Systems analysis of the prostate tumor suppressor NKX3.1 supports roles in DNA repair and luminal cell differentiation

F1000Research

Volumn 3, Issue , 2014, Pages

  Yang, Chih Cheng ^a   Chung, Alicia ^c   Ku, Chia Yu ^a   Brill, Laurence M ^a   Williams, Roy ^a   Wolf, Dieter A ^a,b  

^a BURNHAM INSTITUTE   (United States)

^b University of California San Diego   (United States)

^c GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HOMEODOMAIN PROTEIN; INTERFERON; KU ANTIGEN; MYC PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN KU80; STAT PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NKX3.1; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CANCER INHIBITION; CELL DIFFERENTIATION; CELL TRANSFORMATION; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; HUMAN TISSUE; MOLECULAR BIOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; PROSTATE EPITHELIUM; PROSTATIC INTRAEPITHELIAL NEOPLASIA; PROTEIN DEFECT; PROTEIN DNA INTERACTION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SECRETORY CELL; SECRETORY LUMINAL CELL; SECRETORY LUMINAL CELL DIFFERENTIATION; SIGNAL TRANSDUCTION; SYSTEM ANALYSIS; TRANSCRIPTION INITIATION; TRANSCRIPTOMICS; UNINDEXED SEQUENCE;

EID: 84914814469     PISSN: 20461402     EISSN: 1759796X     Source Type: Journal    
DOI: 10.12688/f1000research.3818.1     Document Type: Article

References (94)

1. 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):717-27. 18557759 10.1111/j.1432-0436.2008.00292.x 3683569
2. Shen MM Abate-Shen C: Roles of the Nkx3.1 homeobox gene in prostate organogenesis and carcinogenesis. Dev Dyn. 2003;228(4):767-78. 14648854 10.1002/dvdy.10397
3. Bhatia-Gaur R Donjacour AA Sciavolino PJ: Roles for Nkx3.1 in prostate development and cancer. Genes Dev. 1999;13(8):966-77. 10215624 316645
4. Tanaka M Komuro I Inagaki H: Nkx3.1, a murine homolog of Ddrosophila bagpipe, regulates epithelial ductal branching and proliferation of the prostate and palatine glands. Dev Dyn. 2000;219(2):248-60. 11002344
5. Kim MJ Bhatia-Gaur R Banach-Petrosky WA: Nkx3.1 mutant mice recapitulate early stages of prostate carcinogenesis. Cancer Res. 2002;62(11):2999-3004. 12036903
6. Abdulkadir SA Magee JA Peters TJ: Conditional loss of Nkx3.1 in adult mice induces prostatic intraepithelial neoplasia. Mol Cell Biol. 2002;22(5):1495-503. 11839815 10.1128/MCB.22.5.1495-1503.2002 134699
7. Gary B Azuero R Mohanty GS: Interaction of Nkx3.1 and p27kip1 in prostate tumor initiation. Am J Pathol. 2004;164(5):1607-14. 15111307 10.1016/S0002-9440(10)63719-4 1615644
8. Kim MJ Cardiff RD Desai N: 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):2884-9. 11854455 10.1073/pnas.042688999 122442
9. Lei Q Jiao J Xin L: NKX3.1 stabilizes p53, inhibits AKT activation, and blocks prostate cancer initiation caused by PTEN loss. Cancer Cell. 2006;9(5):367-78. 16697957 10.1016/j.ccr.2006.03.031
10. Bowen C Bubendorf L Voeller HJ: Loss of NKX3.1 expression in human prostate cancers correlates with tumor progression. Cancer Res. 2000;60(21):6111-5. 11085535
11. Steadman DJ Giuffrida D Gelmann EP: DNA-binding sequence of the human prostate-specific homeodomain protein NKX3.1. Nucleic Acids Res. 2000;28(12):2389-95. 10871372 10.1093/nar/28.12.2389 102730
