Skip to main content Accessibility help
×
Home

Protein undernutrition during development and oxidative impairment in the central nervous system (CNS): potential factors in the occurrence of metabolic syndrome and CNS disease

  • D. J. S. Ferreira (a1), D. F. Sellitti (a2) and C. J. Lagranha (a1) (a3)

Abstract

Mitochondria play a regulatory role in several essential cell processes including cell metabolism, calcium balance and cell viability. In recent years, it has been postulated that mitochondria participate in the pathogenesis of a number of chronic diseases, including central nervous system disorders. Thus, the concept of mitochondrial function now extends far beyond the common view of this organelle as the ‘powerhouse’ of the cell to a new appreciation of the mitochondrion as a transducer of early metabolic insult into chronic disease in later life. In this review, we have attempted to describe some of the associations between nutritional status and mitochondrial function (and dysfunction) during embryonic development with the occurrence of neural oxidative imbalance and neurogenic disease in adulthood.

Copyright

Corresponding author

*Address for correspondence: C. J. Lagranha, Rua Alto do Reservatório, s/n, Núcleo de Educação Física e Ciências do Esporte, Bela Vista, Vitória de Santo Antão 55608-680, PE, Brazil. (Email lagranha@hotmail.com)

References

Hide All
1. Skulachev, VP. Membrane electricity as a convertible energy currency for the cell. Can J Biochem. 1980; 58, 161175.
2. Leverve, XM. Mitochondrial function and substrate availability. Crit Care Med. 2007; 35(Suppl. 9), S454S460.
3. Hagberg, H, Mallard, C, Rousset, CI, Thornton, C. Mitochondria: hub of injury responses in the developing brain. Lancet Neurol. 2014; 13, 217232.
4. Yin, F, Cadenas, E. Mitochondria: the cellular hub of the dynamic coordinated network. Antioxid Redox Signal. 2015; 22, 961964.
5. Ernster, L, Schatz, G. Mitochondria: a historical review. J Cell Biol. 1981; 91(Pt 2), 227s255s.
6. Shaughnessy, DT, McAllister, K, Worth, L, et al. Mitochondria, energetics, epigenetics, and cellular responses to stress. Environ Health Perspect. 2014; 122, 12711278.
7. Porter, MH, Berdanier, CD. Oxidative phosphorylation: key to life. Diabetes Technol Ther. 2002; 4, 253254.
8. Sztark, F, Payen, JF, Piriou, V, et al. Cellular energy metabolism: physiologic and pathologic aspects. Ann Fr Anes Reanim. 1999; 18, 261269.
9. Melov, S. Mitochondrial oxidative stress. Physiologic consequences and potential for a role in aging. Ann N Y Acad Sci. 2000; 908, 219225.
10. Turrens, JF, Freeman, BA, Levitt, JG, Crapo, JD. The effect of hyperoxia on superoxide production by lung submitochondrial particles. Arch Biochem Biophys. 1982; 217, 401410.
11. Boveris, A, Oshino, N, Chance, B. The cellular production of hydrogen peroxide. Biochem J. 1972; 128, 617630.
12. Turrens, JF. Superoxide production by the mitochondrial respiratory chain. Biosci Rep. 1997; 17, 38.
13. Turrens, JF. Mitochondrial formation of reactive oxygen species. J Physiol. 2003; 552(Pt 2), 335344.
14. Figueira, TR, Barros, MH, Camargo, AA, et al. Mitochondria as a source of reactive oxygen and nitrogen species: from molecular mechanisms to human health. Antioxid Redox Signal. 2013; 18, 20292074.
