Phosphorylation of lamins determine their structural properties and signaling functions

Nucleus

Volumn 6, Issue 3, 2015, Pages 166-171

  Torvaldson, Elin ^a,b   Kochin, Vitaly ^c   Eriksson, John E ^a,b  

^a ÅBO AKADEMI UNIVERSITY   (Finland)

^b UNIVERSITY OF TURKU   (Finland)

^c SAPPORO MEDICAL UNIVERSITY   (Japan)

Author keywords

Intermediate filaments; Lamin A C; Laminopathy; Lamins; Phosphorylation; Signaling

Indexed keywords

CYCLIN DEPENDENT KINASE 1; LAMIN; LAMIN A; LAMIN C; LMNA PROTEIN, HUMAN;

ARTICLE; CAENORHABDITIS ELEGANS; CELL CYCLE; DOWN REGULATION; EMERY DREIFUSS MUSCULAR DYSTROPHY; GENE MUTATION; HUMAN; INTERMEDIATE FILAMENT; LAMINOPATHY; MITOSIS; NEOPLASM; NONHUMAN; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; ANIMAL; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; HELA CELL LINE; INTERPHASE; METABOLISM; MUTATION; NUCLEAR LAMINA; PATHOLOGY; PHOSPHORYLATION; PROTEIN TRANSPORT; SOLUBILITY;

ANIMALS; CAENORHABDITIS ELEGANS; GENE EXPRESSION REGULATION; HELA CELLS; HUMANS; INTERMEDIATE FILAMENTS; INTERPHASE; LAMIN TYPE A; MITOSIS; MUSCULAR DYSTROPHY, EMERY-DREIFUSS; MUTATION; NUCLEAR LAMINA; PHOSPHORYLATION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; SOLUBILITY;

EID: 84945182149     PISSN: 19491034     EISSN: 19491042     Source Type: Journal    
DOI: 10.1080/19491034.2015.1017167     Document Type: Article

References (53)

1. Hyder CL, Isoniemi KO, Torvaldson ES, Eriksson JE. Insights into intermediate filament regulation from development to ageing. J Cell Sci 2011; 124: 1363-72; PMID: 21502133; http://dx. doi. org/10. 1242/jcs. 041244.
2. Eriksson JE, Dechat T, Grin B, Helfand B, Mendez M, Pallari H-M, Goldman RD. Introducing intermediate filaments: from discovery to disease. J Clin Invest 2009; 119: 1763-71; PMID: 19587451; http://dx. doi. org/10. 1172/JCI38339.
3. Dechat T, Pfleghaar K, Sengupta K, Shimi T, Shumaker DK, Solimando L, Goldman RD. Nuclear lamins: major factors in the structural organization and function of the nucleus and chromatin. Genes Dev 2008; 22: 832-53; PMID: 18381888; http://dx. doi. org/10. 1101/gad. 1652708.
4. Furukawa K, Hotta Y. cDNA cloning of a germ cell specific lamin B3 from mouse spermatocytes and analysis of its function by ectopic expression in somatic cells. EMBO J 1993; 12: 97-106; PMID: 8094052.
5. Gesson K, Vidak S, Foisner R. Lamina-associated polypeptide (LAP)2? and nucleoplasmic lamins in adult stem cell regulation and disease. Semin Cell Dev Biol 2014; 29: 116-24; PMID: 24374133; http://dx. doi. org/10. 1016/j. semcdb. 2013. 12. 009.
6. Shimi T, Pfleghaar K, Kojima S, Pack C-G, Solovei I, Goldman AE, Adam SA, Shumaker DK, Kinjo M, Cremer T, et al. The A-and B-type nuclear lamin networks: microdomains involved in chromatin organization and transcription. Genes Dev 2008; 22: 3409-21; PMID: 19141474; http://dx. doi. org/10. 1101/gad. 1735208.
7. Dechat T, Gesson K, Foisner R. Lamina-Independent lamins in the nuclear interior serve important functions. Cold Spring Harb Symp Quant Biol 2010; 75: 533-43; PMID: 21209392; http://dx. doi. org/10. 1101/sqb. 2010. 75. 018.
8. Erber A, Riemer D, Bovenschulte M, Weber K. Molecular phylogeny of metazoan intermediate filament proteins. J Mol Evol 1998; 47: 751-62; PMID: 9847417; http://dx. doi. org/10. 1007/PL00006434.
9. Herrmann H, Strelkov SV. History and phylogeny of intermediate filaments: now in insects. BMC Biol 2011; 9: 16; PMID: 21356127; http://dx. doi. org/10. 1186/1741-7007-9-16.
10. Peter A, Stick R. Evolution of the lamin protein family: what introns can tell. Nucl Austin Tex 2012; 3: 44-59; PMID: 22156746.
11. Weber K, Plessmann U, Ulrich W. Cytoplasmic intermediate filament proteins of invertebrates are closer to nuclear lamins than are vertebrate intermediate filament proteins; sequence characterization of two muscle proteins of a nematode. EMBO J 1989; 8: 3221-7; PMID: 2583097.
12. Coffinier C, Chang SY, Nobumori C, Tu Y, Farber EA, Toth JI, Fong LG, Young SG. Abnormal development of the cerebral cortex and cerebellum in the setting of lamin B2 deficiency. Proc Natl Acad Sci U S A 2010; 107: 5076-81; PMID: 20145110; http://dx. doi. org/10. 1073/pnas. 0908790107.
13. Lee JM, Tu Y, Tatar A, Wu D, Nobumori C, Jung H-J, Yoshinaga Y, Coffinier C, de Jong PJ, Fong LG, et al. Reciprocal knock-in mice to investigate the functional redundancy of lamin B1 and lamin B2. Mol Biol Cell 2014; 25: 1666-75; PMID: 24672053; http://dx. doi. org/10. 1091/mbc. E14-01-0683.
14. Kim Y, Sharov AA, McDole K, Cheng M, Hao H, Fan C-M, Gaiano N, Ko MSH, Zheng Y. Mouse B-type lamins are required for proper organogenesis but not by embryonic stem cells. Science 2011; 334: 1706-10; PMID: 22116031; http://dx. doi. org/10. 1126/science. 1211222.
15. Liu J, Ben-Shahar TR, Riemer D, Treinin M, Spann P, Weber K, Fire A, Gruenbaum Y. Essential roles for caenorhabditis elegans lamin gene in nuclear organization, cell cycle progression, and spatial organization of nuclear pore complexes. Mol Biol Cell 2000; 11: 3937-47; PMID: 11071918; http://dx. doi. org/10. 1091/mbc. 11. 11. 3937.
16. Kim Y, Zheng X, Zheng Y. Proliferation and differentiation of mouse embryonic stem cells lacking all lamins. Cell Res 2013; 23: 1420-3; PMID: 23979018; http://dx. doi. org/10. 1038/cr. 2013. 118.
17. Eckersley-Maslin MA, Bergmann JH, Lazar Z, Spector DL. Lamin A/C is expressed in pluripotent mouse embryonic stem cells. Nucl Austin Tex 2013; 4: 53-60; PMID: 23324457; http://dx. doi. org/10. 4161/nucl. 23384.
18. Simon DN, Wilson KL. Partners and post-translational modifications of nuclear lamins. Chromosoma 2013; 122: 13-31; PMID: 23475188; http://dx. doi. org/10. 1007/s00412-013-0399-8.
19. Snider NT, Omary MB. Post-translational modifications of intermediate filament proteins: mechanisms and functions. Nat Rev Mol Cell Biol 2014; 15: 163-77; PMID: 24556839; http://dx. doi. org/10. 1038/nrm3753.
20. Lüscher B, Brizuela L, Beach D, Eisenman RN. A role for the p34cdc2 kinase and phosphatases in the regulation of phosphorylation and disassembly of lamin B2 during the cell cycle. EMBO J 1991; 10: 865-75; PMID: 1849074.
21. Ottaviano Y, Gerace L. Phosphorylation of the nuclear lamins during interphase and mitosis. J Biol Chem 1985; 260: 624-32; PMID: 3965465.
22. Rzepecki R, Fisher PA. In vivo phosphorylation of drosophila melanogaster nuclear lamins during both interphase and mitosis. Cell Mol Biol Lett 2002; 7: 859-76; PMID: 12378269.
23. Peter M, Nakagawa J, Dorée M, Labbé JC, Nigg EA. In vitro disassembly of the nuclear lamina and M phasespecific phosphorylation of lamins by cdc2 kinase. Cell 1990; 61: 591-602; PMID: 2188731; http://dx. doi. org/10. 1016/0092-8674(90)90471-P.
24. Heald R, McKeon F. Mutations of phosphorylation sites in lamin A that prevent nuclear lamina disassembly in mitosis. Cell 1990; 61: 579-89; PMID: 2344612; http://dx. doi. org/10. 1016/0092-8674(90)90470-Y.
25. Dessev GN, Iovcheva-Dessev C, Goldman RD. Lamin dimers. presence in the nuclear lamina of surf clam oocytes and release during nuclear envelope breakdown. J Biol Chem 1990; 265: 12636-41; PMID: 2373705.
26. Dessev G, Iovcheva-Dessev C, Bischoff JR, Beach D, Goldman R. A complex containing p34cdc2 and cyclin B phosphorylates the nuclear lamin and disassembles nuclei of clam oocytes in vitro. J Cell Biol 1991; 112: 523-33; PMID: 1825210; http://dx. doi. org/10. 1083/jcb. 112. 4. 523.
27. Enoch T, Peter M, Nurse P, Nigg EA. p34cdc2 acts as a lamin kinase in fission yeast. J Cell Biol 1991; 112: 797-807; PMID: 1999458; http://dx. doi. org/10. 1083/jcb. 112. 5. 797.
28. Goss VL, Hocevar BA, Thompson LJ, Stratton CA, Burns DJ, Fields AP. Identification of nuclear β II protein kinase C as a mitotic lamin kinase. J Biol Chem 1994; 269: 19074-80; PMID: 8034666.
29. Peter M, Heitlinger E, Häner M, Aebi U, Nigg EA. Disassembly of in vitro formed lamin head-to-tail polymers by CDC2 kinase. EMBO J 1991; 10: 1535-44; PMID: 1851086.
30. Mall M, Walter T, Gorjánácz M, Davidson IF, Nga Ly-Hartig TB, Ellenberg J, Mattaj IW. Mitotic lamin disassembly is triggered by lipid-mediated signaling. J Cell Biol 2012; 198: 981-90; PMID: 22986494; http://dx. doi. org/10. 1083/jcb. 201205103.
31. Chang K-H, Multani PS, Sun K-H, Vincent F, de Pablo Y, Ghosh S, Gupta R, Lee H-P, Lee H, Smith MA, et al. Nuclear envelope dispersion triggered by deregulated Cdk5 precedes neuronal death. Mol Biol Cell 2011; 22: 1452-62; PMID: 21389115; http://dx. doi. org/10. 1091/mbc. E10-07-0654.
32. Bertacchini J, Beretti F, Cenni V, Guida M, Gibellini F, Mediani L, Marin O, Maraldi NM, de Pol A, Lattanzi G, et al. The protein kinase Akt/PKB regulates both prelamin a degradation and lmna gene expression. FASEB J Off Publ Fed Am Soc Exp Biol 2013; 27: 2145-55; PMID: 23430973; http://dx. doi. org/10. 1096/fj. 12-218214.
33. Kochin V, Shimi T, Torvaldson E, Adam SA, Goldman A, Pack C-G, Melo-Cardenas J, Imanishi SY, Goldman RD, Eriksson JE. Interphase phosphorylation of lamin A. J Cell Sci 2014; 127: 2683-96; PMID: 24741066; http://dx. doi. org/10. 1242/jcs. 141820.
34. Eriksson M, Brown WT, Gordon LB, Glynn MW, Singer J, Scott L, Erdos MR, Robbins CM, Moses TY, Berglund P, et al. Recurrent de novo point mutations in lamin a cause hutchinson-gilford progeria syndrome. Nature 2003; 423: 293-8; PMID: 12714972; http://dx. doi. org/10. 1038/nature01629.
35. Yoon BC, Jung H, Dwivedy A, O'Hare CM, Zivraj KH, Holt CE. Local translation of extranuclear lamin B promotes axon maintenance. Cell 2012; 148: 752-64; PMID: 22341447; http://dx. doi. org/10. 1016/j. cell. 2011. 11. 064.
36. Swift J, Ivanovska IL, Buxboim A, Harada T, Dingal PCDP, Pinter J, Pajerowski JD, Spinler KR, Shin J-W, Tewari M, et al. Nuclear lamin-a scales with tissue stiffness and enhances matrix-directed differentiation. Science 2013; 341: 1240104; PMID: 23990565; http://dx. doi. org/10. 1126/science. 1240104.
37. Isermann P, Lammerding J. Nuclear mechanics and mechanotransduction in health and disease. Curr Biol 2013; 23: R1113-21; PMID: 24355792; http://dx. doi. org/10. 1016/j. cub. 2013. 11. 009.
38. Camozzi D, Capanni C, Cenni V, Mattioli E, Columbaro M, Squarzoni S, Lattanzi G. Diverse lamin-dependent mechanisms interact to control chromatin dynamics: focus on laminopathies. Nucl Austin Tex 2014; 5: 427-40; PMID: 25482195.
39. Ho CY, Jaalouk DE, Vartiainen MK, Lammerding J. Lamin A/C and emerin regulate MKL1-SRF activity by modulating actin dynamics. Nature 2013; 497: 507-11; PMID: 23644458; http://dx. doi. org/10. 1038/nature12105.
40. Dreuillet C, Tillit J, Kress M, Ernoult-Lange M. In vivo and in vitro interaction between human transcription factor MOK2 and nuclear lamin A/C. Nucleic Acids Res 2002; 30: 4634-42; PMID: 12409453; http://dx. doi. org/10. 1093/nar/gkf587.
41. Lloyd DJ, Trembath RC, Shackleton S. A novel interaction between lamin A and SREBP1: implications for partial lipodystrophy and other laminopathies. Hum Mol Genet 2002; 11: 769-77; PMID: 11929849; http://dx. doi. org/10. 1093/hmg/11. 7. 769.
42. Markiewicz E, Dechat T, Foisner R, Quinlan RA, Hutchison CJ. Lamin A/C binding protein LAP2α Is required for nuclear anchorage of retinoblastoma protein. Mol Biol Cell 2002; 13: 4401-13; PMID: 12475961; http://dx. doi. org/10. 1091/mbc. E02-07-0450.
43. Harada T, Swift J, Irianto J, Shin J-W, Spinler KR, Athirasala A, Diegmiller R, Dingal PCDP, Ivanovska IL, Discher DE. Nuclear lamin stiffness is a barrier to 3D migration, but softness can limit survival. J Cell Biol 2014; 204: 669-82; PMID: 24567359; http://dx. doi. org/10. 1083/jcb. 201308029.
44. Foster CR, Przyborski SA, Wilson RG, Hutchison CJ. Lamins as cancer biomarkers. Biochem Soc Trans 2010; 38: 297; PMID: 20074078; http://dx. doi. org/10. 1042/BST0380297.
45. Naetar N, Foisner R. Lamin complexes in the nuclear interior control progenitor cell proliferation and tissue homeostasis. Cell Cycle Georget Tex 2009; 8: 1488-93; PMID: 19377295; http://dx. doi. org/10. 4161/cc. 8. 10. 8499.
46. Naetar N, Korbei B, Kozlov S, Kerenyi MA, Dorner D, Kral R, Gotic I, Fuchs P, Cohen TV, Bittner R, et al. Loss of nucleoplasmic LAP2α-lamin a complexes causes erythroid and epidermal progenitor hyperproliferation. Nat Cell Biol 2008; 10: 1341-8; PMID: 18849980; http://dx. doi. org/10. 1038/ncb1793.
47. Dechat T, Korbei B, Vaughan OA, Vlcek S, Hutchison CJ, Foisner R. Lamina-associated polypeptide 2alpha binds intranuclear a-type lamins. J Cell Sci 2000; 113 19: 3473-84; PMID: 10984438.
48. UMD-LMNA at www. umd. be; [Internet].; [cited 2014 Oct 9]; Available from: http://www. umd. be/LMNA/.
49. Cenni V, Sabatelli P, Mattioli E, Marmiroli S, Capanni C, Ognibene A, Squarzoni S, Maraldi N, Bonne G, Columbaro M, et al. Lamin A N-terminal phosphorylation is associated with myoblast activation: impairment in emery-dreifuss muscular dystrophy. J Med Genet 2005; 42: 214-20; PMID: 15744034; http://dx. doi. org/10. 1136/jmg. 2004. 026112.
50. Mitsuhashi H, Hayashi YK, Matsuda C, Noguchi S, Wakatsuki S, Araki T, Nishino I. Specific phosphorylation of Ser458 of A-type lamins in LMNA-associated myopathy patients. J Cell Sci 2010; 123: 3893-900; PMID: 20980393; http://dx. doi. org/10. 1242/jcs. 072157.
51. Guo H, Luo N, Hao F, Bai Y. p. Pro4Arg mutation in LMNA gene: a new atypical progeria phenotype without metabolism abnormalities. Gene 2014; 546: 35-9; PMID: 24861648; http://dx. doi. org/10. 1016/j. gene. 2014. 05. 042.
52. Garg A, Subramanyam L, Agarwal AK, Simha V, Levine B, D'Apice MR, Novelli G, Crow Y. Atypical progeroid syndrome due to heterozygous missense LMNA mutations. J Clin Endocrinol Metab 2009; 94: 4971-83; PMID: 19875478; http://dx. doi. org/10. 1210/jc. 2009-0472.
53. Pethig K, Genschel J, Peters T, Wilhelmi M, Flemming P, Lochs H, Haverich A, Schmidt HH-J. LMNA Mutations in cardiac transplant recipients. Cardiol 2005; 103: 57-62; PMID: 15539782; http://dx. doi. org/10. 1159/000082048.