journal article Open Access Sep 29, 2024

Evaluation of Functional Components of Lactobacillus plantarum AR495 on Ovariectomy-Induced Osteoporosis in Mice And RAW264.7 Cells

Foods Vol. 13 No. 19 pp. 3115 · MDPI AG
View at Publisher Save 10.3390/foods13193115
Abstract
Osteoporosis is a disease characterized by abnormal bone metabolism, where bone resorption outpaces bone formation. In this study, we investigated the key functional components of Lactobacillus plantarum AR495 in mitigating ovariectomy (OVX)-induced osteoporosis in mice. The results indicated that both Lactobacillus plantarum AR495 and its fermentation broth significantly reduced urinary calcium and deoxypyridinoline (DPD) levels in the mice. These interventions inhibited bone resorption and improved trabecular bone architecture by modulating the nuclear factor κB (RANK)/RANK ligand (RANKL)/osteoprotegerin (OPG) signaling pathway. Additionally, the L. plantarum AR495 and fermentation broth groups inhibited the RANKL/TRAF-6 and TLR4/MYD88 pathways, leading to enhanced bone metabolism, improved intestinal barrier function, and reduced intestinal inflammation. In vitro experiments revealed that AR495 fermentation supernatant fractions larger than 100 kDa and those between 50–100 kDa significantly decreased the activity of the osteoclast marker TRAP, regulated the expression of the TLR4/MYD88 pathway, and inhibited osteoclast formation, thereby alleviating the OVX-induced osteoporosis phenotype. These findings suggest that these components may be primary functional elements of L. plantarum AR495 in the treatment of osteoporosis.
Topics

No keywords indexed for this article. Browse by subject →

References
42
[1]
Osteoclast differentiation and activation

William J. Boyle, W. Scott Simonet, David L. Lacey

Nature 2003 10.1038/nature01658
[2]
McDonald "Osteoclasts recycle via osteomorphs during RANKL-stimulated bone resorption" Cell (2021) 10.1016/j.cell.2021.03.010
[3]
Tilg "Gut, inflammation and osteoporosis: Basic and clinical concepts" Gut (2008) 10.1136/gut.2006.117382
[4]
Liu "Extracellular Vesicles from Child Gut Microbiota Enter into Bone to Preserve Bone Mass and Strength" Adv. Sci. (2021) 10.1002/advs.202004831
[5]
Rizzoli, R. (2010). Atlas of Postmenopausal Osteoporosis, Springer. 10.1007/978-1-907673-28-3
[6]
Park "Selective estrogen receptor modulators (SERMS) and their roles in breast cancer prevention" Trends Mol. Med. (2002) 10.1016/s1471-4914(02)02282-7
[7]
Vannala "Therapeutic Dimensions of Bisphosphonates: A Clinical Update" Int. J. Prev. Med. (2020) 10.4103/ijpvm.ijpvm_33_19
[8]
Deng "Bone-organ axes: Bidirectional crosstalk" Mil. Med. Res. (2024)
[9]
Agirman "Signaling inflammation across the gut-brain axis" Science (2021) 10.1126/science.abi6087
[10]
Reid "Potential uses of probiotics in clinical practice" Clin. Microbiol. Rev. (2003) 10.1128/cmr.16.4.658-672.2003
[11]
Konieczna "Bifidobacterium infantis 35624 administration induces Foxp3 T regulatory cells in human peripheral blood: Potential role for myeloid and plasmacytoid dendritic cells" Gut (2012) 10.1136/gutjnl-2011-300936
[12]
Shao "bsh1 Gene of Lactobacillus plantarum AR113 Plays an Important Role in Ameliorating Western Diet-Aggravated Colitis" J. Agric. Food Chem. (2023) 10.1021/acs.jafc.2c08631
[13]
Yeon "Fermented milk of Lactobacillus helveticus IDCC3801 reduces beta-amyloid and attenuates memory deficit" J. Funct. Foods (2010) 10.1016/j.jff.2010.04.002
[14]
Intestinal mucosal adherence and translocation of commensal bacteria at the early onset of type 2 diabetes: molecular mechanisms and probiotic treatment

Jacques Amar, Chantal Chabo, Aurélie Waget et al.

EMBO Molecular Medicine 2011 10.1002/emmm.201100159
[15]
Parvaneh, K., Ebrahimi, M., Sabran, M.R., Karimi, G., Hwei, A.N., Abdul-Majeed, S., Ahmad, Z., Ibrahim, Z., and Jamaluddin, R. (2015). Probiotics (Bifidobacterium longum) Increase Bone Mass Density and Upregulate Sparc and Bmp-2 Genes in Rats with Bone Loss Resulting from Ovariectomy. BioMed Res. Int., 2015. 10.1155/2015/897639
[16]
Britton "Probiotic L. reuteri treatment prevents bone loss in a menopausal ovariectomized mouse model" J. Cell. Physiol. (2014) 10.1002/jcp.24636
[17]
Ohlsson, C., Engdahl, C., Fåk, F., Andersson, A., Windahl, S.H., Farman, H.H., Movérare-Skrtic, S., Islander, U., and Sjögren, K. (2014). Probiotics protect mice from ovariectomy-induced cortical bone loss. PLoS ONE, 9. 10.1371/journal.pone.0092368
[18]
Li, P., Ji, B., Luo, H., Sundh, D., Lorentzon, M., and Nielsen, J. (2022). One-year supplementation with Lactobacillus reuteri ATCC PTA 6475 counteracts a degradation of gut microbiota in older women with low bone mineral density. NPJ Biofilms Microbiomes, 8. 10.1038/s41522-022-00348-2
[19]
Dar "Lactobacillus acidophilus inhibits bone loss and increases bone heterogeneity in osteoporotic mice via modulating Treg-Th17 cell balance" Bone Rep. (2018) 10.1016/j.bonr.2018.02.001
[20]
Sanz "Probiotics as drugs against human gastrointestinal infections" Recent Pat. Anti Infect. Drug Discov. (2007) 10.2174/157489107780832596
[21]
Depommier "Supplementation with Akkermansia muciniphila in overweight and obese human volunteers: A proof-of-concept exploratory study" Nat. Med. (2019) 10.1038/s41591-019-0495-2
[22]
He, X., Zeng, Q., Puthiyakunnon, S., Zeng, Z., Yang, W., Qiu, J., Du, L., Boddu, S., Wu, T., and Cai, D. (2017). Lactobacillus rhamnosus GG supernatant enhance neonatal resistance to systemic Escherichia coli K1 infection by accelerating development of intestinal defense. Sci. Rep., 7. 10.1038/srep43305
[23]
Yu "Anti-osteoporotic potential of Lactobacillus plantarum AR237 and AR495 in ovariectomized mice" J. Funct. Foods (2021) 10.1016/j.jff.2021.104762
[24]
Sakka "Management of primary and secondary osteoporosis in children" Ther. Adv. Musculoskelet. Dis. (2020) 10.1177/1759720x20969262
[25]
Riggs "Changes in bone mineral density of the proximal femur and spine with aging: Differences between the postmenopausal and senile osteoporosis syndromes" J. Clin. Investig. (1982) 10.1172/jci110667
[26]
Soriano "Current and future treatments of secondary osteoporosis" Best Pract. Res. Clin. Endocrinol. Metab. (2014) 10.1016/j.beem.2014.09.004
[27]
Arron "Bone versus immune system" Nature (2000) 10.1038/35046196
[28]
Sato "Th17 functions as an osteoclastogenic helper T cell subset that links T cell activation and bone destruction" J. Exp. Med. (2006) 10.1084/jem.20061775
[29]
The impact of the gut microbiota on the reproductive and metabolic endocrine system

Xinyu Qi, Chuyu Yun, Yanli Pang et al.

Gut Microbes 2021 10.1080/19490976.2021.1894070
[30]
Wang, J.J., Wang, J., Pang, X.Y., Zhao, L.P., Tian, L., and Wang, X.P. (2016). Sex differences in colonization of gut microbiota from a man with short-term vegetarian and inulin-supplemented diet in germ-free mice. Sci. Rep., 6. 10.1038/srep36137
[32]
Du "BRD9-mediated chromatin remodeling suppresses osteoclastogenesis through negative feedback mechanism" Nat. Commun. (2023) 10.1038/s41467-023-37116-5
[33]
Boyce "Functions of RANKL/RANK/OPG in bone modeling and remodeling" Arch. Biochem. Biophys. (2008) 10.1016/j.abb.2008.03.018
[34]
Armstrong "A RANK/TRAF6-dependent signal transduction pathway is essential for osteoclast cytoskeletal organization and resorptive function" J. Biol. Chem. (2002) 10.1074/jbc.m202009200
[35]
Zupan, J., Komadina, R., and Marc, J. (2012). The relationship between osteoclastogenic and anti-osteoclastogenic pro-inflammatory cytokines differs in human osteoporotic and osteoarthritic bone tissues. J. Biomed. Sci., 19. 10.1186/1423-0127-19-28
[36]
Wei "IL-1 mediates TNF-induced osteoclastogenesis" J. Clin. Investig. (2005) 10.1172/jci200523394
[37]
Shanmugarajan "NIP45 negatively regulates RANK ligand induced osteoclast differentiation" J. Cell. Biochem. (2012) 10.1002/jcb.23460
[38]
Mao "Exogenous administration of PACAP alleviates traumatic brain injury in rats through a mechanism involving the TLR4/MyD88/NF-κB pathway" J. Neurotrauma (2012) 10.1089/neu.2011.2244
[39]
Yang "Fuzhuan Brick Tea Polysaccharide Improved Ulcerative Colitis in Association with Gut Microbiota-Derived Tryptophan Metabolism" J. Agric. Food Chem. (2021) 10.1021/acs.jafc.1c02774
[40]
Ren "A review: The mechanism of plant-derived polysaccharides on osteoblasts and osteoclasts" J. Future Foods (2024) 10.1016/j.jfutfo.2023.07.001
[41]
Lucas "Short-chain fatty acids regulate systemic bone mass and protect from pathological bone loss" Nat. Commun. (2018) 10.1038/s41467-017-02490-4
[42]
Xu "Proteome-wide profiling reveals dysregulated molecular features and accelerated aging in osteoporosis: A 9.8-year prospective study" Aging Cell (2024) 10.1111/acel.14035
Metrics
3
Citations
42
References
Details
Published
Sep 29, 2024
Vol/Issue
13(19)
Pages
3115
License
View
Authors
Funding
National Key R&D Program of China Award: 2022-02-08-00-12-F01102
Shanghai Engineering Research Center of food microbiology program Award: 2022-02-08-00-12-F01102
Project of Shanghai for agriculture advance by science and technology Award: 2022-02-08-00-12-F01102
Cite This Article
Zheng Chen, Junlin Shao, Yijin Yang, et al. (2024). Evaluation of Functional Components of Lactobacillus plantarum AR495 on Ovariectomy-Induced Osteoporosis in Mice And RAW264.7 Cells. Foods, 13(19), 3115. https://doi.org/10.3390/foods13193115
Related

You May Also Like