Neutrophil Extracellular Traps in Cancer Therapy Resistance
Abstract
:Simple Summary
Abstract
1. Introduction
2. Neutrophils in Cancer Therapy Resistance
3. The Functional Role of NETs in Cancer Therapy Resistance
3.1. NETs in Chemotherapy Resistance
3.2. NETs in Immunotherapy Resistance
3.3. NETs in Radiation Therapy Resistance
4. NET Components in Cancer Therapy Resistance
4.1. Neutrophil Elastase
4.2. Matrix Metalloproteinase 9
4.3. Cathepsin G
4.4. Carcinoembryonic Antigen Cell Adhesion Molecule 1
4.5. PD-(L)1
5. Clinical Relevance of NETs in Resistance to Cancer Therapy
5.1. NETs and Monitoring Therapeutic Response
5.2. NETs as Targets for Combinatorial Cancer Therapy
6. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Coussens, L.M.; Werb, Z. Inflammation and cancer. Nature 2002, 420, 860–867. [Google Scholar] [CrossRef] [PubMed]
- Gonzalez, H.; Hagerling, C.; Werb, Z. Roles of the immune system in cancer: From tumor initiation to metastatic progression. Genes Dev. 2018, 32, 1267–1284. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cools-Lartigue, J.; Spicer, J.; Najmeh, S.; Ferri, L. Neutrophil extracellular traps in cancer progression. Cell. Mol. Life Sci. 2014, 71, 4179–4194. [Google Scholar] [CrossRef] [PubMed]
- Shaul, M.E.; Fridlender, Z.G. Tumour-associated neutrophils in patients with cancer. Nat. Rev. Clin. Oncol. 2019, 16, 601–620. [Google Scholar] [CrossRef] [PubMed]
- Powell, D.R.; Huttenlocher, A. Neutrophils in the Tumor Microenvironment. Trends Immunol. 2016, 37, 41–52. [Google Scholar] [CrossRef] [Green Version]
- Mizuno, R.; Kawada, K.; Itatani, Y.; Ogawa, R.; Kiyasu, Y.; Sakai, Y. The Role of Tumor-Associated Neutrophils in Colorectal Cancer. Int. J. Mol. Sci. 2019, 20, 529. [Google Scholar] [CrossRef] [Green Version]
- Burn, G.L.; Foti, A.; Marsman, G.; Patel, D.F.; Zychlinsky, A. The Neutrophil. Immunity 2021, 54, 1377–1391. [Google Scholar] [CrossRef]
- Liu, Y.; Liu, L. The pro-tumor effect and the anti-tumor effect of neutrophils extracellular traps. Biosci. Trends 2020, 13, 469–475. [Google Scholar] [CrossRef] [Green Version]
- Hinshaw, D.C.; Shevde, L.A. The Tumor Microenvironment Innately Modulates Cancer Progression. Cancer Res. 2019, 79, 4557–4566. [Google Scholar] [CrossRef] [Green Version]
- Capone, M.; Giannarelli, D.; Mallardo, D.; Madonna, G.; Festino, L.; Grimaldi, A.M.; Vanella, V.; Simeone, E.; Paone, M.; Palmieri, G.; et al. Baseline neutrophil-to-lymphocyte ratio (NLR) and derived NLR could predict overall survival in patients with advanced melanoma treated with nivolumab. J. Immunother. Cancer 2018, 6, 74. [Google Scholar] [CrossRef] [Green Version]
- Diem, S.; Schmid, S.; Krapf, M.; Flatz, L.; Born, D.; Jochum, W.; Templeton, A.J.; Früh, M. Neutrophil-to-Lymphocyte ratio (NLR) and Platelet-to-Lymphocyte ratio (PLR) as prognostic markers in patients with non-small cell lung cancer (NSCLC) treated with nivolumab. Lung Cancer 2017, 111, 176–181. [Google Scholar] [CrossRef] [PubMed]
- Feng, Z.; Wen, H.; Bi, R.; Ju, X.; Chen, X.; Yang, W.; Wu, X. Preoperative Neutrophil-to-Lymphocyte Ratio as a Predictive and Prognostic Factor for High-Grade Serous Ovarian Cancer. PLoS ONE 2016, 11, e0156101. [Google Scholar] [CrossRef] [PubMed]
- Van Soest, R.J.; Templeton, A.J.; Vera-Badillo, F.E.; Mercier, F.; Sonpavde, G.; Amir, E.; Tombal, B.; Rosenthal, M.; Eisenberger, M.A.; Tannock, I.F.; et al. Neutrophil-to-lymphocyte ratio as a prognostic biomarker for men with metastatic castration-resistant prostate cancer receiving first-line chemotherapy: Data from two randomized phase III trials. Ann. Oncol. 2015, 26, 743–749. [Google Scholar] [CrossRef] [PubMed]
- Wu, Y.; Li, C.; Zhao, J.; Yang, L.; Liu, F.; Zheng, H.; Wang, Z.; Xu, Y. Neutrophil-to-lymphocyte and platelet-to-lymphocyte ratios predict chemotherapy outcomes and prognosis in patients with colorectal cancer and synchronous liver metastasis. World J. Surg. Oncol. 2016, 14, 289. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Brinkmann, V.; Reichard, U.; Goosmann, C.; Fauler, B.; Uhlemann, Y.; Weiss, D.S.; Weinrauch, Y.; Zychlinsky, A. Neutrophil extracellular traps kill bacteria. Science 2004, 303, 1532–1535. [Google Scholar] [CrossRef]
- Yipp, B.G.; Kubes, P. NETosis: How vital is it? Blood 2013, 122, 2784–2794. [Google Scholar] [CrossRef]
- Papayannopoulos, V. Neutrophil extracellular traps in immunity and disease. Nat. Rev. Immunol. 2018, 18, 134–147. [Google Scholar] [CrossRef]
- Cools-Lartigue, J.; Spicer, J.; McDonald, B.; Gowing, S.; Chow, S.; Giannias, B.; Bourdeau, F.; Kubes, P.; Ferri, L. Neutrophil extracellular traps sequester circulating tumor cells and promote metastasis. J. Clin. Investig. 2013, 123, 3446–3458. [Google Scholar] [CrossRef]
- Huang, H.; Zhang, H.; Onuma, A.E.; Tsung, A. Neutrophil Elastase and Neutrophil Extracellular Traps in the Tumor Microenvironment. Adv. Exp. Med. Biol. 2020, 1263, 13–23. [Google Scholar] [CrossRef]
