Transmembrane voltage potential controls embryonic eye patterning in Xenopus laevis

Development

Volumn 139, Issue 2, 2012, Pages 313-323

  Pai, Vaibhav P ^a   Aw, Sherry ^a,b   Shomrat, Tal ^a   Lemire, Joan M ^a   Levin, Michael ^a  

^a TUFTS UNIVERSITY   (United States)

^b INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

Author keywords

Bioelectricity; Eyes; Membrane potential; Xenopus

Indexed keywords

CALCIUM CHANNEL; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOENERGY; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; EYE DEVELOPMENT; MEMBRANE POTENTIAL; MORPHOGENESIS; MOUSE; NONHUMAN; ORGANOGENESIS; PRIORITY JOURNAL; XENOPUS LAEVIS;

ANIMALS; CALCIUM CHANNELS; COUMARINS; EMBRYONIC INDUCTION; ETHANOLAMINES; EYE; IN SITU HYBRIDIZATION; MEMBRANE POTENTIALS; MICROSCOPY, FLUORESCENCE; TRANSCRIPTION FACTORS; XENOPUS LAEVIS;

EID: 83755225284     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.073759     Document Type: Article

References (74)

1. Acampora, D., Mazan, S., Lallemand, Y., Avantaggiato, V., Maury, M., Simeone, A. and Brulet, P. (1995). Forebrain and midbrain regions are deleted in Otx2-/- mutants due to a defective anterior neuroectoderm specification during gastrulation. Development 121, 3279-3290.
2. Adams, D. S., Masi, A. and Levin, M. (2007). H+ pump-dependent changes in membrane voltage are an early mechanism necessary and sufficient to induce Xenopus tail regeneration. Development 134, 1323-1335.
3. Andreazzoli, M., Gestri, G., Angeloni, D., Menna, E. and Barsacchi, G. (1999). Role of Xrx1 in Xenopus eye and anterior brain development. Development 126, 2451-2460.
4. Aw, S., Koster, J. C., Pearson, W., Nichols, C. G., Shi, N. Q., Carneiro, K. and Levin, M. (2010). The ATP-sensitive K(+)-channel (K(ATP)) controls early leftright patterning in Xenopus and chick embryos. Dev. Biol. 346, 39-53.
5. Bailey, T. J., El-Hodiri, H., Zhang, L., Shah, R., Mathers, P. H. and Jamrich, M. (2004). Regulation of vertebrate eye development by Rx genes. Int. J. Dev. Biol. 48, 761-770.
6. Beane, W. S., Morokuma, J., Adams, D. S. and Levin, M. (2011). A chemical genetics approach reveals H,K-ATPase-mediated membrane voltage is required for planarian head regeneration. Chem. Biol. 18, 77-89.
7. Beg, A. A. and Jorgensen, E. M. (2003). EXP-1 is an excitatory GABA-gated cation channel. Nat. Neurosci. 6, 1145-1152.
8. Blackiston, D., Adams, D. S., Lemire, J. M., Lobikin, M. and Levin, M. (2011). Transmembrane potential of GlyCl-expressing instructor cells induces a neoplastic-like conversion of melanocytes via a serotonergic pathway. Dis. Model. Mech. 4, 67-85.
9. Bowes, J. B., Snyder, K. A., Segerdell, E., Jarabek, C. J., Azam, K., Zorn, A. M. and Vize, P. D. (2010). Xenbase: gene expression and improved integration. Nucleic Acids Res. 38, D607-D612.
10. Chen, C. S., Mrksich, M., Huang, S., Whitesides, G. M. and Ingber, D. E. (1998). Micropatterned surfaces for control of cell shape, position and function. Biotechnol. Prog. 14, 356-363.
11. Chow, R. L., Altmann, C. R., Lang, R. A. and Hemmati-Brivanlou, A. (1999). Pax6 induces ectopic eyes in a vertebrate. Development 126, 4213-4222.
12. Davies, D. L., Trudell, J. R., Mihic, S. J., Crawford, D. K. and Alkana, R. L. (2003). Ethanol potentiation of glycine receptors expressed in Xenopus oocytes antagonized by increased atmospheric pressure. Alcohol Clin. Exp. Res. 27, 743-755.
13. Dike, L. E., Chen, C. S., Mrksich, M., Tien, J., Whitesides, G. M. and Ingber, D. E. (1999). Geometric control of switching between growth, apoptosis, and differentiation during angiogenesis using micropatterned substrates. In Vitro Cell. Dev. Biol. Anim. 35, 441-448.
14. Erclik, T., Hartenstein, V., McInnes, R. R. and Lipshitz, H. D. (2009). Eye evolution at high resolution: the neuron as a unit of homology. Dev. Biol. 332, 70-79.
15. Ericson, J., Thor, S., Edlund, T., Jessell, T. M. and Yamada, T. (1992). Early stages of motor neuron differentiation revealed by expression of homeobox gene Islet-1. Science 256, 1555-1560.
16. Faber, J. and Nieuwkoop, P. D. (1967). Normal Table of Xenopus Laevis (Daudin); a Systematical and Chronological Survey of the Development from Fertilized Egg Till the End of Metamorphosis. Amsterdam: North Holland.
17. + channels from subunits of different subfamilies: Kir2.1 (IRK1) and Kir4.1 (BIR10). Pflugers Arch. 433, 77-83.
18. Ficker, E., Dennis, A. T., Obejero-Paz, C. A., Castaldo, P., Taglialatela, M. and Brown, A. M. (2000). Retention in the endoplasmic reticulum as a mechanism of dominant-negative current suppression in human long QT syndrome. J. Mol. Cell. Cardiol. 32, 2327-2337.
19. Fukumoto, T., Kema, I. P. and Levin, M. (2005). Serotonin signaling is a very early step in patterning of the left-right axis in chick and frog embryos. Curr. Biol. 15, 794-803.
20. Gargini, C., Terzibasi, E., Mazzoni, F. and Strettoi, E. (2007). Retinal Organization in the retinal degeneration 10 (rd10) mutant mouse: a morphological and ERG study. J. Comp. Neurol. 500, 222-238.
21. Gehring, W. J. and Ikeo, K. (1999). Pax6, mastering eye morphogenesis and eye evolution. Trends Genet. 15, 371-377.
22. Gillespie, J. I. (1983). The distribution of small ions during the early development of Xenopus laevis and Ambystoma mexicanum embryos. J. Physiol. 344, 359-377.
23. Gruler, H. and Nuccitelli, R. (1991). Neural crest cell galvanotaxis: new data and a novel approach to the analysis of both galvanotaxis and chemotaxis. Cell Motil. Cytoskeleton 19, 121-133.
24. Harland, R. M. (1991). In situ hybridization: an improved whole-mount method for Xenopus embryos. Methods Cell Biol. 36, 685-695.
25. Harris, W. A. and Messersmith, S. L. (1992). Two cellular inductions involved in photoreceptor determination in the Xenopus retina. Neuron 9, 357-372.
26. + channels at tyrosine 242. Development 135, 859-867.
27. Hirsch, N. and Harris, W. A. (1997). Xenopus Pax-6 and retinal development. J. Neurobiol. 32, 45-61.
28. Hough, E., Beech, D. J. and Sivaprasadarao, A. (2000). Identification of molecular regions responsible for the membrane trafficking of Kir6.2. Pflugers Arch. 440, 481-487.
29. Huang, S. and Ingber, D. E. (2006). A non-genetic basis for cancer progression and metastasis: self-organizing attractors in cell regulatory networks. Breast Dis. 26, 27-54.
30. Ingber, D. E. (2006). Mechanical control of tissue morphogenesis during embryological development. Int. J. Dev. Biol. 50, 255-266.
31. + overload, major and reversible contributors to weakness by ion channel leaks. Proc. Natl. Acad. Sci. USA 106, 4036-4041.
32. Konig, S., Hinard, V., Arnaudeau, S., Holzer, N., Potter, G., Bader, C. R. and Bernheim, L. (2004). Membrane hyperpolarization triggers myogenin and myocyte enhancer factor-2 expression during human myoblast differentiation. J. Biol. Chem. 279, 28187-28196.
33. Konig, S., Beguet, A., Bader, C. R. and Bernheim, L. (2006). The calcineurin pathway links hyperpolarization (Kir2.1)-induced Ca2+ signals to human myoblast differentiation and fusion. Development 133, 3107-3114.
34. Kurtz, I. and Schrank, A. R. (1955). Bioelectric properties of intact and regenerating earthworms Eisenia foetida. Physiol. Zool. 28, 322-330.
35. Levin, M. (2006). Is the early left-right axis like a plant, a kidney, or a neuron? The Integration of physiological signals in embryonic asymmetry. Birth Defects Res. C Embryo Today 78, 191-223.
36. Levin, M. (2007). Large-scale biophysics: ion flows and regeneration. Trends Cell Biol. 17, 261-270.
37. Levin, M. (2009). Bioelectric mechanisms in regeneration: unique aspects and future perspectives. Semin. Cell Dev. Biol. 20, 543-556.
38. +-ATPase and cell membrane potentials comprise a very early step in left-right patterning. Cell 111, 77-89.
39. Lupo, G., Harris, W. A., Barsacchi, G. and Vignali, R. (2002). Induction and patterning of the telencephalon in Xenopus laevis. Development 129, 5421-5436.
40. Marsh, G. and Beams, H. W. (1947). Orientation of growth direction of the onion root in a transverse electric field. Anat. Rec. 99, 623.
41. McCaig, C. D., Song, B. and Rajnicek, A. M. (2009). Electrical dimensions in cell science. J. Cell Sci. 122, 4267-4276.
42. McDonald, T. F., Sachs, H. G., Orr, C. W. and Ebert, J. D. (1972). External potassium and baby hamster kidney cells: intracellular ions, ATP, growth, DNA synthesis and membrane potential. Dev. Biol. 28, 290-303.
43. Moody, S. A. (1987). Fates of the blastomeres of the 32-cell-stage Xenopus embryo. Dev. Biol. 122, 300-319.
44. Morokuma, J., Blackiston, D., Adams, D. S., Seebohm, G., Trimmer, B. and Levin, M. (2008). Modulation of potassium channel function confers a hyperproliferative invasive phenotype on embryonic stem cells. Proc. Natl. Acad. Sci. USA 105, 16608-16613.
45. Nakanishi, S. and Okazawa, M. (2006). Membrane potential-regulated Ca2+ signalling in development and maturation of mammalian cerebellar granule cells. J. Physiol. 575, 389-395.
46. Nichols, C. G. (2006). KATP channels as molecular sensors of cellular metabolism. Nature 440, 470-476.
47. Nishiyama, M., von Schimmelmann, M. J., Togashi, K., Findley, W. M. and Hong, K. (2008). Membrane potential shifts caused by diffusible guidance signals direct growth-cone turning. Nat. Neurosci. 11, 762-771.
48. Onkal, R., Mattis, J. H., Fraser, S. P., Diss, J. K., Shao, D., Okuse, K. and Djamgoz, M. B. (2008). Alternative splicing of Nav1.5: an electrophysiological comparison of 'neonatal' and 'adult' isoforms and critical involvement of a lysine residue. J. Cell. Physiol. 216, 716-726.
49. Pahuja, S. L., Mullins, B. T. and Reid, T. W. (1985). Bovine retinal glutamine synthetase 1. Purification, characterization and immunological properties. Exp. Eye Res. 40, 61-74.
50. Pannese, M., Polo, C., Andreazzoli, M., Vignali, R., Kablar, B., Barsacchi, G. and Boncinelli, E. (1995). The Xenopus homologue of Otx2 is a maternal homeobox gene that demarcates and specifies anterior body regions. Development 121, 707-720.
51. Prevarskaya, N., Skryma, R. and Shuba, Y. (2010). Ion channels and the hallmarks of cancer. Trends Mol. Med. 16, 107-121.
52. Reid, B., Song, B., McCaig, C. D. and Zhao, M. (2005). Wound healing in rat cornea: the role of electric currents. FASEB J. 19, 379-386.
53. +-driven anion exchanger (NDAE1). A new bicarbonate transporter. J. Biol. Chem. 275, 24552-24559.
54. + channel with an ABC transporter. Neuron 26, 155-167.
55. Secchi, A. G., Segato, T. and Mancini, B. (1976). Release of protein and cations from the lens in the presence of different antigen-antibody interactions. Mod. Probl. Ophthalmol. 16, 80-94.
56. Shan, Q., Haddrill, J. L. and Lynch, J. W. (2001). Ivermectin, an unconventional agonist of the glycine receptor chloride channel. J. Biol. Chem. 276, 12556-12564.
57. Shi, R. and Borgens, R. B. (1995). Three-dimensional gradients of voltage during development of the nervous system as invisible coordinates for the establishment of embryonic pattern. Dev. Dyn. 202, 101-114.
58. Sive, H., Grainger, R. M. and Harland, R.,. (2000). Early Development of Xenopus Laevis: A Laboratory Manual. New York: Cold Spring Harbor Laboratory Press.
59. Strutz-Seebohm, N., Gutcher, I., Decher, N., Steinmeyer, K., Lang, F. and Seebohm, G. (2007). Comparison of potent Kv1.5 potassium channel inhibitors reveals the molecular basis for blocking kinetics and binding mode. Cell. Physiol. Biochem. 20, 791-800.
60. Sundelacruz, S., Levin, M. and Kaplan, D. L. (2009). Role of membrane potential in the regulation of cell proliferation and differentiation. Stem Cell Rev. 5, 231-246.
61. Tseng, A. S., Beane, W. S., Lemire, J. M., Masi, A. and Levin, M. (2010). Induction of vertebrate regeneration by a transient sodium current. J. Neurosci. 30, 13192-13200.
62. Vandenberg, L. N., Morrie, R. D. and Adams, D. S. (2011). V-ATPasedependent ectodermal voltage and Ph regionalization are required for craniofacial morphogenesis. Dev. Dyn. 240, 1889-1904.
63. Viczian, A. S., Solessio, E. C., Lyou, Y. and Zuber, M. E. (2009). Generation of functional eyes from pluripotent cells. PLoS Biol. 7, e1000174.
64. Wacker, S. A., Oswald, F., Wiedenmann, J. and Knochel, W. (2007). A green to red photoconvertible protein as an analyzing tool for early vertebrate development. Dev. Dyn. 236, 473-480.
65. Wang, E., Reid, B., Lois, N., Forrester, J. V., McCaig, C. D. and Zhao, M. (2005). Electrical inhibition of lens epithelial cell proliferation: an additional factor in secondary cataract? FASEB J. 19, 842-844.
66. Wang, Z., Tristani-Firouzi, M., Xu, Q., Lin, M., Keating, M. T. and Sanguinetti, M. C. (1999). Functional effects of mutations in KvLQT1 that cause long QT syndrome. J. Cardiovasc. Electrophysiol. 10, 817-826.
67. Wolff, C., Fuks, B. and Chatelain, P. (2003). Comparative study of membrane potential-sensitive fluorescent probes and their use in ion channel screening assays. J. Biomol. Screen. 8, 533-543.
68. Woodruff, R. I. and Telfer, W. H. (1980). Electrophoresis of proteins in intercellular bridges. Nature 286, 84-86.
69. Yao, L., Shanley, L., McCaig, C. and Zhao, M. (2008). Small applied electric fields guide migration of hippocampal neurons. J. Cell. Physiol. 216, 527-535.
70. Yasuda, T. and Adams, D. J. (2010). Physiological roles of ion channels in adult neural stem cells and their progeny. J. Neurochem. 114, 946-959.
71. Zaghloul, N. A., Yan, B. and Moody, S. A. (2005). Step-wise specification of retinal stem cells during normal embryogenesis. Biol. Cell 97, 321-337.
72. Zhao, M., Song, B., Pu, J., Wada, T., Reid, B., Tai, G., Wang, F., Guo, A., Walczysko, P., Gu, Y. et al. (2006). Electrical signals control wound healing through phosphatidylinositol-3-OH kinase-gamma and PTEN. Nature 442, 457-460.
73. Zuber, M. E. (2010). Eye field specification in Xenopus Laevis. Curr. Top. Dev. Biol. 93, 29-60.
74. Zuber, M. E., Gestri, G., Viczian, A. S., Barsacchi, G. and Harris, W. A. (2003). Specification of the vertebrate eye by a network of eye field transcription factors. Development 130, 5155-5167.