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Current Proteomics


ISSN (Print): 1570-1646
ISSN (Online): 1875-6247

Research Article

iTRAQ-based Quantitative Proteomic Analysis of Dural Tissues Reveals Upregulated Haptoglobin to be a Potential Biomarker of Moyamoya Disease

Author(s): Xiaojun Zhang, Lin Yin, Xiaofang Jia, Yujiao Zhang, Tiefu Liu and Lijun Zhang*

Volume 18, Issue 1, 2021

Published on: 09 December, 2019

Page: [27 - 37] Pages: 11

DOI: 10.2174/1570164617666191210103652

Price: $65


Background: Moyamoya Disease (MMD) is a rare cerebrovascular disease with a high rate of disability and mortality. Immune reactions have been implicated in the pathogenesis of MMD, however, the underlying mechanism is still unclear.

Objective: To identify proteins related to MMD specially involved in the immunogenesis, we performed a proteomic study.

Methods: In this work, dural tissues or plasma from 98 patients with MMD, 17 disease controls without MMD, and 12 healthy donors were included. Proteomic profiles of dural tissues from 4 MMD and 4 disease controls were analyzed by an isobaric tag for relative and absolute quantitation (iTRAQ)- based proteomics. The immune-related proteins were explored by bioinformatics and the key MMDrelated proteins were verified by western blot, multiple reaction monitoring methods, enzyme-linked immunosorbent assay, and tissue microarray.

Results: 1,120 proteins were identified, and 82 MMD-related proteins were found with more than 1.5 fold difference compared with those in the control samples. Gene Ontology analysis showed that 29 proteins were immune-related. In particular, Haptoglobin (HP) was up-regulated in dural tissue and plasma of MMD samples compared to the controls, and its up-regulation was found to be sex- and MMD Suzuki grade dependent. Through Receiver Operating Characteristic (ROC) analysis, HP can well discriminate MMD and healthy donors with the Area Under the Curve (AUC) of 0.953.

Conclusion: We identified the biggest protein database of the dura mater. 29 out of 82 differentially expressed proteins in MMD are involved in the immune process. Of which, HP was up-regulated in dural tissue and plasma of MMD, with sex- and MMD Suzuki grade-dependence. HP might be a potential biomarker of MMD.

Keywords: Moyamoya disease, dura mater, proteomics, iTRAQ, haptoglobin, strokes.

Graphical Abstract
Suzuki, J.; Kodama, N. Moyamoya disease--a review. Stroke, 1983, 14(1), 104-109.
[] [PMID: 6823678]
Bang, O.Y.; Fujimura, M.; Kim, S.K. The pathophysiology of Moyamoya disease: An update. J. Stroke, 2016, 18(1), 12-20.
[] [PMID: 26846756]
Hishikawa, T.; Sugiu, K.; Date, I. Moyamoya disease: A review of clinical research. Acta Med. Okayama, 2016, 70(4), 229-236.
[PMID: 27549666]
Huang, S.; Guo, Z.N.; Shi, M.; Yang, Y.; Rao, M. Etiology and pathogenesis of Moyamoya disease: An update on disease prevalence. Int. J. Stroke, 2017, 12(3), 246-253.
[] [PMID: 28381201]
Kim, J.S. Moyamoya disease: Epidemiology, clinical features, and diagnosis. J. Stroke, 2016, 18(1), 2-11.
[] [PMID: 26846755]
Feghali, J.; Xu, R.; Yang, W.; Liew, J.A.; Blakeley, J.; Ahn, E.S.; Tamargo, R.J.; Huang, J. Moyamoya disease versus moyamoya syndrome: comparison of presentation and outcome in 338 hemispheres. J. Neurosurg., 2019, 1-9. Epub ahead of print
[] [PMID: 31585423]
Hu, J.; Luo, J.; Chen, Q. The susceptibility pathogenesis of Moyamoya disease. World Neurosurg., 2017, 101, 731-741.
[] [PMID: 28153617]
Bersano, A.; Guey, S.; Bedini, G.; Nava, S.; Hervé, D.; Vajkoczy, P.; Tatlisumak, T.; Sareela, M.; van der Zwan, A.; Klijn, C.J.; Braun, K.P.; Kronenburg, A.; Acerbi, F.; Brown, M.M.; Calviere, L.; Cordonnier, C.; Henon, H.; Thines, L.; Khan, N.; Czabanka, M.; Kraemer, M.; Simister, R.; Prontera, P.; Tournier-Lasserve, E.; Parati, E. Research progresses in understanding the pathophysiology of Moyamoya disease. Cerebrovasc. Dis., 2016, 41(3-4), 105-118.
[] [PMID: 26756907]
Campbell, S.; Monagle, P.; Newall, F. Oral anticoagulant therapy interruption in children: A single centre experience. Thromb. Res., 2016, 140, 89-93.
[] [PMID: 26928454]
Feghali, J.; Xu, R.; Yang, W.; Liew, J.; Tamargo, R.J.; Marsh, E.B.; Huang, J. Racial phenotypes in Moyamoya disease: A comparative analysis of clinical presentation and natural history in a single multiethnic cohort of 250 hemispheres. J. Neurosurg., 2019, 101. Epub ahead of print
[] [PMID: 31585430]
Hori, S.; Kashiwazaki, D.; Yamamoto, S.; Acker, G.; Czabanka, M.; Akioka, N.; Kuwayama, N.; Vajkoczy, P.; Kuroda, S. Impact of interethnic difference of collateral angioarchitectures on prevalence of hemorrhagic stroke in Moyamoya disease. Neurosurgery, 2019, 85(1), 134-146.
[] [PMID: 29889273]
Jeon, J.P.; Kim, J.E. A recent update of clinical and research topics concerning adult Moyamoya disease. J. Korean Neurosurg. Soc., 2016, 59(6), 537-543.
[] [PMID: 27847564]
Im, S.H.; Cho, C.B.; Joo, W.I.; Chough, C.K.; Park, H.K.; Lee, K.J.; Rha, H.K. Prevalence and epidemiological features of Moyamoya disease in Korea. J. Cerebrovasc. Endovasc. Neurosurg., 2012, 14(2), 75-78.
[] [PMID: 23210031]
Mineharu, Y.; Liu, W.; Inoue, K.; Matsuura, N.; Inoue, S.; Takenaka, K.; Ikeda, H.; Houkin, K.; Takagi, Y.; Kikuta, K.; Nozaki, K.; Hashimoto, N.; Koizumi, A. Autosomal dominant moyamoya disease maps to chromosome 17q25.3. Neurology, 2008, 70(24 Pt 2), 2357-2363.
[] [PMID: 18463369]
Ge, P.; Zhang, Q.; Ye, X.; Liu, X.; Deng, X.; Li, H.; Wang, R.; Zhang, Y.; Zhang, D.; Zhao, J. Long-term outcome after conservative treatment and direct bypass surgery of Moyamoya disease at late suzuki stage. World Neurosurg., 2017, 103, 283-290.
[] [PMID: 28366750]
Lee, S.U.; Oh, C.W.; Kwon, O.K.; Bang, J.S.; Ban, S.P.; Byoun, H.S.; Kim, T. Surgical treatment of adult Moyamoya disease. Curr. Treat. Options Neurol., 2018, 20(7), 22.
[] [PMID: 29808372]
Konieczny, M.J.; Ri, S.J.; Georgiadis, J.R. Omental approach to functional recovery after cerebrovascular disease. World Neurosurg., 2016, 87, 406-416.
[] [PMID: 26493716]
Yun, T.J.; Paeng, J.C.; Sohn, C.H.; Kim, J.E.; Kang, H.S.; Yoon, B.W.; Choi, S.H.; Kim, J.H.; Lee, H.Y.; Han, M.H.; Zaharchuk, G. Monitoring cerebrovascular reactivity through the use of arterial spin labeling in patients with Moyamoya disease. Radiology, 2016, 278(1), 205-213.
[] [PMID: 26197057]
Yoshino, T.; Muro, K.; Yamaguchi, K.; Nishina, T.; Denda, T.; Kudo, T.; Okamoto, W.; Taniguchi, H.; Akagi, K.; Kajiwara, T.; Hironaka, S.; Satoh, T. Clinical validation of a multiplex kit for RAS mutations in colorectal cancer: Results of the RASKET (RAS KEy Testing) prospective, multicenter study. EBioMedicine, 2015, 2(4), 317-323.
[] [PMID: 26137573]
Kleinloog, R.; Regli, L.; Rinkel, G.J.; Klijn, C.J. Regional differences in incidence and patient characteristics of Moyamoya disease: a systematic review. J. Neurol. Neurosurg. Psychiatry, 2012, 83(5), 531-536.
[] [PMID: 22378916]
Baba, T.; Houkin, K.; Kuroda, S. Novel epidemiological features of Moyamoya disease. J. Neurol. Neurosurg. Psychiatry, 2008, 79(8), 900-904.
[] [PMID: 18077479]
Chung, J.W.; Kim, D.H.; Oh, M.J.; Cho, Y.H.; Kim, E.H.; Moon, G.J.; Ki, C.S.; Cha, J.; Kim, K.H.; Jeon, P.; Yeon, J.Y.; Kim, G.M.; Kim, J.S.; Hong, S.C.; Bang, O.Y. Cav-1 (Caveolin-1) and arterial remodeling in adult moyamoya disease. Stroke, 2018, 49(11), 2597-2604.
[] [PMID: 30355208]
Zhang, Q.; Liu, Y.; Zhang, D.; Wang, R.; Zhang, Y.; Wang, S.; Yu, L.; Lu, C.; Liu, F.; Zhou, J.; Zhang, X.; Zhao, J. RNF213 as the major susceptibility gene for Chinese patients with Moyamoya disease and its clinical relevance. J. Neurosurg., 2016, 1-8.
[PMID: 27128593]
Tashiro, R.; Fujimura, M.; Niizuma, K.; Endo, H.; Sakata, H.; Sato-Maeda, M.; Tominaga, T. De novo development of Moyamoya disease in an adult female with a genetic variant of the RNF-213 gene: Case report. J. Stroke Cerebrovasc. Dis., 2017, 26(1), e8-e11.
[] [PMID: 27789153]
Hosokawa, Y.; Kiyosawa, K.; Kato, R.; Okutomi, T.; Okamoto, H. Retrospective review of labor analgesia for parturients with Moyamoya disease. Masui, 2016, 65(8), 811-816.
[PMID: 30351592]
Akagawa, H.; Mukawa, M.; Nariai, T.; Nomura, S.; Aihara, Y.; Onda, H.; Yoneyama, T.; Kudo, T.; Sumita, K.; Maehara, T.; Kawamata, T.; Kasuya, H. Novel and recurrent RNF213 variants in Japanese pediatric patients with Moyamoya disease. Hum. Genome Var., 2018, 5, 17060.
[] [PMID: 29387438]
Wang, Y.; Mambiya, M.; Li, Q.; Yang, L.; Jia, H.; Han, Y.; Liu, W. RNF213 p.R4810K Polymorphism and the risk of Moyamoya disease, intracranial major artery stenosis/occlusion, and quasi-Moyamoya disease: A meta-analysis. J. Stroke Cerebrovasc. Dis., 2018, 27(8), 2259-2270.
[] [PMID: 29752070]
Kang, H.S.; Moon, Y.J.; Kim, Y.Y.; Park, W.Y.; Park, A.K.; Wang, K.C.; Kim, J.E.; Phi, J.H.; Lee, J.Y.; Kim, S.K. Smooth-muscle progenitor cells isolated from patients with moyamoya disease: Novel experimental cell model. J. Neurosurg., 2014, 120(2), 415-425.
[] [PMID: 24160477]
Mejia-Munne, J.C.; Ellis, J.A.; Feldstein, N.A.; Meyers, P.M.; Connolly, E.S. Moyamoya and inflammation. World Neurosurg., 2017, 100, 575-578.
[] [PMID: 28093343]
Mikami, T.; Suzuki, H.; Komatsu, K.; Mikuni, N. Influence of inflammatory disease on the pathophysiology of moyamoya disease and Quasi-Moyamoya disease. Neurol. Med. Chir. (Tokyo), 2019, 59(10), 361-370.
Weng, L.; Cao, X.; Han, L.; Zhao, H.; Qiu, S.; Yan, Y.; Wang, X.; Chen, X.; Zheng, W.; Xu, X.; Gao, Y.; Chen, Y.; Li, J.; Yang, Y.; Xu, Y. Association of increased Treg and Th17 with pathogenesis of Moyamoya disease., . Sci. Rep., 2017, 7(1), 3071..
[] [PMID: 28596558]
Gao, F.; Yu, L.; Zhang, D.; Zhang, Y.; Wang, R.; Zhao, J. Long noncoding RNAs and their regulatory network: Potential therapeutic targets for adult Moyamoya Disease. World Neurosurg., 2016, 93, 111-119.
[] [PMID: 27268316]
Palomeque-Del-Cerro, L.; Arráez-Aybar, L.A.; Rodríguez-Blanco, C.; Guzmán-García, R.; Menendez-Aparicio, M.; Oliva-Pascual-Vaca, Á. A systematic review of the soft-tissue connections between neck muscles and dura mater: The Myodural Bridge. Spine, 2017, 42(1), 49-54.
[] [PMID: 27116115]
Cheshire, E.C.; Malcomson, R.D.; Rutty, G.N.; James, D.S. Visualisation of the intact dura mater and brain surface in infant autopsies: a minimally destructive technique for the post-mortem assessment of head injury. Int. J. Legal Med., 2015, 129(2), 307-312.
[] [PMID: 25384986]
Lv, X.; Wu, Z.; Li, Y. Innervation of the cerebral dura mater. Neuroradiol. J., 2014, 27(3), 293-298.
[] [PMID: 24976196]
Hoshimaru, M.; Takahashi, J.A.; Kikuchi, H.; Nagata, I.; Hatanaka, M. Possible roles of basic fibroblast growth factor in the pathogenesis of moyamoya disease: an immunohistochemical study. J. Neurosurg., 1991, 75(2), 267-270.
[] [PMID: 2072165]
Sakamoto, S.; Kiura, Y.; Yamasaki, F.; Shibukawa, M.; Ohba, S.; Shrestha, P.; Sugiyama, K.; Kurisu, K. Expression of vascular endothelial growth factor in dura mater of patients with moyamoya disease. Neurosurg. Rev., 2008, 31(1), 77-81.
[] [PMID: 17912564]
Antony, J.; Hacking, C.; Jeffree, R.L. Pachymeningeal enhancement-a comprehensive review of literature. Neurosurg. Rev., 2015, 38(4), 649-659.
[] [PMID: 26264063]
Gadgil, N.; Lam, S.; Pyarali, M.; Paldino, M.; Pan, I.W.; Dauser, R.C. Indirect revascularization with the dural inversion technique for pediatric moyamoya disease: 20-year experience. J. Neurosurg. Pediatr., 2018, 22(5), 541-549.
[] [PMID: 30117790]
Barschke, P.; Oeckl, P.; Steinacker, P.; Ludolph, A.; Otto, M. Proteomic studies in the discovery of cerebrospinal fluid biomarkers for amyotrophic lateral sclerosis. Expert Rev. Proteomics, 2017, 14(9), 769-777.
[] [PMID: 28799854]
Misra, S.; Kumar, A.; Kumar, P.; Yadav, A.K.; Mohania, D.; Pandit, A.K.; Prasad, K.; Vibha, D. Blood-based protein biomarkers for stroke differentiation: A systematic review. Proteomics Clin. Appl., 2017, 11(9-10)
[] [PMID: 28452132]
Pandey, S.P.; Madhukar, P.; Dev, P.; Joshi, D.; Mishra, V.N.; Chaurasia, R.N.; Pathak, A. Blood biomarkers for ischemic stroke subtype differentiation: A systematic review. Cardiovasc. Hematol. Disord. Drug Targets, 2019, 19(3), 215-227.
Robinson, R.A.; Amin, B.; Guest, P.C. Multiplexing biomarker methods, proteomics and considerations for Alzheimer’s disease. Adv. Exp. Med. Biol., 2017, 974, 21-48.
[] [PMID: 28353223]
Zhou, A. Proteomics in stroke research: Potentials of the nascent proteomics. J. Investig. Med., 2016, 64(8), 1236-1240.
[] [PMID: 27430243]
Maestrini, I.; Ducroquet, A.; Moulin, S.; Leys, D.; Cordonnier, C.; Bordet, R. Blood biomarkers in the early stage of cerebral ischemia. Rev. Neurol. (Paris), 2016, 172(3), 198-219.
[] [PMID: 26988891]
Goldenberg, N.A.; Everett, A.D.; Graham, D.; Bernard, T.J.; Nowak-Göttl, U. Proteomic and other mass spectrometry based “omics” biomarker discovery and validation in pediatric venous thromboembolism and arterial ischemic stroke: Current state, unmet needs, and future directions. Proteomics Clin. Appl., 2014, 8(11-12), 828-836.
[] [PMID: 25379629]
Laborde, C.M.; Mourino-Alvarez, L.; Akerstrom, F.; Padial, L.R.; Vivanco, F.; Gil-Dones, F.; Barderas, M.G. Potential blood biomarkers for stroke. Expert Rev. Proteomics, 2012, 9(4), 437-449.
[] [PMID: 22967080]
Araki, Y.; Yoshikawa, K.; Okamoto, S.; Sumitomo, M.; Maruwaka, M.; Wakabayashi, T. Identification of novel biomarker candidates by proteomic analysis of cerebrospinal fluid from patients with moyamoya disease using SELDI-TOF-MS. BMC Neurol., 2010, 10, 112.
[] [PMID: 21059247]
Maruwaka, M.; Yoshikawa, K.; Okamoto, S.; Araki, Y.; Sumitomo, M.; Kawamura, A.; Yokoyama, K.; Wakabayashi, T. Biomarker research for moyamoya disease in cerebrospinal fluid using surface-enhanced laser desorption/ionization time-of-flight mass spectrometry. J. Stroke Cerebrovasc. Dis., 2015, 24(1), 104-111.
[] [PMID: 25440344]
Romeo, M.J.; Espina, V.; Lowenthal, M.; Espina, B.H.; Petricoin, E.F., III; Liotta, L.A. CSF proteome: A protein repository for potential biomarker identification. Expert Rev. Proteomics, 2005, 2(1), 57-70.
[] [PMID: 15966853]
Koh, E.J.; Kim, H.N.; Ma, T.Z.; Choi, H.Y.; Kwak, Y.G. Comparative analysis of serum proteomes of Moyamoya disease and normal controls. J. Korean Neurosurg. Soc., 2010, 48(1), 8-13.
[] [PMID: 20717506]
Smith, E.R. Moyamoya biomarkers. J. Korean Neurosurg. Soc., 2015, 57(6), 415-421.
[] [PMID: 26180608]
Kashiwazaki, D.; Uchino, H.; Kuroda, S. Downregulation of apolipoprotein-E and apolipoprotein-J in Moyamoya Disease-A proteome analysis of cerebrospinal fluid. J. Stroke Cerebrovasc. Dis., 2017, 26(12), 2981-2987.
[] [PMID: 28843803]
Craft, G.E.; Chen, A.; Nairn, A.C. Recent advances in quantitative neuroproteomics. Methods, 2013, 61(3), 186-218.
[] [PMID: 23623823]
Martyniuk, C.J.; Popesku, J.T.; Chown, B.; Denslow, N.D.; Trudeau, V.L. Quantitative proteomics in teleost fish: insights and challenges for neuroendocrine and neurotoxicology research. Gen. Comp. Endocrinol., 2012, 176(3), 314-320.
[] [PMID: 22202605]
Núñez, E.V.; Guest, P.C.; Martins-de-Souza, D.; Domont, G.B.; Nogueira, F.C. Application of iTRAQ shotgun proteomics for measurement of brain proteins in studies of psychiatric disorders. Adv. Exp. Med. Biol., 2017, 974, 219-227.
[] [PMID: 28353239]
Velásquez, E.; Nogueira, F.C.S.; Velásquez, I.; Schmitt, A.; Falkai, P.; Domont, G.B.; Martins-de-Souza, D. Synaptosomal proteome of the orbitofrontal cortex from schizophrenia patients using quantitative label-free and iTRAQ-based shotgun proteomics. J. Proteome Res., 2017, 16(12), 4481-4494.
[] [PMID: 28949146]
Fujimura, M.; Tominaga, T. Diagnosis of Moyamoya disease: international standard and regional differences. Neurol. Med. Chir. (Tokyo), 2015, 55(3), 189-193.
[] [PMID: 25739428]
Zhang, L.; Jia, X.; Feng, Y.; Peng, X.; Zhang, Z.; Zhou, W.; Zhang, Z.; Ma, F.; Liu, X.; Zheng, Y.; Yang, P.; Yuan, Z. Plasma membrane proteome analysis of the early effect of alcohol on liver: implications for alcoholic liver disease. Acta Biochim. Biophys. Sin. (Shanghai), 2011, 43(1), 19-29.
[] [PMID: 21134885]
Shilov, I.V.; Seymour, S.L.; Patel, A.A.; Loboda, A.; Tang, W.H.; Keating, S.P.; Hunter, C.L.; Nuwaysir, L.M.; Schaeffer, D.A. The Paragon algorithm, a next generation search engine that uses sequence temperature values and feature probabilities to identify peptides from tandem mass spectra., . Mol. Cell. Proteomics, 2007, 6(9), 1638-1655..
[] [PMID: 17533153]
Datta, A.; Jingru, Q.; Khor, T.H.; Teo, M.T.; Heese, K.; Sze, S.K. Quantitative neuroproteomics of an in vivo rodent model of focal cerebral ischemia/reperfusion injury reveals a temporal regulation of novel pathophysiological molecular markers. J. Proteome Res., 2011, 10(11), 5199-5213.
[] [PMID: 21950801]
Datta, A.; Park, J.E.; Li, X.; Zhang, H.; Ho, Z.S.; Heese, K.; Lim, S.K.; Tam, J.P.; Sze, S.K. Phenotyping of an in vitro model of ischemic penumbra by iTRAQ-based shotgun quantitative proteomics. J. Proteome Res., 2010, 9(1), 472-484.
[] [PMID: 19916522]
Qiao, J.; Fang, C.Y.; Chen, S.X.; Wang, X.Q.; Cui, S.J.; Liu, X.H.; Jiang, Y.H.; Wang, J.; Zhang, Y.; Yang, P.Y.; Liu, F. Stroma derived COL6A3 is a potential prognosis marker of colorectal carcinoma revealed by quantitative proteomics. Oncotarget, 2015, 6(30), 29929-29946.
[] [PMID: 26338966]
Zhang, L.; Jia, X.; Zhang, X.; Sun, J.; Peng, X.; Qi, T.; Ma, F.; Yin, L.; Yao, Y.; Qiu, C.; Lu, H. Proteomic analysis of PBMCs: characterization of potential HIV-associated proteins. Proteome Sci., 2010, 8, 12.
[] [PMID: 20222986]
MacLean, B.; Tomazela, D.M.; Shulman, N.; Chambers, M.; Finney, G.L.; Frewen, B.; Kern, R.; Tabb, D.L.; Liebler, D.C.; MacCoss, M.J. Skyline: an open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics, 2010, 26(7), 966-968.
[] [PMID: 20147306]
Mehaffy, C.; Dobos, K.M.; Nahid, P.; Kruh-Garcia, N.A. Second generation multiple reaction monitoring assays for enhanced detection of ultra-low abundance Mycobacterium tuberculosis peptides in human serum. Clin. Proteomics, 2017, 14, 21.
[] [PMID: 28592925]
Chou, K.C. Impacts of bioinformatics to medicinal chemistry. Med. Chem., 2015, 11(3), 218-234.
[] [PMID: 25548930]
Behbahani, M.; Mohabatkar, H.; Nosrati, M. Analysis and comparison of lignin peroxidases between fungi and bacteria using three different modes of Chou’s general pseudo amino acid composition. J. Theor. Biol., 2016, 411, 1-5.
[] [PMID: 27615149]
Blanco, F.J.; Camacho-Encina, M.; González-Rodríguez, L.; Rego-Pérez, I.; Mateos, J.; Fernández-Puente, P.; Lourido, L.; Rocha, B.; Picchi, F.; Silva-Díaz, M.T.; Herrero, M.; Martínez, H.; Verges, J.; Ruiz-Romero, C.; Calamia, V. Predictive modeling of therapeutic response to chondroitin sulfate/glucosamine hydrochloride in knee osteoarthritis. Ther. Adv. Chronic Dis., 2019, 102040622319870013
[ ] [PMID: 31489155]
Nambu, M.; Masuda, T.; Ito, S.; Kato, K.; Kojima, T.; Daiko, H.; Ito, Y.; Honda, K.; Ohtsuki, S. Leucine-rich alpha-2-glycoprotein 1 in serum is a possible biomarker to predict response to preoperative chemoradiotherapy for esophageal cancer. Biol. Pharm. Bull., 2019, 42(10), 1766-1771.
[] [PMID: 31582665]
Ma, Y.G.; Zhang, Q.; Yu, L.B.; Zhao, J.Z. Role of ring finger protein 213 in Moyamoya Disease. Chin. Med. J. (Engl.), 2016, 129(20), 2497-2501.
[] [PMID: 27748344]
Liu, W.; Senevirathna, S.T.; Hitomi, T.; Kobayashi, H.; Roder, C.; Herzig, R.; Kraemer, M.; Voormolen, M.H.; Cahová, P.; Krischek, B.; Koizumi, A. Genomewide association study identifies no major founder variant in Caucasian Moyamoya disease. J. Genet., 2013, 92(3), 605-609.
[] [PMID: 24371184]
Bedini, G.; Blecharz, K.G.; Nava, S.; Vajkoczy, P.; Alessandri, G.; Ranieri, M.; Acerbi, F.; Ferroli, P.; Riva, D.; Esposito, S.; Pantaleoni, C.; Nardocci, N.; Zibordi, F.; Ciceri, E.; Parati, E.A.; Bersano, A. Vasculogenic and angiogenic pathways in Moyamoya disease. Curr. Med. Chem., 2016, 23(4), 315-345.
[] [PMID: 26861126]
Bang, O.Y.; Chung, J.W.; Kim, S.J.; Oh, M.J.; Kim, S.Y.; Cho, Y.H.; Cha, J.; Yeon, J.Y.; Kim, K.H.; Kim, G.M.; Chung, C.S.; Lee, K.H.; Ki, C.S.; Jeon, P.; Kim, J.S.; Hong, S.C.; Moon, G.J. Caveolin-1, Ring finger protein 213, and endothelial function in Moyamoya disease. Int. J. Stroke, 2016, 11(9), 999-1008.
[] [PMID: 27462098]
Sung, H.Y.; Lee, J.Y.; Park, A.K.; Moon, Y.J.; Jo, I.; Park, E.M.; Wang, K.C.; Phi, J.H.; Ahn, J.H.; Kim, S.K. Aberrant promoter hypomethylation of sortilin 1: A Moyamoya disease biomarker. J. Stroke, 2018, 20(3), 350-361.
[] [PMID: 30309230]
Hamauchi, S.; Shichinohe, H.; Uchino, H.; Yamaguchi, S.; Nakayama, N.; Kazumata, K.; Osanai, T.; Abumiya, T.; Houkin, K.; Era, T. Cellular functions and gene and protein expression profiles in endothelial cells derived from Moyamoya disease-specific iPS cells. PLoS One, 2016, 11(9)e0163561
[] [PMID: 27662211]
Jia, X.; Chen, J.; Megger, D.A.; Zhang, X.; Kozlowski, M.; Zhang, L.; Fang, Z.; Li, J.; Chu, Q.; Wu, M.; Li, Y.; Sitek, B.; Yuan, Z. Label-free proteomic analysis of exosomes derived from inducible hepatitis B virus-replicating HepAD38 cell line. Mol. Cell. Proteomics, 2017, 16(4)(Suppl. 1), S144-S160.
[] [PMID: 28242843]
Glushakov, A.V.; Arias, R.A.; Tolosano, E.; Doré, S. Age-dependent effects of haptoglobin deletion in neurobehavioral and anatomical outcomes following traumatic brain injury. Front. Mol. Biosci., 2016, 3, 34.
[] [PMID: 27486583]
Yee, J.Y.; Nurjono, M.; Ng, W.Y.; Teo, S.R.; Lee, T.S.; Lee, J. Peripheral blood gene expression of acute phase proteins in people with first episode psychosis. Brain Behav. Immun., 2017, 65, 337-341.
[] [PMID: 28627459]
Przybycien-Szymanska, M.M.; Yang, Y.; Ashley, W.W. Microparticle derived proteins as potential biomarkers for cerebral vasospasm post subarachnoid hemorrhage. A preliminary study. Clin. Neurol. Neurosurg., 2016, 141, 48-55.
[] [PMID: 26736019]

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