De Novo sequencing and transcriptome analysis for tetramorium bicarinatum: A comprehensive venom gland transcriptome analysis from an ant species

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Bouzid, Wafa ^a   Verdenaud, Marion ^b   Klopp, Christophe ^c   Ducancel, Frédéric ^b   Noirot, Céline ^c   Vétillard, Angélique ^a  

^a UNIVERSITÉ DE TOULOUSE   (France)

^b DIF   (France)

^c CEMAGREF   (France)

Author keywords

Ant; de novo assembly; Hymenopteran allergens; Illumina technology; New generation sequencing; Social hymenoptera; Tetramorium bicarinatum; Venom glands; Venom toxins

Indexed keywords

AGATOXIN; ANT VENOM; CONTIG; HYALURONIDASE; PHOSPHOLIPASE A1; PHOSPHOLIPASE A2; PROTEINASE INHIBITOR; SECAPIN; SERINE PROTEINASE; SNAKE VENOM; TRANSCRIPTOME; UNCLASSIFIED DRUG; WAPRIN; ALLERGEN; INSECT PROTEIN;

ANT; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE SEQUENCE; NONHUMAN; OPEN READING FRAME; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN SECRETION; TETRAMORIUM BICARINATUM; TRANSCRIPTOMICS; AMINO ACID SEQUENCE; ANIMAL; ANTIBODY SPECIFICITY; BIOLOGY; CHEMISTRY; GENETICS; HIGH THROUGHPUT SEQUENCING; METABOLISM; MOLECULAR GENETICS; PHYLOGENY; SEQUENCE ALIGNMENT;

ANIMALIA; ARANEAE; ARTHROPODA; FORMICIDAE; HYMENOPTERA; SERPENTES; TETRAMORIUM BICARINATUM;

ALLERGENS; AMINO ACID SEQUENCE; ANIMALS; ANT VENOMS; ANTS; COMPUTATIONAL BIOLOGY; GENE EXPRESSION PROFILING; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; INSECT PROTEINS; MOLECULAR SEQUENCE ANNOTATION; MOLECULAR SEQUENCE DATA; ORGAN SPECIFICITY; PHYLOGENY; SEQUENCE ALIGNMENT; TRANSCRIPTOME;

EID: 84924289802     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-987     Document Type: Article

References (72)

