Expression analysis of putative vitellogenin and lipophorin receptors in honey bee (Apis mellifera L.) queens and workers

Journal of Insect Physiology

Volumn 54, Issue 7, 2008, Pages 1138-1147

  Guidugli Lazzarini, Karina Rosa ^a   do Nascimento, Adriana Mendes ^a   Tanaka, Érica Donato ^a   Piulachs, Maria Dolors ^b   Hartfelder, Klaus ^a   Bitondi, Márcia Gentile ^a   Simões, Zilá Luz Paulino ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b INSTITUT DE BIOLOGIA MOLECULAR DE BARCELONA   (Spain)

Author keywords

Honeybee; LDLR; Lipophorin receptor; Ovary; Vitellogenin receptor

Indexed keywords

CELL RECEPTOR; CELL SURFACE RECEPTOR; EGG PROTEIN; INSECT PROTEIN; LIPOPHORIN RECEPTOR; VITELLOGENIN RECEPTOR;

GENE EXPRESSION; GENETIC ANALYSIS; HONEYBEE; POLYMERASE CHAIN REACTION;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; BEE; CHEMISTRY; CLASSIFICATION; FEMALE; GENE EXPRESSION REGULATION; GENETICS; MALE; METABOLISM; MOLECULAR GENETICS; PHYLOGENY; POLYMERASE CHAIN REACTION; PROTEIN TERTIARY STRUCTURE; SPECIES DIFFERENCE;

AMINO ACID SEQUENCE; ANIMALS; BEES; EGG PROTEINS; FEMALE; GENE EXPRESSION REGULATION; INSECT PROTEINS; MALE; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYMERASE CHAIN REACTION; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, CELL SURFACE; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SPECIES SPECIFICITY;

APIS MELLIFERA; HEXAPODA;

EID: 48549099661     PISSN: 00221910     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jinsphys.2008.04.021     Document Type: Article

References (51)

