{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,11]],"date-time":"2026-07-11T06:25:56Z","timestamp":1783751156741,"version":"3.55.0"},"reference-count":28,"publisher":"Springer Science and Business Media LLC","issue":"11","license":[{"start":{"date-parts":[[2020,1,21]],"date-time":"2020-01-21T00:00:00Z","timestamp":1579564800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2020,1,21]],"date-time":"2020-01-21T00:00:00Z","timestamp":1579564800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["81772756"],"award-info":[{"award-number":["81772756"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["World J Urol"],"published-print":{"date-parts":[[2020,11]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:sec>\n                <jats:title>Objective<\/jats:title>\n                <jats:p>Slingshot homolog-1 (SSH-1) shows an important role in the occurrence and development in various tumors. While, the expression and prognostic implications of SSH-1 in bladder urothelial carcinoma (UC) remain unclear and thus were addressed in this study.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Methods<\/jats:title>\n                <jats:p>Immunohistochemistry (IHC) was performed on tissue microarrays composed of 624 bladder UC specimens after transurethral resection of bladder tumor (TUR-BT) to detect SSH-1 expression. The clinic-pathological features were compared between SSH-1(\u2009+) and SSH-1(\u2212) subgroups. The Kaplan\u2013Meier curve with log-rank test and univariate\/multivariate Cox regression model with stepwise backward elimination methods were performed for survival analyses.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Results<\/jats:title>\n                <jats:p>In this study, 359 (57.53%) specimens were detected with SSH-1 expression. SSH-1 positivity was significantly associated with higher pathological grade (<jats:italic>p<\/jats:italic>\u2009=\u20090.020), lymphovascular invasion (<jats:italic>p<\/jats:italic>\u2009=\u20090.006), tumor recurrence (<jats:italic>p<\/jats:italic>\u2009&lt;\u20090.001) and progression (<jats:italic>p<\/jats:italic>\u2009&lt;\u20090.001) in bladder UC. Besides, SSH-1 positivity predicted a shorter overall survival (OS, <jats:italic>p<\/jats:italic>\u2009=\u20090.024), recurrence-free survival (RFS, <jats:italic>p<\/jats:italic>\u2009&lt;\u20090.001), progression-free survival (PFS, <jats:italic>p<\/jats:italic>\u2009=\u20090.002) and cancer-specific survival (CSS, <jats:italic>p<\/jats:italic>\u2009=\u20090.047). Multivariate Cox proportional hazard analysis showed that tumor size (<jats:italic>p<\/jats:italic>\u2009=\u20090.007), lymphovascular invasion (<jats:italic>p<\/jats:italic>\u2009=\u20090.003), recurrence (<jats:italic>p<\/jats:italic>\u2009&lt;\u20090.001), progression (<jats:italic>p<\/jats:italic>\u2009&lt;\u20090.001) and SSH-1 expression (<jats:italic>p<\/jats:italic>\u2009=\u20090.015) were predictors of poor prognosis in bladder UC patients.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Conclusions<\/jats:title>\n                <jats:p>SSH-1 expression was associated with undesirable clinic-pathological characteristics and poor post-operative prognosis in bladder UC patients. SSH-1 might play an important role in bladder UC and serve as a promising predictor of oncological outcomes in patients with bladder UC.