Infection via mosquito bite alters Zika virus tissue tropism and replication kinetics in rhesus macaques

Nature Communications

Volumn 8, Issue 1, 2017, Pages

  Dudley, Dawn M ^a   Newman, Christina M ^a   Lalli, Joseph ^b   Stewart, Laurel M ^a   Koenig, Michelle R ^a   Weiler, Andrea M ^c   Semler, Matthew R ^a   Barry, Gabrielle L ^c   Zarbock, Katie R ^a   Mohns, Mariel S ^a   Breitbach, Meghan E ^a   Schultz Darken, Nancy ^c   Peterson, Eric ^c   Newton, Wendy ^c   Mohr, Emma L ^a   Capuano, Saverio ^c   Osorio, Jorge E ^b   O'Connor, Shelby L ^a,c   O'Connor, David H ^a,c   Friedrich, Thomas C ^b,c   Aliota, Matthew T ^a,b   more..

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c UNIVERSITY OF WISCONSIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANATOMY; CELLS AND CELL COMPONENTS; DISEASE INCIDENCE; FEMALE; HETEROGENEITY; INFECTIOUS DISEASE; INOCULATION; MOSQUITO; PRIMATE; REACTION KINETICS; VACCINE; VIRAL DISEASE; VIRUS;

ANIMAL TISSUE; ARTICLE; INOCULATION; MOSQUITO BITE; MOSQUITO VECTOR; NONHUMAN; RHESUS MONKEY; TISSUE DISTRIBUTION; TROPISM; VIROGENESIS; VIRUS LOAD; VIRUS REPLICATION; VIRUS TRANSMISSION; ZIKA FEVER; AEDES; ANIMAL; CHLOROCEBUS AETHIOPS; FEMALE; HUMAN; KINETICS; MALE; PHYSIOLOGY; PRIMATE DISEASE; VERO CELL LINE; VIRAL TROPISM; VIROLOGY; ZIKA VIRUS;

ANIMALIA; MACACA MULATTA; PRIMATES; ZIKA VIRUS;

AEDES; ANIMALS; CERCOPITHECUS AETHIOPS; FEMALE; HUMANS; KINETICS; MACACA MULATTA; MALE; MOSQUITO VECTORS; PRIMATE DISEASES; VERO CELLS; VIRAL LOAD; VIRAL TROPISM; VIRUS REPLICATION; ZIKA VIRUS; ZIKA VIRUS INFECTION;

EID: 85038444940     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/s41467-017-02222-8     Document Type: Article

References (59)

