Advances in human brain proteomics analysis of neurodegenerative diseases
Abstract
Neurodegenerative diseases are characterized by progressive loss of neurons manifested as motor dysfunction and/or cognitive decline. Aberrant protein aggregation with altered physicochemical properties occurs in most neurodegenerative diseases. The pathophysiological mechanisms leading to the onset and progress of neurodegenerative diseases are still not fully understood. On the one hand, limited studies investigate neurodegenerative disease from human brain tissues. On the other, a comprehensive and efficient analysis method is needed to detect the signaling pathways evolved in neurodegenerative disease. Proteomics on human brains identifies key diagnostic biomarkers and treatment/therapeutic targets of neurodegenerative disorders. In recent years, several proteomics studies conducted on brain tissues from patients with neurodegenerative diseases have shown that changes in protein abundance or post-translational modification underly the disease pathogenesis. In this review, we summarize the major advances of human brain proteomics in the research on Alzheimer’s disease, Parkinson’s disease, multiple sclerosis, amyotrophic lateral sclerosis and Huntington’s disease as the most common neurodegenerative diseases. Finally, we proposed some perspective clues for future work.
References
- Abreha, M. H., Dammer, E. B., Ping, L., Zhang, T., Duong, D. M., Gearing, M., . . . Seyfried, N. T. (2018). Quantitative Analysis of the Brain Ubiquitylome in Alzheimer's Alzheimer’s Disease. Proteomics, 18(20), e1800108. doi:10.1002/pmic.201800108
- Akıl, E., Bulut, A., Kaplan, İ., Özdemir, H. H., Arslan, D., & Aluçlu, M. U. (2015). The increase of carcinoembryonic antigen (CEA), high-sensitivity C-reactive protein, and neutrophil/lymphocyte ratio in Parkinson's Parkinson’s disease. Neurol Sci, 36(3), 423-428. doi:10.1007/s10072-014-1976-1
- Alonso, R., Pisa, D., Marina, A. I., Morato, E., Rábano, A., Rodal, I., & Carrasco, L. (2015). Evidence for fungal infection in cerebrospinal fluid and brain tissue from patients with amyotrophic lateral sclerosis. International Journal of Biological Sciences, 11(5), 546-558. doi:10.7150/ijbs.11084
- Alzheimer's Association (2021). Alzheimer’s disease facts and figures. Alzheimers Dement, 17(3), 327-406. doi:10.1002/alz.12328
- Amunts, K., Ebell, C., Muller, J., Telefont, M., Knoll, A., & Lippert, T. (2016). The Human Brain Project: Creating a European Research Infrastructure to Decode the Human Brain. NEURON, 92(3), 574-581. doi:10.1016/j.neuron.2016.10.046
- Amunts, K., Knoll, A. C., Lippert, T., Pennartz, C. M. A., Ryvlin, P., Destexhe, A., . . . Bjaalie, J. G. (2019). The Human Brain Project-Synergy between neuroscience, computing, informatics, and brain-inspired technologies. PLOS BIOLOGY, 17(7), e3000344. doi:10.1371/journal.pbio.3000344
- An, C., Pu, X., Xiao, W., & Zhang, H. (2018). Expression of the DJ-1 protein in the serum of Chinese patients with Parkinson's Parkinson’s disease. Neurosci Lett, 665, 236-239. doi:10.1016/j.neulet.2017.12.023
- Arakhamia, T., Lee, C. E., Carlomagno, Y., Duong, D. M., Kundinger, S. R., Wang, K., . . . Fitzpatrick, A. W. P. (2020). Posttranslational Modifications Mediate the Structural Diversity of Tauopathy Strains. Cell, 180(4), 633-644.e612. doi:10.1016/j.cell.2020.01.027
- Attems, J., Walker, L., & Jellinger, K. A. (2014). Olfactory bulb involvement in neurodegenerative diseases. Acta Neuropathol, 127(4), 459-475. doi:10.1007/s00401-014-1261-7
- Atwood, C. S., Martins, R. N., Smith, M. A., & Perry, G. (2002). Senile plaque composition and posttranslational modification of amyloid-beta peptide and associated proteins. Peptides, 23(7), 1343-1350. doi:10.1016/s0196-9781(02)00070-0
- Bai, B., Vanderwall, D., Li, Y., Wang, X., Poudel, S., Wang, H., . . . Peng, J. (2021). Proteomic landscape of Alzheimer's Alzheimer’s Disease: novel insights into pathogenesis and biomarker discovery. Mol Neurodegener, 16(1), 55. doi:10.1186/s13024-021-00474-z
- Bai, B., Wang, X., Li, Y., Chen, P. C., Yu, K., Dey, K. K., . . . Peng, J. (2020). Deep Multilayer Brain Proteomics Identifies Molecular Networks in Alzheimer's Alzheimer’s Disease Progression. Neuron, 105(6), 975-991.e977. doi:10.1016/j.neuron.2019.12.015
- Ballatore, C., Lee, V. M., & Trojanowski, J. Q. (2007). Tau-mediated neurodegeneration in Alzheimer's Alzheimer’s disease and related disorders. Nat Rev Neurosci, 8(9), 663-672. doi:10.1038/nrn2194
- Bennett, E. J., Shaler, T. A., Woodman, B., Ryu, K. Y., Zaitseva, T. S., Becker, C. H., . . . Kopito, R. R. (2007). Global changes to the ubiquitin system in Huntington's Huntington’s disease. NATURE, 448(7154), 704-708. doi:10.1038/nature06022
