Brain-derived Neurotrophic Factor (BDNF) Induces Dendritic Targeting of BDNF and Tyrosine Kinase B MRNAs in Hippocampal Neurons Through a Phosphatidylinositol-3 Kinase-dependent Pathway

Overview

Journal J Neurosci

Specialty Neurology

Date 2000 Apr 25

PMID 10777780

Citations 36

Authors

M Righi

E Tongiorgi

A Cattaneo

Affiliations

Soon will be listed here.

Abstract

This study aims to understand the mechanisms of dendritic targeting of brain-derived neurotrophic factor (BDNF) and tyrosine kinase B (TrkB) mRNAs. We show that brief depolarizations are sufficient to induce accumulation of BDNF and TrkB mRNAs in dendrites of hippocampal neurons. Endogenous BDNF, secreted during the KCl stimulation, contributes significantly to the dendritic accumulation of BDNF-TrkB mRNAs. In the absence of depolarization, 1 min pulses of exogenous BDNF are sufficient to induce dendritic accumulation of BDNF-TrkB mRNAs. After binding to TrkB, BDNF exerts this action by activating a PI-3 kinase-dependent pathway. The accumulation of dendritic mRNA by BDNF is not mediated by BDNF-induced neurotransmitter release. Because most hippocampal neurons coexpress BDNF and TrkB receptors, these results show that the subcellular distribution of BDNF-TrkB mRNAs is under the control of an autocrine-paracrine BDNF-TrkB-dependent loop.

Citing Articles

Influencing factors and repair advancements in rodent models of peripheral nerve regeneration.

Olsen T, LaGuardia J, Chen D, Lebens R, Huang K, Milek D Regen Med. 2024; 19(11):561-577.

PMID: 39469920 PMC: 11633413. DOI: 10.1080/17460751.2024.2405318.

Brain-derived neurotrophic factor protects neurons by stimulating mitochondrial function through protein kinase A.

Swain M, K Soman S, Tapia K, Dagda R, Dagda R J Neurochem. 2023; 167(1):104-125.

PMID: 37688457 PMC: 10543477. DOI: 10.1111/jnc.15945.

Deep cerebellar stimulation enhances cognitive recovery after prefrontal traumatic brain injury in rodent.

Chan H, Hogue O, Mathews N, Hunter J, Kundalia R, Hermann J Exp Neurol. 2022; 355:114136.

PMID: 35667396 PMC: 10203848. DOI: 10.1016/j.expneurol.2022.114136.

The Role of Altered BDNF/TrkB Signaling in Amyotrophic Lateral Sclerosis.

Pradhan J, Noakes P, Bellingham M Front Cell Neurosci. 2019; 13:368.

PMID: 31456666 PMC: 6700252. DOI: 10.3389/fncel.2019.00368.

Mechanisms That Modulate and Diversify BDNF Functions: Implications for Hippocampal Synaptic Plasticity.

De Vincenti A, Rios A, Paratcha G, Ledda F Front Cell Neurosci. 2019; 13:135.

PMID: 31024262 PMC: 6465932. DOI: 10.3389/fncel.2019.00135.

References

Steward O, Halpain S . Lamina-specific synaptic activation causes domain-specific alterations in dendritic immunostaining for MAP2 and CAM kinase II. J Neurosci. 1999; 19(18):7834-45. PMC: 6782448. View

Chamow S, Ashkenazi A . Immunoadhesins: principles and applications. Trends Biotechnol. 1996; 14(2):52-60. DOI: 10.1016/0167-7799(96)80921-8. View

Crino P, Eberwine J . Molecular characterization of the dendritic growth cone: regulated mRNA transport and local protein synthesis. Neuron. 1996; 17(6):1173-87. DOI: 10.1016/s0896-6273(00)80248-2. View

Roberts L, Large C, Higgins M, Stone T, Oshaughnessy C, Morris B . Increased expression of dendritic mRNA following the induction of long-term potentiation. Brain Res Mol Brain Res. 1998; 56(1-2):38-44. DOI: 10.1016/s0169-328x(98)00026-6. View

