Broad cross-species infection of cultured cells by bat HKU2- related swine acute diarrhea syndrome coronavirus and identification of its replication in murine dendritic cells in vivo highlight its potential for diverse interspecies transmission

Journal of Virology

Volumn 93, Issue 24, 2019, Pages

  Yang, Yong Le ^a   Qin, Pan ^a   Wang, Bin ^a   Liu, Yan ^a   Xu, Guo Han ^a   Peng, Lei ^a   Zhou, Jiyong ^a   Zhu, Shu Jeffrey ^a   Huang, Yao Wei ^a  

^a ZHEJIANG UNIVERSITY   (China)

Author keywords

Coronavirus; Interspecies transmission; Mouse infection model; SADS CoV

Indexed keywords

DOUBLE STRANDED RNA; TRYPSIN; VIRAL PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BAT CORONAVIRUS HKU2; CELL CULTURE; CONTROLLED STUDY; CORONAVIRINAE; CORONAVIRUS INFECTION; DENDRITIC CELL; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAT; SPLEEN; SPLEEN CELL; SWINE ACUTE DIARRHEA SYNDROME CORONAVIRUS; VIRAL TROPISM; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS INFECTIVITY; VIRUS REPLICATION; VIRUS TRANSMISSION; ALPHACORONAVIRUS; ANIMAL; BAT; C57BL MOUSE; CELL LINE; CHICKEN; CHINA; CROSS INFECTION; DIARRHEA; DISEASE MODEL; FEMALE; GENETICS; GROWTH, DEVELOPMENT AND AGING; MALE; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; PATHOGENICITY; PATHOLOGY; PHYSIOLOGY; PIG; SARS CORONAVIRUS; SEVERE ACUTE RESPIRATORY SYNDROME; SPECIES DIFFERENCE; VETERINARY MEDICINE; VIROLOGY;

ALPHACORONAVIRUS; ANIMALS; CELL LINE; CELLS, CULTURED; CHICKENS; CHINA; CHIROPTERA; CORONAVIRUS INFECTIONS; CROSS INFECTION; DENDRITIC CELLS; DIARRHEA; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; MALE; MICE; MICE, INBRED C57BL; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; RATS; SARS VIRUS; SEVERE ACUTE RESPIRATORY SYNDROME; SPECIES SPECIFICITY; SPLEEN; SWINE; VIRUS INTERNALIZATION; VIRUS REPLICATION;

EID: 85075814380     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01448-19     Document Type: Article

References (38)

