Generic placeholder image

Current Protein & Peptide Science

Editor-in-Chief

ISSN (Print): 1389-2037
ISSN (Online): 1875-5550

Review Article

Application of Contemporary Neuroproteomic Techniques in Unravelling Neurological Disorders

Author(s): Mallika Khurana, Syed Obaidur Rahman, Abul Kalam Najmi, Faheem Hyder Pottoo and Md Sayeed Akhtar*

Volume 21, Issue 12, 2020

Page: [1146 - 1163] Pages: 18

DOI: 10.2174/1389203721666201104130135

Price: $65

conference banner
Abstract

Decades of research has stunned us with the very distinctive anatomy and physiology of our brain, and on the other hand, its complexity has always posed great difficulty in treating its dysfunction or damage. Understanding the brain under normal and, particularly in the diseased state, has always been very challenging and would have been impossible without proteomics. Neuroproteomic techniques have been extensively used for unraveling both dynamics and content of the proteome of our nervous system. This modern-day investigation and quantification of protein concentration and expression have given us a platform that enhances our knowledge on disease-associated processes and pathways modification and also leads to the identification of possible biomarkers that can be therapeutically targeted. With an increased interest in identifying and targeting possible biomarkers, this article focuses on describing applications of the much discussed neuroproteomics, with a significant role in the disease pathogenesis of some very common neurological disorders. This article will collectively discuss the use and relevance of neuroproteomics in a range of neurological diseases, such as Alzheimer’s disease, Parkinson’s disease, multiple sclerosis, epilepsy, and psychiatric disorders. We have also attempted to present the current successes and failures of the neuroproteomics approach on the results obtained from different clinical studies that targeted biomarkers associated with any particular neurological disorder.

Keywords: Neuroproteomic Techniques, neurological Disorders, Alzheimer’s disease, Parkinson’s disease, multiple sclerosis, epilepsy, psychiatric disorders, Omics.

[1]
Pottoo, F.H.; Tabassum, N.; Javed, M.N.; Nigar, S.; Sharma, S.; Barkat, M.A.; Harshita, ; Alam, M.S.; Ansari, M.A.; Barreto, G.E.; Ashraf, G.M. Raloxifene potentiates the effect of fluoxetine against maximal electroshock induced seizures in mice. Eur. J. Pharm. Sci., 2020, 146, 105261.
[http://dx.doi.org/10.1016/j.ejps.2020.105261] [PMID: 32061655]
[2]
Uddin, M.S.; Kabir, M.T.; Mamun, A.A.; Barreto, G.E.; Rashid, M.; Perveen, A.; Ashraf, G.M. Pharmacological approaches to mitigate neuroinflammation in Alzheimer’s disease. Int. Immunopharmacol., 2020, 84, 106479.
[http://dx.doi.org/10.1016/j.intimp.2020.106479] [PMID: 32353686]
[3]
Uddin, M.S.; Kabir, M.T.; Al Mamun, A.; Behl, T.; Mansouri, R.A.; Aloqbi, A.A.; Perveen, A.; Hafeez, A.; Ashraf, G.M. Exploring Potential of Alkaloidal Phytochemicals Targeting Neuroinflammatory Signaling of Alzheimer’s Disease. Curr. Pharm. Des., 2020.
[http://dx.doi.org/10.2174/1381612826666200531151004] [PMID: 32473620]
[4]
Joshi, K.; Ghodke, Y.; Shintre, P. Traditional medicine and genomics. J. Ayurveda Integr. Med., 2010, 1(1), 26-32.
[http://dx.doi.org/10.4103/0975-9476.59824] [PMID: 21829298]
[5]
Mohd Fauzi, F.; Koutsoukas, A.; Lowe, R.; Joshi, K.; Fan, T-P.; Glen, R.C.; Bender, A. Chemogenomics approaches to rationalizing the mode-of-action of traditional Chinese and Ayurvedic medicines. J. Chem. Inf. Model., 2013, 53(3), 661-673.
[http://dx.doi.org/10.1021/ci3005513] [PMID: 23351136]
[6]
Uddin, M.S.; Kabir, M.T.; Jakaria, M.; Sobarzo-Sánchez, E.; Barreto, G.E.; Perveen, A.; Hafeez, A.; Bin-Jumah, M.N.; Abdel-Daim, M.M.; Ashraf, G.M. Exploring the Potential of Neuroproteomics in Alzheimer’s Disease. Curr. Top. Med. Chem., 2020.
[http://dx.doi.org/10.2174/1568026620666200603112030] [PMID: 32493192]
[7]
Ibrahim, A.M.; Pottoo, F.H.; Dahiya, E.S.; Khan, F.A.; Kumar, J.B.S. Neuron-glia interactions: Molecular basis of alzheimer’s disease and applications of neuroproteomics. Eur. J. Neurosci., 2020, 52(2), 2931-2943.
[http://dx.doi.org/10.1111/ejn.14838] [PMID: 32463535]
[8]
Gulcicek, E.E.; Colangelo, C.M.; McMurray, W.; Stone, K.; Williams, K.; Wu, T.; Zhao, H.; Spratt, H.; Kurosky, A.; Wu, B. Proteomics and the analysis of proteomic data: an overview of current protein-profiling technologies. Curr. Protoc. Bioinformatics, 2005, Chapter 13(1), 1.
[http://dx.doi.org/10.1002/0471250953.bi1301s10] [PMID: 18428746]
[9]
Hudler, P.; Kocevar, N.; Komel, R. Proteomic approaches in biomarker discovery: new perspectives in cancer diagnostics. ScientificWorldJournal, 2014, 2014, 260348.
[http://dx.doi.org/10.1155/2014/260348] [PMID: 24550697]
[10]
Kitchen, R.R.; Rozowsky, J.S.; Gerstein, M.B.; Nairn, A.C. Decoding neuroproteomics: integrating the genome, translatome and functional anatomy. Nat. Neurosci., 2014, 17(11), 1491-1499.
[http://dx.doi.org/10.1038/nn.3829] [PMID: 25349915]
[11]
Bayés, A.; Grant, S.G. Neuroproteomics: understanding the molecular organization and complexity of the brain. Nat. Rev. Neurosci., 2009, 10(9), 635-646.
[http://dx.doi.org/10.1038/nrn2701] [PMID: 19693028]
[12]
Ultanir, S.K.; Yadav, S.; Hertz, N.T.; Oses-Prieto, J.A.; Claxton, S.; Burlingame, A.L.; Shokat, K.M.; Jan, L.Y.; Jan, Y-N. MST3 kinase phosphorylates TAO1/2 to enable Myosin Va function in promoting spine synapse development. Neuron, 2014, 84(5), 968-982.
[http://dx.doi.org/10.1016/j.neuron.2014.10.025] [PMID: 25456499]
[13]
Belin, S.; Nawabi, H.; Wang, C.; Tang, S.; Latremoliere, A.; Warren, P.; Schorle, H.; Uncu, C.; Woolf, C.J.; He, Z.; Steen, J.A. Injury-induced decline of intrinsic regenerative ability revealed by quantitative proteomics. Neuron, 2015, 86(4), 1000-1014.
[http://dx.doi.org/10.1016/j.neuron.2015.03.060] [PMID: 25937169]
[14]
Meleady, P. Two-dimensional gel electrophoresis and 2D-DIGE.Difference Gel Electrophoresis; Humana Press: New York, NY, 2018, pp. 3-14.
[http://dx.doi.org/10.1007/978-1-4939-7268-5_1]
[15]
Sutandy, F. R.; Qian, J.; Chen, C. S.; Zhu, H. MicroRNAs in alcoholic liver disease: Recent advances and future applications J. Cell. Physiol., 2013, 234(1), 382-394.
[http://dx.doi.org/10.1002/0471140864.ps2701s72]
[16]
Zhang, J.; Keene, C.D.; Pan, C.; Montine, K.S.; Montine, T.J. Proteomics of human neurodegenerative diseases. J. Neuropathol. Exp. Neurol., 2008, 67(10), 923-932.
[http://dx.doi.org/10.1097/NEN.0b013e318187a832] [PMID: 18800015]
[17]
Gygi, S.P.; Rist, B.; Gerber, S.A.; Turecek, F.; Gelb, M.H.; Aebersold, R. Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nat. Biotechnol., 1999, 17(10), 994-999.
[http://dx.doi.org/10.1038/13690] [PMID: 10504701]
[18]
Liao, L.; Park, S.K.; Xu, T.; Vanderklish, P.; Yates, J.R., III Quantitative proteomic analysis of primary neurons reveals diverse changes in synaptic protein content in fmr1 knockout mice. Proc. Natl. Acad. Sci. USA, 2008, 105(40), 15281-15286.
[http://dx.doi.org/10.1073/pnas.0804678105] [PMID: 18829439]
[19]
Kitteringham, N.R.; Jenkins, R.E.; Lane, C.S.; Elliott, V.L.; Park, B.K. Multiple reaction monitoring for quantitative biomarker analysis in proteomics and metabolomics. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci., 2009, 877(13), 1229-1239.
[http://dx.doi.org/10.1016/j.jchromb.2008.11.013] [PMID: 19041286]
[20]
Lange, V.; Picotti, P.; Domon, B.; Aebersold, R. Selected reaction monitoring for quantitative proteomics: a tutorial. Mol. Syst. Biol., 2008, 4(1), 222.
[http://dx.doi.org/10.1038/msb.2008.61] [PMID: 18854821]
[21]
Picotti, P.; Aebersold, R. Selected reaction monitoring-based proteomics: workflows, potential, pitfalls and future directions. Nat. Methods, 2012, 9(6), 555-566.
[http://dx.doi.org/10.1038/nmeth.2015] [PMID: 22669653]
[22]
Chang, C.-Y.; Picotti, P.; Hüttenhain, R.; Heinzelmann-Schwarz, V.; Jovanovic, M.; Aebersold, R.; Vitek, O. PGE2 induces apoptosis of hepatic stellate cells and attenuates liver fibrosis in mice by downregulating miR-23a-5p and miR-28a-5p. Biochim. Biophys. Acta Mol. Basis Dis., 2012.
[23]
Rahman, S.O.; Singh, R.K.; Hussain, S.; Akhtar, M.; Najmi, A.K. A novel therapeutic potential of cysteinyl leukotrienes and their receptors modulation in the neurological complications associated with Alzheimer’s disease. Eur. J. Pharmacol., 2019, 842, 208-220.
[http://dx.doi.org/10.1016/j.ejphar.2018.10.040] [PMID: 30389631]
[24]
Blennow, K.; Zetterberg, H. The past and the future of Alzheimer’s disease CSF biomarkers-a journey toward validated biochemical tests covering the whole spectrum of molecular events. Front. Neurosci., 2015, 9, 345.
[http://dx.doi.org/10.3389/fnins.2015.00345] [PMID: 26483625]
[25]
Galasko, D. Expanding the repertoire of biomarkers for Alzheimer’s disease: targeted and non-targeted approaches. Front. Neurol., 2015, 6, 256.
[http://dx.doi.org/10.3389/fneur.2015.00256] [PMID: 26733934]
[26]
Blennow, K.; Hampel, H.; Weiner, M.; Zetterberg, H. Cerebrospinal fluid and plasma biomarkers in Alzheimer disease. Nat. Rev. Neurol., 2010, 6(3), 131-144.
[http://dx.doi.org/10.1038/nrneurol.2010.4] [PMID: 20157306]
[27]
Rahman, S.O.; Panda, B.P.; Parvez, S.; Kaundal, M.; Hussain, S.; Akhtar, M.; Najmi, A.K. Neuroprotective role of astaxanthin in hippocampal insulin resistance induced by Aβ peptides in animal model of Alzheimer’s disease. Biomed. Pharmacother., 2019, 110, 47-58.
[http://dx.doi.org/10.1016/j.biopha.2018.11.043] [PMID: 30463045]
[28]
Andreev, V.P.; Petyuk, V.A.; Brewer, H.M.; Karpievitch, Y.V.; Xie, F.; Clarke, J.; Camp, D.; Smith, R.D.; Lieberman, A.P.; Albin, R.L.; Nawaz, Z.; El Hokayem, J.; Myers, A.J. Label-free quantitative LC-MS proteomics of Alzheimer’s disease and normally aged human brains. J. Proteome Res., 2012, 11(6), 3053-3067.
[http://dx.doi.org/10.1021/pr3001546] [PMID: 22559202]
[29]
Jagust, W.J.; Bandy, D.; Chen, K.; Foster, N.L.; Landau, S.M.; Mathis, C.A.; Price, J.C.; Reiman, E.M.; Skovronsky, D.; Koeppe, R.A. The Alzheimer’s Disease Neuroimaging Initiative positron emission tomography core. Alzheimers Dement., 2010, 6(3), 221-229.
[http://dx.doi.org/10.1016/j.jalz.2010.03.003] [PMID: 20451870]
[30]
Langbaum, J.B.; Chen, K.; Lee, W.; Reschke, C.; Bandy, D.; Fleisher, A.S.; Alexander, G.E.; Foster, N.L.; Weiner, M.W.; Koeppe, R.A.; Jagust, W.J.; Reiman, E.M. Categorical and correlational analyses of baseline fluorodeoxyglucose positron emission tomography images from the Alzheimer’s Disease Neuroimaging Initiative (ADNI). Neuroimage, 2009, 45(4), 1107-1116.
[http://dx.doi.org/10.1016/j.neuroimage.2008.12.072] [PMID: 19349228]
[31]
Cohen, A.D.; Rabinovici, G.D.; Mathis, C.A.; Jagust, W.J.; Klunk, W.E.; Ikonomovic, M.D. Using Pittsburgh Compound B for in vivo PET imaging of fibrillar amyloid-beta.Advances in pharmacology; Elsevier, 2012, Vol. 64, pp. 27-81.
[32]
Craig-Schapiro, R.; Perrin, R.J.; Roe, C.M.; Xiong, C.; Carter, D.; Cairns, N.J.; Mintun, M.A.; Peskind, E.R.; Li, G.; Galasko, D.R.; Clark, C.M.; Quinn, J.F.; D’Angelo, G.; Malone, J.P.; Townsend, R.R.; Morris, J.C.; Fagan, A.M.; Holtzman, D.M. YKL-40: a novel prognostic fluid biomarker for preclinical Alzheimer’s disease. Biol. Psychiatry, 2010, 68(10), 903-912.
[http://dx.doi.org/10.1016/j.biopsych.2010.08.025] [PMID: 21035623]
[33]
Perrin, R.J.; Craig-Schapiro, R.; Malone, J.P.; Shah, A.R.; Gilmore, P.; Davis, A.E.; Roe, C.M.; Peskind, E.R.; Li, G.; Galasko, D.R.; Clark, C.M.; Quinn, J.F.; Kaye, J.A.; Morris, J.C.; Holtzman, D.M.; Townsend, R.R.; Fagan, A.M. Identification and validation of novel cerebrospinal fluid biomarkers for staging early Alzheimer’s disease. PLoS One, 2011, 6(1), e16032.
[http://dx.doi.org/10.1371/journal.pone.0016032] [PMID: 21264269]
[34]
Lönneborg, A. Biomarkers for Alzheimer disease in cerebrospinal fluid, urine, and blood. Mol. Diagn. Ther., 2008, 12(5), 307-320.
[http://dx.doi.org/10.1007/BF03256296] [PMID: 18803429]
[35]
De La Monte, S.M.; Wands, J.R. The AD7c-NTP neuronal thread protein biomarker for detecting Alzheimer’s disease. J. Alzheimers Dis., 2001, 3(3), 345-353.
[http://dx.doi.org/10.3233/JAD-2001-3310] [PMID: 12214056]
[36]
Farrer, L.A.; Cupples, L.A.; Haines, J.L.; Hyman, B.; Kukull, W.A.; Mayeux, R.; Myers, R.H.; Pericak-Vance, M.A.; Risch, N.; van Duijn, C.M. APOE and Alzheimer Disease Meta Analysis Consortium. Effects of age, sex, and ethnicity on the association between apolipoprotein E genotype and Alzheimer disease. A meta-analysis. JAMA, 1997, 278(16), 1349-1356.
[http://dx.doi.org/10.1001/jama.1997.03550160069041] [PMID: 9343467]
[37]
Schaffer, C.; Sarad, N.; DeCrumpe, A.; Goswami, D.; Herrmann, S.; Morales, J.; Patel, P.; Osborne, J. Biomarkers in the diagnosis and prognosis of Alzheimer’s disease. J. Lab. Autom., 2015, 20(5), 589-600.
[http://dx.doi.org/10.1177/2211068214559979] [PMID: 25424384]
[38]
Baird, A.L.; Westwood, S.; Lovestone, S. Blood-based proteomic biomarkers of Alzheimer’s disease pathology. Front. Neurol., 2015, 6, 236.
[http://dx.doi.org/10.3389/fneur.2015.00236] [PMID: 26635716]
[39]
Perneczky, R.; Guo, L-H. Plasma proteomics biomarkers in Alzheimer’s disease: latest advances and challenges.Systems Biology of Alzheimer’s Disease; Springer, 2016, pp. 521-529.
[http://dx.doi.org/10.1007/978-1-4939-2627-5_32]
[40]
Lee, K.S.; Chung, J.H.; Choi, T.K.; Suh, S.Y.; Oh, B.H.; Hong, C.H. Peripheral cytokines and chemokines in Alzheimer’s disease. Dement. Geriatr. Cogn. Disord., 2009, 28(4), 281-287.
[http://dx.doi.org/10.1159/000245156] [PMID: 19828948]
[41]
Clark, L.F.; Kodadek, T. The immune system and neuroinflammation as potential sources of blood-based biomarkers for Alzheimer’s disease, Parkinson’s disease, and Huntington’s disease. ACS Chem. Neurosci., 2016, 7(5), 520-527.
[http://dx.doi.org/10.1021/acschemneuro.6b00042] [PMID: 27046268]
[42]
Kiddle, S.J.; Steves, C.J.; Mehta, M.; Simmons, A.; Xu, X.; Newhouse, S.; Sattlecker, M.; Ashton, N.J.; Bazenet, C.; Killick, R.; Adnan, J.; Westman, E.; Nelson, S.; Soininen, H.; Kloszewska, I.; Mecocci, P.; Tsolaki, M.; Vellas, B.; Curtis, C.; Breen, G.; Williams, S.C.; Lovestone, S.; Spector, T.D.; Dobson, R.J. Plasma protein biomarkers of Alzheimer’s disease endophenotypes in asymptomatic older twins: early cognitive decline and regional brain volumes. Transl. Psychiatry, 2015, 5(6), e584.
[http://dx.doi.org/10.1038/tp.2015.78] [PMID: 26080319]
[43]
Gasser, T. Genetics of Parkinson’s disease. Curr. Opin. Neurol., 2005, 18(4), 363-369.
