1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Biophysics
  4. Volume 51, 2022
  5. Article

Annual Review of Biophysics

Volume 51, 2022

Nanomechanics of Blood Clot and Thrombus Formation

Abstract

Mechanical properties have been extensively studied in pure elastic or viscous materials; however, most biomaterials possess both physical properties in a viscoelastic component. How the biomechanics of a fibrin clot is related to its composition and the microenvironment where it is formed is not yet fully understood. This review gives an outline of the building mechanisms for blood clot mechanical properties and how they relate to clot function. The formation of a blood clot in health conditions or the formation of a dangerous thrombus go beyond the mere polymerization of fibrinogen into a fibrin network. The complex composition and localization of in vivo fibrin clots demonstrate the interplay between fibrin and/or fibrinogen and blood cells. The study of these protein–cell interactions and clot mechanical properties may represent new methods for the evaluation of cardiovascular diseases (the leading cause of death worldwide), creating new possibilities for clinical diagnosis, prognosis, and therapy.

Keyword(s): cardiovascular diseases, clot mechanics, erythrocyte, fibrin fiber, platelet, red blood cell, thrombosis
Loading

Article metrics loading...

/content/journals/10.1146/annurev-biophys-111821-072110
2022-05-09
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/biophys/51/1/annurev-biophys-111821-072110.html?itemId=/content/journals/10.1146/annurev-biophys-111821-072110&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Adhikari AS, Mekhdjian AH, Dunn AR. 2012. Strain tunes proteolytic degradation and diffusive transport in fibrin networks. Biomacromolecules 13:499–506
     [Google Scholar]
  2. 2.
    Aleman MM, Byrnes JR, Wang J-G, Tran R, Lam WA et al. 2014. Factor XIII activity mediates red blood cell retention in venous thrombi. J. Clin. Investig. 124:3590–600
     [Google Scholar]
  3. 3.
    Andrieux A, Hudry-Clergeon G, Ryckewaert JJ, Chapel A, Ginsberg MH et al. 1989. Amino acid sequences in fibrinogen mediating its interaction with its platelet receptor, GPIIbIIIa. J. Biol. Chem. 264:9258–65
     [Google Scholar]
  4. 4.
    Ariëns RAS. 2013. Fibrin(ogen) and thrombotic disease. J. Thromb. Haemost. 11:294–305
     [Google Scholar]
  5. 5.
    Averett RD, Menn B, Lee EH, Helms CC, Barker T, Guthold M. 2012. A modular fibrinogen model that captures the stress-strain behavior of fibrin fibers. Biophys. J. 103:1537–44
     [Google Scholar]
  6. 6.
    Barattin R, Voyer N. 2008. Chemical modifications of AFM tips for the study of molecular recognition events. Chem. Commun. 13:1513–32
     [Google Scholar]
  7. 7.
    Barua RS, Sy F, Srikanth S, Huang G, Javed U et al. 2010. Acute cigarette smoke exposure reduces clot lysis—association between altered fibrin architecture and the response to t-PA. Thromb. Res. 126:426–30
     [Google Scholar]
  8. 8.
    Barua RS, Sy F, Srikanth S, Huang G, Javed U et al. 2010. Effects of cigarette smoke exposure on clot dynamics and fibrin structure: an ex vivo investigation. Arterioscler. Thromb. Vasc. Biol. 30:75–79
     [Google Scholar]
  9. 9.
    Bellin A, Berto P, Themistoclakis S, Chandak A, Giusti P et al. 2019. New oral anti-coagulants versus vitamin K antagonists in high thromboembolic risk patients. PLOS ONE 14:e0222762
     [Google Scholar]
  10. 10.
    Belyaev AV, Panteleev MA, Ataullakhanov FI. 2015. Threshold of microvascular occlusion: Injury size defines the thrombosis scenario. Biophys. J. 109:450–56
     [Google Scholar]
  11. 11.
    Bennett JS. 2005. Structure and function of the platelet integrin αIIbβ3. J. Clin. Investig. 115:3363–69
     [Google Scholar]
  12. 12.
    Bentzon JF, Otsuka F, Virmani R, Falk E. 2014. Mechanisms of plaque formation and rupture. Circ. Res. 114:1852–66
     [Google Scholar]
  13. 13.
    Besser MW, MacDonald SG. 2016. Acquired hypofibrinogenemia: current perspectives. J. Blood Med. 7:217–25
     [Google Scholar]
  14. 14.
    Blat A, Dybas J, Chrabaszcz K, Bulat K, Jasztal A et al. 2019. FTIR, Raman and AFM characterization of the clinically valid biochemical parameters of the thrombi in acute ischemic stroke. Sci. Rep. 9:15475
     [Google Scholar]
  15. 15.
    Bridge K, Philippou H, Ariëns R. 2014. Clot properties and cardiovascular disease. Thromb. Haemost. 112:901–8
     [Google Scholar]
  16. 16.
    Brown AEX, Litvinov RI, Discher DE, Purohit PK, Weisel JW. 2009. Multiscale mechanics of fibrin polymer: gel stretching with protein unfolding and loss of water. Science 325:741–44
     [Google Scholar]
  17. 17.