1. Graham RL, Baric RS. 2010. Recombination, reservoirs, and the modular spike: mechanisms of coronavirus cross-species transmission. J Virol 84:3134-3146. https://doi.org/10.1128/JVI.01394-09.
2. van Boheemen S, de Graaf M, Lauber C, Bestebroer TM, Raj VS, Zaki AM, Osterhaus AD, Haagmans BL, Gorbalenya AE, Snijder EJ, Fouchier RA. 2012. Genomic characterization of a newly discovered coronavirus associated with acute respiratory distress syndrome in humans. mBio 3:e00473-12. https://doi.org/10.1128/mBio.00473-12.
3. Soma T, Saito N, Kawaguchi M, Sasai K. 2018. Feline coronavirus antibody titer in cerebrospinal fluid from cats with neurological signs. J Vet Med Sci 80:59-62. https://doi.org/10.1292/jvms.17-0399.
4. Huang YW, Dickerman AW, Pineyro P, Li L, Fang L, Kiehne R, Opriessnig T, Meng XJ. 2013. Origin, evolution, and genotyping of emergent porcine epidemic diarrhea virus strains in the United States. mBio 4:e00737-13. https://doi.org/10.1128/mBio.00737-13.
5. Lu G, Wang Q, Gao GF. 2015. Bat-to-human: spike features determining "host jump" of coronaviruses SARS-CoV, MERS-CoV, and beyond. Trends Microbiol 23:468-478. https://doi.org/10.1016/j.tim.2015.06.003.
6. Ksiazek TG, Erdman D, Goldsmith CS, Zaki SR, Peret T, Emery S, Tong S, Urbani C, Comer JA, Lim W, Rollin PE, Dowell SF, Ling AE, Humphrey CD, Shieh WJ, Guarner J, Paddock CD, Rota P, Fields B, DeRisi J, Yang JY, Cox N, Hughes JM, LeDuc JW, Bellini WJ, Anderson LJ, SARS Working Group. 2003. A novel coronavirus associated with severe acute respiratory syndrome. N Engl J Med 348:1953-1966. https://doi.org/10.1056/ NEJMoa030781.
7. Drexler JF, Corman VM, Drosten C. 2014. Ecology, evolution and classification of bat coronaviruses in the aftermath of SARS. Antiviral Res 101:45-56. https://doi.org/10.1016/j.antiviral.2013.10.013.
8. Chan JFW, Lau SKP, To KKW, Cheng VCC, Woo PCY, Yuen K-Y. 2015. Middle East respiratory syndrome coronavirus: another zoonotic betacoronavirus causing SARS-like disease. Clin Microbiol Rev 28:465-522. https://doi.org/10.1128/CMR.00102-14.
9. Yin Y, Wunderink RG. 2018. MERS, SARS and other coronaviruses as causes of pneumonia. Respirology 23:130-137. https://doi.org/10.1111/ resp.13196.
10. Hulswit RJG, de Haan CAM, Bosch BJ. 2016. Coronavirus spike protein and tropism changes. Adv Virus Res 96:29-57. https://doi.org/10.1016/ bs.aivir.2016.08.004.
11. Pan Y, Tian X, Qin P, Wang B, Zhao P, Yang YL, Wang L, Wang D, Song Y, Zhang X, Huang YW. 2017. Discovery of a novel swine enteric alphacoronavirus (SeACoV) in southern China. Vet Microbiol 211:15-21. https://doi.org/10.1016/j.vetmic.2017.09.020.
12. Lau SKP, Woo PCY, Li KSM, Huang Y, Wang M, Lam CSF, Xu H, Guo R, Chan K-H, Zheng B-J, Yuen K-Y. 2007. Complete genome sequence of bat coronavirus HKU2 from Chinese horseshoe bats revealed a much smaller spike gene with a different evolutionary lineage from the rest of the genome. Virology 367:428-439. https://doi.org/10.1016/j.virol.2007.06.009.
13. Gong L, Li J, Zhou Q, Xu Z, Chen L, Zhang Y, Xue C, Wen Z, Cao Y. 2017. A new bat-HKU2-like coronavirus in swine, China, 2017. Emerg Infect Dis 23:1607-1609. https://doi.org/10.3201/eid2309.170915.
