Engrafted Neural Stem/Progenitor Cells Promote Functional Recovery through Synapse Reorganization with Spared Host Neurons after Spinal Cord Injury

Stem Cell Reports

Volumn 5, Issue 2, 2015, Pages 264-277

  Yokota, Kazuya ^a   Kobayakawa, Kazu ^a   Kubota, Kensuke ^a   Miyawaki, Atsushi ^b   Okano, Hideyuki ^c   Ohkawa, Yasuyuki ^d   Iwamoto, Yukihide ^a   Okada, Seiji ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^c KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^d KYUSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

2',3' CYCLIC NUCLEOTIDE 3' PHOSPHODIESTERASE; DCX PROTEIN; GAP43 PROTEIN; GFAP PROTEIN; GLUTAMATE DECARBOXYLASE 65; GLUTAMATE DECARBOXYLASE 67; MICROTUBULE ASSOCIATED PROTEIN 2; N METHYL DEXTRO ASPARTIC ACID; NEUROGENIC DIFFERENTIATION FACTOR; PROTEIN; PROTEIN C FOS; PROTEIN HOMER 1; TRANSCRIPTION FACTOR MASH1; TUBB3 PROTEIN; UNCLASSIFIED DRUG; VESICULAR GLUTAMATE TRANSPORTER 1; VESICULAR GLUTAMATE TRANSPORTER 2; VESICULAR INHIBITORY AMINO ACID TRANSPORTER;

ACTION POTENTIAL; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ENGRAFTMENT; FEMALE; GENE EXPRESSION; HISTOPATHOLOGY; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; INJURY SEVERITY; LASER MICRODISSECTION; MOTONEURON; MOUSE; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL TRANSPLANTATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPINAL CORD INJURY; SYNAPSE; SYNAPTIC TRANSMISSION; ANIMAL; C57BL MOUSE; CELL CULTURE; CYTOLOGY; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; PHYSIOLOGY; SPINAL CORD INJURIES; STEM CELL TRANSPLANTATION; TRANSPLANTATION;

ANIMALS; CELLS, CULTURED; FEMALE; MICE; MICE, INBRED C57BL; NEURAL STEM CELLS; NEUROGENESIS; NEURONS; SPINAL CORD INJURIES; STEM CELL TRANSPLANTATION; SYNAPSES;

EID: 84954186615     PISSN: 22136711     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stemcr.2015.06.004     Document Type: Article

References (37)

1. M. Abematsu, K. Tsujimura, M. Yamano, M. Saito, K. Kohno, J. Kohyama, M. Namihira, S. Komiya, and K. Nakashima Neurons derived from transplanted neural stem cells restore disrupted neuronal circuitry in a mouse model of spinal cord injury J. Clin. Invest. 120 2010 3255 3266
2. F.M. Bareyre, M. Kerschensteiner, O. Raineteau, T.C. Mettenleiter, O. Weinmann, and M.E. Schwab The injured spinal cord spontaneously forms a new intraspinal circuit in adult rats Nat. Neurosci. 7 2004 269 277
3. S. Bolsover, J. Fabes, and P.N. Anderson Axonal guidance molecules and the failure of axonal regeneration in the adult mammalian spinal cord Restor. Neurol. Neurosci. 26 2008 117 130
4. E.J. Bradbury, and S.B. McMahon Spinal cord repair strategies: why do they work? Nat. Rev. Neurosci. 7 2006 644 653
5. I.J. Cajigas, G. Tushev, T.J. Will, S. tom Dieck, N. Fuerst, and E.M. Schuman The local transcriptome in the synaptic neuropil revealed by deep sequencing and high-resolution imaging Neuron 74 2012 453 466
6. S. Cohen, and M.E. Greenberg Communication between the synapse and the nucleus in neuronal development, plasticity, and disease Annu. Rev. Cell Dev. Biol. 24 2008 183 209
7. J.A. Coleman, L.A. Harper, P.B. Perrin, S.L. Olivera, J.L. Perdomo, J.A. Arango, and J.C. Arango-Lasprilla The relationship between physical and mental health variables in individuals with spinal cord injury from Latin America PM R 7 2015 9 16
8. A.C. Conta, and D.J. Stelzner Differential vulnerability of propriospinal tract neurons to spinal cord contusion injury J. Comp. Neurol. 479 2004 347 359
9. G. Courtine, B. Song, R.R. Roy, H. Zhong, J.E. Herrmann, Y. Ao, J. Qi, V.R. Edgerton, and M.V. Sofroniew Recovery of supraspinal control of stepping via indirect propriospinal relay connections after spinal cord injury Nat. Med. 14 2008 69 74
10. 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
11. M. Cusimano, D. Biziato, E. Brambilla, M. Donega, C. Alfaro-Cervello, S. Snider, G. Salani, F. Pucci, G. Comi, J.M. Garcia-Verdugo, and et al. Transplanted neural stem/precursor cells instruct phagocytes and reduce secondary tissue damage in the injured spinal cord Brain 135 2012 447 460
12. B.H. Dobkin, A. Curt, and J. Guest Cellular transplants in China: observational study from the largest human experiment in chronic spinal cord injury Neurorehabil. Neural Repair 20 2006 5 13
13. J.P. Doyle, J.D. Dougherty, M. Heiman, E.F. Schmidt, T.R. Stevens, G. Ma, S. Bupp, P. Shrestha, R.D. Shah, M.L. Doughty, and et al. Application of a translational profiling approach for the comparative analysis of CNS cell types Cell 135 2008 749 762
14. T. Fares, and A. Stepanyants Cooperative synapse formation in the neocortex Proc. Natl. Acad. Sci. USA 106 2009 16463 16468
15. S.D. Fenster, W.J. Chung, R. Zhai, C. Cases-Langhoff, B. Voss, A.M. Garner, U. Kaempf, S. Kindler, E.D. Gundelfinger, and C.C. Garner Piccolo, a presynaptic zinc finger protein structurally related to bassoon Neuron 25 2000 203 214
16. S.W. Flavell, and M.E. Greenberg Signaling mechanisms linking neuronal activity to gene expression and plasticity of the nervous system Annu. Rev. Neurosci. 31 2008 563 590
17. J.R. Flynn, B.A. Graham, M.P. Galea, and R.J. Callister The role of propriospinal interneurons in recovery from spinal cord injury Neuropharmacology 60 2011 809 822
18. A. Garg, D.D. Houlihan, V. Aldridge, S. Suresh, K.K. Li, A.L. King, R. Sutaria, J. Fear, R.H. Bhogal, P.F. Lalor, and P.N. Newsome Non-enzymatic dissociation of human mesenchymal stromal cells improves chemokine-dependent migration and maintains immunosuppressive function Cytotherapy 16 2014 545 559
19. J.S. Harrop, R. Hashimoto, D. Norvell, A. Raich, B. Aarabi, R.G. Grossman, J.D. Guest, C.H. Tator, J. Chapman, and M.G. Fehlings Evaluation of clinical experience using cell-based therapies in patients with spinal cord injury: a systematic review J. Neurosurg. Spine 17 1, Suppl 2012 230 246
20. A. Jacobi, A. Schmalz, and F.M. Bareyre Abundant expression of guidance and synaptogenic molecules in the injured spinal cord PLoS One 9 2014 e88449
21. M. Kinoshita, R. Matsui, S. Kato, T. Hasegawa, H. Kasahara, K. Isa, A. Watakabe, T. Yamamori, Y. Nishimura, B. Alstermark, and et al. Genetic dissection of the circuit for hand dexterity in primates Nature 487 2012 235 238
22. K. Kobayakawa, H. Kumamaru, H. Saiwai, K. Kubota, Y. Ohkawa, J. Kishimoto, K. Yokota, R. Ideta, K. Shiba, H. Tozaki-Saitoh, and et al. Acute hyperglycemia impairs functional improvement after spinal cord injury in mice and humans Sci. Transl. Med. 6 2014 256ra137
23. H. Krueger, V.K. Noonan, L.M. Trenaman, P. Joshi, and C.S. Rivers The economic burden of traumatic spinal cord injury in Canada Chronic Dis. Inj. Can. 33 2013 113 122
24. H. Kumamaru, Y. Ohkawa, H. Saiwai, H. Yamada, K. Kubota, K. Kobayakawa, K. Akashi, H. Okano, Y. Iwamoto, and S. Okada Direct isolation and RNA-seq reveal environment-dependent properties of engrafted neural stem/progenitor cells Nat. Commun. 3 2012 1140
25. O. Lindvall, and Z. Kokaia Stem cells in human neurodegenerative disorders - time for clinical translation? J. Clin. Invest. 120 2010 29 40
26. M.K. Lobo, S.L. Karsten, M. Gray, D.H. Geschwind, and X.W. Yang FACS-array profiling of striatal projection neuron subtypes in juvenile and adult mouse brains Nat. Neurosci. 9 2006 443 452
27. P. Lu, Y. Wang, L. Graham, K. McHale, M. Gao, D. Wu, J. Brock, A. Blesch, E.S. Rosenzweig, L.A. Havton, and et al. Long-distance growth and connectivity of neural stem cells after severe spinal cord injury Cell 150 2012 1264 1273
28. A.J. Mothe, and C.H. Tator Review of transplantation of neural stem/progenitor cells for spinal cord injury Int. J. Dev. Neurosci. 31 2013 701 713
29. S. Nishimura, A. Yasuda, H. Iwai, M. Takano, Y. Kobayashi, S. Nori, O. Tsuji, K. Fujiyoshi, H. Ebise, Y. Toyama, and et al. Time-dependent changes in the microenvironment of injured spinal cord affects the therapeutic potential of neural stem cell transplantation for spinal cord injury Mol. Brain 6 2013 3
30. S. Nori, Y. Okada, A. Yasuda, O. Tsuji, Y. Takahashi, Y. Kobayashi, K. Fujiyoshi, M. Koike, Y. Uchiyama, E. Ikeda, and 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
31. S. Okada, K. Ishii, J. Yamane, A. Iwanami, T. Ikegami, H. Katoh, Y. Iwamoto, M. Nakamura, H. Miyoshi, H.J. Okano, and et al. In vivo imaging of engrafted neural stem cells: its application in evaluating the optimal timing of transplantation for spinal cord injury FASEB J. 19 2005 1839 1841
32. G.V. Seledtsova, S.S. Rabinovich, S.N. Belogorodtsev, O.V. Parlyuk, V.I. Seledtsov, and V.A. Kozlov Delayed results of transplantation of fetal neurogenic tissue in patients with consequences of spinal cord trauma Bull. Exp. Biol. Med. 149 2010 530 533
33. P.K. Shah, G. Garcia-Alias, J. Choe, P. Gad, Y. Gerasimenko, N. Tillakaratne, H. Zhong, R.R. Roy, and V.R. Edgerton Use of quadrupedal step training to re-engage spinal interneuronal networks and improve locomotor function after spinal cord injury Brain 136 2013 3362 3377
34. T.C. Südhof Neurotransmitter release: the last millisecond in the life of a synaptic vesicle Neuron 80 2013 675 690
35. 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, L.J. Smithson, and et al. A systematic review of cellular transplantation therapies for spinal cord injury J. Neurotrauma 28 2011 1611 1682
36. V. Volarevic, S. Erceg, S.S. Bhattacharya, P. Stojkovic, P. Horner, and M. Stojkovic Stem cell-based therapy for spinal cord injury Cell Transplant. 22 2013 1309 1323
37. K.H. Zivraj, Y.C. Tung, M. Piper, L. Gumy, J.W. Fawcett, G.S. Yeo, and C.E. Holt Subcellular profiling reveals distinct and developmentally regulated repertoire of growth cone mRNAs J. Neurosci. 30 2010 15464 15478