[http://dx.doi.org/10.1097/01.wco.0000170951.08924.3d] [PMID: 16003110]
[44]
Bonifati, V.; Oostra, B.A.; Heutink, P. Unraveling the pathogenesis of Parkinson’s disease--the contribution of monogenic forms. Cell. Mol. Life Sci., 2004, 61(14), 1729-1750.
[http://dx.doi.org/10.1007/s00018-004-4104-1] [PMID: 15241550]
[45]
Hardy, J.; Cai, H.; Cookson, M.R.; Gwinn-Hardy, K.; Singleton, A. Genetics of Parkinson’s disease and parkinsonism. Ann. Neurol., 2006, 60(4), 389-398.
[http://dx.doi.org/10.1002/ana.21022] [PMID: 17068789]
[46]
Qiang, J.K.; Wong, Y.C.; Siderowf, A.; Hurtig, H.I.; Xie, S.X.; Lee, V.M.Y.; Trojanowski, J.Q.; Yearout, D.; B Leverenz, J.; Montine, T.J.; Stern, M.; Mendick, S.; Jennings, D.; Zabetian, C.; Marek, K.; Chen-Plotkin, A.S. Plasma apolipoprotein A1 as a biomarker for Parkinson disease. Ann. Neurol., 2013, 74(1), 119-127.
[http://dx.doi.org/10.1002/ana.23872] [PMID: 23447138]
[47]
Swanson, C.R.; Li, K.; Unger, T.L.; Gallagher, M.D.; Van Deerlin, V.M.; Agarwal, P.; Leverenz, J.; Roberts, J.; Samii, A.; Gross, R.G.; Hurtig, H.; Rick, J.; Weintraub, D.; Trojanowski, J.Q.; Zabetian, C.; Chen-Plotkin, A.S. Lower plasma apolipoprotein A1 levels are found in Parkinson’s disease and associate with apolipoprotein A1 genotype. Mov. Disord., 2015, 30(6), 805-812.
[http://dx.doi.org/10.1002/mds.26022] [PMID: 25227208]
[48]
Harrington, M.G.; Merril, C.R. Two-dimensional electrophoresis and “ultrasensitive” silver staining of cerebrospinal fluid proteins in neurological diseases. Clin. Chem., 1984, 30(12 Pt 1), 1933-1937.
[http://dx.doi.org/10.1093/clinchem/30.12.1933] [PMID: 6209029]
[49]
Wang, E.S.; Sun, Y.; Guo, J.G.; Gao, X.; Hu, J.W.; Zhou, L.; Hu, J.; Jiang, C.C. Tetranectin and apolipoprotein A-I in cerebrospinal fluid as potential biomarkers for Parkinson’s disease. Acta Neurol. Scand., 2010, 122(5), 350-359.
[http://dx.doi.org/10.1111/j.1600-0404.2009.01318.x] [PMID: 20085559]
[50]
Abdi, F.; Quinn, J.F.; Jankovic, J.; McIntosh, M.; Leverenz, J.B.; Peskind, E.; Nixon, R.; Nutt, J.; Chung, K.; Zabetian, C.; Samii, A.; Lin, M.; Hattan, S.; Pan, C.; Wang, Y.; Jin, J.; Zhu, D.; Li, G.J.; Liu, Y.; Waichunas, D.; Montine, T.J.; Zhang, J. Detection of biomarkers with a multiplex quantitative proteomic platform in cerebrospinal fluid of patients with neurodegenerative disorders. J. Alzheimers Dis., 2006, 9(3), 293-348.
[http://dx.doi.org/10.3233/JAD-2006-9309] [PMID: 16914840]
[51]
Brooks, B.R.; Miller, R.G.; Swash, M.; Munsat, T.L. World Federation of Neurology Research Group on Motor Neuron Diseases. El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. Other Motor Neuron Disord., 2000, 1(5), 293-299.
[http://dx.doi.org/10.1080/146608200300079536] [PMID: 11464847]
[52]
Hong, Z.; Shi, M.; Chung, K.A.; Quinn, J.F.; Peskind, E.R.; Galasko, D.; Jankovic, J.; Zabetian, C.P.; Leverenz, J.B.; Baird, G.; Montine, T.J.; Hancock, A.M.; Hwang, H.; Pan, C.; Bradner, J.; Kang, U.J.; Jensen, P.H.; Zhang, J. DJ-1 and α-synuclein in human cerebrospinal fluid as biomarkers of Parkinson’s disease. Brain, 2010, 133(Pt 3), 713-726.
[http://dx.doi.org/10.1093/brain/awq008] [PMID: 20157014]
[53]
Wijesekera, L.C.; Leigh, P.N. Amyotrophic lateral sclerosis. Orphanet J. Rare Dis., 2009, 4(1), 3.
[http://dx.doi.org/10.1186/1750-1172-4-3] [PMID: 19192301]
[54]
Zhang, J.; Sokal, I.; Peskind, E.R.; Quinn, J.F.; Jankovic, J.; Kenney, C.; Chung, K.A.; Millard, S.P.; Nutt, J.G.; Montine, T.J. CSF multianalyte profile distinguishes Alzheimer and Parkinson diseases. Am. J. Clin. Pathol., 2008, 129(4), 526-529.
[http://dx.doi.org/10.1309/W01Y0B808EMEH12L] [PMID: 18343778]
[55]
Zetterström, R.H.; Solomin, L.; Jansson, L.; Hoffer, B.J.; Olson, L.; Perlmann, T. Dopamine neuron agenesis in Nurr1-deficient mice. Science, 1997, 276(5310), 248-250.
[http://dx.doi.org/10.1126/science.276.5310.248] [PMID: 9092472]
[56]
Krezel, W.; Ghyselinck, N.; Samad, T.A.; Dupé, V.; Kastner, P.; Borrelli, E.; Chambon, P. Impaired locomotion and dopamine signaling in retinoid receptor mutant mice. Science, 1998, 279(5352), 863-867.
[http://dx.doi.org/10.1126/science.279.5352.863] [PMID: 9452386]
[57]
Öhrfelt, A.; Zetterberg, H.; Andersson, K.; Persson, R.; Secic, D.; Brinkmalm, G.; Wallin, A.; Mulugeta, E.; Francis, P.T.; Vanmechelen, E.; Aarsland, D.; Ballard, C.; Blennow, K.; Westman-Brinkmalm, A. Identification of novel α-synuclein isoforms in human brain tissue by using an online nanoLC-ESI-FTICR-MS method. Neurochem. Res., 2011, 36(11), 2029-2042.
[http://dx.doi.org/10.1007/s11064-011-0527-x] [PMID: 21674238]
[58]
Basso, M.; Giraudo, S.; Corpillo, D.; Bergamasco, B.; Lopiano, L.; Fasano, M. Proteome analysis of human substantia nigra in Parkinson’s disease. Proteomics, 2004, 4(12), 3943-3952.
[http://dx.doi.org/10.1002/pmic.200400848] [PMID: 15526345]
[59]
Basso, M.; Giraudo, S.; Lopiano, L.; Bergamasco, B.; Bosticco, E.; Cinquepalmi, A.; Fasano, M. Proteome analysis of mesencephalic tissues: evidence for Parkinson’s disease. Neurol. Sci., 2003, 24(3), 155-156.
[http://dx.doi.org/10.1007/s10072-003-0106-2] [PMID: 14598063]
[60]
Werner, C.J.; Heyny-von Haussen, R.; Mall, G.; Wolf, S. Proteome analysis of human substantia nigra in Parkinson’s disease. Proteome Sci., 2008, 6(1), 8.
[http://dx.doi.org/10.1186/1477-5956-6-8] [PMID: 18275612]
[61]
Gabibov, A.G.; Belogurov, A.A., Jr; Lomakin, Y.A.; Zakharova, M.Y.; Avakyan, M.E.; Dubrovskaya, V.V.; Smirnov, I.V.; Ivanov, A.S.; Molnar, A.A.; Gurtsevitch, V.E.; Diduk, S.V.; Smirnova, K.V.; Avalle, B.; Sharanova, S.N.; Tramontano, A.; Friboulet, A.; Boyko, A.N.; Ponomarenko, N.A.; Tikunova, N.V. Combinatorial antibody library from multiple sclerosis patients reveals antibodies that cross-react with myelin basic protein and EBV antigen. FASEB J., 2011, 25(12), 4211-4221.
[http://dx.doi.org/10.1096/fj.11-190769] [PMID: 21859892]
[62]
Lucca, L.E.; Desbois, S.; Ramadan, A.; Ben-Nun, A.; Eisenstein, M.; Carrié, N.; Guéry, J-C.; Sette, A.; Nguyen, P.; Geiger, T.L.; Mars, L.T.; Liblau, R.S. Bispecificity for myelin and neuronal self-antigens is a common feature of CD4 T cells in C57BL/6 mice. J. Immunol., 2014, 193(7), 3267-3277.
[http://dx.doi.org/10.4049/jimmunol.1400523] [PMID: 25135834]
[63]
Bäumer, D.; Talbot, K.; Turner, M.R. Advances in motor neurone disease. J. R. Soc. Med., 2014, 107(1), 14-21.
[http://dx.doi.org/10.1177/0141076813511451] [PMID: 24399773]
[64]
Al-Chalabi, A.; Hardiman, O. The epidemiology of ALS: a conspiracy of genes, environment and time. Nat. Rev. Neurol., 2013, 9(11), 617-628.
[http://dx.doi.org/10.1038/nrneurol.2013.203] [PMID: 24126629]
[65]
Goldknopf, I.L.; Sheta, E.A.; Bryson, J.; Folsom, B.; Wilson, C.; Duty, J.; Yen, A.A.; Appel, S.H. Complement C3c and related protein biomarkers in amyotrophic lateral sclerosis and Parkinson’s disease. Biochem. Biophys. Res. Commun., 2006, 342(4), 1034-1039.
[http://dx.doi.org/10.1016/j.bbrc.2006.02.051] [PMID: 16516157]
[66]
O’Loughlin, E.; Madore, C.; Lassmann, H.; Butovsky, O. Microglial phenotypes and functions in multiple sclerosis. Cold Spring Harb. Perspect. Med., 2018, 8(2), a028993.
[http://dx.doi.org/10.1101/cshperspect.a028993] [PMID: 29419406]
[67]
Feigin, V.L.; Abajobir, A.A.; Abate, K.H.; Abd-Allah, F.; Abdulle, A.M.; Abera, S.F.; Abyu, G.Y.; Ahmed, M.B.; Aichour, A.N.; Aichour, I. GBD 2015 Neurological Disorders Collaborator Group. Global, regional, and national burden of neurological disorders during 1990-2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet Neurol., 2017, 16(11), 877-897.
[http://dx.doi.org/10.1016/S1474-4422(17)30299-5] [PMID: 28931491]
[68]
Dobson, R.; Giovannoni, G. Multiple sclerosis - a review. Eur. J. Neurol., 2019, 26(1), 27-40.
[http://dx.doi.org/10.1111/ene.13819] [PMID: 30300457]
[69]
Lassmann, H. Multiple sclerosis pathology. Cold Spring Harb. Perspect. Med., 2018, 8(3), a028936.
[http://dx.doi.org/10.1101/cshperspect.a028936] [PMID: 29358320]
[70]
Brownlee, W.J.; Hardy, T.A.; Fazekas, F.; Miller, D.H. Diagnosis of multiple sclerosis: progress and challenges. Lancet, 2017, 389(10076), 1336-1346.
[http://dx.doi.org/10.1016/S0140-6736(16)30959-X] [PMID: 27889190]
[71]
McDonald, W.I.; Compston, A.; Edan, G.; Goodkin, D.; Hartung, H.P.; Lublin, F.D.; McFarland, H.F.; Paty, D.W.; Polman, C.H.; Reingold, S.C.; Sandberg-Wollheim, M.; Sibley, W.; Thompson, A.; van den Noort, S.; Weinshenker, B.Y.; Wolinsky, J.S. Recommended diagnostic criteria for multiple sclerosis: guidelines from the International Panel on the diagnosis of multiple sclerosis. Ann. Neurol., 2001, 50(1), 121-127.
[http://dx.doi.org/10.1002/ana.1032] [PMID: 11456302]
[72]
Singh, V.; Hintzen, R.Q.; Luider, T.M.; Stoop, M.P. Proteomics technologies for biomarker discovery in multiple sclerosis. J. Neuroimmunol., 2012, 248(1-2), 40-47.
[http://dx.doi.org/10.1016/j.jneuroim.2011.11.004] [PMID: 22129845]
[73]
Ghaste, M.; Mistrik, R.; Shulaev, V. Applications of Fourier transform ion cyclotron resonance (FT-ICR) and orbitrap based high resolution mass spectrometry in metabolomics and lipidomics. Int. J. Mol. Sci., 2016, 17(6), 816.
[http://dx.doi.org/10.3390/ijms17060816] [PMID: 27231903]
[74]
Kroksveen, A.C.; Jaffe, J.D.; Aasebø, E.; Barsnes, H.; Bjørlykke, Y.; Franciotta, D.; Keshishian, H.; Myhr, K.M.; Opsahl, J.A.; van Pesch, V.; Teunissen, C.E.; Torkildsen, Ø.; Ulvik, R.J.; Vethe, H.; Carr, S.A.; Berven, F.S. Quantitative proteomics suggests decrease in the secretogranin-1 cerebrospinal fluid levels during the disease course of multiple sclerosis. Proteomics, 2015, 15(19), 3361-3369.
[http://dx.doi.org/10.1002/pmic.201400142] [PMID: 26152395]
[75]
Kroksveen, A.C.; Guldbrandsen, A.; Vaudel, M.; Lereim, R.R.; Barsnes, H.; Myhr, K-M.; Torkildsen, Ø.; Berven, F.S. In-depth cerebrospinal fluid quantitative proteome and deglycoproteome analysis: presenting a comprehensive picture of pathways and processes affected by multiple sclerosis. J. Proteome Res., 2017, 16(1), 179-194.
[http://dx.doi.org/10.1021/acs.jproteome.6b00659] [PMID: 27728768]
[76]
Ottervald, J.; Franzén, B.; Nilsson, K.; Andersson, L.I.; Khademi, M.; Eriksson, B.; Kjellström, S.; Marko-Varga, G.; Végvári, A.; Harris, R.A.; Laurell, T.; Miliotis, T.; Matusevicius, D.; Salter, H.; Ferm, M.; Olsson, T. Multiple sclerosis: Identification and clinical evaluation of novel CSF biomarkers. J. Proteomics, 2010, 73(6), 1117-1132.
[http://dx.doi.org/10.1016/j.jprot.2010.01.004] [PMID: 20093204]
[77]
Harris, V.K.; Donelan, N.; Yan, Q.J.; Clark, K.; Touray, A.; Rammal, M.; Sadiq, S.A. Cerebrospinal fluid fetuin-A is a biomarker of active multiple sclerosis. Mult. Scler., 2013, 19(11), 1462-1472.
[http://dx.doi.org/10.1177/1352458513477923] [PMID: 23439582]
[78]
Stoop, M.P.; Dekker, L.J.; Titulaer, M.K.; Burgers, P.C.; Sillevis Smitt, P.A.; Luider, T.M.; Hintzen, R.Q. Multiple sclerosis-related proteins identified in cerebrospinal fluid by advanced mass spectrometry. Proteomics, 2008, 8(8), 1576-1585.
[http://dx.doi.org/10.1002/pmic.200700446] [PMID: 18351689]
[79]
Kroksveen, A.C.; Guldbrandsen, A.; Vedeler, C.; Myhr, K.M.; Opsahl, J.A.; Berven, F.S. Cerebrospinal fluid proteome comparison between multiple sclerosis patients and controls. Acta Neurol. Scand. Suppl., 2012, 126(195), 90-96.
[http://dx.doi.org/10.1111/ane.12029] [PMID: 23278663]
[80]
Hinsinger, G.; Galéotti, N.; Nabholz, N.; Urbach, S.; Rigau, V.; Demattei, C.; Lehmann, S.; Camu, W.; Labauge, P.; Castelnovo, G.; Brassat, D.; Loussouarn, D.; Salou, M.; Laplaud, D.; Casez, O.; Bockaert, J.; Marin, P.; Thouvenot, E. Chitinase 3-like proteins as diagnostic and prognostic biomarkers of multiple sclerosis. Mult. Scler., 2015, 21(10), 1251-1261.
[http://dx.doi.org/10.1177/1352458514561906] [PMID: 25698171]
[81]
Pavelek, Z.; Vyšata, O.; Tambor, V.; Pimková, K.; Vu, D.L.; Kuča, K.; Šťourač, P.; Vališ, M. Proteomic analysis of cerebrospinal fluid for relapsing-remitting multiple sclerosis and clinically isolated syndrome. Biomed. Rep., 2016, 5(1), 35-40.
[http://dx.doi.org/10.3892/br.2016.668] [PMID: 27347402]
[82]
Timirci-Kahraman, O.; Karaaslan, Z.; Tuzun, E.; Kurtuncu, M.; Baykal, A.T.; Gunduz, T.; Tuzuner, M.B.; Akgun, E.; Gurel, B.; Eraksoy, M.; Kucukali, C.I. Identification of candidate biomarkers in converting and non-converting clinically isolated syndrome by proteomics analysis of cerebrospinal fluid. Acta Neurol. Belg., 2019, 119(1), 101-111.
[http://dx.doi.org/10.1007/s13760-018-0954-4] [PMID: 29873030]
[83]
Singh, V.; Tripathi, A.; Dutta, R. Proteomic approaches to decipher mechanisms underlying pathogenesis in multiple sclerosis patients. Proteomics, 2019, 19(16), e1800335.
[http://dx.doi.org/10.1002/pmic.201800335] [PMID: 31119864]
[84]
Lewin, A.; Hamilton, S.; Witkover, A.; Langford, P.; Nicholas, R.; Chataway, J.; Bangham, C.R.M. Free serum haemoglobin is associated with brain atrophy in secondary progressive multiple sclerosis. Wellcome Open Res., 2016, 1, 10.
[http://dx.doi.org/10.12688/wellcomeopenres.9967.2] [PMID: 27996064]
[85]
Byström, S.; Ayoglu, B.; Häggmark, A.; Mitsios, N.; Hong, M-G.; Drobin, K.; Forsström, B.; Fredolini, C.; Khademi, M.; Amor, S.; Uhlén, M.; Olsson, T.; Mulder, J.; Nilsson, P.; Schwenk, J.M. Affinity proteomic profiling of plasma, cerebrospinal fluid, and brain tissue within multiple sclerosis. J. Proteome Res., 2014, 13(11), 4607-4619.
