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Intracellular Redox State Alters NMDA Receptor Response during Aging through Ca2+/Calmodulin-Dependent Protein Kinase II
Open accessAbstract
The contribution of the NMDA receptors (NMDARs) to synaptic plasticity declines during aging, and the decline is thought to contribute to memory deficits. Here, we demonstrate that an age-related shift in intracellular redox state contributes to the decline in NMDAR responses through Ca 2+/calmodulin-dependent protein kinase II (CaMKII). The oxidizing agent xanthine/xanthine oxidase (X/XO) decreased the NMDAR-mediated synaptic responses at hippocampal CA3–CA1 synapses in slices from young (3–8 months) but not aged (20–25 months) rats. Conversely, the reducing agent dithiothreitol (DTT) selectively enhanced NMDAR response to a greater extent in aged hippocampal slices. The enhancement of NMDAR responses facilitated induction of long-term potentiation in aged but not young animals. The DTT-mediated growth in the NMDAR response was not observed for the AMPA receptor-mediated synaptic responses. A similar increase was observed by intracellular application of the membrane-impermeable reducing agent,l-glutathione (l-GSH), through the intracellular recording pipette, indicating that the increased NMDAR response was dependent on intracellular redox state. DTT enhancement of the NMDAR response was dependent on CaMKII activity and was blocked by the CaMKII inhibitor—myristoylated autocamtide-2-related inhibitory peptide (myr-AIP)—but not by inhibition of the activity of protein phosphatases—PP1 and calcineurin (CaN/PP2B) or protein kinase C. CaMKII activity assays established that DTT increased CaMKII activity in CA1 cytosolic extracts in aged but not in young animals. These findings indicate a link between oxidation of CaMKII during aging, a decline in NMDAR responses, and altered synaptic plasticity.
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“Critically, there is also a reciprocal relationship: NMDAR hypofunction itself leads to cortical oxidative stress and GSH defcits 73,74 .”
From Linking early-life NMDAR hypofunction and oxidative stress in schizophrenia pathogenesis (2016) · cites this paper as [74]
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Citations
Cites
A synaptic model of memory: long-term potentiation in the hippocampus
Bliss, T. V. P., & Collingridge, G. L. (1993) · Nature · doi:10.1038/361031a0 · Cited by 11,566 · cited 2×
“Introduction The NMDA receptor (NMDAR) is a major source of Ca 2 influx into the postsynaptic neuron during the induction of LTP at hippocampal CA3–CA1 synapses (Bliss and Collingridge, 1993).”
BackgroundThe molecular basis of CaMKII function in synaptic and behavioural memory
Lisman, J., Schulman, H., & Cline, H. (2002) · Nature Reviews Neuroscience · doi:10.1038/nrn753 · Cited by 1,860 · cited 3×
“The interaction of NMDARs with CaMKII has been proposed as a model of memory (Lisman et al., 2002) and recent work indicates that disruption of the interaction between CaMKII and NMDAR impairs the induction of LTP and spatial learning (Zhou et al., 2007).”
BackgroundThe essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory.
Tsien, J. Z., Huerta, P. T., & Tonegawa, S. (1996) · Cell · doi:10.1016/s0092-8674(00)81827-9 · Cited by 1,782 · cited 1×
“CA1 region-specific knock-out of the NR1 subunit of the NMDAR abolishes LTP, in addition to impairing spatial memory (Tsien et al., 1996).”
BackgroundGriendling, K. K., Sorescu, D., Lassegue, B. P., & Ushio‐Fukai, M. (2000) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.20.10.2175 · Cited by 955 · cited 2×
“thermore, the enzymatic activity of these kinases can be regulated by the reduction and oxidation of the cysteine residues located in their structure (Raynaud et al., 1997; Griendling et al., 2000; Knapp and Klann, 2000).”
BackgroundImpact of aging on hippocampal function: plasticity, network dynamics, and cognition
Rosenzweig, E. S., & Barnes, C. A. (2003) · Progress in Neurobiology · doi:10.1016/s0301-0082(02)00126-0 · Cited by 755 · cited 3×
“, 1997; Billard and Rouaud, 2007), suggesting that age-related LTP and memory deficits are due to a decrease in the NMDARmediated component of synaptic transmission (Foster, 1999, 2007; Rosenzweig and Barnes, 2003), also referred to here as “NMDAR hypofunction.”
BackgroundTokumitsu, H., Chijiwa, T., Hagiwara, M., Mizutani, A., Terasawa, M., & Hidaka, H. (1990) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)39565-1 · Cited by 624 · cited 2×
“Similarly, bath application of the CaMK inhibitor KN-62 (10 M, 45 min) (Tokumitsu et al., 1990), before and during the application of DTT, blocked (97.9 7.98%, n 5) the DTT-mediated increase in NMDAR-fEPSP in aged animals (Fig.”
MethodInfluentialRegulation of NMDA Receptors by an Associated Phosphatase-Kinase Signaling Complex
Westphal, R. S., Tavalin, S. J., Lin, J., Alto, N. M., Fraser, I. D. C., Langeberg, L. K., Sheng, M., & Scott, J. D. (1999) · Science · doi:10.1126/science.285.5424.93 · Cited by 495 · cited 1×
“CaMKII contributes to DTT-mediated enhancement of NMDAR responses in aged animals NMDAR function is controlled by several intracellular kinases (Ben-Ari et al., 1992; Westphal et al., 1999; Li et al., 2001).”
