Role of fibrinogen in cerebrovascular dysfunction after traumatic brain injury

Brain Injury

Volumn 27, Issue 13-14, 2013, Pages 1508-1515

  Muradashvili, Nino ^a   Lominadze, David ^a  

^a University of Louisville School of Medicine   (United States)

Author keywords

Blood brain barrier; Cerebrovascular permeability; Inflammation; Matrix metalloproteinase 9; Paracellular transport; Transcellular transport

Indexed keywords

ANCROD; FIBRINOGEN; GELATINASE B; PLASMA PROTEIN;

AMNESIA; BLOOD BRAIN BARRIER; BLOOD CLOTTING DISORDER; BLOOD COMPONENT; BLOOD FLOW; BLOOD VESSEL PERMEABILITY; BLOOD VESSEL WALL; BRAIN CIRCULATION; BRAIN ISCHEMIA; CELL TRANSPORT; CEREBROVASCULAR DISEASE; HUMAN; INFLAMMATION; MICROVASCULATURE; NONHUMAN; PROTEIN BLOOD LEVEL; PROTEIN FUNCTION; REVIEW; TRAUMATIC BRAIN INJURY; VASCULAR DISEASE; VASCULAR ENDOTHELIUM;

BIOLOGICAL MARKERS; BLOOD-BRAIN BARRIER; BRAIN INJURIES; CEREBROVASCULAR CIRCULATION; ENDOTHELIUM, VASCULAR; FEMALE; FIBRINOGEN; HUMANS; INFLAMMATION; MALE; MEMORY DISORDERS; MICROCIRCULATION;

EID: 84888870085     PISSN: 02699052     EISSN: 1362301X     Source Type: Journal    
DOI: 10.3109/02699052.2013.823562     Document Type: Review

References (135)

1. Maas A, Roozenbeek B, Manley G. Clinical trials in traumatic brain injury: Past experience and current developments. Neurotherapeutics 2010;7:115-126.
2. Shlosberg D, Benifla M, Kaufer D, Friedman A. Blood-brain barrier breakdown as a therapeutic target in traumatic brain injury. Nature Reviews Neurology 2010;6:393-403.
3. Hawkins BT, Davis TP. The Blood-Brain Barrier/Neurovascular Unit in health and disease. Pharmacological Reviews 2005;57: 173-185.
4. Zlokovic BV, Griffin JH. Cytoprotective protein C pathways and implications for stroke and neurological disorders. Trends in Neurosciences 2011;34:198-209.
5. Degos V, Lescot T, Icke C, Le Manach Y, Fero K, Sanchez P, Hadiji B, Zouaoui A, Boch A-L, Abdennour L, et al. Computed tomography-estimated specific gravity at hospital admission predicts 6-month outcome in mild-to-moderate traumatic brain injury patients admitted to the Intensive Care Unit. Anesthesia & Analgesia 2012;114:1026-1033.
6. Andriessen TMJC, Jacobs B, Vos PE. Clinical characteristics and pathophysiological mechanisms of focal and diffuse traumatic brain injury. Journal of Cellular and Molecular Medicine 2010;14: 2381-2392.
7. Unterberg AW, Stover J, Kress B, Kiening KL. Edema and brain trauma. Neuroscience 2004;129:1019-1027.
8. Huber JD, Egleton RD, Davis TP. Molecular physiology and pathophysiology of tight junctions in the blood-brain barrier. Trends in Neurosciences 2001;24:719-725.
9. Muradashvili N, Qipshidze N, Munjal C, Givvimani S, Benton RL, Roberts AM, Tyagi SC, Lominadze D. Fibrinogen-induced increased pial venular permeability in mice. Journal of Cerebral Blood Flow and Metabolism 2012;32:150-163.
10. Lominadze D, Tsakadze N, Sen U, Falcone JC, D'Souza SE. Fibrinogen-and fragment D-induced vascular constriction. American Journal of Physiology 2005;288:H1257-H1264.
