Plasma-based proteomics reveals lipid metabolic and immunoregulatory dysregulation in post-stroke depression

European Psychiatry

Volumn 29, Issue 5, 2014, Pages 307-315

  Zhan, Y ^a,b   Yang, Y T ^a,b   You, H M ^a,b   Cao, D ^a,b   Liu, C Y ^a,b   Zhou, C J ^a,b   Wang, Z Y ^a,b   Bai, S J ^a,b   Mu, J ^a,b   Wu, B ^a,b   Zhan, Q L ^c   Xie, P ^a,b  

^a CHONGQING MEDICAL UNIVERSITY   (China)

^b CHONGQING KEY LABORATORY OF NEUROBIOLOGY   (China)

^c The Fifth People's Hospital of Chongqing   (China)

Author keywords

Plasma; Post stroke depression; Proteomic; PSD; Stroke

Indexed keywords

ALPHA2 GLYCOPROTEIN; APOLIPOPROTEIN A4; APOLIPOPROTEIN C2; BIOLOGICAL MARKER; C REACTIVE PROTEIN; GELSOLIN; GLYCOPROTEIN; HAPTOGLOBIN; LEUCINE RICH ALPHA2 GLYCOPROTEIN; UNCLASSIFIED DRUG; APOLIPOPROTEIN A; APOLIPOPROTEIN A-IV; LRG1 PROTEIN, HUMAN;

ADULT; AGED; ARTICLE; CEREBROVASCULAR ACCIDENT; CONTROL; DEPRESSION; DISEASE MARKER; DOWN REGULATION; FEMALE; HUMAN; IMMUNOREGULATION; LIPID METABOLISM; LIQUID CHROMATOGRAPHY; MAJOR CLINICAL STUDY; MALE; NUCLEOTIDE SEQUENCE; PATHOPHYSIOLOGY; PLASMA; POST STROKE DEPRESSION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEOMICS; TANDEM MASS SPECTROMETRY; VALIDATION STUDY; WESTERN BLOTTING; COMPLICATION; DEPRESSIVE DISORDER; IMMUNE SYSTEM; METABOLISM; MIDDLE AGED; PHYSIOLOGY;

AGED; APOLIPOPROTEIN C-II; APOLIPOPROTEINS A; C-REACTIVE PROTEIN; DEPRESSIVE DISORDER; FEMALE; GELSOLIN; GLYCOPROTEINS; HAPTOGLOBINS; HUMANS; IMMUNE SYSTEM; LIPID METABOLISM; MALE; MIDDLE AGED; PROTEOMICS; STROKE;

EID: 84902364420     PISSN: 09249338     EISSN: 17783585     Source Type: Journal    
DOI: 10.1016/j.eurpsy.2014.03.004     Document Type: Article

References (79)

