Early, H+-V-ATPase-dependent proton flux is necessary for consistent left-right patterning of non-mammalian vertebrates

Development

Volumn 133, Issue 9, 2006, Pages 1657-1671

  Adams, Dany S ^a   Robinson, Kenneth R ^b   Fukumoto, Takahiro ^c,e   Yuan, Shipeng ^d   Albertson, R Craig ^c   Yelick, Pamela ^c   Kuo, Lindsay ^c   McSweeney, Megan ^c   Levin, Michael ^a  

^a HARVARD SCHOOL OF DENTAL MEDICINE   (United States)

^b PURDUE UNIVERSITY   (United States)

^c FORSYTH INSTITUTE   (United States)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

^e WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Axial patterning; Chick; Cytoplasmic pH; H+ V ATPase; Left right asymmetry; Membrane; V ATPase; Xenopus; Zebrafish

Indexed keywords

ACTIN; CELL PROTEIN; PROTEIN SPAW; PROTON PUMP; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE; SEROTONIN; SONIC HEDGEHOG PROTEIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; CELL PH; CHICKEN; CONTROLLED STUDY; EMBRYO; EMBRYO PATTERN FORMATION; ENZYME ACTIVITY; ENZYME INHIBITION; HETEROTAXY SYNDROME; IMMUNOHISTOCHEMISTRY; KUPFFER CELL; MOLECULAR GENETICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTON TRANSPORT; VERTEBRATE; XENOPUS; ZEBRA FISH;

ACTINS; ANIMALS; BODY PATTERNING; CELL MEMBRANE; CHICK EMBRYO; EMBRYO, NONMAMMALIAN; ENZYME INHIBITORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; H(+)-K(+)-EXCHANGING ATPASE; HYDROGEN-ION CONCENTRATION; IMMUNOHISTOCHEMISTRY; MODELS, BIOLOGICAL; PROTONS; TIME FACTORS; VERTEBRATES; XENOPUS; ZEBRAFISH;

ANIMALIA; DANIO RERIO; ERINACEIDAE; MAMMALIA; VERTEBRATA;

EID: 33744506178     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.02341     Document Type: Article

References (133)