<\/jats:p>\n              <\/jats:sec>","DOI":"10.1007\/s00345-020-03092-4","type":"journal-article","created":{"date-parts":[[2020,1,21]],"date-time":"2020-01-21T15:03:25Z","timestamp":1579619005000},"page":"2849-2856","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["Slingshot homolog-1 expression is a poor prognostic factor of pT1 bladder urothelial carcinoma after transurethral resection"],"prefix":"10.1007","volume":"38","author":[{"given":"Qiang","family":"Luo","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yanxia","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hu","family":"Zhao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peng","family":"Guo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qianwen","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wenjun","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gang","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4483-5707","authenticated-orcid":false,"given":"Bin","family":"Wu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2020,1,21]]},"reference":[{"issue":"1","key":"3092_CR1","doi-asserted-by":"publisher","first-page":"96","DOI":"10.1016\/j.eururo.2016.06.010","volume":"71","author":"S Antoni","year":"2017","unstructured":"Antoni S, Ferlay J, Soerjomataram I, Znaor A, Jemal A, Bray F (2017) Bladder cancer incidence and mortality: a global overview and recent trends. Eur Urol 71(1):96\u2013108","journal-title":"Eur Urol"},{"issue":"6","key":"3092_CR2","doi-asserted-by":"publisher","first-page":"784","DOI":"10.1016\/j.eururo.2018.09.001","volume":"74","author":"MGK Cumberbatch","year":"2018","unstructured":"Cumberbatch MGK, Jubber I, Black PC, Esperto F, Figueroa JD, Kamat AM et al (2018) Epidemiology of bladder cancer: a systematic review and contemporary update of risk factors in 2018. Eur Urol 74(6):784\u2013795","journal-title":"Eur Urol"},{"key":"3092_CR3","doi-asserted-by":"publisher","first-page":"55","DOI":"10.1016\/j.urology.2019.01.039","volume":"128","author":"P Mukherjee","year":"2019","unstructured":"Mukherjee P, George AJP, Yadav BK, Jeyaseelan L, Kumar RM, Mukha RP et al (2019) The impact of narrow band imaging in the detection and resection of bladder tumor in transitional cell carcinoma of the bladder: a prospective, blinded sequential intervention randomized controlled Trial. Urology 128:55\u201361","journal-title":"Urology"},{"issue":"6","key":"3092_CR4","doi-asserted-by":"publisher","first-page":"1655","DOI":"10.1016\/j.juro.2014.01.087","volume":"191","author":"KA Richards","year":"2014","unstructured":"Richards KA, Smith ND, Steinberg GD (2014) The importance of transurethral resection of bladder tumor in the management of nonmuscle invasive bladder cancer: a systematic review of novel technologies. J Urol 191(6):1655\u20131664","journal-title":"J Urol"},{"issue":"11","key":"3092_CR5","doi-asserted-by":"publisher","first-page":"2424","DOI":"10.1161\/ATVBAHA.111.232769","volume":"31","author":"RA Torres","year":"2011","unstructured":"Torres RA, Drake DA, Solodushko V, Jadhav R, Smith E, Rocic P et al (2011) Slingshot isoform-specific regulation of cofilin-mediated vascular smooth muscle cell migration and neointima formation. Arterioscl Throm Vasc 31(11):2424\u20132431","journal-title":"Arterioscl Throm Vasc"},{"issue":"4","key":"3092_CR6","doi-asserted-by":"publisher","first-page":"686","DOI":"10.1016\/j.bbrc.2016.11.095","volume":"482","author":"K Takahashi","year":"2017","unstructured":"Takahashi K, Okabe H, Kanno SI, Nagai T, Mizuno K (2017) A pleckstrin homology-like domain is critical for F-actin binding and cofilin-phosphatase activity of Slingshot-1. Biochem Biophys Res 482(4):686\u2013692","journal-title":"Biochem Biophys Res"},{"issue":"2","key":"3092_CR7","doi-asserted-by":"publisher","first-page":"171","DOI":"10.1016\/j.canlet.2015.02.015","volume":"360","author":"Y Wang","year":"2015","unstructured":"Wang Y, Kuramitsu Y, Kitagawa T, Baron B, Yoshino S, Maehara S et