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Molecules involved in epithelial–mesenchymal transition and epithelial–stromal interaction in phyllodes tumors: implications for histologic grade and prognosis

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Tumor Biology

Abstract

The aim of this study was to investigate the expression of molecules associated with epithelial–mesenchymal transition (EMT) and epithelial–stromal interactions (ESI) and to evaluate their roles in phyllodes tumors (PTs). Tissue microarrays (TMAs) were constructed from 207 PT specimens (157 benign, 34 borderline and 16 malignant). The presence of EMT-related markers including N-cadherin, Twist, TGF-beta, HMGA2, S100A4 and Ezrin as well as ESI-related molecules such as SDF1 and CXCR4 among the TMAs was assessed immunohistochemically. Immunohistochemical results were analyzed in terms of clinicopathologic parameters. For higher grade PTs, expressions of Twist (p < 0.001), HMGA2 (p = 0.005), S100A4 (p < 0.001), CXCR4 (p < 0.001) and TGF-beta (p < 0.001) were higher. As PTs showed higher stromal cellularity, higher stromal mitosis, stromal overgrowth and infiltrative tumor margin, the expressions of Twist, HMGA2 and CXCR4 in the stromal component thereof were increased (p < 0.05). High Twist expression in the stromal component was associated with shorter disease-free survival (DFS) and overall survival (OS) (p < 0.001) as well as shorter OS in multivariate COX analysis (p = 0.031, odds ratio: 24.6). In conclusion, the expressions of Twist, HMGA2, TGF-beta and S100A4, which are EMT-associated molecules, and CXCR4, an ESI-associated molecule, were increased in the stromal component of advanced grade PTs. Further, high expression of Twist in the stromal component was correlated with poorer prognoses.

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References

  1. Tavassoli FADP. World Heath Organization classification of tumors. Pathogenesis and genetics of tumors of the breast and female genital tract. Lyon: IARC Press; 2003.

    Google Scholar 

  2. Anderson B, Lawton T, Lehman C, Moe R. Phyllodes tumor. In: Morrow M, Osborne C, editors. Disease of the breast. Philadelphia: Lippincott & Wilkins; 2004. p. 991–1006.

    Google Scholar 

  3. Ben Hassouna J, Damak T, Gamoudi A, Chargui R, Khomsi F, Mahjoub S, Slimene M, Ben Dhiab T, Hechiche M, Boussen H, Rahal K. Phyllodes tumors of the breast: a case series of 106 patients. Am J Surg. 2006;192(2):141–7. doi:10.1016/j.amjsurg.2006.04.007.

    Article  PubMed  Google Scholar 

  4. Noguchi S, Motomura K, Inaji H, Imaoka S, Koyama H. Clonal analysis of fibroadenoma and phyllodes tumor of the breast. Cancer Res. 1993;53(17):4071–4.

    PubMed  CAS  Google Scholar 

  5. Sawyer EJ, Hanby AM, Ellis P, Lakhani SR, Ellis IO, Boyle S, Tomlinson IP. Molecular analysis of phyllodes tumors reveals distinct changes in the epithelial and stromal components. Am J Pathol. 2000;156(3):1093–8. doi:10.1016/s0002-9440(10)64977-2.

    Article  PubMed  CAS  Google Scholar 

  6. Duband JL, Monier F, Delannet M, Newgreen D. Epithelium–mesenchyme transition during neural crest development. Acta Anat (Basel). 1995;154(1):63–78.

    Article  CAS  Google Scholar 

  7. Kalluri R, Neilson EG. Epithelial–mesenchymal transition and its implications for fibrosis. J Clin Investig. 2003;112(12):1776–84. doi:10.1172/jci20530.

    PubMed  CAS  Google Scholar 

  8. Thiery JP. Epithelial–mesenchymal transitions in tumour progression. Nat Rev Cancer. 2002;2(6):442–54. doi:10.1038/nrc822.

    Article  PubMed  CAS  Google Scholar 

  9. Hay ED. An overview of epithelio-mesenchymal transformation. Acta Anat (Basel). 1995;154(1):8–20.

    Article  CAS  Google Scholar 

  10. Lee JM, Dedhar S, Kalluri R, Thompson EW. The epithelial–mesenchymal transition: new insights in signaling, development, and disease. J Cell Biol. 2006;172(7):973–81. doi:10.1083/jcb.200601018.

