Ablation of matrix metalloproteinase-9 gene decreases cerebrovascular permeability and fibrinogen deposition post traumatic brain injury in mice

Metabolic Brain Disease

Volumn 30, Issue 2, 2015, Pages 411-426

  Muradashvili, Nino ^a   Benton, Richard L ^a   Saatman, Kathryn E ^b   Tyagi, Suresh C ^a   Lominadze, David ^a  

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

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Caveolae; Cellular prion protein (PrPC); Cerebrovascular permeability; Fibrinogen; Macromolecular leakage; Memory loss

Indexed keywords

FIBRINOGEN; GELATINASE B; INTERCELLULAR ADHESION MOLECULE 1; PRION PROTEIN;

ANIMAL; BIOSYNTHESIS; BLOOD BRAIN BARRIER; BRAIN CIRCULATION; BRAIN CORTEX; BRAIN INJURY; BRAIN VEIN; C57BL MOUSE; CAPILLARY; CONTUSION; GENETICS; INJURIES; KNOCKOUT MOUSE; MALE; MEMORY DISORDERS; METABOLISM; MOUSE; PATHOLOGY; PERMEABILITY; PSYCHOLOGY; SHORT TERM MEMORY;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN INJURIES; CAPILLARIES; CEREBRAL CORTEX; CEREBRAL VEINS; CEREBROVASCULAR CIRCULATION; CONTUSIONS; FIBRINOGEN; INTERCELLULAR ADHESION MOLECULE-1; MALE; MATRIX METALLOPROTEINASE 9; MEMORY DISORDERS; MEMORY, SHORT-TERM; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PERMEABILITY; PRPC PROTEINS;

EID: 84939874954     PISSN: 08857490     EISSN: 15737365     Source Type: Journal    
DOI: 10.1007/s11011-014-9550-3     Document Type: Article

References (73)

