Matrix metalloproteinase-9 as a novel player in synaptic plasticity and schizophrenia

Schizophrenia Bulletin

Volumn 41, Issue 5, 2015, Pages 1003-1009

  Lepeta, Katarzyna ^a   Kaczmarek, Leszek ^a  

^a NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

Author keywords

Extracellular matrix; Glutamate; Synaptic plasticity

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CELL ADHESION MOLECULE; GELATINASE B; INTERCELLULAR ADHESION MOLECULE 5; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; TISSUE INHIBITOR OF METALLOPROTEINASE 1; UNCLASSIFIED DRUG; GLUTAMATE RECEPTOR;

ALCOHOLISM; AUTOIMMUNE DISEASE; BIPOLAR DISORDER; COCAINE DEPENDENCE; DENDRITIC SPINE; DEPRESSION; DNA POLYMORPHISM; ENZYME ACTIVITY; EPILEPSY; FRAGILE X SYNDROME; HUMAN; NERVE CELL PLASTICITY; NEUROPATHOLOGY; NONHUMAN; POSITIVE AND NEGATIVE SYNDROME SCALE; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SCHIZOPHRENIA; GENETICS; METABOLISM; PHYSIOLOGY;

HUMANS; MATRIX METALLOPROTEINASE 9; NEURONAL PLASTICITY; RECEPTORS, GLUTAMATE; SCHIZOPHRENIA;

EID: 84943154862     PISSN: 05867614     EISSN: 17451701     Source Type: Journal    
DOI: 10.1093/schbul/sbv036     Document Type: Review

References (69)

