Filopodia and viruses: An analysis of membrane processes in entry mechanisms

Frontiers in Microbiology

Volumn 7, Issue MAR, 2016, Pages

  Chang, Kenneth ^a   Baginski, John ^a   Hassan, Samer F ^b   Volin, Michael ^a   Shukla, Deepak ^b   Tiwari, Vaibhav ^a  

^a MIDWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

Filopodia; Heparan sulfate; Virus entry; Virus cell interaction

Indexed keywords

ACTIN DEPOLYMERIZING FACTOR; BACTERIAL PROTEIN; BLEBBISTATIN; COFILIN; CYTOCHALASIN D; F ACTIN; FASCIN; NANOTUBE; NECTIN 1; P21 ACTIVATED KINASE 1; PROTEIN CDC42; PROTEIN KINASE P60; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; TUNNELING NANOTUBE; UNCLASSIFIED DRUG; WISKOTT ALDRICH SYNDROME PROTEIN;

ACTIN FILAMENT; AVIAN LEUKOSIS VIRUS; CELL ADHESION; CELL INVASION; CELL MIGRATION; CELL POLARITY; CELL SPREADING; DOWN REGULATION; ENDOCYTOSIS; FILOPODIUM; HERPES SIMPLEX; HERPES SIMPLEX VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS; LAMELLIPODIUM; MOUSE MAMMARY TUMOR VIRUS; MURINE LEUKEMIA VIRUS; NONHUMAN; PHAGOCYTOSIS; REVIEW; VACCINIA VIRUS; VESICULOVIRUS; VIRUS ATTACHMENT; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS RELEASE; X LINKED MENTAL RETARDATION;

EID: 84964318659     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.00300     Document Type: Review

References (58)

