Proximity labelling of pro-interleukin-1α reveals evolutionary conserved nuclear interactions.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
08 Aug 2024
08 Aug 2024
Historique:
received:
15
06
2023
accepted:
24
07
2024
medline:
9
8
2024
pubmed:
9
8
2024
entrez:
8
8
2024
Statut:
epublish
Résumé
Interleukin-1α is a suggested dual-function cytokine that diverged from interleukin-1β in mammals potentially by acquiring additional biological roles that relate to highly conserved regions in the pro-domain of interleukin-1α, including a nuclear localisation sequence and histone acetyltransferase-binding domains. Why evolution modified pro-interleukin-1α's subcellular location and protein interactome, and how this shaped interleukin-1α's intracellular role, is unknown. Here we show that TurboID proximity labelling with pro-interleukin-1α suggests a nuclear role for pro-interleukin-1α that involves interaction with histone acetyltransferases, including EP300. We also identify and validate inactivating mutations in the pro-interleukin-1α nuclear localisation sequence of multiple mammalian species, including toothed whales, castorimorpha and marsupials. However, histone acetyltransferase-binding domains are conserved in those species that have lost pro-interleukin-1α nuclear localisation. Together, these data suggest that histone acetyltransferase binding and nuclear localisation occurred together, and that while some species lost the nuclear localisation sequence in their pro-interleukin-1α, histone acetyltransferase binding ability was maintained. The nuclear localisation sequence was lost from several distinct species at different evolutionary times, suggesting convergent evolution, and that the loss of the nuclear localisation sequence confers some important biological outcome.
Identifiants
pubmed: 39117622
doi: 10.1038/s41467-024-50901-0
pii: 10.1038/s41467-024-50901-0
doi:
Substances chimiques
Interleukin-1alpha
0
E1A-Associated p300 Protein
EC 2.3.1.48
Histone Acetyltransferases
EC 2.3.1.48
Nuclear Localization Signals
0
EP300 protein, human
EC 2.3.1.48
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
6750Subventions
Organisme : RCUK | Medical Research Council (MRC)
ID : MR/T016515/1
Organisme : RCUK | Medical Research Council (MRC)
ID : MR/W028867/1
Organisme : RCUK | Medical Research Council (MRC)
ID : MR/T016515/1
Organisme : RCUK | Medical Research Council (MRC)
ID : MR/T016515/1
Organisme : RCUK | Medical Research Council (MRC)
ID : MR/T016515/1
Organisme : RCUK | Medical Research Council (MRC)
ID : MR/T016515/1
Organisme : British Heart Foundation (BHF)
ID : AA/18/4/34221
Organisme : Consejo Nacional de Innovación, Ciencia y Tecnología (CONICYT)
ID : Becas Chile 721704488
Informations de copyright
© 2024. The Author(s).
Références
Bertheloot, D. & Latz, E. HMGB1, IL-1α, IL-33 and S100 proteins: dual-function alarmins. Cell. Mol. Immunol. 14, 43–64 (2017).
pubmed: 27569562
doi: 10.1038/cmi.2016.34
Garlanda, C., Dinarello, C. A. & Mantovani, A. The interleukin-1 family: back to the future. Immunity 39, 1003–1018 (2013).
pubmed: 24332029
pmcid: 3933951
doi: 10.1016/j.immuni.2013.11.010
Rivers-Auty, J., Daniels, M. J. D., Colliver, I., Robertson, D. L. & Brough, D. Redefining the ancestral origins of the interleukin-1 superfamily. Nat. Commun. 9, 1156 (2018).
pubmed: 29559685
pmcid: 5861070
doi: 10.1038/s41467-018-03362-1
Monteleone, M. et al. Interleukin-1β maturation triggers its relocation to the plasma membrane for gasdermin-D-dependent and -independent secretion. Cell Rep. 24, 1425–1433 (2018).
pubmed: 30089254
doi: 10.1016/j.celrep.2018.07.027
Lamacchia, C., Rodriguez, E., Palmer, G. & Gabay, C. Endogenous IL-1α is a chromatin-associated protein in mouse macrophages. Cytokine 63, 135–144 (2013).
pubmed: 23684408
doi: 10.1016/j.cyto.2013.04.010
Wessendorf, J. H., Garfinkel, S., Zhan, X., Brown, S. & Maciag, T. Identification of a nuclear localization sequence within the structure of the human interleukin-1 alpha precursor. J. Biol. Chem. 268, 22100–22104 (1993).
pubmed: 8408068
doi: 10.1016/S0021-9258(20)80653-X
Luheshi, N. M., Rothwell, N. J. & Brough, D. The dynamics and mechanisms of interleukin-1alpha and beta nuclear import. Traffic 10, 16–25 (2009).