al (2015) Cofilin-phosphatase slingshot-1L (SSH1L) is over-expressed in pancreatic cancer (PC) and contributes to tumor cell migration. Cancer Lett 360(2):171\u2013176","journal-title":"Cancer Lett"},{"issue":"1","key":"3092_CR8","doi-asserted-by":"publisher","first-page":"12","DOI":"10.1186\/s12876-018-0739-5","volume":"18","author":"Y Maimaiti","year":"2018","unstructured":"Maimaiti Y, Maimaitiming M, Li Y, Aibibula S, Ainiwaer A, Aili A et al (2018) SSH1 expression is associated with gastric cancer progression and predicts a poor prognosis. BMC Gastroenterol 18(1):12","journal-title":"BMC Gastroenterol"},{"issue":"5","key":"3092_CR9","doi-asserted-by":"publisher","first-page":"727","DOI":"10.1007\/s00428-018-2298-0","volume":"472","author":"H Aggelou","year":"2018","unstructured":"Aggelou H, Chadla P, Nikou S, Karteri S, Maroulis I, Kalofonos HP et al (2018) LIMK\/cofilin pathway and Slingshot are implicated in human colorectal cancer progression and chemoresistance. Virchows Arch 472(5):727\u2013737","journal-title":"Virchows Arch"},{"key":"3092_CR10","doi-asserted-by":"publisher","first-page":"59","DOI":"10.3389\/fimmu.2016.00059","volume":"7","author":"R Ramirez-Munoz","year":"2016","unstructured":"Ramirez-Munoz R, Castro-Sanchez P, Roda-Navarro P (2016) Ultrasensitivity in the cofilin signaling module: a mechanism for tuning T cell responses. Front Immunol 7:59","journal-title":"Front Immunol"},{"issue":"3","key":"3092_CR11","doi-asserted-by":"publisher","first-page":"447","DOI":"10.1016\/j.eururo.2016.05.041","volume":"71","author":"M Babjuk","year":"2017","unstructured":"Babjuk M, Bohle A, Burger M, Capoun O, Cohen D, Comperat EM et al (2017) EAU guidelines on non-muscle-invasive urothelial carcinoma of the bladder: update 2016. Eur Urol 71(3):447\u2013461","journal-title":"Eur Urol"},{"issue":"6","key":"3092_CR12","doi-asserted-by":"publisher","first-page":"925","DOI":"10.1016\/j.eururo.2018.02.014","volume":"73","author":"MGK Cumberbatch","year":"2018","unstructured":"Cumberbatch MGK, Foerster B, Catto JWF, Kamat AM, Kassouf W, Jubber I et al (2018) Repeat transurethral resection in non-muscle-invasive bladder cancer: a systematic review. Eur Urol 73(6):925\u2013933","journal-title":"Eur Urol"},{"issue":"4","key":"3092_CR13","doi-asserted-by":"publisher","first-page":"e784","DOI":"10.1016\/j.clgc.2019.04.014","volume":"17","author":"M Akand","year":"2019","unstructured":"Akand M, Muilwijk T, Raskin Y, De Vrieze M, Joniau S, Van Der Aa F (2019) Quality control indicators for transurethral resection of non-muscle-invasive bladder cancer. Clin Genitourin Cancer 17(4):e784\u2013e792","journal-title":"Clin Genitourin Cancer"},{"issue":"1\u20132","key":"3092_CR14","doi-asserted-by":"publisher","first-page":"E46","DOI":"10.5489\/cuaj.3583","volume":"10","author":"W Kassouf","year":"2016","unstructured":"Kassouf W, Aprikian A, Black P, Kulkarni G, Izawa J, Eapen L et al (2016) Recommendations for the improvement of bladder cancer quality of care in Canada: a consensus document reviewed and endorsed by Bladder Cancer Canada (BCC), Canadian Urologic Oncology Group (CUOG), and Canadian Urological Association (CUA), December 2015. Can Urol Assoc 10(1\u20132):E46\u201380","journal-title":"Can Urol Assoc"},{"issue":"1","key":"3092_CR15","doi-asserted-by":"publisher","first-page":"27","DOI":"10.3233\/BLC-150034","volume":"2","author":"NE Power","year":"2016","unstructured":"Power NE, Izawa J (2016) Comparison of guidelines on non-muscle invasive bladder cancer (EAU, CUA, AUA, NCCN, NICE). Bladder Cancer 2(1):27\u201336","journal-title":"Bladder