Intra-host growth kinetics of dengue virus in the mosquito Aedes aegypti


Autoři: Mario Novelo aff001;  Matthew D. Hall aff001;  Damie Pak aff003;  Paul R. Young aff004;  Edward C. Holmes aff005;  Elizabeth A. McGraw aff001
Působiště autorů: School of Biological Sciences, Monash University, Melbourne, Victoria, Australia aff001;  Center for Infectious Disease Dynamics, Department of Entomology, The Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, Pennsylvania, United States of America aff002;  Center for Infectious Disease Dynamics, Department of Biology, The Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, Pennsylvania, United States of America aff003;  Australian Infectious Diseases Research Centre, School of Chemistry and Molecular Biosciences, The University of Queensland, St Lucia, Queensland, Australia aff004;  Marie Bashir Institute for Infectious Diseases and Biosecurity, Charles Perkins Centre, School of Life and Environmental Sciences and Sydney Medical School, The University of Sydney, New South Wales, Australia aff005
Vyšlo v časopise: Intra-host growth kinetics of dengue virus in the mosquito Aedes aegypti. PLoS Pathog 15(12): e32767. doi:10.1371/journal.ppat.1008218
Kategorie: Research Article
doi: 10.1371/journal.ppat.1008218

Souhrn

Dengue virus (DENV) transmission by mosquitoes is a time-dependent process that begins with the consumption of an infectious blood-meal. DENV infection then proceeds stepwise through the mosquito from the midgut to the carcass, and ultimately to the salivary glands, where it is secreted into saliva and then transmitted anew on a subsequent bite. We examined viral kinetics in tissues of the Aedes aegypti mosquito over a finely graded time course, and as per previous studies, found that initial viral dose and serotype strain diversity control infectivity. We also found that a threshold level of virus is required to establish body-wide infections and that replication kinetics in the early and intermediate tissues do not predict those of the salivary glands. Our findings have implications for mosquito GMO design, modeling the contribution of transmission to vector competence and the role of mosquito kinetics in the overall DENV epidemiological landscape.

Klíčová slova:

Aedes aegypti – Blood – Dengue virus – Dose prediction methods – Mosquitoes – Salivary glands – Viral load – Viral replication


Zdroje

1. Murray N.E., Quam M.B., and Wilder-Smith A., Epidemiology of dengue: past, present and future prospects. Clin Epidemiol, 2013. 5: p. 299–309. 10.2147/CLEP.S34440 doi: 10.2147/CLEP.S34440 23990732

2. Bhatt S., Gething P.W., Brady O.J., Messina J.P., Farlow A.W., Moyes C.L., Drake J.M., Brownstein J.S., Hoen A.G., Sankoh O., Myers M.F., George D.B., Jaenisch T., Wint G.R., Simmons C.P., Scott T.W., Farrar J.J., Hay S.I., The global distribution and burden of dengue. Nature, 2013. 496(7446): p. 504–507. 10.1038/nature12060 doi: 10.1038/nature12060 23563266

3. Brady O.J., Gething P.W., Bhatt S., Messina J.P., Brownstein J.S., Hoen A.G., Moyes C.L., Farlow A.W., Scott T.W., Hay S.I., Refining the global spatial limits of dengue virus transmission by evidence-based consensus. PLOS Negl Trop Dis, 2012. 6(8): p. e1760. 10.1371/journal.pntd.0001760

4. Gubler D.J., Dengue, urbanization and globalization: the unholy trinity of the 21(st) century. Trop Med Health, 2011. 39(4 Suppl): p. 3–11. 10.2149/tmh.2011-S05 doi: 10.2149/tmh.2011-S05 22500131

5. Simmons C.P., Farrar J.J., Nguyen V.V., Willis B., Dengue. New Eng J Med, 2012. 366(15): p. 1423–1432. 10.1056/NEJMra1110265 doi: 10.1056/NEJMra1110265 22494122

6. Powell J.R. and Tabachnick W.J., History of domestication and spread of Aedes aegypti—A Review. Mem Instit Oswaldo Cruz, 2013. 108(Suppl 1): p. 11–17. 10.1590/0074-0276130395

