Insulin-like peptide genes in honey bee fat body respond differently to manipulation of social behavioral physiology

Journal of Experimental Biology

Volumn 214, Issue 9, 2011, Pages 1488-1497

  Nilsen, Kari Anne ^a   Ihle, Kate E ^b   Frederick, Katy ^b   Fondrk, M Kim ^b   Smedal, Bente ^a   Hartfelder, Klaus ^c   Amdam, Gro V ^a,b  

^a NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^b ARIZONA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Division of labor; Nutrition; Peripheral insulin like signaling; RNA interference; Vitellogenin

Indexed keywords

ALBUMINOID; AMINO ACID; INSULIN; JUVENILE HORMONE; MESSENGER RNA; VITELLOGENIN;

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; BEE; BIOLOGICAL MODEL; CYTOLOGY; DRUG EFFECT; FAT BODY; FLUORESCENT ANTIBODY TECHNIQUE; GENE; GENE EXPRESSION REGULATION; GENETICS; HEMOLYMPH; HONEY; METABOLISM; PHYSIOLOGY; REPRODUCIBILITY; SOCIAL BEHAVIOR; TITRIMETRY;

ALBUMINS; AMINO ACIDS; ANIMALS; BEES; BEHAVIOR, ANIMAL; FAT BODY; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; GENES, INSECT; HEMOLYMPH; HONEY; INSULIN; JUVENILE HORMONES; MODELS, BIOLOGICAL; REPRODUCIBILITY OF RESULTS; RNA, MESSENGER; SOCIAL BEHAVIOR; TITRIMETRY; VITELLOGENINS;

APIS MELLIFERA; APOIDEA; HEXAPODA; INVERTEBRATA; MAMMALIA;

EID: 79955045942     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.050393     Document Type: Article

References (57)

1. Amdam, G. V. (2011). Social context, stress, and plasticity of aging. Aging Cell 10, 18-27.
2. Amdam, G. V. and Omholt, S. W. (2003). The hive bee to forager transition in honeybee colonies: the double repressor hypothesis. J. Theor. Biol. 223, 451-464. (Pubitemid 36875741)
3. Amdam, G. V., Norberg, K., Fondrk, M. K. and Page, R. E. J. (2004). Reproductive ground plan may mediate colony-level selection effects on individual foraging behavior in honey bees. Proc. Natl. Acad. Sci. USA 101, 11350-11355. (Pubitemid 39038350)
4. Amdam, G. V., Aase, A. L., Seehuus, S. C., Kim Fondrk, M., Norberg, K. and Hartfelder, K. (2005). Social reversal of immunosenescence in honey bee workers. Exp. Gerontol. 40, 939-947. (Pubitemid 41682394)
5. Amdam, G. V., Nilsen, K. A., Norberg, K., Fondrk, M. K. and Hartfelder, K. (2007). Variation in endocrine signaling underlies variation in social life history. Am Nat. 170, 37-46. (Pubitemid 46984575)
6. Amdam, G. V., Ihle, K. E. and Page, R. E., Jr (2009). Regulation of honey bee worker (Apis mellifera) life histories by vitellogenin. In Hormones, Brain, and Behavior, Vol. 4 (ed. D. Pfaff, A. Arnold, A. Etgen, S. Fahrbach and R. Rubin), pp. 1003-1025. San Diego, CA: Elsevier Academic Press.
7. Ament, S. A., Corona, M., Pollock, H. S. and Robinson, G. E. (2008). Insulin signaling is involved in the regulation of worker division of labor in honey bee colonies. Proc. Natl. Acad. Sci. USA 105, 4226-4231. (Pubitemid 351754362)
8. Ament, S. A., Wang, Y. and Robinson, G. E. (2010). Nutritional regulation of division of labor in honey bees: toward a systems biology perspective. Wiley Interdiscip. Rev. Syst. Biol. Med. 2, 566-576.
9. Badisco, L., Claeys, I., Van Hiel, M., Clynen, E., Huybrechts, J., Vandersmissen, T., Van Soest, S., Vanden Bosch, L., Simonet, G. and Vanden Broeck, J. (2008). Purification and characterization of an insulin-related peptide in the desert locust, Schistocerca gregaria: immunolocalization, cDNA cloning, transcript profiling and interaction with neuroparsin. J. Mol. Endocrinol. 40, 137-150. (Pubitemid 351586823)
10. Bitondi, M. M. G. and Simoes, Z. L. P. (1996). The relationship between level of pollen in the diet, vitellogenin and juvenile hormone titres in Africanized Apis mellifera workers. J. Apic. Res. 35, 27-36.
11. Broughton, S. and Partridge, L. (2009). Insulin/IGF-like signalling, the central nervous system and aging. Biochem. J. 418, 1-12.
12. Chen, Y. P., Higgens, J. A. and Feldlaufer, M. F. (2005). Quantitative real-time reverse transcription-PCR analysis of deformed wing virus infection in the honeybee (Apis mellifera L.) Appl. Environ. Microb. 71, 436-441. (Pubitemid 40116299)
13. Clemmons, D. R. and Underwood, L. E. (1991). Nutritional regulation of IGF-I and IGF binding proteins. Annu. Rev. Nutr. 11, 393-412. (Pubitemid 21903836)
14. Corona, M., Velarde, R. A., Remolina, S., Moran-Lauter, A., Wang, Y., Hughes, K. A. and Robinson, G. E. (2007). Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. Proc. Natl. Acad. Sci. USA 104, 7128-7133. (Pubitemid 47186020)
15. de Azevedo, S. V. and Hartfelder, K. (2008). The insulin signaling pathway in honey bee (Apis mellifera) caste development-differential expression of insulin-like peptides and insulin receptors in queen and worker larvae. J. Insect Physiol. 54, 1064-1071.
16. Dettloff, M., Kaiser, B. and Wiesner, A. (2001). Localization of injected apolipophorin III in vivo - new insights into the immune activation process directed by this protein. J. Insect Physiol. 47, 789-797. (Pubitemid 32489068)
17. Elekonich, M. M. and Roberts, S. P. (2005). Honey bees as a model for understanding mechanisms of life history transitions. Comp. Biochem. Physiol. 141A, 362-371. (Pubitemid 41225431)
18. Flatt, T., Tu, M. P. and Tatar, M. (2005). Hormonal pleiotropy and the juvenile hormone regulation of Drosophila development and life history. BioEssays 27, 999-1010. (Pubitemid 41608957)
19. Fluri, P., Wille, H., Gerig, L. and Luscher, M. (1977). Juvenile hormone, vitellogenin, and hemocyte composition in winter worker honeybees (Apis mellifera). Experientia 33, 1240-1241. (Pubitemid 8175838)
20. Fluri, P., Luscher, M., Wille, H. and Gerig, L. (1982). Changes in weight of the pharyngeal gland and hemolymph titers of juvenile-hormone, protein and vitellogenin in worker bees. J. Insect Physiol. 28, 61-68.
21. Goodman, W., O'Hern, P. A., Zaugg, R. H. and Gilbert, L. I. (1978). Purification and characterization of a juvenile hormone binding protein from the hemolymph of the fourth instar tobacco hornworm, Manduca sexta. Mol. Cell. Endocrinol. 11, 225-242.
22. Goodman, W. G., Coy, D. C., Baker, F. C., Xu, L. and Toong, Y. C. (1990). Development and application of a radioimmunoassay for the juvenile hormones. Insect Biochem. (USA) 20, 357-364.
23. Grönke, S., Clarke, D.-F., Broughton, S., Andrews, T. D. and Partridge, L (2010). Molecular evolution and functional characterization of Drosophila insulin-like peptides. PLoS Genet. 6, e1000857.
24. Guidugli, K. R., Nascimento, A. M., Amdam, G. V., Barchuk, A. R., Omholt, S., Simoes, Z. L. and Hartfelder, K. (2005). Vitellogenin regulates hormonal dynamics in the worker caste of a eusocial insect. FEBS Lett. 579, 4961-4965. (Pubitemid 41242836)
25. Gutierrez, E., Wiggins, D., Fielding, B. and Gould, A. P. (2007). Specialized hepatocyte-like cells regulate Drosophila lipid metabolism. Nature 445, 275-280. (Pubitemid 46122810)
26. Harrison, J. F. and Fewell, J. H. (2002). Environmental and genetic influences on flight metabolic rate in the honey bee, Apis mellifera. Physiol. A. Mol. Integr. Physiol. 133, 323-333. (Pubitemid 35223193)
27. Haydak, M. H. (1970). Honey bee nutrition. Annu. Rev. Entomol. 15, 143-156.
28. Huang, Z. Y. and Robinson, G. E. (1995). Seasonal changes in juvenile hormone titers and rates of biosynthesis in honey bees. J. Comp. Physiol. B 165, 18-28.
29. Huang, Z. Y., Robinson, G. E. and Borst, D. W. (1994). Physiological correlates of division of labor among similarly aged honey bees. J. Comp. Physiol. A 174, 731-739. (Pubitemid 2087096)
30. Ihle, K. E., Page, R. E., Jr, Frederick, K., Fondrk, M. K. and Amdam, G. V. (2010). Genotype effect on regulation of behaviour by vitellogenin supports reproductive origin of honeybee foraging bias. Anim. Behav. 79, 1001-1006.
31. Landim, C. D. C. (1985). Histological and cytological studies on the fat body of the queen honeybee abdomen during the active oviposition phase. Rev. Bras. Biol. 45, 221-232.
32. Lourenco, A. P., Mackert, A., Cristino, A. D. and Simoes, Z. L. P. (2008). Validation of reference genes for gene expression studies in the honey bee, Apis mellifera, by quantitative real-time RT-PCR. Apidologie 39, 372-385. (Pubitemid 351754631)
33. Marco Antonio, D. S., Guidugli-Lazzarini, K. R., do Nascimento, A. M., Simoes, Z. L. and Hartfelder, K. (2008). RNAi-mediated silencing of vitellogenin gene function turns honeybee (Apis mellifera) workers into extremely precocious foragers. Naturwissenschaften 95, 953-961.
34. Mayer, R. J. and Candy, D. J. (1969). Control of haemolymph lipid concentration during locust flight: an adipokinetic hormone from the corpora cardiaca, J. Insect Physiol. 15, 611-620.
35. Murphy, C. T., McCarroll, S. A., Bargmann, C. I., Fraser, A., Kamath, R. S., Ahringer, J., Li, H. and Kenyon, C. (2003). Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature 424, 277-283.
36. Nelson, C. M., Ihle, K. E., Fondrk, M. K., Page, R. E. and Amdam, G. V. (2007). The gene vitellogenin has multiple coordinating effects on social organization. PLoS Biol. 5, e62.
37. Orth, A. P., Doll, S. C. and Goodman, W. G. (2003). Sequence, structure and expression of the hemolymph juvenile hormone binding protein gene in the tobacco hornworm, Manduca sexta. Insect Biochem.?Mol.?Biol. 33, 93-102. (Pubitemid 35431531)
38. Osborn, P. and Dearden, P. K. (2005). Non-radioactive in situ hybridisation to honey bee embryos and ovaries. Apidologie 36, 113-116.
39. Paes-de-Oliveira, V. T. P. and Cruz-Landim, C. (2003). Morphology and function of insect fat body cells: a review. Biociencias 11, 195-205.
40. Paes-de-Oliveira, V. T., Poiani, S. B., Antonialli, W. F. and da Cruz-Landim, C. (2008). Morphometric changes on honey bee Apis mellifera L. workers fat body cells after juvenile hormone topic application at emergence. Micron 39, 426-430. (Pubitemid 351721015)
41. Pan, M. L. and Telfer, W. H. (1992). Selectivity in storage hexamerin clearing demonstrated with hemolymph transfusions between Hyalophora cecropia and Actias luna. Arch. Insect Biochem. Physiol. 19, 203-221.
42. Park, Y. C., Tesch, M. J., Toong, Y. C. and Goodman, W. G. (1993). Affinity purification and binding analysis of the hemolymph juvenile hormone binding protein from Manduca sexta. Biochemistry. 32, 7909-7915. (Pubitemid 23259646)
43. Patel, A., Fondrk, M. K., Kaftanoglu, O., Emore, C., Hunt, G., Frederick, K. and Amdam, G. V. (2007). The making of a queen: TOR pathway is a key player in diphenic caste development. PLoS ONE 2, e509.
44. Pierce, S. B., Costa, M., Wisotzkey, R., Devadhar, S., Homburger, S. A., Buchman, A. R., Ferguson, K. C., Heller, J., Platt, D. M., Pasquinelli, A. et al. (2001). Regulation of DAF-2 receptor signaling by human insulin and ins-1, a member of the unusually large and diverse C. elegans insulin gene family. Genes Dev. 15, 672-686. (Pubitemid 32244897)
45. Pinto, L. Z., Bitondi, M. M. and Simoes, Z. L. (2000). Inhibition of vitellogenin synthesis in Apis mellifera workers by a juvenile hormone analogue, pyriproxyfen. J. Insect Physiol. 46, 153-160. (Pubitemid 30022279)
46. Robinson, G. E., Strambi, C., Strambi, A. and Huang, Z. Y. (1992). Reproduction in worker honey-bees is associated with low juvenile-hormone titers and rates of biosynthesis. Gen. Comp. Endocr. 87, 471-480.
47. Scharlaken, B., de Graaf, D. C., Goossens, K., Brunain, M., Peelman, L. J. and Jacobs, F. J. (2008). Reference gene selection for insect expression studies using quantitative real-time PCR: the head of the honeybee, Apis mellifera, after a bacterial challenge. J. Insect Sci. 8:33, available online: insectscience.org/8.33.
48. Seehuus, S. C., Norberg, K., Gimsa, U., Krekling, T. and Amdam, G. V. (2006). Reproductive protein protects functionally sterile honey bee workers from oxidative stress. Proc. Natl. Acad. Sci. USA 103, 962-967. (Pubitemid 43212204)
49. Seehuus, S. C., Norberg, K., Krekling, T., Fondrk, K. and Amdam, G. V. (2007). Immunogold localization of vitellogenin in the ovaries, hypopharyngeal glands and head fat bodies of honeybee workers, Apis mellifera. J. Insect Physiol. 7, 52.
50. Seeley, T. D. (1982). Adaptive significance of the age polyethism schedule in honeybee colonies. Behav. Ecol. Sociobiol. 11, 287-293.
51. Smedal, B., Brynem, M., Kreibich, C. D. and Amdam, G. V. (2009). Brood pheromone suppresses physiology of extreme longevity in honeybees (Apis mellifera). J. Exp. Biol. 212, 3795-3801.
52. Sullivan, J. P., Fahrbach, S. E., Harrison, J. F., Capaldi, E. A., Fewell, J. H. and Robinson, G. E. (2003). Juvenile hormone and division of labor in honey bee colonies: effects of allatectomy on flight behavior and metabolism. J. Exp. Biol. 206, 2287-2296. (Pubitemid 36821524)
53. Toth, A. L. and Robinson, G. E. (2005). Worker nutrition and division of labour in honeybees. Anim. Behav. 69, 427-435. (Pubitemid 40084841)
54. Tsuruda, J. M., Amdam, G. V. and Page, R. E. J. (2008). Sensory response system of social behavior tied to female reproductive traits. PLoS ONE 3, e3397.
55. Wang, Y., Mutti, N. S., Ihle, K. E., Siegel, A., Dolezal, A. G., Kaftanoglu, O. and Amdam, G. V. (2010). Down-regulation of honey bee IRS gene biases behavior toward food rich in protein. PLoS Genet. 6, e1000896.
56. Weinstock, G. M., Robinson, G. E., Gibbs, R. A., Worley, K. C., Evans, J. D., Maleszka, R., Robertson, H. M., Weaver, D. B., Beye, M., Bork, P. et al. (2006). Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443, 931-949. (Pubitemid 44646165)
57. Wolschin, F. and Amdam, G. V. (2007). Plasticity and robustness of protein patterns during reversible development in the honey bee (Apis mellifera). Anal. Bioanal. Chem. 389, 1095-1100. (Pubitemid 47482258)