Siah2-Dependent Concerted Activity of HIF and FoxA2 Regulates Formation of Neuroendocrine Phenotype and Neuroendocrine Prostate Tumors

Cancer Cell

Volumn 18, Issue 1, 2010, Pages 23-38

  Qi, Jianfei ^a   Nakayama, Koh ^b   Cardiff, Robert D ^c   Borowsky, Alexander D ^c   Kaul, Karen ^d,e   Williams, Roy ^a   Krajewski, Stan ^a   Mercola, Dan ^f   Carpenter, Philip M ^f   Bowtell, David ^g   Ronai, Ze'ev A ^a  

^a BURNHAM INSTITUTE   (United States)

^b TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d NORTHSHORE UNIVERSITY HEALTHSYSTEM   (United States)

^e UNIVERSITY OF CHICAGO   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g PETER MACCALLUM CANCER CENTRE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

HEPATOCYTE NUCLEAR FACTOR 3BETA; HYPOXIA INDUCIBLE FACTOR 1ALPHA; PROTEIN P300; PROTEIN SIAH2; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CONTROLLED STUDY; FEMALE; GENE CONTROL; GENE EXPRESSION; GENE HES6; GENE INTERACTION; GENE JMJD1A; GENE PLOD2; GENE SOX9; MALE; METASTASIS; MOUSE; NEUROENDOCRINE DISEASE; NONHUMAN; NUCLEOTIDE SEQUENCE; ONCOGENE; PHENOTYPE; PRIORITY JOURNAL; PROSTATE TUMOR;

MUS;

EID: 77954291438     PISSN: 15356108     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ccr.2010.05.024     Document Type: Article

References (49)

