Differential expression of N-glycopeptides derived from serum glycoproteins in mild cognitive impairment (MCI) patients.

Item request has been placed! ×
Item request cannot be made. ×
loading   Processing Request
  • Additional Information
    • Source:
      Publisher: Wiley-VCH Country of Publication: Germany NLM ID: 101092707 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1615-9861 (Electronic) Linking ISSN: 16159853 NLM ISO Abbreviation: Proteomics Subsets: MEDLINE
    • Publication Information:
      Original Publication: Weinheim, Germany : Wiley-VCH,
    • Subject Terms:
    • Abstract:
      Mild cognitive impairment (MCI) is an early stage of memory loss that affects cognitive abilities with the aging of individuals, such as language or visual/spatial comprehension. MCI is considered a prodromal phase of more complicated neurodegenerative diseases such as Alzheimer's. Therefore, accurate diagnosis and better understanding of the disease prognosis will facilitate prevention of neurodegeneration. However, the existing diagnostic methods fail to provide precise and well-timed diagnoses, and the pathophysiology of MCI is not fully understood. Alterations of the serum N-glycoproteome expression could represent an essential contributor to the overall pathophysiology of neurodegenerative diseases and be used as a potential marker to assess MCI diagnosis using less invasive procedures. In this approach, we identified N-glycopeptides with different expressions between healthy and MCI patients from serum glycoproteins. Seven of the N-glycopeptides showed outstanding AUC values, among them the antithrombin-III Asn224 + 4-5-0-2 with an AUC value of 1.00 and a p value of 0.0004. According to proteomics and ingenuity pathway analysis (IPA), our data is in line with recent publications, and the glycoproteins carrying the identified N-sites play an important role in neurodegeneration.
      (© 2024 Wiley‐VCH GmbH.)
    • References:
      Petersen, R. C., & Negash, S. (2008). Mild cognitive impairment: An overview. CNS Spectrums, 13, 45–53.
      Petersen, R. C., Smith, G. E., Waring, S. C., Ivnik, R. J., Tangalos, E. G., & Kokmen, E. (1999). Mild cognitive impairment: Clinical characterization and outcome. Archives of Neurology, 56, 303–308.
      Grundman, M. (2004). Mild cognitive impairment can be distinguished from Alzheimer disease and normal aging for clinical trials. Archives of Neurology, 61, 59–66.
      Lindeboom, J., & Weinstein, H. (2004). Neuropsychology of cognitive ageing, minimal cognitive impairment, Alzheimer's disease, and vascular cognitive impairment. European Journal of Pharmacology, 490, 83–86.
      Levey, A., Lah, J., Goldstein, F., Steenland, K., & Bliwise, D. (2006). Mild cognitive impairment: An opportunity to identify patients at high risk for progression to Alzheimer's disease. Clinical Therapeutics, 28, 991–1001.
      Petersen, R. C., Doody, R., Kurz, A., Mohs, R. C., Morris, J. C., Rabins, P. V., Ritchie, K., Rossor, M., Thal, L., & Winblad, B. (2001). Current concepts in mild cognitive impairment. Archives of Neurology, 58, 1985–1992.
      Zhang, D., & Shen, D. (2012). Predicting future clinical changes of MCI patients using longitudinal and multimodal biomarkers. PLoS ONE, 7, e33182.
      Davatzikos, C., Bhatt, P., Shaw, L. M., Batmanghelich, K. N., & Trojanowski, J. Q. (2011). Prediction of MCI to AD conversion, via MRI, CSF biomarkers, and pattern classification. Neurobiology of Aging, 32, 2322e19. e2319‐2327.
      Solfrizzi, V., Panza, F., Colacicco, A. M., D'introno, A., Capurso, C., Torres, F., Grigoletto, F., Maggi, S., Del Parigi, A., Reiman, E. M., Caselli, R. J., Scafato, E., Farchi, G., & Capurso, A. (2004). Vascular risk factors, incidence of MCI, and rates of progression to dementia. Neurology, 63, 1882–1891.
      Da, X., Toledo, J. B., Zee, J., Wolk, D. A., Xie, S. X., Ou, Y., Shacklett, A., Parmpi, P., Shaw, L., Trojanowski, J. Q., & Davatzikos, C. (2014). Integration and relative value of biomarkers for prediction of MCI to AD progression: Spatial patterns of brain atrophy, cognitive scores, APOE genotype and CSF biomarkers. NeuroImage. Clinical, 4, 164–173.
      Dennis, J. W., Granovsky, M., & Warren, C. E. (1999). Protein glycosylation in development and disease. BioEssays, 21, 412–421.
      Huang, Y., Zhou, S., Zhu, J., Lubman, D. M., & Mechref, Y. (2017). LC‐MS/MS isomeric profiling of permethylated N‐glycans derived from serum haptoglobin of hepatocellular carcinoma (HCC) and cirrhotic patients. Electrophoresis, 38, 2160–2167.
      Gutierrez Reyes, C. D., Jiang, P., Donohoo, K., Atashi, M., & Mechref, Y. S. (2021). Glycomics and glycoproteomics: Approaches to address isomeric separation of glycans and glycopeptides. Journal of Separation Science, 44, 403–425.
      Gutierrez‐Reyes, C. D., Jiang, P., Atashi, M., Bennett, A., Yu, A., Peng, W., Zhong, J., & Mechref, Y. (2022). Advances in mass spectrometry‐based glycoproteomics: An update covering the period 2017–2021. Electrophoresis, 43, 370–387.
      Brownlee, M. (1995). Advanced protein glycosylation in diabetes and aging. Annual Review of Medicine, 46, 223–234.
      Zhu, J., Huang, J., Zhang, J., Chen, Z., Lin, Y. u, Grigorean, G., Li, L., Liu, S., Singal, A. G., Parikh, N. D., & Lubman, D. M. (2020). Glycopeptide biomarkers in serum haptoglobin for hepatocellular carcinoma detection in patients with nonalcoholic steatohepatitis. Journal of Proteome Research, 19, 3452–3466.
      Dotz, V., Visconti, A., Lomax‐Browne, H. J., Clerc, F., Hipgrave Ederveen, A. L., Medjeral‐Thomas, N. R., Cook, H. T., Pickering, M. C., Wuhrer, M., & Falchi, M. (2021). O‐ and N‐glycosylation of serum immunoglobulin A is associated with IgA nephropathy and glomerular function. Journal of the American Society of Nephrology, 32, 2455–2465.
      Gutierrez Reyes, C. D., Huang, Y., Atashi, M., Zhang, J., Zhu, J., Liu, S., Parikh, N. D., Singal, A. G., Dai, J., Lubman, D. M., & Mechref, Y. (2021). PRM‐MS quantitative analysis of isomeric N‐glycopeptides derived from human serum haptoglobin of patients with cirrhosis and hepatocellular carcinoma. Metabolites, 11, 563.
      Stowell, S. R., Ju, T., & Cummings, R. D. (2015). Protein glycosylation in cancer. Annual Review of Pathology, 10, 473–510.
      Pinho, S. S., & Reis, C. A. (2015). Glycosylation in cancer: Mechanisms and clinical implications. Nature Reviews Cancer, 15, 540–555.
      Chen, Z., Yu, Q., Hao, L., Liu, F., Johnson, J., Tian, Z., Kao, W. J., Xu, W., & Li, L. (2018). Site‐specific characterization and quantitation of N‐glycopeptides in PKM2 knockout breast cancer cells using DiLeu isobaric tags enabled by electron‐transfer/higher‐energy collision dissociation (EThcD). Analyst, 143, 2508–2519.
      Alvarez, M. R. S., Zhou, Q., Tena, J., Lebrilla, C. B., Completo, G. C., Heralde, F. M., Cabanatan, M., Barzaga, M. T., Tan‐Liu, N., Ladrera, G. I., Danguilan, J. L., Rabajante, J., Padolina, I., & Nacario, R. C. (2022). N‐glycan and glycopeptide serum biomarkers in Philippine lung cancer patients identified using liquid chromatography‐tandem mass spectrometry. ACS Omega, 7, 40230–40240.
      Palmigiano, A., Barone, R., Sturiale, L., Sanfilippo, C., Bua, R. O., Romeo, D. A., Messina, A., Capuana, M. L., Maci, T., Le Pira, F., Zappia, M., & Garozzo, D. (2016). CSF N‐glycoproteomics for early diagnosis in Alzheimer's disease. Journal of Proteomics, 131, 29–37.
      Lundström, S. L., Yang, H., Lyutvinskiy, Y., Rutishauser, D., Herukka, S.‐K., Soininen, H., & Zubarev, R. A. (2014). Blood plasma IgG Fc glycans are significantly altered in Alzheimer's disease and progressive mild cognitive impairment. Journal of Alzheimer's Disease, 38, 567–579.
      Giau, V. O. V., Bagyinszky, E., & An, S. S. A. (2019). Potential fluid biomarkers for the diagnosis of mild cognitive impairment. International Journal of Molecular Sciences, 4149, 20(17), 4149.
      Schedin‐Weiss, S., Gaunitz, S., Sui, P., Chen, Q., Haslam, S. M., Blennow, K., Winblad, B., Dell, A., & Tjernberg, L. O. (2020). Glycan biomarkers for Alzheimer disease correlate with T‐tau and P‐tau in cerebrospinal fluid in subjective cognitive impairment. FEBS Journal, 287, 3221–3234.
      Haukedal, H., & Freude, K. K. (2021). Implications of glycosylation in Alzheimer's disease. Frontiers in Neuroscience, 14, 625348.
      Llop, E., Ardá, A., Zacco, E., O'flaherty, R., García‐Ayllón, M.‐S., Aureli, M., Frenkel‐Pinter, M., Reis, C. A., Greiner‐Tollersrud, O. K., & Cuchillo‐Ibáñez, I. (2022). Proceedings of workshop: “Neuroglycoproteins in health and disease”, INNOGLY cost action. Glycoconjugate Journal, 5, 579–586.
      Chen, Z., Yu, Q., Yu, Q., Johnson, J., Shipman, R., Zhong, X., Huang, J., Asthana, S., Carlsson, C., Okonkwo, O., & Li, L. (2021). In‐depth site‐specific analysis of N‐glycoproteome in human cerebrospinal fluid and glycosylation landscape changes in Alzheimer's disease. Molecular & Cellular Proteomics, 20, 100081.
      Reyes, C. D. G., Hakim, M. d. A., Atashi, M., Goli, M., Gautam, S., Wang, J., Bennett, A. I., Zhu, J., Lubman, D. M., & Mechref, Y. (2022). LC‐MS/MS isomeric profiling of N‐glycans derived from low‐abundant serum glycoproteins in mild cognitive impairment patients. Biomolecules, 12, 1657.
      Zhang, Q., Ma, C., Chin, L.‐S., & Li, L. (2020). Integrative glycoproteomics reveals protein N‐glycosylation aberrations and glycoproteomic network alterations in Alzheimer's disease. Science Advances, 6, eabc5802.
      Freeze, H. H., Eklund, E. A., Ng, B. G., & Patterson, M. C. (2015). Neurological aspects of human glycosylation disorders. Annual Review of Neuroscience, 38, 105–125.
      Albert, M. S., Dekosky, S. T., Dickson, D., Dubois, B., Feldman, H. H., Fox, N. C., Gamst, A., Holtzman, D. M., Jagust, W. J., Petersen, R. C., Snyder, P. J., Carrillo, M. C., Thies, B., & Phelps, C. H. (2011). The diagnosis of mild cognitive impairment due to Alzheimer's disease: Recommendations from the National Institute on Aging‐Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimer's & Dementia, 7, 270–279.
      Pan, S., Chen, R., Aebersold, R., & Brentnall, T. A. (2011). Mass spectrometry based glycoproteomics–from a proteomics perspective. Molecular & Cellular Proteomics, 10, R110.003251.
      Donohoo, K. B., Wang, J., Goli, M., Yu, A., Peng, W., Hakim, M. A., & Mechref, Y. (2021). Advances in mass spectrometry‐based glycomics‐An update covering the period 2017–2021. Electrophoresis, 43(1–2), 119–142.
      Dong, X., Huang, Y., Cho, B. G., Zhong, J., Gautam, S., Peng, W., Williamson, S. D., Banazadeh, A., Torres‐Ulloa, K. Y., & Mechref, Y. (2018). Advances in mass spectrometry‐based glycomics. Electrophoresis, 39, 3063–3081.
      Tsai, T.‐H., Wang, M., Di Poto, C., Hu, Y., Zhou, S., Zhao, Y., Varghese, R. S., Luo, Y., Tadesse, M. G., Ziada, D. H., Desai, C. S., Shetty, K., Mechref, Y., & Ressom, H. W. (2014). LC‐MS profiling of N‐Glycans derived from human serum samples for biomarker discovery in hepatocellular carcinoma. Journal of Proteome Research, 13, 4859–4868.
      Dong, M., Lih, T.‐S. M., Höti, N., Chen, S.‐Y., Ponce, S., Partin, A., & Zhang, H. (2021). Development of parallel reaction monitoring assays for the detection of aggressive prostate cancer using urinary glycoproteins. Journal of Proteome Research, 20, 3590–3599.
      Kim, K. H., Lee, S. Y., Kim, D. G., Lee, S.‐Y., Kim, J. Y., & Yoo, J. S. (2020). Absolute quantification of N‐glycosylation of alpha‐fetoprotein using parallel reaction monitoring with stable isotope‐labeled N‐glycopeptide as an internal standard. Analytical Chemistry, 92, 12588–12595.
      Kim, K. H., Park, G. W., Jeong, J. E., Ji, E. S., An, H. J., Kim, J. Y., & Yoo, J. S. (2019). Parallel reaction monitoring with multiplex immunoprecipitation of N‐glycoproteins in human serum for detection of hepatocellular carcinoma. Analytical and Bioanalytical Chemistry, 411, 3009–3019.
      Ronsein, G. E., Pamir, N., Von Haller, P. D., Kim, D. S., Oda, M. N., Jarvik, G. P., Vaisar, T., & Heinecke, J. W. (2015). Parallel reaction monitoring (PRM) and selected reaction monitoring (SRM) exhibit comparable linearity, dynamic range and precision for targeted quantitative HDL proteomics. Journal of Proteomics, 113, 388–399.
      Gutierrez Reyes, C. D., Sanni, A., Adeniyi, M., Mogut, D., Najera Gonzalez, H. R., Ahmadi, P., Atashi, M., Onigbinde, S., & Mechref, Y. (2024). In S. B. Bradfute (Ed.), Recombinant glycoproteins: Methods and protocols (pp. 231–250). Springer US.
      Gallien, S., Bourmaud, A., Kim, S. Y., & Domon, B. (2014). Technical considerations for large‐scale parallel reaction monitoring analysis. Journal of Proteomics, 100, 147–159.
      Peterson, A. C., Russell, J. D., Bailey, D. J., Westphall, M. S., & Coon, J. J. (2012). Parallel reaction monitoring for high resolution and high mass accuracy quantitative, targeted proteomics. Molecular & Cellular Proteomics, 11, 1475–1488.
      Squitti, R., Quattrocchi, C. C., Forno, G. D., Antuono, P., Wekstein, D. R., Capo, C. R., Salustri, C., & Rossini, P. M. (2007). Ceruloplasmin (2‐D PAGE) pattern and copper content in serum and brain of Alzheimer disease patients. Biomarker Insights, 1, 205–213.
      Tu, C., Rudnick, P. A., Martinez, M. Y., Cheek, K. L., Stein, S. E., Slebos, R. J. C., & Liebler, D. C. (2010). Depletion of abundant plasma proteins and limitations of plasma proteomics. Journal of Proteome Research, 9, 4982–4991.
      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 disease. Alzheimer's & Dementia (New York, N. Y.), 4, 575–590.
      Meraz‐Ríos, M. A., Toral‐Rios, D., Franco‐Bocanegra, D., Villeda‐Hernández, J., & Campos‐Peña, V. (2013). Inflammatory process in Alzheimer's disease. Frontiers in Integrative Neuroscience, 7, 59.
      Dalakas, M. C., Alexopoulos, H., & Spaeth, P. J. (2020). Complement in neurological disorders and emerging complement‐targeted therapeutics. Nature Reviews Neurology, 16, 601–617.
      Sandoval‐Hernández, A. G., Buitrago, L., Moreno, H., Cardona‐Gómez, G. P., & Arboleda, G. (2015). Role of liver X receptor in AD pathophysiology. PLoS ONE, 10, e0145467.
      Mizuno, S., Iijima, R., Ogishima, S., Kikuchi, M., Matsuoka, Y., Ghosh, S., Miyamoto, T., Miyashita, A., Kuwano, R., & Tanaka, H. (2012). AlzPathway: A comprehensive map of signaling pathways of Alzheimer's disease. BMC Systems Biology, 6, 52.
      Pollio, G., Hoozemans, J. J. M., Andersen, C. A., Roncarati, R., Rosi, M. C., Van Haastert, E. S., Seredenina, T., Diamanti, D., Gotta, S., Fiorentini, A., Magnoni, L., Raggiaschi, R., Rozemuller, A. J. M., Casamenti, F., Caricasole, A., & Terstappen, G. C. (2008). Increased expression of the oligopeptidase THOP1 is a neuroprotective response to Abeta toxicity. Neurobiology of Disease, 31, 145–158.
      Husain, M. A., Laurent, B., & Plourde, M. (2021). APOE and Alzheimer's disease: From lipid transport to physiopathology and therapeutics. Frontiers in Neuroscience, 15, 630502.
      Barone, R., Sturiale, L., Palmigiano, A., Zappia, M., & Garozzo, D. (2012). Glycomics of pediatric and adulthood diseases of the central nervous system. Journal of Proteomics, 75, 5123–5139.
      Van Kooyk, Y., & Rabinovich, G. A. (2008). Protein‐glycan interactions in the control of innate and adaptive immune responses. Nature Immunology, 9, 593–601.
      Blixt, O., Collins, B. E., Van Den Nieuwenhof, I. M., Crocker, P. R., & Paulson, J. C. (2003). Sialoside specificity of the siglec family assessed using novel multivalent probes: Identification of potent inhibitors of myelin‐associated glycoprotein. Journal of Biological Chemistry, 278, 31007–31019.
      Kalaria, R. N., Golde, T., Kroon, S. N., & Perry, G. (1993). Serine protease inhibitor antithrombin III and its messenger RNA in the pathogenesis of Alzheimer's disease. American Journal of Pathology, 143, 886–893.
      Begic, E., Hadzidedic, S., Obradovic, S., Begic, Z., & Causevic, M. (2020). Increased levels of coagulation factor XI in plasma are related to Alzheimer's disease diagnosis. Journal of Alzheimer's Disease, 77, 375–386.
      Bots, M. L., Breteler, M. M. B., Van Kooten, F., Haverkate, F., Meijer, P., Koudstaal, P. J., Grobbee, D. E., & Kluft, C. (1998). Coagulation and fibrinolysis markers and risk of dementia. Pathophysiology of Haemostasis and Thrombosis, 28, 216–222.
      Hu, Y., Hosseini, A., Kauwe, J. S. K., Gross, J., Cairns, N. J., Goate, A. M., Fagan, A. M., Townsend, R. R., & Holtzman, D. M. (2007). Identification and validation of novel CSF biomarkers for early stages of Alzheimer's disease. Proteomics Clinical Applications, 1, 1373–1384.
      Yang, M.‐H., Yang, Y.‐H., Lu, C.‐Y., Jong, S.‐B., Chen, L.‐J., Lin, Y.‐F., Wu, S.‐J., Chu, P.‐Y., Chung, T. W., & Tyan, Y. U.‐C. (2012). Activity‐dependent neuroprotector homeobox protein: A candidate protein identified in serum as diagnostic biomarker for Alzheimer's disease. Journal of Proteomics, 75, 3617–3629.
      Elsaadani, M., Ahmed, S. M., Jacovides, C., Lopez, A., Johnson, V. E., Kaplan, L. J., Smith, D. H., & Pascual, J. L. (2021). Post‐traumatic brain injury antithrombin III recovers Morris water maze cognitive performance, improving cued and spatial learning. The Journal of Trauma and Acute Care Surgery, 91, 108–113.
      Puchades, M., Hansson, S. F., Nilsson, C. L., Andreasen, N., Blennow, K., & Davidsson, P. (2003). Proteomic studies of potential cerebrospinal fluid protein markers for Alzheimer's disease. Brain Research Molecular Brain Research, 118, 140–146.
      Porcellini, E., Davis, E., Chiappelli, M., Ianni, E., Di Stefano, G., Forti, P., Ravaglia, G., & Licastro, F. (2008). Elevated plasma levels of alpha‐1‐anti‐chymotrypsin in age‐related cognitive decline and Alzheimer's disease: A potential therapeutic target. Current Pharmaceutical Design, 14, 2659–2664.
      Liu, S., Pan, J., Tang, K., Lei, Q., He, L., Cai, X., & Li, Z. (2021). Alpha 1‐antichymotrypsin may be a biomarker for the progression of amnestic mild cognitive impairment. Acta Neurologica Belgica, 121, 451–464.
      Padmanabhan, J., Levy, M., Dickson, D. W., & Potter, H. (2006). Alpha1‐antichymotrypsin, an inflammatory protein overexpressed in Alzheimer's disease brain, induces tau phosphorylation in neurons. Brain, 129, 3020–3034.
      Nilsson, L. N. G., Arendash, G. W., Leighty, R. E., Costa, D. A., Low, M. A., Garcia, M. F., Cracciolo, J. R., Rojiani, A., Wu, X., Bales, K. R., Paul, S. M., & Potter, H. (2004). Cognitive impairment in PDAPP mice depends on ApoE and ACT‐catalyzed amyloid formation. Neurobiology of Aging, 25, 1153–1167.
      Abraham, C. (2001). Reactive astrocytes and alpha1‐antichymotrypsin in Alzheimer's disease. Neurobiology of Aging, 22, 931–936.
      Abraham, C. R., Selkoe, D. J., & Potter, H. (1988). Immunochemical identification of the serine protease inhibitor α1‐antichymotrypsin in the brain amyloid deposits of Alzheimer's disease. Cell, 52, 487–501.
      Fatoba, O., Itokazu, T., & Yamashita, T. (2022). Complement cascade functions during brain development and neurodegeneration. FEBS Journal, 289, 2085–2109.
      Van Der Ende, E. L., Heller, C., Sogorb‐Esteve, A., Swift, I. J., Mcfall, D., Peakman, G., Bouzigues, A., Poos, J. M., Jiskoot, L. C., Panman, J. L., Papma, J. M., Meeter, L. H., Dopper, E. G. P., Bocchetta, M., Todd, E., Cash, D., Graff, C., Synofzik, M., Moreno, F., & Zulaica, M. (2022). Elevated CSF and plasma complement proteins in genetic frontotemporal dementia: Results from the GENFI study. Journal of Neuroinflammation, 19, 217.
      Hong, S., Beja‐Glasser, V. F., Nfonoyim, B. M., Frouin, A., Li, S., Ramakrishnan, S., Merry, K. M., Shi, Q., Rosenthal, A., Barres, B. A., Lemere, C. A., Selkoe, D. J., & Stevens, B. (2016). Complement and microglia mediate early synapse loss in Alzheimer mouse models. Science, 352, 712–716.
      Krukowski, K., Chou, A., Feng, X., Tiret, B., Paladini, M.‐S., Riparip, L.‐K., Chaumeil, M., Lemere, C., & Rosi, S. (2018). Traumatic brain injury in aged mice induces chronic microglia activation, synapse loss, and complement‐dependent memory deficits. International Journal of Molecular Sciences, 3753, 19, 3753.
      Schafer, D. P., Lehrman, E. K., Kautzman, A. G., Koyama, R., Mardinly, A. R., Yamasaki, R., Ransohoff, R. M., Greenberg, M. E., Barres, B. A., & Stevens, B. (2012). Microglia sculpt postnatal neural circuits in an activity and complement‐dependent manner. Neuron, 74, 691–705.
      Goetzl, E. J., Schwartz, J. B., Abner, E. L., Jicha, G. A., & Kapogiannis, D. (2018). High complement levels in astrocyte‐derived exosomes of Alzheimer disease. Annals of Neurology, 83, 544–552.
      Morgan, A. R., Touchard, S., Leckey, C., O'hagan, C., Nevado‐Holgado, A. J., Barkhof, F., Bertram, L., Blin, O., Bos, I., Dobricic, V., Engelborghs, S., Frisoni, G., Frölich, L., Gabel, S., Johannsen, P., Kettunen, P., Kłoszewska, I., Legido‐Quigley, C., Lleó, A., & Morgan, B. P. (2019). Inflammatory biomarkers in Alzheimer's disease plasma. Alzheimer's & Dementia, 15, 776–787.
      Winston, C. N., Goetzl, E. J., Schwartz, J. B., Elahi, F. M., & Rissman, R. A. (2019). Complement protein levels in plasma astrocyte‐derived exosomes are abnormal in conversion from mild cognitive impairment to Alzheimer's disease dementia. Alzheimer's & Dementia, 11, 61–66.
      Kitamura, Y., Kojima, M., Kurosawa, T., Sasaki, R., Ichihara, S., Hiraku, Y., Tomimoto, H., Murata, M., & Oikawa, S. (2018). Proteomic profiling of exosomal proteins for blood‐based biomarkers in Parkinson's disease. Neuroscience, 392, 121–128.
      Hye, A., Lynham, S., Thambisetty, M., Causevic, M., Campbell, J., Byers, H. L., Hooper, C., Rijsdijk, F., Tabrizi, S. J., Banner, S., Shaw, C. E., Foy, C., Poppe, M., Archer, N., Hamilton, G., Powell, J., Brown, R. G., Sham, P., Ward, M., & Lovestone, S. (2006). Proteome‐based plasma biomarkers for Alzheimer's disease. Brain, 129, 3042–3050.
      Lehtimäki, K. A., Peltola, J., Liimatainen, S., Haapala, A.‐M., & Arvio, M. (2011). Cardiolipin and β2‐Glycoprotein I antibodies associate with cognitive impairment and seizure frequency in developmental disorders. Seizure: The Journal of the British Epilepsy Association, 20, 438–441.
      Hellman, N. E., & Gitlin, J. D. (2002). Ceruloplasmin metabolism and function. Annual Review of Nutrition, 22, 439–458.
    • Grant Information:
      1R01GM112490-08(YM) United States NH NIH HHS; 1R01GM130091-05(YM) United States NH NIH HHS; 1U01CA225753-05(YM/DML) United States NH NIH HHS; 1R01GM112490-08(YM) United States NH NIH HHS; 1R01GM130091-05(YM) United States NH NIH HHS; 1U01CA225753-05(YM/DML) United States NH NIH HHS; 3R01CA160254(DML) National Cancer Institute (NCI); 3R01CA160254-S1(DML) National Cancer Institute (NCI); D-0005(YM) Robert A. Welch Foundation; The CH Foundation (YM)
    • Contributed Indexing:
      Keywords: Biomarker N‐glycopeptide; MCI; Neurological disorder
    • Accession Number:
      0 (Glycopeptides)
      0 (Glycoproteins)
      0 (Biomarkers)
    • Publication Date:
      Date Created: 20240411 Date Completed: 20241010 Latest Revision: 20241010
    • Publication Date:
      20241011
    • Accession Number:
      10.1002/pmic.202300620
    • Accession Number:
      38602241