Attenuation of peripheral salt taste responses and local immune function contralateral to gustatory nerve injury: effects of aldosterone

Guagliardo, Nick A.; West, Katie Nicole; McCluskey, Lynnette Phillips; Hill, David L.

doi:10.1152/ajpregu.00219.2009

Cited by 10 publications

(19 citation statements)

References 46 publications

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“…Consistent with previous reports (Guagliardo et al, 2009; Whitehead et al, 1987), some taste buds were still present 2 weeks after nerve section in all four genotypes and continued to be present 8 weeks after nerve section (Figure 2D). Taste bud number was reduced by both nerve sectioning (F (1,38) =313, p<0.001) and genotype (F (3,38) =3.62, p=0.02).…”

Section: Resultssupporting

confidence: 92%

BDNF is required for taste axon regeneration following unilateral chorda tympani nerve section

Meng

Huang

Sun

et al. 2017

Experimental Neurology

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Taste nerves readily regenerate to reinnervate denervated taste buds; however, factors required for regeneration have not yet been identified. When the chorda tympani nerve is sectioned, expression of brain-derived neurotrophic factor (BDNF) remains high in the geniculate ganglion and lingual epithelium, despite the loss of taste buds. These observations suggest that BDNF is present in the taste system after nerve section and may support taste nerve regeneration. To test this hypothesis, we inducibly deleted Bdnf during adulthood in mice. Shortly after Bdnf gene recombination, the chorda tympani nerve was unilaterally sectioned causing a loss of both taste buds and neurons, irrespective of BDNF levels. Eight weeks after nerve section, however, regeneration was differentially affected by Bdnf deletion. In control mice, there was regeneration of the chorda tympani nerve and taste buds reappeared with innervation. In contrast, few taste buds were reinnervated in mice lacking normal Bdnf expression such that taste bud number remained low. In all genotypes, taste buds that were reinnervated were normal-sized, but non-innervated taste buds remained small and atrophic. On the side of the tongue contralateral to the nerve section, taste buds for some genotypes became larger and all taste buds remained innervated. Our findings suggest that BDNF is required for nerve regeneration following gustatory nerve section.

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Section: Resultssupporting

confidence: 92%

BDNF is required for taste axon regeneration following unilateral chorda tympani nerve section

Meng

Huang

Sun

et al. 2017

Experimental Neurology

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“…Normal taste function recovers by day 2 in control-fed animals, but persists indefinitely in sodium-deficient rats (Wall and McCluskey, 2008). These changes occur before the bilateral macrophage response to injury, and are inconsistent with findings that macrophage levels predict normal taste responses (McCluskey, 2004, Cavallin and McCluskey, 2005, Guagliardo et al, 2009). Thus, we hypothesized that another leukocyte population mediates early functional deficits in uninjured taste receptor cells.…”

contrasting

confidence: 83%

“…We also determined whether LPS initiated macrophage entry to the tongue, since these leukocytes are predictive of normal sodium taste function after injury (McCluskey, 2004, Cavallin and McCluskey, 2005, Guagliardo et al, 2009). ED1 + activated macrophages were elevated on the uninjected (p = 0.03) but not the injected side of the tongue (p>0.05) compared to PBS-injected controls (not shown).…”

Section: Resultsmentioning

confidence: 99%

“…Converging evidence has suggested that the immune response to injury plays an important role in early functional changes in the neighboring, intact taste receptor cells (Phillips and Hill, 1996, Hendricks et al, 2002, McCluskey, 2004, Cavallin and McCluskey, 2005, Cavallin and McCluskey, 2007a, Guagliardo et al, 2009). In the current study, we identify immune cells that mediate changes in sodium taste function soon after CT nerve injury.…”

Section: Discussionmentioning

confidence: 99%

“…The specificity of neutrophil depletion was determined by staining macrophages with mouse anti-rat ED1 (1:400; ABD Serotec). Immunohistochemistry and analyses were performed according to previously published methods (McCluskey, 2004, Cavallin and McCluskey, 2005, Guagliardo et al, 2009). …”

Section: Methodsmentioning

confidence: 99%

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Neutrophil responses to injury or inflammation impair peripheral gustatory function

Steen¹,

Shi²,

He³

et al. 2010

Neuroscience

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The adult peripheral taste system is capable of extensive functional plasticity after injury. Sectioning the chorda tympani (CT), a primary sensory afferent nerve, elicits transient changes in the uninjured, contralateral population of taste receptor cells. Remarkably, the deficits are specific to the sodium transduction pathway. Normal function is quickly restored in the intact nerve, in parallel with an influx of macrophages to both the denervated and uninjured sides of the tongue. However, changing the dietary environment by restricting sodium blocks the macrophage response and prolongs functional alterations. Since the functional deficits occur before macrophages are present in the peripheral taste system, we hypothesized that neutrophils play a role in modulating neural responses in the intact CT. First, the dynamics of the neutrophil response to nerve injury were analyzed in control-fed and sodium-deficient rats. Nerve sectioning briefly increased the number of neutrophils on both the denervated and uninjured sides of the tongue. The low-sodium diet amplified and extended the bilateral neutrophil response to injury, in parallel with the persistent changes in sodium taste function. To test the impact of neutrophils on taste function, we depleted these cells prior to nerve sectioning and recorded neural responses from the intact CT. This treatment restored normal sodium responses in the uninjured nerve. Moreover, recruiting neutrophils to the tongue induced deficits in sodium taste function in both CT nerves. Neutrophils play a critical role in ongoing inflammatory responses in the oral cavity, and may induce changes in taste perception. We also suggest that balanced neutrophil and macrophage responses enable normal neural responses after neural injury.

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Functional role for interleukin‐1 in the injured peripheral taste system

Shi

Sarvepalli

et al. 2012

J of Neuroscience Research

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The peripheral taste system presents an excellent model for studying the consequences of neural injury, for the damaged nerve and sensory cells and the neighboring, intact neural cells. Sectioning a primary afferent nerve, the chorda tympani (CT), rapidly recruits neutrophils to both sides of the tongue. The bilateral neutrophil response induces transient functional deficits in the intact CT. Normal function is subsequently restored as macrophages respond to injury. We hypothesized that macrophages produce the proinflammatory cytokine, interleukin (IL)-1, which contributes to the maintenance of normal taste function after nearby injury. We demonstrate that IL-1β protein levels are significantly increased on the injured side of the tongue at day 2 after injury. Dietary sodium deficiency, a manipulation which prevents macrophage recruitment, inhibits the elevation in IL-1β. IL-1β was expressed in several cell populations, including taste receptor cells and infiltrating neutrophils and macrophages. To test whether IL-1 modulates taste function after injury, we blocked signaling with an IL-1 receptor antagonist (IL-1 RA) and recorded taste responses from the intact CT. This treatment inhibited the bilateral macrophage response to injury, and impaired taste responses in the intact CT. Cytokine actions in the taste system are largely unstudied. These results demonstrate that IL-1 has a beneficial effect on taste function after nearby injury, in contrast to its detrimental role in the injured central nervous system (CNS).

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Attenuation of peripheral salt taste responses and local immune function contralateral to gustatory nerve injury: effects of aldosterone

Cited by 10 publications

References 46 publications

BDNF is required for taste axon regeneration following unilateral chorda tympani nerve section

BDNF is required for taste axon regeneration following unilateral chorda tympani nerve section

Neutrophil responses to injury or inflammation impair peripheral gustatory function

Functional role for interleukin‐1 in the injured peripheral taste system

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