Skip to main content
Top
Published in: Cellular Oncology 2/2016

01-04-2016 | Original Paper

Identification of miR-139-5p as a saliva biomarker for tongue squamous cell carcinoma: a pilot study

Authors: Mehmet Bugrahan Duz, Omer Faruk Karatas, Esra Guzel, Nesrettin Fatih Turgut, Mehmet Yilmaz, Chad J. Creighton, Mustafa Ozen

Published in: Cellular Oncology | Issue 2/2016

Login to get access

Abstract

Background

Of all human oral carcinomas, 41 % are localized to the tongue. Despite considerable improvements in both diagnosis and treatment, tongue squamous cell carcinoma (TSCC) has remained one of the most lethal types of cancer. Here, we aimed at identifying a salivary microRNA (miRNA) expression signature specific for TSCC patients.

Methods

To identify putative diagnostic biomarkers, we compared the miRNA expression profiles of saliva samples from three TSCC patients and four healthy control individuals using an Agilent miRNA microarray platform (V19). Three of the differentially expressed miRNAs identified were selected for further validation using quantitative reverse-transcription PCR (qRT-PCR) in saliva samples from 25 TSCC patients and 25 healthy control individuals.

Results

Through microarray-based expression profiling, we found that 419 miRNAs were deregulated in the saliva samples from the TSCC patients compared to those from the healthy control individuals tested. Subsequent qRT-PCR analysis revealed that the expression level of miR-139-5p was significantly reduced in the TSCC validation samples compared to the controls. Further analysis of post-operative saliva samples derived from TSCC patients revealed that the miR-139-5p expression levels had turned back to normal again. In addition, we found that miR-139-5p exhibited enough power to discriminate pre-operative TSCC patients from both normal individuals (AUC: 0.805) and post-operative TSCC patients (AUC: 0.713), thereby underscoring its diagnostic potential.

