Long-term expression of tissue-inhibitor of matrix metalloproteinase-1 in the murine central nervous system does not alter the morphological and behavioral phenotype but alleviates the course of experimental allergic encephalomyelitis

American Journal of Pathology

Volumn 177, Issue 2, 2010, Pages 840-853

  Althoff, Gioia E M ^a,b   Wolfer, David P ^c,d   Timmesfeld, Nina ^a   Kanzler, Benoit ^e   Schrewe, Heinrich ^f,g   Pagenstecher, Axel ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d ETH ZURICH   (Switzerland)

^e MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

^f MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^g CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

INTERSTITIAL COLLAGENASE;

ADULT; ALLERGIC ENCEPHALOMYELITIS; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BRAIN FUNCTION; CENTRAL NERVOUS SYSTEM; ENZYME ACTIVITY; ENZYME INHIBITION; HISTOLOGY; HUMAN; IN SITU HYBRIDIZATION; INFLAMMATION; LEARNING; MEMORY; MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSGENIC MOUSE; UPREGULATION;

EID: 77957275587     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.090918     Document Type: Article

References (57)

1. Edwards D, Waterhouse P, Holman M, Denhardt D: A growth-responsive gene (16C8) in normal mouse fibroblasts homologous to a human collagenase inhibitor with erythroid-potentiating activity: evidence for inducible and constitutive transcripts. Nucleic Acids Res 1986, 14:8863-8878
2. Leco K, Hayden L, Sharma R, Rocheleau H, Greenberg A, Edwards D: Differential regulation of TIMP-1 and TIMP-2 mRNA expression in normal and Ha-ras-transformed murine fibroblasts. Gene 1992, 117:209-217
3. Sternlicht M, Werb Z: How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 2001, 17:463-516 (Pubitemid 33096184)
4. Vaillant C, Didier-Bazès M, Hutter A, Belin M, Thomasset N: Spatiotemporal expression patterns of metalloproteinases and their inhibitors in the postnatal developing rat cerebellum. J Neurosci 1999, 19:4994-5004
5. Ulrich R, Gerhauser I, Seeliger F, Baumgärtner W, Alldinger S: Matrix metalloproteinases and their inhibitors in the developing mouse brain and spinal cord: a reverse transcription quantitative polymerase chain reaction study. Dev Neurosci 2005, 27:408-418 (Pubitemid 41567388)
6. Fager N, Jaworski D: Differential spatial distribution and temporal regulation of tissue inhibitor of metalloproteinase mRNA expression during rat central nervous system development. Mech Dev 2000, 98:105-109
7. Rivera S, Tremblay E, Timsit S, Canals O, Ben-Ari Y, Khrestchatisky M: Tissue inhibitor of metalloproteinases-1 (TIMP-1) is differentially induced in neurons and astrocytes after seizures: evidence for developmental, immediate early gene, and lesion response. J Neurosci 1997, 17:4223-4235 (Pubitemid 27220613)
8. Sekine-Aizawa Y, Hama E, Watanabe K, Tsubuki S, Kanai-Azuma M, Kanai Y, Arai H, Aizawa H, Iwata N, Saido T: Matrix metalloproteinase (MMP) system in brain: identification and characterization of brainspecific MMP highly expressed in cerebellum. Eur J Neurosci 2001, 13:935-948
9. Ayoub A, Cai T, Kaplan R, Luo J: Developmental expression of matrix metalloproteinases 2 and 9 and their potential role in the histogenesis of the cerebellar cortex. J Comp Neurol 2005, 481:403-415
10. Jourquin J, Tremblay E, Bernard A, Charton G, Chaillan F, Marchetti E, Roman F, Soloway P, Dive V, Yiotakis A, Khrestchatisky M, Rivera S: Tissue inhibitor of metalloproteinases-1 (TIMP-1) modulates neuronal death, axonal plasticity, and learning and memory. Eur J Neurosci 2005, 22:2569-2578 (Pubitemid 41758999)
11. Chaillan F, Rivera S, Marchetti E, Jourquin J, Werb Z, Soloway P, Khrestchatisky M, Roman F: Involvement of tissue inhibition of metalloproteinases-1 in learning and memory in mice. Behav Brain Res 2006, 173:191-198 (Pubitemid 44308496)
12. Yong V, Power C, Forsyth P, Edwards D: Metalloproteinases in biology and pathology of the nervous system. Nat Rev Neurosci 2001, 2:502-511 (Pubitemid 33676585)
13. Webber C, Hocking J, Yong V, Stange C, McFarlane S: Metalloproteases and guidance of retinal axons in the developing visual system. J Neurosci 2002, 22:8091-8100 (Pubitemid 35379115)
14. Pittman R, Williams A: Neurite penetration into collagen gels requires Ca2+-dependent metalloproteinase activity. Dev Neurosci 1989, 11:41-51 (Pubitemid 19057539)
15. Sheffield J, Krasnopolsky V, Dehlinger E: Inhibition of retinal growth cone activity by specific metalloproteinase inhibitors in vitro. Dev Dyn 1994, 200:79-88 (Pubitemid 24178289)
16. Nordstrom L, Lochner J, Yeung W, Ciment G: The metalloproteinase stromelysin-1 (transin) mediates PC12 cell growth cone invasiveness through basal laminae. Mol Cell Neurosci 1995, 6:56-68
17. Pagenstecher A, Stalder A, Kincaid C, Shapiro S, Campbell I: Differential expression of matrix metalloproteinase and tissue inhibitor of matrix metalloproteinase genes in the mouse central nervous system in normal and inflammatory states. Am J Pathol 1998, 152:729-741 (Pubitemid 28110720)
18. Pagenstecher A, Wussler E, Opdenakker G, Volk B, Campbell I: Distinct expression patterns and levels of enzymatic activity of matrix metalloproteinases and their inhibitors in primary brain tumors. J Neuropathol Exp Neurol 2001, 60:598-612 (Pubitemid 32523624)
19. Khrestchatisky M, Jourquin J, Ogier C, Charton G, Bernard A, Tremblay E, Rivera S: Matrix metalloproteinases and their inhibitors, modulators of neuro-immune interactions and of pathophysiological processes in the nervous system. J Soc Biol 2003, 197:133-144
20. Gijbels K, Masure S, Carton H, Opdenakker G: Gelatinase in the cerebrospinal fluid of patients with multiple sclerosis and other inflammatory neurological disorders. J Neuroimmunol 1992, 41:29-34
21. Yong V, Krekoski C, Forsyth P, Bell R, Edwards D: Matrix metalloproteinases and diseases of the CNS. Trends Neurosci 1998, 21:75-80
22. Leppert D, Ford J, Stabler G, Grygar C, Lienert C, Huber S, Miller K, Hauser S, Kappos L: Matrix metalloproteinase-9 (gelatinase B) is selectively elevated in CSF during relapses and stable phases of multiple sclerosis. Brain 1998, 121 (Pt 12):2327-2334 (Pubitemid 28552469)
23. Gijbels K, Galardy R, Steinman L: Reversal of experimental autoimmune encephalomyelitis with a hydroxamate inhibitor of matrix metalloproteases. J Clin Invest 1994, 94:2177-2182 (Pubitemid 24379586)
24. Hewson A, Smith T, Leonard J, Cuzner M: Suppression of experimental allergic encephalomyelitis in the Lewis rat by the matrix metalloproteinase inhibitor Ro31-9790. Inflamm Res 1995, 44:345-349
25. Liedtke W, Cannella B, Mazzaccaro R, Clements J, Miller K, Wucherpfennig K, Gearing A, Raine C: Effective treatment of models of multiple sclerosis by matrix metalloproteinase inhibitors. Ann Neurol 1998, 44:35-46 (Pubitemid 28323653)
26. Crocker S, Whitmire J, Frausto R, Chertboonmuang P, Soloway P, Whitton J, Campbell I: Persistent macrophage/microglial activation and myelin disruption after experimental autoimmune encephalomyelitis in tissue inhibitor of metalloproteinase-1-deficient mice. Am J Pathol 2006, 169:2104-2116
27. Dormán G, Kocsis-Szommer K, Spadoni C, Ferdinandy P: MMP inhibitors in cardiac diseases: an update. Recent Pat Cardiovasc Drug Discov 2007, 2:186-194
28. Pagenstecher A, Lassmann S, Carson M, Kincaid C, Stalder A, Campbell I: Astrocyte-targeted expression of IL-12 induces active cellular immune responses in the central nervous system and modulates experimental allergic encephalomyelitis. J Immunol 2000, 164:4481-4492
29. Van den Steen PE, Van Aelst I, Starckx S, Maskos K, Opdenakker G, Pagenstecher A: Matrix metalloproteinases, tissue inhibitors of MMPs and TACE in experimental cerebral malaria. Laboratory Investigation 2006, 86:873-888
30. Rauer M, Pagenstecher A, Schulte-Mönting J, Sauder C: Upregulation of chemokine receptor gene expression in brains of Borna disease virus (BDV)-infected rats in the absence and presence of inflammation. J Neurovirol 2002, 8:168-179
31. Wolfer D, Madani R, Valenti P, Lipp H: Extended analysis of path data from mutant mice using the public domain software Wintrack. Physiol Behav 2001, 73:745-753
32. Mohajeri M, Madani R, Saini K, Lipp H, Nitsch R, Wolfer D: The impact of genetic background on neurodegeneration and behavior in seizured mice. Genes Brain Behav 2004, 3:228-239
33. Madani R, Kozlov S, Akhmedov A, Cinelli P, Kinter J, Lipp H, Sonderegger P, Wolfer D: Impaired explorative behavior and neophobia in genetically modified mice lacking or overexpressing the extracellular serine protease inhibitor neuroserpin. Mol Cell Neurosci 2003, 23:473-494
34. Altman DG: Practical statistics for medical research. London, Chapman and Hall, 1991
35. Whishaw I: Cholinergic receptor blockade in the rat impairs locale but not taxon strategies for place navigation in a swimming pool. Behav Neurosci 1985, 99:979-1005
36. Gallagher M, Burwell R, Burchinal M: Severity of spatial learning impairment in aging: development of a learning index for performance in the Morris water maze. Behav Neurosci 1993, 107:618-626
37. Kafkafi N, Pagis M, Lipkind D, Mayo C, Bemjamini Y, Golani I, Elmer G: Darting behavior: a quantitative movement pattern designed for discrimination and replicability in mouse locomotor behavior. Behav Brain Res 2003, 142:193-205
38. Vu T, Werb Z: Matrix metalloproteinases: effectors of development and normal physiology. Genes Dev 2000, 14:2123-2133
39. Page-McCaw A, Ewald A, Werb Z: Matrix metalloproteinases and the regulation of tissue remodelling. Nat Rev Mol Cell Biol 2007, 8:221-233
40. Machida C, Rodland K, Matrisian L, Magun B, Ciment G: NGF induction of the gene encoding the protease transin accompanies neuronal differentiation in PC12 cells. Neuron 1989, 2:1587-1596
41. Zuo J, Neubauer D, Dyess K, Ferguson T, Muir D: Degradation of chondroitin sulfate proteoglycan enhances the neurite-promoting potential of spinal cord tissue. Exp Neurol 1998, 154:654-662
42. Oh L, Larsen P, Krekoski C, Edwards D, Donovan F, Werb Z, Yong V: Matrix metalloproteinase-9/gelatinase B is required for process outgrowth by oligodendrocytes. J Neurosci 1999, 19:8464-8475
43. Vaillant C, Meissirel C, Mutin M, Belin M, Lund L, Thomasset N: MMP-9 deficiency affects axonal outgrowth, migration, and apoptosis in the developing cerebellum. Mol Cell Neurosci 2003, 24:395-408
44. Larsen P, DaSilva A, Conant K, Yong V: Myelin formation during development of the CNS is delayed in matrix metalloproteinase-9 and -12 null mice. J Neurosci 2006, 26:2207-2214
45. Larsen P, Wells J, Stallcup W, Opdenakker G, Yong V: Matrix metalloproteinase-9 facilitates remyelination in part by processing the inhibitory NG2 proteoglycan. J Neurosci 2003, 23:11127-11135
46. Hsu J, Bourguignon L, Adams C, Peyrollier K, Zhang H, Fandel T, Cun C, Werb Z, Noble-Haeusslein L: Matrix metalloproteinase-9 facilitates glial scar formation in the injured spinal cord. J Neurosci 2008, 28:13467-13477
47. Troeberg L, Tanaka M, Wait R, Shi Y, Brew K, Nagase H: E. coli expression of TIMP-4 and comparative kinetic studies with TIMP-1 and TIMP-2: insights into the interactions of TIMPs and matrix metalloproteinase 2 (gelatinase A). Biochemistry 2002, 41:15025-15035
48. Nuttall R, Sampieri C, Pennington C, Gill S, Schultz G, Edwards D: Expression analysis of the entire MMP and TIMP gene families during mouse tissue development. FEBS Lett 2004, 563:129-134
49. Elezkurtaj S, Kopitz C, Baker A, Perez-Cantó A, Arlt M, Khokha R, Gansbacher B, Anton M, Brand K, Krüger A: Adenovirus-mediated overexpression of tissue inhibitor of metalloproteinases-1 in the liver: efficient protection against T-cell lymphoma and colon carcinoma metastasis. J Gene Med 2004, 6:1228-1237
50. Michael M, Babic B, Khokha R, Tsao M, Ho J, Pintilie M, Leco K, Chamberlain D, Shepherd F: Expression and prognostic significance of metalloproteinases and their tissue inhibitors in patients with small-cell lung cancer. J Clin Oncol 1999, 17:1802-1808
51. Thomas P, Khokha R, Shepherd F, Feld R, Tsao M: Differential expression of matrix metalloproteinases and their inhibitors in non-small cell lung cancer. J Pathol 2000, 190:150-156
52. Toft-Hansen H, Nuttall R, Edwards D, Owens T: Key metalloproteinases are expressed by specific cell types in experimental autoimmune encephalomyelitis. J Immunol 2004, 173:5209-5218
53. Teesalu T, Hinkkanen A, Vaheri A: Coordinated induction of extracellular proteolysis systems during experimental autoimmune encephalomyelitis in mice. Am J Pathol 2001, 159:2227-2237
54. Lindberg R, De Groot C, Montagne L, Freitag P, van der Valk P, Kappos L, Leppert D: The expression profile of matrix metalloproteinases (MMPs) and their inhibitors (TIMPs) in lesions and normal appearing white matter of multiple sclerosis. Brain 2001, 124:1743-1753
55. Boz C, Ozmenoglu M, Velioglu S, Kilinc K, Orem A, Alioglu Z, Altunayoglu V: Matrix metalloproteinase-9 (MMP-9) and tissue inhibitor of matrix metalloproteinase (TIMP-1) in patients with relapsing-remitting multiple sclerosis treated with interferon beta. Clin Neurol Neurosurg 2006, 108:124-128
56. Ichiyama T, Kajimoto M, Suenaga N, Maeba S, Matsubara T, Furukawa S: Serum levels of matrix metalloproteinase-9 and its tissue inhibitor (TIMP-1) in acute disseminated encephalomyelitis. J Neuroimmunol 2006, 172:182-186
57. Gran B, Tabibzadeh N, Martin A, Ventura E, Ware J, Zhang G, Parr J, Kennedy A, Rostami A: The protease inhibitor, Bowman-Birk Inhibitor, suppresses experimental autoimmune encephalomyelitis: a potential oral therapy for multiple sclerosis. Mult Scler 2006, 12:688-697