Regeneration of mammalian cochlear and vestibular hair cells through Hes1/Hes5 modulation with siRNA

Hearing Research

Volumn 304, Issue , 2013, Pages 91-110

  Du, Xiaoping ^a   Li, Wei ^a   Gao, Xinsheng ^a,d   West, Matthew B ^a   Saltzman, W Mark ^c   Cheng, Christopher J ^c   Stewart, Charles ^a   Zheng, Jie ^a   Cheng, Weihua ^a   Kopke, Richard D ^a,b  

^a HOUGH EAR INSTITUTE   (United States)

^b OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

^c Yale University   (United States)

^d UNIVERSITY OF TEXAS   (United States)

Author keywords

Hair cell regeneration; Inner ear; Mouse; Nanoparticle; Notch pathway; SiRNA

Indexed keywords

NANOPARTICLE; NEOMYCIN; POLYGLACTIN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR HES 1; TRANSCRIPTION FACTOR HES 5;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL FATE; CELL REGENERATION; CELL TRANSDIFFERENTIATION; COCHLEA; CONTROLLED STUDY; EPITHELIUM CELL; GENE; GENE EXPRESSION; GENE SILENCING; GENE TARGETING; HAIR CELL; HES1 GENE; HES5 GENE; MOUSE; NANOENCAPSULATION; NONHUMAN; PRIORITY JOURNAL; SACCULUS; TRANSGENIC MOUSE; UPREGULATION; UTRICLE;

4-HNE; 4-HYDROXY-2-NONENAL; GFP; GREEN FLUORESCENT PROTEIN; HAIR CELL; HAIR CELL REGENERATION; HAIRY AND ENHANCER OF SPLIT 1 AND 5; HC; HES1 AND HES5; INNER EAR; LF; LIPOFECTION; MOUSE; NANOPARTICLE; NOTCH PATHWAY; NP; OC; PLGA; POLY(LACTIDE-CO-GLYCOLIDE ACID); QRT-PCR; QUANTITATIVE REAL-TIME POLYMERASE CHAIN REACTION; SC; SCRAMBLED SIRNA; SCRNA; SIRNA; SMALL INTERFERING RNA; SUPPORTING CELL; THE ORGAN OF CORTI;

ALDEHYDES; ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; HAIR CELLS, AUDITORY; HAIR CELLS, VESTIBULAR; HOMEODOMAIN PROTEINS; HUMANS; LACTIC ACID; MICE; MICE, TRANSGENIC; NANOPARTICLES; NEOMYCIN; POLYGLYCOLIC ACID; RECEPTORS, NOTCH; REGENERATION; REPRESSOR PROTEINS; RNA, MESSENGER; RNA, SMALL INTERFERING; TISSUE CULTURE TECHNIQUES;

EID: 84880787336     PISSN: 03785955     EISSN: 18785891     Source Type: Journal    
DOI: 10.1016/j.heares.2013.06.011     Document Type: Article

References (91)