[http://dx.doi.org/10.1021/pr500609e] [PMID: 25231264]
[86]
Amin, B.; Maurer, A.; Voelter, W.; Melms, A.; Kalbacher, H. New poteintial serum biomarkers in multiple sclerosis identified by proteomic strategies. Curr. Med. Chem., 2014, 21(13), 1544-1556.
[http://dx.doi.org/10.2174/09298673113206660311] [PMID: 24180278]
[87]
Tremlett, H.; Dai, D.L.; Hollander, Z.; Kapanen, A.; Aziz, T.; Wilson-McManus, J.E.; Tebbutt, S.J.; Borchers, C.H.; Oger, J.; Cohen Freue, G.V. Serum proteomics in multiple sclerosis disease progression. J. Proteomics, 2015, 118, 2-11.
[http://dx.doi.org/10.1016/j.jprot.2015.02.018] [PMID: 25753122]
[88]
Yin, L.; Liu, J.; Dong, H.; Xu, E.; Qiao, Y.; Wang, L.; Zhang, L.; Jia, J.; Li, L.; Geng, X. Autophagy-related gene16L2, a potential serum biomarker of multiple sclerosis evaluated by bead-based proteomic technology. Neurosci. Lett., 2014, 562, 34-38.
[http://dx.doi.org/10.1016/j.neulet.2013.12.070] [PMID: 24406150]
[89]
Nishihara, H.; Shimizu, F.; Kitagawa, T.; Yamanaka, N.; Akada, J.; Kuramitsu, Y.; Sano, Y.; Takeshita, Y.; Maeda, T.; Abe, M.; Koga, M.; Nakamura, K.; Kanda, T. Identification of galectin-3 as a possible antibody target for secondary progressive multiple sclerosis. Mult. Scler., 2017, 23(3), 382-394.
[http://dx.doi.org/10.1177/1352458516655217] [PMID: 27339072]
[90]
Fiorini, A.; Koudriavtseva, T.; Bucaj, E.; Coccia, R.; Foppoli, C.; Giorgi, A.; Schininà, M.E.; Di Domenico, F.; De Marco, F.; Perluigi, M. Involvement of oxidative stress in occurrence of relapses in multiple sclerosis: the spectrum of oxidatively modified serum proteins detected by proteomics and redox proteomics analysis. PLoS One, 2013, 8(6), e65184.
[http://dx.doi.org/10.1371/journal.pone.0065184] [PMID: 23762311]
[91]
Ayoglu, B.; Mitsios, N.; Kockum, I.; Khademi, M.; Zandian, A.; Sjöberg, R.; Forsström, B.; Bredenberg, J.; Lima Bomfim, I.; Holmgren, E.; Grönlund, H.; Guerreiro-Cacais, A.O.; Abdelmagid, N.; Uhlén, M.; Waterboer, T.; Alfredsson, L.; Mulder, J.; Schwenk, J.M.; Olsson, T.; Nilsson, P. Anoctamin 2 identified as an autoimmune target in multiple sclerosis. Proc. Natl. Acad. Sci. USA, 2016, 113(8), 2188-2193.
[http://dx.doi.org/10.1073/pnas.1518553113] [PMID: 26862169]
[92]
Han, M.H.; Hwang, S-I.; Roy, D.B.; Lundgren, D.H.; Price, J.V.; Ousman, S.S.; Fernald, G.H.; Gerlitz, B.; Robinson, W.H.; Baranzini, S.E.; Grinnell, B.W.; Raine, C.S.; Sobel, R.A.; Han, D.K.; Steinman, L. Proteomic analysis of active multiple sclerosis lesions reveals therapeutic targets. Nature, 2008, 451(7182), 1076-1081.
[http://dx.doi.org/10.1038/nature06559] [PMID: 18278032]
[93]
Syed, Y.A.; Zhao, C.; Mahad, D.; Möbius, W.; Altmann, F.; Foss, F.; González, G.A.; Sentürk, A.; Acker-Palmer, A.; Lubec, G.; Lilley, K.; Franklin, R.J.M.; Nave, K.A.; Kotter, M.R.N. Antibody-mediated neutralization of myelin-associated EphrinB3 accelerates CNS remyelination. Acta Neuropathol., 2016, 131(2), 281-298.
[http://dx.doi.org/10.1007/s00401-015-1521-1] [PMID: 26687980]
[94]
Maccarrone, G.; Nischwitz, S.; Deininger, S-O.; Hornung, J.; König, F.B.; Stadelmann, C.; Turck, C.W.; Weber, F. MALDI imaging mass spectrometry analysis-A new approach for protein mapping in multiple sclerosis brain lesions. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci., 2017, 1047, 131-140.
[http://dx.doi.org/10.1016/j.jchromb.2016.07.001] [PMID: 27461358]
[95]
Vartiainen, N.; Pyykönen, I.; Hökfelt, T.; Koistinaho, J. Induction of thymosin beta(4) mRNA following focal brain ischemia. Neuroreport, 1996, 7(10), 1613-1616.
[http://dx.doi.org/10.1097/00001756-199607080-00017] [PMID: 8904767]
[96]
Santra, M.; Chopp, M.; Zhang, Z.G.; Lu, M.; Santra, S.; Nalani, A.; Santra, S.; Morris, D.C. Thymosin β 4 mediates oligodendrocyte differentiation by upregulating p38 MAPK. Glia, 2012, 60(12), 1826-1838.
[http://dx.doi.org/10.1002/glia.22400] [PMID: 23073962]
[97]
Liguori, M.; Qualtieri, A.; Tortorella, C.; Direnzo, V.; Bagalà, A.; Mastrapasqua, M.; Spadafora, P.; Trojano, M. Proteomic profiling in multiple sclerosis clinical courses reveals potential biomarkers of neurodegeneration. PLoS One, 2014, 9(8), e103984.
[http://dx.doi.org/10.1371/journal.pone.0103984] [PMID: 25098164]
[98]
Brown, N.; Alkhayer, K.; Clements, R.; Singhal, N.; Gregory, R.; Azzam, S.; Li, S.; Freeman, E.; McDonough, J. Neuronal hemoglobin expression and its relevance to multiple sclerosis neuropathology. J. Mol. Neurosci., 2016, 59(1), 1-17.
[http://dx.doi.org/10.1007/s12031-015-0711-6] [PMID: 26809286]
[99]
Singh, V.; Stingl, C.; Stoop, M.P.; Zeneyedpour, L.; Neuteboom, R.F.; Smitt, P.S.; Hintzen, R.Q.; Luider, T.M. Proteomics urine analysis of pregnant women suffering from multiple sclerosis. J. Proteome Res., 2015, 14(5), 2065-2073.
[http://dx.doi.org/10.1021/pr501162w] [PMID: 25793971]
[100]
Nielsen, H.H.; Beck, H.C.; Kristensen, L.P.; Burton, M.; Csepany, T.; Simo, M.; Dioszeghy, P.; Sejbaek, T.; Grebing, M.; Heegaard, N.H.; Illes, Z. The urine proteome profile is different in neuromyelitis optica compared to multiple sclerosis: a clinical proteome study. PLoS One, 2015, 10(10), e0139659.
[http://dx.doi.org/10.1371/journal.pone.0139659] [PMID: 26460890]
[101]
Manconi, B.; Liori, B.; Cabras, T.; Vincenzoni, F.; Iavarone, F.; Lorefice, L.; Cocco, E.; Castagnola, M.; Messana, I.; Olianas, A. Top-down proteomic profiling of human saliva in multiple sclerosis patients. J. Proteomics, 2018, 187, 212-222.
[http://dx.doi.org/10.1016/j.jprot.2018.07.019] [PMID: 30086402]
[102]
Salvisberg, C.; Tajouri, N.; Hainard, A.; Burkhard, P.R.; Lalive, P.H.; Turck, N. Exploring the human tear fluid: discovery of new biomarkers in multiple sclerosis. Proteomics Clin. Appl., 2014, 8(3-4), 185-194.
[http://dx.doi.org/10.1002/prca.201300053] [PMID: 24488530]
[103]
Pottoo, F.H.; Javed, M.N.; Barkat, M.A.; Alam, M.S.; Nowshehri, J.A.; Alshayban, D.M.; Ansari, M.A. Estrogen and Serotonin: Complexity of Interactions and Implications for Epileptic Seizures and Epileptogenesis. Curr. Neuropharmacol., 2019, 17(3), 214-231.
[http://dx.doi.org/10.2174/1570159X16666180628164432] [PMID: 29956631]
[104]
Sarafroz, M.; Khatoon, Y.; Ahmad, N.; Amir, M.; Pottoo, F.H. Synthesis, Characterization and Anticonvulsant Activity of Novel Fused 1, 2, 4-Triazolo-1, 3, 4-Thiadiazoles. Orient. J. Chem., 2019, 35(1), 64-70.
[http://dx.doi.org/10.13005/ojc/350107]
[105]
Engel, J., Jr; Pitkänen, A.; Loeb, J.A.; Dudek, F.E.; Bertram, E.H., III; Cole, A.J.; Moshé, S.L.; Wiebe, S.; Jensen, F.E.; Mody, I.; Nehlig, A.; Vezzani, A. Epilepsy biomarkers. Epilepsia, 2013, 54(Suppl. 4), 61-69.
[http://dx.doi.org/10.1111/epi.12299] [PMID: 23909854]
[106]
Pottoo, F.H.; Bhowmik, M.; Vohora, D. Raloxifene protects against seizures and neurodegeneration in a mouse model mimicking epilepsy in postmenopausal woman. Eur. J. Pharm. Sci., 2014, 65, 167-173.
