Regulation of subcellular distribution and oncogenic potential of nucleophosmin by plakoglobin

Oncogenesis

Volumn 1, Issue 3, 2012, Pages

  Lam, L ^a   Aktary, Z ^a   Bishay, M ^a   Werkman, C ^a   Kuo, C Y ^a   Heacock, M ^a   Srivastava, N ^a   MacKey, J R ^a   Pasdar, M ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

metastasis suppressor; NPM; plakoglobin; tumor suppressor

Indexed keywords

NUCLEOPHOSMIN; PLAKOGLOBIN; SHORT HAIRPIN RNA;

ARTICLE; BREAST CARCINOMA; CANCER CELL; CARCINOGENESIS; CELL GROWTH; CELL INVASION; CELLULAR DISTRIBUTION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; FEMALE; GENE SILENCING; GENETIC TRANSFECTION; GROWTH RATE; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; METASTASIS; NUCLEOLUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION;

EID: 84868299167     PISSN: None     EISSN: 21579024     Source Type: Journal    
DOI: 10.1038/oncsis.2012.4     Document Type: Article

References (70)

1. Yung BY. Oncogenic role of nucleophosmin/B23. Chang Gung Med J 2007; 30: 285-293. (Pubitemid 47529095)
2. Skaar TC, Prasad SC, Sharareh S, Lippman ME, Brü nner N, Clarke R. Twodimensional gel electrophoresis analyses identify nucleophosmin as an estrogen regulated protein associated with acquired estrogen-independence in human breast cancer cells. J Steroid Biochem Mol Biol 1998; 67: 391-402. (Pubitemid 29049412)
3. Grisendi S, Mecucci C, Falini B, Pandolfi PP. Nucleophosmin and cancer. Nat Rev Cancer 2006; 6: 493-505. (Pubitemid 43980539)
4. Kikuta K, Tochigi N, Shimoda T, Yabe H, Morioka H, Toyama Y et al. Nucleophosmin as a candidate prognostic biomarker of Ewing's sarcoma revealed by proteomics. Clin Cancer Res 2009; 15: 2885-2894.
5. 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.
6. Colombo E, Bonetti P, Lazzerini Denchi E, Martinelli P, Zamponi R, Marine JC et al. Nucleophosmin is required for DNA integrity and p19Arf protein stability. Mol Cell Biol 2005; 25: 8874-8886. (Pubitemid 41429079)
7. Li Z, Hann SR. The Myc-nucleophosmin-ARF network: a complex web unveiled. Cell Cycle 2009; 8: 2703-2707.
8. Gjerset RA. DNA damage, p14ARF, nucleophosmin (NPM/B23), and cancer. J Mol Histol 2006; 37: 239-251. (Pubitemid 44795627)
9. Yada M, Hatakeyama S, Kamura T, Nishiyama M, Tsunematsu R, Imaki H et al. degradation of c-Myc is mediated by the F-box protein Fbw7. EMBO J 2004; 23: 2116-2125. (Pubitemid 38737738)
10. Bonetti 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. (Pubitemid 352008617)
11. Mariano AR, Colombo E, Luzi L, Martinelli P, Volorio S, Bernard L et al. Cytoplasmic localization of NPM in myeloid leukemias is dictated by gain-of-function mutations that create a functional nuclear export signal. Oncogene 2006; 5: 4376-4380. (Pubitemid 44100508)
12. Delva E, Tucker DK, Kowalczyk AP. The desmosome. Cold Spring Harb Perspect Biol 2009; 1: a002543.
13. Zhurinsky J, Shtutman M, Ben-Ze'ev A. Differential mechanisms of LEF/TCF familydependent transcriptional activation by beta-catenin and plakoglobin. Mol Cell Biol 2000; 20: 4238-4252. (Pubitemid 30346619)
14. Chidgey M, Dawson C. Desmosomes: a role in cancer? Br J Cancer 2007; 96: 1783-1787. (Pubitemid 46912021)
15. Cadigan KM, Peifer M. Wnt signaling from development to disease: insights from model systems. Cold Spring Harb Perspect Biol 2009; 1: a002881.
16. Roarty K, Rosen JM. Wnt and mammary stem cells: hormones cannot fly wingless. Curr Opin Pharmacol 2010; 10: 643-649.
