Herpes Simplex Virus Requires Poly(ADP-ribose) Polymerase Activity for Efficient Replication and Induces Extracellular Signal-related Kinase-dependent Phosphorylation and ICP0-dependent Nuclear Localization of Tankyrase 1

Overview

Journal J Virol

Publisher American Society for Microbiology

Date 2011 Oct 21

PMID 22013039

Citations 28

Authors

Zhuan Li

Yohei Yamauchi

Maki Kamakura

Tsugiya Murayama

Fumi Goshima

Hiroshi Kimura

Yukihiro Nishiyama

Affiliations

Soon will be listed here.

Abstract

Tankyrase 1 is a poly(ADP-ribose) polymerase (PARP) which localizes to multiple subcellular sites, including telomeres and mitotic centrosomes. Poly(ADP-ribosyl)ation of the nuclear mitotic apparatus (NuMA) protein by tankyrase 1 during mitosis is essential for sister telomere resolution and mitotic spindle pole formation. In interphase cells, tankyrase 1 resides in the cytoplasm, and its role therein is not well understood. In this study, we found that herpes simplex virus (HSV) infection induced extensive modification of tankyrase 1 but not tankyrase 2. This modification was dependent on extracellular signal-regulated kinase (ERK) activity triggered by HSV infection. Following HSV-1 infection, tankyrase 1 was recruited to the nucleus. In the early phase of infection, tankyrase 1 colocalized with ICP0 and thereafter localized within the HSV replication compartment, which was blocked in cells infected with the HSV-1 ICP0-null mutant R7910. In the absence of infection, ICP0 interacted with tankyrase 1 and efficiently promoted its nuclear localization. HSV did not replicate efficiently in cells depleted of both tankyrases 1 and 2. Moreover, XAV939, an inhibitor of tankyrase PARP activity, decreased viral titers to 2 to 5% of control values. We concluded that HSV targets tankyrase 1 in an ICP0- and ERK-dependent manner to facilitate its replication.

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References

Chi N, Lodish H . Tankyrase is a golgi-associated mitogen-activated protein kinase substrate that interacts with IRAP in GLUT4 vesicles. J Biol Chem. 2000; 275(49):38437-44. DOI: 10.1074/jbc.M007635200. View

Diao L, Zhang B, Xuan C, Sun S, Yang K, Tang Y . Activation of c-Jun N-terminal kinase (JNK) pathway by HSV-1 immediate early protein ICP0. Exp Cell Res. 2005; 308(1):196-210. PMC: 7094335. DOI: 10.1016/j.yexcr.2005.04.016. View

Okamoto K, Shinkai Y . TRFH domain is critical for TRF1-mediated telomere stabilization. Cell Struct Funct. 2009; 34(2):71-6. DOI: 10.1247/csf.09007. View

Stow N, Davison A . Identification of a varicella-zoster virus origin of DNA replication and its activation by herpes simplex virus type 1 gene products. J Gen Virol. 1986; 67 ( Pt 8):1613-23. DOI: 10.1099/0022-1317-67-8-1613. View

Phelan A, Dunlop J, Patel A, Stow N, Clements J . Nuclear sites of herpes simplex virus type 1 DNA replication and transcription colocalize at early times postinfection and are largely distinct from RNA processing factors. J Virol. 1997; 71(2):1124-32. PMC: 191164. DOI: 10.1128/JVI.71.2.1124-1132.1997. View

Hagglund R, Roizman B . Role of ICP0 in the strategy of conquest of the host cell by herpes simplex virus 1. J Virol. 2004; 78(5):2169-78. PMC: 369245. DOI: 10.1128/jvi.78.5.2169-2178.2004. View

Everett R, Cross A, Orr A . A truncated form of herpes simplex virus type 1 immediate-early protein Vmw110 is expressed in a cell type dependent manner. Virology. 1993; 197(2):751-6. DOI: 10.1006/viro.1993.1651. View

Miwa M, Masutani M . PolyADP-ribosylation and cancer. Cancer Sci. 2007; 98(10):1528-35. PMC: 11159171. DOI: 10.1111/j.1349-7006.2007.00567.x. View

Chang P, Coughlin M, Mitchison T . Interaction between Poly(ADP-ribose) and NuMA contributes to mitotic spindle pole assembly. Mol Biol Cell. 2009; 20(21):4575-85. PMC: 2770945. DOI: 10.1091/mbc.e09-06-0477. View

10.

Benetti L, Roizman B . Herpes simplex virus protein kinase US3 activates and functionally overlaps protein kinase A to block apoptosis. Proc Natl Acad Sci U S A. 2004; 101(25):9411-6. PMC: 438990. DOI: 10.1073/pnas.0403160101. View

11.

Lamberti C, Weller S . The herpes simplex virus type 1 cleavage/packaging protein, UL32, is involved in efficient localization of capsids to replication compartments. J Virol. 1998; 72(3):2463-73. PMC: 109547. DOI: 10.1128/JVI.72.3.2463-2473.1998. View

12.

Kuddus R, DeLuca N . DNA-dependent oligomerization of herpes simplex virus type 1 regulatory protein ICP4. J Virol. 2007; 81(17):9230-7. PMC: 1951460. DOI: 10.1128/JVI.01054-07. View

13.

Zhao Y, Holden V, Smith R, OCallaghan D . Regulatory function of the equine herpesvirus 1 ICP27 gene product. J Virol. 1995; 69(5):2786-93. PMC: 188972. DOI: 10.1128/JVI.69.5.2786-2793.1995. View

14.

Boutell C, Everett R . The herpes simplex virus type 1 (HSV-1) regulatory protein ICP0 interacts with and Ubiquitinates p53. J Biol Chem. 2003; 278(38):36596-602. DOI: 10.1074/jbc.M300776200. View

15.

Okamoto K, Iwano T, Tachibana M, Shinkai Y . Distinct roles of TRF1 in the regulation of telomere structure and lengthening. J Biol Chem. 2008; 283(35):23981-8. PMC: 3259774. DOI: 10.1074/jbc.M802395200. View

16.

Chen C, Busson M, Rocha V, Appert M, Lepage V, Dulphy N . Activating KIR genes are associated with CMV reactivation and survival after non-T-cell depleted HLA-identical sibling bone marrow transplantation for malignant disorders. Bone Marrow Transplant. 2006; 38(6):437-44. DOI: 10.1038/sj.bmt.1705468. View

17.

Taus N, Salmon B, Baines J . The herpes simplex virus 1 UL 17 gene is required for localization of capsids and major and minor capsid proteins to intranuclear sites where viral DNA is cleaved and packaged. Virology. 1999; 252(1):115-25. DOI: 10.1006/viro.1998.9439. View

18.

Seimiya H, Smith S . The telomeric poly(ADP-ribose) polymerase, tankyrase 1, contains multiple binding sites for telomeric repeat binding factor 1 (TRF1) and a novel acceptor, 182-kDa tankyrase-binding protein (TAB182). J Biol Chem. 2002; 277(16):14116-26. DOI: 10.1074/jbc.M112266200. View

19.

Kaminker P, Kim S, Taylor R, Zebarjadian Y, Funk W, Morin G . TANK2, a new TRF1-associated poly(ADP-ribose) polymerase, causes rapid induction of cell death upon overexpression. J Biol Chem. 2001; 276(38):35891-9. DOI: 10.1074/jbc.M105968200. View

20.

Frank I, Friedman H . A novel function of the herpes simplex virus type 1 Fc receptor: participation in bipolar bridging of antiviral immunoglobulin G. J Virol. 1989; 63(11):4479-88. PMC: 251078. DOI: 10.1128/JVI.63.11.4479-4488.1989. View