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Diagnostic Pathology
Published in: Diagnostic Pathology 1/2009

Open Access 01-12-2009 | Research

CD10 expression in urothelial carcinoma of the bladder

Authors: Burak Bahadir, Kemal Behzatoglu, Sibel Bektas, Erol R Bozkurt, Sukru O Ozdamar

Published in: Diagnostic Pathology | Issue 1/2009

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Abstract

Background

CD10 antigen is a 100-kDa-cell surface zinc metalloendopeptidase and it is expressed in a variety of normal and neoplastic lymphoid and nonlymphoid tissues. The aim of this study was to evaluate CD10 expression in urothelial carcinoma of the urinary bladder and to determine the correlation between immunohistochemical (IHC) CD10 expression and histopathologic parameters including grade and stage.

Methods

371 cases of urothelial bladder carcinomas, all from transurethral resections, were included in this study. Hematoxylin-eosin (HE) stained sections from each case were reevaluated histopathologically according to WHO 2004 grading system. The TNM system was used for pathologic staging. Selected slides were also studied by IHC and a semiquantitative scoring for CD10 expression based on the percentage of positive cells was performed.

Results

157 cases (42.3%) showed immunostaining while 214 cases (57.7%) were negative for CD10. 1+ staining was seen in 65 CD10 positive cases (41.4%), and 2+ in 92 cases (58.6%). Overall CD10 expression as well as 2+ immunostaining was significantly correlated with high histologic grade. Overall CD10 expression was also significantly higher in invasive pT1 and pT2-3 tumors compared to noninvasive pTa tumors. pT1 and pT2-3 tumors were also significantly correlated with 2+ immunostaining.

