Targeting levels or oligomerization of nucleophosmin 1 induces differentiation and loss of survival of human AML cells with mutant NPM1

Blood

Volumn 118, Issue 11, 2011, Pages 3096-3106

  Balusu, Ramesh ^a   Fiskus, Warren ^a   Rao, Rekha ^a   Chong, Daniel G ^b   Nalluri, Srilatha ^b   Mudunuru, Uma ^a   Ma, Hongwei ^a   Chen, Lei ^a   Venkannagari, Sreedhar ^a   Ha, Kyungsoo ^a   Abhyankar, Sunil ^a   Williams, Casey ^a   McGuirk, Joseph ^a   Khoury, Hanna Jean ^c   Ustun, Celalettin ^d   Bhalla, Kapil N ^a  

^a UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

^b MEDICAL COLLEGE OF GEORGIA   (United States)

^c EMORY UNIVERSITY   (United States)

^d UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTARABINE; NSC 348884; NUCLEOPHOSMIN; PROTEIN INHIBITOR; PROTEIN P21; PROTEIN P53; RETINOIC ACID; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ACUTE GRANULOCYTIC LEUKEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL CYCLE S PHASE; CELL DIFFERENTIATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; NUCLEAR EXPORT SIGNAL; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN TARGETING;

EID: 80052939925     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-09-309674     Document Type: Article

References (50)

