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01-03-2016 | Review and Perspectives

Mantle cell lymphoma—a spectrum from indolent to aggressive disease

Authors: Birgitta Sander, Leticia Quintanilla-Martinez, German Ott, Luc Xerri, Isinsu Kuzu, John K. C. Chan, Steven H. Swerdlow, Elias Campo

Published in: Virchows Archiv | Issue 3/2016

Abstract

Mantle cell lymphoma (MCL) is a distinctive lymphoma type generally characterized by the presence of CCND1 translocation and overexpression of cyclin D1. MCL usually presents with advanced stage and rapid clinical progression. The diagnosis is in most instances uncomplicated but cases with variant morphologies or immunophenotypes, especially cyclin D1-negative cases, may cause diagnostic difficulties. During the mantle cell lymphoma (MCL) session at the European Association of Haematopathology/Society for Hematopathology workshop 2014 held in Istanbul, Turkey, submitted cases illustrated interesting features such as unusual morphology or immunophenotypes. In several submitted cases of cyclin D1-positive MCL, CCND1 rearrangement could not be detected by t(11;14)(q13;q32) dual-color dual-fusion FISH but was suggested by CCND1 break-apart probes, and advantages and disadvantages of different FISH probes were highlighted. Three cyclin D1-negative MCL cases were submitted. These were identified by SOX11 immunohistochemistry and found to carry CCND2 translocations and/or to express high levels of cyclin D2 mRNA. Features associated with aggressive clinical course were presented including high expression of p53 protein and MYC aberrations. The need to integrate histological, immunophenotypic, genetic, and clinical data to arrive at the correct diagnosis was emphasized.

Morton LM, Sampson JN, Cerhan JR, Turner JJ, Vajdic CM, Wang SS, Smedby KE, de Sanjose S, Monnereau A, Benavente Y, Bracci PM, Chiu BC, Skibola CF, Zhang Y, Mbulaiteye SM, Spriggs M, Robinson D, Norman AD, Kane EV, Spinelli JJ, Kelly JL, La Vecchia C, Dal Maso L, Maynadie M, Kadin ME, Cocco P, Costantini AS, Clarke CA, Roman E, Miligi L, Colt JS, Berndt SI, Mannetje A, de Roos AJ, Kricker A, Nieters A, Franceschi S, Melbye M, Boffetta P, Clavel J, Linet MS, Weisenburger DD, Slager SL (2014) Rationale and design of the international lymphoma epidemiology consortium (InterLymph) non-Hodgkin lymphoma subtypes project. J Natl Cancer Inst Monogr 2014(48):1–14. doi:10.1093/jncimonographs/lgu005 CrossRefPubMedPubMedCentral

Swerdlow S, Campo E, Harris NE, Jaffe ES, Pileri SA, Stein H, Thiele J, Vardiman JW (2008) WHO classification of tumours of haematopoietic and lymphoid tissues. IARC press, Lyon

Reya T, O’Riordan M, Okamura R, Devaney E, Willert K, Nusse R, Grosschedl R (2000) Wnt signaling regulates B lymphocyte proliferation through a LEF-1 dependent mechanism. Immunity 13(1):15–24CrossRefPubMed

Tandon B, Peterson L, Gao J, Nelson B, Ma S, Rosen S, Chen YH (2011) Nuclear overexpression of lymphoid-enhancer-binding factor 1 identifies chronic lymphocytic leukemia/small lymphocytic lymphoma in small B-cell lymphomas. Mod Pathol 24(11):1433–1443. doi:10.1038/modpathol.2011.103 CrossRefPubMed

Menter T, Dirnhofer S, Tzankov A (2015) LEF1: a highly specific marker for the diagnosis of chronic lymphocytic B cell leukaemia/small lymphocytic B cell lymphoma. J Clin Pathol. doi:10.1136/jclinpath-2015-202862 PubMed

Walther N, Ulrich A, Vockerodt M, von Bonin F, Klapper W, Meyer K, Eberth S, Pukrop T, Spang R, Trumper L, Kube D (2013) Aberrant lymphocyte enhancer-binding factor 1 expression is characteristic for sporadic Burkitt’s lymphoma. Am J Pathol 182(4):1092–1098. doi:10.1016/j.ajpath.2012.12.013 CrossRefPubMed

Lord M, Wasik AM, Christensson B, Sander B (2015) Utility of mRNA analysis in defining SOX11 expression levels in mantle cell lymphoma and reactive lymph nodes. Haematologica. doi:10.3324/haematol.2015.123885 PubMedPubMedCentral

