Interleukin-1α associates with the tumor suppressor p53 following DNA damage

. 2020 Apr 24 ; 10 (1) : 6995. [epub] 20200424

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid32332775
Odkazy

PubMed 32332775
PubMed Central PMC7181607
DOI 10.1038/s41598-020-63779-x
PII: 10.1038/s41598-020-63779-x
Knihovny.cz E-zdroje

Interleukin-1α (IL-1α) is a dual-function proinflammatory mediator. In addition to its role in the canonical IL-1 signaling pathway, which employs membrane-bound receptors, a growing body of evidence shows that IL-1α has some additional intracellular functions. We identified the interaction of IL-1α with the tumor suppressor p53 in the nuclei and cytoplasm of both malignant and noncancerous mammalian cell lines using immunoprecipitation and the in situ proximity ligation assay (PLA). This interaction was enhanced by treatment with the antineoplastic drug etoposide, which suggests a role for the IL-1α•p53 interaction in genotoxic stress.

Zobrazit více v PubMed

Marchenko ND, et al. Stress-mediated nuclear stabilization of p53 is regulated by ubiquitination and importin-alpha3 binding. Cell death and differentiation. 2010;17:255–267. doi: 10.1038/cdd.2009.173. PubMed DOI PMC

Fritsche M, Haessler C, Brandner G. Induction of nuclear accumulation of the tumor-suppressor protein p53 by DNA-damaging agents. Oncogene. 1993;8:307–318. PubMed

Yonish-Rouach E, et al. Wild-type p53 induces apoptosis of myeloid leukaemic cells that is inhibited by interleukin-6. Nature. 1991;352:345–347. doi: 10.1038/352345a0. PubMed DOI

Livingstone LR, et al. Altered cell cycle arrest and gene amplification potential accompany loss of wild-type p53. Cell. 1992;70:923–935. doi: 10.1016/0092-8674(92)90243-6. PubMed DOI

Smith ML, Chen IT, Zhan Q, O’Connor PM, Fornace AJ., Jr. Involvement of the p53 tumor suppressor in repair of u.v.-type DNA damage. Oncogene. 1995;10:1053–1059. PubMed

Matoba S, et al. p53 regulates mitochondrial respiration. Science. 2006;312:1650–1653. doi: 10.1126/science.1126863. PubMed DOI

Haupt Y, Maya R, Kazaz A, Oren M. Mdm2 promotes the rapid degradation of p53. Nature. 1997;387:296–299. doi: 10.1038/387296a0. PubMed DOI

Kubbutat MH, Jones SN, Vousden KH. Regulation of p53 stability by Mdm2. Nature. 1997;387:299–303. doi: 10.1038/387299a0. PubMed DOI

Grandela C, Pera MF, Grimmond SM, Kolle G, Wolvetang EJ. p53 is required for etoposide-induced apoptosis of human embryonic stem cells. Stem Cell Res. 2007;1:116–128. doi: 10.1016/j.scr.2007.10.003. PubMed DOI

Nelson WG, Kastan MB. DNA strand breaks: the DNA template alterations that trigger p53-dependent DNA damage response pathways. Molecular and cellular biology. 1994;14:1815–1823. doi: 10.1128/MCB.14.3.1815. PubMed DOI PMC

Arriola EL, Lopez AR, Chresta CM. Differential regulation of p21waf-1/cip-1 and Mdm2 by etoposide: etoposide inhibits the p53-Mdm2 autoregulatory feedback loop. Oncogene. 1999;18:1081–1091. doi: 10.1038/sj.onc.1202391. PubMed DOI

Solyakov L, Sayan E, Riley J, Pointon A, Tobin AB. Regulation of p53 expression, phosphorylation and subcellular localization by a G-protein-coupled receptor. Oncogene. 2009;28:3619–3630. doi: 10.1038/onc.2009.225. PubMed DOI PMC

Karpinich NO, Tafani M, Rothman RJ, Russo MA, Farber JL. The course of etoposide-induced apoptosis from damage to DNA and p53 activation to mitochondrial release of cytochrome c. The Journal of biological chemistry. 2002;277:16547–16552. doi: 10.1074/jbc.M110629200. PubMed DOI

Wessendorf JH, Garfinkel S, Zhan X, Brown S, Maciag T. Identification of a nuclear localization sequence within the structure of the human interleukin-1 alpha precursor. The Journal of biological chemistry. 1993;268:22100–22104. PubMed

Rivers-Auty J, Daniels MJD, Colliver I, Robertson DL, Brough D. Redefining the ancestral origins of the interleukin-1 superfamily. Nature communications. 2018;9:1156. doi: 10.1038/s41467-018-03362-1. PubMed DOI PMC

Hu B, et al. A nuclear target for interleukin-1alpha: interaction with the growth suppressor necdin modulates proliferation and collagen expression. Proc Natl Acad Sci USA. 2003;100:10008–10013. doi: 10.1073/pnas.1737765100. PubMed DOI PMC

Pollock AS, Turck J, Lovett DH. The prodomain of interleukin 1alpha interacts with elements of the RNA processing apparatus and induces apoptosis in malignant cells. FASEB journal: official publication of the Federation of American Societies for Experimental Biology. 2003;17:203–213. doi: 10.1096/fj.02-0602com. PubMed DOI

Buryskova M, Pospisek M, Grothey A, Simmet T, Burysek L. Intracellular interleukin-1alpha functionally interacts with histone acetyltransferase complexes. The Journal of biological chemistry. 2004;279:4017–4026. doi: 10.1074/jbc.M306342200. PubMed DOI

Zamostna B, et al. N-terminal domain of nuclear IL-1alpha shows structural similarity to the C-terminal domain of Snf1 and binds to the HAT/core module of the SAGA complex. PloS one. 2012;7:e41801. doi: 10.1371/journal.pone.0041801. PubMed DOI PMC

McCarthy DA, Clark RR, Bartling TR, Trebak M, Melendez JA. Redox control of the senescence regulator interleukin-1alpha and the secretory phenotype. The Journal of biological chemistry. 2013;288:32149–32159. doi: 10.1074/jbc.M113.493841. PubMed DOI PMC

Cohen I, et al. Differential release of chromatin-bound IL-1alpha discriminates between necrotic and apoptotic cell death by the ability to induce sterile inflammation. Proceedings of the National Academy of Sciences of the United States of America. 2010;107:2574–2579. doi: 10.1073/pnas.0915018107. PubMed DOI PMC

Werman A, et al. The precursor form of IL-1alpha is an intracrine proinflammatory activator of transcription. Proc Natl Acad Sci USA. 2004;101:2434–2439. doi: 10.1073/pnas.0308705101. PubMed DOI PMC

Cheng W, et al. Intracellular interleukin-1alpha mediates interleukin-8 production induced by Chlamydia trachomatis infection via a mechanism independent of type I interleukin-1 receptor. Infect Immun. 2008;76:942–951. doi: 10.1128/IAI.01313-07. PubMed DOI PMC

Zhang Y, et al. Propiece IL-1alpha facilitates the growth of acute T-lymphocytic leukemia cells through the activation of NF-kappaB and SP1. Oncotarget. 2017;8:15677–15688. doi: 10.18632/oncotarget.14934. PubMed DOI PMC

Bendtzen K, et al. Cytotoxicity of human pI 7 interleukin-1 for pancreatic islets of Langerhans. Science. 1986;232:1545–1547. doi: 10.1126/science.3086977. PubMed DOI

Kawaguchi Y. IL-1 alpha gene expression and protein production by fibroblasts from patients with systemic sclerosis. Clin Exp Immunol. 1994;97:445–450. doi: 10.1111/j.1365-2249.1994.tb06108.x. PubMed DOI PMC

Nicoll JA, et al. Association of interleukin-1 gene polymorphisms with Alzheimer’s disease. Ann Neurol. 2000;47:365–368. doi: 10.1002/1531-8249(200003)47:3<365::AID-ANA13>3.0.CO;2-G. PubMed DOI PMC

Rainero I, et al. Association between the interleukin-1alpha gene and Alzheimer’s disease: a meta-analysis. Neurobiol Aging. 2004;25:1293–1298. doi: 10.1016/j.neurobiolaging.2004.02.011. PubMed DOI

Sutton C, Brereton C, Keogh B, Mills KH, Lavelle EC. A crucial role for interleukin (IL)-1 in the induction of IL-17-producing T cells that mediate autoimmune encephalomyelitis. J Exp Med. 2006;203:1685–1691. doi: 10.1084/jem.20060285. PubMed DOI PMC

Vicenova B, Vopalensky V, Burysek L, Pospisek M. Emerging role of interleukin-1 in cardiovascular diseases. Physiol Res. 2009;58:481–498. PubMed

Mandrup-Poulsen T, Pickersgill L, Donath MY. Blockade of interleukin 1 in type 1 diabetes mellitus. Nat Rev Endocrinol. 2010;6:158–166. doi: 10.1038/nrendo.2009.271. PubMed DOI

Bou-Dargham MJ, Khamis ZI, Cognetta AB, Sang QA. The Role of Interleukin-1 in Inflammatory and Malignant Human Skin Diseases and the Rationale for Targeting Interleukin-1 Alpha. Medicinal research reviews. 2017;37:180–216. doi: 10.1002/med.21406. PubMed DOI

Cohen I, et al. IL-1alpha is a DNA damage sensor linking genotoxic stress signaling to sterile inflammation and innate immunity. Scientific reports. 2015;5:14756. doi: 10.1038/srep14756. PubMed DOI PMC

Armstrong CA, et al. Heterogeneity of cytokine production by human malignant melanoma cells. Exp Dermatol. 1992;1:37–45. doi: 10.1111/j.1600-0625.1992.tb00070.x. PubMed DOI

Mayo LD, et al. Phosphorylation of human p53 at serine 46 determines promoter selection and whether apoptosis is attenuated or amplified. The Journal of biological chemistry. 2005;280:25953–25959. doi: 10.1074/jbc.M503026200. PubMed DOI

Smeenk L, et al. Role of p53 serine 46 in p53 target gene regulation. PloS one. 2011;6:e17574. doi: 10.1371/journal.pone.0017574. PubMed DOI PMC

Montecucco, A., Zanetta, F. & Biamonti, G. Molecular mechanisms of etoposide. EXCLI J14, 95–108, 10.17179/excli2015-561 2014-561 [pii]Doc95 [pii] (2015). PubMed PMC

Nakai S, Mizuno K, Kaneta M, Hirai Y. A simple, sensitive bioassay for the detection of interleukin-1 using human melanoma A375 cell line. Biochemical and biophysical research communications. 1988;154:1189–1196. doi: 10.1016/0006-291X(88)90266-5. PubMed DOI

Soderberg O, et al. Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nature methods. 2006;3:995–1000. doi: 10.1038/nmeth947. PubMed DOI

Nahalkova J. Novel protein-protein interactions of TPPII, p53, and SIRT7. Molecular and cellular biochemistry. 2015;409:13–22. doi: 10.1007/s11010-015-2507-y. PubMed DOI

Kang MA, et al. A novel pyrido-thieno-pyrimidine derivative activates p53 through induction of phosphorylation and acetylation in colorectal cancer cells. International journal of oncology. 2015;46:342–350. doi: 10.3892/ijo.2014.2720. PubMed DOI

Tembe V, et al. The BARD1 BRCT domain contributes to p53 binding, cytoplasmic and mitochondrial localization, and apoptotic function. Cellular signalling. 2015;27:1763–1771. doi: 10.1016/j.cellsig.2015.05.011. PubMed DOI

Ivanschitz L, et al. PML IV/ARF interaction enhances p53 SUMO-1 conjugation, activation, and senescence. Proceedings of the National Academy of Sciences of the United States of America. 2015;112:14278–14283. doi: 10.1073/pnas.1507540112. PubMed DOI PMC

Pruszko M, et al. The mutant p53-ID4 complex controls VEGFA isoforms by recruiting lncRNA MALAT1. EMBO reports. 2017;18:1331–1351. doi: 10.15252/embr.201643370. PubMed DOI PMC

Chan C, et al. Global re-wiring of p53 transcription regulation by the hepatitis B virus X protein. Molecular oncology. 2016;10:1183–1195. doi: 10.1016/j.molonc.2016.05.006. PubMed DOI PMC

Burzynski LC, Humphry M, Bennett MR, Clarke MC. Interleukin-1alpha Activity in Necrotic Endothelial Cells Is Controlled by Caspase-1 Cleavage of Interleukin-1 Receptor-2: IMPLICATIONS FOR ALLOGRAFT REJECTION. The Journal of biological chemistry. 2015;290:25188–25196. doi: 10.1074/jbc.M115.667915. PubMed DOI PMC

Adey A, et al. The haplotype-resolved genome and epigenome of the aneuploid HeLa cancer cell line. Nature. 2013;500:207–211. doi: 10.1038/nature12064. PubMed DOI PMC

Trave G, Zanier K. HPV-mediated inactivation of tumor suppressor p53. Cell Cycle. 2016;15:2231–2232. doi: 10.1080/15384101.2016.1191257. PubMed DOI PMC

Scheffner M, Werness BA, Huibregtse JM, Levine AJ, Howley PM. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell. 1990;63:1129–1136. doi: 10.1016/0092-8674(90)90409-8. PubMed DOI

Ajay AK, Meena AS, Bhat MK. Human papillomavirus 18 E6 inhibits phosphorylation of p53 expressed in HeLa cells. Cell Biosci. 2012;2:2. doi: 10.1186/2045-3701-2-2. PubMed DOI PMC

