Ago HITS-CLIP Expands Understanding of Kaposi's Sarcoma-associated Herpesvirus miRNA Function in Primary Effusion Lymphomas

PLoS Pathogens

Volumn 8, Issue 8, 2012, Pages

  Haecker, Irina ^a   Gay, Lauren A ^a   Yang, Yajie ^a   Hu, Jianhong ^a   Morse, Alison M ^a   McIntyre, Lauren M ^a   Renne, Rolf ^a,b  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE PROTEIN; MICRORNA; RNA INDUCED SILENCING COMPLEX; VIRUS RNA;

3' UNTRANSLATED REGION; ANGIOFOLLICULAR LYMPH NODE HYPERPLASIA; APOPTOSIS; ARTICLE; CELL CYCLE REGULATION; CELL STRAIN BC 3; CELL STRAIN BCBL 1; CONTROLLED STUDY; CROSS LINKING; GENE EXPRESSION REGULATION; GENE TARGETING; HIGH THROUGHPUT SEQUENCING; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 8; IMMUNE EVASION; IMMUNOPRECIPITATION; KAPOSI SARCOMA; LYMPHOCYTE PROLIFERATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIMARY EFFUSION LYMPHOMA; TUMOR CELL LINE; VIRUS CARCINOGENESIS; VIRUS GENOME; VIRUS PATHOGENESIS;

APOPTOSIS; CELL CYCLE; CELL LINE; CYCLIN D1; HERPESVIRUS 8, HUMAN; HUMANS; LYMPHOMA, PRIMARY EFFUSION; MICRORNAS; RNA, NEOPLASM; RNA, VIRAL; SARCOMA, KAPOSI;

HUMAN HERPESVIRUS 8;

EID: 84866150841     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002884     Document Type: Article

References (93)

1. 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 [see comments]. Science 266: 1865-1869.
2. Cesarman E, Chang Y, Moore PS, Said JW, Knowles DM, (1995) Kaposi's sarcoma-associated herpesvirus-like DNA sequences in AIDS-related body-cavity-based lymphomas. N Engl J Med 332: 1186-1191.
3. Soulier J, Grollet L, Oksenhendler E, Cacoub P, Cazals-Hatem D, et al. (1995) Kaposi's sarcoma-associated herpesvirus-like DNA sequences in multicentric Castleman's disease. Blood 86: 1276-1280.
4. Ambros V, (2004) The functions of animal microRNAs. Nature 431: 350-355.
5. Pfeffer S, Zavolan M, Grasser FA, Chien M, Russo JJ, et al. (2004) Identification of virus-encoded microRNAs. Science 304: 734-736.
6. Boss IW, Plaisance KB, Renne R, (2009) Role of virus-encoded microRNAs in herpesvirus biology. Trends Microbiol 17: 544-553.
7. Skalsky RL, Cullen BR, (2010) Viruses, microRNAs, and host interactions. Annu Rev Microbiol 64: 123-141.
8. Cai X, Lu S, Zhang Z, Gonzalez CM, Damania B, et al. (2005) Kaposi's sarcoma-associated herpesvirus expresses an array of viral microRNAs in latently infected cells. Proc Natl Acad Sci U S A 102: 5570-5575.
9. Grundhoff A, Sullivan CS, Ganem D, (2006) A combined computational and microarray-based approach identifies novel microRNAs encoded by human gamma-herpesviruses. Rna 12: 733-750.
10. Pfeffer S, Sewer A, Lagos-Quintana M, Sheridan R, Sander C, et al. (2005) Identification of microRNAs of the herpesvirus family. Nat Methods 2: 269-276.
11. 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.
12. 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.
13. Gandy SZ, Linnstaedt SD, Muralidhar S, Cashman KA, Rosenthal LJ, et al. (2007) RNA editing of the human herpesvirus 8 kaposin transcript eliminates its transforming activity and is induced during lytic replication. J Virol 81: 13544-13551.
14. Marshall V, Parks T, Bagni R, Wang CD, Samols MA, 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.
15. O'Hara AJ, Chugh P, Wang L, Netto EM, Luz E, et al. (2009) Pre-micro RNA signatures delineate stages of endothelial cell transformation in Kaposi sarcoma. PLoS Pathog 5: e1000389.
16. O'Hara AJ, Wang L, Dezube BJ, Harrington WJ Jr, Damania B, et al. (2009) Tumor suppressor microRNAs are underrepresented in primary effusion lymphoma and Kaposi sarcoma. Blood 113: 5938-5941.
17. Di Leva G, Croce CM, (2010) Roles of small RNAs in tumor formation. Trends Mol Med 16: 257-267.
18. Ziegelbauer JM, Sullivan CS, Ganem D, (2009) Tandem array-based expression screens identify host mRNA targets of virus-encoded microRNAs. Nat Genet 41: 130-134.
19. Samols MA, Hu J, Skalsky RL, Maldonado AM, Riva A, et al. (2007) Identification of cellular genes targeted by KSHV-encoded microRNAs. PLoS Pathog 3: e65.
20. Hansen A, Henderson S, Lagos D, Nikitenko L, Coulter E, et al. (2010) KSHV-encoded miRNAs target MAF to induce endothelial cell reprogramming. Genes Dev 24: 195-205.
21. Abend JR, Uldrick T, Ziegelbauer JM, (2010) 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: 12139-12151.
22. Gottwein E, Mukherjee N, Sachse C, Frenzel C, Majoros WH, et al. (2007) A viral microRNA functions as an orthologue of cellular miR-155. Nature 450: 1096-1099.
23. Skalsky RL, Samols MA, Plaisance KB, Boss IW, Riva A, et al. (2007) Kaposi's sarcoma-associated herpesvirus encodes an ortholog of miR-155. J Virol 81: 12836-12845.
24. Boss IW, Nadeau PE, Abbott JR, Yang Y, Mergia A, et al. (2011) A KSHV encoded ortholog of miR-155 induces human splenic B-cell expansion in NOD/LtSz-scid IL2R{gamma}null mice. J Virol 85: 9877-86.
25. Chi SW, Zang JB, Mele A, Darnell RB, (2009) Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature 460: 479-486.
26. Hafner M, Landthaler M, Burger L, Khorshid M, Hausser J, et al. (2010) Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 141: 129-141.
27. Gottwein E, Corcoran DL, Mukherjee N, Skalsky RL, Hafner M, et al. (2011) Viral microRNA targetome of KSHV-infected primary effusion lymphoma cell lines. Cell Host Microbe 10: 515-526.
28. An FQ, Compitello N, Horwitz E, Sramkoski M, Knudsen ES, et al. (2005) The latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus modulates cellular gene expression and protects lymphoid cells from p16 INK4A-induced cell cycle arrest. J Biol Chem 280: 3862-3874.
29. Jenner RG, Maillard K, Cattini N, Weiss RA, Boshoff C, et al. (2003) Kaposi's sarcoma-associated herpesvirus-infected primary effusion lymphoma has a plasma cell gene expression profile. Proc Natl Acad Sci U S A 100: 10399-10404.
30. Fais F, Gaidano G, Capello D, Gloghini A, Ghiotto F, et al. (1999) Immunoglobulin V region gene use and structure suggest antigen selection in AIDS-related primary effusion lymphomas. Leukemia 13: 1093-1099.
31. Matolcsy A, Nador RG, Cesarman E, Knowles DM, (1998) Immunoglobulin VH gene mutational analysis suggests that primary effusion lymphomas derive from different stages of B cell maturation. Am J Pathol 153: 1609-1614.
32. Fan W, Bubman D, Chadburn A, Harrington WJ Jr, Cesarman E, et al. (2005) Distinct subsets of primary effusion lymphoma can be identified based on their cellular gene expression profile and viral association. J Virol 79: 1244-1251.
33. Leung AK, Young AG, Bhutkar A, Zheng GX, Bosson AD, et al. (2011) Genome-wide identification of Ago2 binding sites from mouse embryonic stem cells with and without mature microRNAs. Nat Struct Mol Biol 18: 237-244.
34. Kishore S, Jaskiewicz L, Burger L, Hausser J, Khorshid M, et al. (2011) A quantitative analysis of CLIP methods for identifying binding sites of RNA-binding proteins. Nat Methods 8: 559-64.
35. Riley KJ, Rabinowitz GS, Yario TA, Luna JM, Darnell RB, et al. (2012) EBV and human microRNAs co-target oncogenic and apoptotic viral and human genes during latency. Embo J 31: 2207-2221.
36. Friedlander MR, Chen W, Adamidi C, Maaskola J, Einspanier R, et al. (2008) Discovering microRNAs from deep sequencing data using miRDeep. Nat Biotechnol 26: 407-415.
37. Khorshid M, Rodak C, Zavolan M, (2011) CLIPZ: a database and analysis environment for experimentally determined binding sites of RNA-binding proteins. Nucleic Acids Res 39: D245-252.
38. Zisoulis DG, Lovci MT, Wilbert ML, Hutt KR, Liang TY, et al. (2010) Comprehensive discovery of endogenous Argonaute binding sites in Caenorhabditis elegans. Nat Struct Mol Biol 17: 173-179.
39. Skalsky RL, Corcoran DL, Gottwein E, Frank CL, Kang D, et al. (2012) The Viral and Cellular MicroRNA Targetome in Lymphoblastoid Cell Lines. PLoS Pathog 8: e1002484.
40. Taganov KD, Boldin MP, Chang KJ, Baltimore D, (2006) NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc Natl Acad Sci U S A 103: 12481-12486.
41. Costinean S, Zanesi N, Pekarsky Y, Tili E, Volinia S, et al. (2006) Pre-B cell proliferation and lymphoblastic leukemia/high-grade lymphoma in E(mu)-miR155 transgenic mice. Proc Natl Acad Sci U S A 103: 7024-7029.
42. Calin GA, Croce CM, (2006) MicroRNA signatures in human cancers. Nat Rev Cancer 6: 857-866.
43. Chandriani S, Ganem D, (2010) Array-based transcript profiling and limiting-dilution reverse transcription-PCR analysis identify additional latent genes in Kaposi's sarcoma-associated herpesvirus. J Virol 84: 5565-5573.
44. Lu F, Stedman W, Yousef M, Renne R, Lieberman PM, (2010) 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: 2697-2706.
45. Bellare P, Ganem D, (2009) Regulation of KSHV lytic switch protein expression by a virus-encoded microRNA: an evolutionary adaptation that fine-tunes lytic reactivation. Cell Host Microbe 6: 570-575.
46. Dolken L, Malterer G, Erhard F, Kothe S, Friedel CC, et al. (2010) Systematic analysis of viral and cellular microRNA targets in cells latently infected with human gamma-herpesviruses by RISC immunoprecipitation assay. Cell Host Microbe 7: 324-334.
47. Nachmani D, Stern-Ginossar N, Sarid R, Mandelboim O, (2009) Diverse herpesvirus microRNAs target the stress-induced immune ligand MICB to escape recognition by natural killer cells. Cell Host Microbe 5: 376-385.
48. Lu CC, Li Z, Chu CY, Feng J, Feng J, et al. (2010) MicroRNAs encoded by Kaposi's sarcoma-associated herpesvirus regulate viral life cycle. EMBO Rep 11: 784-790.
49. Lei X, Bai Z, Ye F, Xie J, Kim CG, et al. (2010) Regulation of NF-kappaB inhibitor IkappaBalpha and viral replication by a KSHV microRNA. Nat Cell Biol 12: 193-199.
50. Li Z, Kim SW, Lin Y, Moore PS, Chang Y, et al. (2009) Characterization of viral and human RNAs smaller than canonical MicroRNAs. J Virol 83: 12751-12758.
51. Liu Y, Sun R, Lin X, Liang D, Deng Q, et al. (2012) Kaposi's sarcoma-associated herpesvirus-encoded microRNA miR-K12-11 attenuates transforming growth factor beta signaling through suppression of SMAD5. J Virol 86: 1372-1381.
52. Suffert G, Malterer G, Hausser J, Viiliainen J, Fender A, et al. (2011) Kaposi's sarcoma herpesvirus microRNAs target caspase 3 and regulate apoptosis. PLoS Pathog 7: e1002405.
53. Xu G, Fewell C, Taylor C, Deng N, Hedges D, et al. (2010) Transcriptome and targetome analysis in MIR155 expressing cells using RNA-seq. Rna 16: 1610-1622.
54. Yin Q, McBride J, Fewell C, Lacey M, Wang X, et al. (2008) MicroRNA-155 is an Epstein-Barr virus-induced gene that modulates Epstein-Barr virus-regulated gene expression pathways. J Virol 82: 5295-5306.
55. O'Connell RM, Rao DS, Chaudhuri AA, Boldin MP, Taganov KD, et al. (2008) Sustained expression of microRNA-155 in hematopoietic stem cells causes a myeloproliferative disorder. J Exp Med 205: 585-594.
56. Lu C, Huang X, Zhang X, Roensch K, Cao Q, et al. (2011) miR-221 and miR-155 regulate human dendritic cell development, apoptosis, and IL-12 production through targeting of p27kip1, KPC1, and SOCS-1. Blood 117: 4293-4303.
57. Costinean S, Sandhu SK, Pedersen IM, Tili E, Trotta R, et al. (2009) Src homology 2 domain-containing inositol-5-phosphatase and CCAAT enhancer-binding protein beta are targeted by miR-155 in B cells of Emicro-MiR-155 transgenic mice. Blood 114: 1374-1382.
58. Ceppi M, Pereira PM, Dunand-Sauthier I, Barras E, Reith W, et al. (2009) MicroRNA-155 modulates the interleukin-1 signaling pathway in activated human monocyte-derived dendritic cells. Proc Natl Acad Sci U S A 106: 2735-2740.
59. Zhou H, Huang X, Cui H, Luo X, Tang Y, et al. (2010) miR-155 and its star-form partner miR-155* cooperatively regulate type I interferon production by human plasmacytoid dendritic cells. Blood 116: 5885-5894.
60. Gironella M, Seux M, Xie MJ, Cano C, Tomasini R, et al. (2007) Tumor protein 53-induced nuclear protein 1 expression is repressed by miR-155, and its restoration inhibits pancreatic tumor development. Proc Natl Acad Sci U S A 104: 16170-16175.
61. Tili E, Michaille JJ, Wernicke D, Alder H, Costinean S, et al. (2011) Mutator activity induced by microRNA-155 (miR-155) links inflammation and cancer. Proc Natl Acad Sci U S A 108: 4908-4913.
62. Selbach M, Schwanhausser B, Thierfelder N, Fang Z, Khanin R, et al. (2008) Widespread changes in protein synthesis induced by microRNAs. Nature 455: 58-63.
63. Baek D, Villen J, Shin C, Camargo FD, Gygi SP, et al. (2008) The impact of microRNAs on protein output. Nature 455: 64-71.
64. Grimson A, Farh KK, Johnston WK, Garrett-Engele P, Lim LP, et al. (2007) MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol Cell 27: 91-105.
65. Fang Z, Rajewsky N, (2011) The impact of miRNA target sites in coding sequences and in 3′UTRs. PLoS One 6: e18067.
66. Huang da W, Sherman BT, Lempicki RA, (2009) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37: 1-13.
67. Huang da W, Sherman BT, Lempicki RA, (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57.
68. Kasof GM, Goyal L, White E, (1999) Btf, a novel death-promoting transcriptional repressor that interacts with Bcl-2-related proteins. Mol Cell Biol 19: 4390-4404.
69. Cuconati A, White E, (2002) Viral homologs of BCL-2: role of apoptosis in the regulation of virus infection. Genes Dev 16: 2465-2478.
70. Delgado T, Carroll PA, Punjabi AS, Margineantu D, Hockenbery DM, et al. (2010) Induction of the Warburg effect by Kaposi's sarcoma herpesvirus is required for the maintenance of latently infected endothelial cells. Proc Natl Acad Sci U S A 107: 10696-10701.
71. Warburg O, (1956) On the Origin of Cancer Cells. Science 123: 309-334.
72. Toscano MA, Campagna L, Molinero LL, Cerliani JP, Croci DO, et al. (2011) Nuclear factor (NF)-kappaB controls expression of the immunoregulatory glycan-binding protein galectin-1. Mol Immunol 48: 1940-1949.
73. Wang P, Wu P, Siegel MI, Egan RW, Billah MM, (1995) Interleukin (IL)-10 inhibits nuclear factor kappa B (NF kappa B) activation in human monocytes. IL-10 and IL-4 suppress cytokine synthesis by different mechanisms. J Biol Chem 270: 9558-9563.
74. Guasparri I, Keller SA, Cesarman E, (2004) KSHV vFLIP is essential for the survival of infected lymphoma cells. J Exp Med 199: 993-1003.
75. Jarviluoma A, Child ES, Sarek G, Sirimongkolkasem P, Peters G, et al. (2006) Phosphorylation of the cyclin-dependent kinase inhibitor p21Cip1 on serine 130 is essential for viral cyclin-mediated bypass of a p21Cip1-imposed G1 arrest. Mol Cell Biol 26: 2430-2440.
76. Sarek G, Jarviluoma A, Ojala PM, (2006) KSHV viral cyclin inactivates p27KIP1 through Ser10 and Thr187 phosphorylation in proliferating primary effusion lymphomas. Blood 107: 725-732.
77. Stern-Ginossar N, Elefant N, Zimmermann A, Wolf DG, Saleh N, et al. (2007) Host immune system gene targeting by a viral miRNA. Science 317: 376-381.
78. Coscoy L, Ganem D, (2001) A viral protein that selectively downregulates ICAM-1 and B7-2 and modulates T cell costimulation. J Clin Invest 107: 1599-1606.
79. Means RE, Ishido S, Alvarez X, Jung JU, (2002) Multiple endocytic trafficking pathways of MHC class I molecules induced by a Herpesvirus protein. Embo J 21: 1638-1649.
80. Jayaprakash AD, Jabado O, Brown BD, Sachidanandam R, (2011) Identification and remediation of biases in the activity of RNA ligases in small-RNA deep sequencing. Nucleic Acids Res 39: e141.
81. Boss IW, Renne R, (2011) Viral miRNAs and immune evasion. Biochim Biophys Acta 1809: 708-14.
82. O'Hara AJ, Vahrson W, Dittmer DP, (2008) Gene alteration and precursor and mature microRNA transcription changes contribute to the miRNA signature of primary effusion lymphoma. Blood 111: 2347-2353.
83. Baccarini A, Chauhan H, Gardner TJ, Jayaprakash AD, Sachidanandam R, et al. (2011) Kinetic analysis reveals the fate of a microRNA following target regulation in mammalian cells. Curr Biol 21: 369-376.
84. Mukherji S, Ebert MS, Zheng GX, Tsang JS, Sharp PA, et al. (2011) MicroRNAs can generate thresholds in target gene expression. Nat Genet 43: 854-859.
85. Dolken L, Perot J, Cognat V, Alioua A, John M, et al. (2007) Mouse cytomegalovirus microRNAs dominate the cellular small RNA profile during lytic infection and show features of posttranscriptional regulation. J Virol 81: 13771-13782.
86. Nelson PT, De Planell-Saguer M, Lamprinaki S, Kiriakidou M, Zhang P, et al. (2007) A novel monoclonal antibody against human Argonaute proteins reveals unexpected characteristics of miRNAs in human blood cells. RNA 13: 1787-1792.
87. Hinck L, Nathke IS, Papkoff J, Nelson WJ, (1994) Dynamics of cadherin/catenin complex formation: novel protein interactions and pathways of complex assembly. J Cell Biol 125: 1327-1340.
88. Rudel S, Flatley A, Weinmann L, Kremmer E, Meister G, (2008) A multifunctional human Argonaute2-specific monoclonal antibody. Rna 14: 1244-1253.
89. Bland JM, Altman DG, (1986) Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1: 307-310.
90. Bland JM, Altman DG, (1988) Misleading statistics: errors in textbooks, software and manuals. Int J Epidemiol 17: 245-247.
91. McIntyre LM, Lopiano KK, Morse AM, Amin V, Oberg AL, et al. (2011) RNA-seq: technical variability and sampling. BMC Genomics 12: 293.
92. Dudoit S, Yang YH, Callow MJ, Speed TP, (2002) Statistical methods for identifying differentially expressed genes in replicated cDNA microarray experiments. Stat Sin 2: 111-139.
93. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B, (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621-628.