Dengue virus type 1 clade replacement in recurring homotypic outbreaks

BMC Evolutionary Biology

Sazaly AbuBakar²  Nor Muhammad Mahadi¹  NorAziyah MatRahim²  Juraina Abd-Jamil²  Mohammed Bashar Danlami²  Meng-Hooi Shu²  Jefree Johari²  Kim-Kee Tan²  Sing-Sin Sam²  Boon-Teong Teoh² 

[1] Malaysia Genome Institute, Kajang, Selangor 43000, Malaysia;Tropical Infectious Diseases Research and Education Centre (TIDREC), Department of Medical Microbiology, Faculty of Medicine, University of Malaya, Kuala Lumpur 50603, Malaysia

关键词: Clade replacement;    Evolution;    Malaysia;    Immunity;    Dengue;    Infectious disease;   

Others  :  1085835
DOI  :  10.1186/1471-2148-13-213

 received in 2013-05-10, accepted in 2013-09-25,  发布年份 2013

【 摘 要 】

Background

Recurring dengue outbreaks occur in cyclical pattern in most endemic countries. The recurrences of dengue virus (DENV) infection predispose the population to increased risk of contracting the severe forms of dengue. Understanding the DENV evolutionary mechanism underlying the recurring dengue outbreaks has important implications for epidemic prediction and disease control.

Results

We used a set of viral envelope (E) gene to reconstruct the phylogeny of DENV-1 isolated between the periods of 1987–2011 in Malaysia. Phylogenetic analysis of DENV-1 E gene revealed that genotype I virus clade replacements were associated with the cyclical pattern of major DENV-1 outbreaks in Malaysia. A total of 9 non-conservative amino acid substitutions in the DENV-1 E gene consensus were identified; 4 in domain I, 3 in domain II and 2 in domain III. Selection pressure analyses did not reveal any positively selected codon site within the full length E gene sequences (1485 nt, 495 codons). A total of 183 (mean dN/dS = 0.0413) negatively selected sites were found within the Malaysian isolates; neither positive nor negative selection was noted for the remaining 312 codons. All the viruses were cross-neutralized by the respective patient sera suggesting no strong support for immunological advantage of any of the amino acid substitutions.

Conclusion

DENV-1 clade replacement is associated with recurrences of major DENV-1 outbreaks in Malaysia. Our findings are consistent with those of other studies that the DENV-1 clade replacement is a stochastic event independent of positive selection.

【 授权许可】

   
2013 Teoh et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Henchal EA, Putnak JR: The dengue viruses. Clin Microbiol Rev 1990, 3(4):376-396.
• [2]Russell PK, Nisalak A: Dengue virus identification by the plaque reduction neutralization test. J Immunol 1967, 99(2):291-296.
• [3]Holmes EC, Burch SS: The causes and consequences of genetic variation in dengue virus. Trends Microbiol 2000, 8(2):74-77.
• [4]Wang E, Ni H, Xu R, Barrett AD, Watowich SJ, Gubler DJ, Weaver SC: Evolutionary relationships of endemic/epidemic and sylvatic dengue viruses. J Virol 2000, 74(7):3227-3234.
• [5]Gubler DJ: The economic burden of dengue. Am J Trop Med Hyg 2012, 86(5):743-744.
• [6]Zhang C, Mammen MP Jr, Chinnawirotpisan P, Klungthong C, Rodpradit P, Monkongdee P, Nimmannitya S, Kalayanarooj S, Holmes EC: Clade replacements in dengue virus serotypes 1 and 3 are associated with changing serotype prevalence. J Virol 2005, 79(24):15123-15130.
• [7]Nisalak A, Endy TP, Nimmannitya S, Kalayanarooj S, Thisayakorn U, Scott RM, Burke DS, Hoke CH, Innis BL, Vaughn DW: Serotype-specific dengue virus circulation and dengue disease in Bangkok, Thailand from 1973 to 1999. Am J Trop Med Hyg 2003, 68(2):191-202.
• [8]Abubakar S, Shafee N: Outlook of dengue in Malaysia: a century later. Malays J Pathol 2002, 24(1):23-27.
• [9]Vu TT, Holmes EC, Duong V, Nguyen TQ, Tran TH, Quail M, Churcher C, Parkhill J, Cardosa J, Farrar J, Wills B, Lennon NJ, Birren BW, Buchy P, Henn MR, Simmons CP: Emergence of the Asian 1 genotype of dengue virus serotype 2 in viet nam: in vivo fitness advantage and lineage replacement in South-East Asia. PLoS Negl Trop Dis 2010, 4(7):e757.
• [10]Bennett SN, Drummond AJ, Kapan DD, Suchard MA, Munoz-Jordan JL, Pybus OG, Holmes EC, Gubler DJ: Epidemic dynamics revealed in dengue evolution. Mol Biol Evol 2010, 27(4):811-818.
• [11]Sam SS, Syed Omar SF, Teoh BT, Abd-Jamil J, AbuBakar S: Review of dengue hemorrhagic fever fatal cases seen among adults: a retrospective study. PLoS Negl Trop Dis 2013, 7(5):e2194.
• [12]Halstead SB: Observations related to pathogensis of dengue hemorrhagic fever. VI. Hypotheses and discussion. Yale J Biol Med 1970, 42(5):350-362.
• [13]Kouri GP, Guzman MG, Bravo JR, Triana C: Dengue haemorrhagic fever/dengue shock syndrome: lessons from the Cuban epidemic, 1981. Bull World Health Organ 1989, 67(4):375-380.
• [14]Halstead SB, Rojanasuphot S, Sangkawibha N: Original antigenic sin in dengue. Am J Trop Med Hyg 1983, 32(1):154-156.
• [15]Mongkolsapaya J, Dejnirattisai W, Xu XN, Vasanawathana S, Tangthawornchaikul N, Chairunsri A, Sawasdivorn S, Duangchinda T, Dong T, Rowland-Jones S, Yenchitsomanus PT, McMichael A, Malasit P, Screaton G: Original antigenic sin and apoptosis in the pathogenesis of dengue hemorrhagic fever. Nat Med 2003, 9(7):921-927.
• [16]Pang T, Cardosa MJ, Guzman MG: Of cascades and perfect storms: the immunopathogenesis of dengue haemorrhagic fever-dengue shock syndrome (DHF/DSS). Immunol Cell Biol 2007, 85(1):43-45.
• [17]Markoff LJ, Innis BL, Houghten R, Henchal LS: Development of cross-reactive antibodies to plasminogen during the immune response to dengue virus infection. J Infect Dis 1991, 164(2):294-301.
• [18]Falconar AK: The dengue virus nonstructural-1 protein (NS1) generates antibodies to common epitopes on human blood clotting, integrin/adhesin proteins and binds to human endothelial cells: potential implications in haemorrhagic fever pathogenesis. Arch Virol 1997, 142(5):897-916.
• [19]Kurane I, Ennis FE: Immunity and immunopathology in dengue virus infections. Semin Immunol 1992, 4(2):121-127.
• [20]Teerasut C, Lei HY, Natthakorn K, Jittmittraphap A, Thammapalo S, Witayathawornwong P, Lin YT, Jarman RG, Sawanpanyalert P, Jampangern W, Limkittikul K: The serotype-independent but concentration-dependent enhancing antibodies among Thai dengue patients. Southeast Asian J Trop Med Public Health 2012, 43(3):624-633.
• [21]Dejnirattisai W, Jumnainsong A, Onsirisakul N, Fitton P, Vasanawathana S, Limpitikul W, Puttikhunt C, Edwards C, Duangchinda T, Supasa S, Chawansuntati K, Malasit P, Mongkolsapaya J, Screaton G: Cross-reacting antibodies enhance dengue virus infection in humans. Science 2010, 328(5979):745-748.
