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Regulatory Effects and Mechanisms of L-Theanine on Neurotransmitters via Liver–Brain Axis Under a High Protein Diet

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Abstract

Excessive protein intake causes liver and brain damage and neurotransmitter disorders, thereby inducing cognitive dysfunction. L-theanine can regulate the neurotransmitter content and show great potential in liver and brain protection. However, it remains unclear whether l-theanine effectively regulates neurotransmitter content under high-protein diet. A 40-day feeding experiment was performed in Sprague Dawley rats to investigate the regulatory effects and mechanisms of l-theanine on neurotransmitters via liver–brain axis in high-protein diets. The results showed that a 30% protein diet increased the liver and brain neurotransmitter content while maintaining the normal structure of liver and the hippocampal CA1 of brain and improving the autonomous behavior of rats. In contrast, 40% and 50% protein diets decreased the content of neurotransmitters, affected autonomous behavior, destroyed the hippocampal CA1 of brain structure, increased hepatic inflammatory infiltration, lipid degeneration, and hepatocyte eosinophilic change in liver, increased liver AST, ALT, MDA, CRP, and blood ammonia level, and decreased liver SOD and CAT level. However, l-theanine improved liver and brain neurotransmitter content, autonomous behavior, liver and hippocampal brain structure, and liver biochemical indicators in 40% and 50% protein diets. To explore how LTA can eliminate the adverse effects of a high-protein diet, we analyzed different metabolites and proteomes and using western blotting for validate quantitatively. We found that l-theanine regulates the activity of PF4 and G protein subunit alpha i2, increases the content of brain-derived neurotrophic factor and dopamine under a 20% protein diet. In addition, l-theanine can activate the adenylate cyclase-protein kinase A pathway through the protein alpha/beta-hydrolase domain protein 12 to regulate the content of neurotransmitters under a 40% protein diet, thereby exerting a neuroprotective effect.

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Data Availability

The datasets generated and analyzed during the current study are available from the corresponding author on reasonable request.

Abbreviations

LTA:

L-theanine

HPD:

High protein diet

AST:

Aspartate aminotransferase

ALT:

Alanine aminotransferase

CAT:

Catalase

MDA:

Malonic dialdehyde

T-SOD:

Total superoxide dismutase

CRP:

C-reactive protein

NE:

Norepinephrine

DA:

Dopamine

5-HT:

5-Hydroxytryptamine

Glu:

Glutamic acid

ACh:

Acetylcholine

GABA:

γ-Aminobutyric acid

BDNF:

Brain-derived neurotrophic factor

AC:

Adenylate cyclase

PKA:

Protein kinase A

GNAI2:

G protein subunit alpha i2

ABHD12:

Alpha/beta-hydrolase domain protein 12

OFT:

Open-field test

LDT:

Light-dark box test

HE:

Hematoxylin-eosin

NS:

Nissl stain

2-AG:

2-Arachidonoyl glycerol

AEA:

Arachidonoyl ethanolamide

PF4:

PLF4_RAT

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Acknowledgements

We would like to thank Editage for English language editing.

Funding

This work was supported by the Natural Science Foundation of Hunan Province, China(2020JJ4036)， National Key Research and Development Program of China (2017YFD0400803), and the key R&D program of Hunan Province (2021NK2016).

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Authors and Affiliations

  1. Key Laboratory of Tea Science of Ministry of Education, Hunan Agricultural University, Changsha, 410128, Hunan, China

    Wei Xu, Yuxin Song, Wenjun Xiao & Zhihua Gong

  2. National Research Center of Engineering and Technology for Utilization of Botanical Functional Ingredients, Hunan Agricultural University, Changsha, 410128, Hunan, China

    Wei Xu, Yuxin Song, Wenjun Xiao & Zhihua Gong

  3. Co-Innovation Center of Education Ministry for Utilization of Botanical Functional Ingredients, Changsha, China

    Wei Xu, Yuxin Song, Wenjun Xiao & Zhihua Gong

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  1. Wei Xu
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All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Wei Xu and Yuxin Song. The first draft of the manuscript was written by Wei Xu and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Wenjun Xiao or Zhihua Gong.

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All experimental procedures and animal care were performed in strict accordance with the NIH guidelines for the care and use of laboratory animals (NIH Publication no. 85-23 Rev. 1985). The protocols were approved by the Ethics Committee of Hunan Agriculture University (registry number: 015063506, Changsha, China).

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Xu, W., Song, Y., Xiao, W. et al. Regulatory Effects and Mechanisms of L-Theanine on Neurotransmitters via Liver–Brain Axis Under a High Protein Diet. Mol Neurobiol 61, 783–798 (2024). https://doi.org/10.1007/s12035-023-03608-0

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