Lee-Rivera I, López-Colomé AM

Language: Spanish
References: 64
Page: 71-81
PDF size: 211.33 Kb.

ABSTRACT

The multiple actions of glutamate in the retina, as a neurotransmitter, a trophic factor or a neurotoxin, are directly related to the heteromeric composition of the NMDA type of glutamate receptors present in this tissue. The tetrameric NMDARs include two NR1 subunits which form the calcium-permeable cation channel, in addition to NR2 and NR3 subunits which modulate its activity. Recent results demonstrate that retinal NMDARs might include tissue-specific NR1 splice variants and NR2 subunits, in both mature and embryonic tissue, which determine structural and functional differences with brain receptors. As a consequence, drugs shown to protect brain neurons from glutamate-induced neuronal death, are ineffective in the retina. The clarification of the precise subunit composition of NMDARs in the retina will allow the future design of drugs aimed to prevent neuronal loss in pathological conditions such as glaucoma, vascular occlusion, optic neuropathy and ischemia, in which glutamate excitotoxicity seems to be involved.

REFERENCES

1. Michaelis, E.K. Molecular biology of glutamate receptors in the central nervous system and their role in excitotoxicity, oxidative stress and aging. Prog. Neurobiol. 54, 369-415 (1998).

2. López-Colomé, A.M. in Excitatory amino acids (eds. Roberts, P. J., Storm-Mathisen, J. & H.F. Bradford) 143-157 (McMillan Press, London, 1986).

3. Massey, S. & Maguire, G. in Excitatory aminoacids and synaptic transmission (eds. Wheal, H. & AM, T.) 201-221 (Academic Press, New York, 1995).

4. Fletcher, E.L., Hack, I., Brandstatter, J.H. & Wassle, H. Synaptic localization of NMDA receptor subunits in the rat retina. J. Comp. Neurol. 420, 98-112 (2000).

5. Alagarsamy, S., Sorensen, S. & Conn, P. Coordinate regulation of metabotropic glutamate receptors. Curr. Op. Neurobiol. 11, 357-362 (2001).

6. Dingledine, R., Borges, K., Bowie, D. & Traynelis, S.F. The glutamate receptor ion channels. Pharmacol. Rev. 51, 7-61 (1999).

7. Moriyoshi, K. et al. Molecular cloning and characterization of the rat NMDA receptor. Nature 354, 31-37 (1991).

8. Kutsuwada, T. et al. Molecular diversity of the NMDA receptor channel. Nature 358, 36-41 (1992).

9. Ciabarra, A.M. et al. Cloning and characterization of chi-1: a developmentally regulated member of a novel class of the ionotropic glutamate receptor family. J. Neurosci. 15, 6498-6508 (1995).

10. Monyer, H. et al. Heteromeric NMDA receptors: molecular and functional distinction of subtypes. Science 256, 1217-1221 (1992).

11. Das, S. et al. Increased NMDA current and spine density in mice lacking the NMDA receptor subunit NR3A. Nature 393, 377-381 (1998).

12. Chatterton, J. et al. Excitatory glycine receptors containing the NR3 family of NMDA receptor subunits. Nature 415, 793-798 (2002).

13. Nicholls, J.G. et al. From Neuron to Brain (Sinauer Associates Inc., Sunderland, MA, USA, 2001).

14. Barnstable, C.J. Glutamate and GABA in retinal circuitry. EXS 66, 121-133 (1993).

15. DeVries, S.H. Bipolar cells use kainate and AMPA receptors to filter visual information into separate channels. Neuron 28, 843-856 (2000).

16. Thoreson, W.B. & Witkovsky, P. Glutamate receptors and circuits in the vertebrate retina. Progress in Retinal & Eye Research 18, 765-810 (1999).

17. Sucher, N.J., Lipton, S.A. & Dreyer, E.B. Molecular basis of glutamate toxicity in retinal ganglion cells. Vision Res. 37, 3483-3493 (1997).

18. López-Colomé, A.M. & Somohano, F. N-methyl-D-aspartate receptors in the retina: 3-[(+/-)-2- carboxypiperazin- 4-yl]-propyl-1-phosphonic acid (CPP) binding studies. Neuropharmacology 31, 577-584 (1992).

19. Calderón, F. & López-Colomé, A.M. Spermine inhibits [3H]glycine binding at the NMDA receptors from plexiform layers of chick retina. Neurochem. Res. 23, 1363-1369 (1998).

