Proteomics comparison of aspartic protease enzyme in insects

Proteomics comparison of aspartic protease enzyme in insects

Aspartic proteases (APs; EC: 3.4.23) are a catalytic type of protease enzymes that use an activated water molecule, bound to one or more aspartate residues, for catalysis of their peptide substrates. In this study, bioinformatic analyses of APs enzymes were performed on insect protein sequences, including nineteen species of eleven different families. According to the conserved motifs obtained with MEME and MAST tools, three motifs were common to all insects. The structural and functional analyses of five selected insects from different orders were performed with ProtParam, SOPMA, SignalP 4.1, TMHMM 2.0, and ProDom tools in the ExPASy database. The tertiary structure of Apis mellifera as a sample of insects was predicted by the Phyre2 server using the "1qdm" model (PDB accession code: 1qdm) and was compared with Swiss-Model. The 3D structure quality was verified by the PROCHECK server. MegAlign was used for protein sequence alignment, and a phylogenetic tree was constructed with MEGA 6.06 software using the neighbor-joining method. In protein-protein interaction analysis with STRING 9.1, zero and twenty-seven significant protein interaction groups were identified in A. mellifera and other species, respectively. The obtained data provide a background for bioinformatic studies of the function and evolution of other insects and organisms.

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  • Alagarsamy S, Larroche C, Pandey A (2006). Microbiology and industrial biotechnology of food-grade proteases: a perspective. Food Technol Biotech 44: 211–220.
  • Bai Y, He S, Zhao G, Chen L, Shi N, Zhou H, Cong H, Zhao Q, Zhu XQ (2012). Toxoplasma gondii: bioinformatics analysis, cloning and expression of a novel protein TgIMP1. Exp Parasitol 132: 458–464.
  • Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009). MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37: W202–208.
  • Balczun C, Siemanowski J, Pausch JK, Helling S, Marcus K, Stephan C, Meyer HE, Schneider T, Cizmowski C, Oldenburg M et al. (2012). Intestinal aspartate proteases TiCatD and TiCatD2 of the haematophagous bug Triatoma infestans(Reduviidae): sequence characterisation, expression pattern and characterisation of proteolytic activity. Insect Biochem Molec 42: 240–250.
  • Baldwin ET, Bhat TN, Gulnik S, Hosur MV, Sowder RC, Cachau RE, Collins J, Silva AM, Erickson JW (1993). Crystal structures of native and inhibited forms of human cathepsin D: implications for lysosomal targeting and drug design. P Natl Acad Sci USA 90: 6796-6800.
  • Barrett A (1977). Cathepsin D and other carboxyl proteinases. In: Barrett AJ, editor. Proteinases in Mammalian Cells and Tissues. Amsterdam, the Netherlands: Elsevier, pp. 209-248.
  • Biasini M, Bienert S, Waterhouse A, Arnold K, Studer G, Schmidt T, Kiefer F, Cassarino TG, Bertoni M, Bordoli L et al. (2014). SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res 42: W252-258.
  • Bjellqvist B, Basse B, Olsen E, Celis JE (1994). Reference points for comparisons of two-dimensional maps of proteins from different human cell types defined in a pH scale where isoelectric points correlate with polypeptide compositions. Electrophoresis 15: 529-539.
  • Bjellqvist B, Hughes GJ, Pasquali C, Paquet N, Ravier F, Sanchez JC, Frutiger S, Hochstrasser D (1993). The focusing positions of polypeptides in immobilized pH gradients can be predicted from their amino acid sequences. Electrophoresis 14: 1023-1031.
  • Blobel G, Dobberstein B (1975). Transfer of proteins across membranes. I. Presence of proteolytically processed and unprocessed nascent immunoglobulin light chains on membrane-bound ribosomes of murine myeloma. J Cell Biol 67: 835-851.
  • Blundell T, Cooper J, Sali A, Zhu Z (1991). Comparison of the sequences, 3-D structures and mechanisms of pepsin-like and retroviral aspartic proteinases. In: Dunn BM, editor. Structure and Function of the Aspartic Proteases. New York, NY, USA: Plenum Press, pp. 443-453.
  • Cho WL, Dhadialla TS, Raikhel AS (1991). Purification and characterization of a lysosomal aspartic protease with cathepsin D activity from the mosquito. Insect Biochem 21: 165-176.
