Skip to main content
Erschienen in: Journal of Cancer Research and Clinical Oncology 4/2018

23.01.2018 | Original Article – Cancer Research

Proliferation-associated miRNAs-494, -205, -21 and -126 detected by in situ hybridization: expression and prognostic potential in breast carcinoma patients

verfasst von: Natalia Gurvits, Tuomo-Artturi Autere, Heli Repo, Marjukka Nykänen, Teijo Kuopio, Pauliina Kronqvist, Kati Talvinen

Erschienen in: Journal of Cancer Research and Clinical Oncology | Ausgabe 4/2018

Einloggen, um Zugang zu erhalten

Abstract

Purpose

To visualize by in situ hybridization (ISH) the levels of a set of proliferation-associated miRNAs and to evaluate their impact and clinical applicability in prognostication of invasive breast carcinoma.

Methods

Tissue specimen from breast carcinoma patients were investigated for miRNAs-494, -205, -21 and -126. Prognostic associations for levels of miRNAs were analyzed based on complete clinical data and up to 22.5-year follow-up of the patient material (n = 285). For detection of the miRNAs, an automated sensitive protocol applying in situ hybridization was developed.

Results

MiRNA-494 indicated prognostic value for patients with invasive breast carcinoma. Among node-negative disease reduced level of miRNA-494 predicted 8.5-fold risk of breast cancer death (p = 0.04). Altered levels and expression patterns of the studied miRNAs were observed in breast carcinomas as compared to benign breast tissue.

Conclusions

The present paper reports for the first time on the prognostic value of miRNA-494 in invasive breast cancer. Particularly, detection of miRNA-494 could benefit patients with node-negative breast cancer in identifying subgroups with aggressive disease. Based on our experience, the developed automatic ISH method to visualize altered levels of miRNAs-494, -205, -21 and -126 could be applied to routine pathology diagnostics providing that conditions of tissue treatment, especially fixation delays, are managed.
Literatur
Zurück zum Zitat Carleton M, Cleary MA, Linsley PS (2007) MicroRNAs and cell cycle regulation. Cell Cycle 6:2127–2132CrossRefPubMed Carleton M, Cleary MA, Linsley PS (2007) MicroRNAs and cell cycle regulation. Cell Cycle 6:2127–2132CrossRefPubMed
Zurück zum Zitat Chatterjee N, Rana S, Espinosa-Diez C, Anand S (2017) MicroRNAs in cancer: challenges and opportunities in early detection, disease monitoring, and therapeutic agents. Curr Pathobiol Rep 5:35–42CrossRefPubMedPubMedCentral Chatterjee N, Rana S, Espinosa-Diez C, Anand S (2017) MicroRNAs in cancer: challenges and opportunities in early detection, disease monitoring, and therapeutic agents. Curr Pathobiol Rep 5:35–42CrossRefPubMedPubMedCentral
Zurück zum Zitat Childs G, Fazzari M, Kung G et al (2009) Low-level expression of microRNAs let-7d and miR-205 are prognostic markers of head and neck squamous cell carcinoma. Am J Pathol 174:736–745CrossRefPubMedPubMedCentral Childs G, Fazzari M, Kung G et al (2009) Low-level expression of microRNAs let-7d and miR-205 are prognostic markers of head and neck squamous cell carcinoma. Am J Pathol 174:736–745CrossRefPubMedPubMedCentral
Zurück zum Zitat Duffy MJ, Walsh S, McDermott EW, Crown J (2015) Biomarkers in breast cancer: where are we and where are we going? Adv Clin Chem 71:1–23CrossRefPubMed Duffy MJ, Walsh S, McDermott EW, Crown J (2015) Biomarkers in breast cancer: where are we and where are we going? Adv Clin Chem 71:1–23CrossRefPubMed
Zurück zum Zitat Ebrahimi F, Gopalan V, Smith RA, Lam AK (2014) miR-126 in human cancers: clinical roles and current perspectives. Exp Mol Pathol 96:98–107CrossRefPubMed Ebrahimi F, Gopalan V, Smith RA, Lam AK (2014) miR-126 in human cancers: clinical roles and current perspectives. Exp Mol Pathol 96:98–107CrossRefPubMed
Zurück zum Zitat Goldhirsch A, Ingle JN, Gelber RD et al (2009) Thresholds for therapies: highlights of the St Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer. Ann Oncol 20:1319–1329CrossRefPubMedPubMedCentral Goldhirsch A, Ingle JN, Gelber RD et al (2009) Thresholds for therapies: highlights of the St Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer. Ann Oncol 20:1319–1329CrossRefPubMedPubMedCentral
Zurück zum Zitat Goldhirsch A, Wood WC, Coates AS et al (2011) Strategies for subtypes—dealing with the diversity of breast cancer: highlights of the St Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer. Ann Oncol 22:1736–1747CrossRefPubMedPubMedCentral Goldhirsch A, Wood WC, Coates AS et al (2011) Strategies for subtypes—dealing with the diversity of breast cancer: highlights of the St Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer. Ann Oncol 22:1736–1747CrossRefPubMedPubMedCentral
Zurück zum Zitat Greene SB, Herschkowitz JI, Rosen JM (2010) The ups and downs of miR-205: identifying the roles of miR-205 in mammary gland development and breast cancer. RNA Biol 7:300–304CrossRefPubMedPubMedCentral Greene SB, Herschkowitz JI, Rosen JM (2010) The ups and downs of miR-205: identifying the roles of miR-205 in mammary gland development and breast cancer. RNA Biol 7:300–304CrossRefPubMedPubMedCentral
Zurück zum Zitat Gurvits N, Repo H, Löyttyniemi E, Nykänen M, Anttinen J, Kuopio T, Talvinen K, Kronqvist P (2016) Prognostic implications of securin expression and sub-cellular localization in human breast cancer. Cell Oncol (Dordr) 39:319–331CrossRef Gurvits N, Repo H, Löyttyniemi E, Nykänen M, Anttinen J, Kuopio T, Talvinen K, Kronqvist P (2016) Prognostic implications of securin expression and sub-cellular localization in human breast cancer. Cell Oncol (Dordr) 39:319–331CrossRef
Zurück zum Zitat Haga CL, Phinney DG (2012) MicroRNAs in the imprinted DLK1-DIO3 region repress the epithelial-to-mesenchymal transition by targeting the TWIST1 protein signaling network. J Biol Chem 287:42695–42707CrossRefPubMedPubMedCentral Haga CL, Phinney DG (2012) MicroRNAs in the imprinted DLK1-DIO3 region repress the epithelial-to-mesenchymal transition by targeting the TWIST1 protein signaling network. J Biol Chem 287:42695–42707CrossRefPubMedPubMedCentral
Zurück zum Zitat Hagman Z, Haflidadóttir BS, Ceder JA et al (2013) miR-205 negatively regulates the androgen receptor and is associated with adverse outcome of prostate cancer patients. Br J Cancer 108:1668–1676CrossRefPubMedPubMedCentral Hagman Z, Haflidadóttir BS, Ceder JA et al (2013) miR-205 negatively regulates the androgen receptor and is associated with adverse outcome of prostate cancer patients. Br J Cancer 108:1668–1676CrossRefPubMedPubMedCentral
Zurück zum Zitat Hanna JA, Hahn L, Agarwal S et al (2012) In situ measurement of miR-205 in malignant melanoma tissue supports its role as a tumor suppressor microRNA. Lab Investig 92:1390–1397CrossRefPubMedPubMedCentral Hanna JA, Hahn L, Agarwal S et al (2012) In situ measurement of miR-205 in malignant melanoma tissue supports its role as a tumor suppressor microRNA. Lab Investig 92:1390–1397CrossRefPubMedPubMedCentral
Zurück zum Zitat He W, Li Y, Chen X, Lu L, Tang B, Wang Z, Pan Y, Cai S, He Y, Ke Z (2014) miR-494 acts as an anti-oncogene in gastric carcinoma by targeting c-myc. J Gastroenterol Hepatol 29:1427–1434CrossRefPubMed He W, Li Y, Chen X, Lu L, Tang B, Wang Z, Pan Y, Cai S, He Y, Ke Z (2014) miR-494 acts as an anti-oncogene in gastric carcinoma by targeting c-myc. J Gastroenterol Hepatol 29:1427–1434CrossRefPubMed
Zurück zum Zitat Healey MA, Hirko KA, Beck AH, Collins LC, Schnitt SJ, Eliassen AH, Holmes MD, Tamimi RM, Hazra A (2017) Assessment of Ki67 expression for breast cancer subtype classification and prognosis in the Nurses’ Health Study. Breast Cancer Res Treat 166:613–622CrossRefPubMed Healey MA, Hirko KA, Beck AH, Collins LC, Schnitt SJ, Eliassen AH, Holmes MD, Tamimi RM, Hazra A (2017) Assessment of Ki67 expression for breast cancer subtype classification and prognosis in the Nurses’ Health Study. Breast Cancer Res Treat 166:613–622CrossRefPubMed
Zurück zum Zitat Hou SX, Ding BJ, Li HZ et al (2013) Identification of microRNA-205 as a potential prognostic indicator for human glioma. J Clin Neurosci 20:933–937CrossRefPubMed Hou SX, Ding BJ, Li HZ et al (2013) Identification of microRNA-205 as a potential prognostic indicator for human glioma. J Clin Neurosci 20:933–937CrossRefPubMed
Zurück zum Zitat Hug KA, Anthony L, Eldeiry D, Benson J, Wheeler E, Mousa S, Shi B (2015) Expression and tissue distribution of MicroRNA-21 in malignant and benign breast tissues. Anticancer Res 35:3175–3183PubMed Hug KA, Anthony L, Eldeiry D, Benson J, Wheeler E, Mousa S, Shi B (2015) Expression and tissue distribution of MicroRNA-21 in malignant and benign breast tissues. Anticancer Res 35:3175–3183PubMed
Zurück zum Zitat Hulf T, Sibbritt T, Wiklund ED et al (2013) Epigenetic-induced repression of microRNA-205 is associated with MED1 activation and a poorer prognosis in localized prostate cancer. Oncogene 32:2891–2899CrossRefPubMed Hulf T, Sibbritt T, Wiklund ED et al (2013) Epigenetic-induced repression of microRNA-205 is associated with MED1 activation and a poorer prognosis in localized prostate cancer. Oncogene 32:2891–2899CrossRefPubMed
Zurück zum Zitat Huo L, Wang Y, Gong Y, Krishnamurthy S, Wang J, Diao L, Liu CG, Liu X, Lin F, Symmans WF, Wei W, Zhang X, Sun L, Alvarez RH, Ueno NT, Fouad TM, Harano K, Debeb BG, Wu Y, Reuben J, Cristofanilli M, Zuo Z (2016) MicroRNA expression profiling identifies decreased expression of miR-205 in inflammatory breast cancer. ModPathol 29:330–346 Huo L, Wang Y, Gong Y, Krishnamurthy S, Wang J, Diao L, Liu CG, Liu X, Lin F, Symmans WF, Wei W, Zhang X, Sun L, Alvarez RH, Ueno NT, Fouad TM, Harano K, Debeb BG, Wu Y, Reuben J, Cristofanilli M, Zuo Z (2016) MicroRNA expression profiling identifies decreased expression of miR-205 in inflammatory breast cancer. ModPathol 29:330–346
Zurück zum Zitat Jørgensen S, Baker A, Møller S, Nielsen BS (2010) Robust one-day in situ hybridization protocol for detection of microRNAs in paraffin samples using LNA probes. Methods 52:375–381CrossRefPubMed Jørgensen S, Baker A, Møller S, Nielsen BS (2010) Robust one-day in situ hybridization protocol for detection of microRNAs in paraffin samples using LNA probes. Methods 52:375–381CrossRefPubMed
Zurück zum Zitat Kaboli PJ, Rahmat A, Ismail P, Ling KH (2015) MicroRNA-based therapy and breast cancer: a comprehensive review of novel therapeutic strategies from diagnosis to treatment. Pharmacol Res 97:104–121CrossRefPubMed Kaboli PJ, Rahmat A, Ismail P, Ling KH (2015) MicroRNA-based therapy and breast cancer: a comprehensive review of novel therapeutic strategies from diagnosis to treatment. Pharmacol Res 97:104–121CrossRefPubMed
Zurück zum Zitat Kalogirou C, Spahn M, Krebs M, Joniau S, Lerut E, Burger M, Scholz CJ, Kneitz S, Riedmiller H, Kneitz B (2013) MiR-205 is progressively down-regulated in lymph node metastasis but fails as a prognostic biomarker in high-risk prostate cancer. Int J Mol Sci 14:21414–21434CrossRefPubMedPubMedCentral Kalogirou C, Spahn M, Krebs M, Joniau S, Lerut E, Burger M, Scholz CJ, Kneitz S, Riedmiller H, Kneitz B (2013) MiR-205 is progressively down-regulated in lymph node metastasis but fails as a prognostic biomarker in high-risk prostate cancer. Int J Mol Sci 14:21414–21434CrossRefPubMedPubMedCentral
Zurück zum Zitat Kapanidou M, Curtis NL, Bolanos-Garcia VM (2017) Cdc20: at the crossroads between chromosome segregation and mitotic exit. Trends Biochem Sci 42:193–205CrossRefPubMed Kapanidou M, Curtis NL, Bolanos-Garcia VM (2017) Cdc20: at the crossroads between chromosome segregation and mitotic exit. Trends Biochem Sci 42:193–205CrossRefPubMed
Zurück zum Zitat Karaayvaz M, Zhang C, Liang S et al (2013) Prognostic significance of miR-205 in endometrial cancer. PLoS One 7:e35158CrossRef Karaayvaz M, Zhang C, Liang S et al (2013) Prognostic significance of miR-205 in endometrial cancer. PLoS One 7:e35158CrossRef
Zurück zum Zitat Karra H, Pitkänen R, Nykänen M, Talvinen K, Kuopio T, Söderström M, Kronqvist P (2012) Securin predicts aneuploidy and survival in breast cancer. Histopathology 60:586–596CrossRefPubMed Karra H, Pitkänen R, Nykänen M, Talvinen K, Kuopio T, Söderström M, Kronqvist P (2012) Securin predicts aneuploidy and survival in breast cancer. Histopathology 60:586–596CrossRefPubMed
Zurück zum Zitat Karra H, Repo H, Ahonen I, Löyttyniemi E, Pitkänen R, Lintunen M, Kuopio T, Söderström M, Kronqvist P (2014) Cdc20 and securin overexpression predict short-term breast cancer survival. Br J Cancer 110:2905–2913CrossRefPubMedPubMedCentral Karra H, Repo H, Ahonen I, Löyttyniemi E, Pitkänen R, Lintunen M, Kuopio T, Söderström M, Kronqvist P (2014) Cdc20 and securin overexpression predict short-term breast cancer survival. Br J Cancer 110:2905–2913CrossRefPubMedPubMedCentral
Zurück zum Zitat Kim WK, Park M, Kim YK, Tae YK, Yang HK, Lee JM, Kim H (2011) MicroRNA-494 downregulates KIT and inhibits gastrointestinal stromal tumor cell proliferation. Clin Cancer Res 17:7584–7594CrossRefPubMed Kim WK, Park M, Kim YK, Tae YK, Yang HK, Lee JM, Kim H (2011) MicroRNA-494 downregulates KIT and inhibits gastrointestinal stromal tumor cell proliferation. Clin Cancer Res 17:7584–7594CrossRefPubMed
Zurück zum Zitat Lim L, Balakrishnan A, Huskey N, Jones KD, Jodari M, Ng R, Song G, Riordan J, Anderton B, Cheung ST, Willenbring H, Dupuy A, Chen X, Brown D, Chang AN, Goga A (2014) MicroRNA-494 within an oncogenic microRNA megacluster regulates G1/S transition in liver tumorigenesis through suppression of mutated in colorectal cancer. Hepatology 59:202–215CrossRefPubMed Lim L, Balakrishnan A, Huskey N, Jones KD, Jodari M, Ng R, Song G, Riordan J, Anderton B, Cheung ST, Willenbring H, Dupuy A, Chen X, Brown D, Chang AN, Goga A (2014) MicroRNA-494 within an oncogenic microRNA megacluster regulates G1/S transition in liver tumorigenesis through suppression of mutated in colorectal cancer. Hepatology 59:202–215CrossRefPubMed
Zurück zum Zitat Liu K, Liu S, Zhang W, Jia B, Tan L, Jin Z, Liu Y (2015) miR-494 promotes cell proliferation, migration and invasion, and increased sorafenib resistance in hepatocellular carcinoma by targeting PTEN. OncolRep 34:1003–1010 Liu K, Liu S, Zhang W, Jia B, Tan L, Jin Z, Liu Y (2015) miR-494 promotes cell proliferation, migration and invasion, and increased sorafenib resistance in hepatocellular carcinoma by targeting PTEN. OncolRep 34:1003–1010
Zurück zum Zitat Ma YB, Li GX, Hu JX, Liu X, Shi BM (2015) Correlation of miR-494 expression with tumor progression and patient survival in pancreatic cancer. Genet Mol Res 14:18153–18159CrossRefPubMed Ma YB, Li GX, Hu JX, Liu X, Shi BM (2015) Correlation of miR-494 expression with tumor progression and patient survival in pancreatic cancer. Genet Mol Res 14:18153–18159CrossRefPubMed
Zurück zum Zitat MacKenzie TA, Schwartz GN, Calderone HM, Graveel CR, Winn ME, Hostetter G, Wells WA, Sempere LF (2014) Stromal expression of miR-21 identifies high-risk group in triple-negative breast cancer. Am J Pathol 184:3217–3225CrossRefPubMedPubMedCentral MacKenzie TA, Schwartz GN, Calderone HM, Graveel CR, Winn ME, Hostetter G, Wells WA, Sempere LF (2014) Stromal expression of miR-21 identifies high-risk group in triple-negative breast cancer. Am J Pathol 184:3217–3225CrossRefPubMedPubMedCentral
Zurück zum Zitat Marino AL, Evangelista AF, Vieira RA, Macedo T, Kerr LM, Abrahão-Machado LF, Longatto-Filho A, Silveira HC, Marques MM (2014) MicroRNA expression as risk biomarker of breast cancer metastasis: a pilot retrospective case-cohort study. BMC Cancer 14:739CrossRefPubMedPubMedCentral Marino AL, Evangelista AF, Vieira RA, Macedo T, Kerr LM, Abrahão-Machado LF, Longatto-Filho A, Silveira HC, Marques MM (2014) MicroRNA expression as risk biomarker of breast cancer metastasis: a pilot retrospective case-cohort study. BMC Cancer 14:739CrossRefPubMedPubMedCentral
Zurück zum Zitat Markou A, Yousef GM, Stathopoulos E et al (2014) Prognostic significance of metastasis-related microRNAs in early breast cancer patients with a long follow-up. Clin Chem 60:197–205CrossRefPubMed Markou A, Yousef GM, Stathopoulos E et al (2014) Prognostic significance of metastasis-related microRNAs in early breast cancer patients with a long follow-up. Clin Chem 60:197–205CrossRefPubMed
