MiRNAs Expression Modulates Osteogenesis in Response to Exercise and Nutrition
Abstract
:1. Introduction
2. Methodology Section
3. Exercise and Osteogenic miRNAs Expression
4. Endogenous miRNAs and Bone Metabolism
5. Micronutrients Intake and Osteogenic miRNAs Expression
5.1. Vitamin D Intakes
5.2. Vitamin C Intakes
5.3. Orthosilicic Acid (OSA) Intakes
5.4. Other Micronutrients Intakes
6. Macronutrients Intake and Osteogenic miRNAs Expression
7. Exogenous miRNA and Bone Metabolism
8. Discussions and Conclusions
9. Limitations of the Study
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Condrat, C.E.; Thompson, D.C.; Barbu, M.G.; Bugnar, O.L.; Boboc, A.; Cretoiu, D.; Suciu, N.; Cretoiu, S.M.; Voinea, S.C. miRNAs as biomarkers in disease: Latest findings regarding their role in diagnosis and prognosis. Cells 2020, 9, 276. [Google Scholar] [CrossRef] [PubMed]
- Hausser, J.; Zavolan, M. Identification and consequences of miRNA–target interactions—Beyond repression of gene expression. Nat. Rev. Genet. 2014, 15, 599–612. [Google Scholar] [CrossRef] [PubMed]
- Schiera, G.; Contrò, V.; Sacco, A.; Macchiarella, A.; Cieszczyk, P.; Proia, P. From epigenetics to anti-doping application: A new tool of detection. Hum. Mov. 2017, 18, 3–10. [Google Scholar] [CrossRef]
- Folwarczna, J.; Zych, M.; Burczyk, J.; Trzeciak, H.; Trzeciak, H.I. Effects of natural phenolic acids on the skeletal system of ovariectomized rats. Planta Med. 2009, 75, 1567–1572. [Google Scholar] [CrossRef] [PubMed]
- Lisse, T.S.; Adams, J.S.; Hewison, M. Vitamin D and microRNAs in bone. Crit. Rev.TM Eukaryot. Gene Expr. 2013, 23, 195–214. [Google Scholar] [CrossRef]
- Beckett, E.L.; Yates, Z.; Veysey, M.; Duesing, K.; Lucock, M. The role of vitamins and minerals in modulating the expression of microRNA. Nutr. Res. Rev. 2014, 27, 94–106. [Google Scholar] [CrossRef]
- Arumugam, B.; Balagangadharan, K.; Selvamurugan, N. Syringic acid, a phenolic acid, promotes osteoblast differentiation by stimulation of Runx2 expression and targeting of Smad7 by miR-21 in mouse mesenchymal stem cells. J. Cell Commun. Signal. 2018, 12, 561–573. [Google Scholar] [CrossRef]
- Kolhe, R.; Mondal, A.K.; Pundkar, C.; Periyasamy-Thandavan, S.; Mendhe, B.; Hunter, M.; Isales, C.M.; Hill, W.D.; Hamrick, M.W.; Fulzele, S. Modulation of miRNAs by vitamin C in human bone marrow stromal cells. Nutrients 2018, 10, 186. [Google Scholar] [CrossRef]
- Valenti, M.T.; Deiana, M.; Cheri, S.; Dotta, M.; Zamboni, F.; Gabbiani, D.; Schena, F.; Dalle Carbonare, L.; Mottes, M. Physical exercise modulates miR-21-5p, miR-129-5p, miR-378-5p, and miR-188-5p expression in progenitor cells promoting osteogenesis. Cells 2019, 8, 742. [Google Scholar] [CrossRef]
- Sohel, M.M.H. Macronutrient modulation of mRNA and microRNA function in animals: A review. Anim. Nutr. 2020, 6, 258–268. [Google Scholar] [CrossRef]
- You, Y.; Ma, W.; Jiao, G.; Zhang, L.; Zhou, H.; Wu, W.; Wang, H.; Chen, Y. Ortho-silicic acid enhances osteogenesis of osteoblasts through the upregulation of miR-130b which directly targets PTEN. Life Sci. 2021, 264, 118680. [Google Scholar] [CrossRef]
