Altered expression of microRNA-30a-3p in papillary thyroid cancer and its association with clinicopathological characteristics

Authors

  • Lidija Todorović Laboratory for Radiobiology and Molecular Genetics, “Vinča” Institute of Nuclear Sciences, University of Belgrade, Mike Petrovića Alasa 12-14, 11351 Belgrade http://orcid.org/0000-0003-0672-0693
  • Vesna Mandušić Laboratory for Radiobiology and Molecular Genetics, “Vinča” Institute of Nuclear Sciences, University of Belgrade, Mike Petrovića Alasa 12-14, 11351 Belgrade http://orcid.org/0000-0002-2221-3707
  • Biljana Vučetić Tadić Institute for Mother and Child Healthcare of Serbia, Radoja Dakića 6, 11000 Belgrade http://orcid.org/0000-0003-2245-8429
  • Vladan Živaljević 1. Center for Endocrine Surgery, Clinical Center of Serbia, Dr Koste Todorovića 8, 11000 Belgrade; 2. School of Medicine, University of Belgrade, Doktora Subotića 8, 11000 Belgrade http://orcid.org/0000-0002-6661-6751
  • Ivan Paunović 1. Center for Endocrine Surgery, Clinical Center of Serbia, Dr Koste Todorovića 8, 11000 Belgrade; 2. School of Medicine, University of Belgrade, Doktora Subotića 8, 11000 Belgrade http://orcid.org/0000-0002-8718-7503
  • Boban Stanojević Laboratory for Radiobiology and Molecular Genetics, “Vinča” Institute of Nuclear Sciences, University of Belgrade, Mike Petrovića Alasa 12-14, 11351 Belgrade http://orcid.org/0000-0002-4674-0384

Keywords:

miR-30a-3p, papillary thyroid cancer (PTC), thyroid cancer, expression, advanced stage

Abstract

Paper description:

  • Identification of novel molecular biomarkers can aid in stratification of patients with papillary thyroid cancer (PTC) into low- and high-risk prognostic groups. A growing body of evidence suggests a role for microRNA-30a-3p in aggressiveness and progression of various types of cancer.
  • We show that miR-30a-3p expression levels were deregulated in PTC compared to non-tumor thyroid tissues. Decreased expression was associated with advanced stage, multifocality and capsular invasion.
  • This is one of few studies of microRNA-30a-3p expression in PTC, indicating its potential involvement in the development and/or progression of this type of cancer.


Abstract: A growing number of studies suggest a tumor suppressive role and potential prognostic significance of miR-30a-3p in different types of cancer. However, relatively few studies have focused on this microRNA in neoplastic thyroid lesions, including papillary thyroid cancer (PTC). The aim of our study was to shed more light on the potential involvement and clinical relevance of miR-30a-3p in this type of cancer. We examined the expression levels of this microRNA in 42 pairs of PTCs and matched non-tumor thyroid tissues using quantitative RT-PCR. We analyzed their association with clinical and histopathological parameters. The results revealed that miR-30a-3p was significantly downregulated in the majority of PTC tissues compared to corresponding non-tumor tissues. Moreover, decreased expression of miR-30a-3p was associated with advanced clinical stage, presence of multiple tumor foci and capsular invasion, suggesting a role in aggressive disease. Although the role of this microRNA and its prognostic utility remain to be elucidated, the presented data suggest that downregulated expression of miR-30a-3p indicates poorer prognosis in PTC patients, warranting further investigations.

https://doi.org/10.2298/ABS191004063T

Received: October 4, 2019; Revised: October 14, 2019; Accepted: October 15, 2019; Published online: October 25, 2019

How to cite this article: Todorović L, Mandušić V, Vučetić Tadić B, Živaljević V, Paunović I,  Stanojević B.Altered expression of microRNA-30a-3p in papillary thyroid cancer and its association with clinicopathological characteristics. Arch Biol Sci. 2020;72(1):31-6.

Downloads

Download data is not yet available.

References

Sipos JA, Mazzaferri EL. Thyroid cancer epidemiology and prognostic variables. Clin Oncol (R Coll Radiol). 2010;22(6):395-404.

Lim H, Devesa SS, Sosa JA, Check D, Kitahara CM. Trends in Thyroid Cancer Incidence and Mortality in the United States, 1974-2013. JAMA. 2017;317(13):1338-48.

