دورية أكاديمية

Neutrophil oxidative stress mediates obesity-associated vascular dysfunction and metastatic transmigration.

التفاصيل البيبلوغرافية
العنوان: Neutrophil oxidative stress mediates obesity-associated vascular dysfunction and metastatic transmigration.
المؤلفون: McDowell SAC; Rosalind and Morris Goodman Cancer Research Centre, McGill University, Montreal, Quebec, Canada.; Department of Physiology, Faculty of Medicine, McGill University, Montreal, Quebec, Canada., Luo RBE; Rosalind and Morris Goodman Cancer Research Centre, McGill University, Montreal, Quebec, Canada.; Department of Human Genetics, McGill University, Montreal, Quebec, Canada., Arabzadeh A; Rosalind and Morris Goodman Cancer Research Centre, McGill University, Montreal, Quebec, Canada., Doré S; Rosalind and Morris Goodman Cancer Research Centre, McGill University, Montreal, Quebec, Canada.; Department of Human Genetics, McGill University, Montreal, Quebec, Canada., Bennett NC; Rosalind and Morris Goodman Cancer Research Centre, McGill University, Montreal, Quebec, Canada.; Department of Physiology, Faculty of Medicine, McGill University, Montreal, Quebec, Canada., Breton V; Rosalind and Morris Goodman Cancer Research Centre, McGill University, Montreal, Quebec, Canada., Karimi E; Rosalind and Morris Goodman Cancer Research Centre, McGill University, Montreal, Quebec, Canada., Rezanejad M; Departments of Psychology and Computer Science, University of Toronto, Toronto, Ontario, Canada., Yang RR; Rosalind and Morris Goodman Cancer Research Centre, McGill University, Montreal, Quebec, Canada.; Department of Microbiology and Immunology, McGill University, Montreal, Quebec, Canada., Lach KD; Department of Pathology, Faculty of Medicine, McGill University, Montreal, Quebec, Canada., Issac MSM; Department of Pathology, Faculty of Medicine, McGill University, Montreal, Quebec, Canada., Samborska B; Rosalind and Morris Goodman Cancer Research Centre, McGill University, Montreal, Quebec, Canada., Perus LJM; Rosalind and Morris Goodman Cancer Research Centre, McGill University, Montreal, Quebec, Canada.; Department of Physiology, Faculty of Medicine, McGill University, Montreal, Quebec, Canada., Moldoveanu D; Rosalind and Morris Goodman Cancer Research Centre, McGill University, Montreal, Quebec, Canada.; Department of Biochemistry, McGill University, Montreal, Quebec, Canada., Wei Y; Rosalind and Morris Goodman Cancer Research Centre, McGill University, Montreal, Quebec, Canada., Fiset B; Rosalind and Morris Goodman Cancer Research Centre, McGill University, Montreal, Quebec, Canada., Rayes RF; Rosalind and Morris Goodman Cancer Research Centre, McGill University, Montreal, Quebec, Canada.; Department of Medicine, Division of Experimental Medicine, McGill University, Montreal, Quebec, Canada., Watson IR; Rosalind and Morris Goodman Cancer Research Centre, McGill University, Montreal, Quebec, Canada.; Department of Biochemistry, McGill University, Montreal, Quebec, Canada., Kazak L; Rosalind and Morris Goodman Cancer Research Centre, McGill University, Montreal, Quebec, Canada.; Department of Biochemistry, McGill University, Montreal, Quebec, Canada., Guiot MC; Department of Pathology, Faculty of Medicine, McGill University, Montreal, Quebec, Canada.; Montreal Neurological Institute, McGill University Health Centre, Montreal, Quebec, Canada., Fiset PO; Department of Pathology, Faculty of Medicine, McGill University, Montreal, Quebec, Canada., Spicer JD; Rosalind and Morris Goodman Cancer Research Centre, McGill University, Montreal, Quebec, Canada.; Department of Medicine, Division of Experimental Medicine, McGill University, Montreal, Quebec, Canada.; Department of Surgery, McGill University Health Centre, Montreal, Quebec, Canada., Dannenberg AJ; Department of Medicine, Weill Cornell Medical College, New York, New York, USA., Walsh LA; Rosalind and Morris Goodman Cancer Research Centre, McGill University, Montreal, Quebec, Canada. logan.walsh@mcgill.ca.; Department of Human Genetics, McGill University, Montreal, Quebec, Canada. logan.walsh@mcgill.ca., Quail DF; Rosalind and Morris Goodman Cancer Research Centre, McGill University, Montreal, Quebec, Canada. daniela.quail@mcgill.ca.; Department of Physiology, Faculty of Medicine, McGill University, Montreal, Quebec, Canada. daniela.quail@mcgill.ca.; Department of Medicine, Division of Experimental Medicine, McGill University, Montreal, Quebec, Canada. daniela.quail@mcgill.ca.