    Bucay I, O'Brien ET, Wulfe SD, Superfine R, Wolberg AS et al. 2015. Physical determinants of fibrinolysis in single fibrin fibers. PLOS ONE 10:e0116350
     [Google Scholar]
  18. 18.
    Burla F, Mulla Y, Vos BE, Aufderhorst-Roberts A, Koenderink GH. 2019. From mechanical resilience to active material properties in biopolymer networks. Nat. Rev. Phys. 1:249–63
     [Google Scholar]
  19. 19.
    Byrnes JR, Duval C, Wang Y, Hansen CE, Ahn B et al. 2015. Factor XIIIa-dependent retention of red blood cells in clots is mediated by fibrin α-chain crosslinking. Blood 126:1940–48
     [Google Scholar]
  20. 20.
    Byrnes JR, Wolberg AS. 2017. Red blood cells in thrombosis. Blood 130:1795–99
     [Google Scholar]
  21. 21.
    Campbell RA, Aleman M, Gray LD, Falvo MR, Wolberg AS. 2010. Flow profoundly influences fibrin network structure: implications for fibrin formation and clot stability in haemostasis. Thromb. Haemost. 104:1281–84
     [Google Scholar]
  22. 22.
    Carvalho FA, Connell S, Miltenberger-Miltenyi G, Pereira SV, Tavares A et al. 2010. Atomic force microscopy-based molecular recognition of a fibrinogen receptor on human erythrocytes. ACS Nano 4:4609–20
     [Google Scholar]
  23. 23.
    Carvalho FA, de Oliveira S, Freitas T, Gonçalves S, Santos NC 2011. Variations on fibrinogen-erythrocyte interactions during cell aging. PLOS ONE 6:e18167
     [Google Scholar]
  24. 24.
    Carvalho FA, Freitas T, Santos NC. 2015. Taking nanomedicine teaching into practice with atomic force microscopy and force spectroscopy. Adv. Physiol. Educ. 39:360–66
     [Google Scholar]
  25. 25.
    Carvalho FA, Guedes AF, Duval C, Macrae FL, Swithenbank L et al. 2018. The 95RGD97 sequence on the Aα chain of fibrinogen is essential for binding to its erythrocyte receptor. Int. J. Nanomed. 13:1985–92
     [Google Scholar]
  26. 26.
    Carvalho FA, Santos NC. 2012. Atomic force microscopy-based force spectroscopy—biological and biomedical applications. IUBMB Life 64:465–72
     [Google Scholar]
  27. 27.
    Casini A, Blondon M, Lebreton A, Koegel J, Tintillier V et al. 2015. Natural history of patients with congenital dysfibrinogenemia. Blood 125:553–61
     [Google Scholar]
  28. 28.
    Chandrashekar A, Singh G, Jonah G, Sikalas N, Labropoulos N 2018. Mechanical and biochemical role of fibrin within a venous thrombus. Eur. J. Vasc. Endovasc. Surg. 55:417–24
     [Google Scholar]
  29. 29.
    Chang H, Kuo MC, Shih LY, Dunn P, Wang PN et al. 2012. Clinical bleeding events and laboratory coagulation profiles in acute promyelocytic leukemia. Eur. J. Haematol. 88:321–28
     [Google Scholar]
  30. 30.
    Chen Z, Lu J, Zhang C, Hsia I, Yu X et al. 2019. Microclot array elastometry for integrated measurement of thrombus formation and clot biomechanics under fluid shear. Nat. Commun. 10:2051
     [Google Scholar]
  31. 31.
    Chernysh IN, Nagaswami C, Kosolapova S, Peshkova AD, Cuker A et al. 2020. The distinctive structure and composition of arterial and venous thrombi and pulmonary emboli. Sci. Rep. 10:5112
     [Google Scholar]
  32. 32.
    Chernysh IN, Spiewak R, Cambor CL, Purohit PK, Weisel JW. 2020. Structure, mechanical properties, and modeling of cyclically compressed pulmonary emboli. J. Mech. Behav. Biomed. Mater. 105:103699
     [Google Scholar]
  33. 33.
    Christensen TD, Jensen C, Larsen TB, Christiansen K, Sørensen B. 2009. Thrombin generation and coagulation factor activities: evaluation and comparison with the international normalized ratio. Blood Coagul. Fibrinol. 20:358–65
     [Google Scholar]
  34. 34.
    Cieslik J, Mrozinska S, Broniatowska E, Undas A 2018. Altered plasma clot properties increase the risk of recurrent deep vein thrombosis: a cohort study. Blood 131:797–807
     [Google Scholar]
  35. 35.
    Collet JP, Allali Y, Lesty C, Tanguy ML, Silvain J et al. 2006. Altered fibrin architecture is associated with hypofibrinolysis and premature coronary atherothrombosis. Arterioscler. Thromb. Vasc. Biol. 26:2567–73
     [Google Scholar]
  36. 36.
    Collet JP, Moen JL, Veklich YI, Gorkun OV, Lord ST et al. 2005. The αC domains of fibrinogen affect the structure of the fibrin clot, its physical properties, and its susceptibility to fibrinolysis. Blood 106:3824–30
     [Google Scholar]
  37. 37.
