Somatodendritic growth during CNS development is essential for the establishment of proper connections (Jan and Jan, 2010). In addition, the morphology of dendritic arbors is maintained and undergoes plastic changes through a process that requires activity-dependent transcription factors (TFs), protein translation, and extracellular neurotrophic factors (Sutton and Schuman, 2006; Wong and Ghosh, 2002; Yap et al., 2018).

Brain-derived neurotrophic factor (BDNF) is a well-known neurotrophin whose transcription is regulated by neuronal activity and is required for the maintenance of dendrites of adult neurons in the CNS. BDNF binds two receptors, tropomyosin kinase receptor B (TrkB) and the p75 neurotrophin receptor (p75). The classical trophic, growth-promoting actions of BDNF largely involve activation of TrkB, as mutant mice with inducible deletion of TrkB receptors exhibit a significant reduction in the number of dendritic arbors and degeneration of cortical neurons (Xu et al., 2000; Horch and Katz, 2002; Cheung et al., 2007; Yan et al., 1997; Huang and Reichardt, 2003).

Dendritic arborization mediated by TrkB activation in neurons is triggered by signaling pathways such as the ERK1/2 and the cAMP response element-binding protein (CREB) pathways (Finkbeiner et al., 1997; Xing et al., 1998; Andres-Alonso et al., 2019). CREB also mediates activity-dependent transcription by regulating early gene expression (Flavell and Greenberg, 2008; Yap and Greenberg, 2018). In addition, activation of the class 1 phosphoinositide 3-kinase (PI3K)/Akt/mammalian target of rapamycin (mTOR) pathway increases the translation of a subset of mRNAs, including those that encode proteins related to BDNF-mediated regulation of dendritic size and shape in the CNS (Takei et al., 2004; Ravindran et al., 2019; Schratt et al., 2004; Leal et al., 2014; Kumar et al., 2005; Minichiello et al., 2002; Dijkhuizen and Ghosh, 2005).

A large amount of evidence has shown that a complex of neurotrophins and neurotrophin receptors continue signaling inside the cell in specialized organelles named signaling endosomes, where neurotrophin receptors encounter specific signaling adaptors (Grimes et al., 1996; Lazo et al., 2014; Debaisieux et al., 2016). Several studies have shown that endocytosis of TrkB is required for survival, dendritic arborization, and cell migration (Zheng et al., 2008; Zhou et al., 2007), indicating that endosomal signaling has a role in the physiological responses to TrkB. Consistent with these observations, studies from our laboratory have shown that there is a functional relationship between BDNF/TrkB signaling and the early recycling pathway in the regulation of dendritic morphology and CREB-dependent transcription of plasticity genes (Lazo et al., 2013; Moya-Alvarado et al., 2018; González-Gutiérrez et al., 2020).

Long-distance communication between neurotrophins in the target tissue and cell bodies has been described in the PNS and requires microtubule-associated molecular motors, such as cytoplasmic dynein (Lazo et al., 2014; Reck-Peterson et al., 2018). During this process, NGF/TrkA signaling endosomes originating from the synaptic terminal propagate distal neurotrophin signals to the nucleus to allow transcriptional regulation, inducing neuronal survival (Cosker and Segal, 2014; Scott-Solomon and Kuruvilla, 2018; Riccio et al., 1997). Although it has been shown that BDNF is retrogradely transported along axons of cortical neurons, whether central neurons respond to distal neurotrophic signals is a relevant and understudied question in the neurobiology field. Indeed, no studies have directly assessed whether axonal BDNF signaling endosomes induce long-distance effects (Zhao et al., 2014; Olenick et al., 2019; Zhou et al., 2012; Stuardo et al., 2020; Cohen et al., 2011). Here, we studied whether axonal BDNF/TrkB signaling has a dendritic growth-promoting effect in the cell bodies of cortical neurons. We demonstrated for the first time that dynein-mediated transport of BDNF/TrkB signaling endosomes can modulate neuronal morphology. We also explored the BDNF/TrkB downstream signaling mechanism that regulates this process and showed that axonal BDNF-TrkB signaling endosomes coordinate the phosphorylation of CREB and PI3K-mTOR pathway-related proteins in cell bodies to increase protein translation and dendritic branching.

