Interactions Between Nuclei and the Cytoskeleton Are Mediated by SUN-KASH Nuclear-Envelope Bridges

Starr, Daniel A.; Fridolfsson, Heidi N.

doi:10.1146/annurev-cellbio-100109-104037

Cited by 508 publications

(645 citation statements)

References 167 publications

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“…As these stresses are much smaller than the maximum stresses membranes can endure (27)(28)(29), our findings may be of value to understanding the nanoarchitecture of the nuclear envelope. Because our model predicts a stable structure over a wide range of tensile stresses, nuclei may be able to easily adjust to the changes in nuclear stresses in a biological setting and yet acquire and maintain their geometry (30).…”

Section: Discussionmentioning

confidence: 99%

Ultradonut topology of the nuclear envelope

Torbati

Lele

Agrawal

2016

Proc. Natl. Acad. Sci. U.S.A.

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The nuclear envelope is a unique topological structure formed by lipid membranes in eukaryotic cells. Unlike other membrane structures, the nuclear envelope comprises two concentric membrane shells fused at numerous sites with toroid-shaped pores that impart a "geometric" genus on the order of thousands. Despite the intriguing architecture and vital biological functions of the nuclear membranes, how they achieve and maintain such a unique arrangement remains unknown. Here, we used the theory of elasticity and differential geometry to analyze the equilibrium shape and stability of this structure. Our results show that modest inand out-of-plane stresses present in the membranes not only can define the pore geometry, but also provide a mechanism for destabilizing membranes beyond a critical size and set the stage for the formation of new pores. Our results suggest a mechanism wherein nanoscale buckling instabilities can define the global topology of a nuclear envelope-like structure.nuclear envelope | lipid membranes | topology | buckling instability T he cell nucleus is bounded by two lipid bilayers arranged in a unique geometry called the nuclear envelope. These two bilayers are shaped into concentric spheres that are maintained at a remarkably uniform spacing of ∼ 30−50 nm (1), and yet are fused together at thousands of pores (holes) at an average spacing of ∼ 250−500 nm from each other [based on areal density measurements (2-4)]. At these pores, the membranes locally take on a toroid shape with a radius of curvature on the order of ∼ 20 nm ( Fig. 1). Lipid structures such as vesicles, spherocylinders (bacterial membranes), and biconcave discoids (red blood cell membranes) are all closed structures with no holes, and hence possess a zero genus (5) (Fig. 1). A donut, on the other hand, is also a closed structure but has one hole, and as a result has a genus of 1 (Fig. 1). If we fuse two donuts, we get a shape with a genus of 2, and if we fuse thousands of donuts and bend them to form a sphere, we obtain a nucleus-membrane-like structure ( Fig. 1). This structure, therefore, can be thought of as an "ultradonut" with a genus on the order of thousands. How the two membranes assemble in a unique arrangement with such a large number of local fusions is a fundamental question in both physics and biology that is still unresolved (6-10). To seek an answer to this puzzle, we ask three natural questions based on the common notions in the field of membrane physics.First, can membrane curvature-mediated interactions determine optimal pore number and interpore separation? This principle has been successfully used to predict the interactions of membraneembedded proteins and nanoparticles (11-13). However, in the case of nuclear envelope, Fig. 1C (14) shows that the curved shapes of the membranes at the pores do not persist over interpore length scales; The "curvature memory" of the membranes is lost beyond ∼ 100 nm and they remain essentially flat in between the pores. As a result, a pore does not sense the presence of other p...

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Section: Discussionmentioning

confidence: 99%

Ultradonut topology of the nuclear envelope

Torbati

Lele

Agrawal

2016

Proc. Natl. Acad. Sci. U.S.A.

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“…Polarized Localization of OsSAD1 on the Nuclear Envelope Is Dependent on ZYGO1 SUN-domain proteins form a key component of the LINC complex that promotes telomere clustering and chromosomal movement (Starr and Fridolfsson, 2010). SUN proteins, such as SUN-1, AtSUN1, AtSUN2, and ZmSUN2, show polarized localization on one side of the nuclear envelope during early prophase I in C. elegans, Arabidopsis, and maize (Penkner et al, 2009;Murphy et al, 2014;Varas et al, 2015).…”

Section: Zygo1 Is Required For Telomere Clustering In Pair1 and Oscom1mentioning

confidence: 99%

“…Then, at the INM, telomeres are associated with the transmembrane linker of nucleoskeleton and cytoskeleton (LINC) complex that is composed of SUN and KASH domain proteins (Ding et al, 2007;Yoshida et al, 2013). This transmembrane complex transduces cytoskeletal forces to telomeres and drives telomere clustering along the INM and, therefore, chromosome movements (Starr and Fridolfsson, 2010). However, so far, the molecular mechanisms underlying telomere bouquet formation in plant species are largely unknown.…”

Section: Introductionmentioning

confidence: 99%

The F-Box Protein ZYGO1 Mediates Bouquet Formation to Promote Homologous Pairing, Synapsis, and Recombination in Rice Meiosis

et al. 2017

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Telomere bouquet formation, a highly conserved meiotic event, plays an important role in homologous pairing and therefore progression of meiosis; however, the underlying molecular mechanism remains largely unknown. Here, we identified ZYGOTENE1 (ZYGO1), a novel F-box protein in rice (Oryza sativa), and verified its essential role in bouquet formation during early meiosis. In zygo1 mutants, zygotene chromosome aggregation and telomere clustering failed to occur. The suppressed telomere clustering in homologous pairing aberration in rice meiosis1 (pair1) zygo1 and rice completion of meiotic recombination (Oscom1) zygo1 double mutants, together with the altered localization of OsSAD1 (a SUN protein associated with the nuclear envelope) in zygo1, showed that ZYGO1 has a significant function in bouquet formation. In addition, the interaction between ZYGO1 and rice SKP1-like protein 1 suggested that ZYGO1 might modulate bouquet formation as a component of the SKP1-Cullin1-F-box complex. Although double-strand break formation and early recombination element installation occurred normally, zygo1 mutants showed defects in full-length pairing and synaptonemal complex assembly. Furthermore, crossover (CO) formation was disturbed, and foci of Human enhancer of invasion 10 were restricted to the partially synapsed chromosome regions, indicating that CO reduction might be caused by the failure of full-length chromosome alignment in zygo1. Therefore, we propose that ZYGO1 mediates bouquet formation to efficiently promote homolog pairing, synapsis, and CO formation in rice meiosis.

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“…A concentrated microtubule-based "cage" or "fork"-like structure has been observed in migrating primary cerebellar or cortical neurons (Rivas and Hatten 1995;Xie et al 2003). Such a defined structure has not been observed so far in the neuroepithelium; nevertheless, the nucleus is surrounded by microtubules, which may be connected to the nuclear membrane by Sad1p, UNC-84 (SUN)-and Klarsicht, ANC-1, Syne Homology (KASH)-domain proteins (Starr and Fridolfsson 2010; Fig. 2).…”

Section: Molecular Motors and The Cytoskeletonmentioning

confidence: 94%

Interkinetic Nuclear Movement in the Ventricular Zone of the Cortex

2011

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The nuclei of neuroepithelial cells move along the apicobasal axis in synchronization with their cell cycle status. This motility is known as interkinetic nuclear movement. We discuss here the importance of cytoskeleton organization, the centrosome, molecular motors, cell polarity proteins, and their regulators in controlling and maintaining this typical behavior. Furthermore, due to the tight linkage between cell proliferation, cell cycle, and nuclear motility, we speculate that interkinetic nuclear movement is likely to be affected in the pathophysiology of microcephaly, where the brain size is markedly reduced.

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Interactions Between Nuclei and the Cytoskeleton Are Mediated by SUN-KASH Nuclear-Envelope Bridges

Cited by 508 publications

References 167 publications

Ultradonut topology of the nuclear envelope

Ultradonut topology of the nuclear envelope

The F-Box Protein ZYGO1 Mediates Bouquet Formation to Promote Homologous Pairing, Synapsis, and Recombination in Rice Meiosis

Interkinetic Nuclear Movement in the Ventricular Zone of the Cortex

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