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Endocrine, Metabolic & Immune Disorders - Drug Targets

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ISSN (Print): 1871-5303
ISSN (Online): 2212-3873

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Research Article

Endogenous Ethanol-producing Bacteria Interference in Pathogen-host Crosstalk

Author(s): Darab Ghadimi*, Regina Fölster-Holst, Christoph Röcken, Hans-Jürgen Kaatsch, Michael Ebsen, Regis Tournebize and Wilhelm Bockelmann

Volume 23, Issue 11, 2023

Published on: 12 June, 2023

Page: [1430 - 1441] Pages: 12

DOI: 10.2174/1871530323666230330111355

Price: $65

Abstract

Background and Aims: The host micronutrient milieu is a compilation of factors of both endogenous and exogenous origin. This milieu shapes the host's immune responses and can control the inflammatory response of the host when infected. Among vitamins, B12 plays a key role in the defense process because there is intense competition for it between pathogenic invaders and infected host cells. Alcoholic beverages and antibiotics can cause biological (in vivo) interferences that affect pathogenhost crosstalk. Ethanol is known to interfere with the absorption, distribution, and excretion of vitamin B12 in men and animals. However, the molecular mechanisms underlying this backdrop are not fully understood. Here, we explored how Gram-positive ethanol-producing and Gram-negative vitamin B12- producing microbes of the infected milieu interact to influence biomarkers of host cell defense responses in absorbing, digesting, and defensive cells.

Material and Methods: We investigated two different cell types of colon and liver origin, hepatic-like Huh7 cells and HT- 29/B6 colon cells. To assess the ability of secreted factors from bacteria to exert influence on co-cultured cell's secretion of host-defense markers in response to invading pathogens, cocultured human colonic HT-29/B6 and human hepatic Huh-7 (hereafter Huh7) cells were stimulated or not with Klebsiella pneumoniae 52145 for 24 h in the presence or absence of either Weissella confusa strain NRRL-B-14171 (as a Gram-positive producer of ethanol), Limosilactobacillus reuteri 20016 (as a Gram-positive producer of vitamin B12), or Pseudomonas nitroreducens 1650 (as a Gram-negative producer of vitamin B12). After stimulation, molecular functional biomarkers of host cell defense responses including total MMP-1, lysozyme activity, ALP, and IL-25 were measured.

Results: While simultaneously reducing IL-25 secretion, Kp52145 alone significantly elicited MMP-1, lysozyme, and ALP secretion from co-cultured cells, as compared to no treatment. When compared with Kp 52145 stimulation alone, Pn1650 significantly potentiated MMP-1 and lysozyme secretions from Kp 52145-stimulated co-cultured cells by 29.7% and 67.4%, respectively. Simultaneously, a potentiated suppression (an overall decrease of 77.3%) in IL-25 secretion occurred 24 hours after Kn52145 plus Pn1650 administration. Compared to Kp52145-stimulation alone, treatment with W. confusa NRRL-B-14171 and Kp52145-stimulated co-cultured cells was associated with significant additive induction of MMP-1 and lysozyme secretions. However, compared to Kp52145-stimulation alone, W. confusa NRRL-B-14171 treatment significantly potentiated Kp52145-induced suppression of IL-25. Using the same condition as mentioned above and compared to Kp52145-stimulation alone, L. reuteri 20016 treatment altered the secretion pattern in response to Kp52145: L. reuteri 20016-treated cells displayed less aversive responses towards Kp52145, suggesting that L. reuteri 20016 modulation may act differently on Kp52145 - induced signaling.

Conclusion: Gram-negative and Gram-positive vitamin B12- producing bacteria differently affect the secretion of key immune biomarkers in co-cultured HT-29/B6 and Huh7 cells following exposure to Kp52145. Ethanol-producing bacteria additively potentiate pathogenicity and inflammatory responses upon infection. To confirm the biological consequences of these effects on human gut microbiota and health, further studies are warranted, incorporating ex vivo studies of human colon samples and host biomarkers such as cytohistological, molecular, or biochemical measurements.

