Porcine aminopeptidase N is not a cellular receptor of porcine epidemic diarrhea virus, but promotes its infectivity via aminopeptidase activity

Journal of General Virology

Volumn 97, Issue 10, 2016, Pages 2528-2539

  Shirato, Kazuya ^a   Maejima, Madoka ^a   Islam, Md Taimur ^b   Miyazaki, Ayako ^c   Kawase, Miyuki ^a   Matsuyama, Shutoku ^a   Taguchi, Fumihiro ^a,b  

^a NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^b NIPPON VETERINARY AND LIFE SCIENCE UNIVERSITY   (Japan)

^c NATIONAL INSTITUTE OF ANIMAL HEALTH   (Japan)

Author keywords

Porcine aminopeptidase N (pAPN); Porcine epidemic diarrhea virus (PEDV); Receptor

Indexed keywords

MICROSOMAL AMINOPEPTIDASE; VIRUS RECEPTOR;

ANIMAL; CORONAVIRUS INFECTION; ENZYMOLOGY; GENETICS; METABOLISM; PHYSIOLOGY; PIG; PORCINE EPIDEMIC DIARRHEA VIRUS; SWINE DISEASE; VETERINARY; VIROLOGY;

ANIMALS; ANTIGENS, CD13; CORONAVIRUS INFECTIONS; PORCINE EPIDEMIC DIARRHEA VIRUS; RECEPTORS, VIRUS; SWINE; SWINE DISEASES;

EID: 84991574465     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/jgv.0.000563     Document Type: Article

References (51)

