Differential expression of the Middle East respiratory syndrome coronavirus receptor in the upper respiratory tracts of humans and dromedary camels

Journal of Virology

Volumn 90, Issue 9, 2016, Pages 4838-4842

  Widagdo, W ^a   Raj, V Stalin ^a   Schipper, Debby ^a   Kolijn, Kimberley ^a   Van Leenders, Geert J L H ^a   Bosch, Berend J ^b   Bensaid, Albert ^c   Segalés, Joaquim ^c,d   Baumgärtner, Wolfgang ^e   Osterhaus, Albert D M E ^a,e,f   Koopmans, Marion P ^a   Van Den Brand, Judith M A ^a   Haagmans, Bart L ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

^c UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^d CENTRE DE RECERCA EN SANITAT ANIMAL CRESA   (Spain)

^e UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^f Artemis One Health   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

DIPEPTIDYL PEPTIDASE IV; MESSENGER RNA; UBIQUITIN C; VIRUS RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRONCHIOLE; BRONCHUS; CONTROLLED STUDY; DAPB GENE; DROMEDARY; GENE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN SITU HYBRIDIZATION; KIDNEY CORTEX; LOWER RESPIRATORY TRACT; LUNG ALVEOLUS; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; NONHUMAN; NORMAL HUMAN; NOSE MUCOSA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RESPIRATORY EPITHELIUM; RESPIRATORY TRACT MUCOSA; SUBMUCOSA; TISSUE DISTRIBUTION; TRACHEA; UBIQUITIN C GENE; UPPER RESPIRATORY TRACT; VIRUS REPLICATION; ANIMAL; CAMEL; CORONAVIRUS INFECTION; GENE EXPRESSION REGULATION; GENETICS; IMMUNOHISTOCHEMISTRY; METABOLISM; PHYSIOLOGY; RESPIRATORY MUCOSA; TRANSMISSION; VIROLOGY;

ANIMALS; CAMELUS; CORONAVIRUS INFECTIONS; DIPEPTIDYL PEPTIDASE 4; GENE EXPRESSION REGULATION; HUMANS; IMMUNOHISTOCHEMISTRY; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; RECEPTORS, VIRUS; RESPIRATORY MUCOSA; RNA, MESSENGER; VIRUS REPLICATION;

EID: 84964978283     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02994-15     Document Type: Article

References (28)

