Serum and cerebrospinal fluid tau protein level as biomarkers for evaluating acute spinal cord injury severity and motor function outcome
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摘要
Tau protein, a microtubule-associated protein, has a high specific expression in neurons and axons. Because traumatic spinal cord injury mainly affects neurons and axons, we speculated that tau protein may be a promising biomarker to reflect the degree of spinal cord injury and prognosis of motor function. In this study, 160 female Sprague-Dawley rats were randomly divided into a sham group, and mild, moderate, and severe spinal cord injury groups. A laminectomy was performed at the T8 level to expose the spinal cord in all groups. A contusion lesion was made with the NYU-MASCIS impactor by dropping a 10 g rod from heights of 12.5 mm(mild), 25 mm(moderate) and 50 mm(severe) upon the exposed dorsal surface of the spinal cord. Tau protein levels were measured in serum and cerebrospinal fluid samples at 1, 6, 12, 24 hours, 3, 7, 14 and 28 days after operation. Locomotor function of all rats was assessed using the Basso, Beattie and Bresnahan locomotor rating scale. Tau protein concentration in the three spinal cord injury groups(both in serum and cerebrospinal fluid) rapidly increased and peaked at 12 hours after spinal cord injury. Statistically significant positive linear correlations were found between tau protein level and spinal cord injury severity in the three spinal cord injury groups, and between the tau protein level and Basso, Beattie, and Bresnahan locomotor rating scale scores. The tau protein level at 12 hours in the three spinal cord injury groups was negatively correlated with Basso, Beattie, and Bresnahan locomotor rating scale scores at 28 days(serum: r =-0.94; cerebrospinal fluid: r =-0.95). Our data suggest that tau protein levels in serum and cerebrospinal fluid might be a promising biomarker for predicting the severity and functional outcome of traumatic spinal cord injury.
Tau protein, a microtubule-associated protein, has a high specific expression in neurons and axons. Because traumatic spinal cord injury mainly affects neurons and axons, we speculated that tau protein may be a promising biomarker to reflect the degree of spinal cord injury and prognosis of motor function. In this study, 160 female Sprague-Dawley rats were randomly divided into a sham group, and mild, moderate, and severe spinal cord injury groups. A laminectomy was performed at the T8 level to expose the spinal cord in all groups. A contusion lesion was made with the NYU-MASCIS impactor by dropping a 10 g rod from heights of 12.5 mm(mild), 25 mm(moderate) and 50 mm(severe) upon the exposed dorsal surface of the spinal cord. Tau protein levels were measured in serum and cerebrospinal fluid samples at 1, 6, 12, 24 hours, 3, 7, 14 and 28 days after operation. Locomotor function of all rats was assessed using the Basso, Beattie and Bresnahan locomotor rating scale. Tau protein concentration in the three spinal cord injury groups(both in serum and cerebrospinal fluid) rapidly increased and peaked at 12 hours after spinal cord injury. Statistically significant positive linear correlations were found between tau protein level and spinal cord injury severity in the three spinal cord injury groups, and between the tau protein level and Basso, Beattie, and Bresnahan locomotor rating scale scores. The tau protein level at 12 hours in the three spinal cord injury groups was negatively correlated with Basso, Beattie, and Bresnahan locomotor rating scale scores at 28 days(serum: r =-0.94; cerebrospinal fluid: r =-0.95). Our data suggest that tau protein levels in serum and cerebrospinal fluid might be a promising biomarker for predicting the severity and functional outcome of traumatic spinal cord injury.
Tau protein, a microtubule-associated protein, has a high specific expression in neurons and axons. Because traumatic spinal cord injury mainly affects neurons and axons, we speculated that tau protein may be a promising biomarker to reflect the degree of spinal cord injury and prognosis of motor function. In this study, 160 female Sprague-Dawley rats were randomly divided into a sham group, and mild, moderate, and severe spinal cord injury groups. A laminectomy was performed at the T8 level to expose the spinal cord in all groups. A contusion lesion was made with the NYU-MASCIS impactor by dropping a 10 g rod from heights of 12.5 mm(mild), 25 mm(moderate) and 50 mm(severe) upon the exposed dorsal surface of the spinal cord. Tau protein levels were measured in serum and cerebrospinal fluid samples at 1, 6, 12, 24 hours, 3, 7, 14 and 28 days after operation. Locomotor function of all rats was assessed using the Basso, Beattie and Bresnahan locomotor rating scale. Tau protein concentration in the three spinal cord injury groups(both in serum and cerebrospinal fluid) rapidly increased and peaked at 12 hours after spinal cord injury. Statistically significant positive linear correlations were found between tau protein level and spinal cord injury severity in the three spinal cord injury groups, and between the tau protein level and Basso, Beattie, and Bresnahan locomotor rating scale scores. The tau protein level at 12 hours in the three spinal cord injury groups was negatively correlated with Basso, Beattie, and Bresnahan locomotor rating scale scores at 28 days(serum: r =-0.94; cerebrospinal fluid: r =-0.95). Our data suggest that tau protein levels in serum and cerebrospinal fluid might be a promising biomarker for predicting the severity and functional outcome of traumatic spinal cord injury.
引文
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Breuzard G,Hubert P,Nouar R,De Bessa T,Devred F,Barbier P,Sturgis JN,Peyrot V(2013)Molecular mechanisms of Tau binding to microtubules and its role in microtubule dynamics in live cells.J Cell Sci 126:2810-2819.
Buongiorno M,Compta Y,Marti MJ(2011)Amyloid-beta and tau biomarkers in Parkinson’s disease-dementia.J Neurol Sci 310:25-30.
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.J Clin Neurosci 15:541-544.
Caprelli MT,Mothe AJ,Tator CH(2017)CNS injury:posttranslational modification of the tau protein as a biomarker.Neuroscientist doi:10.1177/1073858417742125.
Caprelli MT,Mothe AJ,Tator CH(2018)Hyperphosphorylated Tau as a novel biomarker for traumatic axonal injury in the spinal cord.JNeurotrauma 35:1929-1941.
Chen CX,Huang J,Tu GQ,Lu JT,Xie X,Zhao B,Wu M,Shi QJ,Fang SH,Wei EQ,Zhang WP,Lu YB(2017)NAMPT inhibitor protects ischemic neuronal injury in rat brain via anti-neuroinflammation.Neuroscience 356:193-206.
Cheran S,Shanmuganathan K,Zhuo J,Mirvis SE,Aarabi B,Alexander MT,Gullapalli RP(2011)Correlation of MR diffusion tensor imaging parameters with ASIA motor scores in hemorrhagic and nonhemorrhagic acute spinal cord injury.J Neurotrauma 28:1881-1892.
Cruz SA,Qin Z,Stewart AFR,Chen HH(2018)Dabrafenib,an inhibitor of RIP3 kinase-dependent necroptosis,reduces ischemic brain injury.Neural Regen Res 13:252-256.
Duan HQ,Wu QL,Yao X,Fan BY,Shi HY,Zhao CX,Zhang Y,Li B,Sun C,Kong XH,Zhou XF,Feng SQ(2018)Nafamostat mesilate attenuates inflammation and apoptosis and promotes locomotor recovery after spinal cord injury.CNS Neurosci Ther 24:429-438.
Fan YD,Zhu ML,Geng D,Zhou K,Du GJ,Wang ZL(2018)The study on pathological mechanism and solution method for spinal cord ischemia reperfusion injury.Eur Rev Med Pharmacol Sci 22:4063-4068.
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Fu H,Hu D,Zhang L,Shen X,Tang P(2018)Efficacy of oligodendrocyte progenitor cell transplantation in rat models with traumatic thoracic spinal cord injury:a systematic review and meta-analysis.JNeurotrauma doi:10.1089/neu.2017.5606.
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Kim JE,Lee YJ,Kwak MH,Jun G,Koh EK,Song SH,Seong JE,Kim JW,Kim KB,Kim S,Hwang DY(2014)Metabolomics approach to serum biomarker for loperamide-induced constipation in SD rats.Lab Anim Res 30:35-43.
Ko WK,Kim SJ,Jo MJ,Choi H,Lee D,Kwon IK,Lee SH,Han IB,Sohn S(2018)Ursodeoxycholic acid inhibits inflammatory responses and promotes functional recovery after spinal cord injury in rats.Mol Neurobiol doi:10.1007/s12035-018-0994-z.
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Li Q,Zhao X,Gong DH,Geng YM,Zhang HL,Bi PX(2017)Sleep disorders of acute thalamic stroke and its influence on plasma IL-17.JBiol Regul Homeost Agents 31:745-751.
Liliang PC,Liang CL,Weng HC,Lu K,Wang KW,Chen HJ,Chuang JH(2010a)Tau proteins in serum predict outcome after severe traumatic brain injury.J Surg Res 160:302-307.
Liliang PC,Liang CL,Lu K,Wang KW,Weng HC,Hsieh CH,Tsai YD,Chen HJ(2010b)Relationship between injury severity and serum tau protein levels in traumatic brain injured rats.Resuscitation 81:1205-1208.
Magnoni S,Esparza TJ,Conte V,Carbonara M,Carrabba G,Holtzman DM,Zipfel GJ,Stocchetti N,Brody DL(2012)Tau elevations in the brain extracellular space correlate with reduced amyloid-beta levels and predict adverse clinical outcomes after severe traumatic brain injury.Brain 135:1268-1280.
Mukaetova-Ladinska EB,Abdell-All Z,Andrade J,da Silva JA,Boksha I,Burbaeva G,Kalaria RN,J TOB(2018)Platelet tau protein as a potential peripheral biomarker in Alzheimer’s disease:an explorative study.Curr Alzheimer Res 15:800-808.
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Qi ZP,Wang GX,Xia P,Hou TT,Zhou HL,Wang TJ,Yang XY(2016)Effects of microtubule-associated protein tau expression on neural stem cell migration after spinal cord injury.Neural Regen Res11:332-337.
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Barbagallo M,Vitaliti G,Greco F,Pavone P,Matin N,Panta G,Lubrano R,Falsaperla R(2017)Idiopathic intracranial hypertension in a paediatric population:a retrospective observational study on epidemiology,symptoms and treatment.J Biol Regul Homeost Agents 31:195-200.
Basso DM,Beattie MS,Bresnahan JC(1995)A sensitive and reliable locomotor rating scale for open field testing in rats.J Neurotrauma12:1-21.
Bitsch A,Horn C,Kemmling Y,Seipelt M,Hellenbrand U,Stiefel M,Ciesielczyk B,Cepek L,Bahn E,Ratzka P,Prange H,Otto M(2002)Serum tau protein level as a marker of axonal damage in acute ischemic stroke.Eur Neurol 47:45-51.
Brettschneider J,Maier M,Arda S,Claus A,Sussmuth SD,Kassubek J,Tumani H(2005)Tau protein level in cerebrospinal fluid is increased in patients with early multiple sclerosis.Mult Scler 11:261-265.
Breuzard G,Hubert P,Nouar R,De Bessa T,Devred F,Barbier P,Sturgis JN,Peyrot V(2013)Molecular mechanisms of Tau binding to microtubules and its role in microtubule dynamics in live cells.J Cell Sci 126:2810-2819.
Buongiorno M,Compta Y,Marti MJ(2011)Amyloid-beta and tau biomarkers in Parkinson’s disease-dementia.J Neurol Sci 310:25-30.
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.J Clin Neurosci 15:541-544.
Caprelli MT,Mothe AJ,Tator CH(2017)CNS injury:posttranslational modification of the tau protein as a biomarker.Neuroscientist doi:10.1177/1073858417742125.
Caprelli MT,Mothe AJ,Tator CH(2018)Hyperphosphorylated Tau as a novel biomarker for traumatic axonal injury in the spinal cord.JNeurotrauma 35:1929-1941.
Chen CX,Huang J,Tu GQ,Lu JT,Xie X,Zhao B,Wu M,Shi QJ,Fang SH,Wei EQ,Zhang WP,Lu YB(2017)NAMPT inhibitor protects ischemic neuronal injury in rat brain via anti-neuroinflammation.Neuroscience 356:193-206.
Cheran S,Shanmuganathan K,Zhuo J,Mirvis SE,Aarabi B,Alexander MT,Gullapalli RP(2011)Correlation of MR diffusion tensor imaging parameters with ASIA motor scores in hemorrhagic and nonhemorrhagic acute spinal cord injury.J Neurotrauma 28:1881-1892.
Cruz SA,Qin Z,Stewart AFR,Chen HH(2018)Dabrafenib,an inhibitor of RIP3 kinase-dependent necroptosis,reduces ischemic brain injury.Neural Regen Res 13:252-256.
Duan HQ,Wu QL,Yao X,Fan BY,Shi HY,Zhao CX,Zhang Y,Li B,Sun C,Kong XH,Zhou XF,Feng SQ(2018)Nafamostat mesilate attenuates inflammation and apoptosis and promotes locomotor recovery after spinal cord injury.CNS Neurosci Ther 24:429-438.
Fan YD,Zhu ML,Geng D,Zhou K,Du GJ,Wang ZL(2018)The study on pathological mechanism and solution method for spinal cord ischemia reperfusion injury.Eur Rev Med Pharmacol Sci 22:4063-4068.
Feng HL,Dang HZ,Fan H,Chen XP,Rao YX,Ren Y,Yang JD,Shi J,Wang PW,Tian JZ(2016)Curcumin ameliorates insulin signalling pathway in brain of Alzheimer’s disease transgenic mice.Int J Immunopathol Pharmacol 29:734-741.
Fu H,Hu D,Zhang L,Shen X,Tang P(2018)Efficacy of oligodendrocyte progenitor cell transplantation in rat models with traumatic thoracic spinal cord injury:a systematic review and meta-analysis.JNeurotrauma doi:10.1089/neu.2017.5606.
Gu M,Gao Z,Li X,Guo L,Lu T,Li Y,He X(2017)Conditioned medium of olfactory ensheathing cells promotes the functional recovery and axonal regeneration after contusive spinal cord injury.Brain Res1654:43-54.
Guo T,Noble W,Hanger DP(2017)Roles of tau protein in health and disease.Acta Neuropathol 133:665-704.
Hachisuka S,Kamei N,Ujigo S,Miyaki S,Yasunaga Y,Ochi M(2014)Circulating microRNAs as biomarkers for evaluating the severity of acute spinal cord injury.Spinal Cord 52:596-600.
Hulme CH,Brown SJ,Fuller HR,Riddell J,Osman A,Chowdhury J,Kumar N,Johnson WE,Wright KT(2017)The developing landscape of diagnostic and prognostic biomarkers for spinal cord injury in cerebrospinal fluid and blood.Spinal Cord 55:114-125.
Jain NB,Ayers GD,Peterson EN,Harris MB,Morse L,O’Connor KC,Garshick E(2015)Traumatic spinal cord injury in the United States,1993-2012.JAMA 313:2236-2243.
Jazayeri SB,Beygi S,Shokraneh F,Hagen EM,Rahimi-Movaghar V(2015)Incidence of traumatic spinal cord injury worldwide:a systematic review.Eur Spine J 24:905-918.
Josephs KA(2017)Current understanding of neurodegenerative diseases associated with the protein Tau.Mayo Clin Proc 92:1291-1303.
Kim JE,Lee YJ,Kwak MH,Jun G,Koh EK,Song SH,Seong JE,Kim JW,Kim KB,Kim S,Hwang DY(2014)Metabolomics approach to serum biomarker for loperamide-induced constipation in SD rats.Lab Anim Res 30:35-43.
Ko WK,Kim SJ,Jo MJ,Choi H,Lee D,Kwon IK,Lee SH,Han IB,Sohn S(2018)Ursodeoxycholic acid inhibits inflammatory responses and promotes functional recovery after spinal cord injury in rats.Mol Neurobiol doi:10.1007/s12035-018-0994-z.
Krishna V,Andrews H,Varma A,Mintzer J,Kindy MS,Guest J(2014)Spinal cord injury:how can we improve the classification and quantification of its severity and prognosis?J Neurotrauma 31:215-227.
Kuhle J,Gaiottino J,Leppert D,Petzold A,Bestwick JP,Malaspina A,Lu CH,Dobson R,Disanto G,Norgren N,Nissim A,Kappos L,Hurlbert J,Yong VW,Giovannoni G,Casha S(2015)Serum neurofilament light chain is a biomarker of human spinal cord injury severity and outcome.J Neurol Neurosurg Psychiatry 86:273-279.
Lee BG,Leavitt MJ,Bernick CB,Leger GC,Rabinovici G,Banks SJ(2018)A Systematic review of positron emission tomography of tau,amyloid beta,and neuroinflammation in chronic traumatic encephalopathy:the evidence to date.J Neurotrauma 35:2015-2024.
Lewczuk P,Esselmann H,Bibl M,Beck G,Maler JM,Otto M,Kornhuber J,Wiltfang J(2004)Tau protein phosphorylated at threonine181 in CSF as a neurochemical biomarker in Alzheimer’s disease:original data and review of the literature.J Mol Neurosci 23:115-122.
Li Q,Zhao X,Gong DH,Geng YM,Zhang HL,Bi PX(2017)Sleep disorders of acute thalamic stroke and its influence on plasma IL-17.JBiol Regul Homeost Agents 31:745-751.
Liliang PC,Liang CL,Weng HC,Lu K,Wang KW,Chen HJ,Chuang JH(2010a)Tau proteins in serum predict outcome after severe traumatic brain injury.J Surg Res 160:302-307.
Liliang PC,Liang CL,Lu K,Wang KW,Weng HC,Hsieh CH,Tsai YD,Chen HJ(2010b)Relationship between injury severity and serum tau protein levels in traumatic brain injured rats.Resuscitation 81:1205-1208.
Magnoni S,Esparza TJ,Conte V,Carbonara M,Carrabba G,Holtzman DM,Zipfel GJ,Stocchetti N,Brody DL(2012)Tau elevations in the brain extracellular space correlate with reduced amyloid-beta levels and predict adverse clinical outcomes after severe traumatic brain injury.Brain 135:1268-1280.
Mukaetova-Ladinska EB,Abdell-All Z,Andrade J,da Silva JA,Boksha I,Burbaeva G,Kalaria RN,J TOB(2018)Platelet tau protein as a potential peripheral biomarker in Alzheimer’s disease:an explorative study.Curr Alzheimer Res 15:800-808.
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 52:428-433.
Qi ZP,Wang GX,Xia P,Hou TT,Zhou HL,Wang TJ,Yang XY(2016)Effects of microtubule-associated protein tau expression on neural stem cell migration after spinal cord injury.Neural Regen Res11:332-337.
Rink S,Arnold D,Wohler A,Bendella H,Meyer C,Manthou M,Papamitsou T,Sarikcioglu L,Angelov DN(2018)Recovery after spinal cord injury by modulation of the proteoglycan receptor PTPsigma.Exp Neurol 309:148-159.
Roerig A,Carlson R,Tipold A,Stein VM(2013)Cerebrospinal fluid tau protein as a biomarker for severity of spinal cord injury in dogs with intervertebral disc herniation.Vet J 197:253-258.
Rong W,Pan YW,Cai X,Song F,Zhao Z,Xiao SH,Zhang C(2017)The mechanism of Naringin-enhanced remyelination after spinal cord injury.Neural Regen Res 12:470-477.
Sabour H,Latifi S,Soltani Z,Shakeri H,Norouzi Javidan A,Ghodsi SM,Hadian MR,Emami Razavi SH(2017)C-reactive protein as an available biomarker determining mental component of health-related quality of life among individuals with spinal cord injury.J Spinal Cord Med 40:329-337.
Segal MB(1993)Extracellular and cerebrospinal fluids.J Inherit Metab Dis 16:617-638.
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