Age-related learning deficits can be reversible in honeybees Apis mellifera

Experimental Gerontology

Volumn 47, Issue 10, 2012, Pages 764-772

  Baker, Nicholas ^a   Wolschin, Florian ^a,b   Amdam, Gro V ^a,b  

^a ARIZONA STATE UNIVERSITY   (United States)

^b NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

Author keywords

Brain senescence; Cytochrome P450; Heat shock protein 8; LC MS2 proteomics; Pavlovian learning; Peroxiredoxin; Recovery related plasticity

Indexed keywords

ACTIN; ADENOSINE TRIPHOSPHATASE; ADENYLATE KINASE; ALDO KETO REDUCTASE; CYTOCHROME P450 REDUCTASE; FATTY ACID BINDING PROTEIN; GLUTAMATE TRANSPORTER; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 8; OXIDOREDUCTASE; PEROXIREDOXIN; TUBULIN; TUBULIN ALPHA 3; UNCLASSIFIED DRUG;

AGE DISTRIBUTION; AGED; AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN LEVEL; CONTROLLED STUDY; FORAGE; HONEYBEE; LEARNING; LEARNING DISORDER; LIQUID CHROMATOGRAPHY; MENTAL PERFORMANCE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; SENSATION; STRESS; TANDEM MASS SPECTROMETRY;

AGING; ANALYSIS OF VARIANCE; ANIMALS; BEES; BEHAVIOR, ANIMAL; BRAIN CHEMISTRY; CONDITIONING (PSYCHOLOGY); DISCRIMINATION LEARNING; PROTEOME; RECOVERY OF FUNCTION; SMELL; TASTE PERCEPTION;

ANIMALIA; APIS MELLIFERA; APOIDEA;

EID: 84865764277     PISSN: 05315565     EISSN: 18736815     Source Type: Journal    
DOI: 10.1016/j.exger.2012.05.011     Document Type: Article

References (75)

