Chemosensory proteins, major salivary factors in caterpillar mandibular glands

Insect Biochemistry and Molecular Biology

Volumn 42, Issue 10, 2012, Pages 796-805

  Celorio Mancera, Maria de la Paz ^a   Sundmalm, Sara M ^a   Vogel, Heiko ^b   Rutishauser, Dorothea ^c,d   Ytterberg, A Jimmy ^c   Zubarev, Roman A ^c,d   Janz, Niklas ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^c KAROLINSKA INSTITUTE   (Sweden)

^d SCIENCE FOR LIFE LABORATORY   (Sweden)

Author keywords

Amylase; Caterpillar; Chemosensory protein; Insect host plant interaction; Lysozyme; Mandibular glands; Mass spectrometry; Phyllosphere; Proteomics; Saliva

Indexed keywords

INSECT PROTEIN;

ANIMAL; ARTICLE; BUTTERFLY; CHEMISTRY; GENETICS; GROWTH, DEVELOPMENT AND AGING; LARVA; METABOLISM; MOLECULAR GENETICS; PROTEOMICS; SALIVA; SUBMANDIBULAR GLAND;

ANIMALS; BUTTERFLIES; INSECT PROTEINS; LARVA; MOLECULAR SEQUENCE DATA; PROTEOMICS; SALIVA; SUBMANDIBULAR GLAND;

HEXAPODA; NYMPHALIDAE; VANESSA GONERILLA;

EID: 84865861764     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2012.07.008     Document Type: Article

References (55)

