Clonal Expansion of Lgr5-Positive Cells from Mammalian Cochlea and High-Purity Generation of Sensory Hair Cells

Cell Reports

Volumn 18, Issue 8, 2017, Pages 1917-1929

  McLean, Will J ^a,b,c,h   Yin, Xiaolei ^a,c,d,e,f   Lu, Lin ^d,e   Lenz, Danielle R ^a,b   McLean, Dalton ^a,b   Langer, Robert ^c,d,g   Karp, Jeffrey M ^a,c,e,f   Edge, Albert S B ^a,b,c,f  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS EYE AND EAR INFIRMARY   (United States)

^c HARVARD MIT DIVISION OF HEALTH SCIENCES AND TECHNOLOGY   (United States)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^e BRIGHAM AND WOMEN S HOSPITAL   (United States)

^f HARVARD STEM CELL INSTITUTE   (United States)

^g Massachusetts Institute of Technology   (United States)

^h Frequency Therapeutics   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; GLYCOGEN SYNTHASE KINASE 3BETA; HISTONE DEACETYLASE INHIBITOR; LGR5 PROTEIN; PHOSPHOTRANSFERASE INHIBITOR; UNCLASSIFIED DRUG; WNT PROTEIN; G PROTEIN COUPLED RECEPTOR; LGR5 PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ACTIVITY; CELL CLONE; CELL COUNT; CELL EXPANSION; CELL PROLIFERATION; CELL STIMULATION; COCHLEAR HAIR CELL; CONTROLLED STUDY; EPITHELIUM CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; MAMMAL CELL; MOLECULAR BIOLOGY; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; PROTEIN EXPRESSION; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; STEM CELL; SYNAPTOGENESIS; TARGET CELL; TRANSCRIPTION INITIATION; ANIMAL; CELL DIFFERENTIATION; COCHLEA; MAMMAL; METABOLISM; PHYSIOLOGY; SYNAPSE; WNT SIGNALING;

ADULT; ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; COCHLEA; HAIR CELLS, AUDITORY; HUMANS; MALE; MAMMALS; MICE; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; STEM CELLS; SYNAPSES; WNT SIGNALING PATHWAY;

EID: 85013887018     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2017.01.066     Document Type: Article

References (47)

1. Barker, N., van Es, J.H., Kuipers, J., Kujala, P., van den Born, M., Cozijnsen, M., Haegebarth, A., Korving, J., Begthel, H., Peters, P.J., Clevers, H., Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449 (2007), 1003–1007.
2. Bramhall, N.F., Shi, F., Arnold, K., Hochedlinger, K., Edge, A.S., Lgr5-positive supporting cells generate new hair cells in the postnatal cochlea. Stem Cell Reports 2 (2014), 311–322.
3. Chai, R., Kuo, B., Wang, T., Liaw, E.J., Xia, A., Jan, T.A., Liu, Z., Taketo, M.M., Oghalai, J.S., Nusse, R., et al. Wnt signaling induces proliferation of sensory precursors in the postnatal mouse cochlea. Proc. Natl. Acad. Sci. USA 109 (2012), 8167–8172.
4. Cox, B.C., Chai, R., Lenoir, A., Liu, Z., Zhang, L., Nguyen, D.H., Chalasani, K., Steigelman, K.A., Fang, J., Rubel, E.W., et al. Spontaneous hair cell regeneration in the neonatal mouse cochlea in vivo. Development 141 (2014), 816–829.
5. Dallos, P., Wu, X., Cheatham, M.A., Gao, J., Zheng, J., Anderson, C.T., Jia, S., Wang, X., Cheng, W.H., Sengupta, S., et al. Prestin-based outer hair cell motility is necessary for mammalian cochlear amplification. Neuron 58 (2008), 333–339.
6. Davis, A.C., Hearing disorders in the population: first phase findings of the MRC National Study of Hearing. Lutman, M.E., Haggard, M.P., (eds.) Hearing Science and Hearing Disorders, 1983, Academic Press, 35–60.
7. de Lau, W., Barker, N., Low, T.Y., Koo, B.K., Li, V.S., Teunissen, H., Kujala, P., Haegebarth, A., Peters, P.J., van de Wetering, M., et al. Lgr5 homologues associate with Wnt receptors and mediate R-spondin signalling. Nature 476 (2011), 293–297.
8. Denayer, T., Locker, M., Borday, C., Deroo, T., Janssens, S., Hecht, A., van Roy, F., Perron, M., Vleminckx, K., Canonical Wnt signaling controls proliferation of retinal stem/progenitor cells in postembryonic Xenopus eyes. Stem Cells 26 (2008), 2063–2074.
9. Edge, A.S., Chen, Z.Y., Hair cell regeneration. Curr. Opin. Neurobiol. 18 (2008), 377–382.
10. Esteban, M.A., Wang, T., Qin, B., Yang, J., Qin, D., Cai, J., Li, W., Weng, Z., Chen, J., Ni, S., et al. Vitamin C enhances the generation of mouse and human induced pluripotent stem cells. Cell Stem Cell 6 (2010), 71–79.
11. Fujioka, M., Okano, H., Edge, A.S., Manipulating cell fate in the cochlea: a feasible therapy for hearing loss. Trends Neurosci. 38 (2015), 139–144.
12. Greenblatt, D.Y., Vaccaro, A.M., Jaskula-Sztul, R., Ning, L., Haymart, M., Kunnimalaiyaan, M., Chen, H., Valproic acid activates notch-1 signaling and regulates the neuroendocrine phenotype in carcinoid cancer cells. Oncologist 12 (2007), 942–951.
13. Hochedlinger, K., Yamada, Y., Beard, C., Jaenisch, R., Ectopic expression of Oct-4 blocks progenitor-cell differentiation and causes dysplasia in epithelial tissues. Cell 121 (2005), 465–477.
14. Hua, X., Thompson, C.B., Quiescent T cells: actively maintaining inactivity. Nat. Immunol. 2 (2001), 1097–1098.
15. Huch, M., Bonfanti, P., Boj, S.F., Sato, T., Loomans, C.J., van de Wetering, M., Sojoodi, M., Li, V.S., Schuijers, J., Gracanin, A., et al. Unlimited in vitro expansion of adult bi-potent pancreas progenitors through the Lgr5/R-spondin axis. EMBO J. 32 (2013), 2708–2721.
16. Hudspeth, A.J., Making an effort to listen: mechanical amplification in the ear. Neuron 59 (2008), 530–545.
17. Jacques, B.E., Puligilla, C., Weichert, R.M., Ferrer-Vaquer, A., Hadjantonakis, A.K., Kelley, M.W., Dabdoub, A., A dual function for canonical Wnt/β-catenin signaling in the developing mammalian cochlea. Development 139 (2012), 4395–4404.
18. Jeon, S.J., Fujioka, M., Kim, S.C., Edge, A.S.B., Notch signaling alters sensory or neuronal cell fate specification of inner ear stem cells. J. Neurosci. 31 (2011), 8351–8358.
19. Kelley, M.W., Regulation of cell fate in the sensory epithelia of the inner ear. Nat. Rev. Neurosci. 7 (2006), 837–849.
20. Kempfle, J.S., Turban, J.L., Edge, A.S.B., Sox2 in the differentiation of cochlear progenitor cells. Sci. Rep., 6, 2016, 23293.
21. Khimich, D., Nouvian, R., Pujol, R., Tom Dieck, S., Egner, A., Gundelfinger, E.D., Moser, T., Hair cell synaptic ribbons are essential for synchronous auditory signalling. Nature 434 (2005), 889–894.
22. Koo, B.K., Clevers, H., Stem cells marked by the R-spondin receptor LGR5. Gastroenterology 147 (2014), 289–302.
23. Korrapati, S., Roux, I., Glowatzki, E., Doetzlhofer, A., Notch signaling limits supporting cell plasticity in the hair cell-damaged early postnatal murine cochlea. PLoS ONE, 8, 2013, e73276.
24. Li, H., Liu, H., Heller, S., Pluripotent stem cells from the adult mouse inner ear. Nat. Med. 9 (2003), 1293–1299.
25. Liu, B., Hunter, D.J., Rooker, S., Chan, A., Paulus, Y.M., Leucht, P., Nusse, Y., Nomoto, H., Helms, J.A., Wnt signaling promotes Müller cell proliferation and survival after injury. Invest. Ophthalmol. Vis. Sci. 54 (2013), 444–453.
26. Lumpkin, E.A., Collisson, T., Parab, P., Omer-Abdalla, A., Haeberle, H., Chen, P., Doetzlhofer, A., White, P., Groves, A., Segil, N., Johnson, J.E., Math1-driven GFP expression in the developing nervous system of transgenic mice. Gene Expr. Patterns 3 (2003), 389–395.
27. Madisen, L., Zwingman, T.A., Sunkin, S.M., Oh, S.W., Zariwala, H.A., Gu, H., Ng, L.L., Palmiter, R.D., Hawrylycz, M.J., Jones, A.R., et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 13 (2010), 133–140.
28. Martinez-Monedero, R., Yi, E., Oshima, K., Glowatzki, E., Edge, A.S., Differentiation of inner ear stem cells to functional sensory neurons. Dev. Neurobiol. 68 (2008), 669–684.
29. Meyers, J.R., MacDonald, R.B., Duggan, A., Lenzi, D., Standaert, D.G., Corwin, J.T., Corey, D.P., Lighting up the senses: FM1-43 loading of sensory cells through nonselective ion channels. J. Neurosci. 23 (2003), 4054–4065.
30. Mizutari, K., Fujioka, M., Hosoya, M., Bramhall, N., Okano, H.J., Okano, H., Edge, A.S.B., Notch inhibition induces cochlear hair cell regeneration and recovery of hearing after acoustic trauma. Neuron 77 (2013), 58–69.
31. Oshima, K., Grimm, C.M., Corrales, C.E., Senn, P., Martinez Monedero, R., Géléoc, G.S., Edge, A., Holt, J.R., Heller, S., Differential distribution of stem cells in the auditory and vestibular organs of the inner ear. J. Assoc. Res. Otolaryngol. 8 (2007), 18–31.
32. Pan, B., Géléoc, G.S., Asai, Y., Horwitz, G.C., Kurima, K., Ishikawa, K., Kawashima, Y., Griffith, A.J., Holt, J.R., TMC1 and TMC2 are components of the mechanotransduction channel in hair cells of the mammalian inner ear. Neuron 79 (2013), 504–515.
33. Pan, W., Jin, Y., Chen, J., Rottier, R.J., Steel, K.P., Kiernan, A.E., Ectopic expression of activated notch or SOX2 reveals similar and unique roles in the development of the sensory cell progenitors in the mammalian inner ear. J. Neurosci. 33 (2013), 16146–16157.
34. Sato, T., Vries, R.G., Snippert, H.J., van de Wetering, M., Barker, N., Stange, D.E., van Es, J.H., Abo, A., Kujala, P., Peters, P.J., Clevers, H., Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459 (2009), 262–265.
35. Seal, R.P., Akil, O., Yi, E., Weber, C.M., Grant, L., Yoo, J., Clause, A., Kandler, K., Noebels, J.L., Glowatzki, E., et al. Sensorineural deafness and seizures in mice lacking vesicular glutamate transporter 3. Neuron 57 (2008), 263–275.
36. Seib, D.R., Corsini, N.S., Ellwanger, K., Plaas, C., Mateos, A., Pitzer, C., Niehrs, C., Celikel, T., Martin-Villalba, A., Loss of Dickkopf-1 restores neurogenesis in old age and counteracts cognitive decline. Cell Stem Cell 12 (2013), 204–214.
37. Shi, F., Cheng, Y.F., Wang, X.L., Edge, A.S., Beta-catenin up-regulates Atoh1 expression in neural progenitor cells by interaction with an Atoh1 3′ enhancer. J. Biol. Chem. 285 (2010), 392–400.
38. Shi, F., Kempfle, J.S., Edge, A.S., Wnt-responsive Lgr5-expressing stem cells are hair cell progenitors in the cochlea. J. Neurosci. 32 (2012), 9639–9648.
39. Shi, F., Hu, L., Edge, A.S., Generation of hair cells in neonatal mice by β-catenin overexpression in Lgr5-positive cochlear progenitors. Proc. Natl. Acad. Sci. USA 110 (2013), 13851–13856.
40. Shi, F., Hu, L., Jacques, B.E., Mulvaney, J.F., Dabdoub, A., Edge, A.S., β-Catenin is required for hair-cell differentiation in the cochlea. J. Neurosci. 34 (2014), 6470–6479.
41. van Es, J.H., van Gijn, M.E., Riccio, O., van den Born, M., Vooijs, M., Begthel, H., Cozijnsen, M., Robine, S., Winton, D.J., Radtke, F., Clevers, H., Notch/gamma-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Nature 435 (2005), 959–963.
42. Weil, D., Levy, G., Sahly, I., Levi-Acobas, F., Blanchard, S., El-Amraoui, A., Crozet, F., Philippe, H., Abitbol, M., Petit, C., Human myosin VIIA responsible for the Usher 1B syndrome: a predicted membrane-associated motor protein expressed in developing sensory epithelia. Proc. Natl. Acad. Sci. USA 93 (1996), 3232–3237.
43. White, P.M., Doetzlhofer, A., Lee, Y.S., Groves, A.K., Segil, N., Mammalian cochlear supporting cells can divide and trans-differentiate into hair cells. Nature 441 (2006), 984–987.
44. Whyte, J.L., Smith, A.A., Helms, J.A., Wnt signaling and injury repair. Cold Spring Harb. Perspect. Biol., 4, 2012, a008078.
45. Yamamoto, N., Chang, W., Kelley, M.W., Rbpj regulates development of prosensory cells in the mammalian inner ear. Dev. Biol. 353 (2011), 367–379.
46. Yang, Q., Bermingham, N.A., Finegold, M.J., Zoghbi, H.Y., Requirement of Math1 for secretory cell lineage commitment in the mouse intestine. Science 294 (2001), 2155–2158.
47. Yin, X., Farin, H.F., van Es, J.H., Clevers, H., Langer, R., Karp, J.M., Niche-independent high-purity cultures of Lgr5+ intestinal stem cells and their progeny. Nat. Methods 11 (2014), 106–112.