Arenavirus

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Arenaviridae
Viruses-04-02973-g002.webp
(A) Electron micrograph of Lassa virus, bar = 100nm (B) diagram and (C) genome of arenavirus
Virus classification OOjs UI icon edit-ltr.svg
(unranked): Virus
Realm: Riboviria
Kingdom: Orthornavirae
Phylum: Negarnaviricota
Class: Ellioviricetes
Order: Bunyavirales
Family:Arenaviridae
Genera

An arenavirus is a bi- or trisegmented ambisense RNA virus that is a member of the family Arenaviridae. [1] [2] These viruses infect rodents and occasionally humans. A class of novel, highly divergent arenaviruses, properly known as reptarenaviruses, have also been discovered which infect snakes to produce inclusion body disease, mostly in boa constrictors. At least eight arenaviruses are known to cause human disease. The diseases derived from arenaviruses range in severity. Aseptic meningitis, a severe human disease that causes inflammation covering the brain and spinal cord, can arise from the lymphocytic choriomeningitis virus. Hemorrhagic fever syndromes, including Lassa fever, are derived from infections such as Guanarito virus, Junin virus, Lassa virus, Lujo virus, [3] Machupo virus, Sabia virus, or Whitewater Arroyo virus. [4] Because of the epidemiological association with rodents, some arenaviruses and bunyaviruses are designated as roboviruses.

Contents

Structure

Mammarenavirus structure and genome composition. Viruses-12-00784-g001.png
Mammarenavirus structure and genome composition.

Viewed in cross-section, arenaviruses contain grainy particles that are ribosomes acquired from their host cells. It is from this characteristic that they acquired the name arena , from the Latin root meaning sand . [5] The ribosomal structures are not believed to be essential for virus replication. Virus particles, or virions, are pleomorphic (variable in shape) but are often spherical, with a diameter of 60–300 nm, and are covered with surface glycoprotein spikes. [6]

The virus contains a beaded nucleocapsid with two single-stranded RNA segments. The nucleocapsid consists of a core of nucleic acid enclosed in a protein coat. Although they are categorized as negative-sense viruses, [7] arenaviruses are ambisense. While sections of their genome encode genes in the negative sense (reverse polarity), other sections encode genes in the opposite (forward/positive sense) direction. This complex gene expression structure is theorized to be a primitive regulatory system, allowing the virus to control what proteins are synthesized at what point in the life cycle. The life cycle of the arenavirus is restricted to the cell cytoplasm.[ citation needed ]

Genome

Genomes of Arenaviridae Genomes of Arenaviridae.png
Genomes of Arenaviridae

Arenaviruses have a segmented RNA genome that consists of two single-stranded ambisense RNAs. [8] As with all negative-sense RNA viruses, the genomic RNA alone is not infectious and the viral replication machinery is required to initiate infection within a host cell. [9] Genomic sense RNA packaged into the arenavirus virion is designated negative-sense RNA, and must first be copied into a positive-sense mRNA in order to produce viral protein. [10] The RNA segments are denoted Small (S), Medium (M; if present), and Large (L), [8] [11] and code for four viral proteins in a unique ambisense coding strategy. [12] [13] For mammarenaviruses and reptarenaviruses, each RNA segment codes for two viral proteins in opposite orientation such that the negative-sense RNA genome serves as the template for transcription of a single mRNA and the positive-sense copy of the RNA genome templates a second mRNA. [10] The separate coding sequences of the two viral proteins are divided by an intergenic region RNA sequence that is predicted to fold into a stable hairpin structure. [14]

The extreme termini of each RNA segment contains a 19 nucleotide highly conserved sequence that is critical for recruitment of the viral replication machinery and initiation of viral mRNA transcription and genomic replication. [15] [16] [17] [18] [19] The conserved 5' and 3' RNA termini sequences are complementary and allows each RNA segment to adopt a double-stranded RNA panhandle structure [20] that maintains the termini in close proximity and results in a circular appearance to purified arenavirus genomic templates visualized by electron microscopy. [21] [22] The double-stranded RNA panhandle structure is critical for efficient viral RNA synthesis, [18] [23] but potential interterminal double-stranded RNA interactions must be transiently relieved in order to recruit the viral polymerase. [19]

The S-segment RNA is approximately 3.5 kb, and encodes the viral nucleocapsid protein (NP) and glycoprotein (GPC). [24] The L-segment RNA is approximately 7.2 kb, and encodes the viral RNA-dependent RNA-polymerase (L) and a small RING-domain containing protein (Z). [25] [26] [27]

The Z protein forms homo oligomers and a structural component of the virions. [28] The formation of these oligomers is an essential step for particle assembly and budding. Binding between Z and the viral envelope glycoprotein complex is required for virion infectivity. Z also interacts with the L and NP proteins. Polymerase activity appears to be modulated by the association between the L and Z proteins. Interaction between the Z and NP proteins is critical for genome packaging.[ citation needed ]

Microbiology

Arenavirus replication cycle. Viruses-12-00784-g003.png
Arenavirus replication cycle.

The glycoprotein (GP) is synthesised as a precursor molecule. [29] It is cleaved into three parts - GP1, GP2 and a stable signal peptide (SSP). These reactions are catalysed by cellular signal peptidases and the cellular enzyme Subtilisin Kexin Isozyme-1 (SKI-1)/Site-1 Protease (S1P). These processes are essential for fusion competence and incorporation of mature GP into nascent budding virion particles.[ citation needed ]

Taxonomy

Within the family Arenaviridae, arenaviruses were formerly all placed in the genus Arenavirus, but in 2015 were divided into the genera Mammarenavirus for those with mammalian hosts and Reptarenavirus for those infecting snakes. [30] [31] Reptarenaviruses and mammarenavirus are separated by an impenetrable species barrier. Infected rodents cannot pass disease onto snakes, and IBD in captive snakes is not transmissible to humans.[ citation needed ]

A third genus, Hartmanivirus (not to be confused with genus Haartmanvirus of vibrio phages in family Demerecviridae , order Caudovirales ), has also been established, [32] including other species that infect snakes. The organisation of the genome of this genus is typical of arenaviruses but their glycoproteins resemble those of filoviruses. Species in this genus lack the matrix protein. [33]

A fourth genus, Antennavirus , has also been established [34] to accommodate two arenaviruses found in striated frogfish ( Antennarius striatus ). [35] A third antennavirus has been detected in Chinook salmon and sockeye salmon. [36]

Mammarenaviruses can be divided into two serogroups, which differ genetically and by geographical distribution: [37] When the virus is classified "Old World" this means it was found in the Eastern Hemisphere in places such as Europe, Asia, and Africa. When it is found in the Western Hemisphere, in places such as Argentina, Bolivia, Venezuela, Brazil, and the United States, it is classified "New World". Lymphocytic choriomeningitis (LCM) virus is the only mammarenavirus found worldwide because of its ubiquitous Old World host, the house mouse. Old and New World area viruses appear to have diverged ~45,000 years ago. [38] The Old World Mammarenaviruses originated ~23.1-1.88 thousand years ago, most likely in Southern Africa, while the New World Mammarenaviruses evolved in the Latin America-Caribbean region ~41.4-3.3 thousand years ago. [38]

Mammarenavirus

Old World complex

Arenavirus taxonomy and location Fimmu-10-00372-g001.jpg
Arenavirus taxonomy and location

New World complex

Reptarenavirus

Hartmanivirus

Antennavirus

Evolution

The evolution of the Mammarenavirus genus has been studied. [38] The New World and Old World species diverged less than 45,000 years ago. The New World species evolved between 41,400 and 3,300 years ago in the Latin America-Caribbean region. The Old World species evolved between 23,100 and 1,880 years ago, most likely in southern Africa. [38]

