Landon Shannon M, Holder Emily, Ng Amber, Wood Ryan, Kuri Eduardo Gutierrez, Humayun Saima, Pinto Laura Bordallo, Macpherson Lindsey J
Department of Neuroscience, Developmental and Regenerative Biology, The University of Texas at San Antonio, One UTSA Circle, San Antonio, Texas, United States of America.
Brain Health Consortium, The University of Texas at San Antonio, One UTSA Circle, San Antonio, Texas, United States of America.
PLoS One. 2025 Jun 3;20(6):e0325312. doi: 10.1371/journal.pone.0325312. eCollection 2025.
The turnover and re-establishment of peripheral taste synapses is vital to maintain connectivity between primary taste receptor cells and the gustatory neurons which relay taste information from the tongue to the brain. Despite the importance of neuron-taste cell reconnection, the mechanisms governing synapse assembly in the taste bud are largely unknown. To determine whether nerve fiber connectivity is an initiating factor for the recruitment of presynaptic machinery in taste receptor cells, we use the expression of CALHM1 and Bassoon to identify presynaptic sites in type II (sweet, umami, bitter) and type III (sour) taste receptor cells, respectively. Under homeostatic conditions, the vast majority (>90%) of presynaptic sites are directly adjacent to nerve fibers (contacted). In the days immediately following gustatory nerve transection and denervation of taste buds, Bassoon and CALHM1 puncta are markedly reduced. This suggests that nerve fiber innervation is crucial for the recruitment and maintenance of presynaptic sites. During nerve fiber regeneration into the taste bud, presynaptic sites begin to replenish but are not as frequently contacted by nerve fibers as intact controls (35-54% compared to >90%). This reveals that taste cells rely on gustatory fiber innervation to organize presynaptic sites. Additionally, our finding that presynaptic sites are not as frequently contacted by regenerating axons suggests a model whereby trophic factors secreted by gustatory nerve fibers prompt taste receptor cells to produce and/or aggregate presynaptic specializations at the cell membrane prior to contact. This, in turn, may guide neurons to form mature synapses. These findings provide new insights into the mechanisms driving synaptogenesis and synaptic plasticity within the rapidly changing taste bud environment.
外周味觉突触的更新和重建对于维持初级味觉受体细胞与将味觉信息从舌头传递至大脑的味觉神经元之间的连接至关重要。尽管神经元-味觉细胞重新连接很重要，但味蕾中突触组装的调控机制在很大程度上仍不清楚。为了确定神经纤维连接是否是味觉受体细胞中突触前机制募集的起始因素，我们分别利用CALHM1和巴松管的表达来鉴定II型（甜味、鲜味、苦味）和III型（酸味）味觉受体细胞中的突触前位点。在稳态条件下，绝大多数（>90%）突触前位点直接与神经纤维相邻（接触）。在味觉神经横断和味蕾去神经支配后的几天内，巴松管和CALHM1点状结构明显减少。这表明神经纤维支配对于突触前位点的募集和维持至关重要。在神经纤维向味蕾再生的过程中，突触前位点开始补充，但与完整对照相比，神经纤维与之接触的频率较低（完整对照>90%，再生时为35-54%）。这表明味觉细胞依赖味觉纤维支配来组织突触前位点。此外，我们发现再生轴突与突触前位点的接触频率较低，这提示了一种模型，即味觉神经纤维分泌的营养因子促使味觉受体细胞在接触前在细胞膜上产生和/或聚集突触前特化结构。反过来，这可能引导神经元形成成熟的突触。这些发现为快速变化的味蕾环境中驱动突触形成和突触可塑性的机制提供了新的见解。
