Intestinal aspartate proteases TiCatD and TiCatD2 of the haematophagous bug Triatoma infestans (Reduviidae): Sequence characterisation, expression pattern and characterisation of proteolytic activity

Insect Biochemistry and Molecular Biology

Volumn 42, Issue 4, 2012, Pages 240-250

  Balczun, Carsten ^a   Siemanowski, Janna ^a   Pausch, Jennifer Katharina ^a   Helling, Stefan ^b   Marcus, Katrin ^b   Stephan, Christian ^b   Meyer, Helmut E ^b   Schneider, Tobias ^a   Cizmowski, Christian ^a   Oldenburg, Marina ^a   Höhn, Sandra ^a   Meiser, Christian Karl ^a   Schuhmann, Wolfgang ^a   Schaub, Günter A ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

Aspartate protease; Cathepsin D; Haematophagous bug; Intestinal pH; Triatoma infestans

Indexed keywords

ASPARTIC PROTEINASE; COMPLEMENTARY DNA; INSECT PROTEIN;

AFFINITY CHROMATOGRAPHY; AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CHEMISTRY; DNA SEQUENCE; ENZYMOLOGY; GENE EXPRESSION; GENETICS; INTESTINE; ISOLATION AND PURIFICATION; MASS SPECTROMETRY; METABOLISM; MOLECULAR GENETICS; MOLECULAR WEIGHT; PH; TRIATOMA;

AMINO ACID SEQUENCE; ANIMALS; ASPARTIC ACID PROTEASES; CHROMATOGRAPHY, AFFINITY; DNA, COMPLEMENTARY; GENE EXPRESSION; HYDROGEN-ION CONCENTRATION; INSECT PROTEINS; INTESTINES; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; SEQUENCE ANALYSIS, DNA; TRIATOMA;

HEXAPODA; REDUVIIDAE; TRIATOMA INFESTANS;

EID: 84857141774     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2011.12.006     Document Type: Article

References (71)

1. Ahn J.E., Zhu-Salzman K. CmCatD, a cathepsin D-like protease has a potential role in insect defense against a phytocystatin. J. Insect Physiol. 2009, 55:678-685.
2. Altschul S.F., Madden T.L., Schäffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl. Acids Res. 1997, 25:3389-3402.
3. Assumpção T.C., Francischetti I.M., Andersen J.F., Schwarz A., Santana J.M., Ribeiro J.M. An insight into the sialome of the blood-sucking bug Triatoma infestans, a vector of Chagas' disease. Insect Biochem. Mol. Biol. 2008, 38:213-232.
4. Azambuja P., Guimaraes J.A., Garcia E.S. Haemolytic factor from the crop of Rhodnius prolixus: evidence and partial characterization. J. Insect Physiol. 1983, 29:833-837.
5. Barros V.C., Assumpcao J.G., Cadete A.M., Santos V.C., Cavalcante R.R., Araujo R.N., Pereira M.H., Gontijo N.F. The role of salivary and intestinal complement system inhibitors in the midgut protection of triatomines and mosquitoes. PLoS One 2009, 4:e6047.
6. Bendtsen J.D., Nielsen H., von Heijne G., Brunak S. Improved prediction of signal peptides: signalP 3.0. J. Mol. Biol. 2004, 340:783-795.
7. Billingsley P.F., Downe A.E.R. Ultrastructural changes in posterior midgut cells associated with blood feeding in adult female Rhodnius prolixus Stal (Hemiptera, Reduviidae). Can. J. Zool. 1983, 61:2574-2586.
8. Billingsley P.F., Downe A.E.R. Changes in the anterior midgut cells of adult female Rhodnius prolixus (Hemiptera, Reduviidae) after feeding. J. Med. Entomol. 1989, 26:104-108.
9. Blüggel M., Bailey S., Korting G., Stephan C., Reidegeld K.A., Thiele H., Apweiler R., Hamacher M., Meyer H.E. Towards data management of the HUPO Human Brain Proteome Project pilot phase. Proteomics 2004, 4:2361-2362.
10. Borges E.C., Machado E.M., Garcia E.S., Azambuja P. Trypanosoma cruzi: effects of infection on cathepsin D activity in the midgut of Rhodnius prolixus. Exp. Parasitol. 2006, 112:130-133.
11. Britton H.T.S., Robinson R.A. CXCVIII, Universal buffer solutions and the dissociation constant of veronal. J. Chem. Soc. 1931, 198:1456-1462.
12. Chamrad D.C., Koerting G., Gobom J., Thiele H., Klose J., Meyer H.E., Blueggel M. Interpretation of mass spectrometry data for high-throughput proteomics. Anal. Bioanal. Chem. 2003, 376:1014-1022.
13. Cho W.L., Raikhel A.S. Cloning of cDNA for mosquito lysosomal aspartic protease. Sequence analysis of an insect lysosomal enzyme similar to cathepsins D and E. J. Biol. Chem. 1992, 267:21823-21829.
14. Cho W.L., Dhadialla T.S., Raikhel A.S. Purification and characterization of a lysosomal aspartic protease with cathepsin D activity from the mosquito. Insect Biochem. 1991, 21:165-176.
15. Cho W.L., Tsao S.M., Hays A.R., Walter R., Chen J.S., Snigirevskaya E.S., Raikhel A.S. Mosquito cathepsin B-like protease involved in embryonic degradation of vitellin is produced as a latent extraovarian precursor. J. Biol. Chem. 1999, 274:13311-13321.
16. Conner G.E. Isolation of procathepsin-D from mature cathepsin-D by pepstatin affinity-chromatography - autocatalytic proteolysis of the zymogen form of the enzyme. Biochem. J. 1989, 263:601-604.
17. Conner G.E. Cathepsin D. Handbook of Proteolytic Enzymes 2002, 746-751. Academic Press, New York. A.J. Barret, N.D. Rawlings, J.F. Wössner (Eds.).
18. Cristofoletti P.T., Ribeiro A.F., Terra W.R. The cathepsin L-like proteinases from the midgut of Tenebrio molitor larvae: sequence, properties, immunocytochemical localization and function. Insect Biochem. Mol. Biol. 2005, 35:883-901.
19. Davies D.R. The structure and function of the aspartic proteinases. Annu. Rev. Biophys. Biophys. Chem. 1990, 19:189-215.
20. Dunn B.M. Structure and mechanism of the pepsin-like family of aspartic peptidases. Chem. Rev. 2002, 102:4431-4458.
21. Espinoza-Fuentes F.P., Terra W.R. Physiological adaptations for digesting bacteria. Water fluxes and distribution of digestive enzymes in Musca domestica larval midgut. Insect Biochem. 1987, 17:809-817.
22. Etienne M., Dierkes P., Erichsen T., Schuhmann W., Fritsch I. Constant-distance mode scanning potentiometry. High resolution pH measurements in three-dimensions. Electroanalysis 2007, 19:318-323.
23. Garcia E.S., Garcia M.L.M. Control of protease secretion in intestine of fifth instar larvae of Rhodnius prolixus. J. Insect Physiol. 1977, 23:247-251.
24. Garcia E.S., Genta F.A., de Azambuja P., Schaub G.A. Interactions between intestinal compounds of triatomines and Trypanosoma cruzi. Trends Parasitol. 2010, 26:499-505.
25. Gasteiger E., Hoogland C., Gattiker A., Duvaud S., Wilkins M.R., Appel R.D., Bairoch A. Protein identification and analysis tools on the ExPASy server. The Proteomics Protocols Handbook 2005, 571-607. Humana, New York. J.M. Walker (Ed.).
26. Geier G., Banaj H.J., Heid H., Bini L., Pallini V., Zwilling R. Aspartyl proteases in Caenorhabditis elegans. Isolation, identification and characterization by a combined use of affinity chromatography, two-dimensional gel electrophoresis, microsequencing and databank analysis. Eur. J. Biochem. 1999, 264:872-879.
27. Gui Z.Z., Lee K.S., Kim B.Y., Choi Y.S., Wei Y.D., Choo Y.M., Kang P.D., Yoon H.J., Kim I., Je Y.H., Seo S.J., Lee S.M., Guo X.J., Sohn H.D., Jin B.R. Functional role of aspartic proteinase cathepsin D in insect metamorphosis. BMC Dev. Biol. 2006, 6:49. 10.1186/1471-213X-6-49.
28. Henning L. WinPep 2.11: novel software for PC-based analyses of amino acids sequences. Prep. Biochem. Biotechnol. 2001, 31:201-207.
29. Hong L., Tang J. Flap position of free memapsin 2 (beta-secretase), a model for flap opening in aspartic protease catalysis. Biochemistry 2004, 43:4689-4695.
30. Hori K. Physiological conditions in midgut in relation to starch digestion and salivary amylase of the bug Lygus disponsi. J. Insect Physiol. 1971, 17:1153-1167.
31. Houseman J. A thiol-activated digestive proteinase from adults of Rhodnius prolixus Stal (Hemiptera-Reduviidae). Can. J. Zool. 1978, 56:1140-1143.
32. Houseman J.G., Downe A.E.R. Endoproteinase activity in the posterior midgut of Rhodnius prolixus Stal (Hemiptera, Reduviidae). Insect Biochem. 1980, 10:363-366.
33. Houseman J.G., Downe A.E.R. Exoproteinase activity in the posterior midgut of Rhodnius prolixus Stal (Hemiptera, Reduviidae). Insect Biochem. 1981, 11:579-582.
34. Houseman J.G., Downe A.E.R. Identification and partial characterization of digestive proteinases from Triatoma phyllosoma pallidipennis Stal (Hemiptera, Reduviidae). Comp. Biochem. Phys. B. 1981, 70:713-717.
35. Houseman J.G., Downe A.E.R. Characterization of an acidic proteinase from the posterior midgut of Rhodnius prolixus Stal (Hemiptera, Reduviidae). Insect Biochem. 1982, 12:651-655.
36. Houseman J.G., Downe A.E.R. Activity cycles and the control of four digestive proteinases in the posterior midgut of Rhodnius prolixus Stal (Hemiptera, Reduviidae). J. Insect Physiol. 1983, 29:141-148.
37. Houseman J.G., Downe A.E.R. The effects of three metabolic inhibitors on digestive proteinase production in Rhodnius prolixus Stal (Hemiptera, Reduviidae). J. Insect Physiol. 1983, 29:317-321.
38. James M.N.G. Catalytic pathway of aspartic peptidases. Handbook of Proteolytic Enzymes 2004, 12-19. Elsevier, London. A.J. Barret, N.D. Rawlings, J.F. Wössner (Eds.).
39. Khan M.R., Ford J.B. The distribution and localization of digestive enzymes in the alimentary canal and salivary glands of the cotton stainer, Dysdercus fasciatus. J. Insect Physiol. 1967, 13:1619-1628.
40. Kollien A.H., Schaub G.A. The development of Trypanosoma cruzi (Trypanosomatidae) in the reduviid bug Triatoma infestans (Insecta): influence of starvation. J. Eukaryot. Microbiol. 1998, 45:59-63.
41. Kollien A.H., Schaub G.A. The development of Trypanosoma cruzi in Triatominae. Parasitol. Today 2000, 16:381-387.
42. Kollien A.H., Waniek P.J., Nisbet A.J., Billingsley P.F., Schaub G.A. Activity and sequence characterization of two cysteine proteases in the digestive tract of the reduviid bug Triatoma infestans. Insect Mol. Biol. 2004, 13:569-579.
43. Lehane M.J. Managing the blood meal. Biology of Blood-Sucking Insects 1991, 84-115. Cambridge University Press, Cambridge. second ed. M.J. Lehane (Ed.).
44. Lehane M.J. Digestive enzymes, hemolysins and symbionts in the search for vaccines against blood sucking insects. Int. J. Parasitol. 1994, 24:27-32.
45. Lopez-Ordoñez T., Rodriguez M.H., Hernandez-Hernandez F.D. Characterization of a cDNA encoding a cathepsin L-like protein of Rhodnius prolixus. Insect Mol. Biol. 2001, 10:505-511.
