Immunosuppressive Effects of Two Probiotics, Lactobacillus paracasei DSM 13434 and Lactobacillus plantarum DSM 15312, on CD4+ T Cells of Multiple Sclerosis Patients
-
Khadijeh Chakamian
,
Behrouz Robat-Jazi
,
Abdorreza Naser Moghadasi
,
Fatemeh Mansouri
,
Masoumeh Nodehi
,
Elahe Motevaseli
,
Maryam Izad
,
Saeed Yekaninejad
,
Mahdieh Shirzad
,
Kiana Bidad
,
Mona Oraei
,
Bita Ansaripour
,
Ali Akbar Saboor-Yaraghi
Abstract
T cells play an important role in the development and progression of multiple sclerosis (MS), an autoimmune disease of the central nervous system. In the present study, the immunomodulatory impacts of two Lactobacillus strains, L paracasei DSM 13434 and L plantarum DSM 15312, on the frequency and cytokine production of CD4+ T cells in MS patients were explored.
Thirty MS patients were enrolled in this study. The CD4+ T cells were isolated, cultured, and exposed to the media containing cell-free supernatants of L plantarum (group1), L paracasei (group 2), the mixture group of cell-free supernatants of both probiotics (group 3), and vehicle (control) group (group 4). The frequencies of T helper (Th) 1, Th17, Th2, and T regulatory type 1 (Tr1) cells and mean fluorescent intensity (MFI) of the associated cytokines were assessed using flow cytometry. The levels of interleukin 17 (IL-17), transforming growth factor β (TGF-β), and interferon-gamma (IFN-γ) cytokines in supernatants of all groups were measured by enzyme-linked immunosorbent assay.
The percentage of Th1 cells and the MFI of IFN-γ in Th1 cells (CD4+ IFN-γ+) in all three probiotic treatment groups were significantly decreased compared to the control group. However, no significant changes were observed in the proportion and MFI of Th2, Th17, and Tr1 cells. A significant decrease was observed in IL-17 secretion in the supernatant of cultured CD4+ T cells in all three treatment groups in comparison with control. The levels of TGF-β and IFN-γ were not significantly different among any of the study groups.
Collectively, cell-free supernatants of the lactobacilli showed an in vitro anti-inflammatory effect. However, further studies are needed to prove the real effects of probiotics on MS.
1. Goverman J. Autoimmune T cell responses in the central nervous system. Nat Rev Immunol. 2009;9(6):393-407.
2. Ryu CH, Park KY, Hou Y, Jeong CH, Kim SM, Jeun SS. Gene therapy of multiple sclerosis using interferon beta-secreting human bone marrow mesenchymal stem cells. Biomed Res Int. 2013;2013:696738.
3. Cheng W, Chen G. Chemokines and chemokine receptors in multiple sclerosis. Mediators Inflamm. 2014;2014:659206.
4. Yamashita M, Ukibe K, Matsubara Y, Hosoya T, Sakai F, Kon S, et al. Lactobacillus helveticus SBT2171 Attenuates Experimental Autoimmune Encephalomyelitis in Mice. Front Microbiol. 2017;8:2596.
5. Ochoa-Reparaz J, Kasper LH. The influence of gut-derived CD39 regulatory T cells in CNS demyelinating disease. Transl Res. 2017;179:126-38.
6. Jangi S, Gandhi R, Cox LM, Li N, von Glehn F, Yan R, et al. Alterations of the human gut microbiome in multiple sclerosis. Nat Commun. 2016;7:12015.
7. Zhang X, Zhang D, Jia H, Feng Q, Wang D, Liang D, et al. The oral and gut microbiomes are perturbed in rheumatoid arthritis and partly normalized after treatment. Nat Med. 2015;21(8):895-905.
8. Miyake S, Kim S, Suda W, Oshima K, Nakamura M, Matsuoka T, et al. Dysbiosis in the Gut Microbiota of Patients with Multiple Sclerosis, with a Striking Depletion of Species Belonging to Clostridia XIVa and IV Clusters. PLoS One. 2015;10(9):e0137429.
9. Chen J, Chia N, Kalari KR, Yao JZ, Novotna M, Paz Soldan MM, et al. Multiple sclerosis patients have a distinct gut microbiota compared to healthy controls. Sci Rep. 2016;6:28484.
