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Article ; Online: Enteric coronavirus PDCoV evokes a non-Warburg effect by hijacking pyruvic acid as a metabolic hub.

Su, Guanning / Liu, Jiao / Duan, Chenrui / Fang, Puxian / Fang, Liurong / Zhou, Yanrong / Xiao, Shaobo

2024 Volume 71, Page(s) 103112

Abstract: The Warburg effect, also referred as aerobic glycolysis, is a common metabolic program during viral infection. Through targeted metabolomics combined with biochemical experiments and various cell models, we investigated the central carbon metabolism (CCM) ...

Abstract	The Warburg effect, also referred as aerobic glycolysis, is a common metabolic program during viral infection. Through targeted metabolomics combined with biochemical experiments and various cell models, we investigated the central carbon metabolism (CCM) profiles of cells infected with porcine deltacoronavirus (PDCoV), an emerging enteropathogenic coronavirus with zoonotic potential. We found that PDCoV infection required glycolysis but decreased glycolytic flux, exhibiting a non-Warburg effect characterized by pyruvic acid accumulation. Mechanistically, PDCoV enhanced pyruvate kinase activity to promote pyruvic acid anabolism, a process that generates pyruvic acid with concomitant ATP production. PDCoV also hijacked pyruvic acid catabolism to increase biosynthesis of non-essential amino acids (NEAAs), suggesting that pyruvic acid is an essential hub for PDCoV to scavenge host energy and metabolites. Furthermore, PDCoV facilitated glutaminolysis to promote the synthesis of NEAA and pyrimidines for optimal proliferation. Our work supports a novel CCM model after viral infection and provides potential anti-PDCoV drug targets.
MeSH term(s)	Swine ; Animals ; Coronavirus/metabolism ; Pyruvic Acid/metabolism ; Swine Diseases/metabolism ; Swine Diseases/pathology ; Coronavirus Infections/pathology
Chemical Substances	Pyruvic Acid (8558G7RUTR)
Language	English
Publishing date	2024-03-04
Publishing country	Netherlands
Document type	Journal Article
ZDB-ID	2701011-9
ISSN	2213-2317 ; 2213-2317
ISSN (online)	2213-2317
ISSN	2213-2317
DOI	10.1016/j.redox.2024.103112
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Article ; Online: Porcine reproductive and respiratory syndrome virus infection activates ADAM17 to induce inflammatory responses.

Liu, Jiao / Su, Guanning / Duan, Chenrui / Sun, Zheng / Xiao, Shaobo / Zhou, Yanrong / Fang, Liurong

Veterinary microbiology

2024 Volume 292, Page(s) 110066

Abstract: Porcine reproductive and respiratory syndrome (PRRS), which has posed substantial threats to the swine industry worldwide, is primarily characterized by interstitial pneumonia. A disintegrin and metalloproteinase 17 (ADAM17) is a multifunctional sheddase ...

Abstract	Porcine reproductive and respiratory syndrome (PRRS), which has posed substantial threats to the swine industry worldwide, is primarily characterized by interstitial pneumonia. A disintegrin and metalloproteinase 17 (ADAM17) is a multifunctional sheddase involved in various inflammatory diseases. Herein, our study showed that PRRS virus (PRRSV) infection elevated ADAM17 activity, as demonstrated in primary porcine alveolar macrophages (PAMs), an immortalized PAM cell line (IPAM cells), and the lung tissues of PRRSV-infected piglets. We found that PRRSV infection promoted ADAM17 translocation from the endoplasmic reticulum to the Golgi by enhancing its interaction with inactive rhomboid protein 2 (iRhom2), a newly identified ADAM17 regulator, which in turn elevated ADAM17 activity. By screening for PRRSV-encoded structural proteins, viral envelope (E) and nucleocapsid (N) proteins were identified as the predominant ADAM17 activators. E and N proteins bind with both ADAM17 and iRhom2 to form ternary protein complexes, ultimately strengthening their interactions. Additionally, we demonstrated, using an ADAM17-knockout cell line, that ADAM17 augmented the shedding of soluble TNF-α, a pivotal inflammatory mediator. We also discovered that ADAM17-mediated cleavage of porcine TNF-α occurred between Arg-78 and Ser-79. By constructing a precision mutant cell line with Arg-78-Glu/Ser-79-Glu substitution mutations in TNF-α, we further revealed that the ADAM17-mediated production of soluble TNF-α contributed to the induction of inflammatory responses by PRRSV and its E and N proteins. Taken together, our results elucidate the mechanism by which PRRSV infection activates the iRhom2/ADAM17/TNF-α axis to enhance inflammatory responses, providing valuable insights into the elucidation of PRRSV pathogenesis.
MeSH term(s)	Swine ; Animals ; Porcine respiratory and reproductive syndrome virus ; Porcine Reproductive and Respiratory Syndrome/metabolism ; Tumor Necrosis Factor-alpha/metabolism ; Lung ; Macrophages, Alveolar ; Swine Diseases
Chemical Substances	Tumor Necrosis Factor-alpha
Language	English
Publishing date	2024-03-27
Publishing country	Netherlands
Document type	Journal Article
ZDB-ID	753154-0
ISSN	1873-2542 ; 0378-1135
ISSN (online)	1873-2542
ISSN	0378-1135
DOI	10.1016/j.vetmic.2024.110066
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Article ; Online: Orf virus as an adjuvant enhances the immune response to a PCV2 subunit vaccine.

