Elevated plasma F2-isoprostane levels in schizophrenia

Schizophrenia Research

Volumn 176, Issue 2-3, 2016, Pages 320-326

  Lee, Ellen E ^a   Eyler, Lisa T ^a,b   Wolkowitz, Owen M ^c   Martin, Averria Sirkin ^a,d   Reuter, Chase ^a,d   Kraemer, Helena ^e   Jeste, Dilip V ^a,d,f  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d University of California San Diego School of Medicine   (United States)

^e STANFORD UNIVERSITY   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Aging; Body mass index; F2 isoprostanes; Gender; Oxidative stress; Schizophrenia

Indexed keywords

ISOPROSTANE DERIVATIVE; BIOLOGICAL MARKER;

ADULT; AGED; AGING; ARTICLE; BLOOD LEVEL; BODY MASS; COMORBIDITY; CONTROLLED STUDY; DISEASE SEVERITY; EXECUTIVE FUNCTION; FEMALE; GOLD STANDARD; HUMAN; IN VIVO STUDY; MAJOR CLINICAL STUDY; MALE; MORTALITY; OUTPATIENT; OXIDATIVE STRESS; PHYSICAL PERFORMANCE; PRIORITY JOURNAL; SCHIZOPHRENIA; SEX DIFFERENCE; BLOOD; CROSS-SECTIONAL STUDY; MIDDLE AGED; PHYSIOLOGY; PSYCHOSIS;

ADULT; AGED; AGING; BIOMARKERS; BODY MASS INDEX; CROSS-SECTIONAL STUDIES; F2-ISOPROSTANES; FEMALE; HUMANS; MALE; MIDDLE AGED; OXIDATIVE STRESS; PSYCHOTIC DISORDERS; SCHIZOPHRENIA;

EID: 84995579379     PISSN: 09209964     EISSN: 15732509     Source Type: Journal    
DOI: 10.1016/j.schres.2016.06.011     Document Type: Article

References (82)

1. Abdalla, D.S., Monteiro, H.P., Oliveira, J.A., Bechara, E.J., Activities of superoxide dismutase and glutathione peroxidase in schizophrenic and manic-depressive patients. Clin. Chem. 32:5 (1986), 805–807.
2. Akyol, O., Herken, H., Uz, E., Fadillioglu, E., Unal, S., Sogut, S., Ozyurt, H., Savas, H.A., The indices of endogenous oxidative and antioxidative processes in plasma from schizophrenic patients. The possible role of oxidant/antioxidant imbalance. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 26:5 (2002), 995–1005.
3. Al-Asmari, A.K., Khan, M.W., Inflammation and schizophrenia: alterations in cytokine levels and perturbation in antioxidative defense systems. Hum. Exp. Toxicol. 33:2 (2014), 115–122.
4. Aleman, A., Kahn, R.S., Selten, J.P., Sex differences in the risk of schizophrenia: evidence from meta-analysis. Arch. Gen. Psychiatry 60:6 (2003), 565–571.
5. Amann, B.L., Canales-Rodriguez, E.J., Madre, M., Radua, J., Monte, G., Alonso-Lana, S., Landin-Romero, R., Moreno-Alcazar, A., Bonnin, C.M., Sarro, S., Ortiz-Gil, J., Gomar, J.J., Moro, N., Fernandez-Corcuera, P., Goikolea, J.M., Blanch, J., Salvador, R., Vieta, E., McKenna, P.J., Pomarol-Clotet, E., Brain structural changes in schizoaffective disorder compared to schizophrenia and bipolar disorder. Acta Psychiatr. Scand. 133:1 (2016), 23–33.
6. Andreasen, N.C., Olsen, S., Negative v positive schizophrenia. Definition and validation. Arch. Gen. Psychiatry 39:7 (1982), 789–794.
7. Arias-Loza, P.A., Muehlfelder, M., Pelzer, T., Estrogen and estrogen receptors in cardiovascular oxidative stress. Pflugers Arch. 465:5 (2013), 739–746.
8. Bachi, A., Zuccato, E., Baraldi, M., Fanelli, R., Chiabrando, C., Measurement of urinary 8-epi-prostaglandin F2alpha, a novel index of lipid peroxidation in vivo, by immunoaffinity extraction/gas chromatography–mass spectrometry. Basal levels in smokers and nonsmokers. Free Radic. Biol. Med. 20:4 (1996), 619–624.
9. Basu, S., F2-isoprostanes in human health and diseases: from molecular mechanisms to clinical implications. Antioxid. Redox Signal. 10:8 (2008), 1405–1434.
10. Callewaert, D.M., Sloan, C., Enzyme immunoassay of isoprostanes. Methods Mol. Biol. 610 (2010), 435–449.
11. Davi, G., Falco, A., Patrono, C., Determinants of F2-isoprostane biosynthesis and inhibition in man. Chem. Phys. Lipids 128:1–2 (2004), 149–163.
12. Davies, S.S., Roberts, L.J. 2nd, F2-isoprostanes as an indicator and risk factor for coronary heart disease. Free Radic. Biol. Med. 50:5 (2011), 559–566.
13. Delis, D., Kaplan, E., Kramer, J., Delis-Kaplan Executive Function Scale (D-KEFS): Examiner's Manual. 2001, The Psychological Corporation, San Antonio, TX.
14. Dietrich-Muszalska, A., Olas, B., Isoprostenes as indicators of oxidative stress in schizophrenia. World J. Biol. Psychiatry 10:1 (2009), 27–33.
15. Dietrich, M., Block, G., Hudes, M., Morrow, J.D., Norkus, E.P., Traber, M.G., Cross, C.E., Packer, L., Antioxidant supplementation decreases lipid peroxidation biomarker F(2)-isoprostanes in plasma of smokers. Cancer Epidemiol. Biomark. Prev. 11:1 (2002), 7–13.
16. Eranti, S.V., MacCabe, J.H., Bundy, H., Murray, R.M., Gender difference in age at onset of schizophrenia: a meta-analysis. Psychol. Med. 43:1 (2013), 155–167.
17. Evans, J.D., Heaton, R.K., Paulsen, J.S., McAdams, L.A., Heaton, S.C., Jeste, D.V., Schizoaffective disorder: a form of schizophrenia or affective disorder?. J. Clin. Psychiatry 60:12 (1999), 874–882.