BackgroundRegulation of NMDA channel function by endogenous Ca2+-dependent phosphatase
Lieberman, D. N., & Mody, I. (1994) · Nature · doi:10.1038/369235a0 · Cited by 480 · cited 1×
“Furthermore, phosphatase activity decreases NMDAR function (Lieberman and Mody, 1994; Wang et al., 1994).”
Selective modulation of NMDA responses by reduction and oxidation
Aizenman, E., Lipton, S. A., & Loring, R. H. (1989) · Neuron · doi:10.1016/0896-6273(89)90310-3 · Cited by 453 · cited 2×
“The redox state of the extracellular cysteine residues of the NMDARs have been implicated in regulating the NMDAR function in cell cultures and neonatal animals (Aizenman et al., 1989, 1990; Bernard et al., 1997; Choi and Lipton, 2000; Choi et al., 2001).”
BackgroundCysteine regulation of protein function – as exemplified by NMDA-receptor modulation
Lipton, S. A., Choi, Y.-B., Takahashi, H., Zhang, D., Li, W., Godzik, A., & Bankston, L. A. (2002) · Trends in Neurosciences · doi:10.1016/s0166-2236(02)02245-2 · Cited by 375 · cited 2×
“…and in tissue from neonates suggests that redox state is an important determinant of NMDAR function (Aizenman et al., 1989, 1990; Bernard et al., 1997; Choi and Lipton, 2000; Choi et al., 2001), possibly through oxidation of extracellular cysteine residues on the NMDAR (Lipton et al., 2002).”
Background
Cited by
Sorted by citations
The effects of aging in the hippocampus and cognitive decline
Bettio, L. E. B., Rajendran, L., & Gil‐Mohapel, J. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.04.030 · Cited by 700
“Indeed, the maintenance of the intracellular redox state is crucial for appropriate NMDA receptor function at hippocampal synapses during LTP processes (Bodhinathan et al., 2010), and also for neurogenic function within the SGZ of the hippocampus (Huang et al., 2012a).”
Synaptic plasticity in depression: Molecular, cellular and functional correlates
Marsden, W. N. (2012) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2012.12.012 · Cited by 323
Linking early-life NMDAR hypofunction and oxidative stress in schizophrenia pathogenesis
Hardingham, G. E., & Do, K. Q. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2015.19 · Cited by 304
Beckhauser, T. F., Francis-Oliveira, J., & De Pasquale, R. (2016) · Journal of Experimental Neuroscience · doi:10.4137/jen.s39887 · Cited by 301
The origin of NMDA receptor hypofunction in schizophrenia
Nakazawa, K., & Sapkota, K. (2019) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2019.107426 · Cited by 294
“Modulation of intracellular redox state has also been shown to alter the NMDA responses at hippocampal synapses in the aged, but not young rats (Bodhinathan et al., 2010), which may be relevant for the study of age-dependent cognitive decline.”
BackgroundSteullet, P., Cabungcal, J. H., Monin, A., Dwir, D., O'Donnell, P., Cuenod, M., & Do, K. Q. (2016) · Schizophrenia Research · doi:10.1016/j.schres.2014.06.021 · Cited by 262
“, 2001) or by Ca/calmodulin-dependent protein kinase II (Bodhinathan et al., 2010).”
Bioassay‐guided Evaluation of Antioxidant and Antinociceptive Activities of Carvacrol
Guimarães, A. G., Oliveira, G. F., Seabra, M. S. D. M., Cavalcanti, S. C. H., Antoniolli, Â. R., Bonjardim, L. R., Silva, F. A., dos Santos, J. P. A., da Rocha, R. F., Moreira, J. C. F., et al. (2010) · Basic & Clinical Pharmacology & Toxicology · doi:10.1111/j.1742-7843.2010.00609.x · Cited by 225
Vitamin D cell signalling in health and disease
Berridge, M. J. (2015) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2015.01.008 · Cited by 215
Morgan, T. E., Davis, D. A., Iwata, N., Tanner, J. A., Snyder, D., Ning, Z., Kam, W. W.-Y., Hsu, Y., Winkler, J. W., Chen, J., et al. (2011) · Environmental Health Perspectives · doi:10.1289/ehp.1002973 · Cited by 204
“Glutamatergic NMDA receptors are sensitive to H2O2 (Bodhinathan et al. 2010; Yang et al. 2010).”
BackgroundKumar, A. (2011) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2011.00007 · Cited by 175
“Recently, our work demonstrated that the age-related decline in NMDA receptor-mediated synaptic responses is clearly related to the redox state associated with aging (Bodhinathan et al., 2010b).”
BackgroundInfluentialSelf-citationFoster, T. C. (2012) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2012.01.007 · Cited by 163
Self-citationAging, Synaptic Dysfunction, and Insulin-Like Growth Factor (IGF)-1
Deák, F., & Sonntag, W. E. (2012) · The Journals of Gerontology Series A · doi:10.1093/gerona/gls118 · Cited by 151
Insulin-like growth factor-1 in CNS and cerebrovascular aging
Sonntag, W. E., Deák, F., Ashpole, N. M., Tóth, P., Csiszár, A., Freeman, W. M., & Ungvari, Z. I. (2013) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2013.00027 · Cited by 139
Cuénod, M., Steullet, P., Cabungcal, J.-H., Dwir, D., Khadimallah, I., Klauser, P., Conus, P., & Kim, Q. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01374-w · Cited by 134
“On the other side, oxidative conditions negatively and reversibly modulate NMDAR activity via extracellular redox-sensitive sites located on GluN1-GuN2A receptors [134, 135] and inhibition of CaMKII activity [136].”
BackgroundNMDA Receptor Function During Senescence: Implication on Cognitive Performance
Kumar, A. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00473 · Cited by 130
“Results demonstrate that an age-related decrease in NMDA receptor function is related to oxidative stress and a post-synaptic shift in the intracellular redox environment (Bodhinathan et al., 2010a,b; Robillard et al., 2011; Haxaire et al., 2012; Lee et al., 2014).”
BackgroundResultInfluentialSelf-citationKumar, A., Rani, A., Tchigranova, O., Russell, W. L., & Foster, T. C. (2011) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2011.06.023 · Cited by 124
Self-citationRedox Signaling in Neurotransmission and Cognition During Aging
Kumar, A., Yegla, B., & Foster, T. C. (2017) · Antioxidants and Redox Signaling · doi:10.1089/ars.2017.7111 · Cited by 106
“Moreover, using cytosolic extracts, we observed that DTT increased CaMKII activity in an age-dependent manner (31) (Fig.”
BackgroundInfluentialSelf-citationPotential Roles of Redox Dysregulation in the Development of Schizophrenia
Perkins, D. O., Jeffries, C. D., & Do, K. Q. (2020) · Biological Psychiatry · doi:10.1016/j.biopsych.2020.03.016 · Cited by 103
“Intracellular redox state also impacts NMDAR function, with shifts towards oxidation resulting in hypofunction (79) (Figure 2).”
BackgroundReese, L. C., Laezza, F., Woltjer, R. L., & Taglialatela, G. (2011) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2011.07447.x · Cited by 103
“Recent evidence suggests that CaMKII signaling is dysregulated in aged hippocampus (Nyffeler et al. 2007; Bodhinathan et al. 2010), and the presence of Ab further intensifies conditions which impair synaptic plasticity; acute treatment with Ab oligomers has been shown to perturb CaMKII…”
BackgroundFoster, T. C., Kyritsopoulos, C., & Kumar, A. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.05.012 · Cited by 94
“Interestingly, AD patients xhibit a decrease in synaptic CaMKII activity and treatment with decreased CaMKII synaptic activity in mice [98].”
InfluentialSelf-citationLiu, D.-S., Pan, X.-D., Zhang, J., Shen, H., Collins, N. C., Cole, A. M., Koster, K. P., Ben Aissa, M., Dai, X.-M., Zhou, M., et al. (2015) · Molecular Neurodegeneration · doi:10.1186/s13024-015-0002-2 · Cited by 99
“As the NMDAR component of synaptic transmission has been shown to decline during aging [91,92], NMDAR activation may provide a mechanistic pathway for understanding apoE-related memory impairment.”
BackgroundGlutathione Restores the Mechanism of Synaptic Plasticity in Aged Mice to That of the Adult
Robillard, J. M., Gordon, G. R., Choi, H. B., Christie, B. R., & MacVicar, B. A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0020676 · Cited by 89
“with the recent observation that intracellular GSH supplementation enhances NMDAR currents [14], we confirmed that LTP could only be observed in whole-cell conditions in aged hippocampal neurons when GSH was added to the intrapipette solution (Figure S2, A and B).”
InfluentialHaxaire, C., Turpin, F. R., Potier, B., Kervern, M., Sinet, P., Barbanel, G., Mothet, J., Dutar, P., & Billard, J. (2012) · Aging Cell · doi:10.1111/j.1474-9726.2012.00792.x · Cited by 88
NO-dependent CaMKII activation during β-adrenergic stimulation of cardiac muscle
Gutierrez, D. A., Fernández-Tenorio, M., Ogrodnik, J., & Niggli, E. (2013) · Cardiovascular Research · doi:10.1093/cvr/cvt201 · Cited by 90
“To confirm that NO could activate CaMKII in the absence of elevated Ca, we used an in-vitro assay.(34) CaMKII activity was detected with an ELISA test and normalized to that observed in low Ca (< 10 nM; Ca, CaM and EGTA, Figure 4D).”
MethodBodhinathan, K., Kumar, A., & Foster, T. C. (2010) · Journal of Neurophysiology · doi:10.1152/jn.00577.2010 · Cited by 86
Self-citationBelrose, J. C., Xie, Y., Gierszewski, L. J., MacDonald, J. F., & Jackson, M. F. (2012) · Molecular Brain · doi:10.1186/1756-6606-5-11 · Cited by 86
“Of note, HEK293 cells do not express NMDARs nor voltage-gated Ca2+ channels.”
BackgroundFontaine, C. J., Patten, A. R., Sickmann, H. M., Helfer, J. L., & Christie, B. R. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.02.014 · Cited by 83
Lin, C., & Lane, H. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00093 · Cited by 85
“Age-associated shifts in intracellular redox state to a pro-oxidizing environment have been linked to reduced NMDAR activity via the redox regulation of calcium/calmodulin-dependent protein kinase type II (CaMKII), and can be rescued by intracellular glutathione (83).”
