The ATP-sensitive K+-channel (KATP) controls early left-right patterning in Xenopus and chick embryos

Developmental Biology

Volumn 346, Issue 1, 2010, Pages 39-53

  Aw, Sherry ^a,b   Koster, Joseph C ^c   Pearson, Wade ^c   Nichols, Colin G ^c   Shi, Nian Qing ^d   Carneiro, Katia ^a   Levin, Michael ^a  

^a TUFTS UNIVERSITY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

KATP channels; Kir6.1; Left right asymmetry; Tight junctions; Xenopus

Indexed keywords

ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR6.1; PROTEIN NODAL; SONIC HEDGEHOG PROTEIN; INWARDLY RECTIFYING POTASSIUM CHANNEL; POTASSIUM; UK-ATP-1 POTASSIUM CHANNEL;

ANIMAL CELL; ARTICLE; BASEMENT MEMBRANE; BLASTULA; CELL JUNCTION; CHICK; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO; EMBRYO PATTERN FORMATION; HEMISPHERIC DOMINANCE; IMMUNOFLUORESCENCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; TIGHT JUNCTION; XENOPUS LAEVIS; ANIMAL; BLASTOMA; CHICK EMBRYO; EMBRYOLOGY; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MORPHOGENESIS; PHYSIOLOGY;

ERINACEIDAE; XENOPUS LAEVIS;

ANIMALS; BLASTOMERES; BODY PATTERNING; CHICK EMBRYO; KATP CHANNELS; POTASSIUM; POTASSIUM CHANNELS, INWARDLY RECTIFYING; TIGHT JUNCTIONS; XENOPUS LAEVIS;

EID: 77956405385     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2010.07.011     Document Type: Article

References (154)

1. Adams D.S., Levin M. Inverse drug screens: a rapid and inexpensive method for implicating molecular targets. Genesis 2006, 44:530-540.
2. Adams D.S., Levin M. Strategies and techniques for investigation of biophysical signals in patterning. Analysis of Growth Factor Signaling in Embryos 2006, 177-262. Taylor and Francis Books. M. Whitman, A.K. Sater (Eds.).
3. Adams D.S., Robinson K.R., Fukumoto T., Yuan S., Albertson R.C., Yelick P., Kuo L., McSweeney M., Levin M. Early, H+-V-ATPase-dependent proton flux is necessary for consistent left-right patterning of non-mammalian vertebrates. Development 2006, 133:1657-1671.
4. Adams D.S., Robinson K.R., Fukumoto T., Yuan S., Albertson R.C., Yelick P., Kuo L., McSweeney M., Levin M. Early, H+-V-ATPase-dependent proton flux is necessary for consistent left-right patterning of non-mammalian vertebrates. Development 2006, 133:1657-1671.
5. Albrieux M., Villaz M. Bilateral asymmetry of the inositol trisphosphate-mediated calcium signaling in two-cell ascidian embryos. Biol. Cell 2000, 92:277-284.
6. Ashcroft F.M., Harrison D.E., Ashcroft S.J. Glucose induces closure of single potassium channels in isolated rat pancreatic beta-cells. Nature 1984, 312:446-448.
7. Ashford M.L., Sturgess N.C., Trout N.J., Gardner N.J., Hales C.N. Adenosine-5'-triphosphate-sensitive ion channels in neonatal rat cultured central neurones. Pflugers Arch. 1988, 412:297-304.
8. Aw S., Adams D.S., Qiu D., Levin M. H, K-ATPase protein localization and Kir4.1 function reveal concordance of three axes during early determination of left-right asymmetry. Mech. Dev. 2008, 125:353-372.
9. Aw S., Adams D.S., Qiu D., Levin M. H, K-ATPase protein localization and Kir4.1 function reveal concordance of three axes during early determination of left-right asymmetry. Mech. Dev. 2008, 125:353-372.
10. Aw S., Levin M. What's left in asymmetry?. Dev. Dyn. 2008, 237:3453-3463.
11. Aw S., Levin M. Is left-right asymmetry a form of planar cell polarity?. Development 2009, 136:355-366.
12. Bannister J.P., Young B.A., Sivaprasadarao A., Wray D. Conserved extracellular cysteine residues in the inwardly rectifying potassium channel Kir2.3 are required for function but not expression in the membrane. FEBS Lett. 1999, 458:393-399.
13. Basu B., Brueckner M. Cilia: multifunctional organelles at the center of vertebrate left-right asymmetry. Curr. Top. Dev. Biol. 2008, 85:151-174.