1. Rivera S, Khrestchatisky M, Kaczmarek L, Rosenberg GA, Jaworski DM. Metzincin proteases and their inhibitors: foes or friends in nervous system physiology? J Neurosci. 2010;30:15337-15357.
2. Michaluk P, Kaczmarek L. Matrix metalloproteinase-9 in glutamate-dependent adult brain function and dysfunction. Cell Death Differ. 2007;14:1255-1258.
3. Huntley GW. Synaptic circuit remodelling by matrix metalloproteinases in health and disease. Nat Rev Neurosci. 2012;13:743-757.
4. Stawarski M, Rutkowska-Wlodarczyk I, Zeug A, et al. Genetically encoded FRET-based biosensor for imaging MMP-9 activity. Biomaterials. 2014;35:1402-1410.
5. Wilczynski GM, Konopacki FA, Wilczek E, et al. Important role of matrix metalloproteinase 9 in epileptogenesis. J Cell Biol. 2008;180:1021-1035.
6. Gawlak M, Górkiewicz T, Gorlewicz A, Konopacki FA, Kaczmarek L, Wilczynski GM. High resolution in situ zymography reveals matrix metalloproteinase activity at glutamatergic synapses. Neuroscience. 2009;158:167-176.
7. Szklarczyk A, Lapinska J, Rylski M, McKay RD, Kaczmarek L. Matrix metalloproteinase-9 undergoes expression and activation during dendritic remodeling in adult hippocampus. J Neurosci. 2002;22:920-930.
8. Konopacki FA, Rylski M, Wilczek E, et al. Synaptic localization of seizure-induced matrix metalloproteinase-9 mRNA. Neuroscience. 2007;150:31-39.
9. Dziembowska M, Milek J, Janusz A, et al. Activity-dependent local translation of matrix metalloproteinase-9. J Neurosci. 2012;32:14538-14547.
10. Janusz A, Milek J, Perycz M, et al. The Fragile X mental retardation protein regulates matrix metalloproteinase 9 mRNA at synapses. J Neurosci. 2013;33:18234-18241.
11. Malenka RC, Bear MF. LTP and LTD: an embarrassment of riches. Neuron. 2004;44:5-21.
12. Wang XB, Bozdagi O, Nikitczuk JS, Zhai ZW, Zhou Q, Huntley GW. Extracellular proteolysis by matrix metalloproteinase-9 drives dendritic spine enlargement and long-term potentiation coordinately. Proc Natl Acad Sci USA. 2008;105:19520-19525.
13. Michaluk P, Wawrzyniak M, Alot P, et al. Influence of matrix metalloproteinase MMP-9 on dendritic spine morphology. J Cell Sci. 2011;124:3369-3380.
14. Szepesi Z, Hosy E, Ruszczycki B, et al. Synaptically released matrix metalloproteinase activity in control of structural plasticity and the cell surface distribution of GluA1-AMPA receptors. PLoS One. 2014;9:e98274.
15. Bilousova TV, Dansie L, Ngo M, et al. Minocycline promotes dendritic spine maturation and improves behavioural performance in the fragile X mouse model. J Med Genet. 2009;46:94-102.
16. Sidhu H, Dansie LE, Hickmott PW, Ethell DW, Ethell IM. Genetic removal of matrix metalloproteinase 9 rescues the symptoms of fragile X syndrome in a mouse model. J Neurosci. 2014;34:9867-9879.
17. Wright JW, Murphy ES, Elijah IE, et al. Influence of hippocampectomy on habituation, exploratory behavior, and spatial memory in rats. Brain Res. 2004;1023:1-14.
18. Nagy V, Bozdagi O, Matynia A, et al. Matrix metalloproteinase-9 is required for hippocampal late-phase long-term potentiation and memory. J Neurosci. 2006;26:1923-1934.
19. Knapska E, Lioudyno V, Kiryk A, et al. Reward learning requires activity of matrix metalloproteinase-9 in the central amygdala. J Neurosci. 2013;33:14591-14600.
20. Szklarczyk A, Kaczmarek L. Physiology of matrix MMPs and their tissue inhibitors in the brain. BIOTECH International. 2005;17:15-18.
21. Kelly EA, Tremblay ME, Gahmberg CG, Tian L, Majewska AK. Subcellular localization of intercellular adhesion molecule-5 (telencephalin) in the visual cortex is not developmentally regulated in the absence of matrix metalloproteinase-9. J Comp Neurol. 2014;522:676-688.
22. Aujla PK, Huntley GW. Early postnatal expression and localization of matrix metalloproteinases-2 and -9 during establishment of rat hippocampal synaptic circuitry. J Comp Neurol. 2014;522:1249-1263.
23. Mash DC, ffrench-Mullen J, Adi N, Qin Y, Buck A, Pablo J. Gene expression in human hippocampus from cocaine abusers identifies genes which regulate extracellular matrix remodeling. PLoS One. 2007;2:e1187.
24. Domenici E, Willé DR, Tozzi F, et al. Plasma protein biomarkers for depression and schizophrenia by multi analyte profiling of case-control collections. PLoS One. 2010;5:e9166.
25. Mizoguchi H, Yamada K, Nabeshima T. Matrix metalloproteinases contribute to neuronal dysfunction in animal models of drug dependence, Alzheimer's disease, and epilepsy. Biochem Res Int. 2011;2011:681385.
26. Smith AC, Kupchik YM, Scofield MD, et al. Synaptic plasticity mediating cocaine relapse requires matrix metalloproteinases. Nat Neurosci. 2014;17:1655-1657.
27. Rybakowski JK, Skibinska M, Leszczynska-Rodziewicz A, Kaczmarek L, Hauser J. Matrix metalloproteinase-9 gene and bipolar mood disorder. Neuromolecular Med. 2009;11:128-132.
28. Samochowiec A, Grzywacz A, Kaczmarek L, et al. Functional polymorphism of matrix metalloproteinase-9 (MMP-9) gene in alcohol dependence: family and case control study. Brain Res. 2010;1327:103-106.
29. Paribello C, Tao L, Folino A, et al. Open-label add-on treatment trial of minocycline in fragile X syndrome. BMC Neurol. 2010;10:91.
30. Wang LW, Berry-Kravis E, Hagerman RJ. Fragile X: leading the way for targeted treatments in autism. Neurotherapeutics. 2010;7:264-274.
31. Leigh MJ, Nguyen DV, Mu Y, et al. A randomized double-blind, placebo-controlled trial of minocycline in children and adolescents with fragile x syndrome. J Dev Behav Pediatr. 2013;34:147-155.
32. Dziembowska M, Pretto DI, Janusz A, et al. High MMP-9 activity levels in fragile X syndrome are lowered by minocycline. Am J Med Genet A. 2013;161A:1897-1903.
33. St Jean PL, Zhang XC, Hart BK, et al. Characterization of a dinucleotide repeat in the 92 kDa type IV collagenase gene (CLG4B), localization of CLG4B to chromosome 20 and the role of CLG4B in aortic aneurysmal disease. Ann Hum Genet. 1995;59:17-24.
34. Gurling HM, Kalsi G, Brynjolfson J, et al. Genomewide genetic linkage analysis confirms the presence of susceptibility loci for schizophrenia, on chromosomes 1q32.2, 5q33.2, and 8p21-22 and provides support for linkage to schizophrenia, on chromosomes 11q23.3-24 and 20q12.1-11.23. Am J Hum Genet. 2001;68:661-673.
35. Kaczmarek L, Lapinska-Dzwonek J, Szymczak S. Matrix metalloproteinases in the adult brain physiology: a link between c-Fos, AP-1 and remodeling of neuronal connections? EMBO J. 2002;21:6643-6648.
36. Okulski P, Jay TM, Jaworski J, et al. TIMP-1 abolishes MMP-9-dependent long-lasting long-term potentiation in the prefrontal cortex. Biol Psychiatry. 2007;62:359-362.
37. Akil M, Pierri JN, Whitehead RE, et al. Lamina-specific alterations in the dopamine innervation of the prefrontal cortex in schizophrenic subjects. Am J Psychiatry. 1999;156:1580-1589.
38. Bunney WE, Bunney BG. Evidence for a compromised dorsolateral prefrontal cortical parallel circuit in schizophrenia. Brain Res Brain Res Rev. 2000;31:138-146.
39. Je HS, Yang F, Ji Y, Nagappan G, Hempstead BL, Lu B. Role of pro-brain-derived neurotrophic factor (proBDNF) to mature BDNF conversion in activity-dependent competition at developing neuromuscular synapses. Proc Natl Acad Sci USA. 2012;109:15924-15929.
40. Michaluk P, Mikasova L, Groc L, Frischknecht R, Choquet D, Kaczmarek L. Matrix metalloproteinase-9 controls NMDA receptor surface diffusion through integrin beta1 signaling. J Neurosci. 2009;29:6007-6012.
41. Moyer CE, Shelton MA, Sweet RA. Dendritic spine alterations in schizophrenia. Neurosci Lett. 2014.
42. Roberts RC, Conley R, Kung L, Peretti FJ, Chute DJ. Reduced striatal spine size in schizophrenia: a postmortem ultrastructural study. Neuroreport. 1996;7:1214-1218.
43. O'Dushlaine C, Rossin L, Lee P, et al. Psychiatric genomewide association study analyses implicate neuronal, immune and histone pathways. Nat Neurosci. 2015;18:199-209.
44. Fragkouli A, Papatheodoropoulos C, Georgopoulos S, et al. Enhanced neuronal plasticity and elevated endogenous sAPPα levels in mice over-expressing MMP9. J Neurochem. 2012;121:239-251.
45. Gkogkas CG, Khoutorsky A, Cao R, et al. Pharmacogenetic inhibition of eIF4E-dependent Mmp9 mRNA translation reverses fragile X syndrome-like phenotypes. Cell Rep. 2014;9:1742-1755.
46. Zhang B, Ye S, Herrmann SM, et al. Functional polymorphism in the regulatory region of gelatinase B gene in relation to severity of coronary atherosclerosis. Circulation. 1999;99:1788-1794.
47. Rybakowski JK, Skibinska M, Kapelski P, Kaczmarek L, Hauser J. Functional polymorphism of the matrix metalloproteinase-9 (MMP-9) gene in schizophrenia. Schizophr Res. 2009;109:90-93.
48. Han H, He X, Tang J, et al. The C(-1562)T polymorphism of matrix metalloproteinase-9 gene is associated with schizophrenia in China. Psychiatry Res. 2011;190:163-164.
49. Groszewska A, Kapelski P, Skibińska M, Hauser J. [Family based association study of MMP-9 gene-1562C>T polymorphism in schizophrenia]. Psychiatr Pol. 2011;45:317-324.
50. Wiera G, Wozniak G, Bajor M, Kaczmarek L, Mozrzymas JW. Maintenance of long-term potentiation in hippocampal mossy fiber-CA3 pathway requires fine-tuned MMP-9 proteolytic activity. Hippocampus. 2013;23:529-543.
51. Yamamori H, Hashimoto R, Ishima T, et al. Plasma levels of mature brain-derived neurotrophic factor (BDNF) and matrix metalloproteinase-9 (MMP-9) in treatment-resistant schizophrenia treated with clozapine. Neurosci Lett. 2013;556:37-41.
52. Favalli G, Li J, Belmonte-de-Abreu P, Wong AH, Daskalakis ZJ. The role of BDNF in the pathophysiology and treatment of schizophrenia. J Psychiatr Res. 2012;46:1-11.
53. Niitsu T, Ishima T, Yoshida T, et al. A positive correlation between serum levels of mature brain-derived neurotrophic factor and negative symptoms in schizophrenia. Psychiatry Res. 2014;215:268-273.
54. Chang SH, Chiang SY, Chiu CC, et al. Expression of anti-cardiolipin antibodies and inflammatory associated factors in patients with schizophrenia. Psychiatry Res. 2011;187:341-346.
55. Kumarasinghe N, Beveridge NJ, Gardiner E, et al. Gene expression profiling in treatment-naive schizophrenia patients identifies abnormalities in biological pathways involving AKT1 that are corrected by antipsychotic medication. Int J Neuropsychopharmacol. 2013;16:1483-1503.
56. Tsilibary E, Tzinia A, Radenovic L, et al. Neural ECM proteases in learning and synaptic plasticity. Prog Brain Res. 2014;214:135-157.
57. Lin CY, Sawa A, Jaaro-Peled H. Better understanding of mechanisms of schizophrenia and bipolar disorder: from human gene expression profiles to mouse models. Neurobiol Dis. 2012;45:48-56.
58. Fromer M, Pocklington AJ, Kavanagh DH, et al. De novo mutations in schizophrenia implicate synaptic networks. Nature. 2014;506:179-184.
59. Maćkowiak M, Mordalska P, Wędzony K. Neuroligins, synapse balance and neuropsychiatric disorders. Pharmacol Rep. 2014;66:830-835.
60. Peixoto RT, Kunz PA, Kwon H, et al. Transsynaptic signaling by activity-dependent cleavage of neuroligin-1. Neuron. 2012;76:396-409.
61. Meyer-Lindenberg A, Tost H. Neural mechanisms of social risk for psychiatric disorders. Nat Neurosci. 2012;15:663-668.
62. Malaspina D, Goetz RR, Friedman JH, et al. Traumatic brain injury and schizophrenia in members of schizophrenia and bipolar disorder pedigrees. Am J Psychiatry. 2001;158:440-446.
63. van der Kooij MA, Fantin M, Rejmak E, et al. Role for MMP-9 in stress-induced downregulation of nectin-3 in hippocampal CA1 and associated behavioural alterations. Nat Commun. 2014;5:4995.
64. Hayashi T, Kaneko Y, Yu S, et al. Quantitative analyses of matrix metalloproteinase activity after traumatic brain injury in adult rats. Brain Res. 2009;1280:172-177.
65. Oya K, Kishi T, Iwata N. Efficacy and tolerability of minocycline augmentation therapy in schizophrenia: a systematic review and meta-analysis of randomized controlled trials. Hum Psychopharmacol. 2014;29:483-491.
66. Fujita Y, Ishima T, Kunitachi S, et al. Phencyclidine-induced cognitive deficits in mice are improved by subsequent subchronic administration of the antibiotic drug minocycline. Prog Neuropsychopharmacol Biol Psychiatry. 2008;32:336-339.
67. Levkovitz Y, Mendlovich S, Riwkes S, et al. A double-blind, randomized study of minocycline for the treatment of negative and cognitive symptoms in early-phase schizophrenia. J Clin Psychiatry. 2010;71:138-149.
68. Liu F, Guo X, Wu R, et al. Minocycline supplementation for treatment of negative symptoms in early-phase schizophrenia: a double blind, randomized, controlled trial. Schizophr Res. 2014;153:169-176.
69. Chopra K, Baveja A, Kuhad A. MMPs: a novel drug target for schizophrenia. Expert Opin Ther Targets. 2014:1-9.