Sun, Jie / Ma, Jun / Chen, Longfei / Xiao, Shaobo / Xiao, Xun / Fang, Liurong

Veterinary microbiology

2024 Volume 293, Page(s) 110088

Abstract: Orf virus (ORFV), a member of the genus Parapoxvirus, possesses an excellent immune activation capability, which makes it a promising immunomodulation agent. In this study, we evaluated ORFV as a novel adjuvant to enhance the immune response of mice to a ...

Abstract	Orf virus (ORFV), a member of the genus Parapoxvirus, possesses an excellent immune activation capability, which makes it a promising immunomodulation agent. In this study, we evaluated ORFV as a novel adjuvant to enhance the immune response of mice to a subunit vaccine using porcine circovirus type 2 (PCV2) capsid (Cap) protein as a model. Our results showed that both inactivated and live attenuated ORFV activated mouse bone marrow-derived dendritic cells and increased expression of immune-related cytokines interleukin (IL)-1β, IL-6, and TNF-α. Enhanced humoral and cellular immune responses were induced in mice immunized with PCV2 Cap protein combined with inactivated or live attenuated ORFV adjuvant compared with the aluminum adjuvant. Increased secretion of Th1 and Th2 cytokines by splenic lymphocytes in immunized mice further indicated that the ORFV adjuvant promoted a mixed Th1/Th2 immune response. Moreover, addition of the ORFV adjuvant to the PCV2 subunit vaccine significantly reduced the viral load in the spleen and lungs of PCV2-challenged mice and prevented pathological changes in lungs. This study demonstrates that ORFV enhances the immunogenicity of a PCV2 subunit vaccine by improving the adaptive immune response, suggesting the potential application of ORFV as a novel adjuvant.
Language	English
Publishing date	2024-04-16
Publishing country	Netherlands
Document type	Journal Article
ZDB-ID	753154-0
ISSN	1873-2542 ; 0378-1135
ISSN (online)	1873-2542
ISSN	0378-1135
DOI	10.1016/j.vetmic.2024.110088
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Article: Prevention and Control of Swine Enteric Coronaviruses in China: A Review of Vaccine Development and Application.

Kong, Fanzhi / Jia, Huilin / Xiao, Qi / Fang, Liurong / Wang, Qiuhong

Vaccines

2023 Volume 12, Issue 1

Abstract: Swine enteric coronaviruses (SECs) cause significant economic losses to the pig industry in China. Although many commercialized vaccines against transmissible gastroenteritis virus (TGEV) and porcine epidemic diarrhea virus (PEDV) are available, viruses ... ...

Abstract	Swine enteric coronaviruses (SECs) cause significant economic losses to the pig industry in China. Although many commercialized vaccines against transmissible gastroenteritis virus (TGEV) and porcine epidemic diarrhea virus (PEDV) are available, viruses are still widespread. The recent emergence of porcine deltacoronavirus (PDCoV) and swine acute diarrhea syndrome coronavirus (SADS-CoV), for which no vaccines are available, increases the disease burden. In this review, we first introduced the genomic organization and epidemiology of SECs in China. Then, we discussed the current vaccine development and application in China, aiming to provide suggestions for better prevention and control of SECs in China and other countries.
Language	English
Publishing date	2023-12-21
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2703319-3
ISSN	2076-393X
ISSN	2076-393X
DOI	10.3390/vaccines12010011
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Article ; Online: Lactate-lactylation-HSPA6 axis promotes PRRSV replication by impairing IFN-β production.