7. Colón-González F.J., Fezzi C., Lake I.R., Hunter P.R., The Effects of Weather and Climate Change on Dengue. PLOS Negl Trop Dis, 2013. 7(11): p. e2503. 10.1371/journal.pntd.0002503 doi: 10.1371/journal.pntd.0002503 24244765

8. Lequime S., Fontaine A., Ar Gouilh A., Moltini-Conclois I., Lambrechts L., Genetic drift, purifying selection and vector genotype shape dengue virus intra-host genetic diversity in mosquitoes. PLOS Genet, 2016. 12(6): p. e1006111. 10.1371/journal.pgen.1006111 doi: 10.1371/journal.pgen.1006111 27304978

9. Franz A.W.E., Kantor A.M., Passarelli A.L., Clem R.J., Tissue barriers to arbovirus infection in mosquitoes. Viruses, 2015. 7(7): p. 3741–3767. 10.3390/v7072795 doi: 10.3390/v7072795 26184281

10. Khoo C.C., Doty J.B., Held N.L., Olson K.E., Franz A.W., Isolation of midgut escape mutants of two American genotype dengue 2 viruses from Aedes aegypti. Virol J, 2013. 10(1): p. 1–11. 10.1186/1743-422X-10-257

11. Cox J., Brown H.E., and Rico-Hesse R., Variation in vector competence for dengue viruses does not depend on mosquito midgut binding affinity. PLOS Negl Trop Dis, 2011. 5(5): p. e1172. 10.1371/journal.pntd.0001172 doi: 10.1371/journal.pntd.0001172 21610852

12. Black W.C., Bennett K.E., Gorrochotegui-Escalante N., Barillas-Mury C.V., Fernandez-Salas I., de Lourdes Munoz M., Farfan-Ale J.A., Olson K.E., Beaty B.J., Flavivirus susceptibility in Aedes aegypti. Arch Med Res, 2002. 33(4): p. 379–388. doi: 10.1016/s0188-4409(02)00373-9 12234528

13. Macdonald G., The epidemiology and control of malaria. 1957, Amen House, Warwick Square, London E.C.4.: Oxford University Press. xiv + 201 + xl + 11 pp.

14. Deen J.L., Harris E., Willis B., Balmaseda A., Hammond S.N., Rocha C., Dung N.M., Hung N.T., Hien T.T., Farrar J.J., The WHO dengue classification and case definitions: time for a reassessment. The Lancet, 2006. 368(9530): p. 170–173.

15. Perera R. and Kuhn R.J., Structural proteomics of dengue virus. Curr Op Microbiol, 2008. 11(4): p. 369–377. 10.1016/j.mib.2008.06.004

16. Azhar E.I., Hashem A.M., El-Kafrawy S.A., Abol-Ela S., Abd-Alla A.M.M., Sohrab S.S., Farraj S.A., Othman N.A., Ben-Helaby H.G., Shshi A., Madani T.A., Jamjoom G., Complete genome sequencing and phylogenetic analysis of dengue type 1 virus isolated from Jeddah, Saudi Arabia. Virol J, 2015. 12: p. 1. 10.1186/s12985-014-0235-7 doi: 10.1186/s12985-014-0235-7 25591713

17. Anderson J.R. and Rico-Hesse R., Aedes aegypti vectorial capacity is determined by the infecting genotype of dengue virus. Am J Trop Med Hyg, 2006. 75.

18. Armstrong P.M. and Rico-Hesse R., Efficiency of dengue serotype 2 virus strains to infect and disseminate in Aedes aegypti. Am J Trop Med Hyg, 2003. 68.

