Grafted neural progenitors migrate and form neurons after experimental traumatic brain injury

Restorative Neurology and Neuroscience

Volumn 27, Issue 4, 2009, Pages 323-324

  Wallenquist, U ^a,b   Brannvall K ^a,c   Clausen, F ^b   Lewen A ^b   Hillered, L ^b   Forsberg Nilsson, K ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b UPPSALA UNIVERSITY HOSPITAL   (Sweden)

^c Schering Plough AS   (Norway)

Author keywords

CNS; EGFP transgenic mice; Migration; Neural stem cells; Regeneration; TBI; Transplantation

Indexed keywords

ENHANCED GREEN FLUORESCENT PROTEIN;

ANIMAL MODEL; ARTICLE; ASTROCYTE; BRAIN; BRAIN CORTEX; CELL DIFFERENTIATION; CELL FATE; CELL MIGRATION; CONTROLLED STUDY; CORPUS CALLOSUM; ENVIRONMENT; GLIA; HEMISPHERE; LATERAL BRAIN VENTRICLE; MALE; MORTALITY; MOUSE; NERVE CELL; NERVE GRAFT; NERVE REGENERATION; NEURAL STEM CELL; NEURAL STEM CELL TRANSPLANTATION; NONHUMAN; OUTCOME ASSESSMENT; PARENCHYMA; PRIORITY JOURNAL; PROGENY; STEM CELL; TRAUMATIC BRAIN INJURY;

ACTINS; ANIMALS; BRAIN INJURIES; CELL COUNT; CELL MOVEMENT; DISEASE MODELS, ANIMAL; EMBRYO, MAMMALIAN; EMBRYONIC STEM CELLS; GLIAL FIBRILLARY ACIDIC PROTEIN; GREEN FLUORESCENT PROTEINS; INDOLES; INTERMEDIATE FILAMENT PROTEINS; LATERAL VENTRICLES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROTUBULE-ASSOCIATED PROTEINS; NERVE TISSUE PROTEINS; NEURONS; PHOSPHOPYRUVATE HYDRATASE; S100 PROTEINS; TIME FACTORS;

EID: 70349129922     PISSN: 09226028     EISSN: None     Source Type: Journal    
DOI: 10.3233/RNN-2009-0481     Document Type: Article

References (49)