- Broadwater, L., Pandit, A., Clements, R., Azzam, S., Vadnal, J., Sulak, M., . . . McDonough, J. (2011). Analysis of the mitochondrial proteome in multiple sclerosis cortex. Biochim Biophys Acta, 1812(5), 630-641. doi:10.1016/j.bbadis.2011.01.012
- Brown, N., Alkhayer, K., Clements, R., Singhal, N., Gregory, R., Azzam, S., . . . McDonough, J. (2016). Neuronal Hemoglobin Expression and Its Relevance to Multiple Sclerosis Neuropathology. J Mol Neurosci, 59(1), 1-17. doi:10.1007/s12031-015-0711-6
- Buratti, E. (2018). TDP-43 post-translational modifications in health and disease. EXPERT OPINION ON THERAPEUTIC TARGETS, 22(3), 279-293. doi:10.1080/14728222.2018.1439923
- Burrows, D. J., McGown, A., Jain, S. A., De Felice, M., Ramesh, T. M., Sharrack, B., & Majid, A. (2019). Animal models of multiple sclerosis: From rodents to zebrafish. Mult Scler, 25(3), 306-324. doi:10.1177/1352458518805246
- Catherman, A. D., Skinner, O. S., & Kelleher, N. L. (2014). Top Down proteomics: facts and perspectives. BIOCHEMICAL AND BIOPHYSICAL RESEARCH COMMUNICATIONS, 445(4), 683-693. doi:10.1016/j.bbrc.2014.02.041
- Chait, B. T. (2011). Mass spectrometry in the postgenomic era. Annual Review of Biochemistry, 80, 239-246. doi:10.1146/annurev-biochem-110810-095744
- Chen, S., Lu, F. F., Seeman, P., & Liu, F. (2012). Quantitative proteomic analysis of human substantia nigra in Alzheimer's Alzheimer’s disease, Huntington's Huntington’s disease and Multiple sclerosis. NEUROCHEMICAL RESEARCH, 37(12), 2805-2813. doi:10.1007/s11064-012-0874-2
- Chia, S. J., Tan, E. K., & Chao, Y. X. (2020). Historical Perspective: Models of Parkinson's Parkinson’s Disease. INTERNATIONAL JOURNAL OF MOLECULAR SCIENCES, 21(7). doi:10.3390/ijms21072464
- Chiang, M. C., Juo, C. G., Chang, H. H., Chen, H. M., Yi, E. C., & Chern, Y. (2007). Systematic uncovering of multiple pathways underlying the pathology of Huntington disease by an acid-cleavable isotope-coded affinity tag approach. MOLECULAR & CELLULAR PROTEOMICS, 6(5), 781-797. doi:10.1074/mcp.M600356-MCP200
- Chiu, C. C., Yeh, T. H., Lai, S. C., Weng, Y. H., Huang, Y. C., Cheng, Y. C., . . . Lu, C. S. (2016). Increased Rab35 expression is a potential biomarker and implicated in the pathogenesis of Parkinson's Parkinson’s disease. Oncotarget, 7(34), 54215-54227. doi:10.18632/oncotarget.11090
- Comes, A. L., Papiol, S., Mueller, T., Geyer, P. E., Mann, M., & Schulze, T. G. (2018). Proteomics for blood biomarker exploration of severe mental illness: pitfalls of the past and potential for the future. Transl Psychiatry, 8(1), 160. doi:10.1038/s41398-018-0219-2
- Consortium, H. i. (2012). Induced pluripotent stem cells from patients with Huntington's Huntington’s disease show CAG-repeat-expansion-associated phenotypes. Cell Stem Cell, 11(2), 264-278. doi:10.1016/j.stem.2012.04.027
- Cortes, C. J., & La Spada, A. R. (2014). The many faces of autophagy dysfunction in Huntington's Huntington’s disease: from mechanism to therapy. DRUG DISCOVERY TODAY, 19(7), 963-971. doi:10.1016/j.drudis.2014.02.014
- Culver, B. P., Savas, J. N., Park, S. K., Choi, J. H., Zheng, S., Zeitlin, S. O., . . . Tanese, N. (2012). Proteomic analysis of wild-type and mutant huntingtin-associated proteins in mouse brains identifies unique interactions and involvement in protein synthesis. JOURNAL OF BIOLOGICAL CHEMISTRY, 287(26), 21599-21614. doi:10.1074/jbc.M112.359307
- Dawson, T. M., Golde, T. E., & Lagier-Tourenne, C. (2018). Animal models of neurodegenerative diseases. NATURE NEUROSCIENCE, 21(10), 1370-1379. doi:10.1038/s41593-018-0236-8
- De Marchi, F., Sarnelli, M. F., Solara, V., Bersano, E., Cantello, R., & Mazzini, L. (2019). Depression and risk of cognitive dysfunctions in amyotrophic lateral sclerosis. ACTA NEUROLOGICA SCANDINAVICA, 139(5), 438-445. doi:10.1111/ane.13073
- DeJesus-Hernandez, M., Mackenzie, I. R., Boeve, B. F., Boxer, A. L., Baker, M., Rutherford, N. J., . . . Rademakers, R. (2011). Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS. NEURON, 72(2), 245-256. doi:10.1016/j.neuron.2011.09.011
- Deshaies, J. E., Shkreta, L., Moszczynski, A. J., Sidibe, H., Semmler, S., Fouillen, A., . . . Vande Velde, C. (2018). TDP-43 regulates the alternative splicing of hnRNP A1 to yield an aggregation-prone variant in amyotrophic lateral sclerosis. BRAIN, 141(5), 1320-1333. doi:10.1093/brain/awy062
- DeTure, M. A., & Dickson, D. W. (2019). The neuropathological diagnosis of Alzheimer's Alzheimer’s disease. Mol Neurodegener, 14(1), 32. doi:10.1186/s13024-019-0333-5
- DiProspero, N. A., Chen, E. Y., Charles, V., Plomann, M., Kordower, J. H., & Tagle, D. A. (2004). Early changes in Huntington's Huntington’s disease patient brains involve alterations in cytoskeletal and synaptic elements. J Neurocytol, 33(5), 517-533. doi:10.1007/s11068-004-0514-8
