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Recent Progress in Bunyavirus Research

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A special issue of Viruses (ISSN 1999-4915). This special issue belongs to the section "Animal Viruses".

Deadline for manuscript submissions: closed (29 February 2016) | Viewed by 122646

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Dr. Pierre-Yves Lozach

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CellNetworks—Cluster of Excellence and Center for Integrative Infectious Diseases Research (CIID), Department of Infectious Diseases, Virology, University Hospital Heidelberg, 69120 Heidelberg, Germany
Interests: amyloids; arbovirus; cell biology of virus entry; viral virulence factors
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Dr. Jane Tao

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Department of Biochemistry and Cell Biology, Rice University, Houston, MS 140, USA
Interests: RNA viruses, structure and function, assembly, viral RNA replication and transcription
Special Issues, Collections and Topics in MDPI journals

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Dear Colleagues,

The Bunyaviridae is the largest family of RNA viruses, with over 350 isolates worldwide distributed into five genera (i.e. Hantavirus, Orthobunyavirus, Nairovirus, Tospovirus, and Phlebovirus). Many of these viruses are significant human or agricultural pathogens. The increasing number of reports on new emerging bunyaviruses and infection episodes makes it essential that we obtain a comprehensive understanding of bunyaviruses and their infection mechanisms. Although all bunyaviruses possesses a tripartite, negative-sense (or ambi-sense) RNA genome, they exhibit substantial differences in their structure, genome organization and replication strategies, which make functional interpolation across genus boundaries difficult.

Fortunately, the bunyavirus field has witnessed many exciting new findings and breakthroughs in recent years. These discoveries span a wide spectrum of research areas, including structural characterization of viruses and viral proteins, the identification of new viruses, investigations into host switch and vectors of transmission, genome-based analysis of virus evolution and phylogenetic lineages, the development of new research tools such as replicons and reverse genetics, molecular characterization of the virus life cycle at the cell level (i.e. cell entry, replication, transcription, translation, genome packaging, reassortment, and virus assembly, etc.), studies of virus-host interactions and host antiviral defense, the development of vaccines/drugs and the use of bunyaviruses for novel applications.

In this special of Viruses, we would like to include both research and review papers that altogether can provide a glimpse into the latest research on bunyaviruses and at the same time highlight some of the important research achievements made in recent years. Study topics of both fundamental and applied nature are welcome. In doing so, we hope to gain an informed perspective of future research directions and also stimulate research in some of the understudied areas.

Dr. Jane Tao
Dr. Pierre-Yves Lozach
Guest Editors

Please find more related articles on this topic:
- RNA Encapsidation and Packaging in the Phleboviruses, by Hornak, K. et al.
- Viral RNA Silencing Suppression: The Enigma of Bunyavirus NSs Proteins, by Hedil M. and Kormelink R.

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Keywords

Bunyaviridae
Orthobunyavirus
Hantavirus
Phlebovirus
Nairovirus
Tospovirus
Emerging diseases
Vectors and transmission
Virus-host interactions
Bunyavirus entry
Bunyavirus replication
Bunyavirus assembly and release
Viral immunity
Reverse genetics
Vaccine development
Antiviral therapeutics

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Published Papers (13 papers)

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Research

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3413 KiB

Open AccessArticle

Genomic Characterization of the Genus Nairovirus (Family Bunyaviridae)

by Jens H. Kuhn, Michael R. Wiley, Sergio E. Rodriguez, Yīmíng Bào, Karla Prieto, Amelia P. A. Travassos da Rosa, Hilda Guzman, Nazir Savji, Jason T. Ladner, Robert B. Tesh, Jiro Wada, Peter B. Jahrling, Dennis A. Bente and Gustavo Palacios