1. WHO Mers-Cov Research Group. 2013. State of knowledge and data gaps of Middle East respiratory syndrome coronavirus (MERS-CoV) in humans. PLoS Curr 5:ecurrents.outbreaks.0bf719e352e7478f8 ad85fa30127ddb8. doi:http://dx.doi.org/10.1371/currents.outbreaks.0bf719e352e7478f8ad85fa30127ddb8.
2. WHO. 2015. Middle East respiratory syndrome (MERS) in the Republic of Korea. World Health Organization, Geneva, Switzerland. http://www.who.int/csr/disease/coronavirus_infections/situation-assessment/update-15-06-2015/en/.
3. Hemida MG, Chu DK, Poon LL, Perera RA, Alhammadi MA, Ng HY, Siu LY, Guan Y, Alnaeem A, Peiris M. 2014. MERS coronavirus in dromedary camel herd, Saudi Arabia. Emerg Infect Dis 20:1231-1234.
4. Raj VS, Farag EABA, Reusken CBEM, Lamers MM, Pas SD, Voermans J, Smits SL, Osterhaus ADME, Al-Mawlawi N, Al-Romaihi HE, AlHajri MM, El-Sayed AM, Mohran KA, Ghobashy H, Alhajri F, Al-Thani M, Al-Marri SA, El-Maghraby MM, Koopmans MPG, Haagmans BL. 2014. Isolation of MERS coronavirus from a dromedary camel, Qatar, 2014. Emerg Infect Dis 20:1339-1342.
5. Müller MA, Meyer B, Corman VM, Al-Masri M, Turkestani A, Ritz D, Sieberg A, Aldabbagh S, Bosch BJ, Lattwein E, Alhakeem RF, Assiri AM, Albarrak AM, Al-Shangiti AM, Al-Tawfiq JA, Wikramaratna P, Alrabeeah AA, Drosten C, Memish ZA. 2015. Presence of Middle East respiratory syndrome coronavirus antibodies in Saudi Arabia: a nationwide, cross-sectional, serological study. Lancet Infect Dis 15:559-564. http://dx.doi.org/10.1016/S1473-3099(15)70090-3.
6. Müller MA, Corman VM, Jores J, Meyer B, Younan M, Liljander A, Bosch BJ, Lattwein E, Hilali M, Musa BE, Bornstein S, Drosten C. 2014. MERS coronavirus neutralizing antibodies in camels, Eastern Africa, 1983-1997. Emerg Infect Dis 20:2093-2095.
7. Reusken CB, Ababneh M, Raj VS, Meyer B, Eljarah A, Abutarbush S, Godeke GJ, Bestebroer TM, Zutt I, Müller MA, Bosch BJ, Rottier PJ, Osterhaus AD, Drosten C, Haagmans BL, Koopmans MP. 2013. Middle East respiratory syndrome coronavirus (MERS-CoV) serology in major livestock species in an affected region in Jordan, June to September 2013. Euro Surveill 18:20662. http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=20662. http://dx.doi.org/10.2807/1560-7917.ES2013.18.50.20662.
8. Meyer B, Müller MA, Corman VM, Reusken CB, Ritz D, Godeke GJ, Lattwein E, Kallies S, Siemens A, van Beek J, Drexler JF, Muth D, Bosch BJ, Wernery U, Koopmans MP, Wernery R, Drosten C. 2014. Antibodies against MERS coronavirus in dromedary camels, United Arab Emirates, 2003 and 2013. Emerg Infect Dis 20:552-559. http://dx.doi.org/10.3201/eid2004.131746.
9. Reusken CB, Farag EA, Haagmans BL, Mohran KA, Godeke GJ, V, Raj S, Alhajri F, Al-Marri SA, Al-Romaihi HE, Al-Thani M, Bosch BJ, van der Eijk AA, El-Sayed AM, Ibrahim AK, Al-Molawi N, Müller MA, Pasha SK, Drosten C, AlHajri MM, Koopmans MP. 2015. Occupational exposure to dromedaries and risk for MERS-CoV infection, Qatar, 2013-2014. Emerg Infect Dis 21:1422-1425. http://dx.doi.org/10.3201/eid2108.150481.
10. Drosten C, Meyer B, Müller MA, Corman VM, Al-Masri M, Hossain R, Madani H, Sieberg A, Bosch BJ, Lattwein E, Alhakeem RF, Assiri AM, Hajomar W, Albarrak AM, Al-Tawfiq JA, Zumla AI, Memish ZA. 2014. Transmission of MERS-coronavirus in household contacts. N Engl J Med 371:828-835. http://dx.doi.org/10.1056/NEJMoa1405858.
11. Memish ZA, Al-Tawfiq JA, Makhdoom HQ, Al-Rabeeah AA, Assiri A, Alhakeem RF, AlRabiah FA, Al Hajjar S, Albarrak A, Flemban H, Balkhy H, Barry M, Alhassan S, Alsubaie S, Zumla A. 2014. Screening for Middle East respiratory syndrome coronavirus infection in hospital patients and their healthcare worker and family contacts: a prospective descriptive study. Clin Microbiol Infect 20:469-474. http://dx.doi.org/10.1111/1469-0691.12562.
12. Adney DR, van Doremalen N, Brown VR, Bushmaker T, Scott D, de Wit E, Bowen RA, Munster VJ. 2014. Replication and shedding of MERS-CoV in upper respiratory tract of inoculated dromedary camels. Emerg Infect Dis 20:1999-2005. http://dx.doi.org/10.3201/eid2012.141280.
