Regulation of IGF -1 signaling by microRNAs

Frontiers in Genetics

Volumn 5, Issue JAN, 2015, Pages

  Jung, Hwa Jin ^a   Suh, Yousin ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Aging; Aging related disease; IGF 1 signaling; Micrornas; Therapeutic agents

Indexed keywords

INSULIN RECEPTOR; INSULIN RECEPTOR SUBSTRATE; INSULIN RECEPTOR SUBSTRATE 2; MAMMALIAN TARGET OF RAPAMYCIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 2; MICRORNA; MICRORNA 1; MICRORNA 145; MICRORNA 148A; MICRORNA 152; MICRORNA 16; MICRORNA 223; MICRORNA 34A; MICRORNA 370; MICRORNA 486; MICRORNA 497; MICRORNA 675; MICRORNA 681; MICRORNA 96; MICRORNA 98; MICRORNA 99A; MICRORNA 99B; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; S6 KINASE; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; TRANSCRIPTION FACTOR FKHRL1; TRANSCRIPTION FACTOR FOXO; UNCLASSIFIED DRUG; UNINDEXED DRUG;

3' UNTRANSLATED REGION; ALZHEIMER DISEASE; CELL PROLIFERATION; CELL SURVIVAL; GENE EXPRESSION; GENOTYPE; HORMONE SUBSTITUTION; HUMAN; LIVER CELL CARCINOMA; LUCIFERASE ASSAY; MOUTH SQUAMOUS CELL CARCINOMA; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PROTEIN EXPRESSION; PSORIASIS; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION;

EID: 84923259922     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2014.00472     Document Type: Review

References (119)

1. Andreassen, M., Raymond, I., Kistorp, C., Hildebrandt, P., Faber, J., and Kristensen, L. O. (2009). IGF1 as predictor of all cause mortality and cardiovascular disease in an elderly population. Eur. J. Endocrinol. 160, 25-31. doi: 10.1530/EJE-08-0452
2. Arcaro, A. (2013). Targeting the insulin-like growth factor-1 receptor in human cancer. Front. Pharmacol. 4:30. doi: 10.3389/fphar.2013.00030
3. Bai, S., Nasser, M. W., Wang, B., Hsu, S. H., Datta, J., Kutay, H.,et al. (2009). MicroRNA-122 inhibits tumorigenic properties of hepatocellular carcinoma cells and sensitizes these cells to sorafenib. J. Biol. Chem. 284, 32015-32027. doi: 10.1074/jbc. M109.016774
4. Baserga, R. (2000). The contradictions of the insulin-like growth factor 1 receptor. Oncogene 19, 5574-5581. doi: 10.1038/sj.onc.1203854
5. Boehm, M., and Slack, F. (2005). A developmental timing microRNA and its target regulate life span in C. elegans. Science 310, 1954-1957. doi: 10.1126/science.1115596
6. Brady, G., Crean, S. J., Naik, P., and Kapas, S. (2007). Upregulation of IGF-2 and IGF-1 receptor expression in oral cancer cell lines. Int. J. Oncol. 31, 875-881. doi: 10.3892/ijo.31.4.875
7. Brueckner, B., Stresemann, C., Kuner, R., Mund, C., Musch, T., Meister, M.,et al. (2007). The human let-7a-3 locus contains an epigenetically regulated microRNA gene with oncogenic function. Cancer Res. 67, 1419-1423. doi: 10.1158/0008-5472.CAN-06-4074
8. Cantarini, M. C., De La Monte, S. M., Pang, M., Tong, M., D'Errico, A., Trevisani, F.,et al. (2006). Aspartyl-asparagyl beta hydroxylase over-expression in human hepatoma is linked to activation of insulin-like growth factor and notch signaling mechanisms. Hepatology 44, 446-457. doi: 10.1002/hep.21272
9. Care, A., Catalucci, D., Felicetti, F., Bonci, D., Addario, A., Gallo, P.,et al. (2007). MicroRNA-133 controls cardiac hypertrophy. Nat. Med. 13, 613-618. doi: 10.1038/nm1582
10. Castro, J., Garcia, R. I., Kwok, S., Banerjee, A., Petravicz, J., Woodson, J.,et al. (2014). Functional recovery with recombinant human IGF1 treatment in a mouse model of Rett Syndrome. Proc. Natl. Acad. Sci. U.S.A. 111, 9941-9946. doi: 10.1073/pnas.1311685111
11. Chen, L., Wang, Q., Wang, G. D., Wang, H. S., Huang, Y., Liu, X. M.,et al. (2013). miR-16 inhibits cell proliferation by targeting IGF1R and the Raf1-MEK1/2-ERK1/2 pathway in osteosarcoma. FEBS Lett. 587, 1366-1372. doi: 10.1016/j.febslet.2013.03.007
12. Chen, L. H., Chiou, G. Y., Chen, Y. W., Li, H. Y., and Chiou, S. H. (2010). MicroRNA and aging: a novel modulator in regulating the aging network. Ageing Res. Rev. 9(Suppl. 1), S59-S66. doi: 10.1016/j.arr.2010.08.002
13. Chen, Y., Gao, D. Y., and Huang, L. (2014). In vivo delivery of miRNAs for cancer therapy: challenges and strategies. Adv. Drug Deliv. Rev. 81, 128-141. doi: 10.1016/j.addr.2014.05.009
14. Chen, Z., Jin, Y., Yu, D., Wang, A., Mahjabeen, I., Wang, C.,et al. (2012). Down-regulation of the microRNA-99 family members in head and neck squamous cell carcinoma. Oral Oncol. 48, 686-691. doi: 10.1016/j.oraloncology.2012.02.020
15. Cheng, W., Reiss, K., Kajstura, J., Kowal, K., Quaini, F., and Anversa, P. (1995). Down-regulation of the IGF-1 system parallels the attenuation in the proliferative capacity of rat ventricular myocytes during postnatal development. Lab. Invest. 72, 646-655.
