Molecules that target nucleophosmin for cancer treatment: An update

Oncotarget

Volumn 7, Issue 28, 2016, Pages 44821-44840

  Di Matteo, Adele ^a   Franceschini, Mimma ^b   Chiarella, Sara ^b   Rocchio, Serena ^c   Travaglini Allocatelli, Carlo ^c   Federici, Luca ^b  

^a CNR   (Italy)

^b UNIVERSITY OF CHIETI   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Acute myeloid leukemia; B23; Nucleophosmin; Solid tumours; Targeted therapy

Indexed keywords

ALANYLARGINYLARGINYLASPARAGINYLARGINYLARGINYLARGINYLARGINYLTRYPTOPHYLARGINYLGLUTAMIC ACID; ANTINEOPLASTIC AGENT; APTAMER; ASENIC OXIDE; AVRAINVILLAMIDE; CIGB 300; DEGUELIN; DOXORUBICIN; EPIGALLOCATECHIN GALLATE; MYC PROTEIN; NSC 348884; NUCANT 6L; NUCLEOPHOSMIN; PROTEIN INHIBITOR; RETINOIC ACID; TETRA N METHYL PYRIDYL PORPHYRIN; UNCLASSIFIED DRUG; YTR 107; INDOLE DERIVATIVE; NUCLEAR PROTEIN;

AMINO TERMINAL SEQUENCE; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; BIOINFORMATICS; CANCER THERAPY; CARBOXY TERMINAL SEQUENCE; CELLULAR DISTRIBUTION; DRUG IDENTIFICATION; DRUG POTENTIATION; DRUG RECEPTOR BINDING; DRUG STRUCTURE; ENZYME ACTIVATION; HUMAN; IC50; NONHUMAN; NPM1 GENE; OLIGOMERIZATION; PROTEIN DNA BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; PROTEIN TARGETING; AMINO ACID SEQUENCE; ANTAGONISTS AND INHIBITORS; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; HEMATOLOGIC DISEASE; METABOLISM; MOLECULARLY TARGETED THERAPY; NEOPLASM; PROCEDURES; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANTINEOPLASTIC AGENTS; HEMATOLOGIC NEOPLASMS; HUMANS; INDOLES; MOLECULAR STRUCTURE; MOLECULAR TARGETED THERAPY; NEOPLASMS; NUCLEAR PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84978727282     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.8599     Document Type: Article

References (133)

1. Grisendi S, Mecucci C, Falini B, PandolfiPP. Nucleophosmin and cancer. Nat Rev Cancer. 2006; 6:493-505.
2. Wang D, Umekawa H, Olson MO. Expression and subcellular locations of two forms of nucleolar protein B23 in rat tissues and cells. Cell Mol Biol Res. 1993; 39: 33-42.
3. Emmott E, Hiscox JA. Nucleolar targeting: the hub of the matter. EMBO Rep. 2009; 10:231-238.
4. Marasco D, Scognamiglio PL. Identification of inhibitors of biological interactions involving intrinsically disordered proteins. Int J Mol Sci. 2015; 16:7394-7412.
5. Colombo E, Alcalay M, Pelicci PG. Nucleophosmin and its complex network: a possible therapeutic target in hematological diseases. Oncogene. 2011; 30:2595-2609.
6. Lindstrom, MS. NPM1/B23: A Multifunctional Chaperone in Ribosome Biogenesis and Chromatin Remodeling. Biochem Res Int. 2011; 2011:195209.
7. Federici L, Falini B. Nucleophosmin mutations in acute myeloid leukemia: a tale of protein unfolding and mislocalization. Protein Sci. 2013; 22:545-56.
8. Herrera, JE, Savkur R, Olson MO. The ribonuclease activity of nucleolar protein B23. Nucleic Acids Res. 1995; 23:3974-3979.
9. 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; 28:3114-3126.
10. Savkur RS, Olson MO. Preferential cleavage in preribosomal RNA by protein B23 endoribonuclease. Nucleic Acids Res. 1998; 26:4508-4515.
11. Maggi LB Jr, Kuchenruether M, Dadey DY, Schwope RM, Grisendi S, Townsend RR, PandolfiPP, Weber JD. Nucleophosmin serves as a rate-limiting nuclear export chaperone for the mammalian ribosome. Mol Cell Biol. 2008; 28:7050-7065.
12. Okuda M. The role of nucleophosmin in centrosome duplication. Oncogene. 2002; 21:6170-6174.
13. Wang W, Budhu A, Forgues M, Wang XW. Temporal and spatial control of nucleophosmin by the Ran-Crm1 complex in centrosome duplication. Nat Cell Biol. 2005; 7:823-830.
