Skip to main content

Advertisement

SpringerLink
Log in

Telomere size and telomerase activity in Epstein-Barr virus (EBV)-positive and EBV-negative Burkitt’s lymphoma cell lines

  • Brief Report
  • Published:
Archives of Virology Aims and scope Submit manuscript

Summary.

The telomere repeat lengths of BL cell lines were quantified by measuring terminal restriction fragment (TRF). Epstein-Barr virus (EBV)-positive Namalwa, Raji, and EB-3 cell lines have long telomeres, i.e. TRFs 10–19 kbp, whereas the Daudi cell line, producing a transformation-defective EBV mutant, has TRFs ∼2.2 kbp. EBV-negative BJAB and DG75 cell lines have short TRFs 3.9–5.4 kbp, shorter than the ∼12 kbp TRFs in PBLs. Telomerase activities of these BL cell lines are similar. TRFs of non-BL lymphoma cell lines are 2.3–5.5 kbp. Fluorescent in situ hybridization (FISH) studies of these cell lines showed remarkable heterogeneity of telomere size in chromosomes in the same BL cell. These results suggest that EBV-positive and EBV-negative BL cell lines have experienced various telomere dynamics.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • A Adams B Lidin H Strander K Cantell (1975) ArticleTitleSpontaneous interferon production and Epstein-Barr virus antigen expression in human lymphoid cell lines. J Gen Virol 28 219–223 Occurrence Handle170371

    PubMed  Google Scholar 

  • JR Arrand LS Young JD Tugwood (1989) ArticleTitleTwo families of sequences in the small RNA-encoding region of Epstein-Barr virus (EBV) correlate with EBV types A and B. J Virol 63 983–986 Occurrence Handle2536122

    PubMed  Google Scholar 

  • Y Asakawa E Gotoh (1997) ArticleTitleA method for detecting sister chromatid exchanges using prematurely condensed chromosomes and immunogold-silver staining. Mutagenesis 12 175–177 Occurrence Handle9175644

    PubMed  Google Scholar 

  • H Ben-Bassat N Goldblum S Mitrani T Goldblum JM Yoffey MM Cohen Z Bentwich B Ramot E Klein G Klein (1977) ArticleTitleEstablishment in continuous culture of a new type of lymphocyte from a “Burkitt like” malignant lymphoma (line D.G.-75). Int J Cancer 19 27–33 Occurrence Handle188769

    PubMed  Google Scholar 

  • EH Blackburn (1991) ArticleTitleStructure and function of telomeres. Nature 350 569–573

    Google Scholar 

  • P Brousset N Chaouche T Al Saati RC Zenou G Delsol (1998) ArticleTitleTelomerase activity in Hodgkin’s disease. Leuk Lymphoma 30 189–192 Occurrence Handle9669689

    PubMed  Google Scholar 

  • TM Bryan A Englezou L Dalla-Pozza MA Dunham RR Reddel (1997) ArticleTitleEvidence for an alternative mechanism for maintaining telomere length in human tumors and tumor-derived cell lines. Nat Med 3 1271–1274 Occurrence Handle10.1038/nm1197-1271 Occurrence Handle9359704

    Article  PubMed  Google Scholar 

  • TM Bryan A Englezou MA Dunham RR Reddel (1998) ArticleTitleTelomere length dynamics in telomerase-positive immortal human cell populations. Exp Cell Res 239 370–378 Occurrence Handle10.1006/excr.1997.3907 Occurrence Handle9521855

    Article  PubMed  Google Scholar 

  • GB Clements G Klein S Povey (1975) ArticleTitleProduction by EBV infection of an EBNA-positive subline from an EBNA-negative human lymphoma cell line without detectable EBV DNA. Int J Cancer 16 125–133 Occurrence Handle170210

    PubMed  Google Scholar 

  • CM Counter FM Botelho P Wang CB Harley S Bacchetti (1994) ArticleTitleStabilization of short telomeres and telomerase activity accompany immortalization of Epstein-Barr virus-transformed human B lymphocytes. J Virol 68 3410–3414 Occurrence Handle8151802

    PubMed  Google Scholar 

  • CM Counter M Meyerson EN Eaton LW Ellisen SD Caddle DA Haber RA Weinberg (1998) ArticleTitleTelomerase activity is restored in human cells by ectopic expression of hTERT (hEST2), the catalytic subunit of telomerase. Oncogene 16 1217–1222 Occurrence Handle9528864

    PubMed  Google Scholar 

  • T de Lange L Shiue RM Myers DR Cox SL Naylor AM Killery HE Varmus (1990) ArticleTitleStructure and variability of human chromosome ends. Mol Cell Biol 10 518–527 Occurrence Handle2300052

    PubMed  Google Scholar 

  • de Lange T (1995) Telomere dynamics and genome instability in human cancer. In: Blackburn EH, Greider CW (eds) Telomeres. Cold Spring Harbor Laboratory Press, pp 265–293

  • MA Dunham AA Neumann CL Fasching RR Reddel (2000) ArticleTitleTelomere maintenance by recombination in human cells. Nat Genet 26 447–450 Occurrence Handle10.1038/82586 Occurrence Handle11101843

    Article  PubMed  Google Scholar 

  • SA Ely A Chadburn CM Dayton E Cesarman DM Knowles (2000) ArticleTitleTelomerase activity in B-cell non-Hodgkin lymphoma. Cancer 89 445–452 Occurrence Handle10.1002/1097-0142(20000715)89:2<445::AID-CNCR33>3.0.CO;2-T Occurrence Handle10918178

    Article  PubMed  Google Scholar 

  • AP Feinberg B Vogelstein (1983) ArticleTitleA technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132 6–13 Occurrence Handle10.1016/0003-2697(83)90418-9 Occurrence Handle6312838

    Article  PubMed  Google Scholar 

  • PM Glazer WC Summers (1985) ArticleTitleOncogene expression in isogenic, EBV-positive and -negative Burkitt lymphoma cell lines. Intervirology 23 82–89 Occurrence Handle2984143

    PubMed  Google Scholar 

  • E Gotoh T Yamagami H Yamamoto H Okamoto (1988) ArticleTitleChromosomal assignment of human VIP/PHM-27 gene to 6q26—q27 region by spot blot hybridization and in situ hybridization. Biochem Int 17 555–562 Occurrence Handle3202886

    PubMed  Google Scholar 

  • E Gotoh Y Asakawa H Kosaka (1995) ArticleTitleInhibition of protein serine/threonine phosphatases directly induces premature chromosome condensation in mammalian somatic cells. Bimed Res 16 63–68

    Google Scholar 

  • Greider CW (1995) Telomerase biochemistry and regulation. In: Blackburn EH, Greider CW (eds) Telomeres. Cold Spring Harbor Laboratory Press, pp 35–68

  • ML Gulley M Raphael CT Lutz DW Ross N Raab-Traub (1992) ArticleTitleEpstein-Barr virus integration in human lymphomas and lymphoid cell lines. Cancer 70 185–191 Occurrence Handle1318776

    PubMed  Google Scholar 

  • S Harada K Yanagi (1992) ArticleTitleInduced CD25 expression in a human B-lymphoma cell line transfected with the Epstein-Barr virus nuclear antigen 2 gene. Microbiol Immunol 36 479–494 Occurrence Handle1325025

    PubMed  Google Scholar 

  • S Harada Y Kamata Y Ishii H Eda R Kitamura M Obayashi S Ito F Ban J Kuranari H Nakajima T Kuze M Hayashi N Okabe H Senpuku N Miyasaka Y Nakamura H Kanegane K Yanagi (2004) ArticleTitleMaintenance of serum immunoglobulin G antibodies to Epstein-Barr virus (EBV) nuclear antigen 2 in healthy individuals from different age groups in a Japanese population with a high childhood incidence of asymptomatic primary EBV infection. Clin Diagn Lab Immunol 11 123–130 Occurrence Handle10.1128/CDLI.11.1.123-130.2004 Occurrence Handle14715558

