DNA methyltransferase DNMT3A associates with viral proteins and impacts HSV-1 infection

Proteomics

Volumn 15, Issue 12, 2015, Pages 1968-1982

  Rowles, Daniell L ^a   Tsai, Yuan Chin ^a   Greco, Todd M ^a   Lin, Aaron E ^a   Li, Minghao ^a   Yeh, Justin ^a   Cristea, Ileana M ^a  

^a PRINCETON UNIVERSITY   (United States)

Author keywords

DNMT3A; HSV 1; Microbiology; Phosphorylation; Protein protein interaction; Virus host interactions

Indexed keywords

CAPSID PROTEIN; DNA METHYLTRANSFERASE; DNA METHYLTRANSFERASE 3A; FLUORESCENT DYE; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VIRUS PROTEIN; VP26 PROTEIN; CAPSID PROTEIN VP26, HERPES SIMPLEX VIRUS TYPE 1; DNA (CYTOSINE 5) METHYLTRANSFERASE; PROTEOME; VIRAL PROTEIN; VP5 PROTEIN, HERPES SIMPLEX VIRUS TYPE 1;

ANTIBODY AFFINITY; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME ACTIVITY; FIBROBLAST; GENE SILENCING; HERPES SIMPLEX; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; MASS SPECTROMETRY; MICROSCOPY; PRIORITY JOURNAL; PROTEIN ACETYLATION; PROTEIN INTERACTION; PROTEIN ISOLATION; PROTEIN PHOSPHORYLATION; PROTEOMICS; PURIFICATION; VIRUS CAPSID; VIRUS CELL INTERACTION; ANIMAL; CELL CULTURE; CHLOROCEBUS AETHIOPS; CYTOLOGY; HOST PATHOGEN INTERACTION; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MATRIX-ASSISTED LASER DESORPTION-IONIZATION MASS SPECTROMETRY; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; VERO CELL LINE; VIROLOGY; VIRUS REPLICATION;

HUMAN HERPESVIRUS 1; MAMMALIA; MIRIDAE;

ANIMALS; CAPSID PROTEINS; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; FIBROBLASTS; HERPES SIMPLEX; HERPESVIRUS 1, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; PHOSPHORYLATION; PROTEOME; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; VERO CELLS; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 84931006688     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201500035     Document Type: Article

References (91)

