Role of androgen receptor expression in non-muscle-invasive bladder cancer: a systematic review and meta-analysis.
Journal
Histology and histopathology
ISSN: 1699-5848
Titre abrégé: Histol Histopathol
Pays: Spain
ID NLM: 8609357
Informations de publication
Date de publication:
May 2020
May 2020
Historique:
pubmed:
6
12
2019
medline:
27
3
2021
entrez:
6
12
2019
Statut:
ppublish
Résumé
In order to evaluate the potential prognostic/predictive role of androgen receptor (AR) expression in non-muscle-invasive bladder cancer (NMIBC), and whether it may represent a therapeutic target, we conducted a systematic search of the literature using 'androgen receptor or AR', 'testosterone', 'bladder cancer' and 'non-muscle invasive bladder cancer or NMIBC' as keywords. Eleven studies met the inclusion/exclusion criteria. No significant association was found between AR status and patients' gender (p=0.232), tumor size (p=0.975), tumor stage (p=0.237), tumor grade (p=0.444), tumor multicentricity (p=0.397), concomitant CIS (p=0.316) and progression of disease (p=0.397). On the other hand, relative lack of AR expression was significantly correlated to recurrent disease (p=0.001). Evidence for a direct correlation between AR expression and recurrence-free survival of patients with NMIBC indicate ARs as potential markers of BC behavior; moreover, the finding of a role of androgen blockade therapy in improving survival highlights the potential clinical application of this pathway, which deserves to be further explored.
Identifiants
pubmed: 31803932
pii: HH-18-189
doi: 10.14670/HH-18-189
doi:
Substances chimiques
AR protein, human
0
Androgens
0
Biomarkers, Tumor
0
Receptors, Androgen
0
Types de publication
Journal Article
Meta-Analysis
Review
Systematic Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
423-432Subventions
Organisme : -
ID : -
Références
Babjuk M., Böhle A., Burger M., Capoun O., Cohen D., Compérat E.M., Hernandez V., Kaasinen E., Palou J., Roupret M., van Rhijn B.W., Shariat S.F., Soukup V., Sylvester R.J. and Zigeuner R. (2017). EAU guidelines on non-muscle-invasive urothelial carcinoma of the bladder: Update 2016. Eur. Urol. 7, 447-461.
pubmed: 27324428
Boorjian S., Ugras S., Mongan N.P., Gudas L.J., You X., Tickoo S.K. and Scherr D.S. (2004). Androgen receptor expression is inversely correlated with pathologic tumor stage in bladder cancer. Urology 64, 383-388.
pubmed: 15302512
Boorjian S.A., Heemers H.V., Frank I., Farmer S.A., Schmidt L.J., Sebo T.J. and Tindall D.J. (2009). Expression and significance of androgen receptor coactivators in urothelial carcinoma of the bladder. Endocr. Relat. Cancer 16, 123-137.
pmcid: PMC2674368
pubmed: 18845648
Bray F., Jemal A., Grey N., Ferlay J. and Forman D (2011). Global cancer transitions according to the Human Development Index (2008-2030): a population-based study. Lancet Oncol. 13, 790-801.
pubmed: 22658655
Burge F. and Kockelbergh R. (2016). Closing the gender gap: Can we improve bladder cancer survival in women? - A systematic review of diagnosis, treatment and outcomes. Urol. Int. 97, 373-379.
pubmed: 27595416
Cantile M., Cindolo L., Napodano G., Altieri V. and Cillo C. (2003). Hyperexpression of locus C genes in the HOX network is strongly associated in vivo with human bladder transitional cell carcinomas. Oncogene 22, 6462-6468.
pubmed: 14508527
Chavan S., Bray F., Lortet-Tieulent J., Goodman M. and Jemal A. (2014). International variations in bladder cancer incidence and mortality. Eur. Urol. 66, 59-73.
