MicroRNA miR-21 attenuates human cytomegalovirus replication in neural cells by targeting Cdc25a

Journal of Virology

Volumn 89, Issue 2, 2015, Pages 1070-1082

  Fu, Ya Ru ^a   Liu, Xi Juan ^a   Li, Xiao Jun ^a   Shen, Zhang zhou ^a   Yang, Bo ^a   Wu, Cong Cong ^a   Li, Jia Fu ^b   Miao, Ling Feng ^a   Ye, Han Qing ^a   Qiao, Guan Hua ^a   Rayner, Simon ^a   Chavanas, Stéphane ^c   Davrinche, Christian ^c   Britt, William J ^d   Tang, Qiyi ^e   McVoy, Michael ^f   Mocarski, Edward ^g   Luo, Min Hua ^a  

^a WUHAN INSTITUTE OF VIROLOGY   (China)

^b WUHAN UNIVERSITY   (China)

^c INSERM   (France)

^d University of Alabama at Birmingham   (United States)

^e PONCE SCHOOL OF MEDICINE   (Puerto Rico)

^f VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^g EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA 21; PROTEIN CDC25A; REGULATOR PROTEIN; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; CDC25A PROTEIN, HUMAN; MICRORNA; MIRN21 MICRORNA, HUMAN; PROTEIN TYROSINE PHOSPHATASE;

ARTICLE; ASTROCYTOMA CELL LINE; CENTRAL NERVOUS SYSTEM INFECTION; CONTROLLED STUDY; CYTOMEGALOVIRUS INFECTION; DOWN REGULATION; GENE OVEREXPRESSION; GENE PRODUCT; GENE REPRESSION; GENETIC TRANSFECTION; GLIOBLASTOMA CELL LINE; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; IE1 GENE; NEURAL STEM CELL; NEUROPATHOLOGY; NONHUMAN; PP71 GENE; PROGENY; PROTEIN TARGETING; TRANSCRIPTION REGULATION; U 251MG CELL LINE; UL26 GENE; VIROGENESIS; VIRUS CELL INTERACTION; VIRUS GENE; VIRUS INHIBITION; VIRUS REPLICATION; CELL CULTURE; CYTOMEGALOVIRUS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; VIROLOGY;

HUMAN HERPESVIRUS 5;

CDC25 PHOSPHATASES; CELLS, CULTURED; CYTOMEGALOVIRUS; HOST-PATHOGEN INTERACTIONS; HUMANS; MICRORNAS; NEURAL STEM CELLS; VIRUS REPLICATION;

EID: 84920811212     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01740-14     Document Type: Article

References (87)

