Abstract
Ca2+, nitric oxide (NO), and protein kinase G (PKG) are important signaling molecules that play pivotal roles in many physiological processes such as vascular tone control, platelet activation, and synaptic plasticity. TRPC channels allow Ca2+ influx, thus contributing to the production of NO, which subsequently stimulates PKG. It has been demonstrated that PKG can phosphorylate human TRPC3 at Thr-11 and Ser-263 and that this phosphorylation inactivates TRPC3. These two PKG phosphorylation sites, Thr-11 and Ser-263 in human TRPC3, are conserved in other members of the TRPC3/6/7 subfamily, suggesting that PKG may also phosphorylate TRPC6 and TRPC7. In addition, protein kinase C (PKC) also inactivates TRPC3, partly through activating PKG. The PKG-mediated inhibition of TRPC channels may provide a feedback control for the fine tuning of [Ca2+]i levels and protect the cells from the detrimental effects of excessive [Ca2+]i and/or NO.
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References
Ahmmed GU, Mehta D, Vogel S, Holinstat M, Paria BC, Tiruppathi C, Malik AB (2004) Protein kinase Cα phosphorylates the TRPC1 channel and regulates store-operated Ca2+ entry in endothelial cells. J Biol Chem 279:20941–20949
Cohen RA, Weisbrod RM, Gericke M, Yaghoubi M, Bierl C, Bolotina VM (1999) Mechanism of nitric oxide-induced vasodilation: refilling of intracellular stores by sarcoplasmic reticulum Ca2+ ATPase and inhibition of store-operated Ca2+ influx. Circ Res 84:210–219
Corbin JD, Ogreid D, Miller JP, Suva RH, Jastorff B, Doskeland SO (1986) Studies of cGMP analog specificity and function of the two intrasubunit binding sites of cGMP-dependent protein kinase. J Biol Chem 261:1208–1214
Corbin JD, Turko IV, Beasley A, Francis SH (2000) Phosphorylation of phosphodiesterase-5 by cyclic nucleotide-dependent protein kinase alters its catalytic and allosteric cGMP-binding activities. Eur J Biochem 267:2760–2767
Dostmann WR, Taylor MS, Nickl CK, Brayden JE, Frank R, Tegge WT (2000) Highly specific, membrane-permeant peptide blockers of cGMP-dependent protein kinase Iα inhibit NO-induced cerebral dilation. Proc Natl Acad Sci USA 97:14772–14777
Feil R, Lohmann SM, de Jonge H, Walter U, Hofmann F (2003) Cyclic GMP-dependent protein kinases and the cardiovascular system. Insight from genetically modified mice. Circ Res 93:907–916
Feil R, Hofmann F, Kleppisch T (2005) Function of cGMP-dependent protein kinases in the nervous system. Rev Neurosci 16:23–42
Freichel M, Suh SH, Pfeifer A, Schweig U, Trost C, Weissgerber P, Biel M, Philipp S, Freise D, Droogmans G, Hofmann F, Flockerzi V, Nilius B (2001) Lack of an endothelial store-operated Ca2+ current impairs agonist-dependent vasorelaxation in TRP4-/- mice. Nat Cell Biol 3:121–127
Gadbois DM, Crissman HA, Tobey RA, Bradbury EM (1992) Multiple kinase arrest points in the G1 phase of nontransformed mammalian cells are absent in transformed cells. Proc Natl Acad Sci USA 89:8626–8630
Greka A, Navarro B, Oancea E, Duggan A, Clapham DE (2003) TRPC5 is a regulator of hippocampal neurite length and growth cone morphology. Nat Neurosci 6:837–845
Haslam RJ, Dickinson NT, Jang EK (1999) Cyclic nucleotides and phosphodiesterases in platelets. Thromb Haemost 82:412–423
