Abstract
A novel recurrent translocation t(11;14)(p11;q32) was found in three patients with splenic marginal zone B cell lymphoma (MZBCL). Fluorescence in situ hybridization (FISH) studies with IgH probes revealed in all cases involvement of the IgH locus, with breakpoint downstream of the IGVH sequences. Partner genes at 11p11 were not identified. The translocation defined the stem line in two patients, who carried additional cytogenetic aberrations, including a 17p deletion, present in both cases. In one patient a 7q− chromosome was the primary cytogenetic defect, the t(11;14) having been found in four out of 11 abnormal metaphase cells at the time of transformation into high-grade MZBCL. Hematological features in all cases included splenomegaly with peripheral blood (PB) involvement by a monoclonal B cell population consisting of lymphocytes with villous projections and several blast-like cells. The immuno-phenotype was CD19+; CD22bright+; CD23−, CD10−, CD5−, surface Igbright+. A bone biopsy in one patient revealed an interstitial infiltration with an intrasinusoidal pattern of growth. Histological studies on spleen specimens in two patients showed an expanded marginal zone, with small lymphocytes and several blast-like cells. One patient had a therapy-demanding disease, with partial, short-term responses to cytotoxic treatment; one patient transformed into a high-grade MZBCL involving the gut, the PB and the bone marrow 2 years after diagnosis; one patient was unresponsive to cytotoxic treatment and underwent splenectomy. The t(11;14)(p11;q32) may define a subset of splenic MZBCL with a high-grade component and a relatively aggressive clinical behavior.
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References
Capello D, Gaidano G . Molecular pathophysiology of indolent lymphoma Haematologica 2000 85: 195–201
Fifth International Workshop on chromosomes in leukemia–lymphoma . Correlation of chromosome abnormalities with histologic and immunologic characteristics in non-Hodgkin's lymphoma and adult T-cell leukemia–lymphoma Blood 1987 70: 1554–1564
Cuneo A, Bigoni R, Rigolin GM, Roberti MG, Bardi A, Campioni D, Minotto C, Agostini P, Milani R, Bullrich F, Croce C, Castoldi GL . 13q14 deletion in non-Hodgkin's lymphoma: correlation with clinicopathological features Haematologica 1999 84: 589–593
Vandenberghe E, De Wolf-Peeters C, Van Den Oord J, Wlodarska I, Delabie J, Stul M, Thomas J, Michaux JL, Mecucci C, Cassiman JJ, Vandenberghe H . Translocation (11;14): a cytogenetic anomaly associated with B cell lymphomas of non-follicle centre cell lineage J Pathol 1991 163: 13–18
Macpherson N, Lesak D, Klasa R, Horsman D, Connors JM, Barnett M, Gascoyne RD . Small noncleaved, non Burkitt's (Burkitt-like) lymphoma: cytogenetics predict outcome and reflect clinical presentation J Clin Oncol 1999 17: 1558–1567
Schlegelberger B, Zwingers T, Harder T, Nowotny H, Siebert R, Vesely M, Bartels H, Sonnen R, Hopfinger G, Nader A, Ott G, Muller-Hermelink K, Feller A, Heinz R, for the Kiel–Wien-Lymphoma Study Group . Clinicopathogenetic significance of chromosomal abnormalities in patients with blastic peripheral B-cell lymphoma Blood 1999 94: 3114–3120
Offitt K, Lo Coco F, Louie DC, Parsa NZ, Leung D, Portlock C, Ye BH, Lista F, Filippa DA, Rosenbaum A, Landanyi M, Jhanwar S, Dalla-Favera R, Chaganti RSK . Rearrangement of BCL-6 gene as a prognostic marker in diffuse large-cell lymphoma N Engl J Med 1994 331: 74–80
