Article

DL-3-n-butylphthalide ameliorates diabetes-associated cognitive decline by enhancing PI3K/Akt signaling and suppressing oxidative stress

Bei-ni Wang1,2, Cheng-biao Wu3, Zi-miao Chen1, Pei-pei Zheng2, Ya-qian Liu2, Jun Xiong2, Jing-yu Xu4, Pei-feng Li1, Abdullah Al Mamun2, Li-bing Ye2, Zhi-long Zheng2, Yan-qing Wu4, Jian Xiao1,2, Jian Wang1
1 Department of Hand Surgery and Peripheral Neurosurgery, The First Affiliated Hospital of Wenzhou Medical University, Wenzhou 325000, China
2 School of Pharmaceutical Science, Wenzhou Medical University, Wenzhou 325000, China
3 Research Center, Affiliated Xiangshan Hospital, Wenzhou Medical University, Ningbo 315700, China
4 The Institute of Life Sciences, Engineering Laboratory of Zhejiang province for Pharmaceutical Development of Growth Factors, Biomedical Collaborative Innovation Center of Wenzhou, Wenzhou University, Wenzhou 325035, China
Correspondence to: Yan-qing Wu: yqwu220946@yeah.net, Jian Xiao: xfxj2000@126.com, Jian Wang: jianwang0516@126.com,
DOI: 10.1038/s41401-020-00583-3
Received: 1 August 2020
Accepted: 16 November 2020
Advance online: 18 January 2021

Abstract

DL-3-n-Butylphthalide (DL-NBP), a small molecular compound extracted from the seeds of Apium graveolens Linn (Chinese celery), has been shown to exert neuroprotective effects due to its anti-inflammatory, anti-oxidative and anti-apoptotic activities. DL-NBP not only protects against ischemic cerebral injury, but also ameliorates vascular cognitive impairment in dementia patients including AD and PD. In the current study, we investigated whether and how DL-NBP exerted a neuroprotective effect against diabetes-associated cognitive decline (DACD) in db/db mice, a model of type-2 diabetes. db/db mice were orally administered DL-NBP (20, 60, 120 mg· kg−1· d−1) for 8 weeks. Then the mice were subjected to behavioral test, their brain tissue was collected for morphological and biochemical analyses. We showed that oral administration of DL-NBP significantly ameliorated the cognitive decline with improved learning and memory function in Morris water maze testing. Furthermore, DL-NBP administration attenuated diabetes-induced morphological alterations and increased neuronal survival and restored the levels of synaptic protein PSD95, synaptophysin and synapsin-1 as well as dendritic density in the hippocampus, especially at a dose of 60 mg/kg. Moreover, we revealed that DL-NBP administration suppressed oxidative stress by upregulating Nrf2/HO-1 signaling, and increased brain-derived neurotrophic factor (BDNF) expression by activating PI3K/Akt/CREB signaling in the hippocampus. These beneficial effects of DL-NBP were observed in high glucose-treated PC12 cells. Our results suggest that DL-NBP may be a potential pharmacologic agent for the treatment of DACD.
Keywords: diabetes-associated cognitive decline; DL-3-n-butylphthalide; cognitive function; hippocampus; BDNF; oxidative stress; neuroprotection

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