Subgroups of Castration-resistant Prostate Cancer Bone Metastases Defined Through an Inverse Relationship Between Androgen Receptor Activity and Immune Response

European Urology

Volumn 71, Issue 5, 2017, Pages 776-787

  Ylitalo, Erik Bovinder ^a   Thysell, Elin ^a   Jernberg, Emma ^a   Lundholm, Marie ^a   Crnalic, Sead ^a   Egevad, Lars ^b   Stattin, Pär ^a   Widmark, Anders ^a   Bergh, Anders ^a   Wikström, Pernilla ^a  

^a UMEÅ UNIVERSITY   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Bone metastasis; Castration resistance; Immune response; Metabolism; Prostate cancer

Indexed keywords

ANDROGEN RECEPTOR; CD3 ANTIGEN; CHLORDANE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; AR PROTEIN, HUMAN; CYSTEINE PROTEINASE; FOXA1 PROTEIN, HUMAN; HEPATOCYTE NUCLEAR FACTOR 3ALPHA; HLA A ANTIGEN; HOMEODOMAIN PROTEIN; HOXB13 PROTEIN, HUMAN; KALLIKREIN; KALLIKREIN-RELATED PEPTIDASE 3, HUMAN; KLK2 PROTEIN, HUMAN; LMP-2 PROTEIN; MEMBRANE PROTEIN; MESSENGER RNA; NKX3-1 PROTEIN, HUMAN; OXIDOREDUCTASE; PROSTATE SPECIFIC ANTIGEN; SERINE PROTEINASE; STEAP2 PROTEIN, HUMAN; TAP1 PROTEIN, HUMAN; TMPRSS2 PROTEIN, HUMAN; TRANSCRIPTION FACTOR; TRANSPORTER ASSOCIATED WITH ANTIGEN PROCESSING 1; TUMOR PROTEIN;

ADULT; AGED; ARTICLE; BONE METASTASIS; CANCER STAGING; CASTRATION RESISTANT PROSTATE CANCER; DOWN REGULATION; FOLLOW UP; GENE; HLA A GENE; HUMAN; HUMAN TISSUE; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; KLK2 GENE; KLK3 GENE; MAJOR CLINICAL STUDY; MALE; NKX3.1 GENE; PRINCIPAL COMPONENT ANALYSIS; PRIORITY JOURNAL; PROSTATE HYPERTROPHY; PROTEIN EXPRESSION; PSMB9 GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEAP2 GENE; TAP1 GENE; TMPRSS2 GENE; TRANSURETHRAL RESECTION; WHOLE GENOME SEQUENCING; BONE TUMOR; CASE CONTROL STUDY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; MIDDLE AGED; MULTIVARIATE ANALYSIS; PATHOLOGY; SECONDARY; VERY ELDERLY;

AGED; AGED, 80 AND OVER; ATP-BINDING CASSETTE SUB-FAMILY B MEMBER 2; BONE NEOPLASMS; CASE-CONTROL STUDIES; CYSTEINE ENDOPEPTIDASES; GENE EXPRESSION REGULATION, NEOPLASTIC; HEPATOCYTE NUCLEAR FACTOR 3-ALPHA; HLA-A ANTIGENS; HOMEODOMAIN PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; KALLIKREINS; MALE; MEMBRANE PROTEINS; MIDDLE AGED; MULTIVARIATE ANALYSIS; NEOPLASM PROTEINS; OXIDOREDUCTASES; PRINCIPAL COMPONENT ANALYSIS; PROSTATE-SPECIFIC ANTIGEN; PROSTATIC NEOPLASMS, CASTRATION-RESISTANT; RECEPTORS, ANDROGEN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SERINE ENDOPEPTIDASES; TRANSCRIPTION FACTORS;

EID: 84998693352     PISSN: 03022838     EISSN: 18737560     Source Type: Journal    
DOI: 10.1016/j.eururo.2016.07.033     Document Type: Article

References (36)

