GABA neurotransmitter signaling in the developing mouse lens: Dynamic regulation of components and functionality

Developmental Dynamics

Volumn 237, Issue 12, 2008, Pages 3830-3841

  Kwakowsky, Andrea ^a   Schwirtlich, Marija ^a   Kooy, Frank ^b   Ábrahám, István ^c,d   Máté, Zoltán ^a   Katarova, Zoya ^a   Szabó, Gábor ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b UNIVERSITY OF ANTWERP   (Belgium)

^c EÖTVÖS LORÁND UNIVERSITY   (Hungary)

^d UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

GABAA receptor subunits; GABAB receptor subunits; GAD; Intracellular calcium; Lens development; Membrane GABA transporters (GAT1 4); Non neuronal GABA; Vesicular GABA transporter (VGAT)

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR; 4 AMINOBUTYRIC ACID CARRIER; GLUTAMATE DECARBOXYLASE; VESICULAR INHIBITORY AMINO ACID TRANSPORTER;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APICAL MEMBRANE; ARTICLE; BASEMENT MEMBRANE; CALCIUM CELL LEVEL; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; GENE EXPRESSION PROFILING; IMMUNOHISTOCHEMISTRY; LENS; LENS EPITHELIUM; MOUSE; NEUROTRANSMITTER RELEASE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION;

ANIMALS; ANIMALS, NEWBORN; CALCIUM; GABA PLASMA MEMBRANE TRANSPORT PROTEINS; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LENS, CRYSTALLINE; MICE; NEURONS; RECEPTORS, GABA; SIGNAL TRANSDUCTION;

VERTEBRATA;

EID: 57149086087     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.21768     Document Type: Article

References (69)

