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The Evaluation of the Effect of Tolerogenic Probiotics on the Maturation of Healthy Dendritic Cells versus Immature Dendritic Cells

Document Type : Original Article

Authors

1 Immunology Research Center, Mashhad University of Medical Sciences, Mashhad, Iran.

2 Immunology Department, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran.

3 Skin Cancer Prevention Research Center, Torvergata University of Medical Sciences, Rome, Italy.

4 Department of Basic Sciences, Faculty of Medicine, Infectious Diseases Research Center, Gonabad University of Medical Science, Gonabad, Iran.

Abstract

Background: Dendritic cells, (DCs) as one of the important immune cell populations, are responsible for the initiation, development, and control of acquired immune responses. Myeloid dendritic cells can be used as a vaccine for several autoimmune diseases and cancers. Tolerogenic probiotics with regulatory properties can affect the maturation and development of immature dendritic cells (IDC) into mature DCs with certain immunomodulatory effects.
Objective: To assess the immunomodulatory effect of Lactobacillus rhamnosus and Lactobacillus delbrueckii, as two tolerogenic probiotics, in the differentiation and maturation of myeloid dendritic cells.
Methods: The IDCs were derived from the healthy donors in GM-CSF and IL 4 medium. Mature DCs (MDC) were produced with L. delbrueckii, L. rhamnosus, and LPS from IDCs. Real-Time PCR and flow cytometry were used to confirm the DC maturation and to determine DC markers as well as IDO, IL10, and IL12 expression levels, respectively.
Results: Probiotic-derived DCs showed a significant reduction in the level of HLA-DR (P≤0.05), CD86 (P≤0.05), CD80 (P≤0.001), CD83 (P≤0.001), and CD1a. Also, the expression of IDO (P≤0.001) and IL10 increased while IL12 expression decreased (P≤0.001).
Conclusion: Our findings revealed that tolerogenic probiotics could induce regulatory DCs by reducing co-stimulatory molecules along with increasing the expression of IDO and IL10 during the differentiation process. Therefore, the induced regulatory DCs probably can be used in the treatment of various inflammatory diseases.