1. Okuwaki M. The structure and functions of NPM1/nucleophosmin/B23, a multifunctional nucleolar acidic protein. J Biochem. 2008;143(4):441-448. (Pubitemid 351451762)
2. Grisendi S, Mecucci C, Falini B, Pandolfi PP. Nucleophosmin and cancer. Nat Rev Cancer. 2006;6(7):493-505. (Pubitemid 43980539)
3. Naoe T, Suzuki T, Kiyoi H, Urano T. Nucleophosmin: a versatile molecule associated with hematologic malignancies. Cancer Sci. 2006;97(10):963-969. (Pubitemid 44322540)
4. Okuda M. The role of nucleophosmin in centrosome duplication. Oncogene. 2002;21(40):6170-6174.
5. Swaminathan V, Kishore AH, Febitha KK, Kundu TK. Human histone chaperone nucleophosmin enhances acetylation-dependent chromatin transcription. Mol Cell Biol. 2005;25(17):7534-7545. (Pubitemid 41170116)
6. Yu Y, Maggi LB, Jr., Brady SN, et al. Nucleophosmin is essential for ribosomal protein L5 nuclear export. Mol Cell Biol. 2006;26(10):3798-3809. (Pubitemid 43726397)
7. Murano K, Okuwaki M, Hisaoka M, Nagata K. Transcription regulation of the rRNA gene by a multifunctional nucleolar protein, B23/nucleophosmin, through its histone chaperone activity. Mol Cell Biol. 2008;28(10):3114-3126. (Pubitemid 351657078)
8. Colombo E, Marine JC, Danovi D, Falini B, Pelicci PG. Nucleophosmin regulates the stability and transcriptional activity of p53. Nat Cell Biol. 2002;4(7):529-533. (Pubitemid 34752440)
9. Bertwistle D, Sugimoto M, Sherr CJ. Physical and functional interactions of the Arf tumor suppressor protein with nucleophosmin/B23. Mol Cell Biol. 2004;24(3):985-996. (Pubitemid 38112164)
10. Kurki S, Peltonen K, Laiho M. Nucleophosmin, HDM2 and p53: players in UV damage incited nucleolar stress response. Cell Cycle. 2004;3(8):976-979. (Pubitemid 40268643)
11. Tokuyama Y, Horn HF, Kawamura K, Tarapore P, Fukasawa K. Specific phosphorylation of nucleophosmin on Thr(199) by cyclin-dependent kinase 2-cyclin E and its role in centrosome duplication. J Biol Chem. 2001;276(24):21529- 21537.
12. Liu X, Liu Z, Jang SW, et al. Sumoylation of nucleophosmin/B23 regulates its subcellular localization, mediating cell proliferation and survival. Proc Natl Acad Sci U S A. 2007;104(23):9679-9684. (Pubitemid 47175326)
13. Sato K, Hayami R, Wu W, et al. Nucleophosmin/B23 is a candidate substrate for the BRCA1-BARD1 ubiquitin ligase. J Biol Chem. 2004;279(30):30919-30922. (Pubitemid 39037748)
14. Shandilya J, Swaminathan V, Gadad SS, Choudhari R, Kodaganur GS, Kundu TK. Acetylated NPM1 localizes in the nucleoplasm and regulates transcriptional activation of genes implicated in oral cancer manifestation. Mol Cell Biol. 2009;29(18):5115-5127.
15. Hingorani K, Szebeni A, Olson MO. Mapping the functional domains of nucleolar protein B23. J Biol Chem. 2000;275(32):24451-24457. (Pubitemid 30626537)
16. Qi W, Shakalya K, Stejskal A, et al. NSC348884, a nucleophosmin inhibitor disrupts oligomer formation and induces apoptosis in human cancer cells. Oncogene. 2008;27(30):4210-4220. (Pubitemid 351969907)
17. Falini B, Nicoletti I, Bolli N, et al. Translocations and mutations involving the nucleophosmin (NPM1) gene in lymphomas and leukemias. Haematologica. 2007;92(4):519-532. (Pubitemid 350144298)
18. Bischof D, Pulford K, Mason DY, Morris SW. Role of the nucleophosmin (NPM) portion of the non-Hodgkin's lymphoma-associated NPM-anaplastic lymphoma kinase fusion protein in oncogenesis. Mol Cell Biol. 1997;17(4):2312-2325. (Pubitemid 27133318)
19. Yoneda-Kato N, Look AT, Kirstein MN, et al. The t(3;5)(q25.1;q34) of myelodysplastic syndrome and acute myeloid leukemia produces a novel fusion gene, NPM-MLF1. Oncogene. 1996;12(2):265-275. (Pubitemid 26042564)
20. Redner RL, Rush EA, Faas S, Rudert WA, Corey SJ. The t(5;17) variant of acute promyelocytic leukemia expresses a nucleophosmin-retinoic acid receptor fusion. Blood. 1996;87(3):882-886. (Pubitemid 26043517)
21. Falini B, Nicoletti I, Martelli MF, Mecucci C. Acute myeloid leukemia carrying cytoplamic/mutated nucleophosmin (NPMc+ AML): biologic and clinical features. Blood. 2007;109(3):874-885. (Pubitemid 46220630)
22. Falini B, Sportoletti P, Martelli MP. Acute myeloid leukemia with mutated NPM1: diagnosis, prognosis and therapeutic perspectives. Curr Opin Oncol. 2009;21(6):573-581.
23. Grummitt CG, Townsley FM, Johnson CM, Warren AJ, Bycroft M. Structural consequences of nucleophosmin mutations in acute myeloid leukemia. J Biol Chem. 2008;283(34):23326-23332.
24. Grisendi S, Bernardi R, Rossi M, et al. Role of nucleophosmin in embryonic development and tumorigenesis. Nature. 2005;437(7055):147-153. (Pubitemid 41613442)
25. Cheng K, Sportoletti P, Ito K, et al. The cytoplasmic NPM mutant induces myeloproliferation in a transgenic mouse model. Blood. 2010;115(16):3341-3345.
26. Bolli N, Payne EM, Grabher C, et al. Expression of the cytoplasmic NPM1 mutant (NPMc+) causes the expansion of hematopoietic cells in zebrafish. Blood. 2010;115(16):3329-3340.
27. Mullighan CG, Kennedy A, Zhou X, et al. Pediatric acute myeloid leukemia with NPM1 mutations is characterized by a gene expression profile with dysregulated HOX gene expression distinct from MLL-rearranged leukemias. Leukemia. 2007;21(9):2000-2009. (Pubitemid 47299976)
28. Hu YL, Fong S, Ferrell C, Largman C, Shen WF. HOXA9 modulates its oncogenic partner Meis1 to influence normal hematopoiesis. Mol Cell Biol. 2009;29(18):5181-5192.
29. Wang Z, Iwasaki M, Ficara F, et al. GSK-3 promotes conditional association of CREB and its coactivators with MEIS1 to facilitate HOX-mediated transcription and oncogenesis. Cancer Cell. 2010;17(6):597-608.
30. Du W, Zhou Y, Pike S, Pang Q. NPM phosphorylation stimulates Cdk1, overrides G2/M checkpoint and increases leukemic blasts in mice. Carcinogenesis. 2010;31(2):302-310.
31. Lim MJ, Wang XW. Nucleophosmin and human cancer. Cancer Detect Prev. 2006;30(6):481-490. (Pubitemid 44834564)
32. Fiskus W, Wang Y, Sreekumar A, et al. Combined epigenetic therapy with the histone methyltransferase EZH2 inhibitor 3-deazaneplanocin A and the histone deacetylase inhibitor panobinostat against human AML cells. Blood. 2009;114(13):2733-2743.
33. Fiskus W, Buckley KM, Rao R, et al. Panobinostat treatment depletes EZH2 and DNMT1 levels and enhances decitabine mediated de-repression of JunB and loss of survival of human acute leukemia cells. Cancer Biol Ther. 2009;8(10):939-50.
34. Quentmeier H, Martelli MP, Dirks WG, et al. Cell line OCI/AML3 bears exon-12 NPM gene mutation-A and cytoplasmic expression of nucleophosmin. Leukemia. 2005;19(10):1760-1767. (Pubitemid 41486153)
35. Rao R, Nalluri S, Fiskus W, et al. Heat shock protein 90 inhibition depletes TrkA levels and signaling in human acute leukemia cells. Mol Cancer Ther. 2010;9(8):2232-42.
36. Bhalla K, Ibrado AM, Tourkina E, et al. High-dose mitoxantrone induces programmed cell death or apoptosis in human myeloid leukemia cells. Blood. 1993;82(10):3133-3140. (Pubitemid 23334941)
37. Wang GG, Pasillas MP, Kamps MP. Meis1 programs transcription of FLT3 and cancer stem cell character, using a mechanism that requires interaction with Pbx and a novel function of Meis1 Cterminus. Blood. 2005;106(1):254-264. (Pubitemid 40967201)
38. Scaffidi P, Misteli T, Bianchi ME, Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature. 2002;418(6894):191-195. (Pubitemid 34773774)
39. Gale RE, Green C, Allen C, et al. The impact of FLT3 internal tandem duplication mutant level, number, size, and interaction with NPM1 mutations in a large cohort of young adult patients with acute myeloid leukemia. Blood. 2008;111(5):2776-84.
40. Calvo KR, Knoepfler PS, Sykes DB, Pasillas MP, Kamps MP. Meis1a suppresses differentiation by G-CSF and promotes proliferation by SCF: potential mechanisms of cooperativity with Hoxa9 in myeloid leukemia. Proc Natl Acad Sci U S A. 2001;98(23):13120-13125. (Pubitemid 33051327)
41. Alcalay M, Tiacci E, Bergomas R, et al. Acute myeloid leukemia bearing cytoplasmic nucleophosmin (NPMc+ AML) shows a distinct gene expression profile characterized by up-regulation of genes involved in stem-cell maintenance. Blood. 2005;106(3):899-902. (Pubitemid 41076430)
42. Porse BT, Bryder D, Theilgaard-Monch K, et al. Loss of C/EBPalpha cell cycle control increase myeloid progenitor proliferation and transforms the neutrophil granulocyte lineage. J Exp Med. 2005;202(1):85-96. (Pubitemid 41002912)
43. Koschmieder S, Halmos B, Levantini E, Tenen DG. Dysregulation of C/EBPalpha differentiation pathway in human cancer. J Clin Oncol. 2009;27(4):619-628.
44. Nowak D, Steward D, Koeffler HP. Differentiation therapy of leukemia: 3 decades of development. Blood. 2009;113(16):3655-3665.
45. Schlenk RF, Dohner K, Kneba M, et al. Gene mutations and response to treatment with all-trans retinoic acid in elderly patients with acute myeloid leukemia: results from the AMLSG Trial AML HD98B. Haematologica. 2009;94(1):54-60.
46. Burnett AK, Hills RK, Green C, et al. The impact on outcome of the addition of all-trans retinoic acid to intensive chemotherapy in younger patients with nonacute promyelocytic actute myeloid leukemia: overall results and results in genotypic subgroups defined by mutations in NPM1, FLT3, and CEBPA. Blood. 2010;115(5):948-956.
47. Hsu CY, Yung BY. Over-expression of nucleophosmin/B23 decreases the susceptibility of human leukemia HL-60 cells to retinoic acid-induced differentiation and apoptosis. Int J Cancer. 2000;88(3):392-400.
48. Perera Y, Farina HG, Gil J, et al. Anticancer peptide CIGB-300 binds to nucleophosmin/B23, impairs its CK2-mediated phosphorylation, and leads to apoptosis through its nucleolar disassembly activity. Mol Cancer Ther. 2009;8(5):1189-1196.
49. Paschka P, Schlenk RF, Gaidzik VI, et al. IDH1 and IDH2 mutations are frequent genetic alterations in acute myeloid leukemia and confer adverse prognosis in cytogenetically normal acute myeloid leukemia with NPM1 mutation without FLT3 internal tandem duplication. J Clin Oncol. 2010;28(22):3636-3643.
50. Figueroa ME, Abdel-Wahab O, Lu C, et al. Leukemic IDH1 and IDH2 mutations result in a hypermethylation phenotype, disrupt TET2 function, and impair hematopoietic differentiation. Cancer Cell. 2010;18(6):553-567.