p63 expression confers significantly better survival outcomes in highrisk diffuse large B-cell lymphoma and demonstrates p53-like and p53-independent tumor suppressor function

Aging

Volumn 8, Issue 2, 2016, Pages 345-365

  Xu Monette, Zijun Y ^a   Zhang, Shanxiang ^b   Li, Xin ^a   Manyam, Ganiraju C ^a   Wang, Xiao xiao ^a   Xia, Yi ^a   Visco, Carlo ^c   Tzankov, Alexandar ^d   Zhang, Li ^a   Montes Moreno, Santiago ^e   Dybkaer, Karen ^f   Chiu, April ^g   Orazi, Attilio ^h   Zu, Youli ⁱ   Bhagat, Govind ^j   Richards, Kristy L ^k   Hsi, Eric D ^l   Choi, William W L ^m   Van Krieken, Han J ⁿ   Huh, Jooryung ^o   Ponzoni, Maurilio ^p   Ferreri, Andrés J M ^p   Zhao, Xiaoying ^q   Møller, Michael B ^r   Parsons, Ben M ^s   Winter, Jane N ^t   Piris, Miguel A ^e   Medeiros, Jeffrey L ^a   Young, Ken H ^a,u   more..

^a UNIVERSITY OF TEXAS   (United States)

^b INDIANA UNIVERSITY   (United States)

^c SAN BORTOLO HOSPITAL   (Italy)

^d UNIVERSITY HOSPITAL BASEL   (Switzerland)

^e HOSPITAL UNIVERSITARIO MARQUÉS DE VALDECILLA   (Spain)

^f AALBORG UNIVERSITY HOSPITAL   (Denmark)

^g MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^h WEILL CORNELL MEDICAL COLLEGE   (United States)

ⁱ HOUSTON METHODIST HOSPITAL   (United States)

^j New York Presbyterian Morgan Stanley Children's Hospital   (United States)

^k UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^l LERNER RESEARCH INSTITUTE   (United States)

^m UNIVERSITY OF HONG KONG   (Hong Kong)

ⁿ RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^o University of Ulsan College of Medicine   (South Korea)

^p SAN RAFFAELE HOSPITAL   (Italy)

^q ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^r ODENSE UNIVERSITY HOSPITAL   (Denmark)

^s GUNDERSEN LUTHERAN MEDICAL CENTER   (United States)

^t NORTHWESTERN UNIVERSITY   (United States)

^u UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

more..

Author keywords

DLBCL; MDM2; P53; p63; TP53 mutation

Indexed keywords

PROTEIN P53; TP53 PROTEIN, HUMAN; TP63 PROTEIN, HUMAN; TRANSCRIPTION FACTOR; TRANSCRIPTOME; TUMOR MARKER; TUMOR SUPPRESSOR PROTEIN;

ADULT; AGED; DIFFUSE LARGE B CELL LYMPHOMA; DISEASE FREE SURVIVAL; DNA MICROARRAY; FEMALE; HUMAN; IMMUNOHISTOCHEMISTRY; KAPLAN MEIER METHOD; MALE; METABOLISM; MIDDLE AGED; MORTALITY; PROGNOSIS; TISSUE MICROARRAY;

ADULT; AGED; BIOMARKERS, TUMOR; DISEASE-FREE SURVIVAL; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; KAPLAN-MEIER ESTIMATE; LYMPHOMA, LARGE B-CELL, DIFFUSE; MALE; MIDDLE AGED; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROGNOSIS; TISSUE ARRAY ANALYSIS; TRANSCRIPTION FACTORS; TRANSCRIPTOME; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS;

EID: 84961199980     PISSN: 19454589     EISSN: None     Source Type: Journal    
DOI: 10.18632/aging.100898     Document Type: Article

References (60)

1. Su X, Chakravarti D and Flores ER. p63 steps into the limelight: crucial roles in the suppression of tumorigenesis and metastasis. Nat Rev Cancer. 2013; 13:136-143.
2. Yang A and McKeon F. P63 and P73: P53 mimics, menaces and more. Nat Rev Mol Cell Biol. 2000; 1:199-207.
3. Yang A, Kaghad M, Wang Y, Gillett E, Fleming MD, Dotsch V, Andrews NC, Caput D and McKeon F. p63, a p53 homolog at 3q27-29, encodes multiple products with transactivating, deathinducing, and dominant-negative activities. Molecular cell. 1998; 2:305-316.
4. Cho SJ, Jung YS and Chen X. Poly (C)-binding protein 1 regulates p63 expression through mRNA stability. PloS one. 2013; 8:e71724.
5. Pflaum J, Schlosser S and Muller M. p53 Family and Cellular Stress Responses in Cancer. Front Oncol. 2014; 4:285.
6. Levine AJ, Tomasini R, McKeon FD, Mak TW and Melino G. The p53 family: guardians of maternal reproduction. Nat Rev Mol Cell Biol. 2011; 12:259-265.
7. Flores ER, Tsai KY, Crowley D, Sengupta S, Yang A, McKeon F and Jacks T. p63 and p73 are required for p53-dependent apoptosis in response to DNA damage. Nature. 2002; 416:560-564.
8. Venkatanarayan A, Raulji P, Norton W, Chakravarti D, Coarfa C, Su X, Sandur SK, Ramirez MS, Lee J, Kingsley CV, Sananikone EF, Rajapakshe K, Naff K, et al. IAPP-driven metabolic re rogramming induces regression of p53-deficient tumours in vivo. Nature. 2015; 517:626-630.
9. Mills AA, Zheng B, Wang XJ, Vogel H, Roop DR and Bradley A. p63 is a p53 homologue required for limb and epidermal morphogenesis. Nature. 1999; 398:708-713.
10. Suh EK, Yang A, Kettenbach A, Bamberger C, Michaelis AH, Zhu Z, Elvin JA, Bronson RT, Crum CP and McKeon F. p63 protects the female germ line during meiotic arrest. Nature. 2006; 444:624-628.
11. Yang A, Schweitzer R, Sun D, Kaghad M, Walker N, Bronson RT, Tabin C, Sharpe A, Caput D, Crum C and McKeon F. p63 is essential for regenerative proliferation in limb, craniofacial and epithelial development. Nature. 1999; 398:714-718.
12. Sun R, Zhang Y, Lv Q, Liu B, Jin M, Zhang W, He Q, Deng M, Liu X, Li G, Li Y, Zhou G, Xie P, et al. Toll-like receptor 3 (TLR3) induces apoptosis via death receptors and mitochondria by upregulating the transactivating p63 isoform alpha (TAP63alpha). J Biol Chem. 2011; 286:15918-15928.
13. Levrero M, De Laurenzi V, Costanzo A, Gong J, Wang JY and Melino G. The p53/p63/p73 family of transcription factors: overlapping and distinct functions. J Cell Sci. 2000; 113:1661-1670.
14. Dohn M, Zhang S and Chen X. p63alpha and DeltaNp63alpha can induce cell cycle arrest and apoptosis and differentially regulate p53 target genes. Oncogene. 2001; 20:3193-3205.
15. Perez-Losada J, Wu D, DelRosario R, Balmain A and Mao JH. p63 and p73 do not contribute to p53-mediated lymphoma suppressor activity in vivo. Oncogene. 2005; 24:5521-5524.
16. Chakrabarti R, Wei Y, Hwang J, Hang X, Andres Blanco M, Choudhury A, Tiede B, Romano RA, DeCoste C, Mercatali L, Ibrahim T, Amadori D, Kannan N, et al. DeltaNp63 promotes stem cell activity in mammary gland development and basal-like breast cancer by enhancing Fzd7 expression and Wnt signalling. Nat Cell Biol. 2014; 16:1004-1015, 1001-1013.
17. Su X, Chakravarti D, Cho MS, Liu L, Gi YJ, Lin YL, Leung ML, El-Naggar A, Creighton CJ, Suraokar MB, Wistuba I and Flores ER. TAp63 suppresses metastasis through coordinate regulation of Dicer and miRNAs. Nature. 2010; 467:986-990.
18. Guo X, Keyes WM, Papazoglu C, Zuber J, Li W, Lowe SW, Vogel H and Mills AA. TAp63 induces senescence and suppresses tumorigenesis in vivo. Nat Cell Biol. 2009; 11:1451-1457.
19. Xu E, Zhang J, Zhang M, Jiang Y, Cho SJ and Chen X. RNAbinding protein RBM24 regulates p63 expression via mRNA stability. Mol Cancer Res. 2014; 12:359-369.
20. Truong AB, Kretz M, Ridky TW, Kimmel R and Khavari PA. p63 regulates proliferation and differentiation of developmentally mature keratinocytes. Genes Dev. 2006; 20:3185-3197.
21. Hedvat CV, Teruya-Feldstein J, Puig P, Capodieci P, Dudas M, Pica N, Qin J, Cordon-Cardo C and Di Como CJ. Expression of p63 in diffuse large B-cell lymphoma. Appl Immunohistochem Mol Morphol. 2005; 13:237-242.
22. Danilova N, Sakamoto KM and Lin S. p53 family in development. Mech Dev. 2008; 125:919-931.
23. Wolff S, Talos F, Palacios G, Beyer U, Dobbelstein M and Moll UM. The alpha/beta carboxy-terminal domains of p63 are required for skin and limb development. New insights from the Brdm2 mouse which is not a complete p63 knockout but expresses p63 gamma-like proteins. Cell Death Differ. 2009; 16:1108-1117.
24. Okada Y, Osada M, Kurata S, Sato S, Aisaki K, Kageyama Y, Kihara K, Ikawa Y and Katoh I. p53 gene family p51(p63)-encoded, secondary transactivator p51B(TAp63alpha) occurs without forming an immunoprecipitable complex with MDM2, but responds to genotoxic stress by accumulation. Exp Cell Res. 2002; 276:194-200.
25. Di Como CJ, Urist MJ, Babayan I, Drobnjak M, Hedvat CV, Teruya-Feldstein J, Pohar K, Hoos A and Cordon-Cardo C. p63 expression profiles in human normal and tumor tissues. Clin Cancer Res. 2002; 8:494-501.
26. Nylander K, Vojtesek B, Nenutil R, Lindgren B, Roos G, Zhanxiang W, Sjostrom B, Dahlqvist A and Coates PJ. Differential expression of p63 isoforms in normal tissues and neoplastic cells. J Pathol. 2002; 198:417-427.
27. Hallack Neto AE, Siqueira SA, Dulley FL, Ruiz MA, Chamone DA and Pereira J. p63 protein expression in high risk diffuse large B-cell lymphoma. J Clin Pathol. 2009; 62:77-79.
28. Alexandrova EM and Moll UM. Role of p53 family members p73 and p63 in human hematological malignancies. Leuk Lymphoma. 2012; 53:2116-2129.
29. Aubry MC, Roden A, Murphy SJ, Vasmatzis G, Johnson SH, Harris FR, Halling G, Knudson RA, Ketterling RP and Feldman AL. Chromosomal rearrangements and copy number abnormalities of TP63 correlate with p63 protein expression in lung adenocarcinoma. Mod Pathol. 2015; 28:359-366.
30. Geddert H, Kiel S, Heep HJ, Gabbert HE and Sarbia M. The role of p63 and deltaNp63 (p40) protein expression and gene amplification in esophageal carcinogenesis. Hum Pathol. 2003; 34:850-856.
31. Ying H, Chang DL, Zheng H, McKeon F and Xiao ZX. DNAbinding and transactivation activities are essential for TAp63 protein degradation. Mol Cell Biol. 2005; 25:6154-6164.
32. Lo Muzio L, Santarelli A, Caltabiano R, Rubini C, Pieramici T, Trevisiol L, Carinci F, Leonardi R, De Lillo A, Lanzafame S, Bufo P and Piattelli A. p63 overexpression associates with poor prognosis in head and neck squamous cell carcinoma. Hum Pathol. 2005; 36:187-194.
33. Stetsenko GY, Malekirad J, Paulson KG, Iyer JG, Thibodeau RM, Nagase K, Schmidt M, Storer BE, Argenyi ZB and Nghiem P. p63 expression in Merkel cell carcinoma predicts poorer survival yet may have limited clinical utility. Am J Clin Pathol. 2013; 140:838-844.
34. Takahashi Y, Noguchi T, Takeno S, Kimura Y, Okubo M and Kawahara K. Reduced expression of p63 has prognostic implications for patients with esophageal squamous cell carcinoma. Oncol Rep. 2006; 15:323-328.
35. 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, et al. Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature. 2000; 403:503-511.
36. Testoni M, Zucca E, Young KH and Bertoni F. Genetic lesions in diffuse large B-cell lymphomas. Ann Oncol. 2015. 26:1069-1080
37. Xu-Monette ZY, Wu L, Visco C, Tai YC, Tzankov A, Liu WM, Montes-Moreno S, Dybkaer K, Chiu A, Orazi A, Zu Y, Bhagat G, Richards KL, et al. Mutational profile and prognostic significance of TP53 in diffuse large B-cell lymphoma patients treated with RCHOP: report from an International DLBCL Rituximab-CHOP Consortium Program Study. Blood. 2012; 120:3986-3996.
38. Xu-Monette ZY, Moller MB, Tzankov A, Montes-Moreno S, Hu W, Manyam GC, Kristensen L, Fan L, Visco C, Dybkaer K, Chiu A, Tam W, Zu Y, et al. MDM2 phenotypic and genotypic profiling, respective to TP53 genetic status, in diffuse large B-cell lymphoma patients treated with rituximab-CHOP immunochemotherapy: a report from the International DLBCL Rituximab-CHOP Consortium Program. Blood. 2013; 122:2630-2640.
39. Park CK and Oh YH. Expression of p63 in reactive hyperplasias and malignant lymphomas. J Korean Med Sci. 2005; 20:752-758.
40. Vasmatzis G, Johnson SH, Knudson RA, Ketterling RP, Braggio E, Fonseca R, Viswanatha DS, Law ME, Kip NS, Ozsan N, Grebe SK, Frederick LA, Eckloff BW, et al. Genome-wide analysis reveals recurrent structural abnormalities of TP63 and other p53-related genes in peripheral T-cell lymphomas. Blood. 2012; 120:2280-2289.
41. Scott DW, Mungall KL, Ben-Neriah S, Rogic S, Morin RD, Slack GW, Tan KL, Chan FC, Lim RS, Connors JM, Marra MA, Mungall AJ, Steidl C, et al. TBL1XR1/TP63: a novel recurrent gene fusion in B-cell non-Hodgkin lymphoma. Blood. 2012; 119:4949-4952.
42. van Keimpema M, Gruneberg LJ, Mokry M, van Boxtel R, Koster J, Coffer PJ, Pals ST and Spaargaren M. FOXP1 directly represses transcription of proapoptotic genes and cooperates with NF-kappaB to promote survival of human B cells. Blood. 2014; 124:3431-3440.
43. Fukushima N, Satoh T, Sueoka N, Sato A, Ide M, Hisatomi T, Kuwahara N, Tomimasu R, Tsuneyoshi N, Funai N, Sano M, Tokunaga O and Sueoka E. Clinico-pathological characteristics of p63 expression in B-cell lymphoma. Cancer Sci. 2006; 97:1050-1055.
44. Hu S, Xu-Monette ZY, Tzankov A, Green T, Wu L, Balasubramanyam A, Liu WM, Visco C, Li Y, Miranda RN, Montes-Moreno S, Dybkaer K, Chiu A, et al. MYC/BCL2 protein coexpression contributes to the inferior survival of activated Bcell 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. 2013; 121:4021-4031; quiz 4250.
45. Zhang Y, Liao JM, Zeng SX and Lu H. p53 downregulates Down syndrome-associated DYRK1A through miR-1246. EMBO reports. 2011; 12:811-817.
46. Chen J, Xu-Monette ZY, Deng L, Shen Q, Manyam GC, Martinez-Lopez A, Zhang L, Montes-Moreno S, Visco C, Tzankov A, Yin L, Dybkaer K, Chiu A, et al. Dysregulated CXCR4 expression promotes lymphoma cell survival and independently predicts disease progression in germinal center B-cell-like diffuse large Bcell lymphoma. Oncotarget. 2015; 6:5597-5614. DOI: 10.18632/oncotarget.3343.
47. Li Y and Prives C. Are interactions with p63 and p73 involved in mutant p53 gain of oncogenic function? Oncogene. 2007; 26:2220-2225.
48. Dietz S, Rother K, Bamberger C, Schmale H, Mossner J and Engeland K. Differential regulation of transcription and induction of programmed cell death by human p53-family members p63 and p73. FEBS Lett. 2002; 525:93-99.
49. Gaiddon C, Lokshin M, Ahn J, Zhang T and Prives C. A subset of tumor-derived mutant forms of p53 down-regulate p63 and p73 through a direct interaction with the p53 core domain. Mol Cell Biol. 2001; 21:1874-1887.
50. Strano S, Fontemaggi G, Costanzo A, Rizzo MG, Monti O, Baccarini A, Del Sal G, Levrero M, Sacchi A, Oren M and Blandino G. Physical interaction with human tumor-derived p53 mutants inhibits p63 activities. J Biol Chem. 2002; 277:18817-18826.
51. Calabro V, Mansueto G, Parisi T, Vivo M, Calogero RA and La Mantia G. The human MDM2 oncoprotein increases the transcriptional activity and the protein level of the p53 homolog p63. J Biol Chem. 2002; 277:2674-2681.
52. Calabro V, Mansueto G, Santoro R, Gentilella A, Pollice A, Ghioni P, Guerrini L and La Mantia G. Inhibition of p63 transcriptional activity by p14ARF: functional and physical link between human ARF tumor suppressor and a member of the p53 family. Mol Cell Bio. 2004; 24:8529-8540.
53. Kadakia M, Slader C and Berberich SJ. Regulation of p63 function by Mdm2 and MdmX. DNA Cell Biol. 2001; 20:321-330.
54. Gonfloni S, Di Tella L, Caldarola S, Cannata SM, Klinger FG, Di Bartolomeo C, Mattei M, Candi E, De Felici M, Melino G and Cesareni G. Inhibition of the c-Abl-TAp63 pathway protects mouse oocytes from chemotherapy-induced death. Nature medicine. 2009; 15:1179-1185.
55. Visco C, Li Y, Xu-Monette ZY, Miranda RN, Green TM, Li Y, Tzankov A, Wen W, Liu WM, Kahl BS, d'Amore ES, Montes-Moreno S, Dybkaer K, et al. Comprehensive gene expression profiling and immunohistochemical studies support application of immunophenotypic algorithm for molecular subtype classification in diffuse large B-cell lymphoma: a report from the International DLBCL Rituximab-CHOP Consortium Program Study. Leukemia. 2012; 26:2103-2113.
56. Tzankov A, Xu-Monette ZY, Gerhard M, Visco C, Dirnhofer S, Gisin N, Dybkaer K, Orazi A, Bhagat G, Richards KL, Hsi ED, Choi WW, van Krieken JH, et al. Rearrangements of MYC gene facilitate risk stratification in diffuse large B-cell lymphoma patients treated with rituximab-CHOP. Mod Pathol. 2014; 27:958-971.
57. Ok CY, Chen J, Xu-Monette ZY, Tzankov A, Manyam GC, Li L, Visco C, Montes-Moreno S, Dybkaer K, Chiu A, Orazi A, Zu Y, Bhagat G, et al. Clinical Implications of Phosphorylated STAT3 Expression in De Novo Diffuse Large B-cell Lymphoma. Clin Cancer Res. 2014; 20:5113-5123.
58. Hu S, Xu-Monette ZY, Balasubramanyam A, Manyam GC, Visco C, Tzankov A, Liu WM, Miranda RN, Zhang L, Montes-Moreno S, Dybkaer K, Chiu A, Orazi A, et al. CD30 expression defines a novel subgroup of diffuse large B-cell lymphoma with favorable prognosis and distinct gene expression signature: a report from the International DLBCL Rituximab-CHOP Consortium Program Study. Blood. 2013; 121:2715-2724.
59. Visco C, Tzankov A, Xu-Monette ZY, Miranda RN, Tai YC, Li Y, Liu WM, d'Amore ES, Li Y, Montes-Moreno S, Dybkaer K, Chiu A, Orazi A, et al. 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. 2013; 98:255-263.
60. Xu-Monette ZY, Dabaja BS, Wang X, Tu M, Manyam GC, Tzankov A, Xia Y, Li Zhang, Visco C, Dybkaer K, Yin L, Chiu A, Orazi A, et al. Clinical features, tumor biology and prognosis associated with MYC rearrangement and overexpression in diffuse large B-cell lymphoma patients treated with rituximab-CHOP. Modern Pathology. 2015; 28:1555-1573.