16. Chhabra, R. (2014). miRNA and methylation: a multifaceted liaison. Chembiochem doi: 10.1002/cbic.201402449 [Epub ahead of print].
17. Costinean, S., Zanesi, N., Pekarsky, Y., Tili, E., Volinia, S., Heerema, N.,et al. (2006). Pre-B cell proliferation and lymphoblastic leukemia/high-grade lymphoma in E(mu)-miR155 transgenic mice. Proc. Natl. Acad. Sci. U.S.A. 103, 7024-7029. doi: 10.1073/pnas.0602266103
18. Cui, L., Zhou, H., Zhao, H., Zhou, Y., Xu, R., Xu, X.,et al. (2012). MicroRNA-99a induces G1-phase cell cycle arrest and suppresses tumorigenicity in renal cell carcinoma. BMC Cancer 12:546. doi: 10.1186/1471-2407-12-546
19. DeAngelis, T., Chen, J., Wu, A., Prisco, M., and Baserga, R. (2006). Transformation by the simian virus 40 T antigen is regulated by IGF-I receptor and IRS-1 signaling. Oncogene 25, 32-42.
20. de Lencastre, A., Pincus, Z., Zhou, K., Kato, M., Lee, S. S., and Slack, F. J. (2010). MicroRNAs both promote and antagonize longevity in C. elegans. Curr. Biol. 20, 2159-2168. doi: 10.1016/j.cub.2010.11.015
21. Efeyan, A., and Sabatini, D. M. (2010). mTOR and cancer: many loops in one pathway. Curr. Opin. Cell Biol. 22, 169-176. doi: 10.1016/j.ceb.2009.10.007
22. Elia, L., Contu, R., Quintavalle, M., Varrone, F., Chimenti, C., Russo, M. A.,et al. (2009). Reciprocal regulation of microRNA-1 and insulin-like growth factor-1 signal transduction cascade in cardiac and skeletal muscle in physiological and pathological conditions. Circulation 120, 2377-2385. doi: 10.1161/CIRCULATIONAHA.109.879429
23. Elmen, J., Lindow, M., Schutz, S., Lawrence, M., Petri, A., Obad, S.,et al. (2008). LNA-mediated microRNA silencing in non-human primates. Nature 452, 896-899. doi: 10.1038/nature06783
24. Galadari, I., Sharif, M. O., and Galadari, H. (2005). Psoriasis: a fresh look. Clin. Dermatol. 23, 491-502. doi: 10.1016/j.clindermatol.2005.01.009
25. Gilam, A., Edry, L., Mamluk-Morag, E., Bar-Ilan, D., Avivi, C., Golan, D.,et al. (2013). Involvement of IGF-1R regulation by miR-515-5p modifies breast cancer risk among BRCA1 carriers. Breast Cancer Res. Treat. 138, 753-760. doi: 10.1007/s10549-013-2502-5
26. Greer, E. L., and Brunet, A. (2005). FOXO transcription factors at the interface between longevity and tumor suppression. Oncogene 24, 7410-7425. doi: 10.1038/sj.onc.1209086
27. Greising, S. M., Baltgalvis, K. A., Lowe, D. A., and Warren, G. L. (2009). Hormone therapy and skeletal muscle strength: a meta-analysis. J. Gerontol. A Biol. Sci. Med. Sci. 64, 1071-1081. doi: 10.1093/gerona/glp082
28. Guo, S. T., Jiang, C. C., Wang, G. P., Li, Y. P., Wang, C. Y., Guo, X. Y.,et al. (2013). MicroRNA-497 targets insulin-like growth factor 1 receptor and has a tumour suppressive role in human colorectal cancer. Oncogene 32, 1910-1920. doi: 10.1038/onc.2012.214
29. He, Z., Cen, D., Luo, X., Li, D., Li, P., Liang, L.,et al. (2013). Downregulation of miR-383 promotes glioma cell invasion by targeting insulin-like growth factor 1 receptor. Med. Oncol. 30:557. doi: 10.1007/s12032-013-0557-0
30. Hobert, O. (2008). Gene regulation by transcription factors and microRNAs. Science 319, 1785-1786. doi: 10.1126/science.1151651
31. Hong, M., and Lee, V. M. (1997). Insulin and insulin-like growth factor-1 regulate tau phosphorylation in cultured human neurons. J. Biol. Chem. 272, 19547-19553. doi: 10.1074/jbc.272.31.19547
