Preventive effect of Lactobacillus helveticus SBT2171 on collagen-induced arthritis in mice

Frontiers in Microbiology

Volumn 8, Issue JUN, 2017, Pages

  Yamashita, Maya ^a   Matsumoto, Kurumi ^a   Endo, Tsutomu ^b   Ukibe, Ken ^a   Hosoya, Tomohiro ^a   Matsubara, Yumi ^c   Nakagawa, Hisako ^c   Sakai, Fumihiko ^a   Miyazaki, Tadaaki ^c  

^a SNOW BRAND MILK PRODUCTS CO LTD   (Japan)

^b HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c HOKKAIDO UNIVERSITY   (Japan)

Author keywords

+Pro inflammatory cytokines; Autoantibody production; Collagen induced arthritis; Lactobacillus helveticus SBT2171; Rheumatoid arthritis

Indexed keywords

COLLAGEN TYPE 2; COLLAGEN TYPE 2 ANTIBODY; GAMMA INTERFERON; INTERLEUKIN 6; LACTOBACILLUS HELVETICUS SBT2171; NEW DRUG; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; COLLAGEN INDUCED ARTHRITIS; CONTROLLED STUDY; DOWN REGULATION; ENZYME LINKED IMMUNOSORBENT ASSAY; EXPERIMENTAL ARTHRITIS; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; GERMINAL CENTER; HISTOPATHOLOGY; IMMUNIZATION; JOINT SWELLING; LACTOBACILLUS HELVETICUS; LACTOBACILLUS HELVETICUS SBT2171; MALE; MOUSE; NONHUMAN; SCORING SYSTEM; STAINING; WEIGHT REDUCTION;

EID: 85021213600     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2017.01159     Document Type: Article

References (46)

1. Afzali, B., Lombardi, G., Lechler, R. I., and Lord, G. M. (2007). The role of T helper 17 (Th17) and regulatory T cells (Treg) in human organ transplantation and autoimmune disease. Clin. Exp. Immunol. 148, 32-46. doi: 10.1111/j.1365-2249.2007.03356.x
2. Akatsu, H., Iwabuchi, N., Xiao, J. Z., Matsuyama, Z., Kurihara, R., Okuda, K., et al. (2013). Clinical effects of probiotic Bifidobacterium longum BB536 on immune function and intestinal microbiota in elderly patients receiving enteral tube feeding. J. Parenter. Enteral Nutr. 37, 631-640. doi: 10.1177/0148607112467819
3. Amdekar, S., Singh, V., Singh, R., Sharma, P., Keshav, P., and Kumar, A. (2011). Lactobacillus casei reduces the inflammatory joint damage associated with collagen-induced arthritis (CIA) by reducing the pro-inflammatory cytokines-Lactobacillus casei: COX-2 inhibitor. J. Clin. Immunol. 31, 147-154. doi: 10.1007/s10875-010-9457-7
4. Billiau, A., and Matthys, P. (2011). Collagen-induced arthritis and related animal models: how much of their pathogenesis is auto-immune, how much is auto-inflammatory? Cytokine Growth Factor Rev. 22, 339-344. doi: 10.1016/j.cytogfr.2011.11.003
5. Choy, E., and Panayi, G. (2001). Cytokine pathways and joint inflammation in rheumatoid arthritis. N. Engl. J. Med. 344, 907-916. doi: 10.1056/NEJM200103223441207
6. Cohen, S. B., Emery, P., Greenwald, M. W., Dougados, M., Furie, R. A., Genovese, M. C., et al. (2006). Rituximab for rheumatoid arthritis refractory to anti-tumor necrosis factor therapy: results of a multicenter, randomized, double-blind, placebo-controlled, phase III trial evaluating primary efficacy and safety at twenty-four weeks. Arthritis Rheum. 54, 2793-2806. doi: 10.1002/art.22025
7. Edwards, J. C., Szczepanski, L., Szechinski, J., Filipowicz-Sosnowska, A., Emery, P., Close, D. R., et al. (2004). Efficacy of B-cell-targeted therapy with rituximab in patients with rheumatoid arthritis. N. Engl. J. Med. 350, 2572-2581. doi: 10.1056/NEJMoa032534
8. Endo, T., Ito, K., Morimoto, J., Kanayama, M., Ota, D., Ikesue, M., et al. (2015). Syndecan 4 regulation of the development of autoimmune arthritis in mice by modulating B cell migration and germinal center formation. Arthritis Rheumatol. 67, 2512-2522. doi: 10.1002/art.39193
9. Fujimoto, M., Serada, S., and Naka, T. (2008). Role of IL-6 in the development and pathogenesis of CIA and EAE. Nihon Rinsho Meneki Gakkai Kaishi 31, 78-84. doi: 10.2177/jsci.31.78
10. Griet, M., Zelaya, H., Mateos, M. V., Salva, S., Juarez, G. E., de Valdez, G. F., et al. (2014). Soluble factors from Lactobacillus reuteri CRL1098 have anti-inflammatory effects in acute lung injury induced by lipopolysaccharide in mice. PLoS ONE 9:e110027. doi: 10.1371/journal.pone.0110027
11. Hosoya, T., Sakai, F., Yamashita, M., Shiozaki, T., Endo, T., Ukibe, K., et al. (2014). Lactobacillus helveticus SBT2171 inhibits lymphocyte proliferation by regulation of the JNK signaling pathway. PLoS ONE 9:e108360. doi: 10.1371/journal.pone.0108360
12. Johansen, F. E., Pekna, M., Norderhaug, I. N., Haneberg, B., Hietala, M. A., Krajci, P., et al. (1999). Absence of epithelial immunoglobulin A transport, with increased mucosal leakiness, in polymeric immunoglobulin receptor/secretory component-deficient mice. J. Exp. Med. 190, 915-922. doi: 10.1084/jem.190.7.915
13. Kabak, B., and Dobson, A. D. (2011). An introduction to the traditional fermented foods and beverages of Turkey. Crit. Rev. Food Sci. Nutr. 51, 248-260. doi: 10.1080/10408390903569640
14. Kanayama, M., Morimoto, J., Matsui, Y., Ikesue, M., Danzaki, K., Kurotaki, D., et al. (2011). a9β1 integrin-mediated signaling serves as an intrinsic regulator of pathogenic Th17 cell generation. J. Immunol. 187, 5851-5864. doi: 10.4049/jimmunol.1101524
