Role of miR-140 in embryonic bone development and cancer

Clinical Science

Volumn 129, Issue 10, 2015, Pages 863-873

  Green, Darrell ^a   Dalmay, Tamas ^b   Fraser, William D ^a,c  

^a UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^b UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^c NORFOLK AND NORWICH UNIVERSITY HOSPITAL   (United Kingdom)

Author keywords

Bone; Cancer; Cartilage; Chondrocyte; Embryogenesis; MiRNA

Indexed keywords

MICRORNA; MICRORNA 140; RAD51 ASSOCIATED PROTEIN 1; RAD51 PROTEIN; UNCLASSIFIED DRUG; MIRN140 MICRORNA, HUMAN;

BONE DEVELOPMENT; BREAST CANCER; CANCER RESISTANCE; CANCER STEM CELL; CARCINOGENESIS; CARTILAGE; CHONDROGENESIS; COLORECTAL CANCER; DOWN REGULATION; EMBRYO DEVELOPMENT; GENE DUPLICATION; GENE EXPRESSION; HEAD AND NECK TUMOR; HOMEOSTASIS; HUMAN; INTRACELLULAR SIGNALING; LIVER CANCER; MOLECULAR BIOLOGY; NEOPLASM; NONHUMAN; ONCOGENE; OSSIFICATION; OSTEOSARCOMA; OVARY CANCER; PHARMACOGENETICS; PRIORITY JOURNAL; REVIEW; STOMACH CANCER; TUMOR SUPPRESSOR GENE; UPREGULATION; WNT SIGNALING PATHWAY; BIOLOGICAL MODEL; BONE; CARTILAGE CELL; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; SIGNAL TRANSDUCTION;

BONE AND BONES; BONE DEVELOPMENT; CHONDROCYTES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICRORNAS; MODELS, GENETIC; NEOPLASMS; SIGNAL TRANSDUCTION;

EID: 84947312961     PISSN: 01435221     EISSN: 14708736     Source Type: Journal    
DOI: 10.1042/CS20150230     Document Type: Review

References (81)

