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Chapter 54 : Alphaviruses

Authors: David W. Smith, John S. Mackenzie, Scott C. Weaver
Content Type: Reference
Publication Year: 2009

Category: Viruses and Viral Pathogenesis

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Abstract:

The alphaviruses are principally mosquito-borne, positive-strand RNA viruses in the family that exhibit a broad range of pathogenicity in humans and animals. The replication complexes of alphaviruses are associated with cytoplasmic membranes, and the main determinant of membrane attachment seems to be nsP1, which is hydrophobically modified by palmitoylation of cysteine residues. In humans, an age-dependent susceptibility of infants and the elderly to central nervous system (CNS) infection has been observed epidemiologically, although its pathogenesis has not been elucidated. Immature mouse neurons infected with Sindbis Virus (SINV) or Semliki Forest Virus (SFV) die of caspase-dependent apoptosis, while mature neurons survive by producing factors inhibiting virus-induced apoptosis. Apoptosis is induced at the time of alphavirus fusion with the cell membrane, and virus replication is not required. Mayaro virus (MAYV) is the principal New World representative of alphaviruses within the SFV complex. The epidemiological pattern is explained by the forest cycle of viral transmission, probably between mosquitoes and wild vertebrates, including monkeys and marmosets, analogous to the sylvatic cycle of yellow fever. The majority of infections with the arthritogenic alphaviruses are benign but temporarily debilitating. Barmah Forest virus (BFV), named after the site in northern Victoria where it was first isolated from mosquitoes, is antigenically distinct from other alphaviruses, including River virus (RRV) and SINV, that are also found in Australia. Alphaviruses principally are maintained in zoonotic transmission cycles in natural habitats.

Citation: Smith D, Mackenzie J, Weaver S. 2009. Alphaviruses, p 1241-1274. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815981.ch54

Key Concept Ranking

Eastern equine encephalitis virus
0.5085156
Venezuelan equine encephalitis virus
0.5085156
Eastern equine encephalitis virus
0.5085156
Venezuelan equine encephalitis virus
0.5085156
Eastern equine encephalitis virus
0.5085156
Venezuelan equine encephalitis virus
0.5085156
Tumor Necrosis Factor alpha
0.44615784
0.5085156
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Alphaviruses
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Citation: Smith D, Mackenzie J, Weaver S. 2009. Alphaviruses, p 1241-1274. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815981.ch54
/content/10.1128/9781555815981.ch54.ch54fig01
FIGURE 1
Genetic relationship of alphavirus species and some major subtypes (shown in parentheses) based on partial sequences of E1 glycoprotein gene. The main antigenic complexes are indicated on the right. The dotted line represents the recombination event between SINV and EEEV. Numbers on the lines indicate bootstrap values for clades to the right using the neighbor-joining (numbers above branches) or Bayesian (numbers below line) method. (Reprinted from reference with permission.)
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Image of FIGURE 1
FIGURE 1

Genetic relationship of alphavirus species and some major subtypes (shown in parentheses) based on partial sequences of E1 glycoprotein gene. The main antigenic complexes are indicated on the right. The dotted line represents the recombination event between SINV and EEEV. Numbers on the lines indicate bootstrap values for clades to the right using the neighbor-joining (numbers above branches) or Bayesian (numbers below line) method. (Reprinted from reference with permission.)

Citation: Smith D, Mackenzie J, Weaver S. 2009. Alphaviruses, p 1241-1274. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815981.ch54
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FIGURE 2
RRV. (Left) Cryoelectron microscopic image reconstruction of RRV showing the flower-like envelope protein spikes, virion membrane, and nucleocapsid core. (Right) Relationships of spike and capsid proteins and virion RNA. (Courtesy of R. J. Kuhn.)
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Image of FIGURE 2
FIGURE 2

RRV. (Left) Cryoelectron microscopic image reconstruction of RRV showing the flower-like envelope protein spikes, virion membrane, and nucleocapsid core. (Right) Relationships of spike and capsid proteins and virion RNA. (Courtesy of R. J. Kuhn.)

Citation: Smith D, Mackenzie J, Weaver S. 2009. Alphaviruses, p 1241-1274. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815981.ch54
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FIGURE 3
Schematic diagram of alphavirus genome [positive (⊕) sense RNA with poly(A) (A) tail and 5′ terminal cap (CAP); viral complementary RNA (vcRNA) of negative (⊖) sense; and subgenomic mRNA of positive sense]. Viral nonstructural proteins are translated from the 5′ two-thirds region of the genome, yielding polyprotein intermediates and nonstructural proteins nsP1 to nsP4. RNA is replicated into negative-sense RNA templates and transcribed into 26S subgenomic RNA. Cotranslational processing of the subgenomic mRNA yields the three principal structural proteins: capsid and envelope glycoproteins (E1 and E2). ORF, open reading frame; nt, nucleotide.
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Image of FIGURE 3
FIGURE 3

Schematic diagram of alphavirus genome [positive (⊕) sense RNA with poly(A) (A) tail and 5′ terminal cap (CAP); viral complementary RNA (vcRNA) of negative (⊖) sense; and subgenomic mRNA of positive sense]. Viral nonstructural proteins are translated from the 5′ two-thirds region of the genome, yielding polyprotein intermediates and nonstructural proteins nsP1 to nsP4. RNA is replicated into negative-sense RNA templates and transcribed into 26S subgenomic RNA. Cotranslational processing of the subgenomic mRNA yields the three principal structural proteins: capsid and envelope glycoproteins (E1 and E2). ORF, open reading frame; nt, nucleotide.

Citation: Smith D, Mackenzie J, Weaver S. 2009. Alphaviruses, p 1241-1274. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815981.ch54
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FIGURE 4
After binding to the cell membrane (step 1), virions are taken up in endocytic vesicles (steps 2 and 3). The virion and vesicular membranes fuse, releasing the nucleocapsid (step 4). The viral nucleocapsid binds to a ribosome (step 5) and is uncoated, freeing viral RNA (step 6) from the individual capsid (gray dots). Positive-sense viral RNA (heavy line) is replicated (step 7), producing complementary negative-sense RNA (gray line) (step 8), which in turn is transcribed to full-length genomic positive-sense RNA (step 9) or subgenomic RNA (step 10). Nonstructural proteins (nsp) are translated from genomic RNA. Subgenomic RNA is translated to produce capsid proteins (black dots) and envelope proteins, which are modified before insertion into the cell membrane (gray bars) (step 11). Genomic RNA is packaged with capsid proteins into nucleocapsid cores (step 12); capsid and E2 proteins associate (step 13) prior to viral budding (step 14).
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Image of FIGURE 4
FIGURE 4

After binding to the cell membrane (step 1), virions are taken up in endocytic vesicles (steps 2 and 3). The virion and vesicular membranes fuse, releasing the nucleocapsid (step 4). The viral nucleocapsid binds to a ribosome (step 5) and is uncoated, freeing viral RNA (step 6) from the individual capsid (gray dots). Positive-sense viral RNA (heavy line) is replicated (step 7), producing complementary negative-sense RNA (gray line) (step 8), which in turn is transcribed to full-length genomic positive-sense RNA (step 9) or subgenomic RNA (step 10). Nonstructural proteins (nsp) are translated from genomic RNA. Subgenomic RNA is translated to produce capsid proteins (black dots) and envelope proteins, which are modified before insertion into the cell membrane (gray bars) (step 11). Genomic RNA is packaged with capsid proteins into nucleocapsid cores (step 12); capsid and E2 proteins associate (step 13) prior to viral budding (step 14).

Citation: Smith D, Mackenzie J, Weaver S. 2009. Alphaviruses, p 1241-1274. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815981.ch54
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FIGURE 5
Reported cases of EEE among humans in the United States, 1964 to 2006. The reported incidence is highest in Florida, where equine cases are reported perennially from the northeastern coast and throughout the peninsula. Relatively constant inland foci of transmission have been identified in upstate New York, southwestern Michigan, northeastern Indiana, and southcentral Georgia. In Massachusetts, human cases have been reported almost entirely from the eastern counties and in New Jersey from the southern counties. (Reprinted from the Centers for Disease Control and Prevention at http://www.cdc.gov/ncidod/dvbid/arbor/arbocase.htm.)
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FIGURE 5

Reported cases of EEE among humans in the United States, 1964 to 2006. The reported incidence is highest in Florida, where equine cases are reported perennially from the northeastern coast and throughout the peninsula. Relatively constant inland foci of transmission have been identified in upstate New York, southwestern Michigan, northeastern Indiana, and southcentral Georgia. In Massachusetts, human cases have been reported almost entirely from the eastern counties and in New Jersey from the southern counties. (Reprinted from the Centers for Disease Control and Prevention at http://www.cdc.gov/ncidod/dvbid/arbor/arbocase.htm.)

