Herpes simplex virus 1 enters human keratinocytes by a nectin-1-dependent, rapid plasma membrane fusion pathway that functions at low temperature

Journal of Virology

Volumn 90, Issue 22, 2016, Pages 10379-10389

  Sayers, Charlotte L ^a   Elliott, Gillian ^a,b  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF SURREY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN D; NECTIN 1; NECTIN 1 RECEPTOR; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; CELL ADHESION MOLECULE; NECTINS; VIRUS ENVELOPE PROTEIN; VIRUS RECEPTOR;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; CYTOPLASM VESICLE; ENDOCYTOSIS; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; IN VIVO STUDY; KERATINOCYTE; LOW TEMPERATURE; MEMBRANE FUSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; TRANSMISSION ELECTRON MICROSCOPY; VIRION; VIRUS CAPSID; VIRUS ENTRY; ANIMAL; CELL LINE; CHLOROCEBUS AETHIOPS; EPIDERMIS; HELA CELL LINE; METABOLISM; PHYSIOLOGY; TEMPERATURE; TUMOR CELL LINE; VERO CELL LINE; VIROLOGY;

ANIMALS; CELL ADHESION MOLECULES; CELL LINE; CELL LINE, TUMOR; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; ENDOCYTOSIS; EPIDERMIS; HELA CELLS; HERPESVIRUS 1, HUMAN; HUMANS; KERATINOCYTES; MEMBRANE FUSION; RECEPTORS, VIRUS; TEMPERATURE; VERO CELLS; VIRAL ENVELOPE PROTEINS; VIRION; VIRUS INTERNALIZATION;

EID: 84995511503     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01582-16     Document Type: Article

References (43)

