Increased intracranial pressure after diffuse traumatic brain injury exacerbates neuronal somatic membrane poration but not axonal injury: Evidence for primary intracranial pressure-induced neuronal perturbation

Journal of Cerebral Blood Flow and Metabolism

Volumn 32, Issue 10, 2012, Pages 1919-1932

  Lafrenaye, Audrey D ^a   McGinn, Melissa J ^a   Povlishock, John T ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

animal models; basic science; brain trauma; cathepsin B; intracranial pressure; membrane poration

Indexed keywords

CATHEPSIN B; DNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AXONAL INJURY; BRAIN PERFUSION; CELL COMPARTMENTALIZATION; CELLULAR DISTRIBUTION; CEREBRAL PERFUSION PRESSURE; CONTROLLED STUDY; CYTOSOL; DISEASE ASSOCIATION; DNA DAMAGE; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; INTRACRANIAL HYPERTENSION; INTRACRANIAL PRESSURE; INTRACRANIAL PRESSURE MONITORING; LYSOSOME; MALE; NERVE CELL; NERVE CELL LESION; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; TRAUMATIC BRAIN INJURY;

ANIMALS; AXONS; BRAIN; BRAIN INJURIES; CATHEPSIN B; CELL MEMBRANE; INTRACRANIAL HYPERTENSION; MALE; NEURONS; RATS; RATS, INBRED F344;

EID: 84867063815     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2012.95     Document Type: Article

References (40)

1. Bramlett HM, Dietrich WD (2004) Pathophysiology of cerebral ischemia and brain trauma: similarities and differences. J Cereb Blood Flow Metab 24: 133-50 (Pubitemid 38199107)
2. Bratton SL, Chestnut RM, Ghajar J, McConnell Hammond FF, Harris OA, Hartl R, Manley GT, Nemecek A, Newell DW, Rosenthal G, Schouten J, Shutter L, Timmons SD, Ullman JS, Videtta W, Wilberger JE, Wright DW (2007a) Guidelines for the management of severe traumatic brain injury. IX. Cerebral perfusion thresholds. J Neurotrauma 24(Suppl 1): S59-64. (Information also online at https://www.braintrauma.org/coma-guidelines/)
3. Bratton SL, Chestnut RM, Ghajar J, McConnell Hammond FF, Harris OA, Hartl R, Manley GT, Nemecek A, Newell DW, Rosenthal G, Schouten J, Shutter L, Timmons SD, Ullman JS, Videtta W, Wilberger JE, Wright DW (2007b) Guidelines for the management of severe traumatic brain injury. VI. Indications for intracranial pressure monitoring. J Neurotrauma 24(Suppl 1): S37-44. (Information also online at https://www.braintrauma.org/coma-guidelines/)
4. Choo AM, Liu J, Lam CK, Dvorak M, Tetzlaff W, Oxland TR (2007) Contusion, dislocation, and distraction: primary hemorrhage and membrane permeability in distinct mechanisms of spinal cord injury. J Neurosurg Spine 6: 255-66 (Pubitemid 47066078)
5. Cullen DK, Vernekar VN, LaPlaca MC (2011) Traumainduced plasmalemma disruptions in three-dimensional neural cultures are dependent on strain modality and rate. J Neurotrauma 28: 2219-33
6. Dennis AM, Haselkorn ML, Vagni VA, Garman RH, Janesko-Feldman K, Bayir H, Clark RS, Jenkins LW, Dixon CE, Kochanek PM (2009) Hemorrhagic shock after experimental traumatic brain injury in mice: effect on neuronal death. J Neurotrauma 26: 889-99
7. Dixon CE, Lyeth BG, Povlishock JT, Findling RL, Hamm RJ, Marmarou A, Young HF, Hayes RL (1987) A fluid percussion model of experimental brain injury in the rat. J Neurosurg 67: 110-9 (Pubitemid 17085024)
8. Ellis RC, O'Steen WA, Hayes RL, Nick HS, Wang KK, Anderson DK (2005) Cellular localization and enzymatic activity of cathepsin B after spinal cord injury in the rat. Exp Neurol 193: 19-28 (Pubitemid 40463264)
9. Farkas O, Lifshitz J, Povlishock JT (2006) Mechanoporation induced by diffuse traumatic brain injury: an irreversible or reversible response to injury? J Neurosci 26: 3130-40
10. Geddes DM, Cargill RS, II, LaPlaca MC (2003a) Mechanical stretch to neurons results in a strain rate and magnitudedependent increase in plasma membrane permeability. J Neurotrauma 20: 1039-49 (Pubitemid 37288563)
11. Geddes DM, LaPlaca MC, Cargill RS, II (2003b) Susceptibility of hippocampal neurons to mechanically induced injury. Exp Neurol 184: 420-7 (Pubitemid 37444050)
12. Hesdorffer DC, Ghajar J, Iacono L (2002) Predictors of compliance with the evidence-based guidelines for traumatic brain injury care: a survey of United States trauma centers. J Trauma 52: 1202-9 (Pubitemid 34664403)
13. Hill IE, Preston E, Monette R, MacManus JP (1997) A comparison of cathepsin B processing and distribution during neuronal death in rats following global ischemia or decapitation necrosis. Brain Res 751: 206-16 (Pubitemid 27132550)
14. Kilinc D, Gallo G, Barbee KA (2008) Mechanically-induced membrane poration causes axonal beading and localized cytoskeletal damage. Exp Neurol 212: 422-30
15. Kilinc M, Gursoy-Ozdemir Y, Gurer G, Erdener SE, Erdemli E, Can A, Dalkara T (2010) Lysosomal rupture, necroapoptotic interactions and potential crosstalk between cysteine proteases in neurons shortly after focal ischemia. Neurobiol Dis 40: 293-302
16. Langlois JA, Rutland-Brown W, Wald MM (2006) The epidemiology and impact of traumatic brain injury: a brief overview. J Head Trauma Rehabil 21: 375-8 (Pubitemid 44413110)
17. LaPlaca MC, Prado GR, Cullen D, Simon CM (2009) Plasma membrane damage as a marker of neuronal injury. Conf Proc IEEE Eng Med Biol Soc 2009: 1113-6
18. LaPlaca MC, Thibault LE (1998) Dynamic mechanical deformation of neurons triggers an acute calcium response and cell injury involving the N-methyl-Daspartate glutamate receptor. J Neurosci Res 52: 220-9 (Pubitemid 28186166)
19. Li LM, Timofeev I, Czosnyka M, Hutchinson PJ (2010) Review article: the surgical approach to the management of increased intracranial pressure after traumatic brain injury. Anesth Analg 111: 736-48
20. Lusardi TA, Wolf JA, Putt ME, Smith DH, Meaney DF (2004b) Effect of acute calcium influx after mechanical stretch injury in vitro on the viability of hippocampal neurons. J Neurotrauma 21: 61-72 (Pubitemid 38141803)
21. Marin-Caballos AJ, Murillo-Cabezas F, Cayuela-Dominguez A, Dominguez-Roldan JM, Rincon-Ferrari MD, Valencia-Anguita J, Flores-Cordero JM, Munoz-Sanchez MA (2005) Cerebral perfusion pressure and risk of brain hypoxia in severe head injury: a prospective observational study. Crit Care 9: R670-6
22. Miller JD, Becker DP, Ward JD, Sullivan HG, Adams WE, Rosner MJ (1977) Significance of intracranial hypertension in severe head injury. J Neurosurg 47: 503-16 (Pubitemid 8193896)
23. Mollanji R, Bozanovic-Sosic R, Silver I, Li B, Kim C, Midha R, Johnston M (2001) Intracranial pressure accommodation is impaired by blocking pathways leading to extracranial lymphatics. Am J Physiol Regul Integr Comp Physiol 280: R1573-81
24. Nagai A, Ryu JK, Terashima M, Tanigawa Y, Wakabayashi K, McLarnon JG, Kobayashi S, Masuda J, Kim SU (2005) Neuronal cell death induced by cystatin C in vivo and in cultured human CNS neurons is inhibited with cathepsin B. Brain Res 1066: 120-8 (Pubitemid 41790736)
25. Nagra G, Koh L, Zakharov A, Armstrong D, Johnston M (2006) Quantification of cerebrospinal fluid transport across the cribriform plate into lymphatics in rats. Am J Physiol Regul Integr Comp Physiol 291: R1383-9
26. Navarro JC, Pillai S, Cherian L, Garcia R, Grill RJ, Robertson CS (2012) Histopathological and behavioral effects of immediate and delayed hemorrhagic shock after mild traumatic brain injury in rats. J Neurotrauma 29: 322-34
27. Oberle C, Huai J, Reinheckel T, Tacke M, Rassner M, Ekert PG, Buellesbach J, Borner C (2010) Lysosomal membrane permeabilization and cathepsin release is a Bax/Bak-dependent, amplifying event of apoptosis in fibroblasts and monocytes. Cell Death Differ 17: 1167-78
28. Pratt MR, Sekedat MD, Chiang KP, Muir TW (2009) Direct measurement of cathepsin B activity in the cytosol of apoptotic cells by an activity-based probe. Chem Biol 16: 1001-12
29. Reid WM, Rolfe A, Register D, Levasseur JE, Churn SB, Sun D (2010) Strain-related differences after experimental traumatic brain injury in rats. J Neurotrauma 27: 1243-53
30. Sherriff FE, Bridges LR, Gentleman SM, Sivaloganathan S, Wilson S (1994) Markers of axonal injury in post mortem human brain. Acta Neuropathol 88: 433-9 (Pubitemid 24331029)
31. Singleton RH, Povlishock JT (2004) Identification and characterization of heterogeneous neuronal injury and death in regions of diffuse brain injury: evidence for multiple independent injury phenotypes. J Neurosci 24: 3543-53 (Pubitemid 38481111)
32. Stone JR, Singleton RH, Povlishock JT (2000) Antibodies to the C-terminus of the beta-amyloid precursor protein (APP): a site specific marker for the detection of traumatic axonal injury. Brain Res 871: 288-302 (Pubitemid 30433880)
33. Sullivan HG, Martinez J, Becker DP, Miller JD, Griffith R, Wist AO (1976) Fluid-percussion model of mechanical brain injury in the cat. J Neurosurg 45: 521-34
34. Treggiari MM, Schutz N, Yanez ND, Romand JA (2007) Role of intracranial pressure values and patterns in predicting outcome in traumatic brain injury: a systematic review. Neurocrit Care 6: 104-12 (Pubitemid 46934020)
35. Wang JY, Xia Q, Chu KT, Pan J, Sun LN, Zeng B, Zhu YJ, Wang Q, Wang K, Luo BY (2011) Severe global cerebral ischemia-induced programmed necrosis of hippocampal CA1 neurons in rat is prevented by 3-methyladenine: a widely used inhibitor of autophagy. J Neuropathol Exp Neurol 70: 314-22
36. Whalen MJ, Dalkara T, You Z, Qiu J, Bermpohl D, Mehta N, Suter B, Bhide PG, Lo EH, Ericsson M, Moskowitz MA (2008) Acute plasmalemma permeability and protracted clearance of injured cells after controlled cortical impact in mice. J Cereb Blood Flow Metab 28: 490-505 (Pubitemid 351304258)
37. Yacoub A, Park MA, Hanna D, Hong Y, Mitchell C, Pandya AP, Harada H, Powis G, Chen CS, Koumenis C, Grant S, Dent P (2006) OSU-03012 promotes caspase-independent but PERK-, cathepsin B-, BID-, and AIF-dependent killing of transformed cells. Mol Pharmacol 70: 589-603 (Pubitemid 44092320)
38. Yamakami I, McIntosh TK (1991) Alterations in regional cerebral blood flow following brain injury in the rat. J Cereb Blood Flow Metab 11: 655-60
39. Yoshida M, Yamashima T, Zhao L, Tsuchiya K, Kohda Y, Tonchev AB, Matsuda M, Kominami E (2002) Primate neurons show different vulnerability to transient ischemia and response to cathepsin inhibition. Acta Neuropathol 104: 267-72 (Pubitemid 36075387)
40. Zhang H, Zhong C, Shi L, Guo Y, Fan Z (2009) Granulysin induces cathepsin B release from lysosomes of target tumor cells to attack mitochondria through processing of bid leading to Necroptosis. J Immunol 182: 6993-7000