1. Wagner, D.O. and Aspenberg, P. (2011) Where did bone come from? Acta Orthop. 82, 393-398
2. Ito, Y. and Miyazono, K. (2003) RUNX transcription factors as key targets of TGF-beta superfamily signaling. Curr. Opin. Genet. Dev. 13, 43-47
3. Gilbert, S. (2000) The Development of Bones, 6th edn., Sinauer Associates, Sunderland, MA
4. Sosic, D., Brand-Saberi, B., Schmidt, C., Christ, B and Olson, E.N. (1997) Regulation of paraxis expression and somite formation by ectoderm-and neural tube-derived signals. Dev. Biol. 185, 229-243
5. Kozhemyakina, E., Lassar, A.B. and Zelzer, E. (2015) A pathway to bone: signaling molecules and transcription factors involved in chondrocyte development and maturation. Development 142, 817-831
6. Ornitz, D.M. and Marie, P.J. (2002) FGF signaling pathways in endochondral and intramembranous bone development and human genetic disease. Genes Dev. 16, 1446-1465
7. Walzer, S.M., Cetin, E., Grubl-Barabas, R., Sulzbacher, I., Rueger, B., Girsch, W., Toegel, S., Windhager, R. and Fischer, M.B. (2014) Vascularization of primary and secondary ossification centres in the human growth plate. BMC Dev. Biol. 14, 36
8. Cserjesi, P., Brown, D., Ligon, K.L., Lyons, G.E., Copeland, N.G., Gilbert, D.J., Jenkins, N.A. and Olson, E.N. (1995) Scleraxis: a basic helix-loop-helix protein that prefigures skeletal formation during mouse embryogenesis. Development 121, 1099-110
9. Cooper, K.L., Oh, S., Sung, Y., Dasari, R.R., Kirschner, M.W. and Tabin, C.J. (2013) Multiple phases of chondrocyte enlargement underlie differences in skeletal proportions. Nature 495, 375-378
10. Kozhemyakina, E., Zhang, M., Ionescu, A., Ayturk, U.M., Ono, N., Kobayashi, A., Kronenberg, H., Warman, M.L. and Lasser, A.B. (2015) Identification of a Prg4-positive articular cartilage progenitor cell population. Arthritis Rheumatol. 67, 1261-1273
11. Addison, W.N., Fu, M.M., Yang, H.X., Lin, Z., Nagano, K., Gori, F. and Baron, R. (2014) Direct transcriptional repression of Zfp423 by Zfp521 mediates a bone morphogenic protein-dependent osteoblast versus adipocyte lineage commitment switch. Mol. Cell Biol. 34, 3076-3085
12. Wysolmerski, J. (2013) Parathyroid Hormone-Related Protein, 8th edn., Wiley-Blackwell, Singapore
13. Zelzer, E., Mamluk, R., Ferrara, N., Johnson, R.S., Schipani, E. and Olsen, B.R. (2004) VEGFA is necessary for chondrocyte survival during bone development. Development 131, 2161-2171
14. Pelosi, M., Lazzarano, S., Thoms, B.L. and Murphy, C.L. (2013) Parathyroid hormone-related protein is induced by hypoxia and promotes expression of the differentiated phenotype of human articular chondrocytes. Clin. Sci. 125, 461-740
15. Correa, D., Hesse, E., Seriwatanachai, D., Kiviranta, R., Saito, H., Yamana, K., Neff, L., Atfi, A., Coillard, L., Sitara, D. et al. (2010) Zfp521 is a target gene and key effector of parathyroid hormone-related peptide signaling in growth plate chondrocytes. Dev. Cell 19, 533-546
16. Kozhemyakina, E., Cohen, T., Yao, T.P. and Lassar, A.B. (2009) Parathyroid hormone-related peptide represses chondrocyte hypertrophy through a protein phosphatase 2A/histone deacetylase 4/MEF2 pathway. Mol. Cell Biol. 29, 5751-5762
17. Seriwatanachai, D., Densmore, M.J, Sato, T., Correa, D., Neff, L., Baron, R. and Lanske, B. (2011) Deletion of Zfp521 rescues the growth plate phenotype in a mouse model of Jansen metaphyseal chondrodysplasia. FASEB J. 25, 3057-3067
18. Papaioannou, G., Mirzamohammadi, F., Lisse, T.S., Nishimori, S., Wein, M.N. and Kobayashi, T. (2015) MicroRNA-140 provides robustness to the regulation of hypertrophic chondrocyte differentiation by the PTHrP-HDAC4 pathway. J. Bone Miner. Res. 30, 1044-1052
19. Swingler, T.E., Wheeler, G., Carmont, V., Elliott, H.R., Barter, M.J., Abu-Elmagd, M., Donell, S.T., Boot-Handford, R.P., Hajihosseini, M.K., Munsterberg, A. et al. (2012) The expression and function of microRNAs in chondrogenesis and osteoarthritis. Arthritis Rheum. 64, 1909-1919
20. Rodrigo, I., Hill, R.E., Balling, R., Munsterberg, A. and Imai, K. (2003) Pax1 and Pax9 activate Bapx1 to induce chondrogenic differentiation in the sclerotome. Development 130, 473-482
21. Wheeler, G.N. and Brandli, A.W. (2009) Simple vertebrate models for chemical genetics and drug discovery screens: lessons from zebrafish and Xenopus. Dev. Dyn. 238, 1287-1308
22. Calibuso-Salazar, M.J. and Ten Eyck, G.R. (2015) A novel whole-embryo culture model for pharmaceutical and developmental studies. J. Pharmacol. Toxicol. Methods 73c, 21-26
23. Hager, G.L., McNally, J.G. and T. Misteli, T. (2009) Transcription dynamics. Mol. Cell 35, 741-753
24. Lee, R.C., Feinbaum, R.L. and Ambros, V. (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75, 843-854
25. Lee, Y., Kim, M., Han, J., Yeom, K.H., Lee, S., Baek, S.H. and Kim, V.N. (2004) MicroRNA genes are transcribed by RNA polymerase II. EMBO J. 23, 4051-4060
26. Filipowicz, W., Bhattacharyya, S.N. and Sonenberg, N. (2008) Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat. Rev. Genet. 9, 102-114
27. Provost, P., Dishart, D., Doucet, J., Frendewey, D., Samuelsson, B. and Radmark, O. (2002) Ribonuclease activity and RNA binding of recombinant human Dicer. EMBO J. 21, 5864-5874
28. Kiriakidou, M., Nelson, P.T., Kouranov, A., Fitziev, P., Bouyioukos, C., Mourelatos, Z. and Hatzigeorgiou, A. (2004) A combined computational-experimental approach predicts human microRNA targets. Genes Dev. 18, 1165-1178
29. Zhou, H. and Rigoutsos, I. (2014) MiR-103a-3p targets the 5' UTR of GPRC5A in pancreatic cells. RNA 20, 1431-149
30. Hausser, J., Syed, A.P., Bilen, B. and Zavolan, M. (2013) Analysis of CDS-located miRNA target sites suggests that they can effectively inhibit translation. Genome Res. 23, 604-615
31. Kozomara, A. and Griffiths-Jones, S. (2014) miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res. 42, 68-73
32. Hall, A.E. and Dalmay, T. (2013) Discovery of novel small RNAs in the quest to unravel genome complexity. Biochem. Soc. Trans. 41, 866-870
33. Davis, B.N. and Hata, A. (2009) Regulation of microRNA biogenesis: A miRiad of mechanisms. Cell Commun. Signal. 7, 18
34. Pasquinelli, A.E., Reinhart, B.J., Slack, F., Martindale, M.Q., Kuroda, M.I., Maller, B., Hayward, D.C., Ball, E.E., Degnan, B., Muller, P. et al. (2000) Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 408, 86-89
35. Ozsolak, F., Poling, L.L., Wang, Z., Liu, H., Liu, X.S., Roeder, R.G., Zhang, X., Song, J.S. and Fisher, D.E. (2008) Chromatin structure analyses identify miRNA promoters. Genes Dev. 22, 3172-3183
36. Corcoran, D.L., Pandit, K.V., Gordon, B., Bhattacharjee, A., Kaminski, N. and Benos, P.V. (2009) Features of mammalian microRNA promoters emerge from polymerase II chromatin immunoprecipitation data. PloS One 4, e5279
37. Suzuki, H.I., Yamagata, K., Sugimoto, K., Iwamoto, T., Kato, S. and Miyazono, K. (2009) Modulation of microRNA processing by p53. Nature 460, 529-533
38. O'Donnell, K.A., Wentzel, E.A., Zeller, K.I., Dang, C.V. and Mendell, J.T. (2005) c-Myc-regulated microRNAs modulate E2F1 expression. Nature 435, 839-843
39. Lujambio, A. and Esteller, M. (2009) How epigenetics can explain human metastasis: a new role for microRNAs. Cell Cycle 8, 377-382
40. Lujambio, A., Calin, G.A., Villanueva, A., Ropero, S., Sanchez-Cespedes, M., Blanco, D., Montuenga, L.M., Rossi, S., Nicoloso, M.S., Faller, W.J. et al. (2008) A microRNA DNA methylation signature for human cancer metastasis. Proc. Natl. Acad. Sci. U.S.A. 105, 13556-13561
41. Hansen, T.B., Jensen, T.I., Clausen, B.H., Bramsen, J.B., Finsen, B., Damgaard, C.K. and Kjems, J. (2013) Natural RNA circles function as efficient microRNA sponges. Nature 495, 384-388
42. Papaioannou, G., Mirzamohammadi, F. and Kobayashi, T. (2014) MicroRNAs involved in bone formation. Cell. Mol. Life Sci. 71, 4747-4761
43. Watanabe, T., Sato, T., Amano, T., Kawamura, Y., Kawamura, N., Kawaguchi, H., Yamashita, N., Kurihara, H. and Nakaoka, T. (2008) Dnm3os, a non-coding RNA, is required for normal growth and skeletal development in mice. Dev. Dyn. 237, 3738-3748
44. Guan, Y.J., Yang, X., Wei, L. and Chen, Q. (2011) MiR-365: a mechanosensitive microRNA stimulates chondrocyte differentiation through targeting histone deacetylase 4. FASEB J. 25, 4457-4466
45. Gradus, B., Alon, I. and Hornstein, E. (2011) miRNAs control tracheal chondrocyte differentiation. Dev. Biol. 360, 58-65
46. Zhong, N., Sun, J., Min, Z., Zhao, W., Zhang, R., Wang, W., Tian, J., Tian, L., Ma, J., Li, D. et al. (2012) MicroRNA-337 is associated with chondrogenesis through regulating TGFBR2 expression. Osteoarthritis Cartilage 20, 593-602
47. Papaioannou, G., Inloes, J.B., Nakamura, Y., Paltrinieri, E. and Kobayashi, T. (2013) let-7 and miR-140 microRNAs coordinately regulate skeletal development. Proc. Natl. Acad. Sci. U.S.A. 110, 291-300
48. Kim, D., Grun, D. and van Oudenaarden, A. (2013) Dampening of expression oscillations by synchronous regulation of a microRNA and its target. Nat. Genet. 45, 1337-1344
49. Miyaki, S., Nakasa, T., Otsuki, S., Grogan, S.P., Higashiyama, R., Inoue, A., Kato, Y., Sato, T., Lotz, M.K. and Asahara, H. (2009) MicroRNA-140 is expressed in differentiated human articular chondrocytes and modulates interleukin-1 responses. Arthritis Rheum. 60, 2723-2730
50. Liu, S.P., Fu, R.H., Yu, H.H., Li, K.W., Tsai, C.H., Shyu, W.C. and Lin, S.Z. (2009) MicroRNAs regulation modulated self-renewal and lineage differentiation of stem cells. Cell Transplant. 18, 1039-1045
51. Miyaki, S., Sato, T., Inoue, A., Otsuki, S., Ito, Y., Yokoyama, S., Kato, Y., Takemoto, F., Nakasa, T., Yamashita, S. et al. (2010) MicroRNA-140 plays dual roles in both cartilage development and homeostasis. Genes Dev. 24, 1173-1185
52. Wienholds, E., Kloosterman, W.P., Miska, E., Alvarez-Saavedra, E., Berezikov, E., de Bruijn, E., Horvitz, H.R., Kauppinen, S. and Plasterk, R.H. (2005) MicroRNA expression in zebrafish embryonic development. Science 309, 310-311
