Prolonged protein deprivation, but not food restriction, affects parvalbumin-containing interneurons in the dentate gyrus of adult rats

Brain Research

Volumn 1522, Issue , 2013, Pages 22-30

  Cardoso, Armando ^a   Castro, João Paulo ^a   Pereira, Pedro Alberto ^a   Andrade, José Paulo ^a  

^a University of Porto   (Portugal)

Author keywords

Dentate gyrus; Food restriction; Parvalbumin; Protein deprivation

Indexed keywords

PARVALBUMIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM HOMEOSTASIS; CELL PROTECTION; CONTROLLED STUDY; DENTATE GYRUS; DIET RESTRICTION; GRANULE CELL; INTERNEURON; KWASHIORKOR; MALE; MEMORY DISORDER; NONHUMAN; PRIORITY JOURNAL; PROTEIN DIET; PROTEIN RESTRICTION; RAT; UPREGULATION;

ANIMALS; CELL COUNT; DENTATE GYRUS; DIET, PROTEIN-RESTRICTED; IMMUNOHISTOCHEMISTRY; INTERNEURONS; MALE; PARVALBUMINS; PROTEIN DEFICIENCY; RATS; RATS, WISTAR;

ANIMALIA; RATTUS;

EID: 84879798918     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2013.05.034     Document Type: Article

References (66)