1. Allan L.M., Rowan E.N., Thomas A.J., Polvikoski T.M., O'Brien J.T., Kalaria R.N. Long-term incidence of depression and predictors of depressive symptoms in older stroke survivors. Br J Psychiatry 2013, 203(6):453-460.
2. Autenrieth C., Schneider A., Doering A., Meisinger C., Herder C., Koenig W., et al. Association between different domains of physical activity and markers of inflammation. Med Sci Sports Exerc 2009, 41(9):1706-1713.
3. Azuma T., Koths K., Flanagan L., Kwiatkowski D. Gelsolin in complex with phosphatidylinositol 4, 5-bisphosphate inhibits caspase-3 and -9 to retard apoptotic progression. J Biol Chem 2000, 275:3761-3766.
4. Becker P.M., Kazi A.A., Wadgaonkar R., Pearse D.B., Kwiatkowski D., Garcia J.G. Pulmonary vascular permeability and ischemic injury in gelsolin-deficient mice. Am J Respir Cell Mol Biol 2003, 28:478-484.
5. Berg A., Lönnqvist J., Palomäki H., Kaste M. Assessment of depression after stroke: a comparison of different screening instruments. Stroke 2009, 40:523-529.
6. Bini A., Itoh Y., Kudryk B.J., Nagase H. Degradation of cross-linked fibrin by matrix metalloproteinase 3 (stromelysin 1): hydrolysis of the γ Gly 404-Ala 405 peptide bond. Biochemistry 1996, 35:13056-13063.
7. Black S., Kushner I., Samols D. C-reactive protein. J Biol Chem 2004, 279:48487-48490.
8. Brea D., Sobrino T., Blanco M., Fraga M., Agulla J., Rodríguez-Yáñez M., et al. Usefulness of haptoglobin and serum amyloid A proteins as biomarkers for atherothrombotic ischemic stroke diagnosis confirmation. Atherosclerosis 2009, 205:561-567.
9. Brott T., Adams H.P., Olinger C.P., Marler J.R., Barsan W.G., Biller J., et al. Measurements of acute cerebral infarction: a clinical examination scale. Stroke 1989, 20:864-870.
10. Bucki R., Georges P.C., Espinassous Q., Funaki M., Pastore J.J., Chaby R., et al. Inactivation of endotoxin by human plasma gelsolin. Biochemistry 2005, 44:9590-9597.
11. Carboni L., Becchi S., Piubelli C., Mallei A., Giambelli R., Razzoli M., et al. Early-life stress and antidepressants modulate peripheral biomarkers in a gene-environment rat model of depression. Prog Neuropsychopharmacol 2010, 34:1037-1048.
12. Cojocaru I.M., Cojocaru M., Muşuroi C., Druţǎ A., Bǎcanu M. Study of some markers of inflammation in atherothrombotic pathogenesis of acute ischemic stroke. Rom J Intern Med 2001, 40:103-116.
13. de Maat M.P., Kluft C. The association between inflammation markers, coronary artery disease and smoking. Vasc Pharmacol 2002, 39(3):137-139.
14. Dennis G., Sherman B.T., Hosack D.A., Yang J., Gao W., Lane H.C., et al. DAVID: database for annotation, visualization, and integrated discovery. Genome Biol 2003, 4:P3.
15. Domenici E., Willé D.R., Tozzi F., Prokopenko I., Miller S., McKeown A., et al. Plasma protein biomarkers for depression and schizophrenia by multi analyte profiling of case-control collections. PLoS One 2010, 5:e9166.
16. Ejchel T., Araújo L., Ramos L., Cendoroglo M., Smith M.d.A.C. Association of the apolipoprotein A-IV: 360 gln/his polymorphism with cerebrovascular disease, obesity, and depression in a Brazilian elderly population. Am J Med Genet B Neuropsychiatr Genet 2005, 135:65-68.
17. Endicott J., Cohen J., Nee J., Fleiss J., Sarantakos S. Hamilton depression rating scale. Extracted from regular and change versions of the schedule for affective disorders and schizophrenia. Arch Gen Psychiatry 1981, 38:98-103.
18. Endres M., Fink K., Zhu J., Stagliano N.E., Bondada V., Geddes J.W., et al. Neuroprotective effects of gelsolin during murine stroke. J Clin Invest 1999, 103:347-354.
19. Ferretti G., Bacchetti T., Bicchiega V., Curatola G. Effect of human ApoAIV against lipid peroxidation of very low density lipoproteins. Chem Phys Lipids 2002, 114:45-54.
20. Foerch C., Montaner J., Furie K., Ning M., Lo E. Invited article: searching for oracles? Blood biomarkers in acute stroke. Neurology 2009, 73:393-399.
21. Furukawa K., Fu W., Li Y., Witke W., Kwiatkowski D.J., Mattson M.P. The actin-severing protein gelsolin modulates calcium channel and NMDA receptor activities and vulnerability to excitotoxicity in hippocampal neurons. J Neurosci 1997, 17:8178-8186.
