Skip to main content
SpringerLink
Log in

Extranuclear Histones in Teleost Gills: An Evolutionary Study

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

Extranuclear histones and histone fragments (13–15 kDa) in gill microsomes of a phylogenetic series of teleostean fishes (tilapia, trout, carp, eel and elephant fish) were studied. Histones H2A and H2B are the first occurring of these antimicrobial agents. Halfway the evolution of teleosts (carp, trout) H3 fragments emerge, which disappear in later stages of development and are replaced by truncated H1 (tilapia). The hypothesis is forwarded that variation in composition of extranuclear histones is caused by changes in specificity of histone transporters.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • S.A. Adam R. Sterne Mar L. Gerace (1990) ArticleTitleNuclear protein import in permeabilized mammalian cells requires soluble cytoplasmic factors J. Cell Biol. 111 807–816 Occurrence Handle10.1083/jcb.111.3.807 Occurrence Handle2391365 Occurrence Handle1:CAS:528:DyaK3cXlt12kt7s%3D

    Article  PubMed  CAS  Google Scholar 

  • G.S. Bailey G.H. Dixon (1973) ArticleTitleHistone IIb 1 from rainbow trout. Comparison in amino acid sequence with calf thymus IIb 1 J. Biol. Chem. 248 5463–5472 Occurrence Handle4768909 Occurrence Handle1:CAS:528:DyaE3sXltVWrs7g%3D

    PubMed  CAS  Google Scholar 

  • Bara, D. and Bossa, F. 1998. Hemoglobin beta chain (Leisostomus xanthurus). Unpublished, Swiss-Prot accession # P56251

  • W.F. Brandt W.N. Strickland C. Holt ParticleVon (1974) ArticleTitleThe primary structure of histone F3 from shark erythrocytes FEBS Lett. 40 IssueID2 349–352 Occurrence Handle10.1016/0014-5793(74)80261-9 Occurrence Handle4855011 Occurrence Handle1:CAS:528:DyaE2cXksVKmtbo%3D

    Article  PubMed  CAS  Google Scholar 

  • Chandler, V.L., Cone, K.C., Kaeppler, H.F., Kaeppler, S.M. 2002. Sequences from the Plant Chromatin Consortium (NSF Plant Genome project 9975930): EMBL accession # AAL73043

  • J.H. Cho I.Y. Park H.S. Kim W.T. Lee M.S. Kim S.C. Kim (2002a) ArticleTitleCathepsin D produces antimicrobial peptide parasin I from histone H2A in the skin mucosa of fish FASEB J. 16 429–431 Occurrence Handle1:CAS:528:DC%2BD38XhvValurg%3D

    CAS  Google Scholar 

  • J.H. Cho I.Y. Park M.S. Kim S.C. Kim (2002b) ArticleTitleMatrix metalloproteinase 2 is involved in the regulation of the antimicrobial peptide parasin I production in catfish skin mucosa FEBS Lett. 531 459–463 Occurrence Handle10.1016/S0014-5793(02)03584-6 Occurrence Handle1:CAS:528:DC%2BD38XosFCksLg%3D

    Article  CAS  Google Scholar 

  • M.I. Concha V.J. Smith K. Castro A. Bastias A. Romero R.J. Amthauer (2004) ArticleTitleApolipoproteins A-I and A-II are potentially important effectors of innate immunity of the teleost fish Cyprinus carpio Eur. J. Biochem. 271 2984–2990 Occurrence Handle10.1111/j.1432-1033.2004.04228.x Occurrence Handle15233794 Occurrence Handle1:CAS:528:DC%2BD2cXmtVyrtb0%3D

    Article  PubMed  CAS  Google Scholar 

  • G. Crambert M. Füzesi H. Garty S. Karlish K. Geering (2002) ArticleTitlePhospholemman (FXYD1) associates with Na,K-ATPase and regulates its transport properties Proc. Natl. Acad. Sci. USA 99 11476–11481 Occurrence Handle10.1073/pnas.182267299 Occurrence Handle12169672 Occurrence Handle1:CAS:528:DC%2BD38XmslSlsrc%3D

