CD8+ T cells and macrophages regulate pathogenesis in a mouse model of Middle East respiratory syndrome

Journal of Virology

Volumn 91, Issue 1, 2017, Pages

  Coleman, Christopher M ^a   Sisk, Jeanne M ^a,c   Halasz, Gabor ^b   Zhong, Jixin ^a   Beck, Sarah E ^a   Matthews, Krystal L ^a   Venkataraman, Thiagarajan ^a   Rajagopalan, Sanjay ^a   Kyratsous, Christos A ^b   Frieman, Matthew B ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b REGENERON PHARMACEUTICALS INC   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Coronavirus; DPP4; Immune response; MERS; MERS CoV; Mouse model; Pathogenesis; Viral pathogenesis

Indexed keywords

DIPEPTIDYL PEPTIDASE IV; DPP4 PROTEIN, HUMAN; DPP4 PROTEIN, MOUSE; TRANSCRIPTOME; VIRUS RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; IMMUNE RESPONSE; INFLAMMATION; LUNG; MACROPHAGE; MIDDLE EAST RESPIRATORY SYNDROME; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; T CELL DEPLETION; VIRUS PATHOGENESIS; VIRUS REPLICATION; ANIMAL; C57BL MOUSE; CORONAVIRUS INFECTION; DISEASE MODEL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOLOGY; LYMPHOCYTE DEPLETION; PATHOGENICITY; PATHOLOGY; PROMOTER REGION; TRANSGENE; TRANSGENIC MOUSE; VIROLOGY; VIRUS ENTRY;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CORONAVIRUS INFECTIONS; DIPEPTIDYL PEPTIDASE 4; DISEASE MODELS, ANIMAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HOST-PATHOGEN INTERACTIONS; HUMANS; LUNG; LYMPHOCYTE DEPLETION; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; PROMOTER REGIONS, GENETIC; RECEPTORS, VIRUS; TRANSCRIPTOME; TRANSGENES; VIRUS INTERNALIZATION; VIRUS REPLICATION;

EID: 85008178769     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01825-16     Document Type: Article

References (35)