14. Zhou P, Fan H, Lan T, Yang X-L, Shi W-F, Zhang W, Zhu Y, Zhang Y-W, Xie Q-M, Mani S, Zheng X-S, Li B, Li J-M, Guo H, Pei G-Q, An X-P, Chen J-W, Zhou L, Mai K-J, Wu Z-X, Li D, Anderson DE, Zhang L-B, Li S-Y, Mi ZQ, He T-T, Cong F, Guo P-J, Huang R, Luo Y, Liu X-L, Chen J, Huang Y, Sun Q, Zhang X-L-L, Wang Y-Y, Xing S-Z, Chen Y-S, Sun Y, Li J, Daszak P, Wang L-F, Shi Z-L, Tong Y-G, Ma J-Y. 2018. Fatal swine acute diarrhoea syndrome caused by an HKU2-related coronavirus of bat origin. Nature 556:255-258. https://doi.org/10.1038/s41586-018-0010-9.
15. Wang L, Su S, Bi Y, Wong G, Gao GF. 2018. Bat-origin coronaviruses expand their host range to pigs. Trends Microbiol 26:466-470. https:// doi.org/10.1016/j.tim.2018.03.001.
16. Hofmann M, Wyler R. 1988. Propagation of the virus of porcine epidemic diarrhea in cell culture. J Clin Microbiol 26:2235-2239.
17. Wicht O, Li W, Willems L, Meuleman TJ, Wubbolts RW, van Kuppeveld FJ, Rottier PJM, Bosch BJ. 2014. Proteolytic activation of the porcine epidemic diarrhea coronavirus spike fusion protein by trypsin in cell culture. J Virol 88:7952-7961. https://doi.org/10.1128/JVI.00297-14.
18. Li W, Moore MJ, Vasilieva N, Sui J, Wong SK, Berne MA, Somasundaran M, Sullivan JL, Luzuriaga K, Greenough TC, Choe H, Farzan M. 2003. Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 426:450-454. https://doi.org/10.1038/nature02145.
19. Raj VS, Mou H, Smits SL, Dekkers DH, Muller MA, Dijkman R, Muth D, Demmers JA, Zaki A, Fouchier RA, Thiel V, Drosten C, Rottier PJ, Osterhaus AD, Bosch BJ, Haagmans BL. 2013. Dipeptidyl peptidase 4 is a functional receptor for the emerging human coronavirus-EMC. Nature 495:251-254. https://doi.org/10.1038/nature12005.
20. Delmas B, Gelfi J, L'Haridon R, Vogel LK, Sjöström H, Norén O, Laude H. 1992. Aminopeptidase N is a major receptor for the entero-pathogenic coronavirus TGEV. Nature 357:417-420. https://doi.org/10.1038/357417a0.
21. Wang B, Liu Y, Ji C-M, Yang Y-L, Liang Q-Z, Zhao P, Xu L-D, Lei X-M, Luo W-T, Qin P, Zhou J, Huang Y-W. 2018. Porcine deltacoronavirus engages the transmissible gastroenteritis virus functional receptor porcine aminopeptidase N for infectious cellular entry. J Virol 92:e00318-18. https:// doi.org/10.1128/JVI.00318-18.
22. Li W, Hulswit RJG, Kenney SP, Widjaja I, Jung K, Alhamo MA, van Dieren B, van Kuppeveld FJM, Saif LJ, Bosch BJ. 2018. Broad receptor engagement of an emerging global coronavirus may potentiate its diverse cross-species transmissibility. Proc Natl Acad Sci U S A 115:E5135-E5143. https://doi.org/10.1073/pnas.1802879115.
23. Williams RK, Jiang GS, Holmes KV. 1991. Receptor for mouse hepatitis virus is a member of the carcinoembryonic antigen family of glycoproteins. Proc Natl Acad Sci U S A 88:5533-5536. https://doi.org/10.1073/ pnas.88.13.5533.
24. Yang Y-L, Liang Q-Z, Xu S-Y, Mazing E, Xu G-H, Peng L, Qin P, Wang B, Huang Y-W. 2019. Characterization of a novel bat-HKU2-like swine enteric alphacoronavirus (SeACoV) infection in cultured cells and development of a SeACoV infectious clone. Virology 536:110-118. https://doi .org/10.1016/j.virol.2019.08.006.
25. He B, Yang F, Yang W, Zhang Y, Feng Y, Zhou J, Xie J, Feng Y, Bao X, Guo H, Li Y, Xia L, Li N, Matthijnssens J, Zhang H, Tu C. 2013. Characterization of a novel G3P[3] rotavirus isolated from a lesser horseshoe bat: a distant relative of feline/canine rotaviruses. J Virol 87:12357-12366. https://doi .org/10.1128/JVI.02013-13.
26. Chan JF-W, Chan K-H, Choi GK, To KK-W, Tse H, Cai J-P, Yeung ML, Cheng VC-C, Chen H, Che X-Y, Lau SK-P, Woo PC-Y, Yuen K-Y. 2013. Differential cell line susceptibility to the emerging novel human betacoronavirus 2c EMC/2012: implications for disease pathogenesis and clinical manifestation. J Infect Dis 207:1743-1752. https://doi.org/10.1093/infdis/jit123.
