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Current Neuropharmacology

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ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

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Review Article

Deciphering the Metabolome under Stress: Insights from Rodent Models

Author(s): Maria P. Papageorgiou, Daniela Theodoridou, Markus Nussbaumer, Maria Syrrou and Michaela D. Filiou*

Volume 22, Issue 5, 2024

Published on: 13 July, 2023

Page: [884 - 903] Pages: 20

DOI: 10.2174/1570159X21666230713094843

Price: $65

Abstract

Despite intensive research efforts to understand the molecular underpinnings of psychological stress and stress responses, the underlying molecular mechanisms remain largely elusive. Towards this direction, a plethora of stress rodent models have been established to investigate the effects of exposure to different stressors. To decipher affected molecular pathways in a holistic manner in these models, metabolomics approaches addressing altered, small molecule signatures upon stress exposure in a high-throughput, quantitative manner provide insightful information on stress-induced systemic changes in the brain. In this review, we discuss stress models in mice and rats, followed by mass spectrometry (MS) and nuclear magnetic resonance (NMR) metabolomics studies. We particularly focus on acute, chronic and early life stress paradigms, highlight how stress is assessed at the behavioral and molecular levels and focus on metabolomic outcomes in the brain and peripheral material such as plasma and serum. We then comment on common metabolomics patterns across different stress models and underline the need for unbiased -omics methodologies and follow-up studies of metabolomics outcomes to disentangle the complex pathobiology of stress and pertinent psychopathologies.

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[1]
Filiou, M.D.; Sandi, C. Anxiety and brain mitochondria: A bidirectional crosstalk. Trends Neurosci., 2019, 42(9), 573-588.
[http://dx.doi.org/10.1016/j.tins.2019.07.002] [PMID: 31362874]
[2]
Chrousos, G.P. Stress and disorders of the stress system. Nat. Rev. Endocrinol., 2009, 5(7), 374-381.
[http://dx.doi.org/10.1038/nrendo.2009.106] [PMID: 19488073]
[3]
Yip, K.S. Taoism and its impact on mental health of the Chinese communities. Int. J. Soc. Psychiatry, 2004, 50(1), 25-42.
[http://dx.doi.org/10.1177/0020764004038758] [PMID: 15143845]
[4]
Pascoe, M.C.; Thompson, D.R.; Jenkins, Z.M.; Ski, C.F. Mindfulness mediates the physiological markers of stress: Systematic review and meta-analysis. J. Psychiatr. Res., 2017, 95, 156-178.
[http://dx.doi.org/10.1016/j.jpsychires.2017.08.004] [PMID: 28863392]
[5]
Maddux, R.E.; Daukantaité, D.; Tellhed, U. The effects of yoga on stress and psychological health among employees: an 8- and 16-week intervention study. Anxiety Stress Coping, 2018, 31(2), 121-134.
[http://dx.doi.org/10.1080/10615806.2017.1405261] [PMID: 29166771]
[6]
Liu, W.; Ge, T.; Leng, Y.; Pan, Z.; Fan, J.; Yang, W.; Cui, R. The role of neural plasticity in depression: From hippocampus to prefrontal cortex. Neural Plast., 2017, 2017, 1-11.
[http://dx.doi.org/10.1155/2017/6871089] [PMID: 28246558]
[7]
Feyissa, A.M.; Chandran, A.; Stockmeier, C.A.; Karolewicz, B. Reduced levels of NR2A and NR2B subunits of NMDA receptor and PSD-95 in the prefrontal cortex in major depression. Prog. Neuropsychopharmacol. Biol. Psychiatry, 2009, 33(1), 70-75.
[http://dx.doi.org/10.1016/j.pnpbp.2008.10.005] [PMID: 18992785]
[8]
Patchev, V.K.; Patchev, A.V. Experimental models of stress. Dialogues Clin. Neurosci., 2006, 8(4), 417-432.
[http://dx.doi.org/10.31887/DCNS.2006.8.4/vpatchev] [PMID: 17290800]
[9]
Adhikari, A. Distributed circuits underlying anxiety. Front. Behav. Neurosci., 2014, 8, 112.
[http://dx.doi.org/10.3389/fnbeh.2014.00112] [PMID: 24744710]
[10]
Chen, Y.; Baram, T.Z. Toward understanding how early-life stress reprograms cognitive and emotional brain networks. Neuropsychopharmacology, 2016, 41(1), 197-206.
[http://dx.doi.org/10.1038/npp.2015.181] [PMID: 26105143]
[11]
Papadopoulou, Z.; Vlaikou, A.M.; Theodoridou, D.; Markopoulos, G.S.; Tsoni, K.; Agakidou, E.; Drosou-Agakidou, V.; Turck, C.W.; Filiou, M.D.; Syrrou, M. Stressful newborn memories: Pre-Conceptual, in utero, and postnatal events. Front. Psychiatry, 2019, 10, 220.
[http://dx.doi.org/10.3389/fpsyt.2019.00220] [PMID: 31057437]
[12]
Buynitsky, T.; Mostofsky, D.I. Restraint stress in biobehavioral research: Recent developments. Neurosci. Biobehav. Rev., 2009, 33(7), 1089-1098.
[http://dx.doi.org/10.1016/j.neubiorev.2009.05.004] [PMID: 19463853]
[13]
Can, A.; Dao, D.T.; Arad, M.; Terrillion, C.E.; Piantadosi, S.C.; Gould, T.D. The mouse forced swim test. J. Vis. Exp., 2012, (59), e3638.
[PMID: 22314943]
[14]
de Kloet, E.R.; Molendijk, M.L. Coping with the forced swim stressor: Towards understanding an adaptive mechanism. Neural Plast., 2016, 2016, 1-13.
[http://dx.doi.org/10.1155/2016/6503162] [PMID: 27034848]
[15]
Slattery, D.A.; Cryan, J.F. Using the rat forced swim test to assess antidepressant-like activity in rodents. Nat. Protoc., 2012, 7(6), 1009-1014.
[http://dx.doi.org/10.1038/nprot.2012.044] [PMID: 22555240]
[16]
Armario, A.; Gavaldà, A.; Martí, J. Comparison of the behavioural and endocrine response to forced swimming stress in five inbred strains of rats. Psychoneuroendocrinology, 1995, 20(8), 879-890.
[http://dx.doi.org/10.1016/0306-4530(95)00018-6] [PMID: 8834094]
[17]
Bohacek, J.; Manuella, F.; Roszkowski, M.; Mansuy, I.M. Hippocampal gene expression induced by cold swim stress depends on sex and handling. Psychoneuroendocrinology, 2015, 52, 1-12.
