FOXA1 inhibits prostate cancer neuroendocrine differentiation

Oncogene

Volumn 36, Issue 28, 2017, Pages 4072-4080

  Kim, J ^a   Jin, H ^a   Zhao, J C ^a   Yang, Y A ^a   Li, Y ^b   Yang, X ^a   Dong, X ^b   Yu, J ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; ENOLASE 2; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HEPATOCYTE NUCLEAR FACTOR 3ALPHA; INTERLEUKIN 8; JANUS KINASE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROSTATE SPECIFIC ANTIGEN; STAT3 PROTEIN; SYNAPTOPHYSIN; UNCLASSIFIED DRUG; FOXA1 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER INHIBITION; CASTRATION RESISTANT PROSTATE CANCER; CELL DIFFERENTIATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; MALE; MOUSE; NEUROENDOCRINE PROSTATE CANCER; NONHUMAN; PRIMARY TUMOR; PRIORITY JOURNAL; PROSTATE ADENOCARCINOMA; PROSTATE CANCER; PROTEIN BINDING; PROTEIN EXPRESSION; TUMOR XENOGRAFT; ADENOCARCINOMA; CARCINOMA; DISEASE COURSE; GENETICS; MAPK SIGNALING; NEUROENDOCRINE TUMOR; NEUROSECRETORY CELL; PATHOLOGY; PHYSIOLOGY; PROSTATE TUMOR; TUMOR CELL LINE;

ADENOCARCINOMA; CARCINOMA, NEUROENDOCRINE; CELL DIFFERENTIATION; CELL LINE, TUMOR; DISEASE PROGRESSION; DOWN-REGULATION; HEPATOCYTE NUCLEAR FACTOR 3-ALPHA; HUMANS; MALE; MAP KINASE SIGNALING SYSTEM; NEUROENDOCRINE CELLS; NEUROENDOCRINE TUMORS; PROSTATIC NEOPLASMS;

EID: 85015667988     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2017.50     Document Type: Article

References (58)

1. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2016. CA Cancer J Clin 2016; 66: 7-30.
2. Hirano D, Okada Y, Minei S, Takimoto Y, Nemoto N. Neuroendocrine differentiation in hormone refractory prostate cancer following androgen deprivation therapy. Eur Urol 2004; 45: 586-592; discussion 592.
3. Beltran H, Tagawa ST, Park K, MacDonald T, Milowsky MI, Mosquera JM, et al. Challenges in recognizing treatment-related neuroendocrine prostate cancer. J Clin Oncol 2012; 30: e386-e389.
4. Yuan TC, Veeramani S, Lin FF, Kondrikou D, Zelivianski S, Igawa T, et al. Androgen deprivation induces human prostate epithelial neuroendocrine differentiation of androgen-sensitive LNCaP cells. Endocr Relat Cancer 2006; 13: 151-167.
5. Santoni M, Conti A, Burattini L, Berardi R, Scarpelli M, Cheng L, et al. Neuroendocrine differentiation in prostate cancer: novel morphological insights and future therapeutic perspectives. Biochim Biophys Acta 2014; 1846: 630-637.
6. Sagnak L, Topaloglu H, Ozok U, Ersoy H. Prognostic significance of neuroendocrine differentiation in prostate adenocarcinoma. Clin Genitourin Cancer 2011; 9: 73-80.
7. Culine S, El Demery M, Lamy PJ, Iborra F, Avances C, Pinguet F. Docetaxel and cisplatin in patients with metastatic androgen independent prostate cancer and circulating neuroendocrine markers. J Urol 2007; 178: 844-848; discussion 848.
8. Aparicio AM, Harzstark AL, Corn PG, Wen S, Araujo JC, Tu SM, et al. Platinum-based chemotherapy for variant castrate-resistant prostate cancer. Clin Cancer Res 2013; 19: 3621-3630.
9. Parimi V, Goyal R, Poropatich K, Yang XJ. Neuroendocrine differentiation of prostate cancer: a review. Am J Clin Exp Urol 2014; 2: 273-285.
10. Chen H, Sun Y, Wu C, Magyar CE, Li X, Cheng L, et al. Pathogenesis of prostatic small cell carcinoma involves the inactivation of the P53 pathway. Endocr Relat Cancer 2012; 19: 321-331.
11. Murphy C, McGurk M, Pettigrew J, Santinelli A, Mazzucchelli R, Johnston PG, et al. Nonapical and cytoplasmic expression of interleukin-8, CXCR1, and CXCR2 correlates with cell proliferation and microvessel density in prostate cancer. Clin Cancer Res 2005; 11: 4117-4127.
12. Li Z, Chen CJ, Wang JK, Hsia E, Li W, Squires J, et al. Neuroendocrine differentiation of prostate cancer. Asian J Androl 2013; 15: 328-332.
13. Huang J, Yao JL, Zhang L, Bourne PA, Quinn AM, di Sant'Agnese PA, et al. Differential expression of interleukin-8 and its receptors in the neuroendocrine and non-neuroendocrine compartments of prostate cancer. Am J Pathol 2005; 166: 1807-1815.
14. Wilson C, Purcell C, Seaton A, Oladipo O, Maxwell PJ, O'Sullivan JM, et al. Chemotherapy-induced CXC-chemokine/CXC-chemokine receptor signaling in metastatic prostate cancer cells confers resistance to oxaliplatin through potentiation of nuclear factor-kappaB transcription and evasion of apoptosis. J Pharmacol Exp Ther 2008; 327: 746-759.
15. Mori S, Murakami-Mori K, Bonavida B. Interleukin-6 induces G1 arrest through induction of p27(Kip1), a cyclin-dependent kinase inhibitor, and neuron-like morphology in LNCaP prostate tumor cells. Biochem Biophys Res Commun 1999; 257: 609-614.
16. Bang YJ, Pirnia F, Fang WG, Kang WK, Sartor O, Whitesell L, et al. Terminal neuroendocrine differentiation of human prostate carcinoma cells in response to increased intracellular cyclic AMP. Proc Natl Acad Sci USA 1994; 91: 5330-5334.
17. Cox ME, Deeble PD, Bissonette EA, Parsons SJ. Activated 3', 5'-cyclic AMPdependent protein kinase is sufficient to induce neuroendocrine-like differentiation of the LNCaP prostate tumor cell line. J Biol Chem 2000; 275: 13812-13818.
18. Kim J, Adam RM, Freeman MR. Activation of the Erk mitogen-Activated protein kinase pathway stimulates neuroendocrine differentiation in LNCaP cells independently of cell cycle withdrawal and STAT3 phosphorylation. Cancer Res 2002; 62: 1549-1554.
