Notch signaling controls the balance of ciliated and secretory cell fates in developing airways

Development

Volumn 136, Issue 13, 2009, Pages 2297-2307

  Tsao, Po Nien ^a,b   Vasconcelos, Michelle ^a,c   Izvolsky, Konstantin I ^a   Qian, Jun ^a   Lu, Jining ^a   Cardoso, Wellington V ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Airway differentiation; Cell fate; Ciliated cell; Clara cell; Lung development; Neuroendocrine cell; Notch; Pofut1; Rbpjk (Rbpj)

Indexed keywords

FUCOSYLTRANSFERASE; FUCOSYLTRANSFERASE 1; GAMMA SECRETASE INHIBITOR; IMMUNOGLOBULIN J RECOMBINATION SIGNAL SEQUENCE BINDING PROTEIN; NOTCH RECEPTOR; UNCLASSIFIED DRUG;

ALLELE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL DIFFERENTIATION; CELL EXPANSION; CELL FATE; CILIATED EPITHELIUM; CONTROLLED STUDY; EMBRYO; ENDODERM; FEMALE; GENE DELETION; GENE INACTIVATION; LIGAND BINDING; LUNG DEVELOPMENT; MOUSE; NEUROSECRETORY CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; SECRETORY CELL; SIGNAL TRANSDUCTION; STEM CELL;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; CELLS, CULTURED; CILIA; CONGENITAL ABNORMALITIES; EMBRYO LOSS; EPITHELIAL CELLS; FEMALE; FUCOSYLTRANSFERASES; GENE DELETION; HUMANS; LUNG; MALE; MICE; RECEPTORS, NOTCH; RESPIRATORY MUCOSA; SIGNAL TRANSDUCTION; SOXB1 TRANSCRIPTION FACTORS;

MUS;

EID: 69549088763     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.034884     Document Type: Article

References (61)