- Zhang, L.; Chen, T.; Yin, Y.; Zhang, C.-Y.; Zhang, Y.-L. Dietary microRNA—A novel functional component of food. Adv. Nutr. 2019, 10, 711–721. [Google Scholar] [CrossRef] [PubMed]
- Zhang, L.; Hou, D.; Chen, X.; Li, D.; Zhu, L.; Zhang, Y.; Li, J.; Bian, Z.; Liang, X.; Cai, X. Exogenous plant MIR168a specifically targets mammalian LDLRAP1: Evidence of cross-kingdom regulation by microRNA. Cell Res. 2012, 22, 107–126. [Google Scholar] [CrossRef] [PubMed]
- Vimalraj, S.; Arumugam, B.; Miranda, P.; Selvamurugan, N. Runx2: Structure, function, and phosphorylation in osteoblast differentiation. Int. J. Biol. Macromol. 2015, 78, 202–208. [Google Scholar] [CrossRef] [PubMed]
- Oka, S.; Li, X.; Zhang, F.; Tewari, N.; Ma, R.; Zhong, L.; Makishima, M.; Liu, Y.; Bhawal, U.K. MicroRNA-21 facilitates osteoblast activity. Biochem. Biophys. Rep. 2021, 25, 100894. [Google Scholar] [CrossRef] [PubMed]
- Smieszek, A.; Marcinkowska, K.; Pielok, A.; Sikora, M.; Valihrach, L.; Marycz, K. The role of miR-21 in osteoblasts–osteoclasts coupling in vitro. Cells 2020, 9, 479. [Google Scholar] [CrossRef]
- Li, Z.; Hassan, M.Q.; Jafferji, M.; Aqeilan, R.I.; Garzon, R.; Croce, C.M.; van Wijnen, A.J.; Stein, J.L.; Stein, G.S.; Lian, J.B. Correction: Biological functions of miR-29b contribute to positive regulation of osteoblast differentiation. J. Biol. Chem. 2019, 294, 10018. [Google Scholar] [CrossRef]
- Shu, J.; Chiang, K.; Zempleni, J.; Cui, J. Computational characterization of exogenous microRNAs that can be transferred into human circulation. PLoS ONE 2015, 10, e0140587. [Google Scholar] [CrossRef]
- Díez-Sainz, E.; Lorente-Cebrián, S.; Aranaz, P.; Riezu-Boj, J.I.; Martínez, J.A.; Milagro, F.I. Potential mechanisms linking food-derived microRNAs, gut microbiota and intestinal barrier functions in the context of nutrition and human health. Front. Nutr. 2021, 8, 586564. [Google Scholar] [CrossRef]
- Huang, H.; Pham, Q.; Davis, C.D.; Yu, L.; Wang, T.T. Delineating effect of corn microRNAs and matrix, ingested as whole food, on gut microbiota in a rodent model. Food Sci. Nutr. 2020, 8, 4066–4077. [Google Scholar] [CrossRef]
- Di Liegro, C.M.; Schiera, G.; Di Liegro, I. Extracellular vesicle-associated RNA as a carrier of epigenetic information. Genes 2017, 8, 240. [Google Scholar] [CrossRef]
- Ikeda, K.; Satoh, M.; Pauley, K.M.; Fritzler, M.J.; Reeves, W.H.; Chan, E.K. Detection of the argonaute protein Ago2 and microRNAs in the RNA induced silencing complex (RISC) using a monoclonal antibody. J. Immunol. Methods 2006, 317, 38–44. [Google Scholar] [CrossRef] [PubMed]
- Moreira, L.D.F.; Oliveira, M.L.D.; Lirani-Galvão, A.P.; Marin-Mio, R.V.; Santos, R.N.D.; Lazaretti-Castro, M. Physical exercise and osteoporosis: Effects of different types of exercises on bone and physical function of postmenopausal women. Arq. Bras. De Endocrinol. Metabol. 2014, 58, 514–522. [Google Scholar] [CrossRef]
- Amato, A.; Baldassano, S.; Cortis, C.; Cooper, J.; Proia, P. Physical activity, nutrition, and bone health. Hum. Mov. 2018, 19, 1–10. [Google Scholar] [CrossRef]
- Yuan, Y.; Rao, L.-Z.; Zhang, S.-H.; Xu, Y.; Li, T.-T.; Zou, J.; Weng, X.-Q. Exercise regulates bone metabolism via microRNAs. Sheng Li Xue Bao Acta Physiol. Sin. 2023, 75, 429–438. [Google Scholar]