32. Hresko, R. C., and Mueckler, M. (2005). mTOR.RICTOR is the Ser473 kinase for Akt/protein kinase B in 3T3-L1 adipocytes. J. Biol. Chem. 280, 40406-40416. doi: 10.1074/jbc. M508361200
33. Hu, Y. K., Wang, X., Li, L., Du, Y. H., Ye, H. T., and Li, C. Y. (2013). MicroRNA-98 induces an Alzheimer's disease-like disturbance by targeting insulin-like growth factor 1. Neurosci. Bull. 29, 745-751. doi: 10.1007/s12264-013-1348-5
34. Hyun, S., Lee, J. H., Jin, H., Nam, J., Namkoong, B., Lee, G.,et al. (2009). Conserved MicroRNA miR-8/miR-200 and its target USH/FOG2 control growth by regulating PI3K. Cell 139, 1096-1108. doi: 10.1016/j.cell.2009.11.020
35. Jia, C. Y., Li, H. H., Zhu, X. C., Dong, Y. W., Fu, D., Zhao, Q. L.,et al. (2011). MiR-223 suppresses cell proliferation by targeting IGF-1R. PLoS ONE 6:e27008. doi: 10.1371/journal.pone.0027008
36. Jiang, L., Liu, X., Chen, Z., Jin, Y., Heidbreder, C. E., Kolokythas, A.,et al. (2010). MicroRNA-7 targets IGF1R (insulin-like growth factor 1 receptor) in tongue squamous cell carcinoma cells. Biochem. J. 432, 199-205. doi: 10.1042/BJ20100859
37. Jin, Y., Tymen, S. D., Chen, D., Fang, Z. J., Zhao, Y., Dragas, D.,et al. (2013). MicroRNA-99 family targets AKT/mTOR signaling pathway in dermal wound healing. PLoS ONE 8:e64434. doi: 10.1371/journal.pone.0064434
38. Jones, K. B., Salah, Z., Del Mare, S., Galasso, M., Gaudio, E., Nuovo, G. J.,et al. (2012). miRNA signatures associate with pathogenesis and progression of osteosarcoma. Cancer Res. 72, 1865-1877. doi: 10.1158/0008-5472.CAN-11-2663
39. Jung, H. J., and Suh, Y. (2012). MicroRNA in aging: from discovery to biology. Curr. Genomics 13, 548-557. doi: 10.2174/138920212803251436
40. Jung, H. J., and Suh, Y. (2014). Circulating miRNAs in ageing and ageing-related diseases. J. Genet. Genomics 41, 465-472. doi: 10.1016/j.jgg.2014.07.003
41. Kang, J., Lee, S. Y., Lee, S. Y., Kim, Y. J., Park, J. Y., Kwon, S. J.,et al. (2012). microRNA-99b acts as a tumor suppressor in non-small cell lung cancer by directly targeting fibroblast growth factor receptor 3. Exp. Ther. Med. 3, 149-153. doi: 10.3892/etm.2011.366
42. Karp, D. D., Pollak, M. N., Cohen, R. B., Eisenberg, P. D., Haluska, P., Yin, D.,et al. (2009). Safety, pharmacokinetics, and pharmacodynamics of the insulin-like growth factor type 1 receptor inhibitor figitumumab (CP-751,871) in combination with paclitaxel and carboplatin. J. Thorac. Oncol. 4, 1397-1403. doi: 10.1097/JTO.0b013e3181ba2f1d
43. Kefas, B., Godlewski, J., Comeau, L., Li, Y., Abounader, R., Hawkinson, M.,et al. (2008). microRNA-7 inhibits the epidermal growth factor receptor and the Akt pathway and is down-regulated in glioblastoma. Cancer Res. 68, 3566-3572. doi: 10.1158/0008-5472.CAN-07-6639
44. Keniry, A., Oxley, D., Monnier, P., Kyba, M., Dandolo, L., Smits, G.,et al. (2012). The H19 lincRNA is a developmental reservoir of miR-675 that suppresses growth and Igf1r. Nat. Cell Biol. 14, 659-665. doi: 10.1038/ncb2521
45. Kenyon, C. J. (2010). The genetics of ageing. Nature 464, 504-512. doi: 10.1038/nature08980
46. Kimura, K. D., Tissenbaum, H. A., Liu, Y., and Ruvkun, G. (1997). daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 277, 942-946. doi: 10.1126/science.277.5328.942
47. Knezevic, I., Patel, A., Sundaresan, N. R., Gupta, M. P., Solaro, R. J., Nagalingam, R. S.,et al. (2012). A novel cardiomyocyte-enriched microRNA, miR-378, targets insulin-like growth factor 1 receptor: implications in postnatal cardiac remodeling and cell survival. J. Biol. Chem. 287, 12913-12926. doi: 10.1074/jbc. M111.331751