1. Akula, S. M., Naranatt, P. P., Walia, N.-S., Wang, F.-Z., Fegley, B., and Chandran, B. (2003). Kaposi's sarcoma-associated herpesvirus (Human herpesvirus 8) infection of human fibroblast cells occurs through endocytosis. J. Virol. 77, 7978-7990. doi: 10.1128/JVI.77.14.7978-7990.2003
2. Alberts, B., Bray, D., Lewis, J., Raff, M., ROberts, K., and Watson, J. (1994). Molecular Biology of the Cell, 3 Edn. New York, NY: Garland Publishing Inc
3. American Cancer Society (2015). Viruses that Can Lead to Cancer. Available at: http://www.cancer.org/cancer/cancercauses/othercarcinogens/infectiousagents/infectiousagentsandcancer/infectious-agents-and-cancer-viruses
4. Bienkowska-Haba, M., and Sapp, M. (2011). March 10. The cytoskeleton in papillomavirus infection. Viruses 3, 260-271. doi: 10.3390/v3030260
5. Bornschlogl, T. (2013). How filopodia pull: what we know about the mechanics and dynamics of filopodia. Cytoskeleton 70, 590-603. doi: 10.1002/cm.21130
6. Bornsclogl, T., Romero, S., Vestergaard, C. L., Joanny, J.-F., Nhieu, G. T., and Bassereau, P. (2013). Filopodial retraction force is generated by cortical actin dynamics and controlled by reversible tethering at the tip. Proc. Natl. Acad. Sci. U.S.A. 110, 18928-18933. doi: 10.1073/pnas.1316572110
7. Butt, A. Q., and Miggin, S. M. (2012). Cancer and viruses: a double-edged sword. Proteomics 12, 2127-2138. doi: 10.1002/pmic.201100526
8. Carpenter, J. E., Hutchinson, J. A., Jackson, W., and Grose, C. (2008). Egress of light particles among filopodia on the surface of Varicella-Zoster virus-infected cells. J. Virol. 82, 2821-2835. doi: 10.1128/JVI.01821-07
9. Chang, Y., Cesarman, E., Pessin, M., Lee, F., Culpepper, J., Knowles, D., et al. (1994). Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma. Science 266, 1865-1869. doi: 10.1126/science.7997879
10. Chen, Z., Shi, Z., and Baumgart, T. (2015). Regulation of membrane-shape transitions induced by I-BAR domains. Biophys. J. 109, 298-307. doi: 10.1016/j.bpj.2015.06.010
11. Choudhary, S., Burnham, L., Thompson, J. M., Shukla, D., and Tiwari, V. (2013). Role of filopodia in HSV-1 entry into zebrafish 3-O-sulfotransferase-3-expressing cells. Open. Virol. J. 7, 41-48. doi: 10.2174/1874357901307010041
12. Clement, C., Tiwari, V., Scanlan, P. M., Valyi-Nagy, T., Yue, B. Y., and Shukla, D. (2006). A novel role for phagocytosis-like uptake in herpes simplex virus entry. J. Cell. Biol. 174, 1009-1021. doi: 10.1083/jcb.200509155
13. Cooper, G. M. (2000). "The cell: a molecular approach, "in Structure and Organization of Actin Filaments, 2nd Edn, ed. G. M. Cooper (Sunderland, MA: Sinauer Associates). Available at: http://www.ncbi.nlm.nih.gov/books/NBK9908
14. Cossart, P. (2000). Actin-based motility of pathogens: the Arp2/3 complex is a central player. Cell. Microbiol. 2, 195-205. doi: 10.1046/j.1462-5822.2000.00053.x
15. Dent, E. W., Gupton, S. L., and Gertler, F. B. (2011). The growth cone cytoskeleton in axon outgrowth and guidance. Cold Spring Harb. Perspect. Biol. 3:a001800. doi: 10.1101/cshperspect.a001800
16. Dixit, R., Tiwari, V., and Shukla, D. (2008). Herpes simplex virus type 1 induces filopodia in differentiated P19 neural cells to facilitate viral spread. Neurosci. Lett. 440, 113-118. doi: 10.1016/j.neulet.2008.05.031
17. Do, T., Murphy, G., Earl, L. A., Del Prete, G. Q., Grandinetti, G., Li, G.-H., et al. (2014). Three-dimensional imaging of HIV-1 virological synapses reveals membrane architectures involved in virus transmission. J. Virol. 88, 10327-10339. doi: 10.1128/JVI.00788-14
18. Greber, U. (2002). Signalling in viral entry. Cell. Mol. Life Sci. 59, 608-626. doi: 10.1007/s00018-002-8453-3
19. Guillou, H., Depraz-Depland, A., Planus, E., Vianaya, B., Chaussy, J., Grichine, A., et al. (2008). Lamellipodia nucleation by filopodia depends on integrin occupancy and downstream Rac1 signaling. Exp. Cell Res. 314, 478-488. doi: 10.1016/j.yexcr.2007.10.026
