NMDA-receptor inhibition increases spine stability of denervated mouse dentate granule cells and accelerates spine density recovery following entorhinal denervation in vitro

Neurobiology of Disease

Volumn 59, Issue , 2013, Pages 267-276

  Vlachos, Andreas ^a   Helias, Moritz ^b,c   Becker, Denise ^a   Diesmann, Markus ^b,c   Deller, Thomas ^a  

^a GOETHE UNIVERSITY   (Germany)

^b FORSCHUNGSZENTRUM JÜLICH   (Germany)

^c RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

Amantadine; Entorhinal cortex lesion; Homeostatic synaptic plasticity; Memantine; Neurorestauration; Regeneration; Synaptic scaling

Indexed keywords

AMPA RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEAFFERENTATION; DENERVATION; DENTATE GRANULE CELL; ENTORHINAL CORTEX; EXCITATORY POSTSYNAPTIC POTENTIAL; GRANULE CELL; HIPPOCAMPAL CA1 REGION; HOMEOSTASIS; IN VITRO STUDY; MATHEMATICAL MODEL; MOUSE; NERVE CELL CULTURE; NERVE CELL PLASTICITY; NERVE FIBER; NONHUMAN; PREDICTION; PRIORITY JOURNAL; SPINE; SPINE DENSITY; SPINE STABILILITY; SURVIVAL;

AMANTADINE; ENTORHINAL CORTEX LESION; HOMEOSTATIC SYNAPTIC PLASTICITY; MEMANTINE; NEURORESTAURATION; REGENERATION; SYNAPTIC SCALING;

2-AMINO-5-PHOSPHONOVALERATE; 6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; COMPUTER SIMULATION; DENDRITIC SPINES; DENERVATION; DENTATE GYRUS; ENTORHINAL CORTEX; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; GABA ANTAGONISTS; GREEN FLUORESCENT PROTEINS; MALE; MICE; MICE, TRANSGENIC; MODELS, BIOLOGICAL; NEURONS; ORGAN CULTURE TECHNIQUES; PYRIDAZINES; RECEPTORS, N-METHYL-D-ASPARTATE; SODIUM CHANNEL BLOCKERS; TETRODOTOXIN;

EID: 84883286353     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2013.07.018     Document Type: Article

References (79)

