Aggression is associated with aerobic glycolysis in the honey bee brain1

Genes, Brain and Behavior

Volumn 14, Issue 2, 2015, Pages 158-166

  Chandrasekaran, S ^a,b,g   Rittschof, C C ^c,d,e,h,i   Djukovic, D ^f   Gu, H ^f   Raftery, D ^f   Price, N D ^a,b   Robinson, G E ^c,d,e  

^a INSTITUTE FOR SYSTEMS BIOLOGY   (United States)

^b Center for Biophysics and Computational Biology   (United States)

^c Institute for Genomic Biology ^*  (United States)

^d Institute for Genomic Biology   (United States)

^e UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^f UNIVERSITY OF WASHINGTON   (United States)

^g BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^h HARVARD UNIVERSITY   (United States)

ⁱ PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Aerobic glycolysis; Aggression; Brain metabolism; Metabolomics; Neurogenomics; Transcriptomics

Indexed keywords

ADENOSINE TRIPHOSPHATE; NEUROTRANSMITTER; PHEROMONE; GLUCOSE;

ADULT; AEROBIC GLYCOLYSIS; AEROBIC METABOLISM; AGGRESSION; ANIMAL EXPERIMENT; APIS MELLIFERA; ARTICLE; ASSOCIATION; BRAIN; BRAIN FUNCTION; BRAIN METABOLISM; CONTROLLED STUDY; FEMALE; HONEYBEE; METABOLOMICS; MIDDLE AGED; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PRIORITY JOURNAL; TRANSCRIPTOMICS; ANIMAL; ANIMAL BEHAVIOR; BEE; GLYCOLYSIS; METABOLISM; MICROARRAY ANALYSIS; PHYSIOLOGY; PROCEDURES;

APIS MELLIFERA; APOIDEA;

ADENOSINE TRIPHOSPHATE; AGGRESSION; ANIMALS; BEES; BEHAVIOR, ANIMAL; BRAIN; GLUCOSE; GLYCOLYSIS; MICROARRAY ANALYSIS; PHEROMONES;

EID: 84925362347     PISSN: 16011848     EISSN: 1601183X     Source Type: Journal    
DOI: 10.1111/gbb.12201     Document Type: Article

References (42)

