Alterations in phospholipidomic profile in the brain of mouse model of depression induced by chronic unpredictable stress

Neuroscience

Volumn 273, Issue , 2014, Pages 1-11

  Faria, R ^a   Santana, M M ^d,e   Aveleira, C A ^e   Simoes C ^a   Maciel, E ^a   Melo, T ^a   Santinha, D ^a   Oliveira, M M ^b   Peixoto, F ^c   Domingues, P ^a   Cavadas, C ^d,e   Domingues, M R M ^a  

^a UNIVERSITY OF AVEIRO   (Portugal)

^b UNIVERSITY OF TRÁS OS MONTES AND ALTO DOURO   (Portugal)

^c UNIVERSITY OF TRÁS OS MONTES AND ALTO DOURO   (Portugal)

^d UNIVERSITY OF COIMBRA   (Portugal)

^e UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

Brain; Chronic stress; Lipidomic; Mass spectrometry; Oxidative stress; Phospholipids

Indexed keywords

CARDIOLIPIN; CATALASE; GLUTATHIONE; LIPID HYDROPEROXIDE; PHOSPHATIDYLINOSITOL; SUPEROXIDE DISMUTASE; GLUTATHIONE DISULFIDE; GLUTATHIONE REDUCTASE; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; PHOSPHOLIPID;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DAMAGE; CELL LOSS; CHRONIC STRESS; DEPRESSION; ENZYME ACTIVITY; HEART MUSCLE; LIPID OXIDATION; LIPID PEROXIDATION; LIPIDOMICS; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MOUSE; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CONTENT; ANIMAL; BRAIN; C57BL MOUSE; CHRONIC DISEASE; DISEASE MODEL; MALE; MENTAL STRESS; METABOLISM; OXIDATION REDUCTION REACTION; UNCERTAINTY;

ANIMALS; BRAIN; CARDIOLIPINS; CATALASE; CHRONIC DISEASE; DEPRESSIVE DISORDER; DISEASE MODELS, ANIMAL; GLUTATHIONE; GLUTATHIONE DISULFIDE; GLUTATHIONE REDUCTASE; MALE; MICE, INBRED C57BL; MYOCARDIUM; OXIDATION-REDUCTION; PHOSPHATIDYLCHOLINES; PHOSPHATIDYLETHANOLAMINES; PHOSPHATIDYLINOSITOLS; PHOSPHOLIPIDS; STRESS, PSYCHOLOGICAL; SUPEROXIDE DISMUTASE; UNCERTAINTY;

EID: 84901323540     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2014.04.042     Document Type: Article

References (73)

1. Adibhatla R.M., Hatcher J.F. Role of lipids in brain injury and diseases. Future Lipidol 2007, 2:403-422.
2. Adibhatla R.M., Hatcher J. Altered lipid metabolism in brain injury and disorders. Lipids Health Dis 2008, 241-268.
3. Adibhatla R.M., Hatcher J., Dempsey R. Lipids and lipidomics in brain injury and diseases. AAPS J 2006, 8:314-321.
4. Ahmad A., Rasheed N., Banu N., Palit G. Alterations in monoamine levels and oxidative systems in frontal cortex, striatum, and hippocampus of the rat brain during chronic unpredictable stress. Stress 2010, 13:356-365.
5. Bartlett E., Lewis D. Spectrophotometric determination of phosphate esters in the presence and absence of orthophosphate. Anal Biochem 1970, 36:159-167.
6. Bayir H., Tyurin V.A., Tyurina Y.Y., Viner R., Ritov V., Amoscato A.A., Zhao Q., Zhang X.J., Feldman K.L., Janesko, Alexander H. Selective early cardiolipin peroxidation after traumatic brain injury: an oxidative lipidomics analysis. Ann Neurol 2007, 62:154-169.
7. Black P.H. Stress and the inflammatory response: a review of neurogenic inflammation. Brain Behav Immun 2002, 16:622-653.
8. Black P.H., Garbutt L.D. Stress, inflammation and cardiovascular disease. J Psychosom Res 2002, 52:1-23.
9. Bligh E.G., Dyer W.G. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 1959, 37:911-917.
10. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254.
11. Chicco A.J., Sparagna G.C. Role of cardiolipin alterations in mitochondrial dysfunction and disease. Am J Physiol Cell Physiol 2007, 292:C33-C44.
12. Chrousos G.P. Stress and disorders of the stress system. Nat Rev Endocrinol 2009, 5:374-381.
13. Cohen J.I. Stress and mental health: a biobehavioral perspective. Issues Ment Health Nurs 2000, 21:185-202.
14. 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, 9:326-357.
15. David A.S., John F.C. Using the rat forced swim test to assess antidepressant-like activity in rodents. Nat Protoc 2012, 7:1009-1014.
16. Demirkan A., Isaacs A., Ugocsai P., Liebisch G., Struchalin M., et al. Plasma phosphatidylcholine and sphingomyelin concentrations are associated with depression and anxiety symptoms in a Dutch family-based lipidomics study. J Psychiatr Res 2013, 47:357-362.
17. Flerov M., Gerasimova I. Lipid peroxidation in several brain regions during development of post-stress depressions in rats with different strategies of adaptive behavior. Neurochem J 2007, 1:150-155.
18. Galhano V., Peixoto F., Gomes-Laranjo J. Bentazon triggers the promotion of oxidative damage in the Portuguese rice field cyanobacterium Anabaena cylindrica: Response of the antioxidant system. Environ Toxicol 2010, 25:517-526.
19. Giles N.M., Watts A.B., Giles G.I., Fry F.H., Littlechild J.A., Jacob C. Metal and redox modulation of cysteine protein function. Chem Biol 2003, 10:677-693.
20. Gonzalvez F., Gottlieb E. Cardiolipin: setting the beat of apoptosis. Apoptosis 2007, 12:877-885.
21. Gosney J.R. Adrenal corticomedullary hyperplasia in hypobaric hypoxia. J Pathol 1985, 146:59-64.
22. Hammen C., Kim E.Y., Eberhart N.K., Brennan P.A. Chronic and acute stress and the prediction of major depression in women. Depress Anxiety 2009, 26:718-723.
23. Han X. Multi-dimensional mass spectrometry-based shotgun lipidomics and the altered lipids at the mild cognitive impairment stage of Alzheimer's disease. Biochim Biophys Acta 2010, 1801(8):774-783.
24. Hicks A.M., DeLong C.J., Thomas M.J., Samuel M., Cui Z. Unique molecular signatures of glycerophospholipid species in different rat tissues analyzed by tandem mass spectrometry. Biochim Biophys Acta 2006, 1761:1022-1029.
25. Hill M.N., Hellemans K.G., Verma P., Gorzalka B.B., Weinberg J. Neurobiology of chronic mild stress: parallels to major depression. Neurosci Biobehav Rev 2012, 36:2085-2117.
26. Huynh T.N., Krigbaum A.M., Hanna J.J., Conrad C.D. Sex differences and phase of light cycle modify chronic stress effects on anxiety and depressive-like behavior. Behav Brain Res 2011, 222:212-222.
27. Ivanova P.T., Milne S.B., Myers D.S., Brown H.A. Lipidomics: a mass spectrometry based systems level analysis of cellular lipids. Curr Opin Chem Biol 2009, 13:526-531.
28. Jiang Z.Y., Woollard A.C.S., Wolff S.P. Lipid hydroperoxide measurement by oxidation of Fe 2+ in the presence of xylenol orange. Comparison with the TBA assay and an iodometric method. Lipids 1991, 26:853-856.
29. Joels M., Karst H., Alfarez D., Heine V.M., Qin Y., Riel E., Verkuyl M., Lucassen P.J., Krugers H.J. Effects of chronic stress on structure and cell function in rat hippocampus and hypothalamus. Stress 2004, 7:221-231.
30. Jones D.P. Redox potential of GSH/GSSG couple: assay and biological significance. Protein Sens React Oxygen Species B 2002, 348:93-112.
31. Katz R.J., Hersh S. Amitriptyline and scopolamine in an animal model of depression. Neurosci Biobehav Rev 1981, 5:265-271.
32. Kaushik S., Kaur J. Chronic cold exposure affects the antioxidant defense system in various rat tissues. Clin Chim Acta 2003, 333:69-77.
33. Kessler R.C. The effects of stressful life events on depression. Annu Rev Psychol 1997, 48:191-214.
34. Kim J., Minkler P.E., Salomon R.G., Anderson V.E., Hoppel C.L. Cardiolipin: characterization of distinct oxidized molecular species. J Lipid Res 2011, 52:125-135.
35. Kosicek M., Hecimovic S. Phospholipids and Alzheimer's disease: alterations, mechanisms and potential biomarkers. Int J Mol Sci 2013, 14:1310-1322.
36. Krishnan V., Nestler E.J. The molecular neurobiology of depression. Nature 2008, 455:894-902.
37. Liu J., Wang X., Shigenaga M., Yeo H., Mori A., Ames B. Immobilization stress causes oxidative damage to lipid, protein, and DNA in the brain of rats. FASEB J 1996, 10:1532.
38. Lucca G., Comim C.M., Valvassori S.S., Rus G.Z., Vuolo F., Petronilho F., Dal-Pizzol F., Gavioli E.C., Quevedo J. Effects of chronic mild stress on the oxidative parameters in the rat brain. Neurochem int 2009, 54:358-362.
39. Maciel E., Domingues P., Marques D., Simões C., Reis A., Oliveira M.M., Videira R.A., Peixoto F., Domingues M.R.M. Cardiolipin and oxidative stress: Identification of new short chain oxidation products of cardiolipin in in vitro analysis and in nephrotoxic drug-induced disturbances in rat kidney tissue. Int J Mass Spectrum 2011, 301:62-73.
40. Madrigal J.L.M., Olivenza R., Moro M.A., Lizasoain I., Lorenzo P., Rodrigo J., Leza J.C. Glutathione depletion, lipid peroxidation and mitochondrial dysfunction are induced by chronic stress in rat brain. Neuropsychopharmacology 2001, 24:420-429.
41. McGonagle K., Kessler R. Chronic stress, acute stress, and depressive symptoms. Am J Commun Psychol 1990, 18:681-706.
42. Michel T.M., Pülschen D., Thome J. The role of oxidative stress in depressive disorders. Curr Pharm Des 2012, 18:5890-5899.
43. Miller A.H. Depression and immunity: a role for T cells?. Brain Behav Immun 2010, 24:1-8.
44. Mitchell J.P., Vulliet P.R. Altered reactivity of the rat adrenal medulla following periods of chronic stress. Molecular mechanisms of neuronal responsiveness 1987, vol. 221:367-374. Springer, US.
45. Oliveira M.M., Teixeira J.C., Vasconcelos-Nóbrega C., Felix L.M., Sardão V.A., Colaço A.A., Oliveira P.A., Peixoto F.P. Mitochondrial and liver oxidative stress alterations induced by N-butyl-N-(4-hydroxybutyl)nitrosamine: relevance for hepatotoxicity. J Appl Toxicol 2013, 33:434-443.
46. Paradies G., Petrosillo G., Paradies V., Ruggiero F.M. Mitochondrial dysfunction in brain aging: role of oxidative stress and cardiolipin. Neurochem Int 2011, 58:447-457.
47. Paul H.B. Stress and the inflammatory response: a review of neurogenic inflammation. Brain Behav Immun 2002, 16:622-653.
48. Paykel E.S. Life events and affective disorders. Acta Psychiatr Scand 2003, 108:61-66.
49. Pereira V.H., Cerqueira J.J., Palha J.A., Sousa N. Stressed brain, diseased heart: a review on the pathophysiologic mechanisms of neurocardiology. Int J Cardiol 2012, 166:30-37.
50. Pope S, Land JM, Heales SJR (2008) Oxidative stress and mitochondrial dysfunction in neurodegeneration: cardiolipin a critical target? In: 15th European bioenergetic conference, pp 794-799 Dublin, Ireland: Elsevier Science Bv.
51. Sahin E., Gumuslu S. Alterations in brain antioxidant status, protein oxidation and lipid peroxidation in response to different stress models. Behav Brain Res 2004, 155:241-248.
52. Sahin E., Gumuslu S. Cold-stress-induced modulation of antioxidant defence: role of stressed conditions in tissue injury followed by protein oxidation and lipid peroxidation. Int J Biometeorol 2004, 48:165-171.
53. Salomon R.G. Structural identification and cardiovascular activities of oxidized phospholipids. Circ Res 2012, 111(7):930-946.
54. Samson J., Devi R.S., Ravindran R., Senthilvelan M. Effect of noise stress on free radical scavenging enzymes in brain. Environ Toxicol Pharmacol 2005, 20:142-148.
55. Scaria K.S., Premalatha L.S. Cold induced adrenal weight & volume changes in white rats. Indian J Exp Biol 1967, 5:256-257.
56. Schwalbe-Herrmann M., Willmann J., Leibfritz D. Separation of phospholipid classes by hydrophilic interaction chromatography detected by electrospray ionization mass spectrometry. J Chromatogr A 2010, 1217:5179-5183.
57. Smith I.K., Vierheller T.L., Thorne C.A. Assay of glutathione-reductase in crude tissue-homogenates using 5,5'-Dithiobis (2-nitrobenzoic acid). Anal Biochem 1988, 175:408-413.
58. Sparvero L.J., Amoscato A.A., Kochanek P.M., Pitt B.R., Kagan V.E., Bayir H. Mass-spectrometry based oxidative lipidomics and lipid imaging: applications in traumatic brain injury. J Neurochem 2010, 115:1322-1336.
59. Strekalova T., Spanagel R., Bartsch D., Henn F.A., Gass P. Stress-induced anhedonia in mice is associated with deficits in forced swimming and exploration. Neuropsychopharmacology 2004, 29:2007-2017.
60. Tyurin V.A., Tyurina Y.Y., Borisenko G.G., Sokolova T.V., Ritov V.B., Quinn P.J., Rose M., Kochanek P., Graham S.H., Kagan V.E. Oxidative stress following traumatic brain injury in rats. J Neurochem 2000, 75:2178-2189.
61. Tyurin V.A., Tyurina Y.Y., Feng W., Mnuskin A., Jiang J., Tang M., Zhang X., Zhao Q., Kochanek P.M., Clark R.S.B. Mass spectrometric characterization of phospholipids and their primary peroxidation products in rat cortical neurons during staurosporine induced apoptosis. J Neurochem 2008, 107:1614-1633.
62. Tyurin V.A., Tyurina Y.Y., Jung M.Y., Tungekar M.A., Wasserloos K.J., Bayir H., Greenberger J.S., Kochanek P.M., Shvedova A.A., Pitt B. Mass-spectrometric analysis of hydroperoxy-and hydroxy-derivatives of cardiolipin and phosphatidylserine in cells and tissues induced by pro-apoptotic and pro-inflammatory stimuli. J Chromatogr B 2009, 877:2863-2872.
63. Tyurina Y.Y., Tyurin V.A., Kapralova V.I., Wasserloos K., Mosher M., Epperly M.W., Greenberger J.S., Pitt B.R., Kagan V.E. Oxidative lipidomics of gama-radiation-induced lung injury: mass spectrometric characterization of cardiolipin and phosphatidylserine peroxidation. Radiat Res 2011, 175:610-621.
64. Ulrich-Lai Y.M., Figueiredo H.F., Ostrander M.M., Choi D.C., Engeland W.C., Herman J.P. Chronic stress induces adrenal hyperplasia and hypertrophy in a subregion-specific manner. Am J Physiol Endocrinol Metab 2006, 291:E965-E973.
65. Van de Velde M., DeWolff M., Leather H.A., Wouters P.F. Effects of lipids on the functional and metabolic recovery from global myocardial stunning in isolated rabbit hearts. Cardiovasc Res 2000, 48:129-137.
66. WHO (2008) The global burdens of disease: 2004 update. World Health Organization.
67. Wielgat P., Walesiuk A., Braszko J.J. Effects of chronic stress and corticosterone on sialidase activity in the rat hippocampus. Behav Brain Res 2011, 222:363-367.
68. Willner P. Validity, reliability and utility of the chronic mild stress model of depression: a 10-year review and evaluation. Psychopharmacology (Berl) 1997, 134:319-329.
69. Willner P. Chronic mild stress (CMS) revisited: consistency and behavioural-neurobiological concordance in the effects of CMS. Neuropsychobiology 2005, 52:90-110.
70. Willner P., Towell A., Sampson D., Sophokleous S., Muscat R. Reduction of sucrose preference by chronic unpredictable mild stress, and its restoration by a tricyclic antidepressant. Psychopharmacology (Berl) 1987, 93:358-364.
71. Woodcock E.A., Kistler P.M., Ju Y.K. Phosphoinositide signalling and cardiac arrhythmias. Cardiovasc Res 2009, 82:286-295.
72. Wymann M.P., Schneiter R. Lipid signalling in disease. Nat Rev Mol Cell Biol 2008, 9:162-176.
73. Zafir A., Banu N. Modulation of in vivo oxidative status by exogenous corticosterone and restraint stress in rats. Stress 2009, 12:167-177.