Directed Migration of Pulmonary Neuroendocrine Cells toward Airway Branches Organizes the Stereotypic Location of Neuroepithelial Bodies

Cell Reports

Volumn 13, Issue 12, 2015, Pages 2679-2686

  Noguchi, Masafumi ^a   Sumiyama, Kenta ^b   Morimoto, Mitsuru ^a  

^a RIKEN Center for Biosystems Dynamics Research   (Japan)

^b OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

NOTCH RECEPTOR; TRANSCRIPTION FACTOR HES 1;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL DIFFERENTIATION; CELL MATURATION; CELL MIGRATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EX VIVO STUDY; IMMUNOHISTOCHEMISTRY; LUNG DEVELOPMENT; NEUROEPITHELIAL BODY; NEUROSECRETORY CELL; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; THREE DIMENSIONAL IMAGING; ANIMAL; CELL MOTION; CYTOLOGY; LUNG; METABOLISM; MOUSE; PHYSIOLOGY;

ANIMALS; CELL MOVEMENT; IMMUNOHISTOCHEMISTRY; LUNG; MICE; NEUROENDOCRINE CELLS; NEUROEPITHELIAL BODIES;

EID: 84975705408     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.11.058     Document Type: Article

References (33)

1. Abe, T., Kiyonari, H., Shioi, G., Inoue, K., Nakao, K., Aizawa, S., Fujimori, T., Establishment of conditional reporter mouse lines at ROSA26 locus for live cell imaging. Genesis 49 (2011), 579–590.
2. Adriaensen, D., Timmermans, J.P., Brouns, I., Berthoud, H.R., Neuhuber, W.L., Scheuermann, D.W., Pulmonary intraepithelial vagal nodose afferent nerve terminals are confined to neuroepithelial bodies: an anterograde tracing and confocal microscopy study in adult rats. Cell Tissue Res. 293 (1998), 395–405.
3. Artavanis-Tsakonas, S., Rand, M.D., Lake, R.J., Notch signaling: cell fate control and signal integration in development. Science 284 (1999), 770–776.
4. Avadhanam, K.P., Plopper, C.G., Pinkerton, K.E., Mapping the distribution of neuroepithelial bodies of the rat lung. A whole-mount immunohistochemical approach. Am. J. Pathol. 150 (1997), 851–859.
5. Boers, J.E., den Brok, J.L., Koudstaal, J., Arends, J.W., Thunnissen, F.B., Number and proliferation of neuroendocrine cells in normal human airway epithelium. Am. J. Respir. Crit. Care Med. 154 (1996), 758–763.
6. Chang, R.B., Strochlic, D.E., Williams, E.K., Umans, B.D., Liberles, S.D., Vagal Sensory Neuron Subtypes that Differentially Control Breathing. Cell 161 (2015), 622–633.
7. Cutz, E., Chan, W., Sonstegard, K.S., Identification of neuro-epithelial bodies in rabbit fetal lungs by scanning electron microscopy: a correlative light, transmission and scanning electron microscopic study. Anat. Rec. 192 (1978), 459–466.
8. Deterding, R.R., Pye, C., Fan, L.L., Langston, C., Persistent tachypnea of infancy is associated with neuroendocrine cell hyperplasia. Pediatr. Pulmonol. 40 (2005), 157–165.
9. Fujita, T., Kanno, T., Kobayashi, S., The Paraneuron. 1998, Springer-Verlag.
10. Gillan, J.E., Pape, K.E., Cutz, E., Association of changes in bombesin immunoreactive neuroendocrine cells in lungs of newborn infants with persistent fetal circulation and brainstem damage due to birth asphyxia. Pediatr. Res. 20 (1986), 828–833.
11. Gosney, J.R., Sissons, M.C., Allibone, R.O., Neuroendocrine cell populations in normal human lungs: a quantitative study. Thorax 43 (1988), 878–882.
12. Hong, K.U., Reynolds, S.D., Giangreco, A., Hurley, C.M., Stripp, B.R., Clara cell secretory protein-expressing cells of the airway neuroepithelial body microenvironment include a label-retaining subset and are critical for epithelial renewal after progenitor cell depletion. Am. J. Respir. Cell Mol. Biol. 24 (2001), 671–681.
13. Hoyt, R.F. Jr., McNelly, N.A., Sorokin, S.P., Dynamics of neuroepithelial body (NEB) formation in developing hamster lung: light microscopic autoradiography after 3H-thymidine labeling in vivo. Anat. Rec. 227 (1990), 340–350.
14. Ito, T., Udaka, N., Yazawa, T., Okudela, K., Hayashi, H., Sudo, T., Guillemot, F., Kageyama, R., Kitamura, H., Basic helix-loop-helix transcription factors regulate the neuroendocrine differentiation of fetal mouse pulmonary epithelium. Development 127 (2000), 3913–3921.
15. Jain, S., Golden, J.P., Wozniak, D., Pehek, E., Johnson, E.M. Jr., Milbrandt, J., RET is dispensable for maintenance of midbrain dopaminergic neurons in adult mice. J. Neurosci. 26 (2006), 11230–11238.
16. Kuo, C.S., Krasnow, M.A., Formation of a Neurosensory Organ by Epithelial Cell Slithering. Cell 163 (2015), 394–405.
17. Linnoila, R.I., Functional facets of the pulmonary neuroendocrine system. Lab. Invest. 86 (2006), 425–444.
18. Metzger, R.J., Klein, O.D., Martin, G.R., Krasnow, M.A., The branching programme of mouse lung development. Nature 453 (2008), 745–750.
19. Montuenga, L.M., Springall, D.R., Gaer, J., Winter, F.J., Zhao, L., McBride, J.T., Taylor, K.M., Barer, G., Polak, J.M., CGRP-immunoreactive endocrine cell proliferation in normal and hypoxic rat lung studied by immunocytochemical detection of incorporation of 5′-bromodeoxyuridine. Cell Tissue Res. 268 (1992), 9–15.
20. Morimoto, M., Nishinakamura, R., Saga, Y., Kopan, R., Different assemblies of Notch receptors coordinate the distribution of the major bronchial Clara, ciliated and neuroendocrine cells. Development 139 (2012), 4365–4373.
21. Morrisey, E.E., Hogan, B.L., Preparing for the first breath: genetic and cellular mechanisms in lung development. Dev. Cell 18 (2010), 8–23.
22. Perl, A.K., Wert, S.E., Nagy, A., Lobe, C.G., Whitsett, J.A., Early restriction of peripheral and proximal cell lineages during formation of the lung. Proc. Natl. Acad. Sci. USA 99 (2002), 10482–10487.
23. Rackley, C.R., Stripp, B.R., Building and maintaining the epithelium of the lung. J. Clin. Invest. 122 (2012), 2724–2730.
24. Rawlins, E.L., Clark, C.P., Xue, Y., Hogan, B.L., The Id2+ distal tip lung epithelium contains individual multipotent embryonic progenitor cells. Development 136 (2009), 3741–3745.
25. Rawlins, E.L., Okubo, T., Xue, Y., Brass, D.M., Auten, R.L., Hasegawa, H., Wang, F., Hogan, B.L., The role of Scgb1a1+ Clara cells in the long-term maintenance and repair of lung airway, but not alveolar, epithelium. Cell Stem Cell 4 (2009), 525–534.
26. Reynolds, S.D., Giangreco, A., Power, J.H., Stripp, B.R., Neuroepithelial bodies of pulmonary airways serve as a reservoir of progenitor cells capable of epithelial regeneration. Am. J. Pathol. 156 (2000), 269–278.
27. Rock, J.R., Gao, X., Xue, Y., Randell, S.H., Kong, Y.Y., Hogan, B.L., Notch-dependent differentiation of adult airway basal stem cells. Cell Stem Cell 8 (2011), 639–648.
28. Semenova, E.A., Nagel, R., Berns, A., Origins, genetic landscape, and emerging therapies of small cell lung cancer. Genes Dev. 29 (2015), 1447–1462.
29. Song, H., Yao, E., Lin, C., Gacayan, R., Chen, M.H., Chuang, P.T., Functional characterization of pulmonary neuroendocrine cells in lung development, injury, and tumorigenesis. Proc. Natl. Acad. Sci. USA 109 (2012), 17531–17536.
30. Susaki, E.A., Tainaka, K., Perrin, D., Kishino, F., Tawara, T., Watanabe, T.M., Yokoyama, C., Onoe, H., Eguchi, M., Yamaguchi, S., et al. Whole-brain imaging with single-cell resolution using chemical cocktails and computational analysis. Cell 157 (2014), 726–739.
31. Tsao, P.N., Vasconcelos, M., Izvolsky, K.I., Qian, J., Lu, J., Cardoso, W.V., Notch signaling controls the balance of ciliated and secretory cell fates in developing airways. Development 136 (2009), 2297–2307.
32. Young, L.R., Brody, A.S., Inge, T.H., Acton, J.D., Bokulic, R.E., Langston, C., Deutsch, G.H., Neuroendocrine cell distribution and frequency distinguish neuroendocrine cell hyperplasia of infancy from other pulmonary disorders. Chest 139 (2011), 1060–1071.
33. Youngson, C., Nurse, C., Yeger, H., Cutz, E., Oxygen sensing in airway chemoreceptors. Nature 365 (1993), 153–155.