Transplantation of mouse embryonic stem cells into the cochlea of an auditory-neuropathy animal model: Effects of timing after injury

JARO - Journal of the Association for Research in Otolaryngology

Volumn 9, Issue 2, 2008, Pages 225-240

  Lang, Hainan ^a   Schulte, Bradley A ^a   Goddard, John C ^a   Hedrick, Michelle ^a   Schulte, Jason B ^a   Wei, Ling ^a   Schmiedt, Richard A ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Embryonic stem cells; Hearing loss; Injured microenvironment; Inner ear; Neovascularization; Rosenthal's canal; Spiral ganglion neurons

Indexed keywords

BIOLOGICAL MARKER; OUABAIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUDITORY CANAL; CELL DIFFERENTIATION; CELL SURVIVAL; CELL VIABILITY; COCHLEA INJURY; CONTROLLED STUDY; EMBRYONIC STEM CELL; ENDOLYMPH; GERBIL; GLIA CELL; INNER EAR; MICROENVIRONMENT; MOUSE; NERVE CELL NECROSIS; NONHUMAN; PERILYMPH; PRIORITY JOURNAL; SPIRAL GANGLION; STEM CELL TRANSPLANTATION;

ANIMALS; CELL DEATH; CELL DIFFERENTIATION; CELLS, CULTURED; COCHLEA; DISEASE MODELS, ANIMAL; EMBRYONIC STEM CELLS; ENDOLYMPH; ENZYME INHIBITORS; FEMALE; GERBILLINAE; GRAFT SURVIVAL; HEARING LOSS, SENSORINEURAL; MALE; MICE; NEOVASCULARIZATION, PHYSIOLOGIC; NEUROGLIA; NEURONS, AFFERENT; OUABAIN; PERILYMPH; SPIRAL GANGLION; STEM CELL TRANSPLANTATION;

EID: 44449093933     PISSN: 15253961     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10162-008-0119-x     Document Type: Article

References (83)

1. Adams LD, Choi L, Xian HQ, Yang A, Sauer B, Wei L, Gottlieb DI. Double lox targeting for neural cell transgenesis. Brain. Res. Mol. Brain Res. 110(2):220-233, 2003.
2. Adamson CL, Reid MA, Mo ZL, Bowne-English J, Davis RL. Firing features and potassium channel content of murine spiral ganglion neurons vary with cochlear location. J. Comp. Neurol. 447(4):331-350, 2002.
3. Alvarez-Buylla A, Lim DA. For the long run: Maintaining germinal niches in the adult brain. Neuron. 41(5):683-686, 2004.
4. Bain G, Gottlieb DI. Neural cells derived by in vitro differentiation of P19 and embryonic stem cells. Perspect. Dev. Neurobiol. 5(2-3):175-178, 1998.
5. Bain G, Kitchens D, Yao M, Huettner JE, Gottlieb DI. Embryonic stem cells express neuronal properties in vitro. Dev. Biol. 168(2):342-357, 1995.
6. Bhave SA, Oesterle EC, Coltrera MD. Macrophage and microglia-like cells in the avian inner ear. J. Comp. Neurol. 398(2):241-256, 1998.
7. Bianchi LM, Raz Y. Methods for providing therapeutic agents to treat damaged spiral ganglion neurons. Curr. Drug Targets CNS Neurol. Disord. 3(3):195-9, 2004.
8. Chalfie M, Tu Y, Euskirchen G, Ward WW, Prasher DC. Green fluorescent protein as a marker for gene expression. Science 263(5148):802-805, 1994.
9. Chung S, Shin BS, Hedlund E, Pruszak J, Ferree A, Kang UJ, Isacson O, Kim KS. Genetic selection of sox1GFP-expressing neural precursors removes residual tumorigenic pluripotent stem cells and attenuates tumor formation after transplantation. J. Neurochem. 97(5):1467-1480, 2006.
10. Coleman B, Hardman J, Coco A, Epp S, de Silva M, Crook J, Shepherd R. Fate of embryonic stem cells transplanted into the deafened mammalian cochlea. Cell Transplant. 15(5):369-380, 2006.
11. Coleman B, de Silva MG, Shepherd RK. Concise review: The potential of stem cells for auditory neuron generation and replacement. Stem Cells 25(11):2685-2694, 2007.
12. Corrales CE, Pan L, Li H, Liberman MC, Heller S, Edge AS. Engraftment and differentiation of embryonic stem cell-derived neural progenitor cells in the cochlear nerve trunk: Growth of processes into the organ of Corti. J. Neurobiol. 66(13):1489-1500, 2006.
13. Dazert S, Aletsee C, Brors D, Sudhoff H, Ryan AF, Muller AM. Regeneration of inner ear cells from stem cell precursors-a future concept of hearing rehabilitation? DNA Cell Biol. 22(9):565-70, 2003.
14. Doetschman TC, Eistetter H, Katz M, Schmidt W, Kemler R. The in vitro development of blastocyst-derived embryonic stem cell lines: Formation of visceral yolk sac, blood islands and myocardium. J. Embryol. Exp. Morphol. 87:27-45, 1985.
15. Doetzlhofer A, White PM, Johnson JE, Segil N, Groves AK. In vitro growth and differentiation of mammalian sensory hair cell progenitors: A requirement for EGF and periotic mesenchyme. Dev. Biol. 272(2):432-447, 2004.
16. Enzmann GU, Benton RL, Woock JP, Howard RM, Tsoulfas P, Whittemore SR. Consequences of noggin expression by neural stem, glial, and neuronal precursor cells engrafted into the injured spinal cord. Exp. Neurol. 195(2):293-304, 2005.
17. Eriksson C, Bjorklund A, Wictorin K. Neuronal differentiation following transplantation of expanded mouse neurosphere cultures derived from different embryonic forebrain regions. Exp. Neurol. 84(2):615-635, 2003.
18. Flax JD, Aurora S, Yang C, Simonin C, Wills AM, Billinghurst LL, Jendoubi M, Sidman RL, Wolfe JH, Kim SU, Snyder EY. Engraftable human neural stem cells respond to developmental cues, replace neurons, and express foreign genes. Nat. Biotechnol. 16(11):1033-1039, 1998.
19. Gates MA, Olsson M, Bjerregaard K, Bjorklund A. Region-specific migration of embryonic glia grafted to the neonatal brain. Neuroscience 84(4):1013-1023, 1998.
20. Hildebrand MS, Dahl HH, Hardman J, Coleman B, Shepherd RK, de Silva MG. Survival of partially differentiated mouse embryonic stem cells in the scala media of the guinea pig cochlea. J. Assoc. Res. Otolaryngol. 6(4):341-354, 2006.
21. Hu Z, Ulfendahl M, Olivius NP. Central migration of neuronal tissue and embryonic stem cells following transplantation along the adult auditory nerve. Brain Res. 1026(1):68-73, 2004.
22. Hu Z, Wei D, Johansson CB, Holmstrom N, Duan M, Frisen J, Ulfendahl M. Survival and neural differentiation of adult neural stem cells transplanted into the mature inner ear. Exp. Cell Res. 302(1):40-47, 2005.
23. Hu Z, Ulfendahl M. Cell replacement therapy in the inner ear. Stem Cells Dev. 15(3):449-459, 2006.
24. In Park K, Hack MA, Ourednik J, Yandava B, Flax JD, Stieg PE, Gullans S, Jensen FE, Sidman RL, Ourednik V, Snyder EY. Acute injury directs the migration, proliferation, and differentiation of solid organ stem cells: Evidence from the effect of hypoxia-ischemia in the CNS on clonal "reporter" neural stem cells. Exp. Neurol. 199(1):156-178, 2006.
25. Ito J, Kojima K, Kawaguchi S. Survival of neural stem cells in the cochlea. Acta Otolaryngol. 121(2):140-142, 2001.
26. Kasischke KA, Vishwasrao HD, Fisher PJ, Zipfel WR, Webb WW. Neural activity triggers neuronal oxidative metabolism followed by astrocytic glycolysis. Science 305(5680):99-103, 2006.
27. Keirstead HS, Nistor G, Bernal G, Totoiu M, Cloutier F, Sharp K, Steward O. Human embryonic stem cell-derived oligodendrocyte progenitor cell transplants remyelinate and restore locomotion after spinal cord injury. J. Neurosci. 25(19):4694-4705, 2005.
28. Kojima K, Murata M, Nishio T, Kawaguchi S, Ito J. Survival of fetal rat otocyst cells grafted into the damaged inner ear. Acta Otolaryngol. Suppl. 551:53-55, 2004.
29. Kondo T, Johnson SA, Yoder MC, Romand R, Hashino E. Sonic hedgehog and retinoic acid synergistically promote sensory fate specification from bone marrow-derived pluripotent stem cells. Proc. Natl. Acad. Sci. U. S. A. 102(13):4789-4794, 2005.
30. Lagenaur C, Schachner M. Monoclonal antibody (M2) to glial and neuronal cell surfaces. J. Supramol. Struct. Cell Biochem. 15(4):335-346, 1981.
31. Lang H, Schulte BA, Schmiedt RA. Endocochlear potentials and compound action potential recovery functions in the C57BL/6J mouse. Hear Res. 172(1-2):118-126, 2002.
32. Lang H, Schulte BA, Schmiedt RA. Ouabain induces apoptotic cell death in type I spiral ganglion neurons, but not type II neurons. J. Assoc. Res. Otolaryngol. 6(1):63-74, 2005.
33. Lang H, Schulte BA, Zhou D, Smythe N, Spicer SS, Schmiedt RA. Nuclear factor kappaB deficiency is associated with auditory nerve degeneration and increased noise-induced hearing loss. J. Neurosci. 26(13):3541-3550, 2006.
34. Leventhal C, Rafii S, Rafii D, Shahar A, Goldman SA. Endothelial trophic support of neuronal production and recruitment from the adult mammalian subependyma. Mol. Cell Neurosci. 13(6):450-464, 1999.
35. Li H, Liu H, Heller S. Pluripotent stem cells from the adult mouse inner ear. Nat. Med. 9(10):1293-1299, 2003a.
36. Li H, Roblin G, Liu H, Heller S. Generation of hair cells by stepwise differentiation of embryonic stem cells. Proc. Natl. Acad. Sci. U. S. A. 100(23):13495-13500, 2003b.
37. Li H, Corrales CE, Edge A, Heller S. Stem cells as therapy for hearing loss. Trends Mol. Med. 10(7):309-315, 2004.
38. Liu JJ, Shin JH, Hyrc KL, Liu S, Lei D, Holley MC, Bao J. Stem cell therapy for hearing loss: Math1 overexpression in VOT-E36 cells. Otol. Neurotol. 27(3):414-421, 2006a.
39. Liu XS, Zhang ZG, Zhang RL, Gregg S, Morris DC, Wang Y, Chopp M. Stroke induces gene profile changes associated with neurogenesis and angiogenesis in adult subventricular zone progenitor cells. J. Cereb. Blood Flow Metab. 27(3):564-574, 2006b.
40. Losordo DW, Dimmeler S. Therapeutic angiogenesis and vasculogenesis for ischemic disease. Part I: Angiogenic cytokines. Circulation 109(21):2487-2491, 2004.
41. Ma N, Stamm C, Kaminski A, Li W, Kleine HD, Muller-Hilke B, Zhang L, Ladilov Y, Egger D, Steinhoff G. Human cord blood cells induce angiogenesis following myocardial infarction in NOD/scid-mice. Cardiovasc. Res. 66(1):45-54, 2005, (Apr 1).
42. Matsui JI, Parker MA, Ryals BM, Cotanche DA. Regeneration and replacement in the vertebrate inner ear. Drug Discov. Today 10(19):1307-1312, 2005.
43. McDonald JW, Liu XZ, Qu Y, Liu S, Mickey SK, Turetsky D, Gottlieb DI, Choi DW. Transplanted embryonic stem cells survive, differentiate and promote recovery in injured rat spinal cord. Nat. Med. 5(12):1410-1412, 1999.
44. McLendon RE, Bigner DD. Immunohistochemistry of the glial fibrillary acidic protein: basic and applied considerations. Brain Pathol. 4(3):221-228, 1994.
45. Meyer JS, Katz ML, Maruniak JA, Kirk MD. Neural differentiation of mouse embryonic stem cells in vitro and after transplantation into eyes of mutant mice with rapid retinal degeneration. Brain Res. 1014(1-2):131-144, 2004.
46. Meyer JS, Katz ML, Kirk MD. Stem cells for retinal degenerative disorders. Ann. N. Y. Acad. Sci. 1049:135-145, 2005.
47. Miller JT, Bartley JH, Wimborne HJ, Walker AL, Hess DC, Hill WD, Carroll JE. The neuroblast and angioblast chemotaxic factor SDF-1 (CXCL12) expression is briefly up regulated by reactive astrocytes in brain following neonatal hypoxic-ischemic injury. BMC Neurosci. 6:63, 2005, Oct 31.
48. Mou K, Adamson CL, Davis RL. Time-dependence and cell-type specificity of synergistic neurotrophin actions on spiral ganglion neurons. J. Comp. Neurol. 402(1):129-139, 1998.
49. Muller M. The cochlear place-frequency map of the adult and developing Mongolian gerbil. Hear Res. 94(1-2):148-156, 1996.
50. Nakagawa T, Ito J. Application of cell therapy to inner ear diseases. Acta Otolaryngol. Suppl. 551:6-9, 2004.
51. Nam YJ, Stover T, Hartman SS, Altschuler RA. Upregulation of glial cell line- derived neurotrophic factor (GDNF) in the rat cochlea following noise. Hear Res. 146(1-2):1-6, 2000.
52. Nicholl AJ, Kneebone A, Davies D, Cacciabue-Rivolta DI, Rivolta MN, Coffey P, Holley MC. Differentiation of an auditory neuronal cell line suitable for cell transplantation. Eur. J. Neurosci. 22(2):343-353, 2005.
53. Okabe S, Forsberg-Nilsson K, Spiro AC, Segal M, McKay RD. Development of neuronal precursor cells and functional postmitotic neurons from embryonic stem cells in vitro. Mech. Dev. 59(1):89-102, 1996.
54. Okano Y, Iwai H. Effect of the high potassium medium on cultured cochlear epithelial cells. Arch. Otorhinolaryngol. 209(2):121-125, 1975.
55. Okano T, Nakagawa T, Endo T, Kim TS, Kita T, Tamura T, Matsumoto M, Ohno T, Sakamoto T, Iguchi F, Ito J. Engraftment of embryonic stem cell-derived neurons into the cochlear modiolus. Neuroreport 16(17):1919-1922, 2005.
56. Olivius P, Alexandrov L, Miller J, Ulfendahl M, Bagger-Sjoback D, Kozlova EN. Allografted fetal dorsal root ganglion neuronal survival in the guinea pig cochlea. Brain Res. 979(1-2):1-6, 2003, 25.
57. Oyesiku NM, Evans CO, Houston S, Darrell RS, Smith JS, Fulop ZL, Dixon CE, Stein DG. Regional changes in the expression of neurotrophic factors and their receptors following acute traumatic brain injury in the adult rat brain. Brain Res. 833(2):161-172, 1999, (Jul 3).
58. Palmer TD, Willhoite AR, Gage FH. Vascular niche for adult hippocampal neurogenesis. J. Comp. Neurol. 425(4):479-94, 2000, (Oct 2).
59. Parker MA, Cotanche DA. The potential use of stem cells for cochlear repair. Audiol. Neurootol. 9(2):72-80, 2004.
60. Pellicer M, Giraldez F, Pumarola F, Barquinero J. Stem cells for the treatment of hearing loss. Acta Otorrinolaringol. Esp. 56(6):227-232, 2005.
61. Rask-Andersen H, Bostrom M, Gerdin B, Kinnefors A, Nyberg G, Engstrand T, Miller JM, Lindholm D. 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(1-2):180-191, 2005.
62. Reed JC. Mechanisms of Bcl-2 family protein function and dysfunction in health and disease. Behring-Inst. Mitt. 97:72-100, 1996.
63. Regala C, Duan M, Zou J, Salminen M, Olivius P. Xenografted fetal dorsal root ganglion, embryonic stem cell and adult neural stem cell survival following implantation into the adult vestibulocochlear nerve. Exp. Neurol. 193(2):326-333, 2005.
64. Rio C, Dikkes P, Liberman MC, Corfas G. Glial fibrillary acidic protein expression and promoter activity in the inner ear of developing and adult mice. J. Comp. Neurol. 442(2):156-162, 2002.
65. Sakamoto T, Nakagawa T, Endo T, Kim TS, Iguchi F, Naito Y, Sasai Y, Ito J. Fates of mouse embryonic stem cells transplanted into the inner ears of adult mice and embryonic chickens. Acta Otolaryngol. Suppl. 551:48-52, 2004.
66. Schmiedt RA, Okamura H, Lang H, Schute BA. Ouabain application to the round window of the gerbil cochlea: A model of auditory neuropathy and apoptosis. J. Assoc. Res. Otolaryngol. 03:223-233, 2002.
67. Sekiya T, Kojima K, Matsumoto M, Kim TS, Tamura T, Ito J. Cell transplantation to the auditory nerve and cochlear duct. Exp. Neurol. 198(1):12-24, 2006.
68. Senut MC, Gulati-Leekha A, Goldman D. An element in the alpha1-tubulin promoter is necessary for retinal expression during optic nerve regeneration but not after eye injury in the adult zebrafish. J. Neurosci. 24(35):7663-7673, 2004.
69. Simonian PL, Grillot DA, Nunez G. Bcl-2 and Bcl-XL can differentially block chemotherapy-induced cell death. Blood 90(3):1208-1216, 1997.
70. Stowe AM, Plautz EJ, Eisner-Janowicz I, Frost SB, Barbay S, Zoubina EV, Dancause N, Taylor MD, Nudo RJ. VEGF protein associates to neurons in remote regions following cortical infarct. J. Cereb. Blood Flow Metab. 27(1):76-85, 2007.
71. Tamura T, Nakagawa T, Iguchi F, Tateya I, Endo T, Kim TS, Dong Y, Kita T, Kojima K, Naito Y, Omori K, Ito J. Transplantation of neural stem cells into the modiolus of mouse cochleae injured by cisplatin. Acta Otolaryngol. Suppl. 551:65-68, 2004.
72. Thomas-Mudge RJ, Okada-Ban M, Vandenbroucke F, Vincent-Salomon A, Girault JM, Thiery JP, Jouanneau J. Nuclear FGF-2 facilitates cell survival in vitro and during establishment of metastases. Oncogene 23(27):4771-4779, 2004.
73. Ward MM, Jobling AI, Puthussery T, Foster LE, Fletcher EL. Localization and expression of the glutamate transporter, excitatory amino acid transporter 4, within astrocytes of the rat retina. Cell Tissue Res. 315(3):305-310, 2004.
74. Watters K, Li H, Corrales C, Heller S. Cell fusion in Xenotransplantation of mouse stem cell-derivatives into chicken hosts. Hosts Assoc. Res. Otolaryngol. Abstr. 27:904, 2004.
75. Wei L, Cui L, Snider BJ, Rivkin M, Yu SS, Lee CS, Adams LD, Gottlieb DI, Johnson EM, Jr, Yu SP, Choi DW. Transplantation of embryonic stem cells overexpressing Bcl-2 promotes functional recovery after transient cerebral ischemia. Neurobiol. Dis. 19(1-2):183-193, 2005.
76. Weisleder N, Taffet GE, Capetanaki Y. Bcl-2 overexpression corrects mitochondrial defects and ameliorates inherited desmin null cardiomyopathy. Proc. Natl. Acad. Sci. U. S. A. 101(3):769-774, 2004.
77. Wise AK, Richardson R, Hardman J, Clark G, O'leary S. Resprouting and survival of guinea pig cochlear neurons in response to the administration of the neurotrophins brain-derived neurotrophic factor and neurotrophin-3. J. Comp. Neurol. 487(2):147-165, 2005.
78. Wurmser AE, Palmer TD, Gage FH. Neuroscience. Cellular interactions in the stem cell niche. Science 304(5675):1253-1255, 2004.
79. Yuge I, Takumi Y, Koyabu K, Hashimoto S, Takashima S, Fukuyama T, Nikaido T, Usami S. Transplanted human amniotic epithelial cells express connexin 26 and Na-K-adenosine triphosphatase in the inner ear. Transplantation 77(9):1452-1454, 2004.
80. Zanjani HS, Vogel MW, Delhaye-Bouchaud N, Martinou JC, Mariani J. Increased cerebellar Purkinje cell numbers in mice overexpressing a human bcl-2 transgene. J. Comp. Neurol. 374(3):332-341, 1996.
81. Zhai S, Shi L, Wang BE, Zheng G, Song W, Hu Y, Gao WQ. Isolation and culture of hair cell progenitors from postnatal rat cochleae. J. Neurobiol. 65(3):282-293, 2005.
82. Zhang ZG, Zhang L, Jiang Q, Chopp M. Bone marrow-derived endothelial progenitor cells participate in cerebral neovascularization after focal cerebral ischemia in the adult mouse. Circ. Res. 90(3):284-288, 2002.
83. Zou J, Pyykko I, Sutinen P, Toppila E. Vibration induced hearing loss in guinea pig cochlea: expression of TNF-alpha and VEGF. Hear. Res. 202(1-2):13-20, 2005.