Visualization of DNA G-quadruplexes in herpes simplex virus 1-infected cells

Nucleic Acids Research

Volumn 44, Issue 21, 2016, Pages 10343-10353

  Artusi, Sara ^a   Perrone, Rosalba ^a   Lago, Sara ^a   Raffa, Paolo ^a   Di Iorio, Enzo ^a   Palù, Giorgio ^a   Richter, Sara N ^a  

^a UNIVERSITY OF PADOVA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBONUCLEASE; GUANINE QUADRUPLEX; INFECTED CELL PROTEIN 8; VIRUS DNA; MONOCLONAL ANTIBODY;

ANIMAL CELL; ARTICLE; CELL NUCLEUS; CELL NUCLEUS MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA DETERMINATION; DNA REPLICATION; DNA STRUCTURE; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; IMMUNOELECTRON MICROSCOPY; IMMUNOFLUORESCENCE; LATENT VIRUS INFECTION; MOUSE; NONHUMAN; PROTEIN PROCESSING; VIRUS REPLICATION; ANIMAL; CELL CULTURE; CELL LINE; CHEMISTRY; CHLOROCEBUS AETHIOPS; CONFOCAL MICROSCOPY; GENETICS; HERPES SIMPLEX; MOLECULAR IMAGING; PROCEDURES; ULTRASTRUCTURE; VERO CELL LINE; VIROLOGY;

ANIMALS; ANTIBODIES, MONOCLONAL; CELL LINE; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; DNA REPLICATION; DNA, VIRAL; G-QUADRUPLEXES; HERPES SIMPLEX; HERPESVIRUS 1, HUMAN; HUMANS; MICROSCOPY, CONFOCAL; MICROSCOPY, IMMUNOELECTRON; MOLECULAR IMAGING; VERO CELLS; VIRUS REPLICATION;

EID: 85013100383     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkw968     Document Type: Article

References (67)

