A novel marker for traumatic brain injury: CSF αII-spectrin breakdown product levels

Journal of Neurotrauma

Volumn 21, Issue 10, 2004, Pages 1443-1456

  Ringger, N C ^a,b   O'Steen, B E ^a,b   Brabham, J G ^a   Silver, X ^b   Pineda, J ^a,b   Wang, K K W ^a,b   Hayes, R L ^a,b   Papa, L ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

Biomarker; CSF; Injury magnitude; Lesion size; S100 ; Spectrin; Tau

Indexed keywords

FODRIN; MARKER; PROTEIN S 100; TAU PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN INJURY; CEREBROSPINAL FLUID; CONTROLLED STUDY; DISEASE SEVERITY; MALE; MOTOR PERFORMANCE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PROTEIN DEGRADATION; RAT;

ANIMALS; BIOLOGICAL MARKERS; BLOTTING, WESTERN; BRAIN; BRAIN INJURIES; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENZYME-LINKED IMMUNOSORBENT ASSAY; MAGNETIC RESONANCE IMAGING; MALE; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; SPECTRIN;

EID: 7244251494     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2004.21.1443     Document Type: Article

References (68)

1. ABRAHA, H.D., BUTTERWORTH, R.J., BATH, P.M., WASSIF, W.S., GARTHWAITE, J., and SHERWOOD, R.A. (1997). Serum S-100 protein, relationship to clinical outcome in acute stroke. Ann. Clin. Biochem. 34, 546-550.
2. ALBENSI, B.C., KNOBLACH, S.M., CHEW, B.G., O'REILLY, M.P., FADEN, A.I., and PEKAR, J.J. (2000). Diffusion and high resolution MRI of traumatic brain injury in rats: time course and correlation with histology. Exp. Neurol. 162, 61-72.
3. ALI, M.S., HARMER, M., and VAUGHAN, R. (2000). Serum S100 protein as a marker of cerebral damage during cardiac surgery. Br. J. Anaesth. 85, 287-298.
4. ANDERSON, R.E., HANSSON, L.O., NILSSON, O., DIJLAIMERZOUG, R., and SETTERGREN, G. (2001). High serum S100B levels for trauma patients without head injuries. Neurosurgery 48, 1255-1260.
5. ASSAF, Y., BEIT-YANNAI, E., SHOHAMI, E., BERMAN, E., and COHEN, Y. (1997). Diffusion- and T2-weighted MRI of closed-head injury in rats: a time course study and correlation with histology. Magn. Reson. Imaging 15, 77-85.
6. AURELL, A., ROSENGREN, L.E., KARLSSON, B., OLSSON, J.E., ZBORNIKOVA, V., and HAGLID, K.G. (1991). Determination of S-100 and glial fibrillary acidic protein concentrations in cerebrospinal fluid after brain infarction. Stroke 22, 1254-1258.
7. BANIK, N.L., SHIELDS, D.C., RAY, S., et al. (1998). Role of calpain in spinal cord injury: effects of calpain and free radical inhibitors. Ann. NY Acad. Sci. 844, 131-137.
8. BARTUS, R.T., DEAN, R.L., MENNERICK, S., EVELETH, D., and LYNCH, G. (1998). Temporal ordering of pathogenic events following transient global ischemia. Brain Res. 790, 1-13.
9. BARTUS, R.T., ELLIOTT, P.J., HAYWARD, N.J., et al. (1995). Calpain as a novel target for treating acute neurodegenerative disorders. Neurol. Res. 17, 249-258.
10. BARTUS, R.T., HAYWARD, N.J., ELLIOTT, P.J., et al. (1994). Calpain inhibitor AK295 protects neurons from focal brain ischemia. Effects of postocclusion intra-arterial administration. Stroke 25, 2265-2270.
11. BITSCH, A., HORN, C., KEMMLING, Y., et al. (2002). Serum tau protein level as a marker of axonal damage in acute ischemic stroke. Eur. Neurol. 47, 45-51.
12. BUDUHAN, G., and McRITCHIE, D.I. (2000). Missed injuries in patients with multiple trauma. J. Trauma 49, 600-605.
13. BUKI, A., FARKAS, O., DOCZI, T., and POVLISHOCK, J.T. (2003). Preinjury administration of the calpain inhibitor MDL-28170 attenuates traumatically induced axonal injury. J. Neurotrauma 20, 261-268.
14. BUTTNER, T., WEYERS, S., POSTERT, T., SPRENGELMEYER, R., and KUHN, W. (1997). S-100 protein: serum marker of focal brain damage after ischemic territorial MCA infarction. Stroke 28, 1961-1965.