- Papayannopoulos, V.; Metzler, K.D.; Hakkim, A.; Zychlinsky, A. Neutrophil elastase and myeloperoxidase regulate the formation of neutrophil extracellular traps. J. Cell Biol. 2010, 191, 677–691. [Google Scholar] [CrossRef] [Green Version]
- Coffelt, S.B.; Wellenstein, M.D.; de Visser, K.E. Neutrophils in cancer: Neutral no more. Nat. Rev. Cancer 2016, 16, 431–446. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Garley, M.; Jablonska, E.; Dabrowska, D. NETs in cancer. Tumour. Biol. 2016, 37, 14355–14361. [Google Scholar] [CrossRef]
- Maffia, P.C.; Zittermann, S.E.; Scimone, M.L.; Tateosian, N.; Amiano, N.; Guerrieri, D.; Lutzky, V.; Rosso, D.; Romeo, H.E.; Garcia, V.E.; et al. Neutrophil elastase converts human immature dendritic cells into transforming growth factor-beta1-secreting cells and reduces allostimulatory ability. Am. J. Pathol. 2007, 171, 928–937. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rosales, C. Neutrophils at the crossroads of innate and adaptive immunity. J. Leukoc. Biol. 2020, 108, 377–396. [Google Scholar] [CrossRef] [PubMed]
- Albrengues, J.; Shields, M.A.; Ng, D.; Park, C.G.; Ambrico, A.; Poindexter, M.E.; Upadhyay, P.; Uyeminami, D.L.; Pommier, A.; Kuttner, V.; et al. Neutrophil extracellular traps produced during inflammation awaken dormant cancer cells in mice. Science 2018, 361, eaao4227. [Google Scholar] [CrossRef] [Green Version]
- Najmeh, S.; Cools-Lartigue, J.; Rayes, R.F.; Gowing, S.; Vourtzoumis, P.; Bourdeau, F.; Giannias, B.; Berube, J.; Rousseau, S.; Ferri, L.E.; et al. Neutrophil extracellular traps sequester circulating tumor cells via beta1-integrin mediated interactions. Int. J. Cancer 2017, 140, 2321–2330. [Google Scholar] [CrossRef] [Green Version]
- Ravindran, M.; Khan, M.A.; Palaniyar, N. Neutrophil Extracellular Trap Formation: Physiology, Pathology, and Pharmacology. Biomolecules 2019, 9, 365. [Google Scholar] [CrossRef] [Green Version]
- Rayes, R.F.; Mouhanna, J.G.; Nicolau, I.; Bourdeau, F.; Giannias, B.; Rousseau, S.; Quail, D.; Walsh, L.; Sangwan, V.; Bertos, N.; et al. Primary tumors induce neutrophil extracellular traps with targetable metastasis promoting effects. JCI Insight 2019, 5, e128008. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Baskar, R.; Lee, K.A.; Yeo, R.; Yeoh, K.W. Cancer and radiation therapy: Current advances and future directions. Int. J. Med. Sci. 2012, 9, 193–199. [Google Scholar] [CrossRef] [Green Version]
- Heinhuis, K.M.; Ros, W.; Kok, M.; Steeghs, N.; Beijnen, J.H.; Schellens, J.H.M. Enhancing antitumor response by combining immune checkpoint inhibitors with chemotherapy in solid tumors. Ann. Oncol. 2019, 30, 219–235. [Google Scholar] [CrossRef]
- Riley, R.S.; June, C.H.; Langer, R.; Mitchell, M.J. Delivery technologies for cancer immunotherapy. Nat. Rev. Drug Discov. 2019, 18, 175–196. [Google Scholar] [CrossRef] [PubMed]
- Mantovani, A.; Cassatella, M.A.; Costantini, C.; Jaillon, S. Neutrophils in the activation and regulation of innate and adaptive immunity. Nat. Rev. Immunol. 2011, 11, 519–531. [Google Scholar] [CrossRef] [PubMed]
- Hirata, E.; Sahai, E. Tumor Microenvironment and Differential Responses to Therapy. Cold Spring Harb. Perspect. Med. 2017, 7, a026781. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Van der Spek, Y.M.; Kroep, J.R.; Tollenaar, R.; Mesker, W.E. Chemotherapy resistance and stromal targets in breast cancer treatment: A review. Mol. Biol. Rep. 2020, 47, 8169–8177. [Google Scholar] [CrossRef] [PubMed]
- Wang, S.; Li, Y.; Xing, C.; Ding, C.; Zhang, H.; Chen, L.; You, L.; Dai, M.; Zhao, Y. Tumor microenvironment in chemoresistance, metastasis and immunotherapy of pancreatic cancer. Am. J. Cancer Res. 2020, 10, 1937–1953. [Google Scholar] [PubMed]
- Wu, T.; Dai, Y. Tumor microenvironment and therapeutic response. Cancer Lett. 2017, 387, 61–68. [Google Scholar] [CrossRef] [PubMed]
- Zheng, H.C. The molecular mechanisms of chemoresistance in cancers. Oncotarget 2017, 8, 59950–59964. [Google Scholar] [CrossRef] [Green Version]
- Quail, D.F.; Joyce, J.A. Microenvironmental regulation of tumor progression and metastasis. Nat. Med. 2013, 19, 1423–1437. [Google Scholar] [CrossRef]
- Park, J.; Wysocki, R.W.; Amoozgar, Z.; Maiorino, L.; Fein, M.R.; Jorns, J.; Schott, A.F.; Kinugasa-Katayama, Y.; Lee, Y.; Won, N.H.; et al. Cancer cells induce metastasis-supporting neutrophil extracellular DNA traps. Sci. Transl. Med. 2016, 8, 361ra138. [Google Scholar] [CrossRef] [Green Version]
- Deryugina, E.I.; Zajac, E.; Juncker-Jensen, A.; Kupriyanova, T.A.; Welter, L.; Quigley, J.P. Tissue-infiltrating neutrophils constitute the major in vivo source of angiogenesis-inducing MMP-9 in the tumor microenvironment. Neoplasia 2014, 16, 771–788. [Google Scholar] [CrossRef] [Green Version]
- Giese, M.A.; Hind, L.E.; Huttenlocher, A. Neutrophil plasticity in the tumor microenvironment. Blood 2019, 133, 2159–2167. [Google Scholar] [CrossRef] [PubMed]
- Wang, X.; Qiu, L.; Li, Z.; Wang, X.Y.; Yi, H. Understanding the Multifaceted Role of Neutrophils in Cancer and Autoimmune Diseases. Front. Immunol. 2018, 9, 2456. [Google Scholar] [CrossRef] [PubMed]