1. Aboody, K.S., Brown, A., Rainov, N.G., Bower, K.A., Liu, S., Yang, W., Small, J.E., Herrlinger, U., Ourednik, V., & Black, P.M., Breakefield, X.O., Snyder, E.Y. (2000). Neural stem cells display extensive tropism for pathology in adult brain: evidence from intracranial gliomas. Proceedings of the National Academy of Sciences of the United States of America, 97, 12846-12851.
2. Bakshi, A., Keck, C.A., Koshkin, V.S., LeBold, D.G., Siman, R., Snyder, E.Y., & McIntosh, T.K. (2005). Caspase-mediated cell death predominates following engraftment of neural progenitor cells into traumatically injured rat brain. Brain Research, 1065, 8-19.
3. Brannvall, K., Sandelin, M., Wallenquist, U., Forsberg-Nilsson, K., Aldskogius, H., & Kozlova, E.N. (2006). Central nervous system stem/progenitor cells form neurons and peripheral glia after transplantation to the dorsal root ganglion. Neuroreport, 17, 623-628.
4. Brustle, O., Maskos, U., & McKay, R.D.G. (1995). Host-guided migration allows targeted introduction of neurons into the embryonic brain. Neuron, 15, 1275-1285.
5. Cao, Q.L., Zhang, Y.P., Howard, R.M., Walters, W.M., Tsoulfas, P., & Whittemore, S.R. (2001). Pluripotent stem cells engrafted into the normal or lesioned adult rat spinal cord are restricted to a glial lineage. Experimental Neurology, 167, 48-58.
6. Chow, S.Y., Moul, J., Tobias, C.A., Himes, B.T., Liu, Y., Obroc-ka, M., Hodge, L., Tessler, A., & Fischer, I. (2000). Characterization and intraspinal grafting of EGF/bFGF-dependent neurospheres derived from embryonic rat spinal cord. Brain Research, 874, 87-106.
7. Clausen, F., Lorant, T., Lewen, A., & Hillered, L. (2007). T lymphocyte trafficking: a novel target for neuroprotection in traumatic brain injury. Journal of Neurotrauma, 24, 1295-1307.
8. Eriksson, P., Perfilieva, E., Bjork-Eriksson, T., Alborn, A.-M., Nord- borg, C., Peterson, D., & Gage, F. (1998). Neurogenesis in the adult human hippocampus. Nature Medicine, 4, 1313-1317.
9. Fricker, R.A., Carpenter, M.K., Winkler, C., Greco, C., Gates, M.A., & Bjorklund, A. (1999). Site-specific migration and neuronal differentiation of human neural progenitor cells after transplantation in the adult rat brain. J Neurosci, 19, 5990-6005.
10. Gage, F.H., Coates, P.W., Palmer, T.D., Kuhn, H.G., Fisher, L.J., Suhonen, J.O., Peterson, D.A., Suhr, S.T., & Ray, J. (1995). Survival and differentiation of adult neuronal progenitor cells transplanted to the adult brain. Proc Natl Acad Sci, 92, 11879-11883.
11. Gross, R.E., Mehler, M.F., Mabie, P.C., Zhang, Z., Santschi, L., & Kessler, J.A. (1996). Bone morphogenetic proteins promote astroglial lineage committment by mammalian subventriclular zone progenitor cells. Neuron, 17, 595-606.
12. Habgood, M.D., Bye, N., Dziegielewska, K.M., Ek, C.J., Lane, M.A., Potter, A., Morganti-Kossmann, C., & Saunders, N.R. (2007). Changes in blood-brain barrier permeability to large and small molecules following traumatic brain injury in mice. The European Journal of Neuroscience, 25, 231-238.
13. Herrera, D.G., Garcia-Verdugo, J.M., & Alvarez-Buylla, A. (1999). Adult-derived neural precursors transplanted into multiple regions in the adult brain. Annals of Neurology, 46, 867-877.
14. Hillered, L., Vespa, P.M., & Hovda, D.A. (2005). Translational neu-rochemical research in acute human brain injury: the current status and potential future for cerebral microdialysis. Journal of Neurotrauma, 22, 3-41.
15. Hoane, M.R., Becerra, G.D., Shank, J.E., Tatko, L., Pak, E.S., Smith, M., & Murashov, A.K. (2004). Transplantation of neuronal and glial precursors dramatically improves sensorimotor function but not cognitive function in the traumatically injured brain. Journal of Neurotrauma, 21, 163-174.
16. Holmin, S., Mathiesen, T., Shetye, J., & Biberfeld, P. (1995). In-tracerebral inflammatory response to experimental brain contusion. Acta Neurochirurgica, 132, 110-119.