[http://dx.doi.org/10.1016/j.psyneuen.2014.10.026] [PMID: 25459888]
[18]
Gould, T.D. Mood and Anxiety Related Phenotypes in Mice; Humana Totowa: NJ, 2009, XII, p. 334.
[http://dx.doi.org/10.1007/978-1-60761-303-9]
[19]
Fujii, S.; Kaushik, M.K.; Zhou, X.; Korkutata, M.; Lazarus, M. Acute social defeat stress increases sleep in mice. Front. Neurosci., 2019, 13, 322.
[http://dx.doi.org/10.3389/fnins.2019.00322] [PMID: 31001080]
[20]
Monteiro, S.; Roque, S.; de Sá-Calçada, D.; Sousa, N.; Correia-Neves, M.; Cerqueira, J.J. An efficient chronic unpredictable stress protocol to induce stress-related responses in C57BL/6 mice. Front. Psychiatry, 2015, 6, 6.
[http://dx.doi.org/10.3389/fpsyt.2015.00006] [PMID: 25698978]
[21]
Willner, P. Reliability of the chronic mild stress model of depression: A user survey. Neurobiol. Stress, 2017, 6, 68-77.
[http://dx.doi.org/10.1016/j.ynstr.2016.08.001] [PMID: 28229110]
[22]
Munhoz, C.; Madrigal, J.L.M.; García-Bueno, B.; Pradillo, J.M.; Moro, M.A.; Lizasoain, I.; Lorenzo, P.; Scavone, C.; Leza, J.C. TNF-alpha accounts for short-term persistence of oxidative status in rat brain after two weeks of repeated stress. Eur. J. Neurosci., 2004, 20(4), 1125-1130.
[http://dx.doi.org/10.1111/j.1460-9568.2004.03560.x] [PMID: 15305883]
[23]
Glavin, G.B.; Paré, W.P.; Sandbak, T.; Bakke, H.K.; Murison, R. Restraint stress in biomedical research: An update. Neurosci. Biobehav. Rev., 1994, 18(2), 223-249.
[http://dx.doi.org/10.1016/0149-7634(94)90027-2] [PMID: 8058215]
[24]
Hollis, F.; Kabbaj, M. Social defeat as an animal model for depression. ILAR J., 2014, 55(2), 221-232.
[http://dx.doi.org/10.1093/ilar/ilu002] [PMID: 25225302]
[25]
Golden, S.A.; Covington, H.E., III; Berton, O.; Russo, S.J. A standardized protocol for repeated social defeat stress in mice. Nat. Protoc., 2011, 6(8), 1183-1191.
[http://dx.doi.org/10.1038/nprot.2011.361] [PMID: 21799487]
[26]
Badowska-Szalewska, E.; Klejbor, I.; Cecot, T.; Spodnik, J.H. Moryś J. Changes in NGF/c-Fos double staining in the structures of the limbic system in juvenile and aged rats exposed to forced swim test. Acta Neurobiol. Exp., 2009, 69(4), 448-458.
[PMID: 20048762]
[27]
Gardner, K.L.; Thrivikraman, K.V.; Lightman, S.L.; Plotsky, P.M.; Lowry, C.A. Early life experience alters behavior during social defeat: Focus on serotonergic systems. Neuroscience, 2005, 136(1), 181-191.
[http://dx.doi.org/10.1016/j.neuroscience.2005.07.042] [PMID: 16182451]
[28]
Alves, R.L.; Portugal, C.C.; Summavielle, T.; Barbosa, F.; Magalhães, A. Maternal separation effects on mother rodents’ behaviour: A systematic review. Neurosci. Biobehav. Rev., 2020, 117, 98-109.
[http://dx.doi.org/10.1016/j.neubiorev.2019.09.008] [PMID: 31499082]
[29]
Pryce, C.R.; Feldon, J. Long-term neurobehavioural impact of the postnatal environment in rats: Manipulations, effects and mediating mechanisms. Neurosci. Biobehav. Rev., 2003, 27(1-2), 57-71.
[http://dx.doi.org/10.1016/S0149-7634(03)00009-5] [PMID: 12732223]
[30]
Rice, C.J.; Sandman, C.A.; Lenjavi, M.R.; Baram, T.Z. A novel mouse model for acute and long-lasting consequences of early life stress. Endocrinology, 2008, 149(10), 4892-4900.
[http://dx.doi.org/10.1210/en.2008-0633] [PMID: 18566122]
[31]
Spencer, R.L.; Deak, T. A users guide to HPA axis research. Physiol. Behav., 2017, 178, 43-65.
[http://dx.doi.org/10.1016/j.physbeh.2016.11.014] [PMID: 27871862]
[32]
Tsigos, C.; Chrousos, G.P. Hypothalamic–pituitary–adrenal axis, neuroendocrine factors and stress. J. Psychosom. Res., 2002, 53(4), 865-871.
[http://dx.doi.org/10.1016/S0022-3999(02)00429-4] [PMID: 12377295]
[33]
Krontira, A.C.; Cruceanu, C.; Binder, E.B. Glucocorticoids as mediators of adverse outcomes of prenatal stress. Trends Neurosci., 2020, 43(6), 394-405.
[http://dx.doi.org/10.1016/j.tins.2020.03.008] [PMID: 32459992]
[34]
Haller, J.; Aliczki, M.; Gyimesine Pelczer, K. Classical and novel approaches to the preclinical testing of anxiolytics: A critical evaluation. Neurosci. Biobehav. Rev., 2013, 37(10), 2318-2330.
[http://dx.doi.org/10.1016/j.neubiorev.2012.09.001] [PMID: 22981935]
[35]
Pellow, S.; Chopin, P.; File, S.E.; Briley, M. Validation of open: Closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J. Neurosci. Methods, 1985, 14(3), 149-167.
[http://dx.doi.org/10.1016/0165-0270(85)90031-7] [PMID: 2864480]
[36]
Walf, A.A.; Frye, C.A. The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nat. Protoc., 2007, 2(2), 322-328.
[http://dx.doi.org/10.1038/nprot.2007.44] [PMID: 17406592]
[37]
Kraeuter, A.K.; Guest, P.C.; Sarnyai, Z. The open field test for measuring locomotor activity and anxiety-like behavior. Methods Mol. Biol., 2019, 1916, 99-103.
