Developmental changes in cerebral NAD and neuroenergetics of an antioxidant compromised mouse model of schizophrenia.
Journal
Translational psychiatry
ISSN: 2158-3188
Titre abrégé: Transl Psychiatry
Pays: United States
ID NLM: 101562664
Informations de publication
Date de publication:
05 08 2023
05 08 2023
Historique:
received:
19
03
2022
accepted:
24
07
2023
revised:
20
07
2023
medline:
7
8
2023
pubmed:
6
8
2023
entrez:
5
8
2023
Statut:
epublish
Résumé
Defects in essential metabolic regulation for energy supply, increased oxidative stress promoting excitatory/inhibitory imbalance and phospholipid membrane dysfunction have been implicated in the pathophysiology of schizophrenia (SZ). The knowledge about the developmental trajectory of these key pathophysiological components and their interplay is important to develop new preventive and treatment strategies. However, this assertion is so far limited. To investigate the developmental regulations of these key components in the brain, we assessed, for the first time, in vivo redox state from the oxidized (NAD
Identifiants
pubmed: 37543592
doi: 10.1038/s41398-023-02568-2
pii: 10.1038/s41398-023-02568-2
pmc: PMC10404265
doi:
Substances chimiques
Antioxidants
0
NAD
0U46U6E8UK
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
275Informations de copyright
© 2023. Springer Nature Limited.
Références
Owen MJ, Sawa A, Mortensen PB. Schizophrenia. Lancet. 2016;388:86–97.
pubmed: 26777917
pmcid: 4940219
Guzman F. The four dopamine pathways relevant to antipsychotics pharmacology—Psychopharmacology Institute. 2019. https://psychopharmacologyinstitute.com/publication/the-four-dopamine-pathways-relevant-to-antipsychotics-pharmacology-2096#%20References . Accessed 27 Aug 2020.
Cannon TD. How Schizophrenia develops: cognitive and brain mechanisms underlying onset of Psychosis. Trends Cogn Sci. 2015;19:744–56.
pubmed: 26493362
pmcid: 4673025
Hardingham GE, Do KQ. Linking early-life NMDAR hypofunction and oxidative stress in schizophrenia pathogenesis. Nat Rev Neurosci. 2016;17:125–34.
pubmed: 26763624
Cuenod M, Steullet P, Cabungcal J-H, Dwir D, Khadimallah I, Klauser P, et al. Caught in vicious circles: a perspective on dynamic feed-forward loops driving oxidative stress in schizophrenia. Mol Psychiatry. 2021;27:1–12.
Yang J, Chen T, Sun L, Zhao Z, Qi X, Zhou K, et al. Potential metabolite markers of schizophrenia. Mol Psychiatry. 2013;18:67–78.
pubmed: 22024767
Mahadik SP, Evans DR. Is schizophrenia a metabolic brain disorder? Membrane phospholipid dysregulation and its therapeutic implications. Psychiatr Clin. 2003;26:85–102.
Do KQ, Trabesinger AH, Kirsten-Krüger M, Lauer CJ, Dydak U, Hell D, et al. Schizophrenia: glutathione deficit in cerebrospinal fluid and prefrontal cortex in vivo. Eur J Neurosci. 2000;12:3721–8.
pubmed: 11029642
Wang AM, Pradhan S, Coughlin JM, Trivedi A, DuBois SL, Crawford JL, et al. Assessing brain metabolism with 7-T proton magnetic resonance spectroscopy in patients with first-episode Psychosis. JAMA Psychiatry. 2019;76:314–23.
pubmed: 30624573
pmcid: 6439827
Das TK, Javadzadeh A, Dey A, Sabesan P, Théberge J, Radua J, et al. Antioxidant defense in schizophrenia and bipolar disorder: a meta-analysis of MRS studies of anterior cingulate glutathione. Prog Neuropsychopharmacol Biol Psychiatry. 2019;91:94–102.
pubmed: 30125624
Perkins DO, Jeffries CD, Do KQ. Potential roles of redox dysregulation in the development of Schizophrenia. Biol Psychiatry. 2020;88:326–36.
pubmed: 32560962
pmcid: 7395886
Ying W. NAD+/NADH and NADP+/NADPH in cellular functions and cell death: regulation and biological consequences. Antioxid Redox Signal. 2008;10:179–206.
pubmed: 18020963
Pollak N, Dölle C, Ziegler M. The power to reduce: pyridine nucleotides—small molecules with a multitude of functions. Biochem J. 2007;402:205–18.
pubmed: 17295611
pmcid: 1798440
Kim S-Y, Cohen BM, Chen X, Lukas SE, Shinn AK, Yuksel AC, et al. Redox Dysregulation in Schizophrenia Revealed by in vivo NAD+/NADH Measurement. Schizophr Bull. 2017;43:197–204.
pubmed: 27665001
Skupienski R, Do KQ, Xin L. In vivo 31 P magnetic resonance spectroscopy study of mouse cerebral NAD content and redox state during neurodevelopment. Sci Rep. 2020;10:15623.
pubmed: 32973277
pmcid: 7519085
Cabungcal J-H, Steullet P, Kraftsik R, Cuenod M, Do KQ. A developmental redox dysregulation leads to spatio-temporal deficit of parvalbumin neuron circuitry in a schizophrenia mouse model. Schizophrenia Res. 2019;213:96–106.
