Expression of trypsin-like serine peptidases in pre-imaginal stages of Aedes aegypti (Diptera: Culicidae)

Archives of Insect Biochemistry and Physiology

Volumn 76, Issue 4, 2011, Pages 223-235

  Mesquita Rodrigues, Camila ^a   Saboia Vahia, Leonardo ^a   Cuervo, Patrícia ^a   Masini d'Avila Levy, Claudia ^a   Alves Honorio, Nildimar ^a   Domont, Gilberto Barbosa ^b   Batista de Jesus, Jose ^a  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

Aedes aegypti; Protease; Trypsin like serine protease; Zymographic analysis.

Indexed keywords

1,10 PHENANTHROLINE; 1,10-PHENANTHROLINE; BENZYLSULFONYL FLUORIDE; PEPSTATIN; PHENANTHROLINE DERIVATIVE; PROTEINASE INHIBITOR; SERINE PROTEINASE; TOSYLLYSYL CHLOROMETHYL KETONE; TOSYLPHENYLALANYL CHLOROMETHYL KETONE; TRYPSIN LIKE SERINE PROTEASE; TRYPSIN-LIKE SERINE PROTEASE;

AEDES; ANIMAL; ARTICLE; BIOSYNTHESIS; COMPARATIVE STUDY; ENZYMOLOGY; INSECT; ISOLATION AND PURIFICATION; LARVA; METABOLISM; MOLECULAR WEIGHT;

AEDES; ANIMALS; LARVA; MOLECULAR WEIGHT; PEPSTATINS; PHENANTHROLINES; PHENYLMETHYLSULFONYL FLUORIDE; PROTEASE INHIBITORS; PUPA; SERINE ENDOPEPTIDASES; TOSYLLYSINE CHLOROMETHYL KETONE; TOSYLPHENYLALANYL CHLOROMETHYL KETONE;

AEDES AEGYPTI; CULICIDAE; DIPTERA;

EID: 79952652954     PISSN: 07394462     EISSN: 15206327     Source Type: Journal    
DOI: 10.1002/arch.20412     Document Type: Article

References (50)

1. Abraham EG, Pinto SB, Ghosh A, Vanlandingham DL, Budd A, Higgs S, Kafatos FC, Jacobs-Lorena M, Michel K. 2005. An immune-responsive serpin, SRPN6, mediates mosquito defense against malaria parasites. Proc Natl Acad Sci USA 102:16327-16332.
2. Angulo-Valadez CE, Cepeda-Palacios R, Ascencio F, Jacquiet P, Dorchies P, Romero MJ, Khelifa RM. 2007. Proteolytic activity in salivary gland products of sheep bot fly (Oestrus ovis) larvae. Vet Parasitol 149:117-125.
3. Borovsky D, Mahmood F. 1995. Feeding the mosquito Aedes aegypti with TMOF and its analogs; effect on trypsin biosynthesis and egg development. Regul Pept 57:273-281.
4. Borovsky D, Meola SM. 2004. Biochemical and cytoimmunological evidence for the control of Aedes aegypti larval trypsin with Aea-TMOF. Arch Insect Biochem Physiol 55:124-139.
5. Cho WL, Tsao SM, Hays AR, Walter R, Chen JS, Snigirevskaya ES, Raikhel AS. 1999. Mosquito cathepsin B-like protease involved in embryonic degradation of vitellin is produced as a latent extraovarian precursor. J Biol Chem 274:13311-13321.
6. Cuervo P, Mesquita-Rodrigues C, d'Avila Levy CM, Britto C, Pires FA, Gredilha R, Alves CR, De Jesus JB. 2008. Serine protease activities in Oxysarcodexia thornax (Walker) (Diptera: Sarcophagidae) first instar larva. Mem Inst Oswaldo Cruz 103:504-506.
7. de Lima-Camara TN, Honório NA, Lourenço-de-Oliveira R. 2006. Frequency and spatial distribution of Aedes aegypti and Aedes albopictus (Diptera: Culicidae) in Rio de Janeiro, Brazil. Cad Saude Publica 22:2079-2084.
8. De Jesus JB, Cuervo P, Britto C, Sabóia-Vahia L, Silva-Filho FC, Borges-Veloso A, Petrópolis DB, Cupolillo E, Domont GB. 2009. Cysteine peptidase expression in Trichomonas vaginalis isolates displaying high and low virulence phenotypes. J Proteome Res 8:1555-1564.
9. Elpidina EN, Tsybina TA, Dunaevsky YE, Belozersky MA, Zhuzhikov DP, Oppert B. 2005. A chymotrypsin-like proteinase from the midgut of Tenebrio molitor larvae. Biochimie 87:771-779.
10. Fazito do Vale V, Pereira MH, Gontijo NF. 2007. Midgut pH profile and protein digestion in the larvae of Lutzomyia longipalpis (Diptera: Psychodidae). J Insect Physiol 53:1151-1159.
11. Graf R, Briegel H. 1989. The synthetic pathway of trypsin in the mosquito Aedes aegypti (L.) (Diptera: Culicidae) and in vitro stimulation in isolated midguts. Insect Biochem 19:129-137.
12. Graf R, Raikhel AS, Brown MR, Lea AO, Briegel H. 1986. Mosquito trypsin: immunocytochemical localization in the midgut of blood-fed Aedes aegypti (L.). Cell Tissue Res 245:19-27.
13. Gong M, Shen B, Gu Y, Tian H, Ma L, Li X, Yang M, Hu Y, Sun Y, Hu X, Li J, Zhu C. 2005. Serine proteinase over-expression in relation to deltamethrin resistance in Culex pipiens pallens. Arch Biochem Biophys 438:53-62.
14. Gubler DJ. 2002. Epidemic dengue/dengue hemorrhagic fever as a public health, social and economic problem in the 21st century. Trends Microbiol 10:100-103.
15. Han YS, Salazar CE, Reese-Stardy SR, Cornel A, Gorman MJ, Collins FH, Paskewitz SM. 1997. Cloning and characterization of a serine protease from the human malaria vector, Anopheles gambiae. Insect Mol Biol 6:385-395.
16. Ho BC, Khoo HG, Chew LM, Wong KP, Ewert A. 1992. Food ingestion and digestive enzymes in larval Aedes aegypti and Aedes albopictus (Diptera: Culicidae). J Med Entomol 29:960-964.
17. Honório NA, Silva C, Leite PJ, Gonçalves JM, Lounibos LP, Lourenço-de-Oliveira R. 2003. Dispersal of Aedes aegypti and Aedes albopictus (Diptera: Culicidae) in an urban endemic dengue area in the State of Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz 98:191-198.
18. Kaur P, Ponniah M, Murhekar MV, Ramachandran V, Ramachandran R, Raju HK, Perumal V, Mishra AC, Gupte MD. 2008. Chikungunya outbreak, South India, 2006. Emerg Infect Dis 14:1623-1625.
19. Lourenço-de-Oliveira R, Vazeille M, de Filippis AM, Failloux AB. 2004. Aedes aegypti in Brazil: genetically differentiated populations with high susceptibility to dengue and yellow fever viruses. Trans R Soc Trop Med Hyg 98:43-54.
20. Maciel-de-Freitas R, Neto RB, Gonçalves JM, Codeço CT, Lourenço-de-Oliveira R. 2006. Movement of dengue vectors between the human modified environment and an urban forest in Rio de Janeiro. J Med Entomol 43:1112-1120.
21. Mahmood F, Borovsky D. 1992. Biosynthesis of trypsinlike and chymotrypsinlike enzymes in immature Lutzomyia anthophora (Diptera: Psychodidae). J Med Entomol 29:489-495.
22. Maidana NA, Yang HM. 2008. Describing the geographic spread of dengue disease by traveling waves. Math Biosci 215:64-77.
23. Nakajima Y, Tsuji Y, Homma K, Natori S. 1997. A novel protease in the pupal yellow body of Sarcophaga peregrina (flesh fly). Its purification and cDNA cloning. J Biol Chem 272:23805-23810.
24. Nauen R, Sorge D, Sterner A, Borovsky D. 2001. TMOF-like factor controls the biosynthesis of serine proteases in the larval gut of Heliothis virescens. Arch Insect Biochem Physiol 47:169-180.
25. Nene V, Wortman JR, Lawson D, Haas B, Kodira C, Tu ZJ, Loftus B, Xi Z, Megy K, Grabherr M, Ren Q, Zdobnov EM, Lobo NF, Campbell KS, Brown SE, Bonaldo MF, Zhu J, Sinkins SP, Hogenkamp DG, Amedeo P, Arensburger P, Atkinson PW, Bidwell S, Biedler J, Birney E, Bruggner RV, Costas J, Coy MR, Crabtree J, Crawford M, Debruyn B, Decaprio D, Eiglmeier K, Eisenstadt E, El-Dorry H, Gelbart WM, Gomes SL, Hammond M, Hannick LI, Hogan JR, Holmes MH, Jaffe D, Johnston JS, Kennedy RC, Koo H, Kravitz S, Kriventseva EV, Kulp D, Labutti K, Lee E, Li S, Lovin DD, Mao C, Mauceli E, Menck CF, Miller JR, Montgomery P, Mori A, Nascimento AL, Naveira HF, Nusbaum C, O'leary S, Orvis J, Pertea M, Quesneville H, Reidenbach KR, Rogers YH, Roth CW, Schneider JR, Schatz M, Shumway M, Stanke M, Stinson EO, Tubio JM, Vanzee JP, Verjovski-Almeida S, Werner D, White O, Wyder S, Zeng Q, Zhao Q, Zhao Y, Hill CA, Raikhel AS, Soares MB, Knudson DL, Lee NH, Galagan J, Salzberg SL, Paulsen IT, Dimopoulos G, Collins FH, Birren B, Fraser-Liggett CM, Severson DW. 2007. Genome sequence of Aedes aegypti, a major arbovirus vector. Science 316:1718-1723.
26. Nogueira RM, Miagostovich MP, Schatzmayr HG. 2000. Molecular epidemiology of dengue viruses in Brazil. Cad Saude Publica 16:205-211.
27. Noriega FG, Wells MA. 1999. A molecular view of trypsin synthesis in the midgut of Aedes aegypti. J Insect Physiol 45:613-620.
28. Noriega FG, Wang XY, Pennington JE, Barillas-Mury CV, Wells MA. 1996. Early trypsin, a female-specific midgut protease in Aedes aegypti: isolation, aminoterminal sequence determination, and cloning and sequencing of the gene. Insect Biochem Mol Biol 26:119-126.
29. Noriega FG, Edgar KA, Bechet R, Wells MA. 2002. Midgut exopeptidase activities in Aedes aegypti are induced by blood feeding. J Insect Physiol 48:205-212.
30. Okuda K, Caroci A, Ribolla P, Marinotti O, de Bianchi AG, Bijovsky AT. 2005. Morphological and enzymatic analysis of the midgut of Anopheles darlingi during blood digestion. J Insect Physiol 51:769-776.
31. PAHO. 2008.
32. Philip JM, Fitches E, Harrison RL, Bonning B, Gatehouse JA. 2007. Characterisation of functional and insecticidal properties of a recombinant cathepsin L-like proteinase from flesh fly (Sarcophaga peregrina), which plays a role in differentiation of imaginal discs. Insect Biochem Mol Biol 37:589-600.
33. Pires FA, Moya-Borja GE, Barreira JD, Pinho RT, Alves CR. 2007. The main proteinases in Dermatobia hominis second and third instars larvae are serine-proteinases. Vet Parasitol 145:326-331.
34. Ríos-Velásquez CM, Codeço CT, Honório NA, Sabroza PS, Moresco M, Cunha IC, Levino A, Toledo LM, Luz SL. 2007. Distribution of dengue vectors in neighborhoods with different urbanization types of Manaus, state of Amazonas, Brazil. Mem Inst Oswaldo Cruz 102:617-623.
35. Rodrigues J, Agrawal N, Sharma A, Malhotra P, Adak T, Chauhan VS, Bhatnagar RK. 2007. Transcriptional analysis of an immune-responsive serine protease from Indian malarial vector, Anopheles culicifacies. BMC Mol Biol 8:33.
36. Rosenfeld A, Vanderberg JP. 1998. Identification of electrophoretically separated proteases from midgut and hemolymph of adult Anopheles stephensi mosquitoes. J Parasitol 84:361-365.
37. Shope R. 1991. Global climate change and infectious diseases. Environ Health Perspect 96:171-174.
38. Tabouret G, Bret-Bennis L, Dorchies P, Jacquiet P. 2003. Serine protease activity in excretory-secretory products of Oestrus ovis (Diptera: Oestridae) larvae. Vet Parasitol 114:305-314.
39. Terra WR, Ferreira C. 1994. Insect digestive enzymes: properties, compartmentalization and function. Comp Biochem Physiol 109:1-62.
40. Troyo A, Calderón-Arguedas O, Fuller DO, Solano ME, Avendaño A, Arheart KL, Chadee DD, Beier JC. 2008. Seasonal profiles of Aedes aegypti (Diptera: Culicidae) larval habitats in an urban area of Costa Rica with a history of mosquito control. J Vector Ecol 33:76-88.
41. Tsybina TA, Dunaevsky YE, Belozersky MA, Zhuzhikov DP, Oppert B, Elpidina EN. 2005. Digestive proteinases of yellow mealworm (Tenebrio molitor) larvae: purification and characterization of a trypsin-like proteinase. Biochemistry 70:300-305.
42. Vasilakis N, Weaver SC. 2008. The history and evolution of human dengue emergence. Adv Virus Res 72:1-76.
43. Vierstraete E, Cerstiaens A, Baggerman G, Van den Bergh G, De Loof A, Schoofs L 2003. Proteomics in Drosophila melanogaster: first 2D database of larval hemolymph proteins. Biochem Biophys Res Commun 304:831-838.
44. WHO. 2008.
45. Wilder-Smith A, Gubler DJ. 2008. Geographic expansion of dengue: the impact of international travel. Med Clin North Am 92:1377-1390.
46. Yang YJ, Davies DM. 1971. Trypsin and chymotrypsin during metamorphosis in Aedes aegypti and properties of the chymotrypsin. J Insect Physiol 17:117-131.
47. Yang YJ, Davies DM. 1972. The effect of cations on chymotrypsin from Aedes aegypti larvae. J Insect Physiol 18:747-755.
48. Yano T, Takahashi N, Kurata S, Natori S. 1995. Regulation of the expression of cathepsin B in Sarcophaga peregrina (flesh fly) at the translational level during metamorphosis. Eur J Biochem 234:39-43.
49. Zhao Z, Russell PJ. 2003. Trypsin activity assay in substrate-specific one- and two-dimensional gels: a powerful method to separate and characterize novel proteases in active form in biological samples. Electrophoresis 24:3284-3288.
50. Zhao Z, Raftery MJ, Niu XM, Daja MM, Russell PJ. 2004. Application of in-gel protease assay in a biological sample: characterization and identification of urokinase-type plasminogen activator (uPA) in secreted proteins from a prostate cancer cell line PC-3. Electrophoresis 25:1142-1148.