11. Sen U, Tyagi N, Patibandla PK, Dean WL, Tyagi SC, Roberts AM, Lominadze D. Fibrinogen-induced endothelin-1 production from endothelial cells. AJP-Cell Physiology 2009;296: C840-C847.
12. Tyagi N, Roberts AM, Dean WL, Tyagi SC, Lominadze D. Fibrinogen induces endothelial cell permeability. Molecular & Cellular Biochemistry 2008;307:13-22.
13. Patibandla PK, Tyagi N, Dean WL, Tyagi SC, Roberts AM, Lominadze D. Fibrinogen induces alterations of endothelial cell tight junction proteins. Journal of Cellular Physiology 2009;221: 195-203.
14. Muradashvili N, Tyagi N, Tyagi R, Munjal C, Lominadze D. Fibrinogen alters mouse brain endothelial cell layer integrity affecting vascular endothelial cadherin. Biochemical and Biophysical Research Communications 2011;413:509-514.
15. Koenig W. Fibrin(ogen) in cardiovascular disease: An update. Thrombosis and Haemostasis 2003;89:601-609.
16. Patibandla PK, Tyagi N, Tyagi SC, Dean WL, Roberts AM, Lominadze D. An elevated fibrinogen increases matrix metalloproteinases activity in cardiac microvascular endothelial cells. The FASEB Journal 2009;23:592.10.
17. Davalos D, Akassoglou K. Fibrinogen as a key regulator of inflammation in disease. Seminars In Immunopathology 2012;34:43-62.
18. de Almeida V, Silva-Herdade A, Calado A, Rosário H, Saldanha C. Fibrinogen modulates leukocyte recruitment in vivo during the acute inflammatory response. Clinical Hemorheology and Microcirculation 2012; [Epub ahead of print].
19. Komarova Y, Malik AB. Regulation of endothelial permeability via paracellular and transcellular transport pathways. Annual Review of Physiology 2010;72:463-493.
20. Nieswandt B, Kleinschnitz C, Stoll G. Ischaemic stroke: A thrombo-inflammatory disease? The Journal of Physiology 2011; 589:4115-4123.
21. Gonzales C, Pedrazzini T. Progenitor cell therapy for heart disease. Experimental Cell Research 2009;315:3077-3085.
22. Savoia C, Schiffrin EL. Inflammation in hypertension. Current Opinion in Nephrology and Hypertension 2006;15:152-158.
23. Wang TJ, Gona P, Larson MG, Levy D, Benjamin EJ, Tofler GH, Jacques PF, Meigs JB, Rifai N, Selhub J, et al. Multiple biomarkers and the risk of incident hypertension. Hypertension 2007;49: 432-438.
24. Donath MY, Shoelson SE. Type 2 diabetes as an inflammatory disease. Nature Reviews Immunology 2011;11:98-107.
25. Pietropaolo M, Barinas-Mitchell E, Kuller LH. The heterogeneity of diabetes. Diabetes 2007;56:1189-1197.
26. Ross R. Atherosclerosis-an inflammatory disease. New England Journal of Medicine 1999;340:115-126.
27. Cederberg D, Siesjö P. What has inflammation to do with traumatic brain injury? Child's Nervous System 2010;26:221-226.
28. Ziebell J, Morganti-Kossmann M. Involvement of pro-and antiinflammatory cytokines and chemokines in the pathophysiology of traumatic brain injury. Neurotherapeutics 2010;7:22-30.
29. Abou-Raya A, Abou-Raya S. Inflammation: A pivotal link between autoimmune diseases and atherosclerosis. Autoimmunity Reviews 2006;5:331-337.
30. Galli SJ, Tsai M, Piliponsky AM. The development of allergic inflammation. Nature 2008;454:445-454.
31. Broderick L, Tourangeau LM, Kavanaugh A, Wasserman SI. Biologic modulators in allergic and autoinflammatory diseases. Current Opinion in Allergy & Clinical Immunology 2011;11: 355-360.
