Neural stem/progenitor cell properties of glial cells in the adult mouse auditory nerve

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Lang, Hainan ^a   Xing, Yazhi ^a   Brown, Lashardai N ^a   Samuvel, Devadoss J ^a   Panganiban, Clarisse H ^a   Havens, Luke T ^a   Balasubramanian, Sundaravadivel ^a   Wegner, Michael ^b   Krug, Edward L ^a   Barth, Jeremy L ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT STEM CELL; ANIMAL; CELL CULTURE; CENTRAL HEARING LOSS; COCHLEAR NERVE; GLIA; INJURIES; MOUSE; NERVE REGENERATION; NEURAL STEM CELL; PATHOLOGY; STEM CELL; TRANSGENIC MOUSE;

ADULT STEM CELLS; ANIMALS; CELLS, CULTURED; COCHLEAR NERVE; HEARING LOSS, CENTRAL; MICE; MICE, TRANSGENIC; NERVE REGENERATION; NEURAL STEM CELLS; NEUROGLIA; STEM CELLS;

EID: 84940041969     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep13383     Document Type: Article

References (73)

1. Schuknecht, H. F., Gacek, M. R. Cochlear pathology in presbycusis. Ann Otol Rhinol Laryngol 102, 1-16 (1993).
2. Kusunoki, T. et al. Age-related histopathologic changes in the human cochlea: a temporal bone study. Otolaryngol Head Neck Surg 131, 897-903 (2004).
3. Kujawa, S. G., Liberman, M. C. Adding insult to injury: cochlear nerve degeneration after "temporary" noise-induced hearing loss. J Neurosci 29, 14077-14085 (2009).
4. Groves, A. K. et al. Repair of demyelinated lesions by transplantation of purified O-2A progenitor cells. Nature 362, 453-455 (1993).
5. Santilli, G. et al. Mild hypoxia enhances proliferation and multipotency of human neural stem cells. PLoS One 5, e8575 (2010).
6. Geleoc, G. S., Holt, J. R. Sound strategies for hearing restoration. Science 344, 1241062 (2014).
7. Hu, Z., Andang, M., Ni, D., Ulfendahl, M. Neural cograft stimulates the survival and differentiation of embryonic stem cells in the adult mammalian auditory system. Brain Res 1051, 137-144 (2005).
8. Karimi-Abdolrezaee, S., Eftekharpour, E., Wang, J., Morshead, C. M., Fehlings, M. G. Delayed transplantation of adult neural precursor cells promotes remyelination and functional neurological recovery after spinal cord injury. J Neurosci 26, 3377-3389 (2006).
9. Garzon-Muvdi, T., Quinones-Hinojosa, A. Neural stem cell niches and homing: recruitment and integration into functional tissues. Ilar J 51, 3-23 (2009).
10. Lindvall, O., Kokaia, Z. Prospects of stem cell therapy for replacing dopamine neurons in Parkinson's disease. Trends Pharmacol Sci 30, 260-267 (2009).
11. Oshima, K., Senn, P., Heller, S. Isolation of sphere-forming stem cells from the mouse inner ear. Methods Mol Biol 493, 141-162 (2009).
12. Diensthuber, M. et al. Spiral ganglion stem cells can be propagated and differentiated into neurons and glia. Biores Open Access 3, 88-97 (2014).
13. Gage, F. H., Ray, J., Fisher, L. J. Isolation, characterization, and use of stem cells from the CNS. Annu Rev Neurosci 18, 159-192 (1995).
14. Bellenchi, G. C., Volpicelli, F., Piscopo, V., Perrone-Capano, C., di Porzio, U. Adult neural stem cells: an endogenous tool to repair brain injury? J Neurochem 124, 159-167 (2013).
15. Goldman, S. Glia as neural progenitor cells. Trends Neurosci 26, 590-596 (2003).
16. Beckervordersandforth, R. et al. In vivo fate mapping and expression analysis reveals molecular hallmarks of prospectively isolated adult neural stem cells. Cell Stem Cell 7, 744-758 (2010).
17. Sofroniew, M. V. Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci 32, 638-647 (2009).
18. Robel, S., Berninger, B., Gotz, M. The stem cell potential of glia: lessons from reactive gliosis. Nat Rev Neurosci 12, 88-104 (2011).
19. Silver, D. J., Steindler, D. A. Common astrocytic programs during brain development, injury and cancer. Trends Neurosci 32, 303-311 (2009).
20. Nash, B., Ioannidou, K., Barnett, S. C. Astrocyte phenotypes and their relationship to myelination. J Anat 219, 44-52 (2011).
21. Kléber, M. et al. Neural crest stem cell maintenance by combinatorial Wnt and BMP signaling. J Cell Biol 169, 309-20 (2005).
22. Lang, H. et al. Sox2 up-regulation and glial cell proliferation following degeneration of spiral ganglion neurons in the adult mouse inner ear. J Assoc Res Otolaryngol 12, 151-171 (2011).
23. Schmiedt, R. A., Okamura, H. O., Lang, H., Schulte, B. A. Ouabain application to the round window of the gerbil cochlea: a model of auditory neuropathy and apoptosis. J Assoc Res Otolaryngol 3, 223-233 (2002).
24. Wegner, M., Stolt, C. C. From stem cells to neurons and glia: a Soxist's view of neural development. Trends Neurosci 28, 583-588 (2005).
25. Breuskin, I. et al. Glial but not neuronal development in the cochleo-vestibular ganglion requires Sox10. J Neurochem 114, 1827-1839 (2010).
26. Onder, T. T. et al. Chromatin-modifying enzymes as modulators of reprogramming. Nature 483, 598-602 (2012).
27. Lu, C. C., Appler, J. M., Houseman, E. A., Goodrich, L. V. Developmental profiling of spiral ganglion neurons reveals insights into auditory circuit assembly. J Neurosci 31, 10903-10918 (2011).
28. Garcia, A. D., Doan, N. B., Imura, T., Bush, T. G., Sofroniew, M. V. GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat Neurosci 7, 1233-1241 (2004).
29. Jessen, K. R., Mirsky, R. The origin and development of glial cells in peripheral nerves. Nat Rev Neurosci 6, 671-682 (2005).
30. Young, K. M., Merson, T. D., Sotthibundhu, A., Coulson, E. J., Bartlett, P. F. p75 neurotrophin receptor expression defines a population of BDNF-responsive neurogenic precursor cells. J Neurosci 27, 5146-5155 (2007).
31. Weishaupt, N., Blesch, A., Fouad, K. BDNF: the career of a multifaceted neurotrophin in spinal cord injury. Exp Neurol 238, 254-264 (2012).
32. Paratore, C., Goerich, D. E., Suter, U., Wegner, M., Sommer, L. Survival and glial fate acquisition of neural crest cells are regulated by an interplay between the transcription factor Sox10 and extrinsic combinatorial signaling. Development 128, 3949-3961 (2001).
33. Hunt, D. P. et al. A highly enriched niche of precursor cells with neuronal and glial potential within the hair follicle dermal papilla of adult skin. Stem Cells 26, 163-172 (2008).
34. Menendez, L., Yatskievych, T. A., Antin, P. B., Dalton, S. Wnt signaling and a Smad pathway blockade direct the differentiation of human pluripotent stem cells to multipotent neural crest cells. Proc Natl Acad Sci USA 108, 19240-19245 (2011).
35. Nitzan, E., Pfaltzgraff, E. R., Labosky, P. A., Kalcheim, C. Neural crest and Schwann cell progenitor-derived melanocytes are two spatially segregated populations similarly regulated by Foxd3. Proc Natl Acad Sci USA 110, 12709-12714 (2013).
36. Teng, L., Mundell, N. A., Frist, A. Y., Wang, Q., Labosky, P. A. Requirement for Foxd3 in the maintenance of neural crest progenitors. Development 135, 1615-1624 (2008).
37. Imura, T., Kornblum, H. I., Sofroniew, M. V. The predominant neural stem cell isolated from postnatal and adult forebrain but not early embryonic forebrain expresses GFAP. J Neurosci 23, 2824-2832 (2003).
38. Gilyarov, A. V. Nestin in central nervous system cells. Neurosci Behav Physiol 38, 165-169 (2008).
39. Diensthuber, M., Oshima, K., Heller, S. Stem/progenitor cells derived from the cochlear sensory epithelium give rise to spheres with distinct morphologies and features. J Assoc Res Otolaryngol 10, 173-190 (2009).
40. Rask-Andersen, H. et al. Regeneration of human auditory nerve. In vitro/in video demonstration of neural progenitor cells in adult human and guinea pig spiral ganglion. Hear Res 203, 180-191 (2005).
41. Deleyrolle, L. P., Reynolds, B. A. Isolation, expansion, and differentiation of adult Mammalian neural stem and progenitor cells using the neurosphere assay. Methods Mol Biol 549, 91-101 (2009).
42. Graham, V., Khudyakov, J., Ellis, P., Pevny, L. SOX2 functions to maintain neural progenitor identity. Neuron 39, 749-765 (2003).
43. Ramalho-Santos, M., Yoon, S., Matsuzaki, Y., Mulligan, R. C., Melton, D. A. "Stemness": transcriptional profiling of embryonic and adult stem cells. Science 298, 597-600 (2002).
44. Whitlon, D. S., Tieu, D., Grover, M. Purification and transfection of cochlear Schwann cells. Neuroscience 171, 23-30 (2010).
45. D'Amour, K. A., Gage, F. H. Genetic and functional differences between multipotent neural and pluripotent embryonic stem cells. Proc Natl Acad Sci USA 100 Suppl 1, 11866-11872 (2003).
