Mitochondrial proteins differential expression during honeybee (Apis mellifera L.) queen and worker larvae caste determination

Journal of Proteome Research

Volumn 10, Issue 9, 2011, Pages 4263-4280

  Begna, Desalegn ^a   Fang, Yu ^a   Feng, Mao ^a   Li, Jianke ^a  

^a INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

honeybee; mitochondria; pathways; polymorphism; proteome

Indexed keywords

MESSENGER RNA; MITOCHONDRIAL PROTEIN; PROTEOME;

ARTICLE; BIOINFORMATICS; HONEYBEE; INSECT CASTE; LARVA; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; QUEEN (INSECT); REAL TIME POLYMERASE CHAIN REACTION; TWO DIMENSIONAL ELECTROPHORESIS; WORKER (INSECT);

ANIMALS; BEES; COMPUTATIONAL BIOLOGY; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMAGE PROCESSING, COMPUTER-ASSISTED; INSECT PROTEINS; LARVA; MASS SPECTROMETRY; MITOCHONDRIAL PROTEINS; PROTEOMICS; REAL-TIME POLYMERASE CHAIN REACTION; REPRODUCIBILITY OF RESULTS; SIGNAL TRANSDUCTION;

APIS MELLIFERA;

EID: 80052439444     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr200473a     Document Type: Article

References (62)

