CoChat
Sign Up
Cited by 57Viral-associated cancers and disordersMicroRNA in disease regulationCancer-related molecular mechanisms research

Modified Cross-Linking, Ligation, and Sequencing of Hybrids (qCLASH) Identifies Kaposi's Sarcoma-Associated Herpesvirus MicroRNA Targets in Endothelial Cells

Open access
Gay, Lauren A., Sethuraman, Sunantha, Thomas, Merin, Turner, Peter C., Renne, Rolf·2018·Journal of Virology
DOI 10.1128/jvi.02138-17PMC PMC5874430
Open this paper in CoChat — free account

Abstract

Kaposi's sarcoma (KS) tumors are derived from endothelial cells and express Kaposi's sarcoma-associated herpesvirus (KSHV) microRNAs (miRNAs). Although miRNA targets have been identified in B cell lymphoma-derived cells and epithelial cells, little has been done to characterize the KSHV miRNA targetome in endothelial cells. A recent innovation in the identification of miRNA targetomes, cross-linking, ligation, and sequencing of hybrids (CLASH), unambiguously identifies miRNAs and their targets by ligating the two species while both species are still bound within the RNA-induced silencing complex (RISC). We developed a streamlined quick CLASH (qCLASH) protocol that requires a lower cell input than the original method and therefore has the potential to be used on patient biopsy samples. Additionally, we developed a fast-growing, KSHV-negative endothelial cell line derived from telomerase-immortalized vein endothelial long-term culture (TIVE-LTC) cells. qCLASH was performed on uninfected cells and cells infected with either wild-type KSHV or a mutant virus lacking miR-K12-11/11*. More than 1,400 cellular targets of KSHV miRNAs were identified. Many of the targets identified by qCLASH lacked a canonical seed sequence match. Additionally, most target regions in mRNAs originated from the coding DNA sequence (CDS) rather than the 3′ untranslated region (UTR). This set of genes includes some that were previously identified in B cells and some new genes that warrant further study. Pathway analysis of endothelial cell targets showed enrichment in cell cycle control, apoptosis, and glycolysis pathways, among others. Characterization of these new targets and the functional consequences of their repression will be important in furthering our understanding of the role of KSHV miRNAs in oncogenesis. IMPORTANCE KS lesions consist of endothelial cells latently infected with KSHV. Cells that make up these lesions express KSHV miRNAs. Identification of the targets of KSHV miRNAs will help us understand their role in viral oncogenesis. The cross-linking and sequencing of hybrids (CLASH) protocol is a method for unambiguously identifying miRNA targetomes. We developed a streamlined version of CLASH, called quick CLASH (qCLASH). qCLASH requires a lower initial input of cells than for its parent protocol. Additionally, a new fast-growing KSHV-negative endothelial cell line, named TIVE-EX-LTC cells, was established. qCLASH was performed on TIVE-EX-LTC cells latently infected with wild-type (WT) KSHV or a mutant virus lacking miR-K12-11/11*. A number of novel targets of KSHV miRNAs were identified, including targets of miR-K12-11, the ortholog of the cellular oncogenic miRNA (oncomiR) miR-155. Many of the miRNA targets were involved in processes related to oncogenesis, such as glycolysis, apoptosis, and cell cycle control.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1128/jvi.02138-17

Cites

2 of 2 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Chimeric CLIP-seq approaches incorporate a phosphorylation step and an additional ligation step to increase the frequency of chimeric fragments to as much as 5.3%, although it often remains less than 2%.

    “chimeric CLIP-seq approaches (including CLASH, CLEAR-CLIP, and modified iPAR-CLIP) have modified this approach by incorporating both a phosphorylation step (using 3' phosphatase minus T4 Polynucleotide Kinase) as well as an additional ligation step (without adapters) to encourage proximity-based ligation and increase the frequency of chimeric fragments to as much as 5.3%, although it often remains”

    From Scalable and deep profiling of mRNA targets for individual microRNAs with chimeric eCLIP (2022) · cites this paper as Gay et al., 2018

    The Results describe 5′ phosphorylation with T4 polynucleotide kinase followed by intermolecular ligation, and report that approximately 0.3%–1% of filtered qCLASH reads were hybrids. The paper does not report a 5.3% hybrid rate or specify phosphatase-minus T4 PNK for that step; the cited passages also do not establish those details for CLEAR-CLIP or modified iPAR-CLIP. Page numbers are unavailable in our copy. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

  • The transfer and isolation step by itself drives a dramatic reduction in experimental yield.