    Article  PubMed  CAS  Google Scholar 

  11. Thiery JP, Sleeman JP. Complex networks orchestrate epithelial–mesenchymal transitions. Nat Rev Mol Cell Biol. 2006;7(2):131–42. doi:10.1038/nrm1835.

    Article  PubMed  CAS  Google Scholar 

  12. Blick T, Widodo E, Hugo H, Waltham M, Lenburg ME, Neve RM, Thompson EW. Epithelial mesenchymal transition traits in human breast cancer cell lines. Clin Exp Metastasis. 2008;25(6):629–42. doi:10.1007/s10585-008-9170-6.

    Article  PubMed  CAS  Google Scholar 

  13. Sarrio D, Rodriguez-Pinilla SM, Hardisson D, Cano A, Moreno-Bueno G, Palacios J. Epithelial–mesenchymal transition in breast cancer relates to the basal-like phenotype. Cancer Res. 2008;68(4):989–97. doi:10.1158/0008-5472.can-07-2017.

    Article  PubMed  CAS  Google Scholar 

  14. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, Campbell LL, Polyak K, Brisken C, Yang J, Weinberg RA. The epithelial–mesenchymal transition generates cells with properties of stem cells. Cell. 2008;133(4):704–15. doi:10.1016/j.cell.2008.03.027.

    Article  PubMed  CAS  Google Scholar 

  15. Morel AP, Lievre M, Thomas C, Hinkal G, Ansieau S, Puisieux A. Generation of breast cancer stem cells through epithelial–mesenchymal transition. PLoS One. 2008;3(8):e2888. doi:10.1371/journal.pone.0002888.

    Article  PubMed  Google Scholar 

  16. Debies MT, Gestl SA, Mathers JL, Mikse OR, Leonard TL, Moody SE, Chodosh LA, Cardiff RD, Gunther EJ. Tumor escape in a Wnt1-dependent mouse breast cancer model is enabled by p19Arf/p53 pathway lesions but not p16 Ink4a loss. J Clin Investig. 2008;118(1):51–63. doi:10.1172/jci33320.

    Article  PubMed  CAS  Google Scholar 

  17. Moody SE, Perez D, Pan TC, Sarkisian CJ, Portocarrero CP, Sterner CJ, Notorfrancesco KL, Cardiff RD, Chodosh LA. The transcriptional repressor Snail promotes mammary tumor recurrence. Cancer Cell. 2005;8(3):197–209. doi:10.1016/j.ccr.2005.07.009.

    Article  PubMed  CAS  Google Scholar 

  18. Yu L, Lu S, Tian J, Ma J, Li J, Wang H, Xu W. TWIST expression in hypopharyngeal cancer and the mechanism of TWIST-induced promotion of metastasis. Oncol Rep. 2011. doi:10.3892/or.2011.1481.

  19. Yuen HF, Chan YP, Wong ML, Kwok WK, Chan KK, Lee PY, Srivastava G, Law SY, Wong YC, Wang X, Chan KW. Upregulation of Twist in oesophageal squamous cell carcinoma is associated with neoplastic transformation and distant metastasis. J Clin Pathol. 2007;60(5):510–4. doi:10.1136/jcp.2006.039099.

    Article  PubMed  CAS  Google Scholar 

  20. Hristov AC, Cope L, Reyes MD, Singh M, Iacobuzio-Donahue C, Maitra A, Resar LM. HMGA2 protein expression correlates with lymph node metastasis and increased tumor grade in pancreatic ductal adenocarcinoma. Mod Pathol. 2009;22(1):43–9. doi:10.1038/modpathol.2008.140.

    Article  PubMed  CAS  Google Scholar 

  21. Park SM, Shell S, Radjabi AR, Schickel R, Feig C, Boyerinas B, Dinulescu DM, Lengyel E, Peter ME. Let-7 prevents early cancer progression by suppressing expression of the embryonic gene HMGA2. Cell Cycle. 2007;6(21):2585–90.

    Article  PubMed  CAS  Google Scholar 

  22. Peng Y, Laser J, Shi G, Mittal K, Melamed J, Lee P, Wei JJ. Antiproliferative effects by Let-7 repression of high-mobility group A2 in uterine leiomyoma. Mol Cancer Res. 2008;6(4):663–73. doi:10.1158/1541-7786.mcr-07-0370.

    Article  PubMed  CAS  Google Scholar 

  23. Shell S, Park SM, Radjabi AR, Schickel R, Kistner EO, Jewell DA, Feig C, Lengyel E, Peter ME. Let-7 expression defines two differentiation stages of cancer. Proc Natl Acad Sci U S A. 2007;104(27):11400–5. doi:10.1073/pnas.0704372104.

    Article  PubMed  CAS  Google Scholar 

  24. Xue C, Plieth D, Venkov C, Xu C, Neilson EG. The gatekeeper effect of epithelial–mesenchymal transition regulates the frequency of breast cancer metastasis. Cancer Res. 2003;63(12):3386–94.

    PubMed  CAS  Google Scholar 

  25. Yonemura Y, Endou Y, Kimura K, Fushida S, Bandou E, Taniguchi K, Kinoshita K, Ninomiya I, Sugiyama K, Heizmann CW, Schafer BW, Sasaki T. Inverse expression of S100A4 and E-cadherin is associated with metastatic potential in gastric cancer. Clin Cancer Res. 2000;6(11):4234–42.

    PubMed  CAS  Google Scholar 

  26. Wheelock MJ, Shintani Y, Maeda M, Fukumoto Y, Johnson KR. Cadherin switching. J Cell Sci. 2008;121(Pt 6):727–35. doi:10.1242/jcs.000455.

    Article  PubMed  CAS  Google Scholar 

  27. Hunter KW. Ezrin, a key component in tumor metastasis. Trends Mol Med. 2004;10(5):201–4. doi:10.1016/j.molmed.2004.03.001.

    Article  PubMed  CAS  Google Scholar 

  28. Okamura D, Ohtsuka M, Kimura F, Shimizu H, Yoshidome H, Kato A, Miyazaki M. Ezrin expression is associated with hepatocellular carcinoma possibly derived from progenitor cells and early recurrence after surgical resection. Mod Pathol. 2008;21(7):847–55. doi:10.1038/modpathol.2008.59.

    Article  PubMed  CAS  Google Scholar 

  29. Dewan MZ, Ahmed S, Iwasaki Y, Ohba K, Toi M, Yamamoto N. Stromal cell-derived factor-1 and CXCR4 receptor interaction in tumor growth and metastasis of breast cancer. Biomed Pharmacother. 2006;60(6):273–6. doi:10.1016/j.biopha.2006.06.004.

    Article  PubMed  CAS  Google Scholar 

  30. Kucia M, Jankowski K, Reca R, Wysoczynski M, Bandura L, Allendorf DJ, Zhang J, Ratajczak J, Ratajczak MZ. CXCR4–SDF-1 signalling, locomotion, chemotaxis and adhesion. J Mol Histol. 2004;35(3):233–45.

    Article  PubMed  CAS  Google Scholar 

  31. Kang Y, Massague J. Epithelial–mesenchymal transitions: twist in development and metastasis. Cell. 2004;118(3):277–9. doi:10.1016/j.cell.2004.07.011.

    Article  PubMed  CAS  Google Scholar 

  32. Huang KT, Dobrovic A, Yan M, Karim RZ, Lee CS, Lakhani SR, Fox SB. DNA methylation profiling of phyllodes and fibroadenoma tumours of the breast. Breast Cancer Res Treat. 2010;124(2):555–65. doi:10.1007/s10549-010-0970-4.

    Article  PubMed  CAS  Google Scholar 

  33. Kim JH, Choi YD, Lee JS, Lee JH, Nam JH, Choi C, Park MH, Yoon JH. Borderline and malignant phyllodes tumors display similar promoter methylation profiles. Virchows Arch. 2009;455(6):469–75. doi:10.1007/s00428-009-0858-z.

    Article  PubMed  CAS  Google Scholar 

  34. Gort EH, Suijkerbuijk KP, Roothaan SM, Raman V, Vooijs M, van der Wall E, van Diest PJ. Methylation of the TWIST1 promoter, TWIST1 mRNA levels, and immunohistochemical expression of TWIST1 in breast cancer. Cancer Epidemiol Biomarkers Prev. 2008;17(12):3325–30. doi:10.1158/1055-9965.epi-08-0472.

    Article  PubMed  CAS  Google Scholar 

  35. Gomez I, Pena C, Herrera M, Munoz C, Larriba MJ, Garcia V, Dominguez G, Silva J, Rodriguez R, Garcia de Herreros A, Bonilla F, Garcia JM. TWIST1 is expressed in colorectal carcinomas and predicts patient survival. PLoS One. 2011;6(3):e18023. doi:10.1371/journal.pone.0018023.

    Article  PubMed  CAS  Google Scholar 

  36. Lee TK, Poon RT, Yuen AP, Ling MT, Kwok WK, Wang XH, Wong YC, Guan XY, Man K, Chau KL, Fan ST. Twist overexpression correlates with hepatocellular carcinoma metastasis through induction of epithelial–mesenchymal transition. Clin Cancer Res. 2006;12(18):5369–76. doi:10.1158/1078-0432.ccr-05-2722.

    Article  PubMed  CAS  Google Scholar 

  37. Sasaki K, Natsugoe S, Ishigami S, Matsumoto M, Okumura H, Setoyama T, Uchikado Y, Kita Y, Tamotsu K, Sakamoto A, Owaki T, Aikou T. Significance of Twist expression and its association with E-cadherin in esophageal squamous cell carcinoma. J Exp Clin Cancer Res. 2009;28:158. doi:10.1186/1756-9966-28-158.

    Article  PubMed  Google Scholar 

  38. Shibata K, Kajiyama H, Ino K, Terauchi M, Yamamoto E, Nawa A, Nomura S, Kikkawa F. Twist expression in patients with cervical cancer is associated with poor disease outcome. Ann Oncol. 2008;19(1):81–5. doi:10.1093/annonc/mdm344.

    Article  PubMed  CAS  Google Scholar 

  39. Valdes-Mora F, Gomez del Pulgar T, Bandres E, Cejas P, Ramirez de Molina A, Perez-Palacios R, Gallego-Ortega D, Garcia-Cabezas MA, Casado E, Larrauri J, Nistal M, Gonzalez-Baron M, Garcia-Foncillas J, Lacal JC. TWIST1 overexpression is associated with nodal invasion and male sex in primary colorectal cancer. Ann Surg Oncol. 2009;16(1):78–87. doi:10.1245/s10434-008-0166-x.

    Article  PubMed  Google Scholar 

  40. Yu Q, Zhang K, Wang X, Liu X, Zhang Z. Expression of transcription factors snail, slug, and twist in human bladder carcinoma. J Exp Clin Cancer Res. 2010;29:119. doi:10.1186/1756-9966-29-119.

    Article  PubMed  CAS  Google Scholar 

  41. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, Savagner P, Gitelman I, Richardson A, Weinberg RA. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell. 2004;117(7):927–39. doi:10.1016/j.cell.2004.06.006.

    Article  PubMed  CAS  Google Scholar 

  42. Tarin D, Thompson EW, Newgreen DF. The fallacy of epithelial mesenchymal transition in neoplasia. Cancer Res. 2005;65(14):5996–6000. doi:10.1158/0008-5472.can-05-0699. discussion 6000-5991.

    Article  PubMed  CAS  Google Scholar 

  43. Thompson EW, Newgreen DF, Tarin D. Carcinoma invasion and metastasis: a role for epithelial–mesenchymal transition? Cancer Res. 2005;65(14):5991–5. doi:10.1158/0008-5472.can-05-0616. discussion 5995.

    Article  PubMed  CAS  Google Scholar 

  44. Maestro R, Dei Tos AP, Hamamori Y, Krasnokutsky S, Sartorelli V, Kedes L, Doglioni C, Beach DH, Hannon GJ. Twist is a potential oncogene that inhibits apoptosis. Genes Dev. 1999;13(17):2207–17.

    Article  PubMed  CAS  Google Scholar 

  45. Valsesia-Wittmann S, Magdeleine M, Dupasquier S, Garin E, Jallas AC, Combaret V, Krause A, Leissner P, Puisieux A. Oncogenic cooperation between H-Twist and N-Myc overrides failsafe programs in cancer cells. Cancer Cell. 2004;6(6):625–30. doi:10.1016/j.ccr.2004.09.033.

    Article  PubMed  CAS  Google Scholar 

  46. Yang Z, Zhang X, Gang H, Li X, Li Z, Wang T, Han J, Luo T, Wen F, Wu X. Up-regulation of gastric cancer cell invasion by Twist is accompanied by N-cadherin and fibronectin expression. Biochem Biophys Res Commun. 2007;358(3):925–30. doi:10.1016/j.bbrc.2007.05.023.

    Article  PubMed  CAS  Google Scholar 

  47. Karim RZ, Gerega SK, Yang YH, Horvath L, Spillane A, Carmalt H, Scolyer RA, Lee CS. Proteins from the Wnt pathway are involved in the pathogenesis and progression of mammary phyllodes tumours. J Clin Pathol. 2009;62(11):1016–20. doi:10.1136/jcp.2009.066977.

    Article  PubMed  CAS  Google Scholar 

  48. Bertran E, Caja L, Navarro E, Sancho P, Mainez J, Murillo MM, Vinyals A, Fabra A, Fabregat I. Role of CXCR4/SDF-1 alpha in the migratory phenotype of hepatoma cells that have undergone epithelial–mesenchymal transition in response to the transforming growth factor-beta. Cell Signal. 2009;21(11):1595–606. doi:10.1016/j.cellsig.2009.06.006.

    Article  PubMed  CAS  Google Scholar 

  49. Onoue T, Uchida D, Begum NM, Tomizuka Y, Yoshida H, Sato M. Epithelial–mesenchymal transition induced by the stromal cell-derived factor-1/CXCR4 system in oral squamous cell carcinoma cells. Int J Oncol. 2006;29(5):1133–8.

    PubMed  CAS  Google Scholar 

  50. Taki M, Higashikawa K, Yoneda S, Ono S, Shigeishi H, Nagayama M, Kamata N. Up-regulation of stromal cell-derived factor-1alpha and its receptor CXCR4 expression accompanied with epithelial–mesenchymal transition in human oral squamous cell carcinoma. Oncol Rep. 2008;19(4):993–8.

    PubMed  CAS  Google Scholar 

  51. Wang X, Liu X, Li AY, Chen L, Lai L, Lin HH, Hu S, Yao L, Peng J, Loera S, Xue L, Zhou B, Zhou L, Zheng S, Chu P, Zhang S, Ann DK, Yen Y. Overexpression of HMGA2 promotes metastasis and impacts survival of colorectal cancers. Clin Cancer Res. 2011;17(8):2570–80. doi:10.1158/1078-0432.ccr-10-2542.

    Article  PubMed  CAS  Google Scholar 

  52. Muller A, Homey B, Soto H, Ge N, Catron D, Buchanan ME, McClanahan T, Murphy E, Yuan W, Wagner SN, Barrera JL, Mohar A, Verastegui E, Zlotnik A. Involvement of chemokine receptors in breast cancer metastasis. Nature. 2001;410(6824):50–6. doi:10.1038/35065016.

    Article  PubMed  CAS  Google Scholar 

  53. Murakami T, Maki W, Cardones AR, Fang H, Tun Kyi A, Nestle FO, Hwang ST. Expression of CXC chemokine receptor-4 enhances the pulmonary metastatic potential of murine B16 melanoma cells. Cancer Res. 2002;62(24):7328–34.

    PubMed  CAS  Google Scholar 

  54. Smith MC, Luker KE, Garbow JR, Prior JL, Jackson E, Piwnica-Worms D, Luker GD. CXCR4 regulates growth of both primary and metastatic breast cancer. Cancer Res. 2004;64(23):8604–12. doi:10.1158/0008-5472.can-04-1844.

    Article  PubMed  CAS  Google Scholar 

  55. Taichman RS, Cooper C, Keller ET, Pienta KJ, Taichman NS, McCauley LK. Use of the stromal cell-derived factor-1/CXCR4 pathway in prostate cancer metastasis to bone. Cancer Res. 2002;62(6):1832–7.

    PubMed  CAS  Google Scholar 

  56. Burger JA, Stewart DJ. CXCR4 chemokine receptor antagonists: perspectives in SCLC. Expert Opin Investig Drugs. 2009;18(4):481–90. doi:10.1517/13543780902804249.

    Article  PubMed  CAS  Google Scholar 

  57. Chu QD, Panu L, Holm NT, Li BD, Johnson LW, Zhang S. High chemokine receptor CXCR4 level in triple negative breast cancer specimens predicts poor clinical outcome. J Surg Res. 2010;159(2):689–95. doi:10.1016/j.jss.2008.09.020.

