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Role of neurotrophin in the taste system following gustatory nerve injury

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Abstract

Taste system is a perfect system to study degeneration and regeneration after nerve injury because the taste system is highly plastic and the regeneraton is robust. Besides, degeneration and regeneration can be easily measured since taste buds arise in discrete locations, and nerves that innervate them can be accurately quantified. Neurotrophins are a family of proteins that regulate neural surival, function, and plasticity after nerve injury. Recent studies have shown that neurotrophins play an important role in the developmental and mature taste system, indicating neurtrophin might also regulate taste system following gustatory nerve injury. This review will summarize how taste system degenerates and regenerates after gustatory nerve cut and conclude potential roles of neurotrophin in regulating the process.

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References

  • Beidler LM, Smallman RL (1965) Renewal of cells within taste buds. J Cell Biol 27:263–272

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bradbury EJ, Khemani S, Von King R, Priestley JV, McMahon SB (1999) NT-3 promotes growth of lesioned adult rat sensory axons ascending in the dorsal columns of the spinal cord. Eur J Neurosci 11:3873–3883

    Article  CAS  PubMed  Google Scholar 

  • Cain P, Frank ME, Barry MA (1996) Recovery of chorda tympani nerve function following injury. Exp Neurol 141:337–346

    Article  CAS  PubMed  Google Scholar 

  • Carr VM, Sollars SI, Farbman AI (2005) Neuronal cell death and population dynamics in the developing rat geniculate ganglion. Neuroscience 134:1301–1308

    Article  CAS  PubMed  Google Scholar 

  • Cheal M, Oakley B (1977) Regeneration of fungiform taste buds: temporal and spatial characteristics. J Comp Neurol 172:609–626

    Article  CAS  PubMed  Google Scholar 

  • Cheal M, Dickey WP, Jones LB, Oakley B (1977) Taste fiber responses during reinnervation of fungiform papillae. J Comp Neurol 172:627–646

    Article  CAS  PubMed  Google Scholar 

  • Cho TT, Farbman AI (1999) Neurotrophin receptors in the geniculate ganglion. Mol Brain Res 68:1–13

    Article  CAS  PubMed  Google Scholar 

  • Conover J, Erickson J, Katz D, Bianchi L, Poueymirou W, McClain J, Pan L, Helgren M, Ip N, Boland P (1995) Neuronal deficits, not involving motor neurons, in mice lacking BDNF and/or NT4. Nature 375:235–238

  • Cui Q, Lu Q, So K, Yip H (1998) CNTF, not other trophic factors, promotes axonal regeneration of axotomized retinal ganglion cells in adult hamster. Invest Ophthalmol Vis Sci 40:760–766

  • Cui Q, Tang LS, Hu B, So K-F, Yip HK (2002) Expression of trkA, trkB, and trkC in injured and regenerating retinal ganglion cells of adult rats. Invest Ophthalmol Vis Sci 43:1954–1964

    PubMed  Google Scholar 

  • Diamond J, Coughlin M, Macintyre L, Holmes M, Visheau B (1987) Evidence that endogenous beta nerve growth factor is responsible for the collateral sprouting, but not the regeneration, of nociceptive axons in adult rats. Proc Natl Acad Sci U S A 84:6596–6600

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Diamond J, Foerster A, Holmes M, Coughlin M (1992a) Sensory nerves in adult rats regenerate and restore sensory function to the skin independently of endogenous NGF. J Neurosci Off J Soc Neurosci 12:1467–1476

    CAS  Google Scholar 

  • Diamond J, Holmes M, Coughlin M (1992b) Endogenous NGF and nerve impulses regulate the collateral sprouting of sensory axons in the skin of the adult rat. J Neurosci Off J Soc Neurosci 12:1454–1466

    CAS  Google Scholar 

  • Donnerer J (2003) Regeneration of primary sensory neurons. Pharmacology 67:169–181

    Article  CAS  PubMed  Google Scholar 

  • English AW, Meador W, Carrasco DI (2005) Neurotrophin-4/5 is required for the early growth of regenerating axons in peripheral nerves. Eur J Neurosci 21:2624–2634

