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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 (28 February 2022) | Viewed by 41616

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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.

Prof. 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

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20 pages, 1391 KiB

Open AccessArticle

Pathophysiology of Influenza D Virus Infection in Specific-Pathogen-Free Lambs with or without Prior Mycoplasma ovipneumoniae Exposure

by Ema Robinson, Clyde Schulein, B. Tegner Jacobson, Kerri Jones, Jonathon Sago, Victor Huber, Mark Jutila, Diane Bimczok and Agnieszka Rynda-Apple

Viruses 2022, 14(7), 1422; https://0-doi-org.brum.beds.ac.uk/10.3390/v14071422 - 28 Jun 2022

Cited by 4 | Viewed by 2170

Abstract

Polymicrobial pneumonias occur frequently in cattle, swine, and sheep, resulting in major economic losses. Individual pathogens comprising these complex infections may be mild on their own but can instead exhibit synergism or increase host susceptibility. Two examples of such pathogens, Mycoplasma ovipneumoniae (M. ovipneumoniae) and influenza D viruses (IDVs), naturally infect domestic sheep. In sheep, the role of M. ovipneumoniae in chronic nonprogressive pneumonia is well-established, but the pathogenesis of IDV infection has not previously been studied. We utilized a specific-pathogen-free sheep flock to study the clinical response to IDV infection in naïve vs. M. ovipneumoniae-exposed lambs. Lambs were inoculated intranasally with M. ovipneumoniae or mock infection, followed after four weeks by infection with IDV. Pathogen shedding was tracked, and immunological responses were evaluated by measuring acute phase response and IDV-neutralizing antibody titers. While lamb health statuses remained subclinical, M. ovipneumoniae-exposed lambs had significantly elevated body temperatures during IDV infection compared to M. ovipneumoniae-naïve, IDV-infected lambs. Moreover, we found a positive correlation between prior M. ovipneumoniae burden, early-infection IDV shedding, and IDV-neutralizing antibody response. Our findings suggest that IDV infection may not induce clinical symptoms in domestic sheep, but previous M. ovipneumoniae exposure may promote mild IDV-associated inflammation. Full article

(This article belongs to the Special Issue Non-A Influenza 2.0)

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14 pages, 2583 KiB

Open AccessArticle

A Hemagglutinin Stem Vaccine Designed Rationally by AlphaFold2 Confers Broad Protection against Influenza B Infection

by Dian Zeng, Jiabao Xin, Kunyu Yang, Shuxin Guo, Qian Wang, Ying Gao, Huiqing Chen, Jiaqi Ge, Zhen Lu, Limin Zhang, Junyu Chen, Yixin Chen and Ningshao Xia

Viruses 2022, 14(6), 1305; https://0-doi-org.brum.beds.ac.uk/10.3390/v14061305 - 14 Jun 2022

Cited by 3 | Viewed by 4919

Abstract

Two lineages of influenza B viruses (IBV) co-circulating in human beings have been posing a significant public health burden worldwide. A substantial number of broadly neutralizing antibodies (bnAbs) have been identified targeting conserved epitopes on hemagglutinin (HA) stem domain, posing great interest for universal influenza vaccine development. Various strategies to design immunogens that selectively present these conserved epitopes are being explored. However, it has been a challenge to retain native conformation of the HA stem region, especially for soluble expression in prokaryotic systems. Here, using a structure prediction tool AlphaFold2, we rationally designed a stable stem antigen “B60-Stem-8071”, an HA stem vaccine derived from B/Brisbane/60/2006 grafted with a CR8071 epitope as a linker. The B60-Stem-8071 exhibited better solubility and more stable expression in the E. coli system compared to the naïve HA stem antigen. Immunization with B60-Stem-8071 in mice generated cross-reactive antibodies and protected mice broadly against lethal challenge with Yamagata and Victoria lineages of influenza B virus. Notably, soluble expression of B60-stem-8071 in the E. coli system showed the potential to produce the influenza B vaccine in a low-cost way. This study represents a proof of concept for the rational design of HA stem antigen based on structure prediction and analysis. Full article