1. Aliota, M. T. et al. Heterologous Protection against Asian Zika Virus Challenge in Rhesus Macaques. PLoS Negl. Trop. Dis. 10, e0005168 (2016).
2. Dudley, D. M. et al. A rhesus macaque model of Asian-lineage Zika virus infection. Nat. Commun. 7, 12204 (2016).
3. Li, X. F. et al. Characterization of a 2016 clinical isolate of Zika virus in nonhuman primates. EbioMedicine 12, 170-177 (2016).
4. Koide, F. et al. Development of a Zika virus infection model in cynomolgus macaques. Front Microbiol 7, 2028 (2016).
5. Adams Waldorf, K. M. et al. Fetal brain lesions after subcutaneous inoculation of Zika virus in a pregnant nonhuman primate. Nat. Med 22, 1256-1259 (2016).
6. Abbink, P. et al. Protective efficacy of multiple vaccine platforms against Zika virus challenge in rhesus monkeys. Science 353, 1129-1132 (2016).
7. Coffey, L. L. et al. Zika virus tissue and blood compartmentalization in acute infection of rhesus macaques. PLoS ONE 12, e0171148 (2017).
8. Vanderberg, J. et al. Assessment of antibody protection against malaria sporozoites must be done by mosquito injection of sporozoites. Am. J. Pathol. 171, 1405-6 (2007)
9. Thangamani, S. et al. Host immune response to mosquito-transmitted chikungunya virus differs from that elicited by needle inoculated virus. PLoS ONE 5, e12137 (2010).
10. Leitner, W. W., Costero-Saint Denis, A. & Wali, T. Immunological consequences of arthropod vector-derived salivary factors. Eur. J. Immunol. 41, 3396-3400 (2011).
11. Smith, D. R. et al. Venezuelan equine encephalitis virus transmission and effect on pathogenesis. Emerg. Infect. Dis. 12, 1190-1196 (2006).
12. Styer, L. M. et al. Mosquitoes inoculate high doses of West Nile virus as they probe and feed on live hosts. PLoS Pathog. 3, 1262-1270 (2007).
13. Ribeiro, J. M. Role of saliva in blood-feeding by arthropods. Annu. Rev. Entomol. 32, 463-478 (1987).
14. Leitner, W. W., Costero-Saint Denis, A. & Wali, T. Role of immune cell subsets in the establishment of vector-borne infections. Eur. J. Immunol. 42, 3110-3115 (2012).
15. Pingen, M., Schmid, M. A., Harris, E. & McKimmie, C. S. Mosquito biting modulates skin response to virus infection. Trends Parasitol. 33, 645-657 (2017).
16. Styer, L. M. et al. Mosquito saliva causes enhancement of West Nile virus infection in mice. J. Virol. 85, 1517-1527 (2011).
17. Cox, J., Mota, J., Sukupolvi-Petty, S., Diamond, M. S. & Rico-Hesse, R. Mosquito bite delivery of dengue virus enhances immunogenicity and pathogenesis in humanized mice. J. Virol. 86, 7637-7649 (2012).
18. Schmid, M. A. et al. Mosquito Saliva Increases Endothelial Permeability in the Skin, Immune Cell Migration, and Dengue Pathogenesis during Antibody- Dependent Enhancement. PLoS Pathog. 12, e1005676 (2016).
19. Fontaine, A. et al. Implication of haematophagous arthropod salivary proteins in host-vector interactions. Parasit. Vectors 4, 187 (2011).
20. Schneider, B. S. & Higgs, S. The enhancement of arbovirus transmission and disease by mosquito saliva is associated with modulation of the host immune response. Trans. R. Soc. Trop. Med. Hyg. 102, 400-408 (2008).
21. Schneider, B. S. et al. Potentiation of West Nile encephalitis by mosquito feeding. Viral Immunol. 19, 74-82 (2006).
22. Conway, M. J. et al. Mosquito saliva serine protease enhances dissemination of dengue virus into the mammalian host. J. Virol. 88, 164-175 (2014).
23. Pingen, M. et al. Host inflammatory response to mosquito bites enhances the severity of arbovirus infection. Immunity 44, 1455-1469 (2016).
24. Nguyen, S. M. et al. Highly efficient maternal-fetal Zika virus transmission in pregnant rhesus macaques. PLoS Pathog. 13, e1006378 (2017).
25. Gubler, D. J. & Rosen, L. A simple technique for demonstrating transmission of dengue virus by mosquitoes without the use of vertebrate hosts. Am. J. Trop. Med. Hyg. 25, 146-150 (1976).
26. Osuna, C. E. et al. Zika viral dynamics and shedding in rhesus and cynomolgus macaques. Nat. Med. 22, 1448-1455 (2016).
27. Boorman, J. P. & Porterfield, J. S. A simple technique for infection of mosquitoes with viruses; transmission of Zika virus. Trans. R. Soc. Trop. Med. Hyg. 50, 238-242 (1956).
28. Aliota, M. T., Peinado, S. A., Osorio, J. E. & Bartholomay, L. C. Culex pipiens and Aedes triseriatus Mosquito Susceptibility to Zika Virus. Emerg. Infect. Dis. 22, 1857-1859 (2016).
29. Aliota, M. T., Peinado, S. A., Velez, I. D. & Osorio, J. E. The wMel strain of Wolbachia Reduces Transmission of Zika virus by Aedes aegypti. Sci. Rep. 6, 28792 (2016).
30. Lequime, S., Fontaine, A., Ar Gouilh, M., Moltini-Conclois, I. & Lambrechts, L. Genetic drift, purifying selection and vector genotype shape dengue virus intrahost genetic diversity in mosquitoes. PLoS Genet. 12, e1006111 (2016).
31. Grubaugh, N. D. et al. Genetic Drift during Systemic Arbovirus Infection of Mosquito Vectors Leads to Decreased Relative Fitness during Host Switching. Cell Host Microbe 19, 481-492 (2016).
32. Grubaugh, N. D. et al. Genomic epidemiology reveals multiple introductions of Zika virus into the United States. Nature 546, 401-405 (2017).
33. Dzul-Manzanilla, F. et al. Evidence of vertical transmission and co-circulation of chikungunya and dengue viruses in field populations of Aedes aegypti (L.) from Guerrero, Mexico. Trans. R. Soc. Trop. Med. Hyg. 110, 141-144 (2016).
34. Miller, B. R., Monath, T. P., Tabachnick, W. J. & Ezike, V. I. Epidemic yellow fever caused by an incompetent mosquito vector. Trop. Med. Parasitol. 40, 396-399 (1989).
35. Osorio, J. E., Godsey, M. S., Defoliart, G. R. & Yuill, T. M. La Crosse viremias in white-tailed deer and chipmunks exposed by injection or mosquito bite. Am. J. Trop. Med. Hyg. 54, 338-342 (1996).
36. Hirsch, A. J. et al. Zika Virus infection of rhesus macaques leads to viral persistence in multiple tissues. PLoS Pathog. 13, e1006219 (2017).
37. Aid, M. et al. Zika Virus Persistence in the Central Nervous System and Lymph Nodes of Rhesus Monkeys. Cell 169, 610-620.e14 (2017).
38. Villamil-Gomez, W. E. et al. Guillain-Barré syndrome during the Zika virus outbreak in Sucre, Colombia, 2016. Travel Med. Infect. Dis. 16, 62-63 (2017).
39. Dos Santos, T. et al. Zika Virus and the Guillain-Barré Syndrome - Case Series from Seven Countries. N. Engl. J. Med. 375, 1598-1601 (2016).
40. Araujo, A. Q., Silva, M. T. & Araujo, A. P. Zika virus-associated neurological disorders: a review. Brain 139, 2122-2130 (2016).
41. Moreira, J., Peixoto, T. M., Siqueira, A. M. & Lamas, C. C. Sexually acquired Zika virus: a systematic review. Clin. Microbiol. Infect. 23, 296-305 (2017).
42. Faria, N. R. et al. Zika virus in the Americas: Early epidemiological and genetic findings. Science 352, 345-349 (2016).
43. Ciota, A. T. et al. Effects of Zika Virus Strain and Aedes Mosquito Species on Vector Competence. Emerg. Infect. Dis. 23, 1110-1117 (2017).
44. Aliota, M. T. et al. The wMel Strain of Wolbachia Reduces Transmission of Chikungunya Virus in Aedes aegypti. PLoS Negl. Trop. Dis. 10, e0004677 (2016).
45. Musso, D. et al. Molecular detection of Zika virus in blood and RNA load determination during the French Polynesian outbreak. J. Med. Virol. 89, 1505-1510 (2017).
46. Metsky, H. C. et al. Zika virus evolution and spread in the Americas. Nature 546, 411-415 (2017).
47. Halai, U. A. et al. Maternal Zika virus disease severity, virus load, prior dengue antibodies and their relationship to birth outcomes. Clin. Infect. Dis. 65, 877-883 (2017).
48. Bearcroft, W. G. Zika virus infection experimentally induced in a human volunteer. Trans. R. Soc. Trop. Med. Hyg. 50, 442-448 (1956).
49. Althouse, B. M. et al. Potential for Zika Virus to Establish a Sylvatic Transmission Cycle in the Americas. PLoS Negl. Trop. Dis. 10, e0005055 (2016).
50. Rogers, M. E., Ilg, T., Nikolaev, A. V., Ferguson, M. A. & Bates, P. A. Transmission of cutaneous leishmaniasis by sand flies is enhanced by regurgitation of fPPG. Nature 430, 463-467 (2004).
51. Peters, N. C. et al. Vector transmission of leishmania abrogates vaccine-induced protective immunity. PLoS Pathog. 5, e1000484 (2009).
52. Sheehy, S. H. et al. ChAd63-MVA-vectored blood-stage malaria vaccines targeting MSP1 and AMA1: assessment of efficacy against mosquito bite challenge in humans. Mol. Ther. 20, 2355-2368 (2012).
53. Christensen, B. M. & Sutherland, D. R. Brugia pahangi: exsheathment and midgut penetration in Aedes aegypti. Trans. Am. Microsc. Soc. 103, 423-433 (1984).
54. Lanciotti, R. S. et al. Genetic and serologic properties of Zika virus associated with an epidemic, Yap State, Micronesia, 2007. Emerg. Infect. Dis. 14, 1232-1239 (2008).
55. Quick, J. et al. Multiplex PCR method for MinION and Illumina sequencing of Zika and other virus genomes directly from clinical samples. Nat. Protoc. 12, 1261-1276 (2017).
56. Cingolani, P. et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strainw1118; iso-2; iso-3. Fly (Austin) 6, 80-92 (2012).
57. Satya, R. V. & DiCarlo, J. Edge effects in calling variants from targeted amplicon sequencing. BMC Genomics 15, 1073 (2014).
58. Kofler, R. et al. PoPoolation: a toolbox for population genetic analysis of next generation sequencing data from pooled individuals. PLoS ONE 6, e15925 (2011).
59. R Development Core Team. R: a language and environment for statistical computing. https://www.gbif.org/tool/81287/r-a-language-and-environmentfor-statistical-computing (2016).