Inhibition of recombinant N-type and native high voltage-gated neuronal Ca2+ channels by AdGABA: Mechanism of action studies

Toxicology and Applied Pharmacology

Volumn 250, Issue 3, 2011, Pages 270-277

  Martínez Hernández, Elizabeth ^a   Sandoval, Alejandro ^b   González Ramírez, Ricardo ^c   Zoidis, Grigoris ^d   Felix, Ricardo ^a  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^c HOSPITAL GENERAL DR MANUEL GEA GONZÁLEZ   (Mexico)

^d UNIVERSITY OF ATHENS   (Greece)

Author keywords

2 subunit; AdGABA; Calcium channels; Gabapentin; LAT4

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID DERIVATIVE; ADAMANTANE DERIVATIVE; AMINO ACID; VOLTAGE GATED CALCIUM CHANNEL;

AMINO ACID TRANSPORT; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DRUG ACTIVITY; DRUG INTERACTION; DRUG UPTAKE; HETEROLOGOUS EXPRESSION; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; RAT; SPINAL GANGLION;

ADAMANTANE; AMINO ACID TRANSPORT SYSTEM L; ANIMALS; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS; CALCIUM CHANNELS, N-TYPE; CELL LINE; GAMMA-AMINOBUTYRIC ACID; GANGLIA, SPINAL; HUMANS; MICE; MICE, INBRED BALB C; MUTATION; PATCH-CLAMP TECHNIQUES; PROTEIN SUBUNITS; RABBITS; RATS; RECOMBINANT PROTEINS;

EID: 78651451981     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2010.10.030     Document Type: Article

References (38)

1. Andrade A., Sandoval A., Gonzalez-Ramirez R., Lipscombe D., Campbell K.P., Felix R. The α2δ subunit augments functional expression and modifies the pharmacology of CaV1.3L-type channels. Cell Calcium 2009, 46:282-292.
2. Andrade A., Sandoval A., Oviedo N., De Waard M., Elias D., Felix R. Proteolytic cleavage of the voltage-gated Ca2+ channel α2δ subunit: structural and functional features. Eur. J. Neurosci. 2007, 25:1705-1710.
3. Arikkath J., Chen C.C., Ahern C., Allamand V., Flanagan J.D., Coronado R., Gregg R.G., Campbell K.P. γ1 subunit interactions within the skeletal muscle L-type voltage-gated calcium channels. J. Biol. Chem. 2003, 278:1212-1219.
4. Arikkath J., Campbell K.P. Auxiliary subunits: essential components of the voltage-gated calcium channel complex. Curr. Opin. Neurobiol. 2003, 13:298-307.
5. Avila G., Sandoval A., Felix R. Intramembrane charge movement associated with endogenous K+ channel activity in HEK-293 cells. Cell. Mol. Neurobiol. 2004, 24:317-330.
6. Bernstein G.M., Jones O.T. Kinetics of internalization and degradation of N-type voltage-gated calcium channels: role of the α2δ subunit. Cell Calcium 2007, 41:27-40.
7. Bichet D., Cornet V., Geib S., Carlier E., Volsen S., Hoshi T., Mori Y., De Waard M. The I-II loop of the Ca2+ channel α1 subunit contains an endoplasmic reticulum retention signal antagonized by the β subunit. Neuron 2000, 25:177-190.
8. Bodoy S., Martín L., Zorzano A., Palacín M., Estévez R., Bertran J. Identification of LAT4, a novel amino acid transporter with system L activity. J. Biol. Chem. 2005, 280:12002-12011.
9. Brown J.P., Dissanayake V.U., Briggs A.R., Milic M.R., Gee N.S. Isolation of the [3H]gabapentin-binding protein/α2δ Ca2+ channel subunit from porcine brain: development of a radioligand binding assay for α2δ subunits using [3H]leucine. Anal. Biochem. 1998, 255:236-243.
10. Cantí C., Nieto-Rostro M., Foucault I., Heblich F., Wratten J., Richards M.W., Hendrich J., Douglas L., Page K.M., Davies A., Dolphin A.C. The metal-ion-dependent adhesion site in the Von Willebrand factor-A domain of α2β subunits is key to trafficking voltage-gated Ca2+ channels. Proc. Natl Acad. Sci. USA 2005, 102:11230-11235.
11. Castellano A., Wei X., Birnbaumer L., Perez-Reyes E. Cloning and expression of a third calcium channel β subunit. J. Biol. Chem. 1993, 268:3450-3455.
12. Catterall W.A. Structure and regulation of voltage-gated Ca2+ channels. Annu. Rev. Cell Dev. Biol. 2000, 16:521-555.
13. Davies A., Kadurin I., Alvarez-Laviada A., Douglas L., Nieto-Rostro M., Bauer C.S., Pratt W.S., Dolphin A.C. The α2δ subunits of voltage-gated calcium channels form GPI-anchored proteins, a posttranslational modification essential for function. Proc. Natl Acad. Sci. USA 2010, 107:1654-1659.
14. Dirksen R.T. Bi-directional coupling between dihydropyridine receptors and ryanodine receptors. Front. Biosci. 2002, 7:d659-d670.
15. Dooley D.J., Taylor C.P., Donevan S., Feltner D. Ca2+ channel α2δ ligands: novel modulators of neurotransmission. Trends Pharmacol. Sci. 2007, 28:75-82.
16. Felix R. Voltage-dependent Ca2+ channel α2δ auxiliary subunit: structure, function and regulation. Recept. Channels 1999, 6:351-362.
17. Felix R. Molecular regulation of voltage-gated Ca2+ channels. J. Recept. Signal Transduct. Res. 2005, 25:57-71.
18. Felix R., Gurnett C.A., De Waard M., Campbell K.P. Dissection of functional domains of the voltage-dependent Ca2+ channel α2δ subunit. J. Neurosci. 1997, 17:6884-6891.
19. Fujita Y., Mynlieff M., Dirksen R.T., Kim M.S., Niidome T., Nakai J., Friedrich T., Iwabe N., Miyata T., Furuichi T., Furutama D., Mikoshiba K., Mori Y., Beam K.G. Primary structure and functional expression of the ω-conotoxin-sensitive N-type calcium channel from rabbit brain. Neuron 1993, 10:585-598.
20. Gee N.S., Brown J.P., Dissanayake V.U., Offord J., Thurlow R., Woodruff G.N. The novel anticonvulsant drug, gabapentin (Neurontin), binds to the α2β subunit of a calcium channel. J. Biol. Chem. 1996, 271:5768-5776.
21. Gurnett C.A., De Waard M., Campbell K.P. Dual function of the voltage-dependent Ca2+ channel α2β subunit in current stimulation and subunit interaction. Neuron 1996, 16:431-440.
22. Hendrich J., Van Minh A.T., Heblich F., Nieto-Rostro M., Watschinger K., Striessnig J., Wratten J., Davies A., Dolphin A.C. Pharmacological disruption of calcium channel trafficking by the α2δ ligand gabapentin. Proc. Natl Acad. Sci. USA 2008, 105:3628-3633.
23. Kim H.L., Kim H., Lee P., King R.G., Chin H. Rat brain expresses an alternatively spliced form of the dihydropyridine-sensitive L-type Ca2+ channel α2δ subunit. Proc. Natl Acad. Sci. USA 1992, 89:3251-3255.
24. Klockner U., Lee J.H., Cribbs L.L., Daud A., Hescheler J., Pereverzev A., Perez-Reyes E., Schneider T. Comparison of the Ca2+ currents induced by expression of three cloned α1 subunits, α1G, α1H and α1I, of low-voltage-activated T-type Ca2+ channels. Eur. J. Neurosci. 1999, 11:4171-4178.
25. Luo Z.D., Chaplan S.R., Higuera E.S., Sorkin L.S., Stauderman K.A., Williams M.E., Yaksh T.L. Upregulation of dorsal root ganglion α2δ calcium channel subunit and its correlation with allodynia in spinal nerve-injured rats. J. Neurosci. 2001, 21:1868-1875.
26. Luo Z.D., Calcutt N.A., Higuera E.S., Valder C.R., Song Y.H., Svensson C.I., Myers R.R. Injury type-specific calcium channel α2δ-1 subunit up-regulation in rat neuropathic pain models correlates with antiallodynic effects of gabapentin. J. Pharmacol. Exp. Ther. 2002, 303:1199-1205.
27. Marais E., Klugbauer N., Hofmann F. Calcium channel α2δ subunits-structure and gabapentin binding. Mol. Pharmacol. 2001, 59:1243-1248.
28. McCobb D.P., Beam K.G. Action potential waveform voltage-clamp commands reveal striking differences in calcium entry via low and high voltage-activated calcium channels. Neuron 1991, 7:119-127.
29. Perez-Reyes E. Molecular characterization of T-type calcium channels. Cell Calcium 2006, 40:89-96.
30. Sandoval A., Oviedo N., Andrade A., Felix R. Glycosylation of asparagines 136 and 184 is necessary for the α2δ subunit-mediated regulation of voltage-gated Ca2+ channels. FEBS Lett. 2004, 576:21-26.
31. Sandoval A., Andrade A., Beedle A.M., Campbell K.P., Felix R. Inhibition of recombinant N-type CaV channels by the γ2 subunit involves unfolded protein response (UPR)-dependent and UPR-independent mechanisms. J. Neurosci. 2007, 27:3317-3327.
32. Sandoval A., Arikkath J., Monjaraz E., Campbell K.P., Felix R. γ1-dependent down-regulation of recombinant voltage-gated Ca2+ channels. Cell. Mol. Neurobiol. 2007, 27:901-908.
33. Sandoz G., Bichet D., Cornet V., Mori Y., Felix R., De Waard M. Distinct properties and differential β subunit regulation of two C-terminal isoforms of the P/Q-type Ca2+-channel α1A subunit. Eur. J. Neurosci. 2001, 14:987-997.
34. Su T.Z., Feng M.R., Weber M.L. Mediation of highly concentrative uptake of pregabalin by L-type amino acid transport in Chinese hamster ovary and Caco-2 cells. J. Pharmacol. Exp. Ther. 2005, 313:1406-1415.
35. Vega-Hernandez A., Felix R. Down-regulation of N-type voltage-activated Ca2+ channels by gabapentin. Cell. Mol. Neurobiol. 2002, 22:185-190.
36. Walker D., Bichet D., Geib S., Mori E., Cornet V., Snutch T.P., Mori Y., De Waard M. A new β subtype-specific interaction in α1A subunit controls P/Q-type Ca2+ channel activation. J. Biol. Chem. 1999, 274:12383-12390.
37. Wang M.H., Offord J., Oxender D.L., Su T.Z. Structural requirement of the calcium-channel subunit α2δ for gabapentin binding. Biochem. J. 1999, 342:313-320.
38. Zoidis G., Papanastasiou I., Dotsikas I., Sandoval A., Dos Santos R.G., Papadopoulou-Daifoti Z., Vamvakides A., Kolocouris N., Felix R. The novel GABA adamantane derivative (AdGABA): design, synthesis, and activity relationship with gabapentin. Bioorg. Med. Chem. 2005, 13:2791-2798.