Small RNA profiling reveals antisense transcription throughout the KSHV genome and novel small RNAs

RNA

Volumn 16, Issue 8, 2010, Pages 1540-1558

  Lin, Yao Tang ^a   Kincaid, Rodney P ^a   Arasappan, Dhivya ^a   Dowd, Scot E ^b   Hunicke Smith, Scott P ^a   Sullivan, Christopher S ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b Research and Testing Laboratory   (United States)

Author keywords

Antisense; Kaposi's sarcoma associated herpesvirus (KSHV); MicroRNA (miRNA); microRNA offset RNAs (moRNAs)

Indexed keywords

COMPLEMENTARY RNA; DOUBLE STRANDED RNA; MICRORNA; SMALL INTERFERING RNA; VIRUS RNA;

ARTICLE; CONTROLLED STUDY; GENOME; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 8; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; RNA ANALYSIS; RNA SEQUENCE; RNA TRANSCRIPTION; VIRUS INFECTION; VIRUS REPLICATION;

BASE SEQUENCE; GENES, VIRAL; GENOME; HERPESVIRUS 8, HUMAN; HUMANS; MICRORNAS; OPEN READING FRAMES; RNA; RNA, DOUBLE-STRANDED; RNA, UNTRANSLATED; RNA, VIRAL;

HUMAN HERPESVIRUS 8;

EID: 77955098309     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.1967910     Document Type: Article

References (84)

