Omega-3 PUFAs prevent bone impairment and bone marrow adiposity in mouse model of obesity

. 2023 Oct 14 ; 6 (1) : 1043. [epub] 20231014

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid37833362
Odkazy

PubMed 37833362
PubMed Central PMC10575870
DOI 10.1038/s42003-023-05407-8
PII: 10.1038/s42003-023-05407-8
Knihovny.cz E-zdroje

Obesity adversely affects bone and fat metabolism in mice and humans. Omega-3 polyunsaturated fatty acids (omega-3 PUFAs) have been shown to improve glucose metabolism and bone homeostasis in obesity. However, the impact of omega-3 PUFAs on bone marrow adipose tissue (BMAT) and bone marrow stromal cell (BMSC) metabolism has not been intensively studied yet. In the present study we demonstrated that omega-3 PUFA supplementation in high fat diet (HFD + F) improved bone parameters, mechanical properties along with decreased BMAT in obese mice when compared to the HFD group. Primary BMSCs isolated from HFD + F mice showed decreased adipocyte and higher osteoblast differentiation with lower senescent phenotype along with decreased osteoclast formation suggesting improved bone marrow microenvironment promoting bone formation in mice. Thus, our study highlights the beneficial effects of omega-3 PUFA-enriched diet on bone and cellular metabolism and its potential use in the treatment of metabolic bone diseases.

Zobrazit více v PubMed

Bluher M. Adipose tissue dysfunction contributes to obesity related metabolic diseases. Best Pract. Res. Clin. Endocrinol. Metab. 2013;27:163–177. PubMed

Benova A, Tencerova M. Obesity-induced changes in bone marrow homeostasis. Front. Endocrinol. 2020;11:294. PubMed PMC

Swinburn BA, Caterson I, Seidell JC, James WP. Diet, nutrition and the prevention of excess weight gain and obesity. Public Health Nutr. 2004;7:123–146. PubMed

Tencerova M, et al. High-fat diet-induced obesity promotes expansion of bone marrow adipose tissue and impairs skeletal stem cell functions in mice. J. Bone Miner. Res. 2018;33:1154–1165. PubMed

Scheller EL, et al. Changes in skeletal integrity and marrow adiposity during high-fat diet and after weight loss. Front. Endocrinol. 2016;7:102. PubMed PMC

Benova A, et al. Novel thiazolidinedione analog reduces a negative impact on bone and mesenchymal stem cell properties in obese mice compared to classical thiazolidinediones. Mol. Metab. 2022;65:101598. PubMed PMC

Lecka-Czernik B, Stechschulte LA, Czernik PJ, Dowling AR. High bone mass in adult mice with diet-induced obesity results from a combination of initial increase in bone mass followed by attenuation in bone formation; implications for high bone mass and decreased bone quality in obesity. Mol. Cell Endocrinol. 2015;410:35–41. PubMed

Lewgood J, et al. Efficacy of dietary and supplementation interventions for individuals with type 2 diabetes. Nutrients. 2021;13:2378. PubMed PMC

Kirwan JP, Sacks J, Nieuwoudt S. The essential role of exercise in the management of type 2 diabetes. Cleve. Clin. J. Med. 2017;84:S15–S21. PubMed PMC

Saini RK, et al. Omega-3 Polyunsaturated Fatty Acids (PUFAs): emerging plant and microbial sources, oxidative stability, bioavailability, and health benefits-a review. Antioxidants. 2021;10:1627. PubMed PMC

Sistilli G, et al. Krill oil supplementation reduces exacerbated hepatic steatosis induced by thermoneutral housing in mice with diet-induced obesity. Nutrients. 2021;13:437. PubMed PMC

Calder PC. Marine omega-3 fatty acids and inflammatory processes: effects, mechanisms, and clinical relevance. Biochim. Biophys. Acta. 2015;1851:469–484. PubMed

Flachs P, et al. Polyunsaturated fatty acids of marine origin induce adiponectin in mice fed a high-fat diet. Diabetologia. 2006;49:394–397. PubMed

van Schothorst EM, et al. Induction of lipid oxidation by polyunsaturated fatty acids of marine origin in small intestine of mice fed a high-fat diet. BMC Genom. 2009;10:110. PubMed PMC

Kroupova P, et al. Omega-3 phospholipids from krill oil enhance intestinal fatty acid oxidation more effectively than Omega-3 triacylglycerols in high-fat diet-fed obese mice. Nutrients. 2020;12:2037. PubMed PMC

Martyniak K, et al. Do polyunsaturated fatty acids protect against bone loss in our aging and osteoporotic population? Bone. 2021;143:115736. PubMed

Rossmeisl M, et al. Omega-3 phospholipids from fish suppress hepatic steatosis by integrated inhibition of biosynthetic pathways in dietary obese mice. Biochim. Biophys. Acta. 2014;1841:267–278. PubMed

Salari P, Rezaie A, Larijani B, Abdollahi M. A systematic review of the impact of n-3 fatty acids in bone health and osteoporosis. Med. Sci. Monit. 2008;14:RA37–RA44. PubMed

Shen CL, Yeh JK, Rasty J, Li Y, Watkins BA. Protective effect of dietary long-chain n-3 polyunsaturated fatty acids on bone loss in gonad-intact middle-aged male rats. Br. J. Nutr. 2006;95:462–468. PubMed

Bani Hassan E, et al. The effects of dietary fatty acids on bone, hematopoietic marrow and marrow adipose tissue in a murine model of senile osteoporosis. Aging. 2019;11:7938–7947. PubMed PMC

Cao JJ, Gregoire BR, Michelsen KG, Picklo MJ. Increasing dietary fish oil reduces adiposity and mitigates bone deterioration in growing C57BL/6 mice fed a high-fat diet. J. Nutr. 2020;150:99–107. PubMed

Levental KR, et al. omega-3 polyunsaturated fatty acids direct differentiation of the membrane phenotype in mesenchymal stem cells to potentiate osteogenesis. Sci. Adv. 2017;3:eaao1193. PubMed PMC

Cugno C, et al. Omega-3 fatty acid-rich fish oil supplementation prevents rosiglitazone-induced osteopenia in aging C57BL/6 mice and in vitro studies. Sci Rep. 2021;11:10364. PubMed PMC

Bardova K, et al. Additive effects of Omega-3 fatty acids and thiazolidinediones in mice fed a high-fat diet: triacylglycerol/fatty acid cycling in adipose tissue. Nutrients. 2020;12:3737. PubMed PMC

Kerckhofs G, et al. Contrast-enhanced nanofocus X-Ray computed tomography allows virtual three-dimensional histopathology and morphometric analysis of osteoarthritis in small animal models. Cartilage. 2014;5:55–65. PubMed PMC

Sun D, et al. Dietary n-3 fatty acids decrease osteoclastogenesis and loss of bone mass in ovariectomized mice. J. Bone Miner. Res. 2003;18:1206–1216. PubMed

Bhattacharya A, Rahman M, Sun D, Fernandes G. Effect of fish oil on bone mineral density in aging C57BL/6 female mice. J Nutr Biochem. 2007;18:372–379. PubMed

Anez-Bustillos L, et al. Effects of dietary omega-3 fatty acids on bones of healthy mice. Clin Nutr. 2019;38:2145–2154. PubMed PMC

Farahnak Z, Freundorfer MT, Lavery P, Weiler HA. Dietary docosahexaenoic acid contributes to increased bone mineral accretion and strength in young female Sprague-Dawley rats. Prostaglandins Leukot. Essent. Fatty Acids. 2019;144:32–39. PubMed

Mollard RC, Gillam ME, Wood TM, Taylor CG, Weiler HA. (n-3) fatty acids reduce the release of prostaglandin E2 from bone but do not affect bone mass in obese (fa/fa) and lean Zucker rats. J. Nutr. 2005;135:499–504. PubMed

Kerckhofs G, et al. Simultaneous three-dimensional visualization of mineralized and soft skeletal tissues by a novel microCT contrast agent with polyoxometalate structure. Biomaterials. 2018;159:1–12. PubMed

Scheller EL, et al. Use of osmium tetroxide staining with microcomputerized tomography to visualize and quantify bone marrow adipose tissue in vivo. Methods Enzymol. 2014;537:123–139. PubMed PMC

Cho HJ, Lee J, Yoon SR, Lee HG, Jung H. Regulation of hematopoietic stem cell fate and malignancy. Int. J. Mol. Sci. 2020;21:4780. PubMed PMC

Nakanishi A, Tsukamoto I. n-3 polyunsaturated fatty acids stimulate osteoclastogenesis through PPARgamma-mediated enhancement of c-Fos expression, and suppress osteoclastogenesis through PPARgamma-dependent inhibition of NFkB activation. J. Nutr. Biochem. 2015;26:1317–1327. PubMed

Zwart SR, Pierson D, Mehta S, Gonda S, Smith SM. Capacity of omega-3 fatty acids or eicosapentaenoic acid to counteract weightlessness-induced bone loss by inhibiting NF-kappaB activation: from cells to bed rest to astronauts. J. Bone Miner. Res. 2010;25:1049–1057. PubMed

Gani OA. Are fish oil omega-3 long-chain fatty acids and their derivatives peroxisome proliferator-activated receptor agonists? Cardiovasc. Diabetol. 2008;7:6. PubMed PMC

McDonald MM, et al. Osteoclasts recycle via osteomorphs during RANKL-stimulated bone resorption. Cell. 2021;184:1330–1347.e1313. PubMed PMC

Flachs P, et al. Polyunsaturated fatty acids of marine origin upregulate mitochondrial biogenesis and induce beta-oxidation in white fat. Diabetologia. 2005;48:2365–2375. PubMed

Zhang L, Mack R, Breslin P, Zhang J. Molecular and cellular mechanisms of aging in hematopoietic stem cells and their niches. J. Hematol. Oncol. 2020;13:157. PubMed PMC

Omer M, et al. Omega-9 modifies viscoelasticity and augments bone strength and architecture in a high-fat diet-fed murine model. Nutrients. 2022;14:3165. PubMed PMC

Watkins BA, Shen CL, Allen KG, Seifert MF. Dietary (n-3) and (n-6) polyunsaturates and acetylsalicylic acid alter ex vivo PGE2 biosynthesis, tissue IGF-I levels, and bone morphometry in chicks. J. Bone Miner. Res. 1996;11:1321–1332. PubMed

Raisz LG. Prostaglandins and bone: physiology and pathophysiology. Osteoarthritis Cartilage. 1999;7:419–421. PubMed

Kus V, et al. Unmasking differential effects of rosiglitazone and pioglitazone in the combination treatment with n-3 fatty acids in mice fed a high-fat diet. PLoS One. 2011;6:e27126. PubMed PMC

Rossmeisl M, et al. Differential modulation of white adipose tissue endocannabinoid levels by n-3 fatty acids in obese mice and type 2 diabetic patients. Biochim. Biophys. Acta Mol. Cell Biol. Lipids. 2018;1863:712–725. PubMed

Jafari A, et al. Pharmacological inhibition of protein kinase g1 enhances bone formation by human skeletal stem cells through activation of RhoA-Akt Signaling. Stem Cells. 2015;33:2219–2231. PubMed

Tencerova M, et al. Obesity-associated hypermetabolism and accelerated senescence of bone marrow stromal stem cells suggest a potential mechanism for bone fragility. Cell Rep. 2019;27:2050–2062.e2056. PubMed

Halper J, Madel MB, Blin-Wakkach C. Differentiation and phenotyping of murine osteoclasts from bone marrow progenitors, monocytes, and dendritic cells. Methods Mol. Biol. 2021;2308:21–34. PubMed

Hansen MS, et al. GIP reduces osteoclast activity and improves osteoblast survival in primary human bone cells. Eur. J. Endocrinol. 2023;188:lvac004. PubMed

Ding M, Danielsen CC, Hvid I. Age-related three-dimensional microarchitectural adaptations of subchondral bone tissues in guinea pig primary osteoarthrosis. Calcif. Tissue Int. 2006;78:113–122. PubMed

Jardi F, et al. Androgen receptor in neurons slows age-related cortical thinning in male mice. J. Bone Miner. Res. 2019;34:508–519. PubMed

Callewaert F, et al. Sexual dimorphism in cortical bone size and strength but not density is determined by independent and time-specific actions of sex steroids and IGF-1: evidence from pubertal mouse models. J. Bone Miner. Res. 2010;25:617–626. PubMed

Pajuelo Reguera D, et al. Cytochrome c oxidase subunit 4 isoform exchange results in modulation of oxygen affinity. Cells. 2020;9:443. PubMed PMC

Janovska P, et al. Dysregulation of epicardial adipose tissue in cachexia due to heart failure: the role of natriuretic peptides and cardiolipin. J. Cachexia Sarcopenia Muscle. 2020;11:1614–1627. PubMed PMC

Tsugawa H, et al. A lipidome atlas in MS-DIAL 4. Nat. Biotechnol. 2020;38:1159–1163. PubMed

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...