- Bemben, D.A.; Chen, Z.; Buchanan, S.R. Bone-Regulating MicroRNAs and Resistance Exercise: A Mini-Review. Osteology 2022, 2, 11–20. [Google Scholar] [CrossRef]
- Rossi, M.; Pitari, M.R.; Amodio, N.; Di Martino, M.T.; Conforti, F.; Leone, E.; Botta, C.; Paolino, F.M.; Del Giudice, T.; Iuliano, E. miR-29b negatively regulates human osteoclastic cell differentiation and function: Implications for the treatment of multiple myeloma-related bone disease. J. Cell. Physiol. 2013, 228, 1506–1515. [Google Scholar] [CrossRef] [PubMed]
- Tong, X.; Chen, X.; Zhang, S.; Huang, M.; Shen, X.; Xu, J.; Zou, J. The effect of exercise on the prevention of osteoporosis and bone angiogenesis. BioMed Res. Int. 2019, 2019, 8171897. [Google Scholar] [CrossRef]
- Song, M.S.; Salmena, L.; Pandolfi, P.P. The functions and regulation of the PTEN tumour suppressor. Nat. Rev. Mol. Cell Biol. 2012, 13, 283–296. [Google Scholar] [CrossRef]
- Yan, X.; Liu, Z.; Chen, Y. Regulation of TGF-β signaling by Smad7. Acta Biochim. Biophys. Sin. 2009, 41, 263–272. [Google Scholar] [CrossRef]
- Liu, X.; Bruxvoort, K.J.; Zylstra, C.R.; Liu, J.; Cichowski, R.; Faugere, M.-C.; Bouxsein, M.L.; Wan, C.; Williams, B.O.; Clemens, T.L. Lifelong accumulation of bone in mice lacking Pten in osteoblasts. Proc. Natl. Acad. Sci. USA 2007, 104, 2259–2264. [Google Scholar] [CrossRef] [PubMed]
- Weng, N.-P.; Granger, L.; Hodes, R.J. Telomere lengthening and telomerase activation during human B cell differentiation. Proc. Natl. Acad. Sci. USA 1997, 94, 10827–10832. [Google Scholar] [CrossRef]
- Cong, Y.-S.; Wright, W.E.; Shay, J.W. Human telomerase and its regulation. Microbiol. Mol. Biol. Rev. 2002, 66, 407–425. [Google Scholar] [CrossRef] [PubMed]
- Dalle Carbonare, L.; Mottes, M.; Cheri, S.; Deiana, M.; Zamboni, F.; Gabbiani, D.; Schena, F.; Salvagno, G.; Lippi, G.; Valenti, M. Increased gene expression of RUNX2 and SOX9 in mesenchymal circulating progenitors is associated with autophagy during physical activity. Oxidative Med. Cell. Longev. 2019, 2019, 8426259. [Google Scholar] [CrossRef] [PubMed]
- Zhu, H.-Y.; Li, C.; Bai, W.-D.; Su, L.-L.; Liu, J.-Q.; Li, Y.; Shi, J.-H.; Cai, W.-X.; Bai, X.-Z.; Jia, Y.-H. MicroRNA-21 regulates hTERT via PTEN in hypertrophic scar fibroblasts. PLoS ONE 2014, 9, e97114. [Google Scholar] [CrossRef]
- Ahmed, S.; Passos, J.F.; Birket, M.J.; Beckmann, T.; Brings, S.; Peters, H.; Birch-Machin, M.A.; von Zglinicki, T.; Saretzki, G. Telomerase does not counteract telomere shortening but protects mitochondrial function under oxidative stress. J. Cell Sci. 2008, 121, 1046–1053. [Google Scholar] [CrossRef]
- Gutteridge, J.M. Biological origin of free radicals, and mechanisms of antioxidant protection. Chem.-Biol. Interact. 1994, 91, 133–140. [Google Scholar] [CrossRef]
- Winterbourn, C.C. Toxicity of iron and hydrogen peroxide: The Fenton reaction. Toxicol. Lett. 1995, 82, 969–974. [Google Scholar] [CrossRef]
- Rossbach, M. Small non-coding RNAs as novel therapeutics. Curr. Mol. Med. 2010, 10, 361–368. [Google Scholar] [CrossRef]
- Li, J.; Zhang, R.; Du, Y.; Liu, G.; Dong, Y.; Zheng, M.; Cui, W.; Jia, P.; Xu, Y. Osteophilic and Dual-Regulated Alendronate-Gene Lipoplexes for Reversing Bone Loss. Small 2023, e2303456. [Google Scholar] [CrossRef]
