Expression of epithelial to mesenchymal transition-related markers in lymph node metastases as a surrogate for primary tumor metastatic potential in breast cancer

Journal of Translational Medicine

Volumn 10, Issue 1, 2012, Pages

  Markiewicz, Aleksandra ^a,b   Ahrends, Tomasz ^a   Wełnicka Jaśkiewicz, Marzena ^a   Seroczyńska, Barbara ^a   Skokowski, Jarosław ^a   Jaśkiewicz, Janusz ^a   Szade, Jolanta ^a   Biernat, Wojciech ^a   Zaczek, Anna J ^a  

^a MEDICAL UNIVERSITY OF GDANSK   (Poland)

^b MEDICAL UNIVERSITY OF WARSAW   (Poland)

Author keywords

Biomarkers; Breast cancer; Epithelial mesenchymal transition; Gene expression; Immunohistochemistry; Lymph node metastasis; Primary tumor

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTROGEN RECEPTOR; MESSENGER RNA; PROGESTERONE RECEPTOR; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR TWIST; TUMOR MARKER; UVOMORULIN; VIMENTIN;

ADULT; AGED; ARTICLE; BREAST CANCER; CANCER PATIENT; CANCER STAGING; CANCER SURVIVAL; CLINICAL ARTICLE; DISEASE FREE SURVIVAL; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; GENOTYPE; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IMMUNOHISTOLOGY; LIMIT OF DETECTION; LIMIT OF QUANTITATION; LYMPH NODE METASTASIS; METASTASIS POTENTIAL; PHENOTYPE; PRIMARY TUMOR; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ANALYSIS; RNA EXTRACTION; TISSUE MICROARRAY;

ADULT; AGED; BREAST NEOPLASMS; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; LYMPHATIC METASTASIS; MIDDLE AGED; PARAFFIN EMBEDDING; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TISSUE ARRAY ANALYSIS; TUMOR MARKERS, BIOLOGICAL;

EID: 84869122494     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/1479-5876-10-226     Document Type: Article

References (57)

