Multiple mechanisms actively target the SUN protein UNC-84 to the inner nuclear membrane

Molecular Biology of the Cell

Volumn 22, Issue 10, 2011, Pages 1739-1752

  Tapley, Erin C ^a   Ly, Nina ^a   Starr, Daniel A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAENORHABDITIS ELEGANS PROTEIN; HYBRID PROTEIN; MEMBRANE PROTEIN; PROTEIN KASH; PROTEIN SUN; PROTEIN SUN1; PROTEIN UNC 84; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL MIGRATION; CELL NUCLEUS MEMBRANE; ENDOPLASMIC RETICULUM; GENE MUTATION; GENE SEQUENCE; GENETIC CONSERVATION; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN TARGETING; PROTEIN TRANSPORT;

AMINO ACID SEQUENCE; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL NUCLEUS; CLONING, MOLECULAR; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LARVA; MEMBRANE GLYCOPROTEINS; MUTAGENESIS, SITE-DIRECTED; NUCLEAR ENVELOPE; NUCLEAR LOCALIZATION SIGNALS; NUCLEAR PROTEINS; PEPTIDE FRAGMENTS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; SEQUENCE DELETION;

CAENORHABDITIS ELEGANS; MAMMALIA;

EID: 79955966597     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E10-08-0733     Document Type: Article

References (59)

1. Akhtar A, Gasser SM (2007). The nuclear envelope and transcriptional control. Nat Rev Genet 8, 507-517. (Pubitemid 46955211)
2. Bolender RP (1974). Stereological analysis of the guinea pig pancreas. I. Analytical model and quantitative description of nonstimulated pancreatic exocrine cells. J Cell Biol 61, 269-287.
3. Braunagel SC, Williamson ST, Ding Q, Wu X, Summers MD (2007). Early sorting of inner nuclear membrane proteins is conserved. Proc Natl Acad Sci USA 104, 9307-9312. (Pubitemid 47185775)
4. Braunagel SC, Williamson ST, Saksena S, Zhong Z, Russell WK, Russell DH, Summers MD (2004). Trafficking of ODV-E66 is mediated via a sorting motif and other viral proteins: facilitated trafficking to the inner nuclear membrane. Proc Natl Acad Sci USA 101, 8372-8377. (Pubitemid 38736582)
5. Brenner S (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
6. Cokol M, Nair R, Rost B (2000). Finding nuclear localization signals. EMBO Rep 1, 411-415.
7. Cook A, Bono F, Jinek M, Conti E (2007). Structural biology of nucleocytoplasmic transport. Annu Rev Biochem 76, 647-671.
8. Crisp M, Liu Q, Roux K, Rattner JB, Shanahan C, Burke B, Stahl PD, Hodzic D (2006). Coupling of the nucleus and cytoplasm: role of the LINC complex. J Cell Biol 172, 41-53. (Pubitemid 43042628)
9. Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007). Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2, 953-971. (Pubitemid 46745592)
10. Epstein HF, Casey DL, Ortiz I (1993). Myosin and paramyosin of Caenorhabditis elegans embryos assemble into nascent structures distinct from thick filaments and multi-filament assemblages. J Cell Biol 122, 845-858. (Pubitemid 23241094)
11. Fridolfsson HN, Ly N, Meyerzon M, Starr DA (2010). UNC-83 coordinates kinesin-1 and dynein activities at the nuclear envelope during nuclear migration. Dev Biol 338, 237-250.
12. Galy V, Mattaj IW, Askjaer P (2003). Caenorhabditis elegans nucleoporins Nup93 and Nup205 determine the limit of nuclear pore complex size exclusion in vivo. Mol Biol Cell 14, 5104-5115. (Pubitemid 37484824)
13. Geles KG, Adam SA (2001). Germline and developmental roles of the nuclear transport factor importin alpha3 in C. elegans. Development 128, 1817-1830. (Pubitemid 32514861)
14. Gruenbaum Y, Margalit A, Goldman RD, Shumaker DK, Wilson KL (2005). The nuclear lamina comes of age. Nat Rev 6, 21-31. (Pubitemid 40064896)
15. Haque F, Lloyd DJ, Smallwood DT, Dent CL, Shanahan CM, Fry AM, Trembath RC, Shackleton S (2006). SUN1 interacts with nuclear lamin A and cytoplasmic nesprins to provide a physical connection between the nuclear lamina and the cytoskeleton. Mol Cell Biol 26, 3738-3751. (Pubitemid 43726392)
16. Haque F, Mazzeo D, Patel JT, Smallwood DT, Ellis JA, Shannahan CM, Shackleton S (2010). Mammalian SUN protein networks at the inner nuclear membrane and their role in laminopathy disease processes. J Biol Chem 285, 3487-3498.
17. Hasan S, Guttinger S, Muhlhausser P, Anderegg F, Burgler S, Kutay U (2006). Nuclear envelope localization of human UNC84A does not require nuclear lamins. FEBS Lett 580, 1263-1268. (Pubitemid 43221987)
18. Hodzic DM, Yeater DB, Bengtsson L, Otto H, Stahl PD (2004). Sun2 is a novel mammalian inner nuclear membrane protein. J Biol Chem 279, 25805-25812. (Pubitemid 38756845)
19. Holmer L, Worman HJ (2001). Inner nuclear membrane proteins: functions and targeting. Cell Mol Life Sci 58, 1741-1747. (Pubitemid 33108764)
20. Horton P, Nakai K (1997). Better prediction of protein cellular localization sites with the k nearest neighbors classifier. Proc Int Conf Intell Syst Mol Biol 5, 147-152.
21. Horton RM, Cai ZL, Ho SN, Pease LR (1990). Gene splicing by overlap extension: tailor-made genes using the polymerase chain reaction. Biotechniques 8, 528-535. (Pubitemid 20153761)
22. Horvitz HR, Sulston JE (1980). Isolation and genetic characterization of cell-lineage mutants of the nematode Caenorhabditis elegans. Genetics 96, 435-454.
23. Kalderon D, Roberts BL, Richardson WD, Smith AE (1984). A short amino acid sequence able to specify nuclear location. Cell 39, 499-509. (Pubitemid 15198589)
24. King MC, Lusk CP, Blobel G (2006). Karyopherin-mediated import of integral inner nuclear membrane proteins. Nature 442, 1003-1007. (Pubitemid 44330251)
25. Kohara Y (1996). [Large scale analysis of C. elegans cDNA]. Tanpakushitsu Kakusan Koso 41, 715-720.
26. LaCasse EC, Lefebvre YA (1995). Nuclear localization signals overlap DNA- or RNA-binding domains in nucleic acid-binding proteins. Nucleic Acids Res 23, 1647-1656.
27. Lange A, Mills RE, Lange CJ, Stewart M, Devine SE, Corbett AH (2007). Classical nuclear localization signals: definition, function, and interaction with importin alpha. J Biol Chem 282, 5101-5105. (Pubitemid 47093710)
28. Lee KK, Starr DA, Cohen M, Liu J, Han M, Wilson KL, Gruenbaum Y (2002). Lamin-dependent localization of UNC-84, a protein required for nuclear migration in C. elegans. Mol Biol Cell 13, 892-901. (Pubitemid 34250353)
29. Liu D, Wu X, Summers MD, Lee A, Ryan KJ, Braunagel SC (2010). Truncated isoforms of Kap60 facilitate trafficking of Heh2 to the nuclear envelope. Traffic 11, 1506-1518.
30. Liu Q, Pante N, Misteli T, Elsagga M, Crisp M, Hodzic D, Burke B, Roux KJ (2007). Functional association of Sun1 with nuclear pore complexes. J Cell Biol 178, 785-798. (Pubitemid 47347364)
31. Lu X, Shi Y, Lu Q, Ma Y, Luo J, Wang Q, Ji J, Jiang Q, Zhang C (2010). Requirement for lamin B receptor and its regulation by importin β and phosphorylation in nuclear envelope assembly during mitotic exit. J Biol Chem 285, 33281-33293.
32. Lusk CP, Blobel G, King MC (2007). Highway to the inner nuclear membrane: rules for the road. Nat Rev 8, 414-420. (Pubitemid 46643242)
33. Malone CJ, Fixsen WD, Horvitz HR, Han M (1999). UNC-84 localizes to the nuclear envelope and is required for nuclear migration and anchoring during C. elegans development. Development 126, 3171-3181. (Pubitemid 29378180)
34. McGee MD, Rillo R, Anderson AS, Starr DA (2006). 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 17, 1790-1801. (Pubitemid 44011595)
35. McGee MD, Stagljar I, Starr DA (2009). KDP-1 is a nuclear envelope KASH protein required for cell-cycle progression. J Cell Sci 122, 2895-2905.
36. Mello CC, Kramer JM, Stinchcomb D, Ambros V (1991). Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J 10, 3959-3970. (Pubitemid 21905425)
37. Meyerzon M, Fridolfsson HN, Ly N, McNally FJ, Starr DA (2009). UNC-83 is a nuclear-specific cargo adaptor for kinesin-1-mediated nuclear migration. Development 136, 2725-2733.
38. Nigg EA (1997). Nucleocytoplasmic transport: signals, mechanisms and regulation. Nature 386, 779-787.
39. Ohba T, Schirmer EC, Nishimoto T, Gerace L (2004). Energy- and temperature-dependent transport of integral proteins to the inner nuclear membrane via the nuclear pore. J Cell Biol 167, 1051-1062. (Pubitemid 40066621)
40. Ostlund C, Sullivan T, Stewart CL, Worman HJ (2006). Dependence of diffusional mobility of integral inner nuclear membrane proteins on A-type lamins. Biochemistry 45, 1374-1382. (Pubitemid 43214802)
41. Powell L, Burke B (1990). Internuclear exchange of an inner nuclear membrane protein (p55) in heterokaryons: in vivo evidence for the interaction of p55 with the nuclear lamina. J Cell Biol 111, 2225-2234. (Pubitemid 120014509)
42. Rupp RA, Snider L, Weintraub H (1994). Xenopus embryos regulate the nuclear localization of XMyoD. Genes Dev 8, 1311-1323. (Pubitemid 24181322)
43. Sagasti A, Hisamoto N, Hyodo J, Tanaka-Hino M, Matsumoto K, Bargmann CI (2001). The CaMKII UNC-43 activates the MAPKKK NSY-1 to execute a lateral signaling decision required for asymmetric olfactory neuron fates. Cell 105, 221-232. (Pubitemid 32429512)
44. Saksena S, Summers MD, Burks JK, Johnson AE, Braunagel SC (2006). Importin-alpha-16 is a translocon-associated protein involved in sorting membrane proteins to the nuclear envelope. Nat Struct Mol Biol 13, 500-508. (Pubitemid 43848904)
45. Schirmer EC, Florens L, Guan T, Yates JR 3rd, Gerace L (2003). Nuclear membrane proteins with potential disease links found by subtractive proteomics. Science 301, 1380-1382. (Pubitemid 37075814)
46. Starr DA (2009). A nuclear-envelope bridge positions nuclei and moves chromosomes. J Cell Sci 122, 577-586.
47. Starr DA, Fridolfsson HN (2010). Interactions between nuclei and the cytoskeleton are mediated by SUN-KASH nuclear-envelope bridges. Annu Rev Cell Dev Biol 26, 421-444.
48. Starr DA, Han M (2002). Role of ANC-1 in tethering nuclei to the actin cytoskeleton. Science 298, 406-409. (Pubitemid 35176347)
49. Starr DA, Hermann GJ, Malone CJ, Fixsen W, Priess JR, Horvitz HR, Han M (2001). unc-83 encodes a novel component of the nuclear envelope and is essential for proper nuclear migration. Development 128, 5039-5050. (Pubitemid 34083031)
50. Stewart CL, Roux KJ, Burke B (2007). Blurring the boundary: the nuclear envelope extends its reach. Science 318, 1408-1412. (Pubitemid 350208920)
51. Stewart M (2007). Molecular mechanism of the nuclear protein import cycle. Nat Rev 8, 195-208.
52. Sulston JE, Schierenberg E, White JG, Thomson JN (1983). The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 100, 64-119.
53. Turgay Y, Ungricht R, Rothballer A, Kiss A, Csucs G, Horvath P, Kutay U (2010). A classical NLS and the SUN domain contribute to the targeting of SUN2 to the inner nuclear membrane. EMBO J 29, 2262-2275.
54. von Heijne G (1992). Membrane protein structure predictionHydrophobicity analysis and the positive-inside rule. J Mol Biol 225, 487-494.
55. Weibel ER, Staubli W, Gnagi HR, Hess FA (1969). Correlated morphometric and biochemical studies on the liver cellIMorphometric model, stereologic methods, and normal morphometric data for rat liver. J Cell Biol 42, 68-91.
56. Wilkie GS et al. (2011). Several novel nuclear envelope transmembrane proteins identified in skeletal muscle have cytoskeletal associations. Mol Cell Proteomics 10, M110 003129.
57. Worman HJ, Bonne G (2007). "Laminopathies": a wide spectrum of human diseases. Exp Cell Res 313, 2121-2133.
58. Xu D, Farmer A, Chook YM (2010). Recognition of nuclear targeting signals by Karyopherin-beta proteins. Curr Opin Struct Biol 20, 782-790.
59. Yochem J, Gu T, Han M (1998). A new marker for mosaic analysis in Caenorhabditis elegans indicates a fusion between hyp6 and hyp7, two major components of the hypodermis. Genetics 149, 1323-1334. (Pubitemid 28334526)