1. Zaki AM, van Boheemen S, Bestebroer TM, Osterhaus AD, Fouchier RA. 2012 Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N Engl J Med 367:1814-1820. https://doi.org/10.1056/NEJMoa1211721.
2. Lee SS, Wong NS. 2015. Probable transmission chains of Middle East respiratory syndrome coronavirus and the multiple generations of secondary infection in South Korea. Int J Infect Dis 38:65-67. https://doi.org/10.1016/j.ijid.2015.07.014.
3. Ki M. 2015. 2015 MERS outbreak in Korea: hospital-to-hospital transmission. Epidemiol Health 37:e2015033. https://doi.org/10.4178/epih/e2015033.
4. 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.
5. Zhong J, Rao X, Rajagopalan S. 2013. An emerging role of dipeptidyl peptidase 4 (DPP4) beyond glucose control: potential implications in cardiovascular disease. Atherosclerosis 226:305-314. https://doi.org/10.1016/j.atherosclerosis.2012.09.012.
6. Chu H, Zhou J, Wong BH, Li C, Chan JF, Cheng ZS, Yang D, Wang D, Lee AC, Li C, Yeung ML, Cai JP, Chan IH, Ho WK, To KK, Zheng BJ, Yao Y, Qin C, Yuen KY. 2016. Middle East respiratory syndrome coronavirus efficiently infects human primary T lymphocytes and activates the extrinsic and intrinsic apoptosis pathways. J Infect Dis 213:904-914. https://doi.org/10.1093/infdis/jiv380.
7. Tynell J, Westenius V, Ronkko E, Munster VJ, Melen K, Osterlund P, Julkunen I. 2016. Middle East respiratory syndrome coronavirus shows poor replication but significant induction of antiviral responses in human monocyte-derived macrophages and dendritic cells. J Gen Virol 97:344-355. https://doi.org/10.1099/jgv.0.000351.
8. Zhou J, Chu H, Li C, Wong BH, Cheng ZS, Poon VK, Sun T, Lau CC, Wong KK, Chan JY, Chan JF, To KK, Chan KH, Zheng BJ, Yuen KY. 2014. Active replication of Middle East respiratory syndrome coronavirus and aberrant induction of inflammatory cytokines and chemokines in human macrophages: implications for pathogenesis. J Infect Dis 209:1331-1342. https://doi.org/10.1093/infdis/jit504.
9. Karin N, Wildbaum G. 2015. The role of chemokines in shaping the balance between CD4(+) T cell subsets and its therapeutic implications in autoimmune and cancer diseases. Front Immunol 6:609. https://doi.org/10.3389/fimmu.2015.00609.
10. Ng DL, Al Hosani F, Keating MK, Gerber SI, Jones TL, Metcalfe MG, Tong S, Tao Y, Alami NN, Haynes LM, Mutei MA, Abdel-Wareth L, Uyeki TM, Swerdlow DL, Barakat M, Zaki SR. 2016. Clinicopathologic, immunohistochemical, and ultrastructural findings of a fatal case of Middle East respiratory syndrome coronavirus infection in the United Arab Emirates, April 2014. Am J Pathol 186:652-658. https://doi.org/10.1016/j.ajpath.2015.10.024.
11. de Wit E, Rasmussen AL, Falzarano D, Bushmaker T, Feldmann F, Brining DL, Fischer ER, Martellaro C, Okumura A, Chang J, Scott D, Benecke AG, Katze MG, Feldmann H, Munster VJ. 2013. Middle East respiratory syndrome coronavirus (MERS-CoV) causes transient lower respiratory tract infection in rhesus macaques. Proc Natl Acad Sci U S A 110: 16598-16603. https://doi.org/10.1073/pnas.1310744110.
12. Munster VJ, de Wit E, Feldmann H. 2013. Pneumonia from human coronavirus in a macaque model. N Engl J Med 368:1560-1562. https://doi.org/10.1056/NEJMc1215691.
13. Yao Y, Bao L, Deng W, Xu L, Li F, Lv Q, Yu P, Chen T, Xu Y, Zhu H, Yuan J, Gu S, Wei Q, Chen H, Yuen KY, Qin C. 2014. An animal model of MERS produced by infection of rhesus macaques with MERS coronavirus. J Infect Dis 209:236-242. https://doi.org/10.1093/infdis/jit590.
14. Falzarano D, de Wit E, Feldmann F, Rasmussen AL, Okumura A, Peng X, Thomas MJ, van Doremalen N, Haddock E, Nagy L, LaCasse R, Liu T, Zhu J, McLellan JS, Scott DP, Katze MG, Feldmann H, Munster VJ. 2014. Infection with MERS-CoV causes lethal pneumonia in the common marmoset. PLoS Pathog 10:e1004250. https://doi.org/10.1371/journal.ppat.1004250.
15. Johnson RF, Via LE, Kumar MR, Cornish JP, Yellayi S, Huzella L, Postnikova E, Oberlander N, Bartos C, Ork BL, Mazur S, Allan C, Holbrook MR, Solomon J, Johnson JC, Pickel J, Hensley LE, Jahrling PB. 2015. Intratracheal exposure of common marmosets to MERS-CoV Jordan-n3/2012 or MERS-CoV EMC/2012 isolates does not result in lethal disease. Virology 485:422-430. https://doi.org/10.1016/j.virol.2015.07.013.
16. Wentworth DE, Gillim-Ross L, Espina N, Bernard KA. 2004. Mice susceptible to SARS coronavirus. Emerg Infect Dis 10:1293-1296. https://doi.org/10.3201/eid1007.031119.
17. Roberts A, Deming D, Paddock CD, Cheng A, Yount B, Vogel L, Herman BD, Sheahan T, Heise M, Genrich GL, Zaki SR, Baric R, Subbarao K. 2007. A mouse-adapted SARS-coronavirus causes disease and mortality in BALB/c mice. PLoS Pathog 3:e5. https://doi.org/10.1371/journal.ppat.0030005.
