Molecular cloning, characterization and regulation of the cockroach vitellogenin receptor during oogenesis

Insect Molecular Biology

Volumn 14, Issue 4, 2005, Pages 389-401

  Tufail, M ^a   Takeda, M ^a  

^a KOBE UNIVERSITY   (Japan)

Author keywords

LDLR; mRNA; Periplaneta americana; Protein; Regulation; Vitellogenesis; Vitellogenin receptor

Indexed keywords

BLATTARIA; INSECTA; PERIPLANETA; PERIPLANETA AMERICANA;

CELL SURFACE RECEPTOR; EGG PROTEIN; MESSENGER RNA; VITELLOGENIN RECEPTOR;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; BIOSYNTHESIS; CHEMISTRY; COCKROACH; FEMALE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MOLECULAR CLONING; MOLECULAR GENETICS; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; OOCYTE DEVELOPMENT; OVARY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BLOTTING, NORTHERN; CLONING, MOLECULAR; COCKROACHES; EGG PROTEINS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MOLECULAR SEQUENCE DATA; OOGENESIS; OVARY; RECEPTORS, CELL SURFACE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEQUENCE ALIGNMENT;

EID: 24044440493     PISSN: 09621075     EISSN: 13652583     Source Type: Journal    
DOI: 10.1111/j.1365-2583.2005.00570.x     Document Type: Article

References (56)

