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Curr Biol. 2017 Feb 6;27(3):408-414. doi: 10.1016/j.cub.2016.12.002. Epub 2017 Jan 12.

Navigation through the Plasma Membrane Molecular Landscape Shapes Random Organelle Movement.

Author information

1
Institute of Biological Chemistry, Biophysics and Bioengineering, Heriot-Watt University, Edinburgh EH14 4AS, UK; Edinburgh Super-Resolution Imaging Consortium.
2
Department of Mathematics, Maxwell Institute, MACS, Heriot-Watt University, Edinburgh EH14 4AS, UK.
3
Toronto Western Research Institute, Room 11-432, McLaughlin Wing, 399 Bathurst St., Toronto, ON M5T 2S8, Canada.
4
Centre for Inflammation Research, University of Edinburgh, The Queen's Medical Research Institute, 47 Little France Crescent, Edinburgh EH16 4TJ, UK.
5
The Clem Jones Centre for Ageing Dementia Research, Queensland Brain Institute, The University of Queensland, Brisbane, QLD 4072, Australia.
6
Institute of Biological Chemistry, Biophysics and Bioengineering, Heriot-Watt University, Edinburgh EH14 4AS, UK; Edinburgh Super-Resolution Imaging Consortium. Electronic address: r.r.duncan@hw.ac.uk.

Abstract

Eukaryotic plasma membrane organization theory has long been controversial, in part due to a dearth of suitably high-resolution techniques to probe molecular architecture in situ and integrate information from diverse data streams [1]. Notably, clustered patterning of membrane proteins is a commonly conserved feature across diverse protein families (reviewed in [2]), including the SNAREs [3], SM proteins [4, 5], ion channels [6, 7], and receptors (e.g., [8]). Much effort has gone into analyzing the behavior of secretory organelles [9-13], and understanding the relationship between the membrane and proximal organelles [4, 5, 12, 14] is an essential goal for cell biology as broad concepts or rules may be established. Here we explore the generally accepted model that vesicles at the plasmalemma are guided by cytoskeletal tracks to specific sites on the membrane that have clustered molecular machinery for secretion [15], organized in part by the local lipid composition [16]. To increase our understanding of these fundamental processes, we integrated nanoscopy and spectroscopy of the secretory machinery with organelle tracking data in a mathematical model, iterating with knockdown cell models. We find that repeated routes followed by successive vesicles, the re-use of similar fusion sites, and the apparently distinct vesicle "pools" are all fashioned by the Brownian behavior of organelles overlaid on navigation between non-reactive secretory protein molecular depots patterned at the plasma membrane.

KEYWORDS:

actin; cytoskeleton; exocytosis; mathematical modeling; microscopy; super-resolution; vesicle

PMID:
28089515
PMCID:
PMC5300901
DOI:
10.1016/j.cub.2016.12.002
[Indexed for MEDLINE]
Free PMC Article

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