RGK small GTPases and regulation of CaV2 channels

Modulation of Presynaptic Calcium Channels

Volumn 9789400763340, Issue , 2013, Pages 131-149

  Charnet, Pierre ^a   Scamps, Frédérique ^b   Rousset, Matthieu ^a   Menard, Claudine ^a   Bellis, Michel ^a   Cens, Thierry ^a  

^a Centre National de la Recherche Scientifique   (France)

^b Montpellier University Medical Center   (France)

Author keywords

Beta subunits; Heterologous expression; RGK GTPases; Trafficking; Voltage clamp

Indexed keywords

EID: 84925503485     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-94-007-6334-0_6     Document Type: Chapter

References (72)

1. Bannister RA, Colecraft HM, Beam KG (2008) Rem inhibits skeletal muscle EC coupling by reducing the number of functional L-type Ca2C channels. Biophys J 94:2631-2638
2. Beguin P, Nagashima K, Gonoi T, Shibasaki T, Takahashi K, Kashima Y, Ozaki N, Geering K, Iwanaga T, Seino S (2001) Regulation of Ca2C channel expression at the cell surface by the small G-protein kir/Gem. Nature 411:701-706
3. Beguin P, Mahalakshmi RN, Nagashima K, Cher DH, Kuwamura N, Yamada Y, Seino Y, Hunziker W (2005a) Roles of 14-3-3 and calmodulin binding in subcellular localization and function of the small G-protein Rem2. Biochem J 390:67-75
4. Beguin P, Mahalakshmi RN, Nagashima K, Cher DH, Takahashi A, Yamada Y, Seino Y, Hunziker W (2005b) 14-3-3 and calmodulin control subcellular distribution of Kir/Gem and its regulation of cell shape and calcium channel activity. J Cell Sci 118:1923-1934
5. Beguin P, Mahalakshmi RN, Nagashima K, Cher DH, Ikeda H, Yamada Y, Seino Y, Hunziker W (2006) Nuclear sequestration of beta-subunits by Rad and Rem is controlled by 14-3-3 and calmodulin and reveals a novel mechanism for Ca2C channel regulation. J Mol Biol 355:34-46
6. Beguin P, Ng YJ, Krause C, Mahalakshmi RN, Ng MY, Hunziker W (2007) RGK small GTPbinding proteins interact with the nucleotide kinase domain of Ca2C-channel beta-subunits via an uncommon effector binding domain. J Biol Chem 282:11509-11520
7. Bierings R, Beato M, Edel MJ (2008) An endothelial cell genetic screen identifies the GTPase Rem2 as a suppressor of p19ARF expression that promotes endothelial cell proliferation and angiogenesis. J Biol Chem 283:4408-4416
8. Bilan PJ, Moyers JS, Kahn CR (1998) The ras-related protein rad associates with the cytoskeleton in a non-lipid-dependent manner. Exp Cell Res 242:391-400
9. Buraei Z, Yang J (2010) The beta subunit of voltage-gated Ca2C channels. Physiol Rev 90: 1461-1506
10. Catterall WA (2011) Voltage-gated calcium channels. Cold Spring Harb Perspect Biol 3:a003947
11. Cens T, Restituito S, Rousset M, Charnet P (2005) Role of beta subunit in voltage-gated Ca2C channels. In: Zamponi G (ed) Voltage-gated calcium channels. Kluwer Academic/Plenum Publishing, New York, pp 95-112
12. Chen H, Puhl HL III, Niu SL, Mitchell DC, Ikeda SR (2005) Expression of Rem2, an RGK family small GTPase, reduces N-type calcium current without affecting channel surface density. J Neurosci 25:9762-9772
13. Correll RN, Pang C, Finlin BS, Dailey AM, Satin J, Andres DA (2007) Plasma membrane targeting is essential for Rem-mediated Ca2C channel inhibition. J Biol Chem 282:28431-28440
14. Correll RN, Botzet GJ, Satin J, Andres DA, Finlin BS (2008a) Analysis of the Rem2-voltage dependant calcium channel beta subunit interaction and Rem2 interaction with phosphorylated phosphatidylinositide lipids. Cell Signal 20:400-408
15. Correll RN, Pang C, Niedowicz DM, Finlin BS, Andres DA (2008b) The RGK family of GTP-binding proteins: regulators of voltage-dependent calcium channels and cytoskeleton remodeling. Cell Signal 20:292-300
16. Crump SM, Correll RN, Schroder EA, Lester WC, Finlin BS, Andres DA, Satin J (2006) L-type calcium channel alpha-subunit and protein kinase inhibitorsmodulate Rem-mediated regulation of current. Am J Physiol Heart Circ Physiol 291:H1959-H1971
17. Davies A, Kadurin I, Alvarez-Laviada A, Douglas L, Nieto-Rostro M, Bauer CS, Pratt WS, Dolphin AC (2010) The alpha2delta subunits of voltage-gated calcium channels form GPIanchored proteins, a posttranslational modification essential for function. Proc Natl Acad Sci USA 107:1654-1659
18. De Waard M, Pragnell M, Campbell KP (1994) Ca2C channel regulation by a conserved beta subunit domain. Neuron 13:495-503
19. Dolmetsch R (2003) Excitation-transcription coupling: signaling by ion channels to the nucleus. Sci STKE 2003:E4
20. Dolphin AC (2003) Beta subunits of voltage-gated calcium channels. J Bioenerg Biomembr 35:599-620
21. Dolphin AC (2012) Calcium channel auxiliary alpha2delta and beta subunits: trafficking and one step beyond. Nat Rev Neurosci 13:542-555
22. Fan M, Buraei Z, Luo HR, Levenson-Palmer R, Yang J (2010) Direct inhibition of P/Q-type voltage-gated Ca2C channels by Gem does not require a direct Gem/CaVbeta interaction. Proc Natl Acad Sci U S A 107:14887-14892
23. Fan M, Zhang WK, Buraei Z, Yang J (2012) Molecular determinants of gem protein inhibition of P/Q-type Ca2C channels. J Biol Chem 287:22749-22758
24. Finlin BS, Andres DA (1997) Rem is a new member of the Rad-and Gem/Kir Ras-related GTP-binding protein family repressed by lipopolysaccharide stimulation. J Biol Chem 272: 21982-21988
25. Finlin BS, Shao H, Kadono-Okuda K, Guo N, Andres DA (2000) Rem2, a new member of the Rem/Rad/Gem/Kir family of Ras-related GTPases. Biochem J 347:223-231
26. Finlin BS, Mosley AL, Crump SM, Correll RN, Ozcan S, Satin J, Andres DA (2005) Regulation of L-type Ca2C channel activity and insulin secretion by the Rem2 GTPase. J Biol Chem 280:41864-41871
27. Finlin BS, Correll RN, Pang C, Crump SM, Satin J, Andres DA (2006) Analysis of the complex between Ca2C channel beta-subunit and the Rem GTPase. J Biol Chem 281:23557-23566
28. Fischer R, Wei Y, Anagli J, Berchtold MW (1996) Calmodulin binds to and inhibits GTP binding of the ras-like GTPase Kir/Gem. J Biol Chem 271:25067-25070
29. Flynn R, Chen L, Hameed S, Spafford JD, Zamponi GW (2008) Molecular determinants of Rem2 regulation of N-type calcium channels. Biochem Biophys Res Commun 368:827-831
30. Fu Y, Westenbroek RE, Yu FH, Clark JP III, Marshall MR, Scheuer T., Catterall WA (2011) Deletion of the distal C-terminus of CaV1.2 channel leads to loss of beta-adrenergic regulation and heart failure in vivo. J Biol Chem 286:12617-12626
31. Ghiretti AE, Paradis S (2011) The GTPase Rem2 regulates synapse development and dendritic morphology. Dev Neurobiol 71:374-389
32. Gomez-Ospina N, Tsuruta F, Barreto-Chang O, Hu L, Dolmetsch R (2006) The C terminus of the L-type voltage-gated calcium channel CaV1.2 encodes a transcription factor. Cell 127: 591-606
33. Gunton JE, Sisavanh M, Stokes RA, Satin J, Satin LS, Zhang M, Liu SM, Cai W, Cheng K, Cooney GJ, Laybutt DR, So T, Molero JC, Grey ST, Andres DA, Rolph MS, Mackay CR (2012) Mice deficient in GEM GTPase show abnormal glucose homeostasis due to defects in beta-cell calcium handling. PLoS One 7:e39462
34. Hibino H, Pironkova R, Onwumere O, Rousset M, Charnet P, Hudspeth AJ, Lesage F (2003) Direct interaction with a nuclear protein and regulation of gene silencing by a variant of the Ca2Cchannel beta 4 subunit. Proc Natl Acad Sci U S A 100:307-312
35. Iftinca M, Hamid J, Chen L, Varela D, Tadayonnejad R, Altier C, Turner RW, Zamponi GW (2007) Regulation of T-type calcium channels by Rho-associated kinase. Nat Neurosci 10: 854-860
36. Ilany J, Bilan PJ, Kapur S, Caldwell JS, Patti ME, Marette A, Kahn CR (2006) Overexpression of Rad in muscle worsens diet-induced insulin resistance and glucose intolerance and lowers plasma triglyceride level. Proc Natl Acad Sci U S A 103:4481-4486
37. Kordasiewicz HB, Thompson RM, Clark HB, Gomez CM (2006) C-termini of P/Q-type Ca2C channel alpha1A subunits translocate to nuclei and promote polyglutamine-mediated toxicity. Hum Mol Genet 15:1587-1599
38. Leone A, Mitsiades N, Ward Y, Spinelli B, Poulaki V, Tsokos M, Kelly K (2001) The Gem GTP-binding protein promotes morphological differentiation in neuroblastoma. Oncogene 20: 3217-3225
39. Leyris JP, Gondeau C, Charnet A, Delattre C, Rousset M, Cens T, Charnet P (2009) RGK GTPasedependent CaV2.1 Ca2C channel inhibition is independent of CaVbeta-subunit-induced current potentiation. FASEB J 23:2627-2638
40. Maguire J, Santoro T, Jensen P, Siebenlist U, Yewdell J, Kelly K (1994) Gem: an induced, immediate early protein belonging to the Ras family. Traffic 265:241-244
41. Magyar J, Kiper CE, Sievert G, Cai W, Shi GX, Crump SM, Li L, Niederer S, Smith N, Andres DA, Satin J (2012) Rem-GTPase regulates cardiac myocyte L-type calcium current. Channels (Austin) 6:166-173
42. Mahalakshmi RN, Nagashima K, Ng MY, Inagaki N, Hunziker W, Beguin P (2007) Nuclear transport of Kir/Gem requires specific signals and importin alpha5 and is regulated by calmodulin and predicted serine phosphorylations. Traffic 8:1150-1163
43. MarshallMR, Clark JP,Westenbroek R, Yu FH, Scheuer T., CatterallWA (2011) Functional roles of a C-terminal signaling complex of CaV1 channels and A kinase anchoring protein-15 in brain neurons. J Biol Chem 286:12627-12639
44. Muller CS, Haupt A, Bildl W, Schindler J, Knaus HG, Meissner M, Rammner B, Striessnig J, Flockerzi V, Fakler B, Schulte U (2010) Quantitative proteomics of the CaV2 channel nanoenvironments in the mammalian brain. Proc Natl Acad Sci U S A 107:14950-14957
45. Murakami M, Suzuki T, Nakagawasai O, Murakami H, Murakami S, Esashi A, Taniguchi R, Yanagisawa T, Tan-No K, Miyoshi I, Sasano H, Tadano T (2001) Distribution of various calcium channel alpha (1) subunits in murine DRG neurons and antinociceptive effect of omegaconotoxin SVIB in mice. Brain Res 903:231-236
46. Murata M, Cingolani E, McDonald AD, Donahue JK, Marban E (2004) Creation of a genetic calcium channel blocker by targeted gem gene transfer in the heart. Circ Res 95:398-405
47. Opatowsky Y, Sasson Y, Shaked I, Ward Y, Chomsky-Hecht O, Litvak Y, Selinger Z, Kelly K, Hirsch JA (2006) Structure-function studies of the G-domain from human gem, a novel small G-protein. FEBS Lett 580:5959-5964
48. Pan JY, Fieles WE, White AM, Egerton MM, Silberstein DS (2000) Ges, a human GTPase of the Rad/Gem/Kir family, promotes endothelial cell sprouting and cytoskeleton reorganization. J Cell Biol 149:1107-1116
49. Pang C, Crump SM, Jin L, Correll RN, Finlin BS, Satin J, Andres DA (2010) Rem GTPase interacts with the proximal CaV1.2 C-terminus and modulates calcium-dependent channel inactivation. Channels (Austin) 4:192-202
50. Paradis S, Harrar DB, Lin Y, Koon AC, Hauser JL, Griffith EC, Zhu L, Brass LF, Chen C, Greenberg ME (2007) An RNAi-based approach identifies molecules required for glutamatergic and GABAergic synapse development. Neuron 53:217-232
51. Piddini E, Schmid JA, de Martin R, Dotti CG (2001) The Ras-like GTPase Gem is involved in cell shape remodelling and interacts with the novel kinesin-like protein KIF9. EMBO J 20: 4076-4087
52. Reynet C, Kahn CR (1993) Rad: a member of the Ras family overexpressed in muscle of type II diabetic humans. Traffic 262:1441-1444
53. Rousset M, Charnet P, Cens T (2005) Structure of the calcium channel beta subunit: the place of the beta-interaction domain. Med Sci (Paris) 21:279-283
