microRNA-103a functions as a mechanosensitive microRNA to inhibit bone formation through targeting Runx2

Journal of Bone and Mineral Research

Volumn 30, Issue 2, 2015, Pages 330-345

  Zuo, Bin ^a   Zhu, JunFeng ^a   Li, Jiao ^a   Wang, ChuanDong ^a   Zhao, XiaoYing ^a   Cai, GuiQuan ^a   Li, Zheng ^a   Peng, Jianping ^a   Wang, Peng ^a   Shen, Chao ^a   Huang, Yan ^a   Xu, Jiake ^b   Zhang, XiaoLing ^a   Chen, XiaoDong ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Cyclic mechanical stretch; Mechanotransduction; Micrornas; Osteoblast; Runx2

Indexed keywords

ALKALINE PHOSPHATASE; BETA CATENIN; COLLAGEN TYPE 1; COLLAGEN TYPE 1 ALPHA 1; MICRORNA; MICRORNA 103A; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; OSTEOCALCIN; PANK3 PROTEIN; PROTEIN; TRANSCRIPTION FACTOR RUNX2; UNCLASSIFIED DRUG; MIRN103 MICRORNA, HUMAN; MIRN103 MICRORNA, MOUSE;

3' UNTRANSLATED REGION; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING SITE; BONE MASS; BONE REMODELING; CELL DIFFERENTIATION; CONTROLLED STUDY; CYTOSKELETON; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; FEMUR; GENE CONTROL; GENE FUNCTION; GENE LOCUS; GENE OVEREXPRESSION; GENE REPRESSION; HINDLIMB; IN VITRO STUDY; IN VIVO STUDY; LIPID METABOLISM; LUCIFERASE ASSAY; MALE; MECHANICAL STIMULATION; MECHANOTRANSDUCTION; MOLECULAR CLONING; MOUSE; NONHUMAN; OSSIFICATION; OSTEOBLAST; OSTEOLYSIS; OSTEOPOROSIS; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN TARGETING; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION; WESTERN BLOTTING; ANIMAL; BONE DEVELOPMENT; C57BL MOUSE; CELL LINE; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; HUMAN; IMMOBILIZATION; MECHANICAL STRESS; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; WEIGHT BEARING;

ADULT; ANIMALS; CELL DIFFERENTIATION; CELL LINE; CORE BINDING FACTOR ALPHA 1 SUBUNIT; DISEASE MODELS, ANIMAL; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; HINDLIMB SUSPENSION; HUMANS; MALE; MECHANOTRANSDUCTION, CELLULAR; MICE, INBRED C57BL; MICRORNAS; OSTEOBLASTS; OSTEOGENESIS; OSTEOPOROSIS; STRESS, MECHANICAL; TRANSCRIPTION, GENETIC; WEIGHT-BEARING;

EID: 84921793648     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.2352     Document Type: Article

References (75)