Pacini F, Castagna MG, Brilli L, Pentheroudakis G. Thyroid cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2012;23(Suppl 7):vii110-9.

Lebastchi AH, Callender GG. Thyroid cancer. Curr Probl Cancer. 2014;38(2):48-74.

Hayes J, Peruzzi PP, Lawler S. MicroRNAs in cancer: biomarkers, functions and therapy. Trends Mol Med. 2014;20(8):460-9.

Acunzo M, Romano G, Wernicke D, Croce CM. MicroRNA and cancer--a brief overview. Adv Biol Regul. 2015;57:1-9.

Yu N, Yong S, Kim HK, Choi YL, Jung Y, Kim D, Seo J, Lee YE, Baek D, Lee J, Lee S, Lee JE, Kim J. Identification of tumor suppressor miRNAs by integrative miRNA and mRNA sequencing of matched tumor-normal samples in lung adenocarcinoma. Mol Oncol. 2019;13(6):1356-68.

Tang R, Liang L, Luo D, Feng Z, Huang Q, He R, Gan T, Yang L, Chen G. Downregulation of MiR-30a is Associated with Poor Prognosis in Lung Cancer. Med Sci Monit. 2015;21:2514-20.

Jin X, Chen Y, Chen H, Fei S, Chen D, Cai X, Liu L, Lin B, Su H, Zhao L, Su M, Pan H, Shen L, Xie D, Xie C. Evaluation of Tumor-Derived Exosomal miRNA as Potential Diagnostic Biomarkers for Early-Stage Non-Small Cell Lung Cancer Using Next-Generation Sequencing. Clin Cancer Res. 2017;23(17):5311-9.

Zhang Y, Sui J, Shen X, Li C, Yao W, Hong W, Peng H, Pu Y, Yin L, Liang G. Differential expression profiles of microRNAs as potential biomarkers for the early diagnosis of lung cancer. Oncol Rep. 2017;37(6):3543-53.

Perez-Rivas LG, Jerez JM, Carmona R, de Luque V, Vicioso L, Claros MG, Viguera E, Pajares B, Sanchez A, Ribelles N, Alba E, Lozano J. A microRNA signature associated with early recurrence in breast cancer. PLoS One. 2014;9(3):e91884.

Rodriguez-Gonzalez FG, Sieuwerts AM, Smid M, Look MP, Meijer-van Gelder ME, de Weerd V, Sleijfer S, Martens JW, Foekens JA. MicroRNA-30c expression level is an independent predictor of clinical benefit of endocrine therapy in advanced estrogen receptor positive breast cancer. Breast Cancer Res Treat. 2011;127(1):43-51.

Turashvili G, Lightbody ED, Tyryshkin K, SenGupta SK, Elliott BE, Madarnas Y, Ghaffari A, Day A, Nicol CJB. Novel prognostic and predictive microRNA targets for triple-negative breast cancer. FASEB J. 2018;32(11):5937-54.

Ma Y, Zhang P, Yang J, Liu Z, Yang Z, Qin H. Candidate microRNA biomarkers in human colorectal cancer: systematic review profiling studies and experimental validation. Int J Cancer. 2012;130(9):2077-87.

Ichimi T, Enokida H, Okuno Y, Kunimoto R, Chiyomaru T, Kawamoto K, Kawahara K, Toki K, Kawakami K, Nishiyama K, Tsujimoto G, Nakagawa M, Seki N. Identification of novel microRNA targets based on microRNA signatures in bladder cancer. Int J Cancer. 2009;125(2):345-52.

Wang Y, Li L, Qu Z, Li R, Bi T, Jiang J, Zhao H. The expression of miR-30a* and miR-30e* is associated with a dualistic model for grading ovarian papillary serious carcinoma. Int J Oncol. 2014;44(6):1904-14.

Tsukamoto O, Miura K, Mishima H, Abe S, Kaneuchi M, Higashijima A, Miura S, Kinoshita A, Yoshiura K, Masuzaki H. Identification of endometrioid endometrial carcinoma-associated microRNAs in tissue and plasma. Gynecol Oncol. 2014;132(3):715-21.

