar
  6. Brito CA, Sohsten AK, Leitao CC, Brito RC, Valadares LD, Fonte CA, Mesquita ZB, Cunha RV, Luz K, Leao HM, Brito CM, Frutuoso LC. 2016. Pharmacologic management of pain in patients with Chikungunya: a guideline. Rev Soc Bras Med Trop, 49: 668–679.CrossRefPubMedGoogle Scholar
  7. Broeckel R, Haese N, Messaoudi I, Streblow DN. 2015. Nonhuman Primate Models of Chikungunya Virus Infection and Disease (CHIKV NHP Model). Pathogens, 4: 662–681.CrossRefPubMedPubMedCentralGoogle Scholar
  8. US Centers for Disease Control and prevention (CDC). 2016. Chikungunya Virus. Available: Accessed 23 August 2017. 1571–1572.Google Scholar
  9. Cao-Lormeau VM, Musso D. 2014. Emerging arboviruses in the Pacific. Lancet, 384Google Scholar
  10. Cassadou S, Boucau S, Petit-Sinturel M, Huc P, Leparc-Goffart I, Ledrans M. 2014. Emergence of chikungunya fever on the French side of Saint Martin island, October to December 2013. Euro Surveill, 19. pii: 20752CrossRefPubMedGoogle Scholar
  11. Cecilia D, Kakade M, Alagarasu K, Patil J, Salunke A, Parashar D, Shah PS. 2015. Development of a multiplex real-time RTPCR assay for simultaneous detection of dengue and chikungunya viruses. Arch Virol, 160: 323–327.CrossRefPubMedGoogle Scholar
  12. Chang LJ, Dowd KA, Mendoza FH, Saunders JG, Sitar S, Plummer SH, Yamshchikov G, Sarwar UN, Hu Z, Enama ME, Bailer RT, Koup RA, Schwartz RM, Akahata W, Nabel GJ, Mascola JR, Pierson TC, Graham BS, Ledgerwood JE. 2014. Safety and tolerability of chikungunya virus-like particle vaccine in healthy adults: a phase 1 dose-escalation trial. The Lancet, 384: 2046–2052.CrossRefGoogle Scholar
  13. Charrel RN, de Lamballerie X, Raoult D. 2007. Chikungunya outbreaks- the globalization of vectorborne diseases. N Engl J Med, 356: 769–771.CrossRefPubMedGoogle Scholar
  14. Couderc T, Chretien F, Schilte C, Disson O, Brigitte M, Guivel-Benhassine F, Touret Y, Barau G, Cayet N, Schuffenecker I, Despres P, Arenzana-Seisdedos F, Michault A, Albert ML, Lecuit M. 2008. A mouse model for Chikungunya: young age and inefficient type-I interferon signaling are risk factors for severe disease. PLoS Pathog, 4: e29.CrossRefPubMedPubMedCentralGoogle Scholar
  15. De Zure AD, Berkowitz NM, Graham BS, Ledgerwood JE. 2016. Whole-Inactivated and Virus-Like Particle Vaccine Strategies for Chikungunya Virus. J Infect Dis, 214: S497–S499.CrossRefGoogle Scholar
  16. Diallo D, Sall AA, Buenemann M, Chen R, Faye O, Diagne CT, Faye O, Ba Y, Dia I, Watts D, Weaver SC, Hanley KA, Diallo M. 2012. Landscape ecology of sylvatic chikungunya virus and mosquito vectors in southeastern Senegal. PLoS Negl Trop Dis, 6: e1649.CrossRefPubMedPubMedCentralGoogle Scholar
  17. Edelman R, Tacket CO, Wasserman SS, Bodison SA, Perry JG, Mangiafico JA. 2000. Phase II safety and immunogenicity study of live chikungunya virus vaccine TSI-GSD-218. Am J Trop Med Hyg, 62: 681–685.CrossRefPubMedGoogle Scholar
  18. Edwards CJ, Welch SR, Chamberlain J, Hewson R, Tolley H, Cane PA, Lloyd G. 2007. Molecular diagnosis and analysis of Chikungunya virus. J Clin Virol, 39: 271–275.CrossRefPubMedGoogle Scholar
  19. Erasmus JH, Needham J, Raychaudhuri S, Diamond MS, Beasley DW, Morkowski S, Salje H, Fernandez Salas I, Kim DY, Frolov I, Nasar F, Weaver SC. 2015. Utilization of an Eilat Virus- Based Chimera for Serological Detection of Chikungunya Infection. PLoS Negl Trop Dis, 9: e0004119.CrossRefPubMedPubMedCentralGoogle Scholar
