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Review
. 2013:71:149-79.
doi: 10.1016/B978-0-12-407870-3.00007-X.

Contribution and regulation of TRPC channels in store-operated Ca2+ entry

Affiliations
Review

Contribution and regulation of TRPC channels in store-operated Ca2+ entry

Kwong Tai Cheng et al. Curr Top Membr. 2013.

Abstract

Store-operated calcium entry (SOCE) is activated in response to depletion of the endoplasmic reticulum-Ca(2+) stores following stimulation of plasma membrane receptors that couple to PIP2 hydrolysis and IP3 generation. Search for the molecular components of SOCE channels led to the identification of mammalian transient receptor potential canonical (TRPC) family of calcium-permeable channels (TRPC1-TRPC7), which are all activated in response to stimuli that result in PIP2 hydrolysis. While several TRPCs, including TRPC1, TRPC3, and TRPC4, have been implicated in SOCE, the data are most consistent for TRPC1. Extensive studies in cell lines and knockout mouse models have established the contribution of TRPC1 to SOCE. Furthermore, there is a critical functional interaction between TRPC1 and the key components of SOCE, STIM1, and Orai1, which determines the activation of TRPC1. Orai1-mediated Ca(2+) entry is required for recruitment of TRPC1 and its insertion into surface membranes while STIM1 gates the channel. Notably, TRPC1 and Orai1 generate distinct patterns of Ca(2+) signals in cells that are decoded for the regulation of specific cellular functions. Thus, SOCE appears to be a complex process that depends on temporal and spatial coordination of several distinct steps mediated by proteins in different cellular compartments. Emerging data suggest that, in many cell types, the net Ca(2+) entry measured in response to store depletion is the result of the coordinated regulation of different calcium-permeable ion channels. Orai1 and STIM1 are central players in this process, and by mediating recruitment or activation of other Ca(2+) channels, Orai1-CRAC function can elicit rapid changes in global and local [Ca(2+)]i signals in cells. It is most likely that the type of channels and the [Ca(2+)]i signature that are generated by this process reflect the physiological function of the cell that is regulated by Ca(2+).

Keywords: Ca(2+) signaling; Cell function; Orai1; SOCE; STIM1; TRPC channels; TRPC1.

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Figures

Figure 7.1
Figure 7.1
(A) Schematic model showing the different domains of STIM1. The polybasic tail in the C-terminal end is expanded, with the lysines mediating electrostatic interactions with TRPCs in red. The negatively charged residues in the C-terminus of TRPC1, TRPC3, TRPC4, TRPC5, and TRPC6 that binds electrostatically to the lysines are also in red. The ezrin/radixin/moesin (ERM) and STIM1-Orai1-activating region (SOAR) domains are denoted in the model. SP, signaling peptide; EF, EF hand; SAM, sterile α motif; TM, transmembrane; and S/P, serine/proline-rich. (B) Model showing cellular events activated Orai1-mediated Ca2+ entry. Following depletion of the ER-Ca2+ stores, STIM1 aggregates and translocates to the ER–PM junctional regions where it binds to and activates the Orai1 channel. The Orai1-mediated Ca2+ entry may induce the trafficking of homomeric TRPC channels or heteromeric TRPC channels (e.g., TRPC1/TRPC3 and TRPC1/TRPC4) to the cell surface, following by insertion into the plasma membrane and subsequent gating by STIM1. Additionally, the extracellular Ca2+ entering via Orai1 may also directly activate other channels, such as TRPC5. ER, endoplasmic reticulum; PM, plasma membrane.
Figure 7.2
Figure 7.2
Ca2+ signaling mechanisms regulating salivary gland fluid secretion. The figure shows Ca2+-mobilizing events in acinar cells that are initiated by a stimulus and lead to fluid secretion. The coordinated regulation (spatial and temporal) of Ca2+ signaling as well as channel function (KCa, TMEM16A, AQP5 insertion) achieves fluid secretion via the apical membrane of acinar cells. Release of calcium via apically localized IP3Rs triggers the initial apical rise in cytosolic [Ca2+] (denoted in the figure as Ca2+ signal, red stellate area). The Ca2+ signal is then propagated toward the basal region of the cell. It is suggested that apically and basolaterally localized Orai1 and TRPC1 channels mediate Ca2+ entry that is critical for the maintenance of sustained elevation of [Ca2+]i which is required to drive fluid secretion.
Figure 7.3
Figure 7.3
Distinct Ca2+ signals and currents, as well as downstream cellular events associated with Orai1- and TRPC1-mediated Ca2+ entry. (A–C) Distinct Ca2+ signals induced by 1 µM CCh. The pattern shown in control cells reflects the activation of both Orai1 and TRPC1 channels. No response was seen following knockdown ofOrai1. In the case of cells lacking TRPC1, baseline oscillations were seen and these are attributed to the still functional Orai1 channel. (D–F) Activation of NFAT translocation from the cytoplasm into the nuclear (denoted by *) following store depletion. Nuclear translocation of a GFP-tagged NFAT could be clearly seen in control cells but not in cells lacking Orai1, pointing to Ca2+ entry via Orai1 as the primary determinant of NFAT activation. This was further supported by the observation of nuclear translocation of NFAT in cells lacking TRPC1, where the Orai1 channel could still be activated following store depletion. (G–I) Currents activated following store depletion. The ISOC measured in control cells is a combination of currents carried by Ca2+ entry via both TRPC1 and Orai1 channels. Loss of Orai1 expression resulted in no currents, as neither Orai1 nor TRPC1 was functional. However, an ICRAC could be seen in cells lacking TRPC1.

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