14. Fantini D, Vascotto C, Marasco D, D'Ambrosio C, Romanello M, Vitagliano L, Pedone C, Poletto M, Cesaratto L, Quadrifoglio F, Scaloni A, Radicella JP, Tell G. Critical lysine residues within the overlooked N-terminal domain of human APE1 regulate its biological functions. Nucleic Acids Res. 2010; 38:8239-8256.
15. Ziv O, Zeisel A, Mirlas-Neisberg N, Swain U, Nevo R, Ben-Chetrit N, Martelli MP4, Rossi R, Schiesser S, Canman CE, Carell T, Geacintov NE, Falini B, Domany E, Livneh Z. Identification of novel DNA-damage tolerance genes reveals regulation of translesion DNA synthesis by nucleophosmin. Nat Commun. 2014; 5:5437.
16. Okuwaki M, Matsumoto K, Tsujimoto M, Nagata K. Function of nucleophosmin/B23, a nucleolar acidic protein, as a histone chaperone. FEBS Lett. 2001; 506:272-276.
17. Szebeni A, Olson MO. Nucleolar protein B23 has molecular chaperone activities. Protein Sci. 1999; 8:905-912.
18. Eitoku M, Sato L, Senda T, Horikoshi M. Histone chaperones: 30 years from isolation to elucidation of the mechanisms of nucleosome assembly and disassembly. Cell Mol Life Sci. 2008; 65:414-444.
19. Colombo E, Marine JC, Danovi D, Falini B, Pelicci PG. Nucleophosmin regulates the stability and transcriptional activity of p53. Nat Cell Biol. 2002; 4:529-533.
20. Itahana K, Bhat KP, Jin A, Itahana Y, Hawke D, Kobayashi R, Zhang Y. Tumour suppressor ARF degrades B23, a nucleolar protein involved in ribosome biogenesis and cell proliferation. Molecular Cell. 2003; 12:1151-1164.
21. Kurki S, Peltonen K, Latonen L, Kiviharju TM, Ojala PM, Meek D, Laiho M. Nucleolar protein NPM interacts with HDM2 and protects tumour suppressor protein p53 from HDM2-mediated degradation. Cancer Cell. 2004; 5:465-475.
22. Bertwistle D, Sugimoto M, Sherr CJ. Physical and functional interactions of the Arf tumour suppressor protein with nucleophosmin/B23. Mol Cell Biol. 2004; 24:985-996.
23. Kuo ML, den Besten W, Bertwistle D, Roussel MF, Sherr CJ. N-terminal polyubiquitination and degradation of the Arf tumour suppressor. Genes Dev. 2004; 18: 1862-1874.
24. Li Z, Boone D, Hann SR. Nucleophosmin interacts directly with c-Myc and controls c-Myc-induced hyperproliferation and transformation. Proc Natl Acad Sci U S A. 2008; 105:18794-18799.
25. Li Z, Hann SR. Nucleophosmin is essential for c-Myc nucleolar localization and c-Myc-mediated rDNA transcription. Oncogene. 2013; 32:1988-1994.
26. Szebeni A, Olson MO. Nucleolar protein B23 has molecular chaperone activities. Protein Sci. 1999; 8:905-912.
27. Hingorani K, Szebeni A, Olson MO. Mapping the functional domains of nucleolar protein B23. J Biol Chem 2000; 275:24451-24457
28. Mitrea DM, Grace CR, Buljan M, Yun MK, Pytel NJ, Satumba J, Nourse A, Park CG, Madan Babu M, White SW, Kriwacki RW. Structural polymorphism in the N-terminal oligomerization domain of NPM1. Proc Natl Acad Sci U S A. 2014; 111:4466-4471.
29. Federici L, Arcovito A, Scaglione GL, Scaloni F, Lo Sterzo C, Di Matteo A, Falini B, Giardina B, Brunori M. Nucleophosmin C-terminal leukemia-associated domain interacts with G-rich quadruplex forming DNA. J Biol Chem. 2010; 285:37138-37149.
30. Falini B, Mecucci C, Tiacci E, Alcalay M, Rosati R, Pasqualucci L, La Starza R, Diverio D, Colombo E, Santucci A, Bigerna B, Pacini R, Pucciarini A, et al. Cytoplasmic nucleophosmin in acute myelogenous leukemia with a normal karyotype. N Engl J Med. 2005; 352:254-266.
31. Eirín-López JM, Frehlick LJ, Ausió J. Long-term evolution and functional diversification in the members of the nucleophosmin/nucleoplasmin family of nuclear chaperones. Genetics. 2006; 173:1835-1850
32. Lee HH, Kim HS, Kang JY, Lee BI, Ha JY, Yoon HJ, Lim SO, Jung G, Suh SW. Crystal structure of human nucleophosmin-core reveals plasticity of the pentamerpentamer interface. Proteins. 2007; 69:672-678.