15. Andreyev, AY, Kushnareva, YE, Starkov, AA. Mitochondrial metabolism of reactive oxygen species. Biochemistry (Mosc). 2005; 70, 200214.
16. Halliwell, B. Oxidative stress and neurodegeneration: where are we now? J Neurochem. 2006; 97, 16341658.
17. Halliwell, B. Free radicals and antioxidants: a personal view. Nutr Rev. 1994; 52(Pt 1), 253265.
18. Halliwell, B. Free radicals and antioxidants: updating a personal view. Nutr Rev. 2012; 70, 257265.
19. Flora, SJ. Role of free radicals and antioxidants in health and disease. Cell Mol Biol (Noisy-le-grand). 2007; 53, 12.
20. Jackson, MJ, Papa, S, Bolanos, J, et al. Antioxidants, reactive oxygen and nitrogen species, gene induction and mitochondrial function. Mol Aspects Med. 2002; 23, 209285.
21. Conrad, M, Schick, J, Angeli, JP. Glutathione and thioredoxin dependent systems in neurodegenerative disease: what can be learned from reverse genetics in mice. Neurochem Int. 2013; 62, 738749.
22. Perkins, A, Nelson, KJ, Parsonage, D, Poole, LB, Karplus, PA. Peroxiredoxins: guardians against oxidative stress and modulators of peroxide signaling. Trends Biochem Sci. 2015; 40, 435445.
23. Hirooka, Y. Role of reactive oxygen species in brainstem in neural mechanisms of hypertension. Auton Neurosci. 2008; 142, 2024.
24. Peterson, JR, Sharma, RV, Davisson, RL. Reactive oxygen species in the neuropathogenesis of hypertension. Curr Hypertens Rep. 2006; 8, 232241.
25. Shichiri, M. The role of lipid peroxidation in neurological disorders. J Clin Biochem Nutr. 2014; 54, 151160.
26. Fisher-Wellman, K, Bell, HK, Bloomer, RJ. Oxidative stress and antioxidant defense mechanisms linked to exercise during cardiopulmonary and metabolic disorders. Oxid Med Cell Longev. 2009; 2, 4351.
27. Powers, SK, Jackson, MJ. Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol Rev. 2008; 88, 12431276.
28. Li, JM, Shah, AM. Endothelial cell superoxide generation: regulation and relevance for cardiovascular pathophysiology. Am J Physiol Regul Integr Comp Physiol. 2004; 287, R1014R1030.
29. Pritsos, CA. Cellular distribution, metabolism and regulation of the xanthine oxidoreductase enzyme system. Chem Biol Interact. 2000; 129, 195208.
30. Cantu-Medellin, N, Kelley, EE. Xanthine oxidoreductase-catalyzed reactive species generation: a process in critical need of reevaluation. Redox biology. 2013; 1, 353358.
31. Bedard, K, Krause, KH. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev. 2007; 87, 245313.
32. Murphy, MP. How mitochondria produce reactive oxygen species. Biochem J. 2009; 417, 113.
33. Brand, MD. The sites and topology of mitochondrial superoxide production. Exp Gerontol. 2010; 45, 466472.
34. Quinlan, CL, Orr, AL, Perevoshchikova, IV, et al. Mitochondrial complex II can generate reactive oxygen species at high rates in both the forward and reverse reactions. J Biol Chem. 2012; 287, 2725527264.
35. Fisher-Wellman, KH, Gilliam, LA, Lin, CT, et al. Mitochondrial glutathione depletion reveals a novel role for the pyruvate dehydrogenase complex as a key H2O2-emitting source under conditions of nutrient overload. Free Radic Biol Med. 2013; 65, 12011208.
36. Brautigam, CA, Wynn, RM, Chuang, JL, Chuang, DT. Subunit and catalytic component stoichiometries of an in vitro reconstituted human pyruvate dehydrogenase complex. J Biol Chem. 2009; 284, 1308613098.
