Abstract
Lamins are nuclear intermediate filament proteins that are conserved in all multicellular animals. Proteins that resemble lamins are also found in unicellular organisms and in plants. Lamins form a proteinaceous meshwork that outlines the nucleoplasmic side of the inner nuclear membrane, while a small fraction of lamin molecules is also present in the nucleoplasm. They provide structural support for the nucleus and help regulate many other nuclear activities. Much of our knowledge on the function of nuclear lamins and their associated proteins comes from studies in invertebrate organisms and specifically in the nematode Caenorhabditis elegans and the fruit fly Drosophila melanogaster. The simpler lamin system and the powerful genetic tools offered by these model organisms greatly promote such studies. Here we provide an overview of recent advances in the biology of invertebrate nuclear lamins, with special emphasis on their assembly, cellular functions and as models for studying the molecular basis underlying the pathology of human heritable diseases caused by mutations in lamins A/C.
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Abbreviations
- EDMD:
-
Emery–Dreifuss muscular dystrophy
- IF:
-
Intermediate filament
- INM:
-
Inner nuclear membrane
- LINC:
-
Linker of nucleoskeleton and cytoskeleton
- NLS:
-
Nuclear localization signal
- NPC:
-
Nuclear pore complex
- ONM:
-
Outer nuclear membrane
- PEV:
-
Position effect variegation
References
Bank EM, Gruenbaum Y (2011) The nuclear lamina and heterochromatin: a complex relationship. Biochem Soc Trans 39(6):1705–1709. doi:10.1042/BST20110603
Prokocimer M, Davidovich M, Nissim-Rafinia M, Wiesel-Motiuk N, Bar DZ, Barkan R, Meshorer E, Gruenbaum Y (2009) Nuclear lamins: key regulators of nuclear structure and activities. J Cell Mol Med 13(6):1059–1085. doi:10.1111/j.1582-4934.2008.00676.x
Burke B, Stewart CL (2012) The nuclear lamins: flexibility in function. Nat Rev Mol Cell Biol 14(1):13–24. doi:10.1038/nrm3488
Dittmer TA, Misteli T (2011) The lamin protein family. Genome Biol 12(5):222. doi: 10.1186/gb-2011-12-5-222
Stuurman N, Heins S, Aebi U (1998) Nuclear lamins: their structure, assembly, and interactions. J Struct Biol 122(1–2):42–66. doi:10.1006/jsbi.1998.3987
Polychronidou M, Hellwig A, Grosshans J (2010) Farnesylated nuclear proteins Kugelkern and lamin Dm0 affect nuclear morphology by directly interacting with the nuclear membrane. Mol Biol Cell 21(19):3409–3420. doi:10.1091/mbc.E10-03-0230
Dessev G, Iovcheva-Dessev C, Bischoff JR, Beach D, Goldman R (1991) A complex containing p34cdc2 and cyclin B phosphorylates the nuclear lamin and disassembles nuclei of clam oocytes in vitro. J Cell Biol 112(4):523–533
Rzepecki R, Fisher PA (2002) In vivo phosphorylation of Drosophila melanogaster nuclear lamins during both interphase and mitosis. Cell Mol Biol Lett 7(3):859–876
Heald R, McKeon F (1990) Mutations of phosphorylation sites in lamin A that prevent nuclear lamina disassembly in mitosis. Cell 61(4):579–589
Ward GE, Kirschner MW (1990) Identification of cell cycle-regulated phosphorylation sites on nuclear lamin C. Cell 61(4):561–577
Lee KK, Gruenbaum Y, Spann P, Liu J, Wilson KL (2000) C. elegans nuclear envelope proteins emerin, MAN1, lamin, and nucleoporins reveal unique timing of nuclear envelope breakdown during mitosis. Mol Biol Cell 11(9):3089–3099
Stuurman N, Maus N, Fisher PA (1995) Interphase phosphorylation of the Drosophila nuclear lamin: site-mapping using a monoclonal antibody. J Cell Sci 108(Pt 9):3137–3144
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. doi:10.1021/bi9827060
