Embryonic frog epidermis: a model for the study of cell-cell interactions in the development of mucociliary disease
Open accessAbstract
SUMMARY: Specialised epithelia such as mucociliary, secretory and transporting epithelia line all major organs, including the lung, gut and kidney. Malfunction of these epithelia is associated with many human diseases. The frog embryonic epidermis possesses mucus-secreting and multiciliated cells, and has served as an excellent model system for the biogenesis of cilia. However, ionic regulation is important for the function of all specialised epithelia and it is not clear how this is achieved in the embryonic frog epidermis. Here, we show that a third cell type develops alongside ciliated and mucus-secreting cells in the tadpole skin. These cells express high levels of ion channels and transporters; therefore, we suggest that they are analogous to ionocytes found in transporting epithelia such as the mammalian kidney. We show that frog ionocytes express the transcription factor foxi1e, which is required for the development of these cells. Depletion of ionocytes by foxi1e knockdown has detrimental effects on the development of multiciliated cells, which show fewer and aberrantly beating cilia. These results reveal a newly identified role for ionocytes and suggest that the frog embryonic skin is a model system that is particularly suited to studying the interactions of different cell types in mucociliary, as well as in secretory and transporting, epithelia.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
foxi specifies osmoregulatory ionocytes, a characteristic cell type of vertebrate mucociliary epithelia.
“Another member of the Fox family, foxi, specifies the osmoregulatory ionocytes, another characteristic cell type of vertebrate mucociliary epithelia [116];”
From Gastric pouches and the mucociliary sole: setting the stage for nervous system evolution (2015) · cites this paper as [116]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Appendix G: In Situ Hybridization: An Improved Whole-Mount Method for Xenopus Embryos
Harland, R. M. (1991) · Methods in cell biology · doi:10.1016/s0091-679x(08)60307-6 · Cited by 2,048 · see citing works
Mucus clearance as a primary innate defense mechanism for mammalian airways
Knowles, M. R., & Boucher, R. C. (2002) · Journal of Clinical Investigation · doi:10.1172/jci15217 · Cited by 1,082 · see citing works
Mucus clearance as a primary innate defense mechanism for mammalian airways
Knowles, M. R., & Boucher, R. C. (2002) · Journal of Clinical Investigation · doi:10.1172/jci0215217 · Cited by 1,054 · see citing works
Kramer-Zucker, A. G., Olale, F., Haycraft, C. J., Yoder, B. K., Schier, A. F., & Drummond, I. A. S. (2005) · Development · doi:10.1242/dev.01772 · Cited by 671 · see citing works
DIMMER, K.-S., Friedrich, B., Lang, F. J. W., Deitmer, J. W., & Bröer, S. (2000) · Biochemical Journal · doi:10.1042/bj3500219 · Cited by 579 · see citing works
Requirement of Prorenin Receptor and Vacuolar H + -ATPase–Mediated Acidification for Wnt Signaling
Cruciat, C., Ohkawara, B., Acebrón, S. P., Karaulanov, E., Reinhard, C., Ingelfinger, D., Boutros, M., & Niehrs, C. (2010) · Science · doi:10.1126/science.1179802 · Cited by 548 · see citing works
Voynow, J. A., & Rubin, B. K. (2009) · Chest · doi:10.1378/chest.08-0412 · Cited by 504 · see citing works
Functional biology of intestinal goblet cells
Specian, R. D., & Oliver, M. G. (1991) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1991.260.2.c183 · Cited by 468 · see citing works
Park, T. J., Mitchell, B. J., Abitua, P. B., Kintner, C. R., & Wallingford, J. B. (2008) · Nature Genetics · doi:10.1038/ng.104 · Cited by 448 · see citing works
Wagner, C. A., Finberg, K. E., Breton, S., Marshansky, V. N., Brown, D., & Geibel, J. P. (2004) · Physiological Reviews · doi:10.1152/physrev.00045.2003 · Cited by 432 · see citing works
Regulation of mucociliary clearance in health and disease
Houtmeyers, E., Gosselink, R., Gayan‐Ramirez, G., & Decramer, M. (1999) · European Respiratory Journal · doi:10.1034/j.1399-3003.1999.13e39.x · Cited by 421 · see citing works
Aberrant CFTR-dependent HCO-3 transport in mutations associated with cystic fibrosis
Choi, J. Y., Muallem, D. R., Kiselyov, K. I., Lee, M. G., Thomas, P., & Muallem, S. (2001) · Nature · doi:10.1038/35065099 · Cited by 412 · see citing works
Cystic fibrosis: impaired bicarbonate secretion and mucoviscidosis
Quinton, P. (2008) · The Lancet · doi:10.1016/s0140-6736(08)61162-9 · Cited by 376 · see citing works
Garcia, M. A. S., Yang, N., & Quinton, P. (2009) · Journal of Clinical Investigation · doi:10.1172/jci38662 · Cited by 289 · see citing works
A positive feedback mechanism governs the polarity and motion of motile cilia
Mitchell, B. J., Jacobs, R., Li, J., Chien, S., & Kintner, C. R. (2007) · Nature · doi:10.1038/nature05771 · Cited by 285 · see citing works
