Skip to main content
SpringerLink
Log in

Cellular degradation activity is maintained during aging in long-living queen bees

  • Research Article
  • Published:
Biogerontology Aims and scope Submit manuscript

Abstract

Queen honeybees (Apis mellifera) have a much longer lifespan than worker bees. Whether cellular degradation activity is involved in the longevity of queen bees is unknown. In the present study, cellular degradation activity was evaluated in the trophocytes and oenocytes of young and old queen bees. The results indicated that (i) 20S proteasome activity and the size of autophagic vacuoles decreased with aging, and (ii) there were no significant differences between young and old queen bees with regard to 20S proteasome expression or efficiency, polyubiquitin aggregate expression, microtubule-associated protein 1 light chain 3-II (LC3-II) expression, 70 kDa heat shock cognate protein (Hsc70) expression, the density of autophagic vacuoles, p62/SQSTM1 expression, the activity or density of lysosomes, or molecular target of rapamycin expression. These results indicate that cellular degradation activity maintains a youthful status in the trophocytes and oenocytes of queen bees during aging and that cellular degradation activity is involved in maintaining the longevity of queen bees.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Bandyopadhyay U, Kaushik S, Varticovski L, Cuervo AM (2008) The chaperone-mediated autophagy receptor organizes in dynamic protein complexes at the lysosomal membrane. Mol Cell Biol 28:5747–5763

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beedholm R, Clark BFC, Rattan SIS (2004) Mild heat stress stimulates 20S proteasome and its 11S activator in human fibroblasts undergoing aging in vitro. Cell Stress Chaperones 9:49–57

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bjørkøy G, Lamark T, Brech A, Outzen H, Perander M, Overvatn A, Stenmark H, Johansen T (2005) p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol 171:603–614

    Article  PubMed  PubMed Central  Google Scholar 

  • Bulteau AL, Petropoulos I, Friguet B (2000) Age-related alterations of proteasome structure and function in aging epidermis. Exp Gerontol 35:767–777

    Article  CAS  PubMed  Google Scholar 

  • Bulteau AL, Lundberg KC, Humphries KM, Sadek HA, Swzeda PA, Friguet B, Szweda LI (2001) Oxidative modification and inactivation of the proteasome during coronary occlusion/reperfusion. J Biol Chem 276:30057–30063

    Article  CAS  PubMed  Google Scholar 

  • Bulteau AL, Szweda LI, Friguet B (2002) Age-dependent decline in proteasome activity in the heart. Arch Biochem Biophys 397:298–304

    Article  CAS  PubMed  Google Scholar 

  • Caramés B, Taniguchi N, Otsuki S, Blanco FJ, Lotz M (2010) Autophagy is a protective mechanism in normal cartilage and its aging-related loss is linked with cell death and osteoarthritis. Arthritis Rheum 62:791–801

    Article  PubMed  PubMed Central  Google Scholar 

  • Carrard G, Dieu M, Raes M, Toussaint O, Friguet B (2003) Impact of aging on proteasome structure and function in human lymphocytes. Int J Biochem Cell Biol 35:728–739

    Article  CAS  PubMed  Google Scholar 

  • Chan QWT, Mutti NS, Foster LJ, Kocher SD, Amdam GV, Florian W (2011) The worker honeybee fat body proteome is extensively remodeled preceding a major life-history transition. PLoS One 6(9):e24794

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chuang YL, Hsu CY (2013) Changes in mitochondrial energy utilization in young and old worker honeybees (Apis mellifera). Age 35:1867–1879

    Article  CAS  PubMed  Google Scholar 

  • Ciechanover A (2005) Proteolysis: from the lysosome to ubiquitin and the proteasome. Nat Rev Mol Cell Biol 6:79–87

    Article  CAS  PubMed  Google Scholar 

  • Cristofalo VJ, Kabakjian J (1975) Lysosomal enzymes and aging in vitro: subcellular enzyme distribution and effect of hydrocortisone on cell life-span. Mech Ageing Dev 4:19–28

    Article  CAS  PubMed  Google Scholar 

  • Cuervo AM, Dice JF (2000a) When lysosomes get old. Exp Gerontol 35:119–131

    Article  CAS  PubMed  Google Scholar 

  • Cuervo AM, Dice JF (2000b) Regulation of Lamp2a levels in the lysosomal membrane. Traffic 1:570–583