32. Savoia C, Sada L, Zezza L, Pucci L, Lauri FM, Befani A, Alonzo A, Volpe M. Vascular inflammation and endothelial dysfunction in experimental hypertension. International Journal of Hypertension 2011;2011:281240-281247.
33. Curry F-RE, Noll T. Spotlight on microvascular permeability. Cardiovascular Research 2010;87:195-197.
34. Mehta D, Malik AB. Signaling mechanisms regulating endothelial permeability. Physiological Reviews 2006;86:279-367.
35. Lominadze D, Dean WL, Tyagi SC, Roberts AM. Mechanisms of fibrinogen-induced microvascular dysfunction during cardiovascular disease. Acta Physiologica 2010;198:1-13.
36. Michel CC, Curry FE. Microvascular permeability. Physiological Reviews 1999;79:703-761.
37. Laroche M, Kutcher ME, Huang MC, Cohen MJ, Manley GT. Coagulopathy after traumatic brain injury. Neurosurgery 2012;70: 1334-1345.
38. Davenport R. Pathogenesis of acute traumatic coagulopathy. Transfusion 2013;53:23S-27S.
39. Maegele M. Coagulopathy after traumatic brain injury: Incidence, pathogenesis, and treatment options. Transfusion 2013;53: 28S-37S.
40. Brohi K, Cohen MJ, Ganter MT, Schultz MJ, Levi M, Mackersie RC, Pittet J-F. Acute coagulopathy of trauma: Hypoperfusion induces systemic anticoagulation and hyperfibrinolysis. The Journal of Trauma and Acute Care Surgery 2008;64:1211-1217; discussion 1217.
41. Hoyt DB. A clinical review of bleeding dilemmas in trauma. Seminars in Hematology 2004;41:40-43.
42. Gomez PA, Lobato RD, Ortega JM, Cruz JDL. Mild head injury: Differences in prognosis among patients with a Glasgow Coma Scale score of 13 to 15 and analysis of factors associated with abnormal CT findings. British Journal of Neurosurgery 1996;10: 453-460.
43. Danesh J, Lewington S, Thompson SG, Lowe GD, Collins R, Kostis JB, Wilson AC, Folsom AR, Wu K, Benderly M, et al. Plasma fibrinogen level and the risk of major cardiovascular diseases and nonvascular mortality: An individual participant meta-analysis. Journal of the American Medical Association 2005;294: 1799-1809.
44. Chhabra G, Rangarajan K, Subramanian A, Agrawal D, Sharma S, Mukhopadhayay AK. Hypofibrinogenemia in isolated traumatic brain injury in Indian patients. Neurology India 2010;58:756-757.
45. Pahatouridis D, Alexiou G, Zigouris A, Mihos E, Drosos D, Voulgaris S. Coagulopathy in moderate head injury. The role of early administration of low molecular weight heparin. Brain Injury 2010;24:1189-1192.
46. Sun Y, Wang J, Wu X, Xi C, Gai Y, Liu H, Yuan Q, Wang E, Gao L, Hu J, et al. Validating the incidence of coagulopathy and disseminated intravascular coagulation in patients with traumatic brain injury-analysis of 242 cases. British Journal of Neurosurgery 2011;25:363-368.
47. Ernst E, Resch KL. Fibrinogen as a cardiovascular risk factor: A meta-analysis and review of the literature. Annals of Internal Medicine 1993;118:956-963.
48. Woodroofe M, Sarna G, Wadhwa M, Hayes G, Loughlin A, Tinker A, Cuzner M. Detection of interleukin-1 and interleukin-6 in adult rat brain, following mechanical injury, by in vivo microdialysis: Evidence of a role for microglia in cytokine production. Journal of Neuroimmunology 1991;33:227-236.
49. Humphries SE. Genetic regulation of fibrinogen. European Heart Journal 1995;16:16-20.
50. Vasse M, Paysant J, Soria J, Collet JP, Vannier JP, Soria C. Regulation of fibrinogen biosynthesis by cytokines, consequences on the vascular risk. Haemostasis 1996;26:331-339.
