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Energy-regulated molecules maintain young status in the trophocytes and fat cells of old queen honeybees

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Abstract

Queen honeybees (Apis mellifera) have much longer lifespans than worker bees. Energy-regulated molecules in the trophocytes and fat cells of workers during aging have been determined, but are unknown in queen bees. In the present study, energy-regulated molecules were evaluated in the trophocytes and fat cells of young and old queen bees. Adenosine monophosphate-activated protein kinase α2 (AMPK-α2), phosphorylated AMPK-α2 (pAMPK-α2), and cAMP-specific phosphodiesterases activity increased with aging. The pAMPK-α2/AMPK-α2 ratio and AMPK activity; adenosine triphosphate (ATP), adenosine diphosphate (ADP), and adenosine monophosphate (AMP) concentrations; the ADP/ATP ratio and the AMP/ATP ratio; the cyclic adenosine monophosphate concentration; forkhead box protein O expression; Silent information regulator T1 (SirT1) expression and activity; and peroxisome proliferator-activated receptor-α (PPAR-α) expression were not significantly different between young and old queen bees. These results show that energy-regulated molecules maintain a youthful status in the trophocytes and fat cells of queen bees during aging. These cells seem to have longevity-promoting mechanisms and may clarify the secret of longevity in queen bees.

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Abbreviations

AMPK:

AMP-activated protein kinase

pAMPK:

Phosphorylated AMP-activated protein kinase

cAMP:

Cyclic adenosine monophosphate

PDE:

cAMP-specific phosphodiesterases

ATP:

Adenosine triphosphate

ADP:

Adenosine diphosphate

AMP:

Adenosine monophosphate

FoxO:

Forkhead box protein O

SirT1:

Silent information regulator T1

PPAR-α:

Peroxisome proliferator-activated receptor-α

∆ψm:

Mitochondrial membrane potential

NAD+ :

Nicotinamide adenine dinucleotide oxidized form

NADH:

Nicotinamide adenine dinucleotide reduced form

ND1:

NADH dehydrogenase 1

ATR:

Ambient temperature reduction

CR:

Caloric restriction

LKB1:

Liver kinase B1

References

  • Apfeld J, O’Connor G, McDonagh T, DiStefano PS, Curtis R (2004) The AMP-activated protein kinase AAK-2 links energy levels and insulin-like signals to lifespan in C. elegans. Genes Dev 18:3004–3009

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Barthel A, Schmoll D, Kruger KD, Roth RA, Joost HG (2002) Regulation of the forkhead transcription factor FKHR (FOXO1a) by glucose starvation and AICAR, an activator of AMP-activated protein kinase. Endocrinology 143:3183–3186

    Article  CAS  PubMed  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:e19194

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Brys K, Castelein N, Matthijssens F, Vanfleteren JR, Braeckman BP (2010) Disruption of insulin signaling preserves bioenergetic competence of mitochondria in ageing Caenorhabditis elegans. BMC Biol 8:91

    Article  PubMed Central  PubMed  Google Scholar 

  • Cantó C, Auwerx J (2009) Caloric restriction, SIRT1 and longevity. Trends Endocrinol Metab 20:325–331

    Article  PubMed Central  PubMed  Google Scholar 

  • Cantó C, Gerhart-Hines Z, Feige JN, Lagouge M, Norieqa L, Milne JC, Elliott PJ, Puiqserver P, Auwerx J (2009) AMPK regulates energy expenditure by modulating NAD + metabolism and SIRT1 activity. Nature 458:1056–1060

    Article  PubMed Central  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 Central  PubMed  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 

  • Edwards AG, Donato AJ, Lesniewski LA, Gioscia RA, Seals DR, Moore RL (2010) Life-long caloric restriction elicites pronounced protection of the aged myocardium: a role for AMPK. Mech Ageing Dev 131:739–742

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ferrara N, Rinaldi B, Corbi G, Conti V, Stioso P, Boccuti S, Renqo G, Rossi F, Filippelli A (2008) Exercise training promotes SIRT1 activity in aged rats. Rejuvenation Res 11:139–150

    Article  CAS  PubMed  Google Scholar 

  • Forn J, Schonhofer PS, Skidmore IF, Krishna G (1970) Effect of aging on the adenyl cyclase and phosphodiesterase activity of isolated fat cells of rat. Biochim Biophys Acta 208:304–309

    Article  CAS  PubMed  Google Scholar 

  • Greer EC, Oskoui PR, Banko MR, Maniar JM, Gygi MP, Gygi SP, Brunet A (2007) The energy sensor AMP-activated protein kinase directly regulates the mammalian FOXO3 transcription factor. J Biol Chem 282:30107–30119

    Article  CAS  PubMed  Google Scholar 

  • Hardie DG (2004) The AMP-activated protein kinase pathway–new players upstream and downstream. J Cell Sci 117:5479–5487

    Article  CAS  PubMed  Google Scholar 

  • Hardie DG (2007) AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat Rev Mol Cell Biol 8:774–785

    Article  CAS  PubMed  Google Scholar 

  • Hardie DG (2011) AMP-activated protein kinase–an energy sensor that regulates all aspects of cell function. Genes Dev 25:1895–1908

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hardie DG, Ross FA, Hawley SA (2012) AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nature Rev 13:251–262

    Article  CAS  Google Scholar 

  • Hawley SA, Davison M, Woods A, Davies SP, Beri RK, Carling D, Hardie DG (1996) Characterization of the AMP-activated protein kinase kinase from rat liver and identification of threonine 172 as the major site at which it phosphorylates AMP-activated protein kinase. J Biol Chem 271:27879–27887

    Article  CAS  PubMed  Google Scholar 

  • Hayashida S, Arimoto A, Kuramoto Y, Kozako T, Honda SI (2010) Fasting promotes the expression of SIRT1, an NAD+-dependent protein deacetylase, via activation of PPARa in mice. Mol Cell Biochem 339:285–292

    Article  CAS  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  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 Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hsu CY, Chuang YL (2013) Changes in energy-regulated molecules in the trophocytes and fat cells of young and old worker honeybees (Apis mellifera). J Gerontol A Biol Sci Med Sci. doi:10.1093/gerona/glt163

    PubMed Central  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, 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 

  • Iemitsu M, Miyauchi T, Maeda S, Tanabe T, Takanashi M, Irukayama-Tomobe Y, Sakai S, Ohmori H, Matsuda M, Yamaguchi I (2002) Aging-induced decreased in the PPAR-a level in hearts is improved by exercise training. Am J Physiol Heart Circ Physiol 283:H1750–H1760

    CAS  PubMed  Google Scholar 

  • Jornayvaz FR, Shulman GI (2010) Regulation of mitochondrial biogenesis. Essays Biochem 47:69–84

    Article  CAS  PubMed  Google Scholar 

  • Kersten S, Seydoux J, Peters JM, Gonzalez FJ, Desvergne B, Wahli W (1999) Peroxisome proliferator-activated receptor alpha mediates the adaptive response to fasting. J Clin Invest 103:1489–1498

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lan F, Cacicedo JM, Ruderman N, Ido Y (2008) SIRT1 modulation of the acetylation status, cytosolic localization, and activity of LKB1. Possible role in AMP-activated protein kinase activation. J Biol Chem 283:27628–27635

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ljubicic V, Hood DA (2009) Diminished contraction-induced intracellular signaling towards mitochondrial biogenesis in aged skeletal muscle. Aging Cell 8:394–404

    Article  CAS  PubMed  Google Scholar 

  • Masternak MM, Bartke A (2007) PPARs in calorie restricted and genetically long-lived mice. PPAR Res 2007:28436

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 Central  PubMed  Google Scholar 

  • Park SJ, Ahmad F, Philp A, Baar K, Williams T, Luo H, Ke H, Rehmann H, Taussiq R, Brown AL, Kim MK, Beaven MA, Burgin AB, Manganiello V, Chung JH (2012) Resveratrol ameliorates aging-related metabolic phenotypes by inhibiting cAMP phosphodiesterases. Cell 148:421–433

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Planavila A, Iglesias R, Giralt M, Villarroya F (2011) Sirt1 acts in association with PPARα to protect the heart from hypertrophy, metabolic dysregulation, and inflammation. Cardiovasc Res 90:276–284

    Article  CAS  PubMed  Google Scholar 

  • Purushotham A, Schug TT, Xu Q, Surapureddi S, Guo X, Li X (2009) Hepatocyte-specific deletion of SIRT1 alters fatty acid metabolism and results in hepatic steatosis and inflammation. Cell Metab 9:327–338

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Qiang W, Weiqiang K, Qing Z, Pengju Z, Yi L (2007) Aging impairs insulin-stimulated glucose uptake in rat skeletal muscle via suppressing AMPKα. Exp Mol Med 39:535–543

    Article  CAS  PubMed  Google Scholar 

  • Reznick RM, Zong H, Li J, Morino K, Moore IK, Yu HJ, Liu ZX, Dong J, Mustard KJ, Hawley SA, Befroy D, Pypaert M, Hardie DG, Young LH, Shulman GI (2007) Aging-associated reductions in AMP-activated protein kinase activity and mitochondrial biogenesis. Cell Metab 5:151–156

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sanguino E, Roglans N, Alegret M, Sanchez RM, Vazquez-Carrera M, Laguna JC (2005) Atorvastatin reverses age-related reduction in rat hepatic PPARalpha and HNF-4. Br J Pharmacol 145:853–861

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schoeffter P, Stoclet JC (1990) Age-related differences in cyclic AMP metabolism and their consequences on relaxation induced by isoproterenol and phosphodiesterase inhibitors in rat isolated aorta. Mech Ageing Dev 54:197–205

    Article  CAS  PubMed  Google Scholar 

  • Schoonjans K, Staels B, Auwerx J (1996) The peroxisome proliferator activated receptors (PPARs) and their effects on lipid metabolism and adipocyte differentiation. Biochim Biophys Acta 1302:93–109

    Article  CAS  PubMed  Google Scholar 

  • Shinmura K, Tamaki K, Saito K, Nakano Y, Tobe T, Bolli R (2007) Cardioprotective effects of short-term caloric restriction are mediated by adiponectin via activation of AMP-activated protein kinase. Circulation 116:2809–2817

    Article  CAS  PubMed  Google Scholar 

  • Stancheva SL, Alova LG (1991) Age-related changes of cyclic AMP phosphodiesterase activity in rat brain regions and a new phosphodiesterase inhibitor-nootropic agent adafenoxate. Gen Pharmacol 22:955–958

    Article  CAS  PubMed  Google Scholar 

  • Turdi S, Fan X, Li J, Zhao J, Huff AF, Du M, Ren J (2010) AMP-activated protein kinase deficiency exacerbates aging-induced myocardial contractile dysfunction. Aging Cell 9:592–606

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang W, Yang X, Lopez de Silanes I, Carling D, Gorospe M (2003) Increased AMP:ATP ratio and AMP-activated protein kinase activity during cellular senescence linked to reduced HuR function. J Biol Chem 278:27016–28023

    Article  CAS  PubMed  Google Scholar 

  • Yang Q, Li Y (2007) Roles of PPARs on regulating myocardial energy and lipid homeostasis. J Mol Med 85:697–706

    Article  CAS  PubMed  Google Scholar 

  • Ye P, Wang ZJ, Zhang XJ, Zhao YL (2005) Age-related decrease in expression of peroxisome proliferator-activated receptor alpha and its effects on development of dyslipidemia. Chin Med J 118:1093–1098

    CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by a CMRPD 1A0493 grant from Chang Gung Memorial Hospital, Linkou, Taiwan.

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We have no conflicts of interest or disclosures.

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Authors and Affiliations

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

    Chin-Yuan Hsu

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

    Chin-Yuan Hsu & Ting-Hui Hu

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Correspondence to Chin-Yuan Hsu.

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Hsu, CY., Hu, TH. Energy-regulated molecules maintain young status in the trophocytes and fat cells of old queen honeybees. Biogerontology 15, 389–400 (2014). https://doi.org/10.1007/s10522-014-9509-0

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