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Yongguang Zhang
State Key Laboratory of Veterinary Etiological Biology, National/OIE Foot and Mouth Disease Reference Laboratory, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou 730046, China

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Journal article
Published: 27 May 2021 in Viruses
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An alternative vaccine design approach and diagnostic kits are highly required against the anticipated pandemicity caused by the South African Territories type 2 (SAT2) Foot and Mouth Disease Virus (FMDV). However, the distinct antigenicity and immunogenicity of VP1, VP0, and VP3 of FMDV serotype SAT2 are poorly understood. Similarly, the particular roles of the three structural proteins in novel vaccine design and development remain unexplained. We therefore constructed VP1, VP0, and VP3 encoding gene (SAT2:JX014256 strain) separately fused with His-SUMO (histidine-small ubiquitin-related modifier) inserted into pET-32a cassette to express the three recombinant proteins and separately evaluated their antigenicity and immunogenicity in mice. The fusion protein was successfully expressed and purified by the Ni-NTA resin chromatography. The level of serum antibody, spleen lymphocyte proliferation, and cytokines against the three distinct recombinant proteins were analyzed. Results showed that the anti-FMDV humoral response was triggered by these proteins, and the fusion proteins did enhance the splenocyte immune response in the separately immunized mice. We observed low variations among the three fusion proteins in terms of the antibody and cytokine production in mice. Hence, in this study, results demonstrated that the structural proteins of SAT2 FMDV could be used for the development of immunodiagnostic kits and subunit vaccine designs.

ACS Style

Guoxiu Li; Ashenafi Wubshet; Yaozhong Ding; Qian Li; Junfei Dai; Yang Wang; Qian Hou; Jiao Chen; Bing Ma; Anna Szczotka-Bochniarz; Susan Szathmary; Yongguang Zhang; Jie Zhang. Antigenicity and Immunogenicity Analysis of the E. coli Expressed FMDV Structural Proteins; VP1, VP0, VP3 of the South African Territories Type 2 Virus. Viruses 2021, 13, 1005 .

AMA Style

Guoxiu Li, Ashenafi Wubshet, Yaozhong Ding, Qian Li, Junfei Dai, Yang Wang, Qian Hou, Jiao Chen, Bing Ma, Anna Szczotka-Bochniarz, Susan Szathmary, Yongguang Zhang, Jie Zhang. Antigenicity and Immunogenicity Analysis of the E. coli Expressed FMDV Structural Proteins; VP1, VP0, VP3 of the South African Territories Type 2 Virus. Viruses. 2021; 13 (6):1005.

Chicago/Turabian Style

Guoxiu Li; Ashenafi Wubshet; Yaozhong Ding; Qian Li; Junfei Dai; Yang Wang; Qian Hou; Jiao Chen; Bing Ma; Anna Szczotka-Bochniarz; Susan Szathmary; Yongguang Zhang; Jie Zhang. 2021. "Antigenicity and Immunogenicity Analysis of the E. coli Expressed FMDV Structural Proteins; VP1, VP0, VP3 of the South African Territories Type 2 Virus." Viruses 13, no. 6: 1005.

Microbiology
Published: 23 April 2021 in Frontiers in Microbiology
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African swine fever (ASF) has caused huge economic losses to the swine industry worldwide. Since there is no commercial ASF vaccine available, an early diagnosis is extremely important to prevent and control the disease. In this study, ASF virus (ASFV) capsid protein-encoding gene (p72) was selected and used to design primers for establishing a one-step visual loop-mediated isothermal amplification (LAMP) assay with neutral red, a pH-sensitive dye, as the color shift indicator. Neutral red exhibited a sharp contrast of color change from faint orange (negative) to pink (positive) during LAMP for detection of ASFV. The designed primer set targeting highly conserved region of the p72 gene was highly specific to ASFV and showed no cross-reactivity with other swine viruses. The detection limit for the one-step visual LAMP developed was 10 copies/reaction based on the recombinant plasmid containing the p72 gene of ASFV. More importantly, the developed one-step visual LAMP showed high consistency with the results of the real-time polymerase chain reaction (qPCR) method recommended by World Organization for Animal Health (OIE). Furthermore, the results demonstrate that the colorimetric detection with this LAMP assay could be directly applied for the whole blood and serum samples without requiring genome extraction. Based on our results, the developed one-step visual LAMP assay is a promising penside diagnostic tool for development of early and cost-effective ASF monitoring program that would greatly contribute to the prevention and control of ASF.

ACS Style

Yang Wang; Junfei Dai; Yongsheng Liu; Jifei Yang; Qian Hou; Yunwen Ou; Yaozhong Ding; Bing Ma; Haotai Chen; Miaomiao Li; Yuefeng Sun; Haixue Zheng; Keshan Zhang; Ashenafi Kiros Wubshet; Alexei D. Zaberezhny; Taras I. Aliper; Kazimierz Tarasiuk; Zygmunt Pejsak; Zhijie Liu; Yongguang Zhang; Jie Zhang. Development of a Potential Penside Colorimetric LAMP Assay Using Neutral Red for Detection of African Swine Fever Virus. Frontiers in Microbiology 2021, 12, 1 .

AMA Style

Yang Wang, Junfei Dai, Yongsheng Liu, Jifei Yang, Qian Hou, Yunwen Ou, Yaozhong Ding, Bing Ma, Haotai Chen, Miaomiao Li, Yuefeng Sun, Haixue Zheng, Keshan Zhang, Ashenafi Kiros Wubshet, Alexei D. Zaberezhny, Taras I. Aliper, Kazimierz Tarasiuk, Zygmunt Pejsak, Zhijie Liu, Yongguang Zhang, Jie Zhang. Development of a Potential Penside Colorimetric LAMP Assay Using Neutral Red for Detection of African Swine Fever Virus. Frontiers in Microbiology. 2021; 12 ():1.

Chicago/Turabian Style

Yang Wang; Junfei Dai; Yongsheng Liu; Jifei Yang; Qian Hou; Yunwen Ou; Yaozhong Ding; Bing Ma; Haotai Chen; Miaomiao Li; Yuefeng Sun; Haixue Zheng; Keshan Zhang; Ashenafi Kiros Wubshet; Alexei D. Zaberezhny; Taras I. Aliper; Kazimierz Tarasiuk; Zygmunt Pejsak; Zhijie Liu; Yongguang Zhang; Jie Zhang. 2021. "Development of a Potential Penside Colorimetric LAMP Assay Using Neutral Red for Detection of African Swine Fever Virus." Frontiers in Microbiology 12, no. : 1.

Original article
Published: 25 January 2021 in The FEBS Journal
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Inhibitor of DNA‐binding 1 (ID1) protein has been studied intensively for its functions in tumorigenesis and maintenance of stem cell‐like properties, but its roles in virus infection are less understood. In the present study, we have clearly shown that the foot‐and‐mouth disease virus (FMDV) promotes ID1 degradation via Cdh1‐mediated ubiquitination to facilitate its replication. Mechanistic investigations reveal Forkhead Box O1 (FOXO1) as an ID1 partner, which suppresses interferon regulatory factors 3 expression and interferon (IFN) production. Further investigation identified that ID1 suppresses FOXO1 transcription activity through HDAC4‐mediated deacetylation, promoting IFN production and antiviral immune response. These studies establish a prominent role for ID1 in suppressing FDMV replication, which may be extended to other viruses.

ACS Style

Tingting Ren; Haotai Chen; Xinsheng Liu; Yanxue Wang; Aixia Fan; Linlin Qi; Li Pan; Wenlong Bai; Yongguang Zhang; Yuefeng Sun. ID1 inhibits foot‐and‐mouth disease virus replication via targeting of interferon pathways. The FEBS Journal 2021, 1 .

AMA Style

Tingting Ren, Haotai Chen, Xinsheng Liu, Yanxue Wang, Aixia Fan, Linlin Qi, Li Pan, Wenlong Bai, Yongguang Zhang, Yuefeng Sun. ID1 inhibits foot‐and‐mouth disease virus replication via targeting of interferon pathways. The FEBS Journal. 2021; ():1.

Chicago/Turabian Style

Tingting Ren; Haotai Chen; Xinsheng Liu; Yanxue Wang; Aixia Fan; Linlin Qi; Li Pan; Wenlong Bai; Yongguang Zhang; Yuefeng Sun. 2021. "ID1 inhibits foot‐and‐mouth disease virus replication via targeting of interferon pathways." The FEBS Journal , no. : 1.

Journal article
Published: 27 September 2020 in Genes
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Emerging evidence indicates that the host microRNAs (miRNAs) are important intracellular regulators and play pivotal roles in intricate host-pathogen interaction networks. In our previous studies, ssc-microRNA-4334-5p (miR-4334-5p) was identified as a differentially expressed miRNA in microarray-based miRNAs profiling experiment, but whether miR-4334-5p regulates foot and mouth disease virus (FMDV) propagation is less understood. Here, we demonstrated that miR-4334-5p expression level was up-regulated shortly after FMDV infection, transfection of miR-4334-5p mimics promoted, while inhibitor transfection suppressed FMDV replication correspondingly. Further bioinformatic analysis and experimental study suggested ID1 was the direct target of miR-4334-5p, suppressing FMDV replication by regulating interferon (IFN) pathways. These findings shed light on microRNAs-ID1-interferon axis in regulating FMDV replication.

ACS Style

Yanxue Wang; Tingting Ren; Haotai Chen; Kailing Wang; Yongguang Zhang; Lei Liu; Yuefeng Sun. MiR-4334-5p Facilitates Foot and Mouth Disease Virus Propagation by Suppressing Interferon Pathways via Direct Targeting ID1. Genes 2020, 11, 1136 .

AMA Style

Yanxue Wang, Tingting Ren, Haotai Chen, Kailing Wang, Yongguang Zhang, Lei Liu, Yuefeng Sun. MiR-4334-5p Facilitates Foot and Mouth Disease Virus Propagation by Suppressing Interferon Pathways via Direct Targeting ID1. Genes. 2020; 11 (10):1136.

Chicago/Turabian Style

Yanxue Wang; Tingting Ren; Haotai Chen; Kailing Wang; Yongguang Zhang; Lei Liu; Yuefeng Sun. 2020. "MiR-4334-5p Facilitates Foot and Mouth Disease Virus Propagation by Suppressing Interferon Pathways via Direct Targeting ID1." Genes 11, no. 10: 1136.

Journal article
Published: 20 June 2020 in Virus Research
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MicroRNAs play vital roles in regulating the battle between pathogens and host cells during viral challenging. MiR-4331 aggravates transmissible gastroenteritis virus (TGEV) -induced mitochondrial damage, also suppresses transcription of TGEV gene 7 via targeting cellular CDCA7. Otherwise, miR-4331-5p affects H1N1/2009 influenza A virus replication by targeting viral HA and NS. However, whether microRNA ssc-miR-4331-5p (miR-4331-5p) regulates foot and mouth virus (FMDV) replication remains unclear. To explore the role of miR-4331-5p in FMDV infection, we detected the expression level of miR-4331-5p in porcine kidney (PK-15) cells. The results showed that FMDV infection directly upregulates miR-4331-5p expression, while transfection of mimics or inhibitor of miR-4331-5p promotes or inhibits FMDV replication. Further investigation clearly showed that miR-4331-5p increases FMDV replication through inhibiting type I interferon pathways. These data demonstrate that miR-4331-5p plays an important role in regulating FMDV replication.

ACS Style

Tingting Ren; Yanxue Wang; Haotai Chen; Kailing Wang; Xin Gao; Lei Liu; Yongguang Zhang; Yuefeng Sun. MicroRNA-4331-5p promotes FMDV replication through inhibiting interferon pathways in PK-15 cells. Virus Research 2020, 286, 198064 .

AMA Style

Tingting Ren, Yanxue Wang, Haotai Chen, Kailing Wang, Xin Gao, Lei Liu, Yongguang Zhang, Yuefeng Sun. MicroRNA-4331-5p promotes FMDV replication through inhibiting interferon pathways in PK-15 cells. Virus Research. 2020; 286 ():198064.

Chicago/Turabian Style

Tingting Ren; Yanxue Wang; Haotai Chen; Kailing Wang; Xin Gao; Lei Liu; Yongguang Zhang; Yuefeng Sun. 2020. "MicroRNA-4331-5p promotes FMDV replication through inhibiting interferon pathways in PK-15 cells." Virus Research 286, no. : 198064.

Brief report
Published: 12 May 2020 in Archives of Virology
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Although porcine deltacoronavirus (PDCoV) is a significant pandemic threat in the swine population and has caused significant economic losses, information regarding the immune response in conventionally weaned pigs infected with PDCoV is scarce. Hence, the immune response in conventionally weaned pigs infected with PDCoV was assessed after challenge and rechallenge. After the first challenge, obvious diarrhea and viral shedding developed successively in all pigs in the four inoculation dose groups from 3 to 14 days postinfection (dpi), and all pigs recovered (no clinical symptoms or viral shedding) by 21 dpi. All pigs in the four groups exhibited significantly increased PDCoV-specific IgG, IgA and virus-neutralizing (VN) antibody (Ab) titers and IFN-γ levels in the serum after the first challenge. All pigs were completely protected against rechallenge at 21 dpi. The serum levels of PDCoV-specific IgG, IgA, and VN Abs increased further after rechallenge. Notably, the IFN-γ level declined continuously after 7 dpi. In addition, the levels of PDCoV-specific IgG, IgA and VN Abs in saliva increased significantly after rechallenge and correlated well with the serum Ab titers. Furthermore, the appearance of clinical symptoms of PDCoV infection in conventionally weaned pigs was delayed with reduced inoculation doses. In summary, the data presented here offer important reference information for future PDCoV animal infection and vaccine-induced immunoprotection experiments.

ACS Style

Donghong Zhao; Xiang Gao; Peng Zhou; Liping Zhang; Yongguang Zhang; Yonglu Wang; Xinsheng Liu. Evaluation of the immune response in conventionally weaned pigs infected with porcine deltacoronavirus. Archives of Virology 2020, 165, 1653 -1658.

AMA Style

Donghong Zhao, Xiang Gao, Peng Zhou, Liping Zhang, Yongguang Zhang, Yonglu Wang, Xinsheng Liu. Evaluation of the immune response in conventionally weaned pigs infected with porcine deltacoronavirus. Archives of Virology. 2020; 165 (7):1653-1658.

Chicago/Turabian Style

Donghong Zhao; Xiang Gao; Peng Zhou; Liping Zhang; Yongguang Zhang; Yonglu Wang; Xinsheng Liu. 2020. "Evaluation of the immune response in conventionally weaned pigs infected with porcine deltacoronavirus." Archives of Virology 165, no. 7: 1653-1658.

Journal article
Published: 07 May 2020 in BMC Veterinary Research
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Background Porcine Deltacoronavirus (PDCoV) is a newly emerging Coronavirus that was first identified in 2012 in Hong Kong, China. Since then, PDCoV has subsequently been reported worldwide, causing a high number of neonatal piglet deaths and significant economic losses to the swine industry. Therefore, it is necessary to establish a highly sensitive and specific method for the rapid diagnosis of PDCoV. Results In the present study, a highly sensitive and specific diagnostic method using recombinase polymerase amplification combined with a lateral flow dipstick (LFD-RPA) was developed for rapid and visual detection of PDCoV. The system can be performed under a broad range of temperature conditions from 10 to 37 °C, and the detection of PDCoV can be completed in 10 min at 37 °C. The sensitivity of this assay was 10 times higher than that of conventional PCR with a lower detection limit of 1 × 102 copies/µl of PDCoV. Meanwhile, the LFD-RPA assay specifically amplified PDCoV, while there was no cross-amplification with other swine-associated viruses, including Porcine epidemic diarrhea virus (PEDV), Transmissible gastroenteritis virus (TGEV), Porcine kobuvirus (PKoV), Foot and mouth disease virus (FMDV), Porcine reproductive and respiratory syndrome virus (PRRSV), Porcine circovirus type 2 (PCV2), Classical swine fever virus (CSFV) and Seneca valley virus (SVV). The repeatability of the test results indicated that this assay had good repeatability. In addition, 68 clinical samples (48 fecal swab specimens and 20 intestinal specimens) were further tested by LFD-RPA and RT-PCR assay. The positive rate of LFD-RPA clinical samples was 26.47% higher than that of conventional PCR (23.53%). Conclusions The LFD-RPA assay successfully detected PDCoV in less than 20 min in this study, providing a potentially valuable tool to improve molecular detection for PDCoV and to monitor the outbreak of PDCoV, especially in low-resource areas and laboratories.

ACS Style

Xiang Gao; Xinsheng Liu; Yongguang Zhang; Yanming Wei; Yonglu Wang. Rapid and visual detection of porcine deltacoronavirus by recombinase polymerase amplification combined with a lateral flow dipstick. BMC Veterinary Research 2020, 16, 130 -8.

AMA Style

Xiang Gao, Xinsheng Liu, Yongguang Zhang, Yanming Wei, Yonglu Wang. Rapid and visual detection of porcine deltacoronavirus by recombinase polymerase amplification combined with a lateral flow dipstick. BMC Veterinary Research. 2020; 16 (1):130-8.

Chicago/Turabian Style

Xiang Gao; Xinsheng Liu; Yongguang Zhang; Yanming Wei; Yonglu Wang. 2020. "Rapid and visual detection of porcine deltacoronavirus by recombinase polymerase amplification combined with a lateral flow dipstick." BMC Veterinary Research 16, no. 1: 130-8.

Journal article
Published: 02 April 2020 in Virus Research
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Porcine deltacoronavirus (PDCoV) is a novel swine enteropathogenic coronavirus that causes acute diarrhea, vomiting, dehydration and mortality in neonatal piglets, resulting in significant economic losses to the pig industry. However, there is currently little information on vaccine studies and commercially available vaccines for PDCoV. Hence, herein, a PDCoV strain, CH/XJYN/2016, was successfully isolated and serially propagated in vitro, and its biological characteristics were determined. Compared to that of previously reported and recently isolated PDCoV strains from China and the United States, the S gene of the CH/XJYN/2016 strain contains novel mutations. Infection studies revealed that CH/XJYN/2016 is pathogenic to suckling piglets and conventional weaned pigs. In addition, the median pig diarrhea dose (PDD50) of PDCoV in conventional weaned pigs was determined (2.0 log10PDD50/3 mL). Furthermore, an inactivated cell-adapted CH/XJYN/2016-based vaccine candidate was developed with different adjuvants. Compared with nonvaccinated pigs, conventional weaned pigs given the inactivated vaccine developed a potent humoral immune response and showed no clinical signs or viral shedding after challenge, indicating a potent protective effect of the vaccine against PDCoV infection. Therefore, the PDCoV vaccine developed in this study is a promising vaccine candidate that can be used for the control of PDCoV infection in pigs.

