RNPC1, an RNA-binding protein and a p53 target, regulates macrophage inhibitory cytokine-1 (MIC-1) expression through mRNA stability

Journal of Biological Chemistry

Volumn 288, Issue 33, 2013, Pages 23680-23686

  Yin, Tiffany ^a   Cho, Seong Jun ^a   Chen, Xinbin ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GROWTH SUPPRESSIONS; MRNA STABILITY; POST-TRANSCRIPTIONAL MECHANISMS; RNA-BINDING PROTEIN;

CELL GROWTH; GROWTH KINETICS;

NUCLEIC ACIDS;

GROWTH DIFFERENTIATION FACTOR 15; MESSENGER RNA; REGULATOR PROTEIN; RNPC1 PROTEIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ANIMAL CELL; ARTICLE; AU RICH ELEMENT; CELL GROWTH; CONTROLLED STUDY; EMBRYO; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENE INDUCTION; GENE OVEREXPRESSION; GENE SILENCING; GENETIC STABILITY; GROWTH INHIBITION; MIC 1 GENE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; TRANSCRIPTION REGULATION;

CELL PROLIFERATION; GDF-15; GENE REGULATION; MIC-1; MRNA DECAY; P21; P53; RNA-BINDING PROTEIN; RNPC1;

3' UNTRANSLATED REGIONS; ANIMALS; AU RICH ELEMENTS; BASE SEQUENCE; CELL LINE; CELL PROLIFERATION; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; GROWTH DIFFERENTIATION FACTOR 15; HUMANS; MICE; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; RNA STABILITY; RNA, MESSENGER; RNA-BINDING PROTEINS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84882445849     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.480186     Document Type: Article

References (34)

