Generic placeholder image

Combinatorial Chemistry & High Throughput Screening

Editor-in-Chief

ISSN (Print): 1386-2073
ISSN (Online): 1875-5402

Research Article

Identification of Differentially Expressed Proteins in Rats with Early Subacute Spinal Cord Injury using an iTRAQ-based Quantitative Analysis

Author(s): Yongfu Lou, Yigang Lv, Zhen Li, Yi Kang, Mengfan Hou, Zheng Fu, Lu Lu, Lu Liu, Zhiwei Cai, Zhangyang Qi, Huan Jian, Wenyuan Shen, Xueying Li*, Hengxing Zhou* and Shiqing Feng*

Volume 26, Issue 11, 2023

Published on: 15 February, 2023

Page: [1960 - 1973] Pages: 14

DOI: 10.2174/1386207326666230113152622

Price: $65

Open Access Journals Promotions 2
Abstract

Background: Injuries to the central nervous system (CNS), such as spinal cord injury (SCI), may devastate families and society. Subacute SCI may majorly impact secondary damage during the transitional period between the acute and subacute phases. A range of CNS illnesses has been linked to changes in the level of protein expression. However, the importance of proteins during the early subacute stage of SCI remains unknown. The role of proteins in the early subacute phase of SCI has not been established yet.

Methods: SCI-induced damage in rats was studied using isobaric tagging for relative and absolute protein quantification (iTRAQ) to identify proteins that differed in expression 3 days after the injury, as well as proteins that did not alter in expression. Differentially expressed proteins (DEPs) were analyzed employing Gene Ontology (GO) enrichment and Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis to discover the biological processes, cell components, and molecular functions of the proteins. We also performed Gene Set Enrichment Analysis (GSEA) software BP pathway and KEGG analysis on all proteins to further identify their functions. In addition, the first 15 key nodes of a protein-protein interaction (PPI) system were found.

Results: During the early subacute stage of SCI, we identified 176 DEPs in total between the control and damage groups, with 114 (64.77%) being up-regulated and 62 (35.23%) being downregulated. As a result of this study, we discovered the most important cellular components and molecular activities, as well as biological processes and pathways, in the early subacute phase of SCI. The top 15 high-degree core nodes were Alb, Plg, F2, Serpina1, Fgg, Apoa1, Vim, Hpx, Apoe, Agt, Ambp, Pcna, Gc, F12, and Gfap.

Conclusion: Our study could provide new views on regulating the pathogenesis of proteins in the early subacute phase after SCI, which provides a theoretical basis for exploring more effective therapeutic targets for SCI in the future.

Keywords: Spinal cord injury, early subacute phase, isobaric tagging for relative and absolute protein quantification, differentially expressed proteins, nervous system, differentially expressed proteins.

