B-cell differentiation, apoptosis and proliferation in diffuse large B-cell lymphomas

Anticancer Research

Volumn 25, Issue 1 A, 2005, Pages 347-362

  Bai, Maria ^a   Skyrlas, Angelos ^a   Agnantis, Niki J ^a   Kamina, Sevasti ^a   Papoudou Bai, Alexandra ^a   Kitsoulis, Panagiotis ^a   Kanavaros, Panagiotis ^a  

^a UNIVERSITY OF IOANNINA   (Greece)

Author keywords

Apoptosis; Differentiation; Diffuse large B cell lymphomas; Proliferation

Indexed keywords

COMMON ACUTE LYMPHOBLASTIC LEUKEMIA ANTIGEN; PROTEIN; PROTEIN BCL 6; PROTEIN MUM1; SYNDECAN 1; UNCLASSIFIED DRUG;

APOPTOSIS; B CELL LYMPHOMA; B LYMPHOCYTE; B LYMPHOCYTE DIFFERENTIATION; CELL CYCLE; DIFFUSE LARGE B CELL LYMPHOMA; DNA MICROARRAY; GENE EXPRESSION; GENE EXPRESSION PROFILING; HISTOPATHOLOGY; HUMAN; IMMUNOHISTOCHEMISTRY; IMMUNOPHENOTYPING; LYMPHOCYTE PROLIFERATION; NONHODGKIN LYMPHOMA; NONHUMAN; PREDICTION; PRIORITY JOURNAL; REVIEW;

ANIMALS; APOPTOSIS; B-LYMPHOCYTES; CELL DIFFERENTIATION; HUMANS; LYMPHOMA, B-CELL; LYMPHOMA, LARGE-CELL, DIFFUSE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS;

EID: 16344370583     PISSN: 02507005     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (163)

1. Rossi D and Gaidano G: Molecular heterogeneity of diffuse large B-cell lymphoma: implications for disease management and prognosis. Hematology 7: 239-252, 2002.
2. Lossos IS and Levy R: Diffuse large B-cell lymphoma: insights gained from gene expression profiling. Int J Hematol 77: 321-329, 2003.
3. Sanchez-Beato M, Sanchez-Aguilera A and Piris MA: Cell cycle deregulation in B-cell lymphomas. Blood 101: 1220-1235, 2003.
4. Pileri SA, Ascani S, Sabatini E, Fraternali-Orcioni G, Poggi S, Piccioli M, Piccaluga PP, Gamberi B, Zinzani PL, Leoncini L and Falini B: The pathologist's view point. Part II-aggressive lymphomas. Haematologica 85: 1308-1321, 2000.
5. Pileri SA, Dirnhofer S, Went P, Ascani S, Sabattini E, Marafioti T, Tzankov A, Leoncini L, Falini B and Zinzani PL: Diffuse large B-cell lymphoma: one or more entities? Present controversies and possible tools for its subclassification. Histopathology 41: 482-509, 2002.
6. de Leval L and Harris NL: Variability in immunophenotype in diffuse large B-cell lymphoma and its clinical relevance. Histopathology 43: 509-528, 2003.
7. Berglund M, Enblad G, Flordal E, Lui WO, Backlin C, Thunberg U, Sundstrom C, Roos G, Allender SV, Erlanson M, Rosenquist R, Larsson C and Lagercrantz S: Chromosomal imbalances in diffuse large B-cell lymphoma detected by comparative genomic hybridization. Mod Pathol 15: 807-816, 2002.
8. Shaffer AL, Rosenwald A and Staudt LM: Lymphoid malignancies: the dark side of B-cell differentiation. Nat Rev Immunol 2: 920-932, 2002.
9. Falini B and Mason DY: Proteins encoded by genes involved in chromosomal alterations in lymphoma and leukaemia: clinical value of their detection by immunocytochemistry. Blood 99: 409-426, 2002.
10. Leoncini L, Lazzi S, Bellan C and Tosi P: Cell kinetics and cell cycle regulation in lymphomas. J Clin Pathol 55: 648-655, 2002.
11. Moller MB, Pedersen NT and Christensen BE: Diffuse large B-cell lymphoma: clinical implications of extranodal versus nodal presentation-a population-based study of 1575 cases. Br J Haematol 124: 151-159, 2004.
12. Tzardi M, Kouvidou C, Panayiotides J, Stefanaki S, Koutsoubi K, Zois E, Rontogianni D, Eliopoulos G, Delides G and Kanavaros P: Expression of p53, mdm2 and p21/waf-1 proteins in non-Hodgkin's lymphomas. J Clin Pathol (Mol Pathol) 49: M278-283, 1996.
13. WAF1/CIP1 and mdm2 expression in non-Hodgkin's lymphoma and their relationship to p53 status: a p53+, mdm2, p21- immunophenotype associated with missense p53 mutations. J Pathol 181: 51-61, 1997.
14. Kalogeraki A, Tzardi M, Panayiotides I, Bolioti S, Koutsoubi K, Stefanaki K, Zois E, Karidi E, Delides G and Kanavaros P: Ki67 (MIB) expression in non-Hodgkin's lymphomas. Anticancer Res 17: 487-492, 1997.
15. Villuendas R, Sanchez-Beato M, Martinez JC, Saez A, Martinez-Delgado B, Garcia J, Sol-Mateo M, Sanchez-Verde L, Beniter J, Martinez P and Piris M: Loss of p16/INK4A protein expression in non-Hodgkin's lymphomas is a frequent finding associated with tumor progression. Am J Pathol 153: 887-897, 1998.
16. Lai R, Medeiros LJ, Coupland R, McCourty A and Brynes RK: Immunohistochemical detection of E2F-1 in non-Hodgkin's lymphomas: a survey of 124 cases. Mod Pathol 11: 457-463, 1998.
17. Stefanaki, K, Tzardi M, Kouvidou C, Rontogianni D, Bolioti S, Chaniotis V, Vlychou M, Delides G and Kanavaros P: Expression of p53, mdm2, p21, Rb, Ki67, bcl2 and bax proteins in lymphomas of the mucosa-associated lymphoid tissue. Anticancer Res 18: 2403-2408, 1998.
