Abstract
Proline-rich antimicrobial peptides are a group of cationic host defense peptides of vertebrates and invertebrates characterized by a high content of proline residues, often associated with arginine residues in repeated motifs. Those isolated from some mammalian and insect species, although not evolutionarily related, use a similar mechanism to selectively kill Gram-negative bacteria, with a low toxicity to animals. Unlike other types of antimicrobial peptides, their mode of action does not involve the lysis of bacterial membranes but entails penetration into susceptible cells, where they then act intracellularly. Some aspects of the transport system and cytoplasmic targets have been elucidated. These features make them attractive both as anti-infective lead compounds and as a new class of potential cell-penetrating peptides capable of internalising membrane-impermeant drugs into both bacterial and eukaryotic cells
Similar content being viewed by others
Abbreviations
- AMP:
-
Antimicrobial peptide
- CPP:
-
Cell-penetrating peptide
- LPS:
-
Lipopolysaccharide
- PR-AMP:
-
Proline-rich AMPs
- HDP:
-
Host defence peptide
References
Zasloff M (2002) Antimicrobial peptides of multicellular organisms. Nature 415:389–395
Brogden KA (2005) Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat Rev Microbiol 3:238–250
Hancock RE, Brown KL, Mookherjee N (2006) Host defence peptides from invertebrates—emerging antimicrobial strategies. Immunobiology 211:315–322
Matsuzaki K (2009) Control of cell selectivity of antimicrobial peptides. Biochim Biophys Acta 1788:1687–1692
Casteels P, Ampe C, Jacobs F, Vaeck M, Tempst P (1989) Apidaecins: antibacterial peptides from honeybees. EMBO J 8:2387–2391
Boman HG, Agerberth B, Boman A (1993) Mechanisms of action on Escherichia coli of cecropin P1 and PR-39, two antibacterial peptides from pig intestine. Infect Immun 61:2978–2984
Podda E, Benincasa M, Pacor S, Micali F, Mattiuzzo M, Gennaro R, Scocchi M (2006) Dual mode of action of Bac7, a proline-rich antibacterial peptide. Biochim Biophys Acta 1760:1732–1740
Casteels P, Tempst P (1994) Apidaecin-type peptide antibiotics function through a non-poreforming mechanism involving stereospecificity. Biochem Biophys Res Commun 199:339–345
Gennaro R, Zanetti M, Benincasa M, Podda E, Miani M (2002) Pro-rich antimicrobial peptides from animals: structure, biological functions and mechanism of action. Curr Pharm Des 8:763–778
Gennaro R, Skerlavaj B, Romeo D (1989) Purification, composition, and activity of two bactenecins, antibacterial peptides of bovine neutrophils. Infect Immun 57:3142–3146
Bulet P, Urge L, Ohresser S, Hetru C, Otvos L Jr (1996) Enlarged scale chemical synthesis and range of activity of drosocin, an O-glycosylated antibacterial peptide of Drosophila. Eur J Biochem 238:64–69
Castle M, Nazarian A, Yi SS, Tempst P (1999) Lethal effects of apidaecin on Escherichia coli involve sequential molecular interactions with diverse targets. J Biol Chem 274:32555–32564
Otvos L Jr (2002) The short proline-rich antibacterial peptide family. Cell Mol Life Sci 59:1138–1150
Li J, Xu X, Yu H, Yang H, Huang Z, Lai R (2006) Direct antimicrobial activities of PR-bombesin. Life Sci 78:1953–1956
Schnapp D, Kemp GD, Smith VJ (1996) Purification and characterization of a proline-rich antibacterial peptide, with sequence similarity to bactenecin-7, from the haemocytes of the shore crab, Carcinus maenas. Eur J Biochem 240:532–539
Destoumieux D, Bulet P, Strub JM, Van Dorsselaer A, Bachere E (1999) Recombinant expression and range of activity of penaeidins, antimicrobial peptides from penaeid shrimp. Eur J Biochem 266:335–346
Rolland JL, Abdelouahab M, Dupont J, Lefevre F, Bachere E, Romestand B (2010) Stylicins, a new family of antimicrobial peptides from the Pacific blue shrimp Litopenaeus stylirostris. Mol Immunol 47:1269–1277
Gueguen Y, Bernard R, Julie F, Paulina S, Delphine DG, Franck V, Philippe B, Evelyne B (2009) Oyster hemocytes express a proline-rich peptide displaying synergistic antimicrobial activity with a defensin. Mol Immunol 46:516–522
Zanetti M, Gennaro R, Scocchi M, Skerlavaj B (2000) Structure and biology of cathelicidins. Adv Exp Med Biol 479:203–218
Lehrer RI, Ganz T (2002) Cathelicidins: a family of endogenous antimicrobial peptides. Curr Opin Hematol 9:18–22
Scocchi M, Skerlavaj B, Romeo D, Gennaro R (1992) Proteolytic cleavage by neutrophil elastase converts inactive storage proforms to antibacterial bactenecins. Eur J Biochem 209:589–595
Frank RW, Gennaro R, Schneider K, Przybylski M, Romeo D (1990) Amino acid sequences of two proline-rich bactenecins. Antimicrobial peptides of bovine neutrophils. J Biol Chem 265:18871–18874
Scocchi M, Wang S, Gennaro R, Zanetti M (1998) Cloning and analysis of a transcript derived from two contiguous genes of the cathelicidin family. Biochim Biophys Acta 1398:393–396
Shamova O, Brogden KA, Zhao C, Nguyen T, Kokryakov VN, Lehrer RI (1999) Purification and properties of proline-rich antimicrobial peptides from sheep and goat leukocytes. Infect Immun 67:4106–4111
Huttner KM, Lambeth MR, Burkin HR, Burkin DJ, Broad TE (1998) Localization and genomic organization of sheep antimicrobial peptide genes. Gene 206:85–91
Agerberth B, Lee JY, Bergman T, Carlquist M, Boman HG, Mutt V, Jornvall H (1991) Amino acid sequence of PR-39. Isolation from pig intestine of a new member of the family of proline-arginine-rich antibacterial peptides. Eur J Biochem 202:849–854
Pungercar J, Strukelj B, Kopitar G, Renko M, Lenarcic B, Gubensek F, Turk V (1993) Molecular cloning of a putative homolog of proline/arginine-rich antibacterial peptides from porcine bone marrow. FEBS Lett 336:284–288
Scocchi M, Romeo D, Zanetti M (1994) Molecular cloning of Bac7, a proline- and arginine-rich antimicrobial peptide from bovine neutrophils. FEBS Lett 352:197–200
Cabras T, Longhi R, Secundo F, Nocca G, Conti S, Polonelli L, Fanali C, Inzitari R, Petruzzelli R, Messana I, Castagnola M, Vitali A (2008) Structural and functional characterization of the porcine proline-rich antifungal peptide SP-B isolated from salivary gland granules. J Pept Sci 14:251–260
Bulet P, Hetru C, Dimarcq JL, Hoffmann D (1999) Antimicrobial peptides in insects; structure and function. Dev Comp Immunol 23:329–344
Bulet P, Dimarcq JL, Hetru C, Lagueux M, Charlet M, Hegy G, Van Dorsselaer A, Hoffmann JA (1993) A novel inducible antibacterial peptide of Drosophila carries an O-glycosylated substitution. J Biol Chem 268:14893–14897
Li WF, Ma GX, Zhou XX (2006) Apidaecin-type peptides: biodiversity, structure-function relationships and mode of action. Peptides 27:2350–2359
Casteels P, Romagnolo J, Castle M, Casteels-Josson K, Erdjument-Bromage H, Tempst P (1994) Biodiversity of apidaecin-type peptide antibiotics. Prospects of manipulating the antibacterial spectrum and combating acquired resistance. J Biol Chem 269:26107–26115
Cociancich S, Dupont A, Hegy G, Lanot R, Holder F, Hetru C, Hoffmann JA, Bulet P (1994) Novel inducible antibacterial peptides from a hemipteran insect, the sap-sucking bug Pyrrhocoris apterus. Biochem J 300:567–575
Miura K, Ueno S, Kamiya K, Kobayashi J, Matsuoka H, Ando K, Chinzei Y (1996) Cloning of mRNA sequences for two antibacterial peptides in a hemipteran insect, Riptortus clavatus. Zool Sci 13:111–117
Mackintosh JA, Veal DA, Beattie AJ, Gooley AA (1998) Isolation from an ant Myrmecia gulosa of two inducible O-glycosylated proline-rich antibacterial peptides. J Biol Chem 273:6139–6143
Levashina EA, Ohresser S, Bulet P, Reichhart JM, Hetru C, Hoffmann JA (1995) Metchnikowin, a novel immune-inducible proline-rich peptide from Drosophila with antibacterial and antifungal properties. Eur J Biochem 233:694–700
Hara S, Yamakawa M (1995) A novel antibacterial peptide family isolated from the silkworm, Bombyx mori. Biochem J 310:651–656
Casteels P, Ampe C, Riviere L, Van Damme J, Elicone C, Fleming M, Jacobs F, Tempst P (1990) Isolation and characterization of abaecin, a major antibacterial response peptide in the honeybee (Apis mellifera). Eur J Biochem 187:381–386
Lavine MD, Chen G, Strand MR (2005) Immune challenge differentially affects transcript abundance of three antimicrobial peptides in hemocytes from the moth Pseudoplusia includens. Insect Biochem Mol Biol 35:1335–1346
Liu G, Kang D, Steiner H (2000) Trichoplusia ni lebocin, an inducible immune gene with a downstream insertion element. Biochem Biophys Res Commun 269:803–807
Cuthbertson BJ, Deterding LJ, Williams JG, Tomer KB, Etienne K, Blackshear PJ, Bullesbach EE, Gross PS (2008) Diversity in penaeidin antimicrobial peptide form and function. Dev Comp Immunol 32:167–181
Destoumieux D, Munoz M, Bulet P, Bachère E (2000) Penaeidins, a family of antimicrobial peptides from penaeid shrimp (Crustacea, Decapoda). Cell Mol Life Sci 57:1260–1271
Yang Y, Poncet J, Garnier J, Zatylny C, Bachere E, Aumelas A (2003) Solution structure of the recombinant penaeidin-3, a shrimp antimicrobial peptide. J Biol Chem 278:36859–36867
O’Leary NA, Gross PS (2006) Genomic structure and transcriptional regulation of the penaeidin gene family from Litopenaeus vannamei. Gene 371:75–83
Jiravanichpaisal P, Lee SY, Kim YA, Andren T, Soderhall I (2007) Antibacterial peptides in hemocytes and hematopoietic tissue from freshwater crayfish Pacifastacus leniusculus: characterization and expression pattern. Dev Comp Immunol 31:441–455
Imjongjirak C, Amparyup P, Tassanakajon A (2011) Two novel antimicrobial peptides, arasin-likeSp and GRPSp, from the mud crab Scylla paramamosain, exhibit the activity against some crustacean pathogenic bacteria. Fish Shellfish Immunol 30:706–712
Stensvag K, Haug T, Sperstad SV, Rekdal O, Indrevoll B, Styrvold OB (2008) Arasin 1, a proline-arginine-rich antimicrobial peptide isolated from the spider crab, Hyas araneus. Dev Comp Immunol 32:275–285
Noga EJ, Stone KL, Wood A, Gordon WL, Robinette D (2010) Primary structure and cellular localization of callinectin, an antimicrobial peptide from the blue crab. Dev Comp Immunol [Epub ahead of print]
Shi J, Ross CR, Chengappa MM, Sylte MJ, McVey DS, Blecha F (1996) Antibacterial activity of a synthetic peptide (PR-26) derived from PR-39, a proline-arginine-rich neutrophil antimicrobial peptide. Antimicrob Agents Chemother 40:115–121
Chan YR, Zanetti M, Gennaro R, Gallo RL (2001) Anti-microbial activity and cell binding are controlled by sequence determinants in the anti-microbial peptide PR-39. J Invest Dermatol 116:230–235
Linde CM, Hoffner SE, Refai E, Andersson M (2001) In vitro activity of PR-39, a proline-arginine-rich peptide, against susceptible and multi-drug-resistant Mycobacterium tuberculosis. J Antimicrob Chemother 47:575–580
Freer E, Pizarro-Cerda J, Weintraub A, Bengoechea JA, Moriyon I, Hultenby K, Gorvel JP, Moreno E (1999) The outer membrane of Brucella ovis shows increased permeability to hydrophobic probes and is more susceptible to cationic peptides than are the outer membranes of mutant rough Brucella abortus strains. Infect Immun 67:6181–6186
Scocchi M, Romeo D, Cinco M (1993) Antimicrobial activity of two bactenecins against spirochetes. Infect Immun 61:3081–3083
Benincasa M, Scocchi M, Podda E, Skerlavaj B, Dolzani L, Gennaro R (2004) Antimicrobial activity of Bac7 fragments against drug-resistant clinical isolates. Peptides 25:2055–2061
Anderson RC, Hancock RE, Yu PL (2004) Antimicrobial activity and bacterial-membrane interaction of ovine-derived cathelicidins. Antimicrob Agents Chemother 48:673–676
Cuthbertson BJ, Bullesbach EE, Fievet J, Bachere E, Gross PS (2004) A new class (penaeidin class 4) of antimicrobial peptides from the Atlantic white shrimp (Litopenaeus setiferus) exhibits target specificity and an independent proline-rich-domain function. Biochem J 381:79–86
Gallo RL, Ono M, Povsic T, Page C, Eriksson E, Klagsbrun M, Bernfield M (1994) Syndecans, cell surface heparan sulfate proteoglycans, are induced by a proline-rich antimicrobial peptide from wounds. Proc Natl Acad Sci USA 91:11035–11039
Huang HJ, Ross CR, Blecha F (1997) Chemoattractant properties of PR-39, a neutrophil antibacterial peptide. J Leukoc Biol 61:624–629
Li J, Post M, Volk R, Gao Y, Li M, Metais C, Sato K, Tsai J, Aird W, Rosenberg RD, Hampton TG, Sellke F, Carmeliet P, Simons M (2000) PR39, a peptide regulator of angiogenesis. Nat Med 6:49–55
Ramanathan B, Wu H, Ross CR, Blecha F (2004) PR-39, a porcine antimicrobial peptide, inhibits apoptosis: involvement of caspase-3. Dev Comp Immunol 28:163–169
Madhani M, Barchowsky A, Klei L, Ross CR, Jackson SK, Swartz HM, James PE (2002) Antibacterial peptide PR-39 affects local nitric oxide and preserves tissue oxygenation in the liver during septic shock. Biochim Biophys Acta 1588:232–240
James PE, Madhani M, Ross C, Klei L, Barchowsky A, Swartz HM (2003) Tissue hypoxia during bacterial sepsis is attenuated by PR-39, an antibacterial peptide. Adv Exp Med Biol 530:645–652
Tomasinsig L, Skerlavaj B, Papo N, Giabbai B, Shai Y, Zanetti M (2006) Mechanistic and functional studies of the interaction of a proline-rich antimicrobial peptide with mammalian cells. J Biol Chem 281:383–391
Tomasinsig L, Benincasa M, Scocchi M, Skerlavaj B, Tossi A, Zanetti M, Gennaro R (2010) Role of cathelicidin peptides in bovine host defense and healing. Probiotics Antimicro Prot 2:12–20
Otvos L Jr, Bokonyi K, Varga I, Otvos BI, Hoffmann R, Ertl HC, Wade JD, McManus AM, Craik DJ, Bulet P (2000) Insect peptides with improved protease-resistance protect mice against bacterial infection. Protein Sci 9:742–749
Benincasa M, Pelillo C, Zorzet S, Garrovo C, Biffi S, Gennaro R, Scocchi M (2010) The proline-rich peptide Bac7 (1–35) reduces mortality from Salmonella typhimurium in a mouse model of infection. BMC Microbiol 10:178
Cabiaux V, Agerberth B, Johansson J, Homble F, Goormaghtigh E, Ruysschaert JM (1994) Secondary structure and membrane interaction of PR-39, a Pro + Arg-rich antibacterial peptide. Eur J Biochem 224:1019–1027
Raj PA, Edgerton M (1995) Functional domain and poly-l-proline II conformation for candidacidal activity of bactenecin 5. FEBS Lett 368:526–530
Raj PA, Marcus E, Edgerton M (1996) Delineation of an active fragment and poly(l-proline) II conformation for candidacidal activity of bactenecin 5. Biochemistry 35:4314–4325
Niidome T, Mihara H, Oka M, Hayashi T, Saiki T, Yoshida K, Aoyagi H (1998) Structure and property of model peptides of proline/arginine-rich region in bactenecin 5. J Pept Res 51:337–345
Dutta RC, Nagpal S, Salunke DM (2008) Functional mapping of apidaecin through secondary structure correlation. Int J Biochem Cell Biol 40:1005–1015
Cuthbertson BJ, Yang Y, Bachere E, Bullesbach EE, Gross PS, Aumelas A (2005) Solution structure of synthetic penaeidin-4 with structural and functional comparisons with penaeidin-3. J Biol Chem 280:16009–16018
Tokunaga Y, Niidome T, Hatakeyama T, Aoyagi H (2001) Antibacterial activity of bactenecin 5 fragments and their interaction with phospholipid membranes. J Pept Sci 7:297–304
Gobbo M, Benincasa M, Bertoloni G, Biondi B, Dosselli R, Papini E, Reddi E, Rocchi R, Tavano R, Gennaro R (2009) Substitution of the arginine/leucine residues in apidaecin Ib with peptoid residues: effect on antimicrobial activity, cellular uptake, and proteolytic degradation. J Med Chem 52:5197–5206
Otvos L Jr (2000) Antibacterial peptides isolated from insects. J Pept Sci 6:497–511
Wade D, Boman A, Wahlin B, Drain CM, Andreu D, Boman HG, Merrifield RB (1990) All-D amino acid-containing channel-forming antibiotic peptides. Proc Natl Acad Sci USA 87:4761–4765
Bessalle R, Kapitkovsky A, Gorea A, Shalit I, Fridkin M (1990) All-D-magainin: chirality, antimicrobial activity and proteolytic resistance. FEBS Lett 274:151–155
Benincasa M, Pacor S, Gennaro R, Scocchi M (2009) Rapid and reliable detection of antimicrobial peptide penetration into gram-negative bacteria based on fluorescence quenching. Antimicrob Agents Chemother 53:3501–3504
Mattiuzzo M, Bandiera A, Gennaro R, Benincasa M, Pacor S, Antcheva N, Scocchi M (2007) Role of the Escherichia coli SbmA in the antimicrobial activity of proline-rich peptides. Mol Microbiol 66:151–163
Otvos L, Jr., O I, Rogers ME, Consolvo PJ, Condie BA, Lovas S, Bulet P, Blaszczyk-Thurin M (2000) Interaction between heat shock proteins and antimicrobial peptides. Biochemistry 39:14150–14159
Mayer MP, Bukau B (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol Life Sci 62:670–684
Tomoyasu T, Mogk A, Langen H, Goloubinoff P, Bukau B (2001) Genetic dissection of the roles of chaperones and proteases in protein folding and degradation in the Escherichia coli cytosol. Mol Microbiol 40:397–413
Kragol G, Lovas S, Varadi G, Condie BA, Hoffmann R, Otvos L Jr (2001) The antibacterial peptide pyrrhocoricin inhibits the ATPase actions of DnaK and prevents chaperone-assisted protein folding. Biochemistry 40:3016–3026
Chesnokova LS, Slepenkov SV, Witt SN (2004) The insect antimicrobial peptide, l-pyrrhocoricin, binds to and stimulates the ATPase activity of both wild-type and lidless DnaK. FEBS Lett 565:65–69
Liebscher M, Roujeinikova A (2009) Allosteric coupling between the lid and interdomain linker in DnaK revealed by inhibitor binding studies. J Bacteriol 191:1456–1462
Scocchi M, Lüthy C, Decarli P, Mignogna G, Christen P, Gennaro R (2009) The Proline-rich antibacterial peptide Bac7 binds to and inhibits in vitro the molecular chaperone DnaK. Int J Pept Res Therapeut 15:147–155
Scocchi M, Mattiuzzo M, Benincasa M, Antcheva N, Tossi A, Gennaro R (2008) Investigating the mode of action of proline-rich antimicrobial peptides using a genetic approach: a tool to identify new bacterial targets amenable to the design of novel antibiotics. Methods Mol Biol 494:161–176
Pranting M, Negrea A, Rhen M, Andersson DI (2008) Mechanism and fitness costs of PR-39 resistance in Salmonella enterica serovar Typhimurium LT2. Antimicrob Agents Chemother 52:2734–2741
Salomon RA, Farias RN (1995) The peptide antibiotic microcin 25 is imported through the TonB pathway and the SbmA protein. J Bacteriol 177:3323–3325
LeVier K, Phillips RW, Grippe VK, Roop RM 2nd, Walker GC (2000) Similar requirements of a plant symbiont and a mammalian pathogen for prolonged intracellular survival. Science 287:2492–2493
Yorgey P, Lee J, Kordel J, Vivas E, Warner P, Jebaratnam D, Kolter R (1994) Posttranslational modifications in microcin B17 define an additional class of DNA gyrase inhibitor. Proc Natl Acad Sci USA 91:4519–4523
Kragol G, Hoffmann R, Chattergoon MA, Lovas S, Cudic M, Bulet P, Condie BA, Rosengren KJ, Montaner LJ, Otvos L Jr (2002) Identification of crucial residues for the antibacterial activity of the proline-rich peptide, pyrrhocoricin. Eur J Biochem 269:4226–4237
Otvos L Jr, Wade JD, Lin F, Condie BA, Hanrieder J, Hoffmann R (2005) Designer antibacterial peptides kill fluoroquinolone-resistant clinical isolates. J Med Chem 48:5349–5359
Cassone M, Vogiatzi P, La Montagna R, De Olivier Inacio V, Cudic P, Wade JD, Otvos L Jr (2008) Scope and limitations of the designer proline-rich antibacterial peptide dimer, A3-APO, alone or in synergy with conventional antibiotics. Peptides 29:1878–1886
Noto PB, Abbadessa G, Cassone M, Mateo GD, Agelan A, Wade JD, Szabo D, Kocsis B, Nagy K, Rozgonyi F, Otvos L Jr (2008) Alternative stabilities of a proline-rich antibacterial peptide in vitro and in vivo. Protein Sci 17:1249–1255
Szabo D, Ostorhazi E, Binas A, Rozgonyi F, Kocsis B, Cassone M, Wade JD, Nolte O, Otvos L Jr (2010) The designer proline-rich antibacterial peptide A3-APO is effective against systemic Escherichia coli infections in different mouse models. Int J Antimicrob Agents 35:357–361
Rozgonyi F, Szabo D, Kocsis B, Ostorhazi E, Abbadessa G, Cassone M, Wade JD, Otvos L Jr (2009) The antibacterial effect of a proline-rich antibacterial peptide A3-APO. Curr Med Chem 16:3996–4002
Schneider M, Dorn A (2001) Differential infectivity of two Pseudomonas species and the immune response in the milkweed bug, Oncopeltus fasciatus (Insecta: Hemiptera). J Invertebr Pathol 78:135–140
Knappe D, Piantavigna S, Hansen A, Mechler A, Binas A, Nolte O, Martin LL, Hoffmann R (2010) Oncocin (VDKPPYLPRPRPPRRIYNR-NH2): a novel antibacterial peptide optimized against gram-negative human pathogens. J Med Chem 53:5240–5247
Ghiselli R, Giacometti A, Cirioni O, Circo R, Mocchegiani F, Skerlavaj B, D’Amato G, Scalise G, Zanetti M, Saba V (2003) Neutralization of endotoxin in vitro and in vivo by Bac7(1–35), a proline-rich antibacterial peptide. Shock 19:577–581
Lee PH, Ohtake T, Zaiou M, Murakami M, Rudisill JA, Lin KH, Gallo RL (2005) Expression of an additional cathelicidin antimicrobial peptide protects against bacterial skin infection. Proc Natl Acad Sci USA 102:3750–3755
Sadler K, Eom KD, Yang JL, Dimitrova Y, Tam JP (2002) Translocating proline-rich peptides from the antimicrobial peptide bactenecin 7. Biochemistry 41:14150–14157
Dmitriev RI, Ropiak HM, Yashunsky DV, Ponomarev GV, Zhdanov AV, Papkovsky DB (2010) Bactenecin 7 peptide fragment as a tool for intracellular delivery of a phosphorescent oxygen sensor. FEBS J 277:4651–4661
Otvos L Jr, Cudic M, Chua BY, Deliyannis G, Jackson DC (2004) An insect antibacterial peptide-based drug delivery system. Mol Pharm 1:220–232
Viljakainen L, Evans JD, Hasselmann M, Rueppell O, Tingek S, Pamilo P (2009) Rapid evolution of immune proteins in social insects. Mol Biol Evol 26:1791–1801
Chernysh S, Cociancich S, Briand JP, Hetru C, Bulet P (1996) The inducible antibacterial peptides of the hemipteran insect Palomena prasina: identification of a unique family of proline-rich peptides and of a novel insect defensin. J Insect Physiol 42:81–89
Cheng X, Liu G, Ye G, Wang H, Shen X, Wu K, Xie J, Altosaar I (2009) Screening and cloning of antimicrobial DNA sequences using a vital staining method. Gene 430:132–139
Gueguen Y, Garnier J, Robert L, Lefranc MP, Mougenot I, de Lorgeril J, Janech M, Gross PS, Warr GW, Cuthbertson B, Barracco MA, Bulet P, Aumelas A, Yang Y, Bo D, Xiang J, Tassanakajon A, Piquemal D, Bachere E (2006) PenBase, the shrimp antimicrobial peptide penaeidin database: sequence-based classification and recommended nomenclature. Dev Comp Immunol 30:283–288
Acknowledgments
This study was supported by grants from the Italian Ministry for University and Research (PRIN 2008), from the Regione Friuli Venezia Giulia grant under the LR 26/2005, art. 23 for the R3A2 network, and the Marie Curie project PIAP-GA-2008-218191.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Scocchi, M., Tossi, A. & Gennaro, R. Proline-rich antimicrobial peptides: converging to a non-lytic mechanism of action. Cell. Mol. Life Sci. 68, 2317–2330 (2011). https://doi.org/10.1007/s00018-011-0721-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00018-011-0721-7