Wang W, Lin H, Zhou L, Zhu Q, Gao S, Xie H, Liu Z, Xu Z, Wei J, Huang X, Zheng S. MicroRNA-30a-3p inhibits tumor proliferation, invasiveness and metastasis and is downregulated in hepatocellular carcinoma. Eur J Surg Oncol. 2014;40(11):1586-94.

Ozdogan H, Gur Dedeoglu B, Oztemur Islakoglu Y, Aydos A, Kose S, Atalay A, Yegin ZA, Avcu F, Uckan Cetinkaya D, Ilhan O. DICER1 gene and miRNA dysregulation in mesenchymal stem cells of patients with myelodysplastic syndrome and acute myeloblastic leukemia. Leuk Res. 2017;63:62-71.

Gurbuz N, Ozpolat B. MicroRNA-based Targeted Therapeutics in Pancreatic Cancer. Anticancer Res. 2019;39(2):529-32.

Li Y, Sarkar FH. MicroRNA Targeted Therapeutic Approach for Pancreatic Cancer. Int J Biol Sci. 2016;12(3):326-37.

Markopoulos GS, Roupakia E, Tokamani M, Chavdoula E, Hatziapostolou M, Polytarchou C, Marcu KB, Papavassiliou AG, Sandaltzopoulos R, Kolettas E. A step-by-step microRNA guide to cancer development and metastasis. Cell Oncol (Dordr). 2017;40(4):303-39.

Rusek AM, Abba M, Eljaszewicz A, Moniuszko M, Niklinski J, Allgayer H. MicroRNA modulators of epigenetic regulation, the tumor microenvironment and the immune system in lung cancer. Mol Cancer. 2015;14:34.

Wang J, Chen J, Sen S. MicroRNA as Biomarkers and Diagnostics. J Cell Physiol. 2016;231(1):25-30.

Xu J, Li J, Zheng TH, Bai L, Liu ZJ. MicroRNAs in the Occurrence and Development of Primary Hepatocellular Carcinoma. Adv Clin Exp Med. 2016;25(5):971-5.

Sui J, Yang RS, Xu SY, Zhang YQ, Li CY, Yang S, Yin LH, Pu YP, Liang GY. Comprehensive analysis of aberrantly expressed microRNA profiles reveals potential biomarkers of human lung adenocarcinoma progression. Oncol Rep. 2017;38(4):2453-63.

Fan Y, Bian X, Qian P, Wen J, Yan P, Luo Y, Wu J, Zhang Q. miRNA30a3p inhibits metastasis and enhances radiosensitivity in esophageal carcinoma by targeting insulinlike growth factor 1 receptor. Mol Med Rep. 2019;20(1):81-94.

Li D, Yang M, Liao A, Zeng B, Liu D, Yao Y, Hu G, Chen X, Feng Z, Du Y, Zhou Y, He J, Nie Y. Linc00483 as ceRNA regulates proliferation and apoptosis through activating MAPKs in gastric cancer. J Cell Mol Med. 2018.

Xing M. Molecular pathogenesis and mechanisms of thyroid cancer. Nat Rev Cancer. 2013;13(3):184-99.

Nikiforov YE. Thyroid carcinoma: molecular pathways and therapeutic targets. Mod Pathol. 2008;21(Suppl 2):S37-43.

Peng Y, Li C, Luo DC, Ding JW, Zhang W, Pan G. Expression profile and clinical significance of microRNAs in papillary thyroid carcinoma. Molecules. 2014;19(8):11586-99.

Riesco-Eizaguirre G, Wert-Lamas L, Perales-Paton J, Sastre-Perona A, Fernandez LP, Santisteban P. The miR-146b-3p/PAX8/NIS Regulatory Circuit Modulates the Differentiation Phenotype and Function of Thyroid Cells during Carcinogenesis. Cancer Res. 2015;75(19):4119-30.

Lu Z, Sheng J, Zhang Y, Deng J, Li Y, Lu A, Zhang J, Yu H, Zhang M, Xiong Z, Yan H, Diplas BH, Lu Y, Liu B. Clonality analysis of multifocal papillary thyroid carcinoma by using genetic profiles. J Pathol. 2016;239(1):72-83.

Kim KJ, Kim SM, Lee YS, Chung WY, Chang HS, Park CS. Prognostic significance of tumor multifocality in papillary thyroid carcinoma and its relationship with primary tumor size: a retrospective study of 2,309 consecutive patients. Ann Surg Oncol. 2015;22(1):125-31.

Kim HJ, Sohn SY, Jang HW, Kim SW, Chung JH. Multifocality, but not bilaterality, is a predictor of disease recurrence/persistence of papillary thyroid carcinoma. World J Surg. 2013;37(2):376-84.

Pacini F, Schlumberger M, Dralle H, Elisei R, Smit JW, Wiersinga W. European consensus for the management of patients with differentiated thyroid carcinoma of the follicular epithelium. Eur J Endocrinol. 2006;154(6):787-803.

Cooper DS, Doherty GM, Haugen BR, Kloos RT, Lee SL, Mandel SJ, Mazzaferri EL, McIver B, Pacini F, Schlumberger M, Sherman SI, Steward DL, Tuttle RM. Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid. 2009;19(11):1167-214.

Ozdemir D, Ersoy R, Cuhaci N, Arpaci D, Ersoy EP, Korukluoglu B, Guler G, Cakir B. Classical and follicular variant papillary thyroid carcinoma: comparison of clinical, ultrasonographical, cytological, and histopathological features in 444 patients. Endocr Pathol. 2011;22(2):58-65.

Shi X, Liu R, Basolo F, Giannini R, Shen X, Teng D, Guan H, Shan Z, Teng W, Musholt TJ, Al-Kuraya K, Fugazzola L, Colombo C, Kebebew E, Jarzab B, Czarniecka A, Bendlova B, Sykorova V, Sobrinho-Simoes M, Soares P, Shong YK, Kim TY, Cheng S, Asa SL, Viola D, Elisei R, Yip L, Mian C, Vianello F, Wang Y, Zhao S, Oler G, Cerutti JM, Puxeddu E, Qu S, Wei Q, Xu H, O'Neill CJ, Sywak MS, Clifton-Bligh R, Lam AK, Riesco-Eizaguirre G, Santisteban P, Yu H, Tallini G, Holt EH, Vasko V, Xing M. Differential Clinicopathological Risk and Prognosis of Major Papillary Thyroid Cancer Variants. J Clin Endocrinol Metab. 2016;101(1):264-74.

Agrawal N, Akbani R, Aksoy BA, Ally A, Arachchi H, Asa SL, Auman JT, Balasundaram M, Balu S, S.B. B, Behera M, Bernard B. Integrated genomic characterization of papillary thyroid carcinoma. Cell. 2014;159(3):676-90.

Asa SL, Giordano TJ, LiVolsi VA. Implications of the TCGA genomic characterization of papillary thyroid carcinoma for thyroid pathology: does follicular variant papillary thyroid carcinoma exist? Thyroid. 2015;25(1):1-2.

Lee H, Park CS, Deftereos G, Morihara J, Stern JE, Hawes SE, Swisher E, Kiviat NB, Feng Q. MicroRNA expression in ovarian carcinoma and its correlation with clinicopathological features. World J Surg Oncol. 2012;10:174.

Daugaard I, Veno MT, Yan Y, Kjeldsen TE, Lamy P, Hager H, Kjems J, Hansen LL. Small RNA sequencing reveals metastasis-related microRNAs in lung adenocarcinoma. Oncotarget. 2017;8(16):27047-61.

Heinzelmann J, Arndt M, Pleyers R, Fehlmann T, Hoelters S, Zeuschner P, Vogt A, Pryalukhin A, Schaeffeler E, Bohle RM, Gajda M, Janssen M, Stoeckle M, Junker K. 4-miRNA Score Predicts the Individual Metastatic Risk of Renal Cell Carcinoma Patients. Ann Surg Oncol. 2019;26(11):3765-73.

Downloads

Published

2020-03-24

How to Cite

1.
Todorović L, Mandušić V, Vučetić Tadić B, Živaljević V, Paunović I, Stanojević B. Altered expression of microRNA-30a-3p in papillary thyroid cancer and its association with clinicopathological characteristics. Arch Biol Sci [Internet]. 2020Mar.24 [cited 2024Apr.20];72(1):31-6. Available from: https://serbiosoc.org.rs/arch/index.php/abs/article/view/4688

Issue

Vol. 72 No. 1 (2020)

Section

Articles

License

Authors grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution 4.0 International License that allows others to share the work with an acknowledgment of the work’s authorship and initial publication in this journal.