  • Ciechanover A (2005). Proteolysis: from the lysosome to ubiquitin and the proteasome. Nat Rev Mol Cell Bio 6: 79-87.
  • Colebatch G, East P, Cooper P (2001). Preliminary characterisation of digestive proteases of the green mirid, Creontiades dilutus(Hemiptera: Miridae). Insect Biochem Molec 31: 415-423.
  • Combet C, Blanchet C, Geourjon C, Deleage G (2000). NPS@: network protein sequence analysis. Trends Biochem Sci 25: 147-150.
  • Darabi M, Farhadi-Nejad H (2013). Study of the 3-hydroxy-3-methylglotaryl-coenzyme A reductase (HMGR) protein in Rosaceae by bioinformatics tools. Caryologia 66: 351-359.
  • Darabi M, Masoudi-Nejad A, Nemat-Zadeh G (2012). Bioinformatics study of the 3-hydroxy-3-methylglotaryl-coenzyme A reductase (HMGR) gene in Gramineae. Mol Biol Rep 39: 8925-8935.
  • Davies DR (1990). The structure and function of the aspartic proteinases. Annu Rev Biophys Bio 19: 189-215.
  • Dorrah MA, Yousef HA, Bassal TT (2000). Partial characterization of acidic proteinase in the midgut of Parasarcophaga surcoufilarvae (Diptera: Sarcophagidae). J Egypt Soc Parasitol 30: 643-653.
  • Ehrmann M, Clausen T (2004). Proteolysis as a regulatory mechanism. Annu Rev Genet 38: 709-724.
  • Elmelegi M, Dorrah M, Bassal T (2006). Aspartic and serine-peptidase activity in the midgut of the larval Parasarcophaga hertipes (Sarcophagidae, Cyclorrahapha, Diptera). Efflatounia 6: 1-9.
  • Franceschini A, Szklarczyk D, Frankild S, Kuhn M, Simonovic M, Roth A, Lin J, Minguez P, Bork P, von Mering C et al. (2013). STRING v9.1: protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res 41: D808-815.
  • Fraser A, Ring RA, Stewart RK (1961). Intestinal proteinases in an insect, Calliphora vomitoria L. Nature 192: 999-1000.
  • Fruton JS (1971). Pepsin. In: Boyer PD, editor. The Enzymes. New York, NY, USA: Academic Press, pp. 119-164.
  • Fruton JS (1987). Aspartyl proteinases. In: Neuberger A, Brocklehurst K, editors. New Comprehensive Biochemistry. Amsterdam, the Netherlands: Elsevier, pp. 1-38.
  • Gasteiger E, Hoogland C, Gattiker A, Wilkins MR, Appel RD, Bairoch A (2005). Protein identification and analysis tools on the ExPASy server. In: Walker JM, editor. The Proteomics Protocols Handbook. Totowa, NJ, USA: Humana Press, pp. 571-607.
  • Geourjon C, Deleage G (1995). SOPMA: significant improvements in protein secondary structure prediction by consensus prediction from multiple alignments. Comput Appl Biosci 11: 681-684.
  • Greenberg B, Paretsky D (1955). Proteolytic enzymes in the house fly, Musca domestica (L.). Ann Entomol Soc Am 48: 46-50.
  • Hill J, Phylip LH (1997). Bacterial aspartic proteinases. FEBS Lett 409: 357-360.
  • Houseman JG, Campbell FC, Morrison PE (1987). A preliminary characterization of digestive proteases in the posterior midgut of the stable fly Stomoxys calcitrans (L.) (Diptera: Muscidae). Insect Biochem 17: 213-218.
  • Houseman JG, Downe AER (1982). Characterization of an acidic proteinase from the posterior midgut of Rhodnius prolixus Stal (Hemiptera: Reduviidae). Insect Biochem 12: 651-655.
  • Houseman JG, Downe AER (1983). Cathepsin D-like activity in the posterior midgut of Hemipteran insects. Comp Biochem Phys B 75: 509-512.
  • Jiang B, Siregar U, Willeford KO, Luthe DS, Williams WP (1995). Association of a 33-kilodalton cysteine proteinase found in corn callus with the inhibition of fall armyworm larval growth. Plant Physiol 108: 1631-1640.
  • Kelley LA, Sternberg MJ (2009). Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4: 363-371.
  • Kervinen J, Tobin GJ, Costa J, Waugh DS, Wlodawer A, Zdanov A (1999). Crystal structure of plant aspartic proteinase prophytepsin: inactivation and vacuolar targeting. EMBO J 18: 3947-3955.
