Abstract
Apolipophorin III (apoLp-III) from insects and apolipoprotein A-I from humans, are major component of the lipoprotein and share various properties. ApoLp-III is an abundant hemolymph protein. Besides its crucial role in lipid transport, apoLp-III is able to associate with fungal and bacterial membranes and stimulate cellular immune responses. ApoLp-III was isolated and purified from the hemolymph of desert locust Schistocerca gregaria by ion-exchange and reversed-phase chromatography. The purity and the molecular weight of apoLp-III were determined at ∼19,000 Da by sodium dodecyl sulfate-polyacrylamide gel electrophoresis. According to similarities in the amino terminal sequence, molar mass and retention on reversed-phase analytical HPLC column, this protein is a Schistocerca gregaria homologue of Locusta migratoria apoLp-III.
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Abbreviations
- kDa:
-
Kilodalton
- TFA:
-
Trifluoroacetic acid
- PMSF:
-
Phenylmethylsulfonyl fluoride
- TPCK:
-
N-Tosyl-phenylalanyl chloromethyl ketone
- DTT:
-
Dithiothreitol
- SGCI:
-
Schistocerca gregaria chymotrypsin inhibitor
- MUTMAC:
-
4-Methylumbelliferyl p-(NNN-trimethylammonium)cinnamate
- MUB:
-
4-Methylubelliferone
- AMC:
-
7-Amino-4-methyl-coumarin
References
Alexenizer, M., & Dorn, A. (2007). Screening of medicinal and ornamental plants for insecticidal and growth regulating activity. Journal of Pesticide Science, 80, 205–215.
Baker, S. E., Hopkins, R. C., Blanchette, C. D., Walsworth, V. L., Sumbad, R., Fischer, N. O., et al. (2009). Hydrogen production by a hyperthermophilic membrane-bound hydrogenase in water-soluble nanolipoprotein particles. Journal of the American Chemical Society, 10(22), 7508–7509. 131.
Bradford, M. R. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72, 248–254.
Chino, H., Downer, R. G. H., Wyatt, G. R., & Gilbert, L. I. (1981). Lipophorins, a major class of lipoprotein of insect hemolymph. Insect Biochemistry, 11, 491.
Chung, K. T., & Ourth, D. D. (2002). Purification and characterization of apolipophorin III from immune hemolymph of Heliotis virescens pupae. Comparative Biochemistry and Physiology, 132(2002), 505–514.
Cole, K. D., Fernando-Warnakulasuriya, G. J. P., Boguski, M. S., Freeman, M., Gordon, J. I., Clark, W. A., et al. (1987). Primary structure and comparative sequence analysis of an insect apolipoprotein: apolipophorin III from Manduca sexta. Journal of Biological Chemistry, 262, 11794–11800.
Downer, R. G. H., & Chino, H. (1985). Turnover of protein and diacylglycerol components of lipophorin in locust hemolymph. Insect Biochemistry, 15, 627–630.
Duke, J. (2006). Dr. Duke’s Phytochemical and Ethnobotanical Databases. <http://www.ars-grin.gov/duke/.
Fischer, N. O., Infante, E., Ishikawa, T., Blanchette, C. D., & Bourne, N. (2010). Conjugation to nickel-chelating nanolipoprotein particles increases the potency and efficacy of subunit vaccines to prevent West Nile encephalitis. Bioconjugate Chemistry, 21, 1018–1022.
Isman, B. (2006). Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annual Review of Entomology, 51, 45–66.
Jameson, G. W., Adams, D. V., Kyle, W. S., & Elmore, D. T. (1973). Determination of the operational molarity of solutions of bovine α-chymotrypsin, trypsin, thrombin and factor Xa by spectrofluorimetric titration. Biochemical Journal, 131, 107–117.
Kanost, M. R., Boguski, M. S., Freeman, M., Gordon, J. I., Wyatt, G. R., & Wells, M. A. (1988). Primary structure of apolipophorin-III from the migratoria locust, Locusta migratoria. Journal of Biological Chemistry, 263, 10568–10573.