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. doi:10.1371/journal.pone.0032649
Zaremba-Czogalla M, Gagat P, Koziol K, Dubinska-Magiera M, Sikora J, Dadlez M, Rzepecki R (2011) Identification of new in vivo phosphosites on lamin Dm—the evidence of heterogeneity of phosphorylation sites in different Drosophila tissues. Nucleus 2(5):478–488. doi:http://dx.doi.org/10.4161/nucl.2.5.1786410.4161/nucl.2.5.17
Mattout A, Goldberg M, Tzur Y, Margalit A, Gruenbaum Y (2007) Specific and conserved sequences in D. melanogaster and C. elegans lamins and histone H2A mediate the attachment of lamins to chromosomes. J Cell Sci 120(Pt 1):77–85. doi:10.1242/jcs.03325
Aebi U, Cohn J, Buhle L, Gerace L (1986) The nuclear lamina is a meshwork of intermediate-type filaments. Nature 323(6088):560–564. doi:10.1038/323560a0
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
Foeger N, Wiesel N, Lotsch D, Mucke N, Kreplak L, Aebi U, Gruenbaum Y, Herrmann H (2006) Solubility properties and specific assembly pathways of the B-type lamin from Caenorhabditis elegans. J Struct Biol 155(2):340–350. doi:10.1016/j.jsb.2006.03.026
Karabinos A, Schunemann J, Meyer M, Aebi U, Weber K (2003) The single nuclear lamin of Caenorhabditis elegans forms in vitro stable intermediate filaments and paracrystals with a reduced axial periodicity. J Mol Biol 325(2):241–247
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. doi:10.1016/j.jmb.2008.12.024
Wiesel N, Mattout A, Melcer S, Melamed-Book N, Herrmann H, Medalia O, Aebi U, Gruenbaum Y (2008) Laminopathic mutations interfere with the assembly, localization, and dynamics of nuclear lamins. Proc Natl Acad Sci U S A 105(1):180–185. doi:10.1073/pnas.0708974105
Grossman E, Dahan I, Stick R, Goldberg MW, Gruenbaum Y, Medalia O (2012) Filaments assembly of ectopically expressed Caenorhabditis elegans lamin within Xenopus oocytes. J Struct Biol 177(1):113–118. doi:10.1016/j.jsb.2011.11.002
Furukawa K, Ishida K, Tsunoyama TA, Toda S, Osoda S, Horigome T, Fisher PA, Sugiyama S (2009) A-type and B-type lamins initiate layer assembly at distinct areas of the nuclear envelope in living cells. Exp Cell Res 315(7):1181–1189. doi:10.1016/j.yexcr.2008.12.024
Bossie CA, Sanders MM (1993) A cDNA from Drosophila melanogaster encodes a lamin C-like intermediate filament protein. J Cell Sci 104(Pt 4):1263–1272
Zimek A, Weber K (2011) Flanking genes of an essential gene give information about the evolution of metazoa. Eur J Cell Biol 90(4):356–364. doi:10.1016/j.ejcb.2010.10.005
Peter A, Reimer S (2012) Evolution of the lamin protein family: what introns can tell. Nucleus 3(1):44–59
Ohno S (1970) Evolution by gene duplication. Springer, Berlin, NY
Putnam NH, Butts T, Ferrier DE, Furlong RF, Hellsten U, Kawashima T, Robinson-Rechavi M, Shoguchi E, Terry A, Yu JK, Benito-Gutierrez EL, Dubchak I, Garcia-Fernandez J, Gibson-Brown JJ, Grigoriev IV, Horton AC, de Jong PJ, Jurka J, Kapitonov VV, Kohara Y, Kuroki Y, Lindquist E, Lucas S, Osoegawa K, Pennacchio LA, Salamov AA, Satou Y, Sauka-Spengler T, Schmutz J, Shin IT, Toyoda A, Bronner-Fraser M, Fujiyama A, Holland LZ, Holland PW, Satoh N, Rokhsar DS (2008) The amphioxus genome and the evolution of the chordate karyotype. Nature 453(7198):1064–1071. doi:10.1038/nature06967
Erber A, Riemer D, Hofemeister H, Bovenschulte M, Stick R, Panopoulou G, Lehrach H, Weber K (1999) Characterization of the Hydra lamin and its gene: a molecular phylogeny of metazoan lamins. J Mol Evol 49(2):260–271
Liu J, Rolef Ben-Shahar T, Riemer D, Treinin M, Spann P, Weber K, Fire A, Gruenbaum Y (2000) Essential roles for Caenorhabditis elegans lamin gene in nuclear organization, cell cycle progression, and spatial organization of nuclear pore complexes. Mol Biol Cell 11(11):3937–3947
Cohen M, Tzur YB, Neufeld E, Feinstein N, Delannoy MR, Wilson KL, Gruenbaum Y (2002) Transmission electron microscope studies of the nuclear envelope in Caenorhabditis elegans embryos. J Struct Biol 140(1–3):232–240
Margalit A, Liu J, Fridkin A, Wilson KL, Gruenbaum Y (2005) A lamin-dependent pathway that regulates nuclear organization, cell cycle progression and germ cell development. Novartis Found Symp 264:231–240, discussion 240-235
Riemer D, Dodemont H, Weber K (1993) A nuclear lamin of the nematode Caenorhabditis elegans with unusual structural features; cDNA cloning and gene organization. Eur J Cell Biol 62(2):214–223
Gruenbaum Y, Landesman Y, Drees B, Bare JW, Saumweber H, Paddy MR, Sedat JW, Smith DE, Benton BM, Fisher PA (1988) Drosophila nuclear lamin precursor Dm0 is translated from either of two developmentally regulated mRNA species apparently encoded by a single gene. J Cell Biol 106(3):585–596
Guillemin K, Williams T, Krasnow MA (2001) A nuclear lamin is required for cytoplasmic organization and egg polarity in Drosophila. Nat Cell Biol 3(9):848–851. doi:10.1038/ncb0901-848
Harel A, Zlotkin E, Nainudel-Epszteyn S, Feinstein N, Fisher PA, Gruenbaum Y (1989) Persistence of major nuclear envelope antigens in an envelope-like structure during mitosis in Drosophila melanogaster embryos. J Cell Sci 94(Pt 3):463–470
Riemer D, Weber K (1994) The organization of the gene for Drosophila lamin C: limited homology with vertebrate lamin genes and lack of homology versus the Drosophila lamin Dm0 gene. Eur J Cell Biol 63(2):299–306
Chen B, Cai ST, Zhai ZH (1994) Investigation of nuclear lamina in Tetrahymena thermophila. Shi yan sheng wu xue bao 27(2):153–163
Minguez A, Franca S, Diaz M, de la Espina S (1994) Dinoflagellates have a eukaryotic nuclear matrix with lamin-like proteins and topoisomerase II. J Cell Sci 107(Pt 10):2861–2873
Melcer S, Gruenbaum Y, Krohne G (2007) Invertebrate lamins. Exp Cell Res 313(10):2157–2166. doi:10.1016/j.yexcr.2007.03.004
Pappas GD (1956) The fine structure of the nuclear envelope of Amoeba proteus. J Biophys Biochem Cytol 2(4 Suppl):431–434
Schmidt M, Grossmann U, Krohne G (1995) The nuclear membrane-associated honeycomb structure of the unicellular organism Amoeba proteus: on the search for homologies with the nuclear lamina of metazoa. Eur J Cell Biol 67(3):199–208
Kruger A, Batsios P, Baumann O, Luckert E, Schwarz H, Stick R, Meyer I, Graf R (2012) Characterization of NE81, the first lamin-like nucleoskeleton protein in a unicellular organism. Mol Biol Cell 23(2):360–370. doi:10.1091/mbc.E11-07-0595
DuBois KN, Alsford S, Holden JM, Buisson J, Swiderski M, Bart JM, Ratushny AV, Wan Y, Bastin P, Barry JD, Navarro M, Horn D, Aitchison JD, Rout MP, Field MC (2012) NUP-1 Is a large coiled-coil nucleoskeletal protein in trypanosomes with lamin-like functions. PLoS Biol 10(3):e1001287. doi:10.1371/journal.pbio.1001287
Masuda K, Xu ZJ, Takahashi S, Ito A, Ono M, Nomura K, Inoue M (1997) Peripheral framework of carrot cell nucleus contains a novel protein predicted to exhibit a long alpha-helical domain. Exp Cell Res 232(1):173–181. doi:10.1006/excr.1997.3531
Dittmer TA, Stacey NJ, Sugimoto-Shirasu K, Richards EJ (2007) LITTLE NUCLEI genes affecting nuclear morphology in Arabidopsis thaliana. Plant Cell 19(9):2793–2803. doi:10.1105/tpc.107.053231
Dittmer TA, Richards EJ (2008) Role of LINC proteins in plant nuclear morphology. Plant Signal Behav 3(7):485–487
Gruenbaum Y, Lee KK, Liu J, Cohen M, Wilson KL (2002) The expression, lamin-dependent localization and RNAi depletion phenotype for emerin in C. elegans. J Cell Sci 115(Pt 5):923–929
Liu J, Lee KK, Segura-Totten M, Neufeld E, Wilson KL, Gruenbaum Y (2003) MAN1 and emerin have overlapping function(s) essential for chromosome segregation and cell division in Caenorhabditis elegans. Proc Natl Acad Sci U S A 100(8):4598–4603. doi:10.1073/pnas.0730821100
Margalit A, Neufeld E, Feinstein N, Wilson KL, Podbilewicz B, Gruenbaum Y (2007) Barrier to autointegration factor blocks premature cell fusion and maintains adult muscle integrity in C. elegans. J Cell Biol 178(4):661–673. doi:10.1083/jcb.200704049
Lee KK, Starr D, Cohen M, Liu J, Han M, Wilson KL, Gruenbaum Y (2002) Lamin-dependent localization of UNC-84, a protein required for nuclear migration in Caenorhabditis elegans. Mol Biol Cell 13(3):892–901. doi:10.1091/mbc.01-06-0294
Goldberg M, Harel A, Brandeis M, Rechsteiner T, Richmond TJ, Weiss AM, Gruenbaum Y (1999) The tail domain of lamin Dm0 binds histones H2A and H2B. Proc Natl Acad Sci U S A 96(6):2852–2857
Glass CA, Glass JR, Taniura H, Hasel KW, Blevitt JM, Gerace L (1993) The alpha-helical rod domain of human lamins A and C contains a chromatin binding site. EMBO J 12(11):4413–4424
Burke B (1990) On the cell-free association of lamins A and C with metaphase chromosomes. Exp Cell Res 186(1):169–176
Maraldi NM, Lattanzi G, Cenni V, Bavelloni A, Marmiroli S, Manzoli FA (2010) Laminopathies and A-type lamin-associated signalling pathways. Adv enzyme Regul 50(1):248–261. doi:10.1016/j.advenzreg.2009.10.019
Wilson KL, Foisner R (2010) Lamin-binding proteins. Cold Spring Harbor Perspect Biol 2(4):a000554. doi:10.1101/cshperspect.a000554
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. doi:10.1038/nature06727
Finlan LE, Sproul D, Thomson I, Boyle S, Kerr E, Perry P, Ylstra B, Chubb JR, Bickmore WA (2008) Recruitment to the nuclear periphery can alter expression of genes in human cells. PLoS Genet 4(3):e1000039. doi:10.1371/journal.pgen.1000039
Kumaran RI, Spector DL (2008) A genetic locus targeted to the nuclear periphery in living cells maintains its transcriptional competence. J Cell Biol 180(1):51–65. doi:10.1083/jcb.200706060
Meister P, Towbin BD, Pike BL, Ponti A, Gasser SM (2010) The spatial dynamics of tissue-specific promoters during C. elegans development. Genes Dev 24(8):766–782. doi:10.1101/gad.559610
Mattout A, Pike BL, Towbin BD, Bank EM, Gonzalez-Sandoval A, Stadler MB, Meister P, Gruenbaum Y, Gasser SM (2011) An EDMD mutation in C. elegans lamin blocks muscle-specific gene relocation and compromises muscle integrity. Curr Biol:CB 21(19):1603–1614. doi:10.1016/j.cub.2011.08.030
Shevelyov YY, Lavrov SA, Mikhaylova LM, Nurminsky ID, Kulathinal RJ, Egorova KS, Rozovsky YM, Nurminsky DI (2009) The B-type lamin is required for somatic repression of testis-specific gene clusters. Proc Natl Acad Sci U S A 106(9):3282–3287. doi:10.1073/pnas.0811933106
Starr DA (2007) Communication between the cytoskeleton and the nuclear envelope to position the nucleus. Mol bioSyst 3(9):583–589. doi:10.1039/b703878j
Burke B, Roux KJ (2009) Nuclei take a position: managing nuclear location. Dev Cell 17(5):587–597. doi:10.1016/j.devcel.2009.10.018
Patterson K, Molofsky AB, Robinson C, Acosta S, Cater C, Fischer JA (2004) The functions of Klarsicht and nuclear lamin in developmentally regulated nuclear migrations of photoreceptor cells in the Drosophila eye. Mol Biol Cell 15(2):600–610. doi:10.1091/mbc.E03-06-0374
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(Pt 2):239–249. doi:10.1242/jcs.02728
Somsel Rodman J, Wandinger-Ness A (2000) Rab GTPases coordinate endocytosis. J Cell Sci 113(Pt 2):183–192
Audhya A, Desai A, Oegema K (2007) A role for Rab5 in structuring the endoplasmic reticulum. J Cell Biol 178(1):43–56. doi:10.1083/jcb.200701139
Capalbo L, D’Avino PP, Archambault V, Glover DM (2011) Rab5 GTPase controls chromosome alignment through Lamin disassembly and relocation of the NuMA-like protein Mud to the poles during mitosis. Proc Natl Acad Sci U S A 108(42):17343–17348. doi:10.1073/pnas.1103720108
Liu B, Zhou Z (2008) Lamin A/C, laminopathies and premature ageing. Histol Histopathol 23(6):747–763
Burke B, Stewart CL (2002) Life at the edge: the nuclear envelope and human disease. Nat Rev Mol Cell Biol 3(8):575–585. doi:10.1038/nrm879
Fridkin A, Mills E, Margalit A, Neufeld E, Lee KK, Feinstein N, Cohen M, Wilson KL, Gruenbaum Y (2004) Matefin, a Caenorhabditis elegans germ line-specific SUN-domain nuclear membrane protein, is essential for early embryonic and germ cell development. Proc Natl Acad Sci U S A 101(18):6987–6992. doi:10.1073/pnas.0307880101
Tzur YB, Wilson KL, Gruenbaum Y (2006) SUN-domain proteins: ‘Velcro’ that links the nucleoskeleton to the cytoskeleton. Nat Rev Mol Cell Biol 7(10):782–788. doi:10.1038/nrm2003
Haithcock E, Dayani Y, Neufeld E, Zahand AJ, Feinstein N, Mattout A, Gruenbaum Y, Liu J (2005) Age-related changes of nuclear architecture in Caenorhabditis elegans. Proc Natl Acad Sci U S A 102(46):16690–16695. doi:10.1073/pnas.0506955102
Bar DZ, Neufeld E, Feinstein N, Gruenbaum Y (2009) Gliotoxin reverses age-dependent nuclear morphology phenotypes, ameliorates motility, but fails to affect lifespan of adult Caenorhabditis elegans. Cell Motil Cytoskel 66(10):791–797. doi:10.1002/cm.20347
Bonne G, Di Barletta MR, Varnous S, Becane HM, Hammouda EH, Merlini L, Muntoni F, Greenberg CR, Gary F, Urtizberea JA, Duboc D, Fardeau M, Toniolo D, Schwartz K (1999) Mutations in the gene encoding lamin A/C cause autosomal dominant Emery-Dreifuss muscular dystrophy. Nat Genet 21(3):285–288. doi:10.1038/6799
Bank EM, Ben-Harush K, Feinstein N, Medalia O, Gruenbaum Y (2012) Structural and physiological phenotypes of disease-linked lamin mutations in C. elegans. J Struct Biol 177(1):106–112. doi:10.1016/j.jsb.2011.10.009
Bank EM, Ben-Harush K, Wiesel-Motiuk N, Barkan R, Feinstein N, Lotan O, Medalia O, Gruenbaum Y (2011) A laminopathic mutation disrupting lamin filament assembly causes disease-like phenotypes in Caenorhabditis elegans. Mol Biol Cell 22(15):2716–2728. doi:10.1091/mbc.E11-01-0064
Lenz-Bohme B, Wismar J, Fuchs S, Reifegerste R, Buchner E, Betz H, Schmitt B (1997) Insertional mutation of the Drosophila nuclear lamin Dm0 gene results in defective nuclear envelopes, clustering of nuclear pore complexes, and accumulation of annulate lamellae. J Cell Biol 137(5):1001–1016
Harel A, Goldberg M, Ulitzur N, Gruenbaum Y (1998) Structural organization and biological roles of the nuclear lamina. In: Boulikas T (ed) Textbook of gene therapy and molecular biology: from basic mechanism to clinical applications, vol 1. Gene Therapy Press, Palo Alto, CA
Osouda S, Nakamura Y, de Saint PB, McConnell M, Horigome T, Sugiyama S, Fisher PA, Furukawa K (2005) Null mutants of Drosophila B-type lamin Dm(0) show aberrant tissue differentiation rather than obvious nuclear shape distortion or specific defects during cell proliferation. Dev Biol 284(1):219–232. doi:10.1016/j.ydbio.2005.05.022
Uchino R, Nonaka YK, Horigome T, Sugiyama S, Furukawa K (2013) Loss of Drosophila A-type lamin C initially causes tendon abnormality including disintegration of cytoskeleton and nuclear lamina in muscular defects. Dev Biol 373(1):216–227. doi:10.1016/j.ydbio.2012.08.001
Bao X, Girton J, Johansen J, Johansen KM (2007) The lamin Dm0 allele Ari3 acts as an enhancer of position effect variegation of the wm4 allele in Drosophila. Genetica 129(3):339–342. doi:10.1007/s10709-006-0012-7
Muller H (1930) Types of Visible Variations Induced by X-rays in Drosophila. J Genet 22(3):299–334
Dialynas G, Flannery KM, Zirbel LN, Nagy PL, Mathews KD, Moore SA, Wallrath LL (2012) LMNA variants cause cytoplasmic distribution of nuclear pore proteins in Drosophila and human muscle. Human Mol Genet 21(7):1544–1556. doi:10.1093/hmg/ddr592
Schulze SR, Curio-Penny B, Speese S, Dialynas G, Cryderman DE, McDonough CW, Nalbant D, Petersen M, Budnik V, Geyer PK, Wallrath LL (2009) A comparative study of Drosophila and human A-type lamins. PloS One 4(10):e7564. doi:10.1371/journal.pone.0007564
Dialynas G, Speese S, Budnik V, Geyer PK, Wallrath LL (2010) The role of Drosophila Lamin C in muscle function and gene expression. Development 137(18):3067–3077. doi:10.1242/dev.048231
Beard GS, Bridger JM, Kill IR, Tree DR (2008) Towards a Drosophila model of Hutchinson-Gilford progeria syndrome. Biochem Soc Trans 36(Pt 6):1389–1392. doi:10.1042/BST0361389
Tzur YB, Margalit A, Melamed-Book N, Gruenbaum Y (2006) Matefin/SUN-1 is a nuclear envelope receptor for CED-4 during Caenorhabditis elegans apoptosis. Proc Natl Acad Sci U S A 103(36):13397–13402. doi:10.1073/pnas.0604224103
Wagner N, Schmitt J, Krohne G (2004) Two novel LEM-domain proteins are splice products of the annotated Drosophila melanogaster gene CG9424 (Bocksbeutel). Eur J Cell Biol 82(12):605–616. doi:10.1078/0171-9335-00350
Goldberg M, Lu H, Stuurman N, Ashery-Padan R, Weiss AM, Yu J, Bhattacharyya D, Fisher PA, Gruenbaum Y, Wolfner MF (1998) Interactions among Drosophila nuclear envelope proteins lamin, otefin, and YA. Mol Cell Biol 18(7):4315–4323
Wagner N, Weber D, Seitz S, Krohne G (2004) The lamin B receptor of Drosophila melanogaster. J Cell Sci 117(Pt 10):2015–2028. doi:10.1242/jcs.01052
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. doi:10.1242/jcs.02611
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739. doi:10.1093/molbev/msr121
Rzhetsky A, Nei M (1992) A simple method for estimating and testing minimum evolution trees. Mol Biol Evol 9:945–967
Zuckercandl E, Pauling L (1965) Evolutionary divergence and convergence in proteins. In: Bryson V, Vogel HJ (eds) Evolving genes and proteins. Academic, New York, pp 97–166
Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425
Acknowledgments
We thank Yuval Reiss and other members of the Gruenbaum laboratory for critical comments on the manuscript. We also thank Nataly Levi for the assistance in preparation of the Fig. 1. We gratefully acknowledge funding from the Morasha Legacy 1798/10, Israel Ministry of Health (MOH 2965), the Muscular Dystrophy Association (MDA), the Israeli Science Foundation, the Binational Israel-USA Science Foundation (BSF 2007215), and the COST NANONET (BM1002).
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Lyakhovetsky, R., Gruenbaum, Y. (2014). Studying Lamins in Invertebrate Models. In: Schirmer, E., de las Heras, J. (eds) Cancer Biology and the Nuclear Envelope. Advances in Experimental Medicine and Biology, vol 773. Springer, New York, NY. https://doi.org/10.1007/978-1-4899-8032-8_11
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