Immunomodulatory Properties of Probiotics and Their Derived Bioactive Compounds
Abstract
:1. Introduction
2. Hallmarks of Innate and Adaptive Immunity
3. Gut Microbiota and Immunity Crosstalk in Health and Disease
4. Immunomodulatory Properties of Probiotics
5. Probiotic Derived Bioactive Compounds and Immunity
5.1. Bacteriocins
5.1.1. General Features of Bacteriocins
5.1.2. Classification of LAB Bacteriocins
5.1.3. Bacteriocins as Immunomodulatory Molecules
Cell Type | Compound | Immunomodulatory Effect | References |
---|---|---|---|
IECs | Sublancin | Inhibition of NF-κB activation | [90] |
Bacteriocins | Stimulation of host immunity as signaling peptides | [13,99] | |
Neutrophils | Nisin | NETs formation, IL-8 production | [106,107] |
Macrophages | Nisin | IL-12 increase | [108] |
Sublancin | IL-1β, IL-6, TNF-α, and NO production, TLR, NF-κB, and MAPK signaling pathways modulation | [110] | |
DCs | L. plantarum bacteriocin-like peptide | Genes encoding bacteriocin secretion enhance IL-10 over IL-12 | [114] |
PBMCs | Nisin | CD4+ and CD8+ T cell proliferation, macrophages/monocytes increase | [103,104] |
Nisin Z | IL-1β, IL-6, IL-8, MCP-1, Gro-α secretion, TNF-α suppression | [105] | |
Acidocin A | Cytokines- chemokines production | [112] | |
L. plantarum bacteriocin-like peptide | Genes encoding bacteriocin secretion enhance IL-10 over IL-12 | [115] |
5.2. SCFAs
5.2.1. Overview of SCFAs
5.2.2. SCFAs as Immunomodulatory Molecules
Cell Type | Compound | Immunomodulatory Effect | References |
---|---|---|---|
IECs | Acetate | GPR43 and NLRP3 activation, IL-18 production, maintenance of epithelial barrier | [142] |
Butyrate | PPAR-γ activation, β-oxidation and OXPHOS induction, conditions favoring SCFA-producing bacteria | [1,16,17] | |
NF-κB pathway suppression, anti-inflammatory cytokines increase | [127,144] | ||
Acetate, propionate, butyrate | Restoration of mucosal barrier integrity (5-FU treated Caco-2 and IECs) | [131] | |
Neutrophils | Acetate, butyrate | GPR43 activation, chemotaxis induction, p38 MAPK activation | [3,146] |
Acetate, propionate, butyrate | Inhibition of ROS and NO production, NF-κB pathway suppression, HDAC inhibition | [3,148] | |
Macrophages | Acetate, butyrate | Pro-inflammatory cytokines reduction, anti-inflammatory cytokine IL-10 increase | [149] |
Butyrate | Epigenetic modulations, M2 macrophage polarization, immune tolerance enhancement | [150] | |
DCs | Butyrate | GPR109A activation, Tregs differentiation, IL-18 secretion, protection against inflammation–tumorigenesis | [151] |
Balance in Tregs and Th1-Th17 cells population, modulation of gene expression | [152] | ||
Acetate, butyrate | Activation of GPRs, ALDH1a production, increased secretion of IgA by plasma cells | [1,3] | |
NK cells | Butyrate, acetate | NK recruitment, increased IFN-γ production | [140,155] |
CD4+ T cells | Butyrate | GPR43/GPR41 activation, differentiation to Tregs expressing Foxp3 | [130] |
Butyrate, acetate | Th1 activation, mTOR, STAT3 pathways induction, Blimp-1 and IL-10 production | [1] | |
CD8+ T cells | Butyrate | Enhancement of memory CD8+ responses | [158] |
Enhancement of the efficacy of oxaliplatin, amplification of CD8+ T cell responses | [159] | ||
B cells | Acetate, propionate, butyrate | OXPHOS- fatty acid synthesis enhancement, differentiation into plasma cells, epigenetic regulation, IL-6 production, activation of Tfh | [160,161] |
6. Challenges and Future Perspectives
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Zhang, Z.; Tang, H.; Chen, P.; Xie, H.; Tao, Y. Demystifying the manipulation of host immunity, metabolism, and extraintestinal tumors by the gut microbiome. Signal Transduct. Target. Ther. 2019, 4, 41. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mazziotta, C.; Tognon, M.; Martini, F.; Torreggiani, E.; Rotondo, J.C. Probiotics Mechanism of Action on Immune Cells and Beneficial Effects on Human Health. Cells 2023, 12, 184. [Google Scholar] [CrossRef] [PubMed]
- Wang, G.; Huang, S.; Wang, Y.; Cai, S.; Yu, H.; Liu, H.; Zeng, X.; Zhang, G.; Qiao, S. Bridging intestinal immunity and gut microbiota by metabolites. Cell Mol. Life Sci. 2019, 76, 3917–3937. [Google Scholar] [CrossRef] [Green Version]
- Martinez, K.B.; Leone, V.; Chang, E.B. Western diets, gut dysbiosis, and metabolic diseases: Are they linked? Gut Microbes 2017, 8, 130–142. [Google Scholar] [CrossRef] [Green Version]
- Wang, J.; Chen, W.D.; Wang, Y.D. The Relationship Between Gut Microbiota and Inflammatory Diseases: The Role of Macrophages. Front. Microbiol. 2020, 11, 1065. [Google Scholar] [CrossRef] [PubMed]
- Sharma, V.R.; Singh, M.; Kumar, V.; Yadav, M.; Sehrawat, N.; Sharma, D.K.; Sharma, A.K. Microbiome dysbiosis in cancer: Exploring therapeutic strategies to counter the disease. Semin. Cancer Biol. 2021, 70, 61–70. [Google Scholar] [CrossRef]
- Bartolomaeus, H.; McParland, V.; Wilck, N. Darm-Herz-Achse: Wie Darmbakterien kardiovaskuläre Erkrankungen beeinflussen [Gut-heart axis: How gut bacteria influence cardiovascular diseases]. Herz 2020, 45, 134–141. [Google Scholar] [CrossRef]
- Rutsch, A.; Kantsjö, J.B.; Ronchi, F. The Gut-Brain Axis: How Microbiota and Host Inflammasome Influence Brain Physiology and Pathology. Front. Immunol. 2020, 11, 604179. [Google Scholar] [CrossRef]