1. Akai H., Hakim R.S., Kristensen N.P. Labial glands, silk and saliva. Handbuch der Zoologie (Berlin) 2003, 4:377-388.
2. Anderson P., Löfqvist J. Asymmetric oviposition behaviour and the influence of larval competition in the two pyralid moths Ephestia kuehniella and Plodia interpunctella. Oikos 1996, 76:47-56.
3. Asadi A., Ghadamyari M., Sajedi R.H., Sendi J.J., Tabari M. Biochemical characterization of midgut, salivary glands and haemolymph alpha-amylases of Naranga aenescens. Bulletin of Insectology 2010, 63:175-181.
4. Assumpção T.C.F., Francischetti I.M.B., Andersen J.F., Schwarz A., Santana J.M., Ribeiro J.M.C. An insight into the sialome of the blood-sucking bug Triatoma infestans, a vector of Chagas' disease. Insect Biochemistry and Molecular Biology 2008, 38:213-232.
5. Barron M.C., Wratten S.D., Barlow N.D. Phenology and parasitism of the red admiral butterfly Bassaris gonerilla (Lepidoptera: Nymphalidae). New Zealand Journal of Ecology 2004, 28:105-111.
6. Bede J.C., Musser R.O., Felton G.W., Korth K.L. Caterpillar herbivory and salivary enzymes decrease transcript levels of Medicago truncatula genes encoding early enzymes in terpenoid biosynthesis. Plant Molecular Biology 2006, 60:519-531.
7. Bradford M.M. Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Analytical Biochemistry 1976, 72:248-254.
8. Callewaert L., Michiels C.W. Lysozymes in the animal kingdom. Journal of Biosciences 2010, 35:127-160.
9. Celorio-Mancera M.D., Courtiade J., Muck A., Heckel D.G., Musser R.O., Vogel H. Sialome of a generalist lepidopteran herbivore: identification of transcripts and proteins from Helicoverpa armigera labial salivary glands. PLoS ONE 2011, 6.
10. Dawkar V.V., Chikate Y.R., Gupta V.S., Slade S.E., Giri A.P. Assimilatory potential of Helicoverpa armigera reared on host (Chickpea) and nonhost (Cassia tora) diets. Journal of Proteomic Research 2011, 10:5128-5138.
11. de Godoy L.M.F., Olsen J.V., Cox J., Nielsen M.L., Hubner N.C., Frohlich F., Walther T.C., Mann M. Comprehensive mass-spectrometry-based proteome quantification of haploid versus diploid yeast. Nature 2008, 455:1251-1254.
12. Eichenseer H., Mathews M.C., Bi J.L., Murphy J.B., Felton G.W. Salivary glucose oxidase: multifunctional roles for Helicoverpa zea?. Archives of Insect Biochemistry and Physiology 1999, 42:99-109.
13. Felton G.W., Eichenseer H. Herbivore saliva and its effects on plant defense against herbivores and pathogens. Induced Plant Defenses against Pathogens and Herbivores 1999, 19-36. APS Press, St. Paul. A.A. Agrawal, S. Tuzan, E. Bent (Eds.).
14. Freitak D., Wheat C.W., Heckel D.G., Vogel H. Immune system responses and fitness costs associated with consumption of bacteria in larvae of Trichoplusia ni. BMC Biology 2007, 5.
15. Furusawa T., Rakwal R., Nam H.W., Hirano M., Shibato J., Kim Y.S., Ogawa Y., Yoshida Y., Kramer K.J., Kouzuma Y., Agrawal G.K., Yonekura M. Systematic investigation of the hemolymph proteome of Manduca sexta at the fifth instar larvae stage using one- and two-dimensional proteomics platforms. Journal of Proteomic Research 2008, 7:938-959.
16. Gasteiger E., Gattiker A., Hoogland C., Ivanyi I., Appel R.D., Bairoch A. ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Research 2003, 31:3784-3788.
17. Gibbs G.W. New Zealand Butterflies: Identification and Natural History 1980, William Collins Publishers Ltd, Auckland, New Zealand.
18. Gotz S., Garcia-Gomez J.M., Terol J., Williams T.D., Nagaraj S.H., Nueda M.J., Robles M., Talon M., Dopazo J., Conesa A. High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Research 2008, 36:3420-3435.
19. Graham L.A., Brewer D., Lajoie G., Davies P.L. Characterization of a subfamily of beetle odorant-binding proteins found in hemolymph. Molecular & Cellular Proteomics 2003, 2:541-549.
20. Hekmat-Scafe D.S., Scafe C.R., McKinney A.J., Tanouye M.A. Genome-wide analysis of the odorant-binding protein gene family in Drosophila melanogaster. Genome Research 2002, 12:1357-1369.
21. Honson N.S., Gong Y., Plettner E. Chapter Nine Structure and function of insect odorant and pheromone-binding proteins (OBPs and PBPs) and chemosensory-specific proteins (CSPs). Recent Advances in Phytochemistry 2005, 227-268. Elsevier. T.R. John (Ed.).
22. Hou Y., Zou Y., Wang F., Gong J., Zhong X.W., Xia Q.Y., Zhao P. Comparative analysis of proteome maps of silkworm hemolymph during different developmental stages. Proteome Science 2010, 8:10.
23. Iovinella I., Dani F.R., Niccolini A., Sagona S., Michelucci E., Gazzano A., Turillazzi S., Felicioli A., Pelosi P. Differential expression of odorant-binding proteins in the mandibular glands of the honey bee according to caste and age. Journal of Proteomic Research 2011, 10:3439-3449.
24. Jiang H.B., Ma C.C., Lu Z.Q., Kanost M.R.β-1,3-Glucan recognition protein-2 (beta GRP-2) from Manduca sexta: an acute-phase protein that binds beta-1,3-glucan and lipoteichoic acid to aggregate fungi and bacteria and stimulate prophenoloxidase activation. Insect Biochemistry and Molecular Biology 2004, 34:89-100.
25. Jin X., Zhang S.G., Zhang L. Expression of odorant-binding and chemosensory proteins and spatial map of chemosensilla on labial palps of Locusta migratoria (Orthoptera: Acrididae). Arthropod Structure & Development 2006, 35:47-56.
26. Kanost M.R., Kawooya J.K., Ryan R.D., Van Heusden M.C., Ziegler R. Insect hemolymph proteins. Advances in Insect Physiology 1990, 22:299-366.
27. Kawooya J.K., Keim P.S., Ryan R.O., Shapiro J.P., Samaraweera P., Law J.H. Insect apolipophorin-iii - purification and properties. Journal of Biological Chemistry 1984, 259:733-737.
