1887

Journal of General Virology header logo

Volume 101, Issue 3

Identification of amino acid residues involved in the interaction between virus haemagglutinin protein and cellular receptors Open Access

Abstract

virus (PPRV) haemagglutinin (H) protein mediates binding to cellular receptors and then initiates virus entry. To identify the key residues of PPRV H (Hv) protein of the Nigeria 75/1 strain involved in binding to receptors, interaction of the Hv and mutated Hv (mHv) proteins with receptors (SLAM and Nectin 4) and their mutants (mSLAM1, mSLAM2, mSLAM3 and mNectin 4) was investigated using surface plasmon resonance imaging (SPRi) and coimmunoprecipitation (co-IP) assays. The results showed that the Hv protein failed to interact with mSLAM3, but interacted at a strong or medium intensity with SLAM, mSLAM2, Nectin 4 and mNectin 4, and at a low level with mSLAM1. The mHv protein was unable to interact with SLAM and its mutants, but bound to Nectin 4 and mNectin 4 with medium and weak intensity, respectively. Further analysis showed that the Hv protein could precipitate mSLAM1, mSLAM2 and mNectin 4, but not mSLAM3. The mHv protein failed to coprecipitate with SLAM and its mutants. The binding activities of mNectin 4 and Nectin 4 to mHv were less than 30.36 and 51.94 % of the wild-type levels, respectively. Based on the results obtained, amino acids at positions R389, L464, I498, R503, R533, Y541, Y543, F552 and Y553 of H protein and I61, H62, L64, K76, K78, E123, H130, I210, A211, S226 and R227 in SLAM were identified to be essential for the specificity of H–SLAM interaction, while the critical residues of H–Nectin 4 interaction require further study. These findings would improve our understanding of the invasive mechanisms of PPRV.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): co-immunoprecipitation assay , haemagglutinin (H) , peste-des-petits-ruminantsvirus , receptor and surface plasmon resonance imaging
Funding
This study was supported by the:
  • the National Natural Science & Foundation of China (NSFC) (Award 31300142)
    • Principle Award Recipient: xuelian meng
  • National Basic Research Program of China (973 Program) (Award 2016YFD0500108)
    • Principle Award Recipient: Zhidong Zhang
© 2020 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial License.
Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001368
2019-12-20
2024-05-10
Loading full text...

Full text loading...

/deliver/fulltext/jgv/101/3/242.html?itemId=/content/journal/jgv/10.1099/jgv.0.001368&mimeType=html&fmt=ahah