1. Harada S, Rodan GA. Control of osteoblast function and regulation of bone mass. Nature. 2003;423:349-55.
2. Zaidi M. Skeletal remodeling in health and disease. Nat Med. 2007;13:791-801.
3. Hsieh YF, Turner CH. Effects of loading frequency on mechanically induced bone formation. J Bone Miner Res. 2001;16:918-24.
4. Gross TS, Srinivasan S, Liu CC, Clemens TL, Bain SD. Noninvasive loading of the murine tibia: an in vivo model for the study of mechanotransduction. J Bone Miner Res. 2002;17:493-501.
5. Lacouture ME, Schaffer JL, Klickstein LB. A comparison of type I collagen, fibronectin, and vitronectin in supporting adhesion of mechanically strained osteoblasts. J Bone Miner Res. 2002;17:481-92.
6. Cheng MZ, Rawlinson SC, Pitsillides AA, et al. Human osteoblasts' proliferative responses to strain and 17beta-estradiol are mediated by the estrogen receptor and the receptor for insulin-like growth factor I. J Bone Miner Res. 2002;17:593-602.
7. Kapur S, Baylink DJ, Lau KH. Fluid flow shear stress stimulates human osteoblast proliferation and differentiation through multiple interacting and competing signal transduction pathways. Bone. 2003;32:241-51.
8. Patel MJ, Chang KH, Sykes MC, Talish R, Rubin C, Jo H. Low magnitude and high frequency mechanical loading prevents decreased bone formation responses of 2T3 preosteoblasts. J Cell Biochem. 2009;106:306-16.
9. Rubin J, Murphy TC, Fan X, Goldschmidt M, Taylor WR. Activation of extracellular signal-regulated kinase is involved in mechanical strain inhibition of RANKL expression in bone stromal cells. J Bone Miner Res. 2002;17:1452-60.
10. Papachroni KK, Karatzas DN, Papavassiliou KA, Basdra EK, Papavassiliou AG. Mechanotransduction in osteoblast regulation and bone disease. Trends Mol Med. 2009;15:208-16.
11. Bikle DD. Integrins, insulin like growth factors, and the skeletal response to load. Osteoporos Int. 2008;19:1237-46.
12. Papadopoulou AK, Papachristou DJ, Chatzopoulos SA, Pirttiniemi P, Papavassiliou AG, Basdra EK. Load application induces changes in the expression levels of Sox-9. FGFR-3 and VEGF in condylar chondrocytes. FEBS Lett. 2007;581:2041-6.
13. Reijnders CM, Bravenboer N, Tromp AM, Blankenstein MA, Lips P. Effect of mechanical loading on insulin-like growth factor-I gene expression in rat tibia. J Endocrinol. 2007;192:131-40.
14. Rittweger J, Frost HM, Schiessl H, et al. Muscle atrophy and bone loss after 90 days' bed rest and the effects of flywheel resistive exercise and pamidronate: results from the LTBR study. Bone. 2005;36:1019-29.
15. Bucaro MA, Fertala J, Adams CS, et al. Bone cell survival in microgravity: evidence that modeled microgravity increases osteoblast sensitivity to apoptogens. Ann N Y Acad Sci. 2004;1027:64-73.
16. 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;25:1049-57.
17. Trudel G, Payne M, Mödler B, et al. Bone marrow fat accumulation after 60 days of bed rest persisted 1 year after activities were resumed along with hemopoietic stimulation: the Women International Space Simulation for Exploration study. J Appl Physiol. 2009;107:540-8.
18. Morgan JL, Zwart SR, Heer M, Ploutz-Snyder R, Ericson K, Smith SM. Bone metabolism and nutritional status during 30-day head-down-tilt bed rest. J Appl Physiol. 2012;113:1519-29.
19. Searby ND, Steele CR, Globus RK. Influence of increased mechanical loading by hypergravity on the microtubule cytoskeleton and prostaglandin E2 release in primary osteoblasts. Am J Physiol Cell Physiol. 2005;289:C148-58.
20. Skerry TM. The response of bone to mechanical loading and disuse: fundamental principles and influences on osteoblast/osteocyte homeostasis. Arch Biochem Biophys. 2008;473:117-23.
21. Lambers FM, Bouman AR, Rimnac CM, Hernandez CJ. Microdamage caused by fatigue loading in human cancellous bone: relationship to reductions in bone biomechanical performance. PLoS One. 2013;8:e83662.
22. Ambros V. The functions of animal microRNAs. Nature. 2004;431:350-55.
23. Kosik KS. MicroRNAs and cellular phenotypy. Cell. 2010;143:21-6.
24. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004;116:281-97.
25. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell. 2009;136:215-33.
26. Hannon GJ. MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet. 2004;5:522-31.