1. [1] Nelson, P.S., Molecular states underlying androgen receptor activation: a framework for therapeutics targeting androgen signaling in prostate cancer. J Clin Oncol 30 (2012), 644–646.
2. [2] Omlin, A., Pezaro, C., Gillessen Sommer, S., Sequential use of novel therapeutics in advanced prostate cancer following docetaxel chemotherapy. Ther Adv Urol 6 (2014), 3–14.
3. [3] Hörnberg, E., Ylitalo, E.B., Crnalic, S., et al. Expression of androgen receptor splice variants in prostate cancer bone metastases is associated with castration-resistance and short survival. PLoS One, 6, 2011, e19059.
4. [4] Antonarakis, E.S., Lu, C., Wang, H., et al. AR-V7 and resistance to enzalutamide and abiraterone in prostate cancer. N Engl J Med 371 (2014), 1028–1038.
5. [5] Jernberg, E., Thysell, E., Bovinder Ylitalo, E., et al. Characterization of prostate cancer bone metastases according to expression levels of steroidogenic enzymes and androgen receptor splice variants. PLoS One, 8, 2013, e77407.
6. [6] Crnalic, S., Hörnberg, E., Wikström, P., et al. Nuclear androgen receptor staining in bone metastases is related to a poor outcome in prostate cancer patients. Endocr Relat Cancer 17 (2010), 885–895.
7. [7] Hammarsten, P., Karalija, A., Josefsson, A., et al. Low levels of phosphorylated epidermal growth factor receptor in nonmalignant and malignant prostate tissue predict favorable outcome in prostate cancer patients. Clin Cancer Res 16 (2010), 1245–1255.
8. [8] Eriksson, L., Antti, H., Gottfries, J., et al. Using chemometrics for navigating in the large data sets of genomics, proteomics, and metabonomics (gpm). Anal Bioanal Chem 380 (2004), 419–429.
9. [9] Blades, R.A., Keating, P.J., McWilliam, L.J., George, N.J., Stern, P.L., Loss of HLA class I expression in prostate cancer: implications for immunotherapy. Urology 46 (1995), 681–686.
10. [10] Seliger, B., Stoehr, R., Handke, D., et al. Association of HLA class I antigen abnormalities with disease progression and early recurrence in prostate cancer. Cancer Immunol Immunother 59 (2010), 529–540.
11. [11] Kitamura, H., Torigoe, T., Asanuma, H., Honma, I., Sato, N., Tsukamoto, T., Down-regulation of HLA class I antigens in prostate cancer tissues and up-regulation by histone deacetylase inhibition. J Urol 178 (2007), 692–696.
12. [12] Domingo-Domenech, J., Vidal, S.J., Rodriguez-Bravo, V., et al. Suppression of acquired docetaxel resistance in prostate cancer through depletion of notch- and hedgehog-dependent tumor-initiating cells. Cancer Cell 22 (2012), 373–388.
13. [13] Thysell, E., Surowiec, I., Hörnberg, E., et al. Metabolomic characterization of human prostate cancer bone metastases reveals increased levels of cholesterol. PLoS One, 5, 2010, e14175.
14. [14] Iglesias-Gato, D., Wikström, P., Tyanova, S., et al. The proteome of primary prostate cancer. Eur Urol 69 (2016), 942–952.
15. [15] Mahoney, K.M., Rennert, P.D., Freeman, G.J., Combination cancer immunotherapy and new immunomodulatory targets. Nat Rev Drug Discov 14 (2015), 561–584.
16. [16] Marchesi, M., Andersson, E., Villabona, L., et al. HLA-dependent tumour development: a role for tumour associate macrophages?. J Transl Med, 11, 2013, 247.
17. [17] Strasner, A., Karin, M., Immune Infiltration and Prostate Cancer. Front Oncol, 5, 2015, 128.
18. + regulatory T cells with respect to lethal prostate cancer. Mod Pathol 26 (2013), 448–455.
19. + T cells is associated with clinical outcome in prostate cancer. Eur J Cancer 49 (2013), 1273–1279.
