Department of Otolaryngology, Jikei University School of Medicine, Tokyo 105-8461, Japan.
Monell Chemical Senses Center, Philadelphia, PA 19104.
eNeuro. 2021 May 19;8(3). doi: 10.1523/ENEURO.0168-21.2021. Print 2021 May-Jun.
Loss of olfactory sensory neurons (OSNs) after injury to the olfactory epithelium (OE) triggers the generation of OSNs that are incorporated into olfactory circuits to restore olfactory sensory perception. This study addresses how insulin receptor-mediated signaling affects the functional recovery of OSNs after OE injury. Insulin levels were reduced in mice by ablating the pancreatic β cells via streptozotocin (STZ) injections. These STZ-induced diabetic and control mice were then intraperitoneally injected with the olfactotoxic drug methimazole to selectively ablate OSNs. The OE of diabetic and control mice regenerated similarly until day 14 after injury. Thereafter, the OE of diabetic mice contained fewer mature and more apoptotic OSNs than control mice. Functionally, diabetic mice showed reduced electro-olfactogram (EOG) responses and their olfactory bulbs (OBs) had fewer c-Fos-active cells following odor stimulation, as well as performed worse in an odor-guided task compared with control mice. Insulin administered intranasally during days 8-13 after injury was sufficient to rescue recovery of OSNs in diabetic mice compared with control levels, while insulin administration between days 1 and 6 did not. During this critical time window on days 8-13 after injury, insulin receptors are highly expressed and intranasal application of an insulin receptor antagonist inhibits regeneration. Furthermore, an insulin-enriched environment could facilitate regeneration even in non-diabetic mice. These results indicate that insulin facilitates the regeneration of OSNs after injury and suggest a critical stage during recovery (8-13 d after injury) during which the maturation of newly generated OSNs is highly dependent on and promoted by insulin.
嗅觉感觉神经元(OSNs)在嗅上皮(OE)损伤后丧失会触发 OSN 的产生,这些 OSN 被整合到嗅觉回路中以恢复嗅觉感觉感知。本研究探讨了胰岛素受体介导的信号如何影响 OE 损伤后 OSN 的功能恢复。通过链脲佐菌素(STZ)注射破坏胰腺β细胞来降低小鼠中的胰岛素水平。然后,将这些 STZ 诱导的糖尿病和对照小鼠通过腹膜内注射致嗅觉毒性药物甲巯咪唑来选择性地破坏 OSN。糖尿病和对照小鼠的 OE 在损伤后 14 天之前以相似的方式再生。此后,糖尿病小鼠的 OE 中成熟的 OSN 比对照小鼠少,凋亡的 OSN 比对照小鼠多。功能上,与对照小鼠相比,糖尿病小鼠在嗅觉刺激后表现出降低的电嗅觉图(EOG)反应,其嗅球(OB)中具有更少的 c-Fos 活性细胞,并且在气味引导任务中的表现也更差。与对照水平相比,在损伤后第 8-13 天期间经鼻内给予胰岛素足以挽救糖尿病小鼠中 OSN 的恢复,而在第 1-6 天期间给予胰岛素则不行。在损伤后第 8-13 天的这个关键时间窗口期间,胰岛素受体高度表达,并且经鼻内应用胰岛素受体拮抗剂抑制再生。此外,即使在非糖尿病小鼠中,富含胰岛素的环境也可以促进再生。这些结果表明胰岛素促进 OSN 在损伤后的再生,并表明在恢复期间(损伤后 8-13 天)存在一个关键阶段,在此期间,新生成的 OSN 的成熟高度依赖于并受胰岛素的促进。