Matrix metalloproteinase-9 deficiency leads to prolonged foreign body response in the brain associated with increased IL-1β levels and leakage of the blood-brain barrier

Matrix Biology

Volumn 28, Issue 3, 2009, Pages 148-159

  Tian, Weiming ^a   Kyriakides, Themis R ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

Biomaterials; Blood brain barrier; Foreign body response; Interleukin; Matrix metalloproteinase; Neuroinflammation

Indexed keywords

BRAIN PROTEIN; CELLULOSE; ESTER; GELATINASE B; INTERLEUKIN 1BETA; SERUM ALBUMIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; BLOOD VESSEL; BRAIN CORTEX; CONTROLLED STUDY; ENCEPHALITIS; HISTOLOGY; IMMUNOHISTOCHEMISTRY; IMPLANTATION; MACROPHAGE; MICROGLIA; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; TIGHT JUNCTION; WESTERN BLOTTING; WILD TYPE;

ANIMALS; ASTROCYTES; BLOOD-BRAIN BARRIER; BRAIN; CELL COUNT; FOREIGN-BODY REACTION; GLIOSIS; INFLAMMATION; INTERLEUKIN-1BETA; MACROPHAGES; MATRIX METALLOPROTEINASE 9; MEMBRANE PROTEINS; MICE; MICE, INBRED STRAINS; MICE, KNOCKOUT; MICROGLIA; MICROPORE FILTERS; NEOVASCULARIZATION, PATHOLOGIC; NEUTROPHILS; PHOSPHOPROTEINS; PROSTHESES AND IMPLANTS; SERUM ALBUMIN;

MUS;

EID: 67349130899     PISSN: 0945053X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.matbio.2009.02.002     Document Type: Article

References (75)

1. Agah A., Kyriakides T.R., Letrondo N., Bjorkblom B., and Bornstein P. Thrombospondin 2 levels are increased in aged mice: consequences for cutaneous wound healing and angiogenesis. Matrix Biol. 22 (2004) 539-547
2. Agrawal S., Anderson P., Durbeej M., van Rooijen N., Ivars F., Opdenakker G., and Sorokin L.M. Dystroglycan is selectively cleaved at the parenchymal basement membrane at sites of leukocyte extravasation in experimental autoimmune encephalomyelitis. J. Exp. Med. 203 (2006) 1007-1019
3. Agrawal S.M., Lau L., and Yong V.W. MMPs in the central nervous system: where the good guys go bad. Sem. Cell Dev. Biol. 19 (2008) 42-51
4. Albaiceta G.M., Gutierrez-Fernandez A., Parra D., Astudillo A., Garcia-Prieto E., Taboada F., and Fueyo A. Lack of matrix metalloproteinase-9 worsens ventilator-induced lung injury. Am. J. Physiol. Lung Cell. Mol. Physiol. 294 (2008) L535-L543
5. Anderson J.M., Rodriguez A., and Chang D.T. Foreign body reaction to biomaterials. Sem. Immunol. 20 (2008) 86-100
6. Argaw A.T., Zhang Y.T., Snyder B.J., Zhao M.L., Kopp N., Lee S.C., Raine C.S., Brosnan C.F., and John G.R. IL-1 beta regulates blood-brain barrier permeability via reactivation of the hypoxia-angiogenesis program. J. Immunol. 177 (2006) 5574-5584
7. Asahi M., Wang X., Mori T., Sumii T., Jung J.C., Moskowitz M.A., Fini M.E., and Lo E.H. Effects of matrix metalloproteinase-9 gene knock-out on the proteolysis of blood-brain barrier and white matter components after cerebral ischemia. J. Neurosci. 21 (2001) 7724-7732
8. Balasingam V., Dickson K., Brade A., and Yong V.W. Astrocyte reactivity in neonatal mice: apparent dependence on the presence of reactive microglia/macrophages. Glia 18 (1996) 11-26
9. Beck D.W., Hart M.N., and Cancilla P.A. The role of the macrophage in microvascular regeneration following brain injury. J. Neuropathol. Exp. Neurol 42 (1983) 601-614
10. Biran R., Martin D.C., and Tresco P.A. Neuronal cell loss accompanies the brain tissue response to chronically implanted silicon microelectrode arrays. Exp. Neurol. 195 (2005) 115-126
11. Blight A.R. Effects of silica on the outcome from experimental spinal cord injury: implication of macrophages in secondary tissue damage. Neuroscience 60 (1994) 263-273
12. Bolton S.J., Anthony D.C., and Perry V.H. Loss of the tight junction proteins occludin and zonula occludens-1 from cerebral vascular endothelium during neutrophil-induced blood-brain barrier breakdown in vivo. Neuroscience 86 (1998) 1245-1257
13. Canete-Soler R., Gui Y.H., Linask K.K., and Muschel R.J. Developmental expression of MMP-9 (gelatinase B) mRNA in mouse embryos. Dev. Dyn. 204 (1995) 30-40
14. Cheung K.C. Implantable microscale neural interfaces. Biomedical Microdevices 9 (2007) 923-938
15. Copin J.C., and Gasche Y. Matrix metalloproteinase-9 deficiency has no effect on glial scar formation after transient focal cerebral ischemia in mouse. Brain Res. 1150 (2007) 167-173
16. Coulter K.R., Doseff A., Sweeney P., Wang Y.J., Marsh C.B., Wewers M.D., and Knoell D.L. Opposing effect by cytokines on Fas-mediated apoptosis in A549 lung epithelial cells. Am. J. Respir. Cell Mol. Biol. 26 (2002) 58-66
17. Coxon A., Tang T., and Mayadas T.N. Cytokine-activated endothelial cells delay neutrophil apoptosis in vitro and in vivo: a role for granulocyte/macrophage colony-stimulating factor. J. Exp. Med. 190 (1999) 923-933
18. Cunningham L.A., Wetzel M., and Rosenberg G.A. Multiple roles for MMPs and TIMPs in cerebral ischemia. Glia 50 (2005) 329-339
19. Ek C.J., Dziegielewska K.M., Stolp H., and Saunders N.R. Functional effectiveness of the blood brain barrier to small water-soluble molecules in developing and adult opossum (Monodelphis domestica). J. Comp. Neurol. 496 (2006) 13-26
20. Faulkner J.R., Herrmann J.E., Woo M.J., Tansey K.E., Doan N.B., and Sofroniew M.V. Reactive astrocytes protect tissue and preserve function after spinal cord injury. J. Neurosci. 24 (2004) 2143-2155
21. Fournier E., Passirani C., Montero-Menei C.N., and Benoit J.P. Biocompatibility of implantable synthetic polymeric drug carriers: focus on brain biocompatibility. Biomaterials 24 (2003) 3311-3331
22. Gross B., Bitterman N., Levanon D., Nir I., and Harel D. Horseradish peroxidase as a cytochemical marker of blood-brain barrier integrity in oxygen toxicity in the central nervous system. Exp. Neurol. 93 (1986) 471-480
23. Gu Z., Kaul M., Yan B., Kridel S.J., Cui J., Strongin A., Smith J.W., Liddington R.C., and Lipton S.A. S-nitrosylation of matrix metalloproteinases: signaling pathway to neuronal cell death. Science 297 (2002) 1186-1190
24. He W., McConnell G.C., and Bellamkonda R.V. Nanoscale laminin coating modulates cortical scarring response around implanted silicon microelectrode arrays. J. Neural Eng. 3 (2006) 316-326
25. Hogquist K.A., Nett M.A., Sheehan K.C.F., Pendleton K.D., Schreiber R.D., and Chaplin D.D. Generation of monoclonal antibodies to murine IL-1 beta and demonstration of IL-1 in vivo. J. Immunol. 146 (1991) 1534-1540
26. Ito A., Mukaiyama A., Itoh Y., Nagase H., Thogersen I.B., Enghild J.J., Sasaguri Y., and Mori Y. Degradation of interleukin 1beta by matrix metalloproteinases. J. Biol. Chem. 271 (1996) 14657-14660
27. Jacobs T.P., Kempski O., McKinley D., Dutka A.J., Hallenbeck J.M., and Feuerstein G. Blood flow and vascular permeability during motor dysfunction in a rabbit model of spinal cord ischemia. Stroke 23 (1992) 367-373
28. Jaeger C.B., Winn S.R., Tresco P.A., and Aebischer P. Repair of the blood-brain barrier following implantation of polymer capsules. Brain Res. 551 (1991) 163-170
29. Jones J.A., McNally A.K., Chang D.T., Meyerson L.A.Q.H., Colton E., Kwon I.L.K., Matsuda T., and Anderson J.M. Matrix metalloproteinases and their inhibitors in the foreign body reaction on biomaterials. J. Biomed. Mater. Res. Part A 84 (2008) 158-166
30. Kajiwara K., Ito H., and Fukumoto T. Lymphocyte infiltration into normal rat brain following hyperosmotic blood-brain barrier opening. J. Neuroimmunol. 27 (1990) 133-140
31. Kieseier B.C., Seifert T., Giovannoni G., and Hartung H.P. Matrix metalloproteinases in inflammatory demyelination: targets for treatment. Neurology 53 (1999) 20-25
32. Kim Y.T., Hitchcock R.W., Bridge M.J., and Tresco P.A. Chronic response of adult rat brain tissue to implants anchored to the skull. Biomaterials 25 (2004) 2229-2237
33. Kinoh H., Sato H., Tsunezuka Y., Takino T., Kawashima A., Okada Y., and Seiki M. MT-MMP, the cell surface activator of proMMP-2 (pro-gelatinase A), is expressed with its substrate in mouse tissue during embryogenesis. J. Cell Sci. 109 (1996) 953-959
34. Kolaczkowska E., Scislowska-Czarnecka A., Chadzinska M., Plytycz B., van Rooijen N., Opdenakker G., and Arnold B. Enhanced early vascular permeability in gelatinase B (MMP-9)-deficient mice: putative contribution of COX-1-derived PGE(2) of macrophage origin. J. Leukoc. Biol. 80 (2006) 125-132
35. Kyriakides T.R., and Bornstein P. Matricellular proteins as modulators of wound healing and the foreign body response. Thromb. Haemost. 90 (2003) 986-992
36. Kyriakides T.R., Foster M.J., Keeney G.E., Tsai A., Giachelli C.M., Clark-Lewis I., Rollins B.J., and Bornstein P. The CC chemokine ligand, CCL2/MCP1, participates in macrophage fusion and foreign body giant cell formation. Am. J. Pathol. 165 (2004) 2157-2166
37. Laterra J., Guerin C., and Goldstein G.W. Astrocytes induce neural microvascular endothelial cells to form capillary-like structures in vitro. J. Cell. Physiol. 144 (1990) 204-215
38. Lee S.R., and Lo E.H. Induction of caspase-mediated cell death by matrix metalloproteinases in cerebral endothelial cells after hypoxia-reoxygenation. J. Cereb. Blood Flow Metab. 24 (2004) 720-727
39. Lindberg R.L., De Groot C.J., Montagne L., Freitag P., van der Valk P., Kappos L., and Leppert D. The expression profile of matrix metalloproteinases (MMPs) and their inhibitors (TIMPs) in lesions and normal appearing white matter of multiple sclerosis. Brain 124 (2001) 1743-1753
40. Lo E.H., Dalkara T., and Moskowitz M.A. Mechanisms, challenges and opportunities in stroke. Nat. Rev. Neurosc. 4 (2003) 399-415
41. Maclauchlan, S., Skokos, E.A., Meznarich, N., Zhu, D.H., Raoof, S., Shipley, J.M., Senior, R.M., Bornstein, P., Kyriakides, T.R., in press. Macrophage fusion, giant cell formation, and the foreign body response require matrix metalloproteinase 9. J. Leukoc. Biol.
42. McMillan S.J., Kearley J., Campbell J.D., Zhu X.W., Larbi K.Y., Shipley J.M., Senior R.M., Nourshargh S., and Lloyd C.M. Matrix metalloproteinase-9 deficiency results in enhanced allergen-induced airway inflammation. J. Immunol. 172 (2004) 2586-2594
43. Medhora M., and Harder D. Functional role of epoxyeicosatrienoic acids and their production in astrocytes: approaches for gene transfer and therapy (review). Int. J. Mol. Med. 2 (1998) 661-669
44. Mitchell J., Weller R.O., and Evans H. Reestablishment of the blood brain barrier to peroxidase following cold injury to mouse cortex. Acta Neuropathol. 46 (1979) 45-49
45. Mun-Bryce S., and Rosenberg G.A. Gelatinase B modulates selective opening of the blood-brain barrier during inflammation. Am. J. Physiol. 274 (1998) R1203-1211
46. Murphy S., Pearce B., Jeremy J., and Dandona P. Astrocytes as eicosanoid-producing cells. Glia 1 (1988) 241-245
47. Nag S., Picard P., and Stewart D.J. Expression of nitric oxide synthases and nitrotyrosine during blood-brain barrier breakdown and repair after cold injury. Lab. Inv. 81 (2001) 41-49
48. Nagase H., and Woessner Jr. J.F. Matrix metalloproteinases. J. Biol. Chem. 274 (1999) 21491-21494
49. Noble L.J., Donovan F., Igarashi T., Goussev S., and Werb Z. Matrix metalloproteinases limit functional recovery after spinal cord injury by modulation of early vascular events. J. Neurosci. 22 (2002) 7526-7535
50. Noble L.J., and Wrathall J.R. Distribution and time course of protein extravasation in the rat spinal cord after contusive injury. Brain Res. 482 (1989) 57-66
51. Overall C.M., and Lopez-Otin C. Strategies for MMP inhibition in cancer: innovations for the post-trial era. Nat. Rev. Cancer 2 (2002) 657-672
52. Parks W.C., Wilson C.L., and Lopez-Boado Y.S. Matrix metalloproteinases as modulators of inflammation and innate immunity. Nat. Rev. 4 (2004) 617-629
53. Polikov V.S., Tresco P.A., and Reichert W.M. Response of brain tissue to chronically implanted neural electrodes. J. Neurosci. Methods 148 (2005) 1-18
54. Proost P., Van Damme J., and Opdenakker G. Leukocyte gelatinase B cleavage releases encephalitogens from human myelin basic protein. Biochem. Biophys. Res. Commun. 192 (1993) 1175-1181
55. Schenkel A.R., Mamdouh Z., and Muller W.A. Locomotion of monocytes on endothelium is a critical step during extravasation. Nat. Immunol. 5 (2004) 393-400
56. Schonbeck U., Mach F., and Libby P. Generation of biologically active IL-1 beta by matrix metalloproteinases: a novel caspase-1-independent pathway of IL-1 beta processing. J. Immunol. 161 (1998) 3340-3346
57. Shigemori Y., Katayama Y., Mori T., Maeda T., and Kawamata T. Matrix metalloproteinase-9 is associated with blood-brain barrier opening and brain edema formation after cortical contusion in rats. Acta Neurochir. 96 (2006) 130-133
58. Sood R.R., Taheri S., Candelario-Jalil E., Estrada E.Y., and Rosenberg G.A. Early beneficial effect of matrix metalloproteinase inhibition on blood-brain barrier permeability as measured by magnetic resonance imaging countered by impaired long-term recovery after stroke in rat brain. J. Cereb. Blood Flow Metab. 28 (2008) 431-438
59. Stolp H.B., Dziegielewska K.M., Ek C.J., Potter A.M., and Saunders N.R. Long-term changes in blood-brain barrier permeability and white matter following prolonged systemic inflammation in early development in the rat. Eur. J. Neurosci. 22 (2005) 2805-2816
60. Suarez I., Bodega G., Rubio M., Garcia-Segura L.M., and Fernandez B. Astroglial induction of in vivo angiogenesis. J. Neural Transpl. Plast. 5 (1994) 1-10
61. Szarowski D.H., Andersen M.D., Retterer S., Spence A.J., Isaacson M., Craighead H.G., Turner J.N., and Shain W. Brain responses to micro-machined silicon devices. Brain Res. 983 (2003) 23-35
62. Tang J., Liu J., Zhou C., Alexander J.S., Nanda A., Granger D.N., and Zhang J.H. Mmp-9 deficiency enhances collagenase-induced intracerebral hemorrhage and brain injury in mutant mice. J. Cereb. Blood Flow Metab. 24 (2004) 1133-1145
63. Tator C.H., and Fehlings M.G. Review of the secondary injury theory of acute spinal cord trauma with emphasis on vascular mechanisms. J. Neurosurg. 75 (1991) 15-26
64. van Vliet E.A., Araujo S.D., Redeker S., van Schaik R., Aronica E., and Gorter J.A. Blood-brain barrier leakage may lead to progression of temporal lobe epilepsy. Brain 130 (2007) 521-534
65. Visse R., and Nagase H. Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ. Res. 92 (2003) 827-839
66. Vu T.H., Shipley J.M., Bergers G., Berger J.E., Helms J.A., Hanahan D., Shapiro S.D., Senior R.M., and Werb Z. MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell 93 (1998) 411-422
67. Wang M., Qin X., Mudgett J.S., Ferguson T.A., Senior R.M., and Welgus H.G. Matrix metalloproteinase deficiencies affect contact hypersensitivity: stromelysin-1 deficiency prevents the response and gelatinase B deficiency prolongs the response. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 6885-6889
68. Wang P., Dai J., Bai F., Kong K.F., Wong S.J., Montgomery R.R., Madri J.A., and Fikrig E. Matrix metalloproteinase 9 facilitates West Nile virus entry into the brain. J. Virol. 82 (2008) 8978-8985
69. Wang X., Jung J., Asahi M., Chwang W., Russo L., Moskowitz M.A., Dixon C.E., Fini M.E., and Lo E.H. Effects of matrix metalloproteinase-9 gene knock-out on morphological and motor outcomes after traumatic brain injury. J. Neurosci. 20 (2000) 7037-7042
70. Wijsman J.A., and Shivers R.R. Heat stress affects blood-brain barrier permeability to horseradish peroxidase in mice. Acta Neuropathol. 86 (1993) 49-54
71. Williams K.C., and Hickey W.F. Traffic of hematogenous cells through the central nervous system. Curr. Top. Microbiol. Immunol. 202 (1995) 221-245
72. Yang Y., Estrada E.Y., Thompson J.F., Liu W., and Rosenberg G.A. Matrix metalloproteinase-mediated disruption of tight junction proteins in cerebral vessels is reversed by synthetic matrix metalloproteinase inhibitor in focal ischemia in rat. J. Cereb. Blood Flow Metab. 27 (2007) 697-709
73. Yong V.W. Metalloproteinases: mediators of pathology and regeneration in the CNS. Nat. Rev. Neurosci. 6 (2005) 931-944
74. Yoshizumi H., Fujibayashi Y., and Kikuchi H. A new approach to the integrity of dual blood-brain barrier functions of global ischemic rats. Barrier and carrier functions. Stroke 24 (1993) 279-284 discussion 284-275
75. Zhao B.Q., Wang S., Kim H.Y., Storrie H., Rosen B.R., Mooney D.J., Wang X., and Lo E.H. Role of matrix metalloproteinases in delayed cortical responses after stroke. Nat. Med. 12 (2006) 441-445