53. Tuddenham, L., Wheeler, G., Ntounia-Fousara, S., Waters, J., Hajihosseini, M.K., Clark, I. and Dalmay, T. (2006) The cartilage specific microRNA-140 targets histone deacetylase 4 in mouse cells. FEBS Lett. 580, 4214-4217
54. Lagos-Quintana, M., Rauhut, R., Yalcin, A., Meyer, J., Lendeckel, W. and Tuschl, T. (2002) Identification of tissue-specific microRNAs from mouse. Curr. Biol. 12, 735-739
55. Yang, J., Qin, S., Yi, C., Ma, G., Zhu, H., Zhou, W., Xiong, Y., Zhu, X., Wang, Y., He, L. et al. (2011) MiR-140 is co-expressed with Wwp2-C transcript and activated by Sox9 to target Sp1 in maintaining the chondrocyte proliferation. FEBS Lett. 585, 2992-2997
56. Yamashita, S., Miyaki, S., Kato, Y., Yokoyama, S., Sato, T., Barrionuevo, F., Akiyama, H., Scherer, G., Takada, S. and Asahara, H. (2012) L-Sox5 and Sox6 proteins enhance chondrogenic miR-140 microRNA expression by strengthening dimeric Sox9 activity. J. Biol. Chem. 287, 22206-22215
57. Nicolas, F.E. and Dalmay, T. (2013) New evidence supports a role of MiR-140 at early stages of bone development. Arthritis Rheum. 65, 1668-1689
58. Eberhart, J.K., He, X., Swartz, M.E., Yan, Y.L., Song, H., Boling, T.C., Kunerth, A.K., Walker, M.B., Kimmel, C.B. and Postlethwait, J.H. (2008) MicroRNA Mirn140 modulates Pdgf signaling during palatogenesis. Nat. Genet. 40, 290-298
59. Nakamura, Y., Inloes, J.B., Katagiri, T. and Kobayashi, T. (2011) Chondrocyte-specific microRNA-140 regulates endochondral bone development and targets Dnpep to modulate bone morphogenetic protein signaling. Mol. Cell Biol. 31, 3019-3028
60. Miyaki, S. and Asahara, H. (2012) Macro view of microRNA function in osteoarthritis. Nat. Rev. Rheumatol. 8, 543-552
61. Nicolas, F.E., Pais, H., Schwach, F., Lindow, M., Kauppinen, S., Moulton, V. and Dalmay, T. (2008) Experimental identification of microRNA-140 targets by silencing and overexpressing miR-140. RNA 14, 2513-2520
62. Pais, H., Nicolas, F.E., Soond, S.M., Swingler, T.E., Clark, I.M., Chantry, A., Moulton, V. and Dalmay, T. (2010) Analyzing mRNA expression identifies Smad3 as a microRNA-140 target regulated only at protein level. RNA 16, 489-494
63. Mak, I.W., Singh, S., Turcotte, R. and Ghert, M. (2014) The epigenetic regulation of SOX9 by miR-145 in human chondrosarcoma. J. Cell. Biochem. 116, 37-44
64. Yoshitaka, T., Kawai, A., Miyaki, S., Numoto, K., Kikuta, K., Ozaki, T., Lotz, M. and Asahara, H. (2013) Analysis of microRNAs expressions in chondrosarcoma. J. Orthop. Res. 31, 1992-1998
65. Karlsen, T.A, Jakobsen, R.B., Mikkelsen, T.S. and Brinchmann, J.E. (2014) microRNA-140 targets RALA and regulates chondrogenic differentiation of human mesenchymal stem cells by translational enhancement of SOX9 and ACAN. Stem Cells Dev. 23, 290-304
66. Piepoli, A., Tavano, F., Copetti, M., Mazza, T., Palumbo, O., Panza, A., di Mola, F.F., Pazienza, V., Mazzoccoli, G., Biscaglia, G., Gentile, A., Mastrodonato, N., Carella, M., Pellegrini, F., Sebastiano, P. and Andriulli, A. (2012) Mirna expression profiles identify drivers in colorectal and pancreatic cancers. PLoS One 7, e33663
67. Takata, A., Otsuka, M., Yoshikawa, T., Kishikawa, T., Hikiba, Y., Obi, S., Goto, T., Kang, Y.J., Maeda, S., Yoshida, H. et al. (2013) MicroRNA-140 acts as a liver tumor suppressor by controlling NF-kappaB activity by directly targeting DNA methyltransferase 1 (Dnmt1) expression. Hepatology 57, 162-170
68. Al-Ejeh, F., Smart, C.E., Morrison, B.J., Chenevix-Trench, G., Lopez, J.A., Lakhani, S.R., Brown, M.P. and Khanna, K.K. (2011) Breast cancer stem cells: treatment resistance and therapeutic opportunities. Carcinogenesis. 32, 650-658
69. Zhang, Y., Eades, G., Yao, Y., Li, Q. and Zhou, Q. (2012) Estrogen receptor alpha signaling regulates breast tumor-initiating cells by down-regulating miR-140 which targets the transcription factor SOX2. J. Biol. Chem. 287, 41514-41522
70. Fillmore, C.M., Gupta, P.B., Rudnick, J.A., Caballero, S., Keller, P.J., Lander, E.S. and Kuperwasser, C. (2010) Estrogen expands breast cancer stem-like cells through paracrine FGF/Tbx3 signaling. Proc. Natl. Acad. Sci. U.S.A. 107, 21737-21742
71. Serrano, N.A., Xu, C., Liu, Y., Wang, P., Fan, W., Upton, M.P., Houck, J.R., Lohavanichbutr, P., Kao, M., Zhao, L.P. et al. (2012) Integrative analysis in oral squamous cell carcinoma reveals DNA copy number-associated miRNAs dysregulating target genes. Otolaryngol. Head Neck Surg. 147, 501-508
72. Miles, G.D., Seiler, M., Rodriguez, L., Rajagopal, G. and Bhanot, G. (2012) Identifying microRNA/mRNA dysregulations in ovarian cancer. BMC Res. Notes 5, 164
73. Sand, M., Skrygan, M., Sand, D., Georgas, D., Hahn, S.A., Gambichler, T., Altmeyer, P. and Bechara, F.G. (2012) Expression of microRNAs in basal cell carcinoma. Br. J. Dermatol. 167, 847-855
74. Yanaihara, N., Caplen, N., Bowman, E., Seike, M., Kumamoto, K., Yi, M., Stephens, R.M., Okamoto, A., Yokota, J., Tanaka, T. et al. (2006) Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell 9, 189-198
75. Zhang, X., Cairns, M., Rose, B., O'Brien, C., Shannon, K., Clark, J., Gamble, J. and Tran, N. (2009) Alterations in miRNA processing and expression in pleomorphic adenomas of the salivary gland. Int. J. Cancer 124, 2855-2863
76. Song, B., Wang, Y., Xi, Y., Kudo, K., Bruheim, S., Botchkina, G.I., Gavin, E., Wan, Y., Formentini, A., Kornmann, M. et al. (2009) Mechanism of chemoresistance mediated by miR-140 in human osteosarcoma and colon cancer cells. Oncogene 28, 4065-4074
77. Kim, C.H., Kim, H.K., Rettig, R.L., Kim, J., Lee, E.T., Aprelikova, O., Choi, I.J., Munroe, D.J. and Green, J.E. (2011) miRNA signature associated with outcome of gastric cancer patients following chemotherapy. BMC Med. Genomics 4, 79
78. Gregson, C.L., Poole, K.E., McCloskey, E.V., Duncan, E.L., Rittweger, J., Fraser, W.D., Smith, G.D. and Tobias, J.H. (2014) Elevated circulating Sclerostin concentrations in individuals with high bone mass, with and without LRP5 mutations. J. Clin. Endocrinol. Metab. 99, 2897-2907
79. Raisz, L.G. (2005) Pathogenesis of osteoporosis: concepts, conflicts, and prospects. J. Clin. Invest. 115, 3318-3325
80. Schneikert, J. and Behrens, J. (2007) The canonical Wnt signalling pathway and its APC partner in colon cancer development. Gut 56, 417-425
81. Li, X., Ominsky, M.S., Warmington, K.S., Morony, S., Gong, J., Cao, J., Gao, Y., Shalhoub, V., Tipton, B., Haldankar, R. et al. (2009) Sclerostin antibody treatment increases bone formation, bone mass, and bone strength in a rat model of postmenopausal osteoporosis. J. Bone Miner. Res. 24, 578-588