Cochlear stem/progenitor cells from a postnatal cochlea respond to Jagged1 and demonstrate that notch signaling promotes sphere formation and sensory potential

Mechanisms of Development

Volumn 125, Issue 8, 2008, Pages 674-686

  Savary, Etienne ^a,b   Sabourin, Jean Charles ^a   Santo, Julien ^a   Hugnot, Jean Philippe ^a   Chabbert, Christian ^a   Van De Water, Thomas ^c   Uziel, Alain ^a,b,d   Zine, Azel ^a,b  

^a INSERM   (France)

^b UNIV MONTPELLIER   (France)

^c UNIVERSITY OF MIAMI EAR INSTITUTE   (United States)

^d GUI DE CHAULIAC HOSPITAL   (France)

Author keywords

Hair cell regeneration; Hearing loss; Jagged1; Notch signaling; Stem progenitor cells spheres

Indexed keywords

GAMMA SECRETASE INHIBITOR; JAGGED1; MYOSIN VI; MYOSIN VIIA; NOTCH RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL LINEAGE; CELL MATURATION; CELL PROLIFERATION; COCHLEA; CONTROLLED STUDY; HAIR CELL; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; IN VITRO STUDY; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STEM CELL;

ANIMALS; CALCIUM-BINDING PROTEINS; CELL DIFFERENTIATION; CELLS, CULTURED; COCHLEA; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MICE; RECEPTORS, NOTCH; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; STEM CELLS;

MAMMALIA;

EID: 47549084224     PISSN: 09254773     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mod.2008.05.001     Document Type: Article

References (51)

1. Alison M.R. Tissue-based stem cells: ABC transporter proteins take centre stage. J. Pathol. 200 (2003) 547-550
2. Bhattacharya S., Das A., Mallya K., and Ahmad I. Maintenance of retinal stem cells by Abcg2 is regulated by Notch signaling. J. Cell Sci. 120 (2007) 2652-2662
3. Bermingham N.A., Hassan B.A., Price S.D., Vollrath M.A., Ben Arie N., Eatock R.A., Bellen H.J., Lysakowski A., and Zoghbi H.Y. Math1: an essential gene for the generation of inner ear hair cells. Science 284 (1999) 1837-1841
4. Bunting K.D. ABC transporters as phenotypic markers and functional regulators of stem cells. Stem Cells 20 (2002) 11-20
5. Chardin S., and Romand R. Regeneration and mammalian auditory hair cells. Science 267 (1995) 707-709
6. Kip1 links cell proliferation to morphogenesis in the developing organ of Corti. Development 126 (1999) 1581-1590
7. Chen P., Johnson J., Zoghbi H., and Segil N. The role of Math1 in inner ear development: uncoupling the establishment of the sensory primordium from hair cell fate determination. Development 129 (2002) 2495-2505
8. Corwin J.T., and Oberholtzer J.C. Fish n'chicks: model recipes for hair cell regeneration?. Neuron 19 (1997) 951-954
9. Corwin J.T., and Cotanche D.A. Regeneration of sensory hair cells after acoustic trauma. Science 240 (1988) 1772-1774
10. Doetzlhofer A., White P., Johnson J., Segil N., and Groves A. In vitro growth and differentiation of mammalian sensory hair cell progenitors: a requirement for EGF and periotic mesenchyme. Dev. Biol. 272 (2004) 432-447
11. Eddison M., Le Roux I., and Lewis J. Notch signaling in the development of the inner ear: lessons from Drosophila. Proc. Natl. Acad. Sci. USA 97 (2000) 11692-11699
12. Fre S., Huyghe M., Mourikis P., Robine S., Louvard D., and Artavanis-Tsakonas S. Notch signals control the fate of immature progenitor cells in the intestine. Nature 435 (2005) 964-968
13. Gage F.H. Mammalian neural stem cells. Science 287 (2000) 1433-1438
14. Gale J.E., Marcotti W., Kennedy H.J., Kros C.J., and Richardson G.P. FM1-43 dye behaves as a permeant blocker of the hair-cell mechanotransducer channel. J. Neurosci. 21 (2001) 7013-7025
15. Hume C.R., Bratt D.L., and Oesterle E.C. Expression of LHX3 and SOX2 during mouse inner ear development. Gene Expr. Patterns 7 (2007) 798-807
16. Izumikawa M., Minoda R., Kawamoto K., Abrashkin K.A., Swiderski D.L., Dolan D.F., Brough D.E., and Raphael Y. Auditory hair cell replacement and hearing improvement by Atoh1 gene therapy in deaf mammals. Nat. Med. 11 (2005) 271-276
17. Kadesch T. Notch signaling: a dance of proteins changing partners. Exp. Cell Res. 260 (2000) 1-8
18. Kelley M.W. Regulation of cell fate in the sensory epithelia of the inner ear. Nat. Rev. Neurosci. 11 (2006) 837-849
19. Kiernan A.E., Xu J., and Gridley T. The Notch ligand JAG1 is required for sensory progenitor development in the mammalian inner ear. PLoS Genetics 2 1 (2006) e4
20. Kuntz A.L., and Oesterle E.C. Transforming growth factor alpha with insulin stimulates cell proliferation in vivo in adult rat vestibular sensory epithelium. J. Comp. Neurol. 399 (1998) 413-423
21. Lanford P.J., Lan Y., Jiang R.L., Lindsell C., Weinmaster G., Gridley T., and Kelley M.W. Notch signaling pathway mediates hair cell development in mammalian cochlea. Nat. Genet. 21 (1999) 289-292
22. Li H., Liu H.S., and Heller S. Pluripotent stem cells from the adult mouse inner ear. Nat. Med. 9 (2003) 1293-1299
23. Li L., Milner L.A., Deng Y., Iwata M., Banta A., Graf L., Marcovina S., Friedman C., Trask B.J., Hood L., and Torok-Storb B. The Human Homolog of rat Jagged1 expressed by marrow stroma inhibits differentiation of 32D cells through interaction with Notch1. Immunity 8 (1998) 43-55
24. Lim D., and Anniko M. Developmental morphology of the mouse inner ear. A scanning electron microscopic observation. Acta. Otolaryngol. 422 (1985) 1-69
25. Litman T., Brangi M., Hudson E., Fetsch P., Abati A., Ross D.D., Miyake K., Resau J.H., and Bates S.E. The multidrug-resistant phenotype associated with overexpression of the new ABC half-transporter, MXR (ABCG2). J. Cell. Sci. 113 (2000) 2011-2021
26. Mizutani T., Taniguchi Y., Aoki T., Hashimoto N., and Honjo T. Conservation of the biochemical mechanisms of signal transduction among mammalian Notch family members. Proc. Natl. Acad. Sci. USA 98 (2001) 9026-9031
27. Morrison A., Hodgetts C., Gossler A., Hrabe de Angelis M., and Lewis J. Expression of Delta1 and Serrate1 (Jagged1) in the mouse inner ear. Mech. Dev. 84 (1999) 169-172
28. Nyfeler Y., Kirch R., Mantei N., Leone D.P., Radtke F., Suter U., and Taylor V. Jagged1 signals in the postnatal subventricular zone are required for neural stem cell self-renewal. EMBO J. 24 (2005) 3504-3515
29. Ohtsuka T., Ishibashi M., Gradwohl G., Nakanishi S., Guillemot F., and Kageyama R. Hes1 and Hes5 as Notch effectors in mammalian neuronal differentiation. EMBO J. 18 (1999) 2196-2207
30. Oshima K., Grimm C.M., Corrales C.E., Senn P., Martinez Monedero R., Geleoc G.S., Edge A., Holt J.R., and Heller S. Differential distribution of stem cells in the auditory and vestibular organs of the inner ear. J. Assoc. Res. Otolaryngol. 8 (2006) 18-31
31. Reynolds B.A., and Weiss S. Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev. Biol. 175 (1996) 1-13
32. Ruben R.J. Development of the inner ear of the mouse: a radioautographic study of terminal mitoses. Acta Oto-Laryngol. 220 (1967) 1-44
33. Rocchi E., Khodjakov A., Volk E.L., Yang C.H., Litman T., Bates S.E., and Schneider E. The product of the ABC half-transporter gene ABCG2 (BCRP/MXR/ABCP) is expressed in the plasma membrane. Biochem. Biophys. Res. Commun. 271 (2000) 42-46
34. Ryals B.M., and Rubel E.W. Hair cell regeneration after acoustic trauma in adult Coturnix quail. Science 240 (1988) 1774-1776
35. Tokunaga A., Kohyama J., Yoshida T., Nakao K., Sawamoto K., and Okano H. Mapping spatio-temporal activation of Notch signaling during neurogenesis and gliogenesis in the developing mouse brain. J. Neurochem. 90 (2004) 142-154
36. Savary E., Hugnot J.P., Chassigneux Y., Travo C., Duperray C., Van De Water T., and Zine A. Distinct population of hair cell progenitors can be isolated from the postnatal mouse cochlea using side population analysis. Stem Cells 25 (2007) 332-339
37. Shimazaki T., Shingo T., and Weiss S. The ciliary neurotrophic factor/leukemia inhibitory factor/gp130 receptor complex operates in the maintenance of mammalian forebrain neural stem cells. J. Neurosci. 21 (2001) 7642-7653
38. Shou J., Zheng J.L., and Gao W.Q. Robust generation of new hair cells in the mature mammalian inner ear by adenoviral expression of Hath1. Mol. Cell. Neurosci. 23 (2003) 169-179
39. Stone J.S., Oesterle E.C., and Rubel E.W. Recent insights into regeneration of auditory and vestibular hair cells. Curr. Opin. Neurol. 11 (1998) 17-24
40. Wegner M., and Stolt CC. From stem cells to neurons and glia: a Soxist's view of neural development. Trends Neurosci. 28 (2005) 583-588
41. White P.M., Doetzlhofer A., Lee Y.S., Groves A.K., and Segil N. Mammalian cochlear supporting cells can divide and trans-differentiate into hair cells. Nature 441 (2006) 984-987
42. Woods C., Montcouquiol M., and Kelley M.W. Math1 regulates development of the sensory epithelium in the mammalian cochlea. Nat. Neurosci. 7 (2004) 1310-1318
43. Yamashita H., and Oesterle E.C. Induction of cell proliferation in mammalian inner-ear sensory epithelia by transforming growth factor alpha and epidermal growth factor. Proc. Natl. Acad. Sci. USA 92 (1995) 3152-3155
44. Zhai S., Shi L., Wang B.E., Zheng G., Song W., Hu Y., and Gao W.Q. Isolation and culture of hair cell progenitors from postnatal rat cochleae. J. Neurobiol. 65 (2005) 282-293
45. Zheng J.L., and Gao W.Q. Overexpression of Math1 induces robust production of extra hair cells in postnatal rat inner ears. Nat. Neurosci. 3 (2000) 580-586
46. Zhou S., Schuetz J.D., Bunting K.D., Colapietro A.M., Sampath J., Morris J.J., Lagutina I., Grosveld G.C., Osawa M., Nakauchi H., and Sorrentino B.P. The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nat. Med. 9 (2001) 1028-1034
47. Zine A., Hafidi A., and Romand R. Fimbrin in the developing rat cochlea. Hear. Res. 87 (1995) 165-169
48. Zine A., and Romand R. Development of the auditory receptors of the rat: a SEM study. Brain Res. 721 (1996) 49-58
49. Zine A., and de Ribaupierre F. Replacement of mammalian auditory hair cells. NeuroReport 9 (1988) 263-268
50. Zine A., Van De Water T.R., and de Ribaupierre F. Notch signaling regulates the pattern of auditory hair cell differentiation in mammals. Development 127 (2000) 3373-3383
51. Zine A., Aubert A., Qiu J., Therianos S., Guillemot F., Kageyama R., and de Ribaupierre F. Hes1 and Hes5 activities are required for the normal development of the hair cells in the mammalian inner ear. J. Neurosci. 21 (2001) 4712-4720