BackgroundEarly pathogenesis in the adult‐onset neurodegenerative disease amyotrophic lateral sclerosis
van Zundert, B., Izaurieta, P., Fritz, E., & Álvarez, F. J. (2012) · Journal of Cellular Biochemistry · doi:10.1002/jcb.24234 · Cited by 84
Linking Redox Regulation of NMDAR Synaptic Function to Cognitive Decline during Aging
Kumar, A., & Foster, T. C. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2176-13.2013 · Cited by 78
“Redox regulation of NMDARs contributes to age-related impairment of long-term potentiation (LTP; Bodhinathan et al., 2010a; Robillard et al., 2011), which also emerges during middle age in association with impaired cognition (Rex et al., 2005; Fouquet et al., 2011).”
BackgroundMethodInfluentialSelf-citationSartor, G. C., Malvezzi, A. M., Kumar, A., Andrade, N. S., Wiedner, H. J., Vilca, S. J., Janczura, K. J., Bagheri, A., Al‐Ali, H., Powell, S. K., et al. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.1604-18.2018 · Cited by 80
“Brains were removed and hippocampal slices prepared as described previously (Bodhinathan et al., 2010; Kumar, 2010; Kumar and Foster, 2013, 2014; Kumar et al., 2018).”
MethodSelf-citationHorowitz, M. P., Milanese, C., Maio, R. D., Hu, X., Montero, L. M., Sanders, L. H., Tapias, V., Sepe, S., van Cappellen, W. A., Burton, E. A., et al. (2011) · Antioxidants and Redox Signaling · doi:10.1089/ars.2010.3629 · Cited by 76
“The redox state of thiols exerts a profound effect on the physiology of neurons; for instance, it regulates fundamental processes such as synaptic plasticity (11) and controls the conductance of several ion channels involved in neuronal excitability (13, 24).”
BackgroundCalcium, Reactive Oxygen Species, and Synaptic Plasticity
Hidalgo, C., & Arias‐Cavieres, A. (2016) · Physiology · doi:10.1152/physiol.00038.2015 · Cited by 75
“The next LTP phase, which engages Ca2 -dependent activation of protein kinase C (PKC) and calcium-/calmodulindependent protein kinase II (CaMKII), requires local protein synthesis but not gene transcription (179).”
BackgroundInfluentialZhang, H., Liu, J., Sun, S., Pchitskaya, E. I., Александровна, П. Е., & Борисович, Б. И. (2015) · Journal of Alzheimer s Disease · doi:10.3233/jad-142427 · Cited by 73
“neurons [27–30] and impaired maintenance of L-LTP”
Memory in aged mice is rescued by enhanced expression of the GluN2B subunit of the NMDA receptor
Brim, B. C., Haskell, R. E., Awedikian, R., Ellinwood, N. M., Jin, L. E., Kumar, A., Foster, T. C., & Magnusson, K. R. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.10.026 · Cited by 73
Self-citationKaranikas, E., Daskalakis, N. P., & Agorastos, A. (2021) · Brain Sciences · doi:10.3390/brainsci11060723 · Cited by 78
“An intense intracellular Ca “overload”, consequent to increased energy demand, may trigger NOS activation, leading subsequently to excessive formation of NO and finally to OXS [71], and affects NMDA-R function possibly via the decline of Ca/calmodulin-dependent protein kinase II activity [72,73].”
BackgroundWang, Y., & Mattson, M. P. (2013) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2013.07.007 · Cited by 72
Kumar, A., & Foster, T. C. (2018) · Neurochemical Research · doi:10.1007/s11064-018-2634-4 · Cited by 74
Self-citationArias-Cavieres, A., Adasme, T., Sánchez, G., Muñoz, P., & Hidalgo, C. (2017) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2017.00111 · Cited by 70
“Of note, RyR channel inhibition or antioxidant agents significantly decrease the sustained Ca2+-dependent sAHP exhibited by aged hippocampal neurons (Bodhinathan et al., 2010b).”
BackgroundInfluentialArias‐Cavieres, A., Khuu, M. A., Nwakudu, C. U., Barnard, J. E., Dalgin, G., & Garcia, A. J. (2020) · eNeuro · doi:10.1523/eneuro.0024-20.2020 · Cited by 67
Cui, J., Li, Z., Zhuang, S., Qi, S., Li, L., Zhou, J., Zhang, W., & Zhao, Y. (2018) · Cell Stress and Chaperones · doi:10.1007/s12192-017-0841-6 · Cited by 65
Effect of peripheral cellular senescence on brain aging and cognitive decline
Budamagunta, V., Kumar, A., Rani, A., Bean, L. A., Manohar‐Sindhu, S., Yang, Y., Zhou, D., & Foster, T. C. (2023) · Aging Cell · doi:10.1111/acel.13817 · Cited by 68
“…weeks after the eighth cycle of senolytic treatment, rats were sacrificed and electrophysiological recordings were performed on hippocampal slices as described previously (Bodhinathan et al., 2010; Guidi, Kumar, & Foster, 2015; Kumar, 2015; Kumar et al., 2009, 2018, 2019; Kumar & Foster, 2013).”