14. Beny J.L., Schaad O. An evaluation of potassium ions as endothelium-derived hyperpolarizing factor in porcine coronary arteries. Br. J. Pharmacol. 2000, 131:965-973.
15. Bienengraeber M., Olson T.M., Selivanov V.A., Kathmann E.C., O'Cochlain F., Gao F., Karger A.B., Ballew J.D., Hodgson D.M., Zingman L.V., Pang Y.P., Alekseev A.E., Terzic A. ABCC9 mutations identified in human dilated cardiomyopathy disrupt catalytic KATP channel gating. Nat. Genet. 2004, 36:382-387.
16. Boorman C.J., Shimeld S.M. The evolution of left-right asymmetry in chordates. Bioessays 2002, 24:1004-1011.
17. Brizuela B.J., Wessely O., De Robertis E.M. Overexpression of the Xenopus tight-junction protein claudin causes randomization of the left-right body axis. Dev. Biol. 2001, 230:217-229.
18. Brown N.A., Wolpert L. The development of handedness in left/right asymmetry. Development 1990, 109:1-9.
19. Burdine R., Schier A. Conserved and divergent mechanisms in left-right axis formation. Genes Dev. 2000, 14:763-776.
20. Bussemaker E., Wallner C., Fisslthaler B., Fleming I. The Na-K-ATPase is a target for an EDHF displaying characteristics similar to potassium ions in the porcine renal interlobar artery. Br. J. Pharmacol. 2002, 137:647-654.
21. Campbell A.M., Kessler P.D., Fambrough D.M. The alternative carboxyl termini of avian cardiac and brain sarcoplasmic reticulum/endoplasmic reticulum Ca(2+)-ATPases are on opposite sides of the membrane. J. Biol. Chem. 1992, 267:9321-9325.
22. Chuang C.F., Vanhoven M.K., Fetter R.D., Verselis V.K., Bargmann C.I. An innexin-dependent cell network establishes left-right neuronal asymmetry in C. elegans. Cell 2007, 129:787-799.
23. Chutkow W.A., Pu J., Wheeler M.T., Wada T., Makielski J.C., Burant C.F., McNally E.M. Episodic coronary artery vasospasm and hypertension develop in the absence of Sur2 K(ATP) channels. J. Clin. Invest. 2002, 110:203-208.
24. D'Hahan N., Moreau C., Prost A.L., Jacquet H., Alekseev A.E., Terzic A., Vivaudou M. Pharmacological plasticity of cardiac ATP-sensitive potassium channels toward diazoxide revealed by ADP. Proceedings of the National Academy of Sciences of the United States of America. 1999, 96:12162-12167.
25. Dabrowski M., Wahl P., Holmes W.E., Ashcroft F.M. Effect of repaglinide on cloned beta cell, cardiac and smooth muscle types of ATP-sensitive potassium channels. Diabetologia 2001, 44:747-756.
26. Danilchik M.V., Brown E.E., Riegert K. Intrinsic chiral properties of the Xenopus egg cortex: an early indicator of left-right asymmetry?. Development 2006, 133:4517-4526.
27. Danos M.C., Yost H.J. Role of notochord in specification of cardiac left-right orientation in zebrafish and Xenopus. Dev. Biol. 1996, 177:96-103.
28. Dhein S., Pejman P., Krusemann K. Effects of the I(K.ATP) blockers glibenclamide and HMR1883 on cardiac electrophysiology during ischemia and reperfusion. Eur. J. Pharmacol. 2000, 398:273-284.
29. Doyle D.A., Morais Cabral J., Pfuetzner R.A., Kuo A., Gulbis J.M., Cohen S.L., Chait B.T., MacKinnon R. The structure of the potassium channel: molecular basis of K+conduction and selectivity. Science 1998, 280:69-77.
30. Duboc V., Rottinger E., Lapraz F., Besnardeau L., Lepage T. Left-right asymmetry in the sea urchin embryo is regulated by nodal signaling on the right side. Dev. Cell 2005, 9:147-158.
31. Edwards A.G., Rees M.L., Gioscia R.A., Zachman D.K., Lynch J.M., Browder J.C., Chicco A.J., Moore R.L. PKC-permitted elevation of sarcolemmal KATP concentration may explain female-specific resistance to myocardial infarction. J. Physiol. 2009.
