Immunohistochemical and molecular characteristics with prognostic significance in diffuse large b-cell lymphoma

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Bellas, Carmen ^a   García, Diego ^a   Vicente, Yolanda ^a   Kilany, Linah ^a   Abraira, Victor ^b   Navarro, Belen ^a   Provencio, Mariano ^a   Martín, Paloma ^a  

^a HOSPITAL UNIVERSITARIO PUERTA DE HIERRO   (Spain)

^b HOSPITAL RAMÓN Y CAJAL   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

MYC PROTEIN; PROTEIN BCL 2; PROTEIN BCL 6; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXP1; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; BCL 2 GENE; BCL 6 GENE; CANCER PROGNOSIS; CANCER SURVIVAL; CHROMOSOME 18Q; CHROMOSOME TRANSLOCATION 18; CONTROLLED STUDY; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; FOXP1 GENE; GENE EXPRESSION; GENE REARRANGEMENT; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LARGE CELL LYMPHOMA; MAJOR CLINICAL STUDY; MALE; MOLECULAR PATHOLOGY; ONCOGENE MYC; OVERALL SURVIVAL; PHENOTYPE; PROTEIN EXPRESSION; TISSUE MICROARRAY; VERY ELDERLY; ADOLESCENT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MIDDLE AGED; PATHOLOGY; PROGNOSIS; SURVIVAL; TREATMENT OUTCOME; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE REARRANGEMENT; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION, FLUORESCENCE; LYMPHOMA, LARGE B-CELL, DIFFUSE; MALE; MIDDLE AGED; PROGNOSIS; PROTO-ONCOGENE PROTEINS C-MYC; SURVIVAL ANALYSIS; TREATMENT OUTCOME; YOUNG ADULT;

EID: 84902356511     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0098169     Document Type: Article

References (55)