18. Finkel, T., Holbrook, N.J., Oxidants, oxidative stress and the biology of ageing. Nature 408:6809 (2000), 239–247.
19. First, M., Spitzer, R.L., Gibbon, M., Wiliams, J.B.W., Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version, Patient Edition. (SCID-I/P). 2002, Biometrics Research, New York State Psychiatric Institute, New York (November).
20. Fukui, T., Yamauchi, K., Maruyama, M., Yasuda, T., Kohno, M., Abe, Y., Significance of measuring oxidative stress in lifestyle-related diseases from the viewpoint of correlation between d-ROMs and BAP in Japanese subjects. Hypertens. Res. 34:9 (2011), 1041–1045.
21. Gerner, R.H., Merrill, J.E., Cerebrospinal fluid prostaglandin E in depression, mania, and schizophrenia compared to normals. Biol. Psychiatry 18:5 (1983), 565–569.
22. Goff, D.C., Henderson, D.C., Amico, E., Cigarette smoking in schizophrenia: relationship to psychopathology and medication side effects. Am. J. Psychiatry 149:9 (1992), 1189–1194.
23. Hafner, H., Gender differences in schizophrenia. Psychoneuroendocrinology 28:Suppl. 2 (2003), 17–54.
24. Hennekens, C.H., Hennekens, A.R., Hollar, D., Casey, D.E., Schizophrenia and increased risks of cardiovascular disease. Am. Heart J. 150:6 (2005), 1115–1121.
25. Herken, H., Uz, E., Ozyurt, H., Sogut, S., Virit, O., Akyol, O., Evidence that the activities of erythrocyte free radical scavenging enzymes and the products of lipid peroxidation are increased in different forms of schizophrenia. Mol. Psychiatry 6:1 (2001), 66–73.
26. Hoffer, A., Osmond, H., Smythies, J., Schizophrenia; a new approach. II. Result of a year's research. J. Ment. Sci. 100:418 (1954), 29–45.
27. Hughes, J.R., Hatsukami, D.K., Mitchell, J.E., Dahlgren, L.A., Prevalence of smoking among psychiatric outpatients. Am. J. Psychiatry 143:8 (1986), 993–997.
28. Jeste, D.V., Wolkowitz, O.M., Palmer, B.W., Divergent trajectories of physical, cognitive, and psychosocial aging in schizophrenia. Schizophr. Bull. 37:3 (2011), 451–455.
29. Jorgensen, A., Broedbaek, K., Fink-Jensen, A., Knorr, U., Greisen Soendergaard, M., Henriksen, T., Weimann, A., Jepsen, P., Lykkesfeldt, J., Poulsen, H.E., Balslev Jorgensen, M., Increased systemic oxidatively generated DNA and RNA damage in schizophrenia. Psychiatry Res. 209:3 (2013), 417–423.
30. Joseph, J., Depp, C., Martin, A.S., Daly, R.E., Glorioso, D.K., Palmer, B.W., Jeste, D.V., Associations of high sensitivity C-reactive protein levels in schizophrenia and comparison groups. Schizophr. Res. 168:1–2 (2015), 456–460.
31. Kaiya, H., Prostaglandin E1 treatment of schizophrenia. Biol. Psychiatry 19:3 (1984), 457–463.
32. Kaiya, H., Uematsu, M., Ofuji, M., Nishida, A., Takeuchi, K., Nozaki, M., Idaka, E., Elevated plasma prostaglandin E2 levels in schizophrenia. J. Neural Transm. 77:1 (1989), 39–46.
33. Keaney, J.F. Jr., Larson, M.G., Vasan, R.S., Wilson, P.W., Lipinska, I., Corey, D., Massaro, J.M., Sutherland, P., Vita, J.A., Benjamin, E.J., Framingham, S., Obesity and systemic oxidative stress: clinical correlates of oxidative stress in the Framingham study. Arterioscler. Thromb. Vasc. Biol. 23:3 (2003), 434–439.
34. Khadir, A., Tiss, A., Kavalakatt, S., Behbehani, K., Dehbi, M., Elkum, N., Gender-specific association of oxidative stress and inflammation with cardiovascular risk factors in Arab population. Mediat. Inflamm., 2015, 2015, 512603.