22. Goetzl E.J., Lee H., Azuma T., Stossel T.P., Turck C.W., Karliner J.S. Gelsolin binding and cellular presentation of lysophosphatidic acid. J Biol Chem 2000, 275:14573-14578.
23. Goldberg I., Scheraldi C., Yacoub L., Saxena U., Bisgaier C. Lipoprotein ApoC-II activation of lipoprotein lipase. Modulation by apolipoprotein A-IV. J Biol Chem 1990, 265:4266-4272.
24. Guo X.-C., Luo B.-Y., Li X.-F., Yang D.-G., Zheng X.-N., Zhang K. Plasma gelsolin levels and 1-year mortality after first-ever ischemic stroke. J Crit Care 2011, 26:608-612.
25. Haddad J., Harper K., Guoth M., Pietra G., Sanger J. Angiopathic consequences of saturating the plasma scavenger system for actin. Proc Natl Acad Sci U S A 1990, 87:1381-1385.
26. Hampel H., Kötter H., Möller H.-J. Blood-cerebrospinal fluid barrier dysfunction for high molecular weight proteins in Alzheimer disease and major depression: indication for disease subsets. Alzheimer Dis Assoc Disord 1997, 11:78-87.
27. Holme I., Aastveit A.H., Hammar N., Jungner I., Walldius G. Haptoglobin and risk of myocardial infarction, stroke, and congestive heart failure in 342,125 men and women in the Apolipoprotein MOrtality RISk study (AMORIS). Ann Med 2009, 41:522-532.
28. Horrobin D., Bennett C. Depression and bipolar disorder: relationships to impaired fatty acid and phospholipid metabolism and to diabetes, cardiovascular disease, immunological abnormalities, cancer, ageing and osteoporosis. Possible candidate genes. Prostaglandins Leukot Essent Fatty Acids 1999, 60:217-234.
29. Huang J.T.-J., Leweke F.M., Oxley D., Wang L., Harris N., Koethe D., et al. Disease biomarkers in cerebrospinal fluid of patients with first-onset psychosis. PLoS Med 2006, 3:e428.
30. Huang S., Rhoads S.L., DiNubile M.J. Temporal association between serum gelsolin levels and clinical events in a patient with severe falciparum malaria. Clin Infect Dis 1997, 24:951-954.
31. Huang T.-L. Serum lipid profiles in major depression with clinical subtypes, suicide attempts and episodes. J Affect Disord 2005, 86:75-79.
32. Huang T.-L., Wu S.-C., Chiang Y.-S., Chen J.-F. Correlation between serum lipid, lipoprotein concentrations and anxious state, depressive state or major depressive disorder. Psychiatr Res 2003, 118:147-153.
33. Janmey P.A., Lind S.E. Capacity of human serum to depolymerize actin filaments. Blood 1987, 70:524-530.
34. Kardassis D., Roussou A., Papakosta P., Boulias K., Talianidis I., Zannis V. Synergism between nuclear receptors bound to specific hormone response elements of the hepatic control region-1 and the proximal apolipoprotein C-II promoter mediate apolipoprotein C-II gene regulation by bile acids and retinoids. Biochem J 2003, 372:291-304.
35. Koo H.M., Kim J.-H., Hwang I.K., Lee S.-J., Kim T.-H., Rhee K.-H., et al. Refolding of the catalytic and hinge domains of human MT1-MMP expressed in Escherichia coli and its characterization. Mol Cells 2002, 13:118-124.
36. Kwiatkowski D., Mehl R., Izumo S., Nadal-Ginard B., Yin H. Muscle is the major source of plasma gelsolin. J Biol Chem 1988, 263:8239-8243.
37. Kwiatkowski D.J., Stossel T.P., Orkin S.H., Mole J.E., Coltens H.R., Yin H.L. Plasma and cytoplasmic gelsolins are encoded by a single gene and contain a duplicated actin-binding domain. Nature 1986, 323:455-458.
38. Laskowitz D.T., Kasner S.E., Saver J., Remmel K.S., Jauch E.C. Clinical usefulness of a biomarker-based diagnostic test for acute stroke. The Biomarker Rapid Assessment in Ischemic Injury (BRAIN) study. Stroke 2009, 40:77-85.
39. Le H.T., Hirko A.C., Thinschmidt J.S., Grant M., Li Z., Peris J., et al. The protective effects of plasma gelsolin on stroke outcome in rats. Exp Transl Stroke Med 2011, 3:1-9.
40. Lee P.-S., Waxman A.B., Cotich K.L., Chung S.W., Perrella M.A., Stossel T.P. Plasma gelsolin is a marker and therapeutic agent in animal sepsis. Crit Care Med 2007, 35:849-855.