1. Beckers, J., Clark, A., Wunsch, K., Hrabe De Angelis, M. and Gossler, A. (1999). Expression of the mouse Delta1 gene during organogenesis and fetal development. Mech. Dev. 84, 165-168.
2. Brody, S. L., Yan, X. H., Wuerffel, M. K., Song, S. K. and Shapiro, S. D. (2000). Ciliogenesis and left-right axis defects in forkhead factor HFH-4-null mice. Am. J. Respir. Cell Mol. Biol. 23, 45-51.
3. Cardoso, W. V. and Lü, J. (2006). Regulation of early lung morphogenesis: questions, facts and controversies. Development 133, 1611-1624.
4. Chen, F., Desai, T. J., Qian, J., Niederreither, K., Lü, J. and Cardoso, W. V. (2007). Inhibition of Tgf beta signaling by endogenous retinoic acid is essential for primary lung bud induction. Development 134, 2969-2979.
5. Collins, B. J., Kleeberger, W. and Ball, D. W. (2004). Notch in lung development and lung cancer. Semin. Cancer Biol. 14, 357-364.
6. Dabdoub, A., Puligilla, C., Jones, J. M., Fritzsch, B., Cheah, K. S., Pevny, L. H. and Kelley, M. W. (2008). Sox2 signaling in prosensory domain specification and subsequent hair cell differentiation in the developing cochlea. Proc. Natl. Acad. Sci. USA 105, 18396-18401.
7. Dang, T. P., Eichenberger, S., Gonzalez, A., Olson, S. and Carbone, D. P. (2003). Constitutive activation of Notch3 inhibits terminal epithelial differentiation in lungs of transgenic mice. Oncogene 22, 1988-1997.
8. Daniely, Y., Liao, G., Dixon, D., Linnoila, R. I., Lori, A., Randell, S. H., Oren, M. and Jetten, A. M. (2004). Critical role of p63 in the development of a normal esophageal and tracheobronchial epithelium. Am. J. Physiol. Cell Physiol. 287, 171-181.
9. Deblandre, G. A., Wettstein, D. A., Koyano-Nakagawa, N. and Kintner, C. (1999). A two-step mechanism generates the spacing pattern of the ciliated cells in the skin of Xenopus embryos. Development 126, 4715-4728.
10. Evans, C. M., Williams, O. W., Tuvim, M. J., Nigam, R., Mixides, G. P., Blackburn, M. R., DeMayo, F. J., Burns, A. R., Smith, C., Reynolds, S. D. et al. (2004). Mucin is produced by clara cells in the proximal airways of antigen-challenged mice. Am. J. Respir. Cell Mol. Biol. 31, 382-394.
11. Franks, T. J., Colby, T. V., Travis, W. D., Tuder, R. M., Reynolds, H. Y., Brody, A. R., Cardoso, W. V., Crystal, R. G., Drake, C. J., Engelhardt, J. et al. (2008). Resident cellular components of the human lung: current knowledge and goals for research on cell phenotyping and function. Proc. Am. Thorac. Soc. 15, 763-766.
12. Gontan, C., de Munck, A., Vermeij, M., Grosveld, F., Tibboel, D. and Rottier, R. (2008). Sox2 is important for two crucial processes in lung development: branching morphogenesis and epithelial cell differentiation. Dev. Biol. 317, 296-309.
13. Graham, V., Khudyakov, J., Ellis, P. and Pevny, L. (2003). SOX2 functions to maintain neural progenitor identity. Neuron 39, 749-765.
14. Gridley, T. (2007). Notch signaling in vascular development and physiology. Development 134, 2709-2718.
15. Guilmeau, S., Flandez, M., Bancroft, L., Sellers, R. S., Tear, B., Stanley, P. and Augenlicht, L. H. (2008). Intestinal deletion of Pofut1 in the mouse inactivates notch signaling and causes enterocolitis. Gastroenterology 135, 849-860.
16. Guseh, J. S., Bores, S. A., Stanger, B. Z., Zhou, Q., Anderson, W. J., Melton, D. A. and Rajagopal, J. (2009). Notch signaling promotes airway mucous metaplasia and inhibits alveolar development. Development 136, 1751-1759.
17. Han, H., Tanigaki, K., Yamamoto, N., Kuroda, K., Yoshimoto, M., Nakahata, T., Ikuta, K. and Honjo, T. (2002). Inducible gene knockout of transcription factor recombination signal binding protein-J reveals its essential role in T versus B lineage decision. Int. Immunol. 14, 637-645.
18. Harfe, B. D., Scherz, P. J., Nissim, S., Tian, H., McMahon, A. P. and Tabin, C. J. (2004). Evidence for an expansion-based temporal Shh gradient in specifying vertebrate digit identities. Cell 118, 517-528.
19. Harris, K. S., Zhang, Z., McManus, M. T., Harfe, B. D. and Sun, X. (2006). Dicer function is essential for lung epithelium morphogenesis. Proc. Natl. Acad. Sci. USA 103, 2208-2213.
20. Hayes, J. M., Kim, S. K., Abitua, P. B., Park, T. J., Herrington, E. R., Kitayama, A., Grow, M. W., Ueno, N. and Wallingford, J. B. (2007). Identification of novel ciliogenesis factors using a new in vivo model for mucociliary epithelial development. Dev. Biol. 312, 115-130.
21. Ishii, Y., Rex, M., Scotting, P. J. and Yasugi, S. (1998). Region-specific expression of chicken Sox2 in the developing gut and lung epithelium: regulation by epithelial-mesenchymal interactions. Dev. Dyn. 213, 464-475.
22. Ito, T., Udaka, N., Yazawa, T., Okudela, K., Hayashi, H., Sudo, T., Guillemot, F., Kageyama, R. and Kitamura, H. (2000). Basic helix-loop-helix transcription factors regulate the neuroendocrine differentiation of fetal mouse pulmonary epithelium. Development 127, 3913-3921.
23. Johnston, C. J., Finkelstein, J. N., Oberdörster, G., Reynolds, S. D. and Stripp, B. R. (1999). Clara cell secretory protein-deficient mice differ from wild-type mice in inflammatory chemokine expression to oxygen and ozone, but not to endotoxin. Exp. Lung Res. 25, 7-21.
24. Kiernan, A. E., Xu, J. and Gridley, T. (2006). The Notch ligand JAG1 is required for sensory progenitor development in the mammalian inner. PLoS Genet. 2, e4.
25. Kong, Y., Glickman, J., Subramaniam, M., Shahsafaei, A., Allamneni, K. P., Aster, J. C., Sklar, J. and Sunday, M. E. (2004). Functional diversity of notch family genes in fetal lung development. Am. J. Physiol. Lung Cell Mol. Physiol. 286, 1075-1083.
26. Kurotani, R., Tomita, T., Yang, Q., Carlson, B. A., Chen, C. and Kimura, S. (2008). Role of secretoglobin 3A2 in lung development. Am. J. Respir. Crit. Care Med. 178, 389-398.
27. Linnoila, R. I. (2006). Functional facets of the pulmonary neuroendocrine system. Lab. Invest. 86, 425-444.
28. Liu, Y., Pathak, N., Kramer-Zucker, A. and Drummond, I. A. (2007). Notch signaling controls the differentiation of transporting epithelia and multiciliated cells in the zebrafish pronephros. Development 134, 1111-1122.
29. Lü, J., Qian, J., Izvolsky, K. I. and Cardoso, W. V. (2004). Global analysis of genes differentially expressed in branching and non-branching regions of the mouse embryonic lung. Dev. Biol. 273, 418-435.
30. Maeda, Y., Davé, V. and Whitsett, J. A. (2007). Transcriptional control of lung morphogenesis. Physiol. Rev. 87, 219-244.
31. McDowell, E. M., Newkirk, C. and Coleman, B. (1985). Development of hamster tracheal epithelium: I. A quantitative morphologic study in the fetus. Anat. Rec. 213, 429-447.
32. Murtaugh, L. C., Stanger, B. Z., Kwan, K. M. and Melton, D. A. (2003). Notch signaling controls multiple steps of pancreatic differentiation. Proc. Natl. Acad. Sci. USA 100, 14920-14925.
33. Okajima, T. and Matsuda, T. (2006). Roles of O-fucosyltransferase 1 and O-linked fucose in notch receptor function. Methods Enzymol. 417, 111-126.
34. Okamura, Y. and Saga, Y. (2008). Notch signaling is required for the maintenance of enteric neural crest progenitors. Development 135, 3555-3565.
35. Otani, E. M., Newkirk, C. and McDowell, E. M. (1986). Development of hamster tracheal epithelium: IV. Cell proliferation and cytodifferentiation in the neonate. Anat. Rec. 214, 183-192.
36. Park, K. S., Wells, J. M., Zorn, A. M., Wert, S. E., Laubach, V. E., Fernandez, L. G. and Whitsett, J. A. (2006). Transdifferentiation of ciliated cells during repair of the respiratory epithelium. Am. J. Respir. Cell Mol. Biol. 34, 151-115.
37. Post, L. C., Ternet, M. and Hogan, B. L. (2000). Notch/Delta expression in the developing mouse lung. Mech. Dev. 98, 95-98.
38. Que, J., Okubo, T., Goldenring, J. R., Nam, K. T., Kurotani, R., Morrisey, E. E., Taranova, O., Pevny, L. H. and Hogan, B. L. (2007). Multiple dose-dependent roles for Sox2 in the patterning and differentiation of anterior foregut endoderm. Development 134, 2521-2531.
39. Radtke, F. and Raj, K. (2003). The role of Notch in tumorigenesis: oncogene or tumour suppressor? Nat. Rev. Cancer 3, 756-767.
40. Ramirez, M. I., Millien, G., Hinds, A., Cao, Y., Seldin, D. C. and Williams, M. C. (2003). T1alpha, a lung type I cell differentiation gene, is required for normal lung cell proliferation and alveolus formation at birth. Dev. Biol. 256, 61-72.
41. Rawlins, E. L. and Hogan, B. L. (2006). Epithelial stem cells of the lung: privileged few or opportunities for many? Development 133, 2455-2465.
42. Rawlins, E. L., Ostrowski, L. E., Randell, S. H. and Hogan, B. L. (2007). Lung development and repair: contribution of the ciliated lineage. Proc. Natl. Acad. Sci. USA 104, 410-417.
43. Reynolds, S. D., Reynolds, P. R., Pryhuber, G. S., Finder, J. D. and Stripp, B. R. (2002). Secretoblobins SCGB3A1 and SCGB3A2 define secretory cell subsets in mouse and human airways. Am. J. Respir. Crit. Care Med. 166, 1498-1509.
44. Rogers, D. F. (2003).The airway goblet cell. Int. J. Biochem. Cell Biol. 35, 1-6.
45. Sasamura, T., Ishikawa, H. O., Sasaki, N., Higashi, S., Kanai, M., Nakao, S., Ayukawa, T., Aigaki, T., Noda, K., Miyoshi, E. et al. (2007). The O-fucosyltransferase O-fut1 is an extracellular component that is essential for the constitutive endocytic trafficking of Notch in Drosophila. Development 134, 1347-1356.
46. Shan, L., Aster, J. C., Sklar, J. and Sunday, M. E. (2007). Notch-1 regulates pulmonary neuroendocrine cell differentiation in cell lines and in transgenic mice. Am. J. Physiol. Lung Cell Mol. Physiol. 292, 500-509.
47. Shi, S. and Stanley, P. (2003). Protein O-fucosyltransferase 1 is an essential component of Notch signaling pathways. Proc. Natl. Acad. Sci. USA 100, 5234-5239.
48. Shi, S., Stahl, M., Lu, L. and Stanley, P. (2005). Canonical Notch signaling is dispensable for early cell fate specifications in mammals. Mol. Cell. Biol. 225, 9503-9508.
49. Stripp, B. R., Maxson, K., Mera, R. and Singh, G. (1995). Plasticity of airway cell proliferation and gene expression after acute naphthalene injury. Am. J. Physiol. 269, 791-799.
50. Stripp, B. R., Reynolds, S. D., Boe, I. M., Lund, J., Power, J. H., Coppens, J. T., Wong, V., Reynolds, P. R. and Plopper, C. G. (2002). Clara cell secretory protein deficiency alters clara cell secretory apparatus and the protein composition of airway lining fluid. Am. J. Respir. Cell Mol. Biol. 27, 170-178.
51. Stubbs, J. L., Davidson, L., Keller, R. and Kintner, C. (2006). Radial intercalation of ciliated cells during Xenopus skin development. Development 133, 2507-2515.
52. Tilley, A. E., Harvey, B. G., Heguy, A., Hackett, N. R., Wang, R., O'Connor, T. P. and Crystal, R. G. (2009). Downregulation of the notch pathway in human airway epithelium in association with smoking and COPD. Am. J. Respir. Crit. Care Med. 179, 457-466.
53. Toskala, E., Smiley-Jewell, S. M., Wong, V. J., King, D. and Plopper, C. G. (2005). Temporal and spatial distribution of ciliogenesis in the tracheobronchial airways of mice. Am. J. Physiol. Lung Cell Mol. Physiol. 283, 454-459.
54. Tsao, P. N., Chen, F., Izvolsky, K. I., Walker, J., Kukuruzinska, M. A., Lu, J. and Cardoso, W. V. (2008). Gamma-secretase activation of notch signaling regulates the balance of proximal and distal fates in progenitor cells of the developing lung. J. Biol. Chem. 283, 29532-29544.
55. van Es, J. H., van Gijn, M. E., Riccio, O., van den Born, M., Vooijs, M., Begthel, H., Cozijnsen, M., Robine, S., Winton, D. J., Radtke, F. et al. (2005). Notch/gamma-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Nature 435, 959-963.
56. van Tuyl, M., Groenman, F., Kuliszewski, M., Ridsdale, R., Wang, J., Tibboel, D. and Post, M. (2005). Overexpression of lunatic fringe does not affect epithelial cell differentiation in the developing mouse lung. Am. J. Physiol. Lung Cell Mol. Physiol. 288, 672-682.
57. Warburton, D., Perin, L., Defilippo, R., Bellusci, S., Shi, W. and Driscoll, B. (2008). Stem/progenitor cells in lung development, injury repair, and regeneration. Proc. Am. Thorac. Soc. 15, 703-706.
58. Weibel, E. R. (1984). Lung cell biology. In The Pathway for Oxygen: Structure and Function in the Mammalian Respiratory System, pp. 231-233. Cambridge, MA: Harvard University Press.
59. Weinmaster, G. and Kopan, R. (2006). A garden of Notch-ly delight. Development 33, 3277-3282.
60. Wettstein, D. A., Turner, D. L. and Kintner, C. (1997). The Xenopus homolog of Drosophila Suppressor of Hairless mediates Notch signaling during primary neurogenesis. Development 124, 693-702.
61. Zemke, A. C., Snyder, J. C., Brockway, B. L., Drake, J. A., Reynolds, S. D., Kaminski, N. and Stripp, B. R. (2009). Molecular staging of epithelial maturation using secretory cell-specific genes as markers. Am. J. Respir. Cell Mol. Biol. 40, 340-348.