37. Ambrus, A, Nemeria, NS, Torocsik, B, et al. Formation of reactive oxygen species by human and bacterial pyruvate and 2-oxoglutarate dehydrogenase multienzyme complexes reconstituted from recombinant components. Free Radic Biol Med. 2015; 89, 642650.
38. Tretter, L, Adam-Vizi, V. Generation of reactive oxygen species in the reaction catalyzed by alpha-ketoglutarate dehydrogenase. J Neurosci. 2004; 24, 77717778.
39. Starkov, AA, Fiskum, G, Chinopoulos, C, et al. Mitochondrial alpha-ketoglutarate dehydrogenase complex generates reactive oxygen species. J Neurosci. 2004; 24, 77797788.
40. Orr, AL, Quinlan, CL, Perevoshchikova, IV, Brand, MD. A refined analysis of superoxide production by mitochondrial sn-glycerol 3-phosphate dehydrogenase. J Biol Chem. 2012; 287, 4292142935.
41. Tretter, L, Takacs, K, Hegedus, V, Adam-Vizi, V. Characteristics of alpha-glycerophosphate-evoked H2O2 generation in brain mitochondria. J Neurochem. 2007; 100, 650663.
42. St-Pierre, J, Buckingham, JA, Roebuck, SJ, Brand, MD. Topology of superoxide production from different sites in the mitochondrial electron transport chain. J Biol Chem. 2002; 277, 4478444790.
43. Perevoshchikova, IV, Quinlan, CL, Orr, AL, Gerencser, AA, Brand, MD. Sites of superoxide and hydrogen peroxide production during fatty acid oxidation in rat skeletal muscle mitochondria. Free Radic Biol Med. 2013; 61, 298309.
44. Di Lisa, F, Kaludercic, N, Carpi, A, Menabo, R, Giorgio, M. Mitochondria and vascular pathology. Pharmacol Rep. 2009; 61, 123130.
45. Youdim, MB, Edmondson, D, Tipton, KF. The therapeutic potential of monoamine oxidase inhibitors. Nat Rev Neurosci. 2006; 7, 295309.
46. Tipton, KF, Boyce, S, O’Sullivan, J, Davey, GP, Healy, J. Monoamine oxidases: certainties and uncertainties. Curr Med Chem. 2004; 11, 19651982.
47. Toninello, A, Salvi, M, Pietrangeli, P, Mondovi, B. Biogenic amines and apoptosis: minireview article. Amino Acids. 2004; 26, 339343.
48. Herrero, A, Barja, G. Localization of the site of oxygen radical generation inside the complex I of heart and nonsynaptic brain mammalian mitochondria. J Bioenerg Biomembr. 2000; 32, 609615.
49. Lambert, AJ, Brand, MD. Superoxide production by NADH:ubiquinone oxidoreductase (complex I) depends on the pH gradient across the mitochondrial inner membrane. Biochem J. 2004; 382(Pt 2), 511517.
50. Babcock, DF, Herrington, J, Goodwin, PC, Park, YB, Hille, B. Mitochondrial participation in the intracellular Ca2+ network. J Cell Biol. 1997; 136, 833844.
51. Takeuchi, A, Kim, B, Matsuoka, S. The destiny of Ca(2+) released by mitochondria. J Physiol Sci. 2015; 65, 1124.
52. Jakob, R, Beutner, G, Sharma, VK, et al. Molecular and functional identification of a mitochondrial ryanodine receptor in neurons. Neurosci Lett. 2014; 575, 712.
53. Van Petegem, F. Ryanodine receptors: structure and function. J Biol Chem. 2012; 287, 3162431632.
54. Csordas, G, Varnai, P, Golenar, T, et al. Imaging interorganelle contacts and local calcium dynamics at the ER-mitochondrial interface. Mol Cell. 2010; 39, 121132.
55. Csordas, G, Hajnoczky, G. SR/ER-mitochondrial local communication: calcium and ROS. Biochim Biophys Acta. 2009; 1787, 13521362.
56. Santo-Domingo, J, Demaurex, N. Calcium uptake mechanisms of mitochondria. Biochim Biophys Acta. 2010; 1797, 907912.
