Human neural stem cells induce functional myelination in mice with severe dysmyelination

Science Translational Medicine

Volumn 4, Issue 155, 2012, Pages

  Uchida, Nobuko ^a   Chen, Kevin ^b   Dohse, Monika ^a   Hansen, Kelly D ^b   Dean, Justin ^b   Buser, Joshua R ^b   Riddle, Art ^b   Beardsley, Douglas J ^b   Wan, Ying ^b   Gong, Xi ^b   Nguyen, Thuan ^c   Cummings, Brian J ^d   Anderson, Aileen J ^d   Tamaki, Stanley J ^a   Tsukamoto, Ann ^a   Weissman, Irving L ^e   Matsumoto, Steven G ^f   Sherman, Larry S ^f   Kroenke, Christopher D ^c,g   Back, Stephen A ^b,g  

^a StemCells Inc   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^g OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MYELIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CELL DIFFERENTIATION; CELL STRUCTURE; CONTROLLED STUDY; EX VIVO STUDY; FRACTIONAL ANISOTROPY; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HYPOMYELINATION; MOUSE; MYELIN DEFICIENCY; MYELINATION; NERVE CONDUCTION; NEURAL STEM CELL TRANSPLANTATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OLIGODENDROGLIA; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; ULTRASTRUCTURE;

ANIMALS; BRAIN; CENTRAL NERVOUS SYSTEM; DEMYELINATING DISEASES; HUMANS; IMMUNOHISTOCHEMISTRY; MAGNETIC RESONANCE IMAGING; MICE; MYELIN SHEATH; NEURAL STEM CELLS; STEM CELL TRANSPLANTATION;

EID: 84867452128     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3004371     Document Type: Article

References (53)