1. Huppert, J.L. (2008) Four-stranded nucleic acids: structure, function and targeting of G-quadruplexes. Chem. Soc. Rev., 37, 1375-1384.
2. Eddy, J. and Maizels, N. (2006) Gene function correlates with potential for G4 DNA formation in the human genome. Nucleic Acids Res., 34, 3887-3896.
3. Huppert, J.L. and Balasubramanian, S. (2007) G-quadruplexes in promoters throughout the human genome. Nucleic Acids Res., 35, 406-413.
4. Nakken, S., Rognes, T. and Hovig, E. (2009) The disruptive positions in human G-quadruplex motifs are less polymorphic and more conserved than their neutral counterparts. Nucleic Acids Res., 37, 5749-5756.
5. Mani, P., Yadav, V.K., Das, S.K. and Chowdhury, S. (2009) Genome-wide analyses of recombination prone regions predict role of DNA structural motif in recombination. PLoS One, 4, e4399.
6. Rhodes, D. and Lipps, H.J. (2015) G-quadruplexes and their regulatory roles in biology. Nucleic Acids Res., 43, 8627-8637.
7. Biffi, G., Tannahill, D., McCafferty, J. and Balasubramanian, S. (2013) Quantitative visualization of DNA G-quadruplex structures in human cells. Nat. Chem., 5, 182-186.
8. Henderson, A., Wu, Y., Huang, Y.C., Chavez, E.A., Platt, J., Johnson, F.B., Brosh, R.M. Jr, Sen, D. and Lansdorp, P.M. (2014) Detection of G-quadruplex DNA in mammalian cells. Nucleic Acids Res., 42, 860-869.
9. Beaume, N., Pathak, R., Yadav, V.K., Kota, S., Misra, H.S., Gautam, H.K. and Chowdhury, S. (2013) Genome-wide study predicts promoter-G4 DNA motifs regulate selective functions in bacteria: radioresistance of D. radiodurans involves G4 DNA-mediated regulation. Nucleic Acids Res., 41, 76-89.
10. Du, X., Wojtowicz, D., Bowers, A.A., Levens, D., Benham, C.J. and Przytycka, T.M. (2013) The genome-wide distribution of non-B DNA motifs is shaped by operon structure and suggests the transcriptional importance of non-B DNA structures in Escherichia coli. Nucleic Acids Res., 41, 5965-5977.
11. Metifiot, M., Amrane, S., Litvak, S. and Andreola, M.L. (2014) G-quadruplexes in viruses: function and potential therapeutic applications. Nucleic Acids Res., 42, 12352-12366.
12. Amrane, S., Kerkour, A., Bedrat, A., Vialet, B., Andreola, M.L. and Mergny, J.L. (2014) Topology of a DNA G-quadruplex structure formed in the HIV-1 promoter: a potential target for anti-HIV drug development. J. Am. Chem. Soc., 136, 5249-5252.
13. Perrone, R., Nadai, M., Frasson, I., Poe, J.A., Butovskaya, E., Smithgall, T.E., Palumbo, M., Palu, G. and Richter, S.N. (2013) A dynamic G-quadruplex region regulates the HIV-1 long terminal repeat promoter. J. Med. Chem., 56, 6521-6530.
14. Piekna-Przybylska, D., Sullivan, M.A., Sharma, G. and Bambara, R.A. (2014) U3 region in the HIV-1 genome adopts a G-quadruplex structure in its RNA and DNA sequence. Biochemistry, 53, 2581-2593.
15. Perrone, R., Nadai, M., Poe, J.A., Frasson, I., Palumbo, M., Palu, G., Smithgall, T.E. and Richter, S.N. (2013) Formation of a unique cluster of G-quadruplex structures in the HIV-1 Nef coding region: implications for antiviral activity. PLoS One, 8, e73121.
16. Ouyang, Q., Zhao, X., Feng, H., Tian, Y., Li, D., Li, M. and Tan, Z. (2012) High GC content of simple sequence repeats in Herpes simplex virus type 1 genome. Gene, 499, 37-40.
17. Artusi, S., Nadai, M., Perrone, R., Biasolo, M.A., Palu, G., Flamand, L., Calistri, A. and Richter, S.N. (2015) The Herpes Simplex Virus-1 genome contains multiple clusters of repeated G-quadruplex: implications for the antiviral activity of a G-quadruplex ligand. Antiviral Res., 118, 123-131.
18. Honess, R.W. and Roizman, B. (1975) Regulation of herpesvirus macromolecular synthesis: sequential transition of polypeptide synthesis requires functional viral polypeptides. Proc. Natl. Acad. Sci. U.S.A., 72, 1276-1280.
19. Roizman, B., Knipe, D.M. and Whitley, R.J. (2013) Herpes Simplex Viruses. 6th edn. Lippincott Williams & Wilkins, Philadelphia, PA.
20. La Boissiere, S., Izeta, A., Malcomber, S. and O'Hare, P. (2004) Compartmentalization of VP16 in cells infected with recombinant herpes simplex virus expressing VP16-green fluorescent protein fusion proteins. J. Virol., 78, 8002-8014.
21. Hoffmann, R.F., Moshkin, Y.M., Mouton, S., Grzeschik, N.A., Kalicharan, R.D., Kuipers, J., Wolters, A.H., Nishida, K., Romashchenko, A.V., Postberg, J. et al. (2016) Guanine quadruplex structures localize to heterochromatin. Nucleic Acids Res., 44, 152-163.
22. Knipe, D.M., Senechek, D., Rice, S.A. and Smith, J.L. (1987) Stages in the nuclear association of the herpes simplex virus transcriptional activator protein ICP4. J. Virol., 61, 276-284.
23. Tosoni, E., Frasson, I., Scalabrin, M., Perrone, R., Butovskaya, E., Nadai, M., Palu, G., Fabris, D. and Richter, S.N. (2015) Nucleolin stabilizes G-quadruplex structures folded by the LTR promoter and silences HIV-1 viral transcription. Nucleic Acids Res., 43, 8884-8897.
24. Dai, J., Chen, D., Jones, R.A., Hurley, L.H. and Yang, D. (2006) NMR solution structure of the major G-quadruplex structure formed in the human BCL2 promoter region. Nucleic Acids Res., 34, 5133-5144
25. Kuryavyi, V., Phan, A.T. and Patel, D.J. (2010) Solution structures of all parallel-stranded monomeric and dimeric G-quadruplex scaffolds of the human c-kit2 promoter. Nucleic Acids Res., 38, 6757-6773.
26. Mathad, R.I., Hatzakis, E., Dai, J. and Yang, D. (2011) c-MYC promoter G-quadruplex formed at the 5'-end of NHE III1 element: insights into biological relevance and parallel-stranded G-quadruplex stability. Nucleic Acids Res., 39, 9023-9033.
27. Rankin, S., Reszka, A.P., Huppert, J., Zloh, M., Parkinson, G.N., Todd, A.K., Ladame, S., Balasubramanian, S. and Neidle, S. (2005) Putative DNA quadruplex formation within the human c-kit oncogene. J. Am. Chem. Soc., 127, 10584-10589.
28. Kumari, S., Bugaut, A., Huppert, J.L. and Balasubramanian, S. (2007) An RNA G-quadruplex in the 5' UTR of the NRAS proto-oncogene modulates translation. Nat. Chem. Biol., 3, 218-221.
29. Martadinata, H. and Phan, A.T. (2009) Structure of propeller-type parallel-stranded RNA G-quadruplexes, formed by human telomeric RNA sequences in K+ solution. J. Am. Chem. Soc., 131, 2570-2578.
30. Perrone, R., Butovskaya, E., Daelemans, D., Palu, G., Pannecouque, C. and Richter, S.N. (2014) Anti-HIV-1 activity of the G-quadruplex ligand BRACO-19. J. Antimicrob. Chemother., 69, 3248-3258.
31. Richter, S., Ping, Y.H. and Rana, T.M. (2002) TAR RNA loop: a scaffold for the assembly of a regulatory switch in HIV replication. Proc. Natl. Acad. Sci. U.S.A., 99, 7928-7933.
32. Lynch, H.E., Stewart, S.M., Kepler, T.B., Sempowski, G.D. and Alam, S.M. (2014) Surface plasmon resonance measurements of plasma antibody avidity during primary and secondary responses to anthrax protective antigen. J. Immunol. Methods, 404, 1-12.
33. Knipe, D.M. and Cliffe, A. (2008) Chromatin control of herpes simplex virus lytic and latent infection. Nat. Rev. Microbiol., 6, 211-221.
34. Lehman, I.R. and Boehmer, P.E. (1999) Replication of herpes simplex virus DNA. J. Biol. Chem., 274, 28059-28062.
35. Scott, E.S. and O'Hare, P. (2001) Fate of the inner nuclear membrane protein lamin B receptor and nuclear lamins in herpes simplex virus type 1 infection. J. Virol., 75, 8818-8830.
36. Simpson-Holley, M., Baines, J., Roller, R. and Knipe, D.M. (2004) Herpes simplex virus 1 U(L)31 and U(L)34 gene products promote the late maturation of viral replication compartments to the nuclear periphery. J. Virol., 78, 5591-5600.
37. James, S.H. and Prichard, M.N. (2014) Current and future therapies for herpes simplex virus infections: mechanism of action and drug resistance. Curr. Opin. Virol., 8C, 54-61.
38. Weller, S.K. and Coen, D.M. (2012) Herpes simplex viruses: mechanisms of DNA replication. Cold Spring Harb. Perspect. Biol., 4, a013011.
39. Honess, R.W. and Watson, D.H. (1977) Herpes simplex virus resistance and sensitivity to phosphonoacetic acid. J. Virol., 21, 584-600.
40. Brady, T., Agosto, L.M., Malani, N., Berry, C.C., O'Doherty, U. and Bushman, F. (2009) HIV integration site distributions in resting and activated CD4+ T cells infected in culture. Aids, 23, 1461-1471.
41. Liptak, L.M., Uprichard, S.L. and Knipe, D.M. (1996) Functional order of assembly of herpes simplex virus DNA replication proteins into prereplicative site structures. J. Virol., 70, 1759-1767.
42. Quinlan, M.P., Chen, L.B. and Knipe, D.M. (1984) The intranuclear location of a herpes simplex virus DNA-binding protein is determined by the status of viral DNA replication. Cell, 36, 857-868.
43. Taylor, T.J., McNamee, E.E., Day, C. and Knipe, D.M. (2003) Herpes simplex virus replication compartments can form by coalescence of smaller compartments. Virology, 309, 232-247.
44. de Bruyn Kops, A and Knipe, D.M. (1988) Formation of DNA replication structures in herpes virus-infected cells requires a viral DNA binding protein. Cell, 55, 857-868.
45. Adler, J. and Parmryd, I. (2010) Quantifying colocalization by correlation: the Pearson correlation coefficient is superior to the Mander's overlap coefficient. Cytometry A, 77, 733-742.
