[go: up one dir, main page]
More Web Proxy on the site http://driver.im/ Skip to main content
Log in

The changes of age-related molecules in the trophocytes and fat cells of queen honeybees (Apis mellifera)

  • Original article
  • Published:
Apidologie Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
£29.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (United Kingdom)

Instant access to the full article PDF.

Figure 1.
Figure 2.
Figure 3.
Figure 4.
Figure 5.

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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Brunk, U.T., Terman, A. (2002) Lipofuscin: Mechanisms of age-related accumulation and influence on cell functions. Free Radic. Biol. Med. 33, 611–619

    Article  PubMed  CAS  Google Scholar 

  • Camazine, S. (1991) Self-organizing pattern formation on the combs of honey bee colonies. Behav. Ecol. Sociobiol. 28, 61–76

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Draper, H.H., Hadley, M. (1990) Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol. 86, 421–431

    Article  Google Scholar 

  • Draper, H.H., McGirr, L.G., Hadley, M. (1986) The metabolism of malondialdehyde. Lipids 21, 305–307

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hsieh, Y.S., Hsu, C.Y. (2011) Honeybee trophocytes and fat cells as target cells for cellular senescence studies. Exp. Gerontol. 46, 233–240

    Google Scholar 

  • Hsu, C.Y. (2004) The processes of iron deposition in the common hornet (Vespa affinis). Biol. Cell 96, 529–537

    Article  PubMed  CAS  Google Scholar 

  • Hsu, C.Y., Chiu, Y.C. (2009) Ambient temperature influences aging in an annual fish (Nothobranchius rachovii). Aging Cell 8, 726–737

    Article  PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Inal, M.E., Kanbak, G., Sunal, E. (2001) Antioxidant enzyme activities and malondialdehyde levels related to aging. Clin. Chim. Acta 305, 75–80

    Article  PubMed  CAS  Google Scholar 

  • Jemielity, S., Keller, L. (2007) Aging: a young mind in old bees. Curr. Biol. 17, R294–R295

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Lorite, P., Carrillo, J.A., Palomeque, T. (2002) Conservation of (TTAGG)n Telomeric sequences among ants (Hymenoptera, Formicidae). J. Hered. 93, 282–285

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Nakano, M., Oenzil, F., Mizuno, T., Gotoh, S. (1995) Age-related changes in the lipofuscin accumulation of brain and heart. Gerontology 41, 69–79

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Neukirch, A. (1982) Dependence of the lifespan of the honeybee (Apis mellifera) upon flight performance and energy consumption. J. Comp. Physiol. 146, 35–40

    CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Omholt, S.W., Amdam, G.V. (2004) Epigenic regulation of aging in honeybee workers. Aging Knowl. Environ. 26, pe28

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Ozawa, T. (1997) Genetic and functional changes in mitochondria associated with aging. Physiol. Rev. 77, 425–464

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Remolina, S.C., Hughes, K.A. (2008) Evolution and mechanisms of long life and high fertility in queen honey bees. Age 30, 177–185

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Richter, C. (1995) Oxidative damage to mitochondrial DNA and its relationship to ageing. Int. J. Biochem. Cell Biol. 27, 647–653

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Rueppell, O., Christine, S., Mulcrone, C., Groves, L. (2007a) Aging without functional senescence in honey bee workers. Curr. Biol. 17, R274–R275

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Sahara, K., Marec, F., Traut, W. (1999) TTAGG telomeric repeats in chromosomes of some insects and other arthropods. Chromosome Res. 7, 449–460

    Article  PubMed  CAS  Google Scholar 

  • Sasaki, T., Fujiwara, H. (2000) Detection and distribution patterns of telomerase activity in insects. Eur. J. Biochem. 267, 3025–3031

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Tofilski, A. (2000) Senescence and learning in honeybee (Apis mellifera) workers. Acta Neurobiol. Exp. 60, 35–39

    CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Weirich, G.F., Collins, A.M., Williams, V.P. (2002) Antioxidant enzymes in the honey bee, Apis mellifera. Apidologie 33, 3–14

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Winston, M.L. (1987) The biology of the honey bee. Harvard University Press, Cambridge, MA

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Zheng, J., Mutcherson, R., Helfand, S.L. (2005) Calorie restriction delays lipid oxidative damage in Drosophila melanogaster. Aging Cell 4, 209–216

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by CMRPD 190631 grant from Chang Gung Memorial Hospital, Taiwan.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Chin-Yuan Hsu.

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

Reprints 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

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13592-011-0085-x

Keywords

Navigation