Distinct roles for somatically and dendritically synthesized brain-derived neurotrophic factor in morphogenesis of dendritic spines

Journal of Neuroscience

Volumn 33, Issue 28, 2013, Pages 11618-11632

  Orefice, Lauren L ^a   Waterhouse, Emily G ^a   Partridge, John G ^a   Lalchandani, Rupa R ^a   Vicini, Stefano ^a   Xu, Baoji ^a  

^a GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; MESSENGER RNA; SHORT HAIRPIN RNA;

3' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE DENSITY; BRAIN ELECTROPHYSIOLOGY; CELL MIGRATION; CONTROLLED STUDY; DENDRITIC SPINE; EMBRYO; FLUORESCENCE IN SITU HYBRIDIZATION; GENETIC TRANSFECTION; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; MORPHOGENESIS; NONHUMAN; NORTHERN BLOTTING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; REAL TIME POLYMERASE CHAIN REACTION; SINGLE NUCLEOTIDE POLYMORPHISM; SYNAPSE; WESTERN BLOTTING;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELLS, CULTURED; DENDRITES; DENDRITIC SPINES; FEMALE; HEK293 CELLS; HIPPOCAMPUS; HUMANS; MALE; MICE; MORPHOGENESIS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84880424437     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0012-13.2013     Document Type: Article

References (40)

