Impaired dendritic development and synaptic formation of postnatal-born dentate gyrus granular neurons in the absence of brain-derived neurotrophic factor signaling

Experimental Neurology

Volumn 215, Issue 1, 2009, Pages 178-190

  Gao, Xiang ^a   Smith, George M ^a   Chen, Jinhui ^a,b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Brain derived neurotrophic factor; Conditional knockout; Dendrite; Dentate gyrus; Mouse; Postnatal born granular neuron; Spine; Synapse

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CELL STRUCTURE; CONTROLLED STUDY; DENDRITE; DENDRITIC SPINE; DENTATE GYRUS; GRANULAR CELL; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; KNOCKOUT MOUSE; MOUSE; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; SENSORY NERVE; SIGNAL TRANSDUCTION; SYNAPTOGENESIS;

ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; BRAIN-DERIVED NEUROTROPHIC FACTOR; COGNITION DISORDERS; DENDRITES; DENTATE GYRUS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; MAZE LEARNING; MICE; MICE, TRANSGENIC; PRO-OPIOMELANOCORTIN; REACTION TIME; SIGNAL TRANSDUCTION; SYNAPSES;

EID: 57449116962     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2008.10.009     Document Type: Article

References (86)

1. Aakalu G., Smith W.B., Nguyen N., Jiang C., and Schuman E.M. Dynamic visualization of local protein synthesis in hippocampal neurons. Neuron 30 (2001) 489-502
2. Alvarez-Buylla A. Neurogenesis in the adult brain: prospects for brain repair. In: Gage F.H., and Christen Y. (Eds). Isolation, Characterization and Utilization of CNS Stem Cells (1997), Springer, New York 87-100
3. Alvarez-Buylla A., and Garcia-Verdugo J.M. Neurogenesis in adult subventricular zone. J. Neurosci. 22 (2002) 629-634
4. Balthasar N., Coppari R., McMinn J., Liu S.M., Lee C.E., Tang V., Kenny C.D., McGovern R.A., Chua Jr. S.C., Elmquist J.K., and Lowell B.B. Leptin receptor signaling in POMC neurons is required for normal body weight homeostasis. Neuron 42 (2004) 983-991
5. Bear M.F., and Malenka R.C. Synaptic plasticity: LTP and LTD. [Review]. Curr. Opin. Neurobiol. 4 (1994) 389-399
6. Behar T.N., Dugich-Djordjevic M.M., Li Y.X., Ma W., Somogyi R., Wen X., Brown E., Scott C., McKay R.D., and Barker J.L. Neurotrophins stimulate chemotaxis of embryonic cortical neurons. Eur. J. Neurosci. 9 (1997) 2561-2570
7. Borghesani P.R., Peyrin J.M., Klein R., Rubin J., Carter A.R., Schwartz P.M., Luster A., Corfas G., and Segal R.A. BDNF stimulates migration of cerebellar granule cells. Development 129 (2002) 1435-1442
8. Bozdagi O., Shan W., Tanaka H., Benson D.L., and Huntley G.W. Increasing numbers of synaptic puncta during late-phase LTP: N-cadherin is synthesized, recruited to synaptic sites, and required for potentiation. Neuron 28 (2000) 245-259
9. Carlen M., Cassidy R.M., Brismar H., Smith G.A., Enquist L.W., and Frisen J. Functional integration of adult-born neurons. Curr. Biol. 12 (2002) 606-608
10. Chen J., Magavi S.S., and Macklis J.D. Neurogenesis of corticospinal motor neurons extending spinal projections in adult mice. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 16357-16362
11. Cohen-Cory S. The developing synapse: construction and modulation of synaptic structures and circuits. Science 298 (2002) 770-776
12. Conover J.C., and Yancopoulos G.D. Neurotrophin regulation of the developing nervous system: analyses of knockout mice. Rev. Neurosci. 8 (1997) 13-27
13. Dailey M.E., and Smith S.J. The dynamics of dendritic structure in developing hippocampal slices. J. Neurosci. 16 (1996) 2983-2994
14. Deng Y., Thompson B.M., Gao X., and Hall E.D. Temporal relationship of peroxynitrite-induced oxidative damage, calpain-mediated cytoskeletal degradation and neurodegeneration after traumatic brain injury. Exp. Neurol. 205 (2007) 154-165
15. Dijkhuizen P.A., and Ghosh A. BDNF regulates primary dendrite formation in cortical neurons via the PI3-kinase and MAP kinase signaling pathways. J. Neurobiol. 62 (2005) 278-288
16. Doetsch F., Garcia-Verdugo J.M., and Alvarez-Buylla A. Regeneration of a germinal layer in the adult mammalian brain. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 11619-11624