ACS Style

Xiang Gao; Donghong Zhao; Peng Zhou; Liping Zhang; Mingxia Li; Weiyan Li; Yongguang Zhang; Yonglu Wang; Xinsheng Liu. Characterization, pathogenicity and protective efficacy of a cell culture-derived porcine deltacoronavirus. Virus Research 2020, 282, 197955 -197955.

AMA Style

Xiang Gao, Donghong Zhao, Peng Zhou, Liping Zhang, Mingxia Li, Weiyan Li, Yongguang Zhang, Yonglu Wang, Xinsheng Liu. Characterization, pathogenicity and protective efficacy of a cell culture-derived porcine deltacoronavirus. Virus Research. 2020; 282 ():197955-197955.

Chicago/Turabian Style

Xiang Gao; Donghong Zhao; Peng Zhou; Liping Zhang; Mingxia Li; Weiyan Li; Yongguang Zhang; Yonglu Wang; Xinsheng Liu. 2020. "Characterization, pathogenicity and protective efficacy of a cell culture-derived porcine deltacoronavirus." Virus Research 282, no. : 197955-197955.

Journal article
Published: 18 March 2020 in Molecular Immunology
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Foot-and-mouth disease (FMD) is an acute, severe, and highly contagious disease that affects cloven-hoofed animals and can lead to serious economic losses and social effects. Therefore, a safe and effective subunit vaccine is required to prevent and control FMD. Dendritic cells (DCs) are a type of professional antigen presenting cell (APC). Immature DCs are typically stimulated by various adjuvants via immune receptors (e.g., toll-like receptor 4 [TLR4]), which activate DCs to induce their maturation. TLR4 has been well-established to induce both innate and adaptive immune responses to various external microbial or internal damage-related molecular patterns. In this study, the multi-epitope immunogen, HAO, of foot-and-mouth disease virus (FMDV) serotypes A and O was fused with the recombinant protein, heparin-binding hemagglutinin (HBHA), a novel TLR4 agonist, to obtain a new recombinant fusion protein, termed HAO-HBHA. HAO-HBHA was found to be highly efficient at activating murine DCs by the TLR4 pathway, both in vitro and in vivo. HAO-HBHA elicited strong specific humoral immune responses detected with an ELISA and virus neutralizing antibody test (VNT). HAO-HBHA also elevated the cellular immune responses, as indicated by intracellular cytokine (e.g., IFN-γ, TNF-α, IL-4, IL-6, IL-10, and IL-12p70) expression in Th1 and Th2 cells. As a TLR4 agonist, HBHA has significant advantages for enhancing the immune efficacy of a FMDV serotype A and O bivalent multi-epitope vaccine. These findings provide a novel strategy for the development of a safe and effective multi-epitope vaccine candidate against FMDV and further extends the application of TLR agonist-based vaccine platforms.

ACS Style

Yao Lei; Junjun Shao; Feifei Ma; Chenglin Lei; Huiyun Chang; Yongguang Zhang. Enhanced efficacy of a multi-epitope vaccine for type A and O foot‑and-mouth disease virus by fusing multiple epitopes with Mycobacterium tuberculosis heparin-binding hemagglutinin (HBHA), a novel TLR4 agonist. Molecular Immunology 2020, 121, 118 -126.

AMA Style

Yao Lei, Junjun Shao, Feifei Ma, Chenglin Lei, Huiyun Chang, Yongguang Zhang. Enhanced efficacy of a multi-epitope vaccine for type A and O foot‑and-mouth disease virus by fusing multiple epitopes with Mycobacterium tuberculosis heparin-binding hemagglutinin (HBHA), a novel TLR4 agonist. Molecular Immunology. 2020; 121 ():118-126.

Chicago/Turabian Style

Yao Lei; Junjun Shao; Feifei Ma; Chenglin Lei; Huiyun Chang; Yongguang Zhang. 2020. "Enhanced efficacy of a multi-epitope vaccine for type A and O foot‑and-mouth disease virus by fusing multiple epitopes with Mycobacterium tuberculosis heparin-binding hemagglutinin (HBHA), a novel TLR4 agonist." Molecular Immunology 121, no. : 118-126.

Journal article
Published: 13 February 2020 in Microbial Pathogenesis
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To compare different nanoparticle-based nasal vaccines against foot-and-mouth disease (FMD), chitosan (CS)-coated poly (lactic-co-glycolic acid) (PLGA) nanoparticles (NPs) (CS/PLGA-NPs) and amino-functionalized mesoporous silica nanoparticles (Am/MSNs) loaded with FMDV recombinant plasmid (pP12A3C/IFN-CS/PLGA-NPs and pP12A3C/IFN-Am/MS-NPs) were used to induce mucosal and systemic immune responses in guinea pigs via intranasal delivery. Simultaneously, CpG oligodeoxy nucleotides (ODNs) as a vaccine adjuvant were encapsulated in chitosan-coated poly (lactic-co-glycolic acid) nanoparticles (CpG-CS/PLGA-NPs). The pP12A3C/IFN-CS/PLGA-NPs and CpG-CS/PLGA-NPs generated displayed good morphology, high stability, mean diameters of 500 and 400 nm and encapsulation efficiencies of 83.8% and 88.4%, respectively. Data from the in vitro release assay showed that plasmid and CpG were sustainably released from nanoparticles (up to 66.73% and 64%, respectively, of the total amount loaded). Guinea pigs immunized with pP12A3C/IFN-CS/PLGA-NPs + CpG-CS/PLGA-NPs showed markedly higher mucosal, cellular and humoral immune responses than those administered pP12A3C/IFN-CS/PLGA-NPs or naked plasmid vaccine alone. FMDV-specific secretory immunoglobulin A (sIgA) antibodies in nasal washes were initially detected at 3 days post-vaccination with CS/PLGA-NPs loaded with plasmid. Guinea pigs immunized with pP12A3C/IFN-CS/PLGA-NPs also displayed higher cellular and humoral immune responses than pP12A3C-CS/PLGA-NPs and naked plasmid vaccine alone. FMDV-specific immunoglobulin G (IgG) antibodies in serum were initially detected at 5 days post-vaccination (intramuscularly) with the naked plasmid. Finally, challenge experiments 42 days post-vaccine revealed 100% protection in guinea pigs immunized with pP12A3C/IFN-CS/PLGA-NPs + CpG-CS/PLGA-NPs and pP12A3C/IFN-CS/PLGA-NPs. However, plasmid DNA was burst released from pP12A3C/IFN-Am/MS-NPs. Our attempts to use pP12A3C/IFN-Am/MS-NPs to immunize guinea pigs failed to induce immune responses. In conclusion, CpG and IFN-α adjuvant based FMD vaccines elicit protection in guinea pigs. Moreover, CS-coated PLGA NPs present an efficient and safe mucosal immune delivery system for FMDV DNA vaccine. Data from the current study provide a foundation for understanding and further evaluating protective immune responses in pigs.