10. Tankou SK, Regev K, Healy BC, Tjon E, Laghi L, Cox LM, et al. A probiotic modulates the microbiome and immunity in multiple sclerosis. Ann Neurol. 2018;83(6):1147-61.
11. Braniste V, Al-Asmakh M, Kowal C, Anuar F, Abbaspour A, Toth M, et al. The gut microbiota influences blood-brain barrier permeability in mice. Sci Transl Med. 2014;6(263):263ra158.
12. Erny D, Hrabe de Angelis AL, Jaitin D, Wieghofer P, Staszewski O, David E, et al. Host microbiota constantly control maturation and function of microglia in the CNS. Nat Neurosci. 2015;18(7):965-77.
13. Rothhammer V, Mascanfroni ID, Bunse L, Takenaka MC, Kenison JE, Mayo L, et al. Type I interferons and microbial metabolites of tryptophan modulate astrocyte activity and central nervous system inflammation via the aryl hydrocarbon receptor. Nat Med. 2016;22(6):586-97.
14. Hoban AE, Stilling RM, Ryan FJ, Shanahan F, Dinan TG, Claesson MJ, et al. Regulation of prefrontal cortex myelination by the microbiota. Transl Psychiatry. 2016;6:e774.
15. Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, 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(8):506-14.
16. Dwivedi M, Kumar P, Laddha NC, Kemp EH. Induction of regulatory T cells: A role for probiotics and prebiotics to suppress autoimmunity. Autoimmun Rev. 2016;15(4):379-92.
17. Boirivant M, Strober W. The mechanism of action of probiotics. Curr Opin Gastroenterol. 2007;23(6):679-92.
18. Consonni A, Cordiglieri C, Rinaldi E, Marolda R, Ravanelli I, Guidesi E, et al. Administration of bifidobacterium and lactobacillus strains modulates experimental myasthenia gravis and experimental encephalomyelitis in Lewis rats. Oncotarget. 2018;9(32):22269-87.
19. Hosoya T, Sakai F, Yamashita M, Shiozaki T, Endo T, Ukibe K, et al. Lactobacillus helveticus SBT2171 inhibits lymphocyte proliferation by regulation of the JNK signaling pathway. PLoS One. 2014;9(9):e108360.
20. Yamashita M, Matsumoto K, Endo T, Ukibe K, Hosoya T, Matsubara Y, et al. Preventive Effect of Lactobacillus helveticus SBT2171 on Collagen-Induced Arthritis in Mice. Front Microbiol. 2017;8:1159.
21. Mazmanian SK, Round JL, Kasper DL. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature. 2008;453(7195):620-5.
22. Dasgupta S, Erturk-Hasdemir D, Ochoa-Reparaz J, Reinecker HC, Kasper DL. Plasmacytoid dendritic cells mediate anti-inflammatory responses to a gut commensal molecule via both innate and adaptive mechanisms. Cell Host Microbe. 2014;15(4):413-23.
23. Dolpady J, Sorini C, Di Pietro C, Cosorich I, Ferrarese R, Saita D, et al. Oral Probiotic VSL#3 Prevents Autoimmune Diabetes by Modulating Microbiota and Promoting Indoleamine 2,3-Dioxygenase-Enriched Tolerogenic Intestinal Environment. J Diabetes Res. 2016;2016:7569431.
24. Lavasani S, Dzhambazov B, Nouri M, Fak F, Buske S, Molin G, et al. A novel probiotic mixture exerts a therapeutic effect on experimental autoimmune encephalomyelitis mediated by IL-10 producing regulatory T cells. PLoS One. 2010;5(2):e9009.
25. Kwon HK, Kim GC, Kim Y, Hwang W, Jash A, Sahoo A, et al. Amelioration of experimental autoimmune encephalomyelitis by probiotic mixture is mediated by a shift in T helper cell immune response. Clin Immunol. 2013;146(3):217-27.
26. Ezendam J, de Klerk A, Gremmer ER, van Loveren H. Effects of Bifidobacterium animalis administered during lactation on allergic and autoimmune responses in rodents. Clin Exp Immunol. 2008;154(3):424-31.
27. Takata K, Kinoshita M, Okuno T, Moriya M, Kohda T, Honorat JA, et al. The lactic acid bacterium Pediococcus acidilactici suppresses autoimmune encephalomyelitis by inducing IL-10-producing regulatory T cells. PLoS One. 2011;6(11):e27644.