20. Rodriguez-Contreras, A., Calderón, F. & López-Colomé, A.M. Strychnine-insensitive [3H] glycine binding to synaptosomal membranes from the chick retina. Int. J. Dev. Neurosci. 16, 413-421 (1998).

21. Lombardi, G. & Moroni, F. Glutamate receptor antagonists protect against ischemia-induced retinal damage. Eur. J. Pharmacol. 271, 489-495 (1994).

22. Zukin, R.S. & Bennett, M.V. Alternatively spliced isoforms of the NMDARI receptor subunit. Trends Neurosci. 18, 306-313 (1995).

23. Traynelis, S.F., Hartley, M. & Heinemann, S.F. Control of proton sensitivity of the NMDA receptor by RNA splicing and polyamines. Science 268, 873-876 (1995).

24. Durand, G.M., Bennett, M.V. & Zukin, R.S. Splice variants of the N-methyl-D-aspartate receptor NR1 identify domains involved in regulation by polyamines and protein kinase C. Proc. Natl. Acad. Sci. USA 90, 6731-6735 (1993).

25. Hollmann, M. et al. Zinc potentiates agonist-induced currents at certain splice variants of the NMDA receptor. Neuron 10, 943-954 (1993).

26. Lee-Rivera, I., Zarain-Herzberg, A. & López-Colomé, A.M. Developmental expression of N-methyl-D-aspartate glutamate receptor 1 splice variants in the chick retina. J. Neurosci. Res. 73, 369-383 (2003).

27. Standley, S., Roche, K.W., McCallum, J., Sans, N. & Wenthold, R.J. PDZ domain suppression of an ER retention signal in NMDA receptor NR1 splice variants. Neuron 28, 887-898 (2000).

28. Tingley, W. et al. Characterization of protein kinase A and protein kinase C phosphorylation of the N-methyl-D-aspartate receptor NR1 subunit using phosphorylation site-specific antibodies. J. Biol. Chem. 272, 5157-5166 (1997).

29. Okabe, S., Miwa, A. & Okado, H. Alternative splicing of the C-terminal domain regulates cell surface expression of the NMDA receptor NR1 subunit. J. Neurosci. 19, 7781-7792 (1999).

30. Bottai, D., Maler, L. & Dunn, R.J. Alternative RNA splicing of the NMDA receptor NR1 mRNA in the neurons of the teleost electrosensory system. J. Neurosci. 18, 5191-5202 (1998).

31. Tingley, W.G., Roche, K.W., Thompson, A.K. & Huganir, R.L. Regulation of NMDA receptor phosphorylation by alternative splicing of the C-terminal domain. Nature 364, 70-73 (1993).

32. Ehlers, M.D., Zhang, S., Bernhadt, J.P. & Huganir, R.L. Inactivation of NMDA receptors by direct interaction of calmodulin with the NR1 subunit. Cell 84, 745-755 (1996).

33. Meggio, F., Marin, O. & Pinna, L.A. Substrate specificity of protein kinase CK2. Cell Mol. Biol. Res. 40, 401-409 (1994).

34. Kuenzel, E.A., Mulligan, J.A., Sommercorn, J. & Krebs, E.G. Substrate specificity determinants for casein kinase II as deduced from studies with synthetic peptides. J. Biol. Chem. 262, 9136-9140 (1987).

35. Lieberman, D.N. & Mody, I. Casein kinase-II regulates NMDA channel function in hippocampal neurons. Nat. Neurosci. 2, 125-132 (1999).

36. Whitmore, D. et al. A clockwork organ. Biol. Chem. 381, 793-800 (2000).

37. Kornau, H.C., Schenker, L.T., Kennedy, M.B. & Seeburg, P.H. Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science 269, 1737-1740 (1995).

38. Sun, D., Rait, J.L., Kalloniatis, M. & Margalit, E. Inner retinal neurons display differential responses to N-methyl-D-aspartate receptor activation Stargardt disease in a patient with retinoblastoma. Journal of Comparative Neurology 465, 38-56 (2003).

39. Lelong, I.H. et al. Pharmacological properties of N-methyl-D-aspartate receptors on ganglion cells of an amphibian retina. Proceedings of the National Academy of Sciences of the United States of America 89, 8472-8476 (1992).

40. Sucher, N.J. et al. N-methyl-D-aspartate receptor subunit NR3A in the retina: developmental expression, cellular localization, and functional aspects. Investigative Ophthalmology & Visual Science 44, 4451-4456 (2003).

41. Brandstätter, J.H., Hartveit, E., Sassoe-Pognetto, M. & Wässle, H. Expression of NMDA and high-affinity kainate receptor subunit mRNAs in the adult rat retina. Eur. J. Neurosci. 6, 1100-1112 (1994).

42. Watanabe, M., Mishina, M. & Inoue, Y. Differential distributions of the NMDA receptor channel subunit mRNAs in the mouse retina. Brain Res. 634, 328-332 (1994).

43. Gründer, T., Kohler, K., Kaletta, A. & Guenther, E. The distribution and developmental regulation of NMDA receptor subunit proteins in the outer and inner retina of the rat. J. Neurobiol. 44, 333-342 (2000).

44. Brandstätter, J.H., Koulen, P. & Wässle, H. Diversity of glutamate receptors in the mammalian retina. Vision Res. 38, 1385-1397 (1998).

45. Dixon, D.B. & Copenhagen, D.R. Two types of glutamate receptors differentially excite amacrine cells in the tiger salamander retina. Journal of Physiology 449, 589-606 (1992).

46. Scheetz, A.J. & Constantine-Paton, M. Modulation of NMDA receptor function: implications for vertebrate neural development. FASEB Journal 8, 745-752 (1994).

47. Hestrin, S. Developmental regulation of NMDA receptor-mediated synaptic currents at a central synapse. Nature 357, 686-689 (1992).

48. Morrisett, R., Mott, D., Lewis, D., Wilson, W. & Swartzwelder, H. Reduced sensitivity of the N-methyl-D-aspartate component of synaptic transmission to magnesium in hippocampal slices from immature rats. Brain Res. Dev. Brain. Res. 56, 257-262 (1990).

49. Kleckner, N. & Dingledine, R. Regulation of hippocampal NMDA receptors by magnesium and glycine during development. Brain Res. Mol. Brain Res. 11, 151-159 (1991).

50. Somohano, F., Roberts, P.J. & López-Colomé, A.M. Maturational changes in retinal excitatory amino acid receptors. Brain Res. 470, 59-67 (1988).

51. Subramaniam, S. & McGonigle, P. Regional profile of developmental changes in the sensitivity of the N- methyl-D-aspartate receptor to polyamines. J. Neurochem. 62, 1408-1415 (1994).

52. Yamakura, T. & Shimoji, K. Subunit- and site-specific pharmacology of the NMDA receptor channel. Prog. Neurobiol. 59, 279-298 (1999).

53. Cull-Candy, S., Brickley, S. & Farrant, M. NMDA receptor subunits: diversity, development and disease. Current Opinion in Neurobiology 11, 327-335 (2001).

54. Mey, J. & Thanos, S. Development of the visual system of the chick. I. Cell differentiation and histogenesis. Brain Res. Brain Res. Rev. 32, 343-379 (2000).

55. Sugioka, M., Fukuda, Y. & Yamashita, M. Development of glutamate-induced intracellular Ca2+ rise in the embryonic chick retina. J. Neurobiol. 34, 113-125 (1998).

56. Goodman, C. & Shatz, C. Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell 72 Supp, 77-98 (1993).

57. López-Colomé, A.M. & Somohano, F. in Extracellular and intracellular messengers in the vertebrate retina. (eds. Redburn, D. & Pasantes-Morales, H.) (Alan Liss Inc., New York, NY, 1989).

58. Boje, K.M., Skolnick, P., Raber, J., Fletcher, R.T. & Chader, G. Strychnine-insensitive glycine receptors in embryonic chick retina: characteristics and modulation of NMDA neurotoxicity. Neurochem. Int. 20, 473-486 (1992).

59. Clarke, P.G. Neuron death in the developing avian isthmo-optic nucleus, and its relation to the establishment of functional circuitry. J. Neurobiol. 23, 1140-1158 (1992).

60. Wong, R.O. Retinal waves and visual system development. Annu. Rev. Neurosci. 22, 29-47 (1999).

61. Prybylowski, K.L. & Wolfe, B.B. Developmental differences in alternative splicing of the NR1 protein in rat cortex and cerebellum. Brain Res. Dev. Brain Res. 123, 143-150 (2000).

62. Monyer, H., Burnashev, N., Laurie, D.J., Sakmann, B. & Seeburg, P.H. Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12, 529-540 (1994).

63. Vicini, S. et al. Functional and pharmacological differences between recombinant N-methyl- D-aspartate receptors. J. Neurophysiol. 79, 555-566 (1998).

64. Wenzel, A., Benke, D., Mohler, H. & Fritschy, J.M. N-methyl-D-aspartate receptors containing the NR2D subunit in the retina are selectively expressed in rod bipolar cells. Neuroscience 78, 1105-1112 (1997).