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The Evolution of Concepts about the Biological Role of Lampbrush Chromosomes

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Few other chromosomes so insistently demand a functional

interpretation as the lampbrush chromosomes of oocytes

Joseph G. Gall

Abstract

The review is focused on the development of ideas about the role of one of the most mysterious phenomena of developmental biology, i.e., the transformation of chromosomes into the so-called lampbrush chromosomes (LBCs). Eukaryotic chromosomes in the LBC phase are characterized by a low level of condensation and discrete structure formed by numerous linearly arranged compact chromomeres, from which lateral loops coated with transcripts are extruded. Linear sizes of LBCs exceed the sizes of the corresponding mitotic chromosomes by more than 30 times, making LBCs a valuable model for analyzing the structure and functioning of chromosomes, as well as structural and functional organization of the genome as a whole by the methods of molecular cytogenetics and genomics with very high resolution. Wide distribution of this phenomenon in nature suggests its functional importance. However, despite repeated attempts to understand the sense of the transformation of chromosomes into LBCs, many questions still remain open. The review critically examines all the main hypotheses explaining the functional importance of LBCs.

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REFERENCES

  1. Rückert, J., Zur Entwickelungsgeschichte des Ovarialeies bei Selachiern, Anat. Anz., 1892, vol. 7, pp. 107—158.

    Google Scholar 

  2. Chelysheva, L.A., Solovei, I.V., and Rodionov, A.V., The lampbrush chromosomes of the chicken: cytological map of the macrobivalents, Tsitologiya, 1990, vol. 32, no. 4, pp. 303—316.

    CAS  Google Scholar 

  3. Derjusheva, S., Kurganova, A., Krasikova, A., et al., Precise identification of chicken chromosomes in the lampbrush form using chromosome painting probes, Chromosome Res., 2003, vol. 11, pp. 749—757. https://doi.org/10.1023/B:CHRO.0000005778.72909.4d

    Article  CAS  PubMed  Google Scholar 

  4. Saifitdinova, A., Derjusheva, S., Krasikova, A., and Gaginskaya, E., Lampbrush chromosomes of the chaffinch (Fringilla coelebs L.), Chromosome Res., 2003, vol. 11, pp. 99—113. https://doi.org/10.1023/A:1022859713777

    Article  CAS  PubMed  Google Scholar 

  5. Galkina, S., Deryusheva, S., Fillon, V., et al., FISH on avian lampbrush chromosomes produces higher resolution gene mapping, Genetica, 2006, vol. 128, nos. 1—3, pp. 241—251. https://doi.org/10.1007/s10709-005-5776-7

    Article  CAS  PubMed  Google Scholar 

  6. Galkina, S., Fillon, V., Saifitdinova, A., et al., Chicken microchromosomes in the lampbrush phase: a cytogenetic description, Cytogenet. Genome Res., 2017, vol. 152, no. 1, pp. 46—54. https://doi.org/10.1159/000475563

    Article  CAS  PubMed  Google Scholar 

  7. Callan, H.G., Lampbrush Chromosomes, Heidelberg: Springer-Verlag, 1986.

    Book  Google Scholar 

  8. Bostock, C.J. and Samner, A.Th., The Eukaryotic Chromosome, Amsterdam: North-Holland Publ. Comp., 1978.

    Google Scholar 

  9. Davidson, E., Gene Activity in Early Development, Orlando: Acad. Press, 1986, 3rd ed.

    Google Scholar 

  10. Krasikova, A.V. and Kulikova, T.V., Khromosomy tipa lampovykh shchetok: sovremennye predstavleniya i perspektivy issledovanii (Lampbrush Chromosomes: Current Concepts and Research Prospects), St. Petersburg: St. Petersburg Uni., 2020.

  11. Macgregor, H.C., Recent developments in the study of lampbrush chromosomes, Heredity, 1980, vol. 44, pp. 3—35. https://doi.org/10.1038/hdy.1980.2

    Article  Google Scholar 

  12. Macgregor, H.C., Lampbrush chromosomes and gene utilization in meiotic prophase, Symp. Soc. Exp. Biol., 1984, vol. 38, pp. 333—347.

    CAS  PubMed  Google Scholar 

  13. Macgregor, H.C., The lampbrush chromosomes of animal oocytes, in Chromosome Structure and Function, New York: Van Nostrand Reinhold, 1986, pp. 152—186.

    Google Scholar 

  14. Macgregor, H.C., So what’s so special about these things called lampbrush chromosomes?, Chromosome Res., 2012, vol. 20, pp. 903—904. https://doi.org/10.1007/s10577-012-9330-z

    Article  CAS  PubMed  Google Scholar 

  15. Macgregor, H.C., Chromomeres revisited, Chromosome Res., 2012, vol. 20, pp. 911—924. https://doi.org/10.1007/s10577-012-9310-3

    Article  CAS  PubMed  Google Scholar 

  16. Gall, J.G., Diaz, M.O., Stephenson, E.C., and Mahon, K.A., The transcription unit of lampbrush chromosomes, Soc. Dev. Biol. Symp., 1983, vol. 41, pp. 137—146.

  17. Gaginskaya, E.R., Lampbrush chromosomes from amphibian oocytes, Tsitologiya, 1989, vol. 31, no. 11, pp. 1267—1291.

    Google Scholar 

  18. Angelier, N., Penrad-Mobayed, M., Billoud, B., et al., What role might lampbrush chromosomes play in maternal gene expression?, Int. J. Dev. Biol., 1996, vol. 40, no. 4, pp. 645—652. https://doi.org/10.1007/BF00292471

    Article  CAS  PubMed  Google Scholar 

  19. Morgan, G.T., Lampbrush chromosomes and associated bodies: new insights into principles of nuclear structure and function, Chromosome Res., 2002, vol. 10, pp. 177—200. https://doi.org/10.1023/a:1015227020652

    Article  CAS  PubMed  Google Scholar 

  20. Gall, J.C., Wu, Z., Murphy, C., and Gao, H., Structure in the amphibian germinal vesicle, Exp. Cell Res., 2004, vol. 296, pp. 28—34. https://doi.org/10.1016/j.yexcr.2004.03.017

    Article  CAS  PubMed  Google Scholar 

  21. Gaginskaya, E., Kulikova, T., and Krasikova, A., Avian lampbrush chromosomes: a powerful tool for exploration of genome expression, Cytogenet. Genome Res., 2009, vol. 124, nos. 3—4, pp. 251—267. https://doi.org/10.1159/000218130

    Article  CAS  PubMed  Google Scholar 

  22. Gall, J.G., Are lampbrush chromosomes unique to meiotic cells?, Chromosome Res., 2012, vol. 20, pp. 905—910. https://doi.org/10.1007/s10577-012-9329-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Morgan, G.T., Imaging the dynamics of transcription loops in living chromosomes, Chromosoma, 2018, vol. 127, pp. 361—374. https://doi.org/10.1007/s00412-018-0667-8

    Article  PubMed  PubMed Central  Google Scholar 

  24. Krasikova, A.V. and Kulikova, T.V., Identification of genomic loci responsible for the formation of nuclear domains using lampbrush chromosomes, Noncoding RNA, 2020, vol. 6, no. 1. https://doi.org/10.3390/ncrna6010001

  25. Flemming, W., Zellsubstanz, Kern und Zelltheilung, Leipzig: F.C.W. Vogel, 1882.

    Book  Google Scholar 

  26. Holl, M., Über die Reifung der Eizellen des Huhnes, Sitzungsber. Akad. Wiss. Wien, Math.-Naturwiss. Kl., Abt. 3, 1890, vol. 99, pp. 311—370.

  27. Duryee, W.R., Isolation of nuclei and non-mitotic chromosome pairs from grog eggs, Arch. Exp. Zellforsch., 1937, vol. 19, pp. 171—176.

    Google Scholar 

  28. Duryee, W.R., Chromosomal physiology in relation to nuclear structure, Ann. N.Y. Acad. Sci., 1950, vol. 50, pp. 920—953.

    Article  Google Scholar 

  29. Macgregor, H.C., and Varley, J.M., Working with Animal Chromosomes, Chichester: John Wiley, 1988, 2nd ed.

    Google Scholar 

  30. Kropotova, E.V. and Gaginskaya, E.R., Lamp-brush chromosomes from Japanese quail oocytes: light and electron microscopy data, Tsitologiya, 1984, vol. 26, pp. 1006—1015.

    Google Scholar 

  31. Hutchison, N., Lampbrush chromosomes of the chicken, Gallus domesticus, J. Cell Biol., 1987, vol. 105, pp. 1493—1500. https://doi.org/10.1083/jcb.105.4.1493

    Article  CAS  PubMed  Google Scholar 

  32. Solovei, I., Gaginskaya, E., Allen, T., and Macgregor, H., A novel structure associated with a lampbrush chromosome in the chicken, Gallus domesticus, J. Cell Sci., 1992, vol. 101, pp. 759—772.

    Article  PubMed  Google Scholar 

  33. Solovei, I., Gaginskaya, E., and Macgregor, H., The arrangement and transcription of telomere DNA sequences at the ends of lampbrush chromosomes of birds, Chromosome Res., 1994, vol. 2, pp. 460—470. https://doi.org/10.1007/BF01552869

    Article  CAS  PubMed  Google Scholar 

  34. Saifitdinova, A., Galkina, S., Volodkina, V., and Gaginskaya, E., Preparation of lampbrush chromosomes dissected from avian and reptilian growing oocytes, Biol. Commun., 2017, vol. 62, pp. 165—168. https://doi.org/10.21638/11701/spbu03.2017.302

    Article  Google Scholar 

  35. Lisachov, A.P., Galkina, S.A., Saifitdinova, A.F., et al., Identification of sex chromosomes in Eremias velox (Lacertidae, Reptilia) using lampbrush chromosome analysis, Comp. Cytogen., 2019, vol. 13, pp. 121—132. https://doi.org/10.3897/CompCytogen.v13i2.34116

    Article  Google Scholar 

  36. Callan, H.G., Lampbrush chromosomes as seen in historical perspective, Results Probl. Cell Differ., 1987, vol. 14, pp. 5—26. https://doi.org/10.1007/978-3-540-47783-9_2

    Article  CAS  PubMed  Google Scholar 

  37. Macgregor, H.C., Lampbrush chromosomes. http://spass-sci.ru/lbc/. Accessed May 30, 2020.

  38. Janssens, F.A., Das chromatische Element während der Entwicklung des Ovocyts von Triton, Anat. Anz., 1904, vol. 24, pp. 648—651.

    Google Scholar 

  39. Kol'tsov, N.K., Issledovaniya o forme kletki: chast’ I. Issledovanie o spermiyakh desyatinogikh rakov v svyazi s obshchimi soobrazheniyami otnositel’no organizatsii kletki (Studies of Cell Shape: Part I. Study on Decapod Sperm in Connection with General Considerations Concerning the Organization of Cells), Moscow: Moscow Univ., 1905.

  40. Kol’tsov, N.K., The structure of chromosomes and metabolism in them, Biol. Zh., 1938, vol. 7, no. 1, pp. 3—46.

    Google Scholar 

  41. Watson, J.D. and Crick, F.H., Molecular structure of nucleic acids: a structure for deoxyribose nucleic acid, Nature, 1953, vol. 171, pp. 737—738. https://doi.org/10.1038/171737a0

    Article  CAS  PubMed  Google Scholar 

  42. Gall, J.G., Kinetics of deoxyribonuclease action on chromosomes, Nature, 1963, vol. 198, pp. 36—38. https://doi.org/10.1038/198036a0

    Article  CAS  PubMed  Google Scholar 

  43. Callan, H.G., The nature of lampbrush chromosomes, Int. Rev. Cytol., 1963, vol. 15, pp. 1—34.

    Article  CAS  PubMed  Google Scholar 

  44. Miller, O.L., Fine structure of lampbrush chromosomes, Natl. Cancer Inst. Monogr., 1965, vol. 18, pp. 79—99.

    PubMed  Google Scholar 

  45. Miller, O.L., The nucleolus, chromosomes, and visualization of genetic activity, J. Cell Biol., 1981, vol. 91, pp. 15—27. https://doi.org/10.1083/jcb.91.3.15s

    Article  CAS  PubMed Central  Google Scholar 

  46. Ullerich, F.H., DNS-Gehalt und Chromosomenstruktur bei Amphibien, Chromosoma, 1970, vol. 30, pp. 1—37. https://doi.org/10.1007/BF00293907

    Article  CAS  PubMed  Google Scholar 

  47. Krasikova, A., Barbero, J.L., and Gaginskaya, E., Cohesion proteins are present in centromere protein bodies associated with avian lampbrush chromosomes, Chromosome Res., 2005, vol. 13, pp. 675—685. https://doi.org/10.1007/s10577-005-1005-6

    Article  CAS  PubMed  Google Scholar 

  48. Austin, C., Novikova, N., Guacci, V., and Bellini, M., Lampbrush chromosomes enable study of cohesin dynamics, Chromosome Res., 2009, vol. 17, pp. 165—184. https://doi.org/10.1007/s10577-008-9015-9

    Article  CAS  PubMed  Google Scholar 

  49. Krasikova, A., Daks, A., Zlotina, A., and Gaginskaya, E., Polymorphic heterochromatic segments in Japanese quail microchromosomes, Cytogenet. Genome Res., 2009, vol. 126, nos. 1—2, pp. 148—155. https://doi.org/10.1159/000245914

    Article  CAS  PubMed  Google Scholar 

  50. Morgan, G.T., Jones, P., and Bellini, M., Association of modified cytosines and the methylated DNA-binding protein MeCP2 with distinctive structural domains of lampbrush chromatin, Chromosome Res., 2012, vol. 20, pp. 925—942. https://doi.org/10.1007/s10577-012-9324-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Angelier, N., Paintrand, M., Lavaud, A., and Lechaire, J.P., Scanning electron microscopy of amphibian lampbrush chromosomes, Chromosoma, 1984, vol. 9, no. 4, pp. 243—253. https://doi.org/10.1007/bf00292471

    Article  Google Scholar 

  52. Sommerville, J., Baird, J., and Turner, B.M., Histone H4 acetylation and transcription in amphibian chromatin, J. Cell Biol., 1993, vol. 120, pp. 277—290. https://doi.org/10.1083/jcb.120.2.277

    Article  CAS  PubMed  Google Scholar 

  53. Beenders, B., Watrin, E., Legagneux, V., et al., Distribution of XCAP-E and XCAP-D2 in the Xenopus oocyte nucleus, Chromosome Res., 2003, vol. 11, pp. 549—564. https://doi.org/10.1023/a:1024999316867

    Article  CAS  PubMed  Google Scholar 

  54. Zlotina, A., Maslova, A., Pavlova, O., et al., New insights into chromomere organization provided by lampbrush chromosome microdissection and high-throughput sequencing, Front. Genet., 2020, vol. 11, p. 57. https://doi.org/10.3389/fgene.2020.00057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Vlad, M. and Macgregor, H.C., Chromomere number and its genetic significance in lampbrush chromosomes, Chromosoma, 1975, vol. 50, pp. 327—347. https://doi.org/10.1007/BF00327073

    Article  CAS  PubMed  Google Scholar 

  56. Macgregor, H. and Klosterman, L., Observations on the cytology of Bipes (Amphisbaenia) with special reference to its lampbrush chromosomes, Chromosoma, 1979, vol. 72, pp. 67—87. https://doi.org/10.1007/BF00286430

    Article  Google Scholar 

  57. Gregory, T.R., Nicol, J.A., Tamm, H., et al., Eukaryotic genome size databases, Nucleic Acids Res., 2007, p. 35. https://doi.org/10.1093/nar/gkl828

  58. Khutinaeva, M.A., Kropotova, E.V., and Gaginskaya, E.R., The characteristics of the morphofunctional organization of the lampbrush chromosomes from the oocytes of the rock dove, Tsitologiya, 1989, vol. 31, no. 10, pp. 1185—1191.

    CAS  Google Scholar 

  59. Alberts, B., Johnson, A., Lewis, J., and Raff, M., Molecular Biology of the Cell, New York: Garland Sci., 2002, 4th ed.

    Google Scholar 

  60. Gall, J.G. and Murphy, C., Assembly of lampbrush chromosomes from sperm chromatin, Mol. Biol. Cell, 1998, vol. 9, pp. 733—747. https://doi.org/10.1091/mbc.9.4.733

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Solovei, I., Macgregor, H., and Gaginskaya, E., Single stranded nucleic acid binding structures on chicken lampbrush chromosomes, J. Cell Sci., 1995, vol. 108, pp. 1391—1396.

    Article  CAS  PubMed  Google Scholar 

  62. Solovei, I., Macgregor, H., and Gaginskaya, E., Specifically terminal clusters of telomere DNA sequences are transcribed from C-rich strand on chicken lampbrush chromosomes, Chromosome Today, 1995, vol. 11, pp. 147—156.

    Google Scholar 

  63. Solovei, I.V., Joffe, B.I., Gaginskaya, E.R., and Macgregor, H.C., Transcription on lampbrush chromosomes of a centromerically localized highly repeated DNA in pigeon (Columba) relates to sequence arrangement, Chromosome Res., 1996, vol. 4, pp. 588—603. https://doi.org/10.1007/BF02261722

    Article  CAS  PubMed  Google Scholar 

  64. Myakoshina, Yu.A. and Rodionov, A.V., Meiotic chromosomes of turkey Meleagris gallopavo (Galliformes: Meleagrididae) at the stage of lampbrush chromosomes, Genetika (Moscow), 1994, vol. 30, no. 5, pp. 649—656.

    Google Scholar 

  65. Angelier, N., Bonnanfant-Jais, M.-L., Herberts, C., et al., Chromosomes of amphibian oocytes as a model for gene expression: significance of lampbrush loops, Int. J. Dev. Biol., 1990, vol. 34, pp. 69—80.

    CAS  PubMed  Google Scholar 

  66. Kulikova, T., Chervyakova, D., Zlotina, A., et al., Giant poly(A)-rich RNP aggregates form at terminal regions of avian lampbrush chromosomes, Chromosoma, 2016, vol. 125, no. 4, pp. 709—724. https://doi.org/10.1007/s00412-015-0563-4

    Article  CAS  PubMed  Google Scholar 

  67. Scheer, U., Franke, W.W., Trendelenburg, M.F., and Spring, H., Classification of loops of lampbrush chromosomes according to the arrangement of transcriptional complexes, J. Cell Sci., 1976, vol. 22, pp. 503—519.

    Article  CAS  PubMed  Google Scholar 

  68. Scheer, U., Spring, H., and Trendelenburg, M.F., Organization of transcriptionally active chromatin in lampbrush chromosome loop, in The Cell Nucleus, Bush, H., Ed., New York: Academic, 1979, vol. VII, pp. 3—47.

    Google Scholar 

  69. Miller, O.L. and Beatty, B.R., Portrait of a gene, J. Cell Physiol., 1969, vol. 74, suppl. 1, pp. 225—232.

    Article  CAS  Google Scholar 

  70. Hill, R.S., A quantitative electron-microscope analysis of chromatin from Xenopus laevis lampbrush chromosomes, J. Cell Sci., 1979, vol. 40, pp. 145—169.

    Article  CAS  PubMed  Google Scholar 

  71. Gaginskaya, E.R. and Tsvetkov, A.G., Electron microscopic study of chromatin structure in dispersed lampbrush chromosomes of the chicken, Tsitologiya, 1988, vol. 30, no. 2, pp. 142—150.

    Google Scholar 

  72. Patel, S., Novikova, N., Beenders, B., et al., Live images of RNA polymerase II transcription units, Chromosome Res., 2008, vol. 16, pp. 223—232. https://doi.org/10.1007/s10577-007-1189-z

    Article  CAS  PubMed  Google Scholar 

  73. Gall, J.G. and Wu, Z.A., Examining the contents of isolated Xenopus germinal vesicles, Methods, 2010, vol. 51, pp. 45—51. https://doi.org/10.1016/j.ymeth.2009.12.010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Leidescher, S., Nübler, J., Feodorova, Y., et al., Spatial organization of transcribed eukaryotic genes, bioRxiv, 2020. 05.20.106591. https://doi.org/10.1101/2020.05.20.106591

  75. Diaz, M.O., Barsacchi-Pilone, G., Mahon, K.A., and Gall, J.G., Transcripts from both strands of a satellite DNA occur on lampbrush chromosome loops of the newt Notophthalmus, Cell, 1981, vol. 24, pp. 649—659. https://doi.org/10.1016/0092-8674(81)90091-x

    Article  CAS  PubMed  Google Scholar 

  76. Diaz, M.O. and Gall, J.G., Giant readthrough transcription units at the histone loci on lampbrush chromosomes of the newt Notophthalmus, Chromosoma, 1985, vol. 92, pp. 243—253. https://doi.org/10.1007/BF00329807

    Article  CAS  PubMed  Google Scholar 

  77. Morgan, G.T., Macgregor, H.C., and Colman, A., Multiple ribosomal gene sites revealed by in situ hybridization of Xenopus rDNA to Triturus lampbrush chromosomes, Chromosoma, 1980, vol. 80, pp. 309—330. https://doi.org/10.1007/BF00292687

    Article  CAS  PubMed  Google Scholar 

  78. Macgregor, H.C., Varley, J.M., and Morgan, G.T., The transcription of satellite and ribosomal DNA sequences on lampbrush chromosomes of crested newts, in International Cell Biology 1980—1981, Berlin: Springer-Verlag, 1981, pp. 33—46.

    Google Scholar 

  79. Pukkila, P.J., Identification of the lampbrush loops which transcribe 5S ribosomal RNA in Notophthalmus (Triturus) viridescens, Chromosoma, 1975, vol. 53, pp. 71—89. https://doi.org/10.1007/BF00329391

    Article  CAS  PubMed  Google Scholar 

  80. Barsacchi-Pilone, G., Nardi, I., Andronico, F., et al., Chromosome location of the ribosomal RNA genes in Triturus vulgaris meridionalis (Amphibia, Urodela): I. Localization of the DNA sequences complementary to 5S ribosomal RNA on mitotic and lampbrush chromosomes, Chromosoma, 1977, vol. 63, pp. 127—134.

    Article  Google Scholar 

  81. Callan, H.G., Gall, J.G., and Berg, C.A., The lampbrush chromosomes of Xenopus laevis: preparation, identification, and distribution of 5S DNA sequences, Chromosoma, 1987, vol. 95, pp. 236—250. https://doi.org/10.1007/BF00294780

    Article  CAS  PubMed  Google Scholar 

  82. Callan, H.C., Old, R.W., and Gross, K.W., Problems exposed by the results of in situ hybridization to lampbrush chromosomes, Eur. J. Cell Biol., 1980, vol. 22, p. 21.

    Google Scholar 

  83. Gall, J.G., Stephenson, E.C., Erba, H.P., et al., Histone genes are located at the sphere loci of newt lampbrush chromosomes, Chromosoma, 1981, vol. 84, pp. 159—171. https://doi.org/10.1007/BF00399128

    Article  CAS  PubMed  Google Scholar 

  84. Weber, T., Schmidt, E., and Scheer, U., Mapping of transcription units on Xenopus laevis lampbrush chromosomes by in situ hybridization with biotin-labeled cDNA probes, Eur. J. Cell Biol., 1989, vol. 50, pp. 144—153.

    CAS  PubMed  Google Scholar 

  85. Billoud, B., Rodroguez-Martin, M.L., Berard, L., et al., Constitutive expression of a somatic heat-inducible hsp70 gene during amphibian oogenesis, Development, 1993, vol. 119, pp. 921—923.

    Article  CAS  PubMed  Google Scholar 

  86. Stephenson, E.C., Erba, H.P., and Gall, J.G., Histone gene clusters of the newt Notophthalmus are separated by long tracts of satellite DNA, Cell, 1981, vol. 24, pp. 639—647. https://doi.org/10.1016/0092-8674(81)90090-8

    Article  CAS  PubMed  Google Scholar 

  87. Epstein, L.M., Mahon, K.A., and Gall, J.G., Transcription of a satellite DNA in the newt, J. Cell Biol., 1986, vol. 103, pp. 1137—1144. https://doi.org/10.1083/jcb.103.4.1137

    Article  CAS  PubMed  Google Scholar 

  88. Epstein, L.M. and Gall, J.G., Self-cleaving transcripts of satellite DNA from the newt, Cell, 1987, vol. 48, pp. 535—543. https://doi.org/10.1016/0092-8674(87)90204-2

    Article  CAS  PubMed  Google Scholar 

  89. Barsacchi-Pilone, G., Batistoni, R., Andronico, F., et al., Heterochromatic DNA in Triturus (Amphibia, Urodela): I. A satellite DNA component of the pericentric C-bands, Chromosoma, 1986, vol. 93, no. 5, pp. 435—446. https://doi.org/10.1007/BF00285826

    Article  CAS  PubMed  Google Scholar 

  90. Baldwin, L. and Macgregor, H.C., Centromeric satellite DNA in the newt Triturus cristatus karelinii and related species: its distribution and transcription on lampbrush chromosomes, Chromosoma, 1985, vol. 92, pp. 100—107. https://doi.org/10.1007/BF00328461

    Article  CAS  PubMed  Google Scholar 

  91. Jamrich, M., Warrior, R., Steele, R., and Gall, J.G., Transcription of repetitive sequences on Xenopus lampbrush chromosomes, Proc. Natl. Acad. Sci. U.S.A., 1983, vol. 80, pp. 3364—3367. https://doi.org/10.1073/pnas.80.11.3364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Wu, Z., Murphy, C., and Gall, J.G., A transcribed satellite DNA from the bullfrog Rana catesbeiana, Chromosoma, 1986, vol. 93, pp. 291—297. https://doi.org/10.1007/BF00327586

    Article  CAS  PubMed  Google Scholar 

  93. Hori, T., Susuki, Y., Solovei, I., et al., Characterization of DNA sequences constituting the terminal heterochromatin of the chicken Z chromosome, Chromosome Res., 1996, vol. 4, pp. 411—426. https://doi.org/10.1007/BF02265048

    Article  CAS  PubMed  Google Scholar 

  94. Teranishi, M., Shimada, Y., Hori, T., et al., Transcripts of the MHM region of the chicken Z chromosome accumulate as non-coding RNA in the nucleus of female cells adjacent to the DMRT locus, Chromosome Res., 2001, vol. 9, pp. 147—165. https://doi.org/10.1023/A:1009235120741

    Article  CAS  PubMed  Google Scholar 

  95. Krasikova, A., Derjusheva, S., Galkina, S., et al., On the positions of centromeres in chicken lampbrush chromosomes, Chromosome Res., 2006, vol. 14, pp. 777—789. https://doi.org/10.1007/s10577-006-1085-y

    Article  CAS  PubMed  Google Scholar 

  96. Deryusheva, S., Krasikova, A., Kulikova, T., and Gaginskaya, E., Tandem 41-bp repeats in chicken and Japanese quail genomes: FISH mapping and transcription on lampbrush chromosomes, Chromosoma, 2007, vol. 116, pp. 519—530. https://doi.org/10.1007/s00412-007-0117-5

    Article  CAS  PubMed  Google Scholar 

  97. Krasikova, A.V., Vasilevskaya, E.V., and Gaginskaya, E.R., Chicken lampbrush chromosomes: transcription of tandemly repetitive DNA sequences, Russ. J. Genet., 2010, vol. 46, no. 10, pp. 1173—1177. https://doi.org/10.1134/S1022795410100078

    Article  CAS  Google Scholar 

  98. Kulak, M., Komissarov, A., Dyomin, A., et al., Description of new tandem repeats in the genome of Japanese quail, Mol. Cytogenet., 2019, vol. 12, no. 30, p. 63. https://doi.org/10.1186/s13039-019-0439-z

    Article  Google Scholar 

  99. Anderson, D.M. and Smith, L.D., Patterns of synthesis and accumulation of heterogeneous RNA in lampbrush stage oocytes of Xenopus laevis (Daudin), Dev. Biol., 1978, vol. 67, pp. 274—285. https://doi.org/10.1016/0012-1606(78)90199-9

    Article  CAS  PubMed  Google Scholar 

  100. Richter, J.D., Smith, L.D., Anderson, D.M., and Davidson, E.H., Interspersed poly(A) RNAs of amphibian oocytes are not translatable, J. Mol. Biol., 1984, vol. 173, pp. 227—241. https://doi.org/10.1016/0022-2836(84)90191-8

    Article  CAS  PubMed  Google Scholar 

  101. Zagris, N., Kalantzis, K., and Guialis, A., Activation of embryonic genome in chick, Zygote, 1998, vol. 6, pp. 227—231. https://doi.org/10.1017/s0967199498000161

    Article  CAS  PubMed  Google Scholar 

  102. Olszanska, B. and Stepinska, U., Molecular aspects of avian oogenesis and fertilization, Int. J. Dev. Biol., 2008, vol. 52, pp. 187—194. https://doi.org/10.1387/ijdb.072329ob

    Article  CAS  PubMed  Google Scholar 

  103. Gardner, E.J., Nizami, Z.F., Talbot, C.C., and Gall, J.G., Stable intronic sequence RNA (sisRNA), a new class of noncoding RNA from the oocyte nucleus of Xenopus tropicalis, Genes Dev., 2012, vol. 26, pp. 2550—2559. https://doi.org/10.1101/gad.202184.112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Simeoni, I., Gilchrist, M.J., Garrett, N., et al., Widespread transcription in an amphibian oocyte relates to its reprogramming activity on transplanted somatic nuclei, Stem Cells Dev., 2012, vol. 21, pp. 181—190. https://doi.org/10.1089/scd.2011.0162

    Article  PubMed  Google Scholar 

  105. Malewska, A. and Olszanska, B., Accumulation and localisation of maternal RNA in oocytes of Japanese quail, Zygote, 1999, vol. 7, pp. 51—59. https://doi.org/10.1017/s0967199499000398

    Article  CAS  PubMed  Google Scholar 

  106. Bachvarova, R., Davidson, E.H., Allfrey, V.G., and Mirsky, A.E., Activation of RNA synthesis associated with gastrulation, Proc. Natl. Acad. Sci. U.S.A., 1966, vol. 55, no. 2, pp. 358—365. https://doi.org/10.1073/pnas.55.2.358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Talhouarne, G.J.S. and Gall, J.G., Lariat intronic RNAs in the cytoplasm of Xenopus tropicalis oocytes, RNA, 2014, vol. 20, pp. 1476—1487. https://doi.org/10.1261/rna.045781.114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Callan, H.G. and Lloyd, L., Lampbrush chromosomes of crested newts Triturus cristatus (Laurenti), Philos. Transact. R. Soc., B, 1960, vol. 702, pp. 135—219. https://royalsocietypublishing.org/doi/pdf/10.1098/ rstb.1960.0007

  109. Gall, J.G. and Callan, H.G., H3-uridine incorporation in lampbrush chromosomes, Proc. Natl. Acad. Sci. U.S.A., 1962, vol. 48, pp. 562—570.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Snow, M.H.L. and Callan, H.G., Evidence for a polarized movement of the lateral loops of newt lampbrush chromosomes during oogenesis, J. Cell Sci., 1969, vol. 5, pp. 1—25.

    Article  CAS  PubMed  Google Scholar 

  111. Mancino, G. and Barsacchi, G., Le mappe dei cromosomi lampbrushî di Triturus (Anfibi Urodeli): I. Triturus alpestris apuanus, Caryologia, 1965, vol. 18, pp. 637—665.

    Article  Google Scholar 

  112. Mancino, G. and Barsacchi, G., Le mappe dei cromosomi lampbrushî di Triturus (Anfibi Urodeli): II. Triturus helveticus helveticus, Riv. Biol., (Perugia), 1966, vol. 59, pp. 311—351.

  113. Mancino, G. and Barsacchi, G., The maps of the lampbrush chromosomes of Triturus (Amphibia, Urodela). III. Triturus italicus, Ann. Embryol. Morphogen., 1969, vol. 2, pp. 355—377.

    Google Scholar 

  114. Barsacchi, G., Bussotti, L., and Mancino, G., The maps of the lampbrush chromosomes of Triturus (Amphibia, Urodela): IV. Triturus vulgaris meridonalis, Chromosoma, 1970, vol. 31, pp. 255—279. https://doi.org/10.1007/BF00321223

    Article  CAS  PubMed  Google Scholar 

  115. Callan, H.G. and Lloyd, L., Working maps of the lampbrush chromosomes of Amphibia, in Handbook of Genetics, vol. 4: Vertebrates of Genetic Interest, King, R.C., Ed., New York: Plenum, 1975, pp. 57—77.

  116. Solovei, I., Gaginskaya, E., Hutchison, N., and Macgregor, H.C., Avian sex chromosomes in the lampbrush form: the ZW lampbrush bivalents from six species of bird, Chromosome Res., 1993, vol. 1, pp. 153—166. https://doi.org/10.1007/BF00710769

    Article  CAS  PubMed  Google Scholar 

  117. Rodionov, A.V., Lukina, N.A., Galkina, S.A., et al., Crossing over in chicken oogenesis: cytological and chiasma-based genetic maps of chicken lampbrush chromosome 1, J. Hered., 2002, vol. 93, pp. 125—129. https://doi.org/10.1093/jhered/93.2.125

    Article  CAS  PubMed  Google Scholar 

  118. Vishnyakova, N.M., Lacroix, J.C., and Rodionov, A.V., Cytogenetic maps of lampbrush chromosomes of newts of the genus Pleurodeles: an algorithm of lampbrush chromosome identification in Pleurodeles waltl by immunocytochemical staining of landmark loops with polyclonal anti-RO52 antisera, Russ. J. Genet., 2004, vol. 40, no. 5, pp. 491—499. https://doi.org/10.1023/B:RUGE.0000029150.41324.27

    Article  CAS  Google Scholar 

  119. Penrad-Mobayed, M., El Jamil, A., Kanhoush, R., and Perrin, C., Working map of the lampbrush chromosomes or Xenopus tropicalis: a new tool for cytogenetic analysis, Dev. Dyn., 2009, vol. 238, pp. 1492—1501. https://doi.org/10.1002/dvdy.21930

    Article  CAS  PubMed  Google Scholar 

  120. Daks, A.A., Deryusheva, S.E., Krasikova, A.V., et al., Lampbrush chromosomes of the Japanese quail (Coturnix coturnix japonica): a new version of cytogenetic maps, Russ. J. Genet., 2010, vol. 46, no. 10, pp. 1178—1181. https://doi.org/10.1134/S102279541010008X

    Article  CAS  Google Scholar 

  121. Dedukh, D., Mazepa, G., Shabanov, D., et al., Cytological maps of lampbrush chromosomes of European water frogs (Pelophylax esculentus complex) from the Eastern Ukraine, BMC Genet., 2013, vol. 14, p. 26. https://doi.org/10.1186/1471-2156-14-26

    Article  PubMed  PubMed Central  Google Scholar 

  122. Bintu B., Mateo L.J., Su J.-H. et al. Super-resolution chromatin tracing reveals domains and cooperative interactions in single cells, Science, 2018, vol. 362, p. eaau1783. https://doi.org/10.1126/science.aau1783

  123. Callan, H.G., The organization of genetic units in chromosomes, J. Cell Sci., 1967, vol. 2, pp. 1—7.

    Article  CAS  PubMed  Google Scholar 

  124. Whitehouse, H.L.K., A cycloid model for the chromosome, J. Cell Sci., 1967, vol. 2, pp. 9—22.

    Article  CAS  PubMed  Google Scholar 

  125. Callan, H.G., Lampbrush chromosomes, Proc. R. Soc. London, B, 1982, vol. 214, pp. 417—448.

    CAS  Google Scholar 

  126. Lee, M.T., Bonneau, A.R., and Giraldez, A.J., Zygotic genome activation during the maternal-to-zygotic transition, Annu. Rev. Cell Dev. Biol., 2014, vol. 30, pp. 581—613. https://doi.org/10.1146/annurev-cellbio-100913-013027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Gall, J.G., Problems of structure and function in the amphibian oocyte nucleus, Symp. Soc. Exp. Biol., 1955, vol. 9, pp. 358—370.

    Google Scholar 

  128. Davidson, E.H. and Hough, B.R., Genetic information in oocyte RNA, J. Mol. Biol., 1971, vol. 56, no. 3, pp. 491—506.

    Article  CAS  PubMed  Google Scholar 

  129. Davidson, E.H., Gene Activity in Early Development, New York: Academic, 1972.

    Google Scholar 

  130. Davidson, E.H., Crippa, M., Kramer, F.R., and Mirsky, A.E., Genomic function during the lampbrush chromosome stage of amphibian oogenesis, Proc. Natl. Acad. Sci. U.S.A., 1966, vol. 56, no. 3, pp. 856—863. https://doi.org/10.1073/pnas.56.3.856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Thomas, J.O., Glowacka, S.K., and Szer, W., Structure of complexes between a major protein of heterogeneous nuclear ribonucleoprotein particles and polyribonucleotides, J. Mol. Biol., 1983, vol. 171, pp. 439—455. https://doi.org/10.1016/0022-2836(83)90039-6

    Article  CAS  PubMed  Google Scholar 

  132. Calzone, F.J., Lee, J.J., Le, N., Britten, R.J., and Davidson, E.H., A long, nontranslatable poly(A) RNA stored in the egg of the sea urchin Strongylocentrotus purpuratus, Genes Dev., 1988, vol. 2, no. 3, pp. 305—318. https://doi.org/10.1101/gad.2.3.305

    Article  CAS  PubMed  Google Scholar 

  133. Davidson, E.H., Gene Activity in Early Development, London; New York: Academic, 1976, 2nd ed.

    Google Scholar 

  134. Trofimova, I. and Krasikova, A., Transcription of highly repetitive tandemly organized DNA in amphibians and birds: a historical overview and modern concepts, RNA Biol., 2016, vol. 13, pp. 1246—1257. https://doi.org/10.1080/15476286.2016.1240142

    Article  PubMed  PubMed Central  Google Scholar 

  135. Gruzova, M.N., Nucleus in oogenesis (structural and functional aspects), in Sovremennye problemy oogeneza (Modern Challenges in Oogenesis), Moscow: Nauka, 1977, pp. 51—98.

  136. Neifakh, A.A. and Timofeeva, M.Ya., Molekulyarnaya biologiya protsessov razvitiya (Molecular Biology of Developmental Processes), Moscow: Nauka, 1977.

  137. Kafiani, K.A. and Kostomarova, A.A., Informatsionnye makromolekuly v rannem razvitii zhivotnykh (Informational Macromolecules in Early Animal Development), Moscow: Nauka, 1978.

  138. Gilbert, F., Developmental Biology, Sunderland: Sinauer Associates, 2000.

    Google Scholar 

  139. Koshel, E., Galkina, S., Saifitdinova, A., et al., Ribosomal RNA gene functioning in avian oogenesis, Cell Tissue Res., 2016, vol. 366, pp. 533—542. https://doi.org/10.1007/s00441-016-2444-4

    Article  CAS  PubMed  Google Scholar 

  140. Varley, J.M., Macgregor, H.C., and Erba, H.P., Satellite DNA is transcribed on lampbrush chromosomes, Nature, 1980, vol. 283, pp. 686—688. https://doi.org/10.1038/283686a0

    Article  CAS  PubMed  Google Scholar 

  141. Varley, J.M., Macgregor, H.C., Nardi, I., et al., Transcription of highly repeated DNA sequences during the lampbrush stage in Triturus cristatus carnifex, Chromosoma, 1980, vol. 80, pp. 289—307. https://doi.org/10.1007/BF00292686

    Article  CAS  PubMed  Google Scholar 

  142. Bromley, S.E. and Gall, J.G., Transcription of the histone loci on lampbrush chromosomes of the newt Notophthalmus viridescens, Chromosoma, 1987, vol. 95, no. 6, pp. 396—402. https://doi.org/10.1007/BF00333990

    Article  CAS  PubMed  Google Scholar 

  143. Cavalier-Smith, T., Nuclear volume control by nucleoskeletal DNA, selection for cell volume and cell growth rate, and the solution of the DNA C-value paradox, J. Cell Sci., 1978, vol. 34, pp. 247—278.

    Article  CAS  PubMed  Google Scholar 

  144. León, P.E., Function of lampbrush chromosomes: a hypothesis, J. Theor. Biol., 1975, vol. 55, pp. 481—490. https://doi.org/10.1016/s0022-5193(75)80095-6

    Article  PubMed  Google Scholar 

  145. Morgan, H.D., Santos, F., Green, K., et al., Epigenetic reprogramming in mammals, Hum. Mol. Genet., 2005, vol. 14, pp. R47—R58. https://doi.org/10.1093/hmg/ddi114

    Article  CAS  PubMed  Google Scholar 

  146. Cantone, I. and Fisher, A.G., Epigenetic programming and reprogramming during development, Nat. Struct. Mol. Biol., 2013, vol. 20, pp. 282—289. https://doi.org/10.1038/nsmb.2489

    Article  CAS  PubMed  Google Scholar 

  147. Jiang, L., Zhang, J., Wang, J.-J., et al., Sperm, but not oocyte, DNA methylome is inherited by zebrafish early embryos, Cell, 2013, vol. 153, pp. 773—784. https://doi.org/10.1016/j.cell.2013.04.041

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Tikhonov, A.V., Efimova, O.A., Pendina, A.A., and Baranov, V.S., Epigenetic reprogramming in human gametes and preimplantation embryos, Med. Genet., 2017, vol. 16, no. 5, pp. 17—25.

    Google Scholar 

  149. Liu, J.-L. and Gall, J.G., Induction of human lampbrush chromosomes, Chromosome Res., 2012, vol. 20, pp. 971—978. https://doi.org/10.1007/s10577-012-9331-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Halley-Stott, R.P., Pasque, V., Astrand, C., et al., Mammalian nuclear transplantation to germinal vesicle stage Xenopus oocytes—a method for quantitative transcriptional reprogramming, Methods, 2010, vol. 51, no. 1, pp. 56—65. https://doi.org/10.1016/j.ymeth.2010.01.035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  151. Miyamoto, K., Nguyen, K.T., Allen, G.E., et al., Chromatin accessibility impacts transcriptional reprogramming in oocytes, Cell Rep., 2018, vol. 24, pp. 304—311. https://doi.org/10.1016/j.celrep.2018.06.030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  152. Saifitdinova, A., Breakthrough in understanding the phenomenon of lampbrush chromosomes, // Eds Galkina S, Vishnevskaya M in 23rd Int. Colloquium on Animal Cytogenetics and Genomics (23 ICACG), June 9–12, 2018, St. Petersburg, Russia, Galkina, S. and Vishnevskaya, M., Eds., Comp. Cytogenet., 2018, vol. 12, pp. 299–360. https://doi.org/10.3897/CompCytogen.v12i3.27748

  153. Saifitdinova, A.F., Galkina, S.A., Koshel’, E.I., and Gaginskaya, E.R., The role of repetitive sequences in the evolution of sex chromosomes in birds, Tsitologiya, 2016, vol. 58, no. 5, pp. 393—398.

    CAS  Google Scholar 

  154. Russell, S.J. and LaMarre, J., Transposons and the PIWI pathway: genome defense in gametes and embryos, Reproduction, 2018, vol. 156, pp. R111—R124. https://doi.org/10.1530/REP-18-0218

    Article  CAS  PubMed  Google Scholar 

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Funding

This study was supported by the Russian Foundation for Basic Research (grant no. 19-14-50096).

The present review was prepared using the infrastructure of the Research Resource Center Chromas Core Facility of the St. Petersburg State University.

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Authors and Affiliations

  1. Herzen State Pedagogical University of Russia, 191186, St. Petersburg, Russia

    A. F. Saifitdinova

  2. International Center for Reproductive Medicine, 197350, St. Petersburg, Russia

    A. F. Saifitdinova

  3. Saint Petersburg State University, 199034, St. Petersburg, Russia

    S. A. Galkina & E. R. Gaginskaya

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  1. A. F. Saifitdinova
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  2. S. A. Galkina
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  3. E. R. Gaginskaya
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Correspondence to A. F. Saifitdinova.

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Translated by N. Maleeva

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Saifitdinova, A.F., Galkina, S.A. & Gaginskaya, E.R. The Evolution of Concepts about the Biological Role of Lampbrush Chromosomes. Russ J Genet 57, 499–514 (2021). https://doi.org/10.1134/S1022795421050100

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