Katase, H., & Chino, H. (1984). Transport of hydrocarbons by hemolymph lipophorin in Locusta migratoria. Insect Biochemistry, 14, 1–6.
Katase, H., & Chino, H. (1982). Transport of hydrocarbons by the lipophorin of insect hemolymph. Biochimica et Biophysica Acta, 710, 341–348.
Kawooya, J. K., Meredith, S. C., Wells, M. A., Kezdy, F. J., & Law, J. H. (1986). Physical and surface properties of insect apolipophorin III. Journal of Biological Chemistry, 261, 13588–13591.
Kawooya, J. K., Keim, P. S., Ryan, R. O., Shapiro, J. P., Samaraweera, P., & Law, J. H. (1984). Physical and chemical properties of microvitellogenin. A protein from the egg of the tobacco hornworm moth, Manduca sexta. Journal of Biological Chemistry, 259, 10733–10737.
Iimura, Y., Ishikawa, H., Yamamoto, K., & Sehnal, F. (1998). Hemagglutinating properties of apolipophorin III from the hemolymph of Galleria mellonella larvae. Archives of Insect Biochemistry and Physiology, 38, 119–125.
Liu, H., Malhotra, V., & Ryan, R. O. (1991). Displacement of apolipophorin III from the surface of low density lipophorin by human apolipoprotein A-I. Biochemical and Biophysical Research Communications, 179, 734–740.
Malik, Z., Amir, S., Pál, G., Buzás, Z., Várallyay, É., Antal, J., et al. (1999). Proteinase inhibitors from desert locust, Schistocerca gregaria: engineering of both P (1) and P (1)′ residues converts a potent chymotrypsin inhibitor to a potent trypsin inhibitor. Biochimica et Biophysica Acta, 1434, 143–150.
Mwangi, R. W., & Goldsworthy, G. J. (1980). Diacylglycerol-transporting lipoproteins and flight in Locusta. Journal of Insect Physiology, 27, 47–50.
Narayanaswami, V., Wang, J., Kay, C. M., Scraba, D. G., & Ryan, R. O. (1996). Disulfide bond engineering to monitor conformational opening of apolipophorin III during lipid binding. Journal of Biological Chemistry, 271, 26855–26862.
Narayanaswami, V., Weers, P. M. M., Bogerd, J., Kooiman, F. P., Kay, C. M., Scraba, D. G., et al. (1995). Spectroscopic and lipid binding studies on the amino and carboxyl terminal fragments of Locusta migratoria apolipophorin III. Biochemistry, 34, 11822–11830.
Fischer, N. O., Blanchette, C. D., Segelke, B. W., Corzett, M., Chromy, B. A., Kuhn, E. A., et al. (2010). Isolation, characterization, and stability of discretely-sized nanolipoprotein particles assembled with apolipophorin-III. PloS One, 5(7), e11643.
Niere, M., Meißlitzer, C., Dettloff, M., Weise, C., Ziegler, M., & Wiesner, A. (1999). Insect immune activation by recombinant Galleria mellonella apolipophorin III. Biochimica et Biophysica Acta, 1433, 16–26.
Pattnaik, N. M., Mundall, E. C., Trambusti, B. G., Law, J. H., & Kezdy, F. J. (1979). Isolation and charaterization of a larval lipoprotein from the hemolymph of Manduca sextu. Comparative Biochemistry and Physiology, 63B, 469–476.
Ryan, R. O., Prasad, S. V., Henriksen, E. J., Wells, M. A., & Law, J. H. (1986). Lipoprotein interconversions in an insect, Manduca sexta. Evidence for a lipid transfer factor in the hemolymph. Journal of Biological Chemistry, 261, 562–563.
Shapiro, J. P., & Law, J. H. (1983). Locust adipokinetic hormone stimulates lipid mobilization in Manduca sexta. Biochemical and Biophysical Research Communications, 115, 924–931.
Shapiro, J. P., Keim, P. S., & Law, J. H. (1984). Structural studies on lipophorin, an insect lipoprotein. Journal of Biological Chemistry, 259, 3680–3685.
Seo, S. J., Park, K. H., & Cho, K. H. (2008). Apolipophorin III from Hyphantria cunea shows different anti-oxidant ability against LDL oxidation in the lipid-free and lipid-bound state. Comparative Biochemistry and Physiology. B, 151, 433–439.
Smith, A. F., Owen, L. M., Strobel, L. M., Chen, H., Kanost, M. R., Hanneman, E., et al. (1994). Exchangeable apolipoproteins of insects share a common structural motif. Journal of Lipid Research, 35, 1976–1984.
Sun, D., Ziegler, R., Milligan, C. E., Fahrbach, S., & Schwartz, L. M. (1995). Apolipophorin III is dramatically up-regulated during the programmed death of insect skeletal muscle and neurons. Journal of Neurobiology, 26, 119–129.
Schwartz, L. M. (1992). Insect muscle as a model for programmed cell death. Journal of Neurobiology, 23(9), 1312–1326.
Schwartz, L. M. (2008). Atrophy and programmed cell death of skeletal muscle. Cell Death and Differentiation, 15(7), 1163–1169.
Ujvary. (2002). Transforming natural products into natural pesticides experience and expectations. Phytoparasitica, 30, 1–4.
Van der Horst, D. J., van Hoof, D., van Marrewijk, W. J. A., & Rodenburg, K. W. (2002). Alternative lipid mobilization: the insect shuttle system. Molecular and Cellular Biochemistry, 239, 113–119.
Van der Horst, D. J., Ryan, R. O., Van Heusden, M. C., Van Schulz, T. K. F., Doorn, J. M., Law, J. H., et al. (1988). An insect lipoprotein hybrid helps to define the role of apolipophorin III. Journal of Biological Chemistry, 63, 2027–2033.
Weers, P. M. M., & Ryan, R. O. (2006). Apolipophorin III: role model apolipoprotein. Insect Biochemistry and Molecular Biology, 36, 231–240.
Weers, P. M. M., & Ryan, R. O. (2003). Apolipophorin III: a lipid-triggered molecular switch. Insect Biochemistry and Molecular Biology, 33, 1249–1260.
Weers, P. M. M., Wang, J., Van der Horst, D. J., Kay, C. M., Sykes, B. D., & Ryan, O. R. (1998). Recombinant locust apolipophorin III: characterization and NMR spectroscopy. Biochimica et Biophysica Acta, 1393, 99–107.
Weise, C., Franke, P., Kopáček, P., & Wiesner, A. (1998). The primary structure of apolipohorin-III from the greater wax moth, Galleria mellonella. Journal of Protein Chemistry, 17, 633–641.
Wiesner, A., Losen, S., Kopáček, P., Weise, C., & Götz, P. (1997). Isolated apolipophorin III from Galleria mellonella stimulates the immune response of this insect. Journal of Insect Physiology, 43, 383–391.
Wilson, C., Wardell, M. R., Weisgraber, K. H., Mahley, R. W., & Agard, D. A. (1991). Three-dimensional structure of the LDL receptor-binding domain of human apolipoprotein E. Science, 252(5014), 1817–1822.
Acknowledgments
The authors acknowledge Prof. Brigitte Wittman Liebold (Max Delbrück Centrum for Molecular Medicine, Germany) for determining the amino terminal sequence and Dr. Dick J. Van der Horst (Dept. Exp. Zoology, University of Utrecht, The Netherlands) for his generous gift of purified L. migratoria apoLp-III.
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Zulfiqar A. Malik and Sumaira Amir contributed equally to this work.
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Malik, Z.A., Amir, S. An Apolipophorin III Protein from the Hemolymph of Desert Locust, Schistocerca gregaria . Appl Biochem Biotechnol 165, 1779–1788 (2011). https://doi.org/10.1007/s12010-011-9394-9
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DOI: https://doi.org/10.1007/s12010-011-9394-9