Prolonged protein deprivation differentially affects calretinin- and parvalbumin-containing interneurons in the hippocampal dentate gyrus of adult rats

Neuroscience Letters

Volumn 555, Issue , 2013, Pages 154-158

  Hipólito Reis, José ^a   Pereira, Pedro Alberto ^a   Andrade, José Paulo ^a   Cardoso, Armando ^a  

^a University of Porto   (Portugal)

Author keywords

Calretinin; Dentate gyrus; Interneurons; Parvalbumin; Protein deprivation

Indexed keywords

CALRETININ; CASEIN; MOLECULAR LAYER; PARVALBUMIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM HOMEOSTASIS; CELL DEATH; COMPARATIVE STUDY; CONTROLLED STUDY; DENTATE GYRUS; FOOD INTAKE; INTERNEURON; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN RESTRICTION; QUALITATIVE ANALYSIS; RANDOMIZED CONTROLLED TRIAL; RAT; UPREGULATION;

CALRETININ; DENTATE GYRUS; INTERNEURONS; PARVALBUMIN; PROTEIN DEPRIVATION;

ANIMALS; CALBINDIN 2; DENTATE GYRUS; DIET, PROTEIN-RESTRICTED; HIPPOCAMPUS; INTERNEURONS; MALE; PARVALBUMINS; RATS; RATS, WISTAR;

EID: 84885747295     PISSN: 03043940     EISSN: 18727972     Source Type: Journal    
DOI: 10.1016/j.neulet.2013.09.036     Document Type: Article

References (38)

1. Alamy M., Bengelloun W.A. Malnutrition and brain development: an analysis of the effects of inadequate diet during different stages of life in rat. Neurosci. Biobehav. Rev. 2012, 36:1463-1480.
2. Amaral D.G., Witter M.P. The hippocampal formation. The Rat Nervous System 1995, 443-493. Academic Press, San Diego. G. Paxinos (Ed.).
3. Andrade J.P., Castanheira-Vale A.J., Paz-Dias P.G., Madeira M.D., Paula-Barbosa M.M. The dendritic trees of neurons from the hippocampal formation of protein-deprived adult rats. A quantitative Golgi study. Exp. Brain Res. 1996, 109:419-433.
4. Andrade J.P., Lukoyanov N.V., Paula-Barbosa M.M. Chronic food restriction is associated with subtle dendritic alterations in granule cells of the rat hippocampal formation. Hippocampus 2002, 12:149-164.
5. Andrade J.P., Madeira M.D., Paula-Barbosa M.M. Effects of long-term malnutrition and rehabilitation on the hippocampal formation of the adult rat. A morphometric study. J. Anat. 1995, 187:379-393.
6. Andrade J.P., Paula-Barbosa M.M. Protein malnutrition alters the cholinergic and GABAergic systems of the hippocampal formation of the adult rat: an immunocytochemical study. Neurosci. Lett. 1996, 211:211-215.
7. Baimbridge K.G., Celio M.R., Rogers J.H. Calcium-binding proteins in the nervous system. Trends Neurosci. 1992, 15:303-308.
8. Barinka F., Druga R. Calretinin expression in the mammalian neocortex: a review. Physiol. Res. 2010, 59:665-677.
9. Cardoso A., Castro J.P., Pereira P.A., Andrade J.P. Prolonged protein deprivation, but not food restriction, affects parvalbumin-containing interneurons in the dentate gyrus of adult rats. Brain Res. 2013, 1522:22-30.
10. Cardoso A., Paula-Barbosa M.M., Lukoyanov N.V. Reduced density of neuropeptide Y neurons in the somatosensory cortex of old male and female rats: relation to cholinergic depletion and recovery after nerve growth factor treatment. Neuroscience 2006, 137:937-948.
11. Celio M.R. Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 1990, 35:375-475.
12. Chard P.S., Bleakman D., Christakos S., Fullmer C.S., Miller R.J. Calcium buffering properties of calbindin D28k and parvalbumin in rat sensory neurones. J. Physiol. 1993, 472:341-357.
13. Cintra L., Granados L., Aguilar A., Kemper T., DeBassio W., Galler J., Morgane P., Duran P., Diaz-Cintra S. Effects of prenatal protein malnutrition on mossy fibers of the hippocampal formation in rats of four age groups. Hippocampus 1997, 7:184-191.
14. de Jong G.I., Naber P.A., Van der Zee E.A., Thompson L.T., Disterhoft J.F., Luiten P.G. Age-related loss of calcium binding proteins in rabbit hippocampus. Neurobiol. Aging 1996, 17:459-465.
15. Debassio W.A., Kemper T.L., Tonkiss J., Galler J.R. Effect of prenatal protein deprivation on postnatal granule cell generation in the hippocampal dentate gyrus. Brain Res. Bull. 1996, 41:379-383.
16. DeFelipe J. Types of neurons, synaptic connections and chemical characteristics of cells immunoreactive for calbindin-D28K, parvalbumin and calretinin in the neocortex. J. Chem. Neuroanat. 1997, 14:1-19.
17. Diaz-Cintra S., Gonzalez-Maciel A., Morales M.A., Aguilar A., Cintra L., Prado-Alcala R.A. Protein malnutrition differentially alters the number of glutamic acid decarboxylase-67 interneurons in dentate gyrus and CA1-3 subfields of the dorsal hippocampus. Exp. Neurol. 2007, 208:47-53.
18. Einon D.F., Morgan M.J. A critical period for social isolation in the rat. Dev. Psychobiol. 1977, 10:123-132.
19. Ferdman N., Murmu R.P., Bock J., Braun K., Leshem M. Weaning age, social isolation, and gender, interact to determine adult explorative and social behavior, and dendritic and spine morphology in prefrontal cortex of rats. Behav. Brain Res. 2007, 180:174-182.
20. Freund T.F. Interneuron diversity series: rhythm and mood in perisomatic inhibition. Trends Neurosci. 2003, 26:489-495.
21. Freund T.F., Buzsáki G. Interneurons of the hippocampus. Hippocampus 1996, 6:347-470.
22. Gomes da Silva S., Dona F., da Silva Fernandes M.J., Scorza F.A., Cavalheiro E.A., Arida R.M. Physical exercise during the adolescent period of life increases hippocampal parvalbumin expression. Brain Dev. 2010, 32:137-142.
23. Greene J.R., Kerkhoff J.E., Guiver L., Totterdell S. Structural and functional abnormalities of the hippocampal formation in rats with environmentally induced reductions in prepulse inhibition of acoustic startle. Neuroscience 2001, 103:315-323.
24. Gúlyas A.I., Hajos N., Freund T.F. Interneurons containing calretinin are specialized to control other interneurons in the rat hippocampus. J. Neurosci. 1996, 16:3397-3411.
25. Harte M.K., Powell S.B., Swerdlow N.R., Geyer M.A., Reynolds G.P. Deficits in parvalbumin and calbindin immunoreactive cells in the hippocampus of isolation reared rats. J. Neural. Transm. 2007, 114:893-898.
26. Heizmann C.W. Calcium signaling in the brain. Acta Neurobiol. Exp. 1993, 53:15-23.
27. Idrizbegovic E., Bogdanovic N., Willott J.F., Canlon B. Age-related increases in calcium-binding protein immunoreactivity in the cochlear nucleus of hearing impaired C57BL/6J mice. Neurobiol. Aging 2004, 25:1085-1093.
28. Laus M.F., Vales L.D., Costa T.M., Almeida S.S. Early postnatal protein-calorie malnutrition and cognition: a review of human and animal studies. Int. J. Environ. Res. Public Health 2011, 8:590-612.
29. Lister J.P., Blatt G.J., DeBassio W.A., Kemper T.L., Tonkiss J., Galler J.R., Rosene D.L. Effect of prenatal protein malnutrition on numbers of neurons in the principal cell layers of the adult rat hippocampal formation. Hippocampus 2005, 15:393-403.
30. Lister J.P., Blatt G.J., Kemper T.L., Tonkiss J., DeBassio W.A., Galler J.R., Rosene D.L. Prenatal protein malnutrition alters the proportion but not numbers of parvalbumin-immunoreactive interneurons in the hippocampus of the adult Sprague-Dawley rat. Nutr. Neurosci. 2011, 14:165-178.
31. Lukoyanov N.V., Andrade J.P. Behavioral effects of protein deprivation and rehabilitation in adult rats: relevance to morphological alterations in the hippocampal formation. Behav. Brain Res. 2000, 112:85-97.
32. Maglóczky Z., Freund T.F. Impaired and repaired inhibitory circuits in the epileptic human hippocampus. Trends Neurosci. 2005, 28:334-340.
33. Miller R.J. Regulation of calcium homoeostasis in neurons: the role of calcium-binding proteins. Biochem. Soc. Trans. 1995, 23:629-632.
34. Morgane P.J., Mokler D.J., Galler J.R. Effects of prenatal protein malnutrition on the hippocampal formation. Neurosci. Biobehav. Rev. 2002, 26:471-483.
35. Paula-Barbosa M.M., Andrade J.P., Castedo J.L., Azevedo F.P., Camões I., Volk B., Tavares M.A. Cell loss in the cerebellum and hippocampal formation of adult rats after long-term low-protein diet. Exp. Neurol. 1989, 103:186-193.
36. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 1998, Academic Press, San Diego.
37. Sauer J.F., Bartos M. Recruitment of early postnatal parvalbumin-positive hippocampal interneurons by GABAergic excitation. J. Neurosci. 2010, 30:110-115.
38. Steiger J.L., Alexander M.J., Galler J.R., Farb D.H., Russek S.J. Effects of prenatal malnutrition on GABAA receptor alpha1, alpha3 and beta2 mRNA levels. Neuroreport 2003, 14:1731-1735.