Effect of voltage sensitive fluorescent proteins on neuronal excitability (Akemann et al. 2009)

 Download zip file   Auto-launch 
Help downloading and running models
Accession:123453
"Fluorescent protein voltage sensors are recombinant proteins that are designed as genetically encoded cellular probes of membrane potential using mechanisms of voltage-dependent modulation of fluorescence. Several such proteins, including VSFP2.3 and VSFP3.1, were recently reported with reliable function in mammalian cells. ... Expression of these proteins in cell membranes is accompanied by additional dynamic membrane capacitance, ... We used recordings of sensing currents and fluorescence responses of VSFP2.3 and of VSFP3.1 to derive kinetic models of the voltage-dependent signaling of these proteins. Using computational neuron simulations, we quantitatively investigated the perturbing effects of sensing capacitance on the input/output relationship in two central neuron models, a cerebellar Purkinje and a layer 5 pyramidal neuron. ... ". The Purkinje cell model is included in ModelDB.
Reference:
1 . Akemann W, Lundby A, Mutoh H, Knopfel T (2009) Effect of voltage sensitive fluorescent proteins on neuronal excitability. Biophys J 96:3959-76 [PubMed]
Model Information (Click on a link to find other models with that property)
Model Type: Neuron or other electrically excitable cell;
Brain Region(s)/Organism: Cerebellum;
Cell Type(s): Cerebellum purkinje cell;
Channel(s): I Na,t; I A; I K; I h; I K,Ca; I Calcium;
Gap Junctions:
Receptor(s):
Gene(s): Kv1.1 KCNA1; Kv4.3 KCND3; Kv3.3 KCNC3; Kv3.4 KCNC4; HCN1;
Transmitter(s):
Simulation Environment: NEURON;
Model Concept(s):
Implementer(s): Akemann, Walther [akemann at brain.riken.jp];
Search NeuronDB for information about:  Cerebellum purkinje cell; I Na,t; I A; I K; I h; I K,Ca; I Calcium;

Akemann W, Lundby A, Mutoh H, Knopfel T (2009) Effect of voltage sensitive fluorescent proteins on neuronal excitability. Biophys J 96:3959-76[PubMed]

References and models cited by this paper

References and models that cite this paper

Aggarwal SK, MacKinnon R (1996) Contribution of the S4 segment to gating charge in the Shaker K+ channel. Neuron 16:1169-77 [PubMed]

Ahern CA, Horn R (2004) Specificity of charge-carrying residues in the voltage sensor of potassium channels. J Gen Physiol 123:205-16 [PubMed]

Akemann W, Knopfel T (2006) Interaction of Kv3 potassium channels and resurgent sodium current influences the rate of spontaneous firing of Purkinje neurons. J Neurosci 26:4602-12 [Journal] [PubMed]

   Cerebellar purkinje cell: interacting Kv3 and Na currents influence firing (Akemann, Knopfel 2006) [Model]

Antic S, Major G, Zecevic D (1999) Fast optical recordings of membrane potential changes from dendrites of pyramidal neurons. J Neurophysiol 82:1615-21 [Journal] [PubMed]

Armstrong CM, Bezanilla F (1974) Charge movement associated with the opening and closing of the activation gates of the Na channels. J Gen Physiol 63:533-52 [PubMed]

Ataka K, Pieribone VA (2002) A genetically targetable fluorescent probe of channel gating with rapid kinetics. Biophys J 82:509-16 [PubMed]

Baker BJ, Mutoh H, Dimitrov D, Akemann W, Perron A, Iwamoto Y, Jin L, Cohen LB, Isacoff EY, P (2008) Genetically encoded fluorescent sensors of membrane potential. Brain Cell Biol 36:53-67 [PubMed]

Bean BP (2007) The action potential in mammalian central neurons. Nat Rev Neurosci 8:451-65 [PubMed]

Bezanilla F (2000) The voltage sensor in voltage-dependent ion channels. Physiol Rev 80:555-92 [PubMed]

Bezanilla F, Armstrong CM (1974) Gating currents of the sodium channels: three ways to block them. Science 183:753-4 [PubMed]

Chanda B, Blunck R, Faria LC, Schweizer FE, Mody I, Bezanilla F (2005) A hybrid approach to measuring electrical activity in genetically specified neurons. Nat Neurosci 8:1619-26 [PubMed]

Chang SY, Zagha E, Kwon ES, Ozaita A, Bobik M, Martone ME, Ellisman MH, Heintz N, Rudy B (2007) Distribution of Kv3.3 potassium channel subunits in distinct neuronal populations of mouse brain. J Comp Neurol 502:953-72 [PubMed]

Chitwood RA, Hubbard A, Jaffe DB (1999) Passive electrotonic properties of rat hippocampal CA3 interneurones. J Physiol 515 ( Pt 3):743-56 [PubMed]

   [66 reconstructed morphologies on NeuroMorpho.Org]

Cohen LB, Salzberg BM, Davila HV, Ross WN, Landowne D, Waggoner AS, Wang CH (1974) Changes in axon fluorescence during activity: molecular probes of membrane potential. J Membr Biol 19:1-36 [PubMed]

Colbert CM, Johnston D (1996) Axonal action-potential initiation and Na+ channel densities in the soma and axon initial segment of subicular pyramidal neurons. J Neurosci 16:6676-86 [PubMed]

DiFranco M, Capote J, Quinonez M, Vergara JL (2007) Voltage-dependent dynamic FRET signals from the transverse tubules in mammalian skeletal muscle fibers. J Gen Physiol 130:581-600 [PubMed]

Dimitrov D, He Y, Mutoh H, Baker BJ, Cohen L, Akemann W, Knöpfel T (2007) Engineering and characterization of an enhanced fluorescent protein voltage sensor. PLoS One 2:e440-16 [PubMed]

Ferezou I, Haiss F, Gentet LJ, Aronoff R, Weber B, Petersen CC (2007) Spatiotemporal dynamics of cortical sensorimotor integration in behaving mice. Neuron 56:907-23 [PubMed]

Fernandez JM, Taylor RE, Bezanilla F (1983) Induced capacitance in the squid giant axon. Lipophilic ion displacement currents. J Gen Physiol 82:331-46 [PubMed]

Fettiplace R, Andrews DM, Haydon DA (1971) The thickness, composition and structure of some lipid bilayers and natural membranes J Membr Biol 5:277-296

Fromherz P, Hubener G, Kuhn B, Hinner MJ (2008) ANNINE-6plus, a voltage-sensitive dye with good solubility, strong membrane binding and high sensitivity. Eur Biophys J 37:509-14 [PubMed]

Gentet LJ, Stuart GJ, Clements JD (2000) Direct measurement of specific membrane capacitance in neurons. Biophys J 79:314-20 [PubMed]

Grinvald A, Hildesheim R, Farber IC, Anglister L (1982) Improved fluorescent probes for the measurement of rapid changes in membrane potential. Biophys J 39:301-8 [PubMed]

Hille B (2001) Ionic Channels of Excitable Membranes

Hines ML, Carnevale NT (1997) The NEURON simulation environment. Neural Comput 9:1179-209 [PubMed]

Hines ML, Carnevale NT (2001) NEURON: a tool for neuroscientists. Neuroscientist 7:123-35 [Journal] [PubMed]

   Spatial gridding and temporal accuracy in NEURON (Hines and Carnevale 2001) [Model]

Hossain MI, Iwasaki H, Okochi Y, Chahine M, Higashijima S, Nagayama K, Okamura Y (2008) Enzyme domain affects the movement of the voltage sensor in ascidian and zebrafish voltage-sensing phosphatases. J Biol Chem 283:18248-59 [PubMed]

Huebner G, Lambacher A, Fromherz (2003) Anellated hemicyanine dyes with large symmetrical solvatochromism of absorption and fluorescence J Phys Chem B 107:7896-7902

Kalyanaraman B, Feix JB, Sieber F, Thomas JP, Girotti AW (1987) Photodynamic action of merocyanine 540 on artificial and natural cell membranes: involvement of singlet molecular oxygen. Proc Natl Acad Sci U S A 84:2999-3003 [PubMed]

Kang J, Huguenard JR, Prince DA (1996) Two types of BK channels in immature rat neocortical pyramidal neurons. J Neurophysiol 76:4194-7 [PubMed]

Khaliq ZM, Gouwens NW, Raman IM (2003) The contribution of resurgent sodium current to high-frequency firing in Purkinje neurons: an experimental and modeling study. J Neurosci 23:4899-912 [PubMed]

   Cerebellar Purkinje Cell: resurgent Na current and high frequency firing (Khaliq et al 2003) [Model]

Khaliq ZM, Raman IM (2006) Relative contributions of axonal and somatic Na channels to action potential initiation in cerebellar Purkinje neurons. J Neurosci 26:1935-44 [PubMed]

Knöpfel T, Díez-García J, Akemann W (2006) Optical probing of neuronal circuit dynamics: genetically encoded versus classical fluorescent sensors. Trends Neurosci 29:160-6 [PubMed]

Kole MH, Brauer AU, Stuart GJ (2007) Inherited cortical HCN1 channel loss amplifies dendritic calcium electrogenesis and burst firing in a rat absence epilepsy model. J Physiol 578:507-25 [Journal] [PubMed]

   [16 reconstructed morphologies on NeuroMorpho.Org]

Kole MH, Ilschner SU, Kampa BM, Williams SR, Ruben PC, Stuart GJ (2008) Action potential generation requires a high sodium channel density in the axon initial segment. Nat Neurosci 11:178-86 [Journal] [PubMed]

   [1 reconstructed morphology on NeuroMorpho.Org]
   Na+ channel dependence of AP initiation in cortical pyramidal neuron (Kole et al. 2008) [Model]

Korngreen A, Sakmann B (2000) Voltage-gated K+ channels in layer 5 neocortical pyramidal neurones from young rats: subtypes and gradients. J Physiol 525 Pt 3:621-39 [PubMed]

   Pyramidal Neuron Deep: K+ kinetics (Korngreen, Sakmann 2000) [Model]

Larsson HP, Baker OS, Dhillon DS, Isacoff EY (1996) Transmembrane movement of the shaker K+ channel S4. Neuron 16:387-97 [PubMed]

Loew LM, Cohen LB, Salzberg BM, Obaid AL, Bezanilla F (1985) Charge-shift probes of membrane potential. Characterization of aminostyrylpyridinium dyes on the squid giant axon. Biophys J 47:71-7 [PubMed]

Logothetis DE, Movahedi S, Satler C, Lindpaintner K, Nadal-Ginard B (1992) Incremental reductions of positive charge within the S4 region of a voltage-gated K+ channel result in corresponding decreases in gating charge. Neuron 8:531-40 [PubMed]

Lundby A, Mutoh H, Dimitrov D, Akemann W, Knopfel T (2008) Engineering of a genetically encodable fluorescent voltage sensor exploiting fast Ci-VSP voltage-sensing movements. PLoS One 3:e2514-16 [PubMed]

Magee JC, Johnston D (1995) Characterization of single voltage-gated Na+ and Ca2+ channels in apical dendrites of rat CA1 pyramidal neurons. J Physiol 487 ( Pt 1):67-90 [PubMed]

Mainen ZF, Joerges J, Huguenard JR, Sejnowski TJ (1995) A model of spike initiation in neocortical pyramidal neurons. Neuron 15:1427-39 [PubMed]

   Spike Initiation in Neocortical Pyramidal Neurons (Mainen et al 1995) [Model]

Mainen ZF, Sejnowski TJ (1996) Influence of dendritic structure on firing pattern in model neocortical neurons. Nature 382:363-6 [Journal] [PubMed]

   [2 reconstructed morphologies on NeuroMorpho.Org]
   Pyramidal Neuron Deep, Superficial; Aspiny, Stellate (Mainen and Sejnowski 1996) [Model]

Martina M, Metz AE, Bean BP (2007) Voltage-dependent potassium currents during fast spikes of rat cerebellar Purkinje neurons: inhibition by BDS-I toxin. J Neurophysiol 97:563-71 [PubMed]

Martina M, Yao GL, Bean BP (2003) Properties and functional role of voltage-dependent potassium channels in dendrites of rat cerebellar Purkinje neurons. J Neurosci 23:5698-707 [PubMed]

McMahon A, Fowler SC, Perney TM, Akemann W, Knöpfel T, Joho RH (2004) Allele-dependent changes of olivocerebellar circuit properties in the absence of the voltage-gated potassium channels Kv3.1 and Kv3.3. Eur J Neurosci 19:3317-27 [PubMed]

Murata Y, Iwasaki H, Sasaki M, Inaba K, Okamura Y (2005) Phosphoinositide phosphatase activity coupled to an intrinsic voltage sensor. Nature 435:1239-43 [PubMed]

Mutoh H, Perron A, Dimitrov D, Iwamoto Y, Akemann W, Chudakov DM, Knöpfel T (2009) Spectrally-resolved response properties of the three most advanced FRET based fluorescent protein voltage probes. PLoS One 4:e4555-67 [PubMed]

Oberhauser AF, Fernandez JM (1995) Hydrophobic ions amplify the capacitive currents used to measure exocytotic fusion. Biophys J 69:451-9 [PubMed]

Palmer LM, Stuart GJ (2006) Site of action potential initiation in layer 5 pyramidal neurons. J Neurosci 26:1854-63 [PubMed]

Perozo E, Santacruz-Toloza L, Stefani E, Bezanilla F, Papazian DM (1994) S4 mutations alter gating currents of Shaker K channels. Biophys J 66:345-54 [PubMed]

Sakai R, Repunte-Canonigo V, Raj CD, Knöpfel T (2001) Design and characterization of a DNA-encoded, voltage-sensitive fluorescent protein. Eur J Neurosci 13:2314-8 [PubMed]

Schmid G, Goychuk I, Hanggi P (2006) Capacitance fluctuations causing channel noise reduction in stochastic Hodgkin-Huxley systems. Phys Biol 3:248-54 [PubMed]

Seoh SA, Sigg D, Papazian DM, Bezanilla F (1996) Voltage-sensing residues in the S2 and S4 segments of the Shaker K+ channel. Neuron 16:1159-67 [PubMed]

Shoham D, Glaser DE, Arieli A, Kenet T, Wijnbergen C, Toledo Y, Hildesheim R, Grinvald A (1999) Imaging cortical dynamics at high spatial and temporal resolution with novel blue voltage-sensitive dyes. Neuron 24:791-802 [PubMed]

Siegel MS, Isacoff EY (1997) A genetically encoded optical probe of membrane voltage. Neuron 19:735-41 [PubMed]

Sjulson L, Miesenböck G (2007) Optical recording of action potentials and other discrete physiological events: a perspective from signal detection theory. Physiology (Bethesda) 22:47-55 [PubMed]

Sjulson L, Miesenböck G (2008) Rational optimization and imaging in vivo of a genetically encoded optical voltage reporter. J Neurosci 28:5582-93 [PubMed]

Slovin H, Arieli A, Hildesheim R, Grinvald A (2002) Long-term voltage-sensitive dye imaging reveals cortical dynamics in behaving monkeys. J Neurophysiol 88:3421-38 [PubMed]

Stefani E, Toro L, Perozo E, Bezanilla F (1994) Gating of Shaker K+ channels: I. Ionic and gating currents. Biophys J 66:996-1010 [PubMed]

Stuart G, Hausser M (1994) Initiation and spread of sodium action potentials in cerebellar Purkinje cells. Neuron 13:703-12 [PubMed]

Stuart G, Spruston N, Sakmann B, Hausser M (1997) Action potential initiation and backpropagation in neurons of the mammalian CNS. Trends Neurosci 20:125-31 [PubMed]

Swaminathan R, Hoang CP, Verkman AS (1997) Photobleaching recovery and anisotropy decay of green fluorescent protein GFP-S65T in solution and cells: cytoplasmic viscosity probed by green fluorescent protein translational and rotational diffusion. Biophys J 72:1900-7 [PubMed]

Thurbon D, Luscher HR, Hofstetter T, Redman SJ (1998) Passive electrical properties of ventral horn neurons in rat spinal cord slices. J Neurophysiol 79:2485-502 [Journal] [PubMed]

Tsutsui H, Karasawa S, Okamura Y, Miyawaki A (2008) Improving membrane voltage measurements using FRET with new fluorescent proteins. Nat Methods 5:683-5 [PubMed]

Villalba-Galea CA, Sandtner W, Dimitrov D, Mutoh H, Knöpfel T, Bezanilla F (2009) Charge movement of a voltage-sensitive fluorescent protein. Biophys J 96:L19-21 [PubMed]

Villalba-Galea CA, Sandtner W, Starace DM, Bezanilla F (2008) S4-based voltage sensors have three major conformations. Proc Natl Acad Sci U S A 105:17600-7 [PubMed]

Weiser M, Vega-Saenz de Miera E, Kentros C, Moreno H, Franzen L, Hillman D, Baker H, Rudy B (1994) Differential expression of Shaw-related K+ channels in the rat central nervous system. J Neurosci 14:949-72 [PubMed]

Weiss TF (1995) Cellular Biophysics Electrical Properties

Yasuda R, Nimchinsky EA, Scheuss V, Pologruto TA, Oertner TG, Sabatini BL, Svoboda K (2004) Imaging calcium concentration dynamics in small neuronal compartments. Sci STKE 2004:pl5-21

Zimmermann D, Kiesel M, Terpitz U, Zhou A, Reuss R, Kraus J, Schenk WA, Bamberg E, Sukhorukov (2008) A combined patch-clamp and electrorotation study of the voltage- and frequency-dependent membrane capacitance caused by structurally dissimilar lipophilic anions. J Membr Biol 221:107-21 [PubMed]

Zimmermann D, Zhou A, Kiesel M, Feldbauer K, Terpitz U, Haase W, Schneider-Hohendorf T, Bambe (2008) Effects on capacitance by overexpression of membrane proteins. Biochem Biophys Res Commun 369:1022-6 [PubMed]

Carnevale NT, Morse TM (1996-2009) Research reports that have used NEURON Web published citations at the NEURON website [Journal]

(73 refs)