Robust photoregulation of GABA A receptors by allosteric modulation with a propofol analogue

Nature Communications

Volumn 3, Issue , 2012, Pages

  Yue, Lan ^a,b   Pawlowski, Michal ^a   Dellal, Shlomo S ^c,e   Xie, An ^a   Feng, Feng ^a   Otis, Thomas S ^c   Bruzik, Karol S ^a   Qian, Haohua ^a,d   Pepperberg, David R ^a,b  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b University of Illinois at Chicago   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d NATIONAL EYE INSTITUTE   (United States)

^e ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; AZOBENZENE; PROPOFOL;

BENZENE; FROG; GENE EXPRESSION; LIGAND; NERVOUS SYSTEM; NEUROLOGY; PHOTOCHEMISTRY; PHYSIOLOGY;

ALLOSTERIC MODULATION; ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; FEMALE; ISOMER; LIGHT; MALE; MODULATION; MOUSE; NONHUMAN; OOCYTE; PHOTOREGULATION; PURKINJE CELL; RAT; RETINA GANGLION CELL; ULTRAVIOLET RADIATION; XENOPUS LAEVIS;

ALLOSTERIC REGULATION; ANIMALS; AZO COMPOUNDS; ELECTROPHYSIOLOGY; FEMALE; GAMMA-AMINOBUTYRIC ACID; LIGHT; MALE; MICE; MICE, INBRED C57BL; PROPOFOL; PURKINJE CELLS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; XENOPUS LAEVIS;

XENOPUS LAEVIS;

EID: 84869418227     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms2094     Document Type: Article

References (59)