41. Liesz A1, Rüger H., Purrucker J., Zorn M., Dalpke A. Stress mediators and immune dysfunction in patients with acute cerebrovascular diseases. PLoS One 2013, 198(9):e74839.
42. Liew C.-C., Ma J., Tang H.-C., Zheng R., Dempsey A.A. The peripheral blood transcriptome dynamically reflects system wide biology: a potential diagnostic tool. J Lab Clin Med 2006, 147:126-132.
43. Lind S., Smith D.B., Janmey P.A., Stossel T.P. Role of plasma gelsolin and the vitamin D-binding protein in clearing actin from the circulation. J Clin Invest 1986, 78:736-742.
44. Martín A., Garofalakis A., Tavitian B. In vivo evidence that the increase in matrix metalloproteinase activity occurs early after cerebral ischemia. Mol Imaging 2012, 11:22-26.
45. Meader N., Moe-Byrne T., Llewellyn A., Mitchell A.J. Screening for poststroke major depression: a meta-analysis of diagnostic validity studies. J Neurol Neurosurg Psychiatry 2014, 85(2):198-206.
46. Meerschaert K., De Corte V., De Ville Y., Vandekerckhove J., Gettemans J. Gelsolin and functionally similar actin-binding proteins are regulated by lysophosphatidic acid. EMBO J 1998, 17:5923-5932.
47. Miller A.H., Haroon E., Raison C.L., Felger J.C. Cytokine targets in the brain: impact on neurotransmitters and neurocircuits. Depress Anxiety 2013, 30(4):297-306.
48. Montaner J., Perea-Gainza M., Delgado P., Ribó M., Chacón P., Rosell A., et al. Etiologic diagnosis of ischemic stroke subtypes with plasma biomarkers. Stroke 2008, 39:2280-2287.
49. Moulder R., Lönnberg T., Elo L.L., Filén J.-J., Rainio E., Corthals G., et al. Quantitative proteomics analysis of the nuclear fraction of human CD4+ cells in the early phases of IL-4-induced Th2 differentiation. Mol Cell Proteomics 2010, 9:1937-1953.
50. Mounzer K.C., Moncure M., Smith Y.R., DiNubile M.J. Relationship of admission plasma gelsolin levels to clinical outcomes in patients after major trauma. Am J Respir Crit Care Med 1999, 160:1673-1681.
51. Noonan K., Carey L.M., Crewther S.G. Meta-analyses indicate associations between neuroendocrine activation, deactivation in neurotrophic and neuroimaging markers in depression after stroke. J Stroke Cerebrovasc Dis 2012, 9:1-12.
52. Noonan K., Crewther S.G., Carey L.M., Pascoe M.C., Linden T. Sustained inflammation 1.5 years post-stroke is not associated with depression in elderly stroke survivors. Clin Interv Aging 2013, 8:69-74.
53. O'Donnell M.J., Xavier D., Liu L., Zhang H., Chin S.L., Rao-Melacini P., et al. Risk factors for ischaemic and intracerebral haemorrhagic stroke in 22 countries (the INTERSTROKE study): a case-control study. Lancet 2010, 376:112-123.
54. Ohtsu M., Sakai N., Fujita H., Kashiwagi M., Gasa S., Shimizu S., et al. Inhibition of apoptosis by the actin-regulatory protein gelsolin. EMBO J 1997, 16:4650-4656.
55. Ostos M.A., Conconi M., Vergnes L., Baroukh N., Ribalta J., Girona J., et al. Antioxidative and antiatherosclerotic effects of human apolipoprotein A-IV in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 2001, 21:1023-1028.
56. Pan S., Zhan X., Su X., Guo L., Lv L., Su B. Proteomic analysis of serum proteins in acute schemic stroke patients treated with acupuncture. Exp Biol Med 2011, 236:325-333.
57. Parikh R.M., Robinson R.G., Lipsey J.R., Starkstein S.E., Fedoroff J.P., Price T.R. The impact of poststroke depression on recovery in activities of daily living over a 2-year follow-up. Arch Neurol 1990, 47:785-789.
58. Pedro-Botet J., Senti M., Nogues X., Rubies-Prat J., Roquer J., D'olhaberriague L., et al. Lipoprotein and apolipoprotein profile in men with ischemic stroke. Role of lipoprotein (a), triglyceride-rich lipoproteins, and apolipoprotein E polymorphism. Stroke 1992, 23:1556-1562.
59. Qin X., Swertfeger D.K., Zheng S., Hui D.Y., Tso P. Apolipoprotein AIV: a potent endogenous inhibitor of lipid oxidation. Am J Physiol Heart Circ Physiol 1998, 274:H1836-H1840.
60. Robinson R., Starkstein S., Price T. Post-stroke depression and lesion location. Stroke 1988, 19:125-126.
