Human breastmilk-derived <i>Bifidobacterium longum</i> subsp. <i>infantis</i> CCFM1269 regulates bone formation by the GH/IGF axis through PI3K/AKT pathway

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ABSTRACT

Bifidobacterium longum subsp. infantis is a prevalent member of the gut microbiota of breastfed infants. In this study, the effects of human breastmilk-derived B.longum subsp. infantis CCFM1269 on bone formation in developing BALB/c mice were investigated. Newborn female and male mice were assigned to control group (administered saline), CCFM1269 group (administered B. longum subsp. infantis CCFM1269, 1 × 10 ₉ CFU/mouse/day) and I5TI group (administered B. longum subsp. infantis I5TI, 1 × 10 ₉ CFU/mouse/day) from 1-week-old to 3-, 4- and 5-week old. B. longum subsp. infantis I5TI served as a negative control in this study. The results demonstrated that B. longum subsp. infantis CCFM1269 promoted bone formation in growing mice by modulating the composition of the gut microbiota and metabolites. The expression of genes and proteins in the PI3K/AKT pathway was stimulated by B. longum subsp. infantis CCFM1269 through the GH/IGF-1 axis in growing mice. This finding suggests B. longum subsp. infantis CCFM1269 may be useful for modulating bone metabolism during growth.

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The Impact of Dietary Fiber on Gut Microbiota in Host Health and Disease

Fredrik Bäckhed, Kassem Makki, Edward C Deehan … (2018)

Food is a primordial need for our survival and well-being. However, diet is not only essential to maintain human growth, reproduction, and health, but it also modulates and supports the symbiotic microbial communities that colonize the digestive tract-the gut microbiota. Type, quality, and origin of our food shape our gut microbes and affect their composition and function, impacting host-microbe interactions. In this review, we will focus on dietary fibers, which interact directly with gut microbes and lead to the production of key metabolites such as short-chain fatty acids, and discuss how dietary fiber impacts gut microbial ecology, host physiology, and health. Hippocrates' notion "Let food be thy medicine and medicine be thy food" remains highly relevant millennia later, but requires consideration of how diet can be used for modulation of gut microbial ecology to promote health.

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Gut microbiota induce IGF-1 and promote bone formation and growth.

Jing Yan, Jeremy W. Herzog, Kelly Tsang … (2016)

Appreciation of the role of the gut microbiome in regulating vertebrate metabolism has exploded recently. However, the effects of gut microbiota on skeletal growth and homeostasis have only recently begun to be explored. Here, we report that colonization of sexually mature germ-free (GF) mice with conventional specific pathogen-free (SPF) gut microbiota increases both bone formation and resorption, with the net effect of colonization varying with the duration of colonization. Although colonization of adult mice acutely reduces bone mass, in long-term colonized mice, an increase in bone formation and growth plate activity predominates, resulting in equalization of bone mass and increased longitudinal and radial bone growth. Serum levels of insulin-like growth factor 1 (IGF-1), a hormone with known actions on skeletal growth, are substantially increased in response to microbial colonization, with significant increases in liver and adipose tissue IGF-1 production. Antibiotic treatment of conventional mice, in contrast, decreases serum IGF-1 and inhibits bone formation. Supplementation of antibiotic-treated mice with short-chain fatty acids (SCFAs), products of microbial metabolism, restores IGF-1 and bone mass to levels seen in nonantibiotic-treated mice. Thus, SCFA production may be one mechanism by which microbiota increase serum IGF-1. Our study demonstrates that gut microbiota provide a net anabolic stimulus to the skeleton, which is likely mediated by IGF-1. Manipulation of the microbiome or its metabolites may afford opportunities to optimize bone health and growth.

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Short-chain fatty acids regulate systemic bone mass and protect from pathological bone loss

Sébastien Lucas, Yasunori Omata, Jörg Hofmann … (2018)

Microbial metabolites are known to modulate immune responses of the host. The main metabolites derived from microbial fermentation of dietary fibers in the intestine, short-chain fatty acids (SCFA), affect local and systemic immune functions. Here we show that SCFA are regulators of osteoclast metabolism and bone mass in vivo. Treatment of mice with SCFA as well as feeding with a high-fiber diet significantly increases bone mass and prevents postmenopausal and inflammation-induced bone loss. The protective effects of SCFA on bone mass are associated with inhibition of osteoclast differentiation and bone resorption in vitro and in vivo, while bone formation is not affected. Mechanistically, propionate (C3) and butyrate (C4) induce metabolic reprogramming of osteoclasts resulting in enhanced glycolysis at the expense of oxidative phosphorylation, thereby downregulating essential osteoclast genes such as TRAF6 and NFATc1. In summary, these data identify SCFA as potent regulators of osteoclast metabolism and bone homeostasis.

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Author and article information

Journal

Journal ID (nlm-ta): Gut Microbes

Journal ID (iso-abbrev): Gut Microbes

Title: Gut Microbes

Publisher: Taylor & Francis

ISSN (Print): 1949-0976

ISSN (Electronic): 1949-0984

Publication date (Electronic, pub): 20 December 2023

Publication date (Electronic, collection): 2024

Publication date PMC-release: 20 December 2023

Volume: 16

Issue: 1

Electronic Location Identifier: 2290344

Affiliations

[a ]State Key Laboratory of Food Science and Resources, Jiangnan University; , Wuxi, Jiangsu, China

[b ]School of Food Science and Technology, Jiangnan University; , Wuxi, Jiangsu, China

[c ]Department of Applied Nutrition I, China National Center for Food Safety Risk Assessment; , Beijing, China

[d ]International Joint Research Center for Probiotics & Gut Health, Jiangnan University; , Wuxi, Jiangsu, China

[e ]APC Microbiome Ireland, University College Cork; , Cork, Ireland

[f ]Food Biosciences, Teagasc Food Research Centre; , Fermoy, Cork, Ireland

[g ]National Engineering Research Center for Functional Food, Jiangnan University; , Wuxi, Jiangsu, China

Author notes

CONTACT Dong Liang liangdong@ 123456cfsa.net.cn China National Center for Food Safety Risk Assessment; , Beijing 100021, China

Bo Yang bo.yang@ 123456jiangnan.edu.cn School of Food Science and Technology, Jiangnan University; , 1800 Lihu Avenue, Wuxi 214122, China

Author information

Mengfan Ding https://orcid.org/0000-0002-5820-6736

Bowen Li https://orcid.org/0000-0002-4199-7164

Bo Yang https://orcid.org/0000-0002-1347-3718

Article

Publisher ID: 2290344

DOI: 10.1080/19490976.2023.2290344

PMC ID: 10761167

PubMed ID: 38116652

SO-VID: 210ed9f2-8a8b-424d-afcf-d43df13e9139

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This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License ( http://creativecommons.org/licenses/by-nc/4.0/), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. The terms on which this article has been published allow the posting of the Accepted Manuscript in a repository by the author(s) or with their consent.

Human breastmilk-derived Bifidobacterium longum subsp. infantis CCFM1269 regulates bone formation by the GH/IGF axis through PI3K/AKT pathway

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Most cited references 56

The Impact of Dietary Fiber on Gut Microbiota in Host Health and Disease

Gut microbiota induce IGF-1 and promote bone formation and growth.

Short-chain fatty acids regulate systemic bone mass and protect from pathological bone loss

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