1. M. Alamy, and W.A. Bengelloun Malnutrition and brain development: an analysis of the effects of inadequate diet during different stages of life in rat Neurosci. Biobehav. Rev. 36 2012 1463 1480
2. J. Altman, and S.A. Bayer Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods J. Comp. Neurol. 301 1990 365 381
3. D.G. Amaral, and M.P. Witter The hippocampal formation G. Paxinos, The Rat Nervous System 1995 Academic Press San Diego 443 493
4. J.P. Andrade, M.D. Madeira, and M.M. Paula-Barbosa Effects of long-term malnutrition and rehabilitation on the hippocampal formation of the adult rat. A morphometric study J. Anat. 187 Pt 2 1995 379 393
5. J.P. Andrade, A.J. Castanheira-Vale, P.G. Paz-Dias, M.D. Madeira, and M.M. Paula-Barbosa The dendritic trees of neurons from the hippocampal formation of protein-deprived adult rats. A quantitative Golgi study Exp. Brain Res. 109 1996 419 433
6. J.P. Andrade, and M.M. Paula-Barbosa Protein malnutrition alters the cholinergic and GABAergic systems of the hippocampal formation of the adult rat: an immunocytochemical study Neurosci. Lett. 211 1996 211 215
7. J.P. Andrade, M.D. Madeira, and M.M. Paula-Barbosa Differential vulnerability of the subiculum and entorhinal cortex of the adult rat to prolonged protein deprivation Hippocampus 8 1998 33 47
8. 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
9. J.P. Andrade, R. Mesquita, M. Assuncão, and P.A. Pereira Effects of food restriction on synthesis and expression of brain-derived neurotrophic factor and tyrosine kinase B in dentate gyrus granule cells of adult rats Neurosci. Lett. 399 2006 135 140
10. S.A. Bayer Development of the hippocampal region in the rat. I. Neurogenesis examined with 3H-thymidine autoradiography J. Comp. Neurol. 190 1980 87 114
11. S.A. Bayer Changes in the total number of dentate granule cells in juvenile and adult rats: a correlated volumetric and 3H-thymidine autoradiographic study Exp. Brain Res. 46 1982 315 323
12. K.J. Bough, R. Valiyil, F.T. Han, and D.A. Eagles Seizure resistance is dependent upon age and calorie restriction in rats fed a ketogenic diet Epilepsy Res. 35 1999 21 28
13. D.R. Brady, and E.J. Mufson Parvalbumin-immunoreactive neurons in the hippocampal formation of Alzheimer's diseased brain Neuroscience 80 1997 1113 1125
14. A.J. Bruce-Keller, G. Umberger, R. McFall, and M.P. Mattson Food restriction reduces brain damage and improves behavioral outcome following excitotoxic and metabolic insults Ann. Neurol. 45 1999 8 15
15. A. Cardoso, M.M. Paula-Barbosa, and N.V. Lukoyanov 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 137 2006 937 948
16. M.R. Celio Calbindin D-28k and parvalbumin in the rat nervous system Neuroscience 35 1990 375 475
17. P.S. Chard, D. Bleakman, S. Christakos, C.S. Fullmer, and R.J. Miller Calcium buffering properties of calbindin D28k and parvalbumin in rat sensory neurones J. Physiol. 472 1993 341 357
18. L. Cintra, S. Diaz-Cintra, A. Galvan, T. Kemper, and P.J. Morgane Effects of protein undernutrition on the dentate gyrus in rats of three age groups Brain Res. 532 1990 271 277
19. L. Cintra, L. Granados, A. Aguilar, T. Kemper, W. DeBassio, J. Galler, P. Morgane, P. Duran, and S. Diaz-Cintra Effects of prenatal protein malnutrition on mossy fibers of the hippocampal formation in rats of four age groups Hippocampus 7 1997 184 191
20. R.J. Colman, R.M. Anderson, S.C. Johnson, E.K. Kastman, K.J. Kosmatka, T.M. Beasley, D.B. Allison, C. Cruzen, H.A. Simmons, J.W. Kemnitz, and R. Weindruch Caloric restriction delays disease onset and mortality in rhesus monkeys Science 325 2009 201 204
21. G.I. de Jong, P.A. Naber, E.A. Van der Zee, L.T. Thompson, J.F. Disterhoft, and P.G. Luiten Age-related loss of calcium binding proteins in rabbit hippocampus Neurobiol. Aging. 17 1996 459 465
22. W.A. Debassio, T.L. Kemper, J. Tonkiss, and J.R. Galler Effect of prenatal protein deprivation on postnatal granule cell generation in the hippocampal dentate gyrus Brain Res. Bull. 41 1996 379 383
23. J. DeFelipe Types of neurons, synaptic connections and chemical characteristics of cells immunoreactive for calbindin-D28K, parvalbumin and calretinin in the neocortex J. Chem. Neuroanat. 14 1997 1 19
24. W. Duan, and M.P. Mattson Dietary restriction and 2-deoxyglucose administration improve behavioral outcome and reduce degeneration of dopaminergic neurons in models of Parkinson's disease J. Neurosci. Res. 57 1999 195 206
