Remodeling of the Nuclear Envelope and Lamina during Bovine Preimplantation Development and Its Functional Implications.
The present study demonstrates a major remodeling of the nuclear envelope and its underlying lamina during bovine preimplantation development. Up to the onset of major embryonic genome activation (MGA) at the 8-cell stage nuclei showed a non-uniform distribution of nuclear pore complexes (NPCs). NPCs were exclusively present at sites where DNA contacted the nuclear lamina. Extended regions of the lamina, which were not contacted by DNA, lacked NPCs. In post-MGA nuclei the whole lamina was contacted rather uniformly by DNA. Accordingly, NPCs became uniformly distributed throughout the entire nuclear envelope. These findings shed new light on the conditions which control the integration of NPCs into the nuclear envelope. The switch from maternal to embryonic production of mRNAs was accompanied by multiple invaginations covered with NPCs, which may serve the increased demands of mRNA export and protein import. Other invaginations, as well as interior nuclear segments and vesicles without contact to the nuclear envelope, were exclusively positive for lamin B. Since the abundance of these invaginations and vesicles increased in concert with a massive nuclear volume reduction, we suggest that they reflect a mechanism for fitting the nuclear envelope and its lamina to a shrinking nuclear size during bovine preimplantation development. In addition, a deposit of extranuclear clusters of NUP153 (a marker for NPCs) without associated lamin B was frequently observed from the zygote stage up to MGA. Corresponding RNA-Seq data revealed deposits of spliced, maternally provided NUP153 mRNA and little unspliced, newly synthesized RNA prior to MGA, which increased strongly at the initiation of embryonic expression of NUP153 at MGA.
Division of Anthropology and Human Genetics, Biocenter, LMU Munich, Planegg-Martinsried, Germany; Chair for Molecular Animal Breeding and Biotechnology, Gene Center, LMU Munich, Munich, Germany.
Jens
J
Popken
Laboratory for Functional Genome Analysis (LAFUGA), Gene Center, LMU Munich, Munich, Germany.
Alexander
A
Graf
Laboratory for Functional Genome Analysis (LAFUGA), Gene Center, LMU Munich, Munich, Germany.
Stefan
S
Krebs
Laboratory for Functional Genome Analysis (LAFUGA), Gene Center, LMU Munich, Munich, Germany.
Helmut
H
Blum
Institute of Statistics, LMU Munich, Munich, Germany.
Volker J
VJ
Schmid
Division of Genetics, Biocenter, LMU Munich, Planegg-Martinsried, Germany.
Axel
A
Strauss
Chair for Molecular Animal Breeding and Biotechnology, Gene Center, LMU Munich, Munich, Germany.
Tuna
T
Guengoer
Chair for Molecular Animal Breeding and Biotechnology, Gene Center, LMU Munich, Munich, Germany.
Valeri
V
Zakhartchenko
Chair for Molecular Animal Breeding and Biotechnology, Gene Center, LMU Munich, Munich, Germany; Laboratory for Functional Genome Analysis (LAFUGA), Gene Center, LMU Munich, Munich, Germany.
Eckhard
E
Wolf
Division of Anthropology and Human Genetics, Biocenter, LMU Munich, Planegg-Martinsried, Germany.
Thomas
T
Cremer
D017398:Alternative Splicing / Q000235:genetics; D000818:Animals; D002417:Cattle; D053145:Cell Nucleus Size; D002843:Chromatin / Q000378:metabolism; D033481:Chromosomes, Mammalian / Q000378:metabolism; D004247:DNA / Q000378:metabolism; D047108:Embryonic Development; D021621:Imaging, Three-Dimensional; D034882:Lamins / Q000378:metabolism; D008853:Microscopy; D008938:Mitosis; D034881:Nuclear Lamina / Q000378:metabolism*; D022022:Nuclear Pore / Q000378:metabolism; D028861:Nuclear Pore Complex Proteins / Q000378:metabolism; D059467:Transcriptome / Q000235:genetics
D002843:Chromatin; D034882:Lamins; D028861:Nuclear Pore Complex Proteins; D004247:DNA