المصدر: Nature cancer [Nat Cancer] 2021 May; Vol. 2 (5), pp. 545-562. Date of Electronic Publication: 2021 May 03.
نوع المنشور: Journal Article; Research Support, Non-U.S. Gov't
اللغة: English
بيانات الدورية: Publisher: Nature Publishing Group Country of Publication: England NLM ID: 101761119 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 2662-1347 (Electronic) Linking ISSN: 26621347 NLM ISO Abbreviation: Nat Cancer Subsets: MEDLINE
أسماء مطبوعة: Original Publication: [London] : Nature Publishing Group, [2020]-
مواضيع طبية MeSH: Breast Neoplasms*/metabolism , Lung Neoplasms*/metabolism, Animals ; Catalase/metabolism ; Female ; Humans ; Mice ; Neutrophils/metabolism ; Obesity/complications ; Oxidative Stress
مستخلص: Metastasis is the leading cause of cancer-related deaths, and obesity is associated with increased breast cancer (BC) metastasis. Preclinical studies have shown that obese adipose tissue induces lung neutrophilia associated with enhanced BC metastasis to this site. Here we show that obesity leads to neutrophil-dependent impairment of vascular integrity through loss of endothelial adhesions, enabling cancer cell extravasation into the lung. Mechanistically, neutrophil-produced reactive oxygen species in obese mice increase neutrophil extracellular DNA traps (NETs) and weaken endothelial junctions, facilitating the influx of tumor cells from the peripheral circulation. In vivo treatment with catalase, NET inhibitors or genetic deletion of Nos2 reversed this effect in preclinical models of obesity. Imaging mass cytometry of lung metastasis samples from patients with cancer revealed an enrichment in neutrophils with low catalase levels correlating with elevated body mass index. Our data provide insights into potentially targetable mechanisms that underlie the progression of BC in the obese population.
(© 2021. The Author(s), under exclusive licence to Springer Nature America, Inc.)
