A non-inactivating high-voltage-activated two-pore Na+ channel that supports ultra-long action potentials and membrane bistability

Nature Communications

Volumn 5, Issue , 2014, Pages

  Cang, Chunlei ^a   Aranda, Kimberly ^a   Ren, Dejian ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VOLTAGE GATED SODIUM CHANNEL; TPC3 PROTEIN, XENOPUS; TPC3 PROTEIN, ZEBRAFISH; XENOPUS PROTEIN; ZEBRAFISH PROTEIN;

AMPHIBIAN; EGG; EUKARYOTE; ION EXCHANGE; MEMBRANE; NEUROLOGY; PROTEIN; SIGNALING; SPERM;

ACTION POTENTIAL; ARTICLE; DEPOLARIZATION; ELECTRIC POTENTIAL; ENDOSOME; LYSOSOME; MEMBRANE DEPOLARIZATION; MEMBRANE POTENTIAL; NONHUMAN; OOCYTE; PROTEIN FAMILY; SPERM; XENOPUS LAEVIS; ZEBRA FISH; AMINO ACID SEQUENCE; ANIMAL; CELL MEMBRANE; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR GENETICS; NERVE CELL; SEQUENCE ALIGNMENT;

AMPHIBIA; ANIMALIA; EUKARYOTA;

ACTION POTENTIALS; AMINO ACID SEQUENCE; ANIMALS; CELL MEMBRANE; MOLECULAR SEQUENCE DATA; NEURONS; SEQUENCE ALIGNMENT; VOLTAGE-GATED SODIUM CHANNELS; XENOPUS LAEVIS; XENOPUS PROTEINS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84920890446     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6015     Document Type: Article

References (57)

1. Alle, H., Roth, A. & Geiger, J. R. Energy-efficient action potentials in hippocampal mossy fibers. Science 325, 1405-1408 (2009).
2. Hodgkin, A. L. & Huxley, A. F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. 117, 500-544 (1952).
3. Hille, B. Ion Channels of Excitable Membranes edn 3 edn (Sinauer Associates, 2001).
4. Catterall, W. A. Voltage-gated sodium channels at 60: structure, function and pathophysiology. J. Physiol. 590, 2577-2589 (2012).
5. Jan, Y. N. & Jan, L. Y. Voltage-gated potassium channels and the diversity of electrical signaling. J. Physiol. 590, 2592-2599 (2012).
6. Tasaki, I. & Kamiya, N. A study on electrophysiological properties of carnivorous amoebae. J. Cell. Physiol. 63, 365-380 (1964).
7. Tasaki, I. & Kamiya, N. Electrical response of a slime mold to mechanical and electrical stimuli. Protoplasma 39, 333-343 (1950).
8. Findlay, G. & Hope, A. B. Ionic relations of cells of Chara Australis VII. The seprate electrical characteristics of the plasmalemma and tonoplast. Aust. J. Biol. Sci. 17, 62-77 (1964).
9. Favre, P. & Agosti, R. D. Voltage-dependent action potentials in Arabidopsis thaliana. Physiol. Plant. 131, 263-272 (2007).
10. Fromm, J. & Lautner, S. Electrical signals and their physiological significance in plants. Plant Cell Environ. 30, 249-257 (2007).
11. Jaffe, L. A., Kado, R. T. & Kline, D. A calcium-activated sodium conductance produces a long-duration action potential in the egg of a nemertean worm. J. Physiol. 381, 263-278 (1986).
12. Kline, D., Jaffe, L. A. & Kado, R. T. A calcium-activated sodium conductance contributes to the fertilization potential in the egg of the nemertean worm Cerebratulus lacteus. Dev. Biol. 117, 184-193 (1986).
13. Miyazaki, S., Takahashi, K. & Tsuda, K. Calcium and sodium contributions to regenerative responses in the embryonic excitable cell membrane. Science 176, 1441-1443 (1972).
14. Baud, C., Kado, R. T. & Marcher, K. Sodium channels induced by depolarization of the Xenopus laevis oocyte. Proc. Natl Acad. Sci. USA 79, 3188-3192 (1982).
15. Schlichter, L. C. Ionic currents underlying the action potential of Rana pipiens oocytes. Dev. Biol. 134, 59-71 (1989).
16. Jaffe, L. A. & Cross, N. L. Electrical regulation of sperm-egg fusion. Annu. Rev. Physiol. 48, 191-200 (1986).
17. Jaffe, L. A. & Schlichter, L. C. Fertilization-induced ionic conductances in eggs of the frog, Rana pipiens. J. Physiol. 358, 299-319 (1985).
18. Duran, C., Thompson, C. H., Xiao, Q. & Hartzell, H. C. Chloride channels: often enigmatic, rarely predictable. Annu. Rev. Physiol. 72, 95-121 (2010).
19. Ren, D. et al. A prokaryotic voltage-gated sodium channel. Science 294, 2372-2375 (2001).
20. Noda, M. et al. Primary structure of Electrophorus electricus sodium channel deduced from cDNA sequence. Nature 312, 121-126 (1984).
21. Catterall, W. A. From ionic currents to molecular mechanisms: the structure and function of voltage-gated sodium channels. Neuron 26, 13-25 (2000).
22. Zhu, M. X., Ma, J., Parrington, J., Galione, A. & Evans, A. M. TPCs: Endolysosomal channels for Ca2+ mobilization from acidic organelles triggered by NAADP. FEBS Lett. 584, 1966-1974 (2010).
23. Galione, A. NAADP receptors. Cold Spring Harb. Perspect. Biol. 3, a004036 (2011).
24. Calcraft, P. J. et al. NAADP mobilizes calcium from acidic organelles through two-pore channels. Nature 459, 596-600 (2009).
25. Cang, C. et al. mTOR regulates lysosomal ATP-sensitive two-pore Na+ channels to adapt to metabolic state. Cell 152, 778-790 (2013).
26. Cang, C., Bekele, B. & Ren, D. The voltage-gated sodium channel TPC1 confers endolysosomal excitability. Nat. Chem. Biol. 10, 463-469 (2014).
27. Wang, X. et al. TPC proteins are phosphoinositide-activated sodium-selective ion channels in endosomes and lysosomes. Cell 151, 372-383 (2012).
28. Jha, A., Ahuja, M., Patel, S., Brailoiu, E. & Muallem, S. Convergent regulation of the lysosomal two-pore channel-2 by Mg2+, NAADP, PI(3,5)P2 and multiple protein kinases. EMBO J. 33, 501-511 (2014).
29. Schieder, M., Rotzer, K., Bruggemann, A., Biel, M. & Wahl-Schott, C. A. Characterization of two-pore channel 2 (TPCN2)-mediated Ca2+ currents in isolated lysosomes. J. Biol. Chem. 285, 21219-21222 (2010).
30. Pitt, S. J. et al. TPC2 is a novel NAADP-sensitive Ca2+ release channel, operating as a dual sensor of luminal pH and Ca2+. J. Biol. Chem. 285, 35039-35046 (2010).
