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Anaplastic Thyroid Cancer Cells Induce the Release of Mitochondrial Extracellular DNA Traps by Viable Neutrophils

Cristinziano, Leonardo, Modestino, Luca, Loffredo, Stefania, Varricchi, Gilda, Braile, Mariantonia, Ferrara, Anne Lise, de Paulis, Amato, Antonelli, Alessandro, Marone, Gianni, Galdiero, Maria Rosaria·2020·The Journal of Immunology
DOI 10.4049/jimmunol.1900543
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Abstract

Neutrophils are key effector cells that orchestrate inflammatory responses in the tumor microenvironment. Although neutrophil extracellular DNA traps (NETs) entrap and kill pathogens, they also contribute to chronic inflammation and cancer progression. Thyroid cancer (TC) is the most frequently occurring cancer of the endocrine system, accounting for 70% of deaths due to endocrine tumors. Although anaplastic TC (ATC) is rare among TCs, it is highly lethal. We demonstrated in a recent study that tumor-infiltrating neutrophil density correlated with TC size. Moreover, TC-derived soluble mediators modulate the human neutrophil phenotype. Our study aimed to investigate the involvement of NETs in human TC. Highly purified neutrophils from healthy donors were primed in vitro with a papillary TC or ATC cell line conditioned medium (CM) or with a normal thyroid CM as control. NET release was quantified using a High-Content Imaging System. Neutrophil viability was assessed by flow cytometry. Fluorescence microscopy, flow cytometry, and PCR were performed to determine the mitochondrial origin of ATC-induced NETs. ATC CM–primed neutrophils were cocultured with ATC cells to determine the effects exerted by NETs on cell proliferation. ATC CM induce NET release, whereas papillary TC or normal thyroid CM did not. ATC CM–induced NET production occurred in a reactive oxygen species–dependent and cell death–independent manner and was associated with mitochondrial reactive oxygen species production; the NETs contained mitochondrial DNA. ATC CM–primed neutrophils promoted ATC cell proliferation in a NET-dependent manner.

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Metadata

Authors
Cristinziano, L., Modestino, L., Loffredo, S., Varricchi, G., Braile, M., Ferrara, A. L., de Paulis, A., Antonelli, A., Marone, G., & Galdiero, M. R.
Affiliations
  • Department of Translational Medical Sciences, University of Naples Federico II , 80131 Naples ,
  • Department of Clinical and Experimental Medicine, University of Pisa , 56126 Pisa ,
ORCID
Venue
The Journal of Immunology
Publisher
Oxford University Press (OUP)
Published
2020-03-01
Volume
204
Issue
5
Pages
1362-1372
ISSN
  • 0022-1767
  • 1550-6606
DOI
10.4049/jimmunol.1900543
Cited by
83
References
6
Language
en
Licence
academic.oup.com/pages/standard-publication-reuse-rights (vor)

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