(This article belongs to the Special Issue Non-A Influenza 2.0)

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9 pages, 868 KiB

Open AccessArticle

Experimental Infection of Horses with Influenza D Virus

by Chithra C. Sreenivasan, Tirth Uprety, Stephanie E. Reedy, Gun Temeeyasen, Ben M. Hause, Dan Wang, Feng Li and Thomas M. Chambers

Viruses 2022, 14(4), 661; https://0-doi-org.brum.beds.ac.uk/10.3390/v14040661 - 23 Mar 2022

Cited by 4 | Viewed by 2010

Abstract

Antibodies to influenza D virus (IDV) have been detected in horses, but no evidence of disease in the field has been reported. To determine whether IDV is infectious, immunogenic, and pathogenic in horses, four 2-year-old horses seronegative for both influenza A (H3N8) and D viruses were intranasally inoculated with 6.25 × 10⁷ TCID₅₀/animal of D/bovine/California/0363/2019 (D/CA2019) virus, using a portable equine nebulizer system. Horses were observed daily for clinical signs including rectal temperature, nasal discharge, coughing, lung sounds, tachycardia, and tachypnea. No horses exhibited clinical signs of disease. Nasopharyngeal swabs collected from 1–8 days post-infection demonstrated virus shedding by qRT-PCR. The horses showed evidence of seroconversion as early as 13 days post-infection (dpi) and the geometric mean of the antibody titers (GMT) of all four horses ranged from 16.82–160 as demonstrated by the microneutralization assay. Further, deep RNA sequencing of the virus isolated in embryonated chicken eggs revealed no adaptive mutations indicating that IDV can replicate in horses, suggesting the possibility of interspecies transmission of IDV with bovine reservoir into equids in nature. Full article

(This article belongs to the Special Issue Non-A Influenza 2.0)

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14 pages, 3560 KiB

Open AccessArticle

Incidence, Disease Severity, and Follow-Up of Influenza A/A, A/B, and B/B Virus Dual Infections in Children: A Hospital-Based Digital Surveillance Program

by Patrick E. Obermeier, Lea D. Seeber, Maren Alchikh, Brunhilde Schweiger and Barbara A. Rath

Viruses 2022, 14(3), 603; https://0-doi-org.brum.beds.ac.uk/10.3390/v14030603 - 14 Mar 2022

Cited by 1 | Viewed by 1856

Abstract

Influenza virus (IV) coinfection, i.e., simultaneous infection with IV and other viruses, is a common occurrence in humans. However, little is known about the incidence and clinical impact of coinfection with two different IV subtypes or lineages (“dual infections”). We report the incidence, standardized disease severity, and follow-up of IV dual infections from a hospital-based digital surveillance cohort, comprising 6073 pediatric patients fulfilling pre-defined criteria of influenza-like illness in Berlin, Germany. All patients were tested for IV A/B by PCR, including subtypes/lineages. We assessed all patients at the bedside using the mobile ViVI ScoreApp, providing a validated disease severity score in real-time. IV-positive patients underwent follow-up assessments until resolution of symptoms. Overall, IV dual infections were rare (4/6073 cases; 0.07%, incidence 12/100,000 per year) but showed unusual and/or prolonged clinical presentations with slightly above-average disease severity. We observed viral rebound, serial infection, and B/Yamagata-B/Victoria dual infection. Digital tools, used for instant clinical assessments at the bedside, combined with baseline/follow-up virologic investigation, help identify coinfections in cases of prolonged and/or complicated course of illness. Infection with one IV does not necessarily prevent consecutive or simultaneous (co-/dual) infection, highlighting the importance of multivalent influenza vaccination and enhanced digital clinical and virological surveillance. Full article

(This article belongs to the Special Issue Non-A Influenza 2.0)

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12 pages, 1103 KiB

Open AccessArticle

Characterization of Influenza D Virus in Danish Calves

by Nicole B. Goecke, Yuan Liang, Nina D. Otten, Charlotte K. Hjulsager and Lars E. Larsen

Viruses 2022, 14(2), 423; https://0-doi-org.brum.beds.ac.uk/10.3390/v14020423 - 18 Feb 2022

Cited by 5 | Viewed by 2528

Abstract

Influenza D virus (IDV) was first described in 2011 and has been found to mainly circulate among cattle and swine populations worldwide. Nasal swab samples were collected from 100 Danish calf herds (83 dairy and 17 veal herds) from 2018–2020. Influenza D virus was detected in 12 of the herds. Samples with the lowest cycle quantification value were selected for full genome sequencing. A hemagglutinin-esterase fusion (HEF) gene sequence from a Danish IDV collected in 2015 was also included in this study. Phylogenetic analysis showed that viruses from seven of the IDV-positive herds belonged to the D/OK lineage and clustered together in the HEF tree with the IDV collected in 2015. Viruses from the four other herds belonged to the D/660 lineage, where three of the viruses clustered closely together, while the fourth virus was more phylogenetically distant in all gene segments. The high level of genetic similarity between viruses from two different herds involved in calf trading suggests that transmission occurred through the movement of calves. This study is, to our knowledge, the first to describe the characterization of IDV in calves in Denmark. Full article

(This article belongs to the Special Issue Non-A Influenza 2.0)

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15 pages, 1990 KiB

Open AccessArticle

Human SUMOylation Pathway Is Critical for Influenza B Virus

by Runrui Dang, Victor G. J. Rodgers, Adolfo García-Sastre and Jiayu Liao

Viruses 2022, 14(2), 314; https://0-doi-org.brum.beds.ac.uk/10.3390/v14020314 - 03 Feb 2022

Cited by 1 | Viewed by 4941

Abstract

The identification and elucidation of host pathways for viral infection are critical for understanding the viral infection processes and novel therapeutics development. Here, for the first time, we discover that the human SUMOylation pathway is essential for the IBV viral life cycle. First, IBV viruses were completely inhibited by a novel SUMOylation specific inhibitor, STE025, discovered from our FRET-based high-throughput screening, and the inhibition was very potent, with IC₅₀~ 0.1 µM in an IBV-induced cell death rescue assay; Second, we determined that the IBV M1 protein was SUMOylated, which was mediated by the SUMOylation E2 conjugation enzyme and the E3 ligase enzyme at very high affinities, of 0.20 µM and 0.22 µM, respectively; Third, the mutation of the IBV M1 SUMOylation site, K21R, completely abolished the viral particle generation, strongly suggesting the requirement of SUMOylation for the IBV life cycle. These results suggest that the blockage of the host human SUMOylation pathway is very effective for IBV inhibition. We therefore propose that the host SUMOylation pathway is a critical host factor for the IBV virus life cycle. The identification and inhibition of critical host factor(s) provide a novel strategy for future anti-viral therapeutics development, such as IBV and other viruses. Full article

(This article belongs to the Special Issue Non-A Influenza 2.0)

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20 pages, 2862 KiB

Open AccessArticle

Time-Dependent Proinflammatory Responses Shape Virus Interference during Coinfections of Influenza A Virus and Influenza D Virus

by Minhui Guan, Sherry Blackmon, Alicia K. Olivier, Xiaojian Zhang, Liyuan Liu, Amelia Woolums, Mark A. Crenshaw, Shengfa F. Liao, Richard Webby, William Epperson and Xiu-Feng Wan

Viruses 2022, 14(2), 224; https://0-doi-org.brum.beds.ac.uk/10.3390/v14020224 - 24 Jan 2022