1. Wittels M, Spear PG. 1991. Penetration of cells by herpes simplex virus does not require a low pH-dependent endocytic pathway. Virus Res 18: 271-290. http://dx.doi.org/10.1016/0168-1702(91)90024-P.
2. Spear PG. 1993. Entry of alphaherpesviruses into cells. Semin Virol 4:167-180. http://dx.doi.org/10.1006/smvy.1993.1012.
3. Nicola AV, Hou J, Major EO, Straus SE. 2005. Herpes simplex virus type 1 enters human epidermal keratinocytes, but not neurons, via a pHdependent endocytic pathway. J Virol 79:7609-7616. http://dx.doi.org/10.1128/JVI.79.12.7609-7616.2005.
4. Milne RS, Nicola AV, Whitbeck JC, Eisenberg RJ, Cohen GH. 2005. Glycoprotein D receptor-dependent, low-pH-independent endocytic entry of herpes simplex virus type 1. J Virol 79:6655-6663. http://dx.doi.org/10.1128/JVI.79.11.6655-6663.2005.
5. Nicola AV, McEvoy AM, Straus SE. 2003. Roles for endocytosis and low pH in herpes simplex virus entry into HeLa and Chinese hamster ovary cells. J Virol 77:5324-5332. http://dx.doi.org/10.1128/JVI.77.9.5324-5332.2003.
6. Nicola AV, Straus SE. 2004. Cellular and viral requirements for rapid endocytic entry of herpes simplex virus. J Virol 78:7508-7517. http://dx.doi.org/10.1128/JVI.78.14.7508-7517.2004.
7. Rahn E, Petermann P, Hsu MJ, Rixon FJ, Knebel-Morsdorf D. 2011. Entry pathways of herpes simplex virus type 1 into human keratinocytes are dynamin-and cholesterol-dependent. PLoS One 6:e25464. http://dx.doi.org/10.1371/journal.pone.0025464.
8. Devadas D, Koithan T, Diestel R, Prank U, Sodeik B, Dohner K. 2014. Herpes simplex virus internalization into epithelial cells requires Na+/H+ exchangers and p21-activated kinases but neither clathrin-nor caveolin-mediated endocytosis. J Virol 88:13378-13395. http://dx.doi.org/10.1128/JVI.03631-13.
9. Clement C, Tiwari V, Scanlan PM, Valyi-Nagy T, Yue BY, Shukla D. 2006. A novel role for phagocytosis-like uptake in herpes simplex virus entry. J Cell Biol 174:1009-1021. http://dx.doi.org/10.1083/jcb.200509155.
10. Geraghty RJ, Krummenacher C, Cohen GH, Eisenberg RJ, Spear PG. 1998. Entry of alphaherpesviruses mediated by poliovirus receptor-related protein 1 and poliovirus receptor. Science 280:1618-1620. http://dx.doi.org/10.1126/science.280.5369.1618.
11. Huber MT, Wisner TW, Hegde NR, Goldsmith KA, Rauch DA, Roller RJ, Krummenacher C, Eisenberg RJ, Cohen GH, Johnson DC. 2001. Herpes simplex virus with highly reduced gD levels can efficiently enter and spread between human keratinocytes. J Virol 75:10309-10318. http://dx.doi.org/10.1128/JVI.75.21.10309-10318.2001.
12. Petermann P, Thier K, Rahn E, Rixon FJ, Bloch W, Ozcelik S, Krummenacher C, Barron MJ, Dixon MJ, Scheu S, Pfeffer K, Knebel-Morsdorf D. 2015. Entry mechanisms of herpes simplex virus 1 into murine epidermis: involvement of nectin-1 and herpesvirus entry mediator as cellular receptors. J Virol 89:262-274. http://dx.doi.org/10.1128/JVI.02917-14.
13. Montgomery RI, Warner MS, Lum BJ, Spear PG. 1996. Herpes simplex virus-1 entry into cells mediated by a novel member of the TNF/NGF receptor family. Cell 87:427-436. http://dx.doi.org/10.1016/S0092-8674(00)81363-X.
14. Marsters SA, Ayres TM, Skubatch M, Gray CL, Rothe M, Ashkenazi A. 1997. Herpesvirus entry mediator, a member of the tumor necrosis factor receptor (TNFR) family, interacts with members of the TNFRassociated factor family and activates the transcription factors NFkappaB and AP-1. J Biol Chem 272:14029-14032. http://dx.doi.org/10.1074/jbc.272.22.14029.
15. Satoh T, Arii J, Suenaga T, Wang J, Kogure A, Uehori J, Arase N, Shiratori I, Tanaka S, Kawaguchi Y, Spear PG, Lanier LL, Arase H. 2008. PILRalpha is a herpes simplex virus-1 entry coreceptor that associates with glycoprotein B. Cell 132:935-944. http://dx.doi.org/10.1016/j.cell.2008.01.043.
16. Fournier N, Chalus L, Durand I, Garcia E, Pin JJ, Churakova T, Patel S, Zlot C, Gorman D, Zurawski S, Abrams J, Bates EE, Garrone P. 2000. FDF03, a novel inhibitory receptor of the immunoglobulin superfamily, is expressed by human dendritic and myeloid cells. J Immunol 165:1197-1209. http://dx.doi.org/10.4049/jimmunol.165.3.1197.
17. Dickson MA, Hahn WC, Ino Y, Ronfard V, Wu JY, Weinberg RA, Louis DN, Li FP, Rheinwald JG. 2000. Human keratinocytes that express hTERT and also bypass a p16(INK4a)-enforced mechanism that limits life span become immortal yet retain normal growth and differentiation characteristics. Mol Cell Biol 20:1436-1447. http://dx.doi.org/10.1128/MCB.20.4.1436-1447.2000.
18. Jones M, Dry IR, Frampton D, Singh M, Kanda RK, Yee MB, Kellam P, Hollinshead M, Kinchington PR, O'Toole EA, Breuer J. 2014. RNA-seq analysis of host and viral gene expression highlights interaction between varicella zoster virus and keratinocyte differentiation. PLoS Pathog 10: e1003896. http://dx.doi.org/10.1371/journal.ppat.1003896.
19. Patterson NA, Smith JL, Ozbun MA. 2005. Human papillomavirus type 31b infection of human keratinocytes does not require heparan sulfate. J Virol 79:6838-6847. http://dx.doi.org/10.1128/JVI.79.11.6838-6847.2005.
20. Lachmann RH, Sadarangani M, Atkinson HR, Efstathiou S. 1999. An analysis of herpes simplex virus gene expression during latency establishment and reactivation. J Gen Virol 80(Part 5):1271-1282. http://dx.doi.org/10.1099/0022-1317-80-5-1271.
