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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 (31 March 2019) | Viewed by 60660

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Dr. Xiao-Fang Yu

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W. Harry Feinstone Department, Molecular Microbiology & Immunology, Johns Hopkins University Bloomberg School of Public Health, 615 N. Wolfe St., Room E5148, Baltimore, MD 21205, USA
Interests: HIV; HBV; host restriction; innate immunity; vaccine; ubiquitin

Special Issue Information

Dear Colleagues,

The genus Enterovirus is comprised of a unique group of RNA viruses within the Picornaviridae family, including enterovirus, coxsackievirus, poliovirus, echovirus, and rhinovirus, which are causative agents of the widest spectrum of severe and deadly diseases (aseptic meningitis, neonatal sepsis- like disease, encephalitis, acute flaccid paralysis (AFP), non- specificfebrile illness, hand- foot- and- mouth disease (HFMD), herpangina, pleurodynia, pericarditis, and myocarditis) of higher vertebrates, including humans. To date, there are no effective prophylactics or therapeutic treatments available for the treatment of enterovirus diseases. The significance of enterovirus in human health, together with the limited existing intervesion strategies to combat enterovirus infection, makes it extremely urgent to better understand the biology of these viruses and to develop effective countermeasures to prevent them from infecting humans. The goal of this Special Issue is to provide a firm base for the most recent discoveries in enterovirus research, including the molecular and structural biology of the virus, virus–host interactions, viral pathogenesis, antiviral strategies, and vaccine development.

Dr. Xiao-Fang Yu
Guest Editor

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Keywords

Enterovirus
Coxsackievirus
Poliovirus
Echovirus
Rhinovirus
Hand-foot and-mouth disease
HFMD

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Published Papers (11 papers)

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13 pages, 2281 KiB

Open AccessArticle

Identification and Phylogenetic Characterization of Human Enteroviruses Isolated from Cases of Aseptic Meningitis in Brazil, 2013–2017

by Emanuelle Ramalho, Ivanildo Sousa, Jr., Fernanda Burlandy, Eliane Costa, Amanda Dias, Roseane Serrano, Maria Oliveira, Renato Lopes, Maria Debur, Marion Burger, Irina Riediger, Maria L. Oliveira, Osvaldo Nascimento and Edson E. da Silva

Viruses 2019, 11(8), 690; https://doi.org/10.3390/v11080690 - 29 Jul 2019

Cited by 29 | Viewed by 3418

Abstract

Aseptic meningitis is a common viral infection associated with human enteroviruses. The aim of the present study was to identify and characterize the enteroviruses associated with outbreaks and sporadic cases of aseptic meningitis that occurred in different regions of Brazil between 2013 and 2017. Cerebrospinal fluids obtained from patients admitted to public health facilities were analyzed. A total of 303 patients were positive for Human Enteroviruses (EV) by cell culture isolation with a median isolation rate throughout the year of 12%. We were able to identify enterovirus serotypes in 295 clinical specimens. Nineteen different serotypes were identified; the large majority corresponded to HEV-B species. Echovirus 30 (E-30) and Echovirus 6 (E-6) were the most prevalent genotypes (66.8%). Sequence analysis suggested that circulating E-30 was closely related to E-30 from other American countries; while E-6 was derived from Europe. Most of the patients consisted of children ≤ 15 years old. The temporal distribution of all aseptic meningitis and EV-positive cases showed an obvious seasonal pattern during autumn. Our results have provided valuable information about the enteroviral etiology of the aseptic meningitis cases in Brazil pointing to the importance of enterovirus surveillance in neurological diseases. Full article

(This article belongs to the Special Issue Enteroviruses)

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8 pages, 1189 KiB

Open AccessArticle

The Mechanism of Onychomadesis (Nail Shedding) and Beau’s Lines Following Hand-Foot-Mouth Disease

by Hsiu-Hui Chiu, Ming-Tsan Liu, Wen-Hung Chung, Yu-Shien Ko, Chin-Fang Lu, Cheng-Che E. Lan, Chun-Wei Lu and Kai-Che Wei

