Down-regulation of miR-129-5p and the let-7 family in neuroendocrine tumors and metastases leads to up-regulation of their targets Egr1, G3bp1, Hmga2 and Bach1

Genes

Volumn 6, Issue 1, 2015, Pages

  Døssing, Kristina B V ^a   Binderup, Tina ^a,b   Kaczkowski, Bogumil ^c   Jacobsen, Anders ^c,d   Rossing, Maria ^a   Winther, Ole ^e   Federspiel, Birgitte ^a   Knigge, Ulrich ^b,f   Kjær, Andreas ^a,b   Friis Hansen, Lennart ^a,g  

^a Rigshospitalet   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^e TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^f UNIVERSITY OF COPENHAGEN   (Denmark)

^g NAESTVED HOSPITAL   (Denmark)

Author keywords

BACH1; Cancer; EGR1; G3BP1; HMGA2; Let 7; MiR 129 5p; MMP1; Neuroendocrine tumors

Indexed keywords

BACH1 PROTEIN; EARLY GROWTH RESPONSE FACTOR 1; G3BP1 PROTEIN; HIGH MOBILITY GROUP A2 PROTEIN; INTERSTITIAL COLLAGENASE; MICRORNA; MICRORNA 129; PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; BONE METASTASIS; CARCINOGENESIS; CLINICAL ARTICLE; CONTROLLED STUDY; DOWN REGULATION; GROWTH INHIBITION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LUCIFERASE ASSAY; METASTASIS; NEUROENDOCRINE TUMOR; POLYMERASE CHAIN REACTION; PRIMARY TUMOR; PROTEIN CONTENT; PROTEIN EXPRESSION; PROTEIN TARGETING; UPREGULATION; WESTERN BLOTTING;

EID: 84920260820     PISSN: None     EISSN: 20734425     Source Type: Journal    
DOI: 10.3390/genes6010001     Document Type: Article

References (64)

1. Modlin, I.M.; Oberg, K.; Chung, D.C.; Jensen, R.T.; de Herder, W.W.; Thakker, R.V.; Caplin, M.; Delle Fave, G.; Kaltsas, G.A.; Krenning, E.P.; et al. Gastroenteropancreatic neuroendocrine tumours. Lancet Oncol. 2008, 9, 61–72.
2. Kloppel, G. Classification and pathology of gastroenteropancreatic neuroendocrine neoplasms. Endocr.-Relat. Cancer 2011, 18 (Suppl 1), S1–S16.
3. Lee, D.J.; Modlin, R.L. DNA transportation authority. Nat. Med. 2008, 14, 1319–1320.
4. Hanahan, D.; Weinberg, R.A. Hallmarks of cancer: The next generation. Cell 2011, 144, 646–674.
5. Sebolt-Leopold, J.S. Advances in the development of cancer therapeutics directed against the ras-mitogen-activated protein kinase pathway. Clin. Cancer Res. 2008, 14, 3651–3656.
6. Gysin, S.; Salt, M.; Young, A.; McCormick, F. Therapeutic strategies for targeting ras proteins. Genes Cancer 2011, 2, 359–372.
7. Grewal, T.; Koese, M.; Tebar, F.; Enrich, C. Differential regulation of rasgaps in cancer. Genes Cancer 2011, 2, 288–297.
8. Pazman, C.; Mayes, C.A.; Fanto, M.; Haynes, S.R.; Mlodzik, M. Rasputin, the drosophila homologue of the rasgap sh3 binding protein, functions in ras- and rho-mediated signaling. Development 2000, 127, 1715–1725.
9. Irvine, K.; Stirling, R.; Hume, D.; Kennedy, D. Rasputin, more promiscuous than ever: A review of g3bp. Int. J. Dev. Biol. 2004, 48, 1065–1077.
10. Li, W.M.; Barnes, T.; Lee, C.H. Endoribonucleases—Enzymes gaining spotlight in mRNA metabolism. FEBS J. 2010, 277, 627–641.
11. Pagel, J.I.; Deindl, E. Early growth response 1—a transcription factor in the crossfire of signal tranduction cascades. Indian J. Biochem. Biophys. 2011, 48, 226–235.
12. Arvidsson, Y.; Bergstrom, A.; Arvidsson, L.; Kristiansson, E.; Ahlman, H.; Nilsson, O. Hypoxia stimulates cxcr4 signalling in ileal carcinoids. Endoc.-Relat. Cancer 2010, 17, 303–316.
13. Dangi-Garimella, S.; Yun, J.; Eves, E.M.; Newman, M.; Erkeland, S.J.; Hammond, S.M.; Minn, A.J.; Rosner, M.R. Raf kinase inhibitory protein suppresses a metastasis signalling cascade involving lin28 and let-7. EMBO J. 2009, 28, 347–358.
14. Yun, J.; Frankenberger, C.A.; Kuo, W.L.; Boelens, M.C.; Eves, E.M.; Cheng, N.; Liang, H.; Li, W.H.; Ishwaran, H.; Minn, A.J.; et al. Signalling pathway for rkip and let-7 regulates and predicts metastatic breast cancer. EMBO J. 2011, 30, 4500–4514.
15. Kato, M.; Slack, F.J. MicroRNAs: Small molecules with big roles—C. Elegans to human cancer. Biol. Cell 2008, 100, 71–81.
16. Guo, H.; Ingolia, N.T.; Weissman, J.S.; Bartel, D.P. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 2010, 466, 835–840. 17. Cho, W.C. Oncomirs: The discovery and progress of microRNAs in cancers. Mol. Cancer 2007, 6, e60.
17. Esquela-Kerscher, A.; Slack, F.J. Oncomirs—MicroRNAs with a role in cancer. Nat. Rev. Cancer 2006, 6, 259–269.
18. Van Buren, G., 2nd; Rashid, A.; Yang, A.D.; Abdalla, E.K.; Gray, M.J.; Liu, W.; Somcio, R.; Fan, F.; Camp, E.R.; Yao, J.C.; et al. The development and characterization of a human midgut carcinoid cell line. Clin. Cancer Res. 2007, 13, 4704–4712.
19. Peltier, H.J.; Latham, G.J. Normalization of microRNA expression levels in quantitative rt-pcr assays: Identification of suitable reference RNA targets in normal and cancerous human solid tissues. RNA 2008, 14, 844–852.
20. Jorgensen, S.; Baker, A.; Moller, S.; Nielsen, B.S. Robust one-day in situ hybridization protocol for detection of microRNAs in paraffin samples using lna probes. Methods 2010, 52, 375–381.
21. Kustermann, S.; Boess, F.; Buness, A.; Schmitz, M.; Watzele, M.; Weiser, T.; Singer, T.; Suter, L.; Roth, A.B. A label-free, impedance-based real time assay to identify drug-induced toxicities and differentiate cytostatic from cytotoxic effects. Toxicol. In Vitro 2012, 27, 1589–1595.
22. Ke, N.; Wang, X.; Xu, X.; Abassi, Y.A. The xcelligence system for real-time and label-free monitoring of cell viability. Methods Mol. Biol. 2011, 740, 33–43.
23. Gentleman, R.C.; Carey, V.J.; Bates, D.M.; Bolstad, B.; Dettling, M.; Dudoit, S.; Ellis, B.; Gautier, L.; Ge, Y.; Gentry, J.; et al. Bioconductor: Open software development for computational biology and bioinformatics. Genome Biol. 2004, 5, eR80.
24. Gregersen, L.H.; Jacobsen, A.B.; Frankel, L.B.; Wen, J.; Krogh, A.; Lund, A.H. MicroRNA-145 targets yes and stat1 in colon cancer cells. PLOS ONE 2010, 5, e8836.
25. Jacobsen, A.; Wen, J.; Marks, D.S.; Krogh, A. Signatures of RNA binding proteins globally coupled to effective microRNA target sites. Genome Res. 2010, 20, 1010–1019.
26. Hwang, H.W.; Wentzel, E.A.; Mendell, J.T. Cell-cell contact globally activates microRNA biogenesis. Proc. Natl. Acad. Sci. USA 2009, 106, 7016–7021.
27. Hori, T.; Yasuda, T.; Suzuki, K.; Kanamori, M.; Kimura, T. Skeletal metastasis of carcinoid tumors: Two case reports and review of the literature. Oncol. Lett. 2012, 3, 1105–1108.
28. Baron, V.; Adamson, E.D.; Calogero, A.; Ragona, G.; Mercola, D. The transcription factor egr1 is a direct regulator of multiple tumor suppressors including tgfbeta1, pten, p53, and fibronectin. Cancer Gene Ther. 2006, 13, 115–124.
29. Grimson, A.; Farh, K.K.; Johnston, W.K.; Garrett-Engele, P.; Lim, L.P.; Bartel, D.P. MicroRNA targeting specificity in mammals: Determinants beyond seed pairing. Mol. Cell 2007, 27, 91–105.
30. Yao, J.C.; Hassan, M.; Phan, A.; Dagohoy, C.; Leary, C.; Mares, J.E.; Abdalla, E.K.; Fleming, J.B.; Vauthey, J.N.; Rashid, A.; et al. One hundred years after "carcinoid": Epidemiology of and prognostic factors for neuroendocrine tumors in 35,825 cases in the united states. J. Clin. Oncol. 2008, 26, 3063–3072.
31. Bevilacqua, E.; Frankenberger, C.A.; Rosner, M.R. Rkip suppresses breast cancer metastasis to the bone by regulating stroma-associated genes. Int. J. Breast Cancer 2012, 2012, e124704.
32. Ruebel, K.; Leontovich, A.A.; Stilling, G.A.; Zhang, S.; Righi, A.; Jin, L.; Lloyd, R.V. MicroRNA expression in ileal carcinoid tumors: Downregulation of microRNA-133a with tumor progression. Modern Pathol. 2010, 23, 367–375.
33. Wang, B.; Howel, P.; Bruheim, S.; Ju, J.; Owen, L.B.; Fodstad, O.; Xi, Y. Systematic evaluation of three microRNA profiling platforms: Microarray, beads array, and quantitative real-time PCR array. PLOS ONE 2011, 6, e17167.
34. Camarillo, C.; Swerdel, M.; Hart, R.P. Comparison of microarray and quantitative real-time PCR methods for measuring microRNA levels in msc cultures. Methods Mol. Biol. 2011, 698, 419–429.
35. Karaayvaz, M.; Zhai, H.; Ju, J. Mir-129 promotes apoptosis and enhances chemosensitivity to 5-fluorouracil in colorectal cancer. Cell Death Dis. 2013, 4, e659.
36. Tsai, K.W.; Wu, C.W.; Hu, L.Y.; Li, S.C.; Liao, Y.L.; Lai, C.H.; Kao, H.W.; Fang, W.L.; Huang, K.H.; Chan, W.C.; et al. Epigenetic regulation of mir-34b and mir-129 expression in gastric cancer. Int. J. Cancer 2011, 129, 2600–2610.
37. Dyrskjot, L.; Ostenfeld, M.S.; Bramsen, J.B.; Silahtaroglu, A.N.; Lamy, P.; Ramanathan, R.; Fristrup, N.; Jensen, J.L.; Andersen, C.L.; Zieger, K.; et al. Genomic profiling of microRNAs in bladder cancer: Mir-129 is associated with poor outcome and promotes cell death in vitro. Cancer Res. 2009, 69, 4851–4860.
38. Bandres, E.; Agirre, X.; Bitarte, N.; Ramirez, N.; Zarate, R.; Roman-Gomez, J.; Prosper, F.; Garcia-Foncillas, J. Epigenetic regulation of microRNA expression in colorectal cancer. Int. J. Cancer 2009, 125, 2737–2743.
39. Wu, J.; Qian, J.; Li, C.; Kwok, L.; Cheng, F.; Liu, P.; Perdomo, C.; Kotton, D.; Vaziri, C.; Anderlind, C.; et al. Mir-129 regulates cell proliferation by downregulating cdk6 expression. Cell Cycle 2010, 9, 1809–1818.
40. Pignatelli, M.; Luna-Medina, R.; Perez-Rendon, A.; Santos, A.; Perez-Castillo, A. The transcription factor early growth response factor-1 (egr-1) promotes apoptosis of neuroblastoma cells. Biochem. J. 2003, 373, 739–746.
41. Zheng, L.; Pu, J.; Jiang, G.; Weng, M.; He, J.; Mei, H.; Hou, X.; Tong, Q. Abnormal expression of early growth response 1 in gastric cancer: Association with tumor invasion, metastasis and heparanase transcription. Pathol. Int. 2010, 60, 268–277.
42. Gitenay, D.; Baron, V.T. Is egr1 a potential target for prostate cancer therapy? Future Oncol. 2009, 5, 993–1003.
43. Edfeldt, K.; Bjorklund, P.; Akerstrom, G.; Westin, G.; Hellman, P.; Stalberg, P. Different gene expression profiles in metastasizing midgut carcinoid tumors. Endoc.-Relat. Cancer 2011, 18, 479–489.
44. Silverman, E.S.; Collins, T. Pathways of egr-1-mediated gene transcription in vascular biology. Am. J. Pathol. 1999, 154, 665–670.
45. Thiel, G.; Cibelli, G. Regulation of life and death by the zinc finger transcription factor egr-1. J. Cell. Physiol. 2002, 193, 287–292.
46. Karhoff, D.; Sauer, S.; Schrader, J.; Arnold, R.; Fendrich, V.; Bartsch, D.K.; Horsch, D. Rap1/b-raf signaling is activated in neuroendocrine tumors of the digestive tract and raf kinase inhibition constitutes a putative therapeutic target. Neuroendocrinology 2007, 85, 45–53.
47. Ramos, J.W. The regulation of extracellular signal-regulated kinase (erk) in mammalian cells. Int. J. Biochem. Cell Biol. 2008, 40, 2707–2719.
48. Zwang, Y.; Sas-Chen, A.; Drier, Y.; Shay, T.; Avraham, R.; Lauriola, M.; Shema, E.; Lidor-Nili, E.; Jacob-Hirsch, J.; Amariglio, N.; et al. Two phases of mitogenic signaling unveil roles for p53 and egr1 in elimination of inconsistent growth signals. Mol. Cell 2011, 42, 524–535.
49. Welin, S.; Fjallskog, M.L.; Saras, J.; Eriksson, B.; Janson, E.T. Expression of tyrosine kinase receptors in malignant midgut carcinoid tumors. Neuroendocrinology 2006, 84, 42–48.
50. Rickman, O.B.; Vohra, P.K.; Sanyal, B.; Vrana, J.A.; Aubry, M.C.; Wigle, D.A.; Thomas, C.F., Jr. Analysis of erbb receptors in pulmonary carcinoid tumors. Clin. Cancer Res. 2009, 15, 3315–3324.
51. Shim, J.H.; Su, Z.Y.; Chae, J.I.; Kim, D.J.; Zhu, F.; Ma, W.Y.; Bode, A.M.; Yang, C.S.; Dong, Z. Epigallocatechin gallate suppresses lung cancer cell growth through ras-gtpase-activating protein sh3 domain-binding protein 1. Cancer Prev. Res. 2010, 3, 670–679.
52. Zekri, L.; Chebli, K.; Tourriere, H.; Nielsen, F.C.; Hansen, T.V.; Rami, A.; Tazi, J. Control of fetal growth and neonatal survival by the rasgap-associated endoribonuclease g3bp. Mol. Cell. Biol. 2005, 25, 8703–8716.
53. Taniuchi, K.; Nishimori, I.; Hollingsworth, M.A. The N-terminal domain of g3bp enhances cell motility and invasion by posttranscriptional regulation of bart. Mol. Cancer Res. 2011, 9, 856–866.
54. French, J.; Stirling, R.; Walsh, M.; Kennedy, H.D. The expression of ras-gtpase activating protein sh3 domain-binding proteins, g3bps, in human breast cancers. Histochem. J. 2002, 34, 223–231.
55. Wan, P.T.; Garnett, M.J.; Roe, S.M.; Lee, S.; Niculescu-Duvaz, D.; Good, V.M.; Jones, C.M.; Marshall, C.J.; Springer, C.J.; Barford, D.; et al. Mechanism of activation of the raf-erk signaling pathway by oncogenic mutations of b-raf. Cell 2004, 116, 855–867.
56. Tannapfel, A.; Vomschloss, S.; Karhoff, D.; Markwarth, A.; Hengge, U.R.; Wittekind, C.; Arnold, R.; Horsch, D. Braf gene mutations are rare events in gastroenteropancreatic neuroendocrine tumors. Am. J. Clin. Pathol. 2005, 123, 256–260.
57. Roush, S.; Slack, F.J. The let-7 family of micrornas. Trends Cell Biol. 2008, 18, 505–516. 59
58. Nimmo, R.A.; Slack, F.J. An elegant mirror: MicroRNAs in stem cells, developmental timing and cancer. Chromosoma 2009, 118, 405–418.
59. Rahman, M.M.; Qian, Z.R.; Wang, E.L.; Sultana, R.; Kudo, E.; Nakasono, M.; Hayashi, T.; Kakiuchi, S.; Sano, T. Frequent overexpression of hmga1 and 2 in gastroenteropancreatic neuroendocrine tumours and its relationship to let-7 downregulation. Br. J. Cancer 2009, 100, 501–510.
60. Schultz, J.; Lorenz, P.; Gross, G.; Ibrahim, S.; Kunz, M. MicroRNA let-7b targets important cell cycle molecules in malignant melanoma cells and interferes with anchorage-independent growth. Cell Res. 2008, 18, 549–557.
61. Liang, S.; He, L.; Zhao, X.; Miao, Y.; Gu, Y.; Guo, C.; Xue, Z.; Dou, W.; Hu, F.; Wu, K.; et al. MicroRNA let-7f inhibits tumor invasion and metastasis by targeting myh9 in human gastric cancer. PLOS ONE 2011, 6, e18409.
62. King, C.E.; Cuatrecasas, M.; Castells, A.; Sepulveda, A.R.; Lee, J.S.; Rustgi, A.K. Lin28b promotes colon cancer progression and metastasis. Cancer Res. 2011, 71, 4260–4268.
63. Heinzelmann, J.; Henning, B.; Sanjmyatav, J.; Posorski, N.; Steiner, T.; Wunderlich, H.; Gajda, M.R.; Junker, K. Specific miRNA signatures are associated with metastasis and poor prognosis in clear cell renal cell carcinoma. World J. Urol. 2011, 29, 367–373.
64. Qian, Z.R.; Asa, S.L.; Siomi, H.; Siomi, M.C.; Yoshimoto, K.; Yamada, S.; Wang, E.L.; Rahman, M.M.; Inoue, H.; Itakura, M.; et al. Overexpression of hmga2 relates to reduction of the let-7 and its relationship to clinicopathological features in pituitary adenomas. Modern Pathol. 2009, 22, 431–441.