Filopodia and Viruses: An Analysis of Membrane Processes in Entry Mechanisms

Overview

Journal Front Microbiol

Specialty Microbiology

Date 2016 Mar 26

PMID 27014223

Citations 40

Authors

Kenneth Chang

John Baginski

Samer F Hassan

Michael Volin

Deepak Shukla

Vaibhav Tiwari

Affiliations

Soon will be listed here.

Abstract

Filopodia are thin, actin rich bundles protruding from cell plasma membranes, serving physiological purposes, such as probing the environment and facilitating cell-to-cell adhesion. Recent studies have highlighted that actively polymerized filopodial-protrusions are exploited during virus entry, trafficking, spread, and the development of clinical pathology of viral diseases. These observations have caused a surge in investigation of the key determinants of filopodial induction and their influence on cell topography including receptor expression for viral entry. It is now very clear that filopodia can provide unique opportunities for many viruses to invade host cells vertically during primary infection, or horizontally during virus spread from cell-to-cell. These emerging concepts can explain the unprecedented ability of viruses to invade both nearby and long-distant host cells, a feature that may directly contribute to viral tropism. In this review, we summarize the significance of filopodia in viral diseases and discuss future therapeutic possibilities to precisely target filopodial-flyovers to prevent or control infectious diseases.

Citing Articles

The Rac1-PAK1-Arp2/3 signaling axis regulates CHIKV nsP1-induced filopodia and optimal viral genome replication.

Aiqui-Reboul-Paviet O, Bakhache W, Bernard E, Holsteyn L, Neyret A, Briant L J Virol. 2024; 98(10):e0061224.

PMID: 39297643 PMC: 11495065. DOI: 10.1128/jvi.00612-24.

Significance of Artificial Intelligence in the Study of Virus-Host Cell Interactions.

Elste J, Saini A, Mejia-Alvarez R, Mejia A, Millan-Pacheco C, Swanson-Mungerson M Biomolecules. 2024; 14(8).

PMID: 39199298 PMC: 11352483. DOI: 10.3390/biom14080911.

The cellular protrusions for inter-cellular material transfer: similarities between filopodia, cytonemes, tunneling nanotubes, viruses, and extracellular vesicles.

Hu H, Nishimura T, Kawana H, Dante R, DAngelo G, Suetsugu S Front Cell Dev Biol. 2024; 12:1422227.

PMID: 39035026 PMC: 11257967. DOI: 10.3389/fcell.2024.1422227.

Impact of actin polymerization and filopodia formation on herpes simplex virus entry in epithelial, neuronal, and T lymphocyte cells.

Sasivimolrattana T, Bhattarakosol P Front Cell Infect Microbiol. 2023; 13:1301859.

PMID: 38076455 PMC: 10704452. DOI: 10.3389/fcimb.2023.1301859.

Hs27 fibroblast response to contact guidance cues.

Kim C, Robitaille M, Christodoulides J, Ng Y, Raphael M, Kang W Sci Rep. 2023; 13(1):21691.

PMID: 38066191 PMC: 10709656. DOI: 10.1038/s41598-023-48913-9.

References

Taylor M, Koyuncu O, Enquist L . Subversion of the actin cytoskeleton during viral infection. Nat Rev Microbiol. 2011; 9(6):427-39. PMC: 3229036. DOI: 10.1038/nrmicro2574. View

Carpenter J, Hutchinson J, Jackson W, Grose C . Egress of light particles among filopodia on the surface of Varicella-Zoster virus-infected cells. J Virol. 2008; 82(6):2821-35. PMC: 2258984. DOI: 10.1128/JVI.01821-07. View

Hadigal S, Agelidis A, Karasneh G, Antoine T, Yakoub A, Ramani V . Heparanase is a host enzyme required for herpes simplex virus-1 release from cells. Nat Commun. 2015; 6:6985. PMC: 4413471. DOI: 10.1038/ncomms7985. View

Guillou H, Depraz-Depland A, Planus E, Vianay B, Chaussy J, Grichine A . Lamellipodia nucleation by filopodia depends on integrin occupancy and downstream Rac1 signaling. Exp Cell Res. 2007; 314(3):478-88. DOI: 10.1016/j.yexcr.2007.10.026. View

Quetglas J, Hernaez B, Galindo I, Munoz-Moreno R, Cuesta-Geijo M, Alonso C . Small rho GTPases and cholesterol biosynthetic pathway intermediates in African swine fever virus infection. J Virol. 2011; 86(3):1758-67. PMC: 3264358. DOI: 10.1128/JVI.05666-11. View

Hindmarsh P, Laimins L . Mechanisms regulating expression of the HPV 31 L1 and L2 capsid proteins and pseudovirion entry. Virol J. 2007; 4:19. PMC: 1808446. DOI: 10.1186/1743-422X-4-19. View

Leijnse N, Oddershede L, Bendix P . Helical buckling of actin inside filopodia generates traction. Proc Natl Acad Sci U S A. 2014; 112(1):136-41. PMC: 4291626. DOI: 10.1073/pnas.1411761112. View

Zhang X, Wang B, Li J . Implications of heparan sulfate and heparanase in neuroinflammation. Matrix Biol. 2014; 35:174-81. DOI: 10.1016/j.matbio.2013.12.009. View

Nikolic D, Lehmann M, Felts R, Garcia E, Blanchet F, Subramaniam S . HIV-1 activates Cdc42 and induces membrane extensions in immature dendritic cells to facilitate cell-to-cell virus propagation. Blood. 2011; 118(18):4841-52. PMC: 3208294. DOI: 10.1182/blood-2010-09-305417. View

10.

Schelhaas M, Ewers H, Rajamaki M, Day P, Schiller J, Helenius A . Human papillomavirus type 16 entry: retrograde cell surface transport along actin-rich protrusions. PLoS Pathog. 2008; 4(9):e1000148. PMC: 2518865. DOI: 10.1371/journal.ppat.1000148. View

11.

Chen Z, Shi Z, Baumgart T . Regulation of membrane-shape transitions induced by I-BAR domains. Biophys J. 2015; 109(2):298-307. PMC: 4621619. DOI: 10.1016/j.bpj.2015.06.010. View

12.

Bornschlogl T, Romero S, Vestergaard C, Joanny J, Tran van Nhieu G, Bassereau P . Filopodial retraction force is generated by cortical actin dynamics and controlled by reversible tethering at the tip. Proc Natl Acad Sci U S A. 2013; 110(47):18928-33. PMC: 3839779. DOI: 10.1073/pnas.1316572110. View

13.

Xu H, Hao X, Wang S, Wang Z, Cai M, Jiang J . Real-time Imaging of Rabies Virus Entry into Living Vero cells. Sci Rep. 2015; 5:11753. PMC: 4493577. DOI: 10.1038/srep11753. View

14.

Machesky L, Li A . Fascin: Invasive filopodia promoting metastasis. Commun Integr Biol. 2010; 3(3):263-70. PMC: 2918773. DOI: 10.4161/cib.3.3.11556. View

15.

Dent E, Gupton S, Gertler F . The growth cone cytoskeleton in axon outgrowth and guidance. Cold Spring Harb Perspect Biol. 2010; 3(3). PMC: 3039926. DOI: 10.1101/cshperspect.a001800. View

16.

Cossart P . Actin-based motility of pathogens: the Arp2/3 complex is a central player. Cell Microbiol. 2001; 2(3):195-205. DOI: 10.1046/j.1462-5822.2000.00053.x. View

17.

Salameh S, Sheth U, Shukla D . Early events in herpes simplex virus lifecycle with implications for an infection of lifetime. Open Virol J. 2012; 6:1-6. PMC: 3267084. DOI: 10.2174/1874357901206010001. View

18.

Shrivastava A, Prasad A, Kuzontkoski P, Yu J, Groopman J . Slit2N Inhibits Transmission of HIV-1 from Dendritic Cells to T-cells by Modulating Novel Cytoskeletal Elements. Sci Rep. 2015; 5:16833. PMC: 4652184. DOI: 10.1038/srep16833. View

19.

Tiwari V, Shukla D . Nonprofessional phagocytosis can facilitate herpesvirus entry into ocular cells. Clin Dev Immunol. 2012; 2012:651691. PMC: 3312246. DOI: 10.1155/2012/651691. View

20.

Oh M, Akhtar J, Desai P, Shukla D . A role for heparan sulfate in viral surfing. Biochem Biophys Res Commun. 2009; 391(1):176-81. PMC: 2812628. DOI: 10.1016/j.bbrc.2009.11.027. View