Physiological function and characterization of TRPCs in neurons

Cells

Volumn 3, Issue 2, 2014, Pages 455-475

  Sun, Yuyang ^a   Sukumaran, Pramod ^a   Bandyopadhyay, Bidhan C ^b   Singh, Brij B ^a  

^a UNIVERSITY OF NORTH DAKOTA SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Neurodegenerative diseases; Neuronal function; TRPC channels

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CALCIUM BINDING PROTEIN; CALCIUM RELEASE ACTIVATED CALCIUM CHANNEL; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; G PROTEIN COUPLED RECEPTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; INOSITOL 1, 4, 5 TRISPHOSPHATE RECEPTOR; METABOTROPIC RECEPTOR; NEURITE PROMOTING FACTOR; PROTEIN KINASE C; PROTEIN TYROSINE KINASE; REACTIVE OXYGEN METABOLITE; RECEPTOR FOR ACTIVATED C KINASE 1; SCAFFOLD PROTEIN; TRANSIENT RECEPTOR POTENTIAL CHANNEL; TRANSIENT RECEPTOR POTENTIAL CHANNEL 1; TRANSIENT RECEPTOR POTENTIAL CHANNEL 2; TRANSIENT RECEPTOR POTENTIAL CHANNEL 3; TRANSIENT RECEPTOR POTENTIAL CHANNEL 4; TRANSIENT RECEPTOR POTENTIAL CHANNEL 5; TRANSIENT RECEPTOR POTENTIAL CHANNEL 6; TRANSIENT RECEPTOR POTENTIAL CHANNEL 7; UNCLASSIFIED DRUG;

BRAIN ISCHEMIA; CALCIUM CURRENT; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL MEMBRANE DEPOLARIZATION; DEGENERATIVE DISEASE; GAIN OF FUNCTION MUTATION; HUMAN; LONG TERM POTENTIATION; MITOCHONDRIAL MEMBRANE POTENTIAL; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NERVE DEGENERATION; NERVE INJURY; NEUROSECRETION; NONHUMAN; PROTEIN EXPRESSION; REVIEW;

EID: 84924910859     PISSN: None     EISSN: 20734409     Source Type: Journal    
DOI: 10.3390/cells3020455     Document Type: Review

References (140)

1. Clapham, D.E. Calcium signaling. Cell 2007, 131, 1047-1058.
2. Selvaraj, S.; Sun, Y.; Singh, B.B. TRPC channels and their implication in neurological diseases. CNS Neurol. Disord. Drug Targets 2010, 9, 94-104.
3. Yamamoto, S.; Wajima, T.; Hara, Y.; Nishida, M.; Mori, Y. Transient receptor potential channels in Alzheimer's disease. Biochim. Biophys. Acta 2007, 1772, 958-967.
4. Reboreda, A.; Jimenez-Diaz, L.; Navarro-Lopez, J.D. TRP channels and neural persistent activity. Adv. Exp. Med. Biol. 2011, 704, 595-613.
5. Berridge, M.J.; Lipp, P.; Bootman, M.D. The versatility and universality of calcium signalling. Nat. Rev. Mol. Cell Biol. 2000, 1, 11-21.
6. Putney, J.W. The physiological function of store-operated calcium entry. Neurochem. Res. 2011, 36, 1157-1165.
7. Smyth, J.T.; Hwang, S.Y.; Tomita, T.; DeHaven, W.I.; Mercer, J.C.; Putney, J.W. Activation and regulation of store-operated calcium entry. J. Cell. Mol. Med. 2010, 14, 2337-2349.
8. Liu, X.; Cheng, K.T.; Bandyopadhyay, B.C.; Pani, B.; Dietrich, A.; Paria, B.C.; Swaim, W.D.; Beech, D.; Yildrim, E.; Singh, B.B.; et al. Attenuation of store-operated Ca2+ current impairs salivary gland fluid secretion in TRPC1(-/-) mice. Proc. Natl. Acad. Sci. USA 2007, 104, 17542-17547.
9. Liao, Y.; Plummer, N.W.; George, M.D.; Abramowitz, J.; Zhu, M.X.; Birnbaumer, L. A role for Orai in TRPC-mediated Ca2+ entry suggests that a TRPC:Orai complex may mediate store and receptor operated Ca2+ entry. Proc. Natl. Acad. Sci. USA 2009, 106, 3202-3206.
10. Pan, Z.; Yang, H.; Reinach, P.S. Transient receptor potential (TRP) gene superfamily encoding cation channels. Hum. Genomics 2011, 5, 108-116.