1. K. A. Nave, Myelination and the trophic support of long axons. Nat. Rev. Neurosci. 11, 275-283 (2010).
2. I. D. Duncan, Y. Kondo, S. C. Zhang, The myelin mutants as models to study myelin repair in the leukodystrophies. Neurotherapeutics 8, 607-624 (2011).
3. A. Roach, N. Takahashi, D. Pravtcheva, F. Ruddle, L. Hood, Chromosomal mapping of mouse myelin basic protein gene and structure and transcription of the partially deleted gene in shiverer mutant mice. Cell 42, 149-155 (1985).
4. M. Katsuki, M. Sato, M. Kimura, M. Yokoyama, K. Kobayashi, T. Nomura, Conversion of normal behavior to shiverer by myelin basic protein antisense cDNA in transgenic mice. Science 241, 593-595 (1988).
5. A. Gansmuller, E. Clerin, F. Krüger, M. Gumpel, F. Lachapelle, Tracing transplanted oligodendrocytes during migration and maturation in the shiverer mouse brain. Glia 4, 580-590 (1991).
6. P. M. Mathisen, S. Pease, J. Garvey, L. Hood, C. Readhead, Identification of an embryonic isoform of myelin basic protein that is expressed widely in the mouse embryo. Proc. Natl. Acad. Sci. U.S.A. 90, 10125-10129 (1993).
7. M. S. Windrem, M. C. Nunes, W. K. Rashbaum, T. H. Schwartz, R. A. Goodman, G. McKhann II, N. S. Roy, S. A. Goldman, Fetal and adult human oligodendrocyte progenitor cell isolates myelinate the congenitally dysmyelinated brain. Nat. Med. 10, 93-97 (2004).
8. M. S. Windrem, S. J. Schanz, M. Guo, G. F. Tian, V. Washco, N. Stanwood, M. Rasband, N. S. Roy, M.Nedergaard, L. A. Havton, S. Wang, S. A. Goldman, Neonatal chimerizationwith human glial progenitor cells can both remyelinate and rescue the otherwise lethally hypomyelinated shiverer mouse. Cell Stem Cell 2, 553-565 (2008).
9. N. Uchida, D. W. Buck, D. He, M. J. Reitsma, M. Masek, T. V. Phan, A. S. Tsukamoto, F. H. Gage, I. L. Weissman, Direct isolation of human central nervous system stem cells. Proc. Natl. Acad. Sci. U.S.A. 97, 14720-14725 (2000).
10. S. Kelly, T. M. Bliss, A. K. Shah, G. H. Sun, M. Ma, W. C. Foo, J. Masel, M. A. Yenari, I. L. Weissman, N. Uchida, T. Palmer, G. K. Steinberg, Transplanted human fetal neural stem cells survive, migrate, and differentiate in ischemic rat cerebral cortex. Proc. Natl. Acad. Sci. U.S.A. 101, 11839-11844 (2004).
11. B. J. Cummings, N. Uchida, S. J. Tamaki, D. L. Salazar, M. Hooshmand, R. Summers, F. H. Gage, A. J. Anderson, Human neural stem cells differentiate and promote locomotor recovery in spinal cord-injured mice. Proc. Natl. Acad. Sci. U.S.A. 102, 14069-14074 (2005).
12. R. Guzman, N. Uchida, T. M. Bliss, D. He, K. K. Christopherson, D. Stellwagen, A. Capela, J. Greve, R. C. Malenka, M. E. Moseley, T. D. Palmer, G. K. Steinberg, Long-term monitoring of transplanted human neural stem cells in developmental and pathological contexts with MRI. Proc. Natl. Acad. Sci. U.S.A. 104, 10211-10216 (2007).
13. S. J. Tamaki, Y. Jacobs, M. Dohse, A. Capela, J. D. Cooper, M. Reitsma, D. He, R. Tushinski, P. V. Belichenko, A. Salehi, W. Mobley, F. H. Gage, S. Huhn, A. S. Tsukamoto, I. L. Weissman, N. Uchida, Neuroprotection of host cells by human central nervous system stem cells in a mouse model of infantile neuronal ceroid lipofuscinosis. Cell Stem Cell 5, 310-319 (2009).
14. D. L. Salazar, N. Uchida, F. P. Hamers, B. J. Cummings, 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, e12272 (2010).
15. N. Horie, M. P. Pereira, K. Niizuma, G. Sun, H. Keren-Gill, A. Encarnacion, M. Shamloo, S. A. Hamilton, K. Jiang, S. Huhn, T. D. Palmer, T. M. Bliss, G. K. Steinberg, Transplanted stem cell-secreted vascular endothelial growth factor effects poststroke recovery, inflammation, and vascular repair. Stem Cells 29, 274-285 (2011).
16. T. J. McGill, B. Cottam, B. Lu, S. Wang, S. Girman, C. Tian, S. L. Huhn, R. D. Lund, A. Capela, Transplantation of human central nervous system stem cells - Neuroprotection in retinal degeneration. Eur. J. Neurosci. 35, 468-477 (2012).
