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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 (30 November 2019) | Viewed by 56270

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Prof. Dr. Feng Li

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Department of Veterinary Science, Department of Microbiology, Immunology, and Molecular Genetics, University of Kentucky, Lexington, KY 40506, USA
Interests: bovine influenza; influenza virology; rotavirus; veterinary virology
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Influenza viruses are a group of respiratory pathogens that have been classified into four types in the family Orthomyxoviridae: A, B, C, and D. Among them, influenza A and B viruses can cause moderate to severe illness in humans, with influenza A having the potential to trigger an influenza pandemic. Influenza C virus generally causes mild reparatory disease in humans, but its infection can be severe with complications including lower respiratory infection in children, especially those under two years. The recently discovered influenza D primarily affects agricultural animals, with bovines as a reservoir. Of greater public health importance, serological evidence of influenza D virus infection in humans has been recently demonstrated. Within global influenza research, influenza A has been primarily investigated due to its pandemic potential. In contrast, other types of influenza viruses, including influenza B with humans as a primary reservoir, have received considerably less attention. This Special Issue will feature the most recent research and findings on non-A influenza viruses, including epidemiology, evolution, cross-species transmission, molecular biology, antigenic lineage, virus–host interactions, antivirals and vaccine development.

Dr. Feng Li
Guest Editor

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Keywords

orthomyxoviruses
influenza B
influenza C
influenza D
epidemiology
evolution
transmission
molecular biology
antigenic lineage
reverse genetics
virus–host interactions
antivirals

Related Special Issues

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Non-A Influenza 2.0 in Viruses (13 articles)

Published Papers (14 papers)

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Research

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14 pages, 6994 KiB

Open AccessArticle

Experimental Infection Using Mouse-Adapted Influenza B Virus in a Mouse Model

by Elena Prokopyeva, Olga Kurskaya, Ivan Sobolev, Mariia Solomatina, Tatyana Murashkina, Anastasia Suvorova, Alexander Alekseev, Daria Danilenko, Andrey Komissarov, Artem Fadeev, Edward Ramsay, Alexander Shestopalov, Alexander Dygai and Kirill Sharshov

Viruses 2020, 12(4), 470; https://0-doi-org.brum.beds.ac.uk/10.3390/v12040470 - 21 Apr 2020

Cited by 6 | Viewed by 3475

Abstract

Every year, influenza B viruses (IBVs) contribute to annual illness, and infection can lead to serious respiratory disease among humans. More attention is needed in several areas, such as increasing virulence or pathogenicity of circulating B viruses and developing vaccines against current influenza. Since preclinical trials of anti-influenza drugs are mainly conducted in mice, we developed an appropriate infection model, using an antigenically-relevant IBV strain, for furtherance of anti-influenza drug testing and influenza vaccine protective efficacy analysis. A Victoria lineage (clade 1A) IBV was serially passaged 17 times in BALB/c mice, and adaptive amino acid substitutions were found in hemagglutinin (HA) (T214I) and neuraminidase (NA) (D432N). By electron microscopy, spherical and elliptical IBV forms were noted. Light microscopy showed that mouse-adapted IBVs caused influenza pneumonia on day 6 post inoculation. We evaluated the illness pathogenicity, viral load, and histopathological features of mouse-adapted IBVs and estimated anti-influenza drugs and vaccine efficiency in vitro and in vivo. Assessment of an investigational anti-influenza drug (oseltamivir ethoxysuccinate) and an influenza vaccine (Ultrix^®, SPBNIIVS, Saint Petersburg, Russia) showed effectiveness against the mouse-adapted influenza B virus. Full article

(This article belongs to the Special Issue Non-A Influenza)

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15 pages, 1845 KiB

Open AccessArticle

Next-Generation Sequencing Analysis of Cellular Response to Influenza B Virus Infection

by Zizhang Sheng, Chen Huang, Runxia Liu, Yicheng Guo, Zhiguang Ran, Feng Li and Dan Wang

Viruses 2020, 12(4), 383; https://0-doi-org.brum.beds.ac.uk/10.3390/v12040383 - 31 Mar 2020

Cited by 3 | Viewed by 3439

Abstract

Influenza B virus (IBV) is a respiratory pathogen that infects humans and causes seasonal influenza epidemics. However, cellular response to IBV infection in humans and mechanisms of host-mediated restriction of IBV replication are not thoroughly understood. In this study, we used next-generation sequencing (NGS) to perform transcriptome profiling of IBV-infected human lung epithelial A549 cells at 0, 6, 12, and 24 h post infection (hpi) and characterized the cellular gene expression dynamics. We observed that more than 4000 host genes were differentially regulated during the study period, which included up regulation of genes encoding proteins, having a role in the innate antiviral immune responses, immune activation, cellular metabolism, autophagy, and apoptosis, as well as down regulation of genes involved in mitosis and cell proliferation. Further analysis of RNA-Seq data coupled with RT-qPCR validation collectively showed that double-strand RNA recognition pathways, including retinoic acid-inducible gene I (RIG-I) and Toll-like receptor 3 (TLR3), were substantially activated following IBV infection. Taken together, these results provide important initial insights into the intimate interaction between IBV and lung epithelial cells, which can be further explored towards elucidation of the cellular mechanisms in restriction or elimination of IBV infections in humans. Full article

(This article belongs to the Special Issue Non-A Influenza)

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12 pages, 1324 KiB

Open AccessArticle

Risk Mapping of Influenza D Virus Occurrence in Ruminants and Swine in Togo Using a Spatial Multicriteria Decision Analysis Approach

by Maxime Fusade-Boyer, Pidemnéwé S. Pato, Mathias Komlan, Koffi Dogno, Komla Batawui, Emilie Go-Maro, Pamela McKenzie, Claire Guinat, Aurélie Secula, Mathilde Paul, Richard J. Webby, Annelise Tran, Agnès Waret-Szkuta and Mariette F. Ducatez

Viruses 2020, 12(2), 128; https://0-doi-org.brum.beds.ac.uk/10.3390/v12020128 - 21 Jan 2020

Cited by 15 | Viewed by 2902

Abstract

Influenza D virus (IDV) has been identified in several continents, with serological evidence for the virus in Africa. In order to improve the sensitivity and cost–benefit of IDV surveillance in Togo, risk maps were drawn using a spatial multicriteria decision analysis (MCDA) and experts’ opinion to evaluate the relevance of sampling areas used so far. Areas at highest risk of IDV occurrence were the main cattle markets. The maps were evaluated with previous field surveillance data collected in Togo between 2017 and 2019: 1216 sera from cattle, small ruminants, and swine were screened for antibodies to IDV by hemagglutination inhibition (HI) assays. While further samples collections are needed to validate the maps, the risk maps resulting from the spatial MCDA approach generated here highlight several priority areas for IDV circulation assessment. Full article

(This article belongs to the Special Issue Non-A Influenza)

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10 pages, 536 KiB

Open AccessArticle

Influenza D Virus: Serological Evidence in the Italian Population from 2005 to 2017

by Claudia M. Trombetta, Serena Marchi, Ilaria Manini, Otfried Kistner, Feng Li, Pietro Piu, Alessandro Manenti, Fabrizio Biuso, Chithra Sreenivasan, Julian Druce and Emanuele Montomoli

Viruses 2020, 12(1), 30; https://0-doi-org.brum.beds.ac.uk/10.3390/v12010030 - 27 Dec 2019

Cited by 43 | Viewed by 3868

Abstract

Influenza D virus is a novel influenza virus, which was first isolated from an ailing swine in 2011 and later detected in cattle, suggesting that these animals may be a primary natural reservoir. To date, few studies have been performed on human samples and there is no conclusive evidence on the ability of the virus to infect humans. The aim of this serological study was to assess the prevalence of antibodies against influenza D virus in human serum samples collected in Italy from 2005 to 2017. Serum samples were analysed by haemagglutination inhibition and virus neutralization assays. The results showed that the prevalence of antibodies against the virus increased in the human population in Italy from 2005 to 2017, with a trend characterized by a sharp increase in some years, followed by a decline in subsequent years. The virus showed the ability to infect and elicit an immune response in humans. However, prevalence peaks in humans appear to follow epidemics in animals and not to persist in the human population. Full article

(This article belongs to the Special Issue Non-A Influenza)

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11 pages, 649 KiB

Open AccessArticle

Assessment of Influenza D Virus in Domestic Pigs and Wild Boars in France: Apparent Limited Spread within Swine Populations Despite Serological Evidence of Breeding Sow Exposure

by Stéphane Gorin, Christelle Fablet, Stéphane Quéguiner, Nicolas Barbier, Frédéric Paboeuf, Séverine Hervé, Nicolas Rose and Gaëlle Simon

Viruses 2020, 12(1), 25; https://0-doi-org.brum.beds.ac.uk/10.3390/v12010025 - 24 Dec 2019

Cited by 20 | Viewed by 2898

Abstract

In order to assess influenza D virus (IDV) infections in swine in France, reference reagents were produced in specific pathogen free pigs to ensure serological and virological analyses. Hemagglutination inhibition (HI) assays were carried out on 2090 domestic pig sera collected in 2012–2018 in 102 farms. Only 31 sera from breeding sows sampled in 2014–2015 in six farrow-to-finish herds with respiratory disorders contained IDV-specific antibodies. In two of them, within-herd percentage of positive samples (73.3% and 13.3%, respectively) and HI titers (20–160) suggested IDV infections, but virus persistence was not confirmed following new sampling in 2017. All growing pigs tested seronegative, whatever their age and the sampling year. Moreover, PB1-gene RT-qPCR performed on 452 nasal swabs taken in 2015–2018 on pigs with acute respiratory syndrome (137 farms) gave negative results. In Corse, a Mediterranean island where pigs are mainly bred free-range, 2.3% of sera (n = 177) sampled on adult pigs in 2013–2014 obtained low HI titers. Finally, 0.5% of sera from wild boars hunted in 2009–2016 (n = 644) tested positive with low HI titers. These results provide the first serological evidence that sows were exposed to IDV in France but with a limited spread within the swine population. Full article

(This article belongs to the Special Issue Non-A Influenza)

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7 pages, 1923 KiB

Open AccessCommunication

Detection of a New Genetic Cluster of Influenza D Virus in Italian Cattle

by Chiara Chiapponi, Silvia Faccini, Alice Fusaro, Ana Moreno, Alice Prosperi, Marianna Merenda, Laura Baioni, Valentina Gabbi, Carlo Rosignoli, Giovanni L. Alborali, Lara Cavicchio, Isabella Monne, Camilla Torreggiani, Andrea Luppi and Emanuela Foni

Viruses 2019, 11(12), 1110; https://0-doi-org.brum.beds.ac.uk/10.3390/v11121110 - 30 Nov 2019

Cited by 23 | Viewed by 3364

Abstract

Influenza D virus (IDV) has been increasingly reported all over the world. Cattle are considered the major viral reservoir. Based on the hemagglutinin-esterase (HEF) gene, three main genetic and antigenic clusters have been identified: D/OK distributed worldwide, D/660 detected only in the USA and D/Japan in Japan. Up to 2017, all the Italian IDV isolates belonged to the D/OK genetic cluster. From January 2018 to May 2019, we performed virological surveillance for IDV from respiratory outbreaks in 725 bovine farms in Northern Italy by RT-PCR. Seventy-four farms were positive for IDV. A full or partial genome sequence was obtained from 29 samples. Unexpectedly, a phylogenetic analysis of the HEF gene showed the presence of 12 strains belonging to the D/660 cluster, previously unreported in Europe. The earliest D/660 strain was collected in March 2018 from cattle imported from France. Moreover, we detected one viral strain with a reassortant genetic pattern (PB2, PB1, P42, HEF and NP segments in the D/660 cluster, whilst P3 and NS segments in the D/OK cluster). These results confirm the circulation of IDV in the Italian cattle population and highlight the need to monitor the development of the spreading of this influenza virus in order to get more information about the epidemiology and the ecology of IDV viruses. Full article

(This article belongs to the Special Issue Non-A Influenza)

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12 pages, 3219 KiB

Open AccessArticle

Contribution of Host Immune Responses Against Influenza D Virus Infection Toward Secondary Bacterial Infection in a Mouse Model

by Raegan M. Skelton, Kelly M. Shepardson, Alexis Hatton, Patrick T. Wilson, Chithra Sreenivasan, Jieshi Yu, Dan Wang, Victor C. Huber and Agnieszka Rynda-Apple

Viruses 2019, 11(11), 994; https://0-doi-org.brum.beds.ac.uk/10.3390/v11110994 - 29 Oct 2019

Cited by 13 | Viewed by 3055

Abstract

Influenza D viruses (IDV) are known to co-circulate with viral and bacterial pathogens in cattle and other ruminants. Currently, there is limited knowledge regarding host responses to IDV infection and whether IDV infection affects host susceptibility to secondary bacterial infections. To begin to address this gap in knowledge, the current study utilized a combination of in vivo and in vitro approaches to evaluate host cellular responses against primary IDV infection and secondary bacterial infection with Staphylococcus aureus (S. aureus). Primary IDV infection in mice did not result in clinical signs of disease and it did not enhance the susceptibility to secondary S. aureus infection. Rather, IDV infection appeared to protect mice from the usual clinical features of secondary bacterial infection, as demonstrated by improved weight loss, survival, and recovery when compared to S. aureus infection alone. We found a notable increase in IFN-β expression following IDV infection while utilizing human alveolar epithelial A549 cells to analyze early anti-viral responses to IDV infection. These results demonstrate for the first time that IDV infection does not increase the susceptibility to secondary bacterial infection with S. aureus, with evidence that anti-viral immune responses during IDV infection might protect the host against these potentially deadly outcomes. Full article

(This article belongs to the Special Issue Non-A Influenza)

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16 pages, 6154 KiB

Open AccessArticle

High-Throughput MicroRNA Profiles of Permissive Madin-Darby Canine Kidney Cell Line Infected with Influenza B Viruses

by Suthat Saengchoowong, Kritsada Khongnomnan, Witthaya Poomipak, Kesmanee Praianantathavorn, Yong Poovorawan, Qibo Zhang and Sunchai Payungporn

Viruses 2019, 11(11), 986; https://0-doi-org.brum.beds.ac.uk/10.3390/v11110986 - 25 Oct 2019

Cited by 6 | Viewed by 2802

Abstract

Victoria and Yamagata lineages of influenza B viruses are globally circulating in seasonal epidemics. Madin–Darby canine kidney (MDCK) cells are permissive for viral isolation and vaccine manufacture. Nevertheless, the interplay between influenza B viruses and host microRNAs has not been investigated in this cell line. Therefore, the present study aims at high-throughput analysis of canine microRNA profile upon infection of influenza B viruses. Briefly, MDCK cells were infected with Victoria or Yamagata lineage at MOI of 0.01. After being harvested at 6, 12 and 24 h post infection, microRNAs were subjected to high-throughput sequencing based on MiSeq platform (Illumina). The results demonstrated that five microRNAs including cfa-miR-197, cfa-miR-215, cfa-miR361, cfa-miR-1841, and cfa-miR-1842 were overexpressed in both Victoria and Yamagata lineage infections. Interestingly, computational prediction showed that karyopherin alpha 6 (KPNA6) was targeted by cfa-miR-197 and cfa-miR-215. Moreover, the binding sites of both microRNAs were assessed by 3′-UTR reporter assay. The results showed that only cfa-miR-197 could bind to the target sites of KPNA6, leading to suppressing luciferase activity. Additionally, silencing of KPNA6 was confirmed by overexpression of cfa-miR-197. This study provides canine microRNA responses to seasonal influenza B viruses, suggesting that virus-mediated microRNAs might play crucial roles in host gene regulation. Full article

(This article belongs to the Special Issue Non-A Influenza)

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11 pages, 4126 KiB

Open AccessArticle

Comparison of Pathogenicity and Transmissibility of Influenza B and D Viruses in Pigs

by Jinhwa Lee, Liping Wang, Rachel Palinski, Tim Walsh, Dongchang He, Yonghai Li, Rui Wu, Yuekun Lang, Sun-Young Sunwoo, Juergen A. Richt and Wenjun Ma

Viruses 2019, 11(10), 905; https://0-doi-org.brum.beds.ac.uk/10.3390/v11100905 - 27 Sep 2019

Cited by 17 | Viewed by 3981

Abstract

Influenza viruses are important pathogens causing respiratory disease in humans and animals. In contrast to influenza A virus (IAV) that can infect a wide range of animal species, other influenza viruses, including influenza B virus (IBV), influenza C virus (ICV), and influenza D virus (IDV) have a limited host range. Swine can be infected with all four different genera of influenza viruses. IAV infection of pigs causes the well-known swine influenza that poses significant threats to human and animal health. However, influenza virus infection of pigs with IBV, ICV, and IDV are not well-characterized. Herein, we compared pathogenicity of IBV and IDV using intratracheal and intranasal infection of pigs, which are IAV seropositive, and commingled naïve pigs with the infected animals to determine their transmissibility. Both viruses caused fever and some lung lesions, replicated in the lungs of infected pigs, but only IDV transmitted to the contact animals. Although IBV and IDV displayed differing levels of replication in the respiratory tract of infected pigs, no significant differences in pathogenicity of both viruses were observed. These results indicate that both IBV and IDV can replicate, and are pathogenic in pigs. Full article

(This article belongs to the Special Issue Non-A Influenza)

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5 pages, 457 KiB

Open AccessArticle

Serological Evidence of Influenza D Virus Circulation Among Cattle and Small Ruminants in France

by Justine Oliva, Amit Eichenbaum, Jade Belin, Maria Gaudino, Jean Guillotin, Jean-Pierre Alzieu, Philippe Nicollet, Roland Brugidou, Eric Gueneau, Evelyne Michel, Gilles Meyer and Mariette F. Ducatez

Viruses 2019, 11(6), 516; https://0-doi-org.brum.beds.ac.uk/10.3390/v11060516 - 05 Jun 2019

Cited by 42 | Viewed by 4554

Abstract

Influenza D virus (IDV) has first been identified in 2011 in the USA and was shown to mainly circulate in cattle. While IDV is associated with mild respiratory signs, its prevalence is still unknown. In the present study we show that IDV has been circulating throughout France in cattle and small ruminants, with 47.2% and 1.5% seropositivity, respectively. The high prevalence and moderate pathogenicity of IDV in cattle suggest that it may play an initiating role in the bovine respiratory disease complex. Full article

(This article belongs to the Special Issue Non-A Influenza)

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16 pages, 3964 KiB

Open AccessArticle

Determining the Replication Kinetics and Cellular Tropism of Influenza D Virus on Primary Well-Differentiated Human Airway Epithelial Cells

by Melle Holwerda, Jenna Kelly, Laura Laloli, Isabel Stürmer, Jasmine Portmann, Hanspeter Stalder and Ronald Dijkman

Viruses 2019, 11(4), 377; https://0-doi-org.brum.beds.ac.uk/10.3390/v11040377 - 24 Apr 2019

Cited by 32 | Viewed by 6838

Abstract

Influenza viruses are notorious pathogens that frequently cross the species barrier with often severe consequences for both animal and human health. In 2011, a novel member of the Orthomyxoviridae family, Influenza D virus (IDV), was identified in the respiratory tract of swine. Epidemiological surveys revealed that IDV is distributed worldwide among livestock and that IDV-directed antibodies are detected in humans with occupational exposure to livestock. To identify the transmission capability of IDV to humans, we determined the viral replication kinetics and cell tropism using an in vitro respiratory epithelium model of humans. The inoculation of IDV revealed efficient replication kinetics and apical progeny virus release at different body temperatures. Intriguingly, the replication characteristics of IDV revealed higher replication kinetics compared to Influenza C virus, despite sharing the cell tropism preference for ciliated cells. Collectively, these results might indicate why IDV-directed antibodies are detected among humans with occupational exposure to livestock. Full article

(This article belongs to the Special Issue Non-A Influenza)

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18 pages, 2954 KiB

Open AccessArticle

Genetic Evolution and Molecular Selection of the HE Gene of Influenza C Virus

by Wenyan Zhang, Letian Zhang, Wanting He, Xu Zhang, Baiqing Wen, Congcong Wang, Qiuhua Xu, Gairu Li, Jiyong Zhou, Michael Veit and Shuo Su

Viruses 2019, 11(2), 167; https://0-doi-org.brum.beds.ac.uk/10.3390/v11020167 - 19 Feb 2019

Cited by 26 | Viewed by 4163

Abstract

Influenza C virus (ICV) was first identified in humans and swine, but recently also in cattle, indicating a wider host range and potential threat to both the livestock industry and public health than was originally anticipated. The ICV hemagglutinin-esterase (HE) glycoprotein has multiple functions in the viral replication cycle and is the major determinant of antigenicity. Here, we developed a comparative approach integrating genetics, molecular selection analysis, and structural biology to identify the codon usage and adaptive evolution of ICV. We show that ICV can be classified into six lineages, consistent with previous studies. The HE gene has a low codon usage bias, which may facilitate ICV replication by reducing competition during evolution. Natural selection, dinucleotide composition, and mutation pressure shape the codon usage patterns of the ICV HE gene, with natural selection being the most important factor. Codon adaptation index (CAI) and relative codon deoptimization index (RCDI) analysis revealed that the greatest adaption of ICV was to humans, followed by cattle and swine. Additionally, similarity index (SiD) analysis revealed that swine exerted a stronger evolutionary pressure on ICV than humans, which is considered the primary reservoir. Furthermore, a similar tendency was also observed in the M gene. Of note, we found HE residues 176, 194, and 198 to be under positive selection, which may be the result of escape from antibody responses. Our study provides useful information on the genetic evolution of ICV from a new perspective that can help devise prevention and control strategies. Full article

(This article belongs to the Special Issue Non-A Influenza)

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Review

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11 pages, 219 KiB

Open AccessReview

Epidemiology and Clinical Characteristics of Influenza C Virus

by Bethany K. Sederdahl and John V. Williams

Viruses 2020, 12(1), 89; https://0-doi-org.brum.beds.ac.uk/10.3390/v12010089 - 13 Jan 2020

Cited by 35 | Viewed by 4938

Abstract

Influenza C virus (ICV) is a common yet under-recognized cause of acute respiratory illness. ICV seropositivity has been found to be as high as 90% by 7–10 years of age, suggesting that most people are exposed to ICV at least once during childhood. Due to difficulty detecting ICV by cell culture, epidemiologic studies of ICV likely have underestimated the burden of ICV infection and disease. Recent development of highly sensitive RT-PCR has facilitated epidemiologic studies that provide further insights into the prevalence, seasonality, and course of ICV infection. In this review, we summarize the epidemiology and clinical characteristics of ICV. Full article

(This article belongs to the Special Issue Non-A Influenza)

13 pages, 1128 KiB

Open AccessReview

The Development and Use of Reporter Influenza B Viruses

by Rebekah E. Dumm and Nicholas S. Heaton

Viruses 2019, 11(8), 736; https://0-doi-org.brum.beds.ac.uk/10.3390/v11080736 - 09 Aug 2019

Cited by 7 | Viewed by 5262

Abstract

Influenza B viruses (IBVs) are major contributors to total human influenza disease, responsible for ~1/3 of all infections. These viruses, however, are relatively less studied than the related influenza A viruses (IAVs). While it has historically been assumed that the viral biology and mechanisms of pathogenesis for all influenza viruses were highly similar, studies have shown that IBVs possess unique characteristics. Relative to IAV, IBV encodes distinct viral proteins, displays a different mutational rate, has unique patterns of tropism, and elicits different immune responses. More work is therefore required to define the mechanisms of IBV pathogenesis. One valuable approach to characterize mechanisms of microbial disease is the use of genetically modified pathogens that harbor exogenous reporter genes. Over the last few years, IBV reporter viruses have been developed and used to provide new insights into the host response to infection, viral spread, and the testing of antiviral therapeutics. In this review, we will highlight the history and study of IBVs with particular emphasis on the use of genetically modified viruses and discuss some remaining gaps in knowledge that can be addressed using reporter expressing IBVs. Full article

(This article belongs to the Special Issue Non-A Influenza)

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