Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
Metabolic Brain Disease
Published in: Metabolic Brain Disease 3/2015

01-06-2015 | Review Article

Role of neurotrophin in the taste system following gustatory nerve injury

Authors: Lingbin Meng, Xin Jiang, Rui Ji

Published in: Metabolic Brain Disease | Issue 3/2015

Login to get access

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.
Literature
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 11:3873–3883CrossRefPubMed
Cain P, Frank ME, Barry MA (1996) Recovery of chorda tympani nerve function following injury. Exp Neurol 141:337–346CrossRefPubMed
Carr VM, Sollars SI, Farbman AI (2005) Neuronal cell death and population dynamics in the developing rat geniculate ganglion. Neuroscience 134:1301–1308CrossRefPubMed
Cheal M, Oakley B (1977) Regeneration of fungiform taste buds: temporal and spatial characteristics. J Comp Neurol 172:609–626CrossRefPubMed
Cheal M, Dickey WP, Jones LB, Oakley B (1977) Taste fiber responses during reinnervation of fungiform papillae. J Comp Neurol 172:627–646CrossRefPubMed
Cho TT, Farbman AI (1999) Neurotrophin receptors in the geniculate ganglion. Mol Brain Res 68:1–13CrossRefPubMed
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 43:1954–1964PubMed
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 84:6596–6600CrossRefPubMedCentralPubMed
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
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
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 21:2624–2634CrossRefPubMed
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 110:16217–16222CrossRefPubMedCentralPubMed
Farbman AI (1969) Fine structure of degenerating tast buds after denervation. J Embryol Exp Morpholog 22:55–68
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 9:15CrossRefPubMedCentralPubMed
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 15:563–576CrossRefPubMed
Ganchrow JR, Ganchrow D (1989) Long-term effects of gustatory neurectomy on fungiform papillae in the young rat. Anat Rec 225:224–231CrossRefPubMed
Ganchrow JR, Ganchrow D, Oppenheimer M (1986) Chorda tympani innervation of anterior mandibular taste buds in the chicken (Gallus gallus domesticus). Anat Rec 216:434–439CrossRefPubMed
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 455:11–24CrossRefPubMed
Guagliardo NA, Hill DL (2007) Fungiform taste bud degeneration in C57BL/6J mice following chorda-lingual nerve transection. J Comp Neurol 504:206–216CrossRefPubMedCentralPubMed
Guth L (1957) The effects of glossopharyngeal nerve transection on the circumvallate papilla of the rat. Anat Rec 128:715–731CrossRefPubMed
Guth L (1958) Taste buds on the cat’s circumvallate papilla after reinnervation by glossopharyngeal, vagus, and hypoglossal nerves. Anat Rec 130:25–37CrossRefPubMed
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 107:301–309CrossRefPubMed
Hagg T (2006) Collateral sprouting as a target for improved function after spinal cord injury. J Neurotrauma 23:281–294CrossRefPubMed
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
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
Hoshino N, Vatterott P, Egwiekhor A, Rochlin MW (2010) Brain-derived neurotrophic factor attracts geniculate ganglion neurites during embryonic targeting. Dev Neurosci 32:184–196CrossRefPubMedCentralPubMed
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 32:13206–13220CrossRef
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 104:6436–6441CrossRefPubMedCentralPubMed
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 514:131–144CrossRefPubMed
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 191:6165–6177CrossRefPubMed
Ji R, Liu F, Meng L, Chen X (2014a) Structures and biosynthesis of enediyne natural products. Int J Adv Innov Thoughts Ideas 3:110
Ji R, Meng L, Yang R (2014b) Neuroprotective effects of pituitary adenylate cyclase-activating polypeptide. Int J Adv Innov Thoughts Ideas 3:112
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
Koltzenburg M, Wall PD, McMahon SB (1999) Does the right side know what the left is doing? Trends Neurosci 22:122–127CrossRefPubMed
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 288:1294–1302CrossRef
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 232:508–521CrossRefPubMed
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 17:9113–9121PubMed
Liebl DJ, Mbiene J-P, Parada LF (1999) NT4/5 mutant mice have deficiency in gustatory papillae and taste bud formation. Dev Biol 213:378–389CrossRefPubMed
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 29:3354–3364CrossRef
McCluskey LP (2004) Up-regulation of activated macrophages in response to degeneration in the taste system: effects of dietary sodium restriction. J Comp Neurol 479:43–55CrossRefPubMed
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
Mistretta C, Hill D (1994) Development of the taste system: basic neurobiology. Neurol Dis Ther 32:635
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 409:13–24CrossRefPubMedCentralPubMed
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 367:491–502CrossRefPubMed
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 104:896–901CrossRefPubMedCentralPubMed
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 85:431–442CrossRefPubMed
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 392:199–208CrossRefPubMed
Nixon BJ, Doucette R, Jackson PC, Diamond J (1984) Impulse activity evokes precocious sprouting of nociceptive nerves into denervated skin. Somatosens Res 2:97–126PubMed
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 360:698–704CrossRefPubMed
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 376:587–602CrossRefPubMed
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 124:1333–1342PubMed
Oakley B (1970) Reformation of taste buds by crossed sensory nerves in the rat’s tongue. Acta Physiol Scand 79:88–94CrossRefPubMed
Oakley B, Keppel E, Hughes SE (1984) Trophic capacity of experimentally lengthened gustatory axons. Brain Res 318:195–201CrossRefPubMed
Oakley B, Wu LH, Lawton A, deSibour C (1990) Neural control of ectopic filiform spines in adult tongue. Neuroscience 36:831–838CrossRefPubMed
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 26:187–195CrossRefPubMed
Olmsted J (1922) Taste fibers and the chorda tympani nerve. J Comp Neurol 34:337–341CrossRef
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 365:50–60CrossRefPubMed
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 518:3290–3301CrossRefPubMedCentralPubMed
Phillips LM, Hill DL (1996) Novel regulation of peripheral gustatory function by the immune system. Am J Physiol 271:R857–R862PubMed
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 846:40–51CrossRefPubMed
Ramer MS, Priestley JV, McMahon SB (2000) Functional regeneration of sensory axons into the adult spinal cord. Nature 403:312–316CrossRefPubMed
Ringstedt T, Ibáñez CF, Nosrat CA (1999) Role of brain-derived neurotrophic factor in target invasion in the gustatory system. J Neurosci 19:3507–3518PubMed
Robinson PP (1989) The reinnervation of the tongue and salivary glands after lingual nerve injuries in cats. Brain Res 483:259–271CrossRefPubMed
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 422:579–593CrossRefPubMed
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 14:335–348CrossRef
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
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 64:310–320CrossRefPubMed
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 98:353–360CrossRefPubMed
Torrey TW (1936) The relation of nerves to degenerating taste buds. J Comp Neurol 64:325–336CrossRef
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 66:17–25CrossRefPubMed
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 32:5002–5009CrossRef
Wolthers M, Moldovan M, Binderup T, Schmalbruch H, Krarup C (2005) Comparative electrophysiological, functional, and histological studies of nerve lesions in rats. Microsurgery 25:508–519CrossRefPubMed
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 177:282–289CrossRefPubMed
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 26:1521–1529CrossRefPubMed
Yee CL, Jones KR, Finger TE (2003) Brain-derived neurotrophic factor is present in adult mouse taste cells with synapses. J Comp Neurol 459:15–24CrossRefPubMed
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 490:371–390CrossRefPubMed
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 12:4171–4180PubMed
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
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
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 92:841–853CrossRefPubMed
Metadata
Title
Role of neurotrophin in the taste system following gustatory nerve injury
Authors
Lingbin Meng
Xin Jiang
Rui Ji
Publication date
01-06-2015
Publisher
Springer US
Published in
Metabolic Brain Disease / Issue 3/2015
Print ISSN: 0885-7490
Electronic ISSN: 1573-7365
DOI
https://doi.org/10.1007/s11011-014-9626-0

Other articles of this Issue 3/2015

Metabolic Brain Disease 3/2015 Go to the issue

Review Article

Spinal cord injury induced neuropathic pain: Molecular targets and therapeutic approaches

Research Article

Urtica dioica leaves modulates muscarinic cholinergic system in the hippocampus of streptozotocin-induced diabetic mice

Research Article

Asparagine synthetase deficiency detected by whole exome sequencing causes congenital microcephaly, epileptic encephalopathy and psychomotor delay

Review Article

TAM receptor deficiency affects adult hippocampal neurogenesis

Review Article

Glucose metabolism following human traumatic brain injury: methods of assessment and pathophysiological findings

Research Article

Pre-treatment with metformin activates Nrf2 antioxidant pathways and inhibits inflammatory responses through induction of AMPK after transient global cerebral ischemia