Insulin-like growth factors are expressed in the taste system, but do not maintain adult taste buds

PLoS ONE

Volumn 11, Issue 2, 2016, Pages

  Biggs, Bradley T ^a   Tang, Tao ^a   Krimm, Robin F ^a  

^a University of Louisville School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBONATE DEHYDRATASE IV; CYTOKERATIN 14; PHOSPHOLIPASE C BETA2; SOMATOMEDIN B; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; SOMATOMEDIN; SOMATOMEDIN B RECEPTOR; SOMATOMEDIN RECEPTOR;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CONTROLLED STUDY; FACIAL NERVE; GENOTYPE; MOUSE; NONHUMAN; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; TASTE; TASTE BUD; TONGUE; TONGUE EPITHELIUM; ANIMAL; GENICULATE GANGLION; IMMUNOHISTOCHEMISTRY; LASER CAPTURE MICRODISSECTION; METABOLISM; REAL TIME POLYMERASE CHAIN REACTION;

ANIMALS; GENICULATE GANGLION; IMMUNOHISTOCHEMISTRY; LASER CAPTURE MICRODISSECTION; MICE; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR, IGF TYPE 1; RECEPTOR, IGF TYPE 2; RECEPTORS, SOMATOMEDIN; SOMATOMEDINS; TASTE BUDS; TONGUE;

EID: 84960936148     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0148315     Document Type: Article

References (52)