51. Ross R. Mechanisms of disease-Atherosclerosis-An inflammatory disease. New England Journal of Medicine 1999;340:115-126.
52. Kerlin B, Cooley BC, Isermann BH, Hernandez I, Sood R, Zogg M, Hendrickson SB, Mosesson MW, Lord S, Weiler H. Cause-effect relation between hyperfibrinogenemia and vascular disease. Current Opinion in Hematology 2004;103:1728-1734.
53. D'Erasmo E, Acca M, Celi FS, Medici F, Palmerini T, Pisani D. Plasma fibrinogen and platelet count in stroke. Journal of Medicine 1993;24:185-191.
54. del Zoppo GJ, Levy DE, Wasiewski WW, Pancioli AM, Demchuk AM, Trammel J, Demaerschalk BM, Kaste M, Albers GW, Ringelstein EB. Hyperfibrinogenemia and functional outcome from acute ischemic stroke. Stroke 2009;40:1687-1691.
55. Letcher RL, Chien S, Pickering TG, Sealey JE, Laragh JH. Direct relationship between blood pressure and blood viscosity in normal and hypertensive subjects. Role of fibrinogen and concentration. The American Journal of Medicine 1981;70:1195-1202.
56. Lominadze D, Joshua IG, Schuschke DA. Increased erythrocyte aggregation in spontaneously hypertensive rats. American Journal of Hypertension 1998;11:784-789.
57. Cherian L, Robertson C, Contant CJ, Bryan RJ. Lateral cortical impact injury in rats: Cerebrovascular effects of varying depth of cortical deformation and impact velocity. Journal of Neurotrauma 1994;11:573-585.
58. Giri BK, Krishnappa IK, Bryan RM, Robertson C. Regional cerebral blood flow after cortical impact injury complicated by a secondary insult in rats. Stroke 2000;31:961-967.
59. Golding EM, Robertson CS, Fitch JCK, Goodman JC, Bryan Jr RM. Segmentalvascular resistance after mild controlled cortical impact injury in the rat. Journal of Cerebral Blood Flow ad Metabolism 2003;23:210-218.
60. Wei E, Hamm R, Baranova A, Povlishock J. The long-term microvascular and behavioral consequences of experimental traumatic brain injury after hypothermic intervention. Journal of Neurotrauma 2009;26:527-537.
61. Muradashvili N, Khundmiri S, Benton R, Lominadze D. Increased formation of functional caveolae due to increased content of fibrinogen. In Experimental Biology 2012; April 21-25; San Diego, CA. FASEB Journal 2012;26:8623.
62. Muradashvili N, Tyagi R, Lominadze D. A dual-tracer method for differentiating transendothelial transport from paracellular leakage in vivo and in vitro. Frontiers in Physiology 2012;3:166-172.
63. Sahni A, Arévalo MT, Sahni SK, Simpson-Haidaris PJ. The VE-cadherin binding domain of fibrinogen induces endothelial barrier permeability and enhances transendothelial migration of malignant breast epithelial cells. International Journal of Cancer 2009;125:577-584.
64. Rybarczyk BJ, Lawrence SO, Simpson-Haidaris PJ. Matrixfibrinogen enhances wound closure by increasing both cell proliferation and migration. Blood 2003;102:4035-4043.
65. Bazzoni G. Endothelial tight junctions: Permeable barriers of the vessel wall. Thrombosis & Haemostasis 2006;95:36-42.
66. Simionescu M, Popov D, Sima A. Endothelial transcytosis in health and disease. Cell and Tissue Research 2009;335:27-40.
67. Clark TM, Hayes TK, Beyenbach KW. Dose-dependent effects of CRF-like diuretic peptide on transcellular and paracellular transport pathways. American Journal of Physiology Renal Physiology 1998; 274:F834-F840.
68. Lowe GDO, Lee AJ, Rumley A, Price JF, Fowkes FGR. Blood viscosity and risk of cardiovascular events: The Edinburgh Artery Study. British Journal of Haematology 1997;96:168-173.