- Masucci, M.T.; Minopoli, M.; Carriero, M.V. Tumor Associated Neutrophils. Their Role in Tumorigenesis, Metastasis, Prognosis and Therapy. Front. Oncol. 2019, 9, 1146. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hedrick, C.C.; Malanchi, I. Neutrophils in cancer: Heterogeneous and multifaceted. Nat. Rev. Immunol. 2022, 22, 173–187. [Google Scholar] [CrossRef]
- Peng, Z.; Liu, C.; Victor, A.R.; Cao, D.Y.; Veiras, L.C.; Bernstein, E.A.; Khan, Z.; Giani, J.F.; Cui, X.; Bernstein, K.E.; et al. Tumors exploit CXCR4(hi)CD62L(lo) aged neutrophils to facilitate metastatic spread. Oncoimmunology 2021, 10, 1870811. [Google Scholar] [CrossRef]
- Di Maio, M.; Gridelli, C.; Gallo, C.; Shepherd, F.; Piantedosi, F.V.; Cigolari, S.; Manzione, L.; Illiano, A.; Barbera, S.; Robbiati, S.F.; et al. Chemotherapy-induced neutropenia and treatment efficacy in advanced non-small-cell lung cancer: A pooled analysis of three randomised trials. Lancet Oncol. 2005, 6, 669–677. [Google Scholar] [CrossRef]
- He, Y.; Li, T.; Liu, J.; Ou, Q.; Zhou, J. Early onset neutropenia: A useful predictor of chemosensitivity and favorable prognosis in patients with serous ovarian cancer. BMC Cancer 2020, 20, 116. [Google Scholar] [CrossRef] [Green Version]
- Kan, M.; Imaoka, H.; Watanabe, K.; Sasaki, M.; Takahashi, H.; Hashimoto, Y.; Ohno, I.; Mitsunaga, S.; Umemoto, K.; Kimura, G.; et al. Chemotherapy-induced neutropenia as a prognostic factor in patients with pancreatic cancer treated with gemcitabine plus nab-paclitaxel: A retrospective cohort study. Cancer Chemother. Pharmacol. 2020, 86, 203–210. [Google Scholar] [CrossRef]
- Kasi, P.M.; Grothey, A. Chemotherapy-Induced Neutropenia as a Prognostic and Predictive Marker of Outcomes in Solid-Tumor Patients. Drugs 2018, 78, 737–745. [Google Scholar] [CrossRef]
- Meisel, A.; von Felten, S.; Vogt, D.R.; Liewen, H.; de Wit, R.; de Bono, J.; Sartor, O.; Stenner-Liewen, F. Severe neutropenia during cabazitaxel treatment is associated with survival benefit in men with metastatic castration-resistant prostate cancer (mCRPC): A post-hoc analysis of the TROPIC phase III trial. Eur. J. Cancer 2016, 56, 93–100. [Google Scholar] [CrossRef]
- Roviello, G.; Ramello, M.; Catalano, M.; D’Angelo, A.; Conca, R.; Gasperoni, S.; Dreoni, L.; Petrioli, R.; Ianza, A.; Nobili, S.; et al. Association between neutropenia and survival to nab-paclitaxel and gemcitabine in patients with metastatic pancreatic cancer. Sci. Rep. 2020, 10, 19281. [Google Scholar] [CrossRef]
- Shitara, K.; Matsuo, K.; Takahari, D.; Yokota, T.; Inaba, Y.; Yamaura, H.; Sato, Y.; Najima, M.; Ura, T.; Muro, K. Neutropaenia as a prognostic factor in metastatic colorectal cancer patients undergoing chemotherapy with first-line FOLFOX. Eur. J. Cancer 2009, 45, 1757–1763. [Google Scholar] [CrossRef] [PubMed]
- Shitara, K.; Matsuo, K.; Takahari, D.; Yokota, T.; Shibata, T.; Ura, T.; Ito, S.; Sawaki, A.; Tajika, M.; Kawai, H.; et al. Neutropenia as a prognostic factor in advanced gastric cancer patients undergoing second-line chemotherapy with weekly paclitaxel. Ann. Oncol. 2010, 21, 2403–2409. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Chen, Y.; Yin, H.; Gu, X.; Shi, Y.; Dai, G. Timing of chemotherapy-induced neutropenia is a prognostic factor in patients with advanced gastric cancer undergoing first-line chemotherapy with oxaliplatin and capecitabine: A retrospective study. Cancer Med. 2018, 7, 997–1005. [Google Scholar] [CrossRef] [PubMed]
- Yoshino, T.; Cleary, J.M.; Van Cutsem, E.; Mayer, R.J.; Ohtsu, A.; Shinozaki, E.; Falcone, A.; Yamazaki, K.; Nishina, T.; Garcia-Carbonero, R.; et al. Neutropenia and survival outcomes in metastatic colorectal cancer patients treated with trifluridine/tipiracil in the RECOURSE and J003 trials. Ann. Oncol. 2020, 31, 88–95. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Han, Y.; Yu, Z.; Wen, S.; Zhang, B.; Cao, X.; Wang, X. Prognostic value of chemotherapy-induced neutropenia in early-stage breast cancer. Breast Cancer Res. Treat. 2012, 131, 483–490. [Google Scholar] [CrossRef] [PubMed]
- Ramachandran, I.R.; Condamine, T.; Lin, C.; Herlihy, S.E.; Garfall, A.; Vogl, D.T.; Gabrilovich, D.I.; Nefedova, Y. Bone marrow PMN-MDSCs and neutrophils are functionally similar in protection of multiple myeloma from chemotherapy. Cancer Lett. 2016, 371, 117–124. [Google Scholar] [CrossRef]
- Teijeira, A.; Garasa, S.; Ochoa, M.C.; Villalba, M.; Olivera, I.; Cirella, A.; Eguren-Santamaria, I.; Berraondo, P.; Schalper, K.A.; de Andrea, C.E.; et al. IL8, Neutrophils, and NETs in a Collusion against Cancer Immunity and Immunotherapy. Clin. Cancer Res. 2021, 27, 2383–2393. [Google Scholar] [CrossRef]
- Zhang, Y.; Guoqiang, L.; Sun, M.; Lu, X. Targeting and exploitation of tumor-associated neutrophils to enhance immunotherapy and drug delivery for cancer treatment. Cancer Biol. Med. 2020, 17, 32–43. [Google Scholar] [CrossRef]
- Wisdom, A.J.; Hong, C.S.; Lin, A.J.; Xiang, Y.; Cooper, D.E.; Zhang, J.; Xu, E.S.; Kuo, H.C.; Mowery, Y.M.; Carpenter, D.J.; et al. Neutrophils promote tumor resistance to radiation therapy. Proc. Natl. Acad. Sci. USA 2019, 116, 18584–18589. [Google Scholar] [CrossRef] [Green Version]
- Lin, C.; Herlihy, S.E.; Li, M.; Deng, H.; Bernabei, L.; Gabrilovich, D.I.; Vogl, D.T.; Nefedova, Y. NETs promote tumor resistance to anthracyclines. In Proceedings of the American Association for Cancer Research Annual Meeting, Altanta, GA, USA, 29 March–3 April 2019; p. 2103. [Google Scholar]
- Baas, P.; Scherpereel, A.; Nowak, A.K.; Fujimoto, N.; Peters, S.; Tsao, A.S.; Mansfield, A.S.; Popat, S.; Jahan, T.; Antonia, S.; et al. First-line nivolumab plus ipilimumab in unresectable malignant pleural mesothelioma (CheckMate 743): A multicentre, randomised, open-label, phase 3 trial. Lancet 2021, 397, 375–386. [Google Scholar] [CrossRef]
- Bellmunt, J.; de Wit, R.; Vaughn, D.J.; Fradet, Y.; Lee, J.L.; Fong, L.; Vogelzang, N.J.; Climent, M.A.; Petrylak, D.P.; Choueiri, T.K.; et al. Pembrolizumab as Second-Line Therapy for Advanced Urothelial Carcinoma. N. Engl. J. Med. 2017, 376, 1015–1026. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Borghaei, H.; Paz-Ares, L.; Horn, L.; Spigel, D.R.; Steins, M.; Ready, N.E.; Chow, L.Q.; Vokes, E.E.; Felip, E.; Holgado, E.; et al. Nivolumab versus Docetaxel in Advanced Nonsquamous Non-Small-Cell Lung Cancer. N. Engl. J. Med. 2015, 373, 1627–1639. [Google Scholar] [CrossRef] [PubMed]
- Gandhi, L.; Rodríguez-Abreu, D.; Gadgeel, S.; Esteban, E.; Felip, E.; De Angelis, F.; Domine, M.; Clingan, P.; Hochmair, M.J.; Powell, S.F.; et al. Pembrolizumab plus Chemotherapy in Metastatic Non-Small-Cell Lung Cancer. N. Engl. J. Med. 2018, 378, 2078–2092. [Google Scholar] [CrossRef]
- Hellmann, M.D.; Paz-Ares, L.; Bernabe Caro, R.; Zurawski, B.; Kim, S.W.; Carcereny Costa, E.; Park, K.; Alexandru, A.; Lupinacci, L.; de la Mora Jimenez, E.; et al. Nivolumab plus Ipilimumab in Advanced Non-Small-Cell Lung Cancer. N. Engl. J. Med. 2019, 381, 2020–2031. [Google Scholar] [CrossRef]
- Larkin, J.; Chiarion-Sileni, V.; Gonzalez, R.; Grob, J.J.; Rutkowski, P.; Lao, C.D.; Cowey, C.L.; Schadendorf, D.; Wagstaff, J.; Dummer, R.; et al. Five-Year Survival with Combined Nivolumab and Ipilimumab in Advanced Melanoma. N. Engl. J. Med. 2019, 381, 1535–1546. [Google Scholar] [CrossRef] [Green Version]
- Motzer, R.J.; Tannir, N.M.; McDermott, D.F.; Arén Frontera, O.; Melichar, B.; Choueiri, T.K.; Plimack, E.R.; Barthélémy, P.; Porta, C.; George, S.; et al. Nivolumab plus Ipilimumab versus Sunitinib in Advanced Renal-Cell Carcinoma. N. Engl. J. Med. 2018, 378, 1277–1290. [Google Scholar] [CrossRef]
- Paz-Ares, L.; Ciuleanu, T.E.; Cobo, M.; Schenker, M.; Zurawski, B.; Menezes, J.; Richardet, E.; Bennouna, J.; Felip, E.; Juan-Vidal, O.; et al. First-line nivolumab plus ipilimumab combined with two cycles of chemotherapy in patients with non-small-cell lung cancer (CheckMate 9LA): An international, randomised, open-label, phase 3 trial. Lancet Oncol. 2021, 22, 198–211. [Google Scholar] [CrossRef]
- Provencio, M.; Nadal, E.; Insa, A.; García-Campelo, M.R.; Casal-Rubio, J.; Dómine, M.; Majem, M.; Rodríguez-Abreu, D.; Martínez-Martí, A.; De Castro Carpeño, J.; et al. Neoadjuvant chemotherapy and nivolumab in resectable non-small-cell lung cancer (NADIM): An open-label, multicentre, single-arm, phase 2 trial. Lancet Oncol. 2020, 21, 1413–1422. [Google Scholar] [CrossRef]
- Reck, M.; Rodríguez-Abreu, D.; Robinson, A.G.; Hui, R.; Csőszi, T.; Fülöp, A.; Gottfried, M.; Peled, N.; Tafreshi, A.; Cuffe, S.; et al. Pembrolizumab versus Chemotherapy for PD-L1-Positive Non-Small-Cell Lung Cancer. N. Engl. J. Med. 2016, 375, 1823–1833. [Google Scholar] [CrossRef] [Green Version]
- Robert, C.; Schachter, J.; Long, G.V.; Arance, A.; Grob, J.J.; Mortier, L.; Daud, A.; Carlino, M.S.; McNeil, C.; Lotem, M.; et al. Pembrolizumab versus Ipilimumab in Advanced Melanoma. N. Engl. J. Med. 2015, 372, 2521–2532. [Google Scholar] [CrossRef] [PubMed]
- Gibney, G.T.; Weiner, L.M.; Atkins, M.B. Predictive biomarkers for checkpoint inhibitor-based immunotherapy. Lancet Oncol. 2016, 17, e542–e551. [Google Scholar] [CrossRef] [Green Version]
- Han, Y.; Liu, D.; Li, L. PD-1/PD-L1 pathway: Current researches in cancer. Am. J. Cancer Res. 2020, 10, 727–742. [Google Scholar] [PubMed]
- Jiang, Y.; Chen, M.; Nie, H.; Yuan, Y. PD-1 and PD-L1 in cancer immunotherapy: Clinical implications and future considerations. Hum. Vaccin. Immunother. 2019, 15, 1111–1122. [Google Scholar] [CrossRef]
- Teijeira, Á.; Garasa, S.; Gato, M.; Alfaro, C.; Migueliz, I.; Cirella, A.; de Andrea, C.; Ochoa, M.C.; Otano, I.; Etxeberria, I.; et al. CXCR1 and CXCR2 Chemokine Receptor Agonists Produced by Tumors Induce Neutrophil Extracellular Traps that Interfere with Immune Cytotoxicity. Immunity 2020, 52, 856–871.e858. [Google Scholar] [CrossRef]
- Zhang, Y.; Chandra, V.; Riquelme Sanchez, E.; Dutta, P.; Quesada, P.R.; Rakoski, A.; Zoltan, M.; Arora, N.; Baydogan, S.; Horne, W.; et al. Interleukin-17–induced neutrophil extracellular traps mediate resistance to checkpoint blockade in pancreatic cancer. J. Exp. Med. 2020, 217, e2019035. [Google Scholar] [CrossRef]