Conclusions

From our results we conclude that saliva can be used as a feasible source for routine TSCC diagnostics and that miR-139-5p may serve as a potential biomarker for early TSCC detection.
Appendix
Available only for authorised users
Literature
1.
go back to reference J.N. Myers, T. Elkins, D. Roberts, R.M. Byers, Squamous cell carcinoma of the tongue in young adults: increasing incidence and factors that predict treatment outcomes. Otolaryngol. Head Neck Surg. 122, 44–51 (2000)CrossRefPubMed J.N. Myers, T. Elkins, D. Roberts, R.M. Byers, Squamous cell carcinoma of the tongue in young adults: increasing incidence and factors that predict treatment outcomes. Otolaryngol. Head Neck Surg. 122, 44–51 (2000)CrossRefPubMed
2.
go back to reference I.P. Ribeiro, F. Marques, F. Caramelo, J. Pereira, M. Patrício, H. Prazeres, J. Ferrão, M.J. Julião, M. Castelo-Branco, J.B. de Melo, I.P. Baptista, I.M. Carreira, Genetic gains and losses in oral squamous cell carcinoma: impact on clinical management. Cell Oncol. 37, 29–39 (2014)CrossRef I.P. Ribeiro, F. Marques, F. Caramelo, J. Pereira, M. Patrício, H. Prazeres, J. Ferrão, M.J. Julião, M. Castelo-Branco, J.B. de Melo, I.P. Baptista, I.M. Carreira, Genetic gains and losses in oral squamous cell carcinoma: impact on clinical management. Cell Oncol. 37, 29–39 (2014)CrossRef
3.
go back to reference T. Nakaoka, A. Ota, T. Ono, S. Karnan, H. Konishi, A. Furuhashi, Y. Ohmura, Y. Yamada, Y. Hosokawa, Y. Kazaoka, Combined arsenic trioxide-cisplatin treatment enhances apoptosis in oral squamous cell carcinoma cells. Cell Oncol. 37, 119–129 (2014)CrossRef T. Nakaoka, A. Ota, T. Ono, S. Karnan, H. Konishi, A. Furuhashi, Y. Ohmura, Y. Yamada, Y. Hosokawa, Y. Kazaoka, Combined arsenic trioxide-cisplatin treatment enhances apoptosis in oral squamous cell carcinoma cells. Cell Oncol. 37, 119–129 (2014)CrossRef
4.
go back to reference R.S. Patel, J.R. Clark, R. Dirven, R. Wyten, K. Gao, C.J. O'Brien, Prognostic factors in the surgical treatment of patients with oral carcinoma. ANZ J. Surg. 79, 19–22 (2009)CrossRefPubMed R.S. Patel, J.R. Clark, R. Dirven, R. Wyten, K. Gao, C.J. O'Brien, Prognostic factors in the surgical treatment of patients with oral carcinoma. ANZ J. Surg. 79, 19–22 (2009)CrossRefPubMed
5.
go back to reference S. Müller, Y. Pan, R. Li, A.C. Chi, Changing trends in oral squamous cell carcinoma with particular reference to young patients: 1971–2006. The Emory University experience. Head Neck Pathol. 2, 60–66 (2008)CrossRefPubMedPubMedCentral S. Müller, Y. Pan, R. Li, A.C. Chi, Changing trends in oral squamous cell carcinoma with particular reference to young patients: 1971–2006. The Emory University experience. Head Neck Pathol. 2, 60–66 (2008)CrossRefPubMedPubMedCentral
6.
go back to reference A.R. Fakih, R.S. Rao, A.M. Borges, A.R. Patel, Elective versus therapeutic neck dissection in early carcinoma of the oral tongue. Am. J. Surg. 158, 309–313 (1989)CrossRefPubMed A.R. Fakih, R.S. Rao, A.M. Borges, A.R. Patel, Elective versus therapeutic neck dissection in early carcinoma of the oral tongue. Am. J. Surg. 158, 309–313 (1989)CrossRefPubMed
7.
go back to reference K. Rusthoven, A. Ballonoff, D. Raben, C. Chen, Poor prognosis in patients with stage I and II oral tongue squamous cell carcinoma. Cancer 112, 345–351 (2008)CrossRefPubMed K. Rusthoven, A. Ballonoff, D. Raben, C. Chen, Poor prognosis in patients with stage I and II oral tongue squamous cell carcinoma. Cancer 112, 345–351 (2008)CrossRefPubMed
