Implication of NPM1 phosphorylation and preclinical evaluation of the nucleoprotein antagonist N6L in prostate cancer

Oncotarget

Volumn 7, Issue 43, 2016, Pages 69397-69411

  Destouches, Damien ^a,b,c   Sader, Maha ^a,c   Terry, Stéphane ^d   Marchand, Charles ^a,b   Maillé, Pascale ^a,b,e   Soyeux, Pascale ^a,b   Carpentier, Gilles ^a,c   Semprez, Fannie ^a,b   Céraline, Jocelyn ^f   Allory, Yves ^a,b,e   Courty, José ^a,c   De La Taille, Alexandre ^a,b,e   Vacherot, Francis ^a,b  

^a UNIVERSITÉ PARIS EST CRÉTEIL   (France)

^b INSERM U955   (France)

^c CNRS   (France)

^d INSTITUT GUSTAVE ROUSSY   (France)

^e HENRI MONDOR HOSPITAL   (France)

^f UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

Androgen receptor; N6L; NPM1; Phosphorylated NPM1; Prostate cancer

Indexed keywords

ANDROGEN RECEPTOR; ANTINEOPLASTIC AGENT; DOCETAXEL; N6L; NUCLEOPHOSMIN; THREONINE; UNCLASSIFIED DRUG; AR PROTEIN, HUMAN; N6L PEPTIDE; NUCLEAR PROTEIN; NUCLEOPROTEIN; PEPTIDE; PROTEIN BINDING; TAXOID;

22RV1 CELL LINE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CANCER HORMONE THERAPY; CANCER INHIBITION; CASTRATION RESISTANT PROSTATE CANCER; CELL NUCLEUS; CONTROLLED STUDY; DU145 CELL LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LNCAP CELL LINE; MALE; MOUSE; NONHUMAN; NUCLEOPLASM; PC3 CELL LINE; PROSTATE CANCER CELL LINE; PROSTATE CARCINOMA; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; DRUG SCREENING; METABOLISM; NUDE MOUSE; PATHOLOGY; PHOSPHORYLATION; PROSTATE TUMOR; TUMOR CELL LINE; TUMOR VOLUME;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; HUMANS; MALE; MICE, NUDE; NUCLEAR PROTEINS; NUCLEOPROTEINS; PEPTIDES; PHOSPHORYLATION; PROSTATIC NEOPLASMS; PROSTATIC NEOPLASMS, CASTRATION-RESISTANT; PROTEIN BINDING; RECEPTORS, ANDROGEN; TAXOIDS; THREONINE; TUMOR BURDEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84983279655     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.8043     Document Type: Article

References (50)

1. Center MM, Jemal A, Lortet-Tieulent J, Ward E, Ferlay J, Brawley O, Bray F. International variation in prostate cancer incidence and mortality rates. Eur Urol. 2012; 61:1079-1092.
2. Petrylak DP, Tangen CM, Hussain MH, Lara PN, Jr., Jones JA, Taplin ME, Burch PA, Berry D, Moinpour C, Kohli M, Benson MC, Small EJ, Raghavan D, Crawford ED. Docetaxel and estramustine compared with mitoxantrone and prednisone for advanced refractory prostate cancer. N Engl J Med. 2004; 351:1513-1520.
3. Tannock IF, de Wit R, Berry WR, Horti J, Pluzanska A, Chi KN, Oudard S, Theodore C, James ND, Turesson I, Rosenthal MA, Eisenberger MA. Docetaxel plus prednisone or mitoxantrone plus prednisone for advanced prostate cancer. N Engl J Med. 2004; 351:1502-1512.
4. Machiels JP, Mazzeo F, Clausse M, Filleul B, Marcelis L, Honhon B, D'Hondt L, Dopchie C, Verschaeve V, Duck L, Verhoeven D, Jousten P, Bonny MA, Moxhon AM, Tombal B, Kerger J. Prospective randomized study comparing docetaxel, estramustine, and prednisone with docetaxel and prednisone in metastatic hormone-refractory prostate cancer. J Clin Oncol. 2008; 26:5261-5268.
5. Chen CD, Welsbie DS, Tran C, Baek SH, Chen R, Vessella R, Rosenfeld MG, Sawyers CL. Molecular determinants of resistance to antiandrogen therapy. Nat Med. 2004; 10:33-39.
6. Attar RM, Takimoto CH, Gottardis MM. Castrationresistant prostate cancer: locking up the molecular escape routes. Clin Cancer Res. 2009; 15:3251-3255.
7. Scher HI, Fizazi K, Saad F, Taplin ME, Sternberg CN, Miller K, de Wit R, Mulders P, Chi KN, Shore ND, Armstrong AJ, Flaig TW, Flechon A, Mainwaring P, Fleming M, Hainsworth JD, et al. Increased survival with enzalutamide in prostate cancer after chemotherapy. N Engl J Med. 2012; 367:1187-1197.
8. de Bono JS, Logothetis CJ, Molina A, Fizazi K, North S, Chu L, Chi KN, Jones RJ, Goodman OB, Jr., Saad F, Staffurth JN, Mainwaring P, Harland S, Flaig TW, Hutson TE, Cheng T, et al. Abiraterone and increased survival in metastatic prostate cancer. N Engl J Med. 2011; 364:1995-2005.
9. Ryan CJ, Smith MR, de Bono JS, Molina A, Logothetis CJ, de Souza P, Fizazi K, Mainwaring P, Piulats JM, Ng S, Carles J, Mulders PF, Basch E, Small EJ, Saad F, Schrijvers D, et al. Abiraterone in metastatic prostate cancer without previous chemotherapy. N Engl J Med. 2013; 368:138-148.
10. de Bono JS, Oudard S, Ozguroglu M, Hansen S, Machiels JP, Kocak I, Gravis G, Bodrogi I, Mackenzie MJ, Shen L, Roessner M, Gupta S, Sartor AO. Prednisone plus cabazitaxel or mitoxantrone for metastatic castrationresistant prostate cancer progressing after docetaxel treatment: a randomised open-label trial. Lancet. 2010; 376:1147-1154.
11. KantoffPW, Higano CS, Shore ND, Berger ER, Small EJ, Penson DF, Redfern CH, Ferrari AC, Dreicer R, Sims RB, Xu Y, Frohlich MW, Schellhammer PF. Sipuleucel-T immunotherapy for castration-resistant prostate cancer. N Engl J Med. 2010; 363:411-422.
12. Parker C, Nilsson S, Heinrich D, Helle SI, O'Sullivan JM, Fossa SD, Chodacki A, Wiechno P, Logue J, Seke M, Widmark A, Johannessen DC, Hoskin P, Bottomley D, James ND, Solberg A, et al. Alpha emitter radium-223 and survival in metastatic prostate cancer. N Engl J Med. 2013; 369:213-223.
13. Savkur RS, Olson MO. Preferential cleavage in preribosomal RNA byprotein B23 endoribonuclease. Nucleic Acids Res. 1998; 26:4508-4515.
14. 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; 276:21529-21537.
15. 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.
16. Szebeni A, Mehrotra B, Baumann A, Adam SA, Wingfield PT, Olson MO. Nucleolar protein B23 stimulates nuclear import of the HIV-1 Rev protein and NLS-conjugated albumin. Biochemistry. 1997; 36:3941-3949.
17. Feuerstein N, Chan PK, Mond JJ. Identification of numatrin, the nuclear matrix protein associated with induction of mitogenesis, as the nucleolar protein B23. Implication for the role of the nucleolus in early transduction of mitogenic signals. J Biol Chem. 1988; 263:10608-10612.
18. Chan WY, Liu QR, Borjigin J, Busch H, Rennert OM, Tease LA, Chan PK. Characterization of the cDNA encoding human nucleophosmin and studies of its role in normal and abnormal growth. Biochemistry. 1989; 28:1033-1039.
19. Subong EN, Shue MJ, Epstein JI, Briggman JV, Chan PK, Partin AW. Monoclonal antibody to prostate cancer nuclear matrix protein (PRO:4-216) recognizes nucleophosmin/B23. Prostate. 1999; 39:298-304.
20. 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.
21. Shields LB, Gercel-Taylor C, Yashar CM, Wan TC, Katsanis WA, Spinnato JA, Taylor DD. Induction of immune responses to ovarian tumor antigens by multiparity. J Soc Gynecol Investig. 1997; 4:298-304.
22. 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.
23. Yeh CW, Huang SS, Lee RP, Yung BY. Ras-dependent recruitment of c-Myc for transcriptional activation of nucleophosmin/B23 in highly malignant U1 bladder cancer cells. Mol Pharmacol. 2006; 70:1443-1453.