Conclusion

To date, only a few comparative IHC studies have assessed CD10 expression in urothelial carcinoma of the urinary bladder and this study represents the largest series. Our findings indicate that CD10 expression is strongly correlated with high tumor grade and stage in urothelial carcinoma of the bladder, and that CD10 may be associated with tumor progression in bladder cancer pathogenesis.
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Literature
1.
Parkin DM, Bray F, Ferlay J, Pisani P: Global Cancer Statistics, 2002. CA Cancer J Clin. 2005, 55: 74-108. 10.3322/canjclin.55.2.74.CrossRefPubMed
2.
Torti FM, Lum BL: The biology and treatment of superficial bladder cancer. J Clin Oncol. 1984, 2: 505-31.PubMed
3.
Witjes JA, Caris CT, Mungan NA, Debruyne FM, Witjes WP: Results of a randomized phase III trial of sequential intravesical therapy with mitomycin C and bacillus Calmette-Guerin versus mitomycin C alone in patients with superficial bladder cancer. J Urol. 1998, 160: 1668-1671. 10.1016/S0022-5347(01)62377-2. discussion 1671-1672CrossRefPubMed
4.
Huland H, Otto U, Droese M, Klöppel G: Long-term mitomycin C instillation after transurethral resection of superficial bladder carcinoma: influence on recurrence, progression and survival. J Urol. 1984, 132: 27-29.PubMed
5.
Kaufman DS, Shipley WU, Griffin PP, Heney NM, Althausen AF, Efird JT: Selective bladder preservation by combination treatment of invasive bladder cancer. N Engl J Med. 1993, 329: 1377-1382. 10.1056/NEJM199311043291903.CrossRefPubMed
6.
Soloway MS: Evaluation and management of patients with superficial bladder cancer. Urol Clin North Am. 1987, 14: 771-780.PubMed
7.
Holmäng S, Hedelin H, Anderström C, Johansson SL: The relationship among multiple recurrences, progression and prognosis of patients with stages Ta and T1 transitional cell cancer of the bladder followed for at least 20 years. J Uro. 1995, 153: 1823-1826. 10.1016/S0022-5347(01)67321-X. discussion 1826-1827CrossRef
8.
LeBien TW, McCormack RT: The common acute lymphoblastic leukemia antigen (CD10)--emancipation from a functional enigma. Blood. 1989, 73: 625-635.PubMed
9.
Shipp MA, Look AT: Hematopoietic differentiation antigens that are membrane-associated enzymes: Cutting is the key!. Blood. 1993, 82: 1052-1070.PubMed
10.
Arber DA, Weiss LM: CD10: a review. Appl Immunohistochem Mol Morphol. 1997, 5: 125-140. 10.1097/00022744-199709000-00001.CrossRef
11.
Brown G, Hogg N, Greaves M: Candidate leukaemia-specific antigen in man. Nature. 1975, 258: 454-456. 10.1038/258454a0.CrossRefPubMed
12.
Metzgar RS, Borowitz MJ, Jones NH, Dowell BL: Distribution of common acute lymphoblastic leukemia antigen in nonhematopoietic tissues. J Exp Med. 1981, 154: 1249-1254. 10.1084/jem.154.4.1249.CrossRefPubMed
13.
Platt JL, LeBien TW, Michael AF: Stages of renal ontogenesis identified by monoclonal antibodies reactive with lymphohemopoietic differentiation antigens. J Exp Med. 1983, 157: 155-172. 10.1084/jem.157.1.155.CrossRefPubMed
14.
Braun MP, Martin PJ, Ledbetter JA, Hansen JA: Granulocytes and cultured human fibroblasts express common acute lymphoblastic leukemia-associated antigens. Blood. 1983, 61: 718-725.PubMed
15.
Loke SL, Leung CY, Chiu KY, Yau WL, Cheung KN, Ma L: Localisation of CD10 to biliary canaliculi by immunoelectron microscopical examination. J Clin Pathol. 1990, 43: 654-656. 10.1136/jcp.43.8.654.PubMedCentralCrossRefPubMed
16.
