Angiogenin mediates androgen-stimulated prostate cancer growth and enables castration resistance

Molecular Cancer Research

Volumn 11, Issue 10, 2013, Pages 1203-1214

  Li, Shuping ^a   Hu, Miaofen G ^a   Sun, Yeqing ^c   Yoshioka, Norie ^d   Ibaragi, Soichiro ^d   Sheng, Jinghao ^a   Sun, Guangjie ^b   Kishimoto, Koji ^d   Hu, Guo Fu ^a  

^a TUFTS MEDICAL CENTER   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c DALIAN MARITIME UNIVERSITY   (China)

^d OKAYAMA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTOR; ANGIOGENIN; RIBOSOME RNA; ANDROGEN; ANGIOGENIC FACTOR; PANCREATIC RIBONUCLEASE; PROTEIN BINDING;

ANDROGEN DEPENDENT PROSTATE CANCER; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL; CANCER GROWTH; CARCINOGENESIS; CASTRATION RESISTANT PROSTATE CANCER; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TRANSPORT; RNA SYNTHESIS; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CANCER TRANSPLANTATION; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PATHOLOGY; PROMOTER REGION; PROSTATE TUMOR; SCID MOUSE; TUMOR CELL LINE; XENOGRAFT;

ANDROGENS; ANGIOGENESIS INDUCING AGENTS; ANIMALS; CELL LINE, TUMOR; CELL PROLIFERATION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HETEROGRAFTS; HUMANS; MALE; MICE; MICE, SCID; NEOPLASM TRANSPLANTATION; PROMOTER REGIONS, GENETIC; PROSTATIC NEOPLASMS; PROSTATIC NEOPLASMS, CASTRATION-RESISTANT; PROTEIN BINDING; RECEPTORS, ANDROGEN; RIBONUCLEASE, PANCREATIC; RNA, RIBOSOMAL; TRANSCRIPTION, GENETIC;

EID: 84886428485     PISSN: 15417786     EISSN: 15573125     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-13-0072     Document Type: Article

References (45)

