Secretory and internalization pathways of mosquito yolk protein precursors

Cell and Tissue Research

Volumn 290, Issue 1, 1997, Pages 129-142

  Snigirevskaya, Ekaterina S ^a,b   Hays, Alan R ^a   Raikhel, Alexander S ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b INSTITUTE OF CYTOLOGY   (Russian Federation)

Author keywords

Fat body; Immunogold; Mosquito, Aedes aegypti, (Insecta); Oocyte; Receptor mediated endocytosis; Secretion; Yolk accumulation; Yolk protein precursors

Indexed keywords

VITELLOGENIN; YOLK PROTEIN;

AEDES AEGYPTI; ARTICLE; COATED VESICLE; ENDOSOME; FEMALE; GOLGI COMPLEX; IMMUNOCYTOCHEMISTRY; INTERNALIZATION; LYSOSOME; MICROVILLUS; NONHUMAN; OOCYTE; PRIORITY JOURNAL; SECRETORY GRANULE; VITELLOGENESIS;

EID: 0030781011     PISSN: 0302766X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s004410050915     Document Type: Article

References (72)

1. Bendayan M (1989) Protein A-gold and Protein G-gold postembedding immunoelectron microscopy. In: Hayat MA (ed) Colloidal gold: principles, methods, and applications, vol1. Academic Press, San Diego, pp 33-94
2. Bendayan M, Roth J, Perrelet A, Orci L (1980) Quantitative immunocytochemieal localization of pancreatic secretory proteins in subcellular compartments of the rat acinar cell. J Histochem Cytochem 28:149-160
3. Bergen PMP van, Henegouwen P (1989) Immunogold labeling of ultrathin cryosections. In: Hayat MA (ed) Colloidal gold: principles, methods, and applications, vol 1. Academic Press, San Diego, pp 96-111
4. Bose SG, Raikhel AS (1988) Mosquito vitellogenin subunits originate from a common precursor. Biochem Biophys Res Commun 155:436-442
5. Bu G, Schwartz AL (1994) Receptor-mediated endocytosis. In: Arias IM, Boyer JL, Faust N, Jakoby WB, Schachter DA, Shafritz DA (eds) The liver. Biology and pathobiology. Raven, New York, pp 259-274
6. Burgess TL, Kelly RB (1987) Constitutive and regulated secretion of proteins. Annu Rev Cell Biol 3:243-293
7. Chen JS, Raikhel AS (1996) Subunit cleavage of mosquito pro-vitellogenin by a subtilisin-like convertase. Proc Natl Acad Sci USA 93:6186-6190
8. Chen JS, Hays AR, Snigirevskaya ES, Raikhel AS (1995) Mosquito cathepsin B-like thiol protease is a yolk protein precursor produced by the fat body, accumulated by oocytes and activated during embryogenesis. J Cell Biochem 21A:215
9. Cho W-L, Raikhel AS (1992) Cloning of cDNA for mosquito lysosomal aspartic protease: sequence analysis of an insect lysosomal enzyme similar to cathepsin D and E. J Biol Chem 267:21823-21829
10. Cho W-L, Deitsch KW, Raikhel AS (1991) An extraovarian protein accumulated in mosquito oocytes is a carboxypeptidase activated in embryos. Proc Natl Acad Sci USA 88:10821-10824
11. Couble P, Chen TT, Wyatt GR (1979) Juvenile hormone-controlled vitellogenin synthesis in Locusta migratoria fat body: cytological development. J Insect Physiol 25:327-337
12. Davey KG (1981) Hormonal control of vitellogenin uptake in Rhodnius prolixus Stål. Am Zool 21:701-705
13. Dhadialla TS, Raikhel AS (1990) Biosynthesis of mosquito vitellogenin. J Biol Chem 265:9924-9933
14. Dhadialla TS, Hays AR, Raikhel AS (1992) Characterization of the solubilized mosquito vitellogenin receptor. Insect Biochem Mol Biol 22:803-816
15. Dini L, Lentini A, Mantile G, Massimi M, Devirgiliis LC (1992) Receptor-mediated endocytosis of galactose and mannose exposing ligands: an electron microscopic study on adult and neonatal cultured rat hepatocytes. Biol Cell 74:217-224
16. Fagotto F, Maxfield FR (1994) Yolk platelets in Xenopus oocytes maintain an acidic internal pH which may be essential for sodium accumulation. J Cell Biol 125:1047-1056
17. Ferenz H-J (1990) Receptor-mediated endocytosis of insect yolk proteins. In: Hagedorn HH, Hildebrand JG, Kidwell MG, Law JH (eds) Molecular insect science. Plenum New York London, pp 131-138
18. Ferenz H-J (1993) Yolk protein accumulation in Locusta migratoria (R & F) (Orthoptera: Acrididae) oocytes. Int J Inset Morphol Embryol 22:295-314
19. Giorgi F, Licchesi P, Moreli A, Bownes M (1993) Ultrastructural analysis of Drosophila ovarian follicles differing in yolk polypeptide (yps) composition. Development 117:319-328
20. Hagedorn HH, Turner S, Hagedorn EA, Pontecorvo D, Greenhbaum P, Pfeiffer D, Wheelock G, Flanagan TR (1977) Postemergence growth of the ovarian follicles of Aedes aegypti. J Insect Physiol 23:203-206
21. Hays AR, Raikhel AS (1990) A novel protein produced by the vitellogenic fat body and accumulated in mosquito oocytes. Roux's Arch Dev Biol 199:114-121
22. Indrasith LS, Sasaki T, Yamashita O (1988) A unique protease responsible for selective degradation of a yolk protein in Bonibyx mori. J Biol Chem 263:1045-1051
23. Kanost MR, Kawooya JH, Law JH, Ryan RO, Van Heusden MC, Ziegler R (1990) Insect hemolymph proteins. Adv Insect Physiol 22:299-396
24. Kawooya JK, Law JH (1988) Role of lipophorin in lipid transport to the insect egg. J Biol Chem 263:87478-8753
25. Kawooya JK, Osir EO, Law JH (1986) Physical and chemical properties of microvitellogenin. Physical and chemical properties of microvitellogenin. J Biol Chem 261:10844-10849
26. Kimura M, Lukinius A, Ericsson JLE, Grimelius L (1992) Distribution of insulin binding sites on Leydig cells of rat testes using insulin-coated gold particles. Histochemistry 97:213-220
27. Koller CN, Dhadialla TS, Raikhel AS (1989) Selective endocytosis of vitellogenin by oocytes of the mosquito, Aedes aegypti: an in vitro study. Insect Biochem 19:693-702
28. Kulakosky PC, Teller WH (1987) Selective endocytosis, in vitro, by ovarian follicles from Hyalophora cecropia. Insect Biochem 17:845-858
29. Kulakosky PC, Telfer WH (1990) Lipophorin as a yolk precursors in Hyalophora cecropia: uptake kinetics and competition with vitellogenin. Arch Insect Biochem Physiol 14:269-285
30. Kunkel JG, Nordin JH (1985) Yolk proteins 1. In: Kerkut GA and Gilbert LI (eds) Comprehensive insect physiology, biochemistry, and pharmacology. Pergamon, New York, pp 83-112
31. Laemmli UK (1970) Cleavage of structural proteins during the assembly of head of bacteriophage T4. Nature 227:680-685
32. Lea AO (1964) Studies on the dietary and endocrine regulation of autogenous Aedes taeniorhynchus. J Med Entomol 1:40-44
33. Mazzini M, Burrini A, Giorgi F (1989) The secretory pathway of vitellogenin in the fat body of the stick insect Bacillus rossius: an ultrastructural and immunocytochemical study. J Submicrosc Cytol Pathol 24:563-570
34. Medina M, Vallejo CG (1989) The maternal origin of acid hydrolases in Drosophila and their relation with yolk degradation. Dev Growth Differ 31:241-247
35. Medina M, Leon P, Vallejo CG (1988) Drosophila cathepsin B-like proteinase: a suggested role in yolk degradation. Arch Biochem Biopnys 263:355-363
36. Nordin JH, Beauidoin EL, Liu X (1991) Acidification of yolk granules in Blatella germanica eggs coincident with proteolytic processing of vitellin. Arch Insect Biochem Physiol 18: 177-192
37. Raikhel AS (1984a) Accumulation of membrane-free clathrin-like lattices in the mosquito oocyte. Eur J Cell Biol 35:279-283
38. Raikhel AS (1984b) The accumulative pathway of vitellogenin in the mosquito oocyte; a high resolution immuno- and cytochemical study. J Ultrastruct Res 87:285-302
39. Raikhel AS (1986a) Role of lysosomes in regulation of vitellogenin secretion in the mosquito fat body. J Insect Physiol 32:597-604
40. Raikhel AS (1986b) Lysosomes in the cessation of vitellogenin secretion by mosquito fat body; selective degradation of Golgi complexes and secretory granules. Tissue Cell 18:125-142
41. Raikhel AS (1987) Monoclonal antibodies as probes for processing of yolk protein in the mosquito; a high resolution immunolocalization of secretory and accumulative pathways. Tissue Cell 19:515-529
42. Raikhel AS (1992) Vitellogenesis in mosquitoes. Adv Disease Vector Res 9:1-39
43. Raikhel AS, Bose SG (1988) Properties of mosquito yolk protein: a study using monoclonal antibodies. Insect Biochem 18:565-575
44. Raikhel AS, Dhadialla TS (1992) Mechanism of yolk protein accumulation in insect oocytes. Annu Rev Entomol 37:217-251
45. Raikhel AS, Lea AO (1983) Previtellogenic development and synthesis in the fat body of a mosquito: an ultrastructural and immunocytochemical study. Tissue Cell 15:281-300
46. Raikhel AS, Lea AO (1985) Hormone-mediated formation of the endocytic complex in mosquito oocytes. Gen Comp Endocrinol 53:424-435
47. Raikhel AS, Leu AO (1991) Control of follicular epithelium development and vitelline envelope formation in the mosquito; role of juvenile hormone and 20-hydroxyecdysone. Tissue Cell 23:577-591
48. Raikhel AS, Pratt LH, Lea AO (1986) Monoclonal antibodies as probes for processing of yolk protein in the mosquito; production and characterization. J Insect Physiol 32:879-890
49. Raikhel AS, Deitsch KW, Sappington TW (1996) Culture and analysis of the insect fat body. In: Crampton JM, Beard CB, Louis (eds) Molecular biology of vector diseases: a methods manual. Chapman & Hall, London, pp 511-526
50. Sappington TW, Raikhel AS (1995) Receptor-mediated endocytosis of yolk proteins by insect oocytes. In: Ohnishi E, Sonobe H, Takahashi SY (eds) Recent advances in insect biochemistry and molecular biology. University of Nagoya Press, Nagoya, pp 235-257
51. Sappington TW, Hays AR, Raikhel AS (1995) Mosquito vitellogenin receptor: purification, developmental and biochemical characterization. Insect Biochem Mol Biol 25:807-817
52. Sappington TW, Kokoza VA, Cho W-L, Raikhel AS (1996) Molecular characterization of the mosquito vitellogenin receptor reveals unexpected high homology to the Drosophila yolk protein receptor. Proc Natl Acad Sci USA 93:8934-8939
53. Schneider WJ (1992) Lipoprotein receptors in oocyte growth. Clin Investig 70:385-390
54. Segretain D, Egolff M, Gerard N, Pineau C, Jegou B (1992) Receptor-mediated and adsorptive endocytosis by male germ cells of different mammalian species. Cell Tissue Res 268:471-478
