Lamin C2 (LMN C2) is a short product of the lamin a gene. It is a germ cell-specific lamin and has been extensively studied in male germ cells. In this study, we focussed on the expression and localization of LMN C2 in fully-grown germinal vesicle (GV) oocytes. We detected LMN C2 in the fully-grown germinal vesicle oocytes of various mammalian species with confirmation done by immunoblotting the wild type and Lmnc2 gene deleted testes. Expression of LMN C2 tagged with GFP showed localization of LMN C2 to the nuclear membrane of the oocyte. Moreover, the LMN C2 protein notably disappeared after nuclear envelope breakdown (NEBD) and the expression of LMN C2 was significantly reduced in the oocytes from aged females and ceased altogether during meiotic maturation. These results provide new insights regarding LMN C2 expression in the oocytes of various mammalian species.

Department of Animal Production Faculty of Agriculture Cairo University Giza Egypt

Department of Cell and Developmental Biology Biocenter University of Würzburg Würzburg Germany

Laboratory of Applied Proteome Analyses Institute of Animal Physiology and Genetics of the Czech Academy of Sciences Libechov Czech Republic

Laboratory of Biochemistry and Molecular Biology of Germ Cells Institute of Animal Physiology and Genetics of the Czech Academy of Sciences Libechov Czech Republic

Laboratory of Developmental Biology Institute of Animal Physiology and Genetics of the Czech Academy of Sciences Libechov Czech Republic

Zobrazit více v PubMed

Goldman AE, Maul G, Steinert PM, Yang HY, Goldman RD. Keratin-like proteins that coisolate with intermediate filaments of BHK-21 cells are nuclear lamins. Proc Natl Acad Sci U S A. 1986;83: 3839–3843. 10.1073/pnas.83.11.3839 PubMed DOI PMC

McKeon FD, Kirschner MW, Caput D. Homologies in both primary and secondary structure between nuclear envelope and intermediate filament proteins. Nature. 1986;319: 463–468. 10.1038/319463a0 PubMed DOI

Fawcett DW. On the occurrence of a fibrous lamina on the inner aspect of the nuclear envelope in certain cells of vertebrates. American Journal of Anatomy. 1966;119: 129–145. 10.1002/aja.1001190108 PubMed DOI

Furukawa K, Hotta Y. cDNA cloning of a germ cell specific lamin B3 from mouse spermatocytes and analysis of its function by ectopic expression in somatic cells. EMBO J. 1993;12: 97–106. PubMed PMC

Peter M, Kitten GT, Lehner CF, Vorburger K, Bailer SM, Maridor G, et al. Cloning and sequencing of cDNA clones encoding chicken lamins A and B1 and comparison of the primary structures of vertebrate A- and B-type lamins. Journal of Molecular Biology. 1989;208: 393–404. 10.1016/0022-2836(89)90504-4 PubMed DOI

Dittmer TA, Misteli T. The lamin protein family. Genome Biol. 2011;12: 222 10.1186/gb-2011-12-5-222 PubMed DOI PMC

Furukawa K, Inagaki H, Hotta Y. Identification and Cloning of an mRNA Coding for a Germ Cell-Specific A-Type Lamin in Mice. Experimental Cell Research. 1994;212: 426–430. 10.1006/excr.1994.1164 PubMed DOI

Lin F, Worman HJ. Structural organization of the human gene encoding nuclear lamin A and nuclear lamin C. J Biol Chem. 1993;268: 16321–16326. PubMed

Alsheimer M, Benavente R. Change of karyoskeleton during mammalian spermatogenesis: expression pattern of nuclear lamin C2 and its regulation. Exp Cell Res. 1996;228: 181–188. 10.1006/excr.1996.0315 PubMed DOI

Smith A, Benavente R. Identification of a short nuclear lamin protein selectively expressed during meiotic stages of rat spermatogenesis. Differentiation. 1992;52: 55–60. 10.1111/j.1432-0436.1992.tb00499.x PubMed DOI

Vester B, Smith A, Krohne G, Benavente R. Presence of a nuclear lamina in pachytene spermatocytes of the rat. J Cell Sci. 1993;104 (Pt 2): 557–563. PubMed

Alsheimer M, Glasenapp E von, Schnölzer M, Heid H, Benavente R. Meiotic lamin C2: The unique amino-terminal hexapeptide GNAEGR is essential for nuclear envelope association. PNAS. 2000;97: 13120–13125. 10.1073/pnas.240466597 PubMed DOI PMC

Alsheimer M, von Glasenapp E, Hock R, Benavente R. Architecture of the nuclear periphery of rat pachytene spermatocytes: distribution of nuclear envelope proteins in relation to synaptonemal complex attachment sites. Mol Biol Cell. 1999;10: 1235–1245. 10.1091/mbc.10.4.1235 PubMed DOI PMC

Link J, Jahn D, Schmitt J, Göb E, Baar J, Ortega S, et al. The Meiotic Nuclear Lamina Regulates Chromosome Dynamics and Promotes Efficient Homologous Recombination in the Mouse. PLOS Genetics. 2013;9: e1003261 10.1371/journal.pgen.1003261 PubMed DOI PMC

Nakajima N, Abe K. Genomic structure of the mouse A-type lamin gene locus encoding somatic and germ cell-specific lamins. FEBS Lett. 1995;365: 108–114. 10.1016/0014-5793(95)00453-g PubMed DOI

Jahn D, Schramm S, Benavente R, Alsheimer M. Dynamic properties of meiosis-specific lamin C2 and its impact on nuclear envelope integrity. Nucleus. 2010;1: 273–283. 10.4161/nucl.1.3.11800 PubMed DOI PMC

Jahn D, Schramm S, Schnölzer M, Heilmann CJ, Koster CG de, Schütz W, et al. A truncated lamin A in the Lmna−/− mouse line. Nucleus. 2012;3: 463–474. 10.4161/nucl.21676 PubMed DOI PMC

Lišková L, Šušor A, Pivoňková K, Šašková A, Karabínová P, Kubelka M. Detection of condensin I and II in maturing pig oocytes. Reprod Fertil Dev. 2010;22: 644–652. 10.1071/RD09068 PubMed DOI

Jansova D, Tetkova A, Koncicka M, Kubelka M, Susor A. Localization of RNA and translation in the mammalian oocyte and embryo. Palazzo AF, editor. PLOS ONE. 2018;13: e0192544 10.1371/journal.pone.0192544 PubMed DOI PMC

Koncicka M, Tetkova A, Jansova D, Del Llano E, Gahurova L, Kracmarova J, et al. Increased Expression of Maturation Promoting Factor Components Speeds Up Meiosis in Oocytes from Aged Females. Int J Mol Sci. 2018;19 10.3390/ijms19092841 PubMed DOI PMC

Tetkova A, Susor A, Kubelka M, Nemcova L, Jansova D, Dvoran M, et al. Follicle-stimulating hormone administration affects amino acid metabolism in mammalian oocytes†. Biol Reprod. 2019;101: 719–732. 10.1093/biolre/ioz117 PubMed DOI

Masek T, del Llano E, Gahurova L, Kubelka M, Susor A, Roucova K, et al. Identifying the Translatome of Mouse NEBD-Stage Oocytes via SSP-Profiling; A Novel Polysome Fractionation Method. International Journal of Molecular Sciences. 2020;21: 1254 10.3390/ijms21041254 PubMed DOI PMC

Haithcock E, Dayani Y, Neufeld E, Zahand AJ, Feinstein N, Mattout A, et al. Age-related changes of nuclear architecture in Caenorhabditis elegans. Proc Natl Acad Sci USA. 2005;102: 16690–16695. 10.1073/pnas.0506955102 PubMed DOI PMC

Raz V, Vermolen BJ, Garini Y, Onderwater JJM, Mommaas-Kienhuis MA, Koster AJ, et al. The nuclear lamina promotes telomere aggregation and centromere peripheral localization during senescence of human mesenchymal stem cells. J Cell Sci. 2008;121: 4018–4028. 10.1242/jcs.034876 PubMed DOI

Righolt CH, van ‘t Hoff MLR, Vermolen BJ, Young IT, Raz V. Robust nuclear lamina-based cell classification of aging and senescent cells. Aging (Albany NY). 2011;3: 1192–1201. 10.18632/aging.100414 PubMed DOI PMC

Cheng J-M, Liu Y-X. Age-Related Loss of Cohesion: Causes and Effects. Int J Mol Sci. 2017;18 10.3390/ijms18071578 PubMed DOI PMC

Chiang T, Duncan FE, Schindler K, Schultz RM, Lampson MA. Evidence that weakened centromere cohesion is a leading cause of age-related aneuploidy in oocytes. Curr Biol. 2010;20: 1522–1528. 10.1016/j.cub.2010.06.069 PubMed DOI PMC

Gruenbaum Y, Margalit A, Goldman RD, Shumaker DK, Wilson KL. The nuclear lamina comes of age. Nat Rev Mol Cell Biol. 2005;6: 21–31. 10.1038/nrm1550 PubMed DOI

Liu B, Wang J, Chan KM, Tjia WM, Deng W, Guan X, et al. Genomic instability in laminopathy-based premature aging. Nat Med. 2005;11: 780–785. 10.1038/nm1266 PubMed DOI

Cimadomo D, Fabozzi G, Vaiarelli A, Ubaldi N, Ubaldi FM, Rienzi L. Impact of Maternal Age on Oocyte and Embryo Competence. Front Endocrinol (Lausanne). 2018;9 10.3389/fendo.2018.00327 PubMed DOI PMC

MacLennan M, Crichton JH, Playfoot CJ, Adams IR. Oocyte development, meiosis and aneuploidy. Semin Cell Dev Biol. 2015;45: 68–76. 10.1016/j.semcdb.2015.10.005 PubMed DOI PMC

Adhikari D, Zheng W, Shen Y, Gorre N, Ning Y, Halet G, et al. Cdk1, but not Cdk2, is the sole Cdk that is essential and sufficient to drive resumption of meiosis in mouse oocytes. Hum Mol Genet. 2012;21: 2476–2484. 10.1093/hmg/dds061 PubMed DOI

Peter M, Nakagawa J, Dorée M, Labbé JC, Nigg EA. In vitro disassembly of the nuclear lamina and M phase-specific phosphorylation of lamins by cdc2 kinase. Cell. 1990;61: 591–602. 10.1016/0092-8674(90)90471-p PubMed DOI

Link J, Benavente R, Alsheimer M. Analysis of Meiotic Telomere Behavior in the Mouse. Methods Mol Biol. 2016;1411: 195–208. 10.1007/978-1-4939-3530-7_12 PubMed DOI

Tetkova A, Hancova M. Mouse Oocyte Isolation, Cultivation and RNA Microinjection. BIO-PROTOCOL. 2016;6 10.21769/BioProtoc.1729 DOI

Bellve A, Cavicchia J, Millette C, O’Brien D, Bhatnagar Y, Dym M. Spermatogenic cells of the prepuberal mouse: isolation and morphological characterization. J Cell Biol. 1977;74: 68–85. 10.1083/jcb.74.1.68 PubMed DOI PMC

Nucleus reprogramming/remodeling through selective enucleation (SE) of immature oocytes and zygotes: a nucleolus point of view

Nuclear Lamins: Key Proteins for Embryonic Development