pubmed: 24451595
Chen F.L.P., Zhang G., Iwamoto Y. and See W. (2003). Androgen dependent regulation of bacillus Calmette-Guerin induced interleukin-6 expression in human transitional carcinoma cell lines. J. Urol. 170, 2009-2013.
pubmed: 14532843
Chen J., Cui Y., Li P., Liu L., Li C. and Zu X. (2017). Expression and clinical significance of androgen receptor in bladder cancer: A metaanalysis. Mol. Clin. Oncol. 7, 919-927.
pmcid: PMC5700275
pubmed: 29181189
Cicione A., Manno S., Ucciero G., Cantiello F., Damiano R., Lima E., Posti A., Balloni F. and De Nunzio C. (2018). A larger detrusor wall thickness increases the risk of non muscle invasive bladder cancer recurrence and progression: result from a multicenter observational study. Minerva Urol. Nefrol. 70, 310-318.
pubmed: 29241311
Davey R.A. and Grossmann M. (2016). Androgen receptor structure, function and biology: from bench to bedside. Clin. Biochem. Rev. 37, 3-15.
pmcid: PMC4810760
pubmed: 27057074
Dobruch J., Daneshmand S., Fisch M., Lotan Y., Noon A.P., Resnick M.J., Shariat S.F., Zlotta A.R. and Boorjian S.A. (2016). Gender and bladder cancer: A collaborative review of etiology, biology and outcomes. Eur. Urol. 69, 300-310
pmcid: PMC4000496
pubmed: 26346676
Elzamy S., Allah A. and Kandeel W. (2018). The prognostic significance of androgen receptor and beta-catenin immunohistochemical expression in urothelial carcinoma with and without detrusor muscle invasion from an Egyptian institution. Pol. J. Pathol. 69, 234-242.
pubmed: 30509050
Godoy G., Gakis G., Smith C.L. and Fahmy O. (2016). Effects of androgen and estrogen receptor signaling pathways on bladder cancer initiation and progression. Bladder Cancer 2, 127-137.
pmcid: PMC492789
pubmed: 27376135
Hartge P., Harvey E.B., Linehan W.M., Silverman D.T., Sullivan J.W., Hoover R.N. and Fraumeni J.F. (1990). Unexplained excess risk of bladder cancer in men. J. Natl. Cancer Inst. 82, 1636-1640.
pubmed: 2213906
Heinlein C.A. and Chang C. (2004). Androgen receptor in prostate cancer. Endocr. Rev. 25, 276-308.
pubmed: 15082523
Hemelt M., Yamamoto H., Cheng K.K. and Zeegers M.P.A. (2009). The effect of smoking on the male excess of bladder cancer: a metaanalysis and geographical analyses. Int. J. Cancer 124, 412-419.
pubmed: 18792102
Hsu J.W., Hsu I., Xu D., Miyamoto H., Liang L., Wu X.R., Shyr C.R. and Chang C. (2013). Decreased tumorigenesis and mortality from bladder cancer in mice lacking urothelial androgen receptor. Am. J. Pathol. 182, 1811-1820.
pmcid: PMC3644728
pubmed: 23499463
Ide H. and Miyamoto H. (2015). Steroid hormone receptor signals as prognosticators for urothelial tumor. Dis. Markers 2015, 840640.
pmcid: PMC4685115
pubmed: 26770009
Ide H., Inoue S. and Miyamoto H. (2017). Histopathological and prognostic significance of the expression of sex hormone receptors in bladder cancer: A meta-analysis of immunohistochemical studies. PLoS One 12, e0174746.
pmcid: PMC5375178
pubmed: 28362839
Imada S., Akaza H., Ami Y., Koiso K., Ideyama Y. and Takenaka T. (1997). Promoting effects and mechanisms of action of androgen in bladder carcinogenesis in male rats. Eur. Urol. 31, 360-364.
