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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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Research works printed but not linked: 66

  1. Jaillon, 2013, Neutrophils in innate and adaptive immunity, Semin. Immunopathol., 35, 377, 10.1007/s00281-013-0374-8 · DOI
  2. Tecchio, 2013, On the cytokines produced by human neutrophils in tumors, Semin. Cancer Biol., 23, 159, 10.1016/j.semcancer.2013.02.004 · DOI
  3. Cassatella, 2009, Never underestimate the power of a neutrophil, Immunity, 31, 698, 10.1016/j.immuni.2009.10.003 · DOI
  4. Bonavita, 2015, Phagocytes as corrupted policemen in cancer-related inflammation, Adv. Cancer Res., 128, 141, 10.1016/bs.acr.2015.04.013 · DOI
  5. Galdiero, 2018, Roles of neutrophils in cancer growth and progression, J. Leukoc. Biol., 103, 457, 10.1002/JLB.3MR0717-292R · DOI
  6. Mantovani, 2011, Neutrophils in the activation and regulation of innate and adaptive immunity, Nat. Rev. Immunol., 11, 519, 10.1038/nri3024 · DOI
  7. Donskov, 2013, Immunomonitoring and prognostic relevance of neutrophils in clinical trials, Semin. Cancer Biol., 23, 200, 10.1016/j.semcancer.2013.02.001 · DOI
  8. Jensen, 2009, Presence of intratumoral neutrophils is an independent prognostic factor in localized renal cell carcinoma, J. Clin. Oncol., 27, 4709, 10.1200/JCO.2008.18.9498 · DOI
  9. Galdiero, 2016, Occurrence and significance of tumor-associated neutrophils in patients with colorectal cancer, 446
  10. Eruslanov, 2014, Tumor-associated neutrophils stimulate T cell responses in early-stage human lung cancer, J. Clin. Invest., 124, 5466, 10.1172/JCI77053 · DOI
  11. Granot, 2011, Tumor entrained neutrophils inhibit seeding in the premetastatic lung, Cancer Cell, 20, 300, 10.1016/j.ccr.2011.08.012 · DOI · Paper page
  12. Loffredo, 2017, Group V secreted phospholipase A2 induces the release of proangiogenic and antiangiogenic factors by human neutrophils, Front. Immunol., 8, 443, 10.3389/fimmu.2017.00443 · DOI
  13. Queen, 2005, Breast cancer cells stimulate neutrophils to produce oncostatin M: potential implications for tumor progression, Cancer Res., 65, 8896, 10.1158/0008-5472.CAN-05-1734 · DOI
  14. Houghton, 2010, Neutrophil elastase-mediated degradation of IRS-1 accelerates lung tumor growth, Nat. Med., 16, 219, 10.1038/nm.2084 · DOI
  15. Jablonska, 2010, Neutrophils responsive to endogenous IFN-beta regulate tumor angiogenesis and growth in a mouse tumor model, J. Clin. Invest., 120, 1151, 10.1172/JCI37223 · DOI
  16. Brinkmann, 2004, Neutrophil extracellular traps kill bacteria, Science., 303, 1532, 10.1126/science.1092385 · DOI · Paper page
  17. Jaillon, 2007, The humoral pattern recognition receptor PTX3 is stored in neutrophil granules and localizes in extracellular traps, J. Exp. Med., 204, 793, 10.1084/jem.20061301 · DOI
  18. Brinkmann, 2012, Neutrophil extracellular traps: is immunity the second function of chromatin?, J. Cell Biol., 198, 773, 10.1083/jcb.201203170 · DOI · Paper page
  19. Saitoh, 2012, Neutrophil extracellular traps mediate a host defense response to human immunodeficiency virus-1, Cell Host Microbe, 12, 109, 10.1016/j.chom.2012.05.015 · DOI
  20. Varricchi, 2017, Are mast cells MASTers in cancer?, Front. Immunol., 8, 424, 10.3389/fimmu.2017.00424 · DOI
  21. Yousefi, 2016, NETosis - does it really represent nature’s “suicide bomber”?, Front. Immunol., 7, 328, 10.3389/fimmu.2016.00328 · DOI
  22. Gupta, 2005, Induction of neutrophil extracellular DNA lattices by placental microparticles and IL-8 and their presence in preeclampsia, Hum. Immunol., 66, 1146, 10.1016/j.humimm.2005.11.003 · DOI
  23. Gupta, 2010, Activated endothelial cells induce neutrophil extracellular traps and are susceptible to NETosis-mediated cell death, FEBS Lett., 584, 3193, 10.1016/j.febslet.2010.06.006 · DOI
  24. Berger-Achituv, 2013, A proposed role for neutrophil extracellular traps in cancer immunoediting, Front. Immunol., 4, 48, 10.3389/fimmu.2013.00048 · DOI
  25. Davies, 2014, Current thyroid cancer trends in the United States, JAMA Otolaryngol. Head Neck Surg., 140, 317, 10.1001/jamaoto.2014.1 · DOI
  26. Carling, 2014, Thyroid cancer, Annu. Rev. Med., 65, 125, 10.1146/annurev-med-061512-105739 · DOI
  27. Lim, 2017, Trends in thyroid cancer incidence and mortality in the United States, 1974-2013, JAMA, 317, 1338, 10.1001/jama.2017.2719 · DOI · Paper page
  28. Pstrąg, 2018, Thyroid cancers of follicular origin in a genomic light: in-depth overview of common and unique molecular marker candidates, Mol. Cancer, 17, 116, 10.1186/s12943-018-0866-1 · DOI
  29. Salehian, 2019, Clinical trials in management of anaplastic thyroid carcinoma; progressions and set backs: a systematic review, Int. J. Endocrinol. Metab., 17
  30. Nabhan, 2017, Thyroid nodules and cancer management guidelines: comparisons and controversies, Endocr. Relat. Cancer, 24, R13, 10.1530/ERC-16-0432 · DOI
  31. Gobert, 2009, Regulatory T cells recruited through CCL22/CCR4 are selectively activated in lymphoid infiltrates surrounding primary breast tumors and lead to an adverse clinical outcome, Cancer Res., 69, 2000, 10.1158/0008-5472.CAN-08-2360 · DOI · Paper page
  32. Antonelli, 2010, CXCL9 and CXCL11 chemokines modulation by peroxisome proliferator-activated receptor-alpha agonists secretion in Graves’ and normal thyrocytes, J. Clin. Endocrinol. Metab., 95, E413, 10.1210/jc.2010-0923 · DOI
  33. Muzio, 1994, Interleukin-13 induces the production of interleukin-1 receptor antagonist (IL-1ra) and the expression of the mRNA for the intracellular (keratinocyte) form of IL-1ra in human myelomonocytic cells, Blood, 83, 1738, 10.1182/blood.V83.7.1738.1738 · DOI
  34. Calzetti, 2017, The importance of being “pure” neutrophils, 352
  35. Borriello, 2017, GM-CSF and IL-3 modulate human monocyte TNF-α production and renewal in in vitro models of trained immunity, Front. Immunol., 7, 680, 10.3389/fimmu.2016.00680 · DOI
  36. Gupta, 2018, A high-throughput real-time imaging technique to quantify NETosis and distinguish mechanisms of cell death in human neutrophils, J. Immunol., 200, 869, 10.4049/jimmunol.1700905 · DOI
  37. Amini, 2018, Neutrophil extracellular trap formation requires OPA1-dependent glycolytic ATP production, Nat. Commun., 9, 2958, 10.1038/s41467-018-05387-y · DOI · Paper page
  38. Yousefi, 2008, Catapult-like release of mitochondrial DNA by eosinophils contributes to antibacterial defense, Nat. Med., 14, 949, 10.1038/nm.1855 · DOI · Paper page
  39. Van Avondt, 2016, Signal inhibitory receptor on leukocytes-1 limits the formation of neutrophil extracellular traps, but preserves intracellular bacterial killing, J. Immunol., 196, 3686, 10.4049/jimmunol.1501650 · DOI
  40. Sim, 2005, NADPH oxidase-derived reactive oxygen species-mediated activation of ERK1/2 is required for apoptosis of human neutrophils induced by Entamoeba histolytica, J. Immunol., 174, 4279, 10.4049/jimmunol.174.7.4279 · DOI
  41. Rotondi, 2013, CXCL8 in thyroid disease: from basic notions to potential applications in clinical practice, Cytokine Growth Factor Rev., 24, 539, 10.1016/j.cytogfr.2013.08.001 · DOI
  42. Melillo, 2010, Mast cells have a protumorigenic role in human thyroid cancer, Oncogene, 29, 6203, 10.1038/onc.2010.348 · DOI
  43. Liu, 2016, The CXCL8-CXCR1/2 pathways in cancer, Cytokine Growth Factor Rev., 31, 61, 10.1016/j.cytogfr.2016.08.002 · DOI
  44. Galdiero, 2016, The immune network in thyroid cancer, OncoImmunology, 5, 10.1080/2162402X.2016.1168556 · DOI
  45. Ley, 2018, Neutrophils: new insights and open questions, Sci. Immunol., 3, 10.1126/sciimmunol.aat4579 · DOI
  46. Nikiforov, 2011, Molecular genetics and diagnosis of thyroid cancer, Nat. Rev. Endocrinol., 7, 569, 10.1038/nrendo.2011.142 · DOI
  47. Cunha, 2014, The role of the inflammatory microenvironment in thyroid carcinogenesis, Endocr. Relat. Cancer, 21, R85, 10.1530/ERC-13-0431 · DOI
  48. Fallahi, 2018, The paramount role of cytokines and chemokines in papillary thyroid cancer: a review and experimental results, Immunol. Res., 66, 710, 10.1007/s12026-018-9056-x · DOI
  49. Saiselet, 2012, Thyroid cancer cell lines: an overview, Front. Endocrinol. (Lausanne), 3, 133, 10.3389/fendo.2012.00133 · DOI
  50. Morrison, 2015, Characterization of thyroid cancer cell lines in murine orthotopic and intracardiac metastasis models, Horm. Cancer, 6, 87, 10.1007/s12672-015-0219-0 · DOI
  51. Bellelli, 2012, FOXM1 is a molecular determinant of the mitogenic and invasive phenotype of anaplastic thyroid carcinoma, Endocr. Relat. Cancer, 19, 695, 10.1530/ERC-12-0031 · DOI
  52. Antonelli, 2009, Dysregulation of secretion of CXC alpha-chemokine CXCL10 in papillary thyroid cancer: modulation by peroxisome proliferator-activated receptor-gamma agonists, Endocr. Relat. Cancer, 16, 1299, 10.1677/ERC-08-0337 · DOI
  53. Antonelli, 2008, Primary cell cultures from anaplastic thyroid cancer obtained by fine-needle aspiration used for chemosensitivity tests, Clin. Endocrinol. (Oxf.), 69, 148, 10.1111/j.1365-2265.2008.03182.x · DOI
  54. Sun, 2013, Chemoradiation in anaplastic thyroid carcinomas, Crit. Rev. Oncol. Hematol., 86, 290, 10.1016/j.critrevonc.2012.10.006 · DOI
  55. Cortjens, 2016, Neutrophil extracellular traps cause airway obstruction during respiratory syncytial virus disease, J. Pathol., 238, 401, 10.1002/path.4660 · DOI
  56. Brinkmann, 2013, Automatic quantification of in vitro NET formation, Front. Immunol., 3, 413, 10.3389/fimmu.2012.00413 · DOI
  57. Kraaij, 2016, A novel method for high-throughput detection and quantification of neutrophil extracellular traps reveals ROS-independent NET release with immune complexes, Autoimmun. Rev., 15, 577, 10.1016/j.autrev.2016.02.018 · DOI
  58. Mohanty, 2018, NETQUANT: automated quantification of neutrophil extracellular traps, Front. Immunol., 8, 1999, 10.3389/fimmu.2017.01999 · DOI
  59. Hofman, 2004, Molecular regulation of neutrophil apoptosis and potential targets for therapeutic strategy against the inflammatory process, Curr. Drug Targets Inflamm. Allergy, 3, 1, 10.2174/1568010043483935 · DOI
  60. Barreda, 2004, Regulation of myeloid development and function by colony stimulating factors, Dev. Comp. Immunol., 28, 509, 10.1016/j.dci.2003.09.010 · DOI
  61. Kargl, 2017, Neutrophils dominate the immune cell composition in non-small cell lung cancer, Nat. Commun., 8, 14381, 10.1038/ncomms14381 · DOI
  62. Di Caro, 2016, Correction: circulating inflammatory mediators as potential prognostic markers of human colorectal cancer, PLoS One, 11
  63. Tohme, 2016, Neutrophil extracellular traps promote the development and progression of liver metastases after surgical stress, Cancer Res., 76, 1367, 10.1158/0008-5472.CAN-15-1591 · DOI · Paper page
  64. Al-Haidari, 2019, Neutrophil extracellular traps promote peritoneal metastasis of colon cancer cells, Oncotarget, 10, 1238, 10.18632/oncotarget.26664 · DOI
  65. Villanueva, 2011, Netting neutrophils induce endothelial damage, infiltrate tissues, and expose immunostimulatory molecules in systemic lupus erythematosus, J. Immunol., 187, 538, 10.4049/jimmunol.1100450 · DOI
  66. Ng, 2019, Heterogeneity of neutrophils, Nat. Rev. Immunol., 19, 255, 10.1038/s41577-019-0141-8 · DOI

Cited by

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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