References: Lauby-Secretan, B. et al. Body fatness and cancer-viewpoint of the IARC working group. N. Engl. J. Med. 375, 794–798 (2016). (PMID: 27557308675486110.1056/NEJMsr1606602)
Calle, E. E., Rodriguez, C., Walker-Thurmond, K. & Thun, M. J. Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. N. Engl. J. Med. 348, 1625–1638 (2003). (PMID: 1271173710.1056/NEJMoa021423)
Risk, N. C. D. Factor collaboration. Trends in adult body-mass index in 200 countries from 1975 to 2014: a pooled analysis of 1698 population-based measurement studies with 19.2 million participants. Lancet 387, 1377–1396 (2016). (PMID: 10.1016/S0140-6736(16)30054-X)
Calle, E. E. & Kaaks, R. Overweight, obesity and cancer: epidemiological evidence and proposed mechanisms. Nat. Rev. Cancer 4, 579–591 (2004). (PMID: 1528673810.1038/nrc1408)
Ligibel, J. A. et al. American Society of Clinical Oncology position statement on obesity and cancer. J. Clin. Oncol. 32, 3568–3574 (2014). (PMID: 25273035497923710.1200/JCO.2014.58.4680)
Weigelt, B., Peterse, J. L. & van ‘t Veer, L. J. Breast cancer metastasis: markers and models. Nat. Rev. Cancer 5, 591–602 (2005). (PMID: 1605625810.1038/nrc1670)
Ewertz, M. et al. Effect of obesity on prognosis after early-stage breast cancer. J. Clin. Oncol. 29, 25–31 (2011). (PMID: 2111585610.1200/JCO.2010.29.7614)
Osman, M. A. & Hennessy, B. T. Obesity correlation with metastases development and response to first-line metastatic chemotherapy in breast cancer. Clin. Med. Insights Oncol. 9, 105–112 (2015). (PMID: 26628862465943910.4137/CMO.S32812)
Olson, O. C., Quail, D. F. & Joyce, J. A. Obesity and the tumor microenvironment. Science 358, 1130–1131 (2017). (PMID: 2919189310.1126/science.aao5801)
Quail, D. F. et al. Obesity alters the lung myeloid cell landscape to enhance breast cancer metastasis through IL5 and GM-CSF. Nat. Cell Biol. 19, 974–987 (2017). (PMID: 28737771675992210.1038/ncb3578)
Adams, T. D. et al. Long-term mortality after gastric bypass surgery. N. Engl. J. Med. 357, 753–761 (2007). (PMID: 1771540910.1056/NEJMoa066603)
Garcia-Alonso, L., Holland, C. H., Ibrahim, M. M., Turei, D. & Saez-Rodriguez, J. Benchmark and integration of resources for the estimation of human transcription factor activities. Genome Res. 29, 1363–1375 (2019). (PMID: 31340985667371810.1101/gr.240663.118)
Czymai, T. et al. FOXO3 modulates endothelial gene expression and function by classical and alternative mechanisms. J. Biol. Chem. 285, 10163–10178 (2010). (PMID: 20123982285622210.1074/jbc.M109.056663)
Potente, M. et al. Involvement of Foxo transcription factors in angiogenesis and postnatal neovascularization. J. Clin. Invest. 115, 2382–2392 (2005). (PMID: 16100571118403710.1172/JCI23126)
Sang, T., Cao, Q., Wang, Y., Liu, F. & Chen, S. Overexpression or silencing of FOXO3a affects proliferation of endothelial progenitor cells and expression of cell cycle regulatory proteins. PLoS ONE 9, e101703 (2014). (PMID: 25093499412233810.1371/journal.pone.0101703)
Weber, C., Fraemohs, L. & Dejana, E. The role of junctional adhesion molecules in vascular inflammation. Nat. Rev. Immunol. 7, 467–477 (2007). (PMID: 1752575510.1038/nri2096)
Phillipson, M. & Kubes, P. The neutrophil in vascular inflammation. Nat. Med. 17, 1381–1390 (2011). (PMID: 22064428709583010.1038/nm.2514)
Boivin, G. et al. Durable and controlled depletion of neutrophils in mice. Nat. Commun. 11, 2762 (2020). (PMID: 32488020726552510.1038/s41467-020-16596-9)
Gomez-Moreno, D., Adrover, J. M. & Hidalgo, A. Neutrophils as effectors of vascular inflammation. Eur. J. Clin. Invest. 48, e12940 (2018). (PMID: 2968273110.1111/eci.12940)
Rohn, T. T. et al. Priming of human neutrophils by peroxynitrite: potential role in enhancement of the local inflammatory response. J. Leukoc. Biol. 65, 59–70 (1999). (PMID: 988624710.1002/jlb.65.1.59)
