Viral microRNA targetome of KSHV-Infected primary effusion lymphoma cell lines

Cell Host and Microbe

Volumn 10, Issue 5, 2011, Pages 515-526

  Gottwein, Eva ^a   Corcoran, David L ^b   Mukherjee, Neelanjan ^b   Skalsky, Rebecca L ^c   Hafner, Markus ^d   Nusbaum, Jeffrey D ^d   Shamulailatpam, Priscilla ^a   Love, Cassandra L ^b   Dave, Sandeep S ^b   Tuschl, Thomas ^d   Ohler, Uwe ^b,c   Cullen, Bryan R ^c  

^a NORTHWESTERN UNIVERSITY   (United States)

^b DUKE UNIVERSITY   (United States)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; MICRORNA; MIR 142 3P; MIR155; UNCLASSIFIED DRUG; VIRUS RNA;

ANIMAL CELL; ARTICLE; BINDING SITE; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 8; LYMPHOMA CELL LINE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PRIMARY EFFUSION LYMPHOMA; PRIORITY JOURNAL; VIRUS LATENCY; VIRUS REPLICATION;

BASE SEQUENCE; CELL LINE, TUMOR; HERPESVIRUS 8, HUMAN; HUMANS; LYMPHOMA, PRIMARY EFFUSION; MICRORNAS; MOLECULAR SEQUENCE DATA; RNA, VIRAL;

HUMAN HERPESVIRUS 4; HUMAN HERPESVIRUS 8;

EID: 81755161195     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2011.09.012     Document Type: Article

References (50)

1. J.R. Abend, T. Uldrick, and J.M. Ziegelbauer Regulation of tumor necrosis factor-like weak inducer of apoptosis receptor protein (TWEAKR) expression by Kaposi's sarcoma-associated herpesvirus microRNA prevents TWEAK-induced apoptosis and inflammatory cytokine expression J. Virol. 84 2010 12139 12151
2. D.P. Bartel MicroRNAs: target recognition and regulatory functions Cell 136 2009 215 233
3. P. Bellare, and D. Ganem Regulation of KSHV lytic switch protein expression by a virus-encoded microRNA: an evolutionary adaptation that fine-tunes lytic reactivation Cell Host Microbe 6 2009 570 575
4. X. Cai, S. Lu, Z. Zhang, C.M. Gonzalez, B. Damania, and B.R. Cullen Kaposi's sarcoma-associated herpesvirus expresses an array of viral microRNAs in latently infected cells Proc. Natl. Acad. Sci. USA 102 2005 5570 5575
5. X. Cai, A. Schafer, S. Lu, J.P. Bilello, R.C. Desrosiers, R. Edwards, N. Raab-Traub, and B.R. Cullen Epstein-Barr virus microRNAs are evolutionarily conserved and differentially expressed PLoS Pathog. 2 2006 e23 10.1371/journal.ppat.0020023
6. A. Carbone, A. Gloghini, D. Capello, and G. Gaidano Genetic pathways and histogenetic models of AIDS-related lymphomas Eur. J. Cancer 37 2001 1270 1275
7. E. Cesarman, Y. Chang, P.S. Moore, J.W. Said, and D.M. Knowles Kaposi's sarcoma-associated herpesvirus-like DNA sequences in AIDS-related body-cavity-based lymphomas N. Engl. J. Med. 332 1995 1186 1191
8. C.Z. Chen, L. Li, H.F. Lodish, and D.P. Bartel MicroRNAs modulate hematopoietic lineage differentiation Science 303 2004 83 86
9. S.J. Chen, G.H. Chen, Y.H. Chen, C.Y. Liu, K.P. Chang, Y.S. Chang, and H.C. Chen Characterization of Epstein-Barr virus miRNAome in nasopharyngeal carcinoma by deep sequencing PLoS ONE 5 2010 e12745 10.1371/journal.pone.0012745
10. E.Y. Choy, K.L. Siu, K.H. Kok, R.W. Lung, C.M. Tsang, K.F. To, D.L. Kwong, S.W. Tsao, and D.Y. Jin An Epstein-Barr virus-encoded microRNA targets PUMA to promote host cell survival J. Exp. Med. 205 2008 2551 2560
11. D.L. Corcoran, S. Georgiev, N. Mukherjee, E. Gottwein, R.L. Skalsky, J.D. Keene, and U. Ohler PARalyzer: definition of RNA binding sites from PAR-CLIP short-read sequence data Genome Biol. 12 2011 R79
12. S. Costinean, N. Zanesi, Y. Pekarsky, E. Tili, S. Volinia, N. Heerema, and C.M. Croce Pre-B cell proliferation and lymphoblastic leukemia/high-grade lymphoma in E(mu)-miR155 transgenic mice Proc. Natl. Acad. Sci. USA 103 2006 7024 7029
13. L. Dolken, G. Malterer, F. Erhard, S. Kothe, C.C. Friedel, G. Suffert, L. Marcinowski, N. Motsch, S. Barth, and M. Beitzinger Systematic analysis of viral and cellular microRNA targets in cells latently infected with human gamma-herpesviruses by RISC immunoprecipitation assay Cell Host Microbe 7 2010 324 334
14. W. Fan, D. Bubman, A. Chadburn, W.J. Harrington Jr., E. Cesarman, and D.M. Knowles Distinct subsets of primary effusion lymphoma can be identified based on their cellular gene expression profile and viral association J. Virol. 79 2005 1244 1251
15. E. Gottwein, and B.R. Cullen Viral and cellular microRNAs as determinants of viral pathogenesis and immunity Cell Host Microbe 3 2008 375 387
16. E. Gottwein, and B.R. Cullen A human herpesvirus microRNA inhibits p21 expression and attenuates p21-mediated cell cycle arrest J. Virol. 84 2010 5229 5237
17. E. Gottwein, N. Mukherjee, C. Sachse, C. Frenzel, W.H. Majoros, J.T. Chi, R. Braich, M. Manoharan, J. Soutschek, and U. Ohler A viral microRNA functions as an orthologue of cellular miR-155 Nature 450 2007 1096 1099
18. S. Griffiths-Jones, R.J. Grocock, S. van Dongen, A. Bateman, and A.J. Enright miRBase: microRNA sequences, targets and gene nomenclature Nucleic Acids Res. 34 2006 D140 D144
19. A. Grimson, K.K. Farh, W.K. Johnston, P. Garrett-Engele, L.P. Lim, and D.P. Bartel MicroRNA targeting specificity in mammals: determinants beyond seed pairing Mol. Cell 27 2007 91 105
20. A. Grundhoff, C.S. Sullivan, and D. Ganem A combined computational and microarray-based approach identifies novel microRNAs encoded by human gamma-herpesviruses RNA 12 2006 733 750
21. S. Gu, L. Jin, F. Zhang, P. Sarnow, and M.A. Kay Biological basis for restriction of microRNA targets to the 3′ untranslated region in mammalian mRNAs Nat. Struct. Mol. Biol. 16 2009 144 150
22. M. Hafner, M. Landthaler, L. Burger, M. Khorshid, J. Hausser, P. Berninger, A. Rothballer, M. Ascano Jr., A.C. Jungkamp, and M. Munschauer Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP Cell 141 2010 129 141
23. A. Hansen, S. Henderson, D. Lagos, L. Nikitenko, E. Coulter, S. Roberts, F. Gratrix, K. Plaisance, R. Renne, and M. Bower KSHV-encoded miRNAs target MAF to induce endothelial cell reprogramming Genes Dev. 24 2010 195 205
24. W. Huang da, B.T. Sherman, and R.A. Lempicki Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources Nat. Protoc. 4 2009 44 57
25. B. Langmead, C. Trapnell, M. Pop, and S.L. Salzberg Ultrafast and memory-efficient alignment of short DNA sequences to the human genome Genome Biol. 10 2009 R25
26. X. Lei, Z. Bai, F. Ye, J. Xie, C.G. Kim, Y. Huang, and S.J. Gao Regulation of NF-kappaB inhibitor IkappaBalpha and viral replication by a KSHV microRNA Nat. Cell Biol. 12 2010 193 199
27. Z. Li, S.W. Kim, Y. Lin, P.S. Moore, Y. Chang, and B. John Characterization of viral and human RNAs smaller than canonical microRNAs J. Virol. 83 2009 12751 12758
28. L.P. Lim, N.C. Lau, P. Garrett-Engele, A. Grimson, J.M. Schelter, J. Castle, D.P. Bartel, P.S. Linsley, and J.M. Johnson Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs Nature 433 2005 769 773
29. H.R. Lin, and D. Ganem Viral microRNA target allows insight into the role of translation in governing microRNA target accessibility Proc. Natl. Acad. Sci. USA 108 2011 5148 5153
30. Y.T. Lin, R.P. Kincaid, D. Arasappan, S.E. Dowd, S.P. Hunicke-Smith, and C.S. Sullivan Small RNA profiling reveals antisense transcription throughout the KSHV genome and novel small RNAs RNA 16 2010 1540 1558
31. S.D. Linnstaedt, E. Gottwein, R.L. Skalsky, M.A. Luftig, and B.R. Cullen Virally induced cellular microRNA miR-155 plays a key role in B-cell immortalization by Epstein-Barr virus J. Virol. 84 2010 11670 11678
32. A.K. Lo, K.F. To, K.W. Lo, R.W. Lung, J.W. Hui, G. Liao, and S.D. Hayward Modulation of LMP1 protein expression by EBV-encoded microRNAs Proc. Natl. Acad. Sci. USA 104 2007 16164 16169
33. C.C. Lu, Z. Li, C.Y. Chu, J. Feng, R. Sun, and T.M. Rana MicroRNAs encoded by Kaposi's sarcoma-associated herpesvirus regulate viral life cycle EMBO Rep. 11 2010 784 790
34. F. Lu, W. Stedman, M. Yousef, R. Renne, and P.M. Lieberman Epigenetic regulation of Kaposi's sarcoma-associated herpesvirus latency by virus-encoded microRNAs that target Rta and the cellular Rbl2-DNMT pathway J. Virol. 84 2010 2697 2706
35. A.R. Marquitz, A. Mathur, C.S. Nam, and N. Raab-Traub The Epstein-Barr virus BART microRNAs target the pro-apoptotic protein Bim Virology 412 2011 392 400
36. V. Marshall, T. Parks, R. Bagni, C.D. Wang, M.A. Samols, J. Hu, K.M. Wyvil, K. Aleman, R.F. Little, and R. Yarchoan 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 2007 645 659
37. D. Nachmani, N. Stern-Ginossar, R. Sarid, and O. Mandelboim Diverse herpesvirus microRNAs target the stress-induced immune ligand MICB to escape recognition by natural killer cells Cell Host Microbe 5 2009 376 385
38. R.M. O'Connell, D.S. Rao, A.A. Chaudhuri, M.P. Boldin, K.D. Taganov, J. Nicoll, R.L. Paquette, and D. Baltimore Sustained expression of microRNA-155 in hematopoietic stem cells causes a myeloproliferative disorder J. Exp. Med. 205 2008 585 594
39. S. Pfeffer, M. Zavolan, F.A. Grasser, M. Chien, J.J. Russo, J. Ju, B. John, A.J. Enright, D. Marks, and C. Sander Identification of virus-encoded microRNAs Science 304 2004 734 736
40. S. Pfeffer, A. Sewer, M. Lagos-Quintana, R. Sheridan, C. Sander, F.A. Grasser, L.F. van Dyk, C.K. Ho, S. Shuman, and M. Chien Identification of microRNAs of the herpesvirus family Nat. Methods 2 2005 269 276
41. M.A. Samols, R.L. Skalsky, A.M. Maldonado, A. Riva, M.C. Lopez, H.V. Baker, and R. Renne Identification of cellular genes targeted by KSHV-encoded microRNAs PLoS Pathog. 3 2007 e65 10.1371/journal.ppat.0030065
42. R.L. Skalsky, M.A. Samols, K.B. Plaisance, I.W. Boss, A. Riva, M.C. Lopez, H.V. Baker, and R. Renne Kaposi's sarcoma-associated herpesvirus encodes an ortholog of miR-155 J. Virol. 81 2007 12836 12845
43. A. Subramanian, P. Tamayo, V.K. Mootha, S. Mukherjee, B.L. Ebert, M.A. Gillette, A. Paulovich, S.L. Pomeroy, T.R. Golub, and E.S. Lander Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles Proc. Natl. Acad. Sci. USA 102 2005 15545 15550
44. J.L. Umbach, and B.R. Cullen In-depth analysis of Kaposi's sarcoma-associated herpesvirus microRNA expression provides insights into the mammalian microRNA-processing machinery J. Virol. 84 2010 695 703
45. J.L. Umbach, L.I. Strelow, S.W. Wong, and B.R. Cullen Analysis of rhesus rhadinovirus microRNAs expressed in virus-induced tumors from infected rhesus macaques Virology 405 2010 592 599
46. H. Wu, C. Ye, D. Ramirez, and N. Manjunath Alternative processing of primary microRNA transcripts by Drosha generates 5′ end variation of mature microRNA PLoS ONE 4 2009 e7566 10.1371/journal.pone.0007566
47. W. Yang, T.P. Chendrimada, Q. Wang, M. Higuchi, P.H. Seeburg, R. Shiekhattar, and K. Nishikura Modulation of microRNA processing and expression through RNA editing by ADAR deaminases Nat. Struct. Mol. Biol. 13 2006 13 21
48. J. Zhang, D.D. Jima, C. Jacobs, R. Fischer, E. Gottwein, G. Huang, P.L. Lugar, A.S. Lagoo, D.A. Rizzieri, and D.R. Friedman Patterns of microRNA expression characterize stages of human B-cell differentiation Blood 113 2009 4586 4594
49. Y. Zhao, H. Xu, Y. Yao, L.P. Smith, L. Kgosana, J. Green, L. Petherbridge, S.J. Baigent, and V. Nair Critical role of the virus-encoded microRNA-155 ortholog in the induction of Marek's disease lymphomas PLoS Pathog. 7 2011 e1001305 10.1371/journal.ppat.1001305
50. J.M. Ziegelbauer, C.S. Sullivan, and D. Ganem Tandem array-based expression screens identify host mRNA targets of virus-encoded microRNAs Nat. Genet. 41 2009 130 134