NADPH-diaphorase Histochemical Labeling Patterns in the Hippocampal Neuropil and Visual Cortical Neurons in Weaned Rats Reared during Lactation on Different Litter Sizes

References

• Barret, D.E. and Radke-Yarrow, M. (1985 ) “Effects of nutritional supplementation on children’s responses to novel, frustrating and competitive situations”, American Journal of Clinical Nutrition 42, 102–120.
   PubMed Web of Science ®Google Scholar
• Beahl, M.F., Kowall, N.W., Swartz, K.J. and Ferrante, T.J. (1990 ) “Homocysteic acid lesion in rat stritatum spare somatostain- neuropeptide Y (NADPH-diaphorase) neurons”, Neuroscience Letters 108, 36–42.
   PubMed Web of Science ®Google Scholar
• Bidmon, H.J., Emde, B., Kowalski, T., Schmitt, M., Mayer, B., Kato, K., Assayama, K., Witte, O.W. and Ziles, K. (2001 ) “Nitric oxide synthase-I containing cortical interneurons co-express antioxidative enzymes and anti-apoptotic Bcl-2 following focal ischemia: evidence for direct and indirect mechanisms towards their resistance to neuropathology”, Journal of Chemical Neuroanatomy 22, 167–184.
   PubMed Web of Science ®Google Scholar
• Bohme, G.A., Bon, C. and Lemaire, M. (1993 ) “Altered synaptic plasticity and memory formation in nitric oxide synthase inhibitor-treated rats”, Proceedings of the National Academy of Sciences USA 90, 9191–9194.
   PubMed Web of Science ®Google Scholar
• Borba, J.M.C., Araujo, M.S., Picanco-Diniz, C.W., Manhaes-de- Castro, R. and Guedes, R.C.A. (2000) “Permanent and transitory morphometric changes of NADPH-diaphorase- containing neurons in the rat visual cortex after early malnutrition”, Brain Research Bulletin 53, 193–201.
   PubMed Web of Science ®Google Scholar
• Bredt, D.S. and Snyder, S.H. (1989 ) “Nitric oxide mediates glutamate-linked enhancement of cGMP levels in the cerebellum”, Proceedings of the National Academy of Sciences USA 86, 9030–9033.
   PubMed Web of Science ®Google Scholar
• Bredt, D.S., Glatt, C.H., Hwang, P.M., Fotuhi, M., Dawson, T.M. and Snyder, S.H. (1991 ) “Nitric oxide synthase protein and mRNA are discretely localized in neuronal populations of the mammalian CNS together with NADPH diaphorase”, Neuron 7, 615–624.
   PubMed Web of Science ®Google Scholar
• Brock, J.W. and Prasad, C. (1992 ) “Alterations in dendritic spine density in the rat brain associated with protein malnutrition”, Developmental Brain Research 66, 266–269.
   PubMedGoogle Scholar
• Burette, A., Zabel, U., Weinberg, R.J., Schmidt, H.H. and Valtschanoff, J.G. (2002 ) “Synaptic localization of nitric oxide synthase and soluble guanylyl cyclase in the hippocampus”, Journal of Neuroscience 22, 8961–8970.
   PubMed Web of Science ®Google Scholar
• Buwalda, B., Nyakas, C., Gast, J., Luiten, P.G. and Schmidt, H.H. (1995 ) “Aldehyde fixation differentially affects distribution of diaphorase activity but not of nitric oxide synthase immunoreactivity in rat brain”, Brain Research Bulletin 38, 467–473.
   PubMed Web of Science ®Google Scholar
• Catania, M.V., Giuffrida, R., Seminara, G., Barbagallo, G., Aronica, E., Gorter, J.A., Dell’Albani, P., Ravagna, A., Calabrese, V. and Giuffrida-Stella, A.M. (2003) “Upregulation of neuronal nitric oxide synthase in in vitro stelate astrocytes and in vivo reactive astrocytes after electrically induced status epilepticus”, Neurochemical Research 28, 607–615.
   PubMed Web of Science ®Google Scholar
• Chang, H.M., Lue, J.H., Wen, C.Y. and Shieh, J.Y. (2001 ) “Axotomy along with hypoxia enhances the neuronal NADPH-d/NOS expression in lower brain stem motor neurons of adult rats”, Experimental Neurology 171, 116–126.
   PubMed Web of Science ®Google Scholar
• Dawson, T.M., Bredt, D.S., Fotuhi, M., Hwang, P.M. and Snyder, S.H. (1991 ) “Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues”, Proceedings of the National Academy of Sciences USA 88, 7797–7801.
   PubMed Web of Science ®Google Scholar
• Debassio, W.A., Kemper, T.L., Tonkiss, J. and Galler, J.R. (1996 ) “Effect of prenatal protein deprivation on postnatal granule cell generation in the hippocampal dentate gyrus”, Brain Research Bulletin 41, 379–383.
   PubMed Web of Science ®Google Scholar
• Diaz-Cintra, S., Cintra, L., Ortega, A., Kemper, T. and Morgane, PJ. (1990 ) “Effects of protein deprivation on pyramidal cells of the visual cortex in rats of three age groups”, Journal of Comparative Neurology 292, 117–126.
   PubMed Web of Science ®Google Scholar
• Diaz-Cintra, S., Garcia-Ruiz, M., Corkidi, G. and Cintra, L. (1994 ) “Effects of pre-natal malnutrition and post-natal nutritional rehabilitation on CA3 hippocampal pyramidal cells in rats of four ages”, Brain Research 662, 117–126.
   PubMed Web of Science ®Google Scholar
• Dobbing, J. (1968 ) “Vulnerable periods in developing brain ”, In: Davison, N.A. and Dobbing, J., eds, Applied Neurochemistry (Blackwell, Oxford ), pp 287–316.
   Google Scholar
• Dowdeswell, H.J., Slater, A.M., Broomhall, J. and Tripp, J. (1995 ) “Visual deficits in children born at less than 32 weeks gestation with and without major ocular pathology and cerebral damage”, British Journal of Ophthalmology 79, 1–6.
   Web of Science ®Google Scholar
• Dun, N.J., Dun, S.L., Wong, R.K. and Forstermann, U. (1994 ) “Colocalization of nitric oxide synthase and somatostatin immunoreactivity in rat dentate hilar neurons”, Proceedings of the National Academy of Sciences USA 91, 2955–2959.
   PubMed Web of Science ®Google Scholar
• Fabene, P.F., Correia, L., Carvalho, R.A., Cavalheiro, E.A. and Bentivoglio, M. (2001 ) “The spiny rat Proechimys guyannensis as model of resistance to epilepsy: chemical characterization of hippocampal cell populations and pilocarpine-induced changes”, Neuroscience 104, 979–1002.
   PubMed Web of Science ®Google Scholar
• Fernandez, V., Pascual, R. and Ruiz, S. (1993 ) “Early life environmental deterioration, nutrition and ontogenesis of the motor cortex in the rat: a Golgi study”, Biology of the Neonate 64, 245–253.
   PubMedGoogle Scholar
• Ferrante, R.J., Kowall, N.W., Beal, M.F., Richardson, E.P., Jr, Bird, E.D. and Martin, J.B. (1985 ) “Selective sparing of a class of striatal neurons in Huntington’s disease”, Science 230, 561–563.
   PubMed Web of Science ®Google Scholar
• Ferriero, D.M., Arcavi, L.J., Sagar, S.M., McIntosh, T.K. and Simon, R.P. (1988 ) “Selective sparing of NADPH-diaphorase neurons in neonatal hypoxia-ischemia”, Annals of Neurology 24, 670–676.
   PubMed Web of Science ®Google Scholar
• Friedlander, M.J., Montague, P.R., Hester, F. and Marchase, R.B. (1992 ) “Role of nitric oxide in NMDA-receptor mediated release of neurotransmitter in visual cortex”, Society for Neuroscience 18, 210, (Abstract).
   Google Scholar
• Gabbot, P.L. and Bacon, S.J. (1993 ) “Histochemical localization of NADPH-dependent diaphorase (nitric oxide synthase) activity in vascular endothelial cells in the rat brain”, Neuroscience 57, 79–95.
   PubMed Web of Science ®Google Scholar
• Granados-Rojas, L., Larriva-Sahd, J., Gutierrez-Ospina, G., Rondan, A. and Diaz-Cintra, S. (2002 ) “Prenatal protein malnutrition decreases mossy fibers-CA3 thorny excrescences asymmetrical synapses in adult rats”, Brain Research 933, 164–171.
   PubMed Web of Science ®Google Scholar
• Haley, J.E., Wilcox, G.L. and Chapman, P.F. (1992 ) “The role of nitric oxide in hippocampal long-term potentiation”, Neuron 8, 211–216.
   PubMed Web of Science ®Google Scholar
• Hartlage-Rubsamen, M. and Schliebs, R. (2001 ) “Rat basal forebrain cholinergic lesion affects neuronal nitric oxide synthase activity in hippocampal and neocortical target regions”, Brain Research 889, 155–164.
   PubMed Web of Science ®Google Scholar
• Hope, B.T., Michael, G.J., Knigge, K.M. and Vicent, S.R. (1991 ) “Neuronal NADPH-diaphorase is a nitric oxide synthase”, Proceedings of the National Academy of Sciences USA 88, 2811–2814.
   PubMed Web of Science ®Google Scholar
• Jang, M.H., Shin, M.C., Lim, B.V., Chung, J.K., Kang, H.S., Kang, S.A., Choue, R.W., Kim, E.H. and Kim, C.J. (2002 ) “Nicotine administration decreases nitric oxide synthase expression in the hypothalamus of food deprived rats”, Neuroscience Letters 322, 29–32.
   PubMed Web of Science ®Google Scholar
• Jiang, M.H., Kaku, T., Hada, J. and Hayashi, Y. (2002 ) “Different effects of eNOS and nNOS inhibition on transient forebrain ischemia”, Brain Research 946, 139–147.
   PubMed Web of Science ®Google Scholar
• Kehoe, P., Mallinson, K., Bronzino, J. and McCormick, C.M. (2001 ) “Effects of protein malnutrition and neonatal stress on CNS responsiveness”, Developental Brain Research 132, 23 –31.
   PubMed Web of Science ®Google Scholar
• Kim, M.J., Kim, Y., Choe, B.K., Kim, S.A., Lee, H.J., Kim, J.W., Huh, Y., Kin, C. and Chung, J.H. (2000 ) “Differential expression of nicotinamide adenine dinucleotide phosphate-diaphorase in hypothalamic areas of obese Zucker rats”, Neuroscience Letters 292, 60–62.
   PubMed Web of Science ®Google Scholar
• Koh, J.Y., Peters, S. and Choi, D.W. (1986 ) “Neurons containing NADPH-diaphorase are selectively resistant to quinolinate toxicity”, Science 234, 73–76.
   PubMed Web of Science ®Google Scholar
• Leuba, G. and Rabinowicz, T. (1979 ) “Long-term effects of postnatal undernutrition and maternal malnutrition on mouse cerebral cortex. I. Cellular densities, cortical volume and total number of cells”, Experimental Brain Research 37, 283 –298.
   PubMed Web of Science ®Google Scholar
• Lovick, T.A., Brown, L.A. and Key, B.J. (1999 ) “Neurovascular relationships in hippocampal slices: physiological and anatomical studies of mechanisms underlying flow-meta- bolism coupling in intraparenchymal microvessels”, Neuroscience 92, 47–60.
   PubMed Web of Science ®Google Scholar
• Lucas, A. (1997 ) “Long-chain polyunsaturated fatty acids, infant feeding and cognitive development ”, In: Dobbing, J., ed., Developing Brain and Behaviour. The Role of Lipids in Infant Formula (Academic Press, London ), pp 3–39.
   Google Scholar
• Magri, F., Borza, A., Del Vecchio, S., Chytiris, S., Cuzzoni, G., Busconi, L., Rebesco, A. and Ferrari, E. (2003 ) “Nutritional assessment of demented patients: a descriptive study”, Aging Clinical and Experimental Research 15, 148–153.
   PubMed Web of Science ®Google Scholar
• Matsura, T. and Kanno, I. (2002 ) “Effect of nitric oxide synthase inhibitor on the local cerebral blood flow evoked by rat somatosensory stimulation under hyperoxia”, Comparative Biochemistry and Physiology A Molecular and Integrative Physiology 131, 267–274.
   PubMed Web of Science ®Google Scholar
• Meeks-Gardner, J.M. and Grantham-McGregor, S.M. (1994) “Physical activity, undernutrition and child development”, Proceedings of the Nutrition Society 53, 241–248.
   PubMed Web of Science ®Google Scholar
• Montecot, C.L., Rondi-Reig, L., Springhetti, V., Seylaz, J. and Pinard, E. (1998 ) “Inhibition of neuronal (type 1) nitric oxide synthase prevents hyperaemia and hippocampal lesions resulting from kainate-induced seizures”, Neuroscience 84, 791–800.
   PubMed Web of Science ®Google Scholar
• Morgane, P.J., Miller, M., Kemper, T., Stern, W., Forbes, W., Hall, R., Bronzino, J.D., Kissane, J., Hawrylewicz, E. and Resnick, O. (1978 ) “The effects of protein malnutrition on the developing central nervous system in the rat”, Neuroscience and Biobehavioral Reviews 2, 137–230.
   Web of Science ®Google Scholar
• Morgane, P.J., Austin-Lafrance, R.J., Bronzino, J.D., Tonkiss, J., Diaz-Cintra, S., Cintra, L., Kemper, T. and Galler, J.R. (1993 ) “Prenatal malnutrition and development of the brain”, Neuroscience and Biobehavioral Reviews 17, 91–128.
   PubMed Web of Science ®Google Scholar
• Morley, J.E. and Flood, J.F. (1991 ) “Evidence that nitric oxide modulates food intake in mice”, Life Science 49, 707–711.
   PubMed Web of Science ®Google Scholar
• Picanco-Diniz, C.W., Araujo, M.S., Borba, J.M.C. and Guedes, R.C.A. (1998 ) “NADPH-diaphorase containing neurons and biocytin-labelled axon terminal in the visual cortex of adult rats malnourished during development”, Nutritional Neuroscience 1, 35–48.
   PubMedGoogle Scholar
• Plagemann, A., Rake, A., Melchior, K., Rohde, W. and Dorner, G. (1998 ) “Reduction of cholecystokinin-8S-neurons in the paraventricular hypothalamic nucleus of neonatally overfed weanling rats”, Neuroscience Letters 258, 13–16.
   PubMed Web of Science ®Google Scholar
• Plagemann, A., Harder, T., Rake, A., Voits, M., Fink, H., Rohde, W. and Dorner, G. (1999 ) “Perinatal elevation of hypothalamic insulin, acquired malformation of hypothalamic galaninergic neurons, and syndrome x-like alterations in adulthood of neonatally overfed rats”, Brain Research 836, 146–155.
   PubMed Web of Science ®Google Scholar
• Pollitt, E., Gorman, K.S., Engel, P.L., Rivera, J.A. and Martorell, R. (1995 ) “Nutrition in early life and the fulfillment of intellectual potential. Supplement: The INCAP follow-up study”, Journal ofNutrition 125, 1111S-1118S.
   PubMedGoogle Scholar
• Powls, A., Botting, N., Cooke, R.W.I., Stephenson, G. and Marlow, N. (1997 ) “Visual impairment in very low birth-weight children”, Archives of Diseases in Childhood 76, 82–87.
   Web of Science ®Google Scholar
• Quinn, J., Davis, F., Woodward, W.R. and Eckenstein, F. (2001 ) “Beta-amyloid plaques induce neuritic dystrophy of nitric oxide-producing neurons in a transgenic mouse model of Alzheimer’s disease”, Experimental Neurology 168, 203 –212.
   PubMed Web of Science ®Google Scholar
• Rabin, O., Lefauconnier, J.M., Chanez, C., Bernad, G. and Bourre, J.M. (1994 ) “Developmental effects of intrauterine growth retardation on cerebral amino acid transport”, Pediatric Research 35, 640 –648.
   PubMed Web of Science ®Google Scholar
• Rocha-de-Melo, A.P. and Guedes, R.C.A. (1997) “Spreading depression is facilitated in adult rats previously submitted to short episodes of malnutrition during the lactation period”, Brazilian Journal of Medical and Biological Research 30, 663–669.