54. Sasaki T, Shibasaki T, Beguin P, Nagashima K, Miyazaki M, Seino S (2005) Direct inhibition of the interaction between alpha-interaction domain and beta-interaction domain of voltagedependent Ca2C channels by Gem. J Biol Chem 280:9308-9312
55. Seu L, Pitt GS (2006) Dose-dependent and isoform-specific modulation of Ca2C channels by RGK GTPases. J Gen Physiol 128:605-613
56. Splingard A,Menetrey J, Perderiset M, Cicolari J, Regazzoni K, Hamoudi F, Cabanie L, ElMarjou A, Wells A, Houdusse A, de Gunzburg J (2007) Biochemical and structural characterization of the gem GTPase. J Biol Chem 282:1905-1915
57. Tadmouri A, Kiyonaka S, Barbado M, Rousset M, Fablet K, Sawamura S, Bahembera E, Pernet-Gallay K, Arnoult C, Miki T, Sadoul K, Gory-Faure S, Lambrecht C, Lesage F, Akiyama S, Khochbin S, Baulande S, Janssens V, Andrieux A, Dolmetsch R, Ronjat M, Mori Y, De Waard M (2012) Cacnb4 directly couples electrical activity to gene expression, a process defective in juvenile epilepsy. EMBO J 31:3730-3744
58. Walker D, Bichet D, Campbell KP, DeWaard M (1998) A beta 4 isoform-specific interaction site in the carboxyl-terminal region of the voltage-dependent Ca2C channel alpha 1A subunit. J Biol Chem 273:2361-2367
59. Walker D, Bichet D, Geib S,Mori E, Cornet V, Snutch TP,Mori Y, DeWaard M (1999) A new beta subtype-specific interaction in alpha1A subunit controls P/Q-type Ca2C channel activation. J Biol Chem 274:12383-12390
60. Wang HG, Wang C, Pitt GS (2011) Rem2-targeted shRNAs reduce frequency of miniature excitatory postsynaptic currents without altering voltage-gated Ca2C currents. PLoS One 6:e25741
61. Ward Y, Kelly K (2006) Gem protein signaling and regulation. Methods Enzymol 407:468-483
62. Ward Y, Yap SF, Ravichandran V, Matsumura F, Ito M, Spinelli B, Kelly K (2002) The GTP binding proteins Gem and Rad are negative regulators of the Rho-Rho kinase pathway. J Cell Biol 157:291-302
63. Ward Y, Spinelli B, Quon MJ, Chen H, Ikeda SR, Kelly K (2004) Phosphorylation of critical serine residues in gem separates cytoskeletal reorganization from down-regulation of calcium channel activity. Mol Cell Biol 24:651-661
64. Wheeler DG, Groth RD, Ma H, Barrett CF, Owen SF, Safa P, Tsien RW (2012) CaV1 and CaV2 channels engage distinct modes of Ca2C signaling to control CREB-dependent gene expression. Cell 149:1112-1124
65. Xu X, Colecraft HM (2009) Engineering proteins for custom inhibition of CaV channels. Physiology (Bethesda) 24:210-218
66. Xu X, Marx SO, Colecraft HM (2010) Molecular mechanisms, and selective pharmacological rescue, of Rem-inhibited CaV1.2 channels in heart. Circ Res 107:620-630
67. Yada H, Murata M, Shimoda K, Yuasa S, Kawaguchi H, Ieda M, Adachi T, Murata M, Ogawa S, Fukuda K (2007) Dominant negative suppression of Rad leads to QT prolongation and causes ventricular arrhythmias via modulation of L-type Ca2C channels in the heart. Circ Res 101: 69-77
68. Yang T, Suhail Y, Dalton S, Kernan T, Colecraft HM (2007) Genetically encoded molecules for inducibly inactivating CaV channels. Nat Chem Biol 3:795-804
69. Yang T, Xu X, Kernan T, Wu V, Colecraft HM (2010) Rem, a member of the RGK GTPases, inhibits recombinant CaV1.2 channels using multiple mechanisms that require distinct conformations of the GTPase. J Physiol 588:1665-1681
70. Yang T, Puckerin A, Colecraft HM (2012) Distinct RGK GTPases differentially use alpha1-and auxiliary beta-binding-dependent mechanisms to inhibit CaV1.2/CaV2.2 channels. PLoS One 7:e37079
71. Yanuar A, Sakurai S, Kitano K, Hakoshima T (2006) Crystal structure of human Rad GTPase of the RGK-family. Genes Cells 11:961-968
72. Zhang Y, Yamada Y, Fan M, Bangaru SD, Lin B, Yang J (2010) The beta subunit of voltage-gated Ca2C channels interacts with and regulates the activity of a novel isoform of Pax6. J Biol Chem 285:2527-2536