Vol. 70 No. 2 (2024), EDITORIALS

Vol. 70 No. 2 (2024)

Possibilities for Differential Diagnosis of Thyroid Follicular Neoplasia by Evaluation of Small Noncoding RNA

EDITORIALS

https://doi.org/10.37469/0507-3758-2024-70-2-189-201

Published 06.05.2024

Ioannina A. Bandyk

Algimed-Techno LLC, Minsk, the Republic of Belarus

https://orcid.org/0000-0001-6148-6778

Margarita S. Knyazeva

N.N. Petrov National Medicine Research Center of Oncology, St. Petersburg, the Russian Federation

https://orcid.org/0000-0002-2079-5061

Alexander Yu. Garanin

N.N. Petrov National Medicine Research Center of Oncology, St. Petersburg, the Russian Federation

https://orcid.org/0000-0002-8313-3794

Konstantin E. Katsuba

N.N. Petrov National Medicine Research Center of Oncology, St. Petersburg, the Russian Federation

https://orcid.org/0000-0002-7373-5206

Lidia M. Zabegina

N.N. Petrov National Medicine Research Center of Oncology, St. Petersburg, the Russian Federation

https://orcid.org/0000-0003-0827-1641

Tatyana V. Sharonova

N.N. Petrov National Medicine Research Center of Oncology, St. Petersburg, the Russian Federation

https://orcid.org/0000-0002-5372-1253

Andrey V. Shalaev

N.N. Petrov National Medicine Research Center of Oncology, St. Petersburg, the Russian Federation

https://orcid.org/0000-0002-6148-6994

Ekaterina Ya. Grinkova

N.N. Petrov National Medicine Research Center of Oncology, St. Petersburg, the Russian Federation

https://orcid.org/0009-0002-7238-5870

Daniil S. Plevako

N.N. Petrov National Medicine Research Center of Oncology, St. Petersburg, the Russian Federation

https://orcid.org/0000-0002-5657-130X

Анна Олеговна Нюганен

ФГБУ «НМИЦ онкологии им. Н.Н Петрова»

https://orcid.org/0000-0003-2685-5093

Ирина Андреевна Полковникова

СПб ГБУЗ «Городская больница № 40»

https://orcid.org/0000-0002-9178-8512

Анна Сергеевна Артемьева

ФГБУ «НМИЦ онкологии им. Н.Н Петрова»

https://orcid.org/0000-0002-2948-397X

Светлана Вячеславовна Апалько

СПб ГБУЗ «Городская больница № 40»

https://orcid.org/0000-0002-3853-4185

Сергей Григорьевич Щербак

СПб ГБУЗ «Городская больница № 40»

https://orcid.org/0000-0001-5047-2792

Анастасия Валерьевна Малек

ФГБУ «НМИЦ онкологии им. Н.Н Петрова»

https://orcid.org/0000-0001-5334-7292

pdf (Русский)

Keywords

ollicular thyroid cancer
preoperative diagnosis
next generation sequencing
microRNA
piwiRNA

How to Cite

Bandyk , I. A., Knyazeva , M. S., Garanin , A. Y., Katsuba , K. E., Zabegina, L. M., Sharonova , T. V., Shalaev , A. V., Grinkova , E. Y., Plevako , D. S., Нюганен, А. О., Полковникова, И. А., Артемьева, А. С., Апалько, С. В., Щербак, С. Г., & Малек, А. В. (2024). Possibilities for Differential Diagnosis of Thyroid Follicular Neoplasia by Evaluation of Small Noncoding RNA. Voprosy Onkologii, 70(2), 189–201. https://doi.org/10.37469/0507-3758-2024-70-2-189-201

Abstract

Introduction. The preoperative differential diagnosis of follicular thyroid nodules is not a trivial issue due to the absence of objective signs of malignancy. This is stimulating efforts to find molecular markers of follicular cancer and to develop diagnostic test systems. Small regulatory RNAs are a large group of molecules that perform different biological functions, but have a similar biochemical structure. Quantitative analysis of different members of this group can be performed simultaneously using identical technology. This determines the possibility of a comprehensive assessment of the cellular biology of the samples analysed and the development of new diagnostic criteria. The purpose of the study was a comparative analysis of small RNAs expression profile in the samples of follicular thyroid cancer and follicular adenoma of the thyroid gland.