17. Du J.L., and Poo M.M. Rapid BDNF-induced retrograde synaptic modification in a developing retinotectal system. Nature 429 (2004) 878-883
18. Dunaevsky A., Tashiro A., Majewska A., Mason C., and Yuste R. Developmental regulation of spine motility in the mammalian central nervous system. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 13438-13443
19. Emsley J.G., Mitchell B.D., Kempermann G., and Macklis J.D. Adult neurogenesis and repair of the adult CNS with neural progenitors, precursors, and stem cells. Prog. Neurobiol. 75 (2005) 321-341
20. Eriksson P.S., Perfilieva E., Bjork-Eriksson T., Alborn A.M., Nordborg C., Peterson D.A., and Gage F.H. Neurogenesis in the adult human hippocampus. Nat. Med. 4 (1998) 1313-1317
21. Fischer M., Kaech S., Knutti D., and Matus A. Rapid actin-based plasticity in dendritic spines. Neuron 20 (1998) 847-854
22. Friedman H.V., Bresler T., Garner C.C., and Ziv N.E. Assembly of new individual excitatory synapses: time course and temporal order of synaptic molecule recruitment. Neuron 27 (2000) 57-69
23. Gage F.H. Neurogenesis in the adult brain. J. Neurosci. 22 (2002) 612-613
24. Gao X., Arlotta P., Macklis J.D., and Chen J. Conditional knock-out of-catenin in postnatal-born dentate gyrus granule neurons results in dendritic malformation. J. Neurosci. 27 (2007) 14317-14325
25. Gao X., Deng-Bryant Y., Cho W., Carrico K.M., Hall E.D., and Chen J. Selective death of newborn neurons in hippocampal dentate gyrus following moderate experimental traumatic brain injury. J. Neurosci. Res. 86 (2008) 2258-2270
26. Gorski J.A., Zeiler S.R., Tamowski S., and Jones K.R. Brain-derived neurotrophic factor is required for the maintenance of cortical dendrites. J. Neurosci. 23 (2003) 6856-6865
27. Harris K.M. Structure, development, and plasticity of dendritic spines. Curr. Opin. Neurobiol. 9 (1999) 343-348
28. Harris K.M., Jensen F.E., and Tsao B. Three-dimensional structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages: implications for the maturation of synaptic physiology and long-term potentiation. J. Neurosci. 12 (1992) 2685-2705
29. Horch H.W. Local effects of BDNF on dendritic growth. Rev. Neurosci. 15 (2004) 117-129
30. Horch H.W., and Katz L.C. BDNF release from single cells elicits local dendritic growth in nearby neurons. Nat. Neurosci. 5 (2002) 1177-1184
31. Horch H.W., Kruttgen A., Portbury S.D., and Katz L.C. Destabilization of cortical dendrites and spines by BDNF. Neuron 23 (1999) 353-364
32. Inagaki T., Begum T., Reza F., Horibe S., Inaba M., Yoshimura Y., and Komatsu Y. Brain-derived neurotrophic factor-mediated retrograde signaling required for the induction of long-term potentiation at inhibitory synapses of visual cortical pyramidal neurons. Neurosci. Res. 61 (2008) 192-200
33. Itami C., Kimura F., Kohno T., Matsuoka M., Ichikawa M., Tsumoto T., and Nakamura S. Brain-derived neurotrophic factor-dependent unmasking of "silent" synapses in the developing mouse barrel cortex. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 13069-13074
34. Jankowsky J.L., and Patterson P.H. Cytokine and growth factor involvement in long-term potentiation. Mol. Cell. Neurosci. 14 (1999) 273-286
35. Jin X., Hu H., Mathers P.H., and Agmon A. Brain-derived neurotrophic factor mediates activity-dependent dendritic growth in nonpyramidal neocortical interneurons in developing organotypic cultures. J. Neurosci. 23 (2003) 5662-5673
36. Kasai H., Matsuzaki M., Noguchi J., Yasumatsu N., and Nakahara H. Structure-stability-function relationships of dendritic spines. Trends Neurosci. 26 (2003) 360-368
37. Kempermann G., Wiskott L., and Gage F.H. Functional significance of adult neurogenesis. Curr. Opin. Neurobiol. 14 (2004) 186-191
38. Kempermann G., Chesler E.J., Lu L., Williams R.W., and Gage F.H. Natural variation and genetic covariance in adult hippocampal neurogenesis. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 780-785
39. Korte M., Carroll P., Wolf E., Brem G., Thoenen H., and Bonhoeffer T. Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 8856-8860