Manda-Handzlik, A. et al. Nitric oxide and peroxynitrite trigger and enhance release of neutrophil extracellular traps. Cell. Mol. Life Sci. 77, 3059–3075 (2020). (PMID: 3165018510.1007/s00018-019-03331-x)
Yabe, Y., Nishikawa, M., Tamada, A., Takakura, Y. & Hashida, M. Targeted delivery and improved therapeutic potential of catalase by chemical modification: combination with superoxide dismutase derivatives. J. Pharmacol. Exp. Ther. 289, 1176–1184 (1999). (PMID: 10215702)
Chen, A. Y., Lu, J. M., Yao, Q. & Chen, C. Entacapone is an antioxidant more potent than vitamin C and vitamin E for scavenging of hypochlorous acid and peroxynitrite, and the inhibition of oxidative stress-induced cell death. Med. Sci. Monit. 22, 687–696 (2016). (PMID: 26927838477724210.12659/MSM.896462)
Song, E. et al. Deamidated lipocalin-2 induces endothelial dysfunction and hypertension in dietary obese mice. J. Am. Heart Assoc. 3, e000837 (2014). (PMID: 24721803418750510.1161/JAHA.114.000837)
Florence, J. M., Krupa, A., Booshehri, L. M., Allen, T. C. & Kurdowska, A. K. Metalloproteinase-9 contributes to endothelial dysfunction in atherosclerosis via protease activated receptor-1. PLoS ONE 12, e0171427 (2017). (PMID: 28166283529321910.1371/journal.pone.0171427)
Saha, P. et al. Bacterial siderophores hijack neutrophil functions. J. Immunol. 198, 4293–4303 (2017). (PMID: 2843214510.4049/jimmunol.1700261)
Ward, P. P., Mendoza-Meneses, M., Park, P. W. & Conneely, O. M. Stimulus-dependent impairment of the neutrophil oxidative burst response in lactoferrin-deficient mice. Am. J. Pathol. 172, 1019–1029 (2008). (PMID: 18321995227641010.2353/ajpath.2008.061145)
Metzler, K. D. et al. Myeloperoxidase is required for neutrophil extracellular trap formation: implications for innate immunity. Blood 117, 953–959 (2011). (PMID: 20974672303508310.1182/blood-2010-06-290171)
Clark, S. R. et al. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat. Med. 13, 463–469 (2007). (PMID: 1738464810.1038/nm1565)
Albrengues, J. et al. Neutrophil extracellular traps produced during inflammation awaken dormant cancer cells in mice. Science 361, eaao4227 (2018). (PMID: 30262472677785010.1126/science.aao4227)
Szczerba, B. M. et al. Neutrophils escort circulating tumour cells to enable cell cycle progression. Nature 566, 553–557 (2019). (PMID: 3072849610.1038/s41586-019-0915-y)
Perreault, M. & Marette, A. Targeted disruption of inducible nitric oxide synthase protects against obesity-linked insulin resistance in muscle. Nat. Med. 7, 1138–1143 (2001). (PMID: 1159043810.1038/nm1001-1138)
Amano, S. U. et al. Local proliferation of macrophages contributes to obesity-associated adipose tissue inflammation. Cell Metab. 19, 162–171 (2014). (PMID: 2437421810.1016/j.cmet.2013.11.017)
Kichenadasse, G. et al. Association between body mass index and overall survival with immune checkpoint inhibitor therapy for advanced non-small cell lung cancer. JAMA Oncol. 6, 512–518 (2019). (PMID: 699085510.1001/jamaoncol.2019.5241)
McQuade, J. L. et al. Association of body-mass index and outcomes in patients with metastatic melanoma treated with targeted therapy, immunotherapy, or chemotherapy: a retrospective, multicohort analysis. Lancet Oncol. 19, 310–322 (2018). (PMID: 29449192584002910.1016/S1470-2045(18)30078-0)
Domigan, N. M., Charlton, T. S., Duncan, M. W., Winterbourn, C. C. & Kettle, A. J. Chlorination of tyrosyl residues in peptides by myeloperoxidase and human neutrophils. J. Biol. Chem. 270, 16542–16548 (1995). (PMID: 762245910.1074/jbc.270.28.16542)
Harris, I. S. & DeNicola, G. M. The complex interplay between antioxidants and ROS in cancer. Trends Cell Biol. 30, 440–451 (2020).