1. Abuhassan K., Coyle D., Belatreche A., Maguire L. Compensating for synaptic loss in Alzheimer's disease. J. Comput. Neurosci. 2013, 10.1007/s10827-013-0462-8.
2. Becker D., Willems L.M., Vnencak M., Zahn N., Schuldt G., Jedlicka P., et al. Functional and structural properties of dentate granule cells with hilar basal dendrites in mouse entorhino-hippocampal slice cultures. PLoS One 2012, 7:e48500.
3. Blasco-Ibanez J.M., Freund T.F. Distribution, ultrastructure, and connectivity of calretinin-immunoreactive mossy cells of the mouse dentate gyrus. Hippocampus 1997, 7:307-320.
4. Bonhoeffer T., Yuste R. Spine motility. Phenomenology, mechanisms, and function. Neuron 2002, 35:1019-1027.
5. Bourne J.N., Harris K.M. Coordination of size and number of excitatory and inhibitory synapses results in a balanced structural plasticity along mature hippocampal CA1 dendrites during LTP. Hippocampus 2011, 21:354-373.
6. Bourne J.N., Chirillo M.A., Harris K.M. Presynaptic ultrastructural plasticity along CA3→CA1 axons during LTP in mature hippocampus. J. Comp. Neurol. 2013, (in press). 10.1002/cne.23384.
7. Branco T., Staras K., Darcy K.J., Goda Y. Local dendritic activity sets release probability at hippocampal synapses. Neuron 2008, 59:475-485.
8. Caceres A., Steward O. Dendritic reorganization in the denervated dentate gyrus of the rat following entorhinal cortical lesions: a Golgi and electron microscopic analysis. J. Comp. Neurol. 1983, 136:287-295.
9. Cormier R.J., Greenwood A.C., Connor J.A. Bidirectional synaptic plasticity correlated with the magnitude of dendritic calcium transients above a threshold. J. Neurophysiol. 2001, 85:399-406.
10. De Roo M., Klauser P., Muller D. LTP promotes a selective long-term stabilization and clustering of dendritic spines. PLoS Biol. 2008, 6:e219.
11. Del Turco D., Deller T. Organotypic entorhino-hippocampal slice cultures-a tool to study the molecular and cellular regulation of axonal regeneration and collateral sprouting in vitro. Methods Mol. Biol. 2007, 399:55-66.
12. Deller T., Frotscher M. Lesion-induced plasticity of central neurons: sprouting of single fibres in the rat hippocampus after unilateral entorhinal cortex lesion. Prog. Neurobiol. 1997, 53:687-727.
13. Deller T., Frotscher M., Nitsch R. Sprouting of crossed entorhinodentate fibers after a unilateral entorhinal lesion: anterograde tracing of fiber reorganization with Phaseolus vulgaris-leucoagglutinin (PHAL). J. Comp. Neurol. 1996, 365:42-55.
14. Deller T., Bas Orth C., Vlachos A., Merten T., Del Turco D., Dehn D., et al. Plasticity of synaptopodin and the spine apparatus organelle in the rat fascia dentata following entorhinal cortex lesion. J. Comp. Neurol. 2006, 499:471-484.
15. Dinocourt C., Aungst S., Yang K., Thompson S.M. Homeostatic increase in excitability in area CA1 after Schaffer collateral transection in vivo. Epilepsia 2011, 52:1656-1665.
16. Drojdahl N., Hegelund I.V., Poulsen F.R., Wree A., Finsen B. Perforant path lesioning induces sprouting of CA3-associated fibre systems in mouse hippocampal formation. Exp. Brain Res. 2002, 144:79-87.
17. Emre M., Tsolaki M., Bonuccelli U., Destee A., Tolosa E., Kutzelnigg A., et al. Memantine for patients with Parkinson's disease dementia or dementia with Lewy bodies: a randomised, double-blind, placebo-controlled trial. Lancet Neurol. 2010, 9:969-977.
18. Farlow M.R., Cummings J.L. Effective pharmacologic management of Alzheimer's disease. Am. J. Med. 2007, 120:388-397.
19. Feng G., Mellor R.H., Bernstein M., Keller-Peck C., Nguyen Q.T., Wallace M., et al. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 2000, 28:41-51.
20. Gewaltig M.-O., Diesmann M. NEST (neural simulation tool). Scholarpedia 2007, 2:1430.
21. Giacino J.T., Whyte J., Bagiella E., Kalmar K., Childs N., Khademi A., et al. Placebo-controlled trial of amantadine for severe traumatic brain injury. N. Engl. J. Med. 2012, 366:819-826.
22. Gianutsos G., Chute S., Dunn J.P. Pharmacological changes in dopaminergic systems induced by long-term administration of amantadine. Eur. J. Pharmacol. 1985, 110:357-361.
23. Halpain S., Hipolito A., Saffer L. Regulation of F-actin stability in dendritic spines by glutamate receptors and calcineurin. J. Neurosci. 1998, 18:9835-9844.
24. Helias M., Rotter S., Gewaltig M.O., Diesmann M. Structural plasticity controlled by calcium based correlation detection. Front. Comput. Neurosci. 2008, 2:7. 10.3389/neuro.10.007.2008.
25. Hill T.C., Zito K. LTP-induced long-term stabilization of individual nascent dendritic spines. J. Neurosci. 2013, 33:678-686.
26. Holtmaat A., Bonhoeffer T., Chow D.K., Chuckowree J., De Paola V., Hofer S.B., et al. Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window. Nat. Protoc. 2009, 4:1128-1144.
