Neural stem cell engraftment and myelination in the human brain

Science Translational Medicine

Volumn 4, Issue 155, 2012, Pages

  Gupta, Nalin ^a   Henry, Roland G ^a,b   Strober, Jonathan ^a   Kang, Sang Mo ^a   Lim, Daniel A ^a   Bucci, Monica ^a   Caverzasi, Eduardo ^a   Gaetano, Laura ^a   Mandelli, Maria Luisa ^a   Ryan, Tamara ^b   Perry, Rachel ^b   Farrell, Jody ^b   Jeremy, Rita J ^b   Ulman, Mary ^a   Huhn, Stephen L ^c   Barkovich, A James ^a   Rowitch, David H ^a,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c StemCells Inc   (United States)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATOVAQUONE; BICARBONATE; COTRIMOXAZOLE; IMMUNOSUPPRESSIVE AGENT; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; TACROLIMUS;

ALLOGENEIC STEM CELL TRANSPLANTATION; ARTICLE; BICARBONATE BLOOD LEVEL; BRAIN FUNCTION; CASE REPORT; CONTROLLED STUDY; DIARRHEA; DIFFUSION TENSOR IMAGING; DRUG ERUPTION; DRUG SAFETY; DRUG SUBSTITUTION; DRUG TOLERABILITY; DRUG WITHDRAWAL; FEVER; FRACTIONAL ANISOTROPY; FRONTAL LOBE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOSUPPRESSIVE TREATMENT; MYELINATION; NEURAL STEM CELL TRANSPLANTATION; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; ONSET AGE; OPPORTUNISTIC INFECTION; PELIZAEUS MERZBACHER DISEASE; POSITIVE END EXPIRATORY PRESSURE; PRIORITY JOURNAL; PSEUDOMENINGOCELE; RASH; RHINORRHEA; SAFETY; WHITE MATTER;

ADOLESCENT; ADULT; AGED; BRAIN; FEMALE; HUMANS; MALE; MIDDLE AGED; MUTATION; MYELIN SHEATH; NEURAL STEM CELLS; PELIZAEUS-MERZBACHER DISEASE; STEM CELL TRANSPLANTATION;

EID: 84867472678     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3004373     Document Type: Article

References (35)

1. S. Gencic, D. Abuelo, M. Ambler, L. D. Hudson, Pelizaeus-Merzbacher disease: An X-linked neurologic disorder of myelin metabolism with a novel mutation in the gene encoding proteolipid protein. Am. J. Hum. Genet. 45, 435-442 (1989).
2. R. Schiffmann, M. S. van der Knaap, Invited article: An MRI-based approach to the diagnosis of white matter disorders. Neurology 72, 750-759 (2009).
3. J. Y. Garbern, Pelizaeus-Merzbacher disease: Genetic and cellular pathogenesis. Cell. Mol. Life Sci. 64, 50-65 (2007).
4. A. Schneider, P. Montague, I. Griffiths, M. Fanarraga, P. Kennedy, P. Brophy, K. A. Nave, Uncoupling of hypomyelination and glial cell death by a mutation in the proteolipid protein gene. Nature 358, 758-761 (1992).
5. A. S. Dhaunchak, D. R. Colman, K. A. Nave, Misalignment of PLP/DM20 transmembrane domains determines protein misfolding in Pelizaeus- Merzbacher disease. J. Neurosci. 31, 14961-14971 (2011).
6. W. Lin, B. Popko, Endoplasmic reticulum stress in disorders of myelinating cells. Nat. Neurosci. 12, 379-385 (2009).
7. I. D. Duncan, S. Goldman, W. B. Macklin, M. Rao, L. P. Weiner, S. C. Reingold, Stem cell therapy in multiple sclerosis: Promise and controversy. Mult. Scler. 14, 541 -546 (2008).
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 chimerization with human glial progenitor cells can both remyelinate and rescue the otherwise lethally hypomyelinated shiverer mouse. Cell Stem Cell 2, 553-565 (2008).
9. D. H. Rowitch, Glial specification in the vertebrate neural tube. Nat. Rev. Neurosci. 5, 409-419 (2004).
10. 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).
11. N. Uchida, K. Chen, M. Dohse, K. D. Hansen, J. Dean, J. R. Buser, A. Riddle, D. J. Beardsley, Y. Wan, X. Gong, T. Nguyen, B. J. Cummings, A. J. Anderson, S. J. Tamaki, A. Tsukamoto, I. L. Weissman, S. G. Matsumoto, L. S. Sherman, C. D. Kroenke, S. A. Back, Human neural stem cells induce functional myelination in mice with severe dysmyelination. Sci. Transl. Med. 4, 155ra136 (2012).
12. 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).
13. L. A. Harsan, P. Poulet, B. Guignard, J. Steibel, N. Parizel, P. L. de Sousa, N. Boehm, D. Grucker, M. S. Ghandour, Brain dysmyelination and recovery assessment by noninvasive in vivo diffusion tensor magnetic resonance imaging. J. Neurosci. Res. 83, 392-402 (2006).
14. L. A. Harsan, J. Steibel, A. Zaremba, A. Agin, R. Sapin, P. Poulet, B. Guignard, N. Parizel, D. Grucker, N. Boehm, R. H. Miller, M. S. Ghandour, Recovery from chronic demyelination by thyroid hormone therapy: Myelinogenesis induction and assessment by diffusion tensor magnetic resonance imaging. J. Neurosci. 28, 14189-14201 (2008).
15. 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).
16. M. K. Carpenter, X. Cui, Z. Y. Hu, J. Jackson, S. Sherman, A. Seiger, L. U. Wahlberg, In vitro expansion of a multipotent population of human neural progenitor cells. Exp. Neurol. 158, 265-278 (1999).
17. 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).
18. S. K. Song, J. Yoshino, T. Q. Le, S. J. Lin, S. W. Sun, A. H. Cross, R. C. Armstrong, Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage 26, 132-140 (2005).
19. S. P. Fancy, J. R. Chan, S. E. Baranzini, R. J. Franklin, D. H. Rowitch, Myelin regeneration: A recapitulation of development? Annu. Rev. Neurosci. 34, 21-43 (2011).
20. R. Steiner, N. Selden, S. L. Huhn, T. Koch, A. Al-Urzi, D. Sikora, S. Dean, J. Penfield, T. Sutcliffe, R. Bammer, H. Vogel, N. Uchida, paper presented at the 12th International Congress on Neuronal Ceroid Lipofuscinosis, Hamburg, Germany, 2009.
21. A. M. Trepanier, L. Bennett, J. Y. Garbern, paper presented at the American College of Medical Genetics, Albuquerque, NM, 2010.
22. J. Dubois, G. Dehaene-Lambertz, M. Perrin, J. F. Mangin, Y. Cointepas, E. Duchesnay, D. Le Bihan, L. Hertz-Pannier, Asynchrony of the early maturation of white matter bundles in healthy infants: Quantitative landmarks revealed noninvasively by diffusion tensor imaging. Hum. Brain Mapp. 29, 14-27 (2008).
23. P. McGraw, L. Liang, J. M. Provenzale, Evaluation of normal age-related changes in anisotropy during infancy and childhood as shown by diffusion tensor imaging. AJR Am. J. Roentgenol. 179, 1515-1522 (2002).
24. P. Mukherjee, J. H. Miller, J. S. Shimony, T. E. Conturo, B. C. Lee, C. R. Almli, R. C. McKinstry, Normal brain maturation during childhood: Developmental trends characterized with diffusion-tensor MR imaging. Radiology 221, 349-358 (2001).
25. S. P. Narayanan, A. I. Flores, F. Wang, W. B. Macklin, Akt signals through the mammalian target of rapamycin pathway to regulate CNS myelination. J. Neurosci. 29, 6860-6870 (2009).
26. W. A. Tyler, N. Gangoli, P. Gokina, H. A. Kim, M. Covey, S. W. Levison, T. L. Wood, Activation of the mammalian target of rapamycin (mTOR) is essential for oligodendrocyte differentiation. J. Neurosci. 29, 6367-6378 (2009).
27. P. M. Smith, R. J. Franklin, The effect of immunosuppressive protocols on spontaneous CNS remyelination following toxin-induced demyelination. J. Neuroimmunol. 119, 261-268 (2001).
28. O. Brüstle, K. N. Jones, R. D. Learish, K. Karram, K. Choudhary, O. D. Wiestler, I. D. Duncan, R. D. McKay, Embryonic stem cell-derived glial precursors: A source of myelinating transplants. Science 285, 754-756 (1999).
29. N. D. Bull, K. A. Irvine, R. J. Franklin, K. R. Martin, Transplanted oligodendrocyte precursor cells reduce neurodegeneration in a model of glaucoma. Invest. Ophthalmol. Vis. Sci. 50, 4244-4253 (2009).
30. L. A. Harsan, P. Poulet, B. Guignard, N. Parizel, R. P. Skoff, M. S. Ghandour, Astrocytic hypertrophy in dysmyelination influences the diffusion anisotropy of white matter. J. Neurosci. Res. 85, 935-944 (2007).
31. G. Martino, S. Pluchino, The therapeutic potential of neural stem cells. Nat. Rev. Neurosci. 7, 395-406 (2006).
32. M. Zawadzka, L. E. Rivers, S. P. Fancy, C. Zhao, R. Tripathi, F. Jamen, K. Young, A. Goncharevich, H. Pohl, M. Rizzi, D. H. Rowitch, N. Kessaris, U. Suter, W. D. Richardson, R. J. Franklin, CNS-resident glial progenitor/stem cells produce Schwann cells as well as oligodendrocytes during repair of CNS demyelination. Cell Stem Cell 6, 578-590 (2010).
33. J. I. Berman, S. Chung, P. Mukherjee, C. P. Hess, E. T. Han, R. G. Henry, Probabilistic streamline q-ball tractography using the residual bootstrap. Neuroimage 39, 215-222 (2008).
34. H. Zhang, B. B. Avants, P. A. Yushkevich, J. H. Woo, S. Wang, L. F. McCluskey, L. B. Elman, E. R. Melhem, J. C. Gee, High-dimensional spatial normalization of diffusion tensor images improves the detection of white matter differences: An example study using amyotrophic lateral sclerosis. IEEE Trans. Med. Imaging 26, 1585-1597 (2007).
35. S. C. Deoni, High-resolution T1 mapping of the brain at 3T with driven equilibrium single pulse observation of T1 with high-speed incorporation of RF field inhomogeneities (DESPOT1-HIFI). J. Magn. Reson. Imaging 26, 1106-1111 (2007).