Molecular genetics of maternally-controlled cell divisions

English version

Autoři: Elliott W. Abrams ^aff001; Ricardo Fuentes ^aff001; Florence L. Marlow ^aff001; Manami Kobayashi ^aff001; Hong Zhang ^aff001; Sumei Lu ^aff001; Lee Kapp ^aff001; Shai R. Joseph ^aff003; Amy Kugath ^aff001; Tripti Gupta ^aff001; Virginia Lemon ^aff001; Greg Runke ^aff001; Amanda A. Amodeo ^aff004; Nadine L. Vastenhouw ^aff003; Mary C. Mullins ^aff001
Působiště autorů: Department of Cell and Developmental Biology, University of Pennsylvania Perelman School of Medicine, Philadelphia, Pennsylvania, United States of America ^aff001; Department of Biology, Purchase College, The State University of New York, Purchase, New York, United States of America ^aff002; Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany ^aff003; Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton, New Jersey, United States of America ^aff004
Vyšlo v časopise: Molecular genetics of maternally-controlled cell divisions. PLoS Genet 16(4): e1008652. doi:10.1371/journal.pgen.1008652
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008652

Souhrn

Forward genetic screens remain at the forefront of biology as an unbiased approach for discovering and elucidating gene function at the organismal and molecular level. Past mutagenesis screens targeting maternal-effect genes identified a broad spectrum of phenotypes ranging from defects in oocyte development to embryonic patterning. However, earlier vertebrate screens did not reach saturation, anticipated classes of phenotypes were not uncovered, and technological limitations made it difficult to pinpoint the causal gene. In this study, we performed a chemically-induced maternal-effect mutagenesis screen in zebrafish and identified eight distinct mutants specifically affecting the cleavage stage of development and one cleavage stage mutant that is also male sterile. The cleavage-stage phenotypes fell into three separate classes: developmental arrest proximal to the mid blastula transition (MBT), irregular cleavage, and cytokinesis mutants. We mapped each mutation to narrow genetic intervals and determined the molecular basis for two of the developmental arrest mutants, and a mutation causing male sterility and a maternal-effect mutant phenotype. One developmental arrest mutant gene encodes a maternal specific Stem Loop Binding Protein, which is required to maintain maternal histone levels. The other developmental arrest mutant encodes a maternal-specific subunit of the Minichromosome Maintenance Protein Complex, which is essential for maintaining normal chromosome integrity in the early blastomeres. Finally, we identify a hypomorphic allele of Polo-like kinase-1 (Plk-1), which results in a male sterile and maternal-effect phenotype. Collectively, these mutants expand our molecular-genetic understanding of the maternal regulation of early embryonic development in vertebrates.

Klíčová slova:

Cell cycle and cell division – DNA-binding proteins – Embryos – Histones – Chromosome mapping – Messenger RNA – Phenotypes – Zebrafish

Zdroje

1. Tadros W, Lipshitz HD. The maternal-to-zygotic transition: a play in two acts. Development. 2009;136(18):3033–42. Epub 2009/08/25. doi: 10.1242/dev.033183 19700615.

2. Vastenhouw NL, Cao WX, Lipshitz HD. The maternal-to-zygotic transition revisited. Development. 2019;146(11). Epub 2019/06/14. doi: 10.1242/dev.161471 31189646.

3. Kane DA, Kimmel CB. The zebrafish midblastula transition. Development. 1993;119(2):447–56. Epub 1993/10/01. 8287796.

4. Wong CC, Loewke KE, Bossert NL, Behr B, De Jonge CJ, Baer TM, et al. Non-invasive imaging of human embryos before embryonic genome activation predicts development to the blastocyst stage. Nat Biotechnol. 2010;28(10):1115–21. Epub 2010/10/05. doi: 10.1038/nbt.1686 20890283.

5. Telford NA, Watson AJ, Schultz GA. Transition from maternal to embryonic control in early mammalian development: a comparison of several species. Mol Reprod Dev. 1990;26(1):90–100. Epub 1990/05/01. doi: 10.1002/mrd.1080260113 2189447.