  20. Erasmus JH, Rossi SL, Weaver SC. 2016. Development of Vaccines for Chikungunya Fever. J Infect Dis, 214: S488–S496.CrossRefPubMedPubMedCentralGoogle Scholar
  21. Forsell K, Suomalainen M, Garoff H. 1995. Structure-function relation of the NH2-terminal domain of the Semliki Forest virus capsid protein. J Virol, 69: 1556–1563.PubMedPubMedCentralGoogle Scholar
  22. Fourie ED, Morrison JG. 1979. Rheumatoid arthritic syndrome after chikungunya fever. S Afr Med J, 56: 130–132.PubMedGoogle Scholar
  23. Gardner J, Anraku I, Le TT, Larcher T, Major L, Roques P, Schroder WA, Higgs S, Suhrbier A. 2010. Chikungunya virus arthritis in adult wild-type mice. J Virol, 84: 8021–8032.CrossRefPubMedPubMedCentralGoogle Scholar
  24. Gibbons DL, Vaney MC, Roussel A, Vigouroux A, Reilly B, Lepault J, Kielian M, Rey FIA. 2004. Conformational change and protein-protein interactions of the fusion protein of Semliki Forest virus. Nature, 427: 320–325.CrossRefPubMedGoogle Scholar
  25. Goo L, Dowd KA, Lin TY, Mascola JR, Graham BS, Ledgerwood JE, Pierson TC. 2016. A Virus-Like Particle Vaccine Elicits Broad Neutralizing Antibody Responses in Humans to All Chikungunya Virus Genotypes. J Infect Dis, 214: 1487–1491.CrossRefPubMedPubMedCentralGoogle Scholar
  26. Gorchakov R, Wang E, Leal G, Forrester NL, Plante K, Rossi SL, Partidos CD, Adams AP, Seymour RL, Weger J, Borland EM, Sherman MB, Powers AM, Osorio JE, Weaver SC. 2012. Attenuation of Chikungunya virus vaccine strain 181/clone 25 is determined by two amino acid substitutions in the E2 envelope glycoprotein. J Virol, 86: 6084–6096.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Goupil BA, McNulty MA, Martin MJ, McCracken MK, Christofferson RC, Mores CN. 2016. Novel Lesions of Bones and Joints Associated with Chikungunya Virus Infection in Two Mouse Models of Disease: New Insights into Disease Pathogenesis. PLoS One, 11: e0155243.CrossRefPubMedPubMedCentralGoogle Scholar
  28. Grandadam M, Caro V, Plumet S, Thiberge JM, Souares Y, Failloux AB, Tolou HJ, Budelot M, Cosserat D, Leparc-Goffart I, Despres P. 2011. Chikungunya virus, southeastern France. Emerg Infect Dis, 17: 910–913.CrossRefPubMedPubMedCentralGoogle Scholar
  29. Gratz NG. 2004. Critical review of the vector status of Aedes albopictus. Med Vet Entomol, 18: 215–227.CrossRefPubMedGoogle Scholar
  30. Guo R, Peng Z, Song T, He J, Zhong H, Li L, Liang W. 2014. Current infection status and epidemic risk analysis of Dengue fever and Chikungunya in Guangdong province, from 1990 to 2012. Chin J Epidemiol, 35: 167–169. (In Chinese)Google Scholar
  31. Guzman MG, Harris E. 2015. Dengue. Lancet, 385: 453–465.CrossRefPubMedGoogle Scholar
  32. Hallengard D, Kakoulidou M, Lulla A, Kummerer BM, Johansson DX, Mutso M, Lulla V, Fazakerley JK, Roques P, Le Grand R, Merits A, Liljestrom P. 2014. Novel attenuated Chikungunya vaccine candidates elicit protective immunity in C57BL/6 mice. J Virol, 88: 2858–2866.CrossRefPubMedPubMedCentralGoogle Scholar
  33. Hawman DW, Fox JM, Ashbrook AW, May NA, Schroeder KM, Torres RM, Crowe JE, Jr., Dermody TS, Diamond MS, Morrison TE 2016. Pathogenic Chikungunya Virus Evades B Cell Responses to Establish Persistence. Cell Rep, 16: 1326–1338.CrossRefPubMedPubMedCentralGoogle Scholar
