Single molecule analysis of replicated DNA reveals the usage of multiple KSHV genome regions for latent replication

PLoS Pathogens

Volumn 7, Issue 11, 2011, Pages

  Verma, Subhash C ^a   Lu, Jie ^b   Cai, Qiliang ^b   Kosiyatrakul, Settapong ^c   McDowell, Maria E ^a   Schildkraut, Carl L ^c   Robertson, Erle S ^b  

^a UNIVERSITY OF NEVADA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SINGLE MOLECULE ANALYSIS OF REPLICATED DNA; UNCLASSIFIED DRUG; VIRUS DNA; CELL CYCLE PROTEIN; DNA BINDING PROTEIN; LATENCY ASSOCIATED NUCLEAR ANTIGEN; LATENCY-ASSOCIATED NUCLEAR ANTIGEN; MCM3 PROTEIN, HUMAN; NUCLEAR PROTEIN; ORC2 PROTEIN, HUMAN; ORIGIN RECOGNITION COMPLEX; VIRUS ANTIGEN;

ANIMAL CELL; ARTICLE; CELL CYCLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA DETERMINATION; DNA MODIFICATION; DNA REPLICATION; DNA SEQUENCE; GENE DUPLICATION; HUMAN HERPESVIRUS 8; LATENT PERIOD; LONG TERMINAL REPEAT; NONHUMAN; NUCLEOTIDE SEQUENCE; VIRUS GENOME; VIRUS REPLICATION; VIRUS STRAIN; BIOSYNTHESIS; CHEMISTRY; DNA REPLICATION ORIGIN; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE; VIRUS LATENCY;

HUMAN HERPESVIRUS 8;

ANTIGENS, VIRAL; CELL CYCLE; CELL CYCLE PROTEINS; CELL LINE, TUMOR; CHROMATIN IMMUNOPRECIPITATION; DNA REPLICATION; DNA, VIRAL; DNA-BINDING PROTEINS; GENOME, VIRAL; HERPESVIRUS 8, HUMAN; HUMANS; NUCLEAR PROTEINS; ORIGIN RECOGNITION COMPLEX; REPLICATION ORIGIN; VIRUS LATENCY; VIRUS REPLICATION;

EID: 81755187238     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002365     Document Type: Article

References (61)

1. Verma SC, Robertson ES, (2003) Molecular biology and pathogenesis of Kaposi sarcoma-associated herpesvirus. FEMS Microbiol Lett 222: 155-163.
2. Moore PS, Chang Y, (2003) Kaposi's sarcoma-associated herpesvirus immunoevasion and tumorigenesis: two sides of the same coin? Annu Rev Microbiol 57: 609-639.
3. Chang Y, Cesarman E, Pessin MS, Lee F, Culpepper J, et al. (1994) Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma. Science 266: 1865-1869.
4. Renne R, Lagunoff M, Zhong W, Ganem D, (1996) The size and conformation of Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) DNA in infected cells and virions. J Virol 70: 8151-8154.
5. Cotter MA 2nd, Robertson ES, (1999) The latency-associated nuclear antigen tethers the Kaposi's sarcoma-associated herpesvirus genome to host chromosomes in body cavity-based lymphoma cells. Virology 264: 254-264.
6. Ballestas ME, Chatis PA, Kaye KM, (1999) Efficient persistence of extrachromosomal KSHV DNA mediated by latency-associated nuclear antigen. Science 284: 641-644.
7. Zhong W, Wang H, Herndier B, Ganem D, (1996) Restricted expression of Kaposi sarcoma-associated herpesvirus (human herpesvirus 8) genes in Kaposi sarcoma. Proc Natl Acad Sci U S A 93: 6641-6646.
8. Means RE, Choi JK, Nakamura H, Chung YH, Ishido S, et al. (2002) Immune evasion strategies of Kaposi's sarcoma-associated herpesvirus. Curr Top Microbiol Immunol 269: 187-201.
9. Liang C, Lee JS, Jung JU, (2008) Immune evasion in Kaposi's sarcoma-associated herpes virus associated oncogenesis. Semin Cancer Biol 18: 423-436.
10. Rainbow L, Platt GM, Simpson GR, Sarid R, Gao SJ, et al. (1997) The 222- to 234-kilodalton latent nuclear protein (LNA) of Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) is encoded by orf73 and is a component of the latency-associated nuclear antigen. J Virol 71: 5915-5921.
11. Renne R, Blackbourn D, Whitby D, Levy J, Ganem D, (1998) Limited transmission of Kaposi's sarcoma-associated herpesvirus in cultured cells. J Virol 72: 5182-5188.
12. Flore O, Rafii S, Ely S, O'Leary JJ, Hyjek EM, et al. (1998) Transformation of primary human endothelial cells by Kaposi's sarcoma-associated herpesvirus. Nature 394: 588-592.
13. Friborg J Jr, Kong W, Hottiger MO, Nabel GJ, (1999) p53 inhibition by the LANA protein of KSHV protects against cell death. Nature 402: 889-894.
14. Moore PS, Chang Y, (1998) Kaposi's sarcoma-associated herpesvirus-encoded oncogenes and oncogenesis. J Natl Cancer Inst Monogr pp. 65-71.
15. Fujimuro M, Wu FY, ApRhys C, Kajumbula H, Young DB, et al. (2003) A novel viral mechanism for dysregulation of beta-catenin in Kaposi's sarcoma-associated herpesvirus latency. Nat Med 9: 300-306.
16. Cai Q, Murakami M, Si H, Robertson ES, (2007) A potential alpha-helix motif in the amino terminus of LANA encoded by Kaposi's sarcoma-associated herpesvirus is critical for nuclear accumulation of HIF-1alpha in normoxia. J Virol 81: 10413-10423.
17. Borah S, Verma SC, Robertson ES, (2004) ORF73 of herpesvirus saimiri, a viral homolog of Kaposi's sarcoma-associated herpesvirus, modulates the two cellular tumor suppressor proteins p53 and pRb. J Virol 78: 10336-10347.
18. Radkov SA, Kellam P, Boshoff C, (2000) The latent nuclear antigen of Kaposi sarcoma-associated herpesvirus targets the retinoblastoma-E2F pathway and with the oncogene Hras transforms primary rat cells. Nat Med 6: 1121-1127.
19. Verma SC, Borah S, Robertson ES, (2004) Latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus up-regulates transcription of human telomerase reverse transcriptase promoter through interaction with transcription factor Sp1. J Virol 78: 10348-10359.
20. Ye FC, Zhou FC, Yoo SM, Xie JP, Browning PJ, et al. (2004) Disruption of Kaposi's sarcoma-associated herpesvirus latent nuclear antigen leads to abortive episome persistence. J Virol 78: 11121-11129.
21. Barbera AJ, Chodaparambil JV, Kelley-Clarke B, Joukov V, Walter JC, et al. (2006) The nucleosomal surface as a docking station for Kaposi's sarcoma herpesvirus LANA. Science 311: 856-861.
22. Cotter MA 2nd, Subramanian C, Robertson ES, (2001) The Kaposi's sarcoma-associated herpesvirus latency-associated nuclear antigen binds to specific sequences at the left end of the viral genome through its carboxy-terminus. Virology 291: 241-259.
23. Hu J, Garber AC, Renne R, (2002) The latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus supports latent DNA replication in dividing cells. J Virol 76: 11677-11687.
24. Hu J, Renne R, (2005) Characterization of the minimal replicator of Kaposi's sarcoma-associated herpesvirus latent origin. J Virol 79: 2637-2642.
25. Lagunoff M, Ganem D, (1997) The structure and coding organization of the genomic termini of Kaposi's sarcoma-associated herpesvirus. Virology 236: 147-154.
26. Verma SC, Choudhuri T, Robertson ES, (2007) The minimal replicator element of the Kaposi's sarcoma-associated herpesvirus terminal repeat supports replication in a semiconservative and cell-cycle-dependent manner. J Virol 81: 3402-3413.
27. Garber AC, Shu MA, Hu J, Renne R, (2001) DNA binding and modulation of gene expression by the latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus. J Virol 75: 7882-7892.
28. Ballestas ME, Kaye KM, (2001) Kaposi's sarcoma-associated herpesvirus latency-associated nuclear antigen 1 mediates episome persistence through cis-acting terminal repeat (TR) sequence and specifically binds TR DNA. J Virol 75: 3250-3258.
29. Yates JL, Camiolo SM, Bashaw JM, (2000) The minimal replicator of Epstein-Barr virus oriP. J Virol 74: 4512-4522.
30. Dhar SK, Yoshida K, Machida Y, Khaira P, Chaudhuri B, et al. (2001) Replication from oriP of Epstein-Barr virus requires human ORC and is inhibited by geminin. Cell 106: 287-296.
31. Schepers A, Ritzi M, Bousset K, Kremmer E, Yates JL, et al. (2001) Human origin recognition complex binds to the region of the latent origin of DNA replication of Epstein-Barr virus. EMBO J 20: 4588-4602.
32. Chaudhuri B, Xu H, Todorov I, Dutta A, Yates JL, (2001) Human DNA replication initiation factors, ORC and MCM, associate with oriP of Epstein-Barr virus. Proc Natl Acad Sci U S A 98: 10085-10089.
33. Verma SC, Choudhuri T, Kaul R, Robertson ES, (2006) Latency-associated nuclear antigen (LANA) of Kaposi's sarcoma-associated herpesvirus interacts with origin recognition complexes at the LANA binding sequence within the terminal repeats. J Virol 80: 2243-2256.
34. Stedman W, Deng Z, Lu F, Lieberman PM, (2004) ORC, MCM, and histone hyperacetylation at the Kaposi's sarcoma-associated herpesvirus latent replication origin. J Virol 78: 12566-12575.
35. Blow JJ, Hodgson B, (2002) Replication licensing-defining the proliferative state? Trends Cell Biol 12: 72-78.
36. Verma SC, Lan K, Choudhuri T, Cotter MA, Robertson ES, (2007) An autonomous replicating element within the KSHV genome. Cell Host Microbe 2: 106-118.
37. Norio P, Schildkraut CL, (2001) Visualization of DNA replication on individual Epstein-Barr virus episomes. Science 294: 2361-2364.
38. Norio P, Schildkraut CL, (2004) Plasticity of DNA replication initiation in Epstein-Barr virus episomes. PLoS Biol 2: e152.
39. Sfeir A, Kosiyatrakul ST, Hockemeyer D, MacRae SL, Karlseder J, et al. (2009) Mammalian telomeres resemble fragile sites and require TRF1 for efficient replication. Cell 138: 90-103.
40. Guan Z, Hughes CM, Kosiyatrakul S, Norio P, Sen R, et al. (2009) Decreased replication origin activity in temporal transition regions. J Cell Biol 187: 623-635.
41. Aladjem MI, (2007) Replication in context: dynamic regulation of DNA replication patterns in metazoans. Nat Rev Genet 8: 588-600.
42. Machida YJ, Hamlin JL, Dutta A, (2005) Right place, right time, and only once: replication initiation in metazoans. Cell 123: 13-24.
43. Takeda DY, Shibata Y, Parvin JD, Dutta A, (2005) Recruitment of ORC or CDC6 to DNA is sufficient to create an artificial origin of replication in mammalian cells. Genes Dev 19: 2827-2836.
44. Blow JJ, Dutta A, (2005) Preventing re-replication of chromosomal DNA. Nat Rev Mol Cell Biol 6: 476-486.
45. Stillman B, (2005) Origin recognition and the chromosome cycle. FEBS Lett 579: 877-884.
46. Bell SP, Dutta A, (2002) DNA replication in eukaryotic cells. Annu Rev Biochem 71: 333-374.
47. Mizushima T, Takahashi N, Stillman B, (2000) Cdc6p modulates the structure and DNA binding activity of the origin recognition complex in vitro. Genes Dev 14: 1631-1641.
48. DePamphilis ML, (2005) Cell cycle dependent regulation of the origin recognition complex. Cell Cycle 4: 70-79.
49. Dutta A, Bell SP, (1997) Initiation of DNA replication in eukaryotic cells. Annu Rev Cell Dev Biol 13: 293-332.
50. Cai Q, Verma SC, Lu J, Robertson ES, (2010) Molecular biology of Kaposi's sarcoma-associated herpesvirus and related oncogenesis. Adv Virus Res 78: 87-142.
51. Verma SC, Lan K, Robertson E, (2007) Structure and function of latency-associated nuclear antigen. Curr Top Microbiol Immunol 312: 101-136.
52. Godfrey A, Anderson J, Papanastasiou A, Takeuchi Y, Boshoff C, (2005) Inhibiting primary effusion lymphoma by lentiviral vectors encoding short hairpin RNA. Blood 105: 2510-2518.
53. Komatsu T, Ballestas ME, Barbera AJ, Kelley-Clarke B, Kaye KM, (2004) KSHV LANA1 binds DNA as an oligomer and residues N-terminal to the oligomerization domain are essential for DNA binding, replication, and episome persistence. Virology 319: 225-236.
54. Boehmer PE, Lehman IR, (1997) Herpes simplex virus DNA replication. Annu Rev Biochem 66: 347-384.
55. Vogelauer M, Rubbi L, Lucas I, Brewer BJ, Grunstein M, (2002) Histone acetylation regulates the time of replication origin firing. Mol Cell 10: 1223-1233.
56. Toth Z, Maglinte DT, Lee SH, Lee HR, Wong LY, et al. (2010) Epigenetic analysis of KSHV latent and lytic genomes. PLoS Pathog 6: e1001013.
57. Wei X, Samarabandu J, Devdhar RS, Siegel AJ, Acharya R, et al. (1998) Segregation of transcription and replication sites into higher order domains. Science 281: 1502-1506.
58. Pomerantz RT, O'Donnell M, (2008) The replisome uses mRNA as a primer after colliding with RNA polymerase. Nature 456: 762-766.
59. Schultz SS, Desbordes SC, Du Z, Kosiyatrakul S, Lipchina I, et al. (2010) Single-molecule analysis reveals changes in the DNA replication program for the POU5F1 locus upon human embryonic stem cell differentiation. Mol Cell Biol 30: 4521-4534.
60. Ritzi M, Tillack K, Gerhardt J, Ott E, Humme S, et al. (2003) Complex protein-DNA dynamics at the latent origin of DNA replication of Epstein-Barr virus. J Cell Sci 116: 3971-3984.
61. Verma SC, Lan K, Choudhuri T, Robertson ES, (2006) Kaposi's sarcoma-associated herpesvirus-encoded latency-associated nuclear antigen modulates K1 expression through its cis-acting elements within the terminal repeats. J Virol 80: 3445-3458.