Reservoirs

Some arenaviruses are zoonotic pathogens and are generally associated with rodent—transmitted disease in humans. Each virus usually is associated with a particular rodent host species in which it is maintained. Arenaviruses persist in nature by infecting rodents first and then transmitted into humans. Humans can be infected through mucosal exposure to aerosols, or by direct contact of abraded skin with the infectious material, derived from infected rodents. [6] Aerosols are fine mists or sprays of rodent dried excreta, especially urine that is dropped in the environment. Most of the Arenaviruses caught by humans are within their own homes when these rodents seek shelter. The virus can be caught in factories, from food that has been contaminated, or within agricultural work areas. Humans' risk of contracting the Arenavirus infection is related to age, race, or sex within the degree of contact with the dried rodent excreta.[ citation needed ]

Epidemiology

Hosts

Arenavirus diseases and hosts
VirusDiseaseHostDistribution
Dandenong [39] Dandenong hemorrhagic feverUnknownold world ( Australian cases from Serbia )
Lymphocytic choriomeningitis virus Lymphocytic choriomeningitis House mouse (Mus musculus)Worldwide
Lassa virus Lassa fever Natal Multimammate Mouse (Mastomys natalensis)West Africa
Junin virus Argentine hemorrhagic fever Drylands Vesper Mouse (Calomys musculinus) Argentina
Machupo virus Bolivian hemorrhagic fever Large Vesper Mouse (Calomys callosus) Bolivia
Guanarito virus Venezuelan hemorrhagic fever Short-tailed Cane Mouse (Zygodontomys brevicauda) Venezuela
Sabiá virus Brazilian hemorrhagic fever Unknown Brazil
Tacaribe virus Bat ( Artibeus ) Trinidad
Flexal virus Influenza-like illnessRice rat ( Oryzomys )Brazil
Whitewater Arroyo virusHemorrhagic feverWoodrat ( Neotoma )Southwestern United States

Clinical diseases

Comparison of disease phenotypes of OW and NW arenaviruses Fimmu-10-00372-g005.jpg
Comparison of disease phenotypes of OW and NW arenaviruses
  1. Lymphocytic choriomeningitis (LCM) viruses cause influenza-like febrile illness, but occasionally they may cause meningitis, characteristically accompanied by large numbers of lymphocytes in the cerebrospinal fluid (as the name LCM suggests).
  2. Lassa virus causes Lassa fever. Lassa fever is endemic in west Africa. The virus was first isolated from Americans stationed in the village of Lassa, Nigeria. The virus can be transmitted person-to-person.
    • Subclinical diseases: Serological studies suggest that inapparent infections particularly among members of hunting tribes are common.
    • Clinical infections: Lassa fever is characterised by high fever, severe myalgia, coagulopathy, haemorrhagic skin rash, and occasional visceral haemorrhage as well as necrosis of liver and spleen.
  3. Other Arenaviruses like Junin virus, Machupo virus cause haemorrhagic fevers.

All of these diseases pose a great threat to public health in the regions where it is taking place. For example, when the Old World Lassa virus turns into Lassa fever, this usually results in a significant amount of mortality. Similarly the New World Junin virus causes Argentine hemorrhagic fever. This fever is a severe illness with hemorrhagic and neurological manifestations and a case fatality of fifteen to thirty percent. [6] The way this virus spreads is through increased traveling to and from endemic regions. This traveling has led to the importation of Lassa fever into non-endemic metropolitan areas all over the world.