- Dixit, A., Mehta, R., & Singh, A. K. (2019). Proteomics in Human Parkinson's Parkinson’s Disease: Present Scenario and Future Directions. Cell Mol Neurobiol, 39(7), 901-915. doi:10.1007/s10571-019-00700-9
- Dobson, R., & Giovannoni, G. (2019). Multiple sclerosis - a review. EUROPEAN JOURNAL OF NEUROLOGY, 26(1), 27-40. doi:10.1111/ene.13819
- Donnelly, D. P., Rawlins, C. M., DeHart, C. J., Fornelli, L., Schachner, L. F., Lin, Z., . . . Agar, J. N. (2019). Best practices and benchmarks for intact protein analysis for top-down mass spectrometry. NATURE METHODS, 16(7), 587-594. doi:10.1038/s41592-019-0457-0
- Dorsey, E. R., & Bloem, B. R. (2018). The Parkinson Pandemic-A Call to Action. JAMA Neurol, 75(1), 9-10. doi:10.1001/jamaneurol.2017.3299
- Dorsey, E. R., Sherer, T., Okun, M. S., & Bloem, B. R. (2018). The Emerging Evidence of the Parkinson Pandemic. J Parkinsons Dis, 8(s1), S3-s8. doi:10.3233/jpd-181474
- Doty, R. L. (2012). Olfactory dysfunction in Parkinson disease. Nat Rev Neurol, 8(6), 329-339. doi:10.1038/nrneurol.2012.80
- Drummond, E., Nayak, S., Faustin, A., Pires, G., Hickman, R. A., Askenazi, M., . . . Wisniewski, T. (2017). Proteomic differences in amyloid plaques in rapidly progressive and sporadic Alzheimer's Alzheimer’s disease. Acta Neuropathol, 133(6), 933-954. doi:10.1007/s00401-017-1691-0
- Duan, W., Jiang, M., & Jin, J. (2014). Metabolism in HD: still a relevant mechanism? MOVEMENT DISORDERS, 29(11), 1366-1374. doi:10.1002/mds.25992
- Dujardin, S., Commins, C., Lathuiliere, A., Beerepoot, P., Fernandes, A. R., Kamath, T. V., . . . Hyman, B. T. (2020). Tau molecular diversity contributes to clinical heterogeneity in Alzheimer's Alzheimer’s disease. Nat Med, 26(8), 1256-1263. doi:10.1038/s41591-020-0938-9
- Dumitriu, A., Golji, J., Labadorf, A. T., Gao, B., Beach, T. G., Myers, R. H., . . . Latourelle, J. C. (2016). Integrative analyses of proteomics and RNA transcriptomics implicate mitochondrial processes, protein folding pathways and GWAS loci in Parkinson disease. BMC Med Genomics, 9, 5. doi:10.1186/s12920-016-0164-y
- Dutta, D., Ali, N., Banerjee, E., Singh, R., Naskar, A., Paidi, R. K., & Mohanakumar, K. P. (2018). Low Levels of Prohibitin in Substantia Nigra Makes Dopaminergic Neurons Vulnerable in Parkinson's Parkinson’s Disease. Mol Neurobiol, 55(1), 804-821. doi:10.1007/s12035-016-0328-y
- Ehrnhoefer, D. E., Sutton, L., & Hayden, M. R. (2011). Small changes, big impact: posttranslational modifications and function of huntingtin in Huntington disease. NEUROSCIENTIST, 17(5), 475-492. doi:10.1177/1073858410390378
- Engelen-Lee, J., Blokhuis, A. M., Spliet, W. G. M., Pasterkamp, R. J., Aronica, E., Demmers, J. A. A., . . . Van Den Berg, L. H. (2017). Proteomic profiling of the spinal cord in ALS: decreased ATP5D levels suggest synaptic dysfunction in ALS pathogenesis. Amyotroph Lateral Scler Frontotemporal Degener, 18(3-4), 210-220. doi:10.1080/21678421.2016.1245757
- Erkkinen, M. G., Kim, M. O., & Geschwind, M. D. (2018). Clinical Neurology and Epidemiology of the Major Neurodegenerative Diseases. Cold Spring Harb Perspect Biol, 10(4). doi:10.1101/cshperspect.a033118
- Faigle, W., Cruciani, C., Wolski, W., Roschitzki, B., Puthenparampil, M., Tomas-Ojer, P., . . . Martin, R. (2019). Brain Citrullination Patterns and T Cell Reactivity of Cerebrospinal Fluid-Derived CD4(+) T Cells in Multiple Sclerosis. Frontiers in Immunology, 10, 540. doi:10.3389/fimmu.2019.00540
- Fenn, J. B., Mann, M., Meng, C. K., Wong, S. F., & Whitehouse, C. M. (1989). Electrospray ionization for mass spectrometry of large biomolecules. SCIENCE, 246(4926), 64-71. doi:10.1126/science.2675315
- Franco Bocanegra, D. K., Nicoll, J. A. R., & Boche, D. (2018). Innate immunity in Alzheimer's Alzheimer’s disease: the relevance of animal models? J Neural Transm (Vienna), 125(5), 827-846. doi:10.1007/s00702-017-1729-4
- Gao, Y., Liu, J., Wang, J., Liu, Y., Zeng, L. H., Ge, W., & Ma, C. (2022). Proteomic analysis of human hippocampal subfields provides new insights into the pathogenesis of Alzheimer's Alzheimer’s disease and the role of glial cells. Brain Pathol, e13047. doi:10.1111/bpa.13047
- García-Moreno, J. M., Martín de Pablos, A., García-Sánchez, M. I., Méndez-Lucena, C., Damas-Hermoso, F., Rus, M., . . . Fernández, E. (2013). May serum levels of advanced oxidized protein products serve as a prognostic marker of disease duration in patients with idiopathic Parkinson's Parkinson’s disease? Antioxid Redox Signal, 18(11), 1296-1302. doi:10.1089/ars.2012.5026
- Gauthier, S., Rosa-Neto, P., Morais, J. A., & Webster, C. (2021). World Alzheimer Report 2021: Journey through the diagnosis of dementia. Alzheimer's Alzheimer’s Disease International, 17-29.