ACS Style

Huabin Zheng; Li Pan; Jianliang Lv; Zhongwang Zhang; Yuanyuan Wang; Wenfa Hu; Xinsheng Liu; Peng Zhou; Yonglu Wang; Yongguang Zhang. Comparison of immune responses in guinea pigs by intranasal delivery with different nanoparticles-loaded FMDV DNA vaccine. Microbial Pathogenesis 2020, 142, 104061 .

AMA Style

Huabin Zheng, Li Pan, Jianliang Lv, Zhongwang Zhang, Yuanyuan Wang, Wenfa Hu, Xinsheng Liu, Peng Zhou, Yonglu Wang, Yongguang Zhang. Comparison of immune responses in guinea pigs by intranasal delivery with different nanoparticles-loaded FMDV DNA vaccine. Microbial Pathogenesis. 2020; 142 ():104061.

Chicago/Turabian Style

Huabin Zheng; Li Pan; Jianliang Lv; Zhongwang Zhang; Yuanyuan Wang; Wenfa Hu; Xinsheng Liu; Peng Zhou; Yonglu Wang; Yongguang Zhang. 2020. "Comparison of immune responses in guinea pigs by intranasal delivery with different nanoparticles-loaded FMDV DNA vaccine." Microbial Pathogenesis 142, no. : 104061.

Journal article
Published: 01 September 2019 in Virology
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MicroRNAs (miRNAs) play important regulatory roles during interactions between virus pathogens and host cells, but whether and how they work in the case of foot-and-mouth disease virus (FMDV) is less understood. Based on a microarray-based miRNA profiling in the porcine kidney cell line PK-15, we identified 36 differentially expressed host miRNAs at the early stage of FMDV infection, among which miR-1307 was significantly induced. Functional characterization demonstrated that miR-1307 attenuated FMDV replication. Further experiments proved that miR-1307 specifically promoted the degradation of the viral structural protein VP3 indirectly through proteasome pathway. Moreover, innate immune signaling was activated and expression of immune responsive genes was significantly enhanced in the miR-1307-overexpressing clones. Together, our data demonstrated that miR-1307 suppresses FMDV replication by destabilizing VP3 and enhancing host immune response. Importantly, subcutaneous injection of miR-1307 agomir delayed the FMDV-induced lethality in suckling mice, exhibiting its therapeutic potential to control foot-and-mouth disease (FMD).

ACS Style

Linlin Qi; Kailing Wang; Haotai Chen; Xinsheng Liu; Jianliang Lv; Shitong Hou; Yongguang Zhang; Yuefeng Sun. Host microRNA miR-1307 suppresses foot-and-mouth disease virus replication by promoting VP3 degradation and enhancing innate immune response. Virology 2019, 535, 162 -170.

AMA Style

Linlin Qi, Kailing Wang, Haotai Chen, Xinsheng Liu, Jianliang Lv, Shitong Hou, Yongguang Zhang, Yuefeng Sun. Host microRNA miR-1307 suppresses foot-and-mouth disease virus replication by promoting VP3 degradation and enhancing innate immune response. Virology. 2019; 535 ():162-170.

Chicago/Turabian Style

Linlin Qi; Kailing Wang; Haotai Chen; Xinsheng Liu; Jianliang Lv; Shitong Hou; Yongguang Zhang; Yuefeng Sun. 2019. "Host microRNA miR-1307 suppresses foot-and-mouth disease virus replication by promoting VP3 degradation and enhancing innate immune response." Virology 535, no. : 162-170.

Applied genetics and molecular biotechnology
Published: 28 August 2019 in Applied Microbiology and Biotechnology
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Foot-and-mouth disease virus (FMDV) has led to serious losses in the farming industry worldwide, particularly in cattle and swine. In developing countries, the control and eradication of FMD rely upon vaccination, in which the inactivated vaccine is predominant. In the preparation of inactivated vaccine, a series of purification methods were used to remove non-structural proteins (NSPs). It is necessary to develop a quantitative detection method of residual NSP and confirm a threshold value for the evaluation of the vaccine. Meanwhile, it is also important to develop a sensitive and rapid diagnostic method to distinguish infected animals from vaccinated animals (DIVA). In this study, three monoclonal antibodies (MAbs) against NSP 3ABC, designated 2G5, 9E2, and 1E10, were used. Subsequently, a series of overlapping peptides were expressed using a prokaryotic expression system to determine the minimal epitopes identified by the MAbs. Three linear B cell epitopes (BCEs), "92EYIEKA97" "23EGPYAGPLE31" and "209EPHH212", were identified by MAbs 2G5, 9E2, and 1E10, respectively. Alanine-scanning mutagenesis analysis confirmed the critical amino acid in these epitopes. The epitope "92EYIEKA97" is located in 3A, which is deleted in some natural deletion mutants that result in a change in virus tropism. MAb 9E2 that identified the epitope "23EGPYAGPLE31" reacted with 3B1 and 3B2, but did not react with 3B3. In combination with sequence alignment analysis, the epitope "23EGPYAGPLE31" is highly conserved among different FMDV isolates. Preliminary screening using the known positive and negative sera indicated the MAb 9E2 has the potential for the development of a diagnostic method for DIVA. The residual NSP in inactivated vaccines can be detected using 9E2-HRP, which indicated the MAb 9E2 is able to evaluate inactivated vaccines. The four-amino acid epitope is the first reported to date that is recognized by 1E10. These results provide valuable insight into the diagnosis of DIVA and the NSP residual evaluation in inactivated vaccines.

ACS Style

Wei Liu; Junjun Shao; Danian Chen; Yanyan Chang; Huiyun Chang; Yongguang Zhang. Identification of three linear B cell epitopes against non-structural protein 3ABC of FMDV using monoclonal antibodies. Applied Microbiology and Biotechnology 2019, 103, 8075 -8086.