  • Kesici K, Tüney İ, Zeren D, Güden M, Sukatar A (2013). Morphological and molecular identification of pennate diatoms isolated from Urla, İzmir, coast of the Aegean Sea. Turk J Biol 37: 530-537.
  • Knop Wright M, Brandt S, Coudron T, Wagner R, Habibi J, Backus E, Huesing J (2006). Characterization of digestive proteolytic activity in Lygus hesperus Knight (Hemiptera: Miridae). J Insect Physiol 52: 717-728.
  • Kober L, Zehe C, Bode J (2013). Optimized signal peptides for the development of high expressing CHO cell lines. Biotechnol Bioeng 110: 1164-1173.
  • Kooij PW, Rogowska-Wrzesinska A, Hoffmann D, Roepstorff P, Boomsma JJ, Schiøtt M (2014). Leucoagaricus gongylophorususes leaf-cutting ants to vector proteolytic enzymes towards new plant substrate. ISME J 8: 1032-1040.
  • Lambremont EN, Fish FW, Ashrafi S (1959). Pepsin-like enzyme in larvae of stable flies. Science 129: 1484-1485.
  • Laskowski RA, MacArthur MW, Moss DS, Thornton JM (1993). PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 26: 283-291.
  • Laskowski RA, Rullmann JA, MacArthur MW, Kaptein R, Thornton JM (1996). AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J Biomol NMR 8: 477-486.
  • Lemos FJ, Terra WR (1991). Properties and intracellular distribution of a cathepsin D-like proteinase active at the acid region of Musca domestica midgut. Insect Biochem 21: 457-465.
  • Li XC, Luo GH, Han ZJ, Fang JC (2014). Molecular cloning and analysis of aspartic protease (AP) gene in Ty3/gypsyretrotransposon in different geographical populations of Chilo suppressalis (Lepidoptera: Pyralidae) in China. Acta Entomol Sinica 57: 530-537.
  • Lin JS, Lee SK, Chen Y, Lin WD, Kao CH (2011). Purification and characterization of a novel extracellular tripeptidyl peptidase from Rhizopus oligosporus. J Agric Food Chem 59: 11330-11337.
  • Lipke H, Fraenkel G, Liener I (1954). Growth inhibitors---effect of soybean inhibitors on growth of Tribolium confusum. J Agric Food Chem 2: 410-414.
  • López-Otín C, Bond JS (2008). Proteases: multifunctional enzymes in life and disease. J Biol Chem 283: 30433-30437.
  • Martin DM, Berriman M, Barton GJ (2004). GOtcha: a new method for prediction of protein function assessed by the annotation of seven genomes. BMC Bioinformatics 5: 178-195.
  • Mohan S, Ma P, Pechan T, Bassford E, Williams W, Luthe D (2006). Degradation of the S. frugiperda peritrophic matrix by an inducible maize cysteine protease. J Insect Physiol 52: 21-28.
  • Moller S, Croning MD, Apweiler R (2001). Evaluation of methods for the prediction of membrane spanning regions. Bioinformatics 17: 646-653.
  • Morris AL, MacArthur MW, Hutchinson EG, Thornton JM (1992). Stereochemical quality of protein structure coordinates. Proteins 12: 345-364.
  • Najafi MF, Deobagkar D, Deobagkar D (2005). Potential application of protease isolated from Pseudomonas aeruginosa PD100. Electron J Biotechno 8: 79-85.
  • Oikonomopoulou K, Hansen KK, Saifeddine M, Vergnolle N, Tea I, Diamandis EP, Hollenberg MD (2006). Proteinase-mediated cell signalling: targeting proteinase-activated receptors (PARs) by kallikreins and more. Biol Chem 387: 677-685.
  • Pechan T, Cohen A, Williams WP, Luthe DS (2002). Insect feeding mobilizes a unique plant defense protease that disrupts the peritrophic matrix of caterpillars. P Natl Acad Sci USA 99: 13319-13323.
  • Pendola S, Greenberg B (1975). Substrate-specific analysis of proteolytic enzymes in the larval midgut of Calliphora vicina. Ann Entomol Soc Am 68: 341-345.
  • Petersen TN, Brunak S, von Heijne G, Nielsen H (2011). SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8: 785-786.
  • Rabossi A, Stoka V, Puizdar V, Turk V, Quesada-Allué LA (2004). Novel aspartyl proteinase associated to fat body histolysis during Ceratitis capitata early metamorphosis. Arch Insect Biochem Physiol 57: 51-67.
  • Rao MB, Tanksale AM, Ghatge MS, Deshpande VV (1998). Molecular and biotechnological aspects of microbial proteases. Microbiol Mol Biol R 62: 597-635.
  • Rawlings ND, Barrett AJ (1995). Families of aspartic peptidases, and those of unknown catalytic mechanism. Methods Enzymol 248: 105-120.
  • Rawlings ND, Barrett AJ (1999). MEROPS: the peptidase database. Nucleic Acids Res 27: 325-331.
  • Romano P, Giugno R, Pulvirenti A (2011). Tools and collaborative environments for bioinformatics research. Brief Bioinform 12: 549-561.
  • Ryan CA (1990). Protease inhibitors in plants: genes for improving defenses against insects and pathogens. Annu Rev Phytopathol 28: 425-449.
  • Sabotič J, Kos J (2012). Microbial and fungal protease inhibitors---current and potential applications. Appl Microbiol Biot 93: 1351-1375.
  • Seddigh S, Darabi M (2014). Comprehensive analysis of beta-galactosidase protein in plants based on Arabidopsis thaliana. Turk J Biol 38: 140-150.
  • Servant F, Bru C, Carrère S, Courcelle E, Gouzy J, Peyruc D, Kahn D (2002). ProDom: automated clustering of homologous domains. Brief Bioinform 3: 246-251.
  • Sielecki A, Fujinaga M, Read R, James M (1991). Refined structure of porcine pepsinogen at 1.8 Å resolution. J Mol Biol 219: 671-692.
  • Silva CP, Xavier-Filho J (1991). Comparison between the levels of aspartic and cysteine proteinases of the larval midguts of Callosobruchus maculatus (F.) and Zabrotes subfasciatus(BOH.) (Coleoptera: bruchidae). Comp Biochem Phys B 99: 529-533.
  • Sinha M (1975). Pepsin-like activity in the midgut of Sarcophaga ruficornis and Musca domestica. Appl Entomol Zool 10: 313-315.
  • Söding J (2005). Protein homology detection by HMM-HMM comparison. Bioinformatics 21: 951-960.
  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013). MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30: 2725-2729.
  • Tang J (1979). Evolution in the structure and function of carboxyl proteases. Mol Cell Biochem 26: 93-109.
  • Terra WR, Ferreira C, Garcia ES (1988). Origin, distribution, properties and functions of the major Rhodnius prolixusmidgut hydrolases. Insect Biochem 18: 423-434.
  • Thie NM, Houseman JG (1990). Identification of cathepsin B, D and H in the larval midgut of Colorado potato beetle, Leptinotarsa decemlineata Say (Coleoptera: Chrysomelidae). Insect Biochem 20: 313-318.
  • Umezawa H, Aoyagi T, Morishima H, Matsuzaki M, Hamada M (1970). Pepstatin, a new pepsin inhibitor produced by Actinomycetes. J Antibiot 23: 259-262.
  • Von Heijne G (1985). Signal sequences: the limits of variation. J Mol Biol 184: 99-105.
  • Wielkopolan B, Walczak F, Podleśny A, Nawrot R, Obrępalska-Stęplowska A (2015). Identification and partial characterization of proteases in larval preparations of the cereal leaf beetle (Oulema melanopus, Chrysomelidae, Coleoptera). Arch Insect Biochem 88: 192-202.
  • Wolfson J, Murdock L (1987). Suppression of larval Colorado potato beetle growth and development by digestive proteinase inhibitors. Entomol Exp Appl 44: 235-240.
  • Wolfson JL, Murdock LL (1990). Diversity in digestive proteinase activity among insects. J Chem Ecol 16: 1089-1102.
  • Yegin S, Fernandez-Lahore M, Salgado AJG, Guvenc U, Goksungur Y, Tari C (2011). Aspartic proteinases from Mucor spp. in cheese manufacturing. Appl Microbiol Biotechnol 89: 949-960.
  • Zhao G, Zhou A, Lu G, Meng M, Sun M, Bai Y, Han Y, Wang L, Zhou H, Cong H (2013). Identification and characterization of Toxoplasma gondii aspartic protease 1 as a novel vaccine candidate against toxoplasmosis. Parasite Vector 6: 175-188.