    Article  PubMed  CAS  Google Scholar 

  • G.J. Dolecki T. Humphreys (1988) ArticleTitleAn engrailed class homeo box gene in sea urchins Gene 64 IssueID1 21–31 Occurrence Handle10.1016/0378-1119(88)90477-5 Occurrence Handle2899533 Occurrence Handle1:CAS:528:DyaL1cXktFyjtb0%3D

    Article  PubMed  CAS  Google Scholar 

  • W.P. Dubinski L.B. Monti (1986) ArticleTitleResolution of apical from basolateral membrane of shark rectal gland Am. J. Physiol. 251 IssueID20 C721–C726

    Google Scholar 

  • P. Edmann (1956) ArticleTitleOn the mechanism of phenyl isothiocyanate degradation of peptides Acta Chem. Scand. 10 761–768

    Google Scholar 

  • M.D. Esteve-Gassent M.E. Nielson C. Amaro (2003) ArticleTitleThe kinetics of antibody production in mucus and serum of European eel (Anguilla anguilla L.) after vaccination against Vibrio vulnificus : development of a new method for antibody quantification in skin mucus Fish Shellfish Immunol. 15 51–61 Occurrence Handle10.1016/S1050-4648(02)00138-9 Occurrence Handle12787687 Occurrence Handle1:CAS:528:DC%2BD3sXkt1Orur0%3D

    Article  PubMed  CAS  Google Scholar 

  • A. Fago V. Carratore G. diPrisco R.J. Feuerlein L. Sottrup-Jensen R.E. Weber (1995) ArticleTitleThe cathodic hemoglobin of Anguilla anguilla. Amino acid sequence and oxygen equilibria of a reverse Bohr effect hemoglobin with high oxygen affinity and high phosphate sensitivity J. Biol. Chem. 270 118897–18902

    Google Scholar 

  • A. Fago E. Bendixen H. Malte R.E. Weber (1997) ArticleTitleThe anodic hemoglobin of Anguilla anguilla. Molecular basis for allosteric effects in a root-effect hemoglobin J. Biol. Chem. 272 15628–15635 Occurrence Handle10.1074/jbc.272.25.15628 Occurrence Handle9188451 Occurrence Handle1:CAS:528:DyaK2sXktFCgsbs%3D

    Article  PubMed  CAS  Google Scholar 

  • J.M.O. Fernandes G.D. Kemp M.G. Molle V.J. Smith (2002) ArticleTitleAnti-microbial properties of histone H2A from skin secretions of rainbow trout, Oncorhynchus mykiss Biochem. J. 368 611–620 Occurrence Handle10.1042/BJ20020980 Occurrence Handle12164782 Occurrence Handle1:CAS:528:DC%2BD38XovF2jtbo%3D

    Article  PubMed  CAS  Google Scholar 

  • J.M.O. Fernandes G. Molle G.D. Kemp V.J. Smith (2004) ArticleTitleIsolation and characterisation of oncorhyncin II, a histone H1-derived antimicrobial peptide from skin secretions of rainbow trout, Oncorhynchus mykiss Dev. Comp. Immunol. 28 127–138 Occurrence Handle12969798 Occurrence Handle1:CAS:528:DC%2BD3sXntVGntLw%3D

    PubMed  CAS  Google Scholar 

  • J.S. Fruton S. Simmonds (1958) General Biochemistry NumberInSeries2 John Wiley & Sons New York 691

