Multiple roles for the Na,K-ATPase subunits, Atp1a1 and Fxyd1, during brain ventricle development

Developmental Biology

Volumn 368, Issue 2, 2012, Pages 312-322

  Chang, Jessica T ^a,b   Lowery, Laura Anne ^a,b,c   Sive, Hazel ^a,b  

^a WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Atp1a1; Brain ventricles; Fxyd1; Na,K ATPase; Neuroepithelium; Permeability

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ATP1A1 PROTEIN; FXYD1 PROTEIN; OUABAIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SODIUM; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BRAIN VENTRICLE; BRAIN VENTRICLE DEVELOPMENT; CEREBROSPINAL FLUID; EMBRYO; NEUROEPITHELIAL PERMEABILITY; NEUROEPITHELIUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SODIUM CELL LEVEL;

STROPHANTHUS GRATUS; VERTEBRATA;

EID: 84864038649     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2012.05.034     Document Type: Article

References (56)

1. Amano M., Fukata Y., Kaibuchi K. Regulation and functions of Rho-associated kinase. Exp. Cell Res. 2000, 261:44-51.
2. Bagnat M., Cheung I.D., Mostov K.E., Stainier D.Y. Genetic control of single lumen formation in the zebrafish gut. Nat. Cell Biol. 2007, 9:954-960.
3. Bibert S., Roy S., Schaer D., Horisberger J.D., Geering K. Phosphorylation of phospholemman (FXYD1) by protein kinases A and C modulates distinct Na,K-ATPase isozymes. J. Biol. Chem. 2008, 283:476-486.
4. Bossuyt J., Despa S., Martin J.L., Bers D.M. Phospholemman phosphorylation alters its fluorescence resonance energy transfer with the Na,K-ATPase pump. J. Biol. Chem. 2006, 281:32765-32773.
5. Brown P.D., Davies S.L., Speake T., Millar I.D. Molecular mechanisms of cerebrospinal fluid production. Neuroscience 2004, 129:957-970.
6. Canfield V.A., Loppin B., Thisse B., Thisse C., Postlethwait J.H., Mohideen M.A., Rajarao S.J., Levenson R. Na,K-ATPase alpha and beta subunit genes exhibit unique expression patterns during zebrafish embryogenesis. Mech. Dev. 2002, 116:51-59.
7. Cibrian-Uhalte E., Langenbacher A., Shu X., Chen J.N., Abdelilah-Seyfried S. Involvement of zebrafish Na+, K+ ATPase in myocardial cell junction maintenance. J. Cell Biol. 2007, 176:223-230.
8. Ciruna B., Jenny A., Lee D., Mlodzik M., Schier A.F. Planar cell polarity signalling couples cell division and morphogenesis during neurulation. Nature 2006, 439:220-224.
9. Crambert G., Fuzesi M., Garty H., Karlish S., Geering K. Phospholemman (FXYD1) associates with Na,K-ATPase and regulates its transport properties. Proc. Nat. acad. Sci. U.S.A. 2002, 99:11476-11481.
10. Dahl J.P., Binda A., Canfield V.A., Levenson R. Participation of Na,K-ATPase in FGF-2 secretion: rescue of ouabain-inhibitable FGF-2 secretion by ouabain-resistant Na,K-ATPase alpha subunits. Biochem. 2000, 39:14877-14883.
11. Desmond M.E., Levitan M.L., Haas A.R. Internal luminal pressure during early chick embryonic brain growth: descriptive and empirical observations. Anat. Rec. A. Discov. Mol. Cell. Evol. Biol. 2005, 285:737-747.
12. Draper B.W., Morcos P.A., Kimmel C.B. Inhibition of zebrafish fgf8 pre-mRNA splicing with morpholino oligos: a quantifiable method for gene knockdown. Genesis 2001, 30:154-156.
13. 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.
14. Feschenko M.S., Donnet C., Wetzel R.K., Asinovski N.K., Jones L.R., Sweadner K.J. Phospholemman, a single-span membrane protein, is an accessory protein of Na,K-ATPase in cerebellum and choroid plexus. J. Neurosci. 2003, 23:2161-2169.
15. Gato A., Moro J.A., Alonso M.I., Bueno D., De La Mano A., Martin C. Embryonic cerebrospinal fluid regulates neuroepithelial survival, proliferation, and neurogenesis in chick embryos. Anat. Rec. A. Discov. Mol. Cell. Evol. Biol. 2005, 284:475-484.
16. Geering K. The functional role of beta subunits in oligomeric P-type ATPases. J. Bioenerg. Biomembr. 2001, 33:425-438.
17. Geering K. FXYD proteins: new regulators of Na-K-ATPase. American J. Physiol. Renal Physiol. 2006, 290:F241-F250.
18. Graeden, E., Sive, H., 2009. Live imaging of the zebrafish embryonic brain by confocal microscopy. J. Visualized Exp. (26), e1217. http://dx.doi.org/10.3791/1217.
19. Gutzman, J.H., Sive, H., 2009. Zebrafish brain ventricle injection. J. Visualized Exp. (26), e1218. http://dx.doi.org/10.3791/1218.
20. Gutzman J.H., Sive H. Epithelial relaxation mediated by the myosin phosphatase regulator Mypt1 is required for brain ventricle lumen expansion and hindbrain morphogenesis. Development 2010, 137:795-804.
21. Hong E., Brewster R. N-cadherin is required for the polarized cell behaviors that drive neurulation in the zebrafish. Development 2006, 133:3895-3905.
22. Jia L.G., Donnet C., Bogaev R.C., Blatt R.J., McKinney C.E., Day K.H., Berr S.S., Jones L.R., Moorman J.R., Sweadner K.J., Tucker A.L. Hypertrophy, increased ejection fraction, and reduced Na-K-ATPase activity in phospholemman-deficient mice. Am. J. Physiol.-Heart Circ. Physiol. 2005, 288:H1982-H1988.
23. Jiang Y.J., Brand M., Heisenberg C.P., Beuchle D., Furutani-Seiki M., Kelsh R.N., Warga R.M., Granato M., Haffter P., Hammerschmidt M., Kane D.A., Mullins M.C., Odenthal J., van Eeden F.J., Nusslein-Volhard C. Mutations affecting neurogenesis and brain morphology in the zebrafish, Danio rerio. Development 1996, 123:205-216.
24. Kimmel C.B., Ballard W.W., Kimmel S.R., Ullmann B., Schilling T.F. Stages of embryonic development of the zebrafish. Dev. Dyn. 1995, 203:253-310.
25. Knust E., Bossinger O. Composition and formation of intercellular junctions in epithelial cells. Science 2002, 298:1955-1959.
26. Krupinski T., Beitel G.J. Unexpected roles of the Na,K-ATPase and other ion transporters in cell junctions and tubulogenesis. Physiology (Bethesda) 2009, 24:192-201.
27. Lansbery K.L., Burcea L.C., Mendenhall M.L., Mercer R.W. Cytoplasmic targeting signals mediate delivery of phospholemman to the plasma membrane. Am. J. Physiol.-Cell Physiol. 2006, 290:C1275-C1286.
28. Linask K.K., Gui Y.H. Inhibitory effects of ouabain on early heart development and cardiomyogenesis in the chick embryo. Dev. Dyn. 1995, 203:93-105.
29. Lowery L.A., De Rienzo G., Gutzman J.H., Sive H. Characterization and classification of zebrafish brain morphology mutants. Anat. Rec. (Hoboken) 2009, 292:94-106.
30. Lowery L.A., Sive H. Initial formation of zebrafish brain ventricles occurs independently of circulation and requires the nagie oko and snakehead/atp1a1a.1 gene products. Development 2005, 132:2057-2067.
31. Lowery L.A., Sive H. Totally tubular: the mystery behind function and origin of the brain ventricular system. Bioessays 2009, 31:446-458.
32. Mishra N.K., Peleg Y., Cirri E., Belogus T., Lifshitz Y., Voelker D.R., Apell H.J., Garty H., Karlish S.J. FXYD proteins stabilize Na,K-ATPase: amplification of specific phosphatidylserine-protein interactions. J. Biol. Chem. 2011, 286:9699-9712.
33. Morth J.P., Pedersen B.P., Toustrup-Jensen M.S., Sorensen T.L., Petersen J., Andersen J.P., Vilsen B., Nissen P. Crystal structure of the sodium-potassium pump. Nature 2007, 450:1043-1049.
34. Nasevicius A., Ekker S.C. Effective targeted gene 'knockdown' in zebrafish. Nat. Genet. 2000, 26:216-220.
35. Oshio K., Song Y., Verkman A.S., Manley G.T. Aquaporin-1 deletion reduces osmotic water permeability and cerebrospinal fluid production. Acta. Neurochir. Suppl. 2003, 86:525-528.
36. Paul S.M., Palladino M.J., Beitel G.J. A pump-independent function of the Na,K-ATPase is required for epithelial junction function and tracheal tube-size control. Development 2007, 134:147-155.
37. Pavlovic D., Fuller W., Shattock M.J. The intracellular region of FXYD1 is sufficient to regulate cardiac Na,K-ATPase. FASEB J. 2007, 21:1539-1546.
38. Pollay M., Hisey B., Reynolds E., Tomkins P., Stevens F.A., Smith R. Choroid plexus Na+/K+-activated adenosine triphosphatase and cerebrospinal fluid formation. Neurosurgery 1985, 17:768-772.
39. Rajasekaran S.A., Barwe S.P., Gopal J., Ryazantsev S., Schneeberger E.E., Rajasekaran A.K. Na,K-ATPase regulates tight junction permeability through occludin phosphorylation in pancreatic epithelial cells. Am. Physiol. Soc.-Gastrointest. Liver Physiol. 2007, 292:G124-G133.
40. Rajasekaran S.A., Palmer L.G., Moon S.Y., Peralta Soler A., Apodaca G.L., Harper J.F., Zheng Y., Rajasekaran A.K. Na,K-ATPase activity is required for formation of tight junctions, desmosomes, and induction of polarity in epithelial cells. Mol. Biol. Cell 2001, 12:3717-3732.
41. Sagerstrom C.G., Grinbalt Y., Sive H. Anteroposterior patterning in the zebrafish, Danio rerio: an explant assay reveals inductive and suppressive cell interactions. Development 1996, 122:1873-1883.
42. Shinoda T., Ogawa H., Cornelius F., Toyoshima C. Crystal structure of the sodium-potassium pump at 2.4A resolution. Nat. 2009, 459:446-450.
43. Shu X., Cheng K., Patel N., Chen F., Joseph E., Tsai H.J., Chen J.N. Na,K-ATPase is essential for embryonic heart development in the zebrafish. Development 2003, 130:6165-6173.
44. Speake T., Whitwell C., Kajita H., Majid A., Brown P.D. Mechanisms of CSF secretion by the choroid plexus. Microsc. Res. Tech. 2001, 52:49-59.
45. Sweadner K.J., Rael E. The FXYD gene family of small ion transport regulators or channels: cDNA sequence, protein signature sequence, and expression. Genomics 2000, 68:41-56.
46. Szaszi K., Sirokmany G., Di Ciano-Oliveira C., Rotstein O.D., Kapus A. Depolarization induces Rho-Rho kinase-mediated myosin light chain phosphorylation in kidney tubular cells. Am. J. Physiol.-Cell Physiol. 2005, 289:C673-C685.
47. Terry S., Nie M., Matter K., Balda M.S. Rho signaling and tight junction functions. Physiology (Bethesda) 2010, 25:16-26.
48. Ulitsky I., Shkumatava A., Jan C.H., Sive H., Bartel D.P. Conserved function of lincRNAs in vertebrate embryonic development despite rapid sequence evolution. Cell 2011, 147:1537-1550.
49. Waheed F., Speight P., Kawai G., Dan Q., Kapus A., Szaszi K. Extracellular signal-regulated kinase and GEF-H1 mediate depolarization-induced Rho activation and paracellular permeability increase. Am. J. Physiol.-Cell Physiol. 2010, 298:C1376-C1387.
50. Welss P. Secretory activity of the inner layer of the embryonic mid-brain of the chick, as revealed by tissue culture. The Anatomical Record 1934, 58:299-302.
51. Westerfield M., Sprague J., Doerry E., Douglas S., Grp Z. The Zebrafish Information Network (ZFIN): a resource for genetic, genomic and developmental research. Nucleic Acids Res. 2001, 29:87-90.
52. Wilson P.D., Devuyst O., Li X., Gatti L., Falkenstein D., Robinson S., Fambrough D., Burrow C.R Apical plasma membrane mispolarization of NaK-ATPase in polycystic kidney disease epithelia is associated with aberrant expression of the beta2 isoform. Am. J. Pathol. 2000, 156:253-268.
53. Yamamoto M., Ramirez S.H., Sato S., Kiyota T., Cerny R.L., Kaibuchi K., Persidsky Y., Ikezu T. Phosphorylation of claudin-5 and occludin by rho kinase in brain endothelial cells. Am. J. Pathol. 2008, 172:521-533.
54. Yuan S., Joseph E.M. The small heart mutation reveals novel roles of Na+/K+-ATPase in maintaining ventricular cardiomyocyte morphology and viability in zebrafish. Circ. Res. 2004, 95:595-603.
55. Zhang J., Piontek J., Wolburg H., Piehl C., Liss M., Otten C., Christ A., Willnow T.E., Blasig I.E., Abdelilah-Seyfried S. Establishment of a neuroepithelial barrier by Claudin5a is essential for zebrafish brain ventricular lumen expansion. Proc. Nat. acad. Sci. U.S.A. 2010, 107:1425-1430.
56. Zhang X.Q., Qureshi A., Song J., Carl L.L., Tian Q., Stahl R.C., Carey D.J., Rothblum L.I., Cheung J.Y. Phospholemman modulates Na+/Ca2+ exchange in adult rat cardiac myocytes. Am. J. Physiol.-Heart Circ. Physiol. 2003, 284:H225-H233.