19. Spiotto MT, Chung TD. STAT3 mediates IL-6-induced neuroendocrine differentiation in prostate cancer cells. Prostate 2000; 42: 186-195.
20. Zhang XQ, Kondrikov D, Yuan TC, Lin FF, Hansen J, Lin MF. Receptor protein tyrosine phosphatase alpha signaling is involved in androgen depletion-induced neuroendocrine differentiation of androgen-sensitive LNCaP human prostate cancer cells. Oncogene 2003; 22: 6704-6716.
21. Song Y, Washington MK, Crawford HC. Loss of FOXA1/2 is essential for the epithelial-To-mesenchymal transition in pancreatic cancer. Cancer Res 2010; 70: 2115-2125.
22. Besnard V, Wert SE, Kaestner KH, Whitsett JA. Stage-specific regulation of respiratory epithelial cell differentiation by Foxa1. Am J Physiol Lung Cell Mol Physiol 2005; 289: L750-L759.
23. Bernardo GM, Lozada KL, Miedler JD, Harburg G, Hewitt SC, Mosley JD, et al. FOXA1 is an essential determinant of ERalpha expression and mammary ductal morphogenesis. Development 2010; 137: 2045-2054.
24. Gao N, LeLay J, Vatamaniuk MZ, Rieck S, Friedman JR, Kaestner KH. Dynamic regulation of Pdx1 enhancers by Foxa1 and Foxa2 is essential for pancreas development. Genes Dev 2008; 22: 3435-3448.
25. Mirosevich J, Gao N, Matusik RJ. Expression of Foxa transcription factors in the developing and adult murine prostate. Prostate 2005; 62: 339-352.
26. Wan H, Dingle S, Xu Y, Besnard V, Kaestner KH, Ang SL, et al. Compensatory roles of Foxa1 and Foxa2 during lung morphogenesis. J Biol Chem 2005; 280: 13809-13816.
27. DeGraff DJ, Grabowska MM, Case TC, Yu X, Herrick MK, Hayward WJ, et al. FOXA1 deletion in luminal epithelium causes prostatic hyperplasia and alteration of differentiated phenotype. Lab Invest 2014; 94: 726-739.
28. Jin HJ, Zhao JC, Wu L, Kim J, Yu J. Cooperativity and equilibrium with FOXA1 define the androgen receptor transcriptional program. Nat Commun 2014; 5: 3972.
29. Jin HJ, Zhao JC, Ogden I, Bergan RC, Yu J. Androgen receptor-independent function of FoxA1 in prostate cancer metastasis. Cancer Res 2013; 73: 3725-3736.
30. Lin D, Dong X, Wang K, Wyatt AW, Crea F, Xue H, et al. Identification of DEK as a potential therapeutic target for neuroendocrine prostate cancer. Oncotarget 2015; 6: 1806-1820.
31. Zhang X, Coleman IM, Brown LG, True LD, Kollath L, Lucas JM, et al. SRRM4 Expression and the Loss of REST Activity May Promote the Emergence of the Neuroendocrine Phenotype in Castration-Resistant Prostate Cancer. Clin Cancer Res 2015; 21: 4698-4708.
32. Beltran H, Rickman DS, Park K, Chae SS, Sboner A, MacDonald TY, et al. Molecular characterization of neuroendocrine prostate cancer and identification of new drug targets. Cancer Discov 2011; 1: 487-495.
33. Beltran H, Prandi D, Mosquera JM, Benelli M, Puca L, Cyrta J, et al. Divergent clonal evolution of castration-resistant neuroendocrine prostate cancer. Nat Med 2016; 22: 298-305.
34. Akamatsu S, Wyatt AW, Lin D, Lysakowski S, Zhang F, Kim S, et al. The placental gene PEG10 promotes progression of neuroendocrine prostate cancer. Cell reports 2015; 12: 922-936.
35. Martin-Orozco RM, Almaraz-Pro C, Rodriguez-Ubreva FJ, Cortes MA, Ropero S, Colomer R, et al. EGF prevents the neuroendocrine differentiation of LNCaP cells induced by serum deprivation: the modulator role of PI3K/Akt. Neoplasia 2007; 9: 614-624.
36. Wightman SC, Uppal A, Pitroda SP, Ganai S, Burnette B, Stack M, et al. Oncogenic CXCL10 signalling drives metastasis development and poor clinical outcome. Br J Cancer 2015; 113: 327-335.
37. Heidemann J, Ogawa H, Dwinell MB, Rafiee P, Maaser C, Gockel HR, et al. Angiogenic effects of interleukin 8 (CXCL8) in human intestinal microvascular endothelial cells are mediated by CXCR2. J Biol Chem 2003; 278: 8508-8515.
38. Venkatakrishnan G, Salgia R, Groopman JE. Chemokine receptors CXCR-1/2 activate mitogen-Activated protein kinase via the epidermal growth factor receptor in ovarian cancer cells. J Biol Chem 2000; 275: 6868-6875.
39. Morris EJ, Jha S, Restaino CR, Dayananth P, Zhu H, Cooper A, et al. Discovery of a novel ERK inhibitor with activity in models of acquired resistance to BRAF and MEK inhibitors. Cancer Discov 2013; 3: 742-750.
40. Li Y, Donmez N, Sahinalp C, Xie N, Wang Y, Xue H, et al. SRRM4 drives neuroendocrine transdifferentiation of prostate adenocarcinoma under androgen receptor pathway inhibition. Eur Urol 2016; 71: 68-78.
41. Grasso CS, Wu YM, Robinson DR, Cao X, Dhanasekaran SM, Khan AP, et al. The mutational landscape of lethal castration-resistant prostate cancer. Nature 2012; 487: 239-243.
42. Wallace TA, Prueitt RL, Yi M, Howe TM, Gillespie JW, Yfantis HG, et al. Tumor immunobiological differences in prostate cancer between African-American and European-American men. Cancer Res 2008; 68: 927-936.
43. Taylor BS, Schultz N, Hieronymus H, Gopalan A, Xiao Y, Carver BS, et al. Integrative genomic profiling of human prostate cancer. Cancer Cell 2010; 18: 11-22.
44. Sun Y, Goodison S. Optimizing molecular signatures for predicting prostate cancer recurrence. Prostate 2009; 69: 1119-1127.
45. Cai C, Wang H, He HH, Chen S, He L, Ma F, et al. ERG induces androgen receptormediated regulation of SOX9 in prostate cancer. J Clin Invest 2013; 123: 1109-1122.
46. Gao N, Zhang J, Rao MA, Case TC, Mirosevich J, Wang Y, et al. The role of hepatocyte nuclear factor-3 alpha (Forkhead Box A1) and androgen receptor in transcriptional regulation of prostatic genes. Mol Endocrinol 2003; 17: 1484-1507.
47. Lupien M, Eeckhoute J, Meyer CA, Wang Q, Zhang Y, Li W, et al. FoxA1 translates epigenetic signatures into enhancer-driven lineage-specific transcription. Cell 2008; 132: 958-970.
48. Wang D, Garcia-Bassets I, Benner C, Li W, Su X, Zhou Y, et al. Reprogramming transcription by distinct classes of enhancers functionally defined by eRNA. Nature 2011; 474: 390-394.
49. Sahu B, Laakso M, Ovaska K, Mirtti T, Lundin J, Rannikko A, et al. Dual role of FoxA1 in androgen receptor binding to chromatin, androgen signalling and prostate cancer. EMBO J 2011; 30: 3962-3976.
50. Chaffer CL, Brennan JP, Slavin JL, Blick T, Thompson EW, Williams ED. Mesenchymal-To-epithelial transition facilitates bladder cancer metastasis: role of fibroblast growth factor receptor-2. Cancer Res 2006; 66: 11271-11278.
51. Korpal M, Ell BJ, Buffa FM, Ibrahim T, Blanco MA, Celia-Terrassa T, et al. Direct targeting of Sec23a by miR-200s influences cancer cell secretome and promotes metastatic colonization. Nat Med 2011; 17: 1101-1108.
52. Terry S, Beltran H. The many faces of neuroendocrine differentiation in prostate cancer progression. Front Oncol 2014; 4: 60.
53. Mosquera JM, Beltran H, Park K, MacDonald TY, Robinson BD, Tagawa ST, et al. Concurrent AURKA and MYCN gene amplifications are harbingers of lethal treatment-related neuroendocrine prostate cancer. Neoplasia 2013; 15: 1-10.
54. Yu J, Cao Q, Mehra R, Laxman B, Yu J, Tomlins SA, et al. Integrative genomics analysis reveals silencing of beta-Adrenergic signaling by polycomb in prostate cancer. Cancer Cell 2007; 12: 419-431.
55. Yu J, Yu J, Mani RS, Cao Q, Brenner CJ, Cao X, et al. An integrated network of androgen receptor, polycomb, and TMPRSS2-ERG gene fusions in prostate cancer progression. Cancer Cell 2010; 17: 443-454.
56. Yu Y, Liu L, Xie N, Xue H, Fazli L, Buttyan R, et al. Expression and function of the progesterone receptor in human prostate stroma provide novel insights to cell proliferation control. J Clin Endocrinol Metab 2013; 98: 2887-2896.
57. Gao J, Aksoy BA, Dogrusoz U, Dresdner G, Gross B, Sumer SO, et al. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci Signal 2013; 6: pl1.
58. Cerami E, Gao J, Dogrusoz U, Gross BE, Sumer SO, Aksoy BA, et al. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov 2012; 2: 401-404.