40. Kovalchuk Y., Hanse E., Kafitz K.W., and Konnerth A. Postsynaptic Induction of BDNF-Mediated Long-Term Potentiation. Science 295 (2002) 1729-1734
41. Kumar V., Zhang M.X., Swank M.W., Kunz J., and Wu G.Y. Regulation of dendritic morphogenesis by Ras-PI3K-Akt-mTOR and Ras-MAPK signaling pathways. J. Neurosci. 25 (2005) 11288-11299
42. Lendvai B., Stern E.A., Chen B., and Svoboda K. Experience-dependent plasticity of dendritic spines in the developing rat barrel cortex in vivo. Nature 404 (2000) 876-881
43. Li Z., and Sheng M. Some assembly required: the development of neuronal synapses. Nat. Rev. Mol. Cell. Biol. 4 (2003) 833-841
44. Lu B., and Chow A. Neurotrophins and hippocampal synaptic transmission and plasticity. J. Neurosci. Res. 58 (1999) 76-87
45. Lynch G., Rex C.S., and Gall C.M. LTP consolidation: substrates, explanatory power, and functional significance. Neuropharmacology 52 (2007) 12-23
46. Magavi S.S., Leavitt B.R., and Macklis J.D. Induction of neurogenesis in the neocortex of adult mice. Nature 405 (2000) 951-955
47. Malenka R.C. Synaptic plasticity in the hippocampus: LTP and LTD. [Review]. Cell 78 (1994) 535-538
48. Markakis E.A., and Gage F.H. Adult-generated neurons in the dentate gyrus send axonal projections to field CA3 and are surrounded by synaptic vesicles. J. Comp. Neurol. 406 (1999) 449-460
49. Matsuzaki M., Honkura N., Ellis-Davies G.C., and Kasai H. Structural basis of long-term potentiation in single dendritic spines. Nature 429 (2004) 761-766
50. McAllister A.K., Lo D.C., and Katz L.C. Neurotrophins regulate dendritic growth in developing visual cortex. Neuron 15 (1995) 791-803
51. Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Methods. 11 (1984) 47-60
52. Niblock M.M., Brunso-Bechtold J.K., and Riddle D.R. Insulin-like growth factor I stimulates dendritic growth in primary somatosensory cortex. J. Neurosci. 20 (2000) 4165-4176
53. Novak K. Lost in the FOG. Nat. Med. 6 (2000) 864
54. Ohmiya M., Shudai T., Nitta A., Nomoto H., Furukawa Y., and Furukawa S. Brain-derived neurotrophic factor alters cell migration of particular progenitors in the developing mouse cerebral cortex. Neurosci. Lett. 317 (2002) 21-24
55. Okabe S., Miwa A., and Okado H. Spine formation and correlated assembly of presynaptic and postsynaptic molecules. J. Neurosci. 21 (2001) 6105-6114
56. Pang P.T., and Lu B. Regulation of late-phase LTP and long-term memory in normal and aging hippocampus: role of secreted proteins tPA and BDNF. Ageing Res. Rev. 3 (2004) 407-430
57. Patterson S.L., Abel T., Deuel T.A.S., Martin K.C., Rose J.C., and Kandel E.R. Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice. Neuron 16 (1996) 1137-1145
58. Petrak L.J., Harris K.M., and Kirov S.A. Synaptogenesis on mature hippocampal dendrites occurs via filopodia and immature spines during blocked synaptic transmission. J. Comp. Neurol. 484 (2005) 183-190
59. Polleux F., Whitford K.L., Dijkhuizen P.A., Vitalis T., and Ghosh A. Control of cortical interneuron migration by neurotrophins and PI3-kinase signaling. Development 129 (2002) 3147-3160
60. Portera-Cailliau C., Pan D.T., and Yuste R. Activity-regulated dynamic behavior of early dendritic protrusions: evidence for different types of dendritic filopodia. J. Neurosci. 23 (2003) 7129-7142
61. Pozzo-Miller L. BDNF enhances dendritic Ca2+ signals evoked by coincident EPSPs and back-propagating action potentials in CA1 pyramidal neurons. Brain Res. 1104 (2006) 45-54
62. Pozzo-Miller L.D., Gottschalk W., Zhang L., McDermott K., Du J., Gopalakrishnan R., Oho C., Sheng Z.H., and Lu B. Impairments in high-frequency transmission, synaptic vesicle docking, and synaptic protein distribution in the hippocampus of BDNF knockout mice. J. Neurosci. 19 (1999) 4972-4983
63. Rao A., Kim E., Sheng M., and Craig A.M. Heterogeneity in the molecular composition of excitatory postsynaptic sites during development of hippocampal neurons in culture. J. Neurosci. 18 (1998) 1217-1229
64. Redmond L., and Ghosh A. The role of Notch and Rho GTPase signaling in the control of dendritic development. Curr. Opin. Neurobiol. 11 (2001) 111-117
