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Published in: Inflammation Research 5/2017

Open Access 01-05-2017 | Review

NETosis provides the link between activation of neutrophils on hemodialysis membrane and comorbidities in dialyzed patients

Authors: Marie Korabecna, Vladimir Tesar

Published in: Inflammation Research | Issue 5/2017

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Abstract

Introduction

Neutrophil extracellular traps (NETs) are formed by activated neutrophils during the process of NETosis in which the nuclear material is released into extracellular space, including DNA molecules, citrullinated histones, and neutrophil granule enzymes, such as elastase. This material forms networks that are able not only to physically entrap bacteria but also to provide elevated concentration of bactericidal components. Over the last years, it has become clear that NETs can also be formed under numerous sterile inflammatory conditions, i.e., thrombosis, cancer, SLE, atherosclerosis, and diabetes.

Method

We reviewed studies published until July 2016 to find possible associations between elevated cell-free DNA levels in dialyzed patients and the process of NETosis and its consequences.

Results

The process of NETosis, its elevated activation, or impaired clearance provides the link between clinical conditions and elevated levels of cell-free DNA found in plasma after the hemodialytic procedure which itself is able to activate neutrophils via platelets and ROS formation. NETs stimulate thrombosis and endothelial damage, and their formation may contribute to the development of spectrum of comorbidities described in dialyzed patients.

Conclusion

The study of plasma cell-free DNA levels together with markers of NETosis could contribute to the evaluation of the influence of hemodialysis on the immune system of patients.
Literature
4.
go back to reference Jeong JC, Kim JE, Gu JY, Yoo HJ, Ryu JW, Kim DK, et al. Significance of the DNA-histone complex level as a predictor of major adverse cardiovascular events in hemodialysis patients: the effect of uremic toxin on dna-histone complex formation. Blood Purif. 2016;41(1–3):64–71. doi:10.1159/000440974 (PubMed PMID: 26517236).PubMed Jeong JC, Kim JE, Gu JY, Yoo HJ, Ryu JW, Kim DK, et al. Significance of the DNA-histone complex level as a predictor of major adverse cardiovascular events in hemodialysis patients: the effect of uremic toxin on dna-histone complex formation. Blood Purif. 2016;41(1–3):64–71. doi:10.​1159/​000440974 (PubMed PMID: 26517236).PubMed
8.
go back to reference Wong SL, Demers M, Martinod K, Gallant M, Wang Y, Goldfine AB, et al. Diabetes primes neutrophils to undergo NETosis, which impairs wound healing. Nat Med. 2015;21(7):815–9. doi:10.1038/nm.3887 (PubMed PMID: 26076037; PubMed Central PMCID: PMC4631120).CrossRefPubMedPubMedCentral Wong SL, Demers M, Martinod K, Gallant M, Wang Y, Goldfine AB, et al. Diabetes primes neutrophils to undergo NETosis, which impairs wound healing. Nat Med. 2015;21(7):815–9. doi:10.​1038/​nm.​3887 (PubMed PMID: 26076037; PubMed Central PMCID: PMC4631120).CrossRefPubMedPubMedCentral
9.
go back to reference Menegazzo L, Ciciliot S, Poncina N, Mazzucato M, Persano M, Bonora B, et al. NETosis is induced by high glucose and associated with type 2 diabetes. Acta Diabetol. 2015;52(3):497–503. doi:10.1007/s00592-014-0676-x (PubMed PMID: 25387570).CrossRefPubMed Menegazzo L, Ciciliot S, Poncina N, Mazzucato M, Persano M, Bonora B, et al. NETosis is induced by high glucose and associated with type 2 diabetes. Acta Diabetol. 2015;52(3):497–503. doi:10.​1007/​s00592-014-0676-x (PubMed PMID: 25387570).CrossRefPubMed
10.