Viruses 2016, 8(6), 164; https://doi.org/10.3390/v8060164 - 10 Jun 2016

Cited by 56 | Viewed by 11237

Abstract

Nairovirus, one of five bunyaviral genera, includes seven species. Genomic sequence information is limited for members of the Dera Ghazi Khan, Hughes, Qalyub, Sakhalin, and Thiafora nairovirus species. We used next-generation sequencing and historical virus-culture samples to determine 14 complete and nine coding-complete nairoviral genome sequences to further characterize these species. Previously unsequenced viruses include Abu Mina, Clo Mor, Great Saltee, Hughes, Raza, Sakhalin, Soldado, and Tillamook viruses. In addition, we present genomic sequence information on additional isolates of previously sequenced Avalon, Dugbe, Sapphire II, and Zirqa viruses. Finally, we identify Tunis virus, previously thought to be a phlebovirus, as an isolate of Abu Hammad virus. Phylogenetic analyses indicate the need for reassignment of Sapphire II virus to Dera Ghazi Khan nairovirus and reassignment of Hazara, Tofla, and Nairobi sheep disease viruses to novel species. We also propose new species for the Kasokero group (Kasokero, Leopards Hill, Yogue viruses), the Ketarah group (Gossas, Issyk-kul, Keterah/soft tick viruses) and the Burana group (Wēnzhōu tick virus, Huángpí tick virus 1, Tǎchéng tick virus 1). Our analyses emphasize the sister relationship of nairoviruses and arenaviruses, and indicate that several nairo-like viruses (Shāyáng spider virus 1, Xīnzhōu spider virus, Sānxiá water strider virus 1, South Bay virus, Wǔhàn millipede virus 2) require establishment of novel genera in a larger nairovirus-arenavirus supergroup. Full article

(This article belongs to the Special Issue Recent Progress in Bunyavirus Research)

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3124 KiB

Open AccessArticle

Mutational Analysis of the Rift Valley Fever Virus Glycoprotein Precursor Proteins for Gn Protein Expression

by Inaia Phoenix, Nandadeva Lokugamage, Shoko Nishiyama and Tetsuro Ikegami

Viruses 2016, 8(6), 151; https://doi.org/10.3390/v8060151 - 24 May 2016

Cited by 10 | Viewed by 6112

Abstract

The Rift Valley fever virus (RVFV) M-segment encodes the 78 kD, NSm, Gn, and Gc proteins. The 1st AUG generates the 78 kD-Gc precursor, the 2nd AUG generates the NSm-Gn-Gc precursor, and the 3rd AUG makes the NSm’-Gn-Gc precursor. To understand biological changes due to abolishment of the precursors, we quantitatively measured Gn secretion using a reporter assay, in which a Gaussia luciferase (gLuc) protein is fused to the RVFV M-segment pre-Gn region. Using the reporter assay, the relative expression of Gn/gLuc fusion proteins was analyzed among various AUG mutants. The reporter assay showed efficient secretion of Gn/gLuc protein from the precursor made from the 2nd AUG, while the removal of the untranslated region upstream of the 2nd AUG (AUG2-M) increased the secretion of the Gn/gLuc protein. Subsequently, recombinant MP-12 strains encoding mutations in the pre-Gn region were rescued, and virological phenotypes were characterized. Recombinant MP-12 encoding the AUG2-M mutation replicated slightly less efficiently than the control, indicating that viral replication is further influenced by the biological processes occurring after Gn expression, rather than the Gn abundance. This study showed that, not only the abolishment of AUG, but also the truncation of viral UTR, affects the expression of Gn protein by the RVFV M-segment. Full article

(This article belongs to the Special Issue Recent Progress in Bunyavirus Research)

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Open AccessArticle

N-Glycans on the Rift Valley Fever Virus Envelope Glycoproteins Gn and Gc Redundantly Support Viral Infection via DC-SIGN

by Inaia Phoenix, Shoko Nishiyama, Nandadeva Lokugamage, Terence E. Hill, Matthew B. Huante, Olga A.L. Slack, Victor H. Carpio, Alexander N. Freiberg and Tetsuro Ikegami

Viruses 2016, 8(5), 149; https://doi.org/10.3390/v8050149 - 23 May 2016

Cited by 28 | Viewed by 8467

Abstract

Rift Valley fever is a mosquito-transmitted, zoonotic disease that infects humans and ruminants. Dendritic cell specific intercellular adhesion molecule 3 (ICAM-3) grabbing non-integrin (DC-SIGN) acts as a receptor for members of the phlebovirus genus. The Rift Valley fever virus (RVFV) glycoproteins (Gn/Gc) encode five putative N-glycan sequons (asparagine (N)–any amino acid (X)–serine (S)/threonine (T)) at positions: N438 (Gn), and N794, N829, N1035, and N1077 (Gc). The N-glycosylation profile and significance in viral infection via DC-SIGN have not been elucidated. Gc N-glycosylation was first evaluated by using Gc asparagine (N) to glutamine (Q) mutants. Subsequently, we generated a series of recombinant RVFV MP-12 strain mutants, which encode N-to-Q mutations, and the infectivity of each mutant in Jurkat cells stably expressing DC-SIGN was evaluated. Results showed that Gc N794, N1035, and N1077 were N-glycosylated but N829 was not. Gc N1077 was heterogeneously N-glycosylated. RVFV Gc made two distinct N-glycoforms: “Gc-large” and “Gc-small”, and N1077 was responsible for “Gc-large” band. RVFV showed increased infection of cells expressing DC-SIGN compared to cells lacking DC-SIGN. Infection via DC-SIGN was increased in the presence of either Gn N438 or Gc N1077. Our study showed that N-glycans on the Gc and Gn surface glycoproteins redundantly support RVFV infection via DC-SIGN. Full article

