Regulated Cationic Channel Function in Xenopus Oocytes Expressing Drosophila Big Brain

Journal of Neuroscience

Volumn 22, Issue 7, 2002, Pages 2530-2540

  Yanochko, Gina M ^a,b   Yool, Andrea J ^a  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

Aquaporin; Major intrinsic protein; Neurogenic; Tyrosine kinase; Voltage clamp; Xenopus oocyte

Indexed keywords

AMINO ACID; BIG BRAIN PROTEIN; CATION CHANNEL; INSULIN; LAVENDUSTIN A; MEMBRANE PROTEIN; MUTANT PROTEIN; POTASSIUM ION; PROTEIN TYROSINE KINASE INHIBITOR; SODIUM ION; TETRYLAMMONIUM; UNCLASSIFIED DRUG; BIG BRAIN PROTEIN, DROSOPHILA; CATION; COMPLEMENTARY RNA; DROSOPHILA PROTEIN; ENZYME INHIBITOR; ION CHANNEL; WATER;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DROSOPHILA; ELECTRIC POTENTIAL; FEMALE; GENE DELETION; GENE EXPRESSION; ION CONDUCTANCE; ION PERMEABILITY; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; XENOPUS; ANIMAL; CELL MEMBRANE PERMEABILITY; CELL MEMBRANE POTENTIAL; CYTOLOGY; DOSE RESPONSE; DRUG EFFECT; GENETIC TRANSFECTION; GENETICS; ION TRANSPORT; METABOLISM; MICROINJECTION; OSMOLARITY; PATCH CLAMP; PHOSPHORYLATION; PHYSIOLOGY; SITE DIRECTED MUTAGENESIS; STRUCTURE ACTIVITY RELATION;

ANIMALS; CATIONS; CELL MEMBRANE PERMEABILITY; DOSE-RESPONSE RELATIONSHIP, DRUG; DROSOPHILA; DROSOPHILA PROTEINS; ENZYME INHIBITORS; GENE EXPRESSION; INSULIN; ION CHANNELS; ION TRANSPORT; MEMBRANE POTENTIALS; MEMBRANE PROTEINS; MICROINJECTIONS; MUTAGENESIS, SITE-DIRECTED; OOCYTES; OSMOLAR CONCENTRATION; PATCH-CLAMP TECHNIQUES; PHOSPHORYLATION; RNA, COMPLEMENTARY; SIGNAL TRANSDUCTION; STRUCTURE-ACTIVITY RELATIONSHIP; TRANSFECTION; WATER; XENOPUS;

EID: 0036546769     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-07-02530.2002     Document Type: Article

References (78)

1. Adams MD, Dubnick M, Kerlavage AR, Moreno R, Kelley JM, Utterback TR, Nagle JW, Fields C, Venter JC (1992) Sequence identification of 2,375 human brain genes. Nature 355:632-634.
2. Andersen CB, Roth RA, Conti M (1998) Protein kinase B/Akt induces resumption of meiosis in Xenopus oocytes. J Biol Chem 273:18705-18708.
3. Anthony TL, Brooks HL, Boassa D, Leonov S, Yanochko GM, Regan JW, Yool AJ (2000) Cloned human Aquaporin-1 is a cyclic-GMP-gated ion channel. Mol Pharmacol 57:576-588.
4. Applevard SM, McLaughlin JP, Chavkin C (2000) Tyrosine hosphorylation of the κ-opioid receptor regulates agonist efficacy. J Biol Chem 275:38281-38285.
5. Artavanis-Tsakonas S, Matsuno K, Fortini ME (1995) Notch signaling. Science 268:225-232.
6. Artavanis-Tsakonas S, Rand MD, Lake RJ (1999) Notch signaling: cell fate control and signal integration in development. Science 284:770-776.
7. Bagowski CP, Xiong W, Ferrell Jr JE (2001) c-Jun N-terminal kinase activation in Xenopus laevis eggs and embryos. J Biol Chem 276:1459-1465.
8. Bailey AM, Posakony JW (1995) Suppressor of Hairless directly activates transcription of Enhancer of split complex genes in response to Notch receptor activity. Genes Dev 9:2609-2622.
9. Brand M, Campos-Ortega JA (1988) Two groups of interrelated genes regulate early neurogenesis in Drosophila melanogaster. Wilhelm Rouxs Arch Dev Biol 197:457-470.
10. Burris PA, Zhang Y, Rusconi JC, Corbin V (1998) The pore-forming and cytoplasmic domains of the neurogenic gene product, Big Brain; are conserved between Drosophila virilis and Drosophila melanogaster. Gene 206:69-76.
11. Chen C, Jack J, Garofalo RS (1999) The Drosophila insulin receptor is required for normal growth. Endocrinology 137:846-856.
12. Chuang, L-M, Martin Jr MG, Seidner GA, Birnbaum MJ, White MF, Kahn CR (1993) Insulin receptor substrate 1 mediates insulin and insulin-like growth factor 1-stimulated maturation of Xenopus oocytes. Proc Natl Acad Sci USA 90:5172-5175.
13. Cohen GB, Ren R, Baltimore D (1995) Modular binding domains in signal transduction proteins. Cell 80:237-248.
14. de la Concha A, Dietrich U, Weigel D, Campos-Ortega JA (1988) Functional interactions of neurogenic genes of Drosophila melanogaster. Genetics 118:499-508.
15. Delidakis C, Artavanis-Tsakonas S (1992) The Enhancer of split [E(spl)] locus of Drosophila encodes seven independent helix-loop-helix proteins. Proc Natl Acad Sci USA 89:8731-8735.
16. Doherty D, Jan LY, Jan YN (1997) The Drosophila neurogenic gene big brain, which encodes a membrane-associated protein, acts cell autonomously and can act synergistically with Notch and Delta. Development 124:3881-3893.
17. Ehring GR, Zampighi GA, Horwitz J, Bok D, Hall JE (1990) Properties of channels reconstituted from the major intrinsic protein of lens fiber membranes. J Gen Physiol 96:631-664.
18. Ehring GR, Lagos N, Zampighi GA, Hall JE (1991) Phosphorylation modulates the voltage dependence of channels reconstituted from the Major Intrinsic Protein of lens fiber membranes. J Membr Biol 126:75-88.
19. Farah S, Agazie Y, Ohan N, Ngsee JK, Liu XJ (1998) A Rho-associated protein kinase, ROKα, binds insulin receptor substrate-1 and modulates insulin signaling. J Biol Chem 273:4740-4746.
20. Fehon RG, Kooh PJ, Rebay I, Regan CL, Xu T, Muskavitch MAT, Artavanis-Tsakonas S (1940) Molecular interactions between the protein products of the neurogenic loci Notch and Delta, two EGF-homologous genes in Drosophila. Cell 61:523-534.
21. Fernandez R, Tabarini D, Azpiazu N, Frasch M, Schlessinger J (1995) The Drosophila insulin receptor homolog: a gene essential for embryonic development encodes two receptor isoforms with different signaling potential. EMBO J 14:3373-3384.
22. Ferrell Jr JE (1999) Xenopus oocyte maturation: new lessons from a good egg. BioEssays 21:833-842.
23. Fortini ME, Artavanis-Tsakonas S (1994) The Suppressor of Hairless protein participates in Notch receptor signaling. Cell 79:273-282.
24. Frank-Vaillant M, Haccard O, Thibier C, Ozon R, Arlot-Bonnemains Y, Prigent C, Jessus C (2000) Progesterone regulates the accumulation and the activation of Eg2 kinase in Xenopus oocytes. J Cell Sci 113:1127-1138.
25. Fushimi K, Sasaki S, Marumo F (1997) Phosphorylation of serine 256 is required for cAMP-dependent regulatory exocytosis of the aquaporin-2 water channel. J Biol Chem 272:14800-14804.
26. Garcia de Herreros A, Dominguez I, Diaz-Meco MT, Graziani G, Cornett ME, Guddal PH, Johansen T, Moscat J (1991) Requirement of phospholipase C-catalyzed hydrolysis of phosphatidylcholine for maturation of Xenopus laevis oocytes in response to insulin and ras p21. J Biol Chem 266:6825-6829.
27. +ATPase in Xenopus oocytes. Am J Physiol 257:C851-C858.
28. Glahn D, Mark SD, Behr RK, Nuccitelli R (1999) Tyrosine kinase inhibitors block sperm-induced egg activation in Xenopus laevis. Dev Biol 205:171-180.
29. Goodman CS, Spitzer NC (1979) Embryonic development of identified neurones: differentiation from neuroblast to neurone. Nature 280:208-214.
30. Goriely A, Dumont N, Dambly-Chaudière C, Ghysen A (1991) The determination of sense organs in Drosophila: effect of the neurogenic mutations in the embryo. Development 113:1395-1404.
31. Gould GW, Jess TJ, Andrews GC, Herbst JJ, Plevin RJ, Gibbs EM (1994) Evidence for a role of phosphatidylinositol 3-kinase in the regulation of glucose transport in Xenopus oocytes. J Biol Chem 269:26622-26625.
32. Greenspan RJ (1992) Initial determination of the neurectoderm in Drosophila. In: Determinants of neuronal identity (Shankland M, Macagno ER, eds), pp 155-188. New York: Academic.
33. Hainaut P, Kowalski A, Giorgetti S, Baron V, Van Obberghen E (1991) Insulin and insulin-like-growth-factor-1 (IGF-1) receptors in Xenopus laevis oocytes: comparison with insulin receptors from liver and muscle. Biochem J 273:673-678.
34. Han Z, Patil RV (2000) Protein kinase A-dependent phosphorylation of Aquaporin-1. Biochem Biophys Res Commun 273:328-332.
35. Han Z, Wax MB, Patil RV (1998a) Potential role of aquaporins and atrial natriuretic peptides in the aqueous humor dynamics. Exp Eye Res 67:251-253.
36. Han Z, Wax MB, Patil RV (1998b) Regulation of Aquaporin-4 water channels by phorbol ester-dependent protein phosphorylation. J Biol Chem 273:6001-6004.
37. Hidaka H, Inagaki M, Kawamoto S, Sasaki Y (1984) Isoquinolinesulfonamides, novel and potent inhibitors of cyclic nucleotide dependent protein kinase and protein kinase C. Biochemistry 23:5036-5041.
38. Hille B (1992) Ionic channels of excitable membranes. Sunderland, MA: Sinauer.
39. Holmes TC, Fadool DA, Ren R, Levitan IB (1996) Association of src tyrosine kinase with a human potassium channel mediated by SH3 domain. Science 274:2089-2091.
40. Kanemitsu MY, Loo LW, Lau AF, Eckhart W (1997) Tyrosine phosphorylation of connexin 43 by v-src is mediated by SH2 and SH3 domain interactions. J Biol Chem 272:22824-22831.
41. - currents by protein kinases A and C in the Xenopus oocyte. Biochem Pharmacol 59:241-247.
42. Kimble J, Simpson P (1997) The LIN-12/Notch signaling pathway and its regulation. Annu Rev Cell Dev Biol 13:333-361.
43. Koch CA, Anderson D, Moran MF, Ellis C, Pawson T (1991) SH2 and SH3 domains: elements that control interactions of cytoplasmic signaling proteins. Science 252:668-674.
44. Kubota HY, Yoshimoto Y, Yoneda M, Hiramoto Y (1987) Free calcium wave upon activation in Xenopus eggs. Dev Biol 119:129-136.
45. Lai EC, Bodner R, Kavaler J, Freschi G, Posakony JW (2000) Antagonism of Notch signaling activity by members of a novel protein family encoded by the Bearded and Enhancer of split gene complexes. Development 127:291-306.
46. Lawrence DS, Niu J (1998) Protein kinase inhibitors: the tyrosine-specific protein kinases. Pharmacol Ther 77:81-114.
47. Lehmann R, Jimenez F, Dietrich U (1983) On the phenotype and development of mutants of early neurogenesis in Drosophila melanogaster. Wilhelm Rouxs Arch Dev Biol 192:62-74.
48. Liao G-Y, Leonard JP (1999) Insulin modulation of cloned mouse NMDA receptor currents in Xenopus oocytes. J Neurochem 73:1510-1519.
49. Liu, L, Brown III JC, Webster WW, Morrisett RA, Monaghan DT (1995) Insulin potentiates N-methyl-D-aspartate receptor activity in Xenopus oocytes and rat hippocampus. Neurosci Lett 192:5-8.
50. Maurel C, Kado RT, Guern J, Chrispeels MJ (1995) Phosphorylation regulates the water channel activity of the seed-specific aquaporin α-TIP. EMBO J 14:3028-3035.
51. Miller DT, Read R, Rusconi J, Cagan RL (2000) The Drosophila primo locus encodes two low-molecular weight tyrosine phosphatases. Gene 243:1-9.
52. Molokanova E, Trivedi B, Savchenko A, Kramer RH (1997) Modulation of rod photoreceptor cyclic nucleotide-gated channels by tyrosine phosphorylation. J Neurosci 17:9068-9076.
53. Mora S, Kaliman P, Chillaron J, Testar X, Palacin M, Zorzano A (1995) Insulin and insulin-like growth factor (IGF-I) stimulate GLUT4 glucose transporter translocation in Xenopus oocytes. Biochem J 311:59-65.
54. O'Dell TJ, Kandel ER, Grant SGN (1991) Long-term potentiation in the hippocampus is blocked by tyrosine kinase inhibitors. Nature 353:558-560.
55. Pimentel, B, de la Rosa EJ, De Pablo F (1996) Insulin acts as an embryonic growth factor for Drosophila neural cells. Biochem Biophys Res Commun 226:855-861.
56. Preston GM, Carroll TP, Guggino WB, Agre P (1992) Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science 256:385-387.
57. Puglianiello A, Germani D, Rossi P, Cianfarani S (2000) IGF-I stimulates chemotaxis of human neuroblasts. Involvement of type 1 IGF receptor, IGF binding proteins. J Endocrinol 165:123-131.
58. Rao Y, Jan LY, Jan YN (1990) Similarity of the product of the Drosophila neurogenic gene big brain to transmembrane channel proteins. Nature 345:163-167.
59. Rao Y, Bodmer R, Jan LY, Jan YN (1992) The big brain gene of Drosophila functions to control the number of neuronal precursors in the peripheral nervous system. Development 116:31-40.
60. Reizer J, Reizer A, Saier MH (1993) The MIP family of integral membrane channel proteins: sequence comparisons, evolutionary relationships, reconstructed pathway of evolution, and proposed functional differentiation of the two repeated halves of the proteins. Crit Rev Biochem Mol Biol 28:235-257.
61. Rickles RJ, Botfield MC, Weng Z, Taylor JA, Green OM, Brugge JS, Zoller MJ (1994) Identification of Src, Fyn, Lyn, PI3K, and Abl SH3 domain ligands using phage display libraries. EMBO J 13:5598-5604.
62. Rivers RL, Dean RM, Chandy G, Hall JE, Roberts DM, Zeidel ML (1997) Functional analysis of nodulin 26, an aquaporin in soybean root nodule symbiosomes. J Biol Chem 272:16256-16261.
63. Sato K, Aoto M, Mori K, Akasofu S, Tokmakov AA, Sahara S, Fukami Y (1996) Purification and characterization of a src-related p57 protein-tyrosine kinase from Xenopus oocytes. J Biol Chem 271:13250-13257.
64. Sato K, Iwasaki T, Tamaki I, Aoto M, Tokmakov AA, Fukami Y (1998) Involvement of protein-tyrosine phosphorylation and dephosphorylation in sperm-induced Xenopus egg activation. FEBS Lett 424:113-118.
65. Sato K, Iwao Y, Fujimura T, Tamaki I, Ogawa K, Iwasaki T, Tokmakov AA, Hatano O, Fukami Y (1999) Evidence for the involvement of a src-related tyrosine kinase in Xenopus egg activation. Dev Biol 209:308-320.
66. Savchenko A, Kraft TW, Molokanova E, Kramer RH (2001) Growth factors regulate phototransduction in retinal rods by modulating cyclic nucleotide-gated channels through dephosphorylation of a specific tyrosine residue. Proc Natl Acad Sci USA 98:5880-5885.
67. Scavo L, Shuldiner AR, Serrano J, Dashner R, Roth J, De Pablo F (1991) Genes encoding receptors for insulin and insulin-like growth factor I are expressed in Xenopus oocytes and embryos. Proc Natl Acad Sci USA 88:6214-6218.
68. Skeath JB (1998) The Drosophila EGF receptor controls the formation and specification of neuroblasts along the dorso-ventral axis of the Drosophila embryo. Development 125:3301-3312.
69. Songyang, Z, Carraway III KL, Eck MJ, Harrison SC, Feldman RA, Mohammadi M, Schlessinger J, Hubbard SR, Smith DP, Eng C, Lorenzo MJ, Ponder BAJ, Mayer BJ, Cantley LC (1995) Catalytic specificity of protein-tyrosine kinases is critical for selective signalling. Nature 373:536-539.
70. Tsukaguchi H, Shayakul C, Berger UV, Mackenzie B, Devidas S, Guggino WB, van Hoek AN, Hediger MA (1998) Molecular characterization of a broad selectivity neutral solute channel. J Biol Chem 273:24737-24743.
71. Udolph G, Urban J, Rüsing G, Lüer K, Technau GM (1998) Differential effects of EGF receptor signalling on neuroblast lineages along the dorsoventral axis of the Drosophila CNS. Development 125:3291-3299.
72. Volk KA, Husted RF, Snyder PM, Stokes JB (2000) Kinase regulation of hENaC mediated through a region in the COOH-terminal portion of the α-subunit. Am J Physiol 278:C1047-C1054.
73. Wangh LJ (1989) Injection of Xenopus eggs before activation, achieved by control of extracellular factors, improves plasmid DNA replication after activation. J Cell Sci 93:1-8.
74. Weaver CD, Shomer NH, Louis CF, Roberts DM (1994) Nodulin 26, a nodule-specific symbiosome membrane protein from soybean, is an ion channel. J Biol Chem 269:17858-17862.
75. Wischmeyer E, Doring F, Karschin A (1998) Acute suppression of inwardly rectifying Kir2.1 channels by direct tyrosine kinase phosphorylation. J Biol Chem 273:34063-34068.
76. Wolf DP (1974) The cortical response in Xenopus laevis ova. Dev Biol 40:102-115.
77. Yasui M, Hazama A, Kwon T-H, Nielsen S, Guggino WB, Agre P (1999) Rapid gating and anion permeability of an intracellular aquaporin. Nature 402:184-187.
78. Yool AJ, Stamer WD, Regan JW (1996) Forskolin stimulation of water and cation permeability in Aquaporin 1 water channels. Science 273: 1216-1218.