48. Kumar, M. S., Erkeland, S. J., Pester, R. E., Chen, C. Y., Ebert, M. S., Sharp, P. A.,et al. (2008). Suppression of non-small cell lung tumor development by the let-7 microRNA family. Proc. Natl. Acad. Sci. U.S.A. 105, 3903-3908. doi: 10.1073/pnas.0712321105
49. Laios, A., O'Toole, S., Flavin, R., Martin, C., Kelly, L., Ring, M.,et al. (2008). Potential role of miR-9 and miR-223 in recurrent ovarian cancer. Mol. Cancer 7:35. doi: 10.1186/1476-4598-7-35
50. Lanford, R. E., Hildebrandt-Eriksen, E. S., Petri, A., Persson, R., Lindow, M., Munk, M. E.,et al. (2010). Therapeutic silencing of microRNA-122 in primates with chronic hepatitis C virus infection. Science 327, 198-201. doi: 10.1126/science.1178178
51. Lara, P. C., Bordon, E., Rey, A., Moreno, M., Lloret, M., and Henriquez-Hernandez, L. A. (2011). IGF-1R expression predicts clinical outcome in patients with locally advanced oral squamous cell carcinoma. Oral Oncol. 47, 615-619. doi: 10.1016/j.oraloncology.2011.05.005
52. Law, P. T., Ching, A. K., Chan, A. W., Wong, Q. W., Wong, C. K., To, K. F.,et al. (2012). MiR-145 modulates multiple components of the insulin-like growth factor pathway in hepatocellular carcinoma. Carcinogenesis 33, 1134-1141. doi: 10.1093/carcin/bgs130
53. Lee, E. K., and Gorospe, M. (2010). Minireview: posttranscriptional regulation of the insulin and insulin-like growth factor systems. Endocrinology 151, 1403-1408. doi: 10.1210/en.2009-1123
54. Lerman, G., Avivi, C., Mardoukh, C., Barzilai, A., Tessone, A., Gradus, B.,et al. (2011). MiRNA expression in psoriatic skin: reciprocal regulation of hsa-miR-99a and IGF-1R. PLoS ONE 6:e20916. doi: 10.1371/journal.pone.0020916
55. Lewis, B. P., Burge, C. B., and Bartel, D. P. (2005). Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120, 15-20. doi: 10.1016/j.cell.2004.12.035
56. Li, D., Liu, X., Lin, L., Hou, J., Li, N., Wang, C.,et al. (2011). MicroRNA-99a inhibits hepatocellular carcinoma growth and correlates with prognosis of patients with hepatocellular carcinoma. J. Biol. Chem. 286, 36677-36685. doi: 10.1074/jbc. M111.270561
57. Li, Z., and Rana, T. M. (2014). Therapeutic targeting of microRNAs: current status and future challenges. Nat. Rev. Drug Discov. 13, 622-638. doi: 10.1038/nrd4359
58. Liang, R., Khanna, A., Muthusamy, S., Li, N., Sarojini, H., Kopchick, J. J.,et al. (2011). Post-transcriptional regulation of IGF1R by key microRNAs in long-lived mutant mice. Aging Cell 10, 1080-1088. doi: 10.1111/j.1474-9726.2011.00751.x
59. Lin, H., Dai, T., Xiong, H., Zhao, X., Chen, X., Yu, C.,et al. (2010). Unregulated miR-96 induces cell proliferation in human breast cancer by downregulating transcriptional factor FOXO3a. PLoS ONE 5:e15797. doi: 10.1371/journal.pone.0015797
60. Liu, X., Jiang, L., Wang, A., Yu, J., Shi, F., and Zhou, X. (2009a). MicroRNA-138 suppresses invasion and promotes apoptosis in head and neck squamous cell carcinoma cell lines. Cancer Lett. 286, 217-222. doi: 10.1016/j.canlet.2009.05.030
61. Liu, X., Yu, J., Jiang, L., Wang, A., Shi, F., Ye, H.,et al. (2009b). MicroRNA-222 regulates cell invasion by targeting matrix metalloproteinase 1 (MMP1) and manganese superoxide dismutase 2 (SOD2) in tongue squamous cell carcinoma cell lines. Cancer Genomics Proteomics 6, 131-139.
62. Llave, C., Xie, Z., Kasschau, K. D., and Carrington, J. C. (2002). Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 297, 2053-2056. doi: 10.1126/science.1076311
63. Lujambio, A., Ropero, S., Ballestar, E., Fraga, M. F., Cerrato, C., Setien, F.,et al. (2007). Genetic unmasking of an epigenetically silenced microRNA in human cancer cells. Cancer Res. 67, 1424-1429. doi: 10.1158/0008-5472.CAN-06-4218
64. Luo, M., Shen, D., Zhou, X., Chen, X., and Wang, W. (2013). MicroRNA-497 is a potential prognostic marker in human cervical cancer and functions as a tumor suppressor by targeting the insulin-like growth factor 1 receptor. Surgery 153, 836-847. doi: 10.1016/j.surg.2012.12.004
65. Marson, A., Levine, S. S., Cole, M. F., Frampton, G. M., Brambrink, T., Johnstone, S.,et al. (2008). Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell 134, 521-533. doi: 10.1016/j.cell.2008.07.020
66. Martinez, N. J., Ow, M. C., Barrasa, M. I., Hammell, M., Sequerra, R., Doucette-Stamm, L.,et al. (2008). A C. elegans genome-scale microRNA network contains composite feedback motifs with high flux capacity. Genes Dev. 22, 2535-2549. doi: 10.1101/gad.1678608
67. Mellios, N., Woodson, J., Garcia, R. I., Crawford, B., Sharma, J., Sheridan, S. D.,et al. (2014). b2-Adrenergic receptor agonist ameliorates phenotypes and corrects microRNA-mediated IGF1 deficits in a mouse model of Rett syndrome. Proc. Natl. Acad. Sci. U.S.A. 111, 9947-9952. doi: 10.1073/pnas.1309426111
68. Milman, S., Atzmon, G., Huffman, D. M., Wan, J., Crandall, J. P., Cohen, P.,et al. (2014). Low insulin-like growth factor-1 level predicts survival in humans with exceptional longevity. Aging Cell 13, 769-771. doi: 10.1111/acel.12213
69. Olivieri, F., Ahtiainen, M., Lazzarini, R., Pollanen, E., Capri, M., Lorenzi, M.,et al. (2014). Hormone replacement therapy enhances IGF-1 signaling in skeletal muscle by diminishing miR-182 and miR-223 expressions: a study on postmenopausal monozygotic twin pairs. Aging Cell 13, 850-861. doi: 10.1111/acel.12245
70. O'Neill, C., Kiely, A. P., Coakley, M. F., Manning, S., and Long-Smith, C. M. (2012). Insulin and IGF-1 signalling: longevity, protein homoeostasis and Alzheimer's disease. Biochem. Soc. Trans. 40, 721-727. doi: 10.1042/BST20120080
71. Peng, Y., Dai, Y., Hitchcock, C., Yang, X., Kassis, E. S., Liu, L.,et al. (2013). Insulin growth factor signaling is regulated by microRNA-486, an underexpressed microRNA in lung cancer. Proc. Natl. Acad. Sci. U.S.A. 110, 15043-15048. doi: 10.1073/pnas.1307107110
72. Piccirillo, R., Demontis, F., Perrimon, N., and Goldberg, A. L. (2014). Mechanisms of muscle growth and atrophy in mammals and Drosophila. Dev. Dyn. 243, 201-215. doi: 10.1002/dvdy.24036
73. Pini, G., Scusa, M. F., Congiu, L., Benincasa, A., Morescalchi, P., Bottiglioni, I.,et al. (2012). IGF1 as a potential treatment for Rett syndrome: safety assessment in six Rett patients. Autism Res. Treat. 2012:679801. doi: 10.1155/2012/679801
74. Pitts, T. M., Tan, A. C., Kulikowski, G. N., Tentler, J. J., Brown, A. M., Flanigan, S. A.,et al. (2010). Development of an integrated genomic classifier for a novel agent in colorectal cancer: approach to individualized therapy in early development. Clin. Cancer Res. 16, 3193-3204. doi: 10.1158/1078-0432.CCR-09-3191
75. Pollak, M. (2008). Insulin and insulin-like growth factor signalling in neoplasia. Nat. Rev. Cancer 8, 915-928. doi: 10.1038/nrc2536
76. Raemdonck, K., Vandenbroucke, R. E., Demeester, J., Sanders, N. N., and De Smedt, S. C. (2008). Maintaining the silence: reflections on long-term RNAi. Drug Discov. Today 13, 917-931. doi: 10.1016/j.drudis.2008.06.008
77. Ramalingam, S. S., Spigel, D. R., Chen, D., Steins, M. B., Engelman, J. A., Schneider, C. P.,et al. (2011). Randomized phase II study of erlotinib in combination with placebo or R1507, a monoclonal antibody to insulin-like growth factor-1 receptor, for advanced-stage non-small-cell lung cancer. J. Clin. Oncol. 29, 4574-4580. doi: 10.1200/JCO.2011.36.6799
78. Rathod, S. S., Rani, S. B., Khan, M., Muzumdar, D., and Shiras, A. (2014). Tumor suppressive miRNA-34a suppresses cell proliferation and tumor growth of glioma stem cells by targeting Akt and Wnt signaling pathways. FEBS Open Bio 4, 485-495. doi: 10.1016/j.fob.2014.05.002
79. Reidy-Lagunes, D. L., Vakiani, E., Segal, M. F., Hollywood, E. M., Tang, L. H., Solit, D. B.,et al. (2012). A phase 2 study of the insulin-like growth factor-1 receptor inhibitor MK-0646 in patients with metastatic, well-differentiated neuroendocrine tumors. Cancer 118, 4795-4800. doi: 10.1002/cncr.27459
80. Roy, S., Levi, E., Majumdar, A. P., and Sarkar, F. H. (2012). Expression of miR-34 is lost in colon cancer which can be re-expressed by a novel agent CDF. J. Hematol. Oncol. 5:58. doi: 10.1186/1756-8722-5-58
81. Saugstad, J. A. (2010). MicroRNAs as effectors of brain function with roles in ischemia and injury, neuroprotection, and neurodegeneration. J. Cereb. Blood Flow Metab. 30, 1564-1576. doi: 10.1038/jcbfm.2010.101
82. Sayed, D., Hong, C., Chen, I. Y., Lypowy, J., and Abdellatif, M. (2007). MicroRNAs play an essential role in the development of cardiac hypertrophy. Circ. Res. 100, 416-424. doi: 10.1161/01.RES.0000257913.42552.23
83. Scagliotti, G. V., and Novello, S. (2012). The role of the insulin-like growth factor signaling pathway in non-small cell lung cancer and other solid tumors. Cancer Treat. Rev. 38, 292-302. doi: 10.1016/j.ctrv.2011.07.008
84. Scartozzi, M., Bianconi, M., Maccaroni, E., Giampieri, R., Berardi, R., and Cascinu, S. (2010). Dalotuzumab, a recombinant humanized mAb targeted against IGFR1 for the treatment of cancer. Curr. Opin. Mol. Ther. 12, 361-371.
85. Sekharam, M., Zhao, H., Sun, M., Fang, Q., Zhang, Q., Yuan, Z.,et al. (2003). Insulin-like growth factor 1 receptor enhances invasion and induces resistance to apoptosis of colon cancer cells through the Akt/Bcl-xL pathway. Cancer Res. 63, 7708-7716.
86. Shi, B., Sepp-Lorenzino, L., Prisco, M., Linsley, P., Deangelis, T., and Baserga, R. (2007). Micro RNA 145 targets the insulin receptor substrate-1 and inhibits the growth of colon cancer cells. J. Biol. Chem. 282, 32582-32590. doi: 10.1074/jbc. M702806200
87. Small, E. M., and Olson, E. N. (2011). Pervasive roles of microRNAs in cardiovascular biology. Nature 469, 336-342. doi: 10.1038/nature09783
88. Smith-Vikos, T., and Slack, F. J. (2012). MicroRNAs and their roles in aging. J. Cell Sci. 125, 7-17. doi: 10.1242/jcs.099200
89. Stylianopoulos, T., and Jain, R. K. (2013). Combining two strategies to improve perfusion and drug delivery in solid tumors. Proc. Natl. Acad. Sci. U.S.A. 110, 18632-18637. doi: 10.1073/pnas.1318415110
90. Su, H., Yang, J. R., Xu, T., Huang, J., Xu, L., Yuan, Y.,et al. (2009). MicroRNA-101, down-regulated in hepatocellular carcinoma, promotes apoptosis and suppresses tumorigenicity. Cancer Res. 69, 1135-1142. doi: 10.1158/0008-5472.CAN-08-2886
91. Tamimi, R. M., Colditz, G. A., Wang, Y., Collins, L. C., Hu, R., Rosner, B.,et al. (2011). Expression of IGF1R in normal breast tissue and subsequent risk of breast cancer. Breast Cancer Res. Treat. 128, 243-250. doi: 10.1007/s10549-010-1313-1
92. Tatar, M., Kopelman, A., Epstein, D., Tu, M. P., Yin, C. M., and Garofalo, R. S. (2001). A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function. Science 292, 107-110. doi: 10.1126/science.1057987
93. Tazearslan, C., Huang, J., Barzilai, N., and Suh, Y. (2011). Impaired IGF1R signaling in cells expressing longevity-associated human IGF1R alleles. Aging Cell 10, 551-554. doi: 10.1111/j.1474-9726.2011.00697.x
94. Tognon, C. E., and Sorensen, P. H. (2012). Targeting the insulin-like growth factor 1 receptor (IGF1R) signaling pathway for cancer therapy. Expert Opin. Ther. Targets 16, 33-48. doi: 10.1517/14728222.2011.638626
95. Toyota, M., Suzuki, H., Sasaki, Y., Maruyama, R., Imai, K., Shinomura, Y.,et al. (2008). Epigenetic silencing of microRNA-34b/c and B-cell translocation gene 4 is associated with CpG island methylation in colorectal cancer. Cancer Res. 68, 4123-4132. doi: 10.1158/0008-5472.CAN-08-0325
96. Uesugi, A., Kozaki, K., Tsuruta, T., Furuta, M., Morita, K., Imoto, I.,et al. (2011). The tumor suppressive microRNA miR-218 targets the mTOR component Rictor and inhibits AKT phosphorylation in oral cancer. Cancer Res. 71, 5765-5778. doi: 10.1158/0008-5472.CAN-11-0368
97. van Dongen, S., Abreu-Goodger, C., and Enright, A. J. (2008). Detecting microRNA binding and siRNA off-target effects from expression data. Nat. Methods 5, 1023-1025. doi: 10.1038/nmeth.1267
98. Vargas, T., Martinez-Garcia, A., Antequera, D., Vilella, E., Clarimon, J., Mateo, I.,et al. (2011). IGF-I gene variability is associated with an increased risk for AD. Neurobiol. Aging 32, 556.e3-556.e11. doi: 10.1016/j.neurobiolaging.2010.10.017
99. Velloso, C. P. (2008). Regulation of muscle mass by growth hormone and IGF-I. Br. J. Pharmacol. 154, 557-568. doi: 10.1038/bjp.2008.153
100. Wang, L., Chang, L., Li, Z., Gao, Q., Cai, D., Tian, Y.,et al. (2014a). miR-99a and -99b inhibit cervical cancer cell proliferation and invasion by targeting mTOR signaling pathway. Med. Oncol. 31:934. doi: 10.1007/s12032-014-0934-3
101. Wang, X., Wang, Y., Lan, H., and Li, J. (2014b). miR-195 inhibits the growth and metastasis of NSCLC cells by targeting IGF1R. Tumour Biol. 35, 8765-8770. doi: 10.1007/s13277-014-2140-5
102. Wang, X., Liu, P., Zhu, H., Xu, Y., Ma, C., Dai, X.,et al. (2009). miR-34a, a microRNA up-regulated in a double transgenic mouse model of Alzheimer's disease, inhibits bcl2 translation. Brain Res. Bull. 80, 268-273. doi: 10.1016/j.brainresbull.2009.08.006
103. Wang, B., Wang, H., and Yang, Z. (2012). MiR-122 inhibits cell proliferation and tumorigenesis of breast cancer by targeting IGF1R. PLoS ONE 7:e47053. doi: 10.1371/journal.pone.0047053