1. Applied Biosystems . 2009. Whole-genome discovery and profiling of small RNAs using the SOLiD System. BioTechniques 46: 232-234.
2. Areste C, Blackbourn DJ. 2009. Modulation of the immune system by Kaposi's sarcoma-associated herpesvirus. Trends Microbiol 17: 119-129.
3. Arias C, Walsh D, Harbell J, Wilson AC, Mohr I. 2009. Activation of host translational control pathways by a viral developmental switch. PLoS Pathog 5: e1000334. doi: 10.1371/journal.ppat.1000334.
4. Babiarz JE, Ruby JG, Wang Y, Bartel DP, Blelloch R. 2008. Mouse ES cells express endogenous shRNAs, siRNAs, and other Microprocessor- independent, Dicer-dependent small RNAs. Genes Dev 22: 2773-2785.
5. Bartel DP. 2004. MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 116: 281-297.
6. Birney E, Stamatoyannopoulos JA, Dutta A, Guigo R, Gingeras TR, Margulies EH, Weng Z, Snyder M, Dermitzakis ET, Thurman RE, et al. 2007. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447: 799-816.
7. Bisson SA, Page AL, Ganem D. 2009. A Kaposi's sarcoma-associated herpesvirus protein that forms inhibitory complexes with type I interferon receptor subunits, Jak and STAT proteins, and blocks interferon-mediated signal transduction. J Virol 83: 5056-5066.
8. Buck AH, Santoyo-Lopez J, Robertson KA, Kumar DS, Reczko M, Ghazal P. 2007. Discrete clusters of virus-encoded micrornas are associated with complementary strands of the genome and the 7.2-kilobase stable intron in murine cytomegalovirus. J Virol 81: 13761-13770.
9. Burnside J, Bernberg E, Anderson A, Lu C, Meyers BC, Green PJ, Jain N, Isaacs G, Morgan RW. 2006. Marek's disease virus encodes microRNAs that map to meq and the latency-associated transcript. J Virol 80: 8778-8786.
10. Cai X, Cullen BR. 2006. Transcriptional origin of Kaposi's sarcomaassociated herpesvirus microRNAs. J Virol 80: 2234-2242.
11. Cai X, Lu S, Zhang Z, Gonzalez CM, Damania B, Cullen BR. 2005. Kaposi's sarcoma-associated herpesvirus expresses an array of viral microRNAs in latently infected cells. Proc Natl Acad Sci 102: 5570-5575.
12. Cai X, Schafer A, Lu S, Bilello JP, Desrosiers RC, Edwards R, Raab-Traub N, Cullen BR. 2006. Epstein-Barr virus microRNAs are evolutionarily conserved and differentially expressed. PLoS Pathog 2: e23. doi: 10.1371/journal.ppat. 0020023.
13. Carthew RW, Sontheimer EJ. 2009. Origins and mechanisms of miRNAs and siRNAs. Cell 136: 642-655.
14. Chang PJ, Shedd D, Gradoville L, Cho MS, Chen LW, Chang J, Miller G. 2002. Open reading frame 50 protein of Kaposi's sarcoma-associated herpesvirus directly activates the viral PAN and K12 genes by binding to related response elements. J Virol 76: 3168-3178.
15. Chendrimada TP, Gregory RI, Kumaraswamy E, Norman J, Cooch N, Nishikura K, Shiekhattar R. 2005. TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing. Nature 436: 740-744.
16. Coscoy L. 2007. Immune evasion by Kaposi's sarcoma-associated herpesvirus. Nat Rev Immunol 7: 391-401.
17. Cui C, Griffiths A, Li G, Silva LM, Kramer MF, Gaasterland T, Wang XJ, Coen DM. 2006. Prediction and identification of herpes simplex virus 1-encoded microRNAs. J Virol 80: 5499-5508.
18. Cullen BR. 2004. Transcription and processing of human microRNA precursors. Mol Cell 16: 861-865.
19. Cullen BR. 2006. Is RNA interference involved in intrinsic antiviral immunity in mammals? Nat Immunol 7: 563-567.
20. Cullen BR. 2009. Viral and cellular messenger RNA targets of viral microRNAs. Nature 457: 421-425.
21. Denli AM, Tops BB, Plasterk RH, Ketting RF, Hannon GJ. 2004. 2004. Processing of primary microRNAs by the Microprocessor complex. Nature 432: 231-235.
22. Ding SW, Voinnet O. 2007. Antiviral immunity directed by small RNAs. Cell 130: 413-426.
23. Dolken L, Perot J, Cognat V, Alioua A, John M, Soutschek J, Ruzsics Z, Koszinowski U, Voinnet O, Pfeffer S. 2007. Mouse cytomegalovirus microRNAs dominate the cellular small RNA profile during lytic infection and show features of posttranscriptional regulation. J Virol 81: 13771-13782.
24. Dunn W, Trang P, Zhong Q, Yang E, van Belle C, Liu F. 2005. Human cytomegalovirus expresses novel microRNAs during productive viral infection. Cell Microbiol 7: 1684-1695.
25. Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T. 2001. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411: 494-498.
26. Ganem D. 2007. Kaposi's sarcoma-associated herpesvirus. In Fields virology (ed. DM Knipe and PM Howley), 5th ed., pp. 2875-2888. Lippincott Williams & Wilkins, Philadelphia.
27. Gitlin L, Karelsky S, Andino R. 2002. Short interfering RNA confers intracellular antiviral immunity in human cells. Nature 418: 430-434.
28. Gottwein E, Cullen BR. 2008. Viral and cellular microRNAs as determinants of viral pathogenesis and immunity. Cell Host Microbe 3: 375-387. (Pubitemid 351773098)
29. Gottwein E, Cai X, Cullen BR. 2006. A novel assay for viral microRNA function identifies a single nucleotide polymorphism that affects Drosha processing. J Virol 80: 5321-5326.
30. Gottwein E, Mukherjee N, Sachse C, Frenzel C, Majoros WH, Chi JT, Braich R, Manoharan M, Soutschek J, Ohler U, et al. 2007. A viral microRNA functions as an orthologue of cellular miR-155. Nature 450: 1096-1099.
31. Gregory RI, Yan KP, Amuthan G, Chendrimada T, Doratotaj B, Cooch N, Shiekhattar R. 2004. The Microprocessor complex mediates the genesis of microRNAs. Nature 432: 235-240. (Pubitemid 39545855)
32. Grey F, Antoniewicz A, Allen E, Saugstad J, McShea A, Carrington JC, Nelson J. 2005. Identification and characterization of human cytomegalovirus-encoded microRNAs. J Virol 79: 12095-12099. (Pubitemid 41279327)
33. Grey F, Meyers H, White EA, Spector DH, Nelson J. 2007. A human cytomegalovirus-encoded microRNA regulates expression of multiple viral genes involved in replication. PLoS Pathog 3: e163. doi: 10.1371/journal.ppat.0030163.
34. Grey F, Hook L, Nelson J. 2008. The functions of herpesvirus-encoded microRNAs. Med Microbiol Immunol 197: 261-267.
35. Griffiths-Jones S. 2006. miRBase: The microRNA sequence database. Methods Mol Biol 342: 129-138.
36. Grundhoff A, Sullivan CS, Ganem D. 2006. A combined computational and microarray-based approach identifies novel micro- RNAs encoded by human gamma-herpesviruses. RNA 12:733-750.
37. Hussain M, Taft RJ, Asgari S. 2008. An insect virus-encoded micro-RNA regulates viral replication. J Virol 82: 9164-9170.
38. Kim VN. 2005. MicroRNA biogenesis: Coordinated cropping and dicing. Nat Rev Mol Cell Biol 6: 376-385.
39. Langenberger D, Bermudez-Santana C, Hertel J, Hoffmann S, Khaitovich P, Stadler PF. 2009. Evidence for human microRNA-offset RNAs in small RNA sequencing data. Bioinformatics 25: 2298-2301.
40. Lee HR, Kim MH, Lee JS, Liang C, Jung JU. 2009. Viral interferon regulatory factors. J Interferon Cytokine Res 29: 621-627.
41. Li Z, Kim SW, Lin Y, Moore PS, Chang Y, John B. 2009. Characterization of viral and human RNAs smaller than canonical microRNAs. J Virol 83: 12751-12758.
42. Linsen SE, de Wit E, Janssens G, Heater S, Chapman L, Parkin RK, Fritz B, Wyman SK, de Bruijn E, Voest EE, et al. 2009. Limitations and possibilities of small RNA digital gene expression profiling. Nat Methods 6: 474-476.
43. Lukac DM, Kirshner JR, Ganem D. 1999. Transcriptional activation by the product of open reading frame 50 of Kaposi's sarcoma-associated herpesvirus is required for lytic viral reactivation in B cells. J Virol 73: 9348-9361.
44. Maeda N, Kasukawa T, Oyama R, Gough J, Frith M, Engstrom PG, Lenhard B, Aturaliya RN, Batalov S, Beisel KW, et al. 2006. Transcript annotation in FANTOM3: mouse gene catalog based on physical cDNAs. PLoS Genet 2: e62. doi: 10.1371/journal.pgen.0020062.
45. Maran A, Mathews MB. 1988. Characterization of the double-stranded RNA implicated in the inhibition of protein synthesis in cells infected with a mutant adenovirus defective for VA RNA. Virology 164: 106-113.
46. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA, Berka J, Braverman MS, Chen YJ, Chen Z, et al. 2005. Genome sequencing in microfabricated high-density picolitre reactors. Nature 437: 376-380.
47. Marshall V, Parks T, Bagni R, Wang CD, Samols MA, Hu J, Wyvil KM, Aleman K, Little RF, Yarchoan R, et al. 2007. Conservation of virally encoded microRNAs in Kaposi sarcoma-associated herpesvirus in primary effusion lymphoma cell lines and in patients with Kaposi sarcoma or multicentric Castleman disease. J Infect Dis 195: 645-659.
48. Mathews DH, Sabina J, Zuker M, Turner DH. 1999. Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J Mol Biol 288: 911-940. (Pubitemid 29248642)
49. Mattick JS, Makunin IV. 2006. Noncoding RNA. Hum Mol Genet 15: R17-R29.
50. Murphy E, Vanicek J, Robins H, Shenk T, Levine AJ. 2008. Suppression of immediate-early viral gene expression by herpesvirus- coded microRNAs: Implications for latency. Proc Natl Acad Sci 105: 5453-5458.
51. Nair V, Zavolan M. 2006. Virus-encoded microRNAs: Novel regulators of gene expression. Trends Microbiol 14: 169-175.
52. Nakamura H, Lu M, Gwack Y, Souvlis J, Zeichner SL, Jung JU. 2003. Global changes in Kaposi's sarcoma-associated virus gene expression patterns following expression of a tetracycline-inducible Rta transactivator. J Virol 77: 4205-4220. (Pubitemid 36350959)
53. Pearce M, Matsumura S, Wilson AC. 2005. Transcripts encoding K12, v-FLIP, v-cyclin, and the microRNA cluster of Kaposi's sarcoma-associated herpesvirus originate from a common promoter. J Virol 79: 14457-14464. (Pubitemid 41552745)
54. Pfeffer S. 2008. Viral miRNAs: Tiny but mighty helpers for large and small DNA viruses. Future Virol 3: 291-298. (Pubitemid 351720410)
55. Pfeffer S, Zavolan M, Grasser FA, Chien M, Russo JJ, Ju J, John B, Enright AJ, Marks D, Sander C, et al. 2004. Identification of virus-encoded microRNAs. Science 304: 734-736.
56. Pfeffer S, Sewer A, Lagos-Quintana M, Sheridan R, Sander C, Grasser FA, van Dyk LF, Ho CK, Shuman S, Chien M, et al. 2005. Identification of microRNAs of the herpesvirus family. Nat Methods 2: 269-276.
57. Renne R, Zhong W, Herndier B, McGrath M, Abbey N, Kedes D, Ganem D. 1996. Lytic growth of Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) in culture. Nat Med 2: 342-346. (Pubitemid 26080656)
58. Russo JJ, Bohenzky RA, Chien MC, Chen J, Yan M, Maddalena D, Parry JP, Peruzzi D, Edelman IS, Chang Y, et al. 1996. Nucleotide sequence of the Kaposi sarcoma-associated herpesvirus (HHV8). Proc Natl Acad Sci 93: 14862-14867.
59. Sadler R, Wu L, Forghani B, Renne R, Zhong W, Herndier B, Ganem D. 1999. A complex translational program generates multiple novel proteins from the latently expressed kaposin (K12) locus of Kaposi's sarcoma-associated herpesvirus. J Virol 73: 5722-5730. (Pubitemid 29274858)
60. Samols MA, Renne R. 2006. Virus-encoded microRNAs: A new chapter in virus-host cell interactions. Future Virol 1: 233-242.
61. Samols MA, Hu J, Skalsky RL, Renne R. 2005. Cloning and identification of a microRNA cluster within the latency-associated region of Kaposi's sarcoma-associated herpesvirus. J Virol 79: 9301-9305. (Pubitemid 40934841)
62. Samols MA, Skalsky RL, Maldonado AM, Riva A, Lopez MC, Baker HV, Renne R. 2007. Identification of cellular genes targeted by KSHV-encoded microRNAs. PLoS Pathog 3: e65. doi: 10.1371/journal.ppat.0030065.
