Neuronal response to high rate shear deformation depends on heterogeneity of the local strain field

Journal of Neurotrauma

Volumn 23, Issue 9, 2006, Pages 1304-1319

  Cullen, D Kacy ^a   LaPlaca, Michelle C ^a,b  

^a Emory University   (United States)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Cell mechanics; Neuron; Shear strain, strain rate; Traumatic brain injury

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOMECHANICS; BRAIN CELL; CELL INTERACTION; CELL STRAIN; CELL STRUCTURE; CELL VIABILITY; COMPRESSIVE STRENGTH; CONTROLLED STUDY; EMBRYO; EXTRACELLULAR MATRIX; MECHANICAL STRESS; NERVE CELL CULTURE; NERVE CELL LESION; NEUROPATHOLOGY; NONHUMAN; PATHOPHYSIOLOGY; PHYSICAL STRESS; RAT; SHEAR RATE; SHEAR STRENGTH; TENSILE STRENGTH; TRAUMATIC BRAIN INJURY; ANIMAL; BIOLOGICAL MODEL; BRAIN INJURY; CELL SURVIVAL; COMPUTER SIMULATION; CULTURE TECHNIQUE; NERVE CELL; PATHOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

BIOMATRIX PREPARATION; LAMININ;

ANIMALS; BRAIN INJURIES; CELL CULTURE TECHNIQUES; CELL SURVIVAL; COMPUTER SIMULATION; LAMININ; MODELS, NEUROLOGICAL; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; SHEAR STRENGTH; STRESS, MECHANICAL;

EID: 33947667827     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2006.23.1304     Document Type: Article

References (52)

1. ADAMCHIK, Y., FRANTSEVA, M.V., WEISSPAPIR, M., CARLEN, P.L., and PEREZ VELAZQUEZ, J.L. (2000). Methods to induce primary and secondary traumatic damage in organotypic hippocampal slice cultures. Brain Res. Brain Res. Protoc. 5, 153-158.
2. AHMED, S.M., RZIGALINSKI, B.A., WILLOUGHBY, K.A., SITTERDING, H.A., and ELLIS, E.F. (2000). Stretch-induced injury alters mitochondrial membrane potential and cellular ATP in cultured astrocytes and neurons. J. Neurochem. 74, 1951-1960.
3. BALGUDE, A.P., YU, X., SZYMANSKI, A., and BELLAMKONDA, R.V. (2001). Agarose gel stiffness determines rate of DRG neurite extension in 3D cultures. Biomaterials 22, 1077-1084.
4. BARBEE, K.A., MACARAK, E.J., and THIBAULT, L.E. (1994). Strain measurements in cultured vascular smooth muscle cells subjected to mechanical deformation. Ann. Biomed. Eng. 22, 14-22.
5. BINDER, L.I., FRANKFURTER, A., and REBHUN, L.I. (1985). The distribution of tau in the mammalian central nervous system. J. Cell Biol. 101, 1371-1378.
6. 2+]i in NG108-15 cells subjected to high strain rate deformation and chemical hypoxia: an in vitro model for neural trauma. J. Neurotrauma 13, 395-407.
7. CUKIERMAN, E., PANKOV, R., STEVENS, D.R., and YAMADA, K.M. (2001). Taking cell-matrix adhesions to the third dimension. Science 294, 1708-1712.
8. CUKIERMAN, E., PANKOV, R., and YAMADA, K.M. (2002). Cell interactions with three-dimensional matrices. Curr. Opin. Cell Biol. 14, 633-639.
9. CULLEN, D.K., SIMON, C.M., and LAPLACA, M.C. (2005). Mechanical induction of degeneration and reactive astrogliosis in three-dimensional neuronal-astrocytic co-cultures. J. Neurotrauma 22, 1250.
10. DARVISH, K.K., and CRANDALL, J.R. (2001). Nonlinear viscoelastic effects in oscillatory shear deformation of brain tissue. Med. Eng. Phys. 23, 633-645.
11. DEBUS, E., WEBER, K., and OSBORN, M. (1983). Monoclonal antibodies specific for glial fibrillary acidic (GFA) protein and for each of the neurofilament triplet polypeptides. Differentiation 25, 193-203.
12. DONNELLY, B.R., and MEDIGE, J. (1997). Shear properties of human brain tissue. J. Biomech. Eng. 119, 423-432.
13. ELLIS, E.F., MCKINNEY, J.S., WILLOUGHBY, K.A., LIANG, S., and POVLISHOCK, J.T. (1995). A new model for rapid stretch-induced injury of cells in culture: characterization of the model using astrocytes. J. Neurotrauma 12, 325-339.
14. GEODES-KLEIN, D.M., SCHIFFMAN, K.B., and MEANEY, D.F. (2006). Mechanisms and consequences of neuronal stretch injury in vitro differ with the model of trauma. J. Neurotrauma 23, 193-204.
15. GEDDES, D.M., and CARGILL, R.S., 2nd. (2001). An in vitro model of neural trauma: device characterization and calcium response to mechanical stretch. J. Biomech. Eng. 123, 247-255.
16. GEDDES, D.M., CARGILL, R.S., 2nd, and LAPLACA, M. C. (2003a). Mechanical stretch to neurons results in a strain rate and magnitude-dependent increase in plasma membrane permeability. J. Neurotrauma 20, 1039-1049.
17. GEDDES, D.M., LAPLACA, M.C., and CARGILL, R.S., 2nd. (2003b). Susceptibility of hippocampal neurons to mechanically induced injury. Exp. Neurol. 184, 420-427.
18. GENNARELLI, T.A. (1993). Mechanisms of brain injury. J. Emerg. Med. 11, S5-S11.
19. GENNARELLI, T.A. (1997). The pathobiology of traumatic brain injury. The Neuroscientist 3, 73-81.
20. GENNARELLI, T.A., THIBAULT, L.E., ADAMS, J.H., GRAHAM, D.I., THOMPSON, C.J., and MARCINCIN, R.P. (1982). Diffuse axonal injury and traumatic coma in the primate. Ann. Neurol. 12, 564-574.
21. GOEDERT, M., CROWTHER, R.A., and GARNER, C.C. (1991). Molecular characterization of microtubule-associated proteins tau and MAP2. Trends Neurosci. 14, 193-199.
22. GRINNELL, F. (2003). Fibroblast biology in three-dimensional collagen matrices. Trends Cell Biol. 13, 264-269.
23. HOLBOURN, A.H.S. (1943). Mechanics of head injury. The Lancet 2, 438-441.
24. LAPLACA, M.C., CULLEN, D.K., MCLOUGHLIN, J.J., and CARGILL, R.S., 2nd. (2005). High rate shear strain of three-dimensional neural cell cultures: a new in vitro traumatic brain injury model. J. Biomech. 38, 1093-1105.
25. LAPLACA, M.C., LEE, V.M., and THIBAULT, L.E. (1997a). An in vitro model of traumatic neuronal injury: loading rate-dependent changes in acute cytosolic calcium and lactate dehydrogenase release. J. Neurotrauma 14, 355-368.
26. LAPLACA, M.C., and THIBAULT, L.E. (1997b). An in vitro traumatic injury model to examine the response of neurons to a hydrodynamically-induced deformation. Ann. Biomed Eng. 25, 665-677.
27. LUSARDI, T.A., RANGAN, J., SUN, D., SMITH, D.H., and MEANEY, D.F. (2004). A device to study the initiation and propagation of calcium transients in cultured neurons after mechanical stretch. Ann. Biomed. Eng. 32, 1546-1558.
