Neutrophils release extracellular DNA traps in response to exercise

Journal of Applied Physiology

Volumn 117, Issue 3, 2014, Pages 325-333

  Beiter, Thomas ^a   Fragasso, Annunziata ^a   Hudemann, Jens ^a   Schild, Marius ^b   Steinacker, Jürgen ^c   Mooren, Frank C ^b   Niess, Andreas M ^a  

^a UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

^c UNIVERSITY HOSPITAL ULM   (Germany)

Author keywords

Cell free DNA; DNase; Neutrophil extracellular traps

Indexed keywords

DEOXYRIBONUCLEASE; DNA; PEROXIDASE;

ADULT; BLOOD; EXERCISE; EXERCISE TEST; EXTRACELLULAR TRAP; HUMAN; MALE; METABOLISM; NEUTROPHIL; PHYSIOLOGY; PROCEDURES; YOUNG ADULT;

ADULT; DEOXYRIBONUCLEASES; DNA; EXERCISE; EXERCISE TEST; EXTRACELLULAR TRAPS; HUMANS; MALE; NEUTROPHILS; PEROXIDASE; YOUNG ADULT;

EID: 84905493111     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00173.2014     Document Type: Article

References (59)

1. Ammollo CT, Semeraro F, Xu J, Esmon NL, Esmon CT. Extracellular histones increase plasma thrombin generation by impairing thrombomodulindependent protein C activation. J Thromb Haemost 9:1795-1803, 2011.
2. Atamaniuk J, Vidotto C, Tschan H, Bachl N, Stuhlmeier KM, Muller MM. Increased concentrations of cell-free plasma DNA after exhaustive exercise. Clin Chem 50:1668-1670, 2004.
3. Baker VS, Imade GE, Molta NB, Tawde P, Pam SD, Obadofin MO, Sagay SA, Egah DZ, Iya D, Afolabi BB, Baker M, Ford K, Ford R, Roux KH, Keller TC III. Cytokine-Associated neutrophil extracellular traps and antinuclear antibodies in Plasmodium falciparum infected children under six years of age. Malar J 7:41, 2008.
4. Bastien M, Poirier P, Lemieux I, Despres JP. Overview of epidemiology and contribution of obesity to cardiovascular disease. Prog Cardiovasc Dis 56:369-381, 2014.
5. Beiter T, Fragasso A, Hudemann J, Niess AM, Simon P. Short-term treadmill running as a model for studying cell-free DNA kinetics in vivo. Clin Chem 57:633-636, 2011.
6. Borissoff JI, Joosen IA, Versteylen MO, Brill A, Fuchs TA, Savchenko AS, Gallant M, Martinod K, Ten CH, Hofstra L, Crijns HJ, Wagner DD, Kietselaer BL. Elevated levels of circulating DNA and chromatin are independently associated with severe coronary atherosclerosis and a prothrombotic state. Arterioscler Thromb Vasc Biol 33:2032-2040, 2013.
7. Brill A, Fuchs TA, Savchenko AS, Thomas GM, Martinod K, De Meyer SF, Bhandari AA, Wagner DD. Neutrophil extracellular traps promote deep vein thrombosis in mice. J Thromb Haemost 10:136-144, 2012.
8. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, Weinrauch Y, Zychlinsky A. Neutrophil extracellular traps kill bacteria. Science 303:1532-1535, 2004.
9. Brinkmann V, Zychlinsky A. Neutrophil extracellular traps: is immunity the second function of chromatin? J Cell Biol 198:773-783, 2012.
10. Caudrillier A, Kessenbrock K, Gilliss BM, Nguyen JX, Marques MB, Monestier M, Toy P, Werb Z, Looney MR. Platelets induce neutrophil extracellular traps in transfusion-related acute lung injury. J Clin Invest 122:2661-2671, 2012.
11. Chiu RW, Chan LY, Lam NY, Tsui NB, Ng EK, Rainer TH, Lo YM. Quantitative analysis of circulating mitochondrial DNA in plasma. Clin Chem 49:719-726, 2003.
12. Clark SR, Ma AC, Tavener SA, McDonald B, Goodarzi Z, Kelly MM, Patel KD, Chakrabarti S, McAvoy E, Sinclair GD, Keys EM, Len-Vercoe E, Devinney R, Doig CJ, Green FH, Kubes P. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat Med 13:463-469, 2007.
13. 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 Invest 123:3446-3458, 2013.
14. Demers M, Krause DS, Schatzberg D, Martinod K, Voorhees JR, Fuchs TA, Scadden DT, Wagner DD. Cancers predispose neutrophils to release extracellular DNA traps that contribute to cancer-Associated thrombosis. Proc Natl Acad Sci USA 109:13076-13081, 2012.
15. Demers M, Wagner DD. Neutrophil extracellular traps: a new link to cancer-Associated thrombosis and potential implications for tumor progression. Oncoimmunology 2:e22946, 2013.
16. Diana J, Simoni Y, Furio L, Beaudoin L, Agerberth B, Barrat F, Lehuen A. Crosstalk between neutrophils, B-1a cells and plasmacytoid dendritic cells initiates autoimmune diabetes. Nat Med 19:65-73, 2013.
17. Diaz JA, Fuchs TA, Jackson TO, Hovinga JA, Lammle B, Henke PK, Myers DD Jr, Wagner DD, Wakefield TW. Plasma DNA is elevated in patients with deep vein thrombosis. J Vasc Surg Venous Lymphat Disord 1:2013.
18. Doring Y, Drechsler M, Wantha S, Kemmerich K, Lievens D, Vijayan S, Gallo RL, Weber C, Soehnlein O. Lack of neutrophil-derived CRAMP reduces atherosclerosis in mice. Circ Res 110:1052-1056, 2012.
19. Doring Y, Manthey HD, Drechsler M, Lievens D, Megens RT, Soehnlein O, Busch M, Manca M, Koenen RR, Pelisek J, Daemen MJ, Lutgens E, Zenke M, Binder CJ, Weber C, Zernecke A. Auto-Antigenic protein-DNA complexes stimulate plasmacytoid dendritic cells to promote atherosclerosis. Circulation 125:1673-1683, 2012.
20. El-Sayed MS. Exercise and training effects on platelets in health and disease. Platelets 13:261-266, 2002.
21. Engelmann B, Massberg S. Thrombosis as an intravascular effector of innate immunity. Nat Rev Immunol 13:34-45, 2013.
22. Fatouros IG, Destouni A, Margonis K, Jamurtas AZ, Vrettou C, Kouretas D, Mastorakos G, Mitrakou A, Taxildaris K, Kanavakis E, Papassotiriou I. Cell-free plasma DNA as a novel marker of aseptic inflammation severity related to exercise overtraining. Clin Chem 52:1820-1824, 2006.
23. Fatouros IG, Jamurtas AZ, Nikolaidis MG, Destouni A, Michailidis Y, Vrettou C, Douroudos II, Avloniti A, Chatzinikolaou A, Taxildaris K, Kanavakis E, Papassotiriou I, Kouretas D. Time of sampling is crucial for measurement of cell-free plasma DNA following acute aseptic inflammation induced by exercise. Clin Biochem 43:1368-1370, 2010.
24. Fuchs TA, Alvarez JJ, Martinod K, Bhandari AA, Kaufman RM, Wagner DD. Neutrophils release extracellular DNA traps during storage of red blood cell units. Transfusion 53:3210-3216, 2013.
25. Fuchs TA, Brill A, Duerschmied D, Schatzberg D, Monestier M, Myers DD Jr, Wrobleski SK, Wakefield TW, Hartwig JH, Wagner DD. Extracellular DNA traps promote thrombosis. Proc Natl Acad Sci USA 107:15880-15885, 2010.
26. Fuchs TA, Kremer Hovinga JA, Schatzberg D, Wagner DD, Lammle B. Circulating DNA and myeloperoxidase indicate disease activity in patients with thrombotic microangiopathies. Blood 120:1157-1164, 2012.
27. Garcia-Romo GS, Caielli S, Vega B, Connolly J, Allantaz F, Xu Z, Punaro M, Baisch J, Guiducci C, Coffman RL, Barrat FJ, Banchereau J, Pascual V. Netting neutrophils are major inducers of type I IFN production in pediatric systemic lupus erythematosus. Sci Transl Med 3:73ra20, 2011.
28. Gleeson M, Bishop NC, Stensel DJ, Lindley MR, Mastana SS, Nimmo MA. The anti-inflammatory effects of exercise: mechanisms and implications for the prevention and treatment of disease. Nat Rev Immunol 11:607-615, 2011.
29. Guiducci C, Tripodo C, Gong M, Sangaletti S, Colombo MP, Coffman RL, Barrat FJ. Autoimmune skin inflammation is dependent on plasmacytoid dendritic cell activation by nucleic acids via TLR7 and TLR9. J Exp Med 207:2931-2942, 2010.
30. Gunzer M. Traps and hyper inflammation-new ways that neutrophils promote or hinder survival. Br J Haematol 164:189-199, 2014.
31. Hakkim A, Furnrohr BG, Amann K, Laube B, Abed UA, Brinkmann V, Herrmann M, Voll RE, Zychlinsky A. Impairment of neutrophil extracellular trap degradation is associated with lupus nephritis. Proc Natl Acad Sci USA 107:9813-9818, 2010.
32. Holdenrieder S, Stieber P. Clinical use of circulating nucleosomes. Crit Rev Clin Lab Sci 46:1-24, 2009.
33. Kahlenberg JM, Kaplan MJ. Mechanisms of premature atherosclerosis in rheumatoid arthritis and lupus. Annu Rev Med 64:249-263, 2013.
34. Kessenbrock K, Krumbholz M, Schonermarck U, Back W, Gross WL, Werb Z, Grone HJ, Brinkmann V, Jenne DE. Netting neutrophils in autoimmune small-vessel vasculitis. Nat Med 15:623-625, 2009.
35. Kraemer RR, Brown BS. Alterations in plasma-volume-corrected blood components of marathon runners and concomitant relationship to performance. Eur J Appl Physiol Occup Physiol 55:579-584, 1986.
36. Lippi G, Maffulli N. Biological influence of physical exercise on hemostasis. Semin Thromb Hemost 35:269-276, 2009.
37. Lopez AD, Mathers CD, Ezzati M, Jamison DT, Murray CJ. Global and regional burden of disease and risk factors, 2001: systematic analysis of population health data. Lancet 367:1747-1757, 2006.
38. Malickova K, Duricova D, Bortlik M, Hruskova Z, Svobodova B, Machkova N, Komarek V, Fucikova T, Janatkova I, Zima T, Lukas M. Impaired deoxyribonuclease I activity in patients with inflammatory bowel diseases. Autoimmune Dis 2011:945861, 2011.
39. Massberg S, Grahl L, Von Bruehl ML, Manukyan D, Pfeiler S, Goosmann C, Brinkmann V, Lorenz M, Bidzhekov K, Khandagale AB, Konrad I, Kennerknecht E, Reges K, Holdenrieder S, Braun S, Reinhardt C, Spannagl M, Preissner KT, Engelmann B. Reciprocal coupling of coagulation and innate immunity via neutrophil serine proteases. Nat Med 16:887-896, 2010.
40. McDonald B, Urrutia R, Yipp BG, Jenne CN, Kubes P. Intravascular neutrophil extracellular traps capture bacteria from the bloodstream during sepsis. Cell Host Microbe 12:324-333, 2012.
41. Megens RT, Vijayan S, Lievens D, Doring Y, Van Zandvoort MA, Grommes J, Weber C, Soehnlein O. Presence of luminal neutrophil extracellular traps in atherosclerosis. Thromb Haemost 107:597-598, 2012.
42. Meng W, Paunel-Gorgulu A, Flohe S, Witte I, Schadel-Hopfner M, Windolf J, Logters TT. Deoxyribonuclease is a potential counter regulator of aberrant neutrophil extracellular traps formation after major trauma. Mediators Inflamm 2012:149560, 2012.
43. Nordenfelt P, Tapper H. Phagosome dynamics during phagocytosis by neutrophils. J Leukoc Biol 90:271-284, 2011.
44. Oehmcke S, Morgelin M, Herwald H. Activation of the human contact system on neutrophil extracellular traps. J Innate Immun 1:225-230, 2009.
