P-glycoprotein ATPase from the resistant pest, Helicoverpa armigera: Purification, characterization and effect of various insecticides on its transport function

Biochimica et Biophysica Acta - Biomembranes

Volumn 1798, Issue 6, 2010, Pages 1135-1143

  Aurade, Ravindra M ^a   Jayalakshmi, Senigala K ^b   Sreeramulu, Kuruba ^a  

^a GULBARGA UNIVERSITY   (India)

^b AGRICULTURAL RESEARCH STATION   (India)

Author keywords

Drug transport; Helicoverpa armigera; Insecticides; P glycoprotein ATPase; Proteoliposomes; Tryptophan quenching

Indexed keywords

1,10 PHENANTHROLINE; ADENOSINE TRIPHOSPHATASE; BARIUM; CIPERMETHRIN; DOXORUBICIN; EDETIC ACID; EGTAZIC ACID; ENDOSULFAN; FENVALERATE; FLUORESCENT DYE; GLYCOPROTEIN P; INSECTICIDE; LEAD; MANGANESE CHLORIDE; MONOCROTOPHOS; MULTIDRUG RESISTANCE PROTEIN 1; N ETHYLMALEIMIDE; OUABAIN; PARAOXON; PARATHION; PARATHION METHYL; PROBENECID; SODIUM CHLORIDE; TRITON X 100; TRYPTOPHAN; UREA; VANADATE SODIUM; VANADIC ACID; VERAPAMIL;

ARTICLE; BINDING KINETICS; CONTROLLED STUDY; CROP PEST; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME KINETICS; ENZYME PURIFICATION; FLUORESCENCE ANALYSIS; GENETIC CONSERVATION; HELICOVERPA ARMIGERA; INSECTICIDE RESISTANCE; LEPIDOPTERA; MAMMAL; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; PH; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN TRANSPORT; PROTEOLIPOSOME; QUANTITATIVE ANALYSIS; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; TEMPERATURE;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; ANIMALS; DRUG RESISTANCE; HYDROGEN-ION CONCENTRATION; INSECT PROTEINS; INSECTICIDES; KINETICS; MAMMALS; MOTHS; P-GLYCOPROTEIN; SEQUENCE HOMOLOGY, AMINO ACID;

HELICOVERPA ARMIGERA; MAMMALIA;

EID: 77952550862     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2010.02.019     Document Type: Article

References (48)