11. Putney, J.W. Physiological mechanisms of TRPC activation. Pflugers Archiv 2005, 451, 29-34.
12. Hao, B.; Lu, Y.; Wang, Q.; Guo, W.; Cheung, K.H.; Yue, J. Role of STIM1 in survival and neural differentiation of mouse embryonic stem cells independent of Orai1-mediated Ca entry. Stem Cell Res. 2013, 12, 452-466.
13. Pani, B.; Ong, H.L.; Liu, X.; Rauser, K.; Ambudkar, I.S.; Singh, B.B. Lipid rafts determine clustering of STIM1 in endoplasmic reticulum-plasma membrane junctions and regulation of store-operated Ca2+ entry (SOCE). J. Biol. Chem. 2008, 283, 17333-17340.
14. Pani, B.; Bollimuntha, S.; Singh, B.B. The TR (i)P to Ca(2)(+) signaling just got STIMy: An update on STIM1 activated TRPC channels. Front. Biosci. 2012, 17, 805-823.
15. Park, C.Y.; Shcheglovitov, A.; Dolmetsch, R. The CRAC channel activator STIM1 binds and inhibits L-type voltage-gated calcium channels. Science 2010, 330, 101-105.
16. Wang, Y.; Deng, X.; Mancarella, S.; Hendron, E.; Eguchi, S.; Soboloff, J.; Tang, X.D.; Gill, D.L. The calcium store sensor, STIM1, reciprocally controls Orai and CaV1.2 channels. Science 2010, 330, 105-109.
17. Liu, X.; Ong, H.L.; Pani, B.; Johnson, K.; Swaim, W.B.; Singh, B.; Ambudkar, I. Effect of cell swelling on ER/PM junctional interactions and channel assembly involved in SOCE. Cell Calcium 2010, 47, 491-499.
18. Ong, H.L.; Cheng, K.T.; Liu, X.; Bandyopadhyay, B.C.; Paria, B.C.; Soboloff, J.; Pani, B.; Gwack, Y.; Srikanth, S.; Singh, B.B.; et al. Dynamic assembly of TRPC1-STIM1-Orai1 ternary complex is involved in store-operated calcium influx. Evidence for similarities in store-operated and calcium release-activated calcium channel components. J. Biol. Chem. 2007, 282, 9105-9116.
19. Minke, B.; Cook, B. TRP channel proteins and signal transduction. Physiol. Rev. 2002, 82, 429-472.
20. Kiselyov, K.; van Rossum, D.B.; Patterson, R.L. TRPC channels in pheromone sensing. Vitam. Horm. 2010, 83, 197-213.
21. 2+ influx. J. Biol. Chem. 2005, 280, 12908-12916.
22. Liu, X.; Bandyopadhyay, B.C.; Singh, B.B.; Groschner, K.; Ambudkar, I.S. Molecular analysis of a store-operated and 2-acetyl-sn-glycerol-sensitive non-selective cation channel. Heteromeric assembly of TRPC1-TRPC3. J. Biol. Chem. 2005, 280, 21600-21606.
23. Andrade-Talavera, Y.; Duque-Feria, P.; Sihra, T.S.; Rodriguez-Moreno, A. Pre-synaptic kainate receptor-mediated facilitation of glutamate release involves PKA and Ca(2+)-calmodulin at thalamocortical synapses. J. Neurochem. 2013, 126, 565-578.
24. Wong, A.C.; Birnbaumer, L.; Housley, G.D. Canonical transient receptor potential channel subtype 3-mediated hair cell Ca(2+) entry regulates sound transduction and auditory neurotransmission. Eur. J. Neurosci. 2013, 37, 1478-1486.
25. Kerstein, P.C.; Jacques-Fricke, B.T.; Rengifo, J.; Mogen, B.J.; Williams, J.C.; Gottlieb, P.A.; Sachs, F.; Gomez, T.M. Mechanosensitive TRPC1 channels promote calpain proteolysis of talin to regulate spinal axon outgrowth. J. Neurosci. 2013, 33, 273-285.
26. Lohmann, C.; Bonhoeffer, T. A role for local calcium signaling in rapid synaptic partner selection by dendritic filopodia. Neuron 2008, 59, 253-260.
27. Zitt, C.; Zobel, A.; Obukhov, A.G.; Harteneck, C.; Kalkbrenner, F.; Luckhoff, A.; Schultz, G. Cloning and functional expression of a human Ca2+-permeable cation channel activated by calcium store depletion. Neuron 1996, 16, 1189-1196.
28. Wes, P.D.; Chevesich, J.; Jeromin, A.; Rosenberg, C.; Stetten, G.; Montell, C. TRPC1, a human homolog of a Drosophila store-operated channel. Proc. Natl. Acad. Sci. USA 1995, 92, 9652-9656.
29. Liu, X.; Wang, W.; Singh, B.B.; Lockwich, T.; Jadlowiec, J.; O'Connell, B.; Wellner, R.; Zhu, M.X.; Ambudkar, I.S. Trp1, a candidate protein for the store-operated Ca(2+) influx mechanism in salivary gland cells. J. Biol. Chem. 2000, 275, 3403-3411.
30. Strubing, C.; Krapivinsky, G.; Krapivinsky, L.; Clapham, D.E. TRPC1 and TRPC5 form a novel cation channel in mammalian brain. Neuron 2001, 29, 645-655.
31. Lucas, P.; Ukhanov, K.; Leinders-Zufall, T.; Zufall, F. A diacylglycerol-gated cation channel in vomeronasal neuron dendrites is impaired in TRPC2 mutant mice: Mechanism of pheromone transduction. Neuron 2003, 40, 551-561.
32. Liman, E.R.; Corey, D.P.; Dulac, C. TRP2: A candidate transduction channel for mammalian pheromone sensory signaling. Proc. Natl. Acad. Sci. USA 1999, 96, 5791-5796.
33. Hofmann, T.; Obukhov, A.G.; Schaefer, M.; Harteneck, C.; Gudermann, T.; Schultz, G. Direct activation of human TRPC6 and TRPC3 channels by diacylglycerol. Nature 1999, 397, 259-263.
34. Clapham, D.E.; Julius, D.; Montell, C.; Schultz, G. International Union of Pharmacology. XLIX. Nomenclature and structure-function relationships of transient receptor potential channels. Pharmacol. Rev. 2005, 57, 427-450.
35. Lemonnier, L.; Trebak, M.; Putney, J.W., Jr. Complex regulation of the TRPC3, 6 and 7 channel subfamily by diacylglycerol and phosphatidylinositol-4,5-bisphosphate. Cell Calcium 2008, 43, 506-514.
36. Li, Y.; Jia, Y.C.; Cui, K.; Li, N.; Zheng, Z.Y.; Wang, Y.Z.; Yuan, X.B. Essential role of TRPC channels in the guidance of nerve growth cones by brain-derived neurotrophic factor. Nature 2005, 434, 894-898.
37. Philipp, S.; Cavalie, A.; Freichel, M.; Wissenbach, U.; Zimmer, S.; Trost, C.; Marquart, A.; Murakami, M.; Flockerzi, V. A mammalian capacitative calcium entry channel homologous to Drosophila TRP and TRPL. EMBO J. 1996, 15, 6166-6171.
38. Schaefer, M.; Plant, T.D.; Obukhov, A.G.; Hofmann, T.; Gudermann, T.; Schultz, G. Receptor-mediated regulation of the nonselective cation channels TRPC4 and TRPC5. J. Biol. Chem. 2000, 275, 17517-17526.
39. 2+. J. Physiol. 1999, 518, 631-638.
40. Philipp, S.; Hambrecht, J.; Braslavski, L.; Schroth, G.; Freichel, M.; Murakami, M.; Cavalie, A.; Flockerzi, V. A novel capacitative calcium entry channel expressed in excitable cells. EMBO J. 1998, 17, 4274-4282.
41. 2+ channel from mouse brain. J. Biol. Chem. 1998, 273, 10279-10287.
42. Yamada, H.; Wakamori, M.; Hara, Y.; Takahashi, Y.; Konishi, K.; Imoto, K.; Mori, Y. Spontaneous single-channel activity of neuronal TRP5 channel recombinantly expressed in HEK293 cells. Neurosci. Lett. 2000, 285, 111-114.
43. Strubing, C.; Krapivinsky, G.; Krapivinsky, L.; Clapham, D.E. Formation of novel TRPC channels by complex subunit interactions in embryonic brain. J. Biol. Chem. 2003, 278, 39014-39019.
44. Shi, J.; Mori, E.; Mori, Y.; Mori, M.; Li, J.; Ito, Y.; Inoue, R. Multiple regulation by calcium of murine homologues of transient receptor potential proteins TRPC6 and TRPC7 expressed in HEK293 cells. J. Physiol. 2004, 561, 415-432.
45. Huang, W.C.; Young, J.S.; Glitsch, M.D. Changes in TRPC channel expression during postnatal development of cerebellar neurons. Cell Calcium 2007, 42, 1-10.
46. Riccio, A.; Medhurst, A.D.; Mattei, C.; Kelsell, R.E.; Calver, A.R.; Randall, A.D.; Benham, C.D.; Pangalos, M.N. mRNA distribution analysis of human TRPC family in CNS and peripheral tissues. Brain Res. Mol. Brain Res. 2002, 109, 95-104.
47. Okada, T.; Inoue, R.; Yamazaki, K.; Maeda, A.; Kurosaki, T.; Yamakuni, T.; Tanaka, I.; Shimizu, S.; Ikenaka, K.; Imoto, K.; et al. Molecular and functional characterization of a novel mouse transient receptor potential protein homologue TRP7. Ca(2+)-permeable cation channel that is constitutively activated and enhanced by stimulation of G protein-coupled receptor. J. Biol. Chem. 1999, 274, 27359-27370.
48. 2+ influx. J. Biol. Chem. 2002, 277, 12302-12309.
49. 2+ homeostasis and late onset degeneration. Mol. Neurodegener 2013, 8, doi:10.1186/1750-1326-8-23.
50. Bollimuntha, S.; Selvaraj, S.; Singh, B.B. Emerging roles of canonical TRP channels in neuronal function. Adv. Exp. Med. Biol. 2011, 704, 573-593.
51. Wu, X.; Zagranichnaya, T.K.; Gurda, G.T.; Eves, E.M.; Villereal, M.L. A TRPC1/TRPC3-mediated increase in store-operated calcium entry is required for differentiation of H19-7 hippocampal neuronal cells. J. Biol. Chem. 2004, 279, 43392-43402.
52. Boudes, M.; Uvin, P.; Pinto, S.; Freichel, M.; Birnbaumer, L.; Voets, T.; de Ridder, D.; Vennekens, R. Crucial role of TRPC1 and TRPC4 in cystitis-induced neuronal sprouting and bladder overactivity. PLoS One 2013, 8, e69550.
53. Alessandri-Haber, N.; Dina, O.A.; Chen, X.; Levine, J.D. TRPC1 and TRPC6 channels cooperate with TRPV4 to mediate mechanical hyperalgesia and nociceptor sensitization. J. Neurosci. 2009, 29, 6217-6228.
54. Phelan, K.D.; Shwe, U.T.; Abramowitz, J.; Wu, H.; Rhee, S.W.; Howell, M.D.; Gottschall, P.E.; Freichel, M.; Flockerzi, V.; Birnbaumer, L.; et al. Canonical transient receptor channel 5 (TRPC5) and TRPC1/4 contribute to seizure and excitotoxicity by distinct cellular mechanisms. Mol. Pharmacol. 2013, 83, 429-438.
55. Ariano, P.; Dalmazzo, S.; Owsianik, G.; Nilius, B.; Lovisolo, D. TRPC channels are involved in calcium-dependent migration and proliferation in immortalized GnRH neurons. Cell Calcium 2011, 49, 387-394.
56. 2+ entry and embryonic rat neural stem cell proliferation. J. Neurosci. 2005, 25, 2687-2701.
57. Kim, S.J.; Kim, Y.S.; Yuan, J.P.; Petralia, R.S.; Worley, P.F.; Linden, D.J. Activation of the TRPC1 cation channel by metabotropic glutamate receptor mGluR1. Nature 2003, 426, 285-291.
58. 2+-activated cation channel from hamster vomeronasal sensory neurons. J. Physiol. 2003, 548, 777-787.
59. Zhang, J.; Webb, D.M. Evolutionary deterioration of the vomeronasal pheromone transduction pathway in catarrhine primates. Proc. Natl. Acad. Sci. USA 2003, 100, 8337-8341.
60. Abramowitz, J.; Birnbaumer, L. Physiology and pathophysiology of canonical transient receptor potential channels. FASEB J. 2009, 23, 297-328.
61. Yildirim, E.; Birnbaumer, L. TRPC2: Molecular biology and functional importance. Handb. Exp. Pharmacol. 2007, 179, 53-75.
62. Leypold, B.G.; Yu, C.R.; Leinders-Zufall, T.; Kim, M.M.; Zufall, F.; Axel, R. Altered sexual and social behaviors in trp2 mutant mice. Proc. Natl. Acad. Sci. USA 2002, 99, 6376-6381.
63. Stowers, L.; Holy, T.E.; Meister, M.; Dulac, C.; Koentges, G. Loss of sex discrimination and male-male aggression in mice deficient for TRP2. Science 2002, 295, 1493-1500.
64. Kimchi, T.; Xu, J.; Dulac, C. A functional circuit underlying male sexual behaviour in the female mouse brain. Nature 2007, 448, 1009-1014.
65. Wu, M.V.; Manoli, D.S.; Fraser, E.J.; Coats, J.K.; Tollkuhn, J.; Honda, S.-I.; Harada, N.; Shah, N.M. Estrogen masculinizes neural pathways and sex-specific behaviors. Cell 2009, 139, 61-72.
66. 2+ into mouse sperm triggered by egg ZP3. Nat. Cell Biol. 2001, 3, 499-502.
67. Sutton, K.A.; Jungnickel, M.K.; Wang, Y.; Cullen, K.; Lambert, S.; Florman, H.M. Enkurin is a novel calmodulin and TRPC channel binding protein in sperm. Dev. Biol. 2004, 274, 426-435.
68. Li, H.S.; Xu, X.Z.; Montell, C. Activation of a TRPC3-dependent cation current through the neurotrophin BDNF. Neuron 1999, 24, 261-273.
69. Amaral, M.D.; Pozzo-Miller, L. TRPC3 channels are necessary for brain-derived neurotrophic factor to activate a nonselective cationic current and to induce dendritic spine formation. J. Neurosci. 2007, 27, 5179-5189.
70. Amaral, M.D.; Pozzo-Miller, L. BDNF induces calcium elevations associated with ibdnf, a nonselective cationic current mediated by TRPC channels. J. Neurophysiol. 2007, 98, 2476-2482.
71. Freichel, M.; Vennekens, R.; Olausson, J.; Stolz, S.; Philipp, S.E.; Weissgerber, P.; Flockerzi, V. Functional role of TRPC proteins in native systems: Implications from knockout and knock-down studies. J. Physiol. 2005, 567, 59-66.
72. Congar, P.; Leinekugel, X.; Ben-Ari, Y.; Crépel, V. A long-lasting calcium-activated nonselective cationic current is generated by synaptic stimulation or exogenous activation of group I metabotropic glutamate receptors in CA1 pyramidal neurons. J. Neurosci. 1997, 17, 5366-5379.
73. Linden, R. The survival of developing neurons: A review of afferent control. Neuroscience 1994, 58, 671-682.
74. Ruat, M.; Traiffort, E. Roles of the calcium sensing receptor in the central nervous system. Best Pract. Res. Clin. Endocrinol. Metab. 2013, 27, 429-442.
75. Harteneck, C.; Gollasch, M. Pharmacological modulation of diacylglycerol-sensitive TRPC3/6/7 channels. Curr. Pharm. Biotechnol. 2011, 12, 35-41.
76. Hartmann, J.; Dragicevic, E.; Adelsberger, H.; Henning, H.A.; Sumser, M.; Abramowitz, J.; Blum, R.; Dietrich, A.; Freichel, M.; Flockerzi, V.; et al. TRPC3 channels are required for synaptic transmission and motor coordination. Neuron 2008, 59, 392-398.
77. Su, B.; Ji, Y.-S.; Sun, X.-L.; Liu, X.-H.; Chen, Z.-Y. Brain-derived neurotrophic factor (BDNF)-induced mitochondrial motility arrest and presynaptic docking contribute to BDNFenhanced synaptic transmission. J. Biol. Chem. 2014, 289, 1213-1226.
78. Rodríguez-Santiago, M.; Mendoza-Torres, M.; Jiménez-Bremont, J.F.; López-Revilla, R. Knockout of the trcp3 gene causes a recessive neuromotor disease in mice. Biochem. Biophys. Res. Commun. 2007, 360, 874-879.
79. 2+ influx. Mol. Cell 2004, 15, 635-646.
80. 2+ release by mediating the interaction between inositol 1,4,5-trisphosphate receptor and RACK1. J. Biol. Chem. 2008, 283, 32821-32830.
81. Streifel, K.M.; Miller, J.; Mouneimne, R.; Tjalkens, R.B. Manganese inhibits ATP-induced calcium entry through the transient receptor potential channel TRPC3 in astrocytes. Neurotoxicology 2013, 34, 160-166.
82. Obukhov, A.G.; Nowycky, M.C. TRPC4 can be activated by G-protein-coupled receptors and provides sufficient Ca(2+) to trigger exocytosis in neuroendocrine cells. J. Biol. Chem. 2002, 277, 16172-16178.
83. Lee, K.P.; Jun, J.Y.; Chang, I.-Y.; Suh, S.-H.; So, I.; Kim, K.W. TRPC4 is an essential component of the nonselective cation channel activated by muscarinic stimulation in mouse visceral smooth muscle cells. Mol. Cells 2005, 20, 435-441.
84. Zhang, S.; Remillard, C.V.; Fantozzi, I.; Yuan, J.X.J. ATP-induced mitogenesis is mediated by cyclic AMP response element-binding protein-enhanced TRPC4 expression and activity in human pulmonary artery smooth muscle cells. Am. J. Physiol. Cell Physiol. 2004, 287, C1192-C1201.
85. Gao, Y.-Q.; Gao, H.; Zhou, Z.-Y.; Lu, S.-D.; Sun, F.-Y. Expression of transient receptor potential channel 4 in striatum and hippocampus of rats is increased after focal cerebral ischemia. Sheng Li Xue Bao 2004, 56, 153-157.
86. Greka, A.; Navarro, B.; Oancea, E.; Duggan, A.; Clapham, D.E. TRPC5 is a regulator of hippocampal neurite length and growth cone morphology. Nat. Neurosci. 2003, 6, 837-845.
87. Hui, H.; McHugh, D.; Hannan, M.; Zeng, F.; Xu, S.-Z.; Khan, S.-U.-H.; Levenson, R.; Beech, D.J.; Weiss, J.L. Calcium-sensing mechanism in TRPC5 channels contributing to retardation of neurite outgrowth. J. Physiol. 2006, 572, 165-172.
88. 2+/calmodulin kinase Igamma to promote axon formation in hippocampal neurons. J. Neurosci. 2009, 29, 9794-9808.
89. Wu, G.; Lu, Z.-H.; Obukhov, A.G.; Nowycky, M.C.; Ledeen, R.W. Induction of calcium influx through TRPC5 channels by cross-linking of GM1 ganglioside associated with alpha5beta1 integrin initiates neurite outgrowth. J. Neurosci. 2007, 27, 7447-7458.
90. Riccio, A.; Li, Y.; Moon, J.; Kim, K.-S.; Smith, K.S.; Rudolph, U.; Gapon, S.; Yao, G.L.; Tsvetkov, E.; Rodig, S.J.; et al. Essential role for TRPC5 in amygdala function and fear-related behavior. Cell 2009, 137, 761-772.
91. Yan, H.-D.; Villalobos, C.; Andrade, R. TRPC channels mediate a muscarinic receptor-induced afterdepolarization in cerebral cortex. J. Neurosci. 2009, 29, 10038-10046.
92. Calupca, M.A.; Locknar, S.A.; Parsons, R.L. TRPC6 immunoreactivity is colocalized with neuronal nitric oxide synthase in extrinsic fibers innervating guinea pig intrinsic cardiac ganglia. J. Comp. Neurol. 2002, 450, 283-291.
93. Warren, E.J.; Allen, C.N.; Brown, R.L.; Robinson, D.W. The light-activated signaling pathway in SCN-projecting rat retinal ganglion cells. Eur. J. Neurosci. 2006, 23, 2477-2487.
94. Elsaesser, R.; Montani, G.; Tirindelli, R.; Paysan, J. Phosphatidyl-inositide signalling proteins in a novel class of sensory cells in the mammalian olfactory epithelium. Eur. J. Neurosci. 2005, 21, 2692-2700.
95. Chung, Y.H.; Sun Ahn, H.; Kim, D.; Hoon Shin, D.; Su Kim, S.; Yong Kim, K.; Bok Lee, W.; Ik Cha, C. Immunohistochemical study on the distribution of TRPC channels in the rat hippocampus. Brain Res. 2006, 1085, 132-137.
96. Giampà, C.; DeMarch, Z.; Patassini, S.; Bernardi, G.; Fusco, F.R. Immunohistochemical localization of TRPC6 in the rat substantia nigra. Neurosci. Lett. 2007, 424, 170-174.
97. Tai, Y.; Feng, S.; Ge, R.; Du, W.; Zhang, X.; He, Z.; Wang, Y. TRPC6 channels promote dendritic growth via the CaMKIV-CREB pathway. J. Cell. Sci. 2008, 121, 2301-2307.
98. Zhou, J.; Du, W.; Zhou, K.; Tai, Y.; Yao, H.; Jia, Y.; Ding, Y.; Wang, Y. Critical role of TRPC6 channels in the formation of excitatory synapses. Nat. Neurosci. 2008, 11, 741-743.
99. Min, M.-Y.; Shih, P.-Y.; Wu, Y.-W.; Lu, H.-W.; Lee, M.-L.; Yang, H.-W. Neurokinin 1 receptor activates transient receptor potential-like currents in noradrenergic A7 neurons in rats. Mol. Cell. Neurosci. 2009, 42, 56-65.
100. Babich, L.G.; Ku, C.-Y.; Young, H.W.J.; Huang, H.; Blackburn, M.R.; Sanborn, B.M. Expression of capacitative calcium TrpC proteins in rat myometrium during pregnancy. Biol. Reprod. 2004, 70, 919-924.
101. Elg, S.; Marmigere, F.; Mattsson, J.P.; Ernfors, P. Cellular subtype distribution and developmental regulation of TRPC channel members in the mouse dorsal root ganglion. J. Comp. Neurol. 2007, 503, 35-46.
102. 2+ channel mediating angiotensin II-induced myocardial apoptosis. Mol. Cell. Biochem. 2007, 294, 205-215.
103. Föller, M.; Kasinathan, R.S.; Duranton, C.; Wieder, T.; Huber, S.M.; Lang, F. PGE2-induced apoptotic cell death in K562 human leukaemia cells. Cell. Physiol. Biochem. 2006, 17, 201-210.
104. Xue, T.; Do, M.T.; Riccio, A.; Jiang, Z.; Hsieh, J.; Wang, H.C.; Merbs, S.L.; Welsbie, D.S.; Yoshioka, T.; Weissgerber, P.; et al. Melanopsin signalling in mammalian iris and retina. Nature 2011, 479, 67-73.
105. Putney, J.W., Jr. Capacitative calcium entry in the nervous system. Cell Calcium 2003, 34, 339-344.
106. 2+ dependence and time course of somatodendritic dopamine release: Substantia nigra vs. striatum. J. Neurosci. 2001, 21, 7841-7847.
107. Patel, J.C.; Witkovsky, P.; Avshalumov, M.V.; Rice, M.E. Mobilization of calcium from intracellular stores facilitates somatodendritic dopamine release. J. Neurosci. 2009, 29, 6568-6579.
108. Small, D.H. Dysregulation of calcium homeostasis in Alzheimer's disease. Neurochem. Res. 2009, 34, 1824-1829.
109. Yu, J.T.; Chang, R.C.; Tan, L. Calcium dysregulation in Alzheimer's disease: From mechanisms to therapeutic opportunities. Progr. Neurobiol. 2009, 89, 240-255.
110. Giacomello, M.; Oliveros, J.C.; Naranjo, J.R.; Carafoli, E. Neuronal Ca(2+) dyshomeostasis in Huntington disease. Prion 2013, 7, 76-84.
111. Suzuki, M.; Nagai, Y.; Wada, K.; Koike, T. Calcium leak through ryanodine receptor is involved in neuronal death induced by mutant huntingtin. Biochem. Biophys. Res. Commun. 2012, 429, 18-23.
112. Bezprozvanny, I.; Mattson, M.P. Neuronal calcium mishandling and the pathogenesis of Alzheimer's disease. Trends Neurosci. 2008, 31, 454-463.
113. Selvaraj, S.; Sun, Y.; Watt, J.A.; Wang, S.; Lei, S.; Birnbaumer, L.; Singh, B.B. Neurotoxin-induced ER stress in mouse dopaminergic neurons involves downregulation of TRPC1 and inhibition of AKT/mTOR signaling. J. Clin. Investig. 2012, 122, 1354-1367.
114. Henke, N.; Albrecht, P.; Pfeiffer, A.; Toutzaris, D.; Zanger, K.; Methner, A. Stromal interaction molecule 1 (STIM1) is involved in the regulation of mitochondrial shape and bioenergetics and plays a role in oxidative stress. J. Biol. Chem. 2012, 287, 42042-42052.
115. Feng, S.; Li, H.; Tai, Y.; Huang, J.; Su, Y.; Abramowitz, J.; Zhu, M.X.; Birnbaumer, L.; Wang, Y. Canonical transient receptor potential 3 channels regulate mitochondrial calcium uptake. Proc. Natl. Acad. Sci. USA 2013, 110, 11011-11016.
116. 2+ influx. J. Gastrointest. Surg. 2012, 16, 1397-1405.
117. Song, M.Y.; Makino, A.; Yuan, J.X. Role of reactive oxygen species and redox in regulating the function of transient receptor potential channels. Antioxidants Redox Signal. 2011, 15, 1549-1565.
118. Miller, B.A.; Zhang, W. TRP channels as mediators of oxidative stress. Adv. Exp. Med. Biol. 2011, 704, 531-544.
119. Chen, T.; Yang, Y.F.; Luo, P.; Liu, W.; Dai, S.H.; Zheng, X.R.; Fei, Z.; Jiang, X.F. Homer1 knockdown protects dopamine neurons through regulating calcium homeostasis in an in vitro model of Parkinson's disease. Cell. Signalling 2013, 25, 2863-2870.
120. Przedborski, S.; Tieu, K.; Perier, C.; Vila, M. MPTP as a mitochondrial neurotoxic model of Parkinson's disease. J. Bioenerget. Biomembr. 2004, 36, 375-379.
121. Mattson, M.P. Calcium and neurodegeneration. Aging Cell 2007, 6, 337-350.
122. Zeng, X.; Pan, Z.G.; Shao, Y.; Wu, X.N.; Liu, S.X.; Li, N.L.; Wang, W.M. SKF-96365 attenuates toxin-induced neuronal injury through opposite regulatory effects on Homer1a and Homer1b/c in cultured rat mesencephalic cells. Neurosci. Lett. 2013, 543, 183-188.
123. Bollimuntha, S.; Singh, B.B.; Shavali, S.; Sharma, S.K.; Ebadi, M. TRPC1-mediated inhibition of 1-methyl-4-phenylpyridinium ion neurotoxicity in human SH-SY5Y neuroblastoma cells. J. Biol. Chem. 2005, 280, 2132-2140.
124. Selvaraj, S.; Watt, J.A.; Singh, B.B. TRPC1 inhibits apoptotic cell degeneration induced by dopaminergic neurotoxin MPTP/MPP(+). Cell Calcium 2009, 46, 209-218.
125. Ermak, G.; Davies, K.J. Calcium and oxidative stress: From cell signaling to cell death. Mol. Immunol. 2002, 38, 713-721.
126. Wu, J.; Shih, H.P.; Vigont, V.; Hrdlicka, L.; Diggins, L.; Singh, C.; Mahoney, M.; Chesworth, R.; Shapiro, G.; Zimina, O.; et al. Neuronal store-operated calcium entry pathway as a novel therapeutic target for Huntington's disease treatment. Chem. Biol. 2011, 18, 777-793.
127. Briones, N.; Dinu, V. Data mining of high density genomic variant data for prediction of Alzheimer's disease risk. BMC Med. Genet. 2012, 13, 7, doi:10.1186/1471-2350-13-7.
128. 2+ leak channels, a function disrupted by familial Alzheimer's disease-linked mutations. Cell 2006, 126, 981-993.
129. 2+ disruptions in young, adult, and aged Alzheimer's disease mice. J. Neurosci. 2006, 26, 5180-5189.
130. LaFerla, F.M. Calcium dyshomeostasis and intracellular signalling in Alzheimer's disease. Nat. Rev. 2002, 3, 862-872.
131. 2+ entry into HEK293 cells. Cell. Signalling. 2005, 17, 437-445.
132. 2+ entry is associated with the familial Alzheimer's disease presenilin-2 T122R mutation and anticipates the onset of dementia. Neurobiol. Dis. 2005, 18, 638-648.
133. 2+ disruption in Alzheimer's disease by presenilin regulation of InsP3 receptor channel gating. Neuron 2008, 58, 871-883.
134. Bandara, S.; Malmersjo, S.; Meyer, T. Regulators of calcium homeostasis identified by inference of kinetic model parameters from live single cells perturbed by siRNA. Sci. Signal. 2013, 6, ra56.
135. Stranahan, A.M.; Mattson, M.P. Recruiting adaptive cellular stress responses for successful brain ageing. Nat. Rev. Neurosci. 2012, 13, 209-216.
136. McGurk, J.S.; Shim, S.; Kim, J.Y.; Wen, Z.; Song, H.; Ming, G.L. Postsynaptic TRPC1 function contributes to BDNF-induced synaptic potentiation at the developing neuromuscular junction. J. Neurosci. 2011, 31, 14754-14762.
137. Wang, H.J.; Cao, J.P.; Yu, J.K.; Zhang, L.C.; Jiang, Z.J.; Gao, D.S. Calbindin-D28K expression induced by glial cell line-derived neurotrophic factor in substantia nigra neurons dependent on PI3K/Akt/NF-kappaB signaling pathway. Eur. J. Pharmacol. 2008, 595, 7-12.
138. Mattson, M.P. Parkinson's disease: Don't mess with calcium. J. Clin. Investig. 2012, 122, 1195-1198.
139. Sun, S.; Zhang, H.; Liu, J.; Popugaeva, E.; Xu, N.J.; Feske, S.; White, C.L., 3rd; Bezprozvanny, I. Reduced synaptic STIM2 expression and impaired store-operated calcium entry cause destabilization of mature spines in mutant presenilin mice. Neuron 2014, 82, 79-93.
140. 2+ entry in familial Alzheimer's disease. Biochim. Biophys. Acta 2009, 1793, 1050-1057.