27. Muller MA, Raj VS, Muth D, Meyer B, Kallies S, Smits SL, Wollny R, Bestebroer TM, Specht S, Suliman T, Zimmermann K, Binger T, Eckerle I, Tschapka M, Zaki AM, Osterhaus ADME, Fouchier RAM, Haagmans BL, Drosten C. 2012. Human coronavirus EMC does not require the SARS-coronavirus receptor and maintains broad replicative capability in mammalian cell lines. mBio 3:e00515-12. https://doi.org/10.1128/mBio.00515-12.
28. Woo PC, Lau SK, Tsang CC, Lau CC, Wong PC, Chow FW, Fong JY, Yuen KY. 2017. Coronavirus HKU15 in respiratory tract of pigs and first discovery of coronavirus quasispecies in 5=-untranslated region. Emerg Microbes Infect 6:e53. https://doi.org/10.1038/emi.2017.37.
29. Mazaleuskaya L, Veltrop R, Ikpeze N, Martin-Garcia J, Navas-Martin S. 2012. Protective role of Toll-like receptor 3-induced type I interferon in murine coronavirus infection of macrophages. Viruses 4:901-923. https://doi.org/10.3390/v4050901.
30. Kobinger GP, Limberis MP, Somanathan S, Schumer G, Bell P, Wilson JM. 2007. Human immunodeficiency viral vector pseudotyped with the spike envelope of severe acute respiratory syndrome coronavirus transduces human airway epithelial cells and dendritic cells. Hum Gene Ther 18: 413-422. https://doi.org/10.1089/hum.2006.194.
31. Yang Z-Y, Huang Y, Ganesh L, Leung K, Kong W-P, Schwartz O, Subbarao K, Nabel GJ. 2004. pH-dependent entry of severe acute respiratory syndrome coronavirus is mediated by the spike glycoprotein and enhanced by dendritic cell transfer through DC-SIGN. J Virol 78:5642-5650. https://doi.org/10.1128/JVI.78.11.5642-5650.2004.
32. Tsoleridis T, Chappell JG, Onianwa O, Marston DA, Fooks AR, Monchatre-Leroy E, Umhang G, Muller MA, Drexler JF, Drosten C, Tarlinton RE, McClure CP, Holmes EC, Ball JK. 2019. Shared common ancestry of rodent alphacoronaviruses sampled globally. Viruses 11:125. https://doi .org/10.3390/v11020125.
33. Wang W, Lin XD, Guo WP, Zhou RH, Wang MR, Wang CQ, Ge S, Mei SH, Li MH, Shi M, Holmes EC, Zhang YZ. 2015. Discovery, diversity and evolution of novel coronaviruses sampled from rodents in China. Virology 474:19-27. https://doi.org/10.1016/j.virol.2014.10.017.
34. Collins AM, Fell S, Pearson H, Toribio JA. 2011. Colonisation and shedding of Lawsonia intracellularis in experimentally inoculated rodents and in wild rodents on pig farms. Vet Microbiol 150:384-388. https:// doi.org/10.1016/j.vetmic.2011.01.020.
35. Everard CO, Ferdinand GA, Butcher LV, Everard JD. 1989. Leptospirosis in piggery workers on Trinidad. J Trop Med Hyg 92:253-258.
36. Alshukairi AN, Zheng J, Zhao J, Nehdi A, Baharoon SA, Layqah L, Bokhari A, Al Johani SM, Samman N, Boudjelal M, Ten Eyck P, Al-Mozaini MA, Zhao J, Perlman S, Alagaili AN. 2018. High prevalence of MERS-CoV infection in camel workers in Saudi Arabia. mBio 9:e01985-18. https:// doi.org/10.1128/mBio.01985-18.
37. Ji C-M, Wang B, Zhou J, Huang Y-W. 2018. Aminopeptidase-Nindependent entry of porcine epidemic diarrhea virus into Vero or porcine small intestine epithelial cells. Virology 517:16-23. https://doi .org/10.1016/j.virol.2018.02.019.
38. Ou XY, Zheng WL, Shan YW, Mu ZX, Dominguez SR, Holmes KV, Qian ZH. 2016. Identification of the fusion peptide-containing region in betacoronavirus spike glycoproteins. J Virol 90:5586-5600. https://doi.org/10 .1128/JVI.00015-16.