Androgen receptor activation results in metabolite signatures of an aggressive prostate cancer phenotype: An NMR-based metabonomics study

Metabolomics

Volumn 8, Issue 6, 2012, Pages 1026-1036

  MacKinnon, Neil ^a   Khan, Amjad P ^b   Chinnaiyan, Arul M ^b   Rajendiran, Thekkelnaycke M ^b   Ramamoorthy, Ayyalusamy ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Androgen; LnCAP; Metabonomic; NMR; Prostate cancer; R1881

Indexed keywords

ANDROGEN RECEPTOR; INOSITOL; METRIBOLONE; PHOSPHORYLCHOLINE; SELECTIVE ANDROGEN RECEPTOR MODULATOR; SUGAR;

ARTICLE; CANCER GROWTH; CARBOHYDRATE METABOLISM; CONTROLLED STUDY; DISEASE ASSOCIATION; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; MASS SPECTROMETRY; METABOLOMICS; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE; PHENOTYPE; PROSTATE CANCER; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTON NUCLEAR MAGNETIC RESONANCE; SENSITIVITY ANALYSIS;

EID: 84868364473     PISSN: 15733882     EISSN: 15733890     Source Type: Journal    
DOI: 10.1007/s11306-012-0398-4     Document Type: Article

References (58)