Graphical Abstract
[1]
James, S.L.; Theadom, A.; Ellenbogen, R.G.; Bannick, M.S.; Montjoy-Venning, W.; Lucchesi, L.R.; Abbasi, N.; Abdulkader, R.; Abraha, H.N.; Adsuar, J.C.; Afarideh, M.; Agrawal, S.; Ahmadi, A.; Ahmed, M.B.; Aichour, A.N.; Aichour, I.; Aichour, M.T.E.; Akinyemi, R.O.; Akseer, N.; Alahdab, F.; Alebel, A.; Alghnam, S.A.; Ali, B.A.; Alsharif, U.; Altirkawi, K.; Andrei, C.L.; Anjomshoa, M.; Ansari, H.; Ansha, M.G.; Antonio, C.A.T.; Appiah, S.C.Y.; Ariani, F.; Asefa, N.G.; Asgedom, S.W.; Atique, S.; Awasthi, A.; Ayala Quintanilla, B.P.; Ayuk, T.B.; Azzopardi, P.S.; Badali, H.; Badawi, A.; Balalla, S.; Banstola, A.; Barker-Collo, S.L.; Bärnighausen, T.W.; Bedi, N.; Behzadifar, M.; Behzadifar, M.; Bekele, B.B.; Belachew, A.B.; Belay, Y.A.; Bennett, D.A.; Bensenor, I.M.; Berhane, A.; Beuran, M.; Bhalla, A.; Bhaumik, S.; Bhutta, Z.A.; Biadgo, B.; Biffino, M.; Bijani, A.; Bililign, N.; Birungi, C.; Boufous, S.; Brazinova, A.; Brown, A.W.; Car, M.; Cárdenas, R.; Carrero, J.J.; Carvalho, F.; Castañeda-Orjuela, C.A.; Catalá-López, F.; Chaiah, Y.; Champs, A.P.; Chang, J-C.; Choi, J-Y.J.; Christopher, D.J.; Cooper, C.; Crowe, C.S.; Dandona, L.; Dandona, R.; Daryani, A.; Davitoiu, D.V.; Degefa, M.G.; Demoz, G.T.; Deribe, K.; Djalalinia, S.; Do, H.P.; Doku, D.T.; Drake, T.M.; Dubey, M.; Dubljanin, E.; El-Khatib, Z.; Ofori-Asenso, R.; Eskandarieh, S.; Esteghamati, A.; Esteghamati, S.; Faro, A.; Farzadfar, F.; Farzaei, M.H.; Fereshtehnejad, S-M.; Fernandes, E.; Feyissa, G.T.; Filip, I.; Fischer, F.; Fukumoto, T.; Ganji, M.; Gankpe, F.G.; Gebre, A.K.; Gebrehiwot, T.T.; Gezae, K.E.; Gopalkrishna, G.; Goulart, A.C.; Haagsma, J.A.; Haj-Mirzaian, A.; Haj-Mirzaian, A.; Hamadeh, R.R.; Hamidi, S.; Haro, J.M.; Hassankhani, H.; Hassen, H.Y.; Havmoeller, R.; Hawley, C.; Hay, S.I.; Hegazy, M.I.; Hendrie, D.; Henok, A.; Hibstu, D.T.; Hoffman, H.J.; Hole, M.K.; Homaie Rad, E.; Hosseini, S.M.; Hostiuc, S.; Hu, G.; Hussen, M.A.; Ilesanmi, O.S.; Irvani, S.S.N.; Jakovljevic, M.; Jayaraman, S.; Jha, R.P.; Jonas, J.B.; Jones, K.M.; Jorjoran Shushtari, Z.; Jozwiak, J.J.; Jürisson, M.; Kabir, A.; Kahsay, A.; Kahssay, M.; Kalani, R.; Karch, A.; Kasaeian, A.; Kassa, G.M.; Kassa, T.D.; Kassa, Z.Y.; Kengne, A.P.; Khader, Y.S.; Khafaie, M.A.; Khalid, N.; Khalil, I.; Khan, E.A.; Khan, M.S.; Khang, Y-H.; Khazaie, H.; Khoja, A.T.; Khubchandani, J.; Kiadaliri, A.A.; Kim, D.; Kim, Y-E.; Kisa, A.; Koyanagi, A.; Krohn, K.J.; Kuate, Defo B.; Kucuk Bicer, B.; Kumar, G.A.; Kumar, M.; Lalloo, R.; Lami, F.H.; Lansingh, V.C.; Laryea, D.O.; Latifi, A.; Leshargie, C.T.; Levi, M.; Li, S.; Liben, M.L.; Lotufo, P.A.; Lunevicius, R.; Mahotra, N.B.; Majdan, M.; Majeed, A.; Malekzadeh, R.; Manda, A-L.; Mansournia, M.A.; Massenburg, B.B.; Mate, K.K.V.; Mehndiratta, M.M.; Mehta, V.; Meles, H.; Melese, A.; Memiah, P.T.N.; Mendoza, W.; Mengistu, G.; Meretoja, A.; Meretoja, T.J.; Mestrovic, T.; Miazgowski, T.; Miller, T.R.; Mini, G.K.; Mirica, A.; Mirrakhimov, E.M.; Moazen, B.; Mohammadi, M.; Mohammed, S.; Mokdad, A.H.; Molokhia, M.; Monasta, L.; Mondello, S.; Moosazadeh, M.; Moradi, G.; Moradi, M.; Moradi-Lakeh, M.; Moradinazar, M.; Morrison, S.D.; Moschos, M.M.; Mousavi, S.M.; Murthy, S.; Musa, K.I.; Mustafa, G.; Naghavi, M.; Naik, G.; Najafi, F.; Nangia, V.; Nascimento, B.R.; Negoi, I.; Nguyen, T.H.; Nichols, E.; Ningrum, D.N.A.; Nirayo, Y.L.; Nyasulu, P.S.; Ogbo, F.A.; Oh, I-H.; Okoro, A.; Olagunju, A.T.; Olagunju, T.O.; Olivares, P.R.; Otstavnov, S.S.; Owolabi, M.O.; P A, M.; Pakhale, S.; Pandey, A.R.; Pesudovs, K.; Pinilla-Monsalve, G.D.; Polinder, S.; Poustchi, H.; Prakash, S.; Qorbani, M.; Radfar, A.; Rafay, A.; Rafiei, A.; Rahimi-Movaghar, A.; Rahimi-Movaghar, V.; Rahman, M.; Rahman, M.A.; Rai, R.K.; Rajati, F.; Ram, U.; Rawaf, D.L.; Rawaf, S.; Reiner, R.C.; Reis, C.; Renzaho, A.M.N.; Resnikoff, S.; Rezaei, S.; Rezaeian, S.; Roever, L.; Ronfani, L.; Roshandel, G.; Roy, N.; Ruhago, G.M.; Saddik, B.; Safari, H.; Safiri, S.; Sahraian, M.A.; Salamati, P.; Saldanha, R.F.; Samy, A.M.; Sanabria, J.; Santos, J.V.; Santric Milicevic, M.M.M.; Sartorius, B.; Satpathy, M.; Savuon, K.; Schneider, I.J.C.; Schwebel, D.C.; Sepanlou, S.G.; Shabaninejad, H.; Shaikh, M.A.A.; Shams-Beyranvand, M.; Sharif, M.; Sharif-Alhoseini, M.; Shariful Islam, S.M.; She, J.; Sheikh, A.; Shen, J.; Sheth, K.N.; Shibuya, K.; Shiferaw, M.S.; Shigematsu, M.; Shiri, R.; Shiue, I.; Shoman, H.; Siabani, S.; Siddiqi, T.J.; Silva, J.P.; Silveira, D.G.A.; Sinha, D.N.; Smith, M.; Soares Filho, A.M.; Sobhani, S.; Soofi, M.; Soriano, J.B.; Soyiri, I.N.; Stein, D.J.; Stokes, M.A.; Sufiyan, M.B.; Sunguya, B.F.; Sunshine, J.E.; Sykes, B.L.; Szoeke, C.E.I.; Tabarés-Seisdedos, R.; Te Ao, B.J.; Tehrani-Banihashemi, A.; Tekle, M.G.; Temsah, M-H.; Temsah, O.; Topor-Madry, R.; Tortajada-Girbés, M.; Tran, B.X.; Tran, K.B.; Tudor Car, L.; Ukwaja, K.N.; Ullah, I.; Usman, M.S.; Uthman, O.A.; Valdez, P.R.; Vasankari, T.J.; Venketasubramanian, N.; Violante, F.S.; Wagnew, F.W.S.; Waheed, Y.; Wang, Y-P.; Weldegwergs, K.G.; Werdecker, A.; Wijeratne, T.; Winkler, A.S.; Wyper, G.M.A.; Yano, Y.; Yaseri, M.; Yasin, Y.J.; Ye, P.; Yimer, E.M.; Yip, P.; Yisma, E.; Yonemoto, N.; Yoon, S-J.; Yost, M.G.; Younis, M.Z.; Yousefifard, M.; Yu, C.; Zaidi, Z.; Zaman, S.B.; Zamani, M.; Zenebe, Z.M.; Zodpey, S.; Feigin, V.L.; Vos, T.; Murray, C.J.L. Global, regional, and national burden of traumatic brain injury and spinal cord injury, 1990–2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet Neurol., 2019, 18(1), 56-87.
[http://dx.doi.org/10.1016/S1474-4422(18)30415-0] [PMID: 30497965]
[2]
Jain, N.B.; Ayers, G.D.; Peterson, E.N.; Harris, M.B.; Morse, L.; O’Connor, K.C.; Garshick, E. Traumatic spinal cord injury in the United States, 1993-2012. JAMA, 2015, 313(22), 2236-2243.
[http://dx.doi.org/10.1001/jama.2015.6250] [PMID: 26057284]
[3]
Ahuja, C.S.; Wilson, J.R.; Nori, S.; Kotter, M.R.N.; Druschel, C.; Curt, A.; Fehlings, M.G. Traumatic spinal cord injury. Nat. Rev. Dis. Primers, 2017, 3(1), 17018.
[http://dx.doi.org/10.1038/nrdp.2017.18] [PMID: 28447605]
[4]
Silva, N.A.; Sousa, N.; Reis, R.L.; Salgado, A.J. From basics to clinical: A comprehensive review on spinal cord injury. Prog. Neurobiol., 2014, 114, 25-57.
[http://dx.doi.org/10.1016/j.pneurobio.2013.11.002] [PMID: 24269804]
[5]
Huang, H.; Mao, G.; Chen, L.; Liu, A. Progress and challenges with clinical cell therapy in neurorestoratology. J. Neurorestoratol., 2015, 3, 91-95.
[http://dx.doi.org/10.2147/JN.S74140]
[6]
Rowland, J.W.; Hawryluk, G.W.J.; Kwon, B.; Fehlings, M.G. Current status of acute spinal cord injury pathophysiology and emerging therapies: promise on the horizon. Neurosurg. Focus, 2008, 25(5), E2.
[http://dx.doi.org/10.3171/FOC.2008.25.11.E2] [PMID: 18980476]
[7]
Assinck, P.; Duncan, G.J.; Hilton, B.J.; Plemel, J.R.; Tetzlaff, W. Cell transplantation therapy for spinal cord injury. Nat. Neurosci., 2017, 20(5), 637-647.
[http://dx.doi.org/10.1038/nn.4541] [PMID: 28440805]
[8]
Mordillo-Mateos, L.; Sánchez-Ramos, A.; Coperchini, F.; Bustos-Guadamillas, I.; Alonso-Bonilla, C.; Vargas-Baquero, E.; Rodriguez-Carrión, I.; Rotondi, M.; Oliviero, A. Development of chronic pain in males with traumatic spinal cord injury: role of circulating levels of the chemokines CCL2 and CXCL10 in subacute stage. Spinal Cord, 2019, 57(11), 953-959.
[http://dx.doi.org/10.1038/s41393-019-0311-3] [PMID: 31182785]
[9]
Zhou, H.; Kang, Y.; Shi, Z.; Lu, L.; Li, X.; Chu, T.; Liu, J.; Liu, L.; Lou, Y.; Zhang, C.; Ning, G.; Feng, S.; Kong, X. Identification of differentially expressed proteins in rats with spinal cord injury during the transitional phase using an iTRAQ-based quantitative analysis. Gene, 2018, 677, 66-76.
[http://dx.doi.org/10.1016/j.gene.2018.07.050] [PMID: 30036659]
[10]
Huang, H.; Chen, L.; Mao, G.; Sharma, H.S. Clinical neurorestorative cell therapies: Developmental process, current state and future prospective. J. Neurorestoratol., 2020, 8(2), 61-82.
[http://dx.doi.org/10.26599/JNR.2020.9040009]
[11]
Chen, C.; Chen, Q.; Liu, Y.; Zhang, C.; Zhu, K.; Li, X.; Xie, H.; Zhang, R. The cell repair research for Parkinson’s disease: A systematic review. J. Neurorestoratol., 2020, 8(2), 93-103.
[http://dx.doi.org/10.26599/JNR.2020.9040011]
[12]
Dybas, J.M.; O’Leary, C.E.; Ding, H.; Spruce, L.A.; Seeholzer, S.H.; Oliver, P.M. Integrative proteomics reveals an increase in non-degradative ubiquitylation in activated CD4+ T cells. Nat. Immunol., 2019, 20(6), 747-755.
[http://dx.doi.org/10.1038/s41590-019-0381-6] [PMID: 31061531]
[13]
Wiese, S.; Reidegeld, K.A.; Meyer, H.E.; Warscheid, B. Protein labeling by iTRAQ: A new tool for quantitative mass spectrometry in proteome research. Proteomics, 2007, 7(3), 340-350.
[http://dx.doi.org/10.1002/pmic.200600422] [PMID: 17177251]
[14]
Vasunilashorn, S.M.; Ngo, L.H.; Chan, N.Y.; Zhou, W.; Dillon, S.T.; Otu, H.H.; Inouye, S.K.; Wyrobnik, I.; Kuchel, G.A.; McElhaney, J.E.; Xie, Z.; Alsop, D.C.; Jones, R.N.; Libermann, T.A.; Marcantonio, E.R. Development of a dynamic multi-protein signature of postoperative delirium. J. Gerontol. A Biol. Sci. Med. Sci., 2019, 74(2), 261-268.
[http://dx.doi.org/10.1093/gerona/gly036] [PMID: 29529166]
[15]
Craft, G.E.; Chen, A.; Nairn, A.C. Recent advances in quantitative neuroproteomics. Methods, 2013, 61(3), 186-218.
[http://dx.doi.org/10.1016/j.ymeth.2013.04.008] [PMID: 23623823]
[16]
Ban, D.X.; Kong, X.H.; Feng, S.Q.; Ning, G.Z.; Chen, J.T.; Guo, S.F. Intraspinal cord graft of autologous activated Schwann cells efficiently promotes axonal regeneration and functional recovery after rat’s spinal cord injury. Brain Res., 2009, 1256, 149-161.
[http://dx.doi.org/10.1016/j.brainres.2008.11.098] [PMID: 19103176]
[17]
Ashburner, M.; Ball, C.A.; Blake, J.A.; Botstein, D.; Butler, H.; Cherry, J.M.; Davis, A.P.; Dolinski, K.; Dwight, S.S.; Eppig, J.T.; Harris, M.A.; Hill, D.P.; Issel-Tarver, L.; Kasarskis, A.; Lewis, S.; Matese, J.C.; Richardson, J.E.; Ringwald, M.; Rubin, G.M.; Sherlock, G. Gene ontology: tool for the unification of biology. Nat. Genet., 2000, 25(1), 25-29.
[http://dx.doi.org/10.1038/75556] [PMID: 10802651]
[18]
Kanehisa, M.; Goto, S. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res., 2000, 28(1), 27-30.
[http://dx.doi.org/10.1093/nar/28.1.27] [PMID: 10592173]
[19]
Franceschini, A.; Szklarczyk, D.; Frankild, S.; Kuhn, M.; Simonovic, M.; Roth, A.; Lin, J.; Minguez, P.; Bork, P.; von Mering, C.; Jensen, L.J. STRING v9.1: protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res., 2013, 41(Database issue), D808-D815.
[PMID: 23203871]
[20]
Ning, G.Z.; Wu, Q.; Li, Y.L.; Feng, S.Q. Epidemiology of traumatic spinal cord injury in Asia: A systematic review. J. Spinal Cord Med., 2012, 35(4), 229-239.
[http://dx.doi.org/10.1179/2045772312Y.0000000021] [PMID: 22925749]
[21]
Young, W.; AlZoubi, Z.M.; Saberi, H.; Sharma, A.; Muresanu, D.; Feng, S.; Chen, L.; Huang, H. Beijing Declaration of International Association of Neurorestoratology. J. Neurorestoratol., 2015, 3, 121-122.
[22]
Noristani, H.N.; Perrin, F.E. Astrocyte-to-neuron conversion induced by spinal cord injury. Oncotarget, 2016, 7(51), 83831-83832.
[http://dx.doi.org/10.18632/oncotarget.13780] [PMID: 27926495]
[23]
Bareyre, F.M.; Schwab, M.E. Inflammation, degeneration and regeneration in the injured spinal cord: insights from DNA microarrays. Trends Neurosci., 2003, 26(10), 555-563.
[http://dx.doi.org/10.1016/j.tins.2003.08.004] [PMID: 14522149]
[24]
Klusman, I.; Schwab, M.E. Effects of pro-inflammatory cytokines in experimental spinal cord injury. Brain Res., 1997, 762(1-2), 173-184.
[http://dx.doi.org/10.1016/S0006-8993(97)00381-8] [PMID: 9262171]
[25]
Stys, P.K. Anoxic and ischemic injury of myelinated axons in CNS white matter: from mechanistic concepts to therapeutics. J. Cereb. Blood Flow Metab., 1998, 18(1), 2-25.
[http://dx.doi.org/10.1097/00004647-199801000-00002] [PMID: 9428302]
[26]
Anderson, A.J.; Robert, S.; Huang, W.; Young, W.; Cotman, C.W. Activation of complement pathways after contusion-induced spinal cord injury. J. Neurotrauma, 2004, 21(12), 1831-1846.
[http://dx.doi.org/10.1089/neu.2004.21.1831] [PMID: 15684772]
[27]
Reynolds, D.N.; Smith, S.A.; Zhang, Y.P.; Mengsheng, Q.; Lahiri, D.K.; Morassutti, D.J.; Shields, C.B.; Kotwal, G.J. Vaccinia virus complement control protein reduces inflammation and improves spinal cord integrity following spinal cord injury. Ann. N. Y. Acad. Sci., 2004, 1035(1), 165-178.
[http://dx.doi.org/10.1196/annals.1332.011] [PMID: 15681807]
[28]
Beck, K.D.; Nguyen, H.X.; Galvan, M.D.; Salazar, D.L.; Woodruff, T.M.; Anderson, A.J. Quantitative analysis of cellular inflammation after traumatic spinal cord injury: evidence for a multiphasic inflammatory response in the acute to chronic environment. Brain, 2010, 133(2), 433-447.
[http://dx.doi.org/10.1093/brain/awp322] [PMID: 20085927]
[29]
Um, J.W.; Kaufman, A.C.; Kostylev, M.; Heiss, J.K.; Stagi, M.; Takahashi, H.; Kerrisk, M.E.; Vortmeyer, A.; Wisniewski, T.; Koleske, A.J.; Gunther, E.C.; Nygaard, H.B.; Strittmatter, S.M. Metabotropic glutamate receptor 5 is a coreceptor for Alzheimer aβ oligomer bound to cellular prion protein. Neuron, 2013, 79(5), 887-902.
[http://dx.doi.org/10.1016/j.neuron.2013.06.036] [PMID: 24012003]
[30]
Kerrisk, M.E.; Cingolani, L.A.; Koleske, A.J. ECM receptors in neuronal structure, synaptic plasticity, and behavior. Prog. Brain Res., 2014, 214, 101-131.
[http://dx.doi.org/10.1016/B978-0-444-63486-3.00005-0] [PMID: 25410355]
[31]
Prajapati, K.D.; Sharma, S.S.; Roy, N. Current perspectives on potential role of albumin in neuroprotection. revneuro, 2011, 22(3), 355-363.
[http://dx.doi.org/10.1515/rns.2011.028] [PMID: 21591907]
[32]
Avila-Martin, G.; Galan-Arriero, I.; Gómez-Soriano, J.; Taylor, J. Treatment of rat spinal cord injury with the neurotrophic factor albumin-oleic acid: translational application for paralysis, spasticity and pain. PLoS One, 2011, 6(10), e26107.
[http://dx.doi.org/10.1371/journal.pone.0026107] [PMID: 22046257]
[33]
Ho-Tin-Noé, B.; Enslen, H.; Doeuvre, L.; Corsi, J.M.; Lijnen, H.R.; Anglés-Cano, E. Role of plasminogen activation in neuronal organization and survival. Mol. Cell. Neurosci., 2009, 42(4), 288-295.
[http://dx.doi.org/10.1016/j.mcn.2009.08.001] [PMID: 19683575]
[34]
Shigyo, M.; Tohda, C. Extracellular vimentin is a novel axonal growth facilitator for functional recovery in spinal cord-injured mice. Sci. Rep., 2016, 6(1), 28293.
[http://dx.doi.org/10.1038/srep28293] [PMID: 27323867]
[35]
Seitz, A.; Kragol, M.; Aglow, E.; Showe, L.; Heber-Katz, E. Apolipoprotein E expression after spinal cord injury in the mouse. J. Neurosci. Res., 2003, 71(3), 417-426.
[http://dx.doi.org/10.1002/jnr.10482] [PMID: 12526030]
[36]
Ghura, S.; Tai, L.; Zhao, M.; Collins, N.; Che, C.T.; Warpeha, K.M.; LaDu, M.J. Arabidopsis thaliana extracts optimized for polyphenols production as potential therapeutics for the APOE-modulated neuroinflammation characteristic of Alzheimer’s disease in vitro. Sci. Rep., 2016, 6(1), 29364.
[http://dx.doi.org/10.1038/srep29364] [PMID: 27383500]
[37]
Hoe, H.S.; Harris, D.C.; Rebeck, G.W. Multiple pathways of apolipoprotein E signaling in primary neurons. J. Neurochem., 2005, 93(1), 145-155.
[http://dx.doi.org/10.1111/j.1471-4159.2004.03007.x] [PMID: 15773914]
[38]
Wang, K.K.; Yang, Z.; Sarkis, G.; Torres, I.; Raghavan, V. Ubiquitin C-terminal hydrolase-L1 (UCH-L1) as a therapeutic and diagnostic target in neurodegeneration, neurotrauma and neuro-injuries. Expert Opin. Ther. Targets, 2017, 21(6), 627-638.
[http://dx.doi.org/10.1080/14728222.2017.1321635] [PMID: 28434268]
[39]
Kwon, B.K.; Elizei, S.S. The translational importance of establishing biomarkers of human spinal cord injury. Neural Regen. Res., 2017, 12(3), 385-388.
[http://dx.doi.org/10.4103/1673-5374.202933] [PMID: 28469645]
[40]
Hara, M.; Kobayakawa, K.; Ohkawa, Y.; Kumamaru, H.; Yokota, K.; Saito, T.; Kijima, K.; Yoshizaki, S.; Harimaya, K.; Nakashima, Y.; Okada, S. Interaction of reactive astrocytes with type I collagen induces astrocytic scar formation through the integrin–N-cadherin pathway after spinal cord injury. Nat. Med., 2017, 23(7), 818-828.
[http://dx.doi.org/10.1038/nm.4354] [PMID: 28628111]

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