(This article belongs to the Special Issue Recent Progress in Bunyavirus Research)

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Open AccessArticle

Experimental Infection of Calves by Two Genetically-Distinct Strains of Rift Valley Fever Virus

by William C. Wilson, A. Sally Davis, Natasha N. Gaudreault, Bonto Faburay, Jessie D. Trujillo, Vinay Shivanna, Sun Young Sunwoo, Aaron Balogh, Abaineh Endalew, Wenjun Ma, Barbara S. Drolet, Mark G. Ruder, Igor Morozov, D. Scott McVey and Juergen A. Richt

Viruses 2016, 8(5), 145; https://doi.org/10.3390/v8050145 - 23 May 2016

Cited by 29 | Viewed by 6593

Abstract

Recent outbreaks of Rift Valley fever in ruminant livestock, characterized by mass abortion and high mortality rates in neonates, have raised international interest in improving vaccine control strategies. Previously, we developed a reliable challenge model for sheep that improves the evaluation of existing and novel vaccines in sheep. This sheep model demonstrated differences in the pathogenesis of Rift Valley fever virus (RVFV) infection between two genetically-distinct wild-type strains of the virus, Saudi Arabia 2001 (SA01) and Kenya 2006 (Ken06). Here, we evaluated the pathogenicity of these two RVFV strains in mixed breed beef calves. There was a transient increase in rectal temperatures with both virus strains, but this clinical sign was less consistent than previously reported with sheep. Three of the five Ken06-infected animals had an early-onset viremia, one day post-infection (dpi), with viremia lasting at least three days. The same number of SA01-infected animals developed viremia at 2 dpi, but it only persisted through 3 dpi in one animal. The average virus titer for the SA01-infected calves was 1.6 logs less than for the Ken06-infected calves. Calves, inoculated with either strain, seroconverted by 5 dpi and showed time-dependent increases in their virus-neutralizing antibody titers. Consistent with the results obtained in the previous sheep study, elevated liver enzyme levels, more severe liver pathology and higher virus titers occurred with the Ken06 strain as compared to the SA01 strain. These results demonstrate the establishment of a virulent challenge model for vaccine evaluation in calves. Full article

(This article belongs to the Special Issue Recent Progress in Bunyavirus Research)

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2082 KiB

Open AccessArticle

Conserved Endonuclease Function of Hantavirus L Polymerase

by Sylvia Rothenberger, Giulia Torriani, Maria U. Johansson, Stefan Kunz and Olivier Engler

Viruses 2016, 8(5), 108; https://doi.org/10.3390/v8050108 - 2 May 2016

Cited by 8 | Viewed by 6898

Abstract

Hantaviruses are important emerging pathogens belonging to the Bunyaviridae family. Like other segmented negative strand RNA viruses, the RNA-dependent RNA polymerase (RdRp) also known as L protein of hantaviruses lacks an intrinsic “capping activity”. Hantaviruses therefore employ a “cap snatching” strategy acquiring short 5′ RNA sequences bearing 5′cap structures by endonucleolytic cleavage from host cell transcripts. The viral endonuclease activity implicated in cap snatching of hantaviruses has been mapped to the N-terminal domain of the L protein. Using a combination of molecular modeling and structure–function analysis we confirm and extend these findings providing evidence for high conservation of the L endonuclease between Old and New World hantaviruses. Recombinant hantavirus L endonuclease showed catalytic activity and a defined cation preference shared by other viral endonucleases. Based on the previously reported remarkably high activity of hantavirus L endonuclease, we established a cell-based assay for the hantavirus endonuclase function. The robustness of the assay and its high-throughput compatible format makes it suitable for small molecule drug screens to identify novel inhibitors of hantavirus endonuclease. Based on the high degree of similarity to RdRp endonucleases, some candidate inhibitors may be broadly active against hantaviruses and other emerging human pathogenic Bunyaviruses. Full article

(This article belongs to the Special Issue Recent Progress in Bunyavirus Research)

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11731 KiB

Open AccessArticle

Genetic and Phylogenetic Characterization of Tataguine and Witwatersrand Viruses and Other Orthobunyaviruses of the Anopheles A, Capim, Guamá, Koongol, Mapputta, Tete, and Turlock Serogroups

by Alexey M. Shchetinin, Dmitry K. Lvov, Petr G. Deriabin, Andrey G. Botikov, Asya K. Gitelman, Jens H. Kuhn and Sergey V. Alkhovsky

