Regulation of microRNA-17-92 cluster on bone development, remodeling, and metabolism_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

WAN Shan ,  YU Xijie

Laboratory of Endocrinology and Metabolism, Department of Endocrinology, West China Hospital, Sichuan University, Chengdu Sichuan, 610041, P.R.China;

Corresponding author：

YU Xijie, Email: xijieyu@hotmail.com

Keywords：

MicroRNA-17-92 cluster; skeleton development; bone remodeling; bone metabolism; Feingold syndrome

DOI：

10.7507/1002-1892.201701068

Video：

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Objective To review the regulation of microRNA-17-92 cluster on bone development, remodeling, and metabolism. Methods The related literature was reviewed. The clinical genetic phenotype, animal experiment, and cell research were illustrated so as to explore the possible regulatory mechanisms. Results MicroRNA-17-92 cluster is involved in physiological normal organs development, pathological neoplasm occurrence, and development. Recently, studies have shown that microRNA-17-92 cluster constitutes an intricate molecular signaling network with its upstream transcription factors and downstream targeting proteins, which controls bone development, remodeling, and metabolism exquisitely. Conclusion Present fundamental researches have certain understanding of the regulatory mechanisms of microRNA-17-92 cluster on bone development, remodeling, and metabolism. However, the exact mechanisms under these processes remain unknown.

Citation： WAN Shan, YU Xijie. Regulation of microRNA-17-92 cluster on bone development, remodeling, and metabolism. Chinese Journal of Reparative and Reconstructive Surgery, 2017, 31(7): 870-875. doi: 10.7507/1002-1892.201701068 Copy

1.	Ota A, Tagawa H, Karnan S, et al. Identification and characterization of a novel gene, C13orf25, as a target for 13q31-q32 amplification in malignant lymphoma. Cancer Res, 2004, 64(9): 3087-3095.
2.	O’Donnell KA, Wentzel EA, Zeller KI, et al. c-Myc-regulated microRNAs modulate E2F1 expression. Nature, 2005, 435(7043): 839-843.
3.	Aguda BD, Kim Y, Piper-Hunter MG, et al. MicroRNA regulation of a cancer network: consequences of the feedback loops involving miR-17-92, E2F, and Myc. Proc Natl Acad Sci U S A, 2008, 105(50): 19678-19683.
4.	Nittner D, Lambertz I, Clermont F, et al. Synthetic lethality between Rb, p53 and Dicer or miR-17-92 in retinal progenitors suppresses retinoblastoma formation. Nat Cell Biol, 2012, 14(9): 958-965.
5.	Liu W, Qi M, Konermann A, et al. The p53/miR-17/Smurf1 pathway mediates skeletal deformities in an age-related model via inhibiting the function of mesenchymal stem cells. Aging (Albany NY), 2015, 7(3): 205-218.
6.	Ventura A, Young AG, Winslow MM, et al. Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters. Cell, 2008, 132(5): 875-886.
7.	Lu Y, Thomson JM, Wong HY, et al. Transgenic over-expression of the microRNA miR-17-92 cluster promotes proliferation and inhibits differentiation of lung epithelial progenitor cells. Dev Biol, 2007, 310(2): 442-453.
8.	Danielson LS, Park DS, Rotllan N, et al. Cardiovascular dysregulation of miR-17-92 causes a lethal hypertrophic cardiomyopathy and arrhythmogenesis. FASEB J, 2013, 27(4): 1460-1467.
9.	Xiao C, Srinivasan L, Calado DP, et al. Lymphoproliferative disease and autoimmunity in mice with increased miR-17-92 expression in lymphocytes. Nat Immunol, 2008, 9(4): 405-414.
10.	Volinia S, Calin GA, Liu CG, et al. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci U S A, 2006, 103(7): 2257-2261.
11.	Petrocca F, Vecchione A, Croce CM. Emerging role of miR-106b-25/miR-17-92 clusters in the control of transforming growth factor beta signaling. Cancer Res, 2008, 68(20): 8191-8194.
12.	He L, Thomson JM, Hemann MT, et al. A microRNA polycistron as a potential human oncogene. Nature, 2005, 435(7043): 828-833.
13.	Zhang L, Huang J, Yang N, et al. microRNAs exhibit high frequency genomic alterations in human cancer. Proc Natl Acad Sci U S A, 2006, 103(24): 9136-9141.
14.	Xiang J, Wu J. Feud or Friend? The Role of the miR-17-92 Cluster in Tumorigenesis. Curr Genomics, 2010, 11(2): 129-135.
15.	Inomata M, Tagawa H, Guo YM, et al. MicroRNA-17-92 down-regulates expression of distinct targets in different B-cell lymphoma subtypes. Blood, 2009, 113(2): 396-402.
16.	Kuhnert F, Kuo CJ. miR-17-92 angiogenesis micromanagement. Blood, 2010, 115(23): 4631-4633.
17.	Celli J, van Bokhoven H, Brunner HG. Feingold syndrome: clinical review and genetic mapping. Am J Med Genet A, 2003, 122A(4): 294-300.
18.	Feingold M, Hall BD, Lacassie Y, et al. Syndrome of microcephaly, facial and hand abnormalities, tracheoesophageal fistula, duodenal atresia, and developmental delay. Am J Med Genet, 1997, 69(3): 245-249.
19.	van Bokhoven H, Celli J, van Reeuwijk J, et al. MYCN haploinsufficiency is associated with reduced brain size and intestinal atresias in Feingold syndrome. Nat Genet, 2005, 37(5): 465-467.
20.	Marcelis CL, Hol FA, Graham GE, et al. Genotype-phenotype correlations in MYCN-related Feingold syndrome. Hum Mutat, 2008, 29(9): 1125-1132.
21.	de Pontual L, Yao E, Callier P, et al. Germline deletion of the miR-17 approximately 92 cluster causes skeletal and growth defects in humans. Nat Genet, 2011, 43(10): 1026-1030.
22.	Hemmat M, Rumple MJ, Mahon LW, et al. Short stature, digit anomalies and dysmorphic facial features are associated with the duplication of miR-17～92 cluster. Mol Cytogenet, 2014, 7: 27.
23.	Kannu P, Campos-Xavier AB, Hull D, et al. Post-axial polydactyly type A2, overgrowth and autistic traits associated with a chromosome 13q31.3 microduplication encompassing miR-17-92 and GPC5. Eur J Med Genet, 2013, 56(8): 452-457.
24.	Concepcion CP, Bonetti C, Ventura A. The microRNA-17-92 family of microRNA clusters in development and disease. Cancer J, 2012, 18(3): 262-267.
25.	Uziel T, Karginov FV, Xie S, et al. The miR-17～92 cluster collaborates with the Sonic Hedgehog pathway in medulloblastoma. Proc Natl Acad Sci U S A, 2009, 106(8): 2812-2817.
26.	Liu XS, Chopp M, Wang XL, et al. MicroRNA-17-92 cluster mediates the proliferation and survival of neural progenitor cells after stroke. J Biol Chem, 2013, 288(18): 12478-12488.
27.	Han YC, Vidigal JA, Mu P, et al. An allelic series of miR-17 approximately 92-mutant mice uncovers functional specialization and cooperation among members of a microRNA polycistron. NatGenet, 2015, 47(7): 766-775.
28.	Penzkofer D, Bonauer A, Fischer A, et al. Phenotypic characterization of miR-92a-/- mice reveals an important function of miR-92a in skeletal development. PLoS One, 2014, 9(6): e101153.
29.	Sharifi M, Salehi R, Gheisari Y, et al. Inhibition of microRNA miR-92a induces apoptosis and inhibits cell proliferation in human acute promyelocytic leukemia through modulation of p63 expression. Mol Biol Rep, 2014, 41(5): 2799-2808.
30.	Ji X, Chen X, Yu X. MicroRNAs in Osteoclastogenesis and Function: Potential Therapeutic Targets for Osteoporosis. Int J Mol Sci, 2016, 17(3): 349.
31.	Suttamanatwong S. MicroRNAs in bone development and their diagnostic and therapeutic potentials in osteoporosis. Connective Tissue Research, 2017, 58(1): 90-102.
32.	Zou P, Ding J, Fu S. Elevated expression of microRNA-19a predicts a poor prognosis in patients with osteosarcoma. Pathol Res Pract, 2017, 213(3): 194-198.
33.	Zhang Y, Guo X, Li Z, et al. A systematic investigation based on microRNA-mediated gene regulatory network reveals that dysregulation of microRNA-19a/Cyclin D1 axis confers an oncogenic potential and a worse prognosis in human hepatocellular carcinoma. RNA Biol, 2015, 12(6): 643-657.
34.	Lu K, Liu C, Tao T, et al. MicroRNA-19a regulates proliferation and apoptosis of castration-resistant prostate cancer cells by targeting BTG1. FEBS Lett, 2015, 589(13): 1485-1490.
35.	Wu Q, Yang Z, An Y, et al. MiR-19a/b modulate the metastasis of gastric cancer cells by targeting the tumour suppressor MXD1. Cell Death Dis, 2014, 5: e1144.
36.	Feng Y, Liu J, Kang Y, et al. miR-19a acts as an oncogenic microRNA and is up-regulated in bladder cancer. J Exp Clin Cancer Res, 2014, 33: 67.
37.	Huang G, Nishimoto K, Zhou Z, et al. miR-20a encoded by the miR-17-92 cluster increases the metastatic potential of osteosarcoma cells by regulating Fas expression. Cancer Res, 2012, 72(4): 908-916.
38.	Gaur T, Hussain S, Mudhasani R, et al. Dicer inactivation in osteoprogenitor cells compromises fetal survival and bone formation, while excision in differentiated osteoblasts increases bone mass in the adult mouse. Dev Biol, 2010, 340(1): 10-21.
39.	Zheng L, Tu Q, Meng S, et al. Runx2/DICER/miRNA Pathway in Regulating Osteogenesis. J Cell Physiol, 2017, 232(1): 182-191.
40.	Wysokinski D, Pawlowska E, Blasiak J. RUNX2: A Master Bone Growth Regulator That May Be Involved in the DNA Damage Response. DNA Cell Biol, 2015, 34(5): 305-315.
41.	Vimalraj S, Arumugam B, Miranda PJ, et al. Runx2: Structure, function, and phosphorylation in osteoblast differentiation. Int J Biol Macromol, 2015, 78: 202-208.
42.	Tu Q, Zhang J, James L, et al. Cbfa1/Runx2-deficiency delays bone wound healing and locally delivered Cbfa1/Runx2 promotes bone repair in animal models. Wound Repair Regen, 2007, 15(3): 404-412.
43.	Laine CM, Joeng KS, Campeau PM, et al. WNT1 mutations in early-onset osteoporosis and osteogenesis imperfecta. N Engl J Med, 2013, 368(19): 1809-1816.
44.	Kwan Tat S, Amiable N, Pelletier JP, et al. Modulation of OPG, RANK and RANKL by human chondrocytes and their implication during osteoarthritis. Rheumatology (Oxford), 2009, 48(12): 1482-1490.
45.	Kadri A, Ea HK, Bazille C, et al. Osteoprotegerin inhibits cartilage degradation through an effect on trabecular bone in murine experimental osteoarthritis. Arthritis Rheum, 2008, 58(8): 2379-2386.
46.	Zhou M, Ma J, Chen S, et al. MicroRNA-17-92 cluster regulates osteoblast proliferation and differentiation. Endocrine, 2014, 45(2): 302-310.
47.	Moon YJ, Yun CY, Choi H, et al. Smad4 controls bone homeostasis through regulation of osteoblast/osteocyte viability. Exp Mol Med, 2016, 48(9): e256.
48.	Mohan S, Wergedal JE, Das S, et al. Conditional disruption of miR17-92 cluster in collagen type I-producing osteoblasts results in reduced periosteal bone formation and bone anabolic response to exercise. Physiol Genomics, 2015, 47(2): 33-43.
49.	Han Y, Kim CY, Cheong H, Lee KY. Osterix represses adipogenesis by negatively regulating PPARɣ transcriptional activity. Sci Rep, 2016, 6: 35655.
50.	Hamdy NA. Targeting the RANK/RANKL/OPG signaling pathway: a novel approach in the management of osteoporosis. Curr Opin Investig Drugs, 2007, 8(4): 299-303.
51.	Pérez-Sayáns M, Somoza-Martín JM, Barros-Angueira F, et al. RANK/RANKL/OPG role in distraction osteogenesis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod, 2010, 109(5): 679-686.

1. Ota A, Tagawa H, Karnan S, et al. Identification and characterization of a novel gene, C13orf25, as a target for 13q31-q32 amplification in malignant lymphoma. Cancer Res, 2004, 64(9): 3087-3095.
2. O’Donnell KA, Wentzel EA, Zeller KI, et al. c-Myc-regulated microRNAs modulate E2F1 expression. Nature, 2005, 435(7043): 839-843.
3. Aguda BD, Kim Y, Piper-Hunter MG, et al. MicroRNA regulation of a cancer network: consequences of the feedback loops involving miR-17-92, E2F, and Myc. Proc Natl Acad Sci U S A, 2008, 105(50): 19678-19683.
4. Nittner D, Lambertz I, Clermont F, et al. Synthetic lethality between Rb, p53 and Dicer or miR-17-92 in retinal progenitors suppresses retinoblastoma formation. Nat Cell Biol, 2012, 14(9): 958-965.
5. Liu W, Qi M, Konermann A, et al. The p53/miR-17/Smurf1 pathway mediates skeletal deformities in an age-related model via inhibiting the function of mesenchymal stem cells. Aging (Albany NY), 2015, 7(3): 205-218.
6. Ventura A, Young AG, Winslow MM, et al. Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters. Cell, 2008, 132(5): 875-886.
7. Lu Y, Thomson JM, Wong HY, et al. Transgenic over-expression of the microRNA miR-17-92 cluster promotes proliferation and inhibits differentiation of lung epithelial progenitor cells. Dev Biol, 2007, 310(2): 442-453.
8. Danielson LS, Park DS, Rotllan N, et al. Cardiovascular dysregulation of miR-17-92 causes a lethal hypertrophic cardiomyopathy and arrhythmogenesis. FASEB J, 2013, 27(4): 1460-1467.
9. Xiao C, Srinivasan L, Calado DP, et al. Lymphoproliferative disease and autoimmunity in mice with increased miR-17-92 expression in lymphocytes. Nat Immunol, 2008, 9(4): 405-414.
10. Volinia S, Calin GA, Liu CG, et al. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci U S A, 2006, 103(7): 2257-2261.
11. Petrocca F, Vecchione A, Croce CM. Emerging role of miR-106b-25/miR-17-92 clusters in the control of transforming growth factor beta signaling. Cancer Res, 2008, 68(20): 8191-8194.
12. He L, Thomson JM, Hemann MT, et al. A microRNA polycistron as a potential human oncogene. Nature, 2005, 435(7043): 828-833.
13. Zhang L, Huang J, Yang N, et al. microRNAs exhibit high frequency genomic alterations in human cancer. Proc Natl Acad Sci U S A, 2006, 103(24): 9136-9141.
14. Xiang J, Wu J. Feud or Friend? The Role of the miR-17-92 Cluster in Tumorigenesis. Curr Genomics, 2010, 11(2): 129-135.
15. Inomata M, Tagawa H, Guo YM, et al. MicroRNA-17-92 down-regulates expression of distinct targets in different B-cell lymphoma subtypes. Blood, 2009, 113(2): 396-402.
16. Kuhnert F, Kuo CJ. miR-17-92 angiogenesis micromanagement. Blood, 2010, 115(23): 4631-4633.
17. Celli J, van Bokhoven H, Brunner HG. Feingold syndrome: clinical review and genetic mapping. Am J Med Genet A, 2003, 122A(4): 294-300.
18. Feingold M, Hall BD, Lacassie Y, et al. Syndrome of microcephaly, facial and hand abnormalities, tracheoesophageal fistula, duodenal atresia, and developmental delay. Am J Med Genet, 1997, 69(3): 245-249.
