Loss of p53 and altered miR15-a/16-1→MCL-1 pathway in CLL: Insights from TCL1-Tg:p53-/- mouse model and primary human leukemia cells

Leukemia

Volumn 28, Issue 1, 2014, Pages 118-128

  Liu, J ^a,b   Chen, G ^a   Feng, L ^a   Zhang, W ^a,c   Pelicano, H ^a   Wang, F ^a,d   Ogasawara, M A ^a,b   Lu, W ^a   Amin, H M ^a   Croce, C M ^e   Keating, M J ^a   Huang, P ^a,b,d  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSITY OF TEXAS   (United States)

^c NANCHANG UNIVERSITY   (China)

^d SUN YAT SEN UNIVERSITY CANCER CENTER   (China)

^e THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

Author keywords

drug resistance; leukemia; mouse model; p53; TCL1

Indexed keywords

CD5 ANTIGEN; CHLORAMBUCIL; FLUDARABINE; IMMUNOGLOBULIN M; MICRORNA 15A; MICRORNA 16; MICRORNA 16 1; OXALIPLATIN; PROPIDIUM IODIDE; PROTEIN; PROTEIN MCL 1; PROTEIN P17; PROTEIN P53; PROTEIN TCL 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; B CELL LEUKEMIA; B LYMPHOCYTE; CELL PROLIFERATION; CELL SURVIVAL; CHRONIC LYMPHATIC LEUKEMIA; DISEASE COURSE; DRUG SENSITIVITY; GENE EXPRESSION; GENOTYPE; HUMAN; HUMAN CELL; IN VIVO STUDY; INTRACELLULAR SIGNALING; LEUKEMIA CELL; MOUSE; NONHUMAN; PERITONEAL CAVITY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; SPLEEN; WILD TYPE;

ANIMALS; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; GENES, P53; HUMANS; MICE; MICE, TRANSGENIC; MICRORNAS; MYELOID CELL LEUKEMIA SEQUENCE 1 PROTEIN; PROTO-ONCOGENE PROTEINS;

EID: 84891849709     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2013.125     Document Type: Article

References (40)

1. Caligaris-Cappio F, Gobbi M, Bofill M, Janossy G. Infrequent normal B lymphocytes express features of B-chronic lymphocytic leukemia. J Exp Med 1982; 155: 623-628. (Pubitemid 12171305)
2. Landis SH, Murray T, Bolden S, Wingo PA. Cancer statistics, 1998. CA Cancer J Clin 1998; 48: 6-29.
3. Zenz T, Mertens D, Dohner H, Stilgenbauer S. Importance of genetics in chronic lymphocytic leukemia. Blood Rev 2011; 25: 131-137.
4. Dohner H, Stilgenbauer S, Benner A, Leupolt E, Krober A, Bullinger L et al. Genomic aberrations and survival in chronic lymphocytic leukemia. N Engl J Med 2000; 343: 1910-1916. (Pubitemid 32064784)
5. Leonard CJ, Canman CE, Kastan MB. The role of p53 in cell-cycle control and apoptosis: implications for cancer. Important Adv Oncol 1995; 33-42.
6. Zenz T, Krober A, Scherer K, Habe S, Buhler A, Benner A et al. Monoallelic TP53 inactivation is associated with poor prognosis in chronic lymphocytic leukemia: results from a detailed genetic characterization with long-term follow-up. Blood 2008; 112: 3322-3329.
7. Zenz T, Frohling S, Mertens D, Dohner H, Stilgenbauer S. Moving from prognostic to predictive factors in chronic lymphocytic leukaemia (CLL). Best Pract Res Clin Haematol 2010; 23: 71-84.
8. Gonzalez D, Martinez P, Wade R, Hockley S, Oscier D, Matutes E et al. Mutational status of the TP53 gene as a predictor of response and survival in patients with chronic lymphocytic leukemia: results from the LRF CLL4 trial. J Clin Oncol 2011; 29: 2223-2229.
9. de Viron E, Michaux L, Put N, Bontemps F, van den Neste E. Present status and perspectives in functional analysis of p53 in chronic lymphocytic leukemia. Leuk Lymphoma 2012; 53: 1445-1451.
10. Bichi R, Shinton SA, Martin ES, Koval A, Calin GA, Cesari R et al. Human chronic lymphocytic leukemia modeled in mouse by targeted TCL1 expression. Proc Natl Acad Sci USA 2002; 99: 6955-6960. (Pubitemid 34526239)
11. Planelles L, Carvalho-Pinto CE, Hardenberg G, Smaniotto S, Savino W, Gomez-Caro R et al. APRIL promotes B-1 cell-associated neoplasm. Cancer Cell 2004; 6: 399-408. (Pubitemid 39361440)
12. Zapata JM, Krajewska M, Morse 3rd HC, Choi Y, Reed JC. TNF receptor-associated factor (TRAF) domain and Bcl-2 cooperate to induce small B cell lymphoma/chronic lymphocytic leukemia in transgenic mice. Proc Natl Acad Sci USA 2004; 101: 16600-16605. (Pubitemid 39557759)
13. Costinean S, Zanesi N, Pekarsky Y, Tili E, Volinia S, Heerema N et al. Pre-B cell proliferation and lymphoblastic leukemia/high-grade lymphoma in E(mu)-miR155 transgenic mice. Proc Natl Acad Sci USA 2006; 103: 7024-7029.
14. Raveche ES, Salerno E, Scaglione BJ, Manohar V, Abbasi F, Lin YC et al. Abnormal microRNA-16 locus with synteny to human 13q14 linked to CLL in NZB mice. Blood 2007; 109: 5079-5086. (Pubitemid 46890521)
15. Santanam U, Zanesi N, Efanov A, Costinean S, Palamarchuk A, Hagan JP et al. Chronic lymphocytic leukemia modeled in mouse by targeted miR-29 expression. Proc Natl Acad Sci USA 2010; 107: 12210-12215.
16. Robertson LE, Plunkett W, McConnell K, Keating MJ, McDonnell TJ. Bcl-2 expression in chronic lymphocytic leukemia and its correlation with the induction of apoptosis and clinical outcome. Leukemia 1996; 10: 456-459. (Pubitemid 26128784)
17. Pepper C, Lin TT, Pratt G, Hewamana S, Brennan P, Hiller L et al. Mcl-1 expression has in vitro and in vivo significance in chronic lymphocytic leukemia and is associated with other poor prognostic markers. Blood 2008; 112: 3807-3817.
18. Willis SN, Chen L, Dewson G, Wei A, Naik E, Fletcher JI et al. Proapoptotic Bak is sequestered by Mcl-1 and Bcl-xL, but not Bcl-2, until displaced by BH3-only proteins. Genes Dev 2005; 19: 1294-1305. (Pubitemid 41003019)
19. Zenz T, Mohr J, Edelmann J, Sarno A, Hoth P, Heuberger M et al. Treatment resistance in chronic lymphocytic leukemia: the role of the p53 pathway. Leuk Lymphoma 2009; 50: 510-513.
20. Donehower LA, Harvey M, Slagle BL, McArthur MJ, Montgomery Jr CA, Butel JS et al. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 1992; 356: 215-221.
21. Cheson BD, Bennett JM, Rai KR, Grever MR, Kay NE, Schiffer CA et al. Guidelines for clinical protocols for chronic lymphocytic leukemia: recommendations of the National Cancer Institute-sponsored working group. Am J Hematol 1988; 29: 152-163.
22. Trachootham D, Zhang H, Zhang W, Feng L, Du M, Zhou Y et al. Effective elimination of fludarabine-resistant CLL cells by PEITC through a redox-mediated mechanism. Blood 2008; 112: 1912-1922.
23. Pelicano H, Feng L, Zhou Y, Carew JS, Hileman EO, Plunkett W et al. Inhibition of mitochondrial respiration: a novel strategy to enhance drug-induced apoptosis in human leukemia cells by a reactive oxygen species-mediated mechanism. J Biol Chem 2003; 278: 37832-37839. (Pubitemid 37175311)
24. Dohner H, Fischer K, Bentz M, Hansen K, Benner A, Cabot G et al. p53 gene deletion predicts for poor survival and non-response to therapy with purine analogs in chronic B-cell leukemias. Blood 1995; 85: 1580-1589.
25. Enzler T, Kater AP, Zhang W, Widhopf 2nd GF, Chuang HY, Lee J et al. Chronic lymphocytic leukemia of Emu-TCL1 transgenic mice undergoes rapid cell turnover that can be offset by extrinsic CD257 to accelerate disease progression. Blood 2009; 114: 4469-4476.
26. Huang P, Sandoval A, Van Den Neste E, Keating MJ, Plunkett W. Inhibition of RNA transcription: a biochemical mechanism of action against chronic lymphocytic leukemia cells by fludarabine. Leukemia 2000; 14: 1405-1413. (Pubitemid 30599321)
27. Aqeilan RI, Calin GA, Croce CM. miR-15a and miR-16-1 in cancer: discovery, function and future perspectives. Cell Death Differ 2010; 17: 215-220.
28. Wang LL. Biology of osteogenic sarcoma. Cancer J 2005; 11: 294-305. (Pubitemid 44698796)
29. Hollstein M, Sidransky D, Vogelstein B, Harris CC. p53 mutations in human cancers. Science 1991; 253: 49-53. (Pubitemid 21917115)
30. Bennett WP, Hollstein MC, Hsu IC, Sidransky D, Lane DP, Vogelstein B et al. Mutational spectra and immunohistochemical analyses of p53 in human cancers. Chest 1992; 101(3 Suppl): 19S-20S.
31. Levine AJ, Momand J, Finlay CA. The p53 tumour suppressor gene. Nature 1991; 351: 453-456. (Pubitemid 21896613)
32. Cordone I, Masi S, Mauro FR, Soddu S, Morsilli O, Valentini T et al. p53 expression in B-cell chronic lymphocytic leukemia: a marker of disease progression and poor prognosis. Blood 1998; 91: 4342-4349. (Pubitemid 28261999)
33. Levine AJ, Oren M. The first 30 years of p53: growing ever more complex. Nat Rev Cancer 2009; 9: 749-758.
34. Chipuk JE, Green DR. Dissecting p53-dependent apoptosis. Cell Death Differ 2006; 13: 994-1002.
35. Vucic D, Dixit VM, Wertz IE. Ubiquitylation in apoptosis: a post-translational modification at the edge of life and death. Nat Rev Mol Cell Biol 2011; 12: 439-452.
36. Ploner C, Kofler R, Villunger A. Noxa: at the tip of the balance between life and death. Oncogene 2008; 27(Suppl 1): S84-S92.
37. Pietrzak M, Puzianowska-Kuznicka M. p53-dependent repression of the human MCL-1 gene encoding an anti-apoptotic member of the BCL-2 family: the role of Sp1 and of basic transcription factor binding sites in the MCL-1 promoter. Biol Chem 2008; 389: 383-393. (Pubitemid 351773909)
38. Sampath D, Liu C, Vasan K, Sulda M, Puduvalli VK, Wierda WG et al. Histone deacetylases mediate the silencing of miR-15a, miR-16, and miR-29b in chronic lymphocytic leukemia. Blood 2012; 119: 1162-1172.
39. Calin GA, Croce CM. Chronic lymphocytic leukemia: interplay between noncoding RNAs and protein-coding genes. Blood 2009; 114: 4761-4770.
40. Merkel O, Asslaber D, Pinon JD, Egle A, Greil R. Interdependent regulation of p53 and miR-34a in chronic lymphocytic leukemia. Cell Cycle 2010; 9: 2764-2768.