Nuclear lamins and peripheral nuclear antigens during fertilization and embryogenesis in mice and sea urchins.

Abstract

Nuclear structural changes during fertilization and embryogenesis in mice and in sea urchins have been followed by using antibodies against the nuclear lamins A/C and B and against antigens at the periphery of nuclei and chromosomes. Lamins are found on all pronuclei and nuclei during mouse fertilization, but with a diminished intensity on the second polar body nucleus. On sperm in both systems, lamins are reduced and detected only at the acrosomal and centriolar fossae. In sea urchin eggs, lamins are found on both pronuclei. Unlike in other dividing cells, the mitotic chromosomes of sea urchin eggs and embryos retain an association with lamins. The peripheral antibodies delineate each chromosome and nucleus except the mature mouse sperm nucleus. A dramatic change from the expected lamin distribution occurs during early development. In mouse morulae or blastocysts, lamins A/C are no longer recognized, although lamin B remains. In sea urchins both lamins A/C and lamin B, as detected with polyclonal antibodies, are lost after the blastula stage, although a different lamin A/C epitope emerges as recognized by a monoclonal antibody. These results demonstrate that pronucleus formation in both systems involves a new association or exposure of lamins, that the polar body nucleus is largely restricted from the cytoplasmic pool of lamins, and that mitotic chromosomes in the rapidly proliferating sea urchin egg retain associated lamins. They also suggest that changes in the expression or exposure of different lamins are a common feature of embryogenesis.Fertilization requires several dramatic changes in nuclear organization. The architecture of the nuclear surface (reviewed in refs. 1-4) involves the nuclear lamins, which are typically three proteins subjacent to the inner nuclear membrane (5, 6), and nuclear peripheral proteins referred to as "P1" (7) or "Perichromin" (8), which probably reside between the chromatin and the nuclear lamins. During mitosis in somatic cells, the lamins dissociate from the nuclear envelope at prophase and reappear with the reconstituting envelope at telophase (9). Unlike the behavior of the lamins at mitosis, the peripheral antigens separate from the nuclear periphery and ensheathe the condensing chromosomes before nuclear envelope breakdown and dissolution of the lamins during mitosis (7,8). During spermatogenesis the nuclear lamins are lost or vastly reduced (10-12), whereas during oogenesis the lamina may be comprised of only a single lamin (13-16), which differs from somatic lamins (17).In this study the presence and distribution of nuclear lamins and of the nuclear and chromosomal P1 peripheral antigens are traced during fertilization and embryogenesis in mice and in sea urchins. These two systems represent

Natural and artificial routes to pluripotency

“…Its degradation time course may represent one determinant for onset of ZGA. Support for this hypothesis stems from the observation that A-type lamin expression remains repressed until gastrulation (Foster et al, 2007;Hall et al, 2005;Houliston et al, 1988;Schatten et al, 1985). During ZGA, all circuitry essential for toti/pluripotency is up-regulated including the expression of Oct4, Sox2, Nanog and Sall4 which persists until the late blastula.…”

Protein Kinase C-mediated Interphase Lamin B Phosphorylation and Solubilization

“…Thus an unresolved issue is how the integrity of the female pronucleus is maintained during sperm NE disassembly. One possibility is that the female pronucleus contains a different set of lamins that would not be a substrate for PKC (36). This is suggested by the lack of reactivity of female pronuclei by immunofluorescence and immunoblotting using several anti-lamin antibodies (27), whereas sperm nuclei are highly reactive (18).…”

Building up the nucleus: nuclear organization in the establishment of totipotency and pluripotency during mammalian development

“…It was also observed that lamin A from oocytes shows decreased electrophoretic mobility compared with lamin A from fertilized embryos or any other mouse tissues, suggesting the existence of an oocyte-specific post-translational modification of lamin A (Houliston et al 1988). Contrary to B-type lamins that are expressed at similar levels throughout preimplantation development, the level of lamin A/C decreases after fertilization, and several groups were unable to identify A-type lamins beyond the morula stage, the protein only becoming detectable again after embryonic day 9 (E9) (Schatten et al 1985;Maul et al 1987;Stewart and Burke 1987). Others have detected low levels of lamin A/C in all preimplantation stages, including blastocysts (Houliston et al 1988;Eckersley-Maslin et al 2013).…”