Asymmetries in H+/K+-ATPase and cell membrane potentials comprise a very early step in left-right patterning

Cell

Volumn 111, Issue 1, 2002, Pages 77-89

  Levin, Michael ^a,b   Thorlin, Thorleif ^c,d   Robinson, Kenneth R ^d   Nogi, Taisaku ^b   Mercola, Mark ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b FORSYTH INSTITUTE   (United States)

^c SAHLGRENSKA UNIVERSITY HOSPITAL   (Sweden)

^d PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROGEN POTASSIUM ADENOSINE TRIPHOSPHATASE; MESSENGER RNA;

ANIMAL EXPERIMENT; ARTICLE; CELL DIVISION; CELL MEMBRANE POTENTIAL; CHICKEN; CONTROLLED STUDY; ELECTRIC POTENTIAL; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME SUBUNIT; FERTILIZATION; GENE EXPRESSION; NONHUMAN; PRIMITIVE STREAK; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RNA ANALYSIS; TIME; XENOPUS;

ANIMALIA; GALLUS GALLUS;

EID: 0037020041     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(02)00939-X     Document Type: Article

References (85)

1. Altizer A., Moriarty L., Bell S., Schreiner C., Scott W., Borgens R. Endogenous electric current is associated with normal development of the vertebrate limb. Dev. Dyn. 221:2001;391-401.
2. Bashirullah A., Halsell S.R., Cooperstock R.L., Kloc M., Karaiskakis A., Fisher W.W., Fu W., Hamilton J.K., Etkin L.D., Lipshitz H.D. Joint action of two RNA degradation pathways controls the timing of maternal transcript elimination at the midblastula transition in Drosophila melanogaster. EMBO J. 18:1999;2610-2620.
3. Beach D.L., Thibodeaux J., Maddox P., Yeh E., Bloom K. The role of the proteins Kar9 and Myo2 in orienting the mitotic spindle of budding yeast. Curr. Biol. 10:2000;1497-1506.
4. Boettger T., Wittler L., Kessel M. FGF8 functions in the specification of the right body side of the chick. Curr. Biol. 9:1999;277-280.
5. Borgens R., Shi R. Uncoupling histogenesis from morphogenesis in the vertebrate embryo by collapse of the transneural tube potential. Dev. Dyn. 203:1995;456-467.
6. Brauner T., Hulser D., Strasser R. Comparative measurements of membrane potentials with microelectrodes and voltage-sensitive dyes. Biochim. Biophys. Acta. 771:1984;208-216.
7. Brink P. Gap junction voltage dependence. a clear picture emerges J. Gen. Physiol. 116:2000;11-12.
8. Brown N., Wolpert L. The development of handedness in left/right asymmetry. Development. 109:1990;1-9.
9. Burdine R., Schier A. Conserved and divergent mechanisms in left-right axis formation. Genes Dev. 14:2000;763-776.
10. Capdevila J., Vogan K., Tabin C., Belmonte J.I. Mechanisms of left-right determination in vertebrates. Cell. 101:2000;9-21.
11. Casey B. Two rights make a wrong. human left-right malformations Hum. Mol. Genet. 7:1998;1565-1571.
12. Casey B., Hackett B.P. Left-right axis malformations in man and mouse. Curr. Opin. Genet. Dev. 10:2000;257-261.
13. Cooper M.S., Miller J.P., Fraser S.E. Electrophoretic repatterning of charged cytoplasmic molecules within tissues coupled by gap junctions by externally applied electric fields. Dev. Biol. 132:1989;179-188.
14. Croyle M.L., Woo A.L., Lingrel J.B. Extensive random mutagenesis analysis of the Na+/K+-ATPase alpha subunit identifies known and previously unidentified amino acid residues that alter ouabain sensitivity - implications for ouabain binding. Eur. J. Biochem. 248:1997;488-495.
15. Danos M., Yost H. Linkage of cardiac left-right asymmetry and dorsal-anterior development in Xenopus. Development. 121:1995;1467-1474.
16. Diehl-Jones W. Ionic basis of bioelectric currents during oogenesis in an insect. Dev. Biol. 158:1993;301-316.
17. Elinson R.P. Site of sperm entry and a cortical contraction associated with egg activation in the frog Rana pipiens. Dev. Biol. 47:1975;257-268.
18. Epps D., Wolfe M., Groppi V. Characterization of the steady-state and dynamic fluorescence properties of the potential-sensitive dye bis-(1,3-dibutylbarbituric acid)trimethine oxonol(Dibac4(3)) in model systems and cells. Chem. Phys. Lipids. 69:1994;137-150.
19. Fujita A., Horio Y., Higashi K., Mouri T., Hata F., Takeguchi N., Kurachi Y. Specific localization of an inwardly rectifying K+ channel, Kir4.1, at the apical membrane of rat gastric parietal cells; its possible involvement in K+ recycling for the H+-K+ pump. J. Physiol. 540:2002;85-92.
20. Gerhart J., Ubbels G., Black S., Hara K., Kirschner M. A reinvestigation of the role of the grey crescent in axis formation in Xenopus laevis. Nature. 292:1981;511-516.
21. Gottardi C.J., Caplan M.J. An ion-transporting ATPase encodes multiple apical localization signals. J. Cell Biol. 121:1993;283-293. a.
22. Gottardi C.J., Caplan M.J. Molecular requirements for the cell-surface expression of multisubunit ion-transporting ATPases. Identification of protein domains that participate in Na,K-ATPase and H,K-ATPase subunit assembly. J. Biol. Chem. 268:1993;14342-14347. b.
23. Hamburger V., Hamilton H. A series of normal stages in the development of the chick embryo. Dev. Dyn. 195:1992;231-272.
24. Harland R.M. In situ hybridization. an improved whole mount method for Xenopus embryos Kay B.K., Peng H.B. Xenopus laevis: Practical Uses in Cell and Molecular Biology. 1991;Academic Press, San Diego. 685-695.pp.
25. Harris C., Fliegel L. Amiloride and the Na(+)/H(+) exchanger protein. mechanism and significance of inhibition of the Na(+)/H(+) exchanger (review) Int. J. Mol. Med. 3:1999;315-321.
26. Hotary K., Robinson K. Evidence of a role for endogenous electric fields in chick embryo development. Development. 114:1992;985-996.
27. Hotary K.B., Robinson K.R. Endogenous electrical currents and voltage gradients in Xenopus embryos and the consequences of their disruption. Dev. Biol. 166:1994;789-800.
28. Hyatt B., Yost H. The left-right coordinator. the role of Vg1 in organizing left-right axis Cell. 93:1998;37-46.
29. Ikuma M., Binder H., Geibel J. Role of apical H-K exchange and basolateral K channel in the regulation of intracellular pH in rat distal colon crypt cells. J. Membr. Biol. 166:1998;205-212.
30. Jaffe L. The role of ionic currents in establishing developmental pattern. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 295:1981;553-566.
31. Jiang Y., MacKinnon R. The barium site in a potassium channel by x-ray crystallography. J. Gen. Physiol. 115:2000;269-272.
32. Lange C.S., Steele V.E. The mechanism of anterior-posterior polarity control in planarians. Differentiation. 11:1978;1-12.
33. Levin M. Left-right asymmetry and the chick embryo. Semin. Cell Dev. Biol. 9:1998;67-76.
34. Levin M., Mercola M. Gap junctions are involved in the early generation of left right asymmetry. Dev. Biol. 203:1998;90-105.
35. Levin M., Mercola M. Gap junction-mediated transfer of left-right patterning signals in the early chick blastoderm is upstream of Shh asymmetry in the node. Development. 126:1999;4703-4714.
36. Levin M., Johnson R., Stern C., Kuehn M., Tabin C. A molecular pathway determining left-right asymmetry in chick embryogenesis. Cell. 82:1995;803-814.
37. Linask K., Han M., Artman M., Ludwig C. Sodium-calcium exchanger (NCX-1) and calcium modulation. NCX protein expression patterns and regulation of early heart development Dev. Dyn. 221:2001;249-264.
38. Logan M., Pagan-Westphal S., Smith D., Paganessi L., Tabin C. The transcription factor Pitx2 mediates situs-specific morphogenesis in response to left-right asymmetric signals. Cell. 94:1998;307-317.
39. Lohr J., Danos M., Yost H. Left-right asymmetry of a nodal-related gene is regulated by dorsoanterior midline structures during Xenopus development. Development. 124:1997;1465-1472.
40. Marinos E. Observations on the mitochondrial distribution in normal, rotated and cold-treated 2-cell stage embryos of Xenopus laevis. Cell Differ. 18:1986;163-171.
41. Mathews P.M., Claeys D., Jaisser F., Geering K., Horisberger J.D., Kraehenbuhl J.P., Rossier B.C. Primary structure and functional expression of the mouse and frog alpha-subunit of the gastric H(+)-K(+)-ATPase. Am. J. Physiol. 268:1995;C1207-C1214.
42. Mathur S., Karmazyn M. Interaction between anesthetics and the sodium-hydrogen exchange inhibitor HOE 642 (cariporide) in ischemic and reperfused rat hearts. Anesthesiology. 87:1997;1460-1469.
43. Meneton P., Schultheis P.J., Greeb J., Nieman M.L., Liu L.H., Clarke L.L., Duffy J.J., Doetschman T., Lorenz J.N., Shull G.E. Increased sensitivity to K+ deprivation in colonic H,K-ATPase-deficient mice. J. Clin. Invest. 101:1998;536-542.
44. Meneton P., Lesage F., Barhanin J. Potassium ATPases, channels, and transporters. an overview Semin. Nephrol. 19:1999;438-457.
45. Mercola M., Levin M. Left-right asymmetry determination in vertebrates. Annu. Rev. Cell Dev. Biol. 17:2001;779-805.
46. Micklem D.R., Adams J., Grunert S., St Johnston D. Distinct roles of two conserved Staufen domains in oskar mRNA localization and translation. EMBO J. 19:2000;1366-1377.
47. Mizunashi K., Furukawa Y., Katano K., Abe K. Effect of omeprazole, an inhibitor of H+,K(+)-ATPase, on bone resorption in humans. Calcif. Tissue Int. 53:1993;21-25.
48. Morley G.E., Ek-Vitorin J.F., Taffet S.M., Delmar M. Structure of connexin43 and its regulation by pHi. J. Cardiovasc. Electrophysiol. 8:1997;939-951.
49. Munchow S., Sauter C., Jansen R.P. Association of the class V myosin Myo4p with a localised messenger RNA in budding yeast depends on She proteins. J. Cell Sci. 112:1999;1511-1518.
50. Munson K.B., Lambrecht N., Sachs G. Effects of mutations in M4 of the gastric H+,K+-ATPase on inhibition kinetics of SCH28080. Biochemistry. 39:2000;2997-3004.
51. Nieuwkoop, P.D., and Faber, J. (1967). Normal Table of Xenopus laevis (Daudin), Second Edition (Amsterdam: North-Holland Publishing Company).
52. Nonaka S., Tanaka Y., Okada Y., Takeda S., Harada A., Kanai Y., Kido M., Hirokawa N. Randomization of left-right asymmetry due to loss of nodal cilia generating leftward flow of extraembryonic fluid in mice lacking KIF3B motor protein. Cell. 95:1998;829-837.
53. Nonaka S., Shiratori H., Saijoh Y., Hamada H. Determination of left-right patterning of the mouse embryo by artificial nodal flow. Nature. 418:2002;96-99.
54. Ohuchi H., Kimura S., Watamoto M., Itoh N. Involvement of fibroblast growth factor (FGF)18-FGF8 signaling in specification of left-right asymmetry and brain and limb development of the chick embryo. Mech. Dev. 95:2000;55-66.
55. Pagan-Westphal S., Tabin C. The transfer of left-right positional information during chick embryogenesis. Cell. 93:1998;25-35.
56. Pennekamp P., Karcher C., Fischer A., Schweickert A., Skryabin B., Horst J., Blum M., Dworniczak B. The ion channel polycystin-2 is required for left-right axis determination in mice. Curr. Biol. 12:2002;938-943.
57. Pizzonia J.H., Ransom B.R., Pappas C.A. Characterization of Na+/H+ exchange activity in cultured rat hippocampal astrocytes. J. Neurosci. Res. 44:1996;191-198.
58. Psychoyos D., Stern C. Restoration of the organizer after radical ablation of Hensen's node and the anterior primitive streak in the chick embryo. Development. 122:1996;3263-3273.
59. Robinson K., Messerli M. Electric embryos. the embryonic epithelium as a generator of developmental information McCaig C. Nerve Growth and Guidance. 1996;Portland Press, Portland.
60. Rodriguez-Esteban C., Capdevila J., Kawakami Y., Izpisua Belmonte J.C. Wnt signaling and PKA control Nodal expression and left-right determination in the chick embryo. Dev. Suppl. 128:2001;3189-3195.
61. Rose S.M. Differentiation during regeneration caused by migration of repressors in bioelectric fields. Am. Zool. 10:1970;91-99.
62. Sachs G., Shin J.M., Briving C., Wallmark B., Hersey S. The pharmacology of the gastric acid pump. the H+,K+ ATPase Annu. Rev. Pharmacol. Toxicol. 35:1995;277-305.
63. Sanders S.W., Tolman K.G., Greski P.A., Jennings D.E., Hoyos P.A., Page J.G. The effects of lansoprazole, a new H+,K(+)-ATPase inhibitor, on gastric pH and serum gastrin. Aliment. Pharmacol. Ther. 6:1992;359-372.
64. Scharf S.R., Gerhart J.C. Determination of the dorsal-ventral axis in eggs of Xenopus laevis. complete rescue of uv-impaired eggs by oblique orientation before first cleavage Dev. Biol. 79:1980;181-198.
65. Schnorrer F., Bohmann K., Nusslein-Volhard C. The molecular motor dynein is involved in targeting swallow and bicoid RNA to the anterior pole of Drosophila oocytes. Nat. Cell Biol. 2:2000;185-190.
66. Shi R., Borgens R. Embryonic neuroepithelial sodium transport, the resulting physiological potential, and cranial development. Dev. Biol. 165:1994;105-116.
67. Shi R., Borgens R.B. Three-dimensional gradients of voltage during development of the nervous system as invisible coordinates for the establishment of embryonic pattern. Dev. Dyn. 202:1995;101-114.
68. Spemann H. Embryonic Development and Induction. 1938;Yale University Press, New Haven, CT.
69. Spicer Z., Miller M.L., Andringa A., Riddle T.M., Duffy J.J., Doetschman T., Shull G.E. Stomachs of mice lacking the gastric H,K-ATPase alpha-subunit have achlorhydria, abnormal parietal cells, and ciliated metaplasia. J. Biol. Chem. 275:2000;21555-21565.
70. Supp D., Witte D., Potter S., Brueckner M. Mutation of an axonemal dynein affects left-right asymmetry in inversus viscerum mice. Nature. 389:1997;963-966.
71. Supp D., Brueckner M., Kuehn M., Witte D., Lowe L., McGrath J., Cirrakes J., Potter S. Targeted deletion of the ATP binding domain of left-right dynein confirms its role in specifying development of left-right asymmetries. Development. 126:1999;5495-5504.
72. Takeda S., Yonekawa Y., Tanaka Y., Nonaka Y.O.S., Hirokawa N. Left-right asymmetry and kinesin superfamily protein KIF3A. J. Cell Biol. 145:1999;825-836.
73. Takeda S., Yamazaki H., Seog D., Kanai Y., Terada S., Hirokawa N. Kinesin superfamily protein 3 (KIF3) motor transports fodrin-associating vesicles important for neurite building. J. Cell Biol. 148:2000;1255-1265.
74. Takizawa P.A., Vale R.D. The myosin motor, Myo4p, binds Ash1 mRNA via the adapter protein, She3p. Proc. Natl. Acad. Sci. USA. 97:2000;5273-5278.
75. Turin L., Warner A.E. Intracellular pH in early Xenopus embryos. its effect on current flow between blastomeres J. Physiol. 300:1980;489-504.
76. Waddington C. The dependence of head curvature on the development of the heart in the chick embryo. J. Exp. Biol. 14:1937;229-231.
77. Weber J., Senior A.E. Effects of the inhibitors azide, dicyclohexylcarbodiimide, and aurovertin on nucleotide binding to the three F1-ATPase catalytic sites measured using specific tryptophan probes. J. Biol. Chem. 273:1998;33210-33215.
78. White T.W., Bruzzone R., Goodenough D.A., Paul D.L. Voltage gating of connexins. Nature. 371:1994;208-209.
79. Wilhelm J.E., Mansfield J., Hom-Booher N., Wang S., Turck C.W., Hazelrigg T., Vale R.D. Isolation of a ribonucleoprotein complex involved in mRNA localization in Drosophila oocytes. J. Cell Biol. 148:2000;427-440.
80. Woodruff R., Telfer W. Electrophoresis of proteins in intercellular bridges. Nature. 286:1980;84-86.
81. Woodruff R., Kulp J., LaGaccia E. Electrically mediated protein movement in Drosophila follicles. Roux's Archives of Dev. Biol. 197:1988;231-238.
82. Yost H.J. Establishment of left-right asymmetry. Int. Rev. Cytol. 203:2001;357-381.
83. Yu H., Ishii T., Pearson W.R., Takeyasu K. Primary structure of avian H+/K(+)-ATPase β-subunit. Biochim. Biophys. Acta. 1190:1994;189-192.
84. Yuan S., Schoenwolf G. De novo induction of the organizer and formation of the primitive streak in an experimental model of notochord reconstitution in avian embryos. Development. 125:1998;201-213.
85. Zhu L., Marvin M., Gardiner A., Lassar A., Mercola M., Stern C., Levin M. Cerberus regulates left-right asymmetry of the embryonic head and heart. Curr. Biol. 9:1999;931-938.