The p38-MK2-HuR pathway potentiates EGFRvIII-IL-1β-driven IL-6 secretion in glioblastoma cells

Oncogene

Volumn 34, Issue 22, 2015, Pages 2934-2942

  Gurgis, F M S ^a   Yeung, Y T ^a   Tang, M X M ^a   Heng, B ^b   Buckland, M ^a   Ammit, A J ^a   Haapasalo, J ^c   Haapasalo, H ^c   Guillemin, G J ^b   Grewal, T ^a   Munoz, L ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b MACQUARIE UNIVERSITY   (Australia)

^c TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; EPIDERMAL GROWTH FACTOR RECEPTOR 3; HEAT SHOCK PROTEIN 27; HUR PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; LAMIN A; LAMIN C; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 2; MITOGEN ACTIVATED PROTEIN KINASE P38; STRESS ACTIVATED PROTEIN KINASE; SYNAPTOPHYSIN; ELAV LIKE PROTEIN 1; ELAV PROTEIN; ELAVL1 PROTEIN, HUMAN; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR VIII; HU ANTIGEN; IL6 PROTEIN, HUMAN; MAP-KINASE-ACTIVATED KINASE 2; PROTEIN SERINE THREONINE KINASE; SIGNAL PEPTIDE;

ARTICLE; ASTROCYTOMA; CANCER GRADING; CANCER GROWTH; CARCINOGENESIS; CELLULAR DISTRIBUTION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOSOLIC FRACTION; DOWN REGULATION; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME REGULATION; GENE SILENCING; GENE TRANSLOCATION; GLIOBLASTOMA; GLIOBLASTOMA CELL LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOREACTIVITY; INTERNALIZATION; MICROENVIRONMENT; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; PROTEIN STABILITY; PROTEIN SYNTHESIS; PROTEIN TARGETING; RNA DEGRADATION; SIGNAL TRANSDUCTION; UPREGULATION; BRAIN TUMOR; DRUG EFFECTS; GENETICS; INFLAMMATION; METABOLISM; PATHOLOGY; PHYSIOLOGY; SECRETION (PROCESS); TUMOR CELL CULTURE; TUMOR MICROENVIRONMENT;

BRAIN NEOPLASMS; ELAV PROTEINS; ELAV-LIKE PROTEIN 1; GLIOBLASTOMA; HU PARANEOPLASTIC ENCEPHALOMYELITIS ANTIGENS; HUMANS; INFLAMMATION; INTERLEUKIN-1BETA; INTERLEUKIN-6; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MAP KINASE SIGNALING SYSTEM; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; RECEPTOR, EPIDERMAL GROWTH FACTOR; TUMOR CELLS, CULTURED; TUMOR MICROENVIRONMENT;

EID: 84930081017     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2014.225     Document Type: Article

References (38)

