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Simian immunodeficiency virus

Simian immunodeficiency virus (SIV) is a species of retrovirus that cause persistent infections in at least 45 species of non-human primates.[1][2] Based on analysis of strains found in four species of monkeys from Bioko Island, which was isolated from the mainland by rising sea levels about 11,000 years ago, it has been concluded that SIV has been present in monkeys and apes for at least 32,000 years, and probably much longer.[3][4]

Simian immunodeficiency virus
SIV virion model obtained with cryo-electron microscopy scanning
Virus classification Edit this classification
(unranked): Virus
Realm: Riboviria
Kingdom: Pararnavirae
Phylum: Artverviricota
Class: Revtraviricetes
Order: Ortervirales
Family: Retroviridae
Genus: Lentivirus
Species:
Simian immunodeficiency virus

Virus strains from three of these primate species, SIVsmm in sooty mangabeys, SIVgor in gorillas and SIVcpz in chimpanzees, are believed to have crossed the species barrier into humans, resulting in HIV-2 and HIV-1 respectively, the two HIV viruses. The most likely route of transmission of HIV-1 to humans involves contact with the blood of chimps and gorillas that are often hunted for bushmeat in Africa. Four subtypes of HIV-1 (M, N, O, and P) likely arose through four separate transmissions of SIV to humans, and the resulting HIV-1 group M strain most commonly infects people worldwide.[5][6] Therefore, it is theorized that SIV may have previously crossed the species barrier into human hosts multiple times throughout history, but it was not until recently, after the advent of modern transportation and global commuterism, that it finally took hold, spreading beyond localized decimations of a few individuals or single small tribal populations.

Unlike HIV-1 and HIV-2 infections in humans, SIV infections in their natural simian non-human hosts appear in many cases to be non-pathogenic due to evolutionary adaptation of the hosts to the virus. Extensive studies in sooty mangabeys have established that SIVsmm infection does not cause any disease in these primates, despite high levels of circulating virus. Regulation of the activity of the CCR5 coreceptor is one of the natural strategies to avoid disease in some natural host species of SIV.[7]

Unlike SIVsmm infection in sooty mangabeys, a recent[when?] study of SIVcpz in wild living chimpanzees suggests that infected chimpanzees experience an AIDS-like illness similar to HIV-1 infected humans. The later stages of SIV infection develop into sAIDS, much like how HIV infection develops into AIDS.

Taxonomy

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The simian (monkey-hosted) immunodeficiency viruses are a species of retrovirus in the Primate group of genus Lentivirus along with the human viruses HIV-1 and HIV-2 that cause AIDS, and a few other viruses that infect other primates. Related viruses in other groups in the genus infect other mammals like sheep and goats, horses, cattle, cats, and a few others. The genus is one of six genera in subfamily orthoretrovirinae, which together with genus Spumavirus form family retroviridae of all RNA retroviruses (RNA viruses which use a DNA intermediate).[8]

The ICTVdB code of SIV is 61.0.6.5.003.[9] Although HIV-1 and HIV-2 cladistically fall into SIV,[10] ICTV considers them distinct species from ordinary, non-human-infecting SIV.

Strains

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 grp i 
 
 
 
 

HIV-1

 

cpzPtt

 

gor

 

cpzPts

 
 
 

drl

 

mnd2

 
 

rcm

 

agi

 grp ii 
 
 
 

HIV-2

 

mac

 

mne

 

stm

 

smm

 grp iii/agm 
 
 
 

gri

 

ver

 

tan

 

sab

 grp iv 
 
 
 

lho

 

sun

 

prg

 

mnd1

 
 
 

wrc

 

olc

 
 

trc

 

krc

 grp v 
 
 
 
 
 
 

gsn

 

mus2

 (grp vi) 
 
 
 

col

 

kcol1

 

kcol2

blc

 

mon

 

mus1

reg

 
 

tal

 
 

asc

 

bkm

 
 

deb

blu

 
 
 

den

 

syk

 

wol

Phylogenetic relations between simian immunodeficiency viruses (SIVs)[10][11][12][13][14]

While human immunodeficiency virus has a limited number of subtypes, SIV is now known to infect a few dozen species of non-human primates, and distinct strains are often associated with each species, or with a set of closely related species. The thus far categorized ~40 strains are divided into five distinct groups and one subgroup:[10]

In addition to the subgroups defined for extent SIVs, two endogenous SIVs are found in prosimian lemurs. These paleo-SIVs form a basal branch relative to extant SIVs.[15]

History

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Immunodeficiency resembling human AIDS was reported in captive monkeys in the United States beginning in 1983.[16][17][18] SIV was isolated in 1985 from some of these animals, captive rhesus macaques suffering from simian AIDS (SAIDS).[17] The discovery of SIV was made shortly after HIV-1 had been isolated as the cause of AIDS and led to the discovery of HIV-2 strains in West Africa. HIV-2 was more similar to the then-known SIV strains than to HIV-1, suggesting for the first time the simian origin of HIV. Further studies indicated that HIV-2 is derived from the SIVsmm strain found in sooty mangabeys, whereas HIV-1, the predominant virus found in humans, is derived from SIV strains infecting chimpanzees (SIVcpz).[citation needed]

It is not believed that chimpanzees are the original hosts of an independent lineage of SIV, but rather that SIVcpz is a relatively recent acquisition resulting from a recombination of SIVgsn (greater spot-nosed monkeys) and SIVrcm (red-capped mangabeys) within the host chimpanzee. It is known that chimpanzees hunt and consume these monkeys for food.[19] In 2010, researchers reported that SIV had infected monkeys in Bioko for at least 32,000 years. Based on molecular clock analyses of sequences, it was previously thought by many that SIV infection in monkeys had happened over the past few hundred years.[3] Scientists estimated that it would take a similar amount of time before humans would adapt naturally to HIV infection in the way monkeys in Africa have adapted to SIV and not suffer any harm from the infection.[20]

In 2008, discovery of an endogenous lentivirus in a prosimian (proto-monkey) primate, the gray mouse lemur native to Madagascar, pushed the origin of SIV-like lentivirus infections in primates back to at least 14 Ma, the last time there was intermingling of mammals between the island of Madagascar and the African mainland, if the infection is attributed to horizontal transmission between homologous hosts. If the virus was coevolved with the host, rather than acquired, that potentially pushes the date of the endogenous event back to approx. 85 Ma, the split between the lemur-like and monkey-like primate lineages. That date barely antedates the emergence of the primates 87.7 Ma.[21]

Virology

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Structure and genome

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The SIV virion is a spherical to pleomorphic glycoprotein envelope 110-120 nm across enclosing a 110x50nm truncated cone or wedge-shaped (occasionally rod) capsid containing a dimeric pair of positive-sense single-stranded RNA genomes.[citation needed]

Genome

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  • coding regions

Proteome

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Further information: Structure and genome of HIV § Genome organization
  • genes: env, gag, pol, tat, rev, nef, vpr, vif, vpu/vpx
  • Structural proteins (envelope): SU, TM(gag): MA, CA, NC
  • Enzymes: RT, PR, IN
  • Gene regulators: Tat, Rev
  • Accessory proteins: Nef, Vpr, Vpx, Vif

Tropism

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Differences in species specificity of SIV and related retroviruses may be partly explained by variants of the protein TRIM5α in humans and non-human primate species. This intracellular protein recognizes the capsid of various retroviruses and blocks their reproduction. Other proteins, such as APOBEC3G/3F, which exerts antiretroviral immune activity, may also be important in restricting cross-species transmission.[22]

Replication

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  • Attachment
  • Penetration
  • Uncoating
  • Replication
    • reverse transcription
 +ssRNA → -ssDNA → dsDNA → +ssRNA (viral genome)
                         → +ssmRNA → viral protein
  • integration
  • latency
  • cleavage
  • protein synthesis
  • Assembly
  • Budding
  • Maturation

Quasispecies

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The speed and transcription inaccuracies of RNA viruses give rise to antigenically distinct varieties in a single host animal. These quasispecies do not necessarily give rise to population-wide new organisms. The rate of proliferation of quasispecies has significant implication for host immune control, and therefore virulence of the organism.[citation needed]

Pathogenesis

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About 100,000 cells from rhesus macaques, grouped by similarity. Red cells are from monkeys infected with simian-human immunodeficiency virus, while blue cells are from uninfected ones.

