1887

Journal of General Virology header logo

Volume 92, Issue 2

Adaptive mutations in the genomes of enterovirus 71 strains following infection of mouse cells expressing human P-selectin glycoprotein ligand-1 Open Access

Abstract

We recently identified human P-selectin glycoprotein ligand-1 (PSGL-1) as a functional enterovirus 71 (EV71) receptor and demonstrated PSGL-1-dependent replication for some EV71 strains in human leukocytes. Here, we report that four out of five PSGL-1-binding strains of EV71 replicated poorly in mouse L929 cells stably expressing human PSGL-1 (L-PSGL-1 cells). Therefore, we compared the replication kinetics and entire genomic sequence of five original EV71 strains and the corresponding EV71 variants (EV71-LPS), which were propagated once in L-PSGL-1 cells. Direct sequence comparison of the entire genome of the original EV71 strains and EV71-LPS variants identified several possible adaptive mutations during the course of replication in L-PSGL-1 cells, including a putative determinant of the adaptive phenotype in L-PSGL-1 cells at VP2-149. The results suggest that an adaptive mutation, along with a PSGL-1-binding phenotype, may facilitate efficient PSGL-1-dependent replication of the EV71 strains in L-PSGL-1 cells.

  • Received:
  • Accepted:
  • Published Online:
© SGM
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.022418-0
2011-02-01
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/jgv/92/2/287.html?itemId=/content/journal/jgv/10.1099/vir.0.022418-0&mimeType=html&fmt=ahah

References

  1. Arita, M., Ami, Y., Wakita, T. & Shimizu, H.(2008). Cooperative effect of the attenuation determinants derived from poliovirus Sabin 1 strain is essential for attenuation of enterovirus 71 in the NOD/SCID mouse infection model. J Virol 82, 1787–1797.[CrossRef] [Google Scholar]
  2. Bergelson, J. M., Cunningham, J. A., Droguett, G., Kurt-Jones, E. A., Krithivas, A., Hong, J. S., Horwitz, M. S., Crowell, R. L. & Finberg, R. W.(1997). Isolation of a common receptor for coxsackie B viruses and adenoviruses 2 and 5. Science 275, 1320–1323.[CrossRef] [Google Scholar]
  3. Chan, L. G., Parashar, U. D., Lye, M. S., Ong, F. G. L., Zaki, S. R., Alexander, J. P., Ho, K. K., Han, L. L., Pallansch, M. A. & other authors(2000). Deaths of children during an outbreak of hand, foot, and mouth disease in Sarawak, Malaysia: clinical and pathological characteristics of the disease. Clin Infect Dis 31, 678–683.[CrossRef] [Google Scholar]
  4. Chua, B. H., Phuektes, P., Sanders, S. A., Nicholls, P. K. & McMinn, P. C.(2008). The molecular basis of mouse adaptation by human enterovirus 71. J Gen Virol 89, 1622–1632.[CrossRef] [Google Scholar]
  5. Couderc, T., Delpeyroux, F., Le Blay, H. & Blondel, B.(1996). Mouse adaptation determinants of poliovirus type 1 enhance viral uncoating. J Virol 70, 305–312. [Google Scholar]
  6. Eskelinen, E. L., Tanaka, Y. & Saftig, P.(2003). At the acidic edge: emerging functions for lysosomal membrane proteins. Trends Cell Biol 13, 137–145.[CrossRef] [Google Scholar]
  7. Ho, M., Chen, E. R., Hsu, K. H., Twu, S. J., Chen, K. T., Tsai, S. F., Wang, J. R. & Shih, S. R.(1999). An epidemic of enterovirus 71 infection in Taiwan. N Engl J Med 341, 929–935.[CrossRef] [Google Scholar]
  8. Hovi, T. & Stenvik, M.(1994). Selective isolation of poliovirus in recombinant murine cell line expressing the human poliovirus receptor gene. J Clin Microbiol 32, 1366–1368. [Google Scholar]
  9. Laszik, Z., Jansen, P. J., Cummings, R. D., Tedder, T. F., McEver, R. P. & Moore, K. L.(1996). P-selectin glycoprotein ligand-1 is broadly expressed in cells of myeloid, lymphoid, and dendritic lineage and in some nonhematopoietic cells. Blood 88, 3010–3021. [Google Scholar]
  10. McMinn, P. C.(2002). An overview of the evolution of enterovirus 71 and its clinical and public health significance. FEMS Microbiol Rev 26, 91–107.[CrossRef] [Google Scholar]
  11. Mendelsohn, C. L., Wimmer, E. & Racaniello, V. R.(1989). Cellular receptor for poliovirus: molecular cloning, nucleotide sequence, and expression of a new member of the immunoglobulin superfamily. Cell 56, 855–865.[CrossRef] [Google Scholar]
  12. Mizuta, K., Abiko, C., Murata, T., Matsuzaki, Y., Itagaki, T., Sanjoh, K., Sakamoto, M., Hongo, S., Murayama, S. & Hayasaka, K.(2005). Frequent importation of enterovirus 71 from surrounding countries into the local community of Yamagata, Japan, between 1998 and 2003. J Clin Microbiol 43, 6171–6175.[CrossRef] [Google Scholar]
  13. Murray, M. G., Bradley, J., Yang, X. F., Wimmer, E., Moss, E. G. & Racaniello, V. R.(1988). Poliovirus host range is determined by a short amino acid sequence in neutralization antigenic site I. Science 241, 213–215.[CrossRef] [Google Scholar]
  14. Nagata, N., Shimizu, H., Ami, Y., Tano, Y., Harashima, A., Suzaki, Y., Sato, Y., Miyamura, T., Sata, T. & Iwasaki, T.(2002). Pyramidal and extrapyramidal involvement in experimental infection of cynomolgus monkeys with enterovirus 71. J Med Virol 67, 207–216.[CrossRef] [Google Scholar]
  15. Nishimura, Y., Shimojima, M., Tano, Y., Miyamura, T., Wakita, T. & Shimizu, H.(2009). Human P-selectin glycoprotein ligand-1 is a functional receptor for enterovirus 71. Nat Med 15, 794–797.[CrossRef] [Google Scholar]
  16. Pipkin, P. A., Wood, D. J., Racaniello, V. R. & Minor, P. D.(1993). Characterisation of L cells expressing the human poliovirus receptor for the specific detection of polioviruses in vitro. J Virol Methods 41, 333–340.[CrossRef] [Google Scholar]
  17. Sako, D., Chang, X. J., Barone, K. M., Vachino, G., White, H. M., Shaw, G., Veldman, G. M., Bean, K. M., Ahern, T. J. & other authors(1993). Expression cloning of a functional glycoprotein ligand for P-selectin. Cell 75, 1179–1186.[CrossRef] [Google Scholar]
  18. Shafren, D. R., Dorahy, D. J., Greive, S. J., Burns, G. F. & Barry, R. D.(1997). Mouse cells expressing human intercellular adhesion molecule-1 are susceptible to infection by coxsackievirus A21. J Virol 71, 785–789. [Google Scholar]
  19. Shimizu, H., Utama, A., Yoshii, K., Yoshida, H., Yoneyama, T., Sinniah, M., Yusof, M. A. B., Okuno, Y., Okabe, N. & other authors(1999). Enterovirus 71 from fatal and nonfatal cases of hand, foot and mouth disease epidemics in Malaysia, Japan and Taiwan in 1997–1998. Jpn J Infect Dis 52, 12–15. [Google Scholar]
  20. Shimizu, H., Utama, A., Onnimala, N., Li, C., Li-Bi, Z., Yu-Jie, M., Pongsuwanna, Y. & Miyamura, T.(2004). Molecular epidemiology of enterovirus 71 infection in the Western Pacific Region. Pediatr Int 46, 231–235.[CrossRef] [Google Scholar]
  21. Thomas, G. M., Panicot-Dubois, L., Lacroix, R., Dignat-George, F., Lombardo, D. & Dubois, C.(2009). Cancer cell-derived microparticles bearing P-selectin glycoprotein ligand 1 accelerate thrombus formation in vivo. J Exp Med 206, 1913–1927.[CrossRef] [Google Scholar]
  22. Wang, Y. F., Chou, C. T., Lei, H. Y., Liu, C. C., Wang, S. M., Yan, J. J., Su, I. J., Wang, J. R., Yeh, T. M. & other authors(2004). A mouse-adapted enterovirus 71 strain causes neurological disease in mice after oral infection. J Virol 78, 7916–7924.[CrossRef] [Google Scholar]
  23. Yamayoshi, S., Yamashita, Y., Li, J., Hanagata, N., Minowa, T., Takemura, T. & Koike, S.(2009). Scavenger receptor B2 is a cellular receptor for enterovirus 71. Nat Med 15, 798–801.[CrossRef] [Google Scholar]
  24. Yang, F., Ren, L., Xiong, Z., Li, J., Xiao, Y., Zhao, R., He, Y., Bu, G., Zhou, S. & other authors(2009). Enterovirus 71 outbreak in the People's Republic of China in 2008. J Clin Microbiol 47, 2351–2352.[CrossRef] [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.022418-0
Loading
Adaptive mutations in the genomes of enterovirus 71 strains following infection of mouse cells expressing human P-selectin glycoprotein ligand-1
J. Gen. Virol. 92, 287 (2011); https://doi.org/10.1099/vir.0.022418-0
/content/journal/jgv/10.1099/vir.0.022418-0
/content/journal/jgv/10.1099/vir.0.022418-0
Loading

Data & Media loading...

Supplements

vol. , part 2, pp. 287 - 291

Preparation of original EV71 and EV71-LPS

EV71-1095 replication kinetics in RD, Jurkat and human peripheral blood mononuclear cells (PBMC)

Replication of L-PSGL-1-adapted variants in Jurkat cells incubated with the anti-PSGL-1 mAb [Single PDF file](310 KB)

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error