Skip to main content
SpringerLink
Log in

Anti-inflammatory and Anti-osteoporotic Potential of Lactobacillus plantarum A41 and L. fermentum SRK414 as Probiotics

  • Published:
Probiotics and Antimicrobial Proteins Aims and scope Submit manuscript

Abstract

This study involves an investigation on the probiotic properties of lactic acid bacteria and their potential applications in an in vitro model of lipopolysaccharide (LPS)-stimulated inflammation and dexamethasone-induced osteoporosis. Nine strains were pre-screened from 485 lactic acid bacteria based on their survival at a low pH and in a solution containing bile salts. All candidates were capable of surviving in an environment with low pH and with bile salts and could successfully colonize the intestine. Furthermore, their functional properties, such as anti-oxidation and anti-inflammation, were evaluated. Of the nine probiotic candidates, Lactobacillus plantarum A41 and L. fermentum SRK414 exhibited the highest anti-oxidative capacity. Moreover, only L. plantarum A41 and L. fermentum SRK414 could increase gut barrier function by upregulating the mRNA expression of tight junction proteins and inhibit the expression of inflammatory mediators induced by LPS-stimulated inflammation. Interestingly, these two strains were also capable of regulating several bone metabolism-related markers playing a role in bone homeostasis and osteoblast differentiation. In brief, L. plantarum A41 and L. fermentum SRK414 exhibited high probiotic potential and potentially impact immune-related bone health by modulating pro-inflammatory cytokines and bone metabolism-related markers.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Teneva D, Denkova R, Goranov B, Denkova Z, Kostov G (2017) Antimicrobial activity of Lactobacillus plantarum strains against Salmonella pathogens. Ukr Food J 6(1):125–133. https://doi.org/10.24263/2304-974X-2017-6-1-14

    Article  CAS  Google Scholar 

  2. Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S, Calder PC, Sanders ME (2014) The International Scientific Assocication for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol 11(8):506–514. https://doi.org/10.1038/nrgastro.2014.66

    Article  PubMed  Google Scholar 

  3. Tyagi AM, Yu M, Darby TM, Vaccaro C, Li J-Y, Owens JA, Hsu E, Adams J, Weitzmann MN, Jones RM (2018) The microbial metabolite butyrate stimulates bone formation via T regulatory cell-mediated regulation of WNT10B expression. Immunity 49:1116–1131. https://doi.org/10.1016/j.immuni.2018.10.013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Shokryazdan P, Sieo CC, Kalavathy R, Liang JB, Alitheen NB, Faseleh Jahromi M, Ho YW (2014) Probiotic potential of Lactobacillus strains with antimicrobial activity against some human pathogenic strains. Biomed Res Int 2014:927268–927216. https://doi.org/10.1155/2014/927268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Kang J-H, Yun S-I, Park M-H, Park J-H, Jeong S-Y, Park H-O (2013) Anti-obesity effect of Lactobacillus gasseri BNR17 in high-sucrose diet-induced obese mice. PLoS One 8(1):e54617. https://doi.org/10.1371/journal.pone.0054617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Bron PA, Van Baarlen P, Kleerebezem M (2012) Emerging molecular insights into the interaction between probiotics and the host intestinal mucosa. Nat Rev Microbiol 10(1):66–78. https://doi.org/10.1038/nrmicro2690

    Article  CAS  Google Scholar 

  7. Ohlsson C, Sjögren K (2015) Effects of the gut microbiota on bone mass. Trends Endocrinol Metab 26(2):69–74. https://doi.org/10.1016/j.tem.2014.11.004

    Article  CAS  PubMed  Google Scholar 

  8. Lim JH, Yoon SM, Tan PL, Yang S, Kim SH, Park HJ (2018) Probiotic properties of Lactobacillus plantarum LRCC5193, a plant-origin lactic acid bacterium isolated from kimchi and its use in chocolates. J Food Sci 83(11):2802–2811. https://doi.org/10.1111/1750-3841.14364

