Abstract
Probiotics are special bacterial strains with strain specific impacts. They can affect health condition in intestine by producing organic acid, competing with pathogens and maintaining cells homeostasis. Regarding to importance of cell junctions in cells transportation and the influence of pathogens in their functions which lead to inflammation, the impact of probiotic strains comprised of Lactobacillus and Bifidobacterium strains on two important members of gap junctions (Cx26 and Cx43) were assayed. The expressions of cell junction genes in contact with probiotic cocktail along with pathogenic components of enterotoxigenic Escherichia coli and Salmonella typhimurium on HT-29 cell line in different treatment orders were evaluated. Results analysis demonstrated downregulation of cx26 and cx43 along with pathogenic components while, probiotic cocktail could modulate their expression by upregulation. We concluded that Lactobacillus and Bifidobacterium strains were efficient probiotics, when they were used as one cocktail, impacted grater amount on the expression of cell junctions and this might lead to modulate homeostasis and reveal inflammation symptoms in intestine.
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References
Aasen T, Johnstone S, Vidal-Brime L, Lynn KS, Koval M (2018) Connexins: synthesis, post-translational modifications, and trafficking in health and disease. Int J Mol Sci 19(5):1296. https://doi.org/10.3390/ijms19051296
Al-Ghadban S, Kaissi S, Homaidan FR, Naim HY, El-Sabban ME (2016) Cross-talk between intestinal epithelial cells and immune cells in inflammatory bowel disease. Sci Rep 6(1):1–13. https://doi.org/10.1038/srep29783
Bhat AA, Uppada S, Achkar IW, Hashem S, Yadav SK, Shanmugakonar M et al (2019) Tight junction proteins and signaling pathways in cancer and inflammation: a functional crosstalk. Front Physiol 9:1942. https://doi.org/10.3389/fphys.2018.01942
Blackwood BP, Yuan CY, Wood DR, Nicolas JD, Grothaus JS, Hunter CJ (2017) Probiotic Lactobacillus species strengthen intestinal barrier function and tight junction integrity in experimental necrotizing enterocolitis. J Probiotics Health 5:1. https://doi.org/10.4172/2329-8901.1000159
Derangeon M, Bourmeyster N, Plaisance I, Pinet-Charvet C, Chen Q, Duthe F et al (2008) RhoA GTPase and F-actin dynamically regulate the permeability of Cx43-made channels in rat cardiac myocytes. J Biol Chem 283(45):30754–30765. https://doi.org/10.1074/jbc.M801556200
Diezmos EF, Bertrand PP, Liu L (2016) Purinergic signaling in gut inflammation: the role of connexins and pannexins. Front Neurosci 10:311. https://doi.org/10.3389/fnins.2016.00311
Eshaghi M, Bibalan MH, Rohani M, Esghaei M, Douraghi M, Talebi M et al (2017) Bifidobacterium obtained from mother’s milk and their infant stool; A comparative genotyping and antibacterial analysis. Microb Pathog 111:94–98. https://doi.org/10.1016/j.micpath.2017.08.014
Ey B, Eyking A, Gerken G, Podolsky DK, Cario E (2009) TLR2 mediates gap junctional intercellular communication through connexin-43 in intestinal epithelial barrier injury. J Biol Chem 284(33):22332–22343. https://doi.org/10.1074/jbc.M901619200
Ghosh S, Whitley CS, Haribabu B, Jala VR (2021) Regulation of intestinal barrier function by microbial metabolites. CMGH Cell Mol Gastroenterol Hepatol 11(5):1463–1482. https://doi.org/10.1016/j.jcmgh.2021.02.007
Giepmans BN (2004) Gap junctions and connexin-interacting proteins. Cardiovasc Res 62(2):233–245. https://doi.org/10.1016/j.cardiores.2003.12.009
Guttman JA, Lin AE-J, Li Y, Bechberger J, Naus CC, Vogl AW et al (2010) Gap junction hemichannels contribute to the generation of diarrhoea during infectious enteric disease. Gut 59(2):218–226. https://doi.org/10.1136/gut.2008.170464
Hansson E, Skiöldebrand E (2019) Low-grade inflammation causes gap junction-coupled cell dysfunction throughout the body, which can lead to the spread of systemic inflammation. Scand J Pain 19(4):639–649. https://doi.org/10.1515/sjpain-2019-0061
Hsieh CY, Osaka T, Moriyama E, Date Y, Kikuchi J, Tsuneda S (2015) Strengthening of the intestinal epithelial tight junction by Bifidobacterium bifidum. Physiol Rep 3:3. https://doi.org/10.14814/phy2.12327
Jia Y, Xu C, Yang W (2008) Expressions of connexin 32 and connexin 43 in patients with gastric precancerous lesion after eradication of Helicobacter pylori. J Cent South Univ 33(7):628–633
Le B, Yang SH (2018) Efficacy of Lactobacillus plantarum in prevention of inflammatory bowel disease. Toxicol Rep 5:314–317. https://doi.org/10.1016/j.toxrep.2018.02.007
Liu Q, Yu Z, Tian F, Zhao J, Zhang H, Zhai Q et al (2020) Surface components and metabolites of probiotics for regulation of intestinal epithelial barrier. Microb Cell Fact 19(1):23. https://doi.org/10.1186/s12934-020-1289-4
Luissint A-C, Parkos CA, Nusrat A (2016) Inflammation and the intestinal barrier: leukocyte–epithelial cell interactions, cell junction remodeling, and mucosal repair. Gastroenterology 151(4):616–632. https://doi.org/10.1053/j.gastro.2016.07.008
Madsen K, Cornish A, Soper P, McKaigney C, Jijon H, Yachimec C et al (2001) Probiotic bacteria enhance murine and human intestinal epithelial barrier function. Gastroenterology 121(3):580–591. https://doi.org/10.1053/gast.2001.27224
Nielsen MS, Axelsen LN, Sorgen PL, Verma V, Delmar M, Holstein-Rathlou N-H (2012) Gap junctions. Compr Physiol 2:3. https://doi.org/10.1002/cphy.c110051
Rashid SK, Khodja NI, Auger C, Alhosin M, Boehm N, Oswald-Mammosser M et al (2014) Probiotics (VSL# 3) prevent endothelial dysfunction in rats with portal hypertension: role of the angiotensin system. PLoS ONE 9(5):e97458. https://doi.org/10.1371/journal.pone.0097458
Rohani M, Noohi N, Talebi M, Katouli M, Pourshafie MR (2015) Highly heterogeneous probiotic Lactobacillus species in healthy Iranians with low functional activities. PLoS ONE 10(12):e0144467. https://doi.org/10.1371/journal.pone.0144467
Saab JB, Losa D, Chanson M, Ruez R (2014) Connexins in respiratory and gastrointestinal mucosal immunity. FEBS Lett 588(8):1288–1296. https://doi.org/10.1016/j.febslet.2014.02.059
Segretain D, Falk MM (2004) Regulation of connexin biosynthesis, assembly, gap junction formation, and removal. Biochim Biophys Acta Biomembr 1662(1–2):3–21. https://doi.org/10.1016/j.bbamem.2004.01.007
Su V, Lau AF (2014) Connexins: mechanisms regulating protein levels and intercellular communication. FEBS Lett 588(8):1212–1220. https://doi.org/10.1016/j.febslet.2014.01.013
Turroni F, Ventura M, Buttó LF, Duranti S, O’Toole PW, Motherway MOC et al (2014) Molecular dialogue between the human gut microbiota and the host: a Lactobacillus and Bifidobacterium perspective. Cell Mol Life Sci 71(2):183–203. https://doi.org/10.1007/s00018-013-1318-0
Willebrords J, Crespo Yanguas S, Maes M, Decrock E, Wang N, Leybaert L et al (2016) Connexins and their channels in inflammation. Crit Rev Biochem Mol Biol 51(6):413–439. https://doi.org/10.1080/10409238.2016.1204980
Wong J, Chopra J, Chiang LLW, Liu T, Ho J, Wu WK et al (2019) The role of connexins in gastrointestinal diseases. J Mol Biol 431(4):643–652. https://doi.org/10.1016/j.jmb.2019.01.007
Xu C-Y, Zhang W-S, Zhang H, Cao Y, Zhou H-Y (2019) The role of connexin-43 in the inflammatory process: a new potential therapy to influence keratitis. J Ophthalmol. https://doi.org/10.1155/2019/9312827
Yao S, Zhao Z, Wang W, Liu X (2021) Bifidobacterium Longum: protection against inflammatory bowel disease. J Immunol Res. https://doi.org/10.1155/2021/8030297
Yeh T-H, Hsu W-C, Chen Y-S, Hsu C-J, Lee S-Y (2005) Lipopolysaccharide decreases connexin 43 expression on nasal epithelial cells in vitro. Acta Otolaryngol 125(10):1091–1096. https://doi.org/10.1080/00016480510037906
Yu Q, Yuan L, Deng J, Yang Q (2015) Lactobacillus protects the integrity of intestinal epithelial barrier damaged by pathogenic bacteria. Front Cell Infect Microbiol 5:26. https://doi.org/10.3389/fcimb.2015.00026
Zhang J, Yang G-m, Zhu Y, Peng X-y, Li T, Liu L-m (2015) Role of connexin 43 in vascular hyperpermeability and relationship to Rock1-MLC20 pathway in septic rats. Am J Physiol Lung Cell Mol Physiol 309(11):L1323–L1332. https://doi.org/10.1152/ajplung.00016.2015
Acknowledgements
We are sincerely thankful to Dr. Saeideh Najafi, Dr. Amin Sepehr and Dr. Shadi Aghamohammd at Bacteriology Department of Pasteur Institute of Iran for their technical assistance also, Science and Research Branch of Islamic Azad University for their support. This work was supported by Bacteriology Department of Pasteur Institute of Iran [grant number 1694].
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Miri, S.T., Sotoodehnejadnematalahi, F., Amiri, M.M. et al. The impact of Lactobacillus and Bifidobacterium probiotic cocktail on modulation of gene expression of gap junctions dysregulated by intestinal pathogens. Arch Microbiol 204, 417 (2022). https://doi.org/10.1007/s00203-022-03026-1
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DOI: https://doi.org/10.1007/s00203-022-03026-1