Evolutionary aspects in intermediate filament proteins

Current Opinion in Cell Biology

Volumn 32, Issue , 2015, Pages 48-55

  Peter, Annette ^a   Stick, Reimer ^a  

^a UNIVERSITY OF BREMEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOPLASM PROTEIN; INTERMEDIATE FILAMENT PROTEIN; LAMIN; LAMIN A;

MOLECULAR EVOLUTION; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROTEIN STRUCTURE; REVIEW; VERTEBRATE; ANIMAL; CHEMISTRY; GENETICS; METABOLISM;

METAZOA; VERTEBRATA;

ANIMALS; EVOLUTION, MOLECULAR; INTERMEDIATE FILAMENT PROTEINS; LAMINS; PHYLOGENY;

EID: 84920997356     PISSN: 09550674     EISSN: 18790410     Source Type: Journal    
DOI: 10.1016/j.ceb.2014.12.009     Document Type: Review

References (71)

1. Dechat T., Gesson K., Foisner R. Lamina-independent lamins in the nuclear interior serve important functions. Cold Spring Harb Symp Quant Biol 2010, 75:533-543.
2. Hesse M., Magin T.M., Weber K. Genes for intermediate filament proteins and the draft sequence of the human genome: novel keratin genes and a surprisingly high number of pseudogenes related to keratin genes 8 and 18. J Cell Sci 2001, 114:2569-2575.
3. Dodemont H., Riemer D., Weber K. Structure of an invertebrate gene encoding cytoplasmic intermediate filament (IF) proteins: implications for the origin and the diversification of IF proteins. EMBO J 1990, 9:4083-4094.
4. Döring V., Stick R. Gene structure of nuclear lamin LIII of Xenopus laevis; a model for the evolution of IF proteins from a lamin-like ancestor. EMBO J 1990, 9:4073-4081.
5. Herrmann H., Aebi U. Intermediate filaments: molecular structure, assembly mechanism, and integration into functionally distinct intracellular Scaffolds. Annu Rev Biochem 2004, 73:749-789.
6. Riemer D., Wang J., Zimek A., Swalla B.J., Weber K. Tunicates have unusual nuclear lamins with a large deletion in the carboxyterminal tail domain. Gene 2000, 255:317-325.
7. Erber A., Riemer D., Bovenschulte M., Weber K. Molecular phylogeny of metazoan intermediate filament proteins. J Mol Evol 1998, 47:751-762.
8. Dhe-Paganon S., Werner E.D., Chi Y.I., Shoelson S.E. Structure of the globular tail of nuclear lamin. J Biol Chem 2002, 277:17381-17384.
9. Moroz L.L., Kocot K.M., Citarella M.R., Dosung S., Norekian T.P., Povolotskaya I.S., Grigorenko A.P., Dailey C., Berezikov E., Buckley K.M., et al. The ctenophore genome and the evolutionary origins of neural systems. Nature 2014, 510:109-114.
10. Krüger A., Batsios P., Baumann O., Luckert E., Schwarz H., Stick R., Meyer I., Gräf R. Characterization of NE81, the first lamin-like nucleoskeleton protein in a unicellular organism. Mol Biol Cell 2012, 23:360-370.
11. Batsios P., Peter T., Baumann O., Stick R., Meyer I., Gräf R. A lamin in lower eukaryotes?. Nucleus 2012, 3:237-243.
12. Devos D.P., Gräf R., Field M.C. Evolution of the nucleus. Curr Opin Cell Biol 2014, 28C:8-15.
13. Peter A., Stick R. Evolution of the lamin protein family: what introns can tell. Nucleus 2012, 3:44-59.
14. Riemer D., Dodemont H., Weber K. A nuclear lamin of the nematode Caenorhabditis elegans with unusual structural features; cDNA cloning and gene organization. Eur J Cell Biol 1993, 62:214-223.
15. Miller D.J., Ball E.E. The gene complement of the ancestral bilaterian - was Urbilateria a monster?. J Biol 2009, 8:89.81-89.84.
16. Bossie C.A., Sanders M.M. A cDNA from Drosophila melanogaster encodes a lamin C-like intermediate filament protein. J Cell Sci 1993, 104(Pt 4):1263-1272.
17. Ohno S. Gene duplication and the uniqueness of vertebrate genomes circa 1970-1999. Semin Cell Dev Biol 1999, 10:517-522.
18. Kuraku S., Meyer A., Kuratani S. Timing of genome duplications relative to the origin of the vertebrates: did cyclostomes diverge before or after?. Mol Biol Evol 2009, 26:47-59.
19. Sidow A. Gen(om)e duplications in the evolution of early vertebrates. Curr Opin Genet Dev 1996, 6:715-722.
20. Zimek A., Weber K. In contrast to the nematode and fruit fly all 9 intron positions of the sea anemone lamin gene are conserved in human lamin genes. Eur J Cell Biol 2008, 87:305-309.
21. Zimek A., Weber K. Flanking genes of an essential gene give information about the evolution of metazoa. Eur J Cell Biol 2011, 90:356-364.
22. Schilf P., Peter A., Hurek T., Stick R. Lamins of the sea lamprey (Petromyzon marinus) and the evolution of the vertebrate lamin protein family. Eur J Cell Biol 2014, 93:308-321.
23. Wolfe K. Robustness - it's not where you think it is. Nat Genet 2000, 25:3-4.
24. Broers J.L., Machiels B.M., Kuijpers H.J., Smedts F., van den Kieboom R., Raymond Y., Ramaekers F.C. A- and B-type lamins are differentially expressed in normal human tissues. Histochem Cell Biol 1997, 107:505-517.
25. Link J., Jahn D., Schmitt J., Gob E., Baar J., Ortega S., Benavente R., Alsheimer M. The meiotic nuclear lamina regulates chromosome dynamics and promotes efficient homologous recombination in the mouse. PLoS Genet 2013, 9:e1003261.
26. Hesse M., Zimek A., Weber K., Magin T.M. Comprehensive analysis of keratin gene clusters in humans and rodents. Eur J Cell Biol 2004, 83:19-26.
27. Zimek A., Weber K. Terrestrial vertebrates have two keratin gene clusters; striking differences in teleost fish. Eur J Cell Biol 2005, 84:623-635.
28. 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, 8:3221-3227.
29. Halanych K.M. The new view of animal phylogeny. Annu Rev Ecol Evol Syst 2004, 35:229-256.
30. Mencarelli C., Ciolfi S., Caroti D., Lupetti P., Dallai R. Isomin: a novel cytoplasmic intermediate filament protein from an arthropod species. BMC Biol 2011, 9:17.
31. Herrmann H., Strelkov S.V. History and phylogeny of intermediate filaments: now in insects. BMC Biol 2011, 9:16.
32. Pan X., Hobbs R.P., Coulombe P.A. The expanding significance of keratin intermediate filaments in normal and diseased epithelia. Curr Opin Cell Biol 2013, 25:47-56.
33. Riemer D., Karabinos A., Weber K. Analysis of eight cDNAs and six genes for intermediate filament (IF) proteins in the cephalochordate Branchiostoma reveals differences in the IF multigene families of lower chordates and the vertebrates. Gene 1998, 211:361-373.
34. Karabinos A., Riemer D., Panopoulou G., Lehrach H., Weber K. Characterisation and tissue-specific expression of the two keratin subfamilies of intermediate filament proteins in the cephalochordate Branchiostoma. Eur J Cell Biol 2000, 79:17-26.
35. Oshima R.G. Intermediate filaments: a historical perspective. Exp Cell Res 2007, 313:1981-1994.
36. Karabinos A. The cephalochordate Branchiostoma genome contains 26 intermediate filament (IF) genes: implications for evolution of chordate IF proteins. Eur J Cell Biol 2013, 92:295-302.
37. Riemer D., Weber K. Common and variant properties of intermediate filament proteins from lower chordates and vertebrates; two proteins from the tunicate Styela and the identification of a type III homologue. J Cell Sci 1998, 111(Pt 19):2967-2975.
38. Lewis S.A., Cowan N.J. Anomalous placement of introns in a member of the intermediate filament multigene family: an evolutionary conundrum. Mol Cell Biol 1986, 6:1529-1534.
39. Karabinos A., Zimek A., Weber K. The genome of the early chordate Ciona intestinalis encodes only five cytoplasmic intermediate filament proteins including a single type I and type II keratin and a unique IF-annexin fusion protein. Gene 2004, 326:123-129.
40. Krushna Padhi B., Akimenko M.A., Ekker M. Independent expansion of the keratin gene family in teleostean fish and mammals: an insight from phylogenetic analysis and radiation hybrid mapping of keratin genes in zebrafish. Gene 2006, 368:37-45.
41. Vandebergh W., Bossuyt F. Radiation and functional diversification of alpha keratins during early vertebrate evolution. Mol Biol Evol 2012, 29:995-1004.
42. Langbein L., Schweizer J. Keratins of the human hair follicle. Int Rev Cytol 2005, 243:1-78.
43. Schaffeld M., Bremer M., Hunzinger C., Markl J. Evolution of tissue-specific keratins as deduced from novel cDNA sequences of the lungfish Protopterus aethiopicus. Eur J Cell Biol 2005, 84:363-377.
44. Schaffeld M., Haberkamp M., Braziulis E., Lieb B., Markl J. Type II keratin cDNAs from the rainbow trout: implications for keratin evolution. Differentiation 2002, 70:292-299.
45. Schaffeld M., Hoffling S., Haberkamp M., Conrad M., Markl J. Type I keratin cDNAs from the rainbow trout: independent radiation of keratins in fish. Differentiation 2002, 70:282-291.
46. Schaffeld M., Lobbecke A., Lieb B., Markl J. Tracing keratin evolution: catalog, expression patterns and primary structure of shark (Scyliorhinus stellaris) keratins. Eur J Cell Biol 1998, 77:69-80.
47. Garcia D.M., Bauer H., Dietz T., Schubert T., Markl J., Schaffeld M. Identification of keratins and analysis of their expression in carp and goldfish: comparison with the zebrafish and trout keratin catalog. Cell Tissue Res 2005, 322:245-256.
48. Zimek A., Weber K. The organization of the keratin I and II gene clusters in placental mammals and marsupials show a striking similarity. Eur J Cell Biol 2006, 85:83-89.
49. Zimek A., Thiering S., Weber K., Magin T.M. Genes encoding cytoplasmic intermediate filament proteins of vertebrates revisited: identification of a cytoplasmic intermediate filament protein in the sea anemone Nematostella. Eur J Cell Biol 2012, 91:809-817.
50. Hwang J.S., Takaku Y., Chapman J., Ikeo K., David C.N., Gojobori T. Cilium evolution: identification of a novel protein, nematocilin, in the mechanosensory cilium of Hydra nematocytes. Mol Biol Evol 2008, 25:2009-2017.
51. Adjaye J., Plessmann U., Weber K., Dodemont H. Characterisation of neurofilament protein NF70 mRNA from the gastropod Helix aspersa reveals that neuronal and non-neuronal intermediate filament proteins of cerebral ganglia arise from separate lamin-related genes. J Cell Sci 1995, 108(Pt 11):3581-3590.
52. Szaro B.G., Pant H.C., Way J., Battey J. Squid low molecular weight neurofilament proteins are a novel class of neurofilament protein. A nuclear lamin-like core and multiple distinct proteins formed by alternative RNA processing. J Biol Chem 1991, 266:15035-15041.
53. Way J., Hellmich M.R., Jaffe H., Szaro B., Pant H.C., Gainer H., Battey J. A high-molecular-weight squid neurofilament protein contains a lamin-like rod domain and a tail domain with Lys-Ser-Pro repeats. Proc Natl Acad Sci U S A 1992, 89:6963-6967.
54. Zhang G., Fang X., Guo X., Li L., Luo R., Xu F., Yang P., Zhang L., Wang X., Qi H., et al. The oyster genome reveals stress adaptation and complexity of shell formation. Nature 2012, 490:49-54.
55. Bovenschulte M., Riemer D., Weber K. The sequence of a cytoplasmic intermediate filament (IF) protein from the annelid Lumbricus terrestris emphasizes a distinctive feature of protostomic IF proteins. FEBS Lett 1995, 360:223-226.
56. Johansen K.M., Johansen J. Filarin, a novel invertebrate intermediate filament protein present in axons and perikarya of developing and mature leech neurons. J Neurobiol 1995, 27:227-239.
57. Xu Y., Bolton B., Zipser B., Jellies J., Johansen K.M., Johansen J. Gliarin and macrolin, two novel intermediate filament proteins specifically expressed in sets and subsets of glial cells in leech central nervous system. J Neurobiol 1999, 40:244-253.
58. Simakov O., Marletaz F., Cho S.J., Edsinger-Gonzales E., Havlak P., Hellsten U., Kuo D.H., Larsson T., Lv J., Arendt D., et al. Insights into bilaterian evolution from three spiralian genomes. Nature 2013, 493:526-531.
59. Erber A., Riemer D., Hofemeister H., Bovenschulte M., Stick R., Panopoulou G., Lehrach H., Weber K. Characterization of the Hydra lamin and its gene: a molecular phylogeny of metazoan lamins. J Mol Evol 1999, 49:260-271.
60. Zimek A., Weber K. The gene for a cytoplasmic intermediate filament (IF) protein of the hemichordate Saccoglossus kowalevskii; definition of the unique features of chordate IF proteins. Gene 2002, 288:187-193.
61. Dodemont H., Riemer D., Ledger N., Weber K. Eight genes and alternative RNA processing pathways generate an unexpectedly large diversity of cytoplasmic intermediate filament proteins in the nematode Caenorhabditis elegans. EMBO J 1994, 13:2625-2638.
62. Karabinos A., Schmidt H., Harborth J., Schnabel R., Weber K. Essential roles for four cytoplasmic intermediate filament proteins in Caenorhabditis elegans development. Proc Natl Acad Sci USA 2001, 98:7863-7868.
63. Gruenbaum Y., Landesman Y., Drees B., Bare J.W., Saumweber H., Paddy M.R., Sedat J.W., Smith D.E., Benton B.M., Fisher P.A. Drosophila nuclear lamin precursor Dm0 is translated from either of two developmentally regulated mRNA species apparently encoded by a single gene. J Cell Biol 1988, 106:585-596.
64. Holy J., Wessel G., Berg L., Gregg R.G., Schatten G. Molecular characterization and expression patterns of a B-type nuclear lamin during sea urchin embryogenesis. Dev Biol 1995, 168:464-478.
65. Luke G.N., Holland P.W. Amphioxus type I keratin cDNA and the evolution of intermediate filament genes. J Exp Zool 1999, 285:50-56.
66. Riemer D., Dodemont H., Weber K. Analysis of the cDNA and gene encoding a cytoplasmic intermediate filament (IF) protein from the cephalochordate Branchiostoma lanceolatum; implications for the evolution of the IF protein family. Eur J Cell Biol 1992, 58:128-135.
67. Karabinos A., Riemer D., Erber A., Weber K. Homologues of vertebrate type I, II and III intermediate filament (IF) proteins in an invertebrate: the IF multigene family of the cephalochordate Branchiostoma. FEBS Lett 1998, 437:15-18.
68. Wang J., Karabinos A., Schünemann J., Riemer D., Weber K. The epidermal intermediate filament proteins of tunicates are distant keratins; a polymerisation-competent hetero coiled coil of the Styela D protein and Xenopus keratin 8. Eur J Cell Biol 2000, 79:478-487.
69. Wang J., Karabinos A., Zimek A., Meyer M., Riemer D., Hudson C., Lemaire P., Weber K. Cytoplasmic intermediate filament protein expression in tunicate development: a specific marker for the test cells. Eur J Cell Biol 2002, 81:302-311.
70. Coulombe P.A., Ma L., Yamada S., Wawersik M. Intermediate filaments at a glance. J Cell Sci 2001, 114:4345-4347.
71. Karabinos A., Schulze E., Schünemann J., Parry D.A., Weber K. In vivo and in vitro evidence that the four essential intermediate filament (IF) proteins A1, A2, A3 and B1 of the nematode Caenorhabditis elegans form an obligate heteropolymeric IF system. J Mol Biol 2003, 333:307-319.