Evidence that circulating proteins are more promising than miRNAs for identification of patients with squamous cell carcinoma of the tongue
Status PubMed-not-MEDLINE Language English Country United States Media electronic-ecollection
Document type Journal Article
PubMed
29262574
PubMed Central
PMC5732740
DOI
10.18632/oncotarget.21402
PII: 21402
Knihovny.cz E-resources
- Keywords
- NT-3, circulating markers, miR-150, miRNA, squamous cell carcinoma of the tongue,
- Publication type
- Journal Article MeSH
Despite intense research, squamous cell carcinoma of the tongue remains a devastating disease with a five-year survival of around 60%. Late detection and recurrence are the main causes for poor survival. The identification of circulating factors for early diagnosis and/or prognosis of cancer is a rapidly evolving field of interest, with the hope of finding stable and reliable markers of clinical significance. The aim of this study was to evaluate circulating miRNAs and proteins as potential factors for distinguishing patients with tongue squamous cell carcinoma from healthy controls. Array-based profiling of 372 miRNAs in plasma samples showed broad variations between different patients and did not show any evidence for their use in diagnosis of tongue cancer. Although one miRNA, miR-150, was significantly down-regulated in plasma from patients compared to controls. Surprisingly, the corresponding tumor tissue showed an up-regulation of miR-150. Among circulating proteins, 23 were identified as potential markers of squamous cell carcinoma of the tongue. These findings imply that circulating proteins are a more promising source of biomarkers for tongue squamous cell carcinomas than circulating miRNAs. The data also highlight that circulating markers are not always directly associated with tumor cell properties.
Department of Clinical and Experimental Medicine University of Foggia 71122 Foggia Italy
Department of Clinical Sciences ENT Umeå University SE 901 85 Umeå Sweden
Department of Medical Biosciences Pathology Umeå University SE 901 85 Umeå Sweden
Institut de Génétique Moléculaire Université Paris 7 Hôpital St Louis 75010 Paris France
RECAMO Masaryk Memorial Cancer Institute 656 53 Brno Czech Republic
See more in PubMed
Siegel RL, Miller KD, Jemal A. Cancer statistics, 2015. CA Cancer J Clin. 2015;65:5–29. PubMed
Lam L, Logan RM, Luke C, Rees GL. Retrospective study of survival and treatment pattern in a cohort of patients with oral and oropharyngeal tongue cancers from 1987 to 2004. Oral Oncol. 2007;43:150–158. PubMed
Agra IM, Carvalho AL, Pinto CA, Martins EP, Filho JG, Soares FA, Kowalski LP. Biological markers and prognosis in recurrent oral cancer after salvage surgery. Arch Otolaryngol Head Neck Surg. 2008;134:743–749. PubMed
Carvalho AL, Magrin J, Kowalski LP. Sites of recurrence in oral and oropharyngeal cancers according to the treatment approach. Oral Dis. 2003;9:112–118. PubMed
Rothenberg SM, Ellisen LW. The molecular pathogenesis of head and neck squamous cell carcinoma. J Clin Invest. 2012;122:1951–1957. PubMed PMC
Mitchell PS, Parkin RK, Kroh EM, Fritz BR, Wyman SK, Pogosova-Agadjanyan EL, Peterson A, Noteboom J, O’Briant KC, Allen A, Lin DW, Urban N, Drescher CW, et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci USA. 2008;105:10513–18. PubMed PMC
Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell. 1993;75:843–854. PubMed
Weber JA, Baxter DH, Zhang S, Huang DY, Huang KH, Lee MJ, Galas DJ, Wang K. The microRNA spectrum in 12 body fluids. Clin Chem. 2010;56:1733–1741. PubMed PMC
Chen M, Calin GA, Meng QH. Circulating microRNAs as Promising Tumor Biomarkers. Adv Clin Chem. 2014;67:189–214. PubMed
Cheng G. Circulating miRNAs: roles in cancer diagnosis, prognosis and therapy. Adv Drug Deliv Rev. 2015;81:75–93. PubMed
Jarry J, Schadendorf D, Greenwood C, Spatz A, van Kempen LC. The validity of circulating microRNAs in oncology: five years of challenges and contradictions. Mol Oncol. 2014;8:819–829. PubMed PMC
Koberle V, Pleli T, Schmithals C, Augusto Alonso E, Haupenthal J, Bonig H, Peveling-Oberhag J, Biondi RM, Zeuzem S, Kronenberger B, Waidmann O, Piiper A. Differential stability of cell-free circulating microRNAs: implications for their utilization as biomarkers. PLoS One. 2013;8:e75184. PubMed PMC
Aleckovic M, Kang Y. Regulation of cancer metastasis by cell-free miRNAs. Biochim Biophys Acta. 2015;1855:24–42. PubMed PMC
Schwarzenbach H, Nishida N, Calin GA, Pantel K. Clinical relevance of circulating cell-free microRNAs in cancer. Nat Rev Clin Oncol. 2014;11:145–156. PubMed
Troiano G, Boldrup L, Ardito F, Gu X, Lo Muzio L, Nylander K. Circulating miRNAs from blood, plasma or serum as promising clinical biomarkers in oral squamous cell carcinoma: A systematic review of current findings. Oral Oncol. 2016;63:30–37. PubMed
Lilja H, Ulmert D, Vickers AJ. Prostate-specific antigen and prostate cancer: prediction, detection and monitoring. Nat Rev Cancer. 2008;8:268–278. PubMed
Felder M, Kapur A, Gonzalez-Bosquet J, Horibata S, Heintz J, Albrecht R, Fass L, Kaur J, Hu K, Shojaei H, Whelan RJ, Patankar MS. MUC16 (CA125): tumor biomarker to cancer therapy, a work in progress. Mol Cancer. 2014;13:129. PubMed PMC
Kaskas NM, Moore-Medlin T, McClure GB, Ekshyyan O, Vanchiere JA, Nathan CA. Serum biomarkers in head and neck squamous cell cancer. JAMA Otolaryngol Head Neck Surg. 2014;140:5–11. PubMed
Lin HS, Siddiq F, Talwar HS, Chen W, Voichita C, Draghici S, Jeyapalan G, Chatterjee M, Fribley A, Yoo GH, Sethi S, Kim H, Sukari A, et al. Serum prognostic biomarkers in head and neck cancer patients. Laryngoscope. 2014;124:1819–1826. PubMed PMC
Linkov F, Lisovich A, Yurkovetsky Z, Marrangoni A, Velikokhatnaya L, Nolen B, Winans M, Bigbee W, Siegfried J, Lokshin A, Ferris RL. Early detection of head and neck cancer: development of a novel screening tool using multiplexed immunobead-based biomarker profiling. Cancer Epidemiol Biomarkers Prev. 2007;16:102–107. PubMed
Imai R, Takenaka Y, Yasui T, Nakahara S, Yamamoto Y, Hanamoto A, Takemoto N, Fukusumi T, Cho H, Yamamoto M, Inohara H. Prognostic significance of serum squamous cell carcinoma antigen in patients with head and neck cancer. Acta Otolaryngol. 2015;135:295–301. PubMed
Yamashita T, Shimada H, Tanaka S, Araki K, Tomifuji M, Mizokami D, Tanaka N, Kamide D, Miyagawa Y, Suzuki H, Tanaka Y, Shiotani A. Serum midkine as a biomarker for malignancy, prognosis, and chemosensitivity in head and neck squamous cell carcinoma. Cancer Med. 2016;5:415–425. PubMed PMC
Fredriksson S, Gullberg M, Jarvius J, Olsson C, Pietras K, Gustafsdottir SM, Ostman A, Landegren U. Protein detection using proximity-dependent DNA ligation assays. Nat Biotechnol. 2002;20:473–477. PubMed
Gullberg M, Gustafsdottir SM, Schallmeiner E, Jarvius J, Bjarnegard M, Betsholtz C, Landegren U, Fredriksson S. Cytokine detection by antibody-based proximity ligation. Proc Natl Acad Sci U S A. 2004;101:8420–8424. PubMed PMC
Assarsson E, Lundberg M, Holmquist G, Björkesten J, Thorsen SB, Ekman D, Eriksson A, Rennel Dickens E, Ohlsson S, Edfeldt G, Andersson AC, Lindstedt P, Stenvang J, et al. Homogenous 96-plex PEA immunoassay exhibiting high sensitivity, specificity, and excellent scalability. PLoS One. 2014;9:e95192. PubMed PMC
Boldrup L, Gu X, Coates PJ, Norberg-Spaak L, Fahraeus R, Laurell G, Wilms T, Nylander K. Gene expression changes in tumor free tongue tissue adjacent to tongue squamous cell carcinoma. Oncotarget. 2017;8:19389–402. https://doi.org/10.18632/oncotarget.14288. PubMed DOI PMC
Hsu CM, Lin PM, Wang YM, Chen ZJ, Lin SF, Yang MY. Circulating miRNA is a novel marker for head and neck squamous cell carcinoma. Tumour Biol. 2012;33:1933–1942. PubMed
Liu CJ, Kao SY, Tu HF, Tsai MM, Chang KW, Lin SC. Increase of microRNA miR-31 level in plasma could be a potential marker of oral cancer. Oral Dis. 2010;16:360–364. PubMed
Summerer I, Unger K, Braselmann H, Schuettrumpf L, Maihoefer C, Baumeister P, Kirchner T, Niyazi M, Sage E, Specht HM, Multhoff G, Moertl S, Belka C, Zitzelsberger H. Circulating microRNAs as prognostic therapy biomarkers in head and neck cancer patients. Br J Cancer. 2015;113:76–82. PubMed PMC
Wong TS, Liu XB, Wong BY, Ng RW, Yuen AP, Wei WI. Mature miR-184 as Potential Oncogenic microRNA of Squamous Cell Carcinoma of Tongue. Clin Cancer Res. 2008;14:2588–2592. PubMed
Tiberio P, Callari M, Angeloni V, Daidone MG, Appierto V. Challenges in using circulating miRNAs as cancer biomarkers.BioMed Res Int. 2015;2015:731479. PubMed PMC
Boldrup L, Coates PJ, Laurell G, Nylander K. Differences in p63 expression in SCCHN tumours of different sub-sites within the oral cavity. Oral Oncol. 2011;47:861–865. PubMed
Boldrup L, Coates PJ, Wahlgren M, Laurell G, Nylander K. Subsite-based alterations in miR-21, miR-125b, and miR-203 in squamous cell carcinoma of the oral cavity and correlation to important target proteins. J Carcinog. 2012;11:18. PubMed PMC
Trivedi TI, Tankshali RA, Goswami JV, Shukla SN, Shah PM, Shah NG. Identification of site-specific prognostic biomarkers in patients with oral squamous cell carcinoma. Neoplasma. 2011;58:217–226. PubMed
Nylander E, Ebrahimi M, Wahlin YB, Boldrup L, Nylander K. Changes in miRNA expression in sera and correlation to duration of disease in patients with multifocal mucosal lichen planus. J Oral Pathol Med. 2012;41:86–89. PubMed
Aherne ST, Madden SF, Hughes DJ, Pardini B, Naccarati A, Levy M, Vodicka P, Neary P, Dowling P, Clynes M. Circulating miRNAs miR-34a and miR-150 associated with colorectal cancer progression. BMC Cancer. 2015;15:329. PubMed PMC
Selth LA, Tilley WD, Butler LM. Circulating microRNAs: macro-utility as markers of prostate cancer? Endocr Relat Cancer. 2012;19:R99–R113. PubMed
Pritchard CC, Kroh E, Wood B, Arroyo JD, Dougherty KJ, Miyaji MM, Tait JF, Tewari M. Blood cell origin of circulating microRNAs: a cautionary note for cancer biomarker studies. Cancer Prev Res (Phila) 2012;5:492–497. PubMed PMC
Xiao C, Calado DP, Galler G, Thai TH, Patterson HC, Wang J, Rajewsky N, Bender TP, Rajewsky K. MiR-150 controls B cell differentiation by targeting the transcription factor c-Myb. Cell. 2007;131:146–159. PubMed
Lerman G, Avivi C, Mardoukh C, Barzilai A, Tessone A, Gradus B, Pavlotsky F, Barshack I, Polak-Charcon S, Orenstein A, Hornstein E, Sidi Y, Avni D. MiRNA expression in psoriatic skin: reciprocal regulation of hsa-miR-99a and IGF-1R. PLoS One. 2011;6:e20916. PubMed PMC
Bender TP, Kremer CS, Kraus M, Buch T, Rajewsky K. Critical functions for c-Myb at three checkpoints during thymocyte development. Nat Immunol. 2004;5:721–729. PubMed
He Y, Jiang X, Chen J. The role of miR-150 in normal and malignant hematopoiesis. Oncogene. 2014;33:3887–3893. PubMed
Thomas MD, Kremer CS, Ravichandran KS, Rajewsky K, Bender TP. c-Myb is critical for B cell development and maintenance of follicular B cells. Immunity. 2005;23:275–286. PubMed
Nosrat CA. Neurotrophic factors in the tongue: expression patterns, biological activity, relation to innervation and studies of neurotrophin knockout mice. Ann N Y Acad Sci. 1998;855:28–49. PubMed
Louie E, Chen XF, Coomes A, Ji K, Tsirka S, Chen EI. Neurotrophin-3 modulates breast cancer cells and the microenvironment to promote the growth of breast cancer brain metastasis. Oncogene. 2013;32:4064–4077. PubMed PMC
Ricci A, Greco S, Mariotta S, Felici L, Bronzetti E, Cavazzana A, Cardillo G, Amenta F, Bisetti A, Barbolini G. Neurotrophins and neurotrophin receptors in human lung cancer. Am J Respir Cell Mol Biol. 2001;25:439–446. PubMed
Ivanov SV, Panaccione A, Brown B, Guo Y, Moskaluk CA, Wick MJ, Brown JL, Ivanova AV, Issaeva N, El-Naggar AK, Yarbrough WG. TrkC signaling is activated in adenoid cystic carcinoma and requires NT-3 to stimulate invasive behavior. Oncogene. 2013;32:3698–3710. PubMed