Post-translational oxidative modification of fibrinogen is associated with coagulopathy after traumatic injury

Free Radical Biology and Medicine

Volumn 96, Issue , 2016, Pages 181-189

  White, Nathan J ^a,b   Wang, Yi ^b   Fu, Xiaoyun ^b   Cardenas, Jessica C ^c   Martin, Erika J ^d   Brophy, Donald F ^d   Wade, Charles E ^c   Wang, Xu ^a   St John, Alexander E ^a   Lim, Esther B ^a   Stern, Susan A ^a   Ward, Kevin R ^e   López, José A ^b   Chung, Dominic ^b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b Bloodworks Northwest Research Institute   (United States)

^c UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^d VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^e UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

Author keywords

Coagulopathy; Fibrinogen; Hemorrhage; Methionine sulfoxide; Oxidative stress; Trauma

Indexed keywords

FIBRINOGEN; METHIONINE SULFOXIDE; FIBRIN; FIBRINOGEN AALPHA; METHIONINE;

ADULT; ARTICLE; BLOOD CLOTTING DISORDER; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; HUMAN; HUMAN CELL; INJURY; MASS SPECTROMETRY; OXIDATIVE STRESS; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROCESSING; ANALOGS AND DERIVATIVES; BLEEDING; BLOOD CLOTTING; COMPLICATION; FEMALE; GENETICS; MALE; METABOLISM; MIDDLE AGED; PATHOLOGY; THROMBOSIS;

ADULT; BLOOD COAGULATION; FEMALE; FIBRIN; FIBRINOGEN; HEMORRHAGE; HUMANS; MALE; METHIONINE; MIDDLE AGED; OXIDATIVE STRESS; THROMBOSIS; WOUNDS AND INJURIES;

EID: 84964981041     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2016.04.023     Document Type: Article

References (48)

1. K. Brohi, J. Singh, M. Heron, and T. Coats Acute traumatic coagulopathy J. Trauma-Injury Infect. Crit. Care 54 6 2003 1127 1130
2. I.D. Peltan, L.K. Vande Vusse, R.V. Maier, and T.R. Watkins An international normalized ratio-based definition of acute traumatic coagulopathy is associated with mortality, venous thromboembolism, and multiple organ failure after injury Crit. Care Med. 43 7 2015 1429 1438 10.1097/CCM.0000000000000981
3. R. Davenport, J. Manson, H. De'Ath, S. Platton, A. Coates, S. Allard, D. Hart, R. Pearse, K.J. Pasi, P. MacCallum, S. Stanworth, and K. Brohi Functional definition and characterization of acute traumatic coagulopathy Crit. Care Med. 39 12 2011 2652 2658
4. D. Frith, J.C. Goslings, C. Gaarder, M. Maegele, M.J. Cohen, S. Allard, P.I. Johansson, S. Stanworth, C. Thiemermann, and K. Brohi Definition and drivers of acute traumatic coagulopathy: clinical and experimental investigations J. Thromb. Haemost. 8 9 2010 1919 1925 10.1111/j.1538-7836.2010.03945.x
5. K. Brohi, M.J. Cohen, M.T. Ganter, M.A. Matthay, R.C. Mackersie, and J. Pittet Acute traumatic coagulopathy: initiated by hypoperfusion: modulated through the protein C pathway? Ann. Surg. 245 5 2007 812 818
6. J.C. Cardenas, N. Matijevic, L.A. Baer, J.B. Holcomb, B.A. Cotton, and C.E. Wade Elevated tissue plasminogen activator and reduced plasminogen activator inhibitor promote hyperfibrinolysis in trauma patients Shock 41 6 2014 514 521 10.1097/SHK.0000000000000161
7. M. Hayakawa, A. Sawamura, S. Gando, N. Kubota, S. Uegaki, H. Shimojima, M. Sugano, and M. Ieko Disseminated intravascular coagulation at an early phase of trauma is associated with consumption coagulopathy and excessive fibrinolysis both by plasmin and neutrophil elastase Surgery 149 2 2011 221 230
8. J.W. Weisel, and R.I. Litvinov The biochemical and physical process of fibrinolysis and effects of clot structure and stability on the lysis rate Cardiovasc. Hematol. Agents Med. Chem. 6 3 2008 161 180
9. M.E. Carr, and B.M. Alving Effect of fibrin structure on plasmin-mediated dissolution of plasma clots Blood Coagul. Fibrinolysis 6 6 1995 567 573
10. H. Schochl, T. Frietsch, M. Pavelka, and C. Jámbor Hyperfibrinolysis after major trauma: differential diagnosis of lysis patterns and prognostic value of thrombelastometry J. Trauma 67 1 2009 125 131
11. CRASH-2 trial collaborators, H. Shakur, I. Roberts, R. Bautista, J. Caballero, T. Coats, Y. Dewan, H. El-Sayed, T. Gogichaishvili, S. Gupta, J. Herrera, B. Hunt, P. Iribhogbe, M. Izurieta, H. Khamis, E. Komolafe, M.A. Marrero, J. Mejía-Mantilla, J. Miranda, C. Morales, O. Olaomi, F. Olldashi, P. Perel, R. Peto, P.V. Ramana, R.R. Ravi, and S. Yutthakasemsunt Effects of tranexamic acid on death, vascular occlusive events, and blood transfusion in trauma patients with significant haemorrhage (CRASH-2): a randomised, placebo-controlled trial Lancet 3 376(9734) 2010 23 32
12. C. Rourke, N. Curry, S. Khan, R. Taylor, I. Raza, I. Davenport, S. Stanworth, and K. Brohi Fibrinogen levels during trauma hemorrhage, response to replacement therapy, and association with patient outcomes J. Thromb. Haemost. 10 7 2012 1342 1351
13. S.T. Hiippala, G.J. Myllyki, and E.M. Vahtera Hemostatic factors and replacement of major blood loss with plasma-poor red cell concentrates Anesth. Analg. 81 1995 360 365
14. E. Shacter, J.A. Williams, M. Lim, and R.L. Levine Differential susceptibility of plasma proteins to oxidative modification: examination by western blot immunoassay Free Radic. Biol. Med. 17 5 1994 429 437
15. K.M. Weigandt, N. White, D. Chung, E. Ellingson, Y. Wang, X. Fu, and D.C. Pozzo Fibrin clot structure and mechanics associated with specific oxidation of methionine residues in fibrinogen Biophys. J. 103 11 2012 2399 2407 10.1016/j.bpj.2012.10.036
16. P.R. Burney, N. White, and J. Pfaendtner Structural effects of methionine oxidation on isolated subdomains of human fibrin D and αC regions PLoS One 9 1 2014 e86981 10.1371/journal.pone.0086981
17. H. Rosen, S.J. Klebanoff, Y. Wang, N. Brot, J.W. Heinecke, and X. Fu Methionine oxidation contributes to bacterial killing by the myeloperoxidase system of neutrophils Proc. Natl. Acad. Sci. USA 106 44 2009 18686 18691 10.1073/pnas.0909464106
18. H.M. Brandfellner, S.B. Ruparel, J.A. Gelfond, and K.M. Hargreaves Major blunt trauma evokes selective upregulation of oxidative enzymes in circulating leukocytes Shock 40 3 2013 182 187 10.1097/SHK.0b013e31829de02f
19. C. Laplace, O. Huet, E. Vicaut, C. Ract, L. Martin, D. Benhamou, and J. Duranteau Endothelial oxidative stress induced by serum from patients with severe trauma hemorrhage Intensive Care Med. 31 9 2005 1174 1180
20. C. Szabó, and K. Módis Pathophysiological roles of peroxynitrite in circulatory shock Shock 34 Suppl. 1 2010 S4 S14
21. J.B. Holcomb, K.M. Minei, M.L. Scerbo, Z.A. Radwan, C.E. Wade, R.A. Kozar, B.S. Gill, R. Albarado, M.K. McNutt, S. Khan, P.R. Adams, J.J. McCarthy, and B.A. Cotton Admission rapid thrombelastography can replace conventional coagulation tests in the emergency department: experience with 1974 consecutive trauma patients Ann. Surg. 256 3 2012 476 486 10.1097/SLA.0b013e3182658180
22. M.P. Chapman, E.E. Moore, C.R. Ramos, A. Ghasabyan, J.N. Harr, T.L. Chin, J.R. Stringham, A. Sauaia, C.C. Silliman, and A. Banerjee Fibrinolysis greater than 3% is the critical value for initiation of antifibrinolytic therapy J. Trauma Acute Care Surg. 75 6 2013 961 967 10.1097/TA.0b013e3182aa9c9f
23. B.A. Cotton, J.A. Harvin, V. Kostousouv, K.M. Minei, Z.A. Radwan, H. Schockl, C.E. Wade, J.B. Holcomb, and N. Matijevic Hyperfibrinolysis at admission is an uncommon but highly lethal event associated with shock and prehospital fluid administration J. Trauma Acute Care Surg. 73 2 2012 365 370
24. L. Selmeci, M. Székely, P. Soós, L. Seres, N. Klinga, A. Geiger, and G. Acsády Human blood plasma advanced oxidation protein products (AOPP) correlates with fibrinogen levels Free Radic. Res. 40 9 2006 952 958
25. H. Liu, T. Han, J. Tian, Z.Y. Zhu, Y. Liu, Y. Li, S.X. Xiao, Y. Li, and Y.Y. Feng Monitoring oxidative stress in acute-on-chronic liver failure by advanced oxidation protein products Hepatol. Res. 42 2 2012 171 180 10.1111/j.1872-034X.2011.00911.x
26. L. Selmeci, L. Seres, M. Antal, J. Lukács, A. Regöly-Mérei, and G. Acsády Advanced oxidation protein products (AOPP) for monitoring oxidative stress in critically ill patients: a simple, fast and inexpensive automated technique Clin. Chem. Lab. Med. 43 3 2005 294 297
27. V. Witko-Sarsat, M. Friedlander, C. Capeillère-Blandin, T. Nguyen-Khoa, A.T. Nguyen, J. Zingraff, P. Jungers, and B. Descamps-Latscha Advanced oxidation protein products as a novel marker of oxidative stress in uremia Kidney Int. 49 5 1996 1304 1313
28. C. Capeillère-Blandin, V. Gausson, A.T. Nguyen, B. Descamps-Latscha, T. Drüeke, and V. Witko-Sarsat Respective role of uraemic toxins and myeloperoxidase in the uraemic state Nephrol. Dial. Transplant. 21 6 2006 1555 1563
29. M.J. Flick, X. Du, D.P. Witte, M. Jirousková, D.A. Soloviev, S.J. Busuttil, E.F. Plow, and J.L. Degen Leukocyte engagement of fibrin(ogen) via the integrin receptor alphaMbeta2/Mac-1 is critical for host inflammatory response in vivo J. Clin. Invest. 113 11 2004 1596 1606
30. D.I. Pattison, and M.J. Davies Absolute rate constants for the reaction of hypochlorous acid with protein side-chains and peptide bonds Chem. Res. Toxicol. 14 2001 1453 1464
31. J. Arnhold, S. Hammerschmidt, and K. Arnold Role of functional groups of human plasma and luminol in scavenging of NaOCl and neutrophil-derived hypochlorous acid Biochim. Biophys. Acta 1097 2 1991 145 151
32. G. Branlant The enzymology and biochemistry of methionine sulfoxide reductases Biochim. Biophys. Acta 1703 2 2005 231 238
33. A. Nishiyama, H. Masutani, H. Nakamura, Y. Nishinaka, and J. Yodoi Redox regulation by thioredoxin and thioredoxin-binding proteins IUBMB Life 52 1-2 2001 29 33
34. M. Xiang, X. Shi, Y. Li, J. Xu, L. Yin, G. Xiao, M.J. Scott, T.R. Billiar, M.A. Wilson, and J. Fan Hemorrhagic shock activation of NLRP3 inflammasome in lung endothelial cells J. Immunol. 187 9 2011 4809 4811
35. L.T. Rael, R. Bar-Or, K. Salottolo, C.W. Mains, D.S. Slone, P.J. Offner, and D. Bar-Or Injury severity and serum amyloid A correlate with plasma oxidation-reduction potential in multi-trauma patients: a retrospective analysis Scand. J.Trauma Resusc. Emerg. Med. 19 2009 17 57
36. O.V. Gorkun, Y.I. Veklich, L.V. Medved, A.H. Henschen, and J.W. Weisel Role of the alpha C domains of fibrin in clot formation Biochemistry 33 1994 6986 6997
37. J.W. Weisel, and L. Medved The structure and function of the alpha C domains of fibrinogen Ann. N. Y. Acad. Sci. 936 2001 312 327
38. L. Ping, L. Huang, B. Cardinali, A. Profumo, O.V. Gorkun, and S.T. Lord Substitution of the human αC region with the analogous chicken domain generates a fibrinogen with severely impaired lateral aggregation: fibrin monomers assemble into protofibrils but protofibrils do not assemble into fibers Biochemistry 50 42 2011 9066 9075 10.1021/bi201094v
39. G. Tsurupa, I. Pechik, R.I. Litvinov, R.R. Hantgan, N. Tjandra, J.W. Weisel, and L. Medved On the mechanism of αC polymer formation in fibrin Biochemistry 51 12 2012 2526 2538 10.1021/bi2017848
40. H. Maekawa, K. Yamazumi, S. Muramatsu, M. Kaneko, H. Hirata, N. Takahashi, N.B. de Bosch, Z. Carvajal, A. Ojeda, and C.L. Arocha-Piñango An A alpha Ser-434 to N-glycosylated Asn substitution in a dysfibrinogen, fibrinogen Caracas II, characterized by impaired fibrin gel formation J. Biol. Chem. 266 18 1991 11575 11578
41. J.L. Woodhead, C. Nagaswami, M. Matsuda, C.L. Arocha-Piñango, and J.W. Weisel The ultrastructure of fibrinogen Caracas II molecules, fibers, and clots J. Biol. Chem. 271 9 1996 4946 4953
42. N.J. White, J.C. Newton, E.J. Martin, B.M. Mohammed, D. Contaifer Jr., J.L. Bostic, G.M. Brophy, B.D. Spiess, A.E. Pusateri, K.R. Ward, and D.F. Brophy Clot formation is associated with fibrinogen and platelet forces in a cohort of severely-injured Emergency Department trauma patients Shock 44 Suppl. 1 2015 S39 S44
43. A. Nalian, and A.V. Iakhiaev Possible mechanisms contributing to oxidative inactivation of activated protein C: molecular dynamics study Thromb. Haemost. 100 1 2008 18 25
44. C.B. Glaser, J. Morser, J.H. Clarke, E. Blasko, K. McLean, I. Kuhn, R.J. Chang, J.H. Lin, L. Vilander, H. William, W.H. Andrews, and D.R. Light Oxidation of a specific methionine in thrombomodulin by activated neutrophil products blocks cofactor activity J. Clin. Invest. 90 1992 2565 2573
45. Schöchl H1, W. Voelckel, A. Grassetto, and C.J. Schlimp Practical application of point-of-care coagulation testing to guide treatment decisions in trauma J. Trauma Acute Care Surg. 74 6 2013 1587 1598 10.1097/TA.0b013e31828c3171
46. L. Thomson, J. Christie, C. Vadseth, P.N. Lanken, X. Fu, S.L. Hazen, and H. Ischiropoulos Identification of immunoglobulins that recognize 3-nitrotyrosine in patients with acute lung injury after major trauma Am. J. Respir. Cell Mol. Biol. 36 2 2007 152 157
47. A.B. Nathens, M.J. Neff, G.J. Jurkovich, P. Klotz, K. Farver, J.T. Ruzinski, F. Radella, I. Garcia, and R.V. Maier Randomized, prospective trial of antioxidant supplementation in critically ill surgical patients Ann. Surg. 236 6 2002 814 822
48. L. Selmeci, L. Seres, M. Székely, P. Soós, and G. Acsády Assay of oxidized fibrinogen reactivity (OFR) as a biomarker of oxidative stress in human plasma: the role of lysine analogs Clin. Chem. Lab. Med. 48 3 2010 379 382 10.1515/CCLM.2010.076