Recent outbreaks

A new species of arenavirus named the Lujo virus has been linked to five patients who exhibited symptoms of viral hemorrhagic fever in South Africa. [40] The disease originated near Lusaka, Zambia and spread to Johannesburg, South Africa, after the first patient was transported to a hospital there. The results of genetic sequencing tests conducted by epidemiologists at Columbia University in New York City, USA, and at the Special Pathogens Branch of the Centers for Disease Control in Atlanta, USA, provided evidence that the causative agent of the disease is a virus from the family Arenaviridae, which ultimately resulted in the deaths of four out of the five infected in Zambia and South Africa during the outbreak which began in September 2008.[ citation needed ]

Arenavirus has also pinpointed as the cause of death of three donor organ recipients in Australia who contracted the virus after receiving kidney and a liver donations from a single infected organ donor in late 2006. All three died in the first week of 2007. [41] [42]

WHO and its Global Outbreak Alert and Response Network (GOARN) partners continue to support the Ministries of Health of the two countries in various facets of the outbreak investigation, including laboratory diagnosis, investigations, active case finding and follow-up of contacts. [43]

Treatments

Very few treatment methods are available. The current lack of a licensed vaccine and limited therapeutic options for the arenavirus make it arguably among the most neglected virus groups. The only licensed drug for the treatment of human arenavirus infection is the nucleoside analogue ribavirin. [44] Ribavirin reduces morbidity and mortality in humans infected with certain arenaviruses, such as LASV and JUNV infections, if it is taken in the early stages of the disease. Ribavirin displays mixed success in treating severe arenaviral disease and is associated with significant toxicities. [45]

Experimental approaches

Effective antiviral drugs need to be produced at a low cost, taken orally, and able to withstand tropical climates due to the regions where these infections are occurring. For this reason high throughput screening (HTS) of small molecular libraries could be the answer to finding a better remedy. HTS collects libraries of small synthetic molecules that can be used to identify protein promoting "agonist" molecules or protein inhibiting "antagonist" interactions. [44] With HTS sustainable antiviral drugs can be discovered against possible new human pathogenic viruses.

Immunotherapy is another potential approach. Monoclonal antibodies against Junin virus have been tested in animal models. An immunotherapeutic agent active against all tested mammarenaviruses that use the transferrin receptor 1 as their receptor was under investigation in 2020. [46]

Related Research Articles

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Mouse mammary tumor virus (MMTV) is a milk-transmitted retrovirus like the HTL viruses, HI viruses, and BLV. It belongs to the genus Betaretrovirus. MMTV was formerly known as Bittner virus, and previously the "milk factor", referring to the extra-chromosomal vertical transmission of murine breast cancer by adoptive nursing, demonstrated in 1936, by John Joseph Bittner while working at the Jackson Laboratory in Bar Harbor, Maine. Bittner established the theory that a cancerous agent, or "milk factor", could be transmitted by cancerous mothers to young mice from a virus in their mother's milk. The majority of mammary tumors in mice are caused by mouse mammary tumor virus.

<i>Bunyavirales</i> Order of RNA viruses

Bunyavirales is an order of segmented negative-strand RNA viruses with mainly tripartite genomes. Member viruses infect arthropods, plants, protozoans, and vertebrates. It is the only order in the class Ellioviricetes. The name Bunyavirales derives from Bunyamwera, where the original type species Bunyamwera orthobunyavirus was first discovered. Ellioviricetes is named in honor of late virologist Richard M. Elliott for his early work on bunyaviruses.

<i>Lassa mammarenavirus</i> Type of viral hemorrhagic fever

Lassa mammarenavirus (LASV) is an arenavirus that causes Lassa hemorrhagic fever, a type of viral hemorrhagic fever (VHF), in humans and other primates. Lassa mammarenavirus is an emerging virus and a select agent, requiring Biosafety Level 4-equivalent containment. It is endemic in West African countries, especially Sierra Leone, the Republic of Guinea, Nigeria, and Liberia, where the annual incidence of infection is between 300,000 and 500,000 cases, resulting in 5,000 deaths per year.

<span class="mw-page-title-main">Viral hemorrhagic fever</span> Type of illnesses

Viral hemorrhagic fevers (VHFs) are a diverse group of animal and human illnesses. VHFs may be caused by five distinct families of RNA viruses: the families Filoviridae, Flaviviridae, Rhabdoviridae, and several member families of the Bunyavirales order such as Arenaviridae, and Hantaviridae. All types of VHF are characterized by fever and bleeding disorders and all can progress to high fever, shock and death in many cases. Some of the VHF agents cause relatively mild illnesses, such as the Scandinavian nephropathia epidemica, while others, such as Ebola virus, can cause severe, life-threatening disease.

Lymphocytic choriomeningitis (LCM) is a rodent-borne viral infectious disease that presents as aseptic meningitis, encephalitis or meningoencephalitis. Its causative agent is lymphocytic choriomeningitis mammarenavirus (LCMV), a member of the family Arenaviridae. The name was coined by Charles Armstrong in 1934.

Venezuelan hemorrhagic fever (VHF) is a zoonotic human illness first identified in 1989. The disease is most prevalent in several rural areas of central Venezuela and is caused by Guanarito mammarenavirus (GTOV) which belongs to the Arenaviridae family. The short-tailed cane mouse is the main host for GTOV which is spread mostly by inhalation of aerosolized droplets of saliva, respiratory secretions, urine, or blood from infected rodents. Person-to-person spread is possible, but uncommon.

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<i>Andes orthohantavirus</i> Species of virus

Andes orthohantavirus (ANDV), a species of Orthohantavirus, is a major causative agent of hantavirus cardiopulmonary syndrome (HCPS) and hantavirus pulmonary syndrome (HPS) in South America. It is named for the Andes mountains of Chile and Argentina, where it was first discovered. Originating in the reservoir of rodents, Andes orthohantavirus is easily transmitted to humans who come into contact with infected rodents or their fecal droppings. However, infected rodents do not appear ill, so there is no readily apparent indicator to determine whether the rodent is infected or not. Additionally, Andes orthohantavirus, specifically, is the only hantavirus that can be spread by human to human contact via bodily fluids or long-term contact from one infected individual to a healthy person.

<span class="mw-page-title-main">Argentinian mammarenavirus</span> Species of virus

Mammarenavirus juninense, better known as the Junin virus or Junín virus (JUNV), is an arenavirus in the Mammarenavirus genus that causes Argentine hemorrhagic fever (AHF). The virus took its original name from the city of Junín, around which the first cases of infection were reported, in 1958.

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Lujo is a bisegmented RNA virus—a member of the family Arenaviridae—and a known cause of viral hemorrhagic fever (VHF) in humans. Its name was suggested by the Special Pathogens Unit of the National Institute for Communicable Diseases of the National Health Laboratory Service (NICD-NHLS) by using the first two letters of the names of the cities involved in the 2008 outbreak of the disease, Lusaka (Zambia) and Johannesburg. It is the second pathogenic Arenavirus to be described from the African continent—the first being Lassa virus—and since 2012 has been classed as a "Select Agent" under U.S. law.

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<i>Mammarenavirus</i> Genus of viruses

Mammarenavirus is a genus of viruses in the family Arenaviridae. The name is a portmanteau of mammal and the former name Arenavirus, and differentiates it from the reptile-associated Reptarenavirus. Arenavirus comes from the Latin arena (sand) for the sandy appearance of the virions.

<span class="mw-page-title-main">Negative-strand RNA virus</span> Phylum of viruses

Negative-strand RNA viruses are a group of related viruses that have negative-sense, single-stranded genomes made of ribonucleic acid (RNA). They have genomes that act as complementary strands from which messenger RNA (mRNA) is synthesized by the viral enzyme RNA-dependent RNA polymerase (RdRp). During replication of the viral genome, RdRp synthesizes a positive-sense antigenome that it uses as a template to create genomic negative-sense RNA. Negative-strand RNA viruses also share a number of other characteristics: most contain a viral envelope that surrounds the capsid, which encases the viral genome, −ssRNA virus genomes are usually linear, and it is common for their genome to be segmented.

