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Published in: Metabolic Brain Disease 3/2016

01-06-2016 | Review Article

Neuron specific enolase: a promising therapeutic target in acute spinal cord injury

Authors: Azizul Haque, Swapan K. Ray, April Cox, Naren L. Banik

Published in: Metabolic Brain Disease | Issue 3/2016

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Abstract

Enolase is a multifunctional protein, which is expressed abundantly in the cytosol. Upon stimulatory signals, enolase can traffic to cell surface and contribute to different pathologies including injury, autoimmunity, infection, inflammation, and cancer. Cell-surface expression of enolase is often detected on activated macrophages, microglia/macrophages, microglia, and astrocytes, promoting extracellular matrix degradation, production of pro-inflammatory cytokines/chemokines, and invasion of inflammatory cells in the sites of injury and inflammation. Inflammatory stimulation also induces translocation of enolase from the cytosolic pool to the cell surface where it can act as a plasminogen receptor and promote extracellular matrix degradation and tissue damage. Spinal cord injury (SCI) is a devastating debilitating condition characterized by progressive pathological changes including complex and evolving molecular cascades, and insights into the role of enolase in multiple inflammatory events have not yet been fully elucidated. Neuronal damage following SCI is associated with an elevation of neuron specific enolase (NSE), which is also known to play a role in the pathogenesis of hypoxic-ischemic brain injury. Thus, NSE is now considered as a biomarker in ischemic brain damage, and it has recently been suggested to be a biomarker in traumatic brain injury (TBI), stroke and anoxic encephalopathy after cardiac arrest and acute SCI as well. This review article gives an overview of the current basic research and clinical studies on the role of multifunctional enolase in neurotrauma, with a special emphasis on NSE in acute SCI.
Literature
go back to reference Pancholi V (2001) Multifunctional alpha-enolase: its role in diseases. Cellular and Molecular Life Sciences: CMLS 58:902–920 Pancholi V (2001) Multifunctional alpha-enolase: its role in diseases. Cellular and Molecular Life Sciences: CMLS 58:902–920
go back to reference Diaz-Ramos A, Roig-Borrellas A, Garcia-Melero A (2012) Lopez-alemany R (2012) alpha-enolase, a multifunctional protein: its role on pathophysiological situations. J Biomed Biotechnol 156795 Diaz-Ramos A, Roig-Borrellas A, Garcia-Melero A (2012) Lopez-alemany R (2012) alpha-enolase, a multifunctional protein: its role on pathophysiological situations. J Biomed Biotechnol 156795
go back to reference Chen SH, Giblett ER (1976) Enolase: human tissue distribution and evidence for three different loci. Ann Hum Genet 39:277–280CrossRefPubMed Chen SH, Giblett ER (1976) Enolase: human tissue distribution and evidence for three different loci. Ann Hum Genet 39:277–280CrossRefPubMed
go back to reference Fan SS, Zong M, Zhang H, Lu Y, Lu TB, Fan LY (2015) Decreased expression of alpha-enolase inhibits the proliferation of hypoxia-induced rheumatoid arthritis fibroblasts-like synoviocytes. Modern Rheumatology/the Japan Rheumatism Association 25:701–707 Fan SS, Zong M, Zhang H, Lu Y, Lu TB, Fan LY (2015) Decreased expression of alpha-enolase inhibits the proliferation of hypoxia-induced rheumatoid arthritis fibroblasts-like synoviocytes. Modern Rheumatology/the Japan Rheumatism Association 25:701–707
go back to reference Kuehn A, Fischer J, Hilger C, Sparla C, Biedermann T, Hentges F (2014) Correlation of clinical monosensitivity to cod with specific IgE to enolase and aldolase. Annals of allergy, asthma & immunology: official publication of the American College of Allergy, Asthma, & Immunology 113:670–671 e672 Kuehn A, Fischer J, Hilger C, Sparla C, Biedermann T, Hentges F (2014) Correlation of clinical monosensitivity to cod with specific IgE to enolase and aldolase. Annals of allergy, asthma & immunology: official publication of the American College of Allergy, Asthma, & Immunology 113:670–671 e672
go back to reference Fukano K, Kimura K (2014) Measurement of enolase activity in cell lysates. Methods Enzymol 542:115–124CrossRefPubMed Fukano K, Kimura K (2014) Measurement of enolase activity in cell lysates. Methods Enzymol 542:115–124CrossRefPubMed
go back to reference Vermeulen N, Arijs I, Joossens S, Vermeire S, Clerens S, Van den Bergh K, Michiels G, Arckens L, Schuit F, Van Lommel L, Rutgeerts P, Bossuyt X (2008) Anti-alpha-enolase antibodies in patients with inflammatory bowel disease. Clin Chem 54:534–541CrossRefPubMed Vermeulen N, Arijs I, Joossens S, Vermeire S, Clerens S, Van den Bergh K, Michiels G, Arckens L, Schuit F, Van Lommel L, Rutgeerts P, Bossuyt X (2008) Anti-alpha-enolase antibodies in patients with inflammatory bowel disease. Clin Chem 54:534–541CrossRefPubMed
