Kaposi's sarcoma-associated herpesvirus micrornas target GADD45B to protect infected cells from cell cycle arrest and apoptosis

Journal of Virology

Volumn 91, Issue 3, 2017, Pages

  Liu, Xiaoyan ^a,b   Happel, Christine ^b   Ziegelbauer, Joseph M ^b  

^a ZHEJIANG UNIVERSITY   (China)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Cell cycle; DNA damage; Kaposi's sarcoma associated herpesvirus; MicroRNA

Indexed keywords

CASPASE 3; CASPASE 7; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45 BETA; MICRORNA; MICRORNA K9; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NUTLIN 3; UNCLASSIFIED DRUG; VIRUS RNA; 3' UNTRANSLATED REGION; BIOLOGICAL MARKER; DIFFERENTIATION ANTIGEN; GADD45B PROTEIN, HUMAN; IMIDAZOLE DERIVATIVE; PIPERAZINE DERIVATIVE;

3' UNTRANSLATED REGION; APOPTOSIS; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; DNA CONTENT; DNA DAMAGE; G2 PHASE CELL CYCLE CHECKPOINT; GADD45B GENE; GENE REPRESSION; GENE TARGETING; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 8; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; CELL CYCLE CHECKPOINT; CELL LINE; DRUG EFFECTS; ENDOTHELIUM CELL; GENE EXPRESSION REGULATION; GENETICS; HERPES VIRUS INFECTION; HOST PATHOGEN INTERACTION; PHYSIOLOGY; RNA INTERFERENCE; VIROLOGY;

3' UNTRANSLATED REGIONS; ANTIGENS, DIFFERENTIATION; APOPTOSIS; BIOMARKERS; CELL CYCLE CHECKPOINTS; CELL LINE; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; HERPESVIRIDAE INFECTIONS; HERPESVIRUS 8, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; IMIDAZOLES; MICRORNAS; PIPERAZINES; RNA INTERFERENCE; RNA, VIRAL;

EID: 85010903987     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02045-16     Document Type: Article

References (54)