Hassock SR, Zhu MX, Trost C, Flockerzi V, Authi KS (2002) Expression and role of TRPC proteins in human platelets: evidence that TRPC6 forms the store-independent calcium entry channel. Blood 100:2801–2811
Hisatsune C, Kuroda Y, Nakamura K, Inoue T, Nakamura T, Michikawa T, Mizutani A, Mikoshiba K (2004) Regulation of TRPC6 channel activity by tyrosine phosphorylation. J Biol Chem 279:18887–18894
Hofmann F (2005) The biology of cyclic cGMP-dependent protein kinases. J Biol Chem 280:1–4
Jungnickel MK, Marrero H, Birnbaumer L, Lemos JR, Florman HM (2001) Trp2 regulates entry of Ca into mouse sperm triggered by egg ZP3. Nat Cell Biol 3:499–502
Kim SJ, Kim YS, Yuan JP, Petralia RS, Worley PF, Linden DJ (2003) Activation of the TRPC1 cation channel by metabotropic glutamate receptor mGluR1. Nature 426:285–291
Kiselyov K, Xu X, Mozhayeva G, Kuo T, Pessah I, Mignery G, Zhu X, Birnbaumer L, Muallem S (1998) Functional interaction between InsP3 receptors and store-operated Htrp3 channels. Nature 396:478–482
Kwan HY, Huang Y, Yao X (2000) Store-operated calcium entry in vascular endothelial cells is inhibited by cGMP via a protein kinase G-dependent mechanism. J Biol Chem 275:6758–6763
Kwan HY, Huang Y, Yao X (2004) Regulation of canonical transient receptor potential isoform 3 (TRPC3) channel by protein kinase G. Proc Natl Acad Sci USA 101:2625–2630
Kwan HY, Huang Y, Yao X (2006) Protein kinase C can inhibit TRPC3 channels indirectly via stimulating protein kinase G. J Cell Physiol 207:315–321
Li Y, Jia YC, Cui K, Li N, Zheng ZY, Wang YZ, Yuan XB (2005) Essential role of TRPC channels in the guidance of nerve growth cones by brain-derived neurotrophic factor. Nature 434:894–898
Lincoln TM, Dey N, Sellak H (2001) Invited review: cGMP-dependent protein kinase signaling mechanisms in smooth muscle: from the regulation of tone to gene expression. J Appl Physiol 91:1421–1430
Minke B, Cook B (2002) TRP channel proteins and signal transduction. Physiol Rev 82:429–472
Montell C (2005) The TRP superfamily of cation channels. Sci STKE 272:re3
Ogreid D, Ekanger R, Suva RH, Miller JP, Sturm P, Corbin JD, Doskeland SO (1985) Activation of protein kinase isozymes by cyclic nucleotide analogs used singly or in combination. Principles for optimizing the isozyme specificity of analog combinations. Eur J Biochem 150:219–227
Parekh AB, Putney Jr JW (2005) Store depletion and calcium influx. Physiol Rev 85:757–810
Pearson RB, Kemp BE (1991) Protein kinase phosphorylation site sequences and consensus specificity motif: tabulations. Methods Enzymol 200:62–81
Schwede F, Maronde E, Genieser H, Jastorff B (2000) Cyclic nucleotide analogs as biochemical tools and prospective drugs. Pharmacol Ther 87:199–226
Shi J, Mori E, Mori Y, Mori M, Li J, Ito Y, Inoue R (2004) Multiple regulation by calcium of murine homologues of transient receptor potential proteins TRPC6 and TRPC7 expressed in HEK293 cells. J Physiol 561:415–432
Shimoda LA, Welsh LE, Pearse DB (2002) Inhibition of inwardly-rectifying K channels by cGMP in pulmonary vascular endothelial cells. Am J Physiol Lung Cell Mol Physiol 283:L297–L304
Strubing C, Krapivinsky G, Krapivinsky L, Clapham DE (2001) TRPC1 and TRPC5 form a novel cation channel in mammalian brain. Neuron 29:645–655
Tertyshnikova S, Yan XW, Fein A (1998) cGMP inhibits IP3-induced Ca2+ release in intact rat megakaryocytes via cGMP-and cAMP-dependent protein kinase. J Physiol 512:89–96
Tiruppathi C, Freichel M, Vogel SM, Paria BC, Mehta D, Flockerzi V, Malik AB (2002) Impairment of store-operated Ca2+ entry in TRPC4(-/-) mice interferes with increase in lung microvascular permeability. Circ Res 91:70–76
Trebak M, Hempel N, Wedel BJ, Smyth JT, Bird GSJ, Putney Jr JW (2005) Negative regulation of TRPC3 channels by protein kinase C-mediated phosphorylation of serine 712. Mol Pharmacol 67:558–563
Trepakova ES, Cohen RA, Bolotina VM (1999) Nitric oxide inhibits capacitative cation influx in human platelets by promoting sarcoplasmic/endoplasmic reticulum Ca2+-ATPase-dependent refilling of Ca2+ stores. Circ Res 84:201–209
Vazquez G, Wedel BJ, Trebak M, Bird GS, Putney JW Jr (2003) Expression level of the canonical transient receptor potential 3 (TRPC3) channel determines its mechanism of activation. J Biol Chem 278:21649–21654
Vazquez G, Wedel BJ, Kawasaki BT, Bird GS, Putney JW Jr (2004) Obligatory role of Src kinase in the signaling mechanism for TRPC3 cation channels. J Biol Chem 279:40521–40528
Venkatachalam K, Zheng F, Gill DL (2003) Regulation of canonical transient receptor potential (TRPC) channel function by diacylglycerol and protein kinase C. J Biol Chem 278:29031–29040
Viso-Leon MC, Ripoll C, Nadal A (2004) Oestradiol rapidly inhibits Ca2+ signals in ciliary neurons through classical oestrogen receptors in cytoplasm. Pflugers Arch 449:33–41
Wang X, Robinson PJ (1997) Cyclic GMP-dependent protein kinase and cellular signaling in the nervous system. J Neurochem 68:443–456
Yao X, Huang Y (2003) From nitric oxide to endothelial cytosolic Ca2+: a negative feedback control. Trends Pharmacol Sci 24:263–266
Yao X, Kwan HY, Chan FL, Chan NW, Huang Y (2000) A protein kinase G-sensitive channel mediates flow-induced Ca2+ entry into vascular endothelial cells. FASEB J 14:932–938
Yoshioka A, Yamaya Y, Saiki S, Kanemoto M, Hirose G, Pleasure D (2000) Cyclic GMP/cyclic GMP-dependent protein kinase system prevents excitotoxicity in an immortalized oligo-dendroglial cell line. J Neurochem 74:633–640
Yuan SY (2003) Protein kinase signaling in the modulation for microvascular permeability. Vascul Pharmacol 39:213–223
Zavoico GB, Halenda SP, Sha’afi RI, Feinstein MB (1985) Phorbol myristate acetate inhibits thrombin-stimulated Ca2+ mobilization and phosphatidylinositol 4,5-bisphosphate hydrolysis in human platelets. Proc Natl Acad Sci USA 82:3859–3862
Zhang L, Saffen D (2001) Muscarinic acetylcholine receptor regulation of TRP6Ca2+ channel isoforms. Molecular structures and functional characterization. J Biol Chem 276:13331–13339
Zweifach A, Lewis R (1995) Rapid inactivation of depletion-activated calcium current (ICRAC) due to local calcium feedback. J Gen Physiol 105:209–226
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Yao, X. (2007). TRPC, cGMP-Dependent Protein Kinases and Cytosolic Ca2+ . In: Flockerzi, V., Nilius, B. (eds) Transient Receptor Potential (TRP) Channels. Handbook of Experimental Pharmacology, vol 179. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-34891-7_31
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DOI: https://doi.org/10.1007/978-3-540-34891-7_31
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