Taste neurons consist of both a large TrkB-receptor-dependent and a small TrkB-receptor-independent subpopulation

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Fei, Da ^a   Krimm, Robin F ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL SURVIVAL; FEMALE; GENE EXPRESSION; GENICULATE GANGLION; MICE; MICE, KNOCKOUT; NERVE GROWTH FACTORS; NEURONS; RECEPTOR, TRKB; RECEPTORS, PURINERGIC P2X3; TASTE BUDS;

EID: 84893566100     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0083460     Document Type: Article

References (60)

1. Conover JC, Erickson JT, Katz DM, Bianchi LM, Poueymirou WT, et al. (1995) Neuronal deficits, not involving motor neurons, in mice lacking BDNF and/or NT4. Nature 375: 235-238.
2. Liu X, Ernfors P, Wu H, Jaenisch R (1995) Sensory but not motor neuron deficits in mice lacking NT4 and BDNF. Nature 375: 238-241.
3. Patel AV, Krimm RF (2012) Neurotrophin-4 regulates the survival of gustatory neurons earlier in development using a different mechanism than brain-derived neurotrophic factor. Dev Biol 365: 50-60.
4. Hoshino N, Vatterott P, Egwiekhor A, Rochlin MW (2010) Brain-derived neurotrophic factor attracts geniculate ganglion neurites during embryonic targeting. Dev Neurosci 32: 184-196.
5. Ma L, Lopez GF, Krimm RF (2009) Epithelial-derived brain-derived neurotrophic factor is required for gustatory neuron targeting during a critical developmental period. J Neurosci 29: 3354-3364.
6. Mistretta CM, Goosens KA, Farinas I, Reichardt LF (1999) Alterations in size, number, and morphology of gustatory papillae and taste buds in BDNF null mutant mice demonstrate neural dependence of developing taste organs. J Comp Neurol 409: 13-24. (Pubitemid 29242782)
7. Nosrat CA, Blomlof J, ElShamy WM, Ernfors P, Olson L (1997) Lingual deficits in BDNF and NT3 mutant mice leading to gustatory and somatosensory disturbances, respectively. Development 124: 1333-1342. (Pubitemid 27190106)
8. Oakley B, Brandemihl A, Cooper D, Lau D, Lawton A, et al. (1998) The morphogenesis of mouse vallate gustatory epithelium and taste buds requires BDNF-dependent taste neurons. Brain Res Dev Brain Res 105: 85-96. (Pubitemid 28068136)
9. Chao MV (2003) Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat Rev Neurosci 4: 299-309.
10. Huang EJ, Reichardt LF (2003) TRK Receptors: Roles in Neuronal Signal Transduction. Annu Rev Biochem.
11. Fritzsch B, Sarai PA, Barbacid M, Silos-Santiago I (1997) Mice with a targeted disruption of the neurotrophin receptor trkB lose their gustatory ganglion cells early but do develop taste buds. Int J Dev Neurosci 15: 563-576. (Pubitemid 27332106)
12. Patel AV, Huang T, Krimm RF (2010) Lingual and palatal gustatory afferents each depend on both BDNF and NT-4, but the dependence is greater for lingual than palatal afferents. J Comp Neurol 518: 3290-3301.
13. Ito A, Nosrat CA (2009) Gustatory papillae and taste bud development and maintenance in the absence of TrkB ligands BDNF and NT-4. Cell Tissue Res 337: 349-359.
14. Li L, Rutlin M, Abraira VE, Cassidy C, Kus L, et al. (2011) The functional organization of cutaneous low-threshold mechanosensory neurons. Cell 147: 1615-1627.
15. Patel AV, Krimm RF (2010) BDNF is required for the survival of differentiated geniculate ganglion neurons. Dev Biol 340: 419-429.
16. Abercrombie M (1946) Estimation of nuclear population from microtome sections. Anat Rec 94: 239-247.
17. Krimm RF, Miller KK, Kitzman PH, Davis BM, Albers KM (2001) Epithelial overexpression of BDNF or NT4 disrupts targeting of taste neurons that innervate the anterior tongue. Dev Biol 232: 508-521. (Pubitemid 32337111)
18. Nagato T, Matsumoto K, Tanioka H, Kodama J, Toh H (1995) Effect of denervation on morphogenesis of the rat fungiform papilla. Acta Anat (Basel) 153: 301-309. (Pubitemid 26066798)
19. Sollars SI (2005) Chorda tympani nerve transection at different developmental ages produces differential effects on taste bud volume and papillae morphology in the rat. J Neurobiol 64: 310-320.
20. Sollars SI, Smith PC, Hill DL (2002) Time course of morphological alterations of fungiform papillae and taste buds following chorda tympani transection in neonatal rats. J Neurobiol 51: 223-236. (Pubitemid 34477657)
21. Nosrat IV, Agerman K, Marinescu A, Ernfors P, Nosrat CA (2004) Lingual deficits in neurotrophin double knockout mice. J Neurocytol 33: 607-615. (Pubitemid 41434135)
22. Hosley MA, Hughes SE, Morton LL, Oakley B (1987) A sensitive period for the neural induction of taste buds. J Neurosci 7: 2075-2080.
23. Hosley MA, Hughes SE, Oakley B (1987) Neural induction of taste buds. J Comp Neurol 260: 224-232.
24. Hosley MA, Oakley B (1987) Postnatal development of the vallate papilla and taste buds in rats. Anat Rec 218: 216-222. (Pubitemid 17105213)
25. Finger TE, Danilova V, Barrows J, Bartel DL, Vigers AJ, et al. (2005) ATP signaling is crucial for communication from taste buds to gustatory nerves. Science 310: 1495-1499. (Pubitemid 41746346)
26. Ishida Y, Ugawa S, Ueda T, Yamada T, Shibata Y, et al. (2009) P2X(2)- and P2X(3)-positive fibers in fungiform papillae originate from the chorda tympani but not the trigeminal nerve in rats and mice. J Comp Neurol 514: 131-144.
27. Lopez GF, Krimm RF (2006) Refinement of innervation accuracy following initial targeting of peripheral gustatory fibers. J Neurobiol 66: 1033-1043. (Pubitemid 44264929)
28. Ninkina N, Adu J, Fischer A, Pinon LG, Buchman VL, et al. (1996) Expression and function of TrkB variants in developing sensory neurons. Embo J 15: 6385-6393. (Pubitemid 26413771)
29. Luikart BW, Nef S, Shipman T, Parada LF (2003) In vivo role of truncated trkb receptors during sensory ganglion neurogenesis. Neuroscience 117: 847-858. (Pubitemid 36332303)
30. Escandon E, Soppet D, Rosenthal A, Mendoza-Ramirez JL, Szonyi E, et al. (1994) Regulation of neurotrophin receptor expression during embryonic and postnatal development. J Neurosci 14: 2054-2068. (Pubitemid 24108115)
31. Klein R, Smeyne RJ, Wurst W, Long LK, Auerbach BA, et al. (1993) Targeted disruption of the trkB neurotrophin receptor gene results in nervous system lesions and neonatal death. Cell 75: 113-122. (Pubitemid 23306025)
32. Al-Hadlaq SM, Bradley RM, MacCallum DK, Mistretta CM (2003) Embryonic geniculate ganglion neurons in culture have neurotrophin-specific electrophysiological properties. Neuroscience 118: 145-159. (Pubitemid 36369539)
33. Harlow DE, Yang H, Williams T, Barlow LA (2011) Epibranchial placodederived neurons produce BDNF required for early sensory neuron development. Dev Dyn 240: 309-323.
34. Sun H, Oakley B (2002) Development of anterior gustatory epithelia in the palate and tongue requires epidermal growth factor receptor. Dev Biol 242: 31-43. (Pubitemid 34113668)
35. Thirumangalathu S, Harlow DE, Driskell AL, Krimm RF, Barlow LA (2009) Fate mapping of mammalian embryonic taste bud progenitors. Development 136: 1519-1528.
36. Zaidi FN, Krimm RF, Whitehead MC (2007) Exuberant neuronal convergence onto reduced taste bud targets with preservation of neural specificity in mice overexpressing neurotrophin in the tongue epithelium. J Neurosci 27: 13875-13881. (Pubitemid 350278269)
37. Farinas I, Wilkinson GA, Backus C, Reichardt LF, Patapoutian A (1998) Characterization of neurotrophin and Trk receptor functions in developing sensory ganglia: direct NT-3 activation of TrkB neurons in vivo. Neuron 21: 325-334. (Pubitemid 28399693)
38. Fan L, Girnius S, Oakley B (2004) Support of trigeminal sensory neurons by nonneuronal p75 neurotrophin receptors. Brain Res Dev Brain Res 150: 23-39. (Pubitemid 39090080)
39. Nosrat CA, Ebendal T, Olson L (1996) Differential expression of brain-derived neurotrophic factor and neurotrophin 3 mRNA in lingual papillae and taste buds indicates roles in gustatory and somatosensory innervation. J Comp Neurol 376: 587-602.
40. Nosrat CA, Olson L (1995) Brain-derived neurotrophic factor mRNA is expressed in the developing taste bud-bearing tongue papillae of rat. J Comp Neurol 360: 698-704.
41. ElShamy WM, Ernfors P (1997) Brain-derived neurotrophic factor, neurotrophin-3, and neurotrophin-4 complement and cooperate with each other sequentially during visceral neuron development. J Neurosci 17: 8667-8675.
42. Farinas I, Jones KR, Backus C, Wang XY, Reichardt LF (1994) Severe sensory and sympathetic deficits in mice lacking neurotrophin-3. Nature 369: 658-661. (Pubitemid 24199470)
43. Liebl DJ, Tessarollo L, Palko ME, Parada LF (1997) Absence of sensory neurons before target innervation in brain-derived neurotrophic factor-, neurotrophin 3-, and TrkC-deficient embryonic mice. J Neurosci 17: 9113-9121. (Pubitemid 27498439)
44. Tessarollo L, Tsoulfas P, Donovan MJ, Palko ME, Blair-Flynn J, et al. (1997) Targeted deletion of all isoforms of the trkC gene suggests the use of alternate receptors by its ligand neurotrophin-3 in neuronal development and implicates trkC in normal cardiogenesis. Proc Natl Acad Sci U S A 94: 14776-14781.
45. Bamji SX, Majdan M, Pozniak CD, Belliveau DJ, Aloyz R, et al. (1998) The p75 neurotrophin receptor mediates neuronal apoptosis and is essential for naturally occurring sympathetic neuron death. J Cell Biol 140: 911-923. (Pubitemid 28141228)
46. Deppmann CD, Mihalas S, Sharma N, Lonze BE, Niebur E, et al. (2008) A model for neuronal competition during development. Science 320: 369-373. (Pubitemid 351555658)
47. Klau M, Hartmann M, Erdmann KS, Heumann R, Lessmann V (2001) Reduced number of functional glutamatergic synapses in hippocampal neurons overexpressing full-length TrkB receptors. J Neurosci Res 66: 327-336. (Pubitemid 33027399)
48. Leoni C, Valtorta F (2002) Constitutive TrkA activity in receptor-overexpressing PC12 clones. Biochem Biophys Res Commun 291: 972-978. (Pubitemid 34694371)
49. Tan PK, Wang J, Littler PL, Wong KK, Sweetnam TA, et al. (2007) Monitoring interactions between receptor tyrosine kinases and their downstream effector proteins in living cells using bioluminescence resonance energy transfer. Mol Pharmacol 72: 1440-1446. (Pubitemid 350146081)
50. Guagliardo NA, Hill DL (2007) Fungiform taste bud degeneration in C57BL/6J mice following chorda-lingual nerve transection. J Comp Neurol 504: 206-216. (Pubitemid 47327478)
51. Zaidi FN, Whitehead MC (2006) Discrete innervation of murine taste buds by peripheral taste neurons. J Neurosci 26: 8243-8253. (Pubitemid 44309838)
52. Cho TT, Farbman AI (1999) Neurotrophin receptors in the geniculate ganglion. Brain Res Mol Brain Res 68: 1-13. (Pubitemid 29243989)
53. Farbman AI, Brann JH, Rozenblat A, Rochlin MW, Weiler E, et al. (2004) Developmental expression of neurotrophin receptor genes in rat geniculate ganglion neurons. J Neurocytol 33: 331-343. (Pubitemid 39361301)
54. D'Autreaux F, Coppola E, Hirsch MR, Birchmeier C, Brunet JF (2011) Homeoprotein Phox2b commands a somatic-to-visceral switch in cranial sensory pathways. Proc Natl Acad Sci U S A 108: 20018-20023.
55. Matsumoto I, Emori Y, Ninomiya Y, Abe K (2001) A comparative study of three cranial sensory ganglia projecting into the oral cavity: in situ hybridization analyses of neurotrophin receptors and thermosensitive cation channels. Brain Res Mol Brain Res 93: 105-112. (Pubitemid 32925171)
56. Stucky CL, DeChiara T, Lindsay RM, Yancopoulos GD, Koltzenburg M (1998) Neurotrophin 4 is required for the survival of a subclass of hair follicle receptors. J Neurosci 18: 7040-7046. (Pubitemid 28388033)
57. Barker PA, Lomen-Hoerth C, Gensch EM, Meakin SO, Glass DJ, et al. (1993) Tissue-specific alternative splicing generates two isoforms of the trkA receptor. J Biol Chem 268: 15150-15157. (Pubitemid 23206668)
58. Lallemend F, Ernfors P (2012) Molecular interactions underlying the specification of sensory neurons. Trends Neurosci 35: 373-381.
59. Yamout A, Spec A, Cosmano J, Kashyap M, Rochlin MW (2005) Neurotrophic factor receptor expression and in vitro nerve growth of geniculate ganglion neurons that supply divergent nerves. Dev Neurosci 27: 288-298. (Pubitemid 41243216)
60. Farbman AI, Guagliardo N, Sollars SI, Hill DL (2004) Each sensory nerve arising from the geniculate ganglion expresses a unique fingerprint of neurotrophin and neurotrophin receptor genes. J Neurosci Res 78: 659-667. (Pubitemid 39657583)