Epstein-Barr virus reactivation induces MYC-IGH spatial proximity and t(8;14) in B cells.
Burkitt lymphoma, lymphomagenesis
CRISPR/Cas9
EBV
MRE11
t(8;14)
Journal
Journal of medical virology
ISSN: 1096-9071
Titre abrégé: J Med Virol
Pays: United States
ID NLM: 7705876
Informations de publication
Date de publication:
03 2023
03 2023
Historique:
revised:
14
02
2023
received:
04
08
2022
accepted:
16
02
2023
medline:
30
3
2023
pubmed:
4
3
2023
entrez:
3
3
2023
Statut:
ppublish
Résumé
Burkitt lymphoma (BL) is a B cell malignancy associated with the Epstein-Barr virus (EBV). Most BL cases are characterized by a t(8;14) chromosomal translocation involving the MYC oncogene and the immunoglobulin heavy chain gene (IGH). The role of EBV in promoting this translocation remains largely unknown. Here we provide the experimental evidence that EBV reactivation from latency leads to an increase in the proximity between the MYC and IGH loci, otherwise located far away in the nuclear space both in B-lymphoblastoid cell lines and in patients' B-cells. Specific DNA damage within the MYC locus, followed by the MRE11-dependent DNA repair plays a role in this process. Using a CRISPR/Cas9-based B cell model to induce specific DNA double strand breaks in MYC and IGH loci, we have shown that the MYC-IGH proximity induced by EBV reactivation leads to an increased t(8;14) translocation frequency.
Substances chimiques
Proto-Oncogene Proteins c-myc
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e28633Informations de copyright
© 2023 The Authors. Journal of Medical Virology published by Wiley Periodicals LLC.
Références
Brady G, MacArthur GJ, Farrell PJ. Epstein-Barr virus and Burkitt lymphoma. Postgrad Med J. 2008;84(12):372-377. doi:10.1136/jcp.2007.047977
Bornkamm GW. Epstein-Barr virus and the pathogenesis of Burkitt's lymphoma: more questions than answers. Int J Cancer. 2009;124(8):1745-1755. doi:10.1002/ijc.24223
Moormann AM, Bailey JA. Malaria-how this parasitic infection aids and abets EBV-associated Burkitt lymphomagenesis. Current Opinion in Virology. 2016;20:78-84. doi:10.1016/j.coviro.2016.09.006
Mawson AR, Majumdar S. Malaria, Epstein-Barr virus infection and the pathogenesis of Burkitt's lymphoma: malaria, EBV infection and the pathogenesis of Burkitt's lymphoma. Int J Cancer. 2017;141(9):1849-1855. doi:10.1002/ijc.30885
Shmakova A, Germini D, Vassetzky Y. HIV-1, HAART and cancer: a complex relationship. Int J Cancer. 2020;146(10):2666-2679. doi:10.1002/ijc.32730
Amon W, Farrell PJ. Reactivation of Epstein-Barr virus from latency. Rev Med Virol. 2005;15(3):149-156. doi:10.1002/rmv.456
Cohen JI. Epstein-Barr virus infection. N Engl J Med. 2000;343(7):481-492. doi:10.1056/NEJM200008173430707
Epstein MA, Henle G, Achong BG, Barr YM. Morphological and biological studies on a virus in cultured lymphoblasts from Burkitt's lymphoma. J Exp Med. 1965;121:761-770. doi:10.1084/jem.121.5.761
Tsurumi T, Fujita M, Kudoh A. Latent and lytic Epstein-Barr virus replication strategies. Rev Med Virol. 2005;15(1):3-15. doi:10.1002/rmv.441
Countryman J, Miller G. Activation of expression of latent Epstein-Barr herpesvirus after gene transfer with a small cloned subfragment of heterogeneous viral DNA. Proc Natl Acad Sci. 1985;82(12):4085-4089. doi:10.1073/pnas.82.12.4085
Germini D, Sall FB, Shmakova A, et al. Oncogenic properties of the EBV ZEBRA protein. Cancers. 2020;12(6):1479. doi:10.3390/cancers12061479
Grogan E, Jenson H, Countryman J, Heston L, Gradoville L, Miller G. Transfection of a rearranged viral DNA fragment, WZhet, stably converts latent Epstein-Barr viral infection to productive infection in lymphoid cells. Proc Natl Acad Sci. 1987;84(5):1332-1336. doi:10.1073/pnas.84.5.1332
Murata T, Tsurumi T. Switching of EBV cycles between latent and lytic states. Rev Med Virol. 2014;24(3):142-153. doi:10.1002/rmv.1780
Al Tabaa Y, Tuaillon E, Bollore K, et al. Functional Epstein-Barr virus reservoir in plasma cells derived from infected peripheral blood memory B cells. Blood. 2009;113(3):604-611. doi:10.1182/blood-2008-02-136903
Robinson M, Schor S, Barouch-Bentov R, Einav S. Viral journeys on the intracellular highways. Cell Mol Life Sci. 2018;75(20):3693-3714. doi:10.1007/s00018-018-2882-0
Rosemarie Q, Sugden B. Epstein-Barr virus: how its lytic phase contributes to oncogenesis. Microorganisms. 2020;8(11):1824. doi:10.3390/microorganisms8111824
Allday MJ. How does Epstein-Barr virus (EBV) complement the activation of Myc in the pathogenesis of Burkitt's lymphoma? Sem Cancer Biol. 2009;19(6):366-376. doi:10.1016/j.semcancer.2009.07.007
Molyneux EM, Rochford R, Griffin B, et al. Burkitt's lymphoma. Lancet. 2012;379(9822):1234-1244. doi:10.1016/S0140-6736(11)61177-X
Saleh K, Michot JM, Camara-Clayette V, Vassetsky Y, Ribrag V. Burkitt and Burkitt-like lymphomas: a systematic review. Curr Oncol Rep. 2020;22(4):33. doi:10.1007/s11912-020-0898-8
Torgbor C, Awuah P, Deitsch K, Kalantari P, Duca KA, Thorley-Lawson DA. A multifactorial role for P. falciparum malaria in endemic Burkitt's lymphoma pathogenesis. PLoS Pathog. 2014;10(5):e1004170. doi:10.1371/journal.ppat.1004170
Iarovaia OV, Rubtsov M, Ioudinkova E, Tsfasman T, Razin SV, Vassetzky YS. Dynamics of double strand breaks and chromosomal translocations. Mol Cancer. 2014;13:249. doi:10.1186/1476-4598-13-249
Roix JJ, McQueen PG, Munson PJ, Parada LA, Misteli T. Spatial proximity of translocation-prone gene loci in human lymphomas. Nature Genet. 2003;34(3):287-291. doi:10.1038/ng1177
Roukos V, Burman B, Misteli T. The cellular etiology of chromosome translocations. Curr Opin Cell Biol. 2013;25(3):357-364. doi:10.1016/j.ceb.2013.02.015
Canoy RJ, Shmakova A, Karpukhina A, Shepelev M, Germini D, Vassetzky Y. Factors that affect the formation of chromosomal translocations in cells. Cancers. 2022;14(20):5110. doi:10.3390/cancers14205110
Honjo T, Kinoshita K, Muramatsu M. Molecular mechanism of class switch recombination: linkage with somatic hypermutation. Annu Rev Immunol. 2002;20:165-196. doi:10.1146/annurev.immunol.20.090501.112049
Chaudhuri J, Basu U, Zarrin A, et al. Evolution of the immunoglobulin heavy chain class switch recombination mechanism. Adv Immunol. 2007;94:157-214. doi:10.1016/S0065-2776(06)94006-1
Di Noia JM, Neuberger MS. Molecular mechanisms of antibody somatic hypermutation. Annu Rev Biochem. 2007;76:1-22. doi:10.1146/annurev.biochem.76.061705.090740
Sall FB, Germini D, Kovina AP, et al. Effect of environmental factors on nuclear organization and transformation of human B lymphocytes. Biochemistry. 2018;83(4):402-410. doi:10.1134/S0006297918040119
Dorsett Y, Robbiani DF, Jankovic M, Reina-San-Martin B, Eisenreich TR, Nussenzweig MC. A role for AID in chromosome translocations between c-myc and the IgH variable region. J Exp Med. 2007;204(9):2225-2232. doi:10.1084/jem.20070884
