NKX3.1 stabilizes p53, inhibits AKT activation, and blocks prostate cancer initiation caused by PTEN loss

Cancer Cell

Volumn 9, Issue 5, 2006, Pages 367-378

  Lei, Qunying ^a   Jiao, Jing ^a   Xin, Li ^a   Chang, Chun Ju ^a   Wang, Shunyou ^a   Gao, Jing ^a   Gleave, Martin E ^b   Witte, Owen N ^a   Liu, Xin ^a   Wu, Hong ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VANCOUVER GENERAL HOSPITAL   (Canada)

Author keywords

CELLCYCLE; DNA; HUMDISEASE

Indexed keywords

ANDROGEN RECEPTOR; HISTONE DEACETYLASE 1; HOMEODOMAIN PROTEIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; PROTEIN MDM2; PROTEIN NKX3.1; PROTEIN P53; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ACETYLATION; ARTICLE; CARCINOGENESIS; CELL CYCLE; CELL DEATH; CELL PROLIFERATION; ENZYME ACTIVATION; EPITHELIUM; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; MOUSE; NONHUMAN; NULL CELL; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; WILD TYPE;

MURINAE;

EID: 33646342738     PISSN: 15356108     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ccr.2006.03.031     Document Type: Article

References (53)

1. Abdulkadir S.A. Mechanisms of prostate tumorigenesis: Roles for transcription factors Nkx3.1 and Egr1. Ann. NY Acad. Sci. 1059 (2005) 33-40 10.1196/annals.1339.018
2. Abdulkadir S.A., Magee J.A., Peters T.J., Kaleem Z., Naughton C.K., Humphrey P.A., and Milbrandt J. Conditional loss of Nkx3.1 in adult mice induces prostatic intraepithelial neoplasia. Mol. Cell. Biol. 22 (2002) 1495-1503
3. Asatiani E., and Gelmann E.P. Targeted therapies for prostate cancer. Expert Opin. Ther. Targets 9 (2005) 283-298
4. Asatiani E., Huang W.-X., Wang A., Rodriguez Ortner E., Cavalli L.R., Haddad B.R., and Gelmann E.P. Deletion, methylation, and expression of the NKX3.1 suppressor gene in primary human prostate cancer. Cancer Res. 65 (2005) 1164-1173 10.1158/0008-5472.CAN-04-2688
5. Baron S., Manin M., Beaudoin C., Leotoing L., Communal Y., Veyssiere G., and Morel L. Androgen receptor mediates non-genomic activation of phosphatidylinositol 3-OH kinase in androgen-sensitive epithelial cells. J. Biol. Chem. 279 (2004) 14579-14586
6. Bhatia-Gaur R., Donjacour A.A., Sciavolino P.J., Kim M., Desai N., Young P., Norton C.R., Gridley T., Cardiff R.D., Cunha G.R., et al. Roles for Nkx3.1 in prostate development and cancer. Genes Dev. 13 (1999) 966-977
7. Bieberich C.J., Fujita K., He W.W., and Jay G. Prostate-specific and androgen-dependent expression of a novel homeobox gene. J. Biol. Chem. 271 (1996) 31779-31782
8. Bowen C., Bubendorf L., Voeller H.J., Slack R., Willi N., Sauter G., Gasser T.C., Koivisto P., Lack E.E., Kononen J., et al. Loss of NKX3.1 expression in human prostate cancers correlates with tumor progression. Cancer Res. 60 (2000) 6111-6115
9. Brooks C.L., and Gu W. Ubiquitination, phosphorylation and acetylation: the molecular basis for p53 regulation. Curr. Opin. Cell Biol. 15 (2003) 164-171
10. Chen C.D., Welsbie D.S., Tran C., Baek S.H., Chen R., Vessella R., Rosenfeld M.G., and Sawyers C.L. Molecular determinants of resistance to antiandrogen therapy. Nat. Med. 10 (2004) 33-39
11. Chen Z., Trotman L.C., Shaffer D., Lin H.K., Dotan Z.A., Niki M., Koutcher J.A., Scher H.I., Ludwig T., Gerald W., et al. Crucial role of p53-dependent cellular senescence in suppression of Pten-deficient tumorigenesis. Nature 436 (2005) 725-730
12. Cunha G.R., and Donjacour A. Mesenchymal-epithelial interactions: technical considerations. Prog. Clin. Biol. Res. 239 (1987) 273-282
13. Dahia P.L. PTEN, a unique tumor suppressor gene. Endocr. Relat. Cancer 7 (2000) 115-129
14. DeMarzo A.M., Nelson W.G., Isaacs W.B., and Epstein J.I. Pathological and molecular aspects of prostate cancer. Lancet 361 (2003) 955-964
15. Di Cristofano A., De Acetis M., Koff A., Cordon-Cardo C., and Pandolfi P.P. Pten and p27KIP1 cooperate in prostate cancer tumor suppression in the mouse. Nat. Genet. 27 (2001) 222-224
