Abstract
Queen honeybees (Apis mellifera) have much longer lifespans than worker bees. Although the expression of age-related molecules in the trophocytes and fat cells of young and old workers have been determined, the expression of age-related molecules in queens is unknown. In this study, we examined the expression of age-related molecules in the trophocytes and fat cells of young and old queens. Molecular analyses detected no differences in telomerase activity or telomere lengths between trophocytes and fat cells from young and old queens, indicating that these cells do not divide in adulthood. Further assays showed that old queens has higher non-homogeneous cellular morphology, senescence-associated β-galactosidase (SA-β-Gal) activity, accumulation of lipofuscin granules, lipid peroxidation, and protein oxidation compared to young queens. These results demonstrate that age-related molecules can be used to evaluate aging in the trophocytes and fat cells of queens and to lay the foundation for further study of the mechanisms that delay cellular aging in the trophocytes and fat cells of queens.
Similar content being viewed by others
References
Almeida, H., Magalhães, M.C., Magalhães, M.M. (1998) Age-related changes in lipid peroxidation products in rat adrenal gland. Age 21, 119–121
Amdam, G.V., Page, R.E. (2005) Intergenerational transfers may have decoupled physiological and chronological age in a eusocial insect. Ageing Res. Rev. 4, 398–408
Amdam, G.V., Simões, Z.L.P., Hagen, A., Norberg, K., Schrøder, K., Mikkelsen, Ø., Kirkwood, T.B.L., Omholt, S.W. (2004) Hormonal control of the yolk precursor vitellogenin regulates immune function and longevity in honeybees. Exp. Gerontol. 39, 767–773
Argyle, D., Ellsmore, V., Gault, E.A., Munro, A.F., Nasir, L. (2003) Equine telomeres and telomerase in cellular immortalisation and ageing. Mech. Ageing Dev. 124, 759–764
Brunk, U.T., Terman, A. (2002) Lipofuscin: Mechanisms of age-related accumulation and influence on cell functions. Free Radic. Biol. Med. 33, 611–619
Camazine, S. (1991) Self-organizing pattern formation on the combs of honey bee colonies. Behav. Ecol. Sociobiol. 28, 61–76
Collins, A.M., Williams, V., Evans, J.D. (2004) Sperm storage and antioxidative enzyme expression in the honey bee, Apis mellifera. Insect Mol. Biol. 13, 141–146
Corona, M., Velarde, R.A., Remolina, S., Moran-Lauter, A., Wang, Y., Hughes, K.A., Robinson, G.E. (2007) Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. Proc. Natl. Acad. Sci. USA 104, 7128–7133
Das, N., Levine, R.L., Orr, W.C., Sohal, R.S. (2001) Selectivity of protein oxidative damage during aging in Drosophila melanogaster. Biochem. J. 360, 209–216
Davis, T., Skinner, J.W., Faragher, R.G., Jones, C.J., Kipling, D. (2005) Replicative senescence in sheep fibroblasts is a p53 dependent process. Exp. Gerontol. 40, 17–26
Dimri, G.P., Lee, X., Basile, G., Acosta, M., Scott, G., Roskelley, C., Medrano, E.E., Linskens, M., Rubelj, I., Pereira-Smith, O., Peacocke, M., Campisi, J. (1995) A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc. Natl. Acad. Sci. USA 92, 9363–9367
Draper, H.H., Hadley, M. (1990) Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol. 86, 421–431
Draper, H.H., McGirr, L.G., Hadley, M. (1986) The metabolism of malondialdehyde. Lipids 21, 305–307
Genade, T., Benedetti, M., Terzibasi, E., Roncaglia, P., Valenzano, D.R., Cattaneo, A., Cellerino, A. (2005) Annual fishes of the genus Nothobranchius as a model system for aging research. Aging Cell 4, 223–233
Hastings, R., Li, N.C., Lacy, P.S., Patel, H., Herbert, K.E., Stanley, A.G., Williams, B. (2004) Rapid telomere attrition in cardiac tissue of the ageing Wistar rat. Exp. Gerontol. 39, 855–857
Hsieh, Y.S., Hsu, C.Y. (2011) Honeybee trophocytes and fat cells as target cells for cellular senescence studies. Exp. Gerontol. 46, 233–240
Hsu, C.Y. (2004) The processes of iron deposition in the common hornet (Vespa affinis). Biol. Cell 96, 529–537
Hsu, C.Y., Chiu, Y.C. (2009) Ambient temperature influences aging in an annual fish (Nothobranchius rachovii). Aging Cell 8, 726–737
Hsu, C.Y., Li, C.W. (1993) The ultrastructure and formation of iron granules in the honeybee (Apis mellifera). J. Exp. Biol. 180, 1–13
Hsu, C.Y., Chiu, Y.C., Hsu, W.L., Chan, Y.P. (2008) Age-related markers assayed at different developmental stages of the annual fish Nothobranchius rachovii. J. Gerontol. A Biol. Sci. Med. Sci. 63A, 1267–1276
Inal, M.E., Kanbak, G., Sunal, E. (2001) Antioxidant enzyme activities and malondialdehyde levels related to aging. Clin. Chim. Acta 305, 75–80
Jemielity, S., Keller, L. (2007) Aging: a young mind in old bees. Curr. Biol. 17, R294–R295
Jemielity, S., Kimura, M., Parker, K.M., Parker, J.D., Cao, X., Aviv, A., Keller, L. (2007) Short telomeres in short-lived males: what are the molecular and evolutionary causes? Aging Cell 6, 225–233
Kim, N.W., Wu, F. (1997) Advances in quantification and characterization of telomerase activity by the telomeric repeat amplification protocol (TRAP). Nucleic Acids Res. 25, 2595–2597
Kishi, S., Uchiyama, J., Baughman, A., Goto, T., Lin, M., Tsai, S. (2003) The zebrafish as a vertebrate model of functional aging and very gradual senescence. Exp. Gerontol. 38, 777–786
Kurz, D.J., Decary, S., Hong, Y., Erusalimsky, J.D. (2000) Senescence-associated β-galactosidase reflects an increase in lysosomal mass during replicative ageing of human endothelial cells. J. Cell Sci. 113, 3613–3622
Lindsey, J., McGill, N.I., Lindsey, L.A., Green, D.K., Cooke, H.J. (1991) In vivo loss of telomeric repeats with age in humans. Mutat. Res. 256, 45–48
Lorite, P., Carrillo, J.A., Palomeque, T. (2002) Conservation of (TTAGG)n Telomeric sequences among ants (Hymenoptera, Formicidae). J. Hered. 93, 282–285
Mecocci, P., Fano, G., Fulle, S., MacGarvey, U., Shinobu, L., Polidori, M.C., Cherubini, A., Vecchirt, J., Senin, U., Beal, M.F. (1999) Age-dependent increase in oxidative damage to DNA, lipids, and proteins in human skeletal muscle. Free Radic. Biol. Med. 26, 303–308
Moyzis, R.K., Buckingham, J.M., Cram, L.S., Dani, M., Deaven, L.L., Jones, M.D., Meyne, J., Ratliff, R.L., Wu, J.R. (1988) A highly conserved repetitive DNA sequence, (TTAGGG)n, present at the telomeres of human chromosomes. Proc. Natl. Acad. Sci. USA 85, 6622–6626
Nakano, M., Oenzil, F., Mizuno, T., Gotoh, S. (1995) Age-related changes in the lipofuscin accumulation of brain and heart. Gerontology 41, 69–79
Nasir, L., Devlin, P., McKevitt, T., Rutteman, G., Argyle, D.J. (2001) Telomere lengths and telomerase activity in dog tissues: a potential model system to study human telomere and telomerase biology. Neoplasia 3, 351–359
Neukirch, A. (1982) Dependence of the lifespan of the honeybee (Apis mellifera) upon flight performance and energy consumption. J. Comp. Physiol. 146, 35–40
Okazaki, S., Tsuchida, K., Maekawa, H., Ishikawa, H. (1993) Identification of a pentanucleotide telomeric sequence, (TTAGG)n, in the silkworm Bombyx mori and in other insects. Mol. Cell. Biol. 13, 1424–1432
Oliver, C.N., Ahn, B.W., Moerman, E.J., Goldstein, S., Stadtman, E.R. (1987) Age-related changes in oxidized proteins. J. Biol. Chem. 262, 5488–5491
Omholt, S.W., Amdam, G.V. (2004) Epigenic regulation of aging in honeybee workers. Aging Knowl. Environ. 26, pe28
Osanai, M., Kojima, K.K., Futahashi, R., Yaguchi, S., Fujiwara, H. (2006) Identification and characterization of the telomerase reverse transcriptase of Bombyx mori (silkworm) and Tribolium castaneum (flour beetle). Gene 376, 281–289
Ozawa, T. (1997) Genetic and functional changes in mitochondria associated with aging. Physiol. Rev. 77, 425–464
Page, R.E., Peng, C.Y.S. (2001) Aging and development in social insects with emphasis on the honey bee, Apis mellifera L. Exp. Gerontol. 36, 695–711
Remolina, S.C., Hughes, K.A. (2008) Evolution and mechanisms of long life and high fertility in queen honey bees. Age 30, 177–185
Remolina, S.C., Hafez, D.M., Robinson, G.E., Hughes, K.A. (2007) Senescence in the worker honey bee Apis mellifera. J. Insect Physiol. 53, 1027–1033
Richter, C. (1995) Oxidative damage to mitochondrial DNA and its relationship to ageing. Int. J. Biochem. Cell Biol. 27, 647–653
Robertson, H.M., Gordon, K.H.J. (2006) Canonical TTAGG-repeat telomeres and telomerase in the honey bee, Apis mellifera. Genome Res. 16, 1345–1351
Rueppell, O., Christine, S., Mulcrone, C., Groves, L. (2007a) Aging without functional senescence in honey bee workers. Curr. Biol. 17, R274–R275
Rueppell, O., Bachelier, C., Fondrk, M.K., Page Jr., R.E. (2007b) Regulation of life history determines lifespan of worker honey bees (Apis mellifera L.). Exp. Gerontol. 42, 1020–1032
Sahara, K., Marec, F., Traut, W. (1999) TTAGG telomeric repeats in chromosomes of some insects and other arthropods. Chromosome Res. 7, 449–460
Sasaki, T., Fujiwara, H. (2000) Detection and distribution patterns of telomerase activity in insects. Eur. J. Biochem. 267, 3025–3031
Seehuus, S.C., Krekling, T., Amdam, G.V. (2006a) Cellular senescence in honey bee brain is largely independent of chronological age. Exp. Gerontol. 41, 1117–1125
Seehuus, S.C., Norberg, K., Gimsa, U., Krekling, T., Amdam, G.V. (2006b) Reproductive protein protects functionally sterile honey bee workers from oxidative stress. Proc. Natl. Acad. Sci. USA 103, 962–967
Sitte, N., Merker, M., von Zglinicki, T., Davies, K.J.A., Grune, T. (2000a) Protein oxidation and degradation during cellular senescence of human BJ fibroblasts: part I-effects of proliferative senescence. FASEB J. 14, 2495–2502
Sitte, N., Merker, M., von Zglinicki, T., Davies, K.J.A., Grune, T. (2000b) Protein oxidation and degradation during cellular senescence of human BJ fibroblasts: part II-aging of nondividing cells. FASEB J. 14, 2503–2510
Sohal, R.S., Agarwal, S., Dubey, A., Orr, W.C. (1993) Protein oxidative damage is associated with life expectancy of houseflies. Proc. Natl. Acad. Sci. USA 90, 7255–7259
Terman, A., Brunk, U.T. (1998a) On the degradability and exocytosis of ceroid/lipofuscin in cultured rat cardiac myocytes. Mech. Ageing Dev. 100, 145–156
Terman, A., Brunk, U.T. (1998b) Ceroid/lipofuscin formation in cultured human fibroblasts: The role of oxidative stress and lysosomal proteolysis. Mech. Ageing Dev. 104, 277–291
Tian, L., Cai, Q., Wei, H. (1998) Alterations of antioxidant enzymes and oxidative damage to macromolecules in different organs of rats during aging. Free Radic. Biol. Med. 24, 1477–1484
Tofilski, A. (2000) Senescence and learning in honeybee (Apis mellifera) workers. Acta Neurobiol. Exp. 60, 35–39
van der Loo, B., Fenton, M.J., Erusalimsky, J.D. (1998) Cytochemical detection of a senescence-associated b-galactosidase in endothelial and smooth muscle cells from human and rabbit blood vessels. Exp. Cell Res. 241, 309–315
Ward, K.N., Coleman, J.L., Clinnin, K., Fahrbach, S., Rueppell, O. (2008) Age, caste, and behavior determine the replicative activity of intestinal stem cells in honeybees (Apis mellifera L.). Exp. Gerontol. 43, 530–537
Weirich, G.F., Collins, A.M., Williams, V.P. (2002) Antioxidant enzymes in the honey bee, Apis mellifera. Apidologie 33, 3–14
Welis-Knecht, M.C., Huggins, T.G., Dyer, G., Thorpe, S.R., Baynes, J.W. (1993) Oxidized amino acids in lens protein with age. J. Biol. Chem. 268, 12348–12352
Williams, J.B., Roberts, S.P., Elekonich, M.M. (2008) Age and natural metabolically-intensive behavior affect oxidative stress and antioxidant mechanisms. Exp. Gerontol. 43, 538–549
Winston, M.L. (1987) The biology of the honey bee. Harvard University Press, Cambridge, MA
Wright, W.E., Piatysek, M.A., Rainey, W.E., Byrd, W., Shay, J.W. (1996) Telomerase activity in human germline and embryonic tissues and cells. Dev. Genet. 18, 173–179
Yuan, Q., Zhu, X., Sayre, L.M. (2007) Chemical nature of stochastic generation of protein-based carbonyls: metal-catalyzed oxidation versus modification by products of lipid oxidation. Chem. Res. Toxicol. 20, 129–139
Zheng, J., Mutcherson, R., Helfand, S.L. (2005) Calorie restriction delays lipid oxidative damage in Drosophila melanogaster. Aging Cell 4, 209–216
Acknowledgments
This work was supported by CMRPD 190631 grant from Chang Gung Memorial Hospital, Taiwan.
Author information
Authors and Affiliations
Corresponding author
Additional information
Modifications des molécules liées à l’âge dans les trophocytes et les cellules adipeuses des reines d’abeilles ( Apis mellifera )
Vieillissement/ trophocyte / cellule adipeuse / reine / abeille
Altersabhängige molekulare Veränderungen im Fettkörper von Königinnen der Honigbiene ( Apis mellifera )
Alterung / Trophozyten / Fettzelle / Königin / Honigbiene
Manuscript editor: David Tarpy
Rights and permissions
About this article
Cite this article
Hsieh, YS., Hsu, CY. The changes of age-related molecules in the trophocytes and fat cells of queen honeybees (Apis mellifera). Apidologie 42, 728–739 (2011). https://doi.org/10.1007/s13592-011-0085-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13592-011-0085-x