Skip to main content

Identification and Ultrastructural Characterization of a Novel Nuclear Degradation Complex in Differentiating Lens Fiber Cells.

Publication ,  Journal Article
Costello, MJ; Brennan, LA; Mohamed, A; Gilliland, KO; Johnsen, S; Kantorow, M
Published in: PLoS One
2016

An unresolved issue in structural biology is how the encapsulated lens removes membranous organelles to carry out its role as a transparent optical element. In this ultrastructural study, we establish a mechanism for nuclear elimination in the developing chick lens during the formation of the organelle-free zone. Day 12-15 chick embryo lenses were examined by high-resolution confocal light microscopy and thin section transmission electron microscopy (TEM) following fixation in 10% formalin and 4% paraformaldehyde, and then processing for confocal or TEM as described previously. Examination of developing fiber cells revealed normal nuclei with dispersed chromatin and clear nucleoli typical of cells in active ribosome production to support protein synthesis. Early signs of nuclear degradation were observed about 300 μm from the lens capsule in Day 15 lenses where the nuclei display irregular nuclear stain and prominent indentations that sometimes contained a previously undescribed macromolecular aggregate attached to the nuclear envelope. We have termed this novel structure the nuclear excisosome. This complex by confocal is closely adherent to the nuclear envelope and by TEM appears to degrade the outer leaflet of the nuclear envelope, then the inner leaflet up to 500 μm depth. The images suggest that the nuclear excisosome separates nuclear membrane proteins from lipids, which then form multilamellar assemblies that stain intensely in confocal and in TEM have 5 nm spacing consistent with pure lipid bilayers. The denuded nucleoplasm then degrades by condensation and loss of structure in the range 600 to 700 μm depth producing pyknotic nuclear remnants. None of these stages display any classic autophagic vesicles or lysosomes associated with nuclei. Uniquely, the origin of the nuclear excisosome is from filopodial-like projections of adjacent lens fiber cells that initially contact, and then appear to fuse with the outer nuclear membrane. These filopodial-like projections appear to be initiated with a clathrin-like coat and driven by an internal actin network. In summary, a specialized cellular organelle, the nuclear excisosome, generated in part by adjacent fiber cells degrades nuclei during fiber cell differentiation and maturation.

Duke Scholars

Altmetric Attention Stats
Dimensions Citation Stats

Published In

PLoS One

DOI

EISSN

1932-6203

Publication Date

2016

Volume

11

Issue

8

Start / End Page

e0160785

Location

United States

Related Subject Headings

  • Nuclear Envelope
  • Lens, Crystalline
  • Lens Capsule, Crystalline
  • General Science & Technology
  • Chick Embryo
  • Cell Nucleus
  • Cell Differentiation
  • Autophagy
  • Animals
 

Citation

APA
Chicago
ICMJE
MLA
NLM
Costello, M. J., Brennan, L. A., Mohamed, A., Gilliland, K. O., Johnsen, S., & Kantorow, M. (2016). Identification and Ultrastructural Characterization of a Novel Nuclear Degradation Complex in Differentiating Lens Fiber Cells. PLoS One, 11(8), e0160785. https://doi.org/10.1371/journal.pone.0160785
Costello, M Joseph, Lisa A. Brennan, Ashik Mohamed, Kurt O. Gilliland, Sönke Johnsen, and Marc Kantorow. “Identification and Ultrastructural Characterization of a Novel Nuclear Degradation Complex in Differentiating Lens Fiber Cells.PLoS One 11, no. 8 (2016): e0160785. https://doi.org/10.1371/journal.pone.0160785.
Costello MJ, Brennan LA, Mohamed A, Gilliland KO, Johnsen S, Kantorow M. Identification and Ultrastructural Characterization of a Novel Nuclear Degradation Complex in Differentiating Lens Fiber Cells. PLoS One. 2016;11(8):e0160785.
Costello, M. Joseph, et al. “Identification and Ultrastructural Characterization of a Novel Nuclear Degradation Complex in Differentiating Lens Fiber Cells.PLoS One, vol. 11, no. 8, 2016, p. e0160785. Pubmed, doi:10.1371/journal.pone.0160785.
Costello MJ, Brennan LA, Mohamed A, Gilliland KO, Johnsen S, Kantorow M. Identification and Ultrastructural Characterization of a Novel Nuclear Degradation Complex in Differentiating Lens Fiber Cells. PLoS One. 2016;11(8):e0160785.

Published In

PLoS One

DOI

EISSN

1932-6203

Publication Date

2016

Volume

11

Issue

8

Start / End Page

e0160785

Location

United States

Related Subject Headings

  • Nuclear Envelope
  • Lens, Crystalline
  • Lens Capsule, Crystalline
  • General Science & Technology
  • Chick Embryo
  • Cell Nucleus
  • Cell Differentiation
  • Autophagy
  • Animals