    “However, in addition to being complex for novice users and limiting scalability and automated handling, we and others have observed that this transfer and isolation step by itself drives a dramatic reduction in experimental yield, and multiple recent modified RBP immunoprecipitation protocols have been described which leave out this step (Gay et al., 2018;Ilik et al., 2020;Patton et al., 2020).”

    From Scalable and deep profiling of mRNA targets for individual microRNAs with chimeric eCLIP (2022) · cites this paper as Gay et al., 2018

    The Results say that omitting radiolabeling, SDS-PAGE, membrane transfer, and RNA cutting and elution avoids the loss of large amounts of RNA. They attribute the loss to those steps collectively, not to the transfer and isolation step by itself. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

  • Widespread adoption of chimeric CLIP methods remains limited because poor recovery of AGO-crosslinked RNA and low fraction of chimeric reads make it difficult to deeply profile the interactome of a miRNA of interest at a reasonable cost.

    “However, despite the obvious power of direct experimental identification of miRNA targets and recent efforts to improve the efficiency of these approaches in capturing additional chimeric molecules (Bjerke and Yi, 2020;Gay et al., 2018), widespread adoption of these methods remains limited, as both the poor recovery of AGO-crosslinked RNA as well as the low fraction of chimeric reads make it”

    From Scalable and deep profiling of mRNA targets for individual microRNAs with chimeric eCLIP (2022) · cites this paper as Gay et al., 2018

