Hidden prenatal malnutrition in the rat: Role of β1- adrenoceptors on synaptic plasticity in the frontal cortex

Journal of Neurochemistry

Volumn 119, Issue 2, 2011, Pages 314-323

  Flores, Osvaldo ^a   Pérez, Hernán ^a   Valladares, Luis ^a   Morgan, Carlos ^a   Gatica, Arnaldo ^a   Burgos, Héctor ^b,c   Olivares, Ricardo ^a   Hernández, Alejandro ^d  

^a UNIVERSITY OF CHILE   (Chile)

^b UNIVERSIDAD AUTÓNOMA DE CHILE   (Chile)

^c UNIVERSIDAD CENTRAL DE CHILE   (Chile)

^d UNIVERSIDAD DE SANTIAGO DE CHILE   (Chile)

Author keywords

1 adrenoceptor; CaMKII; frontal cortex; long term potentiation; PKA; prenatal malnutrition

Indexed keywords

BETA 1 ADRENERGIC RECEPTOR; CYCLIC AMP DEPENDENT PROTEIN KINASE; DOBUTAMINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING SITE; BODY WEIGHT; BRAIN REGION; BRAIN WEIGHT; CONTROLLED STUDY; CORPUS CALLOSUM; DIETARY INTAKE; FEMALE; FRONTAL CORTEX; LONG TERM POTENTIATION; MALE; MALNUTRITION; NERVE CELL PLASTICITY; NONHUMAN; PREFRONTAL CORTEX; PRENATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; RECEPTOR BINDING;

ADRENERGIC BETA-AGONISTS; ANIMALS; BODY WEIGHT; BRAIN; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DIET; DOBUTAMINE; ELECTROPHYSIOLOGICAL PHENOMENA; FEMALE; FETAL NUTRITION DISORDERS; LONG-TERM POTENTIATION; MALE; MEMBRANES; NEURONAL PLASTICITY; ORGAN SIZE; PREFRONTAL CORTEX; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ADRENERGIC, BETA-1; SRC-FAMILY KINASES;

ANIMALIA; RATTUS;

EID: 80053575858     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2011.07429.x     Document Type: Article

References (62)

1. Adams J. P., and, Dudek S. M., (2005) Late-phase long-term potentiation: getting to the nucleus. Nat. Rev. Neurosci. 6, 737-743. (Pubitemid 43160321)
2. Alier K. A., and, Morris B. J., (2004) Differential regulation of MAP2 and αCamKII expression in hippocampal neurones by forskolin and calcium ionophore treatment. Mol. Brain Res. 122, 10-16. (Pubitemid 38264542)
3. Aoki C., Joh T. H., and, Pickel V. M., (1987) Ultrastructural localization of badrenergic receptor-like immunoreactivity in the cortex and neostriatum of rat brain. Brain Res. 437, 264-282. (Pubitemid 18016214)
4. Austin K. B., Bronzino J., and, Morgane P. J., (1986) Prenatal protein malnutrition affects synaptic potentiation in the dentate gyrus of rats in adulthood. Brain Res. 394, 267-273. (Pubitemid 16017085)
5. Bayer K. U., Löhler J., Schulman H., and, Harbers K., (1999) Developmental expression of the CaM kinase II isoforms: ubiquitous gamma- and delta-CaM kinase II are the early isoforms and most abundant in the developing nervous system. Mol. Brain Res. 70, 147-154. (Pubitemid 29278617)
6. Berridge C. W., and, Waterhouse B. D., (2003) The locus coeruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes. Brain Res. Rev. 42, 33-84. (Pubitemid 36369264)
7. 2C- adrenoceptors impairs water maze navigation. Neuroscience 95, 481-487.
8. Bradford M., (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
9. Bramham C. R., Bacher-Svendsen K., and, Sarvey J. M., (1997) LTP in the lateral perforant path is β-adrenergic receptor-dependent. Neuroreport 8, 719-724. (Pubitemid 27128224)
10. Chapman C. A., Trepel C., Ivanco T. L., Froc D. J., Wilson K., and, Racine R. J., (1998) Changes in field potentials and membrane currents in rat sensorimotor cortex following repeated tetanization of the corpus callosum in vivo. Cereb. Cortex 8, 730-742. (Pubitemid 28550895)
11. Davidkova G., and, Carroll R. C., (2007) Characterization of the role of microtubule-associated protein 1B in metabotropic glutamate receptor-mediated endocytosis of AMPA receptors in hippocampus. J. Neurosci. 27, 13273-13278. (Pubitemid 350220475)
12. De Paermentier F., Cheetham S. C., Crompton M. R., and, Horton R. W., (1989) β-adrenoceptors in human brain labelled with [3H]dihydroalprenolol and [3H]CGP 12177. Eur. J. Pharmacol. 167, 397-405. (Pubitemid 19216544)
13. Dehmelt L., and, Halpain S., (2004) Actin and microtubules in neurite initiation: are MAPs the missing link? J. Neurobiol. 58, 18-33. (Pubitemid 37543335)
14. Duman R. S., Saito N., and, Tallman J. F., (1989) Development of β-adrenergic receptor and G protein messenger RNA in rat brain. Mol. Brain Res. 5, 289-296. (Pubitemid 19128101)
15. Fiacco T. A., Rosene D. L., Galler J. R., and, Blatt G. J., (2003) Increased density of hippocampal kainate receptors but normal density of NMDA and AMPA receptors in a rat model of prenatal protein malnutrition. J. Comp. Neurol. 456, 350-360. (Pubitemid 36120241)
16. Floresco S. B., Seamans J. K., and, Phillips A. G., (1997) Selective roles for hippocampal, prefrontal cortical, and ventral striatal circuits in radial-arm maze tasks with or without a delay. J. Neurosci. 17, 1880-1890. (Pubitemid 27089832)
17. Galeotti N., Bartolini A., and, Ghelardini C., (2004) Alpha-2 agonist-induced memory impairment is mediated by the alpha-2A-adrenoceptor subtype. Behav. Brain Res. 153, 409-417. (Pubitemid 38953115)
18. Gelinas J., Tenorio G., Lemon N., Abel T., and, Nguyen P. V., (2008) β-adrenergic receptor activation during distinct patterns of stimulation critically modulates the PKA-dependence of LTP in the mouse hippocampus. Learn. Mem. 2008 (15), 281-289. (Pubitemid 351629592)
19. 3 adrenoceptors in memory consolidation. Neuroscience 95, 913-922.
20. Gibbs M. E., and, Summers R. J., (2005) Contrasting roles for β1, β2 and β3-adrenoceptors in memory formation in the chick. Neuroscience 131, 31-42. (Pubitemid 40170486)
21. Gõmez-Pinilla F., (2008) Brain foods: the effects of nutrients on brain function. Nat. Rev. Neurosci. 9, 568-578. (Pubitemid 351873468)
