Nkx3.1 and Myc crossregulate shared target genes in mouse and human prostate tumorigenesis

Journal of Clinical Investigation

Volumn 122, Issue 5, 2012, Pages 1907-1919

  Anderson, Philip D ^a   McKissic, Sydika A ^a   Logan, Monica ^b   Roh, Meejeon ^a   Franco, Omar E ^c   Wang, Jie ^a   Doubinskaia, Irina ^a   Van Der Meer, Riet ^a   Hayward, Simon W ^a,c   Eischen, Christine M ^a   Eltoum, Isam Eldin ^d   Abdulkadir, Sarki A ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MEHARRY MEDICAL COLLEGE   (United States)

^c VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^d University of Alabama at Birmingham   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MYC PROTEIN; PROTEIN NKX3.1; TUMOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CANCER RELAPSE; CONTROLLED STUDY; GENE CONTROL; GENE EXPRESSION; GENE SEQUENCE; GENE TARGETING; GENETIC ANALYSIS; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; ONCOGENE C MYC; PRIORITY JOURNAL; PROSTATE TUMOR;

ANIMALS; BASE SEQUENCE; BINDING SITES; CELL LINE; CELL TRANSFORMATION, NEOPLASTIC; CONSENSUS SEQUENCE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE REGULATORY NETWORKS; HOMEODOMAIN PROTEINS; HUMANS; MALE; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, SCID; MICE, TRANSGENIC; NEOPLASM TRANSPLANTATION; PROSTATIC INTRAEPITHELIAL NEOPLASIA; PROSTATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS C-MYC; RATS; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84860586275     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI58540     Document Type: Article

References (59)

