Skip to main content

Advertisement

SpringerLink
Log in

Changes in mitochondrial energy utilization in young and old worker honeybees (Apis mellifera)

  • Published:
AGE Aims and scope Submit manuscript

Abstract

Trophocytes and fat cells in honeybees (Apis mellifera) have served as targets for cellular senescence studies, but mitochondrial energy utilization with advancing age in workers is unknown. In this study, mitochondrial energy utilization was evaluated in the trophocytes and fat cells of young and old workers reared in a field hive. The results showed that (1) mitochondrial density increased with advancing age; (2) mitochondrial membrane potential (∆Ψm), nicotinamide adenine dinucleotide oxidized form (NAD+) concentration, adenosine triphosphate (ATP) concentration, and NAD+/nicotinamide adenine dinucleotide reduced form (NADH) ratio decreased with advancing age; and (3) the expression of NADH dehydrogenase 1 (ND1), ATP synthase, and voltage-dependent anion channel 1 (VDAC1) increased with advancing age, whereas ND1 and ATP synthase did not differ with advancing age after normalization to mitochondrial density and VDAC1. These results show that the trophocytes and fat cells of young workers have higher mitochondrial energy utilization efficiency than those of old workers and that aging results in a decline in mitochondrial energy utilization in the trophocytes and fat cells of worker honeybees.

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

  • Allen RG, Tresini M, Keogh BP, Doggett DL, Cristofalo VJ (1999) Differences in electron transport potential, antioxidant defenses, and oxidant generation in young and senescent fetal lung fibroblasts (WI-38). J Cell Physiol 180:114–122

    Article  PubMed  CAS  Google Scholar 

  • Ames BN, Shigenaga MK, Hagen TM (1995) Mitochondrial decay in aging. Biochim Biophys Acta 1271:165–170

    Article  PubMed  Google Scholar 

  • Artal-Sanz M, Tavernarakis N (2008) Mechanisms of aging and energy metabolism in Caenorhabditis elegans. IUBMB Life 60:315–322

    Article  PubMed  CAS  Google Scholar 

  • Barrientos A, Casademont J, Cardellach F, Estivill X, Urbano-Marquez A, Nunes V (1997) Reduced steady-state levels of mitochondrial RNA and increased mitochondrial DNA amount in human brain with aging. Mol Brain Res 52:284–289

    Article  PubMed  CAS  Google Scholar 

  • Bartosz G, Grzelinska E, Wagner J (1982) Aging of the erythrocytes. XIV. ATP content does decrease. Experientia 38:575

    Article  PubMed  CAS  Google Scholar 

  • Braidy N, Guillemin GJ, Mansour H, Chan-Ling T, Poljak A, Grant R (2011) Age related changes in NAD+ metabolism oxidative stress and sirt1 activity in Wistar rats. PLoS One 6(4):e19194. doi:10.1371/journal.pone.0019194

    Article  PubMed  CAS  Google Scholar 

  • Chang J, Cornell JE, van Remmen H, Hakala K, Ward WF, Richardson A (2007) Effect of aging and caloric restriction on the mitochondrial proteome. J Gerontol A Biol Sci Med Sci 62:223–234

    Article  PubMed  Google Scholar 

  • Chanséaume E, Morio B (2009) Potential mechanisms of muscle mitochondrial dysfunction in aging and obesity and cellular consequences. Int J Mol Sci 10:306–324

    Article  PubMed  Google Scholar 

  • Choksi KB, Nuss JE, Boylston WH, Rabek JP, Papaconstantinou J (2007) Age-related increases in oxidatively damaged proteins of mouse kidney mitochondrial electron transport chain complexes. Free Radical Biol Med 43:1423–1438

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Collins AM, Williams V, Evans JD (2004) Sperm storage and antioxidative enzyme expression in the honey bee, Apis mellifera. Insect Mol Biol 13:141–146

    Article  PubMed  CAS  Google Scholar 

  • Conley KE, Jubrias SA, Esselman PC (2000) Oxidative capacity and ageing in human muscle. J Physiol 526:203–210

    Article  PubMed  CAS  Google Scholar 

  • Corona M, Hughes KA, Weaver DB, Robinson GE (2005) Gene expression patterns associated with queen honey bee longevity. Mech Ageing Develop 6:1230–1238

    Article  Google Scholar 

  • Cuervo AM, Bergamini E, Brunk UT, Drӧge W, Ffrench M, Terman A (2005) Autophagy and aging: the importance of maintaining “clean” cells. Autophagy 1:131–140

    Article  PubMed  Google Scholar 

  • Donoghue P, Staunton L, Mullen E, Manning G, Ohlendieck K (2010) DIGE analysis of rat skeletal muscle proteins using nonionic detergent phase extraction of young adult versus aged gastrocnemius tissue. J Proteomics 73:1441–1453

    Article  PubMed  CAS  Google Scholar 

  • Doran P, O'Connell K, Gannon J, Kavanagh M, Ohlendieck K (2008) Opposite pathobiochemical fate of pyruvate kinase and adenylate kinase in aged rat skeletal muscle as revealed by proteomic DIGE analysis. Proteomics 8:364–377

    Article  PubMed  CAS  Google Scholar 

  • Ferguson M, Mockett RJ, Shen Y, Orr WC, Sohal RS (2005) Age-associated decline in mitochondrial respiration and electron transport in Drosophila melanogaster. Biochem J 390:501–511

    Article  PubMed  CAS  Google Scholar 

  • Gadaleta MN, Rainaldi G, Lezza AMS, Milella F, Fracasso F, Cantatore P (1992) Mitochondrial DNA copy number and mitochondrial DNA deletion in adult and senescent rats. Mutat Res 275:181–193

    Article  PubMed  CAS  Google Scholar 

  • Gelfi C, Viganò A, Ripamonti M, Pontoglio A, Begum S, Pellegrino MA, Grassi B, Bottinelli R, Wait R, Cerretelli P (2006) The human muscle proteome in aging. J Proteome Res 5:1344–1353

    Article  PubMed  CAS  Google Scholar 

  • Guerrieri F, Vendemiale G, Turturro N, Fratello A, Furio A, Muolo L, Grattagliano I, Papa S (1996) Alteration of mitochondrial F0F1 ATP synthase during aging. Ann N Y Acad Sci 786:62–71

    Article  PubMed  CAS  Google Scholar 

  • Gurd BJ, Peters SJ, Heigenhauser GJ, LeBlanc PJ, Doherty TJ, Paterson DH, Kowalchuk JM (2008) O2 uptake kinetics, pyruvate dehydrogenase activity, and muscle deoxygenation in young and older adults during the transition to moderate-intensity exercise. Am J Physiol Regul Integr Comp Physiol 294:R577–R584

    Article  PubMed  CAS  Google Scholar 

  • Hagen TM, Yowe DL, Bartholomew JC, Wehr CM, Do KL, Park JY, Ames BN (1997) Mitochondrial decay in hepatocytes from old rats: membrane potential declines, heterogeneity and oxidants increase. Proc Natl Acad Sci USA 94:3064–3069

    Article  PubMed  CAS  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  PubMed  CAS  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 

  • Hsu CY, Chan YP (2011a) The use of honeybees reared in a thermostatic chamber for aging studies. Age. doi:10.1007/s11357-011-9344-z

  • Hsu CY, Chan YP (2011b) Identification and localization of proteins associated with biomineralization in the iron deposition vesicles of honeybees (Apis mellifera). PLoS One 6(4):e19088. doi:10.1371/journal.pone.0019088

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Imai S (2009) The NAD world: a new systemic regulatory network for metabolism and aging-Sirt1, systemic NAD biosynthesis, and their importance. Cell Biochem Biophys 53:65–74

    Article  PubMed  CAS  Google Scholar 

  • Jayachandran M, Karnicki K, Miller RS, Owen WG, Korach KS, Miller VM (2005) Platelet characteristics change with aging: role of estrogen receptor beta. J Gerontol A Biol Sci Med Sci 60:815–819

    Article  PubMed  Google Scholar 

  • Joo HJ, Ma JY, Choo YG, Choi BK, Jung KY (1999) Age-related alteration of intracellular ATP maintenance in the cell suspensions of mice cerebral cortex. Mech Aging Dev 110:1–12

    Article  PubMed  CAS  Google Scholar 

  • Kawano S, Tanimura H, Sato N, Nagano K, Tsuji S, Takei Y, Tsujii M, Hayashi N, Masuda E, Kashiwagi T, Fusamoto H, Kamada T (1991) Age-related change in human gastric mucosal energy metabolism. Scand J Gastroenterol 26:701–706

    Article  PubMed  CAS  Google Scholar 

  • Kokoszka JE, Coskup P, Esposito LA, Wallace DC (2001) Increased mitochondrial oxidative stress in the Sod2 (+/−) mouse results in the age-related decline of mitochondrial function culminating in increased apoptosis. Proc Natl Acad Sci USA 98:2278–2283

    Article  PubMed  CAS  Google Scholar 

  • Lee HC, Lu CY, Fahn HJ, Wei YH (1998) Aging- and smoking-associated alteration in the relative content of mitochondrial DNA in human lung. FEBS Lett 441:292–296

    Article  PubMed  CAS  Google Scholar 

  • Lee HC, Yin PH, Lu CY, Chi CW, Wei YH (2000) Increase of mitochondria and mitochondrial DNA in response to oxidative stress in human cells. Biochem J 348:425–432

    Article  PubMed  CAS  Google Scholar 

  • Lin SJ, Kaeberlein M, Andalis AA, Sturtz LA, Defossez PA, Culotta VC, Fink GR, Guarente L (2002) Calorie restriction extends Saccharomyces cerevisiae life span by increasing respiration. Nature 418:344–348

    Article  PubMed  CAS  Google Scholar 

  • López-Lluch G, Hunt N, Jones B, Zhu M, Jamieson H, Hilmer S, Cascajo MV, Allard J, Ingram DK, Navas P, de Cabo R (2006) Calorie restriction induces mitochondrial biogenesis and bioenergetic efficiency. Proc Natl Acad Sci USA 103:1768–1773

    Article  PubMed  Google Scholar 

  • López-Lluch G, Irusta PM, Navas P, de Cabo R (2008) Mitochondrial biogenesis and healthy aging. Exp Gerontol 43:813–819

    Article  PubMed  Google Scholar 

  • Martinez AO, Over D, Armstrong LS, Manzano L, Taylor R, Chambers J (1991) Separation of two populations of old human fibroblasts by mitochondria (rhodamine 123) fluorescence. Growth Dev Aging 55:185–191

    PubMed  CAS  Google Scholar 

  • Mizushima N, Yamamoto A, Matsui M, Yoshimori T, Ohsumi Y (2004) In vivo analysis of autophage in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell 15:1101–1111

    Article  PubMed  CAS  Google Scholar 

  • Napoleone P, Bronzetti E, Amenta F (1991) Enzyme histochemistry of aging rat kidney. Mech Ageing Dev 61:187–195

    Article  PubMed  CAS  Google Scholar 

  • Navarro A (2004) Mitochondrial enzyme activities as biochemical markers of aging. Mol Aspects Med 25:37–48

    Article  PubMed  CAS  Google Scholar 

  • Navarro A, Boveris A (2007) The mitochondrial energy transduction system and the aging process. Am J Physiol Cell Physiol 292:C670–C686

    Article  PubMed  CAS  Google Scholar 

  • Navarro A, Sánchez Del Pino MJ, Gomez C, Peralta JL, Boveris A (2002) Behavioral dysfunction, brain oxidative stress, and impaired mitochondrial electron transfer in aging mice. Am J Physiol Regul Integr Comp Physiol 282:R985–R992

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Nicholls DG (2004) Mitochondrial membrane potential and aging. Aging Cell 3:35–40

    Article  PubMed  CAS  Google Scholar 

  • Nicoletti VG, Tendi EA, Lalicata C, Reale S, Costa A, Villa RF, Ragusa N, Giuffrida Stella AM (1995) Changes of mitochondrial cytochrome c oxidase and F0F1 ATP synthase subunits in rat cerebral cortex during aging. Neurochem Res 20:1465–1470

    Article  PubMed  CAS  Google Scholar 

  • Papa S (1996) Mitochondrial oxidative phosphorylation changes in the life span. Molecular aspects and physiopathological implications. Biochim Biophys Acta 1276:87–105

    Article  PubMed  Google Scholar 

  • Passos JF, von Zglinicki T, Kirkwood TBL (2007) Mitochondria and ageing: winning and losing in the numbers game. BioEssays 29:908–917

    Article  PubMed  CAS  Google Scholar 

  • Petersen FK, Befroy D, Dufour S, Dziura J, Ariyan C, Rothman DL, DiPietro L, Cline GW, Shulman GI (2003) Mitochondrial dysfunction in the elderly: possible role in insulin resistance. Science 300:1140–1142

    Article  PubMed  CAS  Google Scholar 

  • Qin W, Yang T, Ho L, Zhao Z, Wang J, Chen L, Zhao W, Thiyagarajan M, MacGrogan D, Rodgers JT, Puigserver P, Sadoshima J, Deng H, Pedrini S, Gandy S, Sauve AA, Pasinetti GM (2006) Neuronal SIRT1 activation as a novel mechanism underlying the prevention of Alzheimer disease amyloid neuropathology by calorie restriction. J Biol Chem 281:21745–21754

    Article  PubMed  CAS  Google Scholar 

  • Ramsey KM, Mills KF, Satoh A, Imai S (2008) Age associated loss of Sirt1-mediated enhancement of glucose-stimulated insulin secretion in β cell-specific Sirt1-overexpressing (BESTO) mice. Aging Cell 7:78–88

    Article  PubMed  CAS  Google Scholar 

  • Remolina SC, Hafez DM, Robinson GE, Hughes KA (2007) Senescence in the worker honey bee Apis mellifera. J Insect Physiol 53:1027–1033

    Article  PubMed  CAS  Google Scholar 

  • Rottenberg H, Wu S (1997) Mitochondrial dysfunction in lymphocytes from old mice: Enhanced activation of the permeability transition. Biochem Biophys Res Commun 240:68–74

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Savitha S, Panneerselvam C (2006) Mitochondrial membrane damage during aging process in rat heart: potential efficacy of L-carnitine and DL α lipoic acid. Mech Ageing Dev 127:349–355

    Article  PubMed  CAS  Google Scholar 

  • Schippers MP, Dukas R, McClelland GB (2010) Lifetime- and caste-specific changes in flight metabolic rate and muscle biochemistry of honeybees, Apis mellifera. J Comp Physiol B 180:45–55

    Article  PubMed  CAS  Google Scholar 

  • Seehuus SC, Krekling T, Amdam GV (2006a) Cellular senescence in honey bee brain is largely independent of chronological age. Exp Gerontol 41:1117–1125

    Article  PubMed  CAS  Google Scholar 

  • Seehuus SC, Norberg K, Gimsa U, Krekling T, Amdam GV (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 

  • Son N, Hur HJ, Sung MJ, Kim MS, Hwang JT, Park JH, Yang HJ, Kwon DY, Yoon SH, Chung HY, Kim HJ (2012) Liquid chromatography-mass spectrometry-based metabolomic analysis of liver from aged rats. J Proteome Res 11:2551–2558

    Article  PubMed  CAS  Google Scholar 

  • Spodnik JH, Wozniak M, Budzko D, Teranishi M, Karbowski M, Nishizawa Y, Usukura J, Wakabayashi T (2002) Mechanism of leflunomide-induced proliferation of mitochondria in mammalian cells. Mitochondrion 2:163–179

    Article  PubMed  CAS  Google Scholar 

  • Suarez RK, Darveau CA, Welch KC, O'Brien DM, Roubik DW, Hochachka PW (2005) Energy metabolism in orchid bee flight muscle: carbohydrate fuels all. J Exp Biol 208:3573–3579

    Article  PubMed  CAS  Google Scholar 

  • Subasinghe W, Spence DM (2008) Simultaneous determination of cell aging and ATP release from erythrocytes and its implications in type 2 diabetes. Analytic Chimica Acta 618:227–233

    Article  CAS  Google Scholar 

  • Torres-Mendoza CE, Albert A, de la Cruz Arriaga MJ (1999) Molecular study of the rat liver NADH: cytochrome c oxidoreductase complex during development and aging. Mol Cell Biochem 195:133–142

    Article  PubMed  CAS  Google Scholar 

  • Trifunovic A, Larsson N-G (2008) Mitochondrial dysfunction as a cause of ageing. J Intern Med 263:167–178

    Article  PubMed  CAS  Google Scholar 

  • Vance JT, Williams JB, Elekonich MM, Roberts SP (2009) The effects of age and behavioral development on honey bee (Apis mellifera) flight performance. J Exp Biol 212:2604–2611

    Article  PubMed  Google Scholar 

  • Vázquez-Memije ME, Capin R, Tolosa A, El-Hafidi M (2008) Analysis of age-associated changes in mitochondrial free radical generation by rat testis. Mol Cell Biochem 307:23–30

    Article  PubMed  Google Scholar 

  • Ward MW, Rego AC, Frenguelli BG, Nicholls DG (2000) Mitochondrial membrane potential and glutamate excitotoxicity in cultured cerebellar granule cells. J Neurosci 20:7208–7219

    PubMed  CAS  Google Scholar 

  • Wei YH (1998) Oxidative stress and mitochondrial DNA mutations in human aging. Proc Soc Exp Biol Med 217:53–63

    Article  PubMed  CAS  Google Scholar 

  • Weirich GF, Collins AM, Williams VP (2002) Antioxidant enzymes in the honey bee, Apis mellifera. Apidologie 33:3–14

    Article  CAS  Google Scholar 

  • Wikowski JM, Micklem HS (1985) Decreased membrane potential of T lymphocytes in ageing mice: flow cytometric studies with a carbocyanine dye. Immunology 56:307–313

    Google Scholar 

  • Williams JB, Roberts SP, Elekonich MM (2008) Age and natural metabolically-intensive behavior affect oxidative stress and antioxidant mechanisms. Exp Gerontol 43:538–549

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Wredenberg A, Wibom R, Wilhelmsson H, Graff C, Wiener HH, Burden SJ, Oldfors A, Westerblad H, Larsson NG (2002) Increased mitochondrial mass in mitochondrial myopathy mice. Proc Natl Acad Sci USA 99:15066–15071

    Article  PubMed  CAS  Google Scholar 

  • Xu D, Finkel T (2002) A role for mitochondria as potential regulators of cellular life span. Biochem Biophys Res Commun 294:245–248

    Article  PubMed  CAS  Google Scholar 

  • Yan LJ, Sohal RS (2000) Prevention of flight activity prolongs the life span of the housefly, Musca domestica, and attenuates the age-associated oxidative damage to specific mitochondrial proteins. Free Radic Biol Med 29:1143–1150

    Article  PubMed  CAS  Google Scholar 

  • Yarian CS, Rebrin I, Sohal RS (2005) Aconitase and ATP synthase are targets of malondialdehyde modification and undergo an age-related decrease in activity in mouse heart mitochondria. Biochem Biophys Res Commun 330:151–156

    Article  PubMed  CAS  Google Scholar 

  • Ziegler M, Niere M (2004) NAD+ surface again. Biochem J 382:e5–e6

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by a grant (CMRPD 1A0491) from Chang Gung Memorial Hospital, Taiwan.

Author information

Authors and Affiliations

  1. Department of Biomedical Sciences, College of Medicine, Chang Gung University, Tao-Yuan, Taiwan

    Chin-Yuan Hsu

  2. Graduate Institute of Biomedical Sciences, College of Medicine, Chang Gung University, Tao-Yuan, Taiwan

    Yu-Lung Chuang & Chin-Yuan Hsu

Authors
  1. Yu-Lung Chuang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chin-Yuan Hsu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Chin-Yuan Hsu.

About this article

Cite this article

Chuang, YL., Hsu, CY. Changes in mitochondrial energy utilization in young and old worker honeybees (Apis mellifera). AGE 35, 1867–1879 (2013). https://doi.org/10.1007/s11357-012-9490-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11357-012-9490-y

Keywords

Search

Navigation