2fib › Citations

The primary fibrin polymerization pocket: three-dimensional structure of a 30-kDa C-terminal gamma chain fragment complexed with the peptide Gly-Pro-Arg-Pro.

Pratt KP, Côté HC, Chung DW, Stenkamp RE, Davie EW
Proc Natl Acad Sci U S A 94 7176-81 (1997)
Cited: 80 times
EuropePMC logo PMID: 9207064

Abstract

After vascular injury, a cascade of serine protease activations leads to the conversion of the soluble fibrinogen molecule into fibrin. The fibrin monomers then polymerize spontaneously and noncovalently to form a fibrin gel. The primary interaction of this polymerization reaction is between the newly exposed N-terminal Gly-Pro-Arg sequence of the alpha chain of one fibrin molecule and the C-terminal region of a gamma chain of an adjacent fibrin(ogen) molecule. In this report, the polymerization pocket has been identified by determining the crystal structure of a 30-kDa C-terminal fragment of the fibrin(ogen) gamma chain complexed with the peptide Gly-Pro-Arg-Pro. This peptide mimics the N terminus of the alpha chain of fibrin. The conformational change in the protein upon binding the peptide is subtle, with electrostatic interactions primarily mediating the association. This is consistent with biophysical experiments carried out over the last 50 years on this fundamental polymerization reaction.

Articles - 2fib mentioned but not cited (7)

  1. The primary fibrin polymerization pocket: three-dimensional structure of a 30-kDa C-terminal gamma chain fragment complexed with the peptide Gly-Pro-Arg-Pro. Pratt KP, Côté HC, Chung DW, Stenkamp RE, Davie EW. Proc Natl Acad Sci U S A 94 7176-7181 (1997)
  2. Identification and characterization of the fibrinogen-like domain of fibrinogen-related proteins in the mosquito, Anopheles gambiae, and the fruitfly, Drosophila melanogaster, genomes. Wang X, Zhao Q, Christensen BM. BMC Genomics 6 114 (2005)
  3. A protein-DNA docking benchmark. van Dijk M, Bonvin AM. Nucleic Acids Res 36 e88 (2008)
  4. Quantitative prediction of protein-protein binding affinity with a potential of mean force considering volume correction. Su Y, Zhou A, Xia X, Li W, Sun Z. Protein Sci 18 2550-2558 (2009)
  5. Electrophilic-Nucleophilic Dualism of Nickel(II) toward Ni···I Noncovalent Interactions: Semicoordination of Iodine Centers via Electron Belt and Halogen Bonding via σ-Hole. Bikbaeva ZM, Ivanov DM, Novikov AS, Ananyev IV, Bokach NA, Kukushkin VY. Inorg Chem 56 13562-13578 (2017)
  6. Using parallelized incremental meta-docking can solve the conformational sampling issue when docking large ligands to proteins. Devaurs D, Antunes DA, Hall-Swan S, Mitchell N, Moll M, Lizée G, Kavraki LE. BMC Mol Cell Biol 20 42 (2019)
  7. High Resolution Prediction of Calcium-Binding Sites in 3D Protein Structures Using FEATURE. Zhou W, Tang GW, Altman RB. J Chem Inf Model 55 1663-1672 (2015)


Reviews citing this publication (14)

  1. Fibrinogen and fibrin structure and functions. Mosesson MW. J Thromb Haemost 3 1894-1904 (2005)
  2. Fibrin clot structure and function: a role in the pathophysiology of arterial and venous thromboembolic diseases. Undas A, Ariëns RA. Arterioscler Thromb Vasc Biol 31 e88-99 (2011)
  3. The molecular basis of quantitative fibrinogen disorders. Asselta R, Duga S, Tenchini ML. J Thromb Haemost 4 2115-2129 (2006)
  4. Fibrinogen gamma chain functions. Mosesson MW. J Thromb Haemost 1 231-238 (2003)
  5. Functional impact of oxidative posttranslational modifications on fibrinogen and fibrin clots. Martinez M, Weisel JW, Ischiropoulos H. Free Radic Biol Med 65 411-418 (2013)
  6. The thrombin-fibrinogen interaction. Scheraga HA. Biophys Chem 112 117-130 (2004)
  7. X-ray crystallographic studies on fibrinogen and fibrin. Doolittle RF. J Thromb Haemost 1 1559-1565 (2003)
  8. Structural basis of the fibrinogen-fibrin transformation: contributions from X-ray crystallography. Doolittle RF. Blood Rev 17 33-41 (2003)
  9. Fibrinogen-Related Proteins in Tissue Repair: How a Unique Domain with a Common Structure Controls Diverse Aspects of Wound Healing. Zuliani-Alvarez L, Midwood KS. Adv Wound Care (New Rochelle) 4 273-285 (2015)
  10. Three-dimensional structural studies on fragments of fibrinogen and fibrin. Doolittle RF, Spraggon G, Everse SJ. Curr Opin Struct Biol 8 792-798 (1998)
  11. Biomaterials for Bioprinting Microvasculature. Barrs RW, Jia J, Silver SE, Yost M, Mei Y. Chem Rev 120 10887-10949 (2020)
  12. Crystal structure studies on fibrinogen and fibrin. Doolittle RF, Yang Z, Mochalkin I. Ann N Y Acad Sci 936 31-43 (2001)
  13. Fibrin(ogen) as a Therapeutic Target: Opportunities and Challenges. Gaule TG, Ajjan RA. Int J Mol Sci 22 6916 (2021)
  14. New insights into fibrin (ogen) structure and function. Everse SJ. Vox Sang 83 Suppl 1 375-382 (2002)

Articles citing this publication (59)

  1. Crystal structures of fragment D from human fibrinogen and its crosslinked counterpart from fibrin. Spraggon G, Everse SJ, Doolittle RF. Nature 389 455-462 (1997)
  2. Structural basis for distinctive recognition of fibrinogen gammaC peptide by the platelet integrin alphaIIbbeta3. Springer TA, Zhu J, Xiao T. J Cell Biol 182 791-800 (2008)
  3. A model of fibrin formation based on crystal structures of fibrinogen and fibrin fragments complexed with synthetic peptides. Yang Z, Mochalkin I, Doolittle RF. Proc Natl Acad Sci U S A 97 14156-14161 (2000)
  4. A novel variant of the immunoglobulin fold in surface adhesins of Staphylococcus aureus: crystal structure of the fibrinogen-binding MSCRAMM, clumping factor A. Deivanayagam CC, Wann ER, Chen W, Carson M, Rajashankar KR, Höök M, Narayana SV. EMBO J 21 6660-6672 (2002)
  5. The crystal structure of modified bovine fibrinogen. Brown JH, Volkmann N, Jun G, Henschen-Edman AH, Cohen C. Proc Natl Acad Sci U S A 97 85-90 (2000)
  6. The 2.0-A crystal structure of tachylectin 5A provides evidence for the common origin of the innate immunity and the blood coagulation systems. Kairies N, Beisel HG, Fuentes-Prior P, Tsuda R, Muta T, Iwanaga S, Bode W, Huber R, Kawabata S. Proc Natl Acad Sci U S A 98 13519-13524 (2001)
  7. Polymerization of fibrin: specificity, strength, and stability of knob-hole interactions studied at the single-molecule level. Litvinov RI, Gorkun OV, Owen SF, Shuman H, Weisel JW. Blood 106 2944-2951 (2005)
  8. Crystal structures of the Tie2 receptor ectodomain and the angiopoietin-2-Tie2 complex. Barton WA, Tzvetkova-Robev D, Miranda EP, Kolev MV, Rajashankar KR, Himanen JP, Nikolov DB. Nat Struct Mol Biol 13 524-532 (2006)
  9. Platelet-rich fibrin application in dentistry: a literature review. Borie E, Oliví DG, Orsi IA, Garlet K, Weber B, Beltrán V, Fuentes R. Int J Clin Exp Med 8 7922-7929 (2015)
  10. Structure of the angiopoietin-2 receptor binding domain and identification of surfaces involved in Tie2 recognition. Barton WA, Tzvetkova D, Nikolov DB. Structure 13 825-832 (2005)
  11. Variations in chondrogenesis of human bone marrow-derived mesenchymal stem cells in fibrin/alginate blended hydrogels. Ma K, Titan AL, Stafford M, Zheng Ch, Levenston ME. Acta Biomater 8 3754-3764 (2012)
  12. Clinical phenotype, laboratory features and genotype of 35 patients with heritable dysfibrinogenaemia. Shapiro SE, Phillips E, Manning RA, Morse CV, Murden SL, Laffan MA, Mumford AD. Br J Haematol 160 220-227 (2013)
  13. Fibrinogen angers with a new deletion (gamma GVYYQ 346-350) causes hypofibrinogenemia with hepatic storage. Dib N, Quelin F, Ternisien C, Hanss M, Michalak S, De Mazancourt P, Rousselet MC, Calès P. J Thromb Haemost 5 1999-2005 (2007)
  14. The Non-catalytic B Subunit of Coagulation Factor XIII Accelerates Fibrin Cross-linking. Souri M, Osaki T, Ichinose A. J Biol Chem 290 12027-12039 (2015)
  15. B:b interactions are essential for polymerization of variant fibrinogens with impaired holes 'a'. Okumura N, Terasawa F, Haneishi A, Fujihara N, Hirota-Kawadobora M, Yamauchi K, Ota H, Lord ST. J Thromb Haemost 5 2352-2359 (2007)
  16. Role of 'B-b' knob-hole interactions in fibrin binding to adsorbed fibrinogen. Geer CB, Tripathy A, Schoenfisch MH, Lord ST, Gorkun OV. J Thromb Haemost 5 2344-2351 (2007)
  17. Hepatic fibrinogen storage disease: identification of two novel mutations (p.Asp316Asn, fibrinogen Pisa and p.Gly366Ser, fibrinogen Beograd) impacting on the fibrinogen γ-module. Asselta R, Robusto M, Braidotti P, Peyvandi F, Nastasio S, D'Antiga L, Perisic VN, Maggiore G, Caccia S, Duga S. J Thromb Haemost 13 1459-1467 (2015)
  18. Ultrathin self-assembled fibrin sheets. O'Brien ET, Falvo MR, Millard D, Eastwood B, Taylor RM, Superfine R. Proc Natl Acad Sci U S A 105 19438-19443 (2008)
  19. Crystal structure of a recombinant alphaEC domain from human fibrinogen-420. Spraggon G, Applegate D, Everse SJ, Zhang JZ, Veerapandian L, Redman C, Doolittle RF, Grieninger G. Proc Natl Acad Sci U S A 95 9099-9104 (1998)
  20. A classification of the fibrin network structures formed from the hereditary dysfibrinogens. Sugo T, Endo H, Matsuda M, Ohmori T, Madoiwa S, Mimuro J, Sakata Y. J Thromb Haemost 4 1738-1746 (2006)