go back to reference Bock A, Tucker N, Kelher MR, Khan SY, Gonzalez E, Wohlauer M, Hansen K, Dzieciatkowska M, Sauaia A, Banerjee A, Moore EE, Silliman CC (2015) Alpha-enolase causes proinflammatory activation of pulmonary microvascular endothelial cells and primes neutrophils through plasmin activation of protease-activated receptor 2. Shock 44:137–142CrossRefPubMed Bock A, Tucker N, Kelher MR, Khan SY, Gonzalez E, Wohlauer M, Hansen K, Dzieciatkowska M, Sauaia A, Banerjee A, Moore EE, Silliman CC (2015) Alpha-enolase causes proinflammatory activation of pulmonary microvascular endothelial cells and primes neutrophils through plasmin activation of protease-activated receptor 2. Shock 44:137–142CrossRefPubMed
go back to reference Kolberg J, Aase A, Bergmann S, Herstad TK, Rodal G, Frank R, Rohde M, Hammerschmidt S (2006) Streptococcus pneumoniae enolase is important for plasminogen binding despite low abundance of enolase protein on the bacterial cell surface. Microbiology 152:1307–1317CrossRefPubMed Kolberg J, Aase A, Bergmann S, Herstad TK, Rodal G, Frank R, Rohde M, Hammerschmidt S (2006) Streptococcus pneumoniae enolase is important for plasminogen binding despite low abundance of enolase protein on the bacterial cell surface. Microbiology 152:1307–1317CrossRefPubMed
go back to reference Bae S, Kim H, Lee N, Won C, Kim HR, Hwang YI, Song YW, Kang JS, Lee WJ (2012) Alpha-enolase expressed on the surfaces of monocytes and macrophages induces robust synovial inflammation in rheumatoid arthritis. J Immunol 189:365–372CrossRefPubMed Bae S, Kim H, Lee N, Won C, Kim HR, Hwang YI, Song YW, Kang JS, Lee WJ (2012) Alpha-enolase expressed on the surfaces of monocytes and macrophages induces robust synovial inflammation in rheumatoid arthritis. J Immunol 189:365–372CrossRefPubMed
go back to reference Shie J, Li Y, Yang X, Yang D, Zhang Y, Liu Y (2014) Upregulation of alpha-enolase in acute rejection of cardiac transplant in rat model: implications for the secretion of interleukin-17. Pediatr Transplant 18:575–585CrossRef Shie J, Li Y, Yang X, Yang D, Zhang Y, Liu Y (2014) Upregulation of alpha-enolase in acute rejection of cardiac transplant in rat model: implications for the secretion of interleukin-17. Pediatr Transplant 18:575–585CrossRef
go back to reference Pouw MH, Hosman AJ, van Middendorp JJ, Verbeek MM, Vos PE, van de Meent H (2009) Biomarkers in spinal cord injury. Spinal Cord 47:519–525CrossRefPubMed Pouw MH, Hosman AJ, van Middendorp JJ, Verbeek MM, Vos PE, van de Meent H (2009) Biomarkers in spinal cord injury. Spinal Cord 47:519–525CrossRefPubMed
go back to reference Redlitz A, Fowler BJ, Plow EF, Miles LA (1995) The role of an enolase-related molecule in plasminogen binding to cells. European Journal of Biochemistry/FEBS 227:407–415CrossRefPubMed Redlitz A, Fowler BJ, Plow EF, Miles LA (1995) The role of an enolase-related molecule in plasminogen binding to cells. European Journal of Biochemistry/FEBS 227:407–415CrossRefPubMed
go back to reference Sawhney S, Hood K, Shaw A, Braithwaite AW, Stubbs R, Hung NA, Royds JA, Slatter TL (2015) Alpha-enolase is upregulated on the cell surface and responds to plasminogen activation in mice expressing a 133p53alpha mimic. PLoS One 10:e0116270CrossRefPubMedPubMedCentral Sawhney S, Hood K, Shaw A, Braithwaite AW, Stubbs R, Hung NA, Royds JA, Slatter TL (2015) Alpha-enolase is upregulated on the cell surface and responds to plasminogen activation in mice expressing a 133p53alpha mimic. PLoS One 10:e0116270CrossRefPubMedPubMedCentral
go back to reference Lopez-Alemany R, Longstaff C, Hawley S, Mirshahi M, Fabregas P, Jardi M, Merton E, Miles LA, Felez J (2003) Inhibition of cell surface mediated plasminogen activation by a monoclonal antibody against alpha-enolase. Am J Hematol 72:234–242CrossRefPubMed Lopez-Alemany R, Longstaff C, Hawley S, Mirshahi M, Fabregas P, Jardi M, Merton E, Miles LA, Felez J (2003) Inhibition of cell surface mediated plasminogen activation by a monoclonal antibody against alpha-enolase. Am J Hematol 72:234–242CrossRefPubMed
go back to reference Pouw MH, Kwon BK, Verbeek MM, Vos PE, van Kampen A, Fisher CG, Street J, Paquette SJ, Dvorak MF, Boyd MC, Hosman AJ, van de Meent H (2014) Structural biomarkers in the cerebrospinal fluid within 24 h after a traumatic spinal cord injury: a descriptive analysis of 16 subjects. Spinal Cord 52:428–433CrossRefPubMed Pouw MH, Kwon BK, Verbeek MM, Vos PE, van Kampen A, Fisher CG, Street J, Paquette SJ, Dvorak MF, Boyd MC, Hosman AJ, van de Meent H (2014) Structural biomarkers in the cerebrospinal fluid within 24 h after a traumatic spinal cord injury: a descriptive analysis of 16 subjects. Spinal Cord 52:428–433CrossRefPubMed
go back to reference Berger RP, Pierce MC, Wisniewski SR, Adelson PD, Clark RS, Ruppel RA, Kochanek PM (2002) Neuron-specific enolase and S100B in cerebrospinal fluid after severe traumatic brain injury in infants and children. Pediatrics 109:E31CrossRefPubMed Berger RP, Pierce MC, Wisniewski SR, Adelson PD, Clark RS, Ruppel RA, Kochanek PM (2002) Neuron-specific enolase and S100B in cerebrospinal fluid after severe traumatic brain injury in infants and children. Pediatrics 109:E31CrossRefPubMed
go back to reference Sribnick EA, Samantaray S, Das A, Smith J, Matzelle DD, Ray SK, Banik NL (2010) Postinjury estrogen treatment of chronic spinal cord injury improves locomotor function in rats. J Neurosci Res 88:1738–1750PubMedPubMedCentral Sribnick EA, Samantaray S, Das A, Smith J, Matzelle DD, Ray SK, Banik NL (2010) Postinjury estrogen treatment of chronic spinal cord injury improves locomotor function in rats. J Neurosci Res 88:1738–1750PubMedPubMedCentral
go back to reference Dumont RJ, Okonkwo DO, Verma S, Hurlbert RJ, Boulos PT, Ellegala DB, Dumont AS (2001) Acute spinal cord injury, part I: pathophysiologic mechanisms. Clin Neuropharmacol 24:254–264CrossRefPubMed Dumont RJ, Okonkwo DO, Verma S, Hurlbert RJ, Boulos PT, Ellegala DB, Dumont AS (2001) Acute spinal cord injury, part I: pathophysiologic mechanisms. Clin Neuropharmacol 24:254–264CrossRefPubMed
go back to reference Oyinbo CA (2011) Secondary injury mechanisms in traumatic spinal cord injury: a nugget of this multiply cascade. Acta Neurobiol Exp 71:281–299 Oyinbo CA (2011) Secondary injury mechanisms in traumatic spinal cord injury: a nugget of this multiply cascade. Acta Neurobiol Exp 71:281–299
go back to reference Zhang N, Yin Y, Xu SJ, Wu YP, Chen WS (2012) Inflammation & apoptosis in spinal cord injury. Indian J Med Res 135:287–296PubMedPubMedCentral Zhang N, Yin Y, Xu SJ, Wu YP, Chen WS (2012) Inflammation & apoptosis in spinal cord injury. Indian J Med Res 135:287–296PubMedPubMedCentral
go back to reference Chamberlain JD, Meier S, Mader L, von Groote PM, Brinkhof MW (2015) Mortality and longevity after a spinal cord injury: systematic review and meta-analysis. Neuroepidemiology 44:182–198CrossRefPubMed Chamberlain JD, Meier S, Mader L, von Groote PM, Brinkhof MW (2015) Mortality and longevity after a spinal cord injury: systematic review and meta-analysis. Neuroepidemiology 44:182–198CrossRefPubMed
go back to reference Tator CH, Fehlings MG (1991) Review of the secondary injury theory of acute spinal cord trauma with emphasis on vascular mechanisms. J Neurosurg 75:15–26CrossRefPubMed Tator CH, Fehlings MG (1991) Review of the secondary injury theory of acute spinal cord trauma with emphasis on vascular mechanisms. J Neurosurg 75:15–26CrossRefPubMed
go back to reference Mortazavi MM, Verma K, Harmon OA, Griessenauer CJ, Adeeb N, Theodore N, Tubbs RS (2015) The microanatomy of spinal cord injury: a review. Clin Anat 28:27–36CrossRefPubMed Mortazavi MM, Verma K, Harmon OA, Griessenauer CJ, Adeeb N, Theodore N, Tubbs RS (2015) The microanatomy of spinal cord injury: a review. Clin Anat 28:27–36CrossRefPubMed
go back to reference Almad A, Sahinkaya FR, McTigue DM (2011) Oligodendrocyte fate after spinal cord injury. Neurotherapeutics: the Journal of the American Society For Experimental NeuroTherapeutics 8:262–273 Almad A, Sahinkaya FR, McTigue DM (2011) Oligodendrocyte fate after spinal cord injury. Neurotherapeutics: the Journal of the American Society For Experimental NeuroTherapeutics 8:262–273
go back to reference Li N, Leung GK (2015) Oligodendrocyte precursor cells in spinal cord injury: A review and update. BioMed Res Int 2015:235195PubMedPubMedCentral Li N, Leung GK (2015) Oligodendrocyte precursor cells in spinal cord injury: A review and update. BioMed Res Int 2015:235195PubMedPubMedCentral
go back to reference Lebioda L, Stec B (1988) Crystal structure of enolase indicates that enolase and pyruvate kinase evolved from a common ancestor. Nature 333:683–686CrossRefPubMed Lebioda L, Stec B (1988) Crystal structure of enolase indicates that enolase and pyruvate kinase evolved from a common ancestor. Nature 333:683–686CrossRefPubMed
go back to reference Wygrecka M, Marsh LM, Morty RE, Henneke I, Guenther A, Lohmeyer J, Markart P, Preissner KT (2009) Enolase-1 promotes plasminogen-mediated recruitment of monocytes to the acutely inflamed lung. Blood 113:5588–5598CrossRefPubMed Wygrecka M, Marsh LM, Morty RE, Henneke I, Guenther A, Lohmeyer J, Markart P, Preissner KT (2009) Enolase-1 promotes plasminogen-mediated recruitment of monocytes to the acutely inflamed lung. Blood 113:5588–5598CrossRefPubMed
go back to reference Hsiao KC, Shih NY, Fang HL, Huang TS, Kuo CC, Chu PY, Hung YM, Chou SW, Yang YY, Chang GC, Liu KJ (2013) Surface alpha-enolase promotes extracellular matrix degradation and tumor metastasis and represents a new therapeutic target. PLoS One 8:e69354CrossRefPubMedPubMedCentral Hsiao KC, Shih NY, Fang HL, Huang TS, Kuo CC, Chu PY, Hung YM, Chou SW, Yang YY, Chang GC, Liu KJ (2013) Surface alpha-enolase promotes extracellular matrix degradation and tumor metastasis and represents a new therapeutic target. PLoS One 8:e69354CrossRefPubMedPubMedCentral
go back to reference Shih NY, Lai HL, Chang GC, Lin HC, Wu YC, Liu JM, Liu KJ, Tseng SW (2010) Anti-alpha-enolase autoantibodies are down-regulated in advanced cancer patients. Jpn J Clin Oncol 40:663–669CrossRefPubMed Shih NY, Lai HL, Chang GC, Lin HC, Wu YC, Liu JM, Liu KJ, Tseng SW (2010) Anti-alpha-enolase autoantibodies are down-regulated in advanced cancer patients. Jpn J Clin Oncol 40:663–669CrossRefPubMed
go back to reference Oliva D, Cali L, Feo S, Giallongo A (1991) Complete structure of the human gene encoding neuron-specific enolase. Genomics 10:157–165CrossRefPubMed Oliva D, Cali L, Feo S, Giallongo A (1991) Complete structure of the human gene encoding neuron-specific enolase. Genomics 10:157–165CrossRefPubMed
go back to reference Hafner A, Obermajer N, Kos J (2012) Gamma-enolase C-terminal peptide promotes cell survival and neurite outgrowth by activation of the PI3K/akt and MAPK/ERK signalling pathways. Biochem J 443:439–450CrossRefPubMed Hafner A, Obermajer N, Kos J (2012) Gamma-enolase C-terminal peptide promotes cell survival and neurite outgrowth by activation of the PI3K/akt and MAPK/ERK signalling pathways. Biochem J 443:439–450CrossRefPubMed
go back to reference Anand N, Stead LG (2005) Neuron-specific enolase as a marker for acute ischemic stroke: a systematic review. Cerebrovasc Dis 20:213–219CrossRefPubMed Anand N, Stead LG (2005) Neuron-specific enolase as a marker for acute ischemic stroke: a systematic review. Cerebrovasc Dis 20:213–219CrossRefPubMed
go back to reference Pleines UE, Morganti-Kossmann MC, Rancan M, Joller H, Trentz O, Kossmann T (2001) S-100 beta reflects the extent of injury and outcome, whereas neuronal specific enolase is a better indicator of neuroinflammation in patients with severe traumatic brain injury. J Neurotrauma 18:491–498CrossRefPubMed Pleines UE, Morganti-Kossmann MC, Rancan M, Joller H, Trentz O, Kossmann T (2001) S-100 beta reflects the extent of injury and outcome, whereas neuronal specific enolase is a better indicator of neuroinflammation in patients with severe traumatic brain injury. J Neurotrauma 18:491–498CrossRefPubMed
go back to reference Cheng F, Yuan Q, Yang J, Wang W, Liu H (2014) The prognostic value of serum neuron-specific enolase in traumatic brain injury: systematic review and meta-analysis. PLoS One 9:e106680CrossRefPubMedPubMedCentral Cheng F, Yuan Q, Yang J, Wang W, Liu H (2014) The prognostic value of serum neuron-specific enolase in traumatic brain injury: systematic review and meta-analysis. PLoS One 9:e106680CrossRefPubMedPubMedCentral
go back to reference Zhang M, Ma YF, Gan JX, Jiang GY, Xu SX, Tao XL, Hong A, Li JK (2005) Basic fibroblast growth factor alleviates brain injury following global ischemia reperfusion in rabbits. Journal of Zhejiang University Science B 6:637–643 Zhang M, Ma YF, Gan JX, Jiang GY, Xu SX, Tao XL, Hong A, Li JK (2005) Basic fibroblast growth factor alleviates brain injury following global ischemia reperfusion in rabbits. Journal of Zhejiang University Science B 6:637–643
go back to reference Li M, Wen H, Yan Z, Ding T, Long L, Qin H, Wang H, Zhang F (2014) Temporal-spatial expression of ENOLASE after acute spinal cord injury in adult rats. Neurosci Res 79:76–82CrossRefPubMed Li M, Wen H, Yan Z, Ding T, Long L, Qin H, Wang H, Zhang F (2014) Temporal-spatial expression of ENOLASE after acute spinal cord injury in adult rats. Neurosci Res 79:76–82CrossRefPubMed
go back to reference Cao F, Yang XF, Liu WG, Hu WW, Li G, Zheng XJ, Shen F, Zhao XQ, Lv ST (2008) Elevation of neuron-specific enolase and S-100beta protein level in experimental acute spinal cord injury. Journal of Clinical Neuroscience: Official Journal of the Neurosurgical Society Of Australasia 15:541–544 Cao F, Yang XF, Liu WG, Hu WW, Li G, Zheng XJ, Shen F, Zhao XQ, Lv ST (2008) Elevation of neuron-specific enolase and S-100beta protein level in experimental acute spinal cord injury. Journal of Clinical Neuroscience: Official Journal of the Neurosurgical Society Of Australasia 15:541–544
