LMP1 mediates multinuclearity through downregulation of shelterin proteins and formation of telomeric aggregates

Blood

Volumn 125, Issue 13, 2015, Pages 2101-2110

  Lajoie, Valérie ^a,b   Lemieux, Bruno ^a,b   Sawan, Bassem ^c   Lichtensztejn, Daniel ^d   Lichtensztejn, Zelda ^d   Wellinger, Raymund ^b,g   Mai, Sabine ^d   Knecht, Hans ^a,b,e,f  

^a Divisond'Hématologie   (Canada)

^b Département DeMicrobiologie Infectiologie   (Canada)

^c CENTRE HOSPITALIER UNIVERSITAIRE DE SHERBROOKE   (Canada)

^d UNIVERSITY OF MANITOBA   (Canada)

^e MCGILL UNIVERSITY   (Canada)

^f MCGILL UNIVERSITY   (Canada)

^g UNIVERSITÉ DE SHERBROOKE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

LATENT MEMBRANE PROTEIN 1; POT1 PROTEIN; TELOMERE BINDING PROTEIN; TELOMERIC REPEAT BINDING FACTOR 1; TELOMERIC REPEAT BINDING FACTOR 2; UNCLASSIFIED DRUG; EBV-ASSOCIATED MEMBRANE ANTIGEN, EPSTEIN-BARR VIRUS; MATRIX PROTEIN; PROTEIN AGGREGATE; SHELTERIN, HUMAN;

ARTICLE; BURKITT LYMPHOMA CELL LINE; CONTROLLED STUDY; DOWN REGULATION; GIANT CELL; HUMAN; HUMAN CELL; MULTINUCLEAR CELL; NUCLEAR SIZE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SPECTRAL KARYOTYPING; STABLE EXPRESSION; TELOMERE; TRANSCRIPTION REGULATION; TRANSLATION REGULATION; CELL NUCLEUS; GENETICS; HODGKIN DISEASE; METABOLISM; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE; VIROLOGY; VIRUS CELL TRANSFORMATION;

CELL LINE, TUMOR; CELL NUCLEUS; CELL TRANSFORMATION, VIRAL; DOWN-REGULATION; GIANT CELLS; HODGKIN DISEASE; HUMANS; PROTEIN AGGREGATES; TELOMERE; TELOMERE-BINDING PROTEINS; VIRAL MATRIX PROTEINS;

EID: 84926172822     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2014-08-594176     Document Type: Article

References (54)

1. Hsu SM, Zhao X, Chakraborty S, et al. Reed-Sternberg cells in Hodgkin's cell lines HDLM, L-428, and KM-H2 are not actively replicating: Lack of bromodeoxyuridine uptake by multinuclear cells in culture. Blood. 1988;71(5):1382-1389.
2. Newcom SR, Kadin ME, Phillips C. L-428 Reed-Sternberg cells and mononuclear Hodgkin's cells arise from a single cloned mononuclear cell. Int J Cell Cloning. 1988;6(6):417-431.
3. Kapp U, Yeh WC, Patterson B, et al. Interleukin 13 is secreted by and stimulates the growth of Hodgkin and Reed-Sternberg cells. J Exp Med. 1999;189(12):1939-1946.
4. Khan G. Epstein-Barr virus, cytokines, and inflammation: A cocktail for the pathogenesis of Hodgkin's lymphoma? Exp Hematol. 2006;34(4): 399-406.
5. Küppers R. The biology of Hodgkin's lymphoma. Nat Rev Cancer. 2009;9(1):15-27.
6. Jones RJ, Gocke CD, Kasamon YL, et al. Circulating clonotypic B cells in classic Hodgkin lymphoma. Blood. 2009;113(23):5920-5926.
7. Louis SF, Vermolen BJ, Garini Y, et al. c-Myc induces chromosomal rearrangements through telomere and chromosome remodeling in the interphase nucleus. Proc Natl Acad Sci USA. 2005;102(27):9613-9618.
8. Knecht H, Sawan B, Lichtensztejn D, Lemieux B, Wellinger RJ, Mai S. The 3D nuclear organization of telomeres marks the transition from Hodgkin to Reed-Sternberg cells. Leukemia. 2009;23(3): 565-573.
9. Knecht H, Sawan B, Lichtensztejn Z, Lichtensztejn D, Mai S. 3D Telomere FISH defines LMP1-expressing Reed-Sternberg cells as end-stage cells with telomere-poor 'ghost' nuclei and very short telomeres. Lab Invest. 2010; 90(4):611-619.
10. Pallesen G, Hamilton-Dutoit SJ, Rowe M, Young LS. Expression of Epstein-Barr virus latent gene products in tumour cells of Hodgkin's disease. Lancet. 1991;337(8737):320-322.
11. Knecht H, Bachmann E, Brousset P, et al. Deletions within the LMP1 oncogene of Epstein-Barr virus are clustered in Hodgkin's disease and identical to those observed in nasopharyngeal carcinoma. Blood. 1993;82(10):2937-2942.
12. Murray PG, Billingham LJ, Hassan HT, et al. Effect of Epstein-Barr virus infection on response to chemotherapy and survival in Hodgkin's disease. Blood. 1999;94(2):442-447.
13. Claviez A, Tiemann M, Lüders H, et al. Impact of latent Epstein-Barr virus infection on outcome in children and adolescents with Hodgkin's lymphoma. J Clin Oncol. 2005;23(18):4048-4056.
14. Keegan TH, Glaser SL, Clarke CA, et al. Epstein-Barr virus as a marker of survival after Hodgkin's lymphoma: A population-based study. J Clin Oncol. 2005;23(30):7604-7613.
15. Dinand V, Arya LS. Epidemiology of childhood Hodgkins disease: is it different in developing countries? Indian Pediatr. 2006;43(2):141-147.
16. Hjalgrim H, Askling J, Rostgaard K, et al. Characteristics of Hodgkin's lymphoma after infectious mononucleosis. N Engl J Med. 2003; 349(14):1324-1332.
17. Louissaint A Jr, Ferry JA, Soupir CP, Hasserjian RP, Harris NL, Zukerberg LR. Infectious mononucleosis mimicking lymphoma: distinguishing morphological and immunophenotypic features. Mod Pathol. 2012;25(8):1149-1159.
18. Knecht H, Kongruttanachok N, Sawan B, et al. Three-Dimensional Telomere Signatures of Hodgkin- and Reed-Sternberg Cells at Diagnosis Identify Patients with Poor Response to Conventional Chemotherapy. Transl Oncol. 2012; 5(4):269-277.
19. Lacoste S, Wiechec E, Dos Santos Silva AG, et al. Chromosomal rearrangements after ex vivo Epstein-Barr virus (EBV) infection of human B cells. Oncogene. 2010;29(4):503-515.
20. Kamranvar SA, Masucci MG. The Epstein-Barr virus nuclear antigen-1 promotes telomere dysfunction via induction of oxidative stress. Leukemia. 2011;25(6):1017-1025.
21. Guffei A, Sarkar R, Klewes L, Righolt C, Knecht H, Mai S. Dynamic chromosomal rearrangements in Hodgkin's lymphoma are due to ongoing threedimensional nuclear remodeling and breakage-bridge-fusion cycles. Haematologica. 2010; 95(12):2038-2046.
22. Floettmann JE, Ward K, Rickinson AB, Rowe M. Cytostatic effect of Epstein-Barr virus latent membrane protein-1 analyzed using tetracycline-regulated expression in B cell lines. Virology. 1996;223(1):29-40.
23. Fukasawa K, Wiener F, Vande Woude GF, Mai S. Genomic instability and apoptosis are frequent in p53 deficient young mice. Oncogene. 1997; 15(11):1295-1302.
24. Rozen S, Skaletsky HJ. Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S, eds. Bioinformatics Methods and Protocols: Methods in Molecular Biology. Totowa, NJ: Humana Press; 2000: 365-386.
25. Ometto L, Menin C, Masiero S, et al. Molecular profile of Epstein-Barr virus in human immunodeficiency virus type 1-related lymphadenopathies and lymphomas. Blood. 1997;90(1):313-322.
26. Escoffier E, Rezza A, Roborel de Climens A, et al. A balanced transcription between telomerase and the telomeric DNA-binding proteins TRF1, TRF2 and Pot1 in resting, activated, HTLV-1-transformed and Tax-expressing human T lymphocytes. Retrovirology. 2005;2:77.
27. Smogorzewska A, de Lange T. Different telomere damage signaling pathways in human and mouse cells. EMBO J. 2002;21(16):4338-4348.
28. Chuang TC, Moshir S, Garini Y, et al. The threedimensional organization of telomeres in the nucleus of mammalian cells. BMC Biol. 2004; 2:12.
29. Schaefer LH, Schuster D, Herz H. Generalized approach for accelerated maximum likelihood based image restoration applied to threedimensional fluorescence microscopy. J Microsc. 2001;204(Pt 2):99-107.
30. Vermolen BJ, Garini Y, Mai S, et al. Characterizing the three-dimensional organization of telomeres. Cytometry A. 2005;67(2):144-150.
31. Mai S, Garini Y. The significance of telomeric aggregates in the interphase nuclei of tumor cells. J Cell Biochem. 2006;97(5):904-915.
32. Sarkar R, Guffei A, Vermolen BJ, Garini Y, Mai S. Alterations of centromere positions in nuclei of immortalized and malignant mouse lymphocytes. Cytometry A. 2007;71(6):386-392.
33. Denchi EL, de Lange T. Protection of telomeres through independent control of ATM and ATR by TRF2 and POT1. Nature. 2007;448(7157): 1068-1071.
34. Thorley-Lawson DA, Gross A. Persistence of the Epstein-Barr virus and the origins of associated lymphomas. N Engl J Med. 2004;350(13): 1328-1337.
35. Roughan JE, Thorley-Lawson DA. The intersection of Epstein-Barr virus with the germinal center. J Virol. 2009;83(8):3968-3976.
36. Glaser SL, Gulley ML, Clarke CA, et al. Racial/ ethnic variation in EBV-positive classical Hodgkin lymphoma in California populations. Int J Cancer. 2008;123(7):1499-1507.
37. Enblad G, Sandvej K, Sundström C, Pallesen G, Glimelius B. Epstein-Barr virus distribution in Hodgkin's disease in an unselected Swedish population. Acta Oncol. 1999;38(4):425-429.
38. Weinreb M, Day PJ, Niggli F, et al. The consistent association between Epstein-Barr virus and Hodgkin's disease in children in Kenya. Blood. 1996;87(9):3828-3836.
39. Celli GB, de Lange T. DNA processing is not required for ATM-mediated telomere damage response after TRF2 deletion. Nat Cell Biol. 2005; 7(7):712-718.
40. Lazzerini Denchi E, Celli G, de Lange T. Hepatocytes with extensive telomere deprotection and fusion remain viable and regenerate liver mass through endoreduplication. Genes Dev. 2006;20(19):2648-2653.
41. Martínez P, Thanasoula M, Muñoz P, et al. Increased telomere fragility and fusions resulting from TRF1 deficiency lead to degenerative pathologies and increased cancer in mice. Genes Dev. 2009;23(17):2060-2075.
42. Okamoto K, Iwano T, Tachibana M, Shinkai Y. Distinct roles of TRF1 in the regulation of telomere structure and lengthening. J Biol Chem. 2008; 283(35):23981-23988.
43. Sfeir A, Kosiyatrakul ST, Hockemeyer D, et al. Mammalian telomeres resemble fragile sites and require TRF1 for efficient replication. Cell. 2009; 138(1):90-103.
44. He H, Wang Y, Guo X, et al. Pot1b deletion and telomerase haploinsufficiency in mice initiate an ATR-dependent DNA damage response and elicit phenotypes resembling dyskeratosis congenita. Mol Cell Biol. 2009;29(1):229-240.
45. Davoli T, Denchi EL, de Lange T. Persistent telomere damage induces bypass of mitosis and tetraploidy. Cell. 2010;141(1):81-93.
46. Knecht H, McQuain C, Martin J, et al. Expression of the LMP1 oncoprotein in the EBV negative Hodgkin's disease cell line L-428 is associated with Reed-Sternberg cell morphology. Oncogene. 1996;13(5):947-953.
47. Knecht H, Berger C, McQuain C, et al. Latent membrane protein 1 associated signaling pathways are important in tumor cells of Epstein-Barr virus negative Hodgkin's disease. Oncogene. 1999;18(50):7161-7167.
48. Chang KC, Chang Y, Jones D, Su IJ. Aberrant expression of cyclin a correlates with morphogenesis of reed-sternberg cells in Hodgkin lymphoma. Am J Clin Pathol. 2009;132(1):50-59.
49. Kim SH, Shin YK, Lee IS, et al. Viral latent membrane protein 1 (LMP-1)-induced CD99 down-regulation in B cells leads to the generation of cells with Hodgkin's and Reed-Sternberg phenotype. Blood. 2000;95(1):294-300.
50. MacLeod RA, Spitzer D, Bar-Am I, et al. Karyotypic dissection of Hodgkin's disease cell lines reveals ectopic subtelomeres and ribosomal DNA at sites of multiple jumping translocations and genomic amplification. Leukemia. 2000; 14(10):1803-1814.
51. Mader A, Brüderlein S, Wegener S, et al. U-HO1, a new cell line derived from a primary refractory classical Hodgkin lymphoma. Cytogenet Genome Res. 2007;119(3-4):204-210.
52. Wu Y, Zakian VA. Identity crisis when telomeres left unprotected. J Mol Cell Biol. 2010;2(1):14-16.
53. Londoñ o-Vallejo JA, Wellinger RJ. Telomeres and telomerase dance to the rhythm of the cell cycle. Trends Biochem Sci. 2012;37(9):391-399.
54. Knecht H, Righolt C, Mai S. Genomic instability: the driving force behind refractory/relapsing Hodgkin's lymphoma. Cancers (Basel). 2013;5(2): 714-725.