46. Leuzinger, H., Ziegler, U., Schraner, E.M., Fraefel, C., Glauser, D.L., Heid, I., Ackermann, M., Mueller, M. and Wild, P. (2005) Herpes simplex virus 1 envelopment follows two diverse pathways. J. Virol., 79, 13047-13059.
47. Wild, P., Leisinger, S., de Oliveira, A.P., Schraner, E.M., Kaech, A., Ackermann, M. and Tobler, K. (2015) Herpes simplex virus 1 Us3 deletion mutant is infective despite impaired capsid translocation to the cytoplasm. Viruses, 7, 52-71.
48. Myllys, M., Ruokolainen, V., Aho, V., Smith, E.A., Hakanen, S., Peri, P., Salvetti, A., Timonen, J., Hukkanen, V., Larabell, C.A. et al. (2016) Herpes simplex virus 1 induces egress channels through marginalized host chromatin. Sci. Rep., 6, 28844.
49. Maizels, N. (2006) Dynamic roles for G4 DNA in the biology of eukaryotic cells. Nat. Struct. Mol. Biol., 13, 1055-1059.
50. Duquette, M.L., Handa, P., Vincent, J.A., Taylor, A.F. and Maizels, N. (2004) Intracellular transcription of G-rich DNAs induces formation of G-loops, novel structures containing G4 DNA. Genes Dev., 18, 1618-1629.
51. Cheung, I., Schertzer, M., Rose, A. and Lansdorp, P.M. (2002) Disruption of dog-1 in Caenorhabditis elegans triggers deletions upstream of guanine-rich DNA. Nat. Genet., 31, 405-409.
52. van Kregten, M. and Tijsterman, M. (2014) The repair of G-quadruplex-induced DNA damage. Exp. Cell Res., 329, 178-183.
53. Miyoshi, D., Matsumura, S., Nakano, S. and Sugimoto, N. (2004) Duplex dissociation of telomere DNAs induced by molecular crowding. J. Am. Chem. Soc., 126, 165-169.
54. Hobbs, W.E. 2nd and DeLuca, N.A. (1999) Perturbation of cell cycle progression and cellular gene expression as a function of herpes simplex virus ICP0. J. Virol., 73, 8245-8255.
55. Ebert, S.N., Subramanian, D., Shtrom, S.S., Chung, I.K., Parris, D.S. and Muller, M.T. (1994) Association between the p170 form of human topoisomerase II and progeny viral DNA in cells infected with herpes simplex virus type 1. J. Virol., 68, 1010-1020.
56. Hammarsten, O., Yao, X. and Elias, P. (1996) Inhibition of topoisomerase II by ICRF-193 prevents efficient replication of herpes simplex virus type 1. J. Virol., 70, 4523-4529.
57. Everett, R.D. (1985) Activation of cellular promoters during herpes virus infection of biochemically transformed cells. EMBO J., 4, 1973-1980.
58. Deng, Z., Kim, E.T., Vladimirova, O., Dheekollu, J., Wang, Z., Newhart, A., Liu, D., Myers, J.L., Hensley, S.E., Moffat, J. et al. (2014) HSV-1 remodels host telomeres to facilitate viral replication. Cell Rep., 9, 2263-2278.
59. Bush, M., Yager, D.R., Gao, M., Weisshart, K., Marcy, A.I., Coen, D.M. and Knipe, D.M. (1991) Correct intranuclear localization of herpes simplex virus DNA polymerase requires the viral ICP8 DNA-binding protein. J. Virol., 65, 1082-1089.
60. de Bruyn Kops, A and Knipe, D.M. (1994) Preexisting nuclear architecture defines the intranuclear location of herpesvirus DNA replication structures. J. Virol., 68, 3512-3526.
61. de Bruyn Kops, A, Uprichard, S.L., Chen, M. and Knipe, D.M. (1998) Comparison of the intranuclear distributions of herpes simplex virus proteins involved in various viral functions. Virology, 252, 162-178.
62. Sawtell, N.M., Poon, D.K., Tansky, C.S. and Thompson, R.L. (1998) The latent herpes simplex virus type 1 genome copy number in individual neurons is virus strain specific and correlates with reactivation. J. Virol., 72, 5343-5350.
63. Schiffer, J.T., Abu-Raddad, L., Mark, K.E., Zhu, J., Selke, S., Koelle, D.M., Wald, A. and Corey, L. (2010) Mucosal host immune response predicts the severity and duration of herpes simplex virus-2 genital tract shedding episodes. Proc. Natl. Acad. Sci. U.S.A., 107, 18973-18978.
64. Orvedahl, A., Alexander, D., Talloczy, Z., Sun, Q., Wei, Y., Zhang, W., Burns, D., Leib, D.A. and Levine, B. (2007) HSV-1 ICP34.5 confers neurovirulence by targeting the Beclin 1 autophagy protein. Cell Host Microbe, 1, 23-35.
65. Vere Hodge, R.A. and Field, H.J. (2013) Antiviral agents for herpes simplex virus. Adv. Pharmacol., 67, 1-38.
66. Bacon, T.H., Levin, M.J., Leary, J.J., Sarisky, R.T. and Sutton, D. (2003) Herpes simplex virus resistance to acyclovir and penciclovir after two decades of antiviral therapy. Clin. Microbiol. Rev., 16, 114-128.
67. Perrone, R., Doria, F., Butovskaya, E., Frasson, I., Botti, S., Scalabrin, M., Lago, S., Grande, V., Nadai, M., Freccero, M. et al. (2015) Synthesis, binding and antiviral properties of potent core-extended naphthalene diimides targeting the HIV-1 long terminal repeat promoter G-quadruplexes. J. Med. Chem., 58, 9639-9652.