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01-09-2020 | Prostate Cancer | Original Article

Claudin-1 upregulation is associated with favorable tumor features and a reduced risk for biochemical recurrence in ERG-positive prostate cancer

Authors: Simon Kind, Franziska Büscheck, Doris Höflmayer, Claudia Hube-Magg, Martina Kluth, Maria Christina Tsourlakis, Stefan Steurer, Till S. Clauditz, Andreas M. Luebke, Eike Burandt, Waldemar Wilczak, Andrea Hinsch, David Dum, Sören Weidemann, Christoph Fraune, Burkhard Beyer, Thomas Steuber, Hartwig Huland, Markus Graefen, Margit Fisch, Ronald Simon, Guido Sauter, Thorsten Schlomm, Sarah Minner, Till Eichenauer

Published in: World Journal of Urology | Issue 9/2020

Abstract

Background

Claudin-1 is a membrane-tight junction protein and important for the sealing of the paracellular cleft in epithelial and endothelial cells. Differential expression of Claudin-1 is linked to disease outcome in various cancers.

Material and methods

To evaluate the potential relevance of Claudin-1 expression in prostate cancer, a tissue microarray containing samples of 17,747 tumors with annotated clinico-pathological and molecular data was immunohistochemically analyzed for Claudin-1 expression.

Results

In normal prostate, glandular cells were always Claudin-1-negative while there was a strong staining of gland-surrounding basal cells. In contrast to normal prostatic glands, a positive Claudin-1 immunostaining, was found, however, in 38.7% of 12,441 interpretable cancers and was considered weak in 12.7%, moderate in 13.2%, and strong in 12.8% of cases. Positive Claudin-1 immunostaining was associated with favorable tumor features like low pT (p = 0.0032), low Gleason grade (p< 0.0001), and a reduced risk of PSA recurrence (p = 0.0005). A positive Claudin-1 staining was markedly more frequent in ERG-positive (63%) than in ERG-negative cancers (23%; p < 0.0001). Subset analyses revealed that all associations of Claudin-1 expression and favorable phenotype and prognosis were driven by ERG-positive cancers. Multivariate analyses revealed, however, that even in ERG-positive cancers, the prognostic impact of high Claudin-1 expression was not independent of established clinico-pathological parameters. Comparison with 12 previously analyzed chromosomal deletions identified conspicuous associations with PTEN and 12p13 deletions potentially indicating functional interactions.

Conclusion

These data identify a peculiar role for Claudin-1 in prostate cancer. The protein is overexpressed in a fraction of prostate cancers and increased Claudin-1 expression levels predict a favorable prognosis in ERG-positive cancer.

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Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68(6):394–424. https://doi.org/10.3322/caac.21492CrossRef

Bill-Axelson A, Holmberg L, Ruutu M, Garmo H, Stark JR, Busch C, Nordling S, Haggman M, Andersson SO, Bratell S, Spangberg A, Palmgren J, Steineck G, Adami HO, Johansson JE, Investigators S (2011) Radical prostatectomy versus watchful waiting in early prostate cancer. N Engl J Med 364(18):1708–1717. https://doi.org/10.1056/NEJMoa1011967PubMedCrossRef

Wilt TJ, Jones KM, Barry MJ, Andriole GL, Culkin D, Wheeler T, Aronson WJ, Brawer MK (2017) Follow-up of prostatectomy versus observation for early prostate cancer. N Engl J Med 377(2):132–142. https://doi.org/10.1056/NEJMoa1615869PubMedCrossRef

Klotz L, Vesprini D, Sethukavalan P, Jethava V, Zhang L, Jain S, Yamamoto T, Mamedov A, Loblaw A (2015) Long-term follow-up of a large active surveillance cohort of patients with prostate cancer. J Clin Oncol 33(3):272–277. https://doi.org/10.1200/JCO.2014.55.1192CrossRef

Fenton JJ, Weyrich MS, Durbin S, Liu Y, Bang H, Melnikow J (2018). In: prostate-specific antigen-based screening for prostate cancer: A systematic evidence review for the U.S. preventive services task force. U.S. preventive services task force evidence syntheses, formerly systematic evidence reviews. rockville (MD)

Gonzalez-Mariscal L, Betanzos A, Nava P, Jaramillo BE (2003) Tight junction proteins. Prog Biophys Mol Biol 81(1):1–44PubMedCrossRef

France MM, Turner JR (2017) The mucosal barrier at a glance. J Cell Sci 130(2):307–314. https://doi.org/10.1242/jcs.193482PubMedPubMedCentralCrossRef

Furuse M, Hata M, Furuse K, Yoshida Y, Haratake A, Sugitani Y, Noda T, Kubo A, Tsukita S (2002) Claudin-based tight junctions are crucial for the mammalian epidermal barrier: a lesson from claudin-1-deficient mice. J Cell Biol 156(6):1099–1111. https://doi.org/10.1083/jcb.200110122PubMedPubMedCentralCrossRef

Jiang WG, Puntis MC, Hallett MB (1994) Molecular and cellular basis of cancer invasion and metastasis: implications for treatment. Br J Surg 81(11):1576–1590PubMedCrossRef

10.

