MiR-17 modulates osteogenic differentiation through a coherent feed-forward loop in mesenchymal stem cells isolated from periodontal ligaments of patients with periodontitis

Stem Cells

Volumn 29, Issue 11, 2011, Pages 1804-1816

  Liu, Yali ^a,c   Liu, Wenjia ^a   Hu, Chenghu ^a   Xue, Zengfu ^b   Wang, Guang ^a   Ding, Bofu ^a   Luo, Hailang ^a   Tang, Liang ^a   Kong, Xiangwei ^a   Chen, Xiaoyan ^a   Liu, Na ^a   Ding, Yin ^a   Jin, Yan ^a  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^c KUNMING MEDICAL UNIVERSITY   (China)

Author keywords

Inflammatory microenvironment; Mesenchymal stem cells; MicroRNA; Osteogenic differentiation

Indexed keywords

PROTEIN SMURF1; REGULATOR PROTEIN; SMAD PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BONE DEVELOPMENT; CELL DIFFERENTIATION; CELL ISOLATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; INFLAMMATION; MESENCHYMAL STEM CELL; MICROENVIRONMENT; MOLECULAR MECHANICS; PERIODONTAL LIGAMENT; PERIODONTITIS; POSITIVE FEEDBACK; PROTEIN EXPRESSION; PROTEIN FUNCTION; WESTERN BLOTTING;

ADULT; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELLS, CULTURED; HUMANS; MESENCHYMAL STEM CELLS; MICRORNAS; OSTEOGENESIS; PERIODONTAL LIGAMENT; PERIODONTITIS; REAL-TIME POLYMERASE CHAIN REACTION; UBIQUITIN-PROTEIN LIGASES;

EID: 80054898958     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.728     Document Type: Article

References (58)

1. Shi S, Gronthos S, Chen S et al. Bone formation by human postnatal bone marrow stromal stem cells is enhanced by telomerase expression. Nat Biotechnol 2002;20:587-591. (Pubitemid 34595152)
2. Zuk PA, Zhu M, Ashjian P et al. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 2002;13:4279-4295. (Pubitemid 35471185)
3. Gronthos S, Mankani M, Brahim J et al. Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. Proc Natl Acad Sci USA 2000;97:13625-13630.
4. Seo BM, Miura M, Gronthos S et al. Investigation of multipotent postnatal stem cells from human periodontal ligament. Lancet 2004;364:149-155. (Pubitemid 38891686)
5. Ding J, Ghali O, Lencel P et al. TNF-alpha and IL-1beta inhibit RUNX2 and collagen expression but increase alkaline phosphatase activity and mineralization in human mesenchymal stem cells. Life Sci 2009;84:499-504.
6. Kastrinaki MC, Sidiropoulos P, Roche S et al. Functional, molecular and proteomic characterisation of bone marrow mesenchymal stem cells in rheumatoid arthritis. Ann Rheum Dis 2008;67:741-749. (Pubitemid 351829372)
7. Shi S, Bartold PM, Miura M et al. The efficacy of mesenchymal stem cells to regenerate and repair dental structures. Orthodontics Craniofacial Res 2005;8:191-199.
8. Liu Y, Zheng Y, Ding G et al. Periodontal ligament stem cell-mediated treatment for periodontitis in miniature swine. Stem Cells (Dayton, OH) 2008;26:1065-1073.
9. Yang Z, Jin F, Zhang X et al. Tissue engineering of cementum/periodontal- ligament complex using a novel three-dimensional pellet cultivation system for human periodontal ligament stem cells. Tissue Eng 2009;15:571-581.
10. Mendell JT. miRiad roles for the miR-17-92 cluster in development and disease. Cell 2008;133:217-222. (Pubitemid 351508308)
11. Fontana L, Pelosi E, Greco P et al. MicroRNAs 17-5p-20a-106a control monocytopoiesis through AML1 targeting and M-CSF receptor upregulation. Nat Cell Biol 2007;9:775-787. (Pubitemid 47019464)
12. Garzon R, Croce CM. MicroRNAs in normal and malignant hematopoiesis. Curr Opin Hematol 2008;15:352-358.
13. Lawrie CH. MicroRNAs and haematology: Small molecules, big function. Brit J Haematol 2007;137:503-512. (Pubitemid 46817340)
14. Mraz M, Pospisilova S, Malinova K et al. MicroRNAs in chronic lymphocytic leukemia pathogenesis and disease subtypes. Leukemia Lymphoma 2009;50:506-509.
15. Matsubara H, Takeuchi T, Nishikawa E et al. Apoptosis induction by antisense oligonucleotides against miR-17-5p and miR-20a in lung cancers overexpressing miR-17-92. Oncogene 2007;26:6099-6105. (Pubitemid 47373805)
16. Takakura S, Mitsutake N, Nakashima M et al. Oncogenic role of miR-17-92 cluster in anaplastic thyroid cancer cells. Cancer Sci 2008;99:1147-1154. (Pubitemid 351676626)
17. Guo R, Yamashita M, Zhang Q et al. Ubiquitin ligase Smurf1 mediates tumor necrosis factor-induced systemic bone loss by promoting proteasomal degradation of bone morphogenetic signaling proteins. J Biol Chem 2008;283:23084-23092.
18. Zhao L, Huang J, Guo R et al. Smurf1 inhibits mesenchymal stem cell proliferation and differentiation into osteoblasts through JunB degradation. J Bone Miner Res 2010;25:1246-1256.
19. Zhao M, Qiao M, Harris SE et al. Smurf1 inhibits osteoblast differentiation and bone formation in vitro and in vivo. J Biol Chem 2004;279:12854-12859. (Pubitemid 38445859)
20. Yamashita M, Ying SX, Zhang GM et al. Ubiquitin ligase Smurf1 controls osteoblast activity and bone homeostasis by targeting MEKK2 for degradation. Cell 2005;121:101-113.
21. Pihlstrom BL, Michalowicz BS, Johnson NW. Periodontal diseases. Lancet 2005;366:1809-1820. (Pubitemid 41642647)
22. Pihlstrom BL. Measurement of attachment level in clinical trials: Probing methods. J Periodontol 1992;63:1072-1077.
23. Armitage GC. The complete periodontal examination. Periodontology 2000 2004;34:22-33. (Pubitemid 41794527)
24. Bretz WA, Weyant RJ, Corby PM et al. Systemic inflammatory markers, periodontal diseases, and periodontal infections in an elderly population. J Am Geriatr Soc 2005;53:1532-1537. (Pubitemid 41602443)
25. de Queiroz AC, Taba M, Jr., O'Connell PA et al. Inflammation markers in healthy and periodontitis patients: a preliminary data screening. Braz Dent J 2008;19:3-8.
26. Gorska R, Gregorek H, Kowalski J et al. Relationship between clinical parameters and cytokine profiles in inflamed gingival tissue and serum samples from patients with chronic periodontitis. J Clin Periodontol 2003;30:1046-1052. (Pubitemid 38011208)
27. Jandinski JJ, Stashenko P, Feder LS et al. Localization of interleukin-1 beta in human periodontal tissue. J Periodontol 1991;62:36-43.
28. Roberts FA, McCaffery KA, Michalek SM. Profile of cytokine mRNA expression in chronic adult periodontitis. J Dent Res 1997;76:1833-1839. (Pubitemid 127732208)
29. Ripa RS, Jorgensen E, Wang Y et al. Stem cell mobilization induced by subcutaneous granulocyte-colony stimulating factor to improve cardiac regeneration after acute ST-elevation myocardial infarction: Result of the double-blind, randomized, placebo-controlled stem cells in myocardial infarction (STEMMI) trial. Circulation 2006;113:1983-1992.
30. Chen SC, Marino V, Gronthos S et al. Location of putative stem cells in human periodontal ligament. J Periodontal Res 2006;41:547-553. (Pubitemid 44656931)
31. Li L, Xie T. Stem cell niche: Structure and function. Annu Rev Cell Dev Biol 2005;21:605-631. (Pubitemid 41740648)
32. Schneider EL, Mitsui Y. The relationship between in vitro cellular aging and in vivo human age. Proc Natl Acad Sci USA 1976;73:3584-3588.
33. Stolzing A, Jones E, McGonagle D et al. Age-related changes in human bone marrow-derived mesenchymal stem cells: consequences for cell therapies. Mech Ageing Dev 2008;129:163-173.
34. Stenderup K, Justesen J, Clausen C et al. Aging is associated with decreased maximal life span and accelerated senescence of bone marrow stromal cells. Bone 2003;33:919-926. (Pubitemid 37543568)
35. Sun LY, Zhang HY, Feng XB et al. Abnormality of bone marrowderived mesenchymal stem cells in patients with systemic lupus erythematosus. Lupus 2007;16:121-128. (Pubitemid 46347934)
36. Sun L, Akiyama K, Zhang H et al. Mesenchymal stem cell transplantation reverses multiorgan dysfunction in systemic lupus erythematosus mice and humans. Stem Cells 2009;27:1421-1432.
37. Wang Z, Goh J, Das De S et al. Efficacy of bone marrow-derived stem cells in strengthening osteoporotic bone in a rabbit model. Tissue Eng 2006;12:1753-1761. (Pubitemid 44162835)
38. Yeh JK, Evans JF, Chen MM et al. Effect of hypophysectomy on the proliferation and differentiation of rat bone marrow stromal cells. Am J Physiol 1999;276:E34-E42. (Pubitemid 29065591)
39. Asselin-Labat ML, Vaillant F, Sheridan JM et al. Control of mammary stem cell function by steroid hormone signalling. Nature 2010;465:798-802.
40. Graves DT, Cochran D. The contribution of interleukin-1 and tumor necrosis factor to periodontal tissue destruction. J Periodontol 2003;74:391-401. (Pubitemid 36939356)
41. El-Awady AR, Messer RL, Gamal AY et al. Periodontal ligament fibroblasts sustain destructive immune modulators of chronic periodontitis. J Periodontol 2010;81:1324-1335.
42. Gangaraju VK, Lin H. MicroRNAs: Key regulators of stem cells. Nat Rev Mol Cell Biol 2009;10:116-125.
43. Luzi E, Marini F, Sala SC et al. Osteogenic differentiation of human adipose tissue-derived stem cells is modulated by the miR-26a targeting of the SMAD1 transcription factor. J Bone Miner Res 2008;23:287-295. (Pubitemid 351160043)
44. Mizuno Y, Yagi K, Tokuzawa Y et al. miR-125b inhibits osteoblastic differentiation by down-regulation of cell proliferation. Biochem Biophys Res Commun 2008;368:267-272.
45. Inose H, Ochi H, Kimura A et al. A microRNA regulatory mechanism of osteoblast differentiation. Proc Natl Acad Sci USA 2009;106: 20794-20799.
46. Huang J, Zhao L, Xing L et al. MicroRNA-204 regulates Runx2 protein expression and mesenchymal progenitor cell differentiation. Stem Cells 2010;28:357-364.
47. Mizuno Y, Tokuzawa Y, Ninomiya Y et al. miR-210 promotes osteoblastic differentiation through inhibition of AcvR1b. FEBS Lett 2009; 583:2263-2268.
48. 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;119:3666-3677.
49. Kapinas K, Kessler C, Ricks T et al. miR-29 modulates Wnt signaling in human osteoblasts through a positive feedback loop. J Biol Chem 285:25221-25231.
50. Li Z, Hassan MQ, Jafferji M et al. Biological functions of miR-29b contribute to positive regulation of osteoblast differentiation. J Biol Chem 2009;284:15676-15684.
51. Kim YJ, Bae SW, Yu SS et al. miR-196a regulates proliferation and osteogenic differentiation in mesenchymal stem cells derived from human adipose tissue. J Bone Miner Res 2009;24: 816-825.
52. Hobert O. Common logic of transcription factor and microRNA action. Trends Biochem Sci 2004;29:462-468. (Pubitemid 39158869)
53. Fontana L, Fiori ME, Albini S et al. Antagomir-17-5p abolishes the growth of therapy-resistant neuroblastoma through p21 and BIM. PLoS ONE 2008;3:e2236.
54. Hayashita Y, Osada H, Tatematsu Y et al. A polycistronic microRNA cluster, miR-17-92, is overexpressed in human lung cancers and enhances cell proliferation. Cancer Res 2005;65:9628-9632. (Pubitemid 41541436)
55. Cloonan N, Brown MK, Steptoe AL et al. The miR-17-5p microRNA is a key regulator of the G1/S phase cell cycle transition. Genome Biol 2008;9:R127.
56. Hossain A, Kuo MT, Saunders GF. Mir-17-5p regulates breast cancer cell proliferation by inhibiting translation of AIB1 mRNA. Mol Cell Biol 2006;26:8191-8201. (Pubitemid 44631015)
57. Scherr M, Venturini L, Battmer K et al. Lentivirus-mediated antagomir expression for specific inhibition of miRNA function. Nucleic Acids Res 2007;35:e149.
58. Kaneki H, Guo R, Chen D et al. Tumor necrosis factor promotes Runx2 degradation through up-regulation of Smurf1 and Smurf2 in osteoblasts. J Biol Chem 2006;281:4326-4333. (Pubitemid 43847863)