Partners and post-translational modifications of nuclear lamins

Chromosoma

Volumn 122, Issue 1-2, 2013, Pages 13-31

  Simon, Dan N ^a   Wilson, Katherine L ^a  

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

Author keywords

Acetylation; Lamin; Laminopathy; Nuclear envelope; Nucleoskeleton; O GlcNAcylation; Oxidation; Phosphorylation; SUMOylation; Ubiquitylation

Indexed keywords

LAMIN; LAMIN A; LAMIN B; LAMIN B1; LAMIN B2; UNCLASSIFIED DRUG;

CELL NUCLEUS; HUMAN; LAMINOPATHY; MUTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PROCESSING; REVIEW;

CELL NUCLEUS; HUMANS; LAMIN TYPE A; LAMIN TYPE B; MUTATION; NUCLEAR ENVELOPE; NUCLEAR MATRIX; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 84876499240     PISSN: 00095915     EISSN: 14320886     Source Type: Journal    
DOI: 10.1007/s00412-013-0399-8     Document Type: Review

References (185)

1. Adam SA, Sengupta K, Goldman RD (2008) Regulation of nuclear lamin polymerization by importin alpha. J Biol Chem 283(13):8462-8468
2. 3H]adenosine: changes during the HeLa cycle. Biochim Biophys Acta 909(3):222-230
3. Al-Haboubi T, Shumaker DK, Koser J, Wehnert M, Fahrenkrog B (2011) Distinct association of the nuclear pore protein Nup153 with A- and B-type lamins. Nucleus 2(5):500-509
4. Alfaro JF, Gong CX, Monroe ME, Aldrich JT, Clauss TR, Purvine SO, Wang Z, Camp DG 2nd, Shabanowitz J, Stanley P, Hart GW, Hunt DF, Yang F, Smith RD (2012) Tandem mass spectrometry identifies many mouse brain O-GlcNAcylated proteins including EGF domain-specific O-GlcNAc transferase targets. Proc Natl Acad Sci U S A 109(19):7280-7285
5. Bao X, Zhang W, Krencik R, Deng H, Wang Y, Girton J, Johansen J, Johansen KM (2005) The JIL-1 kinase interacts with lamin Dm0 and regulates nuclear lamina morphology of Drosophila nurse cells. J Cell Sci 118(Pt 21):5079-5087
6. Barrowman J, Hamblet C, Kane MS, Michaelis S (2012) Requirements for efficient proteolytic cleavage of prelamin A by ZMPSTE24. PLoS One 7(2):e32120
7. Barton RM, Worman HJ (1999) Prenylated prelamin A interacts with Narf, a novel nuclear protein. J Biol Chem 274(42):30008-30018
8. Bartz RR, Piantadosi CA (2010) Clinical review: oxygen as a signaling molecule. Crit Care 14(5):234
9. Beck LA, Hosick TJ, Sinensky M (1990) Isoprenylation is required for the processing of the lamin A precursor. J Cell Biol 110(5):1489-1499
10. Ben-Harush K, Wiesel N, Frenkiel-Krispin D, Moeller D, Soreq E, Aebi U, Herrmann H, Gruenbaum Y, Medalia O (2009) The supramolecular organization of the C. elegans nuclear lamin filament. J Mol Biol 386(5):1392-1402
11. Bengtsson L, Otto H (2008) LUMA interacts with emerin and influences its distribution at the inner nuclear membrane. J Cell Sci 121(4):536-548
12. Bergo MO, Gavino B, Ross J, Schmidt WK, Hong C, Kendall LV, Mohr A, Meta M, Genant H, Jiang Y, Wisner ER, Van Bruggen N, Carano RA, Michaelis S, Griffey SM, Young SG (2002) Zmpste24 deficiency in mice causes spontaneous bone fractures, muscle weakness, and a prelamin A processing defect. Proc Natl Acad Sci U S A 99(20):13049-13054
13. Beullens M, Vancauwenbergh S, Morrice N, Derua R, Ceulemans H, Waelkens E, Bollen M (2005) Substrate specificity and activity regulation of protein kinase MELK. J Biol Chem 280(48):40003-40011
14. Bokenkamp R, Raz V, Venema A, DeRuiter MC, van Munsteren C, Olive M, Nabel EG, Gittenberger-de Groot AC (2011) Differential temporal and spatial progerin expression during closure of the ductus arteriosus in neonates. PLoS One 6(9):e23975
15. 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(24):5797-5810
16. Brussino A, Vaula G, Cagnoli C, Mauro A, Pradotto L, Daniele D, Di Gregorio E, Barberis M, Arduino C, Squadrone S, Abete MC, Migone N, Calabrese O, Brusco A (2009) A novel family with Lamin B1 duplication associated with adult-onset leucoencephalopathy. J Neurol Neurosurg Psychiatry 80(2):237-240
17. Brussino A, Vaula G, Cagnoli C, Panza E, Seri M, Di Gregorio E, Scappaticci S, Camanini S, Daniele D, Bradac GB, Pinessi L, Cavalieri S, Grosso E, Migone N, Brusco A (2010) A family with autosomal dominant leukodystrophy linked to 5q23.2-q23.3 without lamin B1 mutations. Eur J Neurol 17(4):541-549
18. Buendia B, Courvalin JC, Collas P (2001) Dynamics of the nuclear envelope at mitosis and during apoptosis. Cell Mol Life Sci 58(12-13):1781-1789
19. Butin-Israeli V, Adam SA, Goldman AE, Goldman RD (2012) Nuclear lamin functions and disease. Trends Genet 28(9):464-471
20. Cenni V, Bertacchini J, Beretti F, Lattanzi G, Bavelloni A, Riccio M, Ruzzene M, Marin O, Arrigoni G, Parnaik V, Wehnert M, Maraldi NM, de Pol A, Cocco L, Marmiroli S (2008) Lamin A Ser404 is a nuclear target of Akt phosphorylation in C2C12 cells. J Proteome Res 7(11):4727-4735
21. Cenni V, Sabatelli P, Mattioli E, Marmiroli S, Capanni C, Ognibene A, Squarzoni S, Maraldi NM, Bonne G, Columbaro M, Merlini L, Lattanzi G (2005) Lamin A N-terminal phosphorylation is associated with myoblast activation: impairment in Emery-Dreifuss muscular dystrophy. J Med Genet 42(3):214-220
22. 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(5942):834-840
23. Clawson GA, Norbeck LL, Hatem CL, Rhodes C, Amiri P, McKerrow JH, Patierno SR, Fiskum G (1992) Ca(2+)-regulated serine protease associated with the nuclear scaffold. Cell Growth Differ 3(11):827-838
24. 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 U S A 107(11):5076-5081
25. Coffinier C, Jung HJ, Nobumori C, Chang S, Tu Y, Barnes RH 2nd, Yoshinaga Y, de Jong PJ, Vergnes L, Reue K, Fong LG, Young SG (2011) Deficiencies in lamin B1 and lamin B2 cause neurodevelopmental defects and distinct nuclear shape abnormalities in neurons. Mol Biol Cell 22(23):4683-4693
26. Collas P (1999) Sequential PKC- and Cdc2-mediated phosphorylation events elicit zebrafish nuclear envelope disassembly. J Cell Sci 112(6):977-987
27. Collas P, Thompson L, Fields AP, Poccia DL, Courvalin JC (1997) Protein kinase C-mediated interphase lamin B phosphorylation and solubilization. J Biol Chem 272(34):21274-21280
28. 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(1):41-53
29. Cross T, Griffiths G, Deacon E, Sallis R, Gough M, Watters D, Lord JM (2000) PKC-delta is an apoptotic lamin kinase. Oncogene 19(19):2331-2337
30. Daub H, Olsen JV, Bairlein M, Gnad F, Oppermann FS, Korner R, Greff Z, Keri G, Stemmann O, Mann M (2008) Kinase-selective enrichment enables quantitative phosphoproteomics of the kinome across the cell cycle. Mol Cell 31(3):438-448
31. Dechat T, Adam SA, Taimen P, Shimi T, Goldman RD (2010) Nuclear lamins. Cold Spring Harb Perspect Biol 2(11):a000547
32. Dechat T, Korbei B, Vaughan OA, Vlcek S, Hutchison CJ, Foisner R (2000) Lamina-associated polypeptide 2alpha binds intranuclear A-type lamins. J Cell Sci 113(19):3473-3484
33. 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(7):832-853
34. Delbarre E, Tramier M, Coppey-Moisan M, Gaillard C, Courvalin JC, Buendia B (2006) The truncated prelamin A in Hutchinson-Gilford progeria syndrome alters segregation of A-type and B-type lamin homopolymers. Hum Mol Genet 15(7):1113-1122
35. Demmerle J, Koch AJ, Holaska JM (2012) The nuclear envelope protein emerin binds directly to histone deacetylase 3 (HDAC3) and activates HDAC3 activity. J Biol Chem 287(26):22080-22088
36. Dhe-Paganon S, Werner ED, Chi YI, Shoelson SE (2002) Structure of the globular tail of nuclear lamin. J Biol Chem 277(20):17381-17384
37. Dittmer TA, Misteli T (2011) The lamin protein family. Genome Biol 12(5):222
38. Dreuillet C, Tillit J, Kress M, Ernoult-Lange M (2002) In vivo and in vitro interaction between human transcription factor MOK2 and nuclear lamin A/C. Nucleic Acids Res 30(21):4634-4642
39. 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(2):659-671
40. Eggert M, Radomski N, Tripier D, Traub P, Jost E (1991) Identification of phosphorylation sites on murine nuclear lamin C by RP-HPLC and microsequencing. FEBS Lett 292(1-2):205-209
41. Enoch T, Peter M, Nurse P, Nigg EA (1991) p34cdc2 acts as a lamin kinase in fission yeast. J Cell Biol 112(5):797-807
42. Farnsworth CC, Wolda SL, Gelb MH, Glomset JA (1989) Human lamin B contains a farnesylated cysteine residue. J Biol Chem 264(34):20422-20429
43. Favale NO, Sterin Speziale NB, Fernandez Tome MC (2007) Hypertonic-induced lamin A/C synthesis and distribution to nucleoplasmic speckles is mediated by TonEBP/NFAT5 transcriptional activator. Biochem Biophys Res Commun 364(3):443-449
44. Ferraro A, Eufemi M, Cervoni L, Marinetti R, Turano C (1989) Glycosylated forms of nuclear lamins. FEBS Lett 257(2):241-246
45. Fiume R, Ramazzotti G, Teti G, Chiarini F, Faenza I, Mazzotti G, Billi AM, Cocco L (2009) Involvement of nuclear PLCbeta1 in lamin B1 phosphorylation and G2/M cell cycle progression. FASEB J 23(3):957-966
46. Foisner R, Gerace L (1993) Integral membrane proteins of the nuclear envelope interact with lamins and chromosomes, and binding is modulated by mitotic phosphorylation. Cell 73(7):1267-1279
47. Foisner R, Traub P, Wiche G (1991) Protein kinase A- and protein kinase C-regulated interaction of plectin with lamin B and vimentin. Proc Natl Acad Sci U S A 88(9):3812-3816
48. Friedman DL, Ken R (1988) Insulin stimulates incorporation of 32Pi into nuclear lamins A and C in quiescent BHK-21 cells. J Biol Chem 263(3):1103-1106
49. Furukawa K, Kondo T (1998) Identification of the lamina-associated- polypeptide-2-binding domain of B-type lamin. Eur J Biochem 251(3):729-733
50. 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 (2):M110 004796.
51. Gareau JR, Lima CD (2010) The SUMO pathway: emerging mechanisms that shape specificity, conjugation and recognition. Nat Rev Mol Cell Biol 11(12):861-871
52. Geiss-Friedlander R, Melchior F (2007) Concepts in sumoylation: a decade on. Nat Rev Mol Cell Biol 8(12):947-956
53. Gerace L, Blobel G (1980) The nuclear envelope lamina is reversibly depolymerized during mitosis. Cell 19(1):277-287
54. Gerace L, Huber MD (2012) Nuclear lamina at the crossroads of the cytoplasm and nucleus. J Struct Biol 177(1):24-31
55. Glozak MA, Sengupta N, Zhang X, Seto E (2005) Acetylation and deacetylation of non-histone proteins. Gene 363:15-23
56. Goeres J, Chan PK, Mukhopadhyay D, Zhang H, Raught B, Matunis MJ (2011) The SUMO-specific isopeptidase SENP2 associates dynamically with nuclear pore complexes through interactions with karyopherins and the Nup107-160 nucleoporin subcomplex. Mol Biol Cell 22(24):4868-4882
57. Gonzalez JM, Navarro-Puche A, Casar B, Crespo P, Andres V (2008) Fast regulation of AP-1 activity through interaction of lamin A/C, ERK1/2, and c-Fos at the nuclear envelope. J Cell Biol 183(4):653-666
58. Goss VL, Hocevar BA, Thompson LJ, Stratton CA, Burns DJ, Fields AP (1994) Identification of nuclear beta II protein kinase C as a mitotic lamin kinase. J Biol Chem 269(29):19074-19080
59. Grimsby S, Jaensson H, Dubrovska A, Lomnytska M, Hellman U, Souchelnytskyi S (2004) Proteomics-based identification of proteins interacting with Smad3: SREBP-2 forms a complex with Smad3 and inhibits its transcriptional activity. FEBS Lett 577(1-2):93-100
60. Guelen L, Pagie L, Brasset E, Meuleman W, Faza MB, Talhout W, Eussen BH, de Klein A, Wessels L, de Laat W, van Steensel B (2008) Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 453(7197):948-951
61. Guo D, Han J, Adam BL, Colburn NH, Wang MH, Dong Z, Eizirik DL, She JX, Wang CY (2005) Proteomic analysis of SUMO4 substrates in HEK293 cells under serum starvation-induced stress. Biochem Biophys Res Commun 337(4):1308-1318
62. 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(2):237-247
63. Han X, Feng X, Rattner JB, Smith H, Bose P, Suzuki K, Soliman MA, Scott MS, Burke BE, Riabowol K (2008) Tethering by lamin A stabilizes and targets the ING1 tumour suppressor. Nat Cell Biol 10(11):1333-1340
64. 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(10):3738-3751
65. Hart GW, Copeland RJ (2010) Glycomics hits the big time. Cell 143(5):672-676
66. Hay RT (2005) SUMO: a history of modification. Mol Cell 18(1):1-12
67. Heald R, McKeon F (1990) Mutations of phosphorylation sites in lamin A that prevent nuclear lamina disassembly in mitosis. Cell 61(4):579-589
68. Hegele RA, Cao H, Liu DM, Costain GA, Charlton-Menys V, Rodger NW, Durrington PN (2006) Sequencing of the reannotated LMNB2 gene reveals novel mutations in patients with acquired partial lipodystrophy. Am J Hum Genet 79(2):383-389
69. Heitlinger E, Peter M, Haner M, Lustig A, Aebi U, Nigg EA (1991) Expression of chicken lamin B2 in Escherichia coli: characterization of its structure, assembly, and molecular interactions. J Cell Biol 113(3):485-495
70. Hennekes H, Peter M, Weber K, Nigg EA (1993) Phosphorylation on protein kinase C sites inhibits nuclear import of lamin B2. J Cell Biol 120(6):1293-1304
71. Herrmann H, Kreplak L, Aebi U (2004) Isolation, characterization, and in vitro assembly of intermediate filaments. Methods Cell Biol 78:3-24
72. Hocevar BA, Burns DJ, Fields AP (1993) Identification of protein kinase C (PKC) phosphorylation sites on human lamin B. Potential role of PKC in nuclear lamina structural dynamics. J Biol Chem 268(10):7545-7552
73. Holaska JM, Lee KK, Kowalski AK, Wilson KL (2003) Transcriptional repressor germ cell-less (GCL) and barrier to autointegration factor (BAF) compete for binding to emerin in vitro. J Biol Chem 278(9):6969-6975
74. Holaska JM, Wilson KL (2007) An emerin «proteome»: purification of distinct emerin-containing complexes from HeLa cells suggests molecular basis for diverse roles including gene regulation, mRNA splicing, signaling, mechanosensing, and nuclear architecture. Biochemistry 46(30):8897-8908
75. Huang Y, Cai M, Clore GM, Craigie R (2011) No interaction of barrier-to-autointegration factor (BAF) with HIV-1 MA, cone-rod homeobox (Crx) or MAN1-C in absence of DNA. PLoS One 6(9):e25123
76. Imami K, Sugiyama N, Kyono Y, Tomita M, Ishihama Y (2008) Automated phosphoproteome analysis for cultured cancer cells by two-dimensional nanoLC-MS using a calcined titania/C18 biphasic column. Anal Sci 24(1):161-166
77. Isokane M, Hieda M, Hirakawa S, Shudou M, Nakashiro K, Hashimoto K, Hamakawa H, Higashiyama S (2008) Plasma-membrane-anchored growth factor pro-amphiregulin binds A-type lamin and regulates global transcription. J Cell Sci 121(21):3608-3618
78. Itahana Y, Yeh ET, Zhang Y (2006) Nucleocytoplasmic shuttling modulates activity and ubiquitination-dependent turnover of SUMO-specific protease 2. Mol Cell Biol 26(12):4675-4689
79. Ivorra C, Kubicek M, Gonzalez JM, Sanz-Gonzalez SM, Alvarez-Barrientos A, O'Connor JE, Burke B, Andres V (2006) A mechanism of AP-1 suppression through interaction of c-Fos with lamin A/C. Genes Dev 20(3):307-320
80. Johnson ES (2004) Protein modification by SUMO. Annu Rev Biochem 73:355-382
81. Kasahara K, Chida K, Tsunenaga M, Kohno Y, Ikuta T, Kuroki T (1991) Identification of lamin B2 as a substrate of protein kinase C in BALB/MK-2 mouse keratinocytes. J Biol Chem 266(30):20018-20023
82. Kill IR, Hutchison CJ (1995) S-phase phosphorylation of lamin B2. FEBS Lett 377(1):26-30
83. Kim JE, Tannenbaum SR, White FM (2005) Global phosphoproteome of HT-29 human colon adenocarcinoma cells. J Proteome Res 4(4):1339-1346
84. Kim SC, Sprung R, Chen Y, Xu Y, Ball H, Pei J, Cheng T, Kho Y, Xiao H, Xiao L, Grishin NV, White M, Yang XJ, Zhao Y (2006) Substrate and functional diversity of lysine acetylation revealed by a proteomics survey. Mol Cell 23(4):607-618
85. Kim W, Bennett EJ, Huttlin EL, Guo A, Li J, Possemato A, Sowa ME, Rad R, Rush J, Comb MJ, Harper JW, Gygi SP (2011a) Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol Cell 44(2):325-340
86. 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(6063):1706-1710
87. Kolb T, Maass K, Hergt M, Aebi U, Herrmann H (2011) Lamin A and lamin C form homodimers and coexist in higher complex forms both in the nucleoplasmic fraction and in the lamina of cultured human cells. Nucleus 2(5):425-433
88. Krimm I, Ostlund C, Gilquin B, Couprie J, Hossenlopp P, Mornon JP, Bonne G, Courvalin JC, Worman HJ, Zinn-Justin S (2002) The Ig-like structure of the C-terminal domain of lamin A/C, mutated in muscular dystrophies, cardiomyopathy, and partial lipodystrophy. Structure 10(6):811-823
89. Kubben N, Voncken JW, Demmers J, Calis C, van Almen G, Pinto Y, Misteli T (2010) Identification of differential protein interactors of lamin A and progerin. Nucleus 1(6):513-525
90. Kuga T, Nozaki N, Matsushita K, Nomura F, Tomonaga T (2010) Phosphorylation statuses at different residues of lamin B2, B1, and A/C dynamically and independently change throughout the cell cycle. Exp Cell Res 316(14):2301-2312
91. Lai JS, Herr W (1992) Ethidium bromide provides a simple tool for identifying genuine DNA-independent protein associations. Proc Natl Acad Sci U S A 89(15):6958-6962
92. Lee CP, Chen MR (2010) Escape of herpesviruses from the nucleus. Rev Med Virol 20(4):214-230
93. Lee CP, Huang YH, Lin SF, Chang Y, Chang YH, Takada K, Chen MR (2008) Epstein-Barr virus BGLF4 kinase induces disassembly of the nuclear lamina to facilitate virion production. J Virol 82(23):11913-11926
94. Lee KK, Haraguchi T, Lee RS, Koujin T, Hiraoka Y, Wilson KL (2001) Distinct functional domains in emerin bind lamin A and DNA-bridging protein BAF. J Cell Sci 114(Pt 24):4567-4573
95. Libotte T, Zaim H, Abraham S, Padmakumar VC, Schneider M, Lu W, Munck M, Hutchison C, Wehnert M, Fahrenkrog B, Sauder U, Aebi U, Noegel AA, Karakesisoglou I (2005) Lamin A/C-dependent localization of Nesprin-2, a giant scaffolder at the nuclear envelope. Mol Biol Cell 16(7):3411-3424
96. 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(7):769-777
97. Lussi YC, Hugi I, Laurell E, Kutay U, Fahrenkrog B (2011) The nucleoporin Nup88 is interacting with nuclear lamin A. Mol Biol Cell 22(7):1080-1090
98. Ma L, Tsai MY, Wang S, Lu B, Chen R, Iii JR, Zhu X, Zheng Y (2009) Requirement for Nudel and dynein for assembly of the lamin B spindle matrix. Nat Cell Biol 11(3):247-256
99. Maison C, Pyrpasopoulou A, Theodoropoulos PA, Georgatos SD (1997) The inner nuclear membrane protein LAP1 forms a native complex with B-type lamins and partitions with spindle-associated mitotic vesicles. EMBO J 16(16):4839-4850
100. Malhas AN, Lee CF, Vaux DJ (2009) Lamin B1 controls oxidative stress responses via Oct-1. J Cell Biol 184(1):45-55
101. 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(10):4553-4563
102. Mall M, Walter T, Gorjanacz M, Davidson IF, Nga Ly-Hartig TB, Ellenberg J, Mattaj IW (2012) Mitotic lamin disassembly is triggered by lipid-mediated signaling. J Cell Biol 198(6):981-990
103. Mancini MA, Shan B, Nickerson JA, Penman S, Lee WH (1994) The retinoblastoma gene product is a cell cycle-dependent, nuclear matrix-associated protein. Proc Natl Acad Sci U S A 91(1):418-422
104. Mansharamani M, Wilson KL (2005) Direct binding of nuclear membrane protein MAN1 to emerin in vitro and two modes of binding to barrier-to- autointegration factor. J Biol Chem 280(14):13863-13870
105. 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(4):981-985
106. Martelli AM, Bortul R, Tabellini G, Faenza I, Cappellini A, Bareggi R, Manzoli L, Cocco L (2002) Molecular characterization of protein kinase C-alpha binding to lamin A. J Cell Biochem 86(2):320-330
107. Maske CP, Hollinshead MS, Higbee NC, Bergo MO, Young SG, Vaux DJ (2003) A carboxyl-terminal interaction of lamin B1 is dependent on the CAAX endoprotease Rce1 and carboxymethylation. J Cell Biol 162(7):1223-1232
108. Meier R, Muller PR, Hirt A, Leibundgut K, Ridolfi-Luthy A, Wagner HP (1997) Differential phosphorylation of lamin B2 in normal and leukemic cells. Leuk Res 21(9):841-847
109. Mingot JM, Kostka S, Kraft R, Hartmann E, Gorlich D (2001) Importin 13: a novel mediator of nuclear import and export. EMBO J 20(14):3685-3694
110. Mislow JM, Holaska JM, Kim MS, Lee KK, Segura-Totten M, Wilson KL, McNally EM (2002) Nesprin-1alpha self-associates and binds directly to emerin and lamin A in vitro. FEBS Lett 525(1-3):135-140
111. Mitsuhashi H, Hayashi YK, Matsuda C, Noguchi S, Wakatsuki S, Araki T, Nishino I (2010) Specific phosphorylation of Ser458 of A-type lamins in LMNA-associated myopathy patients. J Cell Sci 123(Pt 22):3893-3900
112. Molloy A, Cotter O, van Spaendonk R, Sistermans E, Sweeney B (2012) A patient with a rare leukodystrophy related to lamin B1 duplication. Ir Med J 105(6):186-187
113. Molloy S, Little M (1992) p34cdc2 kinase-mediated release of lamins from nuclear ghosts is inhibited by cAMP-dependent protein kinase. Exp Cell Res 201(2):494-499
114. Moritz A, Li Y, Guo A, Villen J, Wang Y, MacNeill J, Kornhauser J, Sprott K, Zhou J, Possemato A, Ren JM, Hornbeck P, Cantley LC, Gygi SP, Rush J, Comb MJ (2010) Akt-RSK-S6 kinase signaling networks activated by oncogenic receptor tyrosine kinases. Sci Signal 3(136):ra64
115. Neutzner M, Neutzner A (2012) Enzymes of ubiquitination and deubiquitination. Essays Biochem 52:37-50
116. Nigg EA, Kitten GT, Vorburger K (1992) Targeting lamin proteins to the nuclear envelope: the role of CaaX box modifications. Biochem Soc Trans 20(2):500-504
117. 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(3):635-648
118. Olsen JV, Vermeulen M, Santamaria A, Kumar C, Miller ML, Jensen LJ, Gnad F, Cox J, Jensen TS, Nigg EA, Brunak S, Mann M (2010) Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci Signal 3(104):ra3
119. Ozaki T, Saijo M, Murakami K, Enomoto H, Taya Y, Sakiyama S (1994) Complex formation between lamin A and the retinoblastoma gene product: identification of the domain on lamin A required for its interaction. Oncogene 9(9):2649-2653
120. Padiath QS, Saigoh K, Schiffmann R, Asahara H, Yamada T, Koeppen A, Hogan K, Ptacek LJ, Fu YH (2006) Lamin B1 duplications cause autosomal dominant leukodystrophy. Nat Genet 38(10):1114-1123
121. 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(12):2796-2808
122. Pegoraro G, Kubben N, Wickert U, Gohler H, Hoffmann K, Misteli T (2009) Ageing-related chromatin defects through loss of the NURD complex. Nat Cell Biol 11(10):1261-1267
123. Pekovic V, Gibbs-Seymour I, Markiewicz E, Alzoghaibi F, Benham AM, Edwards R, Wenhert M, von Zglinicki T, Hutchison CJ (2011) Conserved cysteine residues in the mammalian lamin A tail are essential for cellular responses to ROS generation. Aging Cell 10(6):1067-1079
124. Pendas AM, Zhou Z, Cadinanos J, Freije JM, Wang J, Hultenby K, Astudillo A, Wernerson A, Rodriguez F, Tryggvason K, Lopez-Otin C (2002) Defective prelamin A processing and muscular and adipocyte alterations in Zmpste24 metalloproteinase-deficient mice. Nat Genet 31(1):94-99
125. Peter A, Stick R (2012) Evolution of the lamin protein family: what introns can tell. Nucleus 3(1)
126. Peter M, Heitlinger E, Haner M, Aebi U, Nigg EA (1991) Disassembly of in vitro formed lamin head-to-tail polymers by CDC2 kinase. EMBO J 10(6):1535-1544
127. Peter M, Nakagawa J, Doree M, Labbe JC, Nigg EA (1990) In vitro disassembly of the nuclear lamina and M phase-specific phosphorylation of lamins by cdc2 kinase. Cell 61(4):591-602
128. Rao L, Modha D, White E (1997) The E1B 19 K protein associates with lamins in vivo and its proper localization is required for inhibition of apoptosis. Oncogene 15(13):1587-1597
129. Reddy KL, Zullo JM, Bertolino E, Singh H (2008) Transcriptional repression mediated by repositioning of genes to the nuclear lamina. Nature 452(7184):243-247
130. 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(164):rs3
131. Roux KJ, Kim DI, Raida M, Burke B (2012) A promiscuous biotin ligase fusion protein identifies proximal and interacting proteins in mammalian cells. J Cell Biol 196(6):801-810
132. Ruan J, Xu C, Bian C, Lam R, Wang JP, Kania J, Min J, Zang J (2012) Crystal structures of the coil 2B fragment and the globular tail domain of human lamin B1. FEBS Lett 586(4):314-318
133. Sakaki M, Koike H, Takahashi N, Sasagawa N, Tomioka S, Arahata K, Ishiura S (2001) Interaction between emerin and nuclear lamins. J Biochem 129(2):321-327
134. Schirmer EC, Gerace L (2004) The stability of the nuclear lamina polymer changes with the composition of lamin subtypes according to their individual binding strengths. J Biol Chem 279(41):42811-42817
135. Schneider U, Mini T, Jeno P, Fisher PA, Stuurman N (1999) Phosphorylation of the major Drosophila lamin in vivo: site identification during both M-phase (meiosis) and interphase by electrospray ionization tandem mass spectrometry. Biochemistry 38(14):4620-4632
136. Schumacher J, Reichenzeller M, Kempf T, Schnolzer M, Herrmann H (2006) Identification of a novel, highly variable amino-terminal amino acid sequence element in the nuclear intermediate filament protein lamin B(2) from higher vertebrates. FEBS Lett 580(26):6211-6216
137. Schuster J, Sundblom J, Thuresson AC, Hassin-Baer S, Klopstock T, Dichgans M, Cohen OS, Raininko R, Melberg A, Dahl N (2011) Genomic duplications mediate overexpression of lamin B1 in adult-onset autosomal dominant leukodystrophy (ADLD) with autonomic symptoms. Neurogenetics 12(1):65-72
138. Shimi T, Pfleghaar K, Kojima S, Pack CG, Solovei I, Goldman AE, Adam SA, Shumaker DK, Kinjo M, Cremer T, Goldman RD (2008) The A- and B-type nuclear lamin networks: microdomains involved in chromatin organization and transcription. Genes Dev 22(24):3409-3421
139. Shimizu T, Cao CX, Shao RG, Pommier Y (1998) Lamin B phosphorylation by protein kinase calpha and proteolysis during apoptosis in human leukemia HL60 cells. J Biol Chem 273(15):8669-8674
140. Shumaker DK, Solimando L, Sengupta K, Shimi T, Adam SA, Grunwald A, Strelkov SV, Aebi U, Cardoso MC, Goldman RD (2008) The highly conserved nuclear lamin Ig-fold binds to PCNA: its role in DNA replication. J Cell Biol 181(2):269-280
141. Sieprath T, Darwiche R, De Vos WH (2012) Lamins as mediators of oxidative stress. Biochem Biophys Res Commun 421(4):635-639
142. Simon DN, Domaradzki T, Hofmann WA, Wilson KL (2013) Lamin A tail modification by SUMO1 is disrupted by familial partial lipodystrophy-causing mutations. Mol Biol Cell 24(3):342-50
143. Simon DN, Wilson KL (2011) The nucleoskeleton as a genome-associated dynamic 'network of networks'. Nat Rev Mol Cell Biol 12(11):695-708
144. 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(3):264-272
145. Smith TC, Fang Z, Luna EJ (2010) Novel interactors and a role for supervillin in early cytokinesis. Cytoskeleton (Hoboken) 67(6):346-364
146. Somech R, Shaklai S, Geller O, Amariglio N, Simon AJ, Rechavi G, Gal-Yam EN (2005) The nuclear-envelope protein and transcriptional repressor LAP2beta interacts with HDAC3 at the nuclear periphery, and induces histone H4 deacetylation. J Cell Sci 118(Pt 17):4017-4025
147. Speese SD, Ashley J, Jokhi V, Nunnari J, Barria R, Li Y, Ataman B, Koon A, Chang YT, Li Q, Moore MJ, Budnik V (2012) Nuclear envelope budding enables large ribonucleoprotein particle export during synaptic Wnt signaling. Cell 149(4):832-846
148. Sridharan DM, McMahon LW, Lambert MW (2006) alphaII-Spectrin interacts with five groups of functionally important proteins in the nucleus. Cell Biol Int 30(11):866-878
149. Steen RL, Beullens M, Landsverk HB, Bollen M, Collas P (2003) AKAP149 is a novel PP1 specifier required to maintain nuclear envelope integrity in G1 phase. J Cell Sci 116(11):2237-2246
150. Steen RL, Collas P (2001) Mistargeting of B-type lamins at the end of mitosis: implications on cell survival and regulation of lamins A/C expression. J Cell Biol 153(3):621-626
151. Stewart CL, Kozlov S, Fong LG, Young SG (2007) Mouse models of the laminopathies. Exp Cell Res 313(10):2144-2156
152. Stierle V, Couprie J, Ostlund C, Krimm I, Zinn-Justin S, Hossenlopp P, Worman HJ, Courvalin JC, Duband-Goulet I (2003) The carboxyl-terminal region common to lamins A and C contains a DNA binding domain. Biochemistry 42(17):4819-4828
153. Strelkov SV, Schumacher J, Burkhard P, Aebi U, Herrmann H (2004) Crystal structure of the human lamin A coil 2B dimer: implications for the head-to-tail association of nuclear lamins. J Mol Biol 343(4):1067-1080
154. Strieter ER, Korasick DA (2012) Unraveling the complexity of ubiquitin signaling. ACS Chem Biol 7(1):52-63
155. Stuurman N (1997) Identification of a conserved phosphorylation site modulating nuclear lamin polymerization. FEBS Lett 401(2-3):171-174
156. Tabellini G, Bortul R, Aluigi M, Billi AM, Bareggi R, Grill V, Narducci P, Martelli AM (2002) Binding of elements of protein kinase C-alpha regulatory domain to lamin B1. Cell Signal 14(10):819-827
157. Takahashi A, Alnemri ES, Lazebnik YA, Fernandes-Alnemri T, Litwack G, Moir RD, Goldman RD, Poirier GG, Kaufmann SH, Earnshaw WC (1996) Cleavage of lamin A by Mch2 alpha but not CPP32: multiple interleukin 1 beta-converting enzyme-related proteases with distinct substrate recognition properties are active in apoptosis. Proc Natl Acad Sci U S A 93(16):8395-8400
158. 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(6):1653-1662
159. Tang K, Finley RL Jr, Nie D, Honn KV (2000) Identification of 12-lipoxygenase interaction with cellular proteins by yeast two-hybrid screening. Biochemistry 39(12):3185-3191
160. 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(1):33-44
161. Thompson LJ, Fields AP (1996) betaII protein kinase C is required for the G2/M phase transition of cell cycle. J Biol Chem 271(25):15045-15053
162. Van Berlo JH, Voncken JW, Kubben N, Broers JL, Duisters R, van Leeuwen RE, Crijns HJ, Ramaekers FC, Hutchison CJ, Pinto YM (2005) A-type lamins are essential for TGF-beta1 induced PP2A to dephosphorylate transcription factors. Hum Mol Genet 14(19):2839-2849
163. Van Hoof D, Munoz J, Braam SR, Pinkse MW, Linding R, Heck AJ, Mummery CL, Krijgsveld J (2009) Phosphorylation dynamics during early differentiation of human embryonic stem cells. Cell Stem Cell 5(2):214-226
164. Varela I, Cadinanos J, Pendas AM, Gutierrez-Fernandez A, Folgueras AR, Sanchez LM, Zhou Z, Rodriguez FJ, Stewart CL, Vega JA, Tryggvason K, Freije JM, Lopez-Otin C (2005) Accelerated ageing in mice deficient in Zmpste24 protease is linked to p53 signalling activation. Nature 437(7058):564-568
165. Vaughan A, Alvarez-Reyes M, Bridger JM, Broers JL, Ramaekers FC, Wehnert M, Morris GE, Whitfield WGF, Hutchison CJ (2001) Both emerin and lamin C depend on lamin A for localization at the nuclear envelope. J Cell Sci 114(14):2577-2590
166. Vergnes L, Peterfy M, Bergo MO, Young SG, Reue K (2004) Lamin B1 is required for mouse development and nuclear integrity. Proc Natl Acad Sci U S A 101(28):10428-10433
167. Vlcek S, Foisner R, Wilson KL (2004) Lco1 is a novel widely expressed lamin-binding protein in the nuclear interior. Exp Cell Res 298(2):499-511
168. Wagner SA, Beli P, Weinert BT, Nielsen ML, Cox J, Mann M, Choudhary C (2011) A proteome-wide, quantitative survey of in vivo ubiquitylation sites reveals widespread regulatory roles. Mol Cell Proteomics 10 (10):M111 013284.
169. Wang B, Malik R, Nigg EA, Korner R (2008) Evaluation of the low-specificity protease elastase for large-scale phosphoproteome analysis. Anal Chem 80(24):9526-9533
170. 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(104):ra2
171. Ward GE, Kirschner MW (1990) Identification of cell cycle-regulated phosphorylation sites on nuclear lamin C. Cell 61(4):561-577
172. Wilkinson KA, Henley JM (2010) Mechanisms, regulation and consequences of protein SUMOylation. Biochem J 428(2):133-145
173. Wilson KL, Foisner R (2010) Lamin-binding proteins. Cold Spring Harb Perspect Biol 2(4):a000554
174. Worman HJ (2012) Nuclear lamins and laminopathies. J Pathol 226(2):316-325
175. Ye Q, Worman HJ (1994) Primary structure analysis and lamin B and DNA binding of human LBR, an integral protein of the nuclear envelope inner membrane. J Biol Chem 269(15):11306-11311
176. Ye Q, Worman HJ (1995) Protein-protein interactions between human nuclear lamins expressed in yeast. Exp Cell Res 219(1):292-298
177. Young SG, Fong LG, Michaelis S (2005) Prelamin A, Zmpste24, misshapen cell nuclei, and progeria - new evidence suggesting that protein farnesylation could be important for disease pathogenesis. J Lipid Res 46(12):2531-2558
178. Zaremba-Czogalla M, Piekarowicz K, Wachowicz K, Koziol K, Dubinska-Magiera M, Rzepecki R (2012) The different function of single phosphorylation sites of Drosophila melanogaster lamin Dm and lamin C. PLoS One 7(2):e32649
179. 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(2):239-249
180. Zastrow MS, Vlcek S, Wilson KL (2004) Proteins that bind A-type lamins: integrating isolated clues. J Cell Sci 117(Pt 7):979-987
181. Zhang D, Beresford PJ, Greenberg AH, Lieberman J (2001) Granzymes A and B directly cleave lamins and disrupt the nuclear lamina during granule-mediated cytolysis. Proc Natl Acad Sci U S A 98(10):5746-5751
182. Zhang H, Saitoh H, Matunis MJ (2002) Enzymes of the SUMO modification pathway localize to filaments of the nuclear pore complex. Mol Cell Biol 22(18):6498-6508
183. 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(1):35-39
184. Zhong N, Radu G, Ju W, Brown WT (2005) Novel progerin-interactive partner proteins hnRNP E1, EGF, Mel 18, and UBC9 interact with lamin A/C. Biochem Biophys Res Commun 338(2):855-861
185. Zullo JM, Demarco IA, Pique-Regi R, Gaffney DJ, Epstein CB, Spooner CJ, Luperchio TR, Bernstein BE, Pritchard JK, Reddy KL, Singh H (2012) DNA sequence-dependent compartmentalization and silencing of chromatin at the nuclear lamina. Cell 149(7):1474-1487