Falini B, Pulford K, Pucciarini A, Carbone A, De Wolf-Peeters C, Cordell J, Fizzotti M, Santucci A, Pelicci PG, Pileri S, Campo E, Ott G, Delsol G, Mason DY . Lymphomas expressing ALK fusion protein(s) other than NPM-ALK Blood 1999 94: 3509–3515
Harris NL, Jaffe ES, Stein H, Banks PM, Chan JKC, Cleary ML, Delsol G, De Wolf-Peeters C, Falini B, Gatter KC, Grogan TM, Isaacson PG, Knowles DM, Mason DY, Muller-Hermelink HK, Pileri SA, Piris MA, Ralfkiaer E, Warnke RA . A revised European–American classification of lymphoid neoplasms: a proposal from the international lymphoma study group Blood 1994 84: 1361–1392
Harris NNL, Jaffe ES, Diebold J, Flandrin G, Muller-Hermelink HK, Vardiman J, Lister TA, Bloomfield CD . World Health Organization classification of neoplastic diseases of hematopoietic and lymphoid tissues: report of the clinical advisory committee – Airlie House, Virginia, November 1997 J Clin Oncol 1999 17: 3835–3849
Dierlamm J, Pittaluga S, Wlodarska I, Stul M, Thomas J, Boogaerts M, Michaux L, Driessen A, Mecucci C, Cassiman JJ, De Wolf-Peeters C, van Den Berghe H . Marginal zone B-cell lymphomas of different sites share similar cytogenetic and morphologic features Blood 1996 87: 299–307
Ott G, Katzenberger T, Greiner A, Kalla J, Rosenwald A, Heinrich U, Ott MM, Muller-Hermelink HK . The t(11;18) (q21;q21) chromosome translocation is a frequent and specific aberration in low-grade but not high-grade malignant non-Hodgkin's lymphomas of the mucosa-associated lymphoid tissue (MALT)-type Cancer Res 1997 57: 3944–3948
Dierlamm J, Baens M, Wlodarska I, Stefanova-Ouzounova M, Hernandez JM, Hossfeld DK, De Wolf Peeters C, Hagemeijer A, Van den Berghe H, Marynen P . The apoptosis inhibitor gene AP12 and a novel 18q gene, MLT, are recurrently rearranged in the t(11;18)(q21;q21) associated with MALT lymphomas Blood 1999 93: 3601–3609
Willis TG, Jadayel DM, Du MQ, Peng H, Perry AR, Abdul-Rauf M, Price H, Karran L, Majekodumni O, Wlodarska I, Pan L, Crook T, Hamoudi R, Isaacson PG, Dyer MJS . BCL10 is involved in t(1;14)(p22;q32) of MALT B cell lymphoma and mutated in multiple tumour types Cell 1999 96: 35–45
Zhang Q, Siebert R, Yan M, Hinzmann B, Cui X, Xue L, Rakestraw KM, Naeve CW, Beckmann G, Weisenburger DD, Sanger WG, Nowotny H, Vesely M, Callet-Bauchu E, Salles G, Dixit VM, Rosenthal A, Schlegelberger B, Morris SW . Inactivating mutations and overexpression of BCL10, a caspase recruitment domain containing gene, in MALT lymphoma with t(14)(p22;q32) Nat Genet 1999 22: 63–68
Morrison AM, Jager U, Chott A, Schebesta M, Haas OA, Busslinger M . Deregulated PAX-5 transcription from a translocated IgH promoter in marginal zone lymphoma Blood 1998 92: 3865–3878
Mateo M, Mollejo M, Villuendas R, Algara P, Sanchez-Beato M, Martìnez P, Piris MA . 7q31-32 allelic loss is a frequent finding in splenic marginal zone lymphoma Am J Pathol 1999 154: 1583–1589
Bennett JM, Catovsky D, Daniel MT, Flandrin G, Galton DAG, Gralnick HR, Sultan C . The French–American–British (FAB) Cooperative Group: proposals for the classification of chronic (mature) B and T lymphoid leukemias J Clin Pathol 1989 42: 567–584
Cuneo A, Bigoni R, Negrini M, Bullrich F, Veronese ML, Roberti MG, Bardi A, Rigolin GM, Cavazzini PL, Croce CM, Castoldi GL . Cytogenetic and interphase cytogenetic characterization of atypical chronic lymphocytic leukemia carrying BCL1 translocation Cancer Res 1997 57: 1144–1150
Cuneo A, Bigoni R, Rigolin GM, Roberti MG, Bardi A, Piva N, Milani R, Bullrich F, Veronese ML, Croce C, Birg F, Dohner H, Hagemeijer A, Castoldi GL . Cytogenetic profile of lymphoma of follicle mantle lineage: correlation with clinicobiological features Blood 1999 93: 1372–1380
Joos S, Haluska FG, Falk MH, Henglein B, Hameister H, Croce CM, Bornkamm GW . Mapping chromosomal breakpoints of Burkitt's (8;14) translocations far upstream of c-myc Cancer Res 1992 52: 6547–6552
Flanagan JG, Rabbitts TH . Arrangement of human immunoglobulin heavy chain constant region genes implies evolutionary duplication of a segment containing gamma, epsilon and alpha genes Nature 1982 300: 709–713
Sato T, Matsuda F, Lee KH, Shin EK, Honjo T . Physical linkage of a variable region segment and the joining region segment of the human immunoglobulin heavy chain locus Biochem Biophys Res Commun 1988 154: 265–271
Taniwaki M, Matsuda F, Jauch A, Nishida K, Takashima T, Tagawa S, Sugiyama H, Misawa S, Abe T, Kashima K . Detection of 14q32 translocations in B-cell malignancies by in situ hybridization with yeast artificial chromosome clones containing the human IgH gene locus Blood 1994 83: 2962–2969
Zhang Y, Matthiesen P, Harder S, Siebert R, Castoldi G, Calasanz MJ, Wong KF, Rosenwald A, Ott G, Atkin NB, Schlegelberger B . A 3-cM commonly deleted region in 6q21 in leukemias and lymphomas delineated by fluorescence in situ hybridization Genes Chromosomes Cancer 2000 27: 52–58
Dierlamm J, Wlodarska I, Michaux L, La-Starza R, Zeller W, Mecucci C, Van den Berghe H . Successful use of the same slide for consecutive fluorescence in situ hybridization experiments Genes Chromosomes Cancer 1996 16: 261–266
Gandini D, Aguiari GL, Cuneo A, Piva R, Castoldi GL, del Senno L . Novel small deletions of the p53 gene in late-stage B-cell chronic lymphocytic leukemia Br J Haematol 1994 88: 881–885
Motokura T, Bloom T, Kim HG, Juppner H, Ruderman JV, Kroneeberg HM, Arnold A . A novel cyclin encoded by a bcl1-linked candidate oncogene Nature 1991 350: 512–515
Tsujimoto Y, Jaffe E, Cossman J, Gorham J, Nowell PC, Croce CM . Clustering of breakpoints on chromosome 11 in human B-cell neoplasms with the t(11;14) chromosome translocation Nature 1985 315: 340–343
Williams ME, Meeker TC, Swerdlow SH . Rearrangement of the chromosome 11 bcl-1 locus in centrocytic lymphoma: analysis with multiple breakpoint probes Blood 1991 78: 493–498
Dalla Favera R, Martinotti S, Gallo R, Erikson J, Croce CM . Translocation and rearrangements of the c-myc oncogene locus in human indifferentiated B-cell lymphomas Science 1983 219: 963–967
Tsujimoto Y, Louie E, Bashir MM, Croce C . The reciprocal partners of both the t(14;18) and the t(11;14) translocations involved in B-cell neoplasms are rearranged by the same mechanism Oncogene 1988 2: 347–351
Gaidano GL, Volpe G, Pastore C, Chiarle R, Capello D, Gloghini A, Perissinotto E, Savinelli F, Bosco M, Mazza U, Pileri S, Palestro G, Carbone A, Saglio G . Detection of BCL-6 rearrangements and p53 mutations in malt-lymphomas Am J Hematol 1997 56: 206–213
Gaidano GL, Ballerini P, Gong JZ, Inghirami G, Neri A, Newcomb E, Magrath IT, Knowles DM, Dalla Favera R . P53 mutations in human lymphoid malignancies: associations with Burkitt lymphoma and chronic lymphocytic leukemia Proc Natl Acad Sci USA 1991 88: 5413–5416
Whang-Peng J, Knutsen T . Cytogenetics of non-Hodgkin's lymphomas In: Magrath I (ed.) The Non-Hodgkin's Lymphomas Arnold: London 1997 pp 277–308
Bloomfield CD, Arthur DC, Frizzera G, Levine EG, Peterson BA, Gajl-Peczalska KJ . Nonrandom chromosome abnormalities in lymphoma Cancer Res 1983 43: 2975–2984
Isaacson PG, Matutes E, Burke M, Catovsky D . The histopathology of splenic lymphoma with villous lymphocytes Blood 1994 84: 3828–3834
Troussard X, Valensi F, Duchayne E, Garand R, Felman P, Tulliez M, Henry-Amar M, Bryon PA, Flandrin G . Splenic lymphoma with villous lymphocytes: clinical presentation, biology and prognostic factors in a series of 100 patients. Groupe Francais d'Hematologie Cellulaire (GFHC) Br J Haematol 1996 93: 731–736
Franco V, Florena AM, Campesi G . Intrasinusoidal bone marrow infiltration: a possible hallmark of splenic lymphoma Histopathology 1996 29: 571–575
Zucca E, Roggero E, Pileri S . B-cell lymphoma of MALT type: a review with special emphasis on diagnostic and management problems of low-grade gastric tumours Br J Haematol 1998 100: 3–14
Matutes E, Owusu-Amkomah K, Morilla R, Garcia-Marco J, Houlian A, Que TH, Catovsky D . The immunological profile of B-cell disorders and proposal of a scoring system for the diagnosis of CLL Leukemia 1994 10: 1640–1645
Baldini L, Fracchiolla NS, Cro LM, Trecca D, Romitti L, Polli E, Maiolo AT, Neri A . Frequent p53 gene involvement in splenic B-cell leukemia/lymphomas of possible marginal zone origin Blood 1994 84: 270–278
Brynes RK, Almaguer PD, Leathery KE, McCourty A, Arber DA, Medeiros LJ, Nathwani BN . Numerical cytogenetic abnormalities of chromosomes 3, 7 and 12 in marginal zone B-cell lymphomas Mod Pathol 1996 9: 995–1000
Tirier C, Zhang Y, Plendl H, Weber-Matthiesen K, Langer W, Heit W, Schlegelberger B . Simultaneous presence of t(11;14) and a variant Burkitt's translocation in the terminal phase of a mantle cell lymphoma Leukemia 1996 10: 346–350
Cuneo A, Bigoni R, Rigolin GM, Roberti MG, Bardi A, Negrini M, Sabbioni S, Russo G, Narducci MG, Minotto C, Agostini P, Campioni D, Milani R, Castoldi GL . Acquired deletion of the ataxia teleangiectasia (ATM) locus in non-Hodgkin's lymphoma: correlation with clinicobiological features J Clin Oncol 2000 18: 2607–2614
Acknowledgements
We thank F Birg (Institut de Cancérologie e d'Immunologie de Marseille, INSERM 119, Marseille, France) for preparing the p53 and p16 probes; Dr J Billet and Dr I Van Den Berghe (AZ S Jan, Brugge) for providing histopathologic data of case 3. This work was supported by MURST 1999 ex 40% and 60%, by CNR, by CNR-MURST ‘Bridge’, by ISS Progetto sulla Terapia dei Tumori, by FIRC (CDA) and by FWO grand G 0338.01. The text presents research results of the Belgian programme on Interuniversity Poles of Attraction initiated by the Belgian State, Prime Minister's Office, Science Policy Programming. The scientific responsibility is assumed by the authors.
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Cuneo, A., Bardi, A., Wlodarska, I. et al. A novel recurrent translocation t(11;14)(p11;q32) in splenic marginal zone B cell lymphoma. Leukemia 15, 1262–1267 (2001). https://doi.org/10.1038/sj.leu.2402191
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DOI: https://doi.org/10.1038/sj.leu.2402191
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