The Serine/Threonine Kinase Ndr2 Controls Integrin Trafficking and Integrin-Dependent Neurite Growth
Open accessAbstract
Integrins have been implicated in various processes of nervous system development, including proliferation, migration, and differentiation of neuronal cells. In this study, we show that the serine/threonine kinase Ndr2 controls integrin-dependent dendritic and axonal growth in mouse hippocampal neurons. We further demonstrate that Ndr2 is able to induce phosphorylation at the activity- and trafficking-relevant site Thr(788/789) of β1-integrin to stimulate the PKC- and CaMKII-dependent activation of β1-integrins, as well as their exocytosis. Accordingly, Ndr2 associates with integrin-positive early and recycling endosomes in primary hippocampal neurons and the surface expression of activated β1-integrins is reduced on dendrites of Ndr2-deficient neurons. The role of Ndr2 in dendritic differentiation is also evident in vivo, because Ndr2-null mutant mice show arbor-specific alterations of dendritic complexity in the hippocampus. This indicates a role of Ndr2 in the fine regulation of dendritic growth; in fact, treatment of primary neurons with Semaphorin 3A rescues Ndr2 knock-down-induced dendritic growth deficits but fails to enhance growth beyond control level. Correspondingly, Ndr2-null mutant mice show a Semaphorin 3A(-/-)-like phenotype of premature dendritic branching in the hippocampus. The results of this study show that Ndr2-mediated integrin trafficking and activation are crucial for neurite growth and guidance signals during neuronal development.
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T788/789 phosphorylation promotes the recognition of integrin substrates such as fibronectin.
“promotes the recognition of integrin substrates such as fibronectin”
From The Serine/Threonine Kinase <scp>NDR2</scp> Regulates Integrin Signaling, Synapse Formation, and Synaptic Plasticity in the Hippocampus (2025) · cites this paper as Rehberg et al. 2014
The Results section (‘Ndr2 controls β1-integrin phosphorylation at Thr 788/789’; page unavailable) reports increased phosphorylation at that site, and the Discussion links the motif to proteins involved in integrin activation. The paper uses fibronectin-coated cultures, but does not show that Thr 788/789 phosphorylation promotes recognition of fibronectin; the Discussion says a high-affinity conformation also requires intracellular binding partners. (LLM, conf=0.82)
Experimental — accuracy not yet measuredIn an in vitro kinase assay targeting the β1 integrin cytoplasmic tail as substrate, there is no direct phosphorylation of β1 integrin by NDR kinases.
“there is no direct phosphorylation of the β1 integrin by NDR kinases”
From The Serine/Threonine Kinase <scp>NDR2</scp> Regulates Integrin Signaling, Synapse Formation, and Synaptic Plasticity in the Hippocampus (2025) · cites this paper as Rehberg et al. 2014
The section “Ndr2 controls β1-integrin phosphorylation at Thr 788/789” reports that Ndr2 did not directly phosphorylate the β1-integrin cytoplasmic domain in an in vitro kinase assay; the Figure 4 caption reports the same result. The experiments described test Ndr2, not NDR kinases generally, so the plural wording extends beyond what this source establishes. (LLM, conf=0.85)
Experimental — accuracy not yet measuredPhosphorylation of β1 integrin by NDR kinases requires Calcium-calmodulin kinase II and Protein kinase C activity.
“a requirement Calcium‐calmodulin kinase II and Protein kinase C activity (Rehberg et al. 2014)”
From The Serine/Threonine Kinase <scp>NDR2</scp> Regulates Integrin Signaling, Synapse Formation, and Synaptic Plasticity in the Hippocampus (2025) · cites this paper as Rehberg et al. 2014
The ‘Ndr2 controls β1-integrin phosphorylation at Thr 788/789’ section reports that Ndr2-induced phosphorylation in HEK-293T cells was sensitive to CaMKII and PKC inhibitors. It also reports that Ndr2 did not phosphorylate β1-integrin directly; the finding concerns Ndr2, not NDR kinases generally. (LLM, conf=0.84)
Experimental — accuracy not yet measuredIn developing neurons, the dendritic growth effects of NDR2 are at least in part mediated by control of intracellular trafficking and recycling of β1 integrins.
“In developing neurons, the dendritic growth effects of NDR2 are at least in part mediated by a control in the intracellular trafficking and recycling of β1 integrins (Rehberg et al. 2014; Demiray et al. 2018).”
From The Serine/Threonine Kinase <scp>NDR2</scp> Regulates Integrin Signaling, Synapse Formation, and Synaptic Plasticity in the Hippocampus (2025) · cites this paper as Rehberg et al. 2014
Sample size was estimated according to similar work published by the group previously.
“No power analysis was performed, but the sample size was estimated according to similar work published by our group previously (Madencioglu 2019; Rehberg et al. 2014; Madencioglu et al. 2021; Hayani et al. 2018).”
From The Serine/Threonine Kinase <scp>NDR2</scp> Regulates Integrin Signaling, Synapse Formation, and Synaptic Plasticity in the Hippocampus (2025) · cites this paper as Rehberg et al. 2014
NDR2 contributes to the T788/789 phosphorylation of the β1 integrin cytoplasmic tail.
“We previously observed that NDR2 contributes to the T788/789 phosphorylation of β1 integrin cytoplasmic tail (Rehberg et al. 2014)”
From The Serine/Threonine Kinase <scp>NDR2</scp> Regulates Integrin Signaling, Synapse Formation, and Synaptic Plasticity in the Hippocampus (2025) · cites this paper as Rehberg et al. 2014
Stimulation of NDR2 activity leads to T788/789 phosphorylation of β1 integrins.
“While stimulation of NDR2 activity leads to T788/789 phosphorylation of β1 integrins, this phosphorylation appears to be indirect.”
From The Serine/Threonine Kinase <scp>NDR2</scp> Regulates Integrin Signaling, Synapse Formation, and Synaptic Plasticity in the Hippocampus (2025) · cites this paper as Rehberg et al. 2014
NDR2 controls integrin-dependent neurite growth.
“We previously demonstrated that NDR2 controls integrin‐dependent neurite growth and integrin trafficking, and its expression modulates the phosphorylation levels of T788/789 on the β1 integrin subunit (Rehberg et al. 2014)”
From The Serine/Threonine Kinase <scp>NDR2</scp> Regulates Integrin Signaling, Synapse Formation, and Synaptic Plasticity in the Hippocampus (2025) · cites this paper as Rehberg et al. 2014
NDR2 controls integrin trafficking.
“We previously demonstrated that NDR2 controls integrin‐dependent neurite growth and integrin trafficking, and its expression modulates the phosphorylation levels of T788/789 on the β1 integrin subunit (Rehberg et al. 2014)”
From The Serine/Threonine Kinase <scp>NDR2</scp> Regulates Integrin Signaling, Synapse Formation, and Synaptic Plasticity in the Hippocampus (2025) · cites this paper as Rehberg et al. 2014
T788/789 phosphorylation ultimately enhances neurite outgrowth.
“ultimately enhancing neurite outgrowth (Rehberg et al. 2014)”
From The Serine/Threonine Kinase <scp>NDR2</scp> Regulates Integrin Signaling, Synapse Formation, and Synaptic Plasticity in the Hippocampus (2025) · cites this paper as Rehberg et al. 2014
T788/789 phosphorylation increases the recruitment of β1 integrins to the cell surface.
“increases the recruitment of β1 integrins to the cell surface”
From The Serine/Threonine Kinase <scp>NDR2</scp> Regulates Integrin Signaling, Synapse Formation, and Synaptic Plasticity in the Hippocampus (2025) · cites this paper as Rehberg et al. 2014
NDR2 expression modulates phosphorylation levels of T788/789 on the β1 integrin subunit.
“its expression modulates the phosphorylation levels of T788/789 on the β1 integrin subunit (Rehberg et al. 2014)”
From The Serine/Threonine Kinase <scp>NDR2</scp> Regulates Integrin Signaling, Synapse Formation, and Synaptic Plasticity in the Hippocampus (2025) · cites this paper as Rehberg et al. 2014
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Kindlins: essential regulators of integrin signalling and cell-matrix adhesion
Larjava, H., Plow, E. F., & Wu, C. (2008) · The EMBO Reports · doi:10.1038/embor.2008.202 · Cited by 268 · see citing works
Neuronal Functions of the Novel Serine/Threonine Kinase Ndr2
Stork, O., Zhdanov, A., Kudersky, A., Yoshikawa, T., Obata, K., & Pape, H.-C. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m403552200 · Cited by 55 · see citing works
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Cited by
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Madencioglu, D. A., Çalışkan, G., Yuanxiang, P., Rehberg, K., Demiray, Y. E., Kul, E., Engler, A., Hayani, H., Bergado-Acosta, J. R., Kummer, A., et al. (2021) · iScience · doi:10.1016/j.isci.2021.102868 · Cited by 8 · see citing works
Self-citationdel Ángel, M., Tsutiya, A., Hayani, H., Madencioglu, D., Kul, E., Caliskan, G., Demiray, Y. E., Dityatev, A., & Stork, O. (2025) · Journal of Neurochemistry · doi:10.1111/jnc.70094 · Cited by 1 · see citing works
“In mammals, the two NDR isoforms NDR1 ( Stk38 ) and NDR2 ( Stk38l ) have been implicated in neuronal development, including control of neuronal polarity and axon guidance and proliferation of neuronal progenitors (Ultanir et al. 2012; Rehberg et al. 2014; Yang et al. 2014).”
InfluentialSelf-citation
- Authors
- Rehberg, K., Kliche, S., Madencioglu, D. A., Thiere, M., Müller, B., Meineke, B. M., Freund, C., Budinger, E., & Stork, O.
- Affiliations
- Center for Behavioral Brain Sciences (DE)
- Otto-von-Guericke-Universität Magdeburg (DE)
- Viện Sinh học (VN)
- Leibniz-Forschungsinstitut für Molekulare Pharmakologie (DE)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2014-04-09
- Volume
- 34
- Issue
- 15
- Pages
- 5342-5354
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6609001
- OpenAlex
- W2093944536
- Cited by
- 49
- References
- 2
- Citations by year
- 2026: 1 · 2025: 5 · 2024: 2 · 2023: 5 · 2022: 6 · 2021: 6 · 2020: 1 · 2019: 5 · 2018: 7 · 2017: 2 · 2016: 4 · 2015: 4 · 2014: 1
- FWCI
- 1.68
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- European Commission
- Deutsche Forschungsgemeinschaft (GRK 1167, SFB-854)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
- Health Sciences › Medicine › Immunology and Allergy › Cell Adhesion Molecules Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- NDR2, serine/threonine kinase, integrin trafficking, beta1 integrin, integrin phosphorylation, protein kinase C, CaMKII, exocytosis, recycling endosomes, dendritic growth, axon growth, neurite guidance, hippocampal neurons, dendritic branching, semaphorin 3A, neuronal development
- MeSH terms
- Animals, Cells, Cultured, Hippocampus, Humans, Mice, Inbred C57BL, Phosphorylation, Protein Binding, Proteins, Endosomes, Neurites, PC12 Cells, Gene Deletion, Integrin beta1, Protein Transport, Semaphorin-3A, NIH 3T3 Cells, Cell Growth Processes, Adaptor Proteins, Signal Transducing, Mice, Rats, HEK293 Cells
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