  34. Hawman DW, Stoermer KA, Montgomery SA, Pal P, Oko L, Diamond MS, Morrison TE. 2013. Chronic joint disease caused by persistent Chikungunya virus infection is controlled by the adaptive immune response. J Virol, 87: 13878–13888.CrossRefPubMedPubMedCentralGoogle Scholar
  35. Her Z, Malleret B, Chan M, Ong EK, Wong SC, Kwek DJ, Tolou H, Lin RT, Tambyah PA, Renia L, Ng LF. 2010. Active infection of human blood monocytes by Chikungunya virus triggers an innate immune response. J Immunol, 184: 5903–5913.CrossRefPubMedGoogle Scholar
  36. Hoornweg TE, van Duijl-Richter MK, Ayala Nunez NV, Albulescu IC, van Hemert MJ, Smit JM. 2016. Dynamics of Chikungunya Virus Cell Entry Unraveled by Single-Virus Tracking in Living Cells. J Virol, 90: 4745–4756.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Huits R, Okabayashi T, Cnops L, Barbe B, Van Den Berg R, Bartholomeeusen K, Arien KK, Jacobs J, Bottieau E, Nakayama EE, Shioda T, Van Esbroeck M. 2017. Diagnostic accuracy of a rapid E1-antigen test for chikungunya virus infection in a reference setting. Clin Microbiol Infect. doi: 10.1016/j.cmi.2017.06.004Google Scholar
  38. Hussain KM, Lee RC, Ng MM, Chu JJ. 2016. Establishment of a Novel Primary Human Skeletal Myoblast Cellular Model for Chikungunya Virus Infection and Pathogenesis. Sci Rep, 6: 21406.CrossRefPubMedPubMedCentralGoogle Scholar
  39. Johnson BW, Goodman CH, Holloway K, de Salazar PM, Valadere AM, Drebot MA. 2016a. Evaluation of Commercially Available Chikungunya Virus Immunoglobulin M Detection Assays. Am J Trop Med Hyg, 95: 182–192.CrossRefPubMedPubMedCentralGoogle Scholar
  40. Johnson BW, Russell BJ, Goodman CH. 2016b. Laboratory Diagnosis of Chikungunya Virus Infections and Commercial Sources for Diagnostic Assays. J Infect Dis, 214: S471–S474.CrossRefPubMedPubMedCentralGoogle Scholar
  41. Jonathan J, Lindsey E, Jun P. 2017. Therapy with CTLA4-Ig and an antiviral monoclonal antibody controls chikungunya virus arthritis. Sci Transl Med.Google Scholar
  42. Josseran L, Paquet C, Zehgnoun A, Caillere N, Le Tertre A, Solet JL, Ledrans M. 2006. Chikungunya disease outbreak, Reunion Island. Emerg Infect Dis, 12: 1994–1995.CrossRefPubMedPubMedCentralGoogle Scholar
  43. Kam YW, Simarmata D, Chow A, Her Z, Teng TS, Ong EK, Renia L, Leo YS, Ng LF. 2012. Early appearance of neutralizing immunoglobulin G3 antibodies is associated with chikungunya virus clearance and long-term clinical protection. J Infect Dis, 205: 1147–1154.CrossRefPubMedPubMedCentralGoogle Scholar
  44. Kashyap RS, Morey SH, Ramteke SS, Chandak NH, Parida M, Deshpande PS, Purohit HJ, Taori GM, Daginawala HF. 2010. Diagnosis of Chikungunya fever in an Indian population by an indirect enzyme-linked immunosorbent assay protocol based on an antigen detection assay: a prospective cohort study. Clin Vaccine Immunol, 17: 291–297.CrossRefPubMedGoogle Scholar
  45. Khan AH, Morita K, Parquet MD, Mdel C, Hasebe F, Mathenge EG, Igarashi A. 2002. Complete nucleotide sequence of chikungunya virus and evidence for an internal polyadenylation site. J GenVirol: 3075–3084.Google Scholar
  46. Khan M, Dhanwani R, Kumar JS, Rao PV, Parida M. 2014. Comparative evaluation of the diagnostic potential of recombinant envelope proteins and native cell culture purified viral antigens of Chikungunya virus. J Med Virol, 86: 1169–1175.CrossRefPubMedGoogle Scholar
