CoChat
Sign Up
Cited by 9Bone Metabolism and DiseasesBone health and osteoporosis researchMicroRNA in disease regulation

Focusing on OB-OC-MΦ Axis and miR-23a to Explore the Pathogenesis and Treatment Strategy of Osteoporosis

Open access
Ma, Tian-Liang, Zhu, Peng, Ke, Zhuo-Ran, Chen, Jing-Xian, Hu, Yi-He, Xie, Jie·2022·Frontiers in Endocrinology
DOI 10.3389/fendo.2022.891313PMC PMC9329542
Open this paper in CoChat — free accountOpen PDF

Abstract

Osteoporosis is a bone metabolic disorder characterized by decreased bone density and deteriorated microstructure, which increases the risk of fractures. The imbalance between bone formation and bone resorption results in the occurrence and progression of osteoporosis. Osteoblast-mediated bone formation, osteoclast-mediated bone resorption and macrophage-regulated inflammatory response play a central role in the process of bone remodeling, which together maintain the balance of the osteoblast-osteoclast-macrophage (OB-OC-MΦ) axis under physiological conditions. Bone formation and bone resorption disorders caused by the imbalance of OB-OC-MΦ axis contribute to osteoporosis. Many microRNAs are involved in the regulation of OB-OC-MΦ axis homeostasis, with microRNA-23a (miR-23a) being particularly crucial. MiR-23a is highly expressed in the pathological process of osteoporosis, which eventually leads to the occurrence and further progression of osteoporosis by inhibiting osteogenesis, promoting bone resorption and inflammatory polarization of macrophages. This review focuses on the role and mechanism of miR-23a in regulating the OB-OC-MΦ axis to provide new clinical strategies for the prevention and treatment of osteoporosis.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3389/fendo.2022.891313

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Clinical analysis between osteoporosis patients and healthy controls revealed that overexpression of miR-23 can significantly reduce expression levels of markers related to osteoblasts.

    “clinical analysis between osteoporosis patients and healthy controls revealed that overexpression of miR-23 can significantly reduce the expression levels of markers related to osteoblasts.”

    From Recent advances of miR-23 in human diseases and growth development (2025) · cites this paper as [116]

    Section 3.1 (page unavailable) reports that miR-23a inhibits osteogenic differentiation by targeting factors including Runx2, supporting the general inhibitory effect on osteoblast-related factors. The paper does not report the claimed clinical comparison between osteoporosis patients and healthy controls or a statistically significant reduction in osteoblast-marker expression from that analysis. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

The citation lists haven’t been fetched yet

References 141 · Cited by 9

Research works printed but not linked: 137

  1. [1]Lane NE. Epidemiology, Etiology, and Diagnosis of Osteoporosis. Am J Obstet Gynecol (2006) 194(2 Suppl): S3– 11. doi: 10.1016/j.ajog.2005.08.047 16448873 · DOI
  2. [2]Chen S Liu D Zhou Z Qin S. Role of Long Non-Coding RNA H19 in the Development of Osteoporosis. Mol Med (2021) 27(1): 122. doi: 10.1186/s10020-021-00386-0 34583640 PMC8480040 · DOI
  3. [3]Singer A Exuzides A Spangler L O'Malley C Colby C Johnston K. Burden of Illness for Osteoporotic Fractures Compared With Other Serious Diseases Among Postmenopausal Women in the United States. Mayo Clin Proc (2015) 90(1): 53– 62. doi: 10.1016/j.mayocp.2014.09.011 25481833 · DOI
  4. [4]Watts NB. Insights From the Global Longitudinal Study of Osteoporosis in Women (GLOW). Nat Rev Endocrinol (2014) 10(7): 412–22. doi: 10.1038/nrendo.2014.55 24751880 · DOI
  5. [5]Tella SH Gallagher JC. Prevention and Treatment of Postmenopausal Osteoporosis. J Steroid Biochem Mol Biol (2014) 142: 155–70. doi: 10.1016/j.jsbmb.2013.09.008 PMC4187361 24176761 · DOI · Paper page
  6. [6]Trajanoska K Rivadeneira F. The Genetic Architecture of Osteoporosis and Fracture Risk. Bone (2019) 126: 2–10. doi: 10.1016/j.bone.2019.04.005 30980960 · DOI
  7. [7]Souza PPC Lerner UH. The Role of Cytokines in Inflammatory Bone Loss. Immunol Invest (2013) 42(7): 555– 622. doi: 10.3109/08820139.2013.822766 24004059 · DOI
  8. [8]Kim JH Jin HM Kim K Song I Youn BU Matsuo K. The Mechanism of Osteoclast Differentiation Induced by IL-1. J Immunol (2009) 183(3): 1862–70. doi: 10.4049/jimmunol.0803007 19587010 · DOI