18. Erlanson M, Portin C, Linderholm B, Lindh J, Roos G and Landberg G: Expression of cyclin E and the cyclin-dependent kinase inhibitor p27 in malignant lymphomas-prognostic implications. Blood 92: 770-777, 1998.
19. Moller MB, Ino Y, Gerdes AM, Skjodt K, Louis DN and Pedersen NT: Aberrations of the p53 pathway components p53, mdm2 and CDKN2A appear independent in diffuse large B cell lymphoma. Leukemia 13: 453-459, 1999.
20. Sanchez-Beato M, Camacho FI, Martinez-Montero JC, Saez AI, Villuendas R, Sanchez-Verde L, Garcia JF and Piris MA: Anomalous high p27/KIP1 expression in a subset of aggressive B-cell lymphomas is associated with cyclin D3 overexpression and P27/KIP1-cyclin D3 colocalization in tumor cells. Blood 94: 765-772, 1999.
21. Moller MB, Nielsen O and Pedersen NT: Oncoprotein MDM2 overexpression is associated with poor prognosis in distinct non-Hodgkin's lymphoma entities. Mod Pathol 12: 1010-1016, 1999.
22. Moller MB, Kania PW, Ino Y, Gerdes AM, Nielsen O, Louis DN, Skjodt K and Pedersen NT: Frequent disruption of the RB1 pathway in diffuse large B cell lymphoma: prognostic significance of E2F-1 and p161NK4A. Leukemia 14: 898-904, 2000.
23. Gronbaek K, de Nully Brown P, Moller MB, Nedergaard T, Ralfkiaer E, Moller P, Zeuthen J and Guldberg P: Concurrent disruption of p16INK4a and the ARF-p53 pathway predicts poor prognosis in aggressive non-Hodgkin's lymphoma. Leukemia 14: 1727-1735, 2001.
24. Sanchez-Beato M, Saez AI, Navas IC, Algara P, Sol Mateo M, Villuendas R, Sanchez-Aguilera A, Camacho FI, Sanchez E and Piris MA: Overall survival in aggressive B-cell lymphomas is dependent on the accumulation of alterations in p53, p16 and p27. Am J Pathol 159: 205-213, 2001.
25. Pabst T, Peters UR, Tinguely M, Scwaller J, Tschan M, Aebi S, Vonlanthev S, Borisch B, Betticher DC, Zimmerman A, Tobler A and Fey MF: Divergent expression of cyclin-dependent kinase inhibitors (Cki) and P14ARF/p16beta in non-Hodgkin's lymphomas and chronic lymphocytic leukemia. Leuk Lymphoma 37: 639-648, 2000.
26. Navratil E, Gaulard P, Kanavaros P, Audouin J, Bougaran J, Martin N, Diebold J and Mason DY: BCL-2 protein expression in mucosa-associated lymphoid tissue lymphomas. J Clin Pathol 48: 18-21, 1995.
27. Kiberu SW, Pringle JH, Sobolewski S, Murphy P and Lauder I: Correlation between apoptosis, proliferation and bcl-2 expression in malignant non-Hodgkin's lymphomas. J Clin Pathol (Mol Pathol) 49: M268-272, 1996.
28. Krajewski S, Gascoyne RD, Zapata JM, Krajewska M, Kitada S, Chhanabhai M, Horsman D, Berean K, Piro LD, Fugier-Vivier I, Liu YJ, Wang HG and Reed JC: Immunolocalization of the ICE/Ced-3-family protease, CPP32 (Caspase-3), in non-Hodgkin's lymphomas, chronic lymphocytic leukemias, and reactive lymph nodes. Blood 89: 3817-3825, 1997.
29. Gascoyne RD, Krajewska M, Krajewski S, Connors JM and Reed JC: Prognostic significance of Bax protein expression in diffuse aggressive non-Hodgkin's lymphoma. Blood 90: 3173-3178, 1997.
30. Wheaton S, Netser J, Guinee D, Rahn M and Perkins S: Bcl-2 and bax protein expression in indolent versus aggressive B-cell non-Hodgkin's lymphomas. Hum Pathol 29: 820-825, 1998.
31. Winter JN, Andersen J, Reed JC, Krajewski S, Variakojis D, Bauer KD, Fisher RI, Gordon LI, Oken MM, Jiang S, Jeffries D and Domer P: BCL-2 expression correlates with lower proliferative activity in the intermediate- and high-grade non-Hodgkin's lymphomas: an Eastern Cooperative Oncology Group and Southwest Oncology Group cooperative laboratory study. Blood 91: 1391-1398, 1998.
32. Bairey O, Zimra Y, Shaklai M, Okon E and Rabizadeh E: Bcl-2, Bcl-X, Bax, and Bak expression in short- and long-lived patients with diffuse large B-cell lymphomas. Clin Cancer Res 5: 2860-2866, 1999.
33. Fang JM, Finn WG, Hussong JW, Goolsby CL, Cubbon AR and Variankojis D: CD 10 antigen expression correlates with the t(14;18)(q32;q21) major breakpoint region in diffuse large B-cell lymphoma. Mod Pathol 12: 295-300, 1999.
34. Skinnider FB, Horsman ED, Dupuis B and Gascoyne DR: Bcl-6 and Bcl-2 protein expression in diffuse large B-cell lymphoma and follicular lymphoma: correlation with 3q27 and 18q21 chromosomal abnormalities. Hum Pathol 30: 803-808, 1999.
35. Camilleri-Brouet S, Camparo P, Mokhtari K, Xuan KH, Martin A, Arborio M, Hauw JJ and Raphael M: Overexpression of BCL-2, BCL-X, and BAX in primary central nervous system lymphomas that occur in immunosuppressed patients. Mod Pathol 13: 158-165, 2000.
36. Dogan A, Bagdi E, Munson P and Isaacson PG: CD 10 and BCL-6 expression in paraffin sections of normal lymphoid tissue and B-cell lymphomas. Am J Surg Pathol 26: 846-852, 2000.
37. King BE, Chen C, Locker J, Kant J, Okuyama K, Falini B and Swerdlow SH: Immunophenotypic and genotypic markers of follicular center cell neoplasia in diffuse large B-cell lymphomas. Mod Pathol 13: 1219-1231, 2000.
38. Barrans LS, Carter I, Owen GR, Davies EF, Patmore DR, Haynes PA, Morgan JG and Jack SA: 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, 2002.