    Google Scholar 

  • R.G. Gillen A. Riggs (1973) ArticleTitleThe hemoglobins of a fresh-water teleost Cichlasoma cyanoguttatum (Baird and Girard). II. Subunit structure and oxygen equilibria of the isolated components Arch. Biochem. Biophys. 154 IssueID1 348–359 Occurrence Handle10.1016/0003-9861(73)90067-2 Occurrence Handle4689783 Occurrence Handle1:CAS:528:DyaE3sXotFajug%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • R. Goldshleger D.M. Tal S.J.D. Karlish (1995) ArticleTitleTopology of the α-subunit of Na,K-ATPase based on proteolysis. Lability of the topological organization Biochemistry 34 8668–8679 Occurrence Handle10.1021/bi00027a016 Occurrence Handle7612607 Occurrence Handle1:CAS:528:DyaK2MXmsVehsrk%3D

    Article  PubMed  CAS  Google Scholar 

  • D. Görlich N. Panté U. Kutay U. Aebi F.R. Bischoff (1996) ArticleTitleIdentification of different roles for RanGDP and RanGTP in nuclear protein import EMBO J. 15 IssueID20 5584–5594 Occurrence Handle8896452

    PubMed  Google Scholar 

  • B. Grujic-Injac G. Braunitzer A. Stangl (1980) ArticleTitleHämoglobine XXXV. Die Sequenz der βA- and βB-Ketten der Hämoglobine des Karpfens (Cyprinus carpio L.) Hoppe Seyler’s Z. Physiol. Chem. 361 1629–1639 Occurrence Handle7450680 Occurrence Handle1:CAS:528:DyaL3MXhtFymsA%3D%3D

    PubMed  CAS  Google Scholar 

  • S. Jäkel D. Görlich (1998) ArticleTitleImportin β, transportin, RanBP5 and RanBP7 mediate nuclear import of ribosomal proteins in mammalian cells EMBO J. 17 4491–4502 Occurrence Handle9687515

    PubMed  Google Scholar 

  • S. Jäkel W. Albig U. Kutay F.R. Bischoff K. Schwamborn D. Doenecke D. Görlich (1999) ArticleTitleThe importin β/importin 7 hetrodimer is a functional nuclear import receptor for histone H1 EMBO J. 18 2411–2423 Occurrence Handle10228156

    PubMed  Google Scholar 

  • H. Kondo I. Kawazoe M. Nakaya K. Kikuchi K. Aida S. Watabe (2001) ArticleTitleThe novel sequences of major plasma apolipoproteins in the eel Anguilla japonica Biochim. Biophys. Acta 1531 132–142 Occurrence Handle11278178 Occurrence Handle1:CAS:528:DC%2BD3MXit1Shsbc%3D

    PubMed  CAS  Google Scholar 

  • A. Kootstra G.S. Bailey (1978) ArticleTitlePrimary structure of histone H2B from trout (Salmo trutta) testes Biochemistry 17 2504–2510 Occurrence Handle10.1021/bi00606a008 Occurrence Handle678528 Occurrence Handle1:CAS:528:DyaE1cXltVahsLw%3D

    Article  PubMed  CAS  Google Scholar 

  • Y.A. Mahmmoud G. Cramb A.B. Maunsbach C.P. Cutler L. Meischke F. Cornelius (2003) ArticleTitleRegulation of Na,K-ATPase by PLMS, the phospholemman-like protein from shark. Molecular cloning, sequence, expression, cellular distribution and functional effects of PLMS J. Biol. Chem. 278 37427–37438 Occurrence Handle10.1074/jbc.M305126200 Occurrence Handle12874284 Occurrence Handle1:CAS:528:DC%2BD3sXnsV2ls70%3D

    Article  PubMed  CAS  Google Scholar 

  • K. Maruyama T. Mikawa S. Ebashi (1984) ArticleTitleDetection of calcium binding proteins by 45Ca autoradiography on nitrocellulose membrane after sodium dodecyl sulfate gel electrophoresis J. Biochem. 95 511–519 Occurrence Handle6715311 Occurrence Handle1:CAS:528:DyaL2cXhtlGgtL8%3D

    PubMed  CAS  Google Scholar 

  • J. Mezquita W. Connor R.J. Winkfein G.H. Dixon (1985) ArticleTitleAn H1 histone gene from rainbow trout (Salmo gairdnerii) J. Mol. Evol. 21 209–219 Occurrence Handle10.1007/BF02102355 Occurrence Handle1:CAS:528:DyaL2MXks1GqsL4%3D

    Article  CAS  Google Scholar 

  • J.R. Moorman S.J. Ackerman G.C. Kowdley M.P. Griffin J.P. Mounsey Z. Chen S.E. Cala J.J. O’Brian G. Szabo L.R. Jones (1995) ArticleTitleUnitary anion currents through phospholemman channel molecules Nature 377 737–740 Occurrence Handle10.1038/377737a0 Occurrence Handle7477264 Occurrence Handle1:CAS:528:DyaK2MXovFygu7w%3D

    Article  PubMed  CAS  Google Scholar 

  • N. Mosammaparast K.R. Jackson Y. Guo C.J. Brame J. Shabanowitz D.F. Hunt L.F. Pemberton (2001) ArticleTitleNuclear import of histone H2A and H2B is mediated by a network of karyopherins J. Cell. Biol. 153 251–262 Occurrence Handle10.1083/jcb.153.2.251 Occurrence Handle11309407 Occurrence Handle1:CAS:528:DC%2BD3MXivFOiur0%3D

    Article  PubMed  CAS  Google Scholar 

  • N. Mosammaparast Y. Guo J. Shabanowitz D.F. Hunt L.F. Pemberton (2002) ArticleTitlePathways mediating the nuclear import of histones H3 and H4 in yeast J. Biol. Chem. 277 862–868 Occurrence Handle11694505 Occurrence Handle1:CAS:528:DC%2BD38XjslGrsw%3D%3D

    PubMed  CAS  Google Scholar 

  • P. Muhlhäusser E.-C. Müller A. Otto U. Kutay (2001) ArticleTitleMultiple pathways contribute to nuclear import of core histones EMBO Rep. 2 IssueID8 690–696 Occurrence Handle11493596

    PubMed  Google Scholar 

  • E.J. Noga Z. Fan U. Silphaduang (2001) ArticleTitleHistone-like proteins from fish are lethal to the parasitic dinoflagellate Amylodinium ocellatum Parasitology 123 57–65 Occurrence Handle10.1017/S0031182001007971 Occurrence Handle11467783 Occurrence Handle1:CAS:528:DC%2BD3MXmtVyisLY%3D

    Article  PubMed  CAS  Google Scholar 

  • K. Okamoto M. Sakai M. Miyata (2001) ArticleTitleMolecular cloning and sequence analysis of α- and β-globin cDNAs from yellowtail, Seriola quinqueradiata Comp. Biochem. Physiol. B 130 207–216 Occurrence Handle11544091 Occurrence Handle1:STN:280:DC%2BD3MvpsFentg%3D%3D

    PubMed  CAS  Google Scholar 

  • C.J. Palmer B.T. Scott L.R. Jones (1991) ArticleTitlePurification and complete sequence determination of the major plasma membrane substrate for c-AMP-dependent protein kinase and protein kinase C in myocardium J. Biol. Chem. 266 11126–11130 Occurrence Handle1710217 Occurrence Handle1:CAS:528:DyaK3MXkvVyisrY%3D

    PubMed  CAS  Google Scholar 

  • N. Panté U. Aebi (1996) ArticleTitleSequential binding of import ligands to distinct nucleopore regions during their nuclear import Science 273 1729–1732 Occurrence Handle8781239

    PubMed  Google Scholar 

  • C.B. Park H.S. Kim S.C. Kim (1998) ArticleTitleMechanism of action of the antimicrobial peptide buforin II: buforin II kills microorganisms by penetrating the cell membrane and inhibiting cellular functions Biochem. Biophys. Res. Commun. 244 253–257 Occurrence Handle9514864 Occurrence Handle1:CAS:528:DyaK1cXhslClsL4%3D

    PubMed  CAS  Google Scholar 

  • C.B. Park K.-S. Yi K. Matsuzaki M.S. Kim S.C. Kim (2000) ArticleTitleStructure-activity analysis of buforin II, a histone H2A-derived antimicrobial peptide: the proline hinge is responsible for the cell-penetrating ability of buforin II. Proc. Natl. Acad. Sci. USA 97 8245–8250 Occurrence Handle10890923 Occurrence Handle1:CAS:528:DC%2BD3cXlt1Ggt7w%3D

    PubMed  CAS  Google Scholar 

  • Y. Park C.B. Park M.S. Kim S.C. Kim (1998) ArticleTitleParasin I, an antimicrobial peptide derived from histone H2A in the catfish, Parasilurus asotis FEBS Lett. 437 258–262 Occurrence Handle10.1016/S0014-5793(98)01238-1 Occurrence Handle9824303 Occurrence Handle1:CAS:528:DyaK1cXntVyht7g%3D

    Article  PubMed  CAS  Google Scholar 

  • A. Patrzykat L. Zhang V. Mendoza G.K. Iwama R.E.W. Hancock (2001) ArticleTitleSynergy of histone-derived peptides of coho salmon with lysozyme and flounder pleurocidin Antimicrob. Agents Chemother. 45 1337–1342 Occurrence Handle10.1128/AAC.45.5.1337-1342.2001 Occurrence Handle11302792 Occurrence Handle1:CAS:528:DC%2BD3MXjtF2hurg%3D

    Article  PubMed  CAS  Google Scholar 

  • G.L. Peterson (1977) ArticleTitleA simplification of the protein assay method of Lowry et al. which is more generally applicable Anal. Biochem. 83 346–356 Occurrence Handle10.1016/0003-2697(77)90043-4 Occurrence Handle603028 Occurrence Handle1:CAS:528:DyaE1cXntFWjtQ%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • R. Petruzzelli D. Barra B.M. Goffredo F. Bossa M. Coletta M. Brunori (1984) ArticleTitleAmino-acid sequence of beta-chain of hemoglobin IV from trout (Salmo irideus) Biochim. Biophys. Acta 789 69–73 Occurrence Handle1:CAS:528:DyaL2cXmtVKht7s%3D

    CAS  Google Scholar 

  • D. Robinette S. Wada T. Arrol M.G. Levy W.L. Miller E.J. Noga (1998) ArticleTitleAntimicrobial activity in the skin of the channel catfish Ictalurus punctatus: characterization of broad-spectrum histone-like antimicrobial proteins Cell. Mol. Life Sci. 54 467–475 Occurrence Handle9645227 Occurrence Handle1:CAS:528:DyaK1cXjsFyit7Y%3D Occurrence Handle10.1007/s000180050175

    Article  PubMed  CAS  Google Scholar 

  • F.M.A.H. Schuurmans Stekhoven G. Flik S.E. Wendelaar Bonga (2001) ArticleTitleN-terminal sequences of small ion channels in rectal glands of sharks: a biochemical hallmark for classification and phylogeny? Biochem Biophys. Res. Commun. 288 670–675 Occurrence Handle1:CAS:528:DC%2BD3MXnslCrs74%3D

    CAS  Google Scholar 

  • F.M.A.H. Schuurmans Stekhoven E. Grell W. Atsma G. Flik S.E. Wendelaar Bonga (2003) ArticleTitleOrgan-related distribution of phospholemman in the spiny dogfish Squalus acanthias Biochem. Biophys. Res. Commun. 303 1008–1011 Occurrence Handle10.1016/S0006-291X(03)00472-8 Occurrence Handle12684034 Occurrence Handle1:CAS:528:DC%2BD3sXis12gsbw%3D

    Article  PubMed  CAS  Google Scholar 

  • K.J. Sweadner E. Rael (2000) ArticleTitleThe FXYD gene family of small ion transport regulators or channels: cDNA sequence, protein signature sequence and expression Genomics 68 41–56 Occurrence Handle10.1006/geno.2000.6274 Occurrence Handle10950925 Occurrence Handle1:CAS:528:DC%2BD3cXlslCqtLo%3D

    Article  PubMed  CAS  Google Scholar 

  • B. Szewczyk L.M. Kozloff (1985) ArticleTitleA method for the efficient blotting of strongly basic proteins from sodium dodecyl sulfate-polyacrylamide gels to nitrocellulose Anal. Biochem. 150 403–407 Occurrence Handle10.1016/0003-2697(85)90528-7 Occurrence Handle4091265 Occurrence Handle1:CAS:528:DyaL2MXmtFSgsrc%3D

    Article  PubMed  CAS  Google Scholar 

  • O. Walaas R.S. Horn S.I. Walaas (1999) ArticleTitleInhibition of insulin-stimulated phosphorylation of the intracellular domain of phospholemman decreases insulin-dependent GLUT4 translocation in streptolysin-O-permeabilized adipocytes Biochem. J. 343 151–157 Occurrence Handle10.1042/0264-6021:3430151 Occurrence Handle10493924 Occurrence Handle1:CAS:528:DyaK1MXmvVyjurY%3D

    Article  PubMed  CAS  Google Scholar 

  • J.E. Walker R. Lutter A. Dupuis M.J. Runswick (1991) ArticleTitleIdentification of the subunits of F1F0-ATPase from bovine heart mitochondria Biochemistry 30 5369–5378 Occurrence Handle1827992 Occurrence Handle1:CAS:528:DyaK3MXisVentrY%3D

    PubMed  CAS  Google Scholar 

  • Walker, P., Schuurmans Stekhoven, F., Duijf, R., Russon, I., Wendelaar Bonga, S. 2004. Are certain fish immune to the ectoparasitic crustacean, Argulus japonicus Theile (crustacea: branchiura)? 6th Int. Symp. Fish Immunol., Univ. Turku, Turku, Finland May 24–29, P-45

  • K. Watson R.J. Edwards S. Shaunak D.C. Parmelee C. Sarraf N.J. Gooderham D.S. Davies (1995) ArticleTitleExtra-nuclear location of histones in activated human peripheral blood lymphocytes and cultured T-cells Biochem. Pharmacol. 50 299–309 Occurrence Handle10.1016/0006-2952(95)00142-M Occurrence Handle7646532 Occurrence Handle1:CAS:528:DyaK2MXnsVeqt7g%3D

    Article  PubMed  CAS  Google Scholar 

  • R.J. Winkfein W. Connor J. Mezquita G.H. Dixon (1985) ArticleTitleHistone H4 and H2B genes in rainbow trout (Salmo gairdnerii) J. Mol. Evol. 22 1–19 Occurrence Handle10.1007/BF02105800 Occurrence Handle2997457 Occurrence Handle1:CAS:528:DyaL2MXlsFGit74%3D

    Article  PubMed  CAS  Google Scholar 

  • J.A. Zadunaisky (1984) The chloride cell: the active transport of chloride and the paracellular pathways W.S. Hoar D.J. Randall (Eds) Fish Physiology NumberInSeriesVol. X (B) Academic Press New York 129–176

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Animal Physiology, Faculty of Science, Radboud University Nijmegen, Toernooiveld 1, 6525, ED, Nijmegen, The Netherlands

    F. M. A. H. Schuurmans Stekhoven, S. E. Wendelaar Bonga & G. Flik

Authors
  1. F. M. A. H. Schuurmans Stekhoven
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. E. Wendelaar Bonga
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. G. Flik
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to G. Flik.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Stekhoven, F.M.A.H.S., Bonga, S.E.W. & Flik, G. Extranuclear Histones in Teleost Gills: An Evolutionary Study. Fish Physiol Biochem 30, 201–211 (2004). https://doi.org/10.1007/s10695-005-7442-5

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-005-7442-5

Keywords

Search

Navigation