  47. Khan M, Dhanwani R, Rao PV, Parida M. 2012. Subunit vaccine formulations based on recombinant envelope proteins of Chikungunya virus elicit balanced Th1/Th2 response and virusneutralizing antibodies in mice. Virus Res, 167: 236–246.CrossRefPubMedGoogle Scholar
  48. Klimstra WB, Nangle EM, Smith MS, Yurochko AD, Ryman KD. 2003. DC-SIGN and L-SIGN Can Act as Attachment Receptors for Alphaviruses and Distinguish between Mosquito Cell- and Mammalian Cell-Derived Viruses. Journal of Virology, 77: 12022–12032.CrossRefPubMedPubMedCentralGoogle Scholar
  49. Labadie K, Larcher T, Joubert C, Mannioui A, Delache B, Brochard P, Guigand L, Dubreil L, Lebon P, Verrier B, de Lamballerie X, Suhrbier A, Cherel Y, Le Grand R, Roques P. 2010. Chikungunya disease in nonhuman primates involves long-term viral persistence in macrophages. J Clin Invest, 120: 894–906.CrossRefPubMedPubMedCentralGoogle Scholar
  50. Lee WW, Teo TH, Her Z, Lum FM, Kam YW, Haase D, Renia L, Rotzschke O, Ng LF. 2015. Expanding regulatory T cells alleviates chikungunya virus-induced pathology in mice. J Virol. pii: JVI.00998-15Google Scholar
  51. Lum FM, Teo TH, Lee WW, Kam YW, Renia L, Ng LF. 2013. An essential role of antibodies in the control of Chikungunya virus infection. J Immunol, 190: 6295–6302.CrossRefPubMedPubMedCentralGoogle Scholar
  52. Marti-Carvajal A, Ramon-Pardo P, Javelle E, Simon F, Aldighieri S, Horvath H, Rodriguez-Abreu J, Reveiz L. 2017. Interventions for treating patients with chikungunya virus infection-related rheumatic and musculoskeletal disorders: A systematic review. PLoS One, 12: e0179028.CrossRefPubMedPubMedCentralGoogle Scholar
  53. Messaoudi I, Vomaske J, Totonchy T, Kreklywich CN, Haberthur K, Springgay L, Brien JD, Diamond MS, Defilippis VR, Streblow DN. 2013. Chikungunya virus infection results in higher and persistent viral replication in aged rhesus macaques due to defects in anti-viral immunity. PLoS Negl Trop Dis, 7: e2343.CrossRefPubMedPubMedCentralGoogle Scholar
  54. Metz SW, Martina BE, van den Doel P, Geertsema C, Osterhaus AD, Vlak JM, Pijlman GP. 2013. Chikungunya virus-like particles are more immunogenic in a lethal AG129 mouse model compared to glycoprotein E1 or E2 subunits. Vaccine, 31: 6092–6096.CrossRefPubMedGoogle Scholar
  55. Miner JJ, Diamond MS. 2017. Zika Virus Pathogenesis and Tissue Tropism. Cell Host Microbe, 21: 134–142.CrossRefPubMedGoogle Scholar
  56. Okabayashi T, Sasaki T, Masrinoul P, Chantawat N, Yoksan S, Nitatpattana N, Chusri S, Morales Vargas RE, Grandadam M, Brey PT, Soegijanto S, Mulyantno KC, Churrotin S, Kotaki T, Faye O, Faye O, Sow A, Sall AA, Puiprom O, Chaichana P, Kurosu T, Kato S, Kosaka M, Ramasoota P, Ikuta K. 2015. Detection of chikungunya virus antigen by a novel rapid immunochromatographic test. J Clin Microbiol, 53: 382–388.CrossRefPubMedPubMedCentralGoogle Scholar
  57. Pan American Health Organization (PAHO). 2017, Geographic Spread of Chikungunya in the Americas 2013–2017. Available: Accessed 23 August 2017.Google Scholar
  58. Panning M, Grywna K, van Esbroeck M, Emmerich P, Drosten C. 2008. Chikungunya fever in travelers returning to Europe from the Indian Ocean region, 2006. Emerg Infect Dis, 14: 416–422.CrossRefPubMedPubMedCentralGoogle Scholar