55. Sire M-F, Bahin PJ, Vernier J-M (1994) Involvement of the lysosomal system in yolk protein deposit and degradation during vitellogenesis and embryonic development in trout. J Exp Zool 269:69-83
56. Snigirevskaya ES, Sappington TW, Raikhel AS (1997) Internalization and recycling of vitellogenin receptor in the mosquito oocyte. Cell Tissue Res (in press)
57. Steinbrecht RA (1993) Freeze-substitution for morphological and immunocytochemical studies of insects. Microsc Res Tech 24:488-504
58. Tanaka A, Yokizaki H (1974) Immunohistochemical detection of vitellogenin in the ovary and fat body during a reproductive cycle of the cockroach, Blatella germanica. Dev Growth Differ 16:247-255
59. Telfer WH (1965) The mechanism and control of yolk formation. Annu Rev Entomol 10:161-184
60. Teller WH, Heubner E, Smith SD (1982) The cell biology of vitellogenic follicles in Hyalophora and Rhodnius. In: Kign RC, Akai H (eds) Insect ultrastructure. Plenum, New York London, pp 118-149
61. Thomsen E, Hansen BL, Hansen GN, Jensen PV (1980) Ultrastructural immunocytochemical localization of vitellogenin in the fat body of the blowfly. Calliphora vicina Rob-Desv. (erythrocephala Meij) by use of the unlabeled antibody-enzyme method. Cell Tissue Res 208:445-455
62. Tokuyasu KT (1986) Application of cryoultramicrotomy to immunocytochemistry. J Microsc 143:139
63. Van Antwerpen R, Law JH (1993) Immunocytochemical localization of a follicle specific protein of the hawkmoth Manduca sexta. Tissue Cell 25:885-892
64. Van Antwerpen R, Conway R, Law JH (1993) Protein and lipoprotein uptake by developing oocytes of the hawkmoth Manduca sexta. An ultrastructural and immunocytochemical study. Tissue Cell 25:205-218
65. Wall DA, Meleka I (1985) An unusual lyosome compartment involved in vitellogenin endocytosis by Xenopus oocytes. J Cell Biol 101:1651-1664
66. Wang JJ, Tang PC, Chao SH, Cheng CH, Ma HJ, Liao YD (1995) Immunocytochemical localization of ribonuclease in yolk granules of adult Rana catebeiana oocytes. Cell Tissue Res 280:259-265
67. Wang X-Y, Cole KD, Law JH (1988) cDNA cloning and deduced amino acid sequence of microvitellogenin, a female specific hemolymph and egg protein from the tobacco hornworm, Manduca sexta. J Biol Chem 263:8851-8855
68. Yamamoto Y, Takahashi SY (1993) Cysteine proteinase from Bombyx eggs; role in programmed degradation of yolk proteins during embryogenesis. Comp Biochem Physiol 106B: 35-45
69. Yamamoto Y, Zhao X, Suzuki AC, Takahashi SY (1994) Cysteine proteinase from the eggs of the silkworm. Bombyx mori: site of synthesis and a suggested role in yolk protein degradation. J Insect Physiol 40:447-454
70. Yoshizaki N (1992) In vivo study of vitellogenin-gold transport in the ovarian follicle and oocyte of Xenopus laevis. Dev Growth Differ 34:517-527
71. Zhang J-Z, Wyatt GR (1990) A new member of a low molecular weight hemolymph protein family from Locusta migratoria. In: Hagedorn HH, Hildebrand JG, Kidwell MG, Law JH (eds) Molecular insect science. Plenum Press, New York, p 385
72. Zhu J, Indrasith LS, Yamashita O (1986) Characterization of vitellin, egg-specific protein and 30-kDa proteins from Bombyx eggs, and their fates during oogenesis and embryogenesis. Biochem Biophys Acta 882:427-436