1. Ahmed A.U., Schmidt R.L., Park C.H., Reed N.R., Hesse S.E., Thomas C.F., Molina J.R., Deschamps C., Yang P., Aubry M.C., Tang A.H. Effect of disrupting seven-in-absentia homolog 2 function on lung cancer cell growth. J. Natl. Cancer Inst. 2008, 100:1606-1629.
2. Amarilio R., Viukov S.V., Sharir A., Eshkar-Oren I., Johnson R.S., Zelzer E. HIF1alpha regulation of Sox9 is necessary to maintain differentiation of hypoxic prechondrogenic cells during early skeletogenesis. Development 2007, 134:3917-3928.
3. Aragones J., Fraisl P., Baes M., Carmeliet P. Oxygen sensors at the crossroad of metabolism. Cell Metab. 2009, 9:11-22.
4. Arany Z., Huang L.E., Eckner R., Bhattacharya S., Jiang C., Goldberg M.A., Bunn H.F., Livingston D.M. An essential role for p300/CBP in the cellular response to hypoxia. Proc. Natl. Acad. Sci. USA 1996, 93:12969-12973.
5. Beyer S., Kristensen M.M., Jensen K.S., Johansen J.V., Staller P. The histone demethylases JMJD1A and JMJD2B are transcriptional targets of hypoxia-inducible factor HIF. J. Biol. Chem. 2008, 283:36542-36552.
6. Bonkhoff H. Neuroendocrine cells in benign and malignant prostate tissue: Morphogenesis, proliferation, and androgen receptor status. Prostate Suppl. 1998, 8:18-22.
7. Chiaverotti T., Couto S.S., Donjacour A., Mao J.H., Nagase H., Cardiff R.D., Cunha G.R., Balmain A. Dissociation of epithelial and neuroendocrine carcinoma lineages in the transgenic adenocarcinoma of mouse prostate model of prostate cancer. Am. J. Pathol. 2008, 172:236-246.
8. Cindolo L., Cantile M., Vacherot F., Terry S., de la Taille A. Neuroendocrine differentiation in prostate cancer: from lab to bedside. Urol. Int. 2007, 79:287-296.
9. Cirillo L.A., Lin F.R., Cuesta I., Friedman D., Jarnik M., Zaret K.S. Opening of compacted chromatin by early developmental transcription factors HNF3 (FoxA) and GATA-4. Mol. Cell 2002, 9:279-289.
10. Deeble P.D., Murphy D.J., Parsons S.J., Cox M.E. Interleukin-6- and cyclic AMP-mediated signaling potentiates neuroendocrine differentiation of LNCaP prostate tumor cells. Mol. Cell. Biol. 2001, 21:8471-8482.
11. Deng X., Liu H., Huang J., Cheng L., Keller E.T., Parsons S.J., Hu C.D. Ionizing radiation induces prostate cancer neuroendocrine differentiation through interplay of CREB and ATF2: implications for disease progression. Cancer Res. 2008, 68:9663-9670.
12. Emerling B.M., Weinberg F., Liu J.L., Mak T.W., Chandel N.S. PTEN regulates p300-dependent hypoxia-inducible factor 1 transcriptional activity through Forkhead transcription factor 3a (FOXO3a). Proc. Natl. Acad. Sci. USA 2008, 105:2622-2627.
13. Erbel P.J., Card P.B., Karakuzu O., Bruick R.K., Gardner K.H. Structural basis for PAS domain heterodimerization in the basic helix-loop-helix-PAS transcription factor hypoxia-inducible factor. Proc. Natl. Acad. Sci. USA 2003, 100:15504-15509.
14. Eun B., Lee Y., Hong S., Kim J., Lee H.W., Kim K., Sun W., Kim H. Hes6 controls cell proliferation via interaction with cAMP-response element-binding protein-binding protein in the promyelocytic leukemia nuclear body. J. Biol. Chem. 2008, 283:5939-5949.
15. Foster B.A., Gingrich J.R., Kwon E.D., Madias C., Greenberg N.M. Characterization of prostatic epithelial cell lines derived from transgenic adenocarcinoma of the mouse prostate (TRAMP) model. Cancer Res. 1997, 57:3325-3330.
16. Frew I.J., Hammond V.E., Dickins R.A., Quinn J.M., Walkley C.R., Sims N.A., Schnall R., Della N.G., Holloway A.J., Digby M.R., et al. Generation and analysis of Siah2 mutant mice. Mol. Cell. Biol. 2003, 23:9150-9161.
17. Fukuba H., Takahashi T., Jin H.G., Kohriyama T., Matsumoto M. Abundance of aspargynyl-hydroxylase FIH is regulated by Siah-1 under normoxic conditions. Neurosci. Lett. 2008, 433:209-214.
18. Gingrich J.R., Barrios R.J., Morton R.A., Boyce B.F., DeMayo F.J., Finegold M.J., Angelopoulou R., Rosen J.M., Greenberg N.M. Metastatic prostate cancer in a transgenic mouse. Cancer Res. 1996, 56:4096-4102.
19. Gustafsson M.V., Zheng X., Pereira T., Gradin K., Jin S., Lundkvist J., Ruas J.L., Poellinger L., Lendahl U., Bondesson M. Hypoxia requires notch signaling to maintain the undifferentiated cell state. Dev. Cell 2005, 9:617-628.
20. Hirano D., Jike T., Okada Y., Minei S., Sugimoto S., Yamaguchi K., Yoshikawa T., Hachiya T., Yoshida T., Takimoto Y. Immunohistochemical and ultrastructural features of neuroendocrine differentiated carcinomas of the prostate: an immunoelectron microscopic study. Ultrastruct. Pathol. 2005, 29:367-375.
21. Hofbauer K.H., Gess B., Lohaus C., Meyer H.E., Katschinski D., Kurtz A. Oxygen tension regulates the expression of a group of procollagen hydroxylases. Eur. J. Biochem. 2003, 270:4515-4522.
22. House C.M., Frew I.J., Huang H.L., Wiche G., Traficante N., Nice E., Catimel B., Bowtell D.D. A binding motif for Siah ubiquitin ligase. Proc. Natl. Acad. Sci. USA 2003, 100:3101-3106.
23. Huss W.J., Gregory C.W., Smith G.J. Neuroendocrine cell differentiation in the CWR22 human prostate cancer xenograft: association with tumor cell proliferation prior to recurrence. Prostate 2004, 60:91-97.
24. Huss W.J., Gray D.R., Tavakoli K., Marmillion M.E., Durham L.E., Johnson M.A., Greenberg N.M., Smith G.J. Origin of androgen-insensitive poorly differentiated tumors in the transgenic adenocarcinoma of mouse prostate model. Neoplasia 2007, 9:938-950.
25. Ivan M., Kondo K., Yang H., Kim W., Valiando J., Ohh M., Salic A., Asara J.M., Lane W.S., Kaelin W.G. HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: Implications for O2 sensing. Science 2001, 292:464-468.
26. Kaidi A., Williams A.C., Paraskeva C. Interaction between beta-catenin and HIF-1 promotes cellular adaptation to hypoxia. Nat. Cell Biol. 2007, 9:210-217.
27. Kasper L.H., Boussouar F., Boyd K., Xu W., Biesen M., Rehg J., Baudino T.A., Cleveland J.L., Brindle P.K. Two transactivation mechanisms cooperate for the bulk of HIF-1-responsive gene expression. EMBO J. 2005, 24:3846-3858.
28. Loh Y.H., Zhang W., Chen X., George J., Ng H.H. Jmjd1a and Jmjd2c histone H3 Lys 9 demethylases regulate self-renewal in embryonic stem cells. Genes Dev. 2007, 21:2545-2557.
29. Makino Y., Kanopka A., Wilson W.J., Tanaka H., Poellinger L. Inhibitory PAS domain protein (IPAS) is a hypoxia-inducible splicing variant of the hypoxia-inducible factor-3alpha locus. J. Biol. Chem. 2002, 277:32405-32408.
30. Mirosevich J., Gao N., Gupta A., Shappell S.B., Jove R., Matusik R.J. Expression and role of Foxa proteins in prostate cancer. Prostate 2006, 66:1013-1028.
31. Moller A., House C.M., Wong C.S., Scanlon D.B., Liu M.C., Ronai Z., Bowtell D.D. Inhibition of Siah ubiquitin ligase function. Oncogene 2009, 28:289-296.
32. Monsef N., Helczynski L., Lundwall A., Pahlman S. Localization of immunoreactive HIF-1alpha and HIF-2alpha in neuroendocrine cells of both benign and malignant prostate glands. Prostate 2007, 67:1219-1229.
33. Nakayama K., Frew I.J., Hagensen M., Skals M., Habelhah H., Bhoumik A., Kadoya T., Erdjument-Bromage H., Tempst P., Frappell P.B., et al. Siah2 regulates stability of prolyl-hydroxylases, controls HIF1alpha abundance, and modulates physiological responses to hypoxia. Cell 2004, 117:941-952.
34. Nakayama K., Qi J., Ronai Z. The ubiquitin ligase Siah2 and the hypoxia response. Mol. Cancer Res. 2009, 7:443-451.
35. Nowak J.A., Polak L., Pasolli H.A., Fuchs E. Hair follicle stem cells are specified and function in early skin morphogenesis. Cell Stem Cell 2008, 3:33-43.
36. Qi J., Nakayama K., Gaitonde S., Goydos J.S., Krajewski S., Eroshkin A., Bar-Sagi D., Bowtell D., Ronai Z. The ubiquitin ligase Siah2 regulates tumorigenesis and metastasis by HIF-dependent and -independent pathways. Proc. Natl. Acad. Sci. USA 2008, 105:16713-16718.
37. Ruas J.L., Berchner-Pfannschmidt U., Malik S., Gradin K., Fandrey J., Roeder R.G., Pereira T., Poellinger L. Complex regulation of the transactivation function of hypoxia-inducible factor-1 alpha by direct interaction with two distinct domains of the CREB-binding protein/p300. J. Biol. Chem. 2010, 285:2601-2609.
38. Schmidt R.L., Park C.H., Ahmed A.U., Gundelach J.H., Reed N.R., Cheng S., Knudsen B.E., Tang A.H. Inhibition of RAS-mediated transformation and tumorigenesis by targeting the downstream E3 ubiquitin ligase seven in absentia homologue. Cancer Res. 2007, 67:11798-11810.
39. Sella A., Konichezky M., Flex D., Sulkes A., Baniel J. Low PSA metastatic androgen- independent prostate cancer. Eur. Urol. 2000, 38:250-254.
40. Semenza G.L. Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer 2003, 3:721-732.
41. Shah R.B., Mehra R., Chinnaiyan A.M., Shen R., Ghosh D., Zhou M., Macvicar G.R., Varambally S., Harwood J., Bismar T.A., et al. Androgen-independent prostate cancer is a heterogeneous group of diseases: lessons from a rapid autopsy program. Cancer Res. 2004, 64:9209-9216.
42. Shimizu S., Kumagai J., Eishi Y., Uehara T., Kawakami S., Takizawa T., Koike M. Frequency and number of neuroendocrine tumor cells in prostate cancer: no difference between radical prostatectomy specimens from patients with and without neoadjuvant hormonal therapy. Prostate 2007, 67:645-652.
43. Sotomayor P., Godoy A., Smith G.J., Huss W.J. Oct4A is expressed by a subpopulation of prostate neuroendocrine cells. Prostate 2009, 69:401-410.
44. Sramkoski R.M., Pretlow T.G., Giaconia J.M., Pretlow T.P., Schwartz S., Sy M.S., Marengo S.R., Rhim J.S., Zhang D., Jacobberger J.W. A new human prostate carcinoma cell line, 22Rv1. In Vitro Cell. Dev. Biol. Anim. 1999, 35:403-409.
45. Vias M., Massie C.E., East P., Scott H., Warren A., Zhou Z., Nikitin A.Y., Neal D.E., Mills I.G. Pro-neural transcription factors as cancer markers. BMC Med. Genomics 2008, 1:17.
46. Wang H., Leav I., Ibaragi S., Wegner M., Hu G.F., Lu M.L., Balk S.P., Yuan X. SOX9 is expressed in human fetal prostate epithelium and enhances prostate cancer invasion. Cancer Res. 2008, 68:1625-1630.
47. Yuan T.C., Veeramani S., Lin F.F., Kondrikou D., Zelivianski S., Igawa T., Karan D., Batra S.K., Lin M.F. Androgen deprivation induces human prostate epithelial neuroendocrine differentiation of androgen-sensitive LNCaP cells. Endocr. Relat. Cancer 2006, 13:151-167.
48. Zhang H., Gao P., Fukuda R., Kumar G., Krishnamachary B., Zeller K.I., Dang C.V., Semenza G.L. HIF-1 inhibits mitochondrial biogenesis and cellular respiration in VHL-deficient renal cell carcinoma by repression of C-MYC activity. Cancer Cell 2007, 11:407-420.
49. Zhou Z., Flesken-Nikitin A., Corney D.C., Wang W., Goodrich D.W., Roy-Burman P., Nikitin A.Y. Synergy of p53 and Rb deficiency in a conditional mouse model for metastatic prostate cancer. Cancer Res. 2006, 66:7889-7898.