20. [20] Lanciotti, M., Masieri, L., Raspollini, M.R., et al. The role of M1 and M2 macrophages in prostate cancer in relation to extracapsular tumor extension and biochemical recurrence after radical prostatectomy. BioMed Res Int, 2014, 2014, 486798.
21. [21] Tidehag, V., Hammarsten, P., Egevad, L., et al. High density of S100A9 positive inflammatory cells in prostate cancer stroma is associated with poor outcome. Eur J Cancer 50 (2014), 1829–1835.
22. [22] Lundholm, M., Hägglöf, C., Wikberg, M.L., et al. Secreted factors from colorectal and prostate cancer cells skew the immune response in opposite directions. Sci Rep, 5, 2015, 15651.
23. [23] Idorn, M., Kollgaard, T., Kongsted, P., Sengelov, L., Thor Straten, P., Correlation between frequencies of blood monocytic myeloid-derived suppressor cells, regulatory T cells and negative prognostic markers in patients with castration-resistant metastatic prostate cancer. Cancer Immunol Immunother 63 (2014), 1177–1187.
24. [24] Wang, L., Gong, Y., Chippada-Venkata, U., et al. A robust blood gene expression-based prognostic model for castration-resistant prostate cancer. BMC Med, 13, 2015, 201.
25. [25] Saad, F., Miller, K., Current and emerging immunotherapies for castration-resistant prostate cancer. Urology 85 (2015), 976–986.
26. [26] Pomerantz, M.M., Li, F., Takeda, D.Y., et al. The androgen receptor cistrome is extensively reprogrammed in human prostate tumorigenesis. Nat Genet 47 (2015), 1346–1351.
27. [27] Cheng, X.H., Black, M., Ustiyan, V., et al. SPDEF inhibits prostate carcinogenesis by disrupting a positive feedback loop in regulation of the Foxm1 oncogene. PLoS Genet, 10, 2014, e1004656.
28. [28] Kim, I.J., Kang, T.W., Jeong, T., Kim, Y.R., Jung, C., HOXB13 regulates the prostate-derived Ets factor: implications for prostate cancer cell invasion. Int J Oncol 45 (2014), 869–876.
29. [29] Mlecnik, B., Bindea, G., Kirilovsky, A., et al. The tumor microenvironment and immunoscore are critical determinants of dissemination to distant metastasis. Sci Transl Med, 8, 2016 327ra26.
30. [30] Bukur, J., Jasinski, S., Seliger, B., The role of classical and non-classical HLA class I antigens in human tumors. Semin Cancer Biol 22 (2012), 350–358.
31. [31] Chang, C.C., Pirozzi, G., Wen, S.H., et al. Multiple structural and epigenetic defects in the human leukocyte antigen class I antigen presentation pathway in a recurrent metastatic melanoma following immunotherapy. J Biol Chem 290 (2015), 26562–26575.
32. [32] Fonsatti, E., Nicolay, H.J., Sigalotti, L., et al. Functional up-regulation of human leukocyte antigen class I antigens expression by 5-aza-2′-deoxycytidine in cutaneous melanoma: immunotherapeutic implications. Clin Cancer Res 13 (2007), 3333–3338.
33. [33] Gannon, P.O., Poisson, A.O., Delvoye, N., Lapointe, R., Mes-Masson, A.M., Saad, F., Characterization of the intra-prostatic immune cell infiltration in androgen-deprived prostate cancer patients. J Immunol Methods 348 (2009), 9–17.
34. [34] Sorrentino, C., Musiani, P., Pompa, P., Cipollone, G., Di Carlo, E., Androgen deprivation boosts prostatic infiltration of cytotoxic and regulatory T lymphocytes and has no effect on disease-free survival in prostate cancer patients. Clin Cancer Res 17 (2011), 1571–1581.
35. [35] Trigunaite, A., Dimo, J., Jorgensen, T.N., Suppressive effects of androgens on the immune system. Cell Immunol 294 (2015), 87–94.
36. [36] Drake, C.G., Sharma, P., Gerritsen, W., Metastatic castration-resistant prostate cancer: new therapies, novel combination strategies and implications for immunotherapy. Oncogene 33 (2014), 5053–5064.