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Cellular and Molecular Life Sciences

, Volume 74, Issue 23, pp 4369–4385 | Cite as

Distinct effects on the dendritic arbor occur by microbead versus bath administration of brain-derived neurotrophic factor

  • Kate M. O’Neill
  • Munjin Kwon
  • Katherine E. Donohue
  • Bonnie L. Firestein
Original Article

Abstract

Proper communication among neurons depends on an appropriately formed dendritic arbor, and thus, aberrant changes to the arbor are implicated in many pathologies, ranging from cognitive disorders to neurodegenerative diseases. Due to the importance of dendritic shape to neuronal network function, the morphology of dendrites is tightly controlled and is influenced by both intrinsic and extrinsic factors. In this work, we examine how brain-derived neurotrophic factor (BDNF), one of the most well-studied extrinsic regulators of dendritic branching, affects the arbor when it is applied locally via microbeads to cultures of hippocampal neurons. We found that local application of BDNF increases both proximal and distal branching in a time-dependent manner and that local BDNF application attenuates pruning of dendrites that occurs with neuronal maturation. Additionally, we examined whether cytosolic PSD-95 interactor (cypin), an intrinsic regulator of dendritic branching, plays a role in these changes and found strong evidence for the involvement of cypin in BDNF-promoted increases in dendrites after 24 but not 48 h of application. This current study extends our previous work in which we found that bath application of BDNF for 72 h, but not shorter times, increases proximal dendrite branching and that this increase occurs through transcriptional regulation of cypin. Moreover, this current work illustrates how dendritic branching is regulated differently by the same growth factor depending on its spatial localization, suggesting a novel pathway for modulation of dendritic branching locally.

Keywords

Hippocampal neurons Dendrite arborization BDNF Cytosolic PSD-95 interactor (cypin) Sholl analysis Local stimulation 

Notes

Acknowledgements

This work is funded in part by National Science Foundation grants IOS-0919747 and IOS-1353724 (to BLF). KMO is supported by the National Institutes of Health under the Ruth L. Kirschstein National Research Service Award 5 T32 GM008339 from the NIGMS, a Predoctoral Fellowship from the New Jersey Commission on Brain Injury Research #CBIR13FEL002, and a Predoctoral GAANN Fellowship #P200A150131 from the DOE. KED was awarded Aresty Research Funding from Rutgers University. The authors would also like to thank Dr. Kelvin Kwan (Rutgers University) for his generous help with imaging of the microbeads.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Supplementary material