32. Ellertsdottir E., Ganz J., Durr K., Loges N., Biemar F., Seifert F., Ettl A.K., Kramer-Zucker A.K., Nitschke R., Driever W. A mutation in the zebrafish Na, K-ATPase subunit atp1a1a.1 provides genetic evidence that the sodium potassium pump contributes to left-right asymmetry downstream or in parallel to nodal flow. Dev. Dyn. 2006, 235:1794-1808.
33. Esser A.T., Smith K.C., Weaver J.C., Levin M. Mathematical model of morphogen electrophoresis through gap junctions. Dev. Dyn. 2006, 235:2144-2159.
34. Ficker E., Dennis A.T., Obejero-Paz C.A., Castaldo P., Taglialatela M., Brown A.M. Retention in the endoplasmic reticulum as a mechanism of dominant-negative current suppression in human long QT syndrome. J. Mol. Cell. Cardiol. 2000, 32:2327-2337.
35. Findlay I., Dunne M.J., Petersen O.H. ATP-sensitive inward rectifier and voltage- and calcium-activated K+channels in cultured pancreatic islet cells. J. Membr. Biol. 1985, 88:165-172.
36. Foster D.B., Rucker J.J., Marban E. Is Kir6.1 a subunit of mitoK(ATP)?. Biochem. Biophys. Res. Commun. 2008, 366:649-656.
37. Fujinaga M., Baden J.M. Evidence for an adrenergic mechanism in the control of body asymmetry. Dev. Biol. 1991, 143:203-205.
38. Fukumoto T., Kema I.P., Levin M. Serotonin signaling is a very early step in patterning of the left-right axis in chick and frog embryos. Curr. Biol. 2005, 15:794-803.
39. Garcia-Castro M.I., Vielmetter E., Bronner-Fraser M. N-Cadherin, a cell adhesion molecule involved in establishment of embryonic left-right asymmetry. Science 2000, 288:1047-1051.
40. Garic-Stankovic A., Hernandez M., Flentke G.R., Zile M.H., Smith S.M. A ryanodine receptor-dependent Cai2+ asymmetry at Hensen's node mediates avian lateral identity. Development 2008.
41. Gloyn A.L., Pearson E.R., Antcliff J.F., Proks P., Bruining G.J., Slingerland A.S., Howard N., Srinivasan S., Silva J.M., Molnes J., Edghill E.L., Frayling T.M., Temple I.K., Mackay D., Shield J.P., Sumnik Z., van Rhijn A., Wales J.K., Clark P., Gorman S., Aisenberg J., Ellard S., Njolstad P.R., Ashcroft F.M., Hattersley A.T. Activating mutations in the gene encoding the ATP-sensitive potassium-channel subunit Kir6.2 and permanent neonatal diabetes. N Engl J. Med. 2004, 350:1838-1849.
42. Gogelein H., Englert H., Kotzan A., Hack Rudiger, Lehr K.-H., Seiz W., Becker R.H.A., Sultan E., Scholkens B.A., Busch A.E. HMR 1098: an inhibitor of cardiac ATP-sensitive potassium channels. Cardiovasc. Drug Rev. 2000, 18:157-174.
43. Gogelein H., Ruetten H., Albus U., Englert H.C., Busch A.E. Effects of the cardioselective KATP channel blocker HMR 1098 on cardiac function in isolated perfused working rat hearts and in anesthetized rats during ischemia and reperfusion. Naunyn Schmiedebergs Arch Pharmacol. 2001, 364:33-41.
44. Gromada J., Dissing S., Kofod H., Frokjaer-Jensen J. Effects of the hypoglycaemic drugs repaglinide and glibenclamide on ATP-sensitive potassium-channels and cytosolic calcium levels in beta TC3 cells and rat pancreatic beta cells. Diabetologia 1995, 38:1025-1032.
45. Hadjantonakis A.K., Pisano E., Papaioannou V.E. Tbx6 regulates left/right patterning in mouse embryos through effects on nodal cilia and perinodal signaling. PLoS ONE 2008, 3:e2511.
46. Harland R.M. In situ hybridization: an improved whole mount method for Xenopus embryos. Xenopus laevis: practical uses in cell and molecular biology 1991, Vol. 36:685-695. Academic Press, San Diego.
47. Harvey R.P., Melton D.A. Microinjection of synthetic Xhox-1A homeobox mRNA disrupts somite formation in developing Xenopus embryos. Cell 1988, 53:687-697.
48. Heginbotham L., Lu Z., Abramson T., MacKinnon R. Mutations in the K+channel signature sequence. Biophys. J. 1994, 66:1061-1067.