1. Adler H.J., Raphael Y. New hair cells arise from supporting cell conversion in the acoustically damaged chick inner ear. Neurosci. Lett. 1996, 205:17-20.
2. Alvarado D.M., Hawkins R.D., Bashiardes S., Veile R.A., Ku Y.C., Powder K.E., Spriggs M.K., Speck J.D., Warchol M.E., Lovett M. An RNA interference-based screen of transcription factor genes identifies pathways necessary for sensory regeneration in the avian inner ear. J.Neurosci. 2011, 31:4535-4543.
3. Barnes A.L., Wassel R.A., Mondalek F., Chen K., Dormer K.J., Kopke R.D. Magnetic characterization of superparamagnetic nanoparticles pulled through model membranes. Biomagn. Res. Technol. 2007, 5:1.
4. Batts S.A., Shoemaker C.R., Raphael Y. Notch signaling and Hes labeling in the normal and drug-damaged organ of Corti. Hear. Res. 2009, 249:15-22.
5. Bergmans H., Logie C., Van Maanen K., Hermsen H., Meredyth M., Van Der Vlugt C. Identification of potentially hazardous human gene products in GMO risk assessment. Environ. Biosafety Res. 2008, 7:1-9.
6. Bermingham N.A., Hassan B.A., Price S.D., Vollrath M.A., Ben-Arie N., Eatock R.A., Bellen H.J., Lysakowski A., Zoghbi H.Y. Math1: an essential gene for the generation of inner ear hair cells. Science 1999, 284:1837-1841.
7. Bermingham-McDonogh O., Rubel E.W. Hair cell regeneration: winging our way towards a sound future. Curr. Opin. Neurobiol. 2003, 13:119-126.
8. Brigande J.V., Heller S. Quo vadis, hair cell regeneration?. Nat. Neurosci. 2009, 12:679-685.
9. Cartiera M.S., Johnson K.M., Rajendran V., Caplan M.J., Saltzman W.M. The uptake and intracellular fate of PLGA nanoparticles in epithelial cells. Biomaterials 2009, 30:2790-2798.
10. Castanotto D., Rossi J.J. The promises and pitfalls of RNA-interference-based therapeutics. Nature 2009, 457:426-433.
11. Chalfie M., Tu Y., Euskirchen G., Ward W.W., Prasher D.C. Green fluorescent protein as a marker for gene expression. Science 1994, 263:802-805.
12. Chen P., Segil N. p27(Kip1) links cell proliferation to morphogenesis in the developing organ of Corti. Development 1999, 126:1581-1590.
13. Cheng C.J., Saltzman W.M. Enhanced siRNA delivery into cells by exploiting the synergy between targeting ligands and cell-penetrating peptides. Biomaterials 2011, 32:6194-6203.
14. Collado M.S., Thiede B.R., Baker W., Askew C., Igbani L.M., Corwin J.T. The postnatal accumulation of junctional E-cadherin is inversely correlated with the capacity for supporting cells to convert directly into sensory hair cells in mammalian balance organs. J.Neurosci. 2011, 31:11855-11866.
15. Corwin J.T., Cotanche D.A. Regeneration of sensory hair cells after acoustic trauma. Science 1988, 240:1772-1774.
16. Cotanche D.A. Genetic and pharmacological intervention for treatment/prevention of hearing loss. J.Commun. Disord. 2008, 41:421-443.
17. Cu Y., Booth C.J., Saltzman W.M. Invivo distribution of surface-modified PLGA nanoparticles following intravaginal delivery. J.Control. Release 2011, 156:258-264.
18. Cu Y., Lemoellic C., Caplan M.J., Saltzman W.M. Ligand-modified gene carriers increase uptake in target cells but reduce DNA release and transfection efficiency. Nanomedicine 2010, 6:334-343.
19. Cu Y., Saltzman W.M. Controlled surface modification with poly(ethylene)glycol enhances diffusion of PLGA nanoparticles in human cervical mucus. Mol. Pharm. 2009, 6:173-181.
