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Alternative lipid mobilization: The insect shuttle system

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Abstract

Lipid mobilization in long-distance flying insects has revealed a novel concept for lipid transport in the circulatory system during exercise. Similar to energy generation for sustained locomotion in mammals, the work accomplished by non-stop flight activity is powered by oxidation of free fatty acids (FFA) derived from endogenous reserves of triacylglycerol. The transport form of the lipid, however, is diacylglycerol (DAG), which is delivered to the flight muscles associated with lipoproteins. In the insect system, the multifunctional lipoprotein, high-density lipophorin (HDLp) is loaded with DAG while additionally, multiple copies of the exchangeable apolipoprotein, apoLp-III, associate with the expanding particle. As a result, lipid-enriched low-density lipophorin (LDLp) is formed. At the flight muscles, LDLp-carried DAG is hydrolyzed and FFA are imported into the muscle cells for energy generation. The depletion of DAG from LDLp results in the recovery of both HDLp and apoLp-III, which are reutilized for another cycle of DAG transport. A receptor for HDLp, identified as a novel member of the vertebrate low-density lipoprotein (LDL) receptor family, does not seem to be involved in the lipophorin shuttle mechanism operative during flight activity. In addition, endocytosis of HDLp mediated by the insect receptor does not seem to follow the classical mammalian LDL pathway.

Many structural elements of the lipid mobilization system in insects are similar to those in mammals. Domain structures of apoLp-I and apoLp-II, the non-exchangeable apolipoprotein components of HDLp, are related to apoB100. ApoLp-III is a bundle of five amphipathic α-helices that binds to a lipid surface very similar to the four-helix bundle of the N-terminal domain of human apoE. Despite these similarities, the functioning of the insect lipoprotein in energy transport during flight activity is intriguingly different, since the TAG-rich mammalian lipoproteins play no role as a carrier of mobilized lipids during exercise and besides, these lipoproteins are not functioning as a reusable shuttle for lipid transport. On the other hand, the deviant behavior of similar molecules in a different biological system may provide a useful alternative model for studying the molecular basis of processes related to human disorders and disease.

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References

  1. Babin PJ, Bogerd J, Kooiman FP, Van Marrewijk WJA, Van der Horst DJ: Apolipophorin II/I, apolipoprotein B, vitellogenin, and microsomal triglyceride transfer protein genes are derived from a common ancestor. J Mol Evol 49: 150–160, 1999

    Google Scholar 

  2. Bogerd J, Babin PJ, Kooiman FP, André M, Ballagny C, Van Marrewijk WJA, Van der Horst DJ: Molecular characterization and gene expression in the eye of the apolipophorin II/I precursor from Locusta migratoria. J Comp Neurol 427: 546–558, 2000

    Google Scholar 

  3. Borén J, Lee I, Zhu W, Arnold K, Taylor S, Innerarity TL: Identification of the low density lipoprotein receptor-binding site in apolipoprotein B100 and the modulation of its binding activity by the carboxyl terminus in familial defective apo-B100. J Clin Invest 101: 1084–1093, 1998

    Google Scholar 

  4. Breiter DB, Kanost MR, Benning MM, Wesenberg G, Law JH, Wells MA, Rayment I, Holden HM: Molecular structure of an apolipoprotein determined at 2.5-Å resolution. Biochemistry 30: 603–608, 1991

    Google Scholar 

  5. Cheon H-M, Seo S-J, Sun J, Sappington TW, Raikhel AS: Molecular characterization of the VLDL receptor homolog mediating uptake of lipophorin in oocytes of the mosquito Aedes aegypti. Insect Biochem Mol Biol 31: 753–760, 2001

    Google Scholar 

  6. Dantuma NP, Pijnenburg MAP, Diederen JHB, Van der Horst DJ: Developmental down-regulation of receptor-mediated endocytosis of an insect lipoprotein. J Lipid Res 38: 254–265, 1997

    Google Scholar 

  7. Dantuma NP, Potters M, De Winther MPJ, Tensen CP, Kooiman FP, Bogerd J, Van der Horst DJ: An insect homolog of the vertebrate low density lipoprotein receptor mediates endocytosis of lipophorins. J Lipid Res 40: 973–978, 1999

    Google Scholar 

  8. Fisher CA, Narayanaswami V, Ryan RO: The lipid-associated conformation of the low density lipoprotein receptor binding domain of human apolipoprotein E. J Biol Chem 275: 33601–33606, 2000

    Google Scholar 

  9. Glatz JFC, Van der Vusse GJ: Cellular fatty acid binding proteins: Their function and physiological significance. Prog Lipid Res 35: 243–282, 1996

    Google Scholar 

  10. Gordon DA, Jamil H: Progress towards understanding the role of microsomal triglyceride transfer protein in apolipoprotein-B lipoprotein assembly. Biochim Biophys Acta 1486: 72–83, 2000

    Google Scholar 

  11. Gretch DG, Sturley SL, Wang L, Lipton BA, Dunning A, Grunwald KAA, Wetterau JR, Yao Z, Talmundi P, Attie AD: The amino terminus of apolipoprotein B is necessary but not sufficient for microsomal triglyceride transfer protein responsiveness. J Biol Chem 271: 8682–8691, 1996

