Postnatal protein malnutrition induces neurochemical alterations leading to behavioral deficits in rats: Prevention by selenium or zinc supplementation

Nutritional Neuroscience

Volumn 17, Issue 6, 2014, Pages 268-278

  Adebayo, Olusegun L ^a,b,c   Adenuga, Gbenga A ^c   Sandhir, Rajat ^a  

^a PANJAB UNIVERSITY   (India)

^b REDEEMER S UNIVERSITY   (Nigeria)

^c OLABISI ONABANJO UNIVERSITY   (Nigeria)

Author keywords

Behavior; Brain; Oxidative stress; Protein malnutrition; Selenium; Zinc

Indexed keywords

CARBONYL DERIVATIVE; CATALASE; GLUTATHIONE; GLUTATHIONE REDUCTASE; GLUTATHIONE TRANSFERASE; NITRITE; SELENIUM; SUPEROXIDE DISMUTASE; THIOL; ZINC; ANTIOXIDANT; PROTEIN INTAKE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR DISORDER; CEREBELLUM; CONTROLLED STUDY; ELEVATED PLUS MAZE TEST; KWASHIORKOR; LIPID PEROXIDATION; LOCOMOTION; MALE; MINERAL SUPPLEMENTATION; NEUROCHEMISTRY; NONHUMAN; OXIDATIVE STRESS; PROTEIN ANALYSIS; RAT; ADMINISTRATION AND DOSAGE; ANIMAL; BLOOD; BRAIN CORTEX; COMPLICATION; DIET SUPPLEMENTATION; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; MENTAL DISORDERS; METABOLISM; PATHOLOGY; PROTEIN CARBONYLATION; PROTEIN INTAKE; PROTEIN-ENERGY MALNUTRITION; WISTAR RAT;

ANIMALIA; RATTUS;

ANIMALS; ANTIOXIDANTS; CATALASE; CEREBELLUM; CEREBRAL CORTEX; DIETARY PROTEINS; DIETARY SUPPLEMENTS; GLUTATHIONE; LIPID PEROXIDATION; MALE; MENTAL DISORDERS; NITRITES; OXIDATIVE STRESS; PROTEIN CARBONYLATION; PROTEIN-ENERGY MALNUTRITION; RATS; RATS, WISTAR; SELENIUM; SUPEROXIDE DISMUTASE; ZINC;

EID: 84919418821     PISSN: 1028415X     EISSN: 14768305     Source Type: Journal    
DOI: 10.1179/1476830513Y.0000000090     Document Type: Article

References (77)