57. Kim, B, Matsuoka, S. Cytoplasmic Na+-dependent modulation of mitochondrial Ca2+ via electrogenic mitochondrial Na+-Ca2+ exchange. J Physiol. 2008; 586, 16831697.
58. Saris, NE, Carafoli, E. A historical review of cellular calcium handling, with emphasis on mitochondria. Biochemistry (Mosc). 2005; 70, 187194.
59. McCormack, JG, Denton, RM. Mitochondrial Ca2+ transport and the role of intramitochondrial Ca2+ in the regulation of energy metabolism. Dev Neurosci. 1993; 15, 165173.
60. Grijalba, MT, Vercesi, AE, Schreier, S. Ca2+-induced increased lipid packing and domain formation in submitochondrial particles. A possible early step in the mechanism of Ca2+-stimulated generation of reactive oxygen species by the respiratory chain. Biochemistry. 1999; 38, 1327913287.
61. Castilho, RF, Kowaltowski, AJ, Meinicke, AR, Bechara, EJ, Vercesi, AE. Permeabilization of the inner mitochondrial membrane by Ca2+ ions is stimulated by t-butyl hydroperoxide and mediated by reactive oxygen species generated by mitochondria. Free Radic Biol Med. 1995; 18, 479486.
62. Rao, VK, Carlson, EA, Yan, SS. Mitochondrial permeability transition pore is a potential drug target for neurodegeneration. Biochim Biophys Acta. 2014; 1842, 12671272.
63. Grancara, S, Battaglia, V, Martinis, P, et al. Mitochondrial oxidative stress induced by Ca2+ and monoamines: different behaviour of liver and brain mitochondria in undergoing permeability transition. Amino Acids. 2012; 42, 751759.
64. Quintanilla, RA, Jin, YN, von Bernhardi, R, Johnson, GV. Mitochondrial permeability transition pore induces mitochondria injury in Huntington disease. Mol Neurodegener. 2013; 8, 45.
65. Frezza, C, Cipolat, S, Martins de Brito, O, et al. OPA1 controls apoptotic cristae remodeling independently from mitochondrial fusion. Cell. 2006; 126, 177189.
66. Mailly, F, Marin, P, Israel, M, Glowinski, J, Premont, J. Increase in external glutamate and NMDA receptor activation contribute to H2O2-induced neuronal apoptosis. J Neurochem. 1999; 73, 11811188.
67. Spencer, WA, Jeyabalan, J, Kichambre, S, Gupta, RC. Oxidatively generated DNA damage after Cu(II) catalysis of dopamine and related catecholamine neurotransmitters and neurotoxins: Role of reactive oxygen species. Free Radic Biol Med. 2011; 50, 139147.
68. Cardaci, S, Filomeni, G, Rotilio, G, Ciriolo, MR. p38(MAPK)/p53 signalling axis mediates neuronal apoptosis in response to tetrahydrobiopterin-induced oxidative stress and glucose uptake inhibition: implication for neurodegeneration. Biochem J. 2010; 430, 439451.
69. Zheng, H, Gal, S, Weiner, LM, et al. Novel multifunctional neuroprotective iron chelator-monoamine oxidase inhibitor drugs for neurodegenerative diseases: in vitro studies on antioxidant activity, prevention of lipid peroxide formation and monoamine oxidase inhibition. J Neurochem. 2005; 95, 6878.
70. Kwan, SW, Bergeron, JM, Abell, CW. Molecular properties of monoamine oxidases A and B. Psychopharmacology (Berl). 1992; 106(Suppl), S1S5.
71. Cobb, CA, Cole, MP. Oxidative and nitrative stress in neurodegeneration. Neurobiol Dis. 2015; 84, 421.
72. Pratico, D, Uryu, K, Leight, S, Trojanoswki, JQ, Lee, VM. Increased lipid peroxidation precedes amyloid plaque formation in an animal model of Alzheimer amyloidosis. J Neurosci. 2001; 21, 41834187.