49. Hegle A.P., Marble D.D., Wilson G.F. A voltage-driven switch for ion-independent signaling by ether-a-go-go K+channels. Proc. Natl Acad. Sci. USA 2006, 103:2886-2891.
50. Hibino T., Ishii Y., Levin M., Nishino A. Ion flow regulates left-right asymmetry in sea urchin development. Dev. Genes Evol. 2006, 216:265-276.
51. Hu Q., Klippel A., Muslin A.J., Fantl W.J., Williams L.T. Ras-dependent induction of cellular responses by constitutively active phosphatidylinositol-3 kinase. Science 1995, 268:100-102.
52. Huopio H., Shyng S.L., Otonkoski T., Nichols C.G. K(ATP) channels and insulin secretion disorders. Am. J. Physiol. Endocrinol. Metab. 2002, 283:E207-E216.
53. Hyatt B.A., Yost H.J. The left-right coordinator: the role of Vg1 in organizing left-right axis formation. Cell 1998, 93:37-46.
54. Jiang Y., Lee A., Chen J., Ruta V., Cadene M., Chait B.T., MacKinnon R. X-ray structure of a voltage-dependent K+channel. Nature 2003, 423:33-41.
55. Jons T., Wittschieber D., Beyer A., Meier C., Brune A., Thomzig A., Ahnert-Hilger G., Veh R.W. K+-ATP-channel-related protein complexes: potential transducers in the regulation of epithelial tight junction permeability. J. Cell Sci. 2006, 119:3087-3097.
56. Jovanovic S., Jovanovic A. High glucose regulates the activity of cardiac sarcolemmal ATP-sensitive K+channels via 1, 3-bisphosphoglycerate: a novel link between cardiac membrane excitability and glucose metabolism. Diabetes 2005, 54:383-393.
57. Kaab S., Zwermann L., Barth A., Hinterseer M., Englert H.C., Gogelein H., Nabauer M. Selective block of sarcolemmal IKATP in human cardiomyocytes using HMR 1098. Cardiovasc. Drugs Ther. 2003, 17:435-441.
58. Kaczmarek L.K. Non-conducting functions of voltage-gated ion channels. Nat. Rev. Neurosci. 2006, 7:761-771.
59. Kane G.C., Behfar A., Dyer R.B., O'Cochlain D.F., Liu X.K., Hodgson D.M., Reyes S., Miki T., Seino S., Terzic A. KCNJ11 gene knockout of the Kir6.2 KATP channel causes maladaptive remodeling and heart failure in hypertension. Hum. Mol. Genet. 2006, 15:2285-2297.
60. Kane G.C., Liu X.K., Yamada S., Olson T.M., Terzic A. Cardiac KATP channels in health and disease. J. Mol. Cell. Cardiol. 2005, 38:937-943.
61. Kang J.Q., Shen W., Macdonald R.L. The GABRG2 mutation, Q351X, associated with generalized epilepsy with febrile seizures plus, has both loss of function and dominant-negative suppression. J. Neurosci. 2009, 29:2845-2856.
62. Kishimoto N., Cao Y., Park A., Sun Z. Cystic kidney gene seahorse regulates cilia-mediated processes and Wnt pathways. Dev. Cell 2008, 14:954-961.
63. Kitaguchi T., Nagai T., Nakata K., Aruga J., Mikoshiba K. Zic3 is involved in the left-right specification of the Xenopus embryo. Dev. Suppl. 2000, 127:4787-4795.
64. Klein S.L. The first cleavage furrow demarcates the dorsal-ventral axis in Xenopus embryos. Dev. Biol. 1987, 120:299-304.
65. Kono Y., Horie M., Takano M., Otani H., Xie L.H., Akao M., Tsuji K., Sasayama S. The properties of the Kir6.1-6.2 tandem channel co-expressed with SUR2A. Pflugers Arch 2000, 440:692-698.
66. Koster J.C., Marshall B.A., Ensor N., Corbett J.A., Nichols C.G. Targeted overactivity of beta cell K(ATP) channels induces profound neonatal diabetes. Cell 2000, 100:645-654.
67. Kramer K.L., Barnette J.E., Yost H.J. PKCgamma regulates syndecan-2 inside-out signaling during xenopus left-right development. Cell 2002, 111:981-990.
68. Kreiling J.A., Balantac Z.L., Crawford A.R., Ren Y., Toure J., Zchut S., Kochilas L., Creton R. Suppression of the endoplasmic reticulum calcium pump during zebrafish gastrulation affects left-right asymmetry of the heart and brain. Mech. Dev. 2008, 125:396-410.