1. Adams RA, Bauer J, Flick MJ, Sikorski SL, Nuriel T, Lassmann H, Degen JL, Akassoglou K (2007) The fibrin-derived γ377-395 peptide inhibits microglia activation and suppresses relapsing paralysis in central nervous system autoimmune disease. J Exp Med 204(3):571–582. doi:10.1084/jem.20061931
2. Ahn HJ, Zamolodchikov D, Cortes-Canteli M, Norris EH, Glickman JF, Strickland S (2010) Alzheimer’s disease peptide β-amyloid interacts with fibrinogen and induces its oligomerization. Proc Natl Acad Sci 107(50):21812–21817. doi:10.1073/pnas.1010373107
3. Altieri DC, Duperray A, Plescia J, Thornton GB, Languino LR (1995) Structural recognition of a novel fibrinogen gamma chain sequence (117–133) by intercellular adhesion molecule-1 mediates leukocyte-endothelium interaction. J Biol Chem 270(2):696–699
4. Bevins RA, Besheer J (2006) Object recognition in rats and mice: a one-trial non-matching-to-sample learning task to study ‘recognition memory’. Nat Protocols 1 (3):1,306–1,311. doi:http://www.nature.com/nprot/journal/v1/n3/suppinfo/nprot.2006.205_S1.html
5. Carson-Walter E, Hampton J, Shue E, Geynisman D, Pillai P, Sathanoori R, Madden S, Hamilton R, Walter K (2005) Plasmalemmal vesicle associated protein-1 is a novel marker implicated in brain tumor angiogenesis. Clin Cancer Res 11(21):7643–7650
6. Cernich A, Kurtz S, Mordecai K, Ryan P (2010) Cognitive rehabilitation in traumatic brain injury. Curr Treat Options Neurol 12(5):412–423. doi:10.1007/s11940-010-0085-6
7. Chhabra G, Rangarajan K, Subramanian A, Agrawal D, Sharma S, Mukhopadhayay A (2010) Hypofibrinogenemia in isolated traumatic brain injury in Indian patients. Neurol India 58(5):756–757. doi:10.4103/0028-3886.72175
8. Choo AM, Miller WJ, Chen Y-C, Nibley P, Patel TP, Goletiani C, Morrison B, Kutzing MK, Firestein BL, Sul J-Y, Haydon PG, Meaney DF (2013) Antagonism of purinergic signalling improves recovery from traumatic brain injury. Brain. doi:10.1093/brain/aws286
9. Chung E, Ji Y, Sun Y, Kascsak R, Kascsak R, Mehta P, Strittmatter S, Wisniewski T (2010) Anti-PrPC monoclonal antibody infusion as a novel treatment for cognitive deficits in an Alzheimer’s disease model mouse. BMC Neurosci 11:130. doi:10.1186/1471-2202-11-130
10. Cohen ZVI, Bonvento G, Lacombe P, Hamel E (1996) Serotonin in the regulation of brain microcirculation. Prog Neurobiol 50(4):335–362. doi:10.1016/s0301-0082(96)00033-0
11. D’Erasmo E, Acca M, Celi FS, Medici F, Palmerini T, Pisani D (1993) Plasma fibrinogen and platelet count in stroke. J Med 24(2–3):185–191
12. Davalos D, Akassoglou K (2012) Fibrinogen as a key regulator of inflammation in disease. Semin Immunopathol 34(1):43–62
13. Davalos D, Kyu Ryu J, Merlini M, Baeten KM, Le Moan N, Petersen MA, Deerinck TJ, Smirnoff DS, Bedard C, Hakozaki H, Gonias Murray S, Ling JB, Lassmann H, Degen JL, Ellisman MH, Akassoglou K (2012) Fibrinogen-induced perivascular microglial clustering is required for the development of axonal damage in neuroinflammation. Nat Commun 3:1,227. doi:http://www.nature.com/ncomms/journal/v3/n11/suppinfo/ncomms2230_S1.html
14. del Zoppo GJ, Levy DE, Wasiewski WW, Pancioli AM, Demchuk AM, Trammel J, Demaerschalk BM, Kaste M, Albers GW, Ringelstein EB (2009) Hyperfibrinogenemia and functional outcome from acute ischemic stroke. Stroke 40(5):1687–1691. doi:10.1161/strokeaha.108.527804
15. Ernst E, Resch KL (1993) Fibrinogen as a cardiovascular risk factor: a meta-analysis and review of the literature. Ann Intern Med 118:956–963
16. Fernandez-Patron C, Zouki C, Whittal R, Chan JS, Davidge ST, Filep JG (2001) Matrix metalloproteinases regulate neutrophil-endothelial cell adhesion through generation of endothelin-1 [1–32]. FASEB J 15(12):2230–2240
17. Fischer MB, Roeckl C, Parizek P, Schwarz HP, Aguzzi A (2000) Binding of disease-associated prion protein to plasminogen. Nature 408(6811):479–483
18. Flick MJ, Du X, Witte DP, Jirouskova M, Soloviev DA, Busuttil SJ, Plow EF, Degen JL (2004) Leukocyte engagement of fibrin (ogen) via the integrin receptor αMβ2/Mac-1 is critical for host inflammatory response in vivo. J Clin Invest 113(11):1596–1606. doi:10.1172/JCI20741
19. Gimbel DA, Nygaard HB, Coffey EE, Gunther EC, Laurén J, Gimbel ZA, Strittmatter SM (2010) Memory impairment in transgenic Alzheimer mice requires cellular prion protein. J Neuroradiol 30(18):6367–6374. doi:10.1523/jneurosci.0395-10.2010
20. Granger D, Senchenkova E (2010) Inflammation and the Microcirculation. Colloquium Series on Integrated Systems Physiology: From Molecule to Function to Disease. Morgan & Claypool Life Sciences, San Rafael
21. Grossetete M, Phelps J, Arko L, Yonas H, Rosenberg G (2009) Elevation of matrix metalloproteinases 3 and 9 in cerebrospinal fluid and blood in patients with severe traumatic brain injury. Neurosurgery 65(4):702–708
22. Hadass O, Tomlinson BN, Gooyit M, Chen S, Purdy JJ, Walker JM, Zhang C, Giritharan AB, Purnell W, Robinson CR II, Shin D, Schroeder VA, Suckow MA, Simonyi AY, Sun G, Mobashery S, Cui J, Chang M, Gu Z (2013) Selective inhibition of matrix metalloproteinase-9 attenuates secondary damage resulting from severe traumatic brain injury. PLoS One 8(10):e76904. doi:10.1371/journal.pone.0076904
23. Hnasko R, McFarland M, Ben-Jonathan N (2002) Distribution and characterization of plasmalemma vesicle protein-1 in rat endocrine glands. J Endocrinol 175(3):649–661. doi:10.1677/joe.0.1750649
24. Hu G, Vogel SM, Schwartz DE, Malik AB, Minshall RD (2008) Intercellular Adhesion Molecule-1–Dependent Neutrophil Adhesion to Endothelial Cells Induces Caveolae-Mediated Pulmonary Vascular Hyperpermeability. Circ Res 102(12):e120–e131. doi:10.1161/circresaha.107.167486
25. Johnson VE, Stewart W, Smith DH (2010) Traumatic brain injury and amyloid-[beta] pathology: a link to Alzheimer’s disease? Nat Rev Neurosci 11(5):361–370
26. Kerlin B, Cooley BC, Isermann BH, Hernandez I, Sood R, Zogg M, Hendrickson SB, Mosesson MW, Lord S, Weiler H (2004) Cause-effect relation between hyperfibrinogenemia and vascular disease. Curr Opin Hematol 103(5):1728–1734
27. Lauren J, Gimbel DA, Nygaard HB, Gilbert JW, Strittmatter SM (2009) Cellular prion protein mediates impairment of synaptic plasticity by amyloid-[bgr] oligomers. Nature 457 (7233):1,128–1,132. doi:http://www.nature.com/nature/journal/v457/n7233/suppinfo/nature07761_S1.html
28. Letcher RL, Chien S, Pickering TG, Sealey JE, Laragh JH (1981) Direct relationship between blood pressure and blood viscosity in normal and hypertensive subjects. Role of fibrinogen and concentration. Am J Med 70:1195–1202
29. Lishko VK, Kudryk B, Yakubenko VP, Yee VC, Ugarova TP (2002) Regulated unmasking of the cryptic binding site foriIntegrin αMβ2 in the γC-domain of fibrinogen. Biochemistry 41(43):12942–12951. doi:10.1021/bi026324c
30. Lominadze D, Joshua IG, Schuschke DA (1998) Increased erythrocyte aggregation in spontaneously hypertensive rats. Am J Hypertens 11:784–789
31. Lominadze D, Tsakadze N, Sen U, Falcone JC, D’Souza SE (2005) Fibrinogen- and fragment D-induced vascular constriction. Am J Physiol 288(3):H1257–H1264
32. Lominadze D, Roberts AM, Tyagi N, Tyagi SC (2006) Homocysteine causes cerebrovascular leakage in mice. Am J Physiol Heart Circ Physiol 290(3):H1206–H1213
33. Lominadze D, Dean WL, Tyagi SC, Roberts AM (2010) Mechanisms of fibrinogen-induced microvascular dysfunction during cardiovascular disease. Acta Physiol 198(1):1–13
34. Lyon L, Saksida L, Bussey T (2012) Spontaneous object recognition and its relevance to schizophrenia: a review of findings from pharmacological, genetic, lesion and developmental rodent models. Psychopharmacology 220(4):647–672. doi:10.1007/s00213-011-2536-5
35. Mansoor O, Cayol M, Gachon P, Boirie Y, Schoeffler P, Obled C, Beaufrère B (1997) Albumin and fibrinogen syntheses increase while muscle protein synthesis decreases in head-injured patients. Am J Physiol Endocrinol Metab 273(5):E898–E902
36. Mehta D, Malik AB (2006) Signaling mechanisms regulating endothelial permeability. Physiol Rev 86(1):279–367