   PubMed Web of Science ®Google Scholar
• Santos-Monteiro, J., Teodosio, N.R. and Guedes, R.C.A. (2000 ) “Long-lasting effects of early environmental stimulation on cortical spreading depression in normal and early-malnourished adult rats”, Nutritional Neuroscience 3, 29–40.
   PubMed Web of Science ®Google Scholar
• Scherer-Singler, U., Vicent, S.R., Kimura, H. and Mcgeer, E.G. (1983 ) “Demonstration of unique population of neurons with NADPH diaphorase histochemistry”, Journal of Neuroscience Methods 9, 229 –234.
   PubMed Web of Science ®Google Scholar
• Sirevaag, A.M., Black, J.E., Shafron, D. and Greenough, W.T. (1988 ) “Direct evidence that complex experience increases capillary branching and surface area in visual cortex of young rats”, Brain Research 471, 299–304.
   PubMed Web of Science ®Google Scholar
• Squadrito, F., Calapai, G., Cucinotta, D., Altavilla, D., Zingarelli, B., Ioculano, M., Urna, G., Sardella, A., Campo, G.M. and Caputi, A.P. (1993 ) “Anorectic activity of NG-nitro-L-arginine, an inhibitor of brain nitric oxide synthase, in obese Zucker rats”, European Journal of Pharmacology 230, 125–128.
   PubMed Web of Science ®Google Scholar
• Squadrito, F., Calapai, G., Altavilla, D., Cucinotta, D., Zingarelli, B., Campo, G.M., Arcoraci, V., Sautebin, L., Mazzaglia, G. and Caputi, A.P. (1994 ) “Food deprivation increases brain nitric oxide synthase and depresses brain serotonin levels in rats”, Neuropharmacology 33, 83–86.
   PubMed Web of Science ®Google Scholar
• Stricker-Krongrad, A., Beck, B. and Burlet, C. (1996 ) “Nitric oxide mediates hyperphagia of obese Zucker rats: relation to specific changes in the microstructure of feeding behavior”, Life Science 58, 9–15.
   PubMedGoogle Scholar
• Teodosio, N.R., Peres, E.P., Alves, A.J., Dimenstein, W. and Guedes, R.C.A. (2000 ) “A new dietary supplement based on bovine blood: recovering Brazilian children from malnutrition”, Nutritional Neuroscience 3, 73–86.
   PubMed Web of Science ®Google Scholar
• Tsuchida, A., Handa, Y., Nojyo, Y. and Kubota, T. (2001 ) “Ultrastructure of NADPH diaphorase-positive nerve fibers and their terminals in the rat cerebral arterial system”, Journal of Chemical Neuroanatomy 21, 267–275.
   PubMed Web of Science ®Google Scholar
• Valtschanoff, J.G., Weinberg, R.J., Kharazia, V.N., Schmidt, H.H.H.W., Nakane, M. and Rustinoni, A. (1993 ) “Neurons in rat cerebral cortex that synthesize nitric oxide: NADPH diaphorase histochemistry, NOS immunocytochemistry, and colocalization with GABA”, Neuroscience Letters 157, 157–161.
   PubMed Web of Science ®Google Scholar
• Vincent, S.R. and Kimura, H. (1992 ) “Histochemical mapping of nitric oxide synthase in the rat brain”, Neuroscience 46, 755–784.
   PubMed Web of Science ®Google Scholar
• Woolf, N.J., Jacobs, R.W. and Butcher, L.L. (1989 ) “The pontomesencephalotegmental cholinergic system does not degenerate in Alzheimer’s disease”, Neuroscience Letters 96, 277–282.
   PubMed Web of Science ®Google Scholar
• Xu, M., Ng, Y.K. and Leong, S.K. (2000 ) “Neuroprotective and neurodestructive functions of nitric oxide after spinal cord hemisection”, Experimental Neurology 161, 472–480.
   PubMed Web of Science ®Google Scholar
• Zhang, Z.G., Choop, M., Gautam, S., Zaloga, C., Zhang, R.L., Schmidt, H.H.H.W., Pollock, J.S. and Förstermann, U. (1994 ) “Upregulation of neuronal nitric oxide synthase and mRNA, and selective sparing of nitric oxide synthase-containing neurons after focal cerebral ischemia in rat”, Brain Research 654, 85–95.
   PubMed Web of Science ®Google Scholar