1. Amdam, G.V., in press. Social modulation of aging - mechanisms, ecology, evolution. Ann. Rev. Ent. 58, xxx-xxx.
2. Amdam G.V., Omholt S.W. The regulatory anatomy of honeybee lifespan. J. Theor. Biol. 2002, 216:209-228.
3. Amdam G.V., Aase A.L.T.O., Seehuus S.C., Norberg K., Hartfelder K., Fondrk M.K. Social reversal of immunosenescence in honey bee workers. Exp. Gerontol. 2005, 40:939-947.
4. Amdam G.V., Norberg K., Page R.E., Erber J., Scheiner R. Downregulation of vitellogenin gene activity increases the gustatory responsiveness of honey bee workers (Apis mellifera). Behav. Brain Res. 2006, 169:201-205.
5. Amdam G.V., Fennern E., Baker N., Rascon B. Honeybee associative learning performance and metabolic stress resilience are positively associated. PLoS One 2010, 5:e9740.
6. Banerjee Mustafi S., Chakraborty P.K., Dey R.S., Raha S. Heat stress upregulates chaperone heat shock protein 70 and antioxidant manganese superoxide dismutase through reactive oxygen species (ROS), p38MAPK, and Akt. Cell Stress Chaperones 2009, 14:579-589.
7. Behrends A., Scheiner R., Baker N., Amdam G.V. Cognitive aging is linked to social role in honey bees (Apis mellifera). Exp. Gerontol. 2007, 42:1146-1153.
8. Bell A.W., Deutsch E.W., Au C.E., Kearney R.E., Beavis R., Sechi S., Nilsson T., Bergeron J.J. A HUPO test sample study reveals common problems in mass spectrometry-based proteomics. Nat. Methods 2009, 6:423-430.
9. Bitterman M.E., Menzel R., Fietz A., Schäfer S. Classical conditioning of proboscis extension in honeybees (Apis mellifera). J. Comp. Physiol. 1983, 97:107-119.
10. Bradford M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
11. Broughton S., Partridge L. Insulin/IGF-like signalling, the central nervous system and aging. Biochem. J. 2009, 418:1-12.
12. Burke S.N., Barnes C.A. Neural plasticity in the ageing brain. Nat. Rev. Neurosci. 2006, 7:30-40.
13. Charles S.T., Carstensen L.L. Social and emotional aging. Annu. Rev. Psychol. 2010, 61:383-409.
14. Chung H., Sztal T., Pasricha S., Sridhar M., Batterham P., Daborn P.J. Characterization of Drosophila melanogaster cytochrome P450 genes. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:5731-5736.
15. Culwell T.F., Thulin C.D., Merrell K.J., Graves S.W. Influence of diet on the proteome of Drosophila melanogaster as assessed by two-dimensional gel electrophoresis and capillary liquid chromatography-mass spectrometry: the hamburger effect revisited. J. Biomol. Tech. 2008, 19:244-250.
16. Dukas R. Mortality rates of honey bees in the wild. Insectes Soc. 2008, 55:252-255.
17. Finch C.E. Longevity, Senescence and the Genome 1990, University of Chicago Press, Chicago.
18. Flatt T., Tu M.P., Tatar M. Hormonal pleiotropy and the juvenile hormone regulation of Drosophila development and life history. Bioessays 2005, 27:999-1010.
19. Goldman D., Ding J. Different regulatory elements are necessary for alpha1 tubulin induction during CNS development and regeneration. Neuroreport 2000, 11:3859-3863.
20. Grzyb J., Latowski D., Strzalka K. Lipocalins - a family portrait. J. Plant Physiol. 2006, 163:895-915.
21. Haddad L.S., Kelbert L., Hulbert A.J. Extended longevity of queen honey bees compared to workers is associated with peroxidation-resistant membranes. Exp. Gerontol. 2007, 42:601-609.
22. Haydak M.H. Age of nurse bees and brood rearing. Minn. Agric. Exp. Sta. Sci. J. Ser. 1963, 5122:101-103.
23. Hedlund E., Gustafsson J.A., Warner M. Cytochrome P450 in the brain; a review. Curr. Drug Metab. 2001, 2:245-263.
24. Huang Z.-Y., Robinson G.E. Regulation of honey bee division of labor by colony age demography. Behav. Ecol. Sociobiol. 1996, 39:147-158.
25. Hunt J.H., Wolschin F., Henshaw M.T., Newman T.C., Toth A.L., Amdam G.V. Differential gene expression and protein abundance evince ontogenetic bias toward castes in a primitively eusocial wasp. PLoS One 2010, 5:e10674.