Gusterson BA, Monaghan P, Mahendran R, Ellis J, O'Hare MJ: Identification of myoepithelial cells in human and rat breasts byanti-common acute lymphoblastic leukemia antigen antibody A 12. Natl Cancer Inst. 1986, 77: 343-349.
17.
Quackenbush EJ, Gougos A, Baumal R, Letarte M: Differential localization within human kidney of five membrane proteins expressed on acute lymphoblastic leukemia cells. J Immunol. 1986, 136: 118-124.PubMed
18.
Sunday ME, Hua J, Torday JS, Reyes B, Shipp MA: CD10/neutral endopeptidase 24.11 in developing human fetal lung. Patterns of expression and modulation of peptide-mediated proliferation. J Clin Invest. 1992, 90: 2517-2525. 10.1172/JCI116145.PubMedCentralCrossRefPubMed
19.
Hokland P, Rosenthal P, Griffin JD, Nadler LM, Daley J, Hokland M, Schlossman SF, Ritz J: Purification and characterization of fetal hematopoietic cells that express the common acute lymphoblastic leukemia antigen (CALLA). J Exp Med. 1983, 157: 114-129. 10.1084/jem.157.1.114.CrossRefPubMed
20.
Greaves MF, Hariri G, Newman RA, Sutherland DR, Ritter MA, Ritz J: Selective expression of the common acute lymphoblastic leukemia (gp 100) antigen on immature lymphoid cells and their malignant counterparts. Blood. 1983, 61: 628-639.PubMed
21.
Swerdlow S, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, Thiele J, Vardiman JW: WHO Classification of Tumors of Hematopoietic and Lymphoid Tissues. 2008, Lyon: IARC
22.
Liu YJ, Johnson GD, Gordon J, MacLennan IC: Germinal centres in T-cell-dependent antibody responses. Immunol Today. 1992, 13: 17-21. 10.1016/0167-5699(92)90199-H.CrossRefPubMed
23.
Chu P, Arber DA: Paraffin-section detection of CD10 in 505 nonhematopoietic neoplasms. Frequent expression in renal cell carcinoma and endometrial stromal sarcoma. J Clin Pathol. 2000, 113: 374-382. 10.1309/8VAV-J2FU-8CU9-EK18.CrossRef
24.
Chu PG, Arber DA, Weiss LM, Chang KL: Utility of CD10 in distinguishing between endometrial stromal sarcoma and uterine smooth muscle tumors: an immunohistochemical comparison of 34 cases. Mod Pathol. 2001, 14: 465-471. 10.1038/modpathol.3880335.CrossRefPubMed
25.
McCluggage WG, Sumathi VP, Maxwell P: CD10 is a sensitive and diagnostically useful immunohistochemical marker of normal endometrial stroma and of endometrial stromal neoplasms. Histopathology. 2001, 39: 273-278. 10.1046/j.1365-2559.2001.01215.x.CrossRefPubMed
26.
Toki T, Shimizu M, Takagi Y, Ashida T, Konishi I: CD10 is a marker for normal and neoplastic endometrial stromal cells. Int J Gynecol Pathol. 2002, 21: 41-47. 10.1097/00004347-200201000-00008.CrossRefPubMed
27.
Notohara K, Hamazaki S, Tsukayama C, Nakamoto S, Kawabata K, Mizobuchi K, Sakamoto K, Okada S: Solidpseudopapillary tumor of the pancreas: immunohistochemical localization of neuroendocrine markers and CD10. Am J Surg Pathol. 2000, 24: 1361-1371. 10.1097/00000478-200010000-00005.CrossRefPubMed
28.
Tawfic S, Niehans GA, Manivel JC: The pattern of CD10 expression in selected pathologic entities of the prostate gland. Hum Pathol. 2003, 34: 450-456. 10.1016/S0046-8177(03)00077-7.CrossRefPubMed
29.
Kanitakis J, Narvaez D, Claudy A: Differential expression of the CD10 antigen (neutral endopeptidase) in primary versus metastatic malignant melanomas of the skin. Melanoma Res. 2002, 12: 241-244. 10.1097/00008390-200206000-00007.CrossRefPubMed
30.
Carrel S, Zografos L, Schreyer M, Rimoldi D: Expression of CALLA/CD10 on human melanoma cells. Melanoma Res. 1993, 3: 319-323. 10.1097/00008390-199310000-00003.CrossRefPubMed
