MDM2 inhibitor nutlin-3a induces apoptosis and senescence in cutaneous T-cell lymphoma: Role of p53

Journal of Investigative Dermatology

Volumn 132, Issue 5, 2012, Pages 1487-1496

  Manfé, Valentina ^a   Biskup, Edyta ^a   Johansen, Peter ^b   Kamstrup, Maria R ^a   Krejsgaard, Thorbjørn F ^c   Morling, Niels ^b   Wulf, Hans C ^a   Gniadecki, Robert ^a,b  

^a BISPEBJERG HOSPITAL   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; NUTLIN 3; PROTEIN MDM2; PROTEIN P53; SMALL INTERFERING RNA;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL AGING; CELL CYCLE G1 PHASE; CONTROLLED STUDY; CUTANEOUS T CELL LYMPHOMA; DRUG TARGETING; HOMOZYGOSITY; HUMAN; HUMAN CELL; MISSENSE MUTATION; NONSENSE MUTATION; PRIORITY JOURNAL; PROTEIN DETERMINATION;

EID: 84859782521     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1038/jid.2012.10     Document Type: Article

References (64)

1. Agar NS, Wedgeworth E, Crichton S et al. (2010) Survival outcomes and prognostic factors in mycosis fungoides/Sezary syndrome: validation of the revised International Society for Cutaneous Lymphomas/European Organisation for Research and Treatment of Cancer staging proposal. J Clin Oncol 28:4730-9
2. Ambrosini G, Sambol EB, Carvajal D et al. (2007) Mouse double minute antagonist Nutlin-3a enhances chemotherapy-induced apoptosis in cancer cells with mutant p53 by activating E2F1. Oncogene 26: 3473-3481 (Pubitemid 46816754)
3. Barbarotto E, Corallini F, Rimondi E et al. (2008) Differential effects of chemotherapeutic drugs versus the MDM-2 antagonist nutlin-3 on cell cycle progression and induction of apoptosis in SKW6.4 lymphoblastoid B-cells. J Cell Biochem 104:595-605 (Pubitemid 351671647)
4. Bossi G, Sacchi A (2007) Restoration of wild-type p53 function in human cancer: relevance for tumor therapy. Head Neck 29:272-84 (Pubitemid 46339325)
5. Brady CA, Jiang D, Mello SS et al. (2011) Distinct p53 transcriptional programs dictate acute DNA-damage responses and tumor suppression. Cell 145:571-83
6. Caelles C, Helmberg A, Karin M (1994) p53-dependent apoptosis in the absence of transcriptional activation of p53-target genes. Nature 370:220-3 (Pubitemid 24236778)
7. Carter BZ, Mak DH, Schober WD et al. (2008) Triptolide sensitizes AML cells to TRAIL-induced apoptosis via decrease of XIAP and p53-mediated increase of DR5. Blood 111:3742-50
8. Coll-Mulet L, Iglesias-Serret D, Santidrian AF et al. (2006) MDM2 antagonists activate p53 and synergize with genotoxic drugs in B-cell chronic lymphocytic leukemia cells. Blood 107:4109-14 (Pubitemid 43726820)
9. Davis TH, Morton CC, Miller-Cassman R et al. (1992) Hodgkin's disease, lymphomatoid papulosis, and cutaneous T-cell lymphoma derived from a common T-cell clone. N Engl J Med 326:1115-22
10. De la Cueva E, Garcia-Cao I, Herranz M et al. (2006) Tumorigenic activity of p21Waf1/Cip1 in thymic lymphoma. Oncogene 25:4128-32 (Pubitemid 44024876)
11. Dereure O, Levi E, Vonderheid EC et al. (2002) Infrequent Fas mutations but no Bax or p53 mutations in early mycosis fungoides: a possible mechanism for the accumulation of malignant T lymphocytes in the skin. J Invest Dermatol 118:949-56 (Pubitemid 34639172)
12. Drakos E, Atsaves V, Schlette E et al. (2009) The therapeutic potential of p53 reactivation by nutlin-3a in ALK+ anaplastic large cell lymphoma with wild-type or mutated p53. Leukemia 23:2290-9
13. Efeyan A, Ortega-Molina A, Velasco-Miguel S et al. (2007) Induction of p53-dependent senescence by the MDM2 antagonist nutlin-3a in mouse cells of fibroblast origin. Cancer Res 67:7350-7 (Pubitemid 47206565)
14. Gartel AL (2006) Is p21 an oncogene? Mol Cancer Ther 5:1385-6 (Pubitemid 44070473)
15. Gazdar AF, Carney DN, Bunn PA et al. (1980) Mitogen requirements for the in vitro propagation of cutaneous T-cell lymphomas. Blood 55:409-17 (Pubitemid 10148261)
16. Gootenberg JE, Ruscetti FW, Mier JW et al. (1981) Human cutaneous T cell lymphoma and leukemia cell lines produce and respond to T cell growth factor. J Exp Med 154:1403-18 (Pubitemid 12235188)
17. Harris SL, Levine AJ (2005) The p53 pathway: positive and negative feedback loops. Oncogene 24:2899-908 (Pubitemid 40638098)
18. Hasegawa H, Yamada Y, Iha H et al. (2009) Activation of p53 by Nutlin-3a, an antagonist of MDM2, induces apoptosis and cellular senescence in adult T-cell leukemia cells. Leukemia 23:2090-101
19. Haupt S, Haupt Y (2004) Manipulation of the tumor suppressor p53 for potentiating cancer therapy. Semin Cancer Biol 14:244-52 (Pubitemid 38824585)
20. Hu G, Zhang W, Deisseroth AB (1992) P53 gene mutations in acute myelogenous leukaemia. Br J Haematol 81:489-94
21. Jin L, Tabe Y, Kojima K et al. (2010) MDM2 antagonist Nutlin-3 enhances bortezomib-mediated mitochondrial apoptosis in TP53-mutated mantle cell lymphoma. Cancer Lett 299:161-70
22. Kaltoft K, Bisballe S, Rasmussen HF et al. (1987) A continuous T-cell line from a patient with Sezary syndrome. Arch Dermatol Res 279:293-8 (Pubitemid 17092161)
23. Kamstrup MR, Biskup E, Gniadecki R (2010a) Notch signalling in primary cutaneous CD30+ lymphoproliferative disorders: a new therapeutic approach? Br J Dermatol 163:781-8
24. Kamstrup MR, Gjerdrum LM, Biskup E et al. (2010b) Notch1 as a potential therapeutic target in cutaneous T-cell lymphoma. Blood 116:2504-12
25. Kamstrup MR, Ralfkiaer E, Skovgaard GL et al. (2008) Potential involvement of Notch1 signalling in the pathogenesis of primary cutaneous CD30-positive lymphoproliferative disorders. Br J Dermatol 158:747-53 (Pubitemid 351415731)
26. Kapur S, Menke MA, Tiemann M et al. (2001) Early mycosis fungoides: molecular analysis for its diagnosis and the absence of p53 gene mutations in cases with progression. J Dermatol Sci 26:36-45 (Pubitemid 32372653)
27. Kapur S, Tiemann M, Menke MA et al. (2005) The role of p53 and anaplastic lymphoma kinase genes in the progression of cutaneous CD30(+) lymphoproliferative diseases. Indian J Med Res 121:46-54 (Pubitemid 40305575)
28. Kojima K, Shimanuki M, Shikami M et al. (2008) The dual PI3 kinase/mTOR inhibitor PI-103 prevents p53 induction by Mdm2 inhibition but enhances p53-mediated mitochondrial apoptosis in p53 wild-type AML. Leukemia 22:1728-36
29. Kurosawa M, Okabe M, Kunieda Y et al. (1995) Analysis of the p53 gene mutations in acute myelogenous leukemia: the p53 gene mutations associated with a deletion of chromosome 17. Ann Hematol 71:83-7
30. Lau LM, Nugent JK, Zhao X et al. (2008) HDM2 antagonist Nutlin-3 disrupts p73-HDM2 binding and enhances p73 function. Oncogene 27: 997-1003 (Pubitemid 351225385)
31. Leroy K, Haioun C, Lepage E et al. (2002) p53 gene mutations are associated with poor survival in low and low-intermediate risk diffuse large B-cell lymphomas. Ann Oncol 13:1108-15
32. Long J, Parkin B, Ouillette P et al. (2010) Multiple distinct molecular mechanisms influence sensitivity and resistance to MDM2 inhibitors in adult acute myelogenous leukemia. Blood 116:71-80
33. Lozano G, Zambetti GP (2005) What have animal models taught us about the p53 pathway? J Pathol 205:206-20 (Pubitemid 40227992)
34. Manfe V, Holst LM, Rosbjerg A et al. (2010) Changes in oncomiR expression in CTCL cell lines during apoptosis induced by Notch inhibition. Leuk Res 34:e235-6
35. Mao X, Lillington D, Scarisbrick JJ et al. (2002) Molecular cytogenetic analysis of cutaneous T-cell lymphomas: identification of common genetic alterations in Sezary syndrome and mycosis fungoides. Br J Dermatol 147:464-75 (Pubitemid 35015279)
36. Marrogi AJ, Khan MA, Vonderheid EC et al. (1999) p53 tumor suppressor gene mutations in transformed cutaneous T-cell lymphoma: a study of 12 cases. J Cutan Pathol 26:369-78 (Pubitemid 29486319)
37. Martin-Caballero J, Flores JM, Garcia-Palencia P et al. (2001) Tumor susceptibility of p21(Waf1/Cip1)-deficient mice. Cancer Res 61:6234-8
38. Nardella C, Clohessy JG, Alimonti A et al. (2011) Pro-senescence therapy for cancer treatment. Nat Rev Cancer 11:503-11
39. Philipp J, Vo K, Gurley KE et al. (1999) Tumor suppression by p27Kip1 and p21Cip1 during chemically induced skin carcinogenesis. Oncogene 18:4689-98 (Pubitemid 29417744)
40. Ri M, Iida S, Ishida T et al. (2009) Bortezomib-induced apoptosis in mature T-cell lymphoma cells partially depends on upregulation of Noxa and functional repression of Mcl-1. Cancer Sci 100:341-8
41. Roninson IB (2003) Tumor cell senescence in cancer treatment. Cancer Res 63:2705-15 (Pubitemid 36667137)
42. Roninson IB, Broude EV, Chang BD (2001) If not apoptosis, then what? Treatment-induced senescence and mitotic catastrophe in tumor cells. Drug Resist Updat 4:303-13 (Pubitemid 34456384)
43. Saha MN, Micallef J, Qiu L et al. (2010) Pharmacological activation of the p53 pathway in haematological malignancies. J Clin Pathol 63:204-9
44. Secchiero P, Melloni E, di Iasio MG et al. (2009) Nutlin-3 up-regulates the expression of Notch1 in both myeloid and lymphoid leukemic cells, as part of a negative feedback antiapoptotic mechanism. Blood 113:4300-8
45. Secchiero P, Zerbinati C, di Iasio MG et al. (2007) Synergistic cytotoxic activity of recombinant TRAIL plus the non-genotoxic activator of the p53 pathway nutlin-3 in acute myeloid leukemia cells. Curr Drug Metab 8:395-403 (Pubitemid 46780067)
46. Shen H, Maki CG (2010) Persistent p21 expression after Nutlin-3a removal is associated with senescence-like arrest in 4N cells. J Biol Chem 285:23105-14
47. Steele AJ, Prentice AG, Hoffbrand AV et al. (2008) p53-mediated apoptosis of CLL cells: evidence for a transcription-independent mechanism. Blood 112:3827-34
48. Steininger A, Mobs M, Ullmann R et al. (2011) Genomic loss of the putative tumor suppressor gene E2A in human lymphoma. J Exp Med 208:1585-93
49. Vaseva AV, Marchenko ND, Moll UM (2009) The transcription-independent mitochondrial p53 program is a major contributor to nutlin-induced apoptosis in tumor cells. Cell Cycle 8:1711-9
50. Vassilev LT, Vu BT, Graves B et al. (2004) In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science 303:844-8 (Pubitemid 38174664)
51. Vermeer MH, van DR, Dijkman R et al. (2008) Novel and highly recurrent chromosomal alterations in Sezary syndrome. Cancer Res 68:2689-98 (Pubitemid 351556266)
52. Villalonga-Planells R, Coll-Mulet L, Martinez-Soler F et al. (2011) Activation of p53 by nutlin-3a induces apoptosis and cellular senescence in human glioblastoma multiforme. PLoS One 6:e18588
53. Villuendas R, Pezzella F, Gatter K et al. (1997) p21WAF1/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 (Pubitemid 27099774)
54. Vogelstein B, Lane D, Levine AJ (2000) Surfing the p53 network. Nature 408:307-10
55. Voltan R, Celeghini C, Melloni E et al. (2010) Perifosine plus nutlin-3 combination shows a synergistic anti-leukaemic activity. Br J Haematol 148:957-61
56. Vousden KH, Prives C (2009) Blinded by the light: the growing complexity of p53. Cell 137:413-31
57. Wada M, Bartram CR, Nakamura H et al. (1993) Analysis of p53 mutations in a large series of lymphoid hematologic malignancies of childhood. Blood 82:3163-9 (Pubitemid 23334946)
58. Wickremasinghe RG, Prentice AG, Steele AJ (2011) p53 and Notch signaling in chronic lymphocytic leukemia: clues to identifying novel therapeutic strategies. Leukemia 25:1400-7
59. Willemze R, Jaffe ES, Burg G et al. (2005) WHO-EORTC classification for cutaneous lymphomas. Blood 105:3768-85 (Pubitemid 40656118)
60. Wojcik I, Szybka M, Golanska E et al. (2005) Abnormalities of the P53, MDM2, BCL2 and BAX genes in acute leukemias. Neoplasma 52: 318-324 (Pubitemid 41076200)
61. Wollina U, Dummer R, Brockmeyer NH et al. (2003) Multicenter study of pegylated liposomal doxorubicin in patients with cutaneous T-cell lymphoma. Cancer 98:993-1001 (Pubitemid 37022100)
62. Wong KB, DeDecker BS, Freund SM et al. (1999) Hot-spot mutants of p53 core domain evince characteristic local structural changes. Proc Natl Acad Sci USA 96:8438-42 (Pubitemid 29354809)
63. Zhu N, Gu L, Li F et al. (2008) Inhibition of the Akt/survivin pathway synergizes the antileukemia effect of nutlin-3 in acute lymphoblastic leukemia cells. Mol Cancer Ther 7:1101-9
64. Zinzani PL, Baliva G, Magagnoli M et al. (2000) Gemcitabine treatment in pretreated cutaneous T-cell lymphoma: experience in 44 patients. J Clin Oncol 18:2603-6 (Pubitemid 30432527)