Injury to the spinal cord niche alters the engraftment dynamics of human neural stem cells

Stem Cell Reports

Volumn 2, Issue 5, 2014, Pages 620-632

  Sontag, Christopher J ^a,b   Uchida, Nobuko ^c   Cummings, Brian J ^a,b   Anderson, Aileen J ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c StemCells Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL DIFFERENTIATION; CELL FATE; CELL MATURATION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENGRAFTMENT; FEMALE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; LIMIT OF QUANTITATION; MOUSE; NEURAL STEM CELL; NEURAL STEM CELL TRANSPLANTATION; NONHUMAN; PRIORITY JOURNAL; SINGLE BLIND PROCEDURE; SPINAL CORD INJURY; STEM CELL NICHE; ADULT; ANIMAL CELL; CELL ISOLATION; CELL LOSS; COMPARATIVE STUDY; HISTOLOGY; OLIGODENDROGLIA; ANIMAL; CELL LINEAGE; CELL MOTION; CYTOLOGY; NONOBESE DIABETIC MOUSE; PATHOLOGY; SCID MOUSE; SPINAL CORD INJURIES; THREE DIMENSIONAL IMAGING; TIME; TRANSPLANTATION; XENOGRAFT;

BROXURIDINE; CASPASE 3;

MUS;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CELL MOVEMENT; CELL PROLIFERATION; HUMANS; IMAGING, THREE-DIMENSIONAL; MICE; MICE, INBRED NOD; MICE, SCID; NEURAL STEM CELLS; OLIGODENDROGLIA; SPINAL CORD INJURIES; TIME FACTORS; TRANSPLANTATION, HETEROLOGOUS;

EID: 84900306248     PISSN: 22136711     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stemcr.2014.03.005     Document Type: Article

References (55)

