Slow and selective death of spinal motor neurons in vivo by intrathecal infusion of kainic acid: Implications for AMPA receptor-mediated excitotoxicity in ALS

Journal of Neurochemistry

Volumn 98, Issue 3, 2006, Pages 782-791

  Sun, Hui ^a,c   Kawahara, Yukio ^a,d   Ito, Kyoko ^a   Kanazawa, Ichiro ^b   Kwak, Shin ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c NATIONAL CENTER FOR GERIATRICS AND GERONTOLOGY   (Japan)

^d WISTAR INSTITUTE   (United States)

Author keywords

AMPA receptor; Amyotrophic lateral sclerosis; Excitotoxicity; GluR2; GluR3; RNA editing

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; 6 NITRO 7 SULFAMOYLBENZO[F]QUINOXALINE 2,3 DIONE; AMPA RECEPTOR; AMPA RECEPTOR AGONIST; CYCLOTHIAZIDE; GLUTAMATE RECEPTOR 2; GLUTAMATE RECEPTOR 3; KAINIC ACID; MESSENGER RNA;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR DISORDER; EXCITOTOXICITY; IN VIVO STUDY; MALE; MOTONEURON; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTOR UPREGULATION; SPINAL CORD DORSAL HORN; SPINAL CORD MOTONEURON; SUBARACHNOID SPACE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; CELL DEATH; EXCITATORY AMINO ACID AGONISTS; INJECTIONS, SPINAL; KAINIC ACID; MALE; MOTOR NEURONS; RATS; RATS, INBRED F344; RATS, WISTAR; RECEPTORS, AMPA; SPINAL CORD; TIME FACTORS;

EID: 33745905621     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2006.03903.x     Document Type: Article

References (40)

1. Broom W. J., Parton M. J., Vance C. A., Russ C., Andersen P. M., Hansen V., Leigh P. N., Powell J. F., Al-Chalabi A. and Shaw C. E. (2004) No association of the SOD1 locus and disease susceptibility or phenotype in sporadic ALS. Neurology 63, 2419-2422.
2. Brorson J. R., Manzolillo P. A., Gibbons S. J. and Miller R. J. (1995) AMPA receptor desensitization predicts the selective vulnerability of cerebellar Purkinje cells to excitotoxicity. J. Neurosci. 15, 4515-4524.
3. Brusa R., Zimmermann F., Koh D., Feldmeyer D., Gass P., Seeburg P. and Sprengel R. (1995) Early-onset epilepsy and postnatal lethality associated with an editing-deficient GluR-B allele in mice. Science 270, 1677-1680.
4. Burnashev N., Khodorova A., Jonas P., Helm P., Wisden W., Monyer H., Seeburg P. and Sakmann B. (1992) Calcium-permeable AMPA-kainate receptors in fusiform cerebellar glial cells. Science 256, 1566-1570.
5. Carriedo S. G., Yin H. Z. and Weiss J. H. (1996) Motor neurons are selectively vulnerable to AMPA/kainate receptor-mediated injury in vitro. J. Neurosci. 16, 4069-4079.
6. Corona J. C. and Tapia R. (2004) AMPA receptor activation, but not the accumulation of endogenous extracellular glutamate, induces paralysis and motor neuron death in rat spinal cord in vivo. J. Neurochem. 89, 988-997.
7. Feldmeyer D., Kask K., Brusa R., Kornau H. C., Kolhekar R., Rozov A., Burnashev N., Jensen V., Hvalby O., Sprengel R., et al. (1999) Neurological dysfunctions in mice expressing different levels of the Q/R. site-unedited AMPAR subunit GluR-B. Nat. Neurosci. 2, 57-64.
8. Gurney M. E., Pu H., Chiu A. Y., Dal Canto M. C., Polchow C. Y., Alexander D. D., Caliendo J., Hentati A., Kwon Y. W., Deng H. X., et al. (1994) Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science 264, 1772-1775.
9. Hashida H., Goto J., Suzuki T., Jeong S., Masuda N., Ooie T., Tachiiri Y., Tsuchiya H. and Kanazawa I. (2001) Single cell analysis of CAG repeat in brains of dentatorubral-pallidoluysian atrophy (DRPLA). J. Neurol. Sci. 190, 87-93.
10. Hirata A., Nakamura R., Kwak S., Nagata N. and Kamakura K. (1997) AMPA receptor-mediated slow neuronal death in the rat spinal cord induced by long-term blockade of glutamate transporters with THA. Brain Res. 771, 37-44.
11. Hollmann M., Hartley M. and Heinemann S. (1991) Ca2+ permeability of KA-AMPA-gated glutamate receptor channels depends on subunit composition. Science 252, 851-853.
12. Howland D. S., Liu J., She Y., Goad B., Maragakis N. J., Kim B., Erickson J., Kulik J., DeVito L., Psaltis G., et al. (2002) Focal loss of the glutamate transporter EAAT2 in a transgenic rat model of SOD1 mutant-mediated amyotrophic lateral sclerosis (ALS). Proc. Natl Acad. Sci. USA 99, 1604-1609.
13. Iihara K., Joo D. T., Henderson J., Sattler R., Taverna F. A., Lourensen S., Orser B. A., Roder J. C. and Tymianski M. (2001) The influence of glutamate receptor 2 expression on excitotoxicity in Glur2 null mutant mice. J. Neurosci. 21, 2224-2239.
14. Jackson M., Al-Chalabi A., Enayat Z. E., Chioza B., Leigh P. N. and Morrison K. E. (1997) Copper/zinc superoxide dismutase 1 and sporadic amyotrophic lateral sclerosis: analysis of 155 cases and identification of a novel insertion mutation. Ann. Neurol. 42, 803-807.
15. Kawahara Y., Kwak S., Sun H., Ito K., Hashida H., Aizawa H., Jeong S.-Y. and Kanazawa I. (2003) Human spinal motoneurons express low relative abundance of GluR2 mRNA: An implication for excitotoxicity in ALS. J. Neurochem. 85, 680-689.
16. Kawahara Y., Ito K., Sun H., Aizawa H., Kanazawa I. and Kwak S. (2004) Glutamate receptors: RNA editing and death of motor neurons. Nature 427, 801.
17. Kawahara Y., Sun H., Ito K., Hideyama T., Aoki M., Sobue G., Tsuji S. and Kwak S. (2006) Underediting of GluR2 mRNA, a neuronal death inducing molecular change in sporadic ALS, does not occur in motor neurons in ALS1 or SBMA. Neurosci. Res. 54, 11-14.
18. Kuner R., Groom A. J., Bresink I., Kornau H. C., Stefovska V., Muller G., Hartmann B., Tschauner K., Waibel S., Ludolph A. C., et al. (2005) Late-onset motoneuron disease caused by a functionally modified AMPA receptor subunit. Proc. Natl Acad. Sci. USA 102, 5826-5831.
19. Kwak S. and Nakamura R. (1995a) Acute and late neurotoxicity in the rat spinal cord in vivo induced by glutamate receptor agonists. J. Neurol. Sci. 129, 99-103.
20. Kwak S. and Nakamura R. (1995b) Selective degeneration of inhibitory interneurons in the rat spinal cord induced by intrathecal infusion of acromelic acid. Brain Res. 702, 61-71.
21. Kwak S., Aizawa H., Ishida M. and Shinozaki H. (1992) Acromelic acid, a novel kainate analogue, induces long-lasting paraparesis with selective degeneration of interneurons in the rat spinal cord. Exp. Neurol. 116, 145-155.
22. May P. C. and Robison P. M. (1993) Cyclothiazide treatment unmasks AMPA excitotoxicity in rat primary hippocampal cultures. J. Neurochem. 60, 1171-1174.
23. Nagai M., Aoki M., Miyoshi I., Kato M., Pasinelli P., Kasai N., Brown R. H. Jr and Itoyama Y. (2001) Rats expressing human cytosolic copper-zinc superoxide dismutase transgenes with amyotrophic lateral sclerosis: associated mutations develop motor neuron disease. J. Neurosci. 21, 9246-9254.
24. Nakamura R., Kamakura K. and Kwak S. (1994) Late-onset selective neuronal damage in the rat spinal cord induced by continuous intrathecal administration of AMPA. Brain Res. 654, 279-285.
25. Nakamura R., Kamakura K., Hirata A. and Kwak S. (1997) Concentration-dependent changes in motor behavior produced by continuous intrathecal infusion of excitatory amino acids in the rat spinal cord. Brain Res. Protocol. 1, 385-390.
26. Ohno K., Okada M., Tsutsumi R., Kohara A. and Yamaguchi T. (1997) Kainate excitotoxicity is mediated by AMPA- but not kainate-preferring receptors in embryonic rat hippocampal cultures. Neurochem. Int. 31, 715-722.
27. Ohno K., Okada M., Tsutsumi R., Matsumoto N. and Yamaguchi T. (1998) Characterization of cyclothiazide-enhanced kainate excitotoxicity in rat hippocampal cultures. Neurochem. Int. 32, 265-271.
28. Partin K. M., Patneau D. K. and Mayer M. L. (1994) Cyclothiazide differentially modulates desensitization of alpha-amino-3-hydroxy-5-methyl-4- isoxazolepropionic acid receptor splice variants. Mol. Pharmacol. 46, 129-138.
29. Rembach A., Turner B. J., Bruce S., Cheah I. K., Scott R. L., Lopes E. C., Zagami C. J., Beart P. M., Cheung N. S., Langford S. J., et al. (2004) Antisense peptide nucleic acid targeting GluR3 delays disease onset and progression in the SOD1 G93A mouse model of familial ALS. J. Neurosci. Res. 77, 573-582.
30. Roland L., Mitsumoto H. and De Vivo D. (2005) Hereditary and acquired motor neuron diseases, in Merritt's Neuology, 11th edn (Roland L., ed.), pp. 861-870. Lippincott, Williams & Wilkins, Philadelphia.
31. Sans N., Vissel B., Petralia R. S., Wang Y. X., Chang K., Royle G. A., Wang C. Y., O'Gorman S., Heinemann S. F. and Wenthold R. J. (2003) Aberrant formation of glutamate receptor complexes in hippocampal neurons of mice lacking the GluR2 AMPA receptor subunit. J. Neurosci. 23, 9367-9373.
32. Sommer B., Kohler M., Sprengel R. and Seeburg P. H. (1991) RNA editing in brain controls a determinant of ion flow in glutamate-gated channels. Cell 67, 11-19.
33. Spalloni A., Albo F., Ferrari F., Mercuri N., Bernardi G., Zona C. and Longone P. (2004) Cu/Zn-superoxide dismutase (GLY93 - >ALA) mutation alters AMPA receptor subunit expression and function and potentiates kainate-mediated toxicity in motor neurons in culture. Neurobiol. Dis 15, 340-350.
34. Sun H., Kawahara Y., Ito K., Kanazawa I. and Kwak S. (2005) Expression profile of AMPA receptor subunit mRNA in single adult rat brain and spinal cord neurons in situ. Neurosci. Res. 52, 228-234.
35. Tateno M., Sadakata H., Tanaka M., Itohara S., Shin R. M., Miura M., Masuda M., Aosaki T., Urushitani M., Misawa H., et al.(2004) Calcium-permeable AMPA receptors promote misfolding of mutant SOD1 protein and development of amyotrophic lateral sclerosis in a transgenic mouse model. Hum. Mol. Genet. 13, 2183-2196.
36. Terro F., Yardin C., Esclaire F., Ayer-Lelievre C. and Hugon J. (1998) Mild kainate toxicity produces selective motoneuron death with marked activation of CA (2+)-permeable AMPA/kainate receptors. Brain Res. 809, 319-324.
37. Tölle T. R., Berthele A., Zieglgänsberger W., Seeburg P. H. and Wisden W. (1993) The differential expression of 16 NMDA and non-NMDA receptor subunits in the rat spinal cord and in periaqueductal gray. J. Neurosci. 13, 5009-5028.
38. Van Damme P., Braeken D., Callewaert G., Robberecht W. and Van Den Bosch L. (2005) GluR2 deficiency accelerates motor neuron degeneration in a mouse model of amyotrophic lateral sclerosis. J. Neuropathol. Exp. Neurol. 64, 605-612.
39. Van Den Bosch L., Vandenberghe W., Klaassen H., Van Houtte E. and Robberecht W. (2000) Ca (2+)-permeable AMPA receptors and selective vulnerability of motor neurons. J. Neurol. Sci. 180, 29-34.
40. Verdoorn T., Burnashev N., Monye R. H., Seeburg P. and Sakmann B. (1991) Structural determinants of ion flow through recombinant glutamate receptor channels. Science 252, 1715-1718.