16. Freeman D.J., Li A.G., Wei G., Li H.H., Kertesz N., Lesche R., Whale A.D., Martinez-Diaz H., Rozengurt N., Cardiff R.D., et al. PTEN tumor suppressor regulates p53 protein levels and activity through phosphatase-dependent and -independent mechanisms. Cancer Cell 3 (2003) 117-130
17. Gregorakis A.K., Holmes E.H., and Murphy G.P. Prostate-specific membrane antigen: current and future utility. Semin. Urol. Oncol. 16 (1998) 2-12
18. Hanahan D., and Weinberg R.A. The hallmarks of cancer. Cell 100 (2000) 57-70
19. He W.W., Sciavolino P.J., Wing J., Augustus M., Hudson P., Meissner P.S., Curtis R.T., Shell B.K., Bostwick D.G., Tindall D.J., et al. A novel human prostate-specific, androgen-regulated homeobox gene (NKX3.1) that maps to 8p21, a region frequently deleted in prostate cancer. Genomics 43 (1997) 69-77
20. Ito A., Kawaguchi Y., Lai C.H., Kovacs J.J., Higashimoto Y., Appella E., and Yao T.P. MDM2-HDAC1-mediated deacetylation of p53 is required for its degradation. EMBO J. 21 (2002) 6236-6245
21. Jones S.N., Roe A.E., Donehower L.A., and Bradley A. Rescue of embryonic lethality in Mdm2-deficient mice by absence of p53. Nature 378 (1995) 206-208
22. Kim M.J., Bhatia-Gaur R., Banach-Petrosky W.A., Desai N., Wang Y., Hayward S.W., Cunha G.R., Cardiff R.D., Shen M.M., and Abate-Shen C. Nkx3.1 mutant mice recapitulate early stages of prostate carcinogenesis. Cancer Res. 62 (2002) 2999-3004
23. Kim M.J., Cardiff R.D., Desai N., Banach-Petrosky W.A., Parsons R., Shen M.M., and Abate-Shen C. Cooperativity of Nkx3.1 and Pten loss of function in a mouse model of prostate carcinogenesis. Proc. Natl. Acad. Sci. USA 99 (2002) 2884-2889
24. Kobet E., Zeng X., Zhu Y., Keller D., and Lu H. MDM2 inhibits p300-mediated p53 acetylation and activation by forming a ternary complex with the two proteins. Proc. Natl. Acad. Sci. USA 97 (2000) 12547-12552
25. Korkmaz C.G., Korkmaz K.S., Manola J., Xi Z., Risberg B., Danielsen H., Kung J., Sellers W.R., Loda M., and Saatcioglu F. Analysis of androgen regulated homeobox gene NKX3.1 during prostate carcinogenesis. J. Urol. 172 (2004) 1134-1139
26. Lois C., Hong E.J., Pease S., Brown E.J., and Baltimore D. Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science 295 (2002) 868-872
27. Ma X., Ziel-van der Made A.C., Autar B., van der Korput H.A., Vermeij M., van Duijn P., Cleutjens K.B., de Krijger R., Krimpenfort P., Berns A., et al. Targeted biallelic inactivation of Pten in the mouse prostate leads to prostate cancer accompanied by increased epithelial cell proliferation but not by reduced apoptosis. Cancer Res. 65 (2005) 5730-5739
28. Maehama T., Taylor G.S., and Dixon J.E. PTEN and myotubularin: novel phosphoinositide phosphatases. Annu. Rev. Biochem. 70 (2001) 247-279
29. Magee J.A., Abdulkadir S.A., and Milbrandt J. Haploinsufficiency at the Nkx3.1 locus. A paradigm for stochastic, dosage-sensitive gene regulation during tumor initiation. Cancer Cell 3 (2003) 273-283
30. Mayo L.D., and Donner D.B. A phosphatidylinositol 3-kinase/Akt pathway promotes translocation of Mdm2 from the cytoplasm to the nucleus. Proc. Natl. Acad. Sci. USA 98 (2001) 11598-11603
31. McDavid K., Lee J., Fulton J.P., Tonita J., and Thompson T.D. Prostate cancer incidence and mortality rates and trends in the United States and Canada. Public Health Rep. 119 (2004) 174-186
32. Neshat M.S., Mellinghoff I.K., Tran C., Stiles B., Thomas G., Petersen R., Frost P., Gibbons J.J., Wu H., and Sawyers C.L. Enhanced sensitivity of PTEN-deficient tumors to inhibition of FRAP/mTOR. Proc. Natl. Acad. Sci. USA 98 (2001) 10314-10319
33. Ornstein D.K., Cinquanta M., Weiler S., Duray P.H., Emmert-Buck M.R., Vocke C.D., Linehan W.M., and Ferretti J.A. Expression studies and mutational analysis of the androgen regulated homeobox gene NKX3.1 in benign and malignant prostate epithelium. J. Urol. 165 (2001) 1329-1334
34. Ouyang X., DeWeese T.L., Nelson W.G., and Abate-Shen C. Loss-of-function of Nkx3.1 promotes increased oxidative damage in prostate carcinogenesis. Cancer Res. 65 (2005) 6773-6779