    Article  PubMed  Google Scholar 

  • English AW, Liu K, Nicolini JM, Mulligan AM, Ye K (2013) Small-molecule trkB agonists promote axon regeneration in cut peripheral nerves. Proc Natl Acad Sci 110:16217–16222

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Farbman AI (1969) Fine structure of degenerating tast buds after denervation. J Embryol Exp Morpholog 22:55–68

    CAS  Google Scholar 

  • Fei D, Huang T, Krimm RF (2014) The neurotrophin receptor p75 regulates gustatory axon branching and promotes innervation of the tongue during development. Neural Dev 9:15

    Article  PubMed Central  PubMed  Google Scholar 

  • Finger TE (2005) Cell types and lineages in taste buds. Chem Senses 30(Suppl 1):i54–i55

    Article  PubMed  Google Scholar 

  • Fritzsch B, Sarai P, Barbacid M, Silos-Santiago I (1997) Mice with a targeted disruption of the neurotrophin receptor< i> trk</i> B lose their gustatory ganglion cells early but do develop taste buds. Int J Dev Neurosci 15:563–576

    Article  CAS  PubMed  Google Scholar 

  • Ganchrow JR, Ganchrow D (1989) Long-term effects of gustatory neurectomy on fungiform papillae in the young rat. Anat Rec 225:224–231

    Article  CAS  PubMed  Google Scholar 

  • Ganchrow JR, Ganchrow D, Oppenheimer M (1986) Chorda tympani innervation of anterior mandibular taste buds in the chicken (Gallus gallus domesticus). Anat Rec 216:434–439

    Article  CAS  PubMed  Google Scholar 

  • Ganchrow D, Ganchrow JR, Verdin-Alcazar M, Whitehead MC (2003) Brain-derived neurotrophic factor-, neurotrophin-3-, and tyrosine kinase receptor-like immunoreactivity in lingual taste bud fields of mature hamster. J Comp Neurol 455:11–24

    Article  CAS  PubMed  Google Scholar 

  • Guagliardo NA, Hill DL (2007) Fungiform taste bud degeneration in C57BL/6J mice following chorda-lingual nerve transection. J Comp Neurol 504:206–216

    Article  PubMed Central  PubMed  Google Scholar 

  • Guth L (1957) The effects of glossopharyngeal nerve transection on the circumvallate papilla of the rat. Anat Rec 128:715–731

    Article  CAS  PubMed  Google Scholar 

  • Guth L (1958) Taste buds on the cat’s circumvallate papilla after reinnervation by glossopharyngeal, vagus, and hypoglossal nerves. Anat Rec 130:25–37

    Article  CAS  PubMed  Google Scholar 

  • Ha SO, Kim JK, Hong HS, Kim DS, Cho HJ (2001) Expression of brain-derived neurotrophic factor in rat dorsal root ganglia, spinal cord and gracile nuclei in experimental models of neuropathic pain. Neuroscience 107:301–309

    Article  CAS  PubMed  Google Scholar 

  • Hagg T (2006) Collateral sprouting as a target for improved function after spinal cord injury. J Neurotrauma 23:281–294

    Article  PubMed  Google Scholar 

  • Hill DL (2004) Neural plasticity in the gustatory system. Nutr Rev 62:S208–S217, discussion S224–241

    Article  PubMed Central  PubMed  Google Scholar 

  • Hill DL, Phillips LM (1994) Functional plasticity of regenerated and intact taste receptors in adult rats unmasked by dietary sodium restriction. J Neurosci Off J Soc Neurosci 14:2904–2910

    CAS  Google Scholar 

  • Hirsch S, Labes M, Bahr M (2000) Changes in BDNF and neurotrophin receptor expression in degenerating and regenerating rat retinal ganglion cells. Restor Neurol Neurosci 17:125–134

    CAS  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hou S, Nicholson L, van Niekerk E, Motsch M, Blesch A (2012) Dependence of regenerated sensory axons on continuous neurotrophin-3 delivery. J Neurosci Off J Soc Neurosci 32:13206–13220

    Article  CAS  Google Scholar 

  • Huang T, Krimm RF (2010) Developmental expression of Bdnf, Ntf4/5, and TrkB in the mouse peripheral taste system. Dev Dyn 239:2637–2646

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Huang T, Krimm RF (2014) BDNF and NT4 play interchangeable roles in gustatory development. Dev Biol 386:308–320

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Huang EJ, Reichardt LF (2001) Neurotrophins: roles in neuronal development and function. Annu Rev Neurosci 24:677–736

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Huang YJ, Maruyama Y, Dvoryanchikov G, Pereira E, Chaudhari N, Roper SD (2007) The role of pannexin 1 hemichannels in ATP release and cell-cell communication in mouse taste buds. Proc Natl Acad Sci U S A 104:6436–6441

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ishida Y, Ugawa S, Ueda T, Yamada T, Shibata Y, Hondoh A, Inoue K, Yu Y, Shimada S (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

    Article  CAS  PubMed  Google Scholar 

  • Ji R, Tian S, Lu HJ, Lu Q, Zheng Y, Wang X, Ding J, Li Q, Lu Q (2013) TAM receptors affect adult brain neurogenesis by negative regulation of microglial cell activation. J Immunol 191:6165–6177

    Article  CAS  PubMed  Google Scholar 

  • Ji R, Liu F, Meng L, Chen X (2014a) Structures and biosynthesis of enediyne natural products. Int J Adv Innov Thoughts Ideas 3:110

    CAS  Google Scholar 

  • Ji R, Meng L, Yang R (2014b) Neuroprotective effects of pituitary adenylate cyclase-activating polypeptide. Int J Adv Innov Thoughts Ideas 3:112

    Google Scholar 

  • Ji R, Yan F, Yang R, Meng L, Ma X (2014c) The preparation and evaluation of DNA microarray probes for detecting Bacillus anthracis. J Microbiol Microb Res 2:8–16

    Google Scholar 

  • Koltzenburg M, Wall PD, McMahon SB (1999) Does the right side know what the left is doing? Trends Neurosci 22:122–127

    Article  CAS  PubMed  Google Scholar 

  • Krimm RF (2006) Mice lacking the p75 receptor fail to acquire a normal complement of taste buds and geniculate ganglion neurons by adulthood. Anat Rec A: Discov Mol Cell Evol Biol 288:1294–1302

    Article  Google Scholar 

  • Krimm RF (2007) Factors that regulate embryonic gustatory development. BMC Neurosci 8(Suppl 3):S4

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Liebl DJ, Mbiene J-P, Parada LF (1999) NT4/5 mutant mice have deficiency in gustatory papillae and taste bud formation. Dev Biol 213:378–389

    Article  CAS  PubMed  Google Scholar 

  • 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 Off J Soc Neurosci 29:3354–3364

    Article  CAS  Google Scholar 

  • McCluskey LP (2004) Up-regulation of activated macrophages in response to degeneration in the taste system: effects of dietary sodium restriction. J Comp Neurol 479:43–55

    Article  PubMed  Google Scholar 

  • Meng L, Jiang X, Ji R (2014) Role of IL6 and TNFα in hippocampal neurogenesis of TAM triple knockout mice. Int J Adv Innov Thoughts Ideas 3:109

    Google Scholar 

  • Mistretta C, Hill D (1994) Development of the taste system: basic neurobiology. Neurol Dis Ther 32:635

    Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Montavon P, Hellekant G, Farbman A (1996) Immunohistochemical, electrophysiological, and electron microscopical study of rat fungiform taste buds after regeneration of chorda tympani through the non-gustatory lingual nerve. J Comp Neurol 367:491–502

    Article  CAS  PubMed  Google Scholar 

  • Murata Y, Yasuo T, Yoshida R, Obata K, Yanagawa Y, Margolskee RF, Ninomiya Y (2010) Action potential-enhanced ATP release from taste cells through hemichannels. J Neurophysiol 104:896–901

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nagahama S, Kurihara K (1985) Norepinephrine as a possible transmitter involved in synaptic transmission in frog taste organs and Ca dependence of its release. J Gen Physiol 85:431–442

    Article  CAS  PubMed  Google Scholar 

  • Nagai T, Delay RJ, Welton J, Roper SD (1998) Uptake and release of neurotransmitter candidates, [3H]serotonin, [3H]glutamate, and [3H]gamma-aminobutyric acid, in taste buds of the mudpuppy, Necturus maculosus. J Comp Neurol 392:199–208

    Article  CAS  PubMed  Google Scholar 

  • Nixon BJ, Doucette R, Jackson PC, Diamond J (1984) Impulse activity evokes precocious sprouting of nociceptive nerves into denervated skin. Somatosens Res 2:97–126

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Oakley B (1970) Reformation of taste buds by crossed sensory nerves in the rat’s tongue. Acta Physiol Scand 79:88–94

    Article  CAS  PubMed  Google Scholar 

  • Oakley B, Keppel E, Hughes SE (1984) Trophic capacity of experimentally lengthened gustatory axons. Brain Res 318:195–201

    Article  CAS  PubMed  Google Scholar 

  • Oakley B, Wu LH, Lawton A, deSibour C (1990) Neural control of ectopic filiform spines in adult tongue. Neuroscience 36:831–838

    Article  CAS  PubMed  Google Scholar 

  • Oakley B, Lawton A, Riddle DR, Wu LH (1993) Morphometric and immunocytochemical assessment of fungiform taste buds after interruption of the chorda-lingual nerve. Microsc Res Tech 26:187–195

    Article  CAS  PubMed  Google Scholar 

  • Olmsted J (1922) Taste fibers and the chorda tympani nerve. J Comp Neurol 34:337–341

    Article  Google Scholar 

  • Patel AV, Krimm RF (2010) BDNF is required for the survival of differentiated geniculate ganglion neurons. Dev Biol 340:419–429

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Phillips LM, Hill DL (1996) Novel regulation of peripheral gustatory function by the immune system. Am J Physiol 271:R857–R862

    CAS  PubMed  Google Scholar 

  • Popper P, Lopez I, Beizai P, Li G, Kim J, Micevych PE, Honrubia V (1999) Expression of BDNF and TrkB mRNAs in the crista neurosensory epithelium and vestibular ganglia following ototoxic damage. Brain Res 846:40–51

    Article  CAS  PubMed  Google Scholar 

  • Ramer MS, Priestley JV, McMahon SB (2000) Functional regeneration of sensory axons into the adult spinal cord. Nature 403:312–316

    Article  CAS  PubMed  Google Scholar 

  • Ringstedt T, Ibáñez CF, Nosrat CA (1999) Role of brain-derived neurotrophic factor in target invasion in the gustatory system. J Neurosci 19:3507–3518

    CAS  PubMed  Google Scholar 

  • Robinson PP (1989) The reinnervation of the tongue and salivary glands after lingual nerve injuries in cats. Brain Res 483:259–271

    Article  CAS  PubMed  Google Scholar 

  • Rochlin MW, O’Connor R, Giger RJ, Verhaagen J, Farbman AI (2000) Comparison of neurotrophin and repellent sensitivities of early embryonic geniculate and trigeminal axons. J Comp Neurol 422:579–593

    Article  CAS  PubMed  Google Scholar 

  • Segerstad CHA, Hellekant G, Farbman AI (1989) Changes in number and morphology of fungiform taste-buds in rat after transection of the chorda tympani or chordalingual nerve. Chem Senses 14:335–348

    Article  Google Scholar 

  • Shuler MG, Krimm RF, Hill DL (2004) Neuron/target plasticity in the peripheral gustatory system. J Comp Neurol 472:183–192

    Article  PubMed Central  PubMed  Google Scholar 

  • Sloan HE, Hughes SE, Oakley B (1983) Chronic impairment of axonal transport eliminates taste responses and taste buds. J Neurosci Off J Soc Neurosci 3:117–123

    CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Starostik MR, Rebello MR, Cotter KA, Kulik A, Medler KF (2010) Expression of GABAergic receptors in mouse taste receptor cells. PLoS One 5:e13639

    Article  PubMed Central  PubMed  Google Scholar 

  • State FA, Dessouky HI (1977) Effect of the length of the distal stump of transected nerve upon the rate of degeneration of taste buds. Acta Anat 98:353–360

    Article  CAS  PubMed  Google Scholar 

  • Torrey TW (1936) The relation of nerves to degenerating taste buds. J Comp Neurol 64:325–336

    Article  Google Scholar 

  • Uchida N, Kanazawa M, Suzuki Y, Takeda M (2003) Expression of BDNF and TrkB in mouse taste buds after denervation and in circumvallate papillae during development. Arch Histol Cytol 66:17–25

    Article  CAS  PubMed  Google Scholar 

  • Wilhelm JC, Xu M, Cucoranu D, Chmielewski S, Holmes T, Lau KS, Bassell GJ, English AW (2012) Cooperative roles of BDNF expression in neurons and Schwann cells are modulated by exercise to facilitate nerve regeneration. J Neurosci Off J Soc Neurosci 32:5002–5009

    Article  CAS  Google Scholar 

  • Wolthers M, Moldovan M, Binderup T, Schmalbruch H, Krarup C (2005) Comparative electrophysiological, functional, and histological studies of nerve lesions in rats. Microsurgery 25:508–519

    Article  CAS  PubMed  Google Scholar 

  • Yan X-B, Wang S-S, Hou H-L, Ji R, Zhou J-N (2007) Lithium improves the behavioral disorder in rats subjected to transient global cerebral ischemia. Behav Brain Res 177:282–289

    Article  CAS  PubMed  Google Scholar 

  • Yasumatsu K, Kusuhara Y, Shigemura N, Ninomiya Y (2007) Recovery of two independent sweet taste systems during regeneration of the mouse chorda tympani nerve after nerve crush. Eur J Neurosci 26:1521–1529

    Article  PubMed  Google Scholar 

  • Yee CL, Jones KR, Finger TE (2003) Brain-derived neurotrophic factor is present in adult mouse taste cells with synapses. J Comp Neurol 459:15–24

    Article  CAS  PubMed  Google Scholar 

  • Yee C, Bartel DL, Finger TE (2005) Effects of glossopharyngeal nerve section on the expression of neurotrophins and their receptors in lingual taste buds of adult mice. J Comp Neurol 490:371–390

    Article  CAS  PubMed  Google Scholar 

  • Zhang JY, Luo XG, Xian CJ, Liu ZH, Zhou XF (2000) Endogenous BDNF is required for myelination and regeneration of injured sciatic nerve in rodents. Eur J Neurosci 12:4171–4180

    CAS  PubMed  Google Scholar 

  • Zhang F, Huang P, Yang P, Zhang X (2009) Effects of p75 neurotrophin receptor knockout on axonal regeneration in a mouse model of facial nerve injury. Neural Regen Res 4:565–569

    CAS  Google Scholar 

  • Zhou XF, Rush RA, McLachlan EM (1996) Differential expression of the p75 nerve growth factor receptor in glia and neurons of the rat dorsal root ganglia after peripheral nerve transection. J Neurosci Off J Soc Neurosci 16:2901–2911

    CAS  Google Scholar 

  • Zhou XF, Chie ET, Deng YS, Zhong JH, Xue Q, Rush RA, Xian CJ (1999) Injured primary sensory neurons switch phenotype for brain-derived neurotrophic factor in the rat. Neuroscience 92:841–853

    Article  CAS  PubMed  Google Scholar 

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Meng, L., Jiang, X. & Ji, R. Role of neurotrophin in the taste system following gustatory nerve injury. Metab Brain Dis 30, 605–613 (2015). https://doi.org/10.1007/s11011-014-9626-0

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