Minocycline promotes dendritic spine maturation and improves behavioural performance in the fragile X mouse model

Journal of Medical Genetics

Volumn 46, Issue 2, 2009, Pages 94-102

  Bilousova, T V ^a   Dansie, L ^a   Ngo, M ^a   Aye, J ^a   Charles, J R ^a   Ethell, D W ^a   Ethell, I M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GELATINASE B; MINOCYCLINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; AUTISM; COGNITION; CONTROLLED STUDY; DENDRITIC SPINE; DRUG MECHANISM; FRAGILE X SYNDROME; HIPPOCAMPUS; KNOCKOUT MOUSE; MAZE TEST; MENTAL DEFICIENCY; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; BEHAVIOR, ANIMAL; DENDRITIC SPINES; DISEASE MODELS, ANIMAL; FRAGILE X MENTAL RETARDATION PROTEIN; FRAGILE X SYNDROME; GENE KNOCKOUT TECHNIQUES; HIPPOCAMPUS; MATRIX METALLOPROTEINASE 9; MICE; MINOCYCLINE; MOTOR ACTIVITY; NEURONS;

ANIMALIA; MUS;

EID: 62149089881     PISSN: 00222593     EISSN: 14686244     Source Type: Journal    
DOI: 10.1136/jmg.2008.061796     Document Type: Article

References (47)

1. Hagerman RJ. The physical and behavioral phenotype. In: Hagerman RJ, Hagerman PJ, eds. Fragile X syndrome: diagnosis, treatment and research. Baltimore: The Johns Hopkins University Press, 2002:3-109.
2. Musumeci SA, Hagerman RJ, Ferri R, Bosco P, Dalla Bernardina B, Tassinari CA, De Sarro, GB, Elia M. Epilepsy and EEG findings in males with fragile X syndrome. Epilepsia 1999;40:1092-9.
3. Greenough WT, Klintsova AY, Irwin SA, Galvez R, Bates KE, Weiler IJ. Synaptic regulation of protein synthesis and the fragile X protein. Proc Natl Acad Sci USA 2001;98:7101-6.
4. Brown V, Jin P, Ceman S, Darnell JC, O'Donnell WT, Tenenbaum SA, Jin X, Feng Y, Wilkinson KD, Keene JD, Darnell RB, Warren ST. Microarray identification of FMRP-associated brain mRNAs and altered mRNA translational profiles in fragile X syndrome. Cell 2001;107:477-87.
5. Feng Y, Absher D, Eberhart DE, Brown V, Malter HE, Warren ST. FMRP associates with polyribosomes as an mRNP, and the I304N mutation of severe fragile X syndrome abolishes this association. Mol Cell 1997;1:109-18.
6. Todd PK, Mack KJ, Malter JS. The fragile X mental retardation protein is required for type-l metabotropic glutamate receptor-dependent translation of PSD-95. Proc Natl Acad Sci USA 2003;100:14374-8.
7. Yan QJ, Rammal M, Tranfaglia M, Bauchwitz RP. Suppression of two major Fragile X Syndrome mouse model phenotypes by the mGluR5 antagonist MPEP. Neuropharmacology 2005;49:1053-66.
8. Rudelli RD, Brown WT, Wisniewski K, Jenkins EC, Laure-Kamionowska M, Connell F, Wisniewski HM. Adult fragile X syndrome. Clinico-neuropathologic findings. Acta Neuropathol (Berl) 1985;67:289-95.
9. Kaufmann WE, Moser HW. Dendritic anomalies in disorders associated with mental retardation. Cereb Cortex 2000;10:981-91.
10. Harris KM. Structure, development, and plasticity of dendritic spines. Curr Opin Neurobiol 1999;9:343-8.
11. Yuste R, Bonhoeffer T. Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu Rev Neurosci 2001;24:1071-89.
12. Carlisle HJ, Kennedy MB. Spine architecture and synaptic plasticity. Trends Neurosci 2005;28:182-7.
13. Ziv NE, Smith SJ. Evidence for a role of dendritic filopodia in synaptogenesis and spine formation. Neuron 1996;17:91-102.
14. Marrs GS, Green SH, Dailey ME. Rapid formation and remodeling of postsynaptic densities in developing dendrites. Nat Neurosci 2001;4:1006-13.
15. Ethell IM, Pasquale EB. Molecular mechanisms of dendritic spine development and remodeling. Prog Neurobiol 2005;75:161-205.
16. Knott GW, Holtmaat A, Wilbrecht L, Welker E, Svoboda K. Spine growth precedes synapse formation in the adult neocortex in vivo. Nat Neurosci 2006;9:1117-24.
17. Comery TA, Harris JB, Willems PJ, Oostra BA, Irwin SA, Weiler IJ, Greenough WT. Abnormal dendritic spines in fragile X knockout mice: maturation and pruning deficits. Proc Natl Acad Sci USA 1997;94:5401-4.
18. Nimchinsky EA, Oberlander AM, Svoboda K. Abnormal development of dendritic spines in FMR1 knock-out mice. J Neurosci 2001;21:5139- 46.
19. Antar LN, Li C, Zhang H, Carroll RC, Bassell GJ. Local functions for FMRP in axon growth cone motility and activity-dependent regulation of filopodia and spine synapses. bMol Cell Neurosci 2006;32:37-48.
20. Grossman AW, Elisseou NM, McKinney BC, Greenough WT. Hippocampal pyramidal cells in adult Fmr1 knockout mice exhibit an immature-appearing profile of dendritic spines. Brain Res 2006;1084:158-64.
21. Vanderklish PW, Edelman GM. Dendritic spines elongate after stimulation of group 1 metabotropic glutamate receptors in cultured hippocampal neurons. Proc Natl Acad Sci USA 2002;99:1639-44.
22. Hayashi ML, Rao BS, Seo JS, Choi HS, Dolan BM, Choi SY, Chattarji S, Tonegawa S. Inhibition of p21-activated kinase rescues symptoms of fragile X syndrome in mice. Proc Natl Acad Sci USA 2007;104:11489-94.
23. Lee CZ, Yao JS, Huang Y, Zhai W, Liu W, Guglielmo BJ, Lin E, Yang GY, Young WL. Dose-response effect of tetracyclines on cerebral matrix metalloproteinase-9 after vascular endothelial growth factor hyperstimulation. J Cereb Blood Flow Metab 2006;26:1157-64.
24. Carobrez AP, Bertoglio LJ. Ethological and temporal analyses of anxiety-like behavior: the elevated plus-maze model 20 years on. Neurosci Biobehav Rev 2005;29:1193-205.
25. Hughes RN. The value of spontaneous alternation behavior (SAB) as a test of retention in pharmacological investigations of memory. Neurosci Biobehav Rev 2004;28:497-505.
26. Caley DW, Johnson C, Liebelt RA. The postnatal development of the retina in the normal and rodless CBA mouse: a light and electron microscopic study. Am J Anat 1972;133:179-212.
27. Wong AA, Brown RE. Visual detection, pattern discrimination and visual acuity in 14 strains of mice. Genes Brain Behav 2006;5:389-403.
28. Wu CC, Reilly JF, Young WG, Morrison JH, Bloom FE. High-throughput morphometric analysis of individual neurons. Cereb Cortex 2004;14:543-54.
29. Henkemeyer M, Itkis OS, Ngo M, Hickmott PW, Ethell IM. Multiple EphB receptor tyrosine kinases shape dendritic spines in the hippocampus. J Cell Biol 2003;163:1313-26.
30. Shi Y, Ethell IM. Integrins control dendritic spine plasticity in hippocampal neurons through NMDA receptor and CaMKII-mediated actin reorganization. J Neurosci 2006;26:1813-22.
31. Bilousova T, Rusakov DA, Ethell DW, Ethell IM. MMP-7 disrupts dendritic spines in hippocampal neurons through NMDA receptor activation. J Neurochem 2006;97:44-56.
32. Zhang JW, Gottschall PE. Zymographic measurement of gelatinase activity in brain tissue after detergent extraction and affinity-support purification. J Neurosci Methods 1997;76:15-20.
33. Ethell DW, Shippy D, Cao C, Cracchiolo JR, Runfeldt M, Blake B, Arendash GW. Abeta-specific T-cells reverse cognitive decline and synaptic loss in Alzheimer's mice. Neurobiol Dis 2006;23:351-61.
34. Fiala JC, Spacek J, Harris KM. Dendritic spine pathology: cause or consequence of neurological disorders? Brain Res Rev 2002;39:29-54.
35. Matsuzaki M, Ellis-Davies GC, Nemoto T, Miyashita Y, lino M, Kasai H. Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat Neurosci 2001;4:1086-92.
36. Matus A. Growth of dendritic spines: a continuing story. Curr Opin Neurobiol 2005;15:67-72.
37. Bear MF, Huber KM, Warren ST. The mGluR theory of fragile X mental retardation. Trends Neurosci 2004;27:370-7.
38. Huber KM, Gallagher SM, Warren ST, Bear MF. Altered synaptic plasticity in a mouse model of fragile X mental retardation. Proc Natl Acad Sci USA 2002;99:7746-50.
39. Bozdagi O, Nagy V, Kwei KT, Huntley GW. In vivo roles for matrix metalloproteinase-9 in mature hippocampal synaptic physiology and plasticity. J Neurophysiol 2007;98:334-44.
40. Ethell IM, Ethell DW. Matrix metalloproteinases in brain development and remodeling: synaptic functions and targets. J Neurosci Res 2007;85:2813-23.
41. Chavis P, Westbrook G. Integrins mediate functional pre- and postsynaptic maturation at a hippocampal synapse. Nature 2001;411:317-21.
42. Lin B, Arai AC, Lynch G, Gall CM. Integrins regulate NMDA receptor-mediated synaptic currents. J Neurophysiol 2003;89:2874- 8.
43. Lauterborn JC, Rex CS, Kramár E, Chen LY, Pandyarajan V, Lynch G, Gall CM. Brainderived neurotrophic factor rescues synaptic plasticity in a mouse model of fragile X syndrome. J Neurosci 2007;27:10685- 94.
44. Tikka T, Fiebich BL, Goldsteins G, Keinanen R, Koistinaho J. Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia. J Neurosci 2001;21:2580-8.
45. Chen M, Ona VO, Li M, Ferrante RJ, Fink KB, Zhu S, Bian J, Guo L, Farrell LA, Hersch SM, Hobbs W, Vonsattel JP, Cha JH, Friedlander RM. Minocycline inhibits caspase-1 and caspase-3 expression and delays mortality in a transgenic mouse model of Huntington disease. Nat Med 2000;6:797-801.
46. Zhu S, Stavrovskaya IG, Drozda M, Kim BY, Ona V, Li M, Sarang S, Liu AS, Hartley DM, Wu DC, Gullans S, Ferrante RJ, Przedborski S, Kristal BS, Friedlander RM. Minocycline inhibits cytochrome c release and delays progression of amyotrophic lateral sclerosis in mice. Nature 2002;417:74-8.
47. Zhang C, Lei B, Lam TT, Yang F, Sinha D, Tso MO. Neuroprotection of photoreceptors by minocycline in light-induced retinal degeneration. Invest Ophthalmol Vis Sci 2004;45:2753-9.