Androgens up-regulate transcription of the notch inhibitor numb in C2C12 myoblasts via wnt/β-catenin signaling to t cell factor elements in the numb promoter

Journal of Biological Chemistry

Volumn 288, Issue 25, 2013, Pages 17990-17998

  Liu, Xin Hua ^a,b   Wu, Yong ^a   Yao, Shen ^b   Levine, Alice C ^b   Kirschenbaum, Alexander ^b   Collier, Lauren ^a   Bauman, William A ^a,b   Cardozo, Christopher P ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

C2C12 MYOBLASTS; CATENIN SIGNALING; NANDROLONE; T-CELL FACTORS; TARGET GENES; UP-REGULATION;

TRANSCRIPTION;

CELL SIGNALING;

ANDROGEN; BETA CATENIN; DICKKOPF 1 PROTEIN; GLYCOGEN SYNTHASE KINASE 3BETA; MESSENGER RNA; NANDROLONE; NUMB PROTEIN; REGULATOR PROTEIN; SECRETED FRIZZLED RELATED PROTEIN 1; T CELL FACTOR PROTEIN; UNCLASSIFIED DRUG; WNT PROTEIN; WNT3A PROTEIN; WNT5A PROTEIN;

ANIMAL CELL; ARTICLE; BINDING SITE; CONTROLLED STUDY; GENE EXPRESSION; MOUSE; MYOBLAST; NONHUMAN; NUMB GENE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SITE DIRECTED MUTAGENESIS; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; UPREGULATION; WNT SIGNALING PATHWAY;

ANABOLIC STEROIDS; ANDROGEN; ANDROGEN RECEPTOR; MYOGENESIS; NOTCH; NUMB; WNT SIGNALING;

ANDROGENS; ANIMALS; BETA CATENIN; BINDING SITES; BLOTTING, WESTERN; CELL LINE; GENE EXPRESSION; GLYCOGEN SYNTHASE KINASE 3; MEMBRANE PROTEINS; MICE; MICROSCOPY, CONFOCAL; MUTATION; MYOBLASTS; NANDROLONE; NERVE TISSUE PROTEINS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TCF TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; UP-REGULATION; WNT PROTEINS; WNT3A PROTEIN;

EID: 84880057379     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.478487     Document Type: Article

References (47)

1. Cossu, G., and Borello, U. (1999) Wnt signaling and the activation of myogenesis in mammals. EMBO J. 18, 6867-6872 (Pubitemid 30000439)
2. Anakwe, K., Robson, L., Hadley, J., Buxton, P., Church, V., Allen, S., Hartmann, C., Harfe, B., Nohno, T., Brown, A. M., Evans, D. J., and Francis-West, P. (2003) Wnt signalling regulates myogenic differentiation in the developing avian wing. Development 130, 3503-3514 (Pubitemid 37010013)
3. Brack, A. S., Conboy, M. J., Roy, S., Lee, M., Kuo, C. J., Keller, C., and Rando, T. A. (2007) Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science 317, 807-810 (Pubitemid 47257918)
4. Brack, A. S., Conboy, I. M., Conboy, M. J., Shen, J., and Rando, T. A. (2008) A temporal switch from notch to Wnt signaling in muscle stem cells is necessary for normal adult myogenesis. Cell Stem Cell 2, 50-59
5. MacDonald, B. T., Tamai, K., and He, X. (2009) Wnt/β-catenin signaling: Components, mechanisms, and diseases. Dev. Cell 17, 9-26
6. Kockeritz, L., Doble, B., Patel, S., and Woodgett, J. R. (2006) Glycogen synthase kinase-3: An overview of an overachieving protein kinase. Curr. Drug Targets 7, 1377-1388 (Pubitemid 44718298)
7. Lange, C., Mix, E., Frahm, J., Glass, A., Müller, J., Schmitt, O., Schmöle, A. C., Klemm, K., Ortinau, S., Hübner, R., Frech, M. J., Wree, A., and Rolfs, A. (2011) Small molecule GSK3 inhibitors increase neurogenesis of human neural progenitor cells. Neurosci. Lett. 488, 36-40
8. Conboy, I. M., and Rando, T. A. (2002) The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Dev. Cell 3, 397-409
9. Luo, D., Renault, V. M., and Rando, T. A. (2005) The regulation of Notch signaling in muscle stem cell activation and postnatal myogenesis. Semin. Cell Dev. Biol. 16, 612-622 (Pubitemid 41247884)
10. Artavanis-Tsakonas, S., Matsuno, K., and Fortini, M. E. (1995) Notch signaling. Science 268, 225-232
11. Munoz-Descalzo, S., de Navascues, J., and Arias, A. M. (2011) Wnt-Notch signaling: An integrated mechanism regulating transitions between cell stages. Bioessays 34, 110-118
12. Yamamizu, K., Matsunaga, T., Uosaki, H., Fukushima, H., Katayama, S., Hiraoka-Kanie, M., Mitani, K., and Yamashita, J. K. (2010) Convergence of Notch and β-catenin signaling induces arterial fate in vascular progenitors. J. Cell Biol. 189, 325-338
13. Nakamura, T., Tsuchiya, K., and Watanabe, M. (2007) Cross-talk between Wnt and Notch signaling in intestinal epithelial cell fate decision. J. Gastroenterol. 42, 705-710 (Pubitemid 47456757)
14. Fre, S., Pallavi, S. K., Huyghe, M., Laé, M., Janssen, K. P., Robine, S., Artavanis-Tsakonas, S., and Louvard, D. (2009) Notch and Wnt signals cooperatively control cell proliferation and tumorigenesis in the intestine. Proc. Natl. Acad. Sci. U.S.A. 106, 6309-6314
15. Hayward, P., Kalmar, T., and Arias, A. M. (2008) Wnt/Notch signaling and information processing during development. Development 135, 411-424
16. Shimizu, T., Kagawa, T., Inoue, T., Nonaka, A., Takada, S., Abutatani, H., and Taga, T. (2008) Stabilizedβ-catenin functions through TCF/LEF proteins and the Notch/RBP-Jk complex to promote proliferation and suppress differentiation of neural precursor cells. Mol. Cell. Biol. 28, 7427-7441
17. Katoh, M., and Katoh, M. (2006) Numb is a break of Wnt-Notch signaling cycle. Int. J. Mol. Med. 18, 517-521
18. Cheng, X., Huber, T. L., Chen, V. C., Gadue, P., and Keller, G. M. (2008) Numb mediates the interaction between Wnt and Notch to modulate primitive erythropoietic specification from the hemangioblast. Development 135, 3447-3458
19. Gulino, A., Di Marcotullio, L., and Screpanti, I. (2010) The multiple functions of Numb. Exp. Cell Res. 316, 900-906
20. Jory, A., Le Roux, I., Gayraud-Morel, B., Rocheteau, P., Cohen-Tannoudji, M., Cumano, A., and Tajbakhsh, S. (2009)Numbpromotes and increase in skeletal muscle progenitor cells in the embryonic somite. Stem Cells 27, 2769-2780
21. Zilian, O., Saner, C., Hagedorn, L., Lee, H. Y., Säuberli, E., Suter, U., Sommer, L., and Aguet, M. (2001) Multiple roles of mouse Numb in tuning developmental cell fates. Curr. Biol. 11, 494-501 (Pubitemid 32305028)
22. Singh, R., Artaza, J. N., Taylor, W. E., Gonzalez-Cadavid, N. F., and Bhasin S. (2003) Androgens stimulate myogenic differentiation and inhibit adipogenesis in C3H 10T1/2 pluripotent cells through an androgen receptormediated pathway. Endocrinology 144, 5081-5088 (Pubitemid 37378423)
23. Kicman, A. T. (2008) Pharmacology of anabolic steroids. Br. J. Pharmacol. 154, 502-521 (Pubitemid 351744954)
24. Wimalawansa, S. M., Chapa, M. T., Wei, J. N., Westlund, K. N., Quast, M. J., and Wimalawansa, S. J. (1999) Reversal of weightlessness-induced musculoskeletal losses with androgens: Quantification by MRI. J. Appl. Physiol. 86, 1841-1846 (Pubitemid 29275557)
25. Taylor, D. C., Brooks, D. E., and Ryan, J. B. (1999) Anabolic-androgenic steroid administration causes hypertrophy of immobilized and nonimmobilized skeletal muscle in a sedentary rabbit model. Am. J. Sports Med. 27, 718-727
26. Gregory, C. M., Vandenborne, K., Huang, H. F., Ottenweller, J. E., and Dudley, G. A. (2003) Effects of testosterone replacement therapy on skeletal muscle after spinal cord injury. Spinal Cord 41, 23-28 (Pubitemid 36132539)
27. Sinha-Hikim, I., Cornford, M., Gaytan, H., Lee, M. L., and Bhasin, S. (2006) Effects of testosterone supplementation on skeletal muscle fiber hypertrophy and satellite cells in community-dwelling older men. J. Clin. Endocrinol. Metab. 91, 3024-3033 (Pubitemid 44271751)
28. Yang, F., Li, X., Sharma, M., Sasaki, C. Y., Longo, D. L., Lim, B., and Sun, Z. (2002) Linking β-catenin to androgen-signaling pathway. J. Biol. Chem. 277, 11336-11344
29. Pawlowski, J. E., Ertel, J. R., Allen, M. P., Xu, M., Butler, C., Wilson, E. M., and Wierman, M. E. (2002) Liganded androgen receptor interaction with β-catenin nuclear co-localization and modulation of transcriptional activity in neuronal cells. J. Biol. Chem. 277, 20702-20710 (Pubitemid 34967374)
30. Singh, R., Bhasin, S., Braga, M., Artaza, J. N., Pervin, S., Taylor, W. E., Krishnan, V., Sinha, S. K., Rajavashisth, T. B., and Jasuja, R. (2009) Regulation of myogenic differentiation by androgens: Cross-talk between androgen receptor/β-catenin and follistatin/transforming growth factor-β signaling pathways. Endocrinology 150, 1259-1268
31. Liu, X. H., Kirschenbaum, A., Yao, S., Liu, G., Aaronson, S. A., and Levine, A. C. (2007) Androgen-induced Wnt signaling in preosteoblasts promotes the growth of MDA-PCa-2b human prostate cancer cells. Cancer Res. 67, 5747-5753 (Pubitemid 46985007)
32. Truica, C. I., Byers, S., and Gelmann, E. P. (2000) β-Catenin affects androgen receptor transcriptional activity and ligand specificity. Cancer Res. 60, 4709-4713
33. Liu, X. H., Yao, S., Qiao, R. F., Levine, A. C., Kirschenbaum, A., Pan, J., Wu, Y., Qin, W., Bauman, W. A., and Cardozo, C. P. (2011) Nandrolone reduces activation of Notch signaling in denervated muscle associated with increased Numb expression. Biophys. Biochem. Res. Commun. 414, 165-169
34. Liu, X. H., Yao, S., Levine, A. C., Kirschenbaum, A., Pan, J., Wu, Y., Qin, W., Collier, L., Bauman, W. A., and Cardozo, C. P. (2012) Nandrolone, an anabolic steroid, stabilizes Numb protein through inhibition of Mdm2 in C2C12 myoblasts. J. Androl. 33, 1216-1223
35. Zhao, W., Pan, J., Wang, X., Wu, Y., Bauman, W. A., and Cardozo, C. P. (2008) Expression of the muscle atrophy factor muscle atrophy F-box is suppressed by testosterone. Endocrinology 149, 5449-5460
36. Livak, K. J., and Schmittgen, T. D. (2001) Analysis of relative gene expression data using real time quantitative PCR and the 2(-δδ CT) method. Methods 25, 402-408 (Pubitemid 34164012)
37. Korinek, V., Barker, N., Morin, P. J., van Wichen, D., de Weger, R., Kinzler, K. W., Vogelstein, B., and Clevers, H. (1997) Constitutive transcriptional activation by a β-catenin-Tcf complex in APC-/-colon carcinoma. Science 275, 1784-1787 (Pubitemid 27136714)
38. van Noort, M., van de Wetering, M., and Clevers, H. (2002) Identification of two novel regulated serines in the N terminus of β-catenin. Exp. Cell Res. 276, 264-272 (Pubitemid 34969320)
39. Logan, C. Y., and Nusse, R. (2004) The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20, 781-810 (Pubitemid 39488658)
40. Liu, X. H., Kirschenbaum, A., Yao, S., and Levine, A. C. (2007) Androgens promote preosteoblast differentiation via activation of the canonical Wnt signaling pathway. Ann. N.Y. Acad. Sci. 1116, 423-431 (Pubitemid 350274319)
41. Singh, R., Artaza, J. N., Taylor, W. E., Braga, M., Yuan, X., Gonzalez-Cadavid, N. F., and Bhasin, S. (2006) Testosterone inhibits adipogenic differentiation in 3T3-L1 cells: Nuclear translocation of androgen receptor complex with β-catenin and T-cell factor 4 may bypass canonical Wnt signaling to down-regulate adipogenic transcription factors. Endocrinology 147, 141-154 (Pubitemid 43004269)
42. Song, L. N., Herrell, R., Byers, S., Shah, S., Wilson, E. M., and Gelmann, E. P. (2003) β-Catenin binds to the activation function 2 region of the androgen receptor and modulates the effects of the N-terminal domain and TIF2 on ligand-dependent transcription. Mol. Cell. Biol. 23, 1674-1687 (Pubitemid 36246049)
43. Kwon, C., Cheng, P., King, I. N., Andersen, P., Shenje, L., Nigam, V., and Srivastava, D. (2011) Notch post-translationally regulates β-catenin protein in stem and progenitor cells. Nat. Cell Biol. 13 1244-1251
44. Shahi, P., Seethammagari, M. R., Valdez, J. M., Xin, L., and Spencer, D. M. (2011) Wnt and Notch pathways have interrelated opposing roles on prostate progenitor cell proliferation and differentiation. Stem Cells 29, 678-688
45. Boulter, L., Govaere, O., Bird, T. G., Radulescu, S., Ramachandran, P., Pellicoro, A., Ridgway, R. A., Seo, S. S., Spee, B., Van Rooijen, N., Sansom, O. J., Iredale, J. P., Lowell, S., Roskams, T., and Forbes, S. J. (2012) Macrophage-derived Wnt opposes Notch signaling to specify hepatic progenitor cell fate in chronic liver disease. Nat. Med. 18, 572-579
46. Di Marcotullio, L., Ferretti, E., Greco, A., De Smaele, E., Po, A., Sico, M. A., Alimandi, M., Giannini, G., Maroder, M., Screpanti, I., and Gulino, A. (2006) Numb is a suppressor of Hedgehog signaling and targets Gli1 for Itch-dependent ubiquitination. Nat. Cell Biol. 8, 1415-1423 (Pubitemid 44835117)
47. Carter, S., and Vousden, K. H. (2008) A role of Numb in p53 stabilization. Genome Biol. 9, 2211-2213