Zebrafish (Danio rerio) endomembrane antiporter similar to a yeast Cation/H+ transporter is required for neural crest development

Biochemistry

Volumn 49, Issue 31, 2010, Pages 6557-6566

  Manohar, Murli ^a,c   Mei, Hui ^a   Franklin, Andrew J ^d   Sweet, Elly M ^a   Shigaki, Toshiro ^c   Riley, Bruce B ^a   MacDiarmid, Colin W ^b   Hirschi, Kendal ^a,c  

^a TEXAS A AND M UNIVERSITY   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

^d WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIPORTS; BIOCHEMICAL CHARACTERIZATION; DANIO RERIO; ENDOMEMBRANE COMPARTMENTS; GROWTH AND DEVELOPMENT; INTEGRAL MEMBRANE PROTEINS; MUTANT CELLS; NEURAL CREST CELLS; NEURAL CRESTS; PH-SENSITIVITY; YEAST CELL; ZEBRAFISH; ZEBRAFISH EMBRYOS;

BIOLOGICAL MEMBRANES; CALCIUM; DEFECTS; YEAST;

PROTEINS;

ANTIPORTER; CATION TRANSPORT PROTEIN; TRANSCRIPTION FACTOR PAX7;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; EMBRYO DEVELOPMENT; GROWTH; HUMAN; HUMAN CELL; JAW; MUTATION; NEURAL CREST; NONHUMAN; NUCLEOTIDE SEQUENCE; PH; PIGMENTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; YEAST; ZEBRA FISH;

ANIMALS; ANTIPORTERS; CATION TRANSPORT PROTEINS; EMBRYO, NONMAMMALIAN; FUNGAL PROTEINS; HYDROGEN-ION CONCENTRATION; INTRACELLULAR MEMBRANES; MEMBRANE TRANSPORT PROTEINS; NEURAL CREST; SACCHAROMYCES CEREVISIAE PROTEINS; SODIUM-HYDROGEN ANTIPORTER; ZEBRAFISH; ZEBRAFISH PROTEINS;

ANIMALIA; DANIO RERIO; VERTEBRATA;

EID: 77955239402     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi100362k     Document Type: Article

References (66)

1. Ashworth, R. and Brennan, C. (2005) Use of transgenic zebrafish reporter lines to study calcium signalling in development Briefings Funct. Genomics Proteomics 4, 186-193
2. Blader, P. and Strahle, U. (2000) Zebrafish developmental genetics and central nervous system development Hum. Mol. Genet. 9, 945-951
3. Creton, R. (2004) The calcium pump of the endoplasmic reticulum plays a role in midline signaling during early zebrafish development Brain Res. Dev. Brain Res. 151, 33-41
4. 2+ ATPases J. Cell Biol. 124, 351-363
5. Cheng, N. H., Pittman, J. K., Barkla, B. J., Shigaki, T., and Hirschi, K. D. (2003) The Arabidopsis cax1 mutant exhibits impaired ion homeostasis, development, and hormonal responses and reveals interplay among vacuolar transporters Plant Cell 15, 347-364
6. +-ATPase activity Planta 227, 659-669
7. + exchanger are involved in the transport and selection of cations J. Biol. Chem. 279, 812-819
8. Shigaki, T., Rees, I., Nakhleh, L., and Hirschi, K. D. (2006) Identification of three distinct phylogenetic groups of CAX cation/proton antiporters J. Mol. Evol. 63, 815-825
9. + antiporter-deficient strains by the overexpressed gene J. Biol. Chem. 268, 11296-11303
10. Ohyama, T., Igarashi, K., and Kobayashi, H. (1994) Physiological role of the chaA gene in sodium and calcium circulations at a high pH in Escherichia coli J. Bacteriol. 176, 4311-4315
11. 2+ levels in S. cerevisiae FEBS Lett. 451, 132-136
12. 2+-ATPase FEBS Lett. 454, 181-186
13. 2+ in E. coli Biochim. Biophys. Acta 1778, 1415-1422
14. + antiporter of Saccharomyces cerevisiae J. Biol. Chem. 282, 24284-24293
15. 2+ exchanger superfamily: phylogenetic analysis and structural implications Mol. Biol. Evol. 21, 1692-1703
16. Berridge, M. J. (2004) Calcium signal transduction and cellular control mechanisms Biochim. Biophys. Acta 174, 3-7
17. Lamason, R. L., Mohideen, M. A., Mest, J. R., Wong, A. C., Norton, H. L., Aros, M. C., Jurynec, M. J., Mao, X., Humphreville, V. R., Humbert, J. E., Sinha, S., Moore, J. L., Jagadeeswaran, P., Zhao, W., Ning, G., Makalowska, I., McKeigue, P. M., O'Donnell, D., Kittles, R., Parra, E. J., Mangini, N. J., Grunwald, D. J., Shriver, M. D., Canfield, V. A., and Cheng, K. C. (2005) 2005 SLC24A5, a putative cation exchanger, affects pigmentation in zebrafish and humans Science 310, 1782-1786
18. 2+ signaling and early embryonic patterning during the blastula and gastrula periods of zebrafish and Xenopus development Biochim. Biophys. Acta 1763, 1192-1208
19. Bouvard, D. and Block, M. R. (1998) Calcium/calmodulin-dependent protein kinase II controls integrin alpha5beta1-mediated cell adhesion through the integrin cytoplasmic domain associated protein-1alpha Biochem. Biophys. Res. Commun. 252, 46-50
20. Price, L. S., Langeslag, M., ten Klooster, J. P., Hordijk, P. L., Jalink, K., and Collard, J. G. (2003) Calcium signaling regulates translocation and activation of Rac J. Biol. Chem. 278, 39413-39421
21. Jin, S. W., Beis, D., Mitchell, T., Chen, J. N., and Stainier, D. Y. (2005) Cellular and molecular analyses of vascular tube and lumen formation in zebrafish Development 132, 5199-5209
22. Felsenstein, J. (1997) An alternating least squares approach to inferring phylogenies from pairwise distances Syst. Biol. 46, 101-111
23. Page, R. D. (2002) Visualizing phylogenetic trees using TreeView. Curr. Protoc. Bioinformatics Chapter 6, Unit 6.2.
24. + antiporter. Identification of an N-terminal autoinhibitory domain Plant Physiol. 127, 1020-1029
25. Eide, D. J., Clark, S., Nair, T. M., Gehl, M., Gribskov, M., Guerinot, M. L., and Harper, J. F. (2005) Characterization of the yeast ionome: a genome-wide analysis of nutrient mineral and trace element homeostasis in Saccharomyces cerevisiae Genome Biol. 6, R77
26. + exchanger in a late endosomal compartment of yeast. Implications for vacuole biogenesis J. Biol. Chem. 273, 21054-21060
27. Nathan, D. F., Vos, M. H., and Lindquist, S. (1999) Identification of SSF1, CNS1, and HCH1 as multicopy suppressors of a Saccharomyces cerevisiae Hsp90 loss-of-function mutation Proc. Natl. Acad. Sci. U.S.A. 96, 1409-1414
28. Bonneaud, N., Ozier-Kalogeropoulos, O., Li, G. Y., Labouesse, M., Minvielle-Sebastia, L., and Lacroute, F. (1991) A family of low and high copy replicative, integrative and single-stranded S. cerevisiae / E. coli shuttle vectors Yeast 7, 609-615
29. MacDiarmid, C. W., Milanick, M. A., and Eide, D. J. (2002) Biochemical properties of vacuolar zinc transport systems of Saccharomyces cerevisiae J. Biol. Chem. 277, 39187-39194
30. Sheff, M. A. and Thorn, K. S. (2004) Optimized cassettes for fluorescent protein tagging in Saccharomyces cerevisiae Yeast 21, 661-670
31. 2+ exchange and induces Ca2+ ATPases in Saccharomyces cerevisiae Mol. Cell. Biol. 16, 2226-2237
32. Longtine, M. S., McKenzie, A., 3rd, Demarini, D. J., Shah, N. G., Wach, A., Brachat, A., Philippsen, P., and Pringle, J. R. (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae Yeast 14, 953-961
33. Zhao, H. and Eide, D. (1996) The yeast ZRT1 gene encodes the zinc transporter protein of a high-affinity uptake system induced by zinc limitation Proc. Natl. Acad. Sci. U.S.A. 93, 2454-2458
34. + antiporters is important for K+ ion homeostasis in plants J. Biol. Chem. 278, 22453-22459
35. Lahner, B., Gong, J., Mahmoudian, M., Smith, E. L., Abid, K. B., Rogers, E. E., Guerinot, M. L., Harper, J. F., Ward, J. M., McIntyre, L., Schroeder, J. I., and Salt, D. E. (2003) Genomic scale profiling of nutrient and trace elements in Arabidopsis thaliana Nat. Biotechnol. 21, 1215-1221
36. +-ATPase as a feature of vacuolar H+-ATPase null mutants J. Biol. Chem. 275, 40088-40095
37. 2+-ATPase in yeast Golgi, has properties distinct from sarco/endoplasmic reticulum and plasma membrane calcium pumps J. Biol. Chem. 272, 9895-9901
38. Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B., and Schilling, T. F. (1995) Stages of embryonic development of the zebrafish Dev. Dyn. 203, 253-310
39. Nasevicius, A. and Ekker, S. C. (2000) Effective targeted gene 'knockdown' in zebrafish Nat. Genet. 26, 216-220
40. Phillips, B. T., Bolding, K., and Riley, B. B. (2001) Dev Zebrafish fgf3 and fgf8 encode redundant functions required for otic placode induction Dev. Biol. 235, 351-365
41. Robu, M. E., Larson, J. D., Nasevicius, A., Beiraghi, S., Brenner, C., Farber, S. A., and Ekker, S. C. (2007) p53 activation by knockdown technologies PLoS Genet. 3, e78
42. Solomon, K. S., Kudoh, T., Dawid, I. B., and Fritz, A. (2003) Zebrafish foxi1 mediates otic placode formation and jaw development Development 130, 929-940
43. Phillips, B. T., Kwon, H. J., Melton, C., Houghtaling, P., Fritz, A., and Riley, B. B. (2006) Zebrafish msxB, msxC and msxE function together to refine the neural-nonneural border and regulate cranial placodes and neural crest development Dev. Biol. 294, 376-390
44. Cheng, N. H., Pittman, J. K., Shigaki, T., Lachmansingh, J., LeClere, S., Lahner, B., Salt, D. E., and Hirschi, K. D. (2005) Functional association of Arabidopsis CAX1 and CAX3 is required for normal growth and ion homeostasis Plant Physiol. 138, 2048-2060
45. + antiporter CAX1 J. Exp. Bot. 58, 3419-3427
46. Li, W. and Cornell, R. A. (2007) Redundant activities of Tfap2a and Tfap2c are required for neural crest induction and development of other non-neural ectoderm derivatives in zebrafish embryos Dev. Biol. 304, 338-354
47. Lacosta, A. M., Canudas, J., Gonzalez, C., Muniesa, P., Sarasa, M., and Dominguez, L. (2007) Pax7 identifies neural crest, chromatophore lineages and pigment stem cells during zebrafish development Int J. Dev. Biol. 51, 327-331
48. 2+ release in yeast is triggered by hypertonic shock and mediated by a TRP channel homologue J. Cell Biol. 156, 29-34
49. 2+ in the yeast endoplasmic reticulum reaches only 10 microM and is mainly controlled by the secretory pathway pump pmr1 EMBO J. 18, 4733-4743
50. 2+ ATPase family Cell 58, 133-145
51. 2+-ATPase homologue, PMR1, is required for normal Golgi function and localizes in a novel Golgi-like distribution Mol. Biol. Cell 3, 633-65
52. Wehrle-Haller, B., Meller, M., and Weston, J. A. (2001) Analysis of melanocyte precursors in Nf1 mutants reveals that MGF/KIT signaling promotes directed cell migration independent of its function in cell survival Dev. Biol. 232, 471-483
53. 2+-dependent and cAMP-dependent signaling pathways affect neurogenesis and melanogenesis of quail neural crest cells in vitro Dev. Genes Evol. 214, 193-199
54. 2+, downstream protein kinases, and oscillatory signaling in regulating fertilization and the activation of development Dev. Biol. 315, 257-279
55. Ebert, A. M., Hume, G. L., Warren, K. S., Cook, N. P., Burns, C. G., Mohideen, M. A., Siegal, G., Yelon, D., Fishman, M. C., and Garrity, D. M. (2005) Calcium extrusion is critical for cardiac morphogenesis and rhythm in embryonic zebrafish hearts Proc. Natl. Acad. Sci. U.S.A. 102, 17705-17710
56. Kreiling, J. A., Balantac, Z. L., Crawford, A. R., Ren, Y., Toure, J., Zchut, S., Kochilas, L., and Creton, R. (2008) Suppression of the endoplasmic reticulum calcium pump during zebrafish gastrulation affects left-right asymmetry of the heart and brain Mech. Dev. 125, 396-410
57. Ouyang, M., Garnett, A. T., Han, T. M., Hama, K., Lee, A., Deng, Y., Lee, N., Liu, H. Y., Amacher, S. L., Farber, S. A., and Ho, S. Y. (2008) A web based resource characterizing the zebrafish developmental profile of over 16,000 transcripts Gene Expr. Patterns 8, 171-180
58. Kimmel, C. B., Miller, C. T., Kruze, G., Ullmann, B., BreMiller, R. A., Larison, K. D., and Snyder, H. C. (1998) The shaping of pharyngeal cartilages during early development of the zebrafish Dev. Biol. 203, 245-263
59. Cramer, H., Schmenger, K., Heinrich, K., Horstmeyer, A., Böning, H., Breit, A., Piiper, A., Lundstrom, K., Müller-Esterl, W., and Schroeder, C. (2001) Coupling of endothelin receptors to the ERK/MAP kinase pathway. Roles of palmitoylation and Galphaq Eur. J. Biochem. 268, 5449-5459
60. Van Raamsdonk, C. D., Fitch, K. R., Fuchs, H., de Angelis, M. H., and Barsh, G. S. (2004) Effects of G-protein mutations on skin color Nat. Genet. 36, 961-968
61. McNeill, M. S., Paulsen, J., Bonde, G., Burnight, E., Hsu, M. Y., and Cornell, R. A. (2007) Cell death of melanophores in zebrafish trpm7 mutant embryos depends on melanin synthesis J. Invest. Dermatol. 127, 2020-2030
62. Wei, C., Wang, X., Chen, M., Ouyang, K., Song, L. S., and Cheng, H. (2009) Calcium flickers steer cell migration Nature 457, 901-905
63. Elizondo, M. R., Arduini, B. L., Paulsen, J., MacDonald, E. L., Sabel, J. L., Henion, P. D., Cornell, R. A., and Parichy, D. M. (2005) Defective skeletogenesis with kidney stone formation in dwarf zebrafish mutant for trpm7 Curr. Biol. 15, 667-671
64. Dickens, C. J., Gillespie, J. I., and Greenwell, J. R. (1990) Measurement of intracellular calcium and pH in avian neural crest cells J. Physiol. 428, 531-544
65. Watabe, H., Valencia, J. C., Yasumoto, K., Kushimoto, T., Ando, H., Muller, J., Vieira, W. D., Mizoguchi, M., Appella, E., and Hearing, V. J. (2004) Regulation of tyrosinase processing and trafficking by organellar pH and by proteasome activity J. Biol. Chem. 279, 7971-7981
66. + exchanger expression and tyrosinase activity in human melanocytes Exp. Cell Res. 298, 521-534