37. Minshall RD, Tiruppathi C, Vogel SM, Niles WD, Gilchrist A, Hamm HE, Malik AB (2000) Endothelial cell-surface gp60 activates vesicle formation and trafficking via G(i)-coupled Src kinase signaling pathway. J Cell Biol 150(5):1057–1070
38. Mori T, Wang X, Aoki T, Lo EH (2002) Downregulation of matrix metalloproteinase-9 and attenuation of edema via inhibition of ERK mitogen activated protein kinase in traumatic brain injury. J Neurotrauma 19(11):1411–1419. doi:10.1089/089771502320914642
39. Mozer A, Whittemore S, Benton R (2010) Spinal microvascular expression of PV-1 is associated with inflammation, perivascular astrocyte loss, and diminished EC glucose transport potential in acute SCI. Curr Neurovasc Res 7(3):238–250
40. Muradashvili N, Lominadz D (2013) Role of fibrinogen in cerebrovascular dysfunction after traumatic brain injury. Brain Inj 27(13–14):1508–1515. doi:10.3109/02699052.2013.823562
41. Muradashvili N, Tyagi N, Tyagi R, Munjal C, Lominadze D (2011) Fibrinogen alters mouse brain endothelial cell layer integrity affecting vascular endothelial cadherin. Biochem Biophys Res Commun 413(4):509–514. doi:10.1016/j.bbrc.2011.07.133
42. Muradashvili N, Qipshidze N, Munjal C, Givvimani S, Benton RL, Roberts AM, Tyagi SC, Lominadze D (2012a) Fibrinogen-induced increased pial venular permeability in mice. J Cereb Blood Flow Metab 32(1):150–163. doi:10.1038/jcbfm.2011.144
43. Muradashvili N, Tyagi R, Lominadze D (2012b) A dual-tracer method for differentiating transendothelial transport from paracellular leakage in vivo and in vitro. Front Physiol 3:166–172. doi:10.3389/fphys.2012.00166
44. Muradashvili N, Benton R, Tyagi S, Lominadz D (2013) Elevated level of fibrinogen increases caveolae formation; Role of matrix metalloproteinase-9. Cell Biochemistry and Biophysics: [Epub ahead of print]
45. Pahatouridis D, Alexiou G, Zigouris A, Mihos E, Drosos D, Voulgaris S (2010) Coagulopathy in moderate head injury. The role of early administration of low molecular weight heparin. Brain Inj 24(10):1189–1192
46. Parton RG, Joggerst B, Simons K (1994) Regulated internalization of caveolae. J Cell Biol 127(5):1199–1215. doi:10.1083/jcb.127.5.1199
47. Patibandla PK, Tyagi N, Dean WL, Tyagi SC, Roberts AM, Lominadze D (2009) Fibrinogen induces alterations of endothelial cell tight junction proteins. J Cell Physiol 221(1):195–203
48. Phillips PG, Birnby LM (2004) Nitric oxide modulates caveolin-1 and matrix metalloproteinase-9 expression and distribution at the endothelial cell/tumor cell interface. Am J Physiol Lung Cell Mol Physiol 286(5):L1055–L1065. doi:10.1152/ajplung.00262.2003
49. Pleasant J, Carlson S, Mao H, Scheff S, Yang K, Saatman K (2011) Rate of neurodegeneration in the mouse controlled cortical impact model is influenced by impactor tip shape: implications for mechanistic and therapeutic studies. Journal of Neurotrauma
50. Plow EF, Haas TA, Zhang L, Loftus J, Smith JW (2000) Ligand binding to integrins. J Biol Chem 275(29):21785–21788
51. Rosell A, Alvarez-Sabin J, Arenillas JF, Rovira A, Delgado P, Fernandez-Cadenas I, Penalba A, Molina CA, Montaner J (2005) 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 36(7):1415–1420
52. Rosell A, Ortega-Aznar A, Alvarez-Sabin J, Fernandez-Cadenas I, Ribo M, Molina CA, Lo EH, Montaner J (2006) Increased brain expression of matrix metalloproteinase-9 after ischemic and hemorrhagic human stroke. Stroke 37(6):1399–1406
53. Ross R (1999) Mechanisms of disease - Atherosclerosis - An inflammatory disease. N Engl J Med 340(2):115–126
54. Rybarczyk BJ, Lawrence SO, Simpson-Haidaris PJ (2003) Matrix-fibrinogen enhances wound closure by increasing both cell proliferation and migration. Blood 102(12):4035–4043. doi:10.1182/blood-2003-03-0822
55. Sahni A, Arévalo MT, Sahni SK, Simpson-Haidaris PJ (2009) The VE-cadherin binding domain of fibrinogen induces endothelial barrier permeability and enhances transendothelial migration of malignant breast epithelial cells. Int J Cancer 125(3):577–584
56. Sangiorgi S, De Benedictis A, Protasoni M, Manelli A, Reguzzoni M, Cividini A, Dell’Orbo C, Tomei G, Balbi S (2013) Early-stage microvascular alterations of a new model of controlled cortical traumatic brain injury: 3D morphological analysis using scanning electron microscopy and corrosion casting. J Neurosurg 118(4):763–774. doi:10.3171/2012.11.JNS12627
57. Schwarzmaier S, Kim S, Trabold R, Plesnila N (2010) Temporal profile of thrombogenesis in the cerebral microcirculation after traumatic brain injury in mice. J Neurotrauma 27(1):121–130
58. Sen U, Tyagi N, Patibandla PK, Dean WL, Tyagi SC, Roberts AM, Lominadze D (2009) Fibrinogen-induced endothelin-1 production from endothelial cells. AJP - Cell Physiol 296(4):C840–C847
59. Shigemori Y, Katayama Y, Mori T, Maeda T, Kawamata T (2006) Matrix metalloproteinase-9 is associated with blood–brain barrier opening and brain edema formation after cortical contusion in rats. In: Hoff JT, Keep RF, Xi G, Hua Y (eds) Brain Edema XIII, vol 96. Acta Neurochirurgica Supplement vol Supplement 96. Springer, Wien, pp 130–133
60. Shlosberg D, Benifla M, Kaufer D, Friedman A (2010) Blood–brain barrier breakdown as a therapeutic target in traumatic brain injury. Nat Rev Neurol 6(7):393–403
61. Shue E, Carson-Walter E, Liu Y, Winans B, Ali Z, Chen J, Walter K (2008) Plasmalemmal vesicle associated protein-1 (PV-1) is a marker of blood–brain barrier disruption in rodent models. BMC Neurosci 9(1):29
62. Simionescu M, Popov D, Sima A (2009) Endothelial transcytosis in health and disease. Cell Tissue Res 335(1):27–40. doi:10.1007/s00441-008-0688-3
63. Stan R-V, Marion K, Palade GE (1999) PV-1 is a component of the fenestral and stomatal diaphragms in fenestrated endothelia. Proc Natl Acad Sci U S A 96(23):13203–13207
64. Sun Y, Hu G, Zhang X, Minshall RD (2009) Phosphorylation of Caveolin-1 Regulates Oxidant–Induced Pulmonary Vascular Permeability via Paracellular and Transcellular Pathways. Circ Res 105(7):676–685. doi:10.1161/circresaha.109.201673
65. Sun Y, Wang J, Wu X, Xi C, Gai Y, Liu H, Yuan Q, Wang E, Gao L, Hu J, Zhou L (2011) Validating the incidence of coagulopathy and disseminated intravascular coagulation in patients with traumatic brain injury – analysis of 242 cases. Br J Neurosurg 25(3):363–368. doi:10.3109/02688697.2011.552650
66. Tran HT, LaFerla FM, Holtzman DM, Brody DL (2011) Controlled cortical impact traumatic brain injury in 3xTg-AD mice causes acute intra-axonal aAmyloid-β accumulation and independently accelerates the development of Tau abnormalities. J Neurosci 31(26):9513–9525. doi:10.1523/jneurosci.0858-11.2011
67. Tyagi N, Roberts AM, Dean WL, Tyagi SC, Lominadze D (2008) Fibrinogen induces endothelial cell permeability. Mol Cell Biochem 307(1–2):13–22
68. Wang X, Jung J, Asahi M, Chwang W, Russo L, Moskowitz MA, Dixon CE, Fini ME, Lo EH (2000) Effects of matrix metalloproteinase-9 gene knock-out on morphological and motor outcomes after traumatic brain injury. J Neurosci 20(18):7037–7042
69. Wei E, Hamm R, Baranova A, Povlishock J (2009) The long-term microvascular and behavioral consequences of experimental traumatic brain injury after hypothermic intervention. J Neurotrauma 26(4):527–537
70. Yamaguchi M, Jadhav V, Obenaus A, Colohan A, Zhang JH (2007) Matrix Metalloproteinase Inhibition Attenuates Brain Edema in An in Vivo Model of Surgically‐Induced Brain Injury. Neurosurgery 61(5):1067–1076, 1010.1227/1001.neu.0000303203.0000307866.0000303218
71. Yu J, Bergaya S, Murata T, Alp IF, Bauer MP, Lin MI, Drab M, Kurzchalia TV, Stan RV, Sessa WC (2006) Direct evidence for the role of caveolin-1 and caveolae in mechanotransduction and remodeling of blood vessels. J Clin Investig 116(5):1284. doi:10.1172/jci27100
72. Zhang R, Yang D, Zhou C, Cheng K, Liu Z, Chen L, Fang L, Xie P (2012) β-Actin as a loading control for plasma-based Western blot analysis of major depressive disorder patients. Anal Biochem 427(2):116–120. doi:10.1016/j.ab.2012.05.008
73. Zlokovic BV, Griffin JH (2011) Cytoprotective protein C pathways and implications for stroke and neurological disorders. Trends Neurosci 34(4):198–209. doi:10.1016/j.tins.2011.01.005