Strain rate-dependent induction of reactive astrogliosis and cell death in three-dimensional neuronal-astrocytic co-cultures

Brain Research

Volumn 1158, Issue 1, 2007, Pages 103-115

  Cullen, D Kacy ^a   Simon, Crystal M ^a   LaPlaca, Michelle C ^a  

^a Emory University   (United States)

Author keywords

Astrogliosis; Cell biomechanic; In vitro; Mechanotransduction; Shear strain; TBI

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; PROTEOCHONDROITIN SULFATE; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ARTICLE; ASTROCYTE; ASTROCYTOSIS; CELL DEATH; CELL DENSITY; COCULTURE; CONTROLLED STUDY; EMBRYO; NERVE CELL CULTURE; NERVE CELL NECROSIS; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; RAT; SHEAR STRESS;

ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; CELL CULTURE TECHNIQUES; CELL DEATH; CELLS, CULTURED; CEREBRAL CORTEX; COCULTURE TECHNIQUES; CYTOKINES; EMBRYO; GLIAL FIBRILLARY ACIDIC PROTEIN; IN SITU NICK-END LABELING; MODELS, NEUROLOGICAL; NEURONS; PHYSICAL STIMULATION; RATS; RATS, SPRAGUE-DAWLEY; SHEAR STRENGTH; STRESS, MECHANICAL;

EID: 34447538299     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2007.04.070     Document Type: Article

References (57)

1. Ahmed S.M., Rzigalinski B.A., Willoughby K.A., Sitterding H.A., and Ellis E.F. Stretch-induced injury alters mitochondrial membrane potential and cellular ATP in cultured astrocytes and neurons. J. Neurochem. 74 (2000) 1951-1960
2. Alenghat F.J., and Ingber D.E. Mechanotransduction: all signals point to cytoskeleton, matrix, and integrins. Sci. STKE 2002 (2002) PE6
3. Asher R.A., Morgenstern D.A., Fidler P.S., Adcock K.H., Oohira A., Braistead J.E., Levine J.M., Margolis R.U., Rogers J.H., and Fawcett J.W. Neurocan is upregulated in injured brain and in cytokine-treated astrocytes. J. Neurosci. 20 (2000) 2427-2438
4. Bowman C.L., Ding J.P., Sachs F., and Sokabe M. Mechanotransducing ion channels in astrocytes. Brain Res. 584 (1992) 272-286
5. Bush T.G., Puvanachandra N., Horner C.H., Polito A., Ostenfeld T., Svendsen C.N., Mucke L., Johnson M.H., and Sofroniew M.V. Leukocyte infiltration, neuronal degeneration, and neurite outgrowth after ablation of scar-forming, reactive astrocytes in adult transgenic mice. Neuron 23 (1999) 297-308
6. Cargill II R.S., and Thibault L.E. Acute alterations in [Ca2+]i in NG108-15 cells subjected to high strain rate deformation and chemical hypoxia: an in vitro model for neural trauma. J. Neurotrauma 13 (1996) 395-407
7. Cavalcanti-Adam E.A., Tomakidi P., Bezler M., and Spatz J.P. Geometric organization of the extracellular matrix in the control of integrin-mediated adhesion and cell function in osteoblasts. Prog. Orthod. 6 (2005) 232-237
8. Cervos-Navarro J., and Lafuente J.V. Traumatic brain injuries: structural changes. J. Neurol. Sci. 103 Suppl (1991) S3-S14
9. Cullen D.K., and LaPlaca M.C. Neuronal response to high rate shear deformation depends on heterogeneity of the local strain field. J. Neurotrauma 23 (2006) 1304-1319
10. Debus E., Weber K., and Osborn M. Monoclonal antibodies specific for glial fibrillary acidic (GFA) protein and for each of the neurofilament triplet polypeptides. Differentiation 25 (1983) 193-203
11. Ellis E.F., McKinney J.S., Willoughby K.A., Liang S., and Povlishock J.T. A new model for rapid stretch-induced injury of cells in culture: characterization of the model using astrocytes. J. Neurotrauma 12 (1995) 325-339
12. Etienne-Manneville S., and Hall A. Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKCzeta. Cell 106 (2001) 489-498
13. Fawcett J.W., and Asher R.A. The glial scar and central nervous system repair. Brain Res. Bull. 49 (1999) 377-391
14. Fitch M.T., Doller C., Combs C.K., Landreth G.E., and Silver J. Cellular and molecular mechanisms of glial scarring and progressive cavitation: in vivo and in vitro analysis of inflammation-induced secondary injury after CNS trauma. J. Neurosci. 19 (1999) 8182-8198
15. Floyd C.L., Gorin F.A., and Lyeth B.G. Mechanical strain injury increases intracellular sodium and reverses Na+/Ca2+ exchange in cortical astrocytes. Glia 51 (2005) 35-46
16. Floyd C.L., Rzigalinski B.A., Sitterding H.A., Willoughby K.A., and Ellis E.F. Antagonism of group I metabotropic glutamate receptors and PLC attenuates increases in inositol trisphosphate and reduces reactive gliosis in strain-injured astrocytes. J. Neurotrauma 21 (2004) 205-216
17. Floyd C.L., Rzigalinski B.A., Weber J.T., Sitterding H.A., Willoughby K.A., and Ellis E.F. Traumatic injury of cultured astrocytes alters inositol (1,4,5)-trisphosphate-mediated signaling. Glia 33 (2001) 12-23
18. Franke H., Krugel U., and Illes P. P2 receptor-mediated proliferative effects on astrocytes in vivo. Glia 28 (1999) 190-200
19. Geddes D.M., and Cargill II R.S. An in vitro model of neural trauma: device characterization and calcium response to mechanical stretch. J. Biomech. Eng. 123 (2001) 247-255
20. Gennarelli T.A., Thibault L.E., Adams J.H., Graham D.I., Thompson C.J., and Marcincin R.P. Diffuse axonal injury and traumatic coma in the primate. Ann. Neurol. 12 (1982) 564-574
21. Goussev S., Hsu J.Y., Lin Y., Tjoa T., Maida N., Werb Z., and Noble-Haeusslein L.J. Differential temporal expression of matrix metalloproteinases after spinal cord injury: relationship to revascularization and wound healing. J. Neurosurg. 99 (2003) 188-197
22. Guharay F., and Sachs F. Stretch-activated single ion channel currents in tissue-cultured embryonic chick skeletal muscle. J. Physiol. 352 (1984) 685-701
23. Hamill O.P., and Martinac B. Molecular basis of mechanotransduction in living cells. Physiol. Rev. 81 (2001) 685-740
24. Hatten M.E. Neuronal inhibition of astroglial cell proliferation is membrane mediated. J. Cell Biol. 104 (1987) 1353-1360
25. Ingber D.E. Tensegrity: the architectural basis of cellular mechanotransduction. Annu. Rev. Physiol. 59 (1997) 575-599
26. Janeczko K. Spatiotemporal patterns of the astroglial proliferation in rat brain injured at the postmitotic stage of postnatal development: a combined immunocytochemical and autoradiographic study. Brain Res. 485 (1989) 236-243
27. Kamm R.D., and Kaazempur-Mofrad M.R. On the molecular basis for mechanotransduction. Mech. Chem. Biosyst. 1 (2004) 201-209
28. Katsumi A., Orr A.W., Tzima E., and Schwartz M.A. Integrins in mechanotransduction. J. Biol. Chem. 279 (2004) 12001-12004
29. Kleinman H.K., McGarvey M.L., Hassell J.R., Star V.L., Cannon F.B., Laurie G.W., and Martin G.R. Basement membrane complexes with biological activity. Biochemistry 25 (1986) 312-318
30. Ko K.S., and McCulloch C.A. Intercellular mechanotransduction: cellular circuits that coordinate tissue responses to mechanical loading. Biochem. Biophys. Res. Commun. 285 (2001) 1077-1083
31. LaPlaca M.C., Lee V.M., and Thibault L.E. An in vitro model of traumatic neuronal injury: loading rate-dependent changes in acute cytosolic calcium and lactate dehydrogenase release. J. Neurotrauma 14 (1997) 355-368
32. LaPlaca M.C., Cullen D.K., McLoughlin J.J., and Cargill II R.S. High rate shear strain of three-dimensional neural cell cultures: a new in vitro traumatic brain injury model. J. Biomech. 38 (2005) 1093-1105
33. Li L., Ye Z., and Zhu J. Astrogliosis and basic fibroblast growth factor. Zhonghua Binglixue Zazhi 26 (1997) 8-10
34. Logan A., Berry M., Gonzalez A.M., Frautschy S.A., Sporn M.B., and Baird A. Effects of transforming growth factor beta 1 on scar production in the injured central nervous system of the rat. Eur. J. Neurosci. 6 (1994) 355-363
35. Margulies S.S., and Thibault L.E. An analytical model of traumatic diffuse brain injury. J. Biomech. Eng. 111 (1989) 241-249
36. Margulies S.S., Thibault L.E., and Gennarelli T.A. Physical model simulations of brain injury in the primate. J. Biomech. 23 (1990) 823-836
37. Mathewson A.J., and Berry M. Observations on the astrocyte response to a cerebral stab wound in adult rats. Brain Res. 327 (1985) 61-69
38. McCarthy K.D., and de Vellis J. Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J. Cell Biol. 85 (1980) 890-902
39. McGraw J., Hiebert G.W., and Steeves J.D. Modulating astrogliosis after neurotrauma. J. Neurosci. Res. 63 (2001) 109-115
40. McIntosh T.K., Juhler M., Raghupathi R., Saatman K.E., and Smith D.H. Secondary brain injury: neurochemical and cellular mediators. Trauma. Brain Inj. (1999)
41. McKeon R.J., Hoke A., and Silver J. Injury-induced proteoglycans inhibit the potential for laminin-mediated axon growth on astrocytic scars. Exp. Neurol. 136 (1995) 32-43
42. McKeon R.J., Jurynec M.J., and Buck C.R. The chondroitin sulfate proteoglycans neurocan and phosphacan are expressed by reactive astrocytes in the chronic CNS glial scar. J. Neurosci. 19 (1999) 10778-10788
43. Meaney D.F., Smith D.H., Shreiber D.I., Bain A.C., Miller R.T., Ross D.T., and Gennarelli T.A. Biomechanical analysis of experimental diffuse axonal injury. J. Neurotrauma 12 (1995) 689-694
44. Moon C., Ahn M., Kim S., Jin J.K., Sim K.B., Kim H.M., Lee M.Y., and Shin T. Temporal patterns of the embryonic intermediate filaments nestin and vimentin expression in the cerebral cortex of adult rats after cryoinjury. Brain Res. 1028 (2004) 238-242
45. Moon L.D., and Fawcett J.W. Reduction in CNS scar formation without concomitant increase in axon regeneration following treatment of adult rat brain with a combination of antibodies to TGFbeta1 and beta2. Eur. J. Neurosci. 14 (2001) 1667-1677
46. Morgenstern D.A., Asher R.A., and Fawcett J.W. Chondroitin sulphate proteoglycans in the CNS injury response. Prog. Brain Res. 137 (2002) 313-332
47. Muir J.K., Willoughby K.A., and Ellis E.F. A confocal microscopic examination of the effects of strain (stretch) on cultured neurons and astrocytes. J. Neurotrauma 19 (2002) 1361
48. Neary J.T., Kang Y., Willoughby K.A., and Ellis E.F. Activation of extracellular signal-regulated kinase by stretch-induced injury in astrocytes involves extracellular ATP and P2 purinergic receptors. J. Neurosci. 23 (2003) 2348-2356
49. Neary J.T., Kang Y., Shi Y.F., Tran M.D., and Wanner I.B. P2 receptor signalling, proliferation of astrocytes, and expression of molecules involved in cell-cell interactions. Novartis Found. Symp. 276 (2006) 131-143 (discussion 143-137, 233-137, 275-181)
50. Nishio T., Kawaguchi S., Yamamoto M., Iseda T., Kawasaki T., and Hase T. Tenascin-C regulates proliferation and migration of cultured astrocytes in a scratch wound assay. Neuroscience 132 (2005) 87-102
51. Ostrow L.W., and Sachs F. Mechanosensation and endothelin in astrocytes-hypothetical roles in CNS pathophysiology. Brain Res. Brain Res. Rev. 48 (2005) 488-508
52. Roskelley C.D., Desprez P.Y., and Bissell M.J. Extracellular matrix-dependent tissue-specific gene expression in mammary epithelial cells requires both physical and biochemical signal transduction. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 12378-12382
53. Rzigalinski B.A., Weber J.T., Willoughby K.A., and Ellis E.F. Intracellular free calcium dynamics in stretch-injured astrocytes. J. Neurochem. 70 (1998) 2377-2385
54. Sjaastad M.D., Angres B., Lewis R.S., and Nelson W.J. Feedback regulation of cell-substratum adhesion by integrin-mediated intracellular Ca2+ signaling. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 8214-8218
55. Tsacopoulos M. Metabolic signaling between neurons and glial cells: a short review. J. Physiol. (Paris) 96 (2002) 283-288
56. Ullian E.M., Sapperstein S.K., Christopherson K.S., and Barres B.A. Control of synapse number by glia. Science 291 (2001) 657-661
57. Vivien D., and Ali C. Transforming growth factor-beta signalling in brain disorders. Cytokine Growth Factor Rev. 17 (2006) 121-128