Leotlela PD, Wade MS, Duray PH, Rhode MJ, Brown HF, Rosenthal DT, Dissanayake SK, Earley R, Indig FE, Nickoloff BJ, Taub DD, Kallioniemi OP, Meltzer P, Morin PJ, Weeraratna AT (2007) Claudin-1 overexpression in melanoma is regulated by PKC and contributes to melanoma cell motility. Oncogene 26(26):3846–3856. https://doi.org/10.1038/sj.onc.1210155PubMedCrossRef

11.

Sobel G, Paska C, Szabo I, Kiss A, Kadar A, Schaff Z (2005) Increased expression of claudins in cervical squamous intraepithelial neoplasia and invasive carcinoma. Hum Pathol 36(2):162–169. https://doi.org/10.1016/j.humpath.2004.12.001PubMedCrossRef

12.

Hoellen F, Waldmann A, Banz-Jansen C, Holtrich U, Karn T, Oberlander M, Habermann JK, Hormann M, Koster F, Ribbat-Idel J, Thill M, Rody A, El-Balat A, Hanker L (2017) Claudin-1 expression in cervical cancer. Mol Clin Oncol 7(5):880–884. https://doi.org/10.3892/mco.2017.1391PubMedPubMedCentralCrossRef

13.

Lee JW, Lee SJ, Seo J, Song SY, Ahn G, Park CS, Lee JH, Kim BG, Bae DS (2005) Increased expressions of claudin-1 and claudin-7 during the progression of cervical neoplasia. Gynecol Oncol 97(1):53–59. https://doi.org/10.1016/j.ygyno.2004.11.058PubMedCrossRef

14.

Chao YC, Pan SH, Yang SC, Yu SL, Che TF, Lin CW, Tsai MS, Chang GC, Wu CH, Wu YY, Lee YC, Hong TM, Yang PC (2009) Claudin-1 is a metastasis suppressor and correlates with clinical outcome in lung adenocarcinoma. Am J Respir Crit Care Med 179(2):123–133. https://doi.org/10.1164/rccm.200803-456OCPubMedCrossRef

15.

de Oliveira SS, de Oliveira IM, De Souza W, Morgado-Diaz JA (2005) Claudins upregulation in human colorectal cancer. FEBS Lett 579(27):6179–6185. https://doi.org/10.1016/j.febslet.2005.09.091PubMedCrossRef

16.

Dhawan P, Singh AB, Deane NG, No Y, Shiou SR, Schmidt C, Neff J, Washington MK, Beauchamp RD (2005) Claudin-1 regulates cellular transformation and metastatic behavior in colon cancer. J Clin Invest 115(7):1765–1776. https://doi.org/10.1172/JCI24543PubMedPubMedCentralCrossRef

17.

Resnick MB, Konkin T, Routhier J, Sabo E, Pricolo VE (2005) Claudin-1 is a strong prognostic indicator in stage II colonic cancer: a tissue microarray study. Modern Pathol 18(4):511–518. https://doi.org/10.1038/modpathol.3800301CrossRef

18.

Huo Q, Kinugasa T, Wang L, Huang J, Zhao J, Shibaguchi H, Kuroki M, Tanaka T, Yamashita Y, Nabeshima K, Iwasaki H, Kuroki M (2009) Claudin-1 protein is a major factor involved in the tumorigenesis of colorectal cancer. Anticancer Res 29(3):851–857PubMed

19.

Kinugasa T, Huo Q, Higashi D, Shibaguchi H, Kuroki M, Tanaka T, Futami K, Yamashita Y, Hachimine K, Maekawa S, Nabeshima K, Iwasaki H, Kuroki M (2007) Selective up-regulation of claudin-1 and claudin-2 in colorectal cancer. Anticancer Res 27(6A):3729–3734PubMed

20.

