Lamin A tail modification by SUMO1 is disrupted by familial partial lipodystrophy-causing mutations

Molecular Biology of the Cell

Volumn 24, Issue 3, 2013, Pages 342-350

  Simon, Dan N ^a   Domaradzki, Tera ^b   Hofmann, Wilma A ^b   Wilson, Katherine L ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LAMIN A; SUMO 1 PROTEIN;

ARTICLE; CELL LINE; CONTROLLED STUDY; ENZYME STRUCTURE; FAMILIAL PARTIAL LIPODYSTROPHY; GENE MUTATION; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN MODIFICATION; PROTEIN MOTIF; SUMOYLATION;

AMINO ACID MOTIFS; ANIMALS; CERCOPITHECUS AETHIOPS; COS CELLS; HELA CELLS; HUMANS; LAMIN TYPE A; LIPODYSTROPHY, FAMILIAL PARTIAL; MUTATION, MISSENSE; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; SUMO-1 PROTEIN; SUMOYLATION; UBIQUITIN-PROTEIN LIGASE COMPLEXES;

EID: 84873353657     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E12-07-0527     Document Type: Article

References (59)

1. Adam SA, Sengupta K, Goldman RD (2008). Regulation of nuclear lamin polymerization by importin alpha. J Biol Chem 283, 8462-8468.
2. Alfaro JF et al. (2012). Tandem mass spectrometry identifies many mouse brain O-GlcNAcylated proteins including EGF domain-specific O-GlcNAc transferase targets. Proc Natl Acad Sci USA 109, 7280-7285.
3. Bidault G, Vatier C, Capeau J, Vigouroux C, Bereziat V (2011). LMNA-linked lipodystrophies: from altered fat distribution to cellular alterations. Biochem Soc Trans 39, 1752-1757.
4. Boguslavsky RL, Stewart CL, Worman HJ (2006). Nuclear lamin A inhibits adipocyte differentiation: implications for Dunnigan-type familial partial lipodystrophy. Hum Mol Genet 15, 653-662.
5. Broers JL, Kuijpers HJ, Ostlund C, Worman HJ, Endert J, Ramaekers FC (2005). Both lamin A and lamin C mutations cause lamina instability as well as loss of internal nuclear lamin organization. Exp Cell Res 304, 582-592.
6. Choudhary C, Kumar C, Gnad F, Nielsen ML, Rehman M, Walther TC, Olsen JV, Mann M (2009). Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325, 834-840.
7. Clements L, Manilal S, Love DR, Morris GE (2000). Direct interaction between emerin and lamin A. Biochem Biophys Res Commun 267, 709-714.
8. Coffinier C, Chang SY, Nobumori C, Tu Y, Farber EA, Toth JI, Fong LG, Young SG (2010). Abnormal development of the cerebral cortex and cerebellum in the setting of lamin B2 deficiency. Proc Natl Acad Sci USA 107, 5076-5081.
9. Coffinier C et al. (2011). Deficiencies in lamin B1 and lamin B2 cause neurodevelopmental defects and distinct nuclear shape abnormalities in neurons. Mol Biol Cell 22, 4683-4692.
10. Cowan J, Li D, Gonzalez-Quintana J, Morales A, Hershberger RE (2010). Morphological analysis of 13 LMNA variants identified in a cohort of 324 unrelated patients with idiopathic or familial dilated cardiomyopathy. Circ Cardiovasc Genet 3, 6-14.
11. Dechat T, Adam SA, Taimen P, Shimi T, Goldman RD (2010a). Nuclear lamins. Cold Spring Harb Perspect Biol 2, a000547.
12. Dechat T, Gesson K, Foisner R (2010b). Lamina-independent lamins in the nuclear interior serve important functions. Cold Spring Harb Symp Quant Biol 75, 533-542.
13. Dechat T, Pfleghaar K, Sengupta K, Shimi T, Shumaker DK, Solimando L, Goldman RD (2008). Nuclear lamins: major factors in the structural organization and function of the nucleus and chromatin. Genes Dev 22, 832-852.
14. Desterro JM, Rodriguez MS, Hay RT (1998). SUMO-1 modification of IkappaBalpha inhibits NF-kappaB activation. Mol Cell 2, 233-239.
15. Dhe-Paganon S, Werner ED, Chi YI, Shoelson SE (2002). Structure of the globular tail of nuclear lamin. J Biol Chem 277, 17381-17384.
16. Dittmer TA, Misteli T (2011). The lamin protein family. Genome Biol 12, 222.
17. Duband-Goulet I et al. (2011). Subcellular localization of SREBP1 depends on its interaction with the C-terminal region of wild-type and disease related A-type lamins. Exp Cell Res 317, 2800-2812.
18. Dutour A et al. (2011). High prevalence of laminopathies among patients with metabolic syndrome. Hum Mol Genet 20, 3779-3786.
19. Eggert M, Radomski N, Linder D, Tripier D, Traub P, Jost E (1993). Identification of novel phosphorylation sites in murine A-type lamins. Eur J Biochem 213, 659-671.
20. Galisson F, Mahrouche L, Courcelles M, Bonneil E, Meloche S, Chelbi-Alix MK, Thibault P (2011). A novel proteomics approach to identify SUMOylated proteins and their modification sites in human cells. Mol Cell Proteomics 10, M110 004796.
21. Gareau JR, Lima CD (2010). The SUMO pathway: emerging mechanisms that shape specificity, conjugation and recognition. Nat Rev Mol Cell Biol 11, 861-871.
22. Geiss-Friedlander R, Melchior F (2007). Concepts in sumoylation: a decade on. Nat Rev Mol Cell Biol 8, 947-956.
23. Gerace L, Huber MD (2012). Nuclear lamina at the crossroads of the cytoplasm and nucleus. J Struct Biol 177, 24-31.
24. Haas M, Jost E (1993). Functional analysis of phosphorylation sites in human lamin A controlling lamin disassembly, nuclear transport and assembly. Eur J Cell Biol 62, 237-247.
25. Haque WA, Oral EA, Dietz K, Bowcock AM, Agarwal AK, Garg A (2003). Risk factors for diabetes in familial partial lipodystrophy, Dunnigan variety. Diabetes Care 26, 1350-1355.
26. Hay RT (2005). SUMO: a history of modification. Mol Cell 18, 1-12.
27. Hofmann WA, Arduini A, Nicol SM, Camacho CJ, Lessard JL, Fuller-Pace FV, de Lanerolle P (2009). SUMOylation of nuclear actin. J Cell Biol 186, 193-200.
28. Johnson ES (2004). Protein modification by SUMO. Annu Rev Biochem 73, 355-382.
29. Kim W et al. (2011a). Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol Cell 44, 325-340.
30. Kim Y, Sharov AA, McDole K, Cheng M, Hao H, Fan CM, Gaiano N, Ko MS, Zheng Y (2011b). Mouse B-type lamins are required for proper organogenesis but not by embryonic stem cells. Science 334, 1706-1710.
31. Krimm I et al. (2002). The Ig-like structure of the C-terminal domain of lamin A/C, mutated in muscular dystrophies, cardiomyopathy, and partial lipodystrophy. Structure 10, 811-822.
32. Lammerding J, Schulze PC, Takahashi T, Kozlov S, Sullivan T, Kamm RD, Stewart CL, Lee RT (2004). Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction. J Clin Invest 113, 370-378.
33. Le Dour et al. (2011). A homozygous mutation of prelamin-A preventing its farnesylation and maturation leads to a severe lipodystrophic phenotype: new insights into the pathogenicity of nonfarnesylated prelamin-A. J Clin Endocrinol Metab 96, E856-862.
34. Lloyd DJ, Trembath RC, Shackleton S (2002). A novel interaction between lamin A and SREBP1: implications for partial lipodystrophy and other laminopathies. Hum Mol Genet 11, 769-777.
35. Malik R, Lenobel R, Santamaria A, Ries A, Nigg EA, Korner R (2009). Quantitative analysis of the human spindle phosphoproteome at distinct mitotic stages. J Proteome Res 8, 4553-4562.
36. Mariappan I, Gurung R, Thanumalayan S, Parnaik VK (2007). Identification of cyclin D3 as a new interaction partner of lamin A/C. Biochem Biophys Res Commun 355, 981-985.
37. Olsen JV, Blagoev B, Gnad F, Macek B, Kumar C, Mortensen P, Mann M (2006). Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127, 635-648.
38. Olsen JV et al. (2010). Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci Signal 3, ra2.
39. Pan C, Olsen JV, Daub H, Mann M (2009). Global effects of kinase inhibitors on signaling networks revealed by quantitative phosphoproteomics. Mol Cell Proteomics 8, 2796-2808.
40. Rigbolt KT, Prokhorova TA, Akimov V, Henningsen J, Johansen PT, Kratchmarova I, Kassem M, Mann M, Olsen JV, Blagoev B (2011). System-wide temporal characterization of the proteome and phosphoproteome of human embryonic stem cell differentiation. Sci Signal 4, rs2.
41. Sarge KD, Park-Sarge OK (2009). Detection of proteins sumoylated in vivo and in vitro. Methods Mol Biol 590, 265-277.
42. Shackleton et al. (2000). LMNA, encoding lamin A/C, is mutated in partial lipodystrophy. Nat Genet 24, 153-156.
43. Simon DN, Wilson KL (2011). The nucleoskeleton as a genome-associated dynamic "network of networks." Nat Rev Mol Cell Biol 12, 695-708.
44. Simon DN, Wilson KL (2013). Partners and post-translational modifications of nuclear lamins. Chromosoma (in press).
45. Simon DN, Zastrow MS, Wilson KL (2010). Direct actin binding to A-and B-type lamin tails and actin filament bundling by the lamin A tail. Nucleus 1, 264-272.
46. Speckman RA, Garg A, Du F, Bennett L, Veile R, Arioglu E, Taylor SI, Lovett M, Bowcock AM (2000). Mutational and haplotype analyses of families with familial partial lipodystrophy (Dunnigan variety) reveal recurrent missense mutations in the globular C-terminal domain of lamin A/C. Am J Hum Genet 66, 1192-1198.
47. Takamori Y, Tamura Y, Kataoka Y, Cui Y, Seo S, Kanazawa T, Kurokawa K, Yamada H (2007). Differential expression of nuclear lamin, the major component of nuclear lamina, during neurogenesis in two germinal regions of adult rat brain. Eur J Neurosci 25, 1653-1662.
48. Taniura H, Glass C, Gerace L (1995). A chromatin binding site in the tail domain of nuclear lamins that interacts with core histones. J Cell Biol 131, 33-44.
49. Tatham MH, Jaffray E, Vaughan OA, Desterro JM, Botting CH, Naismith JH, Hay RT (2001). Polymeric chains of SUMO-2 and SUMO-3 are conjugated to protein substrates by SAE1/SAE2 and Ubc9. J Biol Chem 276, 35368-35374.
50. Visa N, Percipalle P (2010). Nuclear functions of actin. Cold Spring Harb Perspect Biol 2, a000620.
51. Wang Z, Udeshi ND, Slawson C, Compton PD, Sakabe K, Cheung WD, Shabanowitz J, Hunt DF, Hart GW (2010). Extensive crosstalk between O-GlcNAcylation and phosphorylation regulates cytokinesis. Sci Signal 3, ra2.
52. Wilkinson KA, Henley JM (2010). Mechanisms, regulation and consequences of protein SUMOylation. Biochem J 428, 133-145.
53. Wilson KL, Berk JM (2010). The nuclear envelope at a glance. J Cell Sci 123, 1973-1978.
54. Wilson KL, Foisner R (2010). Lamin-binding proteins. Cold Spring Harb Perspect Biol 2, a000554.
55. Worman HJ (2012). Nuclear lamins and laminopathies. J Pathol 226, 316-325.
56. Zastrow MS, Flaherty DB, Benian GM, Wilson KL (2006). Nuclear titin interacts with A-and B-type lamins in vitro and in vivo. J Cell Sci 119, 239-249.
57. Zastrow MS, Vlcek S, Wilson KL (2004). Proteins that bind A-type lamins: integrating isolated clues. J Cell Sci 117, 979-987.
58. Zhang YQ, Sarge KD (2008). Sumoylation regulates lamin A function and is lost in lamin A mutants associated with familial cardiomyopathies. J Cell Biol 182, 35-39.
59. Zhu S, Goeres J, Sixt KM, Bekes M, Zhang XD, Salvesen GS, Matunis MJ (2009). Protection from isopeptidase-mediated deconjugation regulates paralog-selective sumoylation of RanGAP1. Mol Cell 33, 570-580.