Characterization of rapid neutrophil extracellular trap formation and its cooperation with phagocytosis in human neutrophils
DISCOVERIES (ISSN 2359-7232),2014, April-June
Saffarzadeh M, Cabrera-Fuentes HA, Veit F, Jiang D, Scharffetter-Kochanek K, Gille C, Rooijakkers SHM, Hartl D, Preissner KT. Characterization of rapid neutrophil extracellular trap formation and its cooperation with phagocytosis in human neutrophils. Discoveries 2014, Apr-Jun; 2(2): e19. DOI: 10.15190/d.2014.11
Submitted: June 10, 2014; Revised: June 29, 2014; Accepted: June 30, 2014; Published: June 30, 2014;
GO BACK to 2014, April-June issue
GO BACK to DISCOVERIES
Characterization of rapid neutrophil extracellular trap formation and its cooperation with phagocytosis in human neutrophils
Mona Saffarzadeh (1,2,*), Hector A. Cabrera-Fuentes (1) Florian Veit (3), Dongsheng Jiang (4), Karin Scharffetter-Kochanek (4), Christian Gille (5),
Suzan H. M. Rooijakkers (6), Dominik Hartl (7,#), Klaus T. Preissner (1,#),
(1) Department of Biochemistry, School of Medicine, Justus-Liebig-University, Giessen, Germany
(2) Center for Thrombosis and Hemostasis (CTH), University Medical Center Mainz, Mainz, Germany
(3)Excellence Cluster Cardio-Pulmonary System (ECCPS), German Lung Center (DZL), Justus-Liebig-University Giessen, Giessen, Germany
(4) Department of Dermatology and Allergic Diseases, University of Ulm, Ulm, Germany
(5) Department of Pediatrics IV/Neonatology, Eberhard Karls University, Tuebingen, Germany
(6) Medical Microbiology, University Medical Center Utrecht, Utrecht, The Netherlands
(7) Department of Pediatrics I, Eberhard Karls University, Tuebingen, Germany
#These authors contributed equally to this work;
*Correspondence to: Mona Saffarzadeh, Ph.D, Department of Biochemistry, School of Medicine Justus-Liebig-University, Friedrichstrasse 24 D-35392 Giessen, Germany; Phone: +49-641-994-7485; Fax: +49-641-994-7509; E-mail: Mona.Saffarzadeh@biochemie.med.uni-giessen.de;
Abstract
Neutrophils, as the first cellular line of innate host defense, employ phagocytosis and formation of neutrophil extracellular traps (NETs) to combat infections. Classical NET formation induced by phorbol myristate acetate requires several hours to complete. However, recent studies demonstrated rapid NET formation in neutrophils upon stimulation by platelets, Staphylococcus aureus or fungal products. Here we describe that antibody- or complement-induced phagocytosis triggers rapid NET formation. In contrast to classical NETosis, chemical inhibition of NADPH oxidase as well as using NADPH oxidase-deficient patient neutrophils did not affect rapid NET formation. Although phagocytosis and rapid NET formation may not be the prerequisite of each other, cooperation of phagocytosis and rapid NET formation may be essential to improve the efficiency of defense mechanisms in combating disseminating bacteria. Dissecting the differential mechanisms of NET formation is crucial to develop novel therapeutic strategies for infectious and auto-immune diseases where NETs play an essential role.
Access full text of the manuscript here: See full text (pdf) Suppl. Information (pdf)
References
1. Borregaard N, Cowland JB. Granules of the human neutrophilic polymorphonuclear leukocyte. Blood 1997; 89: 3503-3521.
2. Nathan C (2006) Neutrophils and immunity: challenges and opportunities. Nat Rev Immunol 6: 173-182.
3. Soehnlein O. Direct and alternative antimicrobial mechanisms of neutrophil-derived granule proteins. J Mol Med (Berl) 2009; 87: 1157-1164.
4. Hampton MB, Kettle AJ, Winterbourn CC. Inside the neutrophil phagosome: oxidants, myeloperoxidase, and bacterial killing. Blood 1998; 92: 3007-3017.
5. Chapman AL, Hampton MB, Senthilmohan R, Winterbourn CC, Kettle AJ. Chlorination of bacterial and neutrophil proteins during phagocytosis and killing of Staphylococcus aureus. J Biol Chem 2002; 277: 9757-9762.
6. Lee WL, Harrison RE, Grinstein S. Phagocytosis by neutrophils. Microbes Infect 2003; 5: 1299-1306.
7. Mayer-Scholl A, Averhoff P, Zychlinsky A. How do neutrophils and pathogens interact? Curr Opin Microbiol 2004; 7: 62-66.
8. Hickey MJ, Kubes P. Intravascular immunity: the host-pathogen encounter in blood vessels. Nat Rev Immunol 2009; 9: 364-375.
9. Greenberg S, Grinstein S. Phagocytosis and innate immunity. Curr Opin Immunol 2002; 14: 136-145.
10. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, et al. Neutrophil extracellular traps kill bacteria. Science 2004; 303: 1532-1535.
11. Urban CF, Ermert D, Schmid M, Abu-Abed U, Goosmann C, et al. Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathog 2009; 5: e1000639.
12. Saffarzadeh M, Juenemann C, Queisser MA, Lochnit G, Barreto G, et al. Neutrophil extracellular traps directly induce epithelial and endothelial cell death: a predominant role of histones. PLoS One 2012; 7: e32366.
13. Saffarzadeh M, Preissner KT. Fighting against the dark side of neutrophil extracellular traps in disease: manoeuvres for host protection. Curr Opin Hematol 2013; 20: 3-9.
14. Brinkmann V, Zychlinsky A. Beneficial suicide: why neutrophils die to make NETs. Nat Rev Microbiol 2007; 5: 577-582.
15. Clark SR, Ma AC, Tavener SA, McDonald B, Goodarzi Z, et al. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat Med 2007; 13: 463-469.
16. Fuchs TA, Abed U, Goosmann C, Hurwitz R, Schulze I, et al. Novel cell death program leads to neutrophil extracellular traps. J Cell Biol 2007; 176: 231-241.
17. Bruns S, Kniemeyer O, Hasenberg M, Aimanianda V, Nietzsche S, et al. Production of extracellular traps against Aspergillus fumigatus in vitro and in infected lung tissue is dependent on invading neutrophils and influenced by hydrophobin RodA. PLoS Pathog 2010; 6: e1000873.
18. Massberg S, Grahl L, von Bruehl ML, Manukyan D, Pfeiler S, et al. Reciprocal coupling of coagulation and innate immunity via neutrophil serine proteases. Nat Med 2010; 16: 887-896.
19. Byrd AS, O'Brien XM, Johnson CM, Lavigne LM, Reichner JS. An extracellular matrix-based mechanism of rapid neutrophil extracellular trap formation in response to Candida albicans. J Immunol 2013; 190: 4136-4148.
20. Pilsczek FH, Salina D, Poon KK, Fahey C, Yipp BG, et al. A novel mechanism of rapid nuclear neutrophil extracellular trap formation in response to Staphylococcus aureus. J Immunol 2010; 185: 7413-7425.
21. Yipp BG, Petri B, Salina D, Jenne CN, Scott BN, et al. Infection-induced NETosis is a dynamic process involving neutrophil multitasking in vivo. Nat Med 2012; 18: 1386-1393.
22. Costa D, Marques AP, Reis RL, Lima JL, Fernandes E. Inhibition of human neutrophil oxidative burst by pyrazolone derivatives. Free Radic Biol Med 2006; 40: 632-640.
23. Van de Weert-van Leeuwen PB, Van Meegen MA, Speirs JJ, Pals DJ, Rooijakkers SH, et al. Optimal complement-mediated phagocytosis of Pseudomonas aeruginosa by monocytes is cystic fibrosis transmembrane conductance regulator-dependent. Am J Respir Cell Mol Biol 2013; 49: 463-470.
24. Veit F, Pak O, Egemnazarov B, Roth M, Kosanovic D, et al. Function of NADPH Oxidase 1 in Pulmonary Arterial Smooth Muscle Cells After Monocrotaline-Induced Pulmonary Vascular Remodeling. Antioxidants & Redox Signaling 2013; 19: 2213-2231.
25. Brinkmann V, Goosmann C, Kuhn LI, Zychlinsky A. Automatic quantification of in vitro NET formation. Front Immunol 2012; 3: 413.
26. Castellano F, Montcourrier P, Chavrier P. Membrane recruitment of Rac1 triggers phagocytosis. J Cell Sci 2000; 113 ( Pt 17): 2955-2961.
27. McCormick A, Heesemann L, Wagener J, Marcos V, Hartl D, et al. NETs formed by human neutrophils inhibit growth of the pathogenic mold Aspergillus fumigatus. Microbes Infect 2010; 12: 928-936.
28. Neeli I, Dwivedi N, Khan S, Radic M. Regulation of extracellular chromatin release from neutrophils. J Innate Immun 2009; 1: 194-201.
29. Jerjomiceva N, Seri H, Vollger L, Wang Y, Zeitouni N, et al. Enrofloxacin Enhances the Formation of Neutrophil Extracellular Traps in Bovine Granulocytes. J Innate Immun 2014 Mar 14. [Epub ahead of print]
30. Stemerding AM, Kohl J, Pandey MK, Kuipers A, Leusen JH, et al. Staphylococcus aureus formyl peptide receptor-like 1 inhibitor (FLIPr) and its homologue FLIPr-like are potent FcgammaR antagonists that inhibit IgG-mediated effector functions. J Immunol 2013; 191: 353-362.
31. Nishinaka Y, Arai T, Adachi S, Takaori-Kondo A, Yamashita K. Singlet oxygen is essential for neutrophil extracellular trap formation. Biochem Biophys Res Commun 2011; 413: 75-79.
32. Chen K, Nishi H, Travers R, Tsuboi N, Martinod K, et al. Endocytosis of soluble immune complexes leads to their clearance by FcgammaRIIIB but induces neutrophil extracellular traps via FcgammaRIIA in vivo. Blood 2012; 120: 4421-4431.
33. Parker H, Dragunow M, Hampton MB, Kettle AJ, Winterbourn CC. Requirements for NADPH oxidase and myeloperoxidase in neutrophil extracellular trap formation differ depending on the stimulus. J Leukoc Biol 2012; 92: 841-849.
34. Parker H, Winterbourn CC. Reactive oxidants and myeloperoxidase and their involvement in neutrophil extracellular traps. Front Immunol 2012; 3: 424.
35. Pijanowski L, Golbach L, Kolaczkowska E, Scheer M, Verburg-van Kemenade BM, et al. Carp neutrophilic granulocytes form extracellular traps via ROS-dependent and independent pathways. Fish Shellfish Immunol 2013; 34: 1244-1252.
GO BACK to the 2014, April-June issue
GO BACK to DISCOVERIES
MEET OUR EDITORIAL BOARD
SUBMIT A MANUSCRIPT
Email us at info@discoveriesjournals.org if you have any questions.
News & Events Latest news from Discoveries
- 2022, April| AWARDS!
2022 Discoveries Award winning articles!
- Kinal Bhatt et al. 2021 (Larking Health System, FL, USA); Bhatt K, Agolli A, Patel MH, et al. High mortality co-infections of COVID-19 patients: mucormycosis and other fungal infections. Discoveries. 2021;9(1):e126.
27 citations in the past 1 year - $1000 prize- Hasnain Jan et al. 2020 (Quaid-i-Azam University, Pakistan); Jan H, Faisal S, Khan A, et al. COVID-19: Review of Epidemiology and Potential Treatments Against 2019 Novel Coronavirus. Discoveries. 2020;8(2):e108.
23 citations in the past 2 years - $400 prizeCongratulations! Prizes will be received by the awardees in July 2022!
- 2021, July| 2021, Jul-September
Due to the high volume of the submitted articles, both Discoveries and Discoveries Reports are experiencing processing and publication delays during the months of July-September 2021. We will get back to the normal processing and publication times starting in October 2021. Note that our editorial and administrativ work is fully funded by our publishing house at this time and we are striving to KEEP THE NO FEE/NO CHARGE strategy in place as long as possible.
- 2021, January| AWARDS!
2022 DISCOVERIES AWARDS! Discoveries will offer $1000 and $400 awards in early 2022, for the most cited (2021 ISI Citations) and visible articles published in 2018-2021.
- 2020, November| Follow us on Twitter!
You can now follow the latest Discoveries news and updates on Twitter! (@DiscoveriesNews)
- 2020, August| For Authors!
Due to a high volume of article submissions, our peer-review process takes more than usual. The pre-screening decision is released in 1-2 days, while the peer-review process lasts between 10 and 20 days.
- 2020, April | For Authors!
WE DO NOT TOLERATE ANY MISCONDUCT! Please be aware that we are testing all received articles with specialized software for PLAGIARISM and WE WILL TAKE MEASURES if your article is already published or in consideration for publication by other journals! This may result in serious professional consequences for the authors. The latest striking case is the following article which is already published and was re-submitted here.
- 2020, April | For Authors!
We are happy to let you know that all articles published in Discoveries are now included in PubMedCentral (PMC). New accepted articles will be included in PMC and PubMed within 1-2 weeks after their publication.
- 2020, January | For Authors!
Starting in January 2020, Discoveries will also consider articles submitted by Discoveries' Editorial Board members. However, only a small number of such articles (maximum 4 articles/year) will be considered for publication after the peer-review process, and the authors who are also our editors will be clearly disclosed on our website.
- 2019, September | Indexed by PMC
Discoveries is now indexed by PubMedCentral and Pubmed. The agreement with US National Library of Medicine was signed on September 10, 2019. Our next step is ISI Web of Science indexing. NOTE: previously published articles will be included on PubMed in early 2020.
- 2019, September | PubMed inclusion!
We are happy to let you know that Discoveries successfuly passed the last step (Technical Review) required for PubMedCentral and PubMed inclusion!
- 2019, July | PubMed inclusion News!
We are happy to receive positive comments from PMC/NLM-NIH regarding Discoveries' last step (Technical Review) required for PubMedCentral and PubMed inclusion. We will let you know once whole indexing process is completed.
- 2019| Sharing and Distribution!
All articles published in Discoveries are Open Access articles distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited and it is not used for commercial purposes.
- 2018-2019 | For Authors!
From now on and for at least 1 year, we will only accept articles from authors that are NOT members of Discoveries' Editorial Board. All articles submitted by our editors will be immediately rejected until further notice (one accepted article was already rejected).
- 2018 | PubMed inclusion News!
Discoveries successfully passed the Scientific Quality Review by NLM-NIH for PubMedCentral and PubMed indexing. This is the first and the most important step towards PubMedCentral and PubMed indexing! The second (last) step is the Technical Review.
- 2016, April | Faster Peer-Review
Starting on April 13th 2016, all articles selected for a peer-review will receive the post peer-review decision within ~10 days. The initial pre-screening time will remain the same (48h from the submission of the manuscript). This decision will significantly accelerate the publication, with no effect on the quality of the peer-review process.
- 2016, February | Manuscript submission
Discoveries is commited to excellence, quality and high editorial standards. We are receiving an increasing number of manuscripts for which the identity of the authors/corresponding author can't be verified. Please NOTE that ALL these articles were and will be immediately REJECTED. Indicating an institutional email address is the easiest way to overcome this problem! Moreover, we do not accept any pressure on our editorial board to accept a manuscript. This results in a prompt rejection of the article.
Editorial Policies - 2016, January | Main Objective
After reaching all proposed milestones until now (including being indexed by Google Scholar in 2014), Discoveries' next Aim is PubMed indexing of all its articles (already published and upcoming). There will be no charge for the submission or publication of articles before Discoveries is indexed.
- 2015, August | Discoveries - on PubMed
We are happy to announce that our first Discoveries articles were included in PMC and PubMed. More articles (submitted by NIH funded authors) are now processed for being included.
Discoveries articles now on PubMed - 2015, April | Special Issue
DISCOVERIES published the SPECIAL ISSUE entitled "INFLAMMATION BETWEEN DEFENSE AND DISEASE: Impact on Tissue Repair and Chronic Sickness".
Special Issue on "Inflammation" - 2015 | Ischemia Collection
DISCOVERIES launched a call for papers for a Collection of Articles with focus on "ISCHEMIA". If you are interested to submit a manuscript, please contact us at info@discoveriesjournals.org
- 2014, September | Special Issue
DISCOVERIES just publish the SPECIAL ISSUE entitled "CELL SECRETION & MEMBRANE FUSION" in September 2014. Initially scheduled for publication between October 2014-March 2015, this issue was successfully published earlier than scheduled.
Special Issue - 2014, April | Indexed by Google Scholar
All our published articles are now indexed by Google Scholar! First citations to Discoveries articles are included! Search for the article's title (recommended) or the authors:
Google Scholar Search - 2014 | DISCOVERIES
DOIs (Digital Object Identifiers) are now assigned to all our published manuscripts in Discoveries. DOI uniquely identifies an article and is provided by CrossRef.
CrossRef - 2013, July | Manuscript Submission
Submit your manuscript FREE, FAST and EASY ! (in less than 1 minute)! There are NO fees for the manuscript submission or publishing of the accepted manuscripts.
read more - 2013, July | DISCOVERIES
We are now ACCEPTING MANUSCRIPTS for publishing in DISCOVERIES. We aim publishing a small number of high impact experimental articles & reviews (around 40/year) to maintain a high impact factor. Domains of interest: all areas related to Medicine, Biology and Chemistry ...
read more