28. Lagarde A., Spinelli S., Tegoni M., He X., Field L., Zhou J.J., Cambillau C. The crystal structure of odorant binding protein 7 from Anopheles gambiae exhibits an outstanding adaptability of its binding site. Journal of Molecular Biology 2011, 414:401-412.
29. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J., Higgins D.G. Clustal W and clustal X version 2.0. Bioinformatics 2007, 23:2947-2948.
30. Lindow S.E., Brandl M.T. Microbiology of the phyllosphere. Applied and Environmental Microbiology 2003, 69:1875-1883.
31. Liu F., Cui L.W., Cox-Foster D., Felton G.W. Characterization of a salivary lysozyme in larval Helicoverpa zea. Journal of Chemical Ecology 2004, 30:2439-2457.
32. Loo J.A., Yan W., Ramachandran P., Wong D.T. Comparative human salivary and plasma proteomes. Journal of Dental Research 2010, 89:1016-1023.
33. Lourenĉo A.P., Martins J.R., Bitondi M.M.G., Simões Z.L.P. Trade-off between immune stimulation and expression of storage protein genes. Archives of Insect Biochemistry and Physiology 2009, 71:70-87.
34. Mall S.B., Singh A.R., Dixit A. Digestive enzymes of mature larva of Atteva-fabriciella (Swed) (Lepidoptera, Yponomeutidae). Journal of Animal Morphology and Physiology 1978, 25:86-92.
35. Mulnix A.B., Dunn P.E. Structure and induction of a lysozyme gene from the tobacco hornworm, Manduca sexta. Insect Biochemistry and Molecular Biology 1994, 24:271-281.
36. Musser R.O., Cipollini D.F., Hum-Musser S.M., Williams S.A., Brown J.K., Felton G.W. Evidence that the caterpillar salivary enzyme glucose oxidase provides herbivore offense in Solanaceous plants. Archives of Insect Biochemistry and Physiology 2005, 58:128-137.
37. Ngernyuang N., Kobayashi I., Promboon A., Ratanapo S., Tamura T., Ngernsiri L. Cloning and expression analysis of the Bombyx mori alpha-amylase gene (Amy) from the indigenous Thai silkworm strain, Nanglai. Journal of Insect Science 2011, 11.
38. Parthasarathy R., Gopinathan K.P. Comparative analysis of the development of the mandibular salivary glands and the labial silk glands in the mulberry silkworm, Bombyx mori. Gene Expression Patterns 2005, 5:323-339.
39. Paskewitz S.M., Shi L. The hemolymph proteome of Anopheles gambiae. Insect Biochemistry and Molecular Biology 2005, 35:815-824.
40. Pauchet Y., Muck A., Svatos A., Heckel D.G., Preiss S. Mapping the larval midgut lumen proteorne of Helicoverpa armigera, a generalist herbivorous insect. Journal of Proteomic Research 2008, 7:1629-1639.
41. Pauchet Y., Freitak D., Heidel-Fischer H.M., Heckel D.G., Vogel H. Glucanase activity in a glucan-binding protein family from Lepidoptera. Journal of Biological Chemistry 2009, 284:2214-2224.
42. Petersen T.N., Brunak S., von Heijne G., Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nature Methods 2011, 8:785-786.
43. Petrak J., Ivanek R., Toman O., Cmejla R., Cmejlova J., Vyoral D., Zivny J., Vulpe C.D. Deja vu in proteomics. A hit parade of repeatedly identified differentially expressed proteins. Proteomics 2008, 8:1744-1749.
44. Pelosi P., Zhou J.J., Ban L.P., Calvello M. Soluble proteins in insect chemical communication. Cellular and Molecular Life Sciences 2006, 63:1658-1676.
45. Pieper U., Webb B., Barkan D., Schneidman-Duhovny D., Schlessinger A., Braberg H., Yang Z., Meng E., Pettersen E., Huang C., Datta R., Sampathkumar P., Madhusudhan M., Sjolander K., Ferrin T., Burley S., Sali A. MODBASE, a database of annotated comparative protein structure models and associated resources. Nucleic Acids Research 2011, 39:465-474.
46. Ryan R.O., Anderson D.R., Grimes W.J., Law J.H. Arylphorin from Manduca sexta - carbohydrate structure and immunological studies. Archives of Biochemistry and Biophysics 1985, 243:115-124.
47. Shevchenko A., Wilm M., Vorm O., Jensen O.N., Podtelejnikov A.V., Neubauer G., Mortensen P., Mann M. A strategy for identifying gel-separated proteins in sequence databases by MS alone. Biochemical Society Transactions 1996, 24:893-896.
48. Shimomura M., Minami H., Suetsugu Y., Ohyanagi H., Satoh C., Antonio B., Nagamura Y., Kadono-Okuda K., Kajiwara H., Sezutsu H., Nagaraju J., Goldsmith M.R., Xia Q., Yamamoto K., Mita K. KAIKObase: an integrated silkworm genome database and data mining tool. BMC Genomics 2009, 10:486.
49. Shin S.W., Park S.S., Park D.S., Kim M.G., Kim S.C., Brey P.T., Park H.Y. Isolation and characterization of immune-related genes from the fall webworm, Hyphantria cunea, using PCR-based differential display and subtractive cloning. Insect Biochemistry and Molecular Biology 1998, 28:827-837.
50. Silva J.C., Gorenstein M.V., Li G.Z., Vissers J.P.C., Geromanos S.J. Absolute quantification of proteins by LCMSE - a virtue of parallel MS acquisition. Molecular & Cellular Proteomics 2006, 5:144-156.
51. Teese M.G., Campbell P.M., Scott C., Gordon K.H.J., Southon A., Hovan D., Robin C., Russell R.J., Oakeshott J.G. Gene identification and proteomic analysis of the esterases of the cotton bollworm, Helicoverpa armigera. Insect Biochemistry and Molecular Biology 2010, 40:1-16.
52. Vegliante F., Hasenfuss I. Morphology and diversity of exocrine glands in lepidopteran larvae. Annual Review of Entomology 2012, 187-204.
53. Vogel H., Altincicek B., Glockner G., Vilcinskas A. A comprehensive transcriptome and immune-gene repertoire of the lepidopteran model host Galleria mellonella. BMC Genomics 2011, 12.
54. Walker G.P. Salivary glands. Encyclopedia of Insects 2009, 897-901. Academic Press, Elsevier, Amsterdam. second ed. V.H. Resh, R.T. Carde (Eds.).
55. Wroniszewska A. Mandibular glands of the wax moth larva Galleria mellonella (L.). Journal of Insect Physiology 1966, 12:509-552.