Abstract
The selective uptake of storage proteins by the fat body of the corn earworm Helicoverpa zea is mediated by a membrane-bound receptor protein. In this study, the major storage proteins of this insect species, arylphorin and very high density lipoprotein, were directly labeled with colloidal gold-particles of different size. After the fat body had been incubated with the labeled storage proteins, the distribution of these proteins was examined by electron microscopy. Both storage proteins were found at the extracellular side of coated pits and within coated vesicles. Moreover, fusion products of several coated vesicles such as endosomes and multivesicular bodies contained both proteins in their lumen. Ultimately, the proteins accumulated in electron-dense storage granules. Equal numbers of either storage protein were present in each organelle, supporting the notion that a single receptor mediates the uptake of both proteins. In contrast, only small numbers of gold-labeled immunoglobulin G molecules were found in the organelles, indicating that the protein uptake is specific for storage proteins. The results show that storage protein uptake in this lepidoteran species occurs in a process of receptor-mediated endocytosis that is similar to the well-established uptake of specific proteins into mammalian tissues.
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References
Burmester T, Scheller K (1992) Identification of binding proteins involved in the stage-specific uptake of arylphorin by the fat body cells of Calliphora vicina. Insect Biochem Mol Biol 22:211–220
Butterworth FM, Tysell B, Waclawski I (1979) The effects of 20-hydroxyecdysone and protein on granule formation in the in vitro cultured fat body of Drosophila. J Insect Physiol 25:855–850
Dean RL, Collins JV, Locke M (1985) Structure of the fat body. In: Gilbert LI, Kerkut G (eds) Comprehensive insect biochemistry, physiology, and pharmacology, vol 4. Pergamon Press, New York, pp 156–210
Ferenz HJ (1990) Receptor-mediated endocytosis of insect yolk proteins. In: Hagedorn HH, Hildebrand JG, Kidwell MG, Law JH (eds) Molecular insect science. Plenum Press, New York, pp 131–138
Goldstein JL, Anderson RGW, Brown MS (1979) Coated pits, coated vesicles, and receptor-mediated endocytosis. Nature 279:679–685
Goldstein JL, Brown MS, Anderson RGW, Russell DW, Schneider WJ (1985) Receptor-mediated endocytosis: concepts emerging from the LDL receptor system. Annu Rev Cell Biol 1:1–39
Greenstone MG, Stuart MK, Haunerland NH (1991) Using monoclonal antibodies for phylogenetic analysis: an example from the Heliothinae (Lepidoptera: Noctuidae). Ann Entomol Soc Am 84:457–464
Gruenberg J, Howell KE (1989) Membrane traffic in endocytosis: insights from cell-free assays. Annu Rev Cell Biol 5:453–481
Haunerland NH, Bowers WS (1986 a) A larval specific lipoprotein: purification and characterization of a blue chromoprotein from Heliothis zea. Biochem Biophys Res Commun 134:580–586
Haunerland NH, Bowers WS (1986 b) Arylphorin from the corn earworm, Heliothis zea. Insect Biochem 16:617–625
Haunerland NH, Nair KK, Bowers WS (1990) Fat body heterogeneity during development of Heliothis zea. Insect Biochem 20:829–837
Helenius A, Mellman I, Wall D, Hubbard A (1983) Endosomes. Trends Biochem Sci 8:245–250
Jones G, Ryan RO, Haunerland NH, Law JH (1988) Purification and characterization of a very high density chromolipoprotein from the hemolymph of Trichoplusia ni (Hübner). Arch Insect Biochem Physiol 7:1–11
Levenbook L (1985) Storage proteins. In: Gilbert LI, Kerkut G (eds) Comprehensive insect biochemistry, physiology, and pharmacology, vol 10. Pergamon Press, New York, pp 307–346
Locke M (1984) The structure and development of the vacuolar system in the fat body of insects. In: Akai H, King R (eds) Insect ultrastructure, vol 2. Plenum Press, New York, pp 151–197
Locke M, Collins J (1968) Protein uptake into multivesicular bodies and storage granules in the fat body of an insect. J Cell Biol 36:453–483
Marx R (1983) Ultrastructural aspects of protein synthesis and protein transport in larvae of Calliphora vicina. In: Scheller K (ed) The larval serum proteins of insects. Thieme, New York, pp 50–60
Palade G (1975) Intracellular aspects of the process of protein secretion. Science 189:347–385
Pantana R, McAda WC (1973) Tobacco budworm: use of dry diet flakes in rearing. J Econ Entomol 66:817–818
Roth TF, Porter KR (1964) Yolk protein uptake in the oocyte of the mosquito Aedes aegypti. J Cell Biol 20:313–332
Telfer WH, Kunkel JC (1991) The function and evolution of insect storage hexamers. Annu Rev Entomol 36:205–228
Thomasson W, Mitchell H (1972) Hormonal control of protein granule accumulation in fat bodies of Drosophila melanogaster larvae. J Insect Physiol 18:185–199
Ueno K, Natori S (1984) Identification of storage protein receptor and its precursor in the fat body membrane of Sarcophaga peregrina. J Biol Chem 259:12107–12111
Wang Z, Haunerland NH (1991) Ultrastructural study of storage protein granules in fat body of the corn earworm, Heliothis zea. J Insect Physiol 37:353–363
Wang Z, Haunerland NH (1992) Fate of differentiated fat body tissues during metamorphosis of Helicoverpa zea. J Insect Physiol 38:199–213
Wang Z, Haunerland NH (1993) Storage protein uptake in Helicoverpa zea: Purification of the VHDL receptor from perivisceral fat body. J Biol Chem 268:16673–16678
Wang Z, Haunerland NH (1994) Storage protein uptake in Helicovepa zea fat body: a single receptor mediates the uptake of arylphorin and VHDL. Arch Insect Biochem Physiol 26:15–26
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Wang, Z., Haunerland, N.H. Receptor-mediated endocytosis of storage proteins by the fat body of Helicoverpa zea . Cell Tissue Res 278, 107–115 (1994). https://doi.org/10.1007/BF00305782
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DOI: https://doi.org/10.1007/BF00305782