Molecular characterization of the carboxypeptidase B1 of anopheles stephensi and its evaluation as a target for transmission-blocking vaccines

Infection and Immunity

Volumn 81, Issue 6, 2013, Pages 2206-2216

  Raz, Abbasali ^a   Djadid, Navid Dinparast ^a   Zakeri, Sedigheh ^a  

^a PASTEUR INSTITUTE OF IRAN   (Iran)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOXYPEPTIDASE; CARBOXYPEPTIDASE B1; MESSENGER RNA; TRANSMISSION BLOCKING VACCINE; UNCLASSIFIED DRUG; VACCINE;

ANIMAL CELL; ANOPHELES STEPHENSI; ARTICLE; BIOLOGICAL ACTIVITY; CONTROLLED STUDY; ENZYME ANALYSIS; GAMETOCYTE; GENE SEQUENCE; GENOMICS; IN VITRO STUDY; INFECTION RATE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; RNA SEQUENCE; SEXUAL DEVELOPMENT; STRUCTURE ANALYSIS; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ANIMALS; ANOPHELES; BASE SEQUENCE; CARBOXYPEPTIDASE B; FEMALE; GASTROINTESTINAL TRACT; GENE EXPRESSION REGULATION, ENZYMOLOGIC; INSECT PROTEINS; INSECT VECTORS; MALARIA; MALARIA VACCINES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PLASMODIUM FALCIPARUM; PROTEIN CONFORMATION;

EID: 84877821232     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01331-12     Document Type: Article

References (46)