24. 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.
25. Coutinho-Camillo CM, Lourenco SV, Nishimoto IN, Kowalski LP, Soares FA. Nucleophosmin, p53, and Ki-67 expression patterns on an oral squamous cell carcinoma tissue microarray. Hum Pathol. 2010; 41:1079-1086.
26. 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 tumors. Biochem Biophys Res Commun. 2010; 397:499-504.
27. Pianta A, Puppin C, Passon N, Franzoni A, Romanello M, Tell G, Di Loreto C, Bulotta S, Russo D, Damante G. Nucleophosmin delocalization in thyroid tumour cells. Endocr Pathol. 2011; 22:18-23.
28. Okuwaki M. The structure and functions of NPM1/Nucleophsmin/B23, a multifunctional nucleolar acidic protein. J Biochem. 2008; 143:441-448.
29. Shinmura K, Tarapore P, Tokuyama Y, George KR, Fukasawa K. Characterization of centrosomal association of nucleophosmin/B23 linked to Crm1 activity. FEBS Lett. 2005; 579:6621-6634.
30. Okuwaki M, Tsujimoto M, Nagata K. The RNA binding activity of a ribosome biogenesis factor, nucleophosmin/B23, is modulated by phosphorylation with a cell cycledependent kinase and by association with its subtype. Mol Biol Cell. 2002; 13:2016-2030.
31. 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, et al. A simple approach to cancer therapy afforded by multivalent pseudopeptides that target cell-surface nucleoproteins. Cancer Res. 2011; 71:3296-3305.
32. Leotoing L, Meunier L, Manin M, Mauduit C, Decaussin M, Verrijdt G, Claessens F, Benahmed M, Veyssiere 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.
33. Tarapore P, Shinmura K, Suzuki H, Tokuyama Y, Kim SH, Mayeda A, Fukasawa K. Thr199 phosphorylation targets nucleophosmin to nuclear speckles and represses premRNA processing. FEBS Lett. 2006; 580:399-409.
34. Negi SS, Olson MO. Effects of interphase and mitotic phosphorylation on the mobility and location of nucleolar protein B23. J Cell Sci. 2006; 119:3676-3685.
35. Terry S, Maille P, Baaddi H, Kheuang L, Soyeux P, Nicolaiew N, Ceraline J, Firlej V, Beltran H, Allory Y, de la Taille A, Vacherot F. Cross modulation between the androgen receptor axis and protocadherin-PC in mediating neuroendocrine transdifferentiation and therapeutic resistance of prostate cancer. Neoplasia. 2013; 15:761-772.
36. Loberg RD, St John LN, Day LL, Neeley CK, Pienta KJ. Development of the VCaP androgen-independent model of prostate cancer. Urol Oncol. 2006; 24:161-168.
37. Bocker T, Bittinger A, Wieland W, Buettner R, Fauser G, Hofstaedter F, RuschoffJ. In vitro and ex vivo expression of nucleolar proteins B23 and p120 in benign and malignant epithelial lesions of the prostate. Mod Pathol. 1995; 8:226-231.
38. Zhou Y, Shen J, Xia L, Wang Y. Estrogen mediated expression of nucleophosmin 1 in human endometrial carcinoma clinical stages through estrogen receptor-alpha signaling. Cancer Cell Int. 2014; 14:540.
39. Tawfic S, Goueli SA, Olson MO, Ahmed K. Androgenic regulation of the expression and phosphorylation of prostatic nucleolar protein B23. Cell Mol Biol Res. 1993; 39:43-51.
40. Tawfic S, Olson MO, Ahmed K. Role of protein phosphorylation in post-translational regulation of protein B23 during programmed cell death in the prostate gland. J Biol Chem. 1995; 270:21009-21015.
41. Abankwa D, Millard SM, Martel N, Choong CS, Yang M, Butler LM, Buchanan G, Tilley WD, Ueki N, Hayman MJ, Leong GM. Ski-interacting protein (SKIP) interacts with androgen receptor in the nucleus and modulates androgendependent transcription. BMC Biochem. 2013; 14:10.
42. Kurki S, Peltonen K, Laiho M. Nucleophosmin, HDM2 and p53: players in UV damage incited nucleolar stress response. Cell Cycle. 2004; 3:976-979.
43. 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.
44. Jiang PS, Yung BY. Down-regulation of nucleophosmin/B23 mRNA delays the entry of cells into mitosis. Biochem Biophys Res Commun. 1999; 257:865-870.
45. Loubeau G, Boudra R, Maquaire S, Lours-Calet C, Beaudoin C, Verrelle P, Morel L. NPM1 Silencing Reduces Tumour Growth and MAPK Signalling in Prostate Cancer Cells. PLoS One. 2014; 9:e96293.
46. 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.
47. Terry S, Beltran H. The many faces of neuroendocrine differentiation in prostate cancer progression. Front Oncol. 2014; 4:60.
48. Puhr M, Hoefer J, Schafer G, Erb HH, Oh SJ, Klocker H, Heidegger I, Neuwirt H, Culig Z. Epithelial-tomesenchymal transition leads to docetaxel resistance in prostate cancer and is mediated by reduced expression of miR-200c and miR-205. Am J Pathol. 2012; 181:2188-2201.
49. van Zoggel H, Carpentier G, Dos Santos C, Hamma-Kourbali Y, Courty J, Amiche M, Delbe J. Antitumor, angiostatic activities of the antimicrobial peptide dermaseptin B2. PLoS One. 2012; 7:e44351.
50. Destouches D, El Khoury D, Hamma-Kourbali Y, Krust B, Albanese P, Katsoris P, Guichard G, Briand JP, Courty J, Hovanessian AG. Suppression of tumor growth and angiogenesis by a specific antagonist of the cell-surface expressed nucleolin. PLoS One. 2008; 3:e2518.