Genetic control over biogenic crystal morphogenesis in zebrafish.
Journal
Nature chemical biology
ISSN: 1552-4469
Titre abrégé: Nat Chem Biol
Pays: United States
ID NLM: 101231976
Informations de publication
Date de publication:
30 Aug 2024
30 Aug 2024
Historique:
received:
26
01
2024
accepted:
08
08
2024
medline:
31
8
2024
pubmed:
31
8
2024
entrez:
30
8
2024
Statut:
aheadofprint
Résumé
Organisms evolve mechanisms that regulate the properties of biogenic crystals to support a wide range of functions, from vision and camouflage to communication and thermal regulation. Yet, the mechanism underlying the formation of diverse intracellular crystals remains enigmatic. Here we unravel the biochemical control over crystal morphogenesis in zebrafish iridophores. We show that the chemical composition of the crystals determines their shape, particularly through the ratio between the nucleobases guanine and hypoxanthine. We reveal that these variations in composition are genetically controlled through tissue-specific expression of specialized paralogs, which exhibit remarkable substrate selectivity. This orchestrated combination grants the organism with the capacity to generate a broad spectrum of crystal morphologies. Overall, our findings suggest a mechanism for the morphological and functional diversity of biogenic crystals and may, thus, inspire the development of genetically designed biomaterials and medical therapeutics.
Identifiants
pubmed: 39215102
doi: 10.1038/s41589-024-01722-1
pii: 10.1038/s41589-024-01722-1
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s).
Références
Land, M. F. The physics and biology of animal reflectors. Prog. Biophys. Mol. Biol. 24, 75–106 (1972).
pubmed: 4581858
doi: 10.1016/0079-6107(72)90004-1
Gur, D., Palmer, B. A., Weiner, S. & Addadi, L. Light manipulation by guanine crystals in organisms: biogenic scatterers, mirrors, multilayer reflectors and photonic crystals. Adv. Funct. Mater. 27, 1603514 (2017).
doi: 10.1002/adfm.201603514
Palmer, B. A. et al. The image-forming mirror in the eye of the scallop. Science 358, 1172–1175 (2017).
pubmed: 29191905
doi: 10.1126/science.aam9506
Gur, D. et al. The dual functional reflecting iris of the zebrafish. Adv. Sci. 5, 1800338 (2018).
doi: 10.1002/advs.201800338
Denton, E. J. Review lecture: on the organization of reflecting surfaces in some marine animals. Philos. Trans. R. Soc. Lond. B 258, 285–313 (1970).
doi: 10.1098/rstb.1970.0037
Gur, D. et al. Structural basis for the brilliant colors of the sapphirinid copepods. J. Am. Chem. Soc. 137, 8408–8411 (2015).
pubmed: 26098960
doi: 10.1021/jacs.5b05289
Teyssier, J., Saenko, S. V., van der Marel, D. & Milinkovitch, M. C. Photonic crystals cause active colour change in chameleons. Nat. Commun. 6, 6368 (2015).
pubmed: 25757068
doi: 10.1038/ncomms7368
Pilátová, J., Pánek, T., Oborník, M., Čepička, I. & Mojzeš, P. Revisiting biocrystallization: purine crystalline inclusions are widespread in eukaryotes. ISME J. 16, 2290–2294 (2022).
pubmed: 35672454
pmcid: 9381591
doi: 10.1038/s41396-022-01264-1
Pavan, M. E. et al. Guanine crystal formation by bacteria. BMC Biol. 21, 66 (2023).
pubmed: 37013555
pmcid: 10071637
doi: 10.1186/s12915-023-01572-8
Mojzeš, P. et al. Guanine, a high-capacity and rapid-turnover nitrogen reserve in microalgal cells. Proc. Natl Acad. Sci. USA 117, 32722–32730 (2020).
pubmed: 33293415
pmcid: 7768779
doi: 10.1073/pnas.2005460117
Levy-Lior, A. et al. Guanine-based biogenic photonic-crystal arrays in fish and spiders. Adv. Funct. Mater. 20, 320–329 (2010).