[http://dx.doi.org/10.1007/978-1-4939-8994-2_9] [PMID: 30535687]
[38]
Ramos, A.; Mormède, P. Stress and emotionality: A multidimensional and genetic approach. Neurosci. Biobehav. Rev., 1997, 22(1), 33-57.
[http://dx.doi.org/10.1016/S0149-7634(97)00001-8] [PMID: 9491939]
[39]
Porsolt, R.D.; Le Pichon, M.; Jalfre, M. Depression: A new animal model sensitive to antidepressant treatments. Nature, 1977, 266(5604), 730-732.
[http://dx.doi.org/10.1038/266730a0] [PMID: 559941]
[40]
Cryan, J.F.; Mombereau, C. In search of a depressed mouse: Utility of models for studying depression-related behavior in genetically modified mice. Mol. Psychiatry, 2004, 9(4), 326-357.
[http://dx.doi.org/10.1038/sj.mp.4001457] [PMID: 14743184]
[41]
Toth, I.; Neumann, I.D. Animal models of social avoidance and social fear. Cell Tissue Res., 2013, 354(1), 107-118.
[http://dx.doi.org/10.1007/s00441-013-1636-4] [PMID: 23760888]
[42]
Ducottet, C.; Griebel, G.; Belzung, C. Effects of the selective nonpeptide corticotropin-releasing factor receptor 1 antagonist antalarmin in the chronic mild stress model of depression in mice. Prog. Neuropsychopharmacol. Biol. Psychiatry, 2003, 27(4), 625-631.
[http://dx.doi.org/10.1016/S0278-5846(03)00051-4] [PMID: 12787849]
[43]
Monleon, S.; Parra, A.; Simon, V.M.; Brain, P.F.; D’Aquila, P.; Willner, P. Attenuation of sucrose consumption in mice by chronic mild stress and its restoration by imipramine. Psychopharmacology, 1995, 117(4), 453-457.
[http://dx.doi.org/10.1007/BF02246218] [PMID: 7604147]
[44]
Harkin, A.; Houlihan, D.D.; Kelly, J.P. Reduction in preference for saccharin by repeated unpredictable stress in mice and its prevention by imipramine. J. Psychopharmacol., 2002, 16(2), 115-123.
[http://dx.doi.org/10.1177/026988110201600201] [PMID: 12095069]
[45]
McEwen, B.S. Plasticity of the hippocampus: Adaptation to chronic stress and allostatic load. Ann. N. Y. Acad. Sci., 2001, 933(1), 265-277.
[http://dx.doi.org/10.1111/j.1749-6632.2001.tb05830.x] [PMID: 12000027]
[46]
Jones, B.C.; Sarrieau, A.; Reed, C.L.; Azar, M.R.; Mormède, P. Contribution of sex and genetics to neuroendocrine adaptation to stress in mice. Psychoneuroendocrinology, 1998, 23(5), 505-517.
[http://dx.doi.org/10.1016/S0306-4530(98)00014-6] [PMID: 9802125]
[47]
Palme, R. Non-invasive measurement of glucocorticoids: Advances and problems. Physiol. Behav., 2019, 199, 229-243.
[http://dx.doi.org/10.1016/j.physbeh.2018.11.021] [PMID: 30468744]
[48]
Ralph, C.R.; Tilbrook, A.J. Invited review: The usefulness of measuring glucocorticoids for assessing animal welfare. J. Anim. Sci., 2016, 94(2), 457-470.
[http://dx.doi.org/10.2527/jas.2015-9645] [PMID: 27065116]
[49]
Anisman, H.; Hayley, S.; Kelly, O.; Borowski, T.; Merali, Z. Psychogenic, neurogenic, and systemic stressor effects on plasma corticosterone and behavior: Mouse strain-dependent outcomes. Behav. Neurosci., 2001, 115(2), 443-454.
[http://dx.doi.org/10.1037/0735-7044.115.2.443] [PMID: 11345969]
[50]
Sheriff, M.J.; Dantzer, B.; Delehanty, B.; Palme, R.; Boonstra, R. Measuring stress in wildlife: Techniques for quantifying glucocorticoids. Oecologia, 2011, 166(4), 869-887.
[http://dx.doi.org/10.1007/s00442-011-1943-y] [PMID: 21344254]
[51]
Palme, R.; Rettenbacher, S.; Touma, C.; El-Bahr, S.M.; Möstl, E. Stress hormones in mammals and birds: Comparative aspects regarding metabolism, excretion, and noninvasive measurement in fecal samples. Ann. N. Y. Acad. Sci., 2005, 1040(1), 162-171.
[http://dx.doi.org/10.1196/annals.1327.021] [PMID: 15891021]
[52]
Filiou, M.D.; Turck, C.W.; Martins-de-Souza, D. Quantitative proteomics for investigating psychiatric disorders. Proteomics Clin. Appl., 2011, 5(1-2), 38-49.
[http://dx.doi.org/10.1002/prca.201000060] [PMID: 21280236]
[53]
Filiou, M.D.; Martins-de-Souza, D.; Guest, P.C.; Bahn, S.; Turck, C.W. To label or not to label: Applications of quantitative proteomics in neuroscience research. Proteomics, 2012, 12(4-5), 736-747.
[http://dx.doi.org/10.1002/pmic.201100350] [PMID: 22247077]
[54]
Hernandez, L.M.; Kim, M.; Hoftman, G.D.; Haney, J.R.; de la Torre-Ubieta, L.; Pasaniuc, B.; Gandal, M.J. Transcriptomic insight into the polygenic mechanisms underlying psychiatric disorders. Biol. Psychiatry, 2021, 89(1), 54-64.
[http://dx.doi.org/10.1016/j.biopsych.2020.06.005] [PMID: 32792264]
[55]
Geschwind, D.H.; Flint, J. Genetics and genomics of psychiatric disease. Science, 2015, 349(6255), 1489-1494.
[http://dx.doi.org/10.1126/science.aaa8954] [PMID: 26404826]
[56]
von Ziegler, L.M.; Floriou-Servou, A.; Waag, R.; Das Gupta, R.R.; Sturman, O.; Gapp, K.; Maat, C.A.; Kockmann, T.; Lin, H.Y.; Duss, S.N.; Privitera, M.; Hinte, L.; von Meyenn, F.; Zeilhofer, H.U.; Germain, P.L.; Bohacek, J. Multiomic profiling of the acute stress response in the mouse hippocampus. Nat. Commun., 2022, 13(1), 1824.
[http://dx.doi.org/10.1038/s41467-022-29367-5] [PMID: 35383160]
[57]
Floriou-Servou, A.; von Ziegler, L.; Waag, R.; Schläppi, C.; Germain, P.L.; Bohacek, J. The acute stress response in the multiomic era. Biol. Psychiatry, 2021, 89(12), 1116-1126.
[http://dx.doi.org/10.1016/j.biopsych.2020.12.031] [PMID: 33722387]
[58]
Floriou-Servou, A.; von Ziegler, L.; Stalder, L.; Sturman, O.; Privitera, M.; Rassi, A.; Cremonesi, A.; Thöny, B.; Bohacek, J. Distinct proteomic, transcriptomic, and epigenetic stress responses in dorsal and ventral hippocampus. Biol. Psychiatry, 2018, 84(7), 531-541.
[http://dx.doi.org/10.1016/j.biopsych.2018.02.003] [PMID: 29605177]
[59]
Lopes, S.; Teplytska, L.; Vaz-Silva, J.; Dioli, C.; Trindade, R.; Morais, M.; Webhofer, C.; Maccarrone, G.; Almeida, O.F.X.; Turck, C.W.; Sousa, N.; Sotiropoulos, I.; Filiou, M.D. Tau deletion prevents stress-induced dendritic atrophy in prefrontal cortex: Role of synaptic mitochondria. Cereb. Cortex, 2017, 27(4), 2580-2591.
[PMID: 27073221]
[60]
van der Kooij, M.A.; Rojas-Charry, L.; Givehchi, M.; Wolf, C.; Bueno, D.; Arndt, S.; Tenzer, S.; Mattioni, L.; Treccani, G.; Hasch, A.; Schmeisser, M.J.; Vianello, C.; Giacomello, M.; Methner, A. Chronic social stress disrupts the intracellular redistribution of brain hexokinase 3 induced by shifts in peripheral glucose levels. J. Mol. Med., 2022, 100(10), 1441-1453.
[http://dx.doi.org/10.1007/s00109-022-02235-x] [PMID: 35943566]
[61]
Patti, G.J.; Yanes, O.; Siuzdak, G. Metabolomics: the apogee of the omics trilogy. Nat. Rev. Mol. Cell Biol., 2012, 13(4), 263-269.
[http://dx.doi.org/10.1038/nrm3314] [PMID: 22436749]
[62]
Griffiths, W.J.; Koal, T.; Wang, Y.; Kohl, M.; Enot, D.P.; Deigner, H.P. Targeted metabolomics for biomarker discovery. Angew. Chem. Int. Ed., 2010, 49(32), 5426-5445.
[http://dx.doi.org/10.1002/anie.200905579] [PMID: 20629054]
[63]
Schrimpe-Rutledge, A.C.; Codreanu, S.G.; Sherrod, S.D.; McLean, J.A. Untargeted metabolomics strategies—challenges and emerging directions. J. Am. Soc. Mass Spectrom., 2016, 27(12), 1897-1905.
[http://dx.doi.org/10.1007/s13361-016-1469-y] [PMID: 27624161]
[64]
Johnson, C.H.; Ivanisevic, J.; Siuzdak, G. Metabolomics: Beyond biomarkers and towards mechanisms. Nat. Rev. Mol. Cell Biol., 2016, 17(7), 451-459.
[http://dx.doi.org/10.1038/nrm.2016.25] [PMID: 26979502]
[65]
Emwas, A.H.; Roy, R.; McKay, R.T.; Tenori, L.; Saccenti, E.; Gowda, G.A.N.; Raftery, D.; Alahmari, F.; Jaremko, L.; Jaremko, M.; Wishart, D.S. NMR spectroscopy for metabolomics research. Metabolites, 2019, 9(7), 123.
[http://dx.doi.org/10.3390/metabo9070123] [PMID: 31252628]
[66]
Alseekh, S.; Aharoni, A.; Brotman, Y.; Contrepois, K.; D’Auria, J.; Ewald, J.; Ewald, C. J.; Fraser, P.D.; Giavalisco, P.; Hall, R.D.; Heinemann, M.; Link, H.; Luo, J.; Neumann, S.; Nielsen, J.; Perez de Souza, L.; Saito, K.; Sauer, U.; Schroeder, F.C.; Schuster, S.; Siuzdak, G.; Skirycz, A.; Sumner, L.W.; Snyder, M.P.; Tang, H.; Tohge, T.; Wang, Y.; Wen, W.; Wu, S.; Xu, G.; Zamboni, N.; Fernie, A.R. Mass spectrometry-based metabolomics: A guide for annotation, quantification and best reporting practices. Nat. Methods, 2021, 18(7), 747-756.
[http://dx.doi.org/10.1038/s41592-021-01197-1] [PMID: 34239102]
[67]
Humer, E.; Probst, T.; Pieh, C. Metabolomics in psychiatric disorders: What we learn from animal models. Metabolites, 2020, 10(2), 72.
[http://dx.doi.org/10.3390/metabo10020072] [PMID: 32079262]
[68]
Turck, C.W.; Filiou, M.D. What have mass spectrometry-based proteomics and metabolomics (Not) taught us about psychiatric disorders? Mol. Neuropsychiatry, 2015, 1(2), 69-75.
[PMID: 27602358]
[69]
Humer, E.; Pieh, C.; Probst, T. Metabolomic biomarkers in anxiety disorders. Int. J. Mol. Sci., 2020, 21(13), 4784.
[http://dx.doi.org/10.3390/ijms21134784] [PMID: 32640734]
[70]
Mellon, S.H.; Gautam, A.; Hammamieh, R.; Jett, M.; Wolkowitz, O.M. Metabolism, metabolomics, and inflammation in posttraumatic stress disorder. Biol. Psychiatry, 2018, 83(10), 866-875.