45. Parker H, Winterbourn CC. Reactive oxidants and myeloperoxidase and their involvement in neutrophil extracellular traps. Front Immunol 3:424, 2012.
46. Peake J, Wilson G, Hordern M, Suzuki K, Yamaya K, Nosaka K, Mackinnon L, Coombes JS. Changes in neutrophil surface receptor expression, degranulation, and respiratory burst activity after moderateand high-intensity exercise. J Appl Physiol 97:612-618, 2004.
47. Peake JM, Suzuki K, Wilson G, Hordern M, Nosaka K, Mackinnon L, Coombes JS. Exercise-induced muscle damage, plasma cytokines, and markers of neutrophil activation. Med Sci Sports Exerc 37:737-745, 2005.
48. Phillipson M, Kubes P. The neutrophil in vascular inflammation. Nat Med 17:1381-1390, 2011.
49. Pilsczek FH, Salina D, Poon KK, Fahey C, Yipp BG, Sibley CD, Robbins SM, Green FH, Surette MG, Sugai M, Bowden MG, Hussain M, Zhang K, Kubes P. A novel mechanism of rapid nuclear neutrophil extracellular trap formation in response to Staphylococcus aureus. J Immunol 185:7413-7425, 2010.
50. Reid VL, Gleeson M, Williams N, Clancy RL. Clinical investigation of athletes with persistent fatigue and/or recurrent infections. Br J Sports Med 38:42-45, 2004.
51. Sangaletti S, Tripodo C, Chiodoni C, Guarnotta C, Cappetti B, Casalini P, Piconese S, Parenza M, Guiducci C, Vitali C, Colombo MP. Neutrophil extracellular traps mediate transfer of cytoplasmic neutrophil antigens to myeloid dendritic cells toward ANCA induction and associated autoimmunity. Blood 120:3007-3018, 2012.
52. Sengelov H, Kjeldsen L, Borregaard N. Control of exocytosis in early neutrophil activation. J Immunol 150:1535-1543, 1993.
53. Simon D, Simon HU, Yousefi S. Extracellular DNA traps in allergic, infectious, and autoimmune diseases. Allergy 68:409-416, 2013.
54. Swarup V, Rajeswari MR. Circulating (cell-free) nucleic acids-A promising, non-invasive tool for early detection of several human diseases. FEBS Lett 581:795-799, 2007.
55. Urban CF, Ermert D, Schmid M, Bu-Abed U, Goosmann C, Nacken W, Brinkmann V, Jungblut PR, Zychlinsky A. Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathog 5:e1000639, 2009.
56. Von Bruhl ML, Stark K, Steinhart A, Chandraratne S, Konrad I, Lorenz M, Khandoga A, Tirniceriu A, Coletti R, Kollnberger M, Byrne RA, Laitinen I, Walch A, Brill A, Pfeiler S, Manukyan D, Braun S, Lange P, Riegger J, Ware J, Eckart A, Haidari S, Rudelius M, Schulz C, Echtler K, Brinkmann V, Schwaiger M, Preissner KT, Wagner DD, Mackman N, Engelmann B, Massberg S. Monocytes, neutrophils, and platelets cooperate to initiate and propagate venous thrombosis in mice in vivo. J Exp Med 209:819-835, 2012.
57. Walsh NP, Gleeson M, Pyne DB, Nieman DC, Dhabhar FS, Shephard RJ, Oliver SJ, Bermon S, Kajeniene A. Position statement. Part two: maintaining immune health. Exerc Immunol Rev 17:64-103, 2011.
58. Walsh NP, Gleeson M, Shephard RJ, Gleeson M, Woods JA, Bishop NC, Fleshner M, Green C, Pedersen BK, Hoffman-Goetz L, Rogers CJ, Northoff H, Abbasi A, Simon P. Position statement. Part one: immune function and exercise. Exerc Immunol Rev 17:6-63, 2011.
59. Yipp BG, Petri B, Salina D, Jenne CN, Scott BN, Zbytnuik LD, Pittman K, Asaduzzaman M, Wu K, Meijndert HC, Malawista SE, De Boisfleury CA, Zhang K, Conly J, Kubes P. Infection-induced NETosis is a dynamic process involving neutrophil multitasking in vivo. Nat Med 18:1386-1393, 2012.