  9. [9]Yang D-H Yang M-Y. The Role of Macrophage in the Pathogenesis of Osteoporosis. Int J Mol Sci (2019) 20(9): 2093. doi: 10.3390/ijms20092093 PMC6539137 31035384 · DOI
  10. [10]Rupaimoole R Slack FJ. MicroRNA Therapeutics: Towards a New Era for the Management of Cancer and Other Diseases. Nat Rev Drug Discov (2017) 16(3): 203–22. doi: 10.1038/nrd.2016.246 28209991 · DOI · Paper page
  11. [11]Ha M Kim VN. Regulation of microRNA Biogenesis. Nat Rev Mol Cell Biol (2014) 15(8): 509–24. doi: 10.1038/nrm3838 25027649 · DOI · Paper page
  12. [12]Kim DK Bandara G Cho YE Komarow HD Donahue DR Karim B. Mastocytosis-Derived Extracellular Vesicles Deliver miR-23a and miR-30a Into Pre-Osteoblasts and Prevent Osteoblastogenesis and Bone Formation. Nat Commun (2021) 12(1): 2527. doi: 10.1038/s41467-021-22754-4 33953168 PMC8100305 · DOI
  13. [13]Yang J-X Xie P Li Y-S Wen T Yang X-C. Osteoclast-Derived miR-23a-5p-Containing Exosomes Inhibit Osteogenic Differentiation by Regulating Runx2. Cell Signal (2020) 70: 109504. doi: 10.1016/j.cellsig.2019.109504 31857240 · DOI
  14. [14]Luers AJ Loudig OD Berman JW. MicroRNAs Are Expressed and Processed by Human Primary Macrophages. Cell Immunol (2010) 263(1): 1– 8. doi: 10.1016/j.cellimm.2010.03.011 20403586 PMC2906247 · DOI
  15. [15]Ma S Liu M Xu Z Li Y Guo H Ge Y. A Double Feedback Loop Mediated by microRNA-23a/27a/24-2 Regulates M1 Versus M2 Macrophage Polarization and Thus Regulates Cancer Progression. Oncotarget (2016) 7(12): 13502–19. doi: 10.18632/oncotarget.6284 PMC4924657 26540574 · DOI
  16. [16]Florencio-Silva R Sasso GR Sasso-Cerri E Simões MJ Cerri PS. Biology of Bone Tissue: Structure, Function, and Factors That Influence Bone Cells. BioMed Res Int (2015) 2015: 421746. doi: 10.1155/2015/421746 26247020 PMC4515490 · DOI · Paper page
  17. [17]Sims NA Gooi JH. Bone Remodeling: Multiple Cellular Interactions Required for Coupling of Bone Formation and Resorption. Semin Cell Dev Biol (2008) 19(5): 444–51. doi: 10.1016/j.semcdb.2008.07.016 18718546 · DOI · Paper page
  18. [18]Katsimbri P. The Biology of Normal Bone Remodelling. Eur J Cancer Care (Engl) (2017) 26(6): 10.1111/ecc.12740. doi: 10.1111/ecc.12740 28786518 · DOI
  19. [19]Raggatt LJ Partridge NC. Cellular and Molecular Mechanisms of Bone Remodeling. J Biol Chem (2010) 285(33): 25103–8. doi: 10.1074/jbc.R109.041087 PMC2919071 20501658 · DOI · Paper page
  20. [20]Capulli M Paone R Rucci N. Osteoblast and Osteocyte: Games Without Frontiers. Arch Biochem Biophys (2014) 561: 3– 12. doi: 10.1016/j.abb.2014.05.003 24832390 · DOI · Paper page
  21. [21]Boyle WJ Simonet WS Lacey DL. Osteoclast Differentiation and Activation. Nature (2003) 423(6937): 337–42. doi: 10.1038/nature01658 12748652 · DOI · Paper page
  22. [22]Matsuura T Ichinose S Akiyama M Kasahara Y Tachikawa N Nakahama KI. Involvement of CX3CL1 in the Migration of Osteoclast Precursors Across Osteoblast Layer Stimulated by Interleukin-1ß. J Cell Physiol (2017) 232(7): 1739–45. doi: 10.1002/jcp.25577 27579490 · DOI
  23. [23]Faulkner B Astleford K Mansky KC. Regulation of Osteoclast Differentiation and Skeletal Maintenance by Histone Deacetylases. Molecules (2019) 24(7): 1355. doi: 10.3390/molecules24071355 PMC6479495 30959867 · DOI
  24. [24]Fujii T Murata K Mun SH Bae S Lee YJ Pannellini T. MEF2C Regulates Osteoclastogenesis and Pathologic Bone Resorption via C-FOS. Bone Res (2021) 9(1): 4. doi: 10.1038/s41413-020-00120-2 33424022 PMC7797478 · DOI
  25. [25]Muthukuru M Darveau RP. TLR Signaling That Induces Weak Inflammatory Response and SHIP1 Enhances Osteogenic Functions. Bone Res (2014) 2: 14031. doi: 10.1038/boneres.2014.31 26273527 PMC4472124 · DOI
  26. [26]Michalski MN McCauley LK. Macrophages and Skeletal Health. Pharmacol Ther (2017) 174: 43– 54. doi: 10.1016/j.pharmthera.2017.02.017 28185913 PMC5429177 · DOI
  27. [27]Shapouri-Moghaddam A Mohammadian S Vazini H Taghadosi M Esmaeili SA Mardani F. Macrophage Plasticity, Polarization, and Function in Health and Disease. J Cell Physiol (2018) 233(9): 6425–40. doi: 10.1002/jcp.26429 PMC13482560 29319160 · DOI · Paper page
  28. [28]Liu H Wu X Gang N Wang S Deng W Zan L. Macrophage Functional Phenotype Can Be Consecutively and Reversibly Shifted to Adapt to Microenvironmental Changes. Int J Clin Exp Med (2015) 8(2): 3044–53. PMC4402928 25932281
  29. [29]Pieters BCH Cappariello A van den Bosch MHJ van Lent P Teti A van de Loo FAJ. Macrophage-Derived Extracellular Vesicles as Carriers of Alarmins and Their Potential Involvement in Bone Homeostasis. Front Immunol (2019) 10: 1901. doi: 10.3389/fimmu.2019.01901 31440259 PMC6694442 · DOI
  30. [30]Muñoz J Akhavan NS Mullins AP Arjmandi BH. Macrophage Polarization and Osteoporosis: A Review. Nutrients (2020) 12(10): 2999. doi: 10.3390/nu12102999 PMC7601854 33007863 · DOI
  31. [31]Kim JH Kim N. Signaling Pathways in Osteoclast Differentiation. Chonnam Med J (2016) 52(1): 12–7. doi: 10.4068/cmj.2016.52.1.12 PMC4742606 26865996 · DOI
  32. [32]Wiktor-Jedrzejczak W Bartocci A Ferrante AW Jr. Ahmed-Ansari A Sell KW Pollard JW. Total Absence of Colony-Stimulating Factor 1 in the Macrophage-Deficient Osteopetrotic (Op/Op) Mouse. Proc Natl Acad Sci U S A (1990) 87(12): 4828–32. doi: 10.1073/pnas.87.12.4828 PMC54211 2191302 · DOI · Paper page
  33. [33]Ono T Hayashi M Sasaki F Nakashima T. RANKL Biology: Bone Metabolism, the Immune System, and Beyond. Inflammation Regen (2020) 40: 2. doi: 10.1186/s41232-019-0111-3 PMC7006158 32047573 · DOI
  34. [34]Udagawa N Koide M Nakamura M Nakamichi Y Yamashita T Uehara S. Osteoclast Differentiation by RANKL and OPG Signaling Pathways. J Bone Miner Metab (2021) 39(1): 19– 26. doi: 10.1007/s00774-020-01162-6 33079279 · DOI
  35. [35]Theoleyre S Wittrant Y Tat SK Fortun Y Redini F Heymann D. The Molecular Triad OPG/RANK/RANKL: Involvement in the Orchestration of Pathophysiological Bone Remodeling. Cytokine Growth Factor Rev (2004) 15(6): 457–75. doi: 10.1016/j.cytogfr.2004.06.004 15561602 · DOI · Paper page
  36. [36]Kim JM Lin C Stavre Z Greenblatt MB Shim JH. Osteoblast-Osteoclast Communication and Bone Homeostasis. Cells (2020) 9(9): 2073. doi: 10.3390/cells9092073 PMC7564526 32927921 · DOI
  37. [37]Maeda K Kobayashi Y Udagawa N Uehara S Ishihara A Mizoguchi T. Wnt5a-Ror2 Signaling Between Osteoblast-Lineage Cells and Osteoclast Precursors Enhances Osteoclastogenesis. Nat Med (2012) 18(3): 405–12. doi: 10.1038/nm.2653 22344299 · DOI · Paper page
  38. [38]Han Y You X Xing W Zhang Z Zou W. Paracrine and Endocrine Actions of Bone-the Functions of Secretory Proteins From Osteoblasts, Osteocytes, and Osteoclasts. Bone Res (2018) 6: 16. doi: 10.1038/s41413-018-0019-6 29844945 PMC5967329 · DOI
  39. [39]Kreja L Brenner RE Tautzenberger A Liedert A Friemert B Ehrnthaller C. Non-Resorbing Osteoclasts Induce Migration and Osteogenic Differentiation of Mesenchymal Stem Cells. J Cell Biochem (2010) 109(2): 347–55. doi: 10.1002/jcb.22406 19950208 · DOI
  40. [40]Negishi-Koga T Shinohara M Komatsu N Bito H Kodama T Friedel RH. Suppression of Bone Formation by Osteoclastic Expression of Semaphorin 4D. Nat Med (2011) 17(11): 1473–80. doi: 10.1038/nm.2489 22019888 · DOI · Paper page
  41. [41]Kobayashi K Takahashi N Jimi E Udagawa N Takami M Kotake S. Tumor Necrosis Factor Alpha Stimulates Osteoclast Differentiation by a Mechanism Independent of the ODF/RANKL-RANK Interaction. J Exp Med (2000) 191(2): 275–86. doi: 10.1084/jem.191.2.275 PMC2195746 10637272 · DOI
  42. [42]Zhao Z Hou X Yin X Li Y Duan R Boyce BF. TNF Induction of NF-κb RelB Enhances RANKL-Induced Osteoclastogenesis by Promoting Inflammatory Macrophage Differentiation But Also Limits It Through Suppression of NFATc1 Expression. PloS One (2015) 10(8): e0135728. doi: 10.1371/journal.pone.0135728 26287732 PMC4545392 · DOI
  43. [43]Horwood NJ Elliott J Martin TJ Gillespie MT. Osteotropic Agents Regulate the Expression of Osteoclast Differentiation Factor and Osteoprotegerin in Osteoblastic Stromal Cells. Endocrinology (1998) 139(11): 4743–6. doi: 10.1210/endo.139.11.6433 9794488 · DOI
  44. [44]Hofbauer LC Lacey DL Dunstan CR Spelsberg TC Riggs BL Khosla S. Interleukin-1beta and Tumor Necrosis Factor-Alpha, But Not Interleukin-6, Stimulate Osteoprotegerin Ligand Gene Expression in Human Osteoblastic Cells. Bone (1999) 25(3): 255–9. doi: 10.1016/S8756-3282(99)00162-3 10495128 · DOI
  45. [45]O'Brien CA Nakashima T Takayanagi H. Osteocyte Control of Osteoclastogenesis. Bone (2013) 54(2): 258–63. doi: 10.1016/j.bone.2012.08.121 PMC3538915 22939943 · DOI
  46. [46]Wu Q Zhou X Huang D Ji Y Kang F. IL-6 Enhances Osteocyte-Mediated Osteoclastogenesis by Promoting JAK2 and RANKL Activity In Vitro. Cell Physiol Biochem (2017) 41(4): 1360–9. doi: 10.1159/000465455 28278513 · DOI
  47. [47]Devlin RD Reddy SV Savino R Ciliberto G Roodman GD. IL-6 Mediates the Effects of IL-1 or TNF, But Not PTHrP or 1,25(OH)2D3, on Osteoclast-Like Cell Formation in Normal Human Bone Marrow Cultures. J Bone Miner Res (1998) 13(3): 393–9. doi: 10.1359/jbmr.1998.13.3.393 9525339 · DOI