35. Parson W., Parsons T.J., Scheithauer R., and Holland M.M. Population data for 101 Austrian Caucasian mitochondrial DNA d-loop sequences: application of mtDNA sequence analysis to a forensic case. Int. J. Legal Med. 111 (1998) 124-132
36. Pfeifer A., Ikawa M., Dayn Y., and Verma I.M. Transgenesis by lentiviral vectors: lack of gene silencing in mammalian embryonic stem cells and preimplantation embryos. Proc. Natl. Acad. Sci. USA 99 (2002) 2140-2145
37. Plass C. Cancer epigenomics. Hum. Mol. Genet. 11 (2002) 2479-2488
38. Prescott J.L., Blok L., and Tindall D.J. Isolation and androgen regulation of the human homeobox cDNA, NKX3.1. Prostate 35 (1998) 71-80
39. Rocchi P., So A., Kojima S., Signaevsky M., Beraldi E., Fazli L., Hurtado-Coll A., Yamanaka K., and Gleave M. Heat shock protein 27 increases after androgen ablation and plays a cytoprotective role in hormone-refractory prostate cancer. Cancer Res. 64 (2004) 6595-6602
40. Schneider A., Brand T., Zweigerdt R., and Arnold H. Targeted disruption of the Nkx3.1 gene in mice results in morphogenetic defects of minor salivary glands: parallels to glandular duct morphogenesis in prostate. Mech. Dev. 95 (2000) 163-174
41. Sellers W., and Sawyers C. Somatic Genetics of Prostate Cancer: Oncogene and Tumor Suppressors (2002), Lippincott Williams & Wilkins, Philadelphia
42. Stanbrough M., Leav I., Kwan P.W., Bubley G.J., and Balk S.P. Prostatic intraepithelial neoplasia in mice expressing an androgen receptor transgene in prostate epithelium. Proc. Natl. Acad. Sci. USA 98 (2001) 10823-10828
43. Sun M., Yang L., Feldman R.I., Sun X.M., Bhalla K.N., Jove R., Nicosia S.V., and Cheng J.Q. Activation of phosphatidylinositol 3-kinase/Akt pathway by androgen through interaction of p85α, androgen receptor, and Src. J. Biol. Chem. 278 (2003) 42992-43000
44. Suzuki H., Freije D., Nusskern D.R., Okami K., Cairns P., Sidransky D., Isaacs W.B., and Bova G.S. Interfocal heterogeneity of PTEN/MMAC1 gene alterations in multiple metastatic prostate cancer tissues. Cancer Res. 58 (1998) 204-209
45. Tanaka M., Komuro I., Inagaki H., Jenkins N.A., Copeland N.G., and Izumo S. Nkx3.1, a murine homolog of Drosophila bagpipe, regulates epithelial ductal branching and proliferation of the prostate and palatine glands. Dev. Dyn. 219 (2000) 248-260
46. Thompson T.C., Southgate J., Kitchener G., and Land H. Multistage carcinogenesis induced by ras and myc oncogenes in a reconstituted organ. Cell 56 (1989) 917-930
47. Trotman L.C., Niki M., Dotan Z.A., Koutcher J.A., Di Cristofano A., Xiao A., Khoo A.S., Roy-Burman P., Greenberg N.M., Van Dyke T., et al. Pten dose dictates cancer progression in the prostate. PLoS Biol. 1 (2003) e59 10.1371/journal.pbio.0000059
48. Vivanco I., and Sawyers C.L. The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat. Rev. Cancer 2 (2002) 489-501
49. Voeller H.J., Augustus M., Madike V., Bova G.S., Carter K.C., and Gelmann E.P. Coding region of NKX3.1, a prostate-specific homeobox gene on 8p21, is not mutated in human prostate cancers. Cancer Res. 57 (1997) 4455-4459
50. Wang S., Gao J., Lei Q., Rozengurt N., Pritchard C., Jiao J., Thomas G.V., Li G., Roy-Burman P., Nelson P.S., et al. Prostate-specific deletion of the murine Pten tumor suppressor gene leads to metastatic prostate cancer. Cancer Cell 4 (2003) 209-221
51. Xin L., Ide H., Kim Y., Dubey P., and Witte O.N. In vivo regeneration of murine prostate from dissociated cell populations of postnatal epithelia and urogenital sinus mesenchyme. Proc. Natl. Acad. Sci. USA 100 Suppl 1 (2003) 11896-11903
52. Xin L., Lawson D.A., and Witte O.N. The Sca-1 cell surface marker enriches for a prostate-regenerating cell subpopulation that can initiate prostate tumorigenesis. Proc. Natl. Acad. Sci. USA 102 (2005) 6942-6947
53. Zhou B.P., Liao Y., Xia W., Zou Y., Spohn B., and Hung M.C. HER-2/neu induces p53 ubiquitination via Akt-mediated MDM2 phosphorylation. Nat. Cell Biol. 3 (2001) 973-982