1. 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.
2. Haecker I, Gay LA, Yang Y, Hu J, Morse AM, McIntyre LM, 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.
3. Fabian MR, Sonenberg N, Filipowicz W. 2010. Regulation of mRNA translation and stability by microRNAs. Annu Rev Biochem 79:351-379. https://doi.org/10.1146/annurev-biochem-060308-103103.
4. Skalsky RL, Cullen BR. 2010. Viruses, microRNAs, and host interactions. Annu Rev Microbiol 64:123-141.
5. Ramalingam D, Kieffer-Kwon P, Ziegelbauer JM. 2012. Emerging themes from EBV and KSHV microRNA targets. Viruses 4:1687-1710. https://doi.org/10.3390/v4091687.
6. Boss IW, Plaisance KB, Renne R. 2009. Role of virus-encoded microRNAs in herpesvirus biology. Trends Microbiol 17:544-553. https://doi.org/10.1016/j.tim.2009.09.002.
7. 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.
8. 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.
9. Trigg BJ, Ferguson BJ. 2015. Functions of DNA damage machinery in the innate immune response to DNA virus infection. Curr Opin Virol 15: 56-62. https://doi.org/10.1016/j.coviro.2015.08.001.
10. Ou DL, Shyue SK, Lin LI, Feng ZR, Liou JY, Fan HH, Lee BS, Hsu C, Cheng AL. 2015. Growth arrest DNA damage-inducible gene 45 gamma expression as a prognostic and predictive biomarker in hepatocellular carcinoma. Oncotarget 6:27953-27965. https://doi.org/10.18632/oncotarget.4446.
11. Michaelis KA, Knox AJ, Xu M, Kiseljak-Vassiliades K, Edwards MG, Geraci M, Kleinschmidt-DeMasters BK, Lillehei KO, Wierman ME. 2011. Identification of growth arrest and DNA-damage-inducible gene beta (GADD45beta) as a novel tumor suppressor in pituitary gonadotrope tumors. Endocrinology 152:3603-3613. https://doi.org/10.1210/en.2011-0109.
12. Ou DL, Shen YC, Yu SL, Chen KF, Yeh PY, Fan HH, Feng WC, Wang CT, Lin LI, Hsu C, Cheng AL. 2010. Induction of DNA damage-inducible gene GADD45beta contributes to sorafenib-induced apoptosis in hepatocellular carcinoma cells. Cancer Res 70:9309-9318. https://doi.org/10.1158/0008-5472.CAN-10-1033.
13. Liebermann DA, Hoffman B. 2002. Myeloid differentiation (MyD) primary response genes in hematopoiesis. Oncogene 21:3391-3402. https://doi.org/10.1038/sj.onc.1205312.
14. Yang J, Zhu H, Murphy TL, Ouyang W, Murphy KM. 2001. IL-18-stimulated GADD45 beta required in cytokine-induced, but not TCRinduced, IFN-gamma production. Nat Immunol 2:157-164. https://doi.org/10.1038/84264.
15. De Smaele E, Zazzeroni F, Papa S, Nguyen DU, Jin R, Jones J, Cong R, Franzoso G. 2001. Induction of gadd45beta by NF-kappaB downregulates pro-apoptotic JNK signalling. Nature 414:308-313. https://doi.org/10.1038/35104560.
16. Takekawa M, Tatebayashi K, Itoh F, Adachi M, Imai K, Saito H. 2002. Smad-dependent GADD45beta expression mediates delayed activation of p38 MAP kinase by TGF-beta. EMBO J 21:6473-6482. https://doi.org/10.1093/emboj/cdf643.
17. Lang R, Patel D, Morris JJ, Rutschman RL, Murray PJ. 2002. Shaping gene expression in activated and resting primary macrophages by IL-10. J Immunol 169:2253-2263. https://doi.org/10.4049/jimmunol.169.5.2253.
18. Salerno DM, Tront JS, Hoffman B, Liebermann DA. 2012. Gadd45a and Gadd45b modulate innate immune functions of granulocytes and macrophages by differential regulation of p38 and JNK signaling. J Cell Physiol 227:3613-3620. https://doi.org/10.1002/jcp.24067.
19. Kim JH, Qu A, Reddy JK, Gao B, Gonzalez FJ. 2014. Hepatic oxidative stress activates the Gadd45b gene by way of degradation of the transcriptional repressor STAT3. Hepatology 59:695-704. https://doi.org/10.1002/hep.26683.
20. Davis DA, Rinderknecht AS, Zoeteweij JP, Aoki Y, Read-Connole EL, Tosato G, Blauvelt A, Yarchoan R. 2001. Hypoxia induces lytic replication of Kaposi sarcoma-associated herpesvirus. Blood 97:3244-3250. https://doi.org/10.1182/blood.V97.10.3244.
21. Wang V, Davis DA, Haque M, Huang LE, Yarchoan R. 2005. Differential gene up-regulation by hypoxia-inducible factor-1alpha and hypoxiainducible factor-2alpha in HEK293T cells. Cancer Res 65:3299-3306.
22. 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.
23. 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.
24. Thomson DW, Bracken CP, Szubert JM, Goodall GJ. 2013. On measuring miRNAs after transient transfection of mimics or antisense inhibitors. PLoS One 8:e55214. https://doi.org/10.1371/journal.pone.0055214.
25. Secchiero P, Barbarotto E, Tiribelli M, Zerbinati C, di Iasio MG, Gonelli A, Cavazzini F, Campioni D, Fanin R, Cuneo A, Zauli G. 2006. Functional integrity of the p53-mediated apoptotic pathway induced by the nongenotoxic agent nutlin-3 in B-cell chronic lymphocytic leukemia (B-CLL). Blood 107:4122-4129. https://doi.org/10.1182/blood-2005-11-4465.
26. Vassilev LT, Vu BT, Graves B, Carvajal D, Podlaski F, Filipovic Z, Kong N, Kammlott U, Lukacs C, Klein C, Fotouhi N, Liu EA. 2004. In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science 303:844-848. https://doi.org/10.1126/science.1092472.
27. Fan W, Bubman D, Chadburn A, Harrington WJ, Jr, Cesarman E, Knowles DM. 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. https://doi.org/10.1128/JVI.79.2.1244-1251.2005.
28. Vereide DT, Seto E, Chiu YF, Hayes M, Tagawa T, Grundhoff A, Hammerschmidt W, Sugden B. 2014. Epstein-Barr virus maintains lymphomas via its miRNAs. Oncogene 33:1258-1264. https://doi.org/10.1038/onc.2013.71.
29. Higgs MR, Lerat H, Pawlotsky JM. 2010. Downregulation of Gadd45beta expression by hepatitis C virus leads to defective cell cycle arrest. Cancer Res 70:4901-4911. https://doi.org/10.1158/0008-5472.CAN-09-4554.
30. Poole LJ, Yu Y, Kim PS, Zheng QZ, Pevsner J, Hayward GS. 2002. Altered patterns of cellular gene expression in dermal microvascular endothelial cells infected with Kaposi's sarcoma-associated herpesvirus. J Virol 76: 3395-3420. https://doi.org/10.1128/JVI.76.7.3395-3420.2002.
31. Wang L, Damania B. 2008. Kaposi's sarcoma-associated herpesvirus con-fers a survival advantage to endothelial cells. Cancer Res 68:4640-4648. https://doi.org/10.1158/0008-5472.CAN-07-5988.
32. Yu F, Harada JN, Brown HJ, Deng H, Song MJ, Wu TT, Kato-Stankiewicz J, Nelson CG, Vieira J, Tamanoi F, Chanda SK, Sun R. 2007. Systematic identification of cellular signals reactivating Kaposi sarcomaassociated herpesvirus. PLoS Pathog 3:e44. https://doi.org/10.1371/journal.ppat.0030044.
33. Turnell AS, Grand RJ. 2012. DNA viruses and the cellular DNA-damage response. J Gen Virol 93:2076-2097. https://doi.org/10.1099/vir.0.044412-0.
34. Hollingworth R, Grand RJ. 2015. Modulation of DNA damage and repair pathways by human tumour viruses. Viruses 7:2542-2591. https://doi.org/10.3390/v7052542.
35. McKinney CC, Hussmann KL, McBride AA. 2015. The role of the DNA damage response throughout the papillomavirus life cycle. Viruses 7:2450-2469. https://doi.org/10.3390/v7052450.
36. Leidal AM, Cyr DP, Hill RJ, Lee PW, McCormick C. 2012. Subversion of autophagy by Kaposi's sarcoma-associated herpesvirus impairs oncogene-induced senescence. Cell Host Microbe 11:167-180. https://doi.org/10.1016/j.chom.2012.01.005.
37. Lakin ND, Jackson SP. 1999. Regulation of p53 in response to DNA damage. Oncogene 18:7644-7655. https://doi.org/10.1038/sj.onc.1203015.
38. Katano H, Sato Y, Sata T. 2001. Expression of p53 and human herpesvirus-8 (HHV-8)-encoded latency-associated nuclear antigen with inhibition of apoptosis in HHV-8-associated malignancies. Cancer 92:3076-3084. https://doi.org/10.1002/1097-0142(20011215)92:12<3076::AID-CNCR10117>3.0.CO;2-D.
39. Petre CE, Sin SH, Dittmer DP. 2007. Functional p53 signaling in Kaposi's sarcoma-associated herpesvirus lymphomas: implications for therapy. J Virol 81:1912-1922. https://doi.org/10.1128/JVI.01757-06.
40. Nador RG, Cesarman E, Chadburn A, Dawson DB, Ansari MQ, Sald J, Knowles DM. 1996. Primary effusion lymphoma: a distinct clinicopathologic entity associated with the Kaposi's sarcoma-associated herpes virus. Blood 88:645-656.
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.
42. Nakamura H, Li M, Zarycki J, Jung JU. 2001. Inhibition of p53 tumor suppressor by viral interferon regulatory factor. J Virol 75:7572-7582. https://doi.org/10.1128/JVI.75.16.7572-7582.2001.
43. Rivas C, Thlick AE, Parravicini C, Moore PS, Chang Y. 2001. Kaposi's sarcoma-associated herpesvirus LANA2 is a B-cell-specific latent viral protein that inhibits p53. J Virol 75:429-438. https://doi.org/10.1128/JVI.75.1.429-438.2001.
44. Si H, Robertson ES. 2006. Kaposi's sarcoma-associated herpesvirusencoded latency-associated nuclear antigen induces chromosomal instability through inhibition of p53 function. J Virol 80:697-709. https://doi.org/10.1128/JVI.80.2.697-709.2006.
45. Sarek G, Kurki S, Enback J, Iotzova G, Haas J, Laakkonen P, Laiho M, Ojala PM. 2007. Reactivation of the p53 pathway as a treatment modality for KSHV-induced lymphomas. J Clin Investig 117:1019-1028. https://doi.org/10.1172/JCI30945.
46. Paudel N, Sadagopan S, Chakraborty S, Sarek G, Ojala PM, Chandran B. 2012 Kaposi's sarcoma-associated herpesvirus latency-associated nuclear antigen interacts with multifunctional angiogenin to utilize its antiapoptotic functions. J Virol 86:5974-5991. https://doi.org/10.1128/JVI.00070-12.
47. Sarek G, Ojala PM. 2007. p53 reactivation kills KSHV lymphomas efficiently in vitro and in vivo: new hope for treating aggressive viral lymphomas. Cell Cycle 6:2205-2209. https://doi.org/10.4161/cc.6.18.4730.
48. Ye F, Lattif AA, Xie J, Weinberg A, Gao S. 2012. Nutlin-3 induces apoptosis, disrupts viral latency and inhibits expression of angiopoietin-2 in Kaposi sarcoma tumor cells. Cell Cycle 11:1393-1399. https://doi.org/10.4161/cc.19756.
49. Abdollahi A, Lord KA, Hoffman-Liebermann B, Liebermann DA. 1991. Sequence and expression of a cDNA encoding MyD118: a novel myeloid differentiation primary response gene induced by multiple cytokines. Oncogene 6:165-167.
50. An J, Lichtenstein AK, Brent G, Rettig MB. 2002. The Kaposi sarcomaassociated herpesvirus (KSHV) induces cellular interleukin 6 expression: role of the KSHV latency-associated nuclear antigen and the AP1 response element. Blood 99:649-654. https://doi.org/10.1182/blood.V99.2.649.
51. Ye F, Zhou F, Bedolla RG, Jones T, Lei X, Kang T, Guadalupe M, Gao SJ. 2011 Reactive oxygen species hydrogen peroxide mediates Kaposi's sarcoma-associated herpesvirus reactivation from latency. PLoS Pathog 7:e1002054. https://doi.org/10.1371/journal.ppat.1002054.
52. Davis DA, Naiman NE, Wang V, Shrestha P, Haque M, Hu D, Anagho HA, Carey RF, Davidoff KS, Yarchoan R. 2015. Identification of caspase cleavage sites in KSHV latency-associated nuclear antigen and their effects on caspase-related host defense responses. PLoS Pathog 11:e1005064. https://doi.org/10.1371/journal.ppat.1005064.
53. Marshall V, Parks T, Bagni R, Wang CD, Samols MA, Hu J, Wyvil KM, Aleman K, Little RF, Yarchoan R, Renne R, Whitby D. 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. https://doi.org/10.1086/511434.
54. Janssen HL, Reesink HW, Lawitz EJ, Zeuzem S, Rodriguez-Torres M, Patel K, van der Meer AJ, Patick AK, Chen A, Zhou Y, Persson R, King BD, Kauppinen S, Levin AA, Hodges MR. 2013. Treatment of HCV infection by targeting microRNA. N Engl J Med 368:1685-1694. https://doi.org/10.1056/NEJMoa1209026.