Shared and unique metabolic features of the malignant and benign thyroid lesions determined with use of 1H HR MAS NMR spectroscopy

Agnieszka Skorupa,Małgorzata Oczko-Wojciechowska,Maria Sokół,Dagmara Rusinek,Ewa Chmielik,Małgorzata Kowalska,Barbara Jarząb,Tomasz Tyszkiewicz,Mateusz Ciszek,Agnieszka Czarniecka,Łukasz Boguszewicz,Aneta Kluczewska-Gałka

doi:10.1038/s41598-020-79565-8

Agnieszka Skorupa, Małgorzata Oczko-Wojciechowska + Show 10 more

Open Access

https://doi.org/10.1038/s41598-020-79565-8

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Abstract

The purpose of this work was to investigate the distinct and common metabolic features of the malignant and benign thyroid lesions in reference to the non-transformed tissue from the contralateral gland (chronic thyroiditis and colloid goiter). 1H HR MAS NMR spectra of 38 malignant lesions, 32 benign lesions and 112 samples from the non-tumoral tissue (32 from chronic thyroiditis and 80 samples from colloid goiter) were subjected both to multivariate and univariate analysis. The increased succinate, glutamine, glutathione, serine/cysteine, ascorbate, lactate, taurine, threonine, glycine, phosphocholine/glycerophosphocholine and decreased lipids were found in both lesion types in comparison to either colloid goiter or chronic thyroiditis. The elevated glutamate and choline, and reduced citrate and glucose were additionally evident in these lesions in reference to goiter, while the increased myo-inositol—in comparison to thyroiditis. The malignant lesions were characterized by the higher alanine and lysine levels than colloid goiter and thyroiditis, while scyllo-inositol was uniquely increased in the benign lesions (not in cancer) in comparison to both non-tumoral tissue types. Moreover, the benign lesions presented with the unique increase of choline in reference to thyroiditis (not observed in the cancerous tissue). The metabolic heterogeneity of the non-tumoral tissue should be considered in the analysis of metabolic reprogramming in the thyroid lesions.

Highlights

Thyroid nodules are defined as discrete lesions within the thyroid gland
The analysis of the HR MAS 1H NMR spectra revealed the metabolic diversity between colloid goiter and chronic thyroiditis—two benign conditions frequently encountered in the non-tumoral tissue in patients diagnosed with thyroid lesions
Glutamine, glutathione, serine/cysteine, ascorbate, lactate, taurine, threonine, glycine, phosphocholine/glycerophosphocholine and decreased lipids were found in both lesion types in comparison to either colloid goiter or chronic thyroiditis

Summary

Introduction

Thyroid nodules are defined as discrete lesions within the thyroid gland. They are very common in general population: physical examination allows their detection in 4–7% adults, while their prevalence is estimated at 19–67% using ultrasonography[1,2,3]. Some of the most striking changes of tumor cellular bioenergetics, like enhanced aerobic glycolysis, glutaminolysis, altered TCA cycle and fatty acids metabolism in thyroid cancer have already been proved using NMR and mass s pectrometry[9,10,11,12,13,14,15,16] Since both benign and malignant thyroid lesions contain proliferating cells, some of the biochemical processes leading to the biomass increase may be shared between these types of tissue. Identification of their unique metabolic features is important for a better understanding of biochemical reprogramming in the thyroid nodules. We hypothesized that the presence of inflammatory cell infiltrate within the control tissue could be reflected in 1H HR MAS NMR spectra and should be taken into account in the analysis of metabolic reprogramming in the thyroid lesions

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