Caspase-mediated cell death predominates following engraftment of neural progenitor cells into traumatically injured rat brain

Brain Research

Volumn 1065, Issue 1-2, 2005, Pages 8-19

  Bakshi, Asha ^a,b   Keck, Carrie A ^a   Koshkin, Vadim S ^a   Lebold, David G ^a   Siman, Robert ^b   Snyder, Evan Y ^c   McIntosh, Tracy K ^a,d  

^a Traumatic Brain Injury Laboratory   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c BURNHAM INSTITUTE   (United States)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Graft cell death mechanism; Neural progenitor cell; Transplantation; Traumatic brain injury

Indexed keywords

CALPAIN; CASPASE; GREEN FLUORESCENT PROTEIN; PROTEINASE;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN CORTEX; BRAIN INJURY; CELL DEATH; CELL LABELING; CELL SURVIVAL; CELL TRANSPLANTATION; COMPARATIVE STUDY; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT; STEM CELL;

ALGORITHMS; ANIMALS; APOPTOSIS; BRAIN INJURIES; CALPAIN; CASPASES; CELL DEATH; IMMUNOHISTOCHEMISTRY; MALE; NEURONS; PERFUSION; RATS; RATS, SPRAGUE-DAWLEY; STEM CELL TRANSPLANTATION;

ANIMALIA;

EID: 28844498633     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2005.09.059     Document Type: Article

References (91)