104. Weber, M. M., Fottner, C., Liu, S. B., Jung, M. C., Engelhardt, D., and Baretton, G. B. (2002). Overexpression of the insulin-like growth factor I receptor in human colon carcinomas. Cancer 95, 2086-2095. doi: 10.1002/cncr.10945
105. Welsh, G. I., Miller, C. M., Loughlin, A. J., Price, N. T., and Proud, C. G. (1998). Regulation of eukaryotic initiation factor eIF2B: glycogen synthase kinase-3 phosphorylates a conserved serine which undergoes dephosphorylation in response to insulin. FEBS Lett. 421, 125-130. doi: 10.1016/S0014-5793(97)01548-2
106. Wilting, S. M., Van Boerdonk, R. A., Henken, F. E., Meijer, C. J., Diosdado, B., Meijer, G. A.,et al. (2010). Methylation-mediated silencing and tumour suppressive function of hsa-miR-124 in cervical cancer. Mol. Cancer 9:167. doi: 10.1186/1476-4598-9-167
107. Wu, Z., Sun, H., Zeng, W., He, J., and Mao, X. (2012). Upregulation of MircoRNA-370 induces proliferation in human prostate cancer cells by downregulating the transcription factor FOXO1. PLoS ONE 7:e45825. doi: 10.1371/journal.pone.0045825
108. Xu, Q., Jiang, Y., Yin, Y., Li, Q., He, J., Jing, Y.,et al. (2013). A regulatory circuit of miR-148a/152 and DNMT1 in modulating cell transformation and tumor angiogenesis through IGF-IR and IRS1. J. Mol. Cell Biol. 5, 3-13. doi: 10.1093/jmcb/mjs049
109. Yan, B., Fu, Q., Lai, L., Tao, X., Fei, Y., Shen, J.,et al. (2012). Downregulation of microRNA 99a in oral squamous cell carcinomas contributes to the growth and survival of oral cancer cells. Mol. Med. Rep. 6, 675-681. doi: 10.3892/mmr.2012.971
110. Yang, B., Lin, H., Xiao, J., Lu, Y., Luo, X., Li, B.,et al. (2007). The muscle-specific microRNA miR-1 regulates cardiac arrhythmogenic potential by targeting GJA1 and KCNJ2. Nat. Med. 13, 486-491. doi: 10.1038/nm1569
111. Yen, Y. C., Shiah, S. G., Chu, H. C., Hsu, Y. M., Hsiao, J. R., Chang, J. Y.,et al. (2014). Reciprocal regulation of microRNA-99a and insulin-like growth factor I receptor signaling in oral squamous cell carcinoma cells. Mol. Cancer 13:6. doi: 10.1186/1476-4598-13-6
112. Yi, R., O'Carroll, D., Pasolli, H. A., Zhang, Z., Dietrich, F. S., Tarakhovsky, A.,et al. (2006). Morphogenesis in skin is governed by discrete sets of differentially expressed microRNAs. Nat. Genet. 38, 356-362. doi: 10.1038/ng1744
113. Yu, T., Li, J., Yan, M., Liu, L., Lin, H., Zhao, F.,et al. (2014). MicroRNA-193a-3p and -5p suppress the metastasis of human non-small-cell lung cancer by downregulating the ERBB4/PIK3R3/mTOR/S6K2 signaling pathway. Oncogene doi: 10.1038/onc.2013.574 [Epub ahead of print].
114. Yuen, J. S., and Macaulay, V. M. (2008). Targeting the type 1 insulin-like growth factor receptor as a treatment for cancer. Expert Opin. Ther. Targets 12, 589-603. doi: 10.1517/14728222.12.5.589
115. Zemva, J., and Schubert, M. (2011). Central insulin and insulin-like growth factor-1 signaling: implications for diabetes associated dementia. Curr. Diabetes Rev. 7, 356-366. doi: 10.2174/157339911797415594
116. Zha, J., and Lackner, M. R. (2010). Targeting the insulin-like growth factor receptor-1R pathway for cancer therapy. Clin. Cancer Res. 16, 2512-2517. doi: 10.1158/1078-0432.CCR-09-2232
117. Zhao, Y., Ransom, J. F., Li, A., Vedantham, V., Von Drehle, M., Muth, A. N.,et al. (2007). Dysregulation of cardiogenesis, cardiac conduction, and cell cycle in mice lacking miRNA-1-2. Cell 129, 303-317. doi: 10.1016/j.cell.2007.03.030
118. Zhu, H., Shyh-Chang, N., Segre, A. V., Shinoda, G., Shah, S. P., Einhorn, W. S.,et al. (2011). The Lin28/let-7 axis regulates glucose metabolism. Cell 147, 81-94. doi: 10.1016/j.cell.2011.08.033
119. Zhu, Z., Xu, T., Wang, L., Wang, X., Zhong, S., Xu, C.,et al. (2014). MicroRNA-145 directly targets the insulin-like growth factor receptor I in human bladder cancer cells. FEBS Lett. 588, 3180-3185. doi: 10.1016/j.febslet.2014.06.059