In this study, we demonstrated, using microfluidic chambers and compartmentalized cultures derived from different mouse mutants, that BDNF/TrkB signaling endosomes are transported along the axons of cortical neurons in a dynein- and TrkB-dependent manner to regulate dendritic arborization. Although long-distance communication between neurotrophins in the PNS has been well described (Cosker and Segal, 2014; Scott-Solomon and Kuruvilla, 2018; Harrington and Ginty, 2013), whether signaling endosomes have a physiological role in the CNS in mammals, have not been addressed before. Our current study is the first to demonstrate direct evidence for BDNF long-distance signaling contributing to the shape of neuronal morphology in CNS neurons. We showed that this effect depends mainly on the activity of TrkB and not p75 in axons. Additionally, we positioned CREB activity as the central mediator of this effect. In PNS neurons, CREB activity has been associated mainly with neuronal survival and axonal growth induced by target-derived NGF (Harrington and Ginty, 2013) and in injured neurons to the increase in neuronal regeneration (Caracciolo et al., 2018). However, our study is the first to indicate that CREB activity, in the context of BDNF long-distance signaling, is mainly associated with BDNF-induced dendritic growth and not survival. Furthermore, our findings are the first to demonstrate that axonal BDNF and endogenous active TrkB are in signaling endosomes in cell bodies where their activity is required to propagate axonal BDNF signals to the nuclei of cortical neurons. Also, our work is the first report showing that BDNF/TrkB signaling endosomes generated in axons activate mTOR downstream effectors and increase general protein translation, including Arc, upon reaching the cell body. This last activity depended on CREB and mTOR, indicating that axonal signaling endosomes control the transcription and translation of a subset of proteins.

In this study, we have favored pharmacological inhibitors of the different components of downstream BDNF/TrkB signaling over genetic tools. The various drugs used allowed us to inhibit enzymatic or biological activities in a localized manner, that is, in the compartment of cell bodies or the axonal compartment of microfluidic cultures, since current genetic tools do not allow this type of evaluation. Complementary reagents were used to address the limitation in specificity that implies the use of drugs. For example, to evaluate axonal TrkB’s participation in dendritic arborization induced by axonal BDNF we studied rat cultures using the Trks inhibitor K252A and in TrkBF616A knock-in mice cultures, the 1NM-PP1 kinase inhibitor. KG501 and a CREB dominant negative were used to assess CREB involvement. Finally, to evaluate the activation of p4EBP1 in cell bodies in the retrograde signaling of BDNF, the PI3K inhibitor LY294002 and mTOR inhibitor Torin 1 were used. In these experiments, the inhibitors abolished immunofluorescence, indicating a high specificity, at least for the evaluated substrate. Undoubtedly, pharmacological inhibitors have an explicit limitation of selectivity. There is still room for the development of inhibitors that can be used to assess local activities in neuronal cells, such as optogenetic inhibition, as it has been used for RabGTPases and the TrkA receptor (Khamo et al., 2019; Nguyen et al., 2016; Cornejo et al., 2020).

In this study, we clearly showed that BDNF/TrkB signaling endosomes originating in axons are required for dendritic arborization from the cell body. Our studies are in line with previous work showing that snapin, a protein that regulates autophagy and dynein transport, is required for dendritic branching in cortical neurons upon BDNF stimulation (Cheng et al., 2015; Zheng et al., 2008; Zhou et al., 2012) and with the fact that BDNF/TrkB signaling endosomes generated in presynaptic boutons in the hippocampus locally regulate neurotransmitter release (Andres-Alonso et al., 2019). Additionally, our results are related to the retrograde effects of BDNF on dendritic arborization observed in vivo in retinal ganglion cells in Xenopus laevis (Lom et al., 2002).

Using TrkB^F616A knock-in mice and 1NM-PP1, we showed that the application of BDNF to axons increases the transport of activated TrkB to the cell body and that activated somatic TrkB in neurons is required for nuclear responses. The fact that 1NM-PP1 reduced the activation of already activated TrkB suggests that 1NM-PP1 binds the ATP-binding site of the receptor, reducing the tyrosine activity of TrkB without affecting its neurotrophin binding (Chen et al., 2005). There are two possible mechanisms that can explain our results. The first is that TrkB is phosphorylated and dephosphorylated during its transport along the axon; thus, 1NM-PP1 binds the ATP-binding cassette of the receptor and prevents its phosphorylation. Our finding of signaling endosomes containing axonal BDNF and active TrkB in cell bodies supports this possibility (Figure 6). Similar results were found in sympathetic neurons, where TrkA activated in distal axons is required to induce neuronal survival by axonal NGF (Ye et al., 2003). The second possible mechanism is that BDNF retrograde signaling promotes the phosphorylation of somatodendritic TrkB and that this process is required to maintain CREB phosphorylation. In agreement with this last idea, other groups have shown that retrogradely transported TrkA in sympathetic neurons locally accumulates in the somatodendritic compartment. The process increases the phosphorylation of other TrkA receptors in cell bodies (Lehigh et al., 2017; Yamashita et al., 2017). In addition, we also observed activated TrkB receptors positive vesicles not containing BDNF in axonally stimulated cortical neurons in our studies (unpublished observation). These results suggest that axonal BDNF/TrkB signaling endosomes are required to propagate BDNF signaling in cell bodies, which includes activating the cell body TrkB receptors.

Since BDNF can bind p75 and TrkB, we analyzed whether long-distance signaling is dependent on TrkB activation and the dependence of this process on p75 expression. p75 signaling has been reported to have an opposite role as Trk signaling since p75 can induce apoptosis or reduce axonal growth by binding to different ligands and receptors (Ibáñez and Simi, 2012; Kraemer et al., 2014; Pathak et al., 2021). Additionally, p75 negatively regulates dendritic complexity and spine density in hippocampal neurons (Zagrebelsky et al., 2005). We observed that the absence of p75 resulted in a decrease in basal dendritic arborization of cortical neurons in microfluidic devices. Nevertheless, BDNF was able to rescue this phenotype, suggesting that p75 participates in the regulation of dendritic arborization but is not required for axonal BDNF signaling.

We found that PI3K activity in axons does not play a role in the retrograde transport of signaling endosomes. It was speculated that PI3K plays a role in this process due to the role of phosphoinositide accumulation in early endosome-mediated regulation of the early-to-late transition process (transition of Rab5- to Rab7-positive endosomes; Numrich and Ungermann, 2014) required for retrograde sorting of signaling endosomes in motoneurons (Deinhardt et al., 2006). Our results are also different from findings regarding TrkA signaling in sympathetic neurons, as PI3K activity is required for the retrograde transport of TrkA signals (Kuruvilla et al., 2000). Nonetheless, the PI3K-mTOR signaling pathway is required for somatic responses to axonal BDNF. Indeed, our studies showed that PI3K activity is required for axonal BDNF-induced dendritic branching and phosphorylation of 4E-BP1 and S6r, which are downstream targets of mTOR, a process that is also dynein dependent. Consistent with these results, we demonstrated that axonal signaling endosomes activate the general translation of proteins in the cell body and that this process is dependent on CREB-mediated transcription and mTOR-dependent translation. These processes are accompanied by an increase in the protein levels of Arc. The fact that protein translation is also dependent on CREB suggests that CREB-dependent transcripts are specifically translated upon the arrival of signaling endosomes in the cell body in an mTOR-dependent fashion. Arc mRNA is anterogradely transported to dendrites to be locally synthesized (Steward and Worley, 2002), suggesting that axonal signaling may increase local translation in dendrites.

We performed a time-course study of CREB activation after application of BDNF to axons and found sustained activation of CREB after 3 hr of BDNF treatment. These results are different from what we have observed in noncompartmentalized hippocampal neurons, as CREB activity is decreased in these cells after 1 hr of BDNF treatment (González-Gutiérrez et al., 2020). While a dynein inhibitor reduced early activation of CREB by 40%, it reduced late CREB activation (after 3 hr of BDNF treatment) by 80%, suggesting that there is an additional component that contributes to the early activation of CREB by axonal BDNF in our study. In injured PNS neurons it has been observed calcium waves, as mediator of the nuclear regenerative response (Cho et al., 2013). It is possible that similar calcium waves are contributing to early CREB activation by axonal BDNF in our studies. Interestingly, it has been reported that both rapid and sustained CREB phosphorylation is required for proper transcriptional regulation (Dolmetsch et al., 2001), suggesting that in neurons, retrograde BDNF signaling may contribute to sustained CREB phosphorylation for CREB-dependent maintenance of dendritic arborization.

CREB plays a central role in processes such as learning and memory (Finkbeiner et al., 1997; Xing et al., 1998; Lonze and Ginty, 2002). Indeed, mutations in several coregulators or downstream TFs are associated with genetic diseases leading to autism and cognitive disabilities (Lyu et al., 2016; Zhou et al., 2016; McGirr et al., 2016; Wang et al., 2018). Several studies have suggested that axonal BDNF can activate CREB in the cell body Zhou et al., 2012; Watson et al., 1999; Deinhardt et al., 2006; Lazo et al., 2014; however, no studies have addressed the physiological role of CREB activation induced by axonal BDNF signaling. In this work, we showed that CREB is required for long-distance BDNF-induced dendritic arborization in cortical neurons, suggesting that axonal BDNF signaling may contribute to the development and maintenance of different circuits in the brain, including those involved in learning and memory in the hippocampus and motor learning in the cortico-callosal and cortico-striatal pathways (Andreska et al., 2020; Barco et al., 2005; Yap and Greenberg, 2018).

Several studies have shown that CREB is required for the development of dendrites in vitro or during development (Redmond et al., 2002; Kwon et al., 2011; Herzog et al., 2020; González-Gutiérrez et al., 2020). In our studies, we showed that as observed in mice with conditional deletion of TrkB in cortical neurons (Huang and Reichardt, 2003), reduced CREB activity was required for the dendritic maintenance of pyramidal cells. This is consistent with a report indicating that CREB is required for cortical circuit plasticity after stroke (Caracciolo et al., 2018). However, the role of BDNF long-distance signaling regulating CREB activation in vivo remains to be demonstrated.

Together, our results demonstrate that BDNF/TrkB signaling endosomes in axons can coordinate CREB-dependent transcription and mTOR-dependent protein translation in the cell body, likely wiring circuits in the CNS.

All data generated or analyzed during the study are included in the manuscript as supporting file; Source Data have been provided for Figures 1 to Figure 9 and for Figure 3-figure supplement 1 to Figure 8-figure supplement 1.

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Author details

1. Guillermo Moya-Alvarado

   Department of Physiology, Faculty of Biological Sciences and Center for Aging and Regeneration), Pontificia Universidad Católica de Chile. Av. Libertador Bernardo O´Higgins, Santiago, Chile

   Present address

   Department of Biology, Johns Hopkins University, Baltimore, United States

   Contribution

   Conceptualization, Investigation, Methodology, Writing – original draft, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-1948-2156

2. Reynaldo Tiburcio-Felix

   NeuroSignaling Lab (NESLab), Center for Aging and Regeneration (CARE-UC), Institute of Biomedical Sciences (ICB), Faculty of Medicine, and Faculty of Life Sciences, Universidad Andrés Bello, Santiago, Chile

   Contribution

   Investigation

   Competing interests

   No competing interests declared

3. María Raquel Ibáñez

   NeuroSignaling Lab (NESLab), Center for Aging and Regeneration (CARE-UC), Institute of Biomedical Sciences (ICB), Faculty of Medicine, and Faculty of Life Sciences, Universidad Andrés Bello, Santiago, Chile

   Contribution

   Investigation

   Competing interests

   No competing interests declared

4. Alejandro A Aguirre-Soto

   NeuroSignaling Lab (NESLab), Center for Aging and Regeneration (CARE-UC), Institute of Biomedical Sciences (ICB), Faculty of Medicine, and Faculty of Life Sciences, Universidad Andrés Bello, Santiago, Chile

   Contribution

   Investigation

   Competing interests

   No competing interests declared

5. Miguel V Guerra

   1. Department of Physiology, Faculty of Biological Sciences and Center for Aging and Regeneration), Pontificia Universidad Católica de Chile. Av. Libertador Bernardo O´Higgins, Santiago, Chile
   2. NeuroSignaling Lab (NESLab), Center for Aging and Regeneration (CARE-UC), Institute of Biomedical Sciences (ICB), Faculty of Medicine, and Faculty of Life Sciences, Universidad Andrés Bello, Santiago, Chile

   Contribution

   Investigation, Methodology

   Competing interests

   No competing interests declared

6. Chengbiao Wu

   Department of Neurosciences, University of California, San Diego, San Diego, United States

   Contribution

   Supervision, Methodology

   Competing interests

   No competing interests declared

7. William C Mobley

   Department of Neurosciences, University of California, San Diego, San Diego, United States

   Contribution

   Conceptualization, Supervision

   Competing interests

   No competing interests declared

8. Eran Perlson

   Department of Physiology and Pharmacology, Sackler Faculty of Medicine; Sagol School of Neuroscience, Tel Aviv University, Tel Aviv, Israel

   Contribution

   Supervision, Methodology

   Competing interests

   No competing interests declared

9. Francisca C Bronfman

   NeuroSignaling Lab (NESLab), Center for Aging and Regeneration (CARE-UC), Institute of Biomedical Sciences (ICB), Faculty of Medicine, and Faculty of Life Sciences, Universidad Andrés Bello, Santiago, Chile

   Contribution

   Conceptualization, Data curation, Supervision, Funding acquisition, Writing – original draft, Project administration, Writing – review and editing

   For correspondence

   francisca.bronfman@unab.cl

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-3716-8443

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