Chapter 1 The History and Evolution of Human Dengue Emergence

doi:10.1016/S0065-3527(08)00401-6

Advances in Virus Research

Volume 72, 2008, Pages 1-76

https://doi.org/10.1016/S0065-3527(08)00401-6 Get rights and content

Abstract

Dengue viruses (DENV) are the most important human arboviral pathogens. Transmission in tropical and subtropical regions of the world includes a sylvatic, enzootic cycle between nonhuman primates and arboreal mosquitoes of the genus Aedes, and an urban, endemic/epidemic cycle principally between Aedes aegypti, a mosquito that exploits peridomestic water containers as its larval habitats, and human reservoir hosts that are preferred for blood feeding. Genetic studies suggest that all four serotypes of endemic/epidemic DENV evolved independently from ancestral, sylvatic viruses and subsequently became both ecologically and evolutionarily distinct. The independent evolution of these four serotypes was accompanied by the expansion of the sylvatic progenitors' host range in Asia to new vectors and hosts, which probably occurred gradually over a period of several hundred years. Although many emerging viral pathogens adapt to human replication and transmission, the available evidence indicates that adaptation to humans is probably not a necessary component of sylvatic DENV emergence. These findings imply that the sylvatic DENV cycles in Asia and West Africa will remain a potential source of re‐emergence. Sustained urban vector control programs and/or human vaccination will be required to control DEN because the enzootic vectors and primate reservoir hosts are not amenable to interventions.

Section snippets

Introduction to Flaviviruses

Dengue viruses (DENV) are members of the genus Flavivirus in the Family Flaviviridae. Flaviviruses are single‐stranded RNA viruses of positive polarity and most, but not all, require hematophagous arthropods (mosquitoes or ticks) to complete their horizontal transmission cycle. They are responsible for a broad spectrum of pathogenic manifestations in humans, domestic animals, and birds (Heinz et al., 2000). Flaviviruses are widely distributed nearly throughout the world, except Antarctica. More

Classification of dengue viruses

DENV is considered a species within the genus Flavivirus (family Flaviviridae) and includes four distinct but antigenically related serotypes (DENV‐1, ‐2, ‐3, and ‐4) in DEN antigenic complex (Calisher et al., 1989). Of the flaviviruses, DENV are among the most restricted with regard to their natural vertebrate host range, which is believed to include only primates. Currently, all four DENV serotypes can be found in nearly all urban and peri‐urban environments throughout the tropics and

History of dengue virus as a human pathogen

The geographic site of origin of DENV has been a subject of intense speculation; some argue for an African origin due to the same origin of the principal vector, Ae. aegypti (Christophers, 1960, Edwards, 1932). However the ecological and serological work of Smith and Rudnick (Rudnick and Lim, 1986, Smith, 1956), the relative insusceptibility to infection to DENV infection of the ancestral Ae. aegypti formosus from Africa (Diallo et al., 2005) and phylogenetic analyses (Wang et al., 2000) point

DENV evolutionary relationships—origins and emergence

Gubler's (Gubler, 1997) hypothesis that endemic DENV evolved from sylvatic progenitors has been the subject of intense discussion and speculation. As mentioned above, sylvatic DENV cycles occur in the forests of West Africa and Southeast Asia involving only the DENV‐2 serotype in the former region, whereas in the latter all four serotypes may be represented. Virus maintenance in both regions involves sylvatic Aedes spp. mosquito vectors, and presumably non‐human primates serving as reservoir

Epidemics and human contact

Smith (Smith, 1956) and Rudnick (Rudnick, 1986), based on their studies of DENV ecology and seroprevalence in the Malay peninsula, hypothesized that the rural population, especially those living in close proximity to forested and rubber plantation areas, were exposed periodically to sylvatic DENV. As described above in the ‘transmission cycles’ section, all of the sylvatic DENV isolates were obtained from sentinel monkeys or Ae. niveus species mosquito pools, collected within sylvan environs (

Acknowledgments

We thank Edward C. Holmes for helpful advice with the phylogenetic methods and divergence time estimates. NV was supported by the Centers for Disease Control and Prevention Fellowship Training Program in Vector‐Borne Infectious Diseases, T01/CCT622892.

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Dengue virus (DENV) is a prevalent mosquito-transmitted human pathogen, causing about 100 million cases of acute dengue fever and 21,000 deaths annually worldwide. Therapeutic neutralizing antibodies against dengue virus might be effective to treat severe dengue fever. Here, we showed that human monoclonal antibody (HMAb) 9C7 bound to all four intact serotypes of DENV but not to the recombinant envelope protein, suggesting HMAb 9C7 recognized a conformational epitope of the envelope protein. Taken together our results suggested that HMAb 9C7 neutralized all four serotypes of DENV in vitro and, for DENV-1, indicated activity at the pre- and post-attachment steps in the viral life cycle. HMAb 9C7 potently protected suckling mice from lethal challenge with all four serotypes of DENV. FcγRII-mediated uptake of immune complexes and antibody-dependent enhancement at low doses of the antibody were abolished by two Leu-to-Ala (9C7-LALA) mutations or deletion of nine amino acids (9C7-9del) in HMAb 9C7 Fc. Therefore, HMAb 9C7 represented a promising prophylactic and therapeutic agent against all four serotypes of DENV.
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Chapter 1 The History and Evolution of Human Dengue Emergence

Abstract

Section snippets

Introduction to Flaviviruses

Classification of dengue viruses

History of dengue virus as a human pathogen

DENV evolutionary relationships—origins and emergence

Epidemics and human contact

Acknowledgments

Virology

Trans. R. Soc. Trop. Med. Hyg.

Virology

Virology

J. Virol. Methods

Trans. R. Soc. Trop. Med. Hyg.

Arch. Pediatr.

Trans. R. Soc. Trop. Med. Hyg.

Adv. Virus Res.

Cytokine

Lancet

Clin. Microbiol. Infect.

FEMS Immunol. Med. Microbiol.

Trans. R. Soc. Trop. Med. Hyg.

Trans. R. Soc. Trop. Med. Hyg.

Arch. Med. Res.

Trans. R. Soc. Trop. Med. Hyg.

Serologically defined linear epitopes in the envelope protein of dengue 2 (Jamaica strain 1409)

Arch. Virol.

Multiple recombinant dengue type 1 viruses in an isolate from a dengue patient

J. Gen. Virol.

Emergence of dengue virus type 4 genotype IIA in Malaysia

J. Gen. Virol.

Correlation of E protein binding with cell susceptibility to dengue 4 virus infection

J. Gen. Virol.

Cross‐reactive T‐cell responses to the nonstructural regions of dengue viruses among dengue fever and dengue hemorrhagic fever patients in Malaysia

Clin. Vaccine Immunol.

Concurrent infection with dengue virus type‐2 and DENV‐3 in a patient from Ceara, Brazil

Mem. Inst. Oswaldo Cruz

Differential susceptibility of Aedes aegypti to infection by the American and Southeast Asian genotypes of dengue type 2 virus

Vector Borne Zoonotic Dis.

Efficiency of dengue serotype 2 virus strains to infect and disseminate in Aedes aegypti

Am. J. Trop. Med. Hyg.

Experimental investigations regarding the etiology of dengue fever

J. Infect. Dis.

West Nile virus epidemic in horses, Tuscany region, Italy

Emerg. Infect. Dis.

Dengue virus infection of human endothelial cells leads to chemokine production, complement activation, and apoptosis

J. Immunol.

Vascular leakage in severe dengue virus infections: A potential role for the nonstructural viral protein NS1 and complement

J. Infect. Dis.

Predominance of the DEN‐3 genotype during the recent dengue outbreak in Bangladesh

Southeast Asian J. Trop. Med. Public Health

Bat salivary gland virus carrier state in a naturally infected Mexican freetail bat

Am. J. Trop. Med. Hyg.

Investigations on an outbreak of dengue in Delhi in 1967

Indian J. Med. Res.

Fatal hemorrhagic disease and shock associated with primary dengue infection on a Pacific island

Am. J. Trop. Med. Hyg.

The distribution of ‘Stegomyia fasciata’ in India, with remarks on dengue and yellow fever

Indian J. Med. Res.

Recent virological studies on haemorrhagic fever and other arthropod‐borne virus infections in the Philippines

J. Trop. Med. Hyg.

RNA recombination between persisting pestivirus and a vaccine strain: Generation of cytopathogenic virus and induction of lethal disease

J. Virol.

[The clinico‐epidemiological characteristics of Omsk hemorrhagic fever in 1988–1992]

Zh. Mikrobiol. Epidemiol. Immunobiol.

Selection‐driven evolution of emergent dengue virus

Mol. Biol. Evol.

Dengue fever in humanized NOD/SCID mice

J. Virol.

Primary human splenic macrophages, but not T or B cells, are the principal target cells for dengue virus infection in vitro

J. Virol.

Recombinant, live‐attenuated tetravalent dengue virus vaccine formulations induce a balanced, broad, and protective neutralizing antibody response against each of the four serotypes in rhesus monkeys

J. Virol.

Increased production of interleukin‐8 in primary human monocytes and in human epithelial and endothelial cell lines after dengue virus challenge

J. Virol.

Serological evidence of dengue fever among refugees, Hargeysa, Somalia

J. Med. Virol.

Infection enhancement of dengue type 2 virus in the U‐937 human monocyte cell line by antibodies to flavivirus cross‐reactive determinants

Infect. Immun.