Hippocampal neuronal subtypes develop abnormal dendritic arbors in the presence of Fragile X astrocytes

Neuroscience

Volumn 324, Issue , 2016, Pages 202-217

  Jacobs, S ^a   Cheng, C ^a   Doering, L C ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

Arborization; Astrocyte; Dendrite; FMRP; Fragile X; Neuron

Indexed keywords

DREBRIN; GLUTAMATE DECARBOXYLASE 65; GLUTAMATE DECARBOXYLASE 67; MICROTUBULE ASSOCIATED PROTEIN 2; FMR1 PROTEIN, MOUSE; FRAGILE X MENTAL RETARDATION PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; MTAP2 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; ASTROCYTE; CELL ACTIVITY; CELL STRUCTURE; COCULTURE; CONTROLLED STUDY; DENDRITE; DENDRITIC ARBORIZATION; FEMALE; FRAGILE X ASTROCYTE; HIPPOCAMPAL NEURONAL CULTURE; IMMUNOCYTOCHEMISTRY; MALE; MOUSE; NERVE CELL CHARACTERISTICS AND FUNCTIONS; NEUROANATOMY; NONHUMAN; PRIORITY JOURNAL; WILD TYPE; 129 MOUSE; ANIMAL; CELL CULTURE; CYTOLOGY; DISEASE MODEL; FRAGILE X SYNDROME; GENETICS; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; METABOLISM; NERVE CELL; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; TIME FACTOR;

ANIMALS; ASTROCYTES; CELLS, CULTURED; COCULTURE TECHNIQUES; DENDRITES; DISEASE MODELS, ANIMAL; FEMALE; FRAGILE X MENTAL RETARDATION PROTEIN; FRAGILE X SYNDROME; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; MICE, 129 STRAIN; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; NEURONS; TIME FACTORS;

EID: 84961793507     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2016.03.011     Document Type: Article

References (49)