Pang, Yu / Zhou, Yanrong / Wang, Yucheng / Fang, Liurong / Xiao, Shaobo

Journal of virology

2023 Volume 98, Issue 1, Page(s) e0167023

Abstract: Lactate, traditionally considered a metabolic by-product, has recently been identified as a substrate for the induction of lactylation, a newly identified epigenetic modification that plays an important role in the regulation of host gene expression. Our ...

Abstract	Lactate, traditionally considered a metabolic by-product, has recently been identified as a substrate for the induction of lactylation, a newly identified epigenetic modification that plays an important role in the regulation of host gene expression. Our previous study showed that lactate levels were significantly elevated in cells infected with the porcine reproductive and respiratory syndrome virus (PRRSV), an
MeSH term(s)	Animals ; Epigenesis, Genetic ; Gene Expression ; Lactic Acid/metabolism ; Porcine Reproductive and Respiratory Syndrome/virology ; Porcine respiratory and reproductive syndrome virus/physiology ; Swine ; Virus Replication
Chemical Substances	Lactic Acid (33X04XA5AT)
Language	English
Publishing date	2023-12-13
Publishing country	United States
Document type	Journal Article
ZDB-ID	80174-4
ISSN	1098-5514 ; 0022-538X
ISSN (online)	1098-5514
ISSN	0022-538X
DOI	10.1128/jvi.01670-23
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Article ; Online: Deep profiling of potential substrate atlas of porcine epidemic diarrhea virus 3C-like protease.

Zhou, Junwei / Sun, Peng / Wang, Yuanqing / Qiu, Runhui / Yang, Zhixiang / Guo, Jiahui / Li, Zhuang / Xiao, Shaobo / Fang, Liurong

Journal of virology

2024 , Page(s) e0025324

Abstract: Coronavirus (CoV) 3C-like protease ( ... ...

Abstract	Coronavirus (CoV) 3C-like protease (3CL
Language	English
Publishing date	2024-04-09
Publishing country	United States
Document type	Journal Article
ZDB-ID	80174-4
ISSN	1098-5514 ; 0022-538X
ISSN (online)	1098-5514
ISSN	0022-538X
DOI	10.1128/jvi.00253-24
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Zs.A 609: Show issues

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Article ; Online: Porcine Intestinal Organoids: Overview of the State of the Art.

Ma, Panpan / Fang, Puxian / Ren, Tianze / Fang, Liurong / Xiao, Shaobo

Viruses

2022 Volume 14, Issue 5

Abstract: The intestinal tract is a crucial part of the body for growth and development, and its dysregulation can cause several diseases. The lack of appropriate in vitro models hampers the development of effective preventions and treatments against these ... ...

Abstract	The intestinal tract is a crucial part of the body for growth and development, and its dysregulation can cause several diseases. The lack of appropriate in vitro models hampers the development of effective preventions and treatments against these intestinal tract diseases. Intestinal organoids are three-dimensional (3D) polarized structures composed of different types of cells capable of self-organization and self-renewal, resembling their organ of origin in architecture and function. Porcine intestinal organoids (PIOs) have been cultured and are used widely in agricultural, veterinary, and biomedical research. Based on the similarity of the genomic sequence, anatomic morphology, and drug metabolism with humans and the difficulty in obtaining healthy human tissue, PIOs are also considered ideal models relative to rodents. In this review, we summarize the current knowledge on PIOs, emphasizing their culturing, establishment and development, and applications in the study of host-microbe interactions, nutritional development, drug discovery, and gene editing potential.
MeSH term(s)	Animals ; Drug Discovery ; Intestines ; Organoids ; Swine
Language	English
Publishing date	2022-05-21
Publishing country	Switzerland
Document type	Journal Article ; Review ; Research Support, Non-U.S. Gov't
ZDB-ID	2516098-9
ISSN	1999-4915 ; 1999-4915
ISSN (online)	1999-4915
ISSN	1999-4915
DOI	10.3390/v14051110
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Article ; Online: Cleavage of HDAC6 to dampen its antiviral activity by nsp5 is a common strategy of swine enteric coronaviruses.

Li, Zhuang / Xiao, Wenwen / Yang, Zhixiang / Guo, Jiahui / Zhou, Junwei / Xiao, Shaobo / Fang, Puxian / Fang, Liurong

Journal of virology

2024 Volume 98, Issue 2, Page(s) e0181423

Abstract: HDAC6, a structurally and functionally unique member of the histone deacetylase (HDAC) family, is an important host factor that restricts viral infection. The broad-spectrum antiviral activity of HDAC6 makes it a potent antiviral agent. Previously, we ... ...