1. Yeung YT, McDonald KL, Grewal T, Munoz L. Interleukins in glioblastoma pathophysiology: implications for therapy. Br J Pharmacol 2013; 168: 591-606.
2. The Cancer Genome Atlas Research, Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 2008; 455: 1061-1068.
3. Inda M, Bonavia R, Mukasa A, Narita Y, Sah D, Vandenberg S et al. Tumor heterogeneity is an active process maintained by a mutant EGFR-induced cytokine circuit in glioblastoma. Genes Dev 2010; 24: 1731-1745.
4. Jin X, Yin J, Kim S-H, Sohn Y-W, Beck S, Lim YC et al. EGFR-AKT-Smad signaling promotes formation of glioma stem-like cells and tumor angiogenesis by ID3-driven cytokine induction. Cancer Res 2011; 71: 7125-7134.
5. Zhang J, Sarkar S, Cua R, Zhou Y, Hader W, Yong VW. A dialog between glioma and microglia that promotes tumor invasiveness through the CCL2/CCR2/interleukin-6 axis. Carcinogenesis 2012; 33: 312-319.
6. Schulz I, Engel C, Niestroj A, Zeitschel U, Menge K, Kehlen A et al. Heteroarylketones inhibit astroglial interleukin-6 expression via a STAT3/NF-kappaB signaling pathway. J Neuroinflammation 2011; 8: 86.
7. Spooren A, Mestdagh P, Rondou P, Kolmus K, Haegeman G, Gerlo S. IL-1? potently stabilizes IL-6 mRNA in human astrocytes. Biochem Pharmacol 2011; 81: 1004-1015.
8. Yeung Y, Bryce N, Adams S, Braidy N, Konayagi M, McDonald K et al. p38 MAPK inhibitors attenuate pro-inflammatory cytokine production and invasiveness of human U251 glioblastoma cells. J Neurooncol 2012; 109: 35-44.
9. Nabors LB, Gillespie GY, Harkins L, King PH. HuR a 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 2001; 61: 2154-2161.
10. Meisner N-C, Hintersteiner M, Mueller K, Bauer R, Seifert J-M, Naegeli H-U et al. Identification and mechanistic characterization of low-molecular-weight inhibitors for HuR. Nat Chem Biol 2007; 3: 508-516.
11. Doller A, Pfeilschifter J, Eberhardt W. Signalling pathways regulating nucleocytoplasmic shuttling of the mRNA-binding protein HuR. Cell Signal 2008; 20: 2165-2173.
12. Lin W-N, Lin C-C, Cheng H-Y, Yang C-M. Regulation of cyclooxygenase-2 and cytosolic phospholipase A2 gene expression by lipopolysaccharide through the RNA-binding protein HuR: involvement of NADPH oxidase, reactive oxygen species and mitogen-activated protein kinases. Br J Pharmacol 2011; 163: 1691-1706.
13. Fernau NS, Fugmann D, Leyendecker M, Reimann K, Grether-Beck S, Galban S et al. Role of HuR and p38 MAPK in ultraviolet B-induced post-transcriptional regulation of COX-2 expression in the human keratinocyte cell line HaCaT. J Biol Chem 2010; 285: 3896-3904.
14. Wang S, Zhang J, Zhang Y, Kern S, Danner RL. Nitric oxide-p38 MAPK signaling stabilizes mRNA through AU-rich element-dependent and-independent mechanisms. J Leukocyte Biol 2008; 83: 982-990.
15. Ramgolam VS, DeGregorio SD, Rao GK, Collinge M, Subaran SS, Markovic-Plese S et al. T Cell LFA-1 engagement induces HuR-dependent cytokine mRNA stabilization through a Vav-1, Rac1/2, p38MAPK and MKK3 signaling cascade. PLoS ONE 2010; 5: e14450.
16. Winzen R, Kracht M, Ritter B, Wilhelm A, Chen CY, Shyu AB et al. The p38 MAP kinase pathway signals for cytokine-induced mRNA stabilization via MAP kinaseactivated protein kinase 2 and an AU-rich region-targeted mechanism. EMBO J 1999; 18: 4969-4980.
17. Neininger A, Kontoyiannis D, Kotlyarov A, Winzen R, Eckert R, Volk HD et al. MK2 targets AU-rich elements and regulates biosynthesis of tumor necrosis factor and interleukin-6 independently at different post-transcriptional levels. J Biol Chem 2002; 277: 3065-3068.
18. Gaestel M. MAPKAP kinases-MKs-two's company, three's a crowd. Nat Rev Mol Cell Biol 2006; 7: 120-130.
19. Miyata Y, Watanabe S, Sagara Y, Mitsunari K, Matsuo T, Ohba K et al. High expression of HuR in cytoplasm, but not nuclei, is associated with malignant aggressiveness and prognosis in bladder cancer. PLoS ONE 2013; 8: e59095.