Ramiro AR, Jankovic M, Eisenreich T, et al. AID is required for c-myc/IgH chromosome translocations in vivo. Cell. 2004;118(4):431-438. doi:10.1016/j.cell.2004.08.006
Nijland ML, Kersten MJ, Pals ST, Bemelman FJ, ten Berge IJM. Epstein-Barr virus-positive posttransplant lymphoproliferative disease after solid organ transplantation: pathogenesis, clinical manifestations, diagnosis, and management. Transplant Direct. 2016;2(1):e48. doi:10.1097/TXD.0000000000000557
Delecluse S, Poirey R, Zeier M, et al. Identification and cloning of a new western Epstein-Barr virus strain that efficiently replicates in primary B cells. J Virol. 2020;94(10):e01918-19. doi:10.1128/JVI.01918-19
Shmakova A, Lomov N, Viushkov V, et al. Cell models with inducible oncogenic translocations allow to evaluate the potential of drugs to favor secondary translocations. Cancer Commun. 2022;43:154-158. doi:10.1002/cac2.12370
Canoy RJ, André F, Shmakova A, et al. Easy and robust electrotransfection protocol for efficient ectopic gene expression and genome editing in human B cells. Gene Therapy. 2020;30:167-171. doi:10.1038/s41434-020-00194-x
Germini D, Bou Saada Y, Tsfasman T, et al. A one-step PCR-based assay to evaluate the efficiency and precision of genomic DNA-editing tools. Mol Therapy-Methods Clin Development. 2017;5:43-50. doi:10.1016/j.omtm.2017.03.001
Sall FB, El Amine R, Markozashvili D, et al. HIV-1 Tat protein induces aberrant activation of AICDA in human B-lymphocytes from peripheral blood. J Cell Physiol. 2019;234(9):15678-15685. doi:10.1002/jcp.28219
Germini D, Tsfasman T, Klibi M, et al. HIV Tat induces a prolonged MYC relocalization next to IGH in circulating B-cells. Leukemia. 2017;31(11):2515-2522. doi:10.1038/leu.2017.106
Pannunzio NR, Watanabe G, Lieber MR. Nonhomologous DNA end-joining for repair of DNA double-strand breaks. J Biol Chem. 2018;293(27):10512-10523. doi:10.1074/jbc.TM117.000374
Sklyar I, Iarovaia OV, Gavrilov AA, et al. Distinct patterns of colocalization of the CCND1 and CMYC genes with their potential translocation partner IGH at successive stages of B-cell differentiation. JCB. 2016;117(7):1506-1510. doi:10.1002/jcb.25516
Kim KD, Tanizawa H, De Leo A, et al. Epigenetic specifications of host chromosome docking sites for latent Epstein-Barr virus. Nat Commun. 2020;11(1):877. doi:10.1038/s41467-019-14152-8
Li C, Shi Z, Zhang L, et al. Dynamic changes of territories 17 and 18 during EBV-infection of human lymphocytes. Mol Biol Rep. 2010;37(5):2347-2354. doi:10.1007/s11033-009-9740-y
Moquin SA, Thomas S, Whalen S, et al. The Epstein-Barr virus episome maneuvers between nuclear chromatin compartments during reactivation. J Virol. 2018;92(3):e01417. doi:10.1128/JVI.01413-17
Osborne CS, Chakalova L, Mitchell JA, et al. Myc dynamically and preferentially relocates to a transcription factory occupied by Igh. PLoS Biol. 2007;5(8):e192. doi:10.1371/journal.pbio.0050192
Tsai MH, Raykova A, Klinke O, et al. Spontaneous lytic replication and epitheliotropism define an Epstein-Barr virus strain found in carcinomas. Cell Rep. 2013;5(2):458-470. doi:10.1016/j.celrep.2013.09.012
Küppers R, Dalla-Favera R. Mechanisms of chromosomal translocations in B cell lymphomas. Oncogene. 2001;20(40):5580-5594. doi:10.1038/sj.onc.1204640
Simsek D, Jasin M. Alternative end-joining is suppressed by the canonical NHEJ component Xrcc4-ligase IV during chromosomal translocation formation. Nat Struct Mol Biol. 2010;17(4):410-416. doi:10.1038/nsmb.1773
Soni A, Siemann M, Pantelias GE, Iliakis G. Marked contribution of alternative end-joining to chromosome-translocation-formation by stochastically induced DNA double-strand-breaks in G2-phase human cells. Mutation Res/Genetic Toxicol Environmental Mutag. 2015;793:2-8. doi:10.1016/j.mrgentox.2015.07.002
Vogt N, Dai B, Erdmann T, Berdel WE, Lenz G. The molecular pathogenesis of mantle cell lymphoma. Leuk Lymphoma. 2017;58(7):1530-1537. doi:10.1080/10428194.2016.1248965
Hau P, Tsao S. Epstein-Barr virus hijacks DNA damage response transducers to orchestrate its life cycle. Viruses. 2017;9(11):341. doi:10.3390/v9110341
Caridi CP, D'Agostino C, Ryu T, et al. Nuclear F-actin and myosins drive relocalization of heterochromatic breaks. Nature. 2018;559(7712):54-60. doi:10.1038/s41586-018-0242-8
Münz C. Latency and lytic replication in Epstein-Barr virus-associated oncogenesis. Nat Rev Microbiol. 2019;17(11):691-700. doi:10.1038/s41579-019-0249-7
Arvey A, Tempera I, Tsai K, et al. An atlas of the Epstein-Barr virus transcriptome and epigenome reveals host-virus regulatory interactions. Cell Host Microbe. 2012;12(2):233-245. doi:10.1016/j.chom.2012.06.008
Chiu YF, Sugden B. Epstein-Barr virus: the path from latent to productive infection. Annual Rev Virol. 2016;3(1):359-372. doi:10.1146/annurev-virology-110615-042358
Ersing I, Nobre L, Wang LW, et al. A temporal proteomic map of Epstein-Barr virus lytic replication in B cells. Cell Rep. 2017;19(7):1479-1493. doi:10.1016/j.celrep.2017.04.062
Morales-Sánchez A, Fuentes-Panana E. The immunomodulatory capacity of an Epstein-Barr virus abortive lytic cycle: potential contribution to viral tumorigenesis. Cancers. 2018;10(4):98. doi:10.3390/cancers10040098
Wood CD, Veenstra H, Khasnis S, et al. MYC activation and BCL2L11 silencing by a tumour virus through the large-scale reconfiguration of enhancer-promoter hubs. eLife. 2016;5:e18270. doi:10.7554/eLife.18270
Jiang S, Zhou H, Liang J, et al. The Epstein-Barr virus regulome in lymphoblastoid cells. Cell Host Microbe. 2017;22(4):561-573.e4. doi:10.1016/j.chom.2017.09.001
Rodriguez A, Jung EJ, Yin Q, Cayrol C, Flemington EK. Role of c-myc regulation in Zta-mediated induction of the cyclin-dependent kinase inhibitors p21 and p27 and cell growth arrest. Virology. 2001;284(2):159-169. doi:10.1006/viro.2001.0923
Guo R, Jiang C, Zhang Y, et al. MYC controls the Epstein-Barr virus lytic switch. Mol Cell. 2020;78(4):653-669. doi:10.1016/j.molcel.2020.03.025
Ferreiro JF, Morscio J, Dierickx D, et al. Post-transplant molecularly defined Burkitt lymphomas are frequently MYC-negative and characterized by the 11q-gain/loss pattern. Haematologica. 2015;100(7):e275-e279. doi:10.3324/haematol.2015.124305
Djokic M, Le Beau MM, Swinnen LJ, et al. Post-transplant lymphoproliferative disorder subtypes correlate with different recurring chromosomal abnormalities. Genes Chromosom Cancer. 2006;45(3):313-318. doi:10.1002/gcc.20287
Picarsic J, Jaffe R, Mazariegos G, et al. Post-transplant Burkitt lymphoma is a more aggressive and distinct form of post-transplant lymphoproliferative disorder. Cancer. 2011;117(19):4540-4550. doi:10.1002/cncr.26001
Akar Özkan E, Özdemir BH, Akdur A, Deniz EE, Haberal M. Burkitt lymphoma after transplant: an aggressive lymphoproliferative disease. Exp Clin Transplant. 2014;12(Suppl 1):136-138.
Aten JA, Stap J, Krawczyk PM, et al. Dynamics of DNA double-strand breaks revealed by clustering of damaged chromosome domains. Science. 2004;303(5654):92-95. doi:10.1126/science.1088845
Roukos V, Voss TC, Schmidt CK, Lee S, Wangsa D, Misteli T. Spatial dynamics of chromosome translocations in living cells. Science. 2013;341(6146):660-664. doi:10.1126/science.1237150
Valyaeva AA, Tikhomirova MA, Potashnikova DM, et al. Ectopic expression of HIV-1 Tat modifies gene expression in cultured B cells: implications for the development of B-cell lymphomas in HIV-1-infected patients. PeerJ. 2022;10:e13986. doi:10.7717/peerj.13986
Krawczyk PM, Borovski T, Stap J, et al. Chromatin mobility is increased at sites of DNA double-strand breaks. J Cell Sci. 2012;125(Pt 9):2127-2133. doi:10.1242/jcs.089847
Kruhlak MJ, Celeste A, Dellaire G, et al. Changes in chromatin structure and mobility in living cells at sites of DNA double-strand breaks. J Cell Biol. 2006;172(6):823-834. doi:10.1083/jcb.200510015
Miné-Hattab J, Chiolo I. Complex chromatin motions for DNA repair. Front Genet. 2020;11:800. doi:10.3389/fgene.2020.00800
Miné-Hattab J, Rothstein R. Increased chromosome mobility facilitates homology search during recombination. Nature Cell Biol. 2012;14(5):510-517. doi:10.1038/ncb2472
Neumaier T, Swenson J, Pham C. Evidence for formation of DNA repair centers and dose-response nonlinearity in human cells. Proc Natl Acad Sci. 2012;109(2):443-448. doi:10.1073/pnas.1117849108
Liu M, Duke JL, Richter DJ. Two levels of protection for the B cell genome during somatic hypermutation. Nature. 2008;451(7180):841-845. doi:10.1038/nature06547
Boerma EG, Siebert R, Kluin PM, Baudis M. Translocations involving 8q24 in Burkitt lymphoma and other malignant lymphomas: a historical review of cytogenetics in the light of todays knowledge. Leukemia. 2009;23(2):225-234. doi:10.1038/leu.2008.281
Duquette ML, Pham P, Goodman MF, Maizels N. AID binds to transcription-induced structures in c-MYC that map to regions associated with translocation and hypermutation. Oncogene. 2005;24(38):5791-5798. doi:10.1038/sj.onc.1208746
Yu K, Chedin F, Hsieh CL, Wilson TE, Lieber MR. R-loops at immunoglobulin class switch regions in the chromosomes of stimulated B cells. Nature Immunol. 2003;4(5):442-451. doi:10.1038/ni919
Pichugin A, Iarovaia OV, Gavrilov A. The IGH locus relocalizes to a “recombination compartment” in the perinucleolar region of differentiating B-lymphocytes. Oncotarget. 2017;8(25):40079-40089. doi:10.18632/oncotarget.16941
Coghill AE, Proietti C, Liu Z, et al. The association between the comprehensive Epstein-Barr virus serologic profile and endemic burkitt lymphoma. Cancer Epidemiol Biomarkers Prevent. 2020;29(1):57-62. doi:10.1158/1055-9965.EPI-19-0551
Accardi R, Gruffat H, Sirand C. The mycotoxin aflatoxin B1 stimulates Epstein-Barr virus-induced B-cell transformation in in vitro and in vivo experimental models. Carcinogenesis. 2015;36(11):1440-1451. doi:10.1093/carcin/bgv142
Chêne A, Donati D, Guerreiro-Cacais AO. A molecular link between malaria and Epstein-Barr virus reactivation. PLoS Pathog. 2007;3(6):e80. doi:10.1371/journal.ppat.0030080
MacNeil A, Sumba OP, Lutzke ML, Moormann A, Rochford R. Activation of the Epstein-Barr virus lytic cycle by the latex of the plant Euphorbia tirucalli. Br J Cancer. 2003;88(10):1566-1569. doi:10.1038/sj.bjc.6600929
Robbiani DF, Bothmer A, Callen E, et al. AID is required for the chromosomal breaks in c-myc that lead to c-myc/IgH translocations. Cell. 2008;135(6):1028-1038. doi:10.1016/j.cell.2008.09.062
Robbiani DF, Deroubaix S, Feldhahn N, et al. Plasmodium infection promotes genomic instability and AID-dependent B cell lymphoma. Cell. 2015;162(4):727-737. doi:10.1016/j.cell.2015.07.019
Kerr JR. Epstein-Barr virus (EBV) reactivation and therapeutic inhibitors. J Clin Pathol. 2019;72(10):651-658. doi:10.1136/jclinpath-2019-205822