Chloroquine triggers Epstein-Barr virus replication through phosphorylation of KAP1/TRIM28 in Burkitt lymphoma cells

PLoS Pathogens

Volumn 13, Issue 3, 2017, Pages

  Li, Xiaofan ^a   Burton, Eric M ^b   Bhaduri McIntosh, Sumita ^a,b  

^a STONY BROOK UNIVERSITY   (United States)

^b STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; CHLOROQUINE; COREPRESSOR PROTEIN; KRUEPPEL ASSOCIATED BOX ASSOCIATED PROTEIN 1; PEPTIDES AND PROTEINS; RNA RECOGNITION MOTIF PROTEIN; SMALL INTERFERING RNA; TRIPARTITE MOTIF CONTAINING PROTEIN 28; UNCLASSIFIED DRUG; ANTIMALARIAL AGENT; REPRESSOR PROTEIN; TRIM28 PROTEIN, HUMAN;

ARTICLE; B CELL LYMPHOMA CELL; BURKITT LYMPHOMA CELL LINE; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; EPSTEIN BARR VIRUS INFECTION; FLOW CYTOMETRY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; LYMPHOBLASTOID CELL; MALARIA FALCIPARUM; PLASMID; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSCRIPTION REGULATION; VIRUS REPLICATION; BURKITT LYMPHOMA; DRUG EFFECTS; EPSTEIN BARR VIRUS; FLUORESCENT ANTIBODY TECHNIQUE; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; POLYMERASE CHAIN REACTION; TUMOR CELL LINE; VIROLOGY; VIRUS ACTIVATION;

ANTIMALARIALS; ATAXIA TELANGIECTASIA MUTATED PROTEINS; BURKITT LYMPHOMA; CELL LINE, TUMOR; CHLOROQUINE; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; HERPESVIRUS 4, HUMAN; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; PHOSPHORYLATION; POLYMERASE CHAIN REACTION; REPRESSOR PROTEINS; RNA, SMALL INTERFERING; TRANSFECTION; VIRUS ACTIVATION; VIRUS REPLICATION;

EID: 85016471291     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1006249     Document Type: Article

References (45)