pubmed: 9129932
Inoue S., Mizushima T. and Miyamoto H. (2018). Role of the androgen receptor in urothelial cancer. Mol. Cell. Endocrinol. 465, 73-81.
pubmed: 28652170
Izumi K., Taguri M., Miyamoto H., Hara Y., Kishida T., Chiba K., Murai T., Hirai K., Suzuki K., Fujinami K., Ueki T., Udagawa K., Kitami K., Moriyama M., Miyoshi Y., Tsuchiya F., Ikeda I., Kobayashi K., Sato M., Morita S., Noguchi K. and Uemura H. (2014). Androgen deprivation therapy prevents bladder cancer recurrence. Oncotarget 5, 12665-12674.
pmcid: PMC4350350
pubmed: 25557268
Izumi K., Ito Y., Miyamoto H., Miyoshi Y., Ota J., Moriyama M., Murai T., Hayashi H., Inayama Y., Ohashi K., Yao M. and Uemura H. (2016). Expression of androgen receptor in non-muscle-invasive bladder cancer predicts the preventive effect of androgen deprivation therapy on tumor recurrence.Oncotarget 22, 14153-14160.
pmcid: PMC4924704
pubmed: 26885620
Jing Y., Cui D., Guo W., Jiang J., Jiang B., Lu Y., Zhao W., Wang X., Jiang Q., Han B. and Xia S. (2014). Activated androgen receptor promotes bladder cancer metastasis via Slugmediated epithelialmesenchymal transition. Cancer Lett. 348, 135-145.
pubmed: 24662746
Kauffman E.C., Robinson B.D., Downes M.J., Powell L.G., Lee M.M., Scherr D.S., Gudas L.J. and Mongan N.P. (2011). Role of androgen receptor and associated lysine-demethylasecoregulators, LSD1 and JMJD2A, in localized and advanced human bladder cancer. Mol. Carcinog. 50, 931-944.
pmcid: PMC3315373
pubmed: 21400613
Kawahara T., Shareef H.K., Aljarah A.K., Ide H., Li Y., Kashiwagi E., Netto G.J., Zheng Y. and Miyamoto H. (2015). ELK1 is up-regulated by androgen in bladder cancer cells and promotes tumor progression. Oncotarget 6, 29860-29876.
pmcid: PMC4745768
pubmed: 26342199
Kawahara T., Ide H., Kashiwagi E., El-Shishtawy K.A., Li Y., Reis L.O., Zheng Y. and Miyamoto H. (2016). Enzalutamide inhibits androgen receptor-positive bladder cancer cell growth. Urol. Oncol. 34, 432.e15-e23.
pubmed: 27330033
Kim K., Cho Y.M., Park B.H., Lee J.L., Ro J.Y., Go H. and Shim J.W. (2015). Histological and immunohistochemical markers for progression prediction in transurethrally resected high-grade nonmuscle invasive bladder cancer. Int. J. Clin. Exp. Pathol. 8, 743-750.
pmcid: PMC4348879
pubmed: 25755769
Lamont K.R. and Tindall D.J (2011). Minireview: alternative activation pathways for the androgen receptor in prostate cancer. Mol. Endocrinol. 25, 897-907.
pmcid: PMC3100605
pubmed: 21436259
Li Y., Zheng Y., Izumi K., Ishiguro H., Ye B., Li F. and Miyamoto H. (2013). Androgen activates β-catenin signaling in bladder cancer cells. Endocr. Relat. Cancer 20, 293-304.
pubmed: 23447569
Li Y., Ishiguro H., Kawahara T., Miyamoto Y., Izumi K. and Miyamoto H. (2014). GATA3 in the urinary bladder: Suppression of neoplastic transformation and down-regulation by androgens. Am. J. Cancer Res. 4, 461-473.
pmcid: PMC4163611
pubmed: 25232488
Li P., Chen J. and Miyamoto H. (2017). Androgen receptor signaling in bladder cancer. Cancers 9, 20.
