Mutant tristetraprolin: A potent inhibitor of malignant glioma cell growth

Journal of Neuro-Oncology

Volumn 113, Issue 2, 2013, Pages 195-205

  Suswam, Esther A ^a   Shacka, John J ^b,f   Walker, Kiera ^a   Lu, Liang ^a,f   Li, Xuelin ^a,f   Si, Ying ^a,f   Zhang, Xiaowen ^e   Zheng, Lei ^a   Nabors, L Burt ^a   Cao, Heping ^g   King, Peter H ^a,c,d,f  

^a University of Alabama at Birmingham   (United States)

^b University of Alabama at Birmingham   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^d UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^e University of Alabama at Birmingham   (United States)

^f BIRMINGHAM VA MEDICAL CENTER   (United States)

^g SOUTHERN REGIONAL RESEARCH CENTER   (United States)

Author keywords

IL 6; IL 8; Post transcriptional gene regulation; RNA stability; VEGF

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 4 (4 FLUOROPHENYL) 2 (4 HYDROXYPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ADENINE; ALANINE; GROWTH FACTOR; HUR PROTEIN; INTERLEUKIN 6; INTERLEUKIN 8; MUTANT PROTEIN; MUTANT TRISTETRAPROLIN; PHOSPHOSERINE; TRISTETRAPROLIN; UNCLASSIFIED DRUG; URIDINE; VASCULOTROPIN; 3' UNTRANSLATED REGION; MESSENGER RNA; VASCULOTROPIN A; VEGFA PROTEIN, HUMAN;

3' UNTRANSLATED REGION; ANGIOGENESIS; ARTICLE; CANCER INHIBITION; CANCER RESISTANCE; CELL GROWTH; CELL VIABILITY; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GLIOBLASTOMA; GLIOMA CELL; HUMAN; HUMAN CELL; MACROAUTOPHAGY; NUCLEOTIDE SEQUENCE; PHENOTYPE; PHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STABILITY; TUMOR GROWTH; UPREGULATION; APOPTOSIS; BRAIN TUMOR; CELL PROLIFERATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENETICS; GLIOMA; IMMUNOPRECIPITATION; METABOLISM; MUTATION; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA STABILITY; WESTERN BLOTTING;

3' UNTRANSLATED REGIONS; APOPTOSIS; BLOTTING, WESTERN; BRAIN NEOPLASMS; CELL PROLIFERATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GLIOMA; HUMANS; IMMUNOPRECIPITATION; INTERLEUKIN-6; INTERLEUKIN-8; MUTATION; PHOSPHORYLATION; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA STABILITY; RNA, MESSENGER; TRISTETRAPROLIN; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84879069164     PISSN: 0167594X     EISSN: 15737373     Source Type: Journal    
DOI: 10.1007/s11060-013-1112-8     Document Type: Article

References (50)

