RNase L attenuates mitogen-stimulated gene expression via transcriptional and post-transcriptional mechanisms to limit the proliferative response

Journal of Biological Chemistry

Volumn 289, Issue 48, 2014, Pages 33629-33643

  Brennan Laun, Sarah E ^a,b   Li, Xiao Ling ^c   Ezelle, Heather J ^a,b,d   Venkataraman, Thiagarajan ^b   Blackshear, Perry J ^e   Wilson, Gerald M ^a,b   Hassel, Bret A ^a,b,d  

^a UNIVERSITY OF MARYLAND GREENEBAUM CANCER CENTER   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d BALTIMORE VA MEDICAL CENTER   (United States)

^e NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEINS; RNA;

ANTI-PROLIFERATIVE ACTIVITIES; FUNCTIONAL INTERACTION; INDUCED TRANSCRIPTION; POST-TRANSCRIPTIONAL MECHANISMS; PROLIFERATIVE RESPONSE; RNA-BINDING PROTEIN; SERUM-RESPONSE FACTORS; SUBSTRATE SPECIFICITY;

TRANSCRIPTION;

CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLOOXYGENASE 2; CYSTEINE RICH PROTEIN 61; GLUCOSE TRANSPORTER 1; HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 6; KRUPPEL LIKE FACTOR 6; MESSENGER RNA; MYOD PROTEIN; PROTEIN C FOS; PROTEIN KINASE PIM 1; RIBONUCLEASE L; RNA; SERUM RESPONSE FACTOR; TRANSCRIPTION FACTOR JUNB; TRISTETRAPROLIN; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN; 2-5A-DEPENDENT RIBONUCLEASE; MITOGENIC AGENT; RIBONUCLEASE; ZFP36 PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; CELL PROLIFERATION; CFOS GENE; CONTROLLED STUDY; COX 2 GENE; CYR61 GENE; DOWN REGULATION; ENZYME SPECIFICITY; EREG GENE; FEEDBACK SYSTEM; GENE; GENE CONTROL; GENE EXPRESSION; HIF1 ALPHA GENE; HPRT GENE; HUMAN; HUMAN CELL; IL 1BETA GENE; IL 6 GENE; JUNB GENE; KLF6 GENE; MITOGENESIS; MOUSE; MYOD GENE; NONHUMAN; P21CIP GENE; PGK1 GENE; PIM 1 GENE; POSTTRANSCRIPTIONAL GENE SILENCING; PROTEIN EXPRESSION; PROTEIN INTERACTION; RNA METABOLISM; SLC2A1 GENE; SRF GENE; TERA GENE; TNF ALPHA GENE; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; TTP GENE; VEGF GENE; ANIMAL; BIOLOGICAL MODEL; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; HEK293 CELL LINE; HELA CELL LINE; METABOLISM; PHYSIOLOGY; RNA STABILITY;

ANIMALS; CELL PROLIFERATION; ENDORIBONUCLEASES; GENE EXPRESSION REGULATION; HEK293 CELLS; HELA CELLS; HUMANS; MICE; MITOGENS; MODELS, BIOLOGICAL; RNA STABILITY; TRANSCRIPTION, GENETIC; TRISTETRAPROLIN;

EID: 84912139380     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.589556     Document Type: Article

References (117)

1. Lau, L. F., and Nathans, D. (1985) Identification of a set of genes expressed during the G0/G1 transition of cultured mouse cells. EMBO J. 4, 3145-3151
2. Healy, S., Khan, P., and Davie, J. R. (2013) Immediate early response genes and cell transformation. Pharmacol. Ther. 137, 64-77
3. Chang, H. Y., Sneddon, J. B., Alizadeh, A. A., Sood, R., West, R. B., Montgomery, K., Chi, J. T., van de Rijn, M., Botstein, D., and Brown, P. O. (2004) Gene expression signature of fibroblast serum response predicts human cancer progression: similarities between tumors and wounds. PLoS Biol. 2, E7
4. Zullo, J. N., Cochran, B. H., Huang, A. S., and Stiles, C. D. (1985) Platelet-derived growth factor and double-stranded ribonucleic acids stimulate expression of the same genes in 3T3 cells. Cell 43, 793-800
5. Stoecklin, G., Gross, B., Ming, X. F., and Moroni, C. (2003) A novel mechanism of tumor suppression by destabilizing AU-rich growth factor mRNA. Oncogene 22, 3554-3561
6. Brennan, S. E., Kuwano, Y., Alkharouf, N., Blackshear, P. J., Gorospe, M., and Wilson, G. M. (2009) The mRNA-destabilizing protein tristetraprolin is suppressed in many cancers, altering tumorigenic phenotypes and patient prognosis. Cancer Res. 69, 5168-5176
