Synaptic Connections in Developing and Adult Rat Taste Buds

Kinnamon, John C.; Dunlap, Mary K.; Yang, Rong

doi:10.1093/chemse/bjh113

Cited by 5 publications

(5 citation statements)

References 7 publications

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“…Therefore, it would not be surprising if some developmental remodeling were required for taste receptor cells to be innervated by the appropriate nerve fibers. Consistent with this idea, taste innervation is reduced postnatally in the rat and sheep in a manner that suggests reorganization (Kinnamon et al, 2005; Mistretta et al, 1988; Nagai et al, 1988). …”

Section: Introductionmentioning

confidence: 66%

“…As with many other systems (Erzurumlu and Kind, 2001; Espinosa and Stryker, 2012; Marks et al, 2006; Walsh and Lichtman, 2003), postnatal remodeling is likely required for the formation of a mature taste bud with appropriate connections between taste receptor cells and gustatory neurons (Kinnamon et al, 2005; Mistretta et al, 1988; Nagai et al, 1988; Yuan and Yankner, 2000). BDNF regulates this remodeling in other systems (Cabelli et al, 1997; Gonzalez et al, 1999; Kaneko et al, 2008), and in the gustatory system is expressed in postnatal and adult taste buds (Huang and Krimm, 2010).…”

Section: Discussionmentioning

confidence: 99%

“…In sheep, the receptive fields of individual chorda tympani axons are reduced during postnatal development, demonstrating that branching between individual fungiform papillae is reduced (Mistretta et al, 1988; Nagai et al, 1988). In rat, circumvallate taste buds are initially hyper-innervated, and the nerve plexus contains neuro-neuronal synapses (Kinnamon et al, 2005). This plexus decreases in size and neuro-neuronal synapses are lost during postnatal development, which implies reorganization.…”

Section: Discussionmentioning

confidence: 99%

“…Remodeling is not required for neurons to make initial connections with taste buds. However, following initial innervation, taste buds continue to grow and differentiate postnatally (Bigiani et al, 2002; Hosley and Oakley, 1987; Kinnamon et al, 2005; Ohtubo et al, 2012; Zhang et al, 2008), resulting in an adult taste bud that has multiple different cell types based on anatomy, function, and expression (Clapp et al, 2006; Clapp et al, 2004; Delay et al, 1986; Finger, 2005; Kataoka et al, 2008; Murray and Murray, 1967; Murray et al, 1969; Yang et al, 2000a; Yang et al, 2000b; Yee et al, 2001). Therefore, it would not be surprising if some developmental remodeling were required for taste receptor cells to be innervated by the appropriate nerve fibers.…”

Section: Introductionmentioning

confidence: 99%

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Postnatal reduction of BDNF regulates the developmental remodeling of taste bud innervation

Huang

Krimm

2015

Developmental Biology

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The refinement of innervation is a common developmental mechanism that serves to increase the specificity of connections following initial innervation. In the peripheral gustatory system, the extent to which innervation is refined and how refinement might be regulated is unclear. The initial innervation of taste buds is controlled by brain-derived neurotrophic factor (BDNF). Following initial innervation, taste receptor cells are added and become newly innervated. The connections between the taste receptor cells and nerve fibers are likely to be specific in order to retain peripheral coding mechanisms. Here, we explored the possibility that the down-regulation of BDNF regulates the refinement of taste bud innervation during postnatal development. An analysis of BDNF expression in BdnflacZ/+ mice and real-time reverse transcription polymerase chain reaction (RT-PCR) revealed that BDNF was down-regulated between postnatal day (P) 5 and P10. This reduction in BDNF expression was due to a loss of precursor/progenitor cells that express BDNF, while the expression of BDNF in the subpopulations of taste receptor cells did not change. Gustatory innervation, which was identified by P2X3 immunohistochemistry, was lost around the perimeter where most progenitor/precursor cells are located. In addition, the density of innervation in the taste bud was reduced between P5 and P10, because taste buds increase in size without increasing innervation. This reduction of innervation density was blocked by the overexpression of BDNF in the precursor/progenitor population of taste bud cells. Together these findings indicate that the process of BDNF restriction to a subpopulation of taste receptor cells between P5 and P10, results in a refinement of gustatory innervation. We speculate that this refinement results in an increased specificity of connections between neurons and taste receptor cells during development.

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Section: Introductionmentioning

confidence: 66%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Postnatal reduction of BDNF regulates the developmental remodeling of taste bud innervation

Huang

Krimm

2015

Developmental Biology

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“…Our findings suggest the reinterpretation of an earlier study in which BDNF overexpression in α-gustducin-expressing taste receptor cells slightly increased innervation to taste buds ( Nosrat et al, 2012 ). BDNF overexpression likely begins at birth in these mice ( Ohtubo et al, 2012 ), and because remodeling likely occurs during postnatal peripheral gustatory development ( Nagai et al, 1988 ; Kinnamon et al, 2005 ; Huang et al, 2015 ), BDNF overexpression under the control of a gustducin promoter could increase innervation via multiple mechanisms, including prevention of postnatal remodeling ( Huang et al, 2015 ). However, because α-gustducin-expressing taste cells do not normally express BDNF ( Yee et al, 2003 ), BDNF expressed in these taste receptor cells could have attracted abnormal amounts or types of innervation in adulthood.…”

Section: Discussionmentioning

confidence: 99%

Taste Bud-Derived BDNF Is Required to Maintain Normal Amounts of Innervation to Adult Taste Buds

Meng

Ohman-Gault

et al. 2015

eneuro

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Gustatory neurons transmit chemical information from taste receptor cells, which reside in taste buds in the oral cavity, to the brain. As adult taste receptor cells are renewed at a constant rate, nerve fibers must reconnect with new taste receptor cells as they arise. Therefore, the maintenance of gustatory innervation to the taste bud is an active process. Understanding how this process is regulated is a fundamental concern of gustatory system biology. We speculated that because brain-derived neurotrophic factor (BDNF) is required for taste bud innervation during development, it might function to maintain innervation during adulthood. If so, taste buds should lose innervation when Bdnf is deleted in adult mice. To test this idea, we first removed Bdnf from all cells in adulthood using transgenic mice with inducible CreERT2 under the control of the Ubiquitin promoter. When Bdnf was removed, approximately one-half of the innervation to taste buds was lost, and taste buds became smaller because of the loss of taste bud cells. Individual taste buds varied in the amount of innervation each lost, and those that lost the most innervation also lost the most taste bud cells. We then tested the idea that that the taste bud was the source of this BDNF by reducing Bdnf levels specifically in the lingual epithelium and taste buds. Taste buds were confirmed as the source of BDNF regulating innervation. We conclude that BDNF expressed in taste receptor cells is required to maintain normal levels of innervation in adulthood.

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Ultrastructure of Taste Buds

Kinnamon

Yang

2008

The Senses: A Comprehensive Reference

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Synaptic Connections in Developing and Adult Rat Taste Buds

Cited by 5 publications

References 7 publications

Postnatal reduction of BDNF regulates the developmental remodeling of taste bud innervation

Postnatal reduction of BDNF regulates the developmental remodeling of taste bud innervation

Taste Bud-Derived BDNF Is Required to Maintain Normal Amounts of Innervation to Adult Taste Buds

Ultrastructure of Taste Buds

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