go back to reference Krohn M, Dressler J, Bauer M, Schober K, Franke H, Ondruschka B (2015) Immunohistochemical investigation of S100 and NSE in cases of traumatic brain injury and its application for survival time determination. J Neurotrauma 32:430–440CrossRefPubMed Krohn M, Dressler J, Bauer M, Schober K, Franke H, Ondruschka B (2015) Immunohistochemical investigation of S100 and NSE in cases of traumatic brain injury and its application for survival time determination. J Neurotrauma 32:430–440CrossRefPubMed
go back to reference Isgro MA, Bottoni P, Scatena R (2015) Neuron-specific enolase as a biomarker: biochemical and clinical aspects. Adv Exp Med Biol 867:125–143CrossRefPubMed Isgro MA, Bottoni P, Scatena R (2015) Neuron-specific enolase as a biomarker: biochemical and clinical aspects. Adv Exp Med Biol 867:125–143CrossRefPubMed
go back to reference Li K, Tan YH, Light AR, Fu KY (2013) Different peripheral tissue injury induces differential phenotypic changes of spinal activated microglia. Clin Dev Immunol 2013:901420PubMedPubMedCentral Li K, Tan YH, Light AR, Fu KY (2013) Different peripheral tissue injury induces differential phenotypic changes of spinal activated microglia. Clin Dev Immunol 2013:901420PubMedPubMedCentral
go back to reference Mueller CA, Schluesener HJ, Conrad S, Pietsch T, Schwab JM (2006) Spinal cord injury-induced expression of the immune-regulatory chemokine interleukin-16 caused by activated microglia/macrophages and CD8+ cells. J Neurosurg Spine 4:233–240CrossRefPubMed Mueller CA, Schluesener HJ, Conrad S, Pietsch T, Schwab JM (2006) Spinal cord injury-induced expression of the immune-regulatory chemokine interleukin-16 caused by activated microglia/macrophages and CD8+ cells. J Neurosurg Spine 4:233–240CrossRefPubMed
go back to reference God JM, Cameron C, Figueroa J, Amria S, Hossain A, Kempkes B, Bornkamm GW, Stuart RK, Blum JS, Haque A (2015) Elevation of c-MYC disrupts HLA class II-mediated immune recognition of human B cell tumors. J Immunol 194:1434–1445CrossRefPubMedPubMedCentral God JM, Cameron C, Figueroa J, Amria S, Hossain A, Kempkes B, Bornkamm GW, Stuart RK, Blum JS, Haque A (2015) Elevation of c-MYC disrupts HLA class II-mediated immune recognition of human B cell tumors. J Immunol 194:1434–1445CrossRefPubMedPubMedCentral
go back to reference Royds JA, Parsons MA, Taylor CB, Timperley WR (1982) Enolase isoenzyme distribution in the human brain and its tumours. J Pathol 137:37–49CrossRefPubMed Royds JA, Parsons MA, Taylor CB, Timperley WR (1982) Enolase isoenzyme distribution in the human brain and its tumours. J Pathol 137:37–49CrossRefPubMed
go back to reference Johnsson P, Blomquist S, Luhrs C, Malmkvist G, Alling C, Solem JO, Stahl E (2000) Neuron-specific enolase increases in plasma during and immediately after extracorporeal circulation. Ann Thorac Surg 69:750–754CrossRefPubMed Johnsson P, Blomquist S, Luhrs C, Malmkvist G, Alling C, Solem JO, Stahl E (2000) Neuron-specific enolase increases in plasma during and immediately after extracorporeal circulation. Ann Thorac Surg 69:750–754CrossRefPubMed
go back to reference Goncalves CA, Leite MC, Nardin P (2008) Biological and methodological features of the measurement of S100B, a putative marker of brain injury. Clin Biochem 41:755–763CrossRefPubMed Goncalves CA, Leite MC, Nardin P (2008) Biological and methodological features of the measurement of S100B, a putative marker of brain injury. Clin Biochem 41:755–763CrossRefPubMed
go back to reference Fogel W, Krieger D, Veith M, Adams HP, Hund E, Storch-Hagenlocher B, Buggle F, Mathias D, Hacke W (1997) Serum neuron-specific enolase as early predictor of outcome after cardiac arrest. Crit Care Med 25:1133–1138CrossRefPubMed Fogel W, Krieger D, Veith M, Adams HP, Hund E, Storch-Hagenlocher B, Buggle F, Mathias D, Hacke W (1997) Serum neuron-specific enolase as early predictor of outcome after cardiac arrest. Crit Care Med 25:1133–1138CrossRefPubMed
go back to reference Cooper EH (1994) Neuron-specific enolase. Int J Biol Markers 9:205–210PubMed Cooper EH (1994) Neuron-specific enolase. Int J Biol Markers 9:205–210PubMed
go back to reference Tramontina AC, Tramontina F, Bobermin LD, Zanotto C, Souza DF, Leite MC, Nardin P, Gottfried C, Goncalves CA (2008) Secretion of S100B, an astrocyte-derived neurotrophic protein, is stimulated by fluoxetine via a mechanism independent of serotonin. Prog Neuro-Psychopharmacol Biol Psychiatry 32:1580–1583CrossRef Tramontina AC, Tramontina F, Bobermin LD, Zanotto C, Souza DF, Leite MC, Nardin P, Gottfried C, Goncalves CA (2008) Secretion of S100B, an astrocyte-derived neurotrophic protein, is stimulated by fluoxetine via a mechanism independent of serotonin. Prog Neuro-Psychopharmacol Biol Psychiatry 32:1580–1583CrossRef
go back to reference Dang X, Guan L, Hu W, Du G, Li J (2014) S100B ranks as a new marker of multiple traumas in patients and may accelerate its development by regulating endothelial cell dysfunction. Int J Clin Exp Pathol 7:3818–3826PubMedPubMedCentral Dang X, Guan L, Hu W, Du G, Li J (2014) S100B ranks as a new marker of multiple traumas in patients and may accelerate its development by regulating endothelial cell dysfunction. Int J Clin Exp Pathol 7:3818–3826PubMedPubMedCentral
go back to reference Sorci G, Riuzzi F, Arcuri C, Tubaro C, Bianchi R, Giambanco I, Donato R (2013) S100B protein in tissue development, repair and regeneration. World J Biol Chem 4:1–12CrossRefPubMedPubMedCentral Sorci G, Riuzzi F, Arcuri C, Tubaro C, Bianchi R, Giambanco I, Donato R (2013) S100B protein in tissue development, repair and regeneration. World J Biol Chem 4:1–12CrossRefPubMedPubMedCentral
go back to reference Svedin P, Hagberg H, Savman K, Zhu C, Mallard C (2007) Matrix metalloproteinase-9 gene knock-out protects the immature brain after cerebral hypoxia-ischemia. J Neurosci 27:1511–1518CrossRefPubMed Svedin P, Hagberg H, Savman K, Zhu C, Mallard C (2007) Matrix metalloproteinase-9 gene knock-out protects the immature brain after cerebral hypoxia-ischemia. J Neurosci 27:1511–1518CrossRefPubMed
go back to reference Leonardo CC, Pennypacker KR (2009) Neuroinflammation and MMPs: potential therapeutic targets in neonatal hypoxic-ischemic injury. J Neuroinflammation 6:13CrossRefPubMedPubMedCentral Leonardo CC, Pennypacker KR (2009) Neuroinflammation and MMPs: potential therapeutic targets in neonatal hypoxic-ischemic injury. J Neuroinflammation 6:13CrossRefPubMedPubMedCentral
go back to reference Gearing AJ, Beckett P, Christodoulou M, Churchill M, Clements J, Davidson AH, Drummond AH, Galloway WA, Gilbert R, Gordon JL, et al. (1994) Processing of tumour necrosis factor-alpha precursor by metalloproteinases. Nature 370:555–557CrossRefPubMed Gearing AJ, Beckett P, Christodoulou M, Churchill M, Clements J, Davidson AH, Drummond AH, Galloway WA, Gilbert R, Gordon JL, et al. (1994) Processing of tumour necrosis factor-alpha precursor by metalloproteinases. Nature 370:555–557CrossRefPubMed
go back to reference Schonbeck U, Mach F, Libby P (1998) Generation of biologically active IL-1 beta by matrix metalloproteinases: a novel caspase-1-independent pathway of IL-1 beta processing. J Immunol 161:3340–3346PubMed Schonbeck U, Mach F, Libby P (1998) Generation of biologically active IL-1 beta by matrix metalloproteinases: a novel caspase-1-independent pathway of IL-1 beta processing. J Immunol 161:3340–3346PubMed
go back to reference Bruschi F, Bianchi C, Fornaro M, Naccarato G, Menicagli M, Gomez-Morales MA, Pozio E, Pinto B (2014) Matrix metalloproteinase (MMP)-2 and MMP-9 as inflammation markers of trichinella spiralis and trichinella pseudospiralis infections in mice. Parasite Immunol 36:540–549CrossRefPubMed Bruschi F, Bianchi C, Fornaro M, Naccarato G, Menicagli M, Gomez-Morales MA, Pozio E, Pinto B (2014) Matrix metalloproteinase (MMP)-2 and MMP-9 as inflammation markers of trichinella spiralis and trichinella pseudospiralis infections in mice. Parasite Immunol 36:540–549CrossRefPubMed
go back to reference Horn M, Seger F, Schlote W (1995) Neuron-specific enolase in gerbil brain and serum after transient cerebral ischemia. Stroke; a J Cereb Circ 26:290–296 discussion 296-297CrossRef Horn M, Seger F, Schlote W (1995) Neuron-specific enolase in gerbil brain and serum after transient cerebral ischemia. Stroke; a J Cereb Circ 26:290–296 discussion 296-297CrossRef
go back to reference Hardemark HG, Persson L, Bolander HG, Hillered L, Olsson Y, Pahlman S (1988) Neuron-specific enolase is a marker of cerebral ischemia and infarct size in rat cerebrospinal fluid. Stroke; a J Cereb Circ 19:1140–1144CrossRef Hardemark HG, Persson L, Bolander HG, Hillered L, Olsson Y, Pahlman S (1988) Neuron-specific enolase is a marker of cerebral ischemia and infarct size in rat cerebrospinal fluid. Stroke; a J Cereb Circ 19:1140–1144CrossRef
go back to reference Martens P, Raabe A, Johnsson P (1998) Serum S-100 and neuron-specific enolase for prediction of regaining consciousness after global cerebral ischemia. Stroke; a J Cereb Circ 29:2363–2366CrossRef Martens P, Raabe A, Johnsson P (1998) Serum S-100 and neuron-specific enolase for prediction of regaining consciousness after global cerebral ischemia. Stroke; a J Cereb Circ 29:2363–2366CrossRef
go back to reference Pfeifer R, Borner A, Krack A, Sigusch HH, Surber R, Figulla HR (2005) Outcome after cardiac arrest: predictive values and limitations of the neuroproteins neuron-specific enolase and protein S-100 and the Glasgow coma scale. Resuscitation 65:49–55CrossRefPubMed Pfeifer R, Borner A, Krack A, Sigusch HH, Surber R, Figulla HR (2005) Outcome after cardiac arrest: predictive values and limitations of the neuroproteins neuron-specific enolase and protein S-100 and the Glasgow coma scale. Resuscitation 65:49–55CrossRefPubMed
go back to reference Varma S, Janesko KL, Wisniewski SR, Bayir H, Adelson PD, Thomas NJ, Kochanek PM (2003) F2-isoprostane and neuron-specific enolase in cerebrospinal fluid after severe traumatic brain injury in infants and children. J Neurotrauma 20:781–786CrossRefPubMed Varma S, Janesko KL, Wisniewski SR, Bayir H, Adelson PD, Thomas NJ, Kochanek PM (2003) F2-isoprostane and neuron-specific enolase in cerebrospinal fluid after severe traumatic brain injury in infants and children. J Neurotrauma 20:781–786CrossRefPubMed
go back to reference Bottiger BW, Mobes S, Glatzer R, Bauer H, Gries A, Bartsch P, Motsch J, Martin E (2001) Astroglial protein S-100 is an early and sensitive marker of hypoxic brain damage and outcome after cardiac arrest in humans. Circulation 103:2694–2698CrossRefPubMed Bottiger BW, Mobes S, Glatzer R, Bauer H, Gries A, Bartsch P, Motsch J, Martin E (2001) Astroglial protein S-100 is an early and sensitive marker of hypoxic brain damage and outcome after cardiac arrest in humans. Circulation 103:2694–2698CrossRefPubMed
go back to reference Rosen H, Sunnerhagen KS, Herlitz J, Blomstrand C, Rosengren L (2001) Serum levels of the brain-derived proteins S-100 and NSE predict long-term outcome after cardiac arrest. Resuscitation 49:183–191CrossRefPubMed Rosen H, Sunnerhagen KS, Herlitz J, Blomstrand C, Rosengren L (2001) Serum levels of the brain-derived proteins S-100 and NSE predict long-term outcome after cardiac arrest. Resuscitation 49:183–191CrossRefPubMed
go back to reference Rech TH, Vieira SR, Nagel F, Brauner JS, Scalco R (2006) Serum neuron-specific enolase as early predictor of outcome after in-hospital cardiac arrest: a cohort study. Crit Care 10:R133CrossRefPubMedPubMedCentral Rech TH, Vieira SR, Nagel F, Brauner JS, Scalco R (2006) Serum neuron-specific enolase as early predictor of outcome after in-hospital cardiac arrest: a cohort study. Crit Care 10:R133CrossRefPubMedPubMedCentral
go back to reference Schoerkhuber W, Kittler H, Sterz F, Behringer W, Holzer M, Frossard M, Spitzauer S, Laggner AN (1999) Time course of serum neuron-specific enolase. A Predictor of Neurological Outcome in Patients Resuscitated from Cardiac Arrest Stroke; a Journal of Cerebral Circulation 30:1598–1603 Schoerkhuber W, Kittler H, Sterz F, Behringer W, Holzer M, Frossard M, Spitzauer S, Laggner AN (1999) Time course of serum neuron-specific enolase. A Predictor of Neurological Outcome in Patients Resuscitated from Cardiac Arrest Stroke; a Journal of Cerebral Circulation 30:1598–1603
go back to reference Pandey A, Saxena K, Verma M, Bharosay A (2011) Correlative study between neuron-specific enolase and blood sugar level in ischemic stroke patients. J Neurosci Rural Pract 2:50–54CrossRefPubMedPubMedCentral Pandey A, Saxena K, Verma M, Bharosay A (2011) Correlative study between neuron-specific enolase and blood sugar level in ischemic stroke patients. J Neurosci Rural Pract 2:50–54CrossRefPubMedPubMedCentral
go back to reference Tawk RG, Grewal SS, Heckman MG, Rawal B, Miller DA, Edmonston D, Ferguson JL, Navarro R, Ng L, Brown BL, Meschia JF, Freeman WD (2015) The relationship between serum neuron-specific enolase levels and severity of bleeding and functional outcomes in patients with nontraumatic subarachnoid hemorrhage. Neurosurgery. doi:10.1227/NEU.0000000000001140 Tawk RG, Grewal SS, Heckman MG, Rawal B, Miller DA, Edmonston D, Ferguson JL, Navarro R, Ng L, Brown BL, Meschia JF, Freeman WD (2015) The relationship between serum neuron-specific enolase levels and severity of bleeding and functional outcomes in patients with nontraumatic subarachnoid hemorrhage. Neurosurgery. doi:10.​1227/​NEU.​0000000000001140​
go back to reference Bragge P, Piccenna L, Middleton J, Williams S, Creasey G, Dunlop S, Brown D, Gruen R (2015) Developing a spinal cord injury research strategy using a structured process of evidence review and stakeholder dialogue. Part II: Background to a Research Strategy Spinal Cord 53:721–728 Bragge P, Piccenna L, Middleton J, Williams S, Creasey G, Dunlop S, Brown D, Gruen R (2015) Developing a spinal cord injury research strategy using a structured process of evidence review and stakeholder dialogue. Part II: Background to a Research Strategy Spinal Cord 53:721–728
go back to reference Hawryluk GW, Rowland J, Kwon BK, Fehlings MG (2008) Protection and repair of the injured spinal cord: a review of completed, ongoing, and planned clinical trials for acute spinal cord injury. Neurosurg Focus 25:E14CrossRefPubMed Hawryluk GW, Rowland J, Kwon BK, Fehlings MG (2008) Protection and repair of the injured spinal cord: a review of completed, ongoing, and planned clinical trials for acute spinal cord injury. Neurosurg Focus 25:E14CrossRefPubMed
go back to reference Chakrabarti M, Das A, Samantaray S, Smith JA, Banik NL, Haque A, Ray SK (2015) Molecular mechanisms of estrogen for neuroprotection in spinal cord injury and traumatic brain injury. Rev Neurosci. doi:10.1227/NEU.0000000000001140 Chakrabarti M, Das A, Samantaray S, Smith JA, Banik NL, Haque A, Ray SK (2015) Molecular mechanisms of estrogen for neuroprotection in spinal cord injury and traumatic brain injury. Rev Neurosci. doi:10.​1227/​NEU.​0000000000001140​
go back to reference Chakrabarti M, Haque A, Banik NL, Nagarkatti P, Nagarkatti M, Ray SK (2014) Estrogen receptor agonists for attenuation of neuroinflammation and neurodegeneration. Brain Res Bull 109:22–31CrossRefPubMedPubMedCentral Chakrabarti M, Haque A, Banik NL, Nagarkatti P, Nagarkatti M, Ray SK (2014) Estrogen receptor agonists for attenuation of neuroinflammation and neurodegeneration. Brain Res Bull 109:22–31CrossRefPubMedPubMedCentral
go back to reference Lo EH, Dalkara T, Moskowitz MA (2003) Mechanisms, challenges and opportunities in stroke. Nat Rev Neurosci 4:399–415CrossRefPubMed Lo EH, Dalkara T, Moskowitz MA (2003) Mechanisms, challenges and opportunities in stroke. Nat Rev Neurosci 4:399–415CrossRefPubMed
go back to reference Popovich PG, Stokes BT, Whitacre CC (1996) Concept of autoimmunity following spinal cord injury: possible roles for T lymphocytes in the traumatized central nervous system. J Neurosci Res 45:349–363CrossRefPubMed Popovich PG, Stokes BT, Whitacre CC (1996) Concept of autoimmunity following spinal cord injury: possible roles for T lymphocytes in the traumatized central nervous system. J Neurosci Res 45:349–363CrossRefPubMed
go back to reference Jones TB, Hart RP, Popovich PG (2005) Molecular control of physiological and pathological T-cell recruitment after mouse spinal cord injury. J Neurosci 25:6576–6583CrossRefPubMedPubMedCentral Jones TB, Hart RP, Popovich PG (2005) Molecular control of physiological and pathological T-cell recruitment after mouse spinal cord injury. J Neurosci 25:6576–6583CrossRefPubMedPubMedCentral
go back to reference Saville LR, Pospisil CH, Mawhinney LA, Bao F, Simedrea FC, Peters AA, O'Connell PJ, Weaver LC, Dekaban GA (2004) A monoclonal antibody to CD11d reduces the inflammatory infiltrate into the injured spinal cord: a potential neuroprotective treatment. J Neuroimmunol 156:42–57CrossRefPubMed Saville LR, Pospisil CH, Mawhinney LA, Bao F, Simedrea FC, Peters AA, O'Connell PJ, Weaver LC, Dekaban GA (2004) A monoclonal antibody to CD11d reduces the inflammatory infiltrate into the injured spinal cord: a potential neuroprotective treatment. J Neuroimmunol 156:42–57CrossRefPubMed
go back to reference Nguyen HX, O'Barr TJ, Anderson AJ (2007) Polymorphonuclear leukocytes promote neurotoxicity through release of matrix metalloproteinases, reactive oxygen species, and TNF-alpha. J Neurochem 102:900–912CrossRefPubMed Nguyen HX, O'Barr TJ, Anderson AJ (2007) Polymorphonuclear leukocytes promote neurotoxicity through release of matrix metalloproteinases, reactive oxygen species, and TNF-alpha. J Neurochem 102:900–912CrossRefPubMed
go back to reference Banik NL, Matzelle DC, Gantt-Wilford G, Osborne A, Hogan EL (1997) Increased calpain content and progressive degradation of neurofilament protein in spinal cord injury. Brain Res 752:301–306CrossRefPubMed Banik NL, Matzelle DC, Gantt-Wilford G, Osborne A, Hogan EL (1997) Increased calpain content and progressive degradation of neurofilament protein in spinal cord injury. Brain Res 752:301–306CrossRefPubMed
go back to reference Jung DW, Kim WH, Park SH, Lee J, Kim J, Su D, Ha HH, Chang YT, Williams DR (2013) A unique small molecule inhibitor of enolase clarifies its role in fundamental biological processes. ACS Chem Biol 8:1271–1282CrossRefPubMed Jung DW, Kim WH, Park SH, Lee J, Kim J, Su D, Ha HH, Chang YT, Williams DR (2013) A unique small molecule inhibitor of enolase clarifies its role in fundamental biological processes. ACS Chem Biol 8:1271–1282CrossRefPubMed
Metadata
Title
Neuron specific enolase: a promising therapeutic target in acute spinal cord injury
Authors
Azizul Haque
Swapan K. Ray
April Cox
Naren L. Banik
Publication date
01-06-2016
Publisher
Springer US
Published in
Metabolic Brain Disease / Issue 3/2016
Print ISSN: 0885-7490
Electronic ISSN: 1573-7365
DOI
https://doi.org/10.1007/s11011-016-9801-6

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