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Frontiers in Biology

ISSN 1674-7984

ISSN 1674-7992(Online)

CN 11-5892/Q

Front. Biol.    2017, Vol. 12 Issue (1) : 7-18    https://doi.org/10.1007/s11515-016-1436-9
REVIEW
Intracellular organelle networks: Understanding their organization and communication through systems-level modeling and analysis
Qinle Ba1,Ge Yang1,2()
1. Department of Biomedical Engineering, Carnegie Mellon University, Pittsburgh, PA 15213, USA
2. Department of Computational Biology, Carnegie Mellon University, Pittsburgh, PA 15213, USA
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Abstract

BACKGROUND: Membrane-bound intracellular organelles are biochemically distinct compartments used by eukaryotic cells for serving specialized physiological functions and organizing their internal environment. Recent studies revealed surprisingly extensive communication between these organelles and highlighted the network nature of their organization and communication. Since organization and communication of the organelles are carried out at the systems level through their networks, systems-level studies are essential for understanding the underlying mechanisms.

METHODS: We reviewed recent studies that used systems-level quantitative modeling and analysis to understand organization and communication of intracellular organelle networks.

RESULTS: We first review modeling and analysis studies on how fusion/fission and degradation/biogenesis, two essential and closely related classes of activities of individual organelles, collectively mediate the dynamic organization of their networks. We then turn to another important aspect of the dynamic organization of the organelle networks, namely how organelles are physically connected within their networks, a property referred to as the topology of the networks in mathematics, and summarize some of their distinct properties. Lastly, we briefly review modeling and analysis studies that aim to understand communication between different organelle networks, focusing on cellular calcium homeostasis as an example. We conclude with a brief discussion of future directions for research in this area.

CONCLUSIONS: Together, the reviewed studies provide critical insights into how diverse activities of individual organelles collectively mediate the organization and communication of their networks. They demonstrate the essential role of systems-level modeling and analysis in understanding complex behavior of such networks.

Keywords intracellular organelle      organelle network      organelle communication      network analysis      systems modeling     
Corresponding Author(s): Ge Yang   
Just Accepted Date: 23 December 2016   Online First Date: 08 February 2017    Issue Date: 28 February 2017
 Cite this article:   
Qinle Ba,Ge Yang. Intracellular organelle networks: Understanding their organization and communication through systems-level modeling and analysis[J]. Front. Biol., 2017, 12(1): 7-18.
 URL:  
https://academic.hep.com.cn/fib/EN/10.1007/s11515-016-1436-9
https://academic.hep.com.cn/fib/EN/Y2017/V12/I1/7
Fig.1  Graph representation of a dynamic network. (A) Graph representation of a network with 7 nodes and 11 edges. (B) The network in (A) after merging of node 1 with node 2. (C) The network in (A) after splitting of node 3 from node 2.
Fig.2  Examples of different topology exhibited by different organelle networks. (A) Discrete mitochondrial compartments in the axon of a Drosophila motor neuron. Scale bar: 10 mm. (B) Partially connected mitochondrial tubules in a Muntjac skin fibroblast cell. Scale bar: 2 mm. (C) Extensively connected ER network in a COS-7 cell. Scale bar: 2 mm.
Fig.3  Currently known mechanisms for communication between different types of organelle networks. (A) Communication through vesicle trafficking. (B) Communication through membrane fusion and fission. (C) Communication through membrane contact. Upper panel: membrane contact is mediated by tether proteins, shown in red. Lower panel: membrane contact mediates a wide range of cellular functions, such as organelle fission. (D) A diagram that summarizes some currently known communication pathways between organelle networks. All organelles except mitochondria belong to the endomembrane system, hence the different colors. ENDO, endosome; ER, endoplasmic reticulum; GOLGI, Golgi apparatus; LD, lipid droplets; LYSO, lysosome; MITO, mitochondria; PM, plasma membrane; PO, peroxisome.
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