Viruses 2015, 7(11), 5987-6008; https://doi.org/10.3390/v7112918 - 23 Nov 2015

Cited by 32 | Viewed by 9005

Abstract

The family Bunyaviridae has more than 530 members that are distributed among five genera or remain to be classified. The genus Orthobunyavirus is the most diverse bunyaviral genus with more than 220 viruses that have been assigned to more than 18 serogroups based on serological cross-reactions and limited molecular-biological characterization. Sequence information for all three orthobunyaviral genome segments is only available for viruses belonging to the Bunyamwera, Bwamba/Pongola, California encephalitis, Gamboa, Group C, Mapputta, Nyando, and Simbu serogroups. Here we present coding-complete sequences for all three genome segments of 15 orthobunyaviruses belonging to the Anopheles A, Capim, Guamá, Kongool, Tete, and Turlock serogroups, and of two unclassified bunyaviruses previously not known to be orthobunyaviruses (Tataguine and Witwatersrand viruses). Using those sequence data, we established the most comprehensive phylogeny of the Orthobunyavirus genus to date, now covering 15 serogroups. Our results emphasize the high genetic diversity of orthobunyaviruses and reveal that the presence of the small nonstructural protein (NSs)-encoding open reading frame is not as common in orthobunyavirus genomes as previously thought. Full article

(This article belongs to the Special Issue Recent Progress in Bunyavirus Research)

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Review

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250 KiB

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What Do We Know about How Hantaviruses Interact with Their Different Hosts?

by Myriam Ermonval, Florence Baychelier and Noël Tordo

Viruses 2016, 8(8), 223; https://doi.org/10.3390/v8080223 - 11 Aug 2016

Cited by 62 | Viewed by 7221

Abstract

Hantaviruses, like other members of the Bunyaviridae family, are emerging viruses that are able to cause hemorrhagic fevers. Occasional transmission to humans is due to inhalation of contaminated aerosolized excreta from infected rodents. Hantaviruses are asymptomatic in their rodent or insectivore natural hosts with which they have co-evolved for millions of years. In contrast, hantaviruses cause different pathologies in humans with varying mortality rates, depending on the hantavirus species and its geographic origin. Cases of hemorrhagic fever with renal syndrome (HFRS) have been reported in Europe and Asia, while hantavirus cardiopulmonary syndromes (HCPS) are observed in the Americas. In some cases, diseases caused by Old World hantaviruses exhibit HCPS-like symptoms. Although the etiologic agents of HFRS were identified in the early 1980s, the way hantaviruses interact with their different hosts still remains elusive. What are the entry receptors? How do hantaviruses propagate in the organism and how do they cope with the immune system? This review summarizes recent data documenting interactions established by pathogenic and nonpathogenic hantaviruses with their natural or human hosts that could highlight their different outcomes. Full article

(This article belongs to the Special Issue Recent Progress in Bunyavirus Research)

1361 KiB

Open AccessReview

The Role of Phlebovirus Glycoproteins in Viral Entry, Assembly and Release

by Martin Spiegel, Teresa Plegge and Stefan Pöhlmann

Viruses 2016, 8(7), 202; https://doi.org/10.3390/v8070202 - 21 Jul 2016

Cited by 54 | Viewed by 11348

Abstract

Bunyaviruses are enveloped viruses with a tripartite RNA genome that can pose a serious threat to animal and human health. Members of the Phlebovirus genus of the family Bunyaviridae are transmitted by mosquitos and ticks to humans and include highly pathogenic agents like Rift Valley fever virus (RVFV) and severe fever with thrombocytopenia syndrome virus (SFTSV) as well as viruses that do not cause disease in humans, like Uukuniemi virus (UUKV). Phleboviruses and other bunyaviruses use their envelope proteins, Gn and Gc, for entry into target cells and for assembly of progeny particles in infected cells. Thus, binding of Gn and Gc to cell surface factors promotes viral attachment and uptake into cells and exposure to endosomal low pH induces Gc-driven fusion of the viral and the vesicle membranes. Moreover, Gn and Gc facilitate virion incorporation of the viral genome via their intracellular domains and Gn and Gc interactions allow the formation of a highly ordered glycoprotein lattice on the virion surface. Studies conducted in the last decade provided important insights into the configuration of phlebovirus Gn and Gc proteins in the viral membrane, the cellular factors used by phleboviruses for entry and the mechanisms employed by phlebovirus Gc proteins for membrane fusion. Here, we will review our knowledge on the glycoprotein biogenesis and the role of Gn and Gc proteins in the phlebovirus replication cycle. Full article