7. Sanduja, S., Blanco, F. F., Young, L. E., Kaza, V., and Dixon, D. A. (2012) The role of tristetraprolin in cancer and inflammation. Front. Biosci. 17, 174-188
8. DuBois, R. N., McLane, M. W., Ryder, K., Lau, L. F., and Nathans, D. (1990) A growth factor-inducible nuclear protein with a novel cysteine/ histidine repetitive sequence. J. Biol. Chem. 265, 19185-19191
9. Lai, W. S., Stumpo, D. J., and Blackshear, P. J. (1990) Rapid insulin-stimulated accumulation of an mRNA encoding a proline-rich protein. J. Biol. Chem. 265, 16556-16563
10. Klein, G. (1993) Genes that can antagonize tumor development. FASEB J. 7, 821-825
11. Hassel, B. A., Zhou, A., Sotomayor, C., Maran, A., and Silverman, R. H. (1993) A dominant negative mutant of 2-5A-dependent RNase suppresses antiproliferative and antiviral effects of interferon. EMBO J. 12, 3297-3304
12. Andersen, J. B., Mazan-Mamczarz, K., Zhan, M., Gorospe, M., and Hassel, B. A. (2009) Ribosomal protein mRNAs are primary targets of regulation in RNase L-induced senescence. RNA Biol. 6, 305-315
13. Sanduja, S., Kaza, V., and Dixon, D. A. (2009) The mRNA decay factor tristetraprolin (TTP) induces senescence in human papillomavirus-transformed cervical cancer cells by targeting E6-AP ubiquitin ligase. Aging 1, 803-817
14. Hovanessian, A. G. (2007) On the discovery of interferon-inducible, double-stranded RNA activated enzymes: the 2′-5′ oligoadenylate synthetases and the protein kinase PKR. Cytokine Growth Factor Rev. 18, 351-361
15. Silverman, R. H. (2007) A scientific journey through the 2-5A/RNase L system. Cytokine Growth Factor Rev. 18, 381-388
16. Malathi, K., Dong, B., Gale, M., Jr., and Silverman, R. H. (2007) Small self-RNA generated by RNase L amplifies antiviral innate immunity. Nature 448, 816-819
17. Li, X. L., Ezelle, H. J., Kang, T. J., Zhang, L., Shirey, K. A., Harro, J., Hasday, J. D., Mohapatra, S. K., Crasta, O. R., Vogel, S. N., Cross, A. S., and Hassel, B. A. (2008) An essential role for the antiviral endoribonuclease, RNase L, in antibacterial immunity. Proc. Natl. Acad. Sci. U.S.A. 105, 20816-20821
18. Ezelle, H. J., and Hassel, B. A. (2012) Pathologic effects of RNase L dysregulation in immunity and proliferative control. Front. Biosci. 4, 767-786
19. Chakrabarti, A., Jha, B. K., and Silverman, R. H. (2011) New insights into the role of RNase L in innate immunity. J. Interferon Cytokine Res. 31, 49-57
20. Jacobsen, H., Krause, D., Friedman, R. M., and Silverman, R. H. (1983) Induction of ppp(A2′p)nA-dependent RNase in murine JLS-V9R cells during growth inhibition. Proc. Natl. Acad. Sci. U.S.A. 80, 4954-4958
21. Bourgeade, M. F., and Besanc¸on, F. (1984) Induction of 2′,5′-oligoadenylate synthetase by retinoic acid in two transformed human cell lines. Cancer Res. 44, 5355-5360
22. Krishnan, I., and Baglioni, C. (1980) Increased levels of (2′-5′)oligo(A) polymerase activity in human lymphoblastoid cells treated with glucocorticoids. Proc. Natl. Acad. Sci. U.S.A. 77, 6506-6510
23. Al-Haj, L., Blackshear, P. J., and Khabar, K. S. (2012) Regulation of p21/ CIP1/WAF-1 mediated cell-cycle arrest by RNase L and tristetraprolin, and involvement of AU-rich elements. Nucleic Acids Res. 40, 7739-7752
24. Andersen, J. B., Li, X. L., Judge, C. S., Zhou, A., Jha, B. K., Shelby, S., Zhou, L., Silverman, R. H., and Hassel, B. A. (2007) Role of 2-5A-dependent RNase L in senescence and longevity. Oncogene 26, 3081-3088
25. Zhou, A., Paranjape, J., Brown, T. L., Nie, H., Naik, S., Dong, B., Chang, A., Trapp, B., Fairchild, R., Colmenares, C., and Silverman, R. H. (1997) Interferon action and apoptosis are defective in mice devoid of 2′,5′-oligoadenylate-dependent RNase L. EMBO J. 16, 6355-6363
26. Castelli, J. C., Hassel, B. A., Wood, K. A., Li, X. L., Amemiya, K., Dalakas, M. C., Torrence, P. F., and Youle, R. J. (1997) A study of the interferon antiviral mechanism: Apoptosis activation by the 2-5A system. J. Exp. Med. 186, 967-972
27. Liu, W., Liang, S. L., Liu, H., Silverman, R., and Zhou, A. (2007) Tumour suppressor function of RNase L in a mouse model. Eur. J. Cancer 43, 202-209
28. Long, T. M., Chakrabarti, A., Ezelle, H. J., Brennan-Laun, S. E., Raufman, J. P., Polyakova, I., Silverman, R. H., and Hassel, B. A. (2013) RNase L deficiency exacerbates experimental colitis and colitis-associated cancer. Inflamm. Bowel Dis. 19, 1295-1305
29. Carpten, J., Nupponen, N., Isaacs, S., Sood, R., Robbins, C., Xu, J., Faruque, M., Moses, T., Ewing, C., Gillanders, E., Hu, P., Bujnovszky, P., Makalowska, I., Baffoe-Bonnie, A., Faith, D., Smith, J., Stephan, D., Wiley, K., Brownstein, M., Gildea, D., Kelly, B., Jenkins, R., Hostetter, G., Matikainen, M., Schleutker, J., Klinger, K., Connors, T., Xiang, Y., Wang, Z., De Marzo, A., Papadopoulos, N., Kallioniemi, O. P., Burk, R., Meyers, D., Grönberg, H., Meltzer, P., Silverman, R., Bailey-Wilson, J., Walsh, P., Isaacs, W., and Trent, J. (2002) Germline mutations in the ribonuclease L gene in families showing linkage with HPC1. Nat. Genet. 30, 181-184
30. Casey, G., Neville, P. J., Plummer, S. J., Xiang, Y., Krumroy, L. M., Klein, E. A., Catalona, W. J., Nupponen, N., Carpten, J. D., Trent, J. M., Silverman, R. H., and Witte, J. S. (2002) RNASEL Arg462Gln variant is implicated in up to 13% of prostate cancer cases. Nat. Genet. 32, 541-543
31. Meyer, M. S., Penney, K. L., Stark, J. R., Schumacher, F. R., Sesso, H. D., Loda, M., Fiorentino, M., Finn, S., Flavin, R. J., Kurth, T., Price, A. L., Giovannucci, E. L., Fall, K., Stampfer, M. J., Ma, J., and Mucci, L. A. (2010) Genetic variation in RNASEL associated with prostate cancer risk and progression. Carcinogenesis 31, 1597-1603
32. Madsen, B. E., Ramos, E. M., Boulard, M., Duda, K., Overgaard, J., Nordsmark, M., Wiuf, C., and Hansen, L. L. (2008) Germline mutation in RNASEL predicts increased risk of head and neck, uterine cervix and breast cancer. Plos One 3, e2492
33. Dong, B., and Silverman, R. H. (1997) A bipartite model of 2-5A-dependent RNase L. J. Biol. Chem. 272, 22236-22242
34. Zhou, A., Hassel, B. A., and Silverman, R. H. (1993) Expression cloning of 2-5A-dependent RNAase: a uniquely regulated mediator of interferon action. Cell 72, 753-765
35. Zhou, A., Molinaro, R. J., Malathi, K., and Silverman, R. H. (2005) Mapping of the human RNASEL promoter and expression in cancer and normal cells. J. Interferon Cytokine Res. 25, 595-603
36. Clemens, M. J., and Williams, B. R. (1978) Inhibition of cell-free protein synthesis by pppA2′ p5′ A2′ p5′ A: a novel oligonucleotide synthesized by interferon-treated L cell extracts. Cell 13, 565-572
37. Silverman, R. H., Jung, D. D., Nolan-Sorden, N. L., Dieffenbach, C. W., Kedar, V. P., and SenGupta, D. N. (1988) Purification and analysis of murine 2-5A-dependent RNase. J. Biol. Chem. 263, 7336-7341
38. Dong, B., and Silverman, R. H. (1995) 2-5A-dependent RNase molecules dimerize during activation by 2-5A. J. Biol. Chem. 270, 4133-4137
39. Huang, H., Zeqiraj, E., Dong, B., Jha, B. K., Duffy, N. M., Orlicky, S., Thevakumaran, N., Talukdar, M., Pillon, M. C., Ceccarelli, D. F., Wan, L. C., Juang, Y. C., Mao, D. Y., Gaughan, C., Brinton, M. A., Perelygin, A. A., Kourinov, I., Guarné, A., Silverman, R. H., and Sicheri, F. (2014) Dimeric structure of pseudokinase RNase L bound to 2-5A reveals a basis for interferon-induced antiviral activity. Mol. Cell 53, 221-234
40. Han, Y., Donovan, J., Rath, S., Whitney, G., Chitrakar, A., and Korennykh, A. (2014) Structure of human RNase L reveals the basis for regulated RNA decay in the IFN response. Science 343, 1244-1248
41. Silverman, R. H. (2007) Viral encounters with 2′,5′-oligoadenylate synthetase and RNase L during the interferon antiviral response. J. Virol. 81, 12720-12729
42. Fabre, O., Salehzada, T., Lambert, K., Boo Seok, Y., Zhou, A., Mercier, J., and Bisbal, C. (2012) RNase L controls terminal adipocyte differentiation, lipids storage and insulin sensitivity via CHOP10 mRNA regulation. Cell Death Differ. 19, 1470-1481
43. Malathi, K., Paranjape, J. M., Bulanova, E., Shim, M., Guenther-Johnson, J. M., Faber, P. W., Eling, T. E., Williams, B. R., and Silverman, R. H. (2005) A transcriptional signaling pathway in the IFN system mediated by 2′-5′-oligoadenylate activation of RNase L. Proc. Natl. Acad. Sci. U.S.A. 102, 14533-14538
44. Domingo-Gil, E., González, J. M., and Esteban, M. (2010) Identification of cellular genes induced in human cells after activation of the OAS/ RNase L pathway by vaccinia virus recombinants expressing these antiviral enzymes. J. Interferon Cytokine Res. 30, 171-188
45. Brennan-Laun, S. E., Ezelle, H. J., Li, X. L., and Hassel, B. A. (2014) RNase L control of cellular mRNAs: roles in biologic functions and mechanisms of substrate targeting. J. Interferon Cytokine Res. 34, 275-288
46. Fabian, M. R., Sonenberg, N., and Filipowicz, W. (2010) Regulation of mRNA translation and stability by microRNAs. Annu. Rev. Biochem. 79, 351-379
47. Brooks, S. A., Connolly, J. E., and Rigby, W. F. (2004) The role of mRNA turnover in the regulation of tristetraprolin expression: evidence for an extracellular signal-regulated kinase-specific, AU-rich element-dependent, autoregulatory pathway. J. Immunol. 172, 7263-7271
48. Tchen, C. R., Brook, M., Saklatvala, J., and Clark, A. R. (2004) The stability of tristetraprolin mRNA is regulated by mitogen-activated protein kinase p38 and by tristetraprolin itself. J. Biol. Chem. 279, 32393-32400
49. Chen, C. Y., and Shyu, A. B. (1995) AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem. Sci. 20, 465-470
50. Lai, W. S., Carballo, E., Thorn, J. M., Kennington, E. A., and Blackshear, P. J. (2000) Interactions of CCCH zinc finger proteins with mRNA. Binding of tristetraprolin-related zinc finger proteins to Au-rich elements and destabilization of mRNA. J. Biol. Chem. 275, 17827-17837
51. Wilusz, C. J., Wormington, M., and Peltz, S. W. (2001) The cap-to-tail guide to mRNA turnover. Nat. Rev. Mol. Cell Biol. 2, 237-246
52. Sandler, H., Kreth, J., Timmers, H. T., and Stoecklin, G. (2011) Not1 mediates recruitment of the deadenylase Caf1 to mRNAs targeted for degradation by tristetraprolin. Nucleic Acids Res. 39, 4373-4386
53. Hau, H. H., Walsh, R. J., Ogilvie, R. L., Williams, D. A., Reilly, C. S., and Bohjanen, P. R. (2007) Tristetraprolin recruits functional mRNA decay complexes to ARE sequences. J. Cell Biochem. 100, 1477-1492
54. Lykke-Andersen, J., and Wagner, E. (2005) Recruitment and activation of mRNA decay enzymes by two ARE-mediated decay activation domains in the proteins TTP and BRF-1. Genes Dev. 19, 351-361
55. Chen, C. Y., Gherzi, R., Ong, S. E., Chan, E. L., Raijmakers, R., Pruijn, G. J., Stoecklin, G., Moroni, C., Mann, M., and Karin, M. (2001) AU binding proteins recruit the exosome to degrade ARE-containing mRNAs. Cell 107, 451-464
56. Marderosian, M., Sharma, A., Funk, A. P., Vartanian, R., Masri, J., Jo, O. D., and Gera, J. F. (2006) Tristetraprolin regulates cyclin D1 and c-Myc mRNA stability in response to rapamycin in an Akt-dependent manner via p38 MAPK signaling. Oncogene 25, 6277-6290
57. Kim, H. K., Kim, C. W., Vo, M. T., Lee, H. H., Lee, J. Y., Yoon, N. A., Lee, C. Y., Moon, C. H., Min, Y. J., Park, J. W., and Cho, W. J. (2012) Expression of proviral integration site for Moloney murine leukemia virus 1 (Pim-1) is post-transcriptionally regulated by tristetraprolin in cancer cells. J. Biol. Chem. 287, 28770-28778
58. Boutaud, O., Dixon, D. A., Oates, J. A., and Sawaoka, H. (2003) Tristetraprolin binds to the COX-2 mRNA 3′ untranslated region in cancer cells. Adv. Exp. Med. Biol. 525, 157-160
59. Mahat, D. B., Brennan-Laun, S. E., Fialcowitz-White, E. J., Kishor, A., Ross, C. R., Pozharskaya, T., Rawn, J. D., Blackshear, P. J., Hassel, B. A., and Wilson, G. M. (2012) Coordinated expression of tristetraprolin posttranscriptionally attenuates mitogenic induction of the oncogenic Ser/Thr kinase pim-1. PLoS One 7, e33194
60. Lee, H. H., Vo, M. T., Kim, H. J., Lee, U. H., Kim, C. W., Kim, H. K., Ko, M. S., Lee, W. H., Cha, S. J., Min, Y. J., Choi, D. H., Suh, H. S., Lee, B. J., Park, J. W., and Cho, W. J. (2010) Stability of the LATS2 tumor suppressor gene is regulated by tristetraprolin. J. Biol. Chem. 285, 17329-17337
61. Masuda, K., Marasa, B., Martindale, J. L., Halushka, M. K., and Gorospe, M. (2009) Tissue- and age-dependent expression of RNA-binding proteins that influence mRNA turnover and translation. Aging 1, 681-698
62. Johnson, B. A., Geha, M., and Blackwell, T. K. (2000) Similar but distinct effects of the tristetraprolin/TIS11 immediate-early proteins on cell survival. Oncogene 19, 1657-1664
63. Rounbehler, R. J., Fallahi, M., Yang, C., Steeves, M. A., Li, W., Doherty, J. R., Schaub, F. X., Sanduja, S., Dixon, D. A., Blackshear, P. J., and Cleveland, J. L. (2012) Tristetraprolin impairs myc-induced lymphoma and abolishes the malignant state. Cell 150, 563-574
64. Ross, C. R., Brennan-Laun, S. E., and Wilson, G. M. (2012) Tristetraprolin: roles in cancer and senescence. Ageing Res. Rev. 11, 473-484
65. Brooks, S. A., and Blackshear, P. J. (2013) Tristetraprolin (TTP): Interactions with mRNA and proteins, and current thoughts on mechanisms of action. Biochim. Biophys. Acta 1829, 666-679
66. Shi, Z., and Rockey, D. C. (2010) Interferon-γ-mediated inhibition of serum response factor-dependent smooth muscle-specific gene expression. J. Biol. Chem. 285, 32415-32424
67. Taylor, G. A., Carballo, E., Lee, D. M., Lai, W. S., Thompson, M. J., Patel, D. D., Schenkman, D. I., Gilkeson, G. S., Broxmeyer, H. E., Haynes, B. F., and Blackshear, P. J. (1996) A pathogenetic role for TNFα in the syndrome of cachexia, arthritis, and autoimmunity resulting from tristetraprolin (TTP) deficiency. Immunity 4, 445-454
68. Dong, B., and Silverman, R. H. (1999) Alternative function of a protein kinase homology domain in 2′,5′-oligoadenylate dependent RNase L. Nucleic Acids Res. 27, 439-445
69. Lai, W. S., Carballo, E., Strum, J. R., Kennington, E. A., Phillips, R. S., and Blackshear, P. J. (1999) Evidence that tristetraprolin binds to AU-rich elements and promotes the deadenylation and destabilization of tumor necrosis factor α mRNA. Mol. Cell. Biol. 19, 4311-4323
70. Li, X. L., Andersen, J. B., Ezelle, H. J., Wilson, G. M., and Hassel, B. A. (2007) Post-transcriptional regulation of RNase L expression is mediated by the 3′-untranslated region of its mRNA. J. Biol. Chem. 282, 7950-7960
71. Suzuki, A., Tsutomi, Y., Akahane, K., Araki, T., and Miura, M. (1998) Resistance to Fas-mediated apoptosis: activation of caspase 3 is regulated by cell cycle regulator p21WAF1 and IAP gene family ILP. Oncogene 17, 931-939
72. Lal, A., Mazan-Mamczarz, K., Kawai, T., Yang, X., Martindale, J. L., and Gorospe, M. (2004) Concurrent versus individual binding of HuR and AUF1 to common labile target mRNAs. EMBO J. 23, 3092-3102
73. Nakajima, K., and Wall, R. (1991) Interleukin-6 signals activating junB and TIS11 gene transcription in a B-cell hybridoma. Mol. Cell. Biol. 11, 1409-1418
74. Suzuki, K., Nakajima, H., Ikeda, K., Maezawa, Y., Suto, A., Takatori, H., Saito, Y., and Iwamoto, I. (2003) IL-4-Stat6 signaling induces tristetraprolin expression and inhibits TNF-α production in mast cells. J. Exp. Med. 198, 1717-1727
75. Sauer, I., Schaljo, B., Vogl, C., Gattermeier, I., Kolbe, T., Müller, M., Blackshear, P. J., and Kovarik, P. (2006) Interferons limit inflammatory responses by induction of tristetraprolin. Blood 107, 4790-4797
76. Anderson, P. (2010) Post-transcriptional regulons coordinate the initiation and resolution of inflammation. Nat. Rev. Immunol. 10, 24-35
77. Kyriakis, J. M., and Avruch, J. (2012) Mammalian MAPK signal transduction pathways activated by stress and inflammation: a 10-year update. Physiol. Rev. 92, 689-737
78. Lai, W. S., Thompson, M. J., and Blackshear, P. J. (1998) Characteristics of the intron involvement in the mitogen-induced expression of Zfp-36. J. Biol. Chem. 273, 506-517
79. Varnum, B. C., Lim, R. W., Sukhatme, V. P., and Herschman, H. R. (1989) Nucleotide sequence of a cDNA encoding TIS11, a message induced in Swiss 3T3 cells by the tumor promoter tetradecanoyl phorbol acetate. Oncogene 4, 119-120
80. Schaljo, B., Kratochvill, F., Gratz, N., Sadzak, I., Sauer, I., Hammer, M., Vogl, C., Strobl, B., Müller, M., Blackshear, P. J., Poli, V., Lang, R., Murray, P. J., and Kovarik, P. (2009) Tristetraprolin is required for full anti-inflammatory response of murine macrophages to IL-10. J. Immunol. 183, 1197-1206
81. Clark, K. A., and Graves, B. J. (2014) Dual views of SRF: a genomic exposure. Genes Dev. 28, 926-928
82. Treisman, R. (1994) Ternary complex factors: growth factor regulated transcriptional activators. Curr. Opin. Genet. Dev. 4, 96-101
83. Matys, V., Kel-Margoulis, O. V., Fricke, E., Liebich, I., Land, S., Barre-Dirrie, A., Reuter, I., Chekmenev, D., Krull, M., Hornischer, K., Voss, N., Stegmaier, P., Lewicki-Potapov, B., Saxel, H., Kel, A. E., and Wingender, E. (2006) TRANSFAC and its module TRANSCompel: transcriptional gene regulation in eukaryotes. Nucleic Acids Res. 34, D108-D110
84. Descot, A., Hoffmann, R., Shaposhnikov, D., Reschke, M., Ullrich, A., and Posern, G. (2009) Negative regulation of the EGFR-MAPK cascade by actin-MAL-mediated Mig6/Errfi-1 induction. Mol. Cell 35, 291-304
85. Bakheet, T., Williams, B. R., and Khabar, K. S. (2003)ARED2.0: an update of AU-rich element mRNA database. Nucleic Acids Res. 31, 421-423
86. Cha, H. J., Lee, H. H., Chae, S. W., Cho, W. J., Kim, Y. M., Choi, H. J., Choi, D. H., Jung, S. W., Min, Y. J., Lee, B. J., Park, S. E., and Park, J. W. (2011) Tristetraprolin down-regulates the expression of both VEGF and COX-2 in human colon cancer. Hepatogastroenterology 58, 790-795
87. Lee, H. H., Son, Y. J., Lee, W. H., Park, Y. W., Chae, S. W., Cho, W. J., Kim, Y. M., Choi, H. J., Choi, D. H., Jung, S. W., Min, Y. J., Park, S. E., Lee, B. J., Cha, H. J., and Park, J. W. (2010) Tristetraprolin regulates expression of VEGF and tumorigenesis in human colon cancer. Int. J. Cancer 126, 1817-1827
88. Chen, Y. L., Huang, Y. L., Lin, N. Y., Chen, H. C., Chiu, W. C., and Chang, C. J. (2006) Differential regulation of ARE-mediated TNFα and IL-1β mRNA stability by lipopolysaccharide in RAW264.7 cells. Biochem. Biophys. Res. Commun. 346, 160-168
89. Kim, T. W., Yim, S., Choi, B. J., Jang, Y., Lee, J. J., Sohn, B. H., Yoo, H. S., Yeom, Y. I., and Park, K. C. (2010) Tristetraprolin regulates the stability of HIF-1α mRNA during prolonged hypoxia. Biochem. Biophys. Res. Commun. 391, 963-968
90. Volinsky, N., and Kholodenko, B. N. (2013) Complexity of receptor tyrosine kinase signal processing. Cold Spring Harb. Perspect. Biol. 5, a009043
91. Treisman, R. (1992) The serum response element. Trends Biochem. Sci. 17, 423-426
92. Xie, L., Sullivan, A. L., Collier, J. G., and Glass, C. K. (2013) Serum response factor indirectly regulates type I interferon-signaling in macrophages. J. Interferon Cytokine Res. 33, 588-596
93. Jha, B. K., Polyakova, I., Kessler, P., Dong, B., Dickerman, B., Sen, G. C., and Silverman, R. H. (2011) Inhibition of RNase L and RNA-dependent protein kinase (PKR) by sunitinib impairs antiviral innate immunity. J. Biol. Chem. 286, 26319-26326
94. Zhang, S. X., Garcia-Gras, E., Wycuff, D. R., Marriot, S. J., Kadeer, N., Yu, W., Olson, E. N., Garry, D. J., Parmacek, M. S., and Schwartz, R. J. (2005) Identification of direct serum-response factor gene targets during Me2SO-induced P19 cardiac cell differentiation. J. Biol. Chem. 280, 19115-19126
95. Selvaraj, A., and Prywes, R. (2004) Expression profiling of serum inducible genes identifies a subset of SRF target genes that are MKL-dependent. BMC Mol. Biol. 5, 13
96. Stritt, C., Stern, S., Harting, K., Manke, T., Sinske, D., Schwarz, H., Vingron, M., Nordheim, A., and Knöll, B. (2009) Paracrine control of oligodendrocyte differentiation by SRF-directed neuronal gene expression. Nat. Neurosci. 12, 418-427
97. Sun, Q., Chen, G., Streb, J. W., Long, X., Yang, Y., Stoeckert, C. J., Jr., and Miano, J. M. (2006) Defining the mammalian CArGome. Genome Res. 16, 197-207
98. Halees, A. S., El-Badrawi, R., and Khabar, K. S. (2008) ARED Organism: expansion of ARED reveals AU-rich element cluster variations between human and mouse. Nucleic Acids Res. 36, D137-D140
99. Johnson, B. A., Stehn, J. R., Yaffe, M. B., and Blackwell, T. K. (2002) Cytoplasmic localization of tristetraprolin involves 14-3-3-dependent and -independent mechanisms. J. Biol. Chem. 277, 18029-18036
100. Kedar, V. P., Zucconi, B. E., Wilson, G. M., and Blackshear, P. J. (2012) Direct binding of specific AUF1 isoforms to tandem zinc finger domains of tristetraprolin (TTP) family proteins. J. Biol. Chem. 287, 5459-5471
101. Sawaoka, H., Dixon, D. A., Oates, J. A., and Boutaud, O. (2003) Tristetraprolin binds to the 3′-untranslated region of cyclooxygenase-2 mRNA. A polyadenylation variant in a cancer cell line lacks the binding site. J. Biol. Chem. 278, 13928-13935
102. Suswam, E. A., Shacka, J. J., Walker, K., Lu, L., Li, X., Si, Y., Zhang, X., Zheng, L., Nabors, L. B., Cao, H., and King, P. H. (2013) Mutant tristetraprolin: a potent inhibitor of malignant glioma cell growth. J. Neurooncol. 113, 195-205
103. Hanahan, D., and Weinberg, R. A. (2011) Hallmarks of cancer: the next generation. Cell 144, 646-674
104. Spencer, J. A., and Misra, R. P. (1999) Expression of the SRF gene occurs through a Ras/Sp/SRF-mediated-mechanism in response to serum growth signals. Oncogene 18, 7319-7327
105. Hausburg, M. A. (2010) Tristetraprolin Regulation of MyoD mRNA Stablity Commits Quiescent Adult Muscle Stem Cells to Myogenesis. Ph.D. thesis, University of Colorado at Boulder
106. Bisbal, C., Silhol, M., Laubenthal, H., Kaluza, T., Carnac, G., Milligan, L., Le Roy, F., and Salehzada, T. (2000) The 2-5′ oligoadenylate/RNase L/RNase L inhibitor pathway regulates both MyoD mRNA stability and muscle cell differentiation. Mol. Cell. Biol. 20, 4959-4969
107. Guerci, A., Lahoute, C., Hébrard, S., Collard, L., Graindorge, D., Favier, M., Cagnard, N., Batonnet-Pichon, S., Précigout, G., Garcia, L., Tuil, D., Daegelen, D., and Sotiropoulos, A. (2012) Srf-dependent paracrine signals produced by myofibers control satellite cell-mediated skeletal muscle hypertrophy. Cell Metab. 15, 25-37
108. Yi, X., Zeng, C., Liu, H., Chen, X., Zhang, P., Yun, B. S., Jin, G., and Zhou, A. (2013) Lack of RNase L attenuates macrophage functions. Plos One 8, e81269
109. Bros, M., Wiechmann, N., Besche, V., Art, J., Pautz, A., Grabbe, S., Kleinert, H., and Reske-Kunz, A. B. (2010) The RNA-binding protein tristetraprolin influences the activation state of murine dendritic cells. Mol. Immunol. 47, 1161-1170
110. Esnault, C., Stewart, A., Gualdrini, F., East, P., Horswell, S., Matthews, N., and Treisman, R. (2014) Rho-actin signaling to the MRTF coactivators dominates the immediate transcriptional response to serum in fibroblasts. Genes Dev. 28, 943-958
111. Benson, C. C., Zhou, Q., Long, X., and Miano, J. M. (2011) Identifying functional single nucleotide polymorphisms in the human CArGome. Physiol. Genomics 43, 1038-1048
112. Treisman, R. (1995) Journey to the surface of the cell: Fos regulation and the SRE. EMBO J. 14, 4905-4913
113. Raghavan, A., Robison, R. L., McNabb, J., Miller, C. R., Williams, D. A., and Bohjanen, P. R. (2001) HuA and tristetraprolin are induced following T cell activation and display distinct but overlapping RNA binding specificities. J. Biol. Chem. 276, 47958-47965
114. Kimura, Y., Morita, T., Hayashi, K., Miki, T., and Sobue, K. (2010) Myocardin functions as an effective inducer of growth arrest and differentiation in human uterine leiomyosarcoma cells. Cancer Res. 70, 501-511
115. Stoecklin, G., Tenenbaum, S. A., Mayo, T., Chittur, S. V., George, A. D., Baroni, T. E., Blackshear, P. J., and Anderson, P. (2008) Genome-wide analysis identifies interleukin-10 mRNA as target of tristetraprolin. J. Biol. Chem. 283, 11689-11699
116. Kratochvill, F., Machacek, C., Vogl, C., Ebner, F., Sedlyarov, V., Gruber, A. R., Hartweger, H., Vielnascher, R., Karaghiosoff, M., Rülicke, T., Müller, M., Hofacker, I., Lang, R., and Kovarik, P. (2011) Tristetraprolindriven regulatory circuit controls quality and timing of mRNA decay in inflammation. Mol. Syst. Biol. 7, 560
117. Brewer, B. Y., Malicka, J., Blackshear, P. J., and Wilson, G. M. (2004) RNA sequence elements required for high affinity binding by the zinc finger domain of tristetraprolin: conformational changes coupled to the bipartite nature of Au-rich MRNA-destabilizing motifs. J. Biol. Chem. 279, 27870-27877