1. Taplin ME. Androgen receptor: role and novel therapeutic prospects in prostate cancer. Expert Rev Anticancer Ther 2008;8:1495-508.
2. Chen Y, Sawyers CL, Scher HI. Targeting the androgen receptor pathway in prostate cancer. Curr Opin Pharmacol 2008;8:440-8.
3. Feldman BJ, Feldman D. The development of androgen-independent prostate cancer. Nat Rev Cancer 2001;1:34-45.
4. Balk SP, Knudsen KE. AR, the cell cycle, and prostate cancer. Nucl Recept Signal 2008;6:e001.
5. Wang Q, Li W, Liu XS, Carroll JS, Janne OA, Keeton EK, et al. A hierarchical network of transcription factors governs androgen receptor- dependent prostate cancer growth. Mol Cell 2007;27:380-92.
6. Yu J, Mani RS, Cao Q, Brenner CJ, Cao X, Wang X, et al. An integrated network of androgen receptor, polycomb, and TMPRSS2-ERG gene fusions in prostate cancer progression. Cancer Cell 2010;17:443-54.
7. Rosenwald IB. Deregulation of protein synthesis as a mechanism of neoplastic transformation. Bioessays 1996;18:243-50.
8. Mainwaring WI, Wilce PA. The control of the form and function of the ribosomesin androgen-dependent tissues by testosterone. Biochem J 1973;134:795-805.
9. Mainwaring WI, Derry NS. Enhanced transcription of rRNA genes by purified androgen receptor complexes in vitro. J Steroid Biochem 1983;19:101-8.
10. Kabler RL, Srinivasan A, Taylor LJ, Mowad J, Rothblum LI, Cavanaugh AH. Androgen regulation of ribosomal RNA synthesis in LNCaP cells and rat prostate. J Steroid Biochem Mol Biol 1996;59:431-9.
11. Fett JW, Strydom DJ, Lobb RR, Alderman EM, Bethune JL, Riordan JF, et al. Isolation and characterization of angiogenin, an angiogenic protein from human carcinoma cells. Biochemistry 1985;24:5480-6.
12. Hirukawa S, Olson KA, Tsuji T, Hu GF. Neamine inhibits xenografic human tumor growth and angiogenesis in athymic mice. Clin Cancer Res 2005;11:8745-52.
13. Ibaragi S, Yoshioka N, Kishikawa H, Hu JK, Sadow PM, Li M, et al. Angiogenin-stimulated ribosomal RNA transcription is essential for initiation and survival of AKT-induced prostate intraepithelial neoplasia. Mol Cancer Res 2009;7:415-24.
14. Ibaragi S, Yoshioka N, Li S, Hu MG, Hirukawa S, Sadow PM, et al. Neamine inhibits prostate cancer growth by suppressing angiogeninmediated ribosomal RNA transcription. Clin Cancer Res 2009;15: 1981-8.
15. Tsuji T, Sun Y, Kishimoto K, Olson KA, Liu S, Hirukawa S, et al. Angiogenin is translocated to the nucleus of HeLa cells and is involved in ribosomal RNA transcription and cell proliferation. Cancer Res 2005;65:1352-60.
16. Yoshioka N, Wang L, Kishimoto K, Tsuji T, Hu GF. A therapeutic target for prostate cancer based on angiogenin-stimulated angiogenesis and cancer cell proliferation. Proc Natl Acad SciUS A 2006;103:14519-24.
17. Tello-Montoliu A, Patel JV, Lip GY. Angiogenin: a review of the pathophysiology and potential clinical applications. J Thromb Haemost 2006;4:1864-74.
18. Katona TM, Neubauer BL, Iversen PW, Zhang S, Baldridge LA, Cheng L. Elevated expression of angiogenin in prostate cancer and its precursors. Clin Cancer Res 2005;11:8358-63.
19. Majumder PK, Yeh JJ, George DJ, Febbo PG, Kum J, Xue Q, et al. Prostate intraepithelial neoplasia induced by prostate restricted Akt activation: the MPAKT model. Proc Natl Acad Sci U S A 2003;100: 7841-6.
20. Olson KA, Byers HR, Key ME, Fett JW. Prevention of human prostate tumor metastasis in athymic mice by antisense targeting of human angiogenin. Clin Cancer Res 2001;7:3598-605.
21. Olson KA, Byers HR, Key ME, Fett JW. Inhibition of prostate carcinoma establishment and metastatic growth in mice by an antiangiogenin monoclonal antibody. Int J Cancer 2002;98:923-9.
22. Soncin F. Angiogenin supports endothelial and fibroblast cell adhesion. Proc Natl Acad Sci U S A 1992;89:2232-6.
23. Moroianu J, Riordan JF. Nuclear translocation of angiogenin in proliferating endothelial cells is essential to its angiogenic activity. Proc Natl Acad Sci U S A 1994;91:1677-81.
24. Xu ZP, Tsuji T, Riordan JF, Hu GF. Identification and characterization of an angiogenin-binding DNA sequence that stimulates luciferase reporter gene expression. Biochemistry 2003;42:121-8.
25. Kao RY, Jenkins JL, Olson KA, Key ME, Fett JW, Shapiro R. A smallmolecule inhibitor of the ribonucleolytic activity of human angiogenin that possesses antitumor activity. Proc Natl Acad Sci U S A 2002;99: 10066-71.
26. Kishimoto K, Liu S, Tsuji T, Olson KA, Hu GF. Endogenous angiogenin in endothelial cells is a general requirement for cell proliferation and angiogenesis. Oncogene 2005;24:445-56.
27. Horoszewicz JS, Leong SS, Kawinski E, Karr JP, Rosenthal H, ChuTM, et al. LNCaP model of human prostatic carcinoma. Cancer Res 1983;43:1809-18.
28. Chavali GB, Papageorgiou AC, Olson KA, Fett JW, Hu G, Shapiro R, et al. The crystal structure of human angiogenin in complex with an antitumor neutralizing antibody. Structure 2003;11:875-85.
29. Nilsson UW, Abrahamsson A, Dabrosin C. Angiogenin regulation by estradiol in breast tissue: tamoxifen inhibits angiogenin nuclear translocation and antiangiogenin therapy reduces breast cancer growth in vivo. Clin Cancer Res 2010;16:3659-69.
30. Aberg UW, Saarinen N, Abrahamsson A, Nurmi T, Engblom S, Dabrosin C. Tamoxifen and flaxseed alter angiogenesis regulators in normal human breast tissue in vivo. PLoS ONE 2011;6: e25720.
31. Hu G, Xu C, Riordan JF. Human angiogenin is rapidly translocated to the nucleus of human umbilical vein endothelial cells and binds toDNA. J Cell Biochem 2000;76:452-62.
32. Badet J, Soncin F, Guitton JD, Lamare O, Cartwright T, Barritault D. Specific binding of angiogenin to calf pulmonary artery endothelial cells. Proc Natl Acad Sci U S A 1989;86:8427-31.
33. Berthold DR, Sternberg CN, Tannock IF. Management of advanced prostate cancer after first-line chemotherapy. J Clin Oncol 2005;23: 8247-52.
34. Petrylak DP, Tangen CM, Hussain MH, Lara PN Jr, Jones JA, Taplin ME, et al. Docetaxel and estramustine compared with mitoxantrone and prednisone for advanced refractory prostate cancer. N Engl J Med 2004;351:1513-20.
35. Tannock IF, de Wit R, Berry WR, Horti J, Pluzanska A, Chi KN, et al. Docetaxel plus prednisone or mitoxantrone plus prednisone for advanced prostate cancer. N Engl J Med 2004;351:1502-12.
36. Mimeault M, Batra SK. Recent advances on multiple tumorigenic cascades involved in prostatic cancer progression and targeting therapies. Carcinogenesis 2006;27:1-22.
37. Schulz WA, Hatina J. Epigenetics of prostate cancer: beyond DNA methylation. J Cell Mol Med 2006;10:100-25.
38. Trotman LC, Niki M, Dotan ZA, Koutcher JA, Di Cristofano A, Xiao A, et al. Pten dose dictates cancer progression in the prostate. PLoS Biol 2003;1:E59.
39. Furuya Y, Krajewski S, Epstein JI, Reed JC, Isaacs JT. Expression of bcl-2 and the progression of human and rodent prostatic cancers. Clin Cancer Res 1996;2:389-98.
40. De Marzo AM, Marchi VL, Epstein JI, Nelson WG. Proliferative inflammatory atrophy of the prostate: implications for prostatic carcinogenesis. Am J Pathol 1999;155:1985-92.
41. Gupta RA, DuBois RN. Combinations for cancer prevention. Nat Med 2000;6:974-5.
42. Moss T. At the crossroads of growth control; making ribosomal RNA. Curr Opin Genet Dev 2004;14:210-7.
43. Moss T, Langlois F, Gagnon-Kugler T, Stefanovsky V. A housekeeper with power of attorney: the rRNA genes in ribosome biogenesis. Cell Mol Life Sci 2007;64:29-49.
44. Ruggero D, Pandolfi PP. Does the ribosome translate cancer? Nat Rev Cancer 2003;3:179-92.
45. Nazar RN. Ribosomal RNA processing and ribosome biogenesis in eukaryotes. IUBMB Life 2004;56:457-65.