1. Xu, F., Sternberg, M. R., Kottiri, B. J., McQuillan, G. M. et al., Trends in herpes simplex virus type 1 and type 2 seroprevalence in the United States. JAMA 2006, 296, 964-973.
2. Levitz, R. E., Herpes simplex encephalitis: a review. Heart Lung 1998, 27, 209-212.
3. Claoue, C., DeCock, R., The spectrum of herpes simplex virus disease of the anterior segment in the 1990s. Acta Ophthalmol. Scand. 1996, 74, 407-410.
4. Grunewald, K., Desai, P., Winkler, D. C., Heymann, J. B. et al., Three-dimensional structure of herpes simplex virus from cryo-electron tomography. Science 2003, 302, 1396-1398.
5. Baker, M. L., Jiang, W., Wedemeyer, W. J., Rixon, F. J. et al., Ab initio modeling of the herpesvirus VP26 core domain assessed by CryoEM density. PLoS Comput. Biol. 2006, 2, e146.
6. McGeoch, D. J., Dalrymple, M. A., Davison, A. J., Dolan, A. et al., The complete DNA sequence of the long unique region in the genome of herpes simplex virus type 1. J. Gen. Virol. 1988, 69(Pt 7), 1531-1574.
7. Borst, E. M., Mathys, S., Wagner, M., Muranyi, W., Messerle, M., Genetic evidence of an essential role for cytomegalovirus small capsid protein in viral growth. J. Virol. 2001, 75, 1450-1458.
8. Desai, P., DeLuca, N. A., Person, S., Herpes simplex virus type 1 VP26 is not essential for replication in cell culture but influences production of infectious virus in the nervous system of infected mice. Virology 1998, 247, 115-124.
9. Henson, B. W., Perkins, E. M., Cothran, J. E., Desai, P., Self-assembly of Epstein-Barr virus capsids. J. Virol. 2009, 83, 3877-3890.
10. Perkins, E. M., Anacker, D., Davis, A., Sankar, V. et al., Small capsid protein pORF65 is essential for assembly of Kaposi's sarcoma-associated herpesvirus capsids. J. Virol. 2008, 82, 7201-7211.
11. Homa, F. L., Brown, J. C., Capsid assembly and DNA packaging in herpes simplex virus. Rev. Med. Virol. 1997, 7, 107-122.
12. Rixon, F. J., Addison, C., McGregor, A., Macnab, S. J. et al., Multiple interactions control the intracellular localization of the herpes simplex virus type 1 capsid proteins. J. Gen. Virol. 1996, 77(Pt 9), 2251-2260.
13. Desai, P., Akpa, J. C., Person, S., Residues of VP26 of herpes simplex virus type 1 that are required for its interaction with capsids. J. Virol. 2003, 77, 391-404.
14. Lee, J. H., Vittone, V., Diefenbach, E., Cunningham, A. L., Diefenbach, R. J., Identification of structural protein-protein interactions of herpes simplex virus type 1. Virology 2008, 378, 347-354.
15. Uetz, P., Dong, Y. A., Zeretzke, C., Atzler, C. et al., Herpesviral protein networks and their interaction with the human proteome. Science 2006, 311, 239-242.
16. Apcarian, A., Cunningham, A. L., Diefenbach, R. J., Identification of binding domains in the herpes simplex virus type 1 small capsid protein pUL35 (VP26). J. Gen. Virol. 2010, 91, 2659-2663.
17. Ko, D. H., Cunningham, A. L., Diefenbach, R. J., The major determinant for addition of tegument protein pUL48 (VP16) to capsids in herpes simplex virus type 1 is the presence of the major tegument protein pUL36 (VP1/2). J. Virol. 2010, 84, 1397-1405.
18. Douglas, M. W., Diefenbach, R. J., Homa, F. L., Miranda-Saksena, M. et al., Herpes simplex virus type 1 capsid protein VP26 interacts with dynein light chains RP3 and Tctex1 and plays a role in retrograde cellular transport. J. Biol. Chem. 2004, 279, 28522-28530.
19. Wang, L., Liu, L., Che, Y., Jiang, L. et al., Egress of HSV-1 capsid requires the interaction of VP26 and a cellular tetraspanin membrane protein. Virol. J. 7, 156.
20. Lin, A. E., Greco, T. M., Dohner, K., Sodeik, B., Cristea, I. M., A proteomic perspective of inbuilt viral protein regulation: pUL46 viral tegument protein is targeted for degradation by the viral ICP0 protein during HSV-1 infection. Mol. Cell. Proteomics 2013, 12, 3237-3252.
21. Moorman, N. J., Cristea, I. M., Terhune, S. S., Rout, M. P. et al., Human cytomegalovirus protein UL38 inhibits host cell stress responses by antagonizing the tuberous sclerosis protein complex. Cell Host Microbe 2008, 3, 253-262.
22. Moorman, N. J., Sharon-Friling, R., Shenk, T., Cristea, I. M., A targeted spatial-temporal proteomics approach implicates multiple cellular trafficking pathways in human cytomegalovirus virion maturation. Mol. Cell. Proteomics 2010, 9, 851-860.
23. Cristea, I. M., Moorman, N. J., Terhune, S. S., Cuevas, C. D. et al., Human cytomegalovirus pUL83 stimulates activity of the viral immediate-early promoter through its interaction with the cellular IFI16 protein. J. Virol. 2010, 84, 7803-7814.
24. Terhune, S. S., Moorman, N. J., Cristea, I. M., Savaryn, J. P. et al., Human cytomegalovirus UL29/28 protein interacts with components of the NuRD complex which promote accumulation of immediate-early RNA. PLoS Pathog. 2010, 6, e1000965.
25. Kramer, T., Greco, T. M., Taylor, M. P., Ambrosini, A. E. et al., Kinesin-3 mediates axonal sorting and directional transport of alphaherpesvirus particles in neurons. Cell Host Microbe 2012, 12, 806-814.
26. Kratchmarov, R., Kramer, T., Greco, T. M., Taylor, M. P. et al., Glycoproteins gE and gI are required for efficient KIF1A-dependent anterograde axonal transport of alphaherpesvirus particles in neurons. J. Virol. 2013, 87, 9431-9440.
27. Cristea, I. M., Carroll, J. W., Rout, M. P., Rice, C. M. et al., Tracking and elucidating alphavirus-host protein interactions. J. Biol. Chem. 2006, 281, 30269-30278.
28. Cristea, I. M., Rozjabek, H., Molloy, K. R., Karki, S. et al., Host factors associated with the Sindbis virus RNA-dependent RNA polymerase: role for G3BP1 and G3BP2 in virus replication. J. Virol. 2010, 84, 6720-6732.
29. Youn, S., Li, T., McCune, B. T., Edeling, M. A. et al., Evidence for a genetic and physical interaction between nonstructural proteins NS1 and NS4B that modulates replication of west Nile virus. J. Virol. 2012, 86, 7360-7371.
30. Desai, P., Person, S., Incorporation of the green fluorescent protein into the herpes simplex virus type 1 capsid. J. Virol. 1998, 72, 7563-7568.
31. Joshi, P., Greco, T. M., Guise, A. J., Luo, Y. et al., The functional interactome landscape of the human histone deacetylase family. Mol. Systems Biol. 2013, 9, 672.
32. Cristea, I. M., Williams, R., Chait, B. T., Rout, M. P., Fluorescent proteins as proteomic probes. Mol. Cell. Proteomics 2005, 4, 1933-1941.
33. Conlon, F. L., Miteva, Y., Kaltenbrun, E., Waldron, L. et al., Immunoisolation of protein complexes from Xenopus. Methods Mol. Biol. 2012, 917, 369-390.
34. Tsai, Y. C., Greco, T. M., Boonmee, A., Miteva, Y., Cristea, I. M., Functional proteomics establishes the interaction of SIRT7 with chromatin remodeling complexes and expands its role in regulation of RNA polymerase I transcription. Mol. Cell. Proteomics 2012, 11, 60-76.
35. Chi, J. H., Wilson, D. W., ATP-dependent localization of the herpes simplex virus capsid protein VP26 to sites of procapsid maturation. J. Virol. 2000, 74, 1468-1476.
36. Nagel, C. H., Dohner, K., Fathollahy, M., Strive, T. et al., Nuclear egress and envelopment of herpes simplex virus capsids analyzed with dual-color fluorescence HSV1(17+). J. Virol. 2008, 82, 3109-3124.
37. deOliveira, A. P., Glauser, D. L., Laimbacher, A. S., Strasser, R. et al., Live visualization of herpes simplex virus type 1 compartment dynamics. J. Virol. 2008, 82, 4974-4990.