Liu, Y., Pathak, N. H., Kramer-Zucker, A. G., & Drummond, I. A. S. (2007) · Development · doi:10.1242/dev.02806 · Cited by 229 · see citing works
Inherited Distal Renal Tubular Acidosis
Karet, F. E. (2002) · Journal of the American Society of Nephrology · doi:10.1097/01.asn.0000023433.08833.88 · Cited by 215 · see citing works
Distal renal tubular acidosis in mice that lack the forkhead transcription factor Foxi1
Blomqvist, S. R., Viđarsson, H., Fitzgerald, S. M., Johansson, B. R., Ollerstam, A., Brown, R. D., Persson, A. E. G., Bergström, G. M. L., & Enerbäck, S. (2004) · Journal of Clinical Investigation · doi:10.1172/jci20665 · Cited by 214 · see citing works
Mechanisms of Acid and Base Secretion by the Airway Epithelium
Fischer, H., & Widdicombe, J. H. (2006) · The Journal of Membrane Biology · doi:10.1007/s00232-006-0861-0 · Cited by 211 · see citing works
Proton pump-rich cell secretes acid in skin of zebrafish larvae
Lin, L., Horng, J., Kunkel, J. G., & Hwang, P. (2005) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00281.2005 · Cited by 207 · see citing works
Mitochondria-Rich, Proton-Secreting Epithelial Cells
Brown, D., & Breton, S. (1996) · Journal of Experimental Biology · doi:10.1242/jeb.199.11.2345 · Cited by 206 · see citing works
Deblandre, G. A., Wettstein, D. A., Koyano‐Nakagawa, N., & Kintner, C. R. (1999) · Development · doi:10.1242/dev.126.21.4715 · Cited by 199 · see citing works
The PCP Pathway Instructs the Planar Orientation of Ciliated Cells in the Xenopus Larval Skin
Mitchell, B. J., Stubbs, J. L., Huisman, F. M., Taborek, P., Yu, C. C., & Kintner, C. R. (2009) · Current Biology · doi:10.1016/j.cub.2009.04.018 · Cited by 193 · see citing works
Ion uptake and acid secretion in zebrafish (Danio rerio)
Hwang, P. (2009) · Journal of Experimental Biology · doi:10.1242/jeb.026054 · Cited by 192 · see citing works
Simons, M., Gault, W. J., Gotthardt, D. N., Rohatgi, R., Klein, T. J., Shao, Y., Lee, H., Wu, A.-L., Fang, Y., Satlin, L. M., et al. (2009) · Nature Cell Biology · doi:10.1038/ncb1836 · Cited by 178 · see citing works
Hulander, M., Kiernan, A. E., Blomqvist, S. R., Carlsson, P., Samuelsson, E.-J., Johansson, B. R., Steel, K. P., & Enerbäck, S. (2003) · Development · doi:10.1242/dev.00376 · Cited by 178 · see citing works
Pseudomyxoma Peritonei Is a Disease of MUC2-Expressing Goblet Cells
O’Connell, J. T., Tomlinson, J. S., Roberts, A. A., McGonigle, K. F., & Barsky, S. H. (2002) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)64211-3 · Cited by 166 · see citing works
Regulated acid–base transport in the collecting duct
Wagner, C. A., Devuyst, O., Bourgeois, S., & Mohebbi, N. (2009) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-009-0657-z · Cited by 162 · see citing works
Vaccari, T., Duchi, S., Cortese, K., Tacchetti, C., & Bilder, D. H. (2010) · Development · doi:10.1242/dev.045484 · Cited by 154 · see citing works
Hsiao, C., You, M., Guh, Y.-J., Ma, M., Jiang, Y., & Hwang, P. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000302 · Cited by 142 · see citing works
Esaki, M., Hoshijima, K., Kobayashi, S., Fukuda, H., Kawakami, K., & Hirose, S. (2006) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00200.2006 · Cited by 142 · see citing works
Regulation of mucin expression in respiratory diseases
Turner, J., & Jones, C. E. (2009) · Biochemical Society Transactions · doi:10.1042/bst0370877 · Cited by 139 · see citing works
Eley, L., Yates, L. M., & Goodship, J. A. (2005) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2005.04.008 · Cited by 139 · see citing works
Viđarsson, H., Westergren, R., Heglind, M., Blomqvist, S. R., Breton, S., & Enerbäck, S. (2009) · PLoS ONE · doi:10.1371/journal.pone.0004471 · Cited by 136 · see citing works
Radial intercalation of ciliated cells during Xenopus skin development
Stubbs, J. L., Davidson, L. A., Keller, R. E., & Kintner, C. R. (2006) · Development · doi:10.1242/dev.02417 · Cited by 128 · see citing works
Planar cell polarity, ciliogenesis and neural tube defects
Wallingford, J. B. (2006) · Human Molecular Genetics · doi:10.1093/hmg/ddl216 · Cited by 126 · see citing works
Hayes, J. M., Kim, S. K., Abitua, P. B., Park, T. J., Herrington, E. R., Kitayama, A., Grow, M. W., Ueno, N., & Wallingford, J. B. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.09.031 · Cited by 120 · see citing works
Epididymal expression of the forkhead transcription factor Foxi1 is required for male fertility
Blomqvist, S. R., Viđarsson, H., Söder, O., & Enerbäck, S. (2006) · The EMBO Journal · doi:10.1038/sj.emboj.7601272 · Cited by 119 · see citing works
Wnt/Frizzled Signaling Requires dPRR, the Drosophila Homolog of the Prorenin Receptor
Buechling, T., Bartscherer, K., Ohkawara, B., Chaudhary, V., Spirohn, K., Niehrs, C., & Boutros, M. (2010) · Current Biology · doi:10.1016/j.cub.2010.05.028 · Cited by 117 · see citing works
Local mucociliary defence mechanisms
Chilvers, M. A., & O’Callaghan, C. (2000) · Paediatric Respiratory Reviews · doi:10.1053/prrv.2000.0009 · Cited by 115 · see citing works
Expression of hypoxia-inducible carbonic anhydrases in brain tumors
Proescholdt, M. A., Mayer, C., Kubitza, M., Schubert, T. E. O., Liao, S., Stanbridge, E. J., Ivanov, S. V., Oldfield, E. H., Brawanski, A. T., & Merrill, M. J. (2005) · Neuro-Oncology · doi:10.1215/s1152851705000025 · Cited by 104 · see citing works
Jänicke, M., Carney, T. J., & Hammerschmidt, M. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.04.044 · Cited by 99 · see citing works
Horng, J., Lin, L., & Hwang, P. (2009) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00576.2008 · Cited by 95 · see citing works
The Key Role of the H+ V-ATPase in Acid–Base Balance and Na+ Transport Processes in Frog Skin
Ehrenfeld, J., & Klein, U. (1997) · Journal of Experimental Biology · doi:10.1242/jeb.200.2.247 · Cited by 93 · see citing works
Expression of transmembrane carbonic anhydrases, CAIX and CAXII, in human development
Liao, S., Lerman, M. I., & Stanbridge, E. J. (2009) · BMC Developmental Biology · doi:10.1186/1471-213x-9-22 · Cited by 92 · see citing works
Esaki, M., Hoshijima, K., Nakamura, N., Munakata, K., Tanaka, M., Ookata, K., Asakawa, K., Kawakami, K., Wang, W., Weinberg, E. S., et al. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2009.02.026 · Cited by 83 · see citing works
Expression regulation of Na+-K+-ATPase α1-subunit subtypes in zebrafish gill ionocytes
Liao, B., Chen, R., & Hwang, P. (2009) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00029.2009 · Cited by 75 · see citing works
Kyllönen, M. S., Parkkila, S., Rajaniemi, H. J., Waheed, A., Grubb, J. H., Shah, G. N., Sly, W. S., & Kaunisto, K. (2003) · Journal of Histochemistry & Cytochemistry · doi:10.1177/002215540305100912 · Cited by 68 · see citing works
Expression of carbonic anhydrases IX and XII during mouse embryonic development
Kallio, H. M. L., Pastoreková, S., Pastorek, J., Waheed, A., Sly, W. S., Mannisto, S., Heikinheimo, M., & Parkkila, S. (2006) · BMC Developmental Biology · doi:10.1186/1471-213x-6-22 · Cited by 56 · see citing works
Suri, C., Haremaki, T., & Weinstein, D. C. (2005) · Development · doi:10.1242/dev.01865 · Cited by 54 · see citing works
Fine structural changes in the differentiating epidermis of Xenopus laevis embryos.
Billett, F. S., & Gould, R. P. (1971) · PubMed · Cited by 53 · see citing works
YANG, J., & Li, T. (2005) · Experimental Cell Research · doi:10.1016/j.yexcr.2005.05.026 · Cited by 53 · see citing works
FoxI1e activates ectoderm formation and controls cell position in theXenopusblastula
Mir, A., Kofron, M. J., Zorn, A. M., Bajzer, M., Haque, M., Heasman, J., & Wylie, C. C. (2007) · Development · doi:10.1242/dev.02768 · Cited by 48 · see citing works
Jouret, F. C., Auzanneau, C., Debaix, H., Sun‐Wada, G., Pretto, C. M., Marbaix, É., Karet, F. E., Courtoy, P. J., & Devuyst, O. (2005) · Journal of the American Society of Nephrology · doi:10.1681/asn.2004110935 · Cited by 48 · see citing works
Vize, P. D., McCoy, K. E., & Zhou, X. (2009) · Nature Protocols · doi:10.1038/nprot.2009.69 · Cited by 44 · see citing works
The forkhead transcription factor Foxi1 directly activates the AE4 promoter
Kurth, I., Hentschke, M., Hentschke, S., Borgmeyer, U., Gal, A., & Hübner, C. A. (2005) · Biochemical Journal · doi:10.1042/bj20051094 · Cited by 38 · see citing works
The amphibian epidermis: distribution of mitochondria-rich cells and the effect of oxytocin
Brown, D. J., Grosso, A., & de Sousa, R. C. (1981) · Journal of Cell Science · doi:10.1242/jcs.52.1.197 · Cited by 38 · see citing works
Pass the bicarb: the importance of HCO3– for mucin release
Lisle, R. C. D. (2009) · Journal of Clinical Investigation · doi:10.1172/jci40598 · Cited by 30 · see citing works
Nagata, S. (2004) · Glycobiology · doi:10.1093/glycob/cwi010 · Cited by 28 · see citing works
A fork in the road of cell differentiation in the kidney tubule
Al‐Awqati, Q., & Schwartz, G. J. (2004) · Journal of Clinical Investigation · doi:10.1172/jci22029 · Cited by 27 · see citing works
Immunoreactivity against goblet cells in patients with inflammatory bowel disease
Ardesjö, B., Portela‐Gomes, G. M., Rorsman, F., Gerdin, E., Lööf, L., Grimelius, L., Kämpe, O., & Ekwall, O. (2008) · Inflammatory Bowel Diseases · doi:10.1002/ibd.20370 · Cited by 26 · see citing works
Active Proton and Urea Transport by Amphibian Skin
Ehrenfeld, J. (1998) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/s1095-6433(97)00408-x · Cited by 22 · see citing works
Nishikawa, S., Hirata, J., & Sasaki, F. (1992) · Histochemistry and Cell Biology · doi:10.1007/bf00271070 · Cited by 17 · see citing works
Ultrastructure of diploid and haploid cells of Xenopus laevis larvae
Fox, H., & Hamilton, L. (1971) · Development · doi:10.1242/dev.26.1.81 · Cited by 17 · see citing works
Spatial distribution of the DF508 mutation in cystic fibrosis: a review.
Braekeleer, M. D., & Daigneault, J. (1992) · PubMed · Cited by 15 · see citing works
Mir, A., Kofron, M. J., Heasman, J., Mogle, M., Tanadini‐Lang, S., Birsoy, B., & Wylie, C. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.12.022 · Cited by 14 · see citing works
Montorzi, M., Burgos, M. H., & Falchuk, K. H. (2000) · Molecular Reproduction and Development · doi:10.1002/(sici)1098-2795(200001)55:1 · Cited by 14 · see citing works
Nickells, R. W., Cavey, M. J., & Browder, L. W. (1988) · The Journal of Cell Biology · doi:10.1083/jcb.106.3.905 · Cited by 7 · see citing works
The emerging role of pendrin in renal chloride reabsorption
Wagner, C. A. (2006) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00449.2006 · Cited by 6 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
A single-cell atlas of the airway epithelium reveals the CFTR-rich pulmonary ionocyte
Plasschaert, L. W., Žilionis, R., Choo-Wing, R., Savova, V., Knehr, J., Roma, G., Klein, A. M., & Jaffe, A. B. (2018) · Nature · doi:10.1038/s41586-018-0394-6 · Cited by 1,047 · see citing works
Multicilin promotes centriole assembly and ciliogenesis during multiciliate cell differentiation
Stubbs, J. L., Vladar, E. K., Axelrod, J. D., & Kintner, C. R. (2012) · Nature Cell Biology · doi:10.1038/ncb2406 · Cited by 241 · see citing works
Pardo–Saganta, A., Law, B. M., Tata, P. R., Villoria, J., Sáez, B., Mou, H., Zhao, R., & Rajagopal, J. (2015) · Cell stem cell · doi:10.1016/j.stem.2015.01.002 · Cited by 202 · see citing works
Microbiota and Mucosal Immunity in Amphibians
Colombo, B. M., Scalvenzi, T., Benlamara, S., & Pollet, N. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00111 · Cited by 169 · see citing works
Myb promotes centriole amplification and later steps of the multiciliogenesis program
Tan, F. E., Vladar, E. K., Ma, L., Fuentealba, L. C., Hoh, R. A., Espinoza, F. H., Axelrod, J. D., Álvarez-Buylla, A., Stearns, T., Kintner, C. R., et al. (2013) · Development · doi:10.1242/dev.094102 · Cited by 136 · see citing works
Xenbase, the Xenopus model organism database; new virtualized system, data types and genomes
Karpinka, J. B., Fortriede, J. D., Burns, K. A., James‐Zorn, C., Ponferrada, V. G., Lee, J., Karimi, K., Zorn, A. M., & Vize, P. D. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku956 · Cited by 134 · see citing works
Expanding the genetic toolkit in Xenopus: Approaches and opportunities for human disease modeling
Tandon, P., Conlon, F. L., Furlow, J. D., & Horb, M. E. (2016) · Developmental Biology · doi:10.1016/j.ydbio.2016.04.009 · Cited by 125 · see citing works
Gastric pouches and the mucociliary sole: setting the stage for nervous system evolution
Arendt, D., Benito-Gutierrez, E., Brunet, T., & Marlow, H. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2015.0286 · Cited by 112 · see citing works
Specification of ion transport cells in theXenopuslarval skin
Quigley, I. K., Stubbs, J. L., & Kintner, C. R. (2011) · Development · doi:10.1242/dev.055699 · Cited by 120 · see citing works
Planarian Epidermal Stem Cells Respond to Positional Cues to Promote Cell-Type Diversity
Wurtzel, O., Oderberg, I. M., & Reddien, P. W. (2017) · Developmental Cell · doi:10.1016/j.devcel.2017.02.008 · Cited by 99 · see citing works
Understanding ciliated epithelia: The power of Xenopus
Werner, M. E., & Mitchell, B. J. (2011) · genesis · doi:10.1002/dvg.20824 · Cited by 94 · see citing works
Xenopus: An Undervalued Model Organism to Study and Model Human Genetic Disease
Blum, M., & Ott, T. (2018) · Cells Tissues Organs · doi:10.1159/000490898 · Cited by 88 · see citing works
Dubaissi, E., Rousseau, K., Lea, R., Soto, X., Nardeosingh, S., Schweickert, A., Amaya, E., Thornton, D. J., & Papalopulu, N. (2014) · Development · doi:10.1242/dev.102426 · Cited by 81 · see citing works
Self-citationRealizing the Physics of Motile Cilia Synchronization with Driven Colloids
Bruot, N., & Cicuta, P. (2016) · Annual Review of Condensed Matter Physics · doi:10.1146/annurev-conmatphys-031115-011451 · Cited by 77 · see citing works
Transgenic ferret models define pulmonary ionocyte diversity and function
Yuan, F., Gasser, G. N., Lemire, E., Montoro, D. T., Jagadeesh, K. A., Zhang, Y., Duan, Y., Ievlev, V., Wells, K. L., Rotti, P. G., et al. (2023) · Nature · doi:10.1038/s41586-023-06549-9 · Cited by 70 · see citing works
Walentek, P., Bogusch, S., Thumberger, T., Vick, P., Dubaissi, E., Beyer, T., Blum, M., & Schweickert, A. (2014) · Development · doi:10.1242/dev.102343 · Cited by 61 · see citing works
Self-citationControl of vertebrate core PCP protein localization and dynamics by Prickle2
Butler, M. T., & Wallingford, J. B. (2015) · Development · doi:10.1242/dev.121384 · Cited by 58 · see citing works
Werner, M. E., Mitchell, J. W., Putzbach, W., Bacon, E., Kim, S. K., & Mitchell, B. J. (2014) · The Journal of Cell Biology · doi:10.1083/jcb.201312045 · Cited by 58 · see citing works
The involvement of PCP proteins in radial cell intercalations during Xenopus embryonic development
Ossipova, O., Chu, C.-W., Fillatre, J., Brott, B., Itoh, K., & Sokol, S. (2015) · Developmental Biology · doi:10.1016/j.ydbio.2015.06.013 · Cited by 52 · see citing works
Polarized Wnt Signaling Regulates Ectodermal Cell Fate in Xenopus
Huang, Y., & Niehrs, C. (2014) · Developmental Cell · doi:10.1016/j.devcel.2014.03.015 · Cited by 52 · see citing works
BMP signalling controls the construction of vertebrate mucociliary epithelia
Cibois, M., Luxardi, G., Chevalier, B., Thomé, V., Mercey, O., Zaragosi, L., Barbry, P., Pasini, A., Marcet, B., & Kodjabachian, L. (2015) · Development · doi:10.1242/dev.118679 · Cited by 52 · see citing works
Myb promotes centriole amplification and later steps of the multiciliogenesis program
Tan, F. E., Vladar, E. K., Ma, L., Fuentealba, L. C., Hoh, R. A., Espinoza, F. H., Axelrod, J. D., Álvarez-Buylla, A., Stearns, T., Kintner, C. R., et al. (2013) · Journal of Cell Science · doi:10.1242/jcs.143099 · Cited by 47 · see citing works
CFAP43 modulates ciliary beating in mouse and Xenopus
Rachev, E., Schuster-Gossler, K., Fuhl, F., Ott, T., Tveriakhina, L., Beckers, A., Hegermann, J., Boldt, K., Mai, M., Kremmer, E., et al. (2019) · Developmental Biology · doi:10.1016/j.ydbio.2019.12.010 · Cited by 46 · see citing works
Cystic Fibrosis and the Cells of the Airway Epithelium: What Are Ionocytes and What Do They Do?
Shah, V. S., Chivukula, R. R., Lin, B., Waghray, A., & Rajagopal, J. (2021) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev-pathol-042420-094031 · Cited by 45 · see citing works
RNA demethylation by FTO stabilizes the FOXJ1 mRNA for proper motile ciliogenesis
Kim, H., Lee, Y.-S., Kim, S., Jang, S., Choi, H., Lee, J., Kim, T., & Kim, V. N. (2021) · Developmental Cell · doi:10.1016/j.devcel.2021.03.006 · Cited by 44 · see citing works
Miyatake, K., Kusakabe, M., Takahashi, C., & Nishida, E. (2015) · Nature Communications · doi:10.1038/ncomms7666 · Cited by 44 · see citing works
The significance of endogenous and exogenous pectic enzymes in fruit and vegetable processing.
Pilnik, W., & Voragen, A. G. J. (1991) · Socio-Environmental Systems Modeling · Cited by 44 · see citing works
Functional characterization of the mucus barrier on the Xenopus tropicalis skin surface
Dubaissi, E., Rousseau, K., Hughes, G. W., Ridley, C. E., Grencis, R. K., Roberts, I. S., & Thornton, D. J. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1713539115 · Cited by 43 · see citing works
Self-citationKim, K., Lake, B. B., Haremaki, T., Weinstein, D. C., & Sokol, S. Y. (2012) · Developmental Dynamics · doi:10.1002/dvdy.23826 · Cited by 35 · see citing works
Huntingtin is required for ciliogenesis and neurogenesis during early Xenopus development
Haremaki, T., Deglincerti, A., & Brivanlou, A. H. (2015) · Developmental Biology · doi:10.1016/j.ydbio.2015.07.013 · Cited by 38 · see citing works
Walentek, P., Beyer, T., Hagenlocher, C., Müller, C., Feistel, K., Schweickert, A., Harland, R. M., & Blum, M. (2015) · Developmental Biology · doi:10.1016/j.ydbio.2015.03.013 · Cited by 38 · see citing works
Viral Vectors, Animal Models, and Cellular Targets for Gene Therapy of Cystic Fibrosis Lung Disease
Tang, Y., Yan, Z., & Engelhardt, J. F. (2020) · Human Gene Therapy · doi:10.1089/hum.2020.013 · Cited by 34 · see citing works
Desmoplakin is required for epidermal integrity and morphogenesis in the Xenopus laevis embryo
Bharathan, N. K., & Dickinson, A. J. G. (2019) · Developmental Biology · doi:10.1016/j.ydbio.2019.03.010 · Cited by 32 · see citing works
Kim, H. Y., Jackson, T. R., Stuckenholz, C., & Davidson, L. A. (2020) · Nature Communications · doi:10.1038/s41467-020-14385-y · Cited by 32 · see citing works
Beckers, A., Adis, C., Schuster-Gossler, K., Tveriakhina, L., Ott, T., Fuhl, F., Hegermann, J., Boldt, K., Serth, K., Rachev, E., et al. (2020) · Development · doi:10.1242/dev.188052 · Cited by 29 · see citing works
Shu, Y., Jiang, H., Yuen, C. N. T., Wang, W., He, J., Zhang, H., Liu, G., Wei, L., Chen, L., & Wu, H. (2022) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2022.113584 · Cited by 29 · see citing works
Tubulin acetylation promotes penetrative capacity of cells undergoing radial intercalation
Collins, C., Kim, S. K., Ventrella, R., Carruzzo, H. M., Wortman, J. C., Han, H., Suva, E., Mitchell, J. W., Yu, C. C., & Mitchell, B. J. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109556 · Cited by 28 · see citing works
Chammas, S. M., Carneiro, S. M., Ferro, R. S., Antoniazzi, M. M., & Jared, C. (2014) · Acta Zoologica · doi:10.1111/azo.12091 · Cited by 26 · see citing works
Lee, J., Møller, A. F., Chae, S., Bussek, A., Park, T. J., Kim, Y., Lee, H., Pers, T. H., Kwon, T., Sedzinski, J., et al. (2023) · Science Advances · doi:10.1126/sciadv.add5745 · Cited by 22 · see citing works
Collins, C., Ventrella, R., & Mitchell, B. J. (2020) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2020.08.001 · Cited by 25 · see citing works
Fluid Mechanics of Mosaic Ciliated Tissues
Boselli, F., Jullien, J., Lauga, E., & Goldstein, R. E. (2021) · Physical Review Letters · doi:10.1103/physrevlett.127.198102 · Cited by 24 · see citing works
Mucociliary Wnt signaling promotes cilia biogenesis and beating
Seidl, C., Silva, F. D., Zhang, K., Wohlgemuth, K., Omran, H., & Niehrs, C. (2023) · Nature Communications · doi:10.1038/s41467-023-36743-2 · Cited by 24 · see citing works
Acquisition of glial cells missing 2 Enhancers Contributes to a Diversity of Ionocytes in Zebrafish
Shono, T., Kurokawa, D., Miyake, T., & Okabe, M. (2011) · PLoS ONE · doi:10.1371/journal.pone.0023746 · Cited by 23 · see citing works
Multicolor Fluorescent In Situ mRNA Hybridization (FISH) on Whole Mounts and Sections
Lea, R., Bonev, B., Dubaissi, E., Vize, P. D., & Papalopulu, N. (2012) · Methods in molecular biology · doi:10.1007/978-1-61779-992-1_24 · Cited by 23 · see citing works
Self-citationPark, T. J., Kim, S. K., & Wallingford, J. B. (2014) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2014.11.078 · Cited by 22 · see citing works
Ott, T., Kaufmann, L. T., Granzow, M., Hinderhofer, K., Bartram, C. R., Theiß, S., Seitz, A., Paramasivam, N., Schulz, A., Moog, U., et al. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00134 · Cited by 21 · see citing works
ΔNp63 is regulated by BMP4 signaling and is required for early epidermal development in Xenopus
Tríbulo, C., Barrionuevo, M. G., Aguero, T. H., Sánchez, S. S., Calcaterra, N. B., & Aybar, M. J. (2011) · Developmental Dynamics · doi:10.1002/dvdy.23706 · Cited by 21 · see citing works
Ptbp1 and Exosc9 knockdowns trigger skin stability defects through different pathways
Noiret, M., Mottier, S., Angrand, G., Gautier‐Courteille, C., Lerivray, H., Viet, J., Paillard, L., Méreau, A., Hardy, S., & Audic, Y. (2015) · Developmental Biology · doi:10.1016/j.ydbio.2015.11.002 · Cited by 21 · see citing works
The Xenopus animal cap transcriptome: building a mucociliary epithelium
Angerilli, A., Smialowski, P., & Rupp, R. A. W. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky771 · Cited by 18 · see citing works
Regeneration of airway epithelial cells to study rare cell states in cystic fibrosis
Barbry, P., Cavard, A., Chanson, M., Jaffe, A. B., & Plasschaert, L. W. (2019) · Journal of Cystic Fibrosis · doi:10.1016/j.jcf.2019.09.010 · Cited by 20 · see citing works
Ionocyte-Specific Regulation of Cystic Fibrosis Transmembrane Conductance Regulator
Sato, Y., Kim, D., Turner, M. J., Luo, Y., Zaidi, S. S. Z., Thomas, D. Y., & Hanrahan, J. W. (2023) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2022-0241oc · Cited by 19 · see citing works
Zhao, Y., Shi, J., Winey, M., & Klymkowsky, M. W. (2016) · Developmental Biology · doi:10.1016/j.ydbio.2016.01.004 · Cited by 17 · see citing works
In vitro platform to model the function of ionocytes in the human airway epithelium
González, M. V., Pinte, L., Fradique, R., Causa, E., Kool, H. M., Rodrat, M., Morell, C. M., Al-Thani, M., Porter, L., Guo, W., et al. (2024) · Respiratory Research · doi:10.1186/s12931-024-02800-7 · Cited by 15 · see citing works
Shi, J., Zhao, Y., Galati, D. F., Winey, M., & Klymkowsky, M. W. (2014) · Developmental Biology · doi:10.1016/j.ydbio.2014.09.008 · Cited by 15 · see citing works
Mercey, O., Kodjabachian, L., Barbry, P., & Marcet, B. (2016) · Small GTPases · doi:10.1080/21541248.2016.1151099 · Cited by 15 · see citing works
Xenopus: An alternative model system for identifying muco-active agents
Sim, H. J., Kim, S., Myung, K., Kwon, T., Lee, H., & Park, T. J. (2018) · PLoS ONE · doi:10.1371/journal.pone.0193310 · Cited by 13 · see citing works
Castillo-Briceño, P., & Kodjabachian, L. (2014) · Frontiers in Zoology · doi:10.1186/1742-9994-11-9 · Cited by 12 · see citing works
CFTR High Expresser Cells in cystic fibrosis and intestinal diseases
dos Reis, D. C., Dastoor, P. K., Santos, A. K., Sumigray, K., & Ameen, N. A. (2023) · Heliyon · doi:10.1016/j.heliyon.2023.e14568 · Cited by 12 · see citing works
mab21-l3 regulates cell fate specification of multiciliate cells and ionocytes
Takahashi, C., Kusakabe, M., Suzuki, T., Miyatake, K., & Nishida, E. (2015) · Nature Communications · doi:10.1038/ncomms7017 · Cited by 12 · see citing works
The role of nitric oxide during embryonic epidermis development ofXenopus laevis
Tománková, S., Abaffy, P., & Radek Sindelka, E. (2017) · Biology Open · doi:10.1242/bio.023739 · Cited by 12 · see citing works
Shu, Y., Wang, H., Jiang, H., Zhou, S., Zhang, L., Ding, Z., Hong, P., He, J., & Wu, H. (2024) · Environmental Pollution · doi:10.1016/j.envpol.2024.123440 · Cited by 11 · see citing works
Emergence of polar order and cooperativity in hydrodynamically coupled model cilia
Bruot, N., & Cicuta, P. (2013) · Journal of The Royal Society Interface · doi:10.1098/rsif.2013.0571 · Cited by 11 · see citing works
Planar Cell Polarity in Ciliated Epithelia
Walentek, P., Boutin, C., & Kodjabachian, L. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-802438-6.00007-3 · Cited by 11 · see citing works
Blackiston, D. J., Dromiack, H. T., Grasso, C., Varley, T. F., Moore, D. G., Srinivasan, K., Sporns, O., Bongard, J., Levin, M. G., & Walker, S. I. (2025) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1012149 · Cited by 10 · see citing works
Yang, H., Sim, H. J., Cho, H., Bang, W. Y., Kim, H. E., Kwon, T. K., Kwon, T., & Park, T. J. (2020) · Scientific Reports · doi:10.1038/s41598-020-63085-6 · Cited by 10 · see citing works
Xenopus: An in vivo model for studying skin response to ultraviolet B irradiation
Mir, J. E., Fédou, S., Thézé, N., Morice‐Picard, F., Cario, M., Fayyad‐Kazan, H., Thiébaud, P., & Rezvani, H. R. (2023) · Development Growth & Differentiation · doi:10.1111/dgd.12848 · Cited by 10 · see citing works
The Xenopus Embryo: An Ideal Model System to Study Human Ciliopathies
Schweickert, A., & Feistel, K. (2015) · Current Pathobiology Reports · doi:10.1007/s40139-015-0074-2 · Cited by 10 · see citing works
Environmental and molecular control of tissue-specific ionocyte differentiation in zebrafish
Peloggia, J., Lush, M. E., Tsai, Y.-Y., Wood, C., & Piotrowski, T. (2024) · Development · doi:10.1242/dev.202809 · Cited by 8 · see citing works
Antibody Development and Use in Chromogenic and Fluorescent Immunostaining
Dubaissi, E., Panagiotaki, N., Papalopulu, N., & Vize, P. D. (2012) · Methods in molecular biology · doi:10.1007/978-1-61779-992-1_23 · Cited by 8 · see citing works
Self-citationXenopus as a model system for studying pigmentation and pigmentary disorders
Mir, J. E., Nasrallah, A., Thézé, N., Cario, M., Fayyad‐Kazan, H., Thiébaud, P., & Rezvani, H. R. (2024) · Pigment Cell & Melanoma Research · doi:10.1111/pcmr.13178 · Cited by 7 · see citing works
Induction and Differentiation of theXenopusCiliated Embryonic Epidermis
Cibois, M., Scerbo, P., Thomé, V., Pasini, A., & Kodjabachian, L. (2014) · doi:10.1002/9781118492833.ch7 · Cited by 7 · see citing works
Kang, H. J., & Kim, H. Y. (2020) · Journal of Visualized Experiments · doi:10.3791/61604 · Cited by 6 · see citing works
Serotonin and MucXS release by small secretory cells depend on Xpod, a SSC specific marker gene
Kurrle, Y., Kunesch, K., Bogusch, S., & Schweickert, A. (2019) · genesis · doi:10.1002/dvg.23344 · Cited by 6 · see citing works
A ‘tad’ of hope in the fight against airway disease
Dubaissi, E. (2020) · Biochemical Society Transactions · doi:10.1042/bst20200745 · Cited by 6 · see citing works
Self-citationChristodoulou, N., & Skourides, P. A. (2025) · Nature Communications · doi:10.1038/s41467-025-61610-7 · Cited by 5 · see citing works
Lung stem cells and therapy for cystic fibrosis
Vaidyanathan, S., McCarra, M. B., & Desai, T. (2021) · European Respiratory Society eBooks · doi:10.1183/2312508x.10010520 · Cited by 5 · see citing works
Single-cell morphodynamics predict cell fate decisions during mucociliary epithelial differentiation
Tolonen, M., Xu, Z., Beker, O., Kapoor, V., Dumitrascu, B., & Sedzinski, J. (2026) · Molecular Systems Biology · doi:10.1038/s44320-026-00212-x · Cited by 4 · see citing works
Paired and solitary ionocytes in the zebrafish olfactory epithelium
Peloggia, J., Cheung, K. Y., Petkova, M. D., Schalek, R. L., Boulanger-Weill, J., Wu, Y., Wang, S., van Hateren, N. J., Januszewski, M., Jain, V., et al. (2025) · Chemical Senses · doi:10.1093/chemse/bjaf031 · Cited by 4 · see citing works
Bowden, S. A., Brislinger-Engelhardt, M. M., Hansen, M., Andricek, A., Temporal-Plo, A., Weber, D., Hägele, S., Lorenz, F., Litwin, T., Kreutz, C., et al. (2026) · PLoS Biology · doi:10.1371/journal.pbio.3003583 · Cited by 4 · see citing works
Early Development of Epidermis and Neural Tissue
Itoh, K., & Sokol, S. Y. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-405945-0.00011-9 · Cited by 4 · see citing works
Corrie, L. M., Kuecks-Winger, H. N., Ebrahimikondori, H., Birol, İ., & Helbing, C. C. (2024) · Comparative Biochemistry and Physiology Part D Genomics and Proteomics · doi:10.1016/j.cbd.2024.101238 · Cited by 3 · see citing works
Single-cell analyses of the corneal epithelium: Unique cell types and gene expression profilesPreprint
Sonam, S., Bangru, S., Perry, K. J., Kalsotra, A., & Henry, J. J. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.08.06.240036 · Cited by 3 · see citing works
Semeraro, D., Mentino, D., Rossi, R., Scillitani, G., Guglielmi, M. V., & Mastrodonato, M. (2024) · The European Zoological Journal · doi:10.1080/24750263.2024.2422089 · Cited by 2 · see citing works
Mucociliary cell type compositions - bridging the gap between genes and emergent tissue functions
Walentek, P. (2025) · Cells and Development · doi:10.1016/j.cdev.2025.204019 · Cited by 2 · see citing works
Whitfield, K., & Crespi, E. J. (2025) · Developmental Dynamics · doi:10.1002/dvdy.70016 · Cited by 2 · see citing works
Semeraro, D., Mentino, D., Rossi, R., Blasi, C. D., Guglielmi, M. V., Scillitani, G., & Mastrodonato, M. (2025) · Microscopy Research and Technique · doi:10.1002/jemt.70098 · Cited by 1 · see citing works
Fotowat, H., O’Neill, L., Pio‐Lopez, L., Sperry, M. M., Erickson, P., Lin, T. G., & Levin, M. G. (2026) · Advanced Science · doi:10.1002/advs.202508967 · Cited by 1 · see citing works
Savostyanov, G. A. (2014) · Paleontological Journal · doi:10.1134/s0031030114110100 · Cited by 1 · see citing works
Solvent Dehydration and Low Temperature Vacuum Drying for SEM Imaging of Pre‐Hatching Frog Embryos
Zurita‐Paredes, D., Flores‐Bolaños, D., Vizuete, K. S., Debut, A., & Romero‐Carvajal, A. (2025) · Journal of Morphology · doi:10.1002/jmor.70030 · Cited by 1 · see citing works
Fotowat, H., O’Neill, L., Pio‐Lopez, L., Sperry, M. M., Erickson, P., Lin, T., & Levin, M. G. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.04.14.648732 · Cited by 1 · see citing works
Kang, H. J., & Kim, H. Y. (2020) · Journal of Visualized Experiments · doi:10.3791/61604-v
Crb3 stabilizes activated Ezrin-Radixin-Moesin to organize the apical domain of multiciliated cellsPreprint
Burcklé, C., Raitière, J., Kodjabachian, L., & Bivic, A. L. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.01.24.525309
Crb3 is required to organize the apical domain of multiciliated cells
Burcklé, C., Raitière, J., Michaux, G., Kodjabachian, L., & Bivic, A. L. (2023) · Journal of Cell Science · doi:10.1242/jcs.261046
González, M. V., Pinte, L., Fradique, R., Causa, E., Kool, H. M., Rodrat, M., Morell, C. M., Al-Thani, M., Porter, L., Guo, W., et al. (2024) · Figshare · doi:10.6084/m9.figshare.25698161
González, M. V., Pinte, L., Fradique, R., Causa, E., Kool, H. M., Rodrat, M., Morell, C. M., Al-Thani, M., Porter, L., Guo, W., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26712356
González, M. V., Pinte, L., Fradique, R., Causa, E., Kool, H. M., Rodrat, M., Morell, C. M., Al-Thani, M., Porter, L., Guo, W., et al. (2024) · Figshare · doi:10.6084/m9.figshare.25698435
- Authors
- Dubaissi, E., & Papalopulu, N.
- Affiliations
- University of Manchester (GB)
- Corresponding author
- Papalopulu, Nancy
- Venue
- Disease Models & Mechanisms
- Publisher
- The Company of Biologists
- Published
- 2011-03-01
- Volume
- 4
- Issue
- 2
- Pages
- 179-192
- ISSN
- 1754-8403 (ISSN-L)
- 1754-8411
- PMC
- PMC3046089
- OpenAlex
- W2118253874
- Cited by
- 102
- References
- 69
- Citations by year
- 2026: 4 · 2025: 8 · 2024: 9 · 2023: 9 · 2022: 1 · 2021: 6 · 2020: 11 · 2019: 5 · 2018: 5 · 2017: 3 · 2016: 4 · 2015: 12 · 2014: 13 · 2013: 3 · 2012: 4
- FWCI
- 1.98
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc-sa
- Locations
- Disease Models & Mechanisms (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- HighWire Press Open Archive (submittedVersion)
- Research Explorer (The University of Manchester) (submittedVersion)
- Funders
- Wellcome Trust (090868)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and Kidney Cyst Diseases
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Cystic Fibrosis Research Advances
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- ionocytes, multiciliated cells, cilia biogenesis, mucous cells, ion regulation, cell-cell interactions, ciliary beating, epithelial development
- MeSH terms
- Animals, Cell Communication, Cilia, Disease, Embryo, Nonmammalian, Epidermis, Models, Biological, Mucus, Xenopus, Gene Expression Regulation, Developmental, Goblet Cells, Xenopus Proteins, Forkhead Transcription Factors, Gene Knockdown Techniques
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