1. Stein H, Warnke RA, Chan WC, Jaffe ES, Chan JKC, et al. (2008) WHO Classification of Tumours of Haematopoietic and Lymphoid Tissues. Diffuse large B-cell lymphoma, not otherwise specified. In: Swerdlow SH, Campo E, Harris NL, et al. : Lyon: IARC Press233-237.
2. Lossos IS, Czerwinski DK, Alizadeh AA, Wechser MA, Tibshirani R, et al. (2004) Prediction of survival in diffuse large-B-cell lymphoma based on the expression of six genes. N Engl J Med 350: 1828-1837. (Pubitemid 38917249)
3. Alizadeh AA, Eisen MB, Davis RE, Ma C, Lossos IS, et al. (2000) Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature 403: 503-511. (Pubitemid 30082188)
4. Lenz G, Wright G, Dave SS, Xiao W, Powell J, et al. (2008) Stromal gene signatures in large-B-cell lymphomas. N Engl J Med 359: 2313-2323.
5. Rosenwald A, Wright G, Chan WC, Connors JM, Campo E, et al. (2002) The use of molecular profiling to predict survival after chemotherapy for diffuse large-B-cell lymphoma. N Engl J Med 346: 1937-1947. (Pubitemid 34651353)
6. Shipp MA, Ross KN, Tamayo P, Weng AP, Kutok JL, et al. (2002) Diffuse large B-cell lymphoma outcome prediction by gene-expression profiling and supervised machine learning. Nat Med 8: 68-74. (Pubitemid 34101731)
7. Choi WW, Weisenburger DD, Greiner TC, Piris MA, Banham AH, et al. (2009) A new immunostain algorithm classifies diffuse large B-cell lymphoma into molecular subtypes with high accuracy. Clin Cancer Res 15: 5494-5502.
8. Hans CP, Weisenburger DD, Greiner TC, Gascoyne RD, Delabie J, et al. (2004) Confirmation of the molecular classification of diffuse large B-cell lymphoma by immunohistochemistry using a tissue microarray. Blood 103: 275-282. (Pubitemid 38029949)
9. Muris JJ, Meijer CJ, Vos W, van Krieken JH, Jiwa NM, et al. (2006) Immunohistochemical profiling based on Bcl-2, CD10 and MUM1 expression improves risk stratification in patients with primary nodal diffuse large B cell lymphoma. J Pathol 208: 714-723.
10. Gutierrez-Garcia G, Cardesa-Salzmann T, Climent F, Gonzalez-Barca E, Mercadal S, et al. (2011) Gene-expression profiling and not immunophenotypic algorithms predicts prognosis in patients with diffuse large B-cell lymphoma treated with immunochemotherapy. Blood 117: 4836-4843.
11. Meyer PN, Fu K, Greiner TC, Smith LM, Delabie J, et al. (2011) Immunohistochemical methods for predicting cell of origin and survival in patients with diffuse large B-cell lymphoma treated with rituximab. J Clin Oncol 29: 200-207.
12. Moskowitz CH, Zelenetz AD, Kewalramani T, Hamlin P, Lessac-Chenen S, et al. (2005) Cell of origin, germinal center versus nongerminal center, determined by immunohistochemistry on tissue microarray, does not correlate with outcome in patients with relapsed and refractory DLBCL. Blood 106: 3383-3385. (Pubitemid 41609171)
13. Banham AH, Connors JM, Brown PJ, Cordell JL, Ott G, et al. (2005) Expression of the FOXP1 transcription factor is strongly associated with inferior survival in patients with diffuse large B-cell lymphoma. Clin Cancer Res 11: 1065-1072. (Pubitemid 40175755)
14. Natkunam Y, Zhao S, Mason DY, Chen J, Taidi B, et al. (2007) The oncoprotein LMO2 is expressed in normal germinal-center B cells and in human B-cell lymphomas. Blood 109: 1636-1642. (Pubitemid 46239598)
15. Natkunam Y, Farinha P, Hsi ED, Hans CP, Tibshirani R, et al. (2008) LMO2 protein expression predicts survival in patients with diffuse large B-cell lymphoma treated with anthracycline-based chemotherapy with and without rituximab. J Clin Oncol 26: 447-454. (Pubitemid 351171698)
16. Barrans SL, Fenton JA, Banham A, Owen RG, Jack AS (2004) Strong expression of FOXP1 identifies a distinct subset of diffuse large B-cell lymphoma (DLBCL) patients with poor outcome. Blood 104: 2933-2935. (Pubitemid 39434982)
17. Hoeller S, Schneider A, Haralambieva E, Dirnhofer S, Tzankov A (2010) FOXP1 protein overexpression is associated with inferior outcome in nodal diffuse large B-cell lymphomas with non-germinal centre phenotype, independent of gains and structural aberrations at 3p14.1. Histopathology 57: 73-80.
18. Sagaert X, De PP, Libbrecht L, Vanhentenrijk V, Verhoef G, et al. (2006) Forkhead box protein P1 expression in mucosa-associated lymphoid tissue lymphomas predicts poor prognosis and transformation to diffuse large B-cell lymphoma. J Clin Oncol 24: 2490-2497. (Pubitemid 46630625)