  59. Parola P, de Lamballerie X, Jourdan J, Rovery C, Vaillant V, Minodier P, Brouqui P, Flahault A, Raoult D, Charrel RN. 2006. Novel chikungunya virus variant in travelers returning from Indian Ocean islands. Emerg Infect Dis, 12: 1493–1499.CrossRefPubMedPubMedCentralGoogle Scholar
  60. Prince HE, Seaton BL, Matud JL, Batterman HJ. 2015. Chikungunya virus RNA and antibody testing at a National Reference Laboratory since the emergence of Chikungunya virus in the Americas. Clin Vaccine Immunol, 22: 291–297.CrossRefPubMedPubMedCentralGoogle Scholar
  61. Ramachandran V, Kaur P, Kanagasabai K, Vadivoo S, Murhekar MV. 2014. Persistent arthralgia among Chikungunya patients and associated risk factors in Chennai, South India. J Postgrad Med, 60: 3–6.CrossRefPubMedGoogle Scholar
  62. Ramsauer K, Schwameis M, Firbas C, Müllner M, Putnak RJ, Thomas SJ, Desprès P, Tauber E, Jilma B, Tangy F. 2015. Immunogenicity, safety, and tolerability of a recombinant measlesvirus- based chikungunya vaccine: a randomised, double-blind, placebo-controlled, active-comparator, first-in-man trial. The Lancet Infectious Diseases, 15: 519–527.CrossRefPubMedGoogle Scholar
  63. Reddy V, Ravi V, Desai A, Parida M, Powers AM, Johnson BW. 2012. Utility of IgM ELISA, TaqMan real-time PCR, reverse transcription PCR, and RT-LAMP assay for the diagnosis of Chikungunya fever. J Med Virol, 84: 1771–1778.CrossRefPubMedGoogle Scholar
  64. Renault P, Josseran L, Pierre V. 2008. Chikungunya-related fatality rates, Mauritius, India, and Reunion Island. Emerg Infect Dis, 14: 1327.CrossRefPubMedPubMedCentralGoogle Scholar
  65. Rezza G, Nicoletti L, Angelini R, Romi R, Finarelli AC, Panning M, Cordioli P, Fortuna C, Boros S, Magurano F, Silvi G, Angelini P, Dottori M, Ciufolini MG, Majori GC, Cassone A, group Cs. 2007. Infection with chikungunya virus in Italy: an outbreak in a temperate region. Lancet, 370: 1840–1846.CrossRefPubMedGoogle Scholar
  66. Robinson MC. 1955. An epidemic of virus disease in Southern Province, Tanganyika Territory, in 1952-53. I. Clinical features. Trans R Soc Trop Med Hyg, 49: 28–32.CrossRefPubMedGoogle Scholar
  67. Roy CJ, Adams AP, Wang E, Plante K, Gorchakov R, Seymour RL, Vinet-Oliphant H, Weaver SC. 2014. Chikungunya vaccine candidate is highly attenuated and protects nonhuman primates against telemetrically monitored disease following a single dose. J Infect Dis, 209: 1891–1899.CrossRefPubMedPubMedCentralGoogle Scholar
  68. Rudd PA, Wilson J, Gardner J, Larcher T, Babarit C, Le TT, Anraku I, Kumagai Y, Loo YM, Gale M, Jr., Akira S, Khromykh AA, Suhrbier A 2012. Interferon response factors 3 and 7 protect against Chikungunya virus hemorrhagic fever and shock. J Virol, 86: 9888–9898.CrossRefPubMedPubMedCentralGoogle Scholar
  69. Schilte C, Staikowsky F, Couderc T, Madec Y, Carpentier F, Kassab S, Albert ML, Lecuit M, Michault A. 2013. Chikungunya virus-associated long-term arthralgia: a 36-month prospective longitudinal study. PLoS Negl Trop Dis, 7: e2137.CrossRefPubMedPubMedCentralGoogle Scholar
  70. Schwameis M, Buchtele N, Wadowski PP, Schoergenhofer C, Jilma B. 2016. Chikungunya vaccines in development. Hum Vaccin Immunother, 12: 716–731.CrossRefPubMedGoogle Scholar
  71. Schwartz O, Albert ML. 2010. Biology and pathogenesis of chikungunya virus. Nat Rev Microbiol, 8: 491–500.CrossRefPubMedGoogle Scholar
  72. Shukla J, Khan M, Tiwari M, Sannarangaiah S, Sharma S, Rao PV, Parida M. 2009. Development and evaluation of antigen capture ELISA for early clinical diagnosis of chikungunya. Diagn Microbiol Infect Dis, 65: 142–149.CrossRefPubMedGoogle Scholar
  73. Silva LA, Dermody TS. 2017. Chikungunya virus: epidemiology, replication, disease mechanisms, and prospective intervention strategies. J Clin Invest, 127: 737–749.CrossRefPubMedGoogle Scholar
  74. Simon F, Javelle E, Cabie A, Bouquillard E, Troisgros O, Gentile G, Leparc-Goffart I, Hoen B, Gandjbakhch F, Rene-Corail P, Franco JM, Caumes E, Combe B, Poiraudeau S, Gane-Troplent F, Djossou F, Schaerverbeke T, Criquet-Hayot A, Carrere P, Malvy D, Gaillard P, Wendling D, Societe de pathologie infectieuse de langue f. 2015. French guidelines for the management of chikungunya (acute and persistent presentations). November 2014. Med Mal Infect, 45: 243–263.CrossRefPubMedGoogle Scholar
  75. Simon F, Javelle E, Oliver M, Leparc-Goffart I, Marimoutou C. 2011. Chikungunya virus infection. Curr Infect Dis Rep, 13: 218–228.CrossRefPubMedPubMedCentralGoogle Scholar
  76. Singh I, Helenius A. 1992. Role of ribosomes in Semliki Forest virus nucleocapsid uncoating. J Virol, 66: 7049–7058.PubMedPubMedCentralGoogle Scholar
  77. Smith TJ, Cheng RH, Olson NH, Peterson P, Chase E, Kuhn RJ, Baker TS. 1995. Putative receptor binding sites on alphaviruses as visualized by cryoelectron microscopy. Immunology: 10648–10652.Google Scholar
  78. Snyder AJ, Mukhopadhyay S. 2012. The alphavirus E3 glycoprotein functions in a clade-specific manner. J Virol, 86: 13609–13620.CrossRefPubMedPubMedCentralGoogle Scholar
  79. Snyder JE, Kulcsar KA, Schultz KL, Riley CP, Neary JT, Marr S, Jose J, Griffin DE, Kuhn RJ. 2013. Functional characterization of the alphavirus TF protein. J Virol, 87: 8511–8523.CrossRefPubMedPubMedCentralGoogle Scholar
  80. Solignat M, Gay B, Higgs S, Briant L, Devaux C. 2009. Replication cycle of chikungunya: a re-emerging arbovirus. Virology, 393: 183–197.CrossRefPubMedPubMedCentralGoogle Scholar
  81. Sourisseau M, Schilte C, Casartelli N, Trouillet C, Guivel-Benhassine F, Rudnicka D, Sol-Foulon N, et al. 2007. Characterization of Reemerging Chikungunya Virus. PLoS Pathog, 3: e89.CrossRefPubMedPubMedCentralGoogle Scholar
  82. Staples JE, Breiman RF, Powers AM. 2009. Chikungunya fever: an epidemiological review of a re-emerging infectious disease. Clin Infect Dis, 49: 942–948.CrossRefPubMedGoogle Scholar
  83. Strauss JH, Strauss EG. 1994. The alphaviruses: gene expression, replication, and evolution. Microbiol Rev, 58: 491–562.PubMedPubMedCentralGoogle Scholar
  84. Suhrbier A, Jaffar-Bandjee MC, Gasque P. 2012. Arthritogenic alphaviruses-an overview. Nat Rev Rheumatol, 8: 420–429.CrossRefPubMedGoogle Scholar
  85. Teo TH, Lum FM, Claser C, Lulla V, Lulla A, Merits A, Renia L, Ng LF. 2013. A pathogenic role for CD4+ T cells during Chikungunya virus infection in mice. J Immunol, 190: 259–269.CrossRefPubMedGoogle Scholar
  86. Townson H, Nathan MB. 2008. Resurgence of chikungunya. Trans R Soc Trop Med Hyg, 102: 308–309.CrossRefPubMedGoogle Scholar
  87. Tretyakova I, Hearn J, Wang E, Weaver S, Pushko P. 2014. DNA vaccine initiates replication of live attenuated chikungunya virus in vitro and elicits protective immune response in mice. J Infect Dis, 209: 1882–1890.CrossRefPubMedPubMedCentralGoogle Scholar
  88. Villamil-Gomez WE, Gonzalez-Camargo O, Rodriguez-Ayubi J, Zapata-Serpa D, Rodriguez-Morales AJ. 2016. Dengue, chikungunya and Zika co-infection in a patient from Colombia. J Infect Public Health, 9: 684–686.CrossRefPubMedGoogle Scholar
  89. Volk SM, Chen R, Tsetsarkin KA, Adams AP, Garcia TI, Sall AA, Nasar F, Schuh AJ, Holmes EC, Higgs S, Maharaj PD, Brault AC, Weaver SC. 2010. Genome-scale phylogenetic analyses of chikungunya virus reveal independent emergences of recent epidemics and various evolutionary rates. J Virol, 84: 6497–6504.CrossRefPubMedPubMedCentralGoogle Scholar
  90. Voss JE, Vaney MC, Duquerroy S, Vonrhein C, Girard-Blanc C, Crublet E, Thompson A, Bricogne G, Rey FA. 2010. Glycoprotein organization of Chikungunya virus particles revealed by Xray crystallography. Nature, 468: 709–712.CrossRefPubMedGoogle Scholar
  91. World Health Organization (WHO). 2017, Chikungunya. Available: Accessed 23 August 2017.Google Scholar
  92. World Health Organization (WHO). 2006. Outbreak news. Chikungunya and dengue, south-west Indian Ocean. Wkly Epidemiol Rec, 81: 106–108.Google Scholar
  93. Wahid B, Ali A, Rafique S, Idrees M. 2017. Global expansion of chikungunya virus: mapping the 64-year history. Int J Infect Dis, 58: 69–76.CrossRefPubMedGoogle Scholar
  94. Wauquier N, Becquart P, Nkoghe D, Padilla C, Ndjoyi-Mbiguino A, Leroy EM. 2011. The acute phase of Chikungunya virus infection in humans is associated with strong innate immunity and T CD8 cell activation. J Infect Dis, 204: 115–123.CrossRefPubMedGoogle Scholar
  95. Weber C, Berberich E, von Rhein C, Henss L, Hildt E, Schnierle BS. 2017. Identification of Functional Determinants in the Chikungunya Virus E2 Protein. PLoS Negl Trop Dis, 11: e0005318.CrossRefPubMedPubMedCentralGoogle Scholar
  96. Weger-Lucarelli J, Aliota MT, Wlodarchak N, Kamlangdee A, Swanson R, Osorio JE. 2015. Dissecting the Role of E2 Protein Domains in Alphavirus Pathogenicity. J Virol, 90: 2418–2433.CrossRefPubMedGoogle Scholar
  97. Weiss B, Nitschko H, Ghattas I, Wright R, Schlesinger S. 1989. Evidence for specificity in the encapsidation of Sindbis virus RNAs. J Virol, 63: 5310–5318.PubMedPubMedCentralGoogle Scholar
  98. Wintachai P, Wikan N, Kuadkitkan A, Jaimipuk T, Ubol S, Pulmanausahakul R, Auewarakul P, Kasinrerk W, Weng WY, Panyasrivanit M, Paemanee A, Kittisenachai S, Roytrakul S, Smith DR. 2012. Identification of prohibitin as a Chikungunya virus receptor protein. J Med Virol, 84: 1757–1770.CrossRefPubMedGoogle Scholar
  99. Zeller H, Van Bortel W, Sudre B. 2016. Chikungunya: Its History in Africa and Asia and Its Spread to New Regions in 2013-2014. J Infect Dis, 214: S436–S440.CrossRefPubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Viral Disease and Vaccine Translational Research Unit, CAS Key Laboratory of Molecular Virology and Immunology, Institut Pasteur of ShanghaiChinese Academy of SciencesShanghaiChina
  2. 2.Department of Biochemistry and Molecular BiologyPennsylvania State UniversityState CollegeUSA
  3. 3.College of Pharmaceutical SciencesJilin UniversityChangchunChina

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