28. MARGULIES, S.S., and THIBAULT, L.E. (1989). An analytical model of traumatic diffuse brain injury. J. Biomech. Eng. 111, 241-249.
29. MARGULIES, S.S., and THIBAULT, L.E. (1992). A proposed tolerance criterion for diffuse axonal injury in man. J. Biomech. 25, 917-923.
30. MARGULIES, S.S., THIBAULT, L.E., and GENNARELLI, T.A. (1990). Physical model simulations of brain injury in the primate. J. Biomech. 23, 823-836.
31. MCINTOSH, T.K., SAATMAN, K.E., RAGHUPATHI, R., GRAHAM, D.I., SMITH, D.H., LEE, V.M., and TROJANOWSKI, J.Q. (1998). The Dorothy Russell Memorial Lecture. The molecular and cellular sequelae of experimental traumatic brain injury: pathogenetic mechanisms. Neuropathol. Appl. Neurobiol. 24, 251-267.
32. MEANEY, D.F., SMITH, D.H., SHREIBER, D.I., BAIN, A.C., MILLER, R.T., ROSS, D.T., and GENNARELLI, T.A. (1995). Biomechanical analysis of experimental diffuse axonal injury. J. Neurotrauma 12, 689-694.
33. MIGHELI, A., BUTLER, M., BROWN, K., and SHELANSKI, M.L. (1988). Light and electron microscope localization of the microtubule-associated tau protein in rat brain. J. Neurosci. 8, 1846-1851.
34. MILLER, B.E., MILLER, F.R., and HEPPNER, G.H. (1985). Factors affecting growth and drug sensitivity of mouse mammary tumor lines in collagen gel cultures. Cancer Res. 45, 4200-4205.
35. MORRISON, B., 3rd, MEANEY, D.F., and MCINTOSH, T.K. (1998a). Mechanical characterization of an in vitro device designed to quantitatively injure living brain tissue. Ann. Biomed. Eng. 26, 381-390.
36. MORRISON, B., 3rd, SAATMAN, K.E., MEANEY, D.F., and MCINTOSH, T.K. (1998b). In vitro central nervous system models of mechanically induced trauma: a review. J. Neurotrauma 15, 911-928.
37. NAKAYAMA, Y., AOKI, Y., and NIITSU, H. (2001). Studies on the mechanisms responsible for the formation of focal swellings on neuronal processes using a novel in vitro model of axonal injury. J. Neurotrauma 18, 545-554.
38. NUNEZ, J. (1988). Immature and mature variants of MAP2 and tau proteins and neuronal plasticity. Trends Neurosci. 11, 477-479.
39. PETTUS, E.H., CHRISTMAN, C.W., GIEBEL, M.L., and POVLISHOCK, J.T. (1994). Traumatically induced altered membrane permeability: its relationship to traumatically induced reactive axonal change. J. Neurotrauma 11, 507-522.
40. PETTUS, E.H., and POVLISHOCK, J.T. (1996). Characterization of a distinct set of intra-axonal ultrastructural changes associated with traumatically induced alteration in axolemmal permeability. Brain Res. 722, 1-11.
41. PFISTER, B.J., WEIHS, T.P., BETENBAUGH, M., and BAO, G. (2003). An in vitro uniaxial stretch model for axonal injury. Ann. Biomed. Eng. 31, 589-598.
42. ROBERTS, I., SCHIERHOUT, G., and ALDERSON, P. (1998). Absence of evidence for the effectiveness of five interventions routinely used in the intensive care management of severe head injury: a systematic review. J. Neurol. Neurosurg. Psychiatry 65, 729-733.
43. SAHAY, K.B., MEHROTRA, R., SACHDEVA, U., and BANERJI, A.K. (1992). Elastomechanical characterization of brain tissues. J. Biomech. 25, 319-326.
44. SCHMEICHEL, K.L., and BISSELL, M.J. (2003). Modeling tissue-specific signaling and organ function in three dimensions. J. Cell Sci. 116, 2377-2388.
45. SHUCK, L., and ADVANI, S. (1972). Rheological response of human brain tissue in shear. J. Basic Eng. 94, 905-911.
46. SIEG, F., WAHLE, P., and PAPE, H.C. (1999). Cellular reactivity to mechanical axonal injury in an organotypic in vitro model of neurotrauma. J. Neurotrauma 16, 1197-1213.
47. SINGLETON, R.H., and POVLISHOCK, J.T. (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, 3543-3553.
48. SMITH, D.H., WOLF, J.A., LUSARDI, T.A., LEE, V.M., and MEANEY, D.F. (1999). High tolerance and delayed elastic response of cultured axons to dynamic stretch injury. J. Neurosci. 19, 4263-4269.
49. THBAULT, L.E., and GENNARELLI, T.A. (1989). Biomechanics of diffuse brain injuries. Presented at 10th International Tech. Conference on Experimental Safety Vehicles, DOT, NHTSA.
50. WINSTON, F.K., MACARAK, E.J., GORFIEN, S.F., and THIBAULT, L.E. (1989). A system to reproduce and quantify the biomechanical environment of the cell. J. Appl. Physiol. 67, 397-405.
51. WOLF, J.A., STYS, P.K., LUSARDI, T., MEANEY, D., and SMITH, D.H. (2001). Traumatic axonal injury induces calcium influx modulated by tetrodotoxin- sensitive sodium channels. J. Neurosci. 21, 1923-1930.
52. YAMADA, K.M., PANKOV, R., and CUKIERMAN, E. (2003). Dimensions and dynamics in integrin function. Braz. J. Med. Biol. Res. 36, 959-966.