31. Brailoiu, E. et al. An NAADP-gated two-pore channel targeted to the plasma membrane uncouples triggering from amplifying Ca2+ signals. J. Biol. Chem. 285, 38511-38516 (2010).
32. Cai, X. & Patel, S. Degeneration of an intracellular ion channel in the primate lineage by relaxation of selective constraints. Mol. Biol. Evol. 27, 2352-2359 (2010).
33. Zhu, M. X. et al. Calcium signaling via two-pore channels: local or global, that is the question. Am. J. Physiol. Cell Physiol. 298, C430-C441 (2010).
34. Raman, I. M., Sprunger, L. K., Meisler, M. H. & Bean, B. P. Altered subthreshold sodium currents and disrupted firing patterns in Purkinje neurons of Scn8a mutant mice. Neuron 19, 881-891 (1997).
35. Zhang, Z., Okawa, H., Wang, Y. & Liman, E. R. Phosphatidylinositol 4,5-bisphosphate rescues TRPM4 channels from desensitization. J. Biol. Chem. 280, 39185-39192 (2005).
36. Nilius, B. et al. The Ca2+-activated cation channel TRPM4 is regulated by phosphatidylinositol 4,5-biphosphate. EMBO J. 25, 467-478 (2006).
37. Dong, X. P. et al. PI(3,5)P2 controls membrane trafficking by direct activation of mucolipin Ca2+ release channels in the endolysosome. Nat. Commun. 1, 38 (2010).
38. Zhang, X., Li, X. & Xu, H. Phosphoinositide isoforms determine compartmentspecific ion channel activity. Proc. Natl Acad. Sci. USA 109, 11384-11389 (2012).
39. Hilgemann, D. W., Feng, S. & Nasuhoglu, C. The complex and intriguing lives of PIP2 with ion channels and transporters. Sci. STKE 2001, re19 (2001).
40. Suh, B. C. & Hille, B. PIP2 is a necessary cofactor for ion channel function: how and why? Annu. Rev. Biophys. 37, 175-195 (2008).
41. Catterall, W. A., Raman, I. M., Robinson, H. P., Sejnowski, T. J. & Paulsen, O. The Hodgkin-Huxley heritage: from channels to circuits. J. Neurosci. 32, 14064-14073 (2012).
42. Ren, D. Sodium leak channels in neuronal excitability and rhythmic behaviors. Neuron 72, 899-911 (2011).
43. Hagiwara, S. & Jaffe, L. A. Electrical properties of egg cell membranes. Annu. Rev. Biophys. Bioeng. 8, 385-416 (1979).
44. Jaffe, L. A., Gould-Somero, M. & Holland, L. Ionic mechanism of the fertilization potential of the marine worm, Urechis caupo (Echiura). J. Gen. Physiol. 73, 469-492 (1979).
45. Schoenenberger, P., Gerosa, D. & Oertner, T. G. Temporal control of immediate early gene induction by light. PLoS ONE 4, e8185 (2009).
46. Berndt, A., Yizhar, O., Gunaydin, L. A., Hegemann, P. & Deisseroth, K. Bi-stable neural state switches. Nat. Neurosci. 12, 229-234 (2009).
47. Steinhardt, R. A., Lundin, L. & Mazia, D. Bioelectric responses of the echinoderm egg to fertilization. Proc. Natl Acad. Sci. USA 68, 2426-2430 (1971).
48. DeFelice, L. J. & Dale, B. Voltage response to fertilization and polyspermy in sea urchin eggs and oocytes. Dev. Biol. 72, 327-341 (1979).
49. Schlichter, L. C. A role for action potentials in maturing Rana pipiens oocytes. Dev. Biol. 98, 60-69 (1983).
50. Schlichter, L. C. Spontaneous action potentials produced by Na and Cl channels in maturing Rana pipiens oocytes. Dev. Biol. 98, 47-59 (1983).
51. Beane, W. S., Morokuma, J., Lemire, J. M. & Levin, M. Bioelectric signaling regulates head and organ size during planarian regeneration. Development 140, 313-322 (2013).
52. Murnane, J. M. & DeFelice, L. J. Electrical maturation of the murine oocyte: an increase in calcium current coincides with acquisition of meiotic competence. Zygote 1, 49-60 (1993).
53. Georgiou, P., Bountra, C., Bland, K. P. & House, C. R. Calcium-evoked opening of potassium channels in hamster eggs. Q. J. Exp. Physiol. 68, 687-700 (1983).
54. Okamoto, H., Takahashi, K. & Yamashita, N. Ionic currents through the membrane of the mammalian oocyte and their comparison with those in the tunicate and sea urchin. J. Physiol. 267, 465-495 (1977).
55. Lu, B. et al. The neuronal NALCN channel contributes resting sodium permeability and is required for normal respiratory rhythm. Cell 129, 371-383 (2007).
56. Leonard, J. P., Nargeot, J., Snutch, T. P., Davidson, N. & Lester, H. A. Ca channels induced in Xenopus oocytes by rat brain mRNA. J. Neurosci. 7, 875-881 (1987).
57. Liman, E. R., Tytgat, J. & Hess, P. Subunit stoichiometry of a mammalian K+ channel determined by construction of multimeric cDNAs. Neuron 9, 861-871 (1992).