Khadimallah I, Jenni R, Cabungcal J-H, Cleusix M, Fournier M, Beard E, et al. Mitochondrial, exosomal miR137-COX6A2 and gamma synchrony as biomarkers of parvalbumin interneurons, psychopathology, and neurocognition in schizophrenia. Mol Psychiatry. 2021;27:1–13.
Corcoba A, Steullet P, Duarte JMN, Van de Looij Y, Monin A, Cuenod M, et al. Glutathione deficit affects the integrity and function of the Fimbria/Fornix and anterior commissure in mice: relevance for Schizophrenia. Int J Neuropsychopharmacol. 2015;19:pyv110.
pubmed: 26433393
pmcid: 4815475
Monin A, Baumann PS, Griffa A, Xin L, Mekle R, Fournier M, et al. Glutathione deficit impairs myelin maturation: relevance for white matter integrity in schizophrenia patients. Mol Psychiatry. 2015;20:827–38.
pubmed: 25155877
Kulak A, Duarte JMN, Do KQ, Gruetter R. Neurochemical profile of the developing mouse cortex determined by in vivo 1H NMR spectroscopy at 14.1 T and the effect of recurrent anaesthesia. J Neurochem. 2010;115:1466–77.
pubmed: 20946416
das Neves Duarte JM, Kulak A, Gholam-Razaee MM, Cuenod M, Gruetter R, Do KQ. N-Acetylcysteine normalizes neurochemical changes in the glutathione-deficient Schizophrenia mouse model during development. Biol Psychiatry. 2012;71:1006–14.
pubmed: 21945305
Kendig EL, Chen Y, Krishan M, Johansson E, Schneider SN, Genter MB, et al. Lipid metabolism and body composition in Gclm(−/−) mice. Toxicol Appl Pharmacol. 2011;257:338–48.
pubmed: 21967773
pmcid: 3226854
Cabungcal J-H, Steullet P, Kraftsik R, Cuenod M, Do KQ. Early-life insults impair parvalbumin interneurons via oxidative stress: reversal by N-acetylcysteine. Biol Psychiatry. 2013;73:574–82.
pubmed: 23140664
Dutta S, Sengupta P. Men and mice: relating their ages. Life Sci. 2016;152:244–8.
pubmed: 26596563
Hagan C, D.V.M., Ph.D. When are mice considered old? The Jackson Laboratory. 2017. https://www.jax.org/news-and-insights/jax-blog/2017/november/when-are-mice-considered-old . Accessed 29 Jul 2020.
Sengupta P. The laboratory rat: relating its age with human’s. Int J Prev Med. 2013;4:624–30.
pubmed: 23930179
pmcid: 3733029
Gruetter R, Tkác I. Field mapping without reference scan using asymmetric echo-planar techniques. Magn Reson Med. 2000;43:319–23.
pubmed: 10680699
Xie N, Zhang L, Gao W, Huang C, Huber PE, Zhou X, et al. NAD + metabolism: pathophysiologic mechanisms and therapeutic potential. Signal Transduct Target Ther. 2020;5:1–37.
Johnson S, Imai S. NAD+ biosynthesis, aging, and disease. F1000Res. 2018;7:132.
pubmed: 29744033
pmcid: 5795269
Nishida T, Naguro I, Ichijo H. NAMPT-dependent NAD+ salvage is crucial for the decision between apoptotic and necrotic cell death under oxidative stress. Cell Death Discov. 2022;8:1–11.
Rajman L, Chwalek K, Sinclair DA. Therapeutic potential of NAD-boosting molecules: the in vivo evidence. Cell Metab. 2018;27:529–47.
pubmed: 29514064
pmcid: 6342515
Pirinen E, Auranen M, Khan NA, Brilhante V, Urho N, Pessia A, et al. Niacin cures systemic NAD+ deficiency and improves muscle performance in adult-onset mitochondrial myopathy. Cell Metab. 2020;31:1078–1090.e5.
pubmed: 32386566
Yang J, Klaidman LK, Nalbandian A, Oliver J, Chang ML, Chan PH, et al. The effects of nicotinamide on energy metabolism following transient focal cerebral ischemia in Wistar rats. Neurosci Lett. 2002;333:91–94.
pubmed: 12419488
de Picciotto NE, Gano LB, Johnson LC, Martens CR, Sindler AL, Mills KF, et al. Nicotinamide mononucleotide supplementation reverses vascular dysfunction and oxidative stress with aging in mice. Aging Cell. 2016;15:522–30.
pubmed: 26970090
pmcid: 4854911
Hong G, Zheng D, Zhang L, Ni R, Wang G, Fan G-C, et al. Administration of nicotinamide riboside prevents oxidative stress and organ injury in sepsis. Free Radic Biol Med. 2018;123:125–37.
pubmed: 29803807
pmcid: 6236680
Zhu Y, Zhao K-K, Tong Y, Zhou Y-L, Wang Y-X, Zhao P-Q, et al. Exogenous NAD(+) decreases oxidative stress and protects H2O2-treated RPE cells against necrotic death through the up-regulation of autophagy. Sci Rep. 2016;6:26322.
pubmed: 27240523
pmcid: 4886526
Santos ARS, Gerhardt ECM, Moure VR, Pedrosa FO, Souza EM, Diamanti R, et al. Kinetics and structural features of dimeric glutamine-dependent bacterial NAD+ synthetases suggest evolutionary adaptation to available metabolites. J Biol Chem. 2018;293:7397–407.
pubmed: 29581233
pmcid: 5950007
Lavoie S, Steullet P, Kulak A, Preitner F, Do KQ, Magistretti PJ. Glutamate cysteine ligase-modulatory subunit knockout mouse shows normal insulin sensitivity but reduced liver glycogen storage. Front Physiol. 2016;7:142.
pubmed: 27148080
pmcid: 4838631
Lavoie S, Allaman I, Petit J-M, Do KQ, Magistretti PJ. Altered glycogen metabolism in cultured astrocytes from mice with chronic glutathione deficit; relevance for neuroenergetics in schizophrenia. PLoS One. 2011;6:e22875.
pubmed: 21829542
pmcid: 3145770
Lee YJ, Lee JH, Han HJ. Extracellular adenosine triphosphate protects oxidative stress-induced increase of p21(WAF1/Cip1) and p27(Kip1) expression in primary cultured renal proximal tubule cells: role of PI3K and Akt signaling. J Cell Physiol. 2006;209:802–10.
pubmed: 16972266
Yuksel C, Tegin C, O’Connor L, Du F, Ahat E, Cohen BM, et al. Phosphorus magnetic resonance spectroscopy studies in schizophrenia. J Psychiatr Res. 2015;68:157–66.
pubmed: 26228415
Du F, Cooper AJ, Thida T, Sehovic S, Lukas SE, Cohen BM, et al. In vivo evidence for cerebral bioenergetic abnormalities in schizophrenia measured using 31P magnetization transfer spectroscopy. JAMA Psychiatry. 2014;71:19–27.
pubmed: 24196348
pmcid: 7461723
Hosios AM, Hecht VC, Danai LV, Johnson MO, Rathmell JC, Steinhauser ML, et al. Amino acids rather than glucose account for the majority of cell mass in proliferating mammalian cells. Dev Cell. 2016;36:540–9.
pubmed: 26954548
pmcid: 4766004
Reitzer LJ, Wice BM, Kennell D. Evidence that glutamine, not sugar, is the major energy source for cultured HeLa cells. J Biol Chem. 1979;254:2669–76.
pubmed: 429309
Stumvoll M, Perriello G, Meyer C, Gerich J. Role of glutamine in human carbohydrate metabolism in kidney and other tissues. Kidney Int. 1999;55:778–92.
pubmed: 10027916
Bustillo J, Rowland L, Mullins P, Jung R, Chen H, Qualls C, et al. 1H-MRS at 4 Tesla in minimally treated early schizophrenia. Mol Psychiatry. 2010;15:629–36.
pubmed: 19918243
Fournier M, Ferrari C, Baumann PS, Polari A, Monin A, Bellier-Teichmann T, et al. Impaired metabolic reactivity to oxidative stress in early psychosis patients. Schizophr Bull. 2014;40:973–83.
pubmed: 24687046
pmcid: 4133680
Ren J, Malloy CR, Sherry AD. Quantitative measurement of redox state in human brain by 31P MRS at 7T with spectral simplification and inclusion of multiple nucleotide sugar components in data analysis. Magn Reson Med. 2020;84:2338–51.
pubmed: 32385936
pmcid: 7396304
Bosiacki M, Gąssowska-Dobrowolska M, Kojder K, Fabiańska M, Jeżewski D, Gutowska I et al. Perineuronal nets and their role in synaptic homeostasis. Int J Mol Sci. 2019. https://doi.org/10.3390/ijms20174108 .
Pantazopoulos H, Katsel P, Haroutunian V, Chelini G, Klengel T, Berretta S Molecular signature of extracellular matrix pathology in schizophrenia. Eur J Neurosci. 2020. https://doi.org/10.1111/ejn.15009 .
de Graaf RA, De Feyter HM, Brown PB, Nixon TW, Rothman DL, Behar KL. Detection of cerebral NAD+ in humans at 7 T. Magn Reson Med. 2017;78:828–35.
pubmed: 27670385