- Global, regional, and national burden of neurological disorders, 1990-2016: a systematic analysis for the Global Burden of Disease Study 2016. (2019). LANCET NEUROLOGY, 18(5), 459-480. doi:10.1016/s1474-4422(18)30499-x
- Griffiths, J. (2008). A brief history of mass spectrometry. ANALYTICAL CHEMISTRY, 80(15), 5678-5683. doi:10.1021/ac8013065
- Hampel, H., Mesulam, M. M., Cuello, A. C., Farlow, M. R., Giacobini, E., Grossberg, G. T., . . . Khachaturian, Z. S. (2018). The cholinergic system in the pathophysiology and treatment of Alzheimer's Alzheimer’s disease. Brain, 141(7), 1917-1933. doi:10.1093/brain/awy132
- Han, M. H., Hwang, S. I., Roy, D. B., Lundgren, D. H., Price, J. V., Ousman, S. S., . . . Steinman, L. (2008). Proteomic analysis of active multiple sclerosis lesions reveals therapeutic targets. NATURE, 451(7182), 1076-1081. doi:10.1038/nature06559
- Hardy, J. A., & Higgins, G. A. (1992). Alzheimer's Alzheimer’s disease: the amyloid cascade hypothesis. Science, 256(5054), 184-185. doi:10.1126/science.1566067
- He, X., Memczak, S., Qu, J., Belmonte, J. C. I., & Liu, G. H. (2020). Single-cell omics in ageing: a young and growing field. Nat Metab, 2(4), 293-302. doi:10.1038/s42255-020-0196-7
- Hedl, T. J., San Gil, R., Cheng, F., Rayner, S. L., Davidson, J. M., De Luca, A., . . . Lee, A. (2019). Proteomics Approaches for Biomarker and Drug Target Discovery in ALS and FTD. Frontiers in Neuroscience, 13, 548. doi:10.3389/fnins.2019.00548
- Heemels, M. T. (2016). Neurodegenerative diseases. NATURE, 539(7628), 179. doi:10.1038/539179a
- Hou, Y., Dan, X., Babbar, M., Wei, Y., Hasselbalch, S. G., Croteau, D. L., & Bohr, V. A. (2019). Ageing as a risk factor for neurodegenerative disease. Nat Rev Neurol, 15(10), 565-581. doi:10.1038/s41582-019-0244-7
- Huff, T., Müller, C. S., Otto, A. M., Netzker, R., & Hannappel, E. (2001). beta-Thymosins, small acidic peptides with multiple functions. INTERNATIONAL JOURNAL OF BIOCHEMISTRY & CELL BIOLOGY, 33(3), 205-220. doi:10.1016/s1357-2725(00)00087-x
- Hyman, B. T., Phelps, C. H., Beach, T. G., Bigio, E. H., Cairns, N. J., Carrillo, M. C., . . . Montine, T. J. (2012). National Institute on Aging-Alzheimer's Alzheimer’s Association guidelines for the neuropathologic assessment of Alzheimer's Alzheimer’s disease. Alzheimers Dement, 8(1), 1-13. doi:10.1016/j.jalz.2011.10.007
- Ifergan, I., Kebir, H., Terouz, S., Alvarez, J. I., Lécuyer, M. A., Gendron, S., . . . Prat, A. (2011). Role of Ninjurin-1 in the migration of myeloid cells to central nervous system inflammatory lesions. ANNALS OF NEUROLOGY, 70(5), 751-763. doi:10.1002/ana.22519
- Illarioshkin, S. N., Klyushnikov, S. A., Vigont, V. A., Seliverstov, Y. A., & Kaznacheyeva, E. V. (2018). Molecular Pathogenesis in Huntington's Huntington’s Disease. Biochemistry (Mosc), 83(9), 1030-1039. doi:10.1134/s0006297918090043
- International, A. s. D. (2019). World Alzheimer Report 2019: attitudes to dementia. Alzheimer’s Disease International, 13-16.
- Iridoy, M. O., Zubiri, I., Zelaya, M. V., Martinez, L., Ausín, K., Lachen-Montes, M., . . . Jericó, I. (2018). Neuroanatomical Quantitative Proteomics Reveals Common Pathogenic Biological Routes between Amyotrophic Lateral Sclerosis (ALS) and Frontotemporal Dementia (FTD). INTERNATIONAL JOURNAL OF MOLECULAR SCIENCES, 20(1). doi:10.3390/ijms20010004
- Johnson, E. B., Ziegler, G., Penny, W., Rees, G., Tabrizi, S. J., Scahill, R. I., & Gregory, S. (2021). Dynamics of Cortical Degeneration Over a Decade in Huntington's Huntington’s Disease. BIOLOGICAL PSYCHIATRY, 89(8), 807-816. doi:10.1016/j.biopsych.2020.11.009
- Johnson, E. C. B., Carter, E. K., Dammer, E. B., Duong, D. M., Gerasimov, E. S., Liu, Y., . . . Seyfried, N. T. (2022). Large-scale deep multi-layer analysis of Alzheimer's Alzheimer’s disease brain reveals strong proteomic disease-related changes not observed at the RNA level. Nat Neurosci, 25(2), 213-225. doi:10.1038/s41593-021-00999-y
- Johnson, E. C. B., Dammer, E. B., Duong, D. M., Ping, L., Zhou, M., Yin, L., . . . Seyfried, N. T. (2020). Large-scale proteomic analysis of Alzheimer's Alzheimer’s disease brain and cerebrospinal fluid reveals early changes in energy metabolism associated with microglia and astrocyte activation. Nat Med, 26(5), 769-780. doi:10.1038/s41591-020-0815-6
- Kametani, F., Obi, T., Shishido, T., Akatsu, H., Murayama, S., Saito, Y., . . . Hasegawa, M. (2016). Mass spectrometric analysis of accumulated TDP-43 in amyotrophic lateral sclerosis brains. ScientIF-ic Reports, 6, 23281. doi:10.1038/srep23281
- Kerr, J. S., Adriaanse, B. A., Greig, N. H., Mattson, M. P., Cader, M. Z., Bohr, V. A., & Fang, E. F. (2017). Mitophagy and Alzheimer's Alzheimer’s Disease: Cellular and Molecular Mechanisms. Trends Neurosci, 40(3), 151-166. doi:10.1016/j.tins.2017.01.002
- Kim, G., Gautier, O., Tassoni-Tsuchida, E., Ma, X. R., & Gitler, A. D. (2020). ALS Genetics: Gains, Losses, and Implications for Future Therapies. NEURON, 108(5), 822-842. doi:10.1016/j.neuron.2020.08.022
