Role of inflammation in neurological damage and regeneration following spinal cord injury and its therapeutic implications
- Burns & Trauma Vol. 11, Issue 1, (2023)
- 作者机构：
1. Key Laboratory of Neuroregeneration of Jiangsu and the Ministry of Education, Co-innovation Center of Neuroregeneration, NMPA Key Laboratory for Research and Evaluation of Tissue Engineering Technology Products，Nantong University
2. School of Life Sciences, Nantong University
3. School of Medicine, Nantong University
4. NICM Health Research Institute, Western Sydney University
5. Key Laboratory for Stem Cells and Tissue Engineering (Sun Yat-sen University), Ministry of Education
6. innovation Center of Neuroregeneration, Nantong University,Co
- 作者简介：
- 基金信息：
DOI：10.1093/burnst/tkac054
CLC：Published：2023，
Published Online：28 February 2023，
扫 描 看 全 文
Yan Jin, Yixing Song, Jiaqi Lin, Tianqing Liu, Guicai Li, Biqin Lai, Yun Gu, Gang Chen, Lingyan Xing, Role of inflammation in neurological damage and regeneration following spinal cord injury and its therapeutic implications, Burns & Trauma, Volume 11, 2023, tkac054, https://doi.org/10.1093/burnst/tkac054
Yan Jin, Yixing Song, Jiaqi Lin, Tianqing Liu, Guicai Li, Biqin Lai, Yun Gu, Gang Chen, Lingyan Xing, Role of inflammation in neurological damage and regeneration following spinal cord injury and its therapeutic implications, Burns & Trauma, Volume 11, 2023, tkac054, https://doi.org/10.1093/burnst/tkac054 DOI：
摘要
Abstract
Spinal cord injury (SCI) is an incurable trauma that frequently results in partial or complete loss of motor and sensory function. Massive neurons are damaged after the initial mechanical insult. Secondary injuries
which are triggered by immunological and inflammatory responses
also result in neuronal loss and axon retraction. This results in defects in the neural circuit and a deficiency in the processing of information. Although inflammatory responses are necessary for spinal cord recovery
conflicting evidence of their contributions to specific biological processes have made it difficult to define the specific role of inflammation in SCI. This review summarizes our understanding of the complex role of inflammation in neural circuit events following SCI
such as cell death
axon regeneration and neural remodeling. We also review the drugs that regulate immune responses and inflammation in the treatment of SCI and discuss the roles of these drugs in the modulation of neural circuits. Finally
we provide evidence about the critical role of inflammation in facilitating spinal cord neural circuit regeneration in zebrafish
an animal model with robust regenerative capacity
to provide insights into the regeneration of the mammalian central nervous system.
关键词
Keywords
InflammationImmune responseSpinal cord injuryAxon regenerationCell deathZebrafishInflammatory drugsTraumaNeurological damage
references
1.Bracken MB, Shepard MJ, Collins WF, Holford TR, Young W, Baskin DS, et al. A randomized, controlled trial of methylprednisolone or naloxone in the treatment of acute spinal-cord injury. Results of the second national acute spinal cord injury study. N Engl J Med. 1990;322:1405–11.
2.Afshary K, Chamanara M, Talari B, Rezaei P, Nassireslami E. Therapeutic effects of minocycline pretreatment in the locomotor and sensory complications of spinal cord injury in an animal model. J Mol Neurosci. 2020;70:1064–72.
3.Stirling DP, Cummins K, Mishra M, Teo W, Yong VW, Stys P. Toll-like receptor 2-mediated alternative activation of microglia is protective after spinal cord injury. Brain. 2014;137:707–23.
4.El-Daher F, Becker CG. Neural circuit reorganisation after spinal cord injury in zebrafish. Curr Opin Genet Dev. 2020;64:44–51.
5.Ahuja CS, Wilson JR, Nori S, Kotter MRN, Druschel C, Curt A, et al. Traumatic spinal cord injury. Nat Rev Dis Primers. 2017;3:17018.
6.Alizadeh A, Dyck SM, Karimi-Abdolrezaee S. Traumatic spinal cord injury: an overview of pathophysiology, models and acute injury mechanisms. Front Neurol. 2019;10:282.
7.Anjum A, Yazid MD, Fauzi Daud M, Idris J, Ng AMH, Selvi Naicker A, et al. Spinal cord injury: pathophysiology, multimolecular interactions, and underlying recovery mechanisms. Int J Mol Sci. 2020;21:7533.
8.Li JJ, Liu H, Zhu Y, Yan L, Liu R, Wang G, et al. Animal models for treating spinal cord injury using biomaterials-based tissue engineering strategies. Tissue Eng Part B Rev. 2022;28:79–100.
9.Pinchi E, Frati A, Cantatore S, D'errico S, Russa R, Maiese A, et al. Acute spinal cord injury: a systematic review investigating mirna families involved. Int J Mol Sci. 2019;20:1841.
10.Zhang Y, Yang S, Liu C, Han X, Gu X, Zhou S. Deciphering glial scar after spinal cord injury. Burns. Trauma. 2021;9:tkab035.
11.Hellenbrand DJ, Quinn CM, Piper ZJ, Morehouse CN, Fixel JA, Hanna AS. Inflammation after spinal cord injury: a review of the critical timeline of signaling cues and cellular infiltration. J Neuroinflammation. 2021;18:284.
12.Vande Walle L, Lamkanfi M. Pyroptosis. Curr Biol. 2016;26:R568–r72.
13.Al Mamun A, Wu Y, Monalisa I, Jia C, Zhou K, Munir F, et al. Role of pyroptosis in spinal cord injury and its therapeutic implications. J Adv Res. 2021;28:97–109.
14.Wallach D, Kovalenko A. Keeping inflammation at bay. elife. 2014;3:e02583.
15.Szondy Z, Sarang Z, Kiss B, Garabuczi É, Köröskényi K. Anti-inflammatory mechanisms triggered by apoptotic cells during their clearance. Front Immunol. 2017;8:909.
16.Xu J, Kim GM, Chen S, Yan P, Ahmed SH, Ku G, et al. Inos and nitrotyrosine expression after spinal cord injury. J Neurotrauma. 2001;18:523–32.
17.Hausmann ON. Post-traumatic inflammation following spinal cord injury. Spinal Cord. 2003;41:369–78.
18.Yu WR, Fehlings MG. Fas/FasL-mediated apoptosis and inflammation are key features of acute human spinal cord injury: implications for translational, clinical application. Acta Neuropathol. 2011;122:747–61.
19.Ackery A, Robins S, Fehlings MG. Inhibition of Fas-mediated apoptosis through administration of soluble Fas receptor improves functional outcome and reduces posttraumatic axonal degeneration after acute spinal cord injury. J Neurotrauma. 2006;23:604–16.
20.Zhang HW, Ding JD, Zhang ZS, Zhao SS, Duan KY, Zhu BQ, et al. Critical role of p38 in spinal cord injury by regulating inflammation and apoptosis in a rat model. Spine(Phila Pa 1976. 2020;45:E355–e63.
21.Wang C, Zhang L, Ndong JC, Hettinghouse A, Sun G, Chen C, et al. Progranulin deficiency exacerbates spinal cord injury by promoting neuroinflammation and cell apoptosis in mice. J Neuroinflammation. 2019;16:238.
22.Zhang T, Wang F, Li K, Lv C, Gao K, Lv C. Therapeutic effect of metformin on inflammation and apoptosis after spinal cord injury in rats through the Wnt/β-catenin signaling pathway. Neurosci Lett. 2020;739:135440.
23.Holler N, Zaru R, Micheau O, Thome M, Attinger A, Valitutti S, et al. Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nat Immunol. 2000;1:489–95.
24.Liu S, Li Y, Choi HMC, Sarkar C, Koh EY, Wu J, et al. Lysosomal damage after spinal cord injury causes accumulation of RIPK1 and RIPK3 proteins and potentiation of necroptosis. Cell Death Dis. 2018;9:476.
25.Kanno H, Ozawa H, Handa K, Murakami T, Itoi E. Changes in expression of receptor-interacting protein kinase 1 in secondary neural tissue damage following spinal cord injury. Neurosci Insights. 2020;15:2633105520906402.
26.Jiao J, Wang Y, Ren P, Sun S, Wu M. Necrosulfonamide ameliorates neurological impairment in spinal cord injury by improving antioxidative capacity. Front Pharmacol. 2019;10:1538.
27.Fan H, Tang HB, Kang J, Shan L, Song H, Zhu K, et al. Involvement of endoplasmic reticulum stress in the necroptosis of microglia/macrophages after spinal cord injury. Neuroscience. 2015;311:362–73.
28.Fan H, Zhang K, Shan L, Kuang F, Chen K, Zhu K, et al. Reactive astrocytes undergo m1 microglia/macrohpages-induced necroptosis in spinal cord injury. Mol Neurodegener. 2016;11:14.
29.Shao L, Liu X, Zhu S, Liu C, Gao Y, Xu X. The role of Smurf1 in neuronal necroptosis after lipopolysaccharide-induced neuroinflammation. Cell Mol Neurobiol. 2018;38:809–16.
30.Liu M, Wu W, Li H, Li S, Huang LT, Yang YQ, et al. Necroptosis, a novel type of programmed cell death, contributes to early neural cells damage after spinal cord injury in adult mice. J Spinal Cord Med. 2015;38:745–53.
31.Greenhalgh AD, David S. Differences in the phagocytic response of microglia and peripheral macrophages after spinal cord injury and its effects on cell death. J Neurosci. 2014;34:6316–22.
32.Horn KP, Busch SA, Hawthorne AL, Van Rooijen N, Silver J. Another barrier to regeneration in the cns: activated macrophages induce extensive retraction of dystrophic axons through direct physical interactions. J Neurosci. 2008;28:9330–41.
33.Evans TA, Barkauskas DS, Myers JT, Hare EG, You JQ, Ransohoff RM, et al. High-resolution intravital imaging reveals that blood-derived macrophages but not resident microglia facilitate secondary axonal dieback in traumatic spinal cord injury. Exp Neurol. 2014;254:109–20.
34.Tran AP, Warren PM, Silver J. The biology of regeneration failure and success after spinal cord injury. Physiol Rev. 2018;98:881–917.
35.Freria CM, Hall JC, Wei P, Guan Z, Mctigue DM, Popovich PG. Deletion of the fractalkine receptor, CX3CR1, improves endogenous repair, axon sprouting, and synaptogenesis after spinal cord injury in mice. J Neurosci. 2017;37:3568–87.
36.Gensel JC, Nakamura S, Guan Z, Van Rooijen N, Ankeny DP, Popovich PG. Macrophages promote axon regeneration with concurrent neurotoxicity. J Neurosci. 2009;29:3956–68.
37.Yawata I, Takeuchi H, Doi Y, Liang J, Mizuno T, Suzumura A. Macrophage-induced neurotoxicity is mediated by glutamate and attenuated by glutaminase inhibitors and gap junction inhibitors. Life Sci. 2008;82:1111–6.
38.Busch SA, Hamilton JA, Horn KP, Cuascut FX, Cutrone R, Lehman N, et al. Multipotent adult progenitor cells prevent macrophage-mediated axonal dieback and promote regrowth after spinal cord injury. J Neurosci. 2011;31:944–53.
39.Depaul MA, Palmer M, Lang BT, Cutrone R, Tran AP, Madalena KM, et al. Intravenous multipotent adult progenitor cell treatment decreases inflammation leading to functional recovery following spinal cord injury. Sci Rep. 2015;5:16795.
40.Sas AR, Carbajal KS, Jerome AD, Menon R, Yoon C, Kalinski AL, et al. A new neutrophil subset promotes cns neuron survival and axon regeneration. Nat Immunol. 2020;21:1496–505.
41.Ankeny DP, Guan Z, Popovich PG. B cells produce pathogenic antibodies and impair recovery after spinal cord injury in mice. J Clin Invest. 2009;119:2990–9.
42.Lacroix S, Chang L, Rose-John S, Tuszynski MH. Delivery of hyper-interleukin-6 to the injured spinal cord increases neutrophil and macrophage infiltration and inhibits axonal growth. J Comp Neurol. 2002;454:213–28.
43.Jones TB, Basso DM, Sodhi A, Pan JZ, Hart RP, Maccallum RC, et al. Pathological CNS autoimmune disease triggered by traumatic spinal cord injury: implications for autoimmune vaccine therapy. J Neurosci. 2002;22:2690–700.
44.Jones TB, Ankeny DP, Guan Z, Mcgaughy V, Fisher LC, Basso DM, et al. Passive or active immunization with myelin basic protein impairs neurological function and exacerbates neuropathology after spinal cord injury in rats. J Neurosci. 2004;24:3752–61.
45.Ghosh S, Hui SP. Axonal regeneration in zebrafish spinal cord. Regeneration (Oxf). 2018;5:43–60.
46.Iribarne M. Inflammation induces zebrafish regeneration. Neural Regen Res. 2021;16:1693–701.
47.Tsarouchas TM, Wehner D, Cavone L, Munir T, Keatinge M, Lambertus M, et al. Dynamic control of proinflammatory cytokines IL-1β and TNF-α by macrophages in zebrafish spinal cord regeneration. Nat Commun. 2018;9:4670.
48.Oosterhof N, Holtman IR, Kuil LE, Van Der Linde HC, Boddeke EW, Eggen BJ, et al. Identification of a conserved and acute neurodegeneration-specific microglial transcriptome in the zebrafish. Glia. 2017;65:138–49.
49.Hui SP, Sengupta D, Lee SG, Sen T, Kundu S, Mathavan S, et al. Genome wide expression profiling during spinal cord regeneration identifies comprehensive cellular responses in zebrafish. PLoS One. 2014;9:e84212.
50.Hui SP, Dutta A, Ghosh S. Cellular response after crush injury in adult zebrafish spinal cord. Dev Dyn. 2010;239:2962–79.
51.Fleming JC, Norenberg MD, Ramsay DA, Dekaban GA, Marcillo AE, Saenz AD, et al. The cellular inflammatory response in human spinal cords after injury. Brain. 2006;129:3249–69.
52.Kigerl KA, Mcgaughy VM, Popovich PG. Comparative analysis of lesion development and intraspinal inflammation in four strains of mice following spinal contusion injury. J Comp Neurol. 2006;494:578–94.
53.Donnelly DJ, Popovich PG. Inflammation and its role in neuroprotection, axonal regeneration and functional recovery after spinal cord injury. Exp Neurol. 2008;209:378–88.
54.Kigerl KA, Gensel JC, Ankeny DP, Alexander JK, Donnelly DJ, Popovich PG. Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J Neurosci. 2009;29:13435–44.
55.Beck KD, Nguyen HX, Galvan MD, Salazar DL, Woodruff TM, Anderson AJ. Quantitative analysis of cellular inflammation after traumatic spinal cord injury: evidence for a multiphasic inflammatory response in the acute to chronic environment. Brain. 2010;133:433–47.
56.Wang X, Cao K, Sun X, Chen Y, Duan Z, Sun L, et al. Macrophages in spinal cord injury: phenotypic and functional change from exposure to myelin debris. Glia. 2015;63:635–51.
57.Gupta S, Adhikary S, Hui SP. Decoding the proregenerative competence of regulatory t cells through complex tissue regeneration in zebrafish. Clin Exp Immunol. 2021;206:346–53.
58.Casha S, Rice T, Stirling DP, Silva C, Gnanapavan S, Giovannoni G, et al. Cerebrospinal fluid biomarkers in human spinal cord injury from a phase II minocycline trial. J Neurotrauma. 2018;35:1918–28.
59.Casha S, Zygun D, Mcgowan MD, Bains I, Yong VW, Hurlbert RJ. Results of a phase II placebo-controlled randomized trial of minocycline in acute spinal cord injury. Brain. 2012;135:1224–36.
60.Sencar L, Yilmaz DM, Tuli A, Polat S. Effects of combined treatment of minocycline and methylprednisolone on the expression of tumor necrosis factor alpha and interleukine-6 in experimental spinal cord injury: a light and electron microscopic study. Ultrastruct Pathol. 2020;44:283–99.
61.Ren Y, Young W. Managing inflammation after spinal cord injury through manipulation of macrophage function. Neural Plast. 2013;2013:945034.
62.Aschauer-Wallner S, Leis S, Bogdahn U, Johannesen S, Couillard-Despres S, Aigner L. Granulocyte colony-stimulating factor in traumatic spinal cord injury. Drug Discov Today. 2021;26:1642–55.
63.Koda M, Hanaoka H, Fujii Y, Hanawa M, Kawasaki Y, Ozawa Y, et al. Randomized trial of granulocyte colony-stimulating factor for spinal cord injury. Brain. 2021;144:789–99.
64.Genovese T, Esposito E, Mazzon E, Di Paola R, Muià C, Meli R, et al. Effect of cyclopentanone prostaglandin 15-deoxy-Δ12,14-PGJ2 on early functional recovery from experimental spinal cord injury. Shock. 2008;30:142–52.
65.Meng QQ, Feng ZC, Zhang XL, Hu LQ, Wang M, Zhang HF, et al. PPAR-γ activation exerts an anti-inflammatory effect by suppressing the NLRP3 inflammasome in spinal cord-derived neurons. Mediat Inflamm. 2019;2019:6386729.
66.Mctigue DM, Tripathi R, Wei P, Lash AT. The ppar gamma agonist pioglitazone improves anatomical and locomotor recovery after rodent spinal cord injury. Exp Neurol. 2007;205:396–406.
67.Park SW, Yi JH, Miranpuri G, Satriotomo I, Bowen K, Resnick DK, et al. Thiazolidinedione class of peroxisome proliferator-activated receptor gamma agonists prevents neuronal damage, motor dysfunction, myelin loss, neuropathic pain, and inflammation after spinal cord injury in adult rats. J Pharmacol Exp Ther. 2007;320:1002–12.
68.Zou HJ, Guo SW, Zhu L, Xu X, Liu JB. Methylprednisolone induces neuro-protective effects via the inhibition of A1 astrocyte activation in traumatic spinal cord injury mouse models. Front Neurosci. 2021;15:628917.
69.Chio JCT, Xu KJ, Popovich P, David S, Fehlings MG. Neuroimmunological therapies for treating spinal cord injury: evidence and future perspectives. Exp Neurol. 2021;341:113704.
70.Singh PL, Agarwal N, Barrese JC, Heary RF. Current therapeutic strategies for inflammation following traumatic spinal cord injury. Neural Regen Res. 2012;7:1812–21.
71.Zhang Y, Al Mamun A, Yuan Y, Lu Q, Xiong J, Yang S, et al. Acute spinal cord injury: pathophysiology and pharmacological intervention (review). Mol Med Rep. 2021;23:1–18.
72.Squair JW, Ruiz I, Phillips AA, Zheng MMZ, Sarafis ZK, Sachdeva R, et al. Minocycline reduces the severity of autonomic dysreflexia after experimental spinal cord injury. J Neurotrauma. 2018;35:2861–71.
73.Stirling DP, Khodarahmi K, Liu J, Mcphail LT, Mcbride CB, Steeves JD, et al. Minocycline treatment reduces delayed oligodendrocyte death, attenuates axonal dieback, and improves functional outcome after spinal cord injury. J Neurosci. 2004;24:2182–90.
74.Badhiwala JH, Ahuja CS, Fehlings MG. Time is spine: a review of translational advances in spinal cord injury. J Neurosurg Spine. 2018;30:1–18.
75.Afshari K, Momeni Roudsari N, Lashgari NA, Haddadi NS, Haj-Mirzaian A, Hassan Nejad M, et al. Antibiotics with therapeutic effects on spinal cord injury: a review. Fundam Clin Pharmacol. 2021;35:277–304.
76.Wang P, Xie ZD, Xie CN, Lin CW, Wang JL, Xuan LN, et al. Amp-activated protein kinase-dependent induction of autophagy by erythropoietin protects against spinal cord injury in rats. CNS Neurosci Ther. 2018;24:1185–95.
77.Wang H, Zhou WX, Huang JF, Zheng XQ, Tian HJ, Wang B, et al. Endocrine therapy for the functional recovery of spinal cord injury. Front Neurosci. 2020;14:590570.
78.Mofidi A, Bader A, Pavlica S. The use of erythropoietin and its derivatives to treat spinal cord injury. Mini Rev Med Chem. 2011;11:763–70.
79.Matis GK, Birbilis TA. Erythropoietin in spinal cord injury. Eur Spine J. 2009;18:314–23.
80.Lee JY, Choi HY, Ju BG, Yune TY. Estrogen alleviates neuropathic pain induced after spinal cord injury by inhibiting microglia and astrocyte activation. Biochim Biophys Acta Mol basis Dis. 2018;1864:2472–80.
81.Sribnick EA, Wingrave JM, Matzelle DD, Wilford GG, Ray SK, Banik NL. Estrogen attenuated markers of inflammation and decreased lesion volume in acute spinal cord injury in rats. J Neurosci Res. 2005;82:283–93.
82.Hasturk AE, Baran C, Yilmaz ER, Arikan M, Togral G, Hayirli N, et al. Etanercept prevents histopathological damage after spinal cord injury in rats. Asian J Neurosurg. 2018;13:37–45.
83.Marchand F, Tsantoulas C, Singh D, Grist J, Clark AK, Bradbury EJ, et al. Effects of etanercept and minocycline in a rat model of spinal cord injury. Eur J Pain. 2009;13:673–81.
84.Schaal SM, Garg MS, Ghosh M, Lovera L, Lopez M, Patel M, et al. The therapeutic profile of rolipram, PDE target and mechanism of action as a neuroprotectant following spinal cord injury. PLoS One. 2012;7:e43634.
85.Whitaker CM, Beaumont E, Wells MJ, Magnuson DS, Hetman M, Onifer SM. Rolipram attenuates acute oligodendrocyte death in the adult rat ventrolateral funiculus following contusive cervical spinal cord injury. Neurosci Lett. 2008;438:200–4.
86.Costa LM, Pereira JE, Filipe VM, Magalhães LG, Couto PA, Gonzalo-Orden JM, et al. Rolipram promotes functional recovery after contusive thoracic spinal cord injury in rats. Behav Brain Res. 2013;243:66–73.
87.Beaumont E, Whitaker CM, Burke DA, Hetman M, Onifer SM. Effects of rolipram on adult rat oligodendrocytes and functional recovery after contusive cervical spinal cord injury. Neuroscience. 2009;163:985–90.
88.Iannotti CA, Clark M, Horn KP, Van Rooijen N, Silver J, Steinmetz MP. A combination immunomodulatory treatment promotes neuroprotection and locomotor recovery after contusion sci. Exp Neurol. 2011;230:3–15.
89.Nikulina E, Tidwell JL, Dai HN, Bregman BS, Filbin MT. The phosphodiesterase inhibitor rolipram delivered after a spinal cord lesion promotes axonal regeneration and functional recovery. Proc Natl Acad Sci U S A. 2004;101:8786–90.
90.Bao F, Omana V, Brown A, Weaver LC. The systemic inflammatory response after spinal cord injury in the rat is decreased by α4β1 integrin blockade. J Neurotrauma. 2012;29:1626–37.
91.Fleming JC, Bao F, Chen Y, Hamilton EF, Relton JK, Weaver LC. Alpha4beta1 integrin blockade after spinal cord injury decreases damage and improves neurological function. Exp Neurol. 2008;214:147–59.
92.Mashaghi A, Marmalidou A, Tehrani M, Grace PM, Pothoulakis C, Dana R. Neuropeptide substance P and the immune response. Cell Mol Life Sci. 2016;73:4249–64.
93.Jiang MH, Chung E, Chi GF, Ahn W, Lim JE, Hong HS, et al. Substance P induces M2-type macrophages after spinal cord injury. Neuroreport. 2012;23:786–92.
94.Yang L, Li G, Ye J, Lu D, Chen Z, Xiang AP, et al. Substance P enhances endogenous neurogenesis to improve functional recovery after spinal cord injury. Int J Biochem Cell Biol. 2017;89:110–9.
95.Jiang MH, Lim JE, Chi GF, Ahn W, Zhang M, Chung E, et al. Substance P reduces apoptotic cell death possibly by modulating the immune response at the early stage after spinal cord injury. Neuroreport. 2013;24:846–51.
96.Khorasanizadeh M, Eskian M, Vaccaro AR, Rahimi-Movaghar V. Granulocyte colony-stimulating factor (G-CSF) for the treatment of spinal cord injury. CNS Drugs. 2017;31:911–37.
97.Torregrossa F, Sallì M, Grasso G. Emerging therapeutic strategies for traumatic spinal cord injury. World Neurosurg. 2020;140:591–601.
98.Kawabe J, Koda M, Hashimoto M, Fujiyoshi T, Furuya T, Endo T, et al. Neuroprotective effects of granulocyte colony-stimulating factor and relationship to promotion of angiogenesis after spinal cord injury in rats: laboratory investigation. J Neurosurg Spine. 2011;15:414–21.
99.Putatunda R, Bethea JR, Hu WH. Potential immunotherapies for traumatic brain and spinal cord injury. Chin J Traumatol. 2018;21:125–36.
0
Views
0
下载量
0
CSCD
- L-PDFDownload
- Meta-XMLDownload
- BibTeXDownload
- EndnoteDownload
- RefMan Download
- NoteExpressDownload
- NoteFirstDownload
Publicity Resources
Related Articles
Related Author
Related Institution
- Technical support is provided by Beijing Founder electronics co., LTD 京ICP备09064830号-19
京公网安备11010802024621 - It is recommended to read the content of this site in Chrome&IE9+. Please switch to extreme mode in browser 360.
- Cookies We use cookies to help provide and enhance our service and tailor content. By continuing, you agree to the use of cookies.
