Skip to main content

Advertisement

SpringerLink
Log in

Distribution and phylogenetic analysis of Culex flavivirus in mosquitoes in China

  • Original Article
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

Culex flavivirus (CxFV) is an insect-specific virus of the genus Flavivirus. CxFV strains have been isolated from Cx. pipiens, Cx. quinquefasciatus, and other Cx. species in Asia, Africa, North America, Central America and South America. CxFV was isolated for the first time in China in 2006. As this is a novel flavivirus, we explored the distribution and genetic characteristics of Culex flavivirus in China. A total of 46,649 mosquitoes were collected in seven provinces between 2004 and 2012 and were analysed in 871 pools. 29 CxFV RNAs from Cx. pipiens, Cx. tritaeniorhynchus, Anopheles Sinensis, and Culex spp. tested positive for CxFV in real-time RT-PCR. 6 CxFV strains were isolated from Cx. species collected in Shandong, Henan, and Shaanxi provinces, while no virus or viral RNA was detected in samples from Sichuan, Chongqing, Hubei, and Fujian. Phylogenetic analysis of the envelope gene indicated that Chinese strains formed a robust subgroup of genotype 1, together with viruses from the United States and Japan. This study demonstrates that the geographic distribution of CxFV in China is widespread, but geographical boundaries to spread are apparent. Our findings suggest that CxFV can infect various mosquito species in nature.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Kuno G, Chang GJ, Tsuchiya KR, Karabatsos N, Cropp CB (1998) Phylogeny of the genus Flavivirus. J Virol 72:73–83

    PubMed Central  CAS  PubMed  Google Scholar 

  2. Cook S, Holmes EC (2006) A multigene analysis of the phylogenetic relationships among the flaviviruses (Family: Flaviviridae) and the evolution of vector transmission. Arch Virol 151:309–325

    Article  CAS  PubMed  Google Scholar 

  3. Stollar V, Thomas VL (1975) An agent in the Aedes aegypti cell line (Peleg) which causes fusion of Aedes albopictus cells. Virology 64:367–377

    Article  CAS  PubMed  Google Scholar 

  4. Cook S, Bennett SN, Holmes EC, De Chesse R, Moureau G, de Lamballerie X (2006) Isolation of a new strain of the flavivirus cell fusing agent virus in a natural mosquito population from Puerto Rico. J Gen Virol 87:735–748

    Article  CAS  PubMed  Google Scholar 

  5. Crabtree MB, Sang RC, Stollar V, Dunster LM, Miller BR (2003) Genetic and phenotypic characterization of the newly described insect flavivirus. Kamiti River virus. Arch Virol 148:1095–1118

    Article  CAS  PubMed  Google Scholar 

  6. Sang RC, Gichogo A, Gachoya J, Dunster MD, Ofula V, Hunt AR, Crabtree MB, Miller BR, Dunster LM (2003) Isolation of a new flavivirus related to cell fusing agent virus (CFAV) from field-collected flood-water Aedes mosquitoes sampled from a dambo in central Kenya. Arch Virol 148:1085–1093

    Article  CAS  PubMed  Google Scholar 

  7. Hoshino K, Isawa H, Tsuda Y, Yano K, Sasaki T, Yuda M, Takasaki T, Kobayashi M, Sawabe K (2007) Genetic characterization of a new insect flavivirus isolated from Culex pipiens mosquito in Japan. Virology 359:405–414

    Article  CAS  PubMed  Google Scholar 

  8. Hoshino K, Isawa H, Tsuda Y, Sawabe K, Kobayashi M (2009) Isolation and characterization of a new insect flavivirus from Aedes albopictus and Aedes flavopictus mosquitoes in Japan. Virology 391:119–129

    Article  CAS  PubMed  Google Scholar 

  9. Crabtree MB, Nga PT, Miller BR (2009) Isolation and characterization of a new mosquito flavivirus, Quang Binh virus, from Vietnam. Arch Virol 154:857–860

    Article  CAS  PubMed  Google Scholar 

  10. Cook S, Moureau G, Harbach RE, Mukwaya L, Goodger K, Ssenfuka F, Gould E, Holmes EC, de Lamballerie X (2009) Isolation of a novel species of flavivirus and a new strain of Culex flavivirus (Flaviviridae) from a natural mosquito population in Uganda. J Gen Virol 90:2669–2678

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  11. Zuoshu W, Shuyi A, Yan H, Junqiao G (2009) A new virus of flavivirus: Chaoyang virus Isolated ln Liaoning province. Chin J Public Health 25:769–772

    Google Scholar 

  12. Tyler S, Bolling BG, Blair CD, Brault AC, Pabbaraju K, Armijos MV, Clark DC, Calisher CH, Drebot MA (2011) Distribution and phylogenetic comparisons of a novel mosquito flavivirus sequence present in Culex tarsalis Mosquitoes from western Canada with viruses isolated in California and Colorado. Am J Trop Med Hyg 85:162–168

    Article  PubMed Central  PubMed  Google Scholar 

  13. Hobson-Peters J, Yam AW, Lu JW, Setoh YX, May FJ, Kurucz N, Walsh S, Prow NA, Davis SS, Weir R et al (2013) A new insect-specific flavivirus from northern Australia suppresses replication of West Nile virus and Murray Valley encephalitis virus in co-infected mosquito cells. PLoS One 8:e56534

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  14. Vazquez A, Sanchez-Seco MP, Palacios G, Molero F, Reyes N, Ruiz S, Aranda C, Marques E, Escosa R, Moreno J et al (2012) Novel flaviviruses detected in different species of mosquitoes in Spain. Vector Borne Zoonotic Dis 12:223–229

    Article  PubMed Central  PubMed  Google Scholar 

  15. Huanyu W, Haiyan W, Shihong F, Guifang L, Hong L, Xiaoyan G, Lizhi S, Rayner S, Aiqiang X, Guodong L (2012) Isolation and identification of a distinct strain of Culex Flavivirus from mosquitoes collected in Mainland China. Virol J 9:73

    Article  PubMed Central  PubMed  Google Scholar 

  16. Chen YY, Lin JW, Fan YC, Tu WC, Chang GJ, Chiou SS (2013) First detection of the Africa/Caribbean/Latin American subtype of Culex flavivirus in Asian country, Taiwan. Comp Immunol Microbiol Infect Dis 36:387–396

    Article  PubMed  Google Scholar 

  17. Kim DY, Guzman H, Bueno RJ, Dennett JA, Auguste AJ, Carrington CV, Popov VL, Weaver SC, Beasley DW, Tesh RB (2009) Characterization of Culex Flavivirus (Flaviviridae) strains isolated from mosquitoes in the United States and Trinidad. Virology 386:154–159

    Article  CAS  PubMed  Google Scholar 

  18. Blitvich BJ, Lin M, Dorman KS, Soto V, Hovav E, Tucker BJ, Staley M, Platt KB, Bartholomay LC (2009) Genomic sequence and phylogenetic analysis of Culex flavivirus, an insect-specific flavivirus, isolated from Culex pipiens (Diptera: Culicidae) in Iowa. J Med Entomol 46:934–941

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  19. Morales-Betoulle ME, Monzon PM, Sosa SM, Panella N, Lopez MR, Cordon-Rosales C, Komar N, Powers A, Johnson BW (2008) Culex flavivirus isolates from mosquitoes in Guatemala. J Med Entomol 45:1187–1190

    Article  CAS  PubMed  Google Scholar 

  20. Farfan-Ale JA, Lorono-Pino MA, Garcia-Rejon JE, Hovav E, Powers AM, Lin M, Dorman KS, Platt KB, Bartholomay LC, Soto V et al (2009) Detection of RNA from a novel West Nile-like virus and high prevalence of an insect-specific flavivirus in mosquitoes in the Yucatan Peninsula of Mexico. Am J Trop Med Hyg 80:85–95

    PubMed Central  CAS  PubMed  Google Scholar 

  21. Machado DC, Mondini A, Dos SSV, Yonamine PT, Chiaravalloti NF, Zanotto PM, Nogueira ML (2012) First identification of Culex flavivirus (Flaviviridae) in Brazil. Intervirology 55:475–483

    Article  PubMed  Google Scholar 

  22. Goenaga S, Fabbri CM, Garcia JB, Rondan JC, Gardenal N, Calderon GE, Enria DA, Levis SM (2014) New strains of Culex flavivirus isolated in Argentina. J Med Entomol 51:900–906

    Article  PubMed  Google Scholar 

  23. Shuyi A, Jiasong L, Yi R, Zuoshu W, Yue H (2012) Iaolation of the Culex Flavivirus from mosquitoes in Liaoning Province, China. Chin J Virol 28:511–516

    Google Scholar 

  24. Solomon T, Ni H, Beasley DW, Ekkelenkamp M, Cardosa MJ, Barrett AD (2003) Origin and evolution of Japanese encephalitis virus in southeast Asia. J Virol 77:3091–3098

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  25. Sharma S, Dash PK, Agarwal S, Shukla J, Parida MM, Rao PV (2011) Comparative complete genome analysis of dengue virus type 3 circulating in India between 2003 and 2008. J Gen Virol 92:1595–1600

    Article  CAS  PubMed  Google Scholar 

  26. Lounibos LP (2002) Invasions by insect vectors of human disease. Annu Rev Entomol. 47 edn

  27. Gould EA, de Lamballerie X, Zanotto PM, Holmes EC (2003) Origins, evolution, and vector/host coadaptations within the genus Flavivirus. Adv Virus Res 59:277–314

    Article  CAS  PubMed  Google Scholar 

  28. Obara-Nagoya M, Yamauchi T, Watanabe M, Hasegawa S, Iwai-Itamochi M, Horimoto E, Takizawa T, Takashima I, Kariwa H (2013) Ecological and genetic analyses of the complete genomes of Culex flavivirus strains isolated from Culex tritaeniorhynchus and Culex pipiens (Diptera: Culicidae) group mosquitoes. J Med Entomol 50:300–309

    Article  CAS  PubMed  Google Scholar 

  29. Saiyasombat R, Dorman KS, Garcia-Rejon JE, Lorono-Pino MA, Farfan-Ale JA, Blitvich BJ (2010) Isolation and sequence analysis of Culex flavivirus from Culex interrogator and Culex quinquefasciatus in the Yucatan Peninsula of Mexico. Arch Virol 155:983–986

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  30. Cook S, Moureau G, Kitchen A, Gould EA, de Lamballerie X, Holmes EC, Harbach RE (2012) Molecular evolution of the insect-specific flaviviruses. J Gen Virol 93:223–234

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  31. Bolling BG, Eisen L, Moore CG, Blair CD (2011) Insect-specific flaviviruses from Culex mosquitoes in Colorado, with evidence of vertical transmission. Am J Trop Med Hyg 85:169–177

    Article  PubMed Central  PubMed  Google Scholar 

  32. Saiyasombat R, Bolling BG, Brault AC, Bartholomay LC, Blitvich BJ (2011) Evidence of efficient transovarial transmission of Culex flavivirus by Culex pipiens (Diptera: Culicidae). J Med Entomol 48:1031–1038

    Article  PubMed  Google Scholar 

  33. Barreau C, Jousset FX, Bergoin M (1997) Venereal and vertical transmission of the Aedes albopictus parvovirus in Aedes aegypti mosquitoes. Am J Trop Med Hyg 57:126–131

    CAS  PubMed  Google Scholar 

  34. Nasci RS, Hare SG, Willis FS (1989) Interspecific mating between Louisiana strains of Aedes albopictus and Aedes aegypti in the field and laboratory. J Am Mosq Control Assoc 5:416–421

    CAS  PubMed  Google Scholar 

  35. Cammisa-Parks H, Cisar LA, Kane A, Stollar V (1992) The complete nucleotide sequence of cell fusing agent (CFA): homology between the nonstructural proteins encoded by CFA and the nonstructural proteins encoded by arthropod-borne flaviviruses. Virology 189:511–524

    Article  CAS  PubMed  Google Scholar 

  36. Firth AE, Blitvich BJ, Wills NM, Miller CL, Atkins JF (2010) Evidence for ribosomal frameshifting and a novel overlapping gene in the genomes of insect-specific flaviviruses. Virology 399:153–166

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  37. Calzolari M, Ze-Ze L, Ruzek D, Vazquez A, Jeffries C, Defilippo F, Osorio HC, Kilian P, Ruiz S, Fooks AR et al (2012) Detection of mosquito-only flaviviruses in Europe. J Gen Virol 93:1215–1225

    Article  CAS  PubMed  Google Scholar 

  38. Yamanaka A, Thongrungkiat S, Ramasoota P, Konishi E (2013) Genetic and evolutionary analysis of cell-fusing agent virus based on Thai strains isolated in 2008 and 2012. Infect Genet Evol 19:188–194

    Article  PubMed  Google Scholar 

  39. Burivong P, Pattanakitsakul SN, Thongrungkiat S, Malasit P, Flegel TW (2004) Markedly reduced severity of Dengue virus infection in mosquito cell cultures persistently infected with Aedes albopictus densovirus (AalDNV). Virology 329:261–269

    Article  CAS  PubMed  Google Scholar 

  40. Pacca CC, Severino AA, Mondini A, Rahal P, D’Avila SG, Cordeiro JA, Nogueira MC, Bronzoni RV, Nogueira ML (2009) RNA interference inhibits yellow fever virus replication in vitro and in vivo. Virus Genes 38:224–231

    Article  CAS  PubMed  Google Scholar 

  41. Kent RJ, Crabtree MB, Miller BR (2010) Transmission of West Nile virus by Culex quinquefasciatus say infected with Culex Flavivirus Izabal. PLoS Negl Trop Dis 4:e671

    Article  PubMed Central  PubMed  Google Scholar 

  42. Lu Z, Fu SH, Cao L, Tang CJ, Zhang S, Li ZX, Tusong M, Yao XH, Zhang HL, Wang PY et al (2014) Human infection with West Nile Virus, Xinjiang, China, 2011. Emerg Infect Dis 20:1421–1423

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

We thank the staff of the Shandong and Shaanxi Province Centers for Disease Control and Prevention and the local Centers for Disease Control and Prevention (Longkou, Qingdao, Zichuan, Heze, Jining, Rizhao, Linyi, Weinan, Yanan and Hanzhong cities and Weishan County) for assistance with the mosquito collection.

This work was supported by grants from the Development Grant of State Key Laboratory for Infectious Disease Prevention and Control (2014SKLID103), (2012SKLID204), the Ministry of Science and Technology of People’s Republic of China (No. 2013ZX10004101) and (2011CB504702); and National Natural Science Foundation of China (81290342). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Author information

Author notes

    Authors and Affiliations

    1. Department to Epidemiology, School of Medicine, Jinan University, Guangzhou, Guangdong, 510000, People’s Republic of China

      Wenkai Liang, Guang Yang & Chunxia Jing

    2. State Key Laboratory for Infectious Disease Prevention and Control, National Institute for Viral Disease Control and Prevention, Department of Viral Encephalitis, Institute for Viral Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, 102206, People’s Republic of China

      Wenkai Liang, Xiaoxia He, Shihong Fu, Weixin Chen, Ying He, Xiaoyan Tao, Hongyue Jiang, Xiaoyan Gao, Yan Liu, Yuxi Cao, Guodong Liang & Huanyu Wang

    3. Institute for Immunization Program, Shandong province Center for Disease Control and Prevention, Jinan, Shandong, 250014, People’s Republic of China

      Guifang Liu, Min Wang, Xiaojuan Lin & Lei Feng

    4. Institute for Immunization Program, Shaanxi province Center for Disease Control and Prevention, Xi’an, Shaanxi, 710054, People’s Republic of China

      Shaobai Zhang & Weijun Hu

    5. School of Basic Medical Sciences, Harbin Medical University, Harbin, Heilongjiang, 150081, People’s Republic of China

      Yan Liu

    6. Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, Hangzhou, 310003, People’s Republic of China

      Shihong Fu, Ying He, Xiaoyan Tao, Xiaoyan Gao, Yuxi Cao, Guodong Liang & Huanyu Wang

    Authors
    1. Wenkai Liang
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Xiaoxia He
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Guifang Liu
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Shaobai Zhang
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Shihong Fu
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Min Wang
      View author publications

      You can also search for this author in PubMed Google Scholar

    7. Weixin Chen
      View author publications

      You can also search for this author in PubMed Google Scholar

    8. Ying He
      View author publications

      You can also search for this author in PubMed Google Scholar

    9. Xiaoyan Tao
      View author publications

      You can also search for this author in PubMed Google Scholar

    10. Hongyue Jiang
      View author publications

      You can also search for this author in PubMed Google Scholar

    11. Xiaojuan Lin
      View author publications

      You can also search for this author in PubMed Google Scholar

    12. Xiaoyan Gao
      View author publications

      You can also search for this author in PubMed Google Scholar

    13. Weijun Hu
      View author publications

      You can also search for this author in PubMed Google Scholar

    14. Yan Liu
      View author publications

      You can also search for this author in PubMed Google Scholar

    15. Lei Feng
      View author publications

      You can also search for this author in PubMed Google Scholar

    16. Yuxi Cao
      View author publications

      You can also search for this author in PubMed Google Scholar

    17. Guang Yang
      View author publications

      You can also search for this author in PubMed Google Scholar

    18. Chunxia Jing
      View author publications

      You can also search for this author in PubMed Google Scholar

    19. Guodong Liang
      View author publications

      You can also search for this author in PubMed Google Scholar

    20. Huanyu Wang
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding authors

    Correspondence to Chunxia Jing, Guodong Liang or Huanyu Wang.

    Additional information

    W. Liang, X. He, G. Liu and S. Zhang contributed equally to this article.

    Electronic supplementary material

    Below is the link to the electronic supplementary material.

    Supplementary material 1 (DOCX 21 kb)

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Liang, W., He, X., Liu, G. et al. Distribution and phylogenetic analysis of Culex flavivirus in mosquitoes in China. Arch Virol 160, 2259–2268 (2015). https://doi.org/10.1007/s00705-015-2492-1

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s00705-015-2492-1

    Keywords

    Search

    Navigation