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Open Access

A wheat germ-rich diet preserves bone homeostasis by regulating gut microbiota and plasma metabolites in aged rats

Luanfeng Wanga, Zebin Wengb, Tong Chena, Yu Lia, Ling Xionga, Haizhao Songa, Fang Wanga( ), Xiaozhi Tanga, Bo Renc, Xuebo Liud, Xinchun Shena( )
College of Food Science and Engineering, Nanjing University of Finance and Economics/Collaborative Innovation Center for Modern Grain Circulation and Safety, Nanjing 210023, China
School of Traditional Chinese Medicine & School of Integrated Chinese and Western Medicine, Nanjing University of Chinese Medicine, Nanjing 210023, China
School of Food Science and Pharmaceutical Engineering, Nanjing Normal University, Nanjing 210023, China
College of Food Science and Engineering, Northwest A&F University, Yangling 712100, China

Peer review under responsibility of Tsinghua University Press.

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Highlights

• A wheat germ (WG)-rich diet effectively attenuated ageing-induced microstructural damage and differentiation activity changes in the femur.

• The WG-rich diet improved ageing-related oxidation state imbalance and inflammatory response.

• The WG-rich diet enhanced SCFAs-producing microbes and reduced inflammation-related microbes.

• The WG-rich diet ameliorated plasma metabolites related to bone homeostasis.

Graphical Abstract

Abstract

Bone loss caused by ageing has become one of the leading health risk factors worldwide. Wheat germ (WG) is consists of high amounts of bioactive peptides, polyunsaturated fatty acids, and dietary fibre. Currently, WG has been proven to possess strong antioxidant and anti-inflammatory properties. We recently explored the beneficial effects and relevant mechanisms of a WG-rich diet (2.5% and 5% WG, m/m) on bone homeostasis in aged rats. Our results showed that 5% WG supplementation for 12 months effectively attenuated ageing-induced microstructural damage and differentiation activity changes in the femur. The 5% WG supplementation also significantly increased the levels of total antioxidant capacity (T-AOC), glutathione peroxidase (GSH-Px) (P < 0.01), and superoxide dismutase (SOD) (P < 0.05), and decreased inflammatory cytokine levels (tumor necrosis factor-α (TNF-α) and interleukin-6 (IL-6)) (P < 0.01). Furthermore, the WG-rich diet reshaped the composition of the gut microbiota, enhancing short-chain fatty acids (SCFAs)-producing microbes and reducing inflammation-related microbes. In addition, metabolomics analysis showed that 5% WG supplementation improved plasma metabolites related to bone metabolism. Conclusively, our study purports long-term WG-rich diet may preserve bone homeostasis by regulating gut microbiota and plasma metabolites in aged rats.

Keywords

Wheat germBone homeostasisGut microbiotaMetabolitesAgeing

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References

[1]

J.H. Cole, R.E. Marioni, S.E. Harris, et al., Brain age and other bodily ‘ages’: implications for neuropsychiatry, Mol. Psychiatry 24 (2019) 266-281. https://doi.org/10.1038/s41380-018-0098-1.
Crossref Google Scholar
[2]

T. Sözen, L. Özışık, N.Ç. Başaran, An overview and management of osteoporosis, J. Funct. Foods 4 (2017) 46. https://doi.org/10.1016/j.jff.2018.06.013.
Crossref Google Scholar
[3]

J.Y. Reginster, N. Burlet. Osteoporosis: a still increasing prevalence, Bone 38 (2006) 4-9. https://doi.org/10.1016/j.bone.2005.11.024.
Crossref Google Scholar
[4]

V. Domazetovic, G. Marcucci, T. Iantomasi, et al., Oxidative stress in bone remodeling: role of antioxidants, Clin. Cases Miner. Bone Metab. 14 (2017) 209. https://doi.org/10.11138/ccmbm/2017.14.1.209.
Crossref Google Scholar
[5]

D. Maggio, M. Barabani, M. Pierandrei, Marked decrease in plasma antioxidants in aged osteoporotic women: results of a cross-sectional study, J. Clin. Endocrinol. Metab. 88 (2003) 1523-1527. https://doi.org/10.1210/jc.2002-021496.
Crossref Google Scholar
[6]

O.F. Sendur, Y. Turan, E. Tastaban, et al., Antioxidant status in patients with osteoporosis: a controlled study, Joint Bone Spine 76 (2009) 514-518. https://doi.org/10.1016/j.jbspin.2009.02.005.
Crossref Google Scholar
[7]

D.J. Morton, E.L. Barrett-Connor, D.L. Schneider, Vitamin C supplement use and bone mineral density in postmenopausal women, J. Bone Miner. Res. 16 (2001) 135-140. https://doi.org/10.1359/jbmr.2001.16.1.135.
Crossref Google Scholar
[8]

S.C. Manolagas, From estrogen-centric to aging and oxidative stress: a revised perspective of the pathogenesis of osteoporosis, Endocr. Rev. 31 (2010) 266-300. https://doi.org/10.1210/er.2009-0024.
Crossref Google Scholar
[9]

S.C. Kim, D.H. Kim, H. Mogun, et al., Impact of the US Food and Drug Administration’s safety-related announcements on the use of bisphosphonates after hip fracture, J. Bone Miner. Res. 31 (2016) 1536-1540. https://doi.org/10.1002/jbmr.2832.
Crossref Google Scholar
[10]

L. Li, S. Rao, Y. Cheng, et al., Microbial osteoporosis: the interplay between the gut microbiota and bones via host metabolism and immunity, Microbiol. Open 8 (2019) e00810. https://doi.org/10.1002/mbo3.810.
Crossref Google Scholar
[11]

L. Ibáñez, M. Rouleau, A. Wakkach, et al., Gut microbiome and bone, Joint Bone Spine 86 (2019) 43-47. https://doi.org/10.1016/j.jbspin.2018.02.008.
Crossref Google Scholar
[12]

H.J. Wu, I.I. Ivanov, J. Darce, et al., Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells, Immunity 32 (2010) 815-827. https://doi.org/10.1016/j.immuni.2010.06.001.
Crossref Google Scholar
[13]

H. Lan, W. Hong, D. Qian, et al., Quercetin modulates the gut microbiota as well as the metabolome in a rat model of osteoarthritis, Bioengineered 12 (2021) 6240-6250. https://doi.org/10.1080/21655979.2021.1969194.
Crossref Google Scholar
[14]

Y. Luo, G.L. Chen, N. Hannemann, et al., Microbiota from obese mice regulate hematopoietic stem cell differentiation by altering the bone niche, Cell Metab. 22 (2015) 886-894. https://doi.org/10.1016/j.cmet.2015.08.020.
Crossref Google Scholar
[15]

F. Mei, K. Meng, Z. Gu,, et al., Arecanut (Areca catechu L.) seed polyphenol-ameliorated osteoporosis by altering gut microbiome via LYZ and the immune system in estrogen-deficient rats, J. Agric. Food Chem. 69 (2020) 246-258. https://doi.org/10.1021/acs.jafc.0c06671.
Crossref Google Scholar
[16]

B. Li, M. Liu, Y. Wang, et al., Puerarin improves the bone micro-environment to inhibit OVX-induced osteoporosis via modulating SCFAs released by the gut microbiota and repairing intestinal mucosal integrity, Biomed. Pharmacother. 132 (2020) 110923. https://doi.org/10.1016/j.biopha.2020.110923.
Crossref Google Scholar
[17]

L. Zhang, Y. Yue, M. Shi, et al., Dietary Luffa cylindrica (L.) Roem promotes branched-chain amino acid catabolism in the circulation system via gut microbiota in diet-induced obese mice, Food Chem. 320 (2020) 126648. https://doi.org/10.1016/j.foodchem.2020.126648.
Crossref Google Scholar
[18]

Y.Y. Zhu, K. Thakur, J.Y. Feng, et al., Riboflavin bioenriched soymilk alleviates oxidative stress mediated liver injury, intestinal inflammation, and gut microbiota modification in b2 depletion-repletion mice, J. Agric. Food Chem. 70 (2022) 3818-3831. https://doi.org/10.1021/acs.jafc.2c00117.
Crossref Google Scholar
[19]

A. Brandolini, A. Hidalgo. Wheat germ: not only a by-product, Int. J. Food Sci. Nutr. 63 (2012) 71-74. https://doi.org/10.3109/09637486.2011.633898.
Crossref Google Scholar
[20]

L.G. Boros, M. Nichelatti, Y. Shoenfeld, Fermented wheat germ extract (Avemar) in the treatment of cancer and autoimmune diseases, Ann. Ny. Acad. Sci. 1051 (2005) 529-542. https://doi.org/10.1196/annals.1361.097.
Crossref Google Scholar
[21]

A. Iyer, L. Brown, Fermented wheat germ extract (Avemar) in the treatment of cardiac remodeling and metabolic symptoms in rats, Evid-Based. Compl. Alt. (2011) 1-10. https://doi.org/10.1093/ecam/nep090.
Crossref Google Scholar
[22]

C. Liu, Y. Sun, L. Yang, et al., The hypolipidemic and antioxidant activity of wheat germ and wheat germ protein in high-fat diet-induced rats, Molecules 27 (2022) 2260. https://doi.org/10.3390/molecules27072260.
Crossref Google Scholar
[23]

B. Ojo, A.J. Simenson, C.O. Hara, et al., Wheat germ supplementation alleviates insulin resistance and cardiac mitochondrial dysfunction in an animal model of diet-induced obesity, Briti. J. Nutr. 118 (2017) 241-249. https://doi.org/10.1017/s0007114517002082.
Crossref Google Scholar
[24]

R. Weitzen N. Epstein, B. Oberman, et al., Fermented wheat germ extract (FWGE) as a treatment additive for castration-resistant prostate cancer: a pilot clinical trial, Nutr. Cancer 74 (2022) 1338-1346. https://doi.org/10.1080/01635581.2021.1952457.
Crossref Google Scholar
[25]

Z. Weng, Y. Chen, T. Liang, et al., A review on processing methods and functions of wheat germ-derived bioactive peptides, Crit. Rev. Food Sci. 63 (2021) 1-17. https://doi.org/10.1080/10408398.2021.2021139.
Crossref Google Scholar
[26]

M.M. Rahman, A. Bhattacharya, J. Banu, et al., Conjugated linoleic acid protects against age-associated bone loss in C57BL/6 female mice, J. Nutr. Biochem. (2007) 467-474. https://doi.org/10.1016/j.jnutbio.2006.08.002.
Crossref Google Scholar
[27]

A.M. Neyrinck, V.F. Van Hee, N. Piront, et al., Wheat-derived arabinoxylan oligosaccharides with prebiotic effect increase satietogenic gut peptides and reduce metabolic endotoxemia in diet-induced obese mice, Nutr. Diabetes 2 (2012) e28. https://doi.org/10.1038/nutd.2011.24.
Crossref Google Scholar
[28]

A. Carvalho-Wells, L. Helmolz, K. Nodet, et al., Determination of the in vivo prebiotic potential of a maize-based whole grain breakfast cereal: a human feeding study, Br. J. Nutr. 104 (2010) 1353-1356. https://doi.org/10.1017/s0007114510002084.
Crossref Google Scholar
[29]

A. Costabile, A Klinder, F. Fava, et al., Whole-grain wheat breakfast cereal has a prebiotic effect on the human gut microbiota: a double-blind, placebo-controlled, crossover study, Br. J. Nutr. 99 (2008) 110-120. https://doi.org/10.1017/s0007114507793923.
Crossref Google Scholar
[30]

H. Mohammadi, M. Karimifar, Z. Heidari, et al., The effects of wheat germ consumption on mental health and brain-derived neurotrophic factor in subjects with type 2 diabetes mellitus: a randomized, double-blind, placebo-controlled trial, Nutr. Neurosci. 25 (2022) 46-53. https://doi.org/10.1080/1028415x.2019.1708032.
Crossref Google Scholar
[31]

B.A. Ojo, C.O’ Hara, L. Wu, et al., Wheat germ supplementation increases lactobacillaceae and promotes an anti-inflammatory gut milieu in C57BL/6 mice fed a high-fat, high-sucrose diet, J. Nutr. 149 (2019) 1107-1115. https://doi.org/10.1093/jn/nxz061.
Crossref Google Scholar
[32]

A. Moreira-Rosário, C. Marques, H. Pinheiro, et al., Daily intake of wheat germ-enriched bread may promote a healthy gut bacterial microbiota: a randomised controlled trial, Eur. J. Nutr. 59 (2020) 1951-1961. https://doi.org/10.1007/s00394-019-02045-x.
Crossref Google Scholar
[33]

F. Fan, P. Shi, M. Liu, et al., Lactoferrin preserves bone homeostasis by regulating the RANKL/RANK/OPG pathway of osteoimmunology, Food Funct. 9 (2018) 2653-2660. https://doi.org/10.1039/c8fo00303c.
Crossref Google Scholar
[34]

B. Ren, L. Wang, A. Mulati, et al., Methionine restriction improves gut barrier function by reshaping diurnal rhythms of inflammation-related microbes in aged mice, Front. Nutr. 8 (2021) 746592. https://doi.org/10.3389/fnut.2021.746592.
Crossref Google Scholar
[35]

Y.W. Ge, K. Feng, X.L. Liu, et al., Quercetin inhibits macrophage polarization through the p-38 α/β signalling pathway and regulates OPG/RANKL balance in a mouse skull model, J. Cell. Mol. Med. 24 (2020) 3203-3216. https://doi.org/10.1111/jcmm.14995.
Crossref Google Scholar
[36]

K. Park, W.C. Ju, J.H. Yeo, et al., Increased OPG/RANKL ratio in the conditioned medium of soybean-treated osteoblasts suppresses RANKL-induced osteoclast differentiation, Int. J. Mol. Med. 33 (2014) 178-184. https://doi.org/10.3892/ijmm.2013.1557.
Crossref Google Scholar
[37]

J. Li, Z. Yao, X. Liu, et al., TGFβ1+ CCR5+ neutrophil subset increases in bone marrow and causes age-related osteoporosis in male mice, Nat. Commun. 14 (2023) 159. https://doi.org/10.1038/s41467-023-35801-z.
Crossref Google Scholar
[38]

F. Wang, Z. Weng, Y. Lyu, et al., Wheat germ-derived peptide ADWGGPLPH abolishes high glucose-induced oxidative stress via modulation of the PKCζ/AMPK/NOX4 pathway, Food Funct. 11 (2020) 6843-6854. https://doi.org/10.1039/d0fo01229g.
Crossref Google Scholar
[39]

G.R. Mundy, Osteoporosis and inflammation, Nutr. Rev. 65 (2007) 147-151. https://doi.org/10.1111/j.1753-4887.2007.tb00353.x.
Crossref Google Scholar
[40]

A.B. Hall, M. Yassour, J. Sauk, et al., A novel Ruminococcus gnavus clade enriched in inflammatory bowel disease patients, Genome Med. 9 (2017) 1-12. https://doi.org/10.1186/s13073-017-0490-5.
Crossref Google Scholar
[41]

E. Miyauchi, S.W. Kim, W. Suda, et al., Gut microorganisms act together to exacerbate inflammation in spinal cords, Nature 585 (2020) 102-106. https://doi.org/10.1038/s41586-020-2634-9.
Crossref Google Scholar
[42]

G.H. van Muijlwijk, G van Mierlo, P.W. Jansen, et al., Identification of Allobaculum mucolyticum as a novel human intestinal mucin degrader, Gut Microbes 13 (2021) 1966278. https://doi.org/10.1080/19490976.2021.1966278.
Crossref Google Scholar
[43]

X. Liu, B. Mao, J. Gu, et al., Blautia-a new functional genus with potential probiotic properties? Gut Microbes 13 (2021) 1875796. https://doi.org/10.1080/19490976.2021.1875796.
Crossref Google Scholar
[44]

L. Yun, W. Li, Y. Liu, et al., Regulation of wheat germ polysaccharides in the immune response of mice from newborn to adulthood associated with intestinal microbiota, Food Funct. 11 (2020) 9662-9674. https://doi.org/10.1039/d0fo02031a.
Crossref Google Scholar
[45]

M.M. Zaiss, R.M. Jones, G. Schett, et al., The gut-bone axis: how bacterial metabolites bridge the distance, J. Clin. Invest. 129 (2019) 3018-3028. https://doi.org/10.1172/jci128521.
Crossref Google Scholar
[46]

M.-J. Choi, N. M. DiMarco, The effects of dietary taurine supplementation on bone mineral density in ovariectomized rats, Adv. Exp. Med. Biol. 643 (2009) 341-349. https://doi.org/10.1007/978-0-387-75681-3.
Crossref Google Scholar
[47]

G. Duque, C. Vidal, W. Li, et al., Picolinic acid, a catabolite of tryptophan, has an anabolic effect on bone in vivo, J. Bone Miner. Res. 35 (2020) 2275-2288. https://doi.org/10.1002/jbmr.4125.
Crossref Google Scholar
Food Science and Human Wellness
Volume 13 Issue 6,
November 2024
Pages 3582-3594
DOI: 10.26599/FSHW.2023.9250040
Cite this article:
Wang L, Weng Z, Chen T, et al. A wheat germ-rich diet preserves bone homeostasis by regulating gut microbiota and plasma metabolites in aged rats. Food Science and Human Wellness, 2024, 13(6): 3582-3594. https://doi.org/10.26599/FSHW.2023.9250040

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Received: 20 February 2023
Revised: 18 March 2023
Accepted: 30 April 2023
Published: 18 December 2024
© 2024 Beijing Academy of Food Sciences. Publishing services by Tsinghua University Press.

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
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