Behavioral and immunohistological effects of cholinergic damage in immunolesioned rats: Alteration of c-Fos and polysialylated neural cell adhesion molecule expression

Neuroscience

Volumn 147, Issue 4, 2007, Pages 893-905

  Chambon, C ^a   Paban, V ^a   Manrique, C ^a   Alescio Lautier, B ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

Author keywords

192 IgG saporin; dentate gyrus; rat; T maze

Indexed keywords

IMMUNOGLOBULIN G; NERVE CELL ADHESION MOLECULE; PROTEIN C FOS; SAPORIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR CHANGE; BRAIN DAMAGE; CHOLINERGIC NERVE; CONTROLLED STUDY; DENTATE GYRUS; IMMUNOHISTOCHEMISTRY; MALE; NERVE CELL DEGENERATION; NERVE CELL PLASTICITY; NERVE REGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; TASK PERFORMANCE;

ANALYSIS OF VARIANCE; ANIMALS; ANTIBODIES, MONOCLONAL; BASAL NUCLEUS OF MEYNERT; BEHAVIOR, ANIMAL; BRAIN INJURIES; CHOLINE O-ACETYLTRANSFERASE; CHOLINERGIC FIBERS; FOOD DEPRIVATION; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; MALE; N-GLYCOSYL HYDROLASES; NEURAL CELL ADHESION MOLECULE L1; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, WISTAR; SEPTAL NUCLEI; SIALIC ACIDS; TIME FACTORS;

EID: 34547096734     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2007.05.022     Document Type: Article

References (81)