- Plaza-Diaz, J.; Ruiz-Ojeda, F.J.; Gil-Campos, M.; Gil, A. Mechanisms of Action of Probiotics. Adv. Nutr. 2019, 10, S49–S66. [Google Scholar] [CrossRef] [Green Version]
- Hill, C.; Guarner, F.; Reid, G.; Gibson, G.R.; Merenstein, D.J.; Pot, B.; Morelli, L.; Canani, R.B.; Flint, H.J.; Salminen, S.; et al. Expert Consensus Document: The International Scientific Association for Probiotics and Prebiotics Consensus Statement on the Scope and Appropriate Use of the Term Probiotic. Nat. Rev. Gastroenterol. Hepatol. 2014, 11, 506–514. [Google Scholar] [CrossRef] [Green Version]
- Bao, Y.; Zhang, Y.; Zhang, Y.; Liu, Y.; Wang, S.; Dong, X.; Wang, Y.; Zhang, H. Screening of potential probiotic properties of Lactobacillus fermentum isolated from traditional dairy products. Food Control. 2010, 21, 695–701. [Google Scholar] [CrossRef]
- Nagpal, R.; Wang, S.; Ahmadi, S.; Hayes, J.; Gagliano, J.; Subashchandrabose, S.; Kitzman, D.W.; Becton, T.; Read, R.; Yadav, H. Human-origin probiotic cocktail increases short-chain fatty acid production via modulation of mice and human gut microbiome. Sci. Rep. 2018, 8, 12649. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Soltani, S.; Hammami, R.; Cotter, P.D.; Rebuffat, S.; Said, L.B.; Gaudreau, H.; Bédard, F.; Biron, E.; Drider, D.; Fliss, I. Bacteriocins as a new generation of antimicrobials: Toxicity aspects and regulations. FEMS Microbiol. Rev. 2021, 45, fuaa039. [Google Scholar] [CrossRef]
- Azad, M.A.K.; Sarker, M.; Wan, D. Immunomodulatory Effects of Probiotics on Cytokine Profiles. BioMed Res. Int. 2018, 2018, 8063647. [Google Scholar] [CrossRef] [Green Version]
- Nagpal, R.; Kumar, A.; Kumar, M.; Behare, P.V.; Jain, S.; Yadav, H. Probiotics, their health benefits and applications for developing healthier foods: A review. FEMS Microbiol. Lett. 2012, 334, 1–15. [Google Scholar] [CrossRef] [Green Version]
- Chugh, B.; Kamal-Eldin, A. Bioactive compounds produced by probiotics in food products. Curr. Opin. Food Sci. 2020, 32, 76–82. [Google Scholar] [CrossRef]
- Indira, M.; Venkateswarulu, T.C.; Abraham Peele, K.; Nazneen Bobby, M.; Krupanidhi, S. Bioactive molecules of probiotic bacteria and their mechanism of action: A review. 3 Biotech 2019, 9, 306. [Google Scholar] [CrossRef]
- Blacher, E.; Levy, M.; Tatirovsky, E.; Elinav, E. Microbiome-Modulated Metabolites at the Interface of Host Immunity. J. Immunol. 2017, 198, 572–580. [Google Scholar] [CrossRef] [Green Version]
- Shin, J.M.; Gwak, J.W.; Kamarajan, P.; Fenno, J.C.; Rickard, A.H.; Kapila, Y.L. Biomedical applications of nisin. J. Appl. Microbiol. 2016, 120, 1449–1465. [Google Scholar] [CrossRef] [Green Version]
- Małaczewska, J.; Kaczorek-Łukowska, E. Nisin-A lantibiotic with immunomodulatory properties: A review. Peptides 2021, 137, 170479. [Google Scholar] [CrossRef] [PubMed]
- Hernández-González, J.C.; Martínez-Tapia, A.; Lazcano-Hernández, G.; García-Pérez, B.E.; Castrejón-Jiménez, N.S. Bacteriocins from Lactic Acid Bacteria. A Powerful Alternative as Antimicrobials, Probiotics, and Immunomodulators in Veterinary Medicine. Animals 2021, 11, 979. [Google Scholar] [CrossRef] [PubMed]
- Śliżewska, K.; Markowiak-Kopeć, P.; Śliżewska, W. The Role of Probiotics in Cancer Prevention. Cancers 2021, 13, 20. [Google Scholar] [CrossRef] [PubMed]
- Alexopoulou, L.; Kontoyiannis, D. Contribution of microbial-associated molecules in innate mucosal responses. Cell Mol. Life Sci. 2005, 62, 1349–1358. [Google Scholar] [CrossRef]
- Yeşilyurt, N.; Yılmaz, B.; Ağagündüz, D.; Capasso, R. Involvement of Probiotics and Postbiotics in the Immune System Modulation. Biologics 2021, 1, 89–110. [Google Scholar] [CrossRef]
- Amarante-Mendes, G.P.; Adjemian, S.; Branco, L.M.; Zanetti, L.C.; Weinlich, R.; Bortoluci, K.R. Pattern Recognition Receptors and the Host Cell Death Molecular Machinery. Front. Immunol. 2018, 9, 2379. [Google Scholar] [CrossRef] [Green Version]
- Li, D.; Wu, M. Pattern recognition receptors in health and diseases. Signal Transduct. Target. Ther. 2021, 6, 291. [Google Scholar] [CrossRef] [PubMed]
- Cano, R.L.E.; Lopera, H.D.E. Introduction to T and B lymphocytes. In Autoimmunity: From Bench to Bedside; Anaya, J.M., Shoenfeld, Y., Rojas-Villarraga, A., Eds.; El Rosario University Press: Bogota, Colombia, 2013. Available online: https://www.ncbi.nlm.nih.gov/books/NBK459471/ (accessed on 25 January 2023).
- Marshall, J.S.; Warrington, R.; Watson, W.; Kim, H.L. An introduction to immunology and immunopathology. Allergy Asthma Clin. Immunol. 2018, 14, 49. [Google Scholar] [CrossRef] [Green Version]
- Silva-Gomes, S.; Decout, A.; Nigou, J. Pathogen-Associated Molecular Patterns (PAMPs). In Encyclopedia of Inflammatory Diseases; Parnham, M., Ed.; Birkhäuser: Basel, Switzerland, 2014. [Google Scholar] [CrossRef]
- Netea, M.G.; Schlitzer, A.; Placek, K.; Joosten, L.A.B.; Schultze, J.L. Innate and Adaptive Immune Memory: An Evolutionary Continuum in the Host’s Response to Pathogens. Cell Host Microbe 2019, 25, 13–26. [Google Scholar] [CrossRef] [Green Version]
- Alberts, B.; Johnson, A.; Lewis, J.; Raff, M.; Roberts, K.; Walter, P. The Adaptive Immune System. In Molecular Biology of the Cell, 4th ed.; Garland Science: New York, NY, USA, 2002. Available online: https://www.ncbi.nlm.nih.gov/books/NBK21070/ (accessed on 25 January 2023).
- Chaplin, D.D. Overview of the immune response. J. Allergy Clin. Immunol. 2010, 125, S3–S23. [Google Scholar] [CrossRef]
- Bonilla, F.A.; Oettgen, H.C. Adaptive immunity. J. Allergy Clin. Immunol. 2010, 125, S33–S40. [Google Scholar] [CrossRef]
- Luckheeram, R.V.; Zhou, R.; Verma, A.D.; Xia, B. CD4+T cells: Differentiation and functions. Clin. Dev. Immunol. 2012, 2012, 925135. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hirahara, K.; Nakayama, T. CD4+ T-cell subsets in inflammatory diseases: Beyond the Th1/Th2 paradigm. Int. Immunol. 2016, 28, 163–171. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Golubovskaya, V.; Wu, L. Different Subsets of T Cells, Memory, Effector Functions, and CAR-T Immunotherapy. Cancers 2016, 8, 36. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vyas, S.P.; Goswami, R. A Decade of Th9 Cells: Role of Th9 Cells in Inflammatory Bowel Disease. Front. Immunol. 2018, 9, 1139. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Imam, T.; Park, S.; Kaplan, M.H.; Olson, M.R. Effector T Helper Cell Subsets in Inflammatory Bowel Diseases. Front. Immunol. 2018, 9, 1212. [Google Scholar] [CrossRef] [PubMed]
- Keir, M.; Yi, Y.; Lu, T.; Ghilardi, N. The role of IL-22 in intestinal health and disease. J. Exp. Med. 2020, 217, e20192195. [Google Scholar] [CrossRef]
- Cosovanu, C.; Neumann, C. The Many Functions of Foxp3+ Regulatory T Cells in the Intestine. Front. Immunol. 2020, 11, 600973. [Google Scholar] [CrossRef]
- Krishnaswamy, J.K.; Alsén, S.; Yrlid, U.; Eisenbarth, S.C.; Williams, A. Determination of T Follicular Helper Cell Fate by Dendritic Cells. Front. Immunol. 2018, 9, 2169. [Google Scholar] [CrossRef]
- Olvera-Rosales, L.B.; Cruz-Guerrero, A.E.; Ramírez-Moreno, E.; Quintero-Lira, A.; Contreras-López, E.; Jaimez-Ordaz, J.; Castañeda-Ovando, A.; Añorve-Morga, J.; Calderón-Ramos, Z.G.; Arias-Rico, J.; et al. Impact of the Gut Microbiota Balance on the Health-Disease Relationship: The Importance of Consuming Probiotics and Prebiotics. Foods 2021, 10, 1261. [Google Scholar] [CrossRef]
- Liu, Y.; Wang, J.; Wu, C. Modulation of Gut Microbiota and Immune System by Probiotics, Pre-biotics, and Post-biotics. Front. Nutr. 2022, 8, 634897. [Google Scholar] [CrossRef]
- Wu, H.J.; Wu, E. The role of gut microbiota in immune homeostasis and autoimmunity. Gut Microbes. 2012, 3, 4–14. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Peluzio, M.D.C.G.; Martinez, J.A.; Milagro, F.I. Postbiotics: Metabolites and mechanisms involved in microbiota-host interactions. Trends Food Sci. Technol. 2021, 108, 11–26. [Google Scholar] [CrossRef]
- Fan, Y.; Pedersen, O. Gut microbiota in human metabolic health and disease. Nat. Rev. Microbiol. 2021, 19, 55–71. [Google Scholar] [CrossRef]
- Chen, Y.; Zhou, J.; Wang, L. Role and Mechanism of Gut Microbiota in Human Disease. Front. Cell. Infect. Microbiol. 2021, 11, 625913. [Google Scholar] [CrossRef] [PubMed]
- Zheng, D.; Liwinski, T.; Elinav, E. Interaction between microbiota and immunity in health and disease. Cell Res. 2020, 30, 492–506. [Google Scholar] [CrossRef] [PubMed]
- McBurney, M.I.; Davis, C.; Fraser, C.M.; Schneeman, B.O.; Huttenhower, C.; Verbeke, K.; Walter, J.; Latulippe, M.E. Establishing What Constitutes a Healthy Human Gut Microbiome: State of the Science, Regulatory Considerations, and Future Directions. J. Nutr. 2019, 149, 1882–1895. [Google Scholar] [CrossRef] [Green Version]
- Dogra, S.K.; Doré, J.; Damak, S. Gut Microbiota Resilience: Definition, Link to Health and Strategies for Intervention. Front. Microbiol. 2020, 11, 572921. [Google Scholar] [CrossRef]
- Cristofori, F.; Dargenio, V.N.; Dargenio, C.; Miniello, V.L.; Barone, M.; Francavilla, R. Anti-Inflammatory and Immunomodulatory Effects of Probiotics in Gut Inflammation: A Door to the Body. Front. Immunol. 2021, 12, 578386. [Google Scholar] [CrossRef]
- Integrative HMP (iHMP) Research Network Consortium. The Integrative Human Microbiome Project. Nature 2019, 569, 641–648. [Google Scholar] [CrossRef] [Green Version]
- Mörbe, U.M.; Jørgensen, P.B.; Fenton, T.M.; von Burg, N.; Riis, L.B.; Spencer, J.; Agace, W.W. Human gut-associated lymphoid tissues (GALT); diversity, structure, and function. Mucosal Immunol. 2021, 14, 793–802. [Google Scholar] [CrossRef]
- Yadav, M.K.; Kumari, I.; Singh, B.; Sharma, K.K.; Tiwari, S.K. Probiotics, prebiotics and synbiotics: Safe options for next-generation therapeutics. Appl. Microbiol. Biotechnol. 2022, 106, 505–521. [Google Scholar] [CrossRef] [PubMed]
- Jung, C.; Hugot, J.P.; Barreau, F. Peyer’s Patches: The Immune Sensors of the Intestine. Int. J. Inflam. 2010, 2010, 823710. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Macpherson, A.J.; Harris, N.L. Interactions between commensal intestinal bacteria and the immune system. Nat. Rev. Immunol. 2004, 4, 478–485. [Google Scholar] [CrossRef]
- Round, J.L.; Mazmanian, S.K. The gut microbiota shapes intestinal immune responses during health and disease. Nat. Rev. Immunol. 2009, 9, 313–323. [Google Scholar] [CrossRef] [PubMed]
- Mazmanian, S.K.; Liu, C.H.; Tzianabos, A.O.; Kasper, D.L. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 2005, 122, 107–118. [Google Scholar] [CrossRef] [Green Version]
- Ivanov, I.I.; Atarashi, K.; Manel, N.; Brodie, E.L.; Shima, T.; Karaoz, U.; Wei, D.; Goldfarb, K.C.; Santee, C.A.; Lynch, S.V.; et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 2009, 139, 485–498. [Google Scholar] [CrossRef] [Green Version]
- Zheng, Y.; Fang, Z.; Xue, Y.; Zhang, J.; Zhu, J.; Gao, R.; Yao, S.; Ye, Y.; Wang, S.; Lin, C.; et al. Specific gut microbiome signature predicts the early-stage lung cancer. Gut Microbes 2020, 11, 1030–1042. [Google Scholar] [CrossRef]
- Youssef, M.; Ahmed, H.Y.; Zongo, A.; Korin, A.; Zhan, F.; Hady, E.; Umair, M.; Shahid Riaz Rajoka, M.; Xiong, Y.; Li, B. Probiotic Supplements: Their Strategies in the Therapeutic and Prophylactic of Human Life-Threatening Diseases. Int. J. Mol. Sci. 2021, 22, 11290. [Google Scholar] [CrossRef]
- Raheem, A.; Liang, L.; Zhang, G.; Cui, S. Modulatory Effects of Probiotics During Pathogenic Infections with Emphasis on Immune Regulation. Front. Immunol. 2021, 12, 616713. [Google Scholar] [CrossRef]
- Kaur, H.; Ali, S.A. Probiotics and gut microbiota: Mechanistic insights into gut immune homeostasis through TLR pathway regulation. Food Funct. 2022, 13, 7423–7447. [Google Scholar] [CrossRef]
- Aghamohammad, S.; Sepehr, A.; Miri, S.T.; Najafi, S.; Rohani, M.; Pourshafiea, M.R. The effects of the probiotic cocktail on modulation of the NF-kB and JAK/STAT signaling pathways involved in the inflammatory response in bowel disease model. BMC Immunol. 2022, 23, 8. [Google Scholar] [CrossRef] [PubMed]
- Bhardwaj, R.; Singh, B.P.; Sandhu, N.; Singh, N.; Kaur, R.; Rokana, N.; Singh, K.S.; Chaudhary, V.; Panwar, H. Probiotic mediated NF-κB regulation for prospective management of type 2 diabetes. Mol. Biol. Rep. 2020, 47, 2301–2313. [Google Scholar] [CrossRef]
- Dinić, M.; Jakovljević, S.; Đokić, J.; Popović, N.; Radojević, D.; Strahinić, I.; Golić, N. Probiotic-mediated p38 MAPK immune signaling prolongs the survival of Caenorhabditis elegans exposed to pathogenic bacteria. Sci. Rep. 2021, 11, 21258. [Google Scholar] [CrossRef] [PubMed]
- Liu, Q.; Yu, Z.; Tian, F.; Zhao, J.; Zhang, H.; Zhai, Q.; Chen, W. Surface components and metabolites of probiotics for regulation of intestinal epithelial barrier. Microb. Cell Fact. 2020, 19, 23. [Google Scholar] [CrossRef] [Green Version]
- Gill, H.S.; Rutherfurd, K.J.; Prasad, J.; Gopal, P.K. Enhancement of natural and acquired immunity by Lactobacillus rhamnosus (HN001), Lactobacillus acidophilus (HN017) and Bifidobacterium lactis (HN019). Br. J. Nutr. 2000, 83, 167–176. [Google Scholar] [CrossRef] [Green Version]
- Rocha-Ramírez, L.M.; Pérez-Solano, R.A.; Castañón-Alonso, S.L.; Moreno Guerrero, S.S.; Ramírez Pacheco, A.; García Garibay, M.; Eslava, C. Probiotic Lactobacillus Strains Stimulate the Inflammatory Response and Activate Human Macrophages. J. Immunol. Res. 2017, 2017, 4607491. [Google Scholar] [CrossRef] [Green Version]
- Yousefi, B.; Eslami, M.; Ghasemian, A.; Kokhaei, P.; Salek Farrokhi, A.; Darabi, N. Probiotics importance and their immunomodulatory properties. J. Cell Physiol. 2019, 234, 8008–8018. [Google Scholar] [CrossRef] [PubMed]
- Aziz, N.; Bonavida, B. Activation of Natural Killer Cells by Probiotics. Onco Ther. 2016, 7, 41–55. [Google Scholar] [CrossRef] [Green Version]
- Mao, J.; Zhang, S.Z.; Du, P.; Cheng, Z.B.; Hu, H.; Wang, S.Y. Probiotics Can Boost the Antitumor Immunity of CD8+T Cells in BALB/c Mice and Patients with Colorectal Carcinoma. J. Immunol. Res. 2020, 2020, 4092472. [Google Scholar] [CrossRef] [PubMed]
- Maldonado Galdeano, C.; Cazorla, S.I.; Lemme Dumit, J.M.; Vélez, E.; Perdigón, G. Beneficial Effects of Probiotic Consumption on the Immune System. Ann. Nutr. Metab. 2019, 74, 115–124. [Google Scholar] [CrossRef] [Green Version]
- Javanshir, N.; Hosseini, G.N.G.; Sadeghi, M.; Esmaeili, R.; Satarikia, F.; Ahmadian, G.; Allahyari, N. Evaluation of the Function of Probiotics, Emphasizing the Role of their Binding to the Intestinal Epithelium in the Stability and their Effects on the Immune System. Biol. Proced. Online 2021, 23, 23. [Google Scholar] [CrossRef] [PubMed]
- Tripathy, A.; Dash, J.; Kancharla, S.; Kolli, P.; Mahajan, D.; Senapati, S.; Jena, M.K. Probiotics: A Promising Candidate for Management of Colorectal Cancer. Cancers 2021, 13, 3178. [Google Scholar] [CrossRef] [PubMed]
- Rousseaux, A.; Brosseau, C.; Bodinier, M. Immunomodulation of B Lymphocytes by Prebiotics, Probiotics and Synbiotics: Application in Pathologies. Nutrients 2023, 15, 269. [Google Scholar] [CrossRef]
- Pietrzak, B.; Tomela, K.; Olejnik-Schmidt, A.; Mackiewicz, A.; Schmidt, M. Secretory IgA in Intestinal Mucosal Secretions as an Adaptive Barrier against Microbial Cells. Int. J. Mol. Sci. 2020, 21, 9254. [Google Scholar] [CrossRef] [PubMed]
- Sakai, F.; Hosoya, T.; Ono-Ohmachi, A.; Ukibe, K.; Ogawa, A.; Moriya, T.; Kadooka, Y.; Shiozaki, T.; Nakagawa, H.; Nakayama, Y.; et al. Lactobacillus gasseri SBT2055 induces TGF-β expression in dendritic cells and activates TLR2 signal to produce IgA in the small intestine. PLoS ONE 2014, 9, e105370. [Google Scholar] [CrossRef] [PubMed]
- Tiwari, S.K. Bacteriocin-Producing Probiotic Lactic Acid Bacteria in Controlling Dysbiosis of the Gut Microbiota. Front. Cell. Infect. Microbiol. 2022, 12, 851140. [Google Scholar] [CrossRef]
- Nataraj, B.H.; Ali, S.A.; Behare, P.V.; Yadav, H. Postbiotics-parabiotics: The new horizons in microbial biotherapy and functional foods. Microb. Cell Fact. 2020, 19, 168. [Google Scholar] [CrossRef]
- Ma, L.; Tu, H.; Chen, T. Postbiotics in Human Health: A Narrative Review. Nutrients 2023, 15, 291. [Google Scholar] [CrossRef]
- Zamora-Pineda, J.; Kalinina, O.; Osborne, B.A.; Knight, K.L. Probiotic Molecules That Inhibit Inflammatory Diseases. Appl. Sci. 2022, 12, 1147. [Google Scholar] [CrossRef]
- Thorakkattu, P.; Khanashyam, A.C.; Shah, K.; Babu, K.S.; Mundanat, A.S.; Deliephan, A.; Deokar, G.S.; Santivarangkna, C.; Nirmal, N.P. Postbiotics: Current Trends in Food and Pharmaceutical Industry. Foods 2022, 11, 3094. [Google Scholar] [CrossRef]
- Aggarwal, S.; Sabharwal, V.; Kaushik, P.; Joshi, A.; Aayushi, A.; Suri, M. Postbiotics: From emerging concept to application. Front. Sustain. Food Syst. 2022, 6, 887642. [Google Scholar] [CrossRef]
- Klaenhammer, T.R. Bacteriocins of lactic acid bacteria. Biochimie 1988, 70, 337–349. [Google Scholar] [CrossRef]
- Zimina, M.; Babich, O.; Prosekov, A.; Sukhikh, S.; Ivanova, S.; Shevchenko, M.; Noskova, S. Overview of Global Trends in Classification, Methods of Preparation and Application of Bacteriocins. Antibiotics 2020, 9, 553. [Google Scholar] [CrossRef] [PubMed]
- Simons, A.; Alhanout, K.; Duval, R.E. Bacteriocins, Antimicrobial Peptides from Bacterial Origin: Overview of Their Biology and Their Impact against Multidrug-Resistant Bacteria. Microorganisms 2020, 8, 639. [Google Scholar] [CrossRef] [PubMed]
- Darbandi, A.; Asadi, A.; Mahdizade Ari, M.; Ohadi, E.; Talebi, M.; Halaj Zadeh, M.; Darb Emamie, A.; Ghanavati, R.; Kakanj, M. Bacteriocins: Properties and potential use as antimicrobials. J. Clin. Lab. Anal. 2022, 36, e24093. [Google Scholar] [CrossRef]
- Brogden, K.A. Classification of Bacteriocins from Gram-Positive Bacteria. In Prokaryotic Antimicrobial Peptides: From Genes to Applications; Drider, D., Rebuffat, S., Eds.; Springer: New York, NY, USA, 2011; pp. 29–54. [Google Scholar] [CrossRef]
- Huang, F.; Teng, K.; Liu, Y.; Cao, Y.; Wang, T.; Ma, C.; Zhang, J.; Zhong, J. Bacteriocins: Potential for Human Health. Oxidative Med. Cell. Longev. 2021, 2021, 5518825. [Google Scholar] [CrossRef]
- Benítez-Chao, D.F.; León-Buitimea, A.; Lerma-Escalera, J.A.; Morones-Ramírez, J.R. Bacteriocins: An Overview of Antimicrobial, Toxicity, and Biosafety Assessment by in vivo Models. Front Microbiol. 2021, 12, 630695. [Google Scholar] [CrossRef]
- Fernandes, A.; Jobby, R. Bacteriocins from lactic acid bacteria and their potential clinical applications. Appl. Biochem. Biotechnol. 2022, 194, 4377–4399. [Google Scholar] [CrossRef]
- Doublier, S.; Cirrincione, S.; Scardaci, R.; Botta, C.; Lamberti, C.; Giuseppe, F.D.; Angelucci, S.; Rantsiou, K.; Cocolin, L.; Pessione, E. Putative probiotics decrease cell viability and enhance chemotherapy effectiveness in human cancer cells: Role of butyrate and secreted proteins. Microbiol. Res. 2022, 260, 127012. [Google Scholar] [CrossRef]
- Rani, A.; Saini, K.C.; Bast, F.; Varjani, S.; Mehariya, S.; Bhatia, S.K.; Sharma, N.; Funk, C. A Review on Microbial Products and Their Perspective Application as Antimicrobial Agents. Biomolecules 2021, 11, 1860. [Google Scholar] [CrossRef] [PubMed]
- Kaur, S.; Kaur, S. Bacteriocins as Potential Anticancer Agents. Front. Pharmacol. 2015, 6, 272. [Google Scholar] [CrossRef] [Green Version]
- Cesa-Luna, C.; Alatorre-Cruz, J.M.; Carreño-López, R.; Quintero-Hernández, V.; Baez, A. Emerging Applications of Bacteriocins as Antimicrobials, Anticancer Drugs, and Modulators of The Gastrointestinal Microbiota. Pol. J. Microbiol. 2021, 70, 143–159. [Google Scholar] [CrossRef] [PubMed]
- Alvarez-Sieiro, P.; Montalbán-López, M.; Mu, D.; Kuipers, O.P. Bacteriocins of lactic acid bacteria: Extending the family. Appl. Microbiol. Biotechnol. 2016, 100, 2939–2951. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Acedo, J.Z.; Chiorean, S.; Vederas, J.C.; van Belkum, M.J. The expanding structural variety among bacteriocins from Gram-positive bacteria. FEMS Microbiol. Rev. 2018, 42, 805–828. [Google Scholar] [CrossRef]
- Dobson, A.; Cotter, P.D.; Ross, R.P.; Hill, C. Bacteriocin production: A probiotic trait? Appl. Environ. Microbiol. 2012, 78, 1–6. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dreyer, L.; Smith, C.; Deane, S.M.; Dicks, L.M.T.; van Staden, A.D. Migration of Bacteriocins Across Gastrointestinal Epithelial and Vascular Endothelial Cells, as Determined Using In Vitro Simulations. Sci. Rep. 2019, 9, 11481. [Google Scholar] [CrossRef] [Green Version]
- Dicks, L.M.T.; Dreyer, L.; Smith, C.; van Staden, A.D. A Review: The Fate of Bacteriocins in the Human Gastro-Intestinal Tract: Do They Cross the Gut-Blood Barrier? Front. Microbiol. 2018, 9, 2297. [Google Scholar] [CrossRef] [Green Version]
- Jia, Z.; He, M.; Wang, C.; Chen, A.; Zhang, X.; Xu, J.; Fu, H.; Liu, B. Nisin reduces uterine inflammation in rats by modulating concentrations of pro- and anti-inflammatory cytokines. Am. J. Reprod. Immunol. 2019, 81, e13096. [Google Scholar] [CrossRef]
- De Pablo, M.A.; Gaforio, J.J.; Gallego, A.M.; Ortega, E.; Gálvez, A.M.; Alvarez de Cienfuegos López, G. Evaluation of immunomodulatory effects of nisin-containing diets on mice. FEMS Immunol. Med. Microbiol. 1999, 24, 35–42. [Google Scholar] [CrossRef] [Green Version]
- Małaczewska, J.; Kaczorek-Łukowska, E.; Wójcik, R.; Rękawek, W.; Siwicki, A.K. In vitro immunomodulatory effect of nisin on porcine leucocytes. J. Anim. Physiol. Anim. Nutr. 2019, 103, 882–893. [Google Scholar] [CrossRef]
- Kindrachuk, J.; Jenssen, H.; Elliott, M.; Nijnik, A.; Magrangeas-Janot, L.; Pasupuleti, M.; Thorson, L.; Ma, S.; Easton, D.M.; Bains, M.; et al. Manipulation of innate immunity by a bacterial secreted peptide: Lantibiotic nisin Z is selectively immunomodulatory. Innate Immun. 2013, 19, 315–327. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Begde, D.; Bundale, S.; Mashitha, P.; Rudra, J.; Nashikkar, N.; Upadhyay, A. Immunomodulatory efficacy of nisin--a bacterial lantibiotic peptide. J. Pept. Sci. 2011, 17, 438–444. [Google Scholar] [CrossRef] [PubMed]
- Lewies, A.; Du Plessis, L.H.; Wentzel, J.F. Antimicrobial Peptides: The Achilles’ Heel of Antibiotic Resistance? Probiotics Antimicrob. Proteins 2019, 11, 370–381. [Google Scholar] [CrossRef] [PubMed]
- Moein, M.; Imani Fooladi, A.A.; Mahmoodzadeh Hosseini, H. Determining the effects of green chemistry synthesized Ag-nisin nanoparticle on macrophage cells. Microb. Pathog. 2018, 114, 414–419. [Google Scholar] [CrossRef] [PubMed]
- Umair, M.; Jabbar, S.; Zhaoxin, L.; Jianhao, Z.; Abid, M.; Khan, K.R.; Korma, S.A.; Alghamdi, M.A.; El-Saadony, M.T.; Abd El-Hack, M.E.; et al. Probiotic-Based Bacteriocin: Immunity Supplementation Against Viruses. An Updated Review. Front. Microbiol. 2022, 13, 876058. [Google Scholar] [CrossRef]
- Wang, S.; Ye, Q.; Wang, K.; Zeng, X.; Huang, S.; Yu, H.; Ge, Q.; Qi, D.; Qiao, S. Enhancement of Macrophage Function by the Antimicrobial Peptide Sublancin Protects Mice from Methicillin-Resistant Staphylococcus aureus. J. Immunol. Res. 2019, 2019, 3979352. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, S.; Wang, Q.; Zeng, X.; Ye, Q.; Huang, S.; Yu, H.; Yang, T.; Qiao, S. Use of the Antimicrobial Peptide Sublancin with Combined Antibacterial and Immunomodulatory Activities to Protect against Methicillin-Resistant Staphylococcus aureus Infection in Mice. J. Agric. Food Chem. 2017, 65, 8595–8605. [Google Scholar] [CrossRef]
- Antoshina, D.V.; Balandin, S.V.; Bogdanov, I.V.; Vershinina, M.A.; Sheremeteva, E.V.; Toropygin, I.Y.; Finkina, E.I.; Ovchinnikova, T.V. Antimicrobial Activity and Immunomodulatory Properties of Acidocin A, the Pediocin-like Bacteriocin with the Non-Canonical Structure. Membranes 2022, 12, 1253. [Google Scholar] [CrossRef]
- Cotter, P.D.; Ross, R.P.; Hill, C. Bacteriocins—a viable alternative to antibiotics? Nat. Rev. Microbiol. 2013, 11, 95–105. [Google Scholar] [CrossRef]
- Meijerink, M.; van Hemert, S.; Taverne, N.; Wels, M.; de Vos, P.; Bron, P.A.; Savelkoul, H.F.; van Bilsen, J.; Kleerebezem, M.; Wells, J.M. Identification of genetic loci in Lactobacillus plantarum that modulate the immune response of dendritic cells using comparative genome hybridization. PLoS ONE 2010, 5, e10632. [Google Scholar] [CrossRef] [Green Version]
- Van Hemert, S.; Meijerink, M.; Molenaar, D.; Bron, P.A.; de Vos, P.; Kleerebezem, M.; Wells, J.M.; Marco, M.L. Identification of Lactobacillus plantarum genes modulating the cytokine response of human peripheral blood mononuclear cells. BMC Microbiol. 2010, 10, 293. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cong, J.; Zhou, P.; Zhang, R. Intestinal Microbiota-Derived Short Chain Fatty Acids in Host Health and Disease. Nutrients 2022, 14, 1977. [Google Scholar] [CrossRef]
- Akhtar, M.; Chen, Y.; Ma, Z.; Zhang, X.; Shi, D.; Khan, J.A.; Liu, H. Gut microbiota-derived short chain fatty acids are potential mediators in gut inflammation. Anim. Nutr. 2021, 8, 350–360. [Google Scholar] [CrossRef] [PubMed]
- Cummings, J.H.; Pomare, E.W.; Branch, W.J.; Naylor, C.P.; Macfarlane, G.T. Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut 1987, 28, 1221–1227. [Google Scholar] [CrossRef] [Green Version]
- Wang, H.Y.; Wang, C.; Guo, L.X.; Zheng, Y.F.; Hu, W.H.; Dong, T.T.X.; Wang, T.J.; Tsim, K.W.K. Simultaneous determination of short-chain fatty acids in human feces by HPLC with ultraviolet detection following chemical derivatization and solid-phase extraction segmental elution. J. Sep. Sci. 2019, 42, 2500–2509. [Google Scholar] [CrossRef]
- Rios-Covian, D.; González, S.; Nogacka, A.M.; Arboleya, S.; Salazar, N.; Gueimonde, M.; de Los Reyes-Gavilán, C.G. An Overview on Fecal Branched Short-Chain Fatty Acids Along Human Life and as Related with Body Mass Index: Associated Dietary and Anthropometric Factors. Front. Microbiol. 2020, 11, 973. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Z.; Zhang, H.; Chen, T.; Shi, L.; Wang, D.; Tang, D. Regulatory role of short-chain fatty acids in inflammatory bowel disease. Cell Commun. Signal. 2022, 20, 64. [Google Scholar] [CrossRef]
- Hanus, M.; Parada-Venegas, D.; Landskron, G.; Wielandt, A.M.; Hurtado, C.; Alvarez, K.; Hermoso, M.A.; López-Köstner, F.; De la Fuente, M. Immune System, Microbiota, and Microbial Metabolites: The Unresolved Triad in Colorectal Cancer Microenvironment. Front. Immunol. 2021, 12, 612826. [Google Scholar] [CrossRef]
- Gill, P.A.; van Zelm, M.C.; Muir, J.G.; Gibson, P.R. Review article: Short chain fatty acids as potential therapeutic agents in human gastrointestinal and inflammatory disorders. Aliment Pharmacol. Ther. 2018, 48, 15–34. [Google Scholar] [CrossRef] [Green Version]
- Parada Venegas, D.; De la Fuente, M.K.; Landskron, G.; González, M.J.; Quera, R.; Dijkstra, G.; Harmsen, H.J.M.; Faber, K.N.; Hermoso, M.A. Short Chain Fatty Acids (SCFAs)-Mediated Gut Epithelial and Immune Regulation and Its Relevance for Inflammatory Bowel Diseases. Front. Immunol. 2019, 10, 277. [Google Scholar] [CrossRef] [Green Version]
- Van der Hee, B.; Wells, J.M. Microbial Regulation of Host Physiology by Short-chain Fatty Acids. Trends Microbiol. 2021, 29, 700–712. [Google Scholar] [CrossRef] [PubMed]
- Ramos Meyers, G.; Samouda, H.; Bohn, T. Short Chain Fatty Acid Metabolism in Relation to Gut Microbiota and Genetic Variability. Nutrients 2022, 14, 5361. [Google Scholar] [CrossRef]
- Siddiqui, M.T.; Cresci, G.A.M. The Immunomodulatory Functions of Butyrate. J. Inflamm. Res. 2021, 14, 6025–6041. [Google Scholar] [CrossRef] [PubMed]
- Jenab, A.; Roghanian, R.; Emtiazi, G. Bacterial Natural Compounds with Anti-Inflammatory and Immunomodulatory Properties (Mini Review). Drug Des. Dev. Ther. 2020, 14, 3787–3801. [Google Scholar] [CrossRef] [PubMed]
- Ranjbar, R.; Vahdati, S.N.; Tavakoli, S.; Khodaie, R.; Behboudi, H. Immunomodulatory roles of microbiota-derived short-chain fatty acids in bacterial infections. Biomed. Pharmacother. 2021, 141, 111817. [Google Scholar] [CrossRef]
- Kim, C.H. Control of lymphocyte functions by gut microbiota-derived short-chain fatty acids. Cell Mol. Immunol. 2021, 18, 1161–1171. [Google Scholar] [CrossRef]
- Yue, X.; Wen, S.; Long-Kun, D.; Man, Y.; Chang, S.; Min, Z.; Shuang-Yu, L.; Xin, Q.; Jie, M.; Liang, W. Three important short-chain fatty acids (SCFAs) attenuate the inflammatory response induced by 5-FU and maintain the integrity of intestinal mucosal tight junction. BMC Immunol. 2022, 23, 19. [Google Scholar] [CrossRef]
- Louis, P.; Duncan, S.; Sheridan, P.; Walker, A.; Flint, H. Microbial lactate utilisation and the stability of the gut microbiome. Gut Microbiome 2022, 3, E3. [Google Scholar] [CrossRef]
- Iraporda, C.; Errea, A.; Romanin, D.E.; Cayet, D.; Pereyra, E.; Pignataro, O.; Sirard, J.C.; Garrote, G.L.; Abraham, A.G.; Rumbo, M. Lactate and short chain fatty acids produced by microbial fermentation downregulate proinflammatory responses in intestinal epithelial cells and myeloid cells. Immunobiology 2015, 220, 1161–1169. [Google Scholar] [CrossRef]
- Caffaratti, C.; Plazy, C.; Mery, G.; Tidjani, A.R.; Fiorini, F.; Thiroux, S.; Toussaint, B.; Hannani, D.; Le Gouellec, A. What We Know So Far about the Metabolite-Mediated Microbiota-Intestinal Immunity Dialogue and How to Hear the Sound of This Crosstalk. Metabolites 2021, 11, 406. [Google Scholar] [CrossRef]
- Garrote, G.L.; Abraham, A.G.; Rumbo, M. Is lactate an undervalued functional component of fermented food products? Front. Microbiol. 2015, 6, 629. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Iraporda, C.; Romanin, D.E.; Bengoa, A.A.; Errea, A.J.; Cayet, D.; Foligné, B.; Sirard, J.C.; Garrote, G.L.; Abraham, A.G.; Rumbo, M. Local Treatment with Lactate Prevents Intestinal Inflammation in the TNBS-Induced Colitis Model. Front. Immunol. 2016, 7, 651. [Google Scholar] [CrossRef]
- Manoharan, I.; Prasad, P.D.; Thangaraju, M.; Manicassamy, S. Lactate-Dependent Regulation of Immune Responses by Dendritic Cells and Macrophages. Front. Immunol. 2021, 12, 691134. [Google Scholar] [CrossRef]
- Lee, T.Y. Lactate: A multifunctional signaling molecule. Yeungnam Univ. J. Med. 2021, 38, 183–193. [Google Scholar] [CrossRef] [PubMed]
- Caslin, H.L.; Abebayehu, D.; Pinette, J.A.; Ryan, J.J. Lactate Is a Metabolic Mediator That Shapes Immune Cell Fate and Function. Front. Physiol. 2021, 12, 688485. [Google Scholar] [CrossRef]
- Pujari, R.; Banerjee, G. Impact of prebiotics on immune response: From the bench to the clinic. Immunol. Cell Biol. 2021, 99, 255–273. [Google Scholar] [CrossRef]
- Mirzaei, R.; Afaghi, A.; Babakhani, S.; Sohrabi, M.R.; Hosseini-Fard, S.R.; Babolhavaeji, K.; Khani Ali Akbari, S.; Yousefimashouf, R.; Karampoor, S. Role of microbiota-derived short-chain fatty acids in cancer development and prevention. Biomed. Pharmacother. 2021, 139, 111619. [Google Scholar] [CrossRef]
- Li, C.; Liang, Y.; Qiao, Y. Messengers from the Gut: Gut Microbiota-Derived Metabolites on Host Regulation. Front. Microbiol. 2022, 13, 863407. [Google Scholar] [CrossRef]
- Levy, M.; Thaiss, C.A.; Zeevi, D.; Dohnalová, L.; Zilberman-Schapira, G.; Mahdi, J.A.; David, E.; Savidor, A.; Korem, T.; Herzig, Y.; et al. Microbiota-Modulated Metabolites Shape the Intestinal Microenvironment by Regulating NLRP6 Inflammasome Signaling. Cell 2015, 163, 1428–1443. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Russo, E.; Giudici, F.; Fiorindi, C.; Ficari, F.; Scaringi, S.; Amedei, A. Immunomodulating Activity and Therapeutic Effects of Short Chain Fatty Acids and Tryptophan Post-biotics in Inflammatory Bowel Disease. Front. Immunol. 2019, 10, 2754. [Google Scholar] [CrossRef] [Green Version]
- Kinoshita, M.; Suzuki, Y.; Saito, Y. Butyrate reduces colonic paracellular permeability by enhancing PPARgamma activation. Biochem. Biophys. Res. Commun. 2002, 293, 827–831. [Google Scholar] [CrossRef]
- Deleu, S.; Machiels, K.; Raes, J.; Verbeke, K.; Vermeire, S. Short chain fatty acids and its producing organisms: An overlooked therapy for IBD? EBioMedicine 2021, 66, 103293. [Google Scholar] [CrossRef]
- Kamp, M.E.; Shim, R.; Nicholls, A.J.; Oliveira, A.C.; Mason, L.J.; Binge, L.; Mackay, C.R.; Wong, C.H. G Protein-Coupled Receptor 43 Modulates Neutrophil Recruitment during Acute Inflammation. PLoS ONE 2016, 11, e0163750. [Google Scholar] [CrossRef] [Green Version]
- Maslowski, K.M.; Vieira, A.T.; Ng, A.; Kranich, J.; Sierro, F.; Yu, D.; Schilter, H.C.; Rolph, M.S.; Mackay, F.; Artis, D.; et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 2009, 461, 1282–1286. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nakkarach, A.; Foo, H.L.; Song, A.A.L.; Mutalib, N.E.A.; Nitisinprasert, S.; Withayagiat, U. Anti-cancer and anti-inflammatory effects elicited by short chain fatty acids produced by Escherichia coli isolated from healthy human gut microbiota. Microb. Cell Factories 2021, 20, 36. [Google Scholar] [CrossRef]
- Ji, J.; Shu, D.; Zheng, M.; Wang, J.; Luo, C.; Wang, Y.; Guo, F.; Zou, X.; Lv, X.; Li, Y.; et al. Microbial metabolite butyrate facilitates M2 macrophage polarization and function. Sci. Rep. 2016, 6, 24838. [Google Scholar] [CrossRef]
- Singh, N.; Gurav, A.; Sivaprakasam, S.; Brady, E.; Padia, R.; Shi, H.; Thangaraju, M.; Prasad, P.D.; Manicassamy, S.; Munn, D.H.; et al. Activation of Gpr109a, receptor for niacin and the commensal metabolite butyrate, suppresses colonic inflammation and carcinogenesis. Immunity 2014, 40, 128–139. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Arpaia, N.; Campbell, C.; Fan, X.; Dikiy, S.; van der Veeken, J.; deRoos, P.; Liu, H.; Cross, J.R.; Pfeffer, K.; Coffer, P.J.; et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 2013, 504, 451–455. [Google Scholar] [CrossRef] [Green Version]
- Park, J.; Kim, M.; Kang, S.G.; Jannasch, A.H.; Cooper, B.; Patterson, J.; Kim, C.H. Short-chain fatty acids induce both effector and regulatory T cells by suppression of histone deacetylases and regulation of the mTOR-S6K pathway. Mucosal Immunol. 2015, 8, 80–93. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nastasi, C.; Candela, M.; Bonefeld, C.M.; Geisler, C.; Hansen, M.; Krejsgaard, T.; Biagi, E.; Andersen, M.H.; Brigidi, P.; Ødum, N.; et al. The effect of short-chain fatty acids on human monocyte-derived dendritic cells. Sci. Rep. 2015, 5, 16148. [Google Scholar] [CrossRef] [Green Version]
- Poggi, A.; Benelli, R.; Venè, R.; Costa, D.; Ferrari, N.; Tosetti, F.; Zocchi, M.R. Human Gut-Associated Natural Killer Cells in Health and Disease. Front. Immunol. 2019, 10, 961. [Google Scholar] [CrossRef] [Green Version]
- Smith, P.M.; Howitt, M.R.; Panikov, N.; Michaud, M.; Gallini, C.A.; Bohlooly-y, M.; Glickman, J.N.; Garrett, W.S. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 2013, 341, 569–573. [Google Scholar] [CrossRef] [Green Version]
- Sun, M.; Wu, W.; Liu, Z.; Cong, Y. Microbiota metabolite short chain fatty acids, GPCR, and inflammatory bowel diseases. J. Gastroenterol. 2017, 52, 1–8. [Google Scholar] [CrossRef] [PubMed]
- Yang, W.; Cong, Y. Gut microbiota-derived metabolites in the regulation of host immune responses and immune-related inflammatory diseases. Cell. Mol. Immunol. 2021, 18, 866–877. [Google Scholar] [CrossRef] [PubMed]
- He, Y.; Fu, L.; Li, Y.; Wang, W.; Gong, M.; Zhang, J.; Dong, X.; Huang, J.; Wang, Q.; Mackay, C.R.; et al. Gut microbial metabolites facilitate anticancer therapy efficacy by modulating cytotoxic CD8+ T cell immunity. Cell Metab. 2021, 33, 988–1000.e7. [Google Scholar] [CrossRef]
- Kim, M.; Qie, Y.; Park, J.; Kim, C.H. Gut Microbial Metabolites Fuel Host Antibody Responses. Cell Host Microbe 2016, 20, 202–214. [Google Scholar] [CrossRef] [Green Version]
- Kim, C.H. B cell-helping functions of gut microbial metabolites. Microb. Cell. 2016, 3, 529–531. [Google Scholar] [CrossRef] [Green Version]
- Iraporda, C.; Romanin, D.; Rumbo, M.; Garrote, G.; Abraham, A. The role of lactate in the immunomodulatory properties of kefir non bacterial fraction. Food Res. Int. 2014, 62, 247–253. [Google Scholar] [CrossRef]
- Awasthi, D.; Nagarkoti, S.; Sadaf, S.; Chandra, T.; Kumar, S.; Dikshit, M. Glycolysis dependent lactate formation in neutrophils: A metabolic link between NOX-dependent and independent NETosis. Biochim. Biophys. Acta (BBA) Mol. Basis Dis. 2019, 1865, 165542. [Google Scholar] [CrossRef]
- Ranganathan, P.; Shanmugam, A.; Swafford, D.; Suryawanshi, A.; Bhattacharjee, P.; Hussein, M.S.; Koni, P.A.; Prasad, P.D.; Kurago, Z.B.; Thangaraju, M.; et al. GPR81, a Cell-Surface Receptor for Lactate, Regulates Intestinal Homeostasis and Protects Mice from Experimental Colitis. J. Immunol. 2018, 200, 1781–1789. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Errea, A.; Cayet, D.; Marchetti, P.; Tang, C.; Kluza, J.; Offermanns, S.; Sirard, J.-C.; Rumbo, M. Lactate Inhibits the Pro-Inflammatory Response and Metabolic Reprogramming in Murine Macrophages in a GPR81-Independent Manner. PLoS ONE 2016, 11, e0163694. [Google Scholar] [CrossRef] [Green Version]
- Shan, T.; Chen, S.; Chen, X.; Wu, T.; Yang, Y.; Li, S.; Ma, J.; Zhao, J.; Lin, W.; Li, W.; et al. M2-TAM subsets altered by lactic acid promote T-cell apoptosis through the PD-L1/PD-1 pathway. Oncol. Rep. 2020, 44, 1885–1894. [Google Scholar] [CrossRef] [PubMed]
- Dietl, K.; Renner, K.; Dettmer, K.; Timischl, B.; Eberhart, K.; Dorn, C.; Hellerbrand, C.; Kastenberger, M.; Kunz-Schughart, L.A.; Oefner, P.J.; et al. Lactic Acid and Acidification Inhibit TNF Secretion and Glycolysis of Human Monocytes. J. Immunol. 2010, 184, 1200–1209. [Google Scholar] [CrossRef] [Green Version]
- Wang, Ζ.H.; Peng, W.B.; Zhang, P.; Yang, X.P.; Zhou, Q. Lactate in the tumour microenvironment: From immune modulation to therapy. EBioMedicine 2021, 73, 103627. [Google Scholar] [CrossRef]
- Apostolova, P.; Pearce, E.L. Lactic acid and lactate: Revisiting the physiological roles in the tumor microenvironment. Trends Immunol. 2022, 43, 969–977. [Google Scholar] [CrossRef]
- Haas, R.; Smith, J.; Rocher-Ros, V.; Nadkarni, S.; Montero-Melendez, T.; D’Acquisto, F.; Bland, E.J.; Bombardieri, M.; Pitzalis, C.; Perretti, M.; et al. Lactate regulates metabolic and proinflammatory circuits in control of T cell migration and effector functions. PLoS Biol. 2015, 13, e1002202. [Google Scholar] [CrossRef] [PubMed]
- Angelin, A.; Gil-de-Gómez, L.; Dahiya, S.; Jiao, J.; Guo, L.; Levine, M.H.; Wang, Z.; Quinn, W.J.; Kopinski, P.K.; Wang, L.; et al. Foxp3 Reprograms T Cell Metabolism to Function in Low-Glucose, High-Lactate Environments. Cell Metab. 2017, 25, 1282–1293.e7. [Google Scholar] [CrossRef] [Green Version]
- Rodriguez-Arrastia, M.; Martinez-Ortigosa, A.; Rueda-Ruzafa, L.; Folch Ayora, A.; Ropero-Padilla, C. Probiotic Supplements on Oncology Patients’ Treatment-Related Side Effects: A Systematic Review of Randomized Controlled Trials. Int. J. Environ. Res. Public Health. 2021, 18, 4265. [Google Scholar] [CrossRef] [PubMed]
- Sanders, M.E.; Akkermans, L.M.; Haller, D.; Hammerman, C.; Heimbach, J.; Hörmannsperger, G.; Huys, G.; Levy, D.D.; Lutgendorff, F.; Mack, D.; et al. Safety assessment of probiotics for human use. Gut Microbes 2010, 1, 164–185. [Google Scholar] [CrossRef]
- Heilbronner, S.; Krismer, B.; Brötz-Oesterhelt, H.; Peschel, A. The microbiome-shaping roles of bacteriocins. Nat. Rev. Microbiol. 2021, 19, 726–739. [Google Scholar] [CrossRef]
- Flynn, J.; Ryan, A.; Hudson, S.P. Pre-formulation and delivery strategies for the development of bacteriocins as next generation antibiotics. Eur. J. Pharm. Biopharm. 2021, 165, 149–163. [Google Scholar] [CrossRef]
- Todorov, S.D.; Popov, I.; Weeks, R.; Chikindas, M.L. Use of Bacteriocins and Bacteriocinogenic Beneficial Organisms in Food Products: Benefits, Challenges, Concerns. Foods 2022, 11, 3145. [Google Scholar] [CrossRef]
- Zou, J.; Jiang, H.; Cheng, H.; Fang, J.; Huang, G. Strategies for screening, purification and characterization of bacteriocins. Int. J. Biol. Macromol. 2018, 117, 781–789. [Google Scholar] [CrossRef] [PubMed]
- Xiong, R.-G.; Zhou, D.-D.; Wu, S.-X.; Huang, S.-Y.; Saimaiti, A.; Yang, Z.-J.; Shang, A.; Zhao, C.-N.; Gan, R.-Y.; Li, H.-B. Health Benefits and Side Effects of Short-Chain Fatty Acids. Foods 2022, 11, 2863. [Google Scholar] [CrossRef] [PubMed]
- Koh, A.; De Vadder, F.; Kovatcheva-Datchary, P.; Bäckhed, F. From Dietary Fiber to Host Physiology: Short-Chain Fatty Acids as Key Bacterial Metabolites. Cell 2016, 165, 1332–1345. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Cell Type | Immunomodulatory Effect | References |
---|---|---|
IECs | Downregulation of pro-inflammatory cytokines | [133,136] |
Abrogation of IECs activation depending on TLRs and IL-1β | [162] | |
Neutrophils | NETs formation | [139,163] |
DCs | GPR81 activation, suppression of colonic inflammation | [137,164] |
Cell surface markers modulation and cytokine secretion in LPS-activated DCs | [133,137] | |
Macrophages | GPR81-independent metabolic changes, pro-inflammatory cytokines reduction | [165] |
GPR81 activation, suppression of colonic inflammation | [137,164] | |
M2 macrophage polarization, IL-10 increase, IL-12 decrease | [166] | |
Downregulation of cytokine secretion in LPS-activated macrophages | [133] | |
Monocytes | Inhibition of glycolysis, suppression of TNF-α secretion in the TME | [167] |
CD4+ T cells | Glycolysis-dependent inhibition of motility, Th17 differentiation, increased IL-17 levels | [170] |
Tregs proliferation | [171] | |
CD8+ T cells | Glycolysis-independent inhibition of motility, loss of cytolytic function | [170] |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Thoda, C.; Touraki, M. Immunomodulatory Properties of Probiotics and Their Derived Bioactive Compounds. Appl. Sci. 2023, 13, 4726. https://doi.org/10.3390/app13084726
Thoda C, Touraki M. Immunomodulatory Properties of Probiotics and Their Derived Bioactive Compounds. Applied Sciences. 2023; 13(8):4726. https://doi.org/10.3390/app13084726
Chicago/Turabian StyleThoda, Christina, and Maria Touraki. 2023. "Immunomodulatory Properties of Probiotics and Their Derived Bioactive Compounds" Applied Sciences 13, no. 8: 4726. https://doi.org/10.3390/app13084726