Pyroglutamic acid promotes survival of retinal ganglion cells after optic nerve injury

Current Eye Research

Volumn 34, Issue 7, 2009, Pages 598-605

  Oono, Shinichirou ^a   Kurimoto, Takuji ^a   Nakazawa, Toru ^b   Miyoshi, Tomomitsu ^c   Okamoto, Norio ^a   Kashimoto, Ryosuke ^a   Tagami, Yuichi ^a   Ito, Yoshimasa ^d   Mimura, Osamu ^a  

^a HYOGO COLLEGE OF MEDICINE   (Japan)

^b TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c OSAKA UNIVERSITY   (Japan)

^d KINKI UNIVERSITY   (Japan)

Author keywords

Adult rat excitatory amino acid transfer; Optic nerve transection; Pyroglutamic acid; Retinal ganglion cells

Indexed keywords

BETA III TUBULIN; BETA TUBULIN; EXCITATORY AMINO ACID TRANSPORTER; FLUOROGOLD; LEVO PYRROLIDINE 2,4 DICARBOXYLIC ACID; PDC; PYROGLUTAMIC ACID; PYRROLIDINE DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL CULTURE; CELL DENSITY; CELL SURVIVAL; CONTROLLED STUDY; DRUG MECHANISM; EYE; IN VITRO STUDY; IN VIVO STUDY; INJECTION; MALE; NERVE TRANSECTION; NONHUMAN; OPTIC NERVE INJURY; PRIORITY JOURNAL; RAT; RETINA; RETINA GANGLION CELL; SUPERIOR COLLICULUS; SURGICAL SPONGE; VITREOUS BODY;

ANIMALS; AXOTOMY; CELL COUNT; CELL SURVIVAL; CELLS, CULTURED; DICARBOXYLIC ACIDS; GLUTAMATE PLASMA MEMBRANE TRANSPORT PROTEINS; INJECTIONS; MALE; NEUROTRANSMITTER UPTAKE INHIBITORS; OPTIC NERVE; PYRROLIDINES; PYRROLIDONECARBOXYLIC ACID; RATS; RATS, WISTAR; RETINAL GANGLION CELLS; STILBAMIDINES; TUBULIN; VITREOUS BODY;

EID: 70350635440     PISSN: 02713683     EISSN: 14602202     Source Type: Journal    
DOI: 10.1080/02713680902981292     Document Type: Article

References (46)

1. Berkelaar M, Clarke DB, Wang YC, Bray GM, Aguayo AJ. Axotomy results in delayed death and apoptosis of retinal ganglion cells in adult rats. J Neurosci 1994;14:4368-4374.
2. Kurimoto T, Miyoshi T, Suzuki A, Yakura T, Watanabe M, Mimura O, Fukuda Y. Apoptotic death of beta cells after optic nerve transection in adult cats. J Neurosci 2003;23:4023-4028.
3. Mey J, Thanos S. Intravitreal injections of neurotrophic factors support the survival of axotomized retinal ganglion cells in adult rats in vivo. Brain Res 1993;602:304-317.
4. Mansour-Robaey S, Clarke DB, Wang YC, Bray GM, Aguayo A. Effects of ocular injury and administration of brain-derived neurotrophic factor on survival and regrowth of axotomized retinal ganglion cells. Proc Natl Acad Sci USA 1994;91:1632-1636.
5. Peinado-Ŕamon P, Salvador M, Villegas-Ṕeres MP, Vidal-Sanz M. Effects of axotomy and intraocular administration of NT-4, NT-3, and brain-derived neurotrophic factor on the survival of adult rat retinal ganglion cells - A quantitative in vivo study. Invest Ophthalmol Vis Sci 1996;37:489-500.
6. Watanabe M, Tokita Y, Kato M, Fukuda Y. Intravitreal injections of neurotrophic factors and forskolin enhance survival and axonal regeneration of axotomized beta ganglion cells in cat retina. Neuroscience 2003;116:733-742.
7. Kermer P, Klöcker N, Labes M, Bähr M. Insulin-like growth factor-1 protects axotomized rat retinal ganglion cells from secondary death via PI3-K-dependent Akt phosphorylation and inhibition of caspase-3 in vivo. J Neurosci 2000;20:2-8.
8. Kermer P, Klöcker N, Labes M, Bähr M. Inhibition of CPP32- like proteases rescues axotomized retinal ganglion cells from secondary cell death in vivo. J Neurosci 1999;18:4656-4662.
9. Yoles E, Muller S, Scheartz M. NMDA-receptor antagonist protects from secondary degeneration after partial optic nerve crush. J Neurotrauma 1997;14:665-675.
10. Schuettauf F, Naskar R, Vorwerk CK, Zurakowski D, Dreyer EB. Ganglion cell loss after optic nerve mediated through AMPA-Kainate and NMDA receptors. Invest Ophthalmol Vis Sci 2000;41:4313-4316.
11. VanDer Werf P, MeisterA. The metabolic formation and utilization of 5-oxo-L-proline (L-pyroglutamate, L-pyrorolidone carboxylate). Adv Enzymol 1975;43:519-566.
12. AbrahamGN, Podell DN. Pyroglutamic acid non-metabolic formation, function in proteins and peptides, and characteristics of the enzymes effecting its removal. Mol Cell Biochem 1981;38:181-190.
13. Bauer K, Schomburg L, Heuer H, Schäfer MK. Thyrotropinreleasing hormone (TRH), the TRH-receptor and the TRHdegrading ectoenzyme; three elements of a peptidergic signaling system. Results Prob Cell Differ 1999;26:13-42.
14. Drago F, Continella G, Valerio C, D'Agata V, Astuto C, Spadaro F, Continella G, Scapagnini U. Pyroglutamic acid improves learning and memory capacities in old rats. Funct Neurol 1988;3:137-143.
15. Xiao XO, Liu GO. L-pyroglutamic acid protects rat cortical neurons against sodium glutamate-induced injury. Zhongguo Yao Li Xue Bao 1999;20:733-736.
16. Koenig ML, Sgarlat CM, Yourick DL, Long JB, Meyehoff JL. In vitro neuroprotection against glutamate-induced toxicity by pGlu-Glu-Pro-NH2 (EEP). Peptides 2001;22:2091-2097.
17. Hawkins RA, Simpson IA, Mokashi A, Vĩna J.R. Pyroglutamate stimulates Na+-dependent glutamate transport across the blood-brain barrier. FEBS Lett 2006;580:4382-4386. (Pubitemid 44137350)
18. Hawkins RA, O'Kane RL, Simpson IA, Vĩna JR. Structure of the blood-brain barrier and its role in the transport of amino acids. J Nutr 2006;136:218-226.
19. RauenT,Rothstein JD,WässleH.Differential expression of three glutamate transporter subtypes in the rat retina. Cell Tissue Res 1996;286:325-336.
20. Lehre KP, Davanger S, Danbolt NC. Localization of the glutamate transporterGLAST in rat retina. Brain Res 1997;44:129-137.
21. Harada T, Harada C, Watanabe M, Inoue Y, Sakagawa T, Nakayama N, Sasaki S, Okuyama S,Watase K, Tanaka K. Functions of the two glutamate transporters GALST and GLT-1 in the retina. Proc Natl Acad Sci USA 1998;958:4663-4666.
22. Rauen T, Taylor WR, Kuhlbrodt K, Wiessner M. High affinity glutamate transporters in the retina: A major role of the glial glutamate transporter GLAST-1 in transmitter clearance. Cell Tissue Res 1998;291:19-31.
23. Pow DV, Barnett NL, Penfold P. Are neuronal transporters relevant in retinal glutamate homeostasis? Neurochem Int 2003;37:191-198.
24. Pow DV, Barnett NL. Developmental expression of excitatory amino acid transporter 5: A photoreceptor and bipolar cell glutamate transporter in rat retina. Neurosci Lett 2000;280:21-24.
25. Vorwerk CK, Naskar R, Schuettauf F, Quinto K, Zurakowski D, Gochenauer G, Robinson MB, Mackler SA, Dreyer EB. Depression of retinal glutamate transporter function leads to elevated intravitreal glutamate levels and ganglion cell death. Invest Ophthalmol Vis Sci 2000;41:3615-3621.
26. Kurimoto T, Ishi M, Tagami Y, Nishimura M, Miyoshi T, Tsukamoto Y, Mimura O. Xylazine promotes axonal regeneration in the crushed optic nerve of adult rats. Neuroreport 2006;17:1525-1529.
27. Robinson MB,Djali S, Buchhalter JR. Inhibition of glutamate uptake with L-trans-pyrrolidine-2,4-dicarboxylate potentiates glutamate toxicity in primary hippocampal cultures. J Neurochem 1993;61:2099-2103.
28. Arriza JL, Fairman WA, Wadiche JI, Murdoch GH, Kavanaugh MP, Amara SG. Functional comparisons of three glutamate transporter subtypes cloned from human motor cortex. J Neurosci 1994;14:5559-5569.
29. Arriza JL, Eliasof S, Kavanaugh MP, Amara SG. Excitatory amino acid transporter 5, a retinal glutamate transporter coupled to a chloride conductance. Proc Natl Acad Sci USA 1997;94:4155-4160.
30. Wang GJ, Chung HJ, Schnuer J, Pratt K, Zable AC, Kavanaugh MP, Rosenberg PA. High affinity glutamate transport in rat cortical neurons in culture. Mol Pharmacol 1998;53:88-96.
31. Gegelashvili G, Dehnes Y, Danbolt NC, Schousboe A. The high affinity glutamate transporters GLT1, GLAST, and EAAT4 are regulated via different signaling mechanisms. Neurochem Int 2000;37:163-170.
32. Thanos S, Pavlidis C, Mey J, Thiel HJ. Specific transcellular staining of microglia in the adult rat after traumatic degeneration of carbocyanine-filled retinal ganglion cells. Exp Eye Res 1992;55:101-117.
33. Peinado-RaAlmon P, Salvador M, Villegas-Ṕeres MP, Vidal- Sanz M. Effects of axotomy and intraocular administration of NT-4, NT-3, and brain-derived neurotrophic factor on the survival of adult rat retinal ganglion cells-A quantitative in vivo study. Invest Ophthalmol Vis Sci 1996;37:489-500.
34. Nakazawa T, Takahashi H, Nishijima K, Shimura M, Fuse N, Tamai M, Hafezi-Moghadam A, Nishida K. Pitavastin prevents NMDA-induced retinal ganglion cell death by suppressing leukocyte recruitment. J Neurochem 2007;100:1018-1031.
35. Watanabe M, Rutishauser U, Silver L. Formation of the retinal ganglion cell and optic fiber layers. J Neurobiol 1991;22:85-96.
36. Snow RL, Robson JA. Ganglion cell neurogenesis, migration, and early differentiation in the chick retina. Neuroscience 1994;58:399-409.
37. Leon S, Yin Y, Nguyen J, Irwin N, Benowitz L. Lens injury stimulates axon regeneration in the mature rat optic nerve. J Neurosci 2000;20:4615-4626.
38. Luo JM, Zhi Y, Chen Q, Cen LP, Zhang CW, Lam DS, Harvey AR, Cui Q. Influence of macrophages and lymphocytes on the survival and axon regeneration of injured retinal ganglion cells in rats from different autoimmune backgrounds. Eur J Neurosci 2007;26:3475-3485. (Pubitemid 350243528)
39. Harada T, Harada C, Nakamura K, Quah HM, Okumura A, Namekata K, Saeki T, Aihara M, Yoshida H, Mitani A, Tanaka K. The potential role of glutamate transporters in the pathogenesis of normal tension glaucoma. J Clin Invest 2007;117:1763-1770.
40. Yoles E, Schwartz M. Elevation of intraocular glutamate levels in rats with partial lesion of the optic nerve. Arch Ophthalmol 1998;116:906-910.
41. VorwerkCK, Zurakowski D, McDermott LM, MawrinC,Dreyer EB. Effects of axonal injury on ganglion cell survival and glutamate homeostasis. Brain Res Bull 2004;62:485-490.
42. Levkovitch-Verbin H, Martin KR, Quigley HA, Baumrind LA, Pease ME, Valenta DJ. Measurement of amino acid levels in the vitreous humor of rats after chronic intraocular pressure elevation or optic nerve transection. J Glaucoma 2002;11:396-405.
43. Naskar R, Vorwerk CK, Dreyer EB. Concurrent downregulation of a glutamate transporter and receptor in glaucoma. Invest Ophthalmol Vis Sci 2000;41:1940-1944.
44. Himi T, Ikeda M, Yasuhara T, Murota SI. Oxidative neuronal death caused by glutamate uptake inhibition in cultured hippocampal neurons. J Neurosci Res 2003;71:679-688.
45. Re DB, Nafia I, Melon C, Shimamoto K, Goff LK, Had-Aissouni L. Glutamate leakage from a compartmentalized intracellular metabolic pool and activation of the lipoxygenase pathway mediate oxidative astrocyte death by reversed glutamate transport. Glia 2006;54:47-57.
46. Roh YJ, Moon C, Kim SY, Park MH, Bae YC, Chun MH, Moon JI. Glutathione depletion induces differential apoptosis in cells of mouse retina in vivo. Neurosci Lett 2007;417:266-270.