20. Bolognani F, Gallani A-I, Sokol L, Baskin D, Meisner-Kober N. mRNA stability alterations mediated by HuR are necessary to sustain the fast growth of glioma cells. J Neurooncol 2012; 106: 531-542.
21. Filippova N, Yang X, Wang Y, Gillespie GY, Langford C, King PH et al. The RNA-binding protein HuR promotes glioma growth and treatment resistance. Mol Cancer Res 2011; 9: 648-659.
22. Bonavia R, Inda MM, Vandenberg S, Cheng S-Y, Nagane M, Hadwiger P et al. EGFRvIII promotes glioma angiogenesis and growth through the NFkB, interleukin-8 pathway. Oncogene 2011; 31: 4054-4066.
23. Avraham R, Yarden Y. Feedback regulation of EGFR signalling: decision making by early and delayed loops. Nat Rev Mol Cell Biol 2011; 12: 104-117.
24. Brzezinska AA, Johnson JL, Munafo DB, Ellis BA, Catz SD. Signalling mechanisms for Toll-like receptor-activated neutrophil exocytosis: key roles for interleukin-1-receptor-associated kinase-4 and phosphatidylinositol 3-kinase but not Toll/IL-1 receptor (TIR) domain-containing adaptor inducing IFN-? (TRIF). Immunology 2009; 127: 386-397.
25. Sumara G, Formentini I, Collins S, Sumara I, Windak R, Bodenmiller B et al. Regulation of PKD by the MAPK p38? in insulin secretion and glucose homeostasis. Cell 2009; 136: 235-248.
26. Cheng C, Kuo C, Lin C, Hsieh H, Yang C. IL-1? induces expression of matrix metalloproteinase-9 and cell migration via a c-Src-dependent, growth factor receptor transactivation in A549 cells. Br J Pharmacol 2010; 160: 1595-1610.
27. Munoz L, Selig R, Yeung Y, Peifer C, Laufer SA. Fluorescence polarisation binding assay to develop inhibitors of inactive p38a mitogen-activated protein kinase. Anal Biochem 2010; 401: 125-133.
28. Mourey RJ, Burnette BL, Brustkern SJ, Daniels JS, Hirsch JL, Hood WF et al. A Benzothiophene inhibitor of mitogen-activated protein kinase-activated protein kinase 2 inhibits tumor necrosis factor ? production and has oral antiinflammatory efficacy in acute and chronic models of inflammation. J Pharmacol Exp Ther 2010; 333: 797-807.
29. Gurgis FMS, Ziaziaris W, Munoz L. Mitogen-activated protein kinase-activated protein kinase 2 in neuroinflammation, heat shock protein 27 phosphorylation, and cell cycle: role and targeting. Mol Pharmacol 2014; 85: 345-356.
30. Kim HH, Abdelmohsen K, Lal A, Pullmann R, Yang X, Galban S et al. Nuclear HuR accumulation through phosphorylation by Cdk1. Genes Dev 2008; 22: 1804-1815.
31. Li L, Dutra A, Pak E, Labrie JE, Gerstein RM, Pandolfi PP et al. EGFRvIII expression and PTEN loss synergistically induce chromosomal instability and glial tumors. Neuro Oncol 2009; 11: 9-21.
32. Turner JG, Dawson J, Sullivan DM. Nuclear export of proteins and drug resistance in cancer. Biochem Pharmacol 2012; 83: 1021-1032.
33. Liao W, Wang W, Chang W, Tseng JT. The RNA-binding protein HuR stabilizes cytosolic phospholipase A2? mRNA under interleukin-1? treatment in non-small cell lung cancer A549 cells. J Biol Chem 2011; 286: 35499-35508.
34. Tran H, Maurer F, Nagamine Y. Stabilization of urokinase and urokinase receptor mRNAs by HuR is linked to its cytoplasmic accumulation induced by activated mitogen-activated protein kinase-activated protein kinase 2. Mol Cell Biol 2003; 23: 7177-7188.
35. Ohgaki H, Kleihues P. The definition of primary and secondary glioblastoma. Clin Cancer Res 2013; 19: 764-772.
36. Munoz L, Ralay Ranaivo H, Roy SM, Hu W, Craft JM, McNamara LK et al. A novel p38alpha MAPK inhibitor suppresses brain proinflammatory cytokine up-regulation and attenuates synaptic dysfunction and behavioral deficits in an Alzheimer's disease mouse model. J Neuroinflammation 2007; 4: 21.
37. Munoz L, Ramsay E, Manetsch M, Ge Q, Peifer C, Laufer SA et al. Novel p38 MAPK inhibitor ML3403 has potent anti-inflammatory activity in airway smooth muscle. Eur J Pharmacol 2010; 635: 212-218.
38. Guillemin GJ, Smythe G, Takikawa O, Brew BJ. Expression of indoleamine 2, 3-dioxygenase and production of quinolinic acid by human microglia, astrocytes, and neurons. Glia 2005; 49: 15-23.