Abstract	HDAC6, a structurally and functionally unique member of the histone deacetylase (HDAC) family, is an important host factor that restricts viral infection. The broad-spectrum antiviral activity of HDAC6 makes it a potent antiviral agent. Previously, we found that HDAC6 functions to antagonize porcine deltacoronavirus (PDCoV), an emerging enteropathogenic coronavirus with zoonotic potential. However, the final outcome is typically a productive infection that materializes as cells succumb to viral infection, indicating that the virus has evolved sophisticated mechanisms to combat the antiviral effect of HDAC6. Here, we demonstrate that PDCoV nonstructural protein 5 (nsp5) can cleave HDAC6 at glutamine 519 (Q519), and cleavage of HDAC6 was also detected in the context of PDCoV infection. More importantly, the anti-PDCoV activity of HDAC6 was damaged by nsp5 cleavage. Mechanistically, the cleaved HDAC6 fragments (amino acids 1-519 and 520-1159) lost the ability to degrade PDCoV nsp8 due to their impaired deacetylase activity. Furthermore, nsp5-mediated cleavage impaired the ability of HDAC6 to activate RIG-I-mediated interferon responses. We also tested three other swine enteric coronaviruses (transmissible gastroenteritis virus, porcine epidemic diarrhea virus, and swine acute diarrhea syndrome-coronavirus) and found that all these coronaviruses have adopted similar mechanisms to cleave HDAC6 in both an overexpression system and virus-infected cells, suggesting that cleavage of HDAC6 is a common strategy utilized by swine enteric coronaviruses to antagonize the host's antiviral capacity. Together, these data illustrate how swine enteric coronaviruses antagonize the antiviral function of HDAC6 to maintain their infection, providing new insights to the interaction between virus and host.IMPORTANCEViral infections and host defenses are in constant opposition. Once viruses combat or evade host restriction, productive infection is achieved. HDAC6 is a broad-spectrum antiviral protein that has been demonstrated to inhibit many viruses, including porcine deltacoronavirus (PDCoV). However, whether HDAC6 is reciprocally targeted and disabled by viruses remains unclear. In this study, we used PDCoV as a model and found that HDAC6 is targeted and cleaved by nsp5, a viral 3C-like protease. The cleaved HDAC6 loses its deacetylase activity as well as its ability to degrade viral proteins and activate interferon responses. Furthermore, this cleavage mechanism is shared among other swine enteric coronaviruses. These findings shed light on the intricate interplay between viruses and HDAC6, highlighting the strategies employed by viruses to evade host antiviral defenses.
MeSH term(s)	Animals ; Coronavirus/physiology ; Coronavirus Infections/veterinary ; Coronavirus Infections/virology ; Deltacoronavirus ; Interferons/metabolism ; Swine ; Swine Diseases/virology
Chemical Substances	Interferons (9008-11-1)
Language	English
Publishing date	2024-01-30
Publishing country	United States
Document type	Journal Article
ZDB-ID	80174-4
ISSN	1098-5514 ; 0022-538X
ISSN (online)	1098-5514
ISSN	0022-538X
DOI	10.1128/jvi.01814-23
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Article ; Online: Hyperacetylated microtubules assist porcine deltacoronavirus nsp8 to degrade MDA5 via SQSTM1/p62-dependent selective autophagy.

Li, Zhuang / Lai, Yinan / Qiu, Runhui / Tang, Wenbing / Ren, Jie / Xiao, Shaobo / Fang, Puxian / Fang, Liurong

Journal of virology

2024 Volume 98, Issue 3, Page(s) e0000324

Abstract: The microtubule (MT) is a highly dynamic polymer that functions in various cellular processes through MT hyperacetylation. Thus, many viruses have evolved mechanisms to hijack the MT network of the cytoskeleton to allow intracellular replication of viral ...

