Annulate lamellae: An organelle in search of a function

Merisko, Elaine M.

doi:10.1016/0040-8166(89)90049-9

Cited by 29 publications

(24 citation statements)

References 57 publications

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“…AL are frequently observed in rapidly growing or differentiating cells, such as male and female gametes, tumor ceils, and viraUy infected cells. Although they may have an additional functional role, AL are believed to store excess nuclear envelope and pore components for later use (Kessel, 1983(Kessel, , 1992Stafstrom and Staehelin, 1984;Merisko, 1989).…”

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confidence: 99%

Nuclear pore complex assembly studied with a biochemical assay for annulate lamellae formation.

Meier

Miller

Forbes

1995

The Journal of Cell Biology

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Abstract. Formation of the nuclear pore is an intricate process involving membrane fusion and the ordered assembly of up to 1,000 pore proteins. As such, the study of pore assembly is not a simple one. Interestingly, annulate lamellae, a cytoplasmic organelle consisting of stacks of flattened membrane cisternae perforated by numerous pore complexes, have been found to form spontaneously in a reconstitution system derived from Xenopus egg extracts, as determined by electron microscopy (Dabauvalle et al., 1991). In this work, a biochemical assay for annulate lamellae (AL) formation was developed and used to study the mechanism of AL assembly in general and the assembly of individual nucleoporins into pore complexes in particular. Upon incubation of Xenopus egg cytosol and membrane vesicles, the nucleoporins nup58, nup60, nup97, nup153, and nup200 initially present in a disassembled form in the cytosol became associated with membranes and were pelletable. The association was time and temperature dependent and could be measured by immunoblotting. Thin-section electron microscopy as well as negative staining confirmed that annulate lamellae were forming coincident with the incorporation of pore proteins into membranes. Homogenization and subsequent flotation of the membrane fraction allowed us to separate a population of dense membranes, containing the integral membrane pore protein gp210 and all other nucleoporins tested, from the bulk of cellular membranes. Electron microscopy indicated that annulate lamellae were enriched in this dense, pore protein-containing fraction. GTP~/S prevented incorporation of the soluble pore proteins into membranes. To address whether AL form in the absence of N-acetylglucosaminylated pore proteins, AL assembly was carried out in WGAsepharose--depleted cytosol. Under these conditions, annulate lamellae formed but were altered in appearance. When the membrane fraction containing this altered AL was homogenized and subjected to flotation, the pore protein-containing membranes still sedimented in a distinct peak but were less dense than control annulate lamellae. T HE nuclear pore is responsible for establishing the distinct nuclear and cytoplasmic compartments of the eukaryotic cell. The pore is a highly selective channel through which macromolecular traffic must pass to enter or exit the nucleus. Although ions and other small molecules freely diffuse through the pore, larger molecules require a specific targeting signal for transit (for reviews, see Goldfarb and Michaud,.1991;Forbes, 1992;Gerace, 1992;Osborne and Silver, 1993;Powers and Forbes, 1994).The nuclear pore complex is a large and elaborate structure of ~120 million daltons and is comprised of N1,000 proteins. Structurally, it appears to consist of three ringsThe first two authors, Eva Meier and Brian R. Miller, contributed equally to the results presented here.Please address all correspondence to Douglass J. Forbes, Department of Biology, University of California at San Diego, La,lolla, CA 92093-0347. Tel.: (619) 534-0555....

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confidence: 99%

Nuclear pore complex assembly studied with a biochemical assay for annulate lamellae formation.

Meier

Miller

Forbes

1995

The Journal of Cell Biology

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“…This seems to be particularly true for somatic cells where the occurrence of AL might be vastly underestimated (Cordes et al, 1996). Only under conditions of metabolic activity, differentiation and rapid proliferation, does AL seem to be expressed more abundantly (Kessel 1989(Kessel , 1992Merisko, 1989). Some of these conditions are linked to diseases, including cancer, while others are part of normal cell physiological processes.…”

Section: Occurrence and Affecting Factorsmentioning

confidence: 99%

“…For the latter, any suggestions are based on microscopic observations putting their cellular positioning in relation to other organelles. Accordingly, either a nuclear origin, or their formation in conjunction with rough endoplasmic reticulum (rER) were hypothesized (for review : Wischnitzer, 1970;Merisko, 1989;Kessel, 1989Kessel, , 1992. Numerous reports proposed ideas in favour of one of these popular suggestions, because of their own observations of AL located proximal to the cell nucleus, or attached to rER.…”

Section: Biogenesismentioning

confidence: 99%

“…Among the AL-affecting factors, tubulin-depolymerizing agents such as vinblastine sulfate have been proven to be effective inducers of AL in tissue culture cells (De Brabander & Borgers, 1975;Kessel & Katow, 1984;Ewald et al, 1996;Reipert et al, 2009). Given the striking effectiveness of these agents, it was speculated that there is a possible relationship between formation of the AL network and the disassembly of microtubules (MTs) (De Brabander & Borgers, 1975;Merisko, 1989). A direct regulatory effect of tubulins on AL formation, however, has not yet been shown experimentally.…”

Section: Occurrence and Affecting Factorsmentioning

confidence: 99%

“…Previously, the lack of knowledge on AL could be regarded as encouraging the search for their possible functions (Merisko, 1989). Richard Kessel, one of the authorities in AL research, praised AL as the "last frontier in organelle research" (Kessel, 1992).…”

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Tubulohelical Membrane Arrays, Annulate Lamellae and Nuclear Pores: Tripartite Membrane Architecture with the Participation of Nucleoporins

Reipert¹,

Киселева²

2012

Current Frontiers and Perspectives in Cell Biology

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Cytoplasmic distribution of poly(A)‐containing RNA in developing Necturus maculosus oocytes with reference to annulate lamellae

Ganion

1991

Anat. Rec.

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The cytoplasmic distribution of poly(A)+ mRNA and its relationship to annulate lamellae were examined in developing Necturus maculosus oocytes by in situ hybridization with [3H]poly(U). The specificity of [3H]poly(U) binding was tested by incubating control ovarian sections with either KOH or RNase A before in situ hybridization. In both experiments, the silver grain densities were markedly reduced. Poly(A)+ RNA is uniformly distributed in the cytoplasm until the mid-growth phase and then later in vitellogenesis becomes localized in the subcortical ooplasm. The silver grain density in the cytoplasm varied during oogenesis and was greatest in previtellogenic oocytes. Annulate lamellae commonly are observed with the light microscope in oocytes prior to vitellogenesis. In such oocytes, the labeled mRNA probe is observed over cytoplasmic regions of annulate lamellae. The results suggests that a differential localization of messenger RNA occurs during oogenesis in Necturus maculosus. Furthermore, poly(A)+ RNA is present in cytoplasmic regions of annulate lamellae.

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Annulate lamellae: An organelle in search of a function

Cited by 29 publications

References 57 publications

Nuclear pore complex assembly studied with a biochemical assay for annulate lamellae formation.

Nuclear pore complex assembly studied with a biochemical assay for annulate lamellae formation.

Tubulohelical Membrane Arrays, Annulate Lamellae and Nuclear Pores: Tripartite Membrane Architecture with the Participation of Nucleoporins

Cytoplasmic distribution of poly(A)‐containing RNA in developing Necturus maculosus oocytes with reference to annulate lamellae

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