18_2017_2589_MOESM1_ESM.tif (960 kb)
Supplementary Figure 1: Bead distribution along the dendritic arbor. Bead distance from the cell body was measured if beads were within 4.5 μm of a dendrite. Bead distributions are plotted in 20 μm increments. Part 1. Bead distribution along the dendritic arbor is highly correlated between the conditions at different time points. Pearson’s r coefficient is 0.9371, 0.9787, 0.9629, and 0.9773 for 5h, 24h, 48h, and 72h, respectively. Part 2. Bead distribution is highly correlated between treatment conditions in neurons transfected with identical shRNA plasmids. For neurons transfected with GST shRNA, Pearson’s r is 0.9321, 0.8980, and 0.9769 for 5h, 24h, and 48h, respectively. For neurons transfected with cypin shRNA, Pearson’s r is 0.9726, 0.9676, and 0.8708 for 5h, 24h, and 48h, respectively (TIFF 959 kb)
18_2017_2589_MOESM2_ESM.tif (794 kb)
Supplementary Figure 2: Average number of dendrites per neuron is significantly increased after treatment with BDNF-coated beads for at least 48 hours. A. Treatment with BDNF-coated beads for 5 hours does not significantly change the average number of dendrites per neuron. B. Treatment with BDNF-coated beads for 24 hours does not significantly change the average number of dendrites per neuron. C. Treatment with BDNF-coated beads for 48 hours significantly increases the average number of dendrites per neuron (*p<0.05). D. Treatment with BDNF-coated beads for 72 hours significantly increases the average number of dendrites per neuron (*p<0.05). Statistics calculated by Student’s t-test. Error bars indicate SEM (TIFF 793 kb)
18_2017_2589_MOESM3_ESM.tif (1.2 mb)
Supplementary Figure 3: Order-specific analysis of dendrite numbers reveals that treatment with BDNF-coated beads significantly affects distinct orders of dendrites in a time-dependent manner. A-C. Analysis of dendrites of neurons treated for 5 hours with BSA- or BDNF-coated beads. A. Treatment with BDNF-coated beads does not significantly change the number of primary dendrites. B. Treatment with BDNF-coated beads significantly decreases the number of secondary dendrites (*p<0.05). C. Treatment with BDNF-coated beads does not significantly change the number of tertiary and higher order dendrites. D-F. Analysis of dendrites of neurons treated for 24 hours with BSA- or BDNF-coated beads. D. Treatment with BDNF-coated beads significantly increases the number of primary dendrites (**p<0.01). E. Treatment with BDNF-coated beads does not significantly change the number of secondary dendrites. F. Treatment with BDNF-coated beads does not significantly change the number of tertiary and higher order dendrites. G-I. Analysis of dendrites of neurons treated for 48 hours with BSA- or BDNF-coated beads. G. Treatment with BDNF-coated beads does not significantly change the number of primary dendrites. H. Treatment with BDNF-coated beads does not significantly change the number of secondary dendrites. I. Treatment with BDNF-coated beads significantly increases the number of tertiary and higher order dendrites (*p<0.05). J-L. Analysis of dendrites of neurons treated for 72 hours with BSA- or BDNF-coated beads. J. Treatment with BDNF-coated beads significantly increases the number of primary dendrites (*p<0.05). K. Treatment with BDNF-coated beads significantly increases the number of secondary dendrites (*p<0.05). L. Treatment with BDNF-coated beads does not significantly change the number of tertiary and higher order dendrites. Statistics calculated by Student’s t-test. Error bars indicate SEM (TIFF 1260 kb)
18_2017_2589_MOESM4_ESM.tif (917 kb)
Supplementary Figure 4: Average dendrite length per neuron is not altered by treatment with BDNF-coated beads. A. Treatment with BDNF-coated beads for 5 hours does not significantly change the average length of dendrites per neuron. B. Treatment with BDNF-coated beads for 24 hours does not significantly change the average length of dendrites per neuron. C. Treatment with BDNF-coated beads for 48 hours does not significantly change the average length of dendrites per neuron. D. Treatment with BDNF-coated beads for 72 hours does not significantly change the average length of dendrites per neuron. Statistics calculated by Student’s t-test. Error bars indicate SEM. (TIFF 917 kb)
18_2017_2589_MOESM5_ESM.tif (1.4 mb)
Supplementary Figure 5: Order-specific analysis of dendrite lengths reveals that treatment with BDNF-coated beads significantly increases the length of tertiary and higher order dendrites after 72 hours. A-C. Analysis of dendrites of neurons treated for 5 hours with BSA- or BDNF-coated beads. A. Treatment with BDNF-coated beads does not significantly change the average length of primary dendrites. B. Treatment with BDNF-coated beads does not significantly change the average length of secondary dendrites. C. Treatment with BDNF-coated beads does not significantly change the average length of tertiary and higher order dendrites. D-F. Analysis of dendrites of neurons treated for 24 hours with BSA- or BDNF-coated beads. D. Treatment with BDNF-coated beads does not significantly change the average length of primary dendrites. E. Treatment with BDNF-coated beads does not significantly change the average length of secondary dendrites. F. Treatment with BDNF-coated beads does not significantly change the average length of tertiary and higher order dendrites. G-I. Analysis of dendrites of neurons treated for 48 hours with BSA- or BDNF-coated beads. G. Treatment with BDNF-coated beads does not significantly change the average length of primary dendrites. H. Treatment with BDNF-coated beads does not significantly change the average length of secondary dendrites. I. Treatment with BDNF-coated beads does not significantly change the average length of tertiary and higher order dendrites. J-L. Analysis of dendrites of neurons treated for 72 hours with BSA- or BDNF-coated beads. J. Treatment with BDNF-coated beads does not significantly change the average length of primary dendrites. K. Treatment with BDNF-coated beads does not significantly change the average length of secondary dendrites. L. Treatment with BDNF-coated beads significantly increases the average length of tertiary and higher order dendrites (*p<0.05). Statistics calculated by Student’s t-test. Error bars indicate SEM (TIFF 1404 kb)

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Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Department of Cell Biology & NeuroscienceRutgers UniversityPiscatawayUSA
  2. 2.Graduate Program in Biomedical Engineering Rutgers UniversityPiscatawayUSA
  3. 3.Biomedical Engineering Graduate Faculty Rutgers UniversityPiscatawayUSA

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