1. Adams, D. and Levin, M. (2006). Gap junctions and ion fluxes in patterning: strategies for investigating biophysical epigenetic control mechanisms in Xenopus. In Analysis of Growth Factor Signaling in Embryos (ed. M. Whitman and A. K. Sater). Boca Raton, FL: Taylor & Francis (in press).
2. Albertson, R. C. and Yelick, R C. (2005). Roles for Fgf8 signaling in left-right patterning of the visceral organs and craniofacial skeleton. Dev Biol. 283, 310-321.
3. Akopian, A. N., Chen, C. C., Ding, Y., Cesare, P. and Wood, J. N. (2000). A new member of the acid-sensing ion channel family NeuroReport 11, 2217-2222.
4. +)-ATPase and band 3. Am. J. Physiol. 270, C1571-C1580.
5. Amack, J. D. and Yost, H. J. (2004). The T box transcription factor no tail in ciliated cells controls zebrafish left-right asymmetry. Curr. Biol. 14, 685-690.
6. Arif, I., Newman, I. and Keenlyside, N. (1995). Proton flux measurements from tissues in buffered solutions. Plant Cell Environ. 18, 1319-1324.
7. Ayscough, K. (1998). Use of latrunculin-A, an actin monomer-binding drug. Meth. Enzymol. 298, 18-25.
8. Berdiev, B. K., Xia, J., McLean, L. A., Markert, J. M., Gillespie, G. Y., Mapstone, T. B., Naren, A. P., Jovov, B., Bubien, J. K., A, Ji H. L. et al. (2003). Acid-sensing ion channels in malignant gliomas. J. Biol. Chem. 278, 15023-15034.
9. Bidani, A., Wang, C. Z., Saggi, S. J. and Heming, T A. (1998). Evidence for pH sensitivity of tumor necrosis factor-alpha release by alveolar macrophages. Lung 176, 111-121.
10. Black, S. D. and Vincent, J. R (1988). The first cleavage plane and the embryonic axis are determined by separate mechanisms in Xenopus laevis. II. Experimental dissociation by lateral compression of the egg. Dev. Biol. 128, 65-71.
11. Bonnafe, E., Touka, M., AitLounis, A., Baas, D., Barras, E., Ucla, C., Moreau,A., Flamant, E, Dubruille, R., Couble, P. et al. (2004). The transcription factor RFX3 directs nodal cilium development and left-right asymmetry specification. Mol Cell. Biol. 24, 4417-4427.
12. Bowman, E. J., Siebers, A. and Altendorf, K. (1988). Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc. Natl. Acad. Sci. USA 85, 7972-7976.
13. Brown, D. and Breton, S. (2000). H(+)V-ATPase-dependent luminal acidification in the kidney collecting duct and the epididymis/vas deferens: vesicle recycling and transcytotic pathways. J. Exp. Biol. 203, 137-145.
14. Brown, D., Sabolic, I. and Gluck, S. (1992). Polarized targeting of V-ATPase in kidney elpithelial cells. J. Exp. Biol. 172, 231-243.
15. Brown, N. and Wolpert, L. (1990). The development of handedness in left/ right asymmetry. Development 109, 1-9.
16. Brown, N. A., Hoyle, C. I., McCarthy, A. and Wolpert, L. (1989). The development of asymmetry: the sidedness of drug-induced limb abnormalities is reversed in situs inversus mice. Development 107, 637-642.
17. Buckler, K. J. and Vaughan-Jones, R. D. (11990). Application of a new pH-sensitive fluoroprobe (carboxy-SNARF-1) for intracellular pH measurement in small, isolated cells. Pflugers Arch. 417, 234-239.
18. Bunney, T. D., De Boer, A. H. and Levin, M. (2003). Fusicoccin signaling reveals 14-3-3 protein function as a novel step in left-right patterning during amphibian embryogenesis. Development 130, 4847-4858.
19. Burdine, R. and Schier, A. (2000). Conserved and divergent mechanisms in left-right axis formation. Genes Dev. 14, 763-776.
20. Burn, J. (1991). Disturbance of morphological laterality in humans. Ciba Found. Symp. 162,282-296.
21. Busa, W. B. and Nuccitelli, R. (1984). Metabolic-regulation via intracellular Ph. Am. J. Physiol. 246, R409-R438.
22. Chen, S. H., Bubb, M. R., Yarmola, E. G., Zuo, J., Jiang, J., Lee, B. S., Lu, M., Gluck, S. L., Hurst, I. R. and Holliday, L. S. (2004). Vacuolar H+-ATPase binding to microfilaments: regulation in response to phosphatidylinositol 3-kinase activity and detailed characterization of the actin-binding site in subunit B. J. Biol. Chem. 279, 7988-7998.
