Journal Home > Volume 13 , Issue 2

Probiotics have great potential in regulating intestinal pain. In this study, the effects of Lactobacillus plantarum AR495 on the visceral sensitivity and gut microbiota of irritable bowel syndrome (IBS) rats were studied. The results showed that tryptase released after mast cell activation and degranulation plays a key role in visceral pain, and L. plantarum AR495 reduced the stimulation of colonic mast cells and the expression of protease-activated receptor 2 (PAR2) and TRPV1 in dorsal root ganglia. Research further showed that supplementation with L. plantarum AR495 increased the level of short-chain fatty acids (SCFAs) and enhanced the barrier function of the colo n. In addition, the microbiota analysis of the colon indicated that L. plantarum AR495 promoted the proliferation of Bifidobacterium and inhibited the proliferation of Lachnospiraceae, which alleviated the imbalance of the intestinal microbiota caused by IBS to a certain extent. In total, L. plantarum AR495 might reduce visceral sensitivity through the Mast cell-PAR2-TRPV1 signaling pathway by maintaining the homeostasis of the intestinal barrier.


menu
Abstract
Full text
Outline
About this article

Lactobacillus plantarum AR495 improves stress-induced irritable bowel syndrome in rats by targeting gut microbiota and Mast cell-PAR2-TRPV1 signaling pathway

Show Author's information Hongyun Zhanga,Guangqiang WangaZhiqiang XiongaZhuan LiaobYangyan QianbXin SongaLi SuiaLianzhong AibYongjun Xiaa( )
Shanghai Engineering Research Center of Food Microbiology, School of Health Science and Engineering, University of Shanghai for Science and Technology, Shanghai 200093, China
Department of Gastroenterol, Digestive Endoscopy Center, Shanghai Hospital, Shanghai 200093, China

Peer review under responsibility of Tsinghua University Press.

Highlights

1. L. plantarum AR495 decreased the visceral sensitivity of the IBS group

2. L. plantarum AR495 restrained the degranulation of mast cells in the colon

3. L. plantarum AR495 prevented the destruction of colon barrier function

4. L. plantarum AR495 increased the SCFAs and the abundance of Bifidobacterium

5. L. plantarum AR495 inhibited the mast cells-tryptase-PAR2-TRPV1 pathway

Abstract

Probiotics have great potential in regulating intestinal pain. In this study, the effects of Lactobacillus plantarum AR495 on the visceral sensitivity and gut microbiota of irritable bowel syndrome (IBS) rats were studied. The results showed that tryptase released after mast cell activation and degranulation plays a key role in visceral pain, and L. plantarum AR495 reduced the stimulation of colonic mast cells and the expression of protease-activated receptor 2 (PAR2) and TRPV1 in dorsal root ganglia. Research further showed that supplementation with L. plantarum AR495 increased the level of short-chain fatty acids (SCFAs) and enhanced the barrier function of the colo n. In addition, the microbiota analysis of the colon indicated that L. plantarum AR495 promoted the proliferation of Bifidobacterium and inhibited the proliferation of Lachnospiraceae, which alleviated the imbalance of the intestinal microbiota caused by IBS to a certain extent. In total, L. plantarum AR495 might reduce visceral sensitivity through the Mast cell-PAR2-TRPV1 signaling pathway by maintaining the homeostasis of the intestinal barrier.

Keywords: Microbiota, Dorsal root ganglia, Lactobacillus plantarum, Irritable bowel syndrome, Visceral sensitivity, Tryptase

References(49)

[1]

K. Angmo, A. Kumari, Savitri, et al., Probiotic characterization of lactic acid bacteria isolated from fermented foods and beverage of Ladakh, LWT-Food Sci. Technol. 66 (2016) 428-435. https://doi.org/10.1016/j.lwt.2015.10.057.

[2]

I. Bhushan, M. Sharma, M. Mehta, et al., Bioactive compounds and probiotics–a ray of hope in COVID-19 management, Food Sci. Hum. Wellness 10 (2021) 131-140. https://doi.org/10.1016/j.fshw.2021.02.001.

[3]

T. Wang, P.P. Wang, W.P. Ge, et al., The probiotic Companilactobacillus crustorum MN047 alleviates colitis-associated tumorigenesis via modulating the intestinal microenvironment, Food Funct. 12 (2021). https://doi.org/10.1039/D1FO01531A.

[4]

B.M. Daliri, B.H. Lee, New perspectives on probiotics in health and disease, Food Sci. Hum. Wellness 4(2) (2015) 56-65. https://doi.org/10.1016/j.fshw.2015.06.002.

[5]

Y. Xia, Y. Chen, G. Wang, et al., Lactobacillus plantarum AR113 alleviates DSS-induced colitis by regulating the TLR4/MyD88/NF-κB pathway and gut microbiota composition, J. Funct. Foods 67 (2020) 103854. https://doi.org/10.1016/j.jff.2020.103854.

[6]

D. Das, A. Goyal, Antioxidant activity and γ-aminobutyric acid (GABA) producing ability of probiotic Lactobacillus plantarum DM5 isolated from Marcha of Sikkim, LWT-Food Sci. Technol. 61 (2015) 263-268. https://doi.org/10.1016/j.lwt.2014.11.013.

[7]

Q.S. Wang, Y.L. Wang, W.Y. Zhang, et al., Puerarin from Pueraria lobata alleviates the symptoms of irritable bowel syndrome-diarrhea, Food Funct. 12 (2021) 2211. https://doi.org/10.1039/D0FO02848G.

[8]

E. Zannini, E.K. Arendt, Low FODMAPs and gluten-free foods for irritable bowel syndrome treatment: lights and shadows, Food Res. Int. 110 (2017) 33-41. https://doi.org/10.1016/j.foodres.2017.04.001.

[9]

M.I. Pinto-Sanchez, G.B. Hall, K. Ghajar, et al., Probiotic Bifidobacterium longum NCC3001 reduces depression scores and alters brain activity: a pilot study in patients with irritable bowel syndrome, Gastroenterol. 153(2) (2017) 448. https://doi.org/10.1053/j.gastro.2017.05.003..

[10]

T. Ringel-Kulka, J.R. Goldsmith, I.M. Carroll, et al., Lactobacillus acidophilus NCFM affects colonic mucosal opioid receptor expression in patients with functional abdominal pain - a randomised clinical study, Aliment. Pharmacol 40(2) (2014) 200-207. https://doi.org/10.1111/apt.12800.

[11]

B. Fba, B. NL, A. Tdmt, et al., In vitro modulation of human gut microbiota composition and metabolites by Bifidobacterium longum BB-46 and a citric pectin, Food Res. Int. 120 (2019) 595-602. https://doi.org/10.1016/j.foodres.2018.11.010.

[12]

C.L. Williams, R.G. Villar, J.M. Peterso, et al., Stress-induced changes in intestinal transit in the rat: a model for irritable bowel syndrome, Gastroenterol. 94(3) (1988) 611-621. https://doi.org/10.1016/0016-5085(88)90231-4.

[13]

Y.J. Li, C. Dai, M. Jiang, Mechanisms of probiotic VSL#3 in a rat model of visceral hypersensitivity involves the mast cell-PAR2-TRPV1 pathway, Dig. Dis. Sci. 64(5) (2018) 1182-1192. https://doi.org/10.1007/s10620-018-5416-6.

[14]

J.H. La, T.W. Kim, T.S. Sung, et al., Visceral hypersensitivity and altered colonic motility after subsidence of inflammation in a rat model of colitis, World J. Gastroenterol. 9(12) (2003) 2791-2795. https://doi.org/10.1080/00365520310005712.

[15]

H. Shimpo, T. Sakai, S. Kondo, et al., Regulation of prostaglandin E2 synthesis in cells derived from chondrocytes of patients with osteoarthritis, J. Orthop. Sci. 14(5) (2009) 611-617. https://doi.org/10.1007/s00776-009-1370-7.

[16]

S. Murthy., H.S. Cooper, H. Shim, et al., Treatment of dextran sulfate sodium-induced murine colitis by intracolonic cyclosporin, Dig. Dis. 38(9) (1993) 1722-1734. https://doi.org/10.1007/BF01303184.

[17]

S. Zhang, H. Wang, M.J. Zhu, A sensitive GC/MS detection method for analyzing microbial metabolites short chain fatty acids in fecal and serum samples, Talanta 196 (2019) 249-254. https://doi.org/10.1016/j.talanta.2018.12.049.

[18]

Q. Wang, Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy, Appl. Environ. 73 (2007) 5261-5267. https://doi.org/10.1128/AEM.00062-07.

[19]

S.F. Chen, Y.Q. Zhou, Y.R. Chen, et al., fastp: an ultra-fast all-in-one FASTQ preprocessor, Bioinformatics 34 (2018) i884-i890. https://doi.org/10.1093/bioinformatics/bty560.

[20]

X. Su, Z. Qian, J. Hu, et al., Enhanced degradation of biphenyl from PCB-contaminated sediments: the impact of extracellular organic matter from Micrococcus luteus, Appl. Microbiol. Biotechnol. 99(4) (2014). https://doi.org/10.1007/s00253-014-6108-6.

[21]

J. Ritchie, Pain from distension of the pelvic colon by inflating a balloon in the irritable colon syndrome, Gut 14(2) (1973). https://doi.org/125.10.1136/gut.14.2.125.

[22]

W. Whitehead, Tolerance for rectosigmoid distention in irritable bowel syndrome, Gastroenterol. 98 (1990). https://doi.org/10.1016/0016-5085(90)90332-U.

[23]

G. Barbara, V. Stanghellini, R.D. Giorgio, et al., Activated mast cells in proximity to colonic nerves correlate with abdominal pain in irritable bowel syndrome, Gastroenterol. 126(3) (2004) 693-702. https://doi.org/10.1053/j.gastro.2003.11.055.

[24]

G. Barbara, B.Wang, V. Stanghellini, et al., Mast cell-dependent excitation of visceral-nociceptive sensory neurons in irritable bowel syndrome, Gastroenterol. 132(1) (2007) 26-37. https://doi.org/10.1053/j.gastro.2006.11.039.

[25]

M. Guilarte, J. Santo, I. de Torres, et al., Diarrhoea-predominant IBS patients show mast cell activation and hyperplasia in the jejunum, Gut 56(2) (2007) 203-9. https://doi.org/10.1136/gut.2006.100594.

[26]

G. Barbara, B. Wang, V. Stanghellin, et al., Mast cell-dependent excitation of visceral-nociceptive sensory neurons in irritable bowel syndrome, Gastroenterol. 132(1) (2007) 26-37. https://doi.org/10.1053/j.gastro.2006.11.039.

[27]

M.M. Wouter, M. Vicari, J. Santo. The role of mast cells in functional GI disorders, Gut 65(1) (2016) 155. https://doi.org/10.1136/gutjnl-2015-309151.

[28]

H. Liu, D.V. Miller, S. Lourenssen, et al., Paterso, proteinase-activated receptor-2 activation evokes oesophageal longitudinal smooth muscle contraction via a capsaicin-sensitive and neurokinin-2 receptor-dependent pathway, Neurogastroenterol. Motil. 22(2) (2010). https://doi.org/10.1111/j.1365-2982.2009.01394.x.

[29]

R.E. Ley, P.J. Turnbaugh, S. Klein, et al., Microbial ecology: human gut microbes associated with obesity, Nature 444(7122) (2006) 1022-1023. https://doi.org/10.1038/4441022a.

[30]

E.B. Hollister, K.C. Cain, R.J. Shulman, et al., Relationships of microbiome markers with extraintestinal, psychological distress and gastrointestinal symptoms, and quality of life in women with irritable bowel syndrome, J. Clin. Gastroenterol. (2020). https://doi.org/10.1097/MCG.0000000000001107.

[31]

R. Mars, Y. Yang, T. Ward, et al., Longitudinal multi-omics reveals subset-specific mechanisms underlying irritable bowel syndrome, Cell 182 (2020) 1460-1473. https://doi.org/10.1016/j.cell.2020.08.007.

[32]

E.B. Troy, Beneficial effects of Bacteroides fragilis polysaccharides on the immune system, Front. Biosci. 15 (2010). https://doi.org/10.2741/3603.

[33]

H. Luo, Q. Zhou, Roles of tight junction protein claudins phosphorylation in gastrointestinal barrier function, Chinese J. Gastroenterol. 16(7) (2011) 438-441. https://doi.org/10.3969/j.issn.1008-7125.2011.07.013.

[34]

O.R. Colegio, C.V. Itallie, C. Rahner, et al., Claudin extracellular domains determine paracellular charge selectivity and resistance but not tight junction fibril architecture, Am. J. Physiol.-Cell Ph. 284(6) (2003) 1346-1354. https://doi.org/10.1152/ajpcell.00547.2002.

[35]

J.D. Schulzke, M. Fromm. Tight junctions: molecular structure meets function, Ann. N. Y. Acad. Sci. 1165 (2009) 1-6. https://doi.org/10.1111/j.1749-6632.2009.04925.x.

[36]

Z. Fehervari, Maintaining barrier, Nat. Immunol. 16(7) (2015) 688. https://doi.org/10.1038/ni.3217.

[37]

M.A. Azcárate-Peril, M. Sikes, J.M. Bruno-Bárcena, et al., The intestinal microbiota, gastrointestinal environment and colorectal cancer: a putative role for probiotics in prevention of colorectal cancer? Am. J. Physiol.-Gastr. L. (2011). https://doi.org/10.1152/ajpgi.00110.2011.

[38]

E.M. Quigley, O.F. Craig, Irritable bowel syndrome; update on pathophysiology and management, Turkish J. Gastroenterol. 23(4) (2012) 313-322. https://doi.org/10.4318/tjg.2012.0551.

[39]

K. Kasakura, K. Takahashi, T.A. Aizawa, A TLR2 ligand suppresses allergic inflammatory reactions by acting directly on mast cells, Int. Arch. Allergy Immunol. 50(4) (2009) 359-369. https://doi.org/10.1159/000226237.

[40]

P. Forsythe, B. Wang, I. Kham, et al., Systemic effects of ingested Lactobacillus rhamnosus: inhibition of mast cell membrane potassium (IKCa) current and degranulation, PLoS One 7 (2012). https://doi.org/10.1371/journal.pone.0041234.

[41]

A. Ait-Belgnaoui, W. Han, F. Lamine, Lactobacillus farciminis treatment suppresses stress induced visceral hypersensitivity: a possible action through interaction with epithelial cell cytoskeleton contraction, Gut 55(8) (2006) 1090. https://doi.org/10.1136/gut.2005.084194.

[42]

C. Rolland-Fourcade, A. Denadai-Souza, C. Cirillo, et al., Epithelial expression and function of trypsin-3 in irritable bowel syndrome, Gut 42(1) (2015) 71. https://doi.org/10.1136/gutjnl-2016-312094.

[43]

Y. Bhattarai, D.M. Pedrogo, P.C. Kashyap, Irritable bowel syndrome: a gut microbiota-related disorder, Am. J. Physiol. 312(1) (2016). https://doi.org/10.1152/ajpgi.00338.2016.

[44]

Y. Liu, X. Yu, L. Yu, et al., Lactobacillus plantarum CCFM8610 alleviates irritable bowel syndrome and prevents gut microbiota dysbiosis: a randomized, double-blind, placebo-controlled, Pilot Clinical Trial 7(3) (2021) 10.

[45]

F. Durchschein, W. Petritsch, H.F. Hammer, Diet therapy for inflammatory bowel diseases: the established and the new, World J. Gastroenterol. (2016). https://doi.org/10.3748/wjg.v22.i7.2179.

[46]

L.H. Augenlicht, B.G. Heerdt, Modulation of gene expression as a biomarker in colon, J. Cell. Biochem. 50 (2010). https://doi.org/10.1002/jcb.240501126.

[47]

J.M. Mariadason, D.H. Barkla, P.R. Gibson, Effect of short-chain fatty acids on paracellular permeability in Caco-2 intestinal epithelium model, Am. J. Physiol. 272 (1997) 705-712. https://doi.org/10.1046/j.1365-201X.1997.00101.x.

[48]

C.S. Reigstad, C.E. Salmonson, J.F. Rainey, et al., Gut microbes promote colonic serotonin production through an effect of short-chain fatty acids on enterochromaffin cells, FASEB J. 29(4) (2015). https://doi.org/10.1096/fj.14-259598.

[49]

Z. Xia, Y. Han, K. Wang, et al., Oral administration of propionic acid during lactation enhances the colonic barrier function, Lipids Health Dis. 16(1) (2017) 62. https://doi.org/10.1186/s12944-017-0452-3.

Publication history
Copyright
Acknowledgements
Rights and permissions

Publication history

Received: 06 March 2022
Revised: 11 July 2022
Accepted: 15 September 2022
Published: 25 September 2023
Issue date: March 2024

Copyright

© 2024 Beijing Academy of Food Sciences. Publishing services by Tsinghua University Press.

Acknowledgements

Acknowledgment

This work was supported by the shanghai agriculture applied technology development program (2019-02-08-00-07-F01152); the national science fund for distinguished young scholars (32025029); the shanghai engineering research center of food microbiology program (19DZ2281100); and the national key R&D program of china (2018YFC1604305).

Rights and permissions

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Return