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Molecular basis of ancestral vertebrate electroreception

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Abstract

Elasmobranch fishes, including sharks, rays, and skates, use specialized electrosensory organs called ampullae of Lorenzini to detect extremely small changes in environmental electric fields. Electrosensory cells within these ampullae can discriminate and respond to minute changes in environmental voltage gradients through an unknown mechanism. Here we show that the voltage-gated calcium channel CaV1.3 and the big conductance calcium-activated potassium (BK) channel are preferentially expressed by electrosensory cells in little skate (Leucoraja erinacea) and functionally couple to mediate electrosensory cell membrane voltage oscillations, which are important for the detection of specific, weak electrical signals. Both channels exhibit unique properties compared with their mammalian orthologues that support electrosensory functions: structural adaptations in CaV1.3 mediate a low-voltage threshold for activation, and alterations in BK support specifically tuned voltage oscillations. These findings reveal a molecular basis of electroreception and demonstrate how discrete evolutionary changes in ion channel structure facilitate sensory adaptation.

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Figure 1: CaV1.3 and BK channels mediate the major cation currents in electrosensory cells.
Figure 2: Skate CaV has a low voltage threshold.
Figure 3: Positively charged motif confers skate CaV voltage threshold.
Figure 4: Skate BK has a small conductance and short open time.
Figure 5: Intracellular electrostatic adaptations in the pore of skate BK.
Figure 6: ICav and IK tune voltage oscillations and electroreceptive behaviours.

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Change history

  • 12 March 2017

    A minor change was made to the legend to Fig. 1, panel j.

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Acknowledgements

We thank R. Araneda, Y. Kirichok, F. Fieni, N. Ingolia, V. Yorgan, and members of the Julius laboratory for discussions and technical assistance, R. Nicoll for critical reading of the manuscript, and S. Bennett at the Marine Biological Laboratory for help with skates. This work was supported by an NIH Institutional Research Service Award to the UCSF CVRI (T32HL007731 to N.W.B.), a Howard Hughes Medical Institute Fellowship of the Life Sciences Research Foundation (N.W.B.), a Simons Foundation Postdoctoral Fellowship to the Jane Coffin Childs Memorial Fund (D.B.L.), and grants from the NIH (NS081115 and NS055299 to D.J.).

Author information

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Authors

Contributions

N.W.B. designed and performed electrophysiological studies, D.B.L. designed and performed gene expression, anatomical, and behavioural studies, and N.W.B., D.B.L. and D.J. wrote the manuscript.

Corresponding author

Correspondence to David Julius.

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Competing interests

The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 CaV and K+ channel expression in little skate.

a, CaV auxiliary subunit mRNA expression in skate ampullary organs, ampullary canals, skin, and liver. Bars represent fragments per kilobase of exon per million fragments mapped (FPKM). b, Ten most highly expressed K+ channel α-subunit transcripts in ampullary organs.

Extended Data Figure 2 Skate CaV ion selectivity and Ca2+-dependent inactivation.

a–c, Representative currents measured from electrosensory cells (native ICaV, a), HEK293 cells expressing skate CaV1.3 (sCaV, b), or HEK293 cells expressing rat CaV1.3 (rCaV, c) in the presence of 5 mM extracellular Ca2+, Ba2+, or Sr2+. At the end of a 200-ms voltage pulse eliciting maximal current, approximately 50% of current remained in native electrosensory cell ICav or HEK293 cells heterologously expressing sCaV1.3, whereas cells expressing rCaV1.3 had only about 20% of current remaining. In electrosensory cells or cells expressing heterologous sCaV1.3 or rCaV1.3, the percentage of remaining current was significantly increased by replacing extracellular Ca2+ with Ba2+ or Sr2+ (P < 0.05, one-way ANOVA with post hoc Bonferroni test). Data represented as mean relative current remaining at the end of the 200-ms voltage pulse that elicited maximal currents (± s.e.m., n = 5 per condition).

Extended Data Figure 3 Skate CaV pharmacology.

a, b, Pharmacology of skate CaV1.3 (sCav). Representative currents recorded in response to voltage pulses in the presence of vehicle (control, <0.1% DMSO) or 10 μM nifedipine or nimodipine. Currents were incompletely inhibited, similar to native electrosensory cell ICav (Fig. 1e). Dose–response relationships of current amplitudes measured at voltages that elicited maximal currents. Data are represented as mean ± s.e.m., n = 6 per treatment. c, d, Pharmacology of rat CaV1.3 (rCaV). Representative currents in the presence of vehicle or 10 μM nifedipine or nimodipine and associated dose–response relationships. n = 6 per treatment.