References

  1. Baron MD, Diallo A, Lancelot R, Libeau G. Peste des petits ruminants virus. Adv Virus Res 2016; 95:1–42
     [Google Scholar]
  2. Albina E, Kwiatek O, Minet C, Lancelot R, Servan de Almeida R et al. Peste des petits ruminants, the next eradicated animal disease?. Vet Microbiol 2013; 165:38–44 [View Article]
     [Google Scholar]
  3. Banyard AC, Parida S, Batten C, Oura C, Kwiatek O et al. Global distribution of peste des petits ruminants virus and prospects for improved diagnosis and control. J Gen Virol 2010; 91:2885–2897 [View Article]
     [Google Scholar]
  4. Kwiatek O et al. Asian lineage of peste des petits ruminants virus, Africa. Emerg Infect Dis 2011; 17:1223–1231 [View Article]
     [Google Scholar]
  5. Muniraju M, Mahapatra M, Ayelet G, Babu A, Olivier G et al. Emergence of lineage IV peste des petits ruminants virus in Ethiopia: complete genome sequence of an Ethiopian isolate 2010. Transbound Emerg Dis 2016; 63:435–442 [View Article]
     [Google Scholar]
  6. OIE-WAHIS Peste des petits ruminants. retrieved from: annual animal health report, world animal health information database (WAHIS interface) – version 1, world organisation for animal health (OIE), Bulgaria; 2018
  7. Baron MD, Diop B, Njeumi F, Willett BJ, Bailey D. Future research to underpin successful peste des petits ruminants virus (PPRV) eradication. J Gen Virol 2017; 98:2635–2644 [View Article]
     [Google Scholar]
  8. Thomson GR, Fosgate GT, Penrith M-L. Eradication of transboundary animal diseases: can the rinderpest success story be repeated?. Transbound Emerg Dis 2017; 64:459–475 [View Article]
     [Google Scholar]
  9. Altan E, Parida S, Mahapatra M, Turan N, Yilmaz H. Molecular characterization of peste des petits ruminants viruses in the Marmara region of turkey. Transbound Emerg Dis 2019; 66:865–872 [View Article]
     [Google Scholar]
  10. Colf LA, Juo ZS, Garcia KC. Structure of the measles virus hemagglutinin. Nat Struct Mol Biol 2007; 14:1227–1228 [View Article]
     [Google Scholar]
  11. Hashiguchi T, Ose T, Kubota M, Maita N, Kamishikiryo J et al. Structure of the measles virus hemagglutinin bound to its cellular receptor SLAM. Nat Struct Mol Biol 2011; 18:135–141 [View Article]
     [Google Scholar]
  12. Liang Z, Yuan R, Chen L, Zhu X, Dou Y. Molecular evolution and characterization of hemagglutinin (H) in peste des petits ruminants virus. PLoS One 2016; 11:e0152587 [View Article]
     [Google Scholar]
  13. Navaratnarajah CK, Kumar S, Generous A, Apte-Sengupta S, Mateo M et al. The measles virus hemagglutinin stalk: structures and functions of the central fusion activation and membrane-proximal segments. J Virol 2014; 88:6158–6167 [View Article]
     [Google Scholar]
  14. Hu C, Zhang P, Liu X, Qi Y, Zou T et al. Characterization of a region involved in binding of measles virus H protein and its receptor SLAM (CD150). Biochem Biophys Res Commun 2004; 316:698–704 [View Article]
     [Google Scholar]
  15. Xu Q, Zhang P, Hu C, Liu X, Qi Y et al. Identification of amino acid residues involved in the interaction between measles virus Haemagglutin (MVH) and its human cell receptor (signaling lymphocyte activation molecule, SLAM). J Biochem Mol Biol 2006; 39:406–411 [View Article]
     [Google Scholar]
  16. Xu F, Tanaka S, Watanabe H, Shimane Y, Iwasawa M et al. Computational analysis of the interaction energies between amino acid residues of the measles virus hemagglutinin and its receptors. Viruses 2018; 10:236 [View Article]
     [Google Scholar]
  17. Birch J, Juleff N, Heaton MP, Kalbfleisch T, Kijas J et al. Characterization of ovine Nectin-4, a novel peste des petits ruminants virus receptor. J Virol 2013; 87:4756–4761 [View Article]
     [Google Scholar]
  18. Pawar RM, Raj GD, Kumar TM, Raja A, Balachandran C. Effect of siRNA mediated suppression of signaling lymphocyte activation molecule on replication of peste des petits ruminants virus in vitro. Virus Res 2008; 136:118–123 [View Article]
     [Google Scholar]
  19. Mühlebach MD, Mateo M, Sinn PL, Prüfer S, Uhlig KM et al. Adherens junction protein Nectin-4 is the epithelial receptor for measles virus. Nature 2011; 480:530–533 [View Article]
     [Google Scholar]
  20. Seki F, Ono N, Yamaguchi R, Yanagi Y. Efficient isolation of wild strains of canine distemper virus in Vero cells expressing canine SLAM (CD150) and their adaptability to marmoset B95a cells. J Virol 2003; 77:9943–9950 [View Article]
     [Google Scholar]
  21. Pratakpiriya W, Seki F, Otsuki N, Sakai K, Fukuhara H et al. Nectin4 is an epithelial cell receptor for canine distemper virus and involved in neurovirulence. J Virol 2012; 86:10207–10210 [View Article]
     [Google Scholar]
  22. Tatsuo H, Yanagi Y. The morbillivirus receptor SLAM (CD150). Microbiol Immunol 2002; 46:135–142 [View Article]
     [Google Scholar]
  23. Cocks BG, Chang C-CJ, Carballido JM, Yssel H, de Vries JE et al. A novel receptor involved in T-cell activation. Nature 1995; 376:260–263 [View Article]
     [Google Scholar]
  24. Bleharski JR, Niazi KR, Sieling PA, Cheng G, Modlin RL. Signaling lymphocytic activation molecule is expressed on CD40 ligand-activated dendritic cells and directly augments production of inflammatory cytokines. J Immunol 2001; 167:3174–3181 [View Article]
     [Google Scholar]
  25. Ohgimoto S, Ohgimoto K, Niewiesk S, Klagge IM, Pfeuffer J et al. The haemagglutinin protein is an important determinant of measles virus tropism for dendritic cells in vitro . J Gen Virol 2001; 82:1835–1844 [View Article]
     [Google Scholar]
  26. Wang N, Satoskar A, Faubion W, Howie D, Okamoto S et al. The cell surface receptor SLAM controls T cell and macrophage functions. J Exp Med 2004; 199:1255–1264 [View Article]
     [Google Scholar]
  27. Ono N, Tatsuo H, Tanaka K, Minagawa H, Yanagi Y. V domain of human SLAM (CDw150) is essential for its function as a measles virus receptor. J Virol 2001; 75:1594–1600 [View Article]
     [Google Scholar]
  28. Ohishi K, Ando A, Suzuki R, Takishita K, Kawato M et al. Host–virus specificity of morbilliviruses predicted by structural modeling of the marine mammal SLAM, a receptor. Comp Immunol Microbiol Infect Dis 2010; 33:227–241 [View Article]
     [Google Scholar]
  29. Ohno S, Seki F, Ono N, Yanagi Y. Histidine at position 61 and its adjacent amino acid residues are critical for the ability of SLAM (CD150) to act as a cellular receptor for measles virus. J Gen Virol 2003; 84:2381–2388 [View Article]
     [Google Scholar]
  30. Yanagi Y, Takeda M, Ohno S, Hashiguchi T. Measles virus receptors. Curr Top Microbiol Immunol 2009; 329:13–30
     [Google Scholar]
  31. Sarkar J, Balamurugan V, Sen A, Saravanan P, Sahay B et al. Sequence analysis of morbillivirus CD150 receptor-signaling lymphocyte activation molecule (SLAM) of different animal species. Virus Genes 2009; 39:335–341 [View Article]
     [Google Scholar]
  32. Kurita S, Ogita H, Takai Y. Cooperative role of nectin-nectin and nectin-afadin interactions in formation of nectin-based cell-cell adhesion. J. Biol. Chem. 2011; 286:36297–36303 [View Article]
     [Google Scholar]
  33. Takai Y, Miyoshi J, Ikeda W, Ogita H. Nectins and nectin-like molecules: roles in contact inhibition of cell movement and proliferation. Nat Rev Mol Cell Biol 2008; 9:603–615 [View Article]
     [Google Scholar]
  34. Ogita H, Takai Y. Nectins and nectin-like molecules: roles in cell adhesion, polarization, movement, and proliferation. IUBMB Life 2006; 58:334–343 [View Article]
     [Google Scholar]
  35. Takai Y, Nakanishi H. Nectin and afadin: novel organizers of intercellular junctions. J Cell Sci 2003; 116:17–27 [View Article]
     [Google Scholar]
  36. Delpeut S, Noyce RS, Richardson CD. The V domain of dog PVRL4 (Nectin-4) mediates canine distemper virus entry and virus cell-to-cell spread. Virology 2014; 454-455:109–117 [View Article]
     [Google Scholar]
  37. Meng X, Deng R, Zhu X, Zhang Z. Quantitative investigation of the direct interaction between hemagglutinin and fusion proteins of peste des petits ruminant virus using surface plasmon resonance. Virol J 2018; 15:21 [View Article]
     [Google Scholar]
  38. Crennell S, Takimoto T, Portner A, Taylor G. Crystal structure of the multifunctional paramyxovirus hemagglutinin-neuraminidase. Nat Struct Biol 2000; 7:1068–1074
     [Google Scholar]
  39. Hashiguchi T, Kajikawa M, Maita N, Takeda M, Kuroki K et al. Crystal structure of measles virus hemagglutinin provides insight into effective vaccines. Proc Natl Acad Sci U S A 2007; 104:19535–19540 [View Article]
     [Google Scholar]
  40. Zhang X, Lu G, Qi J, Li Y, He Y et al. Structure of measles virus hemagglutinin bound to its epithelial receptor Nectin-4. Nat Struct Mol Biol 2013; 20:67–72 [View Article]
     [Google Scholar]
  41. Tahara M, Takeda M, Shirogane Y, Hashiguchi T, Ohno S et al. Measles virus infects both polarized epithelial and immune cells by using distinctive receptor-binding sites on its hemagglutinin. J Virol 2008; 82:4630–4637 [View Article]
     [Google Scholar]
  42. Ohishi K, Suzuki R, Maruyama T. Host-virus specificity of the morbillivirus receptor, SLAM, in marine mammals: risk assessment of infection based on three-dimensional models. In Romero A, Keith EO. (editors) New Approaches to the Study of Marine Mammals Rijeka, Croatia: InTech; 2014 pp 123–204
     [Google Scholar]
  43. Khosravi M, Bringolf F, Röthlisberger S, Bieringer M, Schneider-Schaulies J et al. Canine distemper virus fusion activation: critical role of residue E123 of CD150/SLAM. J Virol 2016; 90:1622–1637 [View Article]
     [Google Scholar]
  44. Masse N, Ainouze M, Neel B, Wild TF, Buckland R et al. Measles virus (mV) hemagglutinin: evidence that attachment sites for mV receptors SLAM and CD46 overlap on the globular head. J Virol 2004; 78:9051–9063 [View Article]
     [Google Scholar]
  45. Vongpunsawad S, Oezgun N, Braun W, Cattaneo R. Selectively receptor-blind measles viruses: identification of residues necessary for SLAM- or CD46-induced fusion and their localization on a new hemagglutinin structural model. J Virol 2004; 78:302–313 [View Article]
     [Google Scholar]
  46. Leonard VH, Sinn PL, Hodge G, Miest T, Devaux P et al. Measles virus blind to its epithelial cell receptor remains virulent in rhesus monkeys but cannot cross the airway epithelium and is not shed. J Clin Invest 2008; 118:2448–2458
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001368
Loading
Identification of amino acid residues involved in the interaction between peste-des-petits-ruminants virus haemagglutinin protein and cellular receptors
J. Gen. Virol. 101, 242 (2020); https://doi.org/10.1099/jgv.0.001368
/content/journal/jgv/10.1099/jgv.0.001368
/content/journal/jgv/10.1099/jgv.0.001368
Loading

Data & Media loading...

Supplements

Supplementary material 1

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