    Article  CAS  PubMed  Google Scholar 

  • Cuervo AM, Dice JF (2000c) Age-related decline in chaperone-mediated autophagy. J Biol Chem 275:31505–31513

    Article  CAS  PubMed  Google Scholar 

  • Cui J, Bai XY, Shi S, Cui S, Hong Q, Cai G, Chen X (2012) Age-related changes in the function of autophagy in rat kidneys. Age 34:329–339

    Article  CAS  PubMed  Google Scholar 

  • De Priester W, Van Manen R, Knook DL (1984) Lysosomal activity in aging rat liver. II. Morphometry of acid phosphatase positive dense bodies. Mech Ageing Dev 26:205–216

    Article  PubMed  Google Scholar 

  • Del Roso A, Vittorini S, Cavallini G, Donati A, Gori Z, Masini M, Pollera M, Bergamini E (2003) Ageing-related changes in the in vivo function of rat liver macroautophagy and proteolysis. Exp Gerontol 38:519–527

    Article  PubMed  Google Scholar 

  • Dennis PB, Jaeschke A, Saitoh M, Fowler B, Kozma SC, Thomas G (2001) Mammalian TOR: a homeostatic ATP sensor. Science 294:1102–1105

    Article  CAS  PubMed  Google Scholar 

  • Ferrington DA, Husom AD, Thompson LV (2005) Altered proteasome structure, function and oxidation in aged muscle. FASEB J 19:644–646

    CAS  PubMed  Google Scholar 

  • Giorgio M, Trinei M, Migliaccio E, Pelicci PG (2007) Hydrogen peroxide: a metabolic by-product or a common mediator of ageing signals? Nat Rev Mol Cell Biol 8:722–728

    Article  CAS  PubMed  Google Scholar 

  • Hansen TØ, Sarup P, Loeschcke V, Rattan SIS (2012) Age-related and sex-specific differences in proteasome activity in individual Drosophila flies from wild type, longevity-selected and stress resistant strains. Biogerontology 13:429–438

    Article  PubMed  Google Scholar 

  • Hsieh YS, Hsu CY (2011a) Honeybee trophocytes and fat cells as target cells for cellular senescence studies. Exp Gerontol 46:233–240

    Article  CAS  PubMed  Google Scholar 

  • Hsieh YS, Hsu CY (2011b) The changes of age-related molecules in the trophocytes and fat cells of queen honeybees (Apis mellifera). Apidologie 42:728–739

    Article  CAS  Google Scholar 

  • Hsieh YS, Hsu CY (2013) Oxidative stress and anti-oxidant enzyme activities in the trophocytes and fat cells of queen honeybees (Apis mellifera). Rejuvenation Res 16:295–303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hsu CY, Chan YP (2013) The use of honeybees reared in a thermostatic chamber for aging studies. Age 35:149–158

    Article  PubMed  Google Scholar 

  • Hsu CY, Chuang YL (2014) Changes in energy-regulated molecules in the trophocytes and fat cells of young and old worker honeybees (Apis mellifera). J Gerontol A 69:955–964

    Article  CAS  Google Scholar 

  • Hsu CY, Hsieh YS (2014) Oxidative stress decreases in the trophocytes and fat cells of worker honeybees during aging. Biogerontology 15:129–137

    Article  CAS  PubMed  Google Scholar 

  • Hsu CY, Hu TH (2014) Energy-regulated molecules maintain young status in the trophocytes and fat cells of old queen honeybees. Biogerontology 15:389–400

    Article  CAS  PubMed  Google Scholar 

  • Hsu CY, Lu CY (2015) Mitochondrial energy utilization maintains young status in the trophocytes and oenocytes of old queen honeybees. Apidologie 46:583–594

    Article  CAS  Google Scholar 

  • Hsu CY, Chuang YL, Chan YP (2014) Changes in cellular degradation activity in young and old worker honeybees (Apis mellifera). Exp Gerontol 50:128–136

    Article  CAS  PubMed  Google Scholar 

  • Husom AD, Peters EA, Kolling EA, Fugere NA, Thompson LV, Ferrington DA (2004) Altered proteasome function and subunit composition in aged muscle. Arch Biochem Biophys 421:67–76

    Article  CAS  PubMed  Google Scholar 

  • Inoki K, Zhu T, Guan K-L (2003) TSC2 mediates cellular energy response to control cell growth and survival. Cell 115:577–590

    Article  CAS  PubMed  Google Scholar 

  • Johnson ES, Bartel B, Seufert W, Varshavsky A (1992) Ubiquitin as a degradation signal. EMBO J 11:497–505

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 19:5720–5728

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keller JN, Huang FF, Markesbery WR (2000) Decreased levels of proteasome activity and proteasome expression in aging spinal cord. Neuroscience 98:149–156

    Article  CAS  PubMed  Google Scholar 

  • Lu CY, Hsu CY (2015) Ambient temperature reduction extends lifespan via activating cellular degradation activity in an annual fish (Nothobranchius rachovii). Age 37:33. doi:10.1007/s11357-015-9775-z

    Article  PubMed  PubMed Central  Google Scholar 

  • Madeo F, Tavernarakis N, Kroemer G (2010) Can autophagy promote longevity? Nat Cell Biol 12:842–846

    Article  CAS  PubMed  Google Scholar 

  • Maiuri MC, Zalckvar E, Kimchi A, Kroemer G (2007) Selfeating and self-killing: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol 8:741–752

    Article  CAS  PubMed  Google Scholar 

  • Majeski AE, Dice JF (2004) Mechanisms of chaperone-mediated autophagy. Int J Biochem Cell Biol 36:2435–2444

    Article  CAS  PubMed  Google Scholar 

  • Martinez-Vicente M, Sovak G, Cuervo AM (2005) Protein degradation and aging. Exp Gerontol 40:622–633

    Article  CAS  PubMed  Google Scholar 

  • McMulen CA, Ferry AL, Gamboa JL, Andrade FH, Dupont-Versteegden EE (2009) Age-related changes of cell death pathways in rat extraocular muscle. Exp Gerontol 44:420–425

    Article  PubMed Central  Google Scholar 

  • Morse RA, Flottum K (1990) The ABC & XYZ of bee culture. In: An encyclopedia pertaining to the scientific and practical culture of honey bees, 40th edn. The A. I. Root Co, Ohio. Page, p 387–392

  • Nilsen KA, Ihle KE, Frederick K, Fondrk MK, Smedal B, Hartfelder K, Amdam GV (2011) Insulin-like peptide genes in honey bee fat body respond differently to manipulation of social behavioral physiology. J Exp Biol 214:1488–1497

    Article  PubMed  PubMed Central  Google Scholar 

  • Ohtsuka H, Takahashi R, Goto S (1995) Age-related accumulation of high-molecular-weight ubiquitin protein conjugates in mouse brains. J Gerontol A 50A:B277–B281

    Article  CAS  Google Scholar 

  • Omholt SW, Amdam GV (2004) Epigenic regulation of aging in honeybee workers. Aging Knowl Environ 26:pe28

    Google Scholar 

  • Page RE, Peng CYS (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 

  • Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, Outzen H, Øvervatn A, Bjørkøy G, Johansen T (2007) p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem 282:24131–24145

    Article  CAS  PubMed  Google Scholar 

  • Petropoulos I, Conconi M, Wang X, Hoenel B, Brégégère F, Milner Y, Friguet B (2000) Increase of oxidatively modified protein is associated with decrease of proteasome activity and content in aging epidermal cells. J Gerontol A 55:220–227

    Article  Google Scholar 

  • Ponnappan U, Zhong M, Trebilcock GU (1999) Decreased proteasome mediated degradation in T cells from the elderly: a role in immune senescence. Cell Immunol 192:167–174

    Article  CAS  PubMed  Google Scholar 

  • Remolina SC, Hughes KA (2008) Evolution and mechanisms of long life and high fertility in queen honey bees. Age 30:177–185

    Article  PubMed  PubMed Central  Google Scholar 

  • Rueppell O, Bachelier C, Fondrk MK, Page RE Jr (2007) Regulation of life history determines lifespan of worker honey bees (Apis mellifera L.). Exp Gerontol 42:1020–1032

    Article  PubMed  PubMed Central  Google Scholar 

  • Shibatani T, Nazir M, Ward WF (1996) Alteration of rat liver 20S proteasome activities by age and food restriction. J Gerontol A 51:B316–B322

    Article  CAS  Google Scholar 

  • Sitte N, Huber M, Grune T, Ladhoff A, Doecke WD, Von Zglinicki T, Davies KJ (2000a) Proteasome inhibition by lipofuscin/ceroid during post-mitotic aging of fibroblasts. FASEB J 14:1490–1498

    Article  CAS  PubMed  Google Scholar 

  • Sitte N, Merker M, von Zglinicki T, Davies KJA, 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  PubMed  Google Scholar 

  • Taneike M, Yamaguchi O, Nakai A, Hikoso S, Takeda T, Mizote I, Oka T, Tamai T, Oyabu J, Murakawa T, Nishida K, Shimizu T, Hori M, Komuro I, Shirasawa T, Mizushima N, Otsu K (2010) Inhibition of autophagy in the heart induces age-related cardiomyopathy. Autophagy 6:600–606

    Article  CAS  PubMed  Google Scholar 

  • Van Manen R, De Priester W, Knook DL (1983) Lysosomal activity in aging rat liver. I. Variation in enzyme activity within the liver lobule. Mech Ageing Dev 22:159–165

    Article  PubMed  Google Scholar 

  • Veal EA, Day AM, Morgan BA (2007) Hydrogen peroxide sensing and signaling. Mol Cell 26:1–14

    Article  CAS  PubMed  Google Scholar 

  • Verdugo ME, Ray J (1997) Age-related increase in activity of specific lysosomal enzymes in the human retinal pigment epithelium. Exp Eye Res 65:231–240

    Article  CAS  PubMed  Google Scholar 

  • Viteri G, Carrard G, Birlouez-Aragon I, Silva E, Friguet B (2004) Age dependent protein modifications and declining proteasome activity in human lens. Arch Biochem Biophys 427:197–203

    Article  CAS  PubMed  Google Scholar 

  • Wang QJ, Ding Y, Kohtz DS, Mizushima N, Cristea IM, Rout MP, Chait BT, Zhong Y, Heintz N, Yue Z (2006) Induction of autophagy in axonal dystrophy and degeneration. J Neurosci 26:8057–8068

    Article  CAS  PubMed  Google Scholar 

  • Wolf DH, Hilt W (2004) The proteasome: a proteolytic nanomachine of cell regulation and waste disposal. Biochim Biophys Acta 1695:19–31

    Article  CAS  PubMed  Google Scholar 

  • Yoon J, Kim KJ, Choi YW, Shin HS, Kim YH, Min J (2010) The dependence of enhanced lysosomal activity on the cellular aging of bovine aortic endothelial cells. Mol Cell Biochem 340:175–178

    Article  CAS  PubMed  Google Scholar 

  • Zhang C, Cuervo AM (2008) Restoration of chaperone-mediated autophagy in aging liver improves cellular maintenance and hepatic function. Nat Med 14:959–965

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou L, Cai G, Liu F, Fu B, Liu W, Hong Q, Ma Q, Peng Y, Wang J, Chen X (2009) Expression and mechanism of mammalian target of rapamycin in age-related renal cell senescence and organ aging. Mech Aging Dev 130:700–708

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by Grants (CMRPD1C0081, CMRPD180353, CMRPD190631, CRRPG3D0051, CMRPD1E0021, CMRPD1E0381, and CMRPD1E0022) from Chang Gung Memorial Hospital, Linkou, Taiwan.

Author information

Authors and Affiliations

  1. Department of Biomedical Sciences, College of Medicine, Chang Gung University, 259 Wen-Hwa 1st Road, Kwei-Shan, Taoyuan, 333, Taiwan

    Chin-Yuan Hsu & Jiantai Timothy Qiu

  2. Graduate Institute of Biomedical Sciences, College of Medicine, Chang Gung University, Taoyuan, Taiwan

    Chin-Yuan Hsu, Jiantai Timothy Qiu & Yu-Pei Chan

  3. Department of Obstetrics and Gynecology, Chang Gung Memorial Hospital, Linkou, Taiwan

    Chin-Yuan Hsu & Jiantai Timothy Qiu

Authors
  1. Chin-Yuan Hsu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jiantai Timothy Qiu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yu-Pei Chan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Chin-Yuan Hsu.

Ethics declarations

Conflict of interest

The authors declare that no competing financial interests exist.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hsu, CY., Qiu, J.T. & Chan, YP. Cellular degradation activity is maintained during aging in long-living queen bees. Biogerontology 17, 829–840 (2016). https://doi.org/10.1007/s10522-016-9652-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10522-016-9652-x

Keywords

Search

Navigation