    Cooper AV, Standeven KF, Ariëns RA. 2003. Fibrinogen gamma-chain splice variant γ′ alters fibrin formation and structure. Blood 102:535–40
     [Google Scholar]
  38. 38.
    de Moerloose P, Boehlen F, Neerman-Arbez M. 2010. Fibrinogen and the risk of thrombosis. Semin. Thromb. Hemost. 36:7–17
     [Google Scholar]
  39. 39.
    de Moerloose P, Casini A, Neerman-Arbez M. 2013. Congenital fibrinogen disorders: an update. Semin. Thromb. Hemost. 39:585–95
     [Google Scholar]
  40. 40.
    Diaz JA, Fuchs TA, Jackson TO, Kremer Hovinga JA, Lammle B et al. 2013. Plasma DNA is elevated in patients with deep vein thrombosis. J. Vasc. Surg. Venous Lymphat. Disord. 1:341–48.e1
     [Google Scholar]
  41. 41.
    Domingues MM, Macrae FL, Duval C, McPherson HR, Bridge KI et al. 2016. Thrombin and fibrinogen γ′ impact clot structure by marked effects on intrafibrillar structure and protofibril packing. Blood 127:487–95
     [Google Scholar]
  42. 42.
    Domínguez-García P, Dietler G, Forró L, Jeney S 2020. Filamentous and step-like behavior of gelling coarse fibrin networks revealed by high-frequency microrheology. Soft Matter 16:4234–42
     [Google Scholar]
  43. 43.
    D'Souza SE, Ginsberg MH, Matsueda GR, Plow EF 1991. A discrete sequence in a platelet integrin is involved in ligand recognition. Nature 350:66–68
     [Google Scholar]
  44. 44.
    D'Souza SE, Haas TA, Piotrowicz RS, Byers-Ward V, McGrath DE et al. 1994. Ligand and cation binding are dual functions of a discrete segment of the integrin β3 subunit: Cation displacement is involved in ligand binding. Cell 79:659–67
     [Google Scholar]
  45. 45.
    Efthymiou M, Lawrie AS, Mackie I, Arachchillage D, Lane PJ et al. 2015. Thrombin generation and factor X assays for the assessment of warfarin anticoagulation in thrombotic antiphospholipid syndrome. Thromb. Res. 135:1191–97
     [Google Scholar]
  46. 46.
    Esterik FV, Vega AV, Pajanonot KAT, Cuizon DR, Velayo ME et al. 2018. Fibrin network adaptation to cell-generated forces. Rheol. Acta 57:603–10
     [Google Scholar]
  47. 47.
    Evans PA, Hawkins K, Morris RHK, Thirumalai N, Munro R et al. 2010. Gel point and fractal microstructure of incipient blood clots are significant new markers of hemostasis for healthy and anticoagulated blood. Blood 116:3341–46
     [Google Scholar]
  48. 48.
    Farrell DH. 2012. γ′ Fibrinogen as a novel marker of thrombotic disease. Clin. Chem. Lab. Med. 50:1903–9
     [Google Scholar]
  49. 49.
    Fereidoonnezhad B, Dwivedi A, Johnson S, McCarthy R, McGarry P 2021. Blood clot fracture properties are dependent on red blood cell and fibrin content. Acta Biomater. 127:213–28
     [Google Scholar]
  50. 50.
    Fleissner F, Bonn M, Parekh SH. 2016. Microscale spatial heterogeneity of protein structural transitions in fibrin matrices. Sci. Adv. 2:e1501778
     [Google Scholar]
  51. 51.
    French DL, Seligsohn U. 2000. Platelet glycoprotein IIb/IIIa receptors and Glanzmann's thrombasthenia. Arterioscler. Thromb. Vasc. Biol. 20:607–10
     [Google Scholar]
  52. 52.
    Fuchs TA, Brill A, Wagner DD. 2012. Neutrophil extracellular trap (NET) impact on deep vein thrombosis. Arterioscler. Thromb. Vasc. Biol. 32:1777–83
     [Google Scholar]
  53. 53.
    Gailit J, Clarke C, Newman D, Tonnesen MG, Mosesson MW, Clark RA. 1997. Human fibroblasts bind directly to fibrinogen at RGD sites through integrin αvβ3. Exp. Cell Res. 232:118–26
     [Google Scholar]
  54. 54.
    García-Arribas AB, Ahyayauch H, Sot J, López-González PL, Alonso A, Goñi FM 2016. Ceramide-induced lamellar gel phases in fluid cell lipid extracts. Langmuir 32:9053–63
     [Google Scholar]
  55. 55.
    Gatt A, van Veen JJ, Bowyer A, Woolley AM, Cooper P et al. 2008. Wide variation in thrombin generation in patients with atrial fibrillation and therapeutic International Normalized Ratio is not due to inflammation. Br. J. Haematol. 142:946–52
     [Google Scholar]
  56. 56.
    Gersh KC, Edmondson KE, Weisel JW. 2010. Flow rate and fibrin fiber alignment. J. Thromb. Haemost. 8:2826–28
     [Google Scholar]
  57. 57.
    Gersh KC, Nagaswami C, Weisel JW. 2009. Fibrin network structure and clot mechanical properties are altered by incorporation of erythrocytes. Thromb. Haemost. 102:1169–75
     [Google Scholar]
  58. 58.
    Guedes AF, Carvalho FA, Domingues MM, Macrae FL, McPherson HR et al. 2018. Impact of γ′γ′ fibrinogen interaction with red blood cells on fibrin clots. Nanomedicine 13:2491–505
     [Google Scholar]
  59. 59.
    Guedes AF, Carvalho FA, Domingues MM, Macrae FL, McPherson HR et al. 2018. Sensing adhesion forces between erythrocytes and γ′ fibrinogen, modulating fibrin clot architecture and function. Nanomedicine 14:909–18
     [Google Scholar]
  60. 60.
    Guedes AF, Carvalho FA, Malho I, Lousada N, Sargento L, Santos NC. 2016. Atomic force microscopy as a tool to evaluate the risk of cardiovascular diseases in patients. Nat. Nanotechnol. 11:687–92
     [Google Scholar]
  61. 61.
    Guedes AF, Carvalho FA, Moreira C, Nogueira JB, Santos NC. 2017. Essential arterial hypertension patients present higher cell adhesion forces, contributing to fibrinogen-dependent cardiovascular risk. Nanoscale 9:14897–906
     [Google Scholar]
  62. 62.
    Guedes AF, Moreira C, Nogueira JB, Santos NC, Carvalho FA 2019. Fibrinogen-erythrocyte binding and hemorheology measurements in the assessment of essential arterial hypertension patients. Nanoscale 11:2757–66
     [Google Scholar]
  63. 63.
    Helms CC, Ariëns RAS, Uitte de Willige S, Standeven KF, Guthold M 2012. α−α Cross-links increase fibrin fiber elasticity and stiffness. Biophys. J 102:168–75
     [Google Scholar]
  64. 64.
    Herrick S, Blanc-Brude O, Gray A, Laurent G 1999. Fibrinogen. Int. J. Biochem. Cell Biol. 31:741–46
     [Google Scholar]
  65. 65.
    Houser JR, Hudson NE, Ping L, O'Brien ET, Superfine R et al. 2010. Evidence that αC region is origin of low modulus, high extensibility, and strain stiffening in fibrin fibers. Biophys. J. 99:3038–47
     [Google Scholar]
  66. 66.
    Hudson NE. 2017. Biophysical mechanisms mediating fibrin fiber lysis. Biomed. Res. Int. 2017.2748340
     [Google Scholar]
  67. 67.
    Janmey PA, Amis EJ, Ferry JD 1983. Rheology of fibrin clots. VI. Stress relaxation, creep, and differential dynamic modulus of fine clots in large shearing deformations. J. Rheol. 27:135–53
     [Google Scholar]
  68. 68.
    Kamikura Y, Wada H, Nobori T, Kobayashi T, Sase T et al. 2005. Elevated levels of leukocyte tissue factor mRNA in patients with venous thromboembolism. Thromb. Res. 116:307–12
     [Google Scholar]
  69. 69.
    Kaneko N, Ghovvati M, Komuro Y, Guo L, Khatibi K et al. 2021. A new aspiration device equipped with a hydro-separator for acute ischemic stroke due to challenging soft and stiff clots. Interv. Neuroradiol. In press
    [Google Scholar]
  70. 70.
    Kattula S, Byrnes JR, Wolberg AS. 2017. Fibrinogen and fibrin in hemostasis and thrombosis. Arterioscler. Thromb. Vasc. Biol. 37:e13–21
     [Google Scholar]
  71. 71.
    Kim OV, Litvinov RI, Weisel JW, Alber MS. 2014. Structural basis for the nonlinear mechanics of fibrin networks under compression. Biomaterials 35:6739–49
     [Google Scholar]
  72. 72.
    Konings J, Govers-Riemslag JW, Philippou H, Mutch NJ, Borissoff JI et al. 2011. Factor XIIa regulates the structure of the fibrin clot independently of thrombin generation through direct interaction with fibrin. Blood 118:3942–51
     [Google Scholar]
  73. 73.
    Kopytek M, Zabczyk M, Natorska J, Siudut J, Malinowski KP et al. 2019. Viscoelastic properties of plasma fibrin clots are similar in patients on rivaroxaban and vitamin K antagonists. J. Physiol. Pharmacol. 70:79–85
     [Google Scholar]
  74. 74.
    Korte W, Poon MC, Iorio A, Makris M. 2017. Thrombosis in inherited fibrinogen disorders. Transfus. Med. Hemother. 44:70–76
     [Google Scholar]
  75. 75.
    Kozek-Langenecker SA, Ahmed AB, Afshari A, Albaladejo P, Aldecoa C et al. 2017. Management of severe perioperative bleeding: guidelines from the European Society of Anaesthesiology: first update; 2016. Eur. J. Anaesthesiol. 34:332–95
     [Google Scholar]
  76. 76.