Blot, W. J. et al. Nutrition intervention trials in Linxian, China: supplementation with specific vitamin/mineral combinations, cancer incidence, and disease-specific mortality in the general population. J. Natl Cancer Inst. 85, 1483–1492 (1993).
Keaney, J. F. Jr. et al. Obesity and systemic oxidative stress: clinical correlates of oxidative stress in the Framingham Study. Arterioscler. Thromb. Vasc. Biol. 23, 434–439 (2003). (PMID: 1261569310.1161/01.ATV.0000058402.34138.11)
Aleman, J. O. et al. Effects of rapid weight loss on systemic and adipose tissue inflammation and metabolism in obese postmenopausal women. J. Endocr. Soc. 1, 625–637 (2017). (PMID: 29264516568662410.1210/js.2017-00020)
Aruoma, O. I., Halliwell, B., Hoey, B. M. & Butler, J. The antioxidant action of N-acetylcysteine: its reaction with hydrogen peroxide, hydroxyl radical, superoxide, and hypochlorous acid. Free Radic. Biol. Med. 6, 593–597 (1989). (PMID: 254686410.1016/0891-5849(89)90066-X)
Nagareddy, P. R. et al. Adipose tissue macrophages promote myelopoiesis and monocytosis in obesity. Cell Metab. 19, 821–835 (2014). (PMID: 24807222404893910.1016/j.cmet.2014.03.029)
Herishanu, Y., Rogowski, O., Polliack, A. & Marilus, R. Leukocytosis in obese individuals: possible link in patients with unexplained persistent neutrophilia. Eur. J. Haematol. 76, 516–520 (2006). (PMID: 1669677510.1111/j.1600-0609.2006.00658.x)
Gentles, A. J. et al. The prognostic landscape of genes and infiltrating immune cells across human cancers. Nat. Med. 21, 938–945 (2015). (PMID: 26193342485285710.1038/nm.3909)
Coffelt, S. B., Wellenstein, M. D. & de Visser, K. E. Neutrophils in cancer: neutral no more. Nat. Rev. Cancer 16, 431–446 (2016). (PMID: 2728224910.1038/nrc.2016.52)
Kwak, H. J. et al. Myeloid cell-derived reactive oxygen species externally regulate the proliferation of myeloid progenitors in emergency granulopoiesis. Immunity 42, 159–171 (2015). (PMID: 25579427430352610.1016/j.immuni.2014.12.017)
Adrover, J. M. et al. A neutrophil timer coordinates immune defense and vascular protection. Immunity 50, 390–402 e310 (2019). (PMID: 3070974110.1016/j.immuni.2019.01.002)
Ode, Y., Aziz, M. & Wang, P. CIRP increases ICAM-1(+) phenotype of neutrophils exhibiting elevated iNOS and NETs in sepsis. J. Leukoc. Biol. 103, 693–707 (2018). (PMID: 2934538010.1002/JLB.3A0817-327RR)
Bronte, V. et al. Recommendations for myeloid-derived suppressor cell nomenclature and characterization standards. Nat. Commun. 7, 12150 (2016). (PMID: 27381735493581110.1038/ncomms12150)
Xia, S. et al. Gr-1 + CD11b + myeloid-derived suppressor cells suppress inflammation and promote insulin sensitivity in obesity. J. Biol. Chem. 286, 23591–23599 (2011). (PMID: 21592961312312210.1074/jbc.M111.237123)
Clements, V. K. et al. Frontline science: high fat diet and leptin promote tumor progression by inducing myeloid-derived suppressor cells. J. Leukoc. Biol. 103, 395–407 (2018). (PMID: 2934534210.1002/JLB.4HI0517-210R)
Ng, L. G., Ostuni, R. & Hidalgo, A. Heterogeneity of neutrophils. Nat. Rev. Immunol. 19, 255–265 (2019). (PMID: 3081634010.1038/s41577-019-0141-8)
Eiserich, J. P. et al. Myeloperoxidase, a leukocyte-derived vascular NO oxidase. Science 296, 2391–2394 (2002). (PMID: 1208944210.1126/science.1106830)
