CPEB regulation of TAK1 synthesis mediates cytokine production and the inflammatory immune response

Molecular and Cellular Biology

Volumn 35, Issue 3, 2015, Pages 610-618

  Ivshina, Maria ^a   Alexandrov, Ilya M ^a,b   Vertii, Anastassiia ^a   Doxsey, Stephen ^a   Richter, Joel D ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b Biomirex Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

7 OXOZEAENOL; CYTOPLASMIC POLYADENYLATION ELEMENT BINDING PROTEIN; ENZYME INHIBITOR; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; RNA BINDING PROTEIN; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; UNCLASSIFIED DRUG; CPEB PROTEIN, MOUSE; MAP KINASE KINASE KINASE 7; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; TUMOR NECROSIS FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; CROSS LINKING; CYTOKINE PRODUCTION; DRUG POTENCY; ENZYME SYNTHESIS; FIBROBLAST; HYPERSENSITIVITY; IMMUNE RESPONSE; IMMUNOPRECIPITATION; LENTIVIRINAE; MOUSE; MOUSE EMBRYO; NONHUMAN; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA TRANSLATION; SEPTIC SHOCK; SURVIVAL RATE; ANIMAL; IMMUNOLOGY; INFLAMMATION; MALE; METABOLISM; REGULATORY SEQUENCE; SIGNAL TRANSDUCTION;

ANIMALIA; MUS;

ANIMALS; INFLAMMATION; INTERLEUKIN-6; LIPOPOLYSACCHARIDES; MALE; MAP KINASE KINASE KINASES; MICE; NF-KAPPA B; REGULATORY SEQUENCES, NUCLEIC ACID; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84920913931     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00800-14     Document Type: Article

References (44)