Extended Data Figure 4 Skate CaV gating current properties.

a–c, Gating current properties including peak amplitude (peak I), time-to-peak (TTP), exponential decay time constant (τ decay), and peak width at 50% of maximal gating current (width) for skate CaV1.3 (sCaV) versus rat CaV1.3 (rCaV, a), wild-type skate CaV1.3 (WT) versus charge-neutralized skate CaV1.3 (neutral, b), and rat CaV1.3 with charged skate motif (charged) versus rat CaV1.3 with neutralized skate motif (neutral, c). All values were similar except for peak I for sCaV versus rCaV, which is likely to represent increased expression of rCaV compared with sCaV. Data are presented as mean ± s.e.m., n listed above bars. d, Wild-type skate CaV1.3 (sCaV, blue, n = 7) and wild-type rat CaV (rCaV, red, n = 8) relative GV and QONV relationships. Data represented as mean ± s.e.m. e. GV and QONV relationships for wild-type sCaV1.3 (WT, blue) and charge-neutralized sCaV1.3 (neutral, red). Data represented as mean ± s.e.m., n = 7 per condition. f, GV and QONV relationships for rCaV1.3 with charged skate motif (charged, blue) and rCaV1.3 with neutral skate motif (neutral, red). Data represented as mean ± s.e.m., n = 8 per condition.

Extended Data Figure 5 Charged skate motif modulates voltage-dependent activation kinetics.

a, Activation kinetics were faster in charged-rCaV (blue, n = 6) than in wild-type rCaV1.3 (WT-rCaV, grey, n = 7) or neutral-rCaV (red, n = 8). Data represent mean ± s.e.m., P < 0.05 at all voltages for charged-rCaV versus WT-rCaV1.3 or neutral-rCaV, two-way ANOVA with post hoc Bonferroni test. b, Representative currents recorded in response to 1-s voltage pulses between −170 and −90 mV followed by a pulse to −10 mV for 20 ms. Cole–Moore effects, indicated by increased current activation rate at −90 mV (purple) versus −170 mV (green), were observed in currents recorded from charged-rCaV, but not neutral-rCaV. Scale bars, 50 pA, 10 ms. c, Cole–Moore effects quantified as the time to reach half-maximal current (t1/2). Charged-rCaV (blue, n = 9) reached maximal current amplitude faster with increasing prepulse voltage, whereas WT-rCaV (grey, n = 6) and neutral-rCaV (red, n = 8) were unchanged. All data represented as mean ± s.e.m., n ≥ 7, P < 0.05 for charged-rCaV t1/2 comparing −170 with −130, −110, or −90 mV, two-way ANOVA with post hoc Bonferroni test. d, Hypothetical model depicting the intracellular charged motif in the domain IV voltage sensor of sCaV1.3 destabilizing the inactive state of the channel, pushing it into a partially activated or primed state (gold oval) before full activation (green ovals). Because sCaV1.3 is primed for activation, channel activation requires a smaller increase in voltage compared with rCaV1.3.

Extended Data Figure 6 Skate BK properties.

a, Currents measured in response to 0, 1, or 10 μM intracellular Ca2+ at 80 mV from inside-out patches expressing sBK or mBK. Scale bars, 10 pA, 50 ms. Po for sBK compared with mBK was similar for all concentrations tested. Data represented as mean ± s.e.m., n = 5. b, Representative single-channel records at various voltages from patches expressing indicated BK channels. Scale bars, 25 pA, 20 ms. c, Representative currents recorded at 80 mV from patches expressing indicated BK channels. The same patch was exposed to local intracellular K+ concentrations of 140 mM, 640 mM, or 3.14 M. Dashed lines indicate single-channel current amplitude for sBK at 140 mM (green), 640 mM (orange), or 3.14 M (maroon). Scale bars, 50 pA, 20 ms.

Extended Data Figure 7 Adaptations in skate BK promote increased relative ICaV current during channel coupling.

a, Whole-cell currents in response to 200-ms voltage pulses from −80 mV to +80 mV from HEK293 cells expressing sBK, sBK-SE, or mBK in the presence of 0 or 20 μM intracellular Ca2+. Scale bars, 5 nA, 50 ms. b, Average IV relationships for sBK (blue), sBK-SE (green) and mBK (red) in the presence of 0 or 20 μM intracellular Ca2+. n = 7. c, Whole-cell currents from HEK293 cells expressing charged-rCaV1.3 coexpressed with sBK, sBK-SE, or mBK. Scale bars, 500 pA, 50 ms. t, transient current evoked by voltage pulse; s, sustained current. In the presence of CaV1.3, average transient and sustained IV relationships showed a negative shifted reversal potential (EREV) for sBK-SE (green) or mBK (red) compared with sBK (blue), indicating increased relative K+ permeability. d, Reversal potentials for transient and sustained currents evoked in cells coexpressing charged-rCaV1.3 and BK were affected by BK identity. Inset: transient currents mediated by coupling of CaV1.3 and BK (scale bars, 100 pA, 5 ms). Transient EREV: sBK = 32.96 ± 2.17, mBK = 8.43 ± 2.76, sBK-s.e. = 3.42 ± 2.38, P < 0.0001 for sBK versus mBK or sBK-SE. Sustained EREV: sBK = −17.00 ± 2.48, mBK = −50.95 ± 4.16, sBK-SE = −45.13 ± 4.59, P < 0.0001. n = 10. All data represented as mean ± s.e.m. and P values from two-tailed Student’s t-test.