1. Beidler LM, Smallman RL. Renewal of cells within taste buds. J Cell Biol. 1965; 27(2):263-72. PMID: 5884625; PubMed Central PMCID: PMC2106718.
2. Perea-Martinez I, Nagai T, Chaudhari N. Functional cell types in taste buds have distinct longevities. PLoS One. 2013; 8(1):e53399. doi: 10.1371/journal.pone.0053399 PMID: 23320081; PubMed Central PMCID: PMC3540047.
3. Sullivan JM, Borecki AA, Oleskevich S. Stem and progenitor cell compartments within adult mouse taste buds. The European journal of neuroscience. 2010; 31(9):1549-60. doi: 10.1111/j.1460-9568. 2010.07184.x PMID: 20525068.
4. Finger TE. Cell types and lineages in taste buds. Chem Senses. 2005; 30 Suppl 1:i54-5. doi: 10.1093/chemse/bjh110 PMID: 15738192.
5. Murray RG, Murray A. Fine structure of taste buds of rabbit foliate papillae. J Ultrastruct Res. 1967; 19 (3):327-53. PMID: 6053017.
6. Yang R, Crowley HH, Rock ME, Kinnamon JC. Taste cells with synapses in rat circumvallate papillae display SNAP-25-like immunoreactivity. The Journal of comparative neurology. 2000; 424(2):205-15. Epub 2000/07/25. doi: 10.1002/1096-9861(20000821)424:2<205::AID-CNE2>3.0.CO;2-F [pii]. PMID: 10906698.
7. Yang R, Tabata S, Crowley HH, Margolskee RF, Kinnamon JC. Ultrastructural localization of gustducin immunoreactivity in microvilli of type II taste cells in the rat. The Journal of comparative neurology. 2000; 425(1):139-51. PMID: 10940948.
8. Kapsimali M, Barlow LA. Developing a sense of taste. Semin Cell Dev Biol. 2013; 24(3):200-9. doi: 10.1016/j.semcdb.2012.11.002 PMID: 23182899; PubMed Central PMCID: PMC3604069.
9. Ito A, Nosrat CA. Gustatory papillae and taste bud development and maintenance in the absence of TrkB ligands BDNF and NT-4. Cell Tissue Res. 2009; 337(3):349-59. PMID: 19629530. doi: 10.1007/s00441-009-0833-7
10. Ma L, Lopez GF, Krimm RF. Epithelial-derived brain-derived neurotrophic factor is required for gustatory neuron targeting during a critical developmental period. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2009; 29(11):3354-64. PMID: 19295142.
11. Nosrat CA, Ebendal T, Olson L. Differential expression of brain-derived neurotrophic factor and neurotrophin 3 mRNA in lingual papillae and taste buds indicates roles in gustatory and somatosensory innervation. The Journal of comparative neurology. 1996; 376(4):587-602. PMID: 8978472.
12. Guth L. The effects of glossopharyngeal nerve transection on the circumvallate papilla of the rat. Anat Rec. 1957; 128(4):715-31. PMID: 13478886.
13. Mistretta CM. The role of innervation in induction and differentiation of taste organs: introduction and background. Ann N Y Acad Sci. 1998; 855:1-13. Epub 1999/02/04. PMID: 9929582.
14. Oakley B, Witt M. Building sensory receptors on the tongue. J Neurocytol. 2004; 33(6):631-46. PMID: 16217619.
15. McLaughlin SK. Erb and c-Kit receptors have distinctive patterns of expression in adult and developing taste papillae and taste buds. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2000; 20(15):5679-88. PMID: 10908606.
16. Suzuki Y, Takeda M, Sakakura Y, Suzuki N. Distinct expression pattern of insulin-like growth factor family in rodent taste buds. The Journal of comparative neurology. 2005; 482(1):74-84. doi: 10.1002/cne.20379 PMID: 15612015.
17. Huang T, Krimm RF. Developmental expression of Bdnf, Ntf4/5, and TrkB in the mouse peripheral taste system. Dev Dyn. 2010; 239(10):2637-46. Epub 2010/11/03. doi: 10.1002/dvdy.22412 PMID: 21038447.
18. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001; 25(4):402-8. Epub 2002/02/16. doi: 10.1006/meth.2001.1262 S1046-2023(01)91262-9 [pii]. PMID: 11846609.
19. Huang T, Krimm RF. BDNF and NT4 play interchangeable roles in gustatory development. Dev Biol. 2014; 386(2):308-20. Epub 2014/01/01. doi: 10.1016/j.ydbio.2013.12.031 PMID: 24378336.
20. Harlow DE, Yang H, Williams T, Barlow LA. Epibranchial placode-derived neurons produce BDNF required for early sensory neuron development. Dev Dyn. 2011; 240(2):309-23. Epub 2011/01/20. doi: 10.1002/dvdy.22527 PMID: 21246648; PubMed Central PMCID: PMC3070660.
21. Oakley B, Wu LH, Lawton A, de Sibour C. Neural control of ectopic filiform spines in adult tongue. Neuroscience. 1990; 36(3):831-8. PMID: 2234415.
22. Okubo T, Clark C, Hogan BL. Cell lineage mapping of taste bud cells and keratinocytes in the mouse tongue and soft palate. Stem Cells. 2009; 27(2):442-50. Epub 2008/11/29. doi: stemcells.2008-0611 [pii]doi: 10.1634/stemcells.2008-0611 PMID: 19038788.
23. Yee KK, Li Y, Redding KM, Iwatsuki K, Margolskee RF, Jiang P. Lgr5-EGFP marks taste bud stem/progenitor cells in posterior tongue. Stem Cells. 2013; 31(5):992-1000. doi: 10.1002/stem.1338 PMID: 23377989; PubMed Central PMCID: PMC3637415.
24. Liebl DJ, Mbiene JP, Parada LF. NT4/5 mutant mice have deficiency in gustatory papillae and taste bud formation. Dev Biol. 1999; 213(2):378-89. PMID: 10479455.
25. Patel AV, Krimm RF. Neurotrophin-4 regulates the survival of gustatory neurons earlier in development using a different mechanism than brain-derived neurotrophic factor. Dev Biol. 2012; 365(1):50-60. Epub 2012/02/23. doi: 10.1016/j.ydbio.2012.02.008 PMID: 22353733.
26. Zhang Y, Hoon MA, Chandrashekar J, Mueller KL, Cook B, Wu D, et al. Coding of sweet, bitter, and umami tastes: different receptor cells sharing similar signaling pathways. Cell. 2003; 112(3):293-301. PMID: 12581520.
27. Chandrashekar J, Yarmolinsky D, von Buchholtz L, Oka Y, Sly W, Ryba NJ, et al. The taste of carbonation. Science. 2009; 326(5951):443-5. Epub 2009/10/17. doi: 10.1126/science.1174601 PMID: 19833970; PubMed Central PMCID: PMC3654389.
28. Stachelscheid H, Ibrahim H, Koch L, Schmitz A, Tscharntke M, Wunderlich FT, et al. Epidermal insulin/IGF-1 signalling control interfollicular morphogenesis and proliferative potential through Rac activation. EMBO J. 2008; 27(15):2091-101. doi: 10.1038/emboj.2008.141 PMID: 18650937; PubMed Central PMCID: PMC2516889.
29. Nosrat IV, Agerman K, Marinescu A, Ernfors P, Nosrat CA. Lingual deficits in neurotrophin double knockout mice. J Neurocytol. 2004; 33(6):607-15. PMID: 16217617.
30. Patel AV, Krimm RF. BDNF is required for the survival of differentiated geniculate ganglion neurons. Dev Biol. 2010; 340(2):419-29. Epub 2010/02/04. doi: S0012-1606(10)00053-9 [pii]doi: 10.1016/j. ydbio.2010.01.024 PMID: 20122917; PubMed Central PMCID: PMC2854215.
31. Sun H, Oakley B. Development of anterior gustatory epithelia in the palate and tongue requires epidermal growth factor receptor. Dev Biol. 2002; 242(1):31-43. PMID: 11795938.
32. Liu HX, Henson BS, Zhou Y, D'Silva NJ, Mistretta CM. Fungiform papilla pattern: EGF regulates interpapilla lingual epithelium and decreases papilla number by means of PI3K/Akt, MEK/ERK, and p38 MAPK signaling. Dev Dyn. 2008; 237(9):2378-93. doi: 10.1002/dvdy.21657 PMID: 18729215; PubMed Central PMCID: PMC2775556.
33. Petersen CI, Jheon AH, Mostowfi P, Charles C, Ching S, Thirumangalathu S, et al. FGF signaling regulates the number of posterior taste papillae by controlling progenitor field size. PLoS Genet. 2011; 7(6): e1002098. doi: 10.1371/journal.pgen.1002098 PMID: 21655085; PubMed Central PMCID: PMC3107195.
34. Gaillard D, Xu M, Liu F, Millar SE, Barlow LA. beta-Catenin Signaling Biases Multipotent Lingual Epithelial Progenitors to Differentiate and Acquire Specific Taste Cell Fates. PLoS Genet. 2015; 11(5): e1005208. doi: 10.1371/journal.pgen.1005208 PMID: 26020789; PubMed Central PMCID: PMC4447363.
35. Miura H, Scott JK, Harada S, Barlow LA. Sonic hedgehog-expressing basal cells are general postmitotic precursors of functional taste receptor cells. Dev Dyn. 2014; 243(10):1286-97. doi: 10.1002/dvdy.24121 PMID: 24590958; PubMed Central PMCID: PMC4152395.
36. Liu HX, Grosse AS, Iwatsuki K, Mishina Y, Gumucio DL, Mistretta CM. Separate and distinctive roles for Wnt5a in tongue, lingual tissue and taste papilla development. Dev Biol. 2012; 361(1):39-56. doi: 10.1016/j.ydbio.2011.10.009 PMID: 22024319; PubMed Central PMCID: PMC3465690.
37. Liu F, Thirumangalathu S, Gallant NM, Yang SH, Stoick-Cooper CL, Reddy ST, et al. Wnt-beta-catenin signaling initiates taste papilla development. Nat Genet. 2007; 39(1):106-12. PMID: 17128274.
38. Liu HX, Ermilov A, Grachtchouk M, Li L, Gumucio DL, Dlugosz AA, et al. Multiple Shh signaling centers participate in fungiform papilla and taste bud formation and maintenance. Dev Biol. 2013; 382(1):82-97. doi: 10.1016/j.ydbio.2013.07.022 PMID: 23916850; PubMed Central PMCID: PMC3968530.
39. Iwatsuki K, Liu HX, Gronder A, Singer MA, Lane TF, Grosschedl R, et al. Wnt signaling interacts with Shh to regulate taste papilla development. Proc Natl Acad Sci U S A. 2007; 104(7):2253-8. PMID: 17284610.
40. Barlow LA, Northcutt RG. Embryonic origin of amphibian taste buds. Dev Biol. 1995; 169(1):273-85. doi: 10.1006/dbio.1995.1143 PMID: 7750643.
41. Annenkov A. The insulin-like growth factor (IGF) receptor type 1 (IGF1R) as an essential component of the signalling network regulating neurogenesis. Mol Neurobiol. 2009; 40(3):195-215. doi: 10.1007/s12035-009-8081-0 PMID: 19714501.
42. Chao W, D'Amore PA. IGF2: epigenetic regulation and role in development and disease. Cytokine Growth Factor Rev. 2008; 19(2):111-20. doi: 10.1016/j.cytogfr.2008.01.005 PMID: 18308616; PubMed Central PMCID: PMC2314671.
43. Clapp TR, Medler KF, Damak S, Margolskee RF, Kinnamon SC. Mouse taste cells with G protein-coupled taste receptors lack voltage-gated calcium channels and SNAP-25. BMC Biol. 2006; 4:7. Epub 2006/04/01. 1741-7007-4-7 [pii]doi: 10.1186/1741-7007-4-7 PMID: 16573824; PubMed Central PMCID: PMC1444931.
44. Clapp TR, Yang R, Stoick CL, Kinnamon SC, Kinnamon JC. Morphologic characterization of rat taste receptor cells that express components of the phospholipase C signaling pathway. The Journal of comparative neurology. 2004; 468(3):311-21. doi: 10.1002/cne.10963 PMID: 14681927.
45. Delay RJ, Kinnamon JC, Roper SD. Ultrastructure of mouse vallate taste buds: II. Cell types and cell lineage. The Journal of comparative neurology. 1986; 253(2):242-52. PMID: 3793992.
46. Kataoka S, Yang R, Ishimaru Y, Matsunami H, Sevigny J, Kinnamon JC, et al. The candidate sour taste receptor, PKD2L1, is expressed by type III taste cells in the mouse. Chem Senses. 2008; 33(3):243-54. Epub 2007/12/25. bjm083 [pii]doi: 10.1093/chemse/bjm083 PMID: 18156604; PubMed Central PMCID: PMC2642677.
47. Murray RG, Murray A, Fujimoto S. Fine structure of gustatory cells in rabbit taste buds. J Ultrastruct Res. 1969; 27(5):444-61. PMID: 5803342.
48. Yee CL, Yang R, Bottger B, Finger TE, Kinnamon JC. "Type III" cells of rat taste buds: immunohistochemical and ultrastructural studies of neuron-specific enolase, protein gene product 9.5, and serotonin. The Journal of comparative neurology. 2001; 440(1):97-108. PMID: 11745610.
49. Lopez GF, Krimm RF. Refinement of innervation accuracy following initial targeting of peripheral gustatory fibers. J Neurobiol. 2006; 66(10):1033-43. PMID: 16838366.
50. Patel AV, Huang T, Krimm RF. Lingual and palatal gustatory afferents each depend on both BDNF and NT-4, but the dependence is greater for lingual than palatal afferents. The Journal of comparative neurology. 2010; 518(16):3290-301. Epub 2010/06/25. doi: 10.1002/cne.22400 PMID: 20575060.
51. Mistretta CM, Gurkan S, Bradley RM. Morphology of chorda tympani fiber receptive fields and proposed neural rearrangements during development. The Journal of neuroscience: the official journal of the Society for Neuroscience. 1988; 8(1):73-8. PMID: 3339420.
52. Collings VB. Human taste response as a function of locus of stimulation on the tongue and soft plate. Perception and Psychophysics. 1974; 16(1):169-74.