1. Bezbradica JS, Medzhitov R. 2009. Integration of cytokine and heterologous receptor signaling pathways. Nat Immunol 10:333-339. http://dx .doi.org/10.1038/ni.1713.
2. Medzhitov R, Horng T. 2009. Transcriptional control of the inflammatory response. Nat Rev Immunol 9:692-703. http://dx.doi.org/10.1038 /nri2634.
3. Anderson P. 2010. Post-transcriptional regulons coordinate the initiation and resolution of inflammation. Nat Rev Immunol 10:24-35. http://dx .doi.org/10.1038/nri2685.
4. Xiao C, Ghosh S. 2005. NF-kappaB, an evolutionarily conserved mediator of immune and inflammatory responses. Adv Exp Med Biol 560:41- http://dx.doi.org/10.1007/0-387-24180-9_5.
5. Mercurio F, Zhu H, Murray BW, Shevchenko A, Bennett BL, Li J, Young DB, Barbosa M, Mann M, Manning A, Rao A. 1997. IKK-1 and IKK-2: cytokine-activated IkappaB kinases essential for NF-kappaB activation. Science 278:860-866. http://dx.doi.org/10.1126/science.278.5339 .860.
6. Stancovski I, Baltimore D. 1997. NF-kappaB activation: the I kappaB kinase revealed? Cell 91:299 -302. http://dx.doi.org/10.1016/S0092 -8674(00)80413-4.
7. Zandi E, Rothwarf DM, Delhase M, Hayakawa M, Karin M. 1997. The IkappaB kinase complex (IKK) contains two kinase subunits, IKKalpha and IKKbeta, necessary for IkappaB phosphorylation and NF-kappaB activation. Cell 91:243-252. http://dx.doi.org/10.1016 /S0092-8674(00)80406-7.
8. Hoffmann A, Baltimore D. 2006. Circuitry of nuclear factor kappaB signaling. Immunol Rev 210:171-186. http://dx.doi.org/10.1111/j.0105 -2896.2006.00375.x.
9. Verma IM, Stevenson JK, Schwarz EM, Van Antwerp D, Miyamoto S. 1995. Rel/NF-kappa B/I kappa B family: intimate tales of association and dissociation. Genes Dev 9:2723-2735. http://dx.doi.org/10.1101/gad.9.22 .2723.
10. Sakurai H. 2012. Targeting of TAK1 in inflammatory disorders and cancer. Trends Pharmacol Sci 33:522-530. http://dx.doi.org/10.1016/j.tips .2012.06.007.
11. Hao S, Baltimore D. 2009. The stability of mRNA influences the temporal order of the induction of genes encoding inflammatory molecules. Nat Immunol 10:281-288. http://dx.doi.org/10.1038/ni.1699.
12. Zhang T, Kruys V, Huez G, Gueydan C. 2002. AU-rich elementmediated translational control: complexity and multiple activities of trans-activating factors. Biochem Soc Trans 30:952-958. http://dx.doi.org /10.1042/bst0300952.
13. Hake LE, Richter JD. 1994. CPEB is a specificity factor that mediates cytoplasmic polyadenylation during Xenopus oocyte maturation. Cell 79: 617-627. http://dx.doi.org/10.1016/0092-8674(94)90547-9.
14. Richter JD. 2007. CPEB: a life in translation. Trends Biochem Sci 32:279- 285. http://dx.doi.org/10.1016/j.tibs.2007.04.004.
15. Tay J, Hodgman R, Sarkissian M, Richter JD. 2003. Regulated CPEB phosphorylation during meiotic progression suggests a mechanism for temporal control of maternal mRNA translation. Genes Dev 17:1457- 1462. http://dx.doi.org/10.1101/gad.1071403.
16. Tay J, Richter JD. 2001. Germ cell differentiation and synaptonemal complex formation are disrupted in CPEB knockout mice. Dev Cell 1:201-213. http://dx.doi.org/10.1016/S1534-5807(01)00025-9.
17. Alarcon JM, Hodgman R, Theis M, Huang YS, Kandel ER, Richter JD. 2004. Selective modulation of some forms of Schaffer collateral-CA1 synaptic plasticity in mice with a disruption of the CPEB-1 gene. Learn Mem 11:318-327. http://dx.doi.org/10.1101/lm.72704.
18. Richter JD, Klann E. 2009. Making synaptic plasticity and memory last: mechanisms of translational regulation. Genes Dev 23:1-11. http://dx.doi .org/10.1101/gad.1735809.
19. Udagawa T, Swanger SA, Takeuchi K, Kim JH, Nalavadi V, Shin J, Lorenz LJ, Zukin RS, Bassell GJ, Richter JD. 2012. Bidirectional control of mRNA translation and synaptic plasticity by the cytoplasmic polyadenylation complex. Mol Cell 47:253-266. http://dx.doi.org/10 .1016/j.molcel.2012.05.016.
20. Zearfoss NR, Alarcon JM, Trifilieff P, Kandel E, Richter JD. 2008. A molecular circuit composed of CPEB-1 and c-Jun controls growth hormone-mediated synaptic plasticity in the mouse hippocampus. J Neurosci 28:8502-8509. http://dx.doi.org/10.1523/JNEUROSCI.1756-08.2008.
21. Burns DM, D'Ambrogio A, Nottrott S, Richter JD. 2011. CPEB and two poly(A) polymerases control miR-122 stability and p53 mRNA translation. Nature 473:105-108. http://dx.doi.org/10.1038/nature09908.
22. Burns DM, Richter JD. 2008. CPEB regulation of human cellular senescence, energy metabolism, and p53 mRNA translation. Genes Dev 22: 3449-3460. http://dx.doi.org/10.1101/gad.1697808.
23. Groisman I, Ivshina M, Marin V, Kennedy NJ, Davis RJ, Richter JD. 2006. Control of cellular senescence by CPEB. Genes Dev 20:2701-2712. http://dx.doi.org/10.1101/gad.1438906.
24. Groppo R, Richter JD. 2011. CPEB control of NF-kappaB nuclear localization and interleukin-6 production mediates cellular senescence. Mol Cell Biol 31:2707-2714. http://dx.doi.org/10.1128/MCB.05133-11.
25. Alexandrov IM, Ivshina M, Jung DY, Friedline R, Ko HJ, Xu M, O'Sullivan-Murphy B, Bortell R, Huang YT, Urano F, Kim JK, Richter JD. 2012. Cytoplasmic polyadenylation element binding protein deficiency stimulates PTEN and Stat3 mRNA translation and induces hepatic insulin resistance. PLoS Genet 8:e1002457. http://dx.doi .org/10.1371/journal.pgen.1002457.
26. Sarkissian M, Mendez R, Richter JD. 2004. Progesterone and insulin stimulation of CPEB-dependent polyadenylation is regulated by Aurora A and glycogen synthase kinase-3. Genes Dev 18:48-61. http://dx.doi.org /10.1101/gad.1136004.
27. Gratacós FM, Brewer G. 2010. The role of AUF1 in regulated mRNA decay. Wiley Interdiscip Rev RNA 1:457-473. http://dx.doi.org/10.1002 /wrna.26.
28. Schott J, Stoecklin G. 2010. Networks controlling mRNA decay in the immune system. Wiley Interdiscip Rev RNA 1:432-456. http://dx.doi.org /10.1002/wrna.13.
29. Kaplan EL, Meier P. 1958. Nonparametric estimation from incomplete observations. J Am Stat Assoc 53:457-481. http://dx.doi.org/10.1080 /01621459.1958.10501452.
30. Nagaoka K, Udagawa T, Richter JD. 2012. CPEB-mediated ZO-1 mRNA localization is required for epithelial tight-junction assembly and cell polarity. Nat Commun 3:675. http://dx.doi.org/10.1038/ncomms1678.
31. Pahl HL. 1999. Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene 18:6853-6866. http://dx.doi.org/10.1038/sj.onc .1203239.
32. Skaug B, Jiang X, Chen ZJ. 2009. The role of ubiquitin in NF-kappaB regulatory pathways. Annu Rev Biochem 78:769-796. http://dx.doi.org /10.1146/annurev.biochem.78.070907.102750.
33. Ninomiya-Tsuji J, Kishimoto K, Hiyama A, Inoue J, Cao Z, Matsumoto K. 1999. The kinase TAK1 can activate the NIK-IκB as well as the MAP kinase cascade in the IL-1 signalling pathway. Nature 398:252-256. http: //dx.doi.org/10.1038/18465.
34. Hake LE, Mendez R, Richter JD. 1998. Specificity of RNA binding by CPEB: requirement for RNA recognition motifs and a novel zinc finger. Mol Cell Biol 18:685-693.
35. Ninomiya-Tsuji J, Kajino T, Ono K, Ohtomo T, Matsumoto M, Shiina M, Mihara M, Tsuchiya M, Matsumoto K. 2003. A resorcylic acid lactone, 5Z-7-oxozeaenol, prevents inflammation by inhibiting the catalytic activity of TAK1MAPKkinase kinase. J Biol Chem 278:18485-18490. http://dx.doi.org/10.1074/jbc.M207453200.
36. Zhang D, Hu Y, Sun Q, Zhao J, Cong Z, Liu H, Zhou M, Li K, Hang C. 2013. Inhibition of transforming growth factor beta-activated kinase 1 confers neuroprotection after traumatic brain injury in rats. Neuroscience 238:209-217. http://dx.doi.org/10.1016/j.neuroscience.2013.02.022.
37. Anderson P. 2008. Post-transcriptional control of cytokine production. Nat Immunol 9:353-359. http://dx.doi.org/10.1038/ni1584.
38. Anderson P. 2009. Intrinsic mRNA stability helps compose the inflammatory symphony. Nat Immunol 10:233-234. http://dx.doi.org/10.1038 /ni0309-233.
39. Yao P, Potdar AA, Arif A, Ray PS, Mukhopadhyay R, Willard B, Xu Y, Yan J, Saidel GM, Fox PL. 2012. Coding region polyadenylation generates a truncated tRNA synthetase that counters translation repression. Cell 149:88-100. http://dx.doi.org/10.1016/j.cell.2012.02.018.
40. Lu JY, Sadri N, Schneider RJ. 2006. Endotoxic shock in AUF1 knockout mice mediated by failure to degrade proinflammatory cytokine mRNAs. Genes Dev 20:3174-3184. http://dx.doi.org/10.1101/gad.1467606.
41. Sadri N, Schneider RJ. 2009. AUF1/HNRNPD-deficient mice develop pruritic inflammatory skin disease. J Investig Dermatol 29:557-570. http: //dx.doi.org/10.1038/jid.2008.298.
42. Sarkar S, Han J, Sinsimer KS, Liao B, Foster RL, Brewer G, Pestka S. 2011. RNA-binding protein AUF1 regulates lipopolysaccharide-induced IL10 expression by activating IkappaB kinase complex in monocytes. Mol Cell Biol 31:602-615. http://dx.doi.org/10.1128/MCB.00835-10.
43. Liepelt A, Mossanen JC, Denecke B, Heymann F, De Santis R, Tacke F, Marx G, Ostareck DH, Ostareck-Lederer A. 2014. Translation control of TAK1 mRNA by hnRNP K modulates LPS-induced macrophage activation. RNA 20:899-911. http://dx.doi.org/10.1261/rna.042788.113.
44. Phillips K, Kedersha N, Shen L, Blackshear PJ, Anderson P. 2004. Arthritis suppressor genes YIA-1 and TTP dampen the expression of tumor necrosis factor alpha, cyclooxygenase 2, and inflammatory arthritis. Proc Natl Acad Sci U S A 101:2011-2016. http://dx.doi.org/10.1073/pnas .0400148101.