Keywords: Ethanol, micronutrients, pathogens, gut dysbiosis, inflammation, cytokine.

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[1]
Salaspuro, M. Microbial metabolism of ethanol and acetaldehyde and clinical consequences. Addict. Biol., 1997, 2(1), 35-46.
[http://dx.doi.org/10.1080/13556219772840] [PMID: 26735439]
[2]
Gombart, A.F.; Pierre, A.; Maggini, S. A review of micronutrients and the immune system–working in harmony to reduce the risk of infection. Nutrients, 2020, 12(1), 236.
[http://dx.doi.org/10.3390/nu12010236] [PMID: 31963293]
[3]
Lindenbaum, J.; Lieber, C.S. Alcohol-induced malabsorption of vitamin B12 in man. Nature, 1969, 224(5221), 806.
[http://dx.doi.org/10.1038/224806a0] [PMID: 5361658]
[4]
Miyazaki, A.; Sano, M.; Fukuwatari, T.; Shibata, K. Effects of ethanol consumption on the B-group vitamin contents of liver, blood and urine in rats. Br. J. Nutr., 2012, 108(6), 1034-1041.
[http://dx.doi.org/10.1017/S0007114511006192] [PMID: 22172166]
[5]
Mergenhagen, K.A.; Wattengel, B.A.; Skelly, M.K.; Clark, C.M.; Russo, T.A. Fact versus fiction: A review of the evidence behind alcohol and antibiotic interactions. Antimicrob. Agents Chemother., 2020, 64(3), e02167-19.
[http://dx.doi.org/10.1128/AAC.02167-19] [PMID: 31871085]
[6]
Paddock, Z.D.; Renter, D.G.; Shi, X.; Krehbiel, C.R.; DeBey, B.; Nagaraja, T.G. Effects of feeding dried distillers grains with supplemental starch on fecal shedding of Escherichia coli O157:H7 in experimentally inoculated steers1. J. Anim. Sci., 2013, 91(3), 1362-1370.
[http://dx.doi.org/10.2527/jas.2012-5618] [PMID: 23348685]
[7]
Walter, A.L.; Yang, D.; Zeng, Z.; Bayrock, D.; Urriola, P.E.; Shurson, G.C. Assessment of antibiotic resistance from long-term bacterial exposure to antibiotics commonly used in fuel ethanol production. World J. Microbiol. Biotechnol., 2019, 35(4), 66.
[http://dx.doi.org/10.1007/s11274-019-2641-x] [PMID: 30941513]
[8]
Vermassen, A.; Leroy, S.; Talon, R.; Provot, C.; Popowska, M.; Desvaux, M. Cell wall hydrolases in bacteria: Insight on the diversity of cell wall amidases, glycosidases and peptidases toward peptidoglycan. Front. Microbiol., 2019, 10, 331.
[http://dx.doi.org/10.3389/fmicb.2019.00331] [PMID: 30873139]
[9]
Buonomo, E.L.; Cowardin, C.A.; Wilson, M.G.; Saleh, M.M.; Pramoonjago, P.; Petri, W.A., Jr. Microbiota-regulated IL-25 increases eosinophil number to provide protection during clostridium difficile infection. Cell Rep., 2016, 16(2), 432-443.
[http://dx.doi.org/10.1016/j.celrep.2016.06.007] [PMID: 27346351]
[10]
Heneghan, A.F.; Pierre, J.F.; Gosain, A.; Kudsk, K.A. IL-25 improves luminal innate immunity and barrier function during parenteral nutrition. Ann. Surg., 2014, 259(2), 394-400.
[http://dx.doi.org/10.1097/SLA.0b013e318284f510] [PMID: 23426341]
[11]