1. Karmali RA, Horrobin DF, Menezes J, Patel P, Musto J, (1978) Chloroquine enhances Epstein-Barr virus expression. Nature275: 444–445. 211434
2. Lenoir G, Geser A, (1979) Effect of chloroquine on Epstein-Barr virus expression. Nature282: 758. 229421
3. Young LS, Rickinson AB, (2004) Epstein-Barr virus: 40 years on. Nat Rev Cancer4: 757–768. doi: 10.1038/nrc145215510157
4. Daigle D, Megyola C, El-Guindy A, Gradoville L, Tuck D, et al. (2010) Upregulation of STAT3 marks Burkitt lymphoma cells refractory to Epstein-Barr virus lytic cycle induction by HDAC inhibitors. J Virol84: 993–1004. doi: 10.1128/JVI.01745-0919889776
5. Hill ER, Koganti S, Zhi J, Megyola C, Freeman AF, et al. (2013) Signal transducer and activator of transcription 3 limits Epstein-Barr virus lytic activation in B lymphocytes. J Virol87: 11438–11446. doi: 10.1128/JVI.01762-1323966384
6. Bhaduri-McIntosh S, Miller G, (2006) Cells lytically infected with Epstein-Barr virus are detected and separable by immunoglobulins from EBV-seropositive individuals. J Virol Methods137: 103–114. doi: 10.1016/j.jviromet.2006.06.00616843536
7. King CA, Li X, Barbachano-Guerrero A, Bhaduri-McIntosh S, (2015) STAT3 Regulates Lytic Activation of Kaposi's Sarcoma-Associated Herpesvirus. J Virol89: 11347–11355. doi: 10.1128/JVI.02008-1526339061
8. Cheng CT, Kuo CY, Ann DK, (2014) KAPtain in charge of multiple missions: Emerging roles of KAP1. World J Biol Chem5: 308–320. doi: 10.4331/wjbc.v5.i3.30825225599
9. Iyengar S, Farnham PJ, (2011) KAP1 protein: an enigmatic master regulator of the genome. J Biol Chem286: 26267–26276. doi: 10.1074/jbc.R111.25256921652716
10. White D, Rafalska-Metcalf IU, Ivanov AV, Corsinotti A, Peng H, et al. (2012) The ATM substrate KAP1 controls DNA repair in heterochromatin: regulation by HP1 proteins and serine 473/824 phosphorylation. Mol Cancer Res10: 401–414. doi: 10.1158/1541-7786.MCR-11-013422205726
11. Ayrapetov MK, Gursoy-Yuzugullu O, Xu C, Xu Y, Price BD, (2014) DNA double-strand breaks promote methylation of histone H3 on lysine 9 and transient formation of repressive chromatin. Proc Natl Acad Sci U S A111: 9169–9174. doi: 10.1073/pnas.140356511124927542
12. Goodarzi AA, Noon AT, Deckbar D, Ziv Y, Shiloh Y, et al. (2008) ATM signaling facilitates repair of DNA double-strand breaks associated with heterochromatin. Mol Cell31: 167–177. doi: 10.1016/j.molcel.2008.05.01718657500
13. Ziv Y, Bielopolski D, Galanty Y, Lukas C, Taya Y, et al. (2006) Chromatin relaxation in response to DNA double-strand breaks is modulated by a novel ATM- and KAP-1 dependent pathway. Nat Cell Biol8: 870–876. doi: 10.1038/ncb144616862143
14. Fredriksson S, Gullberg M, Jarvius J, Olsson C, Pietras K, et al. (2002) Protein detection using proximity-dependent DNA ligation assays. Nat Biotechnol20: 473–477. doi: 10.1038/nbt0502-47311981560
15. Leuchowius KJ, Weibrecht I, Soderberg O (2011) In situ proximity ligation assay for microscopy and flow cytometry. Curr Protoc Cytom Chapter 9: Unit 9 36.
16. Bakkenist CJ, Kastan MB, (2003) DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature421: 499–506. doi: 10.1038/nature0136812556884
17. Kastan MB, (2008) DNA damage responses: mechanisms and roles in human disease: 2007 G.H.A. Clowes Memorial Award Lecture. Mol Cancer Res6: 517–524. doi: 10.1158/1541-7786.MCR-08-002018403632
18. Hagemeier SR, Barlow EA, Meng Q, Kenney SC, (2012) The cellular ataxia telangiectasia-mutated kinase promotes epstein-barr virus lytic reactivation in response to multiple different types of lytic reactivation-inducing stimuli. J Virol86: 13360–13370. doi: 10.1128/JVI.01850-1223015717
19. Kudoh A, Fujita M, Zhang L, Shirata N, Daikoku T, et al. (2005) Epstein-Barr virus lytic replication elicits ATM checkpoint signal transduction while providing an S-phase-like cellular environment. J Biol Chem280: 8156–8163. doi: 10.1074/jbc.M41140520015611093
20. Wang'ondu R, Teal S, Park R, Heston L, Delecluse H, et al. (2015) DNA Damage Signaling Is Induced in the Absence of Epstein-Barr Virus (EBV) Lytic DNA Replication and in Response to Expression of ZEBRA. PLoS One10: e0126088. doi: 10.1371/journal.pone.012608825950714
21. Heston L, El-Guindy A, Countryman J, Dela Cruz C, Delecluse HJ, et al. (2006) Amino acids in the basic domain of Epstein-Barr virus ZEBRA protein play distinct roles in DNA binding, activation of early lytic gene expression, and promotion of viral DNA replication. J Virol80: 9115–9133. doi: 10.1128/JVI.00909-0616940523
22. Chang PC, Fitzgerald LD, Van Geelen A, Izumiya Y, Ellison TJ, et al. (2009) Kruppel-associated box domain-associated protein-1 as a latency regulator for Kaposi's sarcoma-associated herpesvirus and its modulation by the viral protein kinase. Cancer Res69: 5681–5689. doi: 10.1158/0008-5472.CAN-08-457019584288
23. Rauwel B, Jang SM, Cassano M, Kapopoulou A, Barde I, et al. (2015) Release of human cytomegalovirus from latency by a KAP1/TRIM28 phosphorylation switch. Elife4.
24. King CA, (2013) Kaposi's sarcoma-associated herpesvirus kaposin B induces unique monophosphorylation of STAT3 at serine 727 and MK2-mediated inactivation of the STAT3 transcriptional repressor TRIM28. J Virol87: 8779–8791. doi: 10.1128/JVI.02976-1223740979
25. Bentz GL, Moss CR, 2ndWhitehurst CB, Moody CA, Pagano JS, (2015) LMP1-Induced Sumoylation Influences the Maintenance of Epstein-Barr Virus Latency through KAP1. J Virol89: 7465–7477. doi: 10.1128/JVI.00711-1525948750
26. Gjyshi O, Roy A, Dutta S, Veettil MV, Dutta D, et al. (2015) Activated Nrf2 Interacts with Kaposi's Sarcoma-Associated Herpesvirus Latency Protein LANA-1 and Host Protein KAP1 To Mediate Global Lytic Gene Repression. J Virol89: 7874–7892. doi: 10.1128/JVI.00895-1525995248
27. Sun R, Liang D, Gao Y, Lan K, (2014) Kaposi's sarcoma-associated herpesvirus-encoded LANA interacts with host KAP1 to facilitate establishment of viral latency. J Virol88: 7331–7344. doi: 10.1128/JVI.00596-1424741090
28. Yang M, Huang L, Li X, Kuang E, (2016) Chloroquine inhibits lytic replication of Kaposi's sarcoma-associated herpesvirus by disrupting mTOR and p38-MAPK activation. Antiviral Res133: 223–233. doi: 10.1016/j.antiviral.2016.08.01027521848
29. Rochford R, Cannon MJ, Moormann AM, (2005) Endemic Burkitt's lymphoma: a polymicrobial disease?Nat Rev Microbiol3: 182–187. doi: 10.1038/nrmicro108915685227
30. Laichalk LL, Thorley-Lawson DA, (2005) Terminal differentiation into plasma cells initiates the replicative cycle of Epstein-Barr virus in vivo. J Virol79: 1296–1307. doi: 10.1128/JVI.79.2.1296-1307.200515613356
31. Moss DJ, Burrows SR, Castelino DJ, Kane RG, Pope JH, et al. (1983) A comparison of Epstein-Barr virus-specific T-cell immunity in malaria-endemic and -nonendemic regions of Papua New Guinea. Int J Cancer31: 727–732. 6305850
32. Whittle HC, Brown J, Marsh K, Blackman M, Jobe O, et al. (1990) The effects of Plasmodium falciparum malaria on immune control of B lymphocytes in Gambian children. Clin Exp Immunol80: 213–218. 1972671
33. Whittle HC, Brown J, Marsh K, Greenwood BM, Seidelin P, et al. (1984) T-cell control of Epstein-Barr virus-infected B cells is lost during P. falciparum malaria. Nature312: 449–450. 6095104
34. Geser A, de The G, Lenoir G, Day NE, Williams EH, (1982) Final case reporting from the Ugandan prospective study of the relationship between EBV and Burkitt's lymphoma. Int J Cancer29: 397–400. 6282763
35. Aya T, Kinoshita T, Imai S, Koizumi S, Mizuno F, et al. (1991) Chromosome translocation and c-MYC activation by Epstein-Barr virus and Euphorbia tirucalli in B lymphocytes. Lancet337: 1190. 1673740
36. van den Bosch C, Griffin BE, Kazembe P, Dziweni C, Kadzamira L, (1993) Are plant factors a missing link in the evolution of endemic Burkitt's lymphoma?Br J Cancer68: 1232–1235. 8260378
37. Geser A, Brubaker G, Draper CC, (1989) Effect of a malaria suppression program on the incidence of African Burkitt's lymphoma. Am J Epidemiol129: 740–752. 2923122
38. Maclean KH, Dorsey FC, Cleveland JL, Kastan MB, (2008) Targeting lysosomal degradation induces p53-dependent cell death and prevents cancer in mouse models of lymphomagenesis. J Clin Invest118: 79–88. doi: 10.1172/JCI3370018097482
39. Frosch AE, Venkatesan M, Laufer MK, (2011) Patterns of chloroquine use and resistance in sub-Saharan Africa: a systematic review of household survey and molecular data. Malar J10: 116. doi: 10.1186/1475-2875-10-11621554692
40. Hui-Yuen J, Koganti S, Bhaduri-McIntosh S, (2014) Human B cell immortalization for monoclonal antibody production. Methods Mol Biol1131: 183–189. doi: 10.1007/978-1-62703-992-5_1124515466
41. Bolderson E, Savage KI, Mahen R, Pisupati V, Graham ME, et al. (2012) Kruppel-associated Box (KRAB)-associated co-repressor (KAP-1) Ser-473 phosphorylation regulates heterochromatin protein 1beta (HP1-beta) mobilization and DNA repair in heterochromatin. J Biol Chem287: 28122–28131. doi: 10.1074/jbc.M112.36838122715096
42. El-Guindy AS, Miller G, (2004) Phosphorylation of Epstein-Barr virus ZEBRA protein at its casein kinase 2 sites mediates its ability to repress activation of a viral lytic cycle late gene by Rta. J Virol78: 7634–7644. doi: 10.1128/JVI.78.14.7634-7644.200415220438
43. Feederle R, Kost M, Baumann M, Janz A, Drouet E, et al. (2000) The Epstein-Barr virus lytic program is controlled by the co-operative functions of two transactivators. Embo J19: 3080–3089. doi: 10.1093/emboj/19.12.308010856251
44. Koganti S, de la Paz A, Freeman AF, Bhaduri-McIntosh S, (2014) B lymphocytes from patients with a hypomorphic mutation in STAT3 resist Epstein-Barr virus-driven cell proliferation. J Virol88: 516–524. doi: 10.1128/JVI.02601-1324173212
45. Schmittgen TD, Livak KJ, (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc3: 1101–1108. 18546601