Effect of a Ketogenic Diet on Oxidative Posttranslational Protein Modifications and Brain Homogenate Denaturation in the Kindling Model of Epilepsy in Mice.
Advanced oxidation protein products
Ketogenic diet
Kindling epilepsy model
Protein carbonylation
Journal
Neurochemical research
ISSN: 1573-6903
Titre abrégé: Neurochem Res
Pays: United States
ID NLM: 7613461
Informations de publication
Date de publication:
Jul 2022
Jul 2022
Historique:
received:
17
11
2021
accepted:
12
03
2022
revised:
10
03
2022
pubmed:
23
3
2022
medline:
25
6
2022
entrez:
22
3
2022
Statut:
ppublish
Résumé
This study focused on the ketogenic diet (KD) effects on oxidative posttranslational protein modification (PPM) as presumptive factors implicated in epileptogenesis. A 28-day of KD treatment was performed. The corneal kindling model of epileptogenesis was used. Four groups of adult male ICR mice (25-30 g) were randomized in standard rodent chow (SRC) group, KD-treatment group; SRC + kindling group; KD + kindling group (n = 10 each). Advanced oxidation protein products (AOPP) and protein carbonyl contents of brain homogenates together with differential scanning calorimetry (DSC) were evaluated. Two exothermic transitions (Exo1 and Exo2) were explored after deconvolution of the thermograms. Factor analysis was applied. The protective effect of KD in the kindling model was demonstrated with both decreased seizure score and increased seizure latency. KD significantly decreased glucose and increased ketone bodies (KB) in blood. Despite its antiseizure effect, the KD increased the AOPP level and the brain proteome's exothermic transitions, suggestive for qualitative modifications. The ratio of the two exothermic peaks (Exo2/Exo1) of the thermograms from the KD vs. SRC treated group differed more than twice (3.7 vs. 1.6). Kindling introduced the opposite effect, changing this ratio to 2.7 for the KD + kindling group. Kindling significantly increased glucose and KB in the blood whereas decreased the BW under the SRC treatment. Kindling decreased carbonyl proteins in the brain irrespectively of the diet. Further evaluations are needed to assess the nature of correspondence of calorimetric images of the brain homogenates with PPM.
Identifiants
pubmed: 35316463
doi: 10.1007/s11064-022-03579-z
pii: 10.1007/s11064-022-03579-z
doi:
Substances chimiques
Advanced Oxidation Protein Products
0
Glucose
IY9XDZ35W2
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1943-1955Subventions
Organisme : Bulgarian National Science Fund
ID : DN03/13/2016
Organisme : Bulgarian National Science Fund
ID : DN13/16/2017
Organisme : Medical University Sofia
ID : D-211/2018
Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Devinsky O, Vezzani A, O’Brien T, Jette N, Scheffer IE, de Curtis M, Perucca P (2018) Epilepsy. Nat Rev Dis Primers 4:18024. https://doi.org/10.1038/nrdp.2018.24
doi: 10.1038/nrdp.2018.24
pubmed: 29722352
Granata T, Marchi N, Carlton E, Ghosh C, Gonzalez-Martinez J, Alexopoulos AV, Janigro D (2009) Management of the patient with medically refractory epilepsy. Expert Rev Neurother 9(12):1791–1802. https://doi.org/10.1586/ern.09.114
doi: 10.1586/ern.09.114
pubmed: 19951138
pmcid: 3761964