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 59

  1. [1]1. Chang Y, Cesarman E, Pessin MS, Lee F, Culpepper J, Knowles DM, Moore PS. 1994. Identification of herpesvirus-like DNA sequences in AIDSassociated Kaposi's sarcoma. Science 266:1865-1869. https://doi.org/10 .1126/science.7997879.
  2. [3]3. 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. https:// doi.org/10.1056/NEJM199505043321802. · DOI
  3. [4]4. Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F. 2015. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 136:E359-E386. https://doi.org/10.1002/ijc.29210. · DOI · Paper page
  4. [5]5. Bray F, Ren JS, Masuyer E, Ferlay J. 2013. Global estimates of cancer prevalence for 27 sites in the adult population in 2008. Int J Cancer 132:1133-1145. https://doi.org/10.1002/ijc.27711. · DOI
  5. [7]7. Sturzl M, Blasig C, Schreier A, Neipel F, Hohenadl C, Cornali E, Ascherl G, Esser S, Brockmeyer NH, Ekman M, Kaaya EE, Tschachler E, Biberfeld P. 1997. Expression of HHV-8 latency-associated T0.7 RNA in spindle cells and endothelial cells of AIDS-associated, classical and African Kaposi's sarcoma. Int J Cancer 72:68-71. https://doi.org/10.1002/(SICI)1097-0215 (19970703)72:1 < 68::AID-IJC10 > 3.0.CO;2-6. · DOI
  6. [10]10. Pfeffer S, Sewer A, Lagos-Quintana M, Sheridan R, Sander C, Grasser FA, van Dyk LF, Ho CK, Shuman S, Chien M, Russo JJ, Ju J, Randall G, Lindenbach BD, Rice CM, Simon V, Ho DD, Zavolan M, Tuschl T. 2005. Identification of microRNAs of the herpesvirus family. Nat Methods 2:269-276. https://doi.org/10.1038/nmeth746. · DOI
  7. [11]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. https://doi.org/10 .1128/JVI.79.14.9301-9305.2005.
  8. [12]12. Cai X, Cullen BR. 2006. Transcriptional origin of Kaposi's sarcomaassociated herpesvirus microRNAs. J Virol 80:2234-2242. https://doi.org/ 10.1128/JVI.80.5.2234-2242.2006. · DOI
  9. [13]13. Ambros V. 2004. The functions of animal microRNAs. Nature 431: 350-355. https://doi.org/10.1038/nature02871. · DOI · Paper page
  10. [14]14. Samols MA, Hu J, Skalsky RL, Maldonado AM, Riva A, Lopez MC, Baker HV, Renne R. 2007. Identification of cellular genes targeted by KSHVencoded microRNAs. PLoS Pathog 3:e65. https://doi.org/10.1371/journal .ppat.0030065. · DOI
  11. [15]15. 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. https://doi.org/10.1038/ng.266. · DOI
  12. [16]16. Gottwein E, Mukherjee N, Sachse C, Frenzel C, Majoros WH, Chi JT, Braich R, Manoharan M, Soutschek J, Ohler U, Cullen BR. 2007. A viral microRNA functions as an orthologue of cellular miR-155. Nature 450:1096-1099. https://doi.org/10.1038/nature05992. · DOI
  13. [17]17. 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. https://doi.org/10.1128/JVI .01804-07. · DOI
  14. [18]18. Boss IW, Nadeau PE, Abbott JR, Yang Y, Mergia A, Renne R. 2011. A Kaposi's sarcoma-associated herpesvirus-encoded ortholog of microRNA miR-155 induces human splenic B-cell expansion in NOD/LtSz-scid IL2Rgammanull mice. J Virol 85:9877-9886. https://doi.org/10.1128/JVI .05558-11. · DOI
  15. [19]19. Schenk P, Konrad K. 1985. Ultrastructure of Kaposi's sarcoma in acquired immune deficiency syndrome (AIDS). Arch Otorhinolaryngol 242: 305-313. https://doi.org/10.1007/BF00453555. · DOI
  16. [20]20. Haecker I, Gay LA, Yang Y, Hu J, Morse AM, McIntyre L, Renne R. 2012. Ago-HITS-CLIP expands understanding of Kaposi's sarcoma-associated herpesvirus miRNA function in primary effusion lymphomas. PLoS Pathog 8:e1002884. https://doi.org/10.1371/journal.ppat.1002884. · DOI
  17. [21]21. Chi SW, Zang JB, Mele A, Darnell RB. 2009. Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature 460:479-486. https://doi .org/10.1038/nature08170. · DOI · Paper page
  18. [22]22. Bartel DP. 2009. MicroRNAs: target recognition and regulatory functions. Cell 136:215-233. https://doi.org/10.1016/j.cell.2009.01.002. · DOI · Paper page
  19. [23]23. Hafner M, Landthaler M, Burger L, Khorshid M, Hausser J, Berninger P, Rothballer A, Ascano M, Jr, Jungkamp A-C, Munschauer M, Ulrich A, Wardle GS, Dewell S, Zavolan M, Tuschl T. 2010. Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 141:129-141. https://doi.org/10.1016/j.cell.2010.03.009. · DOI · Paper page
  20. [24]24. Helwak A, Kudla G, Dudnakova T, Tollervey D. 2013. Mapping the human miRNA interactome by CLASH reveals frequent noncanonical binding. Cell 153:654-665. https://doi.org/10.1016/j.cell.2013.03.043. · DOI · Paper page
  21. [25]25. Helwak A, Tollervey D. 2014. Mapping the miRNA interactome by crosslinking ligation and sequencing of hybrids (CLASH). Nat Protoc 9:711-728. https://doi.org/10.1038/nprot.2014.043. · DOI
  22. [27]27. Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114-2120. https://doi.org/10 .1093/bioinformatics/btu170.
  23. [28]28. Travis AJ, Moody J, Helwak A, Tollervey D, Kudla G. 2014. Hyb: a bioinformatics pipeline for the analysis of CLASH (crosslinking, ligation and sequencing of hybrids) data. Methods 65:263-273. https://doi.org/10 .1016/j.ymeth.2013.10.015.
  24. [29]29. Plaisance-Bonstaff K, Choi HS, Beals T, Krueger BJ, Boss IW, Gay LA, Haecker I, Hu J, Renne R. 2014. KSHV miRNAs decrease expression of lytic genes in latently infected PEL and endothelial cells by targeting host transcription factors. Viruses 6:4005-4023. https://doi.org/10.3390/ v6104005.
  25. [30]30. Grosswendt S, Filipchyk A, Manzano M, Klironomos F, Schilling M, Herzog M, Gottwein E, Rajewsky N. 2014. Unambiguous identification of miRNA:target site interactions by different types of ligation reactions. Mol Cell 54:1042-1054. https://doi.org/10.1016/j.molcel.2014.03.049. · DOI · Paper page
  26. [31]31. Gottwein E, Corcoran DL, Mukherjee N, Skalsky RL, Hafner M, Nusbaum JD, Shamulailatpam P, Love CL, Dave SS, Tuschl T, Ohler U, Cullen BR. 2011. Viral microRNA targetome of KSHV-infected primary effusion lymphoma cell lines. Cell Host Microbe 10:515-526. https://doi.org/10.1016/ j.chom.2011.09.012.
  27. [32]32. Suffert G, Malterer G, Hausser J, Viiliainen J, Fender A, Contrant M, Ivacevic T, Benes V, Gros F, Voinnet O, Zavolan M, Ojala PM, Haas JG, Pfeffer S. 2011. Kaposi's sarcoma herpesvirus microRNAs target caspase 3 and regulate apoptosis. PLoS Pathog 7:e1002405. https://doi.org/10 .1371/journal.ppat.1002405.
  28. [33]33. Gottwein E, Cullen BR. 2010. A human herpesvirus microRNA inhibits p21 expression and attenuates p21-mediated cell cycle arrest. J Virol 84:5229-5237. https://doi.org/10.1128/JVI.00202-10. · DOI
  29. [34]34. Lu CC, Li Z, Chu CY, Feng J, Feng J, Sun R, Rana TM. 2010. MicroRNAs encoded by Kaposi's sarcoma-associated herpesvirus regulate viral life cycle. EMBO Rep 11:784-790. https://doi.org/10.1038/embor.2010.132. · DOI
  30. [35]35. Lei X, Bai Z, Ye F, Xie J, Kim CG, Huang Y, Gao SJ. 2010. Regulation of NF-kappaB inhibitor IkappaBalpha and viral replication by a KSHV microRNA. Nat Cell Biol 12:193-199. https://doi.org/10.1038/ncb2019. · DOI
  31. [36]36. Lu F, Stedman W, Yousef M, Renne R, Lieberman PM. 2010. Epigenetic regulation of Kaposi's sarcoma-associated herpesvirus latency by virusencoded microRNAs that target Rta and the cellular Rbl2-DNMT pathway. J Virol 84:2697-2706. https://doi.org/10.1128/JVI.01997-09. · DOI
  32. [37]37. 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. https://doi.org/10.1128/JVI.00884-10. · DOI
  33. [38]38. Abend JR, Ramalingam D, Kieffer-Kwon P, Uldrick TS, Yarchoan R, Ziegelbauer JM. 2012. Kaposi's sarcoma-associated herpesvirus microRNAs target IRAK1 and MYD88, two components of the Toll-like receptor/ interleukin-1R signaling cascade, to reduce inflammatory-cytokine expression. J Virol 86:11663-11674. https://doi.org/10.1128/JVI.01147-12. · DOI
  34. [39]39. Hu M, Wang C, Li W, Lu W, Bai Z, Qin D, Yan Q, Zhu J, Krueger BJ, Renne R, Gao SJ, Lu C. 2015. A KSHV microRNA directly targets G proteincoupled receptor kinase 2 to promote the migration and invasion of endothelial cells by inducing CXCR2 and activating AKT signaling. PLoS Pathog 11:e1005171. https://doi.org/10.1371/journal.ppat.1005171. · DOI
  35. [40]40. Gallaher AM, Das S, Xiao Z, Andresson T, Kieffer-Kwon P, Happel C, Ziegelbauer J. 2013. Proteomic screening of human targets of viral microRNAs reveals functions associated with immune evasion and angiogenesis. PLoS Pathog 9:e1003584. https://doi.org/10.1371/journal .ppat.1003584. · DOI
  36. [41]41. 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. https://doi.org/10.1038/47266. · DOI
  37. [42]42. Si H, Verma SC, Robertson ES. 2006. Proteomic analysis of the Kaposi's sarcoma-associated herpesvirus terminal repeat element binding proteins. J Virol 80:9017-9030. https://doi.org/10.1128/JVI.00297-06. · DOI
  38. [43]43. 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. https://doi.org/10.1038/80459. · DOI
  39. [46]46. Thome M, Schneider P, Hofmann K, Fickenscher H, Meinl E, Neipel F, Mattmann C, Burns K, Bodmer JL, Schroter M, Scaffidi C, Krammer PH, Peter ME, Tschopp J. 1997. Viral FLICE-inhibitory proteins (FLIPs) prevent apoptosis induced by death receptors. Nature 386:517-521. https://doi .org/10.1038/386517a0. · DOI
  40. [47]47. Wang L, Dittmer DP, Tomlinson CC, Fakhari FD, Damania B. 2006. Immortalization of primary endothelial cells by the K1 protein of Kaposi's sarcoma-associated herpesvirus. Cancer Res 66:3658-3666. https://doi .org/10.1158/0008-5472.CAN-05-3680. · DOI
  41. [48]48. Koff A, Polyak K. 1995. p27KIP1, an inhibitor of cyclin-dependent kinases. Prog Cell Cycle Res 1:141-147. https://doi.org/10.1007/978-1-4615-1809 -9\_11. · DOI
  42. [49]49. Potapova TA, Sivakumar S, Flynn JN, Li R, Gorbsky GJ. 2011. Mitotic progression becomes irreversible in prometaphase and collapses when Wee1 and Cdc25 are inhibited. Mol Biol Cell 22:1191-1206. https://doi .org/10.1091/mbc.E10-07-0599. · DOI
  43. [50]50. Delgado T, Carroll PA, Punjabi AS, Margineantu D, Hockenbery DM, Lagunoff M. 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. https://doi.org/ 10.1073/pnas.1004882107. · DOI
  44. [51]51. Yogev O, Lagos D, Enver T, Boshoff C. 2014. Kaposi's sarcoma herpesvirus microRNAs induce metabolic transformation of infected cells. PLoS Pathog 10:e1004400. https://doi.org/10.1371/journal.ppat.1004400. · DOI
  45. [52]52. Yi W, Clark PM, Mason DE, Keenan MC, Hill C, Goddard WA, III, Peters EC, Driggers EM, Hsieh-Wilson LC. 2012. Phosphofructokinase 1 glycosylation regulates cell growth and metabolism. Science 337:975-980. https://doi .org/10.1126/science.1222278. · DOI
  46. [53]53. Guillou C, Freret M, Fondard E, Derambure C, Avenel G, Golinski ML, Verdet M, Boyer O, Caillot F, Musette P, Lequerre T, Vittecoq O. 2016. Soluble alpha-enolase activates monocytes by CD14-dependent TLR4 signalling pathway and exhibits a dual function. Sci Rep 6:23796. https:// doi.org/10.1038/srep23796. · DOI
  47. [54]54. Sturzl M, Gaus D, Dirks WG, Ganem D, Jochmann R. 2013. Kaposi's sarcoma-derived cell line SLK is not of endothelial origin, but is a contaminant from a known renal carcinoma cell line. Int J Cancer 132:1954-1958. https://doi.org/10.1002/ijc.27849. · DOI
  48. [55]55. Agarwal V, Bell GW, Nam JW, Bartel DP. 2015. Predicting effective microRNA target sites in mammalian mRNAs. eLife 4:e05005. https://doi .org/10.7554/eLife.05005. · DOI · Paper page
  49. [57]57. Loeb GB, Khan AA, Canner D, Hiatt JB, Shendure J, Darnell RB, Leslie CS, Rudensky AY. 2012. Transcriptome-wide miR-155 binding map reveals widespread noncanonical microRNA targeting. Mol Cell 48:760-770. https://doi.org/10.1016/j.molcel.2012.10.002. · DOI · Paper page
  50. [58]58. Khorshid M, Hausser J, Zavolan M, van Nimwegen E. 2013. A biophysical miRNA-mRNA interaction model infers canonical and noncanonical targets. Nat Methods 10:253-255. https://doi.org/10.1038/nmeth.2341. · DOI
  51. [59]59. Tay Y, Rinn J, Pandolfi PP. 2014. The multilayered complexity of ceRNA crosstalk and competition. Nature 505:344-352. https://doi.org/10.1038/ nature12986.
  52. [60]60. Jopling CL, Yi M, Lancaster AM, Lemon SM, Sarnow P. 2005. Modulation of hepatitis C virus RNA abundance by a liver-specific microRNA. Science 309:1577-1581. https://doi.org/10.1126/science.1113329. · DOI
  53. [61]61. Luna JM, Scheel TK, Danino T, Shaw KS, Mele A, Fak JJ, Nishiuchi E, Takacs CN, Catanese MT, de Jong YP, Jacobson IM, Rice CM, Darnell RB. 2015. Hepatitis C virus RNA functionally sequesters miR-122. Cell 160: 1099-1110. https://doi.org/10.1016/j.cell.2015.02.025. · DOI
  54. [62]62. Sethuraman S, Gay LA, Jain V, Haecker I, Renne R. 2017. MicroRNA dependent and independent deregulation of long non-coding RNAs by an oncogenic herpesvirus. PLoS Pathog 13:e1006508. https://doi.org/10 .1371/journal.ppat.1006508.
  55. [63]63. Atianand MK, Caffrey DR, Fitzgerald KA. 2017. Immunobiology of long noncoding RNAs. Annu Rev Immunol 35:177-198. https://doi.org/10.1146/ annurev-immunol-041015-055459.
  56. [64]64. An FQ, Folarin HM, Compitello N, Roth J, Gerson SL, McCrae KR, Fakhari FD, Dittmer DP, Renne R. 2006. Long-term-infected telomeraseimmortalized endothelial cells: a model for Kaposi's sarcoma-associated herpesvirus latency in vitro and in vivo. J Virol 80:4833-4846. https:// doi.org/10.1128/JVI.80.10.4833-4846.2006. · DOI
  57. [65]65. Brulois KF, Chang H, Lee AS, Ensser A, Wong LY, Toth Z, Lee SH, Lee HR, Myoung J, Ganem D, Oh TK, Kim JF, Gao SJ, Jung JU. 2012. Construction and manipulation of a new Kaposi's sarcoma-associated herpesvirus bacterial artificial chromosome clone. J Virol 86:9708-9720. https://doi .org/10.1128/JVI.01019-12. · DOI
  58. [66]66. Jain V, Plaisance-Bonstaff K, Sangani R, Lanier C, Dolce A, Hu J, Brulois K, Haecker I, Turner P, Renne R, Krueger B. 2016. A toolbox for herpesvirus miRNA research: construction of a complete set of KSHV miRNA deletion mutants. Viruses 8:E54. https://doi.org/10.3390/v8020054. · DOI
  59. [67]67. Edgar R, Domrachev M, Lash AE. 2002. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30:207-210. https://doi.org/10.1093/nar/30.1.207. · DOI · Paper page