Cancer"},{"key":"3092_CR16","doi-asserted-by":"publisher","first-page":"465","DOI":"10.3389\/fonc.2019.00465","volume":"9","author":"B Calo","year":"2019","unstructured":"Calo B, Chirico M, Fortunato F, Sanguedolce F, Carvalho-Dias E, Autorino R et al (2019) Is Repeat transurethral resection always needed in high-grade t1 bladder cancer? Front Oncol 9:465","journal-title":"Front Oncol"},{"issue":"10","key":"3092_CR17","doi-asserted-by":"publisher","first-page":"811","DOI":"10.1046\/j.1365-2443.2003.00678.x","volume":"8","author":"Y Ohta","year":"2003","unstructured":"Ohta Y, Kousaka K, Nagata-Ohashi K, Ohashi K, Muramoto A, Shima Y et al (2003) Differential activities, subcellular distribution and tissue expression patterns of three members of Slingshot family phosphatases that dephosphorylate cofilin. Genes Cells 8(10):811\u2013824","journal-title":"Genes Cells"},{"issue":"2","key":"3092_CR18","doi-asserted-by":"publisher","first-page":"457","DOI":"10.1016\/j.cellsig.2012.11.001","volume":"25","author":"K Mizuno","year":"2013","unstructured":"Mizuno K (2013) Signaling mechanisms and functional roles of cofilin phosphorylation and dephosphorylation. Cell Signal 25(2):457\u2013469","journal-title":"Cell Signal"},{"issue":"47","key":"3092_CR19","doi-asserted-by":"publisher","first-page":"32542","DOI":"10.1074\/jbc.M804627200","volume":"283","author":"S Kurita","year":"2008","unstructured":"Kurita S, Watanabe Y, Gunji E, Ohashi K, Mizuno K (2008) Molecular dissection of the mechanisms of substrate recognition and F-actin-mediated activation of cofilin-phosphatase Slingshot-1. J Biol Chem 283(47):32542\u201332552","journal-title":"J Biol Chem"},{"issue":"1","key":"3092_CR20","doi-asserted-by":"publisher","first-page":"10","DOI":"10.3390\/ijms18010010","volume":"18","author":"S Shishkin","year":"2016","unstructured":"Shishkin S, Eremina L, Pashintseva N, Kovalev L, Kovaleva M (2016) Cofilin-1 and other ADF\/cofilin superfamily members in human malignant cells. Int J Mol Sci 18(1):10","journal-title":"Int J Mol Sci"},{"issue":"1","key":"3092_CR21","doi-asserted-by":"publisher","first-page":"118","DOI":"10.1016\/j.eururo.2011.10.029","volume":"62","author":"J Palou","year":"2012","unstructured":"Palou J, Sylvester RJ, Faba OR, Parada R, Pena JA, Algaba F et al (2012) Female gender and carcinoma in situ in the prostatic urethra are prognostic factors for recurrence, progression, and disease-specific mortality in T1G3 bladder cancer patients treated with Bacillus Calmette-Guerin. Eur Urol 62(1):118\u2013125","journal-title":"Eur Urol"},{"issue":"4","key":"3092_CR22","doi-asserted-by":"publisher","first-page":"575","DOI":"10.3892\/mco.2014.290","volume":"2","author":"V Den","year":"2014","unstructured":"Den V, Cerruto MA, D'Elia C, Brunelli M, Otte O, Minja A et al (2014) Prognostic role of substaging in T1G3 transitional cell carcinoma of the urinary bladder. Mol Clin Oncol 2(4):575\u2013580","journal-title":"Mol Clin Oncol"},{"issue":"1","key":"3092_CR23","doi-asserted-by":"publisher","first-page":"74","DOI":"10.1016\/j.eururo.2014.06.040","volume":"67","author":"P Gontero","year":"2015","unstructured":"Gontero P, Sylvester R, Pisano F, Joniau S, Vander Eeckt K, Serretta V et al (2015) Prognostic factors and risk groups in T1G3 non-muscle-invasive bladder cancer patients initially treated with Bacillus Calmette-Guerin: results of a retrospective multicenter study of 2451 patients. Eur Urol 67(1):74\u201382","journal-title":"Eur Urol"},{"issue":"6","key":"3092_CR24","doi-asserted-by":"publisher","first-page":"871","DOI":"10.1007\/s00345-015-1715-0","volume":"34","author":"Q Tang","year":"2016","unstructured":"Tang Q, Xiong G, Li X, Fang D, Xi C, Zhang L et al (2016) The prognostic impact of squamous and glandular differentiation for upper tract urothelial carcinoma patients after radical nephroureterectomy. World J Urol 34(6):871\u2013877","journal-title":"World J Urol"},{"issue":"3","key":"3092_CR25","doi-asserted-by":"publisher","first-page":"3522","DOI":"10.3892\/ol.2017.6581","volume":"14","author":"H Xu","year":"2017","unstructured":"Xu H, Xie L, Liu X, Zhang Y, Shen Z, Chen T et al (2017) Impact of squamous and\/or glandular differentiation on recurrence and progression following transurethral resection for non-muscle invasive urothelial carcinoma of bladder. Oncol Lett 14(3):3522\u20133528","journal-title":"Oncol Lett"},{"issue":"2","key":"3092_CR26","doi-asserted-by":"publisher","first-page":"405","DOI":"10.1016\/j.juro.2012.04.020","volume":"188","author":"SP Kim","year":"2012","unstructured":"Kim SP, Frank I, Cheville JC, Thompson RH, Weight CJ, Thapa P et al (2012) The impact of squamous and glandular differentiation on survival after radical cystectomy for urothelial carcinoma. J Urol 188(2):405\u2013409","journal-title":"J Urol"},{"issue":"8","key":"3092_CR27","doi-asserted-by":"publisher","first-page":"1889","DOI":"10.1016\/j.ejca.2013.02.001","volume":"49","author":"E Xylinas","year":"2013","unstructured":"Xylinas E, Rink M, Robinson BD, Lotan Y, Babjuk M, Brisuda A et al (2013) Impact of histological variants on oncological outcomes of patients with urothelial carcinoma of the bladder treated with radical cystectomy. Eur J Cancer 49(8):1889\u20131897","journal-title":"Eur J Cancer"},{"issue":"2","key":"3092_CR28","doi-asserted-by":"publisher","first-page":"117","DOI":"10.1016\/j.urolonc.2012.08.017","volume":"32","author":"AP Mitra","year":"2014","unstructured":"Mitra AP, Bartsch CC, Bartsch G Jr, Miranda G, Skinner EC, Daneshmand S (2014) Does presence of squamous and glandular differentiation in urothelial carcinoma of the bladder at cystectomy portend poor prognosis? An intensive case-control analysis. Urol Oncol 32(2):117\u2013127","journal-title":"Urol Oncol"}],"container-title":["World Journal of Urology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s00345-020-03092-4.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/article\/10.1007\/s00345-020-03092-4\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s00345-020-03092-4.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,1,20]],"date-time":"2021-01-20T00:13:23Z","timestamp":1611101603000},"score":1,"resource":{"primary":{"URL":"http:\/\/link.springer.com\/10.1007\/s00345-020-03092-4"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,1,21]]},"references-count":28,"journal-issue":{"issue":"11","published-print":{"date-parts":[[2020,11]]}},"alternative-id":["3092"],"URL":"https:\/\/doi.org\/10.1007\/s00345-020-03092-4","relation":{},"ISSN":["0724-4983","1433-8726"],"issn-type":[{"value":"0724-4983","type":"print"},{"value":"1433-8726","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,1,21]]},"assertion":[{"value":"11 October 2019","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"10 January 2020","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"21 January 2020","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Compliance with ethical standards"}},{"value":"The authors declare they have no conflict of interest.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflict of interest"}},{"value":"This study has been approved by the ethics committee of Jiangyin People\u2019s Hospital and has been performed according to the ethical standards laid down in the 1964 Declaration of Helsinki.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethical approval"}}]}}