Stem cell-paved biobridge facilitates neural repair in traumatic brain injury

Frontiers in Systems Neuroscience

Volumn 8, Issue JUNE, 2014, Pages

  Tajiri, Naoki ^a   Duncan, Kelsey ^a   Antoine, Alesia ^a   Pabon, Mibel ^a   Acosta, Sandra A ^a   de la Pena, Ike ^a   Hernadez Ontiveros, Diana G ^a   Shinozuka, Kazutaka ^a   Ishikawa, Hiroto ^a   Kaneko, Yuji ^a   Yankee, Ernest ^b   McGrogan, Michael ^b   Case, Casey ^b   Borlongan, Cesar V ^a  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b Sanbio Inc ^*  (United States)

Author keywords

Cell transplantation; Extracellular matrix; Neurogenesis; Regenerative medicine; Trauma

Indexed keywords

CYCLOSPORIN A; GELATINASE B; KI 67 ANTIGEN;

ARTICLE; BRAIN ISCHEMIA; CELL MIGRATION; EXPERIMENTAL MODEL; HUMAN; MESENCHYMAL STROMA CELL; NERVE CELL DIFFERENTIATION; NERVE REGENERATION; NEURAL STEM CELL; NONHUMAN; OLFACTORY ENSHEATHING CELL; PARKINSON DISEASE; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); RAT MODEL; STEM CELL NICHE; STEM CELL TRANSPLANTATION; SUBVENTRICULAR ZONE; TRAUMATIC BRAIN INJURY;

EID: 84908288822     PISSN: 16625137     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnsys.2014.00116     Document Type: Article

References (50)

1. Acosta, S. A., Tajiri, N., Shinozuka, K., Ishikawa, H., Sanberg, P. R., Sanchez-Ramos, J., et al. (2014). Combination therapy of human umbilical cord blood cells and granulocyte colony stimulating factor reduces histopathological and motor impairments in an experimental model of chronic traumatic brain injury. PLoS ONE 9:e90953. doi: 10.1371/journal.pone.0090953
2. Alvarez-Buylla, A., Kohwi, M., Nguyen, T. M., and Merkle, F. T. (2008). The heterogeneity of adult neural stem cells and the emerging complexity of their niche. Cold Spring Harb. Symp. Quant. Biol. 73, 357-365. doi: 10.1101/sqb.2008.73.019
3. Andres, R. H., Horie, N., Slikker, W., Keren-Gill, H., Zhan, K., Sun, G., et al. (2011). Human neural stem cells enhance structural plasticity and axonal transport in the ischaemic brain. Brain 134, 1777-1789. doi: 10.1093/brain/awr094
4. Barbour, H. R., Plant, C. D., Harvey, A. R., and Plant, G. W. (2013). Tissue sparing, behavioral recovery, supraspinal axonal sparing/regeneration following subacute glial transplantation in a model of spinal cord contusion. BMC Neurosci. 14:106. doi: 10.1186/1471-2202-14-106
5. Barha, C. K., Ishrat, T., Epp, J. R., Galea, L. A., and Stein, D. G. (2011). Progesterone treatment normalizes the levels of cell proliferation and cell death in the dentate gyrus of the hippocampus after traumatic brain injury. Exp. Neurol. 231, 72-81. doi: 10.1016/j.expneurol.2011.05.016
6. Barkho, B. Z., Munoz, A. E., Li, X., Li, L., Cunningham, L. A., and Zhao, X. (2008). Endogenous matrix metalloproteinase (MMP)-3 and MMP-9 promote the differentiation and migration of adult neural progenitor cells in response to chemokines. Stem Cells 26, 3139-3149. doi: 10.1634/stemcells.2008-0519
7. Borlongan, C. V. (2011). Bone marrow stem cell mobilization in stroke: a 'bone-head' may be good after all!. Leukemia 25, 1674-1686. doi: 10.1038/leu.2011.167
8. Borlongan, C. V., Hadman, M., Sanberg, C. D., and Sanberg, P. R. (2004). Central nervous system entry of peripherally injected umbilical cord blood cells is not required for neuroprotection in stroke. Stroke 35, 2385-2389. doi: 10.1161/01.STR.0000141680.49960.d7
9. Carlén, M., Meletis, K., Goritz, C., Darsalia, V., Evergren, E., Tanigaki, K., et al. (2009). Forebrain ependymal cells are Notch-dependent and generate neuroblasts and astrocytes after stroke. Nat. Neurosci. 12, 259-267. doi: 10.1038/nn.2268
10. Carrero, R., Cerrada, I., Lledó, E., Dopazo, J., García-García, F., Rubio, M. P., et al. (2012). IL1β induces mesenchymal stem cells migration and leucocyte chemotaxis through NF-κB. Stem Cell Rev. 8, 905-916. doi: 10.1007/s12015-012-9364-9
11. Chiang, Y., Morales, M., Zhou, F. C., Borlongan, C., Hoffer, B. J., and Wang, Y. (2001). Fetal intra-nigral ventral mesencephalon and kidney tissue bridge transplantation restores the nigrostriatal dopamine pathway in hemi-parkinsonian rats. Brain Res. 889, 200-207. doi: 10.1016/S0006-8993(00)03133-4
12. del Zoppo, G. J., Frankowski, H., Gu, Y. H., Osada, T., Kanazawa, M., Milner, R., et al. (2012). Microglial cell activation is a source of metalloproteinase generation during hemorrhagic transformation. J. Cereb. Blood Flow Metab. 32, 919-932. doi: 10.1038/jcbfm.2012.11
13. Ducruet, A. F., Zacharia B. E., Sosunov, S. A., Gigante, P. R., Yeh, M. L., Gorski, J. W., et al. (2012). Complement inhibition promotes endogenous neurogenesis and sustained anti-inflammatory neuroprotection following reperfused stroke. PLoS ONE 7:e38664. doi: 10.1371/journal.pone.0038664
14. Ekdahl, C. T., Kokaia, Z., and Lindvall, O. (2009). Brain inflammation and adult neurogenesis: the dual role of microglia. Neuroscience 158, 1021-1029. doi: 10.1016/j.neuroscience.2008.06.052
15. Hargus, G., Cooper, O., Deleidi, M., Levy, A., Lee, K., Marlow, E., et al. (2010). Differentiated Parkinson patient-derived induced pluripotent stem cells grow in the adult rodent brain and reduce motor asymmetry in Parkinsonian rats. Proc. Natl. Acad. Sci U.S.A. 107, 15921-15926. doi: 10.1073/pnas.1010209107
16. Hassani, Z., Oreilly, J., Pearse, Y., Stroemer, P., Tang, E., Sinden, J., et al. (2012). Human neural progenitor cell engraftment increases neurogenesis and microglial recruitment in the brain of rats with stroke. PLoS ONE 7:e50444. doi: 10.1371/journal.pone.0050444