Wang, Q. et al. Myeloperoxidase deletion prevents high-fat diet-induced obesity and insulin resistance. Diabetes 63, 4172–4185 (2014). (PMID: 25024373423800910.2337/db14-0026)
Zhou, J., Wang, Q., Ding, Y. & Zou, M. H. Hypochlorous acid via peroxynitrite activates protein kinase Ctheta and insulin resistance in adipocytes. J. Mol. Endocrinol. 54, 25–37 (2015). (PMID: 25381390426120410.1530/JME-14-0213)
Kessenbrock, K. et al. Netting neutrophils in autoimmune small-vessel vasculitis. Nat. Med. 15, 623–625 (2009). (PMID: 19448636276008310.1038/nm.1959)
Moorthy, A. N., Tan, K. B., Wang, S., Narasaraju, T. & Chow, V. T. Effect of high-fat diet on the formation of pulmonary neutrophil extracellular traps during influenza pneumonia in BALB/c Mice. Front. Immunol. 7, 289 (2016).
Tohme, S. et al. Neutrophil extracellular traps promote the development and progression of liver metastases after surgical stress. Cancer Res. 76, 1367–1380 (2016). (PMID: 26759232479439310.1158/0008-5472.CAN-15-1591)
Cools-Lartigue, J. et al. Neutrophil extracellular traps sequester circulating tumor cells and promote metastasis. J. Clin. Invest. 123, 3446–3458 (2013).
Brotfain, E. et al. Neutrophil functions in morbidly obese subjects. Clin. Exp. Immunol. 181, 156–163 (2015). (PMID: 25809538446916610.1111/cei.12631)
Shah, D. et al. Obesity-induced adipokine imbalance impairs mouse pulmonary vascular endothelial function and primes the lung for injury. Sci. Rep. 5, 11362 (2015). (PMID: 26068229446432310.1038/srep11362)
Chedid, P. et al. Adiponectin and its globular fragment differentially modulate the oxidative burst of primary human phagocytes. Am. J. Pathol. 180, 682–692 (2012). (PMID: 2211903810.1016/j.ajpath.2011.10.013)
Tilg, H. & Moschen, A. R. Adipocytokines: mediators linking adipose tissue, inflammation and immunity. Nat. Rev. Immunol. 6, 772–783 (2006). (PMID: 1699851010.1038/nri1937)
Miyazaki, Y. et al. Effect of pioglitazone on circulating adipocytokine levels and insulin sensitivity in type 2 diabetic patients. J. Clin. Endocrinol. Metab. 89, 4312–4319 (2004). (PMID: 1535602610.1210/jc.2004-0190)
Quail, D. F. & Dannenberg, A. J. The obese adipose tissue microenvironment in cancer development and progression. Nat. Rev. Endocrinol. 15, 139–154 (2019). (PMID: 30459447637417610.1038/s41574-018-0126-x)
Guy, C. T., Cardiff, R. D. & Muller, W. J. Induction of mammary tumors by expression of polyomavirus middle T oncogene: a transgenic mouse model for metastatic disease. Mol. Cell. Biol. 12, 954–961 (1992). (PMID: 1312220369527)
Gibby, K. et al. Early vascular deficits are correlated with delayed mammary tumorigenesis in the MMTV-PyMT transgenic mouse following genetic ablation of the NG2 proteoglycan. Breast Cancer Res. 14, R67 (2012). (PMID: 22531600344640210.1186/bcr3174)
Ewens, A., Mihich, E. & Ehrke, M. J. Distant metastasis from subcutaneously grown E0771 medullary breast adenocarcinoma. Anticancer Res. 25, 3905–3915 (2005). (PMID: 16312045)
Nishikawa, M. et al. Inhibition of metastatic tumor growth by targeted delivery of antioxidant enzymes. J. Control. Release 109, 101–107 (2005). (PMID: 1625623810.1016/j.jconrel.2005.09.017)
Kaushik, N. et al. Responses of solid tumor cells in DMEM to reactive oxygen species generated by non-thermal plasma and chemically induced ROS systems. Sci. Rep. 5, 8587 (2015).