1. Abbott L.F., Nelson S.B. Synaptic plasticity: taming the beast. Nat Neurosci 2000, 3(Suppl.):1178-1183.
2. Abekhoukh S., Bardoni B. CYFIP family proteins between autism and intellectual disability: links with Fragile X syndrome. Front Cell Neurosci 2014.
3. Allen N.J. Role of glia in developmental synapse formation. Curr Opin Neurobiol 2013, 23:1027-1033.
4. Ballas N., Lioy D.T., Grunseich C., Mandel G. Non-cell autonomous influence of MeCP2-deficient glia on neuronal dendritic morphology. Nat Neurosci 2009, 12:311-317.
5. Banker G.A. Trophic interactions between astroglial cells and hippocampal neurons in culture. Science 1980, 209:809-810.
6. Banker G.A., Cowan W.M. Further observations on hippocampal neurons in dispersed cell culture. J Comp Neurol 1979, 187:469-493.
7. Baptista M.S., Melo C.V., Armelão M., Herrmann D. Role of the proteasome in excitotoxicity-induced cleavage of glutamic acid decarboxylase in cultured hippocampal neurons. PLoS One 2010.
8. Beckel-Mitchener A., Greenough W.T. Correlates across the structural, functional, and molecular phenotypes of fragile X syndrome. Ment Retard Dev Disabil Res Rev 2004, 10:53-59.
9. Braun K., Segal M. FMRP involvement in formation of synapses among cultured hippocampal neurons. Cereb Cortex 2000, 10:1045-1052.
10. Brette R., et al. Simulation of networks of spiking neurons: a review of tools and strategies. J Comput Neurosci 2007, 23:349-398.
11. Comery T.A., Harris J.B., Willems P.J., Oostra B.A., Irwin S.A., Weiler I.J., Greenough W.T. Abnormal dendritic spines in fragile X knockout mice: maturation and pruning deficits. Proc Natl Acad Sci USA 1997, 94:5401-5404.
12. Dailey M.E., Smith S.J. The dynamics of dendritic structure in developing hippocampal slices. J Neurosci 1996, 16:2983-2994.
13. Denis-Donini S., Estenoz M. Interneurons versus efferent neurons: heterogeneity in their neurite outgrowth response to glia from several brain regions. Dev Biol 1988, 130:237-249.
14. Dierssen M., Ramakers G.J.A. Dendritic pathology in mental retardation: from molecular genetics to neurobiology. Genes Brain Behav 2006, 5(Suppl 2):48-60.
15. Garcia O., Torres M., Helguera P., Coskun P., Busciglio J. A role for thrombospondin-1 deficits in astrocyte-mediated spine and synaptic pathology in Down's syndrome. PLoS One 2010, 5:e14200.
16. Gatto C.L., Broadie K. Genetic controls balancing excitatory and inhibitory synaptogenesis in neurodevelopmental disorder models. Front Syn Neurosci 2010, 2:4.
17. Gholizadeh S., Halder S.K., Hampson D.R. Expression of fragile X mental retardation protein in neurons and glia of the developing and adult mouse brain. Brain Res 2015, 1596:22-30.
18. Gibson J.R., Bartley A.F., Hays S.A., Huber K.M. Imbalance of neocortical excitation and inhibition and altered UP states reflect network hyperexcitability in the mouse model of fragile X syndrome. J Neurophysiol 2008, 100:2615-2626.
19. Hagerman R., Hoem G., Hagerman P. Fragile X and autism: intertwined at the molecular level leading to targeted treatments. Mol Autism 2010, 1:12.
20. He C.X., Portera-Cailliau C. The trouble with spines in fragile X syndrome: density, maturity and plasticity. Neuroscience 2012.
21. Hume R.I., Purves D. Geometry of neonatal neurones and the regulation of synapse elimination. Nature 1981, 293:469-471.
22. Irwin S.A., Galvez R., Greenough W.T. Dendritic spine structural anomalies in fragile-X mental retardation syndrome. Cereb Cortex 2000, 10:1038-1044.
23. Jacobs S., Doering L.C. Astrocytes prevent abnormal neuronal development in the fragile x mouse. J Neurosci 2010, 30:4508-4514.
24. Jacobs S., Doering L.C. Primary dissociated astrocyte and neuron co-culture. Protocols for neural cell culture 2010, 269-283. 4th ed.
25. Jacobs S., Nathwani M., Doering L.C. Fragile X astrocytes induce developmental delays in dendrite maturation and synaptic protein expression. BMC Neurosci 2010, 11:132.
26. Jan Y.N., Jan L.Y. Branching out: mechanisms of dendritic arborization. Nat Rev Neurosci 2010, 11:316-328.
27. Kanaani J., Kolibachuk J., Martinez H., Baekkeskov S. Two distinct mechanisms target GAD67 to vesicular pathways and presynaptic clusters. J Cell Biol 2010, 190:911-925.
28. Kaufmann W.E., Moser H.W. Dendritic anomalies in disorders associated with mental retardation. Cereb Cortex 2000.
29. Koch C., Segev I. The role of single neurons in information processing. Nat Neurosci 2000, 3(Suppl):1171-1177.
30. Kriegstein A.R., Dichter M.A. Morphological classification of rat cortical neurons in cell culture. J Neurosci 1983, 3:1634-1647.
31. Lee W.-C.A., Huang H., Feng G., Sanes J.R., Brown E.N., So P.T., Nedivi E. Dynamic remodeling of dendritic arbors in GABAergic interneurons of adult visual cortex. PLoS Biol 2006, 4:e29.
32. Libersat F., Duch C. Mechanisms of dendritic maturation. Mol Neurobiol 2004, 29:303-320.
33. Mangan P.S., Sun C., Carpenter M., Goodkin H.P., Sieghart W., Kapur J. Cultured hippocampal pyramidal neurons express two kinds of GABAA receptors. Mol Pharmacol 2005, 67:775-788.
34. Myrick L.K., Deng P.-Y., Hashimoto H., Oh Y.M., Cho Y., Poidevin M.J., Suhl J.A., Visootsak J., Cavalli V., Jin P., Cheng X., Warren S.T., Klyachko V.A. Independent role for presynaptic FMRP revealed by an FMR1missense mutation associated with intellectual disability and seizures. Proc Natl Acad Sci 2015, 112:949-956.
35. Narro M.L., Yang F., Kraft R., Wenk C., Efrat A., Restifo L.L. NeuronMetrics: software for semi-automated processing of cultured neuron images. Brain Res 2007, 1138:57-75.
36. O'Donnell W.T., Warren S.T. A decade of molecular studies of fragile X syndrome. Annu Rev Neurosci 2002, 25:315-338.
37. Okabe S., Miwa A., Okado H. Spine formation and correlated assembly of presynaptic and postsynaptic molecules. J Neurosci 2001, 21:6105-6114.
38. Pacey L.K.K., Doering L.C. Developmental expression of FMRP in the astrocyte lineage: implications for fragile X syndrome. Glia 2007, 55:1601-1609.
39. Rochefort N.L., Konnerth A. Dendritic spines: from structure to in vivo function. EMBO Rep 2012, 13:699-708.
40. Scheuss V., Bonhoeffer T. Function of dendritic spines on hippocampal inhibitory neurons. Cereb Cortex 2014, 24:3142-3153.
41. Schoenen J. Dendritic organization of the human spinal cord: the motoneurons. J Comp Neurol 1982, 211:226-247.
42. Scott E.K., Luo L. How do dendrites take their shape?. Nat Neurosci 2001, 4:359-365.
43. Sholl D.A. Dendritic organization in the neurons of the visual and motor cortices of the cat. J Anat 1953, 87:387-406.
44. Sloan S.A., Barres B.A. Mechanisms of astrocyte development and their contributions to neurodevelopmental disorders. Curr Opin Neurobiol 2014, 27C:75-81.
45. Threadgill R., Bobb K., Ghosh A. Regulation of dendritic growth and remodeling by Rho, Rac, and Cdc42. Neuron 1997.
46. Vetter P., Roth A., Häusser M. Propagation of action potentials in dendrites depends on dendritic morphology. J Neurophysiol 2001, 85:926-937.
47. Wong T.P., Marchese G., Casu M.A., Ribeiro-da-Silva A., Cuello A.C., De Koninck Y. Imbalance towards inhibition as a substrate of aging-associated cognitive impairment. Neurosci Lett 2006, 397:64-68.
48. Yang Y., Vidensky S., Jin L., Jie C., Lorenzini I., Frankl M., Rothstein J.D. Molecular comparison of GLT1+ and ALDH1L1+ astrocytes in vivo in astroglial reporter mice. Glia 2010, 59:200-207.
49. Yang Q., Feng B., Zhang K., Guo Y.-Y., Liu S.-B., Wu Y.-M., Li X.-Q., Zhao M.-G. Excessive astrocyte-derived neurotrophin-3 contributes to the abnormal neuronal dendritic development in a mouse model of fragile X syndrome. PLoS Genet 2012, 8:e1003172.