Gut Microbiota Mediate the Neuroprotective Effect of Oolong Tea Polyphenols in Cognitive Impairment Induced by Circadian Rhythm Disorder

J Agric Food Chem. 2024 May 29;72(21):12184-12197. doi: 10.1021/acs.jafc.4c01922. Epub 2024 May 14.

Abstract

Oolong tea polyphenols (OTP) have attracted wide attention due to their ability to reduce inflammatory response, regulate gut microbiota, and improve cognitive function. However, exactly how the gut microbiota modulates nervous system activity is still an open question. We previously expounded that supplementing with OTP alleviated neuroinflammation in circadian rhythm disorder (CRD) mice. Here, we showed that OTP can relieve microglia activation by reducing harmful microbial metabolites lipopolysaccharide (LPS) that alleviate CRD-induced cognitive decline. Mechanistically, OTP suppressed the inflammation response by regulating the gut microbiota composition, including upregulating the relative abundance of Muribaculaceae and Clostridia_UCG-014 and downregulating Desulfovibrio, promoting the production of short-chain fatty acids (SCFAs). Moreover, the use of OTP alleviated intestinal barrier damage and decreased the LPS transport to the serum. These results further inhibited the activation of microglia, thus alleviating cognitive impairment by inhibiting neuroinflammation, neuron damage, and neurotoxicity metabolite glutamate elevation. Meanwhile, OTP upregulated the expression of synaptic plasticity-related protein postsynaptic density protein 95 (PSD-95) and synaptophysin (SYN) by elevating the brain-derived neurotrophic factor (BDNF) level. Taken together, our findings suggest that the OTP has the potential to prevent CRD-induced cognition decline by modulating gut microbiota and microbial metabolites.

Keywords: cognition; gut microbiota; microglia; synaptic plasticity; tea polyphenols.

MeSH terms

  • Animals
  • Bacteria / classification
  • Bacteria / drug effects
  • Bacteria / genetics
  • Bacteria / metabolism
  • Brain-Derived Neurotrophic Factor / genetics
  • Brain-Derived Neurotrophic Factor / metabolism
  • Camellia sinensis* / chemistry
  • Chronobiology Disorders* / drug therapy
  • Chronobiology Disorders* / metabolism
  • Chronobiology Disorders* / physiopathology
  • Cognitive Dysfunction* / drug therapy
  • Cognitive Dysfunction* / etiology
  • Cognitive Dysfunction* / metabolism
  • Cognitive Dysfunction* / prevention & control
  • Gastrointestinal Microbiome* / drug effects
  • Humans
  • Male
  • Mice
  • Mice, Inbred C57BL*
  • Microglia / drug effects
  • Microglia / metabolism
  • Neuroprotective Agents* / pharmacology
  • Plant Extracts / administration & dosage
  • Plant Extracts / chemistry
  • Plant Extracts / pharmacology
  • Polyphenols* / administration & dosage
  • Polyphenols* / pharmacology
  • Tea* / chemistry

Substances

  • Polyphenols
  • Tea
  • Neuroprotective Agents
  • Brain-Derived Neurotrophic Factor
  • Plant Extracts