26. Jagger C., Matthews R., Lindesay J., Robinson T., Croft P., Brayne C. The effect of dementia trends and treatments on longevity and disability: a simulation model based on the MRC Cognitive Function and Ageing Study (MRC CFAS). Age Ageing 2009, 38:319-325.
27. Kenyon C. The plasticity of aging: insights from long-lived mutants. Cell 2005, 120:449-460.
28. Kim K.C., Friso S., Choi S.W. DNA methylation, an epigenetic mechanism connecting folate to healthy embryonic development and aging. J. Nutr. Biochem. 2009, 20:917-926.
29. Kim K., Lee S.G., Kegelman T.P., Su Z.Z., Das S.K., et al. Role of excitatory amino acid transporter-2 (EAAT2) and glutamate in neurodegeneration: opportunities for developing novel therapeutics. J. Cell. Physiol. 2010, 226:2484-2493.
30. Kucharski R., Ball E.E., Hayward D.C., Maleszka R. Molecular cloning and expression analysis of a cDNA encoding a glutamate transporter in the honeybee brain. Gene 2000, 242:399-405.
31. Kuwabara M. Bildung des bedingten reflexes von Pavlovs typus bei der honigbiene, Apis mellifica. J. Fac. Sci. Hokkaido Univ. Ser. VI Zool. 1957, 13:458-464.
32. Martindale J.L., Holbrook N.J. Cellular response to oxidative stress: signaling for suicide and survival. J. Cell. Physiol. 2002, 192:1-15.
33. McEntee W.J., Crook T.H. Glutamate: its role in learning, memory, and the aging brain. Psychopharmacology 1993, 111:391-401.
34. Mey J., McCaffery P. Retinoic acid signaling in the nervous system of adult vertebrates. Neuroscientist 2004, 10:409-421.
35. Miksys S., Tyndale R.F. The unique regulation of brain cytochrome P450 2 (CYP2) family enzymes by drugs and genetics. Drug Metab. Rev. 2004, 36:313-333.
36. Miojevic B.D. A new interpretation of the social life of the honeybee. Bee World 1940, 21:39-41.
37. Münch D., Amdam G.V. The curious case of aging plasticity in honey bees. FEBS Lett. 2010, 584:2496-2503.
38. Münch D., Baker N., Kreibich C.D., Bråten A.T., Amdam G.V. In the laboratory and during free-flight: old honey bees reveal learning and extinction deficits that mirror mammalian functional decline. PLoS ONE 2010, 5:e13504.
39. Nelson F.C. Adaptability of young bees under adverse conditions. Am. Bee J. 1927, 67:242-243.
40. Nelson C.M., Ihle K., Amdam G.V., Fondrk M.K., Page R.E. The gene vitellogenin has multiple coordinating effects on social organization. PLoS Biol. 2007, 5:673-677.
41. Pankiw T., Page R.E. Effect of pheromones, hormones, and handling on sucrose response thresholds of honey bees (Apis mellifera L.). J. Comp. Physiol. A 2003, 189:675-684.
42. Power J.H., Asad S., Chataway T.K., Chegini F., Manavis J., et al. Peroxiredoxin 6 in human brain: molecular forms, cellular distribution and association with Alzheimer's disease pathology. Acta Neuropathol. 2008, 115:611-622.
43. Rappsilber J., Ishihama Y., Mann M. Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal. Chem. 2003, 75:663-670.
44. Remolina S.C., Hughes K.A. Evolution and mechanisms of long life and high fertility in queen honey bees. Age 2008, 30:177-185.
45. Robinson G.E., Page R.E., Strambi C., Strambi A. Colony integration in honey bees: mechanisms of behavioral reversion. Ethology 1992, 90:336-348.
46. Rohr M.K., Lang F.R. Aging well together-a mini-review. Gerontology 2009, 55:333-343.
47. Ruan H., Wu C.F. Social interaction-mediated lifespan extension of Drosophila Cu/Zn superoxide dismutase mutants. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:7506-7510.
48. Rueppell O., Bachelier C., Fondrk M.K., Page R.E. Regulation of life history determines lifespan of worker honey bees (Apis mellifera L.). Exp. Gerontol. 2007, 42:1020-1032.
49. Rueppell O., Christine S., Mulcrone C., Groves L. Aging without functional senescence in honey bee workers. Curr. Biol. 2007, 17:R274-R275.
50. Rueppell O., Kaftanoglu O., Page R.E. Honey bee (Apis mellifera) workers live longer in small than in large colonies. Exp. Gerontol. 2009, 44:447-452.
51. Savla G.N., Palmer B.W. Neuropsychology in Alzheimer's disease and other dementia research. Curr. Opin. Psychiatry 2005, 18:621-627.