21. Elliott G, Hafezi W, Whiteley A, Bernard E. 2005. Deletion of the herpes simplex virus VP22-encoding gene (UL49) alters the expression, localization, and virion incorporation of ICP0. J Virol 79:9735-9745. http://dx.doi.org/10.1128/JVI.79.15.9735-9745.2005.
22. Elliott G, O'Hare P. 1997. Intercellular trafficking and protein delivery by a herpesvirus structural protein. Cell 88:223-233. http://dx.doi.org/10.1016/S0092-8674(00)81843-7.
23. Highlander SL, Sutherland SL, Gage PJ, Johnson DC, Levine M, Glorioso JC. 1987. Neutralizing monoclonal antibodies specific for herpes simplex virus glycoprotein D inhibit virus penetration. J Virol 61:3356-3364.
24. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402-408. http://dx.doi.org/10.1006/meth.2001.1262.
25. Warner MS, Geraghty RJ, Martinez WM, Montgomery RI, Whitbeck JC, Xu R, Eisenberg RJ, Cohen GH, Spear PG. 1998. A cell surface protein with herpesvirus entry activity (HveB) confers susceptibility to infection by mutants of herpes simplex virus type 1, herpes simplex virus type 2, and pseudorabies virus. Virology 246:179-189. http://dx.doi.org/10.1006/viro.1998.9218.
26. McClain DS, Fuller AO. 1994. Cell-specific kinetics and efficiency of herpes simplex virus type 1 entry are determined by two distinct phases of attachment. Virology 198:690-702. http://dx.doi.org/10.1006/viro.1994.1081.
27. Huang AS, Wagner RR. 1964. Penetration of herpes simplex virus into human epidermoid cells. Proc Soc Exp Biol Med 116:863-869. http://dx.doi.org/10.3181/00379727-116-29392.
28. Desai PJ, Schaffer PA, Minson AC. 1988. Excretion of non-infectious virus particles lacking glycoprotein H by a temperature-sensitive mutant of herpes simplex virus type 1: evidence that gH is essential for virion infectivity. J Gen Virol 69(Part 6):1147-1156. http://dx.doi.org/10.1099/0022-1317-69-6-1147.
29. Larrick JW, Enns C, Raubitschek A, Weintraub H. 1985. Receptormediated endocytosis of human transferrin and its cell surface receptor. J Cell Physiol 124:283-287. http://dx.doi.org/10.1002/jcp.1041240217.
30. Lippincott-Schwartz J, Roberts TH, Hirschberg K. 2000. Secretory protein trafficking and organelle dynamics in living cells. Annu Rev Cell Dev Biol 16:557-589. http://dx.doi.org/10.1146/annurev.cellbio.16.1.557.
31. Pratten MK, Lloyd JB. 1979. Effects of temperature, metabolic inhibitors and some other factors on fluid-phase and adsorptive pinocytosis by rat peritoneal macrophages. Biochem J 180:567-571. http://dx.doi.org/10.1042/bj1800567.
32. Benedict FG. 1925. Skin Temperature and Heat Loss. Proc Natl Acad Sci U S A 11:549-552. http://dx.doi.org/10.1073/pnas.11.9.549.
33. Benedict FG, Miles WR, Johnson A. 1919. The temperature of the human skin. Proc Natl Acad Sci U S A 5:218-222. http://dx.doi.org/10.1073/pnas.5.6.218.
34. Wang G, Hernandez R, Weninger K, Brown DT. 2007. Infection of cells by Sindbis virus at low temperature. Virology 362:461-467. http://dx.doi.org/10.1016/j.virol.2006.12.036.
35. Vancini R, Wang G, Ferreira D, Hernandez R, Brown DT. 2013. Alphavirus genome delivery occurs directly at the plasma membrane in a time-and temperature-dependent process. J Virol 87:4352-4359. http://dx.doi.org/10.1128/JVI.03412-12.
36. Papadopoulos NG, Sanderson G, Hunter J, Johnston SL. 1999. Rhinoviruses replicate effectively at lower airway temperatures. J Med Virol 58:100-104. http://dx.doi.org/10.1002/(SICI)1096-9071(199905)58:1<100::AID-JMV16 3.0.CO;2-D.
37. Shah A, Farooq AV, Tiwari V, Kim MJ, Shukla D. 2010. HSV-1 infection of human corneal epithelial cells: receptor-mediated entry and trends of re-infection. Mol Vision 16:2476-2486.
38. Petermann P, Rahn E, Thier K, Hsu MJ, Rixon FJ, Kopp SJ, Knebel-Morsdorf D. 2015. Role of Nectin-1 and herpesvirus entry mediator as cellular receptors for herpes simplex virus 1 on primary murine dermal fibroblasts. J Virol 89:9407-9416. http://dx.doi.org/10.1128/JVI.01415-15.
39. Kopp SJ, Banisadr G, Glajch K, Maurer UE, Grunewald K, Miller RJ, Osten P, Spear PG. 2009. Infection of neurons and encephalitis after intracranial inoculation of herpes simplex virus requires the entry receptor nectin-1. Proc Natl Acad SciUSA106:17916-17920. http://dx.doi.org/10.1073/pnas.0908892106.
40. Tiwari V, Oh MJ, Kovacs M, Shukla SY, Valyi-Nagy T, Shukla D. 2008. Role for nectin-1 in herpes simplex virus 1 entry and spread in human retinal pigment epithelial cells. FEBS J 275:5272-5285. http://dx.doi.org/10.1111/j.1742-4658.2008.06655.x.
41. Galen B, Cheshenko N, Tuyama A, Ramratnam B, Herold BC. 2006. Access to nectin favors herpes simplex virus infection at the apical surface of polarized human epithelial cells. J Virol 80:12209-12218. http://dx.doi.org/10.1128/JVI.01503-06.
42. Bender FC, Whitbeck JC, Ponce de Leon M, Lou H, Eisenberg RJ, Cohen GH. 2003. Specific association of glycoprotein B with lipid rafts during herpes simplex virus entry. J Virol 77:9542-9552. http://dx.doi.org/10.1128/JVI.77.17.9542-9552.2003.
43. MacLeod DT, Nakatsuji T, Yamasaki K, Kobzik L, Gallo RL. 2013. HSV-1 exploits the innate immune scavenger receptor MARCO to enhance epithelial adsorption and infection. Nat Commun 4:1963.