15. CHATFIELD, D.A., ZEMLAN, F.P., DAY, D.J., and MENON, D.K. (2002). Discordant temporal patterns of S100beta and cleaved tau protein elevation after head injury: a pilot study. Br. J. Neurosurg. 16, 471-476.
16. CHERIAN, L., ROBERTSON, C.S., CONTANT, C.F., JR., and BRYAN, R.M., JR. (1994). Lateral cortical impact injury in rats: cerebrovascular effects of varying depth of cortical deformation and impact velocity. J. Neurotrauma 11, 573-585.
17. DIXON, C.E., CLIFTON, G.L., LIGHTHALL, J.W., YAGHMAI, A.A., and HAYES, R.L. (1991). A controlled cortical impact model of traumatic brain injury in the rat. J. Neurosci. Methods 39, 253-262.
18. ELTING, J.W., DE JAGER, A.E., TEELKEN, A.W., et al. (2000). Comparison of serum S-100 protein levels following stroke and traumatic brain injury. J. Neurol. Sci. 181, 104-110.
19. 45Ca autoradiographic study. Brain Res. 624, 94-102.
20. FRANZ, G., BEER, R., KAMPFL, A., et al. (2003). Amyloid beta 1-42 and tau in cerebrospinal fluid after severe traumatic brain injury. Neurology 60, 1457-1461.
21. GARCIA, M.L., and CLEVELAND, D.W. (2001). Going new places using an old MAP: tau, microtubules and human neurodegenerative disease. Curr. Opin. Cell Biol. 13, 41-48.
22. GOODMAN, J.C., CHERIAN, L., BRYAN, R.M., JR., and ROBERTSON, C.S. (1994). Lateral cortical impact injury in rats: pathologic effects of varying cortical compression and impact velocity. J. Neurotrauma 11, 587-597.
23. HAMM, R.J., PIKE, B.R., O'DELL, D.M., LYETH, B.G., and JENKINS, L.W. (1994). The rotarod test: an evaluation of its effectiveness in assessing motor deficits following traumatic brain injury. J. Neurotrauma 11, 187-196.
24. HANLON, R.E., DEMERY, J.A., MARTINOVICH, Z., and KELLY, J.P. (1999). Effects of acute injury characteristics on neurophysical status and vocational outcome following mild traumatic brain injury. Brain Inj. 13, 873-887.
25. HANS, V.H., KOSSMANN, T., LENZLINGER, P.M., et al. (1999). Experimental axonal injury triggers interleukin-6 mRNA, protein synthesis and release into cerebrospinal fluid. J. Cereb. Blood Flow Metab. 19, 184-194.
26. HARAD, F.T., and KERSTEIN, M.D. (1992). Inadequacy of bedside clinical indicators in identifying significant intracranial injury in trauma patients. J. Trauma 32, 359-363.
27. HERRMANN, M., CURIO, N., JOST, S., et al. (2001). Release of biochemical markers of damage to neuronal and glial brain tissue is associated with short- and long-term neuropsychological outcome after traumatic brain injury. J. Neurol. Neurosurg. Psychiatry 70, 95-100.
28. HERRMANN, M., EBERT, A.D., TOBER, D., KANN, J., and HUTH, C. (1999). A contrastive analysis of release patterns of biochemical markers of brain damage after coronary artery bypass grafting and valve replacement and their association with the neurobehavioral outcome after cardiac surgery. Eur. J. Cardiothorac Surg. 16, 513-518.
29. HERRMANN, M., JOST, S., KUTZ, S., et al. (2000). Temporal profile of release of neurobiochemical markers of brain damage after traumatic brain injury is associated with intracranial pathology as demonstrated in cranial computerized tomography. J. Neurotrauma 17, 113-122.
30. HESSE, C., ROSENGREN, L., ANDREASEN, N., et al. (2001). Transient increase in total tau but not phospho-tau in human cerebrospinal fluid after acute stroke. Neurosci. Lett. 297, 187-190.
31. HILL, M.D., JACKOWSKI, G., BAYER, N., LAWRENCE, M., and JAESCHKE, R. (2000). Biochemical markers in acute ischemic stroke. CMAJ 162, 1139-1140.
32. HONG, S.C., GOTO, Y., LANZINO, G., SOLEAU, S., KASSELL, N.F., and LEE, K.S. (1994). Neuroprotection with a calpain inhibitor in a model of focal cerebral ischemia. Stroke 25, 663-669.
33. INGEBRIGTSEN, T., and ROMNER, B. (2002). Biochemical serum markers of traumatic brain injury. J. Trauma 52, 798-808.
34. JACKSON, R.G., SAMRA, G.S., RADCLIFFE, J., CLARK, G.H., and PRICE, C.P. (2000). The early fall in levels of S-100 beta in traumatic brain injury. Clin. Chem. Lab. Med. 38, 1165-1167.
35. KELLY, D.F. (1995). Alcohol and head injury: an issue revisited. J. Neurotrauma 12, 883-890.
36. KIDO, D.K., COX, C., HAMILL, R.W., ROTHENBERG, B.M., and WOOLF, P.D. (1992). Traumatic brain injuries: predictive usefulness of CT. Radiology 182, 777-781.
37. KURTH, S.M., BIGLER, E.D., and BLATTER, D.D. (1994). Neuropsychological outcome and quantitative image analysis of acute haemorrhage in traumatic brain injury: preliminary findings. Brain Inj. 8, 489-500.
38. MARKGRAF, C.G., VELAYO, N.L., JOHNSON, M.P., et al. (1998). Six-hour window of opportunity for calpain inhibition in focal cerebral ischemia in rats. Stroke 29, 152-158.
39. MCKEATING, E.G., ANDREWS, P.J., and MASCIA, L. (1998). Relationship of neuron specific enolase and protein S-100 concentrations in systemic and jugular venous serum to injury severity and outcome after traumatic brain injury. Acta Neurochir. Suppl. (Wien) 71, 117-119.
40. MIRSKI, M.A., MUFFELMAN, B., ULATOWSKL J.A., and HANLEY, D.F. (1995). Sedation for the critically ill neurologic patient. Crit. Care Med. 23, 2038-2053.
41. 45Ca accumulation in rat brain after closed head injury; attenuation by the novel neuroprotective agent HU-211. Brain Res. 685, 1-11.
42. NATH, R., RASER, K.J., STAFFORD, D., et al. (1996). Non-erythroid alpha-spectrin breakdown by calpain and interleukin 1 beta-converting-enzyme- like protease(s) in apoptotic cells: contributory roles of both protease families in neuronal apoptosis. Biochem J. 319, Pt 3, 683-690.
43. NEUMANN-HAEFELIN, T., KASTRUP, A., DE CRESPIGNY, A., et al. (2000). Serial MRI after transient focal cerebral ischemia in rats: dynamics of tissue injury, blood-brain barrier damage, and edema formation. Stroke 31, 1965-1973.
44. NEWCOMB, J.K., KAMPFL, A., POSMANTUR, R.M., et al. (1997). Immunohistochemical study of calpain-mediated breakdown products to alpha-spectrin following controlled cortical impact injury in the rat. J. Neurotrauma 14, 369-383.
45. PALMER, G.C., PEELING, J., CORBETT, D., DEL BIGIO, M.R., and HUDZIK, T.J. (2001). T2-weighted MRI correlates with long-term histopathology, neurology scores, and skilled motor behavior in a rat stroke model. Ann. NY Acad. Sci. 939, 283-296.
46. PETZOLD, A., KEIR, G., LIM, D., SMITH., M, and THOMPSON, E.J., (2003). Cerebrospinal fluid (CSF) and serum S100B: release and washout pattern. Brain Res. Bull. 61, 281-285.
47. PIKE, B.R., FLINT, J., DAVE, J.R., et al. (2004). Accumulation of calpain and caspase-3 proteolytic fragments of brain-derived alphaII-spectrin in cerebral spinal fluid after middle cerebral artery occlusion in rats. J. Cereb. Blood Flow Metab. 24, 98-106.
48. PIKE, B.R., FLINT, J., DUTTA, S., JOHNSON, E., WANG, K.K., and HAYES, R.L. (2001). Accumulation of non-erythroid alpha II-spectrin and calpain-cleaved alpha II-spectrin breakdown products in cerebrospinal fluid after traumatic brain injury in rats. J. Neurochem. 78, 1297-1306.
49. PIKE, B.R., ZHAO, X., NEWCOMB, J.K., POSMANTUR, R.M., WANG, K.K., and HAYES, R.L. (1998). Regional calpain and caspase-3 proteolysis of alpha-spectrin after traumatic brain injury. Neuroreport 9, 2437-2442.
50. RAABE, A., GROLMS, C., KELLER, M., DOHNERT, J., SORGE, O., and SEIFERT, V. (1998). Correlation of computed tomography findings and serum brain damage markers following severe head injury. Acta Neurochir. (Wien) 140, 787-792.
51. RAABE, A., and SEIFERT, V. (2000). Protein S-100B as a serum marker of brain damage in severe head injury: preliminary results. Neurosurg. Rev. 23, 136-138.
52. REISER, H. (2003). Proteins in cerebrospinal fluid and blood: barriers, CSF flow rate and source-related dynamics. Restor. Neurol. Neurosci. 21, 79-96.
53. REISER, H., and PETER, J.B. (2001). Cerebrospinal fluid analysis: disease-related data patterns and evaluation programs. J. Neurol. Sci. 184, 101-122.
54. ROBERTS-LEWIS, J.M., SAVAGE, M.J., MARCY, V.R., PINSKER, L.R., and SIMAN, R. (1994). Immunolocalization of calpain I-mediated spectrin degradation to vulnerable neurons in the ischemic gerbil brain. J. Neurosci. 14, 3934-3944.
55. RINGGER, N.C., TOLENTINO, P.J., McKINSEY, D.M., PIKE, B.R., WANG, K.K.W., and HAYES, R.L. (2004). Effects of injury severity on regional and temporal mRNA expression levels of calpains and caspases after traumatic brain injury in rats. J. Neurotrauma 21, 829-841.
56. ROTHOERL, R.D., WOERTGEN, C., and BRAWANSKI, A. (2000). S-100 serum levels and outcome after severe head injury. Acta Neurochir. Suppl. 76, 97-100.
57. SAATMAN, K.E., BOZYCZKO-COYNE, D., MARCY, V., SIMAN, R., and McINTOSH, T.K. (1996a). Prolonged calpain-mediated spectrin breakdown occurs regionally following experimental brain injury in the rat. J. Neuropathol. Exp. Neurol. 55, 850-860.
58. SAATMAN, K.E., MURAI, H., BARTUS, R.T., et al. (1996b). Calpain inhibitor AK295 attenuates motor and cognitive deficits following experimental brain injury in the rat. Proc. Natl. Acad. Sci. USA 93, 3428-3433.
59. SAIDO, T.C., YOKOTA, M., NAGAO, S., et al. (1993). Spatial resolution of fodrin proteolysis in postischemic brain. J. Biol. Chem. 268, 25239-25243.
60. SHAW, G.J., JAUCH, E.C., and ZEMLAN, F.P. (2002). Serum cleaved tau protein levels and clinical outcome in adult patients with closed head injury. Ann. Emerg. Med. 39, 254-257.
61. VERWEIJ, B.H., MUIZELAAR, J.P., VINAS, F.C., PETERSON, P.L., XIONG, Y., and LEE, C.P. (1997). Mitochondria! dysfunction after experimental and human brain injury and its possible reversal with a selective N-type calcium channel antagonist (SNX-111). Neurol. Res. 19, 334-339.
62. WANG, K.K. (2000). Calpain and caspase: can you tell the difference? Trends Neurosci. 23, 59.
63. WANG, K.K., POSMANTUR, R., NATH, R., et al. (1998). Simultaneous degradation of alpha-II- and beta-II-spectrin by caspase 3 (CPP32) in apoptotic cells. J. Biol. Chem. 273, 22490-22497.
64. WILSON, J.T., HADLEY, D.M., WIEDMANN, K.D., and TEASDALE, G.M. (1995). Neuropsychological consequences of two patterns of brain damage shown by MRI in survivors of severe head injury. J. Neurol. Neurosurg. Psychiatry 59, 328-331.
65. XIONG, Y., GU, Q., PETERSON, P.L., MUIZELAAR, J.P., and LEE, C.P. (1997). Mitochondrial dysfunction and calcium perturbation induced by traumatic brain injury. J. Neurotrauma 14, 23-34.
66. ZEMLAN, F.P., JAUCH, E.C., MULCHAHEY, J.J., et al. (2002). C-tau biomarker of neuronal damage in severe brain injured patients: association with elevated intracranial pressure and clinical outcome. Brain Res. 947, 131-139.
67. ZEMLAN, F.P., ROSENBERG, W.S., LUEBBE, P.A., et al. (1999). Quantification of axonal damage in traumatic brain injury: affinity purification and characterization of cerebrospinal fluid tau proteins. J. Neurochem. 72, 741-750.
68. ZINK, B.J. (2001). Traumatic brain injury outcome: concepts for emergency care. Ann. Emerg. Med. 37, 318-332.