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Inheritance and biogenesis of organelles in the secretory pathway

Nature Reviews Molecular Cell Biology volume 8, pages 429–439 (2007)Cite this article

Key Points

  • The duplication and inheritance of both the endoplasmic reticulum (ER) and Golgi apparatus is coupled to cell-cycle progression.

  • Although the exact mechanisms underlying ER and Golgi inheritance differ according to the organism and growth state being studied, there are some common themes. Organelles can either be constructed de novo, or be remodelled and then segregated into the daughter cells. These are not necessarily mutually exclusive options.

  • Organelle structure is controlled by regulatory modifications. The best characterized of these is phosphorylation, but an emerging view is that ubiquitylation is potentially of equal significance.

  • Mitotic kinases, predominantly CDK1, promote the remodelling of organelles in mitosis, and set the stage for their segregation into the daughter cells.

  • In some cases, such as the ER in budding yeast, segregation involves active-transport mechanisms involving microtubule- and/or actin-based motors, whereas in others, for example the Golgi in mammalian cells, passive/stochastic partitioning is likely to be sufficient.

  • The Golgi has been implicated in signalling pathways that control mitotic progression, although the precise details of this regulation differ depending on the organism.

Abstract

In eukaryotic cells, cellular functions are compartmentalized into membrane-bound organelles. This has many advantages, as shown by the success of the eukaryotic lineage, but creates many problems for cells, such as the need to build and partition these organelles during cell growth and division. Diverse mechanisms for biogenesis of the endoplasmic reticulum and Golgi apparatus have evolved, ranging from de novo synthesis to the copying of a template organelle. The different mechanisms by which organelles are inherited in yeasts, protozoa and metazoans probably reflect the differences in the structure and copy number of these organelles.

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Figure 1: Conceptual models for organelle biogenesis and inheritance.
Figure 2: View of the ER and Golgi in yeast and animal cells.
Figure 3: Inheritance of the ER in yeast.
Figure 4: Inheritance of the ER in mammalian cells.
Figure 5: Golgi biogenesis and inheritance in yeast and protozoa.
Figure 6: Inheritance of the Golgi in mammalian cells.

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Acknowledgements

We would like to thank G. Warren and C. He for providing the images of dividing Toxoplasma gondii, V. Allan for images of the ER in animal cells, B. Glick for images of the Golgi in Pichia pastoris and Y. Du and S.Ferro-Novick for images of the budding yeast ER.

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  1. Faculty of Life Sciences, University of Manchester, The Michael Smith Building, Oxford Road, M13 9PT, Manchester, UK

    Martin Lowe

  2. University of Liverpool Cancer Studies Centre, 200 London Road, Liverpool, L3 9TA, UK

    Francis A. Barr

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Correspondence to Francis A. Barr.

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DATABASES

Entrez Genome Project

Toxoplasma gondii

Trypanosoma brucei

Glossary

Centrosome

The main microtubule organizing centre of animal cells.

Rab GTPases

Rab proteins are Ras-like GTPases that regulate membrane-trafficking events in eukaryotic cells. Different Rab proteins are specific for different transport pathways and different subcellular compartments.

Kinesin-1

A member of the kinesin family of microtubule-based motors, which typically move towards microtubule plus ends.

Mitotic spindle

A highly dynamic array of microtubules that forms during mitosis and serves to move the duplicated chromosomes apart.

COPI

Coat-protein complexes that are required for vesicle formation and trafficking between the endoplasmic reticulum and Golgi.

Unknown function essential-1

(Ufe1). A SNARE protein involved in both fusion between endoplasmic reticulum membranes and vesicle fusion with the endoplasmic reticulum.

Exocyst

A multisubunit protein complex that is important for docking secretory vesicles with the plasma membrane, and anchoring the endoplasmic reticulum to the plasma membrane during cell division.

Sec61 translocon

An endoplasmic reticulum (ER)-localized protein complex that facilitates the insertion of newly synthesized secretory and membrane proteins into the ER.

Cdc42

A small Rho-family GTPase that regulates localized actin dynamics in cells.

CDK1

The catalytic subunit of the principal serine/threonine kinase that regulates entry into mitosis.

B-type cyclin

The regulatory subunit of the principal mitotic serine/threonine kinase. In mammals, cyclin B binds to the catalytic subunit CDK1.

Cdc28–cyclin-2

A serine/threonine kinase that regulates entry into S phase, comprising a catalytic subunit (Cdc28) and a regulatory subunit (cyclin-2).

Dynein

A multisubunit microtubule-based motor, typically moving towards microtubule minus ends.

Nuclear lamina

A structure composed of lamin intermediate-filament proteins that is important for integrity of nuclear envelope.

Golgi matrix

A biochemically defined meshwork of proteins that retains the characteristic cisternal shape of Golgi membranes.

ER exit site

A specialized site in the endoplasmic reticulum (ER) where vesicles are generated that transport proteins from the ER to the Golgi.

Basal body

The microtubule organizing centre of protozoa, equivalent to the centrosome of animal cells, typically the nucleating site for flagella and cilia.

Centrin

A calcium-binding protein that is associated with microtubule organizing centres.

Golgin-84

A member of a diverse family of coiled-coil proteins that have been implicated in vesicle trafficking and shaping the Golgi.

GRASP

(Golgi reassembly stacking protein). A family of proteins identified in an in vitro biochemical screen for Golgi stack formation.

Polo-like kinase 1

A serine or threonine kinase that is required for centrosome and spindle function in mitosis and cytokinesis.

Anaphase promoting complex/cyclosome

A ubiquitin ligase that is required for progression through mitosis.

Cytokinesis

The process of cytoplasmic division in animal cells.

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Lowe, M., Barr, F. Inheritance and biogenesis of organelles in the secretory pathway. Nat Rev Mol Cell Biol 8, 429–439 (2007). https://doi.org/10.1038/nrm2179

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