Gutierrez, B.; Gallardo, I.; Ruiz, L.; Alvarez, Y.; Cachofeiro, V.; Margolles, A.; Hernandez, M.; Nieto, M.L. Oleanolic acid ameliorates intestinal alterations associated with EAE. J. Neuroinflammation, 2020, 17(1), 363.
[http://dx.doi.org/10.1186/s12974-020-02042-6] [PMID: 33246492]
[12]
Arasu, M.V.; Sarkar, R.; Sekar, B.S.; Kumar, V.; Rathnasingh, C.; Choi, J.; Song, H.; Seung, D.; Park, S. Isolation of a novel Pseudomonas species SP2 producing vitamin B12 under aerobic condition. Biotechnol. Bioprocess Eng.; BBE, 2013, 18(1), 43-51.
[http://dx.doi.org/10.1007/s12257-012-0518-z]
[13]
Li, S.; Braun, J.C.; Buchner, D.; Haderlein, S.B. Denitrifier method for nitrite removal in electrochemical analysis of the electron accepting capacity of humic substances. Anal. Chem., 2020, 92(1), 616-621.
[http://dx.doi.org/10.1021/acs.analchem.9b03683] [PMID: 31751112]
[14]
Cauwels, A.; Buys, E.S.; Thoonen, R.; Geary, L.; Delanghe, J.; Shiva, S.; Brouckaert, P. Nitrite protects against morbidity and mortality associated with TNF- or LPS-induced shock in a soluble guanylate cyclase–dependent manner. J. Exp. Med., 2009, 206(13), 2915-2924.
[http://dx.doi.org/10.1084/jem.20091236] [PMID: 19934018]
[15]
Waltz, P.; Escobar, D.; Botero, A.M.; Zuckerbraun, B.S. Nitrate/nitrite as critical mediators to limit oxidative injury and inflammation. Antioxid. Redox Signal., 2015, 23(4), 328-339.
[http://dx.doi.org/10.1089/ars.2015.6256] [PMID: 26140517]
[16]
Li, P.; Gu, Q.; Yang, L.; Yu, Y.; Wang, Y. Characterization of extracellular vitamin B12 producing Lactobacillus plantarum strains and assessment of the probiotic potentials. Food Chem., 2017, 234, 494-501.
[http://dx.doi.org/10.1016/j.foodchem.2017.05.037] [PMID: 28551266]
[17]
Ayeni, F.A.; Sánchez, B.; Adeniyi, B.A.; de los Reyes-Gavilán, C.G.; Margolles, A.; Ruas-Madiedo, P. Evaluation of the functional potential of Weissella and Lactobacillus isolates obtained from Nigerian traditional fermented foods and cow’s intestine. Int. J. Food Microbiol., 2011, 147(2), 97-104.
[http://dx.doi.org/10.1016/j.ijfoodmicro.2011.03.014] [PMID: 21482440]
[18]
Tournebize, R.; Doan, B.T.; Dillies, M.A.; Maurin, S.; Beloeil, J.C.; Sansonetti, P.J. Magnetic resonance imaging of Klebsiella pneumoniae-induced pneumonia in mice. Cell. Microbiol., 2006, 8(1), 33-43.
[http://dx.doi.org/10.1111/j.1462-5822.2005.00597.x] [PMID: 16367864]
[19]
Li, N.N.; Li, W.; Feng, J.X.; Du, B.; Zhang, R.; Du, S.H.; Liu, S.Y.; Xue, G.H.; Yan, C.; Cui, J.H.; Zhao, H.Q.; Feng, Y.L.; Gan, L.; Zhang, Q.; Zhang, W.W.; Liu, D.; Chen, C.; Yuan, J. High alcohol-producing Klebsiella pneumoniae causes fatty liver disease through 2,3-butanediol fermentation pathway in vivo. Gut Microbes, 2021, 13(1), 1979883.
[http://dx.doi.org/10.1080/19490976.2021.1979883] [PMID: 34632939]
[20]
Ghadimi, D.; Nielsen, A.; Yoness, H., M.F.; Fölster-Holst, R.; de Vrese, M.; Heller, K.J. Modulation of GSK - 3β/β - catenin cascade by commensal bifidobateria plays an important role for the inhibition of metaflammation-related biomarkers in response to LPS or non-physiological concentrations of fructose: An in vitro study. PharmaNutrition, 2019, 8, 100145.
[http://dx.doi.org/10.1016/j.phanu.2019.100145]
[21]
Kreusel, K.M.; Fromm, M.; Schulzke, J.D.; Hegel, U. Cl- secretion in epithelial monolayers of mucus-forming human colon cells (HT-29/B6). Am. J. Physiol. Cell Physiol., 1991, 261(4), C574-C582.
[http://dx.doi.org/10.1152/ajpcell.1991.261.4.C574] [PMID: 1656765]
[22]
Nakabayashi, H.; Taketa, K.; Miyano, K.; Yamane, T.; Sato, J. Growth of human hepatoma cells lines with differentiated functions in chemically defined medium. Cancer Res., 1982, 42(9), 3858-3863.
[PMID: 6286115]
[23]
Ghadimi, D.; Ebsen, M.; Röcken, C.; Fölster-Holst, R.; Groessner-Schreiber, B.; Dörfer, C.; Bockelmann, W. Oral mucosal in vitro cell culture model to study the effect of Fructilacto bacillus phage on the interplay between food components and oral microbiota. Endocr. Metab. Immune. Disord Drug Targets, 2023, 23(3), 356-374.
[http://dx.doi.org/10.2174/1871530322666220408215101]
[24]
Barret, AJ; Heath, MF. Lysozyme enzymes in liposomes a laboratory hand book. In: Dingle J (ed) North Holland Publishing Co.: New York, (1977); p. 19.
[25]
Ikeda, U.; Shimpo, M.; Ohki, R.; Inaba, H.; Takahashi, M.; Yamamoto, K.; Shimada, K. Fluvastatin inhibits matrix metalloproteinase-1 expression in human vascular endothelial cells. Hypertension, 2000, 36(3), 325-329.
[http://dx.doi.org/10.1161/01.HYP.36.3.325] [PMID: 10988259]
[26]
Kumar, P.; Kumar, R.; Pandey, H.; Sundar, S.; Pai, K. Studies on the arginase, 5′-nucleotidase and lysozyme activity by monocytes from visceral leishmaniasis patients. J. Parasit. Dis., 2012, 36(1), 19-25.
[http://dx.doi.org/10.1007/s12639-011-0066-z] [PMID: 23542635]
[27]
Adikwu, E.; Bokolo, B. Possible hepatotoxic consequence of nevirapine use in juvenile albino rats. J. Pharm. Pharmacogn. Res., 2007, 5(4), 217-226.
[28]
Cano, V.; Moranta, D.; Llobet-Brossa, E.; Bengoechea, J.A.; Garmendia, J. Klebsiella pneumoniae triggers a cytotoxic effect on airway epithelial cells. BMC Microbiol., 2009, 9(1), 156.
[http://dx.doi.org/10.1186/1471-2180-9-156] [PMID: 19650888]
[29]
Hamarneh, S.R.; Kim, B.M.; Kaliannan, K.; Morrison, S.A.; Tantillo, T.J.; Tao, Q.; Mohamed, M.M.R.; Ramirez, J.M.; Karas, A.; Liu, W.; Hu, D.; Teshager, A.; Gul, S.S.; Economopoulos, K.P.; Bhan, A.K.; Malo, M.S.; Choi, M.Y.; Hodin, R.A. Intestinal alkaline phosphatase attenuates alcohol-induced hepatosteatosis in mice. Dig. Dis. Sci., 2017, 62(8), 2021-2034.
[http://dx.doi.org/10.1007/s10620-017-4576-0] [PMID: 28424943]
[30]
Schippers, M.; Post, E.; Eichhorn, I.; Langeland, J.; Beljaars, L.; Malo, M.S.; Hodin, R.A.; Millán, J.L.; Popov, Y.; Schuppan, D.; Poelstra, K. Phosphate groups in the lipid a moiety determine the effects of LPS on hepatic stellate cells: A role for LPS-dephosphorylating activity in liver fibrosis. Cells, 2020, 9(12), 2708.
[http://dx.doi.org/10.3390/cells9122708] [PMID: 33348845]
[31]
Fessard, A.; Remize, F. Why are Weissella spp. not used as commercial starter cultures for food fermentation? Fermentation, 2017, 3(3), 38.
[http://dx.doi.org/10.3390/fermentation3030038]
[32]
Hsiang, C.Y.; Wu, S.L.; Cheng, S.E.; Ho, T.Y. Acetaldehyde-induced interleukin-1β and tumor necrosis factor-α production is inhibited by berberine through nuclear factor-κB signaling pathway in HepG2 cells. J. Biomed. Sci., 2005, 12(5), 791-801.
[http://dx.doi.org/10.1007/s11373-005-9003-4] [PMID: 16132116]
[33]
Purohit, V.; Bode, J.C.; Bode, C.; Brenner, D.A.; Choudhry, M.A.; Hamilton, F.; Kang, Y.J.; Keshavarzian, A.; Rao, R.; Sartor, R.B.; Swanson, C.; Turner, J.R. Alcohol, intestinal bacterial growth, intestinal permeability to endotoxin, and medical consequences: Summary of a symposium. Alcohol, 2008, 42(5), 349-361.
[http://dx.doi.org/10.1016/j.alcohol.2008.03.131] [PMID: 18504085]
[34]
Elías-Arnanz, M. Anaerobic bacteria need their vitamin B 12 to digest estrogen. Proc. Natl. Acad. Sci., 2020, 117(4), 1833-1835.
[http://dx.doi.org/10.1073/pnas.1921340117] [PMID: 31919281]
[35]
Bouguen, G.; Dubuquoy, L.; Desreumaux, P.; Brunner, T.; Bertin, B. Intestinal steroidogenesis. Steroids, 2015, 103, 64-71.
[http://dx.doi.org/10.1016/j.steroids.2014.12.022] [PMID: 25560486]
[36]
Illera, J.C.; Caceres, S.; Peña, L.; de Andres, P.J.; Monsalve, B.; Illera, M.J.; Woodward, W.A.; Reuben, J.M.; Silvan, G. Steroid hormone secretion in inflammatory breast cancer cell lines. Horm. Mol. Biol. Clin. Investig., 2015, 24(3), 137-145.
[http://dx.doi.org/10.1515/hmbci-2015-0024] [PMID: 26495931]
[37]
Sato, R.; Suzuki, T.; Katayose, Y.; Miura, K.; Shiiba, K.; Tateno, H.; Miki, Y.; Akahira, J.; Kamogawa, Y.; Nagasaki, S.; Yamamoto, K.; Ii, T.; Egawa, S.; Evans, D.B.; Unno, M.; Sasano, H. Steroid sulfatase and estrogen sulfotransferase in colon carcinoma: regulators of intratumoral estrogen concentrations and potent prognostic factors. Cancer Res., 2009, 69(3), 914-922.
[http://dx.doi.org/10.1158/0008-5472.CAN-08-0906] [PMID: 19141651]
[38]
Fayol-Messaoudi, D.; Berger, C.N.; Coconnier-Polter, M.H.; Liévin-Le Moal, V.; Servin, A.L. pH-, Lactic acid-, and non-lactic acid-dependent activities of probiotic Lactobacilli against Salmonella enterica Serovar Typhimurium. Appl. Environ. Microbiol., 2005, 71(10), 6008-6013.
[http://dx.doi.org/10.1128/AEM.71.10.6008-6013.2005] [PMID: 16204515]
[39]
Jeffrey, M.P.; Strap, J.L.; Jones Taggart, H.; Green-Johnson, J.M. Suppression of intestinal epithelial cell chemokine production by Lactobacillus rhamnosus R0011 and Lactobacillus helveticus R0389 is mediated by secreted bioactive molecules. Front. Immunol., 2018, 9, 2639.
[http://dx.doi.org/10.3389/fimmu.2018.02639] [PMID: 30524427]
[40]
Sato, K.; Goto, S.; Yonemura, S.; Sekine, K.; Okuma, E.; Takagi, Y.; Hon-Nami, K.; Saiki, T. Effect of yeast extract and vitamin B 12 on ethanol production from cellulose by clostridium thermocellum I-1-B. Appl. Environ. Microbiol., 1992, 58(2), 734-736.
[http://dx.doi.org/10.1128/aem.58.2.734-736.1992] [PMID: 16348657]
[41]
Forgie, A.J.; Fouhse, J.M.; Willing, B.P. Diet-microbe-host interactions that affect gut mucosal integrity and infection resistance. Front. Immunol., 2019, 10, 1802.
[http://dx.doi.org/10.3389/fimmu.2019.01802] [PMID: 31447837]
[42]
Fernandez-Lizarbe, S.; Pascual, M.; Gascon, M.S.; Blanco, A.; Guerri, C. Lipid rafts regulate ethanol-induced activation of TLR4 signaling in murine macrophages. Mol. Immunol., 2008, 45(7), 2007-2016.
[http://dx.doi.org/10.1016/j.molimm.2007.10.025] [PMID: 18061674]
[43]
Lurz, E.; Horne, R.G.; Määttänen, P.; Wu, R.Y.; Botts, S.R.; Li, B.; Rossi, L.; Johnson-Henry, K.C.; Pierro, A.; Surette, M.G.; Sherman, P.M. Vitamin B12 deficiency alters the gut microbiota in a murine model of colitis. Front. Nutr., 2020, 7, 83.
[http://dx.doi.org/10.3389/fnut.2020.00083] [PMID: 32582756]
[44]
Rowley, C.A.; Kendall, M.M. To B12 or not to B12: Five questions on the role of cobalamin in host-microbial interactions. PLoS Pathog., 2019, 15(1), e1007479.
[http://dx.doi.org/10.1371/journal.ppat.1007479] [PMID: 30605490]
[45]
Samuelson, D.R.; Gu, M.; Shellito, J.E.; Molina, P.E.; Taylor, C.M.; Luo, M.; Welsh, D.A. Pulmonary immune cell trafficking promotes host defense against alcohol-associated Klebsiella pneumonia. Commun. Biol., 2021, 4(1), 997.
[http://dx.doi.org/10.1038/s42003-021-02524-0] [PMID: 34426641]
[46]
Romain, M.; Sviri, S.; Linton, D.M.; Stav, I.; van Heerden, P.V. The role of Vitamin B12 in the critically ill-a review. Anaesth. Intensive Care, 2016, 44(4), 447-452.
[http://dx.doi.org/10.1177/0310057X1604400410] [PMID: 27456173]
[47]
Forgie, A.J.; Pepin, D.M.; Ju, T.; Tollenaar, S.; Sergi, C.M.; Gruenheid, S.; Willing, B. Excessive oral intake of vitamin b12 alters microbe-host interactions that stimulate citrobacter rodentium growth and virulence in Mice. Res. Sq 2022 February 8;, rs.3.rs-1236545. doi:10.21203/rs.3.rs-1236545/v1. Preprint.
[http://dx.doi.org/10.21203/rs.3.rs-1236545/v1]
[48]
Pedersen, G. Development, validation and implementation of an in vitro model for the study of metabolic and immune function in normal and inflamed human colonic epithelium. Dan. Med. J., 2015, 62(1), B4973.
[PMID: 25557335]
[49]
Strain, R.; Stanton, C.; Ross, R.P. Effect of diet on pathogen performance in the microbiome. Microbiome Res. Reports, 2022, 1, 13.
[http://dx.doi.org/10.20517/mrr.2021.10]

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