- Sasaki, A.; Nakamura, Y.; Mishima, S.; Kawazoe, A.; Kuboki, Y.; Bando, H.; Kojima, T.; Doi, T.; Ohtsu, A.; Yoshino, T.; et al. Predictive factors for hyperprogressive disease during nivolumab as anti-PD1 treatment in patients with advanced gastric cancer. Gastric Cancer 2019, 22, 793–802. [Google Scholar] [CrossRef] [Green Version]
- Moding, E.J.; Kastan, M.B.; Kirsch, D.G. Strategies for optimizing the response of cancer and normal tissues to radiation. Nat. Rev. Drug Discov. 2013, 12, 526–542. [Google Scholar] [CrossRef] [Green Version]
- Kim, B.M.; Hong, Y.; Lee, S.; Liu, P.; Lim, J.H.; Lee, Y.H.; Lee, T.H.; Chang, K.T.; Hong, Y. Therapeutic Implications for Overcoming Radiation Resistance in Cancer Therapy. Int. J. Mol. Sci. 2015, 16, 26880–26913. [Google Scholar] [CrossRef] [Green Version]
- Shinde-Jadhav, S.; Mansure, J.J.; Rayes, R.F.; Marcq, G.; Ayoub, M.; Skowronski, R.; Kool, R.; Bourdeau, F.; Brimo, F.; Spicer, J.; et al. Role of neutrophil extracellular traps in radiation resistance of invasive bladder cancer. Nat. Commun. 2021, 12, 2776. [Google Scholar] [CrossRef]
- Lerman, I.; Hammes, S.R. Neutrophil elastase in the tumor microenvironment. Steroids 2018, 133, 96–101. [Google Scholar] [CrossRef] [PubMed]
- Martins-Cardoso, K.; Almeida, V.H.; Bagri, K.M.; Rossi, M.I.D.; Mermelstein, C.S.; König, S.; Monteiro, R.Q. Neutrophil Extracellular Traps (NETs) Promote Pro-Metastatic Phenotype in Human Breast Cancer Cells through Epithelial-Mesenchymal Transition. Cancers 2020, 12, 1542. [Google Scholar] [CrossRef] [PubMed]
- Zhu, T.; Zou, X.; Yang, C.; Li, L.; Wang, B.; Li, R.; Li, H.; Xu, Z.; Huang, D.; Wu, Q. Neutrophil extracellular traps promote gastric cancer metastasis by inducing epithelial-mesenchymal transition. Int. J. Mol. Med. 2021, 48, 127. [Google Scholar] [CrossRef]
- Lu, W.; Kang, Y. Epithelial-Mesenchymal Plasticity in Cancer Progression and Metastasis. Dev. Cell 2019, 49, 361–374. [Google Scholar] [CrossRef] [PubMed]
- Yeldag, G.; Rice, A.; Del Río Hernández, A. Chemoresistance and the Self-Maintaining Tumor Microenvironment. Cancers 2018, 10, 471. [Google Scholar] [CrossRef] [Green Version]
- Zhang, Y.; Weinberg, R.A. Epithelial-to-mesenchymal transition in cancer: Complexity and opportunities. Front. Med. 2018, 12, 361–373. [Google Scholar] [CrossRef] [Green Version]
- Dongre, A.; Weinberg, R.A. New insights into the mechanisms of epithelial-mesenchymal transition and implications for cancer. Nat. Rev. Mol. Cell Biol. 2019, 20, 69–84. [Google Scholar] [CrossRef]
- Ribatti, D.; Tamma, R.; Annese, T. Epithelial-Mesenchymal Transition in Cancer: A Historical Overview. Transl. Oncol. 2020, 13, 100773. [Google Scholar] [CrossRef]
- Kalluri, R.; Weinberg, R.A. The basics of epithelial-mesenchymal transition. J. Clin. Investig. 2009, 119, 1420–1428. [Google Scholar] [CrossRef] [Green Version]
- Suarez-Carmona, M.; Lesage, J.; Cataldo, D.; Gilles, C. EMT and inflammation: Inseparable actors of cancer progression. Mol. Oncol. 2017, 11, 805–823. [Google Scholar] [CrossRef]
- Peng, Z.; Wang, C.X.; Fang, E.H.; Wang, G.B.; Tong, Q. Role of epithelial-mesenchymal transition in gastric cancer initiation and progression. World J. Gastroenterol. 2014, 20, 5403–5410. [Google Scholar] [CrossRef] [PubMed]
- Deng, J.; Wang, L.; Chen, H.; Hao, J.; Ni, J.; Chang, L.; Duan, W.; Graham, P.; Li, Y. Targeting epithelial-mesenchymal transition and cancer stem cells for chemoresistant ovarian cancer. Oncotarget 2016, 7, 55771–55788. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dong, J.; Wang, R.; Ren, G.; Li, X.; Wang, J.; Sun, Y.; Liang, J.; Nie, Y.; Wu, K.; Feng, B.; et al. HMGA2-FOXL2 Axis Regulates Metastases and Epithelial-to-Mesenchymal Transition of Chemoresistant Gastric Cancer. Clin. Cancer Res. 2017, 23, 3461–3473. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fischer, K.R.; Durrans, A.; Lee, S.; Sheng, J.; Li, F.; Wong, S.T.; Choi, H.; El Rayes, T.; Ryu, S.; Troeger, J.; et al. Epithelial-to-mesenchymal transition is not required for lung metastasis but contributes to chemoresistance. Nature 2015, 527, 472–476. [Google Scholar] [CrossRef] [PubMed]
- Gu, Y.; Zhang, B.; Gu, G.; Yang, X.; Qian, Z. Metformin Increases the Chemosensitivity of Pancreatic Cancer Cells to Gemcitabine by Reversing EMT Through Regulation DNA Methylation of miR-663. Onco Targets Ther. 2020, 13, 10417–10429. [Google Scholar] [CrossRef]
- Yu, J.; Zhang, W.; Gao, F.; Liu, Y.X.; Chen, Z.Y.; Cheng, L.Y.; Xie, S.F.; Zheng, S.S. FBW7 increases chemosensitivity in hepatocellular carcinoma cells through suppression of epithelial-mesenchymal transition. Hepatobiliary Pancreat. Dis. Int. 2014, 13, 184–191. [Google Scholar] [CrossRef]
- Zeng, D.; Liang, Y.K.; Xiao, Y.S.; Wei, X.L.; Lin, H.Y.; Wu, Y.; Bai, J.W.; Chen, M.; Zhang, G.J. Inhibition of Notch1 reverses EMT and chemoresistance to cisplatin via direct downregulation of MCAM in triple-negative breast cancer cells. Int. J. Cancer 2020, 147, 490–504. [Google Scholar] [CrossRef]