1. Anderson, R.G.W, and Kaplan, J. (1983) Receptor-mediated endocytosis. Mod Cell Biol 1:1-52.
2. Beisiegel, U. (1996) New aspects on the role of plasma upases in lipoprotein catabolism and atherosclerosis. Atherosclerosis 124: 1-8.
3. Blom, N., Gammeltoft, S. and Brunak, S. (1999) Sequence- and structure-based prediction of eukaryotic protein phosphorylation sites. J Mol Biol 5: 1351-1362.
4. Bownes, M., Shirras, A., Blair, M., Collins, J. and Coulson, A. (1988) Evidence that insect embryogenesis is regulated by ecdysteroids released from yolk proteins. Proc Natl Acad Sci USA 85: 1554-1557.
5. Bujo, H., Hermann, M., Kaderli, M.O., Jacobsen, L., Sugawara, S., Nimpf, J., Yamamoto, T. and Schneider, W.J. (1994) Chicken oocyte growth is mediated by an eight ligand repeat member of the LDL receptor family. EMBO J 13: 5165-5175.
6. Bujo, H., Yamamoto, T., Hayashi, K., Hermann, M., Nimpf, J. and Schneider, W.J. (1995) Mutant oocytic low density lipoprotein receptor gene family member causes atherosclerosis and female sterility. Proc Natl Acad Sci USA 92: 9905-9909.
7. Chen, W.J., Goldstein, J.L. and Brown, M.S. (1990) NPXY, a sequence often found in cytoplasmic tails, is required for coated pit-mediated internalization of the low density lipoprotein receptor. J Biol Chem 265: 3116-3123.
8. Chen, M.-E., Lewis, D.K., Keeley, L.L. and Pietrantonio, P.V. (2004) cDNA cloning and transcriptional regulation of the vitellogenin receptor from the fire ant, Solenopsis invicta Buren (Hymenoptera: Formicidae). Insect Mol Biol 13: 195-204.
9. Cho, K.-H. and Raikhel, A.S. (2001) Organization and developmental expression of the mosquito vitellogenin receptor gene. Insect Mol Biol 10: 465-474.
10. Davail, B., Pakdel, F., Bujo, H., Perazzolo, L.M., Waclawek, M., Schneider, W.J. and Le Menn, F. (1998) Evolution of oogenesis: the receptor for vitellogenin from the rainbow trout. J Lipid Res 39: 1929-1937.
11. David, S.R., Matthew, G., Brandy, C., Debra, M.H., Suzanne, S. and Danielle, S. (2001) Yolk protein endocytosis by oocytes in Drosophila melanogaster: immunofluorescent localization of clathrin, adaptin and the yolk protein receptor. J Insect Physiol 47: 715-723.
12. Davis, C.G., Van Driel, I.R., Russell, D.W., Brown, M.S. and Goldstein, J.L. (1987) The low density lipoprotein receptor: identification of amino acids in the cytoplasmic domain required for rapid endocytosis. J Biol Chem 262: 4075-4082.
13. DiMario, P.J., Warren, T.G. and Mahowald, A.P. (1987) Female sterile (1) yolkless: a recessive female sterile mutation in Drosophila melanogester with depressed numbers of coated pits and coated vesicles within the developing oocytes. J Cell Biol 105: 199-206.
14. Fass, D., Blacklow, S., Kim, P.S. and Berger, J.M. (1997) Molecular basis of familial hypercholesterolemia from structure of LDL receptor module. Nature 388: 691-693.
15. Ferenz, H.-J. (1993) Yolk protein accumulation in Locusta migratoria (R. & F.) (Orthoptera: Acrididae) oocytes. Int J Insect Morph Emobryol 22: 295-314.
16. Goldstein, J.L., Anderson, R.G.W, and Brown, M.S. (1979) Coated pits, coated vesicles, and receptor mediated endocytosis. Nature 279: 679-685.
17. Goldstein, J.L., Brown, M.S., Anderson, R.G.W., Russell, D.W. and Schneider, W.J. (1985) Receptor-mediated endocytosis: concepts emerging from the LDL receptor system. Ann Rev Cell Biol 1:1-39.
18. Grant, B. and Hirsh, D. (1999) Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte. Mol Biol Cell 10: 4311-4326.
19. Hafer, J., Fischer, A. and Ferenz, H.-J. (1992) Identification of the yolk receptor protein in oocytes of Nereis virens (Annelida, polychaeta) and comparison with the locust vitellogenin receptor. J Comp Physiol B 162: 148-152.
20. Herz, J., Hamann, U., Rogne, S., Myklebost, O., Gausepohl, H. and Stanley, K.K. (1988) Surface location and high affinity for calcium of a 500-kd liver membrane protein closely related to the LDL-receptor suggest a physiological role as lipoprotein receptor. EMBO J 7: 4119-1127.
21. Hiesberger, T., Hermann, M., Jacobsen, L., Novak, S., Hodits, R.A. and Bujo, H. (1995) The chicken oocyte receptor for yolk precursors as a model for studying the action of receptor-associated protein and lactoferrin. J Biol Chem 270: 18219-18226.
22. 2+-binding receptor with potential intracellular signaling properties. Eur J Biochem 239: 132-137.
23. 2-macroglobulin. J Biol Chem 270: 6468-6475.
24. Kounnas, M.Z., Church, F.C., Argraves, W.S. and Strickland, D.K. (1996) Cellular internalization and degradation of antithrombin III-thrombin, heparin cofactor II-thrombin, and a1-antitrypsin-trypsin complexes is mediated by the low density lipoprotein receptor-related protein. J Biol Chem 271: 6523-6529.
25. Kumar, S., Koichiro, T., Ingrid, B.J. and Masatoshi, N. (2001 ) Mega2: Molecular Evolutionary Genetics Analysis software. Arizona State University, Arizona.
26. MacLachlan, I., Nimpf, J. and Schneider, W.J. (1994) Avian riboflavin binding protein binds to lipoprotein receptors in association with vitellogenin. J Biol Chem 269: 24127-24132.
27. Monigatti, F., Gasteiger, E., Bairoch, A. and Jung, E. (2002) The Sulfinator: predicting tyrosine sulfation sites in protein sequences. Bioinformatics 18: 769-770.
28. Mukherjee, S., Ghosh, R.N. and Maxfield, F.R. (1997) Endocytosis. Physiol Rev 77: 759-803.
29. Nielsen, H., Engelbrecht, J., Brunak, S. and von Heijne, G. (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10: 1-6.
30. Nimpf, J., Stifani, S., Bilous, P.T. and Schneider, W.J. (1994) The somatic cell specific LDL receptor-related protein of the chicken: close kinship to mammalian LDL receptor gene family members. J Biol Chem 269: 212-219.
31. Okabayashi, K., Shoji, H., Nakamura, T., Hashimoto, O., Asashima, M. and Sugino, H. (1996) cDNA cloning and expression of the Xenopus laevis vitellogenin receptor. Biochem Biophys Res Commun 224: 406-413.
32. Part, F., Coward, K., Sumpter, J.P. and Tyler, C.R. (1998) Molecular characterization and expression of two ovarian lipoprotein receptors in the rainbow trout Oncorhynchus mykiss. Biol Reprod 58: 1146-1153.
33. Raikhel, A.S. (1984) The accumulative pathway of vitellogenin in the mosquito oocyte: a high resolution immuno- and cytochemical study. J Ultrastruct Res 87: 285-302.
34. Raikhel, A.S. and Dhadialla, T.S. (1992) Accumulation of yolk proteins in insect oocytes. Annu Rev Entomol 37: 217-251.
35. Roehrkasten, A. and Ferenz, H.-J. (1986) Properties of the vitellogenin receptor of isolated locust oocyte membranes. Int J Invert Reprod Dev 10: 133-142.
36. Roehrkasten, A., Ferenz, H.-J., Buschmann-Gebhardt, B. and Hafer, J. (1989) Isolation of the vitellogenin-binding protein from locust ovaries. Arch Insect Biochem Physiol 10: 141-149.
37. Saito, A., Pietromonaco, S., Loo, A.K.-C. and Farquhar, M.G. (1994) Complete cloning and sequencing of rat gp330/'megalin', a distinctive member of the low density lipoprotein receptor gene family. Proc Natl Acad Sci USA 91: 9725-9729.
38. Sakai, J., Hoshino, A., Miura, Y., Ishii, H., Suzuki, H., Kawarabayasi, Y. and Yamamoto, T. (1994) Structure, chromosome location and expression of the human very low density lipoprotein receptor gene. J Biol Chem 269: 2173-2182.
39. Sappington, T.W. (2002) The major yolk proteins of higher Diptera are homologos of a class of minor yolk proteins in Lepidoptera. J Mol Evol 55: 470-475.
40. Sappington, T.W., Hays, A.R. and Raikhel, A.S. (1995) Mosquito vitellogenin receptor: purification, developmental and biochemical characterization. Insect Biochem Mol Biol 25: 807-817.
41. Sappington, T.W., Kokoza, V.A. and Raikhel, A.S. (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.
42. Sappington, T.W. and Raikhel, A.S. (1998) Molecular characteristics of insect vitellogenins and vitellogenin receptors. Insect Biochem Mol Biol 28: 277-300.
43. Schneider, W.J. (1996) Vitellogenin receptors: oocyte-specific members of the low-density lipoprotein receptor supergene family. Int Rev Cytol 166(103): 137.
44. Schonbaum, C.P, Lee, S. and Mahowald, A.P (1995) The Drosophila yolkless gene encodes a vitellogenin receptor belonging to the low density lipoprotein receptor superfamily. Proc Natl Acad Sci USA 92: 1485-1489.
45. Schonbaum, C.P., Perrino, J.J. and Mahowald, A.P (2000) Regulation of the vitellogenin receptor during Drosophila melanogaster oogenesis. Mol Biol Cell 11: 511-521.
46. Snigirevskaya, E.S., Sappington, T.W. and Raikhel, A.S. (1997) Internalization and recycling of vitellogenin receptor in the mosquito oocyte. Cell Tissue Res 290: 175-183.
47. Springer, T.A. (1998) An extracellular beta-propeller module predicted in lipoprotein and scavenger receptors, tyrosine kinases, epidermal growth factor precursor and extracellular matrix components. J Mol Biol 283: 837-862.
48. Stifani, S., Barber, D.L., Nimpf, J. and Schneider, W.J. (1990) A single chicken oocyte plasma membrane protein mediates uptake of very low density lipoprotein and vitellogenin. Proc Mail Acad Sci USA 87: 1955-1959.
49. Strickland, D.K., Kounas, M.Z. and Argraves, W.S. (1995) LDL receptor-related protein: a multiligand receptor for lipoprotein and proteinase catabolism. FASEB J 9: 890-898.
50. Takahashi, S., Kawarabayasi, S., Nakai, T., Sakai, J. and Yamamoto, T. (1992) Rabbit very low density lipoprotein receptor: a low density lipoprotein receptor like protein with distinct ligand specificity. Proc Natl Acad Sci USA 89: 9252-9256.
51. Thompson, J.D., Higgins, D.G. and Gibson, T.J. (1994) Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-1680.
52. Tufail, M. and Takeda, M. (2002) Vitellogenin of the cockroach, Leucophaea maderae: nucleotide sequence, structure and analysis of processing in the fat body and oocytes. Insect Biochem Mol Biol 32: 1469-1476.
53. Tufail, M., Lee, J.M., Hatakeyama, M., Oishi, K. and Takeda, M. (2000) Cloning of Vitellogenin cDNA of the American cockroach, Periplaneta americana (Dictyoptera), and its structural and expression analyses. Arch Insect Biochem Physiol 45: 37-46.
54. Tufail, M., Hatakeyama, M. and Takeda, M. (2001) Molecular evidence for two Vitellogenin genes and processing of vitellogenins in the American cockroach, Periplaneta americana. Arch Insect Biochem Physiol 48: 72-80.
55. Tufail, M., Raikhel, A.S. and Takeda, M. (2004) Biosynthesis and processing of insect vitellogenins. In Progress in Vitellogenesis (Raikhel, A.S. and Sappington, T.W., eds); Reproductive Biology of Invertebrates (Adiyodi K.G. and Adiyodi R.G., series eds), Vol. XII. Part B. pp. 1-32. Science Publishers, Inc. Enfield, USA and Plymouth UK.
56. Yamamoto, T., Davis, C.G., Brown, M.S., Schneider, W.J., Casey, M.L. and Goldstein, J.L. (1984) The human LDL receptor: a cysteine-rich protein with multiple Alu sequences in its mRNA. Cell 39: 27-38.