17. Simcha I, Geiger B, Yehuda-Levenberg S, Salomon D, Ben-Ze'ev A. Suppression of tumorigenicity by plakoglobin: an augmenting effect of N-cadherin. J Cell Biol 1996; 133: 199-209.
18. Parker HR, Li Z, Sheinin H, Lauzon G, Pasdar M. Plakoglobin induces desmosome formation and epidermoid phenotype in N-cadherin-expressing squamous carcinoma cells deficient in plakoglobin and E-cadherin. Cell Motil Cytoskeleton 1998; 40: 87-100. (Pubitemid 28225544)
19. Rieger-Christ KM, Ng L, Hanley RS, Durrani O, Ma H, Yee AS et al. Restoration of plakoglobin expression in bladder carcinoma cell lines suppresses cell migration and tumorigenic potential. Br J Cancer 2005; 92: 2153-2159. (Pubitemid 40966250)
20. Gastaldi T, Bonvini P, Sartori F, Marrone A, Iolascon A, Rosolen A. Plakoglobin is differentially expressed in alveolar and embryonal rhabdomyosarcoma and is regulated by DNA methylation and histone acetylation. Carcinogenesis 2006; 27: 1758-1767. (Pubitemid 44307828)
21. Li L, Chapman K, Hu X, Wong A, Pasdar M. Modulation of the oncogenic potential of beta-catenin by the subcellular distribution of plakoglobin. Mol Carcinog 2007; 46: 824-838. (Pubitemid 47554279)
22. Aktary Z, Chapman K, Lam L, Lo A, Ji C, Graham K et al. Plakoglobin interacts with and increases the protein levels of metastasis suppressor Nm23-H2 and regulates the expression of Nm23-H1. Oncogene 2010; 29: 2118-2129.
23. Li Z, Gallin WJ, Lauzon G, Pasdar M. L-CAM expression induces fibroblastepidermoid transition in squamous carcinoma cells and down-regulates the endogenous N-cadherin. J Cell Sci 1998; 111: 1005-1019. (Pubitemid 28196083)
24. Hakimelahi S, Parker HR, Gilchrist AJ, Barry M, Li Z, Bleackley RC et al. Plakoglobin regulates the expression of the anti-apoptotic protein BCL-2. J Biol Chem 2000; 275: 10905-10911. (Pubitemid 30212725)
25. Ji C, Li L, Gebre M, Pasdar M, Li L. Identification and quantification of differentially expressed proteins in E-cadherin deficient SCC9 cells and SCC9 transfectants expressing E-cadherin by dimethyl isotope labeling, LC-MALDI MS and MS/MS. J Proteome Res 2005; 4: 1419-1426. (Pubitemid 41208700)
26. Aktary Z, Pasdar M. Plakoglobin: role in tumorigenesis and metastasis. Int J Cell Bio (in press).
27. Oelschlaegel U, Koch S, Mohr B, Schaich M, Falini B, Ehninger G et al. flow cytometric detection of aberrant cytoplasmic localization of nucleophosmin (NPMc) indicating mutant NPM1 gene in acute myeloid leukemia. Leukemia 2010; 24: 1813-1816.
28. Brady SN, Maggi Jr LB, Winkeler CL, Toso EA, Gwinn AS, Pelletier CL. Nucleophosmin protein expression level, but not threonine 198 phosphorylation, is essential in growth and proliferation. Oncogene 2009; 28: 3209-3220.
29. Di Fiore PP. Playing both sides: nucleophosmin between tumor suppression and oncogenesis. J Cell Biol 2008; 182: 7-9. (Pubitemid 352008614)
30. Chan WY, Liu QR, Borjigin J, Busch H, Rennert OM, Tease LA et al. Characterization of the cDNA encoding human nucleophosmin and studies of its role in normal and abnormal growth. Biochemistry 1989; 28: 1033-1039. (Pubitemid 19058676)
31. Lim MJ, Wang XW. Nucleophosmin and human cancer. Cancer Detect Prev 2006; 30: 481-490. (Pubitemid 44834564)
32. 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.
33. 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. (Pubitemid 29244505)
34. Kuo ML, den Besten W, Bertwistle D, Roussel MF, Sherr CJ. N-terminal polyubiquitination and degradation of the Arf tumor suppressor. Genes Dev 2004; 18: 1862-1874. (Pubitemid 39025096)
35. Sportoletti P, Grisendi S, Majid SM, Cheng K, Clohessy JG, Viale A et al. Npm1 is a haploinsufficient suppressor of myeloid and lymphoid malignancies in the mouse. Blood 2008; 111: 3859-3862.
36. 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. (Pubitemid 34752440)
37. Kurki S, Peltonen K, Latonen L, Kiviharju TM, Ojala PM, Meek D et al. Nucleolar protein NPM interacts with HDM2 and protects tumor suppressor protein p53 from HDM2-mediated degradation. Cancer Cell 2004; 5: 465-475. (Pubitemid 38610248)
38. 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. (Pubitemid 38496150)
39. Bertwistle D, Sugimoto M, Sherr CJ. Physical and functional interactions of the Arf tumor suppressor protein with nucleophosmin/B23. Mol Cell Biol 2004; 24: 985-996. (Pubitemid 38112164)
40. Brady SN, Yu Y, Maggi Jr LB, Weber JD. ARF impedes NPM/B23 shuttling in an Mdm2-sensitive tumor suppressor pathway. Mol Cell Biol 2004; 24: 9327-9338. (Pubitemid 39391671)
41. Itahana K, Bhat KP, Jin A, Itahana Y, Hawke D, Kobayashi R et al. Tumor suppressor ARF degrades B23, a nucleolar protein involved in ribosome biogenesis and cell proliferation. Mol Cell 2003; 12: 1151-1164. (Pubitemid 37487925)
42. Falini B, Bolli N, Liso A, Martelli MP, Manucci R, Pileri S et al. Altered nucleophosmin transport in acute myeloid leukaemia with mutated NPM1: molecular basis and clinical implications. Leukemia 2009; 23: 1731-1743.
43. 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.
44. Dhar SK, St Clair DK. Nucleophosmin blocks mitochondrial localization of p53 and apoptosis. J Biol Chem 2009; 284: 16409-16418.
45. Kim CK, Nguyen TL, Lee SB, Park SB, Lee KH, Cho SW et al. Akt2 and nucleophosmin/B23 function as an oncogenic unit in human lung cancer cells. Exp Cell Res 2011; 317: 966-975.
46. Qin FX, Shao HY, Chen XC, Tan S, Zhang HJ, Miao ZY et al. Knockdown of NPM1 by RNA interference inhibits cells proliferation and induces apoptosis in leukemic cell line. Int J Med Sci 2011; 8: 287-294.
47. Kofron M, Heasman J, Lang SA, Wylie CC. Plakoglobin is required for maintenance of the cortical actin skeleton in early Xenopus embryos and for cdc42-mediated wound healing. J Cell Biol 2002; 158: 695-608.
48. Yin T, Getsios S, Caldelari R, Kowalczyk AP, Mü ller EJ, Jones JC et al. suppresses keratinocyte motility through both cell-cell adhesion-dependent and-independent mechanisms. Proc Natl Acad Sci USA 2005; 102: 5420-5425. (Pubitemid 40530273)
49. Shafiei F, Rahnama F, Pawella L, Mitchell MD, Gluckman PD, Lobie PE. DNMT3A and DNMT3B mediate autocrine hGH repression of plakoglobin gene transcription and consequent phenotypic conversion of mammary carcinoma cells. Oncogene 2008; 27: 2602-2612. (Pubitemid 351550882)
50. Todoroviæ V, Desai BV, Patterson MJ, Amargo EV, Dubash AD, Yin T et al. regulates cell motility through Rho-and fibronectin-dependent Src signaling. J Cell Sci 2010; 123: 3576-3586.
51. Bolli N, Nicoletti I, De Marco MF, Bigerna B, Pucciarini A, Mannucci R et al. Born to be exported: COOH-terminal nuclear export signals of different strength ensure cytoplasmic accumulation of nucleophosmin leukemic mutants. Cancer Res 2007; 67: 6230-6237. (Pubitemid 47037504)
52. Falini B, Sportoletti P, Martelli MP. Acute myeloid leukemia with mutated NPM1: diagnosis, prognosis and therapeutic perspectives. Curr Opin Oncol 2009; 21: 573-581.