go back to reference Borissoff JI, Joosen IA, Versteylen MO, Brill A, Fuchs TA, Savchenko AS, et al. Elevated levels of circulating DNA and chromatin are independently associated with severe coronary atherosclerosis and a prothrombotic state. Arterioscler Thromb Vasc Biol. 2013;33(8):2032–40. doi:10.1161/ATVBAHA.113.301627 (PubMed PMID: 23818485; PubMed Central PMCID: PMC3806482).CrossRefPubMedPubMedCentral Borissoff JI, Joosen IA, Versteylen MO, Brill A, Fuchs TA, Savchenko AS, et al. Elevated levels of circulating DNA and chromatin are independently associated with severe coronary atherosclerosis and a prothrombotic state. Arterioscler Thromb Vasc Biol. 2013;33(8):2032–40. doi:10.​1161/​ATVBAHA.​113.​301627 (PubMed PMID: 23818485; PubMed Central PMCID: PMC3806482).CrossRefPubMedPubMedCentral
11.
go back to reference Hakkim A, Furnrohr BG, Amann K, Laube B, Abed UA, Brinkmann V, et al. Impairment of neutrophil extracellular trap degradation is associated with lupus nephritis. Proc Natl Acad Sci USA. 2010;107(21):9813–8. doi:10.1073/pnas.0909927107 (PubMed PMID: 20439745; PubMed Central PMCID: PMC2906830).CrossRefPubMedPubMedCentral Hakkim A, Furnrohr BG, Amann K, Laube B, Abed UA, Brinkmann V, et al. Impairment of neutrophil extracellular trap degradation is associated with lupus nephritis. Proc Natl Acad Sci USA. 2010;107(21):9813–8. doi:10.​1073/​pnas.​0909927107 (PubMed PMID: 20439745; PubMed Central PMCID: PMC2906830).CrossRefPubMedPubMedCentral
14.
go back to reference Korabecna M, Opatrna S, Wirth J, Rulcova K, Eiselt J, Sefrna F, et al. Cell-free plasma DNA during peritoneal dialysis and hemodialysis and in patients with chronic kidney disease. Ann N Y Acad Sci. 2008;1137:296–301. doi:10.1196/annals.1448.014 (PubMed PMID: 18837963).CrossRefPubMed Korabecna M, Opatrna S, Wirth J, Rulcova K, Eiselt J, Sefrna F, et al. Cell-free plasma DNA during peritoneal dialysis and hemodialysis and in patients with chronic kidney disease. Ann N Y Acad Sci. 2008;1137:296–301. doi:10.​1196/​annals.​1448.​014 (PubMed PMID: 18837963).CrossRefPubMed
16.
go back to reference Garcia Moreira V, de la Cera Martinez T, Gago Gonzalez E, Prieto Garcia B, Alvarez Menendez FV. Increase in and clearance of cell-free plasma DNA in hemodialysis quantified by real-time PCR. Clin Chem Lab Med. 2006;44(12):1410–5. doi:10.1515/CCLM.2006.252 (PubMed PMID: 17163815).CrossRefPubMed Garcia Moreira V, de la Cera Martinez T, Gago Gonzalez E, Prieto Garcia B, Alvarez Menendez FV. Increase in and clearance of cell-free plasma DNA in hemodialysis quantified by real-time PCR. Clin Chem Lab Med. 2006;44(12):1410–5. doi:10.​1515/​CCLM.​2006.​252 (PubMed PMID: 17163815).CrossRefPubMed
19.
go back to reference Parker H, Albrett AM, Kettle AJ, Winterbourn CC. Myeloperoxidase associated with neutrophil extracellular traps is active and mediates bacterial killing in the presence of hydrogen peroxide. J Leukoc Biol. 2012;91(3):369–76. doi:10.1189/jlb.0711387 (PubMed PMID: 22131345).CrossRefPubMed Parker H, Albrett AM, Kettle AJ, Winterbourn CC. Myeloperoxidase associated with neutrophil extracellular traps is active and mediates bacterial killing in the presence of hydrogen peroxide. J Leukoc Biol. 2012;91(3):369–76. doi:10.​1189/​jlb.​0711387 (PubMed PMID: 22131345).CrossRefPubMed
20.