    Article  PubMed  CAS  Google Scholar 

  58. Darash-Yahana M, Pikarsky E, Abramovitch R, Zeira E, Pal B, Karplus R, Beider K, Avniel S, Kasem S, Galun E, Peled A. Role of high expression levels of CXCR4 in tumor growth, vascularization, and metastasis. FASEB J. 2004;18(11):1240–2. doi:10.1096/fj.03-0935fje.

    PubMed  CAS  Google Scholar 

  59. Meier R, Muhlethaler-Mottet A, Flahaut M, Coulon A, Fusco C, Louache F, Auderset K, Bourloud KB, Daudigeos E, Ruegg C, Vassal G, Gross N, Joseph JM. The chemokine receptor CXCR4 strongly promotes neuroblastoma primary tumour and metastatic growth, but not invasion. PLoS One. 2007;2(10):e1016. doi:10.1371/journal.pone.0001016.

    Article  PubMed  Google Scholar 

  60. Murakami T, Cardones AR, Hwang ST. Chemokine receptors and melanoma metastasis. J Dermatol Sci. 2004;36(2):71–8. doi:10.1016/j.jdermsci.2004.03.002.

    Article  PubMed  CAS  Google Scholar 

  61. Schimanski CC, Schwald S, Simiantonaki N, Jayasinghe C, Gonner U, Wilsberg V, Junginger T, Berger MR, Galle PR, Moehler M. Effect of chemokine receptors CXCR4 and CCR7 on the metastatic behavior of human colorectal cancer. Clin Cancer Res. 2005;11(5):1743–50. doi:10.1158/1078-0432.ccr-04-1195.

    Article  PubMed  CAS  Google Scholar 

  62. Laverdiere C, Hoang BH, Yang R, Sowers R, Qin J, Meyers PA, Huvos AG, Healey JH, Gorlick R. Messenger RNA expression levels of CXCR4 correlate with metastatic behavior and outcome in patients with osteosarcoma. Clin Cancer Res. 2005;11(7):2561–7. doi:10.1158/1078-0432.ccr-04-1089.

    Article  PubMed  CAS  Google Scholar 

  63. Diomedi-Camassei F, McDowell HP, De Ioris MA, Uccini S, Altavista P, Raschella G, Vitali R, Mannarino O, De Sio L, Cozzi DA, Donfrancesco A, Inserra A, Callea F, Dominici C. Clinical significance of CXC chemokine receptor-4 and c-Met in childhood rhabdomyosarcoma. Clin Cancer Res. 2008;14(13):4119–27. doi:10.1158/1078-0432.ccr-07-4446.

    Article  PubMed  CAS  Google Scholar 

  64. Libura J, Drukala J, Majka M, Tomescu O, Navenot JM, Kucia M, Marquez L, Peiper SC, Barr FG, Janowska-Wieczorek A, Ratajczak MZ. CXCR4–SDF-1 signaling is active in rhabdomyosarcoma cells and regulates locomotion, chemotaxis, and adhesion. Blood. 2002;100(7):2597–606. doi:10.1182/blood-2002-01-0031.

    Article  PubMed  CAS  Google Scholar 

  65. Strahm B, Durbin AD, Sexsmith E, Malkin D. The CXCR4–SDF1alpha axis is a critical mediator of rhabdomyosarcoma metastatic signaling induced by bone marrow stroma. Clin Exp Metastasis. 2008;25(1):1–10. doi:10.1007/s10585-007-9094-6.

    Article  PubMed  CAS  Google Scholar 

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This work was supported by a Yonsei University Research Fund of 2011.

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  1. Department of Pathology, Inje University Sanggye Paik Hospital, Seoul, South Korea

    Ji Eun Kwon

  2. Brain Korea 21 Project for Medical Sciences, Yonsei University College of Medicine, Seoul, South Korea

    Ji Eun Kwon

  3. Department of Pathology, Yonsei University College of Medicine, Severance Hospital, 250 Seongsanno, Seodaemun-gu, Seoul, South Korea

    Woo-Hee Jung & Ja Seung Koo

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Kwon, J.E., Jung, WH. & Koo, J.S. Molecules involved in epithelial–mesenchymal transition and epithelial–stromal interaction in phyllodes tumors: implications for histologic grade and prognosis. Tumor Biol. 33, 787–798 (2012). https://doi.org/10.1007/s13277-011-0296-9

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