Cited by

Sorted by citations

Authors
Gay, L. A., Sethuraman, S., Thomas, M., Turner, P. C., & Renne, R.
Affiliations
University of Florida (US)
ORCID
Venue
Journal of Virology
Publisher
American Society for Microbiology
Published
2018-04-15
Volume
92
Issue
8
ISSN
  • 0022-538X (ISSN-L)
  • 1098-5514
DOI
10.1128/jvi.02138-17
PMC
PMC5874430
OpenAlex
W2794347818
Cited by
57
References
2
Citations by year
2026: 3 · 2025: 5 · 2024: 6 · 2023: 9 · 2022: 9 · 2021: 10 · 2020: 5 · 2019: 8 · 2018: 2
FWCI
2.35
Type
journal article
Language
en
Open access
Licence
journals.asm.org/non-commercial-tdm-license (tdm)
Locations
  • Journal of Virology (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • HHS | NIH | National Cancer Institute (R01 CA119917)
  • HHS | National Institutes of Health (F31 CA180522)
Topics
  • Health Sciences › Medicine › Oncology › Viral-associated cancers and disorders
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer-related molecular mechanisms research
Keywords
Kaposi's sarcoma-associated herpesvirus, miRNA targetome, endothelial cells, RNA-induced silencing complex, viral oncogenesis, cell cycle regulation, apoptosis, glycolysis
MeSH terms
Cell Line, Transformed, Humans, RNA, Viral, Sarcoma, Kaposi, Sequence Analysis, RNA, Herpesvirus 8, Human, 3' Untranslated Regions, MicroRNAs, Endothelial Cells

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review