17. M. J. Hooshmand, C. J. Sontag, N. Uchida, S. Tamaki, A. J. Anderson, 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, e5871 (2009).
18. L. Hook, J. Vives, N. Fulton, M. Leveridge, S. Lingard, M. D. Bootman, A. Falk, S. M. Pollard, T. E. Allsopp, D. Dalma-Weiszhausz, A. Tsukamoto, N. Uchida, T. Gorba, Non-immortalized human neural stem (NS) cells as a scalable platform for cellular assays. Neurochem. Int. 59, 432-444 (2011).
19. S. Tamaki, K. Eckert, D. He, R. Sutton, M. Doshe, G. Jain, R. Tushinski, M. Reitsma, B. Harris, A. Tsukamoto, F. Gage, I. Weissman, N. Uchida, Engraftment of sorted/expanded human central nervous system stem cells from fetal brain. J. Neurosci. Res. 69, 976-986 (2002).
20. J. Steiner, H. G. Bernstein, H. Bielau, A. Berndt, R. Brisch, C. Mawrin, G. Keilhoff, B. Bogerts, Evidence for a wide extra-astrocytic distribution of S100B in human brain. BMC Neurosci. 8, 2 (2007).
21. S. Hachem, A. Aguirre, V. Vives, A. Marks, V. Gallo, C. Legraverend, Spatial and temporal expression of S100B in cells of oligodendrocyte lineage. Glia 51, 81-97 (2005).
22. +channel expression in mouse mutants shiverer and Trembler . Neuron 15, 1337-1347 (1995).
23. K. Sinha, S. Karimi-Abdolrezaee, A. A. Velumian, M. G. Fehlings, Functional changes in genetically dysmyelinated spinal cord axons of shiverer mice: Role of juxtaparanodal Kv1 family K+ channels. J. Neurophysiol. 95, 1683-1695 (2006).
24. B. Trapp, S. Pfeiffer, M. Anitei, J. Kidd, in Myelin Biology and Disorders, R. Lazzarini, Ed. (Elsevier Academic Press, San Diego, CA, 2004), pp. 29-55.
25. C. Readhead, N. Takasashi, H. D. Shine, R. Saavedra, R. Sidman, L. Hood, Role of myelin basic protein in the formation of central nervous system myelin. Ann. N. Y. Acad. Sci. 605, 280-285 (1990).
26. D. K. Crawford, M. Mangiardi, S. K. Tiwari-Woodruff, Assaying the functional effects of demyelination and remyelination: Revisiting field potential recordings. J. Neurosci. Methods 182, 25-33 (2009).
27. S. Mori, J. Zhang, Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron 51, 527- 539 (2006).
28. S. P. Miller, D. M. Ferriero, From selective vulnerability to connectivity: Insights from newborn brain imaging. Trends Neurosci. 32, 496-505 (2009).
29. D. J. Costello, A. F. Eichler, F. S. Eichler, Leukodystrophies: Classification, diagnosis, and treatment. Neurologist 15, 319-328 (2009).
30. S. T. Brady, A. S. Witt, L. L. Kirkpatrick, S. M. de Waegh, C. Readhead, P. H. Tu, V. M. Lee, Formation of compact myelin is required for maturation of the axonal cytoskeleton. J. Neurosci. 19, 7278-7288 (1999).
31. J. Rosenbluth, Central myelin in the mouse mutant shiverer. J. Comp. Neurol. 194, 639-648 (1980).
32. H. Andrews, K. White, C. Thomson, J. Edgar, D. Bates, I. Griffiths, D. Turnbull, P. Nichols, Increased axonal mitochondrial activity as an adaptation to myelin deficiency in the Shiverer mouse. J. Neurosci. Res. 83, 1533-1539 (2006).
33. D. Pitt, E. Gonzales, A. H. Cross, M. P. Goldberg, Dysmyelinated axons in shiverer mice are highly vulnerable to a-amino-3-hydroxy-5-methylisoxazole-4- propionic acid (AMPA) receptor-mediated toxicity. Brain Res. 1309, 146-154 (2010).
34. + glial cell proliferation and oligodendrocyte generation in the hypomyelinating mutant shiverer. Glia 48, 51-63 (2004).
35. A. Craig, N. Ling Luo, D. J. Beardsley, N. Wingate-Pearse, D. W. Walker, A. R. Hohimer, S. A. Back, Quantitative analysis of perinatal rodent oligodendrocyte lineage progression and its correlation with human. Exp. Neurol. 181, 231-240 (2003).
36. S. A. Back, N. L. Luo, N. S. Borenstein, J. J. Volpe, H. C. Kinney, Arrested oligodendrocyte lineage progression during human cerebral white matter development: Dissociation between the timing of progenitor differentiation and myelinogenesis. J. Neuropathol. Exp. Neurol. 61, 197-211 (2002).
37. G. Nair, Y. Tanahashi, H. P. Low, S. Billings-Gagliardi, W. J. Schwartz, T. Q. Duong, Myelination and long diffusion times alter diffusion-tensor-imaging contrast in myelin-deficient shiverer mice. Neuroimage 28, 165-174 (2005).
38. M. Hoehn, E. Küstermann, J. Blunk, D. Wiedermann, T. Trapp, S. Wecker, M. Föcking, H. Arnold, J. Hescheler, B. K. Fleischmann, W. Schwindt, C. Bührle, Monitoring of implanted stem cell migration in vivo: A highly resolved in vivo magnetic resonance imaging investigation of experimental stroke in rat. Proc. Natl. Acad. Sci. U.S.A. 99, 16267-16272 (2002).
39. E. M. Shapiro, K. Sharer, S. Skrtic, A. P. Koretsky, In vivo detection of single cells by MRI. Magn. Reson. Med. 55, 242-249 (2006).
40. N. Gupta, R. G. Henry, J. Strober, S. M. Kang, D. Lim, M. Bucci, E. Caverzasi, L. Gaetano, M. L. Mandelli, T. Ryan, R. Perry, J. Farrell, R. J. Jeremy, M. Ulman, S. L. Huhn, A. J. Barkovich, D. H. Rowitch, Neural stem cell engraftment and myelination in the human brain. Sci. Transl. Med. 4, 155ra137 (2012).
41. J. R. Buser, J. Maire, A. Riddle, X. Gong, T. Nguyen, K. Nelson, N. L. Luo, J. Ren, J. Struve, L. S. Sherman, S. P. Miller, V. Chau, G. Hendson, P. Ballabh, M. R. Grafe, S. A. Back, Arrested preoligodendrocyte maturation contributes to myelination failure in premature infants. Ann. Neurol. 71, 93-109 (2012).
42. J. Gerdes, H. Lemke, H. Baisch, H. H. Wacker, U. Schwab, H. Stein, Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal antibody Ki-67. J. Immunol. 133, 1710-1715 (1984).
43. 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 (Pt. 6), 1253-1263 (1996).
44. T. M. Reeves, L. L. Phillips, J. T. Povlishock, Myelinated and unmyelinated axons of the corpus callosum differ in vulnerability and functional recovery following traumatic brain injury. Exp. Neurol. 196, 126-137 (2005).
45. C. D. Kroenke, G. L. Bretthorst, T. E. Inder, J. J. Neil, Diffusion MR imaging characteristics of the developing primate brain. Neuroimage 25, 1205-1213 (2005).
46. C. D. Kroenke, E. N. Taber, L. A. Leigland, A. K. Knutsen, P. V. Bayly, Regional patterns of cerebral cortical differentiation determined by diffusion tensor MRI. Cereb. Cortex 19, 2916-2929 (2009).
47. S. W. Sun, J. J. Neil, H. F. Liang, Y. Y. He, R. E. Schmidt, C. Y. Hsu, S. K. Song, Formalin fixation alters water diffusion coefficient magnitude but not anisotropy in infarcted brain. Magn. Reson. Med. 53, 1447-1451 (2005).
48. P. G. Batchelor, D. Atkinson, D. L. Hill, F. Calamante, A. Connelly, Anisotropic noise propagation in diffusion tensor MRI sampling schemes. Magn. Reson. Med. 49, 1143-1151 (2003).
49. P. J. Basser, C. Pierpaoli, Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J. Magn. Reson. B 111, 209-219 (1996).
50. S. Pieper, B. Lorensen, W. Schroeder, R. Kikinis, The NA-MIC Kit: ITK, VTK, pipelines, grids and 3D slicer as an open platform for the medical image computing community, Proceedings of the 3rd IEEE International Symposium on Biomedical Imaging: Nano to Macro, Arlington, VA, 6 to 9 April 2006, 698-701.
51. D. T. Gering, A. Nabavi, R. Kikinis, N. Hata, L. J. O'Donnell, W. E. Grimson, F.A. Jolesz, P.M. Black, W. M. Wells III, An integrated visualization system for surgical planning and guidance using image fusion and an open MR. J. Magn. Reson. Imaging 13, 967-975 (2001).
52. P. A. Yushkevich, J. Piven, H. C. Hazlett, R. G. Smith, S. Ho, J. C. Gee, G. Gerig, User-guided 3D active contour segmentation of anatomical structures: Significantly improved efficiency and reliability. Neuroimage 31, 1116-1128 (2006).
53. S. A. Back, A. Craig, N. L. Luo, J. Ren, R. S. Akundi, I. Ribeiro, S. A. Rivkees, Protective effects of caffeine on chronic hypoxia-induced perinatal white matter injury. Ann. Neurol. 60, 696-705 (2006).