Keywords

References
  1. Mellman I. Dendritic cells: master regulators of the immune response. Cancer immunology research 2013; 1:145-149.
  2. Steinman RM, editor Linking innate to adaptive immunity through dendritic cells. Novartis Foundation symposium; 2006.
  3. Mahnke K, Schmitt E, Bonifaz L, Enk AH, Jonuleit H. Immature, but not inactive: the tolerogenic function of immature dendritic cells. Immunology & Cell Biology 2002; 80:477-483.
  4. Saxena M, Bhardwaj N. Re-Emergence of Dendritic Cell Vaccines for Cancer Treatment. Trends in cancer 2018.
  5. Raker VK, Domogalla MP, Steinbrink K. Tolerogenic dendritic cells for regulatory T cell induction in man. Frontiers in immunology 2015; 6:569.
  6. Schmidt SV, Nino-Castro AC, Schultze JL. Regulatory dendritic cells: there is more than just immune activation. Frontiers in immunology 2012; 3:274.
  7. Esmaeili S-A, Taheri RA, Mahmoudi M, Momtazi-Borojeni AA, Morshedi M, Bahramifar A, et al. Inhibitory effects of tolerogenic probiotics on migratory potential of lupus patient-derived DCs. Iranian Journal of Basic Medical Sciences 2021; 24:1509-1514.
  8. Baroroh HN, Nugroho AE, Lukitaningsih E, Nurrochmad A. Immune-enhancing effect of bengkoang (Pachyrhizus erosus (L.) Urban) fiber fractions on mouse peritoneal macrophages, lymphocytes, and cytokines. J Nat Sci Biol Med 2021; 12:84.
  9. Esmaeili A, Rabe SZT, Mahmoudi M, Rastin M. Frequencies of HLA-A, B and DRB1 alleles in a large normal population living in the city of Mashhad, Northeastern Iran. Iranian journal of basic medical sciences 2017; 20:940.
  10. Lim TS, Goh JKH, Mortellaro A, Lim CT, Hämmerling GJ, Ricciardi-Castagnoli P. CD80 and CD86 differentially regulate mechanical interactions of T-cells with antigen-presenting dendritic cells and B-cells. PloS one 2012; 7:e45185.
  11. Aerts‐Toegaert C, Heirman C, Tuyaerts S, Corthals J, Aerts JL, Bonehill A, et al. CD83 expression on dendritic cells and T cells: correlation with effective immune responses. European journal of immunology 2007; 37:686-695.
  12. Chang C-CJ, Wright A, Punnonen J. Monocyte-derived CD1a+ and CD1a− dendritic cell subsets differ in their cytokine production profiles, susceptibilities to transfection, and capacities to direct Th cell differentiation. The Journal of Immunology 2000; 165:3584-3591.
  13. Curti A, Ferri E, Pandolfi S, Isidori A, Lemoli RM. Dendritic cell differentiation. The Journal of Immunology 2004; 172:3-4.
  14. Momtazi-Borojeni AA, Haftcheshmeh SM, Esmaeili S-A, Johnston TP, Abdollahi E, Sahebkar A. Curcumin: A natural modulator of immune cells in systemic lupus erythematosus. Autoimmunity reviews 2017.
  15. Abbas Momtazi-Borojeni A, Esmaeili S-A, Abdollahi E, Sahebkar A. A Review on the pharmacology and toxicology of steviol glycosides extracted from Stevia rebaudiana. Current pharmaceutical design 2017; 23:1616-1622.
  16. Esmaeili SA, Mahmoudi M, Momtazi AA, Sahebkar A, Doulabi H, Rastin M. Tolerogenic probiotics: potential immunoregulators in Systemic Lupus Erythematosus. Journal of cellular physiology 2017; 232:1994-2007.
  17. Atabati H, Yazdanpanah E, Mortazavi H, Raoofi A, Esmaeili S-A, Khaledi A, et al. Immunoregulatory effects of tolerogenic probiotics in multiple sclerosis. Reviews on New Drug Targets in Age-Related Disorders 2021:87-105.
  18. Al-Shawi SG, Ali HI, Abd HM. Producing of probiotics Monterey cheese and study its chemicalcomposition. Pakistan Journal of Biotechnology 2019; 16:205-209.
  19. Medina M, Izquierdo E, Ennahar S, Sanz Y. Differential immunomodulatory properties of Bifidobacterium logum strains: relevance to probiotic selection and clinical applications. Clinical & Experimental Immunology 2007; 150:531-538.
  20. Konieczna P, Schiavi E, Ziegler M, Groeger D, Healy S, Grant R, et al. Human dendritic cell DC-SIGN and TLR-2 mediate complementary immune regulatory activities in response to Lactobacillus rhamnosus JB-1. PLoS One 2015; 10:e0120261.
  21. Ghadimi D, Helwig U, Schrezenmeir J, Heller KJ, Vrese M. Epigenetic imprinting by commensal probiotics inhibits the IL‐23/IL‐17 axis in an in vitro model of the intestinal mucosal immune system. Journal of leukocyte biology 2012; 92:895-911.
  22. van der Kleij H, O'Mahony C, Shanahan F, O'Mahony L, Bienenstock J. Protective effects of Lactobacillus reuteri and Bifidobacterium infantis in murine models for colitis do not involve the vagus nerve. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology 2008; 295:R1131-R1137.
  23. Ferstl R, Frei R, Schiavi E, Konieczna P, Barcik W, Ziegler M, et al. Histamine receptor 2 is a key influence in immune responses to intestinal histamine-secreting microbes. Journal of Allergy and Clinical Immunology 2014; 134:744-746. e743.
  24. Salehipour Z, Haghmorad D, Sankian M, Rastin M, Nosratabadi R, Dallal MMS, et al. Bifidobacterium animalis in combination with human origin of Lactobacillus plantarum ameliorate neuroinflammation in experimental model of multiple sclerosis by altering CD4+ T cell subset balance. Biomedicine & Pharmacotherapy 2017; 95:1535-1548.
  25. Santos Rocha C, Lakhdari O, Blottière HM, Blugeon S, Sokol H, Bermu'Dez-Humara'N LG, et al. Anti-inflammatory properties of dairy lactobacilli. Inflammatory bowel diseases 2011; 18:657-666.
  26. Rocha CS, Gomes-Santos AC, Moreira TG, De Azevedo M, Luerce TD, Mariadassou M, et al. Local and systemic immune mechanisms underlying the anti-colitis effects of the dairy bacterium Lactobacillus delbrueckii. PLoS One 2014; 9:e85923.
  27. Popov I, Li M, Zheng X, San H, Zhang X, Ichim TE, et al. Preventing autoimmune arthritis using antigen-specific immature dendritic cells: a novel tolerogenic vaccine. Arthritis research & therapy 2006; 8:R141.
  28. Gordon JR, Ma Y, Churchman L, Gordon SA, Dawicki W. Regulatory dendritic cells for immunotherapy in immunologic diseases. Frontiers in immunology 2014; 5:7.
  29. Shortman K, Naik SH. Steady-state and inflammatory dendritic-cell development. Nature Reviews Immunology 2007; 7:19.
  30. Esmaeili SA, Mahmoudi M, Rezaieyazdi Z, Sahebari M, Tabasi N, Sahebkar A, et al. Generation of tolerogenic dendritic cells using Lactobacillus rhamnosus and Lactobacillus delbrueckii as tolerogenic probiotics. Journal of cellular biochemistry 2018; 119:7865-7872.
  31. Radmanesh F, Mahmoudi M, Yazdanpanah E, Keyvani V, Kia N, Nikpoor AR, et al. The immunomodulatory effects of mesenchymal stromal cell‐based therapy in human and animal models of systemic lupus erythematosus. IUBMB life 2020; 72:2366-2381.
  32. You J, Dong H, Mann ER, Knight SC, Yaqoob P. Probiotic modulation of dendritic cell function is influenced by ageing. Immunobiology 2014; 219:138-148.
  33. Al-Shawi SG, Dang DS, Yousif AY, Al-Younis ZK, Najm TA, Matarneh SK. The potential use of probiotics to improve animal health, efficiency, and meat quality: A Review. Agriculture 2020; 10:452.
  34. Evrard B, Coudeyras S, Dosgilbert A, Charbonnel N, Alamé J, Tridon A, et al. Dose-dependent immunomodulation of human dendritic cells by the probiotic Lactobacillus rhamnosus Lcr35. PLos one 2011; 6:e18735.
  35. Vahidi Z, Samadi M, Mahmoudi M, RezaieYazdi Z, Sahebari M, Tabasi N, et al. Lactobacillus rhamnosus and Lactobacillus delbrueckii ameliorate the expression of miR-155 and miR-181a in SLE patients. Journal of functional foods 2018; 48:228-233.
  36. Khorasani S, Mahmoudi M, Kalantari MR, Lavi Arab F, Esmaeili SA, Mardani F, et al. Amelioration of regulatory T cells by Lactobacillus delbrueckii and Lactobacillus rhamnosus in pristane‐induced lupus mice model. Journal of Cellular Physiology.
  37. Mardani F, Mahmoudi M, Esmaeili SA, Khorasani S, Tabasi N, Rastin M. In vivo study: Th1–Th17 reduction in pristane‐induced systemic lupus erythematosus mice after treatment with tolerogenic Lactobacillus probiotics. Journal of cellular physiology 2018.
  38. Kawamura K, Iyonaga K, Ichiyasu H, Nagano J, Suga M, Sasaki Y. Differentiation, maturation, and survival of dendritic cells by osteopontin regulation. Clinical and diagnostic laboratory immunology 2005; 12:206-212.
  39. Han TH, Jin P, Ren J, Slezak S, Marincola FM, Stroncek DF. Evaluation of three clinical dendritic cell maturation protocols containing lipopolysaccharide and interferon-gamma. Journal of immunotherapy (Hagerstown, Md: 1997) 2009; 32:399.
  40. Yin W, Ouyang S, Li Y, Xiao B, Yang H. Immature dendritic cell-derived exosomes: a promise subcellular vaccine for autoimmunity. Inflammation 2013; 36:232-240.
  41. Castiello L, Sabatino M, Jin P, Clayberger C, Marincola FM, Krensky AM, et al. Monocyte-derived DC maturation strategies and related pathways: a transcriptional view. Cancer immunology, immunotherapy 2011; 60:457-466.
  42. Muller-Berghaus J, Olson WC, Moulton RA, Knapp WT, Schadendorf D, Storkus WJ. IL-12 production by human monocyte-derived dendritic cells: looking at the single cell. Journal of Immunotherapy 2005; 28:306-313.
  43. Fong FLY, Kirjavainen P, Wong VHY, El-Nezami H. Immunomodulatory effects of Lactobacillus rhamnosus GG on dendritic cells, macrophages and monocytes from healthy donors. Journal of Functional Foods 2015; 13:71-79.
  44. Smits HH, Engering A, van der Kleij D, de Jong EC, Schipper K, van Capel TM, et al. Selective probiotic bacteria induce IL-10–producing regulatory T cells in vitro by modulating dendritic cell function through dendritic cell–specific intercellular adhesion molecule 3–grabbing nonintegrin. Journal of Allergy and Clinical Immunology 2005; 115:1260-1267.
Iranian Journal of Immunology
Volume 20, Issue 1
March 2023
Pages 26-35
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