Acheson A, Conover J, Fandl J, DeChiara T, Russell M, Thadani A . A BDNF autocrine loop in adult sensory neurons prevents cell death. Nature. 1995; 374(6521):450-3. DOI: 10.1038/374450a0. View

Knowles R, Kosik K . Neurotrophin-3 signals redistribute RNA in neurons. Proc Natl Acad Sci U S A. 1998; 94(26):14804-8. PMC: 25118. DOI: 10.1073/pnas.94.26.14804. View

HAMERS-CASTERMAN C, Atarhouch T, Muyldermans S, Robinson G, Hamers C, Songa E . Naturally occurring antibodies devoid of light chains. Nature. 1993; 363(6428):446-8. DOI: 10.1038/363446a0. View

Kafitz K, Rose C, Thoenen H, Konnerth A . Neurotrophin-evoked rapid excitation through TrkB receptors. Nature. 1999; 401(6756):918-21. DOI: 10.1038/44847. View

Berg M, Sternberg D, Parada L, Chao M . K-252a inhibits nerve growth factor-induced trk proto-oncogene tyrosine phosphorylation and kinase activity. J Biol Chem. 1992; 267(1):13-6. View

10.

Corvera S, Czech M . Direct targets of phosphoinositide 3-kinase products in membrane traffic and signal transduction. Trends Cell Biol. 1998; 8(11):442-6. DOI: 10.1016/s0962-8924(98)01366-x. View

11.

Plopper G, McNamee H, Dike L, Bojanowski K, Ingber D . Convergence of integrin and growth factor receptor signaling pathways within the focal adhesion complex. Mol Biol Cell. 1995; 6(10):1349-65. PMC: 301292. DOI: 10.1091/mbc.6.10.1349. View

12.

Dudley D, Pang L, Decker S, Bridges A, Saltiel A . A synthetic inhibitor of the mitogen-activated protein kinase cascade. Proc Natl Acad Sci U S A. 1995; 92(17):7686-9. PMC: 41210. DOI: 10.1073/pnas.92.17.7686. View

13.

Greene L, Tischler A . Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci U S A. 1976; 73(7):2424-8. PMC: 430592. DOI: 10.1073/pnas.73.7.2424. View

14.

Canossa M, Griesbeck O, Berninger B, Campana G, Kolbeck R, Thoenen H . Neurotrophin release by neurotrophins: implications for activity-dependent neuronal plasticity. Proc Natl Acad Sci U S A. 1997; 94(24):13279-86. PMC: 24300. DOI: 10.1073/pnas.94.24.13279. View

15.

Ouyang Y, Rosenstein A, Kreiman G, Schuman E, Kennedy M . Tetanic stimulation leads to increased accumulation of Ca(2+)/calmodulin-dependent protein kinase II via dendritic protein synthesis in hippocampal neurons. J Neurosci. 1999; 19(18):7823-33. PMC: 6782482. View

16.

Tongiorgi E, Righi M, Cattaneo A . Activity-dependent dendritic targeting of BDNF and TrkB mRNAs in hippocampal neurons. J Neurosci. 1998; 17(24):9492-505. PMC: 6573421. View

17.

Goodman L, Valverde J, Lim F, Geschwind M, Federoff H, Geller A . Regulated release and polarized localization of brain-derived neurotrophic factor in hippocampal neurons. Mol Cell Neurosci. 1996; 7(3):222-38. DOI: 10.1006/mcne.1996.0017. View

18.

Lyford G, Yamagata K, Kaufmann W, Barnes C, Sanders L, Copeland N . Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites. Neuron. 1995; 14(2):433-45. DOI: 10.1016/0896-6273(95)90299-6. View

19.

Racca C, Gardiol A, Triller A . Dendritic and postsynaptic localizations of glycine receptor alpha subunit mRNAs. J Neurosci. 1997; 17(5):1691-700. PMC: 6573385. View

20.

TOCCO G, Willoughby D, Najm I, Pasinetti G, Thompson R, Baudry M . BDNF mRNA expression in the developing rat brain following kainic acid-induced seizure activity. Neuron. 1992; 8(6):1127-38. DOI: 10.1016/0896-6273(92)90133-x. View