17. He, B. R., Xie, S. T., Wu, M. M., Hao, D. J., and Yang, H. (2013). Phagocytic removal of neuronal debris by olfactory ensheathing cells enhances neuronal survival and neurite outgrowth via p38MAPK activity. Mol. Neurobiol. 49, 1501-1512. doi: 10.1007/s12035-013-8588-2
18. Hong, S. H., Rampalli, S., Lee, J. B., McNicol, J., Collins, T., Draper, J. S., et al. (2011). Cell fate potential of human pluripotent stem cells is encoded by histone modifications. Cell Stem Cell 9, 24-36. doi: 10.1016/j.stem.2011.06.002
19. Jaskelioff, M., Muller, F. L., Paik, J. H., Thomas, E., Jiang, S., Adams, A. C., et al. (2011). Telomerase reactivation reverses tissue degeneration in aged telomerase-deficient mice. Nature 469, 102-106. doi: 10.1038/nature09603
20. Kim, Y., Sharov, A. A., McDole, K., Cheng, M., Hao, H., Fan, C. M., et al. (2011). Mouse B-type lamins are required for proper organogenesis but not by embryonic stem cells. Science 334, 1706-1710. doi: 10.1126/science. 1211222
21. Lee, H. S., Bae, E. J., Yi, S. H., Shim, J. W., Jo, A. Y., Kang, J. S., et al. (2010). Foxa2 and Nurr1 synergistically yield A9 nigral dopamine neurons exhibiting improved differentiation, function, and cell survival. Stem Cells 28, 501-512. doi: 10.1002/stem.294
22. Lee, J. P., Jeyakumar, M., Gonzalez, R., Takahashi, H., Lee, P. J., Baek, R. C., et al. (2007). Stem cells act through multiple mechanisms to benefit mice with neurodegenerative metabolic disease. Nat. Med. 13, 439-447. doi: 10.1038/ nm1548
23. Lin, C. H., Lee, H. T., Lee, S. D., Lee, W., Cho, C. W., Lin, S. Z., et al. (2013). Role of HIF-1alpha-activated Epac1 on HSC-mediated neuroplasticity in stroke model. Neurobiol. Dis. 58C, 76-91. doi: 10.1016/j.nbd.2013.05.006
24. Liu, Z., Li, Y., Zhang, R. L., Cui, Y., and Chopp, M. (2011). Bone marrow stromal cells promote skilled motor recovery and enhance contralesional axonal connections after ischemic stroke in adult mice. Stroke 42, 740-744. doi: 10.1161/STROKEAHA.110.607226
25. Ma, D. K., Marchetto, M. C., Guo, J. U., Ming, G. L., Gage, F. H., and Song, H. (2010). Epigenetic choreographers of neurogenesis in the adult mammalian brain. Nat. Neurosci. 13, 1338-1344. doi: 10.1038/nn.2672
26. Mazzocchi-Jones, D., Döbrössy, M., and Dunnet, S. B. (2009). Embryonic striatal grafts restore bi-directional synaptic plasticity in a rodent model of Huntington's disease. Eur. J. Neurosci. 30, 2134-2142. doi: 10.1111/j.1460-9568.2009.07006.x
27. Mezey, E. (2011). The therapeutic potential of bone marrow-derived stem cells. J. Cell. Biochem. 112, 2683-2687. doi: 10.1002/jcb.23216
28. Park, K. P., Rosell, A., Foerch, C., Xing, C., Kim, W. J., Lee, S., et al. (2009). Plasma and brain matrix metalloproteinase-9 after acute focal cerebral ischemia in rats. Stroke 40, 2836-2842. doi: 10.1161/STROKEAHA.109.554824
29. Pastori, C., Librizzi, L., Breschi, G. L., Regondi, C., Frassoni, C., Panzica, F., et al. (2008). Arterially perfused neurosphere-derived cells distribute outside the ischemic core in a model of transient focal ischemia and reperfusion in vitro. PLoS ONE 3:e2754. doi: 10.1371/journal.pone.0002754
30. Pollock, K., Stroemer, P., Patel, S., Stevanato, L., Hope, A., Miljan, E., et al. (2006). A conditionally immortal clonal stem cell line form human cortical neuroepithelium for the treatment of ischemic stroke. Exp. Neurol. 199, 143-155. doi: 10.1016/j.expneurol.2005.12.011
31. Redmond, D. E. Jr, Bjugstad, K. B., Teng, Y. D., Ourednik, V., Ourednik, J., Wakeman, D. R., et al. (2007). Behavioral improvement in a primate Parkinson's model is associated with multiple homeostatic effects of human neural stem cells. Proc. Natl. Acad. Sci. U.S.A. 104, 12175-12180. doi: 10.1073/pnas.0704091104
32. Robel, S., Berninger, B., and Gotz, M. (2011). The stem cell potential of glia: lessons from reactive gliosis. Nat. Rev. Neurosci. 12, 88-104. doi: 10.1038/nrn2978
33. Roet, K. C., Franssen, E. H., de Bree, F. M., Essing, A. H., Zijlstra, S. J., Fagoe, N. D., et al. (2013). A multilevel screening strategy defines a molecular fingerprint of proregenerative olfactory ensheathing cells and identifies SCARB2, a protein that improves regenerative sprouting of injured sensory spinal axons. J. Neurosci. 33, 11116-11135. doi: 10.1523/JNEUROSCI.1002-13.2013
34. Sanai, N., Nguyen, T., Ihrie, R. A., Mirzadeh, Z., Tsai, H. H., Wong, M., et al. (2011). Corridors of migrating neurons in the human brain and their decline during infancy. Nature 478, 382-386. doi: 10.1038/nature10487
35. Seol, H. J., Jin, J., Seong, D. H., Joo, K. M., Kang, W., Yang, H., et al. (2011). Genetically engineered human neural stem cells with rabbit carboxyl esterase can target brain metastasis from breast cancer. Cancer Lett. 311, 152-159. doi: 10.1016/j.canlet.2011.07.001
36. Snyder, E. Y., Yoon, C., Flax, J. D., and Macklis, J. D. (1997). 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, 11663-11668. doi: 10.1073/pnas.94.21.11663
37. Sobrino, T., Perez-Mato, M., Brea, D., Rodriguez-Yanez, M., Blanco, M., and Castillo, J. (2012). Temporal profile of molecular signatures associated with circulating endothelial progenitor cells in human ischemic stroke. J. Neurosci. Res. 90, 1788-1793. doi: 10.1002/jnr.23068
38. Tajiri, N., Acosta, S., Glover, L. E., Bickford, P. C., Jacotte Simancas, A., Yasuhara, T., et al. (2012) Intravenous grafts of amniotic fluid-derived stem cells induce endogenous cell proliferation and attenuate behavioral deficits in ischemic stroke rats. PLoS ONE 7:e43779. doi: 10.1371/journal.pone.0043779
39. Tajiri, N., Kaneko, Y., Shinozuka, K., Ishikawa, H., Yankee, E., McGrogan, M., et al. (2013). Stem cell recruitment of newly formed host cells via a successful seduction? Filling the gap between neurogenic niche and injured brain site. PLoS ONE 8:e74857. doi: 10.1371/journal.pone.0074857
40. Tang, F. I., Tien, L. T., Zhou, F. C., Hoffer, B. J., and Wang, Y. (1998). Intranigral ventral mesencephalic grafts and nigrostriatal injections of glial cell line-derived neurotrophic factor restore dopamine release in the striatum of 6-hydroxydopamine-lesioned rats. Exp. Brain Res. 119, 287-296. doi: 10.1007/s002210050344
41. Trueman, R. C., Klein, A., Lindgren, H. S., Lelos, M. J., and Dunnett, S. B. (2013). Repair of the CNS using endogenous and transplanted neural stem cells. Curr. Top. Behav. Neurosci. 15, 357-398. doi: 10.1007/7854_2012_223
42. Wang, L., Chopp, M., Teng, H., Bolz, M., Francisco, M. A., Aluigi, D. M., et al. (2011). Tumor necrosis factor α primes cerebral endothelial cells for erythropoietin-induced angiogenesis. J. Cereb. Blood Flow Metab. 31, 640-647. doi: 10.1038/jcbfm.2010.138
43. Wang, X., Mao, X., Xie, L., Sun, F., Greenberg, D. A., and Jin, K. (2012). Conditional depletion of neurogenesis inhibits long-term recovery after experimental stroke in mice. PLoS ONE 7:e38932. doi: 10.1371/journal.pone.0038932
44. Wang, Y., Tien, L. T., Lapchak, P. A., and Hoffer, B. J. (1996). GDNF triggers fiber outgrowth of fetal ventral mesencephalic grafts from nigra to striatum in 6-OHDA-lesioned rats. Cell Tissue Res. 286, 225-233. doi: 10.1007/s004410050691
45. Wolf, K., Te Lindert, M., Krause, M., Alexander, S., Te Riet, J., Willis, A. L., et al. (2013). Physical limits of cell migration: control by ECM space and nuclear deformation and tuning by proteolysis and traction force. J. Cell Biol. 201, 1069-1084. doi: 10.1083/jcb.201210152
46. Yasuda, A., Tsuji, O., Shibata, S., Nori, S., Takano, M., Kobayashi, Y., et al. (2011). Significance of remyelination by neural stem/progenitor cells transplanted into the injured spinal cord. Stem Cell 29, 1983-1994. doi: 10.1002/stem.767
47. Yasuhara, T., Hara, K., Maki, M., Mays, R. W., Deans, R. J., Hess, D. C., et al. (2008). Intravenous grafts recapitulate the neurorestoration afforded by intracerebrally delivered multipotent adult progenitor cells in neonatal hypoxic-ischemic rats. J. Cereb. Blood Flow Metab. 28, 1804-1810. doi: 10.1038/jcbfm.2008.68
48. Yasuhara, T., Matsukawa, N., Hara, K., Maki, M., Ali, M. M., Yu, S. J., et al. (2009). Notch-induced rat and human bone marrow stromal cell grafts reduce ischemic cell loss and ameliorate behavioral deficits in chronic stroke animals. Stem Cells Dev. 18, 1501-1514. doi: 10.1089/scd.2009.0011
49. Yasuhara, T., Matsukawa, N., Hara, K., Yu, G., Xu, L., Maki, M., et al. (2006). Transplantation of human neural stem cells exerts neuroprotection in a rat model of Parkinson's disease. J. Neurosci. 26, 12497-12511. doi: 10.1523/JNEUROSCI.3719-06.2006
50. Zhao, B. Q., Tejima, E., and Lo, E. H. (2007). Neurovascular proteases in brain injury, hemorrhage and remodeling after stroke. Stroke 38, 748-752. doi: 10.1161/01.STR.0000253500.32979.d1