Singh T, Joshi S, Williamson JM, Kapur J (2020) Neocortical injury-induced status epilepticus. Epilepsia 61(12):2811–2824. https://doi.org/10.1111/epi.16715
doi: 10.1111/epi.16715
pubmed: 33063874
pmcid: 8764937
Wu HY, Lynch DR (2006) Calpain and synaptic function. Mol Neurobiol 33(3):215–236. https://doi.org/10.1385/MN:33:3:215
doi: 10.1385/MN:33:3:215
pubmed: 16954597
Gass P, Kiessling M, Bading H (1993) Regionally selective stimulation of mitogen activated protein (MAP) kinase tyrosine phosphorylation after generalized seizures in the rat brain. Neurosci Lett 162(1–2):39–42. https://doi.org/10.1016/0304-3940(93)90554-x
doi: 10.1016/0304-3940(93)90554-x
pubmed: 7510055
Sánchez RG, Parrish RR, Rich M, Webb WM, Lockhart RM, Nakao K, Ianov L, Buckingham SC, Broadwater DR, Jenkins A, de Lanerolle NC, Cunningham M, Eid T, Riley K, Lubin FD (2019) Human and rodent temporal lobe epilepsy is characterized by changes in O-GlcNAc homeostasis that can be reversed to dampen epileptiform activity. Neurobiol Dis 124:531–543. https://doi.org/10.1016/j.nbd.2019.01.001
doi: 10.1016/j.nbd.2019.01.001
pubmed: 30625365
pmcid: 6379093
Wu H, Chen X, Cheng J, Qi Y (2016) SUMOylation and potassium channels: links to epilepsy and sudden death. Adv Protein Chem Struct Biol 103:295–321. https://doi.org/10.1016/bs.apcsb.2015.11.009
doi: 10.1016/bs.apcsb.2015.11.009
pubmed: 26920693
Laedermann CJ, Decosterd I, Abriel H (2014) Ubiquitylation of voltage-gated sodium channels. In: Ruben P (ed) Voltage gated sodium channels. Handbook of experimental pharmacology, vol 221. Springer, Berlin. https://doi.org/10.1007/978-3-642-41588-3_11
doi: 10.1007/978-3-642-41588-3_11
Furukawa A, Kakita A, Chiba Y, Kitaura H, Fujii Y, Fukuda M, Kameyama S, Shimada A (2020) Proteomic profile differentiating between mesial temporal lobe epilepsy with and without hippocampal sclerosis. Epilepsy Res 168:106502. https://doi.org/10.1016/j.eplepsyres.2020.106502
doi: 10.1016/j.eplepsyres.2020.106502
pubmed: 33197783
Grove RA, Madhavan D, Boone C, Braga CP, Papackova Z, Kyllo H, Samson K, Simeone K, Simeone T, Helikar T, Hanson CK, Adamec J (2020) Aberrant energy metabolism and redox balance in seizure onset zones of epileptic patients. J Proteomics 223:103812. https://doi.org/10.1016/j.jprot.2020.103812
doi: 10.1016/j.jprot.2020.103812
pubmed: 32418907
Hauck AK, Huang Y, Hertzel AV, Bernlohr DA (2019) Adipose oxidative stress and protein carbonylation. J Biol Chem 294:1083–1088. https://doi.org/10.1074/jbc.R118.003214
doi: 10.1074/jbc.R118.003214
pubmed: 30563836
Mazhar F, Malhi SM, Simjee SU (2017) Comparative studies on the effects of clinically used anticonvulsants on the oxidative stress biomarkers in the pentylenetetrazole-induced kindling model of epileptogenesis in mice. J Basic Clin Physiol Pharmacol 28:31–42. https://doi.org/10.1515/jbcpp-2016-0034
doi: 10.1515/jbcpp-2016-0034
pubmed: 27658141
Mantle D, Siddique S, Eddeb F, Mendelow AD (2001) Comparison of protein carbonyl and antioxidant levels in brain tissue from intracerebral haemorrhage and control cases. Clin Chim Acta Int J Clin Chem 312(1–2):185–190. https://doi.org/10.1016/s0009-8981(01)00623-4
doi: 10.1016/s0009-8981(01)00623-4