1. Boppana SB, Ross SA, Shimamura M, Palmer AL, Ahmed A, Michaels MG, Sanchez PJ, Bernstein DI, Tolan RW, Jr, Novak Z, Chowdhury N, Britt WJ, Fowler KB. 2011. Saliva polymerase-chain-reaction assay for cytomegalovirus screening in newborns. N Engl J Med 364:2111-2118. http://dx.doi.org/10.1056/NEJMoa1006561.
2. Misono S, Sie KC, Weiss NS, Huang ML, Boeckh M, Norton SJ, Yueh B. 2011. Congenital cytomegalovirus infection in pediatric hearing loss. Arch Otolaryngol Head Neck Surg 137:47-53. http://dx.doi.org/10.1001/archoto.2010.235.
3. Stagno S, Pass RF, Cloud G, Britt WJ, Henderson RE, Walton PD, Veren DA, Page F, Alford CA. 1986. Primary cytomegalovirus infection in pregnancy. Incidence, transmission to fetus, and clinical outcome. JAMA 256:1904-1908.
4. Mercorelli B, Lembo D, Palu G, Loregian A. 2011. Early inhibitors of human cytomegalovirus: state-of-art and therapeutic perspectives. Pharmacol Ther 131:309-329. http://dx.doi.org/10.1016/j.pharmthera.2011.04.007.
5. Cui X, Lee R, Adler SP, McVoy MA. 2013. Antibody inhibition of human cytomegalovirus spread in epithelial cell cultures. J Virol Methods 192: 44-50. http://dx.doi.org/10.1016/j.jviromet.2013.04.015.
6. Luo MH, Schwartz PH, Fortunato EA. 2008. Neonatal neural progenitor cells and their neuronal and glial cell derivatives are fully permissive for human cytomegalovirus infection. J Virol 82:9994-10007. http://dx.doi.org/10.1128/JVI.00943-08.
7. Ryckman BJ, Chase MC, Johnson DC. 2008. HCMV gH/gL/UL128-131 interferes with virus entry into epithelial cells: evidence for cell typespecific receptors. Proc Natl Acad Sci USA 105:14118-14123. http://dx.doi.org/10.1073/pnas.0804365105.
8. Sinzger C, Jahn G. 1996. Human cytomegalovirus cell tropism and pathogenesis. Intervirology 39:302-319.
9. Wang D, Shenk T. 2005. Human cytomegalovirus UL131 open reading frame is required for epithelial cell tropism. J Virol 79:10330-10338. http://dx.doi.org/10.1128/JVI.79.16.10330-10338.2005.
10. Cobbs CS. 2013. Cytomegalovirus and brain tumor: epidemiology, biology and therapeutic aspects. Curr Opin Oncol 25:682-688. http://dx.doi.org/10.1097/CCO.0000000000000005.
11. Cobbs CS, Harkins L, Samanta M, Gillespie GY, Bharara S, King PH, Nabors LB, Cobbs CG, Britt WJ. 2002. Human cytomegalovirus infection and expression in human malignant glioma. Cancer Res 62:3347-3350.
12. Miller G. 2009. Brain cancer A viral link to glioblastoma? Science 323:30-31. http://dx.doi.org/10.1126/science.323.5910.30.
13. Mitchell DA, Xie W, Schmittling R, Learn C, Friedman A, McLendon RE, Sampson JH. 2008. Sensitive detection of human cytomegalovirus in tumors and peripheral blood of patients diagnosed with glioblastoma. Neuro Oncol 10:10-18. http://dx.doi.org/10.1215/15228517-2007-035.
14. Duan YL, Ye HQ, Zavala AG, Yang CQ, Miao LF, Fu BS, Seo KS, Davrinche C, Luo MH, Fortunato EA. 2014. Maintenance of large numbers of virus genomes in human cytomegalovirus-infected T98G glioblastoma cells. J Virol 88:3861-3873. http://dx.doi.org/10.1128/JVI.01166-13.
15. Luo MH, Fortunato EA. 2007. Long-term infection and shedding of human cytomegalovirus in T98G glioblastoma cells. J Virol 81:10424-10436. http://dx.doi.org/10.1128/JVI.00866-07.
16. Boppana SB, Fowler KB, Vaid Y, Hedlund G, Stagno S, Britt WJ, Pass RF. 1997. Neuroradiographic findings in the newborn period and long-term outcome in children with symptomatic congenital cytomegalovirus infection. Pediatrics 99:409-414. http://dx.doi.org/10.1542/peds.99.3.409.
17. Boppana SB, Pass RF, Britt WJ, Stagno S, Alford CA. 1992. Symptomatic congenital cytomegalovirus infection: neonatal morbidity and mortality. Pediatr Infect Dis J 11:93-99. http://dx.doi.org/10.1097/00006454-199202000-00007.
18. Dahle AJ, Fowler KB, Wright JD, Boppana SB, Britt WJ, Pass RF. 2000. Longitudinal investigation of hearing disorders in children with congenital cytomegalovirus. J Am Acad Audiol 11:283-290.
19. Conboy TJ, Pass RF, Stagno S, Britt WJ, Alford CA, McFarland CE, Boll TJ. 1986. Intellectual development in school-aged children with asymptomatic congenital cytomegalovirus infection. Pediatrics 77:801-806.
20. Grosse SD, Ross DS, Dollard SC. 2008. Congenital cytomegalovirus (CMV) infection as a cause of permanent bilateral hearing loss: a quantitative assessment. J Clin Virol 41:57-62. http://dx.doi.org/10.1016/j.jcv.2007.09.004.
21. Pass RF, Stagno S, Myers GJ, Alford CA. 1980. Outcome of symptomatic congenital cytomegalovirus infection: results of long-term longitudinal follow-up. Pediatrics 66:758-762.
22. Revello MG, Zavattoni M, Furione M, Fabbri E, Gerna G. 2006. Preconceptional primary human cytomegalovirus infection and risk of congenital infection. J Infect Dis 193:783-787. http://dx.doi.org/10.1086/500509.
23. Schachtele SJ, Mutnal MB, Schleiss MR, Lokensgard JR. 2011. Cytomegalovirus-induced sensorineural hearing loss with persistent cochlear inflammation in neonatal mice. J Neurovirol 17:201-211. http://dx.doi.org/10.1007/s13365-011-0024-7.
24. Spector DH. 1996. Activation and regulation of human cytomegalovirus early genes. Intervirology 39:361-377.
25. Fehr AR, Yu D. 2013. Control the host cell cycle: viral regulation of the anaphase-promoting complex. J Virol 87:8818-8825. http://dx.doi.org/10.1128/JVI.00088-13.
26. Hertel L, Mocarski ES. 2004. Global analysis of host cell gene expression late during cytomegalovirus infection reveals extensive dysregulation of cell cycle gene expression and induction of pseudomitosis independent of US28 function. J Virol 78:11988-12011. http://dx.doi.org/10.1128/JVI.78.21.11988-12011.2004.
27. Jault FM, Jault JM, Ruchti F, Fortunato EA, Clark C, Corbeil J, Richman DD, Spector DH. 1995. Cytomegalovirus infection induces high levels of cyclins, phosphorylated Rb, and p53, leading to cell cycle arrest. J Virol 69:6697-6704.
28. Luo MH, Rosenke K, Czornak K, Fortunato EA. 2007. Human cytomegalovirus disrupts both ataxia telangiectasia mutated protein (ATM)-and ATM-Rad3-related kinase-mediated DNA damage responses during lytic infection. J Virol 81:1934-1950. http://dx.doi.org/10.1128/JVI.01670-06.
29. Saffert RT, Kalejta RF. 2006. Inactivating a cellular intrinsic immune defense mediated by Daxx is the mechanism through which the human cytomegalovirus pp71 protein stimulates viral immediate-early gene expression. J Virol 80:3863-3871. http://dx.doi.org/10.1128/JVI.80.8.3863-3871.2006.
30. Salvant BS, Fortunato EA, Spector DH. 1998. Cell cycle dysregulation by human cytomegalovirus: influence of the cell cycle phase at the time of infection and effects on cyclin transcription. J Virol 72:3729-3741.
31. Bogdanow B, Weisbach H, von Einem J, Straschewski S, Voigt S, Winkler M, Hagemeier C, Wiebusch L. 2013. Human cytomegalovirus tegument protein pp150 acts as a cyclin A2-CDK-dependent sensor of the host cell cycle and differentiation state. Proc Natl Acad Sci USA 110: 17510-17515. http://dx.doi.org/10.1073/pnas.1312235110.
32. Oduro JD, Uecker R, Hagemeier C, Wiebusch L. 2012. Inhibition of human cytomegalovirus immediate-early gene expression by cyclin A2-dependent kinase activity. J Virol 86:9369-9383. http://dx.doi.org/10.1128/JVI.07181-11.
33. Zydek M, Hagemeier C, Wiebusch L. 2010. Cyclin-dependent kinase activity controls the onset of the HCMV lytic cycle. PLoS Pathog 6:e1001096. http://dx.doi.org/10.1371/journal.ppat.1001096.
34. Casavant NC, Luo MH, Rosenke K, Winegardner T, Zurawska A, Fortunato EA. 2006. Potential role for p53 in the permissive life cycle of human cytomegalovirus. J Virol 80:8390-8401. http://dx.doi.org/10.1128/JVI.00505-06.
35. Skalsky RL, Cullen BR. 2010. Viruses, microRNAs, and host interactions. Annu Rev Microbiol 64:123-141. http://dx.doi.org/10.1146/annurev.micro.112408.134243.
36. Ambros V. 2004. The functions of animal microRNAs. Nature 431:350-355. http://dx.doi.org/10.1038/nature02871.
37. Bartel DP. 2004. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281-297. http://dx.doi.org/10.1016/S0092-8674(04)00045-5.
38. Kloosterman WP, Plasterk RH. 2006. The diverse functions of micro-RNAs in animal development and disease. Dev Cell 11:441-450. http://dx.doi.org/10.1016/j.devcel.2006.09.009.
39. Grey F, Tirabassi R, Meyers H, Wu G, McWeeney S, Hook L, Nelson JA. 2010. A viral microRNA downregulates multiple cell cycle genes through mRNA 5'UTRs. PLoS Pathog 6:e1000967. http://dx.doi.org/10.1371/journal.ppat.1000967.
40. Cameron JE, Fewell C, Yin Q, McBride J, Wang X, Lin Z, Flemington EK. 2008. Epstein-Barr virus growth/latency III program alters cellular microRNA expression. Virology 382:257-266. http://dx.doi.org/10.1016/j.virol.2008.09.018.
41. Wang FZ, Weber F, Croce C, Liu CG, Liao X, Pellett PE. 2008. Human cytomegalovirus infection alters the expression of cellular microRNA species that affect its replication. J Virol 82:9065-9074. http://dx.doi.org/10.1128/JVI.00961-08.
42. Buggele WA, Krause KE, Horvath CM. 2013. Small RNA profiling of influenza A virus-infected cells identifies miR-449b as a regulator of histone deacetylase 1 and interferon beta. PLoS One 8:e76560. http://dx.doi.org/10.1371/journal.pone.0076560.
43. Yan Q, Li W, Tang Q, Yao S, Lv Z, Feng N, Ma X, Bai Z, Zeng Y, Qin D, Lu C. 2013. Cellular microRNAs 498 and 320d regulate herpes simplex virus 1 induction of Kaposi's sarcoma-associated herpesvirus lytic replication by targeting RTA. PLoS One 8:e55832. http://dx.doi.org/10.1371/journal.pone.0055832.
44. Forte E, Luftig MA. 2011. The role of microRNAs in Epstein-Barr virus latency and lytic reactivation. Microbes Infect 13:1156-1167. http://dx.doi.org/10.1016/j.micinf.2011.07.007.
45. Catrina Ene AM, Borze I, Guled M, Costache M, Leen G, Sajin M, Ionica E, Chitu A, Knuutila S. 2014. MicroRNA expression profiles in Kaposi's sarcoma. Pathol Oncol Res 20:153-159. http://dx.doi.org/10.1007/s12253-013-9678-1.
46. Godshalk SE, Bhaduri-McIntosh S, Slack FJ. 2008. Epstein-Barr virusmediated dysregulation of human microRNA expression. Cell Cycle 7:3595-3600. http://dx.doi.org/10.4161/cc.7.22.7120.
47. Yang GD, Huang TJ, Peng LX, Yang CF, Liu RY, Huang HB, Chu QQ, Yang HJ, Huang JL, Zhu ZY, Qian CN, Huang BJ. 2013. Epstein-Barr virus-encoded LMP1 upregulates microRNA-21 to promote the resistance of nasopharyngeal carcinoma cells to cisplatin-induced apoptosis by suppressing PDCD4 and Fas-L. PLoS One 8:e78355. http://dx.doi.org/10.1371/journal.pone.0078355.
48. Chen Y, Chen J, Wang H, Shi J, Wu K, Liu S, Liu Y, Wu J. 2013. HCV-induced miR-21 contributes to evasion of host immune system by targeting MyD88 and IRAK1. PLoS Pathog 9:e1003248. http://dx.doi.org/10.1371/journal.ppat.1003248.
49. Li SQ, Zhu JG, Zhang WL, Chen YR, Zhang K, Popescu LM, Ma XL, Lau WB, Rong R, Yu XQ, Wang BB, Li YF, Xiao CS, Zhang MM, Wang SY, Yu LP, Chen AF, Yang XC, Cai J. 2011. Signature microRNA expression profile of essential hypertension and its novel link to human cytomegalovirus infection. Circulation 124:175-U154. http://dx.doi.org/10.1161/CIRCULATIONAHA.110.012237.
50. Luo MH, Hannemann H, Kulkarni AS, Schwartz PH, O'Dowd JM, Fortunato EA. 2010. Human cytomegalovirus infection causes premature and abnormal differentiation of human neural progenitor cells. J Virol 84:3528-3541. http://dx.doi.org/10.1128/JVI.02161-09.
51. Stark TJ, Arnold JD, Spector DH, Yeo GW. 2012. High-resolution profiling and analysis of viral and host small RNAs during human cytomegalovirus infection. J Virol 86:226-235. http://dx.doi.org/10.1128/JVI.05903-11.
52. Krichevsky AM, Gabriely G. 2009. miR-21: a small multi-faceted RNA. J Cell Mol Med 13:39-53. http://dx.doi.org/10.1111/j.1582-4934.2008.00556.x.
53. Asangani IA, Rasheed SA, Nikolova DA, Leupold JH, Colburn NH, Post S, Allgayer H. 2008. MicroRNA-21 (miR-21) posttranscriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene 27:2128-2136. http://dx.doi.org/10.1038/sj.onc.1210856.
54. Zhang JG, Wang JJ, Zhao F, Liu Q, Jiang K, Yang GH. 2010. Micro-RNA-21 (miR-21) represses tumor suppressor PTEN and promotes growth and invasion in non-small cell lung cancer (NSCLC). Clin Chim Acta 411:846-852. http://dx.doi.org/10.1016/j.cca.2010.02.074.
55. Zhu SM, Si ML, Wu HL, Mo YY. 2007. MicroRNA-21 targets the tumor suppressor gene tropomyosin 1 (TPM1). J Biol Chem 282:14328-14336. http://dx.doi.org/10.1074/jbc.M611393200.
56. Wang P, Zou F, Zhang X, Li H, Dulak A, Tomko RJ, Jr, Lazo JS, Wang Z, Zhang L, Yu J. 2009. microRNA-21 negatively regulates Cdc25A and cell cycle progression in colon cancer cells. Cancer Res 69:8157-8165. http://dx.doi.org/10.1158/0008-5472.CAN-09-1996.
57. Ray D, Kiyokawa H. 2008. CDC25A phosphatase: a rate-limiting oncogene that determines genomic stability. Cancer Res 68:1251-1253. http://dx.doi.org/10.1158/0008-5472.CAN-07-5983.
58. Boutros R, Lobjois V, Ducommun B. 2007. CDC25 phosphatases in cancer cells: key players? Good targets? Nat Rev Cancer 7:495-507. http://dx.doi.org/10.1038/nrc2169.
59. 1/S transition. J Virol 71:1629-1634.
60. 1 to S. J Virol 70:8850-8857.
61. Pan X, Li XJ, Liu XJ, Yuan H, Li JF, Duan YL, Ye HQ, Fu YR, Qiao GH, Wu CC, Yang B, Tian XH, Hu KH, Miao LF, Chen XL, Zheng J, Rayner S, Schwartz PH, Britt WJ, Xu J, Luo MH. 2013. Later passage neural progenitor cells from neonatal brain are more permissive for human cytomegalovirus infection. J Virol 87:10968-10979. http://dx.doi.org/10.1128/JVI.01120-13.
62. Shen ZZ, Pan X, Miao LF, Ye HQ, Chavanas S, Davrinche C, McVoy M, Luo MH. 2014. Comprehensive analysis of human cytomegalovirus microRNA expression during lytic and quiescent infection. PLoS One 9:e88531. http://dx.doi.org/10.1371/journal.pone.0088531.
63. Tamashiro JC, Hock LJ, Spector DH. 1982. Construction of a cloned library of the EcoRI fragments from the human cytomegalovirus genome (strain AD169). J Virol 42:547-557.
64. Fortunato EA, Dell'Aquila ML, Spector DH. 2000. Specific chromosome 1 breaks induced by human cytomegalovirus. Proc Natl Acad Sci USA 97:853-858. http://dx.doi.org/10.1073/pnas.97.2.853.
65. Su H, Yang JR, Xu T, Huang J, Xu L, Yuan Y, Zhuang SM. 2009. MicroRNA-101, downregulated in hepatocellular carcinoma, promotes apoptosis and suppresses tumorigenicity. Cancer Res 69:1135-1142. http://dx.doi.org/10.1158/0008-5472.CAN-08-2886.
66. Tiscornia G, Singer O, Verma IM. 2006. Production and purification of lentiviral vectors. Nat Protoc 1:241-245. http://dx.doi.org/10.1038/nprot.2006.37.
67. Lou Y, Yang X, Wang F, Cui Z, Huang Y. 2010. MicroRNA-21 promotes the cell proliferation, invasion and migration abilities in ovarian epithelial carcinomas through inhibiting the expression of PTEN protein. Int J Mol Med 26:819-827.
68. Chen C, Okayama H. 1987. High-efficiency transformation of mammalian cells by plasmid DNA. Mol Cell Biol 7:2745-2752.
69. Duan Y, Miao L, Ye H, Yang C, Fu B, Schwartz PH, Rayner S, Fortunato EA, Luo MH. 2012. A faster immunofluorescence assay for tracking infection progress of human cytomegalovirus. Acta Biochim Biophys Sinica 44:597-605. http://dx.doi.org/10.1093/abbs/gms041.
70. Wang HT, Wang B, Liu ZJ, Bai ZQ, Li L, Liu HY, Qian DM, Yan ZY, Song XX. 2009. Effect of human cytomegalovirus infection on nerve growth factor expression in human glioma U251 cells. Biomed Environ Sci 22:354-358. http://dx.doi.org/10.1016/S0895-3988(09)60068-4.
71. Gaspar M, Shenk T. 2006. Human cytomegalovirus inhibits a DNA damage response by mislocalizing checkpoint proteins. Proc Natl Acad Sci USA 103:2821-2826. http://dx.doi.org/10.1073/pnas.0511148103.
72. de Oliveira PE, Zhang L, Wang Z, Lazo JS. 2009. Hypoxia-mediated regulation of Cdc25A phosphatase by p21 and miR-21. Cell Cycle 8:3157-3164. http://dx.doi.org/10.4161/cc.8.19.9704.
73. Li C, Wang Y, Wang S, Wu B, Hao J, Fan H, Ju Y, Ding Y, Chen L, Chu X, Liu W, Ye X, Meng S. 2013. Hepatitis B virus mRNA-mediated miR-122 inhibition upregulates PTTG1-binding protein, which promotes hepatocellular carcinoma tumor growth and cell invasion. J Virol 87: 2193-2205. http://dx.doi.org/10.1128/JVI.02831-12.
74. 1-modulated P53 activity. Hepatology 55:730-741. http://dx.doi.org/10.1002/hep.24809.
75. Wang D, Cao L, Xu Z, Fang L, Zhong Y, Chen Q, Luo R, Chen H, Li K, Xiao S. 2013. miR-125b reduces porcine reproductive and respiratory syndrome virus replication by negatively regulating the NF-κB pathway. PLoS One 8:e55838. http://dx.doi.org/10.1371/journal.pone.0055838.
76. Barth S, Pfuhl T, Mamiani A, Ehses C, Roemer K, Kremmer E, Jaker C, Hock J, Meister G, Grasser FA. 2008. Epstein-Barr virus-encoded microRNA miR-BART2 downregulates the viral DNA polymerase BALF5. Nucleic Acids Res 36:666-675.
77. Lei X, Bai Z, Ye F, Xie J, Kim CG, Huang Y, Gao SJ. 2010. Regulation of NF-κB inhibitor IκBα and viral replication by a KSHV microRNA. Nat Cell Biol 12:193-199. http://dx.doi.org/10.1038/ncb2019.
78. Lin X, Liang D, He Z, Deng Q, Robertson ES, Lan K. 2011. miR-K12-7-5p encoded by Kaposi's sarcoma-associated herpesvirus stabilizes the latent state by targeting viral ORF50/RTA. PLoS One 6:e16224. http://dx.doi.org/10.1371/journal.pone.0016224.
79. Lu CC, Li Z, Chu CY, Feng J, Sun R, Rana TM. 2010. MicroRNAs encoded by Kaposi's sarcoma-associated herpesvirus regulate viral life cycle. EMBO Rep 11:784-790. http://dx.doi.org/10.1038/embor.2010.132.
80. 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. http://dx.doi.org/10.1371/journal.ppat.0030163.
81. Stern-Ginossar N, Saleh N, Goldberg MD, Prichard M, Wolf DG, Mandelboim O. 2009. Analysis of human cytomegalovirus-encoded microRNA activity during infection. J Virol 83:10684-10693. http://dx.doi.org/10.1128/JVI.01292-09.
82. Hook LM, Grey F, Grabski R, Tirabassi R, Doyle T, Hancock M, Landais I, Jeng S, McWeeney S, Britt W, Nelson JA. 2014. Cytomegalovirus miRNAs target secretory pathway genes to facilitate formation of the virion assembly compartment and reduce cytokine secretion. Cell Host Microbe 15:363-373. http://dx.doi.org/10.1016/j.chom.2014.02.004.
83. Chen Y, Shen A, Rider PJ, Yu Y, Wu K, Mu Y, Hao Q, Liu Y, Gong H, Zhu Y, Liu F, Wu J. 2011. A liver-specific microRNA binds to a highly conserved RNA sequence of hepatitis B virus and negatively regulates viral gene expression and replication. FASEB J 25:4511-4521. http://dx.doi.org/10.1096/fj.11-187781.
84. Harkins L, Volk AL, Samanta M, Mikolaenko I, Britt WJ, Bland KI, Cobbs CS. 2002. Specific localization of human cytomegalovirus nucleic acids and proteins in human colorectal cancer. Lancet 360:1557-1563. http://dx.doi.org/10.1016/S0140-6736(02)11524-8.
85. Michaelis M, Doerr HW, Cinatl J. 2009. The story of human cytomegalovirus and cancer: increasing evidence and open questions. Neoplasia 11:1-9.
86. Stragliotto G, Rahbar A, Solberg NW, Lilja A, Taher C, Orrego A, Bjurman B, Tammik C, Skarman P, Peredo I, Soderberg-Naucler C. 2013. Effects of valganciclovir as an add-on therapy in patients with cytomegalovirus-positive glioblastoma: a randomized, double-blind, hypothesis-generating study. Int J Cancer 133:1204-1213. http://dx.doi.org/10.1002/ijc.28111.
87. Yamashita Y, Kasugai I, Sato M, Tanuma N, Sato I, Nomura M, Yamashita K, Sonoda Y, Kumabe T, Tominaga T, Katakura R, Shima H. 2010. CDC25A mRNA levels significantly correlate with Ki-67 expression in human glioma samples. J Neurooncol 100:43-49. http://dx.doi.org/10.1007/s11060-010-0147-3.