28. Maassen CB, Claassen E. Strain-dependent effects of probiotic lactobacilli on EAE autoimmunity. Vaccine. 2008;26(17):2056-7.
29. Libbey JE, Sanchez JM, Doty DJ, Sim JT, Cusick MF, Cox JE, et al. Variations in diet cause alterations in microbiota and metabolites that follow changes in disease severity in a multiple sclerosis model. Benef Microbes. 2018;9(3):495-513.
30. Lavasani S, Dzhambazov B, Nouri M, Fåk F, Buske S, Molin G, et al. A novel probiotic mixture exerts a therapeutic effect on experimental autoimmune encephalomyelitis mediated by IL-10 producing regulatory T cells. PLoS One. 2010;5(2):e9009.
31. Berggren A, Lazou Ahrén I, Larsson N, Önning G. Randomised, double-blind and placebo-controlled study using new probiotic lactobacilli for strengthening the body immune defence against viral infections. Eur J Nutr. 2011;50(3):203-10.
32. Morshedi M, Hashemi R, Moazzen S, Sahebkar A, Hosseinifard ES. Immunomodulatory and anti-inflammatory effects of probiotics in multiple sclerosis: a systematic review. J Neuroinflammation. 2019;16(1):231.
33. Picca A, Fanelli F, Calvani R, Mule G, Pesce V, Sisto A, et al. Gut Dysbiosis and Muscle Aging: Searching for Novel Targets against Sarcopenia. Mediators Inflamm. 2018;2018:7026198.
34. Mielcarz DW, Kasper LH. The gut microbiome in multiple sclerosis. Curr Treat Options Neurol. 2015;17(4):344.
35. Littman DR, Pamer EG. Role of the commensal microbiota in normal and pathogenic host immune responses. Cell Host Microbe. 2011;10(4):311-23.
36. Renz H, Brandtzaeg P, Hornef M. The impact of perinatal immune development on mucosal homeostasis and chronic inflammation. Nat Rev Immunol. 2011;12(1):9-23.
37. Allin KH, Nielsen T, Pedersen O. Mechanisms in endocrinology: Gut microbiota in patients with type 2 diabetes mellitus. Eur J Endocrinol. 2015;172(4):R167-77.
38. Kau AL, Ahern PP, Griffin NW, Goodman AL, Gordon JI. Human nutrition, the gut microbiome and the immune system. Nature. 2011;474(7351):327-36.
39. Flint HJ, Scott KP, Duncan SH, Louis P, Forano E. Microbial degradation of complex carbohydrates in the gut. Gut Microbes. 2012;3(4):289-306.
40. de Oliveira GLV, Leite AZ, Higuchi BS, Gonzaga MI, Mariano VS. Intestinal dysbiosis and probiotic applications in autoimmune diseases. Immunology. 2017;152(1):1-12.
41. Jandhyala SM, Talukdar R, Subramanyam C, Vuyyuru H, Sasikala M, Nageshwar Reddy D. Role of the normal gut microbiota. World J Gastroenterol. 2015;21(29):8787-803.
42. van den Hoogen WJ, Laman JD, t Hart BA. Modulation of Multiple Sclerosis and Its Animal Model Experimental Autoimmune Encephalomyelitis by Food and Gut Microbiota. Front Immunol. 2017;8:1081.
43. LeBlanc JG, Milani C, de Giori GS, Sesma F, van Sinderen D, Ventura M. Bacteria as vitamin suppliers to their host: a gut microbiota perspective. Curr Opin Biotechnol. 2013;24(2):160-8.
44. Abou-Zeid AA, Shehata YM, el-Sherbeny R. Microbial production of cobalamin (vitamin B 12). Zentralbl Bakteriol Parasitenkd Infektionskr Hyg. 1973;128(3):285-96.
45. Pompei A, Cordisco L, Amaretti A, Zanoni S, Matteuzzi D, Rossi M. Folate production by bifidobacteria as a potential probiotic property. Appl Environ Microbiol. 2007;73(1):179-85.
46. Hill MJ. Intestinal flora and endogenous vitamin synthesis. Eur J Cancer Prev. 1997;6 Suppl 1:S43-5.
47. Chu F, Shi M, Lang Y, Shen D, Jin T, Zhu J, et al. Gut Microbiota in Multiple Sclerosis and Experimental Autoimmune Encephalomyelitis: Current Applications and Future Perspectives. Mediators Inflamm. 2018;2018:8168717.
48. Arpaia N, Campbell C, Fan X, Dikiy S, van der Veeken J, deRoos P, et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature. 2013;504(7480):451-5.
49. Kadowaki A, Miyake S, Saga R, Chiba A, Mochizuki H, Yamamura T. Gut environment-induced intraepithelial autoreactive CD4(+) T cells suppress central nervous system autoimmunity via LAG-3. Nat Commun. 2016;7:11639.
50. Cenit MC, Matzaraki V, Tigchelaar EF, Zhernakova A. Rapidly expanding knowledge on the role of the gut microbiome in health and disease. Biochim Biophys Acta. 2014;1842(10):1981-92.
51. Consortium EP, Birney E, Stamatoyannopoulos JA, Dutta A, Guigo R, Gingeras TR, et al. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature. 2007;447(7146):799-816.
52. Petrosino JF, Highlander S, Luna RA, Gibbs RA, Versalovic J. Metagenomic pyrosequencing and microbial identification. Clin Chem. 2009;55(5):856-66.
53. Berer K, Mues M, Koutrolos M, Rasbi ZA, Boziki M, Johner C, et al. Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination. Nature. 2011;479(7374):538-41.
54. Cantarel BL, Waubant E, Chehoud C, Kuczynski J, DeSantis TZ, Warrington J, et al. Gut microbiota in multiple sclerosis: possible influence of immunomodulators. J Investig Med. 2015;63(5):729-34.
55. Gill HS, Guarner F. Probiotics and human health: a clinical perspective. Postgrad Med J. 2004;80(947):516-26.
56. Tlaskalova-Hogenova H, Stepankova R, Hudcovic T, Tuckova L, Cukrowska B, Lodinova-Zadnikova R, et al. Commensal bacteria (normal microflora), mucosal immunity and chronic inflammatory and autoimmune diseases. Immunol Lett. 2004;93(2-3):97-108.
57. Salehipour Z, Haghmorad D, Sankian M, Rastin M, Nosratabadi R, Soltan Dallal MM, 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. Biomed Pharmacother. 2017;95:1535-48.
58. Shida K, Takahashi R, Iwadate E, Takamizawa K, Yasui H, Sato T, et al. Lactobacillus casei strain Shirota suppresses serum immunoglobulin E and immunoglobulin G1 responses and systemic anaphylaxis in a food allergy model. Clin Exp Allergy. 2002;32(4):563-70.
59. Sanchez JMS, Doty DJ, DePaula-Silva AB, Brown DG, Bell R, Klag KA, et al. Molecular patterns from a human gut-derived Lactobacillus strain suppress pathogenic infiltration of leukocytes into the central nervous system. J Neuroinflammation. 2020;17(1):291.
60. Grigoriadis N, van Pesch V, Paradig MSG. A basic overview of multiple sclerosis immunopathology. Eur J Neurol. 2015;(22 Suppl 2):3-13.
61. Dendrou CA, Fugger L, Friese MA. Immunopathology of multiple sclerosis. Nat Rev Immunol. 2015;15(9):545-58.
2. Ryu CH, Park KY, Hou Y, Jeong CH, Kim SM, Jeun SS. Gene therapy of multiple sclerosis using interferon beta-secreting human bone marrow mesenchymal stem cells. Biomed Res Int. 2013;2013:696738.
3. Cheng W, Chen G. Chemokines and chemokine receptors in multiple sclerosis. Mediators Inflamm. 2014;2014:659206.
4. Yamashita M, Ukibe K, Matsubara Y, Hosoya T, Sakai F, Kon S, et al. Lactobacillus helveticus SBT2171 Attenuates Experimental Autoimmune Encephalomyelitis in Mice. Front Microbiol. 2017;8:2596.
5. Ochoa-Reparaz J, Kasper LH. The influence of gut-derived CD39 regulatory T cells in CNS demyelinating disease. Transl Res. 2017;179:126-38.
6. Jangi S, Gandhi R, Cox LM, Li N, von Glehn F, Yan R, et al. Alterations of the human gut microbiome in multiple sclerosis. Nat Commun. 2016;7:12015.
7. Zhang X, Zhang D, Jia H, Feng Q, Wang D, Liang D, et al. The oral and gut microbiomes are perturbed in rheumatoid arthritis and partly normalized after treatment. Nat Med. 2015;21(8):895-905.
8. Miyake S, Kim S, Suda W, Oshima K, Nakamura M, Matsuoka T, et al. Dysbiosis in the Gut Microbiota of Patients with Multiple Sclerosis, with a Striking Depletion of Species Belonging to Clostridia XIVa and IV Clusters. PLoS One. 2015;10(9):e0137429.
9. Chen J, Chia N, Kalari KR, Yao JZ, Novotna M, Paz Soldan MM, et al. Multiple sclerosis patients have a distinct gut microbiota compared to healthy controls. Sci Rep. 2016;6:28484.
10. Tankou SK, Regev K, Healy BC, Tjon E, Laghi L, Cox LM, et al. A probiotic modulates the microbiome and immunity in multiple sclerosis. Ann Neurol. 2018;83(6):1147-61.
11. Braniste V, Al-Asmakh M, Kowal C, Anuar F, Abbaspour A, Toth M, et al. The gut microbiota influences blood-brain barrier permeability in mice. Sci Transl Med. 2014;6(263):263ra158.
12. Erny D, Hrabe de Angelis AL, Jaitin D, Wieghofer P, Staszewski O, David E, et al. Host microbiota constantly control maturation and function of microglia in the CNS. Nat Neurosci. 2015;18(7):965-77.
13. Rothhammer V, Mascanfroni ID, Bunse L, Takenaka MC, Kenison JE, Mayo L, et al. Type I interferons and microbial metabolites of tryptophan modulate astrocyte activity and central nervous system inflammation via the aryl hydrocarbon receptor. Nat Med. 2016;22(6):586-97.
14. Hoban AE, Stilling RM, Ryan FJ, Shanahan F, Dinan TG, Claesson MJ, et al. Regulation of prefrontal cortex myelination by the microbiota. Transl Psychiatry. 2016;6:e774.
15. Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, 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(8):506-14.
16. Dwivedi M, Kumar P, Laddha NC, Kemp EH. Induction of regulatory T cells: A role for probiotics and prebiotics to suppress autoimmunity. Autoimmun Rev. 2016;15(4):379-92.
17. Boirivant M, Strober W. The mechanism of action of probiotics. Curr Opin Gastroenterol. 2007;23(6):679-92.
18. Consonni A, Cordiglieri C, Rinaldi E, Marolda R, Ravanelli I, Guidesi E, et al. Administration of bifidobacterium and lactobacillus strains modulates experimental myasthenia gravis and experimental encephalomyelitis in Lewis rats. Oncotarget. 2018;9(32):22269-87.
19. Hosoya T, Sakai F, Yamashita M, Shiozaki T, Endo T, Ukibe K, et al. Lactobacillus helveticus SBT2171 inhibits lymphocyte proliferation by regulation of the JNK signaling pathway. PLoS One. 2014;9(9):e108360.
20. Yamashita M, Matsumoto K, Endo T, Ukibe K, Hosoya T, Matsubara Y, et al. Preventive Effect of Lactobacillus helveticus SBT2171 on Collagen-Induced Arthritis in Mice. Front Microbiol. 2017;8:1159.
21. Mazmanian SK, Round JL, Kasper DL. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature. 2008;453(7195):620-5.
22. Dasgupta S, Erturk-Hasdemir D, Ochoa-Reparaz J, Reinecker HC, Kasper DL. Plasmacytoid dendritic cells mediate anti-inflammatory responses to a gut commensal molecule via both innate and adaptive mechanisms. Cell Host Microbe. 2014;15(4):413-23.
23. Dolpady J, Sorini C, Di Pietro C, Cosorich I, Ferrarese R, Saita D, et al. Oral Probiotic VSL#3 Prevents Autoimmune Diabetes by Modulating Microbiota and Promoting Indoleamine 2,3-Dioxygenase-Enriched Tolerogenic Intestinal Environment. J Diabetes Res. 2016;2016:7569431.
24. Lavasani S, Dzhambazov B, Nouri M, Fak F, Buske S, Molin G, et al. A novel probiotic mixture exerts a therapeutic effect on experimental autoimmune encephalomyelitis mediated by IL-10 producing regulatory T cells. PLoS One. 2010;5(2):e9009.
25. Kwon HK, Kim GC, Kim Y, Hwang W, Jash A, Sahoo A, et al. Amelioration of experimental autoimmune encephalomyelitis by probiotic mixture is mediated by a shift in T helper cell immune response. Clin Immunol. 2013;146(3):217-27.
26. Ezendam J, de Klerk A, Gremmer ER, van Loveren H. Effects of Bifidobacterium animalis administered during lactation on allergic and autoimmune responses in rodents. Clin Exp Immunol. 2008;154(3):424-31.
27. Takata K, Kinoshita M, Okuno T, Moriya M, Kohda T, Honorat JA, et al. The lactic acid bacterium Pediococcus acidilactici suppresses autoimmune encephalomyelitis by inducing IL-10-producing regulatory T cells. PLoS One. 2011;6(11):e27644.
28. Maassen CB, Claassen E. Strain-dependent effects of probiotic lactobacilli on EAE autoimmunity. Vaccine. 2008;26(17):2056-7.
29. Libbey JE, Sanchez JM, Doty DJ, Sim JT, Cusick MF, Cox JE, et al. Variations in diet cause alterations in microbiota and metabolites that follow changes in disease severity in a multiple sclerosis model. Benef Microbes. 2018;9(3):495-513.
30. Lavasani S, Dzhambazov B, Nouri M, Fåk F, Buske S, Molin G, et al. A novel probiotic mixture exerts a therapeutic effect on experimental autoimmune encephalomyelitis mediated by IL-10 producing regulatory T cells. PLoS One. 2010;5(2):e9009.
31. Berggren A, Lazou Ahrén I, Larsson N, Önning G. Randomised, double-blind and placebo-controlled study using new probiotic lactobacilli for strengthening the body immune defence against viral infections. Eur J Nutr. 2011;50(3):203-10.
32. Morshedi M, Hashemi R, Moazzen S, Sahebkar A, Hosseinifard ES. Immunomodulatory and anti-inflammatory effects of probiotics in multiple sclerosis: a systematic review. J Neuroinflammation. 2019;16(1):231.
33. Picca A, Fanelli F, Calvani R, Mule G, Pesce V, Sisto A, et al. Gut Dysbiosis and Muscle Aging: Searching for Novel Targets against Sarcopenia. Mediators Inflamm. 2018;2018:7026198.
34. Mielcarz DW, Kasper LH. The gut microbiome in multiple sclerosis. Curr Treat Options Neurol. 2015;17(4):344.
35. Littman DR, Pamer EG. Role of the commensal microbiota in normal and pathogenic host immune responses. Cell Host Microbe. 2011;10(4):311-23.
36. Renz H, Brandtzaeg P, Hornef M. The impact of perinatal immune development on mucosal homeostasis and chronic inflammation. Nat Rev Immunol. 2011;12(1):9-23.
37. Allin KH, Nielsen T, Pedersen O. Mechanisms in endocrinology: Gut microbiota in patients with type 2 diabetes mellitus. Eur J Endocrinol. 2015;172(4):R167-77.
38. Kau AL, Ahern PP, Griffin NW, Goodman AL, Gordon JI. Human nutrition, the gut microbiome and the immune system. Nature. 2011;474(7351):327-36.
39. Flint HJ, Scott KP, Duncan SH, Louis P, Forano E. Microbial degradation of complex carbohydrates in the gut. Gut Microbes. 2012;3(4):289-306.
40. de Oliveira GLV, Leite AZ, Higuchi BS, Gonzaga MI, Mariano VS. Intestinal dysbiosis and probiotic applications in autoimmune diseases. Immunology. 2017;152(1):1-12.
41. Jandhyala SM, Talukdar R, Subramanyam C, Vuyyuru H, Sasikala M, Nageshwar Reddy D. Role of the normal gut microbiota. World J Gastroenterol. 2015;21(29):8787-803.
42. van den Hoogen WJ, Laman JD, t Hart BA. Modulation of Multiple Sclerosis and Its Animal Model Experimental Autoimmune Encephalomyelitis by Food and Gut Microbiota. Front Immunol. 2017;8:1081.
43. LeBlanc JG, Milani C, de Giori GS, Sesma F, van Sinderen D, Ventura M. Bacteria as vitamin suppliers to their host: a gut microbiota perspective. Curr Opin Biotechnol. 2013;24(2):160-8.
44. Abou-Zeid AA, Shehata YM, el-Sherbeny R. Microbial production of cobalamin (vitamin B 12). Zentralbl Bakteriol Parasitenkd Infektionskr Hyg. 1973;128(3):285-96.
45. Pompei A, Cordisco L, Amaretti A, Zanoni S, Matteuzzi D, Rossi M. Folate production by bifidobacteria as a potential probiotic property. Appl Environ Microbiol. 2007;73(1):179-85.
46. Hill MJ. Intestinal flora and endogenous vitamin synthesis. Eur J Cancer Prev. 1997;6 Suppl 1:S43-5.
47. Chu F, Shi M, Lang Y, Shen D, Jin T, Zhu J, et al. Gut Microbiota in Multiple Sclerosis and Experimental Autoimmune Encephalomyelitis: Current Applications and Future Perspectives. Mediators Inflamm. 2018;2018:8168717.
48. Arpaia N, Campbell C, Fan X, Dikiy S, van der Veeken J, deRoos P, et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature. 2013;504(7480):451-5.
49. Kadowaki A, Miyake S, Saga R, Chiba A, Mochizuki H, Yamamura T. Gut environment-induced intraepithelial autoreactive CD4(+) T cells suppress central nervous system autoimmunity via LAG-3. Nat Commun. 2016;7:11639.
50. Cenit MC, Matzaraki V, Tigchelaar EF, Zhernakova A. Rapidly expanding knowledge on the role of the gut microbiome in health and disease. Biochim Biophys Acta. 2014;1842(10):1981-92.
51. Consortium EP, Birney E, Stamatoyannopoulos JA, Dutta A, Guigo R, Gingeras TR, et al. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature. 2007;447(7146):799-816.
52. Petrosino JF, Highlander S, Luna RA, Gibbs RA, Versalovic J. Metagenomic pyrosequencing and microbial identification. Clin Chem. 2009;55(5):856-66.
53. Berer K, Mues M, Koutrolos M, Rasbi ZA, Boziki M, Johner C, et al. Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination. Nature. 2011;479(7374):538-41.
54. Cantarel BL, Waubant E, Chehoud C, Kuczynski J, DeSantis TZ, Warrington J, et al. Gut microbiota in multiple sclerosis: possible influence of immunomodulators. J Investig Med. 2015;63(5):729-34.
55. Gill HS, Guarner F. Probiotics and human health: a clinical perspective. Postgrad Med J. 2004;80(947):516-26.
56. Tlaskalova-Hogenova H, Stepankova R, Hudcovic T, Tuckova L, Cukrowska B, Lodinova-Zadnikova R, et al. Commensal bacteria (normal microflora), mucosal immunity and chronic inflammatory and autoimmune diseases. Immunol Lett. 2004;93(2-3):97-108.
57. Salehipour Z, Haghmorad D, Sankian M, Rastin M, Nosratabadi R, Soltan Dallal MM, 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. Biomed Pharmacother. 2017;95:1535-48.
58. Shida K, Takahashi R, Iwadate E, Takamizawa K, Yasui H, Sato T, et al. Lactobacillus casei strain Shirota suppresses serum immunoglobulin E and immunoglobulin G1 responses and systemic anaphylaxis in a food allergy model. Clin Exp Allergy. 2002;32(4):563-70.
59. Sanchez JMS, Doty DJ, DePaula-Silva AB, Brown DG, Bell R, Klag KA, et al. Molecular patterns from a human gut-derived Lactobacillus strain suppress pathogenic infiltration of leukocytes into the central nervous system. J Neuroinflammation. 2020;17(1):291.
60. Grigoriadis N, van Pesch V, Paradig MSG. A basic overview of multiple sclerosis immunopathology. Eur J Neurol. 2015;(22 Suppl 2):3-13.
61. Dendrou CA, Fugger L, Friese MA. Immunopathology of multiple sclerosis. Nat Rev Immunol. 2015;15(9):545-58.
| Files | ||
| Issue | Vol 22 No 1 (2023) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijaai.v22i1.12004 | |
| Keywords | ||
| Immunoregulation Lactobacillus paracasei Lactobacillus plantarum Multiple sclerosis Probiotics | ||
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How to Cite
1.
Chakamian K, Robat-Jazi B, Naser Moghadasi A, Mansouri F, Nodehi M, Motevaseli E, Izad M, Yekaninejad S, Shirzad M, Bidad K, Oraei M, Ansaripour B, Saboor-Yaraghi AA. Immunosuppressive Effects of Two Probiotics, Lactobacillus paracasei DSM 13434 and Lactobacillus plantarum DSM 15312, on CD4+ T Cells of Multiple Sclerosis Patients. Iran J Allergy Asthma Immunol. 2023;22(1):34-45.