73. Reed, TT, Pierce, WM, Markesbery, WR, Butterfield, DA. Proteomic identification of HNE-bound proteins in early Alzheimer disease: insights into the role of lipid peroxidation in the progression of AD. Brain Res. 2009; 1274, 6676.
74. Bubber, P, Haroutunian, V, Fisch, G, Blass, JP, Gibson, GE. Mitochondrial abnormalities in Alzheimer brain: mechanistic implications. Ann Neurol. 2005; 57, 695703.
75. Chen, X, Stern, D, Yan, SD. Mitochondrial dysfunction and Alzheimer’s disease. Curr Alzheimer Res. 2006; 3, 515520.
76. Damiano, M, Galvan, L, Deglon, N, Brouillet, E. Mitochondria in Huntington’s disease. Biochim Biophys Acta. 2010; 1802, 5261.
77. Nasr, P, Gursahani, HI, Pang, Z, et al. Influence of cytosolic and mitochondrial Ca2+, ATP, mitochondrial membrane potential, and calpain activity on the mechanism of neuron death induced by 3-nitropropionic acid. Neurochem Int. 2003; 43, 8999.
78. Luo, Y, Hoffer, A, Hoffer, B, Qi, X. Mitochondria: a therapeutic target for Parkinson’s disease? Int J Mol Sci. 2015; 16, 2070420730.
79. Abdin, AA, Sarhan, NI. Intervention of mitochondrial dysfunction-oxidative stress-dependent apoptosis as a possible neuroprotective mechanism of alpha-lipoic acid against rotenone-induced parkinsonism and L-dopa toxicity. Neurosci Res. 2011; 71, 387395.
80. Seet, RC, Lee, CY, Lim, EC, et al. Oxidative damage in Parkinson disease: measurement using accurate biomarkers. Free Radic Biol Med. 2010; 48, 560566.
81. Dutta, R, McDonough, J, Yin, X, et al. Mitochondrial dysfunction as a cause of axonal degeneration in multiple sclerosis patients. Ann Neurol. 2006; 59, 478489.
82. Schapira, AH. Complex I: inhibitors, inhibition and neurodegeneration. Exp Neurol. 2010; 224, 331335.
83. Broadwater, L, Pandit, A, Clements, R, et al. Analysis of the mitochondrial proteome in multiple sclerosis cortex. Biochim Biophys Acta. 2011; 1812, 630641.
84. Sarti, P, Giuffre, A, Barone, MC, et al. Nitric oxide and cytochrome oxidase: reaction mechanisms from the enzyme to the cell. Free Radic Biol Med. 2003; 34, 509520.
85. Pollari, E, Goldsteins, G, Bart, G, Koistinaho, J, Giniatullin, R. The role of oxidative stress in degeneration of the neuromuscular junction in amyotrophic lateral sclerosis. Front Cell Neurosci. 2014; 8, 131.
86. Robberecht, W, Philips, T. The changing scene of amyotrophic lateral sclerosis. Nat Rev Neurosci. 2013; 14, 248264.
87. Beal, MF, Ferrante, RJ, Browne, SE, et al. Increased 3-nitrotyrosine in both sporadic and familial amyotrophic lateral sclerosis. Ann Neurol. 1997; 42, 644654.
88. Estevez, AG, Crow, JP, Sampson, JB, et al. Induction of nitric oxide-dependent apoptosis in motor neurons by zinc-deficient superoxide dismutase. Science. 1999; 286, 24982500.
89. Harraz, MM, Marden, JJ, Zhou, W, et al. SOD1 mutations disrupt redox-sensitive Rac regulation of NADPH oxidase in a familial ALS model. J Clin Invest. 2008; 118, 659670.
90. Paravicini, TM, Touyz, RM. Redox signaling in hypertension. Cardiovasc Res. 2006; 71, 247258.
91. Chan, SH, Chan, JY. Brain stem NOS and ROS in neural mechanisms of hypertension. Antioxid Redox Signal. 2013; 20, 146163.
92. Hirooka, Y, Kishi, T, Sakai, K, Takeshita, A, Sunagawa, K. Imbalance of central nitric oxide and reactive oxygen species in the regulation of sympathetic activity and neural mechanisms of hypertension. Am J Physiol Regul Integr Comp Physiol. 2011; 300, R818R826.