33. Namboodiri VM, Dutta S, Akey IV, Head JF, Akey CW. The crystal structure of Drosophila NLP-core provides insight into pentamer formation and histone binding. Structure. 2003; 11:175-186.
34. Namboodiri VM, Akey IV, Schmidt-Zachmann MS, Head JF, Akey CW. The structure and function of Xenopus NO38-core, a histone chaperone in the nucleolus. Structure. 2004; 12:2149-2160.
35. Negi SS, Olson MO (2006) Effects of interphase and mitotic phosphorylation on the mobility and location of nucleolar protein B23. J Cell Sci. 2006; 119:3676-3685.
36. Wang W, Budhu A, Forgues M, Wang XW. Temporal and spatial control of nucleophosmin by the Ran-Crm1 complex in centrosome duplication. Nat Cell Biol. 2005; 7:823-830.
37. Marasco D, Ruggiero A, Vascotto C, Poletto M, Scognamiglio PL, Tell G, Vitagliano L. Role of mutual interactions in the chemical and thermal stability of nucleophosmin NPM1 domains. Biochem Biophys Res Commun. 2013; 430:523-528.
38. Herrera JE, Correia JJ, Jones AE, Olson MO. Sedimentation analyses of the salt-and divalent metal ion-induced oligomerization of nucleolar protein B23. Biochemistry. 1996;35:2668-2673.
39. Grummitt CG, Townsley FM, Johnson CM, Warren AJ, Bycroft M. Structural consequences of nucleophosmin mutations in acute myeloid leukemia. J Biol Chem. 2008; 283:23326-23332.
40. Falini B, Bolli N, Shan J, Martelli MP, Liso A, Pucciarini A, Bigerna B, Pasqualucci L, Mannucci R, Rosati R, Gorello P, Diverio D, Roti G, et al. Both carboxy-terminus NES motif and mutated tryptophan(s) are crucial for aberrant nuclear export of nucleophosmin leukemic mutants in NPMc+ AML. Blood. 2006; 107:4514-4523.
41. Wang D, Baumann A, Szebeni A, Olson MO. The nucleic acid binding activity of nucleolar protein B23.1 resides in its carboxyl-terminal end. J Biol Chem. 1994; 269:30994-30998.
42. Xu Y, Fang F, Dhar SK, St Clair WH, Kasarskis EJ, St Clair DK. The role of a single-stranded nucleotide loop in transcriptional regulation of the human sod2 gene. J Biol Chem. 2007; 282:15981-15994.
43. Gallo A, Lo Sterzo C, Mori M, Di Matteo A, Bertini I, Banci L, Brunori M, Federici L. Structure of nucleophosmin DNA-binding domain and analysis of its complex with a G-quadruplex sequence from the c-MYC promoter. J Biol Chem. 2012; 287:26539-26548.
44. Arcovito A, Chiarella S, Della Longa S, Di Matteo A, Lo Sterzo C, Scaglione GL, Federici L. Synergic role of nucleophosmin three-helix bundle and a flanking unstructured tail in the interaction with G-quadruplex DNA. J Biol Chem. 2014; 289:21230-21241.
45. Scognamiglio PL, Di Natale C, Leone M, Poletto M, Vitagliano L, Tell G, Marasco D. G-quadruplex DNA recognition by nucleophosmin: new insights from protein dissection. Biochim Biophys Acta. 2014; 1840:2050-2059.
46. 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; 29:5115-5127.
47. Léotoing L, Meunier L, Manin M, Mauduit C, Decaussin M, Verrijdt G, Claessens F, Benahmed M, Veyssière G, Morel L, Beaudoin C. Influence of nucleophosmin/B23 on DNA binding and transcriptional activity of the androgen receptor in prostate cancer cell. Oncogene. 2008; 27:2858-2867.
48. Yun JP, Miao J, Chen GG, Tian QH, Zhang CQ, Xiang J, Fu J, Lai PB. Increased expression of nucleophosmin/B23 in hepatocellular carcinoma and correlation with clinicopathological parameters. Br J Cancer. 2007; 96:477-484.
49. Pianta A, Puppin C, Franzoni A, Fabbro D, Di Loreto C, Bulotta S, Deganuto M, Paron I, Tell G, Puxeddu E, Filetti S, Russo D, Damante G. Nucleophosmin is overexpressed in thyroid tumours. Biochem Biophys Res Commun. 2010; 397:499-504.
50. Nozawa Y, Van Belzen N, Van der Made AC, Dinjens WN, Bosman FT. Expression of nucleophosmin/B23 in normal and neoplastic colorectal mucosa. J Pathol. 1996; 178:48-52.
51. Tanaka M, Sasaki H, Kino I, Sugimura T, Terada M. Genes preferentially expressed in embryo stomach are predominantly expressed in gastric cancer. Cancer Res. 1992; 52:3372-3377.
52. Zhu Y, Shi M, Chen H, Gu J, Zhang J, Shen B, Deng X, Xie J, Zhan X, Peng C. NPM1 activates metabolic changes by inhibiting FBP1 while promoting the tumourigenicity of pancreatic cancer cells. Oncotarget. 2015; 6:21443-21451. doi: 10.18632/oncotarget.4167.
53. Chen J, Sun J, Yang L, Yan Y, Shi W, Shi J, Huang Q, Chen J, Lan Q. Upregulation of B23 promotes tumour cell proliferation and predicts poor prognosis in glioma. Biochem Biophys Res Commun. 2015; 466:124-30.
54. Holmberg Olausson K, Elsir T, Moazemi Goudarzi K, Nistér M, Lindström MS. NPM1 histone chaperone is upregulated in glioblastoma to promote cell survival and maintain nucleolar shape. Sci Rep. 2015; 5:16495.
55. Kuo YH, Chen YT, Tsai HP, Chai CY, Kwan AL. (2015) Nucleophosmin overexpression is associated with poor survival in astrocytoma. APMIS. 2015; 123:515-522.
56. Yung BY. Oncogenic role of nucleophosmin/B23. Chang Gung Med J. 2007; 30:285-293.
57. Zeller KI, Haggerty TJ, Barrett JF, Guo Q, Wonsey DR, Dang CV. Characterization of nucleophosmin (B23) as a Myc target by scanning chromatin immunoprecipitation. J Biol Chem. 2001; 276:48285-48291.
58. Roussel P, Hernandez-Verdun D. Identification of Ag-NOR proteins, markers of proliferation related to ribosomal gene activity. Exp Cell Res. 1994; 214: 465-472.
59. Poletto M, Malfatti MC, Dorjsuren D, Scognamiglio PL, Marasco D, Vascotto C, Jadhav A, Maloney DJ, Wilson DM 3rd, Simeonov A, Tell G. Inhibitors of the apurinic/apyrimidinic endonuclease 1 (APE1)/nucleophosmin (NPM1) interaction that display anti-tumor properties. Mol Carcinog. 2015; doi: 10.1002/mc.22313.
60. Morris SW, Kirstein MN, Valentine MB, Dittmer KG, Shapiro DN, Saltman DL, Look AT. Fusion of a kinase gene, ALK, to a nucleolar protein gene, NPM, in non-Hodgkin's lymphoma. Science. 1994; 263:1281-1284.
61. Falini B, Nicoletti I, Bolli N, Martelli MP, Liso A, Gorello P, Mandelli F, Mecucci C, Martelli MF. Translocations and mutations involving the nucleophosmin (NPM1) gene in lymphomas and leukemias. Haematologica. 2007; 92:519-532.
62. Chiarle R, Gong JZ, Guasparri I, Pesci A, Cai J, Liu J et al. NPM-ALK transgenic mice spontaneously develop T-cell lymphomas and plasma cell tumours. Blood. 2003; 101:1919-1927.
63. Redner RL, Chen JD, Rush EA, Li H, Pollock SL. The t(5;17) acute promyelocytic leukemia fusion protein NPMRAR interacts with co-repressor and co-activator proteins and exhibits both positive and negative transcriptional properties. Blood. 2000; 95:2683-2690.
64. Okazuka K, Masuko M, Seki Y, Hama H, Honma N, Furukawa T, Toba K, Kishi K, Aizawa Y. Successful all-trans retinoic acid treatment of acute promyelocytic leukemia in a patient with NPM/RAR fusion. Int J Hematol. 2007; 86 246-249.
65. Yoneda-Kato N, Look AT, Kirstein MN, Valentine MB, Raimondi SC, Cohen KJ, Carroll AJ, Morris SW. The t(3;5)(q25.1;q34) of myelodysplastic syndrome and acute myeloid leukemia produces a novel fusion gene, NPMMLF1. Oncogene. 1996; 12:265-275.
66. Berger R, Busson M, Baranger L, Hélias C, Lessard M, Dastugue N, Speleman F. Loss of the NPM1 gene in myeloid disorders with chromosome 5 rearrangements. Leukemia. 2006; 20:319-321.
67. Falini B, Nicoletti I, Martelli MF, Mecucci C. Acute myeloid leukemia carrying cytoplasmic/mutated nucleophosmin (NPMc+ AML): biologic and clinical features. Blood. 2007; 109:874-85.
68. Meani N, Alcalay M. Role of nucleophosmin in acute myeloid leukemia. Expert Rev Anticancer Ther. 2009; 9:1283-94.
69. Scaloni F, Gianni S, Federici L, Falini B, Brunori M. Folding mechanism of the C-terminal domain of nucleophosmin: residual structure in the denatured state and its pathophysiological significance. FASEB J. 2009; 23:2360-2365.
70. Scaloni F, Federici L, Brunori M, Gianni S. Deciphering the folding transition state structure and denatured state properties of Nucleophosmin C-terminal domain. Proc Natl Acad Sci USA. 2010; 107:5447-5452.
71. Falini B, Bolli N, Liso A, Martelli MP, Mannucci R, Pileri S, Nicoletti I. Altered nucleophosmin transport in acute myeloid leukaemia with mutated NPM1: molecular basis and clinical implications. Leukemia. 2009; 23:1731-1743.
72. Falini B, Gionfriddo I, Cecchetti F, Ballanti S, Pettirossi V, Martelli MP. Acute Myeloid Leukemia with mutated nucleophosmin (NPM1): any hope for a targeted therapy? Blood Rev. 2011; 25:247-254.
73. Sportoletti P, Varasano E, Rossi R, Mupo A, Tiacci E, Vassiliou G, Martelli MP, Falini B. Mouse models of NPM1-mutated acute myeloid leukemia: biological and clinical implications. Leukemia. 2015; 29:269-278.
74. Arber D, Brunning RD, Le Beau MM, Falini B, Vardiman JW, Porwit A, et al. Acute myeloid leukaemia with recurrent genetic abnormalities. In: Swerdlow SE, Campo E, Harris NL, et al, editors. WHO classification of tumours of haematopoietic and lymphoid tissues. Lyon, France: International Agency for Research on Cancer (IARC). 2008; 110-123.
75. Ofran Y, Rowe JM. Introducing minimal residual disease in AML. Curr Opin Hematol. 2015; 22:139-145.
76. Di Fiore PP. Playing both sides: nucleophosmin between tumour suppression and oncogenesis. J Cell Biol. 2008;182:7-9.
77. Bonetto P, Davoli T, Sironi C, Amati B, Pelicci PG, Colombo E. Nucleophosmin and its AML-associated mutant regulate c-Myc turnover through Fbw7 gamma. J Cell Biol. 2008; 182:19-26.
78. Colombo E, Martinelli P, Zamponi R, Shing DC, Bonetti P, Luzi L, Volorio S, Bernard L, Pruneri G, Alcalay M, Pelicci PG. Delocalization and destabilization of the Arf tumour suppressor by the leukemia-associated NPM mutant. Cancer Res. 2006; 66:3044-3050.
79. Leong SM, Tan BX, Bte Ahmad B, Yan T, Chee LY, Ang ST, Tay KG, Koh LP, Yeoh AE, Koay ES, Mok YK, Lim TM. Mutant nucleophosmin deregulates cell death and myeloid differentiation through excessive caspase-6 and-8 inhibition. Blood. 2010; 116:3286-96.
80. Noguera NI, Song MS, Divona M, Catalano G, Calvo KL, García F, Ottone T, Florenzano F, Faraoni I, Battistini L, Colombo E, Amadori S, PandolfiPP, Lo-Coco F. Nucleophosmin/B26 regulates PTEN through interaction with HAUSP in acute myeloid leukemia. Leukemia. 2013; 27:1037-43.
81. Di Natale C, Scognamiglio PL, Cascella R, Cecchi C, Russo A, Leone M, Penco A, Relini A, Federici L, Di Matteo A, Chiti F, Vitagliano L, Marasco D. Nucleophosmin contains amyloidogenic regions that are able to form toxic aggregates under physiological conditions. FASEB J. 2015; 29:3689-3701.
82. Qi W, Shakalya K, Stejskal A, Goldman A, Beeck S, Cooke L, Mahadevan D. NSC348884, a nucleophosmin inhibitor disrupts oligomer formation and induces apoptosis in human cancer cells. Oncogene. 2008; 27:4210-4220.
83. Maiguel DA, Jones L, Chakravarty D, Yang C, Carrier F. Nucleophosmin sets a threshold for p53 response to UV radiation. Mol Cell Biol. 2004; 24:3703-3711.
84. Lindström MS, Zhang Y. B23 and ARF: friends or foes? Cell Biochem Biophys. 2006; 46:79-90.
85. Zhang J, Zhao HL, He JF, Li HY. Inhibitory effect of NSC348884, a small molecular inhibitor of nucleophosmin, on the growth of hepatocellular carcinoma cell line hepG2. [Article in Chinese]. Zhongguo Yi Xue Ke Xue Yuan Xue Bao. 2012; 34:58-61.
86. Balusu R, Fiskus W, Rao R, Chong DG, Nalluri S, Mudunuru U, Ma H, Chen L, Venkannagari S, Ha K, Abhyankar S, Williams C, McGuirk J, Khoury HJ, Ustun C, Bhalla KN. Targeting levels or oligomerization of nucleophosmin 1 induces differentiation and loss of survival of human AML cells with mutant NPM1. Blood. 2011; 118:3096-3106.
87. Emmott E, Hiscox JA. Nucleolar targeting: the hub of the matter. EMBO Rep. 2009; 10:231-8.
88. Fankhauser C, Izaurralde E, Adachi Y, Wingfield P, Laemmli UK. Specific complex of human immunodeficiency virus type 1 rev and nucleolar B23 proteins: dissociation by the Rev response element. Mol. Cell. Biol. 1991; 11:2567-2575.
89. Umekawa H, Chang JH, Correia JJ, Wang D, Wingfield PT, Olson MO. Nucleolar protein B23: bacterial expression, purification, oligomerization and secondary structures of two isoforms. Cell Mol Biol Res. 1993; 39:635-45.
90. Szebeni A, Herrera JE, Olson MO. Interaction of nucleolar protein B23 with peptides related to nuclear localization signals. Biochemistry. 1995; 34:8037-8042.
91. Chan HJ, Weng JJ, Yung BY. Nucleophosmin/B23-binding peptide inhibits tumour growth and up-regulates transcriptional activity of p53. Biochem Biophys Res Commun. 2005; 333:396-403.
92. Keefe AD, Pai S, Ellington A. Aptamers as therapeutics. Nat Rev Drug Discov. 2010; 9:537-550.
93. Nimjee SM, Rusconi CP, Sullenger BA. APTAMERS: an emerging class of therapeutics. Annu Rev Med. 2005; 56: 555-583.
94. Jian Y, Gao Z, Sun J, Shen Q, Feng F, Jing Y, Yang C. RNA aptamers interfering with nucleophosmin oligomerization induce apoptosis of cancer cells. Oncogene. 2009; 28:4201-4211.
95. Trembley JH, Wang G, Unger G, Slaton J, Ahmed K. Protein kinase CK2 in health and disease: CK2: a key player in cancer biology. Cell Mol Life Sci. 2009; 66:1858-1867.
96. Ruzzene M, Pinna LA. Addiction to protein kinase CK2: a common denominator of diverse cancer cells? Biochim Biophys Acta. 2010;1804:499-504.
97. Ahmad KA, Wang G, Unger G, Slaton J, Ahmed K. Protein kinase CK2-a key suppressor of apoptosis. Adv Enzyme Regul. 2008; 48:179-187.
98. Perea SE, Reyes O, Baladron I, Perera Y, Farina H, Gil J, Rodriguez A, Bacardi D, Marcelo JL, Cosme K, Cruz M, Valenzuela C, López-Saura PA, et al. CIGB-300, a novel proapoptotic peptide that impairs the CK2 phosphorylation and exhibits anticancer properties both in vitro and in vivo. Mol Cell Biochem. 2008; 316:163-167.
99. Perera Y, Farina HG, Gil J, Rodriguez A, Benavent F, Castellanos L, Gómez RE, Acevedo BE, Alonso DF, Perea SE. 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; 8:1189-1196.
100. Louvet E, Junéra HR, Le Panse S, Hernandez-Verdun D. Dynamics and compartmentation of the nucleolar processing machinery. Exp Cell Res. 2005; 304:457-470.
101. Louvet E, Junéra HR, Berthuy I, Hernandez-Verdun D. Compartmentation of the nucleolar processing proteins in the granular component is a CK2-driven process. Mol Biol Cell. 2006; 17:2537-2546.
102. Szebeni A, Hingorani K, Negi S, Olson MO. Role of protein kinase CK2 phosphorylation in the molecular chaperone activity of nucleolar protein b23. J Biol Chem. 2003; 278:9107-9115.
103. Perera Y, Costales HC, Diaz Y, Reyes O, Farina HG, Mendez L, Gómez RE, AcevedoBE, Gomez DE, Alonso DF, Perea SE. Sensitivity of tumour cells towards CIGB-300 anticancer peptide relies on its nucleolar localization. J Pept Sci. 2012; 18:215-223.
104. Martins LR, Perera Y, Lúcio P, Silva MG, Perea SE, Barata JT. Targeting chronic lymphocytic leukemia using CIGB-300, a clinical-stage CK2-specific cell-permeable peptide inhibitor. Oncotarget. 2014; 5:258-263. doi: 10.18632/oncotarget.1513.
105. Perera Y, Toro ND, Gorovaya L, Fernandez-DE-Cossio J, Farina HG, Perea SE. Synergistic interactions of the anticasein kinase 2 CIGB-300 peptide and chemotherapeutic agents in lung and cervical preclinical cancer models. Mol Clin Oncol. 2014; 2:935-944.
106. Solares AM, Santana A, Baladrón I, Valenzuela C, González CA, Díaz A, Castillo D, Ramos T, Gómez R, Alonso DF, Herrera L, Sigman H, Perea SE, et al. Safety and preliminary efficacy data of a novel casein kinase 2 (CK2) peptide inhibitor administered intralesionally at four dose levels inpatients with cervical malignancies. BMC Cancer. 2009; 9:146.
107. Sarduy MR, García I, Coca MA, Perera A, Torres LA, Valenzuela CM, Baladrón I, Solares M, Reyes V, Hernández I, Perera Y, Martínez YM, Molina L, et al. Optimizing CIGB-300 intralesional delivery in locally advanced cervical cancer. Br J Cancer. 2015; 112:1636-1643.
108. Fenical W, Jensen PR, Cheng XC. Avrainvillamide, a Cytotoxic Marine Natural Product, and Derivatives Thereof. US Patent 6, 066, 635. 2000
109. WulffJE, Siegrist R, Myers AG. The natural product avrainvillamide binds to the oncoprotein nucleophosmin. J Am Chem Soc. 2007; 129:14444-14451.
110. Mukherjee H, Chan KP, Andresen V, Hanley ML, Gjertsen BT, Myers AG. Interactions of the natural product (+)-avrainvillamide with nucleophosmin and exportin-1 mediate the cellular localization of nucleophosmin and its AML-associated mutants. ACS Chem Biol. 2015; 10:855-863.
111. Freyer MW, Buscaglia R, Kaplan K, Cashman D, Hurley LH, Lewis EA. Biophysical Studies of the c-MYC NHE III1 Promoter: Model Quadruplex Interactions with a Cationic Porphyrin. Biophys J. 2007; 92:2007-2015.
112. Siddiqui-Jain, C.L. Grand, D.J. Bearss, L.H. Hurley. Direct evidence for a G-quadruplex in a promoter region and its targeting with a small molecule to repress c-MYC transcription. Proc Natl Acad Sci U S A. 2002; 99:11593-11598.
113. Rapozzi V, Zorzet S, Zacchigna M, Della Pietra E, Cogoi S, Xodo LE (2014) Anticancer activity of cationic porphyrins in melanoma tumour-bearing mice and mechanistic in vitro studies. Mol Cancer. 2014;13:75.
114. Zhang YQ, Zhang YH, Xie J, Li MN, Liu ZR, Shen JY, Shi SS, Lan XY, Wang S, Cheng NL. TMPyP4-regulated cell proliferation and apoptosis through the Wnt/-catenin signaling pathway in SW480 cells. J Recept Signal Transduct Res. 2016; 36:167-172.
115. Drygin D1, Siddiqui-Jain A, O'Brien S, Schwaebe M, Lin A, Bliesath J, Ho CB, Proffitt C, Trent K, Whitten JP, Lim JK, Von HoffD, Anderes K, Rice WG. Anticancer activity of CX-3543: a direct inhibitor of rRNA biogenesis. Cancer Res. 2009; 69:7653-7661.
116. Chiarella S, De Cola A, Scaglione GL, Carletti E, Graziano V, Barcaroli D, Lo Sterzo C, Di Matteo A, Di Ilio C, Falini B, Arcovito A, De Laurenzi V, Federici L. Nucleophosmin mutations alter its nucleolar localization by impairing G-quadruplex binding at ribosomal DNA. Nucleic Acids Res. 2013; 41:3228-3239.
117. De Cola A, Pietrangelo L, Forlì F, Barcaroli D, Budani MC, Graziano V, Protasi F, Di Ilio C, De Laurenzi V, Federici L. AML cells carrying NPM1 mutation are resistant to nucleophosmin displacement from nucleoli caused by the G-quadruplex ligand TmPyP4. Cell Death Dis. 2014; 5:e1427.
118. Lo-Coco F, Avvisati G, Vignetti M, Thiede C, Orlando SM, Iacobelli S, Ferrara F, Fazi P, Cicconi L, Di Bona E, Specchia G, Sica S, Divona M, Levis A, et al. Retinoic acid and arsenic trioxide for acute promyelocytic leukemia. N Engl J Med. 2013; 369:111-121.
119. Sanz MA, Grimwade D, Tallman MS, Lowenberg B, Fenaux P, Estey EH, Naoe T, Lengfelder E, Büchner T, Döhner H, Burnett AK, Lo-Coco F. Management of acute promyelocytic leukemia: recommendations from an expert panel on behalf of the European LeukemiaNet. Blood. 2009; 113:1875-1891.
120. Martelli MP, Gionfriddo I, Mezzasoma F, Milano F, Pierangeli S, Mulas F, Pacini R, Tabarrini A, Pettirossi V, Rossi R, Vetro C, Brunetti L, Sportoletti P, Tet al. Arsenic trioxide and all-trans retinoic acid target NPM1 mutant oncoprotein levels and induce apoptosis in NPM1-mutated AML cells. Blood. 2015; 125:3455-3465.
121. El Hajj H, Dassouki Z, Berthier C, Raffoux E, Ades L, Legrand O, Hleihel R, Sahin U, Tawil N, Salameh A, Zibara K, Darwiche N, Mohty M, Dombret H, Fenaux P, de Thé H, Bazarbachi A. Retinoic acid and arsenic trioxide trigger degradation of mutated NPM1, resulting in apoptosis of AML cells. Blood. 2015; 125:3447-3454.
122. Wang Y, Ma W, Zheng W (2013) Deguelin, a novel antitumourigenic agent targeting apoptosis, cell cycle arrest and anti-angiogenesis for cancer chemoprevention. Mol Clin Oncol. 2013; 1:215-219.
123. Zhang L, Wei Y, Zhang J. Novel mechanisms of anticancer activities of green tea component epigallocatechin-3-gallate. Anticancer Agents Med Chem. 2014; 14:779-786.
124. Yi S, Wen L, He J, Wang Y, Zhao F, Zhao J, Zhao Z, Cui G, Chen Y. Deguelin, a selective silencer of the NPM1 mutant, potentiates apoptosis and induces differentiation in AML cells carrying the NPM1 mutation. Ann Hematol. 2015; 94:201-210.
125. Chi HT, Ly BT, Vu HA, Sato Y, Dung PC, Xinh PT. Down-regulated expression of NPM1 in IMS-M2 cell line by (-)-epigallocatechin-3-gallate. Asian Pac J Trop Biomed. 2014; 4:570-574.
126. Destouches D, Page N, Hamma-Kourbali Y, Machi V, Chaloin O, Frechault S, Birmpas C, Katsoris P, Beyrath J, Albanese P, Maurer M, Carpentier G, Strub JM, Van Dorsselaer A, Muller S, Bagnard D, Briand JP, Courty J. A simple approach to cancer therapy afforded by multivalent pseudopeptides that target cell-surface nucleoproteins. Cancer Res. 2011; 71:3296-3305.
127. Destouches D, Huet E, Sader M, Frechault S, Carpentier G, Ayoul F, Briand JP, Menashi S, Courty J. Multivalent pseudopeptides targeting cell surface nucleoproteins inhibit cancer cell invasion through tissue inhibitor of metalloproteinases 3 (TIMP-3) release. J Biol Chem. 2012; 287:43685-43693.
128. Koike A, Nishikawa H, Wu W, Okada Y, Venkitaraman AR, Ohta T. Recruitment of phosphorylated NPM1 to sites of DNA damage through RNF8-dependent ubiquitin conjugates. Cancer Res. 2010; 70:6746-6756.
129. Sekhar KR, Reddy YT, Reddy PN, Crooks PA, Venkateswaran A, McDonald WH, GengL, Sasi S, Van Der Waal RP, Roti JL, Salleng KJ, Rachakonda G, Freeman ML. The novel chemical entity YTR107 inhibits recruitment of nucleophosmin to sites of DNA damage, suppressing repair of DNA double-strand breaks and enhancing radiosensitization. Clin Cancer Res. 2011; 17:6490-6499.
130. Reddy YT, Sekhar KR, Sasi N, Reddy PN, Freeman ML, Crooks PA. Novel substituted (Z)-5-((N-benzyl-1H-indol-3-yl)methylene)imidazolidine-2, 4-diones and5-((N-benzyl-1H-indol-3-yl)methylene)pyrimidine-2, 4, 6(1H, 3H, 5H)-triones as potent radio-sensitizing agents. Bioorg Med Chem Lett. 2010; 20:600-602.
131. Sekhar KR, Benamar M, Venkateswaran A, Sasi S, Penthala NR, Crooks PA, Hann SR, Geng L, Balusu R, Abbas T, Freeman ML. Targeting nucleophosmin 1 represents a rational strategy for radiation sensitization. Int J Radiat Oncol Biol Phys. 2014; 89:1106-1114.
132. Penthala NR, Ketkar A, Sekhar KR, Freeman ML, EoffRL, Balusu R, Crooks PA. 1-Benzyl-2-methyl-3-indolylmethylene barbituric acid derivatives: Anti-cancer agents that target nucleophosmin 1 (NPM1). Bioorg Med Chem. 2015; 23:7226-7233.
133. Falini B, Brunetti L, Martelli MP. Dactinomycin in NPM1-Mutated Acute Myeloid Leukemia. N Engl J Med. 2015; 373:1180-1182.