19. Lambrechts L., Fansiri T., Pongsi A., Thaisomboonsuk B., Klungthong C., Richardson J.H., Ponlawat A., Jarman R.G., Scott T.W. Dengue-1 virus clade replacement in Thailand associated with enhanced mosquito transmission. J Virol, 2012. 86(3): p. 1853–1861. 10.1128/JVI.06458-11 doi: 10.1128/JVI.06458-11 22130539

20. Ty Hang V.T., Holmes E.C., Duong V., Nguyen T.Q., Tran T.H., Quail M., Churcher C., Parkhill J., Cardosa J., Farrar J., Willis B., Lennon N.J., Birren B.W., Buchy P., Henn M.R., Simmons C.P., Emergence of the Asian 1 genotype of dengue virus serotype 2 in Vietnam: in vivo fitness advantage and lineage replacement in South-East Asia. PLOS Negl Trop Dis, 2010. 4(7):e757. 10.1371/journal.pntd.0000757 doi: 10.1371/journal.pntd.0000757 20651932

21. Guzman M.G. and Harris E., Dengue. The Lancet, 2015. 385(9966): p. 453–465. 10.1016/S0140-6736(14)60572-9

22. Ritchie S.A., Pyke A.T., Hall-Mendelin S., Day A., Mores C.N., Christofferson R.C., Gubler D.J., Bennett S.N., van den Hurk A.F., An explosive epidemic of DENV-3 in Cairns, Australia. PLOS One, 2013. 8(7): p. e68137. 10.1371/journal.pone.0068137 doi: 10.1371/journal.pone.0068137 23874522

23. Cheng G., Liu Y., Wang P., Xiao X, Mosquito defense strategies against viral infection. Trends Parasitol, 2016. 32(3): p. 177–186. 10.1016/j.pt.2015.09.009 doi: 10.1016/j.pt.2015.09.009 26626596

24. Hall M. D., Bento G., and Ebert D. (2017). The evolutionary consequenses of stepwise infection processes. Tr Ecol Evol, 32(8) 612–623. 10.10.16/j.tree.2017.05.009

25. Zieler H., Zieler H., Garon C. F., Fischer E. R., Shahabuddin M. A tubular network associated with the brush-border surface of the Aedes aegypti midgut: implications for pathogen transmission by mosquitoes. J Exp Biol, 2000. 203(Pt 10): p. 1599–611. 10769222

26. Christofferson R.C. and Mores C.N., Estimating the magnitude and direction of altered arbovirus transmission due to viral phenotype. PLOS ONE, 2011. 6(1): p. e16298. doi: 10.1371/journal.pone.0016298 21298018

27. Duong Veasna., Lambrechts Louis., Paul Richard E., Ly Sowath., Lay Rath Srey., Long Kanya C., Huy Rekol., Tarantola Arnaud., Scott Thomas W., Sakuntabhai Anavaj., Buchy, Philippe, Asymptomatic humans transmit dengue virus to mosquitoes. PNAS USA 2015. 112(47): p. 14688–14693. 10.1073/pnas.1508114112 doi: 10.1073/pnas.1508114112 26553981

28. Gubler D.J., Nalim S., Tan R., Saipan H., Sulianti Saroso J., Variation in susceptibility to oral infection with dengue viruses among geographic strains of Aedes aegypti. Am J Trop Med Hyg, 1979. 28(6): p. 1045–1052. doi: 10.4269/ajtmh.1979.28.1045 507282

29. Rosen L., Rosenbloom L.E., Gubler D.J., Lien J.C., Chaniotis B.N., Comparative susceptibility of mosquito species and strains to oral and parenteral infection with dengue and Japanese encephalitis viruses. Am J Trop Med Hyg, 1985. 34(3): p. 603–615. doi: 10.4269/ajtmh.1985.34.603 2860816

30. Fontaine A., Lequime S., Moltini-Conclois I., Jiolle D., Leparc-Goffart I., Reiner R.C., Lambrechts L., Epidemiological significance of dengue virus genetic variation in mosquito infection dynamics. PLOS Pathog, 2018. 14(7): p. e1007187. 10.1371/journal.ppat.1007187 doi: 10.1371/journal.ppat.1007187 30005085

31. Duneau D., Ferdy J. B., Revah J., Kondolf H., Ortiz G. A., Lazzaro B. P., Buchon N. Stochastic variation in the initial phase of bacterial infection predicts the probability of survival in D. melanogaster. Elife, 2017. 6. 10.7554/eLife.28298

