#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

IL-17 Attenuates Degradation of ARE-mRNAs by Changing the Cooperation between AU-Binding Proteins and microRNA16


Interleukin 17A (IL-17), a mediator implicated in chronic and severe inflammatory diseases, enhances the production of pro-inflammatory mediators by attenuating decay of the encoding mRNAs. The decay of many of these mRNAs depends on proteins (AUBps) that target AU-rich elements in the 3′-untranslated region of mRNAs and facilitate either mRNA decay or stabilization. Here we show that AUBps and the target mRNA assemble in a novel ribonucleoprotein complex in the presence of microRNA16 (miR16), which leads to the degradation of the target mRNA. Notably, IL-17 attenuates miR16 expression and promotes the binding of stabilizing AUBps over that of destabilizing AUBps, reducing mRNA decay. These findings indicate that miR16 independently of a seed sequence, directs the competition between degrading and stabilizing AUBps for target mRNAs. Since AUBps affect expression of about 8% of the human transcriptome and miR16 is ubiquitously expressed, IL-17 may in addition to inflammation affect many other cellular processes.


Vyšlo v časopise: IL-17 Attenuates Degradation of ARE-mRNAs by Changing the Cooperation between AU-Binding Proteins and microRNA16. PLoS Genet 9(9): e32767. doi:10.1371/journal.pgen.1003747
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003747

Souhrn

Interleukin 17A (IL-17), a mediator implicated in chronic and severe inflammatory diseases, enhances the production of pro-inflammatory mediators by attenuating decay of the encoding mRNAs. The decay of many of these mRNAs depends on proteins (AUBps) that target AU-rich elements in the 3′-untranslated region of mRNAs and facilitate either mRNA decay or stabilization. Here we show that AUBps and the target mRNA assemble in a novel ribonucleoprotein complex in the presence of microRNA16 (miR16), which leads to the degradation of the target mRNA. Notably, IL-17 attenuates miR16 expression and promotes the binding of stabilizing AUBps over that of destabilizing AUBps, reducing mRNA decay. These findings indicate that miR16 independently of a seed sequence, directs the competition between degrading and stabilizing AUBps for target mRNAs. Since AUBps affect expression of about 8% of the human transcriptome and miR16 is ubiquitously expressed, IL-17 may in addition to inflammation affect many other cellular processes.


Zdroje

1. RouvierE, LucianiMF, MattéiMG, DenizotF, GolsteinP (1993) CTLA-8, cloned from an activated T cell, bearing AU-rich messenger RNA instability sequences, and homologous to a herpesvirus saimiri gene. J Immunol 150: 5445–5456.

2. IwakuraY, IshigameH, SaijoS, NakaeS (2011) Functional specialization of interleukin-17 family members. Immunity 34: 149–162 doi:10.1016/j.immuni.2011.02.012

3. IshigameH, KakutaS, NagaiT, KadokiM, NambuA, et al. (2009) Differential roles of interleukin-17A and -17F in host defense against mucoepithelial bacterial infection and allergic responses. Immunity 30: 108–119 doi:10.1016/j.immuni.2008.11.009

4. WrightJF, BennettF, LiB, BrooksJ, LuxenbergDP, et al. (2008) The human IL-17F/IL-17A heterodimeric cytokine signals through the IL-17RA/IL-17RC receptor complex. J Immunol 181: 2799–2805.

5. ShenF, HuZ, GoswamiJ, GaffenSL (2006) Identification of common transcriptional regulatory elements in interleukin-17 target genes. J Biol Chem 281: 24138–24148 doi:10.1074/jbc.M604597200

6. ShenF, RuddyMJ, PlamondonP, GaffenSL (2005) Cytokines link osteoblasts and inflammation: microarray analysis of interleukin-17- and TNF-alpha-induced genes in bone cells. J Leukoc Biol 77: 388–399 doi:10.1189/jlb.0904490

7. HartupeeJ, LiuC, NovotnyM, SunD, LiX, et al. (2009) IL-17 signaling for mRNA stabilization does not require TNF receptor-associated factor 6. J Immunol 182: 1660–1666.