93. Chan, SH, Tai, MH, Li, CY, Chan, JY. Reduction in molecular synthesis or enzyme activity of superoxide dismutases and catalase contributes to oxidative stress and neurogenic hypertension in spontaneously hypertensive rats. Free Radic Biol Med. 2006; 40, 20282039.
94. Chan, SH, Wu, KL, Chang, AY, Tai, MH, Chan, JY. Oxidative impairment of mitochondrial electron transport chain complexes in rostral ventrolateral medulla contributes to neurogenic hypertension. Hypertension. 2009; 53, 217227.
95. Chan, SH, Wu, CA, Wu, KL, et al. Transcriptional upregulation of mitochondrial uncoupling protein 2 protects against oxidative stress-associated neurogenic hypertension. Circ Res. 2009; 105, 886896.
96. Chan, SH, Chan, JY. Angiotensin-generated reactive oxygen species in brain and pathogenesis of cardiovascular diseases. Antioxid Redox Signal. 2013; 19, 10741084.
97. Nozoe, M, Hirooka, Y, Koga, Y, et al. Inhibition of Rac1-derived reactive oxygen species in nucleus tractus solitarius decreases blood pressure and heart rate in stroke-prone spontaneously hypertensive rats. Hypertension. 2007; 50, 6268.
98. Godfrey, KM, Gluckman, PD, Hanson, MA. Developmental origins of metabolic disease: life course and intergenerational perspectives. Trends Endocrinol Metab. 2010; 21, 199205.
99. Lucas, A, Fewtrell, MS, Cole, TJ. Fetal origins of adult disease-the hypothesis revisited. BMJ. 1999; 319, 245249.
100. Colombo, J. The critical period concept: research, methodology, and theoretical issues. Psychol Bull. 1982; 91, 260275.
101. Hales, CN, Barker, DJ, Clark, PM, et al. Fetal and infant growth and impaired glucose tolerance at age 64. BMJ. 1991; 303, 10191022.
102. Pigliucci, M. Developmental phenotypic plasticity: where internal programming meets the external environment. Curr Opin Plant Biol. 1998; 1, 8791.
103. Khan, I, Dekou, V, Hanson, M, Poston, L, Taylor, P. Predictive adaptive responses to maternal high-fat diet prevent endothelial dysfunction but not hypertension in adult rat offspring. Circulation. 2004; 110, 10971102.
104. Hanson, M, Gluckman, P. Endothelial dysfunction and cardiovascular disease: the role of predictive adaptive responses. Heart. 2005; 91, 864866.
105. Nettle, D, Frankenhuis, WE, Rickard, IJ. The evolution of predictive adaptive responses in human life history. Proc Biol Sci. 2013; 280, 20131343.
106. Wells, JC. The thrifty phenotype hypothesis: thrifty offspring or thrifty mother? J Theor Biol. 2003; 221, 143161.
107. Wells, JC. Flaws in the theory of predictive adaptive responses. Trends Endocrinol Metab. 2007; 18, 331337.
108. Wells, JC. The thrifty phenotype: an adaptation in growth or metabolism? Am J Hum Biol. 2011; 23, 6575.
109. Bale, TL. Epigenetic and transgenerational reprogramming of brain development. Nat Rev Neurosci. 2015; 16, 332344.
110. Martin-Gronert, MS, Ozanne, SE. Mechanisms underlying the developmental origins of disease. Rev Endocr Metab Disord. 2012; 13, 8592.
111. Martinez, SR, Gay, MS, Zhang, L. Epigenetic mechanisms in heart development and disease. Drug Discov Today. 2015; 20, 799811.
112. Ozanne, SE, Constancia, M. Mechanisms of disease: the developmental origins of disease and the role of the epigenotype. Nat Clin Pract Endocrinol Metab. 2007; 3, 539546.
113. Luo, ZC, Fraser, WD, Julien, P, et al. Tracing the origins of ‘fetal origins’ of adult diseases: programming by oxidative stress? Med Hypotheses. 2006; 66, 3844.
114. Mitchell, M, Schulz, SL, Armstrong, DT, Lane, M. Metabolic and mitochondrial dysfunction in early mouse embryos following maternal dietary protein intervention. Biol Reprod. 2009; 80, 622630.
115. Theys, N, Clippe, A, Bouckenooghe, T, Reusens, B, Remacle, C. Early low protein diet aggravates unbalance between antioxidant enzymes leading to islet dysfunction. PLoS One. 2009; 4, e6110.
116. Tarry-Adkins, JL, Chen, JH, Jones, RH, Smith, NH, Ozanne, SE. Poor maternal nutrition leads to alterations in oxidative stress, antioxidant defense capacity, and markers of fibrosis in rat islets: potential underlying mechanisms for development of the diabetic phenotype in later life. FASEB J. 2010; 24, 27622771.
117. Tarry-Adkins, JL, Martin-Gronert, MS, Fernandez-Twinn, DS, 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, 379390.
118. McGaughy, JA, Amaral, AC, Rushmore, RJ, et al. Prenatal malnutrition leads to deficits in attentional set shifting and decreases metabolic activity in prefrontal subregions that control executive function. Dev Neurosci. 2014; 36, 532541.
119. Duran, P, Galler, JR, Cintra, L, Tonkiss, J. Prenatal malnutrition and sleep states in adult rats: effects of restraint stress. Physiol Behav. 2006; 89, 156163.
120. Faa, G, Marcialis, MA, Ravarino, A, et al. Fetal programming of the human brain: is there a link with insurgence of neurodegenerative disorders in adulthood? Curr Med Chem. 2014; 21, 38543876.
121. Airey, CJ, Smith, PJ, Restall, K, et al. Maternal undernutrition affects neurogenesis in the foetal mouse brain. Int J Dev Neurosci. 2015; 47(Pt A), 72.
122. Field, ME, Anthony, RV, Engle, TE, et al. Duration of maternal undernutrition differentially alters fetal growth and hormone concentrations. Domest Anim Endocrinol. 2015; 51, 17.
123. Partadiredja, G, Worrall, S, Bedi, KS. Early life undernutrition alters the level of reduced glutathione but not the activity levels of reactive oxygen species enzymes or lipid peroxidation in the mouse forebrain. Brain Res. 2009; 1285, 2229.
124. Partadiredja, G, Worrall, S, Simpson, R, Bedi, KS. Pre-weaning undernutrition alters the expression levels of reactive oxygen species enzymes but not their activity levels or lipid peroxidation in the rat brain. Brain Res. 2008; 1222, 6978.
125. Franco, MC, Akamine, EH, Reboucas, N, et al. Long-term effects of intrauterine malnutrition on vascular function in female offspring: implications of oxidative stress. Life Sci. 2007; 80, 709715.
126. Franco Mdo, C, Dantas, AP, Akamine, EH, et al. Enhanced oxidative stress as a potential mechanism underlying the programming of hypertension in utero. J Cardiovasc Pharmacol. 2002; 40, 501509.
127. Gupta, P, Narang, M, Banerjee, BD, Basu, S. Oxidative stress in term small for gestational age neonates born to undernourished mothers: a case control study. BMC Pediatr. 2004; 4, 14.
128. Gveric-Ahmetasevic, S, Sunjic, SB, Skala, H, et al. Oxidative stress in small-for-gestational age (SGA) term newborns and their mothers. Free Radic Res. 2009; 43, 376384.
129. Tonkiss, J, Galler, J, Morgane, PJ, Bronzino, JD, Austin-LaFrance, RJ. Prenatal protein malnutrition and postnatal brain function. Ann N Y Acad Sci. 1993; 678, 215227.