19. Barrans SL, Evans PA, O'Connor SJ, Kendall SJ, Owen RG, et al. (2003) The t(14;18) is associated with germinal center-derived diffuse large B-cell lymphoma and is a strong predictor of outcome. Clin Cancer Res 9: 2133-2139. (Pubitemid 36687635)
20. Huang JZ, Sanger WG, Greiner TC, Staudt LM, Weisenburger DD, et al. (2002) The t(14;18) defines a unique subset of diffuse large B-cell lymphoma with a germinal center B-cell gene expression profile. Blood 99: 2285-2290. (Pubitemid 34525409)
21. Gascoyne RD, Adomat SA, Krajewski S, Krajewska M, Horsman DE, et al. (1997) Prognostic significance of Bcl-2 protein expression and Bcl-2 gene rearrangement in diffuse aggressive non-Hodgkin's lymphoma. Blood 90: 244-251. (Pubitemid 27276568)
22. Iqbal J, Sanger WG, Horsman DE, Rosenwald A, Pickering DL, et al. (2004) BCL2 translocation defines a unique tumor subset within the germinal center B-cell-like diffuse large B-cell lymphoma. Am J Pathol 165: 159-166. (Pubitemid 38821823)
23. Kramer MH, Hermans J, Wijburg E, Philippo K, Geelen E, et al. (1998) Clinical relevance of BCL2, BCL6, and MYC rearrangements in diffuse large B-cell lymphoma. Blood 92: 3152-3162. (Pubitemid 28492322)
24. van Imhoff GW, Boerma EJ, van der HB, Schuuring E, Verdonck LF, et al. (2006) Prognostic impact of germinal center-associated proteins and chromosomal breakpoints in poor-risk diffuse large B-cell lymphoma. J Clin Oncol 24: 4135-4142.
25. Vitolo U, Gaidano G, Botto B, Volpe G, Audisio E, et al. (1998) Rearrangements of bcl-6, bcl-2, c-myc and 6q deletion in B-diffuse large-cell lymphoma: clinical relevance in 71 patients. Ann Oncol 9: 55-61. (Pubitemid 28125765)
26. Barrans SL, O'Connor SJ, Evans PA, Davies FE, Owen RG, et al. (2002) Rearrangement of the BCL6 locus at 3q27 is an independent poor prognostic factor in nodal diffuse large B-cell lymphoma. Br J Haematol 117: 322-332. (Pubitemid 34451147)
27. Iqbal J, Greiner TC, Patel K, Dave BJ, Smith L, et al. (2007) Distinctive patterns of BCL6 molecular alterations and their functional consequences in different subgroups of diffuse large B-cell lymphoma. Leukemia 21: 2332-2343. (Pubitemid 350011706)
28. Jerkeman M, Aman P, Cavallin-Stahl E, Torlakovic E, Akerman M, et al. (2002) Prognostic implications of BCL6 rearrangement in uniformly treated patients with diffuse large B-cell lymphoma-a Nordic Lymphoma Group study. Int J Oncol 20: 161-165.
29. Niitsu N, Okamoto M, Nakamura N, Nakamine H, Aoki S, et al. (2007) Prognostic impact of chromosomal alteration of 3q27 on nodal B-cell lymphoma: correlation with histology, immunophenotype, karyotype, and clinical outcome in 329 consecutive patients. Leuk Res 31: 1191-1197.
30. Green TM, Young KH, Visco C, Xu-Monette ZY, Orazi A, et al. (2012) Immunohistochemical double-hit score is a strong predictor of outcome in patients with diffuse large B-cell lymphoma treated with rituximab plus cyclophosphamide, doxorubicin, vincristine, and prednisone. J Clin Oncol 30: 3460-3467.
31. Kluk MJ, Chapuy B, Sinha P, Roy A, Dal Cin P, et al. (2012) Immunohistochemical detection of MYC-driven diffuse large B-cell lymphomas. PLoS One 7: e33813.
32. Miller TP, Grogan TM, Dahlberg S, Spier CM, Braziel RM, et al. (1994) Prognostic significance of the of the Ki-67-associated proliferative antigen in aggressive non-Hodgkin's lymphomas: a prospective Southwest Oncology Group trial. Blood 83: 1460-1466. (Pubitemid 24081556)
33. Johnson NA, Slack GW, Savage KJ, Connors JM, Ben Neriah S, et al. (2012) Concurrent expression of MYC and BCL2 in diffuse large B-cell lymphoma treated with rituximab plus cyclophosphamide, doxorubicin, vincristine, and prednisone. J Clin Oncol 30: 3452-3459.
34. Savage KJ, Johnson NA, Ben Neriah S, Connors JM, Sehn LH, et al. (2009) MYC gene rearrangements are associated with a poor prognosis in diffuse large B-cell lymphoma patients treated with R-CHOP chemotherapy. Blood 114: 3533-3537.
35. Haralambieva E, Kleiverda K, Mason DY, Schuuring E, Kluin PM (2002) Detection of three common translocation breakpoints in non-Hodgkin's lymphomas by fluorescence in situ hybridization on routine paraffin-embedded tissue sections. J Pathol 198: 163-170. (Pubitemid 35243874)
36. Ventura RA, Martin-Subero JI, Jones M, McParland J, Gesk S, et al. (2006) FISH analysis for the detection of lymphoma-associated chromosomal abnormalities in routine paraffin-embedded tissue. J Mol Diagn 8: 141-151. (Pubitemid 43811236)