31.
Bilalovic N, Sandstad B, Golouh R, Nesland JM, Selak I, Torlakovic EE: CD10 protein expression in tumor and stromal cells of malignant melanoma is associated with tumor progression. Modern Pathology. 2004, 17: 1251-1258. 10.1038/modpathol.3800174.CrossRefPubMed
32.
Sato Y, Itoh F, Hinoda Y, Ohe Y, Nakagawa N, Ueda R, Yachi A, Imai K: Expression of CD10/neutral endopeptidase in normal and malignant tissues of the human stomach and colon. J Gastroenterol. 1996, 31: 12-17. 10.1007/BF01211181.CrossRefPubMed
33.
McIntosh GG, Lodge AJ, Watson P, Hall AG, Wood K, Anderson JJ, Angus B, Horne CH, Milton ID: NCL-CD10-270: a new monoclonal antibody recognizing CD10 in parafin-embedded tissue. Am J Pathol. 1999, 154: 77-82.PubMedCentralCrossRefPubMed
34.
Shipp MA, Stefano GB, D'Adamio L, Switzer SN, Howard FD, Sinisterra J, Scharrer B, Reinherz EL: Downregulation of enkephalin-mediated inflammatory responses by CD10/neutral endopeptidase 24.11. Nature. 1990, 347: 394-396. 10.1038/347394a0.CrossRefPubMed
35.
Cutrona G, Ulivi M, Fais F, Roncella S, Ferrarini M: Transfection of the c-myc oncogene into normal Epstein-Barr virus-harboring B cells results in new phenotypic and functional features resembling those of Burkitt lymphoma cells and normal centroblasts. J Exp Med. 1995, 181: 699-711. 10.1084/jem.181.2.699.CrossRefPubMed
36.
Cutrona G, Leanza N, Ulivi M, Melioli G, Burgio VL, Mazzarello G, Gabutti G, Roncella S, Ferrarini M: Expression of CD10 by human T cells that undergo apoptosis both in vitro and in vivo. Blood. 1999, 94: 3067-3076.PubMed
37.
Morabito F, Mangiola M, Rapezzi D, Zupo S, Oliva BM, Ferraris AM, Spriano M, Rossi E, Stelitano C, Callea V, Cutrona G, Ferrarini M: Expression of CD10 by B-chronic lymphocytic leukemia cells undergoing apoptosis in vivo and in vitro. Haematologica. 2003, 88: 864-873.PubMed
38.
Sumitomo M, Shen R, Walburg M, Dai J, Geng Y, Navarro D, Boileau G, Papandreou CN, Giancotti FG, Knudsen B, Nanus DM: Neutral endopeptidase inhibits prostate cancer cell migration by blocking focal adhesion kinase signaling. J Clin Invest. 2000, 106: 1399-1407. 10.1172/JCI10536.PubMedCentralCrossRefPubMed
39.
Kondepudi A, Johnson A: Cytokines increase neutral endopeptidase activity in lung fibroblasts. Am J Respir Cell Mol Biol. 1993, 8: 43-49.CrossRefPubMed
40.
Velden van der VH, Naber BA, Spoel van der P, Hoogsteden HC, Versnel MA: Cytokines and glucocorticoids modulate human bronchial epithelial cell peptidases. Cytokine. 1998, 10: 55-65. 10.1006/cyto.1997.0257.CrossRefPubMed
41.
Papandreou CN, Usmani B, Geng Y, Bogenrieder T, Freeman R, Wilk S, Finstad CL, Reuter VE, Powell CT, Scheinberg D, Magill C, Scher HI, Albino AP, Nanus DM: Neutral endopeptidase 24.11 loss in metastatic human prostate cancer contributes to androgen-independent progression. Nat Med. 1998, 4: 50-57. 10.1038/nm0198-050.CrossRefPubMed
42.
Iwaya K, Ogawa H, Izumi M, Kuroda M, Mukai K: Stromal expression of CD10 in invasive breast carcinoma: a new predictor of clinical outcome. Virchows Arch. 2002, 440: 589-593. 10.1007/s00428-002-0639-4.CrossRefPubMed
43.
Koiso K, Akaza H, Ohtani M, Miyanaga N, Aoyagi K: A new tumor marker for bladder cancer. Int J Urol. 1994, 1: 33-36. 10.1111/j.1442-2042.1994.tb00005.x.CrossRefPubMed
44.
Murali R, Delprado W: CD10 ýmmunohistochemical staining in urothelial neoplasms. Am J Clin Pathol. 2005, 124: 371-379. 10.1309/04BHF6A80BQMH7HT.CrossRefPubMed