23. Cooke, J. (2004). The evolutionary origins and significance of vertebrate left-right organisation. BioEssays 26, 413-421.
24. Danilchik, M. V. and Black, S. D. (1988). The first cleavage plane and the embryonic axis are determined by separate mechanisms in Xenopus laevis. I. Independence in undisturbed embryos. Dev. Biol. 128, 58-64.
25. Danos, M. C. and Yost, H. J. (1995). Linkage of cardiac left-right asymmetry and dorsal-anterior development in Xenopus. Development 121, 1467-1474.
26. Danos, M. C. and Yost, H. J. (1996). Role of notochord in specification of cardiac left-right orientation in zebrafish and Xenopus. Dev. Biol. 177, 96-103.
27. De Brabander, M., Geuens, G., Nuydens, R., Willebrords, R., Aerts, F and De Mey, J. (1986). Microtubule dynamics during the cell cycle: the effects of taxol and nocodazole on the microtubule system of Pt K2 cells at different stages of the mitotic cycle. Int. Rev. Cytol. 101, 215-274.
28. Drose, S., Bindseil, K. U., Bowman, E. J., Siebers, A., Zeeck, A. and Altendorf, K. (1993). Inhibitory effect of modified bafilomycins and concanamycins on P- and V-type adenosinetriphosphatases. Biochemistry 32, 3902-3906.
29. Duboc, V, Rottinger, E., Lapraz, F., Besnardeau, L. and Lepage, T (2005). Left-right asymmetry in the sea urchin embryo is regulated by nodal signaling on the right side. Dev. Cell 9, 147-158.
30. Epps, D., Wolfe, M. and Groppi, V. (11994). 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, 137-150.
31. Essner, J., Vogan, K., Wagner, M., Tabin, C., Yost, H. and Brueckner, M. (2002). Conserved function for embryonic nodal cilia. Nature 418, 37-38.
32. Essner, J. J., Amack, J. D., Nyholm, M. K., Harris, E. B. and Yost, H. J. (2005). Kupffer's vesicle is a ciliated organ of asymmetry in the zebrafish embryo that initiates left-right development of the brain, heart and gut. Development 133, 1247-1260.
33. Finbow, M. E., John, S., Kam, E., Apps, D. K. and Pitts, J. D. (1993). Disposition and orientation of ductin (DCCD-reactive vacuolar H(+)-ATPase subunit) in mammalian membrane complexes. Exp. Cell Res. 207, 261-270.
34. Fukumoto, T., Blakely, R. D. and Levin, M. (2005a). Serotonin transporter function is an early step in left-right patterning in chick and frog embryos. Dev Neurosci. 27,349-363.
35. Fukumoto, T., Kema, I. P. and Levin, M. (2005b). Serotonin signaling is a very early step in patterning of the left-right axis in chick and frog embryos. Curr. Biol. 15, 794-803.
36. Gillespie, J. I. and Greenwell, J. R. (1988). Changes in intracellular pH and pH regulating mechanisms in somitic cells of the early chick embryo: a study using fluorescent pH-sensitive dye. J. Physiol. 405, 385-395.
37. Gluck, S. (1992). V-ATPases of the plasma membrane. J. Exp. Biol. 172, 29-37.
38. Grandin, N. and Charbonneau, M. (1989). Intracellular pH and the increase in protein synthesis accompanying activation of Xenopus eggs. Biol. Cell 67, 321-330.
39. Greenfield, L. J., Jr, Hackett, J. T. and Linden, J. (1990). Xenopus oocyte K+ current. III. Phorbol esters and pH regulate current at gap junctions. Am. J. Physiol. 259, C792-C800.
40. Gross, S. P., Tuma, M. C., Deacon, S. W., Serpinskaya, A. S., Reilein, A. R. and Gelfand, V. I. (2002). Interactions and regulation of molecular motors in Xenopus melanophores. J. Cell Biol. 156, 855-865.
41. Hamada, H., Meno, C., Watanabe, D. and Saijoh, Y. (2002). Establishment of vertebrate left-right asymmetry. Nat. Rev. Genet. 3, 103-113.
42. Hamburger, V. and Hamilton, H. (1992). A series of normal stages in the development of the chick embryo. Dev. Dyn. 195, 231-272.
43. Harland, R. M. (1991). In situ hybridization: an improved whole mount method for Xenopus embryos. In Xeropus laevis: Practical uses in Cell and Molecular Biology, vol. 36 (ed. B. K. Kay and H. B. Peng), pp. 685-695. San Diego: Academic Press.
44. Harvey, R. P. and Melton, D. A. (1988). Microinjection of synthetic Xhox-1A homeobox mRNA disrupts somite formation in developing Xenopus embryos. Cell 53, 687-697.
45. Harvey, W. (1992). Physiology of V-ATPases. In V-ATPases, Vol. 172 (ed. W. Harvey and N. Nelson), pp. 1-17. Philadelphia, PA: Temple University.
46. Harvey, W. R. and Wieczorek, H. (1997). Animal plasma membrane energization by chemosmotic H+ V-ATPases. J. Exp. Biol. 200, 203-216.
47. Hayashi, M., Haga, M., Yatsushiro, S., Yamamoto, A. and Moriyama, Y. (1999). Vesicular monoamine transporter 1 is responsible for storage of 5-hydroxytryptamine in rat pinealocytes. J. Neurochem. 73, 2538-2545.
48. Hibino, T., Yuichiro, I., Levin, M. and Nishino, A. (2006). Ion flow regulates left-right asymmetry in sea urchin development. Dev. Genes Evol. (in press).
49. Hilgemann, D. W. (2003). From a pump to a pore: how palytoxin opens the gates. Proc. Natl. Acad. Sci. USA 100, 386-388.
50. Hotary, K. B., Nuccitelli, R. and Robinson, K. R. (1992). A computerized 2-dimensional vibrating probe for mapping extracellular current patterns. J. Neurosci. Meth. 43, 55-67.
51. Huss, M., Ingenhorst, G., Konig, S., Gassel, M., Drose, S., Zeeck, A., Altendorf, K. and Wieczorek, H. (2002). Concanamycin A, the specific inhibitor of V-ATPases, binds to the Vo subunit c. J. Biol. Chem. 277, 40544-40548.
52. Hyatt, B. A., Lohr, J. L. and Yost, H. J. (1996). Initiation of vertebrate left-right axis formation by maternal Vg1. Nature 384, 62-65.
53. Inoue, I, Wilkens, S. and Forgac, M. (2003). Subunit structure, function, and arrangement in the yeast and coated vesicle V-ATPases. J. Bioenerg. Biomembr. 35, 291-299.
54. Kawa, G., Yamamoto, A., Yoshimori, L Muguruma, K., Matsuda, I and Moriyama, Y. (2000). Immunohistochemical localization of V-ATPases in rat spermatids. Int J. Androl. 23, 278-283.
55. Kawakami, M. and Nakanishi, N. (2001). The role of an endogenous PKA inhibitor, PKIalpha, in organizing left-right axis formation. Development 128, 2509-2515.
56. Kawakami, Y., Raya, A., Raya, R. M., Rodriguez-Esteban, C. and Belmonte, J. C. (2005). Retinoic acid signalling links left-right asymmetric patterning and bilaterally symmetric somitogenesis in the zebrafish embryo. Nature 435, 165-171.
57. Kawasaki-Nishil, S., Nishi, T. and Forgac, M. (2003). Proton translocation driven by ATP hydrolysis in V-ATPases. FEBS Lett. 545, 76-85.
58. Klein, S. L. (1987). The first cleavage furrow demarcates the dorsal-ventral axis in Xenopus embryos. Dev. Biol. 120, 299-304.
59. Klein, U., Timme, M., Zeiske, W. and Ehrenfeld, J. (1997). The H+ pump in frog skin (Rana esculenta): identification and localization of a V-ATPase. J. Membr. Biol. 157, 117-126.
60. Kosaki, K. and Casey, B. (11998). Genetics of human left-right axis malformations. Semin. Cell Dev. Biol. 9, 89-99.
61. Kramer, K. L., Barnette, J. E. and Yost, H. J. (2002). PKCgamma regulates syndecan-2 inside-out signaling during xenopus left-right development. Cell 111, 981-990.
62. Kramer-Zucker, A. G., Olale, F., Haycraft, C. J., Yoder, B. K., Schiller, A. F. and Drummond, I. A. (2005). Cilia-driven fluid flow in the zebrafish pronephros, brain and Kupffer's vesicle is required for normal organogenesis. Development 132, 1907-1921.
63. Lee, B. S., Gluck, S. L. and Holliday, L. S. (1999). Interaction between vacuolar H(+)-ATPase and microfilaments during osteoclast activation. J. Biol. Chem. 274, 29164-29171.
64. Lee, S. C. and Steinhardt R. A. (11981). Observations on intracellular pH during cleavage of eggs of Xenopus laevis. J. Cell Biol. 91, 414-419.
65. Levin, M. (1999). Twinning and embryonic left-right asymmetry. Laterafity 4, 197-208.
66. Levin, M. (2003a). Bioelectromagnetic patterning fields: roles in embryonic development, regeneration, and neoplasm. Bioelectromagnetics 24, 295-315.
67. Levin, M. (2003b). Electric embryos: endogenous ion fluxes and voltage gradients in left-right asymmetry. Dev. Biol. 259, 482.
68. Levin, M. (2003c). Hypothesis: motor proteins and ion pumps, not ciliary motion, initiate LR asymmetry. BioEssays 25, 1002-1010.
69. Levin, M. (2004). A novel immunohistochemical method for evaluation of antibody specificity and detection of labile targets in biological tissue. J. Biochem. Biophys. Meth. 58, 85-96.
70. Levin, M. (2005). Left-right asymmetry in embryonic development: a comprehensive review. Mech. Dev. 122, 3-25.
71. Levin, M. and Mercola, M. (1998). Gap junctions are involved in the early generation of left right asymmetry. Dev. Biol. 203, 90-105.
72. Levin, M. and Mercola, M. (1999). Gap junction-mediated transfer of left-right patterning signals in the early chick blastoderm is upstream of Shh asymmetry in the node. Development 126, 4703-4714.
73. Levin, M., Johnson, R., Stern, C., Kuehn, M. and Tabin, C. (1995). A molecular pathway determining left-right asymmetry in chick embryogenesis. Cell 82, 803-814.
74. Levin, M., Roberts, D., Holmes, L. and Tabin, C. (1996). Laterality defects in conjoined twins. Nature 384, 321.
75. Levin, M., Thorlin, T., Robinson, K. R., Nogi, T. and Mercola, M. (2002). Asymmetries in H+/K+-ATPase and cell membrane potentials comprise a very early step in left-right patterning. Cell 111, 77-89.
76. Lohr, J. L., Danos, M. C., Groth, T. W. and Yost, H. J. (1998). Maintenance of asymmetric nodal expression in Xenopus laevis. Dev. Genet 23, 194-202.
77. Long, S., Ahmad, N. and Rebagliati, M. (2003). The zebrafish nodal-related gene southpaw is required for visceral and diencephalic left-right asymmetry. Development 130, 2303-2316.
78. Lowe, L., Supp, D., Sampath, K., Yokoyama, T, Wright, C., Potter, S., Overbeek, P. and Kuehn, M. (1996a). Conserved left-right asymmetry of nodal expression and alterations in murine situs inversus. Nature 381, 158-161.
79. Lowe, L. A., Supp, D. M., Sampath, K., Yokoyama, L Wright, C. V., Potter, S. S., Overbeek, R and Kuehn, M. R. (1996b). Conserved left-right asymmetry of nodal expression and alterations in murine situs inversus. Nature 381, 158-161.
80. Lu, M., Vergara, S., Zhang, L., Holliday, L. S., Aris, J. and Gluck, S. L. (2002). The amino-terminal domain of the E subunit of vacuolar H(+)-ATPase (V-ATPase) interacts with the H subunit and is required for V-ATPase function. J. Biol. Chem. 277, 38409-38415.
81. Ludwig, M. G., Vanek, M., Guerini, D., Gasser, J. A., Jones, C. E., Junker U., Hofstetter, H., Wolf, R. M. and Seuwen, K. (2003). Proton-sensing G-protein-coupled receptors. Nature 425, 93-98.
82. Masho, R. (1990). Close correlation between the 1st cleavage plane and the body axis in early Xenopus embryos. Dev. Growth Differ. 32, 57-64.
83. Masucla, C. A. and Montero-Lomeli, M. (2000). An NH2-terminal deleted plasma membrane H+-ATPase is a dominant negative mutant and is sequestered in encloplasmic reticulum derived structures. Biochem. Cell Biol. 78, 51-58.
84. Mathews, R M., Claeys, D., Jaisser, E, Geering, K., Horisberger, J. D., Kraehenbuhl, J. R and Rossier, B. C. (1995). Primary structure and functional expression of the mouse and frog alpha-subunit of the gastric H(+)-K(+)-ATPase. Am. J. Physiol. 268, C1207-C1214.
85. Matsuya, H., Okamoto, M., Ochi, T, Nishikawa, A., Shimizu, S., Kataoka, T, Nagai, K., Wasserman, H. H. and Ohkuma, S. (2000). Reversible and potent uncoupling of hog gastric (H(+)+K(+))-ATPase by prodigiosins. Biochem. Pharmacol. 60, 1855-1863.
86. McGrath, J. and Brueckner, M. (2003). Cilia are at the heart of vertebrate left-right asymmetry. Curr. Opin. Genet. Dev. 13, 385-392.
87. McGrath, J., Somlo, S., Makova, S., Tian, X. and Brueckner, M. (2003). Two populations of node monocilia initiate left-right asymmetry in the mouse. Cell 114, 61-73.
88. Mitchison, T. J. (1994). Towards a pharmacological genetics. Chem. Biol. 1, 3-6.
89. Morley, G. E., Taffet, S. M. and Delmar, M. (1996). Intramolecular interactions mediate pH regulation of connexin43 channels. Biophys. J. 70, 1294-1302.
