Groves Lab Publications

Matern, M.S., Durruthy-Durruthy, R., Birol, O., Darmanis, S., Scheibinger, M., Groves, A.K. and Heller, S. (2023). Transcriptional dynamics of delaminating neuroblasts in the mouse otic vesicle. Cell Reports, in press

Mao, K., Borel, C., Ansar, M., Jolly, A., Makrythanasis, P., Froehlich, C., Iwaszkiewicz, J., Wang, B., Xu, X., Blanc, X., Cai, J., Chen, Q., Ankamreddy, H., Singh, S., Zhang, H., Wang, X., Zhao, S., Ranza, E., Paracha, S.A., Syed, F.S., Guida, V., Piceci-Sparascio, F., Melis, D., Dallapiccola, B., Digilio, M.C., Novelli, A, Magliozzi, M, Fadda, M.T., Streff, H., Machol, K., Lewis, R.A., Zoete, V., Squelo, G.M., Prontera, P., Mancano, G., Gori, G., Mariani, M., Selicorni, A., Psoni, S., Fryssira, H., Cox, T.C., Douzgou, S., Marlin, S., Biskup, S., DeLuca, A., Merla, G., Groves, A.K., Lupski, J.R., Zhang, Q., Zhang, Y.-B., and Antonarakis, S.E. (2023). FOXI3 pathogenic variants cause one form of craniofacial microsomia. Nature Communications, 14:2026

McGovern, M.M., Hartman, B.H., Thawani, A., Maunsell, H.R., Zhang, H., Yousaf, R., Heller, S., Stone, J.S. and Groves, A.K. (2022). Fbxo2CreERT2 is expressed in the cochlear duct and vestibular organs in the mouse inner ear. Hearing Research, DOI: 10.1016/j.heares.2022.108686.

Iyer, A., Hosamani, I., Nguyen, J.D., Cai, T., Singh, S., McGovern, M.M., Beyer, L.A., Zhang, H., Jen, H.-I, Yousaf, R., Birol, O., Sun, J., Ray, R.S., Raphael, Y., Segil, N. and Groves, A.K. (2022). Cellular reprogramming with ATOH1, GFI1, and POU4F3 implicate epigenetic changes and cell-cell signaling as obstacles to hair cell regeneration in mature mammals. eLife, 11:e79712. doi. org/ 10. 7554/ eLife. 79712..

Ghosh, R., Bosticardo, M., Singh, S., Similuk, M., Delmonte, O.M., Pala, F., Peng, C., Jodarski, C., Keller, M.D., Chinn, I., Groves, A.K., Notarangelo, L.D., Walkiewicz, M. A., Chinen, J. and Bundy, V. (2022). FOXI3 haploinsufficiency contributes to low T cell receptor excision circles and T cell lymphopenia.  J. Allergy Clin. Immunol., 150(6), 1556-1562.

Tang, P.-C., Chen, L., Singh, S., Groves, A.K., Koehler, K.R., Liu, X.Z., and Nelson, R. (2022). Wnt signaling promotes cell caudalization  in mouse stem cell-derived organoids. Stem Cells, DOI: 10.1093/stmcls/sxac071

Jen, H.-I, Singh, S., Tao, L., Yu, H., Segil, N. and Groves, A.K. (2022). GFI1 regulates hair cell differentiation by acting as an off-DNA transcriptional co-activator of ATOH1, and a DNA-binding repressor. Scientific Reports, 12, 7793.

Li, H., Janssens, J., De Waegeneer, M., Kolluru, S.S., [….] FCA Consortium, Jasper, H., Oliver, B., Perrimon, N., Deplancke, B., Quake, S.R., Luo, L., and Aerts, S. (2022). Fly Cell Atlas: a single-cell transcriptomic atlas of the adult fruit fly.  Science, 375(6584):eabk2432..

Akdemir, E, Woo, J., Bosquez Huerta, N.A., Lozzi, B., Groves, A.K., Harmanci, A., and Deneen, B. (2021). Lunatic Fringe-GFP marks lamina-specific astrocytes that regulate sensory processing. J. Neuoroscience, 42(4), 567-580

Huang, T.-W., Iyer, A.I, Manalo, J.M., Woo, J., Bosquez Huerta, N.A., McGovern, M.M., Schrewe, H., Pereira, F.A., Groves, A.K., Ohlemiller, K.K. and Deneen, B. (2021). Glial-Specific Deletion of Med12 Results in Rapid Hearing Loss via Degradation of the Stria Vascularis. J. Neuroscience 41(34), 7171-7181.

Tao, L., Yu, H., Llamas, J., Trecek, T., Wang, X., Stojanova, Z., Groves, A.K. and Segil, N. (2021). Enhancer decommissioning imposes an epigenetic barrier to sensory hair cell regeneration. Developmental Cell, 56, 2471-2485.

Lee, S., Song, J.-J., Beyer, L.A., Swiderski, D.L., Prieskorn, D.M., Acar, M., Jen, H.-I, Groves, A.K. and Raphael, Y. (2020). Combinatorial Atoh1 and Gfi1 induction enhances hair cell regeneration in the adult cochlea. Scientific Reports, 10(1):21397.

Gnedeva, K., Wang, X., McGovern, M.M., Barton, M., Tao, L., Trecek, T., Monroe, T.O., Llamas, J., Makmura, W., Martin, J.F., Groves, A.K., Warchol, M., and Segil, N. (2020). Organ of Corti size is governed by Yap/Tead-mediated progenitor self-renewal. PNAS 117, 13552-13561.

Brown, R.M., Nelson, J.C., Zhang, H., Kiernan, A.E., and Groves, A.K. (2020). Notch-mediated lateral induction is necessary to maintain vestibular prosensory identity during inner ear development. Developmental Biology 462(1), 74-84.

Bernstock, J.D., Totten, A.H., Elkahloun, A.G., Johnson, K.R., Hurst, A.C., Goldman, F., Groves, A.K., Fady, M.M. and Atkinson, T.P. (2020). Recurrent microdeletions at chromosome 2p11.2 are associated with thymic hypoplasia and features resembling DiGeorge Syndrome. J. Allergy Clin. Immunol. 145(1), 358-367.

Jen, H.-I, Hill, M.C., Tao, L., Sheng, K., Cao, W., Zhang, H., Yu, H.V., Llamas, J., Zong, C., Martin, J.F., Segil, N. and Groves, A.K. (2019). Transcriptomic and epigenetic regulation of hair cell regeneration in the mouse utricle and its potentiation by Atoh1 . eLife, e44328. doi: 10.7554/eLife.44328.

Singh, S., Jangid, R.K., Crowder, A. and Groves, A.K. (2018). Foxi3 transcription factor activity is mediated by a C-terminal transactivation domain and regulated by the Protein Phosphatase 2A (PP2A) complex. Scientific Reports, 8(1), 17249.

Xie, W., Jen, H.-I, Seymour, M., Yeh, S.-Y., Pereira, F., Groves, A.K., Klisch, T., and Zoghbi, H.Y. (2017). An Atoh1-S193A phospho-mutant allele causes hearing deficits and motor impairment. J. Neuroscience 37, 8583-8594.

Semerci, F., Choi, W. T.-S, Bajic, A., Thakkar, A., Encinas, J.M., Depreux, F., Segil, N., Groves, A.K. and Maletic-Savatic, M. (2017). Lunatic fringe-mediated Notch signaling regulates adult hippocampal neural stem cell maintenance. eLIfe, 10.7554/eLife.24660.

Basch, M.L., Brown, R.M., Jen, H.-I, Semerci, F., Depreux, F., Edlund, R.K., Zhang, H., Norton, C.R., Gridley, T., Cole, S.E., Doetzlhofer, A., Maletic-Savatic, M., Segil, N. and Groves, A.K. (2016). Fine-tuning of Notch signaling sets the boundary of the organ of Corti and establishes sensory cell fates. eLife, 10.7554/eLife.19921

Maass, J.C., Gu, R., Cai, T., Wan, Y.-W., Cantellano, S.C., Asprer, J.S.T., Zhang, H., Jen, H.-I, Edlund, R.K., Liu, Z. and Groves, A.K. (2016). Transcriptomic analysis of mouse cochlear supporting cell maturation reveals large-scale changes in Notch responsiveness prior to the onset of hearing. PLoS One 11(12): e0167286 RNA-seq files can be downloaded from GEO here

Li, T., Giagtzoglou, N., Eberl, D.F., Jaiswal, S.N., Jaiswal, M., Cai., T., Godt, D., Groves, A.K. and Bellen, H.J. (2016). The E3 ligase Ubr3 regulates Usher syndrome and MYH9-related disorder proteins in the auditory organs of Drosophila and mammals. eLife, 10.7554/eLife.15258.

Li, T., Fan, J., Blanco-Sanchez, B., Giagtzoglou, N., Lin, G., Yamamoto, S., Jaiswal, M., Chen, K., Zhang, J., Wei, W., Lewis, M., Groves, A.K. , Westerfield, M., Jia, J., and Bellen, H.J. (2016). Ubr3, a novel modulator of Hh signaling affects the degradation of Costal-2 and Kif7 through poly-ubiquitination. PLoS Genetics, 12(5): e1006054.

Gu, R., Brown, R.M., Hsu, C.-W., Crowder, A., Piazza, V.G., Vadakkan, T.J., Cai, T., Dickinson, M.E. and Groves, A.K. (2016). Lineage tracing of Sox2-expressing progenitor cells in the mouse inner ear reveals a broad contribution to non-sensory tissues and insights into the origin of the organ of Corti. Developmental Biology, 414, 72-84.

Shirokova, V., Jussila, M., Biggs, L.C., Ohyama, T., Groves, A.K. and Mikkola, M.L. (2016). Foxi3 deficiency compromises hair follicle stem cell specification and activation. Stem Cells 10.1002/stem.2363

Birol, O., Ohyama, T., Edlund, R.K., Drakou, K., Georgiades, P., and Groves, A.K. (2015). The mouse Foxi3 transcription factor is necessary for the development of posterior placodes. Developmental Biology 409, 139-151.

Jussila, M., Aalto, A., Sanz Navarro, M., Shirokova, V., Kallonen, A., Ohyama, T., Groves, A.K., Mikkola, M.L. and Thesleff, I. (2015). Suppression of epithelial differentiation by Foxi3 is essential for molar crown patterning. Development 142, 3954-3963.

Maass, J.C., Gu, R., Basch, M.L., Waldhaus, J., Martin-Lopez, E., Xia, A., Oghalai, J.S., Heller, S. and Groves, A.K. (2015). Changes in the regulation of the Notch signaling pathway are temporally correlated with regenerative failure in the mouse cochlea. Frontiers in Cellular Neuroscience 9, 110.

Kantarci, H., Edlund, R.K., Groves, A.K. and Riley, B.B. (2015). Tfap2a promotes specification and maturation of neurons in the inner ear through modulation of BMP, FGF and Notch signaling. PLoS Genetics, 11(3): e1005037

Cai, T., Jen, H.-I, Kang, H., Klisch, T.J., Zoghbi, H.Y and Groves, A.K. (2015). Characterization of the transcriptome of nascent hair cells and identification of direct targets of the Atoh1 transcription factor. Journal of Neuroscience 35, 5640-5654 (Supplementary data for Cai et al. (2015) can be downloaded here. Table 1, Table 2, Table 3, Table 4, Table 5, Table 6, Table 7, Table Legends. RNA-seq files can be downloaded from GEO here)

Tassano, E., Jagannathan, V., Drögemüller, C., Leoni, M., Hytönen, M., Severino, M., Gimelli, S., Cuoco, C., Di Rocco, M., Sanio, K., Groves, A.K., Leeb, T and Gimelli, G. (2015). Congenital aural atresia associated with agenesis of internal carotid artery in a girl with a FOXI3 deletion. Am. J. Med Genetics 167A, 537-544.

Gao, S.S., Wang, R., Raphael, P.D., Moayedi, Y., Groves, A.K., Zuo, J., Applegate, B.E. and Oghalai, J.S. (2014). Sharp frequency tuning within the mammalian cochlea does not require active processes. J. Neurophysiology 112, 1192-1204.

Khatri, S.B., Edlund, R.K. and Groves, A.K. (2014) Foxi3 is necessary for the induction of the chick otic placode in response to FGF signaling. Developmental Biology 391, 158-169.

Edlund, R.K., Ohyama, T., Kantarci, H., Riley, B.B. and Groves, A.K. (2014). Foxi transcription factors promote pharyngeal arch development by regulating the formation of FGF signaling centers. Developmental Biology 390, 1-13.

Moayedi, Y., Basch, M.L., Pacheco, N., Gao, S.G., Harrison, W., Xioa, N, Oghalai, J.S., Overbeek, P.A., Mardon G., and Groves A.K. (2014). The splicing factor Sfswap regulates growth and patterning of inner ear sensory organs. PLoS Genetics 10(1): e1004055

Xia A., Song, Y., Wang, R., Gao, S., Clifton, W., Raphael, P., Cho, S.-I., Pereira, F., Groves, A.K. and Oghalai, J.S. (2013). Prestin regulation and function in residual outer hair cels after noise-induced hearing loss. PLoS One 8, e82602

Cai, T, Seymour, M.L., Zhang, H., Pereira, F. A. and Groves, A.K. (2013). Conditional deletion of Atoh1 reveals distinct critical periods for survival and function of hair cells in the organ of Corti. J. Neuroscience 33, 10110-10122.

Yang, L., O’Neill, P., Martin, K., Maass, J.C., Vassilev, V., Ladher, R. and Groves, A.K. (2013). Analysis of FGF-dependent and FGF-independent pathways in otic placode induction. PLoS One 8, e55011.

Khatri, S.B. and Groves, A.K. (2013). Expression of Foxi2 and Foxi3 transcription factors during development of chicken sensory placodes and pharyngeal arches. Gene Expression Patterns 13, 38-42.

White, P.M., Stone, J.S., Groves, A.K. and Segil, N. (2012). EGFR signaling is required for regenerative proliferation in the cochlea: Conservation in birds and mammals. Developmental Biology 363, 191-200.

Basch, M.L., Ohyama, T., Segil, N. and Groves, A.K. (2011). Canonical Notch signaling is not necessary for prosensory induction in the mouse cochlea: Insights from a conditional mutant of RBPjk. Journal of Neuroscience 31, 8046-58.

Reginesi, A., Clarkson, M., Neirjnck, Y., Lu, B., Ohyama, T., Groves, A.K., Sock, E., Wegner, M., Costantini, F., Charboissier, M.C. and Schedl, A (2011). Sox9 controls epithelial branching by activating RET effector genes during kidney development. Human Molecular Genetics 20, 1143-53.

Ohyama, T., Basch, M.L., Mishina, Y., Lyons, K., Segil, N., and Groves, A.K. (2010). BMP signaling is necessary for patterning the sensory and non-sensory regions of the developing mammalian cochlea. Journal of Neuroscience 30, 15044-51.

Doetzlhofer, A., Basch, M.L., Ohyama, T., Gessler, M., Groves, A.K. and Segil, N. (2009). Hey2 regulation by FGF provides a Notch-independent mechanism for maintaining pillar cell fate in the organ of Corti.Developmental Cell 16, 58-69.

Jayasena, C.S., Ohyama, T., Segil, N. and Groves, A.K. (2008). Notch signaling augments the canonical Wnt pathway to specify the size of the otic placode. Development 135, 2251-61.

Raft, S., Koundakjian, E.J., Quinones, H., Jayasena, C.S., Goodrich, L.V., Johnson, J.E., Segil, N. and Groves, A.K. (2007). Cross-regulation of Ngn1 and Math1 coordinates the production of neurons and sensory hair cells during inner ear development. Development 134, 4405-15.

Doetzlhofer, A., White, P.M., Lee, Y.-S., Groves, A.K. and Segil, N. (2006). Prospective identification and purification of hair cell and supporting cell progenitors from the embryonic cochlea. Brain Research 1091, 282-8.

White, P.M., Doetzlhofer, A., Lee, Y.-S., Groves, A.K. and Segil, N. (2006). Cochlear supporting cells retain the ability to divide and transdifferentiate into sensory hair cells. Nature 441, 984-987.

Arnold, J.S., Braunstein, E.M., Ohyama, T., Groves, A.K., Adams, J.C., Brown, M.C. and Morrow, B.E. (2006). Tissue specific roles of Tbx1 in the development of the outer, middle and inner ear, defective in 22q11DS patients. Human Molecular Genetics 15, 1629-39.

Ohyama, T., Mohamed, O.A., Taketo, M.M., Dufort, D. and Groves, A.K. (2006). Wnt signals mediate a fate decision between otic placode and epidermis. Development 133, 865-875.

Martin, K. and Groves, A.K. (2006). Competence of cranial ectoderm to respond to FGF signaling suggests a two step model of otic placode induction. Development 133, 877-887.

Kil, S.-H., Streit, A., Brown, S.T., Agrawal, N., Collazo, A., Zile, M.H. and Groves, A.K. (2005). Distinct roles for hindbrain and paraxial mesoderm in the induction and patterning of the inner ear revealed by a study of vitamin A-deficient quail. Developmental Biology 285, 252-271.

Brown, S.P., Wang, J. and Groves, A.K. (2005). Dlx gene expression during chick inner ear development.Journal of Comparative Neurology 483, 48-65.

Doetzlhofer, A., White, P.M., Johnson, J.E., Segil, N. and Groves, A.K. (2004). In vitro growth and differentiation of mammalian sensory hair cell progenitors: A requirement for EGF and periotic mesenchyme.Developmental Biology 272, 432-447.

Ohyama, T., and Groves, A.K. (2004a). Generation of Pax2-Cre mice by modification of a Pax2 bacterial artificial chromosome. Genesis 38 195-199.

Ohyama, T. and Groves, A.K. (2004b). Expression of mouse Foxi class genes in early craniofacial development. Developmental Dynamics, 231 640–646.

Lumpkin, E.A., Collisson, T., Parab, P., Omer-Abdalla, A., Haeberle, H., Chen, P., Doetzlhofer, A., White, P., Groves, A., Segil, N., and Johnson, J.E. (2003). Math1-driven GFP expression in the developing nervous system of transgenic mice. Gene Expression Patterns 3, 389-95.

Groves, A.K. and Bronner-Fraser, M. (2000). Competence, specification and commitment in otic placode induction. Development 127, 3489-3499.

McGovern, M.M. and Groves, A.K. (2023). Specification and Plasticity of Cochlear Hair Cell Progenitors. In “Hair Cell Regeneration” (Springer Handbook of Auditory Research, vol. 75) J.S. Stone, M.A. Warchol, A. N. Popper, R.R. Fay, eds. (New York, Springer Verlag).

Iyer, A.A. and Groves, A.K. (2021). Transcription factor reprogramming in the inner ear: Turning on cell fate switches to regenerate sensory hair cells. Frontiers in Cellular Neuroscience, 15:660748. doi: 10.3389/fncel.2021.660748

Thawani, A. and Groves, A.K. (2020). Building the Border: Development of the Chordate Neural Plate Border Region and its Derivatives. Frontiers in Physiology 11, 608880. doi: 10.3389/fphys.2020.608880.

Ankamreddy, H., Bok, J. and Groves, A.K. (2020). Uncovering the secreted signals and transcription factors regulating the development of mammalian middle ear ossicles. Developmental Dynamics, 249, 1410-1424.

Brown, R.M. and Groves, A.K. (2020). Hear, hear for Notch: Control of cell fates in the inner ear by Notch signaling. Biomolecules 10(3): 370.doi: 10.3390/biom10030370.

Li, T., Bellen, H.J. and Groves, A.K. (2018). Using Drosophila to study mechanisms of hereditary hearing loss. Disease Models and Mechanisms, 11(6). pii: dmm031492. doi: 10.1242/dmm.031492.

Groves, A.K. and Fekete, D.M. (2017). New Directions in Cochlear Development. In “Understanding the Cochlea” (Springer Handbook of Auditory Research, vol. 62) G. A. Manley, A.W. Gummer, A. N. Popper, R.R. Fay, eds. (New York, Springer Verlag).

Singh, S., and Groves, A.K. (2016). The molecular basis of craniofacial placode development. WIREs Developmental Biology, 5(3), 363-376.

Basch, M.L., Brown, R.M., Jen, H.-I and Groves, A.K. (2016). Where hearing starts: The development of the mammalian cochlea. J. Anatomy, 228, 233-254.

Edlund, R.K., Birol, O. and Groves, A.K. (2015). The role of Foxi family transcription factors in the development of the ear and jaw. Current Topics in Developmental Biology 111, 461-495.

Raft, S. and Groves, A.K. (2015). Segregating neural and mechanosensory fates at the developing ear: patterning, signaling, and transcriptional control. Cell and Tissue Research 359, 315-332.

Cai, T. and Groves, A.K. (2015). The role of Atonal factors in mechanosensory cell specification and function. Cellular Neurobiology, in press.

Gridley, T. and Groves, A.K. (2014). Overview of genetic tools and techniques to study Notch signaling in mice. Methods in Molecular Biology 1187, 47-61.

Groves, A.K., and LaBonne, C. (2014): Setting appropriate boundaries: Fate, patterning and competence at the neural plate border. Developmental Biology, 389, 2-12.

Groves, A.K., Zhang, K.D., and Fekete, D.M. (2013). The genetics of hair cell development and regeneration. Ann. Rev. Neuroscience, 36, 361-381.

Jarman, A.P. and Groves, A.K. (2013). The role of atonal transcription factors in the development of mechanosensitive cells. Seminars in Cell and Developmental Biology, 24, 438-447

Groves, A.K. and Fekete, D.M. (2012). Shaping sound in space: The regulation of inner ear patterning.Development 139, 245-257.

Groves, A.K. (2010). The challenge of hair cell regeneration. Experimental Biology and Medicine, 235, 434-446.

Ohyama, T., Groves, A.K., and Martin, K. (2007). The first steps towards hearing: Mechanisms of otic placode induction. International Journal of Developmental Biology 51, 463-72.

Groves, A. K. (2005). The induction of the otic placode. In “Development of the Inner Ear” (Springer Handbook of Auditory Research, vol. 26) A. N. Popper, M. W. Kelley, and D. K. Wu, eds. (New York, Springer Verlag).

Brown, S.P., Martin K., and Groves, A.K. (2003). Molecular basis of inner ear induction. Curr. Topics Dev. Biol 57,115-49.