45.
Bircan S, Candir O, Kapucuoglu N, Serel TA, Ciris M, Karahan N: CD10 expression in urothelial bladder carcinomas: A pilot study. Urol Int. 2006, 77: 107-113. 10.1159/000093901.CrossRefPubMed
46.
Abdou AG: CD10 expression in tumour and stromal cells of bladder carcinoma: an association with bilharziasis. APMIS. 2007, 115: 1206-1218. 10.1111/j.1600-0643.2007.00645.x.CrossRefPubMed
47.
Sauter G, Algaba F, Amin MB, Busch C, Cheville J, Gasser T, Grignon D, Hofstaedter F, Lopez-Beltran A, Epstein JI: Non-invasive urothelial neoplasias. WHO classification of non-invasive papillary urothelial tumors. Edited by: Eble JN, Sauter G, Epstein JI, Sesterhenn I. 2004, Lyon: IARC Press, 89-157.
48.
Sobin LH, Wittekind C: TNM Classification of Malignant Tumours. 2002, New York: Wiley-Liss
49.
Mitra AP, Datar RH, Cote RJ: Molecular staging of bladder cancer. BJU Int. 2005, 96: 7-12. 10.1111/j.1464-410X.2005.05557.x.CrossRefPubMed
50.
Shariat SF, Tokunaga H, Zhou J, Kim J, Ayala GE, Benedict WF, Lerner SP: p53, p21, pRB, and p16 expression predict clinical outcome in cystectomy with bladder cancer. J Clin Oncol. 2004, 22: 1014-1024. 10.1200/JCO.2004.03.118.CrossRefPubMed
51.
Esrig D, Elmajian D, Groshen S, Freeman JA, Stein JP, Chen SC, Nichols PW, Skinner DG, Jones PA, Cote RJ: Accumulation of nuclear p53 and tumor progression in bladder cancer. N Engl J Med. 1994, 331: 1259-1264. 10.1056/NEJM199411103311903.CrossRefPubMed
52.
Lipponen PK: Over-expression of p53 nuclear oncoprotein in transitional-cell bladder cancer and its prognostic value. Int J Cancer. 1993, 53: 365-370. 10.1002/ijc.2910530304.CrossRefPubMed
53.
Juhl BR, Hartzen SH, Hainau B: A, B, H antigen expression in transitional cell carcinomas of the urinary bladder. Cancer. 1986, 57: 1768-1775. 10.1002/1097-0142(19860501)57:9<1768::AID-CNCR2820570910>3.0.CO;2-E.CrossRefPubMed
54.
Srinivas V, Orihuela E, Lloyd KO, Old LJ, Whitmore WF: Estimation of ABO(H) isoantigen expression in bladder tumors. J Urol. 1985, 133: 25-28.PubMed
55.
Sarkis AS, Dalbagni G, Cordon-Cardo C, Zhang ZF, Sheinfeld J, Fair WR, Herr HW, Reuter VE: Nuclear overexpression of p53 protein in transitional cell bladder carcinoma: a marker for disease progression. J Natl Cancer Inst. 1993, 85: 53-59. 10.1093/jnci/85.1.53.CrossRefPubMed
56.
Otto T, Bex A, Schmidt U, Raz A, Rübben H: Improved prognosis assessment for patients with bladder carcinoma. Am J Pathol. 1997, 150: 1919-1923.PubMedCentralPubMed
57.
Toma V, Hauri D, Schmid U, Ackermann D, Maurer R, Alund G, Knönagel H, Rist M, Gasser TC, Sauter G, Roth J: Focal loss of CD44 variant protein expression is related to recurrence in superficial bladder carcinoma. Am J Pathol. 1999, 155: 1427-1432.PubMedCentralCrossRefPubMed
58.
Del Pizzo JJ, Borkowski A, Jacobs SC, Kyprianou N: Loss of cell cycle regulators p27(Kip1) and cyclin E in transitional cell carcinoma of the bladder correlates with tumor grade and patient survival. Am J Pathol. 1999, 155: 1129-1136.PubMedCentralCrossRefPubMed
59.
Schoenberg M: Biomarkers for transitional cell carcinoma-con. Urology. 2001, 57: 849-851. 10.1016/S0090-4295(01)00975-X.CrossRefPubMed
60.
Basset P, Wolf C, Rouyer N, Bellocq JP, Rio MC, Chambon P: Stromelysin-3 in stromal tissue as a control factor in breast cancer behavior. Cancer. 1994, 74: 1045-1049. 10.1002/1097-0142(19940801)74:3+<1045::AID-CNCR2820741511>3.0.CO;2-7.CrossRefPubMed
