Membrane-type 1 metalloproteinase is upregulated in microglia/brain macrophages in neurodegenerative and neuroinflammatory diseases

Journal of Neuroscience Research

Volumn 92, Issue 3, 2014, Pages 275-286

  Langenfurth, Anika ^a,b   Rinnenthal, Jan Leo ^b   Vinnakota, Katyayni ^a   Prinz, Vincent ^b   Carlo, Anne Sophie ^a,c   Stadelmann, Christine ^d   Siffrin, Volker ^e   Peaschke, Susann ^a   Endres, Matthias ^b   Heppner, Frank ^b   Glass, Rainer ^f   Wolf, Susanne A ^a   Kettenmann, Helmut ^a  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

^d UNIVERSITY OF GÖTTINGEN   (Germany)

^e UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^f LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

Author keywords

Alzheimer's disease; Amyotrophic lateral sclerosis; Macrophages; Metalloproteinase; Microglia; MMP 14; MT1 MMP; Multiple sclerosis; Neurodegeneration; Neuroinflammation; Stroke; Trauma

Indexed keywords

MATRIX METALLOPROTEINASE 14;

ALZHEIMER DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INJURY; CEREBROVASCULAR ACCIDENT; CONTROLLED STUDY; DEGENERATIVE DISEASE; GLIOBLASTOMA; HUMAN; HUMAN TISSUE; MACROPHAGE; MALE; MICROGLIA; MOUSE; MULTIPLE SCLEROSIS; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION;

ALZHEIMER'S DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; MACROPHAGES; METALLOPROTEINASE; MICROGLIA; MMP-14; MT1-MMP; MULTIPLE SCLEROSIS; NEURODEGENERATION; NEUROINFLAMMATION; STROKE; TRAUMA;

ALZHEIMER DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; ENCEPHALITIS; GLIOMA; HUMANS; MACROPHAGES; MALE; MATRIX METALLOPROTEINASE 14; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROGLIA; NEURODEGENERATIVE DISEASES; UP-REGULATION; WOUNDS, STAB;

EID: 84892486218     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.23288     Document Type: Article

References (31)

1. Bar-Or A, Nuttall RK, Duddy M, Alter A, Kim HJ, Ifergan I, Pennington CJ, Bourgoin P, Edwards DR, Yong VW. 2003. Analyses of all matrix metalloproteinase members in leukocytes emphasize monocytes as major inflammatory mediators in multiple sclerosis. Brain 126:2738-2749.
2. Belien AT, Paganetti PA, Schwab ME. 1999. Membrane-type 1 matrix metalloprotease (MT1-MMP) enables invasive migration of glioma cells in central nervous system white matter. J Cell Biol 144:373-384.
3. Charles NA, Holland EC, Gilbertson R, Glass R, Kettenmann H. 2011. The brain tumor microenvironment. Glia 59:1169-1180.
4. Crocker SJ, Frausto RF, Whitton JL, Milner R. 2008. A novel method to establish microglia-free astrocyte cultures: comparison of matrix metalloproteinase expression profiles in pure cultures of astrocytes and microglia. Glia 56:1187-1198.
5. Denes A, Vidyasagar R, Feng J, Narvainen J, McColl BW, Kauppinen RA, Allan SM. 2007. Proliferating resident microglia after focal cerebral ischaemia in mice. J Cereb Blood Flow Metab 27:1941-1953.
6. Forsyth PA, Wong H, Laing TD, Rewcastle NB, Morris DG, Muzik H, Leco KJ, Johnston RN, Brasher PM, Sutherland G, Edwards DR. 1999. Gelatinase-A (MMP-2), gelatinase-B (MMP-9) and membrane type matrix metalloproteinase-1 (MT1-MMP) are involved in different aspects of the pathophysiology of malignant gliomas. Br J Cancer 79:1828-1835.
7. Gabrusiewicz K, Ellert-Miklaszewska A, Lipko M, Sielska M, Frankowska M, Kaminska B. 2011. Characteristics of the alternative phenotype of microglia/macrophages and its modulation in experimental gliomas. PloS One 6(8).
8. Groters S, Alldinger S, Baumgartner W. 2005. Upregulation of mRNA for matrix metalloproteinases-9 and -14 in advanced lesions of demyelinating canine distemper leukoencephalitis. Acta Neuropathol 110:369-382.
9. Henriques A, Pitzer C, Schneider A. 2010. Characterization of a novel SOD-1(G93A) transgenic mouse line with very decelerated disease development. PloS One 5:e15445.
10. Imai Y, Kohsaka S. 2002. Intracellular signaling in M-CSF-induced microglia activation: role of Iba1. Glia 40:164-174.
11. Jung S, Aliberti J, Graemmel P, Sunshine MJ, Kreutzberg GW, Sher A, Littman DR. 2000. Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol Cell Biol 20:4106-4114.
12. Kajita M, Itoh Y, Chiba T, Mori H, Okada A, Kinoh H, Seiki M. 2001. Membrane-type 1 matrix metalloproteinase cleaves CD44 and promotes cell migration. J Cell Biol 153:893-904.
13. Kempermann G, Gast D, Kronenberg G, Yamaguchi M, Gage FH. 2003. Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development 130:391-399.
14. Koshikawa N, Giannelli G, Cirulli V, Miyazaki K, Quaranta V. 2000. Role of cell surface metalloprotease MT1-MMP in epithelial cell migration over laminin-5. J Cell Biol 148:615-624.
15. Laufs U, La Fata V, Plutzky J, Liao JK. 1998. Upregulation of endothelial nitric oxide synthase by HMG CoA reductase inhibitors. Circulation 97:1129-1135.
16. Liao MC, Van Nostrand WE. 2010. Degradation of soluble and fibrillar amyloid beta-protein by matrix metalloproteinase (MT1-MMP) in vitro. Biochemistry 49:1127-1136.
17. Lynch MA. 2009. The multifaceted profile of activated microglia. Mol Neurobiol 40:139-156.
18. Lyons SA, Pastor A, Ohlemeyer C, Kann O, Wiegand F, Prass K, Knapp F, Kettenmann H, Dirnagl U. 2000. Distinct physiologic properties of microglia and blood-borne cells in rat brain slices after permanent middle cerebral artery occlusion. J Cereb Blood Flow Metab 20:1537-1549.
19. Markovic DS, Vinnakota K, Chirasani S, Synowitz M, Raguet H, Stock K, Sliwa M, Lehmann S, Kalin R, van Rooijen N, Holmbeck K, Heppner FL, Kiwit J, Matyash V, Lehnardt S, Kaminska B, Glass R, Kettenmann H. 2009. Gliomas induce and exploit microglial MT1-MMP expression for tumor expansion. Proc Natl Acad Sci U S A 106:12530-12535.
20. Markovic DS, Vinnakota K, van Rooijen N, Kiwit J, Synowitz M, Glass R, Kettenmann H. 2011. Minocycline reduces glioma expansion and invasion by attenuating microglial MT1-MMP expression. Brain Behav Immun 25:624-628.
21. Nakada M, Kita D, Futami K, Yamashita J, Fujimoto N, Sato H, Okada Y. 2001. Roles of membrane type 1 matrix metalloproteinase and tissue inhibitor of metalloproteinases 2 in invasion and dissemination of human malignant glioma. J Neurosurg 94:464-473.
22. Oakley H, Cole SL, Logan S, Maus E, Shao P, Craft J, Guillozet-Bongaarts A, Ohno M, Disterhoft J, Van Eldik L, Berry R, Vassar R. 2006. Intraneuronal beta-amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimer's disease mutations: potential factors in amyloid plaque formation. J Neurosci 26:10129-10140.
23. Ohuchi E, Imai K, Fujii Y, Sato H, Seiki M, Okada Y. 1997. Membrane type 1 matrix metalloproteinase digests interstitial collagens and other extracellular matrix macromolecules. J Biol Chem 272:2446-2451.
24. Olson JK, Miller SD. 2004. Microglia initiate central nervous system innate and adaptive immune responses through multiple TLRs. J Immunol 173:3916-3924.
25. Rathke-Hartlieb S, Budde P, Ewert S, Schlomann U, Staege MS, Jockusch H, Bartsch JW, Frey J. 2000. Elevated expression of membrane type 1 metalloproteinase (MT1-MMP) in reactive astrocytes following neurodegeneration in mouse central nervous system. FEBS Lett 481:227-234.
26. Sato H TT, Okada Y, Cao Y, Shinagawa A, Yamato E, Seiki M. 1994. A matrix metalloproteinase expressed on the surface of invasive tumor cells. Nature 370:61-65.
27. Seiki M. 1999. Membrane-type matrix metalloproteinases. APMIS 107:137-143.
28. Seiki M. 2002. The cell surface: the stage for matrix metalloproteinase regulation of migration. Curr Opin Cell Biol 14:624-632.
29. Takino T, Sato H, Yamamoto E, Seiki M. 1995. Cloning of a human gene potentially encoding a novel matrix metalloproteinase having a C-terminal transmembrane domain. Gene 155:293-298.
30. Tam EM, Morrison CJ, Wu YI, Stack MS, Overall CM. 2004. Membrane protease proteomics: Isotope-coded affinity tag MS identification of undescribed MT1-matrix metalloproteinase substrates. Proc Natl Acad Sci U S A 101:6917-6922.
31. Yamada T, Yoshiyama Y, Sato H, Seiki M, Shinagawa A, Takahashi M. 1995. White matter microglia produce membrane-type matrix metalloprotease, an activator of gelatinase A, in human brain tissues. Acta Neuropathol 90:421-424.