Extended Data Figure 8 BK agonist NS11021 modulates skate BK channels.

a, In representative records from outside-out patches expressing sBK, the BK agonist NS11021 (NS, 10 μM) increased the Po and open-state dwell time of sBK channels and this effect was blocked by iberotoxin (IbTx, 100 nM). Scale bars, 5 pA, 100 ms. Associated all-points histograms demonstrate the increase in open time. Po: basal, 0.0024 ± 0.00068; NS, 0.16 ± 0.041; NS + IbTx, 0.00036 ± 0.00025. P < 0.0001 for NS versus basal or NS + IbTx. Open dwell time: basal, 0.62 ± 0.32; NS, 4.59 ± 0.34; NS + IbTx, 0.30 ± 0.010. P < 0.0001, n = 5. b, Whole-cell currents and average transient and sustained IV relationships from HEK293 cells expressing charged-rCaV1.3 and sBK (scale bars, 500 pA, 50 ms). Transient and sustained IV relationships made from normalizing currents in the presence of NS to basal currents show an increase in CaV1.3-activated sBK current amplitude and negative-shifted EREV in response to 10 μM NS. Transient EREV: basal = 20.71 ± 3.46, NS = −0.72 ± 0.94, P < 0.01. Sustained EREV: basal = −24.62 ± 0.61, NS = −47.21 ± 5.37, P < 0.05. n = 5. c, Representative currents recorded from an electrosensory cell show that 10 μM NS increases ICav-activated IK amplitude resulting in a decrease in relative ICav (scale bars, 100 pA, 50 ms). d, Transient and sustained IV relationships from normalizing currents in the presence of NS to basal currents. IV relationships demonstrate an NS-mediated negative shift in EREV, indicating increased K+ permeability. Transient EREV: basal = −6.15 ± 5.95, NS = −24.9 ± 8.23, P < 0.01. Sustained EREV: basal = −7.59 ± 6.02, NS = −26.65 ± 1.06, P < 0.05. n = 4. All data represented as mean ± s.e.m. and P values from two-tailed Student’s t-test.

Extended Data Figure 9 Ca2+-handling proteins are enriched in ampullae of Lorenzini.

a, Four highest expressed transcripts in ampullae. The Ca2+-binding protein parvalbumin 8 is the most highly expressed and is enriched in ampullae compared with other examined tissues. Bars represent fragments per kilobase of exon per million fragments mapped (FPKM). b, Four highest expressed ATPase transcripts in ampullae. Notably, the plasma membrane Ca2+ ATPase 1a is highly expressed and is enriched in ampullae. c, Proposed mechanism for electrosensory cell Vm oscillations. sCaV1.3 is activated by electrical signals to depolarize the cell and mediate Ca2+ influx. Ca2+ stimulates sBK-mediated K+ current to hyperpolarize the cell. Ca2+-binding proteins (CBP) bind incoming Ca2+ to inhibit BK-mediated hyperpolarization and continue sCaV1.3-driven oscillations.

Extended Data Figure 10 Behavioural paradigm for pharmacologically treated skates and startle response-related control.

a, Schematic drawing of electrical stimulus. A 9-V battery was used to generate a dipole DC stimulus through two independent leads placed into Tygon rubber tubing filled with seawater (left). The ends of these tubes were threaded through an acrylic plate to four different equally spaced locations on the base of the behavioural observation tank, which were then obscured by sand (right). b, Following 30 min of free exploration, control and pharmacologically treated skates were gently tapped upon the pectoral fin. The average distance moved during the startle response is represented as mean ± s.e.m.; n = 10. Differences were not significant according to a two-way ANOVA with post hoc Tukey’s test. c, Schematic drawing traced from typical example of skate startle response following pectoral fin stimulation (red arrow). The distance covered during the startle response was measured from the initial location (left) to the final location where the body axis became straight again (right), and the distance from the centre between the eyes from each respective position was recorded (dotted yellow line).

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Bellono, N., Leitch, D. & Julius, D. Molecular basis of ancestral vertebrate electroreception. Nature 543, 391–396 (2017). https://doi.org/10.1038/nature21401

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