1. Agathocleous, M., Love, N.K., Randlett, O., Harris, J.J., Liu, J., Murray, A.J. & Harris, W.A. (2012) Metabolic differentiation in the embryonic retina. Nat Cell Biol 14, 859-864.
2. Alaux, C., Sinha, S., Hasadsri, L., Hunt, G.J., Guzman-Novoa, E., DeGrandi-Hoffman, G., Uribe-Rubio, J.L., Southey, B.R., Rodriguez-Zas, S. & Robinson, G.E. (2009) Honey bee aggression supports a link between gene regulation and behavioral evolution. Proc Natl Acad Sci USA 106, 15400-15405.
3. Barros, L.F. (2013) Metabolic signaling by lactate in the brain. Trends Neurosci 36, 396-404.
4. Bergersen, L.H. & Gjedde, A. (2012) Is lactate a volume transmitter of metabolic states of the brain? Front Neuroenergetics 4, 5.
5. Boy, F., Evans, C.J., Edden, R.A., Lawrence, A.D., Singh, K.D., Husain, M. & Sumner, P. (2011) Dorsolateral prefrontal gamma-aminobutyric acid in men predicts individual differences in rash impulsivity. Biol Psychiatry 70, 866-872.
6. Boyle, P.J., Scott, J.C., Krentz, A.J., Nagy, R.J., Comstock, E. & Hoffman, C. (1994) Diminished brain glucose metabolism is a significant determinant for falling rates of systemic glucose utilization during sleep in normal humans. J Clin Invest 93, 529.
7. Chandrasekaran, S., Ament, S.A., Eddy, J.A., Rodriguez-Zas, S.L., Schatz, B.R., Price, N.D. & Robinson, G.E. (2011) Behavior-specific changes in transcriptional modules lead to distinct and predictable neurogenomic states. Proc Natl Acad Sci USA 108, 18020-18025.
8. Cummings, M.E., Larkins-Ford, J., Reilly, C.R., Wong, R.Y., Ramsey, M. & Hofmann, H.A. (2008) Sexual and social stimuli elicit rapid and contrasting genomic responses. Proc R Soc B Biol Sci 275, 393-402.
9. El Hassani, A.K., Giurfa, M., Gauthier, M. & Armengaud, C. (2008) Inhibitory neurotransmission and olfactory memory in honeybees. Neurobiol Learn Mem 90, 589-595.
10. Ellis, L.L. & Carney, G.E. (2011) Socially-responsive gene expression in male Drosophila melanogaster is influenced by the sex of the interacting partner. Genetics 187, 157-169.
11. Fahrbach, S.E., Strande, J.L. & Robinson, G.E. (1995) Neurogenesis is absent in the brains of adult honey bees and does not explain behavioral neuroplasticity. Neurosci Lett 197, 145-148.
12. Fox, P.T., Raichle, M.E., Mintun, M.A. & Dence, C. (1988) Nonoxidative glucose consumption during focal physiologic neural activity. Science 241, 462-464.
13. Goyal, Manu S., Hawrylycz, M., Miller, Jeremy A., Snyder, Abraham Z. & Raichle, Marcus E. (2014) Aerobic glycolysis in the human brain is associated with development and neotenous gene expression. Cell Metab 19, 49-57.
14. Harrison, J.F. & Hall, H.G. (1993) African-European honeybee hybrids have low nonintermediate metabolic capacities. Nature 363, 258-260.
15. Herman, J.P., Mueller, N.K. & Figueiredo, H. (2004) Role of GABA and glutamate circuitry in hypothalamo-pituitary-adrenocortical stress integration. Ann N Y Acad Sci 1018, 35-45.
16. Jia, F., Yue, M., Chandra, D., Keramidas, A., Goldstein, P.A., Homanics, G.E. & Harrison, N.L. (2008) Taurine is a potent activator of extrasynaptic GABA(A) receptors in the thalamus. J Neurosci 28, 106-115.
17. Kanehisa, M., Araki, M., Goto, S., Hattori, M., Hirakawa, M., Itoh, M., Katayama, T., Kawashima, S., Okuda, S., Tokimatsu, T. & Yamanishi, Y. (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36, D480-484.
18. Li-Byarlay, H.R., Rittschof, C.C., Massey, J.H., Pittendrigh, B.R. & Robinson, G.E. (2014) Socially responsive effects of brain oxidative metabolism on aggression. Proc Natl Acad Sci USA 111, 12533-12537.
19. Lopez-Cocuera, B., Geerlings, A. & Aragon, C. (2001) Glycine neurotransmitter transporters: an update. Mol Membr Biol 18, 13-20.
20. Lunt, S.Y. & Vander Heiden, M.G. (2011) Aerobic glycolysis: meeting the metabolic requirements of cell proliferation. Annu Rev Cell Dev Biol 27, 441-464.
21. Macone, A., Fontana, M., Barba, M., Botta, B., Nardini, M., Ghirga, F., Calcaterra, A., Pecci, L. & Matarese, R.M. (2011) Antioxidant properties of aminoethylcysteine ketimine decarboxylated dimer: a review. Int J Mol Sci 12, 3072-3084.
22. Madsen, P.L., Hasselbalch, S.G., Hagemann, L.P., Olsen, K.S., Bulow, J., Holm, S., Wildschiodtz, G., Paulson, O.B. & Lassen, N.A. (1995) Persistent resetting of the cerebral oxygen/glucose uptake ratio by brain activation: evidence obtained with the Kety-Schmidt technique. J Cereb Blood Flow Metab 15, 485-491.