[http://dx.doi.org/10.1016/j.biopsych.2018.02.007] [PMID: 29628193]
[71]
Bot, M.; Milaneschi, Y.; Al-Shehri, T.; Amin, N.; Garmaeva, S.; Onderwater, G.L.J.; Pool, R.; Thesing, C.S.; Vijfhuizen, L.S.; Vogelzangs, N.; Arts, I.C.W.; Demirkan, A.; van Duijn, C.; van Greevenbroek, M.; van der Kallen, C.J.H.; Köhler, S.; Ligthart, L.; van den Maagdenberg, A.M.J.M.; Mook-Kanamori, D.O.; de Mutsert, R.; Tiemeier, H.; Schram, M.T.; Stehouwer, C.D.A.; Terwindt, G.M.; Willems van Dijk, K.; Fu, J.; Zhernakova, A.; Beekman, M.; Slagboom, P.E.; Boomsma, D.I.; Penninx, B.W.J.H.; Beekman, M.; Suchiman, H.E.D.; Deelen, J.; Amin, N.; Beulens, J.W.; van der Bom, J.A.; Bomer, N.; Demirkan, A.; van Hilten, J.A.; Meessen, J.M.T.A.; Pool, R.; Moed, M.H.; Fu, J.; Onderwater, G.L.J.; Rutters, F.; So-Osman, C.; van der Flier, W.M.; van der Heijden, A.A.W.A.; van der Spek, A.; Asselbergs, F.W.; Boersma, E.; Elders, P.M.; Geleijnse, J.M.; Ikram, M.A.; Kloppenburg, M.; Meulenbelt, I.; Mooijaart, S.P.; Nelissen, R.G.H.H.; Netea, M.G.; Penninx, B.W.J.H.; Stehouwer, C.D.A.; Teunissen, C.E.; Terwindt, G.M.; ’t Hart, L.M.; van den Maagdenberg, A.M.J.M.; van der Harst, P.; van der Horst, I.C.C.; van der Kallen, C.J.H.; van Greevenbroek, M.M.J.; van Spil, W.E.; Wijmenga, C.; Zwinderman, A.H.; Zhernikova, A.; Jukema, J.W.; Sattar, N. Metabolomics Profile in Depression: A Pooled Analysis of 230 Metabolic Markers in 5283 Cases With Depression and 10,145 Controls. Biol. Psychiatry, 2020, 87(5), 409-418.
[http://dx.doi.org/10.1016/j.biopsych.2019.08.016] [PMID: 31635762]
[72]
Filiou, M.D.; Teplytska, L.; Nussbaumer, M.; Otte, D.M.; Zimmer, A.; Turck, C.W. Multi-omics analysis reveals myelin, presynaptic and nicotinate alterations in the hippocampus of G72/G30 transgenic mice. J. Pers. Med., 2022, 12(2), 244.
[http://dx.doi.org/10.3390/jpm12020244] [PMID: 35207732]
[73]
Filiou, M.D.; Zhang, Y.; Teplytska, L.; Reckow, S.; Gormanns, P.; Maccarrone, G.; Frank, E.; Kessler, M.S.; Hambsch, B.; Nussbaumer, M.; Bunck, M.; Ludwig, T.; Yassouridis, A.; Holsboer, F.; Landgraf, R.; Turck, C.W. Proteomics and metabolomics analysis of a trait anxiety mouse model reveals divergent mitochondrial pathways. Biol. Psychiatry, 2011, 70(11), 1074-1082.
[http://dx.doi.org/10.1016/j.biopsych.2011.06.009] [PMID: 21791337]
[74]
Filiou, M.D.; Asara, J.M.; Nussbaumer, M.; Teplytska, L.; Landgraf, R.; Turck, C.W. Behavioral extremes of trait anxiety in mice are characterized by distinct metabolic profiles. J. Psychiatr. Res., 2014, 58, 115-122.
[http://dx.doi.org/10.1016/j.jpsychires.2014.07.019] [PMID: 25124548]
[75]
Zhang, Y.; Filiou, M.D.; Reckow, S.; Gormanns, P.; Maccarrone, G.; Kessler, M.S. Proteomic and metabolomic profiling of a trait anxiety mouse model implicate affected pathways. Mol. Cell. Proteomics, 2011, 10(12), M111-M008110.
[http://dx.doi.org/10.1074/mcp.M111.008110]
[76]
Weckmann, K.; Deery, M.J.; Howard, J.A.; Feret, R.; Asara, J.M.; Dethloff, F.; Filiou, M.D.; Iannace, J.; Labermaier, C.; Maccarrone, G.; Webhofer, C.; Teplytska, L.; Lilley, K.; Müller, M.B.; Turck, C.W. Ketamine’s antidepressant effect is mediated by energy metabolism and antioxidant defense system. Sci. Rep., 2017, 7(1), 15788.
[http://dx.doi.org/10.1038/s41598-017-16183-x] [PMID: 29150633]
[77]
Weckmann, K.; Deery, M.J.; Howard, J.A.; Feret, R.; Asara, J.M.; Dethloff, F.; Filiou, M.D.; Labermaier, C.; Maccarrone, G.; Lilley, K.S.; Mueller, M.; Turck, C.W. Ketamine’s effects on the glutamatergic and gabaergic systems: a proteomics and metabolomics study in mice. Mol. Neuropsychiatry, 2019, 5(1), 42-51.
[PMID: 31019917]
[78]
Park, D.I.; Dournes, C.; Sillaber, I.; Uhr, M.; Asara, J.M.; Gassen, N.C.; Rein, T.; Ising, M.; Webhofer, C.; Filiou, M.D.; Müller, M.B.; Turck, C.W. Purine and pyrimidine metabolism: Convergent evidence on chronic antidepressant treatment response in mice and humans. Sci. Rep., 2016, 6(1), 35317.
[http://dx.doi.org/10.1038/srep35317] [PMID: 27731396]
[79]
Park, D.I.; Dournes, C.; Sillaber, I.; Ising, M.; Asara, J.M.; Webhofer, C.; Filiou, M.D.; Müller, M.B.; Turck, C.W. Delineation of molecular pathway activities of the chronic antidepressant treatment response suggests important roles for glutamatergic and ubiquitin–proteasome systems. Transl. Psychiatry, 2017, 7(4), e1078.
[http://dx.doi.org/10.1038/tp.2017.39] [PMID: 28375208]
[80]
Nussbaumer, M.; Asara, J.M.; Teplytska, L.; Murphy, M.P.; Logan, A.; Turck, C.W.; Filiou, M.D. Selective mitochondrial targeting exerts anxiolytic effects in vivo. Neuropsychopharmacology, 2016, 41(7), 1751-1758.
[http://dx.doi.org/10.1038/npp.2015.341] [PMID: 26567514]
[81]
Du, Y.; Wei, J.; Zhang, Z.; Yang, X.; Wang, M.; Wang, Y.; Qi, X.; Zhao, L.; Tian, Y.; Guo, W.; Wang, Q.; Deng, W.; Li, M.; Lin, D.; Li, T.; Ma, X. Plasma metabolomics profiling of metabolic pathways affected by major depressive disorder. Front. Psychiatry, 2021, 12, 644555.
[http://dx.doi.org/10.3389/fpsyt.2021.644555] [PMID: 34646171]
[82]
Larrieu, T.; Cherix, A.; Duque, A.; Rodrigues, J.; Lei, H.; Gruetter, R.; Sandi, C. Hierarchical status predicts behavioral vulnerability and nucleus accumbens metabolic profile following chronic social defeat stress. Curr. Biol., 2017, 27(14), 2202-2210.e4.
[http://dx.doi.org/10.1016/j.cub.2017.06.027] [PMID: 28712571]
[83]
Son, H.; Baek, J.H.; Kang, J.S.; Jung, S.; Chung, H.J.; Kim, H.J. Acutely increased β-hydroxybutyrate plays a role in the prefrontal cortex to escape stressful conditions during the acute stress response. Biochem. Biophys. Res. Commun., 2021, 554, 19-24.
[http://dx.doi.org/10.1016/j.bbrc.2021.03.062] [PMID: 33774275]
[84]
Picard, M.; McEwen, B.S. Psychological stress and mitochondria: A systematic review. Psychosom. Med., 2018, 80(2), 141-153.
[http://dx.doi.org/10.1097/PSY.0000000000000545] [PMID: 29389736]
[85]
Picard, M.; McManus, M.J.; Gray, J.D.; Nasca, C.; Moffat, C.; Kopinski, P.K.; Seifert, E.L.; McEwen, B.S.; Wallace, D.C. Mitochondrial functions modulate neuroendocrine, metabolic, inflammatory, and transcriptional responses to acute psychological stress. Proc. Natl. Acad. Sci. USA, 2015, 112(48), E6614-E6623.
[http://dx.doi.org/10.1073/pnas.1515733112] [PMID: 26627253]
[86]
Teague, C.R.; Dhabhar, F.S.; Barton, R.H.; Beckwith-Hall, B.; Powell, J.; Cobain, M.; Singer, B.; McEwen, B.S.; Lindon, J.C.; Nicholson, J.K.; Holmes, E. Metabonomic studies on the physiological effects of acute and chronic psychological stress in Sprague-Dawley rats. J. Proteome Res., 2007, 6(6), 2080-2093.
[http://dx.doi.org/10.1021/pr060412s] [PMID: 17474765]
[87]
Daikhin, Y.; Yudkoff, M. Ketone bodies and brain glutamate and GABA metabolism. Dev. Neurosci., 1998, 20(4-5), 358-364.
[http://dx.doi.org/10.1159/000017331] [PMID: 9778572]
[88]
Nehlig, A. Brain uptake and metabolism of ketone bodies in animal models. Prostaglandins Leukot. Essent. Fatty Acids, 2004, 70(3), 265-275.
[http://dx.doi.org/10.1016/j.plefa.2003.07.006] [PMID: 14769485]
[89]
Sze, Y.; Gill, A.C.; Brunton, P.J. Sex-dependent changes in neuroactive steroid concentrations in the rat brain following acute swim stress. J. Neuroendocrinol., 2018, 30(11), e12644.
[http://dx.doi.org/10.1111/jne.12644] [PMID: 30194779]
[90]
Moreno-Rius, J. The cerebellum under stress. Front. Neuroendocrinol., 2019, 54, 100774.
[http://dx.doi.org/10.1016/j.yfrne.2019.100774] [PMID: 31348932]
[91]
Iliou, A.; Vlaikou, A.M.; Nussbaumer, M.; Benaki, D.; Mikros, E.; Gikas, E.; Filiou, M.D. Exploring the metabolomic profile of cerebellum after exposure to acute stress. Stress, 2021, 24(6), 952-964.
[http://dx.doi.org/10.1080/10253890.2021.1973997] [PMID: 34553679]
[92]
Bassett, S.A.; Young, W.; Fraser, K.; Dalziel, J.E.; Webster, J.; Ryan, L.; Fitzgerald, P.; Stanton, C.; Dinan, T.G.; Cryan, J.F.; Clarke, G.; Hyland, N.; Roy, N.C. Metabolome and microbiome profiling of a stress-sensitive rat model of gut-brain axis dysfunction. Sci. Rep., 2019, 9(1), 14026.
[http://dx.doi.org/10.1038/s41598-019-50593-3] [PMID: 31575902]
[93]
Shi, B.; Tian, J.; Xiang, H.; Guo, X.; Zhang, L.; Du, G.; Qin, X.A. 1H-NMR plasma metabonomic study of acute and chronic stress models of depression in rats. Behav. Brain Res., 2013, 241, 86-91.
[http://dx.doi.org/10.1016/j.bbr.2012.11.036] [PMID: 23219962]
[94]
Dulka, B.N.; Bourdon, A.K.; Clinard, C.T.; Muvvala, M.B.K.; Campagna, S.R.; Cooper, M.A. Metabolomics reveals distinct neurochemical profiles associated with stress resilience. Neurobiol. Stress, 2017, 7, 103-112.
[http://dx.doi.org/10.1016/j.ynstr.2017.08.001] [PMID: 28828396]
[95]
Geng, C.; Guo, Y.; Wang, C.; Liao, D.; Han, W.; Zhang, J.; Jiang, P. Systematic impacts of chronic unpredictable mild stress on metabolomics in rats. Sci. Rep., 2020, 10(1), 700.
[http://dx.doi.org/10.1038/s41598-020-57566-x] [PMID: 31959868]
[96]
Geng, C.; Qiao, Y.; Guo, Y.; Han, W.; Wu, B.; Wang, C.; Zhang, J.; Chen, D.; Yang, M.; Jiang, P. Integrated metabolomics and lipidomics profiling of hippocampus reveal metabolite biomarkers in a rat model of chronic unpredictable mild stress-induced depression. Ann. Transl. Med., 2019, 7(23), 781.
[http://dx.doi.org/10.21037/atm.2019.11.21] [PMID: 32042797]
[97]
Li, X.; Zhou, X.; Teng, T.; Fan, L.; Liu, X.; Xiang, Y.; Jiang, Y.; Xie, P.; Zhu, D. Multi-omics Analysis of the Amygdala in a Rat Chronic Unpredictable Mild Stress Model of Depression. Neuroscience, 2021, 463, 174-183.
[http://dx.doi.org/10.1016/j.neuroscience.2021.03.031] [PMID: 33836246]
[98]
Zhang, Y.; Yuan, S.; Pu, J.; Yang, L.; Zhou, X.; Liu, L.; Jiang, X.; Zhang, H.; Teng, T.; Tian, L.; Xie, P. Integrated metabolomics and proteomics analysis of hippocampus in a rat model of depression. Neuroscience, 2018, 371, 207-220.