27. Hou Q., Zhang D., Jarzylo L., Huganir R.L., Man H.Y. Homeostatic regulation of AMPA receptor expression at single hippocampal synapses. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:775-780.
28. Jahr C.E., Stevens C.F. Glutamate activates multiple single channel conductances in hippocampal neurons. Nature 1987, 325:522-525.
29. Jones E., Oliphant T., Peterson P. SciPy: open source scientific tools for Python Available at:. http://www.scipy.org/.
30. Kasai H., Fukuda M., Watanabe S., Hayashi-Takagi A., Noguchi J. Structural dynamics of dendritic spines in memory and cognition. Trends Neurosci. 2010, 33:121-129.
31. Kim J., Tsien R.W. Synapse-specific adaptations to inactivity in hippocampal circuits achieve homeostatic gain control while dampening network reverberation. Neuron 2008, 58:925-937.
32. Kraus M.F., Smith G.S., Butters M., Donnell A.J., Dixon E., Yilong C., et al. Effects of the dopaminergic agent and NMDA receptor antagonist amantadine on cognitive function, cerebral glucose metabolism and D2 receptor availability in chronic traumatic brain injury: a study using positron emission tomography (PET). Brain Inj. 2005, 19:471-479.
33. Lee K.J., Queenan B.N., Rozeboom A.M., Bellmore R., Lim S.T., Vicini S., et al. Mossy fiber-CA3 synapses mediate homeostatic plasticity in mature hippocampal neurons. Neuron 2013, 77:99-114.
34. Lippman J., Dunaevsky A. Dendritic spine morphogenesis and plasticity. J. Neurobiol. 2005, 64:47-57.
35. Lüscher C., Noicoll R., Malenka R., Muller D. Synaptic plasticity and dynamic modulation of the postsynaptic membrane. Nat. Neurosci. 2000, 3:545-550.
36. 2+ of NMDA responses in spinal cord neurones. Nature 1984, 309:261-263.
37. McKinney R.A., Capogna M., Durr R., Gahwiler B.H., Thompson S.M. Miniature synaptic events maintain dendritic spines via AMPA receptor activation. Nat. Neurosci. 1999, 2:44-49.
38. Mitra A., Mitra S.S., Tsien R.W. Heterogeneous reallocation of presynaptic efficacy in recurrent excitatory circuits adapting to inactivity. Nat. Neurosci. 2012, 15:250-257.
39. Müller C.M., Vlachos A., Deller T. Calcium homeostasis of acutely denervated and lesioned dentate gyrus in organotypic entorhino-hippocampal co-cultures. Cell Calcium 2010, 47:242-252.
40. Nagerl U.V., Kostinger G., Anderson J.C., Martin K.A., Bonhoeffer T. Protracted synaptogenesis after activity-dependent spinogenesis in hippocampal neurons. J. Neurosci. 2007, 27:8149-8156.
41. 2+ signals evoked by coincident EPSPs and backpropagating action potentials in spiny stellate cells of layer 4 in the juvenile rat somatosensory barrel cortex. J. Neurosci. 2004, 24:1689-1699.
42. Nevian T., Sakmann B. Spine Ca signaling in spike-timing dependent plasticity. J. Neurosci. 2006, 26:11001-11013.
43. Nimchinsky E.A., Sabatini B.L., Svoboda K. Structure and function of dendritic spines. Annu. Rev. Physiol. 2002, 64:313-353.
44. Nowak L., Bregestovski P., Ascher P., Herbet A., Prochiantz A. Magnesium gates glutamate-activated channels in mouse central neurones. Nature 1984, 307:462-465.
45. Oh W.C., Hill T.C., Zito K. Synapse-specific and size-dependent mechanisms of spine structural plasticity accompanying synaptic weakening. Proc. Natl. Acad. Sci. U. S. A 2012, 10.1073/pnas.1214705110.
46. Parnavelas J.G., Lynch G., Brecha N., Cotman C.W., Globus A. Spine loss and regrowth in hippocampus following deafferentation. Nature 1974, 248:71-73.
47. Parsons C.G., Stoffler A., Danysz W. Memantine: a NMDA receptor antagonist that improves memory by restoration of homeostasis in the glutamatergic system-too little activation is bad, too much is even worse. Neuropharmacology 2007, 53:699-723.
48. Peixoto R.T., Kunz P.A., Kwon H., Mabb A.M., Sabatini B.L., Philpot B.D., et al. Transsynaptic signaling by activity-dependent cleavage of neuroligin-1. Neuron 2012, 76:396-409.
49. Penzes P., Cahill M.E., Jones K.A., VanLeeuwen J.E., Woolfrey K.M. Dendritic spine pathology in neuropsychiatric disorders. Nat. Neurosci. 2011, 14:285-293.
50. Perederiy J.V., Westbrook G.L. Structural plasticity in the dentate gyrus - revisiting a classic injury model. Front. Neural Circuits 2013, 7:17. 10.3389/fncir.2013.00017.
51. Perederiy J.V., Luikart B.W., Washburn E.K., Schnell E., Westbrook G.L. Neural injury alters proliferation and integration of adult-generated neurons in the dentate gyrus. J. Neurosci. 2013, 33:4754-4767.
52. Prang P., Del Turco D., Deller T. Associational sprouting in the mouse fascia dentata after entorhinal lesion in vitro. Brain Res. 2003, 978:205-212.
53. Rabinowitch I., Segev I. The endurance and selectivity of spatial patterns of long-term potentiation/depression in dendrites under homeostatic synaptic plasticity. J. Neurosci. 2006, 26:13474-13484.
54. Rabinowitch I., Segev I. The interplay between homeostatic synaptic plasticity and functional dendritic compartments. J. Neurophysiol. 2006, 96:276-283.
55. Rabinowitch I., Segev I. Two opposing plasticity mechanisms pulling a single synapse. Trends Neurosci. 2008, 31:377-383.
56. Reeves T.M., Steward O. Changes in the firing properties of neurons in the dentate gyrus with denervation and reinnervation: implications for behavioral recovery. Exp. Neurol. 1988, 102:37-49.
57. Roselli F., Tirard M., Lu J., Hutzler P., Lamberti P., Livrea P., et al. Soluble beta-amyloid1-40 induces NMDA-dependent degradation of postsynaptic density-95 at glutamatergic synapses. J. Neurosci. 2005, 25:11061-11070.
58. Roselli F., Hutzler P., Wegerich Y., Livrea P., Almeida O.F. Disassembly of shank and homer synaptic clusters is driven by soluble beta-amyloid(1-40) through divergent NMDAR-dependent signalling pathways. PLoS One 2009, 4:e6011.
59. Savin C., Triesch J., Meyer-Hermann M. Epileptogenesis due to glia-mediated synaptic scaling. J. R. Soc. Interface 2009, 6:655-668.
60. Segal M., Andersen P. Dendritic spines shaped by synaptic activity. Curr. Opin. Neurobiol. 2000, 10:582-586.
61. Small D.H. Mechanisms of synaptic homeostasis in Alzheimer's disease. Curr. Alzheimer Res. 2004, 1:27-32.
62. Small D.H. Do acetylcholinesterase inhibitors boost synaptic scaling in Alzheimer's disease?. Trends Neurosci. 2004, 27:245-249.
63. Steward O. Reorganization of neuronal circuitry following central nervous system trauma: naturally occurring processes and opportunities for therapeutic intervention. The Neurobiology of Central Nervous System Trauma 1994, 266-287. Oxford University Press, New York. S.K. Salzman, A.I. Faden (Eds.).
64. Steward O., Cotman C.W., Lynch G.S. Re-establishment of electrophysiologically functional entorhinal cortical input to the dentate gyrus deafferented by ipsilateral entorhinal lesions: innervation by the contralateral entorhinal cortex. Exp. Brain Res. 1973, 18:396-414.
65. Steward O., Cotman C.W., Lynch G.S. Growth of a new fiber projection in the brain of adult rats: re-innervation of the dentate gyrus by the contralateral entorhinal cortex following ipsilateral entorhinal lesions. Exp. Brain Res. 1974, 20:45-66.
66. Sutton M.A., Ito H.T., Cressy P., Kempf C., Woo J.C., Schuman E.M. Miniature neurotransmission stabilizes synaptic function via tonic suppression of local dendritic protein synthesis. Cell 2006, 125:785-799.
67. Trasande C.A., Ramirez J.M. Activity deprivation leads to seizures in hippocampal slice cultures: is epilepsy the consequence of homeostatic plasticity?. J. Clin. Neurophysiol. 2007, 24:154-164.
68. Turrigiano G. Homeostatic synaptic plasticity: local and global mechanisms for stabilizing neuronal function. Cold Spring Harb. Perspect. Biol. 2012, 4:a005736.
69. Turrigiano G.G., Nelson S.B. Homeostatic plasticity in the developing nervous system. Nat. Rev. Neurosci. 2004, 5:97-107.
70. Vitureira N., Letellier M., Goda Y. Homeostatic synaptic plasticity: from single synapses to neural circuits. Curr. Opin. Neurobiol. 2012, 22:516-521.
71. Vlachos A., Orth C.B., Schneider G., Deller T. Time-lapse imaging of granule cells in mouse entorhino-hippocampal slice cultures reveals changes in spine stability after entorhinal denervation. J. Comp. Neurol. 2012, 520:1891-1902.
72. Vlachos A., Becker D., Jedlicka P., Winkels R., Roeper J., Deller T. Entorhinal denervation induces homeostatic synaptic scaling of excitatory postsynapses of dentate granule cells in mouse organotypic slice cultures. PLoS One 2012, 7:e32883.
73. Vlachos A., Ikenberg B., Lenz M., Becker D., Reifenberg K., Bas Orth C., Deller T. Synaptopodin regulates denervation-induced homeostatic synaptic plasticity. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:8242-8247.
74. Vuksic M., Del Turco D., Bas Orth C., Burbach G.J., Feng G., Muller C.M., Schwarzacher S.W., Deller T. 3D-reconstruction and functional properties of GFP-positive and GFP-negative granule cells in the fascia dentata of the Thy1-GFP mouse. Hippocampus 2008, 18:364-375.
75. Vuksic M., Del Turco D., Vlachos A., Schuldt G., Muller C.M., Schneider G., et al. Unilateral entorhinal denervation leads to long-lasting dendritic alterations of mouse hippocampal granule cells. Exp. Neurol. 2011, 230:176-185.
76. Wang G., Gilbert J., Man H.Y. AMPA receptor trafficking in homeostatic synaptic plasticity: functional molecules and signaling cascades. Neural Plast. 2012, 2012:825364.
77. Warren K.M., Reeves T.M., Phillips L.L. MT5-MMP, ADAM-10, and N-cadherin act in concert to facilitate synapse reorganization after traumatic brain injury. J. Neurotrauma 2012, 29:1922-1940.
78. Zito K., Scheuss V., Knott G., Hill T., Svoboda K. Rapid functional maturation of nascent dendritic spines. Neuron 2009, 61:247-258.
79. Zuo Y., Yang G., Kwon E., Gan W.B. Long-term sensory deprivation prevents dendritic spine loss in primary somatosensory cortex. Nature 2005, 436:261-265.