Inhibition of Gli1 mobilizes endogenous neural stem cells for remyelination

Nature

Volumn 526, Issue 7573, 2015, Pages 448-452

  Samanta, Jayshree ^a   Grund, Ethan M ^a   Silva, Hernandez M ^a   Lafaille, Juan J ^a   Fishell, Gord ^a   Salzer, James L ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GLI1; GLI PROTEIN, MOUSE; KRUPPEL LIKE FACTOR; NEUROPROTECTIVE AGENT; SHH PROTEIN, MOUSE;

BRAIN; CELLS AND CELL COMPONENTS; IMMUNE SYSTEM; INHIBITION; NERVOUS SYSTEM DISORDER; NEUROLOGY; PROTEIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DEMYELINATION; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FEMALE; FOREBRAIN; HUMAN; HUMAN CELL; MOUSE; MYELINATION; NEURAL STEM CELL; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; REMYELINIZATION; SUBVENTRICULAR ZONE; WHITE MATTER; ADULT STEM CELL; ANIMAL; ANTAGONISTS AND INHIBITORS; CYTOLOGY; DISEASE MODEL; LATERAL BRAIN VENTRICLE; METABOLISM; MULTIPLE SCLEROSIS; MYELIN SHEATH; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ERINACEIDAE;

ADULT STEM CELLS; ANIMALS; CELL DIFFERENTIATION; DISEASE MODELS, ANIMAL; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; HEDGEHOG PROTEINS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; LATERAL VENTRICLES; MICE; MULTIPLE SCLEROSIS; MYELIN SHEATH; NEURAL STEM CELLS; NEUROPROTECTIVE AGENTS; OLIGODENDROGLIA; PROSENCEPHALON; SIGNAL TRANSDUCTION; WHITE MATTER; ZINC FINGER PROTEIN GLI1;

EID: 84944318133     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature14957     Document Type: Article

References (32)

1. Franklin, R. J. M. & Goldman, S. A. Glia disease and repair - remyelination. Cold Spring Harb. Perspect. Biol. http://dx.doi.org/10.1101/cshperspect.a020594 (2015).
2. Xing, Y. L. et al. Adult neural precursor cells from the subventricular zone contribute significantly to oligodendrocyte regeneration and remyelination. J. Neurosci. 34, 14128-14146 (2014).
3. Scolding, N. et al. Oligodendrocyte progenitors are present in the normal adult human CNS and in the lesions of multiple sclerosis. Brain 121, 2221-2228 (1998).
4. Gensert, J.M.&Goldman, J. E. Endogenous progenitors remyelinate demyelinated axons in the adult CNS. Neuron 19, 197-203 (1997).
5. Zawadzka, M. et al. 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).
6. Menn, B. et al. Origin of oligodendrocytes in the subventricular zone of the adult brain. J. Neurosci. 26, 7907-7918 (2006).
7. Nait-Oumesmar, B. et al. Activation of the subventricular zone inmultiple sclerosis: evidence for early glial progenitors. Proc. Natl Acad. Sci. USA 104, 4694-4699 (2007).
8. Fuccillo, M., Joyner, A. L. & Fishell, G. Morphogen to mitogen: the multiple roles of hedgehog signalling in vertebrate neural development. Nature Rev. Neurosci. 7, 772-783 (2006).
9. Petrova, R.&Joyner, A. L. Roles forHedgehog signaling in adult organ homeostasis and repair. Development 141, 3445-3457 (2014).
10. Ferent, J., Zimmer, C., Durbec, P., Ruat, M. & Traiffort, E. Sonic Hedgehog signaling is a positive oligodendrocyte regulator during demyelination. J. Neurosci. 33, 1759-1772 (2013).
11. Ingham, P. W. & McMahon, A. P. Hedgehog signaling in animal development: paradigms and principles. Genes Dev. 15, 3059-3087 (2001).
12. Ahn, S. & Joyner, A. L. Dynamic changes in the response of cells to positive hedgehog signaling during mouse limb patterning. Cell 118, 505-516 (2004).
13. Dessaud, E.,McMahon, A.P.&Briscoe, J. Pattern formation inthe vertebrate neural tube: a sonic hedgehog morphogen-regulated transcriptional network. Development 135, 2489-2503 (2008).
14. Ahn, S. & Joyner, A. L. In vivo analysis of quiescent adult neural stem cells responding to Sonic hedgehog. Nature 437, 894-897 (2005).
15. Sousa, V. H., Miyoshi, G., Hjerling-Leffler, J., Karayannis, T. & Fishell, G. Characterization of Nkx6-2-derived neocortical interneuron lineages. Cereb. Cortex 19 (Suppl. 1), i1-i10 (2009).
16. Matsushima, G. K. & Morell, P. The neurotoxicant, cuprizone, as a model to study demyelination and remyelination in the central nervous system. Brain Pathol. 11, 107-116 (2001).
17. Garcia, A. D., Petrova, R., Eng, L. & Joyner, A. L. Sonic hedgehog regulates discrete populations of astrocytes in the adult mouse forebrain. J. Neurosci. 30, 13597-13608 (2010).
18. Balordi, F. & Fishell, G. Mosaic removal of hedgehog signaling in the adult SVZ reveals that the residual wild-type stem cells have a limited capacity for selfrenewal. J. Neurosci. 27, 14248-14259 (2007).
19. Bai, C. B., Auerbach, W., Lee, J. S., Stephen, D. & Joyner, A. L. Gli2, but not Gli1, is required for initial Shh signaling and ectopic activation of the Shh pathway. Development 129, 4753-4761 (2002).
20. Bambakidis, N. C. & Onwuzulike, K. Sonic Hedgehog signaling and potential therapeutic indications. Vitam. Horm. 88, 379-394 (2012).
21. Xie, J. et al. Activating Smoothened mutations in sporadic basal-cell carcinoma. Nature 391, 90-92 (1998).
22. Rowitch, D. H. Sonic hedgehog regulates proliferation and inhibits differentiation of CNS precursor cells. J. Neurosci. 19, 8954-8965 (1999).
23. Lauth, M., Bergstrom, A., Shimokawa, T. & Toftgard, R. Inhibition of GLI-mediated transcription and tumor cell growth by small-molecule antagonists. Proc. Natl Acad. Sci. USA 104, 8455-8460 (2007).
24. Zhu, X. et al. Age-dependent fate and lineage restriction of single NG2 cells. Development 138, 745-753 (2011).
25. Tuohy, V. K., Sobel, R. A. & Lees, M. B. Myelin proteolipid protein-induced experimental allergic encephalomyelitis. Variations of disease expression in different strains of mice. J. Immunol. 140, 1868-1873 (1988).
26. Wujek, J. R. et al. Axon loss in the spinal cord determines permanent neurological disability in an animalmodel of multiple sclerosis. J. Neuropathol. Exp. Neurol. 61, 23-32 (2002).
27. Recks, M. S. et al. Early axonal damage and progressive myelin pathology define the kinetics of CNS histopathology in a mouse model of multiple sclerosis. Clin. Immunol. 149, 32-45 (2013).
28. Powers, B. E. et al. Remyelination reporter reveals prolonged refinement of spontaneously regenerated myelin. Proc. Natl Acad. Sci. USA 110, 4075-4080 (2013).
29. Aharoni, R. et al. Distinct pathological patterns in relapsing-remitting and chronic models of experimental autoimmune enchephalomyelitis and the neuroprotective effect of glatiramer acetate. J. Autoimmun. 37, 228-241 (2011).
30. Barnabe-Heider, F. et al. Origin of new glial cells in intact and injured adult spinal cord. Cell Stem Cell 7, 470-482 (2010).
31. Elsworth, S. & Howell, J. M. Variation in the response of mice to cuprizone. Res. Vet. Sci. 14, 385-387 (1973).
32. Glausier, J. R.,Khan, Z. U.&Muly, E. C.DopamineD1andD5receptors are localized to discrete populations of interneurons in primate prefrontal cortex. Cereb. Cortex 19, 1820-1834 (2009).