- Kim, R., Kim, H. J., Kim, A., Jang, M., Kim, A., Kim, Y., . . . Jeon, B. (2018). Peripheral blood inflammatory markers in early Parkinson's Parkinson’s disease. J Clin Neurosci, 58, 30-33. doi:10.1016/j.jocn.2018.10.079
- Kinney, J. W., Bemiller, S. M., Murtishaw, A. S., Leisgang, A. M., Salazar, A. M., & Lamb, B. T. (2018). Inflammation as a central mechanism in Alzheimer's Alzheimer’s disease. Alzheimers Dement (N Y), 4, 575-590. doi:10.1016/j.trci.2018.06.014
- Kitamura, Y., Kojima, M., Kurosawa, T., Sasaki, R., Ichihara, S., Hiraku, Y., . . . Oikawa, S. (2018). Proteomic Profiling of Exosomal Proteins for Blood-based Biomarkers in Parkinson's Parkinson’s Disease. Neuroscience, 392, 121-128. doi:10.1016/j.neuroscience.2018.09.017
- Kotelnikova, E., Kiani, N. A., Messinis, D., Pertsovskaya, I., Pliaka, V., Bernardo-Faura, M., . . . Villoslada, P. (2019). MAPK pathway and B cells overactivation in multiple sclerosis revealed by phosphoproteomics and genomic analysis. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 116(19), 9671-9676. doi:10.1073/pnas.1818347116
- Lachén-Montes, M., González-Morales, A., Iloro, I., Elortza, F., Ferrer, I., Gveric, D., . . . Santamaría, E. (2019). Unveiling the olfactory proteostatic disarrangement in Parkinson's Parkinson’s disease by proteome-wide profiling. NEUROBIOLOGY OF AGING, 73, 123-134. doi:10.1016/j.neurobiolaging.2018.09.018
- Laferrière, F., Maniecka, Z., Pérez-Berlanga, M., Hruska-Plochan, M., Gilhespy, L., Hock, E. M., . . . Polymenidou, M. (2019). TDP-43 extracted from frontotemporal lobar degeneration subject brains displays distinct aggregate assemblies and neurotoxic effects reflecting disease progression rates. NATURE NEUROSCIENCE, 22(1), 65-77. doi:10.1038/s41593-018-0294-y
- Langfelder, P., & Horvath, S. (2008). WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics, 9, 559. doi:10.1186/1471-2105-9-559
- Lassmann, H., & Bradl, M. (2017). Multiple sclerosis: experimental models and reality. ACTA NEUROPATHOLOGICA, 133(2), 223-244. doi:10.1007/s00401-016-1631-4
- Liao, L., Cheng, D., Wang, J., Duong, D. M., Losik, T. G., Gearing, M., . . . Peng, J. (2004). Proteomic characterization of postmortem amyloid plaques isolated by laser capture microdissection. J Biol Chem, 279(35), 37061-37068. doi:10.1074/jbc.M403672200
- Licker, V., & Burkhard, P. R. (2014). Proteomics as a new paradigm to tackle Parkinson’s disease research challenges. Translational Proteomics, 4-5, 1-17. doi:10.1016/j.trprot.2014.08.001
- Licker, V., Côte, M., Lobrinus, J. A., Rodrigo, N., Kövari, E., Hochstrasser, D. F., . . . Burkhard, P. R. (2012). Proteomic profiling of the substantia nigra demonstrates CNDP2 overexpression in Parkinson's Parkinson’s disease. J Proteomics, 75(15), 4656-4667. doi:10.1016/j.jprot.2012.02.032
- Licker, V., Kövari, E., Hochstrasser, D. F., & Burkhard, P. R. (2009). Proteomics in human Parkinson's Parkinson’s disease research. Journal of Proteomics, 73(1), 10-29. doi:10.1016/j.jprot.2009.07.007
- Licker, V., Turck, N., Kövari, E., Burkhardt, K., Côte, M., Surini-Demiri, M., . . . Burkhard, P. R. (2014). Proteomic analysis of human substantia nigra identifies novel candidates involved in Parkinson's Parkinson’s disease pathogenesis. Proteomics, 14(6), 784-794. doi:10.1002/pmic.201300342
- Lin, M. T., & Beal, M. F. (2006). Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. NATURE, 443(7113), 787-795. doi:10.1038/nature05292
- Liu, D., Liu, C., Li, J., Azadzoi, K., Yang, Y., Fei, Z., . . . Yang, J. H. (2013). Proteomic analysis reveals differentially regulated protein acetylation in human amyotrophic lateral sclerosis spinal cord. PLoS One, 8(12), e80779. doi:10.1371/journal.pone.0080779
- Lontay, B., Kiss, A., Virág, L., & Tar, K. (2020). How Do Post-Translational Modifications Influence the Pathomechanistic Landscape of Huntington's Huntington’s Disease? A Comprehensive Review. INTERNATIONAL JOURNAL OF MOLECULAR SCIENCES, 21(12). doi:10.3390/ijms21124282
- Ludwig, C., Gillet, L., Rosenberger, G., Amon, S., Collins, B. C., & Aebersold, R. (2018). Data-independent acquisition-based SWATH-MS for quantitative proteomics: a tutorial. Molecular Systems Biology, 14(8), e8126. doi:10.15252/msb.20178126
- Ly, L., Barnett, M. H., Zheng, Y. Z., Gulati, T., Prineas, J. W., & Crossett, B. (2011). Comprehensive tissue processing strategy for quantitative proteomics of formalin-fixed multiple sclerosis lesions. JOURNAL OF PROTEOME RESEARCH, 10(10), 4855-4868. doi:10.1021/pr200672n
- Maccarrone, G., Nischwitz, S., Deininger, S. O., Hornung, J., König, F. B., Stadelmann, C., . . . Weber, F. (2017). MALDI imaging mass spectrometry analysis-A new approach for protein mapping in multiple sclerosis brain lesions. J Chromatogr B Analyt Technol Biomed Life Sci, 1047, 131-140. doi:10.1016/j.jchromb.2016.07.001
- Martin, L., Latypova, X., & Terro, F. (2011). Post-translational modifications of tau protein: implications for Alzheimer's Alzheimer’s disease. Neurochem Int, 58(4), 458-471. doi:10.1016/j.neuint.2010.12.023
- Martin, W. R., Wieler, M., & Hanstock, C. C. (2007). Is brain lactate increased in Huntington's Huntington’s disease? JOURNAL OF THE NEUROLOGICAL SCIENCES, 263(1-2), 70-74. doi:10.1016/j.jns.2007.05.035
- Masrori, P., & Van Damme, P. (2020). Amyotrophic lateral sclerosis: a clinical review. EUROPEAN JOURNAL OF NEUROLOGY, 27(10), 1918-1929. doi:10.1111/ene.14393
- Mayo, S., Benito-León, J., Peña-Bautista, C., Baquero, M., & Cháfer-Pericás, C. (2021). Recent Evidence in Epigenomics and Proteomics Biomarkers for Early and Minimally Invasive Diagnosis of Alzheimer's Alzheimer’s and Parkinson's Parkinson’s Diseases. Curr Neuropharmacol, 19(8), 1273-1303. doi:10.2174/1570159x19666201223154009
- McArdle, A. J., & Menikou, S. (2021). What is proteomics? Arch Dis Child Educ Pract Ed, 106(3), 178-181. doi:10.1136/archdischild-2019-317434
- Mejzini, R., Flynn, L. L., Pitout, I. L., Fletcher, S., Wilton, S. D., & Akkari, P. A. (2019). ALS Genetics, Mechanisms, and Therapeutics: Where Are We Now? Frontiers in Neuroscience, 13, 1310. doi:10.3389/fnins.2019.01310
- Milakovic, T., & Johnson, G. V. (2005). Mitochondrial respiration and ATP production are significantly impaired in striatal cells expressing mutant huntingtin. JOURNAL OF BIOLOGICAL CHEMISTRY, 280(35), 30773-30782. doi:10.1074/jbc.M504749200
- Mullin, S., & Schapira, A. (2013). α-Synuclein and mitochondrial dysfunction in Parkinson's Parkinson’s disease. MOLECULAR NEUROBIOLOGY, 47(2), 587-597. doi:10.1007/s12035-013-8394-x
- Murtaza, N., Uy, J., & Singh, K. K. (2020). Emerging proteomic approaches to identify the underlying pathophysiology of neurodevelopmental and neurodegenerative disorders. Molecular Autism, 11(1), 27. doi:10.1186/s13229-020-00334-5
- Neelagandan, N., Gonnella, G., Dang, S., Janiesch, P. C., Miller, K. K., Küchler, K., . . . Duncan, K. E. (2019). TDP-43 enhances translation of specific mRNAs linked to neurodegenerative disease. NUCLEIC ACIDS RESEARCH, 47(1), 341-361. doi:10.1093/nar/gky972
- Nicaise, A. M., Wagstaff, L. J., Willis, C. M., Paisie, C., Chandok, H., Robson, P., . . . Crocker, S. J. (2019). Cellular senescence in progenitor cells contributes to diminished remyelination potential in progressive multiple sclerosis. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 116(18), 9030-9039. doi:10.1073/pnas.1818348116
- Nicoll, J. A. R., Bloom, T., Clarke, A., Boche, D., & Hilton, D. (2022). BRAIN UK: Accessing NHS tissue archives for neuroscience research. NEUROPATHOLOGY AND APPLIED NEUROBIOLOGY, 48(2), e12766. doi:10.1111/nan.12766
- Olek, M. J. (2021). Multiple Sclerosis. ANNALS OF INTERNAL MEDICINE, 174(6), Itc81-itc96. doi:10.7326/aitc202106150
- Ortiz, G. G., Pacheco-Moisés, F. P., Macías-Islas, M., Flores-Alvarado, L. J., Mireles-Ramírez, M. A., González-Renovato, E. D., . . . Alatorre-Jiménez, M. A. (2014). Role of the blood-brain barrier in multiple sclerosis. ARCHIVES OF MEDICAL RESEARCH, 45(8), 687-697. doi:10.1016/j.arcmed.2014.11.013
- Perkel, J. M. (2021). Single-cell proteomics takes centre stage. NATURE, 597(7877), 580-582. doi:10.1038/d41586-021-02530-6
- Prasad, A., Bharathi, V., Sivalingam, V., Girdhar, A., & Patel, B. K. (2019). Molecular Mechanisms of TDP-43 Misfolding and Pathology in Amyotrophic Lateral Sclerosis. Frontiers in Molecular Neuroscience, 12, 25. doi:10.3389/fnmol.2019.00025
- Qendro, V., Bugos, G. A., Lundgren, D. H., Glynn, J., Han, M. H., & Han, D. K. (2017). Integrative proteomics, genomics, and translational immunology approaches reveal mutated forms of Proteolipid Protein 1 (PLP1) and mutant-specific immune response in multiple sclerosis. PROTEOMICS, 17(6). doi:10.1002/pmic.201600322
- Ratovitski, T., Chaerkady, R., Kammers, K., Stewart, J. C., Zavala, A., Pletnikova, O., . . . Ross, C. A. (2016). Quantitative Proteomic Analysis Reveals Similarities between Huntington's Huntington’s Disease (HD) and Huntington's Huntington’s Disease-Like 2 (HDL2) Human Brains. JOURNAL OF PROTEOME RESEARCH, 15(9), 3266-3283. doi:10.1021/acs.jproteome.6b00448
- Ratovitski, T., Chighladze, E., Arbez, N., Boronina, T., Herbrich, S., Cole, R. N., & Ross, C. A. (2012). Huntingtin protein interactions altered by polyglutamine expansion as determined by quantitative proteomic analysis. CELL CYCLE, 11(10), 2006-2021. doi:10.4161/cc.20423
- Renton, A. E., Majounie, E., Waite, A., Simón-Sánchez, J., Rollinson, S., Gibbs, J. R., . . . Traynor, B. J. (2011). A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD. NEURON, 72(2), 257-268. doi:10.1016/j.neuron.2011.09.010
- Riley, B. E., Gardai, S. J., Emig-Agius, D., Bessarabova, M., Ivliev, A. E., Schüle, B., . . . Johnston, J. A. (2014). Systems-based analyses of brain regions functionally impacted in Parkinson's Parkinson’s disease reveals underlying causal mechanisms. PLoS One, 9(8), e102909. doi:10.1371/journal.pone.0102909
- Rosen, D. R., Siddique, T., Patterson, D., Figlewicz, D. A., Sapp, P., Hentati, A., . . . et al. (1993). Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. NATURE, 362(6415), 59-62. doi:10.1038/362059a0
- Ross, C. A., Aylward, E. H., Wild, E. J., Langbehn, D. R., Long, J. D., Warner, J. H., . . . Tabrizi, S. J. (2014). Huntington disease: natural history, biomarkers and prospects for therapeutics. Nat Rev Neurol, 10(4), 204-216. doi:10.1038/nrneurol.2014.24
- Ross, C. A., Pantelyat, A., Kogan, J., & Brandt, J. (2014). Determinants of functional disability in Huntington's Huntington’s disease: role of cognitive and motor dysfunction. MOVEMENT DISORDERS, 29(11), 1351-1358. doi:10.1002/mds.26012
- Ross, C. A., & Tabrizi, S. J. (2011). Huntington's Huntington’s disease: from molecular pathogenesis to clinical treatment. LANCET NEUROLOGY, 10(1), 83-98. doi:10.1016/s1474-4422(10)70245-3
- Rüb, U., Seidel, K., Heinsen, H., Vonsattel, J. P., den Dunnen, W. F., & Korf, H. W. (2016). Huntington's Huntington’s disease (HD): the neuropathology of a multisystem neurodegenerative disorder of the human brain. BRAIN PATHOLOGY, 26(6), 726-740. doi:10.1111/bpa.12426
- Sandi, D., Kokas, Z., Biernacki, T., Bencsik, K., Klivényi, P., & Vécsei, L. (2022). Proteomics in Multiple Sclerosis: The Perspective of the Clinician. INTERNATIONAL JOURNAL OF MOLECULAR SCIENCES, 23(9). doi:10.3390/ijms23095162
- Santra, M., Chopp, M., Zhang, Z. G., Lu, M., Santra, S., Nalani, A., . . . Morris, D. C. (2012). Thymosin β 4 mediates oligodendrocyte differentiation by upregulating p38 MAPK. GLIA, 60(12), 1826-1838. doi:10.1002/glia.22400
- Saudou, F., & Humbert, S. (2016). The Biology of Huntingtin. NEURON, 89(5), 910-926. doi:10.1016/j.neuron.2016.02.003
- Schönberger, S. J., Jezdic, D., Faull, R. L., & Cooper, G. J. (2013). Proteomic analysis of the human brain in Huntington's Huntington’s Disease indicates pathogenesis by molecular processes linked to other neurodegenerative diseases and to type-2 diabetes. J Huntingtons Dis, 2(1), 89-99. doi:10.3233/jhd-120044
- Selkoe, D. J. (1989). Molecular pathology of amyloidogenic proteins and the role of vascular amyloidosis in Alzheimer's Alzheimer’s disease. Neurobiol Aging, 10(5), 387-395. doi:10.1016/0197-4580(89)90072-9
- Selkoe, D. J., & Hardy, J. (2016). The amyloid hypothesis of Alzheimer's Alzheimer’s disease at 25 years. EMBO Mol Med, 8(6), 595-608. doi:10.15252/emmm.201606210
- Sen, M. K., Almuslehi, M. S. M., Shortland, P. J., Mahns, D. A., & Coorssen, J. R. (2021). Proteomics of Multiple Sclerosis: Inherent Issues in Defining the Pathoetiology and Identifying (Early) Biomarkers. INTERNATIONAL JOURNAL OF MOLECULAR SCIENCES, 22(14). doi:10.3390/ijms22147377
- Shirasaki, D. I., Greiner, E. R., Al-Ramahi, I., Gray, M., Boontheung, P., Geschwind, D. H., . . . Yang, X. W. (2012). Network organization of the huntingtin proteomic interactome in mammalian brain. NEURON, 75(1), 41-57. doi:10.1016/j.neuron.2012.05.024
- Si, Q. Q., Yuan, Y. S., Zhi, Y., Tong, Q., Zhang, L., & Zhang, K. (2018). Plasma transferrin level correlates with the tremor-dominant phenotype of Parkinson's Parkinson’s disease. Neurosci Lett, 684, 42-46. doi:10.1016/j.neulet.2018.07.004
- Song, I. U., Chung, S. W., Kim, J. S., & Lee, K. S. (2011). Association between high-sensitivity C-reactive protein and risk of early idiopathic Parkinson's Parkinson’s disease. Neurol Sci, 32(1), 31-34. doi:10.1007/s10072-010-0335-0
- Sorolla, M. A., Reverter-Branchat, G., Tamarit, J., Ferrer, I., Ros, J., & Cabiscol, E. (2008). Proteomic and oxidative stress analysis in human brain samples of Huntington disease. FREE RADICAL BIOLOGY AND MEDICINE, 45(5), 667-678. doi:10.1016/j.freeradbiomed.2008.05.014
- Su, W., Chen, H. B., Li, S. H., & Wu, D. Y. (2012). Correlational study of the serum levels of the glial fibrillary acidic protein and neurofilament proteins in Parkinson's Parkinson’s disease patients. Clin Neurol Neurosurg, 114(4), 372-375. doi:10.1016/j.clineuro.2011.11.002
- Swarup, V., & Julien, J. P. (2011). ALS pathogenesis: recent insights from genetics and mouse models. Prog Neuropsychopharmacol Biol Psychiatry, 35(2), 363-369. doi:10.1016/j.pnpbp.2010.08.006
- Syed, Y. A., Zhao, C., Mahad, D., Möbius, W., Altmann, F., Foss, F., . . . Kotter, M. R. N. (2016). Antibody-mediated neutralization of myelin-associated EphrinB3 accelerates CNS remyelination. ACTA NEUROPATHOLOGICA, 131(2), 281-298. doi:10.1007/s00401-015-1521-1
- Tabrizi, S. J., Flower, M. D., Ross, C. A., & Wild, E. J. (2020). Huntington disease: new insights into molecular pathogenesis and therapeutic opportunities. Nat Rev Neurol, 16(10), 529-546. doi:10.1038/s41582-020-0389-4
- Tanaka, K., Waki, H., Ido, Y., Akita, S., Yoshida, Y., Yoshida, T., & Matsuo, T. J. R. C. i. M. S. (1988). Protein and polymer analyses up to m/z 100 000 by laser ionization time‐of‐flight mass spectrometry. RAPID COMMUNICATIONS IN MASS SPECTROMETRY, 2(8), 151-153.