1. Lukoyanov NV, Andrade JP. 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.
2. Morgane PJ, Mokler DJ, Galler JR. Effects of prenatal protein malnutrition on the hippocampal formation. Neurosci Biobehav Rev 2002;26:471–83.
3. Valadares CT, Fukuda MT, Francolin-Silva AL, Hernandes AS, Almeida SS. Effects of postnatal protein malnutrition on learning and memory procedures. Nutr Neurosci 2010;13:274–82.
4. da Silva Hernandes A, Francolin-Silva AL, Valadares CT, Fukuda MT, Almeida SS. Effects of different malnutrition techniques on the behavior of rats tested in the elevated T-maze. Behav Brain Res 2005;162:240–5.
5. Huang LT, Lai MC, Wang CL, Wang CA, Yang CH, Hsieh CS, et al. Long-term effects of early-life malnutrition and status epi-lepticus: assessment by spatial navigation and CREB(Serine-133) phosphorylation. Brain Res Dev Brain Res 2003;145:213–8.
6. Bonatto F, Polydoro M, Andrades ME, Conte da Frota ML, Jr, Dal-Pizzol F, Rotta LN, et al. Effects of maternal protein malnutrition on oxidative markers in the young rat cortex and cerebellum. Neurosci Lett 2006;406:281–4.
7. Nunes ML, Batista BB, Micheli F, Batistella V. Effects of early malnutrition and nutritional rehabilitation in rats. J Pediatr (Rio J) 2002;78:39–44.
8. Adebayo OL, Shallie PD, Salau BA, Ajani EO, Adenuga GA. Comparative study on the influence of fluoride on lipid peroxi-dation and antioxidants levels in the different brain regions of well-fed and protein undernourished rats. J Trace Elem Med Biol 2013.
9. Lima JG, Oliveira LM, Lachat JJ, Dal-Bo CM, Almeida SS. Comparison of the effects of lab chow and casein diets based on body and brain development of rats. Braz J Med Biol Res 1993;26:1069–76.
10. Gutierrez-Ospina G, Manjarrez-Gutierrez G, Gonzalez C, Lopez S, Herrera R, Medina Aguirre I, et al. Neither increased nor decreased availability of cortical serotonin (5HT) disturbs barrel field formation in isocaloric undernourished rat pups. Int J Dev Neurosci 2002;20:497–501.
11. Soares EG, De-Oliveira LM, Pereira-Da-Silva MS. Effects of protein malnutrition on newly-weaned rats: effects on behavior, brain catecholamines and nucleic acids. Neurobiology 2008;71: 35–49.
12. Mathangi DC, Namasivayam A. Effect of chronic protein restriction on motor co-ordination and brain neurotransmitters in albino rats. Food Chem Toxicol 2001;39:1039–43.
13. Chen J, Berry MJ. Selenium and selenoproteins in the brain and brain diseases. J Neurochem 2003;86:1–12.
14. Rukmini MS, D’Souza B, D’Souza V. Superoxide dismutase and catalase activities and their correlation with malondialdehyde in schizophrenic patients. Indian J Clin Biochem 2004;11:719–24.
15. Garcia YJ, Rodriguez-Malaver AJ, Penaloza N. Lipid peroxi-dation measurement by thiobarbituric acid assay in rat cerebellar slices. J Neurosci Methods 2005;144:127–35.
16. McGrath LT, McGleenon BM, Brennan S, McColl D, Mc IS, Passmore AP. Increased oxidative stress in Alzheimer’s disease as assessed with 4-hydroxynonenal but not malondialdehyde. QJM 2001;94:485–90.
17. Adebayo OL, Adenuga GA. Protective effect of selenium on protein-undernutrition-induced brain damage in rats. Biol Trace Elem Res 2007;116:227–34.
18. Ishrat T, Parveen K, Khan MM, Khuwaja G, Khan MB, Yousuf S, et al. Selenium prevents cognitive decline and oxidative damage in rat model of streptozotocin-induced experimental dementia of Alzheimer’s type. Brain Res 2009;1281:117–27.
19. Wirth EK, Conrad M, Winterer J, Wozny C, Carlson BA, Roth S, et al. Neuronal selenoprotein expression is required for inter-neuron development and prevents seizures and neurodegenera-tion. FASEB J 2010;24:844–52.
20. Papp LV, Lu J, Holmgren A, Khanna KK. From selenium to selenoproteins: synthesis, identity, and their role in human health. Antioxid Redox Signal 2007;9:775–806.
21. Eersel J, Ke YD, Liu X, Delerue F, Kril JJ, Götz J, et al. Sodium selenate mitigates tau pathology, neurodegeneration, and functional deficits in Alzheimer’s disease models. Proc Natl Acad Sci USA 2010;107:13888–93.
22. Benton D. Selenium intake, mood and other aspects of psychological functioning. Nutr Neurosci 2002;5:363–74.
23. Porciuncula LO, Rocha JBT, Boeck CR, Vendite D, Souza DO. Ebselen prevents excitotoxicity provoked by glutamate in rat cer-ebellar granule neurons. Neurosci Lett 2001;299:217–20.
24. Powell SR. The antioxidant properties of zinc. J Nutr 2000; 130(5S Suppl):1447S–54S.
25. Santos CRA, Martinho A, Quintela T, Goncalves I. Neuroprotective and neuroregenerative properties of metal-lothioneins IUBMB life. 2012;64:126–35.
26. Levitsky DA, Strupp BJ. Malnutrition and the brain: changing concepts, changing concerns. J Nutr 1995;125(8 Suppl): 2212S–20S.