18. Coleman CM, Matthews KL, Goicochea L, Frieman MB. 2014. Wild-type and innate immune-deficient mice are not susceptible to the Middle East respiratory syndrome coronavirus. J Gen Virol 95:408-412. https://doi.org/10.1099/vir.0.060640-0.
19. Cockrell AS, Peck KM, Yount BL, Agnihothram SS, Scobey T, Curnes NR, Baric RS, Heise MT. 2014. Mouse dipeptidyl peptidase 4 is not a functional receptor for Middle East respiratory syndrome coronavirus infection. J Virol 88:5195-5199. https://doi.org/10.1128/JVI.03764-13.
20. van Doremalen N, Miazgowicz KL, Milne-Price S, Bushmaker T, Robertson S, Scott D, Kinne J, McLellan JS, Zhu J, Munster VJ. 2014. Host species restriction of Middle East respiratory syndrome coronavirus through its receptor, dipeptidyl peptidase 4. J Virol 88:9220-9232. https://doi.org/10.1128/JVI.00676-14.
21. Peck KM, Cockrell AS, Yount BL, Scobey T, Baric RS, Heise MT. 2015. Glycosylation of mouse DPP4 plays a role in inhibiting Middle East respiratory syndrome coronavirus infection. J Virol 89:4696-4699. https://doi.org/10.1128/JVI.03445-14.
22. Zhao J, Li K, Wohlford-Lenane C, Agnihothram SS, Fett C, Gale MJ, Jr, Baric RS, Enjuanes L, Gallagher T, McCray PB, Jr, Perlman S. 2014. Rapid generation of a mouse model for Middle East respiratory syndrome. Proc Natl Acad Sci U S A 111:4970-4975. https://doi.org/10.1073/pnas.1323279111.
23. Agrawal AS, Garron T, Tao X, Peng BH, Wakamiya M, Chan TS, Couch RB, Tseng CT. 2015. Generation of a transgenic mouse model of Middle East respiratory syndrome coronavirus infection and disease. J Virol 89: 3659-3670. https://doi.org/10.1128/JVI.03427-14.
24. Gorrell MD, Gysbers V, McCaughan GW. 2001. CD26: a multifunctional integral membrane and secreted protein of activated lymphocytes. Scand J Immunol 54:249-264. https://doi.org/10.1046/j.1365-3083.2001.00984.x.
25. Tao X, Garron T, Agrawal AS, Algaissi A, Peng BH, Wakamiya M, Chan TS, Lu L, Du L, Jiang S, Couch RB, Tseng CT. 2015. Characterization and demonstration of the value of a lethal mouse model of Middle East respiratory syndrome coronavirus infection and disease. J Virol 90: 57-67. https://doi.org/10.1128/JVI.02009-15.
26. Li K, Wohlford-Lenane C, Perlman S, Zhao J, Jewell AK, Reznikov LR, Gibson-Corley KN, Meyerholz DK, McCray PB, Jr. 2016. Middle East respiratory syndrome coronavirus causes multiple organ damage and lethal disease in mice transgenic for human dipeptidyl peptidase 4. J Infect Dis 213:712-722. https://doi.org/10.1093/infdis/jiv499.
27. Pascal KE, Coleman CM, Mujica AO, Kamat V, Badithe A, Fairhurst J, Hunt C, Strein J, Berrebi A, Sisk JM, Matthews KL, Babb R, Chen G, Lai KM, Huang TT, Olson W, Yancopoulos GD, Stahl N, Frieman MB, Kyratsous CA. 2015 Pre-and postexposure efficacy of fully human antibodies against Spike protein in a novel humanized mouse model of MERS-CoV infection. Proc Natl Acad Sci U S A 112:8738-8743. https://doi.org/10.1073/pnas.1510830112.
28. Heng TS, Painter MW, Immunological Genome Project Consortium. 2008. The Immunological Genome Project: networks of gene expression in immune cells. Nat Immunol 9:1091-1094. https://doi.org/10.1038/ni1008-1091.
29. Kupershmidt I, Su QJ, Grewal A, Sundaresh S, Halperin I, Flynn J, Shekar M, Wang H, Park J, Cui W, Wall GD, Wisotzkey R, Alag S, Akhtari S, Ronaghi M. 2010. Ontology-based meta-analysis of global collections of high-throughput public data. PLoS One 55(9):e13066. https://doi.org/10.1371/journal.pone.0013066.
30. Zhao J, Van Rooijen N, Perlman S. 2009. Evasion by stealth: inefficient immune activation underlies poor T cell response and severe disease in SARS-CoV-infected mice. PLoS Pathog 5:e1000636. https://doi.org/10.1371/journal.ppat.1000636.
31. Coleman CM, Frieman MB. 2015. Growth and quantification of MERSCoV infection. Curr Protoc Microbiol 37:15E.2.1-9. https://doi.org/10.1002/9780471729259.mc15e02s37.
32. Loubaki L, Tremblay T, Bazin R. 2013. In vivo depletion of leukocytes and platelets following injection of T cell-specific antibodies into mice. J Immunol Methods 393:38-44. https://doi.org/10.1016/j.jim.2013.04.004.
33. Van Rooijen N, Sanders A. 1994. Liposome mediated depletion of macrophages: mechanism of action, preparation of liposomes and applications. J Immunol Methods 174:83-93. https://doi.org/10.1016/0022-1759(94)90012-4.
34. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. 2008. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621-628. https://doi.org/10.1038/nmeth.1226.
35. Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Genome Biol 11:R106. https://doi.org/10.1186/gb-2010-11-10-r106.