20. Davda J., Labhasetwar V. Characterization of nanoparticle uptake by endothelial cells. Int. J. Pharm. 2002, 233:51-59.
21. Davis M.E., Zuckerman J.E., Choi C.H., Seligson D., Tolcher A., Alabi C.A., Yen Y., Heidel J.D., Ribas A. Evidence of RNAi in humans from systemically administered siRNA via targeted nanoparticles. Nature 2010, 464:1067-1070.
22. Doetzlhofer A., White P., Lee Y.S., Groves A., Segil N. Prospective identification and purification of hair cell and supporting cell progenitors from the embryonic cochlea. Brain Res. 2006, 1091:282-288.
23. Dormer K.J., Awasti V., Galbraith W., Kopke R.D., Chen K., Wassel R. Magnetically targeted, Technetium99m labeled nanoparticles to the inner ear. J.Biomed. Nanotechnology 2008, 4:174-184.
24. Du X., Chen K., Kuriyavar S., Kopke R.D., Grady B.P., Bourne D.H., Li W., Dormer K.J. Magnetic targeted delivery of dexamethasone acetate across the round window membrane in guinea pigs. Otol. Neurotol. 2013, 34:41-47. 10.1097/MAO.0b013e318277a40e.
25. Duncan L.J., Mangiardi D.A., Matsui J.I., Anderson J.K., McLaughlin-Williamson K., Cotanche D.A. Differential expression of unconventional myosins in apoptotic and regenerating chick hair cells confirms two regeneration mechanisms. J.Comp. Neurol. 2006, 499:691-701.
26. Fekete D.M., Muthukumar S., Karagogeos D. Hair cells and supporting cells share a common progenitor in the avian inner ear. J.Neurosci. 1998, 18:7811-7821.
27. Forge A., Li L., Corwin J.T., Nevill G. Ultrastructural evidence for hair cell regeneration in the mammalian inner ear. Science 1993, 259:1616-1619.
28. Forge A., Li L., Nevill G. Hair cell recovery in the vestibular sensory epithelia of mature guinea pigs. J.Comp. Neurol. 1998, 397:69-88.
29. Gao X., Wang Y., Chen K., Grady B., Dormer K., Kopke R. Magnetic assisted transport of PLGA nanoparticles through a human round window membrane model. J.Nanotechnol. Eng. Med. 2010, 10.1115/1.4002043.
30. Ge X., Jackson R.L., Liu J., Harper E.A., Hoffer M.E., Wassel R.A., Dormer K.J., Kopke R.D., Balough B.J. Distribution of PLGA nanoparticles in chinchilla cochleae. Otolaryngol. Head Neck Surg. 2007, 137:619-623.
31. Guzman J., Ruiz J., Eshraghi A.A., Polak M., Garnham C., Balkany T.J., Van de Water T.R. Triamcinolone acetonide protects auditory HCs from 4-hydroxy-2, 3-nonenal (HNE) ototoxicity invitro. Acta Otolaryngol. 2006, 126:685-690.
32. Hartman B.H., Basak O., Nelson B.R., Taylor V., Bermingham-McDonogh O., Reh T.A. Hes5 expression in the postnatal and adult mouse inner ear and the drug-damaged cochlea. J.Assoc. Res. Otolaryngol. 2009, 10:321-340. 10.1007/s10162-009-0162-2.
33. Hori R., Nakagawa T., Sakamoto T., Matsuoka Y., Takebayashi S., Ito J. Pharmacological inhibition of Notch signaling in the mature guinea pig cochlea. Neuroreport 2007, 18:1911-1914.
34. Izumikawa M., Batts S.A., Miyazawa T., Swiderski D.L., Raphael Y. Response of the flat cochlear epithelium to forced expression of Atoh1. Hear. Res. 2008, 240:52-56.
35. Izumikawa M., Minoda R., Kawamoto K., Abrashkin K.A., Swiderski D.L., Dolan D.F., Brough D.E., Raphael Y. Auditory hair cell replacement and hearing improvement by Atoh1 gene therapy in deaf mammals. Nat. Med. 2005, 11:271-276.
36. Jia S., Yang S., Guo W., He D.Z. Fate of mammalian cochlear hair cells and stereocilia after loss of the stereocilia. J.Neurosci. 2009, 2(29):15277-15285.
37. Johnsson L.G., Hawkins J.E. Degeneration patterns in human ears exposed to noise. Ann. Otol. Rhinol. Laryngol. 1976, 85:725-739.
38. Jung J.Y., Avenarius M.R., Adamsky S., Alpert E., Feinstein E., Raphael Y. siRNA targeting Hes5 augments hair cell regeneration in aminoglycoside-damaged mouse utricle. Mol. Ther. 2013, 21:834-841. 10.1038/mt.2013.18.
39. Kain S.R., Adams M., Kondepudi A., Yang T.T., Ward W.W., Kitts P. Green fluorescent protein as a reporter of gene expression and protein localization. Biotechniques 1995, 19:650-655.
40. Kawamoto K., Izumikawa M., Beyer L.A., Atkin G.M., Raphael Y. Spontaneous hair cell regeneration in the mouse utricle following gentamicin ototoxicity. Hear. Res. 2009, 247:17-26.
41. Kawamoto K., Ishimoto S., Minoda R., Brough D.E., Raphael Y. Math1 gene transfer generates new cochlear hair cells in mature guinea pigs invivo. J.Neurosci. 2003, 23:4395-4400.
42. Kelley M.W. Regulation of cell fate in the sensory epithelia of the inner ear. Nat. Rev. Neurosci. 2006, 7:837-849.
43. Kiernan A.E., Cordes R., Kopan R., Gossler A., Gridley T. The Notch ligands DLL1 and JAG2 act synergistically to regulate hair cell development in the mammalian inner ear. Development 2005, 132:4353-4362.
44. Kopke R.D., Jackson R.L., Li G., Rasmussen M.D., Hoffer M.E., Frenz D.A., Costello M., Schultheiss P., T.R Van De Water Growth factor treatment enhances vestibular hair cell renewal and results in improved vestibular function. Proc. Natl. Acad. Sci. U S A 2001, 98:5886-5891.
45. Kopke R.D., Wassel R.A., Mondalek F., Grady B., Chen K., Liu J., Gibson D., Dormer K.J. Magnetic nanoparticles: inner ear targeted molecule delivery and middle ear implant. Audiol. Neurootol. 2006, 11:123-133.
46. Laine H., Sulg M., Kirjavainen A., Pirvola U. Cell cycle regulation in the inner ear sensory epithelia: role of cyclin D1 and cyclin-dependent kinase inhibitors. Dev. Biol. 2010, 337:134-146.
47. Lanford P.J., Lan Y., Jiang R., Lindsell C., Weinmaster G., Gridley T., Kelley M.W. Notch signalling pathway mediates hair cell development in mammalian cochlea. Nat. Genet. 1999, 21:289-292.
48. Lin V., Golub J.S., Nguyen T.B., Hume C.R., Oesterle E.C., Stone J.S. Inhibition of notch activity promotes nonmitotic regeneration of hair cells in the adult mouse utricles. J.Neurosci. 2011, 31:15329-15339.
49. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
50. Lopez I., Honrubia V., Lee S.C., Schoeman G., Beykirch K. Quantification of the process of hair cell loss and recovery in the chinchilla crista ampullaris after gentamicin treatment. Int. J. Dev. Neurosci. 1997, 15:447-461.
51. Löwenheim H., Furness D.N., Kil J., Zinn C., Gültig K., Fero M.L., Frost D., Gummer A.W., Roberts J.M., Rubel E.W., Hackney C.M., Zenner H.P. Gene disruption of p27(Kip1) allows cell proliferation in the postnatal and adult organ of corti. Proc. Natl. Acad. Sci. U. S. A 1999, 96:4084-4088.
52. Ma E.Y., Rubel E.W., Raible D.W. Notch signaling regulates the extent of hair cell regeneration in the zebrafish lateral line. J.Neurosci. 2008, 28:2261-2273.
53. Maeda Y., Fukushima K., Nishizaki K., Smith R.J. Invitro and invivo suppression of GJB2 expression by RNA interference. Hum. Mol. Genet. 2005, 14:1641-1650.
54. Minoda R., Izumikawa M., Kawamoto K., Zhang H., Raphael Y. Manipulating cell cycle regulation in the mature cochlea. Hear. Res. 2007, 232:44-51.
55. Mizutari K., Fujioka M., Hosoya M., Bramhall N., Okano H.J., Okano H., Edge A.S. Notch inhibition induces cochlear hair cell regeneration and recovery of hearing after acoustic trauma. Neuron 2013, 77:58-69. 10.1016/j.neuron.2012.10.032.
56. Mondalek F.G., Zhang Y.Y., Kropp B., Kopke R.D., Ge X., Jackson R.L., Dormer K.J. The permeability of SPION over an artificial three-layer membrane is enhanced by external magnetic field. J.Nanobiotechnology 2006, 4:4. 10.1186/1477-3155-4-4.
57. Mukherjea D., Jajoo S., Whitworth C., Bunch J.R., Turner J.G., Rybak L.P., Ramkumar V. Short interfering RNA against transient receptor potential vanilloid 1 attenuates cisplatin-induced hearing loss in the rat. J.Neurosci. 2008, 28:13056-13065.
58. Murata J., Tokunaga A., Okano H., Kubo T. Mapping of notch activation during cochlear development in mice: implications for determination of prosensory domain and cell fate diversification. J.Comp. Neurol. 2006, 497:502-518.
59. Ozeki M., Hamajima Y., Feng L., Ondrey F.G., Schlentz E., Lin J. Id1 induces the proliferation of cochlear sensory epithelial cells via the nuclear factor-kappaB/cyclin D1 pathway invitro. J.Neurosci. Res. 2007, 85:515-524.
60. Raft S., Koundakjian E.J., Quinones H., Jayasena C.S., Goodrich L.V., Johnson J.E., Segil N., Groves A.K. Cross-regulation of Ngn1 and Math1 coordinates the production of neurons and sensory hair cells during inner ear development. Development 2007, 134:4405-4415.
61. Riley B.B., Chiang M., Farmer L., Heck R. The deltaA gene of zebrafish mediates lateral inhibition of hair cells in the inner ear and is regulated by pax2.1. Development 1999, 126:5669-5678.
62. Ruiz J.W., Guzman J., Polak M., Eshraghi A.A., Balkany T.J., Van De Water T.R. Glutathione ester protects against hydroxynonenal-induced loss of auditory hair cells. Otolaryngol. Head Neck Surg. 2006, 135:792-797.
63. Ryals B.M., Rubel E.W. Hair cell regeneration after acoustic trauma in adult Coturnix quail. Science 1988, 240:1774-1776.
64. Rybak L.P., Ramkumar V. Ototoxicity. Kidney Int. 2007, 72:931-935.
65. Salcher E.E., Wagner E. Chemically programmed polymers for targeted DNA and siRNA transfection. Top. Curr. Chem. 2010, 296:227-249.
66. Seibel N.M., Eljouni J., Nalaskowski M.M., Hampe W. Nuclear localization of enhanced green fluorescent protein homomultimers. Anal. Biochem. 2007, 368:95-99.
67. Shnerson A., Devigne C., Pujol R. Age-related changes in the C57BL/6J mouse cochlea. II. Ultrastructural findings. Brain Res. 1981, 254:77-88.
68. Shou J., Zheng J.L., Gao W.Q. Robust generation of new hair cells in the mature mammalian inner ear by adenoviral expression of Hath1. Mol. Cell Neurosci. 2003, 23:169-179.
69. Sinkkonen S.T., Chai R., Jan T.A., Hartman B.H., Laske R.D., Gahlen F., Sinkkonen W., Cheng A.G., Oshima K., Heller S. Intrinsic regenerative potential of murine cochlear supporting cells. Sci. Rep. 2011, 1:26. 10.1038/srep00026.
70. Sobkowicz H.M., August B.K., Slapnick S.M. Post-traumatic survival and recovery of the auditory sensory cells in culture. Acta Otolaryngol. 1996, 116:257-262.
71. Staecker H., Praetorius M., Baker K., Brough D.E. Vestibular hair cell regeneration and restoration of balance function induced by math1 gene transfer. Otol. Neurotol. 2007, 28:223-231.
72. Stone J.S., Oesterle E.C., Rubel E.W. Recent insights into regeneration of auditory and vestibular hair cells. Curr. Opin. Neurol. 1998, 11:17-24.
73. Takebayashi S., Yamamoto N., Yabe D., Fukuda H., Kojima K., Ito J., Honjo T. Multiple roles of notch signaling in cochlear development. Dev. Biol. 2007, 307:165-178.
74. Tang L.S., Alger H.M., Pereira F.A. COUP-TFI controls notch regulation of hair cell and support cell differentiation. Development 2006, 133:3683-3693.
75. Tateya T., Imayoshi I., Tateya I., Ito J., Kageyama R. Cooperative functions of Hes/Hey genes in auditory hair cell and supporting cell development. Dev. Biol. 2011, 352:329-340. 10.1016/j.ydbio.2011.01.038.
76. Taylor S., Wakem M., Dijkman G., Alsarraj M., Nguyen M. Apractical approach to RT-qPCR-publishing data that conform to the MIQE guidelines. Methods 2010, 50:S1-S5.
77. Torchinsky C., Messana E.P., Arsura M., Cotanche D.A. Regulation of p27Kip1 during gentamicin mediated hair cell death. J.Neurocytol. 1999, 28:913-924.
78. Walsh R.M., Hackney C.M., Furness D.N. Regeneration of the mammalian vestibular sensory epithelium following gentamicin-induced damage. J.Otolaryngol. 2000, 29:351-360.
79. Wang G., Chatterjee I., Batts S., Wong H., Gong T., Gong S., Raphael Y. Notch signaling and Atoh1 expression during hair cell regeneration in the mouse utricle. Hear. Res. 2010, 267:61-70.
80. Wang Y., Gao X., Kuriyavar S., Bourne D., Grady B., Chen K., Dormer K., Kopke R. Incorporation, release and effectiveness of dexamethasone in poly (lactic-co-glycolic acid) nanoparticles for inner ear drug delivery. J.Nanotechnol. Eng. Med. 2011, 10.1115/1.4002928.
81. Wassel R.A., Grady B., Kopke R.D., Dormer K.J. Dispersion of super paramagnetic iron oxide nanoparticles in poly(d, l-lactide-co-glycolide) microparticles. Colloids Surf. A: Physicochem. Eng. Aspects 2007, 292:125-130.
82. Wei X., Henke V.G., Strübing C., Brown E.B., Clapham D.E. Real-time imaging of nuclear permeation by EGFP in single intact cells. Biophys. J. 2003, 84:1317-1327.
83. 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 2006, 441:984-987.
84. Whitehead K.A., Langer R., Anderson D.G. Knocking down barriers: advances in siRNA delivery. Nat. Rev. Drug Discov. 2009, 8:129-138.
85. Woodrow K.A., Cu Y., Booth C.J., Saucier-Sawyer J.K., Wood M.J., Saltzman W.M. Intravaginal gene silencing using biodegradable polymer nanoparticles densely loaded with small-interfering RNA. Nat. Mater. 2009, 8:526-533.
86. Yamamoto N., Tanigaki K., Tsuji M., Yabe D., Ito J., Honjo T. Inhibition of Notch/RBP-J signaling induces hair cell formation in neonate mouse cochleas. J.Mol. Med. 2006, 84:37-45.
87. Ylikoski J., Pirvola U., Lehtonen E. Distribution of F-actin and fodrin in the hair cells of the guinea pig cochlea as revealed by confocal fluorescence microscopy. Hear. Res. 1992, 60:80-88.
88. Zheng J.L., Gao W.Q. Overexpression of Math1 induces robust production of extra hair cells in postnatal rat inner ears. Nat. Neurosci. 2000, 3:580-586.
89. Zheng J.L., Shou J., Guillemot F., Kageyama R., Gao W.Q. Hes1 is a negative regulator of inner ear hair cell differentiation. Development 2000, 127:4551-4560.
90. Zine A., Aubert A., Qiu J., Therianos S., Guillemot F., Kageyama R., de Ribaupierre F. Hes1 and Hes5 activities are required for the normal development of the hair cells in the mammalian inner ear. J.Neurosci. 2001, 21:4712-4720.
91. Zine A., de Ribaupierre F. Notch/Notch ligands and Math1 expression patterns in the organ of Corti of wild-type and Hes1 and Hes5 mutant mice. Hear. Res. 2002, 170:22-31.