27. Partadiredja G, Simpson R, Bedi KS. The effects of pre-weaning undernutrition on the expression levels of free radical deactivating enzymes in the mouse brain. Nutr Neurosci 2005;8:183–93.
28. Partadiredja G, Bedi KS. Mice undernourished before, but not after, weaning performed better in motor coordination and spatial learning tasks than well-fed controls. Nutr Neurosci 2011;14:129–35.
29. Bhasin P, Singla N, Dhawan DK. Protective role of zinc during aluminum-induced hepatotoxicity. Environ Toxicol 2012.
30. Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 1979;95:351–8.
31. Green LC, Wagner DA, Gologwski J, Skipper PL, Wishnok JS, Tannenbaum SR. Analysis of nitrate, nitrite and [15N] nitrate in biological fluids. Anal Biochem 1972;126:131–8.
32. Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz AG, et al. Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol 1990;186:464–78.
33. Hissin PJ, Hilf R. A fluorometric method for determination of oxidized and reduced glutathione in tissues. Anal Biochem 1976;74:214–26.
34. Luck H. Catalase: methods of enzymatic analysis. In: Bergmeyer HU, (ed.) New York: Academic Press; 1971. p. 885–93.
35. Kono Y. Generation of superoxide radical during autoxidation of hydroxylamine and an assay for superoxide dismutase. Arch Biochem Biophys 1978;186:189–95.
36. Carlberg I, Mannervik B. Glutathione reductase assay. In: Methods in enzymology. Volume 113. Orlando: Academic Press; 1985. p. 484–95.
37. Habig WH, Pabst MJ, Jakoby WB. Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 1974;249:7130–9.
38. Frussa-Filho R, Abilio VC, Bergamo M, Palermo-Neto J. Behavioural subsensitivity induced by long-term administration of a low dose of haloperidol to rats. J Pharm Pharmacol 1997; 49:412–5.
39. Itoh J, Nabeshima T, Kameyama T. Utility of an elevated plus-maze for dissociation of amnesic and behavioral effects of drugs in mice. Eur J Pharmacol 1991;194:71–6.
40. Lowry OH, Rosebrough NJ, Farr AL, Randall NJ. Protein measurement with folin phenol reagent. J Biol Chem 1951;193: 265–75.
41. Camargo LM, Nascimento AB, Almeida SS. Differential response to gepirone but not to chlordiazepoxide in malnourished rats subjected to learned helplessness. Braz J Med Biol Res 2008;41:54–9.
42. Fukuda MT, Francolin-Silva AL, Almeida SS. Early postnatal protein malnutrition affects learning and memory in the distal but not in the proximal cue version of the Morris water maze. Behav Brain Res 2002;133:271–7.
43. Shahjadi S, Khan AS, Akhter QS, Aktern N, Hasan SMMMA, Rahman T. Serum free triiodothyronine and thyroid stimulating hormone level in severe protein energy malnourished children. J Dhaka Med Coll 2011;20:174–7.
44. Reyes-Castro LA, Rodriguez JS, Rodriguez-Gonzalez GL, Wimmer RD, McDonald TJ, Larrea F, et al. Pre- and/or postnatal protein restriction in rats impairs learning and motivation in male offspring. Int J Dev Neurosci 2011;29:177–82.
45. Portman OW, Neuringer M, Alexander M. Effects of maternal and long-term postnatal protein malnutrition on brain size and composition in rhesus monkeys. J Nutr 1987;117:1844–51.
46. Bonatto F, Polydoro M, Andrades ME, da Frota Junior ML, Dal-Pizzol F, Rotta LN, et al. Effect of protein malnutrition on redox state of the hippocampus of rat. Brain Res 2005; 1042:17–22.
47. Martinez Y, Diaz-Cintra S, Leon-Jacinto U, Aguilar-Vazquez A, Medina AC, Quirarte GL, et al. Effects of postnatal malnutrition and senescence on learning, long-term memory, and extinction in the rat. Behav Brain Res 2009;203:48–53.
48. Salgueiro MJ, Zubillaga MB, Lysionek AE, Caro RA, Weill R, Boccio JR. The role of zinc in the growth and development of children. Nutrition 2002;18:510–9.
49. Ladd FV, Ladd AA, Ribeiro AA, Costa SB, Coutinho BP, Feitosa GA, et al. Zinc and glutamine improve brain development in suckling mice subjected to early postnatal malnutrition. Nutrition 2010;26:662–70.
50. Goulart EC, Pereira CA, Garcia RC, Giacomelli MB, Rodrigues AL. Effects of lead and/or zinc exposure during the second stage of rapid postnatal brain growth on delta-aminolevulinate dehy-dratase and negative geotaxis of suckling rats. Braz J Med Biol Res 2001;34:785–90.
51. Sidhu P, Garg ML, Dhawan DK. Protective effects of zinc on oxidative stress enzymes in liver of protein deficient rats. Nutr Hosp 2004;19:341–7.
52. Tatli M, Guzel A, Kizil G, Kavak V, Yavuz M, Kizil M. Comparison of the effects of maternal protein malnutrition and intrauterine growth restriction on redox state of central nervous system in offspring rats. Brain Res 2007;1156:21–30.
53. Violi F, Marino R, Milite MT, Loffredo L. Nitric oxide and its role in lipid peroxidation. Diabetes Metab Res Rev 1999;15: 283–8.
54. Tarry-Adkins JL, Martin-Gronert MS, Fernandez-Twinn DS, Hargreaves I, Alfaradhi MZ, Land JM, et al. Poor maternal nutrition followed by accelerated postnatal growth leads to alterations in DNA damage and repair, oxidative and nitrosative stress, and oxidative defense capacity in rat heart. FASEB J 2013; 27:379–90.
55. Alam ZI, Daniel SE, Lees AJ, Marsden DC, Jenner P, Halliwell B. A generalised increase in protein carbonyls in the brain in Parkinson’s but not incidental Lewy body disease. J Neurochem 1997;69:1326–9.
56. Manary MJ, Leeuwenburgh C, Heinecke JW. Increased oxi-dative stress in Kwashiorkor. J Pediatr 2000;137:421–4.
57. Parihar MS, Pandit MK. Free radical induced increase in protein carbonyl is attenuated by low dose of adenosine in hippocampus and mid brain: implication in neurodegenerative disorders. Gen Physiol Biophys 2003;22:29–39.
58. Feoli AM, Siqueira IR, Almeida L, Tramontina AC, Vanzella C, Sbaraini S, et al. Effects of protein malnutrition on oxidative status in rat brain. Nutrition 2006;22:160–5.
59. Merker K, Grune T. Proteolysis of oxidised proteins and cellular senescence. Exp Gerontol 2000;35:779–86.
60. Reddy KP, Sailaja G, Krishnaiah C. Protective effects of selenium on fluoride induced alterations in certain enzymes in brain of mice. J Environ Biol 2009;30(5 Suppl):859–64.
61. Guzman DC, Ruiza NL, Mejia GB, Garcia EH, Vazqueza IRE, Del Angel DS, et al. Antioxidant effects of selenium in rat brain and the stimulating role of nitric oxide. Nutr Neurosci 2003;6: 177–82.
62. Whanger PD. Selenium and the brain: a review. Nutr Neurosci 2001;4:81–97.
63. Steinbrenner H, Sies H. Selenium homeostasis and antioxidant selenoproteins in brain: implications for disorders in the central nervous system. Arch Biochem Biophys 2013; 536:152–57.
64. Anderson RA, Roussel A, Zouari N, Mahjoub S, Matheau J, Kerkeni A. Potential antioxidant effects of zinc and chromium supplementation in people with type 2 diabetes mellitus. J Am Coll Nutr 2001;20:212–8.
65. Huizinga CT, Engelbregt MJ, Rekers-Mombarg LT, Vaessen SF, Delemarre-van de Waal HA, Fodor M. Ligation of the uterine artery and early postnatal food restriction – animal models for growth retardation. Horm Res 2004;62:233–40.
66. Badary OA, AbdEl-Gawad HM, Taha RA, Ali AA, Hamada FM. Effects of benzo[a]pyrene on tissue activities of metabolizing enzymes and antioxidant system in normal and protein-malnourished rats. J Biochem Mol Toxicol 2003;17:86–91.
67. Zafar KS, Siddiqui A, Sayeed I, Ahmad M, Salim S, Islam F. Dose-dependent protective effect of selenium in rat model of Parkinson’s disease: neurobehavioral and neurochemical evidences. J Neurochem 2003;84:438–46.
68. Sandhir R, Parwani S, Kiran R. Effect of fenvalerate exposure on erythrocyte antioxidant status in protein malnourished rats. Toxicol Environ Chem 2002;83:99–106.
69. Bhalla P, Chadha VD, Dhar R, Dhawan DK. Neuroprotective effects of zinc on antioxidant defense system in lithium treated rat brain. Indian J Exp Biol 2007;45:954–8.
70. Iyyaswamy A, Rathinasamy S. Effect of chronic exposure to aspartame on oxidative stress in the brain of albino rats. J Biosci 2012;37:679–88.
71. Li J, Quan N, Bray TM. Supplementation of N-acetylcysteine normalizes lipopolysaccharide-induced nuclear factor kappa B activation and proinflammatory cytokine production during early rehabilitation of protein malnourished mice. J Nutr 2002; 132:3286–92.
72. Ji L, Nazarali AJ, Paterson PG. Protein-energy malnutrition increases activation of the transcription factor, nuclear factor kappa B, in the gerbil hippocampus following global ischemia. J Nutr Biochem 2008;19:770–7.
73. Tor-Agbidye J, Palmer VS, Spencer PS, Craig AM, Blythe LL, Sabri MI. Sodium cyanate alters glutathione homeostasis in rodent brain: relationship to neurodegenerative diseases in protein-deficient malnourished populations in Africa. Brain Res 1999;820:12–9.
74. Alamy M, Errami M, Taghzouti K, Saddiki-Traki F, Bengelloun WA. Effects of postweaning undernutrition on exploratory behavior, memory and sensory reactivity in rats: implication of the dopaminergic system. Physiol Behav 2005;86:195–202.
75. Rocinholi LF, Landeira-Fernandez J. Anxiety-like behavior in weanling and young adult male and female malnourished rats. Physiol Behav 2011;102:13–6.
76. Almeida SS, Tonkiss J, Galler JR. Prenatal protein malnutrition affects exploratory behavior of female rats in the elevated plus-maze test. Physiol Behav 1996;60:675–80.
77. Alamy M, Bengelloun WA. Malnutrition and brain development: an analysis of the effects of inadequate diet during different stages of life in rat. Neurosci Biobehav Rev 2012;36:1463–80.