Abstract	The microtubule (MT) is a highly dynamic polymer that functions in various cellular processes through MT hyperacetylation. Thus, many viruses have evolved mechanisms to hijack the MT network of the cytoskeleton to allow intracellular replication of viral genomic material. Coronavirus non-structural protein 8 (nsp8), a component of the viral replication transcriptional complex, is essential for viral survival. Here, we found that nsp8 of porcine deltacoronavirus (PDCoV), an emerging enteropathogenic coronavirus with a zoonotic potential, inhibits interferon (IFN)-β production by targeting melanoma differentiation gene 5 (MDA5), the main pattern recognition receptor for coronaviruses in the cytoplasm. Mechanistically, PDCoV nsp8 interacted with MDA5 and induced autophagy to degrade MDA5 in wild-type cells, but not in autophagy-related (ATG)5 or ATG7 knockout cells. Further screening for autophagic degradation receptors revealed that nsp8 interacts with sequestosome 1/p62 and promotes p62-mediated selective autophagy to degrade MDA5. Importantly, PDCoV nsp8 induced hyperacetylation of MTs, which in turn triggered selective autophagic degradation of MDA5 and subsequent inhibition of IFN-β production. Overall, our study uncovers a novel mechanism employed by PDCoV nsp8 to evade host innate immune defenses. These findings offer new insights into the interplay among viruses, IFNs, and MTs, providing a promising target to develop anti-viral drugs against PDCoV.IMPORTANCECoronavirus nsp8, a component of the viral replication transcriptional complex, is well conserved and plays a crucial role in viral replication. Exploration of the role mechanism of nsp8 is conducive to the understanding of viral pathogenesis and development of anti-viral strategies against coronavirus. Here, we found that nsp8 of PDCoV, an emerging enteropathogenic coronavirus with a zoonotic potential, is an interferon antagonist. Further studies showed that PDCoV nsp8 interacted with MDA5 and sequestosome 1/p62, promoting p62-mediated selective autophagy to degrade MDA5. We further found that PDCoV nsp8 could induce hyperacetylation of MT, therefore triggering selective autophagic degradation of MDA5 and inhibiting IFN-β production. These findings reveal a novel immune evasion strategy used by PDCoV nsp8 and provide insights into potential therapeutic interventions.
MeSH term(s)	Animals ; Autophagy ; Coronavirus Infections/metabolism ; Coronavirus Infections/veterinary ; Coronavirus Infections/virology ; Deltacoronavirus/metabolism ; Interferons/metabolism ; Microtubules/metabolism ; Sequestosome-1 Protein/genetics ; Sequestosome-1 Protein/metabolism ; Swine ; Swine Diseases/virology
Chemical Substances	Interferons (9008-11-1) ; Sequestosome-1 Protein
Language	English
Publishing date	2024-02-14
Publishing country	United States
Document type	Journal Article
ZDB-ID	80174-4
ISSN	1098-5514 ; 0022-538X
ISSN (online)	1098-5514
ISSN	0022-538X
DOI	10.1128/jvi.00003-24
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Article ; Online: Coinfection and nonrandom recombination drive the evolution of swine enteric coronaviruses.

Guo, Jiahui / Lai, Yinan / Yang, Zhixiang / Song, Wenbo / Zhou, Junwei / Li, Zhuang / Su, Wen / Xiao, Shaobo / Fang, Liurong

Emerging microbes & infections

2024 Volume 13, Issue 1, Page(s) 2332653

Abstract: Coinfection with multiple viruses is a common phenomenon in clinical settings and is a crucial driver of viral evolution. Although numerous studies have demonstrated viral recombination arising from coinfections of different strains of a specific species, ...

Abstract	Coinfection with multiple viruses is a common phenomenon in clinical settings and is a crucial driver of viral evolution. Although numerous studies have demonstrated viral recombination arising from coinfections of different strains of a specific species, the role of coinfections of different species or genera during viral evolution is rarely investigated. Here, we analyzed coinfections of and recombination events between four different swine enteric coronaviruses that infect the jejunum and ileum in pigs, including porcine epidemic diarrhea virus (PEDV), transmissible gastroenteritis virus (TGEV), and swine acute diarrhea syndrome coronavirus (SADS-CoV), and a deltacoronavirus, porcine deltacoronavirus (PDCoV). Various coinfection patterns were observed in 4,468 fecal and intestinal tissue samples collected from pigs in a 4-year survey. PEDV/PDCoV was the most frequent coinfection. However, recombination analyses have only detected events involving PEDV/TGEV and SADS-CoV/TGEV, indicating that inter-species recombination among coronaviruses is most likely to occur within the same genus. We also analyzed recombination events within the newly identified genus
MeSH term(s)	Humans ; Swine ; Animals ; Coronavirus ; Coinfection/veterinary ; Swine Diseases ; Coronavirus Infections/veterinary ; Porcine epidemic diarrhea virus/genetics ; Transmissible gastroenteritis virus/genetics ; Recombination, Genetic ; Alphacoronavirus
Language	English
Publishing date	2024-03-27
Publishing country	United States
Document type	Journal Article
ZDB-ID	2681359-2
ISSN	2222-1751 ; 2222-1751
ISSN (online)	2222-1751
ISSN	2222-1751
DOI	10.1080/22221751.2024.2332653
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