Diffuse large B-cell lymphoma with combined TP53 mutation and MIR34A methylation: Another "double hit" lymphoma with very poor outcome?

Oncotarget

Volumn 5, Issue 7, 2014, Pages 1912-1925

  Asmar, Fazila ^a   Hother, Christoffer ^a   Kulosman, Gorjan ^a   Treppendahl, Marianne Bach ^a   Nielsen, Helene Myrtue ^a   Ralfkiaer, Ulrik ^a   Pedersen, Anja ^a   Møller, Michael Boe ^b   Ralfkiaer, Elisabeth ^a   De Nully Brown, Peter ^a   Grønbæk, Kirsten ^a  

^a Rigshospitalet   (Denmark)

^b ODENSE UNIVERSITY HOSPITAL   (Denmark)

Author keywords

DNA methylation; Epigenetic changes; microRNA; non Hodgkin lymphoma; Tumor suppressors

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; CD19 ANTIGEN; HISTONE H3; MICRORNA; MICRORNA 34A; MICRORNA 3B; MICRORNA 3C; PROTEIN MDM2; RITUXIMAB; UNCLASSIFIED DRUG; MIRN34 MICRORNA, HUMAN; PROTEIN P53; STOP CODON;

ADULT; ARTICLE; B LYMPHOCYTE; CANCER PROGNOSIS; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GENE MUTATION; GENOTYPE; HISTONE METHYLATION; HUMAN; LARGE CELL LYMPHOMA; LYMPHOMA CELL; MAJOR CLINICAL STUDY; MALE; MIR34A GENE; OVERALL SURVIVAL; PROMOTER REGION; SINGLE NUCLEOTIDE POLYMORPHISM; TUMOR SUPPRESSOR GENE; UPREGULATION; AGED; CHEMISTRY; GENETICS; LYMPH NODE; LYMPHOMA, LARGE B-CELL, DIFFUSE; METABOLISM; METHYLATION; MIDDLE AGED; MISSENSE MUTATION; PROGNOSIS; STOP CODON; SURVIVAL RATE; TUMOR CELL LINE;

AGED; ANTIGENS, CD19; B-LYMPHOCYTES; CELL LINE, TUMOR; CODON, NONSENSE; FEMALE; HUMANS; LYMPH NODES; LYMPHOMA, LARGE B-CELL, DIFFUSE; MALE; METHYLATION; MICRORNAS; MIDDLE AGED; MUTATION, MISSENSE; PROGNOSIS; PROMOTER REGIONS, GENETIC; SURVIVAL RATE; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84899027600     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.1877     Document Type: Article

References (62)

1. 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, et al.: Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature 2000; 403: 503-511.
2. Hans CP, Weisenburger DD, Greiner TC, Gascoyne RD, Delabie J, Ott G, Müller-Hermelink HK, Campo E, Braziel RM, Jaffe ES, Pan Z, Farinha P, Smith LM, Falini B, Banham AH, Rosenwald A, et al.: Confirmation of the molecular classification of diffuse large B-cell lymphoma by immunohistochemistry using a tissue microarray. Blood 2004; 103: 275-282.
3. Grønbæ K, Brown PDN, Møller MB, Nedergaard T, Ralfkiaer E, Møller P, Zeuthen J, Guldberg P: Concurrent disruption of p16 INK4a and the ARF-p53 pathway predicts poor prognosis in aggressive non-Hodgkin' s lymphoma. Leukemia 2000; 14: 1727-1735.
4. Lenz G, Wright GW, Emre NCT, Kohlhammer H, Dave SS, Davis RE, Carty S, Lam LT, Shaffer AL, Xiao W, Powell J, Rosenwald A, Ott G, Muller-Hermelink HK, Gascoyne RD, Connors JM, et al.: Molecular subtypes of diffuse large B-cell lymphoma arise by distinct genetic pathways. Proc Natl Acad Sci U S A 2008; 105: 13520-13525.
5. Tagawa H, Suguro M, Tsuzuki S, Matsuo K, Karnan S, Ohshima K, Okamoto M, Morishima Y, Nakamura S, Seto M: Comparison of genome profiles for identification of distinct subgroups of diffuse large B-cell lymphoma. Blood 2005; 106: 1770-1777.
6. Jardin F, Jais JP, Molina TJ, Parmentier F, Picquenot JM, Ruminy P, Tilly H, Bastard C, Salles GA, Feugier P, Thieblemont C, Gisselbrecht C, de Reynies A, Coiffier B, Haioun C, Leroy K: Diffuse large B-cell lymphomas with CDKN2A deletion have a distinct gene expression signature and a poor prognosis under R-CHOP treatment: a GELA study. Blood 2010; 116: 1092-1104.
7. Johnson NA, Savage KJ, Ludkovski O, Ben-Neriah S, Woods R, Steidl C, Dyer MJS, Siebert R, Kuruvilla J, Klasa R, Connors JM, Gascoyne RD, Horsman DE: Lymphomas with concurrent BCL2 and MYC translocations: the critical factors associated with survival. Blood 2009; 114: 2273-2279.
8. Aukema SM, Siebert R, Schuuring E, van Imhoff GW, Kluin-Nelemans HC, Boerma EJ, Kluin PM: Double-hit B-cell lymphomas. Blood 2011; 117: 2319-2331.
9. Saito Y, Liang G, Egger G, Friedman JM, Chuang JC, Coetzee GA, Jones PA: Specific activation of microRNA-127 with downregulation of the proto-oncogene BCL6 by chromatin-modifying drugs in human cancer cells. Cancer Cell 2006; 9: 435-443.
10. Baer C, Claus R, Plass C: Genome-wide epigenetic regulation of miRNAs in cancer. Cancer Res 2013; 73: 473-477.
11. Choi YJ, Lin CP, Ho JJ, He X, Okada N, Bu P, Zhong Y, Kim SY, Bennett MJ, Chen C, Ozturk A, Hicks GG, Hannon GJ, He L: miR-34 miRNAs provide a barrier for somatic cell reprogramming. Nat Cell Biol 2011; 13: 1353-1360.
12. Hermeking H: The miR-34 family in cancer and apoptosis. Cell Death Differ 2010; 17: 193-9.
13. Schirmer U, Doberstein K, Rupp A, Bretz NP, Kiefel H, Breunig C, Fiegl H, Müller-holzner E, Zeillinger R, Schuster E, Zeimet AG, Sültmann H: Role of miR-34a as a suppressor of L1CAM in endometrial carcinoma. Oncotarget 2014; 5, 462-472.
14. Siemens H, Jackstadt R, Kaller M, Hermeking H: Repression of c-Kit by p53 is mediated by miR-34 and is associated with reduced chemoresistance, migration and stemness. Oncotarget 2013; 4: 1399-1415.
15. Fabbri M, Bottoni A, Shimizu M, Spizzo R, Nicoloso MS, Rossi S, Barbarotto E, Cimmino A, Adair B, Wojcik SE, Valeri N, Calore F, Sampath D, Fanini F, Vannini I, Musuraca G, et al.: Association of a microRNA/TP53 feedback circuitry with pathogenesis and outcome of B-cell chronic lymphocytic leukemia. JAMA 2011; 305: 59-67.