37. Goatly A, Bacon CM, Nakamura S, Ye H, Kim I, et al. (2008) FOXP1 abnormalities in lymphoma: translocation breakpoint mapping reveals insights into deregulated transcriptional control. Mod Pathol 21: 902-911. (Pubitemid 351896666)
38. Horn H, Ziepert M, Becher C, Barth TF, Bernd HW, et al. (2013) MYC status in concert with BCL2 and BCL6 expression predicts outcome in diffuse large Bcell lymphoma. Blood 121: 2253-2263.
39. Valera A, Lopez-Guillermo A, Cardesa-Salzmann T, Climent F, Gonzalez-Barca E, et al. (2013) MYC protein expression and genetic alterations have prognostic impact in patients with diffuse large B-cell lymphoma treated with immunochemotherapy. Haematologica 98: 1554-1562.
40. Cattoretti G, Chang CC, Cechova K, Zhang J, Ye BH, et al. (1995) BCL-6 protein is expressed in germinal-center B cells. Blood 86: 45-53.
41. Barrans SL, Carter I, Owen RG, Davies FE, Patmore RD, et al. (2002) Germinal center phenotype and bcl-2 expression combined with the International Prognostic Index improves patient risk stratification in diffuse large B-cell lymphoma. Blood 99: 1136-1143. (Pubitemid 34547064)
42. Kusumoto S, Kobayashi Y, Sekiguchi N, Tanimoto K, Onishi Y, et al. (2005) Diffuse large B-cell lymphoma with extra Bcl-2 gene signals detected by FISH analysis is associated with a "non-germinal center phenotype". Am J Surg Pathol 29: 1067-1073. (Pubitemid 41045552)
43. Visco C, Tzankov A, Xu-Monette ZY, Miranda RN, Tai YC, et al. (2013) Patients with diffuse large B-cell lymphoma of germinal center origin with BCL2 translocations have poor outcome, irrespective of MYC status: a report from an International DLBCL rituximab-CHOP Consortium Program Study. Haematologica 98: 255-263.
44. Nitsu N, Okamoto M, Miura I, Hirano M (2009) Clinical significance of 8q24/c-MYC translocation in diffuse large B-cell lymphoma. Cancer Sci 100: 233-237.
45. Zhang HW, Chen ZW, Li SH, Bai W, Cheng NL, et al. (2011) Clinical significance and prognosis of MYC translocation in diffuse large B-cell lymphoma. Hematol Oncol 29: 185-189.
46. Hu S, Xu-Monette ZY, Tzankov A, Green T, Wu L, et al. (2013) MYC/BCL2 protein coexpression contributes to the inferior survival of activated B-cell subtype of diffuse large B-cell lymphoma and demonstrates high-risk gene expression signatures: a report from The International DLBCL Rituximab-CHOP Consortium Program. Blood 121: 4021-4031.
47. Haralambieva E, Adam P, Ventura R, Katzenberger T, Kalla J, et al. (2006) Genetic rearrangement of FOXP1 is predominantly detected in a subset of diffuse large B-cell lymphomas with extranodal presentation. Leukemia 20: 1300-1303. (Pubitemid 43905839)
48. Wlodarska I, Veyt E, De PP, Vandenberghe P, Nooijen P, et al. (2005) FOXP1, a gene highly expressed in a subset of diffuse large B-cell lymphoma, is recurrently targeted by genomic aberrations. Leukemia 19: 1299-1305. (Pubitemid 41136318)
49. Jais JP, Haioun C, Molina TJ, Rickman DS, de Reynies A, et al. (2008) The expression of 16 genes related to the cell of origin and immune response predicts survival in elderly patients with diffuse large B-cell lymphoma treated with CHOP and rituximab. Leukemia 22: 1917-1924.
50. Copie-Bergman C, Gaulard P, Leroy K, Briere J, Baia M, et al. (2009) Immunofluorescence in situ hybridization index predicts survival in patients with diffuse large B-cell lymphoma treated with R-CHOP: a GELA study. J Clin Oncol 27: 5573-5579.
51. Craig VJ, Cogliatti SB, Imig J, Renner C, Neuenschwander S, et al. (2011) Myc-mediated repression of microRNA-34a promotes high-grade transformation of B-cell lymphoma by dysregulation of FoxP1. Blood 117: 6227-6236.
52. Rao DS, O'Connell RM, Chaudhuri AA, Garcia-Flores Y, Geiger TL, et al. (2010) MicroRNA-34a perturbs B lymphocyte development by repressing the forkhead box transcription factor Foxp1. Immunity 33: 48-59.
53. Li S, Lin P, Fayad LE, Lennon PA, Miranda RN, et al. (2012) B-cell lymphomas with MYC/8q24 rearrangements and IGH@BCL2/t(14;18)(q32;q21): an aggressive disease with heterogeneous histology, germinal center B-cell immunophenotype and poor outcome. Mod Pathol 25: 145-156.
54. Pedersen MØ, Gang AO, Poulsen TS, Knudsen H, Lauritzen AF, et al. (2014) Double-hit BCL2/MYC translocations in a consecutive cohort of patients with large B-cell lymphoma - a single centre's. Eur J Hematol 92: 42-48.
55. Scott DW, Wright GW, Williams PM, Lih CJ, Walsh W, et al. (2014) Determining cell-of-origin subtypes of diffuse large B-cell lymphoma using gene expression in formalin-fixed paraffin embedded tissue. Blood 123: 1214-1217.