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Nutritional Neuroscience
An International Journal on Nutrition, Diet and Nervous System
Volume 22, 2019 - Issue 11
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Articles

Mitochondrial dysfunction: maternal protein restriction as a trigger of reactive species overproduction and brainstem energy failure in male offspring brainstem

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References

  • Nunnari J, Suomalainen A. Mitochondria: in sickness and in health. Cell 2012;148(6):1145–59.
  • Chance B, Williams GR, Holmes WF, Higgins J. Respiratory enzymes in oxidative phosphorylation. V. A mechanism for oxidative phosphorylation. J Biol Chem 1955;217(1):439–51.
  • Brand MD. The sites and topology of mitochondrial superoxide production. Exp Gerontol 2010;45(7–8):466–72.
  • Halliwell B. Free radicals and antioxidants: updating a personal view. Nutr Rev 2012;70(5):257–65.
  • Halliwell B. Oxidative stress and neurodegeneration: where are we now? J Neurochem 2006;97(6):1634–58.
  • Chen X, Stern D, Yan SD. Mitochondrial dysfunction and Alzheimer’s disease. Curr Alzheimer Res 2006;3(5):515–20.
  • Luo Y, Hoffer A, Hoffer B, Qi X. Mitochondria: a therapeutic target for Parkinson’s disease? Int J Mol Sci 2015;16(9):20704–30.
  • Damiano M, Galvan L, Deglon N, Brouillet E. Mitochondria in Huntington’s disease. Biochim Biophys Acta 2010;1802(1):52–61.
  • Broadwater L, Pandit A, Clements R, Azzam S, Vadnal J, Sulak M, et al. Analysis of the mitochondrial proteome in multiple sclerosis cortex. Biochim Biophys Acta 2011;1812(5):630–41.
  • Lopez-Campistrous A, Hao L, Xiang W, Ton D, Semchuk P, Sander J, et al. Mitochondrial dysfunction in the hypertensive rat brain: respiratory complexes exhibit assembly defects in hypertension. Hypertension 2008;51(2):412–19.
  • Chan SH, Wu CA, Wu KL, Ho YH, Chang AY, Chan JY. Transcriptional upregulation of mitochondrial uncoupling protein 2 protects against oxidative stress-associated neurogenic hypertension. Circ Res 2009;105(9):886–96.
  • Dampney RA, Coleman MJ, Fontes MA, Hirooka Y, Horiuchi J, Li YW, et al. Central mechanisms underlying short- and long-term regulation of the cardiovascular system. Clin Exp Pharmacol Physiol 2002;29(4):261–8.
  • Guyenet PG. The sympathetic control of blood pressure. Nat Rev Neurosci 2006;7(5):335–46.
  • de Brito Alves JL, Nogueira VO, de Oliveira GB, da Silva GS, Wanderley AG, Leandro CG, et al. Short- and long-term effects of a maternal low-protein diet on ventilation, O(2)/CO(2) chemoreception and arterial blood pressure in male rat offspring. Br J Nutr 2014;111(4):606–15.
  • Ferreira DJ, Liu Y, Fernandes MP, Lagranha CJ. Perinatal low-protein diet alters brainstem antioxidant metabolism in adult offspring. Nutr Neurosci 2016;19(8):369–75.
  • de Brito Alves JL, de Oliveira JM, Ferreira DJ, de Barros MA, Nogueira VO, Alves DS, et al. Maternal protein restriction induced-hypertension is associated to oxidative disruption at transcriptional and functional levels in the medulla oblongata. Clin Exp Pharmacol Physiol 2016;43(12):1177–84.
  • Reeves PG, Nielsen FH, Fahey GC, Jr. AIN-93 purified diets for laboratory rodents: final report of the American institute of nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr 1993;123(11):1939–51.
  • Ferreira DJ, da Silva Pedroza AA, Braz GR, da Silva-Filho RC, Lima TA, Fernandes MP, et al. Mitochondrial bioenergetics and oxidative status disruption in brainstem of weaned rats: immediate response to maternal protein restriction. Brain Res 2016;1642:553–61.
  • van der Toorn M, Kauffman HF, van der Deen M, Slebos DJ, Koeter GH, Gans RO, et al. Cyclosporin A-induced oxidative stress is not the consequence of an increase in mitochondrial membrane potential. FEBS J 2007;274(12):3003–12.
  • Figueira TR, Melo DR, Vercesi AE, Castilho RF. Safranine as a fluorescent probe for the evaluation of mitochondrial membrane potential in isolated organelles and permeabilized cells. Methods Mol Biol 2012;810:103–17.
  • Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 1987;162(1):156–9.
  • Lagranha CJ, de Lima TM, Senna SM, Doi SQ, Curi R, Pithon-Curi TC. The effect of glutamine supplementation on the function of neutrophils from exercised rats. Cell Biochem Funct 2005;23(2):101–7.
  • Perez S, Royo LJ, Astudillo A, Escudero D, Alvarez F, Rodriguez A, et al. Identifying the most suitable endogenous control for determining gene expression in hearts from organ donors. BMC Mol Biol 2007;8:114.
  • Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976;72:248–54.
  • Le Page C, Noirez P, Courty J, Riou B, Swynghedauw B, Besse S. Exercise training improves functional post-ischemic recovery in senescent heart. Exp Gerontol 2009;44(3):177–82.
  • Boveris A, Erecinska M, Wagner M. Reduction kinetics of cytochromes b. Biochim Biophys Acta 1972;256(2):223–42.
  • Buege JA, Aust SD. Microsomal lipid peroxidation. Methods Enzymol 1978;52:302–10.
  • Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR. Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Anal Biochem 1982;126(1):131–8.
  • Misra HP, Fridovich I. The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 1972;247(10):3170–5.
  • Aebi H. Catalase in vitro. Methods Enzymol 1984;105:121–6.
  • Paglia DE, Valentine WN. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 1967;70(1):158–69.
  • Habig WH, Pabst MJ, Jakoby WB. Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 1974;249(22):7130–9.
  • Hissin PJ, Hilf R. A fluorometric method for determination of oxidized and reduced glutathione in tissues. Anal Biochem 1976;74(1):214–26.
  • da Silva AI, Braz GR, Pedroza AA, Nascimento L, Freitas CM, Ferreira DJ, et al. Fluoxetine induces lean phenotype in rat by increasing the brown/white adipose tissue ratio and UCP1 expression. J Bioenerg Biomembr 2015;47(4):309–18.
  • Brand MD, Nicholls DG. Assessing mitochondrial dysfunction in cells. Biochem J 2011;435(2):297–312.
  • Chance B, Williams GR. Respiratory enzymes in oxidative phosphorylation. I. Kinetics of oxygen utilization. J Biol Chem 1955;217(1):383–93.
  • Nicholls DG, Bernson VS. Inter-relationships between proton electrochemical gradient, adenine-nucleotide phosphorylation potential and respiration, during substrate-level and oxidative phosphorylation by mitochondria from brown adipose tissue of cold-adapted Guinea-pigs. Eur J Biochem 1977;75(2):601–12.
  • Nicholls DG. The effective proton conductance of the inner membrane of mitochondria from brown adipose tissue. Dependency on proton electrochemical potential gradient. Eur J Biochem 1977;77(2):349–56.
  • Azzu V, Brand MD. The on-off switches of the mitochondrial uncoupling proteins. Trends Biochem Sci 2010;35(5):298–307.
  • Mailloux RJ, Harper ME. Uncoupling proteins and the control of mitochondrial reactive oxygen species production. Free Radic Biol Med 2011;51(6):1106–15.
  • 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(8):2762–71.
  • 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(1):379–90.
  • Murphy MP. How mitochondria produce reactive oxygen species. Biochem J 2009;417(1):1–13.
  • Campbell GR, Worrall JT, Mahad DJ. The central role of mitochondria in axonal degeneration in multiple sclerosis. Mult Scler 2014;20(14):1806–13.
  • Tsai CY, Su CH, Chan JY, Chan SH. Nitrosative stress-induced disruption of baroreflex neural circuits in a Rat model of hepatic encephalopathy: a DTI study. Scientific Reports 2017;7:40111.
  • Guggilam A, Cardinale JP, Mariappan N, Sriramula S, Haque M, Francis J. Central TNF inhibition results in attenuated neurohumoral excitation in heart failure: a role for superoxide and nitric oxide. Basic Res Cardiol 2011;106(2):273–86.
  • Kozlov AV, Bahrami S, Redl H, Szabo C. Alterations in nitric oxide homeostasis during traumatic brain injury. Biochim Biophys Acta 2017;1863(10 pt B):2627–32.
  • Kung LC, Chan SH, Wu KL, Ou CC, Tai MH, Chan JY. Mitochondrial respiratory enzyme complexes in rostral ventrolateral medulla as cellular targets of nitric oxide and superoxide interaction in the antagonism of antihypertensive action of eNOS transgene. Mol Pharmacol 2008;74(5):1319–32.
  • Chan SH, Chan JY. Brain stem NOS and ROS in neural mechanisms of hypertension. Antioxid Redox Signal 2014;20(1):146–63.
  • Kishi T, Hirooka Y, Kimura Y, Ito K, Shimokawa H, Takeshita A. Increased reactive oxygen species in rostral ventrolateral medulla contribute to neural mechanisms of hypertension in stroke-prone spontaneously hypertensive rats. Circulation 2004;109(19):2357–62.
  • Alvarez B, Radi R. Peroxynitrite reactivity with amino acids and proteins. Amino Acids 2003;25(3–4):295–311.
  • Murphy MP, Echtay KS, Blaikie FH, Asin-Cayuela J, Cocheme HM, Green K, et al. Superoxide activates uncoupling proteins by generating carbon-centered radicals and initiating lipid peroxidation: studies using a mitochondria-targeted spin trap derived from alpha-phenyl-N-tert-butylnitrone. J Biol Chem 2003;278(49):48534–45.
  • Azzu V, Parker N, Brand MD. High membrane potential promotes alkenal-induced mitochondrial uncoupling and influences adenine nucleotide translocase conformation. Biochem J 2008;413(2):323–32.
  • Nimer F A, Strom M, Lindblom R, Aeinehband S, Bellander BM, Nyengaard JR, et al. Naturally occurring variation in the glutathione-S-transferase 4 gene determines neurodegeneration after traumatic brain injury. Antioxid Redox Signal 2013;18(7):784–94.
  • Shichiri M. The role of lipid peroxidation in neurological disorders. J Clin Biochem Nutr 2014;54(3):151–60.
  • Jewett M, Jimenez-Ferrer I, Swanberg M. Astrocytic expression of GSTA4 is associated to dopaminergic neuroprotection in a Rat 6-OHDA model of Parkinson’s disease. Brain Sci 2017;7(7):pii. E73.
  • Martin-Gronert MS, Ozanne SE. Mechanisms underlying the developmental origins of disease. Rev Endocr Metab Disord 2012;13(2):85–92.
  • Hirose M, Schilf P, Lange F, Mayer J, Reichart G, Maity P, et al. Uncoupling protein 2 protects mice from aging. Mitochondrion 2016;30:42–50.

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