69. Davies PF, Zilberberg J, Helmke BP. Spatial microstimuli in endothelial mechanosignaling. Circulation Research 2003;92:359-370.
70. Chien S, Usami S, Taylor HM, Lundberg JL, Gregersen MI. Effects of hematocrit and plasma proteins on human blood rheology at low shear rates. Journal of Applied Physiology 1966;21:81-87.
71. Shyy J-J, Chien S. Role of integrins in endothelial mechanosensing of shear stress. Circulation Research 2002;91:769-775.
72. Languino LR, Plescia J, Duperrray A, Brian AA, Plow EF, Geltosky JE, Alteri DC. Fibrinogen mediates leukocyte adhesion to vascular endothelium through an ICAM-1-dependent pathway. Cell 1993;73:1423-1434.
73. Springer TA. Adhesion receptors of the immune system. Nature 1990;346:425-434.
74. Plow EF, Haas TA, Zhang L, Loftus J, Smith JW. Ligand binding to integrins. The Journal of Biological Chemistry 2000;275: 21785-21788.
75. Luscinskas FW, Lawler J. Integrins as dynamic regulators of vascular function. The FASEB Journal 1994;8:929-938.
76. Altieri DC, Duperray A, Plescia J, Thornton GB, Languino LR. Structural recognition of a novel fibrinogen gamma chain sequence (117-133) by intercellular adhesion molecule-1 mediates leukocyteendothelium interaction. Journal of Biological Chemistry 1995; 270:696-699.
77. Suehiro K, Gailit J, Plow EF. Fibrinogen is a ligand for integrin alpha beta 5 beta1 on endothelial cells. The Journal of Biological Chemistry 1997;272:5360-5366.
78. Harley SL, Sturge J, Powell JT. Regulation by fibrinogen and its products of intercellular adhesion molecule-1 expression in human saphenous vein endothelial cells. Arteriosclerosis, Thrombosis, and Vascular Biology 2000;20:652-658.
79. Pluskota E, D'Souza SE. Fibrinogen interactions with ICAM-1 (CD54) regulate endothelial cell survival. European Journal of Biochemistry 2000;267:4693-4704.
80. Cohen ZVI, Bonvento G, Lacombe P, Hamel E. Serotonin in the regulation of brain microcirculation. Progress in Neurobiology 1996;50:335-362.
81. Frank PG, Woodman SE, Park DS, Lisanti MP. Caveolin, caveolae, and endothelial cell function. Arteriosclerosis, Thrombosis, and Vascular Biology 2003;23:1161-1168.
82. Dietzen DJ, Hastings WR, Lublin DM. Caveolin is palmitoylated on multiple cysteine residues. Journal of Biological Chemistry 1995;270:6838-6842.
83. Bazzoni G, Dejana E. Endothelial cell-to-cell junctions: Molecular organization and role in vascular homeostasis. Physiological Reviews 2004;84:869-901.
84. Aberle H, Schwartz H, Kemler R. Cadherin-catenin complex: Protein interactions and their implications for cadherin function. Journal of Cellular Biochemistry 1996;61:514-523.
85. Vandenbroucke E, Mehta D, Minshall R, Malik AB. Regulation of endothelial junctional permeability. Annals of the New York Academy of Sciences 2008;1123:134-145.
86. Vestweber D, Hahne M, Levinovitz A. The endothelial selectins: How are they regulated and what are their ligands? Progress in Applied Microcirculation 1995;21:1-6.
87. Ehringer WD, Yamany S, Steier K, Farag A, Roisen FJ, Dozier A, Miller FN. Quantitative image analysis of F-actin in endothelial cells. Microcirculation 1999;6:291-303.
88. Trepat X, Grabulosa M, Buscemi L, Rico F, Farre R, Navajas D. Thrombin and histamine induce stiffening of alveolar epithelial cells. Journal of Applied Physiology 2005; 98:1567-1574.
89. Vestweber D. VE-Cadherin: The major endothelial adhesion molecule controlling cellular junctions and blood vessel formation. Arteriosclerosis, Thrombosis and Vascular Biology 2008;28: 223-232.