Thomas MC, Chiang CM. E6 oncoprotein represses p53-dependent gene activation via inhibition of protein acetylation independently of inducing p53 degradation. Molecular cell. 2005;17:251–264. doi: 10.1016/j.molcel.2004.12.016. PubMed DOI

McCarthy DA, et al. Redox-control of the alarmin, Interleukin-1alpha. Redox biology. 2013;1:218–225. doi: 10.1016/j.redox.2013.03.001. PubMed DOI PMC

Teufel DP, Freund SM, Bycroft M, Fersht AR. Four domains of p300 each bind tightly to a sequence spanning both transactivation subdomains of p53. Proc Natl Acad Sci USA. 2007;104:7009–7014. doi: 10.1073/pnas.0702010104. PubMed DOI PMC

Gamper AM, Roeder RG. Multivalent binding of p53 to the STAGA complex mediates coactivator recruitment after UV damage. Molecular and cellular biology. 2008;28:2517–2527. doi: 10.1128/MCB.01461-07. PubMed DOI PMC

Reed SM, Quelle DE. p53 Acetylation: Regulation and Consequences. Cancers. 2014;7:30–69. doi: 10.3390/cancers7010030. PubMed DOI PMC

Zhang J, Shen L, Sun LQ. The regulation of radiosensitivity by p53 and its acetylation. Cancer letters. 2015;363:108–118. doi: 10.1016/j.canlet.2015.04.015. PubMed DOI

Liu L, et al. p53 sites acetylated in vitro by PCAF and p300 are acetylated in vivo in response to DNA damage. Molecular and cellular biology. 1999;19:1202–1209. doi: 10.1128/MCB.19.2.1202. PubMed DOI PMC

Sakaguchi K, et al. DNA damage activates p53 through a phosphorylation-acetylation cascade. Genes & development. 1998;12:2831–2841. doi: 10.1101/gad.12.18.2831. PubMed DOI PMC

Kawaguchi Y, Ito A, Appella E, Yao TP. Charge modification at multiple C-terminal lysine residues regulates p53 oligomerization and its nucleus-cytoplasm trafficking. The Journal of biological chemistry. 2006;281:1394–1400. doi: 10.1074/jbc.M505772200. PubMed DOI

Knights CD, et al. Distinct p53 acetylation cassettes differentially influence gene-expression patterns and cell fate. The Journal of cell biology. 2006;173:533–544. doi: 10.1083/jcb.200512059. PubMed DOI PMC

Sadoul K, Wang J, Diagouraga B, Khochbin S. The tale of protein lysine acetylation in the cytoplasm. Journal of biomedicine & biotechnology. 2011;2011:970382. doi: 10.1155/2011/970382. PubMed DOI PMC

Martinez E, et al. Human STAGA complex is a chromatin-acetylating transcription coactivator that interacts with pre-mRNA splicing and DNA damage-binding factors in vivo. Molecular and cellular biology. 2001;21:6782–6795. doi: 10.1128/MCB.21.20.6782-6795.2001. PubMed DOI PMC

Lee HS, Park JH, Kim SJ, Kwon SJ, Kwon J. A cooperative activation loop among SWI/SNF, gamma-H2AX and H3 acetylation for DNA double-strand break repair. The EMBO journal. 2010;29:1434–1445. doi: 10.1038/emboj.2010.27. PubMed DOI PMC

Bennett G, Peterson CL. SWI/SNF recruitment to a DNA double-strand break by the NuA4 and Gcn5 histone acetyltransferases. DNA repair. 2015;30:38–45. doi: 10.1016/j.dnarep.2015.03.006. PubMed DOI PMC

Ramachandran S, et al. The SAGA Deubiquitination Module Promotes DNA Repair and Class Switch Recombination through ATM and DNAPK-Mediated gammaH2AX Formation. Cell reports. 2016;15:1554–1565. doi: 10.1016/j.celrep.2016.04.041. PubMed DOI PMC

Ogiwara H, et al. Histone acetylation by CBP and p300 at double-strand break sites facilitates SWI/SNF chromatin remodeling and the recruitment of non-homologous end joining factors. Oncogene. 2011;30:2135–2146. doi: 10.1038/onc.2010.592. PubMed DOI

Wilson, M. D. & Durocher, D. Reading chromatin signatures after DNA double-strand breaks. Philosophical transactions of the Royal Society of London. Series B, Biological sciences 372, 10.1098/rstb.2016.0280 (2017). PubMed PMC

Muslimovic A, Nystrom S, Gao Y, Hammarsten O. Numerical analysis of etoposide induced DNA breaks. PloS one. 2009;4:e5859. doi: 10.1371/journal.pone.0005859. PubMed DOI PMC