    Article  CAS  PubMed  Google Scholar 

  9. Bao Y, Zhang Y, Zhang Y, Liu Y, Wang S, Dong X, Wang Y, Zhang H (2010) Screening of potential probiotic properties of Lactobacillus fermentum isolated from traditional dairy products. Food Control 21(5):695–701. https://doi.org/10.1016/j.foodcont.2009.10.010

    Article  CAS  Google Scholar 

  10. Hemraj V, Diksha S, Avneet G (2013) A review on commonly used biochemical test for bacteria. Innovare J Life Sci 1(1):1–7

    Google Scholar 

  11. Sorokulova IB, Pinchuk IV, Denayrolles M, Osipova IG, Huang JM, Cutting SM, Urdaci MC (2008) The safety of two Bacillus probiotic strains for human use. Dig Dis Sci 53:954–963. https://doi.org/10.1007/s10620-007-9959-1

    Article  PubMed  Google Scholar 

  12. Toba T, Yoshioka E, Itoh T (1991) Potential of Lactobacillus gasseri isolated from infant faeces to produce bacteriocin. Lett Appl Microbiol 12(6):228–231. https://doi.org/10.1111/j.1472-765X.1991.tb00546.x

    Article  Google Scholar 

  13. Verdenelli MC, Ghelfi F, Silvi S, Orpianesi C, Cecchini C, Cresci A (2009) Probiotic properties of Lactobacillus rhamnosus and Lactobacillus paracasei isolated from human faeces. Eur J Nutr 48(6):355–363. https://doi.org/10.1007/s00394-009-0021-2

    Article  PubMed  Google Scholar 

  14. Salminen MK, Tynkkynen S, Rautelin H, Saxelin M, Vaara M, Ruutu P, Sarna S, Valtonen V, Järvinen A (2002) Lactobacillus bacteremia during a rapid increase in probiotic use of Lactobacillus rhamnosus GG in Finland. Clin Infect Dis 35(10):1155–1160. https://doi.org/10.1086/342912

    Article  PubMed  Google Scholar 

  15. Varankovich NV, Nickerson MT, Korber DR (2015) Probiotic-based strategies for therapeutic and prophylactic use against multiple gastrointestinal diseases. Front Microbiol 6:685. https://doi.org/10.3389/fmicb.2015.00685

    Article  PubMed  PubMed Central  Google Scholar 

  16. Collins FL, Rios-Arce ND, Schepper JD, Parameswaran N, McCabe LR (2017) The potential of probiotics as a therapy for osteoporosis. Microbiol spectr 5(4). https://doi.org/10.1128/microbiolspec.BAD-0015-2016

  17. Jacobsen CN, Nielsen VR, Hayford A, Møller PL, Michaelsen K, Paerregaard A, Sandström B, Tvede M, Jakobsen M (1999) Screening of probiotic activities of forty-seven strains of Lactobacillus spp. by in vitro techniques and evaluation of the colonization ability of five selected strains in humans. Appl Environ Microbiol 65(11):4949–4956

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Kim S-J, Cho SY, Kim SH, Song O-J, Shin I-S, Cha DS, Park HJ (2008) Effect of microencapsulation on viability and other characteristics in Lactobacillus acidophilus ATCC 43121. LWT - Food Sci Technol 41(3):493–500. https://doi.org/10.1016/j.lwt.2007.03.025

    Article  CAS  Google Scholar 

  19. Afify AE-MM, Romeilah RM, Sultan SI, Hussein MM (2012) Antioxidant activity and biological evaluations of probiotic bacteria strains. Int J Acad Res 4(6):131–139. https://doi.org/10.7813/2075-4124.2012/4-6/A.18

    Article  Google Scholar 

  20. David-Raoudi M, Deschrevel B, Leclercq S, Galéra P, Boumediene K, Pujol JP (2009) Chondroitin sulfate increases hyaluronan production by human synoviocytes through differential regulation of hyaluronan synthases: role of p38 and Akt. Arthritis & Rheum 60(3):760–770. https://doi.org/10.1002/art.24302

    Article  CAS  Google Scholar 

  21. Bhattacharyya S, Kelley K, Melichian DS, Tamaki Z, Fang F, Su Y, Feng G, Pope RM, Budinger GS, Mutlu GM (2013) Toll-like receptor 4 signaling augments transforming growth factor-β responses: a novel mechanism for maintaining and amplifying fibrosis in scleroderma. Am J Pathol 182(1):192–205. https://doi.org/10.1016/j.ajpath.2012.09.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Li H, Sze S, Tong Y, Ng T (2009) Production of Th1-and Th2-dependent cytokines induced by the Chinese medicine herb, Rhodiola algida, on human peripheral blood monocytes. J Ethnopharmacol 123(2):257–266. https://doi.org/10.1016/j.jep.2009.03.009

    Article  CAS  PubMed  Google Scholar 

  23. Jiang YJ, Teichert AE, Fong F, Oda Y, Bikle DD (2013) 1α, 25 (OH) 2-Dihydroxyvitamin D3/VDR protects the skin from UVB-induced tumor formation by interacting with the β-catenin pathway. J Steroid Biochem Mol Biol 136:229–232. https://doi.org/10.1016/j.jsbmb.2012.09.024

    Article  CAS  PubMed  Google Scholar 

  24. Jian Y, Chen C, Li B, Tian X (2015) Delocalized Claudin-1 promotes metastasis of human osteosarcoma cells. Biochem Biophys Res Commun 466(3):356–361. https://doi.org/10.1016/j.bbrc.2015.09.028

    Article  CAS  PubMed  Google Scholar 

  25. Song X, Liu S, Qu X, Hu Y, Zhang X, Wang T, Wei F (2011) BMP2 and VEGF promote angiogenesis but retard terminal differentiation of osteoblasts in bone regeneration by up-regulating Id1. Acta Biochim Biophys Sin 43(10):796–804. https://doi.org/10.1093/abbs/gmr074

    Article  CAS  PubMed  Google Scholar 

  26. Ding S, Abudupataer M, Zhou Z, Chen J, Li H, Xu L, Zhang W, Zhang S, Zou Y, Hong T (2018) Histamine deficiency aggravates cardiac injury through miR-206/216b-Atg13 axis-mediated autophagic-dependant apoptosis. Cell Death Dis 9(6):694. https://doi.org/10.1038/s41419-018-0723-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Yang B, Lin X, Yang C, Tan J, Li W, Kuang H (2015) Sambucus Williamsii Hance promotes MC3T3-E1 cells proliferation and differentiation via BMP-2/Smad/p38/JNK/Runx2 signaling pathway. Phytother Res 29(11):1692–1699. https://doi.org/10.1002/ptr.5482

    Article  CAS  PubMed  Google Scholar 

  28. Chiang S-S, Pan T-M (2013) Beneficial effects of phytoestrogens and their metabolites produced by intestinal microflora on bone health. Appl Microbiol Biotechnol 97(4):1489–1500. https://doi.org/10.1007/s00253-012-4675-y

    Article  CAS  PubMed  Google Scholar 

  29. Zou D, Zhang Z, He J, Zhu S, Wang S, Zhang W, Zhou J, Xu Y, Huang Y, Wang Y, Han W, Zhou Y, Wang S, You S, Jiang X, Huang Y (2011) Repairing critical-sized calvarial defects with BMSCs modified by a constitutively active form of hypoxia-inducible factor-1alpha and a phosphate cement scaffold. Biomaterials 32(36):9707–9718. https://doi.org/10.1016/j.biomaterials.2011.09.005

    Article  CAS  PubMed  Google Scholar 

  30. Zhou J, Chen S, Guo H, Xia L, Liu H, Qin Y, He C (2013) Pulsed electromagnetic field stimulates osteoprotegerin and reduces RANKL expression in ovariectomized rats. Rheumatol Int 33(5):1135–1141. https://doi.org/10.1007/s00296-012-2499-9

    Article  CAS  PubMed  Google Scholar 

  31. Ramirez-Chavarin M, Wacher C, Eslava-Campos C, Perez-Chabela M (2013) Probiotic potential of thermotolerant lactic acid bacteria strains isolated from cooked meat products. Int Food Res J 20(2):991–1000

    CAS  Google Scholar 

  32. Dencova R, Donka D, Denkova Z (2012) Probiotic properties of Lactobacillus acidophilus A2 of human origin. Modern technologies, in the food industry

  33. Argyri AA, Zoumpopoulou G, Karatzas K-AG, Tsakalidou E, Nychas G-JE, Panagou EZ, Tassou CC (2013) Selection of potential probiotic lactic acid bacteria from fermented olives by in vitro tests. Food Microbiol 33(2):282–291. https://doi.org/10.1016/j.fm.2012.10.005

    Article  CAS  PubMed  Google Scholar 

  34. Tannock GW, Dashkevicz MP, Feighner SD (1989) Lactobacilli and bile salt hydrolase in the murine intestinal tract. Appl Environ Microbiol 55(7):1848–1851

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Guo C-F, Zhang S, Yuan Y-H, Yue T-L, Li J-Y (2015) Comparison of lactobacilli isolated from Chinese suan-tsai and koumiss for their probiotic and functional properties. J Funct Foods 12:294–302. https://doi.org/10.1016/j.jff.2014.11.029

    Article  CAS  Google Scholar 

  36. Mishra V, Shah C, Mokashe N, Chavan R, Yadav H, Prajapati J (2015) Probiotics as potential antioxidants: a systematic review. J Agric Food Chem 63(14):3615–3626. https://doi.org/10.1021/jf506326t

    Article  CAS  PubMed  Google Scholar 

  37. Kim H, Jeong S, Ham J, Chae H, Lee J, Ahn C (2006) Antioxidative and probiotic properties of Lactobacillus gasseri NLRI-312 isolated from Korean infant feces. Asina-Aust J Anim Sci 19(9):1335–1341. https://doi.org/10.5713/ajas.2006.1335

    Article  CAS  Google Scholar 

  38. Philippe D, Favre L, Foata F, Adolfsson O, Perruisseau-Carrier G, Vidal K, Reuteler G, Dayer-Schneider J, Mueller C, Blum S (2011) Bifidobacterium lactis attenuates onset of inflammation in a murine model of colitis. World J Gastroenterol 17(4):459–469. https://doi.org/10.3748/wjg.v17.i4.459

    Article  PubMed  PubMed Central  Google Scholar 

  39. Matsumoto S, Hara T, Hori T, Mitsuyama K, Nagaoka M, Tomiyasu N, Suzuki A, Sata M (2005) Probiotic Lactobacillus-induced improvement in murine chronic inflammatory bowel disease is associated with the down-regulation of pro-inflammatory cytokines in lamina propria mononuclear cells. Clin Exp Immunol 140(3):417–426. https://doi.org/10.1111/j.1365-2249.2005.02790.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Ohlsson C, Engdahl C, Fåk F, Andersson A, Windahl SH, Farman HH, Movérare-Skrtic S, Islander U, Sjögren K (2014) Probiotics protect mice from ovariectomy-induced cortical bone loss. PLoS One 9(3):e92368. https://doi.org/10.1371/journal.pone.0092368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Lam J, Takeshita S, Barker JE, Kanagawa O, Ross FP, Teitelbaum SL (2000) TNF-α induces osteoclastogenesis by direct stimulation of macrophages exposed to permissive levels of RANK ligand. J Clin Invest 106(12):1481–1488. https://doi.org/10.1172/JCI11176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Wei S, Kitaura H, Zhou P, Ross FP, Teitelbaum SL (2005) IL-1 mediates TNF-induced osteoclastogenesis. J Clin Invest 115(2):282–290. https://doi.org/10.1172/JCI23394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Fanning AS, Ma TY, Anderson JM (2002) Isolation and functional characterization of the actin binding region in the tight junction protein ZO-1. FASEB J 16(13):1835–1837. https://doi.org/10.1096/fj.02-0121fje

    Article  CAS  PubMed  Google Scholar 

  44. Karczewski J, Troost FJ, Konings I, Dekker J, Kleerebezem M, Brummer R-JM, Wells JM (2010) Regulation of human epithelial tight junction proteins by Lactobacillus plantarum in vivo and protective effects on the epithelial barrier. Am J Physiol Gastrointest Liver Physiol 298(6):G851–G859. https://doi.org/10.1152/ajpgi.00327.2009

    Article  CAS  PubMed  Google Scholar 

  45. Yang F, Wang A, Zeng X, Hou C, Liu H, Qiao S (2015) Lactobacillus reuteri I5007 modulates tight junction protein expression in IPEC-J2 cells with LPS stimulation and in newborn piglets under normal conditions. BMC Microbiol 15(1):32. https://doi.org/10.1186/s12866-015-0372-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Collins FL, Kim SM, McCabe LR, Weaver CM (2017) Intestinal microbiota and bone health: the role of prebiotics, probiotics, and diet. In: Smith SY, Varela A, Samadfam R (eds) Bone toxicology. Springer, Arkansas, pp 417–443

    Chapter  Google Scholar 

  47. Lee NK, Sowa H, Hinoi E, Ferron M, Ahn JD, Confavreux C, Dacquin R, Mee PJ, McKee MD, Jung DY (2007) Endocrine regulation of energy metabolism by the skeleton. Cell 130(3):456–469. https://doi.org/10.1016/j.cell.2007.05.047

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Hessle L, Johnson KA, Anderson HC, Narisawa S, Sali A, Goding JW, Terkeltaub R, Millán JL (2002) Tissue-nonspecific alkaline phosphatase and plasma cell membrane glycoprotein-1 are central antagonistic regulators of bone mineralization. Proc Natl Acad Sci U S A 99(14):9445–9449. https://doi.org/10.1073/pnas.142063399

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Holm E, Aubin JE, Hunter GK, Beier F, Goldberg HA (2015) Loss of bone sialoprotein leads to impaired endochondral bone development and mineralization. Bone 71:145–154. https://doi.org/10.1016/j.bone.2014.10.007

    Article  CAS  PubMed  Google Scholar 

  50. Huang R, Yuan Y, Tu J, Zou G, Li Q (2014) Opposing TNF-α/IL-1β-and BMP-2-activated MAPK signaling pathways converge on Runx2 to regulate BMP-2-induced osteoblastic differentiation. Cell Death Dis 5(4):e1187. https://doi.org/10.1038/cddis.2014.101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Parvaneh M, Karimi G, Jamaluddin R, Ng MH, Zuriati I, Muhammad SI (2018) Lactobacillus helveticus (ATCC 27558) upregulates Runx2 and Bmp2 and modulates bone mineral density in ovariectomy-induced bone loss rats. Clin Interv Aging 13:1555–1564. https://doi.org/10.2147/CIA.S169223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work was supported by the High Value-Added Food Technology Development Program of the Korea Institute of Planning and Evaluation for Technology in Food, Agriculture, Forestry and Fisheries (iPET), and the Ministry for Food, Agriculture, Forestry and Fisheries of Republic of Korea (117051-03-1-HD020) and Korea University.

Author information

Authors and Affiliations

  1. College of Life Sciences and Biotechnology, Korea University, Seoul, 02841, Republic of Korea

    Chul Sang Lee & Sae Hun Kim

  2. Institute of Life Science and Natural Resources, Korea University, Seoul, 02841, Republic of Korea

    Chul Sang Lee & Sae Hun Kim

Authors
  1. Chul Sang Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sae Hun Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sae Hun Kim.

Ethics declarations

This article does not contain any studies with human or animal subjects.

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lee, C.S., Kim, S.H. Anti-inflammatory and Anti-osteoporotic Potential of Lactobacillus plantarum A41 and L. fermentum SRK414 as Probiotics. Probiotics & Antimicro. Prot. 12, 623–634 (2020). https://doi.org/10.1007/s12602-019-09577-y

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12602-019-09577-y

Keywords

Search

Navigation