63. Sarnow P, Jopling CL, Norman KL, Schutz S, Wehner KA. 2006. MicroRNAs: Expression, avoidance and subversion by vertebrate viruses. Nat Rev Microbiol 4: 651-659.
64. Saveliev A, Zhu F, Yuan Y. 2002. Transcription mapping and expression patterns of genes in the major immediate-early region of Kaposi's sarcoma-associated herpesvirus. Virology 299: 301-314.
65. Seitz H, Zamore PD. 2006. Rethinking the microprocessor. Cell 125: 827-829.
66. Seo GJ, Fink LH, O'Hara B, Atwood WJ, Sullivan CS. 2008. Evolutionarily conserved function of a viral microRNA. J Virol 82: 9823-9828.
67. Seo GJ, Chen CJ, Sullivan CS. 2009. Merkel cell polyomavirus encodes a microRNA with the ability to autoregulate viral gene expression. Virology 383: 183-187.
68. Shi W, Hendrix D, Levine M, Haley B. 2009. A distinct class of small RNAs arises from pre-miRNA-proximal regions in a simple chordate. Nat Struct Mol Biol 16: 183-189.
69. Skalsky RL, Samols MA, Plaisance KB, Boss IW, Riva A, Lopez MC, Baker HV, Renne R. 2007. Kaposi's sarcoma-associated herpesvirus encodes an ortholog of miR-155. J Virol 81: 12836-12845. (Pubitemid 350156921)
70. Stark A, Bushati N, Jan CH, Kheradpour P, Hodges E, Brennecke J, Bartel DP, Cohen SM, Kellis M. 2008. A single Hox locus in Drosophila produces functional microRNAs from opposite DNA strands. Genes Dev 22: 8-13.
71. Sullivan CS. 2008. New roles for large and small viral RNAs in evading host defences. Nat Rev Genet 9: 503-507.
72. Sullivan CS, Cullen BR. 2009. Noncoding regulatory RNAs of the DNA tumor viruses. In DNA tumor viruses (ed. B Damania and JM Pipas), Chap. 25, pp. 645-681. Springer Science, New York.
73. Sullivan CS, Ganem D. 2005. A virus-encoded inhibitor that blocks RNA interference in mammalian cells. J Virol 79: 7371-7379. (Pubitemid 40756773)
74. Sullivan CS, Grundhoff A. 2007. Identification of viral microRNAs. Methods Enzymol 427: 3-23.
75. Sullivan CS, Grundhoff AT, Tevethia S, Pipas JM, Ganem D. 2005. SV40-encoded microRNAs regulate viral gene expression and reduce susceptibility to cytotoxic T cells. Nature 435: 682-686. (Pubitemid 40825513)
76. Sullivan CS, Sung CK, Pack CD, Grundhoff A, Lukacher AE, Benjamin TL, Ganem D. 2009. Murine Polyomavirus encodes a microRNA that cleaves early RNA transcripts but is not essential for experimental infection. Virology 387: 157-167.
77. Sun R, Lin SF, Gradoville L, Miller G. 1996. Polyadenylylated nuclear RNA encoded by Kaposi sarcoma-associated herpesvirus. Proc Natl Acad Sci 93: 11883-11888.
78. Tang S, Bertke AS, Patel A, Wang K, Cohen JI, Krause PR. 2008. An acutely and latently expressed herpes simplex virus 2 viral micro-RNA inhibits expression of ICP34.5, a viral neurovirulence factor. Proc Natl Acad Sci 105: 10931-10936.
79. Tyler DM, Okamura K, Chung WJ, Hagen JW, Berezikov E, Hannon GJ, Lai EC. 2008. Functionally distinct regulatory RNAs generated by bidirectional transcription and processing of microRNA loci. Genes Dev 22: 26-36.
80. Umbach JL, Cullen BR. 2010. In-depth analysis of Kaposi's sarcoma-associated herpesvirus microRNA expression provides insights into the mammalian microRNA-processing machinery. J Virol 84: 695-703.
81. Umbach JL, Kramer MF, Jurak I, Karnowski HW, Coen DM, Cullen BR. 2008. MicroRNAs expressed by herpes simplex virus 1 during latent infection regulate viral mRNAs. Nature 454: 780-783.
82. Vasudevan S, Tong Y, Steitz JA. 2008. Cell-cycle control of micro-RNA-mediated translation regulation. Cell Cycle 7: 1545-1549.
83. Watanabe T, Totoki Y, Toyoda A, Kaneda M, Kuramochi-Miyagawa S, Obata Y, Chiba H, Kohara Y, Kono T, Nakano T, et al. 2008. Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes. Nature 453: 539-543.
84. Weber K, Bolander ME, Sarkar G. 1998. PIG-B: A homemade monophasic cocktail for the extraction of RNA. Mol Biotechnol 9: 73-77.