pubmed: 18939951
doi: 10.1111/j.1600-0854.2008.00840.x
Shvedunova, M. & Akhtar, A. Modulation of cellular processes by histone and non-histone protein acetylation. Nat. Rev. Mol. Cell Biol. 23, 329–349 (2022).
pubmed: 35042977
doi: 10.1038/s41580-021-00441-y
Lee, K. K. & Workman, J. L. Histone acetyltransferase complexes: one size doesn’t fit all. Nat. Rev. Mol. Cell Biol. 8, 284–295 (2007).
pubmed: 17380162
doi: 10.1038/nrm2145
Buryskova, M., Pospisek, M., Grothey, A., Simmet, T. & Burysek, L. Intracellular interleukin-1alpha functionally interacts with histone acetyltransferase complexes. J. Biol. Chem. 279, 4017–4026 (2004).
pubmed: 14612453
doi: 10.1074/jbc.M306342200
Zamostna, B. et al. N-terminal domain of nuclear IL-1α shows structural similarity to the C-terminal domain of Snf1 and binds to the HAT/core module of the SAGA complex. PLoS One 7, e41801 (2012).
pubmed: 22879895
pmcid: 3412866
doi: 10.1371/journal.pone.0041801
McCarthy, D. A. et al. Redox-control of the alarmin, Interleukin-1α. Redox Biol. 1, 218–225 (2013).
pubmed: 24024155
pmcid: 3757693
doi: 10.1016/j.redox.2013.03.001
Branon, T. C. et al. Efficient proximity labeling in living cells and organisms with TurboID. Nat. Biotechnol. 36, 880–887 (2018).
pubmed: 30125270
pmcid: 6126969
doi: 10.1038/nbt.4201
Luheshi, N. M., McColl, B. W. & Brough, D. Nuclear retention of IL-1 alpha by necrotic cells: a mechanism to dampen sterile inflammation. Eur. J. Immunol. 39, 2973–2980 (2009).
pubmed: 19839011
pmcid: 3394668
doi: 10.1002/eji.200939712
Tapia, V. S. et al. The three cytokines IL-1beta, IL-18, and IL-1alpha share related but distinct secretory routes. J. Biol. Chem. 294, 8325–8335 (2019).
pubmed: 30940725
pmcid: 6544845
doi: 10.1074/jbc.RA119.008009
Mi, W. et al. The ZZ-type zinc finger of ZZZ3 modulates the ATAC complex-mediated histone acetylation and gene activation. Nat. Commun. 9, 3759 (2018).
pubmed: 30217978
pmcid: 6138639
doi: 10.1038/s41467-018-06247-5
Kumar, S. et al. TimeTree 5: an expanded resource for species divergence times. Mol. Biol. Evol. 39, msac174 (2022).
Swanson, M. T., Oliveros, C. H. & Esselstyn, J. A. A phylogenomic rodent tree reveals the repeated evolution of masseter architectures. Proc. Biol. Sci. 286, 20190672 (2019).
pubmed: 31064307
pmcid: 6532498
Fabre, P. H., Hautier, L., Dimitrov, D. & Douzery, E. J. A glimpse on the pattern of rodent diversification: a phylogenetic approach. BMC Evol. Biol. 12, 88 (2012).
pubmed: 22697210
pmcid: 3532383
doi: 10.1186/1471-2148-12-88
Wu, S. et al. Molecular and paleontological evidence for a post-cretaceous origin of rodents. PLoS One 7, e46445 (2012).
pubmed: 23071573
pmcid: 3465340
doi: 10.1371/journal.pone.0046445
Burzynski, L. C. et al. The coagulation and immune systems are directly linked through the activation of interleukin-1α by thrombin. Immunity 50, 1033–1042.e1036 (2019).
pubmed: 30926232
pmcid: 6476404
doi: 10.1016/j.immuni.2019.03.003
Zhou, Y. et al. Platypus and echidna genomes reveal mammalian biology and evolution. Nature 592, 756–762 (2021).
pubmed: 33408411
pmcid: 8081666
doi: 10.1038/s41586-020-03039-0
Cavalli, G. et al. Interleukin 1α: a comprehensive review on the role of IL-1α in the pathogenesis and treatment of autoimmune and inflammatory diseases. Autoimmun. Rev. 20, 102763 (2021).
pubmed: 33482337
doi: 10.1016/j.autrev.2021.102763
Martin, S. J. Cell death and inflammation: the case for IL-1 family cytokines as the canonical DAMPs of the immune system. FEBS J. 283, 2599–2615 (2016).
pubmed: 27273805
doi: 10.1111/febs.13775
Orjalo, A. V., Bhaumik, D., Gengler, B. K., Scott, G. K. & Campisi, J. Cell surface-bound IL-1alpha is an upstream regulator of the senescence-associated IL-6/IL-8 cytokine network. Proc. Natl Acad. Sci. USA 106, 17031–17036 (2009).
pubmed: 19805069
pmcid: 2761322
doi: 10.1073/pnas.0905299106
Wiggins, K. A. et al. IL-1α cleavage by inflammatory caspases of the noncanonical inflammasome controls the senescence-associated secretory phenotype. Aging Cell 18, e12946 (2019).
pubmed: 30916891
pmcid: 6516163
doi: 10.1111/acel.12946
Springer, M. S., Foley, N. M., Brady, P. L., Gatesy, J. & Murphy, W. J. Evolutionary models for the diversification of placental mammals across the KPg boundary. Front. Genet. 10, 1241 (2019).
pubmed: 31850081
pmcid: 6896846
doi: 10.3389/fgene.2019.01241
Eldridge, M. D. B., Beck, R. M. D., Croft, D. A., Travouillon, K. J. & Fox, B. J. An emerging consensus in the evolution, phylogeny, and systematics of marsupials and their fossil relatives (Metatheria). J. Mammal. 100, 802–837 (2019).
doi: 10.1093/jmammal/gyz018
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. Proc. Natl Acad. Sci. USA 107, 2574–2579 (2010).
pubmed: 20133797
pmcid: 2823886
doi: 10.1073/pnas.0915018107
Burkard, M., Whitworth, D., Schirmer, K. & Nash, S. B. Establishment of the first humpback whale fibroblast cell lines and their application in chemical risk assessment. Aquat. Toxicol. 167, 240–247 (2015).
pubmed: 26363275
doi: 10.1016/j.aquatox.2015.08.005
Girjes, A. A., Lee, K. E. & Carrick, F. N. Establishment and characterization of a new epithelial cell line, KC-1, from koala (Phascolarctos cinereus) conjunctiva. Vitr. Cell Dev. Biol. Anim. 39, 110–113 (2003).
doi: 10.1007/s11626-003-0002-3
Tashiro, K., Segawa, T., Futami, T., Suzuki, M. & Itou, T. Establishment and characterization of a novel kidney cell line derived from the common bottlenose dolphin. Vitr. Cell Dev. Biol. Anim. 59, 536–549 (2023).
doi: 10.1007/s11626-023-00786-y
Yu, J. et al. Establishment of epidermal cell lines derived from the skin of the Atlantic bottlenose dolphin (Tursiops truncatus). Anat. Rec. A Discov. Mol. Cell Evol. Biol. 287, 1246–1255 (2005).
pubmed: 16281302
doi: 10.1002/ar.a.20266
Grossman, S. R. et al. Polyubiquitination of p53 by a ubiquitin ligase activity of p300. Science 300, 342–344 (2003).
pubmed: 12690203
doi: 10.1126/science.1080386
Shi, D. et al. CBP and p300 are cytoplasmic E4 polyubiquitin ligases for p53. Proc. Natl Acad. Sci. USA 106, 16275–16280 (2009).
pubmed: 19805293
pmcid: 2752525
doi: 10.1073/pnas.0904305106
Lin, X., Zhang, H., Boyce, B. F. & Xing, L. Ubiquitination of interleukin-1α is associated with increased pro-inflammatory polarization of murine macrophages deficient in the E3 ligase ITCH. J. Biol. Chem. 295, 11764–11775 (2020).
pubmed: 32587089
pmcid: 7450106
doi: 10.1074/jbc.RA120.014298
Tyanova, S., Temu, T. & Cox, J. The MaxQuant computational platform for mass spectrometry-based shotgun proteomics. Nat. Protoc. 11, 2301–2319 (2016).
pubmed: 27809316
doi: 10.1038/nprot.2016.136
Hall, B. G. Building phylogenetic trees from molecular data with MEGA. Mol. Biol. Evol. 30, 1229–1235 (2013).
pubmed: 23486614
doi: 10.1093/molbev/mst012
Jones, D. T., Taylor, W. R. & Thornton, J. M. The rapid generation of mutation data matrices from protein sequences. Comput. Appl. Biosci. 8, 275–282 (1992).
pubmed: 1633570
Felsenstein, J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791 (1985).
pubmed: 28561359
doi: 10.2307/2408678
Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547–1549 (2018).
pubmed: 29722887
pmcid: 5967553
doi: 10.1093/molbev/msy096
Kosugi, S., Hasebe, M., Tomita, M. & Yanagawa, H. Systematic identification of cell cycle-dependent yeast nucleocytoplasmic shuttling proteins by prediction of composite motifs. Proc. Natl Acad. Sci. USA 106, 10171–10176 (2009).
pubmed: 19520826
pmcid: 2695404
doi: 10.1073/pnas.0900604106