1. Balliet, J. W., Berson, J., D’Cruz, C. M., Huang, J., Crane, J., Gilbert, J. M. & Bates, P. (1999). Production and characterization of a soluble, active form of Tva, the subgroup a avian sarcoma and leukosis virus receptor. J Virol 73, 3054-3061.
2. Breslin, J. J., Mørk, I., Smith, M. K., Vogel, L. K., Hemmila, E. M., Bonavia, A., Talbot, P. J., Sjöström, H., Norén, O. & Holmes, K. V. (2003). Human coronavirus 229E: receptor binding domain and neutralization by soluble receptor at 37 degrees C. J Virol 77, 4435-4438.
3. Chasey, D. & Cartwright, S. F. (1978). Virus-like particles associated with porcine epidemic diarrhoea. Res Vet Sci 25, 255-256.
4. Chen, J. F., Sun, D. B., Wang, C. B., Shi, H. Y., Cui, X. C., Liu, S. W., Qiu, H. J. & Feng, L. (2008). Molecular characterization and phylogenetic analysis of membrane protein genes of porcine epidemic diarrhea virus isolates in China. Virus Genes 36, 355-364.
5. Chen, L., Lin, Y. L., Peng, G. & Li, F. (2012). Structural basis for multifunctional roles of mammalian aminopeptidase N. Proc Natl Acad Sci U S A 109, 17966-17971.
6. Chen, Q., Li, G., Stasko, J., Thomas, J. T., Stensland, W. R., Pillatzki, A. E., Gauger, P. C., Schwartz, K. J., Madson, D. & other authors (2014). Isolation and characterization of porcine epidemic diarrhea viruses associated with the 2013 disease outbreak among swine in the United States. J Clin Microbiol 52, 234-243.
7. Cong, Y., Li, X., Bai, Y., Lv, X., Herrler, G., Enjuanes, L., Zhou, X., Qu, B., Meng, F. & other authors (2015). Porcine aminopeptidase N mediated polarized infection by porcine epidemic diarrhea virus in target cells. Virology 478, 1-8.
8. Delmas, B., Gelfi, J., L’Haridon, R., Vogel, L. K., Sjöström, H., Norén, O. & Laude, H. (1992). Aminopeptidase N is a major receptor for the entero-pathogenic coronavirus TGEV. Nature 357, 417-420.
9. Delmas, B., Gelfi, J., Kut, E., Sjöström, H., Noren, O. & Laude, H. (1994). Determinants essential for the transmissible gastroenteritis virus-receptor interaction reside within a domain of aminopeptidase-N that is distinct from the enzymatic site. J Virol 68, 5216-5224.
10. Hofmann, M. & Wyler, R. (1988). Propagation of the virus of porcine epidemic diarrhea in cell culture. J Clin Microbiol 26, 2235-2239.
11. Holmes, K. V. & Compton, S. R. (1995). Coronavirus receptors. In The Coronaviridae, pp. 55-71. Edited by S. G. Siddell. New York, NY: Plenum Press.
12. Huang, Y. W., Dickerman, A. W., Piñeyro, P., Li, L., Fang, L., Kiehne, R., Opriessnig, T. & Meng, X. J. (2013). Origin, evolution, and genotyping of emergent porcine epidemic diarrhea virus strains in the United States. MBio 4, e00737-13.
13. Hussey, R. E., Richardson, N. E., Kowalski, M., Brown, N. R., Chang, H. C., Siliciano, R. F., Dorfman, T., Walker, B., Sodroski, J. & Reinherz, E. L. (1988). A soluble CD4 protein selectively inhibits HIV replication and syncytium formation. Nature 331, 78-81.
14. Islam, M. T., Kubota, T., Ujike, M., Yahara, Y. & Taguchi, F. (2016). Phylogenetic and antigenic characterization of newly isolated porcine epidemic diarrhea viruses in Japan. Virus Res 222, 113-119.
15. Kaplan, G., Peters, D. & Racaniello, V. R. (1990). Poliovirus mutants resistant to neutralization with soluble cell receptors. Science 250, 1596-1599.
16. Kawase, M., Shirato, K., Matsuyama, S. & Taguchi, F. (2009). Protease-mediated entry via the endosome of human coronavirus 229E. J Virol 83, 712-721.
17. Kawase, M., Shirato, K., van der Hoek, L., Taguchi, F. & Matsuyama, S. (2012). Simultaneous treatment of human bronchial epithelial cells with serine and cysteine protease inhibitors prevents severe acute respiratory syndrome coronavirus entry. J Virol 86, 6537-6545.
18. Kenny, A. J. & Maroux, S. (1982). Topology of microvillar membrance hydrolases of kidney and intestine. Physiol Rev 62, 91-128.
19. Kim, O. & Chae, C. (2000). In situ hybridization for the detection and localization of porcine epidemic diarrhea virus in the intestinal tissues from naturally infected piglets. Vet Pathol 37, 62-67.
20. Kusanagi, K., Kuwahara, H., Katoh, T., Nunoya, T., Ishikawa, Y., Samejima, T. & Tajima, M. (1992). Isolation and serial propagation of porcine epidemic diarrhea virus in cell cultures and partial characterization of the isolate. J Vet Med Sci 54, 313-318.
21. Lai, M. M. & Cavanagh, D. (1997). The molecular biology of corona-viruses. Adv Virus Res 48, 1-100.
22. Li, B. X., Ge, J. W. & Li, Y. J. (2007). Porcine aminopeptidase N is a functional receptor for the PEDV coronavirus. Virology 365, 166-172.
23. Li, W., Moore, M. J., Vasilieva, N., Sui, J., Wong, S. K., Berne, M. A., Somasundaran, M., Sullivan, J. L., Luzuriaga, K. & other authors (2003). Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 426, 450-454.
24. Li, W., Li, H., Liu, Y., Pan, Y., Deng, F., Song, Y., Tang, X. & He, Q. (2012). New variants of porcine epidemic diarrhea virus, China, 2011. Emerg Infect Dis 18, 1350-1353.
25. Liu, C., Tang, J., Ma, Y., Liang, X., Yang, Y., Peng, G., Qi, Q., Jiang, S., Li, J. & other authors (2015). Receptor usage and cell entry of porcine epidemic diarrhea coronavirus. J Virol 89, 6121-6125.
26. Meng, F., Suo, S., Zarlenga, D. S., Cong, Y., Ma, X., Zhao, Q. & Ren, X. (2014). A phage-displayed peptide recognizing porcine aminopeptidase N is a potent small molecule inhibitor of PEDV entry. Virology 456-457, 20-27.
27. Nam, E. & Lee, C. (2010). Contribution of the porcine aminopeptidase N (CD13) receptor density to porcine epidemic diarrhea virus infection. Vet Microbiol 144, 41-50.
28. Oh, J. S., Song, D. S. & Park, B. K. (2003). Identification of a putative cellular receptor 150 kda polypeptide for porcine epidemic diarrhea virus in porcine enterocytes. J Vet Sci 4, 269-275.
29. Pan, Y., Tian, X., Li, W., Zhou, Q., Wang, D., Bi, Y., Chen, F. & Song, Y. (2012). Isolation and characterization of a variant porcine epidemic diarrhea virus in China. Virol J 9, 195.
30. Park, J. E., Park, E. S., Yu, J. E., Rho, J., Paudel, S., Hyun, B. H., Yang, D. K. & Shin, H. J. (2015). Development of transgenic mouse model expressing porcine aminopeptidase N and its susceptibility to porcine epidemic diarrhea virus. Virus Res 197, 108-115.
31. Park, S. J., Moon, H. J., Yang, J. S., Lee, C. S., Song, D. S., Kang, B. K. & Park, B. K. (2007). Sequence analysis of the partial spike glycoprotein gene of porcine epidemic diarrhea viruses isolated in Korea. Virus Genes 35, 321-332.
32. Pensaert, M. B. & de Bouck, P. (1978). A new coronavirus-like particle associated with diarrhea in swine. Arch Virol 58, 243-247.
33. Puranaveja, S., Poolperm, P., Lertwatcharasarakul, P., Kesdaengsakonwut, S., Boonsoongnern, A., Urairong, K., Kitikoon, P., Choojai, P., Kedkovid, R. & other authors (2009). Chinese-like strain of porcine epidemic diarrhea virus, Thailand. Emerg Infect Dis 15, 1112-1115.
34. Raj, V. S., Mou, H., Smits, S. L., Dekkers, D. H., Müller, M. A., Dijkman, R., Muth, D., Demmers, J. A., Zaki, A. & other authors (2013). Dipeptidyl peptidase 4 is a functional receptor for the emerging human coronavirus-EMC. Nature 495, 251-254.
35. Saeki, K., Ohtsuka, N. & Taguchi, F. (1997). Identification of spike protein residues of murine coronavirus responsible for receptor-binding activity by use of soluble receptor-resistant mutants. J Virol 71, 9024-9031.
36. Semenza, G. (1986). Anchoring and biosynthesis of stalked brush border membrane proteins: glycosidases and peptidases of enterocytes and renal tubuli. Annu Rev Cell Biol 2, 255-313.
37. Shibata, I., Tsuda, T., Mori, M., Ono, M., Sueyoshi, M. & Uruno, K. (2000). Isolation of porcine epidemic diarrhea virus in porcine cell cultures and experimental infection of pigs of different ages. Vet Microbiol 72, 173-182.
38. Shirato, K., Maejima, M., Hirai, A., Ami, Y., Takeyama, N., Tsuchiya, K., Kusanagi, K., Nunoya, T. & Taguchi, F. (2010). Enhanced cell fusion activity in porcine epidemic diarrhea virus adapted to suckling mice. Arch Virol 155, 1989-1995.
39. Shirato, K., Matsuyama, S., Ujike, M. & Taguchi, F. (2011). Role of proteases in the release of porcine epidemic diarrhea virus from infected cells. J Virol 85, 7872-7880.
40. Sun, R. Q., Cai, R. J., Chen, Y. Q., Liang, P. S., Chen, D. K. & Song, C. X. (2012). Outbreak of porcine epidemic diarrhea in suckling piglets, China. Emerg Infect Dis 18, 161-163.
41. Tresnan, D. B., Levis, R. & Holmes, K. V. (1996). Feline aminopeptidase N serves as a receptor for feline, canine, porcine, and human coronaviruses in serogroup I. J Virol 70, 8669-8674.
42. Turgeon, D. C., Morin, M., Jolette, J., Higgins, R., Marsolais, G. & DiFranco, E. (1980). Coronavirus-like particles associated with diarrhea in baby pigs in Quebec. Can Vet J 21, 100-123.
43. Umezawa, H., Aoyagi, T., Suda, H., Hamada, M. & Takeuchi, T. (1976). Bestatin, an inhibitor of aminopeptidase B, produced by actinomycetes. J Antibiot (Tokyo) 29, 97-99.
44. Vui, D. T., Tung, N., Inui, K., Slater, S. & Nilubol, D. (2014). Complete genome sequence of porcine epidemic diarrhea virus in Vietnam. Genome Announc 2, e00753-14.
45. Wang, L., Byrum, B. & Zhang, Y. (2014). New variant of porcine epidemic diarrhea virus, United States, 2014. Emerg Infect Dis 20, 917-919.
46. Watanabe, R., Matsuyama, S., Shirato, K., Maejima, M., Fukushi, S., Morikawa, S. & Taguchi, F. (2008). Entry from the cell surface of severe acute respiratory syndrome coronavirus with cleaved S protein as revealed by pseudotype virus bearing cleaved S protein. J Virol 82, 11985-11991.
47. Weiss, S. R. & Navas-Martin, S. (2005). Coronavirus pathogenesis and the emerging pathogen severe acute respiratory syndrome coronavirus. Microbiol Mol Biol Rev 69, 635-664.
48. Williams, R. K., Jiang, G. S. & Holmes, K. V. (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.
49. Würdinger, T., Verheije, M. H., Raaben, M., Bosch, B. J., de Haan, C. A., van Beusechem, V. W., Rottier, P. J. & Gerritsen, W. R. (2005). Targeting non-human coronaviruses to human cancer cells using a bispecific single-chain antibody. Gene Ther 12, 1394-1404.
50. Yang, C. W., Yang, Y. N., Liang, P. H., Chen, C. M., Chen, W. L., Chang, H. Y., Chao, Y. S. & Lee, S. J. (2007). Novel small-molecule inhibitors of transmissible gastroenteritis virus. Antimicrob Agents Chemother 51, 3924-3931.
51. Yeager, C. L., Ashmun, R. A., Williams, R. K., Cardellichio, C. B., Shapiro, L. H., Look, A. T. & Holmes, K. V. (1992). Human aminopeptidase N is a receptor for human coronavirus 229E. Nature 357, 420-422.