Metabolomics reveals distinct neurochemical profiles associated with stress resilience

Neurobiology of Stress

Volumn 7, Issue , 2017, Pages 103-112

  Dulka, Brooke N ^a   Bourdon, Allen K ^a   Clinard, Catherine T ^a   Muvvala, Mohan B K ^a   Campagna, Shawn R ^a   Cooper, Matthew A ^a  

^a UNIVERSITY OF TENNESSEE   (United States)

Author keywords

Biomarkers; Metabolomics; Oxidative stress; Resilience; Social defeat; Stress

Indexed keywords

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASOLATERAL AMYGDALA; CENTRAL NUCLEUS (AMYGDALA); CONTROLLED STUDY; DOMINANT-SUBORDINATE RELATIONSHIP; DORSAL HIPPOCAMPUS; MALE; MASS SPECTROMETRY; METABOLOME; METABOLOMICS; MOUSE; NEUROCHEMISTRY; NONHUMAN; NUCLEUS ACCUMBENS; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PSYCHOLOGICAL RESILIENCE; SOCIAL INTERACTION TEST; SOCIAL STRESS; SYRIAN HAMSTER; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY; VENTROMEDIAL PREFRONTAL CORTEX;

EID: 85026872408     PISSN: None     EISSN: 23522895     Source Type: Journal    
DOI: 10.1016/j.ynstr.2017.08.001     Document Type: Article

References (87)

1. Abelson, J.L., Khan, S., Liberzon, I., Young, E.A., HPA axis activity in patients with panic disorder: review and synthesis of four studies. Depress. Anxiety 24 (2007), 66–76.
2. Albrecht, P., Bouchachia, I., Goebels, N., Henke, N., Hofstetter, H.H., Issberner, A., Kovacs, Z., Lewerenz, J., Lisak, D., Maher, P., Effects of dimethyl fumarate on neuroprotection and immunomodulation. J. Neuroinflammation 9 (2012), 2094–2099.
3. Altmaier, E., Ramsay, S.L., Graber, A., Mewes, H.-W., Weinberger, K.M., Suhre, K., Bioinformatics analysis of targeted metabolomics—uncovering old and new tales of diabetic mice under medication. Endocrinology 149 (2008), 3478–3489.
4. Álvarez-Diduk, R.n., Galano, A., Tan, D.X., Reiter, R.J., N-Acetylserotonin and 6-hydroxymelatonin against oxidative stress: implications for the overall protection exerted by melatonin. J. Phys. Chem. B 119 (2015), 8535–8543.
5. Armagan, G., Kanıt, L., Yalcin, A., D-serine treatment induces oxidative stress in rat brain. Drug Chem. Toxicol. 34 (2011), 129–138.
6. Babizhayev, M.A., Deyev, A.I., Yermakova, V.N., Semiletov, Y.A., Davydova, N.G., Kurysheva, N.I., Zhukotskii, A.V., Goldman, I.M., N-Acetylcarnosine, a natural histidine-containing dipeptide, as a potent ophthalmic drug in treatment of human cataracts. Peptides 22 (2001), 979–994.
7. Babizhayev, M.A., Seguin, M.C., Gueyne, J., Evstigneeva, R.P., Ageyeva, E.A., Zheltukhina, G.A., L-carnosine (β-alanyl-L-histidine) and carcinine (β-alanylhistamine) act as natural antioxidants with hydroxyl-radical-scavenging and lipid-peroxidase activities. Biochem. J. 304 (1994), 509–516.
8. Bado, P., Madeira, C., Vargas-Lopes, C., Moulin, T.C., Wasilewska-Sampaio, A.P., Maretti, L., de Oliveira, R.V., Amaral, O.B., Panizzutti, R., Effects of low-dose D-serine on recognition and working memory in mice. Psychopharmacology 218 (2011), 461–470.
9. Baker, D.G., Nievergelt, C.M., O'Connor, D.T., Biomarkers of PTSD: neuropeptides and immune signaling. Neuropharmacology 62 (2012), 663–673.
10. Barsacchi, R., Kusmic, C., Damiani, E., Carloni, P., Greci, L., Donato, L., Vitamin E consumption induced by oxidative stress in red blood cells is enhanced by melatonin and reduced by N-Acetylserotonin. Free Radic. Biol. Med. 24 (1998), 1187–1192.
11. Beery, A.K., Zucker, I., Sex bias in neuroscience and biomedical research. Neurosci. Biobehav. Rev. 35 (2011), 565–572.
12. Bekker, M.H., van Mens-Verhulst, J., Anxiety disorders: sex differences in prevalence, degree, and background, but gender-neutral treatment. Gend. Med. 4 (2007), S178–S193.
13. Berton, O., McClung, C.A., Dileone, R.J., Krishnan, V., Renthal, W., Russo, S.J., Graham, D., Tsankova, N.M., Bolanos, C.A., Rios, M., Monteggia, L.M., Self, D.W., Nestler, E.J., Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 311 (2006), 864–868.
14. Bianchi, L., Ballini, C., Colivicchi, M., Della Corte, L., Giovannini, M., Pepeu, G., Investigation on acetylcholine, aspartate, glutamate and GABA extracellular levels from ventral hippocampus during repeated exploratory activity in the rat. Neurochem. Res. 28 (2003), 565–573.
15. Bridges, R., Lutgen, V., Lobner, D., Baker, D.A., Thinking outside the cleft to understand synaptic activity: contribution of the cystine-glutamate antiporter (system xc−) to normal and pathological glutamatergic signaling. Pharmacol. Rev. 64 (2012), 780–802.
16. Charney, D.S., Psychobiological mechanisms of resilience and vulnerability: implications for successful adaptation to extreme stress. Am. J. Psychiatry 161 (2004), 195–216.
17. Charuvastra, A., Cloitre, M., Social bonds and posttraumatic stress disorder. Annu. Rev. Psychol., 59, 2008, 301.
18. Clinard, C.T., Bader, L.R., Sullivan, M.A., Cooper, M.A., Activation of 5-HT2a receptors in the basolateral amygdala promotes defeat-induced anxiety and the acquisition of conditioned defeat in Syrian hamsters. Neuropharmacology 90 (2015), 102–112.
19. Collingridge, G.L., Volianskis, A., Bannister, N., France, G., Hanna, L., Mercier, M., Tidball, P., Fang, G., Irvine, M.W., Costa, B.M., The NMDA receptor as a target for cognitive enhancement. Neuropharmacology 64 (2013), 13–26.
20. Davis, M., Ressler, K., Rothbaum, B.O., Richardson, R., Effects of D-cycloserine on extinction: translation from preclinical to clinical work. Biol. psychiatry 60 (2006), 369–375.
21. Day, D.E., Cooper, M.A., Markham, C.M., Huhman, K.L., NR2B subunit of the NMDA receptor in the basolateral amygdala is necessary for the acquisition of conditioned defeat in Syrian hamsters. Behav. Brain Res. 217 (2011), 55–59.
22. De Groote, L., Linthorst, A., Exposure to novelty and forced swimming evoke stressor-dependent changes in extracellular GABA in the rat hippocampus. Neuroscience 148 (2007), 794–805.
23. Dulka, B.N., Ford, E.C., Lee, M.A., Donnell, N.J., Goode, T.D., Prosser, R., Cooper, M.A., Proteolytic cleavage of proBDNF into mature BDNF in the basolateral amygdala is necessary for defeat-induced social avoidance. Learn. Mem. 23 (2016), 156–160.
24. Dulka, B.N., Lynch, J.F. III, Latsko, M.S., Mulvany, J.L., Jasnow, A.M., Phenotypic responses to social defeat are associated with differences in cued and contextual fear discrimination. Behav. Process. 118 (2015), 115–122.
25. Feder, A., Nestler, E.J., Charney, D.S., Psychobiology and molecular genetics of resilience. Nat. Rev. Neurosci. 10 (2009), 446–457.
26. García-Ruiz, C., Colell, A., Morales, A., Kaplowitz, N., Fernández-Checa, J.C., Role of oxidative stress generated from the mitochondrial electron transport chain and mitochondrial glutathione status in loss of mitochondrial function and activation of transcription factor nuclear factor-kappa B: studies with isolated mitochondria and rat hepatocytes. Mol. Pharmacol. 48 (1995), 825–834.
27. Golden, S.A., Covington, H.E. III, Berton, O., Russo, S.J., A standardized protocol for repeated social defeat stress in mice. Nat. Protoc. 6 (2011), 1183–1191.
28. Gonçalves, L., Dafre, A.L., Carobrez, S.G., Gasparotto, O.C., A temporal analysis of the relationships between social stress, humoral immune response and glutathione-related antioxidant defenses. Behav. Brain Res. 192 (2008), 226–231.
29. Gray, C., Norvelle, A., Larkin, T., Huhman, K., Dopamine in the nucleus accumbens modulates the memory of social defeat in Syrian hamsters (Mesocricetus auratus). Behav. Brain Res. 286 (2015), 22–28.
30. Greenberg, G.D., Laman-Maharg, A., Campi, K.L., Voigt, H., Orr, V.N., Schaal, L., Trainor, B.C., Sex differences in stress-induced social withdrawal: role of brain derived neurotrophic factor in the bed nucleus of the stria terminalis. Front. Behav. Neurosci., 7, 2013.
31. Griffiths, W., Karu, K., Hornshaw, M., Woffendin, G., Wang, Y., Metabolomics and metabolite profiling: past heroes and future developments. Eur. J. Mass Spectrom. 13 (2007), 45–50.
32. Gülçin, I., Comparison of in vitro antioxidant and antiradical activities of L-tyrosine and L-Dopa. Amino acids 32 (2007), 431–438.
33. Hamada-Kanazawa, M., Narahara, M., Takano, M., Min, K.S., Tanaka, K., Miyake, M., β-Citryl-L-glutamate acts as an iron carrier to activate aconitase activity. Biol. Pharm. Bull. 34 (2011), 1455–1464.
34. Heim, C., Newport, D.J., Mletzko, T., Miller, A.H., Nemeroff, C.B., The link between childhood trauma and depression: insights from HPA axis studies in humans. Psychoneuroendocrinology 33 (2008), 693–710.
35. Huhman, K.L., Solomon, M.B., Janicki, M., Harmon, A.C., Lin, S.M., Israel, J.E., Jasnow, A.M., Conditioned defeat in male and female Syrian hamsters. Horm. Behav. 44 (2003), 293–299.
36. Jang, S.-W., Liu, X., Pradoldej, S., Tosini, G., Chang, Q., Iuvone, P.M., Ye, K., N-acetylserotonin activates TrkB receptor in a circadian rhythm. Proc. Natl. Acad. Sci. 107 (2010), 3876–3881.
37. Jasnow, A.M., Huhman, K.L., Activation of GABA A receptors in the amygdala blocks the acquisition and expression of conditioned defeat in Syrian hamsters. Brain Res. 920 (2001), 142–150.
38. Jasnow, A.M., Shi, C., Israel, J.E., Davis, M., Huhman, K.L., Memory of social defeat is facilitated by cAMP response element-binding protein overexpression in the amygdala. Behav. Neurosci. 119 (2005), 1125–1130.
39. Kaddurah-Daouk, R., Kristal, B.S., Weinshilboum, R.M., Metabolomics: a global biochemical approach to drug response and disease. Annu. Rev. Pharmacol. Toxicol. 48 (2008), 653–683.
40. Kessler, R.C., Epidemiology of women and depression. J. Affect. Disord. 74 (2003), 5–13.
41. Krishnan, V., Han, M.H., Graham, D.L., Berton, O., Renthal, W., Russo, S.J., Laplant, Q., Graham, A., Lutter, M., Lagace, D.C., Ghose, S., Reister, R., Tannous, P., Green, T.A., Neve, R.L., Chakravarty, S., Kumar, A., Eisch, A.J., Self, D.W., Lee, F.S., Tamminga, C.A., Cooper, D.C., Gershenfeld, H.K., Nestler, E.J., Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell 131 (2007), 391–404.
42. Kudryavtseva, N., Experience of defeat decreases the behavioural reactivity to conspecifics in the partition test. Behav. Process. 32 (1994), 297–304.
43. Linker, R.A., Lee, D.-H., Ryan, S., van Dam, A.M., Conrad, R., Bista, P., Zeng, W., Hronowsky, X., Buko, A., Chollate, S., Fumaric acid esters exert neuroprotective effects in neuroinflammation via activation of the Nrf2 antioxidant pathway. Brain 134 (2011), 678–692.
44. Lu, W., Clasquin, M.F., Melamud, E., Amador-Noguez, D., Caudy, A.A., Rabinowitz, J.D., Metabolomic analysis via reversed-phase ion-pairing liquid chromatography coupled to a stand alone orbitrap mass spectrometer. Anal. Chem. 82 (2010), 3212–3221.
45. Luo, S., Levine, R.L., Methionine in proteins defends against oxidative stress. FASEB J. 23 (2009), 464–472.
46. Markham, C.M., Luckett, C.A., Huhman, K.L., The medial prefrontal cortex is both necessary and sufficient for the acquisition of conditioned defeat. Neuropharmacology 62 (2012), 933–939.
47. Markham, C.M., Taylor, S.L., Huhman, K.L., Role of amygdala and hippocampus in the neural circuit subserving conditioned defeat in Syrian hamsters. Learn Mem. 17 (2010), 109–116.
48. McCann, K.E., Bicknese, C.N., Norvelle, A., Huhman, K.L., Effects of inescapable versus escapable social stress in Syrian hamsters: the importance of stressor duration versus escapability. Physiol. Behav. 129 (2014), 25–29.
49. Meduri, J.D., Farnbauch, L.A., Jasnow, A.M., Paradoxical enhancement of fear expression and extinction deficits in mice resilient to social defeat. Behav. Brain Res. 256 (2013), 580–590.
50. Meerlo, P., Overkamp, G., Daan, S., Van Den Hoofdakker, R., Koolhaas, J., Changes in behaviour and body weight following a single or double social defeat in rats. Stress 1 (1996), 21–32.
51. Meewisse, M.L., Reitsma, J.B., de Vries, G.J., Gersons, B.P., Olff, M., Cortisol and post-traumatic stress disorder in adults: systematic review and meta-analysis. Br. J. Psychiatry 191 (2007), 387–392.
52. Melamud, E., Vastag, L., Rabinowitz, J.D., Metabolomic analysis and visualization engine for LC− MS data. Anal. Chem. 82 (2010), 9818–9826.
53. Minichiello, L., TrkB signalling pathways in LTP and learning. Nat. Rev. Neurosci. 10 (2009), 850–860.
54. Miyake, M., Kakimoto, Y., Sorimachi, M., Isolation and identification of β-citryl-L-glutamic acid from newborn rat brain. Biochimica Biophysica Acta (BBA)-General Subj. 544 (1978), 656–666.
55. Morrison, K.E., Bader, L.R., Clinard, C.T., Gerhard, D.M., Gross, S.E., Cooper, M.A., Maintenance of dominance status is necessary for resistance to social defeat stress in Syrian hamsters. Behav. Brain Res. 270 (2014), 277–286.
56. Morrison, K.E., Bader, L.R., McLaughlin, C.N., Cooper, M.A., Defeat-induced activation of the ventral medial prefrontal cortex is necessary for resistance to conditioned defeat. Behav. Brain Res. 243 (2013), 158–164.
57. Morrison, K.E., Swallows, C.L., Cooper, M.A., Effects of dominance status on conditioned defeat and expression of 5-HT1A and 5-HT2A receptors. Physiol. Behav. 104 (2011), 283–290.
58. Mothet, J.-P., Parent, A.T., Wolosker, H., Brady, R.O., Linden, D.J., Ferris, C.D., Rogawski, M.A., Snyder, S.H., D-serine is an endogenous ligand for the glycine site of the N-methyl-D-aspartate receptor. Proc. Natl. Acad. Sci. 97 (2000), 4926–4931.
59. Murphy, Michael P., How mitochondria produce reactive oxygen species. Biochem. J. 417 (2009), 1–13.
60. Nandi, D., Patra, R., Swarup, D., Effect of cysteine, methionine, ascorbic acid and thiamine on arsenic-induced oxidative stress and biochemical alterations in rats. Toxicology 211 (2005), 26–35.
61. Nestler, E.J., Hyman, S.E., Animal models of neuropsychiatric disorders. Nat. Neurosci. 13 (2010), 1161–1169.
62. Oldiges, M., Lütz, S., Pflug, S., Schroer, K., Stein, N., Wiendahl, C., Metabolomics: current state and evolving methodologies and tools. Appl. Microbiol. Biotechnol. 76 (2007), 495–511.
63. Ouyang, Y.-B., Giffard, R.G., Changes in astrocyte mitochondrial function with stress: effects of Bcl-2 family proteins. Neurochem. Int. 45 (2004), 371–379.
64. Patra, R., Swarup, D., Dwivedi, S., Antioxidant effects of α tocopherol, ascorbic acid and L-methionine on lead induced oxidative stress to the liver, kidney and brain in rats. Toxicology 162 (2001), 81–88.
65. Peaston, A.E., Whitelaw, E., Epigenetics and phenotypic variation in mammals. Mamm. Genome 17 (2006), 365–374.
66. Reinstein, D.K., Lehnert, H., Scott, N.A., Wurtman, R.J., Tyrosine prevents behavioral and neurochemical correlates of an acute stress in rats. Life Sci. 34 (1984), 2225–2231.
67. Reinstein, D.K., Lehnert, H., Wurtman, R.J., Dietary tyrosine suppresses the rise in plasma corticosterone following acute stress in rats. Life Sci. 37 (1985), 2157–2163.
68. Reissner, K.J., The cystine/glutamate antiporter: when too much of a good thing goes bad. J. Clin. Investig., 124, 2014, 3279.
69. Ribble, D.O., Salvioni, M., Social organization and nest co-occupancy in Peromyscus californicus, a monogamous rodent. Behav. Ecol. Sociobiol. 26 (1990), 9–15.
70. Russo, S.J., Murrough, J.W., Han, M.H., Charney, D.S., Nestler, E.J., Neurobiology of resilience. Nat. Neurosci. 15 (2012), 1475–1484.
71. Schulz, J.B., Lindenau, J., Seyfried, J., Dichgans, J., Glutathione, oxidative stress and neurodegeneration. Eur. J. Biochem. 267 (2000), 4904–4911.
72. Seki, H., Nakazato, K., Hamada-Sato, N., Adenosine monophosphate degradation and inosinic acid accumulation in the shrimp Penaeus japonicus. Int. Aquat. Res., 9, 2017, 37.
73. Shih, A.Y., Erb, H., Sun, X., Toda, S., Kalivas, P.W., Murphy, T.H., Cystine/glutamate exchange modulates glutathione supply for neuroprotection from oxidative stress and cell proliferation. J. Neurosci. 26 (2006), 10514–10523.
74. Suhre, K., Shin, S.-Y., Petersen, A.-K., Mohney, R.P., Meredith, D., Wagele, B., Altmaier, E., CardioGram, Deloukas P., Erdmann, J., Grundberg, E., Hammond, C.J., de Angelis, M.H., Kastenmuller, G., Kottgen, A., Kronenberg, F., Mangino, M., Meisinger, C., Meitinger, T., Mewes, H.-W., Milburn, M.V., Prehn, C., Raffler, J., Ried, J.S., Romisch-Margl, W., Samani, N.J., Small, K.S., Erich Wichmann, H., Zhai, G., Illig, T., Spector, T.D., Adamski, J., Soranzo, N., Gieger, C., Human metabolic individuality in biomedical and pharmaceutical research. Nature 477 (2011), 54–60.
75. Taylor, S., Fedoroff, I.C., Koch, W.J., Thordarson, D.S., Fecteau, G., Nicki, R.M., Posttraumatic stress disorder arising after road traffic collisions: patterns of response to cognitive–behavior therapy. J. Consult. Clin. Psychol., 69, 2001, 541.
76. Trainor, B.C., Stress responses and the mesolimbic dopamine system: social contexts and sex differences. Horm. Behav. 60 (2011), 457–469.
77. Tretter, L., Adam-Vizi, V., Inhibition of Krebs cycle enzymes by hydrogen peroxide: a key role of α-ketoglutarate dehydrogenase in limiting NADH production under oxidative stress. J. Neurosci. 20 (2000), 8972–8979.
78. Vialou, V., Bagot, R.C., Cahill, M.E., Ferguson, D., Robison, A.J., Dietz, D.M., Fallon, B., Mazei-Robison, M., Ku, S.M., Harrigan, E., Prefrontal cortical circuit for depression-and anxiety-related behaviors mediated by cholecystokinin: role of ΔFosB. J. Neurosci. 34 (2014), 3878–3887.
79. Weissbach, H., Redfield, B.G., Axelrod, J., Biosynthesis of melatonin: enzymic conversion of serotonin to N-acetylserotonin. Biochimica Biophhys. acta 43 (1960), 352–353.
80. Wishart, D.S., Jewison, T., Guo, A.C., Wilson, M., Knox, C., Liu, Y., Djoumbou, Y., Mandal, R., Aziat, F., Dong, E., Bouatra, S., Sinelnikov, I., Arndt, D., Xia, J., Liu, P., Yallou, F., Bjorndahl, T., Perez-Pineiro, R., Eisner, R., Allen, F., Neveu, V., Greiner, R., Scalbert, A., HMDB 3.0—the human metabolome Database in 2013. Nucleic Acids Res. 41 (2013), D801–D807.
81. Wong, A.H., Gottesman, I.I., Petronis, A., Phenotypic differences in genetically identical organisms: the epigenetic perspective. Hum. Mol. Genet. 14 (2005), R11–R18.
82. Wutzke, K.D., Lorenz, H., The effect of l-carnitine on fat oxidation, protein turnover, and body composition in slightly overweight subjects. Metabolism 53 (2004), 1002–1006.
83. Xia, J., Psychogios, N., Young, N., Wishart, D.S., MetaboAnalyst: a web server for metabolomic data analysis and interpretation. Nucleic Acids Res. 37 (2009), W652–W660.
84. Yehuda, R., Neylan, T.C., Flory, J.D., McFarlane, A.C., The use of biomarkers in the military: from theory to practice. Psychoneuroendocrinology 38 (2013), 1912–1922.
85. Yen, G.-C., Hsieh, C.-L., Antioxidant effects of dopamine and related compounds. Biosci. Biotechnol. Biochem. 61 (1997), 1646–1649.
86. Yoo, D.Y., Nam, S.M., Kim, W., Lee, C.H., Won, M.-H., Hwang, I.K., Yoon, Y.S., N-acetylserotonin increases cell proliferation and differentiating neuroblasts with tertiary dendrites through upregulation of brain-derived neurotrophic factor in the mouse dentate gyrus. J. Veterinary Med. Sci. 73 (2011), 1411–1416.
87. Zoladz, P.R., Diamond, D.M., Current status on behavioral and biological markers of PTSD: a search for clarity in a conflicting literature. Neurosci. Biobehav. Rev. 37 (2013), 860–895.