69. Kubo Y., Adelman J.P., Clapham D.E., Jan L.Y., Karschin A., Kurachi Y., Lazdunski M., Nichols C.G., Seino S., Vandenberg C.A. International Union of Pharmacology. LIV. Nomenclature and molecular relationships of inwardly rectifying potassium channels. Pharmacol Rev. 2005, 57:509-526.
70. Kurpios N.A., Ibanes M., Davis N.M., Lui W., Katz T., Martin J.F., Belmonte J.C., Tabin C.J. The direction of gut looping is established by changes in the extracellular matrix and in cell:cell adhesion. Proc. Natl Acad. Sci. USA 2008, 105:8499-8506.
71. Lalli M.J., Johns D.C., Janecki M., Liu Y., O'Rourke B., Marban E. Suppression of KATP currents by gene transfer of a dominant negative Kir6.2 construct. Pflugers Arch 1998, 436:957-961.
72. Lang F., Vallon V., Knipper M., Wangemann P. Functional significance of channels and transporters expressed in the inner ear and kidney. Am. J. Physiol. Cell Physiol. 2007, 293:C1187-C1208.
73. Levin M. Left-right asymmetry and the chick embryo. Semin. Cell Dev. Biol. 1998, 9:67-76.
74. Levin M. 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 2006, 78:191-223.
75. Levin M., Buznikov G.A., Lauder J.M. Of minds and embryos: left-right asymmetry and the serotonergic controls of pre-neural morphogenesis. Dev. Neurosci. 2006, 28:171-185.
76. Levin M., Johnson R.L., Stern C.D., Kuehn M., Tabin C. A molecular pathway determining left-right asymmetry in chick embryogenesis. Cell 1995, 82:803-814.
77. Levin M., Mercola M. Gap junctions are involved in the early generation of left right asymmetry. Dev. Biol. 1998, 203:90-105.
78. Levin M., Mercola M. Gap junctions are involved in the early generation of left-right asymmetry. Dev. Biol. 1998, 203:90-105.
79. 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 1999, 126:4703-4714.
80. Levin M., Nascone N. Two molecular models of initial left-right asymmetry generation. Med. Hypotheses 1997, 49:429-435.
81. Levin M., Pagan S., Roberts D.J., Cooke J., Kuehn M.R., Tabin C.J. Left/right patterning signals and the independent regulation of different aspects of Situs in the chick embryo. Dev. Biol. 1997, 189:57-67.
82. Levin M., Palmer A.R. Left-right patterning from the inside out: widespread evidence for intracellular control. Bioessays. 2007, 29:271-287.
83. Levin M., Thorlin T., Robinson K.R., Nogi T., Mercola M. Asymmetries in H+/K+-ATPase and cell membrane potentials comprise a very early step in left-right patterning. Cell 2002, 111:77-89.
84. Light P.E., Kanji H.D., Fox J.E., French R.J. Distinct myoprotective roles of cardiac sarcolemmal and mitochondrial KATP channels during metabolic inhibition and recovery. FASEB J. 2001, 15:2586-2594.
85. Lockwood C., Zaidel-Bar R., Hardin J. The C. elegans zonula occludens ortholog cooperates with the cadherin complex to recruit actin during morphogenesis. Curr. Biol. 2008, 18:1333-1337.
86. Lohr J.L., Danos M.C., Yost H.J. Left-right asymmetry of a nodal-related gene is regulated by dorsoanterior midline structures during Xenopus development. Dev. Suppl. 1997, 124:1465-1472.
87. Lu C., Halvorsen S. Channel activators regulate ATP-sensitive potassium channel (Kir6.1) expression in chick cardiomyocytes. FEBS Lett. 1997, 412:121-125.
88. Maisonneuve C., Guilleret I., Vick P., Weber T., Andre P., Beyer T., Blum M., Constam D.B. Bicaudal C, a novel regulator of Dvl signaling abutting RNA-processing bodies, controls cilia orientation and leftward flow. Development 2009, 136:3019-3030.
89. Malhotra J.D., Kazen-Gillespie K., Hortsch M., Isom L.L. Sodium channel beta subunits mediate homophilic cell adhesion and recruit ankyrin to points of cell-cell contact. J. Biol. Chem. 2000, 275:11383-11388.