90. Narbaitz, R., Bastani, B., Galvin, N. J., Kapal, V. K. and Levine, D. Z. (1995). Ultrastructural and immunocytochemical evidence for the presence of polarised plasma membrane H(+)-ATPase in two specialised cell types in the chick embryo chorioallantoic membrane. J. Anat. 186, 245-252.
91. Nieuwkoop, P. D. and Faber, J. (1967). Normal Table of Xenopus laevis (Daudin). Amsterdam: North-Holland Publishing Company.
92. Nishil, T. (2002). The vacuolar (H+)-ATPases - nature's most versatile proton pumps. Nat. Rev. Mol. Cell Bil. 3, 94-103.
93. Nonaka, S., Tanaka, Y., Okada, Y., Takeda, S., Harada, A., Kanai, Y., Kido, M. and Hirokawa, N. (1998). Randomization of left-right asymmetry due to loss of nodal cilia generating leftward flow of extraernbryonic fluid in mice lacking KIF3B motor protein. Cell 95, 829-837.
94. Nuccitelli, R. (2003). Endogenous electric fields in embryos during development, regeneration and wound healing. Radiat. Prot. Dosimetry 106, 375-383.
95. Okada, Y., Takeda, S., Tanaka, Y., Belmonte, J. C. and Hirokawa, N. (2005). Mechanism of nodal flow: a conserved symmetry breaking event in left-right axis determination. Cell 121, 633-644.
96. Payne-Ferreira, T. L. and Yelick, P. C. (2003). AIk8 is required for neural crest cell formation and development of pharyngeal arch cartilages. Dev. Dyn. 228, 683-696.
97. Peng, S. B., Crider, B. R, Tsai, S. J., Xle, X. S. and Stone, D. K. (1996). Identification of a 14-kDa subunit associated with the catalytic sector of clathrin-coated vesicle H+-ATPase. J. Biol. Chem. 271, 3324-3327.
98. Praetorius, J., Andreasen, D., Jensen, B. L., Ainsworth, M. A., Frilis, U. G. and Johansen, T. (2000). NHE1, NHE2, and NHE3 contribute to regulation of intracellular pH in murine duodenal epithelial cells. Am. J. Physiol. Gastrointest. Liver Physiol. 278, G197-G206.
99. Putney, L. K. and Barber, D. L. (2003). Na-H exchange-dependent increase in intracellular pH times G2/M entry and transition. J. Biol. Chem. 278, 44645-44649.
100. Qiu, D., Cheng, S. M., Wozniak, L., McSweeney, M., Perrone, E. and Levin, M. (2005). Localization and loss-of-function suggest early, cytoplasmic roles for 'ciliary' proteins in embryonic left-right asymmetry. Dev. Dyn. 234, 176-189.
101. Raya, A. and Belmonte, J. C. (2004). Sequential transfer of left-right information during vertebrate embryo development. Curr. Opin. Genet. Dev. 14, 575-581.
102. Raya, A., Kawakami, Y., Rodriguez-Esteban, C., Ibanes, M., Rasskin-Gutman, D., Rodriguez-Leon, J., Buscher, D., Feijo, J. A. and lzpisua Belmonte, J. C. (2004). Notch activity acts as a sensor for extracellular calcium during vertebrate left-right determination. Nature 427, 121-128.
103. Sabirov, R. Z., Azimov, R. R., Ando-Akatsuka, Y., Miyoshi, T. and Okada, Y. (1999). Na(+) sensitivity of ROMK1 K(+) channel: role of the Na(+)/ H(+) antiporter. J. Membr. Biol. 172, 67-76.
104. Sater, A. K., Alderton, J. M. and Steinhardt, R. A. (1994). An increase in intracellular pH during neural induction in Xenopus. Development 120, 433-442.
105. Scarborough, G. A. (2000). The plasma membrane proton-translocating ATPase. Cell. Mol. Life Sci. 57, 871-883.
106. Shen, R., Lin, C. T., Bowman, E. J., Bowman, B. J. and Porco, J. A., Jr (2002). Synthesis and V-ATPase inhibition of simplified lobatamide analogues. Org. Lett. 4, 3103-3106.
107. Shen, R., Lin, C. T., Bowman, E. J., Bowman, B. J. and Porco, J. A., Jr (2003). Lobatamide C: total synthesis, stereochemical assignment, preparation of simplified analogues, and V-ATPase inhibition studies. J. Am. Chem. Soc. 125, 7889-7901.
108. Shimeld, S. M. and Levin, M. (2006). Evidence for the regulation of left-right asymmetry in Ciona intestinalis by ion flux. Dev. Dyn. (in press).
109. Shrode, L. D., Tapper, H. and Grinstein, S. (1997). Role of intracellular pH in proliferation, transformation, and apoptosis. J. Bioenerg. Biomembr 29, 393-399.
110. - exchange to regulation of steady-state pHi in human neutrophils. Am. J. Physiol. 261, C906-C915.
111. Sive, H., Grainger, R. M. and Harland, R. (2000). Early Development of Xenopus laevis. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
112. Smith, P. J. and Trimarchi, J. (2001). Noninvasive measurement of hydrogen and potassium ion flux from single cells and epithelial structures. Am. J. Physiol. Cell Physiol. 280, C1-C11.
113. Smith, R J., Hammar, K., Porterfield, D. M., Sanger, R. H. and Trimarchi, J. R. (1999). Self-referencing, non-invasive, ion selective electrode for single cell detection of trans-plasma membrane calcium flux. Microsc. Res. Tech. 46, 398-417.
114. Stern, C. and Holland, P. (1993). Essential Developmental Biology: A Practical Approach. Oxford: IRL Press at Oxford University Press.
115. Sun-Wada, G., Murata, Y., Yamamoto, A., Kanazawa, H., Wada, Y. and Futai, M. (2000). Acidic endomembrane organelles are required for mouse postimplantation development. Dev. Biol. 228, 315-325.
116. Supp, D. M., Witte, D. P., Potter, S. S. and Brueckner, M. (1997). Mutation of an axonernal dynein affects left-right asymmetry in inversus viscerum mice. Nature 389, 963-966.
117. Tabin, C. J. and Vogan, K. J. (2003). A two-cilia model for vertebrate left-right axis specification. Genes Dev 17, 1-6.
118. Tanaka, Y., Okada, Y. and Hirokawa, N. (2005). FGF-induced vesicular release of Sonic hedgehog and retinoic acid in leftward nodal flow is critical for left-right determination. Nature 435, 172-177.
119. Tosteson, M. T., Scriven, D. R., Bharadwaj, A., Arnadottir, J. and Tosteson, D. C. (1997). Interactions of palytoxin with the Na,K-ATPase. Where are those sites? Ann. N. Y. Acad. Sci. 834, 424-425.
120. Tosteson, M. T., Thomas, J., Arnadottir, J. and Tosteson, D. C. (2003). Effects of palytoxin on cation occlusion and phosphorylation of the (Na+,K+)-ATPase. J. Membr. Biol. 192, 181-189.
121. Turin, L. and Warner, A. E. (1980). Intracellular pH in early Xenopus embryos: its effect on current flow between blastomeres. J. Physiol. 300, 489-504.
122. Uzman, J. A., Patil, S., Uzgare, A. R. and Sater, A. K. (1998). The role of intracellular alkalinization in the establishment of anterior neural fate in Xenopus. Dev. Biol. 193, 10-20.
123. Vitavska, O., Wieczorek, H. and Merzendorfer, H. (2003). A novel role for subunit C in mediating binding of the H(+)-V-ATPase to the actin cytoskeleton. J. Biol. Chem. 278, 18499-18505.
124. Vize, P. D., Melton, D. A., Hemmati-Brivanlou, A. and Harland, R. M. (1991). Assays for gene function in developing Xenopus embryos. Meth. Cell Biol. 36, 367-387.
125. Warner, A. E., Guthrie, S. C. and Gilula, N. B. (1984). Antibodies to gap-junctional protein selectively disrupt junctional communication in the early amphibian embryo. Nature 311, 127-131.
126. Westerfield, M. (1995). The Zebrafish Book. Eugene, OR: University of Oregon Press.
127. Wheatly, M. G. and Gao, Y. (2004). Molecular biology of ion motive proteins in comparative models. J. Exp. Biol. 207, 3253-3263.
128. Whitman, M. and Mercola, M. (2001). TGF-beta superfamily signaling and left-right asymmetry. Sci. STKE 2001, RE1.
129. Wieczorek, H. (1999). Animal plasma membrane energization by proton-motive V-ATPases. BioEssays 21, 637-648.
130. Woo, J., Ohba, Y., Tagami, K., Sumitani, K., Yamaguchi, K. and Tsuji, T. (1996). Concanamycin B, a vacuolar H(+)-ATPase specific inhibitor suppresses bone resorption in vitro. Biol. Pharm. Bull. 19, 297-299.
131. Yost, H. J. (1991). Development of the left-right axis in amphibians. Ciba Found. Symp. 162, 165-176.
132. Yost, H. J. (2001). Establishment of left-right asymmetry. Int. Rev. Cytol. 203, 357-381.
133. Zobel, C., Cho, H. C., Nguyen, T. T. Pekhletski, R., Diaz, R. J., Wilson, G. J. and Backx, P. H. (2003). 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. 550, 365-372.