(This article belongs to the Special Issue Recent Progress in Bunyavirus Research)

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881 KiB

Open AccessReview

Phleboviruses and the Type I Interferon Response

by Jennifer Deborah Wuerth and Friedemann Weber

Viruses 2016, 8(6), 174; https://doi.org/10.3390/v8060174 - 22 Jun 2016

Cited by 77 | Viewed by 11672

Abstract

The genus Phlebovirus of the family Bunyaviridae contains a number of emerging virus species which pose a threat to both human and animal health. Most prominent members include Rift Valley fever virus (RVFV), sandfly fever Naples virus (SFNV), sandfly fever Sicilian virus (SFSV), Toscana virus (TOSV), Punta Toro virus (PTV), and the two new members severe fever with thrombocytopenia syndrome virus (SFTSV) and Heartland virus (HRTV). The nonstructural protein NSs is well established as the main phleboviral virulence factor in the mammalian host. NSs acts as antagonist of the antiviral type I interferon (IFN) system. Recent progress in the elucidation of the molecular functions of a growing list of NSs proteins highlights the astonishing variety of strategies employed by phleboviruses to evade the IFN system. Full article

(This article belongs to the Special Issue Recent Progress in Bunyavirus Research)

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2352 KiB

Open AccessReview

Early Bunyavirus-Host Cell Interactions

by Amelina Albornoz, Anja B. Hoffmann, Pierre-Yves Lozach and Nicole D. Tischler

Viruses 2016, 8(5), 143; https://doi.org/10.3390/v8050143 - 24 May 2016

Cited by 68 | Viewed by 13114

Abstract

The Bunyaviridae is the largest family of RNA viruses, with over 350 members worldwide. Several of these viruses cause severe diseases in livestock and humans. With an increasing number and frequency of outbreaks, bunyaviruses represent a growing threat to public health and agricultural productivity globally. Yet, the receptors, cellular factors and endocytic pathways used by these emerging pathogens to infect cells remain largely uncharacterized. The focus of this review is on the early steps of bunyavirus infection, from virus binding to penetration from endosomes. We address current knowledge and advances for members from each genus in the Bunyaviridae family regarding virus receptors, uptake, intracellular trafficking and fusion. Full article

(This article belongs to the Special Issue Recent Progress in Bunyavirus Research)

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685 KiB

Open AccessReview

Making Bunyaviruses Talk: Interrogation Tactics to Identify Host Factors Required for Infection

by Amber M. Riblett and Robert W. Doms

Viruses 2016, 8(5), 130; https://doi.org/10.3390/v8050130 - 13 May 2016

Cited by 3 | Viewed by 5605

Abstract

The identification of host cellular genes that act as either proviral or antiviral factors has been aided by the development of an increasingly large number of high-throughput screening approaches. Here, we review recent advances in which these new technologies have been used to interrogate host genes for the ability to impact bunyavirus infection, both in terms of technical advances as well as a summary of biological insights gained from these studies. Full article

(This article belongs to the Special Issue Recent Progress in Bunyavirus Research)

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4531 KiB

Open AccessReview

Molecular Insights into Crimean-Congo Hemorrhagic Fever Virus

by Marko Zivcec, Florine E. M. Scholte, Christina F. Spiropoulou, Jessica R. Spengler and Éric Bergeron

Viruses 2016, 8(4), 106; https://doi.org/10.3390/v8040106 - 21 Apr 2016

Cited by 94 | Viewed by 18863

Abstract

Crimean-Congo hemorrhagic fever virus (CCHFV) is a tick-borne pathogen that causes high morbidity and mortality. Efficacy of vaccines and antivirals to treat human CCHFV infections remains limited and controversial. Research into pathology and underlying molecular mechanisms of CCHFV and other nairoviruses is limited. Significant progress has been made in our understanding of CCHFV replication and pathogenesis in the past decade. Here we review the most recent molecular advances in CCHFV-related research, and provide perspectives on future research. Full article

(This article belongs to the Special Issue Recent Progress in Bunyavirus Research)

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Other

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134 KiB

Open AccessObituary

Homage to Richard M. Elliott

by Alain Kohl, Benjamin Brennan and Friedemann Weber

Viruses 2016, 8(8), 224; https://doi.org/10.3390/v8080224 - 10 Aug 2016

Cited by 1 | Viewed by 4249

Abstract

In the last 25 years, the scientiﬁc and public attention paid to bunyaviruses has increased considerably.[...] Full article

(This article belongs to the Special Issue Recent Progress in Bunyavirus Research)

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