1. Lester, H. A., Krouse, M. E., Nass, M. M., Wassermann, N. H. & Erlanger, B. F. A covalently bound photoisomerizable agonist: comparison with reversibly bound agonists at Electrophorus electroplaques. J. Gen. Physiol. 75, 207-232 (1980). (Pubitemid 10105291)
2. Volgraf, M. et al. Reversibly caged glutamate: a photochromic agonist of ionotropic glutamate receptors. J. Am. Chem. Soc. 129, 260-261 (2007). (Pubitemid 46106611)
3. Farrant, M. & Nusser, Z. Variations on an inhibitory theme: phasic and tonic activation of GABAA receptors. Nat. Rev. Neurosci. 6, 215-229 (2005). (Pubitemid 40342416)
4. Olsen, R. W. & Sieghart, W. GABAA receptors: subtypes provide diversity of function and pharmacology. Neuropharmacology 56, 141-148 (2009).
5. Mortensen, M., Ebert, B., Waford, K. & Smart, T. G. Distinct activities of GABA agonists at synaptic-and extrasynaptic-type GABAA receptors. J. Physiol. 588, 1251-1268 (2010).
6. Hales, T. G. & Lambert, J. J. The actions of propofol on inhibitory amino acid receptors of bovine adrenomedullary chromafn cells and rodent central neurones. Br. J. Pharmacol. 104, 619-628 (1991).
7. A receptors in cultured murine hippocampal neurons. J. Neurosci. 14, 7747-7760 (1994).
8. Adodra, S. & Hales, T. G. Potentiation, activation and blockade of GABAA receptors of clonal murine hypothalamic GT1-7 neurones by propofol. Br. J. Pharmacol. 115, 953-960 (1995).
9. A receptor. J. Med. Chem. 45, 3210-3221 (2002). (Pubitemid 34774272)
10. Chang, C. S., Olcese, R. & Olsen, R. W. A single M1 residue in the subunit alters channel gating of GABAA receptor in anesthetic modulation and direct activation. J. Biol. Chem. 278, 42821-42828 (2003). (Pubitemid 37345892)
11. A receptor. Mol. Pharmacol. 65, 68-76 (2004). (Pubitemid 38113887)
12. 3N265M knock-in mouse. J. Neurosci. 29, 2177-2187 (2009).
13. A receptor β3 subunit. FASEB J. 17, 250-252 (2003).
14. Solt, K. & Forman, S. A. Correlating the clinical actions and molecular mechanisms of general anesthetics. Curr. Opin. Anaesthesiol. 20, 300-306 (2007). (Pubitemid 47051888)
15. Banghart, M., Borges, K., Isacof, E., Trauner, D. & Kramer, R. H. Light-activated ion channels for remote control of neuronal fring. Nat Neurosci. 7, 1381-1386 (2004). (Pubitemid 41057762)
16. Standaert, R. F. & Park, S. B. Abc amino acids: design, synthesis and properties of new photoelastic amino acids. J. Org. Chem. 71, 7952-7966 (2006). (Pubitemid 44571799)
17. Volgraf, M. et al. Allosteric control of an ionotropic glutamate receptor with an optical switch. Nat Chem. Biol. 2, 47-52 (2006).
18. Fortin, D. L. et al. Photochemical control of endogenous ion channels and cellular excitability. Nat Meth. 5, 331-338 (2008). (Pubitemid 351455160)
19. Janovjak, H., Szobota, S., Wyart, C., Trauner, D. & Isacof, E. Y. A light-gated, potassium-selective glutamate receptor for the optical inhibition of neuronal fring. Nat Neurosci. 13, 1027-1032 (2010).
20. Beharry, A. A. & Woolley, G. A. Azobenzene photoswitches for biomolecules. Chem. Soc. Rev. 40, 4422-4437 (2011).
21. Bali, M. & Akabas, M. H. The location of a closed channel gate in the GABAA receptor channel. J. Gen. Physiol. 129, 145-159 (2007). (Pubitemid 46184872)
22. A receptor. J. Neurosci. 17, 625-634 (1997). (Pubitemid 27024575)
23. A receptor. J. Neurosci. 18, 8590-8604 (1998).
24. Amin, J. & Weiss, D. S. GABAA receptor needs two homologous domains of the-subunit for activation by GABA but not by pentobarbital. Nature 366, 565569 (1993).
25. Muroi, Y., Teusch, C. M., Czajkowski, C. & Jackson, M. B. Distinct structural changes in the GABAA receptor elicited by pentobarbital and GABA. Biophys. J. 96, 499-509 (2009).
26. Wisden, W., Korpi, E. R. & Bahn, S. The cerebellum: a model system for studying GABAA receptor diversity Neuropharmacol. 35, 1139-1160 (1996). (Pubitemid 27013849)
27. A receptors containing the α1 subunit in Purkinje cells. J. Neurosci. 26, 3245-3255 (2006).
28. Wulf, P. et al. From synapse to behavior: rapid modulation of defned neuronal types with engineered GABAA receptors. Nat Neurosci. 10, 923-929 (2007).
29. A receptors expressed in HEK cells. Neuropharmacology 56, 155-160 (2009).
30. 2β3γ2 γ-aminobutyric acidA receptors. J. Neurochem. 80, 140-148 (2002). (Pubitemid 34614586)
31. Mihic, S. J. & Harris, R. A. Inhibition of ρ1 receptor GABAergic currents by alcohols and volatile anesthetics. J. Pharmacol. Exp. Ter. 277, 411-416 (1996). (Pubitemid 27169087)
32. Kucken, A. M. et al. Identifcation of benzodiazepine binding site residues in the γ2 subunit of the γ-aminobutyric acidA receptor. Mol. Pharmacol. 57, 932-939 (2000). (Pubitemid 30253376)
33. Kucken, A. M., Teissére, J. A., Sefnga-Clark, J., Wagner, D. A. & Czajkowski, C. Structural requirements for imidazobenzodiazepine binding to GABAA receptors. Mol. Pharmacol. 63, 289-296 (2003). (Pubitemid 36158364)
34. Ishida, A. T. & Cohen, B. N. GABA-activated whole-cell currents in isolated retinal ganglion cells. J. Neurophysiol. 60, 381-396 (1988).
35. Fischer, K. F., Lukasiewicz, P. D. & Wong, R. O. L. Age-dependent and cell class-specifc modulation of retinal ganglion cell bursting activity by GABA. J. Neurosci 18, 3767-3778 (1998). (Pubitemid 28225684)
36. Wässle, H., Koulen, P., Brandstätter, J. H., Fletcher, E. L. & Becker, C.-M. Glycine and GABA receptors in the mammalian retina. Vision Res. 38, 1411-1430 (1998). (Pubitemid 28239263)
37. Rotolo, T. C. & Dacheux, R. F. Evidence for glycine, GABAA, and GABAB receptors on rabbit OFF-alpha ganglion cells. Vis. Neurosci. 20, 285-296 (2003). (Pubitemid 38101213)
38. Häusser, M. & Clark, B. A. Tonic synaptic inhibition modulates neuronal output pattern and spatiotemporal synaptic integration. Neuron 19, 665-678 (1997). (Pubitemid 27430752)
39. Smith, S. L. & Otis, T. S. Persistent chances in spontaneous fring of Purkinje neurons triggered by the nitric oxide signaling cascade. J. Neurosci. 23, 367-372 (2003). (Pubitemid 36139534)
40. Santhakumar, V., Hanchar, H. J., Wallner, M., Olsen, R. W. & Otis, T. S. Contributions of the GABAA receptor α6 subunit to phasic and tonic inhibition revealed by a naturally occurring polymorphism in the α6 gene. J. Neurosci. 26, 3357-3364 (2006).
41. Hestrin, S., Nicoll, R. A., Perkel, D. J. & Sah, P. Analysis of excitatory synaptic action in pyramidal cells using whole-cell recording from rat hippocampal slices. J. Physiol 422, 203-225 (1990). (Pubitemid 20109856)
42. Eisenman, L. N. et al. Anticonvulsant and anesthetic efects of a fuorescent neurosteroid analog activated by visible light. Nat Neurosci. 10, 523-530 (2007). (Pubitemid 46494583)
43. Trapani, G., Altomare, C., Sanna, E., Biggio, G. & Liso, G. Propofol in anesthesia. Mechanism of action, structure-activity relationships, and drug delivery. Curr. Med. Chem. 7, 249-271 (2000). (Pubitemid 30396448)
44. A receptor dysfunction in epilepsy: a mutation in the γ2-subunit gene. Nat Genet 28, 46-48 (2001). (Pubitemid 32405815)
45. Palma, E. et al. Abnormal GABAA receptors from the human epileptic hippocampal subiculum microtransplanted to Xenopus oocytes. Proc. Natl Acad. Sci. USA 102, 2514-2518 (2005). (Pubitemid 40279408)
46. Goodkin, H. P., Joshi, S., Mtchedlishvili, Z., Brar, J. & Kapur, J. Subunit-specifc trafcking of GABAA receptors during status epilepticus. J. Neurosci. 28, 2527-2538 (2008). (Pubitemid 351348210)
47. Macdonald, R. L., Kang, J.-Q. & Gallagher, M. J. Mutations in GABAA receptor subunits associated with genetic epilepsies. J. Physiol. 588, 1861-1869 (2010).
48. Power, K. N., Flaatten, H., Gilhus, N. E. & Engelsen, B. A. Propofol treatment in adult refractory status epilepticus. Mortality risk and outcome. Epilepsy Res. 94, 53-60 (2011).
49. Iyer, V. N., Hoel, R. & Rabinstein, A. A. Propofol infusion syndrome in patients with refractory status epilepticus: an 11-year clinical experience. Crit Care Med. 37, 3024-3030 (2009).
50. Rossetti, A. O. & Lowenstein, D. H. Management of refractory status epilepticus in adults: still more questions than answers. Lancet Neurol. 10, 922-930 (2011).
51. Yizhar, O., Fenno, L. E., Davidson, T. J., Mogri, M. & Deisseroth, K. Optogenetics in neural systems. Neuron 71, 9-34 (2011).
52. Qian, H. & Dowling, J. E. GABAA and GABAC receptors on hybrid bass retinal bipolar cells. J. Neurophysiol. 74, 1920-1928 (1995). (Pubitemid 3001676)
53. Lukasiewicz, P. D. & Shields, C. R. Diferent combinations of GABAA and GABAC receptors confer distinct temporal properties to retinal synaptic responses. J. Neurophysiol. 79, 3157-3167 (1998). (Pubitemid 28317042)
54. Palmer, M. J. Functional segregation of synaptic GABAA and GABAC receptors in goldfsh bipolar cell terminals. J. Physiol. 577, 45-53 (2006). (Pubitemid 44698239)
55. Yue, L. et al. Potentiating action of propofol at GABAA receptors of retinal bipolar cells. Invest Ophthalmol. Vis. Sci. 52, 2497-2509 (2011).
56. Xie, A. et al. Propofol potentiates GABA-elicited responses of bipolar and ganglion cells in rat retina. Invest Ophthalmol. Vis. Sci 51, ARVO E-abstract 1865 (2010).
57. Sadovski, O., Beharry, A. A., Zhang, F. & Woolley, G. A. Spectral tuning of azobenzene photoswitches for biological applications. Angew. Chem. Int. Ed. 48, 1484-1486 (2009).
58. Adamian, L. et al. Structural model of ρ1 GABAC receptor based on evolutionary analysis: testing of predicted protein-protein interactions involved in receptor assembly and function. Protein Sci. 18, 2371-2383 (2009).
59. Ramsey, D. J., Ripps, H. & Qian, H. Streptozotocin-induced diabetes modulates GABA receptor activity of rat retinal neurons. Exper. Eye Res. 85, 413-422 (2007). (Pubitemid 47259059)