  48. [48]Sun Y Li J Xie X Gu F Sui Z Zhang K. Macrophage-Osteoclast Associations: Origin, Polarization, and Subgroups. Front Immunol (2021) 12: 778078. doi: 10.3389/fimmu.2021.778078 34925351 PMC8672114 · DOI
  49. [49]Horwood NJ Elliott J Martin TJ Gillespie MT. IL-12 Alone and in Synergy With IL-18 Inhibits Osteoclast Formation In Vitro. J Immunol (2001) 166(8): 4915–21. doi: 10.4049/jimmunol.166.8.4915 11290769 · DOI
  50. [50]Evans KE Fox SW. Interleukin-10 Inhibits Osteoclastogenesis by Reducing NFATc1 Expression and Preventing Its Translocation to the Nucleus. BMC Cell Biol (2007) 8: 4. doi: 10.1186/1471-2121-8-4 17239241 PMC1781937 · DOI
  51. [51]Liu D Yao S Wise GE. Effect of Interleukin-10 on Gene Expression of Osteoclastogenic Regulatory Molecules in the Rat Dental Follicle. Eur J Oral Sci (2006) 114(1): 42–9. doi: 10.1111/j.1600-0722.2006.00283.x 16460340 · DOI
  52. [52]Houri-Haddad Y Soskolne WA Halabi A Shapira L. IL-10 Gene Transfer Attenuates P. Gingivalis-Induced Inflammation. J Dent Res (2007) 86(6): 560–4. doi: 10.1177/154405910708600614 17525358 · DOI
  53. [53]Icer MA Gezmen-Karadag M. The Multiple Functions and Mechanisms of Osteopontin. Clin Biochem (2018) 59: 17– 24. doi: 10.1016/j.clinbiochem.2018.07.003 30003880 · DOI · Paper page
  54. [54]Horwood NJ. Macrophage Polarization and Bone Formation: A Review. Clin Rev Allergy Immunol (2016) 51(1): 79– 86. doi: 10.1007/s12016-015-8519-2 26498771 · DOI
  55. [55]Walker EC McGregor NE Poulton IJ Solano M Pompolo S Fernandes TJ. Oncostatin M Promotes Bone Formation Independently of Resorption When Signaling Through Leukemia Inhibitory Factor Receptor in Mice. J Clin Invest (2010) 120(2): 582–92. doi: 10.1172/JCI40568 PMC2810087 20051625 · DOI
  56. [56]Matsuo K Irie N. Osteoclast-Osteoblast Communication. Arch Biochem Biophys (2008) 473(2): 201–9. doi: 10.1016/j.abb.2008.03.027 18406338 · DOI · Paper page
  57. [57]Yang D Wan Y. Molecular Determinants for the Polarization of Macrophage and Osteoclast. Semin Immunopathol (2019) 41(5): 551–63. doi: 10.1007/s00281-019-00754-3 PMC6815265 31506868 · DOI
  58. [58]Tanaka K Yamagata K Kubo S Nakayamada S Sakata K Matsui T. Glycolaldehyde-Modified Advanced Glycation End-Products Inhibit Differentiation of Human Monocytes Into Osteoclasts via Upregulation of IL-10. Bone (2019) 128: 115034. doi: 10.1016/j.bone.2019.115034 31421252 · DOI
  59. [59]Mandal CC Ghosh Choudhury G Ghosh-Choudhury N. Phosphatidylinositol 3 Kinase/Akt Signal Relay Cooperates With Smad in Bone Morphogenetic Protein-2-Induced Colony Stimulating Factor-1 (CSF-1) Expression and Osteoclast Differentiation. Endocrinology (2009) 150(11): 4989–98. doi: 10.1210/en.2009-0026 PMC2775973 19819979 · DOI
  60. [60]Alexander KA Chang MK Maylin ER Kohler T Müller R Wu AC. Osteal Macrophages Promote In Vivo Intramembranous Bone Healing in a Mouse Tibial Injury Model. J Bone Miner Res (2011) 26(7): 1517–32. doi: 10.1002/jbmr.354 21305607 · DOI · Paper page
  61. [61]Chan JK Glass GE Ersek A Freidin A Williams GA Gowers K. Low-Dose TNF Augments Fracture Healing in Normal and Osteoporotic Bone by Up-Regulating the Innate Immune Response. EMBO Mol Med (2015) 7(5): 547–61. doi: 10.15252/emmm.201404487 PMC4492816 25770819 · DOI
  62. [62]Nicolaidou V Wong MM Redpath AN Ersek A Baban DF Williams LM. Monocytes Induce STAT3 Activation in Human Mesenchymal Stem Cells to Promote Osteoblast Formation. PloS One (2012) 7(7): e39871. doi: 10.1371/journal.pone.0039871 22802946 PMC3389003 · DOI
  63. [63]Kim J Hematti P. Mesenchymal Stem Cell-Educated Macrophages: A Novel Type of Alternatively Activated Macrophages. Exp Hematol (2009) 37(12): 1445–53. doi: 10.1016/j.exphem.2009.09.004 PMC2783735 19772890 · DOI · Paper page
  64. [64]Maggini J Mirkin G Bognanni I Holmberg J Piazzón IM Nepomnaschy I. Mouse Bone Marrow-Derived Mesenchymal Stromal Cells Turn Activated Macrophages Into a Regulatory-Like Profile. PloS One (2010) 5(2): e9252. doi: 10.1371/journal.pone.0009252 20169081 PMC2821929 · DOI
  65. [65]Zha L He L Liang Y Qin H Yu B Chang L. TNF-α Contributes to Postmenopausal Osteoporosis by Synergistically Promoting RANKL-Induced Osteoclast Formation. BioMed Pharmacother (2018) 102: 369–74. doi: 10.1016/j.biopha.2018.03.080 29571022 · DOI
  66. [66]Llorente I García-Castañeda N Valero C González-Álvaro I Castañeda S. Osteoporosis in Rheumatoid Arthritis: Dangerous Liaisons. Front Med (Lausanne) (2020) 7: 601618. doi: 10.3389/fmed.2020.601618 33330566 PMC7719815 · DOI
  67. [67]Mihara M Hashizume M Yoshida H Suzuki M Shiina M. IL-6/IL-6 Receptor System and Its Role in Physiological and Pathological Conditions. Clin Sci (Lond) (2012) 122(4): 143–59. doi: 10.1042/CS20110340 22029668 · DOI
  68. [68]Leng SX Elias JA. Interleukin-11. Int J Biochem Cell Biol (1997) 29(8-9): 1059–62. doi: 10.1016/S1357-2725(97)00017-4 9416001 · DOI
  69. [69]Udagawa N Takahashi N Katagiri T Tamura T Wada S Findlay DM. Interleukin (IL)-6 Induction of Osteoclast Differentiation Depends on IL-6 Receptors Expressed on Osteoblastic Cells But Not on Osteoclast Progenitors. J Exp Med (1995) 182(5): 1461–8. doi: 10.1084/jem.182.5.1461 PMC2192181 7595216 · DOI
  70. [70]Gao Y Morita I Maruo N Kubota T Murota S Aso T. Expression of IL-6 Receptor and GP130 in Mouse Bone Marrow Cells During Osteoclast Differentiation. Bone (1998) 22(5): 487–93. doi: 10.1016/S8756-3282(98)00040-4 9600782 · DOI
  71. [71]Schmidt-Arras D Rose-John S. Endosomes as Signaling Platforms for IL-6 Family Cytokine Receptors. Front Cell Dev Biol (2021) 9: 688314. doi: 10.3389/fcell.2021.688314 34141712 PMC8204807 · DOI
  72. [72]Sims NA. Cell-Specific Paracrine Actions of IL-6 Family Cytokines From Bone, Marrow and Muscle That Control Bone Formation and Resorption. Int J Biochem Cell Biol (2016) 79: 14– 23. doi: 10.1016/j.biocel.2016.08.003 27497989 · DOI
  73. [74]Rachner TD Khosla S Hofbauer LC. Osteoporosis: Now and the Future. Lancet (2011) 377(9773): 1276–87. doi: 10.1016/S0140-6736(10)62349-5 PMC3555696 21450337 · DOI · Paper page
  74. [75]Mundy GR. Osteoporosis and Inflammation. Nutr Rev (2007) 65(12 Pt 2): S147–51. doi: 10.1111/j.1753-4887.2007.tb00353.x 18240539 · DOI
  75. [76]Raehtz S Bierhalter H Schoenherr D Parameswaran N McCabe LR. Estrogen Deficiency Exacerbates Type 1 Diabetes-Induced Bone TNF-α Expression and Osteoporosis in Female Mice. Endocrinology (2017) 158(7): 2086–101. doi: 10.1210/en.2016-1821 PMC5505215 28419209 · DOI
  76. [77]Yin Y Chen G Gong L Ge K Pan W Li N. DNAzyme-Powered Three-Dimensional DNA Walker Nanoprobe for Detection Amyloid Beta-Peptide Oligomer in Living Cells and In Vivo. Anal Chem (2020) 92(13): 9247–56. doi: 10.1021/acs.analchem.0c01592 32536153 · DOI
  77. [78]Qu Z Yang F Hong J Wang W Yan S. Parathyroid Hormone and Bone Mineral Density: A Mendelian Randomization Study. J Clin Endocrinol Metab (2020) 105(11): dgaa579. doi: 10.1210/clinem/dgaa579 32827441 · DOI
  78. [79]Huang JC Sakata T Pfleger LL Bencsik M Halloran BP Bikle DD. PTH Differentially Regulates Expression of RANKL and OPG. J Bone Miner Res (2004) 19(2): 235–44. doi: 10.1359/JBMR.0301226 14969393 · DOI
  79. [80]Silva BC Bilezikian JP. Parathyroid Hormone: Anabolic and Catabolic Actions on the Skeleton. Curr Opin Pharmacol (2015) 22: 41– 50. doi: 10.1016/j.coph.2015.03.005 25854704 PMC5407089 · DOI
  80. [81]O'Brien CA Jilka RL Fu Q Stewart S Weinstein RS Manolagas SC. IL-6 is Not Required for Parathyroid Hormone Stimulation of RANKL Expression, Osteoclast Formation, and Bone Loss in Mice. Am J Physiol Endocrinol Metab (2005) 289(5): E784–93. doi: 10.1152/ajpendo.00029.2005 15956054 · DOI
  81. [82]Neale Weitzmann M Pacifici R. Parathyroid Diseases and T Cells. Curr Osteoporos Rep (2017) 15(3): 135–41. doi: 10.1007/s11914-017-0359-y PMC5598774 28421466 · DOI
  82. [83]Parfitt AM. The Actions of Parathyroid Hormone on Bone: Relation to Bone Remodeling and Turnover, Calcium Homeostasis, and Metabolic Bone Diseases. II. PTH and Bone Cells: Bone Turnover and Plasma Calcium Regulation. Metabolism (1976) 25(8): 909–55. doi: 10.1016/0026-0495(76)90124-4 181659 · DOI
  83. [84]Strege DW Kahn AJ Jeffrey JJ Partridge NC. Stimulation of Collagenase Production by Rat Osteosarcoma Cells Can Occur in a Subpopulation of Cells. J Bone Miner Res (1990) 5(9): 963–71. doi: 10.1002/jbmr.5650050910 2177954 · DOI
  84. [85]Witty JP Foster SA Stricklin GP Matrisian LM Stern PH. Parathyroid Hormone-Induced Resorption in Fetal Rat Limb Bones Is Associated With Production of the Metalloproteinases Collagenase and Gelatinase B. J Bone Miner Res (1996) 11(1): 72–8. doi: 10.1002/jbmr.5650110111 8770699 · DOI
  85. [86]Vandewalle J Luypaert A De Bosscher K Libert C. Therapeutic Mechanisms of Glucocorticoids. Trends Endocrinol Metab (2018) 29(1): 42– 54. doi: 10.1016/j.tem.2017.10.010 29162310 · DOI
  86. [87]Chotiyarnwong P McCloskey EV. Pathogenesis of Glucocorticoid-Induced Osteoporosis and Options for Treatment. Nat Rev Endocrinol (2020) 16(8): 437–47. doi: 10.1038/s41574-020-0341-0 32286516 · DOI · Paper page
  87. [88]Canalis E. Mechanisms of Glucocorticoid Action in Bone. Curr Osteoporos Rep (2005) 3(3): 98– 102. doi: 10.1007/s11914-005-0017-7 16131429 · DOI
  88. [89]Canalis E Mazziotti G Giustina A Bilezikian JP. Glucocorticoid-Induced Osteoporosis: Pathophysiology and Therapy. Osteoporos Int (2007) 18(10): 1319–28. doi: 10.1007/s00198-007-0394-0 17566815 · DOI
  89. [90]Weinstein RS Chen JR Powers CC Stewart SA Landes RD Bellido T. Promotion of Osteoclast Survival and Antagonism of Bisphosphonate-Induced Osteoclast Apoptosis by Glucocorticoids. J Clin Invest (2002) 109(8): 1041–8. doi: 10.1172/JCI0214538 PMC150947 11956241 · DOI
  90. [91]Zhu S Yao F Qiu H Zhang G Xu H Xu J. Coupling Factors and Exosomal Packaging microRNAs Involved in the Regulation of Bone Remodelling. Biol Rev Camb Philos Soc (2018) 93(1): 469–80. doi: 10.1111/brv.12353 28795526 · DOI
  91. [92]Sun W Zhao C Li Y Wang L Nie G Peng J. Osteoclast-Derived microRNA-Containing Exosomes Selectively Inhibit Osteoblast Activity. Cell Discov (2016) 2: 16015. doi: 10.1038/celldisc.2016.15 27462462 PMC4886818 · DOI
  92. [93]Wang X Guo B Li Q Peng J Yang Z Wang A. miR-214 Targets ATF4 to Inhibit Bone Formation. Nat Med (2013) 19(1): 93– 100. doi: 10.1038/nm.3026 23223004 · DOI
  93. [94]Li D Liu J Guo B Liang C Dang L Lu C. Osteoclast-Derived Exosomal miR-214-3p Inhibits Osteoblastic Bone Formation. Nat Commun (2016) 7: 10872. doi: 10.1038/ncomms10872 26947250 PMC4786676 · DOI · Paper page
  94. [95]Zhao C Sun W Zhang P Ling S Li Y Zhao D. miR-214 Promotes Osteoclastogenesis by Targeting Pten/PI3k/Akt Pathway. RNA Biol (2015) 12(3): 343–53. doi: 10.1080/15476286.2015.1017205 PMC4615895 25826666 · DOI
  95. [96]Chen C Cheng P Xie H Zhou HD Wu XP Liao EY. MiR-503 Regulates Osteoclastogenesis via Targeting RANK. J Bone Miner Res (2014) 29(2): 338–47. doi: 10.1002/jbmr.2032 23821519 · DOI
  96. [97]Hassan MQ Gordon JA Beloti MM Croce CM van Wijnen AJ Stein JL. A Network Connecting Runx2, SATB2, and the miR-23a~27a~24-2 Cluster Regulates the Osteoblast Differentiation Program. Proc Natl Acad Sci USA (2010) 107(46): 19879–84. doi: 10.1073/pnas.1007698107 PMC2993380 20980664 · DOI
  97. [98]Tian F Ji XL Xiao WA Wang B Wang F. CXCL13 Promotes Osteogenic Differentiation of Mesenchymal Stem Cells by Inhibiting miR-23a Expression. Stem Cells Int (2015) 2015: 632305. doi: 10.1155/2015/632305 25784941 PMC4345275 · DOI
  98. [99]Komori T. Regulation of Bone Development and Maintenance by Runx2. Front Biosci (2008) 13: 898– 903. doi: 10.2741/2730 17981598 · DOI
  99. [100]Ma Y Gao J Guo H. miR-23a-3p Regulates Runx2 to Inhibit the Proliferation and Metastasis of Oral Squamous Cell Carcinoma. J Oncol (2022) 2022: 8719542. doi: 10.1155/2022/8719542 35342401 PMC8956426 · DOI · Paper page
  100. [101]Hodges WM O'Brien F Fulzele S Hamrick MW. Function of microRNAs in the Osteogenic Differentiation and Therapeutic Application of Adipose-Derived Stem Cells (ASCs). Int J Mol Sci (2017) 18(12): 2597. doi: 10.3390/ijms18122597 PMC5751200 29207475 · DOI
  101. [103]Xu Y Jiang Y Jia B Wang Y Li T. Icariin Stimulates Osteogenesis and Suppresses Adipogenesis of Human Bone Mesenchymal Stem Cells via miR-23a-Mediated Activation of the Wnt/β-Catenin Signaling Pathway. Phytomedicine (2021) 85: 153485. doi: 10.1016/j.phymed.2021.153485 33743412 · DOI
  102. [104]Li T Li H Wang Y Li T Fan J Xiao K. microRNA-23a Inhibits Osteogenic Differentiation of Human Bone Marrow-Derived Mesenchymal Stem Cells by Targeting LRP5. Int J Biochem Cell Biol (2016) 72: 55– 62. doi: 10.1016/j.biocel.2016.01.004 26774446 · DOI
  103. [105]Shen G Ren H Shang Q Zhao W Zhang Z Yu X. Foxf1 Knockdown Promotes BMSC Osteogenesis in Part by Activating the Wnt/β-Catenin Signalling Pathway and Prevents Ovariectomy-Induced Bone Loss. EBioMedicine (2020) 52: 102626. doi: 10.1016/j.ebiom.2020.102626 31981979 PMC6992955 · DOI
  104. [106]Zhuang XM Zhou B. Exosome Secreted by Human Gingival Fibroblasts in Radiation Therapy Inhibits Osteogenic Differentiation of Bone Mesenchymal Stem Cells by Transferring miR-23a. BioMed Pharmacother (2020) 131: 110672. doi: 10.1016/j.biopha.2020.110672 32889404 · DOI
  105. [107]Zhuang XM Zhou B Yuan KF. Role of P53 Mediated miR-23a/CXCL12 Pathway in Osteogenic Differentiation of Bone Mesenchymal Stem Cells on Nanostructured Titanium Surfaces. BioMed Pharmacother (2019) 112: 108649. doi: 10.1016/j.biopha.2019.108649 30784930 · DOI
  106. [108]Sun LY Wang N Ban T Sun YH Han Y Sun LL. MicroRNA-23a Mediates Mitochondrial Compromise in Estrogen Deficiency-Induced Concentric Remodeling via Targeting PGC-1α. J Mol Cell Cardiol (2014) 75: 1– 11. doi: 10.1016/j.yjmcc.2014.06.012 24984145 · DOI
  107. [109]Yu B Huo L Liu Y Deng P Szymanski J Li J. PGC-1α Controls Skeletal Stem Cell Fate and Bone-Fat Balance in Osteoporosis and Skeletal Aging by Inducing TAZ. Cell Stem Cell (2018) 23(2): 193– 209.e5. doi: 10.1016/j.stem.2018.06.009 30017591 PMC6322535 · DOI
  108. [110]Sujitha S Rasool M. Berberine Coated Mannosylated Liposomes Curtail RANKL Stimulated Osteoclastogenesis Through the Modulation of GSK3β Pathway via Upregulating miR-23a. Int Immunopharmacol (2019) 74: 105703. doi: 10.1016/j.intimp.2019.105703 31261037 · DOI
  109. [111]Jang HD Shin JH Park DR Hong JH Yoon K Ko R. Inactivation of Glycogen Synthase Kinase-3β Is Required for Osteoclast Differentiation. J Biol Chem (2011) 286(45): 39043–50. doi: 10.1074/jbc.M111.256768 PMC3234729 21949120 · DOI
  110. [112]Sims NA. The JAK1/STAT3/SOCS3 Axis in Bone Development, Physiology, and Pathology. Exp Mol Med (2020) 52(8): 1185–97. doi: 10.1038/s12276-020-0445-6 PMC8080635 32788655 · DOI
  111. [113]Farr JN Xu M Weivoda MM Monroe DG Fraser DG Onken JL. Targeting Cellular Senescence Prevents Age-Related Bone Loss in Mice. Nat Med (2017) 23(9): 1072–9. doi: 10.1038/nm.4385 PMC5657592 28825716 · DOI · Paper page
  112. [114]Murakami K Kobayashi Y Uehara S Suzuki T Koide M Yamashita T. A Jak1/2 Inhibitor, Baricitinib, Inhibits Osteoclastogenesis by Suppressing RANKL Expression in Osteoblasts In Vitro. PloS One (2017) 12(7): e0181126. doi: 10.1371/journal.pone.0181126 28708884 PMC5510865 · DOI
  113. [115]Su R Dong L Zou D Zhao H Ren Y Li F. microRNA-23a, -27a and -24 Synergistically Regulate JAK1/Stat3 Cascade and Serve as Novel Therapeutic Targets in Human Acute Erythroid Leukemia. Oncogene (2016) 35(46): 6001–14. doi: 10.1038/onc.2016.127 27086927 · DOI
  114. [116]Yunna C Mengru H Lei W Weidong C. Macrophage M1/M2 Polarization. Eur J Pharmacol (2020) 877: 173090. doi: 10.1016/j.ejphar.2020.173090 32234529 · DOI · Paper page
  115. [117]Peng P Li Z Liu X. Reduced Expression of miR-23a Suppresses A20 in TLR-Stimulated Macrophages. Inflammation (2015) 38(5): 1787–93. doi: 10.1007/s10753-015-0156-7 25832477 · DOI
  116. [118]Qu Y Xu Y Jiang Y Yu D Jiang X Zhao L. Macrophage-Derived Extracellular Vesicles Regulates USP5-Mediated HDAC2/NRF2 Axis to Ameliorate Inflammatory Pain. FASEB J (2021) 35(9): e21332. doi: 10.1096/fj.202001185RR 34423867 · DOI
  117. [119]Grillari J Mäkitie RE Kocijan R Haschka J Vázquez DC Semmelrock E. Circulating miRNAs in Bone Health and Disease. Bone (2021) 145: 115787. doi: 10.1016/j.bone.2020.115787 33301964 · DOI
  118. [120]Sun Z Wang H Wang Y Yuan G Yu X Jiang H. MiR-103-3p Targets the M(6) A Methyltransferase METTL14 to Inhibit Osteoblastic Bone Formation. Aging Cell (2021) 20(2): e13298. doi: 10.1111/acel.13298 33440070 PMC7884043 · DOI
  119. [121]Wang Z Xie Q Yu Z Zhou H Huang Y Bi X. A Regulatory Loop Containing miR-26a, GSK3β and C/Ebpα Regulates the Osteogenesis of Human Adipose-Derived Mesenchymal Stem Cells. Sci Rep (2015) 5: 15280. doi: 10.1038/srep15280 26469406 PMC4606799 · DOI
  120. [122]Chen S Zheng Y Zhang S Jia L Zhou Y. Promotion Effects of miR-375 on the Osteogenic Differentiation of Human Adipose-Derived Mesenchymal Stem Cells. Stem Cell Rep (2017) 8(3): 773–86. doi: 10.1016/j.stemcr.2017.01.028 PMC5355733 28262546 · DOI
  121. [123]Lin Z He H Wang M Liang J. MicroRNA-130a Controls Bone Marrow Mesenchymal Stem Cell Differentiation Towards the Osteoblastic and Adipogenic Fate. Cell Prolif (2019) 52(6): e12688. doi: 10.1111/cpr.12688 31557368 PMC6869834 · DOI
  122. [124]Qian M Wang S Guo X Wang J Zhang Z Qiu W. Hypoxic Glioma-Derived Exosomes Deliver microRNA-1246 to Induce M2 Macrophage Polarization by Targeting TERF2IP via the STAT3 and NF-κb Pathways. Oncogene (2020) 39(2): 428–42. doi: 10.1038/s41388-019-0996-y 31485019 · DOI · Paper page
  123. [125]Lian JB Stein GS van Wijnen AJ Stein JL Hassan MQ Gaur T. MicroRNA Control of Bone Formation and Homeostasis. Nat Rev Endocrinol (2012) 8(4): 212–27. doi: 10.1038/nrendo.2011.234 PMC3589914 22290358 · DOI
  124. [126]Sujitha S Dinesh P Rasool M. Berberine Encapsulated PEG-Coated Liposomes Attenuate Wnt1/β-Catenin Signaling in Rheumatoid Arthritis via miR-23a Activation. Eur J Pharm Biopharm (2020) 149: 170–91. doi: 10.1016/j.ejpb.2020.02.007 32068029 · DOI
  125. [127]He Y Meng C Shao Z Wang H Yang S. MiR-23a Functions as a Tumor Suppressor in Osteosarcoma. Cell Physiol Biochem (2014) 34(5): 1485–96. doi: 10.1159/000366353 25322765 · DOI · Paper page
  126. [128]Gindin Y Jiang Y Francis P Walker RL Abaan OD Zhu YJ. miR-23a Impairs Bone Differentiation in Osteosarcoma via Down-Regulation of GJA1. Front Genet (2015) 6: 233. doi: 10.3389/fgene.2015.00233 26191074 PMC4488756 · DOI
  127. [129]Liao W Ning Y Xu HJ Zou WZ Hu J Liu XZ. BMSC-Derived Exosomes Carrying microRNA-122-5p Promote Proliferation of Osteoblasts in Osteonecrosis of the Femoral Head. Clin Sci (Lond) (2019) 133(18): 1955–75. doi: 10.1042/CS20181064 31387936 · DOI
  128. [130]Srivastava M Deal C. Osteoporosis in Elderly: Prevention and Treatment. Clin Geriatr Med (2002) 18(3): 529–55. doi: 10.1016/S0749-0690(02)00022-8 12424871 · DOI
  129. [131]Wang T He C. TNF-α and IL-6: The Link Between Immune and Bone System. Curr Drug Targets (2020) 21(3): 213–27. doi: 10.2174/1389450120666190821161259 31433756 · DOI
  130. [132]Li H Zhai Z Qu X Xu J Qin A Dai K. MicroRNAs as Potential Targets for Treatment of Osteoclast-Related Diseases. Curr Drug Targets (2018) 19(5): 422–31. doi: 10.2174/1389450117666160502144329 27138766 · DOI
  131. [133]Zhou Y Liu Y Cheng L. miR-21 Expression is Related to Particle-Induced Osteolysis Pathogenesis. J Orthop Res (2012) 30(11): 1837–42. doi: 10.1002/jor.22128 22508494 · DOI
  132. [134]Shibuya H Nakasa T Adachi N Nagata Y Ishikawa M Deie M. Overexpression of microRNA-223 in Rheumatoid Arthritis Synovium Controls Osteoclast Differentiation. Mod Rheumatol (2013) 23(4): 674–85. doi: 10.3109/s10165-012-0710-1 22903258 · DOI
  133. [135]Blüml S Bonelli M Niederreiter B Puchner A Mayr G Hayer S. Essential Role of microRNA-155 in the Pathogenesis of Autoimmune Arthritis in Mice. Arthritis Rheumatol (2011) 63(5): 1281–8. doi: 10.1002/art.30281 21321928 · DOI
  134. [136]Nakasa T Shibuya H Nagata Y Niimoto T Ochi M. The Inhibitory Effect of microRNA-146a Expression on Bone Destruction in Collagen-Induced Arthritis. Arthritis Rheumatol (2011) 63(6): 1582–90. doi: 10.1002/art.30321 21425254 · DOI
  135. [137]Lin W Li X-F Ren D-C Song M Duan L Liu J-Z. Administration of Zoledronic Acid Alleviates Osteoporosis in HIV Patients by Suppressing Osteoclastogenesis via Regulating RANKL Expression. Mol Med (2021) 27(1): 19. doi: 10.1186/s10020-021-00276-5 33637048 PMC7908730 · DOI
  136. [138]Qu Y Wang Z Zhou H Kang M Dong R Zhao J. Oligosaccharide Nanomedicine of Alginate Sodium Improves Therapeutic Results of Posterior Lumbar Interbody Fusion With Cages for Degenerative Lumbar Disease in Osteoporosis Patients by Downregulating Serum miR-155. Int J Nanomed (2017) 12: 8459–69. doi: 10.2147/IJN.S143824 PMC5703176 29200854 · DOI
  137. [139]Zhang X-Y Li H-N Chen F Chen Y-P Chai Y Liao J-Z. Icariin Regulates miR-23a-3p-Mediated Osteogenic Differentiation of BMSCs via BMP-2/Smad5/Runx2 and WNT/β-Catenin Pathways in Osteonecrosis of the Femoral Head. Saudi Pharm J (2021) 29(12): 1405–15. doi: 10.1016/j.jsps.2021.10.009 PMC8720822 35002378 · DOI

Authors
Ma, T.-L., Zhu, P., Ke, Z.-R., Chen, J.-X., Hu, Y.-H., & Xie, J.
Affiliations
Central South University (CN)
Corresponding author
Xie, Jie
ORCID
Venue
Frontiers in Endocrinology
Publisher
Frontiers Media SA
Published
2022-07-14
Volume
13
Pages
891313-891313
ISSN
1664-2392 (ISSN-L)
DOI
10.3389/fendo.2022.891313
PMC
PMC9329542
OpenAlex
W4285389107
Cited by
9
References
141
Citations by year
2026: 3 · 2025: 3 · 2024: 2 · 2023: 1
FWCI
0.16
Type
journal article
Language
en
Open access
Licence
Locations
  • Frontiers in Endocrinology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
National Natural Science Foundation of China (Grant No. 81974339)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bone Metabolism and Diseases
  • Health Sciences › Medicine › Orthopedics and Sports Medicine › Bone health and osteoporosis research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
Keywords
osteoporosis, miR-23a, microRNA, bone remodeling, bone formation, bone resorption, macrophage polarization, bone inflammation, osteoporosis treatment
MeSH terms
Bone Resorption, Humans, Macrophages, Osteoblasts, Osteoclasts, Osteoporosis, MicroRNAs

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review