Materials and methods. The study included tissue samples of follicular carcinoma (FC, n = 12) and benign follicular adenoma (FA, n = 12) of the thyroid gland obtained after thyroidectomy and histological examination. Analysis of the expression profile of short RNAs was carried out using next generation sequencing.

Results. The expression (concentration) of transfer RNAs (tRNAs), small nuclear RNAs (snRNAs), and a large group of unclassified molecules (miscRNA) is increased in FC compared to FA, but the diagnostic potential of individual molecules is relatively low. The total concentrations of microRNA molecules (miRNA) turned out to be comparable in the FC and FA groups; analysis of «reciprocal pairs» of miRNA markers allowed to differentiate FC and FA with a high degree of probability (AUC: 0.94-0.98). The total number of piwiRNA molecules was slightly higher in FC samples compared to FA; analysis of «reciprocal pairs» of piwiRNA marker allows us to reliably differentiate FC and FA (AUC: 1.00).

Conclusion. Analysis of the concentration of marker miRNA and piwiRNA in fine-needle aspiration biopsy material appears to be a promising method for additional diagnosis of thyroid nodules with a follicular structure.

https://doi.org/10.37469/0507-3758-2024-70-2-189-201

pdf (Русский)

References

Воробьев С.Л. Морфологическая диагностика заболеваний щитовидной железы: (цитология для патологов, патология для цитологов). Санкт-Петербург. Коста. 2014.

[Vorobyov S.L. Morphological diagnostics of thyroid diseases: (cytology for pathologists, pathology for cytologists). Saint Petersburg. Kosta. 2014. (In Rus)].

Bongiovanni M., Spitale A., Faquin W.C., et al. The Bethesda system for reporting thyroid cytopathology: a meta-analysis. Acta Cytol. 2012; 56(4): 333-9.-DOI: https://doi.org/10.1159/000339959.

Cibas ES, Ali SZ. The 2017 Bethesda system for reporting thyroid cytopathology. Thyroid. 2017; 27(11): 1341-1346.-DOI: https://doi.org/10.1089/thy.2017.0500.

Ali S.Z., Baloch Z.W., Cochand-Priollet B., et al. The 2023 Bethesda system for reporting thyroid cytopathology. Thyroid. 2023; 33(9): 1039-1044.-DOI: https://doi.org/10.1089/thy.2023.0141.

Li W., Song Q., Lan Y., et al. The value of sonography in distinguishing follicular thyroid carcinoma from adenoma. Cancer Manag Res. 2021; 13: 3991-4002.-DOI: https://doi.org/10.2147/CMAR.S307166.

Kuo T.C., Wu M.H., Chen K.Y., et al. Ultrasonographic features for differentiating follicular thyroid carcinoma and follicular adenoma. Asian J Surg. 2020; 43(1): 339-346.-DOI: https://doi.org/10.1016/j.asjsur.2019.04.016.

Lin A.C., Liu Z., Lee J., et al. Generating a multimodal artificial intelligence model to differentiate benign and malignant follicular neoplasms of the thyroid: A proof-of-concept study. Surgery. 2024; 175(1): 121-127.-DOI: https://doi.org/10.1016/j.surg.2023.06.053.

Daniels G.H. Follicular thyroid carcinoma: a perspective. Thyroid. 2018; 28(10): 1229-1242.-DOI: https://doi.org/10.1089/thy.2018.0306.

Weber F., Shen L., Aldred M.A., et al. Genetic classification of benign and malignant thyroid follicular neoplasia based on a three-gene combination. J Clin Endocrinol Metab. 2005; 90(5): 2512-21-DOI: https://doi.org/10.1210/jc.2004-2028.

Borup R., Rossing M., Henao R., et al. Molecular signatures of thyroid follicular neoplasia. Endocr Relat Cancer. 2010; 17(3): 691-708.-DOI: https://doi.org/10.1677/ERC-09-0288.

Lassalle S., Hofman V., Ilie M., et al. Can the microRNA signature distinguish between thyroid tumors of uncertain malignant potential and other well-differentiated tumors of the thyroid gland? Endocr Relat Cancer. 2011; 18(5): 579-94.-DOI: https://doi.org/10.1530/ERC-10-0283.

