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http://dx.doi.org/10.4014/jmb.1909.09041

Surface-Displayed Porcine IFN-λ3 in Lactobacillus plantarum Inhibits Porcine Enteric Coronavirus Infection of Porcine Intestinal Epithelial Cells  

Liu, Yong-Shi (College of Animal Science and Technology, Jilin Provincial Engineering Research Center of Animal Probiotics, Key Laboratory of Animal Production and Product Quality Safety of Ministry of Education, Jilin Agricultural University)
Liu, Qiong (College of Animal Science and Technology, Jilin Provincial Engineering Research Center of Animal Probiotics, Key Laboratory of Animal Production and Product Quality Safety of Ministry of Education, Jilin Agricultural University)
Jiang, Yan-Long (College of Animal Science and Technology, Jilin Provincial Engineering Research Center of Animal Probiotics, Key Laboratory of Animal Production and Product Quality Safety of Ministry of Education, Jilin Agricultural University)
Yang, Wen-Tao (College of Animal Science and Technology, Jilin Provincial Engineering Research Center of Animal Probiotics, Key Laboratory of Animal Production and Product Quality Safety of Ministry of Education, Jilin Agricultural University)
Huang, Hai-Bin (College of Animal Science and Technology, Jilin Provincial Engineering Research Center of Animal Probiotics, Key Laboratory of Animal Production and Product Quality Safety of Ministry of Education, Jilin Agricultural University)
Shi, Chun-Wei (College of Animal Science and Technology, Jilin Provincial Engineering Research Center of Animal Probiotics, Key Laboratory of Animal Production and Product Quality Safety of Ministry of Education, Jilin Agricultural University)
Yang, Gui-Lian (College of Animal Science and Technology, Jilin Provincial Engineering Research Center of Animal Probiotics, Key Laboratory of Animal Production and Product Quality Safety of Ministry of Education, Jilin Agricultural University)
Wang, Chun-Feng (College of Animal Science and Technology, Jilin Provincial Engineering Research Center of Animal Probiotics, Key Laboratory of Animal Production and Product Quality Safety of Ministry of Education, Jilin Agricultural University)
Publication Information
Journal of Microbiology and Biotechnology / v.30, no.4, 2020 , pp. 515-525 More about this Journal
Abstract
Interferon (IFN)-λ plays an essential role in mucosal cells which exhibit strong antiviral activity. Lactobacillus plantarum (L. plantarum) has substantial application potential in the food and medical industries because of its probiotic properties. Alphacoronaviruses, especially porcine epidemic diarrhea virus (PEDV) and transmissible gastroenteritis virus (TGEV), cause high morbidity and mortality in piglets resulting in economic loss. Co-infection by these two viruses is becoming increasingly frequent. Therefore, it is particularly important to develop a new drug to prevent diarrhea infected with mixed viruses in piglets. In this study, we first constructed an anchored expression vector with CWA (C-terminal cell wall anchor) on L. plantarum. Second, we constructed two recombinant L. plantarum strains that anchored IFN-λ3 via pgsA (N-terminal transmembrane anchor) and CWA. Third, we demonstrated that both recombinant strains possess strong antiviral effects against coronavirus infection in the intestinal porcine epithelial cell line J2 (IPEC-J2). However, recombinant L. plantarum with the CWA anchor exhibited a more powerful antiviral effect than recombinant L. plantarum with pgsA. Consistent with this finding, Lb.plantarum-pSIP-409-IFN-λ3-CWA enhanced the expression levels of IFN-stimulated genes (ISGs) (ISG15, OASL, and Mx1) in IPEC-J2 cells more than did recombinant Lb.plantarum-pSIP-409-pgsA'-IFN-λ3. Our study verifies that recombinant L. plantarum inhibits PEDV and TGEV infection in IPEC-J2 cells, which may offer great potential for use as a novel oral antiviral agent in therapeutic applications for combating porcine epidemic diarrhea and transmissible gastroenteritis. This study is the first to show that recombinant L. plantarum suppresses PEDV and TGEV infection of IPEC-J2 cells.
Keywords
Porcine $IFN-{\lambda}3$; Lactobacillus plantarum; surface-displayed; porcine enteric coronaviruses; antiviral agent;
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1 Conti C, Malacrino C, Mastromarino P. 2009. Inhibition of herpes simplex virus type 2 by vaginal lactobacilli. J. Physiol. Pharmacol. 60 (Suppl 6): 19-26.
2 Martin V, Maldonado A, Fernandez L, Rodriguez JM, Connor RI. 2010. Inhibition of human immunodeficiency virus type 1 by lactic acid bacteria from human breastmilk. Breastfeed. Med. 153-158.
3 Zhang X, Li P, Zheng Q, Hou J. 2019. Lactobacillus acidophilus S-layer protein-mediated inhibition of PEDVinduced apoptosis of Vero cells. Vet. Microbiol. 229: 159-167.   DOI
4 Sang Y, Rowland RR, Blecha F. 2010. Molecular characterization and antiviral analyses of porcine type III interferons. J. Interferon Cytokine Res. 30: 801-807.   DOI
5 Pott J, Mahlakoiv T, Mordstein M, Duerr CU, Michiels T, Stockinger S, et al. 2011. IFN-lambda determines the intestinal epithelial antiviral host defense. Proc. Natl. Acad. Sci. USA 108: 7944-7949.   DOI
6 Kotenko SV, Gallagher G, Baurin VV, Lewis-Antes A, Shen M, Shah NK, et al. 2003. IFN-lambdas mediate antiviral protection through a distinct class II cytokine receptor complex. Nat. Immunol. 4: 69-77.   DOI
7 Lazear HM, Nice TJ, Diamond MS. 2015. Interferon-lambda: immune functions at barrier surfaces and beyond. Immunity 43: 15-28.   DOI
8 Wang D, Fang L, Xiao S. 2016. Porcine epidemic diarrhea in China. Virus Res. 226: 7-13.   DOI
9 Zhang Q, Hu R, Tang X, Wu C, He Q, Zhao Z, et al. 2013. Occurrence and investigation of enteric viral infections in pigs with diarrhea in China. Arch. Virol. 158: 1631-1636.   DOI
10 Zhao ZP, Yang Z, Lin WD, Wang WY, Yang J, Jin WJ, et al. 2016. The rate of co-infection for piglet diarrhea viruses in China and the genetic characterization of porcine epidemic diarrhea virus and porcine kobuvirus. Acta Virol. 60: 55-61.   DOI
11 Maragkoudakis PA, Chingwaru W, Gradisnik L, Tsakalidou E, Cencic A. 2010. Lactic acid bacteria efficiently protect human and animal intestinal epithelial and immune cells from enteric virus infection. Int. J. Food Microbiol. 141 Suppl 1: S91-97.   DOI
12 Lakshmi B, Viswanath B, Sai Gopal DV. 2013. Probiotics as antiviral agents in shrimp aquaculture. J. Pathog. 2013: 424123.   DOI
13 Al Kassaa I, Hamze M, Hober D, Chihib NE, Drider D. 2014. Identification of vaginal lactobacilli with potential probiotic properties isolated from women in North Lebanon. Microb. Ecol. 67: 722-734.   DOI
14 Wang Z, Chai W, Burwinkel M, Twardziok S, Wrede P, Palissa C, et al. 2013. Inhibitory influence of Enterococcus faecium on the propagation of swine influenza A virus in vitro. PLoS One 8: e53043.   DOI
15 Cha MK, Lee DK, An HM, Lee SW, Shin SH, Kwon JH, et al. 2012. Antiviral activity of Bifidobacterium adolescentis SPM1005-A on human papillomavirus type 16. BMC Med. 10: 72.   DOI
16 Huang KY, Yang GL, Jin YB, Liu J, Chen HL, Wang PB, et al. 2018. Construction and immunogenicity analysis of Lactobacillus plantarum expressing a porcine epidemic diarrhea virus S gene fused to a DC-targeting peptide. Virus Res. 247: 84-93.   DOI
17 Al Kassaa I, Hober D, Hamze M, Chihib NE, Drider D. 2014. Antiviral potential of lactic acid bacteria and their bacteriocins. Probiotics Antimicrob. Proteins 6: 177-185.   DOI
18 Seo BJ, Rather IA, Kumar VJ, Choi UH, Moon MR, Lim JH, et al. 2012. Evaluation of Leuconostoc mesenteroides YML003 as a probiotic against low-pathogenic avian influenza (H9N2) virus in chickens. J. Appl. Microbiol. 113: 163-171.   DOI
19 Shi SH, Yang WT, Yang GL, Cong YL, Huang HB, Wang Q, et al. 2014. Immunoprotection against influenza virus H9N2 by the oral administration of recombinant Lactobacillus plantarum NC8 expressing hemagglutinin in BALB/c mice. Virology 464-465: 166-176.   DOI
20 Schmittgen TD, Livak KJ. 2008. Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3: 1101-1108.   DOI
21 Arena MP, Capozzi V, Spano G, Fiocco D. 2017. The potential of lactic acid bacteria to colonize biotic and abiotic surfaces and the investigation of their interactions and mechanisms. Appl. Microbiol. Biotechnol. 101: 2641-2657.   DOI
22 Enjuanes L, Smerdou C, Castilla J, Anton IM, Torres JM, Sola I, et al. 1995. Development of protection against coronavirus induced diseases. A review. Adv. Exp. Med. Biol. 380: 197-211.   DOI
23 Mullan BP, Davies GT, Cutler RS. 1994. Simulation of the economic impact of transmissible gastroenteritis on commercial pig production in Australia. Aust. Vet. J. 71: 151-154.   DOI
24 Nice TJ, Baldridge MT, McCune BT, Norman JM, Lazear HM, Artyomov M, et al. 2015. Interferon-lambda cures persistent murine norovirus infection in the absence of adaptive immunity. Science 347: 269-273.   DOI
25 Arena MP, Elmastour F, Sane F, Drider D, Fiocco D, Spano G, et al. 2018. Inhibition of coxsackievirus B4 by Lactobacillus plantarum. Microbiol. Res. 210: 59-64.   DOI
26 Diaz MO, Ziemin S, Le Beau MM, Pitha P, Smith SD, Chilcote RR, et al. 1988. Homozygous deletion of the alphaand beta 1-interferon genes in human leukemia and derived cell lines. Proc. Natl. Acad. Sci. USA 85: 5259-5263.   DOI
27 Sorvig E, Mathiesen G, Naterstad K, Eijsink VG, Axelsson L. 2005. High-level, inducible gene expression in Lactobacillus sakei and Lactobacillus plantarum using versatile expression vectors. Microbiology (Reading, England). 151: 2439-2449.   DOI
28 Dekie L, Toncheva V, Dubruel P, Schacht EH, Barrett L, Seymour LW. 2000. Poly-L-glutamic acid derivatives as vectors for gene therapy. J. Control. Release 65: 187-202.   DOI
29 Michon C, Langella P, Eijsink VG, Mathiesen G, Chatel JM. 2016. Display of recombinant proteins at the surface of lactic acid bacteria: strategies and applications. Microb. Cell Fact. 15: 70.   DOI
30 Thirabunyanon M, Hongwittayakorn P. 2013. Potential probiotic lactic acid bacteria of human origin induce antiproliferation of colon cancer cells via synergic actions in adhesion to cancer cells and short-chain fatty acid bioproduction. Appl. Biochem. Biotechnol. 169: 511-525.   DOI
31 Li L , Fu F , Xue M, Chen W, L iu J , Shi H, et al. 2 017. I FNlambda preferably inhibits PEDV infection of porcine intestinal epithelial cells compared with IFN-alpha. Antiviral Res. 140: 76-82.   DOI
32 Masters PS. 2006. The molecular biology of coronaviruses. Adv. Virus Res. 66: 193-292.   DOI
33 Hofmann M, Wyler R. 1988. Propagation of the virus of porcine epidemic diarrhea in cell culture. J. Clin. Microbiol. 26: 2235-2239.   DOI
34 Sun D, Shi H, Guo D, Chen J, Shi D, Zhu Q, et al. 2015. Analysis of protein expression changes of the Vero E6 cells infected with classic PEDV strain CV777 by using quantitative proteomic technique. J. Virol. Methods 218: 27-39.   DOI
35 Ma SJ, Li K, Li XS, Guo XQ, Fu PF, Yang MF, et al. 2014. Expression of bioactive porcine interferon-alpha in Lactobacillus casei. World J. Microbiol. Biotechnol. 30: 2379-2386.   DOI
36 Diamond MS, Farzan M. 2013. The broad-spectrum antiviral functions of IFIT and IFITM proteins. Nat. Rev. Immunol. 13: 46-57.   DOI
37 Ashiuchi M, Nawa C, Kamei T, Song JJ, Hong SP, Sung MH, et al. 2001. Physiological and biochemical characteristics of poly gammaglutamate synthetase complex of Bacillus subtilis. Eur. J. Biochem. 268: 5321-5328.   DOI
38 Melchjorsen J, Kristiansen H, Christiansen R, Rintahaka J, Matikainen S, Paludan SR, et al. 2009. Differential regulation of the OASL and OAS1 genes in response to viral infections. J. Interferon Cytokine Res. 29: 199-207.   DOI
39 Brass AL, Huang IC, Benita Y, John SP, Krishnan MN, Feeley EM, et al. 2009. The IFITM proteins mediate cellular resistance to influenza A H1N1 virus, West Nile virus, and dengue virus. Cell 139: 1243-1254.   DOI
40 Wells JM, Mercenier A. 2008. Mucosal delivery of therapeutic and prophylactic molecules using lactic acid bacteria. Nat. Rev. Microbiol. 6: 349-362.   DOI
41 Bermudez-Humaran LG, Cortes-Perez NG, Le Loir Y, Alcocer-Gonzalez JM, Tamez-Guerra RS, de Oca-Luna RM, et al. 2004. An inducible surface presentation system improves cellular immunity against human papillomavirus type 16 E7 antigen in mice after nasal administration with recombinant lactococci. J. Med. Microbiol. 53: 427-433.   DOI
42 Lenschow DJ, Lai C, Frias-Staheli N, Giannakopoulos NV, Lutz A, Wolff T, et al. 2007. IFN-stimulated gene 15 functions as a critical antiviral molecule against influenza, herpes, and Sindbis viruses. Proc. Natl. Acad. Sci. USA 104: 1371-1376.   DOI
43 Kochs G, Haller O. 1999. Interferon-induced human MxA GTPase blocks nuclear import of Thogoto virus nucleocapsids. Proc. Natl. Acad. Sci. USA 96: 2082-2086.   DOI