8.
go back to reference D. Sidransky, Nucleic acid-based methods for the detection of cancer. Science 278, 1054–1059 (1997)CrossRefPubMed D. Sidransky, Nucleic acid-based methods for the detection of cancer. Science 278, 1054–1059 (1997)CrossRefPubMed
9.
go back to reference E. Guzel, O.F. Karatas, A. Semercioz, S. Ekici, S. Aykan, S. Yentur, C.J. Creighton, M. Ittmann, M. Ozen, Identification of microRNAs differentially expressed in prostatic secretions of patients with prostate cancer. Int. J. Cancer 136, 875–879 (2015)CrossRefPubMed E. Guzel, O.F. Karatas, A. Semercioz, S. Ekici, S. Aykan, S. Yentur, C.J. Creighton, M. Ittmann, M. Ozen, Identification of microRNAs differentially expressed in prostatic secretions of patients with prostate cancer. Int. J. Cancer 136, 875–879 (2015)CrossRefPubMed
10.
go back to reference J. Hoffmann, A. Munz, M. Krimmel, G. Alfter, Intraoperative and postoperative kinetics of serum tumor markers in patients with oral carcinoma. J. Oral Maxillofac. Surg. 56, 1390–1393 (1998)CrossRefPubMed J. Hoffmann, A. Munz, M. Krimmel, G. Alfter, Intraoperative and postoperative kinetics of serum tumor markers in patients with oral carcinoma. J. Oral Maxillofac. Surg. 56, 1390–1393 (1998)CrossRefPubMed
11.
go back to reference M. Krimmel, J. Hoffmann, C. Krimmel, C.P. Cornelius, N. Schwenzer, Relevance of SCC-Ag, CEA, CA 19.9 and CA 125 for diagnosis and follow-up in oral cancer. J. Craniomaxillofac. Surg. 26, 243–248 (1998)CrossRefPubMed M. Krimmel, J. Hoffmann, C. Krimmel, C.P. Cornelius, N. Schwenzer, Relevance of SCC-Ag, CEA, CA 19.9 and CA 125 for diagnosis and follow-up in oral cancer. J. Craniomaxillofac. Surg. 26, 243–248 (1998)CrossRefPubMed
12.
go back to reference W.R. Kuo, K.W. Lee, K.Y. Ho, S.M. Tsai, F.Y. Chiang, K.H. Juan, Tissue polypeptide antigen, carcinoembryonic antigen, carbohydrate antigen, and CA125 levels as tumor markers in squamous cell carcinoma of the head and neck. Kaohsiung J. Med. Sci. 15, 152–158 (1999)PubMed W.R. Kuo, K.W. Lee, K.Y. Ho, S.M. Tsai, F.Y. Chiang, K.H. Juan, Tissue polypeptide antigen, carcinoembryonic antigen, carbohydrate antigen, and CA125 levels as tumor markers in squamous cell carcinoma of the head and neck. Kaohsiung J. Med. Sci. 15, 152–158 (1999)PubMed
13.
go back to reference A. Korostoff, L. Reder, R. Masood, U.K. Sinha, The role of salivary cytokine biomarkers in tongue cancer invasion and mortality. Oral Oncol. 47, 282–287 (2011)CrossRefPubMed A. Korostoff, L. Reder, R. Masood, U.K. Sinha, The role of salivary cytokine biomarkers in tongue cancer invasion and mortality. Oral Oncol. 47, 282–287 (2011)CrossRefPubMed
14.
go back to reference Y. Ogawa, Y. Taketomi, M. Murakami, M. Tsujimoto, R. Yanoshita, Small RNA transcriptomes of two types of exosomes in human whole saliva determined by next generation sequencing. Biol. Pharm. Bull. 36, 66–75 (2013)CrossRefPubMed Y. Ogawa, Y. Taketomi, M. Murakami, M. Tsujimoto, R. Yanoshita, Small RNA transcriptomes of two types of exosomes in human whole saliva determined by next generation sequencing. Biol. Pharm. Bull. 36, 66–75 (2013)CrossRefPubMed
15.
go back to reference M. Yakob, L. Fuentes, M.B. Wang, E. Abemayor, D.T. Wong, Salivary biomarkers for detection of oral squamous cell carcinoma - current state and recent advances. Curr. Oral Health Rep. 1, 133–141 (2014)CrossRefPubMedPubMedCentral M. Yakob, L. Fuentes, M.B. Wang, E. Abemayor, D.T. Wong, Salivary biomarkers for detection of oral squamous cell carcinoma - current state and recent advances. Curr. Oral Health Rep. 1, 133–141 (2014)CrossRefPubMedPubMedCentral
16.
go back to reference C. Salazar, R. Nagadia, P. Pandit, J. Cooper-White, N. Banerjee, N. Dimitrova, W.B. Coman, C. Punyadeera, A novel saliva-based microRNA biomarker panel to detect head and neck cancers. Cell Oncol. 37, 331–338 (2014)CrossRef C. Salazar, R. Nagadia, P. Pandit, J. Cooper-White, N. Banerjee, N. Dimitrova, W.B. Coman, C. Punyadeera, A novel saliva-based microRNA biomarker panel to detect head and neck cancers. Cell Oncol. 37, 331–338 (2014)CrossRef
17.
go back to reference S. Hu, J. Wang, J. Meijer, S. Ieong, Y. Xie, T. Yu, H. Zhou, S. Henry, A. Vissink, J. Pijpe, C. Kallenberg, D. Elashoff, J.A. Loo, D.T. Wong, Salivary proteomic and genomic biomarkers for primary Sjögren's syndrome. Arthritis Rheum. 56, 3588–3600 (2007)CrossRefPubMedPubMedCentral S. Hu, J. Wang, J. Meijer, S. Ieong, Y. Xie, T. Yu, H. Zhou, S. Henry, A. Vissink, J. Pijpe, C. Kallenberg, D. Elashoff, J.A. Loo, D.T. Wong, Salivary proteomic and genomic biomarkers for primary Sjögren's syndrome. Arthritis Rheum. 56, 3588–3600 (2007)CrossRefPubMedPubMedCentral
18.
go back to reference L. Seugnet, J. Boero, L. Gottschalk, S.P. Duntley, P.J. Shaw, Identification of a biomarker for sleep drive in flies and humans. Proc. Natl. Acad. Sci. U. S. A. 103, 19913–19918 (2006)CrossRefPubMedPubMedCentral L. Seugnet, J. Boero, L. Gottschalk, S.P. Duntley, P.J. Shaw, Identification of a biomarker for sleep drive in flies and humans. Proc. Natl. Acad. Sci. U. S. A. 103, 19913–19918 (2006)CrossRefPubMedPubMedCentral
19.
go back to reference Y. Güven, I. Satman, N. Dinççağ, S. Alptekin, Salivary peroxidase activity in whole saliva of patients with insulin-dependent (type-1) diabetes mellitus. J. Clin. Periodontol. 23, 879–881 (1996)CrossRefPubMed Y. Güven, I. Satman, N. Dinççağ, S. Alptekin, Salivary peroxidase activity in whole saliva of patients with insulin-dependent (type-1) diabetes mellitus. J. Clin. Periodontol. 23, 879–881 (1996)CrossRefPubMed
20.
go back to reference L.C. Fletcher, K.E. Burke, P.L. Caine, N.L. Rinne, C.A. Braniff, H.R. Davis, K.A. Miles, C. Packer, Diagnosing Alzheimer's disease: are we any nearer to useful biomarker-based, non-invasive tests? GMS Health Technol. Assess. 9, Doc01 (2013)PubMedPubMedCentral L.C. Fletcher, K.E. Burke, P.L. Caine, N.L. Rinne, C.A. Braniff, H.R. Davis, K.A. Miles, C. Packer, Diagnosing Alzheimer's disease: are we any nearer to useful biomarker-based, non-invasive tests? GMS Health Technol. Assess. 9, Doc01 (2013)PubMedPubMedCentral
21.
go back to reference C. Streckfus, L. Bigler, T. Dellinger, X. Dai, A. Kingman, J.T. Thigpen, The presence of soluble c-erbB-2 in saliva and serum among women with breast carcinoma: a preliminary study. Clin. Cancer Res. 6, 2363–2370 (2000)PubMed C. Streckfus, L. Bigler, T. Dellinger, X. Dai, A. Kingman, J.T. Thigpen, The presence of soluble c-erbB-2 in saliva and serum among women with breast carcinoma: a preliminary study. Clin. Cancer Res. 6, 2363–2370 (2000)PubMed
22.
go back to reference X.F. Jin, N. Wu, L. Wang, J. Li, Circulating microRNAs: a novel class of potential biomarkers for diagnosing and prognosing central nervous system diseases. Cell. Mol. Neurobiol. 33, 601–613 (2013)CrossRefPubMed X.F. Jin, N. Wu, L. Wang, J. Li, Circulating microRNAs: a novel class of potential biomarkers for diagnosing and prognosing central nervous system diseases. Cell. Mol. Neurobiol. 33, 601–613 (2013)CrossRefPubMed
