Abstract
In the present study, seven novel host cell factors associated with VP22 were identified from the human leukocyte cDNA library using a yeast two-hybrid high-throughput screening system. To confirm some of the interactions, VP22 and its homologues and two candidate targets were tagged with enhanced cyan or yellow fluorescent protein. While RING finger protein 10 (RNF10), WD repeat-containing protein 42A (WDR42A) or VP22 alone showed distinct subcellular localization patterns, RNF10 and WDR42A were relocated when co-expressed with VP22 or its homologues. Thus, these potential host cell factors of VP22 might expand the list of the host targets of VP22.
References
Aints A, Guven H, Gahrton G, Smith CI, Dilber MS (2001) Mapping of herpes simplex virus-1 VP22 functional domains for inter- and subcellular protein targeting. Gene Ther 8:1051–1056
Angers S, Li T, Yi X, MacCoss MJ, Moon RT, Zheng N (2006) Molecular architecture and assembly of the DDB1-CUL4A ubiquitin ligase machinery. Nature 443:590–593
Brignati MJ, Loomis JS, Wills JW, Courtney RJ (2003) Membrane association of VP22, a herpes simplex virus type 1 tegument protein. J Virol 77:4888–4898
Cheshenko N, Liu W, Satlin LM, Herold BC (2005) Focal adhesion kinase plays a pivotal role in herpes simplex virus entry. J Biol Chem 280:31116–31125
Chi JH, Harley CA, Mukhopadhyay A, Wilson DW (2005) The cytoplasmic tail of herpes simplex virus envelope glycoprotein D binds to the tegument protein VP22 and to capsids. J Gen Virol 86:253–261
Cilloniz C, Jackson W, Grose C, Czechowski D, Hay J, Ruyechan WT (2007) The varicella-zoster virus (VZV) ORF9 protein interacts with the IE62 major VZV transactivator. J Virol 81:761–774
Daher KA, Selsted ME, Lehrer RI (1986) Direct inactivation of viruses by human granulocyte defensins. J Virol 60:1068–1074
del Rio T, Werner HC, Enquist LW (2002) The pseudorabies virus VP22 homologue (UL49) is dispensable for virus growth in vitro and has no effect on virulence and neuronal spread in rodents. J Virol 76:774–782
Duffy C, Mbong EF, Baines JD (2009) VP22 of herpes simplex virus 1 promotes protein synthesis at late times in infection and accumulation of a subset of viral mRNAs at early times in infection. J Virol 83:1009–1017
Elliott G, Mouzakitis G, O’Hare P (1995) VP16 interacts via its activation domain with VP22, a tegument protein of herpes simplex virus, and is relocated to a novel macromolecular assembly in coexpressing cells. J Virol 69:7932–7941
Elliott G, O’Hare P (1999) Live-cell analysis of a green fluorescent protein-tagged herpes simplex virus infection. J Virol 73:4110–4119
Fawl RL, Roizman B (1994) The molecular basis of herpes simplex virus pathogenicity. Semin Virol 5:267–271
Fossum E, Friedel CC, Rajagopala SV, Titz B, Baiker A, Schmidt T, Kraus T, Stellberger T, Rutenberg C, Suthram S, Bandyopadhyay S, Rose D, von Brunn A, Uhlmann M, Zeretzke C, Dong YA, Boulet H, Koegl M, Bailer SM, Koszinowski U, Ideker T, Uetz P, Zimmer R, Haas J (2009) Evolutionarily conserved herpesviral protein interaction networks. PLoS Pathog 5:e1000570
Gupta A, Gartner JJ, Sethupathy P, Hatzigeorgiou AG, Fraser NW (2006) Anti-apoptotic function of a microRNA encoded by the HSV-1 latency-associated transcript. Nature 442:82–85
Han SH, Jeon JH, Ju HR, Jung U, Kim KY, Yoo HS, Lee YH, Song KS, Hwang HM, Na YS, Yang Y, Lee KN, Choi I (2003) VDUP1 upregulated by TGF-beta1 and 1, 25-dihydorxyvitamin D3 inhibits tumor cell growth by blocking cell-cycle progression. Oncogene 22:4035–4046
Harms JS, Ren X, Oliveira SC, Splitter GA (2000) Distinctions between bovine herpesvirus 1 and herpes simplex virus type 1 VP22 tegument protein subcellular associations. J Virol 74:3301–3312
Hoshikawa S, Ogata T, Fujiwara S, Nakamura K, Tanaka S (2008) A novel function of RING finger protein 10 in transcriptional regulation of the myelin-associated glycoprotein gene and myelin formation in Schwann cells. PLoS One 3:e3464
Johnson AJ, Chu CF, Milligan GN (2008) Effector CD4+ T-cell involvement in clearance of infectious herpes simplex virus type 1 from sensory ganglia and spinal cords. J Virol 82:9678–9688
Kotsakis A, Pomeranz LE, Blouin A, Blaho JA (2001) Microtubule reorganization during herpes simplex virus type 1 infection facilitates the nuclear localization of VP22, a major virion tegument protein. J Virol 75:8697–8711
Lee JH, Vittone V, Diefenbach E, Cunningham AL, Diefenbach RJ (2008) Identification of structural protein-protein interactions of herpes simplex virus type 1. Virology 378:347–354
Levay AK, Peacock JD, Lu Y, Koch M, Hinton RB Jr, Kadler KE, Lincoln J (2008) Scleraxis is required for cell lineage differentiation and extracellular matrix remodeling during murine heart valve formation in vivo. Circ Res 103:948–956
Li ML, Guo H, Ding Q, Zheng CF (2009) A multiple functional protein: the herpes simplex virus type 1 tegument protein VP22. Virol Sin 24:153–161
Lin J, Friesen MT, Bocangel P, Cheung D, Rawszer K, Wigle JT (2005) Characterization of Mesenchyme Homeobox 2 (MEOX2) transcription factor binding to RING finger protein 10. Mol Cell Biochem 275:75–84
Lopez MR, Schlegel EF, Wintersteller S, Blaho JA (2008) The major tegument structural protein VP22 targets areas of dispersed nucleolin and marginalized chromatin during productive herpes simplex virus 1 infection. Virus Res 136:175–188
Martin A, O’Hare P, McLauchlan J, Elliott G (2002) Herpes simplex virus tegument protein VP22 contains overlapping domains for cytoplasmic localization, microtubule interaction, and chromatin binding. J Virol 76:4961–4970
Mathew SS, Bryant PW, Burch AD (2010) Accumulation of oxidized proteins in Herpesvirus infected cells. Free Radic Biol Med 49:383–391
O’Regan KJ, Bucks MA, Murphy MA, Wills JW, Courtney RJ (2007) A conserved region of the herpes simplex virus type 1 tegument protein VP22 facilitates interaction with the cytoplasmic tail of glycoprotein E (gE). Virology 358:192–200
O’Regan KJ, Murphy MA, Bucks MA, Wills JW, Courtney RJ (2007) Incorporation of the herpes simplex virus type 1 tegument protein VP22 into the virus particle is independent of interaction with VP16. Virology 369:263–280
Osmundson EC, Ray D, Moore FE, Gao Q, Thomsen GH, Kiyokawa H (2008) The HECT E3 ligase Smurf2 is required for Mad2-dependent spindle assembly checkpoint. J Cell Biol 183:267–277
Paludan SR (2001) Requirements for the induction of interleukin-6 by herpes simplex virus-infected leukocytes. J Virol 75:8008–8015
Peri P, Nuutila K, Vuorinen T, Saukko P, Hukkanen V (2011) Cathepsins are involved in virus-induced cell death in ICP4 and Us3 deletion mutant herpes simplex virus type 1-infected monocytic cells. J Gen Virol 92:173–180
Phelan A, Elliott G, O’Hare P (1998) Intercellular delivery of functional p53 by the herpesvirus protein VP22. Nat Biotechnol 16:440–443
Saurin AJ, Borden KL, Boddy MN, Freemont PS (1996) Does this have a familiar RING? Trends Biochem Sci 21:208–214
Schaller MD (2010) Cellular functions of FAK kinases: insight into molecular mechanisms and novel functions. J Cell Sci 123:1007–1013
Schulze PC, Yoshioka J, Takahashi T, He Z, King GL, Lee RT (2004) Hyperglycemia promotes oxidative stress through inhibition of thioredoxin function by thioredoxin-interacting protein. J Biol Chem 279:30369–30374
Sloan DD, Jerome KR (2007) Herpes simplex virus remodels T-cell receptor signaling, resulting in p38-dependent selective synthesis of interleukin-10. J Virol 81:12504–12514
Smith TF, Gaitatzes C, Saxena K, Neer EJ (1999) The WD repeat: a common architecture for diverse functions. Trends Biochem Sci 24:181–185
Taddeo B, Sciortino MT, Zhang W, Roizman B (2007) Interaction of herpes simplex virus RNase with VP16 and VP22 is required for the accumulation of the protein but not for accumulation of mRNA. Proc Natl Acad Sci USA 104:12163–12168
van Leeuwen H, Elliott G, O’Hare P (2002) Evidence of a role for nonmuscle myosin II in herpes simplex virus type 1 egress. J Virol 76:3471–3481
van Leeuwen H, Okuwaki M, Hong R, Chakravarti D, Nagata K, O’Hare P (2003) Herpes simplex virus type 1 tegument protein VP22 interacts with TAF-I proteins and inhibits nucleosome assembly but not regulation of histone acetylation by INHAT. J Gen Virol 84:2501–2510
Yedowitz JC, Kotsakis A, Schlegel EF, Blaho JA (2005) Nuclear localizations of the herpes simplex virus type 1 tegument proteins VP13/14, vhs, and VP16 precede VP22-dependent microtubule reorganization and VP22 nuclear import. J Virol 79:4730–4743
Yoshida T, Oka S, Masutani H, Nakamura H, Yodoi J (2003) The role of thioredoxin in the aging process: involvement of oxidative stress. Antioxid Redox Signal 5:563–570
Yu X, Liu L, Wu L, Wang L, Dong C, Li W, Li Q (2010) Herpes simplex virus type 1 tegument protein VP22 is capable of modulating the transcription of viral TK and gC genes via interaction with viral ICP0. Biochimie 92:1024–1030
Zheng C, Brownlie R, Babiuk LA, van den Hurk S (2005) Characterization of the nuclear localization and nuclear export signals of bovine herpesvirus 1 VP22. J Virol 79:11864–11872
Zuo P, Maniatis T (1996) The splicing factor U2AF35 mediates critical protein-protein interactions in constitutive and enhancer-dependent splicing. Genes Dev 10:1356–1368
Acknowledgments
This work was supported by grants from the Startup Fund of the Hundred Talents Program of the Chinese Academy of Sciences (20071010-141) and National Natural Science Foundation of China (30900059; 81000736). We thank Dr. Zhengfei Liu, Dr. Rui Zhou and Dr. Hua Zhu for the generous gift of viruses BHV-1, PRV and VZV, respectively. We thank Dr. Hong Guo, Shengping Huang and Jingjing Chen for technical assistance.
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Li, M., Wang, L., Ren, X. et al. Host cell targets of tegument protein VP22 of herpes simplex virus 1. Arch Virol 156, 1079–1084 (2011). https://doi.org/10.1007/s00705-011-0960-9
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DOI: https://doi.org/10.1007/s00705-011-0960-9