1. Asada H, Kawamura Y, Maruyama K, Kume H, Ding RG, Kanbara N, Kuzume H, Sanbo M, Yagi T, Obata K. 1997. Cleft palate and decreased brain gamma-aminobutyric acid in mice lacking the 67-kDa isoform of glutamic acid decarboxylase. Proc Natl Acad Sci U S A 94:6496-6499.
2. Balasubramanian S, Teissere JA, Raju DV, Hall RA. 2004. Hetero-oligomerization between GABAA and GABAB receptors regulates GABAB receptor trafficking. J Biol Chem 279:18840-18850.
3. Barker JL, Behar T, Li YX, Liu QY, Ma W, Maric D, Maric I, Schaffner AE, Serafini R, Smith SV, Somogyi R, Vautrin JY, Wen XL, Xian H. 1998. GABAergic cells and signals in CNS development. Perspect Dev Neurobiol 5:305-322.
4. Bassnett S. 2002. Lens organelle degradation. Exp Eye Res 74:1-6.
5. Battaglioli G, Liu H, Martin DL. 2003. Kinetic differences between the isoforms of glutamate decarboxylase: implications for the regulation of GABA synthesis. J Neurochem 86:879-887.
6. Behar TN, Smith SV, Kennedy RT, McKenzie JM, Maric I, Barker JL. 2001. GABA(B) receptors mediate motility signals for migrating embryonic cortical cells. Cereb Cortex 11:744-753.
7. Bettler B, Kaupmann K, Mosbacher J, Gassmann M. 2004. Molecular structure and physiological functions of GABA(B) receptors. Physiol Rev 84:835-867.
8. Bloemendal H, de Jong W, Jaenicke R, Lubsen NH, Slingsby C, Tardieu A. 2004. Ageing and vision: structure, stability and function of lens crystallins. Prog Biophys Mol Biol 86:407-485.
9. Burt DR. 2003. Reducing GABA receptors. Life Sci 73:1741-1758.
10. Calver AR, Medhurst AD, Robbins MJ, Charles KJ, Evans ML, Harrison DC, Stammers M, Hughes SA, Hervieu G, Couve A, Moss SJ, Middlemiss DN, Pangalos MN. 2000. The expression of GABA(B1) and GABA(B2) receptor subunits in the cNS differs from that in peripheral tissues. Neuroscience 100:155-170.
11. Chaudhry FA, Reimer RJ, Bellocchio EE, Danbolt NC, Osen KK, Edwards RH, Storm-Mathisen J. 1998. The vesicular GABA transporter, VGAT, localizes to synaptic vesicles in sets of glycinergic as well as GABAergic neurons. J Neurosci 18:9733-9750.
12. Chen Y, Zhou D, Zhou K, Ren Y, Dai W, Xu M, Lu L, Lu Z. 2007. Study on olfactory function in GABAC receptor/channel rho1 subunit knockout mice. Neurosci Lett 427:10-15.
13. Couve A, Calver AR, Fairfax B, Moss SJ, Pangalos MN. 2004. Unravelling the unusual signalling properties of the GABA(B) receptor. Biochem Pharmacol 68:1527-1536.
14. Culiat CT, Stubbs LJ, Woychik RP, Russell LB, Johnson DK, Rinchik EM. 1995. Deficiency of the beta 3 subunit of the type A gamma-aminobutyric acid receptor causes cleft palate in mice. Nat Genet 11:344-346.
15. Demarque M, Represa A, Becq H, Khalilov I, Ben-Ari Y, Aniksztejn L. 2002. Paracrine intercellular communication by a Ca2+- and SNARE-independent release of GABA and glutamate prior to synapse formation. Neuron 36:1051-1061.
16. Drescher DG, Green GE, Khan KM, Hajela K, Beisel KW, Morley BJ, Gupta AK. 1993. Analysis of gamma-aminobutyric acidA receptor subunits in the mouse cochlea by means of the polymerase chain reaction. J Neurochem 61:1167-1170.
17. Erdo SL, Wolff JR. 1990. gamma-Aminobutyric acid outside the mammalian brain. J Neurochem 54:363-372.
18. Errijgers V, Van Dam D, Gantois I, Van Ginneken CJ, Grossman AW, D'Hooge R, De Deyn PP, Kooy RF. 2007. FVB.129P2-Pde6b(+) Tyr(c-ch)/Ant, a sighted variant of the FVB/N mouse strain suitable for behavioral analysis. Genes Brain Behav 6:552-557.
19. Frederikse PH, Yun E, Kao HT, Zigler JS Jr, Sun Q, Qazi AS. 2004. Synapsin and synaptic vesicle protein expression during embryonic and post-natal lens fiber cell differentiation. Mol Vis 10:794-804.
20. Gammelsaeter R, Froyland M, Aragon C, Danbolt NC, Fortin D, Storm-Mathisen J, Davanger S, Gundersen V. 2004. Glycine, GABA and their transporters in pancreatic islets of Langerhans: evidence for a paracrine transmitter interplay. J Cell Sci 117:3749-3758.
21. Gladkevich A, Korf J, Hakobyan VP, Melkonyan KV. 2006. The peripheral GABAergic system as a target in endocrine disorders. Auton Neurosci 124:1-8.
22. Hagiwara N, Katarova Z, Siracusa LD, Brilliant MH. 2003. Nonneuronal expression of the GABA(A) beta3 subunit gene is required for normal palate development in mice. Dev Biol 254:93-101.
23. Homanics GE, DeLorey TM, Firestone LL, Quinlan JJ, Handforth A, Harrison NL, Krasowski MD, Rick CE, Korpi ER, Makela R, Brilliant MH, Hagiwara N, Ferguson C, Snyder K, Olsen RW. 1997. Mice devoid of gamma-aminobutyrate type A receptor beta3 subunit have epilepsy, cleft palate, and hypersensitive behavior. Proc Natl Acad Sci U S A 94:4143-4148.
24. Ji F, Kanbara N, Obata K. 1999. GABA and histogenesis in fetal and neonatal mouse brain lacking both the isoforms of glutamic acid decarboxylase. Neurosci Res 33:187-194.
25. Jursky F, Nelson N. 1996. Developmental expression of GABA transporters GAT1 and GAT4 suggests involvement in brain maturation. J Neurochem 67:857-867.
26. Karakossian MH, Spencer SR, Gomez AQ, Padilla OR, Sacher A, Loo DD, Nelson N, Eskandari S. 2005. Novel properties of a mouse gamma-aminobutyric acid transporter (GAT4). J Membr Biol 203:65-82.
27. Kash SF, Johnson RS, Tecott LH, Noebels JL, Mayfield RD, Hanahan D, Baekkeskov S. 1997. Epilepsy in mice deficient in the 65-kDa isoform of glutamic acid decarboxylase. Proc Natl Acad Sci U S A 94:14060-14065.
28. Kaufman MH. 1992. The atlas of mouse development. San Diego: Academic Press. xvi, 512 p.
29. Kotlyar M, Fuhrman S, Ableson A, Somogyi R. 2002. Spearman correlation identifies statistically significant gene expression clusters in spinal cord development and injury. Neurochem Res 27:1133-1140.
30. Kralic JE, Korpi ER, O'Buckley TK, Homanics GE, Morrow AL. 2002. Molecular and pharmacological characterization of GABA(A) receptor alpha1 subunit knockout mice. J Pharmacol Exp Ther 302:1037-1045.
31. Kwakowsky A, Schwirtlich M, Zhang Q, Eisenstat DD, Erdelyi F, Baranyi M, Katarova ZD, Szabo G. 2007. GAD isoforms exhibit distinct spatiotemporal expression patterns in the developing mouse lens: correlation with Dlx2 and Dlx5. Dev Dyn 236:3532-3544.
32. Lang RA. 1999. Which factors stimulate lens fiber cell differentiation in vivo? Invest Ophthalmol Vis Sci 40:3075-3078.
33. Lang RA. 2004. Pathways regulating lens induction in the mouse. Int J Dev Biol 48:783-791.
34. Laurie DJ, Seeburg PH, Wisden W. 1992. The distribution of 13 GABAA receptor subunit mRNAs in the rat brain. II. Olfactory bulb and cerebellum. J Neurosci 12:1063-1076.
35. Li X, Ma W, Barker JL, Piatigorsky J. 1995. Transient expression of glutamate decarboxylase and gamma-amino butyric acid in embryonic lens fibers of the rat. Dev Dyn 203:448-455.
36. Liu ZF, Burt DR. 1998. A synthetic standard for competitive RT-PCR quantitation of 13 GABA receptor type A subunit mRNAs in rats and mice. J Neurosci Methods 85:89-98.
37. Lovicu FJ, McAvoy JW. 2005. Growth factor regulation of lens development. Dev Biol 280:1-14.
38. Ma W, Saunders PA, Somogyi R, Poulter MO, Barker JL. 1993. Ontogeny of GABAA receptor subunit mRNAs in rat spinal cord and dorsal root ganglia. J Comp Neurol 338:337-359.
39. McAvoy JW, Chamberlain CG, de Iongh RU, Hales AM, Lovicu FJ. 1999. Lens development. Eye 13(pt 3b):425-437.
40. Menko SA. 2002. Lens epithelial cell differentiation. Exp Eye Res 75:485-490.
41. Mihalek RM, Banerjee PK, Korpi ER, Quinlan JJ, Firestone LL, Mi ZP, Lagenaur C, Tretter V, Sieghart W, Anagnostaras SG, Sage JR, Fanselow MS, Guidotti A, Spigelman I, Li Z, DeLorey TM, Olsen RW, Homanics GE. 1999. Attenuated sensitivity to neuroactive steroids in gamma-aminobutyrate type A receptor delta subunit knockout mice. Proc Natl Acad Sci U S A 96:12905-12910.
42. Min JN, Zhang Y, Moskophidis D, Mivechi NF. 2004. Unique contribution of heat shock transcription factor 4 in ocular lens development and fiber cell differentiation. Genesis 40:205-217.
43. Ogino H, Yasuda K. 2000. Sequential activation of transcription factors in lens induction. Dev Growth Differ 42:437-448.
44. Okada M, Onodera K, Van Renterghem C, Sieghart W, Takahashi T. 2000. Functional correlation of GABA(A) receptor alpha subunits expression with the properties of IPSCs in the developing thalamus. J Neurosci 20:2202-2208.
45. Oppitz M, Mack A, Drews U. 2003. Ca2+-mobilization and cell contraction after muscarinic cholinergic stimulation of the chick embryo lens. Invest Ophthalmol Vis Sci 44:4813-4819.
46. Owens DF, Kriegstein AR. 2002a. Developmental neurotransmitters? Neuron 36:989-991.
47. Owens DF, Kriegstein AR. 2002b. Is there more to GABA than synaptic inhibition? Nat Rev Neurosci 3:715-727.
48. Pearson R, Catsicas M, Becker D, Mobbs P. 2002. Purinergic and muscarinic modulation of the cell cycle and calcium signaling in the chick retinal ventricular zone. J Neurosci 22:7569-7579.
49. Peng Z, Huang CS, Stell BM, Mody I, Houser CR. 2004. Altered expression of the delta subunit of the GABAA receptor in a mouse model of temporal lobe epilepsy. J Neurosci 24:8629-8639.
50. Piatigorsky J. 1981. Lens differentiation in vertebrates. A review of cellular and molecular features. Differentiation 19:134-153.
51. Pirker S, Schwarzer C, Wieselthaler A, Sieghart W, Sperk G. 2000. GABA(A) receptors: immunocytochemical distribution of 13 subunits in the adult rat brain. Neuroscience 101:815-850.
52. Ramadan E, Fu Z, Losi G, Homanics GE, Neale JH, Vicini S. 2003. GABA(A) receptor beta3 subunit deletion decreases alpha2/3 subunits and IPSC duration. J Neurophysiol 89:128-134.
53. Represa A, Ben-Ari Y. 2005. Trophic actions of GABA on neuronal development. Trends Neurosci 28:278-283.
54. Richerson GB, Wu Y. 2003. Dynamic equilibrium of neurotransmitter transporters: not just for reuptake anymore. J Neurophysiol 90:1363-1374.
55. Rudolph U, Crestani F, Mohler H. 2001. GABA(A) receptor subtypes: dissecting their pharmacological functions. Trends Pharmacol Sci 22:188-194.
56. Schousboe A, Sarup A, Larsson OM, White HS. 2004. GABA transporters as drug targets for modulation of GABAergic activity. Biochem Pharmacol 68:1557-1563.
57. Sim JA, Skynner MJ, Pape JR, Herbison AE. 2000. Late postnatal reorganization of GABA(A) receptor signalling in native GnRH neurons. Eur J Neurosci 12:3497-3504.
58. Szabo G, Katarova Z, Greenspan R. 1994. Distinct protein forms are produced from alternatively spliced bicistronic glutamic acid decarboxylase mRNAs during development. Mol Cell Biol 14:7535-7545.
59. Thuault SJ, Brown JT, Sheardown SA, Jourdain S, Fairfax B, Spencer JP, Restituito S, Nation JH, Topps S, Medhurst AD, Randall AD, Couve A, Moss SJ, Collingridge GL, Pangalos MN, Davies CH, Calver AR. 2004. The GABA(B2) subunit is critical for the trafficking and function of native GABA(B) receptors. Biochem Pharmacol 68:1655-1666.
60. Varju P, Katarova Z, Madarasz E, Szabo G. 2001. GABA signalling during development: new data and old questions. Cell Tissue Res 305:239-246.
61. Varju P, Katarova Z, Madarasz E, Szabo G. 2002. Sequential induction of embryonic and adult forms of glutamic acid decarboxylase during in vitro-induced neurogenesis in cloned neuroectodermal cellline, NE-7C2. J Neurochem 80:605-615.
62. Voutsinos B, Dutuit M, Reboul A, Fevre-Montange M, Bernard A, Trouillas P, Akaoka H, Belin MF, Didier-Bazes M. 1998. Serotoninergic control of the activity and expression of glial GABA transporters in the rat cerebellum. Glia 23:45-60.
63. Watanabe M, Maemura K, Kanbara K, Tamayama T, Hayasaki H. 2002. GABA and GABA receptors in the central nervous system and other organs. Int Rev Cytol 213:1-47.
64. Westmoreland JJ, Hancock CR, Condie BG. 2001. Neuronal development of embryonic stem cells: a model of GABAergic neuron differentiation. Biochem Biophys Res Commun 284:674-680.
65. Wisden W, Laurie DJ, Monyer H, Seeburg PH. 1992. The distribution of 13 GABAA receptor subunit mRNAs in the rat brain. I. Telencephalon, diencephalon, mesencephalon. J Neurosci 12:1040-1062.
66. Wojcik SM, Katsurabayashi S, Guillemin I, Friauf E, Rosenmund C, Brose N, Rhee JS. 2006. A shared vesicular carrier allows synaptic corelease of GABA and glycine. Neuron 50:575-587.
67. Wride MA, Mansergh FC, Adams S, Everitt R, Minnema SE, Rancourt DE, Evans MJ. 2003. Expression profiling and gene discovery in the mouse lens. Mol Vis 9:360-396.
68. Wu Y, Wang W, Diez-Sampedro A, Richerson GB. 2007. Nonvesicular inhibitory neurotransmission via reversal of the GABA transporter GAT-1. Neuron 56:851-865.
69. Zampighi GA, Eskandari S, Kreman M. 2000. Epithelial organization of the mammalian lens. Exp Eye Res 71:415-435.