Disruption of the development of cholinergic-induced translocation/ activation of PKC isoforms after prenatal heroin exposure

Brain Research Bulletin

Volumn 69, Issue 2, 2006, Pages 174-181

  Huleihel, Rabab ^a   Yanai, Joseph ^a,b  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Heroin; Hippocampal cholinergic innervation; Mice; PKC; Prenatal exposure

Indexed keywords

CARBACHOL; CHOLINERGIC RECEPTOR; DIAMORPHINE; PROTEIN KINASE C; PROTEIN KINASE C ALPHA; PROTEIN KINASE C BETA; PROTEIN KINASE C GAMMA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR DISORDER; CELL ACTIVATION; CHOLINERGIC ACTIVITY; CHOLINERGIC STIMULATION; CONTROLLED STUDY; DESENSITIZATION; DISEASE COURSE; DRUG EFFECT; DRUG EXPOSURE; ENZYME ACTIVATION; ENZYME ACTIVITY; FEMALE; HIPPOCAMPUS; MALE; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; PERINATAL PERIOD; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; TERATOGENESIS;

ACETYLCHOLINE; ANALGESICS, OPIOID; ANIMALS; ANIMALS, NEWBORN; CHOLINERGIC AGONISTS; CHOLINERGIC FIBERS; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; FEMALE; HEROIN; HEROIN DEPENDENCE; HIPPOCAMPUS; MALE; MICE; NEURAL PATHWAYS; ORGAN CULTURE TECHNIQUES; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PROTEIN ISOFORMS; PROTEIN KINASE C; PROTEIN TRANSPORT; RECEPTORS, CHOLINERGIC; SEPTAL NUCLEI;

EID: 33644859480     PISSN: 03619230     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainresbull.2005.11.023     Document Type: Article

References (53)

1. F. Angenstein, M. Hirschfelder, and S. Staak Activation of metabotropic glutamate receptors increases endogenous protein kinase C substrate phosphorylation in adult hippocampal slices Brain Res. 745 1-2 1997 46 54
2. F. Angenstein, G. Riedel, K.G. Reyman, and S. Staak Transient translocation of protein kinase Cgamma in hippocampal long-term potentiation depends on activation of metabotropic glutamate receptors Neuroscience 93 4 1999 1289 1295
3. F. Angenstein, and S. Staak Receptor-mediated activation of protein kinase C in hippocampal long-term potentiation: facts, problems and implications Prog. Neuropsychopharmacol. Biol. Psychiatry 21 3 1997 427 454
4. E.S. Bachman, J. Berger-Sweeney, J.T. Coyle, and C.F. Hohmann Developmental regulation of adult cortical morphology and behavior: an animal model for mental retardation Int. J. Dev. Neurosci. 12 4 1994 239 253
5. M. Barrios, and S. Liljequist Developmental changes in glutamate receptor-activated translocation of protein kinase C in cerebellar granule neurons Brain Res. Dev. Brain Res. 94 1 1996 22 30
6. F. Battaini, S. Elkabes, S. Bergamaschi, V. Ladisa, L. Lucchi, P. De Graan, T. Schuurman, W.C. Wetsel, M. Trabucchi, and S. Govoni Protein kinase C activity, translocation, and conventional isoforms in aging rat brain Neurobiol. Aging 16 1995 137 148
7. A. Beer, T.A. Slotkin, F.J. Seidler, and J. Yanai Nicotine therapy in adulthood reverses the synaptic and behavioral deficits elicited by prenatal exposure to phenobarbital Neuropsychopharmacology 30 2005 156 165
8. H.J. Beldhuis, H.G. Everts, E.A. Van der Zee, P.G. Luiten, and B. Bohus Amygdala kindling-induced seizures selectively impair spatial memory. 1. Behavioral characteristics and effects on hippocampal neuronal protein kinase C isoforms Hippocampus 2 4 1992 397 409
9. T.V. Bliss, and G.L. Collingridge A synaptic model of memory: long-term potentiation in the hippocampus Nature 361 6407 1993 31 39
10. M.M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72 1976 248 254
11. W.N. Burnette "Western blotting": electrophoretic transfer of proteins from sodium dodecyl sulfate-polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A Anal. Biochem. 112 2 1981 195 203
12. P.J. Colombo, W.C. Wetsel, and M. Gallagher Spatial memory is related to hippocampal subcellular concentrations of calcium-dependent protein kinase C isoforms in young and aged rats Proc. Natl. Acad. Sci. U.S.A. 94 25 1997 14195 14199
13. L. Coussens, L. Rhee, P.J. Parker, and A. Ullrich Alternative splicing increases the diversity of the human protein kinase C family DNA 6 5 1987 389 394
14. A.J. Eisch, M. Barrot, C.A. Schad, D.W. Self, and E.J. Nestler Opiates inhibit neurogenesis in the adult rat hippocampus Proc. Natl. Acad. Sci. U.S.A. 97 13 2000 7579 7584
15. M.S. Haas, and L.A. Dokas Muscarinic receptor- and phorbol ester-stimulated phosphorylation of protein kinase C substrates in adult and neonatal cortical slices Dev. Brain Res. 114 1999 89 98
16. T. Hashimoto, K. Ase, S. Sawamura, U. Kikkawa, N. Saito, C. Tanaka, and Y. Nishizuka Postnatal development of a brain-specific subspecies of protein kinase C in rat J. Neurosci. 8 1988 1678 1683
17. N. Haykal-Coates, T.J. Shafer, W.R. Mundy, and S. Barone Jr. Effects of gestational methylmercury exposure on immunoreactivity of specific isoforms of PKC and enzyme activity during post-natal development of the rat brain Brain Res. Dev. Brain Res. 109 1 1998 33 49
18. C.F. Hohmann, A.R. Brooks, and J.T. Coyle Neonatal lesions of the basal forebrain cholinergic neurons result in abnormal cortical development Brain Res. 470 2 1988 253 264
19. C.F. Hohmann, L. Wilson, and J.T. Coyle Efferent and afferent connections of mouse sensory-motor cortex following cholinergic deafferentation at birth Cereb. Cortex 1 2 1991 158 172
20. R.J. Hussain, P.J. Parsons, and D.O. Carpenter Effects of lead on long-term potentiation in hippocampal CA3 vary with age Brain Res. Dev. Brain Res. 121 2 2000 243 252
21. M. Izrael, E.A. Van der Zee, T.A. Slotkin, and J. Yanai Cholinergic synaptic signaling mechanisms underlying behavioral teratogenicity: effects of nicotine, chlorpyrifos, and heroin converge on protein kinase C translocation in the intermedial part of the hyperstriatum ventrale and on imprinting behavior in an avian model J. Neurosci. Res. 78 2004 499 507
22. X. Jiang, M.U. Naik, J. Hrabe, and T.C. Sacktor Developmental expression of the protein kinase C family in rat hippocampus Brain Res. Dev. Brain Res. 78 2 1994 291 295
23. Y. Kosaka, K. Ogita, K. Ase, H. Nomura, U. Kikkawa, and Y. Nishizuka The heterogeneity of protein kinase C in various rat tissues Biochem. Biophys. Res. Commun. 151 3 1988 973 981
24. J.M. Lauder, J. Liu, L. Devaud, and A.L. Morrow GABA as a trophic factor for developing monoamine neurons Perspect. Dev. Neurobiol. 5 2-3 1998 247 259
25. L. Lichtblau, and S.B. Sparber Opioids and development: a perspective on experimental models and methods Neurobehav. Toxicol. Teratol. 6 1 1984 3 8
26. K. Mahadev, and M.C. Vemuri Selective changes in protein kinase C isoforms and phosphorylation of endogenous substrate proteins in rat cerebral cortex during pre- and postnatal ethanol exposure Arch. Biochem. Biophys. 356 2 1998 249 257
27. E. Masliah, G. Cole, S. Shimohama, L. Hansen, R. DeTeresa, R.D. Terry, and T. Saitoh Differential involvement of protein kinase C isozymes in Alzheimer's disease J. Neurosci. 10 7 1990 2113 2124
28. G.E. McClearn, J.R. Wilson, and W. Meredith The use of isogenic and heterogenic mouse stock in behavioral research G. Lindzey D.D. Thiessen Contributions to Behavior-Genetic Analysis; The Mouse as a Prototype 1970 Appleton-Century-Crofts New York 3 22
29. M.U. Naik, E. Benedikz, I. Hernandez, J. Libien, J. Hrabe, M. Valsamis, D. Dow-Edwards, M. Osman, and T.C. Sacktor Distribution of protein kinase M-zeta and the complete protein kinase C isoform family in the rat brain J. Comp. Neurol. 426 2000 243 258
30. A.C. Newton Protein kinase C: structure, function, and regulation J. Biol. Chem. 270 48 1995 28495 28498
31. A.C. Newton Protein kinase C: structural and spatial regulation by phosphorylation, cofactors, and macromolecular interactions Chem. Rev. 101 8 2001 2353 2364
32. A. Ornoy The impact of intrauterine exposure versus postnatal environment in neurodevelopmental toxicity: long-term neurobehavioral studies in children at risk for developmental disorders Toxicol. Lett. 140-141 2003 171 181
33. A. Pascale, S. Govoni, and F. Battaini Age-related alteration of PKC, a key enzyme in memory processes: physiological and pathological examples Mol. Neurobiol. 16 1 1998 49 62
34. E.P. Riley, and S. Barron The behavioral and neuroanatomical effects of prenatal alcohol exposure in animals Ann. N. Y. Acad. Sci. 562 1989 173 177
35. P.M. Rodier Critical periods for behavioral anomalies in mice Environ. Health Perspect. 18 1976 79 83
36. Y. Rogel-Fuchs, E.A. Zahalka, and J. Yanai Reversal of early phenobarbital-induced cholinergic and related behavioral deficits by neuronal grafting Brain Res. Bull. 33 3 1994 273 279
37. M.P. Roisin, and G. Barbin Differential expression of PKC isoforms in hippocampal neuronal cultures: modifications after basic FGF treatment Neurochem. Int. 30 3 1997 261 270
38. J. Salles, M.A. Wallace, and J.N. Fain Modulation of the phospholipase C activity in rat brain cortical membranes by simultaneous activation of distinct monoaminergic and cholinergic muscarinic receptors Brain Res. Mol. Brain Res. 20 1-2 1993 111 117
39. H. Shahak, T.A. Slotkin, and J. Yanai Alterations in PKCgamma in the mouse hippocampus after prenatal exposure to heroin: a link from cell signaling to behavioral outcome Brain Res. Dev. Brain Res. 140 1 2003 117 125
40. M.S. Shearman, Z. Naor, U. Kikkawa, and Y. Nishizuka Differential expression of multiple protein kinase C subspecies in rat central nervous tissue Biochem. Biophys. Res. Commun. 147 3 1987 911 919
41. N.M. Sposi, L. Bottero, G. Cossu, G. Russo, U. Testa, and C. Peschle Expression of protein kinase C genes during ontogenic development of the central nervous system Mol. Cell. Biol. 9 5 1989 2284 2288
42. R.A. Steingart, M. Abu-Roumi, M.E. Newman, W.F. Silverman, T.A. Slotkin, and J. Yanai Neurobehavioral damage to cholinergic systems caused by prenatal exposure to heroin or phenobarbital: cellular mechanisms and the reversal of deficits by neural grafts Brain Res. Dev. Brain Res. 122 2 2000 125 133
43. R.A. Steingart, J. Barg, J. Maslaton, M. Nesher, and J. Yanai Pre- and postsynaptic alterations in the septohippocampal cholinergic innervations after prenatal exposure to drugs Brain Res. Bull. 46 3 1998 203 209
44. R.A. Steingart, W.F. Silverman, S. Barron, T.A. Slotkin, Y. Awad, and J. Yanai Neural grafting reverses prenatal drug-induced alterations in hippocampal PKC and related behavioral deficits Brain Res. Dev. Brain Res. 125 1-2 2000 9 19
45. H. Towbin, T. Staehelin, and J. Gordon Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications Proc. Natl. Acad. Sci. U.S.A. 76 9 1979 4350 4354
46. S.Z. Xu, L. Bullock, C.J. Shan, K. Cornelius, and B. Rajanna PKC isoforms were reduced by lead in the developing rat brain Int. J. Dev. Neurosci. 23 1 2005 53 64
47. J. Yanai, Y. Avraham, S. Levy, J. Maslaton, C.G. Pick, Y. Rogel-Fuchs, and E.A. Zahalka Alterations in septohippocampal cholinergic innervations and related behaviors after early exposure to heroin and phencyclidine Brain Res. Dev. Brain Res. 69 2 1992 207 214
48. J. Yanai, T. Ben-Hur, S. Katz, and T. Ben-Shaanan Heroin neurobehavioral teratogenicity in mice is reversed by neural progenitor grafts Proceedings of the Satellite Meeting of The International Society for Neurochemistry/European Society for Neurochemistry 2005
49. J. Yanai, R. Huleihel, M. Izrael, S. Metsuyanim, H. Shahak, O. Vatury, and S.P. Yaniv Functional changes after prenatal opiate exposure related to opiate receptors' regulated alterations in cholinergic innervation Int. J. Neuropsychopharmacol. 6 3 2003 253 265
50. S.P. Yaniv, Z. Naor, and J. Yanai Prenatal heroin exposure alters cholinergic receptor stimulated translocation and basal levels of the PKCbetaII and PKCgamma isoforms Brain Res. Bull. 63 2004 339 349
51. I.S. Zagon, P.J. McLaughlin, and E. Zagon Opiates, endorphins, and the developing organism: a comprehensive bibliography, 1982-1983 Neurosci. Biobehav. Rev. 8 3 1984 387 403
52. E.A. Zahalka, F.J. Seidler, S.E. Lappi, E.C. McCook, J. Yanai, and T.A. Slotkin Deficits in development of central cholinergic pathways caused by fetal nicotine exposure: differential effects on choline acetyltransferase activity and [3H]hemicholinium-3 binding Neurotoxicol. Teratol. 14 6 1992 375 382
53. T. Zor, and Z. Selinger Linearization of the Bradford protein assay increases its sensitivity: theoretical and experimental studies Anal. Biochem. 236 2 1996 302 308