25. P. Duran, M. Miranda-Anaya, J. Romero-Sanchez Mde, K. Mondragon-Soto, L. Granados-Rojas, and L. Cintra Time-place learning is altered by perinatal low-protein malnutrition in the adult rat Nutr. Neurosci. 14 2011 145 150
26. A.A. Farooqui, and L.A. Horrocks Excitatory amino acid receptors, neural membrane phospholipid metabolism and neurological disorders Brain Res. Brain Res. Rev. 16 1991 171 191
27. T.A. Fiacco, D.L. Rosene, J.R. Galler, and G.J. Blatt 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 2003 350 360
28. L. Fontana, L. Partridge, and V.D. Longo Extending healthy life span - from yeast to humans Science 328 2010 321 326
29. T.F. Freund Interneuron Diversity series: rhythm and mood in perisomatic inhibition Trends Neurosci. 26 2003 489 495
30. S. Garcia-Belenguer, C. Oliver, and P. Mormede Facilitation and feedback in the hypothalamo-pituitary-adrenal axis during food restriction in rats J. Neuroendocrinol. 5 1993 663 668
31. S. Gomes da Silva, F. Dona, M.J. da Silva Fernandes, F.A. Scorza, E.A. Cavalheiro, and R.M. Arida Physical exercise during the adolescent period of life increases hippocampal parvalbumin expression Brain Dev. 32 2010 137 142
32. P. Gressens, S.M. Muaku, L. Besse, E. Nsegbe, J. Gallego, B. Delpech, C. Gaultier, P. Evrard, J.M. Ketelslegers, and D. Maiter Maternal protein restriction early in rat pregnancy alters brain development in the progeny Brain Res. Dev. Brain Res. 103 1997 21 35
33. H.J. Gundersen, and E.B. Jensen The efficiency of systematic sampling in stereology and its prediction J. Microsc. 147 1987 229 263
34. H.J. Gundersen, T.F. Bendtsen, L. Korbo, N. Marcussen, A. Møller, K. Nielsen, J.R. Nyengaard, B. Pakkenberg, F.B. Sørensen, A. Vesterby, and M.J. West Some new, simple and efficient stereological methods and their use in pathological research and diagnosis APMIS 96 1988 379 394
35. H.J. Gundersen, E.B. Jensen, K. Kiêu, and J. Nielsen The efficiency of systematic sampling in stereology - reconsidered J. Microsc. 193 1999 199 211
36. R.W. Hart, J.E. Leakey, M. Chou, P.H. Duffy, W.T. Allaben, and R.J. Feuers Modulation of chemical toxicity by modification of caloric intake Adv. Exp. Med. Biol. 322 1992 73 81
37. C.W. Heizmann Calcium signaling in the brain Acta Neurobiol. Exp. (Wars) 53 1993 15 23
38. Z.L. Huang, and P.J. Fraker Chronic consumption of a moderately low protein diet does not alter hematopoietic processes in young adult mice J. Nutr. 133 2003 1403 1408
39. E. Idrizbegovic, N. Bogdanovic, J.F. Willott, and B. Canlon Age-related increases in calcium-binding protein immunoreactivity in the cochlear nucleus of hearing impaired C57BL/6J mice Neurobiol. Aging 25 2004 1085 1093
40. R.S. King, W.A. DeBassio, T.L. Kemper, D.L. Rosene, J. Tonkiss, J.R. Galler, and G.J. Blatt Effects of prenatal protein malnutrition and acute postnatal stress on granule cell genesis in the fascia dentata of neonatal and juvenile rats Dev. Brain Res. 150 2004 9 15
41. M.F. Laus, L.D. Vales, T.M. Costa, and S.S. Almeida Early postnatal protein-calorie malnutrition and cognition: a review of human and animal studies Int. J. Environ. Res. Public Health 8 2011 590 612
42. Y.A. Lawrence, T.L. Kemper, M.L. Bauman, and G.J. Blatt Parvalbumin-, calbindin-, and calretinin-immunoreactive hippocampal interneuron density in autism Acta Neurol. Scand. 121 2010 99 108
43. J.P. Lister, G.J. Blatt, W.A. DeBassio, T.L. Kemper, J. Tonkiss, J.R. Galler, and D.L. Rosene Effect of prenatal protein malnutrition on numbers of neurons in the principal cell layers of the adult rat hippocampal formation Hippocampus 15 2005 393 403
44. J.P. Lister, J. Tonkiss, G.J. Blatt, T.L. Kemper, W.A. DeBassio, J.R. Galler, and D.L. Rosene Asymmetry of neuron numbers in the hippocampal formation of prenatally malnourished and normally nourished rats: a stereological investigation Hippocampus 16 2006 946 958
45. J.P. Lister, G.J. Blatt, T.L. Kemper, J. Tonkiss, W.A. DeBassio, J.R. Galler, and D.L. Rosene Prenatal protein malnutrition alters the proportion but not numbers of parvalbumin-immunoreactive interneurons in the hippocampus of the adult Sprague-Dawley rat Nutr. Neurosci. 14 2011 165 178
