Global methylation analysis identifies PITX2 as an upstream regulator of the androgen receptor and IGF-I receptor genes in prostate cancer

Hormone and Metabolic Research

Volumn 44, Issue 7, 2012, Pages 511-519

  Schayek, H ^a   Bentov, I ^a   Jacob Hirsch, J ^b   Yeung, C ^c   Khanna, C ^c   Helman, L J ^c   Plymate, S R ^d   Werner, H ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b SHEBA MEDICAL CENTER   (Israel)

^c NATIONAL CANCER INSTITUTE   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

Author keywords

androgen receptor; DNA methylation; epigenetic regulation; IGF I receptor; insulin like growth factor I (IGF I); prostate cancer

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; ANDROGEN RECEPTOR; SOMATOMEDIN C RECEPTOR; TRANSCRIPTION FACTOR PITX2;

ADULT; ADVANCED CANCER; ARTICLE; BENIGN TUMOR; CANCER CELL CULTURE; CANCER GROWTH; CONTROLLED STUDY; DNA METHYLATION; DNA MICROARRAY; GENE; GENE OVEREXPRESSION; GENETIC ASSOCIATION; GENETIC REGULATION; HUMAN; HUMAN CELL; MALE; METASTASIS; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PITX2 GENE; PRIORITY JOURNAL; PROSTATE CANCER; SIGNAL TRANSDUCTION;

DNA METHYLATION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, NEOPLASM; HOMEODOMAIN PROTEINS; HUMANS; MALE; MIDDLE AGED; PROMOTER REGIONS, GENETIC; PROSTATIC NEOPLASMS; RECEPTOR, IGF TYPE 1; RECEPTORS, ANDROGEN; TRANSCRIPTION FACTORS;

EID: 84862162985     PISSN: 00185043     EISSN: 14394286     Source Type: Journal    
DOI: 10.1055/s-0032-1311566     Document Type: Article

References (54)

1. Gelmann E P. Molecular biology of the androgen receptor. J Clin Oncol: 2002; 20 2001 2015
2. Grossmann M E, Huang H, Tindall D J. Androgen receptor signaling in androgen-refractory prostate cancer. J Natl Cancer Inst: 2001; 93 1687 1697 (Pubitemid 33130257)
3. Shi X B, Ma A H, Xia L, Kung H J, de Vere White R W. Functional analysis of 44 mutant androgen receptors from human prostate cancer. Cancer Res: 2002; 62 1496 1502 (Pubitemid 34407813)
4. Ruan W, Powell-Braxton L, Kopchick J J, Kleinberg D L. Evidence that insulin-like growth factor I and growth hormone are required for prostate gland development. Endocrinology: 1999; 140 1984 1989 (Pubitemid 30639064)
5. DiGiovanni J, Kiguchi K, Frijhoff A, Wilker E, Bol D K, Beltran L, Moats S, Ramirez A, Jorcano J, Conti C. Deregulated expression of insulin-like growth factor I in prostate epithelium leads to neoplasia in transgenic mice. Proc Natl Acad Sci USA: 2000; 97 3455 3460 (Pubitemid 30183324)
6. Wu J D, Haugk K, Woodke L, Nelson P, Coleman I, Plymate S R. Interaction of IGF signaling and the androgen receptor in prostate cancer progression. J Cell Biochem: 2006; 99 392 401 (Pubitemid 44435557)
7. Chan J M, Stampfer M J, Giovannucci E, Gann P H, Ma J, Wilkinson P, Hennekens C H, Pollak M. Plasma insulin-like growth factor-I and prostate cancer risk: a prospective study. Science: 1998; 279 563 566 (Pubitemid 28067285)
8. Rowlands M A, Holly J M, Gunnell D, Donovan J, Lane J A, Hamdy F, Neal D E, Oliver S, Smith G D, Martin R M. Circulating insulin-like growth factors and IGF-binding proteins in PSA-detected prostate cancer: the large case-control study ProtecT. Cancer Res: 2012; 72 503 515
9. Tennant M K, Thrasher J B, Twomey P A, Drivdahl R H, Birnbaum R S, Plymate S R. Protein and mRNA for the type 1 insulin-like growth factor (IGF) receptor is decreased and IGF-II mRNA is increased in human prostate carcinoma compared to benign prostate epithelium. J Clin Endocrinol Metab: 1996; 81 3774 3782 (Pubitemid 26339953)
10. Chott A, Sun Z, Morganstern D, Pan J, Li T, Susani M, Mosberger I, Upton M P, Bubley G J, Balk S P. Tyrosine kinases expressed in vivo by human prostate cancer bone marrow metastases and loss of type 1 insulin-like growth factor receptor. Am J Pathol: 1999; 155 1271 1279 (Pubitemid 29488934)
11. Hellawell G O, Turner G D, Davies D R, Poulsom R, Brewster S F, Macaulay V M. Expression of the type 1 insulin-like growth factor receptor is up-regulated in primary prostate cancer and commonly persists in metastatic disease. Cancer Res: 2002; 62 2942 2950 (Pubitemid 34525783)
12. Liao Y, Abel U, Grobholz R, Hermani A, Trojan L, Angel P, Mayer D. Up-regulation of insulin-like growth factor axis components in human primary prostate cancer correlates with tumor grade. Human Pathol: 2005; 36 1186 1196 (Pubitemid 41540395)
13. Nickerson T, Chang F, Lorimer D, Smeekens S P, Sawyers C L, Pollak M. In vivo progression of LAPC-9 and LNCaP prostate cancer models to androgen independence is associated with increased expression of insulin-like growth factor I (IGF-I) and IGF-I receptor (IGF-IR). Cancer Res: 2001; 61 6276 6280 (Pubitemid 32762567)
14. Turney B W, Turner GD H, Brewster S F, Macaulay V M. Serial analysis of resected prostate cancer suggests up-regulation of type 1 IGF receptor with disease progression. BJU Int: 2011; 107 1489 1499
15. Baylin S B, Herman J G. DNA hypermethylation in tumorigenesis: epigenetics join genetics. Trends Genet: 2000; 16 168 174 (Pubitemid 30169152)
16. Li L-C, Okino S T, Dahiya R. DNA methylation in prostate cancer. Biochim Biophys Acta: 2004; 1704 87 102 (Pubitemid 39195351)
17. Baylin S B, Herman J G, Graff J R, Vertino P M, Issa J P. Alterations in DNA methylation: a fundamental aspect of neoplasia. Adv Cancer Res: 1998; 72 141 196 (Pubitemid 27435555)
18. Li L-C, Zhao H, Shiina H, Kane C J, Dahiya R. PGDB: a curated and integrated database of genes related to the prostate. Nucleic Acids Res: 2003; 31 291 293 (Pubitemid 36150387)
19. Schayek H, Bentov I, Sun S, Plymate S R, Werner H. Progression to metastatic stage in a cellular model of prostate cancer is associated with methylation of the androgen receptor gene and transcriptional suppression of the insulin-like growth factor-I receptor gene. Exp Cell Res: 2010; 316 1479 1488
20. Bae V L, Jackson-Cook C K, Maygarden S J, Plymate S R, Chen J, Ware J L. Metastatic sublines of an SV40 large T antigen immortalized human prostate epithelial cell line. Prostate: 1998; 34 275 282 (Pubitemid 28149872)
21. Bae V L, Jackson-Cook C K, Brothman A R, Maygarden S J, Ware J L. Tumorigenicity of SV40 T antigen immortalized human prostate epithelial cells: association with decreased epidermal growth factor receptor (EGFR) expression. Int J Cancer: 1994; 58 721 729 (Pubitemid 24279437)
22. Frommer M, McDonald L E, Millar D S, Collis C M, Watt F, Grigg G W, Molloy P L, Paul C L. A genomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands. Proc Natl Acad Sci USA: 1992; 89 1827 1831
23. Wiley A, Katsaros D, Chen H, Rigault de la Longrais I A, Beeghly A, Puopolo M, Singal R, Zhang Y, Amoako A, Zelterman D, Yu H. Aberrant promoter methylation of multiple genes in malignant ovarian tumors and in ovarian tumors with low malignant potential. Cancer: 2006; 107 299 308 (Pubitemid 44036559)
24. Mousa S A, Bergh J J, Dier E, Rebbaa A, O'Connor L J, Yalcin M, Aljada A, Dyskin E, Davis F B, Lin H Y, Davis P J. Tetraiodothyroacetic acid, a small molecule integrin ligand, blocks angiogenesis induced by vascular endothelial growth factor and basic fibroblast growth factor. Angiogenesis: 2008; 11 183 190
25. Suzuki M, Shigematsu H, Shames D S, Sunaga N, Takahashi T, Shivapurkar N, Iizasa T, Frenkel E P, Minna J D, Fujisawa T, Gazdar A F. DNA methylation-associated inactivation of TGFbeta-related genes DRM/Gremlin, RUNX3, and HPP1 in human cancers. Br J Cancer: 2005; 93 1029 1037 (Pubitemid 41548398)
26. Jana N R, Sarkar S, Ishizuka M, Yonemoto J, Tohyama C, Sone H. Role of estradiol receptor-alpha in differential expression of 2,3,7, 8-tetrachlorodibenzo-p-dioxin-inducible genes in the RL95-2 and KLE human endometrial cancer cell lines. Arch Biochem Biophys: 1999; 368 31 39 (Pubitemid 29372301)
27. Nimmrich I, Sieuwerts A M, Meijer-van Gelder M E, Schwope I, Bolt-de Vries J, Harbeck N, Koenig T, Hartmann O, Kluth A, Dietrich D, Magdolen V, Portengen H, Look M P, Klijn J G, Lesche R, Schmitt M, Maier S, Foekens J A, Martens J W. DNA hypermethylation of PITX2 is a marker of poor prognosis in untreated lymph node-negative hormone receptor-positive breast cancer patients. Breast Cancer Res Treat: 2008; 111 429 437
28. Wang Q, Williamson M, Bott S, Brookman-Amissah N, Freeman A, Nariculam J, Hubank M J, Ahmed A, Masters J R. Hypomethylation of WNT5A, CRIP1 and S100P in prostate cancer. Oncogene: 2007; 26 6560 6565 (Pubitemid 47530597)
29. Damon S E, Plymate S R, Carroll J M, Sprenger C C, Dechsukhum C, Ware J L, Roberts C T Jr. Transcriptional regulation of insulin-like growth factor-I receptor gene expression in prostate cancer cells. Endocrinology: 2001; 142 21 27 (Pubitemid 32183661)
30. Snoek R, Bruchovsky N, Kasper S, Matusik R J, Gleave M, Sato N, Mawji N R, Rennie P S. Differential transactivation by the androgen receptor in prostate cancer cells. Prostate: 1998; 36 256 263 (Pubitemid 28387881)
31. Werner H, Rauscher F J III, Sukhatme V P, Drummond I A, Roberts C T Jr, LeRoith D. Transcriptional repression of the insulin-like growth factor I receptor (IGF-I-R) gene by the tumor suppressor WT1 involves binding to sequences both upstream and downstream of the IGF-I-R gene transcription start site. J Biol Chem: 1994; 269 12577 12582
32. Park J K, Ryu J K, Yoon W J, Lee S H, Lee G Y, Jeong K S, Kim Y T, Yoon Y B. The role of quantitative NPTX2 hypermethylation as a novel serum diagnostic marker in pancreatic cancer. Pancreas: 2012; 41 95 101
33. Zhang L, Gao J, Li L, Li Z, Du Y, Gong Y. The neuronal pentraxin II gene (NPTX2) inhibit proliferation and invasion of pancreatic cancer cells in vitro. Mol Biol Rep: 2011; 38 4903 4911
34. Winter S F, Acevedo V D, Gangula R D, Freeman K W, Spencer D M, Greenberg N M. Conditional activation of FGFR1 in the prostate epithelium induces angiogenesis with concomitant differential regulation of Ang-1 and Ang-2. Oncogene: 2007; 26 4897 4907 (Pubitemid 47172640)
35. Jee C D, Kim M A, Jung E J, Kim J, Kim W H. Identification of genes epigenetically silenced by CpG methylation in human gastric carcinoma. Eur J Cancer: 2009; 45 1282 1293
36. Morrissey C, True L D, Roudier M P, Coleman I M, Hawley S, Nelson P S, Coleman R, Wang Y C, Corey E, Lange P H, Higano C S, Vessella R L. Differential expression of angiogenesis associated genes in prostate cancer bone, liver and lymph node metastases. Clin Exp Metastasis: 2008; 25 377 388
37. Kioussi C, Briata P, Baek S H, Rose D W, Hamblet N S, Herman T, Ohgi K A, Lin C, Gleiberman A, Wang J, Brault V, Ruiz-Lozano P, Nguyen H D, Kemler R, Glass C K, Wynshaw-Boris A, Rosenfeld M. Identification of a Wnt/Dvl/beta-Catenin→Pitx2 pathway mediating cell-type-specific proliferation during development. Cell: 2002; 111 673 685 (Pubitemid 35441249)
38. Jeronimo C, Esteller M. DNA methylation markers for prostate cancer with a stem cell twist. Cancer Prev Res: 2010; 3 1053 1055
39. Singal R, van Wert J, Bashambu M. Cytosine methylation represses glutathione S-transferase P1 (GSTP1) gene expression in human prostate cancer cells. Cancer Res: 2001; 61 4820 4826 (Pubitemid 32691897)
40. Kuzmin I, Gillespie J W, Protopovov A, Geil L, Dreijerink K, Yang Y, Vocke C D, Duh F-M, Zabarovsky E, Minna J D, Rhim J S, Emmert-Buck M R, Linehan W M, Lerman M I. The RASSF1A tumor suppressor gene is inactivated in prostate tumor and suppresses growth of prostate carcinoma cells. Cancer Res: 2002; 62 3498 3502 (Pubitemid 34651398)
41. Fiori A R, Steinhoff C, Muller M, Seifert H H, Hader C, Engers R, Ackermann R, Schulz W A. Coordinate hypermethylation at specific genes in prostate carcinoma precedes LINE-1 hypomethylation. Br J Cancer: 2004; 91 985 994 (Pubitemid 39273795)
42. Kang G H, Lee S W, Lee H J, Hwang K S. Aberrant CpG island hypermethylation of multiple genes in prostate cancer and prostatic intraepithelial neoplasia. J Pathol: 2004; 202 233 240 (Pubitemid 38208661)
43. Lind A J, Wikström P, Granfors T, Egevad L, Stattin P, Bergh A. Angiopoietin 2 expression is related to histological grade, vascular density, metastases, and outcome in prostate cancer. Prostate: 2005; 62 394 399 (Pubitemid 40224144)
44. Semina E V, Reiter R, Leysens N J, Alward W L, Small K W, Datson N A, Siegel-Bartelt J, Bierke-Nelson D, Bitoun P, Zabel B U, Carey J C, Murray J. Cloning and characterization of a novel bicoid-related homeobox transcription factor gene, RIEG, involved in Rieger syndrome. Nature Genet: 1996; 14 392 399 (Pubitemid 26414582)
45. Cox C J, Espinoza H M, McWilliams B, Chappell K, Morton L, Hjalt T A, Semina E V, Amendt B A. Differential regulation of gene expression by PITX2 isoforms. J Biol Chem: 2002; 277 25001 25010 (Pubitemid 34951803)
46. Bañez L L, Sun L, van Leenders G J, Wheeler T M, Bangma C H, Freedland S J, Ittmann M M, Lark A L, Madden J F, Hartman A, Weiss G, Castaños-Vélez E. Multicenter clinical validation of PITX2 methylation as a prostate specific antigen recurrence predictor in patients with post-radical prostatectomy prostate cancer. J Urol: 2010; 184 149 156
47. Vinarskaja A, Schulz W A, Ingenwerth M, Hader C, Arsov C. Association of PITX2 mRNA down-regulation in prostate cancer with promoter hypermethylation and poor prognosis. Urol Oncol: 2011; July 29 [Epub ahead of print]
48. Weiss G, Cottrell S, Distler J, Schatz P, Kristiansen G, Ittmann M, Haefliger C, Lesche R, Hartmann A, Corman J, Wheeler T. DNA methylation of the PITX2 gene promoter region is a strong independent prognostic marker of biochemical recurrence in patients with prostate cancer after radical prostatectomy. J Urol: 2009; 181 1678 1685
49. Steiner I, Jung K, Schatz P, Horns T, Wittschieber D, Lein M, Dietel M, Erbersdobler A. Gene promoter methylation and its potential relevance in early prostate cancer diagnosis. Pathobiology: 2010; 77 260 266
50. Schatz P, Dietrich D, Koenig T, Burger M, Lukas A, Fuhrmann I, Kristiansen G, Stoehr R, Schuster M, Lesche R, Weiss G, Corman J, Hartmann A. Development of a diagnostic microarray assay to assess the risk of recurrence of prostate cancer based on PITX2 DNA methylation. J Mol Diag: 2010; 12 345 353
51. Vanaja D K, Ehrich M, Van den Boom D, Cheville J C, Karnes R J, Tindall D J, Cantor C R, Young C Y. Hypermethylation of genes for diagnosis and risk stratification of prostate cancer. Cancer Invest: 2009; 27 549 560
52. Lin H K, Yeh S, Kang H Y, Chang C. Akt suppresses androgen-induced apoptosis by phosphorylating and inhibiting androgen receptor. Proc Natl Acad Sci USA: 2001; 98 7200 7205 (Pubitemid 32567926)
53. Orio F, Terouanne B, Georget V, Lumbroso S, Avances C, Siatka C, Sultan C. Potential action of IGF-I and EGF on androgen receptor nuclear transfer and transactivation in normal and cancer human prostate cell lines. Mol Cell Endocrinol: 2002; 198 105 114 (Pubitemid 36169940)
54. Pandini G, Mineo R, Frasca F, Roberts C T Jr, Marcelli M, Vigneri R, Belfiore A. Androgens up-regulate the insulin-like growth factor-I receptor in prostate cancer cells. Cancer Res: 2005; 65 1849 1857 (Pubitemid 40478613)