35. Kirkpatrick, B., Messias, E., Harvey, P.D., Fernandez-Egea, E., Bowie, C.R., Is schizophrenia a syndrome of accelerated aging?. Schizophr. Bull. 34:6 (2008), 1024–1032.
36. Kroenke, K., Spitzer, R.L., Williams, J.B., The PHQ-9: validity of a brief depression severity measure. J. Gen. Intern. Med. 16:9 (2001), 606–613.
37. Li, G., Millard, S.P., Peskind, E.R., Zhang, J., Yu, C.E., Leverenz, J.B., Mayer, C., Shofer, J.S., Raskind, M.A., Quinn, J.F., Galasko, D.R., Montine, T.J., Cross-sectional and longitudinal relationships between cerebrospinal fluid biomarkers and cognitive function in people without cognitive impairment from across the adult life span. JAMA Neurol. 71:6 (2014), 742–751.
38. Lindamer, L.A., Lohr, J.B., Harris, M.J., McAdams, L.A., Jeste, D.V., Gender-related clinical differences in older patients with schizophrenia. J. Clin. Psychiatry 60:1 (1999), 61–67 (quiz 68–69).
39. Linn, B.S., Linn, M.W., Gurel, L., Cumulative illness rating scale. J. Am. Geriatr. Soc. 16:5 (1968), 622–626.
40. Linnoila, M., Whorton, A.R., Rubinow, D.R., Cowdry, R.W., Ninan, P.T., Waters, R.N., CSF prostaglandin levels in depressed and schizophrenic patients. Arch. Gen. Psychiatry 40:4 (1983), 405–406.
41. Magalhaes, P.V., Dean, O., Andreazza, A.C., Berk, M., Kapczinski, F., Antioxidant treatments for schizophrenia. Cochrane Database Syst. Rev., 2, 2016, CD008919.
42. Mathe, A.A., Sedvall, G., Wiesel, F.A., Nyback, H., Increased content of immunoreactive prostaglandin E in cerebrospinal fluid of patients with schizophrenia. Lancet 1:8158 (1980), 16–18.
43. McEvoy, J.P., Meyer, J.M., Goff, D.C., Nasrallah, H.A., Davis, S.M., Sullivan, L., Meltzer, H.Y., Hsiao, J., Scott Stroup, T., Lieberman, J.A., Prevalence of the metabolic syndrome in patients with schizophrenia: baseline results from the clinical antipsychotic trials of intervention effectiveness (CATIE) schizophrenia trial and comparison with national estimates from NHANES III. Schizophr. Res. 80:1 (2005), 19–32.
44. Meagher, E.A., Barry, O.P., Burke, A., Lucey, M.R., Lawson, J.A., Rokach, J., FitzGerald, G.A., Alcohol-induced generation of lipid peroxidation products in humans. J. Clin. Invest. 104:6 (1999), 805–813.
45. Meyer, J.M., Nasrallah, H.A., Medical Illness and Schizophrenia. second ed., 2009, American Psychiatric Publishing, Inc., Arlington, VA.
46. Milne, G.L., Dai, Q., Roberts, L.J. 2nd, The isoprostanes—25 years later. Biochim. Biophys. Acta 1851:4 (2015), 433–445.
47. Milne, G.L., Sanchez, S.C., Musiek, E.S., Morrow, J.D., Quantification of F2-isoprostanes as a biomarker of oxidative stress. Nat. Protoc. 2:1 (2007), 221–226.
48. Montuschi, P., Barnes, P.J., Roberts, L.J. 2nd, Isoprostanes: markers and mediators of oxidative stress. FASEB J. 18:15 (2004), 1791–1800.
49. Morrow, J.D., Frei, B., Longmire, A.W., Gaziano, J.M., Lynch, S.M., Shyr, Y., Strauss, W.E., Oates, J.A., Roberts, L.J. 2nd, Increase in circulating products of lipid peroxidation (F2-isoprostanes) in smokers. Smoking as a cause of oxidative damage. N. Engl. J. Med. 332:18 (1995), 1198–1203.
50. Morrow, J.D., Roberts, L.J., The isoprostanes: unique bioactive products of lipid peroxidation. Prog. Lipid Res. 36:1 (1997), 1–21.
51. Morrow, J.D., Roberts, L.J. 2nd, Mass spectrometric quantification of F2-isoprostanes as indicators of oxidant stress. Methods Mol. Biol. 186 (2002), 57–66.
52. Mukerjee, S., Mahadik, S.P., Scheffer, R., Correnti, E.E., Kelkar, H., Impaired antioxidant defense at the onset of psychosis. Schizophr. Res. 19:1 (1996), 19–26.
53. Nasrallah, H.A., Harvey, P.D., Casey, D., Csoboth, C.T., Hudson, J.I., Julian, L., Lentz, E., Nuechterlein, K.H., Perkins, D.O., Kotowsky, N., Skale, T.G., Snowden, L.R., Tandon, R., Tek, C., Velligan, D., Vinogradov, S., O'Gorman, C., The management of schizophrenia in clinical practice (MOSAIC) registry: a focus on patients, caregivers, illness severity, functional status, disease burden and healthcare utilization. Schizophr. Res. 166:1–3 (2015), 69–79.
54. Ng, F., Berk, M., Dean, O., Bush, A.I., Oxidative stress in psychiatric disorders: evidence base and therapeutic implications. Int. J. Neuropsychopharmacol. 11:6 (2008), 851–876.
55. Padurariu, M., Ciobica, A., Dobrin, I., Stefanescu, C., Evaluation of antioxidant enzymes activities and lipid peroxidation in schizophrenic patients treated with typical and atypical antipsychotics. Neurosci. Lett. 479:3 (2010), 317–320.
56. Patrono, C., FitzGerald, G.A., Isoprostanes: potential markers of oxidant stress in atherothrombotic disease. Arterioscler. Thromb. Vasc. Biol. 17:11 (1997), 2309–2315.
57. Pazvantoglu, O., Selek, S., Okay, I.T., Sengul, C., Karabekiroglu, K., Dilbaz, N., Erel, O., Oxidative mechanisms in schizophrenia and their relationship with illness subtype and symptom profile. Psychiatry Clin. Neurosci. 63:5 (2009), 693–700.
58. Peskind, E.R., Li, G., Shofer, J.B., Millard, S.P., Leverenz, J.B., Yu, C.E., Raskind, M.A., Quinn, J.F., Galasko, D.R., Montine, T.J., Influence of lifestyle modifications on age-related free radical injury to brain. JAMA Neurol. 71:9 (2014), 1150–1154.
59. Reddy, R., Sahebarao, M.P., Mukherjee, S., Murthy, J.N., Enzymes of the antioxidant defense system in chronic schizophrenic patients. Biol. Psychiatry 30:4 (1991), 409–412.
60. Roberts, L.J. 2nd, Reckelhoff, J.F., Measurement of F(2)-isoprostanes unveils profound oxidative stress in aged rats. Biochem. Biophys. Res. Commun. 287:1 (2001), 254–256.
61. Rossi, I.A., Bochud, M., Bovet, P., Paccaud, F., Waeber, G., Vollenweider, P., Taffe, P., Sex difference and the role of leptin in the association between high-sensitivity C-reactive protein and adiposity in two different populations. Eur. J. Epidemiol. 27:5 (2012), 379–384.
62. Saha, S., Chant, D., McGrath, J., A systematic review of mortality in schizophrenia: is the differential mortality gap worsening over time?. Arch. Gen. Psychiatry 64:10 (2007), 1123–1131.
63. Sankhla, M., Sharma, T.K., Mathur, K., Rathor, J.S., Butolia, V., Gadhok, A.K., Vardey, S.K., Sinha, M., Kaushik, G.G., Relationship of oxidative stress with obesity and its role in obesity induced metabolic syndrome. Clin. Lab. 58:5–6 (2012), 385–392.
64. Sarandol, A., Kirli, S., Akkaya, C., Altin, A., Demirci, M., Sarandol, E., Oxidative-antioxidative systems and their relation with serum S100 B levels in patients with schizophrenia: effects of short term antipsychotic treatment. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 31:6 (2007), 1164–1169.
65. Sheehan, D.V., Lecrubier, Y., Sheehan, K.H., Amorim, P., Janavs, J., Weiller, E., Hergueta, T., Baker, R., Dunbar, G.C., The mini-international neuropsychiatric interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J. Clin. Psychiatry 59:Suppl. 20 (1998), 22–33 (quiz 34–57).
66. Stephens, J.W., Khanolkar, M.P., Bain, S.C., The biological relevance and measurement of plasma markers of oxidative stress in diabetes and cardiovascular disease. Atherosclerosis 202:2 (2009), 321–329.
67. van den Berg, E., Ruis, C., Biessels, G.J., Kappelle, L.J., van Zandvoort, M.J., The telephone interview for cognitive status (modified): relation with a comprehensive neuropsychological assessment. J. Clin. Exp. Neuropsychol. 34:6 (2012), 598–605.
68. Vassalle, C., Simoncini, T., Chedraui, P., Perez-Lopez, F.R., Why sex matters: the biological mechanisms of cardiovascular disease. Gynecol. Endocrinol. 28:9 (2012), 746–751.
69. Vincent, H.K., Taylor, A.G., Biomarkers and potential mechanisms of obesity-induced oxidant stress in humans. Int. J. Obes. 30:3 (2006), 400–418.
70. von Zglinicki, T., Oxidative stress shortens telomeres. Trends Biochem. Sci. 27:7 (2002), 339–344.
71. Ware, J.E. Jr., Sherbourne, C.D., The MOS 36-item short-form health survey (SF-36). I. Conceptual framework and item selection. Med. Care 30:6 (1992), 473–483.
72. WHO, The World Health Report: Mental Health: New Understanding, New Hope. 2001, World Health Organization, Geneva.
73. WHO, Introduction to drug utilization research. 2009, World Health Organization Collaborating Centre for Drug Statistics Methodology.
74. WHO, Guidelines for ATC classification and DDD assignment. 2010, World Health Organization.
75. Wiener, C., Rassier, G.T., Kaster, M.P., Jansen, K., Pinheiro, R.T., Klamt, F., Magalhaes, P.V., Kapczinski, F., Ghisleni, G., da Silva, R.A., Gender-based differences in oxidative stress parameters do not underlie the differences in mood disorders susceptibility between sexes. Eur. Psychiatry 29:1 (2014), 58–63.
76. Wu, Z., Zhang, X.Y., Wang, H., Tang, W., Xia, Y., Zhang, F., Liu, J., Fu, Y., Hu, J., Chen, Y., Liu, L., Chen da, C., Xiu, M.H., Kosten, T.R., He, J., Elevated plasma superoxide dismutase in first-episode and drug naive patients with schizophrenia: inverse association with positive symptoms. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 36:1 (2012), 34–38.
77. Yanik, M., Vural, H., Kocyigit, A., Tutkun, H., Zoroglu, S.S., Herken, H., Savas, H.A., Koylu, A., Akyol, O., Is the arginine-nitric oxide pathway involved in the pathogenesis of schizophrenia?. Neuropsychobiology 47:2 (2003), 61–65.
78. Yao, J.K., Leonard, S., Reddy, R., Altered glutathione redox state in schizophrenia. Dis. Markers 22:1–2 (2006), 83–93.
79. Yao, J.K., Leonard, S., Reddy, R.D., Increased nitric oxide radicals in postmortem brain from patients with schizophrenia. Schizophr. Bull. 30:4 (2004), 923–934.
80. Yao, J.K., Reddy, R., van Kammen, D.P., Abnormal age-related changes of plasma antioxidant proteins in schizophrenia. Psychiatry Res. 97:2–3 (2000), 137–151.
81. Zhang, X.Y., Chen da, C., Xiu, M.H., Wang, F., Qi, L.Y., Sun, H.Q., Chen, S., He, S.C., Wu, G.Y., Haile, C.N., Kosten, T.A., Lu, L., Kosten, T.R., The novel oxidative stress marker thioredoxin is increased in first-episode schizophrenic patients. Schizophr. Res. 113:2–3 (2009), 151–157.
82. Zhang, X.Y., Zhou, D.F., Cao, L.Y., Zhang, P.Y., Wu, G.Y., Elevated blood superoxide dismutase in neuroleptic-free schizophrenia: association with positive symptoms. Psychiatry Res. 117:1 (2003), 85–88.