13. Drosten C, Seilmaier M, Corman VM, Hartmann W, Scheible G, Sack S, Guggemos W, Kallies R, Muth D, Junglen S, Müller MA, Haas W, Guberina H, Rohnisch T, Schmid-Wendtner M, Aldabbagh S, Dittmer U, Gold H, Graf P, Bonin F, Rambaut A, Wendtner CM. 2013. Clinical features and virological analysis of a case of Middle East respiratory syndrome coronavirus infection. Lancet Infect Dis 13:745-751. http://dx.doi.org/10.1016/S1473-3099(13)70154-3.
14. Boonacker E, Van Noorden CJ. 2003. The multifunctional or moonlighting protein CD26/DPPIV. Eur J Cell Biol 82:53-73. http://dx.doi.org/10.1078/0171-9335-00302.
15. Raj VS, Mou H, Smits SL, Dekkers DH, Müller 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. http://dx.doi.org/10.1038/nature12005.
16. Mattern T, Scholz W, Feller AC, Flad HD, Ulmer AJ. 1991. Expression of CD26 (dipeptidyl peptidase IV) on resting and activated human T-lymphocytes. Scand J Immunol 33:737-748. http://dx.doi.org/10.1111/j.1365-3083.1991.tb02548.x.
17. Anonymous. 2012. Human tissue and medical research: code of conduct for responsible use (2011). Federa, Rotterdam, The Netherlands. https://www.federa.org/sites/default/files/digital_version_first_part_code_of_conduct_in_uk_2011_12092012.pdf.
18. Haagmans BL, van den Brand JMA, Raj VS, Volz A, Wohlsein P, Smits SL, Schipper D, Bestebroer TM, Okba N, Fux R, Bensaid A, Foz DS, Kuiken T, Baumgärtner W, Segalés J, Sutter G, Osterhaus ADME. 2016. An orthopoxvirus-based vaccine reduces virus excretion afterMERScoronavirus infection in dromedary camels. Science 351:77-81. http://dx.doi.org/10.1126/science.aad1283.
19. Wang F, Flanagan J, Su N, Wang LC, Bui S, Nielson A, Wu X, Vo HT, Ma XJ, Luo Y. 2012. RNAscope: a novel in situ RNA analysis platform for formalin-fixed, paraffin-embedded tissues. J Mol Diagn 14:22-29. http://dx.doi.org/10.1016/j.jmoldx.2011.08.002.
20. Geller C, Varbanov M, Duval RE. 2012. Human coronaviruses: insights into environmental resistance and its influence on the development of new antiseptic strategies. Viruses 4:3044-3068. http://dx.doi.org/10.3390/v4113044.
21. Meyerholz DK, Lambertz AM, McCray PB, Jr. 2016. Dipeptidyl peptidase 4 distribution in the human respiratory tract: implications for the Middle East respiratory syndrome. Am J Pathol 186:78-86. http://dx.doi.org/10.1016/j.ajpath.2015.09.014.
22. Hocke AC, Becher A, Knepper J, Peter A, Holland G, Tonnies M, Bauer TT, Schneider P, Neudecker J, Muth D, Wendtner CM, Ruckert JC, Drosten C, Gruber AD, Laue M, Suttorp N, Hippenstiel S, Wolff T. 2013. Emerging human Middle East respiratory syndrome coronavirus causes widespread infection and alveolar damage in human lungs. Am J Respir Crit Care Med 188:882-886. http://dx.doi.org/10.1164/rccm.201305-0954LE.
23. Bermingham A, Chand MA, Brown CS, Aarons E, Tong C, Langrish C, Hoschler K, Brown K, Galiano M, Myers R, Pebody RG, Green HK, Boddington NL, Gopal R, Price N, Newsholme W, Drosten C, Fouchier RA, Zambon M. 2012. Severe respiratory illness caused by a novel coronavirus, in a patient transferred to the United Kingdom from the Middle East, September 2012. Euro Surveill 17:20290. http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=20290.
24. de Graaf M, Fouchier RA. 2014. Role of receptor binding specificity in influenza A virus transmission and pathogenesis. EMBO J 33:823-841. http://dx.doi.org/10.1002/embj.201387442.
25. Liu L, Wei Q, Alvarez X, Wang H, Du Y, Zhu H, Jiang H, Zhou J, Lam P, Zhang L, Lackner A, Qin C, Chen Z. 2011. Epithelial cells lining salivary gland ducts are early target cells of severe acute respiratory syndrome coronavirus infection in the upper respiratory tracts of rhesus macaques. J Virol 85:4025-4030. http://dx.doi.org/10.1128/JVI.02292-10.
26. Wickham LA, Huang Z, Lambert RW, Sullivan DA. 1997. Effect of sialodacryoadenitis virus exposure on acinar epithelial cells from the rat lacrimal gland. Ocul Immunol Inflamm 5:181-195. http://dx.doi.org/10.3109/09273949709116893.
27. Agu RU, Obimah DU, Lyzenga WJ, Jorissen M, Massoud E, Verbeke N. 2009. Specific aminopeptidases of excised human nasal epithelium and primary culture: a comparison of functional characteristics and gene transcripts expression. J Pharm Pharmacol 61:599-606. http://dx.doi.org/10.1211/jpp/61.05.0008.
28. Abe M, Havre PA, Urasaki Y, Ohnuma K, Morimoto C, Dang LH, Dang NH. 2011. Mechanisms of confluence-dependent expression of CD26 in colon cancer cell lines. BMC Cancer 11:51. http://dx.doi.org/10.1186/1471-2407-11-51.