53. Luo J, Qi C, Xu W, Kamel-Reid S, Brandwein J, Chang H. Cytoplasmic expression of nucleophosmin accuratety predicts mutation in the nucleophosmin gene in patients with acute myeloid leukemia and normal karyotype. Am J Clin Pathol 2010; 133: 34-40.
54. Jeong EG, Lee SH, Yoo NJ, Lee SH. Absence of nucleophosmin 1 (NPM1) gene mutations in common solid cancers. APMIS 2007; 115: 341-346. (Pubitemid 46743947)
55. Shao HY, Miao ZY, Hui-Chen, Qin FX, Chen XC, Tan S et al. Nucleophosmin gene mutations promote NIH3T3 cell migration and invasion through CXCR4 and MMPs. Exp Mol Pathol 2011; 90: 38-44.
56. 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.
57. 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. (Pubitemid 26053395)
58. Yun JP, Miao J, Chen GG, Tian QH, Zhang CQ, Xiang J et al. expression of nucleophosmin/B23 in hepatocellular carcinoma and correlation with clinicopathological parameters. Br J Cancer 2007; 96: 477-484. (Pubitemid 46215220)
59. Tsui KH, Juang HH, Lee TH, Chang PL, Chen CL, Yung BY. Association of nucleophosmin/B23 with bladder cancer recurrence based on immunohistochemical assessment in clinical samples. Acta Pharmacol Sin 2008; 29: 364-370. (Pubitemid 351316984)
60. Pianta A, Puppin C, Passon N, Franzoni A, Romanello M, Tell G et al. Nucleophosmin delocalization in thyroid tumour cells. Endocr Pathol 2011; 22: 18-23.
61. Coutinho-Camillo CM, Lourenço 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.
62. Pozuelo-Rubio M. Proteomic and biochemical analysis of 14-3-3-binding proteins during C2-ceramide-induced apoptosis. FEBS J 2010; 277: 3321-3342.
63. Kerr LE, Birse-Archbold JL, Short DM, McGregor AL, Heron I, Macdonald DC et al. Nucleophosmin is a novel Bax chaperone that regulates apoptotic cell death. Oncogene 2007; 26: 2554-2562. (Pubitemid 46632004)
64. Chartier NT, Oddou CI, Lainé MG, Ducarouge B, Marie CA, Block MR et al. Cyclindependent kinase 2/cyclin E complex is involved in p120 catenin (p120ctn)-dependent cell growth control: a new role for p120ctn in cancer. Cancer Res 2007; 67: 9781-9790. (Pubitemid 47621225)
65. Chang TP, Yu SL, Lin SY, Hsiao YJ, Chang GC, Yang PC et al. Tumor suppressor HLJ1 binds and functionally alters nucleophosmin via activating enhancer binding protein 2alpha complex formation. Cancer Res 2010; 70: 1656-1667.
66. Krause A, Hoffmann I. Polo-like kinase 2-dependent phosphorylation of NPM/B23 on serine 4 triggers centriole duplication. PLoS One 2010; 5: e9849.
67. Karhemo PR, Rivinoja A, Lundin J, Hyvönen M, Chernenko A, Lammi J et al. An extensive tumor array analysis supports tumor suppressive role for nucleophosmin in breast cancer. Am J Pathol 2011; 179: 1004-1014.
68. Lam L, Hu X, Aktary Z, Andrews DW, Pasdar M. Tamoxifen and ICI 182,780 increase Bcl-2 levels and inhibit growth of breast carcinoma cells by modulating PI3K/AKT, ERK and IGF-1R pathways independent of ERalpha. Breast Cancer Res Treat 2009; 118: 605-621.
69. Asgarian N, Hu X, Aktary Z, Chapman KA, Lam L, Chibbar R et al. Learning to predict relapse in invasive ductal carcinomas based on the subcellular localization of junctional proteins. Breast Cancer Res Treat 2010; 121: 527-538.
70. Pasdar M, Nelson WJ. Kinetics of desmosome assembly in Madin-Darby canine kidney epithelial cells: temporal and spatial regulation of desmoplakin organization and stabilization upon cell-cell contact. II. Morphological analysis. J Cell Biol 1988; 106: 687-695. (Pubitemid 18089969)