Regional Interaction of Endoplasmic Reticulum Ca<sup>2+</sup>Signals between Soma and Dendrites through Rapid Luminal Ca<sup>2+</sup>Diffusion

Choi, YoungRok; Kim, Shin Hye; Chung, Sungkwon; Uhm, Dae Yong; Park, Myoung Kyu

doi:10.1523/jneurosci.3158-06.2006

Cited by 70 publications

(55 citation statements)

References 47 publications

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“…These results suggest that Ca 2ϩ enters the cell via TRPC3 but moves into a privileged compartment associated with only a fraction of the cytosol and that this compartment is linked to net transepithelial Ca 2ϩ flux. Ca 2ϩ "tunneling" has been proposed previously in secretory epithelia and in the long dendritic processes of neurons (4,21,25,26). It will be important in future experiments to identify and perhaps image this Ca 2ϩ tunnel in the IMCD-3 cells.…”

Section: Discussionmentioning

confidence: 67%

Role of TRPC3 channels in ATP-induced Ca²⁺signaling in principal cells of the inner medullary collecting duct

Goel

Schilling

2010

American Journal of Physiology-Renal Physiology

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flux across IMCD-3 monolayers is increased by overexpression of TRPC3 and attenuated by a dominant negative TRPC3 construct, suggesting that Ca 2ϩ entry across the apical membrane occurs via TRPC3 channels. To test this hypothesis, we selectively measured the Ca 2ϩ permeability of the apical membrane of fura-2-loaded IMCD-3 cells using the Mn 2ϩ quench technique. Mn 2ϩ influx across the apical membrane was increased 12-to 16-fold by apical ATP and was blocked by the pyrazole derivative BTP2, a known inhibitor of TRPC3 channels, with an IC50 value Ͻ100 nM. In contrast, Mn 2ϩ influx was only increased ϳ2-fold by basolateral ATP. Mn 2ϩ influx was also activated by apical, but not basolateral, 1-stearoyl-2-acetyl-snglycerol (SAG), a known activator of TRPC3 channels. Apical ATPand SAG-induced Mn 2ϩ influx was increased by overexpression of TRPC3 and completely blocked by expression of the dominant negative TRPC3 construct. Mn 2ϩ influx was also stimulated ϳ2-fold by thapsigargin applied to either the apical or basolateral side. Thapsigargin-induced flux was blocked by BTP2 but was unaffected by overexpression of TRPC3 or by dominant negative TRPC3. Apical ATP, but not basolateral ATP, increased transepithelial 45 Ca 2ϩ flux. These results demonstrate that the apical membrane of IMCD-3 cells has two distinct Ca 2ϩ influx pathways: 1) a store-operated channel activated by thapsigargin and basolateral ATP and 2) TRPC3 channels activated by apical ATP. Only activation of TRPC3 leads to net transepithelial apical-to-basolateral Ca 2ϩ flux. Furthermore, these results demonstrate that native TRPC3 is not a store-operated channel in IMCD-3 cells. calcium channels; transient receptor potential channel; fluorescence microscopy; fura 2; manganese quench; inner medullary collecting duct cell line IMCD-3IT IS NOW WELL ESTABLISHED that purinergic receptors of the P2X and P2Y subtype are present in the surface membrane of most cells, including epithelial cells of the renal nephron (1, 32). Purinergic receptors are not only present in the basolateral membrane but also are expressed in the apical membrane of renal epithelial cells, and it is now clear that autocrine purinergic signaling occurs within the tubular lumen throughout the entire nephron (12). Although not fully understood, mechanisms exist for the regulated release of ATP from epithelial cells lining the tubule in response to various agonists or in response to mechanical stimulations such as the shear stress associated with the flow of tubular fluid or changes in membrane stretch associated with hyper-and hypotonicity (12, 28). The enzymes responsible for degradation of ATP, i.e., ectonucleotidases, are also differentially expressed in the apical membrane along the nephron (29). Thus, although the physiological roles of purinergic signaling in the tubular lumen are only slowly coming to light, mechanisms for both the activation and inactivation of this signaling pathway clearly exist within the nephron. There is also increasing evidence that purinergic signaling plays an ...

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Section: Discussionmentioning

confidence: 67%

Role of TRPC3 channels in ATP-induced Ca²⁺signaling in principal cells of the inner medullary collecting duct

Goel

Schilling

2010

American Journal of Physiology-Renal Physiology

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“…This result suggests a continuous ER membrane structure exists. ER continuity also exists between soma and dendrites in rat midbrain (48). Dendritic portions of the ER could be replenished by Ca 2ϩ moving from the soma via a luminally continuous ER (48).…”

Section: Discussionmentioning

confidence: 97%

A Single Luminally Continuous Sarcoplasmic Reticulum with Apparently Separate Ca2+ Stores in Smooth Muscle

McCarron

Olson

2008

Journal of Biological Chemistry

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In smooth muscle, the endoplasmic reticulum (ER) 2 exists as an extensive membrane network of tubules, flattened cisternae, and vesicles (1, 2) to comprise rough (RER, which carries ribosomes) and smooth (SER) reticula. RER predominates around the nucleus and is scattered throughout the cytoplasm and appears to be in luminal continuity with the SER (1, 3, 4). SER is found mainly near the cell surface to run in close apposition to the plasma membrane. In various tissues, changes in ER structure may occur at different developmental stages and when the cells experience prolonged activation (reviewed in Ref. 5). These changes may give the impression of a labile (pleiomorphic) ER network capable of modifications in structure and, consequently, function.The Ca 2ϩ storage element of the ER, the sarcoplasmic reticulum (SR), may be a specialized region of the SER that is endowed with those proteins responsible for the uptake (Ca 2ϩ pumps), storage (calsequestrin), and release ryanodine receptor ((RyR) and inositol 1,4,5-trisphosphate receptor (IP 3 R)) of Ca 2ϩ (4, 6). The SR, by regulating the cytoplasmic Ca 2ϩ concentration ([Ca 2ϩ ] c ), plays a central role in Ca 2ϩ signaling to contribute to activities such as gene expression, growth, contraction, and cell death (reviewed in Refs. 7-10). In determining the qualitative nature of the biological response, the structural arrangement of the SR through the cell may be instrumental in enabling different functions to occur and proceed from various regions of the cell. For example, the SR, as a series of multiple, separate Ca 2ϩ -storage elements, each with their own limited measure of Ca 2ϩ , may explain localized all-or-none responses in restricted regions of the cell, the graded release of Ca 2ϩ from the SR in the "quantal" release process and the various sensitivities to IP 3 measured throughout the cell (11-15). Yet, whether or not the SR exists as multiple separate Ca 2ϩ storage units or as a single luminally continuous entity in which Ca 2ϩ diffuses freely throughout, is unclear.Evidence for the existence of multiple Ca 2ϩ storage units comes from the heterogeneity of the SR in its Ca 2ϩ handling capacity in smooth muscle (1, 4, 16). The SR near the center of the cells may be depleted less readily of its Ca 2ϩ than that of peripherally located SR (1) and x-ray microprobe analysis revealed Ca 2ϩ -rich spots in the central and peripheral SR in portal vein and taenia coli (17, 18). Calsequestrin was not uniformly distributed through the SR network but clustered preferentially at sites most often within the peripheral SR (4). These calsequestrin-rich elements of the SR were also enriched with IP 3 R (4). This evidence provides a morphological basis for the existence of various arrangements of Ca 2ϩ release channels. The SR Ca 2ϩ stores have been classified on the basis of the arrangement of IP 3 R and RyR and conflicting evidence exists regarding their number and receptor arrangement. To determine the organization of the SR Ca 2ϩ stores, in native cells, the predominant...

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“…Neuronal ER forms a continuous network extending from the soma to axons and presynaptic release sites, as well as to dendrites and dendritic spines [128]. In SNc DA neurons, Ca 2þ from somatic ER stores is propagated through this system to dendrites [129].…”

Section: (B) Intracellular Ca 2þ Storesmentioning

confidence: 99%

Somatodendritic dopamine release: recent mechanistic insights

Rice

Patel

2015

Phil. Trans. R. Soc. B

101

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One contribution of 16 to a discussion meeting issue 'Release of chemical transmitters from cell bodies and dendrites of nerve cells'. Dopamine (DA) is a key transmitter in motor, reward and cogitative pathways, with DA dysfunction implicated in disorders including Parkinson's disease and addiction. Located in midbrain, DA neurons of the substantia nigra pars compacta project via the medial forebrain bundle to the dorsal striatum (caudate putamen), and DA neurons in the adjacent ventral tegmental area project to the ventral striatum (nucleus accumbens) and prefrontal cortex. In addition to classical vesicular release from axons, midbrain DA neurons exhibit DA release from their cell bodies and dendrites. Somatodendritic DA release leads to activation of D2 DA autoreceptors on DA neurons that inhibit their firing via G-protein-coupled inwardly rectifying K þ channels. This helps determine patterns of DA signalling at distant axonal release sites. Somatodendritically released DA also acts via volume transmission to extrasynaptic receptors that modulate local transmitter release and neuronal activity in the midbrain. Thus, somatodendritic release is a pivotal intrinsic feature of DA neurons that must be well defined in order to fully understand the physiology and pathophysiology of DA pathways. Here, we review recent mechanistic aspects of somatodendritic DA release, with particular emphasis on the Ca 2þ dependence of release and the potential role of exocytotic proteins.

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Regional Interaction of Endoplasmic Reticulum Ca²⁺Signals between Soma and Dendrites through Rapid Luminal Ca²⁺Diffusion

Cited by 70 publications

References 47 publications

Role of TRPC3 channels in ATP-induced Ca²⁺signaling in principal cells of the inner medullary collecting duct

Role of TRPC3 channels in ATP-induced Ca²⁺signaling in principal cells of the inner medullary collecting duct

A Single Luminally Continuous Sarcoplasmic Reticulum with Apparently Separate Ca2+ Stores in Smooth Muscle

Somatodendritic dopamine release: recent mechanistic insights

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Regional Interaction of Endoplasmic Reticulum Ca2+Signals between Soma and Dendrites through Rapid Luminal Ca2+Diffusion

Cited by 70 publications

References 47 publications

Role of TRPC3 channels in ATP-induced Ca2+signaling in principal cells of the inner medullary collecting duct

Role of TRPC3 channels in ATP-induced Ca2+signaling in principal cells of the inner medullary collecting duct

A Single Luminally Continuous Sarcoplasmic Reticulum with Apparently Separate Ca2+ Stores in Smooth Muscle

Somatodendritic dopamine release: recent mechanistic insights

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Resources

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Regional Interaction of Endoplasmic Reticulum Ca²⁺Signals between Soma and Dendrites through Rapid Luminal Ca²⁺Diffusion

Role of TRPC3 channels in ATP-induced Ca²⁺signaling in principal cells of the inner medullary collecting duct

Role of TRPC3 channels in ATP-induced Ca²⁺signaling in principal cells of the inner medullary collecting duct