61. Calabrò R.S., Spadaro L., Bramanti P. Cerebrovascular Diseases: Post-stroke Depression and Anhedonia. Anhedonia: A Comprehensive Handbook Volume II 2014, 301-318. Springer Netherlands publishing, New York, NY. M.S. Ritsner (Ed.).
62. Rosengart M.R., Arbabi S., Bauer G.J., Garcia I., Jelacic S., Maier R.V. The actin cytoskeleton: an essential component for enhanced TNF [alpha] production by adherent monocytes. Shock 2002, 17:109-113.
63. Rothwell P.M., Howard S.C., Power D.A., Gutnikov S.A., Algra A., van Gijn J., et al. Fibrinogen concentration and risk of ischemic stroke and acute coronary events in 5113 patients with transient ischemic attack and minor ischemic stroke. Stroke 2004, 35:2300-2305.
64. Sacco R.L. Newer risk factors for stroke. Neurology 2001, 57. S31-S4.
65. Schubert D., Burns R., Paras W., Sioson E. Increase of medical hospital length of stay by depression in stroke and amputation patients: a pilot study. Psychother Psychosom 1992, 57:61-66.
66. Spalletta G., Bossu P., Ciaramella A., Bria P., Caltagirone C., Robinson R. The etiology of poststroke depression: a review of the literature and a new hypothesis involving inflammatory cytokines. Mol Psychiatry 2006, 11:984-991.
67. Spalletta G., Cravello L., Imperiale F., Salani F., Bossù P. Neuropsychiatric symptoms and interleukin-6 serum levels in acute stroke. J Neuropsychiatry Clin Neurosci 2013, 25(4):255-263.
68. Steinmetz A., Utermann G. Activation of lecithin: cholesterol acyltransferase by human apolipoprotein A-IV. J Biol Chem 1985, 260:2258-2264.
69. Goldstein M., Barnett H.J.M., Orgogozo J.M., Sartorius N., Symon L., Ereshchagin N.V. Stroke-1989: Recommendations on stroke prevention, diagnosis, and therapy. Report of the WHO task force on stroke and other cerebrovascular disorders. Stroke 1989, 20:1407-1431.
70. Su J.-A., Chou S.-Y., Tsai C.-S., Hung T.-H. Cytokine changes in the pathophysiology of outstroke depression. Gen Hosp Psychiatry 2012, 34:35-39.
71. Ünlü M., de Lange R.P., de Silva R., Kalaria R., St Clair D. Detection of complement factor B in the cerebrospinal fluid of patients with cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy disease using two-dimensional gel electrophoresis and mass spectrometry. Neurosci Lett 2000, 282:149-152.
72. Uyttenboogaart M., Stewart R.E., Vroomen P.C., De Keyser J., Luijckx G.J. Optimizing cutoff scores for the Barthel index and the modified Rankin scale for defining outcome in acute stroke trials. Stroke 2005, 36:1984-1987.
73. White J.H., Attia J., Sturm J., Carter G., Magin P. Predictors of depression and anxiety in community dwelling stroke survivors: a cohort study. Disabil Rehabil 2014, 10.3109/09638288.2014.884172.
74. Wittrup H.H., Nordestgaard B.G., Sillesen H., Schnohr P., Tybjærg-Hansen A. A common mutation in lipoprotein lipase confers a 2-fold increase in risk of ischemic cerebrovascular disease in women but not in men. Circulation 2000, 101:2393-2397.
75. Xu H.B., Zhang R.F., Luo D., Zhou Y., Wang Y., Fang L., et al. Comparative proteomic analysis of plasma from major depressive patients: identification of proteins associated with lipid metabolism and immunoregulation. Int J Neuropsychopharmacol 2012, 15:1413-1425.
76. Yildirim F., Gertz K., Kronenberg G., Harms C., Fink K.B., Meisel A., et al. Inhibition of histone deacetylation protects wildtype but not gelsolin-deficient mice from ischemic brain injury. Exp Neurol 2008, 210:531-542.
77. Zee R.Y., Diehl K.A., Ridker P.M. Complement factor H Y402H gene polymorphism, a C-reactive protein, and risk of incident myocardial infarction, ischaemic stroke, and venous thromboembolism: a nested case-control study. Atherosclerosis 2006, 187:332-335.
78. Zheng P., Gao H.C., Li Q., Shao W.H., Zhang M.L., Cheng K., et al. Plasma metabonomics as a novel diagnostic approach for major depressive disorder. J Proteome Res 2012, 11:1741-1748.
79. Zimmermann-Ivol C.G., Burkhard P.R., Le Floch-Rohr J., Allard L., Hochstrasser D.F. Fatty acid binding protein as a serum marker for the early diagnosis of stroke a pilot study. Mol Cell Proteomics 2004, 3:66-72.