Synaptically released matrix metalloproteinase activity in control of structural plasticity and the cell surface distribution of GluA1-AMPA receptors

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Szepesi, Zsuzsanna ^a   Hosy, Eric ^b   Ruszczycki, Blazej ^a   Bijata, Monika ^a   Pyskaty, Marta ^a   Bikbaev, Arthur ^c   Heine, Martin ^c   Choquet, Daniel ^b   Kaczmarek, Leszek ^a   Wlodarczyk, Jakub ^a  

^a NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

^b University of Bordeaux   (France)

^c LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMATE RECEPTOR; MATRIX METALLOPROTEINASE; AMPA RECEPTOR; GLUTAMATE RECEPTOR IONOTROPIC, AMPA 1;

ANIMAL CELL; ARTICLE; BIOACCUMULATION; CELL FUNCTION; CELL SURFACE; CONTROLLED STUDY; DENDRITIC SPINE; ENZYME ACTIVITY; ENZYME RELEASE; FUNCTIONAL MORPHOLOGY; HIPPOCAMPUS; LONG TERM POTENTIATION; MICROSCOPY; NERVE CELL PLASTICITY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RAT; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; ADULT; ANIMAL; CELL CULTURE; CELL MEMBRANE; ENZYMOLOGY; HUMAN; METABOLISM; SYNAPSE; WISTAR RAT;

ADULT; ANIMALS; CELL MEMBRANE; CELLS, CULTURED; HUMANS; MATRIX METALLOPROTEINASES; NEURONAL PLASTICITY; RATS, WISTAR; RECEPTORS, AMPA; SYNAPSES;

EID: 84901338723     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0098274     Document Type: Article

References (95)

1. Holtmaat A, Svoboda K (2009) Experience-dependent structural synaptic plasticity in the mammalian brain. Nat Rev Neurosci 10: 647-658.
2. Kasai H, Fukuda M, Watanabe S, Hayashi-Takagi A, Noguchi J (2010) Structural dynamics of dendritic spines in memory and cognition. Trends Neurosci 33: 121-129.
3. Yuste R, Bonhoeffer T (2001) Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu Rev Neurosci 24: 1071-1089. (Pubitemid 32695254)
4. Xu T, Yu X, Perlik AJ, Tobin WF, Zweig JA, et al. (2009) Rapid formation and selective stabilization of synapses for enduring motor memories. Nature 462: 915-919.
5. Yang G, Pan F, Gan WB (2009) Stably maintained dendritic spines are associated with lifelong memories. Nature 462: 920-924.
6. Caroni P, Donato F, Muller D (2012) Structural plasticity upon learning: regulation and functions. Nat Rev Neurosci 13: 478-490.
7. Penzes P, Cahill ME, Jones KA, VanLeeuwen JE, Woolfrey KM (2011) Dendritic spine pathology in neuropsychiatric disorders. Nat Neurosci 14: 285-293.
8. Levenga J, Willemsen R (2012) Perturbation of dendritic protrusions in intellectual disability. Prog Brain Res 197: 153-168.
9. Hutsler JJ, Zhang H (2010) Increased dendritic spine densities on cortical projection neurons in autism spectrum disorders. Brain Res 1309: 83-94.
10. Irwin SA, Patel B, Idupulapati M, Harris JB, Crisostomo RA, et al. (2001) Abnormal dendritic spine characteristics in the temporal and visual cortices of patients with fragile-X syndrome: a quantitative examination. Am J Med Genet 98: 161-167. (Pubitemid 32051804)
11. Sweet RA, Henteleff RA, Zhang W, Sampson AR, Lewis DA (2009) Reduced dendritic spine density in auditory cortex of subjects with schizophrenia. Neuropsychopharmacology 34: 374-389.
12. DeKosky ST, Scheff SW (1990) Synapse loss in frontal cortex biopsies in Alzheimer's disease: correlation with cognitive severity. Ann Neurol 27: 457-464. (Pubitemid 20149963)
13. Knobloch M, Mansuy IM (2008) Dendritic spine loss and synaptic alterations in Alzheimer's disease. Mol Neurobiol 37: 73-82.
14. Selemon LD, Begovic A, Goldman-Rakic PS, Castner SA (2007) Amphetamine sensitization alters dendritic morphology in prefrontal cortical pyramidal neurons in the non-human primate. Neuropsychopharmacology 32: 919-931. (Pubitemid 46426180)
15. Kharazia VN, Weinberg RJ (1999) Immunogold localization of AMPA and NMDA receptors in somatic sensory cortex of albino rat. J Comp Neurol 412: 292-302. (Pubitemid 29395366)
16. Nusser Z, Lujan R, Laube G, Roberts JD, Molnar E, et al. (1998) Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus. Neuron 21: 545-559. (Pubitemid 28475506)
17. Takumi Y, Ramirez-Leon V, Laake P, Rinvik E, Ottersen OP (1999) Different modes of expression of AMPA and NMDA receptors in hippocampal synapses. Nat Neurosci 2: 618-624. (Pubitemid 30491212)
18. Barry MF, Ziff EB (2002) Receptor trafficking and the plasticity of excitatory synapses. Curr Opin Neurobiol 12: 279-286. (Pubitemid 34615753)
19. Anggono V, Huganir RL (2012) Regulation of AMPA receptor trafficking and synaptic plasticity. Curr Opin Neurobiol 22: 461-469.
20. Esteban JA (2008) Intracellular machinery for the transport of AMPA receptors. Br J Pharmacol 153 Suppl 1: S35-43.
21. Henley JM, Wilkinson KA (2013) AMPA receptor trafficking and the mechanisms underlying synaptic plasticity and cognitive aging. Dialogues Clin Neurosci 15: 11-27.
22. Kessels HW, Malinow R (2009) Synaptic AMPA receptor plasticity and behavior. Neuron 61: 340-350.
23. Makino H, Malinow R (2009) AMPA receptor incorporation into synapses during LTP: the role of lateral movement and exocytosis. Neuron 64: 381-390.
24. Malinow R, Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25: 103-126. (Pubitemid 34748013)
25. Shepherd JD, Huganir RL (2007) The cell biology of synaptic plasticity: AMPA receptor trafficking. Annu Rev Cell Dev Biol 23: 613-643.
26. Yu SY, Wu DC, Liu L, Ge Y, Wang YT (2008) Role of AMPA receptor trafficking in NMDA receptor-dependent synaptic plasticity in the rat lateral amygdala. J Neurochem 106: 889-899.
27. Rumpel S, LeDoux J, Zador A, Malinow R (2005) Postsynaptic receptor trafficking underlying a form of associative learning. Science 308: 83-88. (Pubitemid 40471002)
28. Humeau Y, Reisel D, Johnson AW, Borchardt T, Jensen V, et al. (2007) A pathway-specific function for different AMPA receptor subunits in amygdala long-term potentiation and fear conditioning. J Neurosci 27: 10947-10956. (Pubitemid 47574151)
29. Mokin M, Zheng Z, Keifer J (2007) Conversion of silent synapses into the active pool by selective GluR1-3 and GluR4 AMPAR trafficking during in vitro classical conditioning. J Neurophysiol 98: 1278-1286. (Pubitemid 47435881)
30. Reisel D, Bannerman DM, Schmitt WB, Deacon RM, Flint J, et al. (2002) Spatial memory dissociations in mice lacking GluR1. Nat Neurosci 5: 868-873. (Pubitemid 34976652)
31. Lee HK, Takamiya K, Han JS, Man H, Kim CH, et al. (2003) Phosphorylation of the AMPA receptor GluR1 subunit is required for synaptic plasticity and retention of spatial memory. Cell 112: 631-643. (Pubitemid 36331776)
32. Dityatev A, Rusakov DA (2011) Molecular signals of plasticity at the tetrapartite synapse. Curr Opin Neurobiol 21: 353-359.
33. Nagase H, Woessner JF, Jr. (1999) Matrix metalloproteinases. J Biol Chem 274: 21491-21494. (Pubitemid 129519680)
34. Michaluk P, Kaczmarek L (2007) Matrix metalloproteinase-9 in glutamate-dependent adult brain function and dysfunction. Cell Death Differ 14: 1255-1258. (Pubitemid 46969864)
35. Mott JD, Werb Z (2004) Regulation of matrix biology by matrix metalloproteinases. Curr Opin Cell Biol 16: 558-564. (Pubitemid 39201241)
36. Sternlicht MD, Werb Z (2001) How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 17: 463-516. (Pubitemid 33096184)
37. Ethell IM, Ethell DW (2007) Matrix metalloproteinases in brain development and remodeling: synaptic functions and targets. J Neurosci Res 85: 2813-2823. (Pubitemid 47523564)
38. Bozdagi O, Nagy V, Kwei KT, Huntley GW (2007) In vivo roles for matrix metalloproteinase-9 in mature hippocampal synaptic physiology and plasticity. J Neurophysiol 98: 334-344. (Pubitemid 47084824)
39. Nagy V, Bozdagi O, Matynia A, Balcerzyk M, Okulski P, et al. (2006) Matrix metalloproteinase-9 is required for hippocampal late-phase long-term potentiation and memory. J Neurosci 26: 1923-1934.
40. Okulski P, Jay TM, Jaworski J, Duniec K, Dzwonek J, et al. (2007) TIMP-1 abolishes MMP-9-dependent long-lasting long-term potentiation in the prefrontal cortex. Biol Psychiatry 62: 359-362. (Pubitemid 47454516)
41. Huntley GW (2012) Synaptic circuit remodelling by matrix metalloproteinases in health and disease. Nat Rev Neurosci 13: 743-757.
42. Wang XB, Bozdagi O, Nikitczuk JS, Zhai ZW, Zhou Q, et al. (2008) Extracellular proteolysis by matrix metalloproteinase-9 drives dendritic spine enlargement and long-term potentiation coordinately. Proc Natl Acad Sci U S A 105: 19520-19525.
43. Bilousova TV, Dansie L, Ngo M, Aye J, Charles JR, et al. (2009) Minocycline promotes dendritic spine maturation and improves behavioural performance in the fragile X mouse model. J Med Genet 46: 94-102.
44. Michaluk P, Wawrzyniak M, Alot P, Szczot M, Wyrembek P, et al. (2011) Influence of matrix metalloproteinase MMP-9 on dendritic spine morphology. J Cell Sci 124: 3369-3380.
45. Xia Z, Dudek H, Miranti CK, Greenberg ME (1996) Calcium influx via the NMDA receptor induces immediate early gene transcription by a MAP kinase/ERK-dependent mechanism. J Neurosci 16: 5425-5436. (Pubitemid 26277871)
46. Otmakhov N, Khibnik L, Otmakhova N, Carpenter S, Riahi S, et al. (2004) Forskolin-induced LTP in the CA1 hippocampal region is NMDA receptor dependent. J Neurophysiol 91: 1955-1962. (Pubitemid 38500915)
47. Esposito A, Dohm CP, Kermer P, Bahr M, Wouters FS (2007) alpha-Synuclein and its disease-related mutants interact differentially with the microtubule protein tau and associate with the actin cytoskeleton. Neurobiol Dis 26: 521-531. (Pubitemid 46756322)
48. Yasumatsu N, Matsuzaki M, Miyazaki T, Noguchi J, Kasai H (2008) Principles of long-term dynamics of dendritic spines. J Neurosci 28: 13592-13608.
49. Goslin K, Banker G (1989) Experimental observations on the development of polarity by hippocampal neurons in culture. J Cell Biol 108: 1507-1516. (Pubitemid 19097054)
50. Tardin C, Cognet L, Bats C, Lounis B, Choquet D (2003) Direct imaging of lateral movements of AMPA receptors inside synapses. Embo J 22: 4656-4665. (Pubitemid 37162902)
51. Giannone G, Hosy E, Levet F, Constals A, Schulze K, et al. (2010) Dynamic superresolution imaging of endogenous proteins on living cells at ultra-high density. Biophys J 99: 1303-1310.
52. Kaech S, Banker G (2006) Culturing hippocampal neurons. Nat Protoc 5: 2406-2415.
53. Molnar E (2011) Long-term potentiation in cultured hippocampal neurons. Semin Cell Dev Biol 22: 506-513.
54. Oh MC, Derkach VA, Guire ES, Soderling TR (2006) Extrasynaptic membrane trafficking regulated by GluR1 serine 845 phosphorylation primes AMPA receptors for long-term potentiation. J Biol Chem 281: 752-758.
55. Niedringhaus M, Chen X, Dzakpasu R, Conant K (2012) MMPs and soluble ICAM-5 increase neuronal excitability within in vitro networks of hippocampal neurons. PLoS One 7: e42631.
56. Szepesi Z, Bijata M, Ruszczycki B, Kaczmarek L, Wlodarczyk J (2013) Matrix metalloproteinases regulate the formation of dendritic spine head protrusions during chemically induced long-term potentiation. PLoS One 8: e63314.
57. Kasai H, Matsuzaki M, Noguchi J, Yasumatsu N, Nakahara H (2003) Structure-stability-function relationships of dendritic spines. Trends Neurosci 26: 360-368. (Pubitemid 36794552)
58. Matsuzaki M, Honkura N, Ellis-Davies GC, Kasai H (2004) Structural basis of long-term potentiation in single dendritic spines. Nature 429: 761-766. (Pubitemid 38833127)
59. Kopec CD, Li B, Wei W, Boehm J, Malinow R (2006) Glutamate receptor exocytosis and spine enlargement during chemically induced long-term potentiation. J Neurosci 26: 2000-2009.
60. Wilczynski GM, Konopacki FA, Wilczek E, Lasiecka Z, Gorlewicz A, et al. (2008) Important role of matrix metalloproteinase 9 in epileptogenesis. J Cell Biol 180: 1021-1035. (Pubitemid 351398426)
61. Hosokawa T, Rusakov DA, Bliss TV, Fine A (1995) Repeated confocal imaging of individual dendritic spines in the living hippocampal slice: evidence for changes in length and orientation associated with chemically induced LTP. J Neurosci 15: 5560-5573.
62. Matsuzaki M, Ellis-Davies GC, Nemoto T, Miyashita Y, Iino M, et al. (2001) Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat Neurosci 4: 1086-1092. (Pubitemid 34116553)
63. Ostroff LE, Fiala JC, Allwardt B, Harris KM (2002) Polyribosomes redistribute from dendritic shafts into spines with enlarged synapses during LTP in developing rat hippocampal slices. Neuron 35: 535-545. (Pubitemid 34879951)
64. Dziembowska M, Wlodarczyk J (2012) MMP9: a novel function in synaptic plasticity. Int J Biochem Cell Biol 44: 709-13.
65. Wiera G, Wozniak G, Bajor M, Kaczmarek L, Mozrzymas JW (2013) Maintenance of long-term potentiation in hippocampal mossy fiber-CA3 pathway requires fine- tuned MMP-9 proteolytic activity. Hippocampus 23:529-43.
66. Selcher JC, Xu W, Hanson JE, Malenka RC, Madison DV (2012) Glutamate receptor subunit GluA1 is necessary for long-term potentiation and synapse unsilencing, but not long-term depression in mouse hippocampus. Brain Res 1435: 8-14.
67. Liao D, Scannevin RH, Huganir R (2001) Activation of silent synapses by rapid activity-dependent synaptic recruitment of AMPA receptors. J Neurosci 21: 6008-6017. (Pubitemid 32737734)
68. Sheng M, Kim MJ (2002) Postsynaptic signaling and plasticity mechanisms. Science 298: 776-780. (Pubitemid 35231521)
69. Bredt DS, Nicoll RA (2003) AMPA receptor trafficking at excitatory synapses. Neuron 40: 361-379. (Pubitemid 37244101)
70. Kielland A, Bochorishvili G, Corson J, Zhang L, Rosin DL, et al. (2009) Activity patterns govern synapse-specific AMPA receptor trafficking between deliverable and synaptic pools. Neuron 62: 84-101.
71. Conant K, Wang Y, Szklarczyk A, Dudak A, Mattson MP, et al. (2010) Matrix metalloproteinase-dependent shedding of intercellular adhesion molecule-5 occurs with long-term potentiation. Neuroscience 166: 508-521.
72. Lonskaya I, Partridge J, Lalchandani RR, Chung A, Lee T, et al. (2013) Soluble ICAM-5, a Product of Activity Dependent Proteolysis, Increases mEPSC Frequency and Dendritic Expression of GluA1. PLoS One 8: e69136.
73. Calo L, Cinque C, Patane M, Schillaci D, Battaglia G, et al. (2006) Interaction between ephrins/Eph receptors and excitatory amino acid receptors: possible relevance in the regulation of synaptic plasticity and in the pathophysiology of neuronal degeneration. J Neurochem 98: 1-10. (Pubitemid 43884705)
74. Adesnik H, Nicoll RA, England PM (2005) Photoinactivation of native AMPA receptors reveals their real-time trafficking. Neuron 48: 977-985. (Pubitemid 41814701)
75. Ashby MC, Maier SR, Nishimune A, Henley JM (2006) Lateral diffusion drives constitutive exchange of AMPA receptors at dendritic spines and is regulated by spine morphology. J Neurosci 26: 7046-7055. (Pubitemid 44309872)
76. Borgdorff AJ, Choquet D (2002) Regulation of AMPA receptor lateral movements. Nature 417: 649-653. (Pubitemid 34614823)
77. Ehlers MD, Heine M, Groc L, Lee MC, Choquet D (2007) Diffusional trapping of GluR1 AMPA receptors by input-specific synaptic activity. Neuron 54: 447-460. (Pubitemid 46659808)
78. Heine M, Groc L, Frischknecht R, Beique JC, Lounis B, et al. (2008) Surface mobility of postsynaptic AMPARs tunes synaptic transmission. Science 320: 201-205. (Pubitemid 351521410)
79. Passafaro M, Piech V, Sheng M (2001) Subunit-specific temporal and spatial patterns of AMPA receptor exocytosis in hippocampal neurons. Nat Neurosci 4: 917-926. (Pubitemid 32801595)
80. Yang Y, Wang XB, Frerking M, Zhou Q (2008) Delivery of AMPA receptors to perisynaptic sites precedes the full expression of long-term potentiation. Proc Natl Acad Sci U S A 105: 11388-11393.
81. Yudowski GA, Puthenveedu MA, Leonoudakis D, Panicker S, Thorn KS, et al. (2007) Real-time imaging of discrete exocytic events mediating surface delivery of AMPA receptors. J Neurosci 27: 11112-11121. (Pubitemid 47574153)
82. Opazo P, Sainlos M, Choquet D (2011) Regulation of AMPA receptor surface diffusion by PSD-95 slots. Curr Opin Neurobiol 22: 453-460.
83. Michaluk P, Mikasova L, Groc L, Frischknecht R, Choquet D, Kaczmarek L (2009) Matrix metalloproteinase-9 controls NMDA receptor surface diffusion through integrin beta1 signaling. J Neurosci. 29: 6007-12.
84. Dityatev A, Schachner M, Sonderegger P (2010) The dual role of the extracellular matrix in synaptic plasticity and homeconantostasis. Nat Rev Neurosci. 11: 735-46.
85. Tian L, Stefanidakis M, Ning L, Van Lint P, Nyman-Huttunen H, et al. (2007) Activation of NMDA receptors promotes dendritic spine development through MMP-mediated ICAM-5 cleavage. J Cell Biol 178: 687-700. (Pubitemid 47267279)
86. Conant K, Lonskaya I, Szklarczyk A, Krall C, Steiner J, et al. (2011) Methamphetamine-associated cleavage of the synaptic adhesion molecule intercellular adhesion molecule-5. J Neurochem. 118: 521-32.
87. Nair D, Hosy E, Petersen JD, Constals A, Giannone G, et al. (2013) Super-Resolution Imaging Reveals That AMPA Receptors Inside Synapses Are Dynamically Organized in Nanodomains Regulated by PSD95. J Neurosci 33: 13204-13224.
88. Frischknecht R, Heine M, Perrais D, Seidenbecher CI, Choquet D, et al. (2009) Brain extracellular matrix affects AMPA receptor lateral mobility and short-term synaptic plasticity. Nat Neurosci 12: 897-904.
89. Peixoto RT, Kunz PA, Kwon H, Mabb AM, Sabatini BL, et al. (2012) Transsynaptic signaling by activity-dependent cleavage of neuroligin-1. Neuron 76: 396-409.
90. Kaufmann WE, Moser HW (2000) Dendritic anomalies in disorders associated with mental retardation. Cereb Cortex 10: 981-991.
91. Kulkarni VA, Firestein BL (2012) The dendritic tree and brain disorders. Mol Cell Neurosci 50: 10-20.
92. Kaczmarek L (2013) Mmp-9 inhibitors in the brain: can old bullets shoot new targets? Curr Pharm Des 19: 1085-1089.
93. Rybakowski JK, Remlinger-Molenda A, Czech-Kucharska A, Wojcicka M, Michalak M, et al. (2013) Increased serum matrix metalloproteinase-9 (MMP-9) levels in young patients during bipolar depression. J Affect Disord 146: 286-289.
94. Rybakowski JK, Skibinska M, Leszczynska-Rodziewicz A, Kaczmarek L, Hauser J (2009) Matrix metalloproteinase-9 gene modulates prefrontal cognition in bipolar men. Psychiatr Genet 19: 108-109.
95. Samochowiec A, Grzywacz A, Kaczmarek L, Bienkowski P, Samochowiec J, et al. (2010) Functional polymorphism of matrix metalloproteinase-9 (MMP-9) gene in alcohol dependence: family and case control study. Brain Res 1327: 103-106.