- Kaur, J.; Saul, D.; Doolittle, M.L.; Rowsey, J.L.; Vos, S.J.; Farr, J.N.; Khosla, S.; Monroe, D.G. Identification of a suitable endogenous control miRNA in bone aging and senescence. Gene 2022, 835, 146642. [Google Scholar] [CrossRef] [PubMed]
- Lin, J.; Li, J.; Huang, B.; Liu, J.; Chen, X.; Chen, X.-M.; Xu, Y.-M.; Huang, L.-F.; Wang, X.-Z. Exosomes: Novel biomarkers for clinical diagnosis. Sci. World J. 2015, 2015, 657086. [Google Scholar] [CrossRef] [PubMed]
- Arroyo, J.D.; Chevillet, J.R.; Kroh, E.M.; Ruf, I.K.; Pritchard, C.C.; Gibson, D.F.; Mitchell, P.S.; Bennett, C.F.; Pogosova-Agadjanyan, E.L.; Stirewalt, D.L. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc. Natl. Acad. Sci. USA 2011, 108, 5003–5008. [Google Scholar] [CrossRef] [PubMed]
- Turchinovich, A.; Weiz, L.; Langheinz, A.; Burwinkel, B. Characterization of extracellular circulating microRNA. Nucleic Acids Res. 2011, 39, 7223–7233. [Google Scholar] [CrossRef]
- Li, Y.-L.; Xiao, Z.-S. Advances in Runx2 regulation and its isoforms. Med. Hypotheses 2007, 68, 169–175. [Google Scholar] [CrossRef]
- Cheng, V.K.F.; Au, P.C.M.; Tan, K.C.; Cheung, C.L. MicroRNA and human bone health. JBMR Plus 2019, 3, 2–13. [Google Scholar] [CrossRef]
- Carrozza, M.J.; Utley, R.T.; Workman, J.L.; Cote, J. The diverse functions of histone acetyltransferase complexes. TRENDS Genet. 2003, 19, 321–329. [Google Scholar] [CrossRef]
- Feng, J.; Fan, G. The role of DNA methylation in the central nervous system and neuropsychiatric disorders. Int. Rev. Neurobiol. 2009, 89, 67–84. [Google Scholar]
- Skalny, A.V.; Aschner, M.; Silina, E.V.; Stupin, V.A.; Zaitsev, O.N.; Sotnikova, T.I.; Tazina, S.I.; Zhang, F.; Guo, X.; Tinkov, A.A. The Role of Trace Elements and Minerals in Osteoporosis: A Review of Epidemiological and Laboratory Findings. Biomolecules 2023, 13, 1006. [Google Scholar] [CrossRef]
- Ferreira, T.J.; de Araújo, C.C.; Lima, A.C.d.S.; Matida, L.M.; Griebeler, A.F.M.; Coelho, A.S.G.; Gontijo, A.P.M.; Cominetti, C.; Vêncio, E.F.; Horst, M.A. Dietary intake is associated with miR-31 and miR-375 expression in patients with head and neck squamous cell carcinoma. Nutr. Cancer 2022, 74, 2049–2058. [Google Scholar] [CrossRef]
- Raisz, L.G. Pathogenesis of osteoporosis: Concepts, conflicts, and prospects. J. Clin. Investig. 2005, 115, 3318–3325. [Google Scholar] [CrossRef] [PubMed]
- Nilsson, S.; Makela, S.; Treuter, E.; Tujague, M.; Thomsen, J.; Andersson, G.R.; Enmark, E.; Pettersson, K.; Warner, M.; Gustafsson, J.-Å. Mechanisms of estrogen action. Physiol. Rev. 2001, 81, 1535–1565. [Google Scholar] [CrossRef] [PubMed]
- Sebastiani, G. Circulating Noncoding RNAs as Candidate Biomarkers of Endocrine and Metabolic Disease. Int. J. Endocrinol. 2018, 2018, 9514927. [Google Scholar] [CrossRef]
- EFSA Panel on Nutrition, Novel Foods and Food Allergens (NDA); Turck, D.; Bohn, T.; Castenmiller, J.; De Henauw, S.; Hirsch-Ernst, K.I.; Knutsen, H.K.; Maciuk, A.; Mangelsdorf, I.; McArdle, H.J.; et al. Guidance for establishing and applying tolerable upper intake levels for vitamins and essential minerals: Draft for internal testing. EFSA J. 2022, 20, e200102. [Google Scholar] [PubMed]