1. Abdi H. Bonferroni and Sidak corrections for multiple comparisons. In: Salkind N.J. (Ed). Encyclopedia of measurement and statistics (2007), Sage, Thousand Oaks, CA 100-251
2. Aggleton J.P., and Brown M.W. Contrasting hippocampal and perirhinal cortex function using immediate early gene imaging. Q J Exp Psychol B 58 (2005) 218-233
3. Baxter M.G. Effects of selective immunotoxic lesions on learning and memory. Methods Mol Biol 166 (2001) 249-265
4. Baxter M.G., Bucci D.J., Gorman L.K., Wiley R.G., and Gallagher M. Selective immunotoxic lesions of basal forebrain cholinergic cells: effects on learning and memory in rats. Behav Neurosci 109 (1995) 714-722
5. Berger-Sweeney J., Heckers S., Mesulam M.M., Wiley R.G., Lappi D.A., and Sharma M. Differential effects on spatial navigation of immunotoxin-induced cholinergic lesions of the medial septal area and nucleus basalis magnocellularis. J Neurosci 14 (1994) 4507-4519
6. Blandini F., Fancellu R., Armentero M.T., Tassorelli C., Greco R., Fornai F., and Nappi G. Unilateral lesion of the subthalamic nucleus enhances cortical fos expression associated with focally evoked seizures in the rat. Brain Res 1101 (2006) 145-150
7. Bonfanti L. PSA-NCAM in mammalian structural plasticity and neurogenesis. Prog Neurobiol 80 (2006) 129-164
8. Burk J.A., and Sarter M. Dissociation between the attentional functions mediated via basal forebrain cholinergic and GABAergic neurons. Neuroscience 105 (2001) 899-909
9. Buytaert K.A., Kline A.E., Montanez S., Likler E., Millar C.J., and Hernandez T.D. The temporal patterns of c-Fos and basic fibroblast growth factor expression following a unilateral anteromedial cortex lesion. Brain Res 894 (2001) 121-130
10. Cooper-Kuhn C.M., Winkler J., and Kuhn H.G. Decreased neurogenesis after cholinergic forebrain lesion in the adult rat. J Neurosci Res 77 (2004) 155-165
11. Cuello A.C., Garofalo L., Maysinger D., Pioro E.P., and Da Silva A.R. Injury and repair of central cholinergic neurons. Prog Brain Res 84 (1990) 301-311
12. Curran T., and Morgan J.I. Memories of fos. Bioessays 7 (1987) 255-258
13. Dragunow M., MacGibbon G.A., Lawlor P., Butterworth N., Connor B., Henderson C., Walton M., Woodgate A., Hughes P., and Faull R.L. Apoptosis, neurotrophic factors and neurodegeneration. Rev Neurosci 8 (1997) 223-265
14. Dragunow M., Goulding M., Faull R.L., Ralph R., Mee E., and Frith R. Induction of c-fos mRNA and protein in neurons and glia after traumatic brain injury: pharmacological characterization. Exp Neurol 107 (1990) 236-248
15. Emery D.L., Fulp C.T., Saatman K.E., Schutz C., Neugebauer E., and McIntosh T.K. Newly born granule cells in the dentate gyrus rapidly extend axons into the hippocampal CA3 region following experimental brain injury. J Neurotrauma 22 (2005) 978-988
16. Fibiger H.C. The organization and some projections of cholinergic neurons of the mammalian forebrain. Brain Res 257 (1982) 327-388
17. Fox G.B., Kjoller C., Murphy K.J., and Regan C.M. The modulations of NCAM polysialylation state that follow transient global ischemia are brief on neurons but enduring on glia. J Neuropathol Exp Neurol 60 (2001) 132-140
18. Galani R., Lehmann O., Bolmont T., Aloy E., Bertrand F., Lazarus C., Jeltsch H., and Cassel J.C. Selective immunolesions of CH4 cholinergic neurons do not disrupt spatial memory in rats. Physiol Behav 76 (2002) 75-90
19. Gaykema R.P., Nyakas C., Horvath E., Hersh L.B., Majtenyi C., and Luiten P.G. Cholinergic fiber aberrations in nucleus basalis lesioned rat and Alzheimer's disease. Neurobiol Aging 13 (1992) 441-448
20. Gibbs R.B., and Johnson D.A. Cholinergic lesions produce task-selective effects on delayed matching to position and configural association learning related to response pattern and strategy. Neurobiol Learn Mem 88 (2007) 19-32
21. Giovannelli L., Casamenti F., and Pepeu G. C-fos expression in the rat nucleus basalis upon excitotoxic lesion with quisqualic acid: a study in adult and aged animals. J Neural Transm 105 (1998) 935-948
22. Giovannelli L., Veltri M., Casamenti F., and Pepeu G. NGF treatment potentiates c-fos expression in the rat nucleus basalis upon excitotoxic lesion with quisqualic acid. Brain Res 853 (2000) 136-141
23. Gritti I., Henny P., Galloni F., Mainville L., Mariotti M., and Jones B.E. Stereological estimates of the basal forebrain cell population in the rat, including neurons containing choline acetyltransferase, glutamic acid decarboxylase or phosphate-activated glutaminase and colocalizing vesicular glutamate transporters. Neuroscience 143 (2006) 1051-1064
24. Haas C.A., Frotscher M., and Deller T. Differential induction of c-Fos, c-Jun and Jun B in the rat central nervous system following unilateral entorhinal cortex lesion. Neuroscience 90 (1999) 41-51
25. Harrell L.E., Parsons D., and Kolasa K. Hippocampal sympathetic ingrowth occurs following 192-IgG-Saporin administration. Brain Res 911 (2001) 158-162
26. Hartonian I., and de Lacalle S. Compensatory changes in cortical cholinergic innervation in the rat following an immunotoxic lesion. Restor Neurol Neurosci 23 (2005) 87-96
27. Heckers S., Ohtake T., Wiley R.G., Lappi D.A., Geula C., and Mesulam M.M. Complete and selective cholinergic denervation of rat neocortex and hippocampus but not amygdala by an immunotoxin against the p75 NGF receptor. J Neurosci 14 (1994) 1271-1289
28. Hengerer B., Lindholm D., Heumann R., Ruther U., Wagner E.F., and Thoenen H. Lesion-induced increase in nerve growth factor mRNA is mediated by c-fos. Proc Natl Acad Sci U S A 87 (1990) 3899-3903
29. Janisiewicz A.M., Jackson III O., Firoz E.F., and Baxter M.G. Environment-spatial conditional learning in rats with selective lesions of medial septal cholinergic neurons. Hippocampus 14 (2004) 265-273
30. Jin K., Peel A.L., Mao X.O., Xie L., Cottrell B.A., Henshall D.C., and Greenberg D.A. Increased hippocampal neurogenesis in Alzheimer's disease. Proc Natl Acad Sci U S A 101 (2004) 343-347
31. Johnson D.A., Zambon N.J., and Gibbs R.B. Selective lesion of cholinergic neurons in the medial septum by 192 IgG-saporin impairs learning in a delayed matching to position T-maze paradigm. Brain Res 943 (2002) 132-141
32. Katano H., Fujita K., Kato T., Asai K., Kawamura Y., Masago A., and Yamada K. Traumatic injury in vitro induces IEG mRNAs in cultured glial cells, suppressed by co-culture with neurons. Neuroreport 10 (1999) 2439-2448
33. Kempermann G., Gast D., and Gage F.H. Neuroplasticity in old age: sustained fivefold induction of hippocampal neurogenesis by long-term environmental enrichment. Ann Neurol 52 (2002) 135-143
34. Kirby B.P., and Rawlins J.N. The role of the septo-hippocampal cholinergic projection in T-maze rewarded alternation. Behav Brain Res 143 (2003) 41-48
35. Lehmann O., Jeltsch H., Lehnardt O., Pain L., Lazarus C., and Cassel J.C. Combined lesions of cholinergic and serotonergic neurons in the rat brain using 192 IgG-saporin and 5,7-dihydroxytryptamine: neurochemical and behavioural characterization. Eur J Neurosci 12 (2000) 67-79
36. Lindefors N., Hurd Y.L., O'Connor W.T., Brene S., Persson H., and Ungerstedt U. Amphetamine regulation of acetylcholine and gamma-aminobutyric acid in nucleus accumbens. Neuroscience 48 (1992) 439-448
37. Liu B.F., Gao E.J., Zeng X.Z., Ji M., Cai Q., Lu Q., Yang H., and Xu Q.Y. Proliferation of neural precursors in the subventricular zone after chemical lesions of the nigrostriatal pathway in rat brain. Brain Res 1106 (2006) 30-39
38. Macas J., Nern C., Plate K.H., and Momma S. Increased generation of neuronal progenitors after ischemic injury in the aged adult human forebrain. J Neurosci 26 (2006) 13114-13119
39. Marcus D.L., Strafaci J.A., Miller D.C., Masia S., Thomas C.G., Rosman J., Hussain S., and Freedman M.L. Quantitative neuronal c-fos and c-jun expression in Alzheimer's disease. Neurobiol Aging 19 (1998) 393-400
40. McGaughy J., Everitt B.J., Robbins T.W., and Sarter M. The role of cortical cholinergic afferent projections in cognition: impact of new selective immunotoxins. Behav Brain Res 115 (2000) 251-263
41. McGaughy J., Dalley J.W., Morrison C.H., Everitt B.J., and Robbins T.W. Selective behavioral and neurochemical effects of cholinergic lesions produced by intrabasalis infusions of 192 IgG-saporin on attentional performance in a five-choice serial reaction time task. J Neurosci 22 (2002) 1905-1913
42. Mikkonen M., Soininen H., Tapiola T., Alafuzoff I., and Miettinen R. Hippocampal plasticity in Alzheimer's disease: changes in highly polysialylated NCAM immunoreactivity in the hippocampal formation. Eur J Neurosci 11 (1999) 1754-1764
43. Mohapel P., Leanza G., Kokaia M., and Lindvall O. Forebrain acetylcholine regulates adult hippocampal neurogenesis and learning. Neurobiol Aging 26 (2005) 939-946
44. Morgan J.I., and Curran T. Calcium and proto-oncogene involvement in the immediate-early response in the nervous system. Ann N Y Acad Sci 568 (1989) 283-290
45. Lalonde R. The neurobiological basis of spontaneous alternation. Neurosci Biobehav Rev 26 (2002) 91-104
46. Paban V., Alescio-Lautier B., Devigne C., and Soumireu-Mourat B. Fos protein expression induced by intracerebroventricular injection of vasopressin in unconditioned and conditioned mice. Brain Res 825 (1999) 1115-1131
47. Paban V., Jaffard M., Chambon C., Malafosse M., and Alescio-Lautier B. Time course of behavioral changes following basal forebrain cholinergic damage in rats: Environmental enrichment as a therapeutic intervention. Neuroscience 132 (2005) 13-32
48. Paban V., Chambon C., Jaffard M., and Alescio-Lautier B. Behavioral effects of basal forebrain cholinergic lesions in young adult and aging rats. Behav Neurosci 119 (2005) 933-945
49. Page K.J., Saha A., and Everitt B.J. Differential activation and survival of basal forebrain neurons following infusions of excitatory amino acids: studies with the immediate early gene c-fos. Exp Brain Res 93 (1993) 412-422
50. Parent M.B., and Baxter M.G. Septohippocampal acetylcholine: involved in but not necessary for learning and memory?. Learn Mem 11 (2004) 9-20
51. Paxinos G., and Watson C. The rat brain in stereotaxic coordinates. 4th ed. (1998), Academic Press, San Diego
52. Perry T., Hodges H., and Gray J.A. Behavioural, histological and immunocytochemical consequences following 192 IgG-saporin immunolesions of the basal forebrain cholinergic system. Brain Res Bull 54 (2001) 29-48
53. Pizzo D.P., Waite J.J., Thal L.J., and Winkler J. Intraparenchymal infusions of 192 IgG-saporin: Development of a method for selective and discrete lesioning of cholinergic basal forebrain nuclei. J Neurosci Methods 91 (1999) 9-19
54. Pizzo D.P., Thal L.J., and Winkler J. Mnemonic deficits in animals depend upon the degree of cholinergic deficit and task complexity. Exp Neurol 177 (2002) 292-305
55. Raivich G., and Behrens A. Role of the AP-1 transcription factor c-Jun in developing, adult and injured brain. Prog Neurobiol 78 (2006) 347-363
56. Richardson C.L., Tate W.P., Mason S.E., Lawlor P.A., Dragunow M., and Abraham W.C. Correlation between the induction of an immediate early gene, zif/268, and long-term potentiation in the dentate gyrus. Brain Res 580 (1992) 147-154
57. Rossner S., Perez-Polo J.R., Wiley R.G., Schliebs R., and Bigl V. Differential expression of immediate early genes in distinct layers of rat cerebral cortex after selective immunolesion of the forebrain cholinergic system. J Neurosci Res 38 (1994) 282-293
58. Rossner S., Schliebs R., Hartig W., Perez-Polo J.R., and Bigl V. Selective induction of c-Jun and NGF in reactive astrocytes after cholinergic degenerations in rat basal forebrain. Neuroreport 8 (1997) 2199-2202
59. Sato K., Hayashi T., Sasaki C., Iwai M., Li F., Manabe Y., Seki T., and Abe K. Temporal and spatial differences of PSA-NCAM expression between young-adult and aged rats in normal and ischemic brains. Brain Res 922 (2001) 135-139
60. Scheiderer C.L., McCutchen E., Thacker E.E., Kolasa K., Ward M.K., Parsons D., Harrell L.E., Dobrunz L.E., and McMahon L.L. Sympathetic sprouting drives hippocampal cholinergic reinnervation that prevents loss of a muscarinic receptor-dependent long-term depression at CA3-CA1 synapses. J Neurosci 26 (2006) 3745-3756
61. Schreiber S.S., and Baudry M. Selective neuronal vulnerability in the hippocampus: a role for gene expression?. Trends Neurosci 18 (1995) 446-451
62. Seki T., and Arai Y. Highly polysialylated neural cell adhesion molecule (NCAM-H) is expressed by newly generated granule cells in the dentate gyrus of the adult rat. J Neurosci 13 (1993) 2351-2358
63. Seki T., and Arai Y. Temporal and spacial relationships between PSA-NCAM-expressing, newly generated granule cells, and radial glia-like cells in the adult dentate gyrus. J Comp Neurol 410 (1999) 503-513
64. Seki T. Expression patterns of immature neuronal markers PSA-NCAM, CRMP-4 and NeuroD in the hippocampus of young adult and aged rodents. J Neurosci Res 70 (2002) 327-334
65. Thakur M.K., Oka T., and Natori Y. Gene expression and aging. Mech Ageing Dev 66 (1993) 283-298
66. Teather L.A., Packard M.G., Smith D.E., Ellis-Behnke R.G., and Bazan N.G. Differential induction of c-Jun and Fos-like proteins in rat hippocampus and dorsal striatum after training in two water maze tasks. Neurobiol Learn Mem 84 (2005) 75-84
67. Torres E.M., Perry T.A., Blockland A., Wilkinson L.S., Wiley R.G., Lappi D.A., and Dunnet S.B. Behavioural, histochemical and biochemical consequences of selective immunolesions in discrete regions of the basal forebrain cholinergic system. Neuroscience 63 (1994) 95-122
68. van der Staay F.J., Bouger P., Lehmann O., Lazarus C., Cosquer B., Koenig J., Stump V., and Cassel J.C. Long-term effects of immunotoxic cholinergic lesions in the septum on acquisition of the cone-field task and noncognitive measures in rats. Hippocampus 16 (2006) 1061-1079
69. Waite J.J., Wardlow M.L., Chen A.C., Lappi D.A., Wiley R.G., and Thal L.J. Time course of cholinergic and monoaminergic changes in rat brain after immunolesioning with 192 IgG-saporin. Neurosci Lett 169 (1994) 154-158
70. Walsh T.J., and Opello K.D. Neuroplasticity, the aging brain, and Alzheimer's disease. Neurotoxicology 13 (1992) 101-110
71. Walsh T.J., Herzog C.D., Gandhi C., Stackman R.W., and Wiley R.G. Injection of IgG 192-saporin into the medial septum produces cholinergic hypofunction and dose-dependent working memory deficits. Brain Res 726 (1996) 69-79
72. Wenk G.L., Stoehr J.D., Quintana G., Mobley S., and Wiley R.G. Behavioral, biochemical, histological, and electrophysiological effects of 192 IgG-saporin injections into the basal forebrain of rats. J Neurosci 14 (1994) 5986-5995
73. Wenk G.L., Zajaczkowski W., and Danysz W. Neuroprotection of acetylcholinergic basal forebrain neurons by memantine and neurokinin B. Behav Brain Res 83 (1997) 129-133
74. Whitehouse P.J., Struble R.G., Clark A.W., and Price D.L. Alzheimer disease: plaques, tangles, and the basal forebrain. Ann Neurol 12 (1982) 494-501
75. Wiley R.G. Neural lesioning with ribosome-inactivating proteins: suicide transport and immunolesioning. Trends Neurosci 15 (1992) 285-290
76. Wrenn C.C., and Wiley R.G. The behavioral functions of the cholinergic basal forebrain: lessons from 192 IgG-saporin. Int J Dev Neurosci 16 (1998) 595-602
77. Yasoshima Y., Scott T.R., and Yamamoto T. Memory-dependent c-Fos expression in the nucleus accumbens and extended amygdala following the expression of a conditioned taste aversive in the rat. Neuroscience 141 (2006) 35-45
78. Zhang B., Wang R.Z., Lian Z.G., Song Y., and Yao Y. Experimental study on plasticity of proliferated neural stem cells in adult rats after cerebral infarction. Chin Med Sci J 21 (2006) 184-188
79. Zhang P., Hirsch E.C., Damier P., Duyckaerts C., and Javoy-Agid F. c-fos Protein-like immunoreactivity: distribution in the human brain and over-expression in the hippocampus of patients with Alzheimer's disease. Neuroscience 46 (1992) 9-21
80. Zimmer L.A., Ennis M., Wiley R.G.G., and Shipley M.T. Nerve gas-induced seizures: role of acetylcholine in the rapid induction of Fos and glial fibrillary acidic protein in piriform cortex. J Neurosci 18 (1998) 3897-3908
81. Zuber C., Lackie P.M., Catterall W.A., and Roth J. Polysialic acid is associated with sodium channels and the neural cell adhesion molecule N-CAM in adult rat brain. J Biol Chem 267 (1992) 9965-9971