65. Redmond L., Oh S.R., Hicks C., Weinmaster G., and Ghosh A. Nuclear Notch1 signaling and the regulation of dendritic development. Nat. Neurosci. 3 (2000) 30-40
66. Rex C.S., Lin C.Y., Kramar E.A., Chen L.Y., Gall C.M., and Lynch G. Brain-derived neurotrophic factor promotes long-term potentiation-related cytoskeletal changes in adult hippocampus. J. Neurosci. 27 (2007) 3017-3029
67. Salama-Cohen P., Arevalo M.A., Meier J., Grantyn R., and Rodriguez-Tebar A. NGF Controls Dendrite Development in Hippocampal Neurons by Binding to p75NTR and Modulating the Cellular Targets of Notch. Mol. Biol. Cell 16 (2005) 339-347
68. Shimada A., Mason C.A., and Morrison M.E. TrkB signaling modulates spine density and morphology independent of dendrite structure in cultured neonatal Purkinje cells. J. Neurosci. 18 (1998) 8559-8570
69. Smith D.H., Okiyama K., Thomas M.J., Claussen B., and McIntosh T.K. Evaluation of memory dysfunction following experimental brain injury using the Morris water maze. J. Neurotrauma 8 (1991) 259-269
70. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21 (1999) 70-71
71. Soule J., Messaoudi E., and Bramham C.R. Brain-derived neurotrophic factor and control of synaptic consolidation in the adult brain. Biochem. Soc. Trans. 34 (2006) 600-604
72. Taupin P. Adult neurogenesis in the mammalian central nervous system: functionality and potential clinical interest. Med. Sci. Monit. 11 (2005) RA247-RA252
73. Taupin P., and Gage F.H. Adult neurogenesis and neural stem cells of the central nervous system in mammals. J. Neurosci. Res. 69 (2002) 745-749
74. Tolwani R.J., Buckmaster P.S., Varma S., Cosgaya J.M., Wu Y., Suri C., and Shooter E.M. BDNF overexpression increases dendrite complexity in hippocampal dentate gyrus. Neuroscience 114 (2002) 795-805
75. Unger T.J., Calderon G.A., Bradley L.C., Sena-Esteves M., and Rios M. Selective deletion of Bdnf in the ventromedial and dorsomedial hypothalamus of adult mice results in hyperphagic behavior and obesity. J. Neurosci. 27 (2007) 14265-14274
76. van Praag H., Schinder A.F., Christie B.R., Toni N., Palmer T.D., and Gage F.H. Functional neurogenesis in the adult hippocampus. Nature 415 (2002) 1030-1034
77. Vicario-Abejon C., Collin C., McKay R.D., and Segal M. Neurotrophins induce formation of functional excitatory and inhibitory synapses between cultured hippocampal neurons. J. Neurosci. 18 (1998) 7256-7271
78. Washbourne P., Bennett J.E., and McAllister A.K. Rapid recruitment of NMDA receptor transport packets to nascent synapses. Nat. Neurosci. 5 (2002) 751-759
79. West M.J., Slomianka L., and Gundersen H.J. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat. Rec. 231 (1991) 482-497
80. Whitford K.L., Marillat V., Stein E., Goodman C.S., Tessier-Lavigne M., Chedotal A., and Ghosh A. Regulation of cortical dendrite development by Slit-Robo interactions. Neuron 33 (2002) 47-61
81. Xu H.T., Pan F., Yang G., and Gan W.B. Choice of cranial window type for in vivo imaging affects dendritic spine turnover in the cortex. Nat. Neurosci. 10 (2007) 549-551
82. Yacoubian T., and Lo D. Truncated and full-length TrkB receptors regulate distinct modes of dendritic growth. Nat. Neurosci. 3 (2000) 342-349
83. Ying S.W., Futter M., Rosenblum K., Webber M.J., Hunt S.P., Bliss T.V., and Bramham C.R. Brain-derived neurotrophic factor induces long-term potentiation in intact adult hippocampus: requirement for ERK activation coupled to CREB and upregulation of Arc synthesis. J. Neurosci. 22 (2002) 1532-1540
84. Yoshii A., and Constantine-Paton M. BDNF induces transport of PSD-95 to dendrites through PI3K-AKT signaling after NMDA receptor activation. Nat. Neurosci. 10 (2007) 702-711
85. Zhou P., Porcionatto M., Pilapil M., Chen Y., Choi Y., Tolias K.F., Bikoff J.B., Hong E.J., Greenberg M.E., and Segal R.A. Polarized signaling endosomes coordinate BDNF-induced chemotaxis of cerebellar precursors. Neuron 55 (2007) 53-68
86. Ziv N.E., and Smith S.J. Evidence for a role of dendritic filopodia in synaptogenesis and spine formation. Neuron 17 (1996) 91-102