go back to reference Bianchi M, Niemiec MJ, Siler U, Urban CF, Reichenbach J. Restoration of anti-Aspergillus defense by neutrophil extracellular traps in human chronic granulomatous disease after gene therapy is calprotectin-dependent. J Allergy Clin Immunol. 2011;127(5):1243–52. doi:10.1016/j.jaci.2011.01.021 (PubMed PMID: 21376380).CrossRefPubMed Bianchi M, Niemiec MJ, Siler U, Urban CF, Reichenbach J. Restoration of anti-Aspergillus defense by neutrophil extracellular traps in human chronic granulomatous disease after gene therapy is calprotectin-dependent. J Allergy Clin Immunol. 2011;127(5):1243–52. doi:10.​1016/​j.​jaci.​2011.​01.​021 (PubMed PMID: 21376380).CrossRefPubMed
21.
go back to reference Kroemer G, Galluzzi L, Vandenabeele P, Abrams J, Alnemri ES, Baehrecke EH, et al. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ. 2009;16(1):3–11. doi:10.1038/cdd.2008.150 (PubMed PMID: 18846107; PubMed Central PMCID: PMC2744427).CrossRefPubMed Kroemer G, Galluzzi L, Vandenabeele P, Abrams J, Alnemri ES, Baehrecke EH, et al. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ. 2009;16(1):3–11. doi:10.​1038/​cdd.​2008.​150 (PubMed PMID: 18846107; PubMed Central PMCID: PMC2744427).CrossRefPubMed
22.
go back to reference Vanden Berghe T, Linkermann A, Jouan-Lanhouet S, Walczak H, Vandenabeele P. Regulated necrosis: the expanding network of non-apoptotic cell death pathways. Nat Rev Mol Cell Biol. 2014;15(2):135–47. doi:10.1038/nrm3737 (PubMed PMID: 24452471).CrossRefPubMed Vanden Berghe T, Linkermann A, Jouan-Lanhouet S, Walczak H, Vandenabeele P. Regulated necrosis: the expanding network of non-apoptotic cell death pathways. Nat Rev Mol Cell Biol. 2014;15(2):135–47. doi:10.​1038/​nrm3737 (PubMed PMID: 24452471).CrossRefPubMed
23.
go back to reference Hoffmann JH, Schaekel K, Gaiser MR, Enk AH, Hadaschik EN. Inter-individual variation of NETosis in healthy donors: introduction and application of a refined method for extracellular trap quantification. Exp Dermatol. 2016. doi:10.1111/exd.13125 (PubMed PMID: 27307108).PubMed Hoffmann JH, Schaekel K, Gaiser MR, Enk AH, Hadaschik EN. Inter-individual variation of NETosis in healthy donors: introduction and application of a refined method for extracellular trap quantification. Exp Dermatol. 2016. doi:10.​1111/​exd.​13125 (PubMed PMID: 27307108).PubMed
27.
go back to reference Hakkim A, Fuchs TA, Martinez NE, Hess S, Prinz H, Zychlinsky A, et al. Activation of the Raf-MEK-ERK pathway is required for neutrophil extracellular trap formation. Nat Chem Biol. 2011;7(2):75–7. doi:10.1038/nchembio.496 (PubMed PMID: 21170021).CrossRefPubMed Hakkim A, Fuchs TA, Martinez NE, Hess S, Prinz H, Zychlinsky A, et al. Activation of the Raf-MEK-ERK pathway is required for neutrophil extracellular trap formation. Nat Chem Biol. 2011;7(2):75–7. doi:10.​1038/​nchembio.​496 (PubMed PMID: 21170021).CrossRefPubMed
28.
29.
30.
31.
32.
go back to reference Neeli I, Khan SN, Radic M. Histone deimination as a response to inflammatory stimuli in neutrophils. J Immunol. 2008;180(3):1895–902 (PubMed PMID: 18209087).CrossRefPubMed Neeli I, Khan SN, Radic M. Histone deimination as a response to inflammatory stimuli in neutrophils. J Immunol. 2008;180(3):1895–902 (PubMed PMID: 18209087).CrossRefPubMed
33.
go back to reference Wang Y, Li M, Stadler S, Correll S, Li P, Wang D, et al. Histone hypercitrullination mediates chromatin decondensation and neutrophil extracellular trap formation. J Cell Biol. 2009;184(2):205–13. doi:10.1083/jcb.200806072 (PubMed PMID: 19153223; PubMed Central PMCID: PMC2654299).CrossRefPubMedPubMedCentral Wang Y, Li M, Stadler S, Correll S, Li P, Wang D, et al. Histone hypercitrullination mediates chromatin decondensation and neutrophil extracellular trap formation. J Cell Biol. 2009;184(2):205–13. doi:10.​1083/​jcb.​200806072 (PubMed PMID: 19153223; PubMed Central PMCID: PMC2654299).CrossRefPubMedPubMedCentral
36.
go back to reference Pilsczek FH, Salina D, Poon KK, Fahey C, Yipp BG, Sibley CD, et al. A novel mechanism of rapid nuclear neutrophil extracellular trap formation in response to Staphylococcus aureus. J Immunol. 2010;185(12):7413–25. doi:10.4049/jimmunol.1000675 (PubMed PMID: 21098229).CrossRefPubMed Pilsczek FH, Salina D, Poon KK, Fahey C, Yipp BG, Sibley CD, et al. A novel mechanism of rapid nuclear neutrophil extracellular trap formation in response to Staphylococcus aureus. J Immunol. 2010;185(12):7413–25. doi:10.​4049/​jimmunol.​1000675 (PubMed PMID: 21098229).CrossRefPubMed
37.
go back to reference Yipp BG, Petri B, Salina D, Jenne CN, Scott BN, Zbytnuik LD, et al. Infection-induced NETosis is a dynamic process involving neutrophil multitasking in vivo. Nat Med. 2012;18(9):1386–93. doi:10.1038/nm.2847 (PubMed PMID: 22922410; PubMed Central PMCID: PMC4529131).CrossRefPubMedPubMedCentral Yipp BG, Petri B, Salina D, Jenne CN, Scott BN, Zbytnuik LD, et al. Infection-induced NETosis is a dynamic process involving neutrophil multitasking in vivo. Nat Med. 2012;18(9):1386–93. doi:10.​1038/​nm.​2847 (PubMed PMID: 22922410; PubMed Central PMCID: PMC4529131).CrossRefPubMedPubMedCentral
38.
go back to reference Clark SR, Ma AC, Tavener SA, McDonald B, Goodarzi Z, Kelly MM, et al. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat Med. 2007;13(4):463–9. doi:10.1038/nm1565 (PubMed PMID: 17384648).CrossRefPubMed Clark SR, Ma AC, Tavener SA, McDonald B, Goodarzi Z, Kelly MM, et al. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat Med. 2007;13(4):463–9. doi:10.​1038/​nm1565 (PubMed PMID: 17384648).CrossRefPubMed
39.
go back to reference Yousefi S, Mihalache C, Kozlowski E, Schmid I, Simon HU. Viable neutrophils release mitochondrial DNA to form neutrophil extracellular traps. Cell Death Differ. 2009;16(11):1438–44. doi:10.1038/cdd.2009.96 (PubMed PMID: 19609275).CrossRefPubMed Yousefi S, Mihalache C, Kozlowski E, Schmid I, Simon HU. Viable neutrophils release mitochondrial DNA to form neutrophil extracellular traps. Cell Death Differ. 2009;16(11):1438–44. doi:10.​1038/​cdd.​2009.​96 (PubMed PMID: 19609275).CrossRefPubMed
40.
44.
go back to reference Jimenez-Alcazar M, Napirei M, Panda R, Kohler EC, Kremer Hovinga JA, Mannherz HG, et al. Impaired DNase1-mediated degradation of neutrophil extracellular traps is associated with acute thrombotic microangiopathies. J Thromb Haemost. 2015;13(5):732–42. doi:10.1111/jth.12796 (PubMed PMID: 25418346).CrossRefPubMed Jimenez-Alcazar M, Napirei M, Panda R, Kohler EC, Kremer Hovinga JA, Mannherz HG, et al. Impaired DNase1-mediated degradation of neutrophil extracellular traps is associated with acute thrombotic microangiopathies. J Thromb Haemost. 2015;13(5):732–42. doi:10.​1111/​jth.​12796 (PubMed PMID: 25418346).CrossRefPubMed
45.
go back to reference Mangold A, Alias S, Scherz T, Hofbauer T, Jakowitsch J, Panzenbock A, et al. Coronary neutrophil extracellular trap burden and deoxyribonuclease activity in ST-elevation acute coronary syndrome are predictors of ST-segment resolution and infarct size. Circ Res. 2015;116(7):1182–92. doi:10.1161/CIRCRESAHA.116.304944 (PubMed PMID: 25547404).CrossRefPubMed Mangold A, Alias S, Scherz T, Hofbauer T, Jakowitsch J, Panzenbock A, et al. Coronary neutrophil extracellular trap burden and deoxyribonuclease activity in ST-elevation acute coronary syndrome are predictors of ST-segment resolution and infarct size. Circ Res. 2015;116(7):1182–92. doi:10.​1161/​CIRCRESAHA.​116.​304944 (PubMed PMID: 25547404).CrossRefPubMed
47.
go back to reference Opatrna S, Wirth J, Korabecna M, Sefrna F. Cell-free plasma DNA during Hemodialysis. Ren Fail. 2009;31(6):475–80 (PubMed PMID: 19839825).CrossRefPubMed Opatrna S, Wirth J, Korabecna M, Sefrna F. Cell-free plasma DNA during Hemodialysis. Ren Fail. 2009;31(6):475–80 (PubMed PMID: 19839825).CrossRefPubMed
48.
go back to reference Daniel L, Fakhouri F, Joly D, Mouthon L, Nusbaum P, Grunfeld JP, et al. Increase of circulating neutrophil and platelet microparticles during acute vasculitis and hemodialysis. Kidney Int. 2006;69(8):1416–23. doi:10.1038/sj.ki.5000306 (PubMed PMID: 16531979).CrossRefPubMed Daniel L, Fakhouri F, Joly D, Mouthon L, Nusbaum P, Grunfeld JP, et al. Increase of circulating neutrophil and platelet microparticles during acute vasculitis and hemodialysis. Kidney Int. 2006;69(8):1416–23. doi:10.​1038/​sj.​ki.​5000306 (PubMed PMID: 16531979).CrossRefPubMed
49.
go back to reference Tovbin D, Novack V, Wiessman MP, Abd Elkadir A, Zlotnik M, Douvdevani A. Circulating cell-free DNA in hemodialysis patients predicts mortality. Nephrol Dial Transplant. 2012;27(10):3929–35. doi:10.1093/ndt/gfs255 (PubMed PMID: 22833622).CrossRefPubMed Tovbin D, Novack V, Wiessman MP, Abd Elkadir A, Zlotnik M, Douvdevani A. Circulating cell-free DNA in hemodialysis patients predicts mortality. Nephrol Dial Transplant. 2012;27(10):3929–35. doi:10.​1093/​ndt/​gfs255 (PubMed PMID: 22833622).CrossRefPubMed
50.
go back to reference McGuire AL, Urosevic N, Chan DT, Dogra G, Inglis TJ, Chakera A. The impact of chronic kidney disease and short-term treatment with rosiglitazone on plasma cell-free DNA levels. PPAR Res. 2014;2014:643189. doi:10.1155/2014/643189 (PubMed PMID: 25371664; PubMed Central PMCID: PMC4211161).CrossRefPubMedPubMedCentral McGuire AL, Urosevic N, Chan DT, Dogra G, Inglis TJ, Chakera A. The impact of chronic kidney disease and short-term treatment with rosiglitazone on plasma cell-free DNA levels. PPAR Res. 2014;2014:643189. doi:10.​1155/​2014/​643189 (PubMed PMID: 25371664; PubMed Central PMCID: PMC4211161).CrossRefPubMedPubMedCentral
51.
go back to reference Atamaniuk J, Kopecky C, Skoupy S, Saemann MD, Weichhart T. Apoptotic cell-free DNA promotes inflammation in haemodialysis patients. Nephrol Dial Transplant. 2012;27(3):902–5. doi:10.1093/ndt/gfr695 (PubMed PMID: 22167588).CrossRefPubMed Atamaniuk J, Kopecky C, Skoupy S, Saemann MD, Weichhart T. Apoptotic cell-free DNA promotes inflammation in haemodialysis patients. Nephrol Dial Transplant. 2012;27(3):902–5. doi:10.​1093/​ndt/​gfr695 (PubMed PMID: 22167588).CrossRefPubMed
52.
go back to reference Troidle L, Hansson J, Juergensen P, Finkelstein FO. We use bioincompatible peritoneal dialysis solutions. Semin Dial. 2016;. doi:10.1111/sdi.12490 (PubMed PMID: 27061506).PubMed Troidle L, Hansson J, Juergensen P, Finkelstein FO. We use bioincompatible peritoneal dialysis solutions. Semin Dial. 2016;. doi:10.​1111/​sdi.​12490 (PubMed PMID: 27061506).PubMed
53.
go back to reference Avogaro A, Pagnin E, Calo L. Monocyte NADPH oxidase subunit p22(phox) and inducible hemeoxygenase-1 gene expressions are increased in type II diabetic patients: relationship with oxidative stress. J Clin Endocrinol Metab. 2003;88(4):1753–9. doi:10.1210/jc.2002-021025 (PubMed PMID: 12679469).CrossRefPubMed Avogaro A, Pagnin E, Calo L. Monocyte NADPH oxidase subunit p22(phox) and inducible hemeoxygenase-1 gene expressions are increased in type II diabetic patients: relationship with oxidative stress. J Clin Endocrinol Metab. 2003;88(4):1753–9. doi:10.​1210/​jc.​2002-021025 (PubMed PMID: 12679469).CrossRefPubMed
54.
go back to reference Bansal S, Siddarth M, Chawla D, Banerjee BD, Madhu SV, Tripathi AK. Advanced glycation end products enhance reactive oxygen and nitrogen species generation in neutrophils in vitro. Mol Cell Biochem. 2012;361(1–2):289–96. doi:10.1007/s11010-011-1114-9 (PubMed PMID: 22048812).CrossRefPubMed Bansal S, Siddarth M, Chawla D, Banerjee BD, Madhu SV, Tripathi AK. Advanced glycation end products enhance reactive oxygen and nitrogen species generation in neutrophils in vitro. Mol Cell Biochem. 2012;361(1–2):289–96. doi:10.​1007/​s11010-011-1114-9 (PubMed PMID: 22048812).CrossRefPubMed
55.
go back to reference Tibrewal S, Ivanir Y, Sarkar J, Nayeb-Hashemi N, Bouchard CS, Kim E, et al. Hyperosmolar stress induces neutrophil extracellular trap formation: implications for dry eye disease. Invest Ophthalmol Vis Sci. 2014;55(12):7961–9. doi:10.1167/iovs.14-15332 (PubMed PMID: 25406284; PubMed Central PMCID: PMC4263134).CrossRefPubMedPubMedCentral Tibrewal S, Ivanir Y, Sarkar J, Nayeb-Hashemi N, Bouchard CS, Kim E, et al. Hyperosmolar stress induces neutrophil extracellular trap formation: implications for dry eye disease. Invest Ophthalmol Vis Sci. 2014;55(12):7961–9. doi:10.​1167/​iovs.​14-15332 (PubMed PMID: 25406284; PubMed Central PMCID: PMC4263134).CrossRefPubMedPubMedCentral
56.
go back to reference Vanholder R, Massy Z, Argiles A, Spasovski G, Verbeke F, Lameire N, et al. Chronic kidney disease as cause of cardiovascular morbidity and mortality. Nephrol Dial Transplant. 2005;20(6):1048–56. doi:10.1093/ndt/gfh813 (PubMed PMID: 15814534).CrossRefPubMed Vanholder R, Massy Z, Argiles A, Spasovski G, Verbeke F, Lameire N, et al. Chronic kidney disease as cause of cardiovascular morbidity and mortality. Nephrol Dial Transplant. 2005;20(6):1048–56. doi:10.​1093/​ndt/​gfh813 (PubMed PMID: 15814534).CrossRefPubMed
60.
61.
go back to reference Kumar SV, Kulkarni OP, Mulay SR, Darisipudi MN, Romoli S, Thomasova D, et al. Neutrophil extracellular trap-related extracellular histones cause vascular necrosis in severe GN. J Am Soc Nephrol. 2015;26(10):2399–413. doi:10.1681/ASN.2014070673 (PubMed PMID: 25644111; PubMed Central PMCID: PMC4587690).CrossRefPubMedPubMedCentral Kumar SV, Kulkarni OP, Mulay SR, Darisipudi MN, Romoli S, Thomasova D, et al. Neutrophil extracellular trap-related extracellular histones cause vascular necrosis in severe GN. J Am Soc Nephrol. 2015;26(10):2399–413. doi:10.​1681/​ASN.​2014070673 (PubMed PMID: 25644111; PubMed Central PMCID: PMC4587690).CrossRefPubMedPubMedCentral
62.
go back to reference Wang Y, Xiao Y, Zhong L, Ye D, Zhang J, Tu Y, et al. Increased neutrophil elastase and proteinase 3 and augmented NETosis are closely associated with beta-cell autoimmunity in patients with type 1 diabetes. Diabetes. 2014;63(12):4239–48. doi:10.2337/db14-0480 (PubMed PMID: 25092677).CrossRefPubMed Wang Y, Xiao Y, Zhong L, Ye D, Zhang J, Tu Y, et al. Increased neutrophil elastase and proteinase 3 and augmented NETosis are closely associated with beta-cell autoimmunity in patients with type 1 diabetes. Diabetes. 2014;63(12):4239–48. doi:10.​2337/​db14-0480 (PubMed PMID: 25092677).CrossRefPubMed
63.
go back to reference Villanueva E, Yalavarthi S, Berthier CC, Hodgin JB, Khandpur R, Lin AM, et al. Netting neutrophils induce endothelial damage, infiltrate tissues, and expose immunostimulatory molecules in systemic lupus erythematosus. J Immunol. 2011;187(1):538–52. doi:10.4049/jimmunol.1100450 (PubMed PMID: 21613614; PubMed Central PMCID: PMC3119769).CrossRefPubMedPubMedCentral Villanueva E, Yalavarthi S, Berthier CC, Hodgin JB, Khandpur R, Lin AM, et al. Netting neutrophils induce endothelial damage, infiltrate tissues, and expose immunostimulatory molecules in systemic lupus erythematosus. J Immunol. 2011;187(1):538–52. doi:10.​4049/​jimmunol.​1100450 (PubMed PMID: 21613614; PubMed Central PMCID: PMC3119769).CrossRefPubMedPubMedCentral
64.
65.
go back to reference Sangaletti S, Tripodo C, Chiodoni C, Guarnotta C, Cappetti B, Casalini P, et al. Neutrophil extracellular traps mediate transfer of cytoplasmic neutrophil antigens to myeloid dendritic cells toward ANCA induction and associated autoimmunity. Blood. 2012;120(15):3007–18. doi:10.1182/blood-2012-03-416156 (PubMed PMID: 22932797).CrossRefPubMed Sangaletti S, Tripodo C, Chiodoni C, Guarnotta C, Cappetti B, Casalini P, et al. Neutrophil extracellular traps mediate transfer of cytoplasmic neutrophil antigens to myeloid dendritic cells toward ANCA induction and associated autoimmunity. Blood. 2012;120(15):3007–18. doi:10.​1182/​blood-2012-03-416156 (PubMed PMID: 22932797).CrossRefPubMed
66.
go back to reference Cools-Lartigue J, Spicer J, McDonald B, Gowing S, Chow S, Giannias B, et al. Neutrophil extracellular traps sequester circulating tumor cells and promote metastasis. J Clin Invest. 2013;. doi:10.1172/JCI67484 (PubMed PMID: 23863628; PubMed Central PMCID: PMC3726160).PubMedPubMedCentral Cools-Lartigue J, Spicer J, McDonald B, Gowing S, Chow S, Giannias B, et al. Neutrophil extracellular traps sequester circulating tumor cells and promote metastasis. J Clin Invest. 2013;. doi:10.​1172/​JCI67484 (PubMed PMID: 23863628; PubMed Central PMCID: PMC3726160).PubMedPubMedCentral
69.
go back to reference Demers M, Krause DS, Schatzberg D, Martinod K, Voorhees JR, Fuchs TA, et al. Cancers predispose neutrophils to release extracellular DNA traps that contribute to cancer-associated thrombosis. Proc Natl Acad Sci U S A. 2012;109(32):13076–81. doi:10.1073/pnas.1200419109 (PubMed PMID: 22826226; PubMed Central PMCID: PMC3420209).CrossRefPubMedPubMedCentral Demers M, Krause DS, Schatzberg D, Martinod K, Voorhees JR, Fuchs TA, et al. Cancers predispose neutrophils to release extracellular DNA traps that contribute to cancer-associated thrombosis. Proc Natl Acad Sci U S A. 2012;109(32):13076–81. doi:10.​1073/​pnas.​1200419109 (PubMed PMID: 22826226; PubMed Central PMCID: PMC3420209).CrossRefPubMedPubMedCentral
70.
71.
go back to reference Grosse-Steffen T, Giese T, Giese N, Longerich T, Schirmacher P, Hansch GM, et al. 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. doi:10.1155/2012/720768 (PubMed PMID: 23227088; PubMed Central PMCID: PMC3514849).CrossRefPubMedPubMedCentral Grosse-Steffen T, Giese T, Giese N, Longerich T, Schirmacher P, Hansch GM, et al. 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. doi:10.​1155/​2012/​720768 (PubMed PMID: 23227088; PubMed Central PMCID: PMC3514849).CrossRefPubMedPubMedCentral
72.
go back to reference Vidal E, Tortosa R, Marco P, Fondevila D, Rabanal RM, Torres JM, et al. Late stage cathepsin C, CXCL13 and Ki-67 overexpression correlate with regional neuropathology in a BSE transgenic murine model. J Comp Pathol. 2013;148(1):22–32. doi:10.1016/j.jcpa.2012.05.004 (PubMed PMID: 22789860).CrossRefPubMed Vidal E, Tortosa R, Marco P, Fondevila D, Rabanal RM, Torres JM, et al. Late stage cathepsin C, CXCL13 and Ki-67 overexpression correlate with regional neuropathology in a BSE transgenic murine model. J Comp Pathol. 2013;148(1):22–32. doi:10.​1016/​j.​jcpa.​2012.​05.​004 (PubMed PMID: 22789860).CrossRefPubMed
73.
go back to reference Davis JC Jr, Manzi S, Yarboro C, Rairie J, McInnes I, Averthelyi D, et al. Recombinant human Dnase I (rhDNase) in patients with lupus nephritis. Lupus. 1999;8(1):68–76 (PubMed PMID: 10025601).CrossRefPubMed Davis JC Jr, Manzi S, Yarboro C, Rairie J, McInnes I, Averthelyi D, et al. Recombinant human Dnase I (rhDNase) in patients with lupus nephritis. Lupus. 1999;8(1):68–76 (PubMed PMID: 10025601).CrossRefPubMed
74.
Metadata
Title
NETosis provides the link between activation of neutrophils on hemodialysis membrane and comorbidities in dialyzed patients
Authors
Marie Korabecna
Vladimir Tesar
Publication date
01-05-2017
Publisher
Springer International Publishing
Published in
Inflammation Research / Issue 5/2017
Print ISSN: 1023-3830
Electronic ISSN: 1420-908X
DOI
https://doi.org/10.1007/s00011-016-1010-6

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