Multiple gains of spliceosomal introns in a superfamily of vertebrate protease inhibitor genes

Ragg H, Kumar A, Köster K, Bentele C, Wang Y, Frese M-A, Prib N, Krüger O (2009)
BMC Evolutionary Biology 9(1): 208.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
Download
OA
Autor*in
Ragg, HermannUniBi; Kumar, Abhishek; Köster, KatharinaUniBi; Bentele, Caterina; Wang, YunjieUniBi; Frese, Marc-Andre; Prib, Natalie; Krüger, Olaf
Abstract / Bemerkung
Background: Intron gains reportedly are very rare during evolution of vertebrates, and the mechanisms underlying their creation are largely unknown. Previous investigations have shown that, during metazoan radiation, the exon-intron patterns of serpin superfamily genes were subject to massive changes, in contrast to many other genes. Results: Here we investigated intron dynamics in the serpin superfamily in lineages pre- and postdating the split of vertebrates. Multiple intron gains were detected in a group of ray-finned fishes, once the canonical groups of vertebrate serpins had been established. In two genes, cooccurrence of non-standard introns was observed, implying that intron gains in vertebrates may even happen concomitantly or in a rapidly consecutive manner. DNA breakage/repair processes associated with genome compaction are introduced as a novel factor potentially favoring intron gain, since all non-canonical introns were found in a lineage of ray-finned fishes that experienced genomic downsizing. Conclusion: Multiple intron acquisitions were identified in serpin genes of a lineage of ray-finned fishes, but not in any other vertebrates, suggesting that insertion rates for introns may be episodically increased. The co-occurrence of non-standard introns within the same gene discloses the possibility that introns may be gained simultaneously. The sequences flanking the intron insertion points correspond to the proto-splice site consensus sequence MAG↑N, previously proposed to serve as intron insertion site. The association of intron gains in the serpin superfamily with a group of fishes that underwent genome compaction may indicate that DNA breakage/repair processes might foster intron birth.
Erscheinungsjahr
2009
Zeitschriftentitel
BMC Evolutionary Biology
Band
9
Ausgabe
1
Seite(n)
208
ISSN
1471-2148
Page URI
https://pub.uni-bielefeld.de/record/1784544

Zitieren

Ragg H, Kumar A, Köster K, et al. Multiple gains of spliceosomal introns in a superfamily of vertebrate protease inhibitor genes. BMC Evolutionary Biology. 2009;9(1):208.
Ragg, H., Kumar, A., Köster, K., Bentele, C., Wang, Y., Frese, M. - A., Prib, N., et al. (2009). Multiple gains of spliceosomal introns in a superfamily of vertebrate protease inhibitor genes. BMC Evolutionary Biology, 9(1), 208. https://doi.org/10.1186/1471-2148-9-208
Ragg, Hermann, Kumar, Abhishek, Köster, Katharina, Bentele, Caterina, Wang, Yunjie, Frese, Marc-Andre, Prib, Natalie, and Krüger, Olaf. 2009. “Multiple gains of spliceosomal introns in a superfamily of vertebrate protease inhibitor genes”. BMC Evolutionary Biology 9 (1): 208.
Ragg, H., Kumar, A., Köster, K., Bentele, C., Wang, Y., Frese, M. - A., Prib, N., and Krüger, O. (2009). Multiple gains of spliceosomal introns in a superfamily of vertebrate protease inhibitor genes. BMC Evolutionary Biology 9, 208.
Ragg, H., et al., 2009. Multiple gains of spliceosomal introns in a superfamily of vertebrate protease inhibitor genes. BMC Evolutionary Biology, 9(1), p 208.
H. Ragg, et al., “Multiple gains of spliceosomal introns in a superfamily of vertebrate protease inhibitor genes”, BMC Evolutionary Biology, vol. 9, 2009, pp. 208.
Ragg, H., Kumar, A., Köster, K., Bentele, C., Wang, Y., Frese, M.-A., Prib, N., Krüger, O.: Multiple gains of spliceosomal introns in a superfamily of vertebrate protease inhibitor genes. BMC Evolutionary Biology. 9, 208 (2009).
Ragg, Hermann, Kumar, Abhishek, Köster, Katharina, Bentele, Caterina, Wang, Yunjie, Frese, Marc-Andre, Prib, Natalie, and Krüger, Olaf. “Multiple gains of spliceosomal introns in a superfamily of vertebrate protease inhibitor genes”. BMC Evolutionary Biology 9.1 (2009): 208.
Alle Dateien verfügbar unter der/den folgenden Lizenz(en):
Copyright Statement:
Dieses Objekt ist durch das Urheberrecht und/oder verwandte Schutzrechte geschützt. [...]
Volltext(e)
Access Level
OA Open Access
Zuletzt Hochgeladen
2019-09-06T08:48:56Z
MD5 Prüfsumme
131ef2c60e3a0bca3cdc2b41e3e0d347


20 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Uncovering missing pieces: duplication and deletion history of arrestins in deuterostomes.
Indrischek H, Prohaska SJ, Gurevich VV, Gurevich EV, Stadler PF., BMC Evol Biol 17(1), 2017
PMID: 28683816
Ancestry & molecular evolutionary analyses of heat shock protein 47 kDa (HSP47/SERPINH1).
Kumar A, Bhandari A, Sarde SJ, Goswami C., Sci Rep 7(1), 2017
PMID: 28871169
Heparin Binds Lamprey Angiotensinogen and Promotes Thrombin Inhibition through a Template Mechanism.
Wei H, Cai H, Wu J, Wei Z, Zhang F, Huang X, Ma L, Feng L, Zhang R, Wang Y, Ragg H, Zheng Y, Zhou A., J Biol Chem 291(48), 2016
PMID: 27681598
Revising angiotensinogen from phylogenetic and genetic variants perspectives.
Kumar A, Sarde SJ, Bhandari A., Biochem Biophys Res Commun 446(2), 2014
PMID: 24631685
Origin of serpin-mediated regulation of coagulation and blood pressure.
Wang Y, Köster K, Lummer M, Ragg H., PLoS One 9(5), 2014
PMID: 24840053
Genetic variants and evolutionary analyses of heparin cofactor II.
Kumar A, Bhandari A, Sarde SJ, Goswami C., Immunobiology 219(9), 2014
PMID: 24950623
Surveying genetic variants and molecular phylogeny of cerebral cavernous malformation gene, CCM3/PDCD10.
Kumar A, Bhandari A, Goswami C., Biochem Biophys Res Commun 455(1-2), 2014
PMID: 25451273
Sequence, phylogenetic and variant analyses of antithrombin III.
Kumar A, Bhandari A, Sarde SJ, Goswami C., Biochem Biophys Res Commun 440(4), 2013
PMID: 24121110
Conservation of tubulin-binding sequences in TRPV1 throughout evolution.
Sardar P, Kumar A, Bhandari A, Goswami C., PLoS One 7(4), 2012
PMID: 22496727
Emergence and evolution of the renin-angiotensin-aldosterone system.
Fournier D, Luft FC, Bader M, Ganten D, Andrade-Navarro MA., J Mol Med (Berl) 90(5), 2012
PMID: 22527880
Intron creation and DNA repair.
Ragg H., Cell Mol Life Sci 68(2), 2011
PMID: 20853128
Functional expression of angiotensinogen depends on splicing enhancers in exon 2.
Cardoso CC, Cabrini DA, May M, Bhagat CS, Eleno N, Cayla C, Walther T, Bader M., Mol Cell Endocrinol 332(1-2), 2011
PMID: 21055442
An unexpected link between angiotensinogen and thrombin.
Wang Y, Ragg H., FEBS Lett 585(14), 2011
PMID: 21722639
Nonsense-mediated decay enables intron gain in Drosophila.
Farlow A, Meduri E, Dolezal M, Hua L, Schlötterer C., PLoS Genet 6(1), 2010
PMID: 20107520

64 References

Daten bereitgestellt von Europe PubMed Central.

The evolution of spliceosomal introns: patterns, puzzles and progress.
Roy SW, Gilbert W., Nat. Rev. Genet. 7(3), 2006
PMID: 16485020
Complex spliceosomal organization ancestral to extant eukaryotes.
Collins L, Penny D., Mol. Biol. Evol. 22(4), 2005
PMID: 15659557
Characterization of intron loss events in mammals.
Coulombe-Huntington J, Majewski J., Genome Res. 17(1), 2006
PMID: 17108319
Intron loss and gain during evolution of the catalase gene family in angiosperms.
Frugoli JA, McPeek MA, Thomas TL, McClung CR., Genetics 149(1), 1998
PMID: 9584109
Intron presence-absence polymorphisms in Daphnia.
Omilian AR, Scofield DG, Lynch M., Mol. Biol. Evol. 25(10), 2008
PMID: 18667441
Massive horizontal gene transfer in bdelloid rotifers.
Gladyshev EA, Meselson M, Arkhipova IR., Science 320(5880), 2008
PMID: 18511688
How were introns inserted into nuclear genes?
Rogers JH., Trends Genet. 5(7), 1989
PMID: 2551082
Models of spliceosomal intron proliferation in the face of widespread ectopic expression.
Rodriguez-Trelles F, Tarrio R, Ayala FJ., Gene 366(2), 2005
PMID: 16288838
Alternative splicing: a missing piece in the puzzle of intron gain.
Tarrio R, Ayala FJ, Rodriguez-Trelles F., Proc. Natl. Acad. Sci. U.S.A. 105(20), 2008
PMID: 18463286
The serpins are an expanding superfamily of structurally similar but functionally diverse proteins. Evolution, mechanism of inhibition, novel functions, and a revised nomenclature.
Silverman GA, Bird PI, Carrell RW, Church FC, Coughlin PB, Gettins PG, Irving JA, Lomas DA, Luke CJ, Moyer RW, Pemberton PA, Remold-O'Donnell E, Salvesen GS, Travis J, Whisstock JC., J. Biol. Chem. 276(36), 2001
PMID: 11435447
The role of serpins in the surveillance of the secretory pathway.
Ragg H., Cell. Mol. Life Sci. 64(21), 2007
PMID: 17668148
Functional diversification during evolution of the murine alpha(1)-proteinase inhibitor family: role of the hypervariable reactive center loop.
Barbour KW, Goodwin RL, Guillonneau F, Wang Y, Baumann H, Berger FG., Mol. Biol. Evol. 19(5), 2002
PMID: 11961105
The ovalbumin serpins revisited: perspective from the chicken genome of clade B serpin evolution in vertebrates.
Benarafa C, Remold-O'Donnell E., Proc. Natl. Acad. Sci. U.S.A. 102(32), 2005
PMID: 16055559
Vertebrate-type intron-rich genes in the marine annelid Platynereis dumerilii.
Raible F, Tessmar-Raible K, Osoegawa K, Wincker P, Jubin C, Balavoine G, Ferrier D, Benes V, de Jong P, Weissenbach J, Bork P, Arendt D., Science 310(5752), 2005
PMID: 16311335
Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization.
Putnam NH, Srivastava M, Hellsten U, Dirks B, Chapman J, Salamov A, Terry A, Shapiro H, Lindquist E, Kapitonov VV, Jurka J, Genikhovich G, Grigoriev IV, Lucas SM, Steele RE, Finnerty JR, Technau U, Martindale MQ, Rokhsar DS., Science 317(5834), 2007
PMID: 17615350
Ancestry and evolution of a secretory pathway serpin.
Kumar A, Ragg H., BMC Evol. Biol. 8(), 2008
PMID: 18793432
Vertebrate serpins: construction of a conflict-free phylogeny by combining exon-intron and diagnostic site analyses.
Ragg H, Lokot T, Kamp PB, Atchley WR, Dress A., Mol. Biol. Evol. 18(4), 2001
PMID: 11264410
The amphioxus genome and the evolution of the chordate karyotype.
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-I T, Toyoda A, Bronner-Fraser M, Fujiyama A, Holland LZ, Holland PW, Satoh N, Rokhsar DS., Nature 453(7198), 2008
PMID: 18563158
The intrarenal renin-angiotensin system: from physiology to the pathobiology of hypertension and kidney disease.
Kobori H, Nangaku M, Navar LG, Nishiyama A., Pharmacol. Rev. 59(3), 2007
PMID: 17878513
On the activation of human leuserpin-2, a thrombin inhibitor, by glycosaminoglycans.
Ragg H, Ulshofer T, Gerewitz J., J. Biol. Chem. 265(9), 1990
PMID: 2318889
A lamprey from the Devonian period of South Africa.
Gess RW, Coates MI, Rubidge BS., Nature 443(7114), 2006
PMID: 17066033
Structure and expression of the gene coding for the human serpin hLS2.
Ragg H, Preibisch G., J. Biol. Chem. 263(24), 1988
PMID: 2841345
Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype.
Jaillon O, Aury JM, Brunet F, Petit JL, Stange-Thomann N, Mauceli E, Bouneau L, Fischer C, Ozouf-Costaz C, Bernot A, Nicaud S, Jaffe D, Fisher S, Lutfalla G, Dossat C, Segurens B, Dasilva C, Salanoubat M, Levy M, Boudet N, Castellano S, Anthouard V, Jubin C, Castelli V, Katinka M, Vacherie B, Biemont C, Skalli Z, Cattolico L, Poulain J, De Berardinis V, Cruaud C, Duprat S, Brottier P, Coutanceau JP, Gouzy J, Parra G, Lardier G, Chapple C, McKernan KJ, McEwan P, Bosak S, Kellis M, Volff JN, Guigo R, Zody MC, Mesirov J, Lindblad-Toh K, Birren B, Nusbaum C, Kahn D, Robinson-Rechavi M, Laudet V, Schachter V, Quetier F, Saurin W, Scarpelli C, Wincker P, Lander ES, Weissenbach J, Roest Crollius H., Nature 431(7011), 2004
PMID: 15496914
From 2R to 3R: evidence for a fish-specific genome duplication (FSGD).
Meyer A, Van de Peer Y., Bioessays 27(9), 2005
PMID: 16108068
Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes.
Aparicio S, Chapman J, Stupka E, Putnam N, Chia JM, Dehal P, Christoffels A, Rash S, Hoon S, Smit A, Gelpke MD, Roach J, Oh T, Ho IY, Wong M, Detter C, Verhoef F, Predki P, Tay A, Lucas S, Richardson P, Smith SF, Clark MS, Edwards YJ, Doggett N, Zharkikh A, Tavtigian SV, Pruss D, Barnstead M, Evans C, Baden H, Powell J, Glusman G, Rowen L, Hood L, Tan YH, Elgar G, Hawkins T, Venkatesh B, Rokhsar D, Brenner S., Science 297(5585), 2002
PMID: 12142439
Evidence that introns arose at proto-splice sites.
Dibb NJ, Newman AJ., EMBO J. 8(7), 1989
PMID: 2792080
Reconstruction of ancestral protosplice sites.
Sverdlov AV, Rogozin IB, Babenko VN, Koonin EV., Curr. Biol. 14(16), 2004
PMID: 15324669
Evidence for insertion of a new intron into an Mhc gene of perch-like fish.
Figueroa F, Ono H, Tichy H, O'Huigin C, Klein J., Proc. Biol. Sci. 259(1356), 1995
PMID: 7740049
Late changes in spliceosomal introns define clades in vertebrate evolution.
Venkatesh B, Ning Y, Brenner S., Proc. Natl. Acad. Sci. U.S.A. 96(18), 1999
PMID: 10468597
Unusual genomic structure: melanocortin receptors in Fugu.
Schioth HB, Haitina T, Fridmanis D, Klovins J., Ann. N. Y. Acad. Sci. 1040(), 2005
PMID: 15891089
Gene structure and functional characterization of growth hormone in dogfish, Squalus acanthias.
Moriyama S, Oda M, Yamazaki T, Yamaguchi K, Amiya N, Takahashi A, Amano M, Goto T, Nozaki M, Meguro H, Kawauchi H., Zool. Sci. 25(6), 2008
PMID: 18624571
The functional repertoires of metazoan genomes.
Ponting CP., Nat. Rev. Genet. 9(9), 2008
PMID: 18663365
Origin of introns by 'intronization' of exonic sequences.
Irimia M, Rukov JL, Penny D, Vinther J, Garcia-Fernandez J, Roy SW., Trends Genet. 24(8), 2008
PMID: 18597887
Diversity of retrotransposable elements in compact pufferfish genomes.
Volff JN, Bouneau L, Ozouf-Costaz C, Fischer C., Trends Genet. 19(12), 2003
PMID: 14642744
Genome evolution and biodiversity in teleost fish.
Volff JN., Heredity (Edinb) 94(3), 2005
PMID: 15674378
Modern origin of numerous alternatively spliced human introns from tandem arrays.
Zhuo D, Madden R, Elela SA, Chabot B., Proc. Natl. Acad. Sci. U.S.A. 104(3), 2007
PMID: 17210920
Evolution of cellular DNA content in teleost fishes
Hinegardner R., 1968
Major events in the genome evolution of vertebrates: paranome age and size differ considerably between ray-finned fishes and land vertebrates.
Vandepoele K, De Vos W, Taylor JS, Meyer A, Van de Peer Y., Proc. Natl. Acad. Sci. U.S.A. 101(6), 2004
PMID: 14757817
Animal Genome Size Database
Gregory TR., 2008
Prevalence of intron gain over intron loss in the evolution of paralogous gene families.
Babenko VN, Rogozin IB, Mekhedov SL, Koonin EV., Nucleic Acids Res. 32(12), 2004
PMID: 15254274
On the incidence of intron loss and gain in paralogous gene families.
Roy SW, Penny D., Mol. Biol. Evol. 24(8), 2007
PMID: 17470438
Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution.
International Chicken Genome Sequencing Consortium., Nature 432(7018), 2004
PMID: 15592404
US DOE Joint Genome Institute
AUTHOR UNKNOWN, 0
Danio rerio Sequencing Group at the Sanger Institute
AUTHOR UNKNOWN, 0
The Broad Institute
AUTHOR UNKNOWN, 0
The medaka draft genome and insights into vertebrate genome evolution.
Kasahara M, Naruse K, Sasaki S, Nakatani Y, Qu W, Ahsan B, Yamada T, Nagayasu Y, Doi K, Kasai Y, Jindo T, Kobayashi D, Shimada A, Toyoda A, Kuroki Y, Fujiyama A, Sasaki T, Shimizu A, Asakawa S, Shimizu N, Hashimoto S, Yang J, Lee Y, Matsushima K, Sugano S, Sakaizumi M, Narita T, Ohishi K, Haga S, Ohta F, Nomoto H, Nogata K, Morishita T, Endo T, Shin-I T, Takeda H, Morishita S, Kohara Y., Nature 447(7145), 2007
PMID: 17554307
Ensembl 2008.
Flicek P, Aken BL, Beal K, Ballester B, Caccamo M, Chen Y, Clarke L, Coates G, Cunningham F, Cutts T, Down T, Dyer SC, Eyre T, Fitzgerald S, Fernandez-Banet J, Graf S, Haider S, Hammond M, Holland R, Howe KL, Howe K, Johnson N, Jenkinson A, Kahari A, Keefe D, Kokocinski F, Kulesha E, Lawson D, Longden I, Megy K, Meidl P, Overduin B, Parker A, Pritchard B, Prlic A, Rice S, Rios D, Schuster M, Sealy I, Slater G, Smedley D, Spudich G, Trevanion S, Vilella AJ, Vogel J, White S, Wood M, Birney E, Cox T, Curwen V, Durbin R, Fernandez-Suarez XM, Herrero J, Hubbard TJ, Kasprzyk A, Proctor G, Smith J, Ureta-Vidal A, Searle S., Nucleic Acids Res. 36(Database issue), 2007
PMID: 18000006
Genome Sequencing Center at Washington University School of Medicine, St. Louis
AUTHOR UNKNOWN, 0
The UCSC Genome Browser Database: 2008 update.
Karolchik D, Kuhn RM, Baertsch R, Barber GP, Clawson H, Diekhans M, Giardine B, Harte RA, Hinrichs AS, Hsu F, Kober KM, Miller W, Pedersen JS, Pohl A, Raney BJ, Rhead B, Rosenbloom KR, Smith KE, Stanke M, Thakkapallayil A, Trumbower H, Wang T, Zweig AS, Haussler D, Kent WJ., Nucleic Acids Res. 36(Database issue), 2007
PMID: 18086701
GeneWise and Genomewise.
Birney E, Clamp M, Durbin R., Genome Res. 14(5), 2004
PMID: 15123596
The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools.
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG., Nucleic Acids Res. 25(24), 1997
PMID: 9396791
Annotation, submission and screening of repetitive elements in Repbase: RepbaseSubmitter and Censor.
Kohany O, Gentles AJ, Hankus L, Jurka J., BMC Bioinformatics 7(), 2006
PMID: 17064419
MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0.
Tamura K, Dudley J, Nei M, Kumar S., Mol. Biol. Evol. 24(8), 2007
PMID: 17488738
Export

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®
Quellen

PMID: 19698129
PubMed | Europe PMC

Suchen in

Google Scholar