1. Ackerstaff, E., Pfug, B. R., Nelson, J. B., & Bhujwalla, Z. M. (2001). Detection of increased choline compounds with proton nuclear magnetic resonance spectroscopy subsequent to malignant transformation of human prostatic epithelial cells. Cancer Research, 61, 3599-3603.
2. 1H HR-MAS spectroscopy of prostate tissue. Magnetic Resonance in Medicine, 61, 525-532.
3. Baek, S. H., Ohgi, K. A., Nelson, C. A., Welsbie, D., Chen, C., Sawyers, C. L., et al. (2006). Ligand-specific allosteric regulation of coactivator functions of androgen receptor in prostate cancer cells. Proceedings of the National Academy of Sciences of the USA, 103, 3100-3105.
4. Bao, B. Y., Chuang, B. F., Wang, Q., Sartor, O., Balk, S. P., Brown, M., et al. (2008). Androgen receptor mediates the expression of UDP-glucuronosyltransferase 2 BI5 and BI7 genes. The Prostate, 68, 839-848.
5. 1H-NMR spectroscopy and self-organizing maps. NMR in Biomedicine, 16, 1-11.
6. Butcher, N. J., Tetlow, N. L., Cheung, C., Broadhurst, G. M., & Minchin, R. F. (2007). Induction of human arylamine N-acetyltransferase type i by androgens in human prostate cancer cells. Cancer Research, 67, 85-92.
7. Cai, C., Wang, H., Xu, Y., Chen, S., & Balk, S. P. (2009). Reactivation of androgen receptor-regulated TMPRSS2: ERG gene expression in castration-resistant prostate cancer. Cancer Research, 69, 6027-6032.
8. Cai, J., Kandagatla, P., Singareddy, R., Kropinski, A., Sheng, S., Cher, M. L., et al. (2010). Androgens induce functional CXCR4 through ERG factor expression in TMRPRSS2-ERG fusion-positive prostate cancer cells. Translational Oncology, 3, 195-203.
9. Chen, M., Tanner, M., Levine, A. C., Levina, E., Ohouo, P., & Buttyan, R. (2009). Androgenic regulation of hedgehog signaling pathway components in prostate cancer cells. Cell Cycle, 8, 149-157.
10. 1H NMR spectroscopy at 9. 4 T. FEBS Letters, 494(1-2), 112-116.
11. Cheng, L. L., Burns, M. A., Taylor, J. L., He, W., Halperin, E. F., McDougal, W. S., et al. (2005). Metabolic characterization of human prostate cancer with tissue magnetic resonance spectroscopy. Cancer Research, 65, 3030-3034.
12. Chipuk, J. E., Cornelius, S. C., Pultz, N. J., Jorgensen, J. S., Bonham, M. J., Kim, S. J., et al. (2002). The androgen receptor represses transforming growth factor-β signaling through interaction with Smad3. The Journal of Biological Chemistry, 277, 1240-1248.
13. Church, D. R., Lee, E., Thompson, T. A., Basu, H. S., Ripple, M. O., Ariazi, R. A., et al. (2005). Induction of AP-I activity by androgen activation of the androgen receptor in LNCaP human prostate carcinoma cells. The Prostate, 63, 155-168.
14. Costello, L. C., Franklin, R. B., & Narayan, P. (1999). Citrate in the diagnosis of prostate cancer. The Prostate, 38, 237-245.
15. Damber, J. E., & Aus, G. (2008). Prostate cancer. Lancet, 37, 1710-1721.
16. 1H NMR metabonomics. Analytical Chemistry, 78, 4281-4290.
17. Feldman, B. J., & Feldman, D. (2001). The development of androgen-independent prostate cancer. Nature Reviews Cancer, 1, 34-45.
18. Flammand, V., Zhao, H., & Peehl, D. M. (2010). Targeting monoamine oxidase A in advanced prostate cancer. Journal of Cancer Research and Clinical Oncology, 136, 1761-1771.
19. Gannon, P. O., Godin-Ethier, J., Hassler, M., Delvoye, N., Aversa, M., Poisson, A. O., et al. (2010). Androgen-regulated expression of arginase 1, arginase 2 and interleukin-8 in human prostate cancer. PLoS ONE, 5, doi: 10. 1371/journal. pone. 0012107.
20. Gavrielides, M. V., Gonzalez-Guerrico, A. M., Riobo, N. A., & Kazanietz, M. G. (2006). Androgens regulate protein kinase Cδ transcription and modulate its apoptotic function in prostate cancer cells. Cancer Research, 66, 11792-11801.
21. Hobisch, A., Eder, I. E., Putz, T., Horninger, W., Bartsch, G., Klocker, H., et al. (1998). Interleukin-6 regulates prostate-specific protein expression in prostate carcinoma cells by activation of the androgen receptor. Cancer Research, 58, 4640-4645.
22. Jackson, J. E. (1991). A user's guide to principal components. New York: Wiley.
23. Jennbacken, K., Gustavsson, H., Tešan, T., Horn, M., Vallbo, C., Welén, K., et al. (2009). The prostatic environment suppresses growth of androgen-independent prostate cancer xenografts: An effect influenced by testosterone. The Prostate, 69, 1164-1175.
24. Kimura, K., Markowski, M., Bowen, C., & Gelmann, E. P. (2001). Androgen blocks apoptosis of hormone-dependent prostate cancer cells. Cancer Research, 61, 5611-5618.
25. Lee, Y. C., Cheng, C. J., Huang, M., Bilen, M. A., Ye, X., Navone, N. M., et al. (2010). Androgen depletion up-regulates cadherin-11 expression in prostate cancer. Journal of Pathology, 221, 68-76.
26. 13C] pyruvate as a metabolic substrate. Magnetic Resonance in Medicine, 62, 1091-1098.
27. Loberg, R. D., McGregor, N., Ying, C., Sargent, E., & Pienta, K. J. (2007). In vivo evaluation of AT-101 (R-(-)-gossypol acetic acid) in androgen-independent growth of VCaP prostate cancer cells in combination with surgical castration. Neoplasia, 9, 1030-1037.
28. Makkonen, H., Kauhanen, M., Jääskeläinen, T., & Palvimo, J. J. (2011). Androgen receptor amplification is reflected in the transcriptional responses of vertebral-cancer of the prostate cells. Molecular and Cellular Endocrinology, 331, 57-65.
29. Mani, R. S., Tomlins, S. A., Callahan, K., Ghosh, A., Nyati, M. K., Varambally, S., et al. (2009). Induced chromosomal proximity and gene fusions in prostate cancer. Science, 326, 1230.
30. Massie, C. E., Lynch, A., Ramos-Montoya, A., Boren, J., Stark, R., Fazli, L., et al. (2011). The androgen receptor fuels prostate cancer by regulating central metabolism and biosynthesis. The EMBO Journal, 1-15, doi: 10. 1038/emboj. 2011. 158.