• [22]Guzman MG, Kouri G, Valdes L, Bravo J, Alvarez M, Vazques S, Delgado I, Halstead SB: Epidemiologic studies on Dengue in Santiago de Cuba, 1997. Am J Epidemiol 2000, 152(9):793-799. discussion 804
• [23]Sangkawibha N, Rojanasuphot S, Ahandrik S, Viriyapongse S, Jatanasen S, Salitul V, Phanthumachinda B, Halstead SB: Risk factors in dengue shock syndrome: a prospective epidemiologic study in Rayong, Thailand. I. The 1980 outbreak. Am J Epidemiol 1984, 120(5):653-669.
• [24]Myat Thu H, Lowry K, Jiang L, Hlaing T, Holmes EC, Aaskov J: Lineage extinction and replacement in dengue type 1 virus populations are due to stochastic events rather than to natural selection. Virology 2005, 336(2):163-172.
• [25]Wittke V, Robb TE, Thu HM, Nisalak A, Nimmannitya S, Kalayanrooj S, Vaughn DW, Endy TP, Holmes EC, Aaskov JG: Extinction and rapid emergence of strains of dengue 3 virus during an interepidemic period. Virology 2002, 301(1):148-156.
• [26]Bennett SN, Holmes EC, Chirivella M, Rodriguez DM, Beltran M, Vorndam V, Gubler DJ, McMillan WO: Selection-driven evolution of emergent dengue virus. Mol Biol Evol 2003, 20(10):1650-1658.
• [27]Carrillo-Valenzo E, Danis-Lozano R, Velasco-Hernandez JX, Sanchez-Burgos G, Alpuche C, Lopez I, Rosales C, Baronti C, de Lamballerie X, Holmes EC, Ramos-Castaneda J: Evolution of dengue virus in Mexico is characterized by frequent lineage replacement. Arch Virol 2010, 155(9):1401-1412.
• [28]Anderson JR, Rico-Hesse R: Aedes aegypti vectorial capacity is determined by the infecting genotype of dengue virus. Am J Trop Med Hyg 2006, 75(5):886-892.
• [29]Armstrong PM, Rico-Hesse R: Efficiency of dengue serotype 2 virus strains to infect and disseminate in Aedes aegypti. Am J Trop Med Hyg 2003, 68(5):539-544.
• [30]Hanley KA, Nelson JT, Schirtzinger EE, Whitehead SS, Hanson CT: Superior infectivity for mosquito vectors contributes to competitive displacement among strains of dengue virus. BMC Ecol 2008, 8:1. BioMed Central Full Text
• [31]Lambrechts L, Fansiri T, Pongsiri A, Thaisomboonsuk B, Klungthong C, Richardson JH, Ponlawat A, Jarman RG, Scott TW: Dengue-1 virus clade replacement in Thailand associated with enhanced mosquito transmission. J Virol 2012, 86(3):1853-1861.
• [32]Adams B, Holmes EC, Zhang C, Mammen MP Jr, Nimmannitya S, Kalayanarooj S, Boots M: Cross-protective immunity can account for the alternating epidemic pattern of dengue virus serotypes circulating in Bangkok. Proc Natl Acad Sci U S A 2006, 103(38):14234-14239.
• [33]Teoh BT, Sam SS, Abd-Jamil J, AbuBakar S: Isolation of ancestral sylvatic dengue virus type 1, Malaysia. Emerg Infect Dis 2010, 16(11):1783-1785.
• [34]A-Nuegoonpipat A, Berlioz-Arthaud A, Chow V, Endy T, Lowry K, le Mai Q, Ninh TU, Pyke A, Reid M, Reynes JM, Su Yun ST, Thu HM, Wong SS, Holmes EC, Aaskov J: Sustained transmission of dengue virus type 1 in the Pacific due to repeated introductions of different Asian strains. Virology 2004, 329(2):505-512.
• [35]Schreiber MJ, Holmes EC, Ong SH, Soh HS, Liu W, Tanner L, Aw PP, Tan HC, Ng LC, Leo YS, Low JG, Ong A, Ooi EE, Vasudevan SG, Hibberd ML: Genomic epidemiology of a dengue virus epidemic in urban Singapore. J Virol 2009, 83(9):4163-4173.
• [36]Ito M, Yamada K, Takasaki T, Pandey B, Nerome R, Tajima S, Morita K, Kurane I: Phylogenetic analysis of dengue viruses isolated from imported dengue patients: possible aid for determining the countries where infections occurred. J Travel Med 2007, 14(4):233-244.
• [37]Yamanaka A, Mulyatno KC, Susilowati H, Hendrianto E, Ginting AP, Sary DD, Rantam FA, Soegijanto S, Konishi E: Displacement of the predominant dengue virus from type 2 to type 1 with a subsequent genotype shift from IV to I in Surabaya, Indonesia 2008–2010. PLoS One 2011, 6(11):e27322.
• [38]Tissera HA, Ooi EE, Gubler DJ, Tan Y, Logendra B, Wahala WM, de Silva AM, Abeysinghe MR, Palihawadana P, Gunasena S, Tam CC, Amarasinghe A, Letson GW, Margolis HS, De Silva AD: New dengue virus type 1 genotype in Colombo, Sri Lanka. Emerg Infect Dis 2011, 17(11):2053-2055.
• [39]Jeong YE, Kim YH, Cho JE, Han MG, Ju YR: Identification of dengue type 1 virus (DENV-1) in Koreans traveling abroad. Public Health Res Perspect 2011, 2(1):34-40.
• [40]Twiddy SS, Farrar JJ, Vinh Chau N, Wills B, Gould EA, Gritsun T, Lloyd G, Holmes EC: Phylogenetic relationships and differential selection pressures among genotypes of dengue-2 virus. Virology 2002, 298(1):63-72.
• [41]Migration issues in the Asia Pacific: Issues paper from Malaysia. http://www.unesco.org/most/apmrnwp9.htm webcite
• [42]Sittisombut N, Sistayanarain A, Cardosa MJ, Salminen M, Damrongdachakul S, Kalayanarooj S, Rojanasuphot S, Supawadee J, Maneekarn N: Possible occurrence of a genetic bottleneck in dengue serotype 2 viruses between the 1980 and 1987 epidemic seasons in Bangkok. Thailand. Am J Trop Med Hyg 1997, 57(1):100-108.
• [43]Lee KS, Lo S, Tan SS, Chua R, Tan LK, Xu H, Ng LC: Dengue virus surveillance in Singapore reveals high viral diversity through multiple introductions and in situ evolution. Infect Genet Evol 2012, 12(1):77-85.
• [44]Modis Y, Ogata S, Clements D, Harrison SC: A ligand-binding pocket in the dengue virus envelope glycoprotein. Proc Natl Acad Sci U S A 2003, 100(12):6986-6991.
• [45]Goncalvez AP, Escalante AA, Pujol FH, Ludert JE, Tovar D, Salas RA, Liprandi F: Diversity and evolution of the envelope gene of dengue virus type 1. Virology 2002, 303(1):110-119.
• [46]Modis Y, Ogata S, Clements D, Harrison SC: Structure of the dengue virus envelope protein after membrane fusion. Nature 2004, 427(6972):313-319.
• [47]Wahala WM, Silva AM: The human antibody response to dengue virus infection. Viruses 2011, 3(12):2374-2395.
• [48]Lee E, Weir RC, Dalgarno L: Changes in the dengue virus major envelope protein on passaging and their localization on the three-dimensional structure of the protein. Virology 1997, 232(2):281-290.
• [49]Butrapet S, Childers T, Moss KJ, Erb SM, Luy BE, Calvert AE, Blair CD, Roehrig JT, Huang CY: Amino acid changes within the E protein hinge region that affect dengue virus type 2 infectivity and fusion. Virology 2011, 413(1):118-127.
• [50]Twiddy SS, Holmes EC, Rambaut A: Inferring the rate and time-scale of dengue virus evolution. Mol Biol Evol 2003, 20(1):122-129.
• [51]Jenkins GM, Rambaut A, Pybus OG, Holmes EC: Rates of molecular evolution in RNA viruses: a quantitative phylogenetic analysis. J Mol Evol 2002, 54(2):156-165.
• [52]Holmes EC: Patterns of intra- and interhost nonsynonymous variation reveal strong purifying selection in dengue virus. J Virol 2003, 77(20):11296-11298.
• [53]Martins VE, Alencar CH, Kamimura MT, de Carvalho Araujo FM, De Simone SG, Dutra RF, Guedes MI: Occurrence of natural vertical transmission of dengue-2 and dengue-3 viruses in Aedes aegypti and Aedes albopictus in Fortaleza, Ceara. Brazil. PLoS One 2012, 7(7):e41386.
• [54]Mulyatno KC, Yamanaka A, Yotopranoto S, Konishi E: Vertical transmission of dengue virus in Aedes aegypti collected in Surabaya, Indonesia, during 2008–2011. Jpn J Infect Dis 2012, 65(3):274-276.
• [55]Rohani A, Suzilah I, Malinda M, Anuar I, Mohd Mazlan I, Salmah Maszaitun M, Topek O, Tanrang Y, Ooi SC, Rozilawati H, Lee HL: Aedes larval population dynamics and risk for dengue epidemics in Malaysia. Trop Biomed 2011, 28(2):237-248.
• [56]Yusoff N, Budin H, Ismail S: Simulation of population dynamics of Aedes aegypti using climate dependent model. World Acad Sci Eng Technol 2012, 62:477-482.
• [57]Masel J: Genetic drift. Curr Biol 2011, 21(20):R837-R838.
• [58]Ohta T: Evolution by nearly-neutral mutations. Genetica 1998, 102–103(1–6):83-90.
• [59]Drummond AJ, Rambaut A: BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 2007, 7:214. BioMed Central Full Text
• [60]Posada D: jModelTest: phylogenetic model averaging. Mol Biol Evol 2008, 25(7):1253-1256.
• [61]Pond SL, Frost SD: Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 2005, 21(10):2531-2533.
• [62]Wong SS, Abd-Jamil J, Abubakar S: Antibody neutralization and viral virulence in recurring dengue virus type 2 outbreaks. Viral Immunol 2007, 20(3):359-368.
• [63]Clarke DH, Casals J: Techniques for hemagglutination and hemagglutination-inhibition with arthropod-borne viruses. Am J Trop Med Hyg 1958, 7(5):561-573.
• [64]World Health Organization: Laboratory diagnosis. In Dengue haemorrhagic fever: diagnosis, treatment and control. 2nd edition. Geneva: World Health Organization; 1997:34-47.
• [65]Okuno Y, Fukunaga T, Srisupaluck S, Fukai K: A modified PAP (peroxidase-anti-peroxidase) staining technique using sera from patients with dengue hemorrhagic fever (DHF): 4 step PAP staining technique. Biken J 1979, 22(4):131-135.