27. Zamore PD, Haley B. Ribo-gnome: the big world of small RNAs. Science. 2005;309:1519-24.
28. Inose H, Ochi H, Kimura A, et al. A microRNA regulatory mechanism of osteoblast differentiation. Proc Natl Acad Sci U S A. 2009;106:20794-9.
29. Li Z, Hassan MQ, Volinia S, et al. A microRNA signature for a BMP2-induced osteoblast lineage commitment program. Proc Natl Acad Sci U S A. 2008;105:13906-11.
30. Hassan MQ, Gordon JA, Beloti MM, et al. A network connecting Runx2, SATB2, and the miR-23a∼27a∼24-2 cluster regulates the osteoblast differentiation program. Proc Natl Acad Sci U S A. 2010;107:19879-84.
31. Zhang Y, Xie RL, Croce CM, et al. A program of microRNAs controls osteogenic lineage progression by targeting transcription factor Runx2. Proc Natl Acad Sci U S A. 2011;108:9863-8.
32. Eskildsen T, Taipaleenmöki H, Stenvang J, et al. MicroRNA-138 regulates osteogenic differentiation of human stromal (mesenchymal) stem cells in vivo. Proc Natl Acad Sci U S A. 2011;108:6139-44.
33. Yoshida CA, Furuichi T, Fujita T, et al. Core-binding factor beta interacts with Runx2 and is required for skeletal development. Nat Genet. 2002;32:633-8.
34. Kundu M, Javed A, Jeon JP, et al. Cbfbeta interacts with Runx2 and has a critical role in bone development. Nat Genet. 2002;32:639-44.
35. Morey-Holton ER, Globus RK. Hindlimb unloading rodent model: technical aspects. J Appl Physiol. 2002;92:1367-77.
36. Wu J, Wang XX, Chiba H, et al. Combined intervention of exercise and genistein prevented androgen deficiency-induced bone loss in mice. J Appl Physiol. 2003;94:335-42.
37. Harris SA, Spelsberg TC. Immortalized human fetal osteoblastic cells. US Patent 5,681,701 dated Oct 28 1997.
38. Harris SA, Enger RJ, Riggs BL, Spelsberg TC. Development and characterization of a conditionally immortalized human fetal osteoblastic cell line. J Bone Miner Res. 1995;10:178-86.
39. Jacobs CR, Yellowley CE, Davis BR, Zhou Z, Cimbala JM, Donahue HJ. Differential effect of steady versus oscillating flow on bone cells. J Biomech. 1998;31:969-76.
40. Sun H, Wu C, Dai K, Chang J, Tang T. Proliferation and osteoblastic differentiation of human bone marrow-derived stromal cells on akermanite-bioactive ceramics. Biomaterials. 2006;27:5651-7.
41. Fritton SP, McLeod KJ, Rubin CT. Quantifying the strain history of bone: spatial uniformity and self-similarity of low-magnitude strains. J Biomech. 2000;33:317-25.
42. Estok DM 2nd, Harris WH. A stem design change to reduce peak cement strains at the tip of cemented total hip arthroplasty. J Arthroplasty. 2000;15:584-9.
43. Cowin SC, Weinbaum S. Strain amplification in the bone mechanosensory system. Am J Med Sci. 1998;316:184-8.
44. You L, Cowin SC, Schaffler MB, Weinbaum S. A model for strain amplification in the actin cytoskeleton of osteocytes due to fluid drag on pericellular matrix. J Biomech. 2001;34:1375-86.
45. Hughes-Fulford M. Signal transduction and mechanical stress. Sci STKE. 2004 Aug 31;2004(249):RE12.
46. Hatton JP, Pooran M, Li CF, Luzzio C, Hughes-Fulford M. A short pulse of mechanical force induces gene expression and growth in MC3T3-E1 osteoblasts via an ERK 1/2 pathway. J Bone Miner Res. 2003;18:58-66.
47. Armstrong VJ, Muzylak M, Sunters A, et al. Wnt/beta-catenin signaling is a component of osteoblastic bone cell early responses to load-bearing and requires estrogen receptor alpha. J Biol Chem. 2007;282:20715-27.
48. Huang J, Zhao L, Xing L, Chen D. MicroRNA-204 regulates Runx2 protein expression and mesenchymal progenitor cell differentiation. Stem Cells. 2010;28:357-64.
49. Trajkovski M, Hausser J, Soutschek J, et al. MicroRNAs 103 and 107 regulate insulin sensitivity. Nature. 2011;474:649-53.
50. Wilfred BR, Wang WX, Nelson PT. Energizing miRNA research: a review of the role of miRNAs in lipid metabolism, with a prediction that miR-103/107 regulates human metabolic pathways. Mol Genet Metab. 2007;91:209-17.
51. John E, Wienecke-Baldacchino A, Liivrand M, Heinöniemi M, Carlberg C, Sinkkonen L. Dataset integration identifies transcriptional regulation of microRNA genes by PPARg in differentiating mouse 3T3-L1 adipocytes. Nucleic Acids Res. 2012;40:4446-60.