Avci, B., Bahadir, A., Tuncel, O. K. & Bilgici, B. Influence of alpha-tocopherol and alpha-lipoic acid on bisphenol-A-induced oxidative damage in liver and ovarian tissue of rats. Toxicol. Ind. Health 32, 1381–1390 (2016). (PMID: 2554837510.1177/0748233714563433)
Davie, S. A. et al. Effects of FVB/NJ and C57Bl/6J strain backgrounds on mammary tumor phenotype in inducible nitric oxide synthase deficient mice. Transgenic Res. 16, 193–201 (2007). (PMID: 17206489182941810.1007/s11248-006-9056-9)
Quail, D. F. et al. The tumor microenvironment underlies acquired resistance to CSF-1R inhibition in gliomas. Science 352, aad3018 (2016). (PMID: 27199435545062910.1126/science.aad3018)
Huang, Y. et al. Pulmonary vascular destabilization in the premetastatic phase facilitates lung metastasis. Cancer Res. 69, 7529–7537 (2009). (PMID: 1977344710.1158/0008-5472.CAN-08-4382)
Najmeh, S., Cools-Lartigue, J., Giannias, B., Spicer, J. & Ferri, L. E. Simplified human neutrophil extracellular traps (NETs) isolation and handling. J. Vis. Exp. 16, 52687 (2015).
Rayes, R. F. et al. Primary tumors induce neutrophil extracellular traps with targetable metastasis promoting effects. JCI Insight 5, e128008 (2019). (PMID: 10.1172/jci.insight.128008)
Yoo, D. G., Floyd, M., Winn, M., Moskowitz, S. M. & Rada, B. NET formation induced by Pseudomonas aeruginosa cystic fibrosis isolates measured as release of myeloperoxidase-DNA and neutrophil elastase-DNA complexes. Immunol. Lett. 160, 186–194 (2014). (PMID: 2467096610.1016/j.imlet.2014.03.003)
Park, J. et al. Cancer cells induce metastasis-supporting neutrophil extracellular DNA traps. Sci. Transl. Med. 8, 361ra138 (2016). (PMID: 27798263555090010.1126/scitranslmed.aag1711)
Robinson, B. D., Shaji, C. A., Lomas, A. & Tharakan, B. Measurement of microvascular endothelial barrier dysfunction and hyperpermeability in vitro. Methods Mol. Biol. 1717, 237–242 (2018). (PMID: 2946859710.1007/978-1-4939-7526-6_19)
Chan, T. F. & Vese, L. A. Active contours without edges. IEEE Trans. Image Process. 10, 266–277 (2001). (PMID: 1824961710.1109/83.902291)
معلومات مُعتمدة: PJT-159742 Canada CIHR; PJT-162137 Canada CIHR
المشرفين على المادة: EC 1.11.1.6 (Catalase)
تواريخ الأحداث: Date Created: 20220205 Date Completed: 20220419 Latest Revision: 20221027
رمز التحديث: 20221213
DOI: 10.1038/s43018-021-00194-9
PMID: 35122017
قاعدة البيانات: MEDLINE
الوصف
تدمد:2662-1347
DOI:10.1038/s43018-021-00194-9