17. Imitola, J., Raddassi, K., Park, K.I., Mueller, F.J., Nieto, M., Teng, Y.D., Frenkel, D., Li, J., Sidman, R.L., Walsh, C.A., Snyder, E.Y., & Khoury, S.J. (2004). Directed migration of neural stem cells to sites of CNS injury by the stromal cell-derived factor 1alpha/CXC chemokine receptor 4 pathway. Proceedings of the National Academy of Sciences of the United States of America, 101, 18117-18122.
18. Israelsson, C., Lewen, A., Kylberg, A., Usoskin, D., Althini, S., Lin-deberg, J., Deng, C.X., Fukuda, T., Wang, Y., Kaartinen, V., Mishina, Y., Hillered, L., & Ebendal, T. (2006). Genetically modified bone morphogenetic protein signalling alters traumatic brain injury-induced gene expression responses in the adult mouse. Journal of Neuroscience Research, 84, 47-57.
19. Johe, K.K., Hazel, T.G., Muller, T., Dugich Djordjevic, M.M., & McKay, R.D. (1996). Single factors direct the differentiation of stem cells from the fetal and adult central nervous system. Genes-Dev, 10, 3129-3140.
20. Katayama, Y., Becker, D.P., Tamura, T., & Hovda, D.A. (1990). Massive increases in extracellular potassium and the indiscriminate release of glutamate following concussive brain injury. Journal of Neurosurgery, 73, 889-900.
21. Kirschenbaum, B., Nedergaard, M., Preuss, A., Barami, K., Fraser, R.A., & Goldman, S.A. (1994). In vitro neuronal production and differentiation by precursor cells derived from the adult human forebrain. Cereb Cortex, 4, 576-589.
22. Kukekov, V.G., Laywell, E.D., Suslov, O., Davies, K., Scheffler, B., Thomas, L.B., O'Brien, T.F., Kusakabe, M., & Steindler, D.A. (1999). Multipotent stem/progenitor cells with similar properties arise from two neurogenic regions of adult human brain. Experimental Neurology, 156, 333-344.
23. Laurer, H.L., & McIntosh, T.K. (1999). Experimental models of brain trauma. Current Opinion in Neurology, 12, 715-721.
24. Lendahl, U., Zimmerman, L., & McKay, R.D.G. (1990). CNS stem cells express a new class of intermediate filament protein. Cell, 60, 585-595.
25. Lewen, A., Fredriksson, A., Li, G.L., Olsson, Y., & Hillered, L. (1999). Behavioural and morphological outcome of mild cortical contusion trauma of the rat brain: influence of NMDA-receptor blockade. Acta neurochirurgica, 141, 193-202.
26. Lois, C., & Alvarez-Buylla, A. (1993). Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proceedings of the National Academy of Sciences of the United States of America, 90, 2074-2077.
27. Longhi, L., Watson, D.J., Saatman, K.E., Thompson, H.J., Zhang, C., Fujimoto, S., Royo, N., Castelbuono, D., Raghupathi, R., Trojanowski, J.Q., Lee, V.M., Wolfe, J.H., Stocchetti, N., & McIntosh, T.K. (2004). Ex vivo gene therapy using targeted engraftment of NGF-expressing human NT2N neurons attenuates cognitive deficits following traumatic brain injury in mice. Journal of Neurotrauma, 21, 1723-1736.
28. Marklund, N., Bakshi, A., Castelbuono, D.J., Conte, V., & McIntosh, T.K. (2006). Evaluation of pharmacological treatment strategies in traumatic brain injury. Current Pharmaceutical Design, 12, 1645-1680.
29. McKay, R. (1997). Stem cells in the central nervous system. Science, 276, 66-71.
30. Mehler, M. (2002). Mechanisms regulating lineage diversity during mammalian cerebral cortical neurogenesis and gliogenesis. Results Probl Cell Differ, 39, 27-52.
31. Narayan, R.K., Michel, M.E., Ansell, B., Baethmann, A., Biegon, A., Bracken, M.B., Bullock, M.R., Choi, S.C., Clifton, G.L., Contant, C.F., Coplin, W.M., Dietrich, W.D., Ghajar, J., Grady, S.M., Grossman, R.G., Hall, E.D., Heetderks, W., Hovda, D.A., Jallo, J., Katz, R.L., Knoller, N., Kochanek, P.M., Maas, A.I., Majde, J., Marion, D.W., Marmarou, A., Marshall, L.F., McIntosh, T.K., Miller, E., Mohberg, N., Muizelaar, J.P., Pitts, L.H., Quinn, P., Riesenfeld, G., Robertson, C.S., Strauss, K.I., Teasdale, G., Temkin, N., Tuma, R., Wade, C., Walker, M.D., Weinrich, M., Whyte, J., Wilberger, J., Young, A.B., & Yurkewicz, L. (2002). Clinical trials in head injury. Journal of Neurotrauma, 19, 503-557.
32. Nilsson, P., Hillered, L., Olsson, Y., Sheardown, M.J., & Hansen, A.J. (1993). Regional changes in interstitial K+ and Ca2+ levels following cortical compression contusion trauma in rats. J Cereb Blood Flow Metab, 13, 183-192.
33. Nilsson, P., Hillered, L., Ponten, U., & Ungerstedt, U. (1990). Changes in cortical extracellular levels of energy-related metabolites and amino acids following concussive brain injury in rats. J Cereb Blood Flow Metab, 10, 631-637.
34. Okabe, M., Ikawa, M., Kominami, K., Nakanishi, T., & Nishimune, Y. (1997). 'Green mice' as a source of ubiquitous green cells. FEBS letters, 407, 313-319.
35. Povlishock, J.T., & Katz, D.I. (2005). Update of neuropathology and neurological recovery after traumatic brain injury. The Journal of Head Trauma Rehabilitation, 20, 76-94.
36. Reynolds, B.A., & Rietze, R.L. (2005). Neural stem cells and neu-rospheres - re-evaluating the relationship. Nature Methods, 2, 333-336.
37. Reynolds, B.A., Tetzlaff, W., & Weiss, S. (1992). A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes. J Neurosci, 12, 4565-4574.
38. Riess, P., Zhang, C., Saatman, K.E., Laurer, H.L., Longhi, L.G., Raghupathi, R., Lenzlinger, P.M., Lifshitz, J., Boockvar, J., Neugebauer, E., Snyder, E.Y., & McIntosh, T.K. (2002). Transplanted neural stem cells survive, differentiate, and improve neurological motor function after experimental traumatic brain injury. Neurosurgery, 51, 1043-1052; Discussion, 1052-11044
39. Schouten, J.W., Fulp, C.T., Royo, N.C., Saatman, K.E., Watson, D.J., Snyder, E.Y., Trojanowski, J.Q., Prockop, D.J., Maas, A.I., & McIntosh, T.K. (2004). A review and rationale for the use of cellular transplantation as a therapeutic strategy for traumatic brain injury. Journal of Neurotrauma, 21, 1501-1538.
40. Shear, D.A., Tate, M.C., Archer, D.R., Hoffman, S.W., Hulce, V.D., Laplaca, M.C., & Stein, D.G. (2004). Neural progenitor cell transplants promote long-term functional recovery after traumatic brain injury. Brain Research, 1026, 11-22.
41. Shihabuddin, L.S., Horner, P.J., Ray, J., & Gage, F.H. (2000). Adult spinal cord stem cells generate neurons after transplantation in the adult dentate gyrus. J Neurosci, 20, 8727-8735.
42. Smith, D.H., Soares, H.D., Pierce, J.S., Perlman, K.G., Saatman, K.E., Meaney, D.F., Dixon, C.E., & McIntosh, T.K. (1995). A model of parasagittal controlled cortical impact in the mouse: cognitive and histopathologic effects. Journal of Neurotrauma, 12, 169-178.
43. Sommer, L., Ma, Q., & Anderson, D.J. (1996). neurogenins, a novel family of atonal-related bHLH transcription factors, are putative mammalian neuronal determination genes that reveal progenitor cell heterogeneity in the developing CNS and PNS. Molecular and Cellular Neurosciences, 8, 221-241.
44. Sun, Y., Nadal-Vicens, M., Misono, S., Lin, M.Z., Zubiaga, A., Hua, X., Fan, G., & Greenberg, M.E. (2001). Neurogenin promotes neurogenesis and inhibits glial differentiation by independent mechanisms. Cell, 104, 365-376.
45. Suslov, O.N., Kukekov, V.G., Ignatova, T.N., & Steindler, D.A. (2002). Neural stem cell heterogeneity demonstrated by molecular phenotyping of clonal neurospheres. Proceedings of the National Academy of Sciences of the United States of America, 99, 14506-14511.
46. Sykova, E., & Jendelova, P. (2005). Magnetic resonance tracking of implanted adult and embryonic stem cells in injured brain and spinal cord. Annals of the New York Academy of Sciences, 1049, 146-160.
47. Tamaki, S., Eckert, K., He, D., Sutton, R., Doshe, M., Jain, G., Tushinski, R., Reitsma, M., Harris, B., Tsukamoto, A., Gage, F., Weissman, I., & Uchida, N. (2002). Engraftment of sorted/expanded human central nervous system stem cells from fetal brain. Journal of Neuroscience Research, 69, 976-986.
48. Wang, K.K., Larner, S.F., Robinson, G., & Hayes, R.L. (2006). Neuroprotection targets after traumatic brain injury. Current Opinion in Neurology, 19, 514-519.
49. Wennersten, A., Meier, X., Holmin, S., Wahlberg, L., & Mathiesen, T. (2004). Proliferation, migration, and differentiation of human neural stem/progenitor cells after transplantation into a rat model of traumatic brain injury. Journal of Neurosurgery, 100, 88-96.