90. Marcus D.C., Wu T., Wangemann P., Kofuji P. KCNJ10 (Kir4.1) potassium channel knockout abolishes endocochlear potential. Am. J. Physiol. Cell Physiol. 2002, 282:C403-C407.
91. Marshall L.J., Muimo R., Riemen C.E., Mehta A. Na+and K+regulate the phosphorylation state of nucleoside diphosphate kinase in human airway epithelium. Am. J. Physiol. 1999, 276:C109-C119.
92. Masho R. Close correlation between the 1st cleavage plane and the body axis in early Xenopus embryos. Dev. Growth Differ. 1990, 32:57-64.
93. Masia R., De Leon D.D., MacMullen C., McKnight H., Stanley C.A., Nichols C.G. A mutation in the TMD0-L0 region of sulfonylurea receptor-1 (L225P) causes permanent neonatal diabetes mellitus (PNDM). Diabetes 2007, 56:1357-1362.
94. Matter K., Balda M.S. Signalling to and from tight junctions. Nat. Rev. Mol. Cell Biol. 2003, 4:225-236.
95. McEwen D.P., Isom L.L. Heterophilic interactions of sodium channel beta1 subunits with axonal and glial cell adhesion molecules. J. Biol. Chem. 2004, 279:52744-52752.
96. McGrath J., Somlo S., Makova S., Tian X., Brueckner M. Two populations of node monocilia initiate left-right asymmetry in the mouse. Cell 2003, 114:61-73.
97. Merzdorf C.S., Chen Y.H., Goodenough D.A. Formation of functional tight junctions in Xenopus embryos. Dev. Biol. 1998, 195:187-203.
98. Miki T., Seino S. Roles of KATP channels as metabolic sensors in acute metabolic changes. J. Mol. Cell. Cardiol. 2005, 38:917-925.
99. Morokuma J., Blackiston D., Levin M. KCNQ1 and KCNE1 K+channel components are involved in early left-right patterning in Xenopus laevis embryos. Cell. Physiol. Biochem. 2008, 21:357-372.
100. Newport J., Kirschner M. A major developmental transition in early Xenopus embryos: I. Characterization and timing of cellular changes at the midblastula stage. Cell 1982, 30:675-686.
101. Newport J., Kirschner M. A major developmental transition in early Xenopus embryos: II. Control of the onset of transcription. Cell 1982, 30:687-696.
102. Nichols C.G. KATP channels as molecular sensors of cellular metabolism. Nature 2006, 440:470-476.
103. Nieto M.A., Patel K., Wilkinson D.G. In situ hybridization analysis of chick embryos in whole mount and tissue sections. Methods Cell Biol. 1996, 51:219-235.
104. Nieuwkoop P.D., Faber J. Normal Table of Xenopus laevis (Daudin) 1967, North-Holland Publishing Company, Amsterdam.
105. Noma A. ATP-regulated K+channels in cardiac muscle. Nature 1983, 305:147-148.
106. Pagan-Westphal S., Tabin C. The transfer of left-right positional information during chick embryogenesis. Cell 1998, 93:25-35.
107. Peeters H., Devriendt K. Human laterality disorders. Eur. J. Med. Genet. 2006, 49:349-362.
108. 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. 2002, 12:938-943.
109. Pountney D.J., Sun Z.Q., Porter L.M., Nitabach M.N., Nakamura T.Y., Holmes D., Rosner E., Kaneko M., Manaris T., Holmes T.C., Coetzee W.A. Is the molecular composition of K(ATP) channels more complex than originally thought?. J. Mol. Cell. Cardiol. 2001, 33:1541-1546.
110. Pu J.L., Ye B., Kroboth S.L., McNally E.M., Makielski J.C., Shi N.Q. Cardiac sulfonylurea receptor short form-based channels confer a glibenclamide-insensitive KATP activity. J. Mol. Cell. Cardiol. 2008, 44:188-200.
111. Qiu D., Cheng S.M., Wozniak L., McSweeney M., Perrone E., Levin M. Localization and loss-of-function implicates ciliary proteins in early, cytoplasmic roles in left-right asymmetry. Dev. Dyn. 2005, 234:176-189.
112. Rajasekaran S.A., Beyenbach K.W., Rajasekaran A.K. Interactions of tight junctions with membrane channels and transporters. Biochim. Biophys. Acta 2008, 1778:757-769.
113. Ramsdell A.F. Left-right asymmetry and congenital cardiac defects: getting to the heart of the matter in vertebrate left-right axis determination. Dev. Biol. 2005, 288:1-20.
114. Raya A., Kawakami Y., Rodriguez-Esteban C., Ibanes M., Rasskin-Gutman D., Rodriguez-Leon J., Buscher D., Feijo J.A., Izpisua Belmonte J.C. Notch activity acts as a sensor for extracellular calcium during vertebrate left-right determination. Nature 2004, 427:121-128.
115. Reimann F., Ashcroft F.M. Inwardly rectifying potassium channels. Curr. Opin. Cell Biol. 1999, 11:503-508.
116. Sampath K., Cheng A.M., Frisch A., Wright C.V. Functional differences among Xenopus nodal-related genes in left-right axis determination. Development 1997, 124:3293-3302. Supplement.
117. Sanders E.J., Dicaprio R.A. Intercellular junctions in the Xenopus embryo prior to gastrulation. J. Exp. Zool. 1976, 197:415-421.
118. Sarmah B., Latimer A.J., Appel B., Wente S.R. Inositol polyphosphates regulate zebrafish left-right asymmetry. Dev. Cell 2005, 9:133-145.
119. Schneider I., Houston D.W., Rebagliati M.R., Slusarski D.C. Calcium fluxes in dorsal forerunner cells antagonize {beta}-catenin and alter left-right patterning. Development 2007.
120. Schwappach B., Zerangue N., Jan Y.N., Jan L.Y. Molecular basis for K(ATP) assembly: transmembrane interactions mediate association of a K+channel with an ABC transporter. Neuron 2000, 26:155-167.
121. Schweickert A., Weber T., Beyer T., Vick P., Bogusch S., Feistel K., Blum M. Cilia-driven leftward flow determines laterality in Xenopus. Curr. Biol. 2007, 17:60-66.
122. Seharaseyon J., Sasaki N., Ohler A., Sato T., Fraser H., Johns D.C., O'Rourke B., Marban E. Evidence against functional heteromultimerization of the KATP channel subunits Kir6.1 and Kir6.2. J. Biol. Chem. 2000, 275:17561-17565.
123. Shibata T., Hibino H., Doi K., Suzuki T., Hisa Y., Kurachi Y. Gastric type H+, K+-ATPase in the cochlear lateral wall is critically involved in formation of the endocochlear potential. Am. J. Physiol. Cell Physiol. 2006, 291:C1038-C1048.
124. Shimeld S.M., Levin M. Evidence for the regulation of left-right asymmetry in Ciona intestinalis by ion flux. Dev. Dyn. 2006, 235:1543-1553.
125. Shimomura K. The K(ATP) channel and neonatal diabetes. Endocr. J. 2009, 56:165-175.
126. Simard A., Di Pietro E., Young C.R., Plaza S., Ryan A.K. Alterations in heart looping induced by overexpression of the tight junction protein Claudin-1 are dependent on its C-terminal cytoplasmic tail. Mech. Dev. 2006, 123:210-227.
127. Sivaprasadarao A., Taneja T.K., Mankouri J., Smith A.J. Trafficking of ATP-sensitive potassium channels in health and disease. Biochem. Soc. Trans. 2007, 35:1055-1059.
128. Sive H.L., Grainger R.M., Harland R.M. Early Development of Xenopus Laevis 2000, Cold Spring Harbor Laboratory Press, New York.
129. Slesinger P.A., Patil N., Liao Y.J., Jan Y.N., Jan L.Y., Cox D.R. Functional effects of the mouse weaver mutation on G protein-gated inwardly rectifying K+channels. Neuron 1996, 16:321-331.
130. Speder P., Petzoldt A., Suzanne M., Noselli S. Strategies to establish left/right asymmetry in vertebrates and invertebrates. Curr. Opin. Genet. Dev. 2007.
131. Spruce A.E., Standen N.B., Stanfield P.R. Voltage-dependent ATP-sensitive potassium channels of skeletal muscle membrane. Nature 1985, 316:736-738.
132. Standen N.B., Quayle J.M., Davies N.W., Brayden J.E., Huang Y., Nelson M.T. Hyperpolarizing vasodilators activate ATP-sensitive K+channels in arterial smooth muscle. Science 1989, 245:177-180.
133. Suzuki M., Kotake K., Fujikura K., Inagaki N., Suzuki T., Gonoi T., Seino S., Takata K. Kir6.1: a possible subunit of ATP-sensitive K+channels in mitochondria. Biochem. Biophys. Res. Commun. 1997, 241:693-697.
134. Suzuki M., Saito T., Sato T., Tamagawa M., Miki T., Seino S., Nakaya H. Cardioprotective effect of diazoxide is mediated by activation of sarcolemmal but not mitochondrial ATP-sensitive potassium channels in mice. Circulation 2003, 107:682-685.
135. Tabin C. Do we know anything about how left-right asymmetry is first established in the vertebrate embryo?. J. Mol. Histol. 2005, 1-7.
136. Tabin C.J., Vogan K.J. A two-cilia model for vertebrate left-right axis specification. Genes Dev. 2003, 17:1-6.
137. Tinker A., Jan Y.N., Jan L.Y. Regions responsible for the assembly of inwardly rectifying potassium channels. Cell 1996, 87:857-868.
138. Toyoizumi R., Kobayashi T., Kikukawa A., Oba J., Takeuchi S. Adrenergic neurotransmitters and calcium ionophore-induced situs inversus viscerum in Xenopus laevis embryos. Dev. Growth Differ. 1997, 39:505-514.
139. Toyoizumi R., Ogasawara T., Takeuchi S., Mogi K. Xenopus nodal related-1 is indispensable only for left-right axis determination. Int. J. Dev. Biol. 2005, 49:923-938.
140. van Bever L., Poitry S., Faure C., Norman R.I., Roatti A., Baertschi A.J. Pore loop-mutated rat KIR6.1 and KIR6.2 suppress KATP current in rat cardiomyocytes. Am. J. Physiol. Heart Circ. Physiol. 2004, 287:H850-H859.
141. Van Itallie C.M., Fanning A.S., Bridges A., Anderson J.M. ZO-1 stabilizes the tight junction solute barrier through coupling to the perijunctional cytoskeleton. Mol. Biol. Cell 2009, 20:3930-3940.
142. Van Laer L., Carlsson P.I., Ottschytsch N., Bondeson M.L., Konings A., Vandevelde A., Dieltjens N., Fransen E., Snyders D., Borg E., Raes A., Van Camp G. The contribution of genes involved in potassium-recycling in the inner ear to noise-induced hearing loss. Hum. Mutat. 2006, 27:786-795.
143. Vandenberg L.N., Levin M. Perspectives and open problems in the early phases of left-right patterning. Semin. Cell Dev. Biol. 2009, 20:456-463.
144. Vanhoven M.K., Bauer Huang S.L., Albin S.D., Bargmann C.I. The claudin superfamily protein nsy-4 biases lateral signaling to generate left-right asymmetry in C. elegans olfactory neurons. Neuron 2006, 51:291-302.
145. Vize P.D., Melton D.A., Hemmati-Brivanlou A., Harland R.M. Assays for gene function in developing Xenopus embryos. Meth. Cell Biol. 1991, 36:367-387.
146. Warner A.E., Guthrie S.C., Gilula N.B. Antibodies to gap-junctional protein selectively disrupt junctional communication in the early amphibian embryo. Nature 1984, 311:127-131.
147. Whitman M., Mercola M. TGF-beta superfamily signaling and left-right asymmetry. Sci. STKE 2001, 2001:RE1.
148. Whitman M., Mercola M. TGF-beta superfamily signaling and left-right asymmetry. Science's STKE [Electronic Resource]: Signal Transduction Knowledge Environment. 2001, 2001:RE1.
149. Xu J., Van Keymeulen A., Wakida N.M., Carlton P., Berns M.W., Bourne H.R. Polarity reveals intrinsic cell chirality. Proc. Natl Acad. Sci. USA 2007, 104:9296-9300.
150. Yamauchi H., Miyakawa N., Miyake A., Itoh N. Fgf4 is required for left-right patterning of visceral organs in zebrafish. Dev. Biol. 2009, 332:177-185.
151. Yost H.J. Diverse initiation in a conserved left-right pathway?. Curr. Opin. Genet. Dev. 1999, 9:422-426.
152. Yost H.J. Establishment of left-right asymmetry. Int. Rev. Cytol. 2001, 203:357-381.
153. Zerangue N., Schwappach B., Jan Y.N., Jan L.Y. A new ER trafficking signal regulates the subunit stoichiometry of plasma membrane K(ATP) channels. Neuron 1999, 22:537-548.
154. Zobel C., Cho H.C., Nguyen T.T., Pekhletski R., Diaz R.J., Wilson G.J., Backx P.H. Molecular dissection of the inward rectifier potassium current (IK1) in rabbit cardiomyocytes: evidence for heteromeric co-assembly of Kir2.1 and Kir2.2. J. Physiol. 2003, 550:365-372.