1. Gunning R.V., Moores G.D., Devonshire A.L. Esterase inhibitors synergise the toxicity of pyrethroids in Australian Helicoverpa armigera (Lepidoptera: Noctuidae). Pest. Biochem. Physiol. 1999, 63:52-62.
2. Srinivas R., Udikeri S.S., Jayalakshmi S.K., Sreeramulu K. Identification of factors responsible for insecticide resistance in Helicoverpa armigera. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2004, 137:261-269.
3. Gunning R.V., Dang H.T., Kemp F.C., Nicholson I.C., Graham D.M. New resistance mechanism in Helicoverpa armigera threatens transgenic crops expressing Bacillus thuringiensis Cry1Ac toxin. Appl. Environ. Microbiol. 2005, 2558-2563.
4. Lanning C.L., Fine R.L., Corcoran J.J., Ayad H.M., Rose R.L., Abou-Donia M.B. Tobacco budworm P-glycoprotein: biochemical characterization and its involvement in pesticide resistance. Biochim. Biophys. Acta 1996, 1291:155-162.
5. Leslie E.M., Deeley R.G., Cole S.P.C. Multidrug resistance proteins: role of P glycoprotein, MRP1, MRP2, and BCRP (ABCG2) in tissue defense. Toxicol. Appl. Pharmacol. 2005, 204:216-237.
6. Jones P.M., George A.M. The ABC transporter structure and mechanism: perspectives on recent research. Cell. Mol. Life Sci. 2004, 61:682-699.
7. Gottesman M.M. Mechanisms of cancer drug resistance. Annu. Rev. Med. 2002, 53:615-627.
8. Robert J., Jarry C. Multidrug resistance reversal agents. J. Med. Chem. 2003, 46:4805-4817.
9. Sharom F.J., Yu X., Chu J.W.K., Doige C.A. Characterization of the ATPase activity of P-glycoprotein from multidrug- resistant Chinese hamster ovary cells. Biochem. J. 1995, 308:381-390.
10. Sharom F.J. The P-glycoprotein efflux pump: how does it transport drugs?. J. Membr. Biol. 1997, 160:161-175.
11. Prasad R., Murthy S.K., Prasad R., Gupta V., Lata S. Multidrug resistance: an emerging threat. Curr. Sci. 1996, 71:205-213.
12. Dassa E., Bouige P. The ABC of ABCs: a phylogenetic and functional classification of ABC systems in living organisms. Res. Microbiol. 2001, 152:211-229.
13. Bain L.J., LeBlanc G.A. Interaction of structurally diverse pesticides with the human MDR1 gene product P-glycoprotein. Toxicol. Appl. Pharmacol. 1996, 141:288-298.
14. Lanning C.L., Fine R.L., Sachs C.W., Rao U.S., Corcoran J.J., Abou-Donia M.B. Chlorpyrifos oxon interacts with the mammalian multidrug resistance protein, P-glycoprotein. J. Toxicol. Environ. Health 1996, 47:395-407.
15. Podsiadlowski L., Matha V., Vilcinskas A. Detection of a P-glycoprotein related pump in Chironomus larvae and its inhibition by verapamil and cyclosporin A. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 1998, 121:443-450.
16. Buss D.S., McCaffery A.R., Callaghan A. Evidence for p-glycoprotein modification of insecticide toxicity in mosquitoes of the Culex pipiens complex. Med. Vet. Entomol. 2002, 16:218-222.
17. Gaertner L.S., Murray C.L., Morris C.E. Transepithelial transport of nicotine and vinblastine in isolated malpighian tubules of the tobacco hornworm (Manduca sexta) suggests a P-glycoprotein-like mechanism. J. Exp. Biol. 1998, 201:2637-2645.
18. Murray C.L., Quaglia M., Arnason J.T., Morris C.E. A putative nicotine pump at the metabolic blood-brain barrier of the tobacco hornworm. J. Neurobiol. 1994, 25:23-34.
19. Leader J.P., O'Donnell M.J. Transepithelial transport of fluorescent p-glycoprotein and MRP2 substrates by insect malpighian tubules: confocal microscopic analysis of secreted fluid droplets. J. Exp. Biol. 2005, 208:4363-4376.
20. Ravindra A., Jayalakshmi S.K., Sreeramulu K. Stimulatory effect of insecticides on partially purified P-glycoprotein ATPase from the resistant pest Helicoverpa armigera. Biochem. Cell Biol. 2006, 84:1045-1050.
21. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 1951, 193:265-275.
22. Borgnia M.J., Eytan G.D., Assaraf Y.G. Competition of hydrophobic peptides, cytotoxic drugs, and chemosensitizers on a common P-glycoprotein pharmacophore as revealed by its ATPase activity. J. Biol. Chem. 1996, 271:3163-3171.
23. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London) 1970, 227:680-685.
24. Gerard C. Purification of glycoproteins. Methods Enzymol. 1990, 182:529-539.
25. Wilkinson G.N. Statistical estimations in enzyme kinetics. Biochem. J. 1961, 80:324.
26. Liu R., Siemiarczuk A., Sharom F.J. Intrinsic fluorescence of the P-glycoprotein multidrug transporter: sensitivity of tryptophan residues to binding of drugs and nucleotides. Biochemistry 2000, 39:14927-14938.
