Aged black tea alleviates constipation in mice by modulating intestinal neurotransmitters and decreasing AQP3 and AQP9 expression

Yu Wu; Qiuhua Li; Junxi Cao; Fenling Fan; Lishe Gan; Rihui Wu; Jingwei Jin; Ruohong Chen; Lingli Sun; Zhenbiao Zhang; Xingfei Lai; Wing-Leung Wong; Shili Sun; Dongli Li

doi:10.29219/fnr.v67.9513

Yu Wu School of Biotechnology and Health Sciences, Wuyi University, Jiangmen, China
Qiuhua Li Tea Research Institute, Guangdong Academy of Agricultural Sciences / Guangdong Provincial Key Laboratory of Tea Plant Resources Innovation & Utilization, Guangzhou, China
Junxi Cao Tea Research Institute, Guangdong Academy of Agricultural Sciences / Guangdong Provincial Key Laboratory of Tea Plant Resources Innovation & Utilization, Guangzhou, China
Fenling Fan School of Biotechnology and Health Sciences, Wuyi University, Jiangmen, China
Lishe Gan School of Biotechnology and Health Sciences, Wuyi University, Jiangmen, China; and International Healthcare Innovation Institute (Jiangmen), Jiangmen, China
Rihui Wu School of Biotechnology and Health Sciences, Wuyi University, Jiangmen, China; and International Healthcare Innovation Institute (Jiangmen), Jiangmen, China
Jingwei Jin School of Biotechnology and Health Sciences, Wuyi University, Jiangmen, China; and International Healthcare Innovation Institute (Jiangmen), Jiangmen, China
Ruohong Chen Tea Research Institute, Guangdong Academy of Agricultural Sciences / Guangdong Provincial Key Laboratory of Tea Plant Resources Innovation & Utilization, Guangzhou, China
Lingli Sun Tea Research Institute, Guangdong Academy of Agricultural Sciences / Guangdong Provincial Key Laboratory of Tea Plant Resources Innovation & Utilization, Guangzhou, China
Zhenbiao Zhang Tea Research Institute, Guangdong Academy of Agricultural Sciences / Guangdong Provincial Key Laboratory of Tea Plant Resources Innovation & Utilization, Guangzhou, China
Xingfei Lai Tea Research Institute, Guangdong Academy of Agricultural Sciences / Guangdong Provincial Key Laboratory of Tea Plant Resources Innovation & Utilization, Guangzhou, China
Wing-Leung Wong School of Biotechnology and Health Sciences, Wuyi University, Jiangmen, China
Shili Sun Tea Research Institute, Guangdong Academy of Agricultural Sciences / Guangdong Provincial Key Laboratory of Tea Plant Resources Innovation & Utilization, Guangzhou, China
Dongli Li School of Biotechnology and Health Sciences, Wuyi University, Jiangmen, China; and International Healthcare Innovation Institute (Jiangmen), Jiangmen, China

DOI: https://doi.org/10.29219/fnr.v67.9513

Keywords: aged black tea, constipation, intestinal neurotransmitter, AQP3, AQP9

Abstract

Background: Black tea is fully fermented tea with abundant functional components that benefit the gastrointestinal tract. But whether black tea extract relieves constipation is unknown. Therefore, we used loperamide to induce constipation in mice to assess the therapeutical effect of extracts from aged black tea with different storage times.

Design: Sixty-three C57BL/6J male mice were randomly divided into Control group (Con), Model group (Mod), Positive group (Pos), aged 6 years group (15Y), aged 4 years group (17Y), aged 2 years group (19Y), and unaged group (21Y). Mice were given loperamide (20 mg/kg, twice a day) to induce constipation for 10 days, and black tea extracts (500 mg/kg) were intragastrically given for 7 days while continuing modeling.

Results: The results showed that black tea extracts relieved constipation symptoms by improving defecation weight, fecal water content, and gastrointestinal transit rate. Black tea extracts can also protect colon tissue, regulate serum neurotransmitters, increase the levels of excitatory neurotransmitters motilin (MTL) and substance P (SP), and decrease the levels of inhibitory neurotransmitters vasoactive intestinal peptide (VIP) and nitric oxide (NO). Immunohistochemistry (IHC) showed that black tea extracts were able to reduce AQP3 and AQP9 expression in the colon of constipated mice. In addition, Reverse transcription-quantitative polymerase chain reaction (RT-qPCR) showed that black tea extracts could decrease AQP3 and AQP9 mRNA expression. The relief effect of aged black tea (15Y) with the longest storage was better than that of other years, which may be due to the role of active ingredients such as thearubigins (TRs), soluble sugar, tea polysaccharide (TPS), gallic acid (GA), and catechin gallate (CG) in aged black tea.

Conclusions: Based on these results, we believe that regular consumption of black tea is effective in relieving constipation, and that black tea is more effective in relieving constipation as the storage time increases.

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References

1.
Rao SSC, Rattanakovit K, Patcharatrakul T. Diagnosis and management of chronic constipation in adults. Nat Rev Gastroenterol Hepatol 2016; 13(5): 295–305. doi: 10.1038/nrgastro.2016.53

2.
Chu H, Zhong L, Li H, Zhang X, Zhang J, Hou X. Epidemiology characteristics of constipation for general population, pediatric population, and elderly population in china. Gastroenterol Res Pract 2014; 2014: 532734. doi: 10.1155/2014/532734

3.
Costilla VC, Foxx-Orenstein AE. Constipation: understanding mechanisms and management. Clin Geriatr Med 2014; 30(1): 107–15. doi: 10.1016/j.cger.2013.10.001

4.
Song H, Peng JS, Yang ZL, Xiang J, Wu XB, Wang HS, et al. Assessment of the psychological status of patients with functional constipation in Chinese population: a meta-analysis. Chin Gen Pract 2011; 14(25): 2930–2+6.

5.
Zhu S, Ran J, Yang B, Mei Z. Aquaporins in digestive system. Adv Exp Med Biol 2017; 969: 123–30. doi: 10.1007/978-94-024-1057-0_8

6.
Lin XY, Liu BY, Yi J, Cai GX. Effect of Simo Decoction on gastrointestinal motility and MTL, SS of mice with different models. China J Tradit Chin Med Pharm 2013; 28(3): 772–4.

7.
Hwang DY, Kim S, Hong HS. Substance-P ameliorates dextran sodium sulfate-induced intestinal damage by preserving tissue barrier function. Tissue Eng Regen Med 2018; 15(1): 63–73. doi: 10.1007/s13770-017-0085-7

8.
Cao PQ, Li XP, Ou-Yang J, Jiang RG, Huang FF, Wen BB, et al. The protective effects of yellow tea extract against loperamide-induced constipation in mice. Food Funct 2021; 12(12): 5621–36. doi: 10.1039/d0fo02969f

9.
Tomita R, Fujisaki S, Ikeda T, Fukuzawa M. Role of nitric oxide in the colon of patients with slow-transit constipation. Dis Colon Rectum 2002; 45(5): 593–600. doi: 10.1007/s10350-004-6251-8

10.
Zhao Q, Chen YY, Xu DQ, Yue SJ, Fu RJ, Yang J, et al. Action mode of gut motility, fluid and electrolyte transport in chronic constipation. Front Pharmacol 2021; 12: 630249. doi: 10.3389/fphar.2021.630249

11.
Ikarashi N, Kon R, Sugiyama K. Aquaporins in the colon as a new therapeutic target in diarrhea and constipation. Int J Mol Sci 2016; 17(7): 1172. doi: 10.3390/ijms17071172

12.
Okada S, Misaka T, Matsumoto I, Watanabe H, Abe K. Aquaporin-9 is expressed in a mucus-secreting goblet cell subset in the small intestine. FEBS Lett 2003; 540(1–3): 157–62. doi: 10.1016/s0014-5793(03)00256-4

13.
Meng Y, Li X, Wang X, Zhang L, Guan J. Network pharmacological prediction and molecular docking analysis of the combination of Atractylodes macrocephala Koidz. and Paeonia lactiflora Pall. in the treatment of functional constipation and its verification. Anim Model Exp Med 2022; 5(2): 120–32. doi: 10.1002/ame2.12226

14.
Zuo ZK, Han JR, Ji SL, He LL. Exploration of the effect of the brain-intestinal axis based on kidney-intestinal tonic formula on the expression of AQP3 and AQP9 in the colon of aged rats with slow-transmission constipation. Chin J Gerontol 2022: 2215–20.

15.
Hu TG, Wen P, Fu HZ, Lin GY, Liao ST, Zou YX. Protective effect of mulberry (Morus atropurpurea) fruit against diphenoxylate-induced constipation in mice through the modulation of gut microbiota. Food Funct 2019; 10(3): 1513–28. doi: 10.1039/c9fo00132h

16.
Tack J, van Outryve M, Beyens G, Kerstens R, Vandeplassche L. Prucalopride (Resolor) in the treatment of severe chronic constipation in patients dissatisfied with laxatives. Gut 2009; 58(3): 357–65. doi: 10.1136/gut.2008.162404

17.
Busti AJ, Murillo JR, Jr., Cryer B. Tegaserod-induced myocardial infarction: case report and hypothesis. Pharmacotherapy 2004; 24(4): 526–31. doi: 10.1592/phco.24.5.526.33351

18.
Kapp JM, Sumner W. Kombucha: a systematic review of the empirical evidence of human health benefit. Ann Epidemiol 2019; 30: 66–70. doi: 10.1016/j.annepidem.2018.11.001

19.
Samanta S. Potential bioactive components and health promotional benefits of tea (Camellia sinensis). J Am Nutr Assoc 2022; 41(1): 65–93. doi: 10.1080/07315724.2020.1827082

20.
Tanaka T, Matsuo Y. Production mechanisms of black tea polyphenols. Chem Pharm Bull 2020; 68(12): 1131–42. doi: 10.1248/cpb.c20-00295

21.
Li G, Wang Q, Qian Y, Zhou Y, Wang R, Zhao X. Component analysis of Pu-erh and its anti-constipation effects. Mol Med Rep 2014; 9(5): 2003–9. doi: 10.3892/mmr.2014.2009

22.
Huang G, Z., Lai Z, X. A brief talk on development prospect of aged tea production in guangdong compilation of guangdong tea industry development forum (2005). 2005, pp. 153–5.

23.
Black CJ, Drossman DA, Talley NJ, Ruddy J, Ford AC. Functional gastrointestinal disorders: advances in understanding and management. Lancet 2020; 396(10263): 1664–74. doi: 10.1016/S0140-6736(20)32115-2

24.
Argoff CE, Brennan MJ, Camilleri M, Davies A, Fudin J, Galluzzi KE, et al. Consensus recommendations on initiating prescription therapies for opioid-induced constipation. Pain Med 2015; 16(12): 2324–37. doi: 10.1111/pme.12937

25.
Nee J, Zakari M, Sugarman MA, Whelan J, Hirsch W, Sultan S, et al. Efficacy of treatments for opioid-induced constipation: systematic review and meta-analysis. Clin Gastroenterol Hepatol 2018; 16(10): 1569–84.e2. doi: 10.1016/j.cgh.2018.01.021

26.
Wang L, Hu L, Yan S, Jiang T, Fang S, Wang G, et al. Effects of different oligosaccharides at various dosages on the composition of gut microbiota and short-chain fatty acids in mice with constipation. Food Funct 2017; 8(5): 1966–78. doi: 10.1039/c7fo00031f

27.
Gong ZP, Ouyang J, Wu XL, Zhou F, Lu DM, Zhao CJ, et al. Dark tea extracts: chemical constituents and modulatory effect on gastrointestinal function. Biomed Pharmacother 2020; 130: 110514. doi: 10.1016/j.biopha.2020.110514

28.
Sharif H, Hoad CL, Abrehart N, Gowland PA, Spiller RC, Kirkham S, et al. Colonic volume changes in paediatric constipation compared to normal values measured using MRI. Diagnostics 2021; 11(6): 974. doi: 10.3390/diagnostics11060974

29.
Ikarashi N. The elucidation of the function and the expression control mechanism of aquaporin-3 in the colon. Yakugaku Zasshi 2013; 133(9): 955–61. doi: 10.1248/yakushi.13-00173

30.
Sun SL, Guo YT, Chen HQ, Liu C, LAI XF, Cao FR. Analysis of biochemical components and evaluation of the in vitro activity of six categories of tea made of Yinghong NO.9. Food Res Dev 2018; 39(9): 159–65. doi: 10.3969/j.issn.1005-6521.2018.09.030

31.
Chaudhuri L, Basu S, Seth P, Chaudhuri T, Besra SE, Vedasiromoni JR, et al. Prokinetic effect of black tea on gastrointestinal motility. Life Sci 2000; 66(9): 847–54. doi: 10.1016/s0024-3205(99)00657-8

32.
Tuohy KM, Conterno L, Gasperotti M, Viola R. Up-regulating the human intestinal microbiome using whole plant foods, polyphenols, and/or fiber. J Agric Food Chem 2012; 60(36): 8776–82. doi: 10.1021/jf2053959

33.
Huang A, Jiang Z, Tao M, Wen M, Xiao Z, Zhang L, et al. Targeted and nontargeted metabolomics analysis for determining the effect of storage time on the metabolites and taste quality of keemun black tea. Food Chem 2021; 359: 129950. doi: 10.1016/j.foodchem.2021.129950