23.
go back to reference J.A. Weber, D.H. Baxter, S. Zhang, D.Y. Huang, K.H. Huang, M.J. Lee, D.J. Galas, K. Wang, The microRNA spectrum in 12 body fluids. Clin. Chem. 56, 1733–1741 (2010)CrossRefPubMed J.A. Weber, D.H. Baxter, S. Zhang, D.Y. Huang, K.H. Huang, M.J. Lee, D.J. Galas, K. Wang, The microRNA spectrum in 12 body fluids. Clin. Chem. 56, 1733–1741 (2010)CrossRefPubMed
24.
go back to reference P.M. Voorhoeve, R. Agami, Classifying microRNAs in cancer: the good, the bad and the ugly. Biochim. Biophys. Acta 1775, 274–282 (2007)PubMed P.M. Voorhoeve, R. Agami, Classifying microRNAs in cancer: the good, the bad and the ugly. Biochim. Biophys. Acta 1775, 274–282 (2007)PubMed
25.
go back to reference M. Seven, O.F. Karatas, M.B. Duz, M. Ozen, The role of miRNAs in cancer: from pathogenesis to therapeutic implications. Future Oncol. 10, 1027–1048 (2014)CrossRefPubMed M. Seven, O.F. Karatas, M.B. Duz, M. Ozen, The role of miRNAs in cancer: from pathogenesis to therapeutic implications. Future Oncol. 10, 1027–1048 (2014)CrossRefPubMed
26.
go back to reference E.J. Omelia, M.L. Uchimoto, G. Williams, Quantitative PCR analysis of blood- and saliva-specific microRNA markers following solid-phase DNA extraction. Anal. Biochem. 435, 120–122 (2013)CrossRefPubMed E.J. Omelia, M.L. Uchimoto, G. Williams, Quantitative PCR analysis of blood- and saliva-specific microRNA markers following solid-phase DNA extraction. Anal. Biochem. 435, 120–122 (2013)CrossRefPubMed
27.
go back to reference Z. Wang, H. Luo, X. Pan, M. Liao, Y. Hou, A model for data analysis of microRNA expression in forensic body fluid identification. Forensic Sci. Int. Genet. 6, 419–423 (2012)CrossRefPubMed Z. Wang, H. Luo, X. Pan, M. Liao, Y. Hou, A model for data analysis of microRNA expression in forensic body fluid identification. Forensic Sci. Int. Genet. 6, 419–423 (2012)CrossRefPubMed
28.
go back to reference O.F. Karatas, E. Guzel, I. Suer, I.D. Ekici, T. Caskurlu, C.J. Creighton, M. Ittmann, M. Ozen, miR-1 and miR-133b are differentially expressed in patients with recurrent prostate cancer. PLos ONE 9(6), e98675 (2014)CrossRefPubMedPubMedCentral O.F. Karatas, E. Guzel, I. Suer, I.D. Ekici, T. Caskurlu, C.J. Creighton, M. Ittmann, M. Ozen, miR-1 and miR-133b are differentially expressed in patients with recurrent prostate cancer. PLos ONE 9(6), e98675 (2014)CrossRefPubMedPubMedCentral
29.
go back to reference C.J. Liu, S.C. Lin, C.C. Yang, H.W. Cheng, K.W. Chang, Exploiting salivary miR-31 as a clinical biomarker of oral squamous cell carcinoma. Head Neck 34, 219–224 (2012)CrossRefPubMed C.J. Liu, S.C. Lin, C.C. Yang, H.W. Cheng, K.W. Chang, Exploiting salivary miR-31 as a clinical biomarker of oral squamous cell carcinoma. Head Neck 34, 219–224 (2012)CrossRefPubMed
30.
go back to reference K.J. Livak, T.D. Schmittgen, Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25, 402–408 (2001)CrossRefPubMed K.J. Livak, T.D. Schmittgen, Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25, 402–408 (2001)CrossRefPubMed
31.
go back to reference R.M. Nagler, M. Barak, M. Peled, H. Ben-Aryeh, M. Filatov, D. Laufer, Early diagnosis and treatment monitoring roles of tumor markers Cyfra 21–1 and TPS in oral squamous cell carcinoma. Cancer 85, 1018–1025 (1999)CrossRefPubMed R.M. Nagler, M. Barak, M. Peled, H. Ben-Aryeh, M. Filatov, D. Laufer, Early diagnosis and treatment monitoring roles of tumor markers Cyfra 21–1 and TPS in oral squamous cell carcinoma. Cancer 85, 1018–1025 (1999)CrossRefPubMed
32.
go back to reference R. Nagler, G. Bahar, T. Shpitzer, R. Feinmesser, Concomitant analysis of salivary tumor markers--a new diagnostic tool for oral cancer. Clin. Cancer Res. 12, 3979–3984 (2006)CrossRefPubMed R. Nagler, G. Bahar, T. Shpitzer, R. Feinmesser, Concomitant analysis of salivary tumor markers--a new diagnostic tool for oral cancer. Clin. Cancer Res. 12, 3979–3984 (2006)CrossRefPubMed
33.
go back to reference S.S. Yilmaz, E. Guzel, O.F. Karatas, M. Yilmaz, C.J. Creighton, M. Ozen, MiR-221 as a pre- and postoperative plasma biomarker for larynx cancer patients. Laryngoscope (2015). doi:10.1002/lary.25332 S.S. Yilmaz, E. Guzel, O.F. Karatas, M. Yilmaz, C.J. Creighton, M. Ozen, MiR-221 as a pre- and postoperative plasma biomarker for larynx cancer patients. Laryngoscope (2015). doi:10.​1002/​lary.​25332
34.
go back to reference T. Blondal, S. Jensby Nielsen, A. Baker, D. Andreasen, P. Mouritzen, M. Wrang Teilum, I.K. Dahlsveen, Assessing sample and miRNA profile quality in serum and plasma or other biofluids. Methods 59, S1–S6 (2013)CrossRefPubMed T. Blondal, S. Jensby Nielsen, A. Baker, D. Andreasen, P. Mouritzen, M. Wrang Teilum, I.K. Dahlsveen, Assessing sample and miRNA profile quality in serum and plasma or other biofluids. Methods 59, S1–S6 (2013)CrossRefPubMed
35.
go back to reference N.J. Park, Y. Li, T. Yu, B.M. Brinkman, D.T. Wong, Characterization of RNA in saliva. Clin. Chem. 52, 988–994 (2006)CrossRefPubMed N.J. Park, Y. Li, T. Yu, B.M. Brinkman, D.T. Wong, Characterization of RNA in saliva. Clin. Chem. 52, 988–994 (2006)CrossRefPubMed
36.
go back to reference S. Hu, Y. Xie, P. Ramachandran, R.R. Ogorzalek Loo, Y. Li, J.A. Loo, D.T. Wong, Large-scale identification of proteins in human salivary proteome by liquid chromatography/mass spectrometry and two-dimensional gel electrophoresis-mass spectrometry. Proteomics 5, 1714–1728 (2005)CrossRefPubMed S. Hu, Y. Xie, P. Ramachandran, R.R. Ogorzalek Loo, Y. Li, J.A. Loo, D.T. Wong, Large-scale identification of proteins in human salivary proteome by liquid chromatography/mass spectrometry and two-dimensional gel electrophoresis-mass spectrometry. Proteomics 5, 1714–1728 (2005)CrossRefPubMed
37.
go back to reference Y. Li, X. Zhou, M.A. St John, D.T. Wong, RNA profiling of cell-free saliva using microarray technology. J. Dent. Res. 83, 199–203 (2004)CrossRefPubMed Y. Li, X. Zhou, M.A. St John, D.T. Wong, RNA profiling of cell-free saliva using microarray technology. J. Dent. Res. 83, 199–203 (2004)CrossRefPubMed
38.
go back to reference N.J. Park, H. Zhou, D. Elashoff, B.S. Henson, D.A. Kastratovic, E. Abemayor, D.T. Wong, Salivary microRNA: discovery, characterization, and clinical utility for oral cancer detection. Clin. Cancer Res. 15, 5473–5477 (2009)CrossRefPubMedPubMedCentral N.J. Park, H. Zhou, D. Elashoff, B.S. Henson, D.A. Kastratovic, E. Abemayor, D.T. Wong, Salivary microRNA: discovery, characterization, and clinical utility for oral cancer detection. Clin. Cancer Res. 15, 5473–5477 (2009)CrossRefPubMedPubMedCentral
39.
go back to reference T.S. Wong, X.B. Liu, B.Y. Wong, R.W. Ng, A.P. Yuen, W.I. Wei, Mature miR-184 as potential oncogenic microRNA of squamous cell carcinoma of tongue. Clin. Cancer Res. 14, 2588–2592 (2008)CrossRefPubMed T.S. Wong, X.B. Liu, B.Y. Wong, R.W. Ng, A.P. Yuen, W.I. Wei, Mature miR-184 as potential oncogenic microRNA of squamous cell carcinoma of tongue. Clin. Cancer Res. 14, 2588–2592 (2008)CrossRefPubMed
40.
go back to reference X. Liu, Z. Chen, J. Yu, J. Xia, X. Zhou, MicroRNA profiling and head and neck cancer. Comp. Funct. Genomics, 837514 (2009). X. Liu, Z. Chen, J. Yu, J. Xia, X. Zhou, MicroRNA profiling and head and neck cancer. Comp. Funct. Genomics, 837514 (2009).
41.
go back to reference K. Krishnan, A.L. Steptoe, H.C. Martin, D.R. Pattabiraman, K. Nones, N. Waddell, M. Mariasegaram, P.T. Simpson, S.R. Lakhani, A. Vlassov, S.M. Grimmond, N. Cloonan, miR-139-5p is a regulator of metastatic pathways in breast cancer. RNA 19, 1767–1780 (2013)CrossRefPubMedPubMedCentral K. Krishnan, A.L. Steptoe, H.C. Martin, D.R. Pattabiraman, K. Nones, N. Waddell, M. Mariasegaram, P.T. Simpson, S.R. Lakhani, A. Vlassov, S.M. Grimmond, N. Cloonan, miR-139-5p is a regulator of metastatic pathways in breast cancer. RNA 19, 1767–1780 (2013)CrossRefPubMedPubMedCentral
42.
go back to reference H.D. Zhang, L.H. Jiang, D.W. Sun, J. Li, J.H. Tang, MiR-139-5p: promising biomarker for cancer. Tumour Biol. 36, 1355–1365 (2015)CrossRefPubMed H.D. Zhang, L.H. Jiang, D.W. Sun, J. Li, J.H. Tang, MiR-139-5p: promising biomarker for cancer. Tumour Biol. 36, 1355–1365 (2015)CrossRefPubMed
43.
go back to reference J.K. Rane, M. Scaravilli, A. Ylipää, D. Pellacani, V.M. Mann, M.S. Simms, M. Nykter, A.T. Collins, T. Visakorpi, N.J. Maitland, MicroRNA expression profile of primary prostate cancer stem cells as a source of biomarkers and therapeutic targets. Eur. Urol. 67, 7–10 (2015)CrossRefPubMed J.K. Rane, M. Scaravilli, A. Ylipää, D. Pellacani, V.M. Mann, M.S. Simms, M. Nykter, A.T. Collins, T. Visakorpi, N.J. Maitland, MicroRNA expression profile of primary prostate cancer stem cells as a source of biomarkers and therapeutic targets. Eur. Urol. 67, 7–10 (2015)CrossRefPubMed
44.
go back to reference E. van Rooij, A.L. Purcell, A.A. Levin, Developing microRNA therapeutics. Circ. Res. 110, 496–507 (2012)CrossRefPubMed E. van Rooij, A.L. Purcell, A.A. Levin, Developing microRNA therapeutics. Circ. Res. 110, 496–507 (2012)CrossRefPubMed
45.
go back to reference L. Boldrup, P.J. Coates, G. Laurell, T. Wilms, R. Fahraeus, K. Nylander, Downregulation of miRNA-424: a sign of field cancerisation in clinically normal tongue adjacent to squamous cell carcinoma. Br. J. Cancer 112, 1760–1765 (2015)CrossRefPubMed L. Boldrup, P.J. Coates, G. Laurell, T. Wilms, R. Fahraeus, K. Nylander, Downregulation of miRNA-424: a sign of field cancerisation in clinically normal tongue adjacent to squamous cell carcinoma. Br. J. Cancer 112, 1760–1765 (2015)CrossRefPubMed
Metadata
Title
Identification of miR-139-5p as a saliva biomarker for tongue squamous cell carcinoma: a pilot study
Authors
Mehmet Bugrahan Duz
Omer Faruk Karatas
Esra Guzel
Nesrettin Fatih Turgut
Mehmet Yilmaz
Chad J. Creighton
Mustafa Ozen
Publication date
01-04-2016
Publisher
Springer Netherlands
Published in
Cellular Oncology / Issue 2/2016
Print ISSN: 2211-3428
Electronic ISSN: 2211-3436
DOI
https://doi.org/10.1007/s13402-015-0259-z

Other articles of this Issue 2/2016

Cellular Oncology 2/2016 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine