Posttranscriptional suppression of proto-oncogene c-fms expression by vigilin in breast cancer

Molecular and Cellular Biology

Volumn 31, Issue 1, 2011, Pages 215-225

  Woo, Ho Hyung ^a   Yi, Xiaofang ^a   Lamb, Tiffany ^a   Menzl, Ina ^a   Baker, Terri ^a   Shapiro, David J ^b   Chambers, Setsuko K ^a  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HUR PROTEIN; MESSENGER RNA; RNA BINDING PROTEIN; RNA BINDING PROTEIN VIGILIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ARTICLE; BREAST CANCER; C FMS PROTO ONCOGENE; CELL INVASION; CELL MOTILITY; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; HALF LIFE TIME; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTO ONCOGENE; RNA BINDING; RNA SEQUENCE; TRANSCRIPTION REGULATION; TRANSLATION REGULATION;

3' UNTRANSLATED REGIONS; ANTIGENS, SURFACE; BASE SEQUENCE; BINDING, COMPETITIVE; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; DISEASE PROGRESSION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, FMS; GENES, REPORTER; HUMANS; MOLECULAR SEQUENCE DATA; NEOPLASM INVASIVENESS; PROTEIN BIOSYNTHESIS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA STABILITY; RNA, MESSENGER; RNA, NEOPLASM; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS;

EID: 78751695662     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01031-10     Document Type: Article

References (46)

1. Amrani, N., S. Ghosh, D. A. Mangus, and A. Jacobson. 2008. Translation factors promote the formation of two states of the closed-loop mRNP. Nature 453:1276-1280. (Pubitemid 351913593)
2. Balagopal, V., and R. Parker. 2009. Polysomes, P bodies and stress granules: states and fates of eukaryotic mRNAs. Curr. Opin. Cell Biol. 21:403-408.
3. Bor, Y. C., J. Swartz, Y. Li, J. Coyle, D. Rekosh, and M. L. Hammarskjold. 2006. Northern blot analysis of mRNA from mammalian polyribosomes. Nat. Protoc. doi:10.1038/nprot.216.
4. Brock, M. L., and D. J. Shapiro. 1983. Estrogen stabilizes vitellogenin mRNA against cytoplasmic degradation. Cell 34:207-214.
5. Chambers, S. K. 2009. Role of CSF-1 in progression of epithelial ovarian cancer. Future Oncol. 5:1429-1440.
6. Chambers, S. K., C. M. Ivins, B. M. Kacinski, and R. B. Hochberg. 2004. An unexpected effect of glucocorticoids on stimulation of c-fms proto-oncogene expression in choriocarcinoma cells that express little glucocorticoid receptor. Am. J. Obstet. Gynecol. 190:974-985.
7. Chambers, S. K., Y. Wang, M. Gilmore-Hebert, and B. M. Kacinski. 1994. Post-transcriptional regulation of c-fms proto-oncogene expression by dexamethasone and of CSF-1 in human breast carcinomas in vitro. Steroids 59:514-522.
8. Chambers, S. K., B. M. Kacinski, C. M. Ivins, and M. L. Carcangiu. 1997. Overexpression of epithelial macrophage colony-stimulating factor (CSF-1) and CSF-1 receptor: a poor prognostic factor in epithelial ovarian cancer, contrasted with a protective effect of stromal CSF-1. Clin. Cancer Res. 3:999-1007.
9. Chen, C. Y., R. Gherzi, S.-E. Ong, E. L. Chan, R. Raijmakers, G. J. M. Pruijn, G. Stoecklin, C. Moroni, M. Mann, and M. Karin. 2001. AU binding proteins recruit the exosome to degrade ARE-containing mRNAs. Cell 107:451-464.
10. Colegrove-Otero, L. J., N. Minshall, and N. Standart. 2005. RNA-binding proteins in early development. Cri. Rev. Biochem. Mol. Biol. 40:21-73.
11. Cunningham, K. S., R. E. Dodson, M. A. Nagel, D. J. Shapiro, and D. R. Schoenberg. 2000. Vigilin binding selectively inhibits cleavage of the vitellogenin mRNA 3′-untranslated region by the mRNA endonucleases polysomal ribonuclease 1. Proc. Natl. Acad. Sci. U. S. A. 97:12498-12502.
12. Dai, X.-M., G. R. Ryan, A. J. Hapel, M. G. Dominguez, R. G. Russell, S. Kapp, V. Sylvestre, and E. R. Stanley. 2009. Targeted disruption of the mouse colony-stimulating factor 1 receptor gene results in osteopetrosis, mononuclear phagocyte deficiency, increased primitive progenitor cell frequencies, and reproductive defects. Blood 99:111-120.
13. Dodson, R. E., and D. J. Shapiro. 1997. Vigilin, a ubiquitous protein with 14 K homology domains, is the estrogen-inducible vitellogenin mRNA 3′-untranslated region-binding protein. J. Biol. Chem. 272:12249-12252.
14. Fan, X. C., and J. Steitz. 1998. Overexpression of HuR, a nuclear-cytoplasmic shuttling protein, increases the in vivo stability of ARE-containing mRNAs. EMBO J. 17:3448-3460.
15. Feng, Y., D. Absher, D. E. Eberhart, V. Brown, H. E. Malter, and S. T. Warren. 1997. FMRP associates with polyribosomes as an mRNA, and the 1304N mutation of severe fragile abolishes this association. Mol. Cell 1:109-118.
16. Fidge, N. H. 1999. High density lipoprotein receptors, binding proteins, and ligands. J. Lipid Res. 40:187-201.
17. Garneau, N. L., J. Wilusz, and C. J. Wilusz. 2007. The highways and byways of mRNA decay. Nat. Rev. Mol. Cell Biol. 8:113-126.
18. Gherzi, R., K. Y. Lee, P. Briata, D. Wegmüller, C. Moroni, M. Karin, and C. Y. Chen. 2004. A KH domain RNA binding protein, KSRP, promotes ARE-directed mRNA turnover by recruiting the degradation machinery. Mol. Cell 14:571-583.
19. Grosset, C., C. Y. Chen, N. Xu, N. Sonenberg, H. Jacquemin-Sablon, and A. B. Shyu. 2000. A mechanism for translationally coupled mRNA turnover: interaction between the poly(A) tail and a c-fos RNA coding determinant via a protein complex. Cell 103:29-40.
20. Hanoune, J., and M. K. Agarwal. 1970. Studies on the half life time of rat transfer RNA species. FEBS Lett. 11:78-80.
21. Hau, H. H., R. J. Walsh, R. L. Ogilvie, D. A. Williams, C. S. Reilly, and P. R. Bohjanen. 2007. Tristetraproline recuits functional mRNA decay complexes to ARE sequences. J. Cell. Biochem. 100:1477-1492.
22. Kacinski, B. M., K. A. Scata, D. Carter, L. D. Yee, E. Sapi, B. L. King, S. K. Chambers, M. A. Jones, M. H. Pirro, and E. R. Stanley. 1991. FMS (CSF-1 receptor) and CSF-1 transcripts and protein are expressed by human breast carcinomas in vivo and in vitro. Oncogene 6:941-952.
23. Kaminski, A., D. H. Ostareck, N. M. Standart, and R. J. Jackson. 1998. Affinity methods for isolating RNA binding proteins, p. 137-160. In C. W. J. Smith (ed.), RNA:protein interactions: a practical approach. Oxford University Press, Oxford, United Kingdom.
24. Kanamori, H., R. E. Dodson, and D. J. Shapiro. 1998. In vitro genetic analysis of the RNA binding site of vigilin, a multi-KH-domain protein. Mol. Cell. Biol. 18:3991-4003.
25. Kawai, T., A. Lal, X. Yang, S. Galban, K. Mazan-Mamczarz, and M. Gorospe. 2006. Translational control of cytochrome c by RNA binding proteins TIA-1 and HuR. Mol. Cell. Biol. 26:3295-3307.
26. Kluger, H. M., M. D. Dolled-Filhart, S. Rodov, B. M. Kacinski, R. L. Camp, and D. L. Rimm. 2004. Macrophage colony-stimulating factor-1 receptor expression is associated with poor outcome in breast cancer by large cohort tissue microarray analysis. Clin. Cancer Res. 10:173-177.
27. Kruse, C., D. Willkomm, J. Gebken, A. Schuh, H. Stossberg, T. Vollbrandt, and P. K. Müller. 2003. The multi-KH protein vigilin associates with free and membrane-bound ribosomes. Cell Mol. Life Sci. 60:2219-2227.
28. Lal, A., K. Mazan-Mamczarz, T. Kawai, X. Yang, J. L. Martindale, and M. Gorospe. 2004. Concurrent versus individual binding of HuR and AUF1 to common labile target mRNAs. EMBO J. 23:3092-3102.
29. Lang, B. D., and J. L. Fridovich-Keil. 2000. Scp160p, a multiple KH-domain protein, is a component of mRNP complexes in yeast. Nucleic Acids Res. 28:1576-1584.
30. Li, W., N. Thakor, E. Y. Xu, Y. Huang, C. Chen, R. Yu, M. Holcik, and A. N. Kong. 2010. An internal ribosomal entry site mediates redox-sensitive translation of Nrf2. Nucleic Acids Res. 38:778-788.
31. Liao, B., Y. Hu, and G. Brewer. 2007. Competitive binding of AUF1 and TIAR to MYC mRNA controls its translation. Nat. Struct. Mol. Biol. 14:511-518.
32. Lin, E. Y., A. V. Nguyen, R. G. Russell, and J. W. Pollard. 2001. Colony-stimulating factor 1 promotes progression of mammary tumors to malignancy. J. Exp. Med. 193:727-740.
33. Lopez de Silanes, I., M. Zhan, A. Lal, X. Yang, and M. Gorospe. 2004. Identification of a target RNA motif for RNA-binding protein HuR. Proc. Natl. Acad. Sci. U. S. A. 101:2987-2992.
34. Mazumder, B., V. Seshardri, and P. L. Fox. 2003. Translational control by the 3′-UTR: the ends specify the means. Trends Biochem. Sci. 28:91-98.
35. McKnight, G. L., J. Redasoner, K. O. Sundquist, B. Hokland, P. A. McKernan, J. Champagne, C. J. Johnson, M. C. Bailey, R. Holly, P. J. O'Hara, and J. F. Oram. 1992. Cloning and expression of a cellular high density lipoprotein-binding protein that is up-regulated by cholesterol loading of cells. J. Biol. Chem. 267:12131-12141.
36. Morris, A. K., N. Mukherjee, and J. D. Keene. 2010. Systematic analysis of posttranscriptional gene expression. Wiley Interdiscip. Rev. Syst. Biol. Med. 2:162-180.
37. Pullman, H. H. Kim, K. Abdelmohsen, A. Lai, J. L. Martindale, X. Yang, and M. Gorospe. 2007. Analysis of turnover and translation regulatory RNA-binding protein expression through binding to cognate mRNAs. Mol. Cell. Biol. 27:6265-6278.
38. Sapi, E., M. B. Flick, M. Gilmore-Hebert, S. Rodov, and B. M. Kacinski. 1995. Transcriptional regulation of the c-fms (CSF-1R) proto-oncogene in human breast carcinoma cells by glucocorticoids. Oncogene 10:529-542.
39. Sarkar, B., Q. Xi, C. He, and R. J. Schneider. 2003. Selective degradation of AU-rich mRNAs promoted by the p37 AUF1 protein isoform. Mol. Cell. Biol. 23:6685-6693.
40. Sharova, L. V., A. A. Sharov, T. Nedorezov, Y. Piao, N. Shaik, and M. S. Ko. 2009. Database for mRNA half-life of 19,977 genes obtained by DNA microarray analysis of pluripotent and differentiating mouse embryonic stem cells. DNA Res. 16:45-58.
41. Sherr, J. S., C. W. Rettenmier, R. Sacca, M. F. Roussel, A. T. Look, and E. R. Stanley. 1985. The c-fms proto-oncogene product is related to the receptor for the mononuclear phagocyte growth factor, CSF-1. Cell 41:665-676.
42. Shyu, A.-B., M. F. Wilkinson, and A. van Hoof. 2008. Messenger RNA regulation: to translation or to degrade. EMBO J. 27:471-481.
43. Toy, E. P., M. Azodi, N. L. Folk, C. M. Zito, C. J. Zeiss, and S. K. Chambers. 2009. Enhanced ovarian cancer tumorigenesis and metastasis by the macrophage colony-stimulating factor. Neoplasia 11:136-144.
44. Toy, E. P., N. Bonafé, A. Savlu, C. Zeiss, W. Zheng, M. Flick, and S. K. Chambers. 2005. Correlation of tumor phenotype with c-fms proto-oncogene expression in an in vivo intraperitoneal model for experimental human breast cancer metastasis. Clin. Exp. Metastasis 22:1-9.
45. Reference deleted.
46. Woo, H. H., Y. Zhou, X. Yi, C. L. David, W. Zheng, M. Gilmore-Hebert, H. M. Kluger, E. C. Ulukus, T. Baker, J. B. Stoffer, and S. K. Chambers. 2009. Regulation of non-AU-rich element containing c-fms proto-oncogene expression by HuR in breast cancer. Oncogene 28:1176-1186.