Skip to main content
SpringerLink
Log in

Common and unique mechanisms of filamentous actin formation by viruses of the genus Orthorubulavirus

  • Original Article
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

We previously found that infection with human parainfluenza virus type 2 (hPIV-2), a member of the genus Orthorubulavirus, family Paramyxoviridae, causes filamentous actin (F-actin) formation to promote viral growth. In the present study, we investigated whether similar regulation of F-actin formation is observed in infections with other rubulaviruses, such as parainfluenza virus type 5 (PIV-5) and simian virus 41 (SV41). Infection with these viruses caused F-actin formation and RhoA activation, which promoted viral growth. These results indicate that RhoA-induced F-actin formation is important for efficient growth of these rubulaviruses. Only SV41 and hPIV-2 V and P proteins bound to Graf1, while the V and P proteins of PIV-5, mumps virus, and hPIV-4 did not bind to Graf1. In contrast, the V proteins of these rubulaviruses bound to both inactive RhoA and profilin 2. These results suggest that there are common and unique mechanisms involved in regulation of F-actin formation by members of the genus Orthorubulavirus.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Lamb RA, Parks GD (2013) Paramyxoviridae: the viruses and their replication. In: Knipe DM, Howley PM, Cohen JI, Griffin DE, Lamb RA, Martin MA, Racaniello VR, Roizman B (eds) Fields virology, vol 1, 6th edn. Lippincott Williams & Wilkins, Philadelphia, pp 975–995

    Google Scholar 

  2. Ohgimoto S, Bando H, Kawano M, Okamoto K, Kondo K, Tsurudome M, Nishio M, Ito Y (1990) Sequence analysis of P gene of human parainfluenza type 2 virus: P and cysteine-rich proteins are translated by two mRNAs that differ by two nontemplated G residues. Virology 177:116–123

    Article  CAS  Google Scholar 

  3. Ohta K, Matsumoto Y, Yumine N, Nishio M (2018) The V protein of human parainfluenza virus type 2 promotes RhoA-induced filamentous actin formation. Virology 524:90–96. https://doi.org/10.1016/j.virol.2018.08.015

    Article  CAS  PubMed  Google Scholar 

  4. Witke W (2004) The role of profilin complexes in cell motility and other cellular processes. Trends Cell Biol 14:461–469. https://doi.org/10.1016/j.tcb.2004.07.003

    Article  CAS  PubMed  Google Scholar 

  5. Goldschmidt-Clermont PJ, Furman MI, Wachsstock D, Safer D, Nachmias VT, Pollard TD (1992) The control of actin nucleotide exchange by thymosin beta 4 and profilin. A potential regulatory mechanism for actin polymerization in cells. Mol Biol Cell 3:1015–1024. https://doi.org/10.1091/mbc.3.9.1015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Watanabe N, Madaule P, Reid T, Ishizaki T, Watanabe G, Kakizuka A, Saito Y, Nakao K, Jockusch BM, Narumiya S (1997) p140mDia, a mammalian homolog of Drosophila diaphanous, is a target protein for Rho small GTPase and is a ligand for profilin. EMBO J 16:3044–3056. https://doi.org/10.1093/emboj/16.11.3044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Watanabe N, Kato T, Fujita A, Ishizaki T, Narumiya S (1999) Cooperation between mDia1 and ROCK in Rho-induced actin reorganization. Nat Cell Biol 1:136–143. https://doi.org/10.1038/11056

    Article  CAS  PubMed  Google Scholar 

  8. Bos JL, Rehmann H, Wittinghofer A (2007) GEFs and GAPs: critical elements in the control of small G proteins. Cell 129:865–877. https://doi.org/10.1016/j.cell.2007.05.018

    Article  CAS  PubMed  Google Scholar 

  9. Ohta K, Goto H, Matsumoto Y, Yumine N, Tsurudome M, Nishio M (2016) Graf1 controls the growth of human parainfluenza virus type 2 through inactivation of RhoA signaling. J Virol 90:9394–9405. https://doi.org/10.1128/JVI.01471-16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Ohta K, Matsumoto Y, Nishio M (2019) Profilin 2 is required for filamentous actin formation induced by human parainfluenza virus type 2. Virology 533:108–114. https://doi.org/10.1016/j.virol.2019.05.013

    Article  CAS  PubMed  Google Scholar 

  11. Nishio M, Tsurudome M, Ito M, Watanabe N, Kawano M, Komada H, Ito Y (1997) Human parainfluenza virus type 2 phosphoprotein: mapping of monoclonal antibody epitopes and location of the multimerization domain. J Gen Virol 78:1303–1308. https://doi.org/10.1099/0022-1317-78-6-1303

    Article  CAS  PubMed  Google Scholar 

  12. Tsurudome M, Nishio M, Komada H, Bando H, Ito Y (1989) Extensive antigenic diversity among human parainfluenza type 2 virus isolates and immunological relationships among paramyxoviruses revealed by monoclonal antibodies. Virology 171:38–48

    Article  CAS  Google Scholar 

  13. Szaszi K, Paulsen A, Szabo EZ, Numata M, Grinstein S, Orlowski J (2002) Clathrin-mediated endocytosis and recycling of the neuron-specific Na+/H+ exchanger NHE5 isoform. Regulation by phosphatidylinositol 3’-kinase and the actin cytoskeleton. J Biol Chem 277:42623–42632. https://doi.org/10.1074/jbc.M206629200

    Article  CAS  PubMed  Google Scholar 

  14. Shahriari S, Wei KJ, Ghildyal R (2018) Respiratory syncytial virus matrix (M) protein interacts with actin in vitro and in cell culture. Viruses 10:E535. https://doi.org/10.3390/v10100535.14

    Article  PubMed  Google Scholar 

  15. Hildebrand JD, Taylor JM, Parsons JT (1996) An SH3domain-containing GTPase-activating protein for Rho and Cdc42 associates with focal adhesion kinase. Mol Cell Biol 16:3169–3178

    Article  CAS  Google Scholar 

  16. Taylor JM, Macklem MM, Parsons JT (1999) Cytoskeletal changes induced by GRAF, the GTPase regulator associated with focal adhesion kinase, are mediated by Rho. J Cell Sci 112:231–242

    CAS  PubMed  Google Scholar 

  17. Shibata H, Oishi K, Yamagiwa A, Matsumoto M, Mukai H, Ono Y (2001) PKNβ interacts with the SH3 domains of Graf and a novel Graf related protein, Graf2, which are GTPase activating proteins for Rho family. J Biochem 130:23–31

    Article  CAS  Google Scholar 

  18. Doherty GJ, Åhlund MK, Howes MT, Morén B, Partonc RG, McMahon HT, Lundmark R (2011) The endocytic protein GRAF1 is directed to cell-matrix adhesion sites and regulates cell spreading. Mol Biol Cell 22:4380–4389. https://doi.org/10.1091/mbc.E10-12-0936

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Nishio M, Tsurudome M, Ito M, Garcin D, Kolakofsky D, Ito Y (2005) Identification of paramyxovirus V protein residues essential for STAT protein degradation and promotion of virus replication. J Virol 79:8591–8601. https://doi.org/10.1128/JVI.79.13.8591-8601.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Ohta K, Matsumoto Y, Ito M, Nishio M (2017) Tetherin antagonism by V proteins is a common trait among the genus Rubulavirus. Med Microbiol Immunol 206:319–326. https://doi.org/10.1007/s00430-017-0509-y

    Article  CAS  PubMed  Google Scholar 

  21. Kitagawa Y, Yamaguchi M, Zhou M, Nishio M, Itoh M, Gotoh B (2013) Human parainfluenza virus type 2 V protein inhibits TRAF6-mediated ubiquitination of IRF7 to prevent TLR7- and TLR9-dependent interferon induction. J Virol 87:7966–7976. https://doi.org/10.1128/JVI.03525-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Ogawa M, Mutsuga N, Tsurudome M, Kawano M, Matsumura H, Kusagawa S, Komada H, Nishio M, Ito Y (1992) Nucleotide sequence analysis of the simian virus 41 gene encoding the large (L) protein and construction of a phylogenetic tree for the L proteins of paramyxoviruses. J Gen Virol 73:2743–2750. https://doi.org/10.1099/0022-1317-73-10-2743

    Article  CAS  PubMed  Google Scholar 

  23. Kawano M, Tsurudome M, Oki N, Nishio M, Komada H, Matsumura H, Kusagawa S, Ohta H, Ito Y (1993) Sequence determination of the P gene of simian virus 41: presence of irregular deletions near the RNA-editing sites of paramyxoviruses. J Gen Virol 74:911–916. https://doi.org/10.1099/0022-1317-74-5-911

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We acknowledge proofreading and editing by Benjamin Phillis, and statistical support by Dr. Toshio Shimokawa at the Clinical Study Support Center, Wakayama Medical University.

Funding

This work was supported by a Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology, Japan (JP17K15703). This work was also supported by GSK Japan Research Grant 2018.

Author information

Authors and Affiliations

  1. Department of Microbiology, School of Medicine, Wakayama Medical University, 811-1, Kimiidera, Wakayama, 641-8509, Japan

    Keisuke Ohta, Yusuke Matsumoto & Machiko Nishio

Authors
  1. Keisuke Ohta
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yusuke Matsumoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Machiko Nishio
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Machiko Nishio.

Ethics declarations

Conflict of interest

The authors declare no conflicts of interest.

Additional information

Handling Editor: Bert K. Rima.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ohta, K., Matsumoto, Y. & Nishio, M. Common and unique mechanisms of filamentous actin formation by viruses of the genus Orthorubulavirus. Arch Virol 165, 799–807 (2020). https://doi.org/10.1007/s00705-020-04565-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-020-04565-y

Search

Navigation