    Article  PubMed  Google Scholar 

  • Harley CB (1995) Telomerase and aging. In: Blackburn EH, Greider CW (eds) Telomeres. Cold Spring Harbor Laboratory Press, pp 247–263

  • G Hatfull AT Bankier BG Barrell PJ Farrell (1988) ArticleTitleSequence analysis of Raji Epstein-Barr virus DNA. Virology 164 334–440 Occurrence Handle10.1016/0042-6822(88)90546-6 Occurrence Handle2835854

    Article  PubMed  Google Scholar 

  • JL Hecht JC Aster (2000) ArticleTitleMolecular biology of Burkitt’s lymphoma. J Clin Oncol 18 3707–3721 Occurrence Handle11054444

    PubMed  Google Scholar 

  • A Henderson S Ripley M Heller E Kieff (1983) ArticleTitleChromosome site for Epstein-Barr virus DNA in a Burkitt tumor cell line and in lymphocytes growth-transformed in vitro. Proc Natl Acad Sci USA 80 1987–1991 Occurrence Handle6300885

    PubMed  Google Scholar 

  • S Humme G Reisbach R Feederle HJ Delecluse K Bousset W Hammerschmidt A Schepers (2003) ArticleTitleThe EBV nuclear antigen 1 (EBNA1) enhances B cell immortalization several thousandfold. Proc Natl Acad Sci USA 100 10989–10994 Occurrence Handle10.1073/pnas.1832776100 Occurrence Handle12947043

    Article  PubMed  Google Scholar 

  • S Ito E Gotoh S Ozawa K Yanagi (2002) ArticleTitleEpstein-Barr virus nuclear antigen-1 is highly colocalized with interphase chromatin and its newly replicated regions in particular. J Gen Virol 83 2377–2383 Occurrence Handle12237418

    PubMed  Google Scholar 

  • S Ito K Yanagi (2003) ArticleTitleEpstein-Barr virus (EBV) nuclear antigen 1 colocalizes with cellular replication foci in the absence of EBV plasmids. J Virol 77 3824–3831 Occurrence Handle10.1128/JVI.77.6.3824-3831.2003 Occurrence Handle12610157

    Article  PubMed  Google Scholar 

  • MD Jones L Foster T Sheedy BE Griffin (1984) ArticleTitleThe EB virus genome in Daudi Burkitt’s lymphoma cells has a deletion similar to that observed in a non-transforming strain (P3HR-1) of the virus. EMBO J 3 813–821 Occurrence Handle6327290

    PubMed  Google Scholar 

  • G Kennedy J Komano B Sugden (2003) ArticleTitleEpstein-Barr virus provides a survival factor to Burkitt’s lymphomas. Proc Natl Acad Sci U S A 100 14269–14274 Occurrence Handle10.1073/pnas.2336099100 Occurrence Handle14603034

    Article  PubMed  Google Scholar 

  • Kieff E, Rickinson AB (2001) Epstein-Barr virus and its replication. In: Knipe DM, Howley PM (eds) Fields virology vol 2. Lippincott Williams & Wilkins, Philadelphia, New York, pp 2511–2573

  • NW Kim MA Piatyszek KR Prowse CB Harley MD West PL Ho GM Coviello WE Wright SL Weinrich JW Shay (1994) ArticleTitleSpecific association of human telomerase activity with immortal cells and cancer. Science 266 2011–2015 Occurrence Handle7605428

    PubMed  Google Scholar 

  • Y Kimura H Toki K Okabe K Suzuki T Hayakawa K Miyamoto (1986) ArticleTitleEstablishment and characterization of a monocytic cell line which expresses the interleukin-2 receptor. Jpn J Cancer Res 77 862–865 Occurrence Handle3095281

    PubMed  Google Scholar 

  • Kipling D (1995) The Telomere. Oxford University Press, Oxford

  • E Klein G Klein JS Nadkarni JJ Nadkarni H Wigzell P Clifford (1968) ArticleTitleSurface IgM-kappa specificity on a Burkitt lymphoma cell in vivo and in derived culture lines. Cancer Res 28 1300–1310 Occurrence Handle4174339

    PubMed  Google Scholar 

  • G Klein T Lindahl M Jondal W Leibold J Menezes K Nilsson C Sundstrom (1974) ArticleTitleContinuous lymphoid cell lines with characteristics of B cells (bone-marrow-derived), lacking the Epstein-Barr virus genome and derived from three human lymphomas. Proc Natl Acad Sci USA 71 3283–3286 Occurrence Handle4369887

    PubMed  Google Scholar 

  • G Klein B Giovanella A Westman JS Stehlin D Mumford (1975) ArticleTitleAn EBV-genome-negative cell line established from an American Burkitt lymphoma; receptor characteristics. EBV infectibility and permanent conversion into EBV-positive sublines by in vitro infection. Intervirology 5 319–334 Occurrence Handle181343

    PubMed  Google Scholar 

  • U Klein G Klein B Ehlin-Henriksson K Rajewsky R Kuppers (1995) ArticleTitleBurkitt’s lymphoma is a malignancy of mature B cells expressing somatically mutated V region genes. Mol Med 1 495–505 Occurrence Handle8529116

    PubMed  Google Scholar 

  • JB Lawrence CA Villnave RH Singer (1988) ArticleTitleSensitive, high-resolution chromatin and chromosome mapping in situ: presence and orientation of two closely integrated copies of EBV in a lymphoma line. Cell 52 51–61 Occurrence Handle10.1016/0092-8674(88)90530-2 Occurrence Handle2830981

    Article  PubMed  Google Scholar 

  • ER Leight B Sugden (2000) ArticleTitleEBNA-1: a protein pivotal to latent infection by Epstein-Barr virus. Rev Med Virol 10 83–100 Occurrence Handle10.1002/(SICI)1099-1654(200003/04)10:2<83::AID-RMV262>3.0.CO;2-T Occurrence Handle10713596

    Article  PubMed  Google Scholar 

  • B Lidin A Adams (1975) ArticleTitleSpontaneous interferon production and Epstein-barr virus antigen expression in two human lymphoid cell lines and their somatic cell hybrids. Intervirology 5 205–215 Occurrence Handle172473

    PubMed  Google Scholar 

  • JC Lin SC Lin BK De WP Chan BL Evatt WC Chan (1993) ArticleTitlePrecision of genotyping of Epstein-Barr virus by polymerase chain reaction using three gene loci (EBNA-2, EBNA-3C, and EBER): predominance of type A virus associated with Hodgkin’s disease. Blood 81 3372–3381 Occurrence Handle8389616

    PubMed  Google Scholar 

  • J Luka W Siegert G Klein (1977) ArticleTitleSolubilization of the Epstein-Barr virus-determined nuclear antigen and its characterization as a DNA-binding protein. J Virol 22 1–8 Occurrence Handle192908

    PubMed  Google Scholar 

  • I Magrath (1990) ArticleTitleThe pathogenesis of Burkitt’s lymphoma. Adv Cancer Res 55 133–270 Occurrence Handle2166998

    PubMed  Google Scholar 

  • MK Maini MV Soares CF Zilch AN Akbar PC Beverley (1999) ArticleTitleVirus-induced CD8+ T cell clonal expansion is associated with telomerase up-regulation and telomere length preservation: a mechanism for rescue from replicative senescence. J Immunol 162 4521–4526 Occurrence Handle10201990

    PubMed  Google Scholar 

  • V Marechal A Dehee R Chikhi-Brachet T Piolot M Coppey-Moisan JC Nicolas (1999) ArticleTitleMapping EBNA-1 domains involved in binding to metaphase chromosomes. J Virol 73 4385–4392 Occurrence Handle10196336

    PubMed  Google Scholar 

  • UM Martens V Brass L Sedlacek M Pantic C Exner Y Guo M Engelhardt PM Lansdorp CF Waller W Lange (2002) ArticleTitleTelomere maintenance in human B lymphocytes. Br J Haematol 119 810–818 Occurrence Handle10.1046/j.1365-2141.2002.03910.x Occurrence Handle12437664

    Article  PubMed  Google Scholar 

  • J Menezes W Leibold G Klein G Clements (1975) ArticleTitleEstablishment and characterization of an Epstein-Barr virus (EBC)-negative lymphoblastoid B cell line (BJA-B) from an exceptional, EBV-genome-negative African Burkitt’s lymphoma. Biomedicine 22 276–284 Occurrence Handle179629

    PubMed  Google Scholar 

  • JP Murnane L Sabatier BA Marder WF Morgan (1994) ArticleTitleTelomere dynamics in an immortal human cell line. EMBO J 13 4953–4962 Occurrence Handle7957062

    PubMed  Google Scholar 

  • M Nonoyama Y Kawai CH Huang JS Pagano Y Hirshaut PH Levine (1974) ArticleTitleEpstein-Barr virus DNA in Hodgkin’s disease, American Burkitt’s lymphoma, and other human tumors. Cancer Res 34 1228–1231 Occurrence Handle4366993

    PubMed  Google Scholar 

  • KF Norrback K Dahlenborg R Carlsson G Roos (1996) ArticleTitleTelomerase activation in normal B lymphocytes and non-Hodgkin’s lymphomas. Blood 88 222–229 Occurrence Handle8704177

    PubMed  Google Scholar 

  • O Nyormoi JH Sinclair G Klein (1973) ArticleTitleIsolation and characterization of an adherent, 8-azaguanine resistant variant of the Burkitt lymphoma cell line, Raji. Exp Cell Res 82 241–251 Occurrence Handle10.1016/0014-4827(73)90337-6 Occurrence Handle4358110

    Article  PubMed  Google Scholar 

  • BD Parker A Bankier S Satchwell B Barrell PJ Farrell (1990) ArticleTitleSequence and transcription of Raji Epstein-Barr virus DNA spanning the B95-8 deletion region. Virology 179 339–346 Occurrence Handle10.1016/0042-6822(90)90302-8 Occurrence Handle2171209

    Article  PubMed  Google Scholar 

  • A Polack H Delius U Zimber GW Bornkamm (1984) ArticleTitleTwo deletions in the Epstein-Barr virus genome of the Burkitt lymphoma nonproducer line Raji. Virology 133 146–157 Occurrence Handle10.1016/0042-6822(84)90433-1 Occurrence Handle6322426

    Article  PubMed  Google Scholar 

  • Pulvertaft RJV (1964) Cytology of Burkitt’s tumour. The Lancet i: 238–240

  • RJV Pulvertaft (1965) ArticleTitleA study of malignant tumours in Nigeria by short-term tissue culture. J Clin Pathol 18 261–273 Occurrence Handle14304234

    PubMed  Google Scholar 

  • A Ratsch S Joos P Kioschis P Lichter (2002) ArticleTitleTopological organization of the MYC/IGK locus in Burkitt’s lymphoma cells assessed by nuclear halo preparations. Exp Cell Res 273 12–20 Occurrence Handle10.1006/excr.2001.5429 Occurrence Handle11795942

    Article  PubMed  Google Scholar 

  • K Remes KF Norrback R Rosenquist C Mehle J Lindh G Roos (2000) ArticleTitleTelomere length and telomerase activity in malignant lymphomas at diagnosis and relapse. Br J Cancer 82 601–607 Occurrence Handle10.1054/bjoc.1999.0970 Occurrence Handle10682672

    Article  PubMed  Google Scholar 

  • Rickinson AB, Kieff E (2001) Epstein-Barr virus. In: Knipe DM, Howley PM (ed) Fields virology, vol 2. Lippincott Williams & Wilkins, pp 2575–2627

  • B Shiramizu F Barriga J Neequaye A Jafri R Dalla-Favera A Neri M Guttierez P Levine I Magrath (1991) ArticleTitlePatterns of chromosomal breakpoint locations in Burkitt’s lymphoma: relevance to geography and Epstein-Barr virus association. Blood 77 1516–1526 Occurrence Handle1849033

    PubMed  Google Scholar 

  • I Toplin G Schidlovsky (1966) ArticleTitlePartial purification and electron microscopy of virus in the EB-3 cell line derived from a Burkitt lymphoma. Science 152 1084–1085 Occurrence Handle5931456

    PubMed  Google Scholar 

  • J Wen YS Cong S Bacchetti (1998) ArticleTitleReconstitution of wild-type or mutant telomerase activity in telomerase-negative immortal human cells. Hum Mol Genet 7 1137–1141 Occurrence Handle10.1093/hmg/7.7.1137 Occurrence Handle9618172

    Article  PubMed  Google Scholar 

  • NP Weng BL Levine CH June RJ Hodes (1995) ArticleTitleHuman naive and memory T lymphocytes differ in telomeric length and replicative potential. Proc Natl Acad Sci USA 92 11091–11094 Occurrence Handle7479943

    PubMed  Google Scholar 

  • NP Weng L Granger RJ Hodes (1997) ArticleTitleTelomere lengthening and telomerase activation during human B cell differentiation. Proc Natl Acad Sci USA 94 10827–10832 Occurrence Handle10.1073/pnas.94.20.10827 Occurrence Handle9380719

    Article  PubMed  Google Scholar 

  • KJ Wu C Grandori M Amacker N Simon-Vermot A Polack J Lingner R Dalla-Favera (1999) ArticleTitleDirect activation of TERT transcription by c-MYC. Nat Genet 21 220–224 Occurrence Handle10.1038/6010 Occurrence Handle9988278

    Article  PubMed  Google Scholar 

  • T Yoshimura M Mayumi T Yorifuji KM Kim T Heike T Miyanomae K Shinomiya H Mikawa (1987) ArticleTitleEstablishment of a common acute lymphoblastic leukemia cell line (LC4-1) and effects of phorbol myristate acetate (PMA) on the surface antigen expression of the cell line. Am J Hematol 26 47–54 Occurrence Handle3115091

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Herpesvirus Laboratory, Department of Virology I, National Institute of Infectious Diseases, Tokyo, Japan

    A. Mochida, S. Harada, R. Kitamura & K. Yanagi

  2. Division of Genetic Resources, National Institute of Infectious Diseases, Tokyo, Japan

    E. Gotoh

  3. Department of Microbiology I, National Institute of Infectious Diseases, Tokyo, Japan

    H. Senpuku

  4. Institute of Medicinal Chemistry, Hoshi University, Tokyo, Japan

    A. Mochida & T. Takahashi

Authors
  1. A. Mochida
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. Gotoh
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. H. Senpuku
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. S. Harada
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. R. Kitamura
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. T. Takahashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. K. Yanagi
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mochida, A., Gotoh, E., Senpuku, H. et al. Telomere size and telomerase activity in Epstein-Barr virus (EBV)-positive and EBV-negative Burkitt’s lymphoma cell lines. Arch Virol 150, 2139–2150 (2005). https://doi.org/10.1007/s00705-005-0557-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-005-0557-2

Keywords

Search

Navigation