1. Veronesi U, Marubini E, Mariani L, Valagussa P, Zucali R. The dissection of internal mammary nodes does not improve the survival of breast cancer patients. 30-year results of a randomised trial. Eur J Cancer 1999, 35:1320-1325. 10.1016/S0959-8049(99)00133-1, 10658521.
2. Engel J, Emeny RT, Holzel D. Positive lymph nodes do not metastasize. Cancer Metastasis Rev 2012, 31:235-246. 10.1007/s10555-011-9343-7, 22198520.
3. Sleeman JP, Cady B, Pantel K. The connectivity of lymphogenous and hematogenous tumor cell dissemination: biological insights and clinical implications. Clin Exp Metastasis 2012, 29:737-746. 10.1007/s10585-012-9489-x, 22669542.
4. Jatoi I, Hilsenbeck SG, Clark GM, Osborne CK. Significance of axillary lymph node metastasis in primary breast cancer. J Clin Oncol 1999, 17:2334.
5. Sleeman JP, Christofori G, Fodde R, Collard JG, Berx G, Decraene C, Ruegg C. Concepts of metastasis in flux: the stromal progression model. Semin Cancer Biol 2012, 22:174-186. 10.1016/j.semcancer.2012.02.007, 22374376.
6. El-Haibi CP, Bell GW, Zhang J, Collmann AY, Wood D, Scherber CM, Csizmadia E, Mariani O, Zhu C, Campagne A, et al. Critical role for lysyl oxidase in mesenchymal stem cell-driven breast cancer malignancy. Proc Natl Acad Sci USA 2012, 109:17460-17465. 10.1073/pnas.1206653109, 23033492.
7. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008, 133:704-715. 10.1016/j.cell.2008.03.027, 2728032, 18485877.
8. Polyak K, Weinberg RA. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer 2009, 9:265-273. 10.1038/nrc2620, 19262571.
9. Thiery JP, Sleeman JP. Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 2006, 7:131-142. 10.1038/nrm1835, 16493418.
10. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell 2009, 139:871-890. 10.1016/j.cell.2009.11.007, 19945376.
11. Ksia{ogonek}żkiewicz M, Markiewicz A, Żaczek AJ. Epithelial-mesenchymal transition: a hallmark in metastasis formation linking circulating tumor cells and cancer stem cells. Pathobiology 2012, 79:195-208. 10.1159/000337106, 22488297.
12. van Nes J, de Kruijf E, Putter H, Faratian D, Munro A, Campbell F, Smit V, Liefers G-J, Kuppen P, van de Velde C, Bartlett J. Co-expression of SNAIL and TWIST determines prognosis in estrogen receptor-positive early breast cancer patients. Breast Cancer Res Treat 2012, 133:49-59. 10.1007/s10549-011-1684-y, 21796367.
13. Elloul S, Bukholt Elstrand M, Nesland JM, Tropé CG, Kvalheim G, Goldberg I, Reich R, Davidson B. Snail, Slug, and Smad-interacting protein 1 as novel parameters of disease aggressiveness in metastatic ovarian and breast carcinoma. Cancer 2005, 103:1631-1643. 10.1002/cncr.20946, 15742334.
14. Martin T, Goyal A, Watkins G, Jiang W. Expression of the transcription factors snail, slug, and twist and their clinical significance in human breast cancer. Ann Surg Oncol 2005, 12:488-496. 10.1245/ASO.2005.04.010, 15864483.
15. Saxena M, Stephens MA, Pathak H, Rangarajan A. Transcription factors that mediate epithelial-mesenchymal transition lead to multidrug resistance by upregulating ABC transporters. Cell Death and Dis 2011, 2:e179.
16. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003, 100:3983-3988. 10.1073/pnas.0530291100, 153034, 12629218.
17. Ding L, Ellis MJ, Li S, Larson DE, Chen K, Wallis JW, Harris CC, McLellan MD, Fulton RS, Fulton LL, et al. Genome remodelling in a basal-like breast cancer metastasis and xenograft. Nature 2010, 464:999-1005. 10.1038/nature08989, 2872544, 20393555.
18. Grunewald T, Herbst S, Heinze J, Burdach S. Understanding tumor heterogeneity as functional compartments - superorganisms revisited. J Transl Med 2011, 9:79. 10.1186/1479-5876-9-79, 3118334, 21619636.
19. De Wever O, Pauwels P, De Craene B, Sabbah M, Emami S, Redeuilh G, Gespach C, Bracke M, Berx G. Molecular and pathological signatures of epithelial-mesenchymal transitions at the cancer invasion front. Histochem Cell Biol 2008, 130:481-494. 10.1007/s00418-008-0464-1, 2522326, 18648847.
20. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, et al. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 2009, 55:611-622. 10.1373/clinchem.2008.112797, 19246619.
21. Supernat A, Markiewicz A, Welnicka-Jaskiewicz M, Seroczynska B, Skokowski J, Sejda A, Szade J, Czapiewski P, Biernat W, Zaczek A. CD73 Expression as a Potential Marker of Good Prognosis in Breast Carcinoma. Appl Immunohistochem Mol Morphol 2012, 20:103-107. 110.1097/PAI.1090b1013e3182311d3182382., 10.1097/PAI.0b013e3182311d82, 22553809.
22. Prasad C, Rath G, Mathur S, Bhatnagar D, Parshad R, Ralhan R. Expression analysis of E-cadherin, slug and GSK3beta in invasive ductal carcinoma of breast. BMC Cancer 2009, 9:325. 10.1186/1471-2407-9-325, 2753637, 19751508.
23. Kim MA, Lee HS, Lee HE, Kim JH, Yang H-K, Kim WH. Prognostic importance of epithelial-mesenchymal transition-related protein expression in gastric carcinoma. Histopathology 2009, 54:442-451. 10.1111/j.1365-2559.2009.03247.x, 19309396.
24. Montserrat N, Gallardo A, Escuin D, Catasus L, Prat J, Gutiérrez-Avignó FJ, Peiró G, Barnadas A, Lerma E. Repression of E-cadherin by SNAIL, ZEB1, and TWIST in invasive ductal carcinomas of the breast: a cooperative effort?. Hum Pathol 2011, 42:103-110. 10.1016/j.humpath.2010.05.019, 20970163.
25. Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics 1977, 33:159-174. 10.2307/2529310, 843571.
26. Altman DG, McShane LM, Sauerbrei W, Taube SE. Reporting recommendations for tumor marker prognostic studies (REMARK): explanation and elaboration. BMC Med 2012, 10:51. 10.1186/1741-7015-10-51, 3362748, 22642691.
27. Halstedt WS. The Results of radical operations for the cure of carcinoma of the breast. Ann Surg 1907, 46:1-19. 10.1097/00000658-190707000-00001, 1414404, 17862045.
28. Amir E, Miller N, Geddie W, Freedman O, Kassam F, Simmons C, Oldfield M, Dranitsaris G, Tomlinson G, Laupacis A, et al. Prospective study evaluating the impact of tissue confirmation of metastatic disease in patients with breast cancer. J Clin Oncol 2012, 30:587-592. 10.1200/JCO.2010.33.5232, 22124102.
29. Aitken SJ, Thomas JS, Langdon SP, Harrison DJ, Faratian D. Quantitative analysis of changes in ER, PR and HER2 expression in primary breast cancer and paired nodal metastases. Ann Oncol 2010, 21:1254-1261. 10.1093/annonc/mdp427, 19858088.
30. Jensen JD, Knoop A, Ewertz M, Laenkholm AV. ER, HER2, and TOP2A expression in primary tumor, synchronous axillary nodes, and asynchronous metastases in breast cancer. Breast Cancer Res Treat 2012, 132:511-521. 10.1007/s10549-011-1610-3, 21667123.
31. Falck AK, Ferno M, Bendahl PO, Ryden L. Does analysis of biomarkers in tumor cells in lymph node metastases give additional prognostic information in primary breast cancer?. World J Surg 2010, 34:1434-1441. 10.1007/s00268-010-0499-z, 20213203.
32. Niikura N, Liu J, Hayashi N, Mittendorf EA, Gong Y, Palla SL, Tokuda Y, Gonzalez-Angulo AM, Hortobagyi GN, Ueno NT. Loss of human epidermal growth factor receptor 2 (HER2) expression in metastatic sites of HER2-overexpressing primary breast tumors. J Clin Oncol 2012, 30:593-599. 10.1200/JCO.2010.33.8889, 22124109.
33. Thompson A, Jordan L, Quinlan P, Anderson E, Skene A, Dewar J, Purdie C, Group tBRiTS Prospective comparison of switches in biomarker status between primary and recurrent breast cancer: the Breast Recurrence In Tissues Study (BRITS). Breast Cancer Res 2010, 12:R92. 10.1186/bcr2771, 3046433, 21059212, Group tBRiTS.
34. Lindström LS, Karlsson E, Wilking UM, Johansson U, Hartman J, Lidbrink EK, Hatschek T, Skoog L, Bergh J. Clinically used breast cancer markers such as estrogen receptor, progesterone receptor, and human epidermal growth factor receptor 2 are unstable throughout tumor progression. J Clin Oncol 2012, 30:2601-2608. 10.1200/JCO.2011.37.2482, 22711854.
35. Liedtke C, Broglio K, Moulder S, Hsu L, Kau S-W, Symmans WF, Albarracin C, Meric-Bernstam F, Woodward W, Theriault RL, et al. Prognostic impact of discordance between triple-receptor measurements in primary and recurrent breast cancer. Ann Oncol 2009, 20:1953-1958. 10.1093/annonc/mdp263, 2791352, 19596702.
36. Macfarlane R, Seal M, Speers C, Woods R, Masoudi H, Aparicio S, Chia SK. Molecular alterations between the primary breast cancer and the subsequent locoregional/metastatic tumor. Oncologist 2012, 17:172-178. 10.1634/theoncologist.2011-0127, 22267852.
37. D'Andrea MR, Limiti MR, Bari M, Zambenedetti P, Montagutti A, Ricci F, Pappagallo GL, Sartori D, Vinante O, Mingazzini PL. Correlation between genetic and biological aspects in primary non-metastatic breast cancers and corresponding synchronous axillary lymph node metastasis. Breast Cancer Res Treat 2007, 101:279-284. 10.1007/s10549-006-9300-2, 16835704.
38. Houssami N, Macaskill P, Balleine RL, Bilous M, Pegram MD. HER2 discordance between primary breast cancer and its paired metastasis: tumor biology or test artefact? Insights through meta-analysis. Breast Cancer Res Treat 2011, 129:659-674. 10.1007/s10549-011-1632-x, 21698410.
39. Simmons C, Miller N, Geddie W, Gianfelice D, Oldfield M, Dranitsaris G, Clemons MJ. Does confirmatory tumor biopsy alter the management of breast cancer patients with distant metastases?. Ann Oncol 2009, 20:1499-1504. 10.1093/annonc/mdp028, 2731014, 19299408.
40. Dawood S, Gonzalez-Angulo AM. To biopsy or not to biopsy: is that the only question?. Oncologist 2012, 17:151-153. 10.1634/theoncologist.2011-0432, 22267854.
41. Nishimura R, Osako T, Okumura Y, Tashima R, Toyozumi Y, Arima N. Changes in the ER, PgR, HER2, p53 and Ki-67 biological markers between primary and recurrent breast cancer: discordance rates and prognosis. World J Surg Oncol 2011, 9:131. 10.1186/1477-7819-9-131, 3214885, 22004841.
42. Moody SE, Perez D, Pan T-C, Sarkisian CJ, Portocarrero CP, Sterner CJ, Notorfrancesco KL, Cardiff RD, Chodosh LA. The transcriptional repressor Snail promotes mammary tumor recurrence. Cancer Cell 2005, 8:197-209. 10.1016/j.ccr.2005.07.009, 16169465.
43. Toyama T, Zhang Z, Iwase H, Yamashita H, Ando Y, Hamaguchi M, Mizutani M, Kondo N, Fujita T, Fujii Y, Iwata H. Low expression of the snail gene is a good prognostic factor in node-negative invasive ductal carcinomas. Jpn J Clin Oncol 2006, 36:357-363. 10.1093/jjco/hyl038, 16766568.
44. Soini Y, Tuhkanen H, Sironen R, Virtanen I, Kataja V, Auvinen P, Mannermaa A, Kosma V-M. Transcription factors zeb1, twist and snai1 in breast carcinoma. BMC Cancer 2011, 11:73. 10.1186/1471-2407-11-73, 3055233, 21324165.
45. Kowalski PJ, Rubin MA, Kleer CG. E-cadherin expression in primary carcinomas of the breast and its distant metastases. Breast Cancer Res 2003, 5:R217-222. 10.1186/bcr651, 314411, 14580257.
46. Kleer CG, van Golen KL, Braun T, Merajver SD. Persistent E-cadherin expression in inflammatory breast cancer. Mod Pathol, Inc 2001, 14:458-464.
47. Kokkinos MI, Wafai R, Wong MK, Newgreen DF, Thompson EW, Waltham M. Vimentin and epithelial-mesenchymal transition in human breast cancer-observations in vitro and in vivo. Cells Tissues Organs 2007, 185:191-203. 10.1159/000101320, 17587825.
48. Gilles C, Polette M, Piette J, Delvigne AC, Thompson EW, Foidart JM, Birembaut P. Vimentin expression in cervical carcinomas: association with invasive and migratory potential. J Pathol 1996, 180:175-180. 10.1002/(SICI)1096-9896(199610)180:2<175::AID-PATH630>3.0.CO;2-G, 8976877.
49. Bonnomet A, Syne L, Brysse A, Feyereisen E, Thompson EW, Noel A, Foidart JM, Birembaut P, Polette M, Gilles C. A dynamic in vivo model of epithelial-to-mesenchymal transitions in circulating tumor cells and metastases of breast cancer. Oncogene 2012, 31:3741-3753. 10.1038/onc.2011.540, 22120722.
50. Nowell PC. The clonal evolution of tumor cell populations. Science 1976, 194:23-28. 10.1126/science.959840, 959840.
51. Greaves M, Maley CC. Clonal evolution in cancer. Nature 2012, 481:306-313. 10.1038/nature10762, 3367003, 22258609.
52. Gerlinger M, Rowan AJ, Horswell S, Larkin J, Endesfelder D, Gronroos E, Martinez P, Matthews N, Stewart A, Tarpey P, et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med 2012, 366:883-892. 10.1056/NEJMoa1113205, 22397650.
53. Shah SP, Roth A, Goya R, Oloumi A, Ha G, Zhao Y, Turashvili G, Ding J, Tse K, Haffari G, et al. The clonal and mutational evolution spectrum of primary triple-negative breast cancers. Nature 2012, 486:395-399.
54. Klein CA. Parallel progression of primary tumours and metastases. Nat Rev Cancer 2009, 9:302-312. 10.1038/nrc2627, 19308069.
55. Pusztai L, Viale G, Kelly CM, Hudis CA. Estrogen and HER-2 receptor discordance between primary breast cancer and metastasis. Oncologist 2010, 15:1164-1168. 10.1634/theoncologist.2010-0059, 3227913, 21041379.
56. Engel KB, Moore HM. Effects of preanalytical variables on the detection of proteins by immunohistochemistry in formalin-fixed, paraffin-embedded tissue. Arch Pathol Lab Med 2011, 135:537-543.
57. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2 - ΔΔCT method. Methods 2001, 25:402-408. 10.1006/meth.2001.1262, 11846609.