1. B.A. Aguado, W. Mulyasasmita, J. Su, K.J. Lampe, and S.C. Heilshorn Improving viability of stem cells during syringe needle flow through the design of hydrogel cell carriers Tissue Eng. Part A 18 2012 806 815
2. A.J. Anderson Mechanisms and pathways of inflammatory responses in CNS trauma: spinal cord injury J. Spinal Cord Med. 25 2002 70 79 discussion 80
3. A.J. Anderson, S. Robert, W. Huang, W. Young, and C.W. Cotman Activation of complement pathways after contusion-induced spinal cord injury J. Neurotrauma 21 2004 1831 1846
4. F. Barnabé-Heider, C. Göritz, H. Sabelström, H. Takebayashi, F.W. Pfrieger, K. Meletis, and J. Frisén Origin of new glial cells in intact and injured adult spinal cord Cell Stem Cell 7 2010 470 482
5. K.D. Beck, H.X. Nguyen, M.D. Galvan, D.L. Salazar, T.M. Woodruff, and A.J. Anderson Quantitative analysis of cellular inflammation after traumatic spinal cord injury: evidence for a multiphasic inflammatory response in the acute to chronic environment Brain 133 2010 433 447
6. J. Bullwinkel, B. Baron-Lühr, A. Lüdemann, C. Wohlenberg, J. Gerdes, and T. Scholzen Ki-67 protein is associated with ribosomal RNA transcription in quiescent and proliferating cells J. Cell. Physiol. 206 2006 624 635
7. Christopher & Dana Reeve Foundation. (2009). Prevalence of paralysis including spinal cord injuries in the United States. http://www. christopherreeve.org/site/c.mtKZKgMWKwG/b.5184255/k.6D74/Prevalence-of- Paralysis.htm.
8. B. Connor, R.J. Gordon, K.S. Jones, and C. Maucksch Deviating from the well travelled path: precursor cell migration in the pathological adult mammalian brain J. Cell. Biochem. 112 2011 1467 1474
9. B.J. Cummings, N. Uchida, S.J. Tamaki, D.L. Salazar, M. Hooshmand, R. Summers, F.H. Gage, and A.J. Anderson Human neural stem cells differentiate and promote locomotor recovery in spinal cord-injured mice Proc. Natl. Acad. Sci. USA 102 2005 14069 14074
10. B.J. Cummings, N. Uchida, S.J. Tamaki, and A.J. Anderson Human neural stem cell differentiation following transplantation into spinal cord injured mice: association with recovery of locomotor function Neurol. Res. 28 2006 474 481
11. B.J. Cummings, M.J. Hooshmand, D.L. Salazar, and A.J. Anderson Human neural stem cell-mediated repair of the contused spinal cord: Timing the microenvironment C. Ribak, From Development to Degneration and Regeneration of the Nervous System 2008 Oxford University Press New York 297 322
12. S. Das, and A. Basu Inflammation: a new candidate in modulating adult neurogenesis J. Neurosci. Res. 86 2008 1199 1208
13. I. Decimo, F. Bifari, M. Krampera, and G. Fumagalli Neural stem cell niches in health and diseases Curr. Pharm. Des. 18 2012 1755 1783
14. C.T. Ekdahl, Z. Kokaia, and O. Lindvall Brain inflammation and adult neurogenesis: the dual role of microglia Neuroscience 158 2009 1021 1029
15. B. Emery Regulation of oligodendrocyte differentiation and myelination Science 330 2010 779 782
16. B. Emery Transcriptional and post-transcriptional control of CNS myelination Curr. Opin. Neurobiol. 20 2010 601 607
17. C.M. Fernández-Martos, C. González-Fernández, P. González, A. Maqueda, E. Arenas, and F.J. Rodríguez Differential expression of Wnts after spinal cord contusion injury in adult rats PLoS ONE 6 2011 e27000
18. J.C. Fleming, M.D. Norenberg, D.A. Ramsay, G.A. Dekaban, A.E. Marcillo, A.D. Saenz, M. Pasquale-Styles, W.D. Dietrich, and L.C. Weaver The cellular inflammatory response in human spinal cords after injury Brain 129 2006 3249 3269
19. J. Gerdes, H. Lemke, H. Baisch, H.H. Wacker, U. Schwab, and H. Stein Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal antibody Ki-67 J. Immunol. 133 1984 1710 1715
20. M.J. Hooshmand, C.J. Sontag, N. Uchida, S. Tamaki, A.J. Anderson, and B.J. Cummings Analysis of host-mediated repair mechanisms after human CNS-stem cell transplantation for spinal cord injury: correlation of engraftment with recovery PLoS ONE 4 2009 e5871
21. C.B. Hurelbrink, R.J. Armstrong, S.B. Dunnett, A.E. Rosser, and R.A. Barker Neural cells from primary human striatal xenografts migrate extensively in the adult rat CNS Eur. J. Neurosci. 15 2002 1255 1266
22. T. Ikegami, M. Nakamura, J. Yamane, H. Katoh, S. Okada, A. Iwanami, K. Watanabe, K. Ishii, F. Kato, and H. Fujita et al. Chondroitinase ABC combined with neural stem/progenitor cell transplantation enhances graft cell migration and outgrowth of growth-associated protein-43-positive fibers after rat spinal cord injury Eur. J. Neurosci. 22 2005 3036 3046
23. S. Karimi-Abdolrezaee, E. Eftekharpour, J. Wang, D. Schut, and M.G. Fehlings Synergistic effects of transplanted adult neural stem/progenitor cells, chondroitinase, and growth factors promote functional repair and plasticity of the chronically injured spinal cord J. Neurosci. 30 2010 1657 1676
24. S. Karimi-Abdolrezaee, D. Schut, J. Wang, and M.G. Fehlings Chondroitinase and growth factors enhance activation and oligodendrocyte differentiation of endogenous neural precursor cells after spinal cord injury PLoS ONE 7 2012 e37589
25. M. Karus, S. Samtleben, C. Busse, T. Tsai, I.D. Dietzel, A. Faissner, and S. Wiese Normal sulfation levels regulate spinal cord neural precursor cell proliferation and differentiation Neural Dev. 7 2012 20
26. S.M. Kearns, E.D. Laywell, V.K. Kukekov, and D.A. Steindler Extracellular matrix effects on neurosphere cell motility Exp. Neurol. 182 2003 240 244
27. K.A. Kigerl, and P.G. Popovich Toll-like receptors in spinal cord injury Curr. Top. Microbiol. Immunol. 336 2009 121 136
28. K.A. Kigerl, W. Lai, S. Rivest, R.P. Hart, A.R. Satoskar, and P.G. Popovich Toll-like receptor (TLR)-2 and TLR-4 regulate inflammation, gliosis, and myelin sparing after spinal cord injury J. Neurochem. 102 2007 37 50
29. I.R. Kill Localisation of the Ki-67 antigen within the nucleolus. Evidence for a fibrillarin-deficient region of the dense fibrillar component J. Cell Sci. 109 1996 1253 1263
30. S.Y. Leong, and A.M. Turnley Regulation of adult neural precursor cell migration Neurochem. Int. 59 2011 382 393
31. S.C. Li, L.M. Tachiki, J. Luo, B.A. Dethlefs, Z. Chen, and W.G. Loudon A biological global positioning system: considerations for tracking stem cell behaviors in the whole body Stem Cell Rev. 6 2010 317 333
32. D.M. McTigue, P. Wei, and B.T. Stokes Proliferation of NG2-positive cells and altered oligodendrocyte numbers in the contused rat spinal cord J. Neurosci. 21 2001 3392 3400
33. A. Nishiyama, M. Komitova, R. Suzuki, and X. Zhu Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity Nat. Rev. Neurosci. 10 2009 9 22
34. S. Nori, Y. Okada, A. Yasuda, O. Tsuji, Y. Takahashi, Y. Kobayashi, K. Fujiyoshi, M. Koike, Y. Uchiyama, and E. Ikeda et al. Grafted human-induced pluripotent stem-cell-derived neurospheres promote motor functional recovery after spinal cord injury in mice Proc. Natl. Acad. Sci. USA 108 2011 16825 16830
35. D. Ogawa, Y. Okada, M. Nakamura, Y. Kanemura, H.J. Okano, Y. Matsuzaki, T. Shimazaki, M. Ito, E. Ikeda, and T. Tamiya et al. Evaluation of human fetal neural stem/progenitor cells as a source for cell replacement therapy for neurological disorders: properties and tumorigenicity after long-term in vitro maintenance J. Neurosci. Res. 87 2009 307 317
36. H. Okano, Y. Ogawa, M. Nakamura, S. Kaneko, A. Iwanami, and Y. Toyama Transplantation of neural stem cells into the spinal cord after injury Semin. Cell Dev. Biol. 14 2003 191 198
37. E. Okun, K.J. Griffioen, T.G. Son, J.H. Lee, N.J. Roberts, M.R. Mughal, E. Hutchison, A. Cheng, T.V. Arumugam, and J.D. Lathia et al. TLR2 activation inhibits embryonic neural progenitor cell proliferation J. Neurochem. 114 2010 462 474
38. S.C. Payne, C.A. Bartlett, D.L. Savigni, A.R. Harvey, S.A. Dunlop, and M. Fitzgerald Early proliferation does not prevent the loss of oligodendrocyte progenitor cells during the chronic phase of secondary degeneration in a CNS white matter tract PLoS ONE 8 2013 e65710
39. A. Petit, D.L. Sellers, D.J. Liebl, M. Tessier-Lavigne, T.E. Kennedy, and P.J. Horner Adult spinal cord progenitor cells are repelled by netrin-1 in the embryonic and injured adult spinal cord Proc. Natl. Acad. Sci. USA 104 2007 17837 17842
40. K.M. Piltti, D.L. Salazar, N. Uchida, B.J. Cummings, and A.J. Anderson Safety of epicenter versus intact parenchyma as a transplantation site for human neural stem cells for spinal cord injury therapy Stem Cells Transl. Med. 2 2013 204 216
41. K.M. Piltti, D.L. Salazar, N. Uchida, B.J. Cummings, and A.J. Anderson Safety of human neural stem cell transplantation in chronic spinal cord injury Stem Cells Transl. Med. 2 2013 961 974
42. P.G. Popovich, and T.B. Jones Manipulating neuroinflammatory reactions in the injured spinal cord: back to basics Trends Pharmacol. Sci. 24 2003 13 17
43. J.K. Sabo, T.J. Kilpatrick, and H.S. Cate Effects of bone morphogenic proteins on neural precursor cells and regulation during central nervous system injury Neurosignals 17 2009 255 264
44. D.L. Salazar, N. Uchida, F.P. Hamers, B.J. Cummings, and A.J. Anderson Human neural stem cells differentiate and promote locomotor recovery in an early chronic spinal cord injury NOD-scid mouse model PLoS ONE 5 2010 e12272
45. N. Sawhney, and P.A. Hall Ki67 - structure, function, and new antibodies J. Pathol. 168 1992 161 162
46. C.J. Sontag, H.X. Nguyen, N. Kamei, N. Uchida, A.J. Anderson, and B.J. Cummings Immunosuppressants affect human neural stem cells in vitro but not in an in vivo model of spinal cord injury Stem Cells Transl Med 2 2013 731 744
47. M. Starborg, K. Gell, E. Brundell, and C. Höög The murine Ki-67 cell proliferation antigen accumulates in the nucleolar and heterochromatic regions of interphase cells and at the periphery of the mitotic chromosomes in a process essential for cell cycle progression J. Cell Sci. 109 1996 143 153
48. R. Tanaka, M. Tainaka, T. Ota, N. Mizuguchi, H. Kato, S. Urabe, Y. Chen, J.M. Fustin, Y. Yamaguchi, and M. Doi et al. Accurate determination of S-phase fraction in proliferative cells by dual fluorescence and peroxidase immunohistochemistry with 5-bromo-2′-deoxyuridine (BrdU) and Ki67 antibodies J. Histochem. Cytochem. 59 2011 791 798
49. D.L. Taylor, G. Pirianov, S. Holland, C.J. McGinnity, A.L. Norman, C. Reali, L.T. Diemel, D. Gveric, D. Yeung, and H. Mehmet Attenuation of proliferation in oligodendrocyte precursor cells by activated microglia J. Neurosci. Res. 88 2010 1632 1644
50. W. Tetzlaff, E.B. Okon, S. Karimi-Abdolrezaee, C.E. Hill, J.S. Sparling, J.R. Plemel, W.T. Plunet, E.C. Tsai, D. Baptiste, and L.J. Smithson et al. A systematic review of cellular transplantation therapies for spinal cord injury J. Neurotrauma 28 2011 1611 1682
51. N. Uchida, D.W. Buck, D. He, M.J. Reitsma, M. Masek, T.V. Phan, A.S. Tsukamoto, F.H. Gage, and I.L. Weissman Direct isolation of human central nervous system stem cells Proc. Natl. Acad. Sci. USA 97 2000 14720 14725
52. F. Ulloa, and J. Briscoe Morphogens and the control of cell proliferation and patterning in the spinal cord Cell Cycle 6 2007 2640 2649
53. J. Yan, L. Xu, A.M. Welsh, G. Hatfield, T. Hazel, K. Johe, and V.E. Koliatsos Extensive neuronal differentiation of human neural stem cell grafts in adult rat spinal cord PLoS Med. 4 2007 e39
54. L.J. Zai, and J.R. Wrathall Cell proliferation and replacement following contusive spinal cord injury Glia 50 2005 247 257
55. C. Zhao, W. Deng, and F.H. Gage Mechanisms and functional implications of adult neurogenesis Cell 132 2008 645 660