130. Morgane, PJ, Austin-LaFrance, R, Bronzino, J, et al. Prenatal malnutrition and development of the brain. Neurosci Biobehav Rev. 1993; 17, 91128.
131. Morgane, PJ, Mokler, DJ, Galler, JR. Effects of prenatal protein malnutrition on the hippocampal formation. Neurosci Biobehav Rev. 2002; 26, 471483.
132. Al-Gubory, KH, Fowler, PA, Garrel, C. The roles of cellular reactive oxygen species, oxidative stress and antioxidants in pregnancy outcomes. Int J Biochem Cell Biol. 2010; 42, 16341650.
133. Bonatto, F, Polydoro, M, Andrades, ME, et al. Effect of protein malnutrition on redox state of the hippocampus of rat. Brain Res. 2005; 1042, 1722.
134. Halliwell, B. Free radicals, reactive oxygen species and human disease: a critical evaluation with special reference to atherosclerosis. Br J Exp Pathol. 1989; 70, 737757.
135. Jackson, JH, Schraufstatter, IU, Hyslop, PA, et al. Role of hydroxyl radical in DNA damage. Transactions of the Association of American Physicians. 1987; 100, 147157.
136. Gutteridge, JM, Wilkins, S. Copper salt-dependent hydroxyl radical formation. Damage to proteins acting as antioxidants. Biochim Biophys Acta. 1983; 759, 3841.
137. Bonatto, F, Polydoro, M, Andrades, ME, et al. Effects of maternal protein malnutrition on oxidative markers in the young rat cortex and cerebellum. Neurosci Lett. 2006; 406, 281284.
138. Alvarez, B, Radi, R. Peroxynitrite reactivity with amino acids and proteins. Amino Acids. 2003; 25, 295311.
139. Feoli, AM, Siqueira, IR, Almeida, L, et al. Effects of protein malnutrition on oxidative status in rat brain. Nutrition. 2006; 22, 160165.
140. Voog, L, Eriksson, T. Toluene-induced decrease in rat plasma concentrations of tyrosine and tryptophan. Acta Pharmacol Toxicol. 1984; 54, 151153.
141. Tatli, M, Guzel, A, Kizil, G, et al. 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, 2130.
142. Ferreira, DJ, Liu, Y, Fernandes, MP, Lagranha, CJ. Perinatal low-protein diet alters brainstem antioxidant metabolism in adult offspring. Nutr Neurosci. 2015; doi:10.1179/1476830515Y.0000000030, in press.
143. Cardoso, LM, Colombari, DS, Menani, JV, et al. Cardiovascular responses to hydrogen peroxide into the nucleus tractus solitarius. Am J Physiol Regul Integr Comp Physiol. 2009; 297, R462R469.
144. Chan, SH, Chan, JY. Brain stem oxidative stress and its associated signaling in the regulation of sympathetic vasomotor tone. J Appl Physiol (1985). 2012; 113, 19211928.
145. Muzzo, S, Gregory, T, Gardner, LI. Oxygen consumption by brain mitochondria of rats malnourished in utero. J Nutr. 1973; 103, 314317.
146. 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, 14631480.
147. Mokler, DJ, Galler, JR, Morgane, PJ. Modulation of 5-HT release in the hippocampus of 30-day-old rats exposed in utero to protein malnutrition. Brain Res Dev Brain Res. 2003; 142, 203208.
148. Olorunsogo, OO. Changes in brain mitochondrial bioenergetics in protein-deficient rats. Br J Exp Pathol. 1989; 70, 607619.

Keywords

Related content

Powered by UNSILO

Protein undernutrition during development and oxidative impairment in the central nervous system (CNS): potential factors in the occurrence of metabolic syndrome and CNS disease

  • D. J. S. Ferreira (a1), D. F. Sellitti (a2) and C. J. Lagranha (a1) (a3)

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed.