In-depth characterization of trypsin-like serine peptidases in the midgut of the sugar fed Culex quinquefasciatus

Parasites and Vectors

Volumn 8, Issue 1, 2015, Pages

  Borges Veloso, André ^a   Saboia Vahia, Leonardo ^a   Dias Lopes, Geovane ^a   Domont, Gilberto B ^b   Britto, Constança ^a   Cuervo, Patricia ^a   De Jesus, Jose B ^a,c  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c FEDERAL UNIVERSITY OF SÃO JOÃO DEL REI   (Brazil)

Author keywords

Culex quinquefasciatus; Mass spectrometry; Trypsin like serine peptidases; Zymography

Indexed keywords

DODECYL SULFATE SODIUM; SERINE PROTEINASE; TRYPSIN; INSECT PROTEIN; SUCROSE;

AMINO ACID SEQUENCE; ANALYTIC METHOD; ANIMAL TISSUE; ARTICLE; BIOINFORMATICS; CONTROLLED STUDY; CULEX QUINQUEFASCIATUS; DATA MINING; DISULFIDE BOND; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME ASSAY; ENZYME LOCALIZATION; ENZYME SUBSTRATE; LIQUID CHROMATOGRAPH; MIDGUT; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN DATABASE; PROTEIN EXPRESSION; PROTEIN MOTIF; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; STRUCTURAL PROTEOMICS; SUGAR INTAKE; TANDEM MASS SPECTROMETRY; ZYMOGRAPHY; ANIMAL; ANIMAL FOOD; CULEX; ENZYMOLOGY; FEMALE; GASTROINTESTINAL TRACT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY;

ANIMALIA; AVES; CANIS FAMILIARIS; CULEX PIPIENS QUINQUEFASCIATUS; CULICIDAE; HEXAPODA; INVERTEBRATA;

AMINO ACID SEQUENCE; ANIMAL FEED; ANIMALS; CULEX; FEMALE; GASTROINTESTINAL TRACT; GENE EXPRESSION REGULATION, ENZYMOLOGIC; INSECT PROTEINS; MOLECULAR SEQUENCE DATA; SERINE ENDOPEPTIDASES; SUCROSE;

EID: 84937045134     PISSN: None     EISSN: 17563305     Source Type: Journal    
DOI: 10.1186/s13071-015-0985-0     Document Type: Article

References (73)

1. Farajollahi A, Fonseca DM, Kramer LD, Kilpatrick AM. Bird biting mosquitoes and human disease: a review of the role of Culex Pipiens complex mosquitoes in epidemiology. Infect Genet Evol. 2011;11(7):1577-85.
2. Simpson JE, Hurtado PJ, Medlock J, Molaei G, Andreadis TG, Galvani AP, et al. Vector host-feeding preferences drive transmission of multi-host pathogens: West Nile virus as a model system. Proc Biol Sci. 2012;279(1730):925-33.
3. Kilpatrick AM, Randolph SE. Drivers, dynamics, and control of emerging vector-borne zoonotic diseases. Lancet. 2012;380(9857):1946-55.
4. Weaver SC, Reisen WK. Present and Future Arboviral Threats. Antiviral Res. 2010;85(2):328-45.
5. Richards SL, Lord CC, Pesko K, Tabachnick WJ. Environmental and biological factors influence Culex pipiens quinquefasciatus Say (Diptera: Culicidae) vector competence for West Nile virus. Am J Trop Med Hyg. 2010;83:126-34.
6. Reddy BN, Labbé P, Corbel V. Culex genome is not just another genome for comparative genomics. Parasit Vectors. 2012;5:63.
7. Arensburger P, Megy K, Waterhouse RM, Abrudan J, Amedeo P, Antelo B, et al. Sequencing of Culex quinquefasciatus establishes a platform for mosquito comparative genomics. Science. 2010;330(6000):86-8.
8. Bartholomay LC, Waterhouse RM, Mayhew GF, Campbell CL, Michel K, Zou Z, et al. Pathogenomics of Culex quinquefasciatus and Meta-Analysis of infection responses to diverse pathogens. Science. 2010;330(6000):88-90.
9. Kalhok SE, Tabak LM, Prosser DE, Brook W, Downe AE, White BN. Isolation sequencing and characterization of two cDNA clones coding for trypsin like enzymes from the midgut of Aedes aegypti. Insect Mol Biol. 1993;2(2):71-9.
10. Barillas-Mury C, Wells MA. Cloning and sequencing of the blood meal-induced late trypsin gene from the mosquito Aedes aegypti and characterization of the upstream regulatory region. Insect Mol Biol. 1993;2(1):7-12.
11. Noriega FG, Edgar KA, Bechet R, Wells MA. Midgut exopeptidases activities in the Aedes aegypti are induced by blood feeding. J Insect Physiol. 2002;48(2):205-12.
12. Isoe J, Rascón Jr AA, Kunz S, Miesfeld RL. Molecular Genetic Analysis of Midgut Serine Proteases inAedes aegyptiMosquitoes. Insect Biochem Mol Biol. 2009;39(12):903-12.
13. Rawlings ND, Waller M, Barrett AJ, Bateman A. MEROPS: the database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res. 2014;42:503-9.
14. Wu DD, Wang GD, Irwin DM, Zhang YP. A profound role for the expansion of trypsin-like serine protease family in the evolution of hematophagy in mosquito. Mol Biol Evol. 2009;26(10):2333-41.
15. Venancio TM, Cristofoletti PT, Ferreira C, Verjovski-Almeida S, Terra WR. The Aedes aegypti larval transcriptome: a comparative perspective with emphasis on trypsins and the domain structure of peritrophins. Insect Mol Biol. 2009;18(1):33-44.
16. Müller HM, Crampton JM, della Torre A, Sinden R, Crisanti A. Members of a trypsin gene family in Anopheles gambiae are induced in the gut by blood meal. EMBO J. 1993;12(7):2891-900.
17. Brackney DE, Isoe J, WCB 4th, Zamora J, Foy BD, Miesfelde RL, et al. Expression profiling and comparative analyses of seven midgut serine proteases from the yellow fever mosquito, Aedes aegypti. J Insect Physiol. 2010;56(7):736-44.
18. Graf R, Briegel H. The synthetic pathway of trypsin in the mosquito Aedes aegypti L. (Diptera: Culicidae) and in vitro stimulation in isolated midguts. Insect Biochemistry. 1989;19(2):129-37.
19. Felix CR, Betschart B, Billingsley PF, Freyvogel TA. Post-feeding induction of trypsin in the midgut of Aedes aegypti L. (Diptera: Culicidae) is separable into two cellular phases. Insect Biochemistry. 1991;21(2):197-203.
20. Müller HM, Catteruccia F, Vizioli J, della Torre A, Crisanti A. Constitutive and blood meal-induced trypsin genes in Anopheles gambiae. Exp Parasitol. 1995;81(3):371-85.
21. Noriega FG, Pennington JE, Barillas-Mury C, Wang XY, Wells MA. Early trypsin, an Aedes aegypti female specific protease, is post-transcriptionally regulated by the blood meal. Insect Mol Biol. 1996;5(1):25-9.
22. Dana AN, Hong YS, Kern MK, Hillenmeyer ME, Harker BW, Lobo NF, et al. Gene expression patterns associated with blood-feeding in the malaria mosquito Anopheles gambiae. BMC Genomics. 2005;6:5.
23. Zdobnov EM, von Mering C, Letunic I, Torrents D, Suyama M, Copley RR, et al. Comparative genome and proteome analysis of Anopheles gambiae and Drosophila melanogaster. Science. 2002;298(5591):149-59.
24. Rascón Jr AA, Gearin J, Isoe J, Miesfeld RL. In vitro activation and enzyme kinetic analysis of recombinant midgut serine proteases from the Dengue vector mosquito Aedes aegypti. BMC Biochem. 2011;12:43.
25. Brackney DE, Foy BD, Olson KE. The effects of midgut serine proteases on dengue virus type 2 infectivity of Aedes aegypti. Am J Trop Med Hyg. 2008;79(2):267-74.
26. Molina-Cruz A, Gupta L, Richardson J, Bennett K, Black 4th W, Barillas-Mury C. Effect of mosquito midgut trypsin activity on dengue-2 virus and dissemination in Aedes aegypti. Am J Trop Med Hyg. 2005;72(5):631-7.
27. Ludwig GV, Christensen BM, Yuill TM, Schultz KT. Enzyme processing of La Crosse virus glycoprotein G1: a bunyavirus-vector infection model. Virology. 1989;171(1):108-13.
28. Ludwig GV, Israel BA, Christensen BM, Yuill TM, Schultz KT. Role of La Crosse virus glycoproteins in attachment of virus to host cells. Virology. 1991;181(2):564-71.
29. Mertens PP, Burroughs JN, Walton A, Wellby MP, Fu H, O'Hara RS, et al. Enhanced infectivity of modified bluetongue virus particles for two insect cell lines and for two Culicoides vector species. Virology. 1996;217(2):582-93.
30. Xu G, Wilson W, Mecham J, Murphy K, Zhou EM, Tabachnick W. VP7: an attachment protein of bluetongue virus for cellular receptors in Culicoides variipennis. J Gen Virol. 1997;78:1617-23.
31. Shahabuddin M, Lemos FJ, Kaslow DC, Jacobs-Lorena M. Antibody-mediated inhibition of Aedes aegypti midgut trypsins blocks sporogonic development of Plasmodium gallinaceum. Infect Immun. 1996;64(3):739-43.
32. Dessens JT, Mendoza J, Claudianos C, Vinetz JM, Khater E, Hassard S, et al. Knockout of the Rodent Malaria Parasite Chitinase PbCHT1 reduces infectivity to mosquitoes. Infect Immun. 2001;69(6):4041-7.
33. Okuda K, de Souza Caroci A, Ribolla PE, de Bianchi AG, Bijovski AT. Functional morphology of adult female Culex quinquefasciatus midgut during blood digestion. Tissue Cell. 2002;34(3):210-9.
34. Borges-Veloso A, Saboia-Vahia L, Cuervo P, Pires RC, Britto C, Fernandes N, et al. Proteolytic profiling and comparative analyses of active trypsin-like serine peptidases in preimaginal stages of Culex quinquefasciatus. Parasit Vectors. 2012;5:123.
35. González-Caballero N, Rodríguez-Vega A, Dias-Lopes G, Valenzuela JG, Ribeiro JM, Carvalho PC, et al. Expression of the mevalonate pathway enzymes in the Lutzomyia longipalpis (Diptera: Psychodidae) sex pheromone gland demonstrated by an integrated proteomic approach. J Proteomics. 2014;96:117-32.
36. Keller A, Nesvizhskii AI, Kolker E, Aebersold R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem. 2002;74(20):5383-92.
37. Nesvizhskii AI, Keller A, Kolker E, Aebersold R. A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem. 2003;75(17):4646-58.
38. Carvalho PC, Yates Iii JR, Barbosa VC. Analyzing shotgun proteomic data with PatternLab for proteomics. Curr Protoc Bioinformatics. 2010;Chapter 13:Unit 13. 13.1-15.
39. Carvalho PC, Fischer JS, Xu T, Cociorva D, Balbuena TS, Valente RH, et al. Search engine processor: Filtering and organizing peptide spectrum matches. Proteomics. 2012;12(7):944-9.
40. Megy K, Emrich SJ, Lawson D, Campbell D, Dialynas E, Hughes DS, et al. VectorBase: improvements to a bioinformatics resource for invertebrate vector genomics. Nucleic Acids Res. 2012;40:729-34.
41. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol. 2011;7:539.
42. Sigrist CJ, de Castro E, Cerutti L, Cuche BA, Hulo N, Bridge A, et al. New and continuing developments at PROSITE. Nucleic Acids Res. 2013;41:D344-7.
43. Petersen TN, Brunak S, von Heijne G, Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods. 2011;8(10):785-6.
44. Blom N, Sicheritz-Pontén T, Gupta R, Gammeltoft S, Brunak S. Prediction of post-translational glycosylation and phosphorylation of proteins from the amino acid sequence. Proteomics. 2004;4(6):1633-49.
45. Steentoft C, Vakhrushev SY, Joshi HJ, Kong Y, Vester-Christensen MB, Schjoldager KT, et al. Precision mapping of the human O-GalNAc glycoproteome through SimpleCell technology. EMBO J. 2013;32(10):1478-88.
46. MacLean B, Tomazela DM, Shulman N, Chambers M, Finney GL, Frewen B, et al. Skyline: an open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics. 2010;26(7):966-8.
47. Soares TS, Watanabe RM, Lemos FJ, Tanaka AS. Molecular characterization of genes encoding trypsin-like enzymes from Aedes aegypti larvae and identification of digestive enzymes. Gene. 2011;489(2):70-5.
48. Vandooren J, Geurts N, Martens E, Van den Steen PE, Opdenakker G. Zymography methods for visualizing hydrolytic enzymes. Nat Methods. 2013;10(3):211-20.
49. D'Avila-Levy CM, Santos ALS, Cuervo P, De Jesus JB, Branquinha MH. Applications of Zymography (Substrate-SDS-PAGE) for Peptidase Screening in a Post-Genomic Era. In: Magdeldin S, editor. Gel Electrophoresis - Advanced Techniques. China: InTech; 2012. p. 265-88.
50. Nauen R, Sorge D, Sterner A, Borovsky D. TMOF-like factor controls the biosynthesis of serine proteases in the larval gut of Heliothis virescens. Arch Insect Biochem Physiol. 2001;47:169-80.
51. Dinglasan RR, Devenport M, Florens L, Johnson JR, McHugh CA, Donnelly-Doman M, et al. The Anopheles gambiae adult midgut peritrophic matrix proteome. Insect Biochem Mol Biol. 2009;39(2):125-34.
52. Mesquita-Rodrigues C, Saboia-Vahia L, Cuervo P, Levy CM, Honório NA, Domont GB, et al. Expression of Trypsin-like serine peptidases in pré-imaginal stages of Aedes aegypti (Diptera:Culicidae). Arch Insect Biochem Physiol. 2011;76(4):223-35.
53. Saboia-Vahia L, Cuervo P, Borges-Veloso A, de Souza NP, Britto C, Dias-Lopes G, et al. The midgut of Aedes albopictus females expresses active trypsin-like serine peptidases. Parasit Vectors. 2014;7:253.
54. Telleria EL, de Araújo AP, Secundino NF, d'Avila-Levy CM, Traub-Csekö YM. Trypsin-Like serine proteases in Lutzomyia longipalpis - expression, activity and possible modulation by Leishmania infantum chagasi. PLoS ONE. 2010;5(5):e10697.
55. Terra WR, Ferreira C. Insect digestive enzymes: properties, compartimentalization and function. Comp Biochem Physiol. 1994;109(1):1-62.
56. Roach JC, Wang K, Gan L, Hood L. The molecular evolution of the vertebrate trypsinogens. J Mol Evol. 1997;45(6):640-52.
57. Muhlia-Almazán A, Sánchez-Paz A, García-Carreño FL. Invertebrate trypsins: a review. J Comp Physiol B. 2008;178(6):655-72.
58. Lehane SM, Assinder SJ, Lehane MJ. Cloning, sequencing, temporal expression and tissue-specificity of two serine proteases from the midgut of the blood-feeding fly Stomoxys calcitrans. Eur J Biochem. 1998;254(2):290-6.
59. Neurath H. Evolution of proteolytic enzymes. Science. 1984;224(4647):350-7.
60. Kénesi E, Katona G, Szilágyi L. Structural and evolutionary consequences of unpaired cysteines in trypsinogen. Biochem Biophys Res Commun. 2003;309(4):749-54.
61. Lopes AR, Juliano MA, Marana SR, Juliano L, Terra WR. Substrate specificity of insect trypsins and the role of their subsites in catalysis. Insect Biochem Mol Biol. 2006;36(2):130-40.
62. Craik CS, Choo QL, Swift GH, Quinto C, MacDonald RJ, Rutter WJ. Structure of two related rat pancreatic trypsin genes. J Biol Chem. 1984;259(22):14255-64.
63. Klein B, Sellos D, Van Wormhoudt A. Genomic organisation and polymorphism of a crustacean trypsin multi-gene family. Gene. 1998;216(1):123-9.
64. Bao YY, Qin X, Yu B, Chen LB, Wang ZC, Zhang CX. Genomic insights into the serine protease gene family and expression profile analysis in the planthopper, Nilaparvata lugens. BMC Genomics. 2014;15:507.
65. Chen CC, Li WH, Sung HM. Patterns of internal gene duplication in the course of metazoan evolution. Gene. 2007;396(1):59-65.
66. Li L, Memon S, Fan Y, Yang S, Tan S. Recent duplications drive rapid diversification of trypsin genes in 12 Drosophila. Genetica. 2012;140(7-9):297-305.
67. Wang S, Magoulas C, Hickey D. Concerted evolution within a trypsin gene cluster in Drosophila. Mol Biol Evol. 1999;16(9):1117-24.
68. Lemos FJ, Cornel AJ, Jacobs-Lorena M. Trypsin and aminopeptidase gene expression is affected by age and food composition in Anopheles gambiae. Insect Biochem Mol Biol. 1996;26(7):651-8.
69. Dias-Lopes G, Borges-Veloso A, Saboia-Vahia L, Domont BG, Britto C, Cuervo P, et al. Expression of active trypsin-like serine peptidases in the midgut of sugar-feeding female Anopheles aquasalis. Parasit Vectors. 2015;8:296.
70. Moll RM, Romoser WS, Modrzakowski MC, Moncayo AC, Lerdthusnee K. Meconial peritrophic membranes and the fate of midgut bacteria during mosquito (Diptera: Culicidae) metamorphosis. J Med Entomol. 2001;38(1):29-32.
71. Robich RM, Denlinger DL. Diapause in the mosquito Culex pipiens evokes a metabolic switch from blood feeding to sugar gluttony. Proc Nat Acad Sci U S A. 2005;102(44):15912-7.
72. Prakash A, Tomazela DM, Frewen B, Maclean B, Merrihew G, Peterman S, et al. Expediting the development of targeted SRM assays: using data from shotgun proteomics to automate method development. J Proteome Res. 2009;8(6):2733-9.
73. Gallien S, Kim SY, Domon B: Large-Scale Targeted Proteomics Using Internal Standard Triggered-Parallel Reaction Monitoring. Mol Cell Proteomics 2015;doi: 10.1074/mcp.O114.043968.