8. BulekK, LiuC, SwaidaniS, WangL, PageRC, et al. (2011) The inducible kinase IKKi is required for IL-17-dependent signaling associated with neutrophilia and pulmonary inflammation. Nat Immunol 12: 844–852 doi:10.1038/ni.2080

9. van den BergA, KuiperM, SnoekM, TimensW, PostmaDS, et al. (2005) Interleukin-17 induces hyperresponsive interleukin-8 and interleukin-6 production to tumor necrosis factor-alpha in structural lung cells. Am J Respir Cell Mol Biol 33: 97–104 doi:10.1165/rcmb.2005-0022OC

10. ShawG, KamenR (1986) A conserved AU sequence from the 3′ untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell 46: 659–667.

11. BakheetT, WilliamsBRG, KhabarKSA (2006) ARED 3.0: the large and diverse AU-rich transcriptome. Nucleic Acids Res 34: D111–114 doi:10.1093/nar/gkj052

12. LaiWS, CarballoE, StrumJR, KenningtonEA, PhillipsRS, et al. (1999) Evidence that tristetraprolin binds to AU-rich elements and promotes the deadenylation and destabilization of tumor necrosis factor alpha mRNA. Mol Cell Biol 19: 4311–4323.

13. KiledjianM, DeMariaCT, BrewerG, NovickK (1997) Identification of AUF1 (heterogeneous nuclear ribonucleoprotein D) as a component of the alpha-globin mRNA stability complex. Mol Cell Biol 17: 4870–4876.

14. FanXC, SteitzJA (1998) Overexpression of HuR, a nuclear-cytoplasmic shuttling protein, increases the in vivo stability of ARE-containing mRNAs. EMBO J 17: 3448–3460 doi:10.1093/emboj/17.12.3448

15. PengSS, ChenCY, XuN, ShyuAB (1998) RNA stabilization by the AU-rich element binding protein, HuR, an ELAV protein. EMBO J 17: 3461–3470 doi:10.1093/emboj/17.12.3461

16. GherziR, LeeK-Y, BriataP, WegmüllerD, MoroniC, et al. (2004) A KH domain RNA binding protein, KSRP, promotes ARE-directed mRNA turnover by recruiting the degradation machinery. Mol Cell 14: 571–583 doi:10.1016/j.molcel.2004.05.002

17. DixonDA, BalchGC, KedershaN, AndersonP, ZimmermanGA, et al. (2003) Regulation of cyclooxygenase-2 expression by the translational silencer TIA-1. J Exp Med 198: 475–481 doi:10.1084/jem.20030616

18. GueydanC, DroogmansL, ChalonP, HuezG, CaputD, et al. (1999) Identification of TIAR as a protein binding to the translational regulatory AU-rich element of tumor necrosis factor alpha mRNA. J Biol Chem 274: 2322–2326.

19. LinkerK, PautzA, FechirM, HubrichT, GreeveJ, et al. (2005) Involvement of KSRP in the post-transcriptional regulation of human iNOS expression-complex interplay of KSRP with TTP and HuR. Nucleic Acids Res 33: 4813–4827 doi:10.1093/nar/gki797

20. FabianMR, SonenbergN, FilipowiczW (2010) Regulation of mRNA translation and stability by microRNAs. Annu Rev Biochem 79: 351–379 doi:10.1146/annurev-biochem-060308-103103

21. van den BergA, MolsJ, HanJ (2008) RISC-target interaction: cleavage and translational suppression. Biochim Biophys Acta 1779: 668–677 doi:10.1016/j.bbagrm.2008.07.005

22. SuswamE, LiY, ZhangX, GillespieGY, LiX, et al. (2008) Tristetraprolin down-regulates interleukin-8 and vascular endothelial growth factor in malignant glioma cells. Cancer Res 68: 674–682 doi:10.1158/0008-5472.CAN-07-2751

23. BalakathiresanNS, BhattacharyyaS, GuttiU, LongRP, JozwikC, et al. (2009) Tristetraprolin regulates IL-8 mRNA stability in cystic fibrosis lung epithelial cells. Am J Physiol Lung Cell Mol Physiol 296: L1012–1018 doi:10.1152/ajplung.90601.2008

24. ShiJ-X, SuX, XuJ, ZhangW-Y, ShiY (2012) MK2 posttranscriptionally regulates TNF-α-induced expression of ICAM-1 and IL-8 via tristetraprolin in human pulmonary microvascular endothelial cells. Am J Physiol Lung Cell Mol Physiol 302: L793–799 doi:10.1152/ajplung.00339.2011

25. PalanisamyV, ParkNJ, WangJ, WongDT (2008) AUF1 and HuR proteins stabilize interleukin-8 mRNA in human saliva. J Dent Res 87: 772–776.

26. SuswamEA, NaborsLB, HuangY, YangX, KingPH (2005) IL-1beta 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 doi:10.1002/ijc.20675

27. WinzenR, ThakurBK, Dittrich-BreiholzO, ShahM, RedichN, et al. (2007) Functional analysis of KSRP interaction with the AU-rich element of interleukin-8 and identification of inflammatory mRNA targets. Mol Cell Biol 27: 8388–8400 doi:10.1128/MCB.01493-07

28. MukaidaN, ShirooM, MatsushimaK (1989) Genomic structure of the human monocyte-derived neutrophil chemotactic factor IL-8. J Immunol 143: 1366–1371.

29. YuY, ChadeeK (2001) The 3′-untranslated region of human interleukin-8 mRNA suppresses IL-8 gene expression. Immunology 102: 498–505.

30. JingQ, HuangS, GuthS, ZarubinT, MotoyamaA, et al. (2005) Involvement of microRNA in AU-rich element-mediated mRNA instability. Cell 120: 623–634 doi:10.1016/j.cell.2004.12.038

31. LajoieS, LewkowichIP, SuzukiY, ClarkJR, SprolesAA, et al. (2010) Complement-mediated regulation of the IL-17A axis is a central genetic determinant of the severity of experimental allergic asthma. Nat Immunol 11: 928–935 doi:10.1038/ni.1926

32. HartupeeJ, LiuC, NovotnyM, LiX, HamiltonT (2007) IL-17 enhances chemokine gene expression through mRNA stabilization. J Immunol 179: 4135–4141.

33. van WissenM, SnoekM, SmidsB, JansenHM, LutterR (2002) IFN-gamma amplifies IL-6 and IL-8 responses by airway epithelial-like cells via indoleamine 2,3-dioxygenase. J Immunol 169: 7039–7044.

34. LutterR, LomanS, SnoekM, RogerT, OutTA, et al. (2000) IL-6 protein production by airway epithelial(-like) cells disabled in IL-6 mRNA degradation. Cytokine 12: 1275–1279 doi:10.1006/cyto.1999.0728

35. DattaS, NovotnyM, PavicicPGJr, ZhaoC, HerjanT, et al. (2010) IL-17 regulates CXCL1 mRNA stability via an AUUUA/tristetraprolin-independent sequence. J Immunol 184: 1484–1491 doi:10.4049/jimmunol.0902423

36. SunD, NovotnyM, BulekK, LiuC, LiX, et al. (2011) Treatment with IL-17 prolongs the half-life of chemokine CXCL1 mRNA via the adaptor TRAF5 and the splicing-regulatory factor SF2 (ASF). Nat Immunol 12: 853–860 doi:10.1038/ni.2081

37. SpasicM, FriedelCC, SchottJ, KrethJ, LeppekK, et al. (2012) Genome-wide assessment of AU-rich elements by the AREScore algorithm. PLoS Genet 8: e1002433 doi:10.1371/journal.pgen.1002433

38. ChiSW, HannonGJ, DarnellRB (2012) An alternative mode of microRNA target recognition. Nat Struct Mol Biol 19: 321–327 doi:10.1038/nsmb.2230

39. LiaoW-L, WangW-C, ChangW-C, TsengJT (2011) The RNA-binding protein HuR stabilizes cytosolic phospholipase A2α mRNA under interleukin-1β treatment in non-small cell lung cancer A549 Cells. J Biol Chem 286: 35499–35508 doi:10.1074/jbc.M111.263582

40. RogerT, OutT, MukaidaN, MatsushimaK, JansenH, et al. (1998) Enhanced AP-1 and NF-kappaB activities and stability of interleukin 8 (IL-8) transcripts are implicated in IL-8 mRNA superinduction in lung epithelial H292 cells. Biochem J 330 (Pt 1) 429–435.

41. ChenC, RidzonDA, BroomerAJ, ZhouZ, LeeDH, et al. (2005) Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res 33: e179 doi:10.1093/nar/gni178

42. SchreiberE, MatthiasP, MüllerMM, SchaffnerW (1989) Rapid detection of octamer binding proteins with “mini-extracts”, prepared from a small number of cells. Nucleic Acids Res 17: 6419.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2013 Číslo 9
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#