1. Land H, Parada LF, Weinberg RA. Tumorigenic conversion of primary embryo fibroblasts requires at least two cooperating oncogenes. Nature. 1983;304(5927):596-602. (Pubitemid 13035496)
2. Ruley HE. Adenovirus early region 1A enables viral and cellular transforming genes to transform primary cells in culture. Nature. 1983;304(5927):602-606. (Pubitemid 13035497)
3. McMurray HR, et al. Synergistic response to oncogenic mutations defines gene class critical to cancer phenotype. Nature. 2008;453(7198):1112-1116. (Pubitemid 351871734)
4. Luo J, Elledge SJ. Cancer: Deconstructing oncogenesis. Nature. 2008;453(7198):995-996. (Pubitemid 351871722)
5. Bhatia-Gaur R, et al. Roles for Nkx3.1 in prostate development and cancer. Genes Dev. 1999;13(8):966-977. (Pubitemid 29200980)
6. Wang X, et al. A luminal epithelial stem cell that is a cell of origin for prostate cancer. Nature. 2009;461(7263):495-500.
7. Abdulkadir SA. Mechanisms of prostate tumorigenesis: roles for transcription factors Nkx3.1 and Egr1. Ann N Y Acad Sci. 2005;1059:33-40. (Pubitemid 43211608)
8. Abate-Shen C, Shen MM, Gelmann E. Integrating differentiation and cancer: the Nkx3.1 homeobox gene in prostate organogenesis and carcinogenesis. Differentiation. 2008;76(6):717-727. (Pubitemid 352032747)
9. Zheng SL, et al. Germ-line mutation of NKX3.1 cosegregates with hereditary prostate cancer and alters the homeodomain structure and function. Cancer Res. 2006;66(1):69-77. (Pubitemid 43166011)
10. Eeles RA, et al. Identification of seven new prostate cancer susceptibility loci through a genome-wide association study. Nat Genet. 2009;41(10):1116-1121.
11. Takata R, et al. Genome-wide association study identifies five new susceptibility loci for prostate cancer in the Japanese population. Nat Genet. 2010;42(9):751-754.
12. Akamatsu S, et al. A functional variant in NKX3.1 associated with prostate cancer susceptibility down-regulates NKX3.1 expression. Hum Mol Genet. 2010;19(21):4265-4272.
13. Kim MJ, et al. Nkx3.1 mutant mice recapitulate early stages of prostate carcinogenesis. Cancer Res. 2002;62(11):2999-3004. (Pubitemid 34602384)
14. Abdulkadir SA, et al. Conditional loss of nkx3.1 in adult mice induces prostatic intraepithelial neoplasia. Mol Cell Biol. 2002;22(5):1495-1503. (Pubitemid 34150785)
15. Kim MJ, et al. Cooperativity of Nkx3.1 and Pten loss of function in a mouse model of prostate carcinogenesis. Proc Natl Acad Sci U S A. 2002;99(5):2884-2889. (Pubitemid 34240555)
16. Abate-Shen C, et al. Nkx3.1; Pten mutant mice develop invasive prostate adenocarcinoma and lymph node metastases. Cancer Res. 2003;63(14):3886-3890. (Pubitemid 36917899)
17. Wang S, et al. Prostate-specific deletion of the murine Pten tumor suppressor gene leads to metastatic prostate cancer. Cancer Cell. 2003;4(3):209-221. (Pubitemid 37163835)
18. Lei Q, et al. NKX3.1 stabilizes p53, inhibits AKT activation, and blocks prostate cancer initiation caused by PTEN loss. Cancer Cell. 2006;9(5):367-378. (Pubitemid 43668733)
19. Zhang Y, et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 2008;9(9):R137.
20. Mogal AP, van der Meer R, Crooke PS, Abdulkadir SA. Haploinsufficient prostate tumor suppression by Nkx3.1: a role for chromatin accessibility in dosage-sensitive gene regulation. J Biol Chem. 2007;282(35):25790-25800. (Pubitemid 47372777)
21. He WW, 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. 1997;43(1):69-77. (Pubitemid 27310524)
22. Bowen C, et al. Loss of NKX3.1 expression in human prostate cancers correlates with tumor progression. Cancer Res. 2000;60(21):6111-6115.
23. O'Geen H, et al. Genome-wide binding of the orphan nuclear receptor TR4 suggests its general role in fundamental biological processes. BMC Genomics. 2010;11:689.
24. Cartharius K, et al. MatInspector and beyond: promoter analysis based on transcription factor binding sites. Bioinformatics. 2005;21(13):2933-2942. (Pubitemid 40916416)
25. Wang Q, et al. A hierarchical network of transcription factors governs androgen receptor-dependent prostate cancer growth. Mol Cell. 2007;27(3):380-392. (Pubitemid 47126935)
26. Lupien M, et al. FoxA1 translates epigenetic signatures into enhancer-driven lineage-specific transcription. Cell. 2008;132(6):958-970. (Pubitemid 351391952)
27. He HH, et al. Nucleosome dynamics define transcriptional enhancers. Nat Genet. 2010;42(4):343-347.
28. Yu J, et al. An integrated network of androgen receptor, polycomb, and TMPRSS2-ERG gene fusions in prostate cancer progression. Cancer Cell. 2010;17(5):443-454.
29. Steadman DJ, Giuffrida D, Gelmann EP. DNAbinding sequence of the human prostate-specific homeodomain protein NKX3.1. Nucleic Acids Res. 2000;28(12):2389-2395. (Pubitemid 30349045)
30. Bailey TL, Elkan C. Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol. 1994;2:28-36.
31. Magee JA, Abdulkadir SA, Milbrandt J. Haploinsufficiency at the Nkx3.1 locus. A paradigm for stochastic, dosage-sensitive gene regulation during tumor initiation. Cancer Cell. 2003;3(3):273-283. (Pubitemid 37443882)
32. Ouyang X, DeWeese TL, Nelson WG, Abate-Shen C. Loss-of-function of Nkx3.1 promotes increased oxidative damage in prostate carcinogenesis. Cancer Res. 2005;65(15):6773-6779. (Pubitemid 41060715)
33. Subramanian A, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A. 2005;102(43):15545-15550. (Pubitemid 41528093)
34. Kanehisa M, Goto S. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 2000;28(1):27-30. (Pubitemid 30047706)
35. Weigel AL, Handa JT, Hjelmeland LM. Microarray analysis of H2O2-, HNE-, or tBH-treated ARPE-19 cells. Free Radic Biol Med. 2002;33(10):1419-1432. (Pubitemid 35284925)
36. Zhang B, Kirov S, Snoddy J. WebGestalt: an integrated system for exploring gene sets in various biological contexts. Nucleic Acids Res. 2005;33(web server issue):W741-W748.
37. Nikolsky Y, Nikolskaya T, Bugrim A. Biological networks and analysis of experimental data in drug discovery. Drug Discov Today. 2005;10(9):653-662. (Pubitemid 40704773)
38. Bindea G, et al. ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics. 2009;25(8):1091-1093.
39. Watson PA, Ellwood-Yen K, King JC, Wongvipat J, Lebeau MM, Sawyers CL. Context-dependent hormone-refractory progression revealed through characterization of a novel murine prostate cancer cell line. Cancer Res. 2005;65(24):11565-11571. (Pubitemid 41821715)
40. Horoszewicz JS, et al. LNCaP model of human prostatic carcinoma. Cancer Res. 1983;43(4):1809-1818. (Pubitemid 13122588)
41. Wang J, et al. Pim1 kinase synergizes with c-MYC to induce advanced prostate carcinoma. Oncogene. 2010;29(17):2477-2487.
42. Wang J, Anderson PD, Luo W, Gius D, Roh M, Abdulkadir SA. Pim1 kinase is required to maintain tumorigenicity in MYC-expressing prostate cancer cells [published online ahead of print August 22, 2011]. Oncogene. doi:10.1038/onc.2011.371.
43. Koh CM, et al. Alterations in nucleolar structure and gene expression programs in prostatic neoplasia are driven by the MYC oncogene. Am J Pathol. 2011;178(4):1824-1834.
44. Taylor BS, et al. Integrative genomic profiling of human prostate cancer. Cancer Cell. 2010;18(1):11-22.
45. Roh M, Kim J, Song C, Wills M, Abdulkadir SA. Transgenic mice for Cre-inducible overexpression of the oncogenes c-MYC and Pim-1 in multiple tissues. Genesis. 2006;44(10):447-453. (Pubitemid 44684991)
46. Kim J, Eltoum IE, Roh M, Wang J, Abdulkadir SA. Interactions between cells with distinct mutations in c-MYC and Pten in prostate cancer. PLoS Genet. 2009;5(7):e1000542.
47. Iwata T, et al. MYC overexpression induces prostatic intraepithelial neoplasia and loss of Nkx3.1 in mouse luminal epithelial cells. PLoS One. 2010;5(2):e9427.
48. Ellwood-Yen K, et al. Myc-driven murine prostate cancer shares molecular features with human prostate tumors. Cancer Cell. 2003;4(3):223-238. (Pubitemid 37163836)
49. Ishii K, Shappell SB, Matusik RJ, Hayward SW. Use of tissue recombination to predict phenotypes of transgenic mouse models of prostate carcinoma. Lab Invest. 2005;85(9):1086-1103. (Pubitemid 43073983)
50. Kusy S, et al. NKX3.1 is a direct TAL1 target gene that mediates proliferation of TAL1-expressing human T cell acute lymphoblastic leukemia. J Exp Med. 2010;207(10):2141-2156.
51. Mathupala SP, Ko YH, Pedersen PL. Hexokinase-2 bound to mitochondria: cancer's stygian link to the "Warburg Effect" and a pivotal target for effective therapy. Semin Cancer Biol. 2009;19(1):17-24.
52. Hellwinkel OJ, et al. Transcription alterations of members of the ubiquitin-proteasome network in prostate carcinoma. Prostate Cancer Prostatic Dis. 2011;14(1):38-45.
53. Dang CV, O'Donnell KA, Zeller KI, Nguyen T, Osthus RC, Li F. The c-Myc target gene network. Semin Cancer Biol. 2006;16(4):253-264. (Pubitemid 44311039)
54. Gurel B, et al. Nuclear MYC protein overexpression is an early alteration in human prostate carcinogenesis. Mod Pathol. 2008;21(9):1156-1167.
55. Bethel CR, et al. Decreased NKX3.1 protein expression in focal prostatic atrophy, prostatic intraepithelial neoplasia, and adenocarcinoma: association with gleason score and chromosome 8p deletion. Cancer Res. 2006;66(22):10683- 10690. (Pubitemid 44876963)
56. Qi Y, Gregory MA, Li Z, Brousal JP, West K, Hann SR. p19ARF directly and differentially controls the functions of c-Myc independently of p53. Nature. 2004;431(7009):712-717. (Pubitemid 39382620)
57. Datta A, et al. Myc-ARF (alternate reading frame) interaction inhibits the functions of Myc. J Biol Chem. 2004;279(35):36698-36707. (Pubitemid 39129016)
58. Seoane J, Pouponnot C, Staller P, Schader M, Eilers M, Massague J. TGFbeta influences Myc, Miz-1 and Smad to control the CDK inhibitor p15INK4b. Nat Cell Biol. 2001;3(4):400-408. (Pubitemid 32288448)
59. Staller P, et al. Repression of p15INK4b expression by Myc through association with Miz-1. Nat Cell Biol. 2001;3(4):392-399. (Pubitemid 32288447)