1. Michener, C. D. The Social Behavior of the Bees: A Comparative Study; Belknap Press: Cambridge, 1974; Vol. 73.
2. Wilson, E. O., Sociobiology: The New Synthesis; Harvard University Press: Cambridge, 1975.
3. Robinson, G. E.; Fahrbach, S. E.; Winston, M. L. Insect societies and the molecular biology of social behavior Bioessays 1997, 19 (12) 1099-1108 (Pubitemid 28012445)
4. Page, R. E., Jr.; Peng, C. Y. Aging and development in social insects with emphasis on the honey bee, Apis mellifera L Exp. Gerontol. 2001, 36 (4-6) 695-711 (Pubitemid 32273413)
5. Amdam, G. V.; Page, R. E., Jr. Intergenerational transfers may have decoupled physiological and chronological age in a eusocial insect Ageing Res. Rev. 2005, 4 (3) 398-408 (Pubitemid 41134194)
6. Wheeler, D. E. Developmental and physiological determinants of caste in social Hymenoptera: evolutionary implications Am. Nat. 1986, 128 (1) 13-34
7. West-Eberhard, M. J. Developmental Plasticity and Evolution; Oxford University Press: New York, 2003.
8. Seehuus, S. C.; Krekling, T.; Amdam, G. V. Cellular senescence in honey bee brain is largely independent of chronological age Exp. Gerontol. 2006, 41 (11) 1117-1125 (Pubitemid 44820717)
9. Cristino, A. S.; Nunes, F. M.; Lobo, C. H.; Bitondi, M. M.; Simoes, Z. L.; da Fontoura Costa, L.; Lattorff, H. M.; Moritz, R. F.; Evans, J. D.; Hartfelder, K. Caste development and reproduction: a genome-wide analysis of hallmarks of insect eusociality Insect Mol. Biol. 2006, 15 (5) 703-714 (Pubitemid 44652095)
10. Evans, J. D.; Wheeler, D. E. Expression profiles during honeybee caste determination. Genome Biol. 2001, 2 (1), reaearch0001.1-0001.6.
11. Rembold, H.; Kremer, J. P.; Ulrich, G. M. Characterization of postembryonic developmental stages of the female castes of the honey bee, Apis mellifera L Apidologie 1980, 11 (1) 29-38
12. Weaver, N. Effects of larval age on dimorphic differentiation of the female honey bee Ann. Entomol. Soc. Am. 1957, 50 (3) 283-294
13. Woyke, J. Correlations between the age at which honeybee brood was grafted, characteristics of the resultant queens, and results of insemination J. Apic. Res. 1971, 10 (1) 45-55
14. Barchuk, A. R.; Cristino, A. S.; Kucharski, R.; Costa, L. F.; Simoes, Z. L.; Maleszka, R. Molecular determinants of caste differentiation in the highly eusocial honeybee Apis mellifera BMC Dev. Biol. 2007, 7, 70
15. Corona, M.; Estrada, E.; Zurita, M. Differential expression of mitochondrial genes between queens and workers during caste determination in the honeybee Apis mellifera J. Exp. Biol. 1999, 202 (Pt 8) 929-938 (Pubitemid 29233404)
16. Corona, M.; Hughes, K. A.; Weaver, D. B.; Robinson, G. E. Gene expression patterns associated with queen honey bee longevity Mech. Ageing Dev. 2005, 126 (11) 1230-1238 (Pubitemid 41356525)
17. Chan, Q. W.; Howes, C. G.; Foster, L. J. Quantitative comparison of caste differences in honeybee hemolymph Mol. Cell. Proteomics 2006, 5 (12) 2252-2262 (Pubitemid 46043025)
18. Li, J.; Wu, J.; Begna Rundassa, D.; Song, F.; Zheng, A.; Fang, Y. Differential protein expression in honeybee (Apis mellifera L.) larvae: underlying caste differentiation PLoS One 2010, 5 (10) e13455
19. Green, D. R.; Reed, J. C. Mitochondria and apoptosis Science 1998, 281 (5381) 1309-1312 (Pubitemid 28406816)
20. Finkel, T.; Holbrook, N. J. Oxidants, oxidative stress and the biology of ageing Nature 2000, 408 (6809) 239-247
21. Henze, K.; Martin, W. Evolutionary biology: essence of mitochondria Nature 2003, 426 (6963) 127-128
22. Insights into social insects from the genome of the honeybee Apis mellifera. Nature 2006, 443 (7114), 931-949.
23. Lin, R. X.; Zhao, H. B.; Li, C. R.; Sun, Y. N.; Qian, X. H.; Wang, S. Q. Proteomic analysis of ionizing radiation-induced proteins at the subcellular level J. Proteome Res. 2009, 8 (1) 390-399
24. Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 1976, 72, 248-254
25. Li, J.; Li, H.; Zhang, Z.; Pan, Y. Identification of the proteome complement of high royal jelly producing bees (Apis mellifera) during worker larval development Apidologie 2007, 38 (6) 545-557 (Pubitemid 351282143)
26. Bindea, G.; Mlecnik, B.; Hackl, H.; Charoentong, P.; Tosolini, M.; Kirilovsky, A.; Fridman, W. H.; Pagès, F.; Trajanoski, Z.; Galon, J. ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks Bioinformatics 2009, 25 (8) 1091
27. Livak, K. J.; Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method Methods 2001, 25 (4) 402-408 (Pubitemid 34164012)
28. Andersen, J. S.; Mann, M. Organellar proteomics: turning inventories into insights EMBO Rep. 2006, 7 (9) 874-879 (Pubitemid 44523965)
29. Patton, W. F., Fluorescence detection of glycoproteins in gels and on electroblots. Curr. Protoc. Cell Biol. 2002, Chapter 6, Unit 6.8.
30. Phizicky, E. M.; Fields, S. Protein-protein interactions: methods for detection and analysis Microbiol. Rev. 1995, 59 (1) 94-123
31. Evans, J. D.; Wheeler, D. E. Differential gene expression between developing queens and workers in the honey bee, Apis mellifera Proc. Natl. Acad. Sci. U.S.A. 1999, 96 (10) 5575-5580 (Pubitemid 29234660)
32. Sardiello, M.; Licciulli, F.; Catalano, D.; Attimonelli, M.; Caggese, C. MitoDrome: a database of Drosophila melanogaster nuclear genes encoding proteins targeted to the mitochondrion Nucleic Acids Res. 2003, 31 (1) 322-324 (Pubitemid 36150395)
33. Liu, X.; Kiss, I.; Lengyel, J. A. Identification of genes controlling malpighian tubule and other epithelial morphogenesis in Drosophila melanogaster Genetics 1999, 151 (2) 685-695 (Pubitemid 29082936)
34. Galloni, M.; Edgar, B. A. Cell-autonomous and non-autonomous growth-defective mutants of Drosophila melanogaster Development 1999, 126 (11) 2365-2375 (Pubitemid 29299006)
35. Sun, X. H.; Tso, J. Y.; Lis, J.; Wu, R. Differential regulation of the two glyceraldehyde-3-phosphate dehydrogenase genes during Drosophila development Mol. Cell. Biol. 1988, 8 (12) 5200-5205
36. Steffan, J. S.; Minard, K. I.; McAlister-Henn, L. Expression and function of heterologous forms of malate dehydrogenase in yeast Arch. Biochem. Biophys. 1992, 293 (1) 93-102
37. Rieske, J. S. Composition, structure, and function of complex III of the respiratory chain Biochim. Biophys. Acta 1976, 456 (2) 195-247
38. Copeland, J. M.; Cho, J.; Lo, T., Jr.; Hur, J. H.; Bahadorani, S.; Arabyan, T.; Rabie, J.; Soh, J.; Walker, D. W. Extension of Drosophila life span by RNAi of the mitochondrial respiratory chain Curr. Biol. 2009, 19 (19) 1591-1598
39. Stroschein-Stevenson, S. L.; Foley, E.; O'Farrell, P. H.; Johnson, A. D. Identification of Drosophila gene products required for phagocytosis of Candida albicans PLoS Biol. 2006, 4 (1) e4
40. Lu, P.; Vogel, C.; Wang, R.; Yao, X.; Marcotte, E. M. Absolute protein expression profiling estimates the relative contributions of transcriptional and translational regulation Nat. Biotechnol. 2007, 25 (1) 117-124 (Pubitemid 46087910)
41. Rachinsky, A.; Strambi, C.; Strambi, A.; Hartfelder, K. Caste and metamorphosis: hemolymph titers of juvenile hormone and ecdysteroids in last instar honeybee larvae Gen. Comp. Endrocrinol. 1990, 79 (1) 31-38 (Pubitemid 20206161)
42. Yoshida, K. M.; Juni, N.; Hori, S. H. Molecular cloning and characterization of Drosophila ornithine aminotransferase gene Genes Genet. Syst. 1997, 72 (1) 9-17 (Pubitemid 27212975)
43. Tilghman, J. A.; Geer, B. W. The effects of a choline deficiency on the lipid composition and ethanol tolerance of Drosophila melanogaster Comp. Biochem. Physiol. C 1988, 90 (2) 439-444
44. Kucharski, R.; Maleszka, R. Arginine kinase is highly expressed in the compound eye of the honey bee, Apis mellifera Gene 1998, 211 (2) 343-349 (Pubitemid 28230347)
45. Thorpe, C.; Kim, J. J. Structure and mechanism of action of the acyl-CoA dehydrogenases FASEB J. 1995, 9 (9) 718-725
46. Hasegawa, M.; Asanuma, S.; Fujiyuki, T.; Kiya, T.; Sasaki, T.; Endo, D.; Morioka, M.; Kubo, T. Differential gene expression in the mandibular glands of queen and worker honeybees, Apis mellifera L.: implications for caste-selective aldehyde and fatty acid metabolism Insect Biochem. Mol. Biol. 2009, 39 (10) 661-667
47. Torroja, L.; Ortuno-Sahagun, D.; Ferrus, A.; Hammerle, B.; Barbas, J. A. scully, an essential gene of Drosophila, is homologous to mammalian mitochondrial type II L-3-hydroxyacyl-CoA dehydrogenase/amyloid-beta peptide-binding protein J. Cell Biol. 1998, 141 (4) 1009-1017 (Pubitemid 28243967)
48. Xun, Z.; Sowell, R. A.; Kaufman, T. C.; Clemmer, D. E. Protein expression in a Drosophila model of Parkinson's disease J. Proteome Res. 2007, 6 (1) 348-357 (Pubitemid 46173686)
49. Feng, M.; Fang, Y.; Li, J. Proteomic analysis of honeybee worker (Apis mellifera) hypopharyngeal gland development BMC Genomics 2009, 10, 645
50. Jianke, L.; Mao, F.; Begna, D.; Yu, F.; Aijuan, Z. Proteome comparison of hypopharyngeal gland development between Italian and royal jelly producing worker honeybees (Apis mellifera L.) J. Proteome Res. 2010, 9 (12) 6578-6594
51. Eveleth, D. D., Jr; Marsh, J. L. Sequence and expression of the Cc gene, a member of the dopa decarboxylase gene cluster of Drosophila: possible translational regulation Nucleic Acids Res. 1986, 14 (15) 6169-6183
52. Li, J.; Fang, Y.; Zhang, L.; Begna, D. Honeybee (Apis mellifera ligustica) drone embryo proteomes J. Insect Physiol. 2011, 57 (3) 372-384
53. Park, J.; Kim, Y.; Choi, S.; Koh, H.; Lee, S. H.; Kim, J. M.; Chung, J. Drosophila Porin/VDAC affects mitochondrial morphology PLoS One 2010, 5 (10) e13151
54. Koc, E. C.; Burkhart, W.; Blackburn, K.; Moseley, A.; Koc, H.; Spremulli, L. L. A proteomics approach to the identification of mammalian mitochondrial small subunit ribosomal proteins J. Biol. Chem. 2000, 275 (42) 32585-32591
55. Goshima, G.; Wollman, R.; Goodwin, S. S.; Zhang, N.; Scholey, J. M.; Vale, R. D.; Stuurman, N. Genes required for mitotic spindle assembly in Drosophila S2 cells Science 2007, 316 (5823) 417-421 (Pubitemid 46651486)
56. Ni, J. Q.; Liu, L. P.; Hess, D.; Rietdorf, J.; Sun, F. L. Drosophila ribosomal proteins are associated with linker histone H1 and suppress gene transcription Genes Dev. 2006, 20 (14) 1959-1973 (Pubitemid 44079332)
57. Spradling, A. C.; Stern, D.; Beaton, A.; Rhem, E. J.; Laverty, T.; Mozden, N.; Misra, S.; Rubin, G. M. The Berkeley Drosophila Genome Project gene disruption project: Single P-element insertions mutating 25% of vital Drosophila genes Genetics 1999, 153 (1) 135-177 (Pubitemid 29434774)
58. Sies, H. Oxidative stress: oxidants and antioxidants Exp. Physiol. 1997, 82 (2) 291-295 (Pubitemid 27182306)
59. Vertuani, S.; Angusti, A.; Manfredini, S. The antioxidants and pro-antioxidants network: an overview Curr. Pharm. Des. 2004, 10 (14) 1677-1694 (Pubitemid 38559778)
60. Li, J.; Zhang, L.; Feng, M.; Zhang, Z.; Pan, Y. Identification of the proteome composition occurring during the course of embryonic development of bees (Apis mellifera) Insect Mol. Biol. 2009, 18 (1) 1-9
61. Baer, B.; Eubel, H.; Taylor, N. L.; O'Toole, N.; Millar, A. H. Insights into female sperm storage from the spermathecal fluid proteome of the honeybee Apis mellifera Genome Biol. 2009, 10 (6) R67
62. Dreger, M. Proteome analysis at the level of subcellular structures Eur. J. Biochem. 2003, 270 (4) 589-599 (Pubitemid 36286572)