27. Lu P., Liu R., Sharom F.J. Drug transport by reconstituted P-glycoprotein in proteoliposomes-effect of substrates and modulators, and dependence on bilayer phase state. Eur. J. Biochem. 2001, 268:1687-1697.
28. Eytan G.D., Regev R., Oren G., Hurwitz C.D., Assaraf Y.G. Efficiency of P-glycoprotein-mediated exclusion of rhodamine dyes from multidrug resistant cells is determined by their passive transmembrane movement rate. Eur. J. Biochem. 1997, 248:104-112.
29. Shapiro A.B., Ling V. ATPase activity of purified and reconstituted P-glycoprotein from Chinese hamster ovary cells. J. Biol. Chem. 1994, 269:3745-3754.
30. Mao Q., Scarborough G.A. Purification of functional human P-glycoprotein expressed in Saccharomyces cerevisiae. Biochim. Biophys. Acta 1997, 1327:107-118.
31. Ramachandra M., Ambudkar S.V., Chen D., Hrycyna C.A., Dey S., Gottesman M.M., Pastan I. Human P-glycoprotein exhibits reduced affinity for substrates during a catalytic transition state. Biochemistry 1998, 37:5010-5019.
32. Sharom F.J., Yu X., Doige C.A. Functional reconstitution of drug transport and ATPase activity in proteoliposomes containing partially purified P-glycoprotein. J. Biol. Chem. 1993, 268:24197-24202.
33. Sreeramulu K., Liu R., Sharom F.J. Interaction of insecticides with mammalian P-glycoprotein and their effect on its transport function. Biochim. Biophys. Acta 2007, 1768:1750-1757.
34. Ambudkar S.V. Purification and reconstitution of functional human P-glycoprotein. J. Bioenerg. Biomembr. 1995, 27:23-29.
35. Al-Shawi M.K., Urbatsch I.L., Senior A.E. Covalent inhibitors of P-glycoprotein ATPase activity. J. Biol. Chem. 1994, 269:8986-8992.
36. Loo T.W., Clarke D.M. Covalent modification of human P-glycoprotein mutants containing a single cysteine in either nucleotide-binding fold abolishes drug stimulated ATPase activity. J. Biol. Chem. 1995, 270:22957-22961.
37. Smith P.C., Karpowich N., Millen L., Moody J.E., Rosen J., Thomas P.J., Hunt J.F. ATP binding to the motor domain from an ABC transporter drives formation of a nucleotide sandwich dimer. Mol. Cell 2002, 10:139-149.
38. Locher K.P., Lee A.T., Rees D.C. The E. coli BtuCD structure: a framework for ABC transporter architecture and mechanism. Science 2002, 296:1091-1098.
39. Chang G. Structure of MsbA from Vibrio cholera: a multidrug resistance ABC transporter homolog in a closed conformation. J. Mol. Biol. 2003, 330:419-430.
40. Takada Y., Yamada K., Taguchi Y., Kino K., Matsuo M., Tucker S.J., Komano T., Amachi T., Ueda K. Non-equivalent cooperation between the two nucleotide-binding folds of P-glycoprotein. Biochim. Biophys. Acta 1998, 1373:131-136.
41. Urbatsch I.L., Beaudet L., Carrier I., Gros P. Mutations in either nucleotide-binding site of P-glycoprotein (Mdr3) prevent vanadate trapping of nucleotide at both sites. Biochemistry 1998, 37:4592-4602.
42. Couture L., Nash J.A., Turgeon J. The ATP-binding cassette transporters and their implication in drug disposition: a special look at the heart. Pharmacol. Rev. 2006, 58:244-258.
43. Gottesman M.M., Pastan I. The multidrug transporter a double edged sword. J. Biol. Chem. 1998, 263:12163-12166.
44. Sharom F.J., Liu R., Qu Q., Romsicki Y. Exploring the structure and function of the p-glycoprotein multidrug transporter using fluorescence spectroscopic tools. Semin. Cell Dev. Biol. 2001, 12:257-266.
45. Pivcevic B., Zaja R. Pesticides and their binary combinations as P-glycoprotein inhibitors in NIH 3T3/MDR1 cells. Environ. Toxicol. Pharmacol. 2006, 22:268-276.
46. Porretta D., Gargani M., Bellini R., Medici A., Punelli F., Urbanelli S. Defence mechanisms against insecticides temephos and diflubenzuron in the mosquito Aedes caspius: the P-glycoprotein efflux pumps. Med. Vet. Entmol. 2008, 22:48-54.
47. Bourguinat C., Ardelli B.F., Pion S.D., Kamgno J., Gardon J., Duke B.O., Boussinesq M., Prichard R.K. P-glycoprotein-like protein, a possible genetic marker for ivermectin resistance selection in Onchocerca volvulus. Mol. Biochem. Parasitol. 2008, 158:101-111.
48. Kuhne A., Tzvetkov M.V., Hagos Y., Lage H., Burckhardt G., Brockmoller J. Influx and efflux transport as determinants of melphalan cytotoxicity: resistance to melphalan in MDR1 overexpressing tumor cell lines. Biochem. Pharmacol. 2009, 78:45-53.