V-ATPase-dependent ectodermal voltage and Ph regionalization are required for craniofacial morphogenesis

Developmental Dynamics

Volumn 240, Issue 8, 2011, Pages 1889-1904

  Vandenberg, Laura N ^a   Morrie, Ryan D ^a   Adams, Dany Spencer ^a  

^a TUFTS UNIVERSITY   (United States)

Author keywords

Bioelectric signaling; Cranial neural crest; Craniofacial development; Ductin; Neurectoderm; Placodes; V ATPase

Indexed keywords

ADENOSINE TRIPHOSPHATASE; HYDROGEN; MICROPHTHALMIA ASSOCIATED TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR OTX2; TRANSCRIPTION FACTOR PAX6; TRANSCRIPTION FACTOR PAX8; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SOX9; XENOPUS PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; BIOENERGY; CONTROLLED STUDY; CRANIOFACIAL DEVELOPMENT; CRANIOFACIAL MALFORMATION; CRANIOFACIAL MORPHOLOGY; DEPOLARIZATION; EMBRYO; GASTRULA; GENE EXPRESSION; HYPERPOLARIZATION; MEMBRANE POTENTIAL; MORPHOGENESIS; NONHUMAN; PH; PRIORITY JOURNAL; PROTON TRANSPORT; REGIONALIZATION; XENOPUS;

AMINO ACID SEQUENCE; ANIMALS; CRANIOFACIAL ABNORMALITIES; ECTODERM; EMBRYONIC INDUCTION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; HYDROGEN-ION CONCENTRATION; MEMBRANE POTENTIALS; MOLECULAR SEQUENCE DATA; MORPHOGENESIS; PROTEOLIPIDS; SEQUENCE ALIGNMENT; SKULL; VACUOLAR PROTON-TRANSLOCATING ATPASES; XENOPUS LAEVIS; XENOPUS PROTEINS;

EID: 79960379493     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.22685     Document Type: Article

References (73)

1. Adams DS. 2008. A new tool for tissue engineers: ions as regulators of morphogenesis during development and regeneration. Tissue Eng Part A 14: 1461-1468.
2. +-V-ATPase-dependent proton flux is necessary for consistent left-right patterning of non-mammalian vertebrates. Development 133: 1657-1671.
3. + pump-dependent changes in membrane voltage are an early mechanism necessary and sufficient to induce Xenopus tail regeneration. Development 134: 1323-1335.
4. +)-ATPase mutants transform cells and define a binding site for the papillomavirus E5 oncoprotein. J Biol Chem 270: 6830-6837.
5. Blackiston DJ, McLaughlin KA, Levin M. 2009. Bioelectric controls of cell proliferation: Ion channels, membrane voltage and the cell cycle. Cell Cycle 8: 1-10.
6. Blackiston D, Adams DS, Lemire JM, Lobikin M, 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.
7. Blasiole B, Canfield VA, Vollrath MA, Huss D, Mohideen MA, Dickman JD, Cheng KC, Fekete DM, Levenson R. 2006 Separate Na, K-ATPase genes are required for otolith formation and semicircular canal development in zebrafish. Dev Biol 294: 148-160.
8. Bowes JB, Snyder KA, Segerdell E, Jarabek CJ, Azam K, Zorn AM, Vize PD. 2010. Xenbase: gene expression and improved integration. Nucleic Acids Res 38: D607-D612.
9. +-ATPase of neurospora crassa, suppress inhibition of growth by concanamycin A, a specific inhibitor of vacuolar ATPases. J Biol Chem 272: 14776-14786.
10. Brugmann SA, Moody SA. 2005. Induction and specification of the vertebrate ectodermal placodes: precursors of the cranial sensory organs. Biol Cell 97: 303-319.
11. Carl TF, Dufton C, Hanken J, Klymkowsky MW. 1999. Inhibition of neural crest migration in Xenopus using antisense slug RNA. Dev Biol 213: 101-115.
12. Coombs GS, Yu J, Canning CA, Velt CA, Covey TM, Cheong JK, Utom V, Banerj N, Zhang ZH, Jadulco RC, Concepcion GP, Bugni TS, Harper MK, Mihalek I, Jones CM, Ireland CM, Virshup DM. 2010. WLS-dependent secretion of WNT3A requires Ser209 acylation and vacuolar acidification. J Cell Science 123: 3357-3367
13. +-ATPase-mediated acidification for Wnt signaling. Science 327: 459-463.
14. Cruz S, Shiao JC, Liao BK, Huang CJ, Hwang PP. 2009. Plasma membrane calcium ATPase required for semicircular canal formation and otolith growth in the zebrafish inner ear. J Exp Biol 212: 639-647.
15. Davidson EH. 1993. Later embryogenesis: regulatory circuitry in morphogenetic fields. Development 118: 665-690.
16. Deardorff MA, Tan C, Saint-Jeannet JP, Klein PS. 2001. A role for frizzled 3 in neural crest development. Development 128: 3655-3663.
17. Disbrow GL, Hanover JA, Schlegel R. 2005. Endoplasmic reticulum-localized human papillomavirus type 16 E5 protein alters endosomal pH but not trans-golgi pH. J Virol 79: 5839-5846.
18. Ducibella T, Schultz RM, Ozil JP. 2006. Role of calcium signals in early development. Semin Cell Dev Biol 17: 324-332.
19. Fagotto F. 1995. Regulation of yolk degradation, or how to make sleepy lysosomes. J Cell Sci 108: 3645-3647.
20. Fagotto F, Maxfield FR. 1994. Changes in yolk platelet pH during Xenopus laevis development correlate with yolk utilization. A quantitative confocal microscopy study. J Cell Sci 107: 3325-3337.
21. Finbow M, Pitts J, Goldstein D, Schlegel R, Findlay J. 1991. The E5 oncoprotein target: a 16-kDa channel-forming protein with diverse functions. Mol Carcinog: 441-444.
22. Gammill LS, Sive H. 2001. Otx2 expression in the ectoderm activates anterior neural determination and is required for Xenopus cement gland formation. Dev Biol 240: 223-236.
23. George A, Leahy H, Zhou J, Morin PJ. 2007. The vacuolar-ATPase inhibitor bafilomycin and mutant vps35 inhibit canonical wnt signaling. Neurobiol Dis 26: 125-133.
24. Goldstein DJ, Finbow ME, Andresson T, McLean P, Smith K, Bubb V, Schlegel R. 1991. Bovine papillomavirus E5 oncoprotein binds to the 16k component of vacuolar H(+)-ATPases. Nature 352: 347-349.
25. Hanken J, Gross JB. 2005. Evolution of cranial development and the role of neural crest: insights from amphibians. J Anat 207: 437-446.
26. Harland RM. 1991. In situ hybridization: An improved whole mount method for Xenopus embryos. In: Kay BK, Peng HB, editors. Xenopus laevis: Practical Uses in Cell and Molecular Biology, vol. 36. San Diego: Academic Press. p 685-695.
27. Hermle T, Saltukoglu D, Grunewald J, Walz G, Simons M. 2010. Regulation of frizzled-dependent planar polarity signaling by a V-ATPase subunit. Curr Biol 20: 1269-1276.
28. Hinton A, Bond S, Forgac M. 2009. V-ATPase functions in normal and disease processes. Pflugers Arch 457: 589-598.
29. Hirsch N, Harris WA. 1997. Xenopus pax6 and retinal development. J Neurobiol 32: 45-61.
30. Ingber DE. 2006. Mechanical control of tissue morphogenesis during embryological development. Int J Dev Biol 50: 255-266.
31. + transport proteins in the developing cochlear lateral wall of guinea pigs with hereditary deafness. Eur J Neurosci 27: 145-154.
32. Jorgensen P, Steen JA, Steen H, Kirschner MW. 2009. The mechanism and pattern of yolk consumption provide insight into embryonic nutrition in Xenopus. Development 136: 1539-1548.
33. Jouhou H, Yamamoto K, Homma A, Hara M, Kaneko A, Yamada M. 2007. Depolarization of isolated horizontal cells of fish acidifies their immediate surrounding by activating V-ATPase. J Physiol 585: 401-412.
34. Koestner U, Shnitsar I, Linnemannstons K, Hufton AL, Borchers A. 2008 Semaphorin and neuropilin expression during early morphogenesis of Xenopus laevis. Dev Dyn 237: 3853-3863.
35. Kumasaka M, Sato S, Yajima I, Goding CR, Yamamoto H. 2005. Regulation of melanoblast and retinal pigment epithelium development by Xenopus laevis mitf. Dev Dyn 234: 523-534.
36. Lecuit T. 2008. Developmental mechanics: Cellular patterns controlled by adhesion, cortical tension and cell division. HFSP J 2: 72-78.
37. +-ATPase 16-kDa subunit results in the triton x-100-insoluble aggregation of beta1 integrin and reduction of its cell surface expression. J Biol Chem 279: 53007-53014.
38. Levin M. 2007a. Gap junctional communication in morphogenesis. Prog Biophys Mol Biol 94: 186-206.
39. Levin M. 2007b. Large-scale biophysics: Ion flows and regeneration. Trends Cell Biol 17: 261-270.
40. Levin M. 2009. Bioelectric mechanisms in regeneration: unique aspects and future perspectives. Semin Cell Dev Biol 20: 543-556.
41. Linker C, Bronner-Fraser M, Mayor R. 2000. Relationship between gene expression domains of xsnail, xslug, and xtwist and cell movement in the prospective neural crest of Xenopus. Dev Biol 224: 215-225.
42. +-ATPase is a dominant negative mutant and is sequestered in endoplasmic reticulum derived structures. Biochem Cell Biol 78: 51-58.
43. McCabe KL, Bronner-Fraser M. 2009. Molecular and tissue interactions governing induction of cranial ectodermal placodes. Dev Biol 332: 189-195.
44. McCaig CD, Rajnicek AM, Song B, Zhao M. 2005. Controlling cell behavior electrically: current views and future potential. Physiol Rev 85: 943-978.
45. Morokuma J, Blackiston D, Adams DS, Seebohm G, Trimmer B, Levin M. 2008a. Modulation of potassium channel function confers a hyperproliferative invasive phenotype on embryonic stem cells. Proc Natl Acad Sci USA 105: 16608-16613.
46. + channel components are involved in early left-right patterning in Xenopus laevis embryos. Cell Physiol Biochem 21: 357-372.
47. Nieuwkoop PD, Faber J. 1967. Normal table of Xenopus laevis (daudin). Amsterdam: North-Holland Publishing Company.
48. +-ATPASES: nature's most versatile proton pumps. Nat Rev Mol Cell Biol 3: 94-103.
49. Pannese M, Polo C, Andreazzoli M, Vignali R, Kablar B, Barsacchi G, Boncinelli E. 1995. The Xenopus homologue of otx2 is a maternal homeobox gene that demarcates and specifies anterior body regions. Development 121: 707-720.
50. Praetorius J, Andreasen D, Jensen BL, Ainsworth MA, Friis UG, Johansen T. 2000. NHE1, NHE2, and NHE3 contribute to regulation of intracellular pH in murine duodenal epithelial cells. Am J Physiol 278: G197-206.
51. Purcell P, Oliver G, Mardon G, Donner AL, Maas RL. 2005. Pax6-dependence of six3, eya1 and dach1 expression during lens and nasal placode induction. Gene Expr Patterns 6: 110-118.
52. Rasmussen JT, Deardorff MA, Tan C, Rao MS, Klein PS, Vetter ML. 2001. Regulation of eye development by frizzled signaling in Xenopus. Proc Natl Acad Sci USA 98: 3861-3866.
53. Saint-Germain N, Lee YH, Zhang Y, Sargent TD, Saint-Jeannet JP. 2004. Specification of the otic placode depends on sox9 function in Xenopus. Development 131: 1755-1763.
54. +-ATPase (ductin) is accompanied by down-regulation of gap junctional intercellular communication and translocation of connexin 43 in NIH3T3 cells. Oncogene 17: 1673-1680.
55. Sauka-Spengler T, Bronner-Fraser M. 2008. A gene regulatory network orchestrates neural crest formation. Nat Rev Mol Cell Biol 9: 557-568.
56. Sampath K, Cheng A, Frisch A, Wright C. 1997. Functional differences among Xenopus nodal-related genes in left-right axis determination. Development 124: 3293-3302.
57. Sater AK, Alderton JM, Steinhardt RA. 1994. An increase in intracellular pH during neural induction in Xenopus. Development 120: 433-442.
58. Schlosser G. 2006. Induction and specification of cranial placodes. Dev Biol 294: 303-351.
59. Schlosser G, Ahrens K. 2004 Molecular anatomy of placode development in Xenopus laevis. Dev Biol 271: 439-466.
60. Schlosser G, Northcutt RG. 2000. Development of neurogenic placodes in Xenopus laevis. J Comp Neuro l418: 121-146.
61. Semenov MV, Habas R, Macdonald BT, He X. 2007. Snapshot: Noncanonical wnt signaling pathways. Cell 131: 1378.
62. Shi DL, Goisset C, Boucaut JC. 1998. Expression of xfz3, a Xenopus frizzled family member, is restricted to the early nervous system. Mech Dev 70: 35-47.
63. Simons M, Gault WJ, Gotthardt D, Rohatgi R, Klein TJ, Shao YM, Lee HJ, Wu AL, Fang YM, Satlin LM, Dow JT, Chen J, Zheng J, Boutros M, Mlodzik M. 2009. Electrochemical cues regulate assembly of the Frizzled/Dishevelled complex at the plasma membrane during planar epithelial polarization. Nature Cell Biol 11: 286-U142
64. Sive H, Grainger RM, Harland R. 2000. Early development of Xenopus laevis. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
65. Stoppler MC, Straight SW, Tsao G, Schlegel R, McCance DJ. 1996. The E5 gene of hpv-16 enhances keratinocyte immortalization by full-length DNA. Virology 223: 251-254.
66. Sundelacruz S, Levin M, Kaplan DL. 2008. Membrane potential controls adipogenic and osteogenic differentiation of mesenchymal stem cells. PLoS One 3: e3737.
67. Sundelacruz S, Levin M, Kaplan DL. 2009. Role of membrane potential in the regulation of cell proliferation and differentiation. Stem Cell Rev Rep 5: 231-246.
68. Uzman JA, Patil S, Uzgare AR, Sater AK. 1998. The role of intracellular alkalinization in the establishment of anterior neural fate in Xenopus. Dev Biol 193: 10-20.
69. Wang H, Kesinger JW, Zhou Q, Wren JD, Martin G, Turner S, Tang Y, Frank MB, Centola M. 2008. Identification and characterization of zebrafish ocular formation genes. Genome 51: 222-235.
70. Yanfeng WA, Tan C, Fagan RJ Klein PS. 2006. Phosphorylation of frizzled-3. J Biol Chem 281: 11603-11609.
71. Zhao H, Bringas P, Chai Y. 2006. An in vitro model for characterizing the post-migratory CNC cells of the first branchial arch. Dev Dyn 235: 1433-1440.
72. Zhao Q, Ovchinnikova K, Chai B, Yoo H, Magula J, Pollack GH. 2009. Role of proton gradients in the mechanism of osmosis. J Phys Chem 113: 10708-10714.
73. Zimmerman SG, Thorpe LM, Medrano VR, Mallozzi CA, McCartney BM. 2010 Apical constriction and invagination downstream of the canonical Wnt signaling pathway requires Rho1 and Myosin II. Dev Biol 340: 54-66.