BDNF and NT4 play interchangeable roles in gustatory development

Developmental Biology

Volumn 386, Issue 2, 2014, Pages 308-320

  Huang, Tao ^a   Krimm, Robin F ^a  

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

Author keywords

Brain derived neurotrophic factor; Geniculate ganglion neurons; Neurotrophin 4; Neurotrophins; Taste

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CASPASE 3; NEUROTROPHIN 4;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AXON GUIDANCE RELATED GENE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; FACIAL NERVE; FEMALE; GENE; GENE CONTROL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GUSTATORY DEVELOPMENT; INNERVATION; KNOCKOUT MOUSE; MALE; MOUSE; NERVE CELL NECROSIS; NERVE FIBER; NERVOUS SYSTEM DEVELOPMENT; NEUROPATHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; TASTE DEVELOPMENT; TONGUE INNERVATION;

MUS;

BRAIN DERIVED NEUROTROPHIC FACTOR; GENICULATE GANGLION NEURONS; NEUROTROPHIN-4; NEUROTROPHINS; TASTE;

ANALYSIS OF VARIANCE; ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CARBOCYANINES; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENICULATE GANGLION; IMMUNOHISTOCHEMISTRY; LASER CAPTURE MICRODISSECTION; MICE; MICE, KNOCKOUT; MICROARRAY ANALYSIS; NERVE GROWTH FACTORS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TASTE;

EID: 84892880044     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2013.12.031     Document Type: Article

References (83)

1. Agerman K., Hjerling-Leffler J., Blanchard M.P., Scarfone E., Canlon B., Nosrat C., Ernfors P. BDNF gene replacement reveals multiple mechanisms for establishing neurotrophin specificity during sensory nervous system development. Development 2003, 130:1479-1491.
2. Al-Hadlaq S.M., Bradley R.M., MacCallum D.K., Mistretta C.M. Embryonic geniculate ganglion neurons in culture have neurotrophin-specific electrophysiological properties. Neuroscience 2003, 118:145-159.
3. Ascano M., Bodmer D., Kuruvilla R. Endocytic trafficking of neurotrophins in neural development. Trends Cell Biol. 2012, 22:266-273.
4. Atwal J.K., Massie B., Miller F.D., Kaplan D.R. The TrkB-Shc site signals neuronal survival and local axon growth via MEK and P13-kinase. Neuron 2000, 27:265-277.
5. Berghuis P., Agerman K., Dobszay M.B., Minichiello L., Harkany T., Ernfors P. Brain-derived neurotrophic factor selectively regulates dendritogenesis of parvalbumin-containing interneurons in the main olfactory bulb through the PLCgamma pathway. J. Neurobiol. 2006, 66:1437-1451.
6. Bibel M., Barde Y.A. Neurotrophins: key regulators of cell fate and cell shape in the vertebrate nervous system. Genes Dev. 2000, 14:2919-2937.
7. Bustin S.A., Beaulieu J.F., Huggett J., Jaggi R., Kibenge F.S., Olsvik P.A., Penning L.C., Toegel S. MIQE precis: practical implementation of minimum standard guidelines for fluorescence-based quantitative real-time PCR experiments. BMC Mol. Biol. 2010, 11:74.
8. Carr V.M., Sollars S.I., Farbman A.I. Neuronal cell death and population dynamics in the developing rat geniculate ganglion. Neuroscience 2005, 134:1301-1308.
9. Cosker K.E., Courchesne S.L., Segal R.A. Action in the axon: generation and transport of signaling endosomes. Curr. Opin. Neurobiol. 2008, 18:270-275.
10. Deveraux Q.L., Reed J.C. IAP family proteins--suppressors of apoptosis. Genes Dev. 1999, 13:239-252.
11. Eng S.R., Gratwick K., Rhee J.M., Fedtsova N., Gan L., Turner E.E. Defects in sensory axon growth precede neuronal death in Brn3a-deficient mice. J. Neurosci. 2001, 21:541-549.
12. Ernfors P., Lee K.F., Jaenisch R. Mice lacking brain-derived neurotrophic factor develop with sensory deficits. Nature 1994, 368:147-150.
13. Fan G., Egles C., Sun Y., Minichiello L., Renger J.J., Klein R., Liu G., Jaenisch R. Knocking the NT4 gene into the BDNF locus rescues BDNF deficient mice and reveals distinct NT4 and BDNF activities. Nat. Neurosci. 2000, 3:350-357.
14. Fan L., Girnius S., Oakley B. Support of trigeminal sensory neurons by nonneuronal p75 neurotrophin receptors. Brain Res. Dev. Brain Res. 2004, 150:23-39.
15. Fritzsch B., Sarai P.A., Barbacid M., Silos-Santiago I. 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.: The official journal of the International Society for Developmental Neuroscience 1997, 15:563-576.
16. Gartner A., Polnau D.G., Staiger V., Sciarretta C., Minichiello L., Thoenen H., Bonhoeffer T., Korte M. Hippocampal long-term potentiation is supported by presynaptic and postsynaptic tyrosine receptor kinase B-mediated phospholipase Cgamma signaling. J. Neurosci. 2006, 26:3496-3504.
17. Grimes M.L., Zhou J., Beattie E.C., Yuen E.C., Hall D.E., Valletta J.S., Topp K.S., LaVail J.H., Bunnett N.W., Mobley W.C. Endocytosis of activated TrkA: evidence that nerve growth factor induces formation of signaling endosomes. J. Neurosci. 1996, 16:7950-7964.
18. Guo T., Mandai K., Condie B.G., Wickramasinghe S.R., Capecchi M.R., Ginty D.D. An evolving NGF-Hoxd1 signaling pathway mediates development of divergent neural circuits in vertebrates. Nat. Neurosci. 2011, 14:31-36.
19. Harlow D.E., Yang H., Williams T., Barlow L.A. Epibranchial placode-derived neurons produce BDNF required for early sensory neuron development. Dev. Dyn.: An official publication of the American Association of Anatomists 2011, 240:309-323.
20. Harrington A.W., Hillaire C., Zweifel L.S., Glebova N.O., Philippidou P., Halegoua S., Ginty D.D. Recruitment of actin modifiers to TrkA endosomes governs retrograde NGF signaling and survival. Cell 2011, 146:421-434.
21. Heerssen H.M., Segal R.A. Location, location, location: a spatial view of neurotrophin signal transduction. Trends Neurosci. 2002, 25:160-165.
22. Hoshino N., Vatterott P., Egwiekhor A., Rochlin M.W. Brain-derived neurotrophic factor attracts geniculate ganglion neurites during embryonic targeting. Dev. Neurosci. 2010, 32:184-196.
23. Hosley M.A., Oakley B. Postnatal development of the vallate papilla and taste buds in rats. Anat. Rec. 1987, 218:216-222.
24. Howe C.L., Mobley W.C. Long-distance retrograde neurotrophic signaling. Curr. Opin. Neurobiol. 2005, 15:40-48.
25. Howe C.L., Valletta J.S., Rusnak A.S., Mobley W.C. NGF signaling from clathrin-coated vesicles: evidence that signaling endosomes serve as a platform for the Ras-MAPK pathway. Neuron 2001, 32:801-814.
26. Huang E.J., Liu W., Fritzsch B., Bianchi L.M., Reichardt L.F., Xiang M. Brn3a is a transcriptional regulator of soma size, target field innervation and axon pathfinding of inner ear sensory neurons. Development 2001, 128:2421-2432.
27. Huang E.J., Reichardt L.F. Trk receptors: roles in neuronal signal transduction. Annu. Rev. Biochem. 2003, 72:609-642.
28. Huang T., Krimm R.F. Developmental expression of Bdnf, Ntf4/5, and TrkB in the mouse peripheral taste system. Dev. Dyn.: An Official Publication of the American Association of Anatomists 2010, 239:2637-2646.
29. Ishida Y., Ugawa S., Ueda T., Yamada T., Shibata Y., Hondoh A., Inoue K., Yu Y., Shimada S. 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. 2009, 514:131-144.
30. Ito A., Nosrat C.A. Gustatory papillae and taste bud development and maintenance in the absence of TrkB ligands BDNF and NT-4. Cell Tissue Res. 2009, 337:349-359.
31. Ito A., Nosrat I.V., Nosrat C.A. Taste cell formation does not require gustatory and somatosensory innervation. Neurosci. Lett. 2010, 471:189-194.
32. Kaufman M. The Atlas of Mouse Development 1995, Academic Press, London.
33. Khatri P., Voichita C., Kattan K., Ansari N., Khatri A., Georgescu C., Tarca A.L., Draghici S. Onto-tools: new additions and improvements in 2006. Nucleic Acids Res. 2007, 35:W206-W211.
34. Krimm R.F., Miller K.K., Kitzman P.H., Davis B.M., Albers K.M. Epithelial overexpression of BDNF or NT4 disrupts targeting of taste neurons that innervate the anterior tongue. Dev. Biol. 232 2001, 508-521.
35. Lakshman M., Subramaniam V., Wong S., Jothy S. CD44 promotes resistance to apoptosis in murine colonic epithelium. J. Cell Physiol. 2005, 203:583-588.
36. Law C.O., Kirby R.J., Aghamohammadzadeh S., Furley A.J. The neural adhesion molecule TAG-1 modulates responses of sensory axons to diffusible guidance signals. Development 2008, 135:2361-2371.
37. Li, C., Hung Wong, W., 2001. Model-based analysis of oligonucleotide arrays: model validation, design issues and standard error application. Genome. Biol. 2, RESEARCH0032.
38. Li C., Wong W.H. Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc. Nat. Acad. Sci. U.S.A. 2001, 98:31-36.
39. Liebl D.J., Tessarollo L., Palko M.E., Parada L.F. Absence of sensory neurons before target innervation in brain-derived neurotrophic factor-, neurotrophin 3-, and TrkC-deficient embryonic mice. J. Neurosci. 1997, 17:9113-9121.
40. Liu X., Ernfors P., Wu H., Jaenisch R. Sensory but not motor neuron deficits in mice lacking NT4 and BDNF. Nature 1995, 375:238-241.
41. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
42. Lopez G.F., Krimm R.F. Epithelial overexpression of BDNF and NT4 produces distinct gustatory axon morphologies that disrupt initial targeting. Dev. Biol. 2006, 292:457-468.
43. Lopez G.F., Krimm R.F. Refinement of innervation accuracy following initial targeting of peripheral gustatory fibers. J. Neurobiol. 2006, 66:1033-1043.
44. Ma L., Lopez G.F., Krimm R.F. Epithelial-derived brain-derived neurotrophic factor is required for gustatory neuron targeting during a critical developmental period. J. Neurosci. 2009, 29:3354-3364.
45. Mandai K., Guo T., Hillaire C., Meabon J.S., Kanning K.C., Bothwell M., Ginty D.D. LIG family receptor tyrosine kinase-associated proteins modulate growth factor signals during neural development. Neuron 2009, 63:614-627.
46. Mbiene J.P. Taste placodes are primary targets of geniculate but not trigeminal sensory axons in mouse developing tongue. J. Neurocytol. 2004, 33:617-629.
47. Mbiene J.P., Maccallum D.K., Mistretta C.M. Organ cultures of embryonic rat tongue support tongue and gustatory papilla morphogenesis in vitro without intact sensory ganglia. J. Comp. Neurol. 1997, 377:324-340.
48. Mielgo A., van Driel M., Bloem A., Landmann L., Gunthert U. A novel antiapoptotic mechanism based on interference of Fas signaling by CD44 variant isoforms. Cell Death Differ. 2006, 13:465-477.
49. Mincheva S., Garcera A., Gou-Fabregas M., Encinas M., Dolcet X., Soler R.M. The canonical nuclear factor-kappaB pathway regulates cell survival in a developmental model of spinal cord motoneurons. J. Neurosci. 2011, 31:6493-6503.
50. Ming G.L., Wong S.T., Henley J., Yuan X.B., Song H.J., Spitzer N.C., Poo M.M. Adaptation in the chemotactic guidance of nerve growth cones. Nature 2002, 417:411-418.
51. Minichiello L. TrkB signalling pathways in LTP and learning. Nat. Rev. Neurosci. 2009, 10:850-860.
52. Minichiello L., Calella A.M., Medina D.L., Bonhoeffer T., Klein R., Korte M. Mechanism of TrkB-mediated hippocampal long-term potentiation. Neuron 2002, 36:121-137.
53. Minichiello L., Casagranda F., Tatche R.S., Stucky C.L., Postigo A., Lewin G.R., Davies A.M., Klein R. Point mutation in trkB causes loss of NT4-dependent neurons without major effects on diverse BDNF responses. Neuron 1998, 21:335-345.
54. Mistretta C.M., Goosens K.A., Farinas I., Reichardt L.F. 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. 1999, 409:13-24.
55. Musumeci G., Sciarretta C., Rodriguez-Moreno A., Al Banchaabouchi M., Negrete-Diaz V., Costanzi M., Berno V., Egorov A.V., Halbach von Bohlen Und, Cestari O., Delgado-Garcia V., Minichiello, L.J.M. TrkB modulates fear learning and amygdalar synaptic plasticity by specific docking sites. J. Neurosci. 2009, 29:10131-10143.
56. Nagato T., Matsumoto K., Tanioka H., Kodama J., Toh H. Effect of denervation on morphogenesis of the rat fungiform papilla. Acta Anat. (Basel) 1995, 153:301-309.
57. Nosrat C.A., Blomlof J., ElShamy W.M., Ernfors P., Olson L. Lingual deficits in BDNF and NT3 mutant mice leading to gustatory and somatosensory disturbances, respectively. Development 1997, 124:1333-1342.
58. Nosrat C.A., 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. J. Comp. Neurol. 1996, 376:587-602.
59. Nosrat C.A., Olson L. Brain-derived neurotrophic factor mRNA is expressed in the developing taste bud-bearing tongue papillae of rat. J. Comp. Neurol. 1995, 360:698-704.
60. Nosrat I.V., Margolskee R.F., Nosrat C.A. Targeted taste cell-specific overexpression of brain-derived neurotrophic factor in adult taste buds elevates phosphorylated TrkB protein levels in taste cells, increases taste bud size, and promotes gustatory innervation. J. Biol. Chem. 2012, 287:16791-16800.
61. Oakley B., Brandemihl A., Cooper D., Lau D., Lawton A., Zhang C. The morphogenesis of mouse vallate gustatory epithelium and taste buds requires BDNF-dependent taste neurons. Brain Res. Dev. Brain Res. 1998, 105:85-96.
62. Patel A.V., Huang T., Krimm R.F. 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. 2010, 518:3290-3301.
63. Patel A.V., Krimm R.F. BDNF is required for the survival of differentiated geniculate ganglion neurons. Dev. Biol. 2010, 340:419-429.
64. Patel A.V., Krimm R.F. Neurotrophin-4 regulates the survival of gustatory neurons earlier in development using a different mechanism than brain-derived neurotrophic factor. Dev. Biol 2012.
65. Pazyra-Murphy M.F., Hans A., Courchesne S.L., Karch C., Cosker K.E., Heerssen H.M., Watson F.L., Kim T., Greenberg M.E., Segal R.A. A retrograde neuronal survival response: target-derived neurotrophins regulate MEF2D and bcl-w. J. Neurosci. 2009, 29:6700-6709.
66. Postigo A., Calella A.M., Fritzsch B., Knipper M., Katz D., Eilers A., Schimmang T., Lewin G.R., Klein R., Minichiello L. Distinct requirements for TrkB and TrkC signaling in target innervation by sensory neurons. Genes Dev. 2002, 16:633-645.
67. Riccio A., Pierchala B.A., Ciarallo C.L., Ginty D.D. An NGF-TrkA-mediated retrograde signal to transcription factor CREB in sympathetic neurons. Science 1997, 277:1097-1100.
68. Riedl S.J., Renatus M., Schwarzenbacher R., Zhou Q., Sun C., Fesik S.W., Liddington R.C., Salvesen G.S. Structural basis for the inhibition of caspase-3 by XIAP. Cell 2001, 104:791-800.
69. Ringstedt T., Ibanez C.F., Nosrat C.A. Role of brain-derived neurotrophic factor in target invasion in the gustatory system. J. Neurosci. 1999, 19:3507-3518.
70. Rochlin M.W., O'Connor R., Giger R.J., Verhaagen J., Farbman A.I. Comparison of neurotrophin and repellent sensitivities of early embryonic geniculate and trigeminal axons. J. Comp. Neurol. 2000, 422:579-593.
71. Runge E.M., Hoshino N., Biehl M.J., Ton S., Rochlin M.W. Neurotrophin-4 is more potent than brain-derived neurotrophic factor in promoting, attracting and suppressing geniculate ganglion neurite outgrowth. Dev. Neurosci 2012.
72. Runge E.M., Hoshino N., Biehl M.J., Ton S., Rochlin M.W. Neurotrophin-4 is more potent than brain-derived neurotrophic factor in promoting, attracting and suppressing geniculate ganglion neurite outgrowth. Dev. Neurosci. 2012, 34:389-401.
73. Schadt E.E., Li C., Ellis B., Wong W.H. Feature extraction and normalization algorithms for high-density oligonucleotide gene expression array data. J. Cell Biochem. Suppl. 2001, 37:120-125.
74. Schadt E.E., Li C., Su C., Wong W.H. Analyzing high-density oligonucleotide gene expression array data. J. Cell Biochem. 2000, 80:192-202.
75. Sciarretta C., Fritzsch B., Beisel K., Rocha-Sanchez S.M., Buniello A., Horn J.M., Minichiello L. PLCgamma-activated signalling is essential for TrkB mediated sensory neuron structural plasticity. BMC Dev. Biol. 2010, 10:103.
76. Shao Y., Akmentin W., Toledo-Aral J.J., Rosenbaum J., Valdez G., Cabot J.B., Hilbush B.S., Halegoua S. Pincher, a pinocytic chaperone for nerve growth factor/TrkA signaling endosomes. J. Cell Biol. 2002, 157:679-691.
77. Sollars S.I. Chorda tympani nerve transection at different developmental ages produces differential effects on taste bud volume and papillae morphology in the rat. J. Neurobiol. 2005, 64:310-320.
78. Thirumangalathu S., Harlow D.E., Driskell A.L., Krimm R.F., Barlow L.A. Fate mapping of mammalian embryonic taste bud progenitors. Development 2009, 136:1519-1528.
79. Uchida M., Enomoto A., Fukuda T., Kurokawa K., Maeda K., Kodama Y., Asai N., Hasegawa T., Shimono Y., Jijiwa M., Ichihara M., Murakumo Y., Takahashi M. Dok-4 regulates GDNF-dependent neurite outgrowth through downstream activation of Rap1 and mitogen-activated protein kinase. J. Cell Sci. 2006, 119:3067-3077.
80. Watson F.L., Heerssen H.M., Bhattacharyya A., Klesse L., Lin M.Z., Segal R.A. Neurotrophins use the Erk5 pathway to mediate a retrograde survival response. Nat. Neurosci. 2001, 4:981-988.
81. Watson F.L., Heerssen H.M., Moheban D.B., Lin M.Z., Sauvageot C.M., Bhattacharyya A., Pomeroy S.L., Segal R.A. Rapid nuclear responses to target-derived neurotrophins require retrograde transport of ligand-receptor complex. J. Neurosci. 1999, 19:7889-7900.
82. Xiang M., Gan L., Zhou L., Klein W.H., Nathans J. Targeted deletion of the mouse POU domain gene Brn-3a causes selective loss of neurons in the brainstem and trigeminal ganglion, uncoordinated limb movement, and impaired suckling. Proc. Nat. Acad. Sci. U.S.A. 1996, 93:11950-11955.
83. Zweifel L.S., Kuruvilla R., Ginty D.D. Functions and mechanisms of retrograde neurotrophin signalling. Nat. Rev. Neurosci. 2005, 6:615-625.