Serotonin and MucXS release by small secretory cells depend on Xpod, a SSC specific marker gene.


Journal

Genesis (New York, N.Y. : 2000)
ISSN: 1526-968X
Titre abrégé: Genesis
Pays: United States
ID NLM: 100931242

Informations de publication

Date de publication:
02 2020
Historique:
received: 10 07 2019
revised: 24 10 2019
accepted: 25 10 2019
pubmed: 11 11 2019
medline: 2 1 2021
entrez: 10 11 2019
Statut: ppublish

Résumé

Mucus secretion and ciliary motility are hallmarks for muco-ciliary epithelia (MCE). Both, mammalian airways as well as the less complex epidermis of Xenopus embryos show cilia-driven mucus flow to protect the organism against harmful effects by exogenous pathogens or pollutants. Four cell types set up the epidermal MCE in Xenopus. Multi-ciliated cells (MCCs) generate an anterior to posterior flow of mucus. Ion secreting cells (ISCs) are characterized by the expression of ion transporters, presumably to maintain a favorable homeostasis. The largest cell type is represented by goblet cells, which cover most of the epidermis and exhibit secretory properties. Additionally, small secretory cells (SSCs) release mucus, antibiotic compounds, and the monoamine serotonin (5-hydroxytryptamine; 5-HT). We have recently shown that serotonin regulates flow velocity by acting on ciliary beat frequency. Here, we describe the identification and functional characterization of Xenopus polka-dots (Xpod). No homologous genes or proteins were found in other vertebrates, including Xenopus tropicalis. We demonstrate that Xpod serves as an SSC-specific marker, starting to be expressed shortly after SSC specification at neurula stages. Overexpression of a tagged Xpod protein resulted in the localization of secretory granules. Notch signaling induced SSC cell fate, in contrast to its repressing effect on MCC and ISC specification. Xpod loss-of-function revealed that mucus and 5-HT release by SSCs was severely diminished, which impaired the ciliary beating of MCCs. In summary, Xpod specifically marked SSCs and was required for muco-ciliary secretion in Xenopus laevis.

Identifiants

pubmed: 31705622
doi: 10.1002/dvg.23344
doi:

Substances chimiques

Receptors, Notch 0
Xenopus Proteins 0
Xolka dots protein, Xenopus 0
Serotonin 333DO1RDJY

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e23344

Informations de copyright

© 2019 The Authors. Genesis published by Wiley Periodicals, Inc.

Références

Afzelius, B. A. (2004). Cilia-related diseases. The Journal of Pathology, 204(4), 470-477. http://doi.org/10.1002/path.1652
Aono, K., Fusada, A., Fusada, Y., Ishii, W., Kanaya, Y., Komuro, M., … Ito, E. (2008). Upside-down gliding of Lymnaea. The Biological Bulletin, 215(3), 272-279. http://doi.org/10.2307/25470711
Belo, J. A., Bouwmeester, T., Leyns, L., Kertesz, N., Gallo, M., Follettie, M., & De Robertis, E. M. (1997). Cerberus-like is a secreted factor with neutralizing activity expressed in the anterior primitive endoderm of the mouse gastrula. Mechanisms of Development, 68(1-2), 45-57.
BéruBé, K., Prytherch, Z., Job, C., & Hughes, T. (2010). Human primary bronchial lung cell constructs: The new respiratory models. Toxicology, 278(3), 311-318. http://doi.org/10.1016/j.tox.2010.04.004
Besnard, V., Wert, S. E., Kaestner, K. H., & Whitsett, J. A. (2005). Stage-specific regulation of respiratory epithelial cell differentiation by Foxa1. American Journal of Physiology Lung Cellular and Molecular Physiology, 289(5), L750-L759. http://doi.org/10.1152/ajplung.00151.2005
Boucher, R. C. (2007). Cystic fibrosis: A disease of vulnerability to airway surface dehydration. Trends in Molecular Medicine, 13(6), 231-240. http://doi.org/10.1016/j.molmed.2007.05.001
Bustamante-Marin, X. M., & Ostrowski, L. E. (2017). Cilia and mucociliary clearance. Cold Spring Harbor Perspectives in Biology, 9(4), a028241. http://doi.org/10.1101/cshperspect.a028241
Deblandre, G. A., Wettstein, D. A., Koyano-Nakagawa, N., & Kintner, C. (1999). A two-step mechanism generates the spacing pattern of the ciliated cells in the skin of Xenopus embryos. Development (Cambridge, England), 126(21), 4715-4728.
Dubaissi, E., & Papalopulu, N. (2011). Embryonic frog epidermis: A model for the study of cell-cell interactions in the development of mucociliary disease. Disease Models & Mechanisms, 4(2), 179-192. http://doi.org/10.1242/dmm.006494
Dubaissi, E., Rousseau, K., Hughes, G. W., Ridley, C., Grencis, R. K., Roberts, I. S., & Thornton, D. J. (2018). Functional characterization of the mucus barrier on the Xenopus tropicalis skin surface. Proceedings of the National Academy of Sciences of the United States of America, 115, 726-731. http://doi.org/10.1073/pnas.1713539115
Dubaissi, E., Rousseau, K., Lea, R., Soto, X., Nardeosingh, S., Schweickert, A., … Papalopulu, N. (2014). A secretory cell type develops alongside multiciliated cells, ionocytes and goblet cells, and provides a protective, anti-infective function in the frog embryonic mucociliary epidermis. Development (Cambridge, England), 141(7), 1514-1525. http://doi.org/10.1242/dev.102426
Esaki, M., Hoshijima, K., Nakamura, N., Munakata, K., Tanaka, M., Ookata, K., … Hirose, S. (2009). Mechanism of development of ionocytes rich in vacuolar-type H(+)-ATPase in the skin of zebrafish larvae. Developmental Biology, 329(1), 116-129. http://doi.org/10.1016/j.ydbio.2009.02.026
Green, C. B., Cahill, G. M., & Besharse, J. C. (1995). Regulation of tryptophan hydroxylase expression by a retinal circadian oscillator in vitro. Brain Research, 677(2), 283-290.
Hayes, J. M., Kim, S. K., Abitua, P. B., Park, T. J., Herrington, E. R., Kitayama, A., … Wallingford, J. B. (2007). Identification of novel ciliogenesis factors using a new in vivo model for mucociliary epithelial development. Developmental Biology, 312(1), 115-130. http://doi.org/10.1016/j.ydbio.2007.09.031
Holland, N. D., & Holland, L. Z. (2006). Stage- and tissue-specific patterns of cell division in embryonic and larval tissues of amphioxus during normal development. Evolution and Development, 8(2), 142-149. http://doi.org/10.1111/j.1525-142X.2006.00085.x
Karimi, K., Fortriede, J. D., Lotay, V. S., Burns, K. A., Wang, D. Z., Fisher, M. E., … Vize, P. D. (2018). Xenbase: A genomic, epigenomic and transcriptomic model organism database. Nucleic Acids Research, 46(D1), D861-D868. http://doi.org/10.1093/nar/gkx936
Knoop, K. A., & Newberry, R. D. (2018). Goblet cells: Multifaceted players in immunity at mucosal surfaces. Mucosal Immunology, 1, 1551-1557. http://doi.org/10.1038/s41385-018-0039-y
Lawal, H. O., & Krantz, D. E. (2013). SLC18: Vesicular neurotransmitter transporters for monoamines and acetylcholine. Molecular Aspects of Medicine, 34(2-3), 360-372. http://doi.org/10.1016/j.mam.2012.07.005
Livraghi, A., & Randell, S. H. (2007). Cystic fibrosis and other respiratory diseases of impaired mucus clearance. Toxicologic Pathology, 35(1), 116-129. http://doi.org/10.1080/01926230601060025
Matsuda, Y., Uno, Y., Kondo, M., Gilchrist, M. J., Zorn, A. M., Rokhsar, D. S., … Taira, M. (2015). A new nomenclature of Xenopus laevis chromosomes based on the phylogenetic relationship to Silurana/Xenopus tropicalis. Cytogenetic and Genome Research, 145(3-4), 187-191. http://doi.org/10.1159/000381292
Meunier, A., & Azimzadeh, J. (2016). Multiciliated cells in animals. Cold Spring Harbor Perspectives in Biology, 8(12), 1-21. http://doi.org/10.1101/cshperspect.a028233
Montoro, D. T., Haber, A. L., Biton, M., Vinarsky, V., Lin, B., Birket, S. E., … Rajagopal, J. (2018). A revised airway epithelial hierarchy includes CFTR-expressing ionocytes. Nature, 560(7718), 319-324. http://doi.org/10.1038/s41586-018-0393-7
Nagata, S. (2005). Isolation, characterization, and extra-embryonic secretion of the Xenopus laevis embryonic epidermal lectin, XEEL. Glycobiology, 15(3), 281-290. http://doi.org/10.1093/glycob/cwi010
Nagata, S., Nakanishi, M., Nanba, R., & Fujita, N. (2003). Developmental expression of XEEL, a novel molecule of the Xenopus oocyte cortical granule lectin family. Development Genes and Evolution, 213(7), 368-370. http://doi.org/10.1007/s00427-003-0341-9
Perez-Vilar, J. (2007). Mucin granule intraluminal organization. American Journal of Respiratory Cell and Molecular Biology, 36(2), 183-190. http://doi.org/10.1165/rcmb.2006-0291TR
Quigley, I. K., Stubbs, J. L., & Kintner, C. (2011). Specification of ion transport cells in the Xenopus larval skin. Development (Cambridge, England), 138(4), 705-714. http://doi.org/10.1242/dev.055699
Ridley, C., & Thornton, D. J. (2018). Mucins: The frontline defence of the lung. Biochemical Society Transactions, 46(5), 1099-1106. http://doi.org/10.1042/BST20170402
Rompolas, P., Patel-King, R. S., & King, S. M. (2010). An outer arm dynein conformational switch is required for metachronal synchrony of motile cilia in planaria. Molecular Biology of the Cell, 21(21), 3669-3679. http://doi.org/10.1091/mbc.E10-04-0373
Rubin, B. K. (2007). Mucus structure and properties in cystic fibrosis. Paediatric Respiratory Reviews, 8(1), 4-7. http://doi.org/10.1016/j.prrv.2007.02.004
Sander, V., Reversade, B., & De Robertis, E. M. (2007). The opposing homeobox genes Goosecoid and Vent1/2 self-regulate Xenopus patterning. The EMBO Journal, 26(12), 2955-2965. http://doi.org/10.1038/sj.emboj.7601705
Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012). NIH image to ImageJ: 25 years of image analysis. Nature Methods, 9(7), 671-675.
Schweickert, A., & Feistel, K. (2015). The Xenopus embryo: An ideal model system to study human Ciliopathies. Current Pathobiology Reports, 3, 1-15. http://doi.org/10.1007/s40139-015-0074-2
Session, A. M., Uno, Y., Kwon, T., Chapman, J. A., Toyoda, A., Takahashi, S., … Rokhsar, D. S. (2016). Genome evolution in the allotetraploid frog Xenopus laevis. Nature, 538(7625), 336-343. http://doi.org/10.1038/nature19840
Sive, H. L., Grainger, R. M., & Harland, R. M. (2000). Early development of Xenopus laevis : A laboratory manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
Thomas, J., Morlé, L., Soulavie, F., Laurençon, A., Sagnol, S., & Durand, B. (2010). Transcriptional control of genes involved in ciliogenesis: A first step in making cilia. Biology of the Cell, 102(9), 499-513. http://doi.org/10.1042/BC20100035
Tilley, A. E., Walters, M. S., Shaykhiev, R., & Crystal, R. G. (2014). Cilia dysfunction in lung disease. Annual Review of Physiology, 77, 379-406. http://doi.org/10.1146/annurev-physiol-021014-071931
Ulmer, B., Tingler, M., Kurz, S., Maerker, M., Andre, P., Mönch, D., … Blum, M. (2017). A novel role of the organizer gene Goosecoid as an inhibitor of Wnt/PCP-mediated convergent extension in Xenopus and mouse. Scientific Reports, 7(43010), 1-17. http://doi.org/10.1038/srep43010
van der Sluis, M., Vincent, A., Bouma, J., Korteland-Van Male, A., van Goudoever, J. B., Renes, I. B., & Van Seuningen, I. (2008). Forkhead box transcription factors Foxa1 and Foxa2 are important regulators of Muc2 mucin expression in intestinal epithelial cells. Biochemical and Biophysical Research Communications, 369(4), 1108-1113. http://doi.org/10.1016/j.bbrc.2008.02.158
Walentek, P. (2018). Manipulating and analyzing cell type composition of the xenopus mucociliary epidermis. Methods in Molecular Biology, 1865(1-2), 251-263. http://doi.org/10.1007/978-1-4939-8784-9_18
Walentek, P., Bogusch, S., Thumberger, T., Vick, P., Dubaissi, E., Beyer, T., … Schweickert, A. (2014). A novel serotonin-secreting cell type regulates ciliary motility in the mucociliary epidermis of Xenopus tadpoles. Development (Cambridge, England), 141(7), 1526-1533. http://doi.org/10.1242/dev.102343
Wan, H., Kaestner, K. H., Ang, S.-L., Ikegami, M., Finkelman, F. D., Stahlman, M. T., … Whitsett, J. A. (2004). Foxa2 regulates alveolarization and goblet cell hyperplasia. Development (Cambridge, England), 131(4), 953-964. http://doi.org/10.1242/dev.00966
Wangkanont, K., Wesener, D. A., Vidani, J. A., Kiessling, L. L., & Forest, K. T. (2016). Structures of Xenopus embryonic epidermal lectin reveal a conserved mechanism of microbial glycan recognition. Journal of Biological Chemistry, 291, 5596-5610. http://doi.org/10.1074/jbc.M115.709212
Yaffe, D., Forrest, L. R., & Schuldiner, S. (2018). The ins and outs of vesicular monoamine transporters. The Journal of General Physiology, 150(5), 671-682. http://doi.org/10.1085/jgp.201711980
Ye, D. Z., & Kaestner, K. H. (2009). Foxa1 and Foxa2 control the differentiation of goblet and enteroendocrine L- and D-cells in mice. Gastroenterology, 137(6), 2052-2062. http://doi.org/10.1053/j.gastro.2009.08.059
Yoshii, S., Yamaguchi, M., Oogata, Y., Tazaki, A., Mochii, M., Suzuki, S., & Kinoshita, T. (2011). The analysis of the expression of a novel gene, Xenopus polka dots, which was expressed in the embryonic and larval epidermis during early development. Zoological Science, 28(11), 809-816. http://doi.org/10.2108/zsj.28.809
Yu, X., Ng, C. P., Habacher, H., & Roy, S. (2008). Foxj1 transcription factors are master regulators of the motile ciliogenic program. Nature Genetics, 40(12), 1445-1453. http://doi.org/10.1038/ng.263

Auteurs

Yvonne Kurrle (Y)

Institute of Zoology, University of Hohenheim, Stuttgart, Germany.

Katharina Kunesch (K)

Institute of Zoology, University of Hohenheim, Stuttgart, Germany.

Susanne Bogusch (S)

Institute of Zoology, University of Hohenheim, Stuttgart, Germany.

Axel Schweickert (A)

Institute of Zoology, University of Hohenheim, Stuttgart, Germany.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH