Thioflavin S binds non-amyloid protein structures in lampbrush chromosomes of <em>Gallus gallus domesticus</em>

Vera Siniukova; Svetlana Galkina; Alexey Galkin

doi:10.21638/spbu03.2022.106

Authors

Vera Siniukova Vavilov Institute of General Genetics, Russian Academy of Sciences, Saint Petersburg Branch, Universitetskaya nab., 7–9, Saint Petersburg, 199034, Russian Federation https://orcid.org/0000-0002-5505-4693
Svetlana Galkina Department of Genetics and Biotechnology, Faculty of Biology, Saint Petersburg State University, Universitetskaya nab., 7–9, Saint Petersburg, 199034, Russian Federation https://orcid.org/0000-0002-7034-2466
Alexey Galkin Vavilov Institute of General Genetics, Russian Academy of Sciences, Saint Petersburg Branch, Universitetskaya nab., 7–9, Saint Petersburg, 199034, Russian Federation; Department of Genetics and Biotechnology, Faculty of Biology, Saint Petersburg State University, Universitetskaya nab., 7–9, Saint Petersburg, 199034, Russian Federation https://orcid.org/0000-0002-7362-8857

DOI:

https://doi.org/10.21638/spbu03.2022.106

Abstract

Proteins that normally function in amyloid form are found in bacteria, yeast, plants and vertebrates, including humans. In particular, amyloid fibrils and amyloid-like structures are described in the germ cells of various organisms. Recently we showed that in chicken oocytes there are some nuclear structures that are stained by the amyloid-specific dye thioflavin S. Here we demonstrate that thioflavin S binds giant terminal RNP aggregates in chicken lampbrush chromosomes. However, these structures are not stained with Congo red and conformation-dependent anti-amyloid antibodies. Thus, thioflavin S stains chromosome-associated proteins that do not have amyloid properties. These data indicate that thioflavin S must be used with caution when identifying new functional and pathological amyloids.

Keywords:

amyloid, thioflavin S, Congo red, anti-amyloid antibodies, chicken, lampbrush chromosomes

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References

Antonets, K. S., Belousov, M. V., Sulatskaya, A. I., Belousova, M. E., Kosolapova, A. O., Sulatsky, M. I., Andreeva, E. A., Zykin, P. A., Malovichko, Y. V., Shtark, O. Y., Lykholay, A. N., Volkov, K. V., Kuznetsova, I. M., Turoverov, K. K., Kochetkova, E. Y., Bobylev, A. G., Usachev, K. S., Demidov, O. N., Tikhonovich, I. A., and Nizhnikov, A. A. 2020. Accumulation of storage proteins in plant seeds is mediated by amyloid formation. PLOS Biology 23:18(7):e3000564. https://doi.org/10.1371/journal.pbio.3000564

Benson, M. D., Buxbaum, J. N., Eisenberg, D. S., Merlini, G., Saraiva, M. J. M., Sekijima, Y., Sipe, J. D., and Westermark, P. 2018. Amyloid nomenclature 2018: recommendations by the International Society of Amyloidosis (ISA) nomenclature committee. Amyloid 25(4):215–219. https://doi.org/10.1080/13506129.2018.1549825

Benson, M. D., Buxbaum, J. N., Eisenberg, D. S., Merlini, G., Saraiva, M. J. M., Sekijima, Y., Sipe, J. D., and Westermark, P. 2020. Amyloid nomenclature 2020: update and recommendations by the International Society of Amyloidosis (ISA) nomenclature committee. Amyloid 27(4):217–222. https://doi.org/10.1080/13506129.2020.1835263

Boke, E., Ruer, M., Wühr, M., Coughlin, M., Lemaitre, R., Gygi, S. P., Alberti, S., Drechsel, D., Hyman, A. A., and Mitchison, T. J. 2016. Amyloid-like self-assembly of a cellular compartment. Cell 166(3):637–650. https://doi.org/10.1016/j.cell.2016.06.051

Bousset, L., Redeker, V., Decottignies, P., Dubois, S., Le Maréchal, P., and Melki, R. 2004. Structural characterization of the fibrillar form of the yeast Saccharomyces cerevisiae prion Ure2p. Biochemistry 4:43(17):5022–5032. https://doi.org/10.1021/bi049828e

Callan, H. G. 1986. Lampbrush chromosomes; pp. 1–24 in Molecular Biology Biochemistry and Biophysics 36. SpringerVerlag, Berlin. https://doi.org/10.1007/978-3-642-827921_1

Carrotta, R., Bauer, R., Waninge, R., and Rischel, C. 2001. Conformational characterization of oligomeric intermediates and aggregates in beta-lactoglobulin heat aggregation. Protein Science 10(7):1312–1318. https://doi.org/10.1110/ps.42501

Chelysheva, L. A., Soloveĭ, I. V., Rodionov, A. V., Iakovlev, A. F., and Gaginskaia, E. R. 1990. The lampbrush chromosomes of the chicken. Cytological maps of the macrobivalents. Tsitologiia 32(4):303–316. (In Russian)

De Ferrari, G. V., Canales, M. A., Shin, I., Weiner, L. M., Silman, I., and Inestrosa, N. C. 2001. A structural motif of acetylcholinesterase that promotes amyloid beta-peptide fibril formation. Biochemistry 40(35):10447–10457. https://doi.org/10.1021/bi0101392

Egge, N., Muthusubramanian, A., and Cornwall, G. A. 2015. Amyloid properties of the mouse egg zona pellucida. PLoS ONE 10(6):e0129907. https://doi.org/10.1371/journal.pone.0129907

Gaginskaya, E., Kulikova, T., and Krasikova, A. 2009. Avian lampbrush chromosomes: a powerful tool for exploration of genome expression. Cytogenetic and Genome Research 124:251–267. https://doi.org/10.1159/000218130

Guyonnet, B., Egge, N., and Cornwall, G. A. 2014. Functional amyloids in the mouse sperm acrosome. Molecular and Cellular Biology 34(14):2624–2634. https://doi.org/10.1128/MCB.00073-14

Howie, A. J., Brewer, D. B., Howell, D., and Jones, A. P. 2008. Physical basis of colors seen in Congo red-stained amyloid in polarized light. Laboratory Investigation 88(3):232–242. https://doi.org/10.1038/labinvest.3700714

Iconomidou, V. A. and Hamodrakas, S. J. 2008. Natural protective amyloids. Current Protein & Peptide Science 9(3):291– 309. https://doi.org/10.2174/138920308784534041

Kabani, M. and Melki, R. 2020. The Yarrowia lipolytica orthologs of Sup35p assemble into thioflavin T-negative amyloid fibrils. Biochemical and Biophysical Research Communications 529(3):533–539. https://doi.org/10.1016/j.bbrc.2020.06.024

Kayed, R., Head, E., Sarsoza, F., Saing, T., Cotman, C. W., Necula, M., Margol, L., Wu, J., Breydo, L., Thompson, J. L., Rasool, S., Gurlo, T., Butler, P., and Glabe, S. G. 2007. Fibril specific, conformation dependent antibodies recognize a generic epitope common to amyloid fibrils and fibrillar oligomers that is absent in prefibrillar oligomers. Molecular Neurodegeneration 2:18. https://doi.org/10.1186/1750-1326-2-18

Khurana, R., Uversky, V. N., Nielsen, L., and Fink, A. L. 2001. Is Congo red an amyloid-specific dye? Journal of Biological Chemistry 276(25):22715–22721. https://doi.org/10.1074/jbc.M011499200

Krasikova, A., Khodyuchenko, T., Maslova, A., and Vasilevskaya, E. 2012. Three-dimensional organisation of RNAprocessing machinery in avian growing oocyte nucleus. Chromosome Research 20(8):979–994. https://doi.org/10.1007/s10577-012-9327-7

Kulikova, T., Chervyakova, D., Zlotina, A., Krasikova, A., and Gaginskaya, E. 2015. Giant poly(A)-rich RNP aggregates form at terminal regions of avian lampbrush chromosomes. Chromosoma 125(4):709–724. https://doi.org/10.1007/s00412-015-0563-4

Linke, R. P. 2000. Highly sensitive diagnosis of amyloid and various amyloid syndromes using Congo red fluorescence. Virchows Archiv 436(5):439–448. https://doi.org/10.1007/s004280050471

Liu, S., Mozaffari-Jovin, S., Wollenhaupt, J., Santos, K. F., Theuser, M., Dunin-Horkawicz, S., Fabrizio, P., Bujnicki, J. M., Lührmann, R., and Wahl, M. C. 2015. A composite double-/single-stranded RNA-binding region in protein Prp3 supports tri-snRNP stability and splicing. eLife 4:e07320. https://doi.org/10.7554/eLife.07320

Mason, T. and Shimanovich, U. 2018. Fibrous protein selfassembly in biomimetic materials. Advanced Materials 30(41):e1706462. https://doi.org/10.1002/adma.201706462

Pimentel, R. N., Navarro, P. A., Wang, F., Robinson Jr, L. G., Cammer, M., Liang, F., Kramer, Y., and Keefe, D. L. 2019. Amyloid-like substance in mice and human oocytes and embryos. Journal of Assisted Reproduction and Genetics 36(9):1877–1890. https://doi.org/10.1007/s10815-019-01530-w

Podrabsky, J. E., Carpenter, J. F., and Hand, S. C. 2001. Survival of water stress in annual fish embryos: dehydration avoidance and egg envelope amyloid fibers. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology 280(1):R123–R131. https://doi.org/10.1152/ajpregu.2001.280.1.R123

Ryzhova, T. A., Sopova, J. V., Zadorsky, S. P., Siniukova, V. A., Sergeeva, A. V., Galkina, S. A., Nizhnikov, A. A., Shenfeld, A. A., Volkov, K. V., and Galkin, A. P. 2018. Screening for amyloid proteins in the yeast proteome. Current Genetics 64(2):469–478. https://doi.org/10.1007/s00294-017-0759-7

Saifitdinova, A., Galkina, S., Volodkina, V., and Gaginskaya, E. 2017. Preparation of lampbrush chromosomes dissected from avian and reptilian growing oocytes. Biological Communications 62(3):165–168. https://doi.org/10.21638/11701/spbu03.2017.302

Sergeeva, A. V. and Galkin, A. P. 2020. Functional amyloids of eukaryotes: criteria, classification, and biological significance. Current Genetics 66(5):849–866. https://doi.org/10.1007/s00294-020-01079-7

Siniukova, V. A., Sopova, J. V., Galkina, S. A., and Galkin, A. P. 2020. Search for functional amyloid structures in chicken and fruit fly female reproductive cells. Prion 14(1):278–282. https://doi.org/10.1080/19336896.2020.1859439

Xu, S., Li, Q., Xiang, J., Yang, Q., Sun, H., Guan, A., Wang, L., Liu, Y., Yu, L., Shi, Y., Chen, H., and Tang, Y. 2016. Thioflavin T as an efficient fluorescence sensor for selective recognition of RNA G-quadruplexes. Scientific Reports 21(6):24793. https://doi.org/10.1038/srep24793