    Kurniawan NA, Grimbergen J, Koopman J, Koenderink GH. 2014. Factor XIII stiffens fibrin clots by causing fiber compaction. J. Thromb. Haemost. 12:1687–96
     [Google Scholar]
  77. 77.
    Lakshmanan HHS, Shatzel JJ, Olson SR, McCarty OJT, Maddala J. 2019. Modeling the effect of blood vessel bifurcation ratio on occlusive thrombus formation. Comput. Methods Biomech. Biomed. Engin. 22:972–80
     [Google Scholar]
  78. 78.
    Lau YC, Hardy LJ, Philippou H, Blann AD, Lip GY. 2016. Altered fibrin clot structure in patients with atrial fibrillation and worsening renal function. Thromb. Haemost. 116:408–9
     [Google Scholar]
  79. 79.
    Lauricella AM, Quintana IL, Kordich LC 2002. Effects of homocysteine thiol group on fibrin networks: another possible mechanism of harm. Thromb. Res. 107:75–79
     [Google Scholar]
  80. 80.
    Lawrence MJ, Sabra A, Mills G, Pillai SG, Abdullah W et al. 2015. A new biomarker quantifies differences in clot microstructure in patients with venous thromboembolism. Br. J. Haematol. 168:571–75
     [Google Scholar]
  81. 81.
    Lee I, Marchant RE 2003. Molecular interaction studies of hemostasis: fibrinogen ligand-human platelet receptor interactions. Ultramicroscopy 97:341–52
     [Google Scholar]
  82. 82.
    Litvinov RI, Faizullin DA, Zuev YF, Weisel JW. 2012. The α-helix to β-sheet transition in stretched and compressed hydrated fibrin clots. Biophys. J. 103:1020–27
     [Google Scholar]
  83. 83.
    Litvinov RI, Weisel JW. 2017. Fibrin mechanical properties and their structural origins. Matrix Biol60–61110–23
     [Google Scholar]
  84. 84.
    Litvinov RI, Weisel JW. 2017. Role of red blood cells in haemostasis and thrombosis. ISBT Sci. Ser. 12:176–83
     [Google Scholar]
  85. 85.
    Liu SL, Wu NQ, Shi HW, Dong Q, Dong QT et al. 2020. Fibrinogen is associated with glucose metabolism and cardiovascular outcomes in patients with coronary artery disease. Cardiovasc. Diabetol. 19:36
     [Google Scholar]
  86. 86.
    Liu W, Carlisle CR, Sparks EA, Guthold M. 2010. The mechanical properties of single fibrin fibers. J. Thromb. Haemost. 8:1030–36
     [Google Scholar]
  87. 87.
    Lominadze D, Schuschke DA, Joshua IG, Dean WL 2002. Increased ability of erythrocytes to aggregate in spontaneously hypertensive rats. Clin. Exp. Hypertens. 24:397–406
     [Google Scholar]
  88. 88.
    Longstaff C, Varju I, Sotonyi P, Szabo L, Krumrey M et al. 2013. Mechanical stability and fibrinolytic resistance of clots containing fibrin, DNA, and histones. J. Biol. Chem. 288:6946–56
     [Google Scholar]
  89. 89.
    Lord ST. 2007. Fibrinogen and fibrin: scaffold proteins in hemostasis. Curr. Opin. Hematol. 14:236–41
     [Google Scholar]
  90. 90.
    MacDonald S, Luddington R. 2010. Critical factors contributing to the thromboelastography trace. Semin. Thromb. Hemost. 36:712–22
     [Google Scholar]
  91. 91.
    Maeda N, Seike M, Kume S, Takaku T, Shiga T. 1987. Fibrinogen-induced erythrocyte aggregation: erythrocyte-binding site in the fibrinogen molecule. Biochim. Biophys. Acta 904:81–91
     [Google Scholar]
  92. 92.
    Mahendra JV, Kumar SD, Anuradha TS, Talikoti P, Nagaraj RS, Vishali V. 2015. Plasma fibrinogen in type 2 diabetic patients with metabolic syndrome and its relation with ischemic heart disease (IHD) and retinopathy. J. Clin. Diagn. Res. 9:BC18–21
     [Google Scholar]
  93. 93.
    Memtsas VP, Arachchillage DRJ, Gorog DA. 2021. Role, laboratory assessment and clinical relevance of fibrin, factor XIII and endogenous fibrinolysis in arterial and venous thrombosis. Int. J. Mol. Sci. 22:1472
     [Google Scholar]
  94. 94.
    Mohandas N, Gallagher PG. 2008. Red cell membrane: past, present, and future. Blood 112:3939–48
     [Google Scholar]
  95. 95.
    Moll S, Mackman N 2008. Venous thromboembolism: a need for more public awareness and research into mechanisms. Arterioscler. Thromb. Vasc. Biol. 28:367–69
     [Google Scholar]
  96. 96.
    Munster S, Jawerth LM, Fabry B, Weitz DA. 2013. Structure and mechanics of fibrin clots formed under mechanical perturbation. J. Thromb. Haemost. 11:557–60
     [Google Scholar]
  97. 97.
    Neeves KB, Illing DA, Diamond SL. 2010. Thrombin flux and wall shear rate regulate fibrin fiber deposition state during polymerization under flow. Biophys. J. 98:1344–52
     [Google Scholar]
  98. 98.
    Nelb GW, Gerth C, Ferry JD, Lorand L. 1976. Rheology of fibrin clots. Biophys. Chem. 5:377–87
     [Google Scholar]
  99. 99.
    Paraboschi EM, Duga S, Asselta R 2017. Fibrinogen as a pleiotropic protein causing human diseases: the mutational burden of Aα, Bβ, and γ chains. Int. J. Mol. Sci. 18:2711
     [Google Scholar]
  100. 100.
    Pathare SJ, Eng W, Lee S-JJ, Ramasubramanian AK. 2021. Fibrin prestress due to platelet aggregation and contraction increases clot stiffness. Biophys. Rep. 1:100022
     [Google Scholar]
  101. 101.
    Perisanidis C, Psyrri A, Cohen EE, Engelmann J, Heinze G et al. 2015. Prognostic role of pretreatment plasma fibrinogen in patients with solid tumors: a systematic review and meta-analysis. Cancer Treat. Rev. 41:960–70
     [Google Scholar]
  102. 102.
    Phillips DR, Charo IF, Parise LV, Fitzgerald LA. 1988. The platelet membrane glycoprotein IIb-IIIa complex. Blood 71:831–43
     [Google Scholar]
  103. 103.
    Pieters M, Wolberg AS. 2019. Fibrinogen and fibrin: an illustrated review. Res. Pract. Thromb. Haemost. 3:161–72
     [Google Scholar]
  104. 104.
    Pischel KD, Bluestein HG, Woods VL Jr 1988. Platelet glycoproteins Ia, Ic, and IIa are physicochemically indistinguishable from the very late activation antigens adhesion-related proteins of lymphocytes and other cell types. J. Clin. Investig. 81:505–13
     [Google Scholar]
  105. 105.
    Plow EF, Haas TA, Zhang L, Loftus J, Smith JW. 2000. Ligand binding to integrins. J. Biol. Chem. 275:21785–88
     [Google Scholar]
  106. 106.
    Pretorius E, Steyn H, Engelbrecht M, Swanepoel AC, Oberholzer HM. 2011. Differences in fibrin fiber diameters in healthy individuals and thromboembolic ischemic stroke patients. Blood Coagul. Fibrinolys. 22:696–700
     [Google Scholar]
  107. 107.
    Pujadas-Mestres L, Lopez-Vilchez I, Arellano-Rodrigo E, Reverter JC, Lopez-Farre A et al. 2017. Differential inhibitory action of apixaban on platelet and fibrin components of forming thrombi: studies with circulating blood and in a platelet-based model of thrombin generation. PLOS ONE 12:e0171486
     [Google Scholar]
  108. 108.
    Rajangam T, An SS. 2013. Fibrinogen and fibrin based micro and nano scaffolds incorporated with drugs, proteins, cells and genes for therapeutic biomedical applications. Int. J. Nanomed. 8:3641–62
     [Google Scholar]
  109. 109.
    Rampling MW. 1981. The binding of fibrinogen and fibrinogen degradation products to the erythrocyte membrane and its relationship to haemorheology. Acta Biol. Med. Ger. 40:373–78
     [Google Scholar]
  110. 110.
    Ranucci M, Di Dedda U, Baryshnikova E. 2020. Trials and tribulations of viscoelastic-based determination of fibrinogen concentration. Anesthes. Analges. 130:644–53
     [Google Scholar]
  111. 111.
    Raphael J, Mazer CD, Subramani S, Schroeder A, Abdalla M et al. 2019. Society of Cardiovascular Anesthesiologists clinical practice improvement advisory for management of perioperative bleeding and hemostasis in cardiac surgery patients. J. Cardiothorac. Vasc. Anesth. 33:2887–99
     [Google Scholar]
  112. 112.
    Ricci D, Braga PC. 2004. Imaging methods in atomic force microscopy. Methods Mol. Biol. 242:13–23
     [Google Scholar]
  113. 113.
    Roberts WW, Kramer O, Rosser RW, Nestler FHM, Ferry JD. 1974. Rheology of fibrin clots. I. Biophys. Chem. 1:152–60
     [Google Scholar]
  114. 114.
    Rooth E, Wallen NH, Blomback M, He S. 2011. Decreased fibrin network permeability and impaired fibrinolysis in the acute and convalescent phase of ischemic stroke. Thromb. Res. 127:51–56
     [Google Scholar]
  115. 115.
    Ryan EA, Mockros LF, Weisel JW, Lorand L. 1999. Structural origins of fibrin clot rheology. Biophys. J. 77:2813–26
     [Google Scholar]
  116. 116.
    Sabeti S, Exner M, Mlekusch W, Amighi J, Quehenberger P et al. 2005. Prognostic impact of fibrinogen in carotid atherosclerosis: nonspecific indicator of inflammation or independent predictor of disease progression?. Stroke 36:1400–4
     [Google Scholar]
  117. 117.
    Sahli SD, Rössler J, Tscholl DW, Studt J-D, Spahn DR, Kaserer A. 2020. Point-of-care diagnostics in coagulation management. Sensors 20:4254
     [Google Scholar]
  118. 118.
    Sahni A, Odrljin T, Francis CW. 1998. Binding of basic fibroblast growth factor to fibrinogen and fibrin. J. Biol. Chem. 273:7554–59
     [Google Scholar]
  119. 119.
    Said AS, Doctor A. 2017. Influence of red blood cell-derived microparticles upon vasoregulation. Blood Transfus. 15:522–34
     [Google Scholar]
  120. 120.
    Sarker H, Hardy E, Haimour A, Maksymowych WP, Botto LD, Fernandez-Patron C. 2019. Identification of fibrinogen as a natural inhibitor of MMP-2. Sci. Rep. 9:4340
     [Google Scholar]
  121. 121.
    Sato M, Ohshima N. 1990. Effect of wall shear rate on thrombogenesis in microvessels of the rat mesentery. Circ. Res. 66:941–49
     [Google Scholar]
  122. 122.
    Sauls DL, Wolberg AS, Hoffman M. 2003. Elevated plasma homocysteine leads to alterations in fibrin clot structure and stability: implications for the mechanism of thrombosis in hyperhomocysteinemia. J. Thromb. Haemost. 1:300–6
     [Google Scholar]
  123. 123.
    Schuett K, Savvaidis A, Maxeiner S, Lysaja K, Jankowski V et al. 2017. Clot structure: a potent mortality risk factor in patients on hemodialysis. J. Am. Soc. Nephrol. 28:1622–30
     [Google Scholar]
  124. 124.
    Simpson-Haidaris PJ, Rybarczyk B. 2001. Tumors and fibrinogen: the role of fibrinogen as an extracellular matrix protein. Ann. N. Y. Acad. Sci. 936:406–25
     [Google Scholar]
  125. 125.
    Smith EB. 1994. Lipids and plasma fibrinogen: early and late composition of the atherosclerotic plaque. Cardiologia 39:169–72
     [Google Scholar]
  126. 126.
    Standeven KF, Carter AM, Grant PJ, Weisel JW, Chernysh I et al. 2007. Functional analysis of fibrin γ-chain cross-linking by activated factor XIII: determination of a cross-linking pattern that maximizes clot stiffness. Blood 110:902–7
     [Google Scholar]
  127. 127.
    Stein-Merlob AF, Kessinger CW, Erdem SS, Zelada H, Hilderbrand SA et al. 2015. Blood accessibility to fibrin in venous thrombosis is thrombus age-dependent and predicts fibrinolytic efficacy: an in vivo fibrin molecular imaging study. Theranostics 5:1317–27
     [Google Scholar]
  128. 128.
    Swieringa F, Baaten CC, Verdoold R, Mastenbroek TG, Rijnveld N et al. 2016. Platelet control of fibrin distribution and microelasticity in thrombus formation under flow. Arterioscler. Thromb. Vasc. Biol. 36:692–99
     [Google Scholar]
  129. 129.
    Swieringa F, Spronk HMH, Heemskerk JWM, van der Meijden PEJ. 2018. Integrating platelet and coagulation activation in fibrin clot formation. Res. Pract. Thromb. Haemost. 2:450–60
     [Google Scholar]
  130. 130.
    Swystun LL, Liaw PC. 2016. The role of leukocytes in thrombosis. Blood 128:753–62
     [Google Scholar]
  131. 131.
    Task Force Patient Blood Manag. Adult Card. Surg. Eur. Assoc. Cardio-Thorac. Surg. (EACTS), Eur. Assoc. Cardiothorac. Anesthesiol. (EACTA) Boer C, Meesters MI, Milojevic M et al. 2018. 2017 EACTS/EACTA guidelines on patient blood management for adult cardiac surgery. J. Cardiothorac. Vasc. Anesth 32:88–120
     [Google Scholar]
  132. 132.
    Ting LH, Feghhi S, Taparia N, Smith AO, Karchin A et al. 2019. Contractile forces in platelet aggregates under microfluidic shear gradients reflect platelet inhibition and bleeding risk. Nat. Commun. 10:1204
     [Google Scholar]
  133. 133.
    Tombak A. 2017. Red blood cells and relation to thrombosis, transfusion medicine and scientific developments. Transfusion Medicine and Scientific Developments AWMM Koopman-van Gemert. N.p.: IntechOpen. https://doi.org/10.5772/intechopen.69551
    [Crossref] [Google Scholar]
  134. 134.
    Tutwiler V, Singh J, Litvinov RI, Bassani JL, Purohit PK, Weisel JW. 2020. Rupture of blood clots: mechanics and pathophysiology. Sci. Adv. 6:eabc0496
     [Google Scholar]
  135. 135.
    Undas A, Ariëns RA. 2011. Fibrin clot structure and function: a role in the pathophysiology of arterial and venous thromboembolic diseases. Arterioscler. Thromb. Vasc. Biol. 31:e88–99
     [Google Scholar]
  136. 136.
    Undas A, Podolec P, Zawilska K, Pieculewicz M, Jedlinski I et al. 2009. Altered fibrin clot structure/function in patients with cryptogenic ischemic stroke. Stroke 40:1499–501
     [Google Scholar]
  137. 137.
    Undas A, Slowik A, Wolkow P, Szczudlik A, Tracz W. 2010. Fibrin clot properties in acute ischemic stroke: relation to neurological deficit. Thromb. Res. 125:357–61
     [Google Scholar]
  138. 138.
    Undas A, Szuldrzynski K, Stepien E, Zalewski J, Godlewski J et al. 2008. Reduced clot permeability and susceptibility to lysis in patients with acute coronary syndrome: effects of inflammation and oxidative stress. Atherosclerosis 196:551–57
     [Google Scholar]
  139. 139.
    van Dijk AC, Donkel SJ, Zadi T, Sonneveld MAH, Schreuder F et al. 2019. Association between fibrinogen and fibrinogen γ′ and atherosclerotic plaque morphology and composition in symptomatic carotid artery stenosis: Plaque-At-RISK study. Thromb. Res. 177:130–35
     [Google Scholar]
  140. 140.
    Varjú I, Sótonyi P, Machovich R, Szabó L, Tenekedjiev K et al. 2011. Hindered dissolution of fibrin formed under mechanical stress. J. Thromb. Haemost. 9:979–86
     [Google Scholar]
  141. 141.
    Vilar R, Fish RJ, Casini A, Neerman-Arbez M. 2020. Fibrin(ogen) in human disease: both friend and foe. Haematologica 105:284–96
     [Google Scholar]
  142. 142.
    von Bruhl ML, Stark K, Steinhart A, Chandraratne S, Konrad I et al. 2012. Monocytes, neutrophils, and platelets cooperate to initiate and propagate venous thrombosis in mice in vivo. J. Exp. Med. 209:819–35
     [Google Scholar]
  143. 143.
    Vos BE, Liebrand LC, Vahabi M, Biebricher A, Wuite GJL et al. 2017. Programming the mechanics of cohesive fiber networks by compression. Soft Matter 13:8886–93
     [Google Scholar]
  144. 144.
    Vos BE, Martinez-Torres C, Burla F, Weisel JW, Koenderink GH. 2020. Revealing the molecular origins of fibrin's elastomeric properties by in situ X-ray scattering. Acta Biomater. 104:39–52
     [Google Scholar]
  145. 145.
    Wagner CL, Mascelli MA, Neblock DS, Weisman HF, Coller BS, Jordan RE. 1996. Analysis of GPIIb/IIIa receptor number by quantification of 7E3 binding to human platelets. Blood 88:907–14
     [Google Scholar]
  146. 146.
    Wang W, Diacovo TG, Chen J, Freund JB, King MR 2013. Simulation of platelet, thrombus and erythrocyte hydrodynamic interactions in a 3D arteriole with in vivo comparison. PLOS ONE 8:e76949
     [Google Scholar]
  147. 147.
    Wang Y, Kumar S, Nisar A, Bonn M, Rausch MK, Parekh SH. 2021. Probing fibrin's molecular response to shear and tensile deformation with coherent Raman microscopy. Acta Biomater. 121:383–92
     [Google Scholar]
  148. 148.
    Weisel JW, Litvinov RI. 2013. Mechanisms of fibrin polymerization and clinical implications. Blood 121:1712–19
     [Google Scholar]
  149. 149.
    Weisel JW, Litvinov RI. 2019. Red blood cells: the forgotten player in hemostasis and thrombosis. J. Thromb. Haemost. 17:271–82
     [Google Scholar]
  150. 150.
    Whelihan MF, Mann KG. 2013. The role of the red cell membrane in thrombin generation. Thromb. Res. 131:377–82
     [Google Scholar]
  151. 151.
    Whiting D, DiNardo JA. 2014. TEG and ROTEM: technology and clinical applications. Am. J. Hematol. 89:228–32
     [Google Scholar]
  152. 152.
    Young G, Yonekawa KE, Nakagawa PA, Blain RC, Lovejoy AE, Nugent DJ. 2007. Differential effects of direct thrombin inhibitors and antithrombin-dependent anticoagulants on the dynamics of clot formation. Blood Coagul. Fibrinol. 18:97–103
     [Google Scholar]
  153. 153.
    Zhmurov A, Brown AEX, Litvinov RI, Dima RI, Weisel JW, Barsegov V. 2011. Mechanism of fibrin(ogen) forced unfolding. Structure 19:1615–24
     [Google Scholar]
  154. 154.
    Zhmurov A, Kononova O, Litvinov RI, Dima RI, Barsegov V, Weisel JW. 2012. Mechanical transition from α-helical coiled coils to β-sheets in fibrin(ogen). J. Am. Chem. Soc. 134:20396–402
     [Google Scholar]
/content/journals/10.1146/annurev-biophys-111821-072110
Loading
Nanomechanics of Blood Clot and Thrombus Formation
Annual Review of Biophysics 51, 201 (2022); https://doi.org/10.1146/annurev-biophys-111821-072110
/content/journals/10.1146/annurev-biophys-111821-072110
/content/journals/10.1146/annurev-biophys-111821-072110
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error