    Google Scholar 

  12. Haunerland NH: Transport and utilization of lipids in insect flight muscle. Comp Biochem Physiol 117B: 475–482, 1997

    Google Scholar 

  13. Heeren J, Beisiegel U: Intracellular metabolism of triglyceride-rich lipoproteins. Curr Opin Lipidol 12: 255–260, 2001

    Google Scholar 

  14. Maatman RGHJ, Degano M, Van Moerkerk HTB, Van Marrewijk WJA, Van der Horst DJ, Sacchettini JC, Veerkamp JH: Primary structure and binding characteristics of locust and human muscle fatty-acid-binding proteins. Eur J Biochem 221: 801–810, 1994

    Google Scholar 

  15. Mahley RW, Huang Y: Apolipoprotein E: From atherosclerosis to Alzheimer's disease and beyond. Curr Opin Lipidol 10: 207–217, 1999

    Google Scholar 

  16. Mann CJ, Anderson TA, Read J, Chester SA, Harrison GB, Köchl S, Ritchie PJ, Bradbury P, Hussain FS, Almey J, Vanloo B, Rosseneu M, Infante R, Hancock JM, Levitt DG, Banaszak LJ, Scott J, Shoulders C: The structure of vitellogenin provides a molecular model for the assembly and secretion of atherogenic lipoproteins. J Mol Biol 285: 391–408, 1999

    Google Scholar 

  17. Mukherjee S, Ghosh RN, Maxfield FR: Endocytosis. Physiol Rev 77: 759–803, 1997

    Google Scholar 

  18. Narayanaswami V, Ryan RO: Molecular basis of exchangeable apolipoprotein function. Biochim Biophys Acta 1483: 15–36, 2000

    Google Scholar 

  19. Narayanaswami V, Wang J, Schieve D, Kay CM, Ryan RO: A molecular trigger of lipid-binding induced opening of a helix bundle exchangeable apolipoprotein. Proc Natl Acad Sci USA 96: 4366–4371, 1999

    Google Scholar 

  20. Ryan RO: Dynamics in insect lipophorin metabolism. J Lipid Res 31: 1725–1739, 1990

    Google Scholar 

  21. Ryan RO, Van der Horst DJ: Lipid transport biochemistry and its role in energy production. Annu Rev Entomol 45: 233–260, 2000

    Google Scholar 

  22. Segrest JP, Jones MK, De Loof H, Dashti N: Structure of apolipoprotein B-100 in low density lipoproteins. J Lipid Res 42: 1346–1367, 2001

    Google Scholar 

  23. Soulages JL, Arrese EL: Dynamics and hydration of the α-helices of apolipophorin III. J Biol Chem 275: 17501–17509, 2000

    Google Scholar 

  24. Soulages JL, Wells MA: Lipophorin: the structure of an insect lipoprotein and its role in lipid transport in insects. Adv Prot Chem 45: 371–415, 1994

    Google Scholar 

  25. Spector AA: Fatty acid binding to plasma albumin. J Lipid Res 16: 165–179, 1995

    Google Scholar 

  26. Van der Horst DJ: Lipid transport function of lipoproteins in flying insects. Biochim Biophys Acta 1047: 195–211, 1990

    Google Scholar 

  27. Van der Horst DJ, Van Marrewijk WJA, Diederen JHB: Adipokinetic hormones of insect: Release, signal transduction, and responses. Int Rev Cytol 211: 179–240, 2001

    Google Scholar 

  28. Van der Horst DJ, Weers PMM, Van Marrewijk WJA: Lipoproteins and lipid transport. In: D.W. Stanley-Samuelson, D.R. Nelson (eds). Insect Lipids: Chemistry, Biochemistry and Biology. University of Nebraska Press, Lincoln, NE, 1993, pp 1–24

    Google Scholar 

  29. Weers PMM, Van der Horst DJ, Ryan RO: Interaction of locust apolipophorin III with lipoproteins and phospholipid vesicles: Effect of glycosylation. J Lipid Res 41: 416–423, 2000

    Google Scholar 

  30. Weers PMM, Van Marrewijk WJA, Beenakkers AMT, Van der Horst DJ: Biosynthesis of locust lipophorin: Apolipophorin I and II originate from a common precursor. J Biol Chem 268: 4300–4303, 1993

    Google Scholar 

  31. Weisgraber KH: Apolipoprotein E: Structure-function relationships. Adv Prot Chem 45: 249–302, 1994

    Google Scholar 

  32. Wetterau JR, Lin MCM, Jamil H: Microsomal triglyceride transfer protein. Biochim Biophys Acta 1345: 136–150, 1997

    Google Scholar 

  33. Wilson C, Wardell MR, Weisgraber KH, Mahley RW, Agard DA: Three dimensional structure of the LDL-receptor binding domain of human apolipoprotein E. Science 252: 1817–1822, 1991

    Google Scholar 

  34. Zanotti G, Scapin G, Spadon P, Veerkamp JH, Sacchettini JC: Threedimensional structure of recombinant human muscle fatty acid-binding protein. J Biol Chem 267: 18541–18550, 1992

    Google Scholar 

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Van der Horst, D.J., Van Hoof, D., Van Marrewijk, W.J. et al. Alternative lipid mobilization: The insect shuttle system. Mol Cell Biochem 239, 113–119 (2002). https://doi.org/10.1023/A:1020541010547

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  • DOI: https://doi.org/10.1023/A:1020541010547

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