Lennicke C, Rahn J, Heimer N, Lichtenfels R, Wessjohann LA, Seliger B (2016) Redox proteomics: methods for the identification and enrichment of redox-modified proteins and their applications. Proteomics 16(2):197–213. https://doi.org/10.1002/pmic.201500268
doi: 10.1002/pmic.201500268
pubmed: 26508685
Oliveira MF, Geihs MA, França T, Moreira DC, Hermes-Lima M (2018) Is “Preparation for Oxidative Stress” a case of physiological conditioning hormesis? Front Physiol 9:945. https://doi.org/10.3389/fphys.2018.00945
doi: 10.3389/fphys.2018.00945
pubmed: 30116197
pmcid: 6082956
Borowicz-Reutt KK, Czuczwar SJ (2020) Role of oxidative stress in epileptogenesis and potential implications for therapy. Pharmacol Rep 72(5):1218–1226. https://doi.org/10.1007/s43440-020-00143-w
doi: 10.1007/s43440-020-00143-w
pubmed: 32865811
pmcid: 7550371
Walczyk T, Wick JY (2017) The ketogenic diet: making a comeback. Consult Pharm 32:388–396. https://doi.org/10.4140/TCP.n.2017.388
doi: 10.4140/TCP.n.2017.388
pubmed: 28701250
Rusek M, Pluta R, Ułamek-Kozioł M, Czuczwar SJ (2019) Ketogenic diet in Alzheimer’s disease. Int J Mol Sci 20(16):3892. https://doi.org/10.3390/ijms20163892
doi: 10.3390/ijms20163892
pmcid: 6720297
Phillips MCL, Murtagh DKJ, Gilbertson LJ, Asztely FJS, Lynch CDP (2018) Low-fat versus ketogenic diet in Parkinson’s disease: a pilot randomized controlled trial. Mov Disord 33(8):1306–1314. https://doi.org/10.1002/mds.27390
doi: 10.1002/mds.27390
pubmed: 30098269
pmcid: 6175383
Rieger J, Bähr O, Maurer GD, Hattingen E, Franz K, Brucker D, Walenta S, Kämmerer U, Coy JF, Weller M, Steinbach JP (2014) ERGO: a pilot study of ketogenic diet in recurrent glioblastoma. Int J Oncol 44:1843–1852. https://doi.org/10.3892/ijo.2014.2382
doi: 10.3892/ijo.2014.2382
pubmed: 24728273
pmcid: 4063533
Hutfles LJ, Wilkins HM, Koppel SJ, Weidling IW, Selfridge JE, Tan E, Thyfault JP, Slawson C, Fenton AW, Zhu H, Swerdlow RH (2017) A bioenergetics systems evaluation of ketogenic diet liver effects. Appl Physiol Nutr Metab 42(9):955–962. https://doi.org/10.1139/apnm-2017-0068
doi: 10.1139/apnm-2017-0068
pubmed: 28514599
pmcid: 5857360
Mehdikhani F, Ghahremani H, Nabati S, Tahmouri H, Sirati-Sabet M, Salami S (2019) Histone butyrylation/acetylation remains unchanged in triple negative breast cancer cells after a long term metabolic reprogramming. Asian Pac J Cancer Prev 20(12):3597–3601. https://doi.org/10.31557/APJCP.2019.20.12.3597
doi: 10.31557/APJCP.2019.20.12.3597
pubmed: 31870099
pmcid: 7173388
Taksande JB, Sonwane PP, Trivedi RV, Wadher KJ, Umekar MJ (2017) Formulation and pharmacodynamic investigations of lamotrigine microspheres in pentylenetetrazoleinduced seizures in mice. AJP 11(1):S215. https://doi.org/10.22377/ajp.v11i01.1111
doi: 10.22377/ajp.v11i01.1111
Shah M, Patel D (2019) Development of an oxcarbazepine solid dispersion using skimmed milk to improve the solubility and dissolution profile. IJPSDR. https://doi.org/10.25004/IJPSDR.2019.110509
doi: 10.25004/IJPSDR.2019.110509
Johnson CM (2013) Differential scanning calorimetry as a tool for protein folding and stability. Arch Biochem Biophys 531:100–109. https://doi.org/10.1016/j.abb.2012.09.008
doi: 10.1016/j.abb.2012.09.008
pubmed: 23022410
Tsvetkov PO, Tabouret E, Roman AY, Romain S, Bequet C, Ishimbaeva O, Honoré S, Figarella-Branger D, Chinot O, Devred F (2018) Differential scanning calorimetry of plasma in glioblastoma: toward a new prognostic/monitoring tool. Oncotarget 9:9391–9399. https://doi.org/10.18632/oncotarget.24317
doi: 10.18632/oncotarget.24317
pubmed: 29507697
pmcid: 5823627
Kendrick SK, Zheng Q, Garbett NC, Brock GN (2017) Application and interpretation of functional data analysis techniques to differential scanning calorimetry data from lupus patients. PLoS ONE 12:e0186232. https://doi.org/10.1371/journal.pone.0186232
doi: 10.1371/journal.pone.0186232
pubmed: 29121669
pmcid: 5679774
Escobedo G, Arjona-Román JL, Meléndez-Pérez R, Suárez-Álvarez K, Guzmán C, Aguirre-García J, Gutiérrez-Reyes G, Vivas O, Varela-Fascinetto G, Rodríguez-Romero A, Robles-Díaz G, Kershenobich D (2013) Liver exhibits thermal variations according to the stage of fibrosis progression: a novel use of modulated-differential scanning calorimetry for research in hepatology: thermal methodologies for assessing liver fibrosis. Hepatol Res 43:785–794. https://doi.org/10.1111/hepr.12026
doi: 10.1111/hepr.12026
pubmed: 23252661
Tenchov B, Abarova S, Koynova R, Traikov L, Dragomanova S, Tancheva L (2017) A new approach for investigating neurodegenerative disorders in mice based on DSC. J Therm Anal Calorim 127:483–486. https://doi.org/10.1007/s10973-01
doi: 10.1007/s10973-01
Tenchov B, Abarova S, Koynova R, Traikov L, Tancheva L (2017) Low-temperature exothermic transitions in brain proteome of mice, effect of scopolamine. Thermochim Acta 650:26–32. https://doi.org/10.1016/j.tca.2017.01.012
doi: 10.1016/j.tca.2017.01.012
Kazmi Z, Zeeshan S, Khan A, Malik S, Shehzad A, Seo EK, Khan S (2020) Antiepileptic activity of daidzin in PTZ-induced mice model by targeting oxidative stress and BDNF/VEGF signaling. NeuroToxicol. https://doi.org/10.1016/j.neuro.2020.05.005
doi: 10.1016/j.neuro.2020.05.005
PANACHE - Public Access to Neuroactive & Anticonvulsant CHemical Evaluations (PANAChE) database, NINDS, NIH, 2016. https://panache.ninds.nih.gov/Model2A.aspx . Accessed 22 Feb 2020
Jiang Y, Yang Y, Wang S, Ding Y, Guo Y, Zhang MM, Wen SQ, Ding MP (2012) Ketogenic diet protects against epileptogenesis as well as neuronal loss in amygdaloid-kindling seizures. Neurosci Lett 508(1):22–26. https://doi.org/10.1016/j.neulet.2011.12.002
doi: 10.1016/j.neulet.2011.12.002
pubmed: 22178860
Lusardi TA, Akula KK, Coffman SQ, Ruskin DN, Masino SA, Boison D (2015) Ketogenic diet prevents epileptogenesis and disease progression in adult mice and rats. Neuropharmacology 99:500–509. https://doi.org/10.1016/j.neuropharm.2015.08.007
doi: 10.1016/j.neuropharm.2015.08.007
pubmed: 26256422
pmcid: 4655189
Pinto A, Bonucci A, Maggi E, Corsi M, Businaro R (2018) Antioxidant and anti-inflammatory activity of ketogenic diet: new perspectives for neuroprotection in Alzheimer’s disease. Antioxidants 7(5):63. https://doi.org/10.3390/antiox7050063
doi: 10.3390/antiox7050063
pmcid: 5981249
Kephart WC, Mumford PW, Mao X, Romero MA, Hyatt HW, Zhang Y, Mobley CB, Quindry JC, Young KC, Beck DT, Martin JS, McCullough DJ, D’Agostino DP, Lowery RP, Wilson JM, Kavazis AN, Roberts MD (2017) The 1-week and 8-month effects of a ketogenic diet or ketone salt supplementation on multi-organ markers of oxidative stress and mitochondrial function in rats. Nutrients 9(9):1019. https://doi.org/10.3390/nu9091019
doi: 10.3390/nu9091019
pmcid: 5622779
Parry HA, Kephart WC, Mumford PW, Romero MA, Mobley CB, Zhang Y, Roberts MD, Kavazis AN (2018) Ketogenic diet increases mitochondria volume in the liver and skeletal muscle without altering oxidative stress markers in rats. Heliyon 4:e00975. https://doi.org/10.1016/j.heliyon.2018.e00975
doi: 10.1016/j.heliyon.2018.e00975
pubmed: 30533548
pmcid: 6260463
Milder JB, Liang LP, Patel M (2010) Acute oxidative stress and systemic Nrf2 activation by the ketogenic diet. Neurobiol Dis 40:238–244. https://doi.org/10.1016/j.nbd.2010.05.030
doi: 10.1016/j.nbd.2010.05.030
pubmed: 20594978
pmcid: 3102314
Gryszczyńska B, Formanowicz D, Budzyń M, Wanic-Kossowska M, Pawliczak E, Formanowicz P, Majewski W, Strzyżewski KW, Kasprzak MP, Iskra M (2017) Advanced oxidation protein products and carbonylated proteins as biomarkers of oxidative stress in selected atherosclerosis-mediated diseases. BioMed Res Intern. https://doi.org/10.1155/2017/4975264
doi: 10.1155/2017/4975264
Gryszczynska B, Formanowicz D, Budzyń M, Wanic-Kossowska M, Pawliczak E, Formanowicz P, Majewski W, Strzyżewski KW, Kasprzak MP, Iskra M (2017) Advanced oxidation protein products and carbonylated proteins as biomarkers of oxidative stress in selected atherosclerosis-mediated diseases. BioMed Res Intern. https://doi.org/10.1155/2017/4975264
doi: 10.1155/2017/4975264
Didonna A, Benetti F (2015) Post-translational modifications in neurodegeneration. AIMS Biophysics 3:27–49. https://doi.org/10.3934/biophy.2016.1.27
doi: 10.3934/biophy.2016.1.27
Lauritzen KH, Hasan-Olive MM, Regnell CE, Kleppa L, Scheibye-Knudsen M, Gjedde A, Klungland A, Bohr VA, Storm-Mathisen J, Bergersen LH (2016) A ketogenic diet accelerates neurodegeneration in mice with induced mitochondrial DNA toxicity in the forebrain. Neurobiol Aging 48:34–47. https://doi.org/10.1016/j.neurobiolaging.2016.08.005
doi: 10.1016/j.neurobiolaging.2016.08.005
pubmed: 27639119
pmcid: 5629920
Guo ZJ, Niu HX, Hou FF, Zhang L, Fu N, Nagai R, Lu X, Chen BH, Shan YX, Tian JW, Nagaraj RH, Xie D, Zhang X (2008) Advanced oxidation protein products activate vascular endothelial cells via a RAGE-mediated signaling pathway. Antioxid Redox Signal 10(10):1699–1712. https://doi.org/10.1089/ars.2007.1999
doi: 10.1089/ars.2007.1999
pubmed: 18576917
pmcid: 6464001
Gill P, Moghadam TT, Ranjbar B (2010) Differential scanning calorimetry techniques: applications in biology and nanoscience. J Biomol Tech 21(4):167–193
pubmed: 21119929
pmcid: 2977967
Mayengbam S, Ellegood J, Kesler M, Reimer RA, Shearer J, Murari K, Rho JM, Lerch JP, Cheng N (2021) A ketogenic diet affects brain volume and metabolome in juvenile mice. Neuroimage 244:118542. https://doi.org/10.1016/j.neuroimage.2021.118542
doi: 10.1016/j.neuroimage.2021.118542
pubmed: 34530134
Chwiej J, Skoczen A, Janeczko K, Kutorasinska J, Matusiak K, Figiel H, Dumas P, Sandt C, Setkowicz Z (2015) The biochemical changes in hippocampal formation occurring in normal and seizure-experiencing rats as a result of a ketogenic diet. Analyst 140(7):2190–2204. https://doi.org/10.1039/c4an01857e
doi: 10.1039/c4an01857e