32. Taracena M.L., Bottino-Rojas V., Talyuli O.A.C., Walter-Nuno A.B., Oliveira J.H.M., Anglero-Rodriguez Y., Wells M.B., Dimopoulos G., Regulation of midgut cell proliferation impacts Aedes aegypti susceptibility to dengue virus. PLOS Negl Trop Dis, 2018. 12(5): p. e0006498. 10.1371/journal.pntd.0006498 doi: 10.1371/journal.pntd.0006498 29782512

33. Chotiwan N., Andre B.G., Sanchez-Vargas I., Islam M.N., Grabowski J.M., Hopf-Jannasch A., Gough E., Nakayasu E., Blair C.D., Belisle J.T., Hill C.A., Kuhn R.J., Perera R., Dynamic remodeling of lipids coincides with dengue virus replication in the midgut of Aedes aegypti mosquitoes. PLOS Pathog, 2018. 14(2): p. e1006853. 10.1371/journal.ppat.1006853 doi: 10.1371/journal.ppat.1006853 29447265

34. Choy M.M., Sessions O.M., Gubler D.J., Ooi E.E., Production of infectious dengue virus in Aedes aegypti is dependent on the ubiquitin proteasome pathway. PLOS Negl Trop Dis, 2015. 9(11): p. e0004227. 10.1371/journal.pntd.0004227 doi: 10.1371/journal.pntd.0004227 26566123

35. Reid D.W., Campos R.K., Child J.R., Zheng T., Chan K.W.K., Bradrick S.S., Vasudevan S.G., Garcia-Blanco M.A., Nicchitta C.V., Dengue virus selectively annexes endoplasmic reticulum-associated translation machinery as a strategy for co-opting host cell protein synthesis. J Virol, 2018. 92(7): p. e01766–17. 10.1128/JVI.01766-17 doi: 10.1128/JVI.01766-17 29321322

36. Helt A.-M. and Harris E., S-phase-dependent enhancement of dengue virus 2 replication in mosquito cells, but not in human cells. J Virol, 2005. 79(21): p. 13218–13230. doi: 10.1128/JVI.79.21.13218-13230.2005 16227245

37. Forrester N.L., Guerbois M., Seymour R.L., Spratt H., Weaver S.C., Vector-borne transmission iImposes a severe bottleneck on an RNA virus population. PLOS Pathog, 2012. 8(9): p. e1002897. 10.1371/journal.ppat.1002897 doi: 10.1371/journal.ppat.1002897 23028310

38. Zhu Y., Zhu, Yibin., Zhang, Rudian., Zhang, Bei., Zhao, Tongyan., Wang, Penghua., Liang, Guodong., Cheng, Gong. Blood meal acquisition enhances arbovirus replication in mosquitoes through activation of the GABAergic system. Nat Comm, 2017. 8(1): p. 1262. 10.1038/s41467-017-01244-6

39. Muturi E.J., Buckner E., and Bara J., Superinfection interference between dengue-2 and dengue-4 viruses in Aedes aegypti mosquitoes. Trop Med Int Health, 2017. 22(4): p. 399–406. 10.1111/tmi.12846 doi: 10.1111/tmi.12846 28150899

40. Le Coupanec A., Le Coupanec A., Tchankouo-Nguetcheu S., Roux P., Khun H., Huerre M., Morales-Vargas R., Enguehard M., Lavillette D., Misse D., Choumet V. Co-infection of mosquitoes with chikungunya and dengue viruses reveals modulation of the replication of both viruses in midguts and salivary glands of Aedes aegypti mosquitoes. Int J Mol Sci, 2017. 18(8). 10.3390/ijms18081708

41. Smartt C.T., Shin D., and Alto B.W., Dengue serotype-specific immune response in Aedes aegypti and Aedes albopictus. Mem Instit Oswaldo Cruz, 2017. 112(12): p. 829–837. 10.1590/0074-02760170182

