LEM2 recruits CHMP7 for ESCRT-mediated nuclear envelope closure in fission yeast and human cells

Proceedings of the National Academy of Sciences of the United States of America

Volumn 114, Issue 11, 2017, Pages E2166-E2175

  Gu, Mingyu ^a,b   LaJoie, Dollie ^a   Chen, Opal S ^a   Von Appen, Alexander ^b   Ladinsky, Mark S ^c   Redd, Michael J ^d   Nikolova, Linda ^d   Bjorkman, Pamela J ^c   Sundquist, Wesley I ^a   Ullman, Katharine S ^a   Frost, Adam ^a,b  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c California Institute of Technology   (United States)

^d UNIVERSITY OF UTAH   (United States)

Author keywords

CHMP7; ESCRT III; LEM2; Nuclear envelope; VPS4

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CHMP7 PROTEIN; ESCRT PROTEIN; HYBRID PROTEIN; LEM2 PROTEIN; MEMBRANE PROTEIN; UNCLASSIFIED DRUG; CHMP7 PROTEIN, HUMAN; LEMD2 PROTEIN, HUMAN; NUCLEAR PROTEIN; PROTEIN BINDING; SCHIZOSACCHAROMYCES POMBE PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL NUCLEUS MEMBRANE; CELL STRUCTURE; CONTROLLED STUDY; FISSION YEAST; FUNGUS GROWTH; GENE INTERACTION; HUMAN; HUMAN CELL; IN VITRO STUDY; LOSS OF FUNCTION MUTATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SCHIZOSACCHAROMYCES POMBE; YEAST CELL; ALLELE; BIOLOGICAL MODEL; FLUORESCENCE MICROSCOPY; GENE DELETION; GENETICS; HELA CELL LINE; METABOLISM; MITOSIS; SCHIZOSACCHAROMYCES; TIME LAPSE IMAGING; ULTRASTRUCTURE;

ALLELES; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; HELA CELLS; HUMANS; MEMBRANE PROTEINS; MICROSCOPY, FLUORESCENCE; MITOSIS; MODELS, BIOLOGICAL; NUCLEAR ENVELOPE; NUCLEAR PROTEINS; PHENOTYPE; PROTEIN BINDING; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; SEQUENCE DELETION; TIME-LAPSE IMAGING;

EID: 85015402125     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1613916114     Document Type: Article

References (59)

1. Devos DP, Gräf R, Field MC (2014) Evolution of the nucleus. Curr Opin Cell Biol 28: 8-15.
2. Madhani HD (2013) The frustrated gene: Origins of eukaryotic gene expression. Cell 155(4):744-749.
3. Heath IB (1980) Variant mitoses in lower eukaryotes: Indicators of the evolution of mitosis. Int Rev Cytol 64:1-80.
4. Byers B, Goetsch L (1975) Behavior of spindles and spindle plaques in the cell cycle and conjugation of Saccharomyces cerevisiae. J Bacteriol 124(1):511-523.
5. Kubai DF (1975) The evolution of the mitotic spindle. Int Rev Cytol 43:167-227.
6. Tamm T, et al. (2011) Brr6 drives the Schizosaccharomyces pombe spindle pole body nuclear envelope insertion/extrusion cycle. J Cell Biol 195(3):467-484.
7. McCully EK, Robinow CF (1971) Mitosis in the fission yeast Schizosaccharomyces pombe: A comparative study with light and electron microscopy. J Cell Sci 9(2):475-507.
8. Ding R, West RR, Morphew DM, Oakley BR, McIntosh JR (1997) The spindle pole body of Schizosaccharomyces pombe enters and leaves the nuclear envelope as the cell cycle proceeds. Mol Biol Cell 8(8):1461-1479.
9. Adams IR, Kilmartin JV (2000) Spindle pole body duplication: A model for centrosome duplication? Trends Cell Biol 10(8):329-335.
10. Tallada VA, Tanaka K, Yanagida M, Hagan IM (2009) The S. pombe mitotic regulator Cut12 promotes spindle pole body activation and integration into the nuclear envelope. J Cell Biol 185(5):875-888.
11. Witkin KL, Friederichs JM, Cohen-Fix O, Jaspersen SL (2010) Changes in the nuclear envelope environment affect spindle pole body duplication in Saccharomyces cerevisiae. Genetics 186(3):867-883.
12. Muñoz-Centeno MC, et al. (1999) Saccharomyces cerevisiae MPS2 encodes a membrane protein localized at the spindle pole body and the nuclear envelope. Mol Biol Cell 10(7):2393-2406.
13. Jaspersen SL, Winey M (2004) The budding yeast spindle pole body: Structure, duplication, and function. Annu Rev Cell Dev Biol 20:1-28.
14. Fischer T, et al. (2004) Yeast centrin Cdc31 is linked to the nuclear mRNA export machinery. Nat Cell Biol 6(9):840-848.
15. Niepel M, Strambio-de-Castillia C, Fasolo J, Chait BT, Rout MP (2005) The nuclear pore complex-Associated protein, Mlp2p, binds to the yeast spindle pole body and promotes its efficient assembly. J Cell Biol 170(2):225-235.
16. Frost A, et al. (2012) Functional repurposing revealed by comparing S. pombe and S. cerevisiae genetic interactions. Cell 149(6):1339-1352.
17. Costanzo M, et al. (2010) The genetic landscape of a cell. Science 327(5964):425-431.
18. Henne WM, Buchkovich NJ, Emr SD (2011) The ESCRT pathway. Dev Cell 21(1):77-91.
19. McCullough J, Colf LA, Sundquist WI (2013) Membrane fission reactions of the mammalian ESCRT pathway. Annu Rev Biochem 82:663-692.
20. Hurley JH (2015) ESCRTs are everywhere. EMBO J 34(19):2398-2407.
21. Webster BM, Colombi P, Jäger J, Lusk CP (2014) Surveillance of nuclear pore complex assembly by ESCRT-III/Vps4. Cell 159(2):388-401.
22. Morita E, et al. (2010) Human ESCRT-III and VPS4 proteins are required for centrosome and spindle maintenance. Proc Natl Acad Sci USA 107(29):12889-12894.
23. Olmos Y, Hodgson L, Mantell J, Verkade P, Carlton JG (2015) ESCRT-III controls nuclear envelope reformation. Nature 522(7555):236-239.
24. Vietri M, et al. (2015) Spastin and ESCRT-III coordinate mitotic spindle disassembly and nuclear envelope sealing. Nature 522(7555):231-235.
25. Raab M, et al. (2016) ESCRT III repairs nuclear envelope ruptures during cell migration to limit DNA damage and cell death. Science 352(6283):359-362.
26. Denais CM, et al. (2016) Nuclear envelope rupture and repair during cancer cell migration. Science 352(6283):353-358.
27. Monroe N, Hill CP (2016) Meiotic clade AAA ATPases: Protein polymer disassembly machines. J Mol Biol 428(9 Pt B):1897-1911.
28. Yang D, et al. (2008) Structural basis for midbody targeting of spastin by the ESCRT-III protein CHMP1B. Nat Struct Mol Biol 15(12):1278-1286.
29. Bauer I, Brune T, Preiss R, Kölling R (2015) Evidence for a nonendosomal function of the Saccharomyces cerevisiae ESCRT-III-like protein Chm7. Genetics 201(4):1439-1452.
30. Connell JW, Lindon C, Luzio JP, Reid E (2009) Spastin couples microtubule severing to membrane traffic in completion of cytokinesis and secretion. Traffic 10(1):42-56.
31. Gonzalez Y, Saito A, Sazer S (2012) Fission yeast Lem2 and Man1 perform fundamental functions of the animal cell nuclear lamina. Nucleus 3(1):60-76.
32. King MC, Lusk CP, Blobel G (2006) Karyopherin-mediated import of integral inner nuclear membrane proteins. Nature 442(7106):1003-1007.
33. Barton LJ, Soshnev AA, Geyer PK (2015) Networking in the nucleus: A spotlight on LEM-domain proteins. Curr Opin Cell Biol 34:1-8.
34. Kutay U, Hetzer MW (2008) Reorganization of the nuclear envelope during open mitosis. Curr Opin Cell Biol 20(6):669-677.
35. Brachner A, Reipert S, Foisner R, Gotzmann J (2005) LEM2 is a novel MAN1-related inner nuclear membrane protein associated with A-Type lamins. J Cell Sci 118(Pt 24): 5797-5810.
36. Campsteijn C, Vietri M, Stenmark H (2016) Novel ESCRT functions in cell biology: Spiraling out of control? Curr Opin Cell Biol 41:1-8.
37. Liu HL, Osmani AH, Osmani SA (2015) The inner nuclear membrane protein Src1 is required for stable post-mitotic progression into G1 in Aspergillus nidulans. PLoS One 10(7):e0132489.
38. Tapia O, Fong LG, Huber MD, Young SG, Gerace L (2015) Nuclear envelope protein Lem2 is required for mouse development and regulates MAP and AKT kinases. PLoS One 10(3):e0116196.
39. Banday S, Farooq Z, Rashid R, Abdullah E, Altaf M (2016) Role of inner nuclear membrane protein complex Lem2-Nur1 in heterochromatic gene silencing in S. pombe. J Biol Chem 291(38):20021-20029.
40. Tange Y, et al. (2016) Inner nuclear membrane protein Lem2 augments heterochromatin formation in response to nutritional conditions. Genes Cells 21(8):812-832.
41. Barrales RR, Forn M, Georgescu PR, Sarkadi Z, Braun S (2016) Control of heterochromatin localization and silencing by the nuclear membrane protein Lem2. Genes Dev 30(2):133-148.
42. Huber MD, Guan T, Gerace L (2009) Overlapping functions of nuclear envelope proteins NET25 (Lem2) and emerin in regulation of extracellular signal-regulated kinase signaling in myoblast differentiation. Mol Cell Biol 29(21):5718-5728.
43. Ulbert S, Antonin W, Platani M, Mattaj IW (2006) The inner nuclear membrane protein Lem2 is critical for normal nuclear envelope morphology. FEBS Lett 580(27): 6435-6441.
44. Anderson DJ, Vargas JD, Hsiao JP, Hetzer MW (2009) Recruitment of functionally distinct membrane proteins to chromatin mediates nuclear envelope formation in vivo. J Cell Biol 186(2):183-191.
45. Asencio C, et al. (2012) Coordination of kinase and phosphatase activities by Lem4 enables nuclear envelope reassembly during mitosis. Cell 150(1):122-135.
46. Olmos Y, Perdrix-Rosell A, Carlton JG (2016) Membrane binding by CHMP7 coordinates ESCRT-III-dependent nuclear envelope reformation. Curr Biol 26(19):2635-2641.
47. Morita E, Arii J, Christensen D, Votteler J, Sundquist WI (2012) Attenuated protein expression vectors for use in siRNA rescue experiments. Biotechniques, 10.2144/000113909.
48. Bajorek M, et al. (2009) Biochemical analyses of human IST1 and its function in cytokinesis. Mol Biol Cell 20(5):1360-1373.
49. McCullough J, et al. (2015) Structure and membrane remodeling activity of ESCRT-III helical polymers. Science 350(6267):1548-1551.
50. von Schwedler UK, et al. (2003) The protein network of HIV budding. Cell 114(6): 701-713.
51. McDonald KL, Auer M (2006) High-pressure freezing, cellular tomography, and structural cell biology. Biotechniques 41(2):137-143.
52. Mastronarde DN (2005) Automated electron microscope tomography using robust prediction of specimen movements. J Struct Biol 152(1):36-51.
53. Kremer JR, Mastronarde DN, McIntosh JR (1996) Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116(1):71-76.
54. Mastronarde DN (2008) Correction for non-perpendicularity of beam and tilt axis in tomographic reconstructions with the IMOD package. J Microsc 230(Pt 2):212-217.
55. Díez DC, Seybert A, Frangakis AS (2006) Tilt-series and electron microscope alignment for the correction of the non-perpendicularity of beam and tilt-Axis. J Struct Biol 154(2):195-205.
56. Mackay DR, Elgort SW, Ullman KS (2009) The nucleoporin Nup153 has separable roles in both early mitotic progression and the resolution of mitosis. Mol Biol Cell 20(6): 1652-1660.
57. Talamas JA, Hetzer MW (2011) POM121 and Sun1 play a role in early steps of interphase NPC assembly. J Cell Biol 194(1):27-37.
58. Li P, Noegel AA (2015) Inner nuclear envelope protein SUN1 plays a prominent role in mammalian mRNA export. Nucleic Acids Res 43(20):9874-9888.
59. Webster BM, et al. (2016) Chm7 and Heh1 collaborate to link nuclear pore complex quality control with nuclear envelope sealing. EMBO J 35(22):2447-2467.