pubmed: 25705743
Abarova S, Koynova R, Tancheva L, Tenchov B (2017) A novel DSC approach for evaluating protectant drugs efficacy against dementia. Biochim Biophys Acta Mol Basis Dis 1863:2934–2941. https://doi.org/10.1016/j.bbadis.2017.07.033
doi: 10.1016/j.bbadis.2017.07.033
pubmed: 28778589
Olson CA, Vuong HE, Yano JM, Liang QY, Nusbaum DJ, Hsiao EY (2018) The gut microbiota mediates the anti-seizure effects of the ketogenic diet. Cell 173:1728-1741.e13. https://doi.org/10.1016/j.cell.2018.04.027
doi: 10.1016/j.cell.2018.04.027
pubmed: 29804833
pmcid: 6003870
Castellano I, Merlino A (2012) γ-Glutamyltranspeptidases: sequence, structure, biochemical properties, and biotechnological applications. Cell Mol Life Sci 69(20):3381–3394. https://doi.org/10.1007/s00018-012-0988-3
doi: 10.1007/s00018-012-0988-3
pubmed: 22527720
Yudkoff M, Daikhin Y, Melø TM, Nissim I, Sonnewald U, Nissim I (2007) The ketogenic diet and brain metabolism of amino acids: relationship to the anticonvulsant effect. Annu Rev Nutr 27:415–430. https://doi.org/10.1146/annurev.nutr.27.061406.093722
doi: 10.1146/annurev.nutr.27.061406.093722
pubmed: 17444813
pmcid: 4237068
Van der Auwera I, Wera S, Van Leuven F, Henderson ST (2005) A ketogenic diet reduces amyloid beta 40 and 42 in a mouse model of Alzheimer’s disease. Nutr Metab 2:28. https://doi.org/10.1186/1743-7075-2-28
doi: 10.1186/1743-7075-2-28
Roberts MN, Wallace MA, Tomilov AA, Zhou Z, Marcotte GR, Tran D, Perez G, Gutierrez-Casado E, Koike S, Knotts TA, Imai DM, Griffey SM, Kim K, Hagopian K, McMackin MZ, Haj FG, Baar K, Cortopassi GA, Ramsey JJ, Lopez-Dominguez JA (2018) A ketogenic diet extends longevity and healthspan in adult mice. Cell Metab 27:1156. https://doi.org/10.1016/j.cmet.2018.04.005
doi: 10.1016/j.cmet.2018.04.005
pubmed: 29719228
Cooper MA, Menta BW, Perez-Sanchez C, Jack MM, Khan ZW, Ryals JM, Winter M, Wright DE (2018) A ketogenic diet reduces metabolic syndrome-induced allodynia and promotes peripheral nerve growth in mice. Exp Neurol 306:149–157. https://doi.org/10.1016/j.expneurol.2018.05.011
doi: 10.1016/j.expneurol.2018.05.011
pubmed: 29763602
pmcid: 5994385
Garbow JR, Doherty JM, Schugar RC, Travers S, Weber ML, Wentz AE, Ezenwajiaku N, Cotter DG, Brunt EM, Crawford PA (2011) Hepatic steatosis, inflammation, and ER stress in mice maintained long term on a very low-carbohydrate ketogenic diet. Am J Physiol Gastrointest Liver Physiol 300:G956–G967. https://doi.org/10.1152/ajpgi.00539.2010
doi: 10.1152/ajpgi.00539.2010
pubmed: 21454445
pmcid: 3119109
Ellenbroek JH, van Dijck L, Töns HA, Rabelink TJ, Carlotti F, Ballieux BE, de Koning EJ (2014) Long-term ketogenic diet causes glucose intolerance and reduced beta and alpha cell mass but no weight loss in mice. Am J Physiol Endocrinol Metab 306:E552–E558. https://doi.org/10.1152/ajpendo.00453.2013
doi: 10.1152/ajpendo.00453.2013
pubmed: 24398402
Martin-McGill KJ, Bresnahan R, Levy RG, Cooper PN (2020) Ketogenic diets for drug-resistant epilepsy. Cochrane Database Syst Rev 6(6):CD001903. https://doi.org/10.1002/14651858.CD001903.pub5
doi: 10.1002/14651858.CD001903.pub5
pubmed: 32588435
Mantis JG, Fritz CL, Marsh J, Heinrichs SC, Seyfried TN (2009) Improvement in motor and exploratory behavior in Rett syndrome mice with restricted ketogenic and standard diets. Epilepsy Behav 15(2):133–141. https://doi.org/10.1016/j.yebeh.2009.02.038
doi: 10.1016/j.yebeh.2009.02.038
pubmed: 19249385
Zhou W, Mukherjee P, Kiebish MA, Markis WT, Mantis JG, Seyfried TN (2007) The calorically restricted ketogenic diet, an effective alternative therapy for malignant brain cancer. Nutr Metab 4:5. https://doi.org/10.1186/1743-7075-4-5
doi: 10.1186/1743-7075-4-5
Koppel SJ, Swerdlow RH (2018) Neuroketotherapeutics: a modern review of century-old therapy. Neurochem Intl 117:114–125. https://doi.org/10.1016/j.neuint.2017.05.019
doi: 10.1016/j.neuint.2017.05.019
Wright E Jr, Scism-Bacon JL, Glass LC (2006) Oxidative stress in type 2 diabetes: the role of fasting and postprandial glycemia. Int J Clin Pract 60(3):308–314. https://doi.org/10.1111/j.1368-5031.2006.00825.x
doi: 10.1111/j.1368-5031.2006.00825.x
pubmed: 16494646
Cai Z, Yan L-J (2013) Protein oxidative modifications: beneficial roles in disease and health. J Biochem Pharmacol Res 1:15–26
pubmed: 23662248
pmcid: 3646577
Fedorova M, Bollineni RC, Hoffmann R (2014) Protein carbonylation as a major hallmark of oxidative damage: update of analytical strategies: protein carbonylation: an analytical update. Mass Spec Rev 33:79–97. https://doi.org/10.1002/mas.21381
doi: 10.1002/mas.21381
Suzuki Y (2019) Oxidant-mediated protein amino acid conversion. Antioxidants 8:50. https://doi.org/10.3390/antiox8020050
doi: 10.3390/antiox8020050
pmcid: 6406366
Wong CM, Bansal G, Marcocci L, Suzuki YJ (2012) Proposed role of primary protein carbonylation in cell signaling. Redox Rep 17:90–94. https://doi.org/10.1179/1351000212Y.0000000007
doi: 10.1179/1351000212Y.0000000007
pubmed: 22564352
Gilby KL, Sydserff S, Patey AM, Thorne V, St-Onge V, Jans J, McIntyre DC (2009) Postnatal epigenetic influences on seizure susceptibility in seizure-prone versus seizure-resistant rat strains. Behav Neurosci 123(2):337–346. https://doi.org/10.1037/a0014730
doi: 10.1037/a0014730
pubmed: 19331457
Michnik A, Drzazga Z (2010) Thermal denaturation of mixtures of human serum proteins: DSC study. J Therm Anal Calorim 101:513–518. https://doi.org/10.1007/s10973-010-0826-5
doi: 10.1007/s10973-010-0826-5
Zhou HX, Pang X (2018) Electrostatic interactions in protein structure, folding, binding, and condensation. Chem Rev 118(4):1691–1741. https://doi.org/10.1021/acs.chemrev.7b00305
doi: 10.1021/acs.chemrev.7b00305
pubmed: 29319301
pmcid: 5831536
Petrov D, Zagrovic B (2011) Microscopic analysis of protein oxidative damage: effect of carbonylation on structure, dynamics, and aggregability of villin headpiece. J Am Chem Soc 133:7016–7024. https://doi.org/10.1021/ja110577e
doi: 10.1021/ja110577e
pubmed: 21506564
pmcid: 3088313
Mobbs CV (2018) Glucose-induced transcriptional hysteresis: role in obesity, metabolic memory, diabetes, and aging. Front Endocrinol 9:232. https://doi.org/10.3389/fendo.2018.00232
doi: 10.3389/fendo.2018.00232
Miller VJ, Villamena FA, Volek JS (2018) Nutritional ketosis and mitohormesis: potential implications for mitochondrial function and human health. J Nutr Metab. https://doi.org/10.1155/2018/5157645
doi: 10.1155/2018/5157645
pubmed: 30305961
pmcid: 6165613