Citation: Smith D, Mackenzie J, Weaver S. 2009. Alphaviruses, p 1241-1274. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815981.ch54
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FIGURE 6
Reported cases of EEE (broken line) and WEE (solid line), United States, 1964 to 2006. (Reprinted from the Centers for Disease Control and Prevention at http://www.cdc.gov/ncidod/dvbid/arbor/arbocase.htm.)
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FIGURE 6

Reported cases of EEE (broken line) and WEE (solid line), United States, 1964 to 2006. (Reprinted from the Centers for Disease Control and Prevention at http://www.cdc.gov/ncidod/dvbid/arbor/arbocase.htm.)

Citation: Smith D, Mackenzie J, Weaver S. 2009. Alphaviruses, p 1241-1274. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815981.ch54
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FIGURE 7
Schematic diagram of the EEE transmission cycle; solid lines show known portions, and broken lines show speculative portions. The principal enzootic mosquito vector, transmits the virus among birds and occasionally initiates an outbreak among pheasants or other captive birds. Various other species bridge the enzootic cycle to infect humans and horses, which are dead-end hosts; the principal species include found in salt marsh coastal habitat; associated with open meadows and flooded ground pools; associated with woodland pools; and found in open freshwater swamps with emerging vegetation. The viral overwintering mechanism is unknown but potentially includes vertically infected mosquitoes, persistently infected birds, and other vertebrates.
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Image of FIGURE 7
FIGURE 7

Schematic diagram of the EEE transmission cycle; solid lines show known portions, and broken lines show speculative portions. The principal enzootic mosquito vector, transmits the virus among birds and occasionally initiates an outbreak among pheasants or other captive birds. Various other species bridge the enzootic cycle to infect humans and horses, which are dead-end hosts; the principal species include found in salt marsh coastal habitat; associated with open meadows and flooded ground pools; associated with woodland pools; and found in open freshwater swamps with emerging vegetation. The viral overwintering mechanism is unknown but potentially includes vertically infected mosquitoes, persistently infected birds, and other vertebrates.

Citation: Smith D, Mackenzie J, Weaver S. 2009. Alphaviruses, p 1241-1274. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815981.ch54
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FIGURE 8
Reported cases of EEE and WEE by month, United States, 1972 to 1989. (Data from the Centers for Disease Control and Prevention at http://www.cdc.gov/ncidod/dvbid/arbor/arbocase.htm.)
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Image of FIGURE 8
FIGURE 8

Reported cases of EEE and WEE by month, United States, 1972 to 1989. (Data from the Centers for Disease Control and Prevention at http://www.cdc.gov/ncidod/dvbid/arbor/arbocase.htm.)

Citation: Smith D, Mackenzie J, Weaver S. 2009. Alphaviruses, p 1241-1274. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815981.ch54
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FIGURE 9
Reported cases of WEE among humans in the United States, 1964 to 2006. (Reprinted from the Centers for Disease Control and Prevention at http://www.cdc.gov/ncidod/dvbid/arbor/arbocase.htm.)
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Image of FIGURE 9
FIGURE 9

Reported cases of WEE among humans in the United States, 1964 to 2006. (Reprinted from the Centers for Disease Control and Prevention at http://www.cdc.gov/ncidod/dvbid/arbor/arbocase.htm.)

Citation: Smith D, Mackenzie J, Weaver S. 2009. Alphaviruses, p 1241-1274. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815981.ch54
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FIGURE 10
Geographic distribution of VEE epizootics and sylvatic viral subtypes.
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Image of FIGURE 10
FIGURE 10

Geographic distribution of VEE epizootics and sylvatic viral subtypes.

Citation: Smith D, Mackenzie J, Weaver S. 2009. Alphaviruses, p 1241-1274. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815981.ch54
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FIGURE 11
(A) Sylvatic VEEVs circulate continuously in silent tropical and subtropical foci among mosquitoes and small mammals or aquatic birds. Humans (e.g., soldiers on jungle bivouacs) are infected when they chance upon transmission foci. Bridging vectors (e.g., ) that feed on viremic vertebrates in a sylvatic focus can carry the virus to nearby areas of human activity. (B) In contrast to the continuous cycling of sylvatic VEEV subtypes, until recently, epizootic VEEV had never been isolated except during periodic outbreaks. Once introduced, epizootic viruses are rapidly amplified among equines (horses and burros). Equines develop high viremia levels, so various mosquito species can function as biological vectors (only some important species are shown) and other biting insects, such as blackflies, can spread the virus mechanically. Humans develop illness with high viremia levels but probably have an insignificant role, if any, in viral amplification. Transmission declines as susceptible equines are exhausted by natural infection or immunization. It is speculated that epizootic IC viruses arise by mutation from sylvatic ID viruses; the subpopulation circulates in a sylvatic cycle and under appropriate conditions is amplified, leading to epizootic and epidemic spread.
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Image of FIGURE 11
FIGURE 11

(A) Sylvatic VEEVs circulate continuously in silent tropical and subtropical foci among mosquitoes and small mammals or aquatic birds. Humans (e.g., soldiers on jungle bivouacs) are infected when they chance upon transmission foci. Bridging vectors (e.g., ) that feed on viremic vertebrates in a sylvatic focus can carry the virus to nearby areas of human activity. (B) In contrast to the continuous cycling of sylvatic VEEV subtypes, until recently, epizootic VEEV had never been isolated except during periodic outbreaks. Once introduced, epizootic viruses are rapidly amplified among equines (horses and burros). Equines develop high viremia levels, so various mosquito species can function as biological vectors (only some important species are shown) and other biting insects, such as blackflies, can spread the virus mechanically. Humans develop illness with high viremia levels but probably have an insignificant role, if any, in viral amplification. Transmission declines as susceptible equines are exhausted by natural infection or immunization. It is speculated that epizootic IC viruses arise by mutation from sylvatic ID viruses; the subpopulation circulates in a sylvatic cycle and under appropriate conditions is amplified, leading to epizootic and epidemic spread.

Citation: Smith D, Mackenzie J, Weaver S. 2009. Alphaviruses, p 1241-1274. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815981.ch54
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FIGURE 12
Reported chikungunya epidemics by year.
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FIGURE 12

Reported chikungunya epidemics by year.

Citation: Smith D, Mackenzie J, Weaver S. 2009. Alphaviruses, p 1241-1274. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815981.ch54
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FIGURE 13
Small papular lesions seen in Sindbis (Ockelbo) fever. (Courtesy of B. Niklasson.)
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FIGURE 13

Small papular lesions seen in Sindbis (Ockelbo) fever. (Courtesy of B. Niklasson.)

Citation: Smith D, Mackenzie J, Weaver S. 2009. Alphaviruses, p 1241-1274. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815981.ch54
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FIGURE 14
Notifications and notification rates of RRV infections, Australia, 2005–2006, by Statistical Division of residence. (Reprinted from reference with permission.)
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Image of FIGURE 14
FIGURE 14

Notifications and notification rates of RRV infections, Australia, 2005–2006, by Statistical Division of residence. (Reprinted from reference with permission.)

Citation: Smith D, Mackenzie J, Weaver S. 2009. Alphaviruses, p 1241-1274. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815981.ch54
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FIGURE 15
Crude annual rate of BFV and RRV infection notifications, Australia, 1 July 1991 to 30 June 2006, by season of onset. (Reprinted from reference with permission.)
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Image of FIGURE 15
FIGURE 15

Crude annual rate of BFV and RRV infection notifications, Australia, 1 July 1991 to 30 June 2006, by season of onset. (Reprinted from reference with permission.)

Citation: Smith D, Mackenzie J, Weaver S. 2009. Alphaviruses, p 1241-1274. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815981.ch54
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References

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Tables

Alphaviruses
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Citation: Smith D, Mackenzie J, Weaver S. 2009. Alphaviruses, p 1241-1274. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815981.ch54
/content/10.1128/9781555815981.ch54.ch54tab01
TABLE 1
Selected characteristics of alphaviruses
Generic image for table
TABLE 1

Selected characteristics of alphaviruses

Citation: Smith D, Mackenzie J, Weaver S. 2009. Alphaviruses, p 1241-1274. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815981.ch54
/content/10.1128/9781555815981.ch54.ch54tab02
TABLE 2
Alphavirus proteins
Generic image for table
TABLE 2

Alphavirus proteins

Citation: Smith D, Mackenzie J, Weaver S. 2009. Alphaviruses, p 1241-1274. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815981.ch54
/content/10.1128/9781555815981.ch54.ch54tab03
TABLE 3
Initial diagnosis of diseases ultimately proven by laboratory test to be either WEE or St. Louis encephalitis
Generic image for table
TABLE 3

Initial diagnosis of diseases ultimately proven by laboratory test to be either WEE or St. Louis encephalitis

Citation: Smith D, Mackenzie J, Weaver S. 2009. Alphaviruses, p 1241-1274. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815981.ch54
/content/10.1128/9781555815981.ch54.ch54tab04
TABLE 4
Precautions to minimize exposure to mosquitoes and ticks
Generic image for table
TABLE 4

Precautions to minimize exposure to mosquitoes and ticks

Citation: Smith D, Mackenzie J, Weaver S. 2009. Alphaviruses, p 1241-1274. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815981.ch54

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