Higashi Y, Suzuki S, Sakaguchi T, Nakamura T, Baba S, Reinecker HC, Nakamura S, Konno H (2007) Loss of claudin-1 expression correlates with malignancy of hepatocellular carcinoma. J Surg Res 139(1):68–76. https://doi.org/10.1016/j.jss.2006.08.038PubMedCrossRef

21.

Tokes AM, Kulka J, Paku S, Szik A, Paska C, Novak PK, Szilak L, Kiss A, Bogi K, Schaff Z (2005) Claudin-1, -3 and -4 proteins and mRNA expression in benign and malignant breast lesions: a research study. Breast Cancer Res 7(2):R296–305. https://doi.org/10.1186/bcr983PubMedPubMedCentralCrossRef

22.

Lu S, Singh K, Mangray S, Tavares R, Noble L, Resnick MB, Yakirevich E (2013) Claudin expression in high-grade invasive ductal carcinoma of the breast: correlation with the molecular subtype. Mod Pathol 26(4):485–495. https://doi.org/10.1038/modpathol.2012.187PubMedCrossRef

23.

Resnick MB, Gavilanez M, Newton E, Konkin T, Bhattacharya B, Britt DE, Sabo E, Moss SF (2005) Claudin expression in gastric adenocarcinomas: a tissue microarray study with prognostic correlation. Hum Pathol 36(8):886–892. https://doi.org/10.1016/j.humpath.2005.05.019PubMedCrossRef

24.

Wang H, Yang X (2015) The expression patterns of tight junction protein claudin-1, -3, and -4 in human gastric neoplasms and adjacent non-neoplastic tissues. Int J Clin Exp Pathol 8(1):881–887PubMedPubMedCentral

25.

Huang J, Li J, Qu Y, Zhang J, Zhang L, Chen X, Liu B, Zhu Z (2014) The expression of claudin 1 correlates with beta-catenin and is a prognostic factor of poor outcome in gastric cancer. Int J Oncol 44(4):1293–1301. https://doi.org/10.3892/ijo.2014.2298PubMedCrossRef

26.

Weischenfeldt J, Simon R, Feuerbach L, Schlangen K, Weichenhan D, Minner S, Wuttig D, Warnatz HJ, Stehr H, Rausch T, Jager N, Gu L, Bogatyrova O, Stutz AM, Claus R, Eils J, Eils R, Gerhauser C, Huang PH, Hutter B, Kabbe R, Lawerenz C, Radomski S, Bartholomae CC, Falth M, Gade S, Schmidt M, Amschler N, Hass T, Galal R, Gjoni J, Kuner R, Baer C, Masser S, von Kalle C, Zichner T, Benes V, Raeder B, Mader M, Amstislavskiy V, Avci M, Lehrach H, Parkhomchuk D, Sultan M, Burkhardt L, Graefen M, Huland H, Kluth M, Krohn A, Sirma H, Stumm L, Steurer S, Grupp K, Sultmann H, Sauter G, Plass C, Brors B, Yaspo ML, Korbel JO, Schlomm T (2013) Integrative genomic analyses reveal an androgen-driven somatic alteration landscape in early-onset prostate cancer. Cancer Cell 23(2):159–170. https://doi.org/10.1016/j.ccr.2013.01.002PubMedCrossRef

27.

Pyo JS, Kim NY, Cho WJ (2019) Prognostic role of claudin-1 immunohistochemistry in malignant solid tumors: a meta-analysis. J Pathol Transl Med 53(3):173–179. https://doi.org/10.4132/jptm.2019.02.03PubMedPubMedCentralCrossRef

28.

Vare P, Loikkanen I, Hirvikoski P, Vaarala MH, Soini Y (2008) Low claudin expression is associated with high Gleason grade in prostate adenocarcinoma. Oncol Rep 19(1):25–31PubMed

29.

Sheehan GM, Kallakury BV, Sheehan CE, Fisher HA, Kaufman RP Jr, Ross JS (2007) Loss of claudins-1 and -7 and expression of claudins-3 and -4 correlate with prognostic variables in prostatic adenocarcinomas. Hum Pathol 38(4):564–569. https://doi.org/10.1016/j.humpath.2006.11.007PubMedCrossRef

30.

Seo KW, Kwon YK, Kim BH, Kim CI, Chang HS, Choe MS, Park CH (2010) Correlation between claudins expression and prognostic factors in prostate cancer. Korean J Urol 51(4):239–244. https://doi.org/10.4111/kju.2010.51.4.239PubMedPubMedCentralCrossRef

31.

Krajewska M, Olson AH, Mercola D, Reed JC, Krajewski S (2007) Claudin-1 immunohistochemistry for distinguishing malignant from benign epithelial lesions of prostate. Prostate 67(9):907–910. https://doi.org/10.1002/pros.20578PubMedCrossRef

32.

Sauter G, Steurer S, Clauditz TS, Krech T, Wittmer C, Lutz F, Lennartz M, Janssen T, Hakimi N, Simon R, von Petersdorff-Campen M, Jacobsen F, von Loga K, Wilczak W, Minner S, Tsourlakis MC, Chirico V, Haese A, Heinzer H, Beyer B, Graefen M, Michl U, Salomon G, Steuber T, Budaus LH, Hekeler E, Malsy-Mink J, Kutzera S, Fraune C, Gobel C, Huland H, Schlomm T (2016) Clinical utility of quantitative gleason grading in prostate biopsies and prostatectomy specimens. Eur Urol 69(4):592–598. https://doi.org/10.1016/j.eururo.2015.10.029PubMedCrossRef

33.

Kononen J, Bubendorf L, Kallioniemi A, Barlund M, Schraml P, Leighton S, Torhorst J, Mihatsch MJ, Sauter G, Kallioniemi OP (1998) Tissue microarrays for high-throughput molecular profiling of tumor specimens. Nat Med 4(7):844–847PubMedCrossRef

34.

Tennstedt P, Koster P, Bruchmann A, Mirlacher M, Haese A, Steuber T, Sauter G, Huland H, Graefen M, Schlomm T, Minner S, Simon R (2012) The impact of the number of cores on tissue microarray studies investigating prostate cancer biomarkers. Int J Oncol 40(1):261–268. https://doi.org/10.3892/ijo.2011.1216PubMedCrossRef

35.

Minner S, Enodien M, Sirma H, Luebke AM, Krohn A, Mayer PS, Simon R, Tennstedt P, Muller J, Scholz L, Brase JC, Liu AY, Schluter H, Pantel K, Schumacher U, Bokemeyer C, Steuber T, Graefen M, Sauter G, Schlomm T (2011) ERG status is unrelated to PSA recurrence in radically operated prostate cancer in the absence of antihormonal therapy. Clin Cancer Res 17(18):5878–5888. https://doi.org/10.1158/1078-0432.Ccr-11-1251PubMedCrossRef

36.

Minner S, Wittmer C, Graefen M, Salomon G, Steuber T, Haese A, Huland H, Bokemeyer C, Yekebas E, Dierlamm J, Balabanov S, Kilic E, Wilczak W, Simon R, Sauter G, Schlomm T (2011) High level PSMA expression is associated with early PSA recurrence in surgically treated prostate cancer. Prostate 71(3):281–288. https://doi.org/10.1002/pros.21241PubMedCrossRef

37.

Krohn A, Seidel A, Burkhardt L, Bachmann F, Mader M, Grupp K, Eichenauer T, Becker A, Adam M, Graefen M, Huland H, Kurtz S, Steurer S, Tsourlakis MC, Minner S, Michl U, Schlomm T, Sauter G, Simon R, Sirma H (2013) Recurrent deletion of 3p13 targets multiple tumour suppressor genes and defines a distinct subgroup of aggressive ERG fusion-positive prostate cancers. J Pathol 231(1):130–141. https://doi.org/10.1002/path.4223PubMedCrossRef

38.

Burkhardt L, Fuchs S, Krohn A, Masser S, Mader M, Kluth M, Bachmann F, Huland H, Steuber T, Graefen M, Schlomm T, Minner S, Sauter G, Sirma H, Simon R (2013) CHD1 is a 5q21 tumor suppressor required for ERG rearrangement in prostate cancer. Can Res 73(9):2795–2805. https://doi.org/10.1158/0008-5472.Can-12-1342CrossRef

39.

Kluth M, Hesse J, Heinl A, Krohn A, Steurer S, Sirma H, Simon R, Mayer PS, Schumacher U, Grupp K, Izbicki JR, Pantel K, Dikomey E, Korbel JO, Plass C, Sauter G, Schlomm T, Minner S (2013) Genomic deletion of MAP3K7 at 6q12-22 is associated with early PSA recurrence in prostate cancer and absence of TMPRSS2:ERG fusions. Modern Pathol 26(7):975–983. https://doi.org/10.1038/modpathol.2012.236CrossRef

40.

Kluth M, Amschler NN, Galal R, Moller-Koop C, Barrow P, Tsourlakis MC, Jacobsen F, Hinsch A, Wittmer C, Steurer S, Krech T, Buscheck F, Clauditz TS, Beyer B, Wilczak W, Graefen M, Huland H, Minner S, Schlomm T, Sauter G, Simon R (2017) Deletion of 8p is an independent prognostic parameter in prostate cancer. Oncotarget 8(1):379–392. https://doi.org/10.18632/oncotarget.13425PubMedCrossRef

41.

Krohn A, Diedler T, Burkhardt L, Mayer PS, De Silva C, Meyer-Kornblum M, Kotschau D, Tennstedt P, Huang J, Gerhauser C, Mader M, Kurtz S, Sirma H, Saad F, Steuber T, Graefen M, Plass C, Sauter G, Simon R, Minner S, Schlomm T (2012) Genomic deletion of PTEN is associated with tumor progression and early PSA recurrence in ERG fusion-positive and fusion-negative prostate cancer. Am J Pathol 181(2):401–412. https://doi.org/10.1016/j.ajpath.2012.04.026PubMedCrossRef

42.

Kluth M, Ahrary R, Hube-Magg C, Ahmed M, Volta H, Schwemin C, Steurer S, Wittmer C, Wilczak W, Burandt E, Krech T, Adam M, Michl U, Heinzer H, Salomon G, Graefen M, Koop C, Minner S, Simon R, Sauter G, Schlomm T (2015) Genomic deletion of chromosome 12p is an independent prognostic marker in prostate cancer. Oncotarget 6(29):27966–27979. https://doi.org/10.18632/oncotarget.4626PubMedPubMedCentralCrossRef

43.

Kluth M, Scherzai S, Buschek F, Fraune C, Moller K, Hoflmayer D, Minner S, Gobel C, Moller-Koop C, Hinsch A, Neubauer E, Tsourlakis MC, Sauter G, Heinzer H, Graefen M, Wilczak W, Luebke AM, Burandt E, Steurer S, Schlomm T, Simon R (2018) 13q deletion is linked to an adverse phenotype and poor prognosis in prostate cancer. Genes Chromosom Cancer 57(10):504–512. https://doi.org/10.1002/gcc.22645PubMedCrossRef

44.

Kluth M, Jung S, Habib O, Eshagzaiy M, Heinl A, Amschler N, Masser S, Mader M, Runte F, Barow P, Frogh S, Omari J, Moller-Koop C, Hube-Magg C, Weischenfeldt J, Korbel J, Steurer S, Krech T, Huland H, Graefen M, Minner S, Sauter G, Schlomm T, Simon R (2017) Deletion lengthening at chromosomes 6q and 16q targets multiple tumor suppressor genes and is associated with an increasingly poor prognosis in prostate cancer. Oncotarget 8(65):108923–108935. https://doi.org/10.18632/oncotarget.22408PubMedPubMedCentralCrossRef

45.

Kluth M, Harasimowicz S, Burkhardt L, Grupp K, Krohn A, Prien K, Gjoni J, Hass T, Galal R, Graefen M, Haese A, Simon R, Huhne-Simon J, Koop C, Korbel J, Weischenfeld J, Huland H, Sauter G, Quaas A, Wilczak W, Tsourlakis MC, Minner S, Schlomm T (2014) Clinical significance of different types of p53 gene alteration in surgically treated prostate cancer. Int J Cancer 135(6):1369–1380. https://doi.org/10.1002/ijc.28784PubMedCrossRef

46.

Kluth M, Graunke M, Moller-Koop C, Hube-Magg C, Minner S, Michl U, Graefen M, Huland H, Pompe R, Jacobsen F, Hinsch A, Wittmer C, Lebok P, Steurer S, Buscheck F, Clauditz T, Wilczak W, Sauter G, Schlomm T, Simon R (2016) Deletion of 18q is a strong and independent prognostic feature in prostate cancer. Oncotarget 7(52):86339–86349. https://doi.org/10.18632/oncotarget.13404PubMedPubMedCentralCrossRef

47.

Heinrich MC, Gobel C, Kluth M, Bernreuther C, Sauer C, Schroeder C, Moller-Koop C, Hube-Magg C, Lebok P, Burandt E, Sauter G, Simon R, Huland H, Graefen M, Heinzer H, Schlomm T, Heumann A (2018) PSCA expression is associated with favorable tumor features and reduced PSA recurrence in operated prostate cancer. BMC Cancer 18(1):612. https://doi.org/10.1186/s12885-018-4547-7PubMedPubMedCentralCrossRef

48.