doi: 10.1002/adfm.200901437
Eyal, Z. et al. Plate-like guanine biocrystals form via templated nucleation of crystal leaflets on preassembled scaffolds. J. Am. Chem. Soc. 144, 22440–22445 (2022).
pubmed: 36469805
pmcid: 9756333
doi: 10.1021/jacs.2c11136
Wagner, A. et al. Macromolecular sheets direct the morphology and orientation of plate-like biogenic guanine crystals. Nat. Commun. 14, 589 (2023).
pubmed: 36737617
pmcid: 9898273
doi: 10.1038/s41467-023-35894-6
Gur, D. et al. In situ differentiation of iridophore crystallotypes underlies zebrafish stripe patterning. Nat. Commun. 11, 6391 (2020).
pubmed: 33319779
pmcid: 7738553
doi: 10.1038/s41467-020-20088-1
Hirata, M., Nakamura, K. & Kondo, S. Pigment cell distributions in different tissues of the zebrafish, with special reference to the striped pigment pattern. Dev. Dyn. 234, 293–300 (2005).
pubmed: 16110504
doi: 10.1002/dvdy.20513
Hirata, M., Nakamura, K., Kanemaru, T., Shibata, Y. & Kondo, S. Pigment cell organization in the hypodermis of zebrafish. Dev. Dyn. 227, 497–503 (2003).
pubmed: 12889058
doi: 10.1002/dvdy.10334
Pedley, A. M. & Benkovic, S. J.Anew view into the regulation of purine metabolism: the purinosome. Trends Biochem. Sci. 42, 141–154 (2017).
pubmed: 28029518
doi: 10.1016/j.tibs.2016.09.009
Wagner, A. et al. The non-classical crystallization mechanism of a composite biogenic guanine crystal. Adv. Mater. 34, e2202242 (2022).
pubmed: 35608485
doi: 10.1002/adma.202202242
Gur, D. et al. Guanine-based photonic crystals in fish scales form from an amorphous precursor. Angew. Chem. 52, 388–391 (2013).
doi: 10.1002/anie.201205336
Ullate-Agote, A. et al. Genome mapping of a LYST mutation in corn snakes indicates that vertebrate chromatophore vesicles are lysosome-related organelles. Proc. Natl Acad. Sci. USA 117, 26307–26317 (2020).
pubmed: 33020272
pmcid: 7584913
doi: 10.1073/pnas.2003724117
Jantschke, A. et al. Anhydrous β-guanine crystals in a marine dinoflagellate: structure and suggested function. J. Struct. Biol. 207, 12–20 (2019).
pubmed: 30991101
doi: 10.1016/j.jsb.2019.04.009
Bagnara, J. T. et al. Common origin of pigment cells. Science 203, 410–415 (1979).
pubmed: 760198
doi: 10.1126/science.760198
Palmer, B. A., Gur, D., Weiner, S., Addadi, L. & Oron, D. The organic crystalline materials of vision: structure–function considerations from the nanometer to the millimeter scale. Adv. Mater. 30, e1800006 (2018).
pubmed: 29888511
doi: 10.1002/adma.201800006
Gur, D. et al. Guanine crystallization in aqueous solutions enables control over crystal size and polymorphism. Cryst. Growth Des. 16, 4975–4980 (2016).
doi: 10.1021/acs.cgd.6b00566
Hirsch, A. et al. Biologically controlled morphology and twinning in guanine crystals. Angew. Chem. 56, 9420–9424 (2017).
doi: 10.1002/anie.201704801
Guo, D. et al. Formation mechanism of twinned β-form anhydrous guanine platelets in scallop eyes. CrystEngComm 25, 4521–4530 (2023).
doi: 10.1039/D3CE00485F
Greenstein, L. Nacreous pigments and their properties. Proc. Sci. Sect. Toilet Goods Assoc. 26, 20–26 (1966).
Pinsk, N. et al. Biogenic guanine crystals are solid solutions of guanine and other purine metabolites. J. Am. Chem. Soc. 144, 5180–5189 (2022).
pubmed: 35255213
pmcid: 8949762
doi: 10.1021/jacs.2c00724
Department of Health and Human Services, Food and Drug Administration Guanine. Code of Federal Regulations https://www.ecfr.gov/current/title-21/chapter-I/subchapter-A/part-73/subpart-C/section-73.2329 (1977).
Higdon, C. W., Mitra, R. D. & Johnson, S. L. Gene expression analysis of zebrafish melanocytes, iridophores, and retinal pigmented epithelium reveals indicators of biological function and developmental origin. PLoS ONE 8, e67801 (2013).
pubmed: 23874447
pmcid: 3706446
doi: 10.1371/journal.pone.0067801
Kimura, T. Pigments in teleosts and their biosynthesis. In Pigments, Pigment Cells and Pigment Patterns (eds Hashimoto, H., Goda, M., Futahashi, R., Kelsh, R. & Akiyama, T.) (Springer, 2021).
Jang, H. S. et al. Epigenetic dynamics shaping melanophore and iridophore cell fate in zebrafish. Genome Biol. 22, 282 (2021).
pubmed: 34607603
pmcid: 8489059
doi: 10.1186/s13059-021-02493-x
Li, Y. et al. Integrative analysis of circadian transcriptome and metabolic network reveals the role of de novo purine synthesis in circadian control of cell cycle. PLoS Comput. Biol. 11, e1004086 (2015).
pubmed: 25714999
pmcid: 4340947
doi: 10.1371/journal.pcbi.1004086
Kimura, T., Takehana, Y. & Naruse, K. pnp4a is the causal gene of the medaka iridophore mutant guanineless. G3 (Bethesda) 7, 1357–1363 (2017).
pubmed: 28258112
doi: 10.1534/g3.117.040675
Ide, H. & Hama, T. Guanine formation in isolated iridophores from bullfrog tadpoles. Biochim. Biophys. Acta 286, 269–271 (1972).
pubmed: 4540813
doi: 10.1016/0304-4165(72)90264-4
Owen, J., Yates, C. & Kelsh, R. N. Pigment patterning in teleosts. In Pigments, Pigment Cells and Pigment Patterns (eds Hashimoto, H. et al.) (Springer, 2021).
Irion, U., Singh, A. P. & Nüsslein-Volhard, C. The developmental genetics of vertebrate color pattern formation: lessons from zebrafish. Curr. Top. Dev. Biol. 117, 141–169 (2016).
pubmed: 26969976
doi: 10.1016/bs.ctdb.2015.12.012
Subkhankulova, T. et al. Zebrafish pigment cells develop directly from persistent highly multipotent progenitors. Nat. Commun. 14, 1258 (2023).
pubmed: 36878908
pmcid: 9988989
doi: 10.1038/s41467-023-36876-4
Lister, J. A., Lane, B. M., Nguyen, A. & Lunney, K. Embryonic expression of zebrafish MiT family genes tfe3b, tfeb, and tfec. Dev. Dyn. 240, 2529–2538 (2011).
pubmed: 21932325
pmcid: 3197887
doi: 10.1002/dvdy.22743
Saunders, L. M. et al. Thyroid hormone regulates distinct paths to maturation in pigment cell lineages. eLife 8, e45181 (2019).
pubmed: 31140974
pmcid: 6588384
doi: 10.7554/eLife.45181
Szklarczyk, D. et al. STRING v11: protein–protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res. 47, D607–D613 (2019).
pubmed: 30476243
doi: 10.1093/nar/gky1131
Zhou, Y. et al. Metascape provides a biologist-oriented resource for the analysis of systems-level datasets. Nat. Commun. 10, 1523 (2019).
pubmed: 30944313
pmcid: 6447622
doi: 10.1038/s41467-019-09234-6
Ng, A., Uribe, R. A., Yieh, L., Nuckels, R. & Gross, J. M. Zebrafish mutations in gart and paics identify crucial roles for de novo purine synthesis in vertebrate pigmentation and ocular development. Development 136, 2601–2611 (2009).
pubmed: 19570845
pmcid: 2709066
doi: 10.1242/dev.038315
Fernández, J. R., Byrne, B. & Firestein, B. L. Phylogenetic analysis and molecular evolution of guanine deaminases: from guanine to dendrites. J. Mol. Evol. 68, 227–235 (2009).
pubmed: 19221682
doi: 10.1007/s00239-009-9205-x
Wu, X. W., Lee, C. C., Muzny, D. M. & Caskey, C. T. Urate oxidase: primary structure and evolutionary implications. Proc. Natl Acad. Sci. USA 86, 9412–9416 (1989).
pubmed: 2594778
pmcid: 298506
doi: 10.1073/pnas.86.23.9412
Dong, Y. et al. High mass resolution, spatial metabolite mapping enhances the current plant gene and pathway discovery toolbox. New Phytol. 228, 1986–2002 (2020).
pubmed: 32654288
doi: 10.1111/nph.16809
Baek, M. et al. Accurate prediction of protein structures and interactions using a three-track neural network. Science 373, 871–876 (2021).
pubmed: 34282049
pmcid: 7612213
doi: 10.1126/science.abj8754
Li, Z. et al. Uni-Fold: an open-source platform for developing protein folding models beyond AlphaFold. Preprint at bioRxiv https://doi.org/10.1101/2022.08.04.502811 (2022).
Mirdita, M. et al. ColabFold: making protein folding accessible to all. Nat. Methods 19, 679–682 (2022).
pubmed: 35637307
pmcid: 9184281
doi: 10.1038/s41592-022-01488-1
Wu, R. et al. High-resolution de novo structure prediction from primary sequence. Preprint at bioRxiv https://doi.org/10.1101/2022.07.21.500999 (2022).
Rives, A. et al. Biological structure and function emerge from scaling unsupervised learning to 250 million protein sequences. Proc. Natl Acad. Sci. USA 118, e2016239118 (2021).
pubmed: 33876751
pmcid: 8053943
doi: 10.1073/pnas.2016239118
Jumper, J. et al. Highly accurate protein structure prediction with AlphaFold. Nature 596, 583–589 (2021).
pubmed: 34265844
pmcid: 8371605
doi: 10.1038/s41586-021-03819-2
Zhang, Y. & Ealick, S. E. Purine nucleoside phosphorylase. In Computational and Structural Approaches to Drug Discovery: Ligand–Protein Interactions (eds Stroud, R. & Finer-Moore, J.) (RSC, 2007).
Hartman, P. & Perdok, W. G. On the relations between structure and morphology of crystals. I. Acta Crystallogr. 8, 49–52 (1955).
doi: 10.1107/S0365110X55000121
Addadi, L. et al. Growth and dissolution of organic crystals with `tailor-made' inhibitors—implications in stereochemistry and materials science. Angew. Chem. 24, 466–485 (1985).
doi: 10.1002/anie.198504661
Berkovitch-Yellin, Y. et al. Crystal morphology engineering by ‘tailor-made’ inhibitors; a new probe to fine intermolecular interactions. J. Am. Chem. Soc. 107, 3111–3122 (1985).
doi: 10.1021/ja00297a017
Levesque, M. P., Krauss, J., Koehler, C., Boden, C. & Harris, M. P. New tools for the identification of developmentally regulated enhancer regions in embryonic and adult zebrafish. Zebrafish 10, 21–29 (2013).
pubmed: 23461416
pmcid: 3670562
doi: 10.1089/zeb.2012.0775
Lewis, V. M. et al. Fate plasticity and reprogramming in genetically distinct populations of Danio leucophores. Proc. Natl Acad. Sci. USA 116, 11806–11811 (2019).
pubmed: 31138706
pmcid: 6575160
doi: 10.1073/pnas.1901021116
Elinger, D., Gabashvili, A. & Levin, Y. Suspension trapping (S-Trap) is compatible with typical protein extraction buffers and detergents for bottom-up. J. Proteome Res. 18, 1441–1445 (2019).
pubmed: 30761899
doi: 10.1021/acs.jproteome.8b00891
Millikin, R. J., Solntsev, S. K., Shortreed, M. R. & Smith, L. M. Ultrafast peptide label-free quantification with FlashLFQ. Proteome Res. 17, 386–391 (2018).
doi: 10.1021/acs.jproteome.7b00608
Miller, R. M. et al. Improved protein inference from multiple protease bottom-up mass spectrometry data. Proteome Res. 18, 3429–3438 (2019).
doi: 10.1021/acs.jproteome.9b00330
Tyanova, S. et al. The Perseus computational platform for comprehensive analysis of (prote)omics data. Nat. Methods 13, 731–740 (2016).
pubmed: 27348712
doi: 10.1038/nmeth.3901
Tamura, K., Stecher, G. & Kumar, S. MEGA11: Molecular Evolutionary Genetics Analysis version 11. Mol. Biol. Evol. 38, 3022–3027 (2021).
pubmed: 33892491
pmcid: 8233496
doi: 10.1093/molbev/msab120
Kroll, F. et al. A simple and effective F
pubmed: 33416493
pmcid: 7793621
doi: 10.7554/eLife.59683
Kwan, K. M. et al. The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev. Dyn. 236, 3088–3099 (2007).
pubmed: 17937395
doi: 10.1002/dvdy.21343
Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).
pubmed: 22743772
doi: 10.1038/nmeth.2019
Haubold, C. et al. Segmenting and tracking multiple dividing targets using ilastik. Adv. Anat. Embryol. Cell Biol. 219, 199–229 (2016).
pubmed: 27207368
doi: 10.1007/978-3-319-28549-8_8
Schmittgen, T. & Livak, K. Analyzing real-time PCR data by the comparative CT method. Nat. Protoc. 3, 1101–1108 (2008).
pubmed: 18546601
doi: 10.1038/nprot.2008.73
Tang, R. et al. Validation of zebrafish (Danio rerio) reference genes for quantitative real-time RT–PCR normalization. Acta Biochim. Biophys. Sin. 39, 384–390 (2007).
pubmed: 17492136
doi: 10.1111/j.1745-7270.2007.00283.x
Dong, Y. et al. PICA: pixel intensity correlation analysis for deconvolution and metabolite identification in mass spectrometry imaging. Anal. Chem. 95, 1652–1662 (2023).
pubmed: 36594613
pmcid: 9850408
Bemis, K. D. et al. Cardinal: an R package for statistical analysis of mass spectrometry-based imaging experiments. Bioinformatics 31, 2418–2420 (2015).
pubmed: 25777525
pmcid: 4495298
doi: 10.1093/bioinformatics/btv146
Mastronarde, D. N. Automated electron microscope tomography using robust prediction of specimen movements. J. Struct. Biol. 152, 36–51 (2005).
pubmed: 16182563
doi: 10.1016/j.jsb.2005.07.007
Mastronarde, D. N. & Held, S. R. Automated tilt series alignment and tomographic reconstruction in IMOD. J. Struct. Biol. 197, 102–113 (2017).
pubmed: 27444392
doi: 10.1016/j.jsb.2016.07.011
Chen, F., Liu, Y., Li, L., Qi, L. & Ma, Y. Synthesis of bio-inspired guanine microplatelets: morphological and crystallographic control. Chemistry 26, 16228–16235 (2020).
pubmed: 32888220
doi: 10.1002/chem.202003156
Perez-Riverol, Y. et al. The PRIDE database resources in 2022: a hub for mass spectrometry-based proteomics evidences. Nucleic Acids Res. 50, D543–D552 (2022).
pubmed: 34723319
doi: 10.1093/nar/gkab1038