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Human and Bovine Coronaviruses Recognize Sialic Acid-Containing Receptors Similar to Those of Influenza C Viruses

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Human and Bovine Coronaviruses Recognize Sialic Acid-Containing Receptors Similar to Those of Influenza C Viruses Proc. Natl. Acad. Sci. USA Vol. 85, pp. 4526-4529, June 1988 Microbiology Human and bovine coronaviruses recognize sialic acid-containing receptors similar to those of influenza C viruses (receptor-destroying enzyme/acetylesterase/hemagglutlnation/gangliosides) REINHARD VLASAK*, WILLEM LUYTJESt, WILLY SPAANt, AND PETER PALESE* *Mount Sinai School of Medicine, Department of Microbiology, New York, NY 10029; and tState University of Utrecht, Department of Infectious Diseases and Immunology, Utrecht, The Netherlands Communicated by Bernard N. Fields, March 2, 1988 (receivedfor review January 21, 1988) ABSTRACT Human coronavirus OC43 and bovine coro- Thus the published evidence does not necessarily exclude navirus elute from agglutinated chicken erythrocytes when the possibility that coronaviruses recognize modified sialic incubated at 37TC, suggesting the presence of a receptor- acids as cell receptors, and we suggest in the present study destroying enzyme. Moreover, bovine coronavirus exhibits an that HCV OC43 and BCV bind to sialylated receptors similar acetylesterase activity in vitro using bovine submaillary mucin to those recognized by influenza C viruses. Furthermore, we as substrate similar to the enzymatic activity found in influenza report that BCV possesses an esterase activity that may C viruses. Furthermore, pretreatment of erythrocytes with function as receptor-destroying enzyme. either influenza C virus or bovine coronavirus eliminates subsequent binding and agglutination by either coronaviruses or influenza C virus, whereas binding of influenza A virus MATERIALS AND METHODS remains intact. In addition, hemag-utination by coronaviruses Viruses and Cells. HCV OC43 was obtained from the can be inhibited by pretreatment of erythrocytes with Arthro- American Type Culture Collection (ATCC 759-VR). BCV bacter ureafaciens or Closrtidimwperfringens neuraminidase or was obtained from Duphar B. V. Weesp (Amsterdam). BCV by addition ofsialic acid-containing gangliosides. These results was grown in Madin-Darby bovine kidney (MDBK) cells, suggest that, like influenza C viruses, human coronavirus concentrated by polyethylene glycol precipitation (17), and OC43 and bovine coronavirus recognize 0-acetylated'sialic purified on a 20-60% sucrose step gradient as described (18). acid or a similar derivative as cell receptor. Influenza C/JHG/66 virus and influenza A/PR/8/34 virus were grown in embryonated eggs as described (19). Chicken, Coronaviruses have been associated with a variety of dis- mouse, and rat erythrocytes in Alsever's solution were eases in many different host species (1-3). Human corona- obtained from Pocono Rabbit Farm (Canadensis, PA). virus strain OC43 (HCV OC43) in general affects the respi- Removal of Receptors. Five percent erythrocyte suspen- ratory tract (4), causing symptoms similar to those of rhino- sions in phosphate-buffered saline (PBS) were incubated with viruses or influenza viruses, whereas bovine coronavirus influenza C virus, BCV, 200 milliunits of Clostridium per- (BCV) is the cause of enteric infections in cattle (5). Mouse fringens neuraminidase per ml (type IV, Sigma; EC 3.2.1.18) hepatitis virus (MHV), a third virus that belongs to the same or 200 milliunits of Arthrobacter ureafaciens neuraminidase antigenic cluster of coronaviruses (6), may infect different per ml (Boehringer Mannheim; EC 3.2.1.18). All incubations organs, causing enteric, respiratory, and neurologic disease were performed at pH 7.2 and 370C. Incubation time was (7, 8). Recently, substantial sequence similarity was ob- usually 1 hr, except when BCV was used, for which incuba- served (W.L. and W.S., unpublished data) between an open tion time was 3 hr. After incubation, cells were washed four reading frame encoded by mRNA2 of MHV strain A59 and times with PBS and finally resuspended in the same buffer to the influenza C virus HE protein, which exhibits receptor- 0.5% (vol/vol). Control incubations were done with PBS. binding and receptor-destroying (esterase) activity (9, 10). Binding Assays. Hemagglutination and hemagglutination- Therefore we reexamined the possibility that coronaviruses inhibition assays were done in V-shaped microtiter plates might recognize cell receptors similar to those of influenza (Flow Laboratories) as described (20). Bovine brain ganglio- viruses. Earlier studies (11) revealed that treatment of eryth- sides (type III) were obtained from Sigma. rocytes with Vibrio cholerae neuraminidase (EC 3.2.1.18) did Acetylesterase Assay. Virus preparations were suspended not remove cell receptors recognized by HCV OC38 and in 50 A1 of PBS, mixed with 250 pl of bovine submaxillary OC43, and no neuraminidase activity was found to be mucin (type I, Sigma; 25 mg/ml), and incubated at 370C. At associated with HCV OC43 (12, 13). It was also reported that different times the presence of acetate was determined by the hemagglutination pattern of avian infectious bronchitis using a test kit (Boehringer Mannheim). A polyethylene virus and of a mouse enteric coronavirus was unstable at glycol precipitate (17) from a culture supernatant of mock- elevated temperature, suggesting the presence of a receptor- infected MDBK cells was used as control. destroying enzyme (14, 15). In all of those instances, how- ever, the receptor-binding and/or receptor-destroying activ- ity was found to be different from those of influenza A virus. RESULTS Recently, a plasma membrane protein with affinity for MHV Preliminary tests were performed to select erythrocytes that strain A59 was described and its presence or absence was were agglutinated by all viruses used in the study. As correlated with differences in virus susceptibility of target described earlier, HCV OC43 and BCV were found to cells (16). However, the precise mechanism of interaction agglutinate mouse and rat erythrocytes (11, 21). Since avian between the host cell protein and the virus was not eluci- erythrocytes were routinely used in the laboratory for agglu- datted. tination by influenza A and C viruses we tested these cells The publication costs ofthis article were defrayed in part by page charge Abbreviations: HCV OC43, human coronavirus OC43; BCV, bovine payment. This article must therefore be hereby marked "advertisement" coronavirus; MHV, mouse hepatitis virus; MDBK, Madin-Darby in accordance with 18 U.S.C. §1734 solely to indicate this fact. bovine kidney. Downloaded by guest on September 30, 2021 4526 Microbiology: Vlasak et al. Proc. Natl. Acad. Sci. USA 85 (1988) 4527 and found that BCV and HCV OC43 also agglutinated these erythrocytes. Therefore all experiments were done with a A~ _a HICV OC43 avian erythrocytes. q';j¢us * BCV Hemagglutination titers were determined after incubation A 0~ _p C/JIIG/66 for 1 hr at 40C. If incubation was continued at room 4 temperature or at 370C we observed elution of HCV OC43 A/PR/8/3- and BCV, which started in wells containing the highest concentration ofvirus. This phenomenon has been described in earlier studies on HCV OC43 (11) and had been used for HCV OC43 partial purification ofthis virus (22). Since elution is observed }BCV% regularly with viruses containing a receptor-destroying en- B I Ak zyme (23-25), we proceeded to test BCV for a similar rr _ % C/JlIG/66 activity. Specifically, the sequence similarity between an t'a N.N m t ta t taa at N'%m open reading frame in the mRNA2 of MHV A59 and the %A..AV Xt~w' A/PR/8/34 influenza C virus HE protein (W.L. and W.S., unpublished data) led us to test for the presence of an influenza C virus-like activity. The influenza C virus receptor-destroying ,vb$;rtjffe 51g5) IICV OC43 activity is a sialate O-acetylesterase (EC 3.1.1.53) (10), which can be measured in vitro by using synthetic (9) and natural (10) esterase substrates such as p-nitrophenylacetate and !(W~~C/JINQ~~~)$4>* IG/66 bovine submaxillary mucin, respectively. We tested for the presence of acetylesterase activity in BCV, using bovine A/PR/8/34 submaxillary mucin as substrate (Fig. 1). Purified prepara- FIG. 2. Removal of cell receptors by treatment with BCV. tions of BCV and influenza C virus released comparable Hemagglutination was performed at 4°C using chicken erythrocytes amounts of acetate over time. Control preparations of mock- and at serial 1:2 dilutions (left to right) human coronavirus OC43, infected MDBK cells or of influenza A virus did not hydro- BCV, influenza C/JHG/66 virus, or influenza A/PR/8/34 virus. (A) lyze the O-acetylated sialic acids in bovine submaxillary Untreated erythrocytes. (B) One-half milliliter of erythrocytes (5%) mucin. This experiment suggests the presence of an enzyme was preincubated with purified BCV (420 jig) for 3 hr at 37°C, in BCV with specificities similar to those of the influenza C washed, resuspended to 0.5%, and used in the assay. (C) One-half virus HE protein. milliliter of erythrocytes (5%) was pretreated for 1 hr at 37°C with We then asked whether this esterase activity associated concentrated influenza C/JHG/66 virus (250 ,ug), washed, resus- with BCV eliminates virus receptors similar to those de- pended, and used as in B. stroyed by the influenza C virus HE protein. For further suggested that the receptor-destroying activity of BCV af- experiments we selected avian erythrocytes derived from fects viral cell receptors recognized by another coronavirus chicken strain Rhode Island Red sex-linked chromosome X, (HCV OC43) as well as by influenza C virus. In contrast, which gave the most rapid elution patterns for HCV OC43 receptors for influenza A virus were not altered by the BCV and BCV at 37°C. Suspensions of erythrocytes were incu- The analogous experiment using the influenza C bated with concentrated BCV or influenza C/JHG/66 virus enzyme. at 37°C. Cells then were washed four times with PBS, virus receptor-destroying enzyme is shown in Fig. 2C. resuspended to a 0.5% (vol/vol) suspension, and used for Treatment of erythrocytes with influenza C/JHG/66 virus hemagglutination assays.
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