1. Bootcov, M. R., Bauskin, A. R., Valenzuela, S. M., Moore, A. G., Bansal, M., He, X. Y., Zhang, H. P., Donnellan, M., Mahler, S., Pryor, K., Walsh, B. J., Nicholson, R. C., Fairlie, W. D., Por, S. B., Robbins, J. M., and Breit, S. N. (1997) MIC-1, a novel macrophage inhibitory cytokine, is a divergent member of the TGF-superfamily. Proc. Natl. Acad. Sci. U.S.A. 94, 11514-11519
2. Lawton, L. N., Bonaldo, M. F., Jelenc, P. C., Qiu, L., Baumes, S. A., Marcelino, R. A., de Jesus, G. M., Wellington, S., Knowles, J. A., Warburton, D., Brown, S., and Soares, M. B. (1997) Identification of a novel member of the TGF-superfamily highly expressed in human placenta. Gene 203, 17-26
3. Tan, M., Wang, Y., Guan, K., and Sun, Y. (2000) PTGF, a type transforming growth factor (TGF-) superfamily member, is a p53 target gene that inhibits tumor cell growth via TGF-signaling pathway. Proc. Natl. Acad. Sci. U.S.A. 97, 109-114
4. Fairlie, W. D., Moore, A. G., Bauskin, A. R., Russell, P. K., Zhang, H. P., and Breit, S. N. (1999) MIC-1 is a novel TGF-superfamily cytokine associated with macrophage activation. J. Leukoc. Biol. 65, 2-5
5. Böttner, M., Suter-Crazzolara, C., Schober, A., and Unsicker, K. (1999) Expression of a novel member of the TGF-superfamily, growth/ differentiation factor-15/macrophage-inhibiting cytokine-1 (GDF-15/MIC-1) in adult rat tissues. Cell Tissue Res. 297, 103-110
6. Schober, A., Böttner, M., Strelau, J., Kinscherf, R., Bonaterra, G. A., Barth, M., Schilling, L., Fairlie, W. D., Breit, S. N., and Unsicker, K. (2001) Expression of growth differentiation factor-15/macrophage inhibitory cytokine-1 (GDF-15/MIC-1) in the perinatal, adult, and injured rat brain. J. Comp. Neurol. 439, 32-45
7. Welsh, J. B., Sapinoso, L. M., Kern, S. G., Brown, D. A., Liu, T., Bauskin, A. R., Ward, R. L., Hawkins, N. J., Quinn, D. I., Russell, P. J., Sutherland, R. L., Breit, S. N., Moskaluk, C. A., Frierson, H. F., Jr., and Hampton, G. M. (2003) Large-scale delineation of secreted protein biomarkers overexpressed in cancer tissue and serum. Proc. Natl. Acad. Sci. U.S.A. 100, 3410-3415
8. Kempf, T., Eden, M., Strelau, J., Naguib, M., Willenbockel, C., Tongers, J., Heineke, J., Kotlarz, D., Xu, J., Molkentin, J. D., Niessen, H. W., Drexler, H., and Wollert, K. C. (2006) The transforming growth factor-superfamily member growth-differentiation factor-15 protects the heart from ischemia/ reperfusion injury. Circ. Res. 98, 351-360
9. Wiklund, F. E., Bennet, A. M., Magnusson, P. K., Eriksson, U. K., Lindmark, F., Wu, L., Yaghoutyfam, N., Marquis, C. P., Stattin, P., Pedersen, N. L., Adami, H. O., Grönberg, H., Breit, S. N., and Brown, D. A. (2010) Macrophage inhibitory cytokine-1 (MIC-1/GDF15): a new marker of allcause mortality. Aging Cell 9, 1057-1064
10. Brown, D. A., Ward, R. L., Buckhaults, P., Liu, T., Romans, K. E., Hawkins, N. J., Bauskin, A. R., Kinzler, K. W., Vogelstein, B., and Breit, S. N. (2003) MIC-1 serum level and genotype: associations with progress and prognosis of colorectal carcinoma. Clin. Cancer Res. 9, 2642-2650
11. Brown, D. A., Lindmark, F., Stattin, P., Bälter, K., Adami, H. O., Zheng, S. L., Xu, J., Isaacs, W. B., Grönberg, H., Breit, S. N., and Wiklund, F. E. (2009) Macrophage inhibitory cytokine 1: a new prognostic marker in prostate cancer. Clin. Cancer Res. 15, 6658-6664
12. Cheng, J. C., Chang, H. M., and Leung, P. C. (2011) Wild-type p53 attenuates cancer cell motility by inducing growth differentiation factor-15 expression. Endocrinology 152, 2987-2995
13. Li, P. X., Wong, J., Ayed, A., Ngo, D., Brade, A. M., Arrowsmith, C., Austin, R. C., and Klamut, H. J. (2000) Placental transforming growth factor-is a downstream mediator of the growth arrest and apoptotic response of tumor cells to DNA damage and p53 overexpression. J. Biol. Chem. 275, 20127-20135
14. Bauskin, A. R., Brown, D. A., Kuffner, T., Johnen, H., Luo, X. W., Hunter, M., and Breit, S. N. (2006) Role of macrophage inhibitory cytokine-1 in tumorigenesis and diagnosis of cancer. Cancer Res. 66, 4983-4986
15. Bauskin, A. R., Brown, D. A., Junankar, S., Rasiah, K. K., Eggleton, S., Hunter, M., Liu, T., Smith, D., Kuffner, T., Pankhurst, G. J., Johnen, H., Russell, P. J., Barret, W., Stricker, P. D., Grygiel, J. J., Kench, J. G., Henshall, S. M., Sutherland, R. L., and Breit, S. N. (2005) The propeptide mediates formation of stromal stores of PROMIC-1: role in determining prostate cancer outcome. Cancer Res. 65, 2330-2336
16. Husaini, Y., Qiu, M. R., Lockwood, G. P., Luo, X. W., Shang, P., Kuffner, T., Tsai, V. W., Jiang, L., Russell, P. J., Brown, D. A., and Breit, S. N. (2012) Macrophage inhibitory cytokine-1 (MIC-1/GDF15) slows cancer development but increases metastases in TRAMP prostate cancer prone mice. PLoS One 7, e43833
17. Kadowaki, M., Yoshioka, H., Kamitani, H., Watanabe, T., Wade, P. A., and Eling, T. E. (2012) DNA methylation-mediated silencing of nonsteroidal anti-inflammatory drug-activated gene (NAG-1/GDF15) in glioma cell lines. Int. J. Cancer 130, 267-277
18. Yoshioka, H., Kamitani, H., Watanabe, T., and Eling, T. E. (2008) Nonsteroidal anti-inflammatory drug-activated gene (NAG-1/GDF15) expression is increased by the histone deacetylase inhibitor trichostatin A. J. Biol. Chem. 283, 33129-33137
19. Harms, K., Nozell, S., and Chen, X. (2004) The common and distinct target genes of the p53 family transcription factors. Cell Mol. Life Sci. 61, 822-842
20. Riley, T., Sontag, E., Chen, P., and Levine, A. (2008) Transcriptional control of human p53-regulated genes. Nat. Rev. Mol. Cell Biol. 9, 402-412
21. Vogelstein, B., Lane, D., and Levine, A. J. (2000) Surfing the p53 network. Nature 408, 307-310
22. Yang, H., Filipovic, Z., Brown, D., Breit, S. N., and Vassilev, L. T. (2003) Macrophage inhibitory cytokine-1: a novel biomarker for p53 pathway activation. Mol. Cancer Ther. 2, 1023-1029
23. Kim, I. Y., Park, S. Y., Kang, Y., Thapa, D., Choi, H. G., and Kim, J. A. (2011) Role of nonsteroidal anti-inflammatory drug-activated gene-1 in docetaxel-induced cell death of human colorectal cancer cells with different p53 status. Arch. Pharm. Res. 34, 323-330
24. Qian, Y., Jung, Y. S., and Chen, X. (2012) Differentiated embryo-chondrocyte expressed gene 1 regulates p53-dependent cell survival versus cell death through macrophage inhibitory cytokine-1. Proc. Natl. Acad. Sci. U.S.A. 109, 11300-11305
25. Shu, L., Yan, W., and Chen, X. (2006) RNPC1, an RNA-binding protein and a target of the p53 family, is required for maintaining the stability of the basal and stress-induced p21 transcript. Genes Dev. 20, 2961-2972
26. Zhang, J., Jun Cho, S., and Chen, X. (2010) RNPC1, an RNA-binding protein and a target of the p53 family, regulates p63 expression through mRNA stability. Proc. Natl. Acad. Sci. U.S.A. 107, 9614-9619
27. Yan, W., Zhang, J., Zhang, Y., Jung, Y. S., and Chen, X. (2012) p73 expression is regulated by RNPC1, a target of the p53 family, via mRNA stability. Mol. Cell. Biol. 32, 2336-2348
28. Zhang, J., Cho, S. J., Shu, L., Yan, W., Guerrero, T., Kent, M., Skorupski, K., Chen, H., and Chen, X. (2011) Translational repression of p53 by RNPC1, a p53 target overexpressed in lymphomas. Genes Dev. 25, 1528-1543
29. Cho, S. J., Zhang, J., and Chen, X. (2010) RNPC1 modulates the RNAbinding activity of, and cooperates with, HuR to regulate p21 mRNA stability. Nucleic Acids Res. 38, 2256-2267
30. Soto-Cerrato, V., Viñals, F., Lambert, J. R., and Pérez-Tomás, R. (2007) The anticancer agent prodigiosin induces p21WAF1/CIP1 expression via transforming growth factor-receptor pathway. Biochem. Pharmacol. 74, 1340-1349
31. Kim, J. S., Baek, S. J., Sali, T., and Eling, T. E. (2005) The conventional nonsteroidal anti-inflammatory drug sulindac sulfide arrests ovarian cancer cell growth via the expression of NAG-1/MIC-1/GDF-15. Mol. Cancer Ther. 4, 487-493
32. Lee, S. H., Krisanapun, C., and Baek, S. J. (2010) NSAID-activated gene-1 as a molecular target for capsaicin-induced apoptosis through a novel molecular mechanism involving GSK3, C/EBP-and ATF3. Carcinogenesis 31, 719-728
33. Brown, D. A., Hance, K. W., Rogers, C. J., Sansbury, L. B., Albert, P. S., Murphy, G., Laiyemo, A. O., Wang, Z., Cross, A. J., Schatzkin, A., Danta, M., Srasuebkul, P., Amin, J., Law, M., Breit, S. N., and Lanza, E. (2012) Serum macrophage inhibitory cytokine-1 (MIC-1/GDF15): a potential screening tool for the prevention of colon cancer? Cancer Epidemiol. Biomarkers Prev. 21, 337-346
34. Vaňhara, P., Hampl, A., Kozubík, A., and Souček, K. (2012) Growth/differentiation factor-15: prostate cancer suppressor or promoter? Prostate Cancer Prostatic Dis. 15, 320-328