46. Szablowska-Gadomska, I., Zayat, V., Buzanska, L. Influence of low oxygen tensions on expression of pluripotency genes in stem cells. Acta Neurobiol Exp (Wars) 71, 86-93 (2011).
47. Hockfield, S., McKay, R. D. Identification of major cell classes in the developing mammalian nervous system. J Neurosci 5, 3310-3328 (1985).
48. Boda, E., Buffo, A. Glial cells in non-germinal territories: insights into their stem/progenitor properties in the intact and injured nervous tissue. Arch Ital Biol 148, 119-136 (2010).
49. Buffo, A. et al. Origin and progeny of reactive gliosis: A source of multipotent cells in the injured brain. Proc Natl Acad Sci USA 105, 3581-3586 (2008).
50. Hanna, L. A., Foreman, R. K., Tarasenko, I. A., Kessler, D. S., Labosky, P. A. Requirement for Foxd3 in maintaining pluripotent cells of the early mouse embryo. Genes Dev 16, 2650-2661 (2002).
51. Doetsch, F., Caille, I., Lim, D. A., Garcia-Verdugo, J. M., Alvarez-Buylla, A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97, 703-716 (1999).
52. Laywell, E. D., Rakic, P., Kukekov, V. G., Holland, E. C., Steindler, D. A. Identification of a multipotent astrocytic stem cell in the immature and adult mouse brain. Proc Natl Acad Sci USA 97, 13883-13888 (2000).
53. Steindler, D. A., Laywell, E. D. Astrocytes as stem cells: nomenclature, phenotype, and translation. Glia 43, 62-69 (2003).
54. Widera, D. et al. Schwann cells can be reprogrammed to multipotency by culture. Stem Cells Dev 20, 2053-2064 (2011).
55. Ferri, A. L. et al. Sox2 deficiency causes neurodegeneration and impaired neurogenesis in the adult mouse brain. Development 131, 3805-3819 (2004).
56. Pevny, L. H., Nicolis, S. K. Sox2 roles in neural stem cells. Int J Biochem Cell Biol 42, 421-424 (2010).
57. Engelen, E. et al. Sox2 cooperates with Chd7 to regulate genes that are mutated in human syndromes. Nat Genet 43, 607-611 (2011).
58. Juliandi, B., Abematsu, M., Nakashima, K. Chromatin remodeling in neural stem cell differentiation. Curr Opin Neurobiol 20 (2010).
59. MacDonald, J. L., Roskams, A. J. Histone deacetylases 1 and 2 are expressed at distinct stages of neuro-glial development. Dev Dyn 237, 2256-2267 (2008).
60. Jacob, C. et al. HDAC1 and HDAC2 control the transcriptional program of myelination and the survival of Schwann cells. Nat Neurosci 14, 429-436 (2011).
61. Sirko, S. et al. Reactive glia in the injured brain acquire stem cell properties in response to sonic hedgehog. [corrected]. Cell Stem Cell 12, 426-439 (2013).
62. Simon, M. C., Keith, B. The role of oxygen availability in embryonic development and stem cell function. Nat Rev Mol Cell Biol 9, 285-296 (2008).
63. Panchision, D. M. The role of oxygen in regulating neural stem cells in development and disease. J Cell Physiol 220, 562-568 (2009).
64. Felling, R. J. et al. Neural stem/progenitor cells participate in the regenerative response to perinatal hypoxia/ischemia. J Neurosci 26, 4359-4369 (2006).
65. Mathieu, J. et al. Hypoxia induces re-entry of committed cells into pluripotency. Stem Cells 31, 1737-1748 (2013).
66. Forshammar, J., Block, L., Lundborg, C., Biber, B., Hansson, E. Naloxone and ouabain in ultralow concentrations restore Na?ATPase and cytoskeleton in lipopolysaccharide-treated astrocytes. J Biol Chem 286, 31586-97 (2011).
67. Forshammar, J. et al. Anti-inflammatory substances can influence some glial cell types but not others. Brain Res 1539, 34-40 (2013).
68. Niu, W. et al. In vivo reprogramming of astrocytes to neuroblasts in the adult brain. Nat Cell Biol 15, 1164-1175 (2013).
69. Allen, D. L. et al. Effects of spaceflight on murine skeletal muscle gene expression. J Appl Physiol (1985) 106, 582-595 (2009).
70. Irizarry, R. A. et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4, 249-264 (2003).
71. Li, C., Wong, W. H. Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc Natl Acad Sci USA 98, 31-6 (2001).
72. Ho Sui, S. J., Fulton, D. L., Arenillas, D. J., Kwon, A. T., Wasserman, W. W. oPOSSUM: integrated tools for analysis of regulatory motif over-representation. Nucleic Acids Res 35 (Web Server issue), W245-52 (2007).
73. Ho-Sui, S. J. et al. oPOSSUM: Identification of over-represented transcription factor binding sites in co-expressed genes. Nucleic Acids Res 33, 3154-64 (2005).