20. Hadigal, S. R., Agelidis, A. M., Karasneh, G. A., Antoine, T. E., Yakoub, A. M., and Ramani, V. C. (2015). Heparanase is a host enzyme required for herpes simplex virus-1 release from cells. Nat. Commun. 6:6985. doi: 10.1038/ncomms7985
21. Hashimoto, M., Bhuyan, F., Hiyoshi, M., Noyori, O., Nasser, H., Miyazaki, M., et al. (2016). Potential role of the formation of tunneling nanotubes in HIV-1 spread in macrophages. J. Immunol. 196, 1832-1841. doi: 10.4049/jimmunol.1500845
22. Hindmarsh, P. L., and Laimins, L. A. (2007). Mechanisms regulating expression of the HPV 31 L1 and L2 capsid proteins and pseudovirion entry. J. Virol. 4:19. doi: 10.1186/1743-422X-4-19
23. Huang, C.-Y., Lu, T.-Y., Bair, C.-H., Chang, Y.-S., Jwo, J.-K., and Chang, W. (2008). A novel cellular protein, VPEF, facilitates vaccinia virus penetration into HeLa cells through fluid phase endocytosis. J. Virol. 82, 7988-7999. doi: 10.1128/JVI.00894-08
24. Jose, J., Tang, J., Taylor, A. B., Baker, T. S., and Kuhn, R. J. (2015). Fluorescent protein-tagged sindbis virus E2 glycoprotein allows single particle analysis of virus budding from live cells. Viruses 7, 6182-6199. doi: 10.3390/v7122926
25. Kolesnikova, L., Bohil, A., Cheney, R., and Becker, S. (2007). Budding of Marburgvirus is associated with filopodia. Cell. Microbiol. 9, 939-951. doi: 10.1111/j.1462-5822.2006.00842.x
26. Komano, J., Miyauchi, K., Matsuda, Z., and Yamamoto, N. (2004). Inhibiting the Arp2/3 complex limits infection of both intracellular mature vaccinia virus and primate lentiviruses. Mol. Biol. Cell. 15, 5197-5207. doi: 10.1091/mbc. E04-04-0279
27. LeBrasseur, N. (2007). Viruses infect filopodia. J. Cell. Biol. 176:733. doi: 10.1083/jcb.1766rr1
28. Lehmann, M. J., Sherer, N. M., Marks, C. B., Pypaert, M., and Mothes, W. (2005). Actin-and myosin-driven movement of viruses along filopodia precedes their entry into cells. J. Cell. Biol. 170, 317-325. doi: 10.1083/jcb.200503059
29. Leijnse, N., Oddershede, L. B., and Bendix, P. M. (2015a). An updated look at actin dynamics in filopodia. Cytoskeleton 72, 71-79. doi: 10.1002/cm.21216
30. Leijnse, N., Oddershede, L. B., and Bendix, P. M. (2015b). Helical buckling of actin inside filopodia generates traction. Proc. Natl. Acad. Sci. U.S.A. 112, 136-141. doi: 10.1073/pnas.1411761112
31. Machesky, L. M., and Li, A. (2010). Fascin: invasive filopodia promoting metastasis. Commun. Integr. Biol. 3, 263-270. doi: 10.4161/cib.3.3.11556
32. Mattila, P. K., and Lappalainen, P. (2008). Filopodia: molecular architecture and cellular functions. Nat. Rev. Mol. Cell. Biol. 9, 446-454. doi: 10.1038/nrm2406
33. Melnick, M., Sedghizadeh, P. P., Allen, C. M., and Jaskoll, T. (2012). Human cytomegalovirus and mucoepidermoid carcinoma of salivary glands: cell-specific localization of active viral and oncogenic signaling proteins is confirmatory of a causal relationship. Exp. Mol. Pathol. 92, 118-125. doi: 10.1016/j.yexmp.2011.10.011
34. Mercer, J., Knebel, S., Schmidt, F. L., and Helenius, A. (2010a). Vaccinia virus strains use distinct forms of macropinocytosis for host-cell entry. Proc. Natl. Acad. Sci. U.S.A. 107, 9346-9351. doi: 10.1073/pnas.1004618107atl
35. Mercer, J., Schelhaas, M., and Helenius, A. (2010b). Virus entry by endocytosis. Annu. Rev. Biochem. 79, 803-833. doi: 10.1146/annurev-biochem-060208-104626
36. Mothes, W., Sherer, N. M., Jin, J., and Zhong, P. (2010). Virus Cell-to-cell transmission. J. Virol. 84, 8360-8368. doi: 10.1128/JVI.00443-10
37. Nikolic, D., Lehmann, M., Felts, R., Garcia, E., Blanchet, F., Subramaniam, S., et al. (2011). HIV-1 activates Cdc42 and induces membrane extensions in immature dendritic cells to facilitate cell-to-cell virus propagation. Blood 118, 4841-4852. doi: 10.1182/blood-2010-09-305417
38. Oh, M., Akhtar, J., Desai, P., and Shukla, D. (2010). A role for heparan sulfate in viral surfing. Biochem. Biophs. Res. Commun. 391, 176-181. doi: 10.1016/j.bbrc.2009.11.027
39. Quetglas, J. I., Hernáez, B., Galindo, I., Muñoz-Moreno, R., Cuesta-Geijo, M. A., and Alonso, C. (2012). Small Rho GTPases and cholesterol biosynthetic pathway intermediates in african swine fever virus infection. J. Virol. 86, 1758-1767. doi: 10.1128/JVI.05666-11