1. M. Abercrombie Estimation of nuclear population from microtome sections Anat. Rec. 94 1946 239 247
2. P. Akerud, J.M. Canals, E.Y. Snyder, and E. Arenas Neuroprotection through delivery of glial cell line-derived neurotrophic factor by neural stem cells in a mouse model of Parkinson's disease J. Neurosci. 21 2001 8108 8118
3. E. Arenas, M. Trupp, P. Akerud, and C.F. Ibanez GDNF prevents degeneration and promotes the phenotype of brain noradrenergic neurons in vivo Neuron 15 1995 1465 1473
4. A. Ashkenazi, and V.M. Dixit Apoptosis control by death and decoy receptors Curr. Opin. Cell Biol. 11 1999 255 260
5. H. Auchincloss Jr., and D.H. Sachs Xenogeneic transplantation Annu. Rev. Immunol. 16 1998 433 470
6. G.R. Baker, P.M. Sullam, and J. Levin A simple, fluorescent method to internally label platelets suitable for physiological measurements Am. J. Hematol. 56 1997 17 25
7. R.A. Barker, S.B. Dunnett, A. Faissner, and J.W. Fawcett The time course of loss of dopaminergic neurons and the gliotic reaction surrounding grafts of embryonic mesencephalon to the striatum. Exp. Neurol. 141 1996 79 93
8. R. Beer, G. Franz, A. Srinivasan, R.L. Hayes, B.R. Pike, J.K. Newcomb, X. Zhao, E. Schmutzhard, W. Poewe, and A. Kampfl Temporal profile and cell subtype distribution of activated caspase-3 following experimental traumatic brain injury J. Neurochem. 75 2000 1264 1273
9. P. Berardi, M. Russell, A. El Osta, and K. Riabowol Functional links between transcription, DNA repair and apoptosis Cell. Mol. Life Sci. 61 2004 2173 2180
10. N. Bizat, J.M. Hermel, S. Humbert, C. Jacquard, C. Creminon, C. Escartin, F. Saudou, S. Krajewski, P. Hantraye, and E. Brouillet In vivo calpain/caspase cross-talk during 3-nitropropionic acid-induced striatal degeneration- Implication of a calpain-mediated cleavage of active caspase-3 J. Biol. Chem. 278 2003 43245 43253
11. J.A. Boockvar, J. Schouten, N. Royo, M. Millard, Z. Spangler, D. Castelbuono, E. Snyder, D. O'Rourke, and T. McIntosh Experimental traumatic brain injury modulates the survival, migration, and terminal phenotype of transplanted epidermal growth factor receptor-activated neural stem cells Neurosurgery 56 2005 163 171
12. R.L. Branton, and D.J. Clarke Apoptosis in primary cultures of E14 rat ventral mesencephala: time course of dopaminergic cell death and implications for neural transplantation Exp. Neurol. 160 1999 88 98
13. P. Brundin, J. Karlsson, M. Emgard, G.S. Schierle, O. Hansson, A. Petersen, and R.F. Castilho Improving the survival of grafted dopaminergic neurons: a review over current approaches Cell Transplant 9 2000 179 195
14. N. Cambray, and V. Wilson Axial progenitors with extensive potency are localised to the mouse chordoneural hinge Development 129 2002 4855 4866
15. S. Ceccatelli, C. Tamm, E. Sleeper, and S. Orrenius Neural stem cells and cell death Toxicol. Lett. 149 2004 59 66
16. S.L. Chan, and M.P. Mattson Caspase and calpain substrates: roles in synaptic plasticity and cell death J. Neurosci. Res. 58 1999 167 190
17. A. Cheng, S.L. Chan, O. Milhavet, S. Wang, and M.P. Mattson p38 MAP kinase mediates nitric oxide-induced apoptosis of neural progenitor cells J. Biol. Chem. 276 2001 43320 43327
18. F. Cicchetti, L. Costantini, R. Belizaire, W. Burton, O. Isacson, and W. Fodor Combined inhibition of apoptosis and complement improves neural graft survival of embryonic rat and porcine mesencephalon in the rat brain Exp. Neurol. 177 2002 376 384
19. R.S. Clark, P.M. Kochanek, M. Chen, S.C. Watkins, D.W. Marion, J. Chen, R.L. Hamilton, J.E. Loeffert, and S.H. Graham Increases in Bcl-2 and cleavage of caspase-1 and caspase-3 in human brain after head injury FASEB J. 13 1999 813 821
20. R.S. Clark, P.M. Kochanek, S.C. Watkins, M. Chen, C.E. Dixon, N.A. Seidberg, J. Melick, J.E. Loeffert, P.D. Nathaniel, K.L. Jin, and S.H. Graham Caspase-3 mediated neuronal death after traumatic brain injury in rats J. Neurochem. 74 2000 740 753
21. M.A. Colicos, C.E. Dixon, and P.K. Dash Delayed, selective neuronal death following experimental cortical impact injury in rats: possible role in memory deficits Brain Res. 739 1996 111 119
22. A.C. Conti, R. Raghupathi, J.Q. Trojanowski, and T.K. McIntosh Experimental brain injury induces regionally distinct apoptosis during the acute and delayed post-traumatic period J. Neurosci. 18 1998 5663 5672
23. M. Davenne, C. Custody, P. Charneau, and P.M. Lledo In vivo imaging of migrating neurons in the Mammalian forebrain Chem. Senses 30 Suppl. 1 2005 i115 i116
24. W.M. Duan, H. Widner, E.M. Frodl, and P. Brundin Immune-reactions following systemic immunization prior or subsequent to intrastriatal transplantation of allogeneic mesencephalic tissue in adult-rats Neuroscience 64 1995 629 641
25. M. Emgard, J. Karlsson, O. Hansson, and P. Brundin Patterns of cell death and dopaminergic neuron survival in intrastriatal nigral grafts Exp. Neurol. 160 1999 279 288
26. M. Emgard, U. Hallin, J. Karlsson, B.A. Bahr, P. Brundin, and K. Blomgren Both apoptosis and necrosis occur early after intracerebral grafting of ventral mesencephalic tissue: a role for protease activation J. Neurochem. 86 2003 1223 1232
27. A.I. Faden, P. Demediuk, S.S. Panter, and R. Vink The role of excitatory amino acids and NMDA receptors in traumatic brain injury Science 244 1988 798 800
28. C. Gahm, S. Holmin, and T. Mathiesen Temporal profiles and cellular sources of three nitric oxide synthase isoforms in the brain after experimental contusion Neurosurgery 46 2000 169 177
29. N. Gordon Apoptosis (programmed cell-death) and other reasons for elimination of neurons and axons Brain Dev. 17 1995 73 77
30. O. Hansson, R.F. Castilho, G.S. Kaminski Schierle, J. Karlsson, P. Nicotera, M. Leist, and P. Brundin Additive effects of caspase inhibitor and lazaroid on the survival of transplanted rat and human embryonic dopamine neurons Exp. Neurol. 164 2000 102 111
31. C.E. Helt, G.R. Hoernig, D.S. Albeck, G.A. Gerhardt, B. Ickes, M.E. Reyland, D.O. Quissell, I. Stromberg, and A.C. Granholm Neuroprotection of grafted neurons with a GDNF/caspase inhibitor cocktail Exp. Neurol. 170 2001 258 269
32. C.B. Hurelbrink, R.J. Armstrong, L.M. Luheshi, S.B. Dunnett, A.E. Rosser, and R.A. Barker Death of dopaminergic neurons in vitro and in nigral grafts: reevaluating the role of caspase activation Exp. Neurol. 171 2001 46 58
33. N. Joza, S.A. Susin, E. Daugas, W.L. Stanford, S.K. Cho, C.Y. Li, T. Sasaki, A.J. Elia, H.Y. Cheng, L. Ravagnan, K.F. Ferri, N. Zamzami, A. Wakeham, R. Hakem, H. Yoshida, Y.Y. Kong, T.W. Mak, J.C. Zuniga-Pflucker, G. Kroemer, and J.M. Penninger Essential role of the mitochondrial apoptosis-inducing factor in programmed cell death Nature 410 2001 549 554
34. Y. Katayama, M.K. Cheung, A. Alves, and D.P. Becker Ion fluxes and cell swelling in experimental traumatic brain injury: the role of excitatory amino acids J.T. Hoff A.L. Betz Intracranial Pressure VII 1989 Springer-Verlag Berlin 584 588
35. A. Khaldi, C.C. Chiueh, M.R. Bullock, and J.J. Woodward The significance of nitric oxide production in the brain after injury. Ann. N. Y. Acad. Sci. 962 2002 53 59
36. D.E. Kim, D. Schellingerhout, K. Ishii, K. Shah, and R. Weissleder Imaging of stem cell recruitment to ischemic infarcts in a murine model Stroke 35 2004 952 957
37. S.M. Knoblach, M. Nikolaeva, X. Huang, L. Fan, S. Krajewski, J.C. Reed, and A.I. Faden Multiple caspases are activated after traumatic brain injury: evidence for involvement in functional outcome J. Neurotrauma 19 2002 1155 1170
38. P.M. Lenzlinger, M.C. Morganti-Kossmann, H.L. Laurer, and T.K. McIntosh The duality of the inflammatory response to traumatic brain injury Mol. Neurobiol. 24 2001 169 181