42. Sim S. and Dimopoulos G., Dengue virus inhibits immune responses in Aedes aegypti cells. PLOS ONE, 2010. 5(5): p. e10678. 10.1371/journal.pone.0010678 doi: 10.1371/journal.pone.0010678 20502529

43. Cao-Lormeau V.-M., Dengue viruses binding proteins from Aedes aegypti and Aedes polynesiensis salivary glands. Virol J, 2009. 6(1): p. 35. 10.1186/1743-422X-6-35

44. Salazar M.I., Richardson J.H., Sanchez-Vargas I., Olson K.E., Beaty B.J., Dengue virus type 2: replication and tropisms in orally infected Aedes aegypti mosquitoes. BMC Microbiol, 2007. 7: p. 9. doi: 10.1186/1471-2180-7-9 17263893

45. Raquin V. and Lambrechts L., Dengue virus replicates and accumulates in Aedes aegypti salivary glands. Virol, 2017. 507: p. 75–81.

46. Dumre S.P., Bhandari R., Shakya G., Shrestha S.K., Cherif M.S., Ghimire P., Klungthong C., Yoon I.K., Hirayama K., Na-Bangchang K., Dengue virus serotypes 1 and 2 responsible for major dengue outbreaks in Nepal: clinical, laboratory, and epidemiological features. Am J Trop Med Hyg, 2017. 97(4): p. 1062–1069. 10.4269/ajtmh.17-0221 doi: 10.4269/ajtmh.17-0221 29031282

47. Shrivastava S., Tiraki D., Diwan A., Lalwani S.K., Modak M., Mishra A.C., Arankalle V.A., Co-circulation of all the four dengue virus serotypes and detection of a novel clade of DENV-4 (genotype I) virus in Pune, India during 2016 season. PLOS ONE, 2018. 13(2): p. e0192672. 10.1371/journal.pone.0192672 doi: 10.1371/journal.pone.0192672 29470509

48. Liebman K.A., Stoddard S.T., Morrison A.C., Rocha C., Minnick S., Sihuincha M., Russell K.L., Olson J.G., Blair P.J., Watts D.M., Kochel T., Scott T.W., Spatial dimensions of dengue virus transmission across interepidemic and epidemic periods in Iquitos, Peru (1999–2003). PLOS Negl Trop Dis, 2012. 6(2): p. e1472. 10.1371/journal.pntd.0001472 doi: 10.1371/journal.pntd.0001472 22363822

49. Sasmono R.T., Taurel A.F., Prayitno A., Sitompul H., Yohan B., Hayati R.F., Bouckenooghe A., Hadinegoro S.R., Nealon J., Dengue virus serotype distribution based on serological evidence in pediatric urban population in Indonesia. PLOS Negl Trop Dis, 2018. 12(6): p. e0006616. 10.1371/journal.pntd.0006616 doi: 10.1371/journal.pntd.0006616 29953438

50. Balmaseda A., Hammond S.N., Perez L., Tellez Y., Saborio S.I., Mercado J.C., Cuadra R., Rocha J., Perez M.A., Rocha C., Harris E., Serotype-specific differences in clinical manifestations of dengue. Am J Trop Med Hyg, 2006. 74: p. 449–456. 16525106

51. OhAinle M., Balmaseda A., Macalalad A.R., Tellez Y., Zody M.C., Saborio S., Nunez A., Lennon N.J., Birren B.W., Gordon A., Henn M.R., Harris E., Dynamics of dengue disease severity determined by the interplay between viral genetics and serotype-specific immunity. Sci Transl Med, 2011. 3(114): p. 114ra128. 10.1126/scitranslmed.3003084

52. Vaughn D.W., Green S., Kalayanarooj K., Innis B.L., Nimmannitya S., Suntayakorn S., Endy T.P., Raengsakulrach B., Rothman A.L., Ennis F.A., Nisalak A., Dengue viremia titer, antibody response pattern, and virus serotype correlate with disease severity. J Infect Dis, 2000. 181(1): p. 2–9. doi: 10.1086/315215 10608744

