Nonmuscle myosin heavy chain IIA mediates Epstein-Barr virus infection of nasopharyngeal epithelial cells

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 35, 2015, Pages 11036-11041

  Xiong, Dan ^a   Du, Yong ^a   Wang, Hong Bo ^a   Zhao, Bo ^b   Zhang, Hua ^a   Li, Yan ^a   Hu, Li Juan ^a   Cao, Jing Yan ^a   Zhong, Qian ^a   Liu, Wan Li ^a   Li, Man Zhi ^a   Zhu, Xiao Feng ^a   Tsao, Sai Wah ^c   Hutt Fletcher, Lindsey M ^d   Song, Erwei ^e   Zeng, Yi Xin ^a   Kieff, Elliott ^b   Zeng, Mu Sheng ^a  

^a SUN YAT SEN UNIVERSITY CANCER CENTER   (China)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c UNIVERSITY OF HONG KONG   (Hong Kong)

^d LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^e SUN YAT SEN UNIVERSITY   (China)

Author keywords

BMI1; Epstein Barr virus; gH gL; Nasopharyngeal carcinoma; NMHC IIA

Indexed keywords

GLYCOPROTEIN B; MYOSIN HEAVY CHAIN; NEUROPILIN 1; NONMUSCLE MYOSIN HEAVY CHAIN IIA; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EPITHELIUM CELL; EPSTEIN BARR VIRUS; EPSTEIN BARR VIRUS INFECTION; FLOW CYTOMETRY; GENE EXPRESSION; GENE SILENCING; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; LIQUID CHROMATOGRAPHY; NASOPHARYNX CARCINOMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SURFACE PROPERTY; TANDEM MASS SPECTROMETRY; AMINO ACID SEQUENCE; CHEMISTRY; MOLECULAR GENETICS; NASOPHARYNX; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; TRANSFORMED CELL LINE; VIROLOGY;

AMINO ACID SEQUENCE; CELL LINE, TRANSFORMED; EPSTEIN-BARR VIRUS INFECTIONS; HUMANS; MOLECULAR SEQUENCE DATA; MYOSIN HEAVY CHAINS; NASOPHARYNX;

EID: 84941013212     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1513359112     Document Type: Article

References (42)

1. Cohen JI (2000) Epstein-Barr virus infection. N Engl J Med 343(7):481-492.
2. Lieberman PM (2014) Virology. Epstein-Barr virus turns 50. Science 343(6177):1323-1325.
3. Young LS (2014) Epstein-Barr virus at 50-future perspectives. Chin J Cancer 33(11):527-528.
4. Hutt-Fletcher LM (2007) Epstein-Barr virus entry. J Virol 81(15):7825-7832.
5. Tanner J, Weis J, Fearon D, Whang Y, Kieff E (1987) Epstein-Barr virus gp350/220 binding to the B lymphocyte C3d receptor mediates adsorption, capping, and endocytosis. Cell 50(2):203-213.
6. Ogembo JG, et al. (2013) Human complement receptor type 1/CD35 is an Epstein-Barr Virus receptor. Cell Rep 3(2):371-385.
7. Wang X, Hutt-Fletcher LM (1998) Epstein-Barr virus lacking glycoprotein gp42 can bind to B cells but is not able to infect. J Virol 72(1):158-163.
8. Mullen MM, Haan KM, Longnecker R, Jardetzky TS (2002) Structure of the Epstein-Barr virus gp42 protein bound to the MHC class II receptor HLA-DR1. Mol Cell 9(2):375-385.
9. Tugizov SM, Berline JW, Palefsky JM (2003) Epstein-Barr virus infection of polarized tongue and nasopharyngeal epithelial cells. Nat Med 9(3):307-314.
10. Wang HB, et al. (2015) Neuropilin 1 is an entry factor that promotes EBV infection of nasopharyngeal epithelial cells. Nat Commun 6:6240.
11. Borza CM, Hutt-Fletcher LM (2002) Alternate replication in B cells and epithelial cells switches tropism of Epstein-Barr virus. Nat Med 8(6):594-599.
12. Turk SM, Jiang R, Chesnokova LS, Hutt-Fletcher LM (2006) Antibodies to gp350/220 enhance the ability of Epstein-Barr virus to infect epithelial cells. J Virol 80(19):9628-9633.
13. Molesworth SJ, Lake CM, Borza CM, Turk SM, Hutt-Fletcher LM (2000) Epstein-Barr virus gH is essential for penetration of B cells but also plays a role in attachment of virus to epithelial cells. J Virol 74(14):6324-6332.
14. Omerović J, Lev L, Longnecker R (2005) The amino terminus of Epstein-Barr virus glycoprotein gH is important for fusion with epithelial and B cells. J Virol 79(19):12408-12415.
15. Wu L, Hutt-Fletcher LM (2007) Point mutations in EBV gH that abrogate or differentially affect B cell and epithelial cell fusion. Virology 363(1):148-155.
16. Chesnokova LS, Nishimura SL, Hutt-Fletcher LM (2009) Fusion of epithelial cells by Epstein-Barr virus proteins is triggered by binding of viral glycoproteins gHgL to integrins alphavbeta6 or alphavbeta8. Proc Natl Acad Sci USA 106(48):20464-20469.
17. Chen J, Rowe CL, Jardetzky TS, Longnecker R (2012) The KGD motif of Epstein-Barr virus gH/gL is bifunctional, orchestrating infection of B cells and epithelial cells. MBio 3(1):e00290-11.
18. Matsuura H, Kirschner AN, Longnecker R, Jardetzky TS (2010) Crystal structure of the Epstein-Barr virus (EBV) glycoprotein H/glycoprotein L (gH/gL) complex. Proc Natl Acad Sci USA 107(52):22641-22646.
19. Connolly SA, Jackson JO, Jardetzky TS, Longnecker R (2011) Fusing structure and function: A structural view of the herpesvirus entry machinery. Nat Rev Microbiol 9(5):369-381.
20. Chesnokova LS, Hutt-Fletcher LM (2011) Fusion of Epstein-Barr virus with epithelial cells can be triggered by αvβ5 in addition to αvβ6 and αvβ8, and integrin binding triggers a conformational change in glycoproteins gHgL. J Virol 85(24):13214-13223.
21. Chesnokova LS, Ahuja MK, Hutt-Fletcher LM (2014) Epstein-Barr virus glycoprotein gB and gHgL can mediate fusion and entry in trans, and heat can act as a partial surrogate for gHgL and trigger a conformational change in gB. JVirol88(21):12193-12201.
22. Wu L, Borza CM, Hutt-Fletcher LM (2005) Mutations of Epstein-Barr virus gH that are differentially able to support fusion with B cells or epithelial cells. J Virol 79(17):10923-10930.
23. Molofsky AV, He S, Bydon M, Morrison SJ, Pardal R (2005) Bmi-1 promotes neural stem cell self-renewal and neural development but not mouse growth and survival by repressing the p16Ink4a and p19Arf senescence pathways. Genes Dev 19(12):1432-1437.
24. Lessard J, Sauvageau G (2003) Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature 423(6937):255-260.
25. Song LB, et al. (2006) Bmi-1 is a novel molecular marker of nasopharyngeal carcinoma progression and immortalizes primary human nasopharyngeal epithelial cells. Cancer Res 66(12):6225-6232.
26. Park IK, Morrison SJ, Clarke MF (2004) Bmi1, stem cells, and senescence regulation. J Clin Invest 113(2):175-179.
27. Arii J, et al. (2010) Non-muscle myosin IIA is a functional entry receptor for herpes simplex virus-1. Nature 467(7317):859-862.
28. Vicente-Manzanares M, Ma X, Adelstein RS, Horwitz AR (2009) Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat Rev Mol Cell Biol 10(11):778-790.
29. Shannon-Lowe C, Rowe M (2011) Epstein-Barr virus infection of polarized epithelial cells via the basolateral surface by memory B cell-mediated transfer infection. PLoS Pathog 7(5):e1001338.
30. Shannon-Lowe CD, Neuhierl B, Baldwin G, Rickinson AB, Delecluse HJ (2006) Resting B cells as a transfer vehicle for Epstein-Barr virus infection of epithelial cells. Proc Natl Acad Sci USA 103(18):7065-7070.
31. Imai S, Nishikawa J, Takada K (1998) Cell-to-cell contact as an efficient mode of Epstein-Barr virus infection of diverse human epithelial cells. J Virol 72(5):4371-4378.
32. Valencia SM, Hutt-Fletcher LM (2012) Important but differential roles for actin in trafficking of Epstein-Barr virus in B cells and epithelial cells. J Virol 86(1):2-10.
33. Lo KW, To KF, Huang DP (2004) Focus on nasopharyngeal carcinoma. Cancer Cell 5(5):423-428.
34. Temple RM, et al. (2014) Efficient replication of Epstein-Barr virus in stratified epithelium in vitro. Proc Natl Acad Sci USA 111(46):16544-16549.
35. Kong QL, Guan S, Guo BH, Zeng MS (2009) Pre-malignant nasopharyngeal epithelial cell models. Chin J Cancer 28(10):1012-1015.
36. Lan K, Verma SC, Murakami M, Bajaj B, Robertson ES (2007) Epstein-Barr Virus (EBV): Infection, propagation, quantitation, and storage. Curr Protoc Microbiol Chapter 14:Unit 14E.2.
37. Shimizu N, Yoshiyama H, Takada K (1996) Clonal propagation of Epstein-Barr virus (EBV) recombinants in EBV-negative Akata cells. J Virol 70(10):7260-7263.
38. Strnad BC, et al. (1982) Production and characterization of monoclonal antibodies against the Epstein-Barr virus membrane antigen. J Virol 41(1):258-264.
39. Li Q, Turk SM, Hutt-Fletcher LM (1995) The Epstein-Barr virus (EBV) BZLF2 gene product associates with the gH and gL homologs of EBV and carries an epitope critical to infection of B cells but not of epithelial cells. J Virol 69(7):3987-3994.
40. Lo YM, et al. (1999) Quantitative analysis of cell-free Epstein-Barr virus DNA in plasma of patients with nasopharyngeal carcinoma. Cancer Res 59(6):1188-1191.
41. Song LB, et al. (2009) The polycomb group protein Bmi-1 represses the tumor suppressor PTEN and induces epithelial-mesenchymal transition in human nasopharyngeal epithelial cells. J Clin Invest 119(12):3626-3636.
42. Weiss LM, Chen YY (2013) EBER in situ hybridization for Epstein-Barr virus. Methods Mol Biol 999:223-230.