38. Sugimoto, K., Uema, M., Sagara, H., Tanaka, M. et al., Simultaneous tracking of capsid, tegument, and envelope protein localization in living cells infected with triply fluorescent herpes simplex virus 1. J. Virol. 2008, 82, 5198-5211.
39. Nagel, C. H., Dohner, K., Binz, A., Bauerfeind, R., Sodeik, B., Improper tagging of the non-essential small capsid protein VP26 impairs nuclear capsid egress of herpes simplex virus. PLoS One 2012, 7, e44177.
40. Bowman, B. R., Baker, M. L., Rixon, F. J., Chiu, W., Quiocho, F. A., Structure of the herpesvirus major capsid protein. EMBO J. 2003, 22, 757-765.
41. Zhou, Z. H., He, J., Jakana, J., Tatman, J. D. et al., Assembly of VP26 in herpes simplex virus-1 inferred from structures of wild-type and recombinant capsids. Nat. Struct. Biol. 1995, 2, 1026-1030.
42. Newcomb, W. W., Trus, B. L., Booy, F. P., Steven, A. C. et al., Structure of the herpes simplex virus capsid. Molecular composition of the pentons and the triplexes. J. Mol. Biol. 1993, 232, 499-511.
43. Coller, K. E., Lee, J. I., Ueda, A., Smith, G. A., The capsid and tegument of the alphaherpesviruses are linked by an interaction between the UL25 and VP1/2 proteins. J. Virol. 2007, 81, 11790-11797.
44. Ogasawara, M., Suzutani, T., Yoshida, I., Azuma, M., Role of the UL25 gene product in packaging DNA into the herpes simplex virus capsid: location of UL25 product in the capsid and demonstration that it binds DNA. J. Virol. 2001, 75, 1427-1436.
45. Newcomb, W. W., Homa, F. L., Brown, J. C., Herpes simplex virus capsid structure: DNA packaging protein UL25 is located on the external surface of the capsid near the vertices. J. Virol. 2006, 80, 6286-6294.
46. Thurlow, J. K., Murphy, M., Stow, N. D., Preston, V. G., Herpes simplex virus type 1 DNA-packaging protein UL17 is required for efficient binding of UL25 to capsids. J. Virol. 2006, 80, 2118-2126.
47. Yang, K., Wills, E., Lim, H. Y., Zhou, Z. H., Baines, J. D., Association of herpes simplex virus pUL31 with capsid vertices and components of the capsid vertex-specific complex. J. Virol. 2014, 88, 3815-3825.
48. Yu, D., Weller, S. K., Herpes simplex virus type 1 cleavage and packaging proteins UL15 and UL28 are associated with B but not C capsids during packaging. J. Virol. 1998, 72, 7428-7439.
49. White, C. A., Stow, N. D., Patel, A. H., Hughes, M., Preston, V. G., Herpes simplex virus type 1 portal protein UL6 interacts with the putative terminase subunits UL15 and UL28. J. Virol. 2003, 77, 6351-6358.
50. Hong, Z., Beaudet-Miller, M., Durkin, J., Zhang, R., Kwong, A. D., Identification of a minimal hydrophobic domain in the herpes simplex virus type 1 scaffolding protein which is required for interaction with the major capsid protein. J. Virol. 1996, 70, 533-540.
51. Trus, B. L., Cheng, N., Newcomb, W. W., Homa, F. L. et al., Structure and polymorphism of the UL6 portal protein of herpes simplex virus type 1. J. Virol. 2004, 78, 12668-12671.
52. Vittone, V., Diefenbach, E., Triffett, D., Douglas, M. W. et al., Determination of interactions between tegument proteins of herpes simplex virus type 1. J. Virol. 2005, 79, 9566-9571.
53. Pasdeloup, D., Beilstein, F., Roberts, A. P., McElwee, M. et al., Inner tegument protein pUL37 of herpes simplex virus type 1 is involved in directing capsids to the trans-Golgi network for envelopment. J. Gen. Virol. 91, 2145-2151.
54. Schipke, J., Pohlmann, A., Diestel, R., Binz, A. et al., The C terminus of the large tegument protein pUL36 contains multiple capsid binding sites that function differently during assembly and cell entry of herpes simplex virus. J. Virol. 86, 3682-3700.
55. Yamada, H., Daikoku, T., Yamashita, Y., Jiang, Y. M. et al., The product of the US10 gene of herpes simplex virus type 1 is a capsid/tegument-associated phosphoprotein which copurifies with the nuclear matrix. J. Gen. Virol. 1997, 78(Pt 11), 2923-2931.
56. Krusong, K., Carpenter, E. P., Bellamy, S. R., Savva, R., Baldwin, G. S., A comparative study of uracil-DNA glycosylases from human and herpes simplex virus type 1. J. Biol. Chem. 2006, 281, 4983-4992.
57. Farnsworth, A., Johnson, D. C., Herpes simplex virus gE/gI must accumulate in the trans-Golgi network at early times and then redistribute to cell junctions to promote cell-cell spread. J. Virol. 2006, 80, 3167-3179.
58. Kato, A., Yamamoto, M., Ohno, T., Kodaira, H. et al., Identification of proteins phosphorylated directly by the Us3 protein kinase encoded by herpes simplex virus 1. J. Virol. 2005, 79, 9325-9331.
59. Asai, R., Ohno, T., Kato, A., Kawaguchi, Y., Identification of proteins directly phosphorylated by UL13 protein kinase from herpes simplex virus 1. Microbes Infect. 2007, 9, 1434-1438.
60. Bell, C., Desjardins, M., Thibault, P., Radtke, K., Proteomics analysis of herpes simplex virus type 1-infected cells reveals dynamic changes of viral protein expression, ubiquitylation, and phosphorylation. J. Proteome Res. 2013, 12, 1820-1829.
61. McNabb, D. S., Courtney, R. J., Posttranslational modification and subcellular localization of the p12 capsid protein of herpes simplex virus type 1. J. Virol. 1992, 66, 4839-4847.
62. Yaffe, M. B., Rittinger, K., Volinia, S., Caron, P. R. et al., The structural basis for 14-3-3: phosphopeptide binding specificity. Cell 1997, 91, 961-971.
63. D'Orso, I., Frankel, A. D., Tat acetylation modulates assembly of a viral-host RNA-protein transcription complex. Proc. Natl. Acad. Sci. USA 2009, 106, 3101-3106.
64. Quinlan, E. J., Culleton, S. P., Wu, S. Y., Chiang, C. M., Androphy, E. J., Acetylation of conserved lysines in bovine papillomavirus E2 by p300. J. Virol. 87, 1497-1507.
65. Baker, M. L., Jiang, W., Bowman, B. R., Zhou, Z. H. et al., Architecture of the herpes simplex virus major capsid protein derived from structural bioinformatics. J. Mol. Biol. 2003, 331, 447-456.
66. Kato, A., Liu, Z., Minowa, A., Imai, T. et al., Herpes simplex virus 1 protein kinase Us3 and major tegument protein UL47 reciprocally regulate their subcellular localization in infected cells. J. Virol. 2011, 85, 9599-9613.
67. Carter, K. L., Roizman, B., The promoter and transcriptional unit of a novel herpes simplex virus 1 alpha gene are contained in, and encode a protein in frame with, the open reading frame of the alpha 22 gene. J. Virol. 1996, 70, 172-178.
68. Kim, G. D., Ni, J., Kelesoglu, N., Roberts, R. J., Pradhan, S., Co-operation and communication between the human maintenance and de novo DNA (cytosine-5) methyltransferases. EMBO J. 2002, 21, 4183-4195.
69. Ay, E., Banati, F., Mezei, M., Bakos, A. et al., Epigenetics of HIV infection: promising research areas and implications for therapy. AIDS Rev. 2013, 15, 181-188.
70. Rongrui, L., Na, H., Zongfang, L., Fanpu, J., Shiwen, J., Epigenetic mechanism involved in the HBV/HCV-related hepatocellular carcinoma tumorigenesis. Curr. Pharm. Design 2014, 20, 1715-1725.
71. Guise, A. J., Budayeva, H. G., Diner, B. A., Cristea, I. M., Histone deacetylases in herpesvirus replication and virus-stimulated host defense. Viruses 2013, 5, 1607-1632.
72. Bachman, K. E., Rountree, M. R., Baylin, S. B., Dnmt3a and Dnmt3b are transcriptional repressors that exhibit unique localization properties to heterochromatin. J. Biol. Chem. 2001, 276, 32282-32287.
73. Chen, T., Ueda, Y., Xie, S., Li, E., A novel Dnmt3a isoform produced from an alternative promoter localizes to euchromatin and its expression correlates with active de novo methylation. J. Biol. Chem. 2002, 277, 38746-38754.
74. Zhu, Y. Z., Zhu, R., Fan, J., Pan, Q. et al., Hepatitis B virus X protein induces hypermethylation of p16(INK4A) promoter via DNA methyltransferases in the early stage of HBV-associated hepatocarcinogenesis. J. Viral. Hepat. 2010, 17, 98-107.
75. Wei, X., Xiang, T., Ren, G., Tan, C. et al., miR-101 is down-regulated by the hepatitis B virus x protein and induces aberrant DNA methylation by targeting DNA methyltransferase 3A. Cell Signal. 2013, 25, 439-446.
76. Shamay, M., Krithivas, A., Zhang, J., Hayward, S. D., Recruitment of the de novo DNA methyltransferase Dnmt3a by Kaposi's sarcoma-associated herpesvirus LANA. Proc. Natl. Acad. Sci. USA 2006, 103, 14554-14559.
77. Brueckner, B., Garcia Boy, R., Siedlecki, P., Musch, T. et al., Epigenetic reactivation of tumor suppressor genes by a novel small-molecule inhibitor of human DNA methyltransferases. Cancer Res. 2005, 65, 6305-6311.
78. Stresemann, C., Brueckner, B., Musch, T., Stopper, H., Lyko, F., Functional diversity of DNA methyltransferase inhibitors in human cancer cell lines. Cancer Res. 2006, 66, 2794-2800.
79. Trus, B. L., Newcomb, W. W., Cheng, N., Cardone, G. et al., Allosteric signaling and a nuclear exit strategy: binding of UL25/UL17 heterodimers to DNA-filled HSV-1 capsids. Mol. Cell 2007, 26, 479-489.
80. Yamauchi, Y., Wada, K., Goshima, F., Takakuwa, H. et al., The UL14 protein of herpes simplex virus type 2 translocates the minor capsid protein VP26 and the DNA cleavage and packaging UL33 protein into the nucleus of coexpressing cells. J. Gen. Virol. 2001, 82, 321-330.
81. Topper, M., Luo, Y., Zhadina, M., Mohammed, K. et al., Posttranslational acetylation of the human immunodeficiency virus type 1 integrase carboxyl-terminal domain is dispensable for viral replication. J. Virol. 2007, 81, 3012-3017.
82. Terreni, M., Valentini, P., Liverani, V., Gutierrez, M. I. et al., GCN5-dependent acetylation of HIV-1 integrase enhances viral integration. Retrovirology 2010, 7, 18.
83. Cilia, M., Johnson, R., Sweeney, M., DeBlasio, S. L. et al., Evidence for lysine acetylation in the coat protein of a polerovirus. J. Gen. Virol. 2014, 95, 2321-2327.
84. Zheng, D. L., Zhang, L., Cheng, N., Xu, X. et al., Epigenetic modification induced by hepatitis B virus X protein via interaction with de novo DNA methyltransferase DNMT3A. J. Hepatol. 2009, 50, 377-387.
85. Zhao, Z., Wu, Q., Cheng, J., Qiu, X. et al., Depletion of DNMT3A suppressed cell proliferation and restored PTEN in hepatocellular carcinoma cell. J. Biomed. Biotechnol. 2010, 2010, 737535.
86. Wu, Z., Huang, K., Yu, J., Le, T. et al., Dnmt3a regulates both proliferation and differentiation of mouse neural stem cells. J. Neurosci. Res. 2012, 90, 1883-1891.
87. Xu, H., Sun, J., Shi, C., Sun, C. et al., miR-29s inhibit the malignant behavior of U87MG glioblastoma cell line by targeting DNMT3A and 3B. Neurosci. Lett. 2015, 590C, 40-46.
88. Li, J. Y., Pu, M. T., Hirasawa, R., Li, B. Z. et al., Synergistic function of DNA methyltransferases Dnmt3a and Dnmt3b in the methylation of Oct4 and Nanog. Mol. Cell. Biol. 2007, 27, 8748-8759.
89. Haney, S. L., Hlady, R. A., Opavska, J., Klinkebiel, D. et al., Methylation-independent repression of Dnmt3b contributes to oncogenic activity of Dnmt3a in mouse MYC-induced T-cell lymphomagenesis. Oncogene 2015, doi: 10.1038/onc.2014.472.
90. Challen, G. A., Sun, D., Mayle, A., Jeong, M. et al., Dnmt3a and Dnmt3b have overlapping and distinct functions in hematopoietic stem cells. Cell Stem Cell 2014, 15, 350-364.
91. Wu, J., Xu, Y., Mo, D., Huang, P. et al., Kaposi's sarcoma-associated herpesvirus (KSHV) vIL-6 promotes cell proliferation and migration by upregulating DNMT1 via STAT3 activation. PLoS One 2014, 9, e93478.