Viruses 2019, 11(6), 522; https://doi.org/10.3390/v11060522 - 6 Jun 2019

Cited by 16 | Viewed by 5528

Abstract

Background: Nail changes, including onychomadesis (nail shedding) and Beau’s line, following hand-foot-mouth disease (HFMD) are a common emergence at the stage of late complications of HFMD. However, the exact mechanism is still unknown. Therefore, we conducted this study to elucidate the mechanism of nail changes following HFMD. Methods: We collected 11 patients suffering from onychomadesis following HFMD. Nail samples from all of them were collected. Real time reverse transcription polymerase chain reaction (RT-PCR) and sequencing for human enteroviruses (HEV) were performed. Throat swabs for RT-PCR and sequencing for HEV were performed for three cases. Results: RT-PCR demonstrated the presence of Coxackievirus A6 (CVA6) in nail samples from three patients and one with Echovirus. Conclusion: In conclusion, we believe that the major cause of onychomadesis following HFMD is that certain novel viruses, mostly CVA6, are virulent and may damage nail matrix. Direct injury caused by cutaneous lesions of HFMD around nail matrix is a minor cause. There are still other virulent HEV which may result in onychomadesis. In addition, the novel strain of CVA6 also causes atypical clinical presentations, such as adult involvement and delayed-onset palmar and plantar desquamation. Physicians should be familiar with atypical presentations caused by novel viruses to avoid misdiagnosis and even inform patients of the possibility of onychomadesis that may take place weeks later to reassure patients. Full article

(This article belongs to the Special Issue Enteroviruses)

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12 pages, 4244 KiB

Open AccessArticle

Enterovirus A71 VP1 Variation A289T Decreases the Central Nervous System Infectivity via Attenuation of Interactions between VP1 and Vimentin In Vitro and In Vivo

by Huimin Zhu, Yujuan Cao, Weitao Su, Shan Huang, Weizhi Lu, Yezhen Zhou, Jing Gao, Wei Zhao, Bao Zhang and Xianbo Wu

Viruses 2019, 11(5), 467; https://doi.org/10.3390/v11050467 - 22 May 2019

Cited by 11 | Viewed by 3706

Abstract

Vimentin (VIM) is a surface receptor for enterovirus-A71, mediating the initial binding and subsequent increase in EV-A71 infectivity. The caspid protein VP1 variation, A289T, is reportedly closely associated with less severe central nervous system (CNS) infections in humans. However, it is unclear whether VIM is associated with a reduction in CNS infections of EV-A71 in the presence of A289T. We investigated whether VIM served as a receptor for EV-A71 in the presence of an A298T substitution in VP1. EV-A71-289A and EV-A71-289T were used to infect human rhabdomyosarcoma cells, control human brain microvascular endothelial cells (HBMECs), and VIM-knockout (KO) HBMECs and inoculated BALB/c mice, SV129 mice, and VIM-KO SV129 mice. Furthermore, we cloned VP1-289A-Flag and VP1-289T-Flag proteins for co-immunoprecipitation analysis. Analysis of viral function revealed that the capacity of viral attachment, replication, and protein synthesis and secretion decreased in HBMECs during an EV-A71-289A infection, the infectivity being higher than that of EV-A71-289T upon VIM-KO. Histopathological and immunohistochemical analyses of brain tissue revealed that cerebral cortical damage was more extensive in EV-A71-289A than in EV-A71-289T infections in control SV129 mice; however, no significant difference was observed upon VIM-KO. Co-immunoprecipitation analysis revealed an interaction between VP1 and VIM, which was attenuated in VP1 harboring A289T; however, this attenuation was reversed by VIM (1-58) peptide. The A289T variation of VP1 specifically decreased the virulence of EV-A71 in HBMECs, and the attenuated interaction between VP1 harboring the A289T variation and VIM essentially decreased the CNS infectivity of EV-A71 in vitro and vivo. Full article

(This article belongs to the Special Issue Enteroviruses)

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13 pages, 9891 KiB

Open AccessArticle

Environmental Surveillance for Poliovirus and Other Enteroviruses: Long-Term Experience in Moscow, Russian Federation, 2004–2017

by Olga E. Ivanova, Maria S. Yarmolskaya, Tatiana P. Eremeeva, Galina M. Babkina, Olga Y. Baykova, Lyudmila V. Akhmadishina, Alexandr Y. Krasota, Liubov I. Kozlovskaya and Alexander N. Lukashev

Viruses 2019, 11(5), 424; https://doi.org/10.3390/v11050424 - 8 May 2019

Cited by 44 | Viewed by 5035

Abstract

Polio and enterovirus surveillance may include a number of approaches, including incidence-based observation, a sentinel physician system, environmental monitoring and acute flaccid paralysis (AFP) surveillance. The relative value of these methods is widely debated. Here we summarized the results of 14 years of environmental surveillance at four sewage treatment plants of various capacities in Moscow, Russia. A total of 5450 samples were screened, yielding 1089 (20.0%) positive samples. There were 1168 viruses isolated including types 1–3 polioviruses (43%) and 29 different types of non-polio enteroviruses (51%). Despite using the same methodology, a significant variation in detection rates was observed between the treatment plants and within the same facility over time. The number of poliovirus isolates obtained from sewage was roughly 60 times higher than from AFP surveillance over the same time frame. All except one poliovirus isolate were Sabin-like polioviruses. The one isolate was vaccine-derived poliovirus type 2 with 17.6% difference from the corresponding Sabin strain, suggesting long-term circulation outside the scope of the surveillance. For some non-polio enterovirus types (e.g., Echovirus 6) there was a good correlation between detection in sewage and incidence of clinical cases in a given year, while other types (e.g., Echovirus 30) could cause large outbreaks and be almost absent in sewage samples. Therefore, sewage monitoring can be an important part of enterovirus surveillance, but cannot substitute other approaches. Full article

(This article belongs to the Special Issue Enteroviruses)

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10 pages, 1326 KiB

Open AccessArticle

Propagation of Rhinovirus C in Differentiated Immortalized Human Airway HBEC3-KT Epithelial Cells

by Mina Nakauchi, Noriyo Nagata, Ikuyo Takayama, Shinji Saito, Hideyuki Kubo, Atsushi Kaida, Kunihiro Oba, Takato Odagiri and Tsutomu Kageyama

Viruses 2019, 11(3), 216; https://doi.org/10.3390/v11030216 - 4 Mar 2019

Cited by 13 | Viewed by 5365

Abstract

Rhinoviruses (RVs) are classified into three species: RV-A, B, and C. Unlike RV-A and -B, RV-C cannot be propagated using standard cell culture systems. In order to isolate RV-Cs from clinical specimens and gain a better understanding of their biological properties and pathogenesis, we established air–liquid-interface (ALI) culture methods using HBEC3-KT and HSAEC1-KT immortalized human airway epithelial cells. HBEC3- and HSAEC1-ALI cultures morphologically resembled pseudostratified epithelia with cilia and goblet cells. Two fully sequenced clinical RV-C isolates, RV-C9 and -C53, were propagated in HBEC3-ALI cultures, and increases in viral RNA ranging from 1.71 log₁₀ to 7.06 log₁₀ copies were observed. However, this propagation did not occur in HSAEC1-ALI cultures. Using the HBEC3-ALI culture system, 11 clinical strains of RV-C were isolated from 23 clinical specimens, and of them, nine were passaged and re-propagated. The 11 clinical isolates were classified as RV-C2, -C6, -C9, -C12, -C18, -C23, -C40, and -C53 types according to their VP1 sequences. Our stable HBEC3-ALI culture system is the first cultivable cell model that supports the growth of multiple RV-C virus types from clinical specimens. Thus, the HBEC3-ALI culture system provides a cheap and easy-to-use alternative to existing cell models for isolating and investigating RV-Cs. Full article

(This article belongs to the Special Issue Enteroviruses)

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14 pages, 3489 KiB

Open AccessArticle

Staufen1 Protein Participates Positively in the Viral RNA Replication of Enterovirus 71

by Young-Mao Chen, Bo-Ting Ou, Chao-Ying Chen, Han-Hsiang Chan, Chih-Jung Chen and Robert YL Wang

Viruses 2019, 11(2), 142; https://doi.org/10.3390/v11020142 - 8 Feb 2019

Cited by 18 | Viewed by 3852

Abstract

The double-stranded RNA-binding protein Staufen1 (Stau1) has multiple functions during RNA virus infection. In this study, we investigated the role of Stau1 in viral translation by using a combination of enterovirus 71 (EV-A71) infection, RNA reporter transfection, and in vitro functional and biochemical assays. We demonstrated that Stau1 specifically binds to the 5′-untranslated region of EV-A71 viral RNA. The RNA-binding domain 2-3 of Stau1 is responsible for this binding ability. Subsequently, we created a Stau1 knockout cell line using the CRISPR/Cas9 approach to further characterize the functional role of Stau1’s interaction with viral RNA in the EV-A71-infected cells. Both the viral RNA accumulation and viral protein expression were downregulated in the Stau1 knockout cells compared with the wild-type naïve cells. Moreover, dysregulation of viral RNA translation was observed in the Stau1 knockout cells using ribosome fractionation assay, and a reduced RNA stability of 5′-UTR of the EV-A71 was also identified using an RNA stability assay, which indicated that Stau1 has a role in facilitating viral translation during EV-A71 infection. In conclusion, we determined the functional relevance of Stau1 in the EV-A71 infection cycle and herein describe the mechanism of Stau1 participation in viral RNA translation through its interaction with viral RNA. Our results suggest that Stau1 is an important host factor involved in viral translation and influential early in the EV-A71 replication cycle. Full article

(This article belongs to the Special Issue Enteroviruses)

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17 pages, 3563 KiB

Open AccessArticle

Viperin Inhibits Enterovirus A71 Replication by Interacting with Viral 2C Protein

by Chunyu Wei, Caishang Zheng, Jianhong Sun, Dan Luo, Yan Tang, Yuan Zhang, Xianliang Ke, Yan Liu, Zhenhua Zheng and Hanzhong Wang

Viruses 2019, 11(1), 13; https://doi.org/10.3390/v11010013 - 26 Dec 2018

Cited by 19 | Viewed by 5834

Abstract

Enterovirus A71 (EVA71) is a human enterovirus belonging to the Picornaviridae family and mostly causes hand-foot-and-mouth disease in infants. Viperin is an important interferon-stimulated gene with a broad antiviral activity against various viruses. However, the effect of viperin on human enteroviruses and the interaction mechanism between EVA71 and viperin remains elusive. Here, we confirmed the EVA71-induced expression of viperin in a mouse model and cell lines and showed that viperin upregulation by EVA71 infection occurred on both the mRNA and protein level. Viperin knockdown and overexpression in EVA71-infected cells indicated that this protein can markedly inhibit EVA71 infection. Interestingly, immunofluorescent confocal microscopy and co-immunoprecipitation assays indicated that viperin interacts and colocalizes with the EVA71 protein 2C in the endoplasmic reticulum. Furthermore, amino acids 50–60 in the N-terminal domain of viperin were the key residues responsible for viperin interaction with 2C. More importantly, the N-terminal domain of viperin was found responsible for inhibiting EVA71 replication. Our findings can potentially aid future research on the prevention and treatment of nervous system damage caused by EVA71 and may provide a potential target for antiviral therapy. Full article

(This article belongs to the Special Issue Enteroviruses)

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20 pages, 2533 KiB

Open AccessArticle

Toll-Like Receptor 3 Is Involved in Detection of Enterovirus A71 Infection and Targeted by Viral 2A Protease

by Kuan-Ru Chen, Chun-Keung Yu, Szu-Hao Kung, Shun-Hua Chen, Chuan-Fa Chang, Tzu-Chuan Ho, Yi-Ping Lee, Hung-Chuan Chang, Lan-Yin Huang, Shih-Yen Lo, Jui-Chung Chang and Pin Ling

Viruses 2018, 10(12), 689; https://doi.org/10.3390/v10120689 - 5 Dec 2018

Cited by 14 | Viewed by 4811

Abstract

Enterovirus A71 (EV-A71) has emerged as a major pathogen causing hand, foot, and mouth disease, as well as neurological disorders. The host immune response affects the outcomes of EV-A71 infection, leading to either resolution or disease progression. However, the mechanisms of how the mammalian innate immune system detects EV-A71 infection to elicit antiviral immunity remain elusive. Here, we report that the Toll-like receptor 3 (TLR3) is a key viral RNA sensor for sensing EV-A71 infection to trigger antiviral immunity. Expression of TLR3 in HEK293 cells enabled the cells to sense EV-A71 infection, leading to type I, IFN-mediated antiviral immunity. Viral double-stranded RNA derived from EV-A71 infection was a key ligand for TLR3 detection. Silencing of TLR3 in mouse and human primary immune cells impaired the activation of IFN-β upon EV-A71 infection, thus reinforcing the importance of the TLR3 pathway in defending against EV-A71 infection. Our results further demonstrated that TLR3 was a target of EV-A71 infection. EV-A71 protease 2A was implicated in the downregulation of TLR3. Together, our results not only demonstrate the importance of the TLR3 pathway in response to EV-A71 infection, but also reveal the involvement of EV-A71 protease 2A in subverting TLR3-mediated antiviral defenses. Full article

(This article belongs to the Special Issue Enteroviruses)

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13 pages, 547 KiB

Open AccessReview

Impact of Rhinovirus Infections in Children

by Silvia Vandini, Carlotta Biagi, Maximilian Fischer and Marcello Lanari

Viruses 2019, 11(6), 521; https://doi.org/10.3390/v11060521 - 5 Jun 2019

Cited by 57 | Viewed by 9796

Abstract

Rhinovirus (RV) is an RNA virus that causes more than 50% of upper respiratory tract infections in humans worldwide. Together with Respiratory Syncytial Virus, RV is one of the leading causes of viral bronchiolitis in infants and the most common virus associated with wheezing in children aged between one and two years. Because of its tremendous genetic diversity (>150 serotypes), the recurrence of RV infections each year is quite typical. Furthermore, because of its broad clinical spectrum, the clinical variability as well as the pathogenesis of RV infection are nowadays the subjects of an in-depth examination and have been the subject of several studies in the literature. In fact, the virus is responsible for direct cell cytotoxicity in only a small way, and it is now clearer than ever that it may act indirectly by triggering the release of active mediators by structural and inflammatory airway cells, causing the onset and/or the acute exacerbation of asthmatic events in predisposed children. In the present review, we aim to summarize the RV infection’s epidemiology, pathogenetic hypotheses, and available treatment options as well as its correlation with respiratory morbidity and mortality in the pediatric population. Full article

(This article belongs to the Special Issue Enteroviruses)

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13 pages, 1279 KiB

Open AccessReview

Current Understanding of Human Enterovirus D68

by Jing Sun, Xiao-Yi Hu and Xiao-Fang Yu

Viruses 2019, 11(6), 490; https://doi.org/10.3390/v11060490 - 29 May 2019

Cited by 45 | Viewed by 8433

Abstract

Human enterovirus D68 (EV-D68), a member of the species Enterovirus D of the Picornaviridae family, was first isolated in 1962 in the United States. EV-D68 infection was only infrequently reported until an outbreak occurred in 2014 in the US; since then, it has continued to increase worldwide. EV-D68 infection leads to severe respiratory illness and has recently been reported to be linked to the development of the neurogenic disease known as acute flaccid myelitis (AFM), mostly in children, seriously endangering public health. Hitherto, treatment options for EV-D68 infections were limited to supportive care, and as yet there are no approved, specific antiviral drugs or vaccines. Research on EV-D68 has mainly focused on its epidemiology, and its virologic characteristics and pathogenesis still need to be further explored. Here, we provide an overview of current research on EV-D68, including the genotypes and genetic characteristics of recent epidemics, the mechanism of infection and virus–host interactions, and its relationship to acute flaccid myelitis (AFM), in order to broaden our understanding of the biological features of EV-D68 and provide a basis for the development of effective antiviral agents. Full article

(This article belongs to the Special Issue Enteroviruses)

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7 pages, 503 KiB

Open AccessBrief Report

Detection and Characterization of Enterovirus B73 from a Child in Brazil

by Geovani de Oliveira Ribeiro, Adriana Luchs, Flávio Augusto de Pádua Milagres, Shirley Vasconcelos Komninakis, Danielle Elise Gill, Márcia Cristina Alves Brito Sayão Lobato, Rafael Brustulin, Rogério Togisaki das Chagas, Maria de Fátima Neves dos Santos Abrão, Cassia Vitória de Deus Alves Soares, Steven S. Witkin, Fabiola Villanova, Xutao Deng, Ester Cerdeira Sabino, Eric Delwart, Antonio Charlys Da Costa and Élcio Leal

Viruses 2019, 11(1), 16; https://doi.org/10.3390/v11010016 - 28 Dec 2018

Cited by 12 | Viewed by 3527

Abstract

Enterovirus B73 is a new member of the Enterovirus B species. First detected in the USA, it has been subsequently identified in China, India, Oman, and the Netherlands. In this study, we characterize the first B73 strain (named TO-127) to be detected in South America. TO-127 was obtained from a child with acute gastroenteritis living in a rural area in Northern Brazil. The subject was not infected with any known enteric pathogens such as norovirus, rotavirus, helminths, or enteric bacteria. Analysis of the nearly full-length TO-127 genome (6993 nt) indicated a 74–75% nucleotide similarity with EV-B73 strains from other countries. Evolutionary analysis suggests that B73 is endemic and widespread. Full article

(This article belongs to the Special Issue Enteroviruses)

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