52. Scheiner R., Amdam G.V. Impaired tactile learning is related to social role in honeybees. J. Exp. Biol. 2009, 212:994-1002.
53. Scheiner R., Erber J., Page R.E. Tactile learning and the individual evaluation of the reward in honey bees (Apis mellifera). J. Comp. Physiol. A 1999, 185:1-10.
54. Scheiner R., Page R.E., Erber J. The effects of genotype, foraging role, and sucrose responsiveness on the tactile learning performance of honey bees (Apis mellifera L.). Neurobiol. Learn. Mem. 2001, 76:138-150.
55. Seehuus S.C., Krekling T., Amdam G.V. Cellular senescence in the honey bee brain may be largely independent of chronological age. Exp. Gerontol. 2006, 41:1117-1125.
56. Seehuus S.C., Norberg K., Gimsa U., Krekling T., Amdam G.V. Reproductive protein protects sterile honey bee workers from oxidative stress. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:962-967.
57. Seeley T.D. Adaptive significance of the age polyethism schedule in honeybee colonies. Behav. Ecol. Sociobiol. 1982, 11:287-293.
58. Selkirk J.V., Stiefel T.H., Stone I.M., Naeve G.S., Foster A.C., Poulsen D.J. Over-expression of the human EAAT2 glutamate transporter within neurons of mouse organotypic hippocampal slice cultures leads to increased vulnerability of CA1 pyramidal cells. Eur. J. Neurosci. 2005, 21:2291-2296.
59. Small G.W. What we need to know about age related memory loss. BMJ 2002, 324:1502-1505.
60. Smith B.H. The olfactory memory of the honeybee Apis mellifera. I. Odorant modulation of short- and intermediate-term memory after single trial conditioning. J. Exp. Biol. 1991, 161:367-382.
61. Sorolla M.A., Reverter-Branchat G., Tamarit J., Ferrer I., Ros J., Cabiscol E. Proteomic and oxidative stress analysis in human brain samples of Huntington disease. Free Radic. Biol. Med. 2008, 45:667-678.
62. Tabb D.L., Vega-Montoto L., Rudnick P.A., Variyath A.M., Ham A.J., Bunk D.M., Kilpatrick L.E., Billheimer D.D., Blackman R.K., Cardasis H.L., et al. Repeatability and reproducibility in proteomic identifications by liquid chromatography-tandem mass spectrometry. J. Proteome Res. 2009, 9:761-776.
63. Tatar M. Can we develop genetically tractable models to assess healthspan (rather than lifespan) in animal models?. J. Gerontol. 2009, 64A:161-163.
64. Tofilski A. Senescence and learning in honeybee (Apis mellifera) workers. Acta Neurobiol. Exp. 2000, 60:35-39.
65. Vance J.T., Williams J.B., Elekonich M.M., Roberts S.P. The effects of age and behavioral development on honey bee (Apis mellifera) flight performance. J. Exp. Biol. 2009, 212:2604-2611.
66. Visscher P.K., Dukas R. Survivorship of foraging honey bees. Insectes Soc. 1997, 44:1-5.
67. Voos W. Mitochondrial protein homeostasis: the cooperative roles of chaperones and proteases. Res. Microbiol. 2009, 160:718-725.
68. Wan H., Rehngren M., Giordanetto F., Bergstrom F., Tunek A. High-throughput screening of drug-brain tissue binding and in silico prediction for assessment of central nervous system drug delivery. J. Med. Chem. 2007, 50:4606-4615.
69. Wessel D., Flugge U.I. A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal. Biochem. 1984, 138:141-143.
70. Winston M.L. The Biology of the Honey Bee 1987, Harvard University Press, Cambridge MA.
71. Wolschin F., Amdam G.V. Comparative proteomics reveal characteristics of life-history transitions in a social insect. Proteome Sci. 2007, 5:e10.
72. Wolschin F., Amdam G.V. Plasticity and robustness of protein patterns during reversible development in the honey bee (Apis mellifera). Anal. Bioanal. Chem. 2007, 389:1095-1100.
73. Wolschin F., Munch D., Amdam G.V. Structural and proteomic analyses reveal regional brain differences during honeybee aging. J. Exp. Biol. 2009, 212:4027-4032.
74. Wood Z.A., Schroder E., Robin Harris J., Poole L.B. Structure, mechanism and regulation of peroxiredoxins. Trends Biochem. Sci. 2003, 28:32-40.
75. Zayed A., Naeger N.L., Rodriguez-Zas S.L., Robinson G.E. Common and novel transcriptional routes to behavioral maturation in worker and male honey bees. Genes Brain Behav. 2012, 11:253-256.