1. Albert S., Bhattacharya D., Klaudiny J., Schmitzová J., and Simúth J. The family of major royal jelly proteins and its evolution. Journal of Molecular Evolution 49 (1999) 290-297
2. Amdam G.V., and Omholt S.W. The hive bee to forager transition in honey bee colonies: the double repressor hypothesis. Journal of Theoretical Biology 223 (2003) 451-464
3. Amdam G.V., Norberg K., Hagen A., and Omholt S.W. Social exploitation of vitellogenin. Proceedings of the National Academy of Sciences of the United States of America 100 (2003) 1799-1802
4. Amdam G.V., Aase A.L., Seehuus S.C., Fondrk M.K., Norberg K., and Hartfelder K. Social reversal of immunosenescence in honey bee workers. Experimental Gerontology 40 (2005) 939-947
5. Amdam G.V., Csondes A., Fondrk M.K., and Page R.E. Complex social behaviour derived from maternal reproductive traits. Nature 439 (2006) 76-78
6. Amdam G.V., Nilsen K.A., Norberg K., Fondrk M.K., and Hartfelder K. Variation in endocrine signaling underlies variation in social life history. The American Naturalist 170 (2007) 37-46
7. Bitondi M.M.G., Nascimento A.M., Cunha A.D., Guidugli K.R., Nunes F.M.F., and Simões Z.L.P. Characterization and expression of the Hex 110 gene encoding a glutamine-rich hexamerin in the honey bee, Apis mellifera. Archives of Insect Biochemistry and Physiology 63 (2006) 57-72
8. Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17 (2000) 540-552
9. Chen J.S., Sappington T.W., and Raikhel A.S. Extensive sequence conservation among insect, nematode, and vertebrate vitellogenins reveals common ancestry. Journal of Molecular Evolution 44 (1997) 440-451
10. Chen M.E., Lewis D.K., Keeley L.L., and Pietrantonio P.V. cDNA cloning and transcriptional regulation of the vitellogenin receptor from the imported fire ant, Solenopsis invicta Buren (Hymenoptera: Formicidae). Insect Molecular Biology 13 (2004) 195-204
11. Cho K.-H., and Raikhel A.S. Organization and developmental expression of the mosquito vitellogenin receptor gene. Insect Molecular Biology 10 (2001) 465-474
12. Ciudad L., Piulachs M.D., and Bellés X. Systemic RNAi of the cockroach vitellogenin receptor results in a phenotype similar to that of the Drosophila yolkless mutant. FEBS Journal 273 (2006) 325-335
13. Ciudad L., Bellés X., and Piulachs M.D. Structural and RNAi characterization of the German cockroach lipophorin receptor, and the evolutionary relationships of lipoprotein receptors. BMC Molecular Biology 8 (2007) 53
14. Combet C., Blanchet C., Geourjon C., and Deléage G. NPS@: network protein sequence analysis. Trends in Biochemical Sciences 25 (2000) 147-150
15. Corona M., Velarde R.A., Remolina S., Moran-Lauter A., Wang Y., Hughes K.A., and Robinson G.E. Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. Proceedings of the National Academy of Sciences of the United States of America 104 (2007) 7128-7133
16. Drapeau M.D., Albert S., Kucharski R., Prusko C., and Maleszka R. Evolution of the Yellow/Major royal jelly protein family and the emergence of social behavior in honey bees. Genome Research 16 (2007) 1385-1394
17. Gopalapillai R., Kadono-Okuda K., Tsuchida K., Yamamoto K., Nohata J., Ajimura M., and Mita K. Lipophorin receptor from the silkworm, Bombyx mori: cDNA cloning, genomic structure, alternative splicing and isolation of a new isoform. Journal of Lipid Research 47 (2006) 1005-1013
18. Guidugli K.R., Piulachs M.D., Bellés X., Lourenço A.P., and Simões Z.L.P. Vitellogenin expression in queen ovaries and in larvae of both sexes of Apis mellifera. Archives of Insect Biochemistry and Physiology 59 (2005) 211-218
19. Guidugli K.R., Nascimento A.M., Amdam G.V., Barchuk A.R., Omholt S., Simões Z.L.P., and Hartfelder K. Vitellogenin regulates hormonal dynamics in the worker caste of a eusocial insect. FEBS Letters 579 (2005) 4961-4965
20. Guindon S., and Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52 (2003) 696-704
21. Hartfelder K., and Engels W. Social insect polymorphism: hormonal regulation of plasticity in development and reproduction in the honey bee. Current Topics in Developmental Biology 40 (1998) 45-77
22. Hartfelder K., Makert G.R., Judice C.C., Pereira G.A.G., Santana W.C., Dallacqua R., and Bitondi M.M.G. Physiological and genetic mechanisms underlying caste development, reproduction and division of labor in stingless bees. Apidologie 37 (2006) 144-163
23. Hiramatsu N., Chapman R.W., Lindzey J.K., Haynes M.R., and Sullivan C.V. Molecular characterization and expression of vitellogenin receptor from white perch (Morone americana). Biology of Reproduction 70 (2004) 1720-1730
24. Kawooya J.K., Osir E.O., and Law J.H. Uptake of the major hemolymph lipoprotein and its transformation in the insect egg. Journal of Biological Chemistry 263 (1988) 8740-8747
25. Lee C.S., Han J.H., Kim B.S., Lee S.M., Hwang J.S., Kang S.W., Lee B.H., and Kim H.R. Wax moth, Galleria mellonella, high density lipophorin receptor: alternative splicing, tissue-specific expression, and developmental regulation. Insect Biochemistry and Molecular Biology 33 (2003) 761-771
26. Lourenço A.P., Mackert A., Cristino A.S., and Simões Z.L.P. Validation of reference genes for gene expression studies in the honey bee, Apis mellifera, by quantitative real-time RT-PCR. Apidologie 39 (2008) 372-385
27. Makert G.R., Paxton R.J., and Hartfelder K. Ovariole number - a predictor of differential reproductive success among worker subfamilies in queenless honeybee (Apis mellifera L.) colonies. Behavioral Ecology and Sociobiology 60 (2006) 815-825
28. Mitchell III R.D., Ross E., Osgood C., Sonenshine D.E., Donohue K.V., Khalil S.M., Thompson D.M., and Roe R.M. Molecular characterization, tissue-specific expression and RNAi knockdown of the first vitellogenin receptor from a tick. Insect Biochemistry and Molecular Biology 37 (2007) 375-388
29. Nelson C.M., Ihle K.E., Fondrk M.K., Page R.E., and Amdam G.V. The gene vitellogenin has multiple coordinating effects on social organization. PLoS Biology 5 (2007) 673-677
30. Okabayashi K., Shoji H., Nakamura T., Hashimoto O., Asashima M., and Sugino H. cDNA cloning and expression of the Xenopus laevis vitellogenin receptor. Biochemical and Biophysical Research Communications 224 (1996) 406-413
31. Osborne P., and Dearden P. Non-radioactive in-situ hybridisation to honeybee embryos and ovaries. Apidologie 36 (2005) 113-118
32. Perazzolo L.M., Coward K., Davail B., Normand E., Tyler C.R., Pakdel F., Schneider W.J., and Le Menn F. Expression and localization of messenger ribonucleic acid for the vitellogenin receptor in ovarian follicles throughout oogenesis in the rainbow trout, Oncorhynchus mykiss. Biology of Reproduction 60 (1999) 1057-1068
33. Piulachs M.D., Guidugli K.R., Barchuk A.R., Cruz J., Simões Z.L.P., and Bellés X. The vitellogenin cDNA of the honey bee, Apis mellifera: structural analysis and expression studies. Insect Biochemistry and Molecular Biology 33 (2003) 459-465
34. Raikhel A.S., and Dhadialla T.S. Accumulation of yolk proteins in insect oocytes. Annual Review of Entomology 37 (1992) 217-251
35. Raikhel A.S., Brown M.R., and Bellés X. Hormonal control of reproductive processes. In: Gilbert L.I., Iatrou K., and Gill S.S. (Eds). Comprehensive Insect Molecular Science vol. 3 (2005), Elsevier, Amsterdam 433-491
36. Rodenburg K.W., Smolenaars M.M., Van Hoof D., and Van der Horst D.J. Sequence analysis of the non-recurring C-terminal domains shows that insect lipoprotein receptors constitute a distinct group of LDL receptor family members. Insect Biochemistry and Molecular Biology 36 (2006) 250-263
37. Sappington T.W., and Raikhel A.S. Molecular characteristics of insect vitellogenins and vitellogenin receptors. Insect Biochemistry and Molecular Biology 28 (1998) 277-300
38. Sappington T.W., Kokoza V.A., Cho W.L., and Raikhel A.S. Molecular characterization of the mosquito vitellogenin receptor reveals unexpected high homology to the Drosophila yolk protein receptor. Proceedings of the National Academy of Sciences of the United States of America 93 (1996) 8934-8939
39. Schonbaum C.P., Lee S., and Mahowald A.P. The Drosophila yolkless gene encodes a vitellogenin receptor belonging to the low density lipoprotein receptor superfamily. Proceedings of the National Academy of Sciences of the United States of America 92 (1995) 1485-1489
40. Schonbaum C.P., Perrino J.J., and Mahowald A.P. Regulation of the vitellogenin receptor during Drosophila melanogaster oogenesis. Molecular Biology of the Cell 11 (2000) 511-521
41. Seehuus S.C., Norberg K., Gimsa U., Krekling T., and Amdam G.V. Reproductive protein protects functionally sterile honey bee workers from oxidative stress. Proceedings of the National Academy of Sciences of the United States of America 103 (2006) 962-967
42. Seo S.J., Cheon H.M., Sun J., Sappington T.W., and Raikhel A.S. Tissue- and stage-specific expression of two lipophorin receptor variants with seven and eight ligand-binding repeats in adult mosquito. Journal of Biological Chemistry 278 (2003) 41954-41962
43. Sun J., Hiraoka T., Dittmer N.T., Cho K.H., and Raikhel A.S. Lipophorin as a yolk protein precursor in the mosquito, Aedes aegypti. Insect Biochemistry and Molecular Biology 30 (2000) 1161-1171
44. Tanaka E.D., and Hartfelder K. The initial stages of oogenesis and their relation to differential fertility in the honey bee (Apis mellifera) castes. Arthropod Structure & Development 33 (2004) 431-442
45. Tanaka E.D., Schmidt Capella I.C., and Hartfelder K. Cell death in the germline-mechanisms and consequences for reproductive plasticity in social bees. Brazilian Journal of Morphological Science 23 (2006) 15-26
46. The Honey Bee Genome Sequencing Consortium. Insights into social insects from the genome of the honey bee Apis mellifera. Nature 443 (2006) 931-949
47. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., and Higgins D.G. The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25 (1997) 4876-4882
48. Trenczek T.A., Zillikens A., and Engels W. Developmental patterns of vitellogenin haemolymph titre and rate of synthesis in adult drone honey bees (Apis mellifera). Journal of Insect Physiology 35 (1989) 475-481
49. Tufail M., and Takeda M. Molecular cloning, characterization and regulation of the cockroach vitellogenin receptor during oogenesis. Insect Molecular Biology 14 (2005) 389-401
50. Tufail M., and Takeda M. Molecular cloning and developmental expression pattern of the vitellogenin receptor from the cockroach, Leucophaea maderae. Insect Biochemistry and Molecular Biology 37 (2007) 235-245
51. Wheeler D.E., and Kawooya J.K. Purification and characterization of honey bee vitellogenin. Archives of Insect Biochemistry and Physiology 14 (1990) 253-267