22. Gressens P., Muaku S. M., Besse L., Nsegbe E., Gallego J., Delpech B., Gaultier C., Evrard P., Ketelslegers J. M., and, Maiter D., (1997) Maternal protein restriction early in rat pregnancy alters brain development in the progeny. Brain Res. Dev. Brain Res. 103, 21-35. (Pubitemid 27465707)
23. Hernández A., Burgos H., Mondaca M., et al. (2008) Effect of prenatal protein malnutrition on long-term potentiation and BDNF protein expression in the rat entorhinal cortex after neocortical and hippocampal tetanization. Neural Plast. 2008, 646919.
24. Hescham S., Grace L., Kellaway L. A., Bugarith K., and, Russell V. A., (2009) Effect of exercise on synaptophysin and calcium/calmodulin-dependent protein kinase levels in prefrontal cortex and hippocampus of a rat model of developmental stress. Metab. Brain Dis. 24, 701-709.
25. Hikosaka K., and, Watanabe M., (2000) Delay activity of orbital and lateral prefrontal neurons of the monkey varying with different rewards. Cereb. Cortex 10, 263-271. (Pubitemid 30159293)
26. Hopkins W. F., and, Johnston D., (1988) Noradrenergic enhancement of long-term potentiation at mossy fiber synapses in the hippocampus. J. Neurophysiol. 59, 667-687. (Pubitemid 18069331)
27. Huang Y. Y., Kandel E. R., Varshavsky L., Brandon E. P., Qi M., Idzerda R. L., McKnight G. S., and, Bourtchouladze R., (1995) A genetic test of the effects of mutations in PKA on mossy fiber LTP and its relation to spatial and contextual learning. Cell 1995, 83.
28. Kandel E. R., (2001) The molecular biology of memory storage: a dialogue between genes and synapses. Science 294, 1030-1038. (Pubitemid 33041851)
29. Kawakami S., Muramoto K., Ichikawa M., and, Kuroda Y., (2003) Localization of microtubule-associated protein (MAP) 1B in the postsynaptic densities of the rat cerebral cortex. Cell. Mol. Neurobiol. 23, 887-894. (Pubitemid 38063329)
30. Keller E. A., Munaro N. I., and, Orsingher O. A., (1982) Perinatal undernutrition reduces alpha and beta adrenergic receptor binding in adult rat brain. Science 215, 1269-1270. (Pubitemid 12106500)
31. Langley-Evans S. C., (2009) Nutritional programming of disease: unravelling the mechanism. J. Anat. 215, 36-51.
32. Lin Y. W., Min M. Y., Chiu T. H., and, Yang H. W., (2003) Enhancement of associative long-term potentiation by activation of β-adrenergic receptors at CA1 synapses in rat hippocampal slices. J. Neurosci. 23, 4173-4181.
33. 2-adrenoceptors; comparisons with the unmodified receptors. Br. J. Pharmacol. 1308, 1825-1832. (Pubitemid 30655793)
34. 2-Adrenoceptor modulation of long-term potentiation elicited in vivo in rat occipital cortex. Brain Res. 1021, 292-296. (Pubitemid 39165809)
35. Morgane P. J., Austin-LaFrance R., Bronzino J., Tonkiss J., Díaz-Cintra S., Cintra L., Kemper T., and, Galler J. R., (1993) Prenatal malnutrition and development of the brain. Neurosci. Biobehav. Rev. 17, 91-128. (Pubitemid 23068946)
36. Murchison C. F., Zhang X. Y., Zhang W. P., Ouyang M., Lee A., and, Thomas S. A., (2004) A distinct role for norepinephrine in memory retrieval. Cell 117, 131-143. (Pubitemid 38469904)
37. National Research Council (1985) Guide for the Care and Use of Laboratory Animals. Publication No. 85-23 (rev.). National Institutes of Health, Bethesda, MD.
38. Nowicky A. V., Christofi G., and, Bindman L. J., (1992) Investigation of β-adrenergic modulation of synaptic transmission and postsynaptic induction of associative LTP in layer V neurones in slices of rat sensorimotor cortex. Neurosci. Lett. 137, 270-273.
39. O'Dell T. J., Connor S. A., Gelinas J. N., and, Nguyen P. V., (2010) Viagra for your synapses: enhancement of hippocampal long-term potentiation by activation of beta-adrenergic receptors. Cell. Signal. 5, 728-736.
40. Pellegrino L. J., and, Cushman A. J., (1967) A stereotaxic atlas of the rat brain, in The Century Psychology Series (, Elliott R. M., Lindzey G., and, MacCorquodale K., eds), plate 22. Appleton-Century-Crofts, New York.
41. Peters Y. M., O'Donnell P., and, Carelli R. M., (2005) Prefrontal cortical cell firing during maintenance, extinction, and reinstatement of goal-directed behavior for natural reward. Synapse 56, 74-83. (Pubitemid 40389558)
42. Pittman R. N., Minneman K. P., and, Molinoff P. B., (1980) Ontogeny of β1- and β2-adrenergic receptors in rat cerebellum and cerebral cortex. Brain Res. 188, 357-368. (Pubitemid 10144282)
43. Rainbow T. C., Parsons B., and, Wolfe B. B., (1984) Quantitative autoradiography of β1- and β2-adrenergic receptors in rat brain. Proc. Natl Acad. Sci. USA 81, 1585-1589. (Pubitemid 14174548)
44. Ramos B. P., and, Arnsten A. F., (2007) Adrenergic pharmacology and cognition: focus on the prefrontal cortex. Pharmacol. Ther. 113, 523-536. (Pubitemid 46365960)
45. Resnick O., Morgane P. J., Hasson R., and, Miller M., (1982) Overt and hidden forms of chronic malnutrition in the rat and their relevance to man. Neurosci. Biobehav. Rev. 6, 55-76.
46. Sheng M., and, Kim M. J., (2002) Postsynaptic signaling and plasticity mechanisms. Science 298, 776-780. (Pubitemid 35231521)
47. Sheng M., and, Pak D. T., (2000) Ligand-gated ion channel interactions with cytoskeletal and signaling proteins. Annu. Rev. Physiol. 62, 755-778. (Pubitemid 30618281)
48. Skalhegg B. S., and, Taskén K., (2000) Specificity in the cAMP/PKA signaling pathway. Differential expression, regulation, and subcellular localization of subunits of PKA. Front. Biosci. 5, 678-693.
49. Skeberdis V. A., Chevaleyre V., Lau C. G., et al. (2006) Protein kinase A regulates calcium permeability of NMDA receptors. Nat. Neurosci. 9, 501-510.
50. Soto-Moyano R., Alarcõn S., Belmar J., Kusch C., Pérez H., Ruiz S., and, Hernández A., (1998) Prenatal protein restriction alters synaptic mechanisms of callosal connections in the rat visual cortex. Int. J. Dev. Neurosci. 16, 75-84. (Pubitemid 28371994)
51. 2C-adrenoceptor density in the cerebral cortex during postnatal life and impairs neocortical long-term potentiation and visuo-spatial performance in rats. J. Neurochem. 93, 1099-1109. (Pubitemid 40776565)
52. Stanton P. K., and, Sarvey J. M., (1985) Blockade of norepinephrine- induced long-lasting potentiation in the hippocampal dentate gyrus by an inhibitor of protein synthesis. Brain Res. 361, 276-283. (Pubitemid 16185364)
53. Summers R. J., Papaioannou M., Harris S., and, Evans B. A., (1995) Expression of b3-adrenoceptor mRNA in rat brain. Br. J. Pharmacol. 116, 2547-2548.
54. Thiagarajan T. C., Piedras-Renteria E. S., and, Tsien R. W., (2002) α- and βCaMKII. Inverse regulation by neuronal activity and opposing effects on synaptic strength. Neuron 36, 1103-1114. (Pubitemid 36044511)
55. Tonkiss J., and, Galler J. R., (1990) Prenatal protein malnutrition and working memory performance in adult rats. Behav. Brain Res. 40, 95-107. (Pubitemid 20369875)
56. Tonkiss J., Foster G. A., and, Galler J. R., (1991) Prenatal protein malnutrition and hippocampal function: partial reinforcement extinction effect. Brain Res. Bull. 27, 809-813.
57. Trepel C., and, Racine R. J., (1998) Long-term potentiation in the neocortex of the adult, freely moving rat. Cereb. Cortex 8, 719-729. (Pubitemid 28550894)
58. Tsuchihashi H., Nakashima Y., Kinami J., and, Nagatomo T., (1990) Characteristics of 125I-iodocyanopindolol binding to β-adrenergic and serotonin-1B receptors of rat brain: selectivity of β-adrenergic agents. Jpn. J. Pharmacol. 522, 195-200. (Pubitemid 20070261)
59. Ul Haq R., Liotta A., Kovacs R., Rösler A., Jarosch M. J., Heinemann U., and, Behrens C. J., (2011) Adrenergic modulation of sharp wave-ripple activity in rat hippocampal slices. Hippocampus. Published Online doi:.
60. Wayman G. A., Lee Y. S., Tokumitsu H., Silva A. J., and, Soderling T. R., (2008) Calmodulin-kinases: modulators of neuronal development and plasticity. Neuron 59, 914-931.
61. 2+/ calmodulin-dependent protein kinase IIα in dendritic spine enlargement, long-term potentiation, and learning. J. Neurosci. 29, 7607-7618.
62. Zawilska J. B., Zalewska-Kaszubska J., Marczak G., Gõrska D., and, Woldan-Tambor A., (2000) Characterization of β-adrenergic receptors in duck cerebral cortex. Acta Neurobiol. Exp. 603, 301-307. (Pubitemid 30659906)