6. Newport J, Kirschner M. A major developmental transition in early Xenopus embryos: I. characterization and timing of cellular changes at the midblastula stage. Cell. 1982;30(3):675–86. Epub 1982/10/01. doi: 10.1016/0092-8674(82)90272-0 6183003.

7. Driever W, Solnica-Krezel L, Schier AF, Neuhauss SC, Malicki J, Stemple DL, et al. A genetic screen for mutations affecting embryogenesis in zebrafish. Development. 1996;123 : 37–46. Epub 1996/12/01. 9007227.

8. Haffter P, Granato M, Brand M, Mullins MC, Hammerschmidt M, Kane DA, et al. The identification of genes with unique and essential functions in the development of the zebrafish, Danio rerio. Development. 1996;123 : 1–36. Epub 1996/12/01. 9007226.

9. Mullins MC, Hammerschmidt M, Haffter P, Nusslein-Volhard C. Large-scale mutagenesis in the zebrafish: in search of genes controlling development in a vertebrate. Curr Biol. 1994;4(3):189–202. Epub 1994/03/01. doi: 10.1016/s0960-9822(00)00048-8 7922324.

10. Dosch R, Wagner DS, Mintzer KA, Runke G, Wiemelt AP, Mullins MC. Maternal control of vertebrate development before the midblastula transition: mutants from the zebrafish I. Dev Cell. 2004;6(6):771–80. Epub 2004/06/05. doi: 10.1016/j.devcel.2004.05.002 15177026.

11. Kishimoto Y, Koshida S, Furutani-Seiki M, Kondoh H. Zebrafish maternal-effect mutations causing cytokinesis defect without affecting mitosis or equatorial vasa deposition. Mech Dev. 2004;121(1):79–89. Epub 2004/01/07. doi: 10.1016/j.mod.2003.10.001 14706702.

12. Pelegri F, Dekens MP, Schulte-Merker S, Maischein HM, Weiler C, Nusslein-Volhard C. Identification of recessive maternal-effect mutations in the zebrafish using a gynogenesis-based method. Dev Dyn. 2004;231(2):324–35. Epub 2004/09/15. doi: 10.1002/dvdy.20145 15366009.

13. Wagner DS, Dosch R, Mintzer KA, Wiemelt AP, Mullins MC. Maternal control of development at the midblastula transition and beyond: mutants from the zebrafish II. Dev Cell. 2004;6(6):781–90. Epub 2004/06/05. doi: 10.1016/j.devcel.2004.04.001 15177027.

14. Gupta T, Marlow FL, Ferriola D, Mackiewicz K, Dapprich J, Monos D, et al. Microtubule actin crosslinking factor 1 regulates the Balbiani body and animal-vegetal polarity of the zebrafish oocyte. PLoS Genet. 2010;6(8):e1001073. Epub 2010/09/03. doi: 10.1371/journal.pgen.1001073 20808893; PubMed Central PMCID: PMC2924321 haplotype-specific extraction, and another author (DF) was an employee of Generation Biotech at the time of the work. DM developed the Region Specific Extraction method in collaboration with Generation Biotech.

15. Marlow FL, Mullins MC. Bucky ball functions in Balbiani body assembly and animal-vegetal polarity in the oocyte and follicle cell layer in zebrafish. Dev Biol. 2008;321(1):40–50. Epub 2008/06/28. doi: 10.1016/j.ydbio.2008.05.557 18582455; PubMed Central PMCID: PMC2606906.

16. Abrams EW, Mullins MC. Early zebrafish development: it's in the maternal genes. Curr Opin Genet Dev. 2009;19(4):396–403. Epub 2009/07/18. doi: 10.1016/j.gde.2009.06.002 19608405; PubMed Central PMCID: PMC2752143.

17. Abrams EW, Zhang H, Marlow FL, Kapp L, Lu S, Mullins MC. Dynamic assembly of brambleberry mediates nuclear envelope fusion during early development. Cell. 2012;150(3):521–32. Epub 2012/08/07. doi: 10.1016/j.cell.2012.05.048 22863006; PubMed Central PMCID: PMC3700733.

18. Bontems F, Stein A, Marlow F, Lyautey J, Gupta T, Mullins MC, et al. Bucky ball organizes germ plasm assembly in zebrafish. Curr Biol. 2009;19(5):414–22. Epub 2009/03/03. doi: 10.1016/j.cub.2009.01.038 19249209.

19. Ge X, Grotjahn D, Welch E, Lyman-Gingerich J, Holguin C, Dimitrova E, et al. Hecate/Grip2a acts to reorganize the cytoskeleton in the symmetry-breaking event of embryonic axis induction. PLoS Genet. 2014;10(6):e1004422. Epub 2014/06/27. doi: 10.1371/journal.pgen.1004422 24967891; PubMed Central PMCID: PMC4072529.

20. Kapp LD, Abrams EW, Marlow FL, Mullins MC. The integrator complex subunit 6 (Ints6) confines the dorsal organizer in vertebrate embryogenesis. PLoS Genet. 2013;9(10):e1003822. Epub 2013/11/10. doi: 10.1371/journal.pgen.1003822 24204286; PubMed Central PMCID: PMC3814294.

21. Langdon YG, Mullins MC. Maternal and zygotic control of zebrafish dorsoventral axial patterning. Annu Rev Genet. 2011;45 : 357–77. Epub 2011/09/29. doi: 10.1146/annurev-genet-110410-132517 21942367.

22. Nair S, Marlow F, Abrams E, Kapp L, Mullins MC, Pelegri F. The chromosomal passenger protein birc5b organizes microfilaments and germ plasm in the zebrafish embryo. PLoS Genet. 2013;9(4):e1003448. Epub 2013/05/03. doi: 10.1371/journal.pgen.1003448 23637620; PubMed Central PMCID: PMC3630083.

23. Jaeger S, Barends S, Giege R, Eriani G, Martin F. Expression of metazoan replication-dependent histone genes. Biochimie. 2005;87(9–10):827–34. Epub 2005/09/17. doi: 10.1016/j.biochi.2005.03.012 16164992.

24. Pelegri F, Mullins MC. Genetic screens for mutations affecting adult traits and parental-effect genes. Methods Cell Biol. 2016;135 : 39–87. Epub 2016/07/23. doi: 10.1016/bs.mcb.2016.05.006 27443920.

25. Aken BL, Achuthan P, Akanni W, Amode MR, Bernsdorff F, Bhai J, et al. Ensembl 2017. Nucleic Acids Res. 2017;45(D1):D635–D42. Epub 2016/12/03. doi: 10.1093/nar/gkw1104 27899575; PubMed Central PMCID: PMC5210575.

26. Deegan TD, Diffley JF. MCM: one ring to rule them all. Curr Opin Struct Biol. 2016;37 : 145–51. Epub 2016/02/13. doi: 10.1016/j.sbi.2016.01.014 26866665.

27. Kettleborough RN, Busch-Nentwich EM, Harvey SA, Dooley CM, de Bruijn E, van Eeden F, et al. A systematic genome-wide analysis of zebrafish protein-coding gene function. Nature. 2013;496(7446):494–7. Epub 2013/04/19. doi: 10.1038/nature11992 23594742; PubMed Central PMCID: PMC3743023.

28. Shinya M, Machiki D, Henrich T, Kubota Y, Takisawa H, Mimura S. Evolutionary diversification of MCM3 genes in Xenopus laevis and Danio rerio. Cell Cycle. 2014;13(20):3271–81. Epub 2014/12/09. doi: 10.4161/15384101.2014.954445 25485507; PubMed Central PMCID: PMC4615024.

29. Miller-Bertoglio VE, Fisher S, Sanchez A, Mullins MC, Halpern ME. Differential regulation of chordin expression domains in mutant zebrafish. Dev Biol. 1997;192(2):537–50. Epub 1998/01/27. doi: 10.1006/dbio.1997.8788 9441687.

30. Sasai Y, Lu B, Steinbeisser H, Geissert D, Gont LK, De Robertis EM. Xenopus chordin: a novel dorsalizing factor activated by organizer-specific homeobox genes. Cell. 1994;79(5):779–90. Epub 1994/12/02. doi: 10.1016/0092-8674(94)90068-x 8001117; PubMed Central PMCID: PMC3082463.

31. Schulte-Merker S, Hammerschmidt M, Beuchle D, Cho KW, De Robertis EM, Nusslein-Volhard C. Expression of zebrafish goosecoid and no tail gene products in wild-type and mutant no tail embryos. Development. 1994;120(4):843–52. Epub 1994/04/01. 7600961.

32. Amsterdam A, Nissen RM, Sun Z, Swindell EC, Farrington S, Hopkins N. Identification of 315 genes essential for early zebrafish development. Proc Natl Acad Sci U S A. 2004;101(35):12792–7. Epub 2004/07/17. doi: 10.1073/pnas.0403929101 15256591; PubMed Central PMCID: PMC516474.

33. Zhong H, Xin S, Zhao Y, Lu J, Li S, Gong J, et al. Genetic approach to evaluate specificity of small molecule drug candidates inhibiting PLK1 using zebrafish. Mol Biosyst. 2010;6(8):1463–8. Epub 2010/07/14. doi: 10.1039/b919743e 20625580.

34. Schmucker S, Sumara I. Molecular dynamics of PLK1 during mitosis. Mol Cell Oncol. 2014;1(2):e954507. Epub 2014/04/01. doi: 10.1080/23723548.2014.954507 27308323; PubMed Central PMCID: PMC4905186.

35. Baran V, Solc P, Kovarikova V, Rehak P, Sutovsky P. Polo-like kinase 1 is essential for the first mitotic division in the mouse embryo. Mol Reprod Dev. 2013;80(7):522–34. Epub 2013/05/08. doi: 10.1002/mrd.22188 23649868.

36. Rahman MM, Munzig M, Kaneshiro K, Lee B, Strome S, Muller-Reichert T, et al. Caenorhabditis elegans polo-like kinase PLK-1 is required for merging parental genomes into a single nucleus. Mol Biol Cell. 2015;26(25):4718–35. Epub 2015/10/23. doi: 10.1091/mbc.E15-04-0244 26490119; PubMed Central PMCID: PMC4678026.

37. Rahman M, Chang IY, Harned A, Maheshwari R, Amoateng K, Narayan K, et al. C. elegans pronuclei fuse after fertilization through a novel membrane structure. J Cell Biol. 2020;219(2). Epub 2019/12/14. doi: 10.1083/jcb.201909137 31834351.

38. Ning J, Otto TD, Pfander C, Schwach F, Brochet M, Bushell E, et al. Comparative genomics in Chlamydomonas and Plasmodium identifies an ancient nuclear envelope protein family essential for sexual reproduction in protists, fungi, plants, and vertebrates. Genes Dev. 2013;27(10):1198–215. Epub 2013/05/24. doi: 10.1101/gad.212746.112 23699412; PubMed Central PMCID: PMC3672651.

39. Marzluff WF, Koreski KP. Birth and Death of Histone mRNAs. Trends Genet. 2017;33(10):745–59. Epub 2017/09/05. doi: 10.1016/j.tig.2017.07.014 28867047; PubMed Central PMCID: PMC5645032.

40. Wang ZF, Ingledue TC, Dominski Z, Sanchez R, Marzluff WF. Two Xenopus proteins that bind the 3' end of histone mRNA: implications for translational control of histone synthesis during oogenesis. Mol Cell Biol. 1999;19(1):835–45. Epub 1998/12/22. doi: 10.1128/mcb.19.1.835 9858606; PubMed Central PMCID: PMC83940.

41. Thelie A, Pascal G, Angulo L, Perreau C, Papillier P, Dalbies-Tran R. An oocyte-preferential histone mRNA stem-loop-binding protein like is expressed in several mammalian species. Mol Reprod Dev. 2012;79(6):380–91. Epub 2012/04/03. doi: 10.1002/mrd.22040 22467188.

42. Labrecque R, Lodde V, Dieci C, Tessaro I, Luciano AM, Sirard MA. Chromatin remodelling and histone m RNA accumulation in bovine germinal vesicle oocytes. Mol Reprod Dev. 2015;82(6):450–62. Epub 2015/05/06. doi: 10.1002/mrd.22494 25940597.

43. He WX, Wu M, Liu Z, Li Z, Wang Y, Zhou J, et al. Oocyte-specific maternal Slbp2 is required for replication-dependent histone storage and early nuclear cleavage in zebrafish oogenesis and embryogenesis. RNA. 2018;24(12):1738–48. Epub 2018/09/07. doi: 10.1261/rna.067090.118 30185624; PubMed Central PMCID: PMC6239174.

44. Imai F, Yoshizawa A, Matsuzaki A, Oguri E, Araragi M, Nishiwaki Y, et al. Stem-loop binding protein is required for retinal cell proliferation, neurogenesis, and intraretinal axon pathfinding in zebrafish. Dev Biol. 2014;394(1):94–109. Epub 2014/08/12. doi: 10.1016/j.ydbio.2014.07.020 25106852.

45. Arnold DR, Francon P, Zhang J, Martin K, Clarke HJ. Stem-loop binding protein expressed in growing oocytes is required for accumulation of mRNAs encoding histones H3 and H4 and for early embryonic development in the mouse. Dev Biol. 2008;313(1):347–58. Epub 2007/11/27. doi: 10.1016/j.ydbio.2007.10.032 18036581; PubMed Central PMCID: PMC5123872.

46. Sanchez R, Marzluff WF. The stem-loop binding protein is required for efficient translation of histone mRNA in vivo and in vitro. Mol Cell Biol. 2002;22(20):7093–104. Epub 2002/09/21. doi: 10.1128/MCB.22.20.7093-7104.2002 12242288; PubMed Central PMCID: PMC139811.

47. Dominski Z, Marzluff WF. Formation of the 3' end of histone mRNA. Gene. 1999;239(1):1–14. Epub 1999/11/26. doi: 10.1016/s0378-1119(99)00367-4 10571029.

48. Amodeo AA, Jukam D, Straight AF, Skotheim JM. Histone titration against the genome sets the DNA-to-cytoplasm threshold for the Xenopus midblastula transition. Proc Natl Acad Sci U S A. 2015;112(10):E1086–95. Epub 2015/02/26. doi: 10.1073/pnas.1413990112 25713373; PubMed Central PMCID: PMC4364222.

49. Joseph SR, Palfy M, Hilbert L, Kumar M, Karschau J, Zaburdaev V, et al. Competition between histone and transcription factor binding regulates the onset of transcription in zebrafish embryos. Elife. 2017;6. Epub 2017/04/21. doi: 10.7554/eLife.23326 28425915; PubMed Central PMCID: PMC5451213.

50. Zamir E, Kam Z, Yarden A. Transcription-dependent induction of G1 phase during the zebra fish midblastula transition. Mol Cell Biol. 1997;17(2):529–36. Epub 1997/02/01. doi: 10.1128/mcb.17.2.529 9001205; PubMed Central PMCID: PMC231777.

51. Kwan KM, Fujimoto E, Grabher C, Mangum BD, Hardy ME, Campbell DS, et al. The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev Dyn. 2007;236(11):3088–99. Epub 2007/10/17. doi: 10.1002/dvdy.21343 17937395.

52. Higashijima S, Okamoto H, Ueno N, Hotta Y, Eguchi G. High-frequency generation of transgenic zebrafish which reliably express GFP in whole muscles or the whole body by using promoters of zebrafish origin. Dev Biol. 1997;192(2):289–99. Epub 1998/01/27. doi: 10.1006/dbio.1997.8779 9441668.

53. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol. 2011;7 : 539. Epub 2011/10/13. doi: 10.1038/msb.2011.75 21988835; PubMed Central PMCID: PMC3261699.

54. Simossis VA, Heringa J. PRALINE: a multiple sequence alignment toolbox that integrates homology-extended and secondary structure information. Nucleic Acids Res. 2005;33(Web Server issue):W289–94. Epub 2005/06/28. doi: 10.1093/nar/gki390 15980472; PubMed Central PMCID: PMC1160151.

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