1. malERA Consultative Group on Vaccines. 2011. A research agenda for malaria eradication: vaccines. PLoS Med. 8:e1000398. doi:10.1371/journal .pmed.1000398.
2. Duffy PE, Kaslow DC. 1997. A novel malaria protein, Pfs28, and Pfs25 are genetically linked and synergistic as falciparum malaria transmissionblocking vaccines. Infect. Immun. 65:1109-1113.
3. Hisaeda H, Yasutomo K. 2002. Development of malaria vaccines that block transmission of parasites by mosquito vectors. J. Med. Invest. 49: 118-123.
4. Kaslow DC. 1997. Transmission-blocking vaccines: uses and current status of development. Int. J. Parasitol. 27:183-189.
5. Kaslow DC. 2002. Transmission-blocking vaccines. Chem. Immunol. 80: 287-307.
6. Tsuboi T, Tachibana M, Kaneko O, Torii M. 2003. Transmissionblocking vaccine of vivax malaria. Parasitol. Int. 52:1-11.
7. Dinglasan RR, Fields I, Shahabuddin M, Azad AF, Sacci JB, Jr. 2003. Monoclonal antibody MG96 completely blocks Plasmodium yoelii development in Anopheles stephensi. Infect. Immun. 71:6995-7001.
8. Lal AA, Patterson PS, Sacci JB, Vaughan JA, Paul C, Collins WE, Wirtz RA, Azad AF. 2001. Anti-mosquito midgut antibodies block development of Plasmodium falciparum and Plasmodium vivax in multiple species of Anopheles mosquitoes and reduce vector fecundity and survivorship. Proc. Natl. Acad. Sci. U. S. A. 98:5228-5233.
9. Shahabuddin M, Lemos FJ, Kaslow DC, Jacobs-Lorena M. 1996. Antibody- mediated inhibition of Aedes aegypti midgut trypsins blocks sporogonic development of Plasmodium gallinaceum. Infect. Immun. 64:739-743.
10. Srikrishnaraj KA, Ramasamy R, Ramasamy MS. 1995. Antibodies to Anopheles midgut reduce vector competence for Plasmodium vivax malaria. Med. Vet. Entomol. 9:353-357.
11. Lavazec C, Boudin C, Lacroix R, Bonnet S, Diop A, Thiberge S, Boisson B, Tahar R, Bourgouin C. 2007. Carboxypeptidases B of Anopheles gambiae as targets for a Plasmodium falciparum transmission-blocking vaccine. Infect. Immun. 75:1635-1642.
12. Bonnet S, Prevot G, Jacques JC, Boudin C, Bourgouin C. 2001. Transcripts of the malaria vector Anopheles gambiae that are differentially regulated in the midgut upon exposure to invasive stages of Plasmodium falciparum. Cell. Microbiol. 3:449-458.
13. Lavazec C, Bonnet S, Thiery I, Boisson B, Bourgouin C. 2005. cpbAg1 encodes an active carboxypeptidase B expressed in the midgut of Anopheles gambiae. Insect Mol. Biol. 14:163-174.
14. Titani K, Ericsson LH, Walsh KA, Neurath H. 1975. Amino-acid sequence of bovine carboxypeptidase B. Proc. Natl. Acad. Sci. U. S. A. 72: 1666-1670.
15. Gardell SJ, Craik CS, Clauser E, Goldsmith EJ, Stewart CB, Graf M, Rutter WJ. 1988. A novel rat carboxypeptidase, CPA2: characterization, molecular cloning, and evolutionary implications on substrate specificity in the carboxypeptidase gene family. J. Biol. Chem. 263:17828-17836.
16. Bown DP, Gatehouse JA. 2004. Characterization of a digestive carboxypeptidase from the insect pest corn earworm (Helicoverpa armigera) with novel specificity towards C-terminal glutamate residues. Eur. J. Biochem. 271:2000-2011.
17. Edwards MJ, Lemos FJ, Donnelly-Doman M, Jacobs-Lorena M. 1997. Rapid induction by a blood meal of a carboxypeptidase gene in the gut of the mosquito Anopheles gambiae. Insect Biochem. Mol. Biol. 27:1063-1072.
18. 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.
19. Ramos A, Mahowald A, Jacobs-Lorena M. 1993. Gut-specific genes from the black fly Simulium vittatum encoding trypsin-like and carboxypeptidase- like proteins. Insect Mol. Biol. 1:149-163.
20. Gooding RH. 1977. Digestive processes of haematophagous insects. XIV. Haemolytic activity in the midgut of Glossina morsitans morstians Westwood (Diptera: Glossinidae). Can. J. Zool. 55:1899-1905.
21. Moskalyk LA. 1998. Carboxypeptidase B in Anopheles gambiae (Diptera: Culicidae): effects of abdominal distention and blood ingestion. J. Med. Entomol. 35:216-221.
22. Yan J, Cheng Q, Li CB, Aksoy S. 2002. Molecular characterization of three gut genes from Glossina morsitans morsitans: cathepsin B, zincmetalloprotease and zinc-carboxypeptidase. Insect Mol. Biol. 11:57-65.
23. Scotto-Lavino E, Du G, Frohman MA. 2006. 3= end cDNA amplification using classic RACE. Nat. Protoc. 1:2742-2745.
24. Djadid ND, Barjesteh H, Raeisi A, Hassanzahi A, Zakeri S. 2006. Identification, sequence analysis, and comparative study on GSTe2 insecticide resistance gene in three main world malaria vectors: Anopheles stephensi, Anopheles culicifacies, and Anopheles fluviatilis. J. Med. Entomol. 43:1171-1177.
25. Djadid ND, Gholizadeh S, Aghajari M, Zehi AH, Raeisi A, Zakeri S. 2006. Genetic analysis of rDNA-ITS2 and RAPD loci in field populations of the malaria vector, Anopheles stephensi (Diptera: Culicidae): implications for the control program in Iran. Acta Trop. 97:65-74.
26. Jackson LR, Fox JG. 1995. Institutional policies and guidelines on adjuvants and antibody production. ILAR J. 37:141-152.
27. Ventura S, Villegas V, Sterner J, Larson J, Vendrell J, Hershberger CL, Aviles FX. 1999. Mapping the pro-region of carboxypeptidase B by protein engineering. Cloning, overexpression, and mutagenesis of the porcine proenzyme. J. Biol. Chem. 274:19925-19933.
28. Sun S-W, Lin Y-C, Weng Y-M, Chen M-J. 2006. Efficiency improvements on ninhydrin method for amino acid quantification. J. Food Compos. Anal. 19:112-117.
29. Jensen JB. 1979. Observations on gametogenesis in Plasmodium falciparum from continuous culture. J. Protozool. 26:129-132.
30. Trager W, Jensen JB. 1976. Human malaria parasites in continuous culture. Science 193:673-675.
31. Hyde JE (ed). 1993. Methods in molecular biology, vol 21. Protocols in molecular parasitology. Humana Press Inc, New York, NY.
32. Lambros C, Vanderberg JP. 1979. Synchronization of Plasmodium falciparum erythrocytic stages in culture. J. Parasitol. 65:418-420.
33. Fivelman QL, McRobert L, Sharp S, Taylor CJ, Saeed M, Swales CA, Sutherland CJ, Baker DA. 2007. Improved synchronous production of Plasmodium falciparum gametocytes in vitro. Mol. Biochem. Parasitol. 154:119-123.
34. Carter R, Miller LH. 1979. Evidence for environmental modulation of gametocytogenesis in Plasmodium falciparum in continuous culture. Bull. World Health Organ. 57(Suppl 1):37-52.
35. Xi Z, Das S, Garver L, Dimopoulos G. 2007. Protocol for Plasmodium falciparum infections in mosquitoes and infection phenotype determination. J. Vis. Exp. 2007(5):222. doi:10.3791/222.
36. Tchuinkam T, Mulder B, Dechering K, Stoffels H, Verhave JP, Cot M, Carnevale P, Meuwissen JH, Robert V. 1993. Experimental infections of Anopheles gambiae with Plasmodium falciparum of naturally infected gametocyte carriers in Cameroon: factors influencing the infectivity to mosquitoes. Trop. Med. Parasitol. 44:271-276.
37. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT. 2009. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 55:611-622.
38. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402-408.
39. Clauser E, Gardell SJ, Craik CS, MacDonald RJ, Rutter WJ. 1988. Structural characterization of the rat carboxypeptidase A1 and B genes. Comparative analysis of the rat carboxypeptidase gene family. J. Biol. Chem. 263:17837-17845.
40. Alter GM, Leussing DL, Neurath H, Vallee BL. 1977. Kinetic properties of carboxypeptidase B in solutions and crystals. Biochemistry 16:3663-3668.
41. Bradley G, Naude RJ, Muramoto K, Yamauchi F, Oelofsen W. 1996. Ostrich (Struthio camelus) carboxypeptidase B: purification, kinetic properties and characterization of the pancreatic enzyme. Int. J. Biochem. Cell Biol. 28:521-529.
42. Marinkovic DV, Marinkovic JN, Erdos EG, Robinson CJ. 1977. Purification of carboxypeptidase B from human pancreas. Biochem. J. 163:253-260.
43. Allary M, Schrevel J, Florent I. 2002. Properties, stage-dependent expression and localization of Plasmodium falciparum M1 family zincaminopeptidase. Parasitology 125:1-10.
44. Lavazec C, Bourgouin C. 2008. Mosquito-based transmission blocking vaccines for interrupting Plasmodium development. Microbes Infect. 10: 845-849.
45. Tan AK, Eaton DL. 1995. Activation and characterization of procarboxypeptidase B from human plasma. Biochemistry 34:5811-5816.
46. Vaughan JA, Noden BH, Beier JC. 1992. Population dynamics of Plasmodium falciparum sporogony in laboratory-infected Anopheles gambiae. J. Parasitol. 78:716-724.