[http://dx.doi.org/10.1016/j.ejps.2014.09.002] [PMID: 25218046]
[107]
Wiebe, S.; Blume, W.T.; Girvin, J.P.; Eliasziw, M. Effectiveness and Efficiency of Surgery for Temporal Lobe Epilepsy Study Group. A randomized, controlled trial of surgery for temporal-lobe epilepsy. N. Engl. J. Med., 2001, 345(5), 311-318.
[http://dx.doi.org/10.1056/NEJM200108023450501] [PMID: 11484687]
[108]
Pottoo, F.H.; Tabassum, N.; Javed, M.N.; Nigar, S.; Rasheed, R.; Khan, A.; Barkat, M.A.; Alam, M.S.; Maqbool, A.; Ansari, M.A.; Barreto, G.E.; Ashraf, G.M. The synergistic effect of raloxifene, fluoxetine, and bromocriptine protects against pilocarpine-induced status epilepticus and temporal lobe epilepsy. Mol. Neurobiol., 2019, 56(2), 1233-1247.
[http://dx.doi.org/10.1007/s12035-018-1121-x] [PMID: 29881945]
[109]
Eun, J-P.; Choi, H-Y.; Kwak, Y-G. Proteomic analysis of human cerebral cortex in epileptic patients. Exp. Mol. Med., 2004, 36(2), 185-191.
[http://dx.doi.org/10.1038/emm.2004.26] [PMID: 15150448]
[110]
Yang, J.W.; Czech, T.; Felizardo, M.; Baumgartner, C.; Lubec, G. Aberrant expression of cytoskeleton proteins in hippocampus from patients with mesial temporal lobe epilepsy. Amino Acids, 2006, 30(4), 477-493.
[http://dx.doi.org/10.1007/s00726-005-0281-y] [PMID: 16583313]
[111]
Yang, J-W.; Czech, T.; Gelpi, E.; Lubec, G. Extravasation of plasma proteins can confound interpretation of proteomic studies of brain: a lesson from apo A-I in mesial temporal lobe epilepsy. Brain Res. Mol. Brain Res., 2005, 139(2), 348-356.
[http://dx.doi.org/10.1016/j.molbrainres.2005.06.010] [PMID: 16095751]
[112]
Czech, T.; Yang, J-W.; Csaszar, E.; Kappler, J.; Baumgartner, C.; Lubec, G. Reduction of hippocampal collapsin response mediated protein-2 in patients with mesial temporal lobe epilepsy. Neurochem. Res., 2004, 29(12), 2189-2196.
[http://dx.doi.org/10.1007/s11064-004-7025-3] [PMID: 15672539]
[113]
Ryu, M.J.; Kim, D.; Kang, U.B.; Kim, J.; Shin, H.S.; Lee, C.; Yu, M.H. Proteomic analysis of γ-butyrolactone-treated mouse thalamus reveals dysregulated proteins upon absence seizure. J. Neurochem., 2007, 102(3), 646-656.
[http://dx.doi.org/10.1111/j.1471-4159.2007.04504.x] [PMID: 17419809]
[114]
Ryu, M.J.; Lee, C.; Kim, J.; Shin, H.S.; Yu, M.H. Proteomic analysis of stargazer mutant mouse neuronal proteins involved in absence seizure. J. Neurochem., 2008, 104(5), 1260-1270.
[http://dx.doi.org/10.1111/j.1471-4159.2007.05100.x] [PMID: 17973978]
[115]
Green, D. R.; Reed, J. C. The Autoregulatory Feedback Loop of MicroRNA-21/Programmed Cell Death Protein 4/Activation Protein-1 (MiR-21/PDCD4/AP-1) as a Driving Force for Hepatic Fibrosis Development. J. Biol. Chem., 1998.
[116]
Waagepetersen, H.S.; Sonnewald, U.; Schousboe, A. The GABA paradox: multiple roles as metabolite, neurotransmitter, and neurodifferentiative agent. J. Neurochem., 1999, 73(4), 1335-1342.
[http://dx.doi.org/10.1046/j.1471-4159.1999.0731335.x] [PMID: 10501176]
[117]
Liu, X.Y.; Yang, J.L.; Chen, L.J.; Zhang, Y.; Yang, M.L.; Wu, Y.Y.; Li, F.Q.; Tang, M.H.; Liang, S.F.; Wei, Y.Q. Comparative proteomics and correlated signaling network of rat hippocampus in the pilocarpine model of temporal lobe epilepsy. Proteomics, 2008, 8(3), 582-603.
[http://dx.doi.org/10.1002/pmic.200700514] [PMID: 18186018]
[118]
Schatz, G. Mitochondria: beyond oxidative phosphorylation. Biochimica et Biophysica Acta (BBA)-. Molecular Basis of Disease, 1995, 1271(1), 123-126.
[http://dx.doi.org/10.1016/0925-4439(95)00018-Y]
[119]
Jiang, W.; Du, B.; Chi, Z.; Ma, L.; Wang, S.; Zhang, X.; Wu, W.; Wang, X.; Xu, G.; Guo, C. Preliminary explorations of the role of mitochondrial proteins in refractory epilepsy: some findings from comparative proteomics. J. Neurosci. Res., 2007, 85(14), 3160-3170.
[http://dx.doi.org/10.1002/jnr.21384] [PMID: 17893921]
[120]
Junker, H.; Späte, K.; Suofu, Y.; Walther, R.; Schwarz, G.; Kammer, W.; Nordheim, A.; Walker, L.C.; Runge, U.; Kessler, C.; Popa-Wagner, A. Proteomic identification of the involvement of the mitochondrial rieske protein in epilepsy. Epilepsia, 2005, 46(3), 339-343.
[http://dx.doi.org/10.1111/j.0013-9580.2005.46904.x] [PMID: 15730530]
[121]
Goffin, K.; Van Paesschen, W.; Dupont, P.; Van Laere, K. Longitudinal microPET imaging of brain glucose metabolism in rat lithium-pilocarpine model of epilepsy. Exp. Neurol., 2009, 217(1), 205-209.
[http://dx.doi.org/10.1016/j.expneurol.2009.02.008] [PMID: 19236862]
[122]
Jupp, B.; Williams, J.; Binns, D.; Hicks, R.J.; Cardamone, L.; Jones, N.; Rees, S.; O’Brien, T.J. Hypometabolism precedes limbic atrophy and spontaneous recurrent seizures in a rat model of TLE. Epilepsia, 2012, 53(7), 1233-1244.
[http://dx.doi.org/10.1111/j.1528-1167.2012.03525.x] [PMID: 22686573]
[123]
Guo, Y.; Gao, F.; Wang, S.; Ding, Y.; Zhang, H.; Wang, J.; Ding, M-P. In vivo mapping of temporospatial changes in glucose utilization in rat brain during epileptogenesis: an 18F-fluorodeoxyglucose-small animal positron emission tomography study. Neuroscience, 2009, 162(4), 972-979.
[http://dx.doi.org/10.1016/j.neuroscience.2009.05.041] [PMID: 19477240]
[124]
Shultz, S.R.; Cardamone, L.; Liu, Y.R.; Hogan, R.E.; Maccotta, L.; Wright, D.K.; Zheng, P.; Koe, A.; Gregoire, M.C.; Williams, J.P.; Hicks, R.J.; Jones, N.C.; Myers, D.E.; O’Brien, T.J.; Bouilleret, V. Can structural or functional changes following traumatic brain injury in the rat predict epileptic outcome? Epilepsia, 2013, 54(7), 1240-1250.
[http://dx.doi.org/10.1111/epi.12223] [PMID: 23718645]
[125]
Holtman, L.; van Vliet, E.A.; Aronica, E.; Wouters, D.; Wadman, W.J.; Gorter, J.A. Blood plasma inflammation markers during epileptogenesis in post-status epilepticus rat model for temporal lobe epilepsy. Epilepsia, 2013, 54(4), 589-595.
[http://dx.doi.org/10.1111/epi.12112] [PMID: 23398413]
[126]
McCutcheon, R.A.; Reis Marques, T.; Howes, O.D. Schizophrenia-An Overview. JAMA Psychiatry, 2020, 77(2), 201-210.
[http://dx.doi.org/10.1001/jamapsychiatry.2019.3360] [PMID: 31664453]
[127]
Crider, A. Schizophrenia: A biopsychological perspective; Routledge, 2020.
[128]
Razafsha, M.; Khaku, A.; Azari, H.; Alawieh, A.; Behforuzi, H.; Fadlallah, B.; Kobeissy, F.H.; Wang, K.K.; Gold, M.S. Biomarker identification in psychiatric disorders: from neuroscience to clinical practice. J. Psychiatr. Pract., 2015, 21(1), 37-48.
[http://dx.doi.org/10.1097/01.pra.0000460620.87557.02] [PMID: 25603450]
[129]
Johnston-Wilson, N.L.; Sims, C.D.; Hofmann, J.P.; Anderson, L.; Shore, A.D.; Torrey, E.F.; Yolken, R.H. The Stanley Neuropathology Consortium. Disease-specific alterations in frontal cortex brain proteins in schizophrenia, bipolar disorder, and major depressive disorder. Mol. Psychiatry, 2000, 5(2), 142-149.