61.
Talvensaari-Mattila A, Pääkkö P, Höyhtyä M, Blanco-Sequeiros G, Turpeenniemi-Hujanen T: Matrix metalloproteinase-2 immunoreactive protein: a marker of aggressiveness in breast carcinoma. Cancer. 1998, 83: 1153-1162. 10.1002/(SICI)1097-0142(19980915)83:6<1153::AID-CNCR14>3.0.CO;2-4.CrossRefPubMed
62.
Cheng L, Neumann RM, Nehra A, Spotts BE, Weaver AL, Bostwick DG: Cancer heterogeneity and its biologic implications in the grading of urothelial carcinoma. Cancer. 2000, 88: 1663-1670. 10.1002/(SICI)1097-0142(20000401)88:7<1663::AID-CNCR21>3.0.CO;2-8.CrossRefPubMed
63.
Lee R, Droller MJ: The natural history of bladder cancer: implications for therapy. Urol Clin N Am. 2000, 27: 1-13. 10.1016/S0094-0143(05)70229-9.CrossRef
64.
Cheng L, Cheville JC, Neumann RM, Bostwick DG: Natural history of urothelial dysplasia of the bladder. Am J Surg Pathol. 1999, 23: 443-447. 10.1097/00000478-199904000-00009.CrossRefPubMed
65.
Bai M, Agnantis NJ, Skyrlas A, Tsanou E, Kamina S, Galani V, Kanavaros P: Increased expression of the Bcl6 and CD10 proteins is associated with increased apoptosis and proliferation in diffuse large B-cell lymphomas. Mod Pathol. 2003, 16: 471-480. 10.1097/01.MP.0000067684.78221.6E.CrossRefPubMed
66.
Di Maria GU, Bellofiore S, Geppetti P: Regulation of airway neurogenic inflammation by neutral endopeptidase. Eur Respir J. 1998, 12: 1454-1462. 10.1183/09031936.98.12061454.CrossRefPubMed
67.
Ordi J, Romagosa C, Tavassoli FA, Nogales F, Palacin A, Condom E, Torne A, Cardesa A: CD10 expression in epithelial tissues and tumors of the gynecologic tract: a useful marker in the diagnosis of mesonephric, trophoblastic, and clear cell tumors. Am J Surg Pathol. 2003, 27: 178-186. 10.1097/00000478-200302000-00005.CrossRefPubMed
68.
Cameron RI, Ashe P, O'Rourke DM, Foster H, McCluggage WG: A panel of immunohistochemical stains assists in the distinction between ovarian and renal clear cell carcinoma. Int J Gynecol Pathol. 2003, 22: 272-276. 10.1097/01.PGP.0000071044.12278.43.CrossRefPubMed
69.
Cohen AJ, Bunn PA, Franklin W, Magill-Solc C, Hartmann C, Helfrich B, Gilman L, Folkvord J, Helm K, Miller YE: Neutral endopeptidase: variable expression in human lung, inactivation in lung cancer, and modulation of peptide-induced calcium flux. Cancer Res. 1996, 56: 831-839.PubMed
70.
Ogawa H, Iwaya K, Izumi M, Kuroda M, Serizawa H, Koyanagi Y, Mukai K: Expression of CD10 by stromal cells during colorectal tumor development. Hum Pathol. 2002, 33: 806-811. 10.1053/hupa.2002.125773.CrossRefPubMed
71.
Yao T, Takata M, Tustsumi S, Nishiyama K, Taguchi K, Nagai E, Tsuneyoshi M: Phenotypic expression of gastrointestinal differentiation markers in colorectal adenocarcinomas with liver metastasis. Pathology. 2002, 34: 556-560. 10.1080/0031302021000035965-4.CrossRefPubMed
72.
Dai J, Shen R, Sumitomo M, Goldberg JS, Geng Y, Navarro D, Xu S, Koutcher JA, Garzotto M, Powell CT, Nanus DM: Tumor suppressive effects of neutral endopeptidase in androgen-independent prostate cancer cells. Clin Cancer Res. 2001, 7: 1370-1377.PubMed
Metadata
Title
CD10 expression in urothelial carcinoma of the bladder
Authors
Burak Bahadir
Kemal Behzatoglu
Sibel Bektas
Erol R Bozkurt
Sukru O Ozdamar
Publication date
01-12-2009
Publisher
BioMed Central
Published in
Diagnostic Pathology / Issue 1/2009
Electronic ISSN: 1746-1596
DOI
https://doi.org/10.1186/1746-1596-4-38

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