31. Migliaccio, A., Castoria, G., Di Domenico, M., de Falco, A., Bilancio, A., Lombardi, M., et al. (2000). Steroid-induced androgen receptor-oestradiol receptor β-Src complex triggers prostate cancer cell proliferation. The EMBO Journal, 19, 5406-5417.
32. Nicholson, J. K., Focall, P. J. D., Spraul, M., Farrant, R. D., & Lindon, J. C. (1995). 750 MHz 1H and 1H-13C NMR spectroscopy of human blood plasma. Analytical Chemistry, 67, 793-811.
33. Park, S. Y., Kim, Y. J., Gao, A. C., Mohler, J. L., Onate, S. A., Hidalgo, A. A., et al. (2006). Hypoxia increases androgen receptor activity in prostate cancer cells. Cancer Research, 66, 5121-5129.
34. Putluri, N., Shojaie, A., Vasu, V. T., Nalluri, S., Vareed, S. K., Putluir, V., et al. (2011). Metabolomic profiling reveals a role for androgen in activating amino acid metabolism and methylation in prostate cancer cells. PLoS ONE, 6, doi: 10. 1371/journal. pone. 0021417.
35. Qi, H., Fillion, C., Labrie, Y., Grenier, J., Fournier, A., Berger, L., et al. (2002). AlbZIP, a novel bZIP gene located on chromosome 1q21. 3 that is highly expressed in prostate tumors and of which the expression is up-regulated by androgens in LNCaP human prostate cancer cells. Cancer Research, 62, 721-733.
36. Rantalainen, M., Cloarec, O., Beckonert, O., Wilson, I. D., Jackson, D., Tonge, R., et al. (2006). Statistically integrate metabonomic-proteomic studies on a human prostate cancer xenograft model in mice. Journal of Proteome Research, 5, 2642-2655.
37. Ross, B. D. (1991). Biochemical considerations in 1H spectroscopy. Glutamate and glutamine; Myo-inositol and related metabolites. NMR in Biomedicine, 4, 59-63.
38. Serkova, N. J., Gamito, E. J., Jones, R. H., O'Donnell, C., Brown, J. L., Green, S., et al. (2008). The metabolites citrate, myo-inositol, and spermine are potential age-independent markers of prostate cancer in human expressed prostatic secretions. The Prostate, 68, 620-628.
39. Sitter, B., Sonnewald, U., Spraul, M., Fjösne, H. E., & Gribbestad, I. S. (2002). High-resolution magic angle spinning MRS of breast cancer tissue. NMR in Biomedicine, 15, 327-337.
40. 2-induced responses through transcriptional down-regulation of Smad3 in prostate epithelial cells. Molecular Endocrinology, 24, 2019-2029.
41. Sreekumar, A., Poisson, L. M., Rajendiran, T. M., Khan, A. P., Cao, Q., Yu, J., et al. (2009). Metabolomic profiles delineate potential role for sarcosine in prostate cancer progression. Nature, 457, 910-915.
42. Swanson, M. G., Vigneron, D. B., Tabatabai, Z. L., Males, R. G., Schmitt, L., Carroll, P. R., et al. (2003). Proton HR-MAS spectroscopy and quantitative pathologic analysis of MRI/3D-MRSI-targeted postsurgical prostate tissues. Magnetic Resonance in Medicine, 50, 944-954.
43. 1H HR-MAS spectroscopy. Magnetic Resonance in Medicine, 55, 1257-1264.
44. Swanson, M. G., Keshari, K. R., Tabatabai, Z. L., Simko, J. P., Shinohara, K., Carroll, P. R., et al. (2008). Quantification of choline- and ethanolamine-containing metabolites in human prostate tissues using 1H HR-MAS total correlation spectroscopy. Magnetic Resonance in Medicine, 60, 33-40.
45. Teahan, O., Bevan, C. L., Waxman, J., & Keun, H. C. (2010). Metabolic signatures of malignant progression in prostate epithelial cells. International Journal of Biochemistry and Cell Biology,. doi: 10. 1016/j. biocel. 2010. 07. 003.
46. 1H HR-MAS spectroscopy of biopsy tissues. Magnetic Resonance in Medicine, 60, 510-516.
47. 1H-NMR analysis: Evidence for unusual phospholipid metabolism. The Prostate, 68, 1035-1047.
48. 1H nuclear magnetic resonance analysis of intact prostatic hyperplastic and tumour tissues. Analytical Communications, 35, 113-115.
49. Tomlins, S. A., Rhodes, D. R., Perner, S., Dhanasekaran, S. M., Mehra, R., Sun, X. W., et al. (2005). Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science, 310, 644-648.
50. Tomlins, S. A., Laxman, B., Varambally, S., Cao, X., Yu, J., Helgeson, B. E., et al. (2008). Role of the TMPRSS2-ERG gene fusion in prostate cancer. Neoplasia, 10, 177-188.
51. van Asten, J. J. A., Cuijpers, V., van de Hulsbergen-Kaa, C., Soede-Huijbregts, C., Witjes, J. A., Verhofstad, A., et al. (2008). High resolution magic angle spinning NMR spectroscopy for metabolic assessment of cancer presence and Gleason score in human prostate needle biopsies. Magnetic Resonance Materials in Physics Biology and Medicine, 21, 435-442.
52. 1H NMR spectra for improved metabolic biomarker recovery. Analytical Chemistry, 81, 56-66.
53. Wang, Q., Li, W., Zhang, Y., Yuan, X., Xu, K., Yu, J., et al. (2009). Androgen receptor regulates a distinct transcription program in androgen-independent prostate cancer. Cell, 138, 245-256.
54. Wong, J. W. H., Cagney, G., & Cartwright, H. M. (2005a). SpecAlign-processing and alignment of mass spectra datasets. Bioinformatics, 21, 2088-2090.
55. Wong, J. W. H., Durante, C., & Cartwright, H. M. (2005b). Application of fast fourier transform cross-correlation for the alignment of large chromatographic and spectral datasets. Analytical Chemistry, 77, 5655-5661.
56. Wu, C., Taylor, J. L., He, W., Zepeda, A. G., Halperin, E. F., Bielecki, A., et al. (2003). Proton high-resolution magic angle spinning NMR analysis of fresh and previously frozen tissue of human prostate. Magnetic Resonance in Medicine, 50, 1307-1311.
57. Yu, J., Yu, J., Mani, R. S., Cao, Q., Brenner, C. J., Cao, X., et al. (2010). An integrated network of androgen receptor, polycomb, and TMPRSS2-ERG gene fusions in prostate cancer progression. Cancer Cell, 17, 443-454.
58. Zhu, H., Mazor, M., Kawano, Y., Walker, M. M., Leung, H. Y., Armstrong, K., et al. (2004). Analysis of Wnt gene expression in prostate cancer: Mutual inhibition of WNT11 and the androgen receptor. Cancer Research, 2004(64), 7918-7926.