[http://dx.doi.org/10.1016/j.neuroscience.2017.12.001] [PMID: 29237567]
[99]
Liu, L.; Zhou, X.; Zhang, Y.; Pu, J.; Yang, L.; Yuan, S.; Zhao, L.; Zhou, C.; Zhang, H.; Xie, P. Hippocampal metabolic differences implicate distinctions between physical and psychological stress in four rat models of depression. Transl. Psychiatry, 2018, 8(1), 4.
[http://dx.doi.org/10.1038/s41398-017-0018-1] [PMID: 29317595]
[100]
Ling-hu, T.; Liu, S.; Gao, Y.; Han, Y.; Tian, J.; Qin, X. Stable isotope-resolved metabolomics reveals the abnormal brain glucose catabolism in depression based on chronic unpredictable mild stress rats. J. Proteome Res., 2021, 20(7), 3549-3558.
[http://dx.doi.org/10.1021/acs.jproteome.1c00155] [PMID: 34077228]
[101]
Ni, Y.; Su, M.; Lin, J.; Wang, X.; Qiu, Y.; Zhao, A.; Chen, T.; Jia, W. Metabolic profiling reveals disorder of amino acid metabolism in four brain regions from a rat model of chronic unpredictable mild stress. FEBS Lett., 2008, 582(17), 2627-2636.
[http://dx.doi.org/10.1016/j.febslet.2008.06.040] [PMID: 18586036]
[102]
Duan, L.; Fan, R.; Li, T.; Yang, Z.; Hu, E.; Yu, Z.; Tian, J.; Luo, W.; Zhang, C. Metabolomics analysis of the prefrontal cortex in a rat chronic unpredictable mild stress model of depression. Front. Psychiatry, 2022, 13, 815211.
[http://dx.doi.org/10.3389/fpsyt.2022.815211] [PMID: 35370823]
[103]
Linghu, T.; Gao, Y.; Li, A.; Shi, B.; Tian, J.; Qin, X. A unique insight for energy metabolism disorders in depression based on chronic unpredictable mild stress rats using stable isotope-resolved metabolomics. J. Pharm. Biomed. Anal., 2020, 191, 113588.
[http://dx.doi.org/10.1016/j.jpba.2020.113588] [PMID: 32927418]
[104]
Wu, Q.; Xia, D.M.; Lan, F.; Wang, Y.K.; Tan, X.; Sun, J.C.; Wang, W.Z.; Wang, R.; Peng, X.D.; Liu, M. UPLC–QTOF/MS‐based metabolomics reveals the mechanism of chronic unpredictable mild stress‐induced hypertension in rats. Biomed. Chromatogr., 2019, 33(10), e4619.
[http://dx.doi.org/10.1002/bmc.4619] [PMID: 31177559]
[105]
Li, Z.; Gao, C.; Peng, J.; Liu, M.; Cong, B. Multi-omics analysis of pathological changes in the amygdala of rats subjected to chronic restraint stress. Behav. Brain Res., 2020, 392, 112735.
[http://dx.doi.org/10.1016/j.bbr.2020.112735] [PMID: 32502515]
[106]
Liu, L.; Zhou, X.; Zhang, Y.; Liu, Y.; Yang, L.; Pu, J.; Zhu, D.; Zhou, C.; Xie, P. The identification of metabolic disturbances in the prefrontal cortex of the chronic restraint stress rat model of depression. Behav. Brain Res., 2016, 305, 148-156.
[http://dx.doi.org/10.1016/j.bbr.2016.03.005] [PMID: 26947756]
[107]
Chen, S.; Lu, D.; Wang, W.; Chen, W.; Zhang, S.; Wei, S. Plasma metabolomic profiling of repeated restraint stress in rats. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci., 2020, 1160, 122294.
[http://dx.doi.org/10.1016/j.jchromb.2020.122294] [PMID: 32920479]
[108]
Hamilton, P.J.; Chen, E.Y.; Tolstikov, V.; Peña, C.J.; Picone, J.A.; Shah, P.; Panagopoulos, K.; Strat, A.N.; Walker, D.M.; Lorsch, Z.S.; Robinson, H.L.; Mervosh, N.L.; Kiraly, D.D.; Sarangarajan, R.; Narain, N.R.; Kiebish, M.A.; Nestler, E.J. Chronic stress and antidepressant treatment alter purine metabolism and beta oxidation within mouse brain and serum. Sci. Rep., 2020, 10(1), 18134.
[http://dx.doi.org/10.1038/s41598-020-75114-5] [PMID: 33093530]
[109]
Dudek, K.A.; Dion-Albert, L.; Lebel, M.; LeClair, K.; Labrecque, S.; Tuck, E.; Ferrer Perez, C.; Golden, S.A.; Tamminga, C.; Turecki, G.; Mechawar, N.; Russo, S.J.; Menard, C. Molecular adaptations of the blood–brain barrier promote stress resilience vs. depression. Proc. Natl. Acad. Sci., 2020, 117(6), 3326-3336.
[http://dx.doi.org/10.1073/pnas.1914655117] [PMID: 31974313]
[110]
Zhang, Y.; Lu, W.; Wang, Z.; Zhang, R.; Xie, Y.; Guo, S.; Jiao, L.; Hong, Y.; Di, Z.; Wang, G.; Aa, J. Reduced Neuronal cAMP in the nucleus accumbens damages blood-brain barrier integrity and promotes stress vulnerability. Biol. Psychiatry, 2020, 87(6), 526-537.
[http://dx.doi.org/10.1016/j.biopsych.2019.09.027] [PMID: 31812254]
[111]
Wang, W.; Guo, H.; Zhang, S.X.; Li, J.; Cheng, K.; Bai, S.J.; Yang, D.Y.; Wang, H.Y.; Liang, Z.H.; Liao, L.; Sun, L.; Xie, P. Targeted metabolomic pathway analysis and validation revealed glutamatergic disorder in the prefrontal cortex among the chronic social defeat stress mice model of depression. J. Proteome Res., 2016, 15(10), 3784-3792.
[http://dx.doi.org/10.1021/acs.jproteome.6b00577] [PMID: 27599184]
[112]
Xu, K.; He, Y.; Chen, X.; Tian, Y.; Cheng, K.; Zhang, L.; Wang, Y.; Yang, D.; Wang, H.; Wu, Z.; Li, Y.; Lan, T.; Dong, Z.; Xie, P. Validation of the targeted metabolomic pathway in the hippocampus and comparative analysis with the prefrontal cortex of social defeat model mice. J. Neurochem., 2019, 149(6), 799-810.
[http://dx.doi.org/10.1111/jnc.14641] [PMID: 30520040]
[113]
Yang, L.N.; Pu, J.C.; Liu, L.X.; Wang, G.W.; Zhou, X.Y.; Zhang, Y.Q.; Liu, Y.Y.; Xie, P. Integrated metabolomics and proteomics analysis revealed second messenger system disturbance in hippocampus of chronic social defeat stress rat. Front. Neurosci., 2019, 13, 247.
[http://dx.doi.org/10.3389/fnins.2019.00247] [PMID: 30983951]
[114]
Fan, L.; Yang, L.; Li, X.; Teng, T.; Xiang, Y.; Liu, X.; Jiang, Y.; Zhu, Y.; Zhou, X.; Xie, P. Proteomic and metabolomic characterization of amygdala in chronic social defeat stress rats. Behav. Brain Res., 2021, 412, 113407.
[http://dx.doi.org/10.1016/j.bbr.2021.113407] [PMID: 34111472]
[115]
Cui, Y.; Cao, K.; Lin, H.; Cui, S.; Shen, C.; Wen, W.; Mo, H.; Dong, Z.; Bai, S.; Yang, L.; Shi, Y.; Zhang, R. Early-life stress induces depression-like behavior and synaptic-plasticity changes in a maternal separation rat model: Gender difference and metabolomics study. Front. Pharmacol., 2020, 11, 102.
[http://dx.doi.org/10.3389/fphar.2020.00102] [PMID: 32174832]
[116]
Nitto, T.; Onodera, K. Linkage between coenzyme a metabolism and inflammation: Roles of pantetheinase. J. Pharmacol. Sci., 2013, 123(1), 1-8.
[http://dx.doi.org/10.1254/jphs.13R01CP] [PMID: 23978960]
[117]
Wojtczak, L.; Slyshenkov, V.S. Protection by pantothenic acid against apoptosis and cell damage by oxygen free radicals-the role of glutathione. Biofactors, 2003, 17(1-4), 61-73.
[http://dx.doi.org/10.1002/biof.5520170107] [PMID: 12897429]
[118]
Milakfsky, L.; Hare, T.A.; Miller, J.M.; Vogel, W.H. Rat plasma levels of amino acids and related compounds during stress. Life Sci., 1985, 36(8), 753-761.
[http://dx.doi.org/10.1016/0024-3205(85)90195-X] [PMID: 3974409]
[119]
Zhao, S.; Khoo, S.; Ng, S.C.; Chi, A. Brain functional network and amino acid metabolism association in females with subclinical depression. Int. J. Environ. Res. Public Health, 2022, 19(6), 3321.
[http://dx.doi.org/10.3390/ijerph19063321] [PMID: 35329007]
[120]
Meyer, J.H. Chapter 16 - Molecular imaging findings in bipolar disorder. In: Joao Quevedo AFC, Eduard Viet, editor; Neurobiology of bipolar disorder: Academic Press, 2021; p. 183-95.
[121]
Pu, J.; Liu, Y.; Gui, S.; Tian, L.; Yu, Y.; Song, X.; Zhong, X.; Chen, X.; Chen, W.; Zheng, P.; Zhang, H.; Gong, X.; Liu, L.; Wu, J.; Wang, H.; Xie, P. Metabolomic changes in animal models of depression: A systematic analysis. Mol. Psychiatry, 2021, 26(12), 7328-7336.
[http://dx.doi.org/10.1038/s41380-021-01269-w] [PMID: 34471249]
[122]
Liu, L.Y.; Zhang, H.J.; Luo, L.Y.; Pu, J.B.; Liang, W.Q.; Zhu, C.Q.; Li, Y.P.; Wang, P.R.; Zhang, Y.Y.; Yang, C.Y.; Zhang, Z.J. Blood and urinary metabolomic evidence validating traditional Chinese medicine diagnostic classification of major depressive disorder. Chin. Med., 2018, 13(1), 53.
[http://dx.doi.org/10.1186/s13020-018-0211-z] [PMID: 30386416]
[123]
Rosso, I.M.; Crowley, D.J.; Silveri, M.M.; Rauch, S.L.; Jensen, J.E. Hippocampus glutamate and n-acetyl aspartate markers of excitotoxic neuronal compromise in posttraumatic stress disorder. Neuropsychopharmacology, 2017, 42(8), 1698-1705.
[http://dx.doi.org/10.1038/npp.2017.32] [PMID: 28195577]
[124]
Duttaroy, A.K. Bioactive lipids and brain function: From their mechanistic roles to clinical trials; Evidence-based nutrition and clinical evidence of bioactive foods in human health and disease, 2021, p. 79-101.
[125]
Oliveira, T.G.; Chan, R.B.; Bravo, F.V.; Miranda, A.; Silva, R.R.; Zhou, B.; Marques, F.; Pinto, V.; Cerqueira, J.J.; Di Paolo, G.; Sousa, N. The impact of chronic stress on the rat brain lipidome. Mol. Psychiatry, 2016, 21(1), 80-88.
[http://dx.doi.org/10.1038/mp.2015.14] [PMID: 25754084]
[126]
Li, S.; Xu, Y.; Zheng, L.; Pang, H.; Zhang, Q.; Lou, L.; Huang, X. Sex difference in global burden of major depressive disorder: findings from the global burden of disease study 2019. Front. Psychiatry, 2022, 13, 789305.
[http://dx.doi.org/10.3389/fpsyt.2022.789305] [PMID: 35264985]
[127]
Filiou, M.D.; Nussbaumer, M.; Teplytska, L.; Turck, C.W. Behavioral and Metabolome Differences between C57BL/6 and DBA/2 Mouse Strains: Implications for Their Use as Models for Depression- and Anxiety-Like Phenotypes. Metabolites, 2021, 11(2), 128.
[http://dx.doi.org/10.3390/metabo11020128] [PMID: 33672326]
[128]
O’Mahony, C.M.; Clarke, G.; Gibney, S.; Dinan, T.G.; Cryan, J.F. Strain differences in the neurochemical response to chronic restraint stress in the rat: Relevance to depression. Pharmacol. Biochem. Behav., 2011, 97(4), 690-699.
[http://dx.doi.org/10.1016/j.pbb.2010.11.012] [PMID: 21110995]

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