Ctenidins: antimicrobial glycine-rich peptides from the hemocytes of the spider Cupiennius salei
Tóm tắt
Three novel glycine-rich peptides, named ctenidin 1–3, with activity against the Gram-negative bacterium E. coli, were isolated and characterized from hemocytes of the spider Cupiennius salei. Ctenidins have a high glycine content (>70%), similarly to other glycine-rich peptides, the acanthoscurrins, from another spider, Acanthoscurria gomesiana. A combination of mass spectrometry, Edman degradation, and cDNA cloning revealed the presence of three isoforms of ctenidin, at least two of them originating from simple, intronless genes. The full-length sequences of the ctenidins consist of a 19 amino acid residues signal peptide followed by the mature peptides of 109, 119, or 120 amino acid residues. The mature peptides are post-translationally modified by the cleavage of one or two C-terminal cationic amino acid residue(s) and amidation of the newly created mature C-terminus. Tissue expression analysis revealed that ctenidins are constitutively expressed in hemocytes and to a small extent also in the subesophageal nerve mass.
Tài liệu tham khảo
Jiravanichpaisal P, Lee BL, Söderhäll K (2006) Cell-mediated immunity in arthropods: hematopoiesis, coagulation, melanization and opsonization. Immunobiology 211:213–236
Lavine MD, Strand MR (2002) Insect hemocytes and their role in immunity. Insect Biochem Mol Biol 32:1295–1309
Hwang PM, Vogel HJ (1998) Structure-function relationships of antimicrobial peptides. Biochem Cell Biol 76:235–246
Bulet P, Stöcklin R, Menin L (2004) Anti-microbial peptides: from invertebrates to vertebrates. Immunol Rev 198:169–184
Andreu D, Rivas L (1998) Animal antimicrobial peptides: an overview. Biopolymers 47:415–433
van ‘t Hof W, Veerman EC, Helmerhorst EJ, Amerongen AV (2001) Antimicrobial peptides: properties and applicability. Biol Chem 382:597–619
Sonenshine DE, Hynes WL, Ceraul SM, Mitchell R, Benzine T (2005) Host blood proteins and peptides in the midgut of the tick Dermacentor variabilis contribute to bacterial control. Exp Appl Acarol 36:207–223
Lamberty M, Zachary D, Lanot R, Bordereau C, Robert A, Hoffmann JA, Bulet P (2001) Insect immunity: constitutive expression of a cysteine-rich antifungal and a linear antibacterial peptide in a termite insect. J Biol Chem 276:4085–4092
Mitta G, Vandenbulcke F, Roch P (2000) Original involvement of antimicrobial peptides in mussel innate immunity. FEBS Lett 486:185–190
Destoumieux D, Munoz M, Cosseau C, Rodriguez J, Bulet P, Comps M, Bachère E (2000) Penaeidins, antimicrobial peptides with chitin-binding activity, are produced and stored in shrimp granulocytes and released after microbial challenge. J Cell Sci 113:461–469
Iwanaga S, Lee BL (2005) Recent advances in the innate immunity of invertebrate animals. J Biochem Mol Biol 38:128–150
Rodríguez de la Vega RC, García BI, D’Ambrosio C, Diego-García E, Scaloni A, Possani LD (2004) Antimicrobial peptide induction in the haemolymph of the Mexican scorpion Centruroides limpidus limpidus in response to septic injury. Cell Mol Life Sci 61:1507–1519
Lorenzini DM, da Silva PI Jr, Fogaça AC, Bulet P, Daffre S (2003) Acanthoscurrin: a novel glycine-rich antimicrobial peptide constitutively expressed in the hemocytes of the spider Acanthoscurria gomesiana. Dev Comp Immunol 27:781–791
Silva PI Jr, Daffre S, Bulet P (2000) Isolation and characterization of gomesin, an 18-residue cysteine-rich defense peptide from the spider Acanthoscurria gomesiana hemocytes with sequence similarities to horseshoe crab antimicrobial peptides of the tachyplesin family. J Biol Chem 275:33464–33470
Fukuzawa AH, Vellutini BC, Lorenzini DM, Silva PI Jr, Mortara RA, da Silva JM, Daffre S (2008) The role of hemocytes in the immunity of the spider Acanthoscurria gomesiana. Dev Comp Immunol 32:716–725
Egorov TA, Odintsova TI, Pukhalsky VA, Grishin EV (2005) Diversity of wheat anti-microbial peptides. Peptides 26:2064–2073
Park CJ, Park CB, Hong SS, Lee HS, Lee SY, Kim SC (2000) Characterization and cDNA cloning of two glycine- and histidine-rich antimicrobial peptides from the roots of shepherd’s purse, Capsella bursa-pastoris. Plant Mol Biol 44:187–197
El Amri C, Nicolas P (2008) Plasticins: membrane-damaging peptides with ‘chameleon-like’ properties. Cell Mol Life Sci 65:895–909
Herbinière J, Braquart-Varnier C, Grève P, Strub JM, Frère J, Van Dorsselaer A, Martin G (2005) Armadillidin: a novel glycine-rich antibacterial peptide directed against gram-positive bacteria in the woodlouse Armadillidium vulgare (terrestrial isopod, Crustacean). Dev Comp Immunol 29:489–499
Otvos L Jr (2000) Antibacterial peptides isolated from insects. J Pept Sci 6:497–511
Sperstad SV, Haug T, Vasskog T, Stensvag K (2009) Hyastatin, a glycine-rich multi-domain antimicrobial peptide isolated from the spider crab (Hyas araneus) hemocytes. Mol Immunol 46:2604–2612
Söderhäll K, Smith VJ (1983) Separation of the haemocyte populations of Carcinus maenas and other marine decapods, and prophenoloxidase distribution. Dev Comp Immunol 7:229–239
Chang JY, Knecht R (1991) Direct analysis of the disulfide content of proteins: methods for monitoring the stability and refolding process of cystine-containing proteins. Anal Biochem 197:52–58
Bidlingmeyer BA, Cohen SA, Tarvin TL (1984) Rapid analysis of amino acids using pre-column derivatization. J Chromatogr 336:93–104
Pereira LS, Silva PI Jr, Miranda MT, Almeida IC, Naoki H, Konno K, Daffre S (2007) Structural and biological characterization of one antibacterial acylpolyamine isolated from the hemocytes of the spider Acanthocurria gomesiana. Biochem Biophys Res Commun 352:953–959
Choi SJ, Parent R, Guillaume C, Deregnaucourt C, Delarbre C, Ojcius DM, Montagne JJ, Celerier ML, Phelipot A, Amiche M, Molgo J, Camadro JM, Guette C (2004) Isolation and characterization of Psalmopeotoxin I and II: two novel antimalarial peptides from the venom of the tarantula Psalmopoeus cambridgei. FEBS Lett 572:109–117
Ostrow KL, Mammoser A, Suchyna T, Sachs F, Oswald R, Kubo S, Chino N, Gottlieb PA (2003) cDNA sequence and in vitro folding of GsMTx4, a specific peptide inhibitor of mechanosensitive channels. Toxicon 42:263–274
Kapuscinski M, Green M, Sinha SN, Shepherd JJ, Shulkes A (1993) Peptide alpha-amidation activity in human plasma: relationship to gastrin processing. Clin Endocrinol 39:51–58
Dai L, Corzo G, Naoki H, Andriantsiferana M, Nakajima T (2002) Purification, structure-function analysis, and molecular characterization of novel linear peptides from scorpion Opisthacanthus madagascariensis. Biochem Biophys Res Commun 293:1514–1522
Zeng XC, Wang SX, Zhu Y, Zhu SY, Li WX (2004) Identification and functional characterization of novel scorpion venom peptides with no disulfide bridge from Buthus martensii Karsch. Peptides 25:143–150
Destoumieux D, Bulet P, Loew D, Van Dorsselaer A, Rodriguez J, Bachère E (1997) Penaeidins, a new family of antimicrobial peptides isolated from the shrimp Penaeus vannamei (Decapoda). J Biol Chem 272:28398–28406
Nakamura T, Furunaka H, Miyata T, Tokunaga F, Muta T, Iwanaga S, Niwa M, Takao T, Shimonishi Y (1988) Tachyplesin, a class of antimicrobial peptide from the hemocytes of the horseshoe crab (Tachypleus tridentatus): isolation and chemical structure. J Biol Chem 263:16709–16713
Lorenzini DM, Fukuzawa AH, da Silva PI Jr, Machado-Santelli G, Bijovsky AT, Daffre S (2003) Molecular cloning, expression analysis and cellular localization of gomesin, an anti-microbial peptide from hemocytes of the spider Acanthoscurria gomesiana. Insect Biochem Mol Biol 33:1011–1016
Shigenaga T, Muta T, Toh Y, Tokunaga F, Iwanaga S (1990) Antimicrobial tachyplesin peptide precursor: cDNA cloning and cellular localization in the horseshoe crab (Tachypleus tridentatus). J Biol Chem 265:21350–21354
Schikorski D, Cuvillier-Hot V, Leippe M, Boidin-Wichlacz C, Slomianny C, Macagno E, Salzet M, Tasiemski A (2008) Microbial challenge promotes the regenerative process of the injured central nervous system of the medicinal leech by inducing the synthesis of antimicrobial peptides in neurons and microglia. J Immunol 181:1083–1095
Damen WG, Hausdorf M, Seyfarth EA, Tautz D (1998) A conserved mode of head segmentation in arthropods revealed by the expression pattern of Hox genes in a spider. Proc Natl Acad Sci USA 95:10665–10670
Schwager EE, Schoppmeier M, Pechmann M, Damen WG (2007) Duplicated Hox genes in the spider Cupiennius salei. Front Zool 4:10
Winans KA, King DS, Rao VR, Bertozzi CR (1999) A chemically synthesized version of the insect antibacterial glycopeptide, diptericin, disrupts bacterial membrane integrity. Biochemistry 38:11700–11710
Park KH, Park Y, Park IS, Hahm KS, Shin SY (2008) Bacterial selectivity and plausible mode of antibacterial action of designed Pro-rich short model antimicrobial peptides. J Pept Sci 14:876–882
Sagisaka A, Miyanoshita A, Ishibashi J, Yamakawa M (2001) Purification, characterization and gene expression of a glycine and proline-rich antibacterial protein family from larvae of a beetle, Allomyrina Dichotoma. Insect Mol Biol 10:293–302
Carlsson A, Engström P, Palva ET, Bennich H (1991) Attacin, an antibacterial protein from Hyalophora cecropia, inhibits synthesis of outer membrane proteins in Escherichia coli by interfering with omp gene transcription. Infect Immun 59:3040–3045
Kragol G, Lovas S, Varadi G, Condie BA, Hoffmann R, Otvos L (2001) The antibacterial peptide pyrrhocoricin inhibits the ATPase actions of dnak and prevents chaperone-assisted protein folding. Biochemistry 40:3016–3026
Remuzgo C, Andrade GF, Temperini ML, Miranda MT (2009) Acanthoscurrin fragment 101–132: total synthesis at 60°C of a novel difficult sequence. Biopolymers (Pep Sci) 92:65–75
El Amri C, Lacombe C, Zimmerman K, Ladram A, Amiche M, Nicolas P, Bruston F (2006) The plasticins: membrane adsorption, lipid disorders, and biological activity. Biochemistry 45:14285–14297
Sousa JC, Berto RF, Gois EA, Fontenele-Cardi NC, Honório JE Jr, Konno K, Richardson M, Rocha MF, Camargo AA, Pimenta DC, Cardi BA, Carvalho KM (2009) Leptoglycin: a new Glycine/Leucine-rich antimicrobial peptide isolated from the skin secretion of the South American frog Leptodactylus pentadactylus (Leptodactylidae). Toxicon 54:23–32
Beamer LJ, Carroll SF, Eisenberg D (1998) The BPI/LBP family of proteins: a structural analysis of conserved regions. Protein Sci 7:906–914
Iijima R, Kurata S, Natori S (1993) Purification, characterization, and cDNA cloning of an antifungal protein from the hemolymph of Sarcophaga peregrina (flesh fly) larvae. J Biol Chem 268:12055–12061
Lee SY, Moon HJ, Kurata S, Natori S, Lee BL (1995) Purification and cDNA cloning of an antifungal protein from the hemolymph of Holotrichia diomphalia larvae. Biol Pharm Bull 18:1049–1052
Pelegrini PB, Murad AM, Silva LP, Dos Santos RC, Costa FT, Tagliari PD, Bloch C Jr, Noronha EF, Miller RN, Franco OL (2008) Identification of a novel storage glycine-rich peptide from guava (Psidium guajava) seeds with activity against Gram-negative bacteria. Peptides 29:1271–1279
Sachetto-Martins G, Franco LO, de Oliveira DE (2000) Plant glycine-rich proteins: a family or just proteins with a common motif? Biochim Biophys Acta 1492:1–14
Lee YJ, Chung TJ, Park CW, Hahn Y, Chung JH, Lee BL, Han DM, Jung YH, Kim S, Lee Y (1996) Structure and expression of the tenecin 3 gene in Tenebrio molitor. Biochem Biophys Res Commun 218:6–11