19. van Bokhoven H, Celli J, van Reeuwijk J, et al. MYCN haploinsufficiency is associated with reduced brain size and intestinal atresias in Feingold syndrome. Nat Genet, 2005, 37(5): 465-467.
20. Marcelis CL, Hol FA, Graham GE, et al. Genotype-phenotype correlations in MYCN-related Feingold syndrome. Hum Mutat, 2008, 29(9): 1125-1132.
21. de Pontual L, Yao E, Callier P, et al. Germline deletion of the miR-17 approximately 92 cluster causes skeletal and growth defects in humans. Nat Genet, 2011, 43(10): 1026-1030.
22. Hemmat M, Rumple MJ, Mahon LW, et al. Short stature, digit anomalies and dysmorphic facial features are associated with the duplication of miR-17～92 cluster. Mol Cytogenet, 2014, 7: 27.
23. Kannu P, Campos-Xavier AB, Hull D, et al. Post-axial polydactyly type A2, overgrowth and autistic traits associated with a chromosome 13q31.3 microduplication encompassing miR-17-92 and GPC5. Eur J Med Genet, 2013, 56(8): 452-457.
24. Concepcion CP, Bonetti C, Ventura A. The microRNA-17-92 family of microRNA clusters in development and disease. Cancer J, 2012, 18(3): 262-267.
25. Uziel T, Karginov FV, Xie S, et al. The miR-17～92 cluster collaborates with the Sonic Hedgehog pathway in medulloblastoma. Proc Natl Acad Sci U S A, 2009, 106(8): 2812-2817.
26. Liu XS, Chopp M, Wang XL, et al. MicroRNA-17-92 cluster mediates the proliferation and survival of neural progenitor cells after stroke. J Biol Chem, 2013, 288(18): 12478-12488.
27. Han YC, Vidigal JA, Mu P, et al. An allelic series of miR-17 approximately 92-mutant mice uncovers functional specialization and cooperation among members of a microRNA polycistron. NatGenet, 2015, 47(7): 766-775.
28. Penzkofer D, Bonauer A, Fischer A, et al. Phenotypic characterization of miR-92a-/- mice reveals an important function of miR-92a in skeletal development. PLoS One, 2014, 9(6): e101153.
29. Sharifi M, Salehi R, Gheisari Y, et al. Inhibition of microRNA miR-92a induces apoptosis and inhibits cell proliferation in human acute promyelocytic leukemia through modulation of p63 expression. Mol Biol Rep, 2014, 41(5): 2799-2808.
30. Ji X, Chen X, Yu X. MicroRNAs in Osteoclastogenesis and Function: Potential Therapeutic Targets for Osteoporosis. Int J Mol Sci, 2016, 17(3): 349.
31. Suttamanatwong S. MicroRNAs in bone development and their diagnostic and therapeutic potentials in osteoporosis. Connective Tissue Research, 2017, 58(1): 90-102.
32. Zou P, Ding J, Fu S. Elevated expression of microRNA-19a predicts a poor prognosis in patients with osteosarcoma. Pathol Res Pract, 2017, 213(3): 194-198.
33. Zhang Y, Guo X, Li Z, et al. A systematic investigation based on microRNA-mediated gene regulatory network reveals that dysregulation of microRNA-19a/Cyclin D1 axis confers an oncogenic potential and a worse prognosis in human hepatocellular carcinoma. RNA Biol, 2015, 12(6): 643-657.
34. Lu K, Liu C, Tao T, et al. MicroRNA-19a regulates proliferation and apoptosis of castration-resistant prostate cancer cells by targeting BTG1. FEBS Lett, 2015, 589(13): 1485-1490.
35. Wu Q, Yang Z, An Y, et al. MiR-19a/b modulate the metastasis of gastric cancer cells by targeting the tumour suppressor MXD1. Cell Death Dis, 2014, 5: e1144.
36. Feng Y, Liu J, Kang Y, et al. miR-19a acts as an oncogenic microRNA and is up-regulated in bladder cancer. J Exp Clin Cancer Res, 2014, 33: 67.
37. Huang G, Nishimoto K, Zhou Z, et al. miR-20a encoded by the miR-17-92 cluster increases the metastatic potential of osteosarcoma cells by regulating Fas expression. Cancer Res, 2012, 72(4): 908-916.
38. Gaur T, Hussain S, Mudhasani R, et al. Dicer inactivation in osteoprogenitor cells compromises fetal survival and bone formation, while excision in differentiated osteoblasts increases bone mass in the adult mouse. Dev Biol, 2010, 340(1): 10-21.
39. Zheng L, Tu Q, Meng S, et al. Runx2/DICER/miRNA Pathway in Regulating Osteogenesis. J Cell Physiol, 2017, 232(1): 182-191.
40. Wysokinski D, Pawlowska E, Blasiak J. RUNX2: A Master Bone Growth Regulator That May Be Involved in the DNA Damage Response. DNA Cell Biol, 2015, 34(5): 305-315.
41. Vimalraj S, Arumugam B, Miranda PJ, et al. Runx2: Structure, function, and phosphorylation in osteoblast differentiation. Int J Biol Macromol, 2015, 78: 202-208.
42. Tu Q, Zhang J, James L, et al. Cbfa1/Runx2-deficiency delays bone wound healing and locally delivered Cbfa1/Runx2 promotes bone repair in animal models. Wound Repair Regen, 2007, 15(3): 404-412.
43. Laine CM, Joeng KS, Campeau PM, et al. WNT1 mutations in early-onset osteoporosis and osteogenesis imperfecta. N Engl J Med, 2013, 368(19): 1809-1816.
44. Kwan Tat S, Amiable N, Pelletier JP, et al. Modulation of OPG, RANK and RANKL by human chondrocytes and their implication during osteoarthritis. Rheumatology (Oxford), 2009, 48(12): 1482-1490.
45. Kadri A, Ea HK, Bazille C, et al. Osteoprotegerin inhibits cartilage degradation through an effect on trabecular bone in murine experimental osteoarthritis. Arthritis Rheum, 2008, 58(8): 2379-2386.
46. Zhou M, Ma J, Chen S, et al. MicroRNA-17-92 cluster regulates osteoblast proliferation and differentiation. Endocrine, 2014, 45(2): 302-310.
47. Moon YJ, Yun CY, Choi H, et al. Smad4 controls bone homeostasis through regulation of osteoblast/osteocyte viability. Exp Mol Med, 2016, 48(9): e256.
48. Mohan S, Wergedal JE, Das S, et al. Conditional disruption of miR17-92 cluster in collagen type I-producing osteoblasts results in reduced periosteal bone formation and bone anabolic response to exercise. Physiol Genomics, 2015, 47(2): 33-43.
49. Han Y, Kim CY, Cheong H, Lee KY. Osterix represses adipogenesis by negatively regulating PPARɣ transcriptional activity. Sci Rep, 2016, 6: 35655.
50. Hamdy NA. Targeting the RANK/RANKL/OPG signaling pathway: a novel approach in the management of osteoporosis. Curr Opin Investig Drugs, 2007, 8(4): 299-303.
51. Pérez-Sayáns M, Somoza-Martín JM, Barros-Angueira F, et al. RANK/RANKL/OPG role in distraction osteogenesis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod, 2010, 109(5): 679-686.

Chinese Journal of Reparative and Reconstructive Surgery

Regulation of microRNA-17-92 cluster on bone development, remodeling, and metabolism

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