46. Medina M., Vallejo C.G. An aspartic proteinase in Drosophila: maternal origin and yolk localization. Int. J. Dev. Biol. 1989, 33:313-315.
47. Meiser C.K., Piechura H., Meyer H.E., Warscheid B., Schaub G.A., Balczun C. A salivary serine protease of the haematophagous reduviid Panstrongylus megistus: sequence characterization, expression pattern and characterization of proteolytic activity. Insect Mol. Biol. 2010, 19:409-421.
48. Neurath H. Proteolytic processing and regulation. Enzyme 1991, 45:239-243.
49. Nicholas K.B., Nicholas H.B.J., Deerfield D.W. GeneDoc: analysis and visualization of genetic variations. Embnet News 1997, 4:1-4.
50. Padilha M.H., Pimentel A.C., Ribeiro A.F., Terra W.R. Sequence and function of lysosomal and digestive cathepsin D-like proteinases of Musca domestica midgut enzymes. Insect Biochem. Mol. Biol. 2009, 39:782-791.
51. Park Y.N., Aikawa J., Nishiyama M., Horinouchi S., Beppu T. Involvement of a residue at position 75 in the catalytic mechanism of a fungal aspartic proteinase, Rhizomucor pusillus pepsin. Replacement of tyrosine 75 on the flap by asparagine enhances catalytic efficiency. Protein Eng. 1996, 9:869-875.
52. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001, 29:e45.
53. ©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 2002, 30:e36.
54. Rabossi A., Stoka V., Puizdar V., Turk V., Quesada-Allue L.A. Novel aspartyl proteinase associated to fat body histolysis during Ceratitis capitata early metamorphosis. Arch. Insect Biochem. Physiol. 2004, 57:51-67.
55. Ramakers C., Ruijter J.M., Deprez R.H., Moorman A.F. Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci. Lett. 2003, 339:62-66.
56. Reddy K.R., Turcu F., Schulte A., Kayastha A.M., Schuhmann W. Fabrication of a potentiometric/amperometric bifunctional enzyme microbiosensor. Anal. Chem. 2005, 77:5063-5067.
57. Sajid M., McKerrow J.H. Cysteine proteases of parasitic organisms. Mol. Biochem. Parasitol. 2002, 120:1-21.
58. Schaub G.A. Trypanosoma cruzi: quantitative studies of development of two strains in small intestine and rectum of the vector Triatoma infestans. Exp. Parasitol. 1989, 68:260-273.
59. Schaub, G.A., 2008. Kissing bugs. In: Mehlhorn, H. (Ed.), Encyclopedia of Parasitology, vol. 1. Biology, Structure, Function, third edn. Springer-Verlag, Heidelberg, pp. 684-686.
60. Schaub G.A. Interactions of trypanosomatids and triatomines. Adv. Insect Physiol. 2009, 37:177-242.
61. Silva C.P., Terra W.R. Digestive and absorptive sites along the midgut of the cotton seed sucker bug Dysdercus peruvianus (Hemiptera: Pyrrhocoridae). Insect Biochem. Mol. Biol. 1994, 24:493-505.
62. Sojka D., Franta Z., Horn M., Hajdusek O., Caffrey C.R., Mares M., Kopacek P. Profiling of proteolytic enzymes in the gut of the tick Ixodes ricinus reveals an evolutionarily conserved network of aspartic and cysteine peptidases. Parasit. Vectors 2008, 1:7. 10.1186/1756-3305-1-7.
63. Tamura K., Dudley J., Nei M., Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007, 24:1596-1599.
64. Terra W.R. Evolution of digestive systems of insects. Annu. Rev. Entomol. 1990, 35:181-200.
65. Terra W.R., Ferreira C. Insect digestive enzymes - Properties, compartmentalization and function. Comp. Biochem. Physiol. B-Biochem. Mol. Biol. 1994, 109:1-62.
66. Terra W.R., Ferreira C., Baker J.E. Compartimentalization of digestion. Biology of the Insect Midgut 1996, 206-235. Chapman & Hall, London. M.J. Lehane, P.F. Billingsley (Eds.).
67. Terra W.R., Ferreira C., Garcia E.S. Origin, distribution, properties and functions of the major Rhodnius prolixus midgut hydrolases. Insect Biochem. 1988, 18:423-434.
68. Thie N.M.R., Houseman J.G. Identification of cathepsin-B, cathepsin-D and cathepsin-H in the larval midgut of Colorado potato beetle, Leptinotarsa decemlineata Say (Coleoptera, Chrysomelidae). Insect Biochem. 1990, 20:313-318.
69. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997, 25:4876-4882.
70. Waniek P.J., Hendgen-Cotta U.B., Stock P., Mayer C., Kollien A.H., Schaub G.A. Serine proteinases of the human body louse (Pediculus humanus): sequence characterization and expression patterns. Parasitol. Res. 2005, 97:486-500.
71. Winnebeck E.C., Millar C.D., Warman G.R. Why does insect RNA look degraded?. J. Insect Sci. 2010, 10:159.