39. A.K. Liou, R.S. Clark, D.C. Henshall, X.M. Yin, and J. Chen To die or not to die for neurons in ischemia, traumatic brain injury and epilepsy: a review on the stress-activated signaling pathways and apoptotic pathways Prog. Neurobiol. 69 2003 103 142
40. X. Liu, T. Van Vleet, and R.G. Schnellmann The role of calpain in oncotic cell death Annu. Rev. Pharmacol. Toxicol. 44 2004 349 370
41. P. Lu, L.L. Jones, E.Y. Snyder, and M.H. Tuszynski Neural stem cells constitutively secrete neurotrophic factors and promote extensive host axonal growth after spinal cord injury Exp. Neurol. 181 2003 115 129
42. T.J. Mahalik, W.E. Hahn, G.H. Clayton, and G.P. Owens Programmed cell-death in developing grafts of fetal substantia-nigra Exp. Neurol. 129 1994 27 36
43. D.M. Marchionini, T.J. Collier, M.R. Pitzer, and C.E. Sortwell Reassessment of caspase inhibition to augment grafted dopamine neuron survival Cell Transplant 13 2004 273 282
44. T.K. McIntosh, R. Vink, L. Noble, I. Yamakami, S. Fernyak, and A.I. Faden Traumatic brain injury in the rat: Characterization of a lateral fluid percussion model Neuroscience 28 1989 233 244
45. B. Nadarajah, P. Alifragis, R.O. Wong, and J.G. Parnavelas Ventricle-directed migration in the developing cerebral cortex Nat. Neurosci. 5 2002 218 224
46. R.W. Neumar, F.H. Meng, A.M. Mills, Y.A. Xu, C. Zhang, F.A. Welsh, and R. Siman Calpain activity in the rat brain after transient forebrain ischemia Exp. Neurol. 170 2001 27 35
47. R.W. Neumar, Y.A. Xu, H. Gada, R.P. Guttmann, and R. Siman Cross-talk between calpain and caspase proteolytic systems during neuronal apoptosis J. Biol. Chem. 278 2003 14162 14167
48. G. Nikkhah, M. Olsson, J. Eberhard, C. Bentlage, M.G. Cunningham, and A. Bjorklund A microtransplantation approach for cell suspension grafting in the rat Parkinson model: a detailed account of the methodology Neuroscience 63 1994 57 72
49. T.F. Oo, R. Siman, and R.E. Burke Distinct nuclear and cytoplasmic localization of caspase cleavage products in two models of induced apoptotic death in dopamine neurons of the substantia nigra Exp. Neurol. 175 2002 1 9
50. A.M. Palmer, D.W. Marion, M.L. Botscheller, P.E. Swedlow, S.D. Styren, and S.T. DeKosky Traumatic brain injury-induced excitotoxicity assessed in a controlled cortical impact model J. Neurochem. 61 1993 2015 2024
51. Z. Pang, V. Bondada, T. Sengoku, R. Siman, and J.W. Geddes Calpain facilitates the neuron death induced by 3-nitropropionic acid and contributes to the necrotic morphology J. Neuropathol. Exp. Neurol. 62 2003 633 643
52. B.R. Pike, X. Zhao, J.K. Newcomb, R.M. Posmantur, K.K.W. Wang, and R.L. Hayes Regional calpain and caspase-3 proteolysis of a-spectrin after traumatic brain injury. NeuroReport 9 1998 2437 2442
53. B.R. Pike, X. Zhao, J.K. Newcomb, K.K. Wang, R.M. Posmantur, and R.L. Hayes Temporal relationships between de novo protein synthesis, calpain and caspase 3-like protease activation, and DNA fragmentation during apoptosis in septo-hippocampal cultures J. Neurosci. Res. 52 1998 505 520
54. G.V. Putcha, C.A. Harris, K.L. Moulder, R.M. Easton, C.B. Thompson, and E.M. Johnson Intrinsic and extrinsic pathway signaling during neuronal apoptosis: lessons from the analysis of mutant mice J. Cell Biol. 157 2002 441 453
55. S.K. Ray, D.D. Matzelle, G.G. Wilford, E.L. Hogan, and N.L. Banik Increased calpain expression is associated with apoptosis in rat spinal cord injury: calpain inhibitor provides neuroprotection Neurochem. Res. 25 2000 1191 1198
56. P. Riess, C. Zhang, K.E. Saatman, H.L. Laurer, L.G. Longhi, R. Raghupathi, P.M. Lenzlinger, J. Lifshitz, J. Boockvar, E. Neugebauer, E.Y. Snyder, and T.K. McIntosh Transplanted neural stem cells survive, differentiate, and improve neurological motor function after experimental traumatic brain injury Neurosurgery 51 2002 1043 1054
57. N.C. Ringger, P.J. Tolentino, D.M. McKinsey, B.R. Pike, K.K. Wang, and R.L. Hayes Effects of injury severity on regional and temporal mRNA expression levels of calpains and caspases after traumatic brain injury in rats J. Neurotrauma 21 2004 829 841
58. A. Rink, K.-M. Fung, J.Q. Trojanowski, V.M.Y. Lee, E. Neugebauer, and T.K. McIntosh Evidence of apoptotic cell death after experimental traumatic brain injury in the rat Am. J. Pathol. 147 1995 1575 1583
59. J.M. Roberts-Lewis, M.J. Savage, V.R. Marcy, L.R. Pinsker, and R. Siman Immunolocalization of calpain I-mediated spectrin degradation to vulnerable neurons in the ischemic gerbil brain J. Neurosci. 14 6 1994 3934 3944
60. C.M. Rosario, B.D. Yandava, B. Kosaras, D. Zurakowski, R.L. Sidman, and E.Y. Snyder Differentiation of engrafted multipotent neural progenitors towards replacement of missing granule neurons in meander tail cerebellum may help determine the locus of mutant gene action Development 124 1997 4213 4224
61. G.D. Rosen, and J.D. Harry Brain volume estimation from serial section measurements: a comparison of methodologies J. Neurosci. Methods 35 1990 115 124
62. C. Rosenblad, D. Kirik, and A. Bjorklund Neurturin enhances the survival of intrastriatal fetal dopaminergic transplants NeuroReport 10 1999 1783 1787
63. E.F. Ryder, E.Y. Snyder, and C.L. Cepko Establishment and characterization of multipotent neural cell lines using retrovirus vector-mediated oncogene transfer J. Neurobiol. 21 1990 356 375
64. K.E. Saatman, D. Bozyczko-Coyne, V. Marcy, R. Siman, and T.K. McIntosh Prolonged calpain-mediated spectrin breakdown occurs regionally following experimental brain injury in the rat J. Neuropathol. Exp. Neurol. 55 1996 850 860
65. G.S. Schierle, O. Hansson, M. Leist, P. Nicotera, H. Widner, and P. Brundin Caspase inhibition reduces apoptosis and increases survival of nigral transplants Nat. Med. 5 1999 97 100
66. J.W. Schouten, N.C. Royo, K.E. Saatman, E.Y. Snyder, J.Q. Trojanowski, D.J. Prockop, A. Maas, and T. McIntosh A review and rationale for the use of cellular transplantation as a therapeutic strategy for traumatic brain injury J. Neurotrauma 21 11 2004 1501 1538
67. K. Schulze-Osthoff, D. Ferrari, M. Los, S. Wesselborg, and M.E. Peter Apoptosis signaling by death receptors Eur. J. Biochem. 254 1998 439 459
68. P.T. Shah, K.-W. Yoon, X.M. Xu, and L.D. Broder Apoptosis mediates cell death following traumatic injury in rat hippocampal neurons Neuroscience 79 1997 999 1004
69. R. Siman, M. Baudry, and G. Lynch Brain fodrin: substitute for calpain I, an endogenous calcium-activated protease Proc. Natl. Acad. Sci. 81 1984 3572 3576
70. H.H. Slagsvold, C.M. Rosseland, C. Jacobs, E. Khuong, N. Kristoffersen, M. Gaarder, A.B. Fallgren, H.S. Huitfeldt, and R.E. Paulsen High molecular weight DNA fragments are processed by caspase sensitive or caspase independent pathways in cultures of cerebellar granule neurons Brain Res. 984 2003 111 121
71. E.Y. Snyder, D.L. Deitcher, C. Walsh, S. Aldea-Arnold, E.A. Hartwieg, and C.L. Cepko Multipotent neural cell lines can engraft and participate in development of mouse cerebullum Cell 68 1992 33 51
72. E.Y. Snyder, C. Yoon, J.D. Flax, and J.D. Macklis Multipotent neural precursors can differentiate toward replacement of neurons undergoing targeted apoptotic degeneration in adult mouse neocortex Proc. Natl. Acad. Sci. U. S. A. 94 1997 11663 11668
73. H.D. Soares, R.R. Hicks, D.H. Smith, and T.K. McIntosh Inflammatory leukocytic recruitment and diffuse neuronal degeneration are separate pathological processes resulting from traumatic brain injury J. Neurosci. 15 1995 8223 8233
74. C.E. Sortwell Strategies for the augmentation of grafted dopamine neuron survival Front. Biosci. 8 2003 s522 s532
75. C.E. Sortwell, M.R. Pitzer, and T.J. Collier Time course of apoptotic cell death within mesencephalic cell suspension grafts: Implications for improving grafted dopamine neuron survival Exp. Neurol. 165 2000 268 277
76. P.G. Sullivan, J.N. Keller, W.L. Bussen, and S.W. Scheff Cytochrome c release and caspase activation after traumatic brain injury Brain Res. 949 2002 88 96
77. S.A. Susin, E. Daugas, L. Ravagnan, K. Samejima, N. Zamzami, M. Loeffler, P. Costantini, K.F. Ferri, T. Irinopoulou, M.C. Prevost, G. Brothers, T.W. Mak, J. Penninger, W.C. Earnshaw, and G. Kroemer Two distinct pathways leading to nuclear apoptosis J. Exp. Med. 192 2000 571 580
78. C. Tamm, J.D. Robertson, E. Sleeper, M. Enoksson, M. Emgard, S. Orrenius, and S. Ceccatelli Differential regulation of the mitochondrial and death receptor pathways in neural stem cells Eur. J. Neurosci. 19 2004 2613 2621
79. V.A. Tyurin, Y.Y. Tyurina, G.G. Borisenko, T.V. Sokolova, V.B. Ritov, P.J. Quinn, M. Rose, P. Kochanek, S.H. Graham, and V.E. Kagan Oxidative stress following traumatic brain injury in rats: quantitation of biomarkers and detection of free radical intermediates J. Neurochem. 75 2000 2178 2189
80. E.A. Vitarbo, K. Chatzipanteli, K. Kinoshita, J.S. Truettner, O.F. Alonso, and W.D. Dietrich Tumor necrosis factor alpha expression and protein levels after fluid percussion injury in rats: the effect of injury severity and brain temperature Neurosurgery 55 2004 416 424
81. K. Wada, K. Chatzipanteli, R. Busto, and W.D. Dietrich Role of nitric oxide in traumatic brain injury in the rat J. Neurosurg. 89 1998 807 818
82. L. Wennberg, K.A. Czech, L.C. Larsson, B. Mirza, W. Bennet, Z. Song, and H. Widner Effects of immunosuppressive treatment on host responses against intracerebral porcine neural tissue xenografts in rats Transplantation 71 2001 1797 1806
83. S. Williams, R. Raghupathi, M.A. MacKinnon, T.K. McIntosh, K.E. Saatman, and D.I. Graham In situ DNA fragmentation occurs in white matter up to 12 months after head injury in man Acta Neuropathol. 102 2001 581 590
84. S. Williams, M.-A. MacKinnon, R. Raghupathi, K.E. Saatman, T.K. McIntosh, D.I. Graham, TUNEL+cells in the brains of fatally head injured patients surviving up to 12 months. J. Neurotrauma (submitted for publication). (Ref:abstract).
85. S. Wilson, R. Raghupathi, K.E. Saatman, M.A. Mac Kinnon, T.K. McIntosh, and D.I. Graham Continued in situ DNA fragmentation of microglia/macrophages in white matter weeks and months after traumatic brain injury J. Neurotrauma 21 2004 239 250
86. A.G. Yakovlev, S. Knoblach, L. Fan, G.B. Fox, R. Goodnight, and A.I. Faden Activation of CPP32-like caspases contributes to neuronal apoptosis and neurological dysfunction after traumatic brain injury J. Neurosci. 17 1997 7415 7424
87. V. Zaman, and A.K. Shetty Combined neurotrophic supplementation and caspase inhibition enhances survival of fetal hippocampal CA3 cell grafts in lesioned CA3 region of the aging hippocampus Neuroscience 109 2002 537 553
88. V. Zaman, and A.K. Shetty Fetal hippocampal CA3 cell grafts enriched with fibroblast growth factor-2 exhibit enhanced neuronal integration into the lesioned aging rat hippocampus in a kainate model of temporal lobe epilepsy Hippocampus 13 2003 618 632
89. W.M. Zawada, D.J. Zastrow, E.D. Clarkson, F.S. Adams, K.P. Bell, and C.R. Freed Growth factors improve immediate survival of embryonic dopamine neurons after transplantation into rats Brain Res. 786 1998 96 103
90. C. Zhang, R. Siman, Y.A. Xu, A.M. Mills, J.R. Frederick, and R.W. Neumar Comparison of calpain and caspase activities in the adult rat brain after transient forebrain ischemia Neurobiol. Dis. 10 2002 289 305
91. R. Zietlow, S.R. Sinclair, C.J. Schwiening, S.B. Dunnett, and J.W. Fawcettt The release of excitatory amino acids, dopamine, and potassium following transplantation of embryonic mesencephalic dopaminergic grafts to the rat striatum, and their effects on dopaminergic neuronal survival in vitro Cell Transplant 11 2002 637 652