90. Baldwin A, Thurston G. Mechanics of endothelial cell architecture and vascular permeability. Critical Reviews in Biomedical Engineering 2001;29:247-278.
91. Stan R-V, Marion K, Palade GE. PV-1 is a component of the fenestral and stomatal diaphragms in fenestrated endothelia. Proceedings of the National Academy of Sciences of the United States of America 1999;96:13203-13207.
92. Stan RV. Endothelial stomatal and fenestral diaphragms in normal vessels and angiogenesis. Journal of Cellular and Molecular Medicine 2007;11:621-643.
93. Tse D, Stan RV. Morphological heterogeneity of endothelium. Seminars in Thrombosis & Hemostasis 2010;36: 236-245.
94. Sörensson J, Fierlbeck W, Heider T, Schwarz K, Park DS, Mundel P, Lisanti M, Ballermann BJ. Glomerular endothelial fenestrae in vivo are not formed from caveolae. Journal of the American Society of Nephrology 2002;13:2639-2647.
95. Thorn H, Stenkula KG, Karlsson M, O rtegren U, Nystrom FH, Gustavsson J, Stralfors P. Cell surface orifices of caveolae and localization of caveolin to the necks of caveolae in adipocytes. Molecular Biology of the Cell 2003;14:3967-3976.
96. Cai T, Wang H, Chen Y, Liu L, Gunning WT, Quintas LEM, Xie Z-J. Regulation of caveolin-1 membrane trafficking by the Na/KATPase. The Journal of Cell Biology 2008;182:1153-1169.
97. Yu J, Bergaya S, Murata T, Alp IF, Bauer MP, Lin MI, Drab M, Kurzchalia TV, Stan RV, Sessa WC. Direct evidence for the role of caveolin-1 and caveolae in mechanotransduction and remodeling of blood vessels. Journal of Clinical Investigation 2006;116: 1284.
98. Matveev S, Li X, Everson W, Smart EJ. The role of caveolae and caveolin in vesicle-dependent and vesicle-independent trafficking. Advanced Drug Delivery Reviews 2001;49:237-250.
99. Hnasko R, McFarland M, Ben-Jonathan N. Distribution and characterization of plasmalemma vesicle protein-1 in rat endocrine glands. Journal of Endocrinology 2002;175:649-661.
100. Carson-Walter E, Hampton J, Shue E, Geynisman D, Pillai P, Sathanoori R, Madden S, Hamilton R, Walter K. Plasmalemmal vesicle associated protein-1 is a novel marker implicated in brain tumor angiogenesis. Clinical Cancer Research 2005;11: 7643-7650.
101. Stan RV. Structure of caveolae. Biochimica et Biophysica Acta (BBA)-Molecular Cell Research 2005;1746:334-348.
102. Hnasko R, Lisanti MP. The biology of caveolae: Lessons from caveolin knockout mice and implications for human disease. Molecular Interventions 2003;3:445-464.
103. Mozer A, Whittemore S, Benton R. Spinal microvascular expression of PV-1 is associated with inflammation, perivascular astrocyte loss, and diminished EC glucose transport potential in acute SCI. Current Neurovascular Research 2010;7:238-250.
104. Shue E, Carson-Walter E, Liu Y, Winans B, Ali Z, Chen J, Walter K. Plasmalemmal vesicle associated protein-1 (PV-1) is a marker of blood-brain barrier disruption in rodent models. BMC Neuroscience 2008;9:29.
105. Fernandez-Patron C, Zouki C, Whittal R, Chan JS, Davidge ST, Filep JG. Matrix metalloproteinases regulate neutrophilendothelial cell adhesion through generation of endothelin-1[1-32]. The FASEB Journal 2001;15:2230-2240.
106. Rosell A, Alvarez-Sabin J, Arenillas JF, Rovira A, Delgado P, Fernandez-Cadenas I, Penalba A, Molina CA, Montaner J. A matrix metalloproteinase protein array reveals a strong relation between MMP-9 and MMP-13 with diffusion-weighted image lesion increase in human stroke. Stroke 2005;36:1415-1420.
107. Rosell A, Ortega-Aznar A, Alvarez-Sabin J, Fernandez-Cadenas I, Ribo M, Molina CA, Lo EH, Montaner J. Increased brain expression of matrix metalloproteinase-9 after ischemic and hemorrhagic human stroke. Stroke 2006;37:1399-1406.
108. Chen F, Ohashi N, Li W, Eckman C, Nguyen JH. Disruptions of occludin and claudin-5 in brain endothelial cells in vitro and in brains of mice with acute liver failure. Hepatology 2009;50: 1914-1923.
109. Mori T, Wang X, Aoki T, Lo EH. Downregulation of matrix metalloproteinase-9 and attenuation of edema via inhibition of ERK mitogen activated protein kinase in traumatic brain injury. Journal of Neurotrauma 2002;19:1411-1419.
110. Wang X, Jung J, Asahi M, Chwang W, Russo L, Moskowitz MA, Dixon CE, Fini ME, Lo EH. Effects of matrix metalloproteinase-9 gene knock-out on morphological and motor outcomes after traumatic brain injury. The Journal of Neuroscience 2000;20: 7037-7042.
111. Cuzzocrea S, Deigner H-P, Genovese T, Mazzon E, Esposito E, Crisafulli C, Di Paola R, Bramanti P, Matuschak G, Salvemini D. Inhibition of ceramide biosynthesis ameliorates pathological consequences of spinal cord injury. Shock 2009;31:634-644.
112. Asahi M, Wang X, Mori T, Sumii T, Jung J-C, Moskowitz MA, Fini ME, Lo EH. Effects of matrix metalloproteinase-9 gene knock-out on the proteolysis of blood-brain barrier and white matter components after cerebral ischemia. The Journal of Neuroscience 2001;21:7724-7732.
113. Phillips PG, Birnby LM. Nitric oxide modulates caveolin-1 and matrix metalloproteinase-9 expression and distribution at the endothelial cell/tumor cell interface. American Journal of Physiology-Lung Cellular and Molecular Physiology 2004; 286:L1055-L1065.
114. Cernich A, Kurtz S, Mordecai K, Ryan P. Cognitive rehabilitation in traumatic brain injury. Current Treatment Options in Neurology 2010;12:412-423.
115. Ahn HJ, Zamolodchikov D, Cortes-Canteli M, Norris EH, Glickman JF, Strickland S. Alzheimer's disease peptide b-amyloid interacts with fibrinogen and induces its oligomerization. Proceedings of the National Academy of Sciences 2010;107: 21812-21817.
116. Cortes-Canteli M, Strickland S. Fibrinogen, a possible key player in Alzheimer's disease. Journal of Thrombosis and Haemostasis 2009;7:146-150.
117. Cortes-Canteli M, Paul J, Norris EH, Bronstein R, Ahn HJ, Zamolodchikov D, Bhuvanendran S, Fenz KM, Strickland S. Fibrinogen and b-Amyloid association alters thrombosis and fibrinolysis: A possible contributing factor to Alzheimer's Disease. Neuron 2010;66:695-709.
118. Hardy J, Selkoe DJ. The amyloid hypothesis of Alzheimer's disease: Progress and problems on the road to therapeutics. Science 2002;297:353.
119. Cleary JP, Walsh DM, Hofmeister JJ, Shankar GM, Kuskowski MA, Selkoe DJ, Ashe KH. Natural oligomers of the amyloid-[beta] protein specifically disrupt cognitive function. Nature Neuroscience 2005;8:79-84.
120. Zamolodchikov D, Strickland S. Ab delays fibrin clot lysis by altering fibrin structure and attenuating plasminogen binding to fibrin. Blood 2012;119:3342-3351.
121. Gimbel DA, Nygaard HB, Coffey EE, Gunther EC, Laurén J, Gimbel ZA, Strittmatter SM. Memory impairment in transgenic Alzheimer mice requires cellular prion protein. The Journal of Neuroscience 2010;30:6367-6374.
122. Chung E, Ji Y, Sun Y, Kascsak R, Kascsak R, Mehta P, Strittmatter S, Wisniewski T. Anti-PrPC monoclonal antibody infusion as a novel treatment for cognitive deficits in an Alzheimer's disease model mouse. BMC Neuroscience 2010;11:130-140.
123. Vidal B, Serrano AL, Tjwa M, Suelves M, Ardite E, De Mori R, Baeza-Raja B, Martinez de Lagran M, Lafuste P, Ruiz-Bonilla V, et al. Fibrinogen drives dystrophic muscle fibrosis via a TGFbeta/alternative macrophage activation pathway. Genes & Development 2008;22:1747-1752.
124. Tennent GA, Brennan SO, Stangou AJ, O'Grady J, Hawkins PN, Pepys MB. Human plasma fibrinogen is synthesized in the liver. Blood 2007;109:1971-1974.
125. Vasse M, Paysant J, Soria J, Mirshahi SS, Vannier JP, Soria C. Down-regulation of fibrinogen biosynthesis by IL-4, IL-10 and IL-13. British Journal of Haematology 1996;93:955-961.
126. Clausen F, Hanell A, Björk M, Hillered L, Mir AK, Gram H, Marklund N. Neutralization of interleukin-1b modifies the inflammatory response and improves histological and cognitive outcome following traumatic brain injury in mice. European Journal of Neuroscience 2009;30:385-396.
127. Wang D-S, Hanamoto M, Fang F, Ohba M, Ishii M, Kimura F, Higaki E, Senga H. Defibrinogenating effect of batroxobin (Defibrase-) in rats and inhibition of migration of human vascular smooth muscle cells by the plasma of batroxobin-treated rats in vitro. Atherosclerosis 2001;156:73-80.
128. Kockx M, Gervois PP, Poulain P, Derudas B, Peters JM, Gonzalez FJ, Princen HMG, Kooistra T, Staels B. Fibrates suppress fibrinogen gene expression in rodents via activation of the peroxisome proliferator-activated receptor-a. Blood 1999;93: 2991-2998.
129. Handagama PJ, Shuman MA, Bainton DF. In vivo defibrination results in markedly decreased amounts of fibrinogen in rat megakaryocytes and platelets. American Journal of Pathology 1990;137:1393-1399.
130. Johnson A, ahamont MV, Malik AB. Thrombin-induced lung vascular injury. Roles of fibrinogen and fibrinolysis. The American Review of Respiratory Disease 1983;128:38-44.
131. Paul J, Strickland S, Melchor JP. Fibrin deposition accelerates neurovascular damage and neuroinflammation in mouse models of Alzheimer's disease. The Journal of Experimental Medicine 2007; 204:1999-2008.
132. Bell W, Shapiro S, Martinez J, Nossel H. The effects of ancrod, the coagulating enzyme from the venom of Malayan pit viper (A. rhodostoma) on prothrombin and fibrinogen metabolism and fibrinopeptide A release in man. The Journal of Laboratory and Clinical Medicine 1978;91:592-604.
133. Levy DE, del Zoppo GJ, Demaerschalk BM, Demchuk AM, Diener H-C, Howard G, Kaste M, Pancioli AM, Ringelstein EB, Spatareanu C, Wasiewski WW. Ancrod in acute ischemic stroke: Results of 500 subjects beginning treatment within 6 hours of stroke onset in the ancrod stroke program. Stroke 2009;40: 3796-3803.
134. Hao Z, Liu M, Counsell C, Wardlaw J, Lin S, Zhao X. Fibrinogen depleting agents for acute ischaemic stroke. The Cochrane Database of Systematic Reviews (Online). Oxford, UK; Vista, CA: John Wiley & Sons, Ltd; 2012. p 46.
135. Pollak V, Glueck H, Weiss M, Lebron-Berges A, Miller M. Defibrination with ancrod in glomerulonephritis: Effects on clinical and histologic findings and on blood coagulation. American Journal of Nephrology 1982;2:195-207.