52. Krützfeldt J, Rajewsky N, Braich R, et al. Silencing of microRNAs in vivo with 'antagomirs'. Nature. 2005;438:685-9.
53. Wang KC, Garmire LX, Young A, et al. Role of microRNA-23b in flow-regulation of Rb phosphorylation and endothelial cell growth. Proc Natl Acad Sci U S A. 2010;107:3234-9.
54. Qin X, Wang X, Wang Y, et al. MicroRNA-19a mediates the suppressive effect of laminar flow on cyclin D1 expression in human umbilical vein endothelial cells. Proc Natl Acad Sci U S A. 2010;107:3240-4.
55. Yehya N, Yerrapureddy A, Tobias J, Margulies SS. MicroRNA modulate alveolar epithelial response to cyclic stretch. BMC Genomics. 2012;13:154.
56. Mohamed JS, Lopez MA, Boriek AM. Mechanical stretch up-regulates microRNA-26a and induces human airway smooth muscle hypertrophy by suppressing glycogen synthase kinase-3β. J Biol Chem. 2010;285:29336-47.
57. Shyu KG, Wang BW, Wu GJ, Lin CM, Chang H. Mechanical stretch via transforming growth factor-β1 activates microRNA208a to regulate endoglin expression in cultured rat cardiac myoblasts. Eur J Heart Fail. 2013;15:36-45.
58. Guan YJ, Yang X, Wei L, Chen Q. MiR-365: a mechanosensitive microRNA stimulates chondrocyte differentiation through targeting histone deacetylase 4. FASEB J. 2011;25:4457-66.
59. Stein GS, Lian JB, van Wijnen AJ, et al. Runx2 control of organization, assembly and activity of the regulatory machinery for skeletal gene expression. Oncogene. 2004;23:4315-29.
60. Otto F, Thornell AP, Crompton T, et al. Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell. 1997;89:765-71.
61. Kaneki H, Guo R, Chen D, et al. TNF promotes RUNX2 degradation through up-regulation of SMURF1 and SMURF2 in osteoblasts. J Biol Chem. 2006;281:4326-33.
62. Wang X, Guo B, Li Q, et al. miR-214 targets ATF4 to inhibit bone formation. Nat Med. 2013;19:93-100.
63. Li H, Xie H, Liu W, et al. A novel microRNA targeting HDAC5 regulates osteoblast differentiation in mice and contributes to primary osteoporosis in humans. J Clin Invest. 2009;119:3666-77.
64. Jordan SD, Krüger M, Willmes DM, et al. Obesity-induced overexpression of miRNA-143 inhibits insulin-stimulated AKT activation and impairs glucose metabolism. Nat Cell Biol. 2011;13:434-46.
65. Favereaux A, Thoumine O, Bouali-Benazzouz R, et al. Bidirectional integrative regulation of Cav1.2 calcium channel by microRNA miR-103: role in pain. EMBO J. 2011;30:3830-41.
66. Weber DG, Johnen G, Bryk O, Jöckel KH, Brüning T. Identification of miRNA-103 in the cellular fraction of human peripheral blood as a potential biomarker for malignant mesothelioma - a pilot study. PLoS One. 2012;7:e30221.
67. Glass DA 2nd, Karsenty G. In vivo analysis of Wnt signaling in bone. Endocrinology. 2007;148:2630-4.
68. Sinaki M, Brey RH, Hughes CA, Larson DR, Kaufman KR. Significant reduction in risk of falls and back pain in osteoporotic-kyphotic women through a Spinal Proprioceptive Extension Exercise Dynamic (SPEED) program. Mayo Clin Proc. 2005;80:849-55.
69. Liu W, Toyosawa S, Furuichi T, et al. Overexpression of Cbfa1 in osteoblasts inhibits osteoblast maturation and causes osteopenia with multiple fractures. J Cell Biol. 2001 Oct 1;155(1):157-66.
70. Marie PJ. Transcription factors controlling osteoblastogenesis. Arch Biochem Biophys. 2008;473:98-105.
71. Kemmler W, Lauber D, Weineck J, Hensen J, Kalender W, Engelke K. Benefits of 2 years of intense exercise on bone density, physical fitness, and blood lipids in early postmenopausal osteopenic women: results of the Erlangen Fitness Osteoporosis Prevention Study (EFOPS). Arch Intern Med. 2004;164:1084-91.
72. Wolf S, Augat P, Eckert-Hübner K, Laule A, Krischak GD, Claes LE. Effects of high-frequency, low-magnitude mechanical stimulus on bone healing. Clin Orthop Relat Res. 2001 Apr; (385):192-8.
73. Augat P, Simon U, Liedert A, Claes L. Mechanics and mechano-biology of fracture healing in normal and osteoporotic bone. Osteoporos Int. 2005; 16(Suppl 2):S36-43.
74. Goodship AE, Kenwright J. The influence of induced micromovement upon the healing of experimental tibial fractures. J Bone Joint Surg Br. 1985;67:650-5.
75. Scott A, Khan KM, Duronio V, Hart DA. Mechanotransduction in human bone: in vitro cellular physiology that underpins bone changes with exercise. Sports Med. 2008;38:139-60.