1. Sanduja S, Blanco FF, Dixon DA (2011) The roles of TTP and BRF proteins in regulated mRNA decay. Wiley Interdiscip Rev RNA 2:42-57
2. Blackshear PJ (2002) Tristetraprolin and other CCCH tandem zinc-finger proteins in the regulation of mRNA turnover. Biochem Soc Trans 30:945-952
3. Fischer I, Gagner J-P, Law M, Newcomb EW, Zagzag D (2005) Angiogenesis in gliomas: biology and molecular pathophysiology. Brain Pathol 15:297-310
4. Brat DJ, Bellail AC, Van Meir EG (2005) The role of interleukin-8 and its receptors in gliomagenesis and tumoral angiogenesis. Neuro-oncol 7:122-133
5. Inda MM, Bonavia R, Mukasa A, Narita Y, Sah DW, Vandenberg S, Brennan C, Johns TG, Bachoo R, Hadwiger P, Tan P, Depinho RA, Cavenee W, Furnari F (2010) Tumor heterogeneity is an active process maintained by a mutant EGFR-induced cytokine circuit in glioblastoma. Genes Dev 24:1731-1745
6. Jin X, Yin J, Kim S-H, Sohn Y-W, Beck S, Lim YC, Nam D-H, Choi Y-J, Kim H (2011) EGFR-AKT-Smad signaling promotes formation of glioma stem-like cells and tumor angiogenesis by ID3-driven cytokine induction. Cancer Res 71:7125-7134
7. Beier D, Schulz J, Beier C (2011) Chemoresistance of glioblastoma cancer stem cells-much more complex than expected. Mol Cancer 10:128
8. de la Iglesia N, Konopka G, Lim KL, Nutt CL, Bromberg JF, Frank DA, Mischel PS, Louis DN, Bonni A (2008) Deregulation of a STAT3-interleukin 8 signaling pathway promotes human glioblastoma cell proliferation and invasiveness. J Neurosci 28:5870-5878
9. Raychaudhuri B, Vogelbaum M (2011) IL-8 is a mediator of NF-κB induced invasion by gliomas. J Neurooncol 101:227-235
10. Liu Q, Li G, Li R, Shen J, He Q, Deng L, Zhang C, Zhang J (2010) IL-6 promotion of glioblastoma cell invasion and angiogenesis in U251 and T98G cell lines. J Neurooncol 100:165-176
11. Filippova N, Yang X, Wang Y, Gillespie GY, Langford C, King PH, Wheeler C, Nabors LB (2011) The RNA-binding protein HuR promotes glioma growth and treatment resistance. Mol Cancer Res 9:648-659
12. Suswam E, Li Y, Zhang X, Gillespie GY, Li X, Shacka JJ, Lu L, Zheng L, King PH (2008) Tristetraprolin down-regulates interleukin-8 and vascular endothelial growth factor in malignant glioma cells. Cancer Res 68:674-682
13. Cao H, Deterding LJ, Blackshear PJ (2007) Phosphorylation site analysis of the anti-inflammatory and mRNA-destabilizing protein tristetraprolin. Expert Rev Proteomics 4:711-726
14. Cao H, Deterding LJ, Venable JD, Kennington EA, Yates JR, Tomer KB, Blackshear PJ (2006) Identification of the anti-inflammatory protein tristetraprolin as a hyperphosphorylated protein by mass spectrometry and site-directed mutagenesis. Biochem J 394:285-297
15. Carballo E, Cao H, Lai WS, Kennington EA, Campbell D, Blackshear PJ (2001) Decreased sensitivity of tristetraprolin-deficient cells to p38 inhibitors suggests the involvement of tristetraprolin in the p38 signaling pathway. J Biol Chem 276:42580-42587
16. Hitti E, Iakovleva T, Brook M, Deppenmeier S, Gruber AD, Radzioch D, Clark AR, Blackshear PJ, Kotlyarov A, Gaestel M (2006) Mitogen-activated protein kinase-activated protein kinase 2 regulates tumor necrosis factor mRNA stability and translation mainly by altering tristetraprolin expression, stability, and binding to adenine/uridine-rich element. Mol Cell Biol 26:2399-2407
17. Chen Y-L, Huang Y-L, Lin N-Y, Chen H-C, Chiu W-C, 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
18. Qian X, Ning H, Zhang J, Hoft DF, Stumpo DJ, Blackshear PJ, Liu J (2011) Posttranscriptional regulation of IL-23 expression by IFN-{gamma} through tristetraprolin. J Immunol 186(11):6454-6464
19. Meng Z, Jackson NL, Choi H, King PH, Emanuel PD, Blume SW (2008) Alterations in RNA-binding activities of IRES-regulatory proteins as a mechanism for physiological variability and pathological dysregulation of IGF-IR translational control in human breast tumor cells. J Cell Physiol 217:172-183
20. Nabors LB, Gillespie GY, Harkins L, King PH (2001) HuR, an RNA stability factor, is expressed in malignant brain tumors and binds to adenine and uridine-rich elements within the 3′ untranslated regions of cytokine and angiogenic factor mRNAs. Cancer Res 61:2154-2161
21. Nabors LB, Suswam E, Huang Y, Yang X, Johnson MJ, King PH (2003) Tumor necrosis factor-α induces angiogenic factor up-regulation in malignant glioma cells: a role for RNA stabilization and HuR. Cancer Res 63:4181-4187
22. Suswam EA, Nabors LB, Huang Y, Yang X, King PH (2005) IL-1β induces stabilization of IL-8 mRNA in malignant breast cancer cells via the 3′ untranslated region: involvement of divergent RNA-binding factors HuR, KSRP and TIAR. Int J Cancer 113:911-919
23. Vasudevan S, Steitz JA (2007) AU-Rich-element-mediated upregulation of translation by FXR1 and Argonaute 2. Cell 128:1105-1118
24. Chrestensen CA, Schroeder MJ, Shabanowitz J, Hunt DF, Pelo JW, Worthington MT, Sturgill TW (2004) MAPKAP kinase 2 phosphorylates tristetraprolin on in vivo sites including Ser178, a site required for 14-3-3 binding. J Biol Chem 279:10176-10184
25. Maher EA, Furnari FB, Bachoo RM, Rowitch DH, Louis DN, Cavenee WK, DePinho RA (2001) Malignant glioma: genetics and biology of a grave matter. Genes Dev 15:1311-1333
26. Brook M, Tchen CR, Santalucia T, McIlrath J, Arthur JSC, Saklatvala J, Clark AR (2006) Posttranslational regulation of tristetraprolin subcellular localization and protein stability by p38 mitogen-activated protein kinase and extracellular signal-regulated kinase pathways. Mol Cell Biol 26:2408-2418
27. Fiedler MA, Wernke-Dollries K, Stark JM (1996) Mechanism of RSV-induced IL-8 gene expression in A549 cells before viral replication. Am J Physiol Lung Cell Mol Physiol 271:L963-L971
28. Liang J, Lei T, Song Y, Yanes N, Qi Y, Fu M (2009) RNA-destabilizing factor tristetraprolin negatively regulates NF-kappaB signaling. J Biol Chem 284:29383-29390
29. Schichl YM, Resch U, Hofer-Warbinek R, de Martin R (2009) Tristetraprolin impairs NF-kappaB/p65 nuclear translocation. J Biol Chem 284:29571-29581
30. Amit I, Citri A, Shay T, Lu Y, Katz M, Zhang F, Tarcic G, Siwak D, Lahad J, Jacob-Hirsch J, Amariglio N, Vaisman N, Segal E, Rechavi G, Alon U, Mills GB, Domany E, Yarden Y (2007) A module of negative feedback regulators defines growth factor signaling. Nat Genet 39:503-512
31. Meyer-Ficca ML, Meyer RG, Kaiser H, Brack AR, Kandolf R, Kupper J-H (2004) Comparative analysis of inducible expression systems in transient transfection studies. Anal Biochem 334:9-19
32. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJB, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J, Janzer RC, Ludwin SK, Gorlia T, Allgeier A, Lacombe D, Cairncross JG, Eisenhauer E, Mirimanoff RO (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987-996
33. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 19:5720-5728
34. Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK et al (2008) Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 4:151-175
35. Brennan SE, Kuwano Y, Alkharouf N, Blackshear PJ, Gorospe M, Wilson GM (2009) The mRNA-destabilizing protein tristetraprolin is suppressed in many cancers, altering tumorigenic phenotypes and patient prognosis. Cancer Res 69:5168-5176
36. Ronkina N, Menon MB, Schwermann J, Tiedje C, Hitti E, Kotlyarov A, Gaestel M (2010) MAPKAP kinases MK2 and MK3 in inflammation: complex regulation of TNF biosynthesis via expression and phosphorylation of tristetraprolin. Biochem Pharmacol 80:1915-1920
37. Young LE, Sanduja S, Bemis-standoli K, Pena EA, Price RL, Dixon DA (2009) The mRNA binding proteins HuR and tristetraprolin regulate cyclooxygenase 2 expression during colon carcinogenesis. Gastroenterology 136:1669-1679
38. Dixon DA, Tolley ND, King PH, Nabors LB, McIntyre TM, Zimmerman GA, Prescott SM (2001) Altered expression of the mRNA stability factor HuR promotes cyclooxygenase-2 expression in colon cancer cells. J Clin Invest 108:1657-1665
39. Levy NS, Chung S, Furneaux H, Levy AP (1998) Hypoxic stabilization of vascular endothelial growth factor mRNA by the RNA-binding protein HuR. J Biol Chem 273:6417-6423
40. Spooren A, Mestdagh P, Rondou P, Kolmus K, Haegeman G, Gerlo S (2011) IL-1[beta] potently stabilizes IL-6 mRNA in human astrocytes. Biochem Pharmacol 81:1004-1015
41. Ming X-F, Stoecklin G, Lu M, Looser R, Moroni C (2001) Parallel and independent regulation of interleukin-3 mRNA turnover by phosphatidylinositol 3-kinase and p38 mitogen-activated protein kinase. Mol Cell Biol 21:5778-5789
42. Johnson BA, Stehn JR, Yaffe MB, Blackwell TK (2002) Cytoplasmic localization of tristetraprolin involves 14-3-3-dependent and -independent mechanisms. J Biol Chem 277:18029-18036
43. Zhu W, Brauchle MA, Di Padova F, Gram H, New L, Ono K, Downey JS, Han J (2001) Gene suppression by tristetraprolin and release by the p38 pathway. Am J Physiol Lung Cell Mol Physiol 281:L499-L508
44. Sandler H, Stoecklin G (2008) Control of mRNA decay by phosphorylation of tristetraprolin. Biochem Soc Trans 36:491-496
45. Anderson P, Kedersha N (2006) RNA granules. J Cell Biol 172:803-808
46. Clement SL, Scheckel C, Stoecklin G, Lykke-Andersen J (2011) Phosphorylation of tristetraprolin by MK2 impairs AU-rich element mRNA decay by preventing deadenylase recruitment. Mol Cell Biol 31:256-266
47. Franks TM, Lykke-Andersen J (2007) TTP and BRF proteins nucleate processing body formation to silence mRNAs with AU-rich elements. Genes Dev 21:719-735
48. Brennan CM, Steitz JA (2001) HuR and mRNA stability. Cell Mol Life Sci 58:266-277
49. Abdelmohsen K, Yuki K, Kim HH, Gorospe M (2008) Posttranscriptional gene regulation by RNA-binding proteins during oxidative stress: implications for cellular senescence. Biol Chem 389:243-255
50. Meads MB, Hazlehurst LA, Dalton WS (2008) The bone marrow microenvironment as a tumor sanctuary and contributor to drug resistance. Clin Cancer Res 14:2519-2526