12. Choi CY Kim YH Kwon HJ: The homeodomain protein NK-3 recruits Groucho and a histone deacetylase complex to repress transcription. J Biol Chem. 1999;274(47):33194-7. 10559189
13. Simmons SO Horowitz JM: Nkx3.1 binds and negatively regulates the transcriptional activity of Sp-family members in prostate-derived cells. Biochem J. 2006;393(Pt 1):397-409. 16201967 10.1042/BJ20051030 1383699
14. Chen H Nandi AK Li X: NKX-3.1 interacts with prostate-derived Ets factor and regulates the activity of the PSA promoter. Cancer Res. 2002;62(2):338-40. 11809674
15. Liu W Zhang P Chen W: Characterization of two functional NKX 3.1 binding sites upstream of the PCAN1 gene that are involved in the positive regulation of PCAN1 gene transcription. BMC Mol Biol. 2008;9(1):45. 18454873 10.1186/1471-2199-9-45 2390571
16. Anderson PD McKissic SA Logan M: Nkx3.1 and Myc crossregulate shared target genes in mouse and human prostate tumorigenesis. J Clin Invest. 2012;122(5):1907-19. 22484818 10.1172/JCI58540 3336973
17. Carson JA Fillmore RA Schwartz RJ: The smooth muscle gamma-actin gene promoter is a molecular target for the mouse bagpipe homologue, mNkx3-1, and serum response factor. J. Biol Chem. 2000;275(50):39061-72. 10993896 10.1074/jbc.M006532200
18. Tan PY Chang CW Chng KR: Integration of regulatory networks by NKX3-1 promotes androgen-dependent prostate cancer survival. Mol Cell Biol. 2012;32(2):399-414. 22083957 10.1128/MCB.05958-11 3255774
19. 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):273-83. 12676585 10.1016/S1535-6108(03)00047-3
20. Ouyang X DeWeese TL Nelson WG: Loss-of-function of Nkx3.1 promotes increased oxidative damage in prostate carcinogenesis. Cancer Res. 2005;65(15):6773-9. 16061659 10.1158/0008-5472.CAN-05-1948
21. Ju JH Maeng JS Zemedkun M: Physical and functional interactions between the prostate suppressor homeoprotein NKX3.1 and serum response factor. J Mol Biol. 2006;360(5):989-99. 16814806 10.1016/j.jmb.2006.05.064
22. Bowen C Stuart A Ju JH: NKX3.1 homeodomain protein binds to topoisomerase I and enhances its activity. Cancer Res. 2007;67(2):455-64. 17234752 10.1158/0008-5472.CAN-06-1591
23. Song L Bowen C Gelmann EP: Structural and functional interactions of the prostate cancer suppressor protein NKX3.1 with topoisomerase I. Biochem J. 2013;453(1):125-36. 23557481 10.1042/BJ20130012
24. Bowen C Gelmann EP: NKX3.1 activates cellular response to DNA damage. Cancer Res. 2010;70(8):3089-97. 20395202 10.1158/0008-5472.CAN-09-3138
25. Berger R Febbo PG Majumder PK: Androgen-induced differentiation and tumorigenicity of human prostate epithelial cells. Cancer Res. 2004;64(24):8867-8875. 15604246 10.1158/0008-5472.CAN-04-2938
26. Lu L Schulz H Wolf DA: The F-box protein SKP2 mediates androgen control of p27 stability in LNCaP human prostate cancer cells. BMC Cell Biol. 2002;3(1):22. 12188931 10.1186/1471-2121-3-22 122093
27. Brill LM Motamedchaboki K Wu S: Comprehensive proteomic analysis of Schizosaccharomyces pombe by two-dimensional HPLC-tandem mass spectrometry. Methods. 2009;48(3):311-9. 19272449 10.1016/j.ymeth.2009.02.023 2710416
28. Sha Z Brill LM Cabrera R: The eIF3 interactome reveals the translasome, a supercomplex linking protein synthesis and degradation machineries. Mol Cell. 2009;36(1):141-52. 19818717 10.1016/j.molcel.2009.09.026 2789680
29. Liu H Sadygov RG Yates JR 3rd: A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal Chem. 2004;76(14):4193-201. 15253663 10.1021/ac0498563
30. Keller A Eng J Zhang N: A uniform proteomics MS/MS analysis platform utilizing open XML file formats. Mol Syst Biol. 2005. 16729052 10.1038/msb4100024 1681455
31. Schmidt MW Houseman A Ivanov AR: Comparative proteomic and transcriptomic profiling of the fission yeast Schizosaccharomyces pombe. Mol Syst Biol. 2007;3:79. 17299416 10.1038/msb4100117 1828747
32. Wu G Feng X Stein L: A human functional protein interaction network and its application to cancer data analysis. Genome Biol. 2010;11(5):R53. 20482850 10.1186/gb-2010-11-5-r53 2898064
33. Nanni S Priolo C Grasselli A: Epithelial-restricted gene profile of primary cultures from human prostate tumors: a molecular approach to predict clinical behavior of prostate cancer. Mol Cancer Res. 2006;4(2):79-92. 16513839 10.1158/1541-7786.MCR-05-0098
34. Li X Guan B Maghami S: NKX3.1 is regulated by protein kinase CK2 in prostate tumor cells. Mol Cell Biol. 2006;26(8):3008-17. 16581776 10.1128/MCB.26.8.3008-3017.2006 1446956
35. Markowski MC Bowen C Gelmann EP: Inflammatory cytokines induce phosphorylation and ubiquitination of prostate suppressor protein NKX3.1. Cancer Res. 2008;68(17):6896-901. 18757402 10.1158/0008-5472.CAN-08-0578 2586101
36. Smith GC Jackson SP: The DNA-dependent protein kinase. Genes Dev. 1999;13(8):916-934. 10215620
37. Giffin W Torrance H Rodda DJ: Sequence-specific DNA binding by Ku autoantigen and its effects on transcription. Nature. 1996;380(6571):265-8. 8637578 10.1038/380265a0
38. Krishnakumar R Kraus WL: The PARP side of the nucleus: molecular actions, physiological outcomes, and clinical targets. Mol Cell. 2010;39(1):8-24. 20603072 10.1016/j.molcel.2010.06.017 2923840
39. Schild-Poulter C Pope L Giffin W: The binding of Ku antigen to homeodomain proteins promotes their phosphorylation by DNA-dependent protein kinase. J Biol Chem. 2001;276(20):16848-16856. 11279128 10.1074/jbc.M100768200
40. Ruscetti T Lehnert BE Halbrook J: Stimulation of the DNA-dependent protein kinase by poly(ADP-ribose) polymerase. J Biol Chem. 1998;273(23):14461-14467. 9603959
41. Erbaykent-Tepedelen B Karamil S Gonen-Korkmaz C: DNA damage response (DDR) via NKX3.1 expression in prostate cells. J Steroid Biochem Mol Biol. 2014;141:26-36. 24434284 10.1016/j.jsbmb.2014.01.001
42. Ting NS Kao PN Chan DW: DNA-dependent protein kinase interacts with antigen receptor response element binding proteins NF90 and NF45. J Biol Chem. 1998;273(4):2136-2145. 9442054
43. Jønson L Vikesaa J Krogh A: Molecular composition of IMP1 ribonucleoprotein granules. Mol Cell Proteomics. 2007;6(5):798-811. 17289661 10.1074/mcp.M600346-MCP200
44. Han SP Tang YH Smith R: Functional diversity of the hnRNPs: past, present and perspectives. Biochem J. 2010;430(3):379-92. 20795951 10.1042/BJ20100396
45. Andersen JS Lyon CE Fox AH: Directed proteomic analysis of the human nucleolus. Curr Biol 2002;12(1):1-11. 11790298 10.1016/S0960-9822(01)00650-9
46. Scherl A Coute Y Deon C: Functional proteomic analysis of human nucleolus. Mol Biol Cell. 2002;13(11):4100-9. 12429849 10.1091/mbc.E02-05-0271 133617
47. Pandit S Wang D Fu XD: Functional integration of transcriptional and RNA processing machineries. Curr Opin Cell Biol. 2008;20(3):260-5. 18436438 10.1016/j.ceb.2008.03.001 2701685
48. Fang X Yoon JG Li L: Landscape of the SOX2 protein-protein interactome. Proteomics. 2011;11(5):921-34. 21280222 10.1002/pmic.201000419
49. Segura-Totten M Wilson KL: BAF: roles in chromatin, nuclear structure and retrovirus integration. Trends Cell Biol. 2004;14(5):261-6. 15130582 10.1016/j.tcb.2004.03.004
50. Wang X Xu S Rivolta C: Barrier to autointegration factor interacts with the cone-rod homeobox and represses its transactivation function. J Biol Chem. 2002;277(45):43288-300. 12215455 10.1074/jbc.M207952200
51. Norris JD Chang CY Wittmann BM: The homeodomain protein HOXB13 regulates the cellular response to androgens. Mol Cell. 2009;36(3):405-16. 19917249 10.1016/j.molcel.2009.10.020 2788777
52. Ewing CM Ray AM Lange EM: Germline mutations In HOXB13 and prostate-cancer risk. N Engl J Med. 2012;366(2):141-9. 22236224 10.1056/NEJMoa1110000 3779870
53. Wang XD Leow CC Zha J: Notch signaling is required for normal prostatic epithelial cell proliferation and differentiation. Dev Biol. 2006;290(1):66-80. 16360140 10.1016/j.ydbio.2005.11.009
54. Missero C Calautti E Eckner R: Involvement of the cell-cycle inhibitor Cip1/WAF1 and the E1A-associated p300 protein in terminal differentiation. Proc Natl Acad Sci U S A. 1995;92(12):5451-5. 7777529 10.1073/pnas.92.12.5451 41712
55. Rehman I Cross SS Catto JW: Promoter hyper-methylation of calcium binding proteins S100A6 and S100A2 in human prostate cancer. Prostate. 2005;65(4):322-30. 16015609 10.1002/pros.20302
56. Lodygin D Diebold J Hermeking H: Prostate cancer is characterized by epigenetic silencing of 14-3-3sigma expression. Oncogene. 2004;23(56):9034-41. 15489902 10.1038/sj.onc.1208004
57. Urano T Takahashi S Suzuki T: 14-3-3sigma is down-regulated in human prostate cancer. Biochem Biophys Res Commun. 2004;319(3):795-800. 15184053 10.1016/j.bbrc.2004.05.056
58. Sathyanarayana UG Padar A Suzuki M: Aberrant promoter methylation of laminin-5-encoding genes in prostate cancers and its relationship to clinicopathological features. Clin Cancer Res. 2003;9(17):6395-400. 14695140
59. Sheehan GM Kallakury BV Sheehan CE: Loss of claudins-1 and -7 and expression of claudins-3 and -4 correlate with prognostic variables in prostatic adenocarcinomas. Hum Pathol. 2007;38(4):564-9. 17306334 10.1016/j.humpath.2006.11.007
60. Takahashi S Suzuki S Inaguma S: Down-regulated expression of prostasin in high-grade or hormone-refractory human prostate cancers. Prostate. 2003;54(3):187-93. 12518323 10.1002/pros.10178
61. Jarrard DF Paul R van Bokhoven A: P-Cadherin is a basal cell-specific epithelial marker that is not expressed in prostate cancer. Clin Cancer Res. 1997;3(11):2121-8. 9815605
62. Yousef GM Scorilas A Chang A: Down-regulation of the human kallikrein gene 5 (KLK5) in prostate cancer tissues. Prostate. 2002;51(2):126-32. 11948967 10.1002/pros.10067
63. Henrique R Costa VL Cerveira N: Hypermethylation of Cyclin D2 is associated with loss of mRNA expression and tumor development in prostate cancer. J Mol Med (Berl). 2006;84(11):911-8. 17016690 10.1007/s00109-006-0099-4
64. Cornford PA Dodson AR Parsons KF: Heat shock protein expression independently predicts clinical outcome in prostate cancer. Cancer Res. 2000;60(24):7099-7105. 11156417
65. Wang MH Grossmann ME Young CY: Forced expression of heat-shock protein 70 increases the secretion of Hsp70 and provides protection against tumour growth. Br J Cancer. 2004;90(4):926-31. 14970875 10.1038/sj.bjc.6601583 2410170
66. Tomlinson V Newbery H Wray N: Translation elongation factor eEF1A2 is a potential oncoprotein that is overexpressed in two-thirds of breast tumours. BMC Cancer. 2005;5(1):113. 16156888 10.1186/1471-2407-5-113 1236916
67. Namkoong H Shin S Kim H: The bone morphogenetic protein antagonist gremlin 1 is overexpressed in human cancers and interacts with YWHAH protein. BMC Cancer. 2006;6(1):74. 16545136 10.1186/1471-2407-6-74 1459871
68. Katoh M Katoh M: Human FOX gene family (Review). Int J Oncol. 2004;25(5):1495-500. 15492844 10.3892/ijo.25.5.1495
69. Jaggi M Nazemi T Abrahams NA: N-cadherin switching occurs in high Gleason grade prostate cancer. Prostate. 2006;66(2):193-9. 16173043 10.1002/pros.20334
70. Bethel CR Faith D Li X: 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):10683-90. 17108105 10.1158/0008-5472.CAN-06-0963
71. Ashida S Nakagawa H Katagiri T: Molecular features of the transition from prostatic intraepithelial neoplasia (PIN) to prostate cancer: genome-wide gene-expression profiles of prostate cancers and PINs. Cancer Res. 2004;64(17):5963-5972. 15342375 10.1158/0008-5472.CAN-04-0020
72. Hermeking H Lengauer C Polyak K: 14-3-3 sigma is a p53-regulated inhibitor of G2/M progression. Mol Cell. 1997;1(1):3-11. 9659898 10.1016/S1097-2765(00)80002-7
73. el-Deiry WS Tokino T Velculescu VE: WAF1, a potential mediator of p53 tumor suppression. Cell. 1993;75(4):817-25. 8242752
74. Attardi LD Reczek EE Cosmas C: PERP, an apoptosis-associated target of p53, is a novel member of the PMP-22/gas3 family. Genes Dev. 2000;14(6):704-718. 10733530 316461
75. Ongusaha PP Ouchi T Kim K: BRCA1 shifts p53-mediated cellular outcomes towards irreversible growth arrest. Oncogene. 2003;22(24):3749-58. 12802282 10.1038/sj.onc.1206439
76. Komarova EA Diatchenko L Rokhlin OW: Stress-induced secretion of growth inhibitors: a novel tumor suppressor function of p53. Oncogene. 1998;17(9):1089-96. 9764819 10.1038/sj.onc.1202303
77. Thomas-Tikhonenko A Viard-Leveugle I Dews M: Myc-transformed epithelial cells down-regulate rlusterin, which inhibits their growth in vitro and carcinogenesis in vivo. Cancer Res. 2004;64(9):3126-3136. 15126350 10.1158/0008-5472.CAN-03-1953
78. Ceballos E Munoz-Alonso MJ Berwanger B: Inhibitory effect of c-Myc on p53-induced apoptosis in leukemia cells. Microarray analysis reveals defective induction of p53 target genes and upregulation of chaperone genes. Oncogene. 2005;24(28):4559-71. 15856024 10.1038/sj.onc.1208652
79. Shimono A Okuda T Kondoh H: N-myc-dependent repression of ndr1, a gene identified by direct subtraction of whole mouse embryo cDNAs between wild type and N-myc mutant. Mech Dev. 1999;83(1-2):39-52. 10381566 10.1016/S0925-4773(99)00025-8
80. Kaplan-Albuquerque N Bogaert YE Van Putten V: Patterns of gene expression differentially regulated by platelet-derived growth factor and hypertrophic stimuli in vascular smooth muscle cells. J Biol Chem. 2005;280(20):19966-19976. 15774477 10.1074/jbc.M500917200
81. Yu J Liu XW Kim HR: Platelet-derived growth factor (PDGF) receptor-alpha-activated c-Jun NH2-terminal kinase-1 is critical for PDGF-induced p21WAF1/CIP1 promoter activity independent of p53. J Biol Chem. 2003;278(49):49582-49588. 14506245 10.1074/jbc.M309986200
82. Butler R Mitchell SH Tindall DJ: Nonapoptotic cell death associated with S-phase arrest of prostate cancer cells via the peroxisome proliferator-activated receptor gamma ligand, 15-deoxy-delta12,14-prostaglandin J2. Cell Growth Differ. 2000;11(1):49-61. 10672903
83. Thiery JP Acloque H Huang RY: Epithelial-mesenchymal transitions in development and disease. Cell. 2009;139(5):871-90. 19945376 10.1016/j.cell.2009.11.007
84. Horrevoets AJ Fontijn RD van Zonneveld AJ: Vascular endothelial genes that are responsive to tumor necrosis factor-alpha in vitro are expressed in atherosclerotic lesions, including inhibitor of apoptosis protein-1, stannin, and two novel genes. Blood. 1999;93(10):3418-3431. 10233894
85. Kalai M Lamkanfi M Denecker G: Regulation of the expression and processing of caspase-12. J Cell Biol. 2003;162(3):457-467. 12885762 10.1083/jcb.200303157 2172698
86. Mann K Hainaut P: Aminothiol WR1065 induces differential gene expression in the presence of wild-type p53. Oncogene. 2005;24(24):3964-75. 15750621 10.1038/sj.onc.1208563
87. Manna SK Mukhopadhyay A Aggarwal BB: Human chorionic gonadotropin suppresses activation of nuclear transcription factor-ΚB and activator protein-1 Induced by tumor necrosis factor. J Biol Chem. 2000;275(18):13307-13314. 10788437 10.1074/jbc.275.18.13307
88. Xie X Lu J Kulbokas EJ: Systematic discovery of regulatory motifs in human promoters and 3' UTRs by comparison of several mammals. Nature. 2005;434(7031):338-45. 15735639 10.1038/nature03441 2923337
89. Xiao W Hodge DR Wang L: NF-kappaB activates IL-6 expression through cooperation with c-Jun and IL6-AP1 site, But is independent of its IL6-NFkappaB regulatory site in autocrine human multiple myeloma cells. Cancer Biol Ther. 2004;3(10):1007-17. 15467434 10.4161/cbt.3.10.1141
90. Garraway LA Lin D Signoretti S: Intermediate basal cells of the prostate: in vitro and in vivo characterization. Prostate. 2003;55(3):206-18. 12692787 10.1002/pros.10244
91. Schadt EE Friend SH Shaywitz DA: A network view of disease and compound screening. Nat Rev Drug Discov. 2009;8(4):286-95. 19337271 10.1038/nrd2826
92. Nagata Y Todokoro K: Requirement of activation of JNK and p38 for environmental stress-induced erythroid differentiation and apoptosis and of inhibition of ERK for apoptosis. Blood. 1999;94(3):853-63. 10419875
93. Dong C Yang DD Wysk M: Defective T cell differentiation in the absence of Jnk1. Science. 1998;282(5396):2092-5. 9851932 10.1126/science.282.5396.2092
94. Yang CC Chung A Ku CY: NKX3.1 expression and interactions Dataset. Figshare. 2014. Data Source