SIV pathogenesis encompasses both pathogenic and non-pathogenic SIV infections. SIV infection of non-human primates (NHPs) invariably results in persistent infection, but rarely acute disease. Pathogenic infection is typified by Rhesus macaques infected with SIV strains derived from sooty mangabeys. Disease progression to AIDS occurs within a period of months to years, depending upon the SIV strain used. Non-pathogenic infection is typified by African NHPs naturally infected with SIV. These animals rarely progress to AIDS despite maintaining viral loads that are equivalent to SIV viral loads in pathogenic infections. It is postulated that AIDS-like disease in African NHPs represents horizontal transmission of the virus from one or more homologous species in the recent evolutionary past, before equilibrium of co-adaptation has occurred.[citation needed]

SIV/HIV infection similarities and differences

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The similarities of the two types of virus infections:[23]

  • high level of virus replication during primary infection (0–180 days)
  • high level of CD4+ T-cell loss (0–180 days)
  • restricted role of humoral immune response

The differences (what happens in nonhuman primates):

  • lower level of CCR5+ T-cells
  • stable level of viral replication (180 days-years)
  • restoration of CD4+ T-cells
  • early cytokine production (0–10 days after infection)
  • normal level of immune activation
  • high level of functional immune cells
  • establishment of anti-inflammatory milieu

Epidemiology

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strain lineage host binomial disease
HIV-1 SIVcpz humans H. sapiens AIDS
HIV-2 SIVsmm humans H. sapiens AIDS
SIVcpz SIVrcm/SIVgsn Chimpanzee P. Troglodytes SAIDS
SIVgor SIVcpz Gorilla G. gorilla ( - )
SIVsmm Sooty mangabey ( - )

Beatrice Hahn of the University of Pennsylvania and a team of researchers in 2009 found that chimpanzees do die from simian AIDS in the wild and that the AIDS outbreak in Africa has contributed to the decline of chimpanzee populations. Testing wild chimpanzees, researchers detected organ and tissue damage similar to late-stage human AIDS. The infected chimpanzees had a 10 to 16 times greater risk of dying than uninfected ones; infected females were less likely to give birth, could pass the virus to their infants, and had a higher infant mortality rate than uninfected females.[24][25] Bonobos appear to avoid simian immunodeficiency virus (SIV) and its effects, though it is not known why.[19]

African green monkeys (also called vervets, genus Chlorocebus) in African populations are heavily infected with SIVagm,[26][27] while the virus is absent in the founder isolate vervet populations in the Caribbean.[28] The prevalence of SIV infection in African populations ranges 78-90% in adult females and 36-57% in adult males, while SIV infection is rare in immature individuals.[27][26] SIV infected vervets in the wild do not develop chronic immune activation or microbial translocation (assessed by sCD14 as a surrogate biomarker). During natural SIV infection, the gut microbiome showed a significant increase in microbial diversity, a decrease in Proteobacteria/Succinivibrio and an increase of Veillonella, a decrease in genes involved in pathways of microbial invasion, and partial reversibility of acute infection-related shifts in microbial abundance.[29] The pattern of natural selection in the monkey genome in genes involved in HIV responses and those regulated in response to experimental SIV infection in monkeys, but not macaques, suggests a natural adaptation to SIV in Chlorocebus monkeys in Africa.[30]

Vaccine research

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In 2012, researchers reported that initial infection of rhesus monkeys by neutralization-resistant SIV strains[31] could be partially prevented through use of an anti-SIVSME543 vaccine obligately including Env protein antigens.[32]

In 2013, a study by a group of authors reported on successful testing of a vaccine containing SIV protein-expressing rhesus cytomegalovirus vector. Approximately 50% of vaccinated rhesus macaques manifested durable, aviraemic control of infection with the highly pathogenic strain SIVmac239.[33]

See also

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References

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  1. ^ Peeters M, Courgnaud V, Abela B (2001). "Genetic Diversity of Lentiviruses in Non-Human Primates" (PDF). AIDS Reviews. 3: 3–10. Retrieved 2020-07-11.
  2. ^ Peeters M, Courgnaud V (2002). Kuiken C, Foley B, Freed E, Hahn B, Korber B, Marx PA, McCutchan FE, Mellors JW, Wolinsky S (eds.). Overview of Primate Lentiviruses and their Evolution in Non-human Primates in Africa (PDF). HIV sequence compendium. Los Alamos, NM: Theoretical Biology and Biophysics Group, Los Alamos National Laboratory. pp. 2–23. Retrieved 2010-09-19.
  3. ^ a b McNeil Donald G. Jr (September 16, 2010). "Precursor to H.I.V. Was in Monkeys for Millennia". New York Times. Retrieved 2010-09-17.
  4. ^ Worobey M, Telfer P, Souquière S, Hunter M, Coleman CA, Metzger MJ, et al. (September 2010). "Island biogeography reveals the deep history of SIV". Science. 329 (5998): 1487. Bibcode:2010Sci...329.1487W. doi:10.1126/science.1193550. PMID 20847261. S2CID 37803712..
  5. ^ Sharp PM, Hahn BH (August 2010). "The evolution of HIV-1 and the origin of AIDS". Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences. 365 (1552): 2487–2494. doi:10.1098/rstb.2010.0031. PMC 2935100. PMID 20643738.
  6. ^ Peeters M, D'Arc M, Delaporte E (2014). "Origin and diversity of human retroviruses". AIDS Reviews. 16 (1): 23–34. PMC 4289907. PMID 24584106.
  7. ^ Jasinska AJ, Pandrea I, Apetrei C (2022-01-27). "CCR5 as a Coreceptor for Human Immunodeficiency Virus and Simian Immunodeficiency Viruses: A Prototypic Love-Hate Affair". Frontiers in Immunology. 13: 835994. doi:10.3389/fimmu.2022.835994. ISSN 1664-3224. PMC 8829453. PMID 35154162.
  8. ^ "Taxon Details | ICTV". ictv.global.
  9. ^ ICTV database entry: 61.0.6.5.003
  10. ^ a b c Sharp PM, Hahn BH (September 2011). "Origins of HIV and the AIDS pandemic". Cold Spring Harbor Perspectives in Medicine. 1 (1): a006841. doi:10.1101/cshperspect.a006841. PMC 3234451. PMID 22229120.
  11. ^ Ahuka-Mundeke S, Ayouba A, Mbala-Kingebeni P, Liegeois F, Esteban A, Lunguya-Metila O, et al. (December 2011). "Novel multiplexed HIV/simian immunodeficiency virus antibody detection assay". Emerging Infectious Diseases. 17 (12): 2277–2286. doi:10.3201/eid1712.110783. PMC 3311211. PMID 22172157.
  12. ^ Pancino G, Silvestri G, Fowke KR (2012). Models of Protection Against HIV/SIV: Avoiding AIDS in Humans and Monkeys. Elsevier. p. 6. ISBN 978-0-12-387715-4.
  13. ^ Peeters M, Courgnaud V, Abela B, Auzel P, Pourrut X, Bibollet-Ruche F, et al. (May 2002). "Risk to human health from a plethora of simian immunodeficiency viruses in primate bushmeat". Emerging Infectious Diseases. 8 (5): 451–457. doi:10.3201/eid0805.010522. PMC 2732488. PMID 11996677.
  14. ^ Lauck M, Switzer WM, Sibley SD, Hyeroba D, Tumukunde A, Weny G, et al. (October 2013). "Discovery and full genome characterization of two highly divergent simian immunodeficiency viruses infecting black-and-white colobus monkeys (Colobus guereza) in Kibale National Park, Uganda". Retrovirology. 10: 107. doi:10.1186/1742-4690-10-107. PMC 4016034. PMID 24139306.
  15. ^ Gilbert, C; Maxfield, DG; Goodman, SM; Feschotte, C (March 2009). "Parallel germline infiltration of a lentivirus in two Malagasy lemurs". PLOS Genetics. 5 (3): e1000425. doi:10.1371/journal.pgen.1000425. PMC 2651035. PMID 19300488.
  16. ^ Letvin NL, Eaton KA, Aldrich WR, Sehgal PK, Blake BJ, Schlossman SF, et al. (May 1983). "Acquired immunodeficiency syndrome in a colony of macaque monkeys". Proceedings of the National Academy of Sciences of the United States of America. 80 (9): 2718–2722. Bibcode:1983PNAS...80.2718L. doi:10.1073/pnas.80.9.2718. PMC 393899. PMID 6221343.
  17. ^ a b Daniel MD, Letvin NL, King NW, Kannagi M, Sehgal PK, Hunt RD, et al. (June 1985). "Isolation of T-cell tropic HTLV-III-like retrovirus from macaques". Science. 228 (4704): 1201–1204. Bibcode:1985Sci...228.1201D. doi:10.1126/science.3159089. PMID 3159089.
  18. ^ King NW, Hunt RD, Letvin NL (December 1983). "Histopathologic changes in macaques with an acquired immunodeficiency syndrome (AIDS)". The American Journal of Pathology. 113 (3): 382–388. PMC 1916356. PMID 6316791.
  19. ^ a b Sharp PM, Shaw GM, Hahn BH (April 2005). "Simian immunodeficiency virus infection of chimpanzees". Journal of Virology. 79 (7): 3891–3902. doi:10.1128/JVI.79.7.3891-3902.2005. PMC 1061584. PMID 15767392.
  20. ^ "HIV precursor in monkeys ancient: study". CBC News. 17 September 2010. Archived from the original on March 25, 2013. Retrieved 17 September 2010.
  21. ^ Gifford, RJ; Katzourakis, A; Tristem, M; Pybus, OG; Winters, M; Shafer, RW (23 December 2008). "A transitional endogenous lentivirus from the genome of a basal primate and implications for lentivirus evolution". Proceedings of the National Academy of Sciences of the United States of America. 105 (51): 20362–7. doi:10.1073/pnas.0807873105. PMC 2603253. PMID 19075221.
  22. ^ Heeney JL, Dalgleish AG, Weiss RA (July 2006). "Origins of HIV and the evolution of resistance to AIDS". Science. 313 (5786): 462–466. Bibcode:2006Sci...313..462H. doi:10.1126/science.1123016. PMID 16873637. S2CID 27673160.
  23. ^ Pandrea, Ivona; Sodora, Donald L.; Silvestri, Guido; Apetrei, Cristian (September 2008). "Into the Wild: Simian Immunodeficiency Virus (SIV) Infection in Natural Hosts". Trends in Immunology. 29 (9): 419–428. doi:10.1016/j.it.2008.05.004. ISSN 1471-4906. PMC 2840226. PMID 18676179.
  24. ^ Chimpanzees Do Die From Simian AIDS, Study Finds by Lawrence K. Altman Chimpanzees Do Die from Simian AIDS, Study Finds
  25. ^ Keele BF, Jones JH, Terio KA, Estes JD, Rudicell RS, Wilson ML, et al. (July 2009). "Increased mortality and AIDS-like immunopathology in wild chimpanzees infected with SIVcpz". Nature. 460 (7254): 515–519. Bibcode:2009Natur.460..515K. doi:10.1038/nature08200. PMC 2872475. PMID 19626114.
  26. ^ a b Ma D, Jasinska A, Kristoff J, Grobler JP, Turner T, Jung Y, et al. (January 2013). "SIVagm infection in wild African green monkeys from South Africa: epidemiology, natural history, and evolutionary considerations". PLOS Pathogens. 9 (1): e1003011. doi:10.1371/journal.ppat.1003011. PMC 3547836. PMID 23349627.
  27. ^ a b Ma D, Jasinska AJ, Feyertag F, Wijewardana V, Kristoff J, He T, et al. (May 2014). "Factors associated with siman immunodeficiency virus transmission in a natural African nonhuman primate host in the wild". Journal of Virology. 88 (10): 5687–5705. doi:10.1128/JVI.03606-13. PMC 4019088. PMID 24623416.
  28. ^ Kapusinszky B, Mulvaney U, Jasinska AJ, Deng X, Freimer N, Delwart E (August 2015). "Local Virus Extinctions following a Host Population Bottleneck". Journal of Virology. 89 (16): 8152–8161. doi:10.1128/jvi.00671-15. PMC 4524239. PMID 26018153.
  29. ^ Jasinska AJ, Dong TS, Lagishetty V, Katzka W, Jacobs JP, Schmitt CA, et al. (November 2020). "Shifts in microbial diversity, composition, and functionality in the gut and genital microbiome during a natural SIV infection in vervet monkeys". Microbiome. 8 (1): 154. doi:10.1186/s40168-020-00928-4. PMC 7648414. PMID 33158452.
  30. ^ Svardal H, Jasinska AJ, Apetrei C, Coppola G, Huang Y, Schmitt CA, et al. (December 2017). "Ancient hybridization and strong adaptation to viruses across African vervet monkey populations". Nature Genetics. 49 (12): 1705–1713. doi:10.1038/ng.3980. PMC 5709169. PMID 29083404.
  31. ^ "Neutralization-resistant" refers to strains which are not able to be neutralized by the native immune response due to compensating mutation; see HIV-1 related information.
  32. ^ Barouch DH, Liu J, Li H, Maxfield LF, Abbink P, Lynch DM, et al. (January 2012). "Vaccine protection against acquisition of neutralization-resistant SIV challenges in rhesus monkeys". Nature. 482 (7383): 89–93. Bibcode:2012Natur.482...89B. doi:10.1038/nature10766. PMC 3271177. PMID 22217938.
  33. ^ Hansen SG, Piatak M, Ventura AB, Hughes CM, Gilbride RM, Ford JC, et al. (October 2013). "Immune clearance of highly pathogenic SIV infection". Nature. 502 (7469): 100–104. Bibcode:2013Natur.502..100H. doi:10.1038/nature12519. PMC 3849456. PMID 24025770.

Further reading

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