39. Huang JZ, Sanger WG, Greiner TC, Staudt LM, Weisenburger DD, Pickering DL, Lynch JC, Armitage JO, Warnke RA, Alizadeh AA, Lossos IS, Levy R and Chan WC: 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, 2002.
40. Barrans SL, Evans PA, O'Connor SJ, Kendall SJ, Owen RG, Haynes AP, Morgan GJ and Jack AS: 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, 2003.
41. Xerri L, Parc P, Brousset P, Schlaifer D, Hassoun J, Reed JC, Krajewski S and Birnbaum D. Predominant expression of the long isoform of Bcl-x (Bcl-xL) in human lymphomas. Br J Haematol 92: 900-906, 1996.
42. MacNamara B, Wang W, Chen Z, Hou M, Mazur J, Gruber A and Porwit-MacDonald A: Telomerase activity in relation to pro- and anti-apoptotic protein expression in high grade non-Hodgkin's lymphomas. Haematologica 86: 386-393, 2001.
43. Pagnano KB, Silva MD, Vassallo J, Aranha FJ and Saad ST: Apoptosis-regulating proteins and prognosis in diffuse large B cell non-Hodgkin's lymphomas. Acta Haematol 107: 29-34, 2002.
44. Sohn SK, Jung JT, Kim DH, Kim JG, Kwak EK, Park T, Shin DG, Sohn KR and Lee KB: Prognostic significance of bcl-2, bax and p53 expression in diffuse large B-cell lymphoma. Am J Hematol 73: 101-107, 2003.
45. Hirokawa M, Kawabata Y and Miura AB: Deregulation of apoptosis and a novel mechanism of defective apoptotic signal transduction in human B-cell lymphomas. Leuk Lymphoma 43: 243-249, 2002.
46. Xerri L, Devilard E, Hassoun J, Haddad P and Birg F: Malignant and reactive cells from human lymphomas frequently express Fas ligand but display a different sensitivity to Fas-mediated apoptosis. Leukemia 11: 1868-1877, 1997.
47. Plumas J, Jacob MC, Chaperot L, Molens JP, Sotto JJ and Bensa JC: Tumor B cells from non-Hodgkin's lymphoma are resistant to CD95 (Fas/Apo-1)-mediated apoptosis. Blood 91: 2875-2885, 1998.
48. Xerri L, Devilard E, Bouabdallah R, Hassoun J, Chaperot L, Birg F and Plumas J: Quantitative analysis detects ubiquitous expression of apoptotic regulators in B cell non-Hodgkin's lymphomas. Leukemia 13: 1548-1553, 1999.
49. Xerri L, Palmerini F, Devilard E, Defrance T, Bouabdalah R, Hassoun J and Birg F: Frequent nuclear localization of ICAD and cytoplasmic co-expression of caspase-8 and caspase-3 in human lymphomas. J Pathol 192: 194-202, 2000.
50. Dukers DF, Oudejans JJ, Vos W, ten Berger RL and Meijer CJ: Apoptosis in B-cell lymphomas and reactive lymphoid tissue always involves activation of caspase 3 as determined by a new in situ method. J Pathol 196: 307-315, 2002.
51. Smolewski P, Darzynkiewicz Z and Robak T: Caspase-mediated cell death in hematological malignancies: theoretical considerations, methods of assessment and clinical implications. Leuk Lymphoma 44: 1089-1104, 2003.
52. Adida C, Haioun C, Gaulard P, Lepage E, Morel P, Briere J, Dombret H, Reyes F, Diebold J, Gisselbrecht C, Salles G, Altieri DC and Molina TJ: Prognostic significance of survivin expression in diffuse large B-cell lymphomas. Blood 96: 1921-1925, 2000.
53. Kuttler F, Valnet-Rabier MB, Angonin R, Ferrand C, Decininck E, Mougin C, Cahn JY and Fest T: Relationship between expression of genes involved in cell cycle control and apoptosis in diffuse large B cell lymphoma: a preferential survivin-cyclin B link. Leukemia 16: 726-735, 2002.
54. Kawasaki C, Ohshima K, Muta H, Deyev V, Podack ER and Kikuchi M: Prognostic value of Bcl 10 rearrangement in diffuse large B-cell lymphoma. Leuk Lymphoma 43: 823-826, 2002.
55. Sakalidou A, Kanavaros P, Tzardi M and Kalmanti M: Expression of myc and ras oncogene proteins in childhood lymphomas. Anticancer Res 16: 487-492, 1996.
56. Kanavaros P, Stefanaki K, Vlachonickolis J, Rontogianni D, Antonakopoulos G, Arvanitis D, Gorgoulis V, Bai M and Agnantis NJ: Immunohistochemical expression of p53, p21, Rb, p16 and Ki67 proteins in multiple myelomas. Anticancer Res 20: 4619-4625, 2000.
57. Hans CP, Weisenburger DD, Greiner TC, Gascoyne RD, Delabie J, Ott G, Muller-Hermelink HK, Campo E, Braziel RM, Jaffe ES, Pan Z, Farihna P, Smith LM, Falini B, Banham AH, Rosenwald A, Staudt LM, Connors JM, Armitage JO and Chan WC: Confirmation of the molecular classification of diffuse large B-cell lymphoma by immunohistochemistry using a tissue microarray. Blood 103: 275-282, 2003.
58. Bai M, Vlachonikolis J, Agnantis NJ, Tsanou E, Dimou S, Nicolaides C, Stefanaki S, Pavlidis N and Kanavaros P: Low expression of p27 protein combined with altered p53 and Rb/p16 expression status is associated with increased expression of cyclin A and cyclin B1 in diffuse large B-cell lymphomas. Mod Pathol 14: 1105-1113, 2001.
59. Bai M, Tsanou E, Agnantis NJ, Dimou D, Chaidos A, Skyrlas A, Dimou S, Vlychou M, Galani V and Kanavaros P: Expression of cyclin D3 and cyclin E and identification of distinct clusters of proliferative activity and apoptosis status in diffuse large B-cell lymphomas. Histol Histopathol 18: 449-457, 2003.
60. Bai M, Agnantis NJ, Skyrlas A, Tsanou E. Kamina S, Galani V and Kanavaros P: Increased expression of the bcl6 and CD10 proteins is associated with increased apoptosis and proliferation in diffuse large B-cell lymphomas. Mod Pathol 16: 471-480, 2003.
61. Bai M, Skyrlas A, Agnantis NJ, Tsanou E, Kamina S, Galani V and Kanavaros P: Diffuse large B-cell lymphomas with germinal center B-cell-like differentiation immunophenotypic profile are associated with high apoptotic index, high expression of the pro-apoptotic proteins bax, bak and bid and low expression of the anti-apoptotic protein bcl-xl. Mod Pathol 17: 847-856, 2004.
62. Colomo L, Lopez-Guillermo A, Perales M, Rives S, Martinez A, Bosch F, Colomer D, Falini B, Montserrat E and Campo E: Clinical impact of the differentiation profile assessed by immunophenotyping in patients with diffuse large B-cell lymphoma. Blood 101: 78-84, 2003.
63. Leoncini L, Cossu A, Megha T, Bellan C, Lazzi S, Luzi P, Tosi P, Barbini P, Cevenini G, Pileri S, Giordano A, Kraft R, Laissue JA and Cottier H: Expression of p34 (cdc2) and cyclins A and B compared to other proliferative features of non-Hodgkin's lymphomas: a multivariate cluster analysis. Int J Cancer 83: 203-209, 1999.
64. Leoncini L, Del Vecchio MT, Megha T, Barbini P, Galieni P, Pileri S, Sabattini E, Gherlinzoni F, Tosi P and Kraft R: Correlation between apoptotic and proliferative indices in malignant non-Hodgkin's lymphomas. Am J Pathol 142: 755-763, 1993.
65. Du M, Singh N, Hussein A, Isaacson PG and Pan LX: Positive correlation between apoptotic and proliferative indices in gastrointestinal lymphoma of mucosa-associated lymphoid tissue. J Pathol 178: 379-384, 1996.
66. Soini Y, Raunio H and Paakko P: High-grade malignant non-Hodgkin's lymphomas differ from low-grade lymphomas in the extent of apoptosis and their expression of bcl-2, mcl-1, bax and p53. Tumour Biol 19: 176-185, 1998.
67. Soini Y and Paakko P: Apoptosis and expression of caspases 3, 6 and 8 in malignant non-Hodgkin's lymphomas. APMIS 107: 1043-1050, 1999.
68. Donoghue S, Baden HS, Lauder I, Sobolewski S and Pringle JH: Immunohistochemical localization of caspase-3 correlates with clinical outcome in B-cell diffuse large cell lymphoma. Cancer Res 59: 5386-5391, 1999.
69. Tominaga K, Yamaguchi N, Nozawa Y, Abe M and Wakasa H: Proliferation in non-Hodgkin's lymphomas as determined by immunohistochemical double staining for Ki-67. Hematol Oncol 10: 163-169, 1992.
70. Miller TP, Crogan TM, Dahlberg S, Spier CM, Braziel RM, Banks PM, Foucar K, Kjeldsberg CR, Levy N, Nathwani BN, Schnitzer B, Tubbs RR, Gaynor ER and Fisher RI: Prognostic significance of the Ki-67 associated proliferative antigen in aggressive non-Hodgkin's lymphomas: a prospective Southwest Oncology Group trial. Blood 83: 1460-1466, 1994.
71. Sanchez E, Chacon I, Plaza MM, Munoz E, Cruz B, Martinez B, Lopez L, Martinez-Montero JC, Orradre JL, Saez AI, Garcia JF and Piris M: Clinical outcome in diffuse large B-cell lymphoma is dependent on the relationship between different cell-cycle regulator proteins. J Clin Oncol 16: 1931-1939, 1998.
72. Spina D, Leoncini L, Del Vecchio MT, Megha T, Minacci C, Poggi SA, Pileri S, Tosi P, Kraft R, Laissue JA and Cottier H: Low versus high cell turnover in diffusely growing non-Hodgkin's lymphomas. J Pathol 177: 335-341, 1995.
73. Wolowiec D, Berger F, Ffrench P, Bryon PA and Ffrench M: CDK1 and cyclin A expression is linked to cell proliferation and associated with prognosis in non-Hodgkin's lymphomas. Leuk Lymphoma 35: 147-157, 1999.
74. Mullauer L, Mosberger I and Chott A: Fas ligand expression in non-Hodgkin's lymphomas. Mod Pathol 11: 369-375, 1998.
75. Dales JP, Plumas J, Palmerini F, Devilard E, Defrance T, Lajmanovich A, Pradel V, Birg F and Xerri L: Correlation between apoptosis microarray gene expression profiling and histopathological lymph node lesions. J Clin Pathol (Mol Pathol) 54: M17-M23, 2001.
76. Staudt LM: Gene expression physiology and pathophysiology of the immune system. Trends Immunol 22: 35-40, 2001.
77. Ramaswamy S and Golub TR: DNA microarrays in clinical oncology J Clin Oncol 20: 1932-1941, 2002.
78. Davis RE, Brown KD, Siebenlist U and Staudt LM: Constitutive nuclear factor KappaB activity is required for survival of activated B cell-like diffuse large B cell lymphoma cells. J Exp Med 194: 1861-1874, 2001.
79. Alizadeh AA, Eisen MB, Davis RE, Ma C, Lossos IS, Rosenwald A, Boldrick JC, Sabet H, Tran T, Yu X, Powell JI, Yang L, Marti GE, Moore T, Hudson J, Lu L, Lewis DB, Tibshirani R, Sherlock G, Chan WC, Greiner TC, Weisenburger DD, Armitage JD, Warnke R, Levy R, Wilson W, Grever MR, Byrd JC, Botstein D, Brown PO and Staudt LM: Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature 403: 503-511, 2000.
80. Rosenwald A, Wright G, Chan WC, Connors JM, Campo E, Fischer RI, Gascoyne RD, Muller-Hermelink HK, Smeland EB, Giltnane JM, Hurt EM, Zhao H, Averett L, Yang L, Wilson WH, Jaffe ES, Simon R, Klausner RD, Powell J, Duffey PL, Longo DL, Greiner TC, Weisenburger DD, Sanger WG, Dave BJ, Lynch JC, Vose J, Armitage JO, Montserrat E, Lopez-Guillermo A, Grogan TM, Miller TP, LeBlanc M, Ott G, Kvaloy S, Delabie J, Holte H, Krajci P, Stokke T and Staudt LM: The use of molecular profiling to predict survival after chemotherapy for diffuse large B-cell lymphoma. N Engl J Med 346: 1937-1947, 2002.
81. Wright G, Tan B, Rosenwald A, Hurt EH, Wiestner A and Staudt LM: A gene expression-based method to diagnose clinically distinct subgroups of diffuse large B-cell lymphoma. Proc Natl Acad Sci USA 19: 9991-9996, 2003.
82. Shipp MA, Ross KN, Tamayo P, Weng AP, Kutok JL, Aguiar RC, Gaasenbeek M, Angelo M, Reich M, Pinkus GS, Ray TS, Koval MA, Last KW, Norton A, Lister TA, Mesirov J, Neuberg DS, Lander ES, Aster JC and Golub TR: Diffuse large B-cell lymphoma outcome prediction by gene-expression profiling and supervised machine learning. Nat Med 8: 68-74, 2002.
83. Lossos IS, Alizadeh AA, Eisen MB, Chan WC, Brown PO, Botstein D, Staudt LM and Levy R: Ongoing immunoglobulin somatic mutation in germinal center B cell-like but not in activated B cell-like diffuse large B cell lymphoma. Proc Natl Acad Sci USA 97: 10290-10213, 2000.
84. De Leval L, Braaten KM, Ancukiewicz M, Kiggundu E, Mankin HJ and Harris NL: Diffuse large B-cell lymphoma of bone: an analysis of differentiation- associated antigens with clinical correlation. Am J Surg Pathol 27: 1269-1277, 2003.
85. Tzankov A, Pehrs AC, Zimpfer A, Ascani S, Lugli A, Pileri S and Dirnhofer S: Prognostic significance of CD44 expression in diffuse large B cell lymphoma of activated and germinal center B cell-like types: a tissue microarray analysis of 90 cases. J Clin Pathol 56: 747-752, 2003.
86. Chiu KC, Fine M, Ikle D, Slovak ML and Arber DA: Telomerase activity and proliferation index in aggressive mature B-cell lymphoma: comparison to germinal center phenotypic markers. Hum Pathol 34: 1259-1264, 2003.
87. Ponzoni M, Ferreri AJ, Pruneri G, Pozzi B, Dell'Oro S, Pigni A, Pinotti G, Villa E, Freschi M, Viale G and Capella C: Prognostic value of bcl-6, CD10 and CD38 immunoreactivity in stage I-II gastric lymphomas: identification of a subset of CD10+ large B-cell lymphomas with a favorable outcome. Int J Cancer 106: 288-291, 2003.
88. Zhang H, Okada S, Hatano M, Okabe S and Tokuhisa T: A new functional domain of Bcl6 family that recruits histone deacetylases. Biochim Biophys Acta 1540: 188-200, 2001.
89. Albagli O, Lantoine D, Quief S, Quignon F, Englert C, Kerckaert JP, Montarras D, Pinset C and Lindon C: Overexpressed BCL6 (LAZ3) oncoprotein triggers apoptosis, delays S phase progression and associates with replication foci. Oncogene 18: 5063-5075, 1999.
90. Yamochi T, Kaneita Y, Akiyama T, Mori S and Moriyama M: Adenovirus-mediated high expression of BCL-6 in CV-1 cells induces apoptotic cell death accompanied by down-regulation of BCL-2 and BCL-X (L). Oncogene 18: 487-494, 1999.
91. Tang TTL, Dowbenko D, Jackson A, Toney L, Lewin DA, Dent AL and Lasky LA: The forkhead transcription factor AFX activates apoptosis by induction of the bcl6 transcriptional repressor. J Biol Chem 277: 14255-14265, 2002.
92. Shaffer AL, Yu X, Boldrick J, Chan EP and Staudt LM: BCL-6 represses genes that function in lymphocyte differentiation, inflammation and cell cycle control. Immunity 13: 199-212, 2000.
93. Hosokawa Y, Maeda Y and Seto M: Target genes downregulated by the BCL-6/LAZ3 oncoprotein in mouse Ba/F3 cells. Biochem Biophys Res Commun 283: 563-568, 2001.
94. Shvarts A, Brummelkamp RT, Scheeren F, Koh E, Daley QG, Spits H and Bernards R: A senescence rescue screen identifies BCL6 as an inhibitor of anti-proliferative p19ARF-p53 signaling. Genes Develop 16: 681-686, 2002.
95. Kumagai T, Miki T, Kikuchi M, Fukuda T, Miyasaka N, Kamiyama R and Hirosawa S: The proto-oncogene bcl6 inhibits apoptotic cell death in differentiation-induced mouse myogenic cells. Oncogene 18: 467-75, 1999.
96. Kojima S, Hatano M, Okada S, Fukuda T, Toyama Y, Yuasa S, Ito H and Tokuhisa T: Testicular germ cell apoptosis in bcl6-deficient mice. Development 128: 57-65, 2001.
97. Baron BW, Anastasi J, Thirman JM, Furukawa Y, Fears S, Kim CD, Simone F, Birkenbach M, Montag A, Sadhu A, Zeleznic-Le N and McKeithan WT: The human programmed cell death-2 (PDCD2) gene is a target of BCL6 repression: implication for a role of BCL6 in the down-regulation of apoptosis. Proc Natl Acad Sci USA 99: 2860-2865, 2002.
98. Kurosu T, Fukuda T, Miki T and Miura O: BCL6 overexpression prevents increase in reactive oxygen species and inhibits apoptosis induced by chemotherapeutic reagents in B-cell lymphoma cells. Oncogene 22: 4459-4468, 2003.
99. Allman D, Jain A, Dent A, Maile RR, Selvaggi T, Kehry MR and Staudt LM: Bcl-6 expression during B-cell activation. Blood 87: 5257-5268, 1996.
100. Cutrona G, Dono M, Pastorino S, Ulivi M, Burgio VL, Zupo S, Roncella S and Ferrarini M: The propensity to apoptosis of centrocytes and centroblasts correlates with elevated levels of intracellular myc protein. Eur J Immunol 27: 234-238, 1997.
101. Cutrona G, Leanza N, Ulivi M, Melioli G, Burgio VL, Mazzarello G, Gabutti G, Roncella S and Ferrarini M: Expression of CD10 by human T cells that undergo apoptosis both in vitro and in vivo. Blood 94: 3067-3076, 1999.
102. Cutrona G, Tasso P, Dono M, Roncella S, Ulivi M, Carpaneto E.M., Fontana V, Comis M, Morabito F, Spinelli M, Frascella E, Boffa LC, Basso G, Pistoia V and Ferrarini M: CD 10 is a marker for cycling cells with propensity to apoptosis in childhood ALL. Br J Cancer 86: 1776-1785, 2002.
103. Morabito F, Mangiola M, Rapezzi D, Zupo S, Oliva BM, Ferraris AM, Spriano M, Rossi E, Stelitano C, Callea V, Cutrona G and Ferrarini M: Expression of CD10 by B-chronic lymphocytic leukemia cells undergoing apoptosis in vivo and in vitro. Haematologica 88: 864-873, 2003.
104. Martinez-Valdez H, Guret C, de Bouteiller O, Fugier I, Banchereau J and Liu YJ: Human germinal center B cells express the apoptosis-inducing genes Fas, c-myc, p53, and Bax but not the survival gene bcl-2. J Exp Med 183: 971-977, 1996.
105. Dono M, Burgio VL, Tacchetti C, Favre A, Augliera A, Zupo S, Taborelli G, Chiorazzi N, Grossi CE and Ferrarini M: Subepithelial B cells in the human palatine tonsil. I. Morphologic, cytochemical and phenotypic characterization. Eur J Immunol 26: 2035-2041, 1996.
106. Dent AL, Shatter AL, Yu X, Allman D and Staudt LM: Control of inflammation, cytokine expression, and germinal center formation by BCL-6. Science 276: 589-592, 1997.
107. Ye BH, Cattoretti G, Shen Q, Zhang J, Hawe N, De Waard R, Leung C, Nouri-Shirazi M, Orazi A, Chaganti R, Rothman P, Stall A, Pandolfi P and Dalla-Favera R: The BCL-6 proto-oncogene controls germinal-centre formation and Th2-type inflammation. Nat Genet 16: 161-170, 1997.
108. Dent AL, Vasanwala FH and Toney L: Regulation of gene expression by the proto-oncogene BCL-6. Crit Rev Oncol Hematol 41: 1-9, 2002.
109. Lococo F, Ye BH, Lista F, Corradini P, Offit K, Knowles DM, Chaganti RSK and Dalla-Favera R: Rearrangements of the BCL6 gene in diffuse large cell non-Hodgkin's lymphoma. Blood 83: 1757-1759, 1994.
110. Otsuki T, Yano T, Clark HM, Bastard C, Kerckaert JP, Jaffe ES and Raffeld M: Analysis of LAZ3 (BCL6) status in B-cell non-Hodgkin lymphomas: results of rearrangement and gene expression studies and a mutational analysis of coding region sequences. Blood 85: 2877-2884, 1995.
111. Offit K, Louie DC, Parsa NZ, Roy P, Lo Coco F, Zelenetz A, Dalla-Favera R and Chaganti RS: Bcl6 gene rearrengement and other cytogenetic abnormalities in diffuse large cell lymphoma. Leuk Lymphoma 20: 85-89, 1995.
112. Ohno H and Fukuhara S: Significance of rearrangement of the bcl6 gene in B-cell lymphoid neoplasms. Leuk Lymphoma 27: 53-63, 1997.
113. Kramer MH, Hermans J, Wijburg E, Philippe K, Geelen E, van Kricken JH, de Jong D, Maartense E, Schuuring E and Kluin PM: Clinical relevance of BCL2, BCL6, and MYC rearrangements in diffuse large B-cell lymphoma. Blood 92: 3152-3162, 1998.
114. Kawasaki C, Ohshima K and Suzumiya J: Rearrangements of bcl-1, bcl-2, bcl-6 and c-myc in diffuse large B-cell lymphoma. Leuk Lymphoma 42: 1099-1106, 2001.
115. Capello D, Vitolo U, Pasqualucci L, Quattrone S, Migliaretti G, Fassone L, Ariatti C, Vivenza D, Gloghini A, Pastore C, Lanza C, Nomdedeu J, Botto B, Freilone R, Buonaiuto D, Zagonel V, Gallo E, Palestro G, Saglio G, Dalla-Favera R, Carbone A and Gaidano G: Distribution and pattern of BCL-6 mutations throughout the spectrum of B-cell neoplasia. Blood 95: 651-659, 2000.
116. Go JH, Yang WI and Ree HJ: Mutational analysis of the 5'noncoding region of the BCL-6 gene in primary gastric lymphomas. Mod Pathol 14: 410-414, 2001.
117. Artiga MJ, Saez AI, Romero C, Sanchez-Beato M, Mateo MS, Navas C, Mollejo M and Piris MA: A short mutational hot spot in the first exon of BCL-6 is associated with increased BCL-6 expression and with longer overall survival in large B-cell lymphomas. Am J Pathol 160: 1371-1380, 2002.
118. Pasqualucci L, Migliazza A, Basso K, Houldsworth J, Chaganti RSK and Dalla-Favera R: Mutations of the BCL-6 proto-oncogene disrupt its negative autoregulation in diffuse large B-cell lymphoma. Blood 101: 2914-2923, 2002.
119. Larocca LM, Capello D, Rinelli A, Nori S, Antinori A, Gloghini A, Cingolani A, Mogliazza A, Saglio G, Cammileri-Broet S, Raphael M, Carbone A and Gaidano G: The molecular and phenotypic profile of primary central nervous system lymphoma identifies distinct categories of the disease and is consistent with histogenetic derivation from germinal center-related B-cells. Blood 92: 1011-1019, 1998.
120. Dunphy CH, Polski JM, Lance Evans H and Gardner LJ: Paraffin immunoreactivity of CD10, CDw75 and bcl6 in follicle center cell lymphoma. Leuk Lymphoma 41: 585-592, 2001.
121. Ree HJ, Yang WI, Kim CW, Huh J, Lee SS, Cho EY, Ko YH and Charney D: Coexpression of Bcl-6 and CD 10 in diffuse large B-cell lymphomas: significance of Bcl-6 expression patterns in identifying germinal center B-cell lymphoma. Hum Pathol 32: 954-962, 2001.
122. Arber DA and Weiss LM: CD10: a review. Appl Immunohistochem 5: 125-140, 1997.
123. Ohshima K, Kawasaki C, Muta H, Deyev V, Haraoka S, Suzumiya J, Podack ER and Kikuchi M: CD10 and Bcl10 expression in diffuse large B-cell lymphoma: CD10 is a marker of improved prognosis. Histopathology 39: 156-162, 2002.
124. Xu Y, McKenna RW and Kroft SH: Comparison of multiparameter flow cytometry with cluster analysis and immunohistochemistry for the detection of CD 10 in diffuse large B-cell lymphomas. Mod Pathol 15: 413-419, 2002.
125. Falini B, Fizzoti M, Pucciarini A, Bigerna B, Marafioti T, Gambacorta M, Pacini R, Alunni C, Natali-Tanci L, Ugolini B, Sebastiani C, Cattoreti G, Pileri S, Dallla-Favera R and Stein H: A monoclonal antibody (MUM1p) detects expression of the MUM1/IRF-4 protein in a subset of germinal center B-cells, plasma cells and activated T-cells. Blood 95: 2084-2092, 2000.
126. Tsuboi K, Iida S, Inagaki H, Kato M, Hayami Y, Hanamura I, Miura K, Harada S, Kikuchi M, Komatsu H, Banno S, Wakita A, Nakamura S, Eimoto T and Ueda R: MUM1/IRF4 expression as a frequent event in mature lymphoid malignancies. Leukemia 14: 449-456, 2000.
127. Natkunam Y, Warnke RA, Montgomery K, Falini B and van De Rijn M: Analysis of MUM1/IRF4 protein expression using tissue microarray and immunohistochemistry. Mod Pathol 14: 686-694, 2001.
128. Grumont RJ and Gerondakis S: Rel induces interferon regulatory factor 4 (IRF-4) expression in lymphocytes: modulation of interferon-regulated gene expression by rel/nuclear factor kappaB. J Exp Med 191: 1281-1292, 2000.
129. Dhodapkar MV and Sanderson RD: Syndecan-1 (CD138) in myeloma and lymphoid malignancies: a multifunctional regulator of cell behavior within the tumor microenvironment. Leuk Lymphoma 34: 35-43, 1999.
130. Carbone A, Gloghini A, Larocca M. L, Capello D, Pierconti F, Canzonieri V, Tirelli U, Dalla-Favera R and Gaidano G: Expression profile of MUM1/IRF4, BCL-6, and CD138/syndecan-1 defines novel histogenetic subsets of human immunodeficiency virus-related lymphomas. Blood 97: 744-751, 2001.
131. Braaten KM, Betensky RA, de Leval L, Okada Y, Hochberg FH, Louis DN, Harris NL and Batchelor TT: BCL-6 expression predicts improved survival in patients with primary central nervous system lymphoma. Clin Cancer Res 9: 1063-1069, 2003.
132. Losses IS, Jones CD, Warnke R, Natkunam Y, Kaizer H, Zehnder JL, Tibshirani R and Levy R: Expression of a single gene BCL-6, strongly predicts survival in patients with diffuse large B-cell lymphoma. Blood 98: 945-951, 2001.
133. de Leval L, Braaten KM, Ancukiewicz M, Kiggundu E, Delaney T, Mankin HJ and Harris NL: Diffuse large B-cell lymphoma of bone: an analysis of differentiation-associated antigens with clinical correlation. Am J Surg Pathol 27: 1269-1277, 2003.
134. Paulli M, Viglio A, Vivenza D, Capello d, Rossi D, Riboni R, Lucioni M, Incardona P, Boveri E, Bellosta M, Borroni G, Lazzarino M, Berti E, Alessi E, Magrini U and Gaidano G: Primary cutaneous large B-cell lymphoma of the leg: histogenetic analysis of a controversial clinicopathologic entity. Hum Pathol 33: 937-943, 2002.
135. Kwon MS, Go JH, Choi JS, Lee SS, Ko YH, Rhee JC and Ree HJ: Critical evaluation of the Bcl-6 expression in diffuse large B-cell lymphoma of the stomach and small intestine. Am J Surg Pathol 27: 790-798, 2003.
136. Ree HJ, Ohsima K, Aozasa K, Takeuchi K, Kim CW, Yang WI, Huh JY, Lee SS, Ko YH, Kwon MS, Cho EY, Choi YL, Kikuchi M and Moris S: Detection of germinal center B-cell lymphoma in archival specimens: critical evaluation of Bcl-6 protein expression in diffuse large B-cell lymphoma of the tonsil. Hum Pathol 34: 730-736, 2003.
137. Linderoth J, Jerkeman M, Cavallin-Stahl E, Kvaloy S and Torlakovic E: Nordic Lymphoma Group Study. Immunohistochemical expression of CD23 and CD40 may identify prognostically favorable subgroups of diffuse large B-cell lymphoma: a Nordic Lymphoma Group Study. Clin Cancer Res 9: 722-728, 2003.
138. Houldsworth J, Olshen AB, Cattoretti G, Donnelly GB, Teruya-Feldstein J, Qin J, Palanisamy N, Shen Y, Dyomina K, Petlakh M, Pan Q, Zelenetz AD, Dalla-Favera R and Chaganti RS: Relationship between REL amplification, REL function and clinical and biologic features in diffuse large B-cell lymphomas. Blood 103: 1862-1868, 2003.
139. Kanavaros P, Gaulard Ph, Charlotte F, Martin N, Ducos C, Lebezu M and Mason DY: Discordant expression of immunoglobulin and its associated MB-1/CD79a molecule is frequently found in mediastinal large B-cell lymphomas. Am J Pathol 146: 735-741, 1995.
140. De Leval L, Ferry JA, Falini B, Shipp M and Harris NL: Expression of bcl-6 and CD 10 in primary mediastinal large B-cell lymphomas: evidence from derivation from germinal center B cells. Am J Surg Pathol 25: 1277-1282, 2001.
141. Copie-Bergman C, Plonquet A, Alonso MA, Boulland ML, Marquet J, Divine M, Moller P, Leroy K and Gaulard P: MAL expression in lymphoid cells: further evidence for MAL as a distinct molecular marker of primary mediastinal large B-cell lymphomas. Mod Pathol 15: 1172-1180, 2002.
142. Pileri SA, Gaidano G, Zinzani PL, Falini B, Gaulard P, Zucca E, Pieri F, Berra E, Sabattini E, Ascani S, Piccioli M, Johnson PW, Giardini R, Pescarmona E, Novero D, Piccaluga PP, Marafioti T, Alonso MA and Cavalli F: Primary mediastinal B-cell lymphoma: high frequency of BCL-6 mutations and consistent expression of the transcription factors OCT-2, BOB.1, and PU.1 in the absence of immunoglobulins. Am J Pathol 762: 243-253, 2003.
143. Rosenwald A, Wright G, Leroy K, Yu X, Gaulard P, Gascoyne RD, Chan WC, Zhao T, Haioun C, Greiner TC, Weisinburger DD, Lynch JC, Vose J, Armitage JO, Smeland EB, Kvaloy S, Holte H, Delabie J, Campo E, Montserrat E, Lopez-Guillermo A, Ott G, Muller-Hermelink HK, Connors JM, Braziel R, Grogan TM, Fisher RI, Miller TP, LeBlanc M, Chiorazzi M, Zhao H, Yang L, Powell J, Wilson WH, Jaffe ES, Simon R, Klausner RD and Staudt LM: Molecular diagnosis of primary mediastinal B cell lymphoma identifies a clinically favorable subgroup of diffuse large B cell lymphoma related to Hodgkin lymphoma. J Exp Med 198: 851-862, 2003.
144. Savage KJ, Monti S, Kutok JL, Cattoretti G, Neuberg D, De Levai L, Kurtin P, Dal Cin P, Ladd C, Feuerhake F, Aguiar RC, Li S, Salles G, Berger F, Jing W, Pinkus GS, Habermann T, Dalla-Favera R, Harris NL, Aster JC, Golub TR and Shipp MA: The molecular signature of mediastinal large B-cell lymphoma differs from that of other diffuse large B-cell lymphomas and shares features with classical Hodgkin lymphomas. Blood 702: 3871-3879, 2003.
145. Chang CC, McClintock S, Cleveland RP, Trzpuc T, Vesole DH, Logan B, Kajdacsy-Balla A and Perkins SL: Immunohistochemical expression patterns of germinal center and activation B-cell markers correlate with prognosis in diffuse large B-cell lymphoma. Am J Surg Pathol 28: 464-470, 2004.
146. Niu H: The proto-oncogene BCL-6 in normal and malignant B cell development. Hematol Oncol 20: 155-166, 2002.
147. Sherr CJ: The Pezcoller lecture: cancer cell cycles revisited. Cancer Res 60: 3689-3695, 2000.
148. Malumbres M and Barbacid M: To cycle or not to cycle: a critical decision in cancer. Nat Rev Cancer 1: 222-231, 2001.
149. Evan GI and Vousden KH: Proliferation, cell cycle and apoptosis in cancer. Nature 411: 342-348, 2001.
150. Rossi D and Gaidano G: Messengers of cell death: apoptotic signaling in health and disease. Haematologica 88: 212-218, 2003.
151. Igney FH and Krammer PH: Death and anti-death: tumour resistance to apoptosis. Nat Rev Cancer 2: 277-288, 2002.
152. Opferman JT and Korsmeyer SJ: Apoptosis in the development and maintenance of the immune system. Nat Immunol 4: 410-415, 2003.
153. Baldwin AS: The transcription factor NF-kB and human disease. J Clin Invest 107: 3-6, 2001.
154. Karin M, Cao Y, Greten FR and Li ZW: NF-kB in cancer. From innocent bystander to major culprit. Nat Rev Cancer 2: 301-310, 2002.
155. Karin M and Lin A: NF-kappa B at the crossroads of life and death. Nat Immunol 3: 221-227, 2002.
156. Harada S, Suzuki R, Uehira K, Yatabe Y, Kagami Y, Ogura M, Suzuki H, Oyama A,Kodera Y, Ueda R, Morishima Y, Nakamura S and Seto M: Molecular and immunological dissection of diffuse large B cell lymphoma: CD5+, and CD5- with CD10+ groups may constitute clinically relevant subtypes. Leukemia 13: 1441-1447, 1999.
157. Yamaguchi M, Seto M, Okamoto M, Ichinohasama R, Nakamura N, Yoshino T, Suzumiya J, Murase T, Miura I, Akasaka T, Tamaru J, Suzuki R, Kagami Y, Hirano M, Morishima Y, Ueda R, Shiku H and Nakamura S: De novo CD5+ diffuse large B-cell lymphoma: a clinicopathologic study of 109 patients. Blood 99: 815-821, 2002.
158. Katzenberger T, Lohr A, Schwarz S, Dreyling M, Schoof J, Nickenig C, Stilgenbauer S, Kalla J, Ott MM, Muller-Hermelink HK and Ott G: Genetic analysis of de novo CD5+ diffuse large B-cell lymphomas suggests an origin from a somatically mutated CD5+ progenitor B cell. Blood 101: 699-702, 2003.
159. Salles G, Zain M, Jiang WM, Boussiotis VA and Shipp MA: Alternatively spliced CD44 transcripts in diffuse large-cell lymphomas: characterization and comparison with normal activated B cells and epithelial malignancies. Blood 82: 3539-3547, 1993.
160. Stauder R, Eisterer W, Thaler J and Gunthert U: CD44 variant isoforms in non-Hodgkin's lymphoma: a new independent prognostic factor. Blood 85: 2885-2899, 1995.
161. Drillenburg P, Wielenga VJ, Kramer MH, van Krieken JH, Kluin-Nelemans HC, Hermans J, Heisterkamp S, Noordijk EM, Kluin PM and Pals ST: CD44 expression predicts disease outcome in localized large B cell lymphoma. Leukemia 13: 1448-1455, 1999.
162. Inagaki H, Banno S, Wakita A, Ueda R and Eimoto T: Prognostic significance of CD44v6 in diffuse large B-cell lymphoma. Mod Pathol 12: 546-552, 1999.
163. Drillenburg P and Pals ST: Cell adhesion molecules in lymphoma dissemination. Blood 95: 1900-1910, 2000.