[http://dx.doi.org/10.1038/sj.mp.4000696] [PMID: 10822341]
[130]
Prabakaran, S.; Swatton, J.E.; Ryan, M.M.; Huffaker, S.J.; Huang, J.T.; Griffin, J.L.; Wayland, M.; Freeman, T.; Dudbridge, F.; Lilley, K.S.; Karp, N.A.; Hester, S.; Tkachev, D.; Mimmack, M.L.; Yolken, R.H.; Webster, M.J.; Torrey, E.F.; Bahn, S. Mitochondrial dysfunction in schizophrenia: evidence for compromised brain metabolism and oxidative stress. Mol. Psychiatry, 2004, 9(7), 684-697, 643.
[http://dx.doi.org/10.1038/sj.mp.4001511] [PMID: 15098003]
[131]
Beasley, C.L.; Pennington, K.; Behan, A.; Wait, R.; Dunn, M.J.; Cotter, D. Proteomic analysis of the anterior cingulate cortex in the major psychiatric disorders: Evidence for disease-associated changes. Proteomics, 2006, 6(11), 3414-3425.
[http://dx.doi.org/10.1002/pmic.200500069] [PMID: 16637010]
[132]
Clark, D.; Dedova, I.; Cordwell, S.; Matsumoto, I. A proteome analysis of the anterior cingulate cortex gray matter in schizophrenia. Mol. Psychiatry, 2006, 11(5), 459-470, 423.
[http://dx.doi.org/10.1038/sj.mp.4001806] [PMID: 16491132]
[133]
Novikova, S.I.; He, F.; Cutrufello, N.J.; Lidow, M.S. Identification of protein biomarkers for schizophrenia and bipolar disorder in the postmortem prefrontal cortex using SELDI-TOF-MS ProteinChip profiling combined with MALDI-TOF-PSD-MS analysis. Neurobiol. Dis., 2006, 23(1), 61-76.
[http://dx.doi.org/10.1016/j.nbd.2006.02.002] [PMID: 16549361]
[134]
Pennington, K.; Beasley, C.L.; Dicker, P.; Fagan, A.; English, J.; Pariante, C.M.; Wait, R.; Dunn, M.J.; Cotter, D.R. Prominent synaptic and metabolic abnormalities revealed by proteomic analysis of the dorsolateral prefrontal cortex in schizophrenia and bipolar disorder. Mol. Psychiatry, 2008, 13(12), 1102-1117.
[http://dx.doi.org/10.1038/sj.mp.4002098] [PMID: 17938637]
[135]
Behan, A.T.; Byrne, C.; Dunn, M.J.; Cagney, G.; Cotter, D.R. Proteomic analysis of membrane microdomain-associated proteins in the dorsolateral prefrontal cortex in schizophrenia and bipolar disorder reveals alterations in LAMP, STXBP1 and BASP1 protein expression. Mol. Psychiatry, 2009, 14(6), 601-613.
[http://dx.doi.org/10.1038/mp.2008.7] [PMID: 18268500]
[136]
Pennington, K.; Dicker, P.; Dunn, M.J.; Cotter, D.R. Proteomic analysis reveals protein changes within layer 2 of the insular cortex in schizophrenia. Proteomics, 2008, 8(23-24), 5097-5107.
[http://dx.doi.org/10.1002/pmic.200800415] [PMID: 19003868]
[137]
Sibson, N.R.; Dhankhar, A.; Mason, G.F.; Rothman, D.L.; Behar, K.L.; Shulman, R.G. Stoichiometric coupling of brain glucose metabolism and glutamatergic neuronal activity. Proc. Natl. Acad. Sci. USA, 1998, 95(1), 316-321.
[http://dx.doi.org/10.1073/pnas.95.1.316] [PMID: 9419373]
[138]
Behar, K.L.; Rothman, D.L. In vivo nuclear magnetic resonance studies of glutamate-γ-aminobutyric acid-glutamine cycling in rodent and human cortex: the central role of glutamine. J. Nutr., 2001, 131(9)(Suppl.), 2498S-2504S.
[http://dx.doi.org/10.1093/jn/131.9.2498S] [PMID: 11533301]
[139]
Patel, A.B.; de Graaf, R.A.; Mason, G.F.; Rothman, D.L.; Shulman, R.G.; Behar, K.L. The contribution of GABA to glutamate/glutamine cycling and energy metabolism in the rat cortex in vivo. Proc. Natl. Acad. Sci. USA, 2005, 102(15), 5588-5593.
[http://dx.doi.org/10.1073/pnas.0501703102] [PMID: 15809416]
[140]
Coyle, J.T.; Tsai, G.; Goff, D. Converging evidence of NMDA receptor hypofunction in the pathophysiology of schizophrenia. Ann. N. Y. Acad. Sci., 2003, 1003(1), 318-327.
[http://dx.doi.org/10.1196/annals.1300.020] [PMID: 14684455]
[141]
Clancy, K.P.; Berger, R.; Cox, M.; Bleskan, J.; Walton, K.A.; Hart, I.; Patterson, D. Localization of the L-glutamine synthetase gene to chromosome 1q23. Genomics, 1996, 38(3), 418-420.
[http://dx.doi.org/10.1006/geno.1996.0645] [PMID: 8975719]
[142]
Martins-de-Souza, D.; Gattaz, W.F.; Schmitt, A.; Maccarrone, G.; Hunyadi-Gulyás, E.; Eberlin, M.N.; Souza, G.H.; Marangoni, S.; Novello, J.C.; Turck, C.W.; Dias-Neto, E. Proteomic analysis of dorsolateral prefrontal cortex indicates the involvement of cytoskeleton, oligodendrocyte, energy metabolism and new potential markers in schizophrenia. J. Psychiatr. Res., 2009, 43(11), 978-986.
[http://dx.doi.org/10.1016/j.jpsychires.2008.11.006] [PMID: 19110265]
[143]
Martins-de-Souza, D.; Gattaz, W.F.; Schmitt, A.; Rewerts, C.; Maccarrone, G.; Dias-Neto, E.; Turck, C.W. Prefrontal cortex shotgun proteome analysis reveals altered calcium homeostasis and immune system imbalance in schizophrenia. Eur. Arch. Psychiatry Clin. Neurosci., 2009, 259(3), 151-163.
[http://dx.doi.org/10.1007/s00406-008-0847-2] [PMID: 19165527]
[144]
Nesvaderani, M.; Matsumoto, I.; Sivagnanasundaram, S. Anterior hippocampus in schizophrenia pathogenesis: molecular evidence from a proteome study. Aust. N. Z. J. Psychiatry, 2009, 43(4), 310-322.
[http://dx.doi.org/10.1080/00048670902721103] [PMID: 19296286]
[145]
Petrak, J.; Ivanek, R.; Toman, O.; Cmejla, R.; Cmejlova, J.; Vyoral, D.; Zivny, J.; Vulpe, C.D. Déjà vu in proteomics. A hit parade of repeatedly identified differentially expressed proteins. Proteomics, 2008, 8(9), 1744-1749.
[http://dx.doi.org/10.1002/pmic.200700919] [PMID: 18442176]
[146]
Sultana, R.; Reed, T.; Perluigi, M.; Coccia, R.; Pierce, W.M.; Butterfield, D.A. Proteomic identification of nitrated brain proteins in amnestic mild cognitive impairment: a regional study. J. Cell. Mol. Med., 2007, 11(4), 839-851.
[http://dx.doi.org/10.1111/j.1582-4934.2007.00065.x] [PMID: 17760844]
[147]
Albertini, V.; Benussi, L.; Paterlini, A.; Glionna, M.; Prestia, A.; Bocchio-Chiavetto, L.; Amicucci, G.; Galluzzi, S.; Adorni, A.; Geroldi, C.; Binetti, G.; Frisoni, G.B.; Ghidoni, R. Distinct cerebrospinal fluid amyloid-beta peptide signatures in cognitive decline associated with Alzheimer’s disease and schizophrenia. Electrophoresis, 2012, 33(24), 3738-3744.
[http://dx.doi.org/10.1002/elps.201200307] [PMID: 23161113]
[148]
Wijte, D.; McDonnell, L.A.; Balog, C.I.; Bossers, K.; Deelder, A.M.; Swaab, D.F.; Verhaagen, J.; Mayboroda, O.A. A novel peptidomics approach to detect markers of Alzheimer’s disease in cerebrospinal fluid. Methods, 2012, 56(4), 500-507.
[http://dx.doi.org/10.1016/j.ymeth.2012.03.018] [PMID: 22465281]
[149]
Di Domenico, F.; Sultana, R.; Barone, E.; Perluigi, M.; Cini, C.; Mancuso, C.; Cai, J.; Pierce, W.M.; Butterfield, D.A. Quantitative proteomics analysis of phosphorylated proteins in the hippocampus of Alzheimer’s disease subjects. J. Proteomics, 2011, 74(7), 1091-1103.
[http://dx.doi.org/10.1016/j.jprot.2011.03.033] [PMID: 21515431]
[150]
Rudrabhatla, P.; Grant, P.; Jaffe, H.; Strong, M.J.; Pant, H.C. Quantitative phosphoproteomic analysis of neuronal intermediate filament proteins (NF-M/H) in Alzheimer’s disease by iTRAQ. FASEB J., 2010, 24(11), 4396-4407.
[http://dx.doi.org/10.1096/fj.10-157859] [PMID: 20624930]
[151]
Vincow, E.S.; Merrihew, G.; Thomas, R.E.; Shulman, N.J.; Beyer, R.P.; MacCoss, M.J.; Pallanck, L.J. The PINK1-Parkin pathway promotes both mitophagy and selective respiratory chain turnover in vivo. Proc. Natl. Acad. Sci. USA, 2013, 110(16), 6400-6405.
[http://dx.doi.org/10.1073/pnas.1221132110] [PMID: 23509287]
[152]
Leverenz, J.B.; Umar, I.; Wang, Q.; Montine, T.J.; McMillan, P.J.; Tsuang, D.W.; Jin, J.; Pan, C.; Shin, J.; Zhu, D.; Zhang, J. Proteomic identification of novel proteins in cortical lewy bodies. Brain Pathol., 2007, 17(2), 139-145.
[http://dx.doi.org/10.1111/j.1750-3639.2007.00048.x] [PMID: 17388944]
[153]
Cocciolo, A.; Di Domenico, F.; Coccia, R.; Fiorini, A.; Cai, J.; Pierce, W.M.; Mecocci, P.; Butterfield, D.A.; Perluigi, M. Decreased expression and increased oxidation of plasma haptoglobin in Alzheimer disease: Insights from redox proteomics. Free Radic. Biol. Med., 2012, 53(10), 1868-1876.
[http://dx.doi.org/10.1016/j.freeradbiomed.2012.08.596] [PMID: 23000119]
[154]
Zahid, S.; Oellerich, M.; Asif, A.R.; Ahmed, N. Phosphoproteome profiling of substantia nigra and cortex regions of Alzheimer’s disease patients. J. Neurochem., 2012, 121(6), 954-963.
[http://dx.doi.org/10.1111/j.1471-4159.2012.07737.x] [PMID: 22436009]
[155]
Ringman, J.M.; Schulman, H.; Becker, C.; Jones, T.; Bai, Y.; Immermann, F.; Cole, G.; Sokolow, S.; Gylys, K.; Geschwind, D.H.; Cummings, J.L.; Wan, H.I. Proteomic changes in cerebrospinal fluid of presymptomatic and affected persons carrying familial Alzheimer disease mutations. Arch. Neurol., 2012, 69(1), 96-104.
[http://dx.doi.org/10.1001/archneurol.2011.642] [PMID: 22232349]
[156]
de Carvalho, M.; Dengler, R.; Eisen, A.; England, J.D.; Kaji, R.; Kimura, J.; Mills, K.; Mitsumoto, H.; Nodera, H.; Shefner, J.; Swash, M. Electrodiagnostic criteria for diagnosis of ALS. Clin. Neurophysiol., 2008, 119(3), 497-503.
[http://dx.doi.org/10.1016/j.clinph.2007.09.143] [PMID: 18164242]
[157]
Kroksveen, A.C.; Aasebø, E.; Vethe, H.; Van Pesch, V.; Franciotta, D.; Teunissen, C.E.; Ulvik, R.J.; Vedeler, C.; Myhr, K-M.; Barsnes, H.; Berven, F.S. Discovery and initial verification of differentially abundant proteins between multiple sclerosis patients and controls using iTRAQ and SID-SRM. J. Proteomics, 2013, 78, 312-325.
[http://dx.doi.org/10.1016/j.jprot.2012.09.037] [PMID: 23059536]
[158]
Füvesi, J.; Hanrieder, J.; Bencsik, K.; Rajda, C.; Kovács, S.K.; Kaizer, L.; Beniczky, S.; Vécsei, L.; Bergquist, J. Proteomic analysis of cerebrospinal fluid in a fulminant case of multiple sclerosis. Int. J. Mol. Sci., 2012, 13(6), 7676-7693.
[http://dx.doi.org/10.3390/ijms13067676] [PMID: 22837721]
[159]
Berge, T.; Eriksson, A.; Brorson, I.S.; Høgestøl, E.A.; Berg-Hansen, P.; Døskeland, A.; Mjaavatten, O.; Bos, S.D.; Harbo, H.F.; Berven, F. Quantitative proteomic analyses of CD4+ and CD8+ T cells reveal differentially expressed proteins in multiple sclerosis patients and healthy controls. Clin. Proteomics, 2019, 16(1), 19.
[http://dx.doi.org/10.1186/s12014-019-9241-5] [PMID: 31080378]
[160]
Bedri, S.K.; Nilsson, O.B.; Fink, K.; Månberg, A.; Hamsten, C.; Ayoglu, B.; Manouchehrinia, A.; Nilsson, P.; Olsson, T.; Hillert, J.; Grönlund, H.; Glaser, A. Plasma protein profiling reveals candidate biomarkers for multiple sclerosis treatment. PLoS One, 2019, 14(5), e0217208.
[http://dx.doi.org/10.1371/journal.pone.0217208] [PMID: 31141529]
[161]
Qin, Z.; Qin, Y.; Liu, S. Alteration of DBP levels in CSF of patients with MS by proteomics analysis. Cell. Mol. Neurobiol., 2009, 29(2), 203-210.
[http://dx.doi.org/10.1007/s10571-008-9312-z] [PMID: 18807170]
[162]
Chen, S.; Lu, F.F.; Seeman, P.; Liu, F. Quantitative proteomic analysis of human substantia nigra in Alzheimer’s disease, Huntington’s disease and Multiple sclerosis. Neurochem. Res., 2012, 37(12), 2805-2813.
[http://dx.doi.org/10.1007/s11064-012-0874-2] [PMID: 22926577]
[163]
Liu, J.; Yin, L.; Dong, H.; Xu, E.; Zhang, L.; Qiao, Y.; Liu, Y.; Li, L.; Jia, J. Decreased serum levels of nucleolin protein fragment, as analyzed by bead-based proteomic technology, in multiple sclerosis patients compared to controls. J. Neuroimmunol., 2012, 250(1-2), 71-76.
[http://dx.doi.org/10.1016/j.jneuroim.2012.05.002] [PMID: 22633274]
[164]
Pieragostino, D.; Lanuti, P.; Cicalini, I.; Cufaro, M.C.; Ciccocioppo, F.; Ronci, M.; Simeone, P.; Onofrj, M.; van der Pol, E.; Fontana, A.; Marchisio, M.; Del Boccio, P. Proteomics characterization of extracellular vesicles sorted by flow cytometry reveals a disease-specific molecular cross-talk from cerebrospinal fluid and tears in multiple sclerosis. J. Proteomics, 2019, 204, 103403.
[http://dx.doi.org/10.1016/j.jprot.2019.103403] [PMID: 31170500]
[165]
Keren-Aviram, G.; Dachet, F.; Bagla, S.; Balan, K.; Loeb, J.A.; Dratz, E.A. Proteomic analysis of human epileptic neocortex predicts vascular and glial changes in epileptic regions. PLoS One, 2018, 13(4), e0195639.
[http://dx.doi.org/10.1371/journal.pone.0195639] [PMID: 29634780]
[166]
Mériaux, C.; Franck, J.; Park, D.B.; Quanico, J.; Kim, Y.H.; Chung, C.K.; Park, Y.M.; Steinbusch, H.; Salzet, M.; Fournier, I. Human temporal lobe epilepsy analyses by tissue proteomics. Hippocampus, 2014, 24(6), 628-642.
[http://dx.doi.org/10.1002/hipo.22246] [PMID: 24449190]
[167]
Li, G.; Ren, F.; Yao, J.; Wang, M.; Feng, X.; Liu, D. Human serum amyloid A (SAA) protein changes in acute epilepsy patients. Int. J. Neurosci., 2013, 123(4), 265-268.
[http://dx.doi.org/10.3109/00207454.2012.756876] [PMID: 23230824]
[168]
Reynolds, J.P.; Jimenez-Mateos, E.M.; Cao, L.; Bian, F.; Alves, M.; Miller-Delaney, S.F.; Zhou, A.; Henshall, D.C. Proteomic analysis after status epilepticus identifies UCHL1 as protective against hippocampal injury. Neurochem. Res., 2017, 42(7), 2033-2054.
[http://dx.doi.org/10.1007/s11064-017-2260-6] [PMID: 28397067]
[169]
Xiao, F.; Chen, D.; Lu, Y.; Xiao, Z.; Guan, L.F.; Yuan, J.; Wang, L.; Xi, Z.Q.; Wang, X.F. Proteomic analysis of cerebrospinal fluid from patients with idiopathic temporal lobe epilepsy. Brain Res., 2009, 1255, 180-189.
[http://dx.doi.org/10.1016/j.brainres.2008.12.008] [PMID: 19109932]
[170]
He, S.; Wang, Q.; He, J.; Pu, H.; Yang, W.; Ji, J. Proteomic analysis and comparison of the biopsy and autopsy specimen of human brain temporal lobe. Proteomics, 2006, 6(18), 4987-4996.
[http://dx.doi.org/10.1002/pmic.200600078] [PMID: 16912969]
[171]
Persike, D.S.; Marques-Carneiro, J.E.; Stein, M.L.L.; Yacubian, E.M.T.; Centeno, R.; Canzian, M.; Fernandes, M.J.D.S. Altered Proteins in the Hippocampus of Patients with Mesial Temporal Lobe Epilepsy. Pharmaceuticals, 2018, 11(4), 95.
[http://dx.doi.org/10.3390/ph11040095] [PMID: 30274397]
[172]
Yang, J.W.; Czech, T.; Yamada, J.; Csaszar, E.; Baumgartner, C.; Slavc, I.; Lubec, G. Aberrant cytosolic acyl-CoA thioester hydrolase in hippocampus of patients with mesial temporal lobe epilepsy. Amino Acids, 2004, 27(3-4), 269-275.
[http://dx.doi.org/10.1007/s00726-004-0138-9] [PMID: 15592755]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy