View Item 

Show simple item record

Spiral ganglion cell degeneration‐induced deafness as a consequence of reduced GATA factor activity
dc.contributor.authorHoshino, Tomofumi
dc.contributor.authorTerunuma, Tsumoru
dc.contributor.authorTakai, Jun
dc.contributor.authorUemura, Satoshi
dc.contributor.authorNakamura, Yasuhiro
dc.contributor.authorHamada, Michito
dc.contributor.authorTakahashi, Satoru
dc.contributor.authorYamamoto, Masayuki
dc.contributor.authorEngel, James Douglas
dc.contributor.authorMoriguchi, Takashi
dc.date.accessioned2019-09-30T15:30:52Z
dc.date.availableWITHHELD_12_MONTHS
dc.date.available2019-09-30T15:30:52Z
dc.date.issued2019-08
dc.identifier.citationHoshino, Tomofumi; Terunuma, Tsumoru; Takai, Jun; Uemura, Satoshi; Nakamura, Yasuhiro; Hamada, Michito; Takahashi, Satoru; Yamamoto, Masayuki; Engel, James Douglas; Moriguchi, Takashi (2019). "Spiral ganglion cell degeneration‐induced deafness as a consequence of reduced GATA factor activity." Genes to Cells 24(8): 534-545.
dc.identifier.issn1356-9597
dc.identifier.issn1365-2443
dc.identifier.urihttps://hdl.handle.net/2027.42/151287
dc.description.abstractZinc‐finger transcription factors GATA2 and GATA3 are both expressed in the developing inner ear, although their overlapping versus distinct activities in adult definitive inner ear are not well understood. We show here that GATA2 and GATA3 are co‐expressed in cochlear spiral ganglion cells and redundantly function in the maintenance of spiral ganglion cells and auditory neural circuitry. Notably, Gata2 and Gata3 compound heterozygous mutant mice had a diminished number of spiral ganglion cells due to enhanced apoptosis, which resulted in progressive hearing loss. The decrease in spiral ganglion cellularity was associated with lowered expression of neurotrophin receptor TrkC that is an essential factor for spiral ganglion cell survival. We further show that Gata2 null mutants that additionally bear a Gata2 YAC (yeast artificial chromosome) that counteracts the lethal hematopoietic deficiency due to complete Gata2 loss nonetheless failed to complement the deficiency in neonatal spiral ganglion neurons. Furthermore, cochlea‐specific Gata2 deletion mice also had fewer spiral ganglion cells and resultant hearing impairment. These results show that GATA2 and GATA3 redundantly function to maintain spiral ganglion cells and hearing. We propose possible mechanisms underlying hearing loss in human GATA2‐ or GATA3‐related genetic disorders.Our results demonstrate that GATA2 and GATA3 redundantly function to maintain inner ear spiral ganglion cells and hearing. We propose possible mechanisms underlying hearing loss in human GATA2‐ or GATA3‐related genetic disorders.
dc.publisherWiley Periodicals, Inc.
dc.subject.otherinner ear
dc.subject.otherspiral ganglion
dc.subject.otheryeast artificial chromosome (YAC)
dc.subject.otherGata2
dc.titleSpiral ganglion cell degeneration‐induced deafness as a consequence of reduced GATA factor activity
dc.typeArticle
dc.rights.robotsIndexNoFollow
dc.subject.hlbsecondlevelGenetics
dc.subject.hlbtoplevelHealth Sciences
dc.description.peerreviewedPeer Reviewed
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/151287/1/gtc12705.pdf
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/151287/2/gtc12705_am.pdf
dc.identifier.doi10.1111/gtc.12705
dc.identifier.sourceGenes to Cells
dc.identifier.citedreferenceRubel, E. W., & Fritzsch, B. ( 2002 ). Auditory system development: Primary auditory neurons and their targets. Annual Review of Neuroscience, 25, 51 – 101. https://doi.org/10.1146/annurev.neuro.25.112701.142849
dc.identifier.citedreferenceLieuw, K. W., Li, G., Zhou, Y., Grosveld, F., & Engel, J. D. ( 1997 ). Temporal and spatial control of murine GATA‐3 transcription by promotor‐proximal regulatory elements. Developmental Biology, 188, 1 – 16.
dc.identifier.citedreferenceLillevali, K., Matilainen, T., Karis, A., & Salminen, M. ( 2004 ). Partially overlapping expression of Gata2 and Gata3 during inner ear development. Developmental Dynamics, 231, 775 – 781. https://doi.org/10.1002/dvdy.20185
dc.identifier.citedreferenceLim, K.‐C., Hosoya, T., Brandt, W., Ku, C.‐J., Hosoya‐Ohmura, S., Camper, S. A., … Engel, J. D. ( 2012 ). Conditional Gata2 inactivation results in HSC loss and lymphatic mispatterning. Journal of Clinical Investigation, 122, 3705 – 3717. https://doi.org/10.1172/JCI61619
dc.identifier.citedreferenceLim, K. C., Lakshmanan, G., Crawford, S. E., Gu, Y., Grosveld, F., & Engel, J. D. ( 2000 ). Gata3 loss leads to embryonic lethality due to noradrenaline deficiency of the sympathetic nervous system. Nature Genetics, 25, 209 – 212. https://doi.org/10.1038/76080
dc.identifier.citedreferenceMehl, A. L., & Thomson, V. ( 2002 ). The Colorado newborn hearing screening project, 1992–1999: On the threshold of effective population‐based universal newborn hearing screening. Pediatrics, 109, E7. https://doi.org/10.1542/peds.109.1.e7
dc.identifier.citedreferenceMinegishi, N., Suzuki, N., Yokomizo, T., Pan, X., Fujimoto, T., Takahashi, S., … Yamamoto, M. ( 2003 ). Expression and domain‐specific function of GATA2 during differentiation of the hematopoietic precursor cells in midgestation mouse embryos. Blood, 102, 896 – 905. https://doi.org/10.1182/blood-2002-12-3809
dc.identifier.citedreferenceMinichiello, L., & Klein, R. ( 1996 ). TrkB and TrkC neurotrophin receptors cooperate in promoting survival of hippocampal and cerebellar granule neurons. Genes & Development, 10, 2849 – 2858. https://doi.org/10.1101/gad.10.22.2849
dc.identifier.citedreferenceMoriguchi, T., Hoshino, T., Rao, A., Yu, L., Takai, J., Uemura, S., … Engel, J. D. ( 2018 ). A Gata3 3′ distal otic vesicle enhancer directs inner ear‐specific Gata3 expression. Molecular and Cellular Biology, 38, https://doi.org/10.1128/MCB.00302-18
dc.identifier.citedreferenceMoriguchi, T., Takako, N., Hamada, M., Maeda, A., Fujioka, Y., Kuroha, T., … Engel, J. D. ( 2006 ). Gata3 participates in a complex transcriptional feedback network to regulate sympathoadrenal differentiation. Development, 133, 3871 – 3881. https://doi.org/10.1242/dev.02553
dc.identifier.citedreferenceNardelli, J., Thiesson, D., Fujiwara, Y., Tsai, F. Y., & Orkin, S. H. ( 1999 ). Expression and genetic interaction of transcription factors GATA‐2 and GATA‐3 during development of the mouse central nervous system. Developmental Biology, 210, 305 – 321. https://doi.org/10.1006/dbio.1999.9278
dc.identifier.citedreferenceNozawa, D., Suzuki, N., Kobayashi‐Osaki, M., Pan, X., Engel, J. D., & Yamamoto, M. ( 2009 ). GATA2‐dependent and region‐specific regulation of Gata2 transcription in the mouse midbrain. Genes to Cells, 14, 569 – 582. https://doi.org/10.1111/j.1365-2443.2009.01289.x
dc.identifier.citedreferenceOstergaard, P., Simpson, M. A., Connell, F. C., Steward, C. G., Brice, G., Woollard, W. J., … Mansour, S. ( 2011 ). Mutations in GATA2 cause primary lymphedema associated with a predisposition to acute myeloid leukemia (Emberger syndrome). Nature Genetics, 2011 ( 43 ), 929 – 931. https://doi.org/10.1038/ng.923
dc.identifier.citedreferencePandolfi, P. P., Roth, M. E., Karis, A., Leonard, M. W., Dzierzak, E., Grosveld, F. G., … Lindenbaum, M. H. ( 1995 ). Targeted disruption of the GATA3 gene causes severe abnormalities in the nervous system and fetal liver haematopoiesis. Nature Genetics, 11, 40 – 44. https://doi.org/10.1038/ng0995-40
dc.identifier.citedreferencePata, I., Studer, M., van Doorninck, J. H., Briscoe, J., Kuuse, S., Engel, J. D., … Karis, A. ( 1999 ). The transcription factor GATA3 is a downstream effector of Hoxb1 specification in rhombomere 4. Development, 126, 5523 – 5531.
dc.identifier.citedreferenceBarald, K. F., & Kelley, M. W. ( 2004 ). From placode to polarization: New tunes in inner ear development. Development, 131, 4119 – 4130. https://doi.org/10.1242/dev.01339
dc.identifier.citedreferenceSchimmang, T., Tan, J., Müller, M., Zimmermann, U., Rohbock, K., Köpschall, I., … Knipper, M. ( 2003 ). Lack of Bdnf and TrkB signalling in the postnatal cochlea leads to a spatial reshaping of innervation along the tonotopic axis and hearing loss. Development, 130, 4741 – 4750. https://doi.org/10.1242/dev.00676
dc.identifier.citedreferenceShibata, S. B., Budenz, C. L., Bowling, S. A., Pfingst, B. E., & Raphael, Y. ( 2011 ). Nerve maintenance and regeneration in the damaged cochlea. Hearing Research, 281, 56 – 64. https://doi.org/10.1016/j.heares.2011.04.019
dc.identifier.citedreferenceSpinner, M. A., Sanchez, L. A., Hsu, A. P., Shaw, P. A., Zerbe, C. S., Calvo, K. R., … Holland, S. M. ( 2014 ). GATA2 deficiency: A protean disorder of hematopoiesis, lymphatics, and immunity. Blood, 123, 809 – 821. https://doi.org/10.1182/blood-2013-07-515528
dc.identifier.citedreferenceSuzuki, N., Ohneda, O., Minegishi, N., Nishikawa, M., Ohta, T., Takahashi, S., … Yamamoto, M. ( 2006 ). Combinatorial Gata2 and Sca1 expression defines hematopoietic stem cells in the bone marrow niche. Proceedings of the National Academy of Sciences of the United States of America, 103, 2202 – 2207. https://doi.org/10.1073/pnas.0508928103
dc.identifier.citedreferenceTsai, F.‐Y., Keller, G., Kuo, F. C., Weiss, M., Chen, J., Rosenblatt, M., … Orkin, S. H. ( 1994 ). An early haematopoietic defect in mice lacking the transcription factor GATA‐2. Nature, 371, 221 – 226. https://doi.org/10.1038/371221a0
dc.identifier.citedreferencevan der Wees, J., van Looij, M. A. J., de Ruiter, M. M., Elias, H., van der Burg, H., Liem, S.‐S., … van Doorninck, J. H. ( 2004 ). Hearing loss following Gata3 haploinsufficiency is caused by cochlear disorder. Neurobiology of Diseases, 16, 169 – 178. https://doi.org/10.1016/j.nbd.2004.02.004
dc.identifier.citedreferencevan Doornick, J. H., Van der Wees, J., Karis, A., Goedknegt, E., Engel, J. D., & Coesmans, M., … DeZeeuw, C. I. ( 1999 ). Gata3 is involved in the development of serotonergic neurons in the caudal raphe nuclei. Journal of Neuroscience, 19 ( RC12 ), 1 – 8.
dc.identifier.citedreferenceVan Esch, H., Groenen, P., Nesbit, M. A., Schuffenhauer, S., Lichtner, P., Vanderlinden, G., … Devriendt, K. ( 2000 ). GATA3 haplo‐insufficiency causes human HDR syndrome. Nature, 406, 419 – 422. https://doi.org/10.1038/35019088
dc.identifier.citedreferenceWang, J., & Puel, J. L. ( 2018 ). Toward cochlear therapies. Physiological Reviews, 98, 2477 – 2522. https://doi.org/10.1152/physrev.00053.2017
dc.identifier.citedreferenceWhitfield, T. T. ( 2015 ). Development of the inner ear. Current Opinion in Genetics & Development, 32, 112 – 118. https://doi.org/10.1016/j.gde.2015.02.006
dc.identifier.citedreferenceYamamoto, M., Ko, L. J., Leonard, M. W., Beug, H., Orkin, S. H., & Engel, J. D. ( 1990 ). Activity and tissue‐specific expression of the transcription factor NF‐E1 [GATA] multigene family. Genes & Dev, 4, 1650 – 1662.
dc.identifier.citedreferenceZhou, Y., Lim, K. C., Onodera, K., Takahashi, S., Ohta, J., Minegishi, N., … Engel, J. D. ( 1998 ). Rescue of the embryonic lethal hematopoietic defect reveals a critical role for GATA2 in urogenital development. EMBO Journal, 17, 6689 – 6700. https://doi.org/10.1093/emboj/17.22.6689
dc.identifier.citedreferenceZhou, Y., Yamamoto, M., & Engel, J. D. ( 2000 ). GATA2 is required for the generation of V2 interneurons. Development, 127, 3829 – 3838.
dc.identifier.citedreferenceAinoya, K., Moriguchi, T., Ohmori, S., Souma, T., Takai, J., Morita, M., … Yamamoto, M. ( 2012 ). UG4 enhancer‐driven GATA‐2 and bone morphogenetic protein 4 complementation remedies the CAKUT phenotype in Gata2 hypomorphic mutant mice. Molecular and Cellular Biology, 32, 2312 – 2322. https://doi.org/10.1128/MCB.06699-11
dc.identifier.citedreferenceCraven, S. E., Lim, K. C., Ye, W., Engel, J. D., de Sauvage, F., & Rosenthal, A. ( 2004 ). Gata2 specifies serotonergic neurons downstream of sonic hedgehog. Development, 131, 1165 – 1173. https://doi.org/10.1242/dev.01024
dc.identifier.citedreferenceDuncan, J. S., Lim, K. C., Engel, J. D., & Fritzsch, B. ( 2011 ). Limited inner ear morphogenesis and neurosensory development are possible in the absence of GATA3. International Journal of Developmental Biology, 55, 297 – 303. https://doi.org/10.1387/ijdb.103178jd
dc.identifier.citedreferenceFritzsch, B., Silos Santiago, I., Bianchi, L. M., & Farinas, I. ( 1997 ). The role of neurotrophic factors in regulating the development of inner ear innervation. Trends in Neurosciences, 20, 159 – 164. https://doi.org/10.1016/S0166-2236(96)01007-7
dc.identifier.citedreferenceFritzsch, B., Tessarollo, L., Coppola, E., & Reichardt, L. F. ( 2004 ). Neurotrophins in the ear: Their roles in sensory neuron survival and fiber guidance. Progress in Brain Research, 146, 265 – 278. https://doi.org/10.1016/S0079-6123(03)46017-2
dc.identifier.citedreferenceGeorge, K. M., Leonard, M. W., Roth, M. W., Liew, K. W., Kioussis, D., Grosveld, F., & Engel, J. D. ( 1994 ). Embryonic expression and cloning of the murine GATA‐3 gene. Development, 120, 2673 – 2686.
dc.identifier.citedreferenceHaugas, M., Lillevli, K., Hakanen, J., & Salminen, M. ( 2010 ). Gata2 is required for the development of inner ear semicircular ducts and the surrounding perilymphatic space. Developmental Dynamics, S239, 2452 – 2469. https://doi.org/10.1002/dvdy.22373
dc.identifier.citedreferenceHebert, J. M., & McConnell, S. K. ( 2000 ). Targeting of cre to the Foxg1 (BF‐1) locus mediates loxP recombination in the telencephalon and other developing head structures. Developmental Biology, 222, 296 – 306. https://doi.org/10.1006/dbio.2000.9732
dc.identifier.citedreferenceHendriks, R. W., Nawijn, M. C., Engel, J. D., van Doorninck, H., Grosveld, F., & Karis, A. ( 1999 ). Expression of the transcription factor GATA3 is required for the development of the earliest T cell progenitors and correlates with stages of cellular proliferation in the thymus. European Journal of Immunology, 29, 1912 – 1918. https://doi.org/10.1002/(SICI)1521-4141(199906)29:06<1912:AID-IMMU1912>3.0.CO;2-D
dc.identifier.citedreferenceHoshino, T., Shimizu, R., Ohmori, S., Nagano, M., Pan, X., Ohneda, O., … Engel, J. D. ( 2008 ). Reduced BMP4 abundance in Gata2 hypomorphic mutant mice result in uropathies resembling human CAKUT. Genes to Cells, 13, 159 – 170. https://doi.org/10.1111/j.1365-2443.2007.01158.x
dc.identifier.citedreferenceHoshino, T., Tabuchi, K., Nishimura, B., Tanaka, S., Nakayama, M., Ishii, T., … Hara, A. ( 2011 ). Protective role of Nrf2 in age‐related hearing loss and gentamicin ototoxicity. Biochemical and Biophysical Research Communications, 415, 94 – 98. https://doi.org/10.1016/j.bbrc.2011.10.019
dc.identifier.citedreferenceKaris, A., Pata, I., van Doorninck, J. H., Grosveld, F., de Zeeuw, C. I., de Caprona, D., & Fritzsch, B. ( 2001 ). Transcription factor GATA3 alters pathway selection of olivocochlear neurons and affects morphogenesis of the ear. The Journal of Comparative Neurology, 429, 615 – 630. https://doi.org/10.1002/1096-9861(20010122)429:4<615:AID-CNE8>3.0.CO;2-F
dc.identifier.citedreferenceKazenwadel, J., Secker, G. A., Liu, Y. J., Rosenfeld, J. A., Wildin, R. S., Cuellar‐Rodriguez, J., … Harvey, N. L. ( 2012 ). Loss‐of‐function Germline GATA2 mutations in patients with MDS/AML or MonoMAC syndrome and primary lymphedema reveal a key role for GATA2 in the lymphatic vasculature. Blood, 119, 1283 – 1291. https://doi.org/10.1182/blood-2011-08-374363
dc.identifier.citedreferenceKhandekar, M., Brandt, W., Zhou, Y., Dagenais, S., Glover, T. W., Suzuki, N., … Engel, J. D. ( 2007 ). A Gata2 intronic enhancer confers its pan‐endothelia‐specific regulation. Development, 134, 1703 – 1712. https://doi.org/10.1242/dev.001297
dc.identifier.citedreferenceKhandekar, M., Suzuki, N., Lewton, J., Yamamoto, M., & Engel, J. D. ( 2004 ). Multiple, distant Gata2 enhancers specify temporally and tissue‐specific patterning in the developing urogenital system. Molecular and Cellular Biology, 24, 10263 – 10276. https://doi.org/10.1128/MCB.24.23.10263-10276.2004
dc.identifier.citedreferenceKim, W. Y., Fritzsch, B., Serls, A., Bakel, L. A., Huang, E. J., Reichardt, L. F., … Lee, J. E. ( 2001 ). NeuroD‐null mice are deaf due to a severe loss of the inner ear sensory neurons during development. Development, 128, 417 – 426.
dc.identifier.citedreferenceKo, L. J., & Engel, J. D. ( 1993 ). DNA‐binding specificities of the GATA transcription factor family. Molecular and Cellular Biology, 13, 4011 – 4022. https://doi.org/10.1128/MCB.13.7.4011
dc.identifier.citedreferenceLakshmanan, G., Lieuw, K. H., Grosveld, F., & Engel, J. D. ( 1998 ). Partial rescue of GATA‐3 by yeast artificial chromosome transgene. Developmental Biology, 204, 451 – 463. https://doi.org/10.1006/dbio.1998.8991
dc.identifier.citedreferenceLakshmanan, G., Lieuw, K. H., Lim, K. C., Gu, Y., Grosveld, F., Engel, J. D., & Karis, A. ( 1999 ). Localization of distant urogenital system‐, central nervous system‐ and endocardium‐specific transcriptional regulatory elements in the GATA‐3 locus. Molecular and Cellular Biology, 19, 1558 – 1568. https://doi.org/10.1128/MCB.19.2.1558
dc.identifier.citedreferenceLawoko‐Kerali, G., Rivolta, M. N., & Holley, M. ( 2002 ). Expression of the transcription factors GATA3 and Pax2 during development of the mammalian inner ear. The Journal of Comparative Neurology, 442, 378 – 391. https://doi.org/10.1002/cne.10088
dc.owningcollnameInterdisciplinary and Peer-Reviewed


Files in this item

Name:
gtc12705.pdf
Size:
1.183MB
Format:
PDF
View/Open
Name:
gtc12705_am.pdf
Size:
834.6KB
Format:
PDF
View/Open

Show simple item record

Remediation of Harmful Language

The University of Michigan Library aims to describe library materials in a way that respects the people and communities who create, use, and are represented in our collections. Report harmful or offensive language in catalog records, finding aids, or elsewhere in our collections anonymously through our metadata feedback form. More information at Remediation of Harmful Language.

Accessibility

If you are unable to use this file in its current format, please select the Contact Us link and we can modify it to make it more accessible to you.