Ek S, Dictor M, Jerkeman M, Jirstrom K, Borrebaeck CA (2008) Nuclear expression of the non B-cell lineage Sox11 transcription factor identifies mantle cell lymphoma. Blood 111(2):800–805. doi:10.1182/blood-2007-06-093401 CrossRefPubMed

Mozos A, Royo C, Hartmann E, De Jong D, Baro C, Valera A, Fu K, Weisenburger DD, Delabie J, Chuang SS, Jaffe ES, Ruiz-Marcellan C, Dave S, Rimsza L, Braziel R, Gascoyne RD, Sole F, Lopez-Guillermo A, Colomer D, Staudt LM, Rosenwald A, Ott G, Jares P, Campo E (2009) SOX11 expression is highly specific for mantle cell lymphoma and identifies the cyclin D1-negative subtype. Haematologica 94(11):1555–1562. doi:10.3324/haematol.2009.010264 CrossRefPubMedPubMedCentral

10.

Gradowski JF, Sargent RL, Craig FE, Cieply K, Fuhrer K, Sherer C, Swerdlow SH (2012) Chronic lymphocytic leukemia/small lymphocytic lymphoma with cyclin D1 positive proliferation centers do not have CCND1 translocations or gains and lack SOX11 expression. Am J Clin Pathol 138(1):132–139. doi:10.1309/AJCPIVKZRMPF93ET CrossRefPubMedPubMedCentral

11.

Soldini D, Valera A, Sole C, Palomero J, Amador V, Martin-Subero JI, Ribera-Cortada I, Royo C, Salaverria I, Bea S, Gonzalvo E, Johannesson H, Herrera M, Colomo L, Martinez A, Campo E (2014) Assessment of SOX11 expression in routine lymphoma tissue sections: characterization of new monoclonal antibodies for diagnosis of mantle cell lymphoma. Am J Surg Pathol 38(1):86–93. doi:10.1097/PAS.0b013e3182a43996 CrossRefPubMed

12.

Wasik AM, Priebe V, Lord M, Jeppsson-Ahlberg A, Christensson B, Sander B (2014) Flow cytometric analysis of SOX11: a new diagnostic method for distinguishing B-cell chronic lymphocytic leukemia/small lymphocytic lymphoma from mantle cell lymphoma. Leuk Lymphoma 1–7. doi:10.3109/10428194.2014.953147

13.

Nakashima MO, Durkin L, Bodo J, Lin J, Quintanilla-Martinez L, Fu K, Hsi ED (2014) Utility and diagnostic pitfalls of SOX11 monoclonal antibodies in mantle cell lymphoma and other lymphoproliferative disorders. Appl Immunohistochem Mol Morphol AIMM/Off Publ Soc Appl Immunohistochem 22(10):720–727. doi:10.1097/PAI.0000000000000067 CrossRef

14.

Swerdlow SH, Zukerberg LR, Yang WI, Harris NL, Williams ME (1996) The morphologic spectrum of non-Hodgkin’s lymphomas with BCL1/cyclin D1 gene rearrangements. Am J Surg Pathol 20(5):627–640CrossRefPubMed

15.

Akhter A, Mahe E, Street L, Pournazari P, Perizzolo M, Shabani-Rad MT, Stewart DA, Mansoor A (2015) CD10-positive mantle cell lymphoma: biologically distinct entity or an aberrant immunophenotype? Insight, through gene expression profile in a unique case series. J Clin Pathol. doi:10.1136/jclinpath-2015-202955 PubMed

16.

Avet-Loiseau H, Garand R, Gaillard F, Daviet A, Mellerin MP, Robillard N, Bouyge I, Arcot S, Batzer M, Talmant P, Harousseau JL, Milpied N, Bataille R (1998) Detection of t(11;14) using interphase molecular cytogenetics in mantle cell lymphoma and atypical chronic lymphocytic leukemia. Genes Chromosomes Cancer 23(2):175–182CrossRefPubMed

17.

Li JY, Gaillard F, Moreau A, Harousseau JL, Laboisse C, Milpied N, Bataille R, Avet-Loiseau H (1999) Detection of translocation t(11;14)(q13;q32) in mantle cell lymphoma by fluorescence in situ hybridization. Am J Pathol 154(5):1449–1452. doi:10.1016/S0002-9440(10)65399-0 CrossRefPubMedPubMedCentral

18.

Delas A, Sophie D, Brousset P, Laurent C (2013) Unusual concomitant rearrangements of cyclin D1 and MYC genes in blastoid variant of mantle cell lymphoma: case report and review of literature. Pathol Res Pract 209(2):115–119. doi:10.1016/j.prp.2012.12.001 CrossRefPubMed

19.

Rocha CK, Praulich I, Gehrke I, Hallek M, Kreuzer KA (2011) A rare case of t(11;22) in a mantle cell lymphoma like B-cell neoplasia resulting in a fusion of IGL and CCND1: case report. Mol Cytogenet 4(1):8. doi:10.1186/1755-8166-4-8 CrossRefPubMedPubMedCentral

20.

Komatsu H, Iida S, Yamamoto K, Mikuni C, Nitta M, Takahashi T, Ueda R, Seto M (1994) A variant chromosome translocation at 11q13 identifying PRAD1/cyclin D1 as the BCL-1 gene. Blood 84(4):1226–1231PubMed

21.

Espinet B, Salaverria I, Bea S, Ruiz-Xiville N, Balague O, Salido M, Costa D, Carreras J, Rodriguez-Vicente AE, Luis Garcia J, Hernandez-Rivas JM, Calasanz MJ, Siebert R, Ferrer A, Salar A, Carrio A, Polo N, Garcia-Marco JA, Domingo A, Gonzalez-Barca E, Romagosa V, Marugan I, Lopez-Guillermo A, Milla F, Luis Mate J, Luno E, Sanzo C, Collado R, Oliver I, Monzo S, Palacin A, Gonzalez T, Sant F, Salinas R, Ardanaz MT, Font L, Escoda L, Florensa L, Serrano S, Campo E, Sole F (2010) Incidence and prognostic impact of secondary cytogenetic aberrations in a series of 145 patients with mantle cell lymphoma. Genes Chromosomes Cancer 49(5):439–451. doi:10.1002/gcc.20754 PubMed

22.

Wlodarska I, Meeus P, Stul M, Thienpont L, Wouters E, Marcelis L, Demuynck H, Rummens JL, Madoe V, Hagemeijer A (2004) Variant t(2;11)(p11;q13) associated with the IgK-CCND1 rearrangement is a recurrent translocation in leukemic small-cell B-non-Hodgkin lymphoma. Leukemia 18(10):1705–1710. doi:10.1038/sj.leu.2403459 CrossRefPubMed

23.

Woroniecka R, Grygalewicz B, Pienkowska-Grela B, Rymkiewicz G, Konecki R, Swoboda P, Janik P (2007) Variant t(2;11)(p11.2;q13) without IGK involvement in a case of mantle cell lymphoma. Cancer Genet Cytogenet 175(2):154–158. doi:10.1016/j.cancergencyto.2007.02.012 CrossRefPubMed

24.

Belaud-Rotureau MA, Parrens M, Dubus P, Garroste JC, de Mascarel A, Merlio JP (2002) A comparative analysis of FISH, RT-PCR, PCR, and immunohistochemistry for the diagnosis of mantle cell lymphomas. Mod Pathol 15(5):517–525CrossRefPubMed

25.

Ventura RA, Martin-Subero JI, Jones M, McParland J, Gesk S, Mason DY, Siebert R (2006) FISH analysis for the detection of lymphoma-associated chromosomal abnormalities in routine paraffin-embedded tissue. J Mol Diagn JMD 8(2):141–151. doi:10.2353/jmoldx.2006.050083 CrossRefPubMed

26.

Greisman HA, Lu Z, Tsai AG, Greiner TC, Yi HS, Lieber MR (2012) IgH partner breakpoint sequences provide evidence that AID initiates t(11;14) and t(8;14) chromosomal breaks in mantle cell and Burkitt lymphomas. Blood 120(14):2864–2867. doi:10.1182/blood-2012-02-412791 CrossRefPubMedPubMedCentral

27.

Fu K, Weisenburger DD, Greiner TC, Dave S, Wright G, Rosenwald A, Chiorazzi M, Iqbal J, Gesk S, Siebert R, De Jong D, Jaffe ES, Wilson WH, Delabie J, Ott G, Dave BJ, Sanger WG, Smith LM, Rimsza L, Braziel RM, Muller-Hermelink HK, Campo E, Gascoyne RD, Staudt LM, Chan WC (2005) Cyclin D1-negative mantle cell lymphoma: a clinicopathologic study based on gene expression profiling. Blood 106(13):4315–4321. doi:10.1182/blood-2005-04-1753 CrossRefPubMedPubMedCentral

28.

Salaverria I, Zettl A, Bea S, Moreno V, Valls J, Hartmann E, Ott G, Wright G, Lopez-Guillermo A, Chan WC, Weisenburger DD, Gascoyne RD, Grogan TM, Delabie J, Jaffe ES, Montserrat E, Muller-Hermelink HK, Staudt LM, Rosenwald A, Campo E (2007) Specific secondary genetic alterations in mantle cell lymphoma provide prognostic information independent of the gene expression-based proliferation signature. J Clin Oncol 25(10):1216–1222. doi:10.1200/JCO.2006.08.4251 CrossRefPubMedPubMedCentral

29.

Hartmann EM, Campo E, Wright G, Lenz G, Salaverria I, Jares P, Xiao W, Braziel RM, Rimsza LM, Chan WC, Weisenburger DD, Delabie J, Jaffe ES, Gascoyne RD, Dave SS, Mueller-Hermelink HK, Staudt LM, Ott G, Bea S, Rosenwald A (2010) Pathway discovery in mantle cell lymphoma by integrated analysis of high-resolution gene expression and copy number profiling. Blood 116(6):953–961. doi:10.1182/blood-2010-01-263806 CrossRefPubMedPubMedCentral

30.

Salaverria I, Royo C, Carvajal-Cuenca A, Clot G, Navarro A, Valera A, Song JY, Woroniecka R, Rymkiewicz G, Klapper W, Hartmann EM, Sujobert P, Wlodarska I, Ferry JA, Gaulard P, Ott G, Rosenwald A, Lopez-Guillermo A, Quintanilla-Martinez L, Harris NL, Jaffe ES, Siebert R, Campo E, Bea S (2013) CCND2 rearrangements are the most frequent genetic events in cyclin D1(−) mantle cell lymphoma. Blood 121(8):1394–1402. doi:10.1182/blood-2012-08-452284 CrossRefPubMedPubMedCentral

31.

Gesk S, Klapper W, Martin-Subero JI, Nagel I, Harder L, Fu K, Bernd HW, Weisenburger DD, Parwaresch R, Siebert R (2006) A chromosomal translocation in cyclin D1-negative/cyclin D2-positive mantle cell lymphoma fuses the CCND2 gene to the IGK locus. Blood 108(3):1109–1110. doi:10.1182/blood-2006-01-0015 CrossRefPubMed

32.

Shiller SM, Zieske A, Holmes H 3rd, Feldman AL, Law ME, Saad R (2011) CD5-positive, cyclin D1-negative mantle cell lymphoma with a translocation involving the CCND2 gene and the IGL locus. Cancer Genet 204(3):162–164. doi:10.1016/j.cancergencyto.2010.08.016 CrossRefPubMed

33.

Herens C, Lambert F, Quintanilla-Martinez L, Bisig B, Deusings C, de Leval L (2008) Cyclin D1-negative mantle cell lymphoma with cryptic t(12;14)(p13;q32) and cyclin D2 overexpression. Blood 111(3):1745–1746. doi:10.1182/blood-2007-10-120824 CrossRefPubMed

34.

Quintanilla-Martinez L, Slotta-Huspenina J, Koch I, Klier M, Hsi ED, de Leval L, Klapper W, Gesk S, Siebert R, Fend F (2009) Differential diagnosis of cyclin D2+ mantle cell lymphoma based on fluorescence in situ hybridization and quantitative real-time-PCR. Haematologica 94(11):1595–1598. doi:10.3324/haematol.2009.010173 CrossRefPubMedPubMedCentral

35.

Wlodarska I, Dierickx D, Vanhentenrijk V, Van Roosbroeck K, Pospisilova H, Minnei F, Verhoef G, Thomas J, Vandenberghe P, De Wolf-Peeters C (2008) Translocations targeting CCND2, CCND3, and MYCN do occur in t(11;14)-negative mantle cell lymphomas. Blood 111(12):5683–5690. doi:10.1182/blood-2007-10-118794 CrossRefPubMed

36.

Martin P, Chadburn A, Christos P, Weil K, Furman RR, Ruan J, Elstrom R, Niesvizky R, Ely S, Diliberto M, Melnick A, Knowles DM, Chen-Kiang S, Coleman M, Leonard JP (2009) Outcome of deferred initial therapy in mantle-cell lymphoma. J Clin Oncol 27(8):1209–1213. doi:10.1200/JCO.2008.19.6121 CrossRefPubMed

37.

Nygren L, Baumgartner Wennerholm S, Klimkowska M, Christensson B, Kimby E, Sander B (2012) Prognostic role of SOX11 in a population-based cohort of mantle cell lymphoma. Blood 119(18):4215–4223. doi:10.1182/blood-2011-12-400580 CrossRefPubMed

38.

Eve HE, Furtado MV, Hamon MD, Rule SA (2009) Time to treatment does not influence overall survival in newly diagnosed mantle-cell lymphoma. J Clin Oncol Off J Am Soc Clin Oncol 27(32):e189–e190. doi:10.1200/JCO.2009.23.9731, author reply e191 CrossRef

39.

Adam P, Schiefer AI, Prill S, Henopp T, Quintanilla-Martinez L, Bosmuller HC, Chott A, Fend F (2012) Incidence of preclinical manifestations of mantle cell lymphoma and mantle cell lymphoma in situ in reactive lymphoid tissues. Mod Pathol 25(12):1629–1636. doi:10.1038/modpathol.2012.117 CrossRefPubMed

40.

Carvajal-Cuenca A, Sua LF, Silva NM, Pittaluga S, Royo C, Song JY, Sargent RL, Espinet B, Climent F, Jacobs SA, Delabie J, Naresh KN, Bagg A, Brousset P, Warnke RA, Serrano S, Harris NL, Swerdlow SH, Jaffe ES, Campo E (2012) In situ mantle cell lymphoma: clinical implications of an incidental finding with indolent clinical behavior. Haematologica 97(2):270–278. doi:10.3324/haematol.2011.052621 CrossRefPubMedPubMedCentral

41.

Fend F, Cabecadas J, Gaulard P, Jaffe ES, Kluin P, Kuzu I, Peterson L, Wotherspoon A, Sundstrom C (2012) Early lesions in lymphoid neoplasia: conclusions based on the Workshop of the XV. Meeting of the European Association of Hematopathology and the Society of Hematopathology, in Uppsala, Sweden. J Hematop 5(3):169–199. doi:10.1007/s12308-012-0148-6 CrossRef

42.

Karube K, Scarfo L, Campo E, Ghia P (2014) Monoclonal B cell lymphocytosis and “in situ” lymphoma. Semin Cancer Biol 24:3–14. doi:10.1016/j.semcancer.2013.08.003 CrossRefPubMed

43.

Lecluse Y, Lebailly P, Roulland S, Gac AC, Nadel B, Gauduchon P (2009) t(11;14)-positive clones can persist over a long period of time in the peripheral blood of healthy individuals. Leukemia 23(6):1190–1193. doi:10.1038/leu.2009.31 CrossRefPubMed

44.

Hirt C, Schuler F, Dolken L, Schmidt CA, Dolken G (2004) Low prevalence of circulating t(11;14)(q13;q32)-positive cells in the peripheral blood of healthy individuals as detected by real-time quantitative PCR. Blood 104(3):904–905. doi:10.1182/blood-2004-02-0738 CrossRefPubMed

45.

Espinet B, Ferrer A, Bellosillo B, Nonell L, Salar A, Fernandez-Rodriguez C, Puigdecanet E, Gimeno J, Garcia-Garcia M, Vela MC, Luno E, Collado R, Navarro JT, de la Banda E, Abrisqueta P, Arenillas L, Serrano C, Lloreta J, Minana B, Cerutti A, Florensa L, Orfao A, Sanz F, Sole F, Dominguez-Sola D, Serrano S (2014) Distinction between asymptomatic monoclonal B-cell lymphocytosis with cyclin D1 overexpression and mantle cell lymphoma: from molecular profiling to flow cytometry. Clin Cancer Res. doi:10.1158/1078-0432.CCR-13-1077 PubMedPubMedCentral

46.

Espinet B, Sole F, Pedro C, Garcia M, Bellosillo B, Salido M, Florensa L, Camacho FI, Baro T, Lloreta J, Serrano S (2005) Clonal proliferation of cyclin D1-positive mantle lymphocytes in an asymptomatic patient: an early-stage event in the development or an indolent form of a mantle cell lymphoma? Hum Pathol 36(11):1232–1237. doi:10.1016/j.humpath.2005.08.021 CrossRefPubMed

47.

Fernandez V, Salamero O, Espinet B, Sole F, Royo C, Navarro A, Camacho F, Bea S, Hartmann E, Amador V, Hernandez L, Agostinelli C, Sargent RL, Rozman M, Aymerich M, Colomer D, Villamor N, Swerdlow SH, Pileri SA, Bosch F, Piris MA, Montserrat E, Ott G, Rosenwald A, Lopez-Guillermo A, Jares P, Serrano S, Campo E (2010) Genomic and gene expression profiling defines indolent forms of mantle cell lymphoma. Cancer Res 70(4):1408–1418. doi:10.1158/0008-5472.CAN-09-3419 CrossRefPubMed

48.

Racke F, Simpson S, Christian B, Blum KA, Hasserjian R, Zhao W (2010) Evidence of long latency periods prior to development of mantle cell lymphoma. Blood Abstract 116:323

49.

Edlefsen KL, Greisman HA, Yi HS, Mantei KM, Fromm JR (2011) Early lymph node involvement by mantle cell lymphoma limited to the germinal center: report of a case with a novel “follicular in situ” growth pattern. Am J Clin Pathol 136(2):276–281. doi:10.1309/AJCP6KFFGTC8PLVR CrossRefPubMed

50.

Christian B, Zhao W, Hamadani M, Sotomayor EM, Navarro W, Devine SM, Racke F, Blum KA (2010) Mantle cell lymphoma 12 years after allogeneic bone marrow transplantation occurring simultaneously in recipient and donor. J Clin Oncol 28(31):e629–e632. doi:10.1200/JCO.2010.29.8992 CrossRefPubMed

51.

Majlis A, Pugh WC, Rodriguez MA, Benedict WF, Cabanillas F (1997) Mantle cell lymphoma: correlation of clinical outcome and biologic features with three histologic variants. J Clin Oncol 15(4):1664–1671PubMed

52.

Tiemann M, Schrader C, Klapper W, Dreyling MH, Campo E, Norton A, Berger F, Kluin P, Ott G, Pileri S, Pedrinis E, Feller AC, Merz H, Janssen D, Hansmann ML, Krieken H, Moller P, Stein H, Unterhalt M, Hiddemann W, Parwaresch R (2005) Histopathology, cell proliferation indices and clinical outcome in 304 patients with mantle cell lymphoma (MCL): a clinicopathological study from the European MCL Network. Br J Haematol 131(1):29–38CrossRefPubMed

53.

Leitch HA, Gascoyne RD, Chhanabhai M, Voss NJ, Klasa R, Connors JM (2003) Limited-stage mantle-cell lymphoma. Ann Oncol 14(10):1555–1561CrossRefPubMed

54.

Nygren L, Wasik AM, Baumgartner-Wennerholm S, Jeppsson-Ahlberg A, Klimkowska M, Andersson P, Buhrkuhl D, Christensson B, Kimby E, Wahlin BE, Sander B (2014) T-cell levels are prognostic in mantle cell lymphoma. Clin Cancer Res. doi:10.1158/1078-0432.CCR-14-0889 PubMed

55.

Hoster E, Dreyling M, Klapper W, Gisselbrecht C, van Hoof A, Kluin-Nelemans HC, Pfreundschuh M, Reiser M, Metzner B, Einsele H, Peter N, Jung W, Wormann B, Ludwig WD, Duhrsen U, Eimermacher H, Wandt H, Hasford J, Hiddemann W, Unterhalt M (2008) A new prognostic index (MIPI) for patients with advanced-stage mantle cell lymphoma. Blood 111(2):558–565. doi:10.1182/blood-2007-06-095331 CrossRefPubMed

56.

Jares P, Colomer D, Campo E (2012) Molecular pathogenesis of mantle cell lymphoma. J Clin Invest 122(10):3416–3423. doi:10.1172/JCI61272 CrossRefPubMedPubMedCentral

57.

Ondrejka SL, Lai R, Smith SD, Hsi ED (2011) Indolent mantle cell leukemia: a clinicopathological variant characterized by isolated lymphocytosis, interstitial bone marrow involvement, kappa light chain restriction, and good prognosis. Haematologica 96(8):1121–1127. doi:10.3324/haematol.2010.036277 CrossRefPubMedPubMedCentral

58.

Royo C, Navarro A, Clot G, Salaverria I, Gine E, Jares P, Colomer D, Wiestner A, Wilson WH, Vegliante MC, Fernandez V, Hartmann EM, Trim N, Erber WN, Swerdlow SH, Klapper W, Dyer MJ, Vargas-Pabon M, Ott G, Rosenwald A, Siebert R, Lopez-Guillermo A, Campo E, Bea S (2012) Non-nodal type of mantle cell lymphoma is a specific biological and clinical subgroup of the disease. Leukemia 26(8):1895–1898. doi:10.1038/leu.2012.72 CrossRefPubMedPubMedCentral

59.

Orchard J, Garand R, Davis Z, Babbage G, Sahota S, Matutes E, Catovsky D, Thomas PW, Avet-Loiseau H, Oscier D (2003) A subset of t(11;14) lymphoma with mantle cell features displays mutated IgVH genes and includes patients with good prognosis, nonnodal disease. Blood 101(12):4975–4981CrossRefPubMed

60.

Navarro A, Clot G, Royo C, Jares P, Hadzidimitriou A, Agathangelidis A, Bikos V, Darzentas N, Papadaki T, Salaverria I, Pinyol M, Puig X, Palomero J, Vegliante MC, Amador V, Martinez-Trillos A, Stefancikova L, Wiestner A, Wilson W, Pott C, Calasanz MJ, Trim N, Erber W, Sander B, Ott G, Rosenwald A, Colomer D, Gine E, Siebert R, Lopez-Guillermo A, Stamatopoulos K, Bea S, Campo E (2012) Molecular subsets of mantle cell lymphoma defined by the IGHV mutational status and SOX11 expression have distinct biologic and clinical features. Cancer Res 72(20):5307–5316. doi:10.1158/0008-5472.CAN-12-1615 CrossRefPubMedPubMedCentral

61.

Chapman-Fredricks J, Sandoval-Sus J, Vega F, Lossos IS (2014) Progressive leukemic non-nodal mantle cell lymphoma associated with deletions of TP53, ATM, and/or 13q14. Ann Diagn Pathol 18(4):214–219. doi:10.1016/j.anndiagpath.2014.03.006 CrossRefPubMed

62.

Parry-Jones N, Matutes E, Morilla R, Brito-Babapulle V, Wotherspoon A, Swansbury GJ, Catovsky D (2007) Cytogenetic abnormalities additional to t(11;14) correlate with clinical features in leukaemic presentation of mantle cell lymphoma, and may influence prognosis: a study of 60 cases by FISH. Br J Haematol 137(2):117–124. doi:10.1111/j.1365-2141.2007.06526.x CrossRefPubMed

63.

Nordstrom L, Sernbo S, Eden P, Gronbaek K, Kolstad A, Raty R, Karjalainen ML, Geisler C, Ralfkiaer E, Sundstrom C, Laurell A, Delabie J, Ehinger M, Jerkeman M, Ek S (2014) SOX11 and TP53 add prognostic information to MIPI in a homogenously treated cohort of mantle cell lymphoma—a Nordic Lymphoma Group study. Br J Haematol 166(1):98–108. doi:10.1111/bjh.12854 CrossRefPubMedPubMedCentral

64.

Royo C, Salaverria I, Hartmann EM, Rosenwald A, Campo E, Bea S (2011) The complex landscape of genetic alterations in mantle cell lymphoma. Semin Cancer Biol 21(5):322–334. doi:10.1016/j.semcancer.2011.09.007 CrossRefPubMed

65.

Klapper W, Hoster E, Determann O, Oschlies I, van der Laak J, Berger F, Bernd HW, Cabecadas J, Campo E, Cogliatti S, Hansmann ML, Kluin PM, Kodet R, Krivolapov YA, Loddenkemper C, Stein H, Moller P, Barth TE, Muller-Hermelink K, Rosenwald A, Ott G, Pileri S, Ralfkiaer E, Rymkiewicz G, van Krieken JH, Wacker HH, Unterhalt M, Hiddemann W, Dreyling M (2009) Ki-67 as a prognostic marker in mantle cell lymphoma-consensus guidelines of the pathology panel of the European MCL Network. J Hematop. doi:10.1007/s12308-009-0036-x PubMedPubMedCentral

66.

Hao S, Sanger W, Onciu M, Lai R, Schlette EJ, Medeiros LJ (2002) Mantle cell lymphoma with 8q24 chromosomal abnormalities: a report of 5 cases with blastoid features. Mod Pathol 15(12):1266–1272. doi:10.1097/01.MP.0000037310.82136.99 CrossRefPubMed

67.

Michaux L, Wlodarska I, Theate I, Stul M, Scheiff JM, Deneys V, Ferrant A, Hagemeijer A (2004) Coexistence of BCL1/CCND1 and CMYC aberrations in blastoid mantle cell lymphoma: a rare finding associated with very poor outcome. Ann Hematol 83(9):578–583. doi:10.1007/s00277-004-0879-2 CrossRefPubMed

68.

Aukema SM, Siebert R, Schuuring E, van Imhoff GW, Kluin-Nelemans HC, Boerma EJ, Kluin PM (2011) Double-hit B-cell lymphomas. Blood 117(8):2319–2331. doi:10.1182/blood-2010-09-297879 CrossRefPubMed

69.

Pinyol M, Hernandez L, Cazorla M, Balbin M, Jares P, Fernandez PL, Montserrat E, Cardesa A, Lopez-Otin C, Campo E (1997) Deletions and loss of expression of p16INK4a and p21Waf1 genes are associated with aggressive variants of mantle cell lymphomas. Blood 89(1):272–280PubMed

70.

Chisholm KM, Bangs CD, Bacchi CE, Molina-Kirsch H, Cherry A, Natkunam Y (2015) Expression profiles of MYC protein and MYC gene rearrangement in lymphomas. Am J Surg Pathol 39(3):294–303. doi:10.1097/PAS.0000000000000365 CrossRefPubMed

71.

Oberley MJ, Rajguru SA, Zhang C, Kim K, Shaw GR, Grindle KM, Kahl BS, Kanugh C, Laffin J, Yang DT (2013) Immunohistochemical evaluation of MYC expression in mantle cell lymphoma. Histopathology 63(4):499–508. doi:10.1111/his.12207 PubMedPubMedCentral

72.

Halldorsdottir AM, Lundin A, Murray F, Mansouri L, Knuutila S, Sundstrom C, Laurell A, Ehrencrona H, Sander B, Rosenquist R (2011) Impact of TP53 mutation and 17p deletion in mantle cell lymphoma. Leukemia 25(12):1904–1908. doi:10.1038/leu.2011.162 CrossRefPubMed

73.

Slotta-Huspenina J, Koch I, de Leval L, Keller G, Klier M, Bink K, Kremer M, Raffeld M, Fend F, Quintanilla-Martinez L (2012) The impact of cyclin D1 mRNA isoforms, morphology and p53 in mantle cell lymphoma: p53 alterations and blastoid morphology are strong predictors of a high proliferation index. Haematologica 97(9):1422–1430. doi:10.3324/haematol.2011.055715 CrossRefPubMedPubMedCentral

74.

Greiner TC, Moynihan MJ, Chan WC, Lytle DM, Pedersen A, Anderson JR, Weisenburger DD (1996) p53 mutations in mantle cell lymphoma are associated with variant cytology and predict a poor prognosis. Blood 87(10):4302–4310PubMed

75.

Hernandez L, Fest T, Cazorla M, Teruya-Feldstein J, Bosch F, Peinado MA, Piris MA, Montserrat E, Cardesa A, Jaffe ES, Campo E, Raffeld M (1996) p53 gene mutations and protein overexpression are associated with aggressive variants of mantle cell lymphomas. Blood 87(8):3351–3359PubMed

76.

Katzenberger T, Kienle D, Stilgenbauer S, Holler S, Schilling C, Mader U, Puppe B, Petzoldt C, Sander S, Bullinger L, Stocklein H, Kalla J, Hartmann E, Adam P, Ott MM, Muller-Hermelink HK, Rosenwald A, Ott G (2008) Delineation of distinct tumour profiles in mantle cell lymphoma by detailed cytogenetic, interphase genetic and morphological analysis. Br J Haematol 142(4):538–550. doi:10.1111/j.1365-2141.2008.07199.x CrossRefPubMed

Title: Mantle cell lymphoma—a spectrum from indolent to aggressive disease
Authors: Birgitta Sander
Leticia Quintanilla-Martinez
German Ott
Luc Xerri
Isinsu Kuzu
John K. C. Chan
Steven H. Swerdlow
Elias Campo
Publication date: 01-03-2016
Publisher: Springer Berlin Heidelberg
Published in: Virchows Archiv / Issue 3/2016
Print ISSN: 0945-6317
Electronic ISSN: 1432-2307
DOI: https://doi.org/10.1007/s00428-015-1840-6

At a glance: The STEP trials

Springer Medicine

Mantle cell lymphoma—a spectrum from indolent to aggressive disease

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

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