AMA Style

Wei Liu, Junjun Shao, Danian Chen, Yanyan Chang, Huiyun Chang, Yongguang Zhang. Identification of three linear B cell epitopes against non-structural protein 3ABC of FMDV using monoclonal antibodies. Applied Microbiology and Biotechnology. 2019; 103 (19):8075-8086.

Chicago/Turabian Style

Wei Liu; Junjun Shao; Danian Chen; Yanyan Chang; Huiyun Chang; Yongguang Zhang. 2019. "Identification of three linear B cell epitopes against non-structural protein 3ABC of FMDV using monoclonal antibodies." Applied Microbiology and Biotechnology 103, no. 19: 8075-8086.

Communication
Published: 03 May 2019 in Molecules
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Foot-and-mouth disease (FMD) is a highly contagious viral disease of cloven-hoofed animals, which has significant economic consequences in affected countries. As the currently available vaccines against FMD provide no protection until 4-7 days post-vaccination, the only alternative method to control the spread of FMD virus (FMDV) during outbreaks is the application of antiviral agents. Hence, it is important to identify effective antiviral agents against FMDV infection. In this study, we found that mizoribine has potent antiviral activity against FMDV replication in IBRS-2 cells. A time-of-drug-addition assay demonstrated that mizoribine functions at the early stage of replication. Moreover, mizoribine also showed antiviral effect on FMDV in vivo. In summary, these results revealed that mizoribine could be a potential antiviral drug against FMDV.

ACS Style

Shi-Fang Li; Mei-Jiao Gong; Yue-Feng Sun; Jun-Jun Shao; Yong-Guang Zhang; Hui-Yun Chang. In Vitro and in Vivo Antiviral Activity of Mizoribine Against Foot-And-Mouth Disease Virus. Molecules 2019, 24, 1723 .

AMA Style

Shi-Fang Li, Mei-Jiao Gong, Yue-Feng Sun, Jun-Jun Shao, Yong-Guang Zhang, Hui-Yun Chang. In Vitro and in Vivo Antiviral Activity of Mizoribine Against Foot-And-Mouth Disease Virus. Molecules. 2019; 24 (9):1723.

Chicago/Turabian Style

Shi-Fang Li; Mei-Jiao Gong; Yue-Feng Sun; Jun-Jun Shao; Yong-Guang Zhang; Hui-Yun Chang. 2019. "In Vitro and in Vivo Antiviral Activity of Mizoribine Against Foot-And-Mouth Disease Virus." Molecules 24, no. 9: 1723.

Biotechnological products and process engineering
Published: 19 March 2019 in Applied Microbiology and Biotechnology
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Many recent studies have shown that flagellin fused to heterologous antigens can induce significantly enhanced humoral and cellular immune responses through its adjuvant activity. Therefore, in this study, two key B cell epitopes and a truncated VP1 (ΔVP1) protein from foot-and-mouth disease virus (FMDV) were expressed as flagellin fusion proteins in different patterns. Specifically, ΔVP1 and two duplicates of two key B cell epitopes (2×B1B2) were fused separately to the C-terminus of flagellin with a universal exogenous T cell epitope to construct FT (Flagellin-Truncated VP1) and FME (Flagellin-Multiple Epitopes). In addition, the D3 domain of flagellin was replaced by ΔVP1 in FME, yielding FTME (Flagellin-Truncated VP1-Multiple Epitopes). The immunogenicity and protective efficacy of the three fusion proteins as novel FMDV vaccine candidates were evaluated. The results showed that FT, FME, and FTME elicited significant FMDV-specific IgG responses at 10 μg/dose compared with the mock group (P < 0.05), with FTME producing the highest response. No significant differences in the antibody response to FTME were observed between different immunization routes or among adjuvants (ISA-206, poly(I·C), MPLA, and CpG-ODN) in mice. In addition, at 30 μg/dose, all three fusion proteins significantly induced neutralizing antibody production and upregulated the levels of some cytokines, including TNF-α, IFN-γ, and IL-12, in guinea pigs. Importantly, all three fusion proteins provided effective protective immunity against FMDV challenge in guinea pigs, though different protection rates were found. The results presented in this study indicate that the FTME fusion protein is a promising novel vaccine candidate for the future prevention and control of foot-and-mouth disease.

ACS Style

Baofeng Cui; Xinsheng Liu; Peng Zhou; Yuzhen Fang; Donghong Zhao; Yongguang Zhang; Yonglu Wang. Immunogenicity and protective efficacy of recombinant proteins consisting of multiple epitopes of foot-and-mouth disease virus fused with flagellin. Applied Microbiology and Biotechnology 2019, 103, 3367 -3379.

AMA Style

Baofeng Cui, Xinsheng Liu, Peng Zhou, Yuzhen Fang, Donghong Zhao, Yongguang Zhang, Yonglu Wang. Immunogenicity and protective efficacy of recombinant proteins consisting of multiple epitopes of foot-and-mouth disease virus fused with flagellin. Applied Microbiology and Biotechnology. 2019; 103 (8):3367-3379.

Chicago/Turabian Style

Baofeng Cui; Xinsheng Liu; Peng Zhou; Yuzhen Fang; Donghong Zhao; Yongguang Zhang; Yonglu Wang. 2019. "Immunogenicity and protective efficacy of recombinant proteins consisting of multiple epitopes of foot-and-mouth disease virus fused with flagellin." Applied Microbiology and Biotechnology 103, no. 8: 3367-3379.

Original article
Published: 11 March 2019 in Archives of Virology
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Since 2010, continual outbreaks of highly virulent variants of porcine epidemic diarrhea virus (PEDV) belonging to genotype GII have led to serious economic losses for the Chinese swine industry. To better understand the biological characteristics and pathogenicity of the current prevalent Chinese PEDV field strains, in this study, a highly virulent Chinese genotype GIIa PEDV strain, CH/HBXT/2018, was isolated and serially propagated using Vero cells. Sequencing and phylogenetic analysis showed that strain CH/HBXT/2018 contained novel insertion and deletion mutations in the S gene region relative to the classical strain and belonged to the genotype GIIa, similar to other recently isolated PEDV strains from China and the United States. Pig infection studies indicated that the CH/HBXT/2018 strain was highly virulent in suckling piglets, and the median pig diarrhea dose (PDD50) was 8.63 log10PDD50/3 mL at 7 days postinfection (DPI). The results of the present study are important for future PEDV challenge studies and the development of new PEDV vaccines based on prevalent field strains for the prevention and control of PED in China.

ACS Style

Liping Zhang; Xinsheng Liu; Qiaoling Zhang; Peng Zhou; Yuzhen Fang; Zhaoliang Dong; Donghong Zhao; Weiyan Li; Jiaxin Feng; Yongguang Zhang; Yonglu Wang. Biological characterization and pathogenicity of a newly isolated Chinese highly virulent genotype GIIa porcine epidemic diarrhea virus strain. Archives of Virology 2019, 164, 1287 -1295.

AMA Style

Liping Zhang, Xinsheng Liu, Qiaoling Zhang, Peng Zhou, Yuzhen Fang, Zhaoliang Dong, Donghong Zhao, Weiyan Li, Jiaxin Feng, Yongguang Zhang, Yonglu Wang. Biological characterization and pathogenicity of a newly isolated Chinese highly virulent genotype GIIa porcine epidemic diarrhea virus strain. Archives of Virology. 2019; 164 (5):1287-1295.

Chicago/Turabian Style

Liping Zhang; Xinsheng Liu; Qiaoling Zhang; Peng Zhou; Yuzhen Fang; Zhaoliang Dong; Donghong Zhao; Weiyan Li; Jiaxin Feng; Yongguang Zhang; Yonglu Wang. 2019. "Biological characterization and pathogenicity of a newly isolated Chinese highly virulent genotype GIIa porcine epidemic diarrhea virus strain." Archives of Virology 164, no. 5: 1287-1295.

Short communication
Published: 12 February 2019 in Veterinary Microbiology
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Although highly virulent GII-genotype PEDV strains have become pandemic in the swine population worldwide, little is known about the differences in immunogenicity and cross-protective efficacy between the GIIa and GIIb subgenotypes. Hence, in the present study, we vaccinated suckling piglets with GIIa (CH/HBXT/2018) and GIIb (CH/HNPJ/2017) PEDV strain-based inactivated vaccine candidates and compared their immunogenicity and cross-protective efficacy. The results showed that both vaccine candidates induced high levels of PEDV-specific IgG antibodies and IFN-γ and reduced the levels of neutralizing antibodies at 21 dpv in suckling piglets. The GIIa-based inactivated vaccine protected all piglets (8/8) against virulent homologous and heterologous virus challenge, while the GIIb strain-based inactivated vaccine protected only 2/4 and 1/4 piglets against virulent homologous and heterologous virus challenge, respectively. Furthermore, antibodies against the GIIa and GIIb strains cross-reacted and cross-neutralized both strains in vitro. Taken together, the data presented in this study indicate that GIIa strain-based inactivated vaccine candidates are more promising than GIIb-based candidates for the development of an effective vaccine against the current highly virulent pandemic PEDV strains.

ACS Style

Xinsheng Liu; Liping Zhang; Qiaoling Zhang; Peng Zhou; Yuzhen Fang; Donghong Zhao; Jiaxin Feng; Weiyan Li; Yongguang Zhang; Yonglu Wang. Evaluation and comparison of immunogenicity and cross-protective efficacy of two inactivated cell culture-derived GIIa- and GIIb-genotype porcine epidemic diarrhea virus vaccines in suckling piglets. Veterinary Microbiology 2019, 230, 278 -282.

AMA Style

Xinsheng Liu, Liping Zhang, Qiaoling Zhang, Peng Zhou, Yuzhen Fang, Donghong Zhao, Jiaxin Feng, Weiyan Li, Yongguang Zhang, Yonglu Wang. Evaluation and comparison of immunogenicity and cross-protective efficacy of two inactivated cell culture-derived GIIa- and GIIb-genotype porcine epidemic diarrhea virus vaccines in suckling piglets. Veterinary Microbiology. 2019; 230 ():278-282.

Chicago/Turabian Style

Xinsheng Liu; Liping Zhang; Qiaoling Zhang; Peng Zhou; Yuzhen Fang; Donghong Zhao; Jiaxin Feng; Weiyan Li; Yongguang Zhang; Yonglu Wang. 2019. "Evaluation and comparison of immunogenicity and cross-protective efficacy of two inactivated cell culture-derived GIIa- and GIIb-genotype porcine epidemic diarrhea virus vaccines in suckling piglets." Veterinary Microbiology 230, no. : 278-282.

Journal article
Published: 14 January 2019 in PeerJ
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Several studies have shown that epitope vaccines exhibit substantial advantages over conventional vaccines. However, epitope vaccines are associated with limited immunity, which can be overcome by conjugating antigenic epitopes with built-in adjuvants (e.g., some carrier proteins or new biomaterials) with special properties, including immunologic specificity, good biosecurity and biocompatibility, and the ability to vastly improve the immune response of epitope vaccines. When designing epitope vaccines, the following types of built-in adjuvants are typically considered: (1) pattern recognition receptor ligands (i.e., toll-like receptors); (2) virus-like particle carrier platforms; (3) bacterial toxin proteins; and (4) novel potential delivery systems (e.g., self-assembled peptide nanoparticles, lipid core peptides, and polymeric or inorganic nanoparticles). This review primarily discusses the current and prospective applications of these built-in adjuvants (i.e., biological carriers) to provide some references for the future design of epitope-based vaccines.

ACS Style

Yao Lei; Furong Zhao; Junjun Shao; Yangfan Li; Shifang Li; Huiyun Chang; Yongguang Zhang. Application of built-in adjuvants for epitope-based vaccines. PeerJ 2019, 6, e6185 .

AMA Style

Yao Lei, Furong Zhao, Junjun Shao, Yangfan Li, Shifang Li, Huiyun Chang, Yongguang Zhang. Application of built-in adjuvants for epitope-based vaccines. PeerJ. 2019; 6 ():e6185.

Chicago/Turabian Style

Yao Lei; Furong Zhao; Junjun Shao; Yangfan Li; Shifang Li; Huiyun Chang; Yongguang Zhang. 2019. "Application of built-in adjuvants for epitope-based vaccines." PeerJ 6, no. : e6185.

