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

Published online by Cambridge University Press:  15 April 2020

Y. Zhan ,
Y.-T. Yang ,
H.-M. You ,
D. Cao ,
C.-Y. Liu ,
C.-J. Zhou ,
Z.-Y. Wang ,
S.-J. Bai ,
J. Mu  and
B. Wu
...Show all authors
Y. Zhan
Affiliation:
Chongqing Key Laboratory of Neurobiology, Chongqing, China Institute of Neuroscience, Chongqing Medical University, Chongqing, China
Y.-T. Yang
Affiliation:
Department of Neurology, The First Affiliated Hospital at Chongqing Medical University, 1, Yixue Road, Yuzhong District, Chongqing, 400016, China Chongqing Key Laboratory of Neurobiology, Chongqing, China Institute of Neuroscience, Chongqing Medical University, Chongqing, China
H.-M. You
Affiliation:
Chongqing Key Laboratory of Neurobiology, Chongqing, China Institute of Neuroscience, Chongqing Medical University, Chongqing, China
D. Cao
Affiliation:
Department of Neurology, The First Affiliated Hospital at Chongqing Medical University, 1, Yixue Road, Yuzhong District, Chongqing, 400016, China Chongqing Key Laboratory of Neurobiology, Chongqing, China Institute of Neuroscience, Chongqing Medical University, Chongqing, China
C.-Y. Liu
Affiliation:
Chongqing Key Laboratory of Neurobiology, Chongqing, China Institute of Neuroscience, Chongqing Medical University, Chongqing, China
C.-J. Zhou
Affiliation:
Department of Neurology, The First Affiliated Hospital at Chongqing Medical University, 1, Yixue Road, Yuzhong District, Chongqing, 400016, China Chongqing Key Laboratory of Neurobiology, Chongqing, China Institute of Neuroscience, Chongqing Medical University, Chongqing, China
Z.-Y. Wang
Affiliation:
Chongqing Key Laboratory of Neurobiology, Chongqing, China Institute of Neuroscience, Chongqing Medical University, Chongqing, China
S.-J. Bai
Affiliation:
Chongqing Key Laboratory of Neurobiology, Chongqing, China Institute of Neuroscience, Chongqing Medical University, Chongqing, China
J. Mu
Affiliation:
Department of Neurology, The First Affiliated Hospital at Chongqing Medical University, 1, Yixue Road, Yuzhong District, Chongqing, 400016, China Chongqing Key Laboratory of Neurobiology, Chongqing, China Institute of Neuroscience, Chongqing Medical University, Chongqing, China
B. Wu
Affiliation:
Chongqing Key Laboratory of Neurobiology, Chongqing, China Institute of Neuroscience, Chongqing Medical University, Chongqing, China
Q.-L. Zhan
Affiliation:
Department of Neurology, The Fifth People's Hospital of Chongqing, Chongqing, China
P. Xie*
Affiliation:
Department of Neurology, The First Affiliated Hospital at Chongqing Medical University, 1, Yixue Road, Yuzhong District, Chongqing, 400016, China Chongqing Key Laboratory of Neurobiology, Chongqing, China Institute of Neuroscience, Chongqing Medical University, Chongqing, China
*
*Corresponding author. Tel.: +86 23 68485490; fax: +86 23 68485111. E-mail address:[email protected] (P. Xie).
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Abstract

Background:

Post-stroke depression (PSD) is the most common psychiatric complication facing stroke survivors and has been associated with increased distress, physical disability, poor rehabilitation, and suicidal ideation. However, the pathophysiological mechanisms underlying PSD remain unknown, and no objective laboratory-based test is available to aid PSD diagnosis or monitor progression.

Methods:

Here, an isobaric tags for relative and absolute quantitation (iTRAQ)-based quantitative proteomic approach was performed to identify differentially expressed proteins in plasma samples obtained from PSD, stroke, and healthy control subjects.

Results:

The significantly differentiated proteins were primarily involved in lipid metabolism and immunoregulation. Six proteins associated with these processes – apolipoprotein A-IV (ApoA-IV), apolipoprotein C-II (ApoC-II), C-reactive protein (CRP), gelsolin, haptoglobin, and leucine-rich alpha-2-glycoprotein (LRG) – were selected for Western blotting validation. ApoA-IV expression was significantly upregulated in PSD as compared to stroke subjects. ApoC-II, LRG, and CRP expression were significantly downregulated in both PSD and HC subjects relative to stroke subjects. Gelsolin and haptoglobin expression were significantly dysregulated across all three groups with the following expression profiles: gelsolin, healthy control > PSD > stroke subjects; haptoglobin, stroke > PSD > healthy control.

Conclusions:

Early perturbation of lipid metabolism and immunoregulation may be involved in the pathophysiology of PSD. The combination of increased gelsolin levels accompanied by decreased haptoglobin levels shows promise as a plasma-based diagnostic biomarker panel for detecting increased PSD risk in post-stroke patients.

Keywords

Post-stroke depressionPSDStrokePlasmaProteomic
Type
Original articles
Information
European Psychiatry , Volume 29 , Issue 5 , June 2014 , pp. 307 - 315
Copyright
Copyright © Elsevier Masson SAS 2014

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Footnotes

1

These authors contributed equally to this study.

References

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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Berg, A., Lönnqvist, J., Palomäki, H., Kaste, M.Assessment of depression after stroke: a comparison of different screening instruments. Stroke 2009;40:523–529.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Black, S., Kushner, I., Samols, D.C-reactive protein. J Biol Chem 2004;279:48487–48490.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Brott, T., Adams, H.P. Jr., 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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Cojocaru, I.M., Cojocaru, M., Muşuroi, C., Druţă, A., Băcanu, M.Study of some markers of inflammation in atherothrombotic pathogenesis of acute ischemic stroke. Rom J Intern Med 2001;40:103–116.Google Scholar
de Maat, M.P., Kluft, C.The association between inflammation markers, coronary artery disease and smoking. Vasc Pharmacol 2002;39(3):137–139.CrossRefGoogle ScholarPubMed
Dennis, G. Jr., 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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.Google ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Huang, T.-L.Serum lipid profiles in major depression with clinical subtypes, suicide attempts and episodes. J Affect Disord 2005;86:75–79.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Janmey, P.A., Lind, S.E.Capacity of human serum to depolymerize actin filaments. Blood 1987;70:524–530.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.Google ScholarPubMed
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.Google ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Liesz, A, 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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Robinson, R., Starkstein, S., Price, T.Post-stroke depression and lesion location. Stroke 1988;19:125–126.CrossRefGoogle ScholarPubMed
Calabrò, R.S., Spadaro, L., Bramanti, P.Cerebrovascular Diseases: Post-stroke Depression and Anhedonia. In: Ritsner, M.S.Anhedonia: A Comprehensive Handbook Volume II New York, NY: Springer Netherlands publishing; 2014. p. 301–318.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Sacco, R.L.Newer risk factors for stroke. Neurology 2001;57:S31–S4.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Steinmetz, A., Utermann, G.Activation of lecithin: cholesterol acyltransferase by human apolipoprotein A-IV. J Biol Chem 1985;260:2258–2264.Google ScholarPubMed
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.Google Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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. http://dx.doi.org/10.3109/09638288.2014.884172.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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