- Wu, J.; Liang, J.; Li, M.; Lin, M.; Mai, L.; Huang, X.; Liang, J.; Hu, Y.; Huang, Y. Modulation of miRNAs by vitamin C in H2O2-exposed human umbilical vein endothelial cells. Int. J. Mol. Med. 2020, 46, 2150–2160. [Google Scholar] [CrossRef] [PubMed]
- Ghafouri-Fard, S.; Abak, A.; Shoorei, H.; Mohaqiq, M.; Majidpoor, J.; Sayad, A.; Taheri, M. Regulatory role of microRNAs on PTEN signaling. Biomed. Pharmacother. 2021, 133, 110986. [Google Scholar] [CrossRef]
- Yang, L.; Li, C.; Liang, F.; Fan, Y.; Zhang, S. MiRNA-155 promotes proliferation by targeting caudal-type homeobox 1 (CDX1) in glioma cells. Biomed. Pharmacother. 2017, 95, 1759–1764. [Google Scholar] [CrossRef]
- Lai, Y.L.; Yamaguchi, M. Phytocomponent p-hydroxycinnamic acid stimulates bone formation and inhibits bone resorption in rat femoral tissues in vitro. Mol. Cell. Biochem. 2006, 292, 45–52. [Google Scholar] [CrossRef]
- Lai, Y.L.; Yamaguchi, M. Oral administration of phytocomponent p-hydroxycinnamic acid has anabolic effects on bone calcification in femoral tissues of rats in vivo. J. Health Sci. 2006, 52, 308–312. [Google Scholar] [CrossRef]
- Raut, N.; Wicks, S.M.; Lawal, T.O.; Mahady, G.B. Epigenetic regulation of bone remodeling by natural compounds. Pharmacol. Res. 2019, 147, 104350. [Google Scholar] [CrossRef]
- Hsu, Y.L.; Liang, H.L.; Hung, C.H.; Kuo, P.L. Syringetin, a flavonoid derivative in grape and wine, induces human osteoblast differentiation through bone morphogenetic protein-2/extracellular signal-regulated kinase 1/2 pathway. Mol. Nutr. Food Res. 2009, 53, 1452–1461. [Google Scholar] [CrossRef]
- Srinivasulu, C.; Ramgopal, M.; Ramanjaneyulu, G.; Anuradha, C.; Kumar, C.S. Syringic acid (SA)–A review of its occurrence, biosynthesis, pharmacological and industrial importance. Biomed. Pharmacother. 2018, 108, 547–557. [Google Scholar] [CrossRef] [PubMed]
- Yin, S.; Lin, S.; Xu, J.; Yang, G.; Chen, H.; Jiang, X. Dominoes with interlocking consequences triggered by zinc: Involvement of microelement-stimulated MSC-derived small extracellular vesicles in senile osteogenesis and osteoclast dialogue. Res. Sq. 2023. [Google Scholar] [CrossRef]
- Norouzi, Z.; Zarezadeh, R.; Mehdizadeh, A.; Niafar, M.; Germeyer, A.; Fayyazpour, P.; Fayezi, S. Free Fatty Acids from Type 2 Diabetes Mellitus Serum Remodel Mesenchymal Stem Cell Lipids, Hindering Differentiation into Primordial Germ Cells. Appl. Biochem. Biotechnol. 2023, 195, 3011–3026. [Google Scholar] [CrossRef] [PubMed]
- Gan, K.; Dong, G.-H.; Wang, N.; Zhu, J.-F. miR-221-3p and miR-222-3p downregulation promoted osteogenic differentiation of bone marrow mesenchyme stem cells through IGF-1/ERK pathway under high glucose condition. Diabetes Res. Clin. Pract. 2020, 167, 108121. [Google Scholar] [CrossRef]
- Qu, B.; Gong, K.; Yang, H.-S.; Li, Y.-G.; Jiang, T.; Zeng, Z.-M.; Cao, Z.-R.; Pan, X.-M. MiR-449 overexpression inhibits osteogenic differentiation of bone marrow mesenchymal stem cells via suppressing Sirt1/Fra-1 pathway in high glucose and free fatty acids microenvironment. Biochem. Biophys. Res. Commun. 2018, 496, 120–126. [Google Scholar] [CrossRef]
- Dong, Z.; Yang, C.; Tan, J.; Dou, C.; Chen, Y. Modulation of SIRT6 activity acts as an emerging therapeutic implication for pathological disorders in the skeletal system. Genes Dis. 2022, 10, 864–876. [Google Scholar] [CrossRef]
- Li, Y. Role of Neonatal Dietary Ca in Bone Development and Characteristics of Porcine Mesenchymal Stem Cells; North Carolina State University: Raleigh, NC, USA, 2014. [Google Scholar]
- Kanakis, I.; Alameddine, M.; Scalabrin, M.; van’t Hof, R.J.; Liloglou, T.; Ozanne, S.E.; Goljanek-Whysall, K.; Vasilaki, A. Low protein intake compromises the recovery of lactation-induced bone loss in female mouse dams without affecting skeletal muscles. FASEB J. 2020, 34, 11844–11859. [Google Scholar] [CrossRef]
- Proia, P.; Amato, A.; Drid, P.; Korovljev, D.; Vasto, S.; Baldassano, S. The impact of diet and physical activity on bone health in children and adolescents. Front. Endocrinol. 2021, 12, 704647. [Google Scholar] [CrossRef]
- Remer, T.; Manz, F. Estimation of the renal net acid excretion by adults consuming diets containing variable amounts of protein. Am. J. Clin. Nutr. 1994, 59, 1356–1361. [Google Scholar] [CrossRef]
- Baldassano, S.; Alioto, A.; Amato, A.; Rossi, C.; Messina, G.; Bruno, M.R.; Stallone, R.; Proia, P. Fighting the Consequences of the COVID-19 Pandemic: Mindfulness, Exercise, and Nutrition Practices to Reduce Eating Disorders and Promote Sustainability. Sustainability 2023, 15, 2120. [Google Scholar] [CrossRef]
- Conigrave, A.; Brown, E.; Rizzoli, R. Dietary protein and bone health: Roles of amino acid–sensing receptors in the control of calcium metabolism and bone homeostasis. Annu. Rev. Nutr. 2008, 28, 131–155. [Google Scholar] [CrossRef] [PubMed]
- Philip, A.; Ferro, V.A.; Tate, R.J. Determination of the potential bioavailability of plant microRNAs using a simulated human digestion process. Mol. Nutr. Food Res. 2015, 59, 1962–1972. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Y.; Dong, J.; Chen, J.; Pan, X. Evaluating the effect of food components on the digestion of dietary nucleic acids in human gastric juice in vitro. Food Sci. Nutr. 2023, 00, 1–10. [Google Scholar] [CrossRef]
- López de las Hazas, M.-C.; del Pozo-Acebo, L.; Hansen, M.S.; Gil-Zamorano, J.; Mantilla-Escalante, D.C.; Gómez-Coronado, D.; Marín, F.; Garcia-Ruiz, A.; Rasmussen, J.T.; Dávalos, A. Dietary bovine milk miRNAs transported in extracellular vesicles are partially stable during GI digestion, are bioavailable and reach target tissues but need a minimum dose to impact on gene expression. Eur. J. Nutr. 2022, 61, 1043–1056. [Google Scholar] [CrossRef] [PubMed]
- Saunders, M.A.; Liang, H.; Li, W.-H. Human polymorphism at microRNAs and microRNA target sites. Proc. Natl. Acad. Sci. USA 2007, 104, 3300–3305. [Google Scholar] [CrossRef]
- Singh, S.K.; Pal Bhadra, M.; Girschick, H.J.; Bhadra, U. MicroRNAs–micro in size but macro in function. FEBS J. 2008, 275, 4929–4944. [Google Scholar] [CrossRef]
- Baier, S.R.; Nguyen, C.; Xie, F.; Wood, J.R.; Zempleni, J. MicroRNAs are absorbed in biologically meaningful amounts from nutritionally relevant doses of cow milk and affect gene expression in peripheral blood mononuclear cells, HEK-293 kidney cell cultures, and mouse livers. J. Nutr. 2014, 144, 1495–1500. [Google Scholar] [CrossRef]