BackgroundMethodSelf-citationGuidi, M., Kumar, A., & Foster, T. C. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.3523-14.2015 · Cited by 63
“Together with previous work indicating that an oxidize redox state mediates senescent neurophysiology in the hippocampus (Bodhinathan et al., 2010a, b; Kumar and Foster, 2013; Lee et al., 2014), the results point to redox state changes as a process that contributes to the vulnerability of brain…”
BackgroundMethodInfluentialSelf-citationJourdain, P., Rothenfusser, K., Benadiba, C., Allaman, I., Marquet, P. P., & Magistretti, P. J. (2018) · Scientific Reports · doi:10.1038/s41598-018-31534-y · Cited by 65
Marsden, W. N. (2011) · Medical Hypotheses · doi:10.1016/j.mehy.2011.06.021 · Cited by 64
“memory impairment, an effect which is reversed by reducing agents [327].”
BackgroundIn Vivo Imaging with Genetically Encoded Redox Biosensors
Kostyuk, A. I., Panova, A. S., Kokova, A. D., Kotova, D. A., Maltsev, D. I., Podgorny, O. V., Belousov, V. V., & Bilan, D. S. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21218164 · Cited by 66
Craft, S., Foster, T. C., Landfield, P. W., Maier, S. F., Resnick, S. M., & Yaffe, K. (2012) · The Journals of Gerontology Series A · doi:10.1093/gerona/gls112 · Cited by 62
Self-citationThe hypoxia-tolerant vertebrate brain: Arresting synaptic activity
Buck, L. T., & Pamenter, M. E. (2017) · Comparative Biochemistry and Physiology Part B Biochemistry and Molecular Biology · doi:10.1016/j.cbpb.2017.11.015 · Cited by 64
Sun, H., Wu, Z., Nie, X.-W., & Bian, J. (2020) · Current Neuropharmacology · doi:10.2174/1570159x18666200905143550 · Cited by 62
Paula-Lima, A. C., Adasme, T., & Hidalgo, C. (2014) · Antioxidants and Redox Signaling · doi:10.1089/ars.2013.5796 · Cited by 59
“Moreover, the treatment of hippocampal slices from aged rats with dithiothreitol (DTT) enhances CaMKII activity/NMDA receptor-dependent responses (38).”
Dietary phytoestrogen intakes and cognitive function during the menopausal transition
Greendale, G. A., Huang, M.-H., Leung, K., Crawford, S. L., Gold, E. B., Wight, R. G., Waetjen, E., & Karlamangla, A. S. (2012) · Menopause The Journal of The North American Menopause Society · doi:10.1097/gme.0b013e318242a654 · Cited by 57
Wang, T., Yang, Y., Wu, P., Wang, W., Hu, Z., Long, L., Xie, N., Fu, H. Q., Wang, F., & Chen, J. (2010) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2010.10.002 · Cited by 55
Stein, L. R., O’Dell, K. A., Funatsu, M., Zorumski, C. F., & Izumi, Y. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.05.020 · Cited by 60
“For instance, the decline in NMDAR function during aging may be mediated by intracellular redox state (Bodhinathan et al., 2010, Yang et al., 2010).”
BackgroundTitus, D. J., Furones, C., Kang, Y. J., & Atkins, C. M. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.12.002 · Cited by 53
“Oxidative damage is greater in aged animals after TBI, and the oxidation of either a-Ca2+/calmodulindependent protein kinase II or protein kinase C, key mediators of LTP, may be altered in aged animals after TBI (Zhang et al., 2009; Bodhinathan et al., 2010).”
Re-Opening the Critical Window for Estrogen Therapy
Bean, L. A., Kumar, A., Rani, A., Guidi, M., Rosario, A. M., Cruz, P. E., Golde, T. E., & Foster, T. C. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.1890-15.2015 · Cited by 53
“After collection of the total-fEPSP responses, the recording medium was switched to a medium which permitted the isolation of the NMDAR component of synaptic transmission (Bodhinathan et al., 2010; Kumar and Foster, 2013; Lee et al., 2014; Guidi et al., 2015).”
BackgroundMethodInfluentialSelf-citation‘Tagging’ along memories in aging: Synaptic tagging and capture mechanisms in the aged hippocampus
Shetty, M. S., & Sajikumar, S. (2017) · Ageing Research Reviews · doi:10.1016/j.arr.2016.12.008 · Cited by 54
Redox signaling and metabolism in Alzheimer's disease
Holubiec, M. I., Gellert, M., & Hanschmann, E.-M. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.1003721 · Cited by 53
“Inversely, NMDA receptors can be modulated by the cellular redox state, altering synaptic functions in AD (Bodhinathan et al., 2010; Guidi et al., 2015).”
BackgroundDe Simone, G., Mazza, B., Vellucci, L., Barone, A., Ciccarelli, M., & de Bartolomeis, A. (2023) · Antioxidants · doi:10.3390/antiox12040975 · Cited by 49
Aziz, W., Kraev, I., Mizuno, K., Kirby, A. J., Fang, T., Rupawala, H., Kasbi, K., Rothe, S., Jozsa, F., Rosenblum, K., et al. (2019) · Current Biology · doi:10.1016/j.cub.2019.08.064 · Cited by 45
“The late phase of LTP requires synaptic tagging by aCaMKII [46] and aging leads to reduced aCaMKII activity due to direct oxidation of the protein [47].”
Patten, A. R., Brocardo, P. S., Sakiyama, C., Wortman, R. C., Noonan, A., Gil‐Mohapel, J., & Christie, B. R. (2013) · Hippocampus · doi:10.1002/hipo.22199 · Cited by 45
“GSH can modulate the redox state of the NMDA receptor, causing an increase in its activity (Tang and Aizenman, 1993; Janaky et al., 1999; Bodhinathan et al., 2010) and suggesting that increasing GSH may be beneficial in restoring LTP.”
Ghosh, D., LeVault, K. R., & Brewer, G. J. (2013) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2013.06.023 · Cited by 43
“Bodhinathan et al. (2010a, 2010b) found intracellular redox state to enhance N-methyl-Daspartate (NMDA receptor activity, long-term potentiation (LTP), and better-control calcium dynamics in aged but not young mouse.”
Hertelendy, P., Varga, D. P., Menyhárt, Á., Bari, F., & Farkas, E. (2018) · Neurochemistry International · doi:10.1016/j.neuint.2018.10.010 · Cited by 43
“Declining NMDA receptor function was, for example, linked to the oxidation of Ca2+/calmodulin-dependent protein kinase II (Bodhinathan et al., 2010).”
BackgroundKumar, A., Thinschmidt, J. S., & Foster, T. C. (2019) · Aging · doi:10.18632/aging.102108 · Cited by 39
“Oxidizing agents decrease the NMDAR synaptic response, specifically in young animals [6, 14, 40].”
BackgroundResultInfluentialSelf-citationOxidation of ion channels in the aging nervous system
Patel, R., & Sesti, F. (2016) · Brain Research · doi:10.1016/j.brainres.2016.02.046 · Cited by 41
α-Tocopherol and Hippocampal Neural Plasticity in Physiological and Pathological Conditions
Ambrogini, P., Betti, M., Galati, C., Palma, M. D., Lattanzi, D., Savelli, D., Galli, F., Cuppini, R., & Minelli, A. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17122107 · Cited by 39
“ROS have been implicated as modulators of hippocampus-dependent learning and memory [148–150], and can regulate several molecules involved in synaptic transmission (neurotransmitter receptors, such as NMDA (N-methyl-D-aspartate) [151,152] and GABA (γ-aminobutyric acid) receptors [153]; ion channels, such as calcium, s…”
BackgroundFinelli, M. J. (2020) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2020.00254 · Cited by 38
“Interestingly, hyper-S-nitrosation of RyRs shifts these receptors from a finely regulated state to unregulated Ca2+ leak channels (Bull et al., 2008; Bellinger et al., 2009; Bodhinathan et al., 2010b; Liu et al., 2012; Lacampagne et al., 2017; Muñoz et al., 2020).”
BackgroundMethodWang, P., Wang, F., Ni, L., Wu, P., & Chen, J. (2020) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2020.11.012 · Cited by 38
“According to Bodhinathan et al.60, the mechanisms underlying the age-dependent redox modulation of NMDARs are mediated by redox-triggered CaMKII inactivation.”
BackgroundRussell, W. L., Kumar, A., Rani, A., & Foster, T. C. (2013) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2013.12.002 · Cited by 36
“Furthermore, SOD1 overexpression resulted in a decline in NMDAR-mediated synaptic responses and impaired LTP. Co-expression of CAT rescued the effects of overexpression of SOD1 on GSH levels, glutathione peroxidase (GPx) activity, NMDAR function, and LTP. Finally, application of the reducing agent dithiolthreitol (DTT…”
InfluentialSelf-citationRussell, W. L., Kumar, A., Rani, A., Herrera, J., Xu, J., Someya, S., & Foster, T. C. (2011) · Antioxidants and Redox Signaling · doi:10.1089/ars.2011.4054 · Cited by 34
“H 2 O 2 application to hippocampal slices mimics age-related changes, promoting calcium release from internal stores (21), decreasing synaptic CaMKII activity (44), and impairing LTP (3, 26, 40).”
InfluentialSelf-citationImpairments of Synaptic Plasticity in Aged Animals and in Animal Models of Alzheimer's Disease
Balietti, M., Tamagnini, F., Fattoretti, P., Burattini, C., Casoli, T., Platano, D., Lattanzio, F., & Aicardi, G. (2012) · Rejuvenation Research · doi:10.1089/rej.2012.1318 · Cited by 34
“The decline in NMDA receptor responsiveness may be due to age-related alterations in: (1) calcium (Ca(2) + ) homeostasis, leading to increased activity of the phosphatase calcineurin, which in turn reduces Ca(2) + influx through the receptor,(2) and (2) redox state (decrease in redox buffering capacity), leading to ox…”
BackgroundLi, Y., Wu, P., Chen, J., Wang, S., Han, Q.-Q., Li, D., Wang, W., Guan, X., Li, D., Long, L., et al. (2017) · Antioxidants and Redox Signaling · doi:10.1089/ars.2016.6936 · Cited by 33
Dukoff, D. J., Hogg, D. W., Hawrsyh, P. J., & Buck, L. T. (2014) · Journal of Experimental Biology · doi:10.1242/jeb.105825 · Cited by 31
“This may also explain why the effects of H2O2 were reversed by reperfusion but the effects of MPG and NAC were not, similar to other studies in which the effects of oxidizing but not reducing agents were reversed by washout (Bodhinathan et al., 2010; Köhr et al., 1994).”
BackgroundResultGonzález-Fraguela, M. E., Blanco, L., Fernández, C. I., Lorigados, L., Serrano, T., & Fernández, J. L. (2017) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2017.11.015 · Cited by 32
Islam, S., Shajib, M. S., Rashid, R. B., Khan, M. F., Al-Mansur, M. A., Datta, B. K., & Rashid, M. A. (2019) · BMC Complementary and Alternative Medicine · doi:10.1186/s12906-019-2565-x · Cited by 32
“Thus, it can be suggested that antinociceptive effect of HEBA and (+)-catechin involves opening of the ATP-sensitive K channel followed by an efflux of K ions and suppression of excitability of cellular membrane by hyperpolarization and/or repolarization [45].”
BackgroundWu, K., Li, S., Bodhinathan, K., Meyers, C., Chen, W., Campbell‐Thompson, M., McIntyre, L. M., Foster, T. C., Muzyczka, N., & Kumar, A. (2011) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2011.09.006 · Cited by 32
Self-citationSenolytic treatment alleviates doxorubicin‐induced chemobrain
Budamagunta, V., Kumar, A., Rani, A., Sindhu, S. M., Yang, Y., Zhou, D., & Foster, T. C. (2024) · Aging Cell · doi:10.1111/acel.14037 · Cited by 35
“Two weeks after the final senolytic treatment, rats were killed, and electrophysiological assays were performed on rat hippocampal sections as described previously (Bodhinathan et al., 2010; Guidi et al., 2015; Kumar, 2015; Kumar et al., 2009, 2019; Kumar & Foster, 2013; Kumar, Rani, et al., 2018).”
BackgroundMethodSelf-citationHuman Serine Racemase: Key Residues/Active Site Motifs and Their Relation to Enzyme Function
Graham, D. L., Beio, M. L., Nelson, D. L., & Berkowitz, D. B. (2019) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2019.00008 · Cited by 31
Age-Induced Alterations in Hippocampal Function and Metabolism.
Shetty, P. K., Galeffi, F., & Turner, D. A. (2011) · PubMed Central · Cited by 31
Beta-amyloid short- and long-term synaptic entanglement
Lanni, C., Fagiani, F., Racchi, M., Preda, S., Pascale, A., Grilli, M., Allegri, N., & Govoni, S. (2019) · Pharmacological Research · doi:10.1016/j.phrs.2018.11.018 · Cited by 29
Cheong, R. Y., Kwakowsky, A., Barad, Z., Porteous, R. W., Herbison, A. E., & Ábrahám, I. M. (2012) · Endocrinology · doi:10.1210/en.2012-1232 · Cited by 30
Kumar, A., Rani, A., Scheinert, R. B., Ormerod, B. K., & Foster, T. C. (2018) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2018.06.026 · Cited by 30
Self-citationAdulthood systemic inflammation accelerates the trajectory of age-related cognitive decline
Barter, J., Kumar, A., Bean, L. A., Ciesla, M. R., & Foster, T. C. (2021) · Aging · doi:10.18632/aging.203588 · Cited by 29
“Methods for collection of hippocampal slices and recordings have been published previously [34, 40, 76].”
BackgroundSelf-citationAntinociceptive effect of methanol extract of Celosia cristata Linn. in mice
Islam, S., Shajib, M. S., & Ahmed, T. (2016) · BMC Complementary and Alternative Medicine · doi:10.1186/s12906-016-1393-5 · Cited by 28
“The NMDA signaling in the pain inducement is influenced by the free radicals [69].”
BackgroundBillard, J. (2018) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2018.00106 · Cited by 28
“, 2013) but defects affecting the functional modulation of the receptor have also been later characterized including deregulation at the redox site (Kuehl-Kovarik et al., 2003; Bodhinathan et al., 2010; Yang et al., 2010; Kumar et al., 2017), changes in non-competitive blockade (Norris and Foster, 1999) and even alter…”
BackgroundFebo, M., & Foster, T. C. (2016) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2016.00158 · Cited by 28
“Recent work indicates that the oxidation–reduction (redox) status of neurons underlies senescent physiology including impaired synaptic plasticity and the emergence of cognitive impairment (Bodhinathan et al., 2010a,b; Kumar and Foster, 2013; Lee et al., 2014; Guidi et al., 2015a).”
BackgroundSelf-citationCheng, Y.-F., Guo, L., Xie, Y., Liu, Y., Zhang, J., Qingwen, W., & Li, J. (2012) · Neurochemical Research · doi:10.1007/s11064-012-0894-y · Cited by 27
“An age-related increase in oxidative stress is likely to contribute to a rise in intracellular calcium originating from L-channels, as well as a decrease in calcium influx through NMDA receptors [42].”
Triclosan Impairs Hippocampal Synaptic Plasticity and Spatial Memory in Male Rats
Arias‐Cavieres, A., More, J., Vicente, J. M., Adasme, T., Hidalgo, J., Valdés, J. L., Humeres, A., Valdés-Undurraga, I., Sánchez, G., Hidalgo, C., et al. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00429 · Cited by 27
“We evaluated the effect of triclosan on membrane capacity and membrane resistance of primary hippocampal neurons under the cell-attach configuration, as described (Bournaud et al., 1998).”
MethodRani, A., & Prasad, S. (2014) · Neurochemical Research · doi:10.1007/s11064-014-1388-x · Cited by 25
Chiang, T.-I., Yu, Y., Lin, C., & Lane, H. (2021) · Clinical Psychopharmacology and Neuroscience · doi:10.9758/cpn.2021.19.3.423 · Cited by 26
Calcium Signaling During Brain Aging and Its Influence on the Hippocampal Synaptic Plasticity
Kumar, A. (2019) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-12457-1_39 · Cited by 25
Self-citationBaucum, A. J., Strack, S., & Colbran, R. J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031554 · Cited by 24
Proteome profiling in the hippocampus, medial prefrontal cortex, and striatum of aging rat
Hamezah, H. S., Durani, L. W., Yanagisawa, D., Ibrahim, N. F., Aizat, W. M., Bellier, J., Makpol, S., Ngah, W. Z. W., Damanhuri, H. A., & Tooyama, I. (2018) · Experimental Gerontology · doi:10.1016/j.exger.2018.07.002 · Cited by 26
“In addition, a previous study provided a link between age-related alterations in NMDA receptors with CAMK2 function (Bodhinathan et al. 2010).”
BackgroundCitrulline prevents age-related LTP decline in old rats
Ginguay, A., Regazzetti, A., Laprévôte, O., Moinard, C., Bandt, J. P. D., Cynober, L., Billard, J., Allinquant, B., & Dutar, P. (2019) · Scientific Reports · doi:10.1038/s41598-019-56598-2 · Cited by 23
Hosseini, M., Karami, Z., Yousefifard, M., Janzadeh, A., Zamani, E., & Nasirinezhad, F. (2020) · Brain and Behavior · doi:10.1002/brb3.1576 · Cited by 23
Modulation of GDF11 expression and synaptic plasticity by age and training
Domenico, E. D., D’Arcangelo, G., Faraoni, I., Palmieri, M., Tancredi, V., Graziani, G., Grimaldi, P., & Tentori, L. (2017) · Oncotarget · doi:10.18632/oncotarget.19854 · Cited by 22
Dopamine D4 receptor activation restores CA 1 LTP in hippocampal slices from aged mice
Guo, F., Zhao, J., Zhao, D., Wang, J., Wang, X., Feng, Z., Vreugdenhil, M., & Lu, C. (2017) · Aging Cell · doi:10.1111/acel.12666 · Cited by 22
“This may be because with aging Ca influx through NMDARs is reduced (Bodhinathan et al., 2010) and Ca influx through L-type VDCCs is increased (Norris et al.”
BackgroundArias‐Cavieres, A., Fonteh, A., Castro-Rivera, C. I., & Garcia, A. J. (2021) · Experimental Neurology · doi:10.1016/j.expneurol.2021.113808 · Cited by 17
Jekabsone, A., Jankevičiūtė, S., Pampuščenko, K., Borutaitė, V., & Morkūnienė, R. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241512315 · Cited by 21
Redox Sensitivity of Tyrosine Hydroxylase Activity and Expression in Dopaminergic Dysfunction
Giovanni, G. D., Pessia, M., & Maio, R. D. (2012) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/187152712800792938 · Cited by 21
“The redox state of thiols exerts a profound effect on the physiology of neurons; for instance, it regulates fundamental processes such as synaptic plasticity [45] and controls the conductance of several ion channels involved in neuronal excitability [46, 47].”
Cariati, I., Bonanni, R., Annino, G., Scimeca, M., Bonanno, E., D’Arcangelo, G., & Tancredi, V. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.678449 · Cited by 21
“…which is known to be caused by a decrease in N-methyl-D-aspartate receptor activity that occurs during the aging process and is partially linked to a condition of oxidative stress (Tombaugh et al., 2002; Billard and Rouaud, 2007; Bodhinathan et al., 2010; Kumar, 2015; Kumar and Foster, 2019).”
Background
Metadata
- Authors
- Bodhinathan, K., Kumar, A., & Foster, T. C.
- Affiliations
- University of Florida (US)
- Corresponding author
- Foster, Thomas C.
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2010-02-03
- Volume
- 30
- Issue
- 5
- Pages
- 1914-1924
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC2853968
- OpenAlex
- W1990653561
- Cited by
- 153
- References
- 56
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 4 · 2023: 5 · 2022: 3 · 2021: 10 · 2020: 10 · 2019: 12 · 2018: 12 · 2017: 12 · 2016: 14 · 2015: 16 · 2014: 7 · 2013: 9 · 2012: 17
- FWCI
- 5.30
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Brain Research Foundation
- McKnight Foundation
- Evelyn F. McKnight Brain Research Foundation
- National Institutes of Health
- National Institute on Aging (R01AG014979, AG014979, P30AG028740)
- National Institute of Mental Health (MH 059891, R01MH059891)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- NMDA receptor, cellular redox state, aging, CaMKII, oxidative stress, synaptic plasticity, long-term potentiation, hippocampus, CA3-CA1 synapses, xanthine/xanthine oxidase, dithiothreitol, glutathione, memory impairment
- MeSH terms
- Aging, Animals, Calcium, Hippocampus, Neuronal Plasticity, Oxidation-Reduction, Rats, Inbred F344, Synapses, Receptors, N-Methyl-D-Aspartate, Reactive Oxygen Species, Rats, Calcium-Calmodulin-Dependent Protein Kinase Type 2
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