40. Salameh, S., Sheth, U., and Shukla, D. (2012). Early events in herpes simplex virus lifecycle with implications for an infection of lifetime. Open. Virol. J. 6, 1-6. doi: 10.2174/1874357901206010001
41. Schelhaas, M. (2010). Come in and take your coat off-how host cells provide endocytosis for virus entry. Cell Microbiol. 12, 1375-1388. doi: 10.1111/j.1462-5822.2010.01510.x
42. Schelhaas, M., Ewers, H., Rajamäki, M.-L., Day, P. M., Schiller, J. T., and Helenius, A. (2008). Human papillomavirus type 16 entry: retrograde cell surface transport along actin-rich protrusions. PLoS Pathog. 4:148. doi: 10.1371/journal.ppat.1000148
43. Schudt, G., Kolesnikova, L., Dolnik, O., Sodeik, B., and Becker, S. (2013). Live-cell imaging of Marburg virus-infected cells uncovers actin-dependent transport of nucleocapsids over long distances. Proc. Natl. Acad. Sci. U.S.A. 110, 14402-14407. doi: 10.1073/pnas.1307681110
44. Sherer, N. M., Lehmann, M. J., and Jimenez-Soto, L. F. (2007). Retroviruses can establish filopodial bridges for efficient cell-to-cell transmission. Nat. Cell. Biol. 9, 310-315. doi: 10.1038/ncb1544
45. Shrivastava, A., Prasad, A., Kuzontkoski, P. M., Yu, J., and Groopman, J. E. (2015). Slit2N inhibits transmission of HIV-1 from dendritic cells to T-cells by modulating novel cytoskeletal elements. Sci. Rep. 19:16833. doi: 10.1038/srep16833
46. Simon Davis, D. A., and Parish, C. R. (2013). Heparan Sulfate: a ubiquitous glycosaminoglycan with multiple roles in immunity. Front. Immunol. 4:470. doi: 10.3389/fimmu.2013.00470
47. Smith, J. L., Lidke, D. S., and Ozbun, M. A. (2008). Virus activated filopodia promote human papillomavirus type 31 uptake from the extracellular matrix. Virology 381, 16-21. doi: 10.1016/j.virol.2008.08.040
48. Takada, Y., Isono, K., Shinga, J., Turner, J. M., Kitamura, H., Ohara, O., et al. (2007). Mammalian polycomb Scmh1 mediates exclusion of polycomb complexes from the XY body in the pachytene spermatocytes. Development 134, 579-590. doi: 10.1242/dev.02747
49. Taylor, M. P., Koyuncu, O. O., and Enquist, L. W. (2011). Subversion of the actin cytoskeleton during viral infection. Nat. Rev. Microbiol. 9, 427-439. doi: 10.1038/nrmicro2574
50. Tiwari, V., Maus, E., Sigar, I. M., Ramsey, K. H., and Shukla, D. (2012). Role of heparan sulfate in sexually transmitted infections. Glycobiology 22, 1402-1412. doi: 10.1093/glycob/cws106
51. Tiwari, V., and Shukla, D. (2012). Nonprofessional phagocytosis can facilitate herpesvirus entry into ocular cells. Clin. Dev. Immunol. 8, 651-691. doi: 10.1155/2012/651691
52. Tiwari, V., Tarbutton, M. S., and Shukla, D. (2015). Diversity of heparan sulfate and hsv entry: basic understanding and treatment strategies. Molecules 20, 2707-2727. doi: 10.3390/molecules20022707
53. Welch, M., and Mullins, R. (2002). Cellular control of actin nucleation. Annu. Rev. Cell Dev. Biol. 18, 247-288. doi: 10.1146/annurev.cellbio.18.040202.112133
54. Wheeler, D. L., Iida, M., and Dunn, E. F. (2009). The role of Src in solid tumors. Oncologist 14, 667-678. doi: 10.1634/theoncologist.2009-0009
55. Xiang, Y., Zheng, K., Ju, H., Wang, S., Pei, Y., Wang, Y., et al. (2012). Cofilin 1-mediated biphasic F-actin dynamics of neuronal cells affect herpes simplex virus 1 infection and replication. J. Virol. 86, 8440-8451. doi: 10.1128/JVI.00609-12
56. Xu, H., Hao, X., Wang, S., Wang, Z., Cai, M., Jiang, J., et al. (2015). Real-time imaging of rabies virus entry into living vero cells. Sci. Rep. 5:11753. doi: 10.1038/srep11753
57. Zhang, H., Berg, J. S., Li, Z., Wang, Y., Lång, P., Sousa, A. D., et al. (2004). Myosin-X provides a motor-based link between integrins and the cytoskeleton. Nat. Cell Biol. 6, 523-531. doi: 10.1038/ncb1136
58. Zhang, X., Wang, B., and Li, J. P. (2014). Implications of heparan sulfate and heparanase in neuroinflammation. Matrix Biol. 35, 174-181. doi: 10.1016/j.matbio.2013.12.009