How Plants LINC the SUN to KASH

Overview

Journal Nucleus

Date 2013 May 18

PMID 23680964

Citations 27

Authors

Xiao Zhou

Iris Meier

Affiliations

Soon will be listed here.

Abstract

Linkers of the nucleoskeleton to the cytoskeleton (LINC) complexes formed by SUN and KASH proteins are conserved eukaryotic protein complexes that bridge the nuclear envelope (NE) via protein-protein interactions in the NE lumen. Revealed by opisthokont studies, LINC complexes are key players in multiple cellular processes, such as nuclear and chromosomal positioning and nuclear shape determination, which in turn influence the generation of gametes and several aspects of development. Although comparable processes have long been known in plants, the first plant nuclear envelope bridging complexes were only recently identified. WPP domain-interacting proteins at the outer NE have little homology to known opisthokont KASH proteins, but form complexes with SUN proteins at the inner NE that have plant-specific properties and functions. In this review, we will address the importance of LINC complex-regulated processes, describe the plant NE bridging complexes and compare them to opisthokont LINC complexes.

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References

McGee M, Rillo R, Anderson A, Starr D . UNC-83 IS a KASH protein required for nuclear migration and is recruited to the outer nuclear membrane by a physical interaction with the SUN protein UNC-84. Mol Biol Cell. 2006; 17(4):1790-801. PMC: 1415293. DOI: 10.1091/mbc.e05-09-0894. View

Stewart-Hutchinson P, Hale C, Wirtz D, Hodzic D . Structural requirements for the assembly of LINC complexes and their function in cellular mechanical stiffness. Exp Cell Res. 2008; 314(8):1892-905. PMC: 2562747. DOI: 10.1016/j.yexcr.2008.02.022. View

Bass H, Marshall W, Sedat J, Agard D, Cande W . Telomeres cluster de novo before the initiation of synapsis: a three-dimensional spatial analysis of telomere positions before and during meiotic prophase. J Cell Biol. 1997; 137(1):5-18. PMC: 2139864. DOI: 10.1083/jcb.137.1.5. View

Guttinger S, Laurell E, Kutay U . Orchestrating nuclear envelope disassembly and reassembly during mitosis. Nat Rev Mol Cell Biol. 2009; 10(3):178-91. DOI: 10.1038/nrm2641. View

Frohnert C, Schweizer S, Hoyer-Fender S . SPAG4L/SPAG4L-2 are testis-specific SUN domain proteins restricted to the apical nuclear envelope of round spermatids facing the acrosome. Mol Hum Reprod. 2010; 17(4):207-18. DOI: 10.1093/molehr/gaq099. View

Starr D, Han M . Role of ANC-1 in tethering nuclei to the actin cytoskeleton. Science. 2002; 298(5592):406-9. DOI: 10.1126/science.1075119. View

Murphy S, Bass H . The maize (Zea mays) desynaptic (dy) mutation defines a pathway for meiotic chromosome segregation, linking nuclear morphology, telomere distribution and synapsis. J Cell Sci. 2012; 125(Pt 15):3681-90. DOI: 10.1242/jcs.108290. View

Zhou X, Graumann K, Evans D, Meier I . Novel plant SUN-KASH bridges are involved in RanGAP anchoring and nuclear shape determination. J Cell Biol. 2012; 196(2):203-11. PMC: 3265956. DOI: 10.1083/jcb.201108098. View

Zhou K, Rolls M, Hall D, Malone C, Hanna-Rose W . A ZYG-12-dynein interaction at the nuclear envelope defines cytoskeletal architecture in the C. elegans gonad. J Cell Biol. 2009; 186(2):229-41. PMC: 2717649. DOI: 10.1083/jcb.200902101. View

10.

Malone C, Fixsen W, Horvitz H, Han M . UNC-84 localizes to the nuclear envelope and is required for nuclear migration and anchoring during C. elegans development. Development. 1999; 126(14):3171-81. DOI: 10.1242/dev.126.14.3171. View

11.

Malone C, Misner L, Le Bot N, Tsai M, Campbell J, Ahringer J . The C. elegans hook protein, ZYG-12, mediates the essential attachment between the centrosome and nucleus. Cell. 2003; 115(7):825-36. DOI: 10.1016/s0092-8674(03)00985-1. View

12.

Park S, Howden R, Twell D . The Arabidopsis thaliana gametophytic mutation gemini pollen1 disrupts microspore polarity, division asymmetry and pollen cell fate. Development. 1998; 125(19):3789-99. DOI: 10.1242/dev.125.19.3789. View

13.

Koszul R, Kim K, Prentiss M, Kleckner N, Kameoka S . Meiotic chromosomes move by linkage to dynamic actin cables with transduction of force through the nuclear envelope. Cell. 2008; 133(7):1188-201. PMC: 2601696. DOI: 10.1016/j.cell.2008.04.050. View

14.

Starr D, Fridolfsson H . Interactions between nuclei and the cytoskeleton are mediated by SUN-KASH nuclear-envelope bridges. Annu Rev Cell Dev Biol. 2010; 26:421-44. PMC: 4053175. DOI: 10.1146/annurev-cellbio-100109-104037. View

15.

Murphy S, Simmons C, Bass H . Structure and expression of the maize (Zea mays L.) SUN-domain protein gene family: evidence for the existence of two divergent classes of SUN proteins in plants. BMC Plant Biol. 2010; 10:269. PMC: 3017857. DOI: 10.1186/1471-2229-10-269. View

16.

Crisp M, Liu Q, Roux K, Rattner J, Shanahan C, Burke B . Coupling of the nucleus and cytoplasm: role of the LINC complex. J Cell Biol. 2005; 172(1):41-53. PMC: 2063530. DOI: 10.1083/jcb.200509124. View

17.

Morimoto A, Shibuya H, Zhu X, Kim J, Ishiguro K, Han M . A conserved KASH domain protein associates with telomeres, SUN1, and dynactin during mammalian meiosis. J Cell Biol. 2012; 198(2):165-72. PMC: 3410425. DOI: 10.1083/jcb.201204085. View

18.

Padmakumar V, Libotte T, Lu W, Zaim H, Abraham S, Noegel A . The inner nuclear membrane protein Sun1 mediates the anchorage of Nesprin-2 to the nuclear envelope. J Cell Sci. 2005; 118(Pt 15):3419-30. DOI: 10.1242/jcs.02471. View

19.

Rivero F, Kuspa A, Brokamp R, Matzner M, Noegel A . Interaptin, an actin-binding protein of the alpha-actinin superfamily in Dictyostelium discoideum, is developmentally and cAMP-regulated and associates with intracellular membrane compartments. J Cell Biol. 1998; 142(3):735-50. PMC: 2148174. DOI: 10.1083/jcb.142.3.735. View

20.

Razafsky D, Blecher N, Markov A, Stewart-Hutchinson P, Hodzic D . LINC complexes mediate the positioning of cone photoreceptor nuclei in mouse retina. PLoS One. 2012; 7(10):e47180. PMC: 3465324. DOI: 10.1371/journal.pone.0047180. View