Cited by 5 | Viewed by 2487

Abstract

Both influenza A virus (IAV) and influenza D virus (IDV) are enzootic in pigs. IAV causes approximately 100% morbidity with low mortality, whereas IDV leads to only mild respiratory diseases in pigs. In this study, we performed a series of coinfection experiments in vitro and in vivo to understand how IAV and IDV interact and cause pathogenesis during coinfection. The results showed that IAV inhibited IDV replication when infecting swine tracheal epithelial cells (STECs) with IAV 24 or 48 h prior to IDV inoculation and that IDV suppressed IAV replication when IDV preceded IAV inoculation by 48 h. Virus interference was not identified during simultaneous IAV/IDV infections or with 6 h between the two viral infections, regardless of their order. The interference pattern at 24 and 48 h correlated with proinflammatory responses induced by the first infection, which, for IDV, was slower than for IAV by about 24 h. The viruses did not interfere with each other if both infected the cells before proinflammatory responses were induced. Coinfection in pigs further demonstrated that IAV interfered with both viral shedding and virus replication of IDV, especially in the upper respiratory tract. Clinically, coinfection of IDV and IAV did not show significant enhancement of disease pathogenesis, compared with the pigs infected with IAV alone. In summary, this study suggests that interference during coinfection of IAV and IDV is primarily due to the proinflammatory response; therefore, it is dependent on the time between infections and the order of infection. This study facilitates our understanding of virus epidemiology and pathogenesis associated with IAV and IDV coinfection. Full article

(This article belongs to the Special Issue Non-A Influenza 2.0)

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24 pages, 13516 KiB

Open AccessArticle

Cell-Adapted Mutations and Antigenic Diversity of Influenza B Viruses in Missouri, 2019–2020 Season

by Cynthia Y. Tang, Karen Segovia, Jane A. McElroy, Tao Li, Minhui Guan, Xiaojian Zhang, Shamita Misra, Jun Hang and Xiu-Feng Wan

Viruses 2021, 13(10), 1896; https://0-doi-org.brum.beds.ac.uk/10.3390/v13101896 - 22 Sep 2021

Cited by 3 | Viewed by 2642

Abstract

Influenza B viruses (IBVs) are causing an increasing burden of morbidity and mortality, yet the prevalence of culture-adapted mutations in human seasonal IBVs are unclear. We collected 368 clinical samples from patients with influenza-like illness in Missouri during the 2019–2020 influenza season and recovered 146 influenza isolates including 38 IBV isolates. Of MDCK-CCL34, MDCK-Siat1, and humanized MDCK (hCK), hCK showed the highest virus recovery efficiency. All Missourian IBVs belonged to the Victoria V1A.3 lineage, all of which contained a three-amino acid deletion on the HA protein and were antigenically distant from the Victoria lineage IBV vaccine strain used during that season. By comparing genomic sequences of these IBVs in 31 paired samples, eight cell-adapted nonsynonymous mutations were identified, with the majority in the RNA polymerase. Analyses of IBV clinical sample–isolate pairs from public databases further showed that cell- and egg-adapted mutations occurred more widely in viral proteins, including the receptor and antibody binding sites on HA. Our study suggests that hCK is an effective platform for IBV isolation and that culture-adapted mutations may occur during IBV isolation. As culture-adapted mutations may affect subsequent virus studies and vaccine development, the knowledge from this study may help optimize strategies for influenza surveillance, vaccine strain selection, and vaccine development. Full article

(This article belongs to the Special Issue Non-A Influenza 2.0)

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13 pages, 4456 KiB

Open AccessArticle

Tissue Microarrays to Visualize Influenza D Attachment to Host Receptors in the Respiratory Tract of Farm Animals

by Nikoloz Nemanichvili, Alinda J. Berends, Richard W. Wubbolts, Andrea Gröne, Jolianne M. Rijks, Robert P. de Vries and Monique H. Verheije

Viruses 2021, 13(4), 586; https://0-doi-org.brum.beds.ac.uk/10.3390/v13040586 - 31 Mar 2021