46. F.H. Lopes da Silva, M.P. Witter, P.H. Boeijinga, and A.H. Lohman Anatomic organization and physiology of the limbic cortex Physiol. Rev. 70 1990 453 511
47. J. Luebke St, J. John, and J.R. Galler Prenatal protein malnutrition results in increased frequency of miniature inhibitory synaptic currents in rat CA1 pyramidal cells Synapse 37 2000 23 31
48. N.V. Lukoyanov, and J.P. Andrade Behavioral effects of protein deprivation and rehabilitation in adult rats: relevance to morphological alterations in the hippocampal formation Behav. Brain Res. 112 2000 85 97
49. M.D. Madeira, A. Cadete-Leite, J.P. Andrade, and M.M. Paula-Barbosa Effects of hypothyroidism upon the granular layer of the dentate gyrus in male and female adult rats: a morphometric study J. Comp. Neurol. 314 1991 171 186
50. J.A. Mattison, G.S. Roth, T.M. Beasley, E.M. Tilmont, A.M. Handy, R.L. Herbert, D.L. Longo, D.B. Allison, J.E. Young, M. Bryant, D. Barnard, W.F. Ward, W. Qi, D.K. Ingram, and R. de Cabo Impact of caloric restriction on health and survival in rhesus monkeys from the NIA study Nature 489 2012 318 321
51. R.M. Mesquita, P.A. Pereira, and J.P. Andrade Low levels of brain-derived neurotrophic factor and tyrosine kinase receptor B are related to loss of dentate granule cells after prolonged low-protein feeding in the rat Neurosci. Lett. 330 2002 155 158
52. P.J. Morgane, D.J. Mokler, and J.R. Galler Effects of prenatal protein malnutrition on the hippocampal formation Neurosci. Biobehav. Rev. 26 2002 471 483
53. M.M. Paula-Barbosa, J.P. Andrade, J.L. Castedo, F.P. Azevedo, I. Camoes, B. Volk, and M.A. Tavares Cell loss in the cerebellum and hippocampal formation of adult rats after long-term low-protein diet Exp. Neurol. 103 1989 186 193
54. G. Paxinos, and C. Watson The Rat Brain in Stereotaxic Coordinates fourth ed. 1998 Academic Press San Diego
55. L.W. Roth, and A.J. Polotsky Can we live longer by eating less? A review of caloric restriction and longevity Maturitas 71 2012 315 319
56. J.F. Sauer, and M. Bartos Recruitment of early postnatal parvalbumin-positive hippocampal interneurons by GABAergic excitation J. Neurosci. 30 2010 110 115
57. R. Schmidt-Kastner, D. Meller, and U.T. Eysel Immunohistochemical changes of neuronal calcium-binding proteins parvalbumin and calbindin-D-28k following unilateral deafferentation in the rat visual system Exp. Neurol. 117 1992 230 246
58. B. Schwaller, I.V. Tetko, P. Tandon, D.C. Silveira, M. Vreugdenhil, T. Henzi, M.C. Potier, M.R. Celio, and A.E. Villa Parvalbumin deficiency affects network properties resulting in increased susceptibility to epileptic seizures Mol. Cell Neurosci. 25 2004 650 663
59. K. Seidel, C. Helmeke, G. Poeggel, and K. Braun Repeated neonatal separation stress alters the composition of neurochemically characterized interneuron subpopulations in the rodent dentate gyrus and basolateral amygdala Dev. Neurobiol. 68 2008 1137 1152
60. L. Seress Comparative anatomy of the hippocampal dentate gyrus in adult and developing rodents, non-human primates and humans H.E. Scharfman, The Dentate Gyrus: A Comprehensive Guide to Structure, Function, and Clinical Implications 2007 Elsevier Amsterdam 23 41
61. S.R. Smith, T. Bledsoe, and M.K. Chhetri Cortisol metabolism and the pituitary-adrenal axis in adults with protein-calorie malnutrition J. Clin. Endocrinol. Metab. 40 1975 43 52
62. E.Y. Sonoda, S. Gomes da Silva, R.M. Arida, P.N. Giglio, N.F. Margarido, C.A. Martinez, A.P. Pansani, S. Maciel Rde, E.A. Cavalheiro, and F.A. Scorza Hippocampal plasticity in rats submitted to a gastric restrictive procedure Nutr. Neurosci. 14 2011 181 185
63. W.C. Stern, W.B. Forbes, O. Resnick, and P.J. Morgane Seizure susceptibility and brain amine levels following protein malnutrition during development in the rat Brain Res. 79 1974 375 384
64. T. Szilagyi, K. Orban-Kis, E. Horvath, J. Metz, Z. Pap, and Z. Pavai Morphological identification of neuron types in the rat hippocampus Rom. J. Morphol. Embryol. 52 2011 15 20
65. M. Vreugdenhil, J.G. Jefferys, M.R. Celio, and B. Schwaller Parvalbumin-deficiency facilitates repetitive IPSCs and gamma oscillations in the hippocampus J. Neurophysiol. 89 2003 1414 1422
66. M.J. West, L. Slomianka, and H.J. Gundersen Unbiased stereological estimation of the total number of neurons in thesubdivisions of the rat hippocampus using the optical fractionator Anat. Rec. 231 1991 482 497