Rybak P, et al. Low level phosphorylation of histone H2AX on serine 139 (gammaH2AX) is not associated with DNA double-strand breaks. Oncotarget. 2016;7:49574–49587. doi: 10.18632/oncotarget.10411. PubMed DOI PMC

Al Rashid ST, et al. Evidence for the direct binding of phosphorylated p53 to sites of DNA breaks in vivo. Cancer research. 2005;65:10810–10821. doi: 10.1158/0008-5472.CAN-05-0729. PubMed DOI

Frydryskova, K., Masek, T. & Pospisek, M. Changing faces of stress: Impact of heat and arsenite treatment on the composition of stress granules. WIREs RNA,10.1002/wrna.1596 (2020). PubMed

Shin HJ, Kwon HK, Lee JH, Anwar MA, Choi S. Etoposide induced cytotoxicity mediated by ROS and ERK in human kidney proximal tubule cells. Scientific reports. 2016;6:34064. doi: 10.1038/srep34064. PubMed DOI PMC

Chamani E, Rabbani-Chadegani A, Zahraei Z. Spectroscopic detection of etoposide binding to chromatin components: the role of histone proteins. Spectrochimica acta. Part A, Molecular and biomolecular spectroscopy. 2014;133:292–299. doi: 10.1016/j.saa.2014.05.068. PubMed DOI

Gudkov AV, Gurova KV, Komarova EA. Inflammation and p53: A Tale of Two Stresses. Genes & cancer. 2011;2:503–516. doi: 10.1177/1947601911409747. PubMed DOI PMC

Uehara, I. & Tanaka, N. Role of p53 in the Regulation of the Inflammatory Tumor Microenvironment and Tumor Suppression. Cancers10, 10.3390/cancers10070219 (2018). PubMed PMC

Webster GA, Perkins ND. Transcriptional cross talk between NF-kappaB and p53. Molecular and cellular biology. 1999;19:3485–3495. doi: 10.1128/mcb.19.5.3485. PubMed DOI PMC

Wadgaonkar R, et al. CREB-binding protein is a nuclear integrator of nuclear factor-kappaB and p53 signaling. The Journal of biological chemistry. 1999;274:1879–1882. doi: 10.1074/jbc.274.4.1879. PubMed DOI

Mantovani A, Barajon I, Garlanda C. IL-1 and IL-1 regulatory pathways in cancer progression and therapy. Immunological reviews. 2018;281:57–61. doi: 10.1111/imr.12614. PubMed DOI PMC

Stevenson FT, Turck J, Locksley RM, Lovett DH. The N-terminal propiece of interleukin 1 alpha is a transforming nuclear oncoprotein. Proceedings of the National Academy of Sciences of the United States of America. 1997;94:508–513. doi: 10.1073/pnas.94.2.508. PubMed DOI PMC

Wolf JS, et al. IL (interleukin)-1alpha promotes nuclear factor-kappaB and AP-1-induced IL-8 expression, cell survival, and proliferation in head and neck squamous cell carcinomas. Clinical cancer research: an official journal of the American Association for Cancer Research. 2001;7:1812–1820. PubMed

Palmer G, et al. Pre-interleukin-1alpha expression reduces cell growth and increases interleukin-6 production in SaOS-2 osteosarcoma cells: Differential inhibitory effect of interleukin-1 receptor antagonist (icIL-1Ra1) Cytokine. 2005;31:153–160. doi: 10.1016/j.cyto.2005.03.007. PubMed DOI

Xie L, et al. A synthetic interaction screen identifies factors selectively required for proliferation and TERT transcription in p53-deficient human cancer cells. PLoS genetics. 2012;8:e1003151. doi: 10.1371/journal.pgen.1003151. PubMed DOI PMC

Schindelin J, et al. Fiji: an open-source platform for biological-image analysis. Nature methods. 2012;9:676–682. doi: 10.1038/nmeth.2019. PubMed DOI PMC

Rueden CT, et al. ImageJ2: ImageJ for the next generation of scientific image data. BMC bioinformatics. 2017;18:529. doi: 10.1186/s12859-017-1934-z. PubMed DOI PMC

Stommel JM, et al. A leucine-rich nuclear export signal in the p53 tetramerization domain: regulation of subcellular localization and p53 activity by NES masking. The EMBO journal. 1999;18:1660–1672. doi: 10.1093/emboj/18.6.1660. PubMed DOI PMC

Zamostna, B. Elucidating the interactions of interleukin-1α with components of the eukaryotic transcription machinery. Ph.D. thesis, Charles University (2013).

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace