Peptidomic comparison and characterization of the major components of the venom of the giant ant Dinoponera quadriceps collected in four different areas of Brazil.
Cologna, Camila Takeno; Cardoso, Jaqueline Dos Santos; Jourdan, Emmanuelet al.
Ant; Antimicrobial peptides; De novo sequencing; Dinoponera quadriceps; Mass spectrometry; Venom
Abstract :
[en] Despite the noxious effects inflicted by Dinoponera ant's envenomation, the information about the biological properties and composition of their venom is still very limited. Ants from the genus Dinoponera are believed to be the world's largest living ants with a body length of 3cm. Their occurrence is restricted to tropical areas of South America. In this work, we study the venom of the giant Dinoponera quadriceps ant collected in 4 different regions of Brazil. By using a combination of complementary mass spectrometric approaches, we aim at: (i) characterizing the venom composition of these ants; (ii) establishing a comparative analysis of the venom from four geographically different regions in Brazil. This approach demonstrates that ant venom is a copious source of new compounds. Several peptides were identified and selected for "de novo sequencing". Since most of the new peptides showed similarities with antimicrobial peptides (AMPs), antimicrobial assays were performed with the purpose of evaluating their activity. In regard to the comparative study of the four regions, we observed not only major differences in the venom compositions, but also that the venoms collected in closest areas are more similar than the ones collected in distant regions. These observations seem to highlight an adaption of the ant venoms to the local environment. Concerning the biological assays, the peptides called Dq-3162 and Da-3177 showed a wide-ranging antimicrobial activity. The characterization of new AMPs with a broad spectrum of activity and different scaffolds may aid scientists to design new therapeutic agents and understand the mechanisms of those peptides to interact with microbial membranes. The results obtained betoken the biotechnological potential of ant's venom. BIOLOGICAL SIGNIFICANCE: For the first time this manuscript describes an extensive proteomics characterization of the D. quadriceps venom. In addition this study reports the variation in venom composition of primitive ants from 4 geographically different areas of Brazil. The results reveal the presence of ~335 compounds for each venom/area and inter-colony variations were observed. 16 new peptides were characterized and 2 of them were synthesized and biologically assayed. These findings highlight the considerable and still unexplored diversity of ant's venom which could be used as valuable research tools in different areas of knowledge.
Disciplines :
Chemistry
Author, co-author :
Cologna, Camila Takeno
Cardoso, Jaqueline Dos Santos
Jourdan, Emmanuel
Degueldre, Michel ; Université de Liège - ULiège > Département de chimie (sciences) > GIGA-R : Laboratoire de spectrométrie de masse (L.S.M.)
Upert, Gregory
Gilles, Nicolas
Uetanabaro, Ana Paula Trovatti
Costa Neto, Eraldo Medeiro
Thonart, Philippe ; Université de Liège - ULiège > Département des sciences de la vie > Biochimie et microbiologie industrielles
De Pauw, Edwin ; Université de Liège - ULiège > Département de chimie (sciences) > GIGA-R : Laboratoire de spectrométrie de masse (L.S.M.)
Quinton, Loïc ; Université de Liège - ULiège > Département de chimie (sciences) > Chimie biologique
Language :
English
Title :
Peptidomic comparison and characterization of the major components of the venom of the giant ant Dinoponera quadriceps collected in four different areas of Brazil.
Pluzhnikov K., Nosyreva E., Shevchenko L., Kokoz Y., Schmalz D., Hucho F., et al. Analysis of ectatomin action on cell membranes. Eur J Biochem 1999, 262:501-506.
Duval A., Malécot C.O., Pelhate M., Piek T. Poneratoxin, a new toxin form an ant venom, reveals an interconversion between two gating modes of the Na+ channels in frog skeletal muscle fibres. Pflugers Archiv 1992, 420:239-247.
Orivel J., Redeker V., Le Caer J.P., Krier F., Revol-Junelles A.M., Longeon A., et al. Ponericins, new antibacterial and insecticidal peptides from the venom of the ant Pachycondyla goeldii. J Biol Chem 2001, 276:17823-17829.
Pereira H.A. Novel therapies based on cationic antimicrobial peptides. Curr Pharm Biotechnol 2006, 7:229-234.
Haddad Junior V., Cardoso J.L., Moraes R.H. Description of an injury caused by a false tocandira (Dinoponera gigantean) with a revision on folkloric, pharmacological and clinical aspects of the giant ants of the genera Paraponera and Dinoponera (subfamily Ponerinae). Rev Inst Med Trop Sao Paulo 2005, 47:235-238.
Sousa P.L., Quinet Y., Ponte E.L., Vale J.F., Torres A.F., Pereira M.G., et al. Venom's antinociceptive property in the primitive ant Dinoponera quadriceps. J Ethnopharmacol Oct 31 2012, 144(1):213-216.
Costa Neto E. Entomotherapy, or the medicinal use of insects. J Etnobiol 2005, 25(1):93-114.
Johnson S.R., Copello J.A., Steven M.E., Suarez A.V. A biochemical characterization of the major peptides from the venom of the giant neotropical hunting ant Dinoponera australis. Toxicon 2010, 55:702-710.
Favreau P., Menin L., Michalet S., Perret F., Cheneval O., Stöcklin M., et al. Mass spectrometry strategies for venom mapping and peptide sequencing from crude venoms: case applications with single arthropod specimen. Toxicon 2006, 47:676-687.
Pimenta A., Lima M.E. Small peptides, big world: biotechnological potential in neglected bioactive peptides from arthropods venoms. J Pept Sci 2005, 11:670-676.
Orts D.J.B., Peigneur S., Madio B., Cassoli J.S., Montandon G.G., Pimenta A.M.C., et al. Biochemical and electrophysiological characterization of two sea anemone type 1 potassium toxins from a geographically distant population of Bunodosoma caissarum. Mar Drugs 2013, 11:655-679.
Romeo C., Di F.L., Oliverio M., Palazzo P., Massilia G.R., Ascenzi P., et al. Conusventricosus venom peptides profiling by HPLC-MS: a new insight in the intraspecific variation. J Sep Sci 2008, 31:488-498.
Newton K.A., Clench M.R., Deshmukh R., Jeyaseelan K., Strong P.N. Mass fingerprinting of toxic fractions from the venom of the Indian red scorpion, Mesobuthustamulus: biotope-specific variation in the expression of venom peptides. Rapid Commun Mass Spectrom 2007, 21:3467-3476.
Abdel-Rahman M.A., Omran M.A., Abdel-Nabi I.M., Ueda H., McVean A. Intraspecific variation in the Egyptian scorpion Scorpio mauruspalmatus venom collected from different biotopes. Toxicon 2009, 53(3):349-359.
Palagi A., Koh J.M.S., Leblanc M., Wilson D., Dutertre S., King G.K., et al. Unravelling the complex venom landscapes of lethal Australian funnel-web spiders (Hexathelidae: Atracinae) using LC-MALDI-TOF mass spectrometry. J Proteomics 2013, 80:292-310.
Uçkan F., Ergin E., Rivers D.B., Gençer N. Age and diet influence the composition of venom from the endoparasitic wasp Pimplaturionellae L. (Hymenoptera: Ichneumonidae). Arch Insect Biochem Physiol 2006, 63:177-187.
Ferreira Junior R.S., Sciani J.M., Marques-Porto R., Lourenço A., Orsi R.O., Barravieira B., et al. Africanized honey bee (Apismellifera) venom profiling: seasonal variation of melittin and phospholipase A2 levels. Toxicon 2010, 56(3):355-362.
Harrison R.A., Cook D.A. renjifo C, Caseweel NR, Currier RB, Wagstaff SC. Research strategies to improve snakebite treatment: challenges and progress. J Proteomics 2011, 74:1768-1780.
Casewell N.R., Wüster W., Vonk F.J., Harrison R.A., Fry B.G. Complex cocktails: the evolutionary novelty of venoms. Cell Press 2013, 28(4):219-229.
Daltry J.C., Wüster W., Thorpe R.S. Diet and snake venom evolution. Nature 1996, 379:537-540.
Sasa M. Diet and snake venom evolution: can local selection alone explain intraspecific venom variation?. Toxicon 1999, 37:249-252.
Creer S., Malhotra A., Thorpe R.S., Stocklin R., Favreau P., Chou W.H. Genetic and ecological correlates of intraspecific variation in pitviper venom composition detected using matrix-assisted laser desorption time-of-flight mass spectrometry (MALDI-TOF-MS) and isoelectric focusing. J Mol Evol 2003, 56:317-329.
Araujo A., Rodrigues S. Foraging behavior of the queenlessant Dinoponera quadriceps Santschi (Hymenoptera: Formicidae). Neotrop Entomol 2006, 35(2):159-164.
Simmaco M., Mignogna G., Canofeni S., Miele R., Mangoni M.L., Barra D. Temporins, antimicrobial peptides from the European red frog Ranatemporaria. Eur J Biochem 1996, 242(3):788-792.
Yang X., Xia J., Yu Z., Hu Y., Li F., Meng H., et al. Characterization of diverse antimicrobial peptides in skin secretion of Chungan torrent frog Amolopschunganensis. Peptides 2012, 38(1):41-53.
Conlon J.M., Mechkarska M., Ahmed E., Coquet L., Jouenne T., Leprince J., et al. Host defense peptides in skin secretions of the Oregon spotted frog Ranapretiosa: implications for species resistance to chytridiomycosis. Dev Comp Immunol 2011, 35(6):644-649.
Abbassi F., Oury B., Blasco T., Sereno D., Bolbach G., Nicolas P., et al. Isolation, characterization and molecular cloning of new temporins from the skin of the North African ranid Pelophylax saharica. Peptides 2008, 29(9):1526-1533.
Avitabile C., Netti F., Orefice O., Palmieri M., Nocerino N., Malgieri G., et al. Design, structural and functional characterization of a Temporin 1-b analog active against Gram negative bacteria. Biochim Biophys Acta 2013, 1830(6):3767-3775.
Nicolas P., Amri C.E. The dermaseptin superfamily: a gene-based combinatorial library of antimicrobial peptides. Biochim Biophys Acta 2009, 1788:1537-1550.
Wechselberger C. Cloning of cDNAsenconding new peptides of the demaseptin-family. Biochim Biophys Acta 1998, 1388(1):279-283.
Conlon J.M., Demandt A., Nielsen P.F., Leprince J., Vaudry H., Woodhams D.C. The alyteserins: two families of antimicrobial peptides from the skin secretions of the midwife toad Alytes obstericans (Alystidae). Peptides 2009, 30(6):1069-1073.
Amri E.C., Lacombe C., Zimmerman K., Ladram A., Amiche M., Nicolas P., et al. The plasticins: membrane adsorption, lipid disorders, and biological activity. Biochemistry 2006, 45(48):14285-14297.
Leite J.R., Silva L.P., Rodrigues M.I., Prates M.V., Brand G.D., Lacava B.M., et al. Phylloseptins: a novel class of anti-bacterial and anti-protozoan peptides form the Phyllomedusa genus. Peptides 2005, 26(4):565-573.
Winley W.C. Describing the mechanism of antimicrobial peptide action with the interfacial activity model. ACS Chem Biol 2010, 5(10):905-917.
Kuhn-Netnwig L. Antimicrobial and cytolytic peptides of venomous arthropods. Cell Mol Life Sci 2003, 60:2651-2668.
Santos-Pinto J.R.A., Fox E.G.P., Saidemberg D.M., Santos L.D., Menegasso A.R.S., Costa-Manso E., et al. Proteomic view of the venom from the fire ant Solenopsis invicta Buren. J Proteome Res 2012, 11(9):4643-4653.
Mihajlovic M., Lazaridis T. Charge distribution and imperfect amphipathicity affect the pore formation by antimicrobial peptides. Biochim Biophys Acta 1818, 2012:1274-1283.