pmcid: PMC5332943
pubmed: 28241422
Lin C., Yang L., Tanasa B., Hutt K., Ju B., Ohgi K.A., Zhang J, Rose D.W., Fu X.D., Glass C.K. and Rosenfeld M.G. (2009). Nuclear receptor-induced chromosomal proximity and DNA breaks underlie specific translocations in cancer. Cell 139, 1069-1083.
pmcid: PMC2812435
pubmed: 19962179
Lin C., Yin Y., Stemler K., Humphrey P., Kibel A.S., Mysorekar I.U. and Ma L. (2013). Constitutive beta-catenin activation induces malespecific tumorigenesis in the bladder urothelium. Cancer Res. 73, 5914-5925.
pmcid: PMC3790859
pubmed: 23928991
Lombard A.P. and Mudryj M. (2015). The emerging role of the androgen receptor in bladder cancer. Endocr. Relat. Cancer 22, R265-277.
pubmed: 26229034
Mashhadi R., Pourmand G., Kosari F., Mehrsai A., Salem S., Pourmand M.R., Alatab S., Khonsari M., Heydari F., Beladi L. and Alizadeh F. (2014). Role of steroid hormone receptors in formation and progression of bladder carcinoma: a case-control study. Urol. J. 11, 1968-1973.
pubmed: 25433476
McBeth L., Grabnar M., Selman S. and Hinds T.D. Jr (2015). Involvement of the androgen and glucocorticoid receptors in bladder cancer. Int. J. Endocrinol. 2015, 384860.
pmcid: PMC4546983
pubmed: 26347776
McGrath M., Michaud D.S. and De Vivo I. (2006). Hormonal and reproductive factors and the risk of bladder cancer in women. Am. J. Epidemiol. 163, 236-244.
pubmed: 16319290
Mir C., Shariat S.F., van der Kwast T.H., Ashfaq R., Lotan Y., Evans A., Skeldon S., Hanna S., Vajpeyi R., Kuk C., Alkhateeb S., Morote J., van Rhijn B.W.G., Bostrom P., Yao J., Miyamoto H., Jewett M., Fleshner N., Messing E. and Zlotta A.R. (2011). Loss of androgen receptor expression is not associated with pathological stage, grade, gender or outcome in bladder cancer: a large multi-institutional study. BJU Int. 108, 24-30.
pubmed: 21070579
Miyamoto H., Yang Z., Chen Y.T., Ishiguro H., Uemura H., Kubota Y., Nagashima Y., Chang Y.J., Hu Y.C., Hu Y.C., Tsai M.Y., Yeh S., Messing E.M. and Chang C. (2007). Promotion of bladder cancer development and progression by androgen receptor signals. J. Natl. Cancer Inst. 99, 558-568
pubmed: 17406000
Miyamoto H., Yao J.L., Chaux A., Zheng Y., Hsu I., Izumi K., Chang C., Messing E.M., Netto G.J. and Yeh S. (2012). Expression of androgen and oestrogen receptors and its prognostic significance in urothelial neoplasm of the urinary bladder. BJU Int. 109, 1716- 1726.
pubmed: 22221549
Moher D., Liberati A., Tetzlaff J. and Altman D.G. (2010). Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. Int. J. Surg. 8, 336-341.
pubmed: 20171303
Morales E.E., Grill S., Svatek R.S., Kaushik D., Thompson I.M. Jr, Ankerst D.P. and Liss M.A. (2016). Finasteride reduces risk of bladder cancer in a large prospective screening study. Eur. Urol. 69, 407-410.
pubmed: 26320383
Nam J.K., Park S.W., Lee S.D. and Chung M.K. (2014). Prognostic value of sex-hormone receptor expression in non-muscle invasive bladder cancer. Yonsei Med. J. 55, 1214-1221.
pmcid: PMC4108804
pubmed: 25048477
Norm D., Sandip M., Amit R., Adam B., Joseph J., Aria R., Chieko M., Todd S., Brandon P. and Gary D. (2016). Bladder cancer mortality in the United States: A geographic and temporal analysis of socioeconomic and environmental factors. J. Urol. 195, 290-296.
pubmed: 26235377
Okajima E., Hiramatsu T., Iriya K., Ijuin M., Matsushima S. and Yamada K. (1975). Effects of sex hormones on development of urinary bladder tumours in rats induced by N-butyl-N-(4- hydroxybutyl) nitrosamine. Urol. Res. 3, 73-79.
pubmed: 1162802
Ouzzani M., Hammady H., Fedorowicz Z. and Elmagarmid A. (2016). Rayyan-a web and mobile app for systematic reviews. Syst. Rev. 5, 210.
pmcid: PMC5139140
pubmed: 27919275
Rahmani A.H., Alzohairy M., Babiker A.Y.Y., Khan A.A., Aly S.M. and Rizvi M.A. (2013). Implication of androgen receptor in urinary bladder cancer: a critical mini review. Int. J. Mol. Epidemiol. Genet. 12, 150-155.
pmcid: PMC3773566
pubmed: 24046807
Rau K.M., Chen Y.J., Sun M.T. and Jang H.Y. (2011). Prognostic effects and regulation of activing A, maspin, and the androgen receptor in upper urinary tract urothelial carcinoma. Anticancer Res. 31, 1713- 1720.
pubmed: 21617230
Reid L.M., Leav I., Kwan P.W., Russell P. and Merk F.B (1984). Characterization of a human, sex steroid-responsive transitional cell carcinoma maintained as a tumor line (R198) in athymic nude mice. Cancer Res. 44, 4560-4573.
pubmed: 6467211
Rosenzweig B.A., Bolina P.S., Birch L., Moran C., Marcovici I. and Prins G.S. (1995). Location and concentration of estrogen, progesterone, and androgen receptors in the bladder and urethra of the rabbit. Neurourol. Urodyn. 14, 87-96.
pubmed: 7742854
Schweizer M.T. and Yu E.Y. (2017). AR-Signaling in human malignancies: Prostate cancer and beyond. Cancers 9, 7.
pmcid: PMC5295778
pubmed: 28085048
Scosyrev E., Noyes K., Geng C. and Messing E. (2009) Sex and racial differences in bladder cancer presentation and mortality in the US. Cancer 115, 68-74.
pubmed: 19072984
Shang Z., Li Y., Zhang M., Tian J., Han R., Shyr C.R., Messing E., Yeh S., Niu Y. and Chang C. (2015). Antiandrogen therapy with hydroxyflutamide or androgen receptor degradation enhancer ASCJ9 enhances BCG efficacy to better suppress bladder cancer progression. Mol. Cancer Ther. 14, 2586-2594.
pmcid: PMC4704455
pubmed: 26264279
Shiota M., Yokomizo A., Takeuchi A., Imada K., Kiyoshima K., Inokuchi J., Tatsugami K., Ohga S., Nakamura K., Honda H. and Naito S. (2015). Secondary bladder cancer after anticancer therapy for prostate cancer: reduced comorbidity after androgen-deprivation therapy. Oncotarget 6, 14710-14719.
pmcid: PMC4546499
pubmed: 25900243
Shiota M., Kiyoshima K., Yokomizo A., Takeuchi A., Kashiwagi E., Dejima T., Takahashi R., Inokuchi J., Tatsugami K. and Eto M. (2017). Suppressed recurrent bladder cancer after androgen suppression with androgen deprivation therapy or 5alpha-reductase inhibitor. J. Urol. 197, 308-313.
pubmed: 27506696
Shortliffe L.M.D., Ye Y., Behr B. and Wang B. (2014). Testosterone changes bladder and kidney structure in juvenile male rats. J. Urol. 191, 1913-1919.