23. Mauro, C., Leow, S.C., Anso, E., Rocha, S., Thotakura, A.K., Tornatore, L., Moretti, M., De Smaele, E., Beg, A.A., Tergaonkar, V., Chandel, N.S. & Franzoso, G. (2011) NF-kappaB controls energy homeostasis and metabolic adaptation by upregulating mitochondrial respiration. Nat Cell Biol 13, 1272-1279.
24. Papandreou, I., Cairns, R.A., Fontana, L., Lim, A.L. & Denko, N.C. (2006) HIF-1 mediates adaptation to hypoxia by actively downregulating mitochondrial oxygen consumption. Cell Metab 3, 187-197.
25. Pfeiffer, T., Schuster, S. & Bonhoeffer, S. (2001) Cooperation and competition in the evolution of ATP-producing pathways. Science 292, 504-507.
26. Phelps, M.E. & Barrio, J.R. (2010) Correlation of brain amyloid with "aerobic glycolysis": a question of assumptions? Proc Natl Acad Sci USA 107, 17459-17460.
27. Powers, W.J., Videen, T.O., Markham, J., McGee-Minnich, L., Antenor-Dorsey, J.V., Hershey, T. & Perlmutter, J.S. (2007) Selective defect of in vivo glycolysis in early Huntington's disease striatum. Proc Natl Acad Sci USA 104, 2945-2949.
28. Prabakaran, S., Swatton, J.E., Ryan, M.M., Huffaker, S.J., Huang, J.T., Griffin, J.L., Wayland, M., Freeman, T., Dudbridge, F., Lilley, K.S., Karp, N.A., Hester, S., Tkachev, D., Mimmack, M.L., Yolken, R.H., Webster, M.J., Torrey, E.F. & Bahn, S. (2004) Mitochondrial dysfunction in schizophrenia: evidence for compromised brain metabolism and oxidative stress. Mol Psychiatry 9, 684-697, 643.
29. Ragland, G.J., Denlinger, D.L. & Hahn, D.A. (2010) Mechanisms of suspended animation are revealed by transcript profiling of diapause in the flesh fly. Proc Natl Acad Sci USA 107, 14909-14914.
30. Raichle, M.E., Posner, J.B. & Plum, F. (1970) Cerebral blood flow during. Arch Neurol 23, 394.
31. Sattler, R. & Tymianski, M. (2001) Molecular mechanisms of glutamate receptor-mediated excitotoxic neuronal cell death. Mol Neurobiol 24, 107-129.
32. Signorotti, L., Jaisson, P. & d'Ettorre, P. (2014) Larval memory affects adult nest-mate recognition in the ant Aphaenogaster senilis. Proc R Soc B Biol Sci 281, 20132579.
33. Stevenson, P.A., Dyakonova, V., Rillich, J. & Schildberger, K. (2005) Octopamine and experience-dependent modulation of aggression in crickets. J Neurosci 25, 1431-1441.
34. Tsacopoulos, M., Veuthey, A.L., Saravelos, S.G., Perrottet, P. & Tsoupras, G. (1994) Glial cells transform glucose to alanine, which fuels the neurons in the honeybee retina. J Neurosci 14, 1339-1351.
35. Vaishnavi, S.N., Vlassenko, A.G., Rundle, M.M., Snyder, A.Z., Mintun, M.A. & Raichle, M.E. (2010) Regional aerobic glycolysis in the human brain. Proc Natl Acad Sci 107, 17757-17762.
36. Vander Heiden, M.G., Cantley, L.C. & Thompson, C.B. (2009) Understanding the Warburg effect: the metabolic requirements of cell proliferation. Sci Signall 324, 1029.
37. Vlassenko, A.G., Vaishnavi, S.N., Couture, L., Sacco, D., Shannon, B.J., Mach, R.H., Morris, J.C., Raichle, M.E. & Mintun, M.A. (2010) Spatial correlation between brain aerobic glycolysis and amyloid-beta (Abeta) deposition. Proc Natl Acad Sci USA 107, 17763-17767.
38. Wang, T.A., Yu, Y.V., Govindaiah, G., Ye, X., Artinian, L., Coleman, T.P., Sweedler, J.V., Cox, C.L. & Gillette, M.U. (2012) Circadian rhythm of redox state regulates excitability in suprachiasmatic nucleus neurons. Science 337, 839-842.
39. Warburg, O. (1956) On the origin of cancer cells. Science 123, 309-314.
40. Wegener, G. (1988) Oxygen availability, energy metabolism, and metabolic rate in invertebrates and vertebrates. In Oxygen Sensing in Tissues. Springer, pp. 13-35.
41. Wnuk, A., Kostowski, W., Korczynska, J., Szczuka, A., Symonowicz, B., Bienkowski, P., Mierzejewski, P. & Godzinska, E.J. (2013) Brain GABA and glutamate levels in workers of two ant species (Hymenoptera: Formicidae): interspecific differences and effects of queen presence/absence. Insect Sci 21: 647-658.
42. Yang, J., Ruchti, E., Petit, J.M., Jourdain, P., Grenningloh, G., Allaman, I. & Magistretti, P.J. (2014) Lactate promotes plasticity gene expression by potentiating NMDA signaling in neurons. Proc Natl Acad Sci USA 111, 12228-12233.