15. Kano, H., Mogami, O., and Uchida, M. (2003). Oral administration of milk fermented with Lactobacillus delbrueckii ssp. bulgaricus OLL1073R-1 to DBA/1 mice inhibits secretion of proinflammatory cytokines. Cytotechnology 40, 67-73. doi: 10.1023/A:1023966121989
16. Kato, I., Endo-Tanaka, K., and Yokokura, T. (1998). Suppressive effects of the oral administration of Lactobacillus casei on type II collagen-induced arthritis in DBA/1 mice. Life Sci. 63, 635-644. doi: 10.1016/S0024-3205(98)00315-4
17. Kim, J. E., Chae, C. S., Kim, G. C., Hwang, W., Hwang, J., Hwang, S. M., et al. (2015). Lactobacillus helveticus suppresses experimental rheumatoid arthritis by reducing inflammatory T cell responses. J. Funct. Foods 13, 350-362. doi: 10.1016/j.jff.2015.01.002
18. King, C., Tangye, S. G., and Mackay, C. R. (2008). T follicular helper (TFH) cells in normal and dysregulated immune responses. Annu. Rev. Immunol. 26, 741-766. doi: 10.1146/annurev.immunol.26.021607.090344
19. Koch, A. E. (2005). Chemokines and their receptors in rheumatoid arthritis: future targets? Arthritis Rheum. 52, 710-721. doi: 10.1002/art.20932
20. Leavenworth, J. W., Tang, X., Kim, H. J., Wang, X., and Cantor, H. (2013). Amelioration of arthritis through mobilization of peptide-specific CD8 + regulatory T cells. J. Clin. Invest. 123, 1382-1389. doi: 10.1172/JCI66938
21. Linterman, M. A., Rigby, R. J., Wong, R. K., Yu, D., Brink, R., Cannons, J. L., et al. (2009). Follicular helper T cells are required for systemic autoimmunity. J. Exp. Med. 206, 561-576. doi: 10.1084/jem.20081886
22. Mullazehi, M., Wick, M. C., Klareskog, L., van Vollenhoven, R., and Rönnelid, J. (2012). Anti-type II collagen antibodies are associated with early radiographic destruction in rheumatoid arthritis. Arthritis Res. Ther. 14, R100. doi: 10.1186/ar3825
23. Murooka, Y., and Yamshita, M. (2008). Traditional healthful fermented products of Japan. J. Ind. Microbiol. Biotechnol. 35, 791-798. doi: 10.1007/s10295-008-0362-5
24. Nakashima, Y., Kondo, M., Miyahara, H., and Iwamoto, Y. (2014). Drug delivery options to increase patient adherence and satisfaction in the management of rheumatoid arthritis-Focus on subcutaneous tocilizumab. Drug Des. Dev. Ther. 8, 913-919. doi: 10.2147/DDDT.S52099
25. Nakayama, Y., Moriya, T., Sakai, F., Ikeda, N., Shiozaki, T., Hosoya, T., et al. (2014). Oral administration of Lactobacillus gasseri SBT2055 is effective for preventing influenza in mice. Sci. Rep. 10:4638. doi: 10.1038/srep04638
26. Namba, K., Hatano, M., Yaeshima, T., Takase, M., and Suzuki, K. (2010). Effects of Bifidobacterium longum BB536 administration on influenza infection, influenza vaccine antibody titer, and cell-mediated immunity in the elderly. Biosci. Biotechnol. Biochem. 74, 939-945. doi: 10.1271/bbb.90749
27. Nandakumar, K. S., Andrén, M., Martinsson, P., Bajtner, E., Hellström, S., Holmdahl, R., et al. (2003). Induction of arthritis by single monoclonal IgG anti-collagen type II antibodies and enhancement of arthritis in mice lacking inhibitory FcγRIIB. Eur. J. Immunol. 33, 2269-2277. doi: 10.1002/eji.200323810
28. Novotny, N. I., Maldonado, G. C., Moreno, L. A., and Perdigon, G. (2015). Lactobacillus casei CRL 431 administration decreases inflammatory cytokines in a diet-induced obese mouse model. Nutrition 31, 1000-1007. doi: 10.1016/j.nut.2015.02.006
29. Parvez, S., Malik, K. A., Ah Kang, S., and Kim, H. Y. (2006). Probiotics and their fermented food products are beneficial for health. J. Appl. Microbiol. 100, 1171-1185. doi: 10.1111/j.1365-2672.2006.02963.x
30. Patole, P. S., Zecher, D., Pawar, R. D., Gröne, H. J., Schlöndorff, D., and Anders, H. J. (2005). G-rich DNA suppresses systemic lupus. J. Am. Soc. Nephrol. 16, 3273-3280. doi: 10.1681/ASN.2005060658
31. Sasaki, M., Bosman, B. W., and Tan, P. S. T. (1996). A new, broad-substrate-specificity aminopeptidase from the dairy organism Lactobacillus helveticus SBT 2171. Microbiology 142, 799-808. doi: 10.1099/00221287-142-4-799
32. Shandilya, U. K., Sharma, A., Kapila, R., and Kansal, V. K. (2016). Probiotic Dahi containing Lactobacillus acidophilus and Bifidobacterium bifidum modulates immunoglobulin levels and cytokines expression in whey proteins sensitised mice. J. Sci. Food Agric. 96, 3180-3187. doi: 10.1002/jsfa.7497
33. Simpson, N., Gatenby, P. A., Wilson, A., Malik, S., Fulcher, D. A., Tangye, S. G., et al. (2010). Expansion of circulating T cells resembling follicular helper T cells is a fixed phenotype that identifies a subset of severe systemic lupus erythematosus. Arthritis Rheum. 62, 234-244. doi: 10.1002/art.25032
34. So, J. S., Lee, C. G., Kwon, H. K., Yi, H. J., Chae, C. S., Park, J. A., et al. (2008). Lactobacillus casei potentiates induction of oral tolerance in experimental arthritis. Mol. Immunol. 46, 172-180. doi: 10.1016/j.molimm.2008.07.038
35. Stolk, M., Leon-Ponte, M., Merrill, M., Ahern, G. P., and O'Connell, P. J. (2006). IP3Rs are sufficient for dendritic cell Ca2+ signaling in the absence of RyR1. J. Leukoc. Biol. 80, 651-658. doi: 10.1189/jlb.1205739
36. Svensson, L., Jirholt, J., Holmdahl, R., and Jansson, L. (1998). B cell-deficient mice do not develop type II collagen-induced arthritis (CIA). Clin. Exp. Immunol. 111, 521-526. doi: 10.1046/j.1365-2249.1998.00529.x
37. Thorvaldson, L., Fuchs, D., Magnusson, S., and Kleinau, S. (2006). IgG immune complex-binding in macrophages from arthritis-susceptible and arthritis-resistant mice following collagen type II immunization. Scand. J. Immunol. 63, 347-354. doi: 10.1111/j.1365-3083.2006.01749.x
38. Vanderleyden, I., Linterman, M. A., and Smith, K. (2014). Regulatory T cells and control of the germinal centre response. Arthritis Res. Ther. 16, 471. doi: 10.1186/s13075-014-0471-7
39. Vinuesa, C. G., and Cyster, J. G. (2011). How T cells earn the follicular rite of passage. Immunity 35, 671-680. doi: 10.1016/j.immuni.2011.11.001
40. Vinuesa, C. G., Sanz, I., and Cook, M. C. (2009). Dysregulation of germinal centres in autoimmune disease. Nat. Rev. Immunol. 9, 845-857. doi: 10.1038/nri2637
41. Wang, Y., Liu, L., Moore, D. J., Shen, X., Peek, R. M., Acra, S. A., et al. (2016). An LGG-derived protein promotes IgA production through upregulation of APRIL expression in intestinal epithelial cells. Mucosal Immunol. 10, 373-384. doi: 10.1038/mi.2016.57
42. Wang, Y., Yamamoto, Y., Shigemori, S., Watanabe, T., Oshiro, K., Wang, X., et al. (2015). Inhibitory/suppressive oligodeoxynucleotide nanocapsules as simple oral delivery devices for preventing atopic dermatitis in mice. Mol. Ther. 23, 297-309. doi: 10.1038/mt.2014.239
43. Weyand, C. M., and Goronzy, J. J. (2003). Ectopic germinal center formation in rheumatoid synovitis. Ann. N. Y. Acad. Sci. 987, 140-149. doi: 10.1111/j.1749-6632.2003.tb06042.x
44. Yamamoto, K., Yokoyama, K., Matsukawa, T., Kato, S., Kato, S., Yamada, K., et al. (2016). Efficacy of prolonged ingestion of Lactobacillus acidophilus L-92 in adult patients with atopic dermatitis. J. Dairy Sci. 99, 5039-5046. doi: 10.3168/jds.2015-10605
45. Yamashita, M., Ukibe, K., Uenishi, H., Hosoya, T., Sakai, F., and Kadooka, Y. (2014). Lactobacillus helveticus SBT2171, a cheese starter, regulates proliferation and cytokine production of immune cells. J. Dairy Sci. 97, 4772-4779. doi: 10.3168/jds.2014-8041
46. Yanaba, K., Hamaguchi, Y., Venturi, G. M., Steeber, D. A., St Clair, E. W., Tedder, T. F., et al. (2007). B cell depletion delays collagen-induced arthritis in mice: arthritis induction requires synergy between humoral and cell-mediated immunity. J. Immunol. 179, 1369-1380. doi: 10.4049/jimmunol.179.2.1369