Review
Published: 11 December 2018 in Cellular Physiology and Biochemistry
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The interferons (IFNs) are a primary defense against pathogens because of the strong antiviral activities they induce. IFNs can be classified into three groups: type I, type II and type III, according to their genetic, structural, and functional characteristics and their receptors on the cell surface. The type I IFNs are the largest group and include IFN-α, IFN-β, IFN-ε, IFN-ω, IFN-κ, IFN-δ, IFN-τ and IFN-ζ. The use of IFNs for the treatment of viral infectious diseases on their antiviral activity may become an important therapeutic option, for example, IFN-α is well known for the successful treatment of hepatitis B and C virus infections, and interest is increasing in the antiviral efficacy of other novel IFN classes and their potential applications. Therefore, in this review, we summarize the recent progress in the study of the biological activities of all the type I IFN classes and their potential applications in the treatment of infections with immunodeficiency virus, hepatitis viruses, and influenza viruses.

ACS Style

Shi-Fang Li; Mei-Jiao Gong; Fu-Rong Zhao; Jun-Jun Shao; Yin-Li Xie; Yong-Guang Zhang; Hui-Yun Chang. Type I Interferons: Distinct Biological Activities and Current Applications for Viral Infection. Cellular Physiology and Biochemistry 2018, 51, 2377 -2396.

AMA Style

Shi-Fang Li, Mei-Jiao Gong, Fu-Rong Zhao, Jun-Jun Shao, Yin-Li Xie, Yong-Guang Zhang, Hui-Yun Chang. Type I Interferons: Distinct Biological Activities and Current Applications for Viral Infection. Cellular Physiology and Biochemistry. 2018; 51 (5):2377-2396.

Chicago/Turabian Style

Shi-Fang Li; Mei-Jiao Gong; Fu-Rong Zhao; Jun-Jun Shao; Yin-Li Xie; Yong-Guang Zhang; Hui-Yun Chang. 2018. "Type I Interferons: Distinct Biological Activities and Current Applications for Viral Infection." Cellular Physiology and Biochemistry 51, no. 5: 2377-2396.

Research article
Published: 31 October 2018 in Journal of Medical Virology
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Foot-and-mouth disease (FMD) is a disease of worldwide economic importance, and vaccines play an important role in preventing FMDV outbreaks. However, new control strategies are still needed since FMDV outbreaks still occur in some disease-free countries. Currently, interferon (IFN)-based strategies have been demonstrated to be an efficient biotherapeutic option against FMDV; however, interferon omega (IFN-ω) has not yet been assessed in this capacity. Thus, this study evaluated the antiviral activity of porcine IFN omega 7 (PoIFN-ω7) against FMDV. After the PoIFN-ω7 was expressed and purified, cell proliferation assays and RT-qPCR were used to evaluate the effective anti-cytopathic concentration of PoIFN-ω7 and its effectiveness pre- and post-infection with FMDV in swine kidney cells (IBRS-2). Results showed the rHis-PoIFN-ω7 fusion protein was considerably expressed using Escherichia coli BL21 (DE3) strain, and the recombinant protein exhibited significant in vitro protection against FMDV, including two strains belonging to type O and A FMDV, respectively. In addition, PoIFN-ω7 unregulated the transcription of Mx1, ISG15, OAS1, and PKR genes. These findings indicated that IFN-ω has potential for serving as a useful therapeutic agent to prevent FMDV or other viral outbreaks in pigs. This article is protected by copyright. All rights reserved.

ACS Style

Shi-Fang Li; Fu-Rong Zhao; Mei-Jiao Gong; Jun-Jun Shao; Yin-Li Xie; Hui-Yun Chang; Yong-Guang Zhang. Antiviral activity of porcine interferon omega 7 against foot‐and‐mouth disease virus in vitro. Journal of Medical Virology 2018, 91, 208 -214.

AMA Style

Shi-Fang Li, Fu-Rong Zhao, Mei-Jiao Gong, Jun-Jun Shao, Yin-Li Xie, Hui-Yun Chang, Yong-Guang Zhang. Antiviral activity of porcine interferon omega 7 against foot‐and‐mouth disease virus in vitro. Journal of Medical Virology. 2018; 91 (2):208-214.

Chicago/Turabian Style

Shi-Fang Li; Fu-Rong Zhao; Mei-Jiao Gong; Jun-Jun Shao; Yin-Li Xie; Hui-Yun Chang; Yong-Guang Zhang. 2018. "Antiviral activity of porcine interferon omega 7 against foot‐and‐mouth disease virus in vitro." Journal of Medical Virology 91, no. 2: 208-214.

Article
Published: 31 October 2018 in ChemElectroChem
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Metal sulfide has been considered as one of the most promising anode materials in lithium‐ion batteries. However, large volume change and low intrinsic electrical conductivity significantly restrict its performance. Herein, flexible electrode materials comprising of ZnS nanotubes/carbon cloth are prepared by combined solvothermal and ion‐exchange sulfidation technique. The ZnS nanotubes array/carbon cloth electrode is assessed for application in lithium ion batteries and remarkable improvement towards reversible capacity was observed. A notable capacity of 1053 mAh g‐1 at 0.2 C and maintain a reversible capacity of 608 mAh g‐1 after 100 cycles are observed, which are both comparable to similar materials in the previous published reports. The ZnS nanotubes with small dimension and uniform dispersion grown directly on carbon cloth can effectively shorten the path of the lithium ions, facilitating the charge transfer of the electrode. In the meanwhile, the carbon cloth and the three‐dimensional (3D) structured carbon fiber having a high surface area can efficiently reduce the volume change during the discharge/charge cycles.

ACS Style

Lanyan Huang; Yongguang Zhang; Chaoqun Shang; Xin Wang; Guofu Zhou; Jian Zhen Ou; Yichao Wang. ZnS Nanotubes/Carbon Cloth as a Reversible and High-Capacity Anode Material for Lithium-Ion Batteries. ChemElectroChem 2018, 6, 461 -466.

AMA Style

Lanyan Huang, Yongguang Zhang, Chaoqun Shang, Xin Wang, Guofu Zhou, Jian Zhen Ou, Yichao Wang. ZnS Nanotubes/Carbon Cloth as a Reversible and High-Capacity Anode Material for Lithium-Ion Batteries. ChemElectroChem. 2018; 6 (2):461-466.

Chicago/Turabian Style

Lanyan Huang; Yongguang Zhang; Chaoqun Shang; Xin Wang; Guofu Zhou; Jian Zhen Ou; Yichao Wang. 2018. "ZnS Nanotubes/Carbon Cloth as a Reversible and High-Capacity Anode Material for Lithium-Ion Batteries." ChemElectroChem 6, no. 2: 461-466.