53. Halsey E.S., Marks M.A., Gotuzzo E., Fiestas V., Suarez L., Vargas J., Aguayo N., Madrid C., Vimos C., Kochel T.J., Laguna-Torres V.A., Correlation of serotype-specific dengue virus infection with clinical manifestations. PLOS Negl Trop Dis, 2012. 6(5): p. e1638. 10.1371/journal.pntd.0001638 doi: 10.1371/journal.pntd.0001638 22563516

54. R Reich Nicholas G., Shrestha Sourya., King Aaron A., Rohani Pejman., Lessler Justin., Kalayanarooj Siripen., Yoon In-Kyu., Gibbons Robert V., Burke Donald S., Cummings Derek A. T. Interactions between serotypes of dengue highlight epidemiological impact of cross-immunity. J Royal Soc Interface, 2013. 10(86). 10.1098/rsif.2013.0414 doi: 10.1098/rsif.2013.0414 23825116

55. Frentiu F.D., Robinson J., Young P.R. McGraw E.A., O'Neill S.L, Wolbachia-mediated resistance to dengue virus infection and death at the cellular level. PLOS ONE, 2010. 5(10): p. e13398. 10.1371/journal.pone.0013398 doi: 10.1371/journal.pone.0013398 20976219

56. Amuzu H.E., Simmons C.P., and McGraw E.A., Effect of repeat human blood feeding on Wolbachia density and dengue virus infection in Aedes aegypti. Parasit Vectors, 2015. 8: p. 246. 10.1186/s13071-015-0853-y doi: 10.1186/s13071-015-0853-y 25903749

57. Ye Y.H., Carrasco A.M., Frentiu F.D., Chenoweth S.F., Beebe N.W., van den Hurk A.F., Simmons C.P., O'Neill S.L., McGraw E.A., Wolbachia reduces the transmission potential of dengue-infected Aedes aegypti. PLOS Negl Trop Dis, 2015. 9(6): p. e0003894. 10.1371/journal.pntd.0003894 doi: 10.1371/journal.pntd.0003894 26115104

58. Ye Y.H., Ng T. S., Frentiu F. D., Walker T., van den Hurk A. F., O'Neill S. L., Beebe N. W., McGraw E. A., Comparative susceptibility of mosquito populations in North Queensland, Australia to oral infection with dengue virus. Am J Trop Med Hyg, 2014. 90(3): p. 422–30. 10.4269/ajtmh.13-0186 doi: 10.4269/ajtmh.13-0186 24420782

59. Ritz C., Baty F., Streibig J.C., Gerhard D., Dose-response analysis using R. PLOS ONE, 2016. 10(12): p. e0146021. 10.1371/journal.pone.0146021

Štítky
Hygiena a epidemiologie Infekční lékařství Laboratoř

Článek vyšel v časopise

PLOS Pathogens


2019 Číslo 12

Nejčtenější v tomto čísle

Tomuto tématu se dále věnují…


Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Farmaceutická péče o pacienta s inhalační terapií
nový kurz
Autoři: Mgr. Ondřej Šimandl

Revmatoidní artritida: včas a k cíli
Autoři: MUDr. Heřman Mann

Jistoty a nástrahy antikoagulační léčby aneb kardiolog - neurolog - farmakolog - nefrolog - právník diskutují
Autoři: doc. MUDr. Štěpán Havránek, Ph.D., prof. MUDr. Roman Herzig, Ph.D., doc. MUDr. Karel Urbánek, Ph.D., prim. MUDr. Jan Vachek, MUDr. et Mgr. Jolana Těšínová, Ph.D.

Léčba akutní pooperační bolesti
Autoři: doc. MUDr. Jiří Málek, CSc.

Nové antipsychotikum kariprazin v léčbě schizofrenie
Autoři: prof. MUDr. Cyril Höschl, DrSc., FRCPsych.

Všechny kurzy
Přihlášení
Zapomenuté heslo

Nemáte účet?  Registrujte se

Zapomenuté heslo

Zadejte e-mailovou adresu se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se