Nikiforova M.N., Wald A.I., Roy S., et al. Targeted next-generation sequencing panel (ThyroSeq) for detection of mutations in thyroid cancer. J Clin Endocrinol Metab. 2013; 98(11): E1852-60.-DOI: https://doi.org/10.1210/jc.2013-2292.

Stokowy T., Wojtas B., Jarzab B., et al. Two-miRNA classifiers differentiate mutation-negative follicular thyroid carcinomas and follicular thyroid adenomas in fine needle aspirations with high specificity. Endocrine. 2016; 54(2): 440-447.-DOI: https://doi.org/10.1007/s12020-016-1021-7.

Dom G., Frank S., Floor S., et al. Thyroid follicular adenomas and carcinomas: molecular profiling provides evidence for a continuous evolution. Oncotarget. 2017; 9(12): 10343-10359.-DOI: https://doi.org/10.18632/oncotarget.23130.

Wojtas B., Pfeifer A., Oczko-Wojciechowska M., Krajewska J, et al. Gene expression (mRNA) markers for differentiating between malignant and benign follicular thyroid tumours. Int J Mol Sci. 2017; 18(6): 1184.-DOI: https://doi.org/10.3390/ijms18061184.

Jung C.K., Kim Y., Jeon S., et al. Clinical utility of EZH1 mutations in the diagnosis of follicular-patterned thyroid tumors. Hum Pathol. 2018; 81: 9-17.-DOI: https://doi.org/10.1016/j.humpath.2018.04.018.

Rossing M., Borup R., Henao R., et al. Down-regulation of microRNAs controlling tumourigenic factors in follicular thyroid carcinoma. J Mol Endocrinol. 2012; 48(1): 11-23.-DOI: https://doi.org/10.1530/JME-11-0039.

Duan H., Liu X., Ren X., et al. Mutation profiles of follicular thyroid tumors by targeted sequencing. Diagn Pathol. 2019; 14(1): 39.-DOI: https://doi.org/10.1186/s13000-019-0817-1.

Knyazeva M., Korobkina E., Karizky A., et al. Reciprocal dysregulation of MiR-146b and MiR-451 contributes in malignant phenotype of follicular thyroid tumor. Int J Mol Sci. 2020; 21(17): 5950.-DOI: https://doi.org/10.3390/ijms21175950.

Hossain M.A., Asa T.A., Rahman M.M., et al. Network-based genetic profiling reveals cellular pathway differences between follicular thyroid carcinoma and follicular thyroid adenoma. Int J Environ Res Public Health. 2020; 17(4): 1373.-DOI: https://doi.org/10.3390/ijerph17041373.

Paulsson J.O., Rafati N., DiLorenzo S., et al. Whole-genome sequencing of follicular thyroid carcinomas reveal recurrent mutations in microRNA processing subunit DGCR8. J Clin Endocrinol Metab. 2021; 106(11): 3265-3282.-DOI: https://doi.org/10.1210/clinem/dgab471.

Титов С.Е., Лукьянов С.А., Сергийко С.В., et al. Проблемы диагностики фолликулярного рака щитовидной железы. Опухоли головы и шеи. 2023; 13(3): 10-23.-DOI: https://doi.org/10.17650/2222-1468-2023-13-3-10-23.

[Titov S.E., Lukyanov S.A., Sergiyko S.V., et al. Problems of follicular thyroid carcinoma diagnostics. Head and Neck Tumors (HNT). 2023; 13(3): 10-23.-DOI: https://doi.org/10.17650/2222-1468-2023-13-3-10-23. (In Rus)].

Titov S.E., Ivanov M.K., Demenkov P.S., et al. Combined quantitation of HMGA2 mRNA, microRNAs, and mitochondrial-DNA content enables the identification and typing of thyroid tumors in fine-needle aspiration smears. BMC Cancer. 2019; 19(1): 1010.

Kniazeva M., Zabegina L., Shalaev A., et al. NOVAprep-miR-Cervix: new method for evaluation of cervical dysplasia severity based on analysis of six miRNAs. Int J Mol Sci. 2023; 24(11): 9114.-DOI: https://doi.org/10.3390/ijms24119114.

Wingett S.W., Andrews S. FastQ Screen: A tool for multi-genome mapping and quality control. F1000Res. 2018; 7: 1338.-DOI: https://doi.org/10.12688/f1000research.15931.2.

Fehlmann T., Kern F., Laham O., et al. miRMaster 2.0: multi-species non-coding RNA sequencing analyses at scale. Nucleic Acids Res. 2021; 49(W1): W397-W408.-DOI: https://doi.org/10.1093/nar/gkab268.

Kozomara A., Birgaoanu M., Griffiths-Jones S. miRBase: from microRNA sequences to function. Nucleic Acids Res. 2019; 47(D1): D155-D162.-DOI: https://doi.org/10.1093/nar/gky1141.

Kozomara A., Griffiths-Jones S. miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res. 2014; 42(Database issue): D68-73.-DOI: https://doi.org/10.1093/nar/gkt1181.

Yates A.D., Achuthan P., Akanni W., et al. Ensembl 2020. Nucleic Acids Res. 2020; 48(D1): D682-D688.-DOI: https://doi.org/10.1093/nar/gkz966.

Sweeney B.A., Petrov A.I., Ribas C.E., et al. RNAcentral Consortium. RNAcentral 2021: secondary structure integration, improved sequence search and new member databases. Nucleic Acids Res. 2021; 49(D1): D212-D220.-DOI: https://doi.org/10.1093/nar/gkaa921.

Thornlow B.P., Armstrong J., Holmes A.D., et al. Predicting transfer RNA gene activity from sequence and genome context. Genome Res. 2020; 30(1): 85-94.-DOI: https://doi.org/10.1101/gr.256164.119.

Zhao Y., Li H., Fang S., et al. NONCODE 2016: an informative and valuable data source of long non-coding RNAs. Nucleic Acids Res. 2016; 44(D1): D203-8.-DOI: https://doi.org/10.1093/nar/gkv1252.

Glažar P., Papavasileiou P., Rajewsky N. circBase: a database for circular RNAs. RNA. 2014; 20(11): 1666-70.-DOI: https://doi.org/10.1261/rna.043687.113.

Walter N.G. Are non-protein coding RNAs junk or treasure? An attempt to explain and reconcile opposing viewpoints of whether the human genome is mostly transcribed into non-functional or functional RNAs. Bioessays. 2024; 46(4): e2300201.-DOI: https://doi.org/10.1002/bies.202300201.

Palazzo A.F., Lee E.S. Non-coding RNA: what is functional and what is junk? Front Genet. 2015; 6.-DOI: https://doi.org/10.3389/fgene.2015.00002.

Valadkhan S., Gunawardane L.S. Role of small nuclear RNAs in eukaryotic gene expression. Essays Biochem. 2013; 54: 79-90.-DOI: https://doi.org/10.1042/bse0540079.

Pinkard O., McFarland S., Sweet T., Coller J. Quantitative tRNA-sequencing uncovers metazoan tissue-specific tRNA regulation. Nat Commun. 2020; 11(1): 4104.-DOI: https://doi.org/10.1038/s41467-020-17879-x.

Torres A.G. Enjoy the silence: nearly half of human tRNA genes are silent. Bioinform Biol Insights. 2019; 13: 1177932219868454.-DOI: https://doi.org/10.1177/1177932219868454.

Yu M., Lu B., Zhang J., et al. tRNA-derived RNA fragments in cancer: current status and future perspectives. J Hematol Oncol. 2020; 13(1): 121.-DOI: https://doi.org/10.1186/s13045-020-00955-6.

Ren D., Mo Y., Yang M., et al. Emerging roles of tRNA in cancer. Cancer Lett. 2023; 563: 216170.-DOI: https://doi.org/10.1016/j.canlet.2023.216170.

Ozata D.M., Gainetdinov I., Zoch A., et al. PIWI-interacting RNAs: small RNAs with big functions. Nat Rev Genet. 2019; 20(2): 89-108.-DOI: https://doi.org/10.1038/s41576-018-0073-3.

Yuan C., Qin H., Ponnusamy M., et al. PIWI‑interacting RNA in cancer: Molecular mechanisms and possible clinical implications (Review). Oncol Rep. 2021; 46(3): 209.-DOI: https://doi.org/10.3892/or.2021.8160.

Yao J., Xie M., Ma X., et al. PIWI-interacting RNAs in cancer: Biogenesis, function, and clinical significance. Front Oncol. 2022; 12: 965684.-DOI: https://doi.org/10.3389/fonc.2022.965684.

Zhang Z., Liu N. PIWI interacting RNA-13643 contributes to papillary thyroid cancer development through acting as a novel oncogene by facilitating PRMT1 mediated GLI1 methylation. Biochim Biophys Acta Gen Subj. 2023; 1867(11): 130453.-DOI: https://doi.org/10.1016/j.bbagen.2023.130453.

Chang Z., Ji G., Huang R., et al. PIWI-interacting RNAs piR-13643 and piR-21238 are promising diagnostic biomarkers of papillary thyroid carcinoma. Aging (Albany NY). 2020; 12(10): 9292-9310.-DOI: https://doi.org/10.18632/aging.103206.

This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

Most read articles by the same author(s)

Petr Vladimirovich Krivorotko, Yana Igorevna Bondarchuk, Alexander Valerievich Komyahov , Sergey Sergeevich Bagnenko, Elena Konstantinovna Zhiltsova, Antonina Viktorovna Chernaya , Vladislav Vladimirovich Semiglazov, Anna Sergeevna Artemyeva, Tengiz Tengizovich Tabagua, Larisa Pavlovna Gigolaeva, Alexander Sergeevich Emelyanov, Nikolay Sergeevich Amirov, Roman Sergeevich Pesotsky, Victoria Vladimirovna Mortada, Nestan Bekkeldievna Bekkeldieva, Sergey Sergeevich Yerechshenko, Konstantin Yurievich Zernov, Kirill Stanislavovich Nikolaev, Valery Evgenievich Levchenko, Daria Glebovna Ulrikh, Diana Arturovna Enaldieva, Alexey Mikhailovich Belyaev, Vladimir Fedorovich Semiglazov, Control of Resection Margins during Breast-Conserving and Oncoplastic Surgeries , Voprosy onkologii : Vol. 70 No. 1 (2024)
Leonid Kramynin, Margarita Motalkina , Larisa Filatova, Ilya Zyuzgin, Anna Artemyeva, Lymphomatoid papulosis in a patient with recurrent Hodgkin's lymphoma: a clinical case , Voprosy onkologii : Vol. 69 No. 3 (2023)
Asel Galimovna Kudaibergenova , Alexander Olegovich Ivantsov, Julia Dyusekovna Von, Ekaterina Sergeevna Artemyeva , Anna Sergeyevna Artemyeva , Development of Pathomorphology at the N.N. Petrov NMRC of Oncology. Dedicated to M.F. Glazunov , Voprosy onkologii : Vol. 69 No. 6 (2023)
Petr V. Krivorotko, Nikolay S. Amirov, Anna S. Artemyeva, Ekaterina A. Busko, Tengiz T. Tabagua, Alexander S. Emelyanov , Sergey S. Yereschenko , Roman S. Pesotsky, Viktoriia V. Mortada, Konstantin Yu. Zernov, Elena K. Ziltsova, Larisa P. Gigolaeva, Kirill S. Nikolaev, Alexander V. Komyahov, Yana I. Bondarchuk, Diana A. Enaldieva, Nestan Bekkeldiyeva, Daria Ulrikh, Sergey N. Novikov, Pavel I. Krzhivitskiy, Zhanna V. Bryantseva, Irina A. Akulova, Roman V. Donskikh, Vladimir F. Semiglazov, Aleksey M. Belyaev, Treatment Outcomes Evaluation in Breast Cancer Patients with a Pathological Complete Response after Neoadjuvant Systemic Therapy Depending on Different Types of Local Treatment , Voprosy onkologii : Vol. 70 No. 2 (2024)
Valery Anatolyevich Alexandrov, Yuliya Gennadievna Zmitrichenko, Alexander Nikolaevich Stukov, Natalia Nikolaevna Haritonova, Olesya Alexandrovna Belyaeva, Dmitry Nikolaevich Suslov , Anna Olegovna Nyuganen, Grigory Viktorovich Tochilnikov, Dilorom Khamidovna Latipova, Tatiana Yuryevna Semiglazova, Comparative Activity of Chlonisol and Lomustinе in Mice with Intraorbital Transplant of Ehrlich Carcinoma , Voprosy onkologii : Vol. 70 No. 2 (2024)