Transcriptome analyses of taste organoids reveal multiple pathways involved in taste cell generation

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Ren, Wenwen ^a   Aihara, Eitaro ^b   Lei, Weiwei ^a   Gheewala, Nishi ^a   Uchiyama, Hironobu ^c   Margolskee, Robert F ^a   Iwatsuki, Ken ^c   Jiang, Peihua ^a  

^a MONELL CHEMICAL SENSES CENTER   (United States)

^b UNIVERSITY OF CINCINNATI   (United States)

^c TOKYO UNIVERSITY OF AGRICULTURE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; G PROTEIN COUPLED RECEPTOR; NOTCH RECEPTOR; SONIC HEDGEHOG PROTEIN; TRANSCRIPTOME; WNT PROTEIN;

ANIMAL; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; GENE EXPRESSION REGULATION; GENETICS; MALE; METABOLISM; MOUSE; ORGANOID; SIGNAL TRANSDUCTION; STEM CELL; TASTE;

ANIMALS; BONE MORPHOGENETIC PROTEINS; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; GENE EXPRESSION REGULATION; HEDGEHOG PROTEINS; MALE; MICE; ORGANOIDS; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; STEM CELLS; TASTE; TASTE PERCEPTION; TRANSCRIPTOME; WNT PROTEINS;

EID: 85021230867     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-04099-5     Document Type: Article

References (49)

1. Bachmanov, A. A. & Beauchamp, G. K. Taste receptor genes. Annu Rev Nutr 27, 389-414 (2007).
2. Yarmolinsky, D. A., Zuker, C. S. & Ryba, N. J. Common sense about taste: from mammals to insects. Cell 139, 234-244 (2009).
3. Barlow, L. A. Toward a unified model of vertebrate taste bud development. J Comp Neurol 457, 107-110 (2003).
4. Miura, H., Scott, J. K., Harada, S. & Barlow, L. A. Sonic hedgehog-expressing basal cells are general post-mitotic precursors of functional taste receptor cells. Dev Dyn 243, 1286-1297 (2014).
5. Chaudhari, N. & Roper, S. D. The cell biology of taste. J Cell Biol 190, 285-296 (2010).
6. Hamamichi, R., Asano-Miyoshi, M. & Emori, Y. Taste bud contains both short-lived and long-lived cell populations. Neuroscience 141, 2129-2138 (2006).
7. Beidler, L. M. & Smallman, R. L. Renewal of cells within taste buds. J Cell Biol 27, 263-272 (1965).
8. Perea-Martinez, I., Nagai, T. & Chaudhari, N. Functional cell types in taste buds have distinct longevities. PLoS One 8, e53399 (2013).
9. Yee, K. K. et al. Lgr5-EGFP marks taste bud stem/progenitor cells in posterior tongue. Stem Cells 31, 992-1000 (2013).
10. Takeda, N. et al. Lgr5 identifies progenitor cells capable of taste bud regeneration after injury. PLoS One 8, e66314 (2013).
11. Ren, W. et al. Single Lgr5- or Lgr6-expressing taste stem/progenitor cells generate taste bud cells ex vivo. Proc Natl Acad Sci USA 111, 16401-16406 (2014).
12. Aihara, E. et al. Characterization of stem/progenitor cell cycle using murine circumvallate papilla taste bud organoid. Sci Rep 5, 17185 (2015).
13. Gaillard, D., Xu, M., Liu, F., Millar, S. E. & Barlow, L. A. Beta-catenin signaling biases multipotent lingual epithelial progenitors to differentiate and acquire specific taste cell fates. PLoS Genet 11, e1005208 (2015).
14. Thirumangalathu, S. & Barlow, L. A. Beta-catenin signaling regulates temporally discrete phases of anterior taste bud development. Development 142, 4309-4317 (2015).
15. Liu, H. X. et al. Multiple Shh signaling centers participate in fungiform papilla and taste bud formation and maintenance. Dev Biol 382, 82-97 (2013).
16. Barlow, L. A. & Klein, O. D. Developing and regenerating a sense of taste. Curr Top Dev Biol 111, 401-419 (2015).
17. Castillo, D. et al. Induction of ectopic taste buds by SHH reveals the competency and plasticity of adult lingual epithelium. Development 141, 2993-3002 (2014).
18. Kumari, A. et al. Hedgehog pathway blockade with the cancer drug LDE225 disrupts taste organs and taste sensation. J Neurophysiol 113, 1034-1040 (2015).
19. Yang, H., Cong, W. N., Yoon, J. S. & Egan, J. M. Vismodegib, an antagonist of hedgehog signaling, directly alters taste molecular signaling in taste buds. Cancer Med 4, 245-252 (2015).
20. McLaughlin, S. K., McKinnon, P. J. & Margolskee, R. F. Gustducin is a taste-cell-specific G protein closely related to the transducins. Nature 357, 563-569 (1992).
21. Chandrashekar, J. et al. The taste of carbonation. Science 326, 443-445 (2009).
22. Zhang, Z., Zhao, Z., Margolskee, R. & Liman, E. The transduction channel TRPM5 is gated by intracellular calcium in taste cells. J Neurosci 27, 5777-5786 (2007).
23. Clapp, T. R., Medler, K. F., Damak, S., Margolskee, R. F. & Kinnamon, S. C. Mouse taste cells with G protein-coupled taste receptors lack voltage-gated calcium channels and SNAP-25. BMC Biol 4, 7 (2006).
24. Chattopadhyaya, B. et al. Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period. J Neurosci 24, 9598-9611 (2004).
25. Tomchik, S. M., Berg, S., Kim, J. W., Chaudhari, N. & Roper, S. D. Breadth of tuning and taste coding in mammalian taste buds. J Neurosci 27, 10840-10848 (2007).
26. Hisha, H. et al. Establishment of a novel lingual organoid culture system: generation of organoids having mature keratinized epithelium from adult epithelial stem cells. Sci Rep 3, 3224 (2013).
27. Huang da, W., Sherman, B. T. & Lempicki, R. A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4, 44-57 (2009).
28. Huang da, W., Sherman, B. T. & Lempicki, R. A. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37, 1-13 (2009).
29. Fernandes, A. D., Macklaim, J. M., Linn, T. G., Reid, G. & Gloor, G. B. ANOVA-like differential expression (ALDEx) analysis for mixed population RNA-Seq. PLoS One 8, e67019 (2013).
30. Gaillard, D. & Barlow, L. A. Taste bud cells of adult mice are responsive to Wnt/beta-catenin signaling: implications for the renewal of mature taste cells. Genesis 49, 295-306 (2011).
31. Zhou, Y., Liu, H. X. & Mistretta, C. M. Bone morphogenetic proteins and noggin: inhibiting and inducing fungiform taste papilla development. Dev Biol 297, 198-213 (2006).
32. Seta, Y., Seta, C. & Barlow, L. A. Notch-associated gene expression in embryonic and adult taste papillae and taste buds suggests a role in taste cell lineage decisions. J Comp Neurol 464, 49-61 (2003).
33. Grinspan, J. B. Bone morphogenetic proteins: inhibitors of myelination in development and disease. Vitam Horm 99, 195-222 (2015).
34. Sato, T. et al. Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett's epithelium. Gastroenterology 141, 1762-1772 (2011).
35. Milano, J. et al. Modulation of notch processing by gamma-secretase inhibitors causes intestinal goblet cell metaplasia and induction of genes known to specify gut secretory lineage differentiation. Toxicol Sci 82, 341-358 (2004).
36. van Es, J. H. et al. Notch/gamma-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Nature 435, 959-963 (2005).
37. Benvenuto, M. et al. In vitro and in vivo inhibition of breast cancer cell growth by targeting the Hedgehog/GLI pathway with SMO (GDC-0449) or GLI (GANT-61) inhibitors. Oncotarget (2016).
38. Thirumangalathu, S., Harlow, D. E., Driskell, A. L., Krimm, R. F. & Barlow, L. A. Fate mapping of mammalian embryonic taste bud progenitors. Development 136, 1519-1528 (2009).
39. Iwatsuki, K. et al. Wnt signaling interacts with Shh to regulate taste papilla development. Proc Natl Acad Sci USA 104, 2253-2258 (2007).
40. Jiang, H. L., Jiang, L. M. & Han, W. D. Wnt/beta-catenin signaling pathway in lung cancer stem cells is a potential target for the development of novel anticancer drugs. J BUON 20, 1094-1100 (2015).
41. Wang, R. et al. Notch and Wnt/beta-catenin signaling pathway play important roles in activating liver cancer stem cells. Oncotarget (2015).
42. Maimets, M. et al. Long-Term In Vitro Expansion of Salivary Gland Stem Cells Driven by Wnt Signals. Stem Cell Reports 6, 150-162 (2016).
43. Borggrefe, T. et al. The Notch intracellular domain integrates signals from Wnt, Hedgehog, TGFbeta/BMP and hypoxia pathways. Biochim Biophys Acta 1863, 303-313 (2016).
44. Seta, Y., Toyono, T., Kataoka, S. & Toyoshima, K. Regulation of taste bud cell differentiation by notch signaling pathway. Chem Senses 30(Suppl 1), i48-49 (2005).
45. Hevezi, P. et al. Genome-wide analysis of gene expression in primate taste buds reveals links to diverse processes. PLoS One 4, e6395 (2009).
46. Rossier, O. et al. Analysis of a human fungiform papillae cDNA library and identification of taste-related genes. Chem Senses 29, 13-23 (2004).
47. Hoon, M. A. et al. Putative mammalian taste receptors: a class of taste-specific GPCRs with distinct topographic selectivity. Cell 96, 541-551 (1999).
48. Lossow, K. et al. Comprehensive analysis of mouse bitter taste receptors reveals different molecular receptive ranges for orthologous receptors in mice and humans. J Biol Chem 291, 15358-15377 (2016).
49. Schumacher, M. A. et al. The use of murine-derived fundic organoids in studies of gastric physiology. J Physiol 593, 1809-1827 (2015).