- Xie, W.; Melzig, M.F. The stability of medicinal plant microRNAs in the herb preparation process. Molecules 2018, 23, 919. [Google Scholar] [CrossRef]
- Askenase, P.W. Exosomes provide unappreciated carrier effects that assist transfers of their miRNAs to targeted cells; I. They are ‘The Elephant in the Room’. RNA Biol. 2021, 18, 2038–2053. [Google Scholar] [CrossRef]
- Rani, P.; Vashisht, M.; Golla, N.; Shandilya, S.; Onteru, S.K.; Singh, D. Milk miRNAs encapsulated in exosomes are stable to human digestion and permeable to intestinal barrier in vitro. J. Funct. Foods 2017, 34, 431–439. [Google Scholar] [CrossRef]
- Horne, R.; St. Pierre, J.; Odeh, S.; Surette, M.; Foster, J.A. Microbe and host interaction in gastrointestinal homeostasis. Psychopharmacology 2019, 236, 1623–1640. [Google Scholar] [CrossRef] [PubMed]
- Peck, B.C.; Mah, A.T.; Pitman, W.A.; Ding, S.; Lund, P.K.; Sethupathy, P. Functional transcriptomics in diverse intestinal epithelial cell types reveals robust microRNA sensitivity in intestinal stem cells to microbial status. J. Biol. Chem. 2017, 292, 2586–2600. [Google Scholar] [CrossRef]
- Liang, G.; Zhu, Y.; Sun, B.; Shao, Y.; Jing, A.; Wang, J.; Xiao, Z. Assessing the survival of exogenous plant microRNA in mice. Food Sci. Nutr. 2014, 2, 380–388. [Google Scholar] [CrossRef] [PubMed]
- Chen, X.; Zhou, Y.; Yu, J. Exosome-like nanoparticles from ginger rhizomes inhibited NLRP3 inflammasome activation. Mol. Pharm. 2019, 16, 2690–2699. [Google Scholar] [CrossRef] [PubMed]
- Cao, M.; Yan, H.; Han, X.; Weng, L.; Wei, Q.; Sun, X.; Lu, W.; Wei, Q.; Ye, J.; Cai, X. Ginseng-derived nanoparticles alter macrophage polarization to inhibit melanoma growth. J. Immunother. Cancer 2019, 7, 326. [Google Scholar] [CrossRef]
- Kim, H.; Wang, S.Y.; Kwak, G.; Yang, Y.; Kwon, I.C.; Kim, S.H. Exosome-guided phenotypic switch of M1 to M2 macrophages for cutaneous wound healing. Adv. Sci. 2019, 6, 1900513. [Google Scholar] [CrossRef]
- Zhao, Q.; Mao, Q.; Zhao, Z.; Dou, T.; Wang, Z.; Cui, X.; Liu, Y.; Fan, X. Prediction of plant-derived xenomiRs from plant miRNA sequences using random forest and one-dimensional convolutional neural network models. BMC Genom. 2018, 19, 839. [Google Scholar] [CrossRef]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Proia, P.; Rossi, C.; Alioto, A.; Amato, A.; Polizzotto, C.; Pagliaro, A.; Kuliś, S.; Baldassano, S. MiRNAs Expression Modulates Osteogenesis in Response to Exercise and Nutrition. Genes 2023, 14, 1667. https://doi.org/10.3390/genes14091667
Proia P, Rossi C, Alioto A, Amato A, Polizzotto C, Pagliaro A, Kuliś S, Baldassano S. MiRNAs Expression Modulates Osteogenesis in Response to Exercise and Nutrition. Genes. 2023; 14(9):1667. https://doi.org/10.3390/genes14091667
Chicago/Turabian StyleProia, Patrizia, Carlo Rossi, Anna Alioto, Alessandra Amato, Caterina Polizzotto, Andrea Pagliaro, Szymon Kuliś, and Sara Baldassano. 2023. "MiRNAs Expression Modulates Osteogenesis in Response to Exercise and Nutrition" Genes 14, no. 9: 1667. https://doi.org/10.3390/genes14091667