Zurück zum Zitat Nielsen BS, Balslev E, Poulsen TS, Nielsen D, Møller T, Mortensen CE, Holmstrøm K, Høgdall E (2014) miR-21 expression in cancer cells may not predict resistance to adjuvant trastuzumab in primary breast cancer. Front Oncol 4:207CrossRefPubMedPubMedCentral Nielsen BS, Balslev E, Poulsen TS, Nielsen D, Møller T, Mortensen CE, Holmstrøm K, Høgdall E (2014) miR-21 expression in cancer cells may not predict resistance to adjuvant trastuzumab in primary breast cancer. Front Oncol 4:207CrossRefPubMedPubMedCentral
Zurück zum Zitat Piovan C, Palmieri D, Di Leva G, Braccioli L, Casalini P, Nuovo G, Tortoreto M, Sasso M, Plantamura I, Triulzi T, Taccioli C, Tagliabue E, Iorio MV, Croce CM (2012) Oncosuppressive role of p53-induced miR-205 in triple negative breast cancer. Mol Oncol 6:458–472CrossRefPubMedPubMedCentral Piovan C, Palmieri D, Di Leva G, Braccioli L, Casalini P, Nuovo G, Tortoreto M, Sasso M, Plantamura I, Triulzi T, Taccioli C, Tagliabue E, Iorio MV, Croce CM (2012) Oncosuppressive role of p53-induced miR-205 in triple negative breast cancer. Mol Oncol 6:458–472CrossRefPubMedPubMedCentral
Zurück zum Zitat Qi L, Bart J, Tan LP, Platteel I, Sluis T, Huitema S, Harms G, Fu L, Hollema H, Berg A (2009) Expression of miR-21 and its targets (PTEN, PDCD4, TM1) in flat epithelial atypia of the breast in relation to ductal carcinoma in situ and invasive carcinoma. BMC Cancer 9:163-2407-9-163 Qi L, Bart J, Tan LP, Platteel I, Sluis T, Huitema S, Harms G, Fu L, Hollema H, Berg A (2009) Expression of miR-21 and its targets (PTEN, PDCD4, TM1) in flat epithelial atypia of the breast in relation to ductal carcinoma in situ and invasive carcinoma. BMC Cancer 9:163-2407-9-163
Zurück zum Zitat Quesne JL, Jones J, Warren J, Dawson SJ, Ali HR, Bardwell H, Blows F, Pharoah P, Caldas C (2012) Biological and prognostic associations of miR-205 and let-7b in breast cancer revealed by in situ hybridization analysis of micro-RNA expression in arrays of archival tumour. J Pathol 227:306–314CrossRefPubMed Quesne JL, Jones J, Warren J, Dawson SJ, Ali HR, Bardwell H, Blows F, Pharoah P, Caldas C (2012) Biological and prognostic associations of miR-205 and let-7b in breast cancer revealed by in situ hybridization analysis of micro-RNA expression in arrays of archival tumour. J Pathol 227:306–314CrossRefPubMed
Zurück zum Zitat R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Zurück zum Zitat Rask L, Balslev E, Jorgensen S, Eriksen J, Flyger H, Moller S, Hogdall E, Litman T, Nielsen BS (2011) High expression of miR-21 in tumor stroma correlates with increased cancer cell proliferation in human breast cancer. APMIS 119:663–673CrossRefPubMed Rask L, Balslev E, Jorgensen S, Eriksen J, Flyger H, Moller S, Hogdall E, Litman T, Nielsen BS (2011) High expression of miR-21 in tumor stroma correlates with increased cancer cell proliferation in human breast cancer. APMIS 119:663–673CrossRefPubMed
Zurück zum Zitat Repo H, Gurvits N, Löyttyniemi E, Nykänen M, Lintunen M, Karra H, Kurki S, Kuopio T, Talvinen K, Söderström M, Kronqvist P (2017) PTTG1-interacting protein (PTTG1IP/PBF) predicts breast cancer survival. BMC Cancer 17:705CrossRefPubMedPubMedCentral Repo H, Gurvits N, Löyttyniemi E, Nykänen M, Lintunen M, Karra H, Kurki S, Kuopio T, Talvinen K, Söderström M, Kronqvist P (2017) PTTG1-interacting protein (PTTG1IP/PBF) predicts breast cancer survival. BMC Cancer 17:705CrossRefPubMedPubMedCentral
Zurück zum Zitat Sempere LF (2014) Fully automated fluorescence-based four-color multiplex assay for co-detection of microRNA and protein biomarkers in clinical tissue specimens. Methods Mol Biol 1211:151–170CrossRefPubMed Sempere LF (2014) Fully automated fluorescence-based four-color multiplex assay for co-detection of microRNA and protein biomarkers in clinical tissue specimens. Methods Mol Biol 1211:151–170CrossRefPubMed
Zurück zum Zitat Sempere LF, Christensen M, Silahtaroglu A, Bak M, Heath CV, Schwartz G, Wells W, Kauppinen S, Cole CN (2007) Altered MicroRNA expression confined to specific epithelial cell subpopulations in breast cancer. Cancer Res 67:11612–11620CrossRefPubMed Sempere LF, Christensen M, Silahtaroglu A, Bak M, Heath CV, Schwartz G, Wells W, Kauppinen S, Cole CN (2007) Altered MicroRNA expression confined to specific epithelial cell subpopulations in breast cancer. Cancer Res 67:11612–11620CrossRefPubMed
Zurück zum Zitat Sempere LF, Preis M, Yezefski T, Ouyang H, Suriawinata AA, Silahtaroglu A, Conejo-Garcia JR, Kauppinen S, Wells W, Korc M (2010) Fluorescence-based codetection with protein markers reveals distinct cellular compartments for altered MicroRNA expression in solid tumors. Clin Cancer Res 16:4246–4255CrossRefPubMedPubMedCentral Sempere LF, Preis M, Yezefski T, Ouyang H, Suriawinata AA, Silahtaroglu A, Conejo-Garcia JR, Kauppinen S, Wells W, Korc M (2010) Fluorescence-based codetection with protein markers reveals distinct cellular compartments for altered MicroRNA expression in solid tumors. Clin Cancer Res 16:4246–4255CrossRefPubMedPubMedCentral
Zurück zum Zitat Singh U, Keirstead N, Wolujczyk A, Odin M, Albassam M, Garrido R (2014) General principles and methods for routine automated microRNA in situ hybridization and double labeling with immunohistochemistry. Biotech Histochem 89:259–266CrossRefPubMed Singh U, Keirstead N, Wolujczyk A, Odin M, Albassam M, Garrido R (2014) General principles and methods for routine automated microRNA in situ hybridization and double labeling with immunohistochemistry. Biotech Histochem 89:259–266CrossRefPubMed
Zurück zum Zitat Song L, Liu D, Wang B, He J, Zhang S, Dai Z, Ma X, Wang X (2015) miR-494 suppresses the progression of breast cancer in vitro by targeting CXCR4 through the Wnt/β-catenin signaling pathway. Oncol Rep 34:525–531CrossRefPubMed Song L, Liu D, Wang B, He J, Zhang S, Dai Z, Ma X, Wang X (2015) miR-494 suppresses the progression of breast cancer in vitro by targeting CXCR4 through the Wnt/β-catenin signaling pathway. Oncol Rep 34:525–531CrossRefPubMed
Zurück zum Zitat Sun HB, Chen X, Ji H, Wu T, Lu HW, Zhang Y, Li H, Li YM (2014) miR 494 is an independent prognostic factor and promotes cell migration and invasion in colorectal cancer by directly targeting PTEN. Int J Oncol 45:2486–2494CrossRefPubMed Sun HB, Chen X, Ji H, Wu T, Lu HW, Zhang Y, Li H, Li YM (2014) miR 494 is an independent prognostic factor and promotes cell migration and invasion in colorectal cancer by directly targeting PTEN. Int J Oncol 45:2486–2494CrossRefPubMed
Zurück zum Zitat Talvinen K, Karra H, Hurme S, Nykänen M, Nieminen A, Anttinen J, Kuopio T, Kronqvist P (2009) Securin promotes the identification of favourable outcome in invasive breast cancer. Br J Cancer 101:1005–1010CrossRefPubMedPubMedCentral Talvinen K, Karra H, Hurme S, Nykänen M, Nieminen A, Anttinen J, Kuopio T, Kronqvist P (2009) Securin promotes the identification of favourable outcome in invasive breast cancer. Br J Cancer 101:1005–1010CrossRefPubMedPubMedCentral
Zurück zum Zitat Tavazoie SF, Alarcon C, Oskarsson T, Padua D, Wang Q, Bos PD, Gerald WL, Massague J (2008) Endogenous human microRNAs that suppress breast cancer metastasis. Nature 451:147–152CrossRefPubMedPubMedCentral Tavazoie SF, Alarcon C, Oskarsson T, Padua D, Wang Q, Bos PD, Gerald WL, Massague J (2008) Endogenous human microRNAs that suppress breast cancer metastasis. Nature 451:147–152CrossRefPubMedPubMedCentral
Zurück zum Zitat Yamanaka S, Campbell NR, An F, Kuo SC, Potter JJ, Mezey E, Maitra A, Selaru FM (2012) Coordinated effects of microRNA-494 induce G(2)/M arrest in human cholangiocarcinoma. CellCycle 11:2729–2738 Yamanaka S, Campbell NR, An F, Kuo SC, Potter JJ, Mezey E, Maitra A, Selaru FM (2012) Coordinated effects of microRNA-494 induce G(2)/M arrest in human cholangiocarcinoma. CellCycle 11:2729–2738
Zurück zum Zitat Yang YK, Xi WY, Xi RX, Li JY, Li Q, Gao YE (2015) MicroRNA-494 promotes cervical cancer proliferation through the regulation of PTEN. OncolRep 33:2393–2401 Yang YK, Xi WY, Xi RX, Li JY, Li Q, Gao YE (2015) MicroRNA-494 promotes cervical cancer proliferation through the regulation of PTEN. OncolRep 33:2393–2401
Zurück zum Zitat Yang A, Wang X, Yu C, Jin Z, Wei L, Cao J, Wang Q, Zhang M, Zhang L, Zhang L, Hao C (2017) microRNA-494 is a potential prognostic marker and inhibits cellular proliferation, migration and invasion by targeting SIRT1 in epithelial ovarian cancer. Oncol Lett 3177–3184 Yang A, Wang X, Yu C, Jin Z, Wei L, Cao J, Wang Q, Zhang M, Zhang L, Zhang L, Hao C (2017) microRNA-494 is a potential prognostic marker and inhibits cellular proliferation, migration and invasion by targeting SIRT1 in epithelial ovarian cancer. Oncol Lett 3177–3184
Zurück zum Zitat Yerushalmi R, Woods R, Ravdin PM, Hayes MM, Gelmon KA (2010) Ki67 in breast cancer: prognostic and predictive potential. Lancet Oncol 11:174–183CrossRefPubMed Yerushalmi R, Woods R, Ravdin PM, Hayes MM, Gelmon KA (2010) Ki67 in breast cancer: prognostic and predictive potential. Lancet Oncol 11:174–183CrossRefPubMed
Zurück zum Zitat Zhang J, Du YY, Lin YF, Chen YT, Yang L, Wang HJ, Ma D (2008) The cell growth suppressor, mir-126, targets IRS-1. Biochem Biophys Res Commun 377:136–140CrossRefPubMed Zhang J, Du YY, Lin YF, Chen YT, Yang L, Wang HJ, Ma D (2008) The cell growth suppressor, mir-126, targets IRS-1. Biochem Biophys Res Commun 377:136–140CrossRefPubMed
Zurück zum Zitat Zhang JY, Sun MY, Song NH, Deng ZL, Xue CY, Yang J (2015) Prognostic role of microRNA-205 in multiple human malignant neoplasms: a meta-analysis of 17 studies. BMJ Open 5(1):e006244CrossRefPubMedPubMedCentral Zhang JY, Sun MY, Song NH, Deng ZL, Xue CY, Yang J (2015) Prognostic role of microRNA-205 in multiple human malignant neoplasms: a meta-analysis of 17 studies. BMJ Open 5(1):e006244CrossRefPubMedPubMedCentral
Zurück zum Zitat Zhang C, Liu K, Li T, Fang J, Ding Y, Sun L, Tu T, Jiang X, Du S, Hu J, Zhu W, Chen H, Sun X (2016) miR-21: a gene of dual regulation in breast cancer. Int J Oncol 48:161–172CrossRefPubMed Zhang C, Liu K, Li T, Fang J, Ding Y, Sun L, Tu T, Jiang X, Du S, Hu J, Zhu W, Chen H, Sun X (2016) miR-21: a gene of dual regulation in breast cancer. Int J Oncol 48:161–172CrossRefPubMed
Zurück zum Zitat Zhao X, Zhou Y, Chen YU, Yu F (2016) miR-494 inhibits ovarian cancer cell proliferation and promotes apoptosis by targeting FGFR2. OncolLett 11:4245–4251 Zhao X, Zhou Y, Chen YU, Yu F (2016) miR-494 inhibits ovarian cancer cell proliferation and promotes apoptosis by targeting FGFR2. OncolLett 11:4245–4251
Metadaten
Titel
Proliferation-associated miRNAs-494, -205, -21 and -126 detected by in situ hybridization: expression and prognostic potential in breast carcinoma patients
verfasst von
Natalia Gurvits
Tuomo-Artturi Autere
Heli Repo
Marjukka Nykänen
Teijo Kuopio
Pauliina Kronqvist
Kati Talvinen
Publikationsdatum
23.01.2018
Verlag
Springer Berlin Heidelberg
Erschienen in
Journal of Cancer Research and Clinical Oncology / Ausgabe 4/2018
Print ISSN: 0171-5216
Elektronische ISSN: 1432-1335
DOI
https://doi.org/10.1007/s00432-018-2586-8

Weitere Artikel der Ausgabe 4/2018

Journal of Cancer Research and Clinical Oncology 4/2018 Zur Ausgabe

Update Onkologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.