1. Fernandes-Pedrosa MF, JF-S: An Integrated View of the Molecular Recognition and Toxinology - From Analytical Procedures to Biomedical Applications. Edited by: Gandhi Rádis B. InTech; 544. Chapters published July 01, 2013 under CC BY 3.0 license doi:10.5772/3429. ISBN 978-953-51-1151-1.
2. Palma MS: Insect Venom Peptides. In Handb Biol Act Pept. San Diego: Kastin, A. Academic Press; 2006:409-417.
3. Palma MS, Brochetto-Braga MR: Biochemical variability between venoms from different honey-bee ( Apis mellifera ) races. Comp Biochem Physiol Part C Pharmacol Toxicol Endocrinol 1993, 106:423-427. 10.1016/0742-8413(93)90157-G
4. Schumacher MJ, Schmidt JO, Egen NB, Dillon KA: Biochemical variability of venoms from individual European and Africanized honeybees ( Apis mellifera ). J Allergy Clin Immunol 1992, 90:59-65. 10.1016/S0091-6749(06)80011-4
5. de Lima PR, Brochetto-Braga MR: Hymenoptera venom review focusing on Apis mellifera . J Venom Anim Toxins Incl Trop Dis 2003, 9:149-162.
6. De Graaf DC, Aerts M, Brunain M, Desjardins CA, Jacobs FJ, Werren JH, Devreese B: Insights into the venom composition of the ectoparasitoid wasp Nasonia vitripennis from bioinformatic and proteomic studies. Insect Mol Biol 2010,19(Suppl 1):11-26.
7. Hoffman DR: Ant venoms. Curr Opin Allergy Clin Immunol 2010, 10:342-346. 10.1097/ACI.0b013e328339f325
8. Torres AFC, Huang C, Chong C-M, Leung SW, Prieto-da-Silva ARB, Havt A, Quinet YP, Martins AMC, Lee SMY, Rádis-Baptista G: Transcriptome analysis in venom gland of the predatory giant ant Dinoponera quadriceps: insights into the polypeptide toxin arsenal of hymenopterans. PLoS One 2014, 9:e87556. 10.1371/journal.pone.0087556
9. Warrell DA, Gutiérrez JM, Calvete JJ, Williams D: New approaches & technologies of venomics to meet the challenge of human envenoming by snakebites in India. Indian J Med Res 2013, 138:38-59.
10. Ménez A, Stöcklin R, Mebs D: "Venomics" or: the venomous systems genome project. Toxicon 2006, 47:255-259. 10.1016/j.toxicon.2005.12.010
11. Gruber CW, Muttenthaler M: Discovery of defense- and neuropeptides in social ants by genome-mining. PLoS One 2012, 7:e32559. 10.1371/journal.pone.0032559
12. Von Sicard NA, Candy DJ, Anderson M: The biochemical composition of venom from the pavement ant ( Tetramorium caespitum L.). Toxicon 1989, 27:1127-1133. 10.1016/0041-0101(89)90006-8
13. Bouzid W, Klopp C, Verdenaud M, Ducancel F, Vétillard A: Profiling the venom gland transcriptome of Tetramorium bicarinatum (hymenoptera: formicidae): the first transcriptome analysis of an ant species. Toxicon 2013, 70:70-81.
14. Duan J, Xia C, Zhao G, Jia J, Kong X: Optimizing de novo common wheat transcriptome assembly using short-read RNA-Seq data. BMC Genomics 2012, 13:392. 10.1186/1471-2164-13-392
15. Anders S, Huber W: Differential Expression of RNA-Seq Data at the Gene Level-the DESeq Package. http://www.bioconductor.org/packages/release/bioc/vignettes/DESeq/inst/doc/DESeq.pdf
16. Fernandes-Pedrosa Mde F, Junqueira-de-Azevedo Ide L, Gonçalves-de-Andrade RM, Kobashi LS, Almeida DD, Ho PL, Tambourgi DV: Transcriptome analysis of Loxosceles laeta (Araneae, Sicariidae) spider venomous gland using expressed sequence tags. BMC Genomics 2008, 9:279. 10.1186/1471-2164-9-279
17. Hoffman DR: Hymenoptera venom allergens. Clin Rev Allergy Immunol 2006, 30:109-128. 10.1385/CRIAI:30:2:109
18. Padavattan S, Schmidt M, Hoffman DR, Marković-Housley Z: Crystal structure of the major allergen from fire ant venom, Sol i 3. J Mol Biol 2008, 383:178-185. 10.1016/j.jmb.2008.08.023
19. Zhu J, Ye G, Hu C: Molecular cloning and characterization of acid phosphatase in venom of the endoparasitoid wasp Pteromalus puparum (Hymenoptera: Pteromalidae). Toxicon 2008, 51:1391-1399. 10.1016/j.toxicon.2008.03.008
20. Grunwald T, Bockisch B, Spillner E, Ring J, Bredehorst R, Ollert MW: Molecular cloning and expression in insect cells of honeybee venom allergen acid phosphatase (Api m 3). J Allergy Clin Immunol 2006, 117:848-854. 10.1016/j.jaci.2005.12.1331
21. Rifflet A, Gavalda S, Téné N, Orivel J, Leprince J, Guilhaudis L, Génin E, Vétillard A, Treilhou M: Identification and characterization of a novel antimicrobial peptide from the venom of the ant Tetramorium bicarinatum . Peptides 2012, 38:363-370. 10.1016/j.peptides.2012.08.018
22. Rifflet A: Study of Exotic Ants Venoms: Identification and Characterization of an Antimicrobial Peptide. Montpellier 1; 2012.
23. Inagaki H, Akagi M, Imai HT, Taylor RW, Wiese MD, Davies NW, Kubo T: Pilosulin 5, a novel histamine-releasing peptide of the Australian ant, Myrmecia pilosula (Jack Jumper Ant). Arch Biochem Biophys 2008, 477:411-416. 10.1016/j.abb.2008.05.014
24. Vanhoye D, Bruston F, Nicolas P, Amiche M: Antimicrobial peptides from hylid and ranin frogs originated from a 150-million-year-old ancestral precursor with a conserved signal peptide but a hypermutable antimicrobial domain. Eur J Biochem 2003, 270:2068-2081. 10.1046/j.1432-1033.2003.03584.x
25. Gilly WF, Richmond TA, Duda TF, Elliger C, Lebaric Z, Schulz J, Bingham JP, Sweedler JV: A diverse family of novel peptide toxins from an unusual cone snail, Conus californicus. J Exp Biol 2011,214(Pt 1):147-161.
26. Kreil G, Haiml L, Suchanek G: Stepwise cleavage of the pro part of promelittin by dipeptidylpeptidase IV. Evidence for a new type of precursor-product conversion. Eur J Biochem 1980, 111:49-58.
27. Hoffman DR: Allergens in hymenoptera venom XXIV: the amino acid sequences of imported fire ant venom allergens Sol i II, Sol i III, and Sol i IV. J Allergy Clin Immunol 1993,91(1 Pt 1):71-78.
28. Borer AS, Wassmann P, Schmidt M, Hoffman DR, Zhou J-J, Wright C, Schirmer T, Marković-Housley Z: Crystal structure of Sol I 2: a major allergen from fire ant venom. J Mol Biol 2012, 415:635-648. 10.1016/j.jmb.2011.10.009
29. Dos Santos Pinto JRA, Fox EGP, Saidemberg DM, Santos LD, da Silva Menegasso AR, Costa-Manso E, Machado EA, Bueno OC, Palma MS: Proteomic view of the venom from the fire ant Solenopsis invicta Buren. J Proteome Res 2012, 11:4643-4653. 10.1021/pr300451g
30. Lomonte B, Angulo Y, Rufini S, Cho W, Giglio JR, Ohno M, Daniele JJ, Geoghegan P, Gutiérrez JM: Comparative study of the cytolytic activity of myotoxic phospholipases A2 on mouse endothelial (tEnd) and skeletal muscle (C2C12) cells in vitro. Toxicon 1999, 37:145-158. 10.1016/S0041-0101(98)00171-8
31. White SP, Scott DL, Otwinowski Z, Gelb MH, Sigler PB: Crystal structure of cobra-venom phospholipase A2 in a complex with a transition-state analogue. Science 1990, 250:1560-1563. 10.1126/science.2274787
32. Balsinde J: Roles of various phospholipases A2 in providing lysophospholipid acceptors for fatty acid phospholipid incorporation and remodelling. Biochem J 2002,364(Pt 3):695-702.
33. Valentin E, Lambeau G: What can venom phospholipases A(2) tell us about the functional diversity of mammalian secreted phospholipases A(2)? Biochimie 2000, 82:815-831. 10.1016/S0300-9084(00)01168-8
34. Dos Santos LD, Santos KS, Pinto JRA, Dias NB, de Souza BM, dos Santos MF, Perales J, Domont GB, Castro FM, Kalil JE, Palma MS: Profiling the proteome of the venom from the social wasp Polybia paulista: a clue to understand the envenoming mechanism. J Proteome Res 2010, 9:3867-3877. 10.1021/pr1000829
35. King TP, Spangfort MD: Structure and biology of stinging insect venom allergens. Int Arch Allergy Immunol 2000, 123:99-106. 10.1159/000024440
36. Zalat S, Schmidt J, Moawad TI: Lipase and phospholipase activities of Hymenoptera venoms (wasps and ants). Egypt J Biol 2005, 5:138-147.
37. Schmidt JO, Blum MS: A harvester ant venom: chemistry and pharmacology. Science 1978, 200:1064-1066. 10.1126/science.653354
38. Hoffman DR, Sakell RH, Schmidt M: Sol i 1, the phospholipase allergen of imported fire ant venom. J Allergy Clin Immunol 2005, 115:611-616. 10.1016/j.jaci.2004.11.020
39. Soldatova L, Kochoumian L, King TP: Sequence similarity of a hornet ( D. maculata ) venom allergen phospholipase A1 with mammalian lipases. FEBS Lett 1993, 320:145-149. 10.1016/0014-5793(93)80080-E
40. Pringos E, Vignes M, Martinez J, Rolland V: Peptide neurotoxins that affect voltage-gated calcium channels: a close-up on ω-agatoxins. Toxins (Basel) 2011, 3:17-42. 10.3390/toxins3010017
41. Araya C, Lomonte B: Antitumor effects of cationic synthetic peptides derived from Lys49 phospholipase A2 homologues of snake venoms. Cell Biol Int 2007, 31:263-268. 10.1016/j.cellbi.2006.11.007
42. Almunia C, Bretaudeau M, Held G, Babon A, Marchetti C, Castelli FA, Ménez A, Maillere B, Gillet D: Bee venom phospholipase A2, a good "chauffeur" for delivering tumor antigen to the MHC I and MHC II peptide-loading compartments of the dendritic cells: the case of NY-ESO-1. PLoS One 2013, 8:e67645. 10.1371/journal.pone.0067645
43. Justo Jacomini DL, Campos Pereira FD, Aparecido dos Santos Pinto JR, dos Santos LD, da Silva Neto AJ, Giratto DT, Palma MS, de Lima Zollner R, Brochetto Braga MR: Hyaluronidase from the venom of the social wasp Polybia paulista (Hymenoptera, Vespidae): cloning, structural modeling, purification, and immunological analysis. Toxicon 2013, 64:70-80.
44. Jin C, Focke M, Léonard R, Jarisch R, Altmann F, Hemmer W: Reassessing the role of hyaluronidase in yellow jacket venom allergy. J Allergy Clin Immunol 2010, 125:184-190. e1 10.1016/j.jaci.2009.08.037
45. Kemparaju K, Girish KS: Snake venom hyaluronidase: a therapeutic target. Cell Biochem Funct 2006, 24:7-12. 10.1002/cbf.1261
46. Hink WF, Pappas PW, Jaworski DC: Partial biochemical characterization of venom from the ant, Pseudomyrmex triplarinus . Toxicon 1994, 32:763-772. 10.1016/0041-0101(94)90002-7
47. Choo YM, Lee KS, Yoon HJ, Kim BY, Sohn MR, Roh JY, Je YH, Kim NJ, Kim I, Woo SD, Sohn HD, Jin BR: Dual function of a bee venom serine protease: prophenoloxidase-activating factor in arthropods and fibrin (ogen) olytic enzyme in mammals. PLoS One 2010, 5:e10393. 10.1371/journal.pone.0010393
48. Hoffman DR, Jacobson RS: Allergens in hymenoptera venom. XXVII: bumblebee venom allergy and allergens. J Allergy Clin Immunol 1996, 97:812-821. 10.1016/S0091-6749(96)80159-X
49. Lima PRM DE, Brochetto-Braga MR, Chaud-netto J: Proteolytic activity of africanized honeybee ( Apis mellifera: hymenoptera, apidae) venom. J Venom Anim Toxins 2000, 6:64-76.
50. Falquet L, Pagni M, Bucher P, Hulo N, Sigrist CJA, Hofmann K, Bairoch A: The PROSITE database, its status in 2002. Nucleic Acids Res 2002, 30:235-238. 10.1093/nar/30.1.235
51. Ali MF, Lips KR, Knoop FC, Fritzsch B, Miller C, Conlon JM: Antimicrobial peptides and protease inhibitors in the skin secretions of the crawfish frog, Rana areolata . Biochim Biophys Acta 2002, 1601:55-63. 10.1016/S1570-9639(02)00432-6
52. Hagiwara K, Kikuchi T, Endo Y, Huqun , Usui K, Takahashi M, Shibata N, Kusakabe T, Xin H, Hoshi S, Miki M, Inooka N, Tokue Y, Nukiwa T: Mouse SWAM1 and SWAM2 are antibacterial proteins composed of a single whey acidic protein motif. J Immunol 2003, 170:1973-1979. 10.4049/jimmunol.170.4.1973
53. Wiedow O, Schröder JM, Gregory H, Young JA, Christophers E: Elafin: an elastase-specific inhibitor of human skin. Purification, characterization, and complete amino acid sequence. J Biol Chem 1990, 265:14791-14795.
54. St Pierre L, Earl ST, Filippovich I, Sorokina N, Masci PP, De Jersey J, Lavin MF: Common evolution of waprin and kunitz-like toxin families in Australian venomous snakes. Cell Mol Life Sci 2008, 65:4039-4054. 10.1007/s00018-008-8573-5
55. Nair DG, Fry BG, Alewood P, Kumar PP, Kini RM: Antimicrobial activity of omwaprin, a new member of the waprin family of snake venom proteins. Biochem J 2007, 402:93-104. 10.1042/BJ20060318
56. Liu D, Wang Y, Wei L, Ye H, Liu H, Wang L, Liu R, Li D, Lai R: Snake venom-like waprin from the frog of Ceratophrys calcarata contains antimicrobial function. Gene 2013, 514:99-104. 10.1016/j.gene.2012.11.007
57. Orivel J, Redeker V, Le Caer JP, Krier F, Revol-Junelles AM, Longeon A, Chaffotte A, Dejean A, Rossier J: Ponericins, new antibacterial and insecticidal peptides from the venom of the ant Pachycondyla goeldii . J Biol Chem 2001, 276:17823-17829. 10.1074/jbc.M100216200
58. Yount NY, Yeaman MR: Multidimensional signatures in antimicrobial peptides. Proc Natl Acad Sci U S A 2004, 101:7363-7368. 10.1073/pnas.0401567101
59. Mariette J, Escudié F, Allias N, Salin G, Noirot C, Thomas S, Klopp C: NG6: integrated next generation sequencing storage and processing environment. BMC Genomics 2012, 13:462. 10.1186/1471-2164-13-462
60. Li H, Durbin R: Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009, 25:1754-1760. 10.1093/bioinformatics/btp324
61. Schulz MH, Zerbino DR, Vingron M, Birney E: Oases: robust de novo RNA-seq assembly across the dynamic range of expression levels. Bioinformatics 2012, 28:1086-1092. 10.1093/bioinformatics/bts094
62. Li W, Godzik A: Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 2006, 22:1658-1659. 10.1093/bioinformatics/btl158
63. Gouzy J, Carrere S, Schiex T: FrameDP: sensitive peptide detection on noisy matured sequences. Bioinformatics 2009, 25:670-671. 10.1093/bioinformatics/btp024
64. Consortium T: The universal protein resource (UniProt) in 2010. Nucleic Acids Res 2010,38(Database issue):D142-D148.
65. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL: BLAST+: architecture and applications. BMC Bioinformatics 2009, 10:421. 10.1186/1471-2105-10-421
66. Zdobnov EM, Apweiler R: InterProScan-an integration platform for the signature-recognition methods in InterPro. Bioinformatics 2001, 17:847-848. 10.1093/bioinformatics/17.9.847
67. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M: Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 2005, 21:3674-3676. 10.1093/bioinformatics/bti610
68. Jungo F, Bairoch A: Tox-Prot, the toxin protein annotation program of the Swiss-Prot protein knowledgebase. Toxicon 2005, 45:293-301. 10.1016/j.toxicon.2004.10.018
69. Bendtsen JD, Nielsen H, von Heijne G, Brunak S: Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 2004, 340:783-795. 10.1016/j.jmb.2004.05.028
70. Edgar RC: MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32:1792-1797. 10.1093/nar/gkh340
71. Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ: Jalview version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 2009, 25:1189-1191. 10.1093/bioinformatics/btp033
72. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard J-F, Guindon S, Lefort V, Lescot M, Claverie J-M, Gascuel O: Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 2008,36(Web Server issue):W465-W469.