Chronic difluoromethylornithine treatment impairs spatial learning and memory in rats

Pharmacology Biochemistry and Behavior

Volumn 100, Issue 3, 2012, Pages 464-473

  Gupta, Neeraj ^a,b   Zhang, Hu ^b   Liu, Ping ^a,b  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

Growth; Hippocampus; Putrescine; Spatial learning and memory; Spermidine; Spermine

Indexed keywords

4 AMINOBUTYRIC ACID; AGMATINE; EFLORNITHINE; GLUTAMIC ACID; PUTRESCINE; SPERMIDINE; SPERMINE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; DENTATE GYRUS; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA2 REGION; HIPPOCAMPAL CA3 REGION; LEARNING DISORDER; LONG TERM CARE; MALE; MAZE TEST; MEMORY DISORDER; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; TASK PERFORMANCE;

AGMATINE; ANIMALS; ANTINEOPLASTIC AGENTS; BEHAVIOR, ANIMAL; EFLORNITHINE; ENZYME INHIBITORS; HIPPOCAMPUS; LEARNING DISORDERS; MALE; MAZE LEARNING; MEMORY; MEMORY DISORDERS; ORGAN SPECIFICITY; ORNITHINE DECARBOXYLASE; PREFRONTAL CORTEX; PUTRESCINE; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; SPATIAL BEHAVIOR; SPERMIDINE; TOXICITY TESTS, CHRONIC;

ANIMALIA; RATTUS;

EID: 80155125095     PISSN: 00913057     EISSN: 18735177     Source Type: Journal    
DOI: 10.1016/j.pbb.2011.10.011     Document Type: Article

References (62)

1. J.B. Aimone, W. Deng, and F.H. Gage Resolving new memories: a critical look at the dentate gyrus, adult neurogenesis, and pattern separation Neuron 70 2011 589 596
2. J. Altman, and S.A. Bayer Mosaic organization of the hippocampal neuroepithelium and the multiple germinal sources of dentate granule cells J Comp Neurol 301 1990 325 342 (Pubitemid 20368498)
3. J.P. Andrade, N.V. Lukoyanov, and M.M. Paula-Barbosa Chronic food restriction is associated with subtle dendritic alterations in granule cells of the rat hippocampal formation Hippocampus 12 2002 149 164 (Pubitemid 34436700)
4. N. Babbar, and E.W. Gerner Targeting polyamines and inflammation for cancer prevention Recent Results Cancer Res 188 2011 49 64
5. D.H. Bergin, and P. Liu Agmatine protects against beta-amyloid25-35- induced memory impairments in the rat Neuroscience 169 2010 794 811
6. A.P. Brown, R.L. Morrissey, J.A. Crowell, and B.S. Levine Difluoromethylornithine in combination with tamoxifen in female rats: 13-week oral toxicity study Cancer Chemother Pharmacol 44 1999 475 483 (Pubitemid 29501017)
7. D.P. Cain Testing the NMDA, long-term potentiation, and cholinergic hypotheses of spatial learning Neurosci Biobehav Rev 22 1998 181 193 (Pubitemid 28194377)
8. L.J. Cizek, and M.R. Nocenti Relationship between water and food ingestion in the rat Am J Physiol 208 1965 615 620
9. C.D. Clelland, M. Choi, C. Romberg, G.D. Clemenson Jr., A. Fragniere, and P. Tyers A functional role for adult hippocampal neurogenesis in spatial pattern separation Science 325 2009 210 213
10. I. Driscoll, S.R. Howard, J.C. Stone, M.H. Monfils, B. Tomanek, and W.M. Brooks The aging hippocampus: a multi-level analysis in the rat Neuroscience 139 2006 1173 1185
11. D. Dupret, J.M. Revest, M. Koehl, F. Ichas, F. De Giorgi, and P. Costet Spatial relational memory requires hippocampal adult neurogenesis PLoS One 3 2008 e1959
12. S.A. Ferguson, and A.M. Cada Developmental treatment with difluoromethylornithine has few effects on behavior or body weight in Sprague-Dawley rats Neurotoxicol Teratol 26 2004 83 93 (Pubitemid 38299112)
13. F.H. Gage Neurogenesis in the adult brain J Neurosci 22 2002 612 613 (Pubitemid 34141738)
14. N. Gupta, H. Zhang, and P. Liu Behavioral and neurochemical effects of acute putrescine depletion by difluoromethylornithine in rats Neuroscience 161 2009 691 706
15. A. Halaris, and J. Piletz Agmatine: metabolic pathway and spectrum of activity in brain CNS Drugs 21 2007 885 900 (Pubitemid 47557104)
16. J. Hoge, and R.P. Kesner Role of CA3 and CA1 subregions of the dorsal hippocampus on temporal processing of objects Neurobiol Learn Mem 88 2007 225 231 (Pubitemid 47241225)
17. O.A. Jänne, A. Crozat, J. Palvimo, and L.M. Eisenberg Androgen-regulation of ornithine decarboxylase and S-adenosylmethionine decarboxylase genes J Steroid Biochem Mol Biol 40 1991 307 315
18. G. Kempermann, L. Wiskott, and F.H. Gage Functional significance of adult neurogenesis Curr Opin Neurobiol 14 2004 186 191 (Pubitemid 38479935)
19. R. Kesner Behavioral functions of the CA3 subregion of the hippocampus Learn Mem 14 2007 771 781 (Pubitemid 350172775)
20. R.P. Kesner, I. Lee, and P. Gilbert A behavioral assessment of hippocampal function based on a subregional analysis Rev Neurosci 15 2004 333 351 (Pubitemid 39536383)
21. R.P. Kesner, M.R. Hunsaker, and M.W. Warthen The CA3 subregion of the hippocampus is critical for episodic memory processing by means of relational encoding in rats Behav Neurosci 122 2008 1217 1225
22. B. Leitch, O. Shevtsova, K. Reusch, D.H. Bergin, and P. Liu Spatial learning-induced increase in agmatine levels at hippocampal CA1 synapses Synapse 65 2011 146 153
23. Y. Lin, J.C. Liu, X.J. Zhang, G.W. Li, L.N. Wang, and Y.H. Xi Downregulation of the ornithine decarboxylase/polyamine system inhibits angiotensin-induced hypertrophy of cardiomyocytes through the NO/cGMP-dependent protein kinase type-I pathway Cell Physiol Biochem 25 2010 443 450
24. P. Liu, and D.H. Bergin Differential effects of intracerebroventricular microinfusion of agmatine on spatial working and reference memory in the rat Neuroscience 159 2009 951 961
25. P. Liu, and D.K. Bilkey The effects of excitotoxic lesions centered on the hippocampus or perirhinal cortex in object recognition and spatial memory tasks Behav Neurosci 115 2001 94 111 (Pubitemid 32185154)
26. P. Liu, and N.D. Collie Behavioral effects of agmatine in naive rats are task- and delay-dependent Neuroscience 163 2009 82 96
27. P. Liu, P.F. Smith, I. Appleton, C.L. Darlington, and D.K. Bilkey Regional variations and age-related changes in nitric oxide synthase and arginase in the sub-regions of the hippocampus Neuroscience 119 2003 679 687 (Pubitemid 36694796)
28. P. Liu, P.F. Smith, I. Appleton, C.L. Darlington, and D.K. Bilkey Potential involvement of NOS and arginase in age-related behavioural impairments Exp Gerontol 39 2004 1207 1222 (Pubitemid 39024370)
29. P. Liu, P.F. Smith, I. Appleton, C.L. Darlington, and D.K. Bilkey Age-related changes in nitric oxide synthase and arginase in the rat prefrontal cortex Neurobiol Aging 25 2004 547 552 (Pubitemid 38317353)
30. P. Liu, P.F. Smith, I. Appleton, C.L. Darlington, and D.K. Bilkey Hippocampal nitric oxide synthase and arginase and age-associated behavioural deficits Hippocampus 15 2005 642 655 (Pubitemid 41149585)
31. P. Liu, N.D. Collie, S. Chary, Y. Jing, and H. Zhang Spatial learning results in elevated agmatine levels in the rat brain Hippocampus 18 2008 1094 1098
32. P. Liu, S. Chary, R. Devaraj, Y. Jing, C.L. Darlington, and P.F. Smith Effects of aging on agmatine levels in memory-associated brain structures Hippocampus 18 2008 853 856
33. P. Liu, N. Gupta, Y. Jing, and H. Zhang Age-related changes in polyamines in memory-associated brain structures in rats Neuroscience 155 2008 789 796
34. P. Liu, Y. Jing, N.D. Collie, S. Chary, and H. Zhang Memory-related changes in L-citrulline and agmatine in the rat brain Hippocampus 19 2009 597 602
35. P. Liu, Y. Jing, and H. Zhang Age-related changes in arginine and its metabolites in memory-associated brain structures Neuroscience 164 2009 611 628
36. P. Liu, H. Zhang, R. Devaraj, G.S. Ganesalingam, and P.F. Smith A multivariate analysis of the effects of aging on glutamate, GABA and arginine metabolites in the rat vestibular nucleus Hear Res 269 2010 122 133
37. J. Malaterre, C. Strambi, A. Aouane, A. Strambi, G. Rougon, and M. Cayre A novel role for polyamines in adult neurogenesis in rodent brain Eur J Neurosci 20 2004 317 330 (Pubitemid 38969617)
38. M. McWilliams, G. Chen, and L. Fechter Characterization of the ototoxicity of difluoromethylornithine and its enantiomers Toxicol Sci 56 2000 124 132 (Pubitemid 30441471)
39. B.W. Metcalf, P. Bey, and C. Danzin Catalytic irreversible inhibition of mammalian ornithine decarboxylase by substrate and product analogues J Am Chem Soc 100 1978 2551 2563
40. F.L. Meyskens Jr., C.E. McLaren, D. Pelot, S. Fujikawa-Brooks, P.M. Carpenter, and E. Hawk Difluoromethylornithine plus sulindac for the prevention of sporadic colorectal adenomas: a randomized placebo-controlled, double-blind trial Cancer Prev Res (Phila) 1 2008 32 38
41. C. Moinard, L. Cynober, and J.P. de Bandt Polyamines: metabolism and implications in human diseases Clin Nutr 24 2005 184 197 (Pubitemid 40392801)
42. D.M. Morgan Difluoromethylornithine (DFMO), an inhibitor of nitrite production by macrophages? Biochem Soc Trans 22 1994 389S (Pubitemid 24373108)
43. S.M. Oredsson Polyamine dependence of normal cell-cycle progression Biochem Soc Trans 31 2003 366 370 (Pubitemid 36520678)
44. D.M. Rock, and R.L. Macdonald Polyamine regulation of N-methyl-D-aspartate receptor channels Annu Rev Pharmacol Toxicol 35 1995 463 482
45. L.N. Rotta, A.P. Schmidt, T. Mello e Souza, C.W. Nogueira, K.B. Souza, and I.A. Izquierdo Effects of undernutrition on glutamatergic parameters in rat brain Neurochem Res 28 2003 1181 1186 (Pubitemid 36734549)
46. J. Satriano Agmatine: at the crossroads of the arginine pathways Ann N Y Acad Sci 1009 2003 34 43 (Pubitemid 38265088)
47. U. Schmitt, and C. Hiemke Combination of open field and elevated plus-maze: a suitable test battery to assess strain as well as treatment differences in rat behavior Prog Neuropsychopharmacol Biol Psychiatry 22 1998 1197 1215 (Pubitemid 28511595)
48. S. Seo, P. Liu, and B. Leitch Spatial learning-induced accumulation of agmatine and glutamate at hippocampal CA1 synaptic terminals Neuroscience 192 2011 28 36
49. A.R. Simoneau, E.W. Gerner, R. Nagle, A. Ziogas, S. Fujikawa-Brooks, and H. Yerushalmi The effect of difluoromethylornithine on decreasing prostate size and polyamines in men: results of a year-long phase IIb randomized placebo-controlled chemoprevention trial Cancer Epidemiol Biomarkers Prev 17 2008 292 299 (Pubitemid 351272778)
50. T.A. Slotkin, F.J. Seidler, P.A. Trepanier, W.L. Whitmore, L. Lerea, and G.A. Barnes Ornithine decarboxylase and polyamines in tissues of the neonatal rat: effects of alpha-difluoromethylornithine, a specific, irreversible inhibitor of ornithine decarboxylase J Pharmacol Exp Ther 222 1982 741 745 (Pubitemid 12018856)
51. M. Sparapani, M. Virgili, M. Caprini, F. Facchinetti, E. Ciani, and A. Contestabile Effects of gestational or neonatal treatment with alpha-difluoromethylornithine on ornithine decarboxylase and polyamines in developing rat brain and on adult rat neurochemistry Exp Brain Res 108 1996 433 440 (Pubitemid 26095296)
52. L.R. Squire, C.E. Stark, and R.E. Clark The medial temporal lobe Annu Rev Neurosci 27 2004 279 306 (Pubitemid 39050405)
53. R.J. Sutherland, I.Q. Whishaw, and B. Kolb A behavioural analysis of spatial localization following electrolytic, kainate- or colchicine-induced damage to the hippocampal formation in the rat Behav Brain Res 7 1983 133 153 (Pubitemid 13184613)
54. H. Van Praag, A.F. Schinder, B.R. Christie, N. Toni, T.D. Palmer, and F.H. Gage Functional neurogenesis in the adult hippocampus Nature 415 2002 1030 1034 (Pubitemid 34193451)
55. H.M. Wallace The physiological role of the polyamines Eur J Clin Invest 30 2000 1 3
56. H.M. Wallace, A.V. Fraser, and A. Hughes A perspective of polyamine metabolism Biochem J 376 2003 1 14 (Pubitemid 37487199)
57. H. Wati, K. Kudo, C. Qiao, T. Kuroki, and S. Kanba A decreased survival of proliferated cells in the hippocampus is associated with a decline in spatial memory in aged rats Neurosci Lett 399 2006 171 174
58. K. Williams Interactions of polyamines with ion channels Biochem J 325 1997 289 297 (Pubitemid 27338704)
59. K. Williams, A.M. Zappia, D.B. Pritchett, Y.M. Shen, and P.B. Molinoff Sensitivity of the N-methyl-D-aspartate receptor to polyamines is controlled by NR2 subunits Mol Pharmacol 45 1994 803 809 (Pubitemid 24155769)
60. G. Wu, and S.M. Morris Jr. Arginine metabolism: nitric oxide and beyond Biochem J 336 1998 1 17 (Pubitemid 28532555)
61. G.F. Xavier, F.J. Oliveira-Filho, and A.M. Santos Dentate gyrus-selective colchicine lesion and disruption of performance in spatial tasks: difficulties in "place strategy" because of a lack of flexibility in the use of environmental cues? Hippocampus 9 1999 668 681 (Pubitemid 30018858)
62. J.F. Zolman Biostatistics: Experimental Design and Statistical Inference 1993 Oxford University Press Oxford