- Taylor, J. P., Brown, R. H., Jr., & Cleveland, D. W. (2016). Decoding ALS: from genes to mechanism. NATURE, 539(7628), 197-206. doi:10.1038/nature20413
- Thompson, A. J., Baranzini, S. E., Geurts, J., Hemmer, B., & Ciccarelli, O. (2018). Multiple sclerosis. LANCET, 391(10130), 1622-1636. doi:10.1016/s0140-6736(18)30481-1
- Tiwari, S., Atluri, V., Kaushik, A., Yndart, A., & Nair, M. (2019). Alzheimer's Alzheimer’s disease: pathogenesis, diagnostics, and therapeutics. Int J Nanomedicine, 14, 5541-5554. doi:10.2147/ijn.S200490
- Tolosa, E., Garrido, A., Scholz, S. W., & Poewe, W. (2021). Challenges in the diagnosis of Parkinson's Parkinson’s disease. Lancet Neurol, 20(5), 385-397. doi:10.1016/s1474-4422(21)00030-2
- Trist, B. G., Genoud, S., Roudeau, S., Rookyard, A., Abdeen, A., Cottam, V., . . . Double, K. L. (2022). Altered SOD1 maturation and post-translational modification in amyotrophic lateral sclerosis spinal cord. BRAIN. doi:10.1093/brain/awac165
- Umemura, A., Oeda, T., Yamamoto, K., Tomita, S., Kohsaka, M., Park, K., . . . Sawada, H. (2015). Baseline Plasma C-Reactive Protein Concentrations and Motor Prognosis in Parkinson Disease. PLoS One, 10(8), e0136722. doi:10.1371/journal.pone.0136722
- Umoh, M. E., Dammer, E. B., Dai, J., Duong, D. M., Lah, J. J., Levey, A. I., . . . Seyfried, N. T. (2018). A proteomic network approach across the ALS-FTD disease spectrum resolves clinical phenotypes and genetic vulnerability in human brain. EMBO Molecular Medicine, 10(1), 48-62. doi:10.15252/emmm.201708202
- van Es, M. A., Hardiman, O., Chio, A., Al-Chalabi, A., Pasterkamp, R. J., Veldink, J. H., & van den Berg, L. H. (2017). Amyotrophic lateral sclerosis. LANCET, 390(10107), 2084-2098. doi:10.1016/s0140-6736(17)31287-4
- Vassileff, N., Vella, L. J., Rajapaksha, H., Shambrook, M., Kenari, A. N., McLean, C., . . . Cheng, L. (2020). Revealing the Proteome of Motor Cortex Derived Extracellular Vesicles Isolated from Amyotrophic Lateral Sclerosis Human Postmortem Tissues. Cells, 9(7). doi:10.3390/cells9071709
- Villar-Conde, S., Astillero-Lopez, V., Gonzalez-Rodriguez, M., Villanueva-Anguita, P., Saiz-Sanchez, D., Martinez-Marcos, A., . . . Ubeda-Bañon, I. (2021). The Human Hippocampus in Parkinson's Parkinson’s Disease: An Integrative Stereological and Proteomic Study. J Parkinsons Dis, 11(3), 1345-1365. doi:10.3233/jpd-202465
- Walker, F. O., & Raymond, L. A. (2004). Targeting energy metabolism in Huntington's Huntington’s disease. LANCET, 364(9431), 312-313. doi:10.1016/s0140-6736(04)16739-1
- Walton, C., King, R., Rechtman, L., Kaye, W., Leray, E., Marrie, R. A., . . . Baneke, P. (2020). Rising prevalence of multiple sclerosis worldwide: Insights from the Atlas of MS, third edition. Mult Scler, 26(14), 1816-1821. doi:10.1177/1352458520970841
- Wang, W., Zhao, F., Ma, X., Perry, G., & Zhu, X. (2020). Mitochondria dysfunction in the pathogenesis of Alzheimer's Alzheimer’s disease: recent advances. Mol Neurodegener, 15(1), 30. doi:10.1186/s13024-020-00376-6
- Wang, Y., & Mandelkow, E. (2016). Tau in physiology and pathology. Nat Rev Neurosci, 17(1), 5-21. doi:10.1038/nrn.2015.1
- Ward, M., Güntert, A., Campbell, J., & Pike, I. (2009). Proteomics for brain disorders--the promise for biomarkers. Annals of the New York Academy of Sciences, 1180, 68-74. doi:10.1111/j.1749-6632.2009.05018.x
- Wegrzynowicz, M., Holt, H. K., Friedman, D. B., & Bowman, A. B. (2012). Changes in the striatal proteome of YAC128Q mice exhibit gene-environment interactions between mutant huntingtin and manganese. JOURNAL OF PROTEOME RESEARCH, 11(2), 1118-1132. doi:10.1021/pr200839d
- Wesseling, H., Mair, W., Kumar, M., Schlaffner, C. N., Tang, S., Beerepoot, P., . . . Steen, J. A. (2020). Tau PTM Profiles Identify Patient Heterogeneity and Stages of Alzheimer's Disease. Cell, 183(6), 1699-1713.e1613. doi:10.1016/j.cell.2020.10.029
- Wyss-Coray, T., & Rogers, J. (2012). Inflammation in Alzheimer disease-a brief review of the basic science and clinical literature. Cold Spring Harb Perspect Med, 2(1), a006346. doi:10.1101/cshperspect.a006346
- Xiong, F., Ge, W., & Ma, C. (2019). Quantitative proteomics reveals distinct composition of amyloid plaques in Alzheimer's Alzheimer’s disease. Alzheimers Dement, 15(3), 429-440. doi:10.1016/j.jalz.2018.10.006
- Xu, B., Xiong, F., Tian, R., Zhan, S., Gao, Y., Qiu, W., . . . Ma, C. (2016). Temporal lobe in human aging: A quantitative protein profiling study of samples from Chinese Human Brain Bank. EXPERIMENTAL GERONTOLOGY, 73, 31-41. doi:10.1016/j.exger.2015.11.016
- Xu, J., Patassini, S., Rustogi, N., Riba-Garcia, I., Hale, B. D., Phillips, A. M., . . . Unwin, R. D. (2019). Regional protein expression in human Alzheimer's Alzheimer’s brain correlates with disease severity. Commun Biol, 2, 43. doi:10.1038/s42003-018-0254-9
- Yamagishi, Y., Saigoh, K., Saito, Y., Ogawa, I., Mitsui, Y., Hamada, Y., . . . Kusunoki, S. (2018). Diagnosis of Parkinson's Parkinson’s disease and the level of oxidized DJ-1 protein. Neurosci Res, 128, 58-62. doi:10.1016/j.neures.2017.06.008
- Yates, J. R., Ruse, C. I., & Nakorchevsky, A. (2009). Proteomics by mass spectrometry: approaches, advances, and applications. Annual Review of Biomedical Engineering, 11, 49-79. doi:10.1146/annurev-bioeng-061008-124934
- Zabel, C., Mao, L., Woodman, B., Rohe, M., Wacker, M. A., Kläre, Y., . . . Bates, G. P. (2009). A large number of protein expression changes occur early in life and precede phenotype onset in a mouse model for huntington disease. MOLECULAR & CELLULAR PROTEOMICS, 8(4), 720-734. doi:10.1074/mcp.M800277-MCP200
- Zhang, J., Zhang, Z. G., Morris, D., Li, Y., Roberts, C., Elias, S. B., & Chopp, M. (2009). Neurological functional recovery after thymosin beta4 treatment in mice with experimental auto encephalomyelitis. NEUROSCIENCE, 164(4), 1887-1893. doi:10.1016/j.neuroscience.2009.09.054
- Zou, Z. Y., Zhou, Z. R., Che, C. H., Liu, C. Y., He, R. L., & Huang, H. P. (2017). Genetic epidemiology of amyotrophic lateral sclerosis: a systematic review and meta-analysis. J Neurol Neurosurg Psychiatry, 88(7), 540-549. doi:10.1136/jnnp-2016-315018a
How to Cite
How to Cite
Downloads
Article Details
Most Read This Month
License
Copyright (c) 2022 Human Brain
This work is licensed under a Creative Commons Attribution-NoDerivatives 4.0 International License.