Comparative analyses of the neurodegeneration induced by the non-competitive NMDA-receptor-antagonist drug MK801 in mice and rats

Neurotoxicology and Teratology

Volumn 32, Issue 5, 2010, Pages 542-550

  Bender, Crhistian ^a   de Olmos, Soledad ^a   Bueno, Adrián ^a,b   de Olmos, José ^a   Lorenzo, Alfredo ^a,b  

^a Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^b UNIVERSIDAD NACIONAL DE CÓRDOBA   (Argentina)

Author keywords

Animal models; Mice; MK801; Neurodegeneration; Non competitive NMDA antagonist

Indexed keywords

DIZOCILPINE MALEATE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; C57BL 6 MOUSE; CELL DEATH; COMPARATIVE STUDY; CONTROLLED STUDY; DENTATE GYRUS; DISEASE ASSOCIATION; EXCITOTOXICITY; FEMALE; MALE; MOUSE; NERVE DEGENERATION; NEUROTOXICITY; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; PYRIFORM CORTEX; RAT; SCHIZOPHRENIA; SEX DIFFERENCE; SPECIES DIFFERENCE; SURVIVAL TIME; WISTAR RAT;

ANIMALIA; MUS; MUS MUSCULUS; RATTUS; RATTUS NORVEGICUS; RODENTIA;

EID: 77955513190     PISSN: 08920362     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ntt.2010.05.002     Document Type: Article

References (71)

1. Andiné P., Widermark R., Axelson R., Nyberg G., Olofsson G., Martenson E., Sandberg M. Characterization of MK-801-induced behavior as a putative rat model of psychosis. J. Pharmacol. Exp. Ther. 1999, 290:1393-1408.
2. Asan E., Yilmazer-Hanke D.M., Eliava M., Hantsch M., Lesch K.P., Schmitt A. The corticotropin-releasing factor (CRF)-system and monoaminergic afferents in the central amygdala: investigations in different mouse strains and comparison with the rat. Neuroscience 2005, 131:953-967.
3. Auer R.N. Effect of age and sex on N-Methyl-D-Aspartate antagonist-induced neuronal necrosis in rats. Stroke 1996, 27:743-746.
4. Benkovic S.A., O'Callaghan J.P., Miller D.B. Regional neuropathology following kainic acid intoxication in adult and aged C57BL/6J mice. Brain Res. 2006, 1070:215-231.
5. Benkovic S.A., O'Callaghan J.P., Miller D.B. Sensitive indicators of injury reveal hippocampal damage in C57BL/6J mice treated with kainic acid in the absence of tonic-clonic seizures. Brain Res. 2004, 1024:59-76.
6. Brosnan-Watters G., Ogimi T., Ford D., Tatekawa L., Gilliam D., Bilsky E.J., Nash D. Differential effects of MK-801 on cerebrocortical neuronal injury in C57BL/6J, NSA, and ICR mice. Neuropsychopharmacol. Biol. Psychiatry 2000, 24:925-938.
7. Brosnan-Watters G., Wozniak D.F., Nardi A., Olney J.W. Parallel recovery of MK-801-induced spatial learning impairment and neuronal injury in male mice. Pharmacol. Biochem. Behav. 1999, 62:111-122.
8. Bueno A., de Olmos S., Heimer L., de Olmos J.S. NMDA-antagonist MK-801 induced neuronal degeneration in Wistar rat brain detected by the amino-cupric silver method. Exp. Toxicol. Pathol. 2003, 54:319-334.
9. Bueno A., de Olmos S., Manzini M., Desmond N., de Olmos J.S. Strain differences in the neurotoxic sequelae of MK801 visualized with the amino-cupric silver method. Exp. Toxicol. Pathol. 2003, 55:287-294.
10. Chavez C., Gogos A., Jones M.E., van den Buuse M. Psychotropic drug-induced locomotor hyperactivity and prepulse inhibition regulation in male and female aromatase knockout (ArKO) mice: role of dopamine D1 and D2 receptors and dopamine transporters. Psychopharmacology 2009, 206:267-279.
11. Chen S.R., Samoriski G., Pan H.L. Antinociceptive effects of chronic administration of uncompetitive NMDA receptor antagonists in a rat model of diabetic neuropathic pain. Neuropharmacology 2009, 57:121-126.
12. Colbourne F., RakiĆ D., Auer R.N. The effects of temperature and scopolamine on N-methyl-D-aspartate antagonist-induced neuronal necrosis in the rat. Neuroscience 1999, 90:87-94.
13. D'Souza D.N., Harlan R.E., Garcia M.M. Sexual dimorphic effect of morphine and MK-801: sex steroid-dependent and -independent mechanism. J. Appl. Physiol. 2002, 92:493-503.
14. de Olmos J.S., Beltramino C.A., de Olmos S. Use of an amino-cupric-silver technique for the detection of early and semiacute neuronal degeneration caused by neurotoxicants, hypoxia, and physical trauma. Neurotoxicol. Teratol. 1994, 16:545-561.
15. de Olmos S., Bender C., de Olmos J.S., Lorenzo A. Neurodegeneration and prolonged immediate early gene expression throughout cortical areas of the rat brain following acute administration of dizocilpine. Neuroscience 2009, 164:1347-1359.
16. de Olmos S., Bueno A., Bender C., Lorenzo A., de Olmos J. Sex differences and influence of gonadal hormones on MK801-induced neuronal degeneration in the granular retrosplenial cortex of the rat. Brain Struct. Funct. 2008, 213:229-238.
17. de Olmos J.S., Ebbesson S.O.E., Heimer L. Silver methods for the impregnation of degenerating axoplasm. Neuroanatomical Tract-tracing Methods 1981, 117-170. Plenum Press. L. Heimer, M.J. RoBards (Eds.).
18. Deng X., Ladenheim B., Jayanthi S., Cadet J.L. Methamphetamine administration causes death of dopaminergic neurons in the mouse olfactory bulb. Biol. Psychiatry 2007, 61:1235-1243.
19. Duncan G., Miyamoto S., Gu H., Lieberman J., Koller B., Snouwaert J. Alterations in regional brain metabolism in genetic and pharmacological models of reduced NMDA receptor function. Brain Res. 2002, 951:166-176.
20. Ellison G. Competitive and non-competitive NMDA antagonists induce similar limbic degeneration. NeuroReport 1994, 5:2688-2692.
21. Farber N.B. The NMDA receptor hypofunction model of psychosis. Ann. N.Y. Acad. Sci. 2003, 1003:119-130.
22. Farber N.B., Kim S.H., Dikranian K., Jiang X.P., Heinkel C. Receptor mechanisms and circuitry underlying NMDA antagonist neurotoxicity. Mol. Psychiatry 2002, 7:32-43.
23. Fiske B.K., Brunjes P.C. NMDA receptor regulation of cell death in the rat olfactory bulb. J. Neurobiol. 2001, 47:223-232.
24. Fix A.S., Ross J., Stitzel S.R., Switzer R.C. Integrated evaluation of central nervous system lesions: stains for neurons, astrocytes, and microglia reveal the spatial and temporal features of MK-801-induced neuronal necrosis in the rat cerebral cortex. Toxicol. Pathol. 1996, 24:291-304.
25. Gao X.M., Elmer G.I., Adams-Huet B., Tamminga C.A. Social memory in mice: disruption with an NMDA antagonist and attenuation with antipsychotic drugs. Pharmacol. Biochem. Behav. 2009, 2:236-242.
26. Gould E. How widespread is adult neurogenesis in mammals?. Nat. Rev. Neurosci. 2007, 8:481-488.
27. Grant G., Holländer H., Aldskogius H. Suppressive silver methods-a tool for identifying axotomy-induced neuron degeneration. Brain Res. Bull. 2004, 62:261-269.
28. Grauer S.M., Pulito V.L., Navarra R.L., Kelly M.P., Kelley C., Graf R., Langen B., Logue S., Brennan J., Jiang L., et al. Phosphodiesterase 10A inhibitor activity in preclinical models of the positive, cognitive, and negative symptoms of schizophrenia. J. Pharmacol. Exp. Ther. 2009, 331:574-590.
29. Hashimoto K., Fujita Y., Horio M., Kunitachi S., Iyo M., Ferraris D., Tsukamoto T. Co-administration of a D-amino acid oxidase inhibitor potentiates the efficacy of D-serine in attenuating prepulse inhibition deficits after administration of dizocilpine. Biol. Psychiatry 2009, 65:1103-1106.
30. Herculano-Houzel S., Collins C.E., Wong P., Kaas J.H. Cellular scaling rules for primate brains. Proc. Natl. Acad. Sci. USA 2007, 104:3562-3567.
31. Herculano-Houzel S., Mota B., Lent R. Cellular scaling rules for rodent brains. Proc. Natl. Acad. Sci. USA 2006, 103:12138-12143.
32. Hönack D., Löscher W. Sex differences in NMDA receptor mediated responses in rats. Brain Res. 1993, 620:167-170.
33. Horvath Z.C. MK-801-induced neuronal damage in rats. Brain Res. 1997, 753:181-195.
34. Hur G.H., Son W.C., Shin S., Kang J.K., Kim Y.B. Sex differences in dizocilpine (MK801) neurotoxicity in rats. Environ. Toxicol. Pharmacol. 1999, 7:143-146.
35. Jevtovic-Todorovic V., Beals J., Benshoff N., Olney J.W. Prolonged exposure to inhalational anesthetic nitrous oxide kills neurons in adult rat brain. Neuroscience 2003, 122:609-616.
36. Kaindl A.M., Ikonomidou C. Glutamate antagonists are neurotoxins for the developing brain. Neurotox. Res. 2007, 11:203-218.
37. Kalia L.V., Kalia S.K., Salter M.W. NMDA receptors in clinical neurology: excitatory times ahead. Lancet Neurol. 2008, 7:742-755.
38. Kelly S., Bieneman A., Uney J.B., McCulloch J. Cerebral glucose utilization in transgenic mice overexpressing heat shock protein 70 is altered by dizocilpine. Eur. J. Neurosci. 2002, 15:945-952.
39. Kitt C.A., Höhmann C., Coyle J.T., Price D.L. Cholinergic innervation of mouse forebrain structures. J. Comp. Neurol. 1994, 341:117-129.
40. Kocerha J., Faghihi M.A., Lopez-Toledano M.A., Huang J., Ramsey A.J., Caron M.G., Sales N., Willoughby D., Elmen J., Hansen H.F., et al. MicroRNA-219 modulates NMDA receptor-mediated neurobehavioral dysfunction. Proc. Natl. Acad. Sci. USA 2009, 106:3507-3512.
41. Livy D.J., Parnell S.E., West J.R. Blood ethanol concentration profiles: a comparison between rats and mice. Alcohol 2003, 29:165-171.
42. Majewski-Tiedeken C.R., Rabin C.R., Siegel S.J. Ketamine exposure in adult mice leads to increased cell death in C3H, DBA2 and FVB inbred mouse strains. Drug Alcohol Depend. 2008, 92:217-227.
43. Mandairon N., Jourdan F., Didier A. Deprivation of sensory inputs to the olfactory bulb up-regulates cell death and proliferation in the subventricular zone of adult mice. Neuroscience 2003, 119:507-516.
44. Matsuki H., Shirayama Y., Hashimoto K., Tanaka A., Minabe Y. Effects of age and gender on the expression of brain-derived neurotrophic factor mRNA in rat retrosplenial cortex following administration of dizocilpine. Neuropsychopharmacology 2001, 25:258-266.
45. Moghaddam B., Jackson M.E. Glutamatergic animal models of schizophrenia. Ann. N.Y. Acad. Sci. 2003, 1003:131-137.
46. Morgan C.J., Muetzelfeldt L., Curran H.V. Consequences of chronic ketamine self-administration upon neurocognitive function and psychological wellbeing: a 1-year longitudinal study. Addiction 2009, 105:121-133.
47. Morgan C.J., Muetzelfeldt L., Curran H.V. Ketamine use, cognition and psychological wellbeing: a comparison of frequent, infrequent and ex-users with polydrug and non-using controls. Addiction 2009, 104:77-87.
48. Nabeshima T., Kitaichi K., Noda Y. Functional changes in neuronal systems induced by phencyclidine administration. Ann. N.Y. Acad. Sci. 1996, 801:29-38.
49. Nabeshima T., Yamaguchi K., Furukawa H., Kameyama T. Role of sex hormones in sex-dependent differences in phencyclidine-induced stereotyped behaviors in rats. Eur. J. Pharmacol. 1984, 105:197-206.
50. Noguchi K.K., Nemmers B., Farber N.B. Age has a similar influence on the susceptibility to NMDA antagonist-induced neurodegeneration in most brain regions. Brain Res. Dev. Brain Res. 2005, 158:82-91.
51. O'Neill M.F., Hicks C.A., Shaw G., Parameswaran T., Cardwell G.P., O'Neill M.J. Effects of 5-hydroxytryptamine2 receptor antagonism on the behavioral activation and immediate early gene expression induced by dizocilpine. J. Pharmacol. Exp. Ther. 1998, 287:839-846.
52. Olney J., Labruyere J., Price M. Pathological changes induced in cerebrocortical neurons by phencyclidine and related drugs. Science 1989, 244:1360-1362.
53. Olney J.W., Newcomer J.W., Farber N.B. NMDA receptor hypofunction model of schizophrenia. J. Psychiatr. Res. 1999, 33:523-533.
54. Paxinos G., Franklin K.B. The Mouse Brain in Stereotaxic Coordinates 2001, Academic Press, San Diego. Edition.
55. Paxinos G., Watson C. The Rat Brain Stereotaxic Coordinates 2007, Academic Press, San Diego. Edition.
56. Picciotto M.R., Wickman K. Using knockout and transgenic mice to study neurophysiology and behavior. Physiol. Rev. 1998, 78:1131-1163.
57. 4 receptor-deficient mice display cortical hyperexcitability. J. Neurosci. 2001, 21:3756-3763.
58. Rubinstein M., Mogil J.S., Japón M., Chan E.C., Allen R.G., Low M.J. Absence of opioid stress-induced analgesia in mice lacking beta-endorphin by site-directed mutagenesis. PNAS 1996, 93:3995-4000.
59. Schmued L.C., Hopkins K.J. Fluoro-Jade B: a high affinity fluorescent marker for the localization of neuronal degeneration. Brain Res. 2000, 874:123-130.
60. Sharp F.R., Jasper P., Hall J., Noble L., Sagar S.M. MK801 and ketamine induce heat shock protein hsp72 in injured neurons in posterior cingulate and retroesplenial cortex. Ann. Neurol. 1991, 30:801-809.
61. Sharp F.R., Tomitaka M., Bernaudin M., Tomitaka S. Psychosis: pathological activation of limbic thalamocortical circuits by psychomimetics and schizophrenia?. Trends Neurosci. 2001, 24:330-334.
62. Stone T.W., Addae J.I. The pharmacological manipulation of glutamate receptors and neuroprotection. Eur. J. Pharmacol. 2002, 447:285-296.
63. Switzer R.C. Application of silver degeneration stains for neurotoxicity testing. Toxicol. Pathol. 2000, 28:70-83.
64. Tamminga C.A., Lahti A.C., Medoff D.R., Gao X.M., Holcomb H.H. Evaluating glutamatergic transmission in schizophrenia. Ann. N.Y. Acad. Sci. 2003, 1003:113-118.
65. Väisänen J., Saarelainen T., Koponen E., Castrén E. Altered trkB neurotrophin receptor activation does not influence the N-methyl-D-aspartate receptor antagonist-mediated neurotoxicity in mouse posterior cingulate cortex. Neurosci. Lett. 2003, 350:1-4.
66. van Groen T., Kadish I., Wyss J.M. Species differences in the projections from the entorhinal cortex to the hippocampus. Brain Res. Bull. 2002, 57:553-556.
67. Wei L.N. Transgenic animals as new approaches in pharmacological studies. Annu. Rev. Pharmacol. Toxicol. 1997, 37:119-141.
68. Wessinger W.D. Sexual dimorphic effects of chronic phencyclidine in rats. Eur. J. Pharmacol. 1995, 277:107-112.
69. Wozniak D., Dikranian K., Ishimaru M., Nardi A., Corso T., Tenkova T., Olney J., Fix A. Disseminated corticolimbic neuronal degeneration induced in rat brain by MK-801: potential relevance to Alzheimer disease. Neurobiol. Dis. 1998, 5:305-322.
70. Wozniak D.F., Brosnan-Watters G., Nardi A., McEwen M., Corso T.D., Olney J.W., Fix A.S. MK-801 neurotoxicity in male mice: histologic effects and chronic impairment in spatial learning. Brain Res. 1996, 707:165-179.
71. Yamaguchi M., Mori K. Critical period for sensory experience-dependent survival of newly generated granule cells in the adult mouse olfactory bulb. Proc. Natl. Acad. Sci. USA 2005, 102:9697-9702.