Mopeia mammarenavirus (MOPV) is a species of virus in the genus Mammarenavirus. It was initially isolated from the Mastomys natalensis mouse in the East African country of Mozambique in 1977. It is of the "Old World" Arenavirus lineage and is closely related to Lassa mammarenavirus, sharing 75% of its amino acid sequence.

References

  1. ↑ Radoshitzky, SR; Buchmeier, MJ; Charrel, RN; Clegg, JCS; Gonzalez, JJ; Günther, S; Hepojoki, J; Kuhn, JH; Lukashevich, IS; Romanowski, V; Salvato, MS; Sironi, M; Stenglein, MD; de la Torre, JC; ICTV Report, Consortium (August 2019). "ICTV Virus Taxonomy Profile: Arenaviridae". The Journal of General Virology. 100 (8): 1200–1201. doi: 10.1099/jgv.0.001280 . hdl: 10281/509719 . PMID   31192784.
  2. ↑ Shi, Mang; Lin, Xian-Dan; Chen, Xiao; Tian, Jun-Hua; Chen, Liang-Jun; Li, Kun; Wang, Wen; Eden, John-Sebastian; Shen, Jin-Jin; Li, Liu; Holmes, Edward C.; Zhang, Yong-Zhen (2018). "The evolutionary history of vertebrate RNA viruses". Nature. 561 (7722): 202. doi: 10.1038/s41586-018-0310-0 . PMID   29946168. S2CID   49433735.
  3. ↑ Briese T, Paweska JT, McMullan LK, et al. (May 2009). "Genetic detection and characterization of Lujo virus, a new hemorrhagic fever-associated arenavirus from southern Africa". PLOS Pathog. 5 (5): e1000455. doi: 10.1371/journal.ppat.1000455 . PMC   2680969 . PMID   19478873.
  4. ↑ Botten, J; Whitton, JL; Barrowman, P; Sidney, J; Whitmire, JK; Alexander, J; Kotturi, MF; Sette, A; Buchmeier, MJ (2010). "A Multivalent Vaccination Strategy for the Prevention of Old World Arenavirus Infection in Humans". Journal of Virology. 84 (19): 9947–56. doi:10.1128/JVI.00672-10. PMC   2937778 . PMID   20668086.
  5. ↑ Rowe, Wallace P.; Murphy, Frederick A.; Bergold, Gernot H.; Casals, Jordi; Hotchin, John; Johnson, Karl M.; Lehmann-Grube, Fritz; Mims, Cedric A.; Traub, Eric; Webb, Patricia A. (May 1970). "Arenoviruses: Proposed Name for a Newly Defined Virus Group". Journal of Virology. 5 (5): 652. doi:10.1128/jvi.5.5.651-652.1970. PMC   376052 . PMID   4986852.
  6. 1 2 3 Emonet, Sebastien E.; Urata, Shuzo; De La Torre, Juan C. (2011). "Arenavirus reverse genetics: New approaches for the investigation of arenavirus biology and development of antiviral strategies". Virology. 411 (2): 416–425. doi:10.1016/j.virol.2011.01.013. PMC   3057228 . PMID   21324503.
  7. ↑ "Arenaviridae - Negative Sense RNA Viruses - Negative Sense RNA Viruses (2011)". International Committee on Taxonomy of Viruses (ICTV). Archived from the original on 19 December 2018. Retrieved 23 May 2019.
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  9. ↑ Lee KJ, Novella IS, Teng MN, Oldstone MB, de La Torre JC (April 2000). "NP and L proteins of lymphocytic choriomeningitis virus (LCMV) are sufficient for efficient transcription and replication of LCMV genomic RNA analogs". J. Virol. 74 (8): 3470–7. doi:10.1128/jvi.74.8.3470-3477.2000. PMC   111854 . PMID   10729120.
  10. 1 2 Meyer BJ, de la Torre JC, Southern PJ (2002). "Arenaviruses: Genomic RNAs, Transcription, and Replication". Arenaviruses I. Current Topics in Microbiology and Immunology. Vol. 262. pp. 139–57. doi:10.1007/978-3-642-56029-3_6. ISBN   978-3-540-42244-0. PMID   11987804.{{cite book}}: |journal= ignored (help)
  11. ↑ Pedersen IR (March 1973). "Different classes of ribonucleic acid isolated from lymphocytic choriomeningitis virus". J. Virol. 11 (3): 416–23. doi:10.1128/JVI.11.3.416-423.1973. PMC   355116 . PMID   4734917.
  12. ↑ Auperin DD, Romanowski V, Galinski M, Bishop DH (December 1984). "Sequencing studies of pichinde arenavirus S RNA indicate a novel coding strategy, an ambisense viral S RNA". J. Virol. 52 (3): 897–904. doi:10.1128/JVI.52.3.897-904.1984. PMC   254611 . PMID   6492264.
  13. ↑ Auperin DD, McCormick JB (February 1989). "Nucleotide sequence of the Lassa virus (Josiah strain) S genome RNA and amino acid sequence comparison of the N and GPC proteins to other arenaviruses". Virology. 168 (2): 421–5. doi:10.1016/0042-6822(89)90287-0. PMID   2916333.
  14. ↑ Auperin DD, Galinski M, Bishop DH (April 1984). "The sequences of the N protein gene and intergenic region of the S RNA of pichinde arenavirus". Virology. 134 (1): 208–19. doi:10.1016/0042-6822(84)90286-1. PMID   6324469.
  15. ↑ Auperin D, Dimock K, Cash P, Rawls WE, Leung WC, Bishop DH (January 1982). "Analyses of the genomes of prototype pichinde arenavirus and a virulent derivative of Pichinde Munchique: evidence for sequence conservation at the 3' termini of their viral RNA species". Virology. 116 (1): 363–7. doi:10.1016/0042-6822(82)90429-9. PMID   6278715.
  16. ↑ Auperin DD, Compans RW, Bishop DH (August 1982). "Nucleotide sequence conservation at the 3' termini of the virion RNA species of New World and Old World arenaviruses". Virology. 121 (1): 200–3. doi:10.1016/0042-6822(82)90130-1. PMID   6287720.
  17. ↑ Mattsson L (1989). "Chronic non-A, non-B hepatitis with special reference to the transfusion-associated form". Scand J Infect Dis Suppl. 59: 1–55. doi:10.3109/inf.1988.20.suppl-59.01. PMID   2502835.
  18. 1 2 Hass M, Westerkofsky M, Müller S, Becker-Ziaja B, Busch C, Günther S (December 2006). "Mutational analysis of the lassa virus promoter". J. Virol. 80 (24): 12414–9. doi:10.1128/JVI.01374-06. PMC   1676312 . PMID   17005649.
  19. 1 2 Kranzusch PJ, Schenk AD, Rahmeh AA, et al. (November 2010). "Assembly of a functional Machupo virus polymerase complex". Proc. Natl. Acad. Sci. U.S.A. 107 (46): 20069–74. Bibcode:2010PNAS..10720069K. doi: 10.1073/pnas.1007152107 . PMC   2993349 . PMID   20978208.
  20. ↑ Bishop DH, Auperin DD (1987). "Arenavirus Gene Structure and Organization". Arenaviruses. Current Topics in Microbiology and Immunology. Vol. 133. pp. 5–17. doi:10.1007/978-3-642-71683-6_2. ISBN   978-3-642-71685-0. PMID   2435460.{{cite book}}: |journal= ignored (help)
  21. ↑ Young PR, Howard CR (April 1983). "Fine structure analysis of Pichinde virus nucleocapsids". J. Gen. Virol. 64 (4): 833–42. doi: 10.1099/0022-1317-64-4-833 . PMID   6682139.
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