pubmed: 24518779
Shyr C.R., Chen C.C., Hsieh T.F., Chang C.H., Ma W.L., Yeh S., Messing E., Li T.H., Li F.Y. and Chang C. (2013). The expression and actions of androgen receptor in upper urinary tract urothelial carcinoma (UUTUC) tissues and the primary cultured cells. Endocrine 43, 191-199.
pubmed: 22851332
Sievert K.D., Amend B., Nagele U., Schilling D., Bedke J., Horstmann M., Hennenlotter J., Kruck S. and Stenzl A. (2009). Economic aspects of bladder cancer: What are the benefits and costs? World J. Urol. 27, 295-300.
pmcid: PMC2694315
pubmed: 19271220
Sikic D., Breyer J., Hartmann A., Burger M., Erben P., Denzinger S., Eckstein M., Stöhr R., Wach S., Wullich B., Keck B., Wirtz R.M. and Otto W. (2017). High androgen receptor mRNA expression is independently associated with prolonged cancer-specific and recurrence-free survival in stage T1 bladder cancer. Transl. Oncol. 10, 340-345.
pmcid: PMC5367846
pubmed: 28342317
Terada S., Suzuki N., Uchide K., Akasofu K., Nishida E. (1992). Effect of testosterone on the development of bladder tumors and calculi in female rats. Gynecol. Obstet. Investig. 34, 105-110.
pubmed: 1398261
Tuygun C., Kankaya D., Imamoglu A., Sertcelik A., Zengin K., Oktay M. and Sertcelik N. (2011). Sex-specific hormone receptors in urothelial carcinomas of the human urinary bladder: a comparative analysis of clinicopathological features and survival outcomes according to receptor expression. Urol. Oncol. 29, 43-51.
pubmed: 19372057
Williams E.M., Higgins J.P., Sangoi A.R., McKenney J.K. and Troxell M.L. (2015). Androgen receptor immunohistochemistry in genitourinary neoplasms. Int. Urol. Nephrol. 47, 81-85.
pubmed: 25218615
Yasui M., Kawahara T., Izumi K., Yao M., Ishiguro Y., Ishiguro H., Uemura H. and Miyoshi Y. (2019). Androgen receptor mRNA expression is a predictor for recurrence-free survival in non-muscle invasive bladder cancer. BMC Cancer 19, 331.
pmcid: PMC6454612
pubmed: 30961575
Ye X., Guo J., Zhang H., Meng Q., Ma Y., Lin R., Yi X., Lu H., Bai X. and Cheng J. (2019). The enhanced expression of estrogen-related receptor α in human bladder cancer tissues and the effects of estrogen-related receptor α knockdown on bladder cancer cells. J. Cell Biochem. 120, 13841-13852.
pubmed: 30977157
Yonekura S., Terauchi F., Hoshi K., Yamaguchi T. and Kawai S. (2019). Androgen receptor predicts first and multiple recurrences in nonmuscle invasive urothelial carcinoma of the bladder. Pathol. Oncol. Res. 25, 987-994.
pubmed: 29862474
Zaitsu M., Toyokawa S., Tonooka A., Nakamura F., Takeuchi T., Homma Y and Kobayashi Y. (2015). Sex differences in bladder cancer pathology and survival: analysis of a population-based cancer registry. Cancer Med. 4, 363-370.
pmcid: PMC4380962
pubmed: 25533611
Zheng Y., Izumi K., Yao J.L. and Miyamoto H. (2011). Dihydrotestosteroneupregulates the expression of epidermal growth factor receptor and ERBB2 in androgen receptor-positive bladder cancer cells. Endocr. Relat. Cancer 18, 451-464.
pubmed: 21613411
Zhuang Y.H., Blauer M., Tammela T. and Tuohimaa P. (1997). Immunodetection of androgen receptor in human urinary bladder cancer. Histopathology 30, 556-562.
pubmed: 9205860