Ca2+ Regulation of Dynamin-Independent Endocytosis in Cortical Astrocytes

Jiang, Min; Chen, Gong

doi:10.1523/jneurosci.6139-08.2009

Cited by 44 publications

(45 citation statements)

References 78 publications

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“…Importantly, dynamin-independent endocytotic routes have been described in different cell types, e.g. in astrocytes, as the major pathway that is tightly regulated by cytosolic Ca 2ϩ concentration and rab5 (42). Moreover, a dynamin-but Ca 2ϩ -independent endocytic mechanism was described in DRG neurons.…”

Section: Discussionmentioning

confidence: 99%

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Agonist- and Ca2+-dependent Desensitization of TRPV1 Channel Targets the Receptor to Lysosomes for Degradation

Sanz-Salvador

Andrés-Bordería

Ferrer‐Montiel

et al. 2012

Journal of Biological Chemistry

132

121

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Background:The contribution of TRPV1 trafficking to vanilloid-induced desensitization and tachyphylaxis remains unexplored. Results: Agonist exposure promotes TRPV1 internalization and degradation in nociceptors and HEK293 cells, in a time-, dose-, and Ca 2ϩ -dependent manner. Conclusion: Agonist-induced TRPV1 internalization and degradation notably contribute to long-term nociceptor desensitization. Significance: Modulation of surface TRPV1 levels could be a therapeutic approach for pain treatment.

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Section: Discussionmentioning

confidence: 99%

“…Moreover, a dynamin-but Ca 2ϩ -independent endocytic mechanism was described in DRG neurons. It was promoted by high frequency or extreme physiological stimulation (42).…”

Section: Discussionmentioning

confidence: 99%

Agonist- and Ca2+-dependent Desensitization of TRPV1 Channel Targets the Receptor to Lysosomes for Degradation

Sanz-Salvador

Andrés-Bordería

Ferrer‐Montiel

et al. 2012

Journal of Biological Chemistry

132

121

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“…Other reports suggested a strong dependence of endocytic events on both the osmolarity of the medium and both the sodium and calcium concentration (Daukas and Zigmond, 1985;Heuser and Anderson, 1989;Jiang and Chen, 2009). We used these features to further delineate the mechanism of angiogenin uptake in astrocyte cultures by increasing the sodium and calcium concentration and osmolarity of Neurobasal medium.…”

Section: Astroglia Take Up Angiogenin Via Clathrin-mediated Endocytosismentioning

confidence: 94%

Motoneurons Secrete Angiogenin to Induce RNA Cleavage in Astroglia

Skorupa

King²,

Aparicio³

et al. 2012

J. Neurosci.

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Amyotrophic lateral sclerosis (ALS) is an incurable neurodegenerative disorder affecting motoneurons. Mutations in angiogenin, encoding a member of the pancreatic RNase A superfamily, segregate with ALS. We previously demonstrated that angiogenin administration shows promise as a neuroprotective therapeutic in studies using transgenic ALS mice and primary motoneuron cultures. Its mechanism of action and target cells in the spinal cord, however, are largely unknown. Using mixed motoneuron cultures, motoneuron-like NSC34 cells, and primary astroglia cultures as model systems, we here demonstrate that angiogenin is a neuronally secreted factor that is endocytosed by astroglia and mediates neuroprotection in paracrine. We show that wild-type angiogenin acts unidirectionally to induce RNA cleavage in astroglia, while the ALS-associated K40I mutant is also secreted and endocytosed, but fails to induce RNA cleavage. Angiogenin uptake into astroglia requires heparan sulfate proteoglycans, and engages clathrin-mediated endocytosis. We show that this uptake mechanism exists for mouse and human angiogenin, and delivers a functional RNase output. Moreover, we identify syndecan 4 as the angiogenin receptor mediating the selective uptake of angiogenin into astroglia. Our data provide new insights into the paracrine activities of angiogenin in the nervous system, and further highlight the critical role of non-neuronal cells in the pathogenesis of ALS.

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“…Short exposure of mouse cortical astrocytes in culture to micromolar concentrations of FM4-64 (6.7 M, 2 min) at room temperature (RT) followed by a 10-min wash showed the expected FM4-64 puncta (14,18,19) associated with a diffuse labeling. Rupturing the PM in zero extracellular Ca 2ϩ concentration ([Ca 2ϩ ] o ) reduced the diffuse labeling without affecting the puncta (Fig.…”

Section: Endocytosis Is Not a Major Mechanism For Astrocytic Fm4-64 Umentioning

confidence: 99%

“…Their activity-dependent uptake and destaining has made them common probes for synaptic vesicle cycling at the nerve terminals (9-11). Cultured astrocytes internalize FM dyes (3,(12)(13)(14)(15)(16)(17)(18). However, this uptake is not modified by the activation of metabotropic glutamate receptors (19), and its mechanism remains elusive.…”

mentioning

confidence: 99%

FM dyes enter via a store-operated calcium channel and modify calcium signaling of cultured astrocytes

Hérault

Oheim

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

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The amphiphilic fluorescent styryl pyridinium dyes FM1-43 and FM4-64 are used to probe activity-dependent synaptic vesicle cycling in neurons. Cultured astrocytes can internalize FM1-43 and FM4-64 inside vesicles but their uptake is insensitive to the elevation of cytosolic calcium (Ca 2؉ ) concentration and the underlying mechanism remains unclear. Here we used total internal reflection fluorescence microscopy and pharmacological tools to study the mechanisms of FM4-64 uptake into cultured astrocytes from mouse neocortex. Our data show that: (i) endocytosis is not a major route for FM4-64 uptake into astrocytes; (ii) FM4-64 enters astrocytes through an aqueous pore and strongly affects Ca 2؉ homeostasis; (iii) partitioning of FM4-64 into the outer leaflet of the plasma membrane results in a facilitation of store-operated Ca 2؉ entry (SOCE) channel gating; (iv) FM4-64 permeates and competes with Ca 2؉ for entry through a SOCE channel; (v) intracellular FM4-64 mobilizes Ca 2؉ from the endoplasmic reticulum stores, conveying a positive feedback to activate SOCE and to sustain dye uptake into astrocytes. Our study demonstrates that FM dyes are not markers of cycling vesicles in astrocytes and calls for a careful interpretation of FM fluorescence.calcium homeostasis ͉ endoplasmic reticulum ͉ lipid bilayer ͉ styryl dye ͉ TIRF I n astrocytes the strong expression of the plasma membrane (PM) store-operated Ca 2ϩ entry (SOCE) (1-4) contrasts with a relatively small expression of voltage-gated channels and AMPA/ NMDA ligand-gated channels that are mostly expressed by neurons. In response to neuronal activity and neurotransmitter release, the activation of astroglial metabotropic receptors induces a reduction of the endoplasmic reticulum (ER) Ca 2ϩ concentration ([Ca 2ϩ ] ER ) that leads to the activation of the SOCE and to an elevation of the intracellular Ca 2ϩ concentration ([Ca 2ϩ ] i ) (4) that is critical for the electrically silent astrocytes to release gliotransmitters and control nearby neurons, glia, and blood vessels (5). The type 1-2 stromal interaction molecules (STIM1-2) and Orai1-3 membrane proteins are key components of the SOCE, being the ER Ca 2ϩ sensor and the PM pore-forming subunit, respectively (6, 7). A possible participation of the classical transient receptor potential (TRPC) channels to the protein complex generating the SOCE is debated in several cell types (8), including astrocytes (3).Styryl pyridinium FM dyes are amphiphilic molecules that reversibly partition in lipid membranes. Their positively charged pyridinium head prevents them from diffusing through the PM. Only weakly fluorescent in aqueous solution their quantum yield increases in a lipid environment. Their activity-dependent uptake and destaining has made them common probes for synaptic vesicle cycling at the nerve terminals (9-11). Cultured astrocytes internalize FM dyes (3,(12)(13)(14)(15)(16)(17)(18). However, this uptake is not modified by the activation of metabotropic glutamate receptors (19), and its mechanism remains elusiv...

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Ca2+ Regulation of Dynamin-Independent Endocytosis in Cortical Astrocytes

Cited by 44 publications

References 78 publications

Agonist- and Ca2+-dependent Desensitization of TRPV1 Channel Targets the Receptor to Lysosomes for Degradation

Agonist- and Ca2+-dependent Desensitization of TRPV1 Channel Targets the Receptor to Lysosomes for Degradation

Motoneurons Secrete Angiogenin to Induce RNA Cleavage in Astroglia

FM dyes enter via a store-operated calcium channel and modify calcium signaling of cultured astrocytes

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