Cited by 8 | Viewed by 2613

Abstract

The trimeric hemagglutinin-esterase fusion protein (HEF) of influenza D virus (IDV) binds 9-O-acetylated sialic acid receptors, which are expressed in various host species. While cattle are the main reservoir for IDV, the viral genome has also been detected in domestic pigs. In addition, antibodies against IDV have been detected in other farm animals such as sheep, goats, and horses, and even in farmers working with IDV positive animals. Viruses belonging to various IDV clades circulate, but little is known about their differences in host and tissue tropism. Here we used recombinantly produced HEF proteins (HEF S57A) from the major clades D/Oklahoma (D/OK) and D/Oklahoma/660 (D/660) to study their host and tissue tropism and receptor interactions. To this end, we developed tissue microarrays (TMA) composed of respiratory tissues from various farm animals including cattle, domestic pigs, sheep, goats, and horses. Protein histochemical staining of farm animal respiratory tissue-microarrays with HEF proteins showed that cattle have receptors present over the entire respiratory tract while receptors are only present in the nasal and pharyngeal epithelium of pigs, sheep, goats, and horses. No differences in tropism for tissues and animals were observed between clades, while hemagglutination assays showed that D/OK has a 2-fold higher binding affinity than D/660 for receptors on red blood cells. The removal of O-acetylation from receptors via saponification treatment confirmed that receptor-binding of both clades was dependent on O-acetylated sialic acids. Full article

(This article belongs to the Special Issue Non-A Influenza 2.0)

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16 pages, 5202 KiB

Open AccessArticle

Establishment of a Reverse Genetic System from a Bovine Derived Influenza D Virus Isolate

by Melle Holwerda, Laura Laloli, Manon Wider, Lutz Schönecker, Jens Becker, Mireille Meylan and Ronald Dijkman

Viruses 2021, 13(3), 502; https://0-doi-org.brum.beds.ac.uk/10.3390/v13030502 - 18 Mar 2021

Cited by 3 | Viewed by 3813

Abstract

The ruminant-associated influenza D virus (IDV) has a broad host tropism and was shown to have zoonotic potential. To identify and characterize molecular viral determinants influencing the host spectrum of IDV, a reverse genetic system is required. For this, we first performed 5′ and 3′ rapid amplification of cDNA ends (RACE) of all seven genomic segments, followed by assessment of the 5′ and 3′ NCR activity prior to constructing the viral genomic segments of a contemporary Swiss bovine IDV isolate (D/CN286) into the bidirectional pHW2000 vector. The bidirectional plasmids were transfected in HRT-18G cells followed by viral rescue on the same cell type. Analysis of the segment specific 5′ and 3′ non-coding regions (NCR) highlighted that the terminal 3′ end of all segments harbours an uracil instead of a cytosine nucleotide, similar to other influenza viruses. Subsequent analysis on the functionality of the 5′ and 3′ NCR in a minireplicon assay revealed that these sequences were functional and that the variable sequence length of the 5′ and 3′ NCR influences reporter gene expression. Thereafter, we evaluated the replication efficiency of the reverse genetic clone on conventional cell lines of human, swine and bovine origin, as well as by using an in vitro model recapitulating the natural replication site of IDV in bovine and swine. This revealed that the reverse genetic clone D/CN286 replicates efficiently in all cell culture models. Combined, these results demonstrate the successful establishment of a reverse genetic system from a contemporary bovine IDV isolate that can be used for future identification and characterization of viral determinants influencing the broad host tropism of IDV. Full article

(This article belongs to the Special Issue Non-A Influenza 2.0)

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15 pages, 1832 KiB

Open AccessArticle

Growth Kinetics of Influenza C Virus Antigenic Mutants That Escaped from Anti-Hemagglutinin Esterase Monoclonal Antibodies and Viral Antigenic Changes Found in Field Isolates

by Yoko Matsuzaki, Kanetsu Sugawara, Yoshitaka Shimotai, Yoko Kadowaki, Seiji Hongo, Katsumi Mizuta and Hidekazu Nishimura

Viruses 2021, 13(3), 401; https://0-doi-org.brum.beds.ac.uk/10.3390/v13030401 - 03 Mar 2021

Cited by 3 | Viewed by 1603

Abstract

The antigenicity of the hemagglutinin esterase (HE) glycoprotein of influenza C virus is known to be stable; however, information about residues related to antigenic changes has not yet been fully acquired. Using selection with anti-HE monoclonal antibodies, we previously obtained some escape mutants and identified four antigenic sites, namely, A-1, A-2, A-3, and Y-1. To confirm whether the residues identified as the neutralizing epitope possibly relate to the antigenic drift, we analyzed the growth kinetics of these mutants. The results showed that some viruses with mutations in antigenic site A-1 were able to replicate to titers comparable to that of the wild-type, while others showed reduced titers. The mutants possessing substitutions in the A-2 or A-3 site replicated as efficiently as the wild-type virus. Although the mutant containing a deletion at positions 192 to 195 in the Y-1 site showed lower titers than the wild-type virus, it was confirmed that this region in the 190-loop on the top side of the HE protein is not essential for viral propagation. Then, we revealed that antigenic changes due to substitutions in the A-1, A-3, and/or Y-1 site had occurred in nature in Japan for the past 30 years. These results suggest that some residues (i.e., 125, 176, 192) in the A-1 site, residue 198 in the A-3 site, and residue 190 in the Y-1 site are likely to mediate antigenic drift while maintaining replicative ability. Full article

(This article belongs to the Special Issue Non-A Influenza 2.0)

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16 pages, 3258 KiB

Open AccessArticle

Features of Nuclear Export Signals of NS2 Protein of Influenza D Virus

by Lingcai Zhao, Huizhi Xia, Jingjin Huang, Yiqing Zheng, Chang Liu, Juan Su and Jihui Ping

Viruses 2020, 12(10), 1100; https://0-doi-org.brum.beds.ac.uk/10.3390/v12101100 - 29 Sep 2020

Cited by 10 | Viewed by 2956

Abstract

Emerging influenza D viruses (IDVs), the newest member in the genus Orthomyxovirus family, which can infect and transmit in multiple mammalian species as its relatives the influenza A viruses (IAVs). Additional studies of biological characteristics of IDVs are needed; here, we studied the characteristics of IDV nonstructural protein 2 (NS2), which shares the lowest homology to known influenza proteins. First, we generated reassortant viruses via reverse genetics to analyze the segment compatibility and gene interchangeability between IAVs and IDVs. Next, we investigated the locations and exact sequences of nuclear export signals (NESs) of the IDV NS2 protein. Surprisingly, three separate NES regions were found to contribute to the nuclear export of an eGFP fusion protein. Alanine scanning mutagenesis identified critical amino acid residues within each NES, and co-immunoprecipitation experiments demonstrated that their nuclear export activities depend on the CRM1-mediated pathway, particularly for the third NES (136-146aa) of IDV NS2. Interestingly, the third NES was important for the interaction of NS2 protein with CRM1. The findings in this study contribute to the understanding of IDV NS2 protein’s role during nucleocytoplasmic transport of influenza viral ribonucleoprotein complexes (vRNPs) and will also facilitate the development of novel anti-influenza drugs targeting nuclear export signals of IDV NS2 protein. Full article

(This article belongs to the Special Issue Non-A Influenza 2.0)

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10 pages, 1420 KiB

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Comparing Influenza Virus Biology for Understanding Influenza D Virus

by Raegan M. Skelton and Victor C. Huber

Viruses 2022, 14(5), 1036; https://0-doi-org.brum.beds.ac.uk/10.3390/v14051036 - 13 May 2022

Cited by 6 | Viewed by 5532

Abstract

The newest type of influenza virus, influenza D virus (IDV), was isolated in 2011. IDV circulates in several animal species worldwide, causing mild respiratory illness in its natural hosts. Importantly, IDV does not cause clinical disease in humans and does not spread easily from person to person. Here, we review what is known about the host–pathogen interactions that may limit IDV illness. We focus on early immune interactions between the virus and infected host cells in our summary of what is known about IDV pathogenesis. This work establishes a foundation for future research into IDV infection and immunity in mammalian hosts. Full article

(This article belongs to the Special Issue Non-A Influenza 2.0)

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