- Deryugina, E.; Carré, A.; Ardi, V.; Muramatsu, T.; Schmidt, J.; Pham, C.; Quigley, J.P. Neutrophil Elastase Facilitates Tumor Cell Intravasation and Early Metastatic Events. iScience 2020, 23, 101799. [Google Scholar] [CrossRef]
- Gaida, M.M.; Steffen, T.G.; Günther, F.; Tschaharganeh, D.F.; Felix, K.; Bergmann, F.; Schirmacher, P.; Hänsch, G.M. Polymorphonuclear neutrophils promote dyshesion of tumor cells and elastase-mediated degradation of E-cadherin in pancreatic tumors. Eur. J. Immunol. 2012, 42, 3369–3380. [Google Scholar] [CrossRef]
- Grosse-Steffen, T.; Giese, T.; Giese, N.; Longerich, T.; Schirmacher, P.; Hänsch, G.M.; Gaida, M.M. Epithelial-to-mesenchymal transition in pancreatic ductal adenocarcinoma and pancreatic tumor cell lines: The role of neutrophils and neutrophil-derived elastase. Clin. Dev. Immunol. 2012, 2012, 720768. [Google Scholar] [CrossRef]
- Mayer, C.; Darb-Esfahani, S.; Meyer, A.S.; Hübner, K.; Rom, J.; Sohn, C.; Braicu, I.; Sehouli, J.; Hänsch, G.M.; Gaida, M.M. Neutrophil Granulocytes in Ovarian Cancer—Induction of Epithelial-To-Mesenchymal-Transition and Tumor Cell Migration. J. Cancer 2016, 7, 546–554. [Google Scholar] [CrossRef] [PubMed]
- Cabral-Pacheco, G.A.; Garza-Veloz, I.; Castruita-De la Rosa, C.; Ramirez-Acuña, J.M.; Perez-Romero, B.A.; Guerrero-Rodriguez, J.F.; Martinez-Avila, N.; Martinez-Fierro, M.L. The Roles of Matrix Metalloproteinases and Their Inhibitors in Human Diseases. Int. J. Mol. Sci. 2020, 21, 9739. [Google Scholar] [CrossRef] [PubMed]
- De Palma, M.; Biziato, D.; Petrova, T.V. Microenvironmental regulation of tumour angiogenesis. Nat. Rev. Cancer 2017, 17, 457–474. [Google Scholar] [CrossRef] [PubMed]
- Hawinkels, L.J.A.C.; Zuidwijk, K.; Verspaget, H.W.; de Jonge-Muller, E.S.M.; Duijn, W.V.; Ferreira, V.; Fontijn, R.D.; David, G.; Hommes, D.W.; Lamers, C.B.H.W.; et al. VEGF release by MMP-9 mediated heparan sulphate cleavage induces colorectal cancer angiogenesis. Eur. J. Cancer 2008, 44, 1904–1913. [Google Scholar] [CrossRef] [PubMed]
- Mittal, V.; El Rayes, T.; Narula, N.; McGraw, T.E.; Altorki, N.K.; Barcellos-Hoff, M.H. The Microenvironment of Lung Cancer and Therapeutic Implications. Adv. Exp. Med. Biol. 2016, 890, 75–110. [Google Scholar] [CrossRef]
- Nalla, A.K.; Gorantla, B.; Gondi, C.S.; Lakka, S.S.; Rao, J.S. Targeting MMP-9, uPAR, and cathepsin B inhibits invasion, migration and activates apoptosis in prostate cancer cells. Cancer Gene Ther. 2010, 17, 599–613. [Google Scholar] [CrossRef] [Green Version]
- Gao, H.; Lan, X.; Li, S.; Xue, Y. Relationships of MMP-9, E-cadherin, and VEGF expression with clinicopathological features and response to chemosensitivity in gastric cancer. Tumour. Biol. 2017, 39, 1010428317698368. [Google Scholar] [CrossRef] [Green Version]
- Yang, Y.; Ma, L.; Xu, Y.; Liu, Y.; Li, W.; Cai, J.; Zhang, Y. Enalapril overcomes chemoresistance and potentiates antitumor efficacy of 5-FU in colorectal cancer by suppressing proliferation, angiogenesis, and NF-κB/STAT3-regulated proteins. Cell Death Dis. 2020, 11, 477. [Google Scholar] [CrossRef]
- Viallard, C.; Larrivée, B. Tumor angiogenesis and vascular normalization: Alternative therapeutic targets. Angiogenesis 2017, 20, 409–426. [Google Scholar] [CrossRef]
- Nishida, N.; Yano, H.; Nishida, T.; Kamura, T.; Kojiro, M. Angiogenesis in cancer. Vasc. Health Risk Manag. 2006, 2, 213–219. [Google Scholar] [CrossRef]
- Bui, T.M.; Yalom, L.K.; Sumagin, R. Tumor-associated neutrophils: Orchestrating cancer pathobiology and therapeutic resistance. Expert Opin. Ther. Targets 2021, 25, 573–583. [Google Scholar] [CrossRef] [PubMed]
- Da Ros, M.; De Gregorio, V.; Iorio, A.L.; Giunti, L.; Guidi, M.; de Martino, M.; Genitori, L.; Sardi, I. Glioblastoma Chemoresistance: The Double Play by Microenvironment and Blood-Brain Barrier. Int. J. Mol. Sci. 2018, 19, 2879. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wilson, T.J.; Nannuru, K.C.; Futakuchi, M.; Singh, R.K. Cathepsin G-mediated enhanced TGF-beta signaling promotes angiogenesis via upregulation of VEGF and MCP-1. Cancer Lett. 2010, 288, 162–169. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Brown, Y.; Hua, S.; Tanwar, P.S. Extracellular matrix-mediated regulation of cancer stem cells and chemoresistance. Int. J. Biochem. Cell Biol. 2019, 109, 90–104. [Google Scholar] [CrossRef]
- Guan, X.; Lu, Y.; Zhu, H.; Yu, S.; Zhao, W.; Chi, X.; Xie, C.; Yin, Z. The Crosstalk Between Cancer Cells and Neutrophils Enhances Hepatocellular Carcinoma Metastasis via Neutrophil Extracellular Traps-Associated Cathepsin G Component: A Potential Therapeutic Target. J. Hepatocell. Carcinoma 2021, 8, 451–465. [Google Scholar] [CrossRef]
- Khan, M.; Carmona, S.; Sukhumalchandra, P.; Roszik, J.; Philips, A.; Perakis, A.A.; Kerros, C.; Zhang, M.; Qiao, N.; John, L.S.S.; et al. Cathepsin G Is Expressed by Acute Lymphoblastic Leukemia and Is a Potential Immunotherapeutic Target. Front. Immunol. 2018, 8, 1975. [Google Scholar] [CrossRef]
- Rayes, R.F.; Vourtzoumis, P.; Bou Rjeily, M.; Seth, R.; Bourdeau, F.; Giannias, B.; Berube, J.; Huang, Y.H.; Rousseau, S.; Camilleri-Broet, S.; et al. Neutrophil Extracellular Trap-Associated CEACAM1 as a Putative Therapeutic Target to Prevent Metastatic Progression of Colon Carcinoma. J. Immunol. 2020, 204, 2285–2294. [Google Scholar] [CrossRef]
- Beauchemin, N.; Arabzadeh, A. Carcinoembryonic antigen-related cell adhesion molecules (CEACAMs) in cancer progression and metastasis. Cancer Metastasis Rev. 2013, 32, 643–671. [Google Scholar] [CrossRef]
- Dankner, M.; Gray-Owen, S.D.; Huang, Y.H.; Blumberg, R.S.; Beauchemin, N. CEACAM1 as a multi-purpose target for cancer immunotherapy. Oncoimmunology 2017, 6, e1328336. [Google Scholar] [CrossRef] [Green Version]
- Huang, Y.H.; Zhu, C.; Kondo, Y.; Anderson, A.C.; Gandhi, A.; Russell, A.; Dougan, S.K.; Petersen, B.S.; Melum, E.; Pertel, T.; et al. CEACAM1 regulates TIM-3-mediated tolerance and exhaustion. Nature 2015, 517, 386–390. [Google Scholar] [CrossRef] [Green Version]
- Ortenberg, R.; Sapoznik, S.; Zippel, D.; Shapira-Frommer, R.; Itzhaki, O.; Kubi, A.; Zikich, D.; Besser, M.J.; Schachter, J.; Markel, G. Serum CEACAM1 Elevation Correlates with Melanoma Progression and Failure to Respond to Adoptive Cell Transfer Immunotherapy. J. Immunol. Res. 2015, 2015, 902137. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yang, F.; Zeng, Z.; Li, J.; Ren, X.; Wei, F. TIM-3 and CEACAM1 are Prognostic Factors in Head and Neck Squamous Cell Carcinoma. Front. Mol. Biosci. 2021, 8, 619765. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Y.; Cai, P.; Li, L.; Shi, L.; Chang, P.; Liang, T.; Yang, Q.; Liu, Y.; Wang, L.; Hu, L. Co-expression of TIM-3 and CEACAM1 promotes T cell exhaustion in colorectal cancer patients. Int. Immunopharmacol. 2017, 43, 210–218. [Google Scholar] [CrossRef]
- Wherry, E.J. T cell exhaustion. Nat. Immunol. 2011, 12, 492–499. [Google Scholar] [CrossRef]
- Sharma, P.; Hu-Lieskovan, S.; Wargo, J.A.; Ribas, A. Primary, Adaptive, and Acquired Resistance to Cancer Immunotherapy. Cell 2017, 168, 707–723. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jiang, W.; He, Y.; He, W.; Wu, G.; Zhou, X.; Sheng, Q.; Zhong, W.; Lu, Y.; Ding, Y.; Lu, Q.; et al. Exhausted CD8+T Cells in the Tumor Immune Microenvironment: New Pathways to Therapy. Front. Immunol. 2021, 11, 622509. [Google Scholar] [CrossRef] [PubMed]
- Kaltenmeier, C.; Yazdani, H.O.; Morder, K.; Geller, D.A.; Simmons, R.L.; Tohme, S. Neutrophil Extracellular Traps Promote T Cell Exhaustion in the Tumor Microenvironment. Front. Immunol. 2021, 12, 785222. [Google Scholar] [CrossRef] [PubMed]
- Holdenrieder, S.; Stieber, P.; von Pawel, J.; Raith, H.; Nagel, D.; Feldmann, K.; Seidel, D. Circulating Nucleosomes Predict the Response to Chemotherapy in Patients with Advanced Non–Small Cell Lung Cancer. Clin. Cancer Res. 2004, 10, 5981–5987. [Google Scholar] [CrossRef] [Green Version]
- Capizzi, E.; Gabusi, E.; Grigioni, A.D.; De Iaco, P.; Rosati, M.; Zamagni, C.; Fiorentino, M. Quantification of free plasma DNA before and after chemotherapy in patients with advanced epithelial ovarian cancer. Diagn. Mol. Pathol. 2008, 17, 34–38. [Google Scholar] [CrossRef]
- Chua, W.; Goldstein, D.; Lee, C.K.; Dhillon, H.; Michael, M.; Mitchell, P.; Clarke, S.J.; Iacopetta, B. Molecular markers of response and toxicity to FOLFOX chemotherapy in metastatic colorectal cancer. Br. J. Cancer 2009, 101, 998–1004. [Google Scholar] [CrossRef] [Green Version]
- Kamat, A.A.; Bischoff, F.Z.; Dang, D.; Baldwin, M.F.; Han, L.Y.; Lin, Y.G.; Merritt, W.M.; Landen, C.N., Jr.; Lu, C.; Gershenson, D.M.; et al. Circulating cell-free DNA: A novel biomarker for response to therapy in ovarian carcinoma. Cancer Biol. Ther. 2006, 5, 1369–1374. [Google Scholar] [CrossRef] [Green Version]
- Kuroi, K.; Tanaka, C.; Toi, M. Clinical significance of plasma nucleosome levels in cancer patients. Int. J. Oncol. 2001, 19, 143–148. [Google Scholar] [CrossRef] [PubMed]
- Patsch, K.; Matasci, N.; Soundararajan, A.; Diaz, P.; Agus, D.B.; Ruderman, D.; Gross, M.E. Monitoring dynamic cytotoxic chemotherapy response in castration-resistant prostate cancer using plasma cell-free DNA (cfDNA). BMC Res. Notes 2019, 12, 275. [Google Scholar] [CrossRef] [PubMed]
- Trejo-Becerril, C.; Oñate-Ocaña, L.F.; Taja-Chayeb, L.; Vanoye-Carlo, A.; Cetina, L.; Duenas-Gonzalez, A. Serum nucleosomes during neoadjuvant chemotherapy in patients with cervical cancer. Predictive and prognostic significance. BMC Cancer 2005, 5, 65. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Anagnostou, V.; Forde, P.M.; White, J.R.; Niknafs, N.; Hruban, C.; Naidoo, J.; Marrone, K.; Sivakumar, I.K.A.; Bruhm, D.C.; Rosner, S.; et al. Dynamics of Tumor and Immune Responses during Immune Checkpoint Blockade in Non-Small Cell Lung Cancer. Cancer Res. 2019, 79, 1214–1225. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cabel, L.; Riva, F.; Servois, V.; Livartowski, A.; Daniel, C.; Rampanou, A.; Lantz, O.; Romano, E.; Milder, M.; Buecher, B.; et al. Circulating tumor DNA changes for early monitoring of anti-PD1 immunotherapy: A proof-of-concept study. Ann. Oncol. 2017, 28, 1996–2001. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Goldberg, S.B.; Narayan, A.; Kole, A.J.; Decker, R.H.; Teysir, J.; Carriero, N.J.; Lee, A.; Nemati, R.; Nath, S.K.; Mane, S.M.; et al. Early Assessment of Lung Cancer Immunotherapy Response via Circulating Tumor DNA. Clin. Cancer Res. 2018, 24, 1872–1880. [Google Scholar] [CrossRef] [Green Version]
- Mondelo-Macía, P.; García-González, J.; León-Mateos, L.; Anido, U.; Aguín, S.; Abdulkader, I.; Sánchez-Ares, M.; Abalo, A.; Rodríguez-Casanova, A.; Díaz-Lagares, Á.; et al. Clinical potential of circulating free DNA and circulating tumour cells in patients with metastatic non-small-cell lung cancer treated with pembrolizumab. Mol. Oncol. 2021, 15, 2923–2940. [Google Scholar] [CrossRef]
- Fuchs, T.A.; Kremer Hovinga, J.A.; Schatzberg, D.; Wagner, D.D.; Lämmle, B. Circulating DNA and myeloperoxidase indicate disease activity in patients with thrombotic microangiopathies. Blood 2012, 120, 1157–1164. [Google Scholar] [CrossRef] [Green Version]
- Tan, C.; Aziz, M.; Wang, P. The vitals of NETs. J. Leukoc. Biol. 2021, 110, 797–808. [Google Scholar] [CrossRef]
- Tilley, D.O.; Abuabed, U.; Arndt, U.Z.; Schmid, M.; Florian, S.; Jungblut, P.R.; Brinkmann, V.; Herzig, A.; Zychlinsky, A. Histone H3 clipping is a novel signature of human neutrophil extracellular traps. bioRxiv 2021. [Google Scholar] [CrossRef]
- Masuda, S.; Nakazawa, D.; Shida, H.; Miyoshi, A.; Kusunoki, Y.; Tomaru, U.; Ishizu, A. NETosis markers: Quest for specific, objective, and quantitative markers. Clin. Chim. Acta 2016, 459, 89–93. [Google Scholar] [CrossRef] [PubMed]
- Fisher, J.; Mohanty, T.; Karlsson, C.A.Q.; Khademi, S.M.H.; Malmström, E.; Frigyesi, A.; Nordenfelt, P.; Malmstrom, J.; Linder, A. Proteome Profiling of Recombinant DNase Therapy in Reducing NETs and Aiding Recovery in COVID-19 Patients. Mol. Cell. Proteomics 2021, 20, 100113. [Google Scholar] [CrossRef] [PubMed]
- Barnes, B.J.; Adrover, J.M.; Baxter-Stoltzfus, A.; Borczuk, A.; Cools-Lartigue, J.; Crawford, J.M.; Daßler-Plenker, J.; Guerci, P.; Huynh, C.; Knight, J.S.; et al. Targeting potential drivers of COVID-19: Neutrophil extracellular traps. J. Exp. Med. 2020, 217, e20200652. [Google Scholar] [CrossRef]
- ClinicalTrials.gov. DISmantling COvid iNduced Neutrophil ExtraCellular Traps (DISCONNECT-1). Available online: https://clinicaltrials.gov/ct2/show/NCT04409925 (accessed on 24 December 2021).
- Belaaouaj, A.; McCarthy, R.; Baumann, M.; Gao, Z.; Ley, T.J.; Abraham, S.N.; Shapiro, S.D. Mice lacking neutrophil elastase reveal impaired host defense against gram negative bacterial sepsis. Nat. Med. 1998, 4, 615–618. [Google Scholar] [CrossRef]
- Sato, T.; Takahashi, S.; Mizumoto, T.; Harao, M.; Akizuki, M.; Takasugi, M.; Fukutomi, T.; Yamashita, J. Neutrophil elastase and cancer. Surg. Oncol. 2006, 15, 217–222. [Google Scholar] [CrossRef]
- Aikawa, N.; Kawasaki, Y. Clinical utility of the neutrophil elastase inhibitor sivelestat for the treatment of acute respiratory distress syndrome. Ther. Clin. Risk Manag. 2014, 10, 621–629. [Google Scholar] [CrossRef] [Green Version]
- Makino, H.; Kunisaki, C.; Kosaka, T.; Akiyama, H.; Morita, S.; Endo, I. Perioperative use of a neutrophil elastase inhibitor in video-assisted thoracoscopic oesophagectomy for cancer. Br. J. Surg. 2011, 98, 975–982. [Google Scholar] [CrossRef]
- Sahebnasagh, A.; Saghafi, F.; Safdari, M.; Khataminia, M.; Sadremomtaz, A.; Talaei, Z.; Rezai Ghaleno, H.; Bagheri, M.; Habtemariam, S.; Avan, R. Neutrophil elastase inhibitor (sivelestat) may be a promising therapeutic option for management of acute lung injury/acute respiratory distress syndrome or disseminated intravascular coagulation in COVID-19. J. Clin. Pharm. Ther. 2020, 45, 1515–1519. [Google Scholar] [CrossRef]
- Wang, Z.Q.; Chen, L.Q.; Yuan, Y.; Wang, W.P.; Niu, Z.X.; Yang, Y.S.; Cai, J. Effects of neutrophil elastase inhibitor in patients undergoing esophagectomy: A systematic review and meta-analysis. World J. Gastroenterol. 2015, 21, 3720–3730. [Google Scholar] [CrossRef]
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Shahzad, M.H.; Feng, L.; Su, X.; Brassard, A.; Dhoparee-Doomah, I.; Ferri, L.E.; Spicer, J.D.; Cools-Lartigue, J.J. Neutrophil Extracellular Traps in Cancer Therapy Resistance. Cancers 2022, 14, 1359. https://doi.org/10.3390/cancers14051359
Shahzad MH, Feng L, Su X, Brassard A, Dhoparee-Doomah I, Ferri LE, Spicer JD, Cools-Lartigue JJ. Neutrophil Extracellular Traps in Cancer Therapy Resistance. Cancers. 2022; 14(5):1359. https://doi.org/10.3390/cancers14051359
Chicago/Turabian StyleShahzad, Muhammad H., Lixuan Feng, Xin Su, Ariane Brassard, Iqraa Dhoparee-Doomah, Lorenzo E. Ferri, Jonathan D. Spicer, and Jonathan J. Cools-Lartigue. 2022. "Neutrophil Extracellular Traps in Cancer Therapy Resistance" Cancers 14, no. 5: 1359. https://doi.org/10.3390/cancers14051359