1. Adachi N, Kohara K, Tsumoto T (2005) Difference in trafficking of brainderived neurotrophic factor between axons and dendrites of cortical neurons, revealed by live-cell imaging. BMC Neurosci 6:42. CrossRef Medline
2. An JJ, Gharami K, Liao GY, Woo NH, Lau AG, Vanevski F, Torre ER, Jones KR, Feng Y, Lu B, Xu B (2008) Distinct role of long 3 UTR BDNF mRNA in spine morphology and synaptic plasticity in hippocampal neurons. Cell 134:175-187. CrossRef Medline
3. Bhatt DH, Zhang S, Gan WB (2009) Dendritic spine dynamics. Annu Rev Physiol 71:261-282. CrossRef Medline
4. Brummelkamp TR, Bernards R, Agami R (2002) A system for stable expression of short interfering RNAs in mammalian cells. Science 296:550-553. CrossRef Medline
5. Churchill JD, Grossman AW, Irwin SA, Galvez R, Klintsova AY, Weiler IJ, Greenough WT (2002) A converging-methods approach to fragile X syndrome. Dev Psychobiol 40:323-338. CrossRef Medline
6. Comery TA, Harris JB, Willems PJ, Oostra BA, Irwin SA, Weiler IJ, Greenough WT (1997) Abnormal dendritic spines in fragile X knockout mice: maturation and pruning deficits. Proc Natl Acad Sci U S A 94:5401-5404. CrossRef Medline
7. Dean C, Liu H, Dunning FM, Chang PY, Jackson MB, Chapman ER (2009) Synaptotagmin-IV modulates synaptic function and long-term potentiation by regulating BDNF release. Nat Neurosci 12:767-776. CrossRef Medline
8. Dieni S, Matsumoto T, Dekkers M, Rauskolb S, Ionescu MS, Deogracias R, Gundelfinger ED, Kojima M, Nestel S, Frotscher M, Barde YA (2012) BDNF and its pro-peptide are stored in presynaptic dense core vesicles in brain neurons. J Cell Biol 196:775-788. CrossRef Medline
9. English CN, Vigers AJ, Jones KR (2012) Genetic evidence that brain-derived neurotrophic factor mediates competitive interactions between individual cortical neurons. Proc Natl Acad Sci U S A 109:19456-19461. CrossRef Medline
10. Ethell IM, Pasquale EB (2005) Molecular mechanisms of dendritic spine development and remodeling. Prog Neurobiol 75:161-205. CrossRef Medline
11. Ethell IM, Irie F, Kalo MS, Couchman JR, Pasquale EB, Yamaguchi Y (2001) EphB/syndecan-2 signaling in dendritic spine morphogenesis. Neuron 31:1001-1013. CrossRef Medline
12. Fischer M, Kaech S, Knutti D, Matus A (1998) Rapid actin-based plasticity in dendritic spines. Neuron 20:847-854. CrossRef Medline
13. Grutzendler J, Kasthuri N, Gan WB (2002) Long-term dendritic spine stability in the adult cortex. Nature 420:812-816. CrossRef Medline
14. Harris KM (1999) Structure, development, and plasticity of dendritic spines. Curr Opin Neurobiol 9:343-348. CrossRef Medline
15. Holtmaat A, Svoboda K (2009) Experience-dependent structural synaptic plasticity in the mammalian brain. Nat Rev Neurosci 10:647-658. CrossRef Medline
16. Huttenlocher PR (1979) Synaptic density in human frontal cortexdevelopmental changes and effects of aging. Brain Res 163:195-205. CrossRef Medline
17. Kaneko M, Xie Y, An JJ, Stryker MP, Xu B (2012) Dendritic BDNF synthesis is required for late-phase spine maturation and recovery of cortical responses following sensory deprivation. J Neurosci 32:4790-4802. CrossRef Medline
18. Marin-Padilla M (1967) Number and distribution of the apical dendritic spines of the layer V pyramidal cells in man. J Comp Neurol 131:475-490. CrossRef Medline
19. Mataga N, Mizuguchi Y, Hensch TK (2004) Experience-dependent pruning of dendritic spines in visual cortex by tissue plasminogen activator. Neuron 44:1031-1041. CrossRef Medline
20. Matsuda N, Lu H, Fukata Y, Noritake J, Gao H, Mukherjee S, Nemoto T, Fukata M, Poo MM (2009) Differential activity-dependent secretion of brain-derived neurotrophic factor from axon and dendrite. J Neurosci 29:14185-14198. CrossRef Medline
21. Matsuzaki M, Ellis-Davies GC, Nemoto T, Miyashita Y, Iino M, Kasai H (2001) Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat Neurosci 4:1086-1092. CrossRef Medline
22. Matsuzaki M, Honkura N, Ellis-Davies GC, Kasai H (2004) Structural basis of long-term potentiation in single dendritic spines. Nature 429:761-766. CrossRef Medline
23. Murase K, Ryu PD, Randic M (1989) Excitatory and inhibitory amino acids and peptide-induced responses in acutely isolated rat spinal dorsal horn neurons. Neurosci Lett 103:56-63. CrossRef Medline
24. Murthy VN, Sejnowski TJ, Stevens CF (1997) Heterogeneous release properties of visualized individual hippocampal synapses. Neuron 18:599-612. CrossRef Medline
25. Nusser Z, Lujan R, Laube G, Roberts JD, Molnar E, Somogyi P (1998) Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus. Neuron 21:545-559. CrossRef Medline
26. Papa M, Bundman MC, Greenberger V, Segal M (1995) Morphological analysis of dendritic spine development in primary cultures of hippocampal neurons. J Neurosci 15:1-11. Medline
27. Racca C, Stephenson FA, Streit P, Roberts JD, Somogyi P (2000) NMDA receptor content of synapses in stratum radiatum of the hippocampal CA1 area. J Neurosci 20:2512-2522. Medline
28. Rakic P, Bourgeois JP, Eckenhoff MF, Zecevic N, Goldman-Rakic PS (1986) Concurrent overproduction of synapses in diverse regions of the primate cerebral cortex. Science 232:232-235. CrossRef Medline
29. Rostami E, Krueger F, Zoubak S, Dal Monte O, Raymont V, Pardini M, Hodgkinson CA, Goldman D, Risling M, Grafman J (2011) BDNF polymorphism predicts general intelligence after penetrating traumatic brain injury. PLoS One 6:e27389. CrossRef Medline
30. Sala C, Rudolph-Correia S, Sheng M (2000) Developmentally regulated NMDA receptor-dependent dephosphorylation of cAMP response element-binding protein (CREB) in hippocampal neurons. J Neurosci 20:3529-3536. Medline
31. Sala C, Piëch V, Wilson NR, Passafaro M, Liu G, Sheng M (2001) Regulation of dendritic spine morphology and synaptic function by Shank and Homer. Neuron 31:115-130. CrossRef Medline
32. Sala C, Cambianica I, Rossi F (2008) Molecular mechanisms of dendritic spine development and maintenance. Acta Neurobiol Exp (Wars) 68:289-304.
33. Schikorski T, Stevens CF (1997) Quantitative ultrastructural analysis of hippocampal excitatory synapses. J Neurosci 17:5858-5867. Medline
34. Timmusk T, Palm K, Metsis M, Reintam T, Paalme V, Saarma M, Persson H (1993) Multiple promoters direct tissue-specific expression of the rat BDNF gene. Neuron 10:475-489. CrossRef Medline
35. Tolias KF, Bikoff JB, Kane CG, Tolias CS, Hu L, Greenberg ME (2007) The Rac1 guanine nucleotide exchange factor Tiam1 mediates EphB receptordependent dendritic spine development. Proc Natl Acad Sci U S A 104: 7265-7270. CrossRef Medline
36. Waterhouse EG, Xu B (2009) New insights into the role of brain-derived neurotrophic factor in synaptic plasticity. Mol Cell Neurosci 42:81-89. CrossRef Medline
37. Weickert CS, Hyde TM, Lipska BK, Herman MM, Weinberger DR, Kleinman JE (2003) Reduced brain-derived neurotrophic factor in prefrontal cortex of patients with schizophrenia. Mol Psychiatry 8:592-610. CrossRef Medline
38. Yoshihara Y, De Roo M, Muller D (2009) Dendritic spine formation and stabilization. Curr Opin Neurobiol 19:146-153. CrossRef Medline
39. Zuo Y, Lin A, Chang P, Gan WB (2005a) Development of long-term dendritic spine stability in diverse regions of cerebral cortex. Neuron 46:181-189. CrossRef Medline
40. Zuo Y, Yang G, Kwon E, Gan WB (2005b) Long-term sensory deprivation prevents dendritic spine loss in primary somatosensory cortex. Nature 436:261-265. CrossRef Medline