Tsourlakis MC, Eleftheriadou A, Stender A, Weigand P, Grupp K, Hube-Magg C, Kluth M, Schroeder C, Steurer S, Hinsch A, Luebke A, Angerer A, Wittmer C, Friedrich E, Gobel C, Buscheck F, Heinzer H, Graefen M, Simon R, Sauter G, Wilczak W, Minner S, Schlomm T, Jacobsen F (2017) FOXA1 expression is a strong independent predictor of early PSA recurrence in ERG negative prostate cancers treated by radical prostatectomy. Carcinogenesis 38(12):1180–1187. https://doi.org/10.1093/carcin/bgx105PubMedCrossRef

49.

Epstein JI, Feng Z, Trock BJ, Pierorazio PM (2012) Upgrading and downgrading of prostate cancer from biopsy to radical prostatectomy: incidence and predictive factors using the modified Gleason grading system and factoring in tertiary grades. Eur Urol 61(5):1019–1024. https://doi.org/10.1016/j.eururo.2012.01.050PubMedPubMedCentralCrossRef

50.

Shah RB, Zhou M, LeBlanc M, Snyder M, Rubin MA (2002) Comparison of the basal cell-specific markers, 34betaE12 and p63, in the diagnosis of prostate cancer. Am J Surg Pathol 26(9):1161–1168PubMedCrossRef

51.

Szasz AM, Nyirady P, Majoros A, Szendroi A, Szucs M, Szekely E, Tokes AM, Romics I, Kulka J (2010) beta-catenin expression and claudin expression pattern as prognostic factors of prostatic cancer progression. BJU Int 105(5):716–722. https://doi.org/10.1111/j.1464-410X.2009.08808.xPubMedCrossRef

52.

Colegio OR, Van Itallie C, Rahner C, Anderson JM (2003) Claudin extracellular domains determine paracellular charge selectivity and resistance but not tight junction fibril architecture. Am J Physiol Cell Physiol 284(6):C1346–1354. https://doi.org/10.1152/ajpcell.00547.2002PubMedCrossRef

53.

Capaldo CT, Nusrat A (2015) Claudin switching: physiological plasticity of the tight junction. Semin Cell Dev Biol 42:22–29. https://doi.org/10.1016/j.semcdb.2015.04.003PubMedCrossRef

54.

Koval M (2013) Claudin heterogeneity and control of lung tight junctions. Annu Rev Physiol 75:551–567. https://doi.org/10.1146/annurev-physiol-030212-183809PubMedCrossRef

55.

Kinugasa T, Akagi Y, Ochi T, Tanaka N, Kawahara A, Ishibashi Y, Gotanda Y, Yamaguchi K, Shiratuchi I, Oka Y, Kage M, Shirouzu K (2012) Increased claudin-1 protein expression in hepatic metastatic lesions of colorectal cancer. Anticancer Res 32(6):2309–2314PubMed

56.

Brase JC, Johannes M, Mannsperger H, Falth M, Metzger J, Kacprzyk LA, Andrasiuk T, Gade S, Meister M, Sirma H, Sauter G, Simon R, Schlomm T, Beissbarth T, Korf U, Kuner R, Sultmann H (2011) TMPRSS2-ERG -specific transcriptional modulation is associated with prostate cancer biomarkers and TGF-beta signaling. BMC Cancer 11:507. https://doi.org/10.1186/1471-2407-11-507PubMedPubMedCentralCrossRef

57.

Gupta S, Iljin K, Sara H, Mpindi JP, Mirtti T, Vainio P, Rantala J, Alanen K, Nees M, Kallioniemi O (2010) FZD4 as a mediator of ERG oncogene-induced WNT signaling and epithelial-to-mesenchymal transition in human prostate cancer cells. Can Res 70(17):6735–6745. https://doi.org/10.1158/0008-5472.CAN-10-0244CrossRef

58.

Jhavar S, Brewer D, Edwards S, Kote-Jarai Z, Attard G, Clark J, Flohr P, Christmas T, Thompson A, Parker M, Shepherd C, Stenman UH, Marchbank T, Playford RJ, Woodhouse C, Ogden C, Fisher C, Kovacs G, Corbishley C, Jameson C, Norman A, De-Bono J, Bjartell A, Eeles R, Cooper CS (2009) Integration of ERG gene mapping and gene-expression profiling identifies distinct categories of human prostate cancer. BJU Int 103(9):1256–1269. https://doi.org/10.1111/j.1464-410X.2008.08200.xPubMedCrossRef

59.

Taylor BS, Schultz N, Hieronymus H, Gopalan A, Xiao Y, Carver BS, Arora VK, Kaushik P, Cerami E, Reva B, Antipin Y, Mitsiades N, Landers T, Dolgalev I, Major JE, Wilson M, Socci ND, Lash AE, Heguy A, Eastham JA, Scher HI, Reuter VE, Scardino PT, Sander C, Sawyers CL, Gerald WL (2010) Integrative genomic profiling of human prostate cancer. Cancer Cell 18(1):11–22. https://doi.org/10.1016/j.ccr.2010.05.026PubMedPubMedCentralCrossRef

60.

Fishilevich S, Nudel R, Rappaport N, Hadar R, Plaschkes I, Iny Stein T, Rosen N, Kohn A, Twik M, Safran M, Lancet D, Cohen D (2017) GeneHancer: genome-wide integration of enhancers and target genes in GeneCards. Database (Oxford). https://doi.org/10.1093/database/bax028CrossRef

61.

Wu L, Zhao JC, Kim J, Jin HJ, Wang CY, Yu J (2013) ERG is a critical regulator of Wnt/LEF1 signaling in prostate cancer. Can Res 73(19):6068–6079. https://doi.org/10.1158/0008-5472.CAN-13-0882CrossRef

62.

Muller J, Ehlers A, Burkhardt L, Sirma H, Steuber T, Graefen M, Sauter G, Minner S, Simon R, Schlomm T, Michl U (2013) Loss of pSer2448-mTOR expression is linked to adverse prognosis and tumor progression in ERG-fusion-positive cancers. Int J Cancer 132(6):1333–1340. https://doi.org/10.1002/ijc.27768PubMedCrossRef

63.

Grupp K, Ospina-Klinck D, Tsourlakis MC, Koop C, Wilczak W, Adam M, Simon R, Sauter G, Izbicki JR, Graefen M, Huland H, Steurer S, Schlomm T, Minner S, Quaas A (2014) NY-ESO-1 expression is tightly linked to TMPRSS2-ERG fusion in prostate cancer. Prostate 74(10):1012–1022. https://doi.org/10.1002/pros.22816PubMedCrossRef

64.

Burdelski C, Bujupi E, Tsourlakis MC, Hube-Magg C, Kluth M, Melling N, Lebok P, Minner S, Koop C, Graefen M, Heinzer H, Wittmer C, Sauter G, Wilczak W, Simon R, Schlomm T, Steurer S, Krech T (2015) Loss of SOX9 expression is associated with PSA recurrence in ERG-positive and PTEN deleted prostate cancers. PLoS ONE 10(6):e0128525. https://doi.org/10.1371/journal.pone.0128525PubMedPubMedCentralCrossRef

65.

Burdelski C, Dieckmann T, Heumann A, Hube-Magg C, Kluth M, Beyer B, Steuber T, Pompe R, Graefen M, Simon R, Minner S, Tsourlakis MC, Koop C, Izbicki J, Sauter G, Krech T, Schlomm T, Wilczak W, Lebok P (2016) p16 upregulation is linked to poor prognosis in ERG negative prostate cancer. Tumour Biol 37(9):12655–12663. https://doi.org/10.1007/s13277-016-5167-yPubMedCrossRef

66.

Stumm L, Burkhardt L, Steurer S, Simon R, Adam M, Becker A, Sauter G, Minner S, Schlomm T, Sirma H, Michl U (2013) Strong expression of the neuronal transcription factor FOXP2 is linked to an increased risk of early PSA recurrence in ERG fusion-negative cancers. J Clin Pathol 66(7):563–568. https://doi.org/10.1136/jclinpath-2012-201335PubMedCrossRef

67.

Grupp K, Boumesli R, Tsourlakis MC, Koop C, Wilczak W, Adam M, Sauter G, Simon R, Izbicki JR, Graefen M, Huland H, Steurer S, Schlomm T, Minner S, Quaas A (2014) The prognostic impact of high Nijmegen breakage syndrome (NBS1) gene expression in ERG-negative prostate cancers lacking PTEN deletion is driven by KPNA2 expression. Int J Cancer 135(6):1399–1407. https://doi.org/10.1002/ijc.28778PubMedCrossRef

68.

Heumann A, Heinemann N, Hube-Magg C, Lang DS, Grupp K, Kluth M, Minner S, Moller-Koop C, Graefen M, Heinzer H, Tsourlakis MC, Wilczak W, Wittmer C, Jacobsen F, Huland H, Simon R, Schlomm T, Sauter G, Steurer S, Lebok P, Hinsch A (2018) High BCAR1 expression is associated with early PSA recurrence in ERG negative prostate cancer. BMC Cancer 18(1):37. https://doi.org/10.1186/s12885-017-3956-3PubMedPubMedCentralCrossRef

69.

Melling N, Rashed M, Schroeder C, Hube-Magg C, Kluth M, Lang D, Simon R, Moller-Koop C, Steurer S, Sauter G, Jacobsen F, Buscheck F, Wittmer C, Clauditz T, Krech T, Tsourlakis MC, Minner S, Huland H, Graefen M, Budaus L, Thederan I, Salomon G, Schlomm T, Wilczak W (2017) High-level gamma-glutamyl-hydrolase (ggh) expression is linked to poor prognosis in ERG negative prostate cancer. Int J Mol Sci 18(2):286. https://doi.org/10.3390/ijms18020286PubMedCentralCrossRef

70.

Grupp K, Jedrzejewska K, Tsourlakis MC, Koop C, Wilczak W, Adam M, Quaas A, Sauter G, Simon R, Izbicki JR, Graefen M, Huland H, Schlomm T, Minner S, Steurer S (2013) High mitochondria content is associated with prostate cancer disease progression. Mol Cancer 12(1):145. https://doi.org/10.1186/1476-4598-12-145PubMedPubMedCentralCrossRef

71.

Kluth M, Runte F, Barow P, Omari J, Abdelaziz ZM, Paustian L, Steurer S, Christina Tsourlakis M, Fisch M, Graefen M, Tennstedt P, Huland H, Michl U, Minner S, Sauter G, Simon R, Adam M, Schlomm T (2015) Concurrent deletion of 16q23 and PTEN is an independent prognostic feature in prostate cancer. Int J Cancer 137(10):2354–2363. https://doi.org/10.1002/ijc.29613PubMedCrossRef

72.

Semba S, Satake S, Matsushita M, Yokozaki H (2009) Phosphatase activity of nuclear PTEN is required for CDX2-mediated intestinal differentiation of gastric carcinoma. Cancer Lett 274(1):143–150. https://doi.org/10.1016/j.canlet.2008.09.019PubMedCrossRef

73.

Egevad L, Ahmad AS, Algaba F, Berney DM, Boccon-Gibod L, Comperat E, Evans AJ, Griffiths D, Grobholz R, Kristiansen G, Langner C, Lopez-Beltran A, Montironi R, Moss S, Oliveira P, Vainer B, Varma M, Camparo P (2013) Standardization of Gleason grading among 337 European pathologists. Histopathology 62(2):247–256. https://doi.org/10.1111/his.12008PubMedCrossRef

74.

Wilczak W, Wittmer C, Clauditz T, Minner S, Steurer S, Buscheck F, Krech T, Lennartz M, Harms L, Leleu D, Ahrens M, Ingwerth S, Gunther CT, Koop C, Simon R, Jacobsen F, Tsourlakis MC, Chirico V, Hoflmayer D, Vettorazzi E, Haese A, Steuber T, Salomon G, Michl U, Budaus L, Tilki D, Thederan I, Fraune C, Gobel C, Henrich MC, Juhnke M, Moller K, Bawahab AA, Uhlig R, Adam M, Weidemann S, Beyer B, Huland H, Graefen M, Sauter G, Schlomm T (2018) Marked prognostic impact of minimal lymphatic tumor spread in prostate cancer. Eur Urol 74(3):376–386. https://doi.org/10.1016/j.eururo.2018.05.034PubMedCrossRef

Title: Claudin-1 upregulation is associated with favorable tumor features and a reduced risk for biochemical recurrence in ERG-positive prostate cancer
Authors: Simon Kind
Franziska Büscheck
Doris Höflmayer
Claudia Hube-Magg
Martina Kluth
Maria Christina Tsourlakis
Stefan Steurer
Till S. Clauditz
Andreas M. Luebke
Eike Burandt
Waldemar Wilczak
Andrea Hinsch
David Dum
Sören Weidemann
Christoph Fraune
Burkhard Beyer
Thomas Steuber
Hartwig Huland
Markus Graefen
Margit Fisch
Ronald Simon
Guido Sauter
Thorsten Schlomm
Sarah Minner
Till Eichenauer
Publication date: 01-09-2020
Publisher: Springer Berlin Heidelberg
Keywords: Prostate Cancer
Prostate Cancer
Published in: World Journal of Urology / Issue 9/2020
Print ISSN: 0724-4983
Electronic ISSN: 1433-8726
DOI: https://doi.org/10.1007/s00345-019-03017-w

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Claudin-1 upregulation is associated with favorable tumor features and a reduced risk for biochemical recurrence in ERG-positive prostate cancer

Abstract

Background

Material and methods

Results

Conclusion

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Material and methods

Results

Conclusion

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