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MERS Coronaviruses from Camels in Africa Exhibit Region-Dependent Genetic Diversity

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MERS Coronaviruses from Camels in Africa Exhibit Region-Dependent Genetic Diversity MERS coronaviruses from camels in Africa exhibit region-dependent genetic diversity Daniel K. W. Chua,1, Kenrie P. Y. Huia,1, Ranawaka A. P. M. Pereraa,1, Eve Miguelb,c,1, Daniela Niemeyerd, Jincun Zhaoe,f, Rudragouda Channappanavare, Gytis Dudasg, Jamiu O. Oladipoa,h, Amadou Traoréi,OuafaaFassi-Fihrij, Abraham Alik, Getnet F. Demissiél, Doreen Muthd, Michael C. W. Chana, John M. Nichollsm, David K. Meyerholzn, Sulyman A. Kurangah, Gezahegne Mamoo, Ziqi Zhoua, Ray T. Y. Soa, Maged G. Hemidap,q, Richard J. Webbyr, Francois Rogerb,s, Andrew Rambautt,u, Leo L. M. Poona, Stanley Perlmane, Christian Drostend, Veronique Chevalierb,v, and Malik Peirisa,2 aSchool of Public Health, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region, Republic of China; bAnimal, Santé, Territoires, Risques et Ecosystèmes, Centre de Coopération Internationale en Recherche Agronomique pour le Développement, Institut National de la Recherche Agronomique, Université de Montpellier, F-34398 Montpellier, France; cMaladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle, L’Institut de Recherche pour le Développement, CNRS, Universitè de Montpellier, F-34398 Montpellier, France; dInstitute of Virology, Campus Charite Mitte, Charite-Universitätsmedizin Berlin, 10117 Berlin, Germany; eDepartment of Microbiology and Immunology, University of Iowa, Iowa City, IA 52242; fState Key Laboratory of Respiratory Disease, National Clinical Research Center for Respiratory Disease, Guangzhou Institute of Respiratory Disease, The First Affiliated Hospital of Guangzhou Medical University, Guangdong, Republic of China 510000; gVaccine and Infectious Diseases Division, Fred Hutchinson Cancer Research Center, Seattle, WA 98109; hDepartment of Surgery, Faculty of Clinical Sciences, University of Ilorin, Ilorin, Nigeria; iLaboratoire de Biologie et Santé Animals, L’Institut de l’Environnement et de Recherches Agricoles du Burkina Faso/Centre National de la Recherche Scientifique et Technologique, 04 BP 8645 Ouagadougou 04, Burkina Faso; jInstitut Agronomique et Vétérinaire, Hassan II Université, B.P. 6202 Rabat-Instituts, Rabat, Morocco; kBacterial, Parasitic and Zoonotic Diseases Research Directorate, Ethiopian Public Health Institute, Addis Ababa, Ethiopia; lCollege of Veterinary Medecine, Haramaya University, Dire Dawa, Ethiopia; mDepartment of Pathology, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Hong Kong Special Administrative Region, China; nDepartment of Pathology, University of Iowa, Iowa City, IA 52242; oDepartment of Veterinary Microbiology, Immunology and Public Health, College of Veterinary Medicine and Agriculture, Addis Ababa University, Bishoftu, Ethiopia; pDepartment of Microbiology and Parasitology, College of Veterinary Medicine, King Faisal University, Al-Hasa, Saudi Arabia; qDepartment of Virology, Faculty of Veterinary Medicine, Kafrelsheikh University, Kafrelsheikh, Egypt; rDepartment of Infectious Diseases, St. Jude Children’s Research Hospital, Memphis, TN 38105; sKasetsart University, 10900 Bangkok, Thailand; tInstitute of Evolutionary Biology, University of Edinburgh, EH9 2FL Edinburgh, United Kingdom; uFogarty International Center, National Institutes of Health, Bethesda, MD 20892; and vInstitut Pasteur du Cambodge, Phnom Penh, Cambodia Contributed by Malik Peiris, February 6, 2018 (sent for review November 3, 2017; reviewed by Stephen S. Morse and Vincent J. Munster) Middle East respiratory syndrome coronavirus (MERS-CoV) causes a zoonotic infections have not been reported from Africa. Hypotheses zoonotic respiratory disease of global public health concern, and for this pattern of zoonotic disease include genetic differences in the dromedary camels are the only proven source of zoonotic infection. viruses; cultural, behavioral, or dietary differences in interactions Although MERS-CoV infection is ubiquitous in dromedaries across Africa between humans and camels and camel products; or unnoticed as well as in the Arabian Peninsula, zoonotic disease appears confined to human cases through lack of awareness and surveillance in African the Arabian Peninsula. MERS-CoVs from Africa have hitherto been countries. Data on phylogenetic and phenotypic characterization of poorly studied. We genetically and phenotypically characterized MERS- CoV from dromedaries sampled in Morocco, Burkina Faso, Nigeria, and Significance Ethiopia. Viruses from Africa (clade C) are phylogenetically distinct from contemporary viruses from the Arabian Peninsula (clades A and B) but Middle East respiratory syndrome (MERS) is a zoonotic disease remain antigenically similar in microneutralization tests. Viruses from of global health concern, and dromedary camels are the source West (Nigeria, Burkina Faso) and North (Morocco) Africa form a of human infection. Although Africa has the largest number of subclade, C1, that shares clade-defining genetic signatures including dromedary camels, and MERS-coronavirus (MERS-CoV) is en- deletions in the accessory gene ORF4b.Comparedwithhumanand demic in these camels, locally acquired zoonotic MERS is not camel MERS-CoV from Saudi Arabia, virus isolates from Burkina Faso reported from Africa. However, little is known of the genetic or (BF785) and Nigeria (Nig1657) had lower virus replication compe- phenotypic characterization of MERS-CoV from Africa. In this tence in Calu-3 cells and in ex vivo cultures of human bronchus study we characterize MERS-CoV from Burkina Faso, Nigeria, and lung. BF785 replicated to lower titer in lungs of human DPP4- Morocco, and Ethiopia. We demonstrate viral genetic and phe- transduced mice. A reverse genetics-derived recombinant MERS-CoV notypic differences in viruses from West Africa, which may be (EMC) lacking ORF4b elicited higher type I and III IFN responses than relevant to differences in zoonotic potential, highlighting the the isogenic EMC virus in Calu-3 cells. However, ORF4b deletions may need for studies of MERS-CoV at the animal–human interface. not be the major determinant of the reduced replication competence of BF785 and Nig1657. Genetic and phenotypic differences in West Author contributions: R.J.W., F.R., L.L.M.P., S.P., V.C., and M.P. designed research; African viruses may be relevant to zoonotic potential. There is an D.K.W.C., K.P.Y.H., R.A.P.M.P., E.M., D.N., J.Z., R.C., J.O.O., A.T., O.F.-F., A.A., G.F.D., urgent need for studies of MERS-CoV at the animal–human interface. D.M., M.C.W.C., J.M.N., D.K.M., S.A.K., G.M., Z.Z., R.T.Y.S., M.G.H., and C.D. performed research; C.D. contributed new reagents/analytic tools; G.D., A.R., and M.P. analyzed data; and L.L.M.P., S.P., and M.P. wrote the paper. MERS | coronavirus | evolution | Africa | zoonosis Reviewers: S.S.M., Columbia University; and V.J.M., National Institutes of Health. The authors declare no conflict of interest. iddle East respiratory syndrome (MERS) remains a dis- This open access article is distributed under Creative Commons Attribution-NonCommercial- Mease of global public health concern (1). Many human NoDerivatives License 4.0 (CC BY-NC-ND). infections are zoonotic in origin, but some result from clusters of Data deposition: The sequences reported in this paper have been deposited in the Gen- human-to-human transmission, especially within hospitals and Bank database (accession nos. MG923465–MG923481). health care facilities (2). Zoonotic disease has been reported 1D.K.W.C., K.P.Y.H., R.A.P.M.P., and E.M. contributed equally to this work. from the Arabian Peninsula, and dromedary camels are the only 2To whom correspondence should be addressed. Email: [email protected]. confirmed source of zoonotic infection (3). Although MERS- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. coronavirus (MERS-CoV) is also endemic in dromedaries in 1073/pnas.1718769115/-/DCSupplemental. Africa, where the majority of dromedary camels are found (4–7), Published online March 5, 2018. 3144–3149 | PNAS | March 20, 2018 | vol. 115 | no. 12 www.pnas.org/cgi/doi/10.1073/pnas.1718769115 Downloaded by guest on October 1, 2021 MERS-CoV from Africa are limited. We previously reported the tree), homoplasies (repeat mutations), and reversions within that MERS-CoV from Egypt and Nigeria appear to be phyloge- available MERS-CoV full-genomesequencesisshowninFig. S2. netically distinct from those currently circulating in the Arabian Viruses from Burkina Faso (n = 3), Morocco (n = 1), and Nigeria Peninsula (5, 6). We now report a comprehensive genetic and (n = 9) had signature deletions in the ORF4b and/or ORF3 gene re- phenotypic analysis of MERS-CoV from North (Morocco), West gions (Fig. S3) and are designated “clade C1” (Fig. 1). Clade C viruses (Nigeria, Burkina Faso), and East (Ethiopia) Africa compared from Ethiopia (n = 4) and Egypt (n = 3) did not have such gene with viruses from the Arabian Peninsula. deletions, nor do the majority of viruses from the Arabian Peninsula. However, sequences of two clade B human viruses detected in 2012 Results (Riyadh_1_2012 and Bisha_1_2012) available in public databases also ORF4b Genetic Characterization. The epidemiological aspects of field studies of have short (17-nt) deletions in the region in a similar, although not identical, region as the African isolates (Fig. S3). Targeted se- dromedary camels in Morocco, Burkina Faso, Ethiopia, and Nigeria, ORF3 including seroprevalence and RT-PCR detection of virus from nasal quencing of the /4b gene region was done on additional African swabs, have
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