16. He L, He X, Lim LP, de Stanchina E, Xuan Z, Liang Y, Xue W, Zender L, Magnus J, Ridzon D, Jackson AL, Linsley PS, Chen C, Lowe SW, Cleary MA, Hannon GJ: A microRNA component of the p53 tumour suppressor network. Nature 2007; 447: 1130-1134.
17. Christoffersen NR, Shalgi R, Frankel LB, Leucci E, Lees M, Klausen M, Pilpel Y, Nielsen FC, Oren M, Lund AH: p53-independent upregulation of miR-34a during oncogene-induced senescence represses MYC. Cell Death Differ 2010; 17: 236-245.
18. Wei JS, Song YK, Durinck S, Chen QR, Cheuk a TC, Tsang P, Zhang Q, Thiele CJ, Slack A, Shohet J, Khan J: The MYCN oncogene is a direct target of miR-34a. Oncogene 2008; 27: 5204-5213.
19. Sun F, Fu H, Liu Q, Tie Y, Zhu J, Xing R, Sun Z, Zheng X: Downregulation of CCND1 and CDK6 by miR-34a induces cell cycle arrest. FEBS Lett 2008; 582: 1564-1568.
20. Asslaber D, Piñón JD, Seyfried I, Desch P, Stöcher M, Tinhofer I, Egle A, Merkel O, Greil R: microRNA-34a expression correlates with MDM2 SNP309 polymorphism and treatment-free survival in chronic lymphocytic leukemia. Blood 2010; 115: 4191-4197.
21. Craig VJ, Cogliatti SB, Imig J, Renner C, Neuenschwander S, Rehrauer H, Schlapbach R, Dirnhofer S, Tzankov A, Müller A: Myc-mediated repression of microRNA-34a promotes high-grade transformation of B-cell lymphoma by dysregulation of FoxP1. Blood 2011; 117: 6227-6236.
22. Dufour A, Palermo G, Zellmeier E, Mellert G, Duchateau-Nguyen G, Schneider S, Benthaus T, Kakadia PM, Spiekermann K, Hiddemann W, Braess J, Truong S, Patten N, Wu L, Lohmann S, Dornan D, et al. Inactivation of TP53 correlates with disease progression and low miR-34a expression in previously treated chronic lymphocytic leukemia patients. Blood 2013; 121: 3650-3657.
23. Wong KY, Huang X, Chim CS: DNA methylation of microRNA genes in multiple myeloma. Carcinogenesis 2012; 33: 1629-1638.
24. Wong KY, Yim RLH, So CC, Jin DY, Liang R, Chim CS: Epigenetic inactivation of the MIR34B/C in multiple myeloma. Blood 2011; 118: 5901-5904.
25. Zhu Y, Monni O, Franssila K, Elonen E, Vilpo J, Joensuu H, Knuutila S: Deletions at 11q23 in different lymphoma subtypes. Haematologica 2000; 85: 908-912.
26. Tagawa H, Tsuzuki S, Suzuki R, Karnan S, Ota A, Kameoka Y, Suguro M, Matsuo K, Yamaguchi M, Okamoto M, Morishima Y, Nakamura S, Seto M: Genome-wide array-based comparative genomic hybridization of diffuse large B-cell lymphoma: comparison between CD5-positive and CD5-negative cases. Cancer Res 2004; 64: 5948-5955.
27. Amini RM, Berglund M, Rosenquist R, Von Heideman A, Lagercrantz S, Thunberg U, Bergh J, Sundström C, Glimelius B, Enblad G: A novel B-cell line (U-2932) established from a patient with diffuse large B-cell lymphoma following Hodgkin lymphoma. Leuk Lymphoma 2002; 43: 2179-2189.
28. Lawrie CH, Soneji S, Marafioti T, Cooper CDO, Palazzo S, Paterson JC, Cattan H, Enver T, Mager R, Boultwood J, Wainscoat JS, Hatton CSR: MicroRNA expression distinguishes between germinal center B cell-like and activated B cell-like subtypes of diffuse large B cell lymphoma. Int J Cancer 2007; 121: 1156-1161.
29. Lawrie CH, Gal S, Dunlop HM, Pushkaran B, Liggins AP, Pulford K, Banham AH, Pezzella F, Boultwood J, Wainscoat JS, Hatton CSR, Harris AL: Detection of elevated levels of tumour-associated microRNAs in serum of patients with diffuse large B-cell lymphoma. Br J Haematol 2008; 141: 672-675.
30. Lawrie CH, Chi J, Taylor S, Tramonti D, Ballabio E, Palazzo S, Saunders NJ, Pezzella F, Boultwood J, Wainscoat JS, Hatton CSR: Expression of microRNAs in diffuse large B cell lymphoma is associated with immunophenotype, survival and transformation from follicular lymphoma. J Cell Mol Med 2009; 13: 1248-1260.
31. Pedersen IM, Otero D, Kao E, Miletic AV, Hother C, Ralfkiaer E, Rickert RC, Grønbæk K, David M: Onco-miR-155 targets SHIP1 to promote TNFalpha-dependent growth of B cell lymphomas. EMBO Mol Med 2009; 1: 288-95.
32. Costinean S, Sandhu SK, Pedersen IM, Tili E, Trotta R, Perrotti D, Ciarlariello D, Neviani P, Harb J, Kauffman LR, Shidham A, Croce CM: Src homology 2 domain-containing inositol-5-phosphatase and CCAAT enhancer-binding protein beta are targeted by miR-155 in B cells of Emicro-MiR-155 transgenic mice. Blood 2009; 114: 1374-1382.
33. Chang TC, Wentzel EA, Kent OA, Ramachandran K, Mullendore M, Lee KH, Feldmann G, Yamakuchi M, Ferlito M, Lowenstein CJ, Arking DE, Beer MA, Maitra A, Mendell JT: Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol Cell 2007; 26: 745-752.
34. Leucci E, Cocco M, Onnis A, De Falco G, van Cleef P, Bellan C, van Rijk A, Nyagol J, Byakika B, Lazzi S, Tosi P, van Krieken H, Leoncini L: MYC translocation-negative classical Burkitt lymphoma cases: an alternative pathogenetic mechanism involving miRNA deregulation. J Pathol 2008; 216: 440-450.
35. Yamakuchi M, Ferlito M, Lowenstein CJ: miR-34a repression of SIRT1 regulates apoptosis. Proc Natl Acad Sci U S A 2008; 105: 13421-13426.
36. Cannell IG, Kong YW, Johnston SJ, Chen ML, Collins HM, Dobbyn HC, Elia A, Kress TR, Dickens M, Clemens MJ, Heery DM, Gaestel M, Eilers M, Willis AE, Bushell M: p38 MAPK/MK2-mediated induction of miR-34c following DNA damage prevents Myc-dependent DNA replication. Proc Natl Acad Sci U S A 2010; 107: 5375-5380.
37. Rao DS, O'Connell RM, Chaudhuri AA, Garcia-Flores Y, Geiger TL, Baltimore D: MicroRNA-34a perturbs B lymphocyte development by repressing the forkhead box transcription factor Foxp1. Immunity 2010; 33: 48-59.
38. Craig VJ, Tzankov a, Flori M, Schmid C a, Bader a G, Müller a: Systemic microRNA-34a delivery induces apoptosis and abrogates growth of diffuse large B-cell lymphoma in vivo. Leukemia 2012; 26: 2421-2424.
39. Gal-Yam EN, Egger G, Iniguez L, Holster H, Einarsson S, Zhang X, Lin JC, Liang G, Jones PA, Tanay A: Frequent switching of Polycomb repressive marks and DNA hypermethylation in the PC3 prostate cancer cell line. Proc Natl Acad Sci U S A 2008; 105: 12979-12984.
40. Mills AA: Throwing the cancer switch: reciprocal roles of polycomb and trithorax proteins. Nat Rev Cancer 2010; 10: 669-682.
41. Asmar F, Punj V, Christensen J, Pedersen MT, Pedersen A, Nielsen AB, Hother C, Ralfkiaer U, Brown P, Ralfkiaer E, Helin K, Grønbæk K: Genome-wide profiling identifies a DNA methylation signature that associates with TET2 mutations in diffuse large B-cell lymphoma. Haematologica 2013; 98: 1912-1920.
42. Lodygin D, Tarasov V, Epanchintsev A, Berking C, Knyazeva T, Körner H, Knyazev P, Diebold J, Hermeking H: Inactivation of miR-34a by aberrant CpG methylation in multiple types of cancer. Cell Cycle 2008; 7: 2591-2600.
43. Chim CS, Wong KY, Qi Y, Loong F, Lam WL, Wong LG, Jin DY, Costello JF, Liang R: Epigenetic inactivation of the miR-34a in hematological malignancies. Carcinogenesis 2010; 31: 745-750.
44. Zainuddin N, Berglund M, Wanders A, Ren Z-P, Amini R-M, Lindell M, Kanduri M, Roos G, Rosenquist R, Enblad G: TP53 mutations predict for poor survival in de novo diffuse large B-cell lymphoma of germinal center subtype. Leuk Res 2009; 33: 60-66.
45. Bittenbring J, Parisot F, Wabo A, Mueller M, Kerschenmeyer L, Kreuz M, Truemper L, Landt O, Menzel A, Pfreundschuh M, Roemer K: MDM2 gene SNP309 T/G and p53 gene SNP72 G/C do not influence diffuse large B-cell non-Hodgkin lymphoma onset or survival in central European Caucasians. BMC Cancer 2008; 8: 116.
46. Ichikawa A, Kinoshita T, Watanabe T, Kato H, Nagai H, Tsushita K, Saito H, Hotta T: Mutations of the p53 gene as a prognostic factor in aggressive B-cell lymphoma. N Engl J Med 1997; 337: 529-534.
47. Young KH, Leroy K, Møller MB, Colleoni GWB, Sánchez-Beato M, Kerbauy FR, Haioun C, Eickhoff JC, Young AH, Gaulard P, Piris MA, Oberley TD, Rehrauer WM, Kahl BS, Malter JS, Campo E, et al.: Structural profiles of TP53 gene mutations predict clinical outcome in diffuse large B-cell lymphoma: an international collaborative study. Blood 2008; 112: 3088-3098.
48. Xu-Monette ZY, Wu L, Visco C, Tai YC, Tzankov A, Liu W, Montes-Moreno S, Dybkaer K, Chiu A, Orazi A, Zu Y, Bhagat G, Richards KL, Hsi ED, Zhao XF, Choi WWL, et al.: Mutational profile and prognostic significance of TP53 in diffuse large B-cell lymphoma patients treated with R-CHOP: report from an International DLBCL Rituximab-CHOP Consortium Program Study. Blood 2012; 120: 3986-3996.
49. Dunleavy K, Pittaluga S, Maeda LS, Advani R, Chen CC, Hessler J, Steinberg SM, Grant C, Wright G, Varma G, Staudt LM, Jaffe ES, Wilson WH: Dose-adjusted EPOCH-rituximab therapy in primary mediastinal B-cell lymphoma. N Engl J Med 2013; 368: 1408-1416.
50. Merkel O, Asslaber D, Piñón JD, Egle A, Greil R: Interdependent regulation of p53 and miR-34a in chronic lymphocytic leukemia. Cell Cycle 2010; 9: 2764-2768.
51. Van Leeuwen IMM: Cyclotherapy: opening a therapeutic window in cancer treatment. Oncotarget 2012; 3: 596-600.
52. Blagosklonny M V: Sequential activation and inactivation of G2 checkpoints for selective killing of p53-deficient cells by microtubule-active drugs. Oncogene 2002; 21: 6249-6254.
53. Rao B, van Leeuwen IMM, Higgins M, Campbel J, Thompson AM, Lane DP, Lain S: Evaluation of an Actinomycin D/VX-680 aurora kinase inhibitor combination in p53-based cyclotherapy. Oncotarget 2010; 1: 639-650.
54. Ji Q, Hao X, Meng Y, Zhang M, Desano J, Fan D, Xu L: Restoration of tumor suppressor miR-34 inhibits human p53-mutant gastric cancer tumorspheres. BMC Cancer 2008; 8: 266.
55. Wiggins JF, Ruffino L, Kelnar K, Omotola M, Patrawala L, Brown D, Bader AG: Development of a lung cancer therapeutic based on the tumor suppressor microRNA-34. Cancer Res 2010; 70: 5923-5930.
56. Zhao J, Lammers P, Torrance CJ, Bader AG: TP53-independent function of miR-34a via HDAC1 and p21(CIP1/WAF1.). Mol Ther 2013; 21: 1678-86.
57. Bader AG: miR-34-a microRNA replacement therapy is headed to the clinic. Front Genet 2012.
58. Bernardo BC, Gao X-M, Winbanks CE, Boey EJH, Tham YK, Kiriazis H, Gregorevic P, Obad S, Kauppinen S, Du X-J, Lin RCY, McMullen JR: Therapeutic inhibition of the miR-34 family attenuates pathological cardiac remodeling and improves heart function. Proc Natl Acad Sci 2012; 109: 17615-17620.
59. Guldberg P, Nedergaard T, Nielsen HJ, Olsen AC, Ahrenkiel V, Zeuthen J: Single-step DGGE-based mutation scanning of the p53 gene: application to genetic diagnosis of colorectal cancer. Hum Mutat 1997; 9: 348-355.
60. Worm J, Aggerholm A, Guldberg P: In-tube DNA methylation profiling by fluorescence melting curve analysis. Clin Chem 2001; 47: 1183-1189.
61. Toyota M, Suzuki H, Sasaki Y, Maruyama R, Imai K, Shinomura Y, Tokino T: Epigenetic silencing of microRNA-34b/c and B-cell translocation gene 4 is associated with CpG island methylation in colorectal cancer. Cancer Res 2008; 68: 4123-4132.
62. Guldberg P, Worm J, Grønbaek K: Profiling DNA methylation by melting analysis. Methods 2002; 27: 121-127.