Isolation and Characterization of Mammalian Otic Progenitor Cells that Can Differentiate into Both Sensory Epithelial and Neuronal Cell Lineages.
Animals
Basic Helix-Loop-Helix Transcription Factors
/ metabolism
Cell Differentiation
/ physiology
Cell Lineage
/ physiology
Ear, Inner
/ cytology
Hair Cells, Auditory
/ cytology
Myosin VIIa
/ metabolism
Nanog Homeobox Protein
/ metabolism
Nestin
/ metabolism
Neurons
/ cytology
Rats
Rats, Wistar
Stem Cells
/ cytology
ganglion cell
inner ear
multipotent progenitor
otocyst
sensory epithelia
Journal
Anatomical record (Hoboken, N.J. : 2007)
ISSN: 1932-8494
Titre abrégé: Anat Rec (Hoboken)
Pays: United States
ID NLM: 101292775
Informations de publication
Date de publication:
03 2020
03 2020
Historique:
received:
03
05
2018
revised:
25
11
2019
accepted:
03
12
2019
pubmed:
17
1
2020
medline:
28
1
2021
entrez:
17
1
2020
Statut:
ppublish
Résumé
The mammalian inner ear mediates hearing and balance and during development generates both cochleo-vestibular ganglion neurons and sensory epithelial receptor cells, that is, hair cells and support cells. Cell marking experiments have shown that both hair cells and support cells can originate from a common progenitor. Here, we demonstrate the lineage potential of individual otic epithelial cell clones using three cell lines established by a combination of limiting dilution and gene-marking techniques from an embryonic day 12 (E12) rat otocyst. Cell-type specific marker analyses of these clonal lines under proliferation and differentiation culture conditions demonstrate that during differentiation immature cell markers (Nanog and Nestin) were downregulated and hair cell (Myosin VIIa and Math1), support cell (p27
Substances chimiques
Basic Helix-Loop-Helix Transcription Factors
0
Myosin VIIa
0
Nanog Homeobox Protein
0
Nestin
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
451-460Informations de copyright
© 2020 American Association for Anatomy.
Références
Barald KF, Lindberg KH, Hardiman K, Kavka AI, Lewis JE, Victor JC, Gardner CA, Poniatowski A. 1997. Immortalized cell lines from embryonic avian and murine otocysts: tools for molecular studies of the developing inner ear. Int J Dev Neurosci 15(4-5):523-540.
Bermingham NA, Hassan BA, Price SD, Vollrath MA, Ben-Arie N, Eatock RA, Bellen HJ, Lysakowski A, Zoghbi HY. 1999. Math1: an essential gene for the generation of inner ear hair cells. Science 284(5421):1837-1841.
Bryant J, Goodyear RJ, Richardson GP. 2002. Sensory organ development in the inner ear: molecular and cellular mechanisms. Br Med Bull 63:39-57.
Cepko C. 1988. Retrovirus vectors and their applications in neurobioloby. Neuron 1:345-353.
Chambers I, Colby D, Robertson M, Nichols J, Lee S, Tweedie S, Smith A. 2003. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 113(5):643-655.
Chen P, Johnson JE, Zoghbi HY, Segil N. 2002. The role of Math1 in inner eardevelopment: Uncoupling the establishment of the sensory primordium from haircell fate determination. Development 129:2495-2505
Chen P, Segil N. 1999. p27(Kip1) links cell proliferation to morphogenesis in the developing organ of Corti. Development 126(8):1581-1590.
Fekete D, Wu D. 2002. Revisiting cell fate specification in the inner ear. Curr Opin Neurobiol 12:35-42.
Fekete DM, Muthukumar S, Karagogeos D. 1998. Hair cells and supporting cells share a common progenitor in the avian inner ear. J Neurosci 18(19):7811-7821.
Freshney RI. 2000. Culture of animal cells. New York: A John Wiley and Sons, Inc.
Fritzsch B, Beisel KW, Bermingham NA. 2000. Developmental evolutionary biology of the vertebrate ear: conserving mechanoelectric transduction and developmental pathways in diverging morphologies. Neuroreport 11(17):R35-R44.
Gage FH. 2000. Mammalian neural stem cells. Science 287(5457):1433-1438.
Haddon C, Jiang YJ, Smithers L, Lewis J. 1998. Delta-Notch signalling and the patterning of sensory cell differentiation in the zebrafish ear: evidence from the mind bomb mutant. Development 125(23):4637-4644.
Hartenstein V, Posakony JW. 1989. Development of adult sensilla on the wing and notum of Drosophila melanogaster. Development 107(2):389-405.
Hasson T, Heintzelman MB, Santos-Sacchi J, Corey DP, Mooseker MS. 1995. Expression in cochlea and retina of myosin VIIa, the gene product defective in Usher syndrome type 1B. Proc Natl Acad Sci U S A 92(21):9815-9819.
Herbrand H, Guthrie S, Hadrys T, Hoffmann S, Arnold HH, Rinkwitz-Brandt S, Bober E. 1998. Two regulatory genes, cNkx5-1 and cPax2, show different responses to local signals during otic placode and vesicle formation in the chick embryo. Development 125(4):645-654.
Hidalgo Sanchez M, Alvarado Mallart R, Alvarez IS. 2000. Pax2, Otx2, Gbx2 and Fgf8 expression in early otic vesicle development. Mech Dev 95(1-2):225-229.
Holley MC, Nishida Y, Grix N. 1997. Conditional immortalization of hair cells from the inner ear. Int J Dev Neurosci 15(4-5):541-552.
Hume CR, Kirkegaard M, Oesterle EC. 2003. ErbB expression: the mouse inner ear and maturation of the mitogenic response to heregulin. J Assoc Res Otolaryngol Sep 4(3):422-443.
Kalinec F, Kalinec G, Boukhvalova M, Kachar B. 1999. Establishment and characterization of conditionally immortalized organ of corti cell lines. Cell Biol Int 23(3):175-184.
Kelley MW, Talreja DR, Corwin JT. 1995. Replacement of hair cells after laser microbeam irradiation in cultured organs of corti from embryonic and neonatal mice. J Neurosci 15(4):3013-3026.
Kiang N, Rho J, Northrop C, Liberman M, Ryugo D. 1982. Hair-cell innervation by spiral ganglion cells in adult cats. Science 217:175-177.
Kil SH, Collazo A. 2001. Origins of inner ear sensory organs revealed by fate map and time-lapse analyses. Dev Biol 233(2):365-379.
Kim WY, Fritzsch B, Serls A, Bakel LA, Huang EJ, Reichardt LF, Barth DS, Lee JE. 2001. NeuroD-null mice are deaf due to a severe loss of the inner ear sensory neurons during development. Development 128(3):417-426.
Kojima K, Takebayashi S, Nakagawa T, Ito J. 2004. Expression of nestin epitopes in the developing rat cochlea sensory epithelia. Acta Otolaryngol 124(supplement 551):14-17.
Kornblum HI, Zurcher SD, Werb Z, Derynck R, Seroogy KB. 1999. Multiple trophic actions of heparin-binding epidermal growth factor (HB-EGF) in the central nervous system. Eur J Neurosci 11(9):3236-3246.
Kuijpers W, Peters TA, Tonnaer EL, Ramaekers FC. 1991. Expression of cytokeratin polypeptides during development of the rat inner ear. Histochemistry 96(6):511-521.
Lanford PJ, Shailam R, Norton CR, Gridley T, Kelley MW. 2000. Expression of Math1 and HES5 in the cochleae of wildtype and Jag2 mutant mice. J Assoc Res Otolaryngol 1(2):161-171.
Lang H, Fekete DM. 2001. Lineage analysis in the chicken inner ear shows differences in clonal dispersion for epithelial, neuronal, and mesenchymal cells. Dev Biol 234(1):120-137.
Lawlor P, Marcotti W, Rivolta MN, Kros CJ, Holley MC. 1999. Differentiation of mammalian vestibular hair cells from conditionally immortal, postnatal supporting cells. J Neurosci 19(21):9445-9458.
Lendahl U, Zimmerman LB, McKay RD. 1990. CNS stem cells express a new class of intermediate filament protein. Cell 60(4):585-595.
Li H, Liu H, Heller S. 2003a. Pluripotent stem cells from the adult mouse inner ear. Nat Med 9(10):1293-1299.
Li H, Roblin G, Liu H, Heller S. 2003b. Generation of hair cells by stepwise differentiation of embryonic stem cells. Proc Natl Acad Sci U S A 100(23):13495-13500.
Ma Q, Chen Z, del Barco Barrantes I, de la Pompa JL, Anderson DJ. 1998. neurogenin1 is essential for the determination of neuronal precursors for proximal cranial sensory ganglia. Neuron 20(3):469-482.
Malgrange B, Belachew S, Thiry M, Nguyen L, Rogister B, Alvarez ML, Rigo JM, van de Water TR, Moonen G, Lefebvre PP. 2002. Proliferative generation of mammalian auditory hair cells in culture. Mech Dev 112:79-88.
Mitsui K, Tokuzawa Y, Itoh H, Segawa K, Murakami M, Takahashi K, Maruyama M, Maeda M, Yamanaka S. 2003. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 113(5):631-642.
Noden DM. 1983. The role of the neural crest in patterning of avian cranial skeretal, connective, and muscle tissue. DevBiol 96:144-165.
Palmer TD, Takahashi J, Gage FH. 1997. The adult rat hippocampus contains primordial neural stem cells. Mol Cell Neurosci 8(6):389-404.
Rivolta MN, Grix N, Lawlor P, Ashmore JF, Jagger DJ, Holley MC. 1998. Auditory hair cell precursors immortalized from the mammalian inner ear. Proc R Soc Lond B Biol Sci 265(1406):1595-1603.
Rivolta M, Halsall A, Johnson C, Tones M, Holley M. 2002. Transcript profiling of functionally related groups of genes during conditional differentiation of a Mammalian cochlear hair cell line. Genome Res 12:1091-1099.
Rubel EW, Fritzsch B. 2002. Auditory system development: primary auditory neurons and their targets. Annu Rev Neurosci 25:51-101.
Ruben RJ. 1967. Development of the inner ear of the mouse: a radioautographic study of terminal mitoses. Acta Otolaryngol 220:1-44.
Sejersen T, Lendahl U. 1993. Transient expression of the intermediate filament nestin during skeletal muscle development. J Cell Sci 106(Pt 4):1291-1300.
Self T, Sobe T, Copeland NG, Jenkins NA, Avraham KB, Steel KP. 1999. Role of myosin VI in the differentiation of cochlear hair cells. Dev Biol 214(2):331-341.
Sher AE. 1971. The embryonic and postnatal development of the inner ear of the mouse. Acta Otolaryngol 285:1-77.
Sibilia M, Fleischmann A, Behrens A, Stingl L, Carroll J, Watt FM, Schlessinger J, Wagner EF. 2000. The EGF receptor provides an essential survival signal for SOS-dependent skin tumor development. Cell 102(2):211-220.
Tanigaki K, Nogaki F, Takahashi J, Tashiro K, Kurooka H, Honjo T. 2001. Notch1 and Notch3 instructively restrict bFGF-responsive multipotent neural progenitor cells to an astroglial fate. Neuron 29:45-55.
Torres M, Gomez-Pardo E, Gruss P. 1996. Pax2 contributes to inner ear patterning and optic nerve trajectory. Development 122:3381-3391.
Van De Water TR, Kojima K, Tateya I, Ito J, Malgrange B, Lefebvre PP, Staecker H, Mehler MF. 2004. Stem cell biology of the inner ear and potential therapeutic applications. In: Turksen K, editor. Adult stem cell. Totowa, NJ: Humana Press. p 269-288.
Wang W, Grimmer JF, Van De Water T, Lufkin T. 2004. Hmx2and Hmx3 homeobox genes direct development of the murine inner ear and hypothalmus and can be functionally replaced by Drosophila Hmx. Dev Cell 7:439-453.
White PM, Doetzlhofer A, Lee YS, Groves AK, Segil N. 2006. Mammalian cochlear supporting cells can divide and trans-differentiate into hair cells. Nature 441(7096):984-987.
Woods C, Montcouquiol M, Kelley MW. Math 1 regulates development of the sensory epithelium in the mammalian cochlea. Nat. Neurosci. Dec 2004;7(12):1310-1318.
Xiang M, Gan L, Li D, Chen ZY, Zhou L, O'Malley BW Jr, Klein W, Nathans J. 1997. Essential role of POU-domain factor Brn-3c in auditory and vestibular hair cell development. Proc Natl Acad Sci U S A 94(17):9445-9450.
Yamashita H, Oesterle EC. 1995. Induction of cell proliferation in mammalian inner-ear sensory epithelia by transforming growth factor alpha and epidermal growth factor. Proc Natl Acad Sci U S A 92(8):3152-3155.
Zhai S, Shi L, Wang BE, Zheng G, Song W, Hu Y, Gao WQ. 2005. Isolation and culture of hair cell progenitors from postnatal rat cochleae. J Neurobiol 65(3):282-293.
Zhao HB. 2001. Long-term natural culture of cochlear sensory epithelia of Guinea pigs. Neurosci Lett 315(1-2):73-76.
Zheng JL, Gao WQ. 2000. Overexpression of Math1 induces robust production of extra hair cells in postnatal rat inner ears. Nat Neurosci 3(6):580-586.
Zheng J, Shou J, Guillemot F, Kageyama R, Gao W. 2000. Hes1 is a negative regulator of inner ear hair cell differentiation. Development 127:4551-4560.
Zine A. 2003. Molecular mechanisms that regulate auditory hair-cell differentiationin the mammalian cochlea. Mol Neurobiol 27:223-238.
Zine A, Aubert A, Qiu J, Therianos S, Guillemot F, Kageyama R, de Ribaupierre F. 2001. Hes1 and Hes5 activities are required for the normal development of the hair cells in the mammalian inner ear. J Neurosci 21:4712-4720.