  21. A double-headed Gly-Pro-Arg-Pro ligand mimics the functions of the E domain of fibrin for promoting the end-to-end crosslinking of gamma chains by factor XIIIa. Lorand L, Parameswaran KN, Murthy SN. Proc Natl Acad Sci U S A 95 537-541 (1998)
  22. Fibrinogen variant BbetaD432A has normal polymerization but does not bind knob "B". Bowley SR, Lord ST. Blood 113 4425-4430 (2009)
  23. Molecular mechanisms, thermodynamics, and dissociation kinetics of knob-hole interactions in fibrin. Kononova O, Litvinov RI, Zhmurov A, Alekseenko A, Cheng CH, Agarwal S, Marx KA, Weisel JW, Barsegov V. J Biol Chem 288 22681-22692 (2013)
  24. Functional analysis of the fibrinogen-related scabrous gene from Drosophila melanogaster identifies potential effector and stimulatory protein domains. Lee EC, Yu SY, Hu X, Mlodzik M, Baker NE. Genetics 150 663-673 (1998)
  25. Multivalent viral capsids with internal cargo for fibrin imaging. Obermeyer AC, Capehart SL, Jarman JB, Francis MB. PLoS One 9 e100678 (2014)
  26. The incipient stage in thrombin-induced fibrin polymerization detected by FCS at the single molecule level. Bark N, Földes-Papp Z, Rigler R. Biochem Biophys Res Commun 260 35-41 (1999)
  27. Hepatitis B spliced protein (HBSP) generated by a spliced hepatitis B virus RNA participates in abnormality of fibrin formation and functions by binding to fibrinogen γ chain. Chen JY, Chen WN, Liu LL, Lin WS, Jiao BY, Wu YL, Lin JY, Lin X. J Med Virol 82 2019-2026 (2010)
  28. Molecular dynamics-based analyses of the structural instability and secondary structure of the fibrinogen gamma chain protein with the D356V mutation. Ali SK, Sneha P, Priyadharshini Christy J, Zayed H, George Priya Doss C. J Biomol Struct Dyn 35 2714-2724 (2017)
  29. Determining the crystal structure of fibrinogen. Doolittle RF. J Thromb Haemost 2 683-689 (2004)
  30. Fibrin-polyethylene oxide interpenetrating polymer networks: new self-supported biomaterials combining the properties of both protein gel and synthetic polymer. Akpalo E, Bidault L, Boissière M, Vancaeyzeele C, Fichet O, Larreta-Garde V. Acta Biomater 7 2418-2427 (2011)
  31. Patho- physiological role of BDNF in fibrin clotting. Amadio P, Porro B, Sandrini L, Fiorelli S, Bonomi A, Cavalca V, Brambilla M, Camera M, Veglia F, Tremoli E, Barbieri SS. Sci Rep 9 389 (2019)
  32. Programmable microbial ink for 3D printing of living materials produced from genetically engineered protein nanofibers. Duraj-Thatte AM, Manjula-Basavanna A, Rutledge J, Xia J, Hassan S, Sourlis A, Rubio AG, Lesha A, Zenkl M, Kan A, Weitz DA, Zhang YS, Joshi NS. Nat Commun 12 6600 (2021)
  33. Structural Basis of Interfacial Flexibility in Fibrin Oligomers. Zhmurov A, Protopopova AD, Litvinov RI, Zhukov P, Mukhitov AR, Weisel JW, Barsegov V. Structure 24 1907-1917 (2016)
  34. Electrospray ionization mass spectrometry identification of fibrinogen Banks Peninsula (gamma280Tyr-->Cys): a new variant with defective polymerization. Fellowes AP, Brennan SO, Ridgway HJ, Heaton DC, George PM. Br J Haematol 101 24-31 (1998)
  35. Fibrinogens Kosai and Ogasa: Bbeta15Gly-->Cys (GGT-->TGT) substitution associated with impairment of fibrinopeptide B release and lateral aggregation. Hirota-Kawadobora M, Terasawa F, Yonekawa O, Sahara N, Shimizu E, Okumura N, Katsuyama T, Shigematsu H. J Thromb Haemost 1 275-283 (2003)
  36. Recombinant γT305A fibrinogen indicates severely impaired fibrin polymerization due to the aberrant function of hole 'A' and calcium binding sites. Ikeda M, Kobayashi T, Arai S, Mukai S, Takezawa Y, Terasawa F, Okumura N. Thromb Res 134 518-525 (2014)
  37. Buffers Strongly Modulate Fibrin Self-Assembly into Fibrous Networks. Kurniawan NA, van Kempen THS, Sonneveld S, Rosalina TT, Vos BE, Jansen KA, Peters GWM, van de Vosse FN, Koenderink GH. Langmuir 33 6342-6352 (2017)
  38. Fibrinogen residue γAla341 is necessary for calcium binding and 'A-a' interactions. Park R, Ping L, Song J, Hong SY, Choi TY, Choi JR, Gorkun OV, Lord ST. Thromb Haemost 107 875-883 (2012)
  39. Sulfated sericin is a novel anticoagulant influencing the blood coagulation cascade. Sano M, Tamada Y, Niwa K, Morita T, Yoshino G. J Biomater Sci Polym Ed 20 773-783 (2009)
  40. A method to detect nonproline cis peptide bonds in proteins. Weiss MS, Hilgenfeld R. Biopolymers 50 536-544 (1999)
  41. Fibrinogen Seoul (FGG Ala341Asp): a novel mutation associated with hypodysfibrinogenemia. Song KS, Park NJ, Choi JR, Doh HJ, Chung KH. Clin Appl Thromb Hemost 12 338-343 (2006)
  42. Trimeric structure and conformational equilibrium of M-ficolin fibrinogen-like domain. Tanio M, Kondo S, Sugio S, Kohno T. J Synchrotron Radiat 15 243-245 (2008)
  43. A novel fibrinogen variant--Liberec: dysfibrinogenaemia associated with gamma Tyr262Cys substitution. Kotlín R, Sobotková A, Suttnar J, Salaj P, Walterová L, Riedel T, Reicheltová Z, Dyr JE. Eur J Haematol 81 123-129 (2008)
  44. Fibrinogen Milano XIII (Aalpha 19 Arg-->Gly): a dysfunctional variant with an amino acid substitution in the N-terminal polymerization site. Bolliger-Stucki B, Bucciarelli P, Lämmle B, Furlan M. Thromb Res 96 399-405 (1999)
  45. Address Fibrinogen: evolution of the structure-function concept. Keynote address at fibrinogen 2000 congress. Blombäck B. Ann N Y Acad Sci 936 1-10 (2001)
  46. Residue gamma153Cys is essential for the formation of the complexes Aalphagamma and Bbetagamma, assembly intermediates for the AalphaBbetagamma complex and intact fibrinogen. Terasawa F, Fujita K, Okumura N. Clin Chim Acta 353 157-164 (2005)
  47. Fibrinogen Poissy II (gammaN361K): a novel dysfibrinogenemia associated with defective polymerization and peptide B release. Mathonnet F, Guillon L, Detruit H, Mazmanian GM, Dreyfus M, Alvarez JC, Giudicelli Y, de Mazancourt P. Blood Coagul Fibrinolysis 14 293-298 (2003)
  48. Inhaled thrombolytics reduce lung microclot and leukocyte infiltration after acute blood loss. Conhaim RL, Watson KE, Dovi WF, Bates ML. Shock 41 528-536 (2014)
  49. Molecular basis of non-self recognition by the horseshoe crab lectins. Kawabata S, Tsuda R. J Endotoxin Res 8 437-439 (2002)
  50. Polymerization site a function dependence on structural integrity of its nearby calcium binding site. Lounes KC, Okumura N, Hogan KA, Ping L, Lord ST. Ann N Y Acad Sci 936 205-209 (2001)
  51. Self-assembly of soluble unlinked and cross-linked fibrin oligomers. Rosenfeld MA, Leonova VB, Biryukova MI, Vasileva MV. Biochemistry (Mosc) 76 1155-1163 (2011)
  52. Structure and function of fibrinogen BβN-domains. Medved L, Yakovlev S. Ukr Biochem J 92 22-32 (2020)
  53. Thrombin inhibitors based on single-stranded DNA aptamers. Gribkova IV, Spiridonova VA, Gorbatenko AS, Denisov SS, Ataullakhanov FI, Sinauridze EI. Blood Coagul Fibrinolysis 25 39-45 (2014)
  54. Bothrops jararaca Snake Venom Inflammation Induced in Human Whole Blood: Role of the Complement System. Leonel TB, Gabrili JJM, Squaiella-Baptistão CC, Woodruff TM, Lambris JD, Tambourgi DV. Front Immunol 13 885223 (2022)
  55. The fibrinogen RIBS-I epitope (gamma373-385) appears proximate to the gamma408-411 adhesive domain but is not involved in interaction between receptor-bound or surface-adsorbed fibrinogen and platelet GPIIbIIIa. Liu Q, Frojmovic MM. Biochim Biophys Acta 1429 217-229 (1998)
  56. Caprin-1 binding to the critical stress granule protein G3BP1 is influenced by pH. Schulte T, Panas MD, Han X, Williams L, Kedersha N, Fleck JS, Tan TJC, Dopico XC, Olsson A, Morro AM, Hanke L, Nilvebrant J, Giang KA, Nygren PÅ, Anderson P, Achour A, McInerney GM. Open Biol 13 220369 (2023)
  57. Case Reports Fibrin clot interference in a human chorionic gonadotrophin assay causing a false Down syndrome screening result. Akagac AE, Yavuz HB. Biochem Med (Zagreb) 33 011001 (2023)
  58. Optimization and evaluation of a two-stage chromogenic assay procedure for measurement of emicizumab plasma levels. Hamedani NS, Oldenburg J, Pötzsch B, Müller J